TEXT-BOOKS OF ANIMAL BIOLOGY

*
Edited by JULIAN S. HUXLEY, F.R.S.
A General Zoology of the Invertebrates
by G. S. Carter
Vertebrate Zoology
by G. R. de Beer
Comparative Physiology
by L. T. Hogben
Animal Ecology
by Challes Elton
Life in Inland Waters
by Kathleen Carpenter
The Development of Sex in Vertebrates
by F. W. Rogers Brambell

Edited by H.
*
MUNRO Fox, F.R.S.
Animal
/
Evolution
by G. S. Carter
Zoogeography of the Land and Inland Waters
by L. F. de Beaufort
Parasitism and Symbiosis
by M. Caullery
PARASITISM
AND
~SYMBIOSIS

BY

MAURICE CAULLERY

Translated by Averil M. Lysaght, M.Sc., Ph.D.

SIDGWICK AND JACKSON LIMITED

LONDON
 First Published 1952

!.lADE AND PRINTED IN GREAT BRITAIN BY

WILLIAM CLOWES AND SONS, LlMITED, LONDON AND BECCLES
 CONTENTS

LIST OF ILLUSTRATIONS vii

PREFACE TO THE ENGLISH EDITION xi

CHAPTER I Commensalism
Introduction-commensalism in marine animals-fishes and sea
anemones-associations on coral reefs-widespread nature of
these relationships-hermit crabs and their associates

CHAPTER II Commensalism in Terrestrial

Animals
Commensals of ants and termites-morphological modifications
in symphiles-ants.and slavery-myrmecophilous plants . 16

CHAPTER III From Commensalism to

Inquilinism and Parasitism
Inquilinism-epizoites-intermittent parasites-general nature
of modifications produced by parasitism 30

CHAPTER IV Adaptations to Parasitism

in Annelids and Molluscs
Polychates-molluscs; lamellibranchs; gastropods 40
CHAPTER V Adaptation to Parasitism in
the Crustacea
Isopoda-families of Epicarida-Rhizocephala-Ascothoracica
-Copepoda 65

CHAPTER VI Temporary Parasitism

Monstrillida - Orthonectida - Eunicida - Unionida - Gor-
dian worms~entomophagous insects 108

CHAPTER VII Parasites which change their Host

Cestoda - Cestodaria - Trematoda - Nematoda - Acantho-
cephala-Pentastomida-Protozoa-parasitic plants 127
v
vi CONTENTS

CHAPTER VIII Adaptive Modifications in the

Reproduction of Parasites
Hermaphroditism and change 'Of sex-increase in egg numbers-
accessory reproductive phases-discussion 154

CHAPTER IX Specificity in Parasites and Modes

of Host Infestation
Strict specificity-modified specificity-trophic prophylaxis-host
parasite equilibrium-relative specificity-specificity and access
to the host-myiases-hereditary transmission 171

CHAPTER X Reciprocal Reactions of Parasite

and Host
Parasites and foreign bodies-phagocytosis in normal and
abnormal parasites-parasites and toxins-the effect of the
parasite on the general metabolism of the host-parasitic castra-
tion-special cases of reaction of hosts to parasites-gall forma-
tiM 1~

CHAPTER XI Symbiosis between Animals and Plants

Introduction-symbiosis in animals and plants-ectosymbiosis-
ants and fungi-termites and fungi-endosymbiosis-protozoa
and intestinal bacteria-termites and flagellates-ruminants and
infusoria-zoochlorella! and zooxanthella!-mycetomes of insects
-bloodsucking animals-animal luminescence-experimental
research on symbiosis 217

CHAPTER XII Symbiosis in Plants

Lichens-myxomycetes-myxobacteria-mycorrhiza 256

CHAPTER XIII Is Symbiosis a Primordial

Characteristic of the Cell ?
BIBLIOGRAPHY 277
INDEX 287
 LIST OF ILLUSTRATIONS

Aspidosiphon and Heteropsammia cochlea 6

2 Hermit crab in an artificial glass shell, with its commensal
Nereilepas Jucata coming out to take part in a meal of sea
urchin ovary 8
3 Association of Eupagurus prideauxi and Adamsia palliata. 11
4 Melia tesselata holding a sea anemone in each of its chela: 13
5 Insects that live as commensals with ants 20
6 Larva of Pachycondyla vorax bearing a larva of Metopina
pachycondyke 21
7 Head and mandibles of workers of Polyergus ruJescens and
of Formica Jusca . 26
8 Ichthyotomus sanguinarius attached to the fin of Myrus
vulgaris . 41
9 The stylets forming the organ of fixation in Ichthyotomus . 41
10 Ellobiophrya donacis 42
11 Anterior region of Ichthyotomus 43
12. Thyca stellasteris and T. ectoconcha 50
13 Mucronalia palmipedis 52
14 Anatomy of Stylifer linckice . 54
15 Gasterosiphon deimatis 55
16 Structure of Entocolax, Entoconcha and Enteroxenos 58
17 Entoconcha mirabilis and its relationships with the host 59
18 Part of the gut of Stichopus bearing individuals of Enter-
oxenos of various sizes 60
19 Veliger larva of Entoconcha 61
20 Pcedophoropus dicfElobius 63
21 Gnathia maxillaris 67
22 Epicarid larva of Cancricepon elegans 69
23 Microniscus stage, on Calanus elongatus 70
24 Cepon elegans,' cryptoniscan larva and adult dwarf male 71
25 Bopyrus Jougerouxi, a parasite of Leander serratus '. 73
26 Cepon elegans,' adult female . 74
27 An adult entoniscid, Portunion mcenadis, in its normal posi-
tion inside the carapace of Carcinus mcenas 77
vii
Vlll LIST OF ILLUSTRATIONS
28 Portunion manadis. Stages of development in the crab
Carcinus manas 78
29 Portunion manadis: very young female at the beginning of
its metamorphosis (asticot stage) . 79
30 Portunion kossmanni: adult female with the brood pouch
filled with embryos 79
31 Portunion kossmanni: adult male greatly enlarged 80
32 Epicarids of the family Dajidre 82
33 Ancyroniscus bonnieri: sub-adult female before egg de-
position; adult female after laying 84
34 Crab carrying Sacculina, showing the root system 86
35 Larval development of Sacculina . 88
36 Jnternal stage of Sacculina 90
37 Thompsonia sp. on Synalpheus brucei 91
38 Cypris larva of Myriocladus 95
39 A. Fragment of the stem of Metacrinus rotundus bearing
two females of Synagoga metacrinicola; B. Female of Syna-
goga metacrinicola with half the carapace removed 96
40 Laura gerardim 98
41 Baccalaureus japonicus, female 99
42 Baccalaureus japonicus, male 100
43 Myriocladus okadai, female . 102
44 Myriocladus okadai, male 103
45 Xenocr.eloma brl/mpti attached to Polycirrus arenivorus 106
46 Monstrillid parasite in the dorsal vessel of Syllis gracilis. 109
47 Development of some Monstrillidre 111
48 Developmental cycle of Rhopalura ophiocomm 114
49 G10chidium larva 116
50 Primary larvre of various entomophagous Hymenoptera 125
51 Larval forms of Bothriocephalus latus 130
52 Caryophyllaus laticeps, a parasite in the gut of the carp 133
53 Miracidium of Parorchis avitus, a parasite of the gull Larus
argenta/us . 137
54 Schistosoma hmmatobium 140
55 Development of Schistosoma mansoni 141
56 Cycle of Porospora portunidarum . 146
57 Developmental cycle of Plasmodium cynomolgi 149
58 Dwarf males parasitizing females in the Ceratioidea 157
 LIST OF ILLUSTRATIONS ix
)Y 8phcerularia bombi 159
60 Gyrodactylus elegans 164
61 Polyembryony in Encyrtus fuscicollis 166
62 Lithocystis schneideri . 194
63 Modifications in the abdomen of Carcinus mamas under
the influence of Sacculina 201
64 The abdomen of Inachus mauritanicus showing modifica-
tions due to Sacculina 202
65 Cellular reactions of the host to coccidIa and gregarines . 206
66 A. Fragment of the test of Phormosoma uranus with numer-
ous prominent spherical galls of Pionodesmotes phormo-
somce; B. Interior aspect of one of the galls . 209
67 Longitudinal section of the root of a melon attacked by
Heterodera radicicola . 211
70 Ciliates in the paunch of ruminants 227
71 Larva of a green-fly, Drepanosiphum platanoides, showing
the green body or mycetome 236
72 Symbiotic yeasts and mycetocytes in Homoptera 237
73 Sections of luminous organs in Rondeletia minor and
Sepiola intermedia 247
74 Cells of luminous tissue from Pyrosoma giganteum with
photogenic bacteria 250
75 LarVa! of Sitodrepa panicea ten weeks old 253
76 Louse, Pediculus humanus capitis, female 255
77 Intracellular termination (arbusc1e and sporangioles) of an
endotrophic mycorrhiza in Allium sphcerocephalum . 264
78 Seedling of Phalcenopsis grown in a sterile tube by being
sown on cotton wool steeped in a decoction of salep with
Rhizoctonia mucoroides 267
79 Lelio-Cattleya sown in sterile tubes inoculated with
Rhizoctonia of increasing activity . 272
80 Section of a germinating Odontoglossum, showing the
penetration of the suspensor after one month, and the intra-
cellular coiling' of Rhizoctonia lanuginosa, as well as its
destruction by phagocytosis 273
 PREFACE TO THE ENGLISH EDITION

IN the present work I have dealt with parasitism from the point
of view of general biology. Parasitism is a relationship of direct
and limited importance between two organisms, each usually
having a clearly defined role, either of host or parasite; the
parasite lives at the expense of the host. It is really a special case
of the relationship of every organism to its environment, in
this instance to another organism, an association which is
particularly precise. There exist other associations between
organisms, less restricted-but which are also very often
specific-that are described as commensalism and mutualism.
There are others again which are, on the contrary, more
restricted, more constant and less unilateral, to which the name
symbiosis has been given. Commensalism, parasitism and
symbiosis are man-made categories which in nature are not
discontinuous but are really different aspects of the same
general laws. This book seeks to make this clear by reviewing
these types of association one by one, within the framework of
the theory of evolution. Ignorant as we still are of the mecha-
nisms by which evolution is brought about, its reality cannot
easily be controverted, and it imposes itself on us more and
more as our knowledge increases. Parasites are perhaps the
org<lonisms in which this is most evident. In effect they are
closely adapted to the very peculiar conditions in which they
live, and their organization, specialized as it may be, always
appears not like that of autonomous types forming an inde-
pendent class of beings but as the transformation of various
types of animals living under normal conditions. The world of
parasites was formed gradually, after the differentiation of the
various groups of animals. It is the result of a secondary evolu-
tion which is less remote. If this were not so it would be
necessary to assume that a capricious Providence had specially
attached to each animal a cortege of parasites curiously mal-
formed according to a predetermined plan. And, in this case,
xi
xu PREFACE TO THE ENGLISH EDITION
why should not these parasites constitute special groups? The
study of parasitism is a particularly clear illustration of
evolution.
This book does not aim at an equivalent treatment of para-
sitism among animals and among plants, which might logically
be expected. As a zoologist, I have not been able to avoid giving
preponderance to facts drawn from the animal kingdom, if only
because I feel myself more competent to deal with them. Also
there is a vast domain intimately connected with parasitism
which remains almost completely outside the scope of this
book, namely bacteriology. Most bacteria, pathogenic or not,
are parasites. Their relationships with their hosts involve
above all else the major problem of immunity, natural or
acquired, and it is perhaps astonishing that it should not occupy
here the place to which it appears to be entitled. In point of
fact bacteriology and the problems it raises have on account
of their theoretical and practical importance their place in
other works; in this one, therefore, they have been left on
one side.
It goes without saying that questions of a general character
can only be treated through facts that are concrete and exact.
In the field of biology the general exists only through the
particular. It is necessary, therefore, to bring all the ideas
expressed back to precise facts. Thus, in order to give an idea
of the malformations due to parasitism, instead of keeping to
affirmations of principle, or to general aspects, a certain num.her
of especially characteristic examples have been chosen. They
have been selected as far as possible from recent researches,
thus avoiding the detailed repetition of examples which -have
become classical.
 CHAPTER I

COMMENSALISM

PARASITISM may be defined as the condition of life which is

normal and necessary for an organism nourishing itself at the
expense of another---called the host-without destroying it as
the predator does its prey. In fact there is a complete series
of transitions between the two conditions. In order to live
regularly on its host, the parasite, save in exceptional cases,
remains in permanent contact with it, perhaps on its outer
surface, perhaps within it. Parasitism is then an association,
generally continuous, between two different organisms, one of
which lives at the expense of the other. The association has an
essentially unilateral character: it is necessary to the parasite,
which dies for lack of nourishment if separated from the host;
it is not in the least necessary to the host. The organization of
the parasite is modified according to the conditions under which
it lives on the host: adaptation is the hallmark of parasitism.
But one can imagine, and there exist in fact, associations not
having the same unilateral character: two species associating
regularly but without the one living on the other. One of them
may indeed benefit in protection or nutrition without the other's
gaining any advantage. These associations are grouped under
the term commensalism. In some of them, which come under
the heading of mutualism, there are clearly reciprocal advan-
tages for both associates. In addition, the regular localization
of one species within the interior of another one may have a
peculiar spatial sigJ?,ificance without any physiological relation-
ship being involved. Associations of this nature come under
the heading of inquilinism. It is clear that there are many transi-
tions between these associations and parasitism which is no
more than a unilateral deviation from them. The study of
commensalism, inquilinism and mutualism is then the natural
prelude to that of parasitism and will allow us to grasp the
1
2 COMMENSALISM
diversity of the relationships which can become established
between two species.
Very similar in meaning to commensalism is the term
synrecy (avv with, oZl<os- house), which has been suggested
for certain particular cases. Synrecy implies, bowever, more than
a simple spatial relationship, which would be a much more
widespread phenomenon. There is, indeed, in the grouping of
organisms, a general relationship, closely bound up with the
laws of their interdependence, which is beyond the scope of the
present work and which gives rise to the general facies of flora
and fauna, that is, organic pppulations. It leads to what the
botanists call formations of plants; the zoologist will easily find
analogous groupings which are termed bioca:noses. A coral reef
comprises a major association of this kind, which entails a
certain persistent stability among all the creatures which live
there and come constantly into contact. It would be possible to
cite from the sea shores of Europe many other associations of
the same kind but more limited, each comprising a definite
population. The terrestrial fauna shows them equally clearly;
we shall have to return to those concerned with the social
insects, particularly ants and termites. On an isolated plant,
particularly a tree, a whole series of species associates regularly.
These general associations, however, involve a very loose re-
lationship, much less precise than that denoted by the term
commensalism.

COMMENSALISM IN MARINE ANIMALS

Commensalism implies a regular association between two
species, recurring constantly in widely separated localities. On
analysis it is found that this simple relationship involves very
marked modifications, particularly of a psychophysiological
nature. The double danger of research into this type of phenome-
non lies, on the one hand, in bringing to them preconceived
ideas of too subjective a nature, bordering on an illusory
anthropomorphism and, on the other hand, in trying to reduce
complex facts to simple elementary reactions.
Let us consider the classical case of the commensalism of
sharks and the pilot fish (Naucrates ductor) or the remora
(Echeneis remora). These scombrids accompany the sharks, the
 FISHES AND SEA ANEMONES 3
remora attaching itself to them temporarily by means of its
dorsal fin, modified to form a sucker. This mode of life pre-
supposes a very precise adaptation of neryous reflexes which
can be surmised when a remora and a Carcharias are seen
together, as I have seen them in an aquarium at Bermuda. The
first follows the other as a piece of iron does a magnet, obeying
instantly the incessant and irregular changes of direction shown
by the shark in an aquarium. The synchronism of the remora's
swimming with that of the shark must be associated with a
close adaptation of sensory organs and nerve centres, an
adaptation as considerable as that of the sucker in the morpho-
logical field. From this instance it is clear that the facts of
commensalism must be studied from life, and as far as possible
through experiment.
Apparently quite simple, but probably very complex, is the
similar association between anemones and fishes known in
many localities in tropical seas, and studied carefully by
Sluiter 48 in Batavia. A fish of the genus Trachichthys (or
Amphiprion) always remains amongst the tentacles of a large
anemone. Plate has also seen this association in the Red Sea,
where the anemone is, according to him, Crambactis arabica,
more than 30 cm. in diameter. If the anemone closes up, the
fish is imprisoned and momentarily vanishes within its digestive
cavity. Now, it is only necessary to be present when an
anemone's prey comes into contact with the tentacles and is
enclosed within them to see how formidable contact with the
nematocysts can be. The fishes cited here must thus possess an
immunity against the urticarious poisons of the anemones that
they frequent, an immunity which has, no doubt, been gradu-
ally acquired and which, by itself alone, witnesses to the very
definite nature of an association which appears to be purely
. casual. This association satisfies two different needs, nutrition
and protection. Concerning nutrition, the authors do not give
very precise information but it may be supposed that when the
anemone engulfs its prey and, at the same time, closes over the
fish, the latter gets a share of the food. As for protection,
Sluiter has demonstrated it directly. For several months he
was able to keep living Trachichthys in an aquarium where he
had placed carnivorous fishes and also the anemone. The
Trachichthys never left the latter. On the other hand, when
4 COMMENSALISM
placed alone with the carnivorous species in an aquarium they
were always eaten after a few hours. The anemone, then, truly
shelters the fish. Thus here we have an example of a highly
efficient association comprising precise physiological immunity
and, very probably, co-ordination of the reflexes of the two
associates.
It is evident that a similar interpretation must be given
to an association, easily observed on French coasts, between
acraspedote medusre, in particular Rhizostoma cuvieri, and the
amphipod Hyperina medusarutn, or young fishes, mainly
Caranx trachurus.
Hyperina swims in shoals under the umbrella of the medusa,
and takes shelter in the sub-genital cavities. Caranx forms fair-
sized shoals with the same habit, never leaving the medusa and
sometimes taking refuge within it, as do the amphipods. The
same association has been met with in very distant regions.
It has been found between a Caranx and a crambessid in the
Gambier Islands in the Australian Pacific by Seurat, and
between Caranx melampygus and Crambessa palmipes near
Mauritius by LuneP6.
The members of the genus Physalia, whose nematocysts are
particularly urticarious, are frequently accompanied by little
fishes (Nomeus gronovii) related to Caranx and apparently
immune to the poison of the siphonophore;* they evidently
derive protection from its proximity and possibly profit by
sharing its prey.
Associations of this type are very common on coral reefs.
Coutiere 22 has seen a number of examples at Djibouti. A trans-
parent pontoniid prawn, Periclimenes, constantly remains, like
the fishes cited above, within the zone of protection formed by
the tentacles of a large anemone; anchovies, Engraulis, take
refuge amongst the long spines of a sea urchin, Diadema
setosum; a large asteroid, Cu/cita, permanen~ly shelters a hippo-
lytid prawn beneath its disc. Many alpheids live in the shelter
of madrepore corals (Pocillopora, Porites, etc.). In the Gambier
• The various aspects of commensalism raise many complex problems of
immunity each of which demands special study. I shall limit myself here to
recalling the work of J. Cantacuzene on immunity in invertebrates, and his report
on this subject'at the 75th anniversary of the Societe de Biologle (1 923,pp. 48-219).
This work provides a starting point for research into immunity amongst com-
mensals.
 ASSOCIATIONS ON CORAL REEFS 5
Islands, Seurat (in Coutiere 22) has seen an alpheid prawn, Arete
dorsalis, living beside a sea urchin (Heterocentrotus mamillatus)
in holes occupied by the latter within a coral, and the prawn is
of the same colour as the urchin (homochromous); a similar
phenomenon occurs in many of the examples already given.
Potts 45 says that in Torres Straits Synalpheus brucei lives in
pairs (male and female) in the arms of a comatulid (Comanthus
annulatus) and he has seen many other crustaceans (alpheids,
pontoniids, Galathea, Cirolana, etc.), annelids and gastropods,
which are commensal with crinoids under the same conditions
on reefs. In Madagascar Geay has observed a crab, Lisso-
carcinus orbicularis, living permanently at the mouth of a holo-
thurian, which, when the tentacles are retracted, is surrounded
by these and momentarily trapped within the buccal cavity just
as the fishes discussed above are trapped by the anemones.
Here again the crab is homochromous with the holothurian.
Borradaile has seen the same kind of phenomenon in the
Maldives.
Sometimes the commensal even produces a malformation in
the animal with which it shelters, causing a kind of gall. Such
is the case with the crab Eumedon convictor, observed by
Seurat 15 in the 'Gambier Islands; this animal lives in quite a
large cavity, almost enclosed and formed by the folding back of
the apical region of a sea urchin (Echinothrix turca), with which
the crab is homochromous.
Similar malformations are produced in Pocillopora by
another crab (Hapalocarcinus marsupialis), first noted by Semper
in the Philippines and studied again later by Potts 267 in Torres
Straits.
A very curious association (Fig. 1) is that of the sipunculid
Aspidosiphon with a solitary polyp of the genus Heteropsammia
(=Heterocyathus). It has been studied principally by Bouvier 14
and by Sluiter 49. The Aspidosiphon begins by establishing itself
in a little empty gastropod shell as if it were a hermit crab; the
larval polyp settles on the shell, covers it and grows beyond it,
forming a considerable mass in which the worm would be
immured did it not establish within it a gallery with a terminal
opening as well as a series of lateral ones. The Aspidosiphon is
thus effectively protected by the polyp whose mobility is
assured by it; it can, in fact, project its anterior extremity and,
6 COMMENSALISM

arching up on itself, can move about, dragging the PQlyp after

it. The manner in which this association develops suggests that
it must be accidental; it is however found with the same species
in places as widely separate as Reunion, the Red Sea and the
Malay Archipelago.
Many instances of commensalism have been observed without
having been sufficiently studied in life. In the sand of the French
beaches the !lpatangid urchin Echinocardium cordatum is very
often accompanied by a bivalve mollusc, Montacllta ferru-
ginosa, which occurs near the anus of the spatangid and which
lives in the same kind of association with some synaptid holo-
thurians as does the amphipod Urothoe marinus. These animals
probably utilize the stream of water produced by the sea urchin.
In the lateral folds of the anterior region of Balanoglossus

A
Figure 1. Aspidosiphon and Heteropsammia cochlea (after
Bouvier).
A, the sipunculid moving along and dragging the polyp. B, the sipunculid
in isolation.

(=Ptychodera) there regularly occurs a number of annelids,

which must be attracted there by the stream of water from the
gill slits of the enteropneust. Thus Giard 32 has found a hesionid,
Ophiodromus herrmanni, on Balanoglossus in the Glenans
Islands; Gravier 33 has described a large polynoid, Lepid-
asthenia digueti, living in the same way on Balanoglossus in the
Gulf of California; the ornamentation of the commensal makes
it almost invisible on the enteropneust. Other polynoids, such
as Nychia cirrosa and Lamilla setosissima, live within the tubes
of Chcetopterus. On the species of Balanoglossus which in the
Gulf of California is associated with Lepidasthenia digueti there
is often found a crustacean, Lysiosquilla. A copepod genus,
Hersiliodes, is represented by some species which live in the
 HERMIT CRABS 7
galleries dug in sand by a c1ymenid or Callianassa. Within the
tube of a large terebellid, Loimia medusa, of tropical seas there
frequently occur porcellanid crabs of the genus Polyonyx.
De Saint-Joseph 46 has seen numbers of them on samples of
this species brought from Senegal, and I have had the oppor-
tunity of seeing the same association with Loimia medusa
collected jn the Malay Archipelago by the Siboga expedition.
Under the same conditions Polyonyx associates with other
annelids. Inde'ed, of 99 individuals of Chretopterus collected
at Beaufort (North Carolina) on the Atlantic coast of America,
Enders 27 found only 11 without Polyonyx, while 75 of the
Chretopterus tubes contained 176 of the porcellanids. This
author remarks that it is very uncommon to find the crustacean
free-living, and that in the tube its death quickly follows that
of the worm; it is likely that the current of water produced by
the worm is essential for the crab's respiration.
This selection of examples, to which could be added many
others, shows how commonly and regularly these associations
occur. We shall conclude with those formed by the pagurids,
on which some important researches have been carried out.
It is well known that the pagurids, or hermit crabs, take
shelter in the empty shells of gastropods and are highly adapted
to this habitat, as is shown by the softness and asymmetry of
the abdomen, the conformation of the terminal appendages
(uropods) and a number of other characters. * There are
numerous commensals associated with the pagurids; we shall
consider some of them.
These associations are very varied, even among the species
of the French coasts. Chevreux 18 has carried out a methodical
examination of Buccinum shells occupied by Eupagurus bern-
hardus on the Normandy coast where this species is collected
and used both for food and for bait. The shells often bear an
anemone, Calliactis parasitica. Almost all are covered by a
hydroid, Hydractinia echinata; 10 per cent. contain a polynold,
HarmotllOe c(£/iata; 30 per cent. of them have Nereilepas
jilcata, which we shall discuss later on (Malaquin found 50 per
cent. at Portel). In many of the shells there also lives a copepod,
Sunaristes paguri, and, in addition, Chevreux collected 8 species
* For reversion to symmetry due to livmg without shelter see Bouvier,
Recherches sur les affinites des Llthodes et des Lomis avec les Pagurides, Ann.
Sci. nat. Zool., ser. 7, 18, 1895.
8 COMMENSALISM

of amphipods, 4 of which were common. Until then, one of

the latter was believed to be a rarity, so we may conclude that
its normal habitat is within the shells inhabited by the pagurids.
It is very likely that further quantitative investigations, similar
to those carried out by Chevreux, on other species in other
localities will produce analogous results. Bonnier and Perez 12,
working in the Red Sea, have found, in shells inhabited by
Pagurus brevipes, the schizopod crustacean Gnathomysis
gerlachei, which is the type of a new family.

o
!
< :_"""?=: ,r",0J.JP 1\),,'k!~U1, I~ij~
Figure 2. Hermit crab in an artificial glass shell, with its com-
mensal Nereilepas fucata coming out to take part in a meal
of sea urchin ovary (drawing lent by G. Thorson).
The commensalism of Nereilepas fucata has be~n the subject
of interesting observations by Chevreux and Coupin 21. First it
must be noted that it is always this species that is found under
these particular conditions, and no other nereids; the asso-
ciation is rigorously specific. The worm conceals itself in the
terminal whorls of the shell where it finds shelter. It is truly a
commensal in the strict sense of the term. Chevreux, indeed,
when feeding Eupagurus bernhardus with mussels in an
aquarium, observed that when the pagurid gets one, the nereid,
 HERMIT CRABS AND NEREIDS 9
probably attracted by an olfactory stimulus, leaves its place
inside the shell and comes up, between the mouth-parts of the
crab, to seize pieces of the prey. Coupin has made analogous
observations when feeding the pagurid with Cardium, and he
remarks that the crab never attempts to devour the annelid,
although this could easily be done. There is obvious toleration,
which implies special reflexes and precise instincts. These details
have recently been confirmed and extended by G. Thorson. He
succeeded in making both partners accept artificial shells made
of glass, in which tlie behaviour of the worm could be followed,
particularly in a red light which closely conforms to the illumina-
tion of its natural home. The nereid usually remained quietly
at the bottom of the shell, with its ventral surface against the
glass. If the crab was given a piece of the ovary of a sea urchin
and began to eat it the nereid would be seen hurrying forwards
to seize its share close to the very mouth of the crab. The
occurrence did not last a minute. The crab did not try to get
rid of the intruder, who is a tolerated tenant admitted to the
table of the landlord. In this association we see that the roles
of the two partners are not equal; the nereid appropriates a
share of the crab's prey and therefore lives at its expense.
The shells inhabited by the pagurids are very often covered
near the aperture by the hydroids Podocoryne and Hydractinia.
The polyps grow up from a mat of a horny substance
which, in the case of Hydractinia, even extends beyond the
margins of the shell and prolongs it. It appears that in this
association there are reciprocal advantages: ,the nematocysts of
the hydroid must give the pagurid some protection, and the
hydroid must gain extra food as a result of the pagurid's move-
ments in search of prey.

Let us now consider the anemones which are attached to

these shells. On the French coasts Calliactis parasitica is asso-
ciated with several species of pagurids: Eupagurus bernhardus,
Pagurus striatus and P. angulatus; Adamsia palliata, on the
contrary, is always commensal on Eupagurus prideauxi. At
great depths Pagurus pilosimanus regularly occupies shells
covered with a colonial anthozoan, Epizoanthus parasiticus.
In the last two cases the body of the commensal grows beyond
the shell, thus enlarging the pagurid's dwelling, particularly so
10 COMMENSALISM

where Epizoanthus is concerned. It is noticeable that Calliactis

parasitica and Adamsia palliata show very highly developed
acontia, long filaments bearing nematocysts, which they dis-
charge through lateral openings, the cinclides, and it cannot be
doubted that these constitute a specialized defensive mechanism
both for them and for the pagurids.
The Calliactis-pagurid association is much less intimate than
that of Adamsia with E. prideauxi. There may be as many as
seven or eight individual Calliactis on the same shell, necessarily
occupying very varied positions. Moreover, this anemone is
able to live a solitary life, though normally it associates with
the pagurid, as may be seen in aquaria. Faurot 30 indeed has
shown that if the pagurid is taken out of a shell on which a
Calliactis is fixed, the latter will, after a few hours, spontane-
ously detach itself from the empty shell. The pagurids literally
capture the Calliactis when they meet one: these tactics have
been followed in detail by Cowles 20 on Pagurus de/ormis and
P. asper in the Philippines, which occupy the shells of Dolium,
Strombus and Cassis. They transplant their anemones when
they change shells. The anemone lends itself to this manreuvre;
it does not contract and after a few moments detaches itself;
the pagurid then rolls it along and transfers it to the new shell.
Faurot has noted that in none of these cases are the acontia
discharged although their discharge is regularly brought about
in other circumstances by a much weaker stimulus. The
association therefore involves a complex of precise reflexes.
The work of numerous authors, notably Faurot 31, has shown
that with Adamsia the facts are much more significant. Here
the pagurid, Eupagurus prideauxi, always lives in a shell too
small to contain it; the shell serves less as a shelter than as a
means of attachment for the anemone. The latter, which
always occurs singly, forms the true shelter for the crab
and is proportionate in size; it provides a supple covering,
moulded to some extent upon its inmate and aUowing it an
agility of movement which distinguishes it from the pagurids
associated with Calliactis; these are much heavier and slower.
A comparison of the appendages of a number of pagurids shows
clearly how perfectly those of Eupagurus prideauxi are adapted
to its association with Adamsia palliata; with such a type of
movement it could not live in a deep shell.
 HERMIT CRABS AND SEA ANEMONES 11
Adamsia occupies an unvarying position upon the shell, its
mouth always opening on the ventral surface of the pagurid,
behind the mouth of the latter; it thus often ingests a large
share of the pagurid's prey without the crab's offering any
resistance.
As soon as the anemone is fixed, after having been captured
by the pagurid, it expands, undergoing a very great change of
shape and secreting a membranous cuticle from the concave
plantar surface which prolongs the shell.
It appears that Adamsia cannot live except in association with

Figure 3. Association of Eupagurus prideauxi and Adamsia

palliata (after Faurot).
A, the anemone alone. E, the anemone attached to a Scaphander shell (its
mouth on the lower surface). C, the hermit crab with the anemone.

the pagurid. If, indeed, the latter is removed, the anemone

rapidly detaches itself from the shell. It settles on the bottom
but does not survive for long even when fed. Adaptation in
these associates is reciprocal and very close. There are clear
advantages for each partner: shelter and protection for the
pagurid, food for the anemone. Here, undeniably, there exists
mutualism between two distinct species, and each has been
modified, both in structure and behaviour, by the association.
This association is one of those which have been most
studied; nevertheless, it could still furnish material for many
experiments. The association of Pagurus pilosimanus and
12 COMMENSALISM
Epizoanthus parasiticus is probably equally intimate; unhappily
it is not accessible to experiment. Many tropical pagurids could
certainly provide material for observations of the same kind as
those discussed above.
The pagurids are not the only Crustacea that associate with
anemones. On the coasts of Chile, Burger 17 has seen an analo-
gous association between a crab, Hepatus chilensis, and Actino-
loha reticulata. Out of sixty of these crabs collected at Coquimbo,
only four were solitary; each of the others had its back and
carapace covered with the anemones. Burger separated the
animals from each other and placed them in an aquarium. The
anemones first settled on the bottom, but after a few days they
spontaneously detached themselves. Burger noticed that on
coming into contact with a crab they attached themselves by
the foot to one of its limbs and then moved up until they
reached the back. Here, then, it is the anemone that takes the
initiative in the association, the reverse of that which occurs
with anemones and pagurids.
The preceding associations may be compared with the very
curious behaviour of certain crabs that are always found
holding an anemone in each claw. This singular association
was first observed in the Seychelles, in 1880, by Mobius, in
Melia tesselata. It was found again in the same species by Borra-
daile in the Maldives, then in Hawaii; it is clear, then, that it
is not fortuitous, but a normal association. Duerden 25 made a
very interesting study of it in Hawaii, where he discovered
another case in a crab, Polydectes cupulifera. The anemones
carried by Melia seen to be the same in the three localities men-
tioned, in spite of the distance apart. There are two species,
one belonging to the genus Bunodeopsis, the other to Sagartia.
Duerden observes that the crab does not discriminate between
them. Polydectes carries another anemone, df the genus
Phellia. I shall restrict myself to a summary of the most
important facts about Melia. The claws of the crab are very
slender and are borne by the highly mobile chelipeds; their
inner, opposing surfaces bear a row of sharp teeth like a saw, by
means of which the anemone is carried. The claw is only half
shut, so that the anemone is lightly held but it cannot be
detached without being torn. The crab can, however, release it
spontaneously.
 HERMIT CRABS AND SEA ANEMONES l3
The anemones have a fixed position, the mouth turned
towards the dorsal surface of the crab, with the tentacles
upwards. As soon as the crab is disturbed it thrusts out its
claws in the direction of the intruder, brandishing the anemones
as if they were a kind of weapon. Duerden has watched it eating.
It uses the second pair of walking legs to put food into its mouth,
but not the chelipeds even when the anemones have been
removed. If the latter are offered food, such as a piece of meat,
they close on it immediately, and if the morsel is small enough
to be swallowed in one gulp they get the lot; if it is large and
sticks out of the mouth, the crab hastily seizes it with its other

Figure 4. Melia tesse/ala holding a sea anemone in each of its

chelre (after Duerden).

limbs and eats it. It is certain that the crab feeds largely on
prey stolen from the anemone after having used the latter to
capture it. *
If the anemones are removed and then put separately in the
aquarium containing the crab, it remains indifferent as long as
it does not chance to come into contact with them. But as soon
as contact has been made with one of them the crab seizes it
* Borradaile and Giard, independently of each other, compare the way m
which the crab uses its anemones with the way the workers of the ant lEcophylla
smaragdina hold a larva in their jaws (see Doflein: "Beobachtungen an den
Weberameisen ", BioI., Centralbl. vol. 25, 1905, p. 497). The larva, which has
highly developed salivary glands, spins a thread of silk whIch the workers use
for joining leaves by their edges. The adult worker has no spinnmg glands and
therefore makes use of those of the larv:.e. Giard has suggested that this kmd of
behaviour should be known as biontergasy (j3lWV hvmg, £pyaa{a work, Rev.
Scienlif" 1905, 1st sem., p. 314).
14 COMMENSALISM
and goes through a series of manreuvres in order to detach it
from the bottom and place it within its claw, in the position
already described. Even a fragment of an anemone suffices to
release a series of reflex actions. Without going into further
detail we can see that Duerden's interesting experiments demon-
strate, in the crab at least, highly elaborate and differentiated
reflexes such as occur in the pagurid-Adamsia association.
Duerden wa$ unsuccessful in finding isolated anemones of the
genera Meiia, Bunodeopsis and Sagartia, but he found solitary
Phellia. His observations show that the crab benefits from the
association much more than the anemone. *
In addition to the associations already discussed, pagurids
commonly form another type with a monaxonid sponge,
Suberites domuncula, which first covers the shells with a thick,
fleshy mass and then resorbs the shell itself. Within the substance
of the sponge, the pagurid forms a gallery which extends the
original shell cavity and remains open to the exterior. The mass
of the sponge provides a very secure shelter, particularly
'" There is undoubtedly a link between the preceding facts and certain instincts
of crustaceans which are not stnctly cases of commensahsm but which must
arise from the same physiological mechanisms and whIch serve to elucIdate
commensalism proper. I refer to the instinct of dIsguIsing. It is particularly
developed In the oxyrhyncous crabs (Maia, Hyas, etc) and is easIly seen on our
coasts. It also occurs in the Dromiacea. The principal facts, known for a long
time, were carefully descrIbed in 1889 by AurivIllius 11, and their psycho-
physiological SIgnificance has been the subject of profound researches by
Mmklewicz 39. The objects used by the oxyrhynchids to clothe themselves vary
greatly-green or red algre, sponges, compound ascidians, hydroids, etc.-but
are always selected so as to be homochromous with the substratum on which the
crab hves. Maia has even been seen III an aquarium disguising itself wIth the eggs
of a cuttlefish, detaching them one by one from a cluster. These objects are
attached to hooked setre on the dorsal surface and the crab uses its long chelipeds
to fix them there after having tom them. Crabs can be brought to disguise them-
selves WIth non-hving material such as paper or rags; if they are of dIfferent
colours the animal sorts them to obtain a covering homochromous with the
bottom, or else, having adopted its disgUIse, it moves on to a bottom matching it.
Crabs still disguise themselves, but WIthout regard to colour, when their ocular
peduncles have been removed and the connectIves between the cerebral ganglia
and the ventral nerve cord severed. The senes of reflexes is completed once the
initial reflex has been released. The instinct for concealment, concludes
Minkiewlcz, "est un enchainement de reflexes des appendIces thoraciques
anterieurs, provoques par les tangoreceptions des pinces, diriges par des tango- et
chemoreceptions des pu':ces buccales et pousses par les tangoreceptions des
crochets dorsaux flexibles vers leur but terminal' '. Colour choice is superimposed
on the instinct for disguise and IS determined by a "chromotropism" corre-
spondmg with the environment, compelling the animal to seek certam coloured
surfaces and to avoid others. Data recently obtained on arthropod endocrinology,
and the effect upon chromatophores of a gland in the eye stalk of decapod
Crustacea, throw considerable lIght on the observatIon of Minkiewicz on Maia
10 which the eyes had been removed.
 CONCLUSIONS 15
against octopuses. • of the association are little
The early stages
knqwn.*
It is obvious from the examples of commensalism given above
-to which many others could be "added-that under a guise of
simplicity these associations involve complicated reflexes which
are the culmination of long-standing adaptations just as are
morphological specializations. It is only through observation
of the living animals and through experiment that we can
further our knowledge.
Some of these associations, like those of Eupagurus pri-
deauxi and Adamsia palliata, are clear examples of mutualism;
others appear to be exclusively for the benefit of only one of the
associates which can accordingly be regarded, in some respects,
as a parasite.
Commensalism ought not to be regarded as a rigid and
clearly defined entity, but as a general term gathering together
cases of extreme diversity where the relationships vary from
simple proximity to well-defined associations involving precise
reflexes. At the same time there may be reciprocal immunity
against the secretions of each partner. Many of these associa-
tions, if carefully studied in this regard, would undoubtedly
produce interesting results.
* Suberites is also employed as a disguise by the Dromiacea which place
small pIeces of the sponge on their backs where It grows and takes on the shape
of the carapace.
 CHAPTER II

COMMENSALISM IN TERRESTRIAL
ANIMALS

IN terrestrial animals there are perhaps fewer clear-cut associa-

tions than in the marine animals already discussed; most of
those which could be quoted are better dealt with as cases of
parasitism. Some, however, are analogous, such as the relation-
ships between ungulates and certain birds which follow the
herds, sometimes resting on the animals and picking off the
ticks and the restrid larva! that infest the hide. Starlings do
this, also some wagtails (Motacilla flava) and magpies in
France, Crotophagus in America, and Buphagus, the ox-pecker,
in Africa. The last genus associates particularly with rhinoceros
and the larger antelopes. *
It is among the social insects, particularly the ants and
termites, that the greatest number and variety of facts con-
nected with commensalism are found. Wasmann 71 , estimated
that in 1895 there were 1,246 myrmecophilous species known,
1,177 of which were insects (including 993 beetles), 60 arachnids,
and 9 crustaceans. At the same time he enumerated 109
termitophiles, 87 of which were beetles. .
Amongst these various commensals he distinguished four
main groups:
1. SYN<EKETES (auv with, OLKOS house), or true commensals,
simply sharing the subterranean dwelling of the ants and
termites, and living on debris, scraps left from their hosts' food,
or even corpses of the latter. The ants are indifferent to them.
>I< "Credited with removing these insects are the ox-peckers (Buphagus a/ri-
canus) which, however, in the Uele district and the Bahr-el·Ghazal are far more
eager to follow the herds of giant eland. It so happens that at least one of these
birds always seems to be on the lookout to warn bIg game of the slIghtest danger.
As the little ox-peckers rise higher and higher into the air their sharp shrill notes
act as a magic whip even for the rhinoceroses. Without a moment's delay the
thud of sWIftly moving feet affirms the obedience shown to the tInY feathered
sentmels." H. Lang, "The WhIte Rhinoceros of the Belgian Congo", Bull. N. Y.
Zool. Soc, 23, 1920, p. 89.
16
 • I

COMMENSALISM IN TERRESTRIAL ANIMALS 17

2. SYNECHTImANS (avv with, EXOpOS enemy), which enter
the nest as robbers, feeding on the stores accumulated there or
devouring the larvre. The ants attack them and put them to
death.
3. SYMPHILES (avv with, CPLAOS friend). These are the species
sought by the ants and termites, even obtained by brute force,
and fed by them. This group includes the myrmecoxenes and
termitoxenes of Forel and Emery. Symphiles are by no means
always welcome to the hosts who harbour them, as we shall
see.
4. PARASITES, which we shall consider later.
The synceketes of ant-hills comprise a considerable number
of species: acarines (Trachyuropoda bostocki, Lelaps equitans),
spiders (Micaria scintillaris, Thyreostenus biovata, Tetrilus
arietinus), isopods (Platyarthrus hoffmannseggii), Collembola
(Beckia albina), Diptera (Phyllomyzajormica, larvre of phorids
and syrphids, the limaciform larva of Microdon mutabilis),
Hemiptera (Alydus calcaratus, Nabis iativentris), Micro-
lepidoptera, Orthoptera (an apterous cricket Myrmecophila,
Attaphila) and numerous Coleoptera; among these last are the
histerids (Heta!rius), staphylinids (Dinarda dentata, D. hagensi),
larvre of Clytra, Cetoninre (Cetonia floricola), etc. These various
species do not occur at random in the ant-hills. Most are per-
manently located in the nests of particular species. Thus some
staphylinids, such as Mimeciton and Ecitomorpha, live with the
Dorylinre which they mimic to some extent. There are even
some ants living as synceketes in the nests of other species; this
is the case with Formicoxenus nitidulus and Solenopsis jilgax in
the nests of Formica rufa.
The synechthrans of ant-hills are mainly certain staphylinids,
for instance, Myrmedonia humeralis (with Formica rufa) ,
M.funesta (with Lasiusfuliginosus), and Quedius brevis. Among
the bees there are also synechthrans, such as the wax moths
Galleria melonella and Achraa grisella, that lay their eggs on
the combs, the larvre living on wax and riddling it with galleries
lined with silken threads, and Acherontia atropos, the death's
head sphinx, which devours the honey as does also Cetonia
cardui.
Symphiles are very numerous. They are principally beetles
belonging to a variety of families: staphylinids (Lomechusa,
18 COMMENSALISM IN TERRESTRIAL ANIMALS
Atemeles, Xenodusa, etc.); Pselaphida:, especially the Claviger-
ina:; Paussida:, which are completely adapted to a myrme-
cophilous life; Histerida: (Hetarius, Ty/ois, Chlamydopsis);
Cetonina:; and some Nitulida:. Most of them are the specific
guests of a particular species of ant or termite. The ants care
for them, feed them by regurgitation and rear their larva:.
Generally the ants are attracted to the beetles by aromatic
ethers of which they are very fond. These secretions are
produced by glands situated at the base of tufts of hairs, usually
reddish ),ellow in colour, called trichomes and located prin-
cipally on the sides of the abdomen. These ethers are derived
more or less directly from the fat body: they are not truly
nutritive but the ants delight in them and lick them greedily
from the hairs amongst which they are exuded. This sometimes
leads to true aberrations of instinct.
Such is the case, for instance, with Lomechusa, one of the
myrmecophiles which has been most studied. Lomechusa
strumosa lives in the ant-hills of Formica sanguinea; the ants
seek it even to the extent of seizing it from other ant-hills; they
nourish it and lick it; they raise and feed its larva:, carrying •
them to safety in case of danger. Now, these larva: of Lomechusa
are the worst enemies of the ant larva:, which they eat, and yet
the ants feed them at the expense of their own larva:. An ant-hill
of Formica sanguinea infested with Lomechusa degenerates and
finally disappears. After a certain time, indeed, no more normal
females develop but only some that are more or less atrophied
and rather like the workers (pseudogynes): in the end the
ant-hill is no more. Lomechusa then migrates to another. It is
obvious that this guest is altogether disastrous to the ants, but
all the same it is avidly sought by them. Wasmann rightly com-
pares this aberrant instinct of the ants to the use of tobacco,
opium or alcohol by man.
Lomechusa, Atemeles and other aleocharines have a means of
defence against the ants that attack them; K. H. Jordan 62 has
shown that they possess a gland the secretion from which
collects in a reservoir situated ventrally and opening beneath
the fourth abdominal segment. The staphylinid, when attacked,
raises its abdomen and squirts the secretion, which smells of
amyl acetate, over the ant, which is stupefied by it. Amyl
acetate, in vitro, has the same effect. This gland is not an
 ANTS AND BEETLES 19
adaptive structure since it is found in aleocharines which are
not myrmecophilous.
Atemeles, a genus containing several species, lives only with
definite species of ants whose relationships with it are similar
to those of other ants with Lomechusa but are less detrimental
to the hosts since Atemeles does not live permanently with
them. Most individuals migrate regularly from one ant-hill
to another, living in spring and summer with Formica and in
autumn and winter with Myrmica. Xenodusa is the genus which,
in America, takes the place of Atemeles..
The Paussidre are beetles which are gigantic compared with
ants and have a very characteristic appearance, particularly as
regards the antennre; they are highly adapted to a myrme-
cophilous life. According to Escherich 55 they are derived from
the Carabidre. They are mainly tropi'cal, living for the most part
in the ant-hills of Pheidole; only two species, Paussusfavieri and
P. turcicus, are found in the Mediterranean region. They feed
on the larvre of the ants. When disturbed they make an explosive
noise and emit a smell, and Peringuey thought that this bom-
bardment terrified the ants which therefore tolerated the
paussids. Really, however, this reaction never occurs within the
ant-hills. The ants not only tolerate the paussids but lick their
trichomes; they do not feed them. They tend the paussid larvre
which, according to Bceving's observations, are carnivorous
like the adults. The paussids, then, although cared for by the
ants, are destructive guests which well deserve the name of
parasites.
The Clavigerinre are a very large group comprising numerous
genera and species; in France Cia viger testaceus and C. longi-
corn is live in the ant-hills of Lasius flavus and L. niger; their
larvre are still unknown. The adults are meticulously cared for
by the ants who feed them and carry them to safety when in
danger, as they do their own larvre. They produce a secretion
in a dorsal depression of the abdomen, which is licked up by
the ants. Cia viger does not appear to be harmful to its hosts
like the beetles already discussed. However, C. testaceus has
sometimes been seen vigorously biting and killing larvre of
Lasius.
Histerid beetles of the genus Hetcerius, which live in many of
the ant-hills of species indigenous to France (Formica fusca,
20 COMMENSALISM IN TERRESTRIAL ANIMALS
F. rufibarbis, and F. sanguinea), feed on the corpses of ants or
other insects but appear never to attack the healthy larvre of
the ants.
Diptera are represented in ant-hills and termitaries by a
series of types which are highly adapted, particularly with
regard to their wings which are rudimentary or even com-
pletely atrophied (Psyliomyia living with Doryius, Commoptera

ell
Figure 5. Insects that live as commensals with ants ..
A, Lomechusa strumosa (after Wheeler). B, Paussus turcicus (after
Escherich). C, Mimeciton pulex (after Wasmann). D, Claviger testa-
ceus (after Wheeler).

with Soienopsis, Ecitomyia with Eciton, etc., Termitoxenia in the

termitaries). Many phorids live there as larvre and some of
these larvre have very curious habits, such as those of Metopina
pachycondyke, which Wheeler 77 found in Texas in the ant-hills
of Pachycondyia vorax. This larva adheres by a posterior disc
to one of the ant larvre, forming a collar round it, and when a
worker presents food to the ant larva the dipterous larva
elongates its anterior end and captures the morsel intended for
 ANTS AND CaTERPILLARS 21
its host. It can pass from one larva to another and finally
pupates within a cocoon of an ant larva. Pachycondyla does not
treat it as an enemy but cleans it at the same time as its own
larvre. This behaviour recalls that of Braula, a pupiparous form
that lives op. bees, clinging to them and forcing them to disgorge
drops of honey which it secures. It is not without resemblance
to Nereilepas in relation to hermit crabs; in short, it tends
towards parasitism. I

Among Lepidoptera, the caterpillars of the Lycrenidre have,

in general, relations with ants analogous to those between
beetles and ants that we have already considered. They usually

Figure 6. Larva of Pachycondyla vorax bearing a larva (p) of

Metopina pachycondyke (after W4eeler).

live on papilionaceous plants to begin with but cannot com-

plete their development there. They are sought and captured
by'the ants and finish their larval life within th~ ant-hill. They
possess abdominal glands discovered by Guenee, unpaired ones
on the dorsal surface of the seventh segment and paired ones
on the eighth. The ants are very greedy for the secretion from
these glands, which they lick up; the caterpillars then protrude
the gland openings as tubular structures which can be sucked.
According to de Niceville certain ants rear the lycrenid cater-
pillars in flocks, constructing shelters for them where they
remain during the day, and leading them out to feed at night.
Other lycrenids develop in galls produced by Crematogaster on
p.s.-2
22 COMMENSALISM IN TERRESTRIAL ANIMALS
acacias. Some species have carnivorous caterpillars which feed
on the la:rvce of the ants which harbour them, as Oberthiir 66
has found in Lyccena alcon and L. euphemus; nevertheless these
are sought by the ants and taken into the ant-hills. Here again,
then, are relationships analogous to those of Lomechusa.
Evidently there remain many similar cases to be carefully
studied, differing in detail from one species to another.
The relationships between ants and aphids are long-estab-
lished classics; even Linnreus wrote' , Aphis formicarum vacca' '.
At the beginning of the 19th century Huber made detailed
studies of them and his results have often been confirmed since
then. Here there is true nutrition of the ant and not a search
for a secretion which is simply agreeable. The aphids cannot
utilize all the sugar that they extract from plants, and excrete
an appreciable amount by the anus, in the form of liquid
droplets ejected on to the leaves. It is this that forms the honey
dew which was known already by Hesiod and which in another
form constituted the manna of the Hebrews; since the 18th
century it has been much studied (Reaumur, Treviranus,
Boussingault, Darwin, Biisgen, Forel, etc.). Huber had noticed
that the ants induced the emission of a sugary liquid by catching
the aphids and stroking the abdomen with their antennre. This
brings about the welling up of a droplet which the ants imme-
diately absorb. They are truly milking a domestic animal. They
go to milk the aphids on the leaves. The radicolce are
captured and led into the ant-hills where the ants rear them
and protect them as if they were their own larvre. In good
weather Aphis maidiradicis is carried on to its food plants and
brought back into the ant-hills on cool nights, or sometimes
carried from old roots on to young ones. The aphids adopt a
passive attitude to all this. This particular kind of association
is known as trophobiosis.
Symphilism, then, includes associations in which the relation-
ships are very varied and which are far from being mutuaL
It is always the ants that appear to play the leading part.
The regularity and persistence of these events in widely separate
localities dhow that for the species discussed this is a normal
and necessary mode of life, the result of the evolution both of
behaviour and of form. Wasmann 75, who has carried out the
greatest number of researches on symphilism, believes that we
 MOn.PHOLOGICAL MODIFICATIONS 23
have here a special instinct which has been derived from the
ants' instinct for adoption. Janet 60 and Escherich 56 con-
sider this an unsatisfactory hypothesis. The ants care for the
symphiles as if they were their own offspring and it is rather
the symphiles that have adapted themselves to the instincts of
the ants and have exploited them for their own profit, sometimes
becoming true parasites, letting themselves be fed and their
progeny reared as in the case of the cuckoo. This has produced
truly aberrant instincts among ants, which make them sacrifice
their own larva! and which Escherich has compared to social
failings such as alcoholism in human societies.
Amongst the symphiles, adaptation extends to morpho-
logical modifications. Coleoptera living in ant-hills display
characters which are clearly adaptive, as with the trichomes,
and in mouth-parts where there is more or less marked reduc-
tion of the palps in species whicoh live on food regurgitated by
the ants. In Cia viger all the palps are short; the maxillary palps
are reduced to a single segment while those of the free-living
pselaphids are very long. The staphylinid aleocharines (Lome-
chusa, Atemeles, Xenodusa), which are fed by the ants, also
have highly abbreviated labial palps and a wide and short
tongue; this is particularly marked in the termitophilous
species: Spirachtha eurymedusa possesses only the rudiments
of labial palps.* However, there are some species of Termito-
morpha which have retained a very long maxillary palp.
Wasmann 72 explains this anomaly by the fact that the insect
uses this palp to stroke the termites and thus excites them to
feed it; Lomechusa, Atemeles and Claviger use their antenna!
on the ants in the same way.
Another adaptive character found in symphiles is physogastry,
or the more or less considerable hypertrophy of the abdomen.
This is particularly marked in termitophiles but has also been
observed in CIa viger, among the myrmecophilous aleocharines
(Lomechusa, Atemeles) and especially amongst the species
(Ecitochara, etc.) found with Eciton in Brazil. In the termito-
philous aleocharines (Spirachtha, Termitobia, Termitomorpha,
etc.) the abdomen is so greatly hypertrophied that its segments
are scarcely recognizable; it is either extended In the normal
* The same reduction of the palps is to be seen in the slave-making ants
(Anergates) which are dependent on their slaves for food.
24 COMMENSALISM IN TERRESTRIAL ANIMALS
position (TermitQmorpha) or rolled right up on itself with the
tip turned towards the thorax (Spirachtha).
It is very significant to see physogastry developed not only
in the aleocharines but also amongst the termitophilous
carabid beetles (Glyptus sculptus living in Africa with Termes
bellicosus, etc.). This is a most remarkable case of convergence.
The origin of this physogastry must be alimentary. One can
imagine that overfeeding by the ants or termites leads to hyper-
trophy of the fat body; this alteration is on the same level as
the modifications of the mouth-parts.
Finally, a last peculiarity of adaptation lies in the structure
of the antennre which are modified in different ways to become
very sensitive tactile organs.
As a result of these various adaptive forces a certain number
of symphiles have come to resemble ants both in appearance
and behaviour. Wasmann and some other workers consider
them to be mimics (cf. Mimeciton pulex, Fig. 5c, p. 20).
Here it is convenient to add to the preceding associations
others existing between different species of ants, and usually
regarded as types of slavery. We know that some species of ants
carry off the pupre of others and take them into their own ant-
hills where, after metamorphosis, they play the part of auxiliary
workers. This phenomenon of abduction, termed dulosis by
Forel, can be interpreted in various ways. Forel attributes its
origin to the highly developed instinct of pillage possessed by
ants. Darwin tried to explain it by selection. In the first place
the ants would have carried off the larvre of other species for
food, then some of the pupre which had escaped slaughter
would develop into adults which, obeying their nursing instinets,
would tend the larvre of the pillaging species. This circum-
stance, at first accidental, would become persistent on account
of the advantage it conferred on the colony. But, as in all social
modifications among ants, it is not obvious how this change in
instinct could be transmitted and fixed by selection since the
workers are sterile. Wasmann 74 does not accept Darwin's
explanation. He points out that the queen, the only fertile
member of the ant colony, does not take part in the hunt for
slaves and that therefore the instinct to rob cannot be inherited
through her; nevertheless in seeking the explanation, we must
take her as the starting point. It is necessary, on the one
 ANTS AND SLAVERY 25
hand, to take into account that the ants captured as slaves are
strictly specific and, on the other hand, the circumstances in
which a new ant-hill is founded.
The simplest case is when, after the nuptial flight, the queen
digs underground, lays her eggs and rears the first workers
without assistance. This occurs in species such as Formica jusca
and F. rufibarbis. Here there is evidently a difficult initial phase
in the founding of the colony. Certain other species occupy
deserted nests, or install themselves near the nest of other
species that they will rob.. Thus Solenopsis settles near the nests
of Messor barbarus. This proceeding may be termed clepto-
biosis (Wheeler) or lestobiosis (Forel). The female of some other
species installs herself in the nest of yet another one where she
is tolerated. This is what Forel calls parabiosis and must be the
explanation of a certain number of mixed ant-hills; the female
of Formicoxenus nitidulus establishes herself in this way in the
nests of Formica ruja or F. pratensis.
But in many species the fertilized female, incapable of
founding a nest by herself, is picked up after the nuptial flight
by the workers of a nest near which she has fallen. The workers
of Formica ruja and F. pratensis act in this way towards their
own species. Often, however, the adopted female may be of
another species; thus F. rufa adopts females of F. truncico/a, and
in America, F. incerta adopts those of F. consocius. As a result,
we find colonies which are temporarily mixed and remain
so until the original workers have died out. In other cases the
colonies remain mixed because the workers of the incoming
species pillage the pupre of the species to which the original
auxiliary workers belong. Thus F. sanguinea pillages the larvre
of F. jusca and F. rufibarbis.
According to Wasmann, these adoptions were the prelude to
slave-making. The species which steal pupre to make auxiliary
workers of them are those whose colony is founded by adop-
tion, and the workers captured later always belong to the species
that provided the initial workers. Slave-making would be an
aberration of the instinct of adoption found in ants. The queen
would participate in the evolution of this instinct through the
circumstances of her adoption and one can imagine that it might
be possible for her to transmit these modifications of it.
Evolution of the type of behaviour from which slave-making
26 COMMENSALISM IN TERRESTRIAL ANIMALS

results leads to morphological evolution. All or some social

activities are progressively transferred to the slave workers and
finally their owners are fed by them, the mouth-parts becoming
so modified that it is impossible for them to feed themselves;
they are thus absolutely dependent upon their slaves. Primitive
adoption becomes transformed into social parasitism.
This is what happens in Polyergus rufescens, the Amazon ant.
The members of this species have sabre-like mandibles (Fig. 7a),
which are weap~ns of attack. They are excellent warriors and
are energetic in carrying off the pupre from which they will later
obtain workers. Now, the captured pupre always belong to the
species (Formica fusca, F. rufibarbis) which have helped to
establish the nest. The mandibles of Polyergus have lost their

Figure 7. Head and mandibles of workers of Polyergus rufescens

(a) and of Formicafusca (b) (after Bondroit).

masticating edge (cf. Fig. 7b); the workers cannot carry out
the domestic work of the ant-hill; they even lose the instinct of
feeding themselves directly. They depend on their slaves, whose
number is always proportional to that of their masters.
Leptothorax emersoni thus parasitizes Myrmica brevinodis.
It dies when there are no Myrmica to regurgitate food for it.
This line of evolution culminates in the disappearance of the
workers, as in Anergates, of which one species, A. atratulus, in
Europe, forms obligatorily mixed colonies with Tetramorium
ccespitum. Wheeler 78 has also noted the complete absence of
workers in Epcecus pergandei. But slavery can lead to para-
doxical aberrations of instinct in the conquered species, as has
been found in Monomorium salomonis, which, reduced .to
slavery by Wheeleriella santschii, kills its own queen, thus con-
 MYRMECOPHILOUS PLANTS 27
demning its own colony to perish. Pieron 67 considers this volun-
tary sterilization of the parasitized colony as a social form of
parasitic castration.
Wheeler's views 78 on the origin and evolution of slavery
amongst ants are somewhat similar to those of Wasmann. He
starts in the same way with the founding of the colony but does
not believe that it is always a question of the adoption of the
female by the workers of another species: the female of Formica
sanguinea, for instance, after the nuptial flight, conquers the
larva! which will be the first workers in the new nest. For
Emery 54, too, the initial proceeding is one of violence; he con-
siders that a female penetrating into a nest kills and disperses
the workers and forms a new colony with the larva!. *
The trutli is certainly less simple than any of these general
theories. It is obvious how closely these phenomena resemble
commensalism and how impossible it is to distinguish clearly
between them and parasitism.
We shall now examine another type of association which,
under the influence of Darwinism, has occupied a prominent
place in evolutionary thought. I refer to myrmecophilous plants.
Fritz Muller, and later Schimper, considered them the result
of special adaptation developed by natural selection. They
provide shelters for ants, as in the hollow-trunked Cecropia
(Urticacea!) described below, or in the form of fleshy swellings
which are hollow, as in various rubiaceous epiphytes (Myrme-
2odia, Hydnophytum), or by means of hollow spines which are
large and swollen, as in Acacia sph(Procephala. Most of these
plants also possess numerous nectaries. On the leaf petioles of
Cecropia are minute structures (Muller's bodies) containing
oils and albuminoids. Acacia sphc£rocephala possesses minute
succulent structures at the tips of the pinnules.
These various organs provide for the ants a food which
attracts them and is automatically renewed. Therefore ant
colonies are nearly always found on these plants. The advantage
to the plants of being protected hy the ants from animals that
attack their foliage is said to have led by selection to the
development of these special organs. Myrmecophilous plants
have thus become a favourite example in the theory of natural
selection. This interpretation is opposed by workers who have
... See also p. 29.
28 COMMENSALISM IN TERRESTRIAL ANIMALS

observed the ants at first hand. From amongst these we shall

summarize the work carried out at Sao-Paolo by H. von
Ihering S9 on Cecropia spp. (mainly C. adenopus, the imbauba)
and the symbiotic ants of the genus Azteca.
According to the myrmecophilous plant theory, Azteca for
the most part protects Cecropia against Atta, a genus of leaf-
cutting ants which sometimes despoil whole trees of their
foliage. Work on the habits of Azteca is difficult since these
ants inhabit cavities within Cecropia and, at the least disturb-
ance, become very aggressive and bite savagely. All the old
imbauba trunks, contain Azteca but this is by no means the case
with the young trees and when they have been rid of the ants
it has been observed that they do not suffer from Alta. Thus
Azteca is not indispensable to them. These ants feed principally
on the young growths of the tree as well as on MUller's bodies,
at the base of the petioles. They penetrate into the tree in the
upper region of the internodes, where there is least resistance,
and establish their nests within the hollow trunk. The opening
so formed has been termed a stoma and around it the paren-
chyma proliferates, forming the stomatome, rich in fats and
sugar which provide food for the ants, so that they induce the
formation of successive stomatomes as fast as the tree grows.
Ihering tried unsuccessfully to produce stoma tomes experi-
mentally but the saliva of the ants seems necessary for this. In
short, it is a question of gall formation.
As for Atta, when these ants venture on to the imbaubas they
are chased off by Azteca, but they have no special liking for
these trees and the Azteca ants are only concerned with pro-
tecting their own nests and remain unmoved by the attack of
other animals, such as chrysomelid beetles, caterpillars :rnd
particularly sloths (Bradypus), which do infinitely more damage
to Cecropia; they only attack certain species of ants and tolerate
others. The imbauba is clearly the normal habitat of Azteca,
and provides it with shelter and food. The ant exploits the
tree and only protects it to protect itself. The ant is by no
means indispensable to the tree and, to quote Ihering, the
Cecropia lives without Azteca as easily as a dog without fleas.
Azteca is more closely adapted to the tree. ,According to
Wheeler, the ants perish when the tree is felled; they are really
parasites on_it. The saI11e author considers that in general the
 MYRMECOPHILOUS PLANTS 29
ants are adapted to the so-called myrmecophilous plants but
that the converse has definitely not been established. Too many
of the observations on which the theories of selection are
based have been hastily made by travellers.
In the same connection, Chodat 52 has established that in
Paraguay the swellings in various plants (Cordia, Acacia) occu-
pied by ants (Azteca, Pseudomyrma) and regarded as myrme-
cophilous adaptations were, in reality, galls produced by
chalcids (Eurytoma), the emerging adults leaving exit holes
through which the ants entered. The latter have only made use
of a modification in the plant, which was produced indepen-
dently of them, and the true adaptation here is the correlation
between them and the chalcids. It would be of great interest to
find out how widely such explanations apply to various myrme-
cophilous plants.
The few examples given in the preceding pages imply the
existence of a considerable variety in associations of this type,
each one of which demands a very detailed study.
Recent research in Switzerland A
by Stumper and Kutter 596-8 has
brought to' hght two extreme
cases of parasitism in ants. The
first of these concerns Teleuto-
rnyrmex schneideri n. sp., in col-
omes of Tetramoriurn crespiturn.
In isolation the parasite dies. Its
mandibles are atrophied, and the
tarsi modified as organs of attach-
ment. The female penetrates into
the nest of the host immediately
after the nuptial flight, loses her
wings and attaches herself to the
Tetrarnorium queen, who may Female of Tetramorium with Teleuto-
carry several of these parasites myrmex attached (after Stumper).
(Fig A). They are tended by the
workers, become physogastric
(Fig. B) and lay their eggs; the brood IS mixed. There are no workers in
Teleutomyrmex; brother and sister matmg occurs.
The second parasite is EpimYI ma stumperi. The female penetrates the nest
of the host Leptothorax nigriceps, and there uses her limbs to smear herself
With the cutaneous secretions of the host workers. Thus disguised, she kills the
queen and IS adopted by the workers who tend her eggs and larvre. The
workers of Epimyrma live on food regurgitated by the workers of the host
species.

2*
 CHAPTER III

FROM COMMENSALISM TO INQUILINISM

AND PARASITISM
INQUILINISM
WE shall now consider a different series of associations. In these
one animal lives within another but without feeding entirely
at its expense although finding a shelter and diverting for its
own use a part of the food collected by its partner. These are
not true parasitism and are often given the name of inquili-
nism* (Raumparasitismus of German authors), They form a
graduated series leading to true parasitism.
A classic example is provided by the fishes belonging to the
genus Fierasfer (family Ammodytidre), which generally live
within holothurians (they are also found in starfishes, Culcita,
and bivalves, Pinna), either in the respiratory tree or even in
the general body cavity when the wall of the branchial sac has
ruptured. They do not actually feed on the holothurian but on
small crustaceans, emerging from time to time to hunt for
them,~Emery 54 has studied their relationship to the host. They
enter by the cloaca, meeting with some resistance from the
holothurian which, in exceptional cases, even expels its viscera,
but usually tolerates them and does not appear to suffer even
when harbouring three or four. What Fierasfer seeks from its
host is a shelter. When kept in an aquarium without one, and
with predatory fishes, it is speedily attacked and eaten.
In the Bahamas Plate 43 found a similar close association
between a fish (Apogonichthys strombi, 3-6 cm. long) and a
gastropod, Strom bus gigas; the fish shelters during the day in
the mantle cavity of the mollusc, emerging at night in search
of food. .
Many crustaceans obtain similar shelte,r within the mantle
cavity of bivalves; Pontonia lodges in Pinna, and Perez 42 found
* Inquilim, from incolinus, who lives within.
30
 'INQUILINE CRUSTACEANS 31
pairs of the prawn Anchistus miersi in a Red Sea Spondylus.
Pinnotherid crabs normally occupy such a habitat; there are
many species in this family and most of them lodge in the
mantle cavity of bivalves, though a few are found in other
animals. Semper has seen them with Fiergs/er in holothurians.
This way of life even attracted the attention of the ancients,
who believed that the crab apprised the mollusc of the presence
of its prey. The biology of the pinnotherids deserves careful
attention. It is generally supposed that, when the mollusc's
valves are half open, the crabs lie in wait 'for prey passing
nearby, but Coupin 21 has found that their intestine contains the
same vegetable residues as that of the mollusc that shelters
them.
Numerous other examples of inquiline crabs cQuld be quoted.
~"
Semper found a crab living in the mantle cavity of Haliotis
and a prawn in the gill cavity of a large pagurid. In various
sponges, particularly hexactinellids, we find Pontonia, Typton,
Spongicola and ./Ega, which are, moreover, considerably
modified. Then there is the classic case of the barrel shrimp,
Phronima, the female of which lives in the test of Pyrosoma or
the'branchial chamber of salps. In the gill chamber of Lepas
are annelids of the genus Hipponoe. Malacobdella, a nemertean
with suckers, lives in the mantle cavity of bivalves (Cyprina,
Mya, Pholas). An oligochrete, Epitelphusa catensis, occurs
regularly within the gill chamber of the freshwater crab
Telphusa. And there are other cases~
Inquilinism merges by slow degrees into parasitism, as we
cab. see in the copepods that parpsitize ascidians. Even the true
inquilines living within the bi~mchial chamber undergo con-
siderable malformation, at least in the case of the females.
Most of them live on minute organisms and particles brought
into the branchial chamber by the respiratory currents of the
ascidian, and in such cases (Notodelphys, Doropygus) they still
retain the biting mouth-parts of the free-living forms. But some
related forms (Enterocola) have migrated into the stomach, or,
in the case of Enteropsis, into the epicardial tubes, and are true
parasites, their buccal apparatus being modified for sucking
up liquid food provided by the host. Other genera (Ophoseides,
Ooneides), of which Chatton 47 has made a particular study,
are even more degenerate.
32 FROM COMMENSALISM TO INQUILINISM

EPIZOITES
Verging on parasitism is the case of those animals which
always live on the surface of another animal, sometimes
attached to it, sometimes free. Permanent attachment to a
support is an important factor in morphological change, and
its effects are often comparable to those of parasitism. In many
sedentary animals the support plays only a mechanical part and
its nature varies accordingly. As, however, conditions differ
from one support to another, many animals tend to become
localized on more or less definite types, or rather development
is more successful on some types than on others.
This is particularly so in the case of living supports where
the attached animals as a rule show a very considerable degree
of specificity as well as definite localizations. This leads to
precise and constant associations, and epizootic animals, like
epiphytic plants, form a special type of commensalism.
There are very many cases of this. Many infusoria live on
marine or freshwater animals and generally on definite species.
We find this in many vorticellids (Cothurnia, Urceolaria,
Trichodina). They take nothing from their host in the way of
food but utilize the currents of water it produces, feeding on
the particles which are brought to them. Faure-Fn!miet 29
has made interesting observations on Opercu/aria attached to
various freshwater animals (Gammarus, Asellus, Cyclops and
Notonecta). He has noted tliat infusoria soon die when detached
from their host, even when, for instance, the limb to which they
are fixed is isolated with them. It is the movement of the host
and the resulting disturbance of the water which matter to
them, and most infusoria remain healthy if the isolated limb
is kept moving. Different species of Opercuiaria are confined to
different hosts and if they are transferred from a Notonecta to
a Dytiscus they fare badly and dwindle away. They must find
favourable environmental conditions on one particular host and
from this there results the specific nature'of these associations.
The class Acineta, or Suctoria, all the members of which are
fixed either to inanimate objects or to living organisms whether
plant or animal, con"tains a rather high proportion of true
commensals, a few tending towards inquilinism or becoming
true parasites. Even on plants there are certain specific associa-
 AND PARASITISM 33
tions. Thus, as Collin 19 has observed, Discophrya cothurnata
has never been found except on the roots of Lemna. Others are
always attached to the shells 'of gastropods (Paludina, Limncea),
or to the limbs of some specific aquatic beetle (Discophrya
ferrum equinum to Hydrophilus piceus, D. steinii to Dytiscus
marginalis, D. cybistri to Cybister). Some very peculiar forms,
such as Ophryodendron sertuiarice, live on hydroids. * A great
variety of Suctoria is carried by crustaceans: Dendrosomides
paguri on the limb setre of pagurids, Dendrocometes paradoxus
op. the branchial plates of Gammarus, Stylocometes digitatus on
the gills of Asellus, etc. ; and Ophryodendron annulatorum occurs
on annelids. Some have penetrated into the outer region of the
internal cavities of their hosts: Trichophrya salparum occurs in
the pharynx of salps, and at the opening of the branchial
chamber in many ascidians, t sometimes together with Hypo-
coma ascidiarum.t
Under analogous conditions certain hydroids (Hydractinia,
Podocoryne) live on the skin of fish or the shells occupied by
pagurids; Stylactis (=Podocoryne) minoi, found in the Indian
Ocean by Alcock 10 on Minous inermis, in the region of the
opercular opening, has been observed by Doflein under the
same conditions in Japan. In Puget Sound, Heath 34 found that
on 25 per cent. of Hypsagonus quadricornis there was a rich
growth of Perigonimus pugetensis, for the most part on the fins
and belly. Nudiclava monacanthi lives on a fish in Indian seas.
Ichthyocodium sarcotreti has been observed by Jungersen 35 on
a copepod, Sarcotretes scopeU, itself a parasite of a Scope Ius
glaciaUs.
Among the Kamptozoa (Polyzoa Endoprocta), Loxosoma
spp. live only as epizoites on a limited number of animals, such
as Gephyrea, Annelida (Aphrodite, Capitellidre, etc.). In material
from the Caudan expedition I myself saw on an abyssal
Nephropsis a peculiar polyzoan belonging to the Ctenostomata.
Among the Cirripedia, all fixed at least to some passive
support, there are some occurring only on certain animals such
... This species IS really a true parasite feeding on the outer layers of Sertuiaria.
t Acineta tuberosa is often very abundant on copepods.
t In an association between a cilIate and a suctorian there has recently been
discovered the curious fact that the pentrich ciliate Epistylis living on the skin of
a newt is in realIty usually attached to a suctonan, Tokophrya, fixed to the newt.
It IS a regular association, the constancy of which has been carefully worked out
by Faun!-Fn!miet. Ann. Acad. Brasil Sciencias 20, 1948.
34 FROM COMMENSALISM TO INQUILINISM
as whales or sharks; Coronula on Megaptera, Tubicinella buried
in the skin of the Australian baleen whales, Alepas and Anelasma
squalicola on sharks. Many species of Sealpellum occur on
hydroids and others of the same genus on Bryozoa and sponges.
Beside the epizoites which may be properly said to be fixed
must be placed the animals which also live upon another but
which are unattached and feed on various scraps and waste
from the animal itself: nemerteans, such as Polia involuta living
in the midst of crab's eggs, feeding on eggs that are dying or
dead but apparently not attacking healthy embryos; Histriob-
della homari (probably a modified annelid) living similarly
among the eggs of lobsters or within the gill chamber. Most
caprellids remain upon other animals such as sponges (Halichon-
dria), Alcyonaria, ascidians, etc., and from this group is derived
Cyamus, the whale louse, which lives clinging to the skin of
Cetacea. With all the animals living under such conditions it is
necessary to ascertain precisely the conditions in which they
feed; some of them are true parasites and others are just
commensals.
Having to some extent separated the preceding examples
from real parasites we still find that among the organisms
which are generally agreed to be true parasites there are some
that could also be classed with inquilines and which very
probably are derived from them. These are the intestinal
parasites which, properly speaking, do not feed on the actual
substance of the host but on its intestinal contents, that is, on
ingested material in the process of being assimilated but not
yet incorporated into the organism. This is obviously a subtle
distinction and these nutritive substances are undoubtedly
taken at the host's expense; we can indeed consider such aniplals
as true parasites. For example, there are the cestodes, and no
one would dispute that they are authentic parasites. But within
the intestine there are other organisms which feed on waste
matter that the host cannot utilize, or they may even act on
food substances so that these become more digestible. The
normal bacterial flora of an organism plays such a part and
Pasteur has questioned if an aseptic life would indeed be
possible; at the end of this book we shall consider this problem.
In the intestine of termites there are the trichonymphids which
are always present in great numbers in the workers and are not
 AND PARASITISM 35
only harmless but assist in the digestion of wood. The vast
numbers of infusoria (Ophryoscolecid~), which are always
found in the rumen of ruminants and in the c~cum of horses,
have no noxious effect in spite of their multitude and live on
either vegetable debris or on the bacteria which develop in this
medium. There is even good reason for believing that they help
in the digestion of cellulose. In any case they are rather to be
regarded as commensals or inquilines than as true parasites
and they end by being digested in the small intestine. It is the
same with at least some of the Protozoa in the large intestine
and rectum, li-ving as saprophytes, for instance Opalina, Nycto-
therus, certain flagellates and amreb~, such as Chlamydophrys
stercorea which swarms as a naked am reba in the rectum of
the horse and encysts in the droppings; and also for some
nematodes, such as the eelworms in cow dung.

INTERMITTENT PARASITES
One of the sources of true parasitism is gradual adaptation
to an exclusive diet, monophagy. Such a habit cannot in itself
be regarded as parasitism although it creates and maintains
the relation of predator and prey that is essential for this. Many
nudibranchs live regularly on the hydro ids on which they graze,
assimilating even nematocysts within their hepatic diverticula;
pycnogonids are constantly found on hydroids for the same
reason, Lamelfaria on compound ascidians, Creloplana on
Alcyonaria. Most caterpillars are confined to a definite plant,
as are aphids, and by such gradual steps we come to the gall-
producing species whose status as parasites is undeniable. Such
a graduated series is also shown by the blood-sucking insects.
Amongst these there are some, such as the culicids, which are
not exclusively blood-suckers. Many, for instance the Taba-
nid~, the Simuliid~ and the Hemiptera, are still obviously free-
living. But there are others which, in spite of appearing to be
free-living, are, in fact, intermittent parasiteyGlossina, the
tsetse fly, feeds only on vertebrate blood taken from a blood
vessel and, as we shall see, has undergone in_ both its digestive
and reproductive systems modifications which are parallel to
those of Diptera Pupipara, which are true parasites permanently
restricted to their host, for instance, Melophagus on sheep,
36 FROM COMMENSALISM TO INQUILINISM
Hippobosca on horses, Liptotena on deer, Lynchia, Ornithomyia,
etc., on birds. Of other groups, the Muscidre, in their larval
stages, show a similar range of habits: Auchmeromyia lives on
man and other naked mammals (the aard~vark, Orycteropus,
and the wart~hog, Phacochcerus), and certain Phormia and Pro to-
calliphora on birds. Fleas, bugs and leeches show us advanced
stages of adaptation to parasitism, but retain a relatively free
mode of life. Among the isopods the Cymothoidre and Gnathia
provide analogous series.
In all these vadous examples we are faced with types which
are indisputably parasites but which are related, by very gradual
series, to other forms that are clearly free-living although their
way of life is analogous. The limits of parasitism are difficult to
decide. The criterion which comes to mind is that of being
established more or less permanently on an individual and
specific host, as are the Pupipara and ticks; this is, however,
inadequate, and it is not possible to exclude intermittent para-
sites passing very gradually into free-living forms.

GENERAL NATURE OF MODIFICATIONS

PRODUCED BY PARASITISM
Inquilinism and parasitism, properly speaking, entail con-
siderable morphological change which is one of the most
interesting things to be studied in them, both from the point of
view of comparative anatomy and evolution. These modifica~
tions are always connected with the special conditions of life
of the parasite on the host and their interpretation presupposes
an analysis of these conditions, in short, research into the
physiology of the parasites, a study which, in general, is still in
its infancy and is very often difficult to undertake. It is not
surprising that here, too, morphology has largely preceded
physiology.
It is out of the question to include in a few pages all the
adaptive modifications shown by parasites; they are infinitely
variable and, to give some idea of this, it is better to take several
examples which are significant in themselves as well as by com-
parison with related free-living forms. Generally, these modifica-
tions may be summed up as a simplification of the organs
relating the animal to the environment, that is, the sensory and
 AND P ARASITlSM 37
locomotory systems, and a hypertrophy of those connected with
nutrition-the digestive and reproductive systems. We can by
no means always directly relate to adaptation all the changes
that have come to pass; many must have resulted from corre-
lations which, acting in an orthogenetic manner, have led to
extreme states in which the purpose of the adaptation is no
longer recognizable: this must occur with parasitic forms just
as much as with free-living ones, bUtt here it is a matter of a
secondary evolution whose point of departure is usually easy
to reconstruct.
The organs of locomotion of parasites either eventually
atrophy or disappear, or, on the other hand, differentiate into
organs of attachment. In arthropods the distal segments of the
limbs become hooked claws (Cyamus, Cymothoidre, Epicaridre,
etc.). In the Myzostomaria, a group derived from the annelids
and parasitic on crinoids, the parapodia are completely atro-
phied and represented by a pair of chretre. The leeches, also
derived from annelids, have lost all vestige of appendages;
however, an archaic genus, Acanthobdella, parasitizing
salmonids in Russian lakes and rivers, possesses chretre (five
groups on either side towards the anterior extremity in A. palla-
dina), indicating that parapodia were present formerly.*
The counterpart of the degeneration of appendages in para-
sites is the development of organs of fixation, either, as we have
already said, by modification of the appendages themselves, or
by the development of new structures, particularly suckers or
hooks. The trematodes, cestodes and leeches provide numerous
examples illustrating the first and, often at the same time, the
second condition which also occurs in other groups such as
the Acanthocephala.
The central nervous system of parasites is often reduced and
so are the sense organs, particularly the eyes. In the digestive
system there is generally a modification of the mouth-parts,
which very often become adapted for sucking, and a more or
less marked reduction of the hind gut since the parasite ingests
little or no waste matter with its food. The alimentary canal
may even disappear completely as in the cestodes and Acantho-
cephala where nutrition is by means of diffusion through the
* Acanthobdella also possesses vestiges of a spacious crelom typical of the true
annelids.
38 FROM COMMENSALISM TO INQUILINISM
body wall of assimilable matter elaborated by the host, or, as
in the Rhizocephala, by a system of roots spreading throughout
the whole structure of the host. A modification of this kind also
occurs in certain parasitic infusoria such as Opalina; they no
longer ingest solid food but obtain nourishment by diffusion.
In most parasites, particularly the blood-sucking ones,
ingested matter accumulates in the mid-gut, which becomes a
vast pouch from which there is gradual resorption. Leeches,
ticks, biting flies and bed bugs become gorged in this way at .
more or less widely spaced intervals of time, and similarly many
parasitic crustaceans (Epicaridre, Gnathia) accumulate nutritive
matter sucked from the host, in the hypertrophied liver. Such
methods of nutrition correspond to peculiar physiological
mechanisms which are not yet well understood. Thus, most
blood-sucking parasites apparently possess anticoagulants
which keep the ingested blood in a liquid state. This has been
found in leeches (Haycraft 375, Apathy 371), where it is due
to glands opening near the mouth within the sucker, in ticks
(Sabatini 299), in the larvre of blood-sucking restrid flies
(Weinberg 390), in Ancylostomum duodenale (L. Lreb and
A. J. Smith 379) and also in a parasitic annelid (Ichthyotomus,
Eisig 180) which we shall consider later. This is a significant
example of a similarity of adaptations occurring in organisms
living under.a particular set of circumstances, even though they
belong to different groups and are manifestly independent.
There must be many other facts of the same nature in the
physiology of digestion in parasites.
Reproduction is the process which is most sensitive to the
results of parasitism and it assumes a preponderant importance:
we shall study its principal modifications in a special chapter;
here we shall limit ourselves to noting in general that there is
hypertrophy of the ovary and an increase, often enormous, in
the number of eggs, offsetting the very considerable numbers
of embryos which are lost on account of the difficulties of
finding the host.
Parasitism thus modifies the organism very profoundly and
-it is customary to say that it results in degeneration or regres-
sion. Indeed, it leads to simplification of many organs and even
to their disappearance. But we must not forget that, on the other
hand, it causes hypertrophy <?r differentiation of other organs.
 AND PARASITISM 39
It is therefore preferable to say that parasitism results in
specialization rather than in degeneration; in short, certain
parasites, degraded in comparison with the normal members
of the group to which they belong, are marvellously adapted to
the very peculiar conditions under which they live, and the
evolution which they have undergone in departing from the
normal type is by no means a regression but progressive modi-
fication in a definite direction.
Since the modifications resulting from parasitism vary so
greatly, generalizations about them could only be vague and it
will be better to examine them in the light of certain particular
examples. We shall begin with parasites that have developed as
an exception in groups of animals that are generally free-living.
Such examples are particularly significant on account of the
clear-cut comparisons which they allow.
 CHAPTER IV

ADAPTATIONS TO PARASITISM IN
ANNELIDS AND MOLLUSCS

POLYCHLETES
ICHTHYOTOMUS SANGUINARIUS. The case with which I shall begin
will give us an idea of the first effects of parasitism. It concerns
an animal that is only slightly modified and belongs to a group
in which parasitism is very exceptional, the polychrete annelids.
This particular species, Ichthyotomus sanguinarius, was dis-
covered and studied in great detail by H. Eisig 180 at Naples; it
parasitizes an eel, Myrus vulgaris.
It is interesting to see the beginning of adaptation to para-
sitism in an annelid because this group is probably the stock
from which the Hirudinea and Myzostomaria were derived and
these consist entirely of parasites and are profoundly modified;
we can imagine, then, how their modifications arose. Besides
Ichthyotomus there are some other cases of parasitism in poly-
chretes known to us, both in the Eunicidre and in the Syllidre,
which we shall consider later. A. Treadwell has briefly described
under the name of Haplosyllis cephalata a specimen that was
discovered attached by the pharynx to the cirri of a eunicid
already preserved in alcohol. F. A. Potts 182 described as Para-
sitosyllis an annelid found under the same conditions as annelids-
and nemerteans from Zanzibar; its structure appears to be
typical but its evaginated pharynx is firmly fastened to the body
wall of the host from which it cannot be detached. It seems, then,
that in both cases it is a matter of permanent attachment to a
host by the pharyngeal region*, but it is essential that they
should be studied alive and in large numbers. This is what Eisig
was able to do under the most favourable conditions with
Ichthyotomus sanguinarius.
* The syillds are carnivorous annelIds which attack their prey byevaginating
the pharynx and perforatmg the body wall (cf. Malaqum, Recherches sur les
Sylhdiens. Mem. Soc. Sciences et Arts de Lille, 1893, p. 246).
40
 A PARASITIC POLYCH..£TE 41
This animal (the adult is 7-10 mm. long), which is firmly
attached to the fins (Fig. 8) of Myrus, and in particular to the
dorsal one, looks like an ordinary annelid with well-developed
parapodia, and it is its organ of fixation which, above all else,
deserves the most close study. This organ consists of two stylets
projecting from the mouth and turning on each other by their
articulating surfaces as they diverge (Fig. 9). The distal part
embedded in the skin of the host is spoon-shaped with a toothed
edge which holds it firmly in position. The animal bites with its
stylets close together, it then separates them from each other,
so tearing the host's skin and the walls of small blood vessels.

Figure 8. lchthyotomus san- Figure 9. The stylets forming

guinarius attached to the the organ of fixation in
fin of Myrus vulgaris /'chthyotomus (after Eisig).
(after Eisig).

It is very difficult to detach an Ichthyotomus from its host

without wounding the latter. The divergence of the stylets
ensures attachment and at the same time corresponds with a
resting state in the motor muscles; thus the animal is fixed when
it is passive and has to exert muscular contraction to free itself.
Here, therefore, is an organ of attachment that is an extremely
effective and highly specialized mechanism that can be com-
pared to the two-pronged hooks that were driven into a ceiling to
hold a chandelier. We must ask how it originated. Is it by the
continuous modification of an apparatus present in syllids
whether they are free-living or not? At the entrance to the reso-
phagus many syllids possess a tooth or a ring of teeth but nothing
42 ADAP'J' A TIONS TO PARASITISM IN ANNELIDS
resembling the apparatus of Ichthyotomus, except, it seems, in
a syllid, Gnathosyllis diplodonta, observed by Schmarda, which
has two teeth which may perhaps be analogous. Unfortunately,
the description is no more than a summary and this species has
not been found since. The mechanism by which this structure

-C
'f'"-_ _

b D

~
A tJ • '~C
Figure 10. Ellobiophrya donacis.
A, the ciliate attached by its posterior limbs to a trabecula of the
molluscan gill and bearing a bud, b, in an advanced stage of growth; .
c, aboral cilIated crown of the bud; 0, oral pole of bud; E, an isolated
individual of Ellobiophrya at the beginning of longitudinal fission
(the peristome is dividing). C, D, the junction of the two limbs under
normal conditions, and after rupture (after Chatton and Lwoff).

was achieved is mysterious: we can hardly invoke a lamarckian

explanation; these stylets are non-living structures, they have
their definitive form from the beginning-and the way they work
cannot influence their structure; the animal must make use of
them as they are; on the other hand, we cannot reasonably
accept as a matter of pure chance the sudden achievement of a
 A PARASITIC POLYCH2TE 43
piece of apparatus which is so complicated and also well suited
for attachment.* The problem will remain obscure until the dis-
covery of related forms possessing an analogous organ but one
that is less differentiated. But at present we have no knowledge
of such a case apart from Schmarda's species. And this simple
example shows how most of the morphological problems con-
cerning adaptation to parasitism present themselves; at the same

Figure 11. Anterior region of Ichthyotomus (after Bisig).

am, median antenna; ai, lateral antenna (rudimentary); c, brain; h, h<emo-
philous glands; ce, eye; ces, cesophagus; p, pharynx; s, attachment
stylets.

time it shows that parasitism is far from leading only to regres-

sion or degeneration.
Adaptation in Ichthyotomus is shown by other characters, par-
ticularly in the anterior region which is in the process of being
modified as a sucker. As the stylets tear the skin of the eel they
cause bleeding at t~e point of attachment. The polychrete gorges
* Here we have a tYPical example of what Cuenot has called coaptations. Many
cases are known amongst parasites as well as amongst free-living forms. There is
a tYPical example in a pentrich, Ellobiophrya donaels, which hves on the gills of
a bivalve, Donax vittatus, and has been thoroughly mvestigated by E. Chatton
andA. Lwoff 88. Two flexible cylindncal branches are given off from the posterior
part of the body of the peritnch; they encircle one of the trabeculre of the mol-
luscan gill, meet each other and adhere by a clampmg deVice, thus forming a firm
closed nng comparable to a padlock or to the ring on an earring (hence the name
Ellobiophrya).
44 ADAPTATIONS TO PARASITISM IN ANNELIDS

itself on the blood and at the same instant may be seen applying
to the skin of the eel its entire anterior region which becomes
concave alt1;lOugh usually it is convex. This part, forming the
temporary sucker, is the head, which in the annelids carries
special appendages, antennre, palps, etc, principally sensory in
function with well-defined nervous areas on the surface of the .
skin corresponding to them. In the syllids, which Ichthyotomus
obviously resembles, there are three dorsal antennre (one median
and two lateral) and two ventral palps. Now, on the head of
Ichthyotomus, Bisig has found the nervous areas corresponding
to these various <:tppendages, but the appendages themselves
have disappeared and the nervous areas are included in the
sucker-forming zone. Here, we can clearly grasp the modifica-
tion of the anterior extremity of the animal in relation to its
mode of life; it is obviously of a regressive nature, but at the
same time it constitutes a differentiation appropriate to its way
of life and certainly illustrates a stage of the process of modifi-
cation culminating in the Hirudinea in which the sucker has
become permanent and the primitive structure of the annelid
head has left no trace.
Ichthyotomus is an example of the blood-sucking parasites
mentioned above (p. 38) which prevent coagulation of the blood
they have ingested. Bisig has made exact observations and experi-
ments on this subject. Although the blood simply extracted from
a vessel of the fish clots very quickly, that ingested by the
worm remains liquid. The absence of clotting is due to the secre-
tion of extensive glands, the hremophilous glands, of which there
are two pairs opening to the exterior in the part of the anterior
region forming the sucker. Their secretion mingles with the
blood before it can reach the pharynx. Eisig has established bX
direct experiment their anti-coagulant action. Thanks to it the
blood remains liquid and is constantly moving in the alimentary
canal. Besides the effect that this has on assimilation, Bisig sees
in it a modification of a respiratory nature. Iildeed, the intestine
gives off extensive lateral diverticula in each segment of the
annelid and they extend even into the parapodia and cirri, con-
trary to what usually occurs in annelids. On the other hand,
Ichthyotomus has neither vessels nor gills.
The presence of hremophilous glands is an important adaptive
character; they are probably not altogether new structures.
 A PARASITIC POL YCHAnE 45
Other syllids possess glands on the head which are most likely
to be homologous with them and at the expense of which they
doubtless differentiated, both by hypertrophy and by acquiring
an anti-coagulant property in relation to parasitic nutrition.
One may imagine either that this was a gradual development or
that such a property existed in certain forms in a state of pre-
adaptation; it would then be the pre-adapted animals which
would be particularly likely to become parasites. We have not
the data to decide between the two hypotheses. The second
ranks with those readily formulated in connection with numerous
facts of evolution. The first seems to me infinitely preferable. It
ties up with the production of anti-bodies and one may well
suppose that the gradual establishment of an increasingly exclu-
sive diet of blood has induced in the organism modifications of
certain glandular secretions, which have resulted in an anti-
coagulant character. In addition, the very general occurrence
of anti-coagulant properties in blood-sucking parasites from
widely divergent groups living under the most variable con-
ditions appears to me forcibly to suggest that this physiological
character is a direct consequence of conditions of nutrition. It
seems to me that merely chance mutations are insufficient to
account for the widespread appearance of this phenomenon
amongst all blood-sucking parasites.
In addition to the hremophilous glands of the cephalic region,
Ichthyotomus possesses in each segment organs of the same
structure and probably of the same significance although, in
fact, they do not appear to be functional. Their presence is
doubtless a demonstration of the way in which the different parts
of the organism are correlated.
Eisig has shown still other effects of parasitism in this annelid.
The general musculature of the parapodia is reduced. The eyes
are small, lying beneath the skin, directly above the brain and in
a state of regression. The pharynx differs from that of a normal
syllid and corresponds to an embryonic state. The reproductive
system is clearly hypertrophied. Thus the whole structure has
been infipenced by parasitism. But the animal still retains the
characteristics of a free-living annelid and, moreover, it can
change places on its host and attach itself afresh either on the
same eel or upon another. Here we find a very interesting case
of an animal which is still becoming modified. The detailed work
46 ADAPTATIONS TO PARASITISM IN ANNELIDS
carried out by Eisig also shows how fruitful it is to combine
morphological and physiological data. Even in a case as
thoroughly investigated as this, the means by which the modifi-
cations have been brought about still remain obscure and even
if certain characters, such as hremophily, seem clearly to be
related to the functional activities of the animal, there are others,
such as the differentiation of the stylets, which are much more
perplexing unless they were the starting point from which others
were derived.
MOLLUSCS
The molluscs, like the annelids, are a group in which para-
sitism is quite exceptional but which provides a series of gradu-
ated examples leading to a degree of extreme regression, a series
which is the more significant since molluscs are animals showing
a very high degree of organization. The range of examples allows
us to imagine, by analogy, the origin of groups which have been
wholly and profoundly modified by parasitism. It shows us,
besides, that such a regression is not achieved by following along
a single linear series but by a number of separate branches origi-
nating simultaneously, with many secondary variations, and
comprising one of the most interesting fields of study in com-
parative anatomy. The behaviour of molluscs is extremely varied
but they are essentially free-living animals. There are, however,
some exceptions to this general rule amongst the bivalves and
gastropods. We shall examine them in order.

1. LAMELLIBRANCHS
The facts to be observed in this group fall rather within the
bounds of commensalism or inquilinism than those of true para-
sitism and do not involve profound changes in organization,
although this is modified to some extent. The shell is reduced
and often covered by the mantle. Hermaphroditism and incuba-
tion of the embryos have been found in most cases. The animals
so modified belong more or less obviously to the Lucinidre,
characterized in particular by the presence of a single branchial
lamella.
(a) En to valva. These are species commensal on holothurians
and especially on synaptids.
 AND IN MOLLUSCS 47
1. En to valva mirabilis, internal parasite of a synaptid from
Zanzibar, described by Vreltzkov (1890).
2. En to valva perrieri found on synaptids at Saint-Vaast-Ia-
Hogue by Malard (1903) and studied later in the same locality
by L. Anthony 330. This species is, as a rule, attached to the out-
side of the synaptid by a voluminous pedal papilla. If it is pulled
off and put in a dish near the synaptid it very rapidly attempts
to attach itself again. The foot is highly developed.
On a synaptid at Cherbourg, Herpin 341 found a small speci-
men (5 mm. long), which was perhaps a very young stage of
E. perrieri; it possessed a long appendage (2 cm.), which is
probably the foot.
3. Entovalva semperi, found in Japan by Oshima 361, also on
a synaptid, is perhaps the same species as one briefly noted by
Semper (1868) in the Philippines.
4. Entovalva major, described by A. F. Brunn 334 from speci-
mens collected by Mortensen at Ghardaqa (Red Sea) and found
by him inside Holothuria curiosa.
These different examples show that En to valva has a wide geo-
graphical distribution and represents a very stable type of a
circumscribed association between bivalves and holothurians.
(b) Montacuta. The species M. ferruginosa is common on the
French and English coasts, where it lives in the sand in direct
contact with a spatangid sea urchin, Echinocardium cordatum.
It is a well-established and regular association.
(c) Scioberetia. F. Bernard 332 described under this name a
bivalve nearly related to those above and living between the
spines of a spatangid, Tripylus, at Cape Horn. It is hermaphro-
dite and incubates its eggs. The mantle covers the shell. The
pedal and shell muscles and the foot itself are reduced.
(d) Lepton. This genus, observed by P. Fischer (1873) at
Arcachon, was rediscovered there by Ch. Perez on Sipunculus
nudus and studied by Pelseneer. It is very close to Montacuta.
(e) Ephippodonta. The species E. macdougalli, described by
Tate (1889), lives in the burrows of a crustacean, Axius plecto-
rhynchus, on the southern coasts of Australia.
I shall not go into further detail here. The anatomy of these
various types is, in short, not much modified, but their state of
commensalism or inquilinism is undoubted and their geo-
graphical range shows that it is a firmly fixed type of behaviour.
48 ADAPTATIONS TO PARASITISM IN ANNELIDS

II. GASTROPODS
The gastropods, among types that are very limited in com-
parison with the class as a whole, provide us with a series which
is both much more varied and much more marked by profound
morphological change due to true parasitism. We shall survey
it briefly.
Amongst the Pyramidellid<e Pelseneer has made known many
cases where the radula is reduced or absent, implying a radical '
change in feeding. He noted an Odostomia from China seas,
which uses its proboscis to perforate the mantle of a Tellina;
ano,ther species belonging to the same genus has an analogous
relationship with the pearl oyster (Pinctada margaritifera).
Finally, he has demonstrated that on French coasts species of
Odostomia live under similar conditions: O. rissoides at the
expense of the common mussel, and O. pal/ida on Pecten. They
drive in their long proboscis when the valves are slightly open
and suck at the mantle of these bivalves. The radula has disap-
peared; otherwise they are little modified.
But the most significant facts are those provided by a series
of gastropods parasitizing echinoderms, which have often under-
gone considerable modification. They belong to the families
Capulidre, Eulimidre, Entoconchidre, and Predophoropodidre.
Most of them are tropical species and comparatively rare. They
are summed up in the table on the next page.
1. CAPULID1E. These are trenioglossid prosobranchs with a
shell that is slightly coiled or in the form of a simple incurved
cone. They are now represented by the genus Thyca that has
been found on various starfish and they are relatively little modi-
fied. In Fig. 12B the drawing of T. ectoconcha gives an idea' of
organization in this genus. It shows that on the whole this
gastropod is still normal in structure. The modifications affect
the peribuccal region and the foot. The latter (rp) is reduced and
no longer displays an operculum. The peribuccal region has
developed as a large disc (pseudo-foot dj), making a kind of
sucker by which the animal adheres to the host. From its centre
projects the proboscis which thrusts through the tegument of
the starfish (Linckia). The proboscis, slightly' developed in
T. ectoconcha, is very long, three times the length of the body,
in T. cristallina. The radula has completely disappeared, imply-
 AND IN MOLLUSCS 49

Family Genus No. of Host Locality

species
. Indian Ocean, Malay
Capulidre Thyea 5 Starfish (Linekia)
Archipelago
Platyeetas 7 Fossils (Silunan~
Triassic) on cn-
noids and star-
fish
Eulimidre Eulima* Crinoids, starfish
Robillardia Sea urchin Indian Ocean
Mlleronalia Sea urchins, Malay Archipelago
ophiuroids, and Indian Ocean
starfish and
holothunans
Styli/ert Starfish, OphlU- Ceylon and Malay
roids Archipelago
Megadenus 4 Holothurians Bahama, ZanzIbar
Rosenia 1 Sea urchin North Sea
Pelseneeria 1 Holothunans Azores
Gasterosiphon 3 Holothurians Indian Ocean
Diaeolax 1 Holothurians Falkland Isles
Entocon- Enteroxenos 1 Holothurians Norway
chldre
Thyonicola 1 Holothurians Cape of Good Hope
Entoeolax 3 Holothunans Benng Sea
Entoconeha 2 Holothurians Adriatic (Trieste),
PhilIppines
Predophor- PlRdophoropus 1 Holothurians Sea of Japan
opodidre
? Asterosiphon 1 Starfish Japan
Ctenoseulum 1 Starfish Hawaiian Isles

* A fair number of species of Eulima have been described by malacologists

from empty shells found in isolation, which could have come from either free-
living or parasitic forms.
t The remark on Eulima applies here too.
ing that the food is liquid and is sucked up. The species with a
long proboscis have also enormous salivary glands, while the
intestine and liver are reduced.
T. stellasteris (Fig. 12A), thoroughly investigated by Krehler
and Vaney, is the least modified species. The proboscis is rudi-
mentary and the foot retains an operculum. The animal must
move about on its host.
In these various species the sexes are separate; the male is
clearly smaller than the female (Fig. 12A), and there is a certain
amount of dimorphism in the shell, very marked in T. cristallina,
where in the male it is turriculated and in the female simply
cupular.
50 ADAPTATIONS TO PARASITISM IN ANNELIDS

Adaptation of the Capulidre to parasitism of echinoderms is

very long-standing, since, from the Devonian to the Triassic,
there are many forms comprising the genus Platyceras, with a
shell recalling that of Thyca, attached to the anal region of
crinoids. From 1888 onwards Keyes described a dozen species.
Later (1920), A. O. Thomas 369, when describing P. inopinatum,
noted the perfect adaptation of the shell margin to irregularities
on the .Surface of the crinoid. The occurrence of these very

... ~-.--,~ .
.B d/""~ __

Figure 12. Thyca steTlasteris and T. ectoconcha.

A, sexual dimorphism in Thyca stellasteris (after Krehler and Vaney).
B, anatomy of Thyca eCloconcha (after P. and F. Sarasin); br, gill; c, braiq;
i, intestine; m, mantle; IE, eye; ot, otocyst;pd, pedal ganglion; rp, foot;
rj, frontal fold; dj, pseudo-foot; bp, pharynx; Ir, proboscis .

•
ancient forms indicates that the parasitic capulids have passed
through long geological periods of more recent date without
showing any marked evolution.
2. EULIMIDlB. This is a family allied to the Trenioglossa but
lacking a radula (Aglossa). The shell is generally thin and trans-
lucent.
(a) Eulima is represented by a rather numerous assortment of
small species whose turreted shells are common enough in the
 AND IN MOLLUSCS 51
littoral zone of our coasts. Certain Eulima, such as E. polita,
still have a radula and are perhaps free-living. E. distorta, found
on the coasts of Norway, is commensal or perhaps parasitic in a
holothurian. Related species have been found in the alimentary
canal of holothurians in Fiji and the Philippines where Semper
has found them alive, creeping on the inner surface of the host's
intestine. Three plainly parasitic species have been found:
E. ptilocrinicola attached to an abyssal crinoid, Ptilocrinus pin-
natus; E. capillastericola found at the base of an arm of Capil-
laster multiradiata at Singapore; and E. equestris on an arm of
Stellaster equestris. This last species has been minutely studied
by Krehler and Vaney 348. It is a case of a true parasite which
thrusts its long proboscis into the host, penetrating the general
body cavity and acting as a sucking organ,. Its anatomy is, on
the whole, little modified; however, the foot is much reduced.
The sexes are separate.
(b) Pelseneeria (a genus with which Vaney has fused the genus
Rosenia) is comprised of species living on sea urchins and lacking
a radula. One of these species, P. styli/era, has been found living
on sea urchins in the North Sea. It moves about among the
spines of its host but without leaving it to lay its eggs. Krehler
and Vaney have described three species, P. profunda, P. media
and P. minor, from the dredge-hauls of the Princesse Alice. In
these the proboscis is thrust through the test of the sea urchin.
In P. profunda the mouth is surrounded by a large collar, with
an irregular jagged border, partly covering the shell; we shall
find this structure more or less developed in the following genera
where it is known as the pseudopallium. It is a newly acquired
adaptive structure, apparently derived from the epipodium. The
foot is quite well developed but has no operculum. There is no
radula. Pelseneeria species are hermaphrodite. With the excep-
tion of these characters their general anatomy is unmodified.
(c) Megadenus now includes four species: M. holothuricola,
and M. w:eltzkowi living in the respiratory trees of holothurians;
M. cystico[a, found by Koehler and Vaney, producing thick-
walled galls on the spines of a sea urchin, Dorocidaris tiara, in
the Indian Ocean; and M. arrhynchus, found by A. V. Ivanov 345
on a starfish, Anthenoides rugulosus, in the Yellow Sea, where it,
too, forms a kind of gall on the dorsal surface of the host. In the
first two species there is a long proboscis, buried in the general
52 ADAPTATIONS TO PARASITISM IN ANNELIDS
body cavity of the host (M. arrhynchus lacks this, according to
Ivanov). M. cysticola likewise has a proboscis. There is no oper-
culum on the foot. A pseudopaUium covers part of the shell
round the mouth. The shell itself is turreted. Here, the sexes
are separate and the animals are found in pairs, the male being
the smaller (this is so in each gall containing M. cystico!a), with
the eggs nearby.
(d) Mur;rcfnalia. This genus includes rather a large number of
species vn the single expedition of the Siboga six were collected)
attached to sea urchins, ophiuroids, starfish and holothurians.

Figure 13. Mucronalia palmipedis (after Krehler and Vaney).

op, operculum; ps, pseudopallium; It, tentacles; Ir, proboscis.

The shell is well developed, as in the preceding genera, and'

terminates apically by several whorls which form a small cylin-
drical mucro. In this case, the operculum persists on the foot
which itself is somewhat reduced. There is a long proboscis,
without a radula, thrusting into the general body cavity of the
host. On the other hand, the pseudopallium is very little differen-
tiated. The sexes are separate. The anatomy remains clearly
normal. It appears that these parasites always remain attached
to one part of the host. Details of sexual phenomena have not
been investigated up to the present.
M. variabilis, a parasite of Synapta sop lax in Zanzibar, has
 AND IN MOLLUSCS 53
sometimes been found within the alimentary canal, sometimes
on the external surface. It is a very variable species, primitive in
some respects, modified in others. One aspect of modification
which is of particular interest in connection with the following
forms is the important regression shown by the alimentary
canal. The proboscis pierces the intestinal wall of the synaptid
and the parasite feeds by sucking up the host's crelomic fluid.
There is neither a radula nor salivary glands. One cannot find
stomach or liver, and from the resophagus there leads only a
short canal ending blindly without an anus. The sensory organs
remain; the eyes, which are very variable, tend to be buried
under the skin. The animal is hermaphrodite. These different
characters are very inconsistent, as is the behaviour of the
animal.
In this genus, Mucronalia, the modifications undergone xary
markedly from one species to another and these do not form a
single plain series.
(e) Stylifer. This genus, too, contains a series of species some
of which have been known for a long time. It is fairly closely
allied to Mucronalia, but the foot, much reduced, has no oper-
culum. The shell is thin and merely corneous. In certain species,
S. celebensis, S. linckiCE, the pseudopallium is very greatly
developed (Fig. 14ps) and completely covers the shell; the animal
is enveloped in it. A comparatively long proboscis, lacking a
radula, penetrates into the crelom of the host and sometimes
spreads out into a large terminal swelling. The alimentary canal
shows degeneration, notably in the liver which is rudimentary
or completely absent. Four species of Stylifer are known. One,
S. sibogCE, is hermaphrodite; in the others the sexes appear to be
separate, and this is certainly so in S. linckiCE. This genus is
altogether interesting, particularly on account of the further
development of the pseudopallium and the reduction of the foot.
On the whole, anatomically, it does not diverge very far from
the normal.
The various genera that we have just considered are fairly
close to one another and represent multiple variations of the
'genus Eulima. They retain the fundamental anatomy of the
prosobranchs. _
(f) Gasterosiphon. The modifications due to parasitism be-
come much more striking in this genus, of which two specimens
p.s.-3
54 ADAPTATIONS TO PARASITISM IN ANNELIDS
have been found by Krehler and Vaney 348 in an abyssal
holothurian, Deima blakei, in the Indian Ocean. They are of
great interest as they clearly relate the Eulimidre, which we have
dealt with, to the Entdconchidre which we shall come to later.
Gasterosiphon deimatis (Fig. 15) is an internal parasite remain~
ing in contact with the outside world by means of a small
opening passing through the skin of the holothurian. Examina~
tion of the general body cavity of the latter shows a slender duct

Figure 14. Anatomy of Stylifer linckice (after P. and F. Sarasin).

br, gill; gb, buccal ganglion; gc, cerebral ganglion; (E, eye; ot, otocyst;
(ES, <:esophagus; p, foot; ps, pseudopallium; tr, proboscis.

leaving this opening; this is the siphon, s, which is about 10 mm.

long and leads to an ovoid swelling of from 5 to 10 rum., from
which there continues a second duct, also thin and very long
(104 mm. long and 0·7 mm. in diameter); this second duct is
attached distally to the marginal vessel on the intestine of the
holothurian and is homologous with the proboscis of the pre-
ceding genera, but very highly developed. The parasite feeds by
imbibing the blood of its host.
 AND IN MOLLUSCS 55
If one opens the swelling connecting the two tubes (siphon
and proboscis) one finds (Fig. 15B) within it a clearly recog·
nizable gastropod although manifestly degenerate. The shell has
completely vanished but a visceral hump remains and there are
vestiges of the foot,p. There is nothing to be seen of the cephalic
tentacles, nor of the true mantle, the gills, kidney or heart. The
central nervous system is, on the other hand, retained as a whole
and condensed. The <:esophagus leads into a gastric cavity, st,
from which there ramify ducts constituting a hepato-pancreas.

'-.
....
-
:-':::~)-

Figure 15. Gasterosiphon deimatis (after Krehler and Vaney).

A, the whole parasite, B, its anatomy; po, egg masses; ps, pseudopaUium;
s, siphon; fr, proboscis; (l!S, resophagus; eer, brain; I, blood lacuna;
ot, otocyst; p, foot; eg, oviduct; t, testis; OV, ovary; sf, stomach;
eoq-ps, pseudo-pallial shell calcIfication; th, body-wall of host.

There is neither intestine nor anus. The animal is hermaphro·

dite. Ovary, OV, and testes, t, are two distinct glands, but the
ducts unite. Round the visceral mass the cavity of the swelling
in which it is enclosed is :filled with developing embryos. The
outer wall of this swelling is none other than the pseudopallium
enormously developed. In Sty lifer linckice it totally encloses
the animal, which no longer communicates with the outside
except by a narrow aperture. Here the pseudopallium has
56 ADAPTATIONS TO PARASITISM IN ANNELIDS
developed further and is enclosed within the narrow duct which
forms the siphon and maintains communication with the external
environment. A slender peripheral calcareous ring ensures that
the end of the siphon remains open.
In spite of the/"magnitude of the changes that have taken place
Gasterosiphon--is readily linked with Sty lifer and to all the pre-
ceding exarriPles.
(g) !?iacolax. This genus was described in 1945 by Mandahl-
Barth 356 from a single specimen found on a holothurian, Cucu-
lrJaria mendax, in the Falkland Islands. It is an external parasite.
The pseudopalli1;lm completely covers the body, forming an
ovoid mass terminating in a point, the siphon. The anterior
extremity of the animal penetrates far into the general body
cavity of the holothurian. The visceral mass (in the midst of the
pseudo-pallium) consists only of the intestine surrounded by the
ovary. There is no longer a shell. Within the cavity of the pseudo-
pallium there are numerous groups of eggs in various stages of
development. Segmentation is total and spiral. The veliger larva,
resembling that of Entocolax and Pcedophoropus, has a thin
hyaline shell, slightly thickened at the peristome and with a
greatly flattened apex.
Diacolax, according to Mandahl-Barth, would be the culmi-
nation of the Eulimidre series (Eulima-Mucronalia-Stylifer-
Gasterosiphon-Diacolax).
3. ENTOCONCHlDlE. The genus Gasterosiphonis of particular
interest in that it provides a solid basis for interpreting types
that are much more degenerate than the Entoconchidre. In fact,
Schiemenz had, before the discovery of Gasterosiphon, inter-
preted these types fairly correctly although his grounds for
doing so were purely conjectural. Knowledge of Gasterosipho1:l
gave him a solid foundation of fact.
Anatomical degeneration in the Entoconchidre is so con-
siderable that it was the cause of a mistake in interpretation
which remains historically significant. In Trieste, in 1851, Joh.
Muller, studying the genital glands of a holothurian, Synapta
digitata, found that in their vicinity there were in certain animals
some long and unbranched ducts containing embryos I
and veliger
larvre of gastropods. He gave to these larvre the name of Ento-
concha mirabilis, but explained their presence by a most singular
hypothesis, suggested by the idea, then becoming current, of
 AND IN MOLLUSCS 57
alternating generations. In fact, he believed that he had come
across a case of this kind involving molluscs and holothurians,
and that Synapta itself was producing the gastropod larvre. *
He missed the explanation, in reality so simple, of its being a
case of parasitism; but it must be pointed out that there is no
indication of molluscan structure in the ducts containing the
veligers and, further, at that time none of the examples given
above was known. It was Baur who, in 1861, on returning to'the
study of the holothurians of Trieste, showed that it was indeed
a case of parasitism.
Since that time two genera analogous to Entoconcha have
been discovered in holothurians: Entocolax, first met with in
synaptids from the Bering Sea, and Enteroxenos in Stichopus
tremulus, from the coasts of Norway. Enteroxenos has been
thoroughly investigated, even cytologically. Degeneration in
these three types (Entoconcha, Entocolax and Enteroxenos) is
extreme. They are reduced to simple vermiform tubes where,
practically speaking, there is no trace of molluscan structure;
the larvre alone allow of the identification of the group.
(a) Entocolax is now represented by three species which are
internal parasites of holothurians: E. ludwigii in Myriotrochus
rinkii (Bering Sea), E. schiemen~i in Chiridota pisanii (Chile),
and E. trochodotce in Trochodota purpurea. We owe the correct
interpretation of the anatomy of the genus to Schiemenz 366.
One end of the animal is fixed to the skin of the host. An
initial tubular section swells out into a vesicle from which is
given off a long narrow duct floating freely in the geberal body
cavity of the holothurian (Fig; 16A). This last duct is none other
than the proboscis, with the cesophagus, res, which at its proxi-
mal extremity enlarges to form a kind of blind stomach, ih,
abutting against a mass of tissue within the base of the vesicle;
within this mass, which juts out into the vesicular cavity, one can
recognize ovary, oviduct and uterus. The eggs fall into the cavity
and develop there. Now that we are familiar with Gasterosiphon,
the vesicular swelling and the duct which attaches it to the skin
of the host can be interpreted as a highly developed pseudo-
pallium. But the visceral mass, which in Gasterosiphon still
.. Hreckel made a similar mistake, though less extreme, In connection With
certain medusre, Cunina, which develop as parasites in other medusre, but which
he believed to be a stage in the life cycle of the latter.
58 ADAPT ATIONS TO PARASITISM IN ANNELIDS

contains the typical organs of a gastropod, is here reduced to

the ovary.
Reding 339, in 1935, made known a third species of Entocolax,
E. trochodotce close to the preceding ones, and he recognized
X
dwarf males (he found seven) attached to the inner surface of
the pseudopallium within the vesicular cavity; similar males had
been discovered earlier by Schwanzwitsch 367 in E. ludwigii.
The eggs develop freely in the cavity of the pseudopallium and

.s •• d
CIa" .t

.p8

,
.~.zh
A

Figure 16. Structure of Entocolax (A), Entoconcha (B) and Entero-

xenos (C) (after Vaney).
ct, ciliated canal; ilz, hepatic intestine; od, oviduct; (J!S, cesophagus;
ps, pseudopallium; s, siphon; t, testis; en, sheath of the host's peri-
toneum (enveloping Enteroxenos); viz, ventral vessel of the host's
intestine. .

give rise to veliger larvre of typical gastropods, with shell, velum

and foot.
It is clear that Entocolax shows marked regression in com-
parison with Gasterosiphon, and in particular with the other
genera of Eulimidre that we have considered.
(b) Entoconcha provided J. Muller and Baur with relatively
abundant material and it would be interesting to study this
genus again, using modern techniques. We can still count on
finding it in the Adriatic. E. mirabilis occurs (Fig. 17) in Synapta,
in the shape of thin cylindrical tubes without any swelling and
 AND IN MOLLUSCS 59
attaining a length of up to 80 mm. They are attached by one
end, the proboscis, to the ventral vessel of Synapta. From the
point of attachment three successive regions can be distin-
guished: the first is the proboscis; the mouth (b) of the parasite
is buried in the ventral vessel, VV, of the host; the digestive appa-
ratus is reduced to a simple tube, the resophagus, which extends
for about a third of the total length and ends blindly. At the end
of this section there is a partition enclosing the ovary and sepa-
rating the resophagus from another cavity which extends the
whole length of the distal region and in which the embryos and

Figure 17. Entoconcha mirabilis (after Baur) and its relationships

with the host.
b, mouth, fixed to the ventral vessel,
VV, of the host's intestine; i, intestine;
ov, ovary; ps, pseudopallium; vo, masses of developing eggs; t, testes;
cl, ciliated canal.
larvre are found. It corresponds as a whole to the median
swelling and siphon of Gasterosiphon and Entocolax. But here,
at least as far as one can judge from the old descriptions, organic
regression has gone even further. Of the viscera of the mollusc
only the ovary remains. A group of small vesicles, varying in
number and with a contractile wall, juts out into the siphon
towards its distal extremity and is considered to be the testis.
In the light of the more recent observations made by Reding 339
on Entocolax, we may ask whether these so-called vesicles are
not, in fact, dwarf males, attached at this point.
60 ADAPT A TIONS TO PARASITISM IN ANNELIDS

(C) Enteroxenos. The adults are tubular and 100 to 150 nun.
in length, lying free in the general body-cavity of the holo-
thurian, Stichopus tremulus. The young stages are attached to
the outer surface of the anterior region of the intestine (Fig. 18).
Younger stages have even been found completely enclosed
within the w~ll of the resophagus. It is the most degenerate of
all the parasitic gastropods. The tube constituting it shows,
indeed, only a single axial cavity extending along its whole
length \Fig. 16C); it terminates blindly at its distal end and opens
by a slender canal on the proximal side. The ovary lies in the
wall of the central canal, the testis at one end. We can no longer
distinguish either proboscis or a distinct alimentary canal, at

Figure 18. Part of the gut of Stichopus bearing individuals of

Enteroxenos of various sizes (after Bonnevie).

any rate in the stages studied. The whole length of the animal
seems to correspond to the pseudopallium. The parasite is thus
reduced to a sac of embryos no longer showing any trace of the
primitive structure of a mollusc.
On the other hand, the larVa! of these degenerate types imme-
diately reveal their nature. They are typical veligers, with a
coiled shell, velum, visceral hump, foot, operculum, nervous
system and otocysts (Fig. 19).
(d) Thyonicola. This genus was described in 1941 by Mandahl-
Barth 355 from a species Thyonicola mortenseni, found inside an
abyssal holothurian, Thyone secreta, collected in the vicinity of
the Cape of Good Hope. As many as 30 and 40 parasites (from
 AND IN MOLLUSCS 61
a few millimetres to 7-8 centimetres in length) were found in the
same host. The large specimens formed compact tangled knots.
They are tubular, long and narrow, and fixed by their anterior
end to the intestine of the holothurian. There is no trace of
intestine nor of other organs. At the anterior extremity there is
a testis, at the posterior one an ovary. Within the tubes the eggs
are incubated by thousands. The veliger larva possesses a tiny
coiled shell and an operculum. Mandahl-Barth observes that in
many ways this parasite resembles Enteroxenos rentergios.*
At present we know only six species and four genera of Ento-
conchidre. It is to be presumed that others exist. These four
genera, Entocolax, Entoconcha, Enteroxenos and Thyonicola,
while displaying great similarity in general, nevertheless differ
much in their structure and their relations with the host. They

V op gB
Figure 19. Veliger larva of Entoconcha. A, external aspect.
B, optical longitudinal section (after Baur).
b, mouth; g, pedal gland; i, gut; op, operculum; ot, otocyst; s, sac-like
invagination; v, residual yolk; ve, velum.

cannot be regarded as being directly derived from one another.

They belong rather to parallel series, having evolved indepen-
dently, and the broadly similar conditions of parasitism have
led to their general convergence. Knowledge of Gasterosiphon
suggests that they may be derived from the Eulimidre, but,
starting from types such as Thyca, other forms have been able
to develop which are equally degenerate and more or less similar.
Here let us briefly consider two other types of gastropods
which are also very degenerate and were discovered on echino-
derms collected by the Albatross: one, Ctenosculum hawaiiense,
of< On account of their being hermaphrodite, Mandahl-Barth puts forward the
possibilIty of affinity between the Enteroxenidre and the Opistobranchia. I will
confine myself here to drawing attention to thiS suggestion, which appears to me
to be scarcely plausible.
3*
62 ADAPTATIONS TO PARASITISM IN ANNELIDS
described by Heath 338 from a starfish, Brisinga evermanni, near
the islands of Hawaii; the other by Heath and Randall 362 as
Asterophila japonica from a Pedicellaster in the Sea of Japan.
Ctenosculum produces on the arms of the starfish a type of gall
provided with an external opening; Asterophila is entirely
immersed in the crelom of the arm and is attached to the wall of
the latter by a filament; it has no means of communication with
the exterior. These are highly modified forms but they are less
degenerate than the preceding ones. The globular body is entirely
surrounded by a pseudopallium. In both there are vestiges of
typical molluscan organs (complete alimentary canal, radula,
liver, foot). We may consider, without stressing it further here,
that they belong to a series clearly distinct from those discussed
above. Ctenosculum is hermaphrodite.
4. PAlDOPHOROPODIDJE. Finally, there is another type of
parasitic gastropod, Padophoropus dic{plobius, living within holo-
thurians and quite distinct from the preceding molluscs. It is
found either in the Polian vesicles or in the respiratory organ of
Eupyrgus pacificus in the Sea of Japan, and has been thoroughly
investigated by A. M. Ivanov 346. He was able to examine a
dozen specimens (7 females, 5 males). These parasites (Fig. 20)
live in pairs, the male on the right side of the female. Both
sexes possess a long proboscis which is applied to the alimen-
tary canal of the host. The body itself forms a conical mass at
the base of which the organs of the head may be seen. There
is no trace of the shell. The male has a very large penis.
Within the visceral mass are the principal systems of gastropod
organs (digestive tube and related structures, nervous system,
kidney, ovary or testis). There are, however, neither gills nor
heart, and there is no structure to be seen that corresponds with
the pseudopallium. The foot is produced into right and left
lateral lobes; in the female these join along the middle line,
forming an enormous spherical sac, opening ventrally, within
which the embryos are incubated. The musculature of this foot
is rudimentary. The larvre have the typical and highly differen-
tiated structure of a gastropod, with a dextral shell which is thin
and transparent, an operculum, a voluminous foot with two large
glands (anterior and posterior). Padophoropus thus constitutes a
type clearly distinct from the preceding ones and Ivanov has very
properly created a new family for it, the Predophoropodidre.
 AND IN MOLLUSCS 63
LAMELLARIIDlE. In conclusion we must mention a type of
molluscan parasite, Pseudosaeeulus okai, described by Hirase
from material collected by the Albatross and found in the depth
of the test of some ascidians, AseMia prunum and Boltenia
ovifera, forming a type of gall open to the exterior. All things
considered, the anatomy of these animals does not show any
clear mark of parasitism. Hirase has been led to relate them to

Figure 20. Pcedophoropus dic{p/obius (after A. W. Ivanov).

A, young female (left side), B, adult female (right side), C, male (ventral
surface); c, cephalic region; d, brood pouch (early age); g, genital
regions (<jl); 0, orifice of the pedal gland; og, region of the genital
opening; p, p', right and left lobes of the foot; Tr, penis; SV, visceral
sac; t, tentacle (rudimentary); tr, proboscis.

the Lamellariidre. If one considers that Lamellaria lays its eggs

in batches in the depths of colonies of compound ascidians,
where they appear as a kind of gall in which the embryos
develop and from which they emerge as larvre, and if, on the
other hand, one remembers that Pseudosaeeulus has been found
in groups of eleven and nineteen individuals in one gall, one is
led to ask whether here we have simply a case of a gastropod
close to Lamellaria laying its eggs in batches from which the
64 ADAPTATIONS TO PARASITISM IN ANNELIDS

young escape in a very advanced stage, and whether it would

have been these late larvre, just about to escape, that the
Japanese writer had before him.

I have thought it essential to examine in some detail these

different cases of parasitism in molluscs, and especially in the
gastropods, because they appear to me to demonstrate with
particular significance the changes which may be determined by
parasitism. In them the starting point may clearly be seen and
from Thyca to Sty lifer and in the Entoconchidre we have been
able to gauge the'extent to which these modifications occur and
the morphological degeneration that results from them. On the
other hand, it is clear that in a given group parasitism is not a
one-way track but that starting from the same general initial type
it can lead to completely independent modifications, differing
profoundly from one another. Particularly suggestive, to my
mind, is the formation and progressive development of the
pseudopallium in the Eulimidre and the Entoconchidre and its
total absence in Fcedophoropus where, on the other hand, we
find the foot modified and hypertrophied to form a brood pouch.
As I have already said, it is probable that other types of gas-
tropod parasites, whether members or not of the preceding
series, still remain to be discovered. In this chapter I have left
on one side the facts relating to temporary parasitism occurring
amongst the bivalves belonging to the Unionidre. They are of a
special type and we shall return to them later.
 CHAPTER V

ADAPTATION TO PARASITISM IN THE

CRUSTACEA

IN the preceding chapter the molluscs have provided lis with a

graduated series of significant examples showing morphological
degeneration under the influence of parasitism. We shall meet
with the same kind of facts amongst the Crustacea, a group
which, like the Mollusca, is essentially composed of free-living
forms. But here, in the different orders and families, the cases of
parasitism are much more numerous and extend to whole
groups, families or collections of families, with varying degrees
of adaptation. Considering the almost geometrical type of mor-
phology amongst these animals, we shall find that the resulting
malformations are highly significant and interesting to analyze.
Let us first, from a general point of view, look at the way in
which parasitism has extended into the different subdivisions of
this class.
Among the Entomostraca there are several groups of parasites.
1. CIRRIPEDIA. Amongst these are the Rhizocephala para-
sitizing other Crustacea, and the Ascothoracica parasitizing
crelenterates and echinoderms. These two groups are entirely
composed of parasites and are both profoundly modified.
2. COPEPODA. This enormous order includes many families,
consisting for the most part of free-living forms but with many
members adapted to parasitism on a great variety of hosts and
therefore more or less modified, sometimes very considerably.
The Malacostraca include the following:
3. AMPHIPODA. In this order there is only one isolated case
of parasitism, that of Cyamus, the whale lous~, which lives as a
parasite but is little modified.
4. ISOPODA. This order provides us with examples of adapta-
tions to parasitism that are varied and more or less profound in
extent in the Gnathiidre, which are parasitic in the larval stages
6S
66 ADAPTATION TO PARASITISM IN THE CRUSTACEA
and free-living as adults; in the Cymothoidre which, are external
parasites of fish, and, above all, in the Epicaridre, which para-
sitize other Crustacea; they particularly hold our attention on
account of the diversity and extent of their modifications.

ISOPODA
GNATHUDlE. Amongst the Isopoda the Gnathiidre comprise
a sub-order of a highly specialized and homogeneous character,
from the point of view of both morphology and behaviour.
They have been the subject of exhaustive research by Monod 255.
During the course of development they are for a time parasitic
on fish and suck their blood. At the end of this phase, that is
when they are adult, they are free-living and show considerable
sexual dimorphism, so much so that for a long time the males and
females of a single species were placed in different genera: the
males in Anceus Risso 1816 and the females and young of both
sexes in Praniza Leach 1817. The adult female was first des-
cribed as Gnathia by Leach (1813), a name which is still valid
on account of the law of priority. It was E. Hesse 246, who, in
1885, showed that Praniza was a young stage of Anceus*. The
generic name of Gnathia was restored to priority in 1880 by
Harges.
The larva, as in all isopods, has all its segments differentiated
when it hatches; it swims about, soon attaching itself to a fish
and sucking its blood; this produces hypertrophy of the third,
fourth and fifth thoracic segments and leads to the praniza
form. The host species is very variable, and also the place of
attachment. The skin of the fish is pierced by the first pair of .
maxillre and the mandibles serve to fix the parasite in place.
Monod calculates that the parasitic phase lasts for six months.
Metamorphosis of the male into an anceus form, and of the
female into a gnathia, occurs after the parasites have left the
host; it is much more extensive in the male than in the female.
The adults live in holes dug out in the mud of estuaries, or within
hollows such as empty Balanus shells, where they form small
>I< "On 19th August, 1852, I collected from a Trigia hirundo aPran'iza which, as
usual, I was eager to paint in order to record its exact shape and colouring. As I
was obliged to be away from home for a few days I kept it lh seawater instead of
putting it into alcohol as I always do. On my return my first thought was to Visit
my Praniza; but, what was my astonishment to find it replaced by an Anceus."
(Hesse 247, p. 235.)
 CYMOTHOIDlE 67
communities usually consisting of one male and a series of
females. The embryos develop within the body of the female,
which gradually swells up. The blood ingested during the para-
sitic phase still fills the creca of the intestine.
Parasitism is thus limited to the larval stages and so comes
into the category of protelean parasitism which we shall con-
sider later.

A D B
Figure 21. Gnathia maxillaris.
A, adult male (anceus form). B, adult female (praniza form). C, larva
(praniza form). D, larval mandibles (after G. o. Sars).

CYMOTHOIDlE. This group ofIsopoda has been divided into

some ten families of which two (JEgidre, Cymothoidre, sensu
stricta) have some parasitic characters. The JEgiclre are com-
mensals or inquilines rather than true parasites, e.g. ./Ega
spongiophila in Euplectella aspergillum. However, many species
live on the skin of fishes, where they attach themselves by means
of the hooked terminal segments of their anterior limbs; the
posterior limbs remain clearly ambulatory. The mouth-parts are
modified for piercing, plainly an adaptation for parasitism.
The Cymothoidre are much more obviously parasites. They
are sedentary on the skin of fishes. One genus, Ichthyoxenus, of
which four species are known, even lives in a special cavity, con-
structed so that it passes through the body wall of the host and
bulges into the general body cavity. Inside this sac there are
always two individuals, a male and a female, which must have
made their way in while young and have completed their growth
68 ADAPTAT,ION TO PARASITISM IN THE CRUSTACEA
there. Most of the Cymothoidre change their sex, a peCUliarity
which is probably due to parasitism. On the whole, their struc-
ture is but little modified.
EPICARIDlE. There is a very different state of affairs in the
case of the Epicaridre, which have a special interest for us on
account of the often considerable extent and diversity of their
modifications: resulting from adaptation to parasitism on various
groups of 6ther CFustacea. They have been the subject of a great
deal of research, some of the most valuable being that of
A. Giard and J. Bonnier, between 1880 and 1900. Facts estab-
lished by them remain valid for us today; certain details
have, however, been determined or corrected in more recent
works.
One of the difficulties in studying the Epicaridre is that very
often the only available specimens are few in number and pre-
served in alcohol, since they come from museums or material
collected by oceanographical expeditions. In many accessible
localities they are usually rare animals, but this is not a case
of absolute rarity, and a certain species which is extremely
uncommon in some places is very abundant in others. I shall
give two examples of this: Hemioniscus balani, a parasite of
Balanus balanoides which in the English Channel covers the
rocks in the upper part of the intertidal zone, and Portunion
mamadis, an internal parasite of the common crab, Carcinus
manas. At Wimereux, Giard and Bonnier examined tens of
thousands of these two hosts, but were only able to collect one
or two Hemioniscus and a very occasional Portunion. But in th~
vicinity of the Cape de la Hague, F. Mesnil and myself 228 were
able to collect large numbers of all stages of Hemioniscus with-
out any difficulty, and recently Veillet 278 collected quantities of
Portunion, also in all stages, near Sete, in the lagoon at Thau.
It is only under such conditions that one can elucidate the
details that are still obscure.
The Epicaridre comprise well-defined types, very different
from each other and profoundly modified, each type corre-
sponding to a definite group of hosts. There has been special
adaptation to each group. In the Epicaridre this has resulted in
a series of highly individualized families that we shall now
review. But first we shall examine the fundamental unity of the
sub-order which is clearly apparent from the strictly uniform
 EPICARIDJE 69
character of its larval types. Here we have a striking case of
evolution brought about under the influence of parasitism.
There are three consecutive stages: epicaridian, microniscan
and cryptoniscan. The eggs, as in all the isopods, are incubated
by the female, either externally, beneath the thorax in a cavity
bounded by the brood lamellre which are the epipodites o~ the
thoracic limbs, or (in the Cryptoniscidre) in a special cavity,
which develops at sexual maturity, within the body of the female.
This double arrangement also occurs amongst the free-living
Isopoda.
(a) Epicaridian phase. The larvre hatch in the epicaridian
stage (Fig. 22) and appear as typical small isopods like Spha-

Figure 22. Epicarid larva of Cancricepon elegans (after Giard and

Bonnier).

roma or Cymothoa, with all the thoracic and abdominal seg-

ments and appendages well defined, and apparently normal.
Their parasitic nature is, however, shown by the hooked extre-
mities of the thoracic limbs and more especially by the mouth-
parts modified as stylets for piercing (Fig. 24C). This larval
type is common to the whole family and is perfectly uniform.
After hatching they swim actively and are part of the surface
plankton.
(b) Microniscan phase. I was the first to have the oppor-
tunity of seeing, in living laboratory material 225, how these
epicarid larvre, when placed in contact with other planktonic
animals, rapidly attach themselves to copepods, as Acartia,
70 ADAPTATION TO PARASITISM IN THE CRUSTACEA
Calanus, etc. (Fig. 23). It had already been observed that micro-
niscan stages were pr~sent on copepods in plankton samples,
but Giard and Bonnier, in particular, believed that these were
autonomous Epicaridre, localized on copepods. However,
G. O. Sars had suggested that Microniscus was simply a stage in
the development of various Epicaridre.
Microniscan larvre metamorphose on the copepod which
carries them while they are undergoing their moults. Caroli 223
was able to follow these in detail in an aquarium. The epicari-

Figure 23. Microniscus stage, on Calanus elongatus (after

G. O. Sars).

dian larvre of lone thoracica, a parasite of Callianassa stebbingi,

were placed in contact with planktonic copepods to which they
attached themselves, and Caroli was able to watch the changes
by which in two successive moults and after six or seven days
they achieved the larval form known as crypto:niscan; this larva
leaves the copepod and is free swimming.
(c) Cryptoniscan phase. This third larval type (Fig. 24A) is
much more slender than the epicarid and, like it, is very regular
in character throughout the Epicaridre. It, too, has the structure
and appearance of a free-living isopod, swims actively, and is
 EPICARIDlE 71
frequently found in pelagic samples. All the thoracic and abdo-
minal appendages are present and normal in structure; the
mouth-parts retain their piercing and sucking character. It is
this larva that seeks for and attaches itself to the final host, or
the planktonic larva! of the latter. This marks the onset of the

Figure 24. Cepon elegans.

A, cryptoniscan larva (ventral aspect). B, adult dwarf male (ventral
surface): {, liver; pI, rudimentary pleopod; t, testis. C, rostrum of the
epicarid larva with the mouth parts: md, mandible; mxr. first maxilla;
mX2, second maxilla (after Giard and Bon~er).

truly parasitic phase. While up to now we have seen perfect

regularity throughout the group, henceforth we shall witness
profound divergences according to the different groups of hosts.
We shall now indicate the principal types, constituting as many
families.
72 ADAPTATION TO PARASITISM IN THE CRUSTACEA

FAMILIES OF EPICARIDlE
1. BOPYRIDJE, parasites in the branchial cavity of decapod
Crustacea. They are subdivided into Bopyrinre, parasitizing
prawns and their allies, and Ioninre, parasitizing Brachyura and
Anomura. Principal genera: Bopyrus, Cepon, lone, etc.
2. PHR YXIDJE, found fixed to the abdomen of decapods
(Macrura, Paguridre), and generally very asymmetrical. Genera:
Phryxus, Athelges, etc.
3. ENTONISCIDJE, internal parasites of decapods, principally
crabs, found among the viscera of the host and profoundly modi-
fied. Genera: Entoniscus, Portunion, Priapion, etc.
4. DAJIDJE, external parasites of schizopods, attached to
various parts of the host (thorax, abdomen, gills) and more or
less modified. Genera: Dajus, Notophryxus, Branchiophryxus,
etc.
Let us notice here and now a common characteristic of these
four families: the sexes are strictly separate; the dwarf males,
curiously modified, live regularly on the females, generally
beneath the abdomen or in the brood pouch of the latter.
5. CRYPTONISCIDJE, a very extensive group of varied aspect,
found on different types of Crustacea (Entomostraca and Mala-
costraca), and profoundly modified. Amongst them one may
distinguish a series of separate families, each corresponding to
a given group of hosts. Let us now note that here, contrary to
the preceding groups, there is sex reversal, with first a male
phase in the free-Jiving cryptoniscan larva, and secondly a
female phase when the animal is attached to the host and
becomes profoundly malformed. Here the brood poucn is
internal.
Among the Cryptoniscidre, the Cabiropsidre live on isopods
(some are hyperparasites attached to other Epicaridre). The
Cyproniscidre live on ostracods, the Hemioniscidre on cirripedes
(Balanus), the Liriopsidre on Rhizocephala (and as a result some
such as Danalia are secondarily carried on the crabs which are
hosts of Rhizocephala), etc.
Altogether the Cryptoniscidre vary in very different ways,
according to the different types of host, but show a fundamental
unity demonstrated by hermaphroditism and the conditions
under which the embryos are incubated.
 BOPYRIDJE AND PHRYXIDJE 73
These few facts suffice to show the special interest of the
Epicaridre for the general study of parasitism. Let us now
examine separately each one of these groups.
(1,2) BOPYRIDJE and PHRYXIDJE. Th~ Bopyridre are, on the
whole, the least modified of the Epicaridre and form a natural
group localized on decapods. Bopyrus and the Ioninre live in the
branchial cavity of their hosts and everyone has had occasion
to notice the lateral swelling that a Bopyrus produces on the
thorax of edible prawns (Leander). The Phryxidre (Phryxus,

Figure 25. Bopyrus fougerouxi, a parasite of Leander serratus,

from the ventral aspect.
Ii, brood lamellre (oostegites); pe, thoracic limbs (pereiopods); pi, abdo-
minal appendages (pleopods); ~i dwarf male (after J. Bonnier).

Athelges) live on the abdomen of their hosts (Carididre, Pagu-

ridre) and have a rather different appearance though their struc-
ture is very similar.
In the female Bopyrus (Fig. 25) one may easily recognize the
isopod type. It is enlarged but all the segments are easily made
out and have retained their appendages: hooked pereiopods and
lamellar pleopods with a respiratory function. These last appen-
dages are highly developed in the Ioninre (Cepon, Fig. 26), where
they are pinnate and even branched. Between the pleopods
there is always a male, dwarfed and slim, closely resembling the
74 ADAPTATION TO PARASITISM IN THE CRUSTACEA
cryptoniscan larva but usually lacking its pleopods. In all the
Bopyrid<e there is marked asymmetry in connection with their
lateral (right or left) attachment to the host. Among the Phryxid<e
this asymmetry is very pronounced and leads to the disappear-
ance of all the appendages on one side. This clearly shows how
much the malformation of parasites depends on the conditions
of parasitism. In the present case, is the development of asym-
metry directl~ dependent on the site of attachment or does each

Figure 26. Cepon elegans, a parasite of Pilumnus hirtellus (after

Giard and Bonnier). .
Adult female (dorsal aspect) with dwarf male, 6; ce, cephalogaster;
/, liver; 0, oostegites; pi, pleopods.

larva, in becoming attached, select one side for this on account

of its appropriate constitution? Only precise experiments would
allow us to decide this question and they are hardly possible in
practice. For the sake of comparison, we may recall that among
the gastropod molluscs which are also asymmetriqil (dextral or
sinistral), the direction of asymmetry is fixed in the egg and is
expressed by the orientation of the spindle at the first division
of cleavage.,
Attachment of the parasite to the host generally takes place
 SEX DETERMINATION 75
when the latter is very young, either approaching the end of its
larval life or immediately afterwards. I have myself.qad occasion
to see this in Bopyrus parasitizing a prawn. The growth of the
parasite parallels that of the host and Caroli 376 was able to see
that their moults occur simultaneously.
All these parasites, in order to feed, pierce the body wall of
the host with their mouth-parts (mandibles and maxillre) modi-
fied as stylets (actually in the epicaridian stage) and ending in a
small toothed blade. They suck the blood. On the dorsal part of
the cephalic region there is a double hemispherical swelling
forming the cephalogaster (Fig. 26 ce), especially developed in
the Entoniscidre, which must play an important part in the
aspiration of the host's fluids. It is clearly an adaptive arrange-
ment. The last part of the intestine is no longer functional; the
imbibed fluids accumulate in the hepatic ducts, which Qecome
very large. There they are gradually dialyzed and altered so that
finally they constitute reserves of fat within a special tissue or
in the vitelline substance of the egg. Ventrally the thoracic seg-
ments bear the hooked pereiopods with epipodites constituting
the brood lamellre, oostegites, relatively little developed in
Bopyrus (Fig. 25) but much more so in the Ioninre (Fig. 26), and
these lamellre enclose the brood pouch where the embryos
develop until they hatch as epicaridian larvre.
The question of the conditions governing the determination
and differentiation of sex in these parasites comes naturally to
mind. An obvious conclusion is that sex results from the very
conditions of parasitism; a cryptoniscan larva a~taching itself
directly to the host and therefore finding favourable conditions
for feeding would develop as a female; on the other hand, a
larva newly established on a young female would become a male.
I myself have suggested 227 that it could be thus, particularly
among the Entoniscidre where (see below), in the brood pouch
of each female, one always finds rather large numbers of males
and of cryptoniscan larvre which will develop as males. Recent
observations (D. Atkins, Veillet) do not bear this out and tend
to show that in the Entoniscidre sex is already determined in the
cryptoniscan larval stage where entry into the host occurs.
But my hypothesis is clearly established by some exact experi-
ments carried out with one of the Ioninre (lone thoracica, a para-
site in the branchial cavity of Callianassa subterranea) and in
76 ADAPTATION TO PARASITISM IN THE CRUSTACEA
addition with one of the Phryxidre (Stegophryxus hyptius, a
parasite on the abdomen of Pagurus IOlJgicorpus). Actually,
Reverberi and Pitotti 272 took young males of lone thoracica at
the beginning of their metamorphosis on females and moved
them into the branchial cavity of an unparasitized Callianassa;
they quickly attached themselves, lived there and in most cases
became/emales. Here we have an undeniable reversal of the sex
which would normally have been realized. On the other hand,
Reverberi 27) 'obtained in one case a contrary reversal, that of
a young ipdividual, already developing as a young female, into
a male/He took an adult female and a very young female (at
the tle'ginning of the post-cryptoniscan metamorphosis) and
placed them in a dish, putting the young female on the old one;
the association persisted and the young one fed. When its nurse
came to die Reverberi replaced her by another. This enabled
him to extend the experiment over several months and in one
case he finally obtained a typical male with testes and sper-
matozoa.
Quite recently, Reinhard 269 carried out an analogous experi-
ment with Stegophryxus hyptius. Some presumptive females,
still very young but already attached to the abdomen of the
pagurid, were taken off and transferred to older females. They
changed into males. He was not successful in obtaining the
reverse change (of a presumptive male into a female) as he was
not able to bring about the attachment of young males to the
pagurids.
The definitive sex in the Bopyridre and Phryxidre then seems
to be labile and to result from the conditions, particularly as
regards nutrition, in which the individual develops from the
cryptoniscan stage onwards. This conclusion seems natural
enough when one considers the normal change of sex in the
Cryptoniscidre (see below, p. 83).
(3) ENTONISCIDlE. This group is perhaps the most special-
ized of the Epicaridre, and the profound malformation of its
members is obviously the result of parasitism. They live within
the visceral cavity of the host (crabs, Porcellanidre) and are
enclosed within a membrane which in reality belongs to the
host. When the parasite is mature, and just as the eggs are being
laid, one end of this membrane becomes attached to the wall of
the host's branchial cavity and forms an opening there by which
 ENTONISCIDlE 77
the epicarid larvre can make their escape. On account of this
arrangement, Giard and Bonnier supposed that the membrane
enclosing the parasite was a diverticulum of the host's branchial
cavity. According to them the parasite penetrated into the
branchial cavity of the host, causing a hernia which projected
into the visceral cavity but always remained in communication
with the exterior; thus, they claimed, there must be a con-
tinuous flow of water round the parasite ensuring its respiration.
Contrary to appearances, then, the Entoniscidre would be
ectoparasites.
This thesis prevailed generally until quite recently on account
of the uncontested aulhority of Giard and Bonnier on this sub-
ject. I should say, however, that I fOllnd it difficult to accept, as
I have many times found young Entoniscidre (Portunion koss-

Figure 27. An adult entoniscid, Portunion mcenadis, in its normal

position inside the carapace of Carcinus mcenas (after Giard).

manni in the crab Platyonychus latipes) in the midst of the host's

viscera, far from its body wall and certainly without any external
communication. But the truth of endoparasitism in the Ento-
niscidre has recently been completely confirmed by the researches
of P. Drach 237 and in particular by those of A. Veillet 278;
indirectly also by the observations of D. Atkins 214. Drach puts
crabs, Carcinus mamas, in sea water to which methylene blue has
been added (1 part per 1,000). After a few hours their branchial
cavity is deeply stained; on the contrary, young Entoniscidre
found in the visceral cavity show no trace of tlie colouring
matter which they should do if the sheath enveloping them com-
municated with the branchial cavity of the host.
At Sete, where Portunion ma:nadis occurs very commonly in
Carcinus ma:nas, Veillet was able to work with abundant material
of every stage. Now, he was able to show clearly the way in which
78 ADAPTATION TO PARASITISM IN THE CRUSTACEA
the entoniscid, as a cryptoniscan larva, penetrates directly into
the general body cavity of the crab. He found these typicallarvre,
particularly beneath the hypodermis of the mouth-parts
(Fig. 28A, B) or the apodemes, and watched their transformation
into apodous larvre while, at the same time, he recovered the
empty cast of the cryptoniscan larva with the thoracic limbs
still retaining their muscles. The young apodous female (Fig. 28C)

Figure 28. Portunion mamadis: stages of development in the crab

Carcinus mcenas (after Veillet).
A, B, penetration of the cryptoniscan larva under the cuticle of an apodeme
(profile and surface view). C, young female after the moult in the
cryptoniscan stage; ch, chromatophores; hp, hepatopancreas.
D, female before the appendages have appeared (asticot stage).
E, the stage when the pleopods begin to appear. F, a later stage (at
the beginning of the formation of the oostegites, 0). The scale is shown
by the drawing of one millimetre beside the various sketches.

moves about between the hypodermis and the chitin and finally
passes into the general body cavity of the crab. He was able to
follow all the stages of the change into the typical entoniscid
form (differentiation of the cephalogaster, appearance of the
appendages), and to follow its growth and differentiation.
As fO,r the enveloping sheath, Veillet's observations have
shown that during growth it forms a complete sac, closely
applied to the parasite, and that it is produced by an agglomera-
 ENTONISCIDlE 79
tion of the lymphocytes of the crab, just as during phagocytosis
a sheath is formed round a foreign body; thus Kossmann's.
opinion, formulated in 1882, is confirmed. The mouth-parts of
the entoniscid make a little opening in the sheath, enabling it to
feed. Respiration takes place across the sheath. When the female
is ripe and about to set the epicarid larVa! free, the sheath
becomes fastened to the wall of the crab's branchial cavity and
an opening is pierced in it so that there is a passage into the
branchial cavity by which the larVa! will escape. But this passage
is secondary and does not exist during the growth of the epi-'
caridian. The entoniscid, in the crab, is a true endoparasite.

Figure 29. Portunion mamadis: Figure 30. Portunion koss-

very young female at the manni: adult female with
b.eginning of its metamor- the brood pouch filled with
phosis (asticot stage, after embryos (after Giard and
Giard and Bonnier). Bonnier).

In the adult stage, the entoniscid cannot be recognized as a

typical isopod (Fig. 30). There is scarcely any metamerism, nor
are appendages visible. The thoracic region is surrounded by
enormous oostegites bounding the brood pouch and forming
extremely extensive lobes. One recognizes the cephalic region in
the cephalogaster. On the abdomen, the pleopods, serving as
gills, are extensively scalloped and fringed. But it has, in fact,
been possible to follow all the stages of differentiation in the
animal from the moment when, still lacking oostegites, it resem-
bles a worm (asticot stage, Fig. 29), and to see the gradual
development of the oostegites and the pleopods. This has been
80 ADAPTATION TO PARASITISM IN THE CRUSTACEA
done by Veillet with Portunion manadis parasitizing Carcinus
manas, and by Giard and Bonnier, who worked on this species
as well as on Portunion kossmanni parasitizing Platyonychus
iatipes.
As for the male, it is ajcomplete dwarf (scarcely 1 mm. long)
and remains in the brood pouch of the female, in the centre of the
egg mass. There are often several of them (Veillet has found up
to thirty) and at the same time a certain number of cryptoniscan
larva:! that Giard and Bonnier thought were neotenic males. The
males are _...nluch less malformed than the females and have
retainedA{plainly isopod character (Fig. 31). They penetrate into
the s;nib as the females do, in the cryptoniscan larval stage, and
can develop as typical males without having any contact with

Figure 31. Porlunion kossmanni: adult male greatly enlarged

(after Giard and Bonnier).

the female, as Miss D. Atkins 214 has observed in Pinnotherion

vermiforme, a parasite of Pinnotheres pisum. It is quite easy to
rec~nstruct the transformation of the cryptoniscan larva into
the adult male. The last changes in the male have been carefully
followed by H. Sansin.
In connection with sex determination in the males, Veillet,
basing his ideas mainly on the observations made by D. Atkins,
is inclined to consider it as already decided in the larval stage
and not to result from contact with the female. Th~ experiments
described above, made by Reverberi and Reinhard, together
with the fact that large numbers of cryptoniscan larVa:! and
males are found in the brood pouch of the Entoniscidre,
strengthen me in thinking that I was possibly right in the theory
 ,
DAJIDJE AND CRYPTONISCIDJE 81
I put forward in 1941; precise experiments with Entoniscidre are
clearly very difficult to make and I do not underrate the value
of D. Atkins' observations.
What has just been said is sufficient to show the great interest
of the Entoniscidre for the study of parasitism, and the diffi-
culty of the problems which face the worker, problems which
can only be solved with abundant material. Recent researches,
particularly those of Veillet, have, thanks to this, considerably
modified the views which were previously held.
(4) DAJIDJE. We shall deal much more briefly with this family,
which consists of external parasites on schizopods. Their mode of
malformation is very homogeneous. In them, as a general rule,
the posterior segments of the thorax (two to four, according to
the genus) hypertrophy but lose their pereiopods, the first seg-
ments retaining theirs which are grouped in the arc of a circle
on the anterior ventral surface. The oostegites of these first
thoracic segments remain rudimentary while, on the contrary,
those behind them grow to a large size. The abdomen is much
reduced and more or less completely devoid of pleopods. The
lateral regions of the thorax develop to fOrm two large sacs
sheltering the embryos. The exact nature of _this brood pouch
has never yet been carefully studied. I should be inclined to
think that it is really an internal structure in the Dajidre and is
produced by lateral invaginations such as we shall find in the
Cryptoniscidre. Plentiful material would be necessary for the
solution of this problem.
(5) CRYPTONISCIDJE. Although they form a very coherent
group, the Cryptoniscidre are divided into a series of sub-
families each with its own special character and localized on the
same group of hosts. On the whole, when adult, they display
very considerable degeneration of all their organs. They are no
more than sacs of embryos, dying when the brood emerges,
which must be unique. They appear in the most disconcerting
shapes, bearing no resemblance to an isopod, nor even to a crus-
tacean. They show no trace of appendages nor of segmentation.
The alimentary canal is only represented by mere vestiges; the
mouth has vanished. The nervous system itself is reduced to a
very few ganglia. Nothing is more divergent than the series of
different types of Cryptoniscidre. It is not possible to study each
one of them in detail here. We shall limit ourselves to a rather
82 ADAPTATION TO PARASITISM IN THE CRUSTACEA
rapid examination of a certain number, in order to gain some
concrete idea of their diversity.
In Hemioniscus, which lives as an ectoparasite on Balanus,
without physical continuity with its host, the head and first four
thoracic segments retain the exact structure of the cryptoniscan

Figure 32. Epicarids of the family Dajidre (after Giard and

Bonnier).
A, Aspidophryxus sarsi on Erythrops microphthalma. B, Dajus mysidis
(ventral aspect) ; 01. os, first and fifth oostegites; (E, eggs after laying;
plh first pleopod; 0', male.

larva, while behind them the whole of the rest of the body
becomes a shapeless sac of considerable size, more or less lobed,
without appendages or distinct segments. The name Hemio-
niscus gives a good idea of this dual aspect of the body. The pos-
terior region finally becomes a sac full of embryos. The brood
 CR YPTONISCIDiE: SEX REVERSAL 83
pouch develops as an invagination of the ventral surface into the
general body cavity.
The Asconiscidre, parasites of schizopods, show the same type
of degeneration, but our knowledge of them is limited to work
on a few specimens, performed by G. O. Sars on a single species
parasitizing a deep-water Mysis.
The Cyproniscidre, parasitizing the ostracods, are scarcely
better known. Up to the present time very few specimens of only
two species have been studied. Scarcely more is known of the
Podasconidre, parasites of Amphipoda, and the Crinoniscidre
which are found on Balanus. We are better acquainted with the
Cabiropsidre on isopods, and the Liriopsidre on Rhizocephala,
since in these two cases abundant material of the different stages
of certain species has been available for study.
Let us notice here that some of the Cryptoniscidre are hyper-
parasites, for instance Danalia (Liriopsidre) on Sacculina, and
Liriopsis on Peltogaster; certain Cabiropsidre are parasites of
Epicaridre (Gnomoniscus on Podascon, Cabirops on Bopyrus).
Recently, Carayon (1942) has studied another case of this hyper-
parasitism, that of Cabirops perezi on one of the Bopyrinre,
Pseudione jraissei, itself a parasite in the branchial cavity of a
pagurid (Clibanarius misanthropus).
I myself have had the good fortune to be able to work with
ample material of all stages of several different types of Crypto-
niscidre: at Naples, with Danalia (on a crab) and Liriopsis (on
Peltogaster); at the Cape de la Hague (with F. Mesnil) with
HemioNiscus balani (on Balanus balanoides) and with one of the
Cabiropsidre, Ancyroniscus bonnieri (Fig. 33) on an isopod. It
was thus possible to ascertain several important matters in con-
nection with the biology of the group.
One of these matters was sex reversal, which is general through-
out the group. All individuals first become functional males at
the cryptoniscan larval stage, as well as growing to some extent.
One finds these cryptoniscan males free-living and moving about
on the surface of the females. They subsequently change into
females, and one finds some individuals showing at the same
time the remains or'testes and rudiments of ovaries in various
stages of development. It is then that they become attached to
the host and undergo their metamorphosis. The sex life of the
Cryptoniscidre is then quite different from that of the other
84 ADAPTATION TO PARASITISM IN THE CRUSTACEA
families (Bopyridre, Entoniscidre and Dajidre). The young females
attached to the host are fertilized at an early stage and the sper-
matozoa remain in the female genital tracts until the single batch
of eggs is laid. The female phase thus includes a period of growth
and youth, when the parasite nourishes itself at the expense of
the host and undergoes its metamorphosis. At the same time
reserve ,substances are accumulated in the large hepatic sacs and

Figure 33. Ancyroniscus bonnieri (after Caullery and Mesnil).

A, sub-adult female (before egg deposition); the two pairs of lower lobes
belonging to the abdomen are lodged in the visceral cavity of the host.
B, adult female after laying, reduced to a lobed and closed sac filled
with embryos.

these will later be utilized in the developing ovary. The eggs are
deposited in the brood pouch, which in this case is inside the
animal. We were able to follow its development very closely in
Hemioniscus balani and found that it was very similar in Ancyro-
niscus and the Liriopsidre. It may be taken almost for granted
that it is on the same lines throughout the Cryptoniscidre. This
brood pouch, which originates as a pair of ectodermal invagina-
tions in the ventral region, spreads throughout the body and
 RHIZOCEPHALA 85'
compresses all the organs, which become vestigial and non-
functional. As a rule, in the advanced stages of incubation the
mother possesses neither mouth nor alimentary canal and only
a few nerve ganglia remain ventrally. The animal, however, con-
tinues to contract regularly and rhythmically, thus ensuring the
respiration of the developing embryos. *
As we have already been able to see, the Epicaridre provide a
highly significant example of the value of parasitism as a factor
in evolution, whichis the reason that I have lingered rather long
over them. Starting from very similar types and being submitted
to conditions of parasitism in different crustacean hosts they
have developed into forms which are highly divergent when com-
pared with each other. Each family of hosts has been the source
of a particular evolution. Let us note that the initial character of
these modifications is far from having persisted during develop-
ment, as may be seen in the structure of the mouth-parts which,
from the epicarid stage, have the definitive form corresponding
to the parasitic life.
The progress that has recently been made in our knowledge
of the Epicaridre is due to their having been studied in suitable
localities where there has been. abundant material to work on,
and where they have been observed in a living state and to some
extent experimented on. Under such circumstances we may yet
expect new facts and I draw the attention of research workers to
this point.
RHIZOCEPHALA
Amongst the Crustacea the Rhizocephala provide another
example of the intensity of changes brought about by parasitism.
The most classical example in the order is that of the genus
Sacculina, a parasite of crabs and Anomura. It appears as a
fleshy sac (Fig. 34) attached transversely to the ventral surface of
the abdomen and separating the latter from the ventral surface
of the cephalothorax. At the free apex of the sac there is a median
* The dual conditions of incubation of the embryos in the Crypt6niscidre and
the other Epicaridre cannot be considered to be the result of parasitism. Actually
they are also found in the free-living Isopoda of the famIly Sphreromidre where,
in certain genera, such, for instance, as Dynamene, the eggs are incubated in an
external cavity beneath the thorax, whIle in others, such as Cymodoce, there is an
mternal brood pouch. ThiS suggests that within the Isopoda the Epicandre may
have had a double origin, commg from two sources showing thiS difference in the
methods of incubation.
p.s.-4
86 ADAPTATION TD PARASITISM IN THE CRUSTACEA
opening leading into a flattened cavity called the pallial cavity,
which extends round a central, fleshy, visceral mass, and which,
in the adult, is full of developing embryos. The visceral mass
consists almost entirely of the paired ovary, besides which there
is a pair of small testes and a nerve ganglion. This collection of
organs outside the host does not constitute the whole Sacculina;
there must be added to it an internal part consisting of a system
of roots radiating and ramifying throughout the crab. It is by
means of them that the Sacculina, like a plant, is able to assimi-
late its food at the expense of its host and to produce successive

Figure 34. Crab carrying Saccu/ina, s; the system of roots is

shown on the left side of the figure (after Boas).

batches of eggs. These few facts show how degenerate the Saccu-
!ina is, lacking appendages, alimentary canal, sense organs, etc.
Even its relationship could not be ascertained from the adult.
Hermit crabs are parasitized by Peltogaster, which is close to
Sacculina. and still other genera of Rhizocephala are known:
Parthenopea on Gebia (= Upogebia); Callianassa' and Lernceo-
discus on Galathea and Porcellana; and Thompsonia (=Thylaco-
plethus) on crabs (Melia imd Thalamita) and Alpheus.
Development reveals the affinities of the Rhizocephala which
are Crustacea related to the Cirripedia, a group consisting of
 SACCULINA 87
fixed forms, Balanus, Lepas, etc. Indeed, the larvce which leave
the mantle of Sacculina are, at hatching, nauplii with lateral
frontal horns like those of cirripedes (Fig. 35 I). Furthermore,
after four successive moults in five days, the nauplius changes
into a cypris larva (Fig. 35 II), equally characteristic of cirri-
pedes. These two larval forms thus leave no doubt about the
zoological position of the Rhizocephala. However, they differ in
several ways from corresponding forms amongst the cirripedes:
neither possesses an alimentary canal; interiorly there is a mass
of tissue containing a great deal of fat, and no other differentia-
tion of organs except. for an eyespot; so here there is modifica-
tion due to parasitism such as we have seen in the mouth-parts
of epicarid larvce of the Epicaridce.
Cypris larvce of cirri pedes as a rule attach themselves by the
antennule to the support where they will complete their develop-
ment, and it is easy to watch the organs of the larva change into
those of the adult. The larvce of Sacculina similarly attach them-
selves to the crab and, by analogy, it was supposed from the
very first that the system of rootlets derives from the anterior
or cephalic region, hence the name of Rhizocephala for the
group. It seemed evident, too, that the fixation of the cypris larva
must take place where the adult parasite is found, that is, under
the abdomen of the crab in the case of Sacculina; this must be
the direct result of the metamorphosis in situ of the cypris. But
one never finds sacculinas of a size comparable with that qf a
cypris larva (0·2 mm.); the smallest are from two to three milli-
metres, or ten times the It\llgth. In reality, between the larval
cypris and the smallest sacculinas that may be seen attached to
the abdomen of the crab, there is interposed a very unexpected
and surprising series of stages whose discovery we owe to
Y. Delage 235 and which can only be the result of a long evolu-
tion under the influence of parasitism. Uncertainty remains only
about the stages by which such an evolution has taken place
and on the precise causes that determined it.
The cypris larva, after swimming about for a few hours, fixes
itself by one of its antennules to a young crab (Carcinus mamas)
of 4 to 7 mm.; this attachment only takes place during darkness,
but it can be brought about during the day if a darkened vessel
is used. But it never takes place, as one would naturally suppose,
at the spot where the Sacculina wi11later be found. The cypris
88 ADAPTATION TO PARASITISM IN THE CRUSTACEA
settles anywhere on the surface of the crab, but it will only be
successful in certain positions, in particular at the base of a seta
on the carapace. As soon as it is fixed the larva begins to meta-
morphose (Fig. 35 III); its internal contents contract into rather
a small, cellular, vesicular mass, and the carapace, with its larval
limbs, becomes detached and is cast off; the internal mass, now

Figure 35. Larval development of Sacculina (after Y. Delage).

T, nauplius; II, free-living cypris; III, cypris attached to the base of a seta
of the crab, having begun to degenerate: IV, end of regression in the
cypris larva; V, kentrogon stage.

external (Fig. 35 IV), becomes covered over with a thin new layer
of chitin. In the anterior part of this cellular mass, near the point
of attachment, there differentiates a thin internal tube, chitinous
and dart-shaped, which penetrates by means of the attaching
antennule through the integument of the crab, which is thin here
 SACCULINA 89
on account of the articulation of the seta; by this kind of trocar
(Fig. 35 V) the cypridian cellular mass is, so to speak, injected
into the body cavity of the crab. Delage named this larval stage
the kentrogon. The cypris larva is thus changed into a small
cellular mass, naked and undifferentiated, and now within the
body of the crab. There has taken place, then, a very great
regression, beginning in the free-living stages and particularly
from the ancestral cypris in which there were already the rudi-
ments of all the essential organs of the adult cirripede. Sacculina
will remain as an internal parasite of the crab for a very long
time, according to Delage about twenty months, during which
the crab completes its growth. Its history during this period was
elucidated by G. Smith,* who confirmed 274 and, in 1906, defi-
nitely placed beyond dispute the facts set out by Delage, which
had been contested, particularly by Giard, on account of their
peculiar nature.
The internal, undifferentiated Sacculina undertakes a regular
migration within the crab, from the point of entry, which may
be anywhere, to the position on the abdomen where the external
Sacculina is regularly found. Using Sacculina in Inachus
mauritdnicus (=1. scorpio), Smith succeeded in fiqding the
different stages of this migration which takes place along the
length of the intestine, from the anterior region, where the paired
ca:ca are given off, to almost opposite the unpaired abdominal
ca:cum, where it stops (Fig. 36). During this time the parasite
is composed of a shapeless, lobed mass from which prolonga-
tions are pushed out, constituting the beginning of the radical
system. At a certain moment, towards the end of migration, there
becomes differentiated in the central part, from which the first
roots are given off, a sort of tumour, or nucleus, which is the
beginning of the actual Sacculina. The parasite, having arrived
at the abdomen of the host, finally takes up its place on the ven-
tral surface of the intestine, opposite the unpaired posterior
crecum. Within the nucleus there form, by a new differentiation,
as Smith showed (and not, as Delage supposed, froPl rudiments
present in the cypris stage), the definitive organs (pallial cavity,
genital glands, nerve ganglia, etc.). Thus there is constituted the
internal Sacculina. It presses against the ventral wall of the
* Geoffrey Smith, who was consIdered to be one of the best English biologIsts
of his generation, was kIlled In 1917, at the battle of the Somme.
90 ADAPTATION TO PARASITISM IN THE CRUSTACEA
crab's abdomen and by. its contact produces a necrosis of the
parietal muscles and of the epidermis and then a softening of the
chitin over a small disc of two to three millimetres. This disc
gives way, or else the crab moults, and Sacculina is then external;
it now grows rapidly.
A parallel type of evolution has been found in Peltogaster
(ScWmkewitch, Smith); in other much rarer genera it has not
yet been studied.
. The processes which constitute the development of the internal
Sacculina (dedifferentiation and migration, then new differenti-
ation) can only be the result of a progressive evolution (evidently

. Figure 36. Internal stage of Sacculina.

S, in the course of its migration along the gut of the crab, with the differen-
tiation of the root system, r; ca, anterior creca, and cp, posterior
crecum of the crab's intestine; n, nucleus (future external Sacculina)
(after Geoffrey Smith).

determined by the conditions of parasitism), of a more or less

rapid type, with a succession of stages in the past which still
remain entirely unknown to us. Perhaps the genera other than
Sacculina and Peltogaster, whose development has not yet been
studied, will throw light on these stages. *
* Smith observed that a clrripede, Anelasma squalicola, attached to the skm of
a shark (Spinax) possesses roothke prolongatIons buried in the integument of the
host; but these are merely organs of attachment and the animal differs from the
Rhizocephala III having a well-developed ahmentary canal. It cannot possIbly be
considered to be one of the Rhizocephala. On the other hand, SmIth considers
that a parasIte attached to the ventral surface of the isopod Calathura branchiata
IS probably a primitive member of the Rhizocephala, perhaps lackmg roots. This
animal, whIch was named Duplorbis calathurce, is still very little known, and has
unfortunately been found only once, in Greenland.
 GREGARIOUS RHIZOCEPHALA 91
The external sac of the Rhizocephala seems clearly to con-
stitute the differentiated part of the individual, the system of
roots playing only a trophic role. It is interesting, in this connec-
tion, to quote here an observation of Ch. Perez 266 on Pelto-
gaster paguri. On the root system he saw a recurrent branch
slowly form, and after the descent of the Peltogaster (the roots
were watched for several years) aneurisms were formed on these
recurrent branches and in the aneurisms there developed ovaries
whose oocytes matured but could not be shed. The question
arises oLknowing whether these late radical ovarian structures

Figure 37. Thompsoma sp. on Synalphells brucei (after F. A. Potts).

actually derive from the primordial genital cells of the individual

or whether they are a straightforward new differentiation of root
tissue, separate from the germ plasm.
Coutiere 234 thought that in a gregarious genus which he
called Thylacoplethus, found by him on the Alpheidre, he had
discovered a primitive form of Rhizocephala with direct develop-
ment, not migrating into the interior of the host. Each indi-
vidual, he thought, must have developed at the point where it
was found, and the gregarious condition resulted from the
attachment of a large number of cypris larvre to the same host.
This genus is, in reality, identical with Thompsonia (Fig. 37)
92 ADAPTATION TO PARASITISM IN THE CRUSTACEA

mentioned earlier, and the researches of F. A. Potts 267 have

shown that it is, on the contrary, a type still more modified than
the others, which under the influence of parasitism has acquired
a new and particularly interesting habit, asexual reproduction.
Thompsonia is not the only gregarious member of the Rhizo-
cephala. On the French coasts, particularly in the Mediterra-
nean, the hermit crabs Eupagurus prideauxi and E. meticlilosliS
sometimes carry a Peltogaster (= Chlorogaster) which is never
solitary but always in groups often to twenty individuals, appar-
ently of the same age, and therefore called Peltogaster socialis.
Smith had already suggested that these multiple individuals
could result from the budding of an undifferentiated internal
stage but had not been able to demonstrate it, having always
found that each individual was provided with its own system of
roots, was independent of the others, and could therefore derive
from a separate cypris larva.
In Thompsonia gregariousness is much more accentuated
and often more than one hundred individuals are associated
while there may even be two hundred (Fig. 37). These forms
have until now only been found in the tropics, particularly in
the Pacific, on crabs (Melia, Thalamita, Pilumnus, Actaa), on
pagurids (Diptychus), and on Alpheidre. They are attached to
many different parts of the carapace and appendages. The ana-
tomical study of these individuals reveals a much more simple
organization than in Sacculina. Here all the individuals stand
out from a single radical system which is common to all of them,
suggesting that they arise by budding. Potts observed on an
Alpheus that all these external individuals are cast off whenever
the host moults, after having discharged their embryos (it seems
that they lay only one batch of eggs), and that a fresh generation
shoots out again from the system of roots within the host, as
successive crops of cultivated mushrooms develop from the
mycelium. Smith's suggestion is thus confirmed and it is very
likely that it applies equally to Peltogaster socialis; but in this
last case there must be either precocious and definitive frag-
mentation in the internal stage which succeeds the cypris or a
budding resembling polyembryony. This type of sexual repro-
duction has been carefully studied by Ch. Perez 234, working
on the social Peltogastridre of the genus Chlorogaster, para~
sitizing pagurids. He showed that the individuals which emerge
 ASCOTHORACICA 93
successively from the abdomen of the host arise from buds
formed on the system of roots that surrounds the mid-gut of the
pagurid, and he has followed out their differentiation. All the
members of one branch develop at the same time. In other res-
pects this reproductive cycle displays a certain amount of plas-
ticity.
Thus, in the Rhizocephala, parasitism, after leading to the
intercalation of an internal phase characterized by an absence
of cellular differentiation and by the radical nutrition that we
have seen in Sacculina, has also resulted, thanks to this lack of
differentiation, in a process of asexual reproduction that is
altogether surprising in a group such as the Crustacea. These
animals, which, as far as individuality and organic functioning
are concerned, are amongst the most highly differentiated in the
animal kingdom, have been led by parasitism to a way of life
and reproduction akin to the lowest of the Metazoa-the crelen-
terates and even the sponges-and recalling plants to an even
greater extent.
ASCOTHORACICA
I shall now devote some pages to the group of Ascothoracica,
which are close to the ostracods and the cirripedes; our know-
ledge of them has recently made important advances. They,
also, are a striking example of the different degrees to which
parasitism affects the modifications of a single group, and thus
of a true secondary evolution developing from a known point
of departure. First of all, for the sake of clarity, a list of the
forms so far studied is given in the table on the next page; a
complete bibliography is provided by Yo K. Okada 260.
It is to Lacaze-Duthiers 250 that we owe our first knowledge
of this group. He gave an excellent and detailed anatomical des-
cription of Laura gerardice which he found at La Calle (Algeria)
on Gerardia, one of the Antipatharia. We may note that his hos-
tility to, and his lack of understanding of, the theory of evo-
lution prevented him from arranging his description in a
clearly comparative way. The best comparative study of the
group is that of Yo K. Okada 260, who, as well as studying
different species in vivo, has also carefully worked over the
material collected by Norman and Fowler, which is in the
British Museum.
4*
94 ADAPTATiON TO PARASITISM IN THE CRUSTACEA

Position
Species Hosts lU Localities Authors
host
Fam. I
Synagogldre
Synagoga mira Antipar/tes Ecto- Naples Norman 1887,
larix (Ca:l.) parasIte 1913
S. metacrinicola Metacrinus do. Japan Okada 1926.
rotundus 1939
(Echm.)
Ascothorax Ophiocten do. Iceland, biakonow 1914
ophioctenis sericeum etc. Stephensen
(Echm.) 1935
Fam. n
Petrarcidre
Petrarca Bathyactls Pacific Fowler 1889
bathyactidls symmetrica (abyssal)
(Ca:l.)
Fam. III
Laundre
Laura gerardi(/! GelardJa Ecto- Mediterranean Lacaze-Duthlers
(Ca:l.) parasIte 1883
Baccalallreus AntJpatharia do PacIfic Broch 1929
japonieus (Ca:I) YOSll 1931
B. maldiVlemis do. do Maldives Pyefinch 1935
B. argallcorms do. do. Madagascar Brattstrom 1936
Fam. IV
bendrogastridre
Ulophysema Echinocardlllm Endo- Norway Brattstrom 1936
oresundense cordatum parasite
U. pourtales;(/! POut ralesia do. Greenland Brattstrom 1937
jeffreysl
(Echm.)
Dendrogaster Echinaster, do. White Sea, Kmpowitsch 1892
astericola Solaster PacIfic W. 'K. Fisher
(Echm.) 19-
D. murmanellsis Solaster, do. Murman Kluge, Korschelt
Crossaster coast 1933
(Echm.)
Myriocladus Dipsacaster do. The Cape 0, Le Roi 1905
arborescens studeni Okada 1926
(Echm,)
M.ludwigil Eehinaster do. Pacific, O. I.e Roi 1907
/allax, Japan
Certonardoa
semlregu/aris
(Echin.)
M. astropectinis As/ropec/en do. Japan YoSll 1931
mU/Uacan-
theis(Echm.)
M.okadai Asterias do. Japan Yosi! 1931
ca/amaria
(Echin.)
 ASCOTHORACICA 95
The fundamental feature in the organization of the Asco-
thoracica is that the actual body of the animal is enveloped in a
kind of sheath formed by a bivalved carapace, often of great size
in comparison with the animal itself. It is within the mantle
cavity that the eggs develop until the hatching of the larvre.
First of all, it must be said that this carapace is nothing but the
bivalved shell of the cypris larva, the existence of which shows

Figure 38. Cypris larva of Mynocladus (after Yo K. Okada).

an, antenna; Ab1-Ab s, abdominal segments; B, buccal cone; CC, cavity of
the right valve; fo, olfactory filament; Pl-PS, thoracic limbs; Th" Th 6,
fourth and fifth thoracic segments.

clearly that the Ascothoracica belong to the cirripedes, as

Lacaze-Duthiers recognized from other characters. We must
note, however, that the nauplius larva of the Ascothoracica lacks
the anterior lateral horns that characterize the cirripedes, and
their absence serves to mark the autonomy of the group. In some
forms, principally the polar species, hatching does not take place
until the cypris stage.
The cypris larva (Fig. 38) will provide us, in other respects,
96 ADAPTATION TO PARASITISM IN THE CRUSTACEA
with a general landmark for interpreting the group. The different
parts of the body may be recognized without difficulty. The
buccal cone, B, encloses the mandibles and maxillre, which are
modified for piercing and sucking, a sign of adaptation to para-
sitism. Let us now see the different ways in which this prototype
becomes modified.
SYNAGOGIDJE. Synagoga. Only two species of this genus are
so far known, S. mira, found on Antipathes larix at Naples by
Norman, and S. m'etacrinicola, found on a crinoid, Metacrinus
rotundus, in Japan by Okada. Only a few specimens of each of

A 8
,Figure 39. A, fragment of the stem of Metacrinus rotundus
bearing two females of Synagoga metacrinicola,' between them
are the marks of a third indIvidual which has fallen off. B, female
of Synagoga metacrinicola (left half of the carapace removed).
an, antenna; cc, cavity of carapace; ci, cavity of brood pouch; m, muscle;
ma, the adductor muscle of the valves in section; PCP6, thoracic
limbs; Th 1-Th6 , thoraCIC segments (after Yo K. Okada).

these species have been studied. They are external parasites

(Fig. 39A) appearing as somewhat globular masses, attached to
the surface of the host and limited by a bivalved carapace, the
edges of which are more or less joined. Within the carapace is
the animal itself (Fig. 39B), which closely resembles'the larval
form described above. In it we recognize the typical structure of
a crustacean, with head, thorax and abdomen clearly seg-
mented; the thoracic segments bearing biramous pereiopods. In
the buccal cone the mouth-parts are modified for piercing (as in
 PETRARCIDJE 97
the larva). The first abdominal segment in the female bears a
chitinous process which corresponds to the penis, very much
more developed in the male. The internal organization scarcely
departs from the normal except that both the alimentary canal,
on leaving the stomach, and the genital glands send into the two
valves of the carapace a pair of diverticula which ramify there.
This is one of the chief characteristics of the group.
The sexes are separate. The male is smaller than the female
(1 mm. instead of 2·5 mm.) and is flatter. In shape and structure
they are visibly similar. Okada, after studying Norman's speci-
mens of S. mira at the British Museum, came to the conclusion
that they were all males. .
Ascothorax. The species A. ophioctenis is a parasite living in
the branchial sacs of the ophiuroid, Ophiocten sericeum. First
described by Diakonow 236 it has been further studied by
Stephensen 275 from fresh material collected by the Ingolf expe-
dition. The two sexes are usually found beside each other, the
male being smaller than the female. We may still consider this
as a case of external parasitism, the branchial sacs of the ophiu-
roid being, in short, part of the external environment. The
organization of Ascothorax agrees for the most part with that of
Synagoga, but there is already a clear reduction of the thoracic
appendages, particularly in the male; the pereiopods especially
have lost the long terminal setre that they possess in Synagoga.
PETRARCIDlE. To this family belongs Petrarca bathyactidis,
which has been found on only one specimen of an abyssal
anemone, Bathyactis symmetrica, dredged by the Challenger at
a depth of 3,000 fathoms. Only three specimens of the parasite
are known; they were studied in 1889 by Fowler, and re-examined
later in the British Museum by Okada. They live in the digestive
cavity of the anemone, which communicates with the exterior,
so that, properly speaking, they are not internal parasites.
Their morphology recalls that of Synagoga, a more or less
spherical structure within a bivalved carapace. The cephalic
region bears antennules with many segments. The pereiopods
are reduced to foliaceous, unjointed protuberances; the abdo-
men has only three segments. The digestive tube gives off two
diverticula which ramify in the carapace; the ovaries and testes
do likewise. Petrarca is hermaphrodite, the only such case we
have so far seen.
98 ADAPTATION TO PARASITISM IN THE CRUSTACEA
LAURIDlE. This consists of the two genera Laura and Bacca-
laureus. Laura gerardice was discovered and studied by Lacaze-
Duthiers. The animal is attached to a branch of the host,
Gerardia (Antipatharia) (Fig. 40A). The two valves of the flat-
tened carapace are enormous in comparison with the animal
itself, and their edges are joined except at one point in the

a
v

8
. Figure 40. Laura gerardifli.
A, the female attached to a stem of Gerardia (the polyps covering it have
been removed) ; 0, orifices of the valves. E, valves opened along the line
of insertion on the stem of Gerardia and pressed back; in the aXIs the
body of Laura (p, posterior extremity) ; m the wall of the valves are
the ramifications of the intestinal diverticula, di, covered externally
by the ovary, OV. C, the male within the valves, v; ab, abdomen;
a, antenna. D, nauplius stage (after Lacaze-Duthiers).

vicinity of the mouth. In the natural state the carapace is covered

by the polyps of the ccelenterate. But it is still, in reality, an
external parasite. The animal itself, which is very small (Fig. 40B),
is to be seen inside the carapace, opposite its free surface and in
the immediate vicinity of the external opening. Its structure is
allied to that of Synagoga, showing the same regions of the body
(head, thorax and abdomen) and a regression of the setigerous
 LAURIDlE 99
armature of the pereiopods. From the stomach is given off a
pair of diverticula, di, which ramify in the two valves of the cara-
pace, these ramifications being accompanied by those of the
til

D
Figure 41. Baccalaureus japonicus Sf! (after Yosii).
A, in the carapace. B, external aspect, right valve removed. C, the actual
body isolated (left aspect). D, internal anatomy: ai-aS, abdominal
segments; th, thoracic segment; an, antenna; b, buccal cone; c,
body of the animal; ce, cerebral ganglia; di, intestinal diverticula
ramifying through each valve; e, stomach; ma, adductor muscles;
0, orifice of the carapace; re, laid eggs; res, resophagus; OV, ovary
(forming an external sheath to the intestinal diverticula); pel-pe4,
pereiopods.

ovary, OV, which they mask. The dwarf male (Fig. 40C) within
the valves was drawn by Lacaze~Duthiers 250 (pI. VIII, Fig. 102),
but not recognized as such by him. He referred to it as "un
100 ADAPTATION TO PARASITISM IN THE CRUSTACEA
animal indetermine representant peut-etre la forme cypridi-
enne", but he states that, when he compressed it there escaped
from within it some corpuscles filled with motionless filaments,
which are perhaps spermatozoa. Giard (1891) recognized that
it was a male and Okada 260 gave the same interpretation, in-
dependently.
In the genus Baccalaureus, first described by Broch 220, there
are now three species known (japonicus, maldiviensis and argali-
cornis), all parasites of Antipatharia. They are close to Laura but

A
Figure 42. Baccalaureus japonicus b' (after Yosii).
A, external aspect of the carapace. B, external structure Oeft valve
removed). C, internal anatomy: aI-aS, abdominal segments; an,
antenna; b, buccal cone; ce, cerebral ganglia; e, stomach; i, intestine;
ma, adductor muscles; (£S, resophagus; pe, pereiopods; n, nervous
system; pe, penis; t, testis.
reach a new stage in the regression of the thoracic appendages
which are no longer clearly articulated. On the other hand, in
the anterior region there is a pair of very large appendages,
probably the first pair of pereiopods, whose function is doubt-
less the moving about of the eggs in the brood pouch; these are
not nearly so well developed in Laura. The dwarfing of the male
is very pronounced (0·6 mm. in length as agail1st 8 mm. in the
female). The anatomy of both sexes has been thoroughly studied
by Yosii 280, Again, there are always two diverticula from the
 DENDROGASTRID)E 101
stomach, ramifying with the ovary or testis in the valves of the
carapace (Fig. 42).
DENDROGASTRID)E. All the known members of this family
are internal parasites of echinoderms: Ulophysema occurs in sea
urchins (Spatangidre); Dendrogaster and Myriocladus in star-
fish. In this family we see a profound modification of the
bivalved carapace which changes into a double arborescence
of branching diverticula corresponding to the ramifications of
the alimentary canal and ovary. The body proper, enveloped
here by a sheath which is closely applied to it and is only a
vestige of the bivalved carapace of the preceding forms, is no
more than a small tubercle in the centre of the arborization.
Ulophysema. This genus, set up by Brattstrom 218, now com-
prises two species: U. oresundense, a parasite of Echinocardium
cordatum in Norwegian waters, where it has been found in
abundance, and U. pourtalesia!, a parasite of another spatangid,
Pourtalesia jeffreys_i, in Greenland waters. These parasites live
within the general body cavity of these sea urchins; U. oresun-
dense is found near the gonads of Echinocardium. The young
stages are free-living, the older individuals are attached to the
test of the urchin and at that point there is a small hole, formed
by the parasite, through which the larvre escape. Ulophysema
attains a length of 30 mm. and looks like a simple unbranched
sac with a small median conical protuberance in which there is a
slit-like opening leading into the mantle. This last structure is
formed by the two valves of the cypris larva, which have become
joined together. As in the preceding types, its wall contains the
ramified branches of the paired diverticula from the stomach
and the ovary. The tips of these branches bulge at the surface like
a kind of excrescence. The body proper, which is very small, lies
in the conical protuberance of the pallial sac noticed above. In
it are the structures that characterized the preceding types: a
buccal cone with antennules, an unsegmented thorax with almost
rudimentary pereiopods and four pairs of lateral prominences,
and a segmented abdomen. To sum up, there is the same general
structure but reduced differentiation in some regions. The eggs
ripen in the branches of the ovarian diverticula and fall into the
mantle cavity where they develop, giving rise to a nauplius
which changes to a perfectly regular cypris with biramous
pereiopods. Brattstrom did not find any males and wondered
102 ADAPTATION TO PARASITISM IN THE CRUSTACEA
whether Ulophysema might not be hermaphrodite. He placed
this genus in the Dendrogastridre, of which it is in any case only
one representative and rather a primitive one.
Dendrogaster and Myriocladus. The genus Dendrogaster was
created by Knipowitsch 24'S for D. astericola. Of the other
species described by O. Le Roi 251-2, D. arborescens and

Figure 43. Myriocladus okadai.

A, female (note the minute size of the actual body, c, in comparison with
the ramifications). E, optical section of the central part of the body
of the young female; a, antenna, Ab, abdomen; b, buccal cone;
cp, pallial cavity; eg, lumen of stomach; OV, ovary; Th, thorax (after
Yo K. Okada). C, central region of the body with the base of the
lateral branching diverticula. D, diagram of the structure of the
central region of the body showing the base of the two lateral
diverticula in section: c, central region; b, buccal cone; di, intestinal
diverticula; 0, ovary; (E, deposited eggs;p, pallial cavity (after Yosii).

D. ludwigii were finally placed by Okada in a distinct genus,

Myriocladus, which now contains two other species, M. okadai
and M. astropectinis, described by Yosii 2S0. These types
appear to be particularly common in the Sea of Japan. They are
internal parasites of starfish.
Dendrogaster and Myriocladus are characterized by a general
regression of the mantle, which is reduced to a sort of small
 DENDROGASTRID.tE 103
cylindrical tubercle (Fig. 43A , c) covering the body proper. From
the base of the tubercle are given, off two tubes containing the
gastric diverticula, and branching more or less freely. The
two valves have thus become an arborization (Fig. 43A) with
branches enclosing the diverticula of the mantle cavity, the gas-
tric and ovarian creca. Thus here again we find the primitive
type but with prodigious malformation. It is highly probable
that nutrition takes place, at least to some extent, by diffusion
across the walls of the branching diverticula which are bathed
in the crelomic fluid of the host. At all events, we are witnessing
a profound modification of the morphology of the animal as a
result of parasitism.

I - 0,5 mm.---f
Figure 44. Male of Myriocladus okadai (after Yo K. Okada);
the left valve has been removed to show the animal's body.
al-QS,abdominal rings; an, antenna; B, buccal cone; CC, cavity of the right
valve; cs, gastric crecum; PI-PS, pereiopods; T 4-T6, fourth to sixth
thoracic segments; t, testis; vd, vas deferens.

The genus Dendrogaster sensu stricto at present contains two

species (astericola and murmanensis) with less developed rami-
fications. The two primary arms each divide into five branches,
which are lobed but not arborescent.
There is a different state of affairs in the genus Myriocladus
(created by Okada for Dendrogaster arborescens); here the two
initial arms divide into secondary arms, which themselves give
off lateral branches. This arborization attains its maximum in
M. okadai (Fig. 43A). In the female, the animal proper, greatly
reduced, lies in the central tubercle near the opening of the
104 ADAPTATION TO PARASITISM IN THE CRUSTACEA
mantle. In it one finds the buccal cone with its antennule (Fig.
43B); and an undifferentiated mass representing both thorax
and abdomen which lack distinr;:t segments. The male, on the
other hand, has retained the cypris structure with all its appen-
dages (Fig. 44).
We see what a range of regressive and, at the same time,
adaptive changes in the mantle have resulted from parasitism
in the Ascothoracica. There obviously remain many points to be
de~aded, either by knowledge of new forms or by the careful
investigation 'Of species now known, using plenty of material
in good condition. But, all things considered, we have here a
multiple series of modifications of a very definite type, induced
by parasitism.

COPEPODA
To the preceding data we shall add some facts relating to
the copepods. Amongst the Crustacea this order is the one con-
taining the most extensive and varied types of parasitism.
There are copepods parasitizing almost every group of marine
animals (Alcyonaria, anemones, annelids, Crustacea, molluscs,
tunicates, fish, cetaceans, etc.) as well as freshwater fishes; they
display all kinds 'Of parasitism: external, intestinal, even crelo-
mic, and all degrees of adaptation from considerable reduction
of the appendages to their complete disappearance, the body
being reduced to a sac, more or less bizarre in form. Usual1y
there is very pronounced sexual dimorphism as in the Bopy-
ridre; the male remains free-living or partly so, while the female
is obviously parasitic; he is a dwarf in comparison with her; in
many species he comes to live on her. The female is hyper-
trophied and produces several batches of eggs. As in the Bpi-
caridre, nutrition takes place by the sucking up or aspiration of
the host's fluids (blood, or crelomic lymph) into the gut. The
number of genera and species known is very large. It is not pos-
sible to consider them all here. I shall restrict myself to sum-
marizing the life history of an exceptionally degraded type which,
on account of its anatomical relationships with the host, has
undergone modifications of the same degree of importance as
those of Sacculina; I refer to Xenoc(£/oma 230, a parasite of the
annelid Polycirrus; it is perhaps connected with the Herpyllo-
 COPEPODA: XENOC<ELOMA 105
biidre, which are parasites of annelids and include some highly
modified types. *
At first sight XenocfEloma is simply an external parasite form-
ing a cylindrical sac on the side of its host, without any appen-
dages, cephalic or otherwise, and recognizable as a copepod by
its ovigerous sacs ~nd its nauplius larva. Under the microscope
one can see that the sac unites with the body wall of the annelid
without any discontinuity of the tissues. The histological exami-
nation of serial sections, both longitudinal and transverse, imme-
diately reveal that in reality XenocfEloma is not an external para-
site but is entirely covered by the epidermis of Polycirrus and
communicates with the exterior only by the terminal opening
from which emerge the two strings of eggs: in short, it is lodged
in a hernia of the host's skin. But its structure is paradoxical in
that it is the epidermis of the host that serves as the external
body wall of the parasite, the integument of the latter having
disappeared. On the other hand, the parietal striated muscle has
been retained and is, moreover, strongly developed as a network
which is inserted under the annelid epithelium. There is union
and complete interdependence of the tissues of both annelid and
crustacean.
There is no trace of either cephalic region or nervous system
in the copepod. Its axis, for about two-thirds of the length, is
occupied by a cavity which opens directly into the general body
cavity of the annelid and is lined by the peritoneal endothelium
of the latter; it is then in reality a diverticulum of the host's
ccelom (hence the name XenocfEloma): this endothelium is
applied tQ a wall belonging to the crustacean and constituting
the proper wall of the axial cavity and perhaps representing the
digestive tube. One sees to how great an extent there is reciprocal
penetration between parasite and host; part of the tissues of the
second being radically incorporated into the first, both morpho-
logically and functionally. It is an example which is so far
unique, and indicates extreme adaptation. One may consider
from one point of view that this arrangement is the opposite of
that shown by Sacculina. In the latter, indeed, it is the parasite
that penetrates into the host by means of its roots, but with
* The polychretes also harbour other partIcularly degenerate copepods, such as
Flabellicola, found by Gravier on Siphonostoma diplochaitos, and dIfferent types
(Saccopsis, Crypsidomus, etc.) from Greenland, which are still almost unknown.
106 ADAPTATION TO PARASITISM IN THE CRUSTACEA
Xenoc(]!/oma it is the host that covers the parasite with its epi-
dermis and penetrates into it by means of its peritoneal endo-
thelium and its ccelom. Of the copepod organism, which is of
some size (5-6 mm.long), there remains, in short, only the genital
apparatus which is, as it were, grafted on to the annelid. The
ovary continuously produces eggs which ripen in the oviducts;
filling almost the whole mass of the parasite and finally passing
out into an atrial cavity, which opens by the terminal aperture
of the sac mentioned above. In other respects the ovaries ,and

Figure 45. Xenocadoma brumpti attached to Po[ycirrus arenivorus.

i, gut of host filled with sand; a, axial cavity of the copepod;
0, oviduct;
OV,ovary; fE, oocytes undergoing maturation; t, testes (after Caullery
and MesniI).

oviducts are similar to those found in less degenerate copepods.

But Xenoc(]!/oma presents a further paradox, differing from all
other known copepods, in being hermaphrodite; the end of the
body is occupied by two large testes which produce giant sper-
matozoa (1·5 mm. long) and open into a median seminal vesicle
from which the spermatozoa pass out by spertniducts opening
at the distal extremity of the oviducts; there is self-fertilization;
the males seem to have completely disappeared.
The developing eggs give rise to a typical nauplius larva,
 COPEPODA: XENOC<ELOMA 101
which, however, completely lacks a digestive tube. It has not so
far been possible to follow larval development between hatching
and attachment to the host. It is probable that fixation takes
place, as in other copepods, only after a free-living period and
some moults. The youngest stages fouUd on Polycirrus, which
are scarcely larger than the nauplius and cannot have been
attached for long, already show rudiments of the organs of the
adult, and in particular that of the ovary. The testes do not
develop until much later. *
At this time the sub-epidermal parasitic tumour is completely
closed. Its structure is already very complex and it is impossible
to find in it the organization of other copepods. There are
grounds for thinking that, as in the case of Sacculina, it results
from a new differentiation, due to the special adaptation of this
type and largely independent of the organization of the free-
living larva.
Under the influence of this tumour the parietal musculature
of the annelid, to which the lower side of the tumour is applied,
gives way and is resorbed; the tumour then comes into contact
with the peritoneal endothelium and breaks down, so that the
endothelium comes to spread into its interior. Thus are achieved
the specialized relationships that we have seen in the adult. The
rest is no more than a matter of growth.
We see that this parasite, differing completely from Sacculina,
shows changes which are no less remarkable both from the
importance of the regressions sustained and from the establish-
ment of particularly intimate connections with the host. One
may say here that the parasite is indeed incorporated into the
host, certain organs becoming truly common, both in structure
and function.
We shall note, at the same time, in this case and in that of
Sacculina, that if there is extreme degeneration it is accom-
panied by the development of the most perfect adaptive modi·
fications ensuring nutrition and the functioning of the parasite
on the host, so that on the whole it is better to regard the changes
brought about in these organisms by the influence of parasitism
as a specialization rather than a simple degeneration.
* This is an important fact, for it proves clearly that the spermatozoa found in
the adult could not come from a male which might have copulated with the
female during a free-living phase before she settles; we actually have such a case
as this In Lerncea. '
 I CHAPTER VI

TEMPORARY PARASITISM

IN the examples that we have just considered, which are repre-

sentative of the .general state of affairs, the parasitic life begins
after an initial free-living phase and is final. After having reached
the host the organism undergoes adaptive modifications or per-
manent regressions. There are, however, exceptional cases,
which have been augmented in number by recent research,
where, on the contrary, parasitism is only a temporary youthful
phase and leads to a free-living adult with normal structure. The
young animal may sometimes undergo very profound modifica-
tions, but they are only transitory adaptations and their echoes
in the final structure are very faint or non-existent. It is a
remarkable and paradoxical state of affairs which goes to prove
how complex the effects of parasitism are; it may be called
provisional parasitism or one may use a special term, protelean
parasitism (7TpO before, 7""A"ios adult). We shall devote the
present chapter to its study.

MONSTRILLID.tE
Our first example, a striking one, is taken from the copepods
of the family Monstrillidre. In the adult state they are higl1ly
adapted for pelagic life and are rapid swimmers (Fig. 47, I): they
have a nauplius eye, as bright as a jewel, and robust appendages
for swimming; they show marked sexual dimorphism; the male
is much smaller than the female. The alimentary canal is atro-
phied and reduced to a thin non-functional filament, and there
are no longer buccal or thoracic appendages. The animal does
not feed: in short, the case is similar to the state of affairs in
praniza forms which are perfect examples ofprotelean parasites;
but this atrophy of the alimentary canal, and cessation of
feeding, may also occur quite independently of parasitism in the
adults of certain types, as in some Sphreromidre (Dynamene
108 •
 MONSTRILLIDlE 109
bidentata), in some annelids (i.e., epitokal forms, as Dodecaceria
concharum, cf. Caullery and Mesnil S 92), and in some insects.
The adult, or imago, is only a means of disseminating the ripe
genital products; it no longer needs to assimilate. Such is the
case in the Monstrillidre.
Young Monstrillidre are never found in pelagic samples;
there are only adults, as perfect as the imagos of halo meta bolo us
insects. The reason for this is that they are parasites during the

Figure 46. Monstrillid parasite, M, in the dorsal vessel of Syllis

gracilis.
Note the considerable length of the absorbing appendages, a; i, intestine
of the annelid (after Caullery and Mesnil l29).

whole period of growth, just as Giard observed in 1896 240 in

material collected by F. Mesnil; he was dealing with Thaumaleus
which was, indeed, a parasite in an annelid, Polydora giardi.
The parasite was inside a sheath which Giard compared with
the enveloping membrane in the Entoniscidre, believing that
here endoparasitism was only apparent and that in reality the
monstrillid caused a hernia within the host, and remained in
communication with the external world. Since then other
110 TEMPORARY PARASITISM

monstrillids have been found parasitizing Syllidre* (Fig. 46),'

and Salmacinat. In reality, as Malaquin recognized 253, these are
true internal parasites, lodged in the vascular system of the host,
lacking communication with the outside, and only emerging
when they are fully adult. That is why the young are never found
in pelagic samples.
Here is a summary of their development, which was thoroughly
worked out by Malaquin 253 in Hcemocera dance, a parasite of
Salmacina. The egg develops as far as the nauplius stage within
an ovigerous sac carried posteriorly by the free-living female
(Fig. 47, I). The nauplius (Fig. 47, II) lacks a digestive tube and
the third pair of appendages is reduced to a pair of hooks. It
swims actively, then makes its way through the integument of
Salmacina; here, it moults, casting off both body wall and appen-
dages and becoming reduced, like Sacculina, to an undifferen-
tiated cellular mass (Fig. 47, III). In this form it makes its way,
doubtless by amceboid movement, into the longitudinal vessel
of the annelid. There it surrounds itself with a chitinous cuticle,
a proceeding equivalent to a moult. At the anterior extremity
there develop two unsegmented lobes (Fig. 47, IV), which
elongate as two long intravascular appendages; they function as
organs of absorption, like the roots of Sacculina. In the species
parasitizing Polydora and Syllis there is only one pair of
appendages; in Monstrilla dance, found in Salmacina, there are
two (Fig. 47, V); in Monstrilla helgolandica, a parasite of Odos-
tomia rissoides, discovered and studied by Pelseneer 264, there
are three pairs. The morphological significance of these appen-
dages is an interesting problem: are they entirely new adaptive
structures, or are they metanaupliar appendages (mandibles and
maxillre which no longer exist in the adult) changed into organs
of absorption?
The first chitinous cuticle formed around the parasite is cast off
and replaced by another which will form an expanding envelope
persisting throughout the rest of development; it is orna-
mented posteriorly with rows of little spines and constitutes the
... Besides the species shown in Fig. 31, I had the opportunity, in Naples in 1906,
of finding another case (m connectIOn with a species that was certainly different)
in another syllid, but I was unable to pursue this observation further; I mention
it here in order to record it.
t Pelseneer even found a species of monstillid parasitIzing a mollusc, Odos-
tomia rissoides 264.
 MONSTRILLIDlE 111
sheath, incorrectly mterpreted by Giard, which does indeed
belong to the parasite and has probably the morphological value
of a moult.
Within this sheath, and feeding by absorption through the
appendages just described, the adult monstrillid progressively
differentiates with all its organs and appendages (Fig. 47, VI),

FIgure 47. Development of some Monstrillidfe (after Malaquin).

I, Htemocera dante, adult female carrying an egg mass, 0; II, free-swimming
nauplius; III, the stage at which the animal is an undifferentiated
cellular mass in the vessel of the host; IV, development of the
absorbing appendages, a; V, larva with two pairs of absorbing appen-
dages; VI, stage towards the end of the parasitic period; the mon-
strillid is completely differentiated within the larval sheath.

and its gonads. When development is complete it emerges from

the sheath and its host in the perfect state, as a butterfly leaves
the chrysalis. Its pelagic life begins, during which the animal
does not feed; the sexes meet, the female lays her eggs and
carries them in the ovigerous sacs until the nauplii hatch.
112 TEMPORARY PARASITISM

Such is the'development of an individual monstrillid. It shows

us the greatest possible degree of endoparasitism, starting off by
complete regression, continuing by a method of nutrition
depending on diffusion through roots, and therefore doubly
reminiscent of Sacculina. Here again we know of no other stage
in the achievement of so specialized an adaptation; it must
nevertheless result from a long evolutionary process. Only, far
from there being a final regression, as in the Rhizocephala and
Xenoct1!loma, here there is only temporary degeneration, which is
not reflected in the adult, except for the complete atrophy of the
alimentary canal, the buccal and thoracic appendages. One could,
object that the adult ancestors of Sacculina were very different
from the pelagic copepods ancestral to the Monstrillidre, and
that this difference is sufficient to explain the different condition
of the two actual parasites. But Xenoct1!loma is a copepod like
the Monstrillidre, whose ancestors were free-living in the adult
state, and the objection is not valid here. In any case, the Mon-
strillidre are by no means an isolated example.
In reality, the evolution of a parasite depends in the first place
on the connections which are established between its host and
itself. We may imagine that the unmodified adult has persisted
in the Monstrillidre because in this family adaptation to para-
sitism has been in special temporary structures, the organs
of absorption, and the organization of the adult has remained
independent of these structures; or else, if, as I believe, these are
modified metanaupliar appendages, the result of this adaptation
has been the loss of these appendages in the adult, and that has
doubtless involved the atrophy of the mouth and the alimentary
canal. But, this sacrifice once made, so to speak, the rest of the
final organization is built up more or less sheltered from para-
sitism and independently of it, while in Xenocadoma the whole
of, the young organism is adapted to parasitism and ultimately
it degenerates.
PARASITIC PLACENTATION. Giard has very suggestively,
and to my mind very rightly, compared this kind of parasitism
to placentation such as we find in mammals, salps and other
animals: the comparison applies, moreover, to several of the
examples which follow. Parasitic placentati(Jn differs from nor-
mal embryonic placentation in that the latter is a graft on an
individual of the same spec;ies instead of on an alien one. Physio-
 P ARASITIC PLACENTATION 113
logically, the organs of absorption in a monstrillid are equivalent
to the villi in the placenta of mammals whose embryos feed by
means of this placenta and are truly parasitic on their mother;
this does not prevent them from reaching a final state which
reflects nothing of this temporary parasitism. But, here again,
this parasitism is operated by a subsidiary organ, while the
embryo itself, in every part of its structure, is organized for an
independent life. One can complete this comparison by con-
trasting the case of Xenocteloma with it. This animal, too,
achieves placentation on its host. Nothing could be better com-
pared with a placenta than its axial cavity where there is the
most intimate union, as in a mass of maternal and placentary
villi, of the peritoneal endothelium of the annelid and the
tissue of the crustacean. But here placentation, instead of being
achieved by means of an accessory structure, is established at
the expense of the essential organs of the individual, which are
thus irremediably utilized. There is no more material available
for constructing the normal adult. It is clear, therefore, that
there is no irreducible contradiction between the two cases but
that they may be connected by transitional stages. In many of
the cases ofprotelean parasitism that we are going to review, the
animal emerges more or less in the condition of the perfect
imago* with its sexual organs completely mature, and has
nothing further to do but immediately to dispose of the eggs
without having to elaborate anything.
In the Crustacea we have another example which can be
related to that of the Monstrillidre, in that it is limited to the
growing period: this is the case of Gnathia with which we
were concerned earlier (pp. 66-7). It is, in other respects, less
accentuated and only reflected in the mouth-parts and the
digestive apparatus. It may be noted that the mouth-parts,
which have undergone adaptive modifications in the parasitic
phase, disappear in the adult.

ORTHONECTID.tE
We may consider the Orthonectidre as an example of
protelean parasitism. Let us' begin with the cycle of Rhopalura
'" We may repeat that types such as the MonstriIlidre behave like holometa-
bolous insects. Parasitism goes no further than the larval organs, leaving the
permanent organs to develop as if from imaginal discs.
114 TEMPORAR Y PARASITISM
ophiocomce, which is the most completely known, starting off
with the larva. These ciliated larvre, which escape from the free-
living female, penetrate into the genital openings of A mph iura
squamata and give rise in various tissues of the ophiuroid to
plasmodia in which the germ cells differentiate and develop

Figure 48. Developmental cycle of Rhopalura ophiocomce ..

1, emission of male and female adults from the host, Amphiura squamata;
2, fertilization; 2', ripe oocyte; 3, emission of polar bodies; 3, fertiliza-
tion (stage of vesiculate pronuclei); 4, 5, segmentation; 6, ciliated
larva; 7, emission of ciliated larv<e; 8, 9, their penetration into the
ophiuroid; 10-14, initial stages of the plasmodia and differentiation
of the germ cells; 15, male and female plasmodia.

into the males and females of Rhopalura. These, in fact,

constitute a new generation for which the plasmodium acts
as a placenta. They emerge, like the Monstrillidre, in the adult
state to lead an independent life, for which they are obviously
constructed. The adult orthonectid has much more the appear-
ance of a free-living animal than of a parasite. Its powerful
 EUNICIDJE 115
cilia allow it to swim rapidly in the surrounding water. A more
careful histological study than any so far made will probably
disclose a nerve ring. What is lacking is the digestive apparatus,
as in the Monstrillidre, and this is almost certainly because the
life of the adult is here even more ephemeral, and entirely
devoted to the production and dissemination of larvre. Indeed,
both sexes are perfectly ripe on leaving the host; after a few
moments, and while they are swimming rapidly about, pairing
takes place (Caullery and Lavallee 134) and the fertilized eggs
immediately begin to develop. After about twenty-four hours
the ciliated larvre hatch and proceed to complete the cycle by
infecting another ophiuroid. We may suppose that the absence
of a gut in the Orthonectidre has not been determined simply
by degeneration brought about by parasitism, but also, perhaps
altogether, because the animal does not need to feed during its
very short adult life. Of the two gen~rations which alternate
regularly in this cycle, it is the asexual generation, formed by the
plasmodia, which is really parasitic. The sexual generation may
be considered as developing with the assistance of a type of
placentation, its own independent life being essentially
ep~emeral.

EUNICIDLE
A certain number of Eunicidre develop up to the adult stage
as internal parasites of annelids or other invertebrates, without,
however, showing any sign of regression except for some
simplification of the jaws. Here are the cases now known to us:
Oligognathus bonellia (SpengeI 184) developing in Bonellia and
attaining a length of 10 cm. with more than 200 segments
(Naples).
Hamatocleptes terebellidis (Wiren, 1886) in the 10ngitudinaJ
vessel (cf. the Monstrillidre) of Terebellides strami (Green-
land).
Labrorostratus parasiticus (de Saint-Joseph 183) in various
syllids, particularly Odontosyllis ctenostoma (English Channel).
Oligognathus parasiticus (Cerruti, 1909), in Spio meczniko-
vianus (Naples). .
Labidognathus parasiticus (Caullery 179) in a terebellid from
the Siboga expedition (Malay Archipelago).
116 TEMPORARY PARASITISM

It seems that another species was collected under the same

conditions in Marphysa by Koch (1847).
It is, then, a type of development which is widespread in the
Eunicidre. The parasite often comes to be as long as the host in
which it lives. In spite of the intensity of such parasitism the
annelid remains normal and must leave its host when it is ready
to reproduce. It certainly enters at an early stage (one Labro-
rostralus observed by de Saint-Joseph possessed only nine seg-
ments with neither parapodia nor chretre); it then accomplishes
the whole of its growth as a parasite, without undergoing any
regression.

UNIONIDLE
The bivalves of this family, the freshwater mussels, Unio,
Anodonta, Margaritana, pass through an equally intense phase
of protelean parasitism which leaves no trace in the adult. The

Figure 49. Glochidium larva.

a and b, free-living stage in optical section, from the internal aspect
(after Flemming); c, two glochidia encysted in a branchial lamella of
Cyprina (after Harms).

eggs are incubated amongst the branchiallamellre of the mother

and give rise to a larva known as the glochidium, of a very
special character. It has a bivalved shell with a pair oflong teeth
in the plane of symmetry, and accessory spines laterally
 UNIONIDlE 117
(Fig. 49 a-b). The mantle is covered by a special kind of epithe-
lium with tufts of sensitive hairs. The visceral mass is quite rudi-
mentary; there is no digestive tube. In the centre there rises up a
long slender mobile tentacle that can be seen moving between
the valves. At this stage the glochidia are discharged and float
about. Leydig, in 1866, discovered that they become parasites
of fishes (Cyprinidre). When a glochidium comes into contact
with a cyprinid (often through being drawn in with the
respiratory current), then as a result of a tactile reflex in the
tentacle described above, the valves tend to close and their teeth
penetrate the tissues of the fish, particularly on the branchial
lamellre (Fig. 49c). They are easily found at the right season and
it is very simple to produce experimental infection of cyprinids
and amphibia. The host rapidly reacts to the presence of the
parasite (we shall return later to this phenomenon) and envelops
it in a thick vascular cyst. The mantle cells of the glochidium, as
Faussek has shown, although epidermal in character, behave as
active phagocytes, digesting, on contact, the tissues of the host
and so ensuring the nutrition of the young parasite, which has
no alimentary canal. The vascular tissue of the cyst formed by
the host may be compared with a placenta. Under these con-
ditions of nutrition the definitive organs (digestive tube and
mouth, foot, kidney, etc.) of the young Unio gradually develop,
and the definitive shell slowly forms around that of the larva.
After a delay, depending on the temperature (80 days at 8°-10°,
21 days at 16°_18°, 12 days at 20°, according to Harms 337), the
young mollusc abandons the cyst, which it ruptures with its foot,
leaves the fish and falls to the bottom, where it will complete its
growth.
Here again we have a case of parasitism that is intense and
temporary, anticipated by a preliminary adaptation which allows
of the differentiation of special organs, simultaneously with the
regression of normal organs. The relationship with the host,
during the period of parasitism, suggests a striking physiological
analogy with a placenta, and nutrition is carried on by the
metabolic activities of accessory organs (larval mantle). The
definitive organs (digestive tube, etc.) are unaffected by
parasitism; one may therefore consider them to be formed in the
normal way. Contrary to the state of affairs in the Monstrillidre,
the digestive tube here persists, evidently because parasitism
p.s.-5
118 TEMPORAR Y PARASITISM

comes to an end at a very early stage and the whole of the

animal's growth is accomplished in the free-living state. *

GORDIAN WORMS
The gordians, a group related to the nematodes, complete the
whole of their growth as internal parasites of terrestrial arthro-
pods (insects and myriapods). When adult they escape from the
host by breaking out of it under the influence of humidity, and
reproduce, outside it, in the free-living state. They resemble long
thin twists of twine that have been compared to the strings of a
violin; the females are several decimetres long, sometimes more
than a metre; the males are usually smaller. These strings undu-
late and move about in the water. The digestive tube is com-
pletely atrophied.
Their development and biology were thoroughly studied by
Dorier 189 in 1930. Their escape from the host takes place as a
rule when the latter is in water (generally by accident). Once free
they usually form clusters containing males and females, and
pairing takes place. These adults, unable to feed, cannot live
long in a free state. The eggs are laid immediately after pairing
and the larvre hatch out. They are free-living for a time and then
either encyst or are swallowed by an aquatic animal (insect
larva, mollusc, etc.) in which, however, they soon encyst again.
For the completion of development it is necessary that the inter-
mediate host, and with it the cysts, should be swallowed by a
suitable final host, which is always terrestrial. The gordians
are thus essentially internal parasites, but they have an adult
free-living phase during which reproduction takes plaee. They
may therefore be classified amongst the protelean parasites.
Completely analogous conditions are to be found in species
of Nectonema, which may be regarded as the marine representa-
tives of the gordians. They, too, look like long thin strings, white
and opaque, and are found from time to time in the surface
plankton, where they were first pointed out by Verrill (1879).
Externally they possess two brushes of long swimming chretre,
* One of the marine Aviculidre, Phl!obrya, has a larva analogous to a glochi-
dium, but Its development IS not known. The larva of South American Umorudre,
called alasidium, IS rather different from the glochldium; Itis not known for certam
whether it has a parasitic stage in fishes.
 ENTOMOPHAGOUS INSECTS 119
arranged longitudinally. Since then they have been seen sporadi-
cally as internal parasites in various decapod Crustacea: Pala-
monetes (Ward, 1892), Pontophilus (Brinkmann 187); Ch. Perez
(199) found them at Roscoff in Paguridre (12 individuals from
239 specimens of Anapagurus hyndmanni) and once saw a Necto-
nema emerging from one of the pagurids in an aquarium; under
the uniform cuticle the chretal brushes were visible: evidently
the newly freed animal was going to moult. In 1930 Brink-
mann 187 was able to make more complete observations,
finding that, in Norwegian waters, the galatheid Munida tenat-
mana is the regular host of Nectonema munida. Out of 776
specimens of Munida examined, 61 were parasitized; the para-
sites were in clusters in lacunre in the cephalothorl:ix. The males,
completely devoid of pigment, were from 90 to 155 mm. long,
the females from 170 to 845 mm.; six of them exceeded one
metre. The chretre attained a length of 300tt. Nectonema is
clearly a marine gordian, and, like Gordius, is an example of pro-
telean parasitism.

ENTOMOPHAGOUS INSECTS
The most considerable example of protelean parasitism is
provided for us by the entomophagous insects, in the first place
by Hymenoptera and secondarily by Diptera. Far from con-
sisting, like the preceding cases, of curious and specialized
exceptions, it is here a very general phenomenon and of funda-
mental importance for the equilibrium of species in nature.
Starting either from the egg, or from a more or less precocious
larval stage, they develop as parasites in, or on, other insects and
emerge as free-living imagos in no way modified by this pre-
liminary parasitism. Here again the imago is usually short-
lived, entirely engaged in disseminating the eggs, and in many
cases it takes no food; the alimentary canal is often so con-
structed that it is impossible for the animal to feed.
The importance of this type of parasitism is seen from the
number of species of Hymenoptera alone that exist: there are
200,000 of them, perhaps more, according to Sharp, and they are
distributed amongst ten families. * The parasitic Diptera, which
* The Cynipidre, Proctotrypidre, Chalcididre, Ichneumonidre and Braconida:
are the most important.
120 TEMPORARY P ARASITIS,M
are less numerous and are not limited to insect hosts, are also
legion; they belong to the Calyptene. * Of the story of this para-
sitism we still know only vague scraps, pointing to many impor-
tant aspects and processes of fundamental interest for biology.
Each species has for its victim a more or less strictly specific
host, and all these victims perish without reproducing. The part
played by a phenomenon of this magnitude is at once apparent.
As soon as one of these entomophagous Hymenoptera begins
to multiply-and the hundreds of eggs l~id by these minute
insects allow of very rapid multiplication under favourable
circumstances_:'_the parasitized species is decimated. On the
other hand, if the latter becomes exceptionally abundant it
immediately supplies numerous victims to the parasite and so
favours its reproduction. The entomophagous insects are thus by
far the most efficient natural agency checking the mUltiplication
of a very large number of insects, above all, the Lepidoptera
and also the Coleoptera. In particular they are a factor of the
first importance in the control of harmful insects; indeed, they
are the most powerful barrier to their excessive propagation.
In addition, there is a matter worth mentioning here,
although, strictly speaking, it does not come into the scope of
this work: attempts are now made to utilize insects from
this point of view, both experimentally and directly. The entomo-
logical service in the United States has regularly made use of
these data. Under natural conditions a comparatively stable
equilibrium is automatically established amongst the species
composing a fauna, and it is both difficult and dangerous to
upset it. But in our time the intensive development of communi-
cations and trade between countries and continents far removed
from one another constantly introduces grave disturbances into
natural states of equilibrium. The accidental introduction of a
new insect into a fauna where it did not previously exist may
have serious consequences, even when in the country of its
origin it was relatively inoffensive. Phylloxera on vines, intro-
duced from America into Europe, is a terrible example of this.
There is another more recent one in the Colorado potato beetle,
Leptinotarsa decemlineata. It was possible to check the first inva-
sions into Germany in the second part of the 19th century.
A second invasion, in the Bordeaux region of France, during
* Anthomyidre, Tachinidre, Dexiidre, Sarcophagidre, (Estridre, Muscidre.
 ENTOMOPHAGOUSINSECTS 121
the 1914-1918 war, was not dealt within time and now the beetle
has become established in France, and every year, in spite of the
war waged against it, it causes considerable damage. Conversely,
very many Asiatic and European insects introduced into the
United States have found suitable conditions for breeding there,
and have thus changed into formidable pests. *
Such was the case with two of the Bombycidre, which caused
minor damage in Europe, but in the United States rapidly
became terribly destructive: Lymantria dispar (Gipsy Moth) and
Euproctis chrysorrhrea (Brown Tail). The gipsy moth invasion of
America was started by the escape of a few caterpillars that were
bred by the entomologist Trouvelot at Medford, near Boston,
about 1868. He had sent for this species from Europe in order
to study hybrids between it and the American forms. In a few
years Lymantria dispar had multiplied to the extent of destroying
whole forests, and also the trees of towns in Massachusetts and
the neighbouring states. The fight against insects there is carried
out by an annual expenditure of several millions of dollars, and
it is now based primarily on the exploitation of parasitism by
the entomophagous insects. As early as 188p Riley had tri-
uplphed over an exotic scale insect, Icerya purchasi, which was
devastating the citrus orchards of California, by introducing and
naturalizing an Australian coccinellid, Novius cardinalis,
which was, moreover, not a parasite but a predator of the scale
insect; the same experiment has been repeated in other countries
with constant success. Riley applied the same principle against
the white cabbage butterfly, Pieris brassicl£, using an entomo-
phagous hymenopteron, Apanteles glomeratus, and against the
olive scale, Lecanium olel£, using a chalcid, Scutellista cyanea, a
parasite from the Cape.
One of the principal reasons for the enormous increase in
numbers of an insect newly introduced into a country like the
United States is that it arrives there without being accom-
panied by the many parasites which, in its native country,
check its multiplication. In the experimental introduction of
these parasites equilibrium must be re-established. Working
from this principle, the naturalists of the Bureau of Entomology
* We know, moreover, how similar introductions of European plants and
ammals into Australia and New Zealand have had disastrous consequences for
numerous elements of the indigenous fauna and flora of these isolated regions
where independent states of equilibrium had been reached.
122 TEMPORAR Y PARASITISM
in Washington attempted to control the Gipsy and Brown
Tail Moths by coming to Europe to make a thorough investi-
gation into all the parasites of these two species; then hundreds
of thousands of caterpHlars and pupre of both moths were
taken from Europe and Japan to America so that the para-
sites could be collected, bred in numbers in special laboratories,
and finally acclimatized under natural conditions 297, 305. In
Europe, no less than 27 species of Hymenoptera, and 25 species
of Diptera are known to attack the caterpillars of Lymantria
dispar. The caterpillar of a geometrid, Cheimatobia brunnea, is
parasitized in Europe by 63 Hymenoptera.
But a war of this nature leads to many surprises. Together
with the parasites that destroy a harmful species in conformity
with the intentions of the experimenter, there are the parasites,
or hyperparasites, of these useful parasites, which, by attacking
the latter, reduce their numbers and thus indirectly favour the
propagation of the enemy. The parasites are auxiliaries, the
hyperparasites adversaries, and they are introduced simul-
taneously. The balance of the operation will then depend on the
predominance of the one over the other, once acclimatization
has been achieved. Sometimes, too, under new conditions, a
parasite changes into a hyperparasite. Thus, a chalcid, Ptero-
malus egregius, a European parasite of Euproctis chrysorrh(Ea,
also lays its eggs in the larvre of a braconid, Apanteles lacticoior,
which itself is a parasite of Lymantria. It also happens that
American species, parasites of indigenous caterpillars, have
changed, after the introduction of the European Hymenoptera,
into hyperparasites of these Hymenoptera, thus becoming harm-
ful themselves. Apanteles ju/vipes, a braconid introduced· from
Europe as a useful parasite, was attacked in the United States
by 16 American species, which became hyperparasitic on it and
thus checked its expected increase. One sees how complex and
important a part is played by the entomophagous insects in the
balance of species and on what a vast scale this factor works;
and, as a result, how interesting this class of parasite is, both
for general and applied biology. In the United States, the war
waged under the direction of the Bureau of Entomology against
the Gipsy Moth has supplied biology with data of paramount
importance which it .was only possible to assemble thanks to
enormous resources of material, equipment and staff.
 ENTOMOPHAGOUS INSECTS 123
But let us return to the investigation of parasitism itself
amongst the entomophagous insects. It is clear that a pheno-
menon of this magnitude admits of a considerable number of
categories which cannot here be reviewed in detail. They fall
into the following major classes:
1. The eggs of the parasite are laid in the external environ-
ment, and the larva, after hatching, searches actively for its
victim on which it lives as an external parasite.
2. The eggs being la1d under the aame conditions, the larva
penetrates into its host where it completes its development as
an internal parasite.
3. The parasite inserts its eggs directly within the host where
they will complete their entire development; in this case the eggs
are either placed in larvre of various instars, or they may be
inserted in an egg which has not yet developed.
The development of entomophagous insects, although it has
been the subject of a large number of researches, is still very
incompletely known to us. The imagos are discovered more
easily since very often the rearing of a larva, e.g., a caterpillar,
brings about not the emergence of the awaited butterfly but, in its
stead, and at the expense of the chrysalis, either hymenopterous
or dipterous parasites. But there are few species in which the
whole of the development is known, and we must still expect
many interesting facts from these studies.
The circumstances in which the eggs are laid, which are often
difficult to observe, set us problems of very great general import-
ance. How does the parasite recognize the presence of the larva
or egg on which it will deposit its eggs and where its progeny
will find favourable conditions for development? What factor,
for example, reveals to the Ichneumonidre or Braconidre the
presence of a wood-eating larva under the bark of a branch or
trunk? And nevertheless the hymenopteron knows how to find
the exact point where, by drilling with its ovipositor, it will
deposit its egg, just touching the larva that it cannot see but
wishes to parasitize. Thus Thalessa luna tor reaches the larva of
Sirex gigas, deep in wood. And so, as Picard and Lichten-
stein 301 have shown us precisely, does the braconid Sycosoter
lavagnei drill through a branch of the fig tree to lay its egg on
the larva of a scolytid, Hypoborus ficus, which lives in the wood.
From the egg thus deposited there hatches a larva which remains
124 TEMPORAR Y PARASITISM

motionless on the host without penetrating into it: with its

sharp-edged mandibles it pierces the skin of the Hypoborus
larva and sucks'up from the general body-cavity the fluid on
which it lives, slowly emptying its victim which nevertheless
continues to feed. It is true that this instinct is far from being
infallible and many insects sometimes make regular mistakes
to the detriment of their progeny. Thus Pteromalus egregius,
which lays its eggs in the caterpillars of Euproctis chrysorrh(J!a,
frequently places its eggs on the cast skins of the caterpillars
where they are lost. And so, quite generally, many larvre are lost
through the mistakes made by the females when laying their
eggs. * '
The larval forms of entomophagous insects are often most
unexpected and most difficult to explain. Such are those of
Platygaster, a genus of Proctotrypidre-, which lays eggs in the
larvre of the Cecidomyidre, and whose development was first
studied by Ganin, and later by Marchal 303. The first-stage larva
is quite different from the vermiform larvre commonly found in
the Hymenoptera. It is strongly chitinized with a huge and dis-
tinct cephalic region and a small abdomen. It recalls a copepod
and hence has been called a cyclopoid larva. The mandibles are
enormous. Its affinities will probably be clearer when we are
better acquainted with the development of species where the
larva is free-living to begin with and only penetrates into the
host at a rather later stage. Such is, for instance, the planidium
larva, discovered by Wheeler 398, belonging to the chalcids
Orasema and Perilampus, which penetrates into tachinid larvre,
sometimes themselves the internal parasites of caterpillars. It is
very different in structure from the usual vermiform larva. The
first stage larvre of parasitic Hymenoptera must, besides, bt> very
variable. Some of them are illustrated here (Fig. 50), amongst
them that of Eucoila keilini, discovered by Kellin 300 in a larva
of Pegomyia (Diptera) .
.. The development of the larvre of entomophagous insects in other insects
makes it necessary for the former to leave the body of the latter before the emer-
gence of the imago and this is sometimes achieved by arrangements which appear
as very precise adaptations. In this' connection Kunckel d'Herculais observed
that a dipterous fiy, Systropus conopoides, one of the Bombyliidre, WhICh develops
in the caterpillar of Sibine bona:rensis and becomes enclosed in the pupal cocoon,
leaves it by the same means as the pupa itself; with the help of a sharp point on
the head and a gyratory movement It cuts a ring in the cocoon. Thus the parasite
has acquired an organ slIDilar to that of the host. Ktinckel glVes thIS parallelism
the name of homll!opraxy (op.o{os, sImilar, "pag,s, action).
 ENTOMOPHAGOUS INSECTS 125
The difficulty of understanding these larval forms applies par-
ticularly to those that are not manifestly adjusted to the con-
ditions existing where they are found. And yet the egg from
which they come is adapted to these conditions both in its struc-
ture and in its early development. It is very poor in yolk and
segmentation is total, which is related to the fact that the larva
will immediately find beside it the wherewithal for nourishment.
Doubtless, an ancestral larval form has been retained here by
hatching at a very precocious stage, in the .same way that the
free-living imago is retained at the end of the larval period.
Usually these entomophagous larvre live in or on their hosts
without destroying their essential organs, or even without
t 2

;} 4

Figure 50. Primary larva! of various entomophagous Hymenoptera.

1, Platygaster (Trichacis remulus) (after Marchal); 2, planidium of
Perilampus (after H. S. Smith); 3, Teleas· (after Ayers); 4, Eucoi'!a
keilini (after Keilin).

devouring the fat body, as has sometimes been believed. At the

beginning of development, and until the emergence of the larva,
they are frequently surrounded by an epithelium originating from
the host and isolating them from it. Within this envelope the egg
segments and right from the start the actual embryo is separated
from the easily stained vegetative masses which fragment and
evidently play an important part in nutrition. Here again,
then, at least at the beginning of development, there is an
arrangement for nutrition recalling placentation. This must play
an important part in the retention of the initial1arval forms
with which we are concerned. When these larvre have hatched
and are mobile within the host, they suck up the fluid of the
general body cavity which contains substances extracted from
5*
126 TEMPORARY PARASITISM

the plant food of the host and elaborated by it. Their develop-
ment would doubtless be checked if the host only ceased to feed.
Thus the latter may be ctmsidered as a mere intermediary for
transforming nutritive substances during larval growth and, as
the imaginal organs are for the most part new structures which
among the holometabolous insects play no part in the func-
tionallife of the larva, so it is clear that in any causative sense
the parasitism of the larva may not affect them and may lead to
an imago similar to that of insects with free-living larvre. In
this sense t4e present example is connected with some preceding
ones, such as that of the Monstrillidre. One may explain, too,
that in families like the Cynipidre there are, in addition to the
entomophagous forms, other closely related types that are gall-
forming. Under conditions that we shall come to later, they
induce in plants, particularly oaks, the formation of galls where
the plant accumulates reserve materials and juices on which the
parasitic larvre feed. Thus they take directly from the plants
what entomophagous forms absorb indirectly, and in an already
elaborated state, in the body of a host. It is clear that different
species of the same type have been able to adapt themselves to
either regime, much less different in reality than in appearance.
But still this is only a vague analogy and it is obyious that the
precise physiological investigation of nutrition in both the para-
sitic forms as well as the gall-producing ones will be of very great
interest.
In the whole of this discussion we have so far only considered
entomophagous insects, but a certain number of foims develop
in an analogous fashion as plant parasites, and in animals
other than insects. One finds parasitic dipterous larvre in widely
different groups. When Keilin was studying the development of
Pollenia rudis, a very common fly whose larvre he found in the
seminal vesicles of an earthworm, Allolobophora chlorotica, he
reviewed the general features of parasitism in the larvre of the
Cyclorrhapha. A certain number of these Diptera are of special
interest as parasites of vertebrates, particularly of mammals and
man. The phenomenon of myiasis is interesting on account of the
variety of conditions it reveals in this type of ,parasitism. These
somewhat cursory indications allow us to perceive the enormous
extent and practical interest of this subject of the entomo-
phagous insects.
 CHAPTER VII

PARASITES WHICH CHANGE THEIR HOST

THE preceding chapters have shown us clearly enough that the

major event in the life of a parasite is the meeting with the host.
Failure to find, at the right moment, a suitable host-and this
is usually strictly specific-results in the death of the young para-
site, embryo or larva. An enormous number of individUals fails
to make this propitious meeting and is thus lost; we shall see
how this immense loss of individuals is compensated. But there
are some parasites for which the cycle of development is even
more complicated and full of risk; they are those that can only
complete it by passing through two successive hosts: the first,
a temporary orJe called the provisional or intermediate host, in
which the immature parasite lives, and the second, called the
final or definitive host, in which the adult stage is reached. There
are even some parasites that must pass through three successive
hosts. These changes of host are termed migrations and the para-
sites in which they occur are said to be heteroxenous.
The existence of migrations complicates the study of para-
sites, for it is extremely difficult, in general, to identify them in
their successive phases or, on finding them in one of two hosts,
to determine what the other one is. On this account the story of
the migrations of parasites is of special interest and we shall
review the different cases known to us. passing rapidly over the
classical examples and laying more stress on others discovered
later.
CESTODA
The first case of parasitic migration to be discovered was that
of the cestodes. It was elucidated about the middle of the 19th
century. Until then they were considered to be two distinct
zoological types, one the ribbon-like Tania dwelling in the verte-
brate intestine, the other the vesicular worm cysts, which we
127
128 PARASITES WHICH CHANGE THEIR HOST
know today as the cysticercus stage, situated in the deeper
organs such as the peritoneum, the muscles, the liver and
brain.
Kiichenmeister and P. J. Van Beneden were the first to show
experimentally that the cysticercus was simply a stage in the
development of the tapeworm, and that the change of one into
the other was conditional on the change of host. The cysticercus
dwells in an intermediate host and becomes a tapeworm when it
is ingested, with all or part of this temporary host, by the defini-
tive host. Without this necessary step, it remains indefinitely
in the cysticercus stage and finally degenerates.
Today the developmental cycle of the cestodes is classical and
has actually been followed out in a considerable number of
species. Let us summarize the case of Tania solium. The egg
develops in the uterus of the segment or proglottis of the trenia,
where it originated, and gives rise to an embryo provided with
six hooks, arranged in three pairs; this is called the hexacanth
embryo or the onchosphere. Together with the proglottis, it is
evacuated from the host. If it is then swallowed by a mammal-
the pig is the typical host but other species may serve-the egg
shell is broken down by the action of the gastric juices and the
onchosphere is set free. With the help of the hooks it passes
through the intestinal wall, makes its way into the blood vessels
and lymphatics and is drawn into the general circulation. Finally,
in the capillary network, it attaches itself to the connective
tissue of the muscles, swells up into a vesicle and so becomes a
cysticercus, the so-called Cysticercus cellulosa. At the end of
some weeks an invagination develops in the vesicle and in it
there differentiates a scolex, a structure which may conveniently
be termed the head of the future Tania. But, at this point,
development is arrested tend the cysticercus may remain in this
state for months or even years. This cysticercus infestation of the
muscles of the pig produces the condition known as "measly"
pork. If such meat is eaten by an appropriate mammal such as
man, the cysticercus is set free, the scolex evaginates, attaches
itself to the mucous membrane of the intestine, elongates and
strobilates into the adult Tania.
One finds in textbooks of zoology and parasitology the des-
cription of the life history of many species. I shall confine myself
here to giving a table in which some of them are summarized.
 CESTODA 129

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130 PARASITES WHICH CHANGE THEIR HOST
Each one of these cycles has its own particular characteristics.
The intermediate hosts are very varied, a circumstance which
has led to surprises and mistakes. P. J. Van Beneden carried out
experiments before a commission in Paris in order to prove the
specific identity of Cysticercus pisiformis and Tania serrata.
Young dogs fed exclusively on milk were made to swallow cysti-
cerci from rabbits. At the autopsy he was surprised to see that,
in addition to Tania serrata, the dogs contained Dipylidium
caninum. Today this is easily explained because although the

a 6 c
Figure 51. Larval forms of Bothriocephalus latus (after Rosen).
a, free-living larva (coracid); b, Cyclops infested by a procercoid larva, c.

dogs were fed entirely on milk they were nevertheless infested

with the other species through their fleas and lice, about which
no precautions had been taken.
The cycle is sometimes complicated by there being two inter-
mediate hosts instead of only one. Such is the case with Bothrio-
cephalus, whose complete life cycle was worked out by
F. Rosen 172. It has been long known that a,Bothriocephalus
larva infests man. It is an elongated whitish worm, called a
plerocercoid larva, which lives in the viscera and muscles of
different fishes (Salmonidre, pike), and man becomes infected
 CESTODARIA 131
through eating undercooked fish* and, in particular, their roes
(caviar). But the stages between the egg and this larva were
unknown. The eggs of Bothriocephalus only develop when they
have passed outside the host and then very slowly, taking
several months; in running water they develop in 10-15 days at
30-35°. The hexacanth embryo is here covered with a coat of
long cilia; it hatches and lives in water as a free-swimming larva
or coracid (Fig. 51a). The researches of Rosen have shown that
this coracid must be ingested by the first intermediate host,
which is a copepod (Cyclops strenuus or Diaptomus gracilis). It
passes into the general body cavity of the hostt and there
develops into a larval form called the procercoid larva (Fig.
51b, c). On swallowing copepods infested with these larvre, fish
such as salmonids and pike become infested in their turn with
the plerocercoid larvre previously known. Thus here there are
two intermediate hosts-copepod and fish-preceding the defi-
nitive host where the actual Bothriocephalus develops.t Under
these circumstances it is not surprising that Bothriocephalus
must produce immense numbers of eggs; it is frequently eight
metres long and may be fifteen, with several thousand pro-
glottids.
CESTODARIA
The best established facts and the conclusions to be drawn
from them can scarcely ever be generally applied without reser-
vations and exceptions, and the cycle in the Bothriocephalidre,
as it has just been set out, provides us with an interesting
example throwing light on this. The cycle is repeated with minor
variations in numerous genera and species, but the increase in
our knowledge shows that it allows of exceptionally interesting
variations. These concern the cestodes that are classified as
* For this reason, Bothriocephalus is found particularly in the lake districts of
Switzerland and Italy, and in Finland.
t Development is not successful except in certain species of copepods; in others,
such as Cyclops viridis, the coracids are digested.
t Rosen has shown expenmentally that the same type of development occurs
in Trill!nophorus nodulosus, one of the Bothriocephalidre which, when adult, lives
in the pike (intermediate hosts: Cyclops, perch); also in Abothrium in/lmdlbuli-
forme, a parasite of trout (Trutta lacustris) with a coracid devoid of cilia (inter-
mediate hosts: Cyclops, perch); and, finally, in Ligula simplidssima which. when
adult, lives in the intestine of water birds (Colymbus, Mergus, Anas). The eggs of
Ligula pass out with the freces of the bird host and fall into water. The larva
passes through a Ciliated coracid stage, infests a Cyclops and later a fish (gudgeon,
bream or roach).
132 PARASITES WHICH CHANGE THEIR HOST
Cestodaria: Ampl(ilina, Gyrocotyle, Caryophyllceus, and Archi-
getes, the first three parasitizing fish, the last occurring in the
crelom of earthworms. In these, the body of the adult, at the
time when the genital products are being formed, is no longer
segmented into proglottids. The careful examination of these
types has recently resulted in their being regarded as more or
less c10sdy related to the Bothriocephalidre, but as reproducing
at the stage which in the latter family is larval. This is a case
of Ileoteny.
Amphilina is, a parasite in the intestine of sturgeons; investiga-
tion into the cycle of development has shown that there is an
intermediate host, a copepod, in which there becomes differen-
tiated a tailed larva corresponding to the procercoid larva of
Bothriocephalus. The sturgeon ingests the copepod together with
this larva which, in the fish's gut, develops into the sexually
mature Amphilina, corresponding to the plerocercoid stage of
Bothriocephalus. Thus sexual maturity is achieved in a larval
stage; that is to say, it is a case of neoteny.
Gyrocotyle is a parasite in the intestine of Chimara, a sela-
chian of the high seas, on which it is almost impossible to experi-
ment; thus the development of these Cestodaria remains un-
known but from their structure they appear to correspond
closely to the plerocercoid stage.
Caryophyllceus is a parasite of the Cyprinidre and accordingly
more accessible to embryological research. The structure of the
adult relates them rather closely to the plerocercoid stages of
Bothriocephalus. Now, they pass through a procercoid stage,
found in the crelom of earthworms; they then have a long tail
and the gonads are already beginning to differentiate. Develop-
ment is completed when the earthworm is swallowed by a
carp and the Caryophyllaus becomes sexually mature in this
phase which corresponds to the plerocercoid. Here again, it is a
case of neoteny.
There remains Archigetes. This animal is also found in the
crelom of earthworms and resembles a stage of a procercoid
larva; it has a tail bearing at its tip the hooks of the first larval
form. But here sexual maturity is attained at this stage. It is thus
a much more pronounced case of neoteny than the preceding
examples; nothing is known suggesting that Archigetes might
achieve further development in a second host.
 CESTODARIA 133

.. ·.· c t
v

Ii
o

I
d
v
t
-
-

P
Ii

Figure 52. A-C, Caryophylkeus latjeeps, a parasite in the gut of

the carp (after Fuhrmann). _
A, adult (4 cm. long); B, posterior extremity further enlarged; C, plero-
cercoid larva, parasite in the general body cavity of Tubi/ex tubi/ex
(rudimentary genital organs at the posterior end of the body);
D, Archigetes appendiculatus, parasite in the general body cavity of
Tubi/ex tubi/ex (after Mrazek): d, vas deferens; 0, ovary; p, penis;
t, testis; u, uterus; v, yolk glands.
134 pARASITES WHICH CHANGE THEIR HOST
A question presents itself in connection with these various
Cestodaria: is their development, which we have just sum~
marized, a matter of secondary regression through the loss of
the cestode adult, or does it, in the general development of the
group, represent a primitive stage, antecedent to the differen~
tiation of the typical form1: of true cestodes? It is impossible to
reply categorically to this question. It is nevertheless probable
that at least in Archigetes we are witnessing a secondary state
resulting from the loss of development of more advanced stages
and the neotenic acquisition of sexual maturity in the first inter~
meoiate hust.
I have briefly given these details here to show the diversity of
facts in a given group and the general interest of the problems
raised. As well as in the Bothriocephalidre, one may see in other
typical cestodes modifications of the usual conditions of develop-
ment, consisting of the suppression, by secondary adaptation,
of the intermediate host, and direct development in the definitive
host. This was established by Grassi and Rovelli 153 for a tape~
worm (Hymenolepis fraterna = H. murina) in rodents; and by
Calandruccio for Hymenolepis nana in man. The hexacanth
embryos change within the lumen of the intestine into cysti~
cercoids which do not acquire the vesicular structure of a cysti-
cercus but attach themselves to the intestinal wall' and develop
directly into adult tapeworms.
The experimental study of the developmental cycle of cestodes
still suggests great numbers of special problems that need
elucidation. We have precise knowledge of only a relatively
small proportion of existing species. It is a vast chapter of
zoology which cannot here be dealt with in detail but only in its
general aspects.
TREMATODA
We find, in general, two distinct categories in the develop-
mental cycle of trematodes. Those that are ectoparasites com-
plete their whole development on a single host; they are termed
monogenetic. On the other hand, those that .are endoparasites
undertake, in the course of development, migrations to two or
even three successive hosts, these migrations being accom-
panied by reproductive processes; they are termed digenetic.
Since the present chapter is devoted to heteroxenous parasites
 MONOGENETIC TREMATODES 135
it must be restricted to the second category. Nevertheless, I shall
first mention, by way of parenthesis, the very interesting par-
ticulars of development in Polystomum integerrimum, a mono-
genetic trematode parasitic in the bladder of frogs. It is possible
that analogous cases will be found later.
MONOGENETIC TREMATODES. The case of Polystomum
integerrimum. The monogenetic trematodes constitute an exten-
sive group comprising numerous forms that are parasites on the
external surface of aquatic animals of different groups, either
on the skin or on the gills. They only reproduce sexually. In the
family Polystomidre, certain species, amongst them Polystomum
integerrimum, are parasites in the bladder of amphibia or rep-
tiles. In P. integerrimum, Zeller 177, 178 showed that there is
developmental dimorphism. He observed that as a rule the
larvre attach themselves to the gills of frog tadpoles, leaving
them at the metamorphosis of the host, and migrating via the
gut to the bladder. In this their development parallels that of
the frog, sexual maturity being achieved only after a period of
three years. But, on the other hand, certain larvre grow very
rapidly on the gills of the tadpole, their rudimentary gonads
develop, eggs are laid and a new generation of larvre is produced.
This is a case' of neoteny.
This cycle of development has been methodically and pre-
cisely re-investigated by Gallien 150. I shall restrict myself here
to recalling the essential results of his experiments. He showed
that the two types of development depended on the age of the
tadpoles carrying the larvre. On tadpoles less than eight days
old and still provided with external gills, they all developed
rapidly as neotenic individuals which laid eggs after thirty days.
If attachment occurred on tadpoles between eight and thirteen
days old both types of development resulted, that is, neotenic
and normal, the latter with migration into the bladder and
sexual maturity only in the third year. On tadpoles more than
thirteen days old there was only retarded development with
migration to the bladder and reproduction at three years. The
fate of a larva, then, depends essentially on the type of nutrition
in the tadpole, and on the effect of hormones, with a threshold
of change existing between the eighth and thirteenth day of the
tadpole's life. Experiments have clearly shown that the par-
ticular constitution of the different larvre does not intervene, but
136 PARASITES WHICH CHANGE THEIR HOST
that the result depends exclusively on the age of the tadpole.
From Polystomum eggs of the same batch one can produce
either type of development at will. On the other hand, Polysto-
mum larvre produced by the neotenic generation, even when
fixed on tadpoles less than eight days old, always undergo the
retarded type of development. Neoteny cannot be repeated in
successive generations. Here is a fact of great interest for general
biology. Perhaps it will be found with other variations in related
types parasitizing other amphibia and reptiles. Perhaps also
processes of this kind are involved in naturally neotenic forms
like Archigetes.
DIGENETIC TREMATODES. Although the cycle in trema-
todes has been the subject of very numerous researches, it is only
well known in a limited number of species. Broadly speaking, it
follows fairly regular lines, and I shall briefly review its essen-
tial aspects. The larva, on leaving the egg, first of all pene-
trates into an intermediate host, a mollusc, in which the animal
passes through the stages of sporocyst, redia and cercaria. The
classical case and the first to be elucidated is that of Distomum
(=Fasciola) hepaticum, the large liver-fluke of sheep; the
numerous eggs are evacuated with the freces of the sheep and
df!velop slowly (in two to three weeks at 25°, and very much
more slowly at low temperatures), giving rise to a ciliated
larva, the miracidium, which emerges in water and swims about
freely for a time until it meets a small pulmonate snail, Limncea
truncatula. It is only within this species, at least in Europe,
that its further development can be completed; in Limncea
stagnalis it begins but does not go far. * The miracidium
settles in the pulmonary sac of the snail and there metamor-
phoses into a sporocyst, in the interior of which redire are
formed. These migrate to the liver and immediately give rise
either to cercarire or to a fresh generation of redire. The ripe
cercarire leave the snail, swim about for a few hours and then
settle on a blade of grass where they encyst. When the cyst is
swallowed by a herbivore such as a sheep, it breaks down in the
• Quite recently, S. B. Kendall (Nature, 163,1949, p. 880) succeeded in infesting
newly hatched Limntea stagnalis with miracidia of D. hepaticum (13 Limnfea were
infested out of 101 that were used in the experiment), but he was unsuccessful in
infesting adult Limnfea. This result is not, however, of importance from a prac-
tical veterinary point of view, on account of the entirely aquatic habitat of
Limnfta stagnalis.
 DIGENETIC TREMATODES 137
stomach and the young Distomum, set at liberty, gains the bile
ducts where it reaches maturity. These data are classical and
text-books of zoology and parasitology should be referred to for
details. *
Cycles of this kind involve the loss of a considerable number
of organisms, a loss compensated by extreme fecundity. Here is
a typical example:
E. Meyerhof and M. Rothschild 166 report an individual
Littorina littorea infested with Cryptocotyle lingua, and kept in
captivity in the laboratory for five years; it emitted about
1,300,000 cercarire per annum. Now, in certain localities it has
been found that the proportional parasitism of gastropods was
as much as 40 per cent. One sees what an enormous number of
cercarire is implied.
The complete life cycle is known for only a limited number

Figure 53. Miracidium of Parorchis avitus (parasite of the gull

Larus argentatus) on hatching, with a young redia (after Linton).

of species. Some of them are summarized for the sake of

reference in a table (p. 138). In some very common forms, such
as Distomum lanceolatum (the smallliver-fiuke of sheep), the
intermediate host has not yet been determined. Likewise many
sporocysts and cercarire are known, but not their adult forms.
The redia stage is sometimes suppressed. This happens in
Distomum macrostomum, a parasite of birds (woodpeckers, etc.),
whose very remarkable sporocyst, the so-called Leucochloridium
paradoxum, lives in Succinea putris. It branches into ducts, one
of which distends the tentacles of the mollusc and there hyper-
trophies into a large tube that pulses in sunlight and is brightly
• Another distome, living in the bile ducts of various mammals, both wild and
domesticated, and commonly in man in the Far East, is Clonorchis sinensis. The
miracidium develops in different species of Bithynia and Melania. The second
intermediate host is a cypnnid fish, particularly the common goldfish, Carassius
allratlls.
138 PARASITES WHICH CHANGE THEIR HOST

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 BILHARZIOSIS 139
coloured. This peculiarity attracts the attention of birds, which
go for the parasitized Succinea, devour them and become
infested. In these sporocysts there is direct development of
cercarire.
Many species of cercarire, instead of encysting externally
as in Distomwn hepaticum, penetrate into a second intermediate
host' where they encyst in the general body cavity and wait
there until this host is ingested by the definitive one. The animal
at this stage of the cycle is termed a metacercaria: metacercarire
are very widely distributed, particularly in the polychretes; the
lugworm, Arenicola, for instance, very commonly contains
one belonging to the genus Echinostomum (characterized by a
series of hooks arranged like a cape) and these cysts in their
turn are covered by a thick mantle of phagocytes from the
annelid. Many of these metacercarire are doomed individuals
which will never reach maturity for lack of being swallowed by
the final host.
In an account by P. Mathias 165 there is a good experimental
study of this cycle in three species of trematodes which are para-
sites of birds (especially of ducks): Strigea tarda (fam. Holo-
stomidre), Hypoderceum conoideum (fam. Echinostomidre) and
Psilotrema spiculigera (fam. Psilostomidre).
It is only in comparatively recent decades that we have under-
stood the cycle of two trematodes that cause severe illness in
man; these cycles are interesting on account of the way in which
they differ from the general run of such life histories.
One of these dis tomes causes a disease, bilharziosis, that is
widespread in warmer countries. It was Dr. Bilharz, in Egypt,
who recognized that it is due to a trematode (Schistosoma
(=Bilharzia) hcematobium) living in the venous system. The
Schistosomidre have the curious characteristic, found nowhere
else in the trematodes, of being unisexual, the male regularly
carrying the young female in a ventral groove. The way in which
infestation with this parasite occurs long remained unknown.
It was noticed that infection was most common in men working
in water, such as the workers in rice fields. Looss, guided by his
researches on Ancylostomum, concluded that the miracidium
penetrated directly into the skin when in water. In 1913,
in Japan, Miyairi and Susuki 167 discovered the life history of
these trematodes; it is in reality closely parallel to that of
140 PARASITES WHICH CHANGE THEIR HOST
Distomum hepaticum. The results of the Japanese authors were
rapidly confirmed by Leiper 161 in Egypt, by Iturbe and Gon-
zalez 157 in Venezuela, and by Lutz 164 in Brazil.
The eggs that pass out with either the urine or fa:ces (depend-
ing on the species) contain a ciliated miracidium which hatches
when the egg reaches pure water. It then penetrates into an inter-
mediate host, Planorbis, Bullinus or Physa: the favourite place
of entry is through the tentacles of the mollusc. The miracidium
develops into a sporocyst within the tentacle which swells up.

Figure 54. Schistosoma hamatobium (after Looss).

After about twenty days the primary sporocysts, now mature,

burst in situ, emitting numerous undifferentiated cellular masses,
which will, in the different viscera (liver, gonads) of the water
snail, develop into secondary sporocysts where there will
differentiate very large numbers of cercaria: with forked tails.
Under the influence of warmth and bright sunlight these cerca-
ria: leave the snail. They come to the surface ,of the water
and float there, hanging by the tail. Man becomes infested
either by their coming into contact with his skin when he is
bathing, or when he drmks contaminated water. The cercaria:
 BILHARZIOSIS 141
accordingly penetrate either the skin, or the mucous membrane
of the mouth or resophagus. Penetration takes place rapidly, in
a matter of some twelve minutes. Experimental infection has
been achieved with rodents. We now know a whole series of
Schistosomidre which cause serious infection in man or domestic
mammals. Let us quote only the following:
Schistosoma hcematobium, causative agent of vesical bil-
harziosis, characterized by hrematuria, very common in hot
countries (particularly Egypt). The intermediate molluscan host
is Bullinus ;
Schistosoma mansoni, causing intestinal bilharziosis (South

Figure 55. Development of Schistosoma (=Bilharzia) mansoni

(after Lutz).
1, normal egg containing the ciliated embryo; 2, infested tentacle (swollen)
of Planorbis olivacells; 3, normal tentacle; 4, secondary sporocyst;
5, the same at a later stage of development; 6, cercaria with forked
tail.

America, Antilles, Mrica) and also splenomegaly (particularly

in Egypt); the intermediate hosts are species of Planorbis;
Schistosoma japonicus, the subject of the researches carried
out by the Japanese workers Miyairi and Susuki 167, who
thereby established a method for the experimental study of
bilharzia diseases. The worm infests various domestic and wild
animals. The host in which the cercaria develops is Oncome-
lania nosophora. The disease it causes is termed arterio-venous
bilharziosis, which is common in China and Japan;
142 PARASITES WHICH CHANGE THEIR HOST
Schistosoma bovis, a parasite of cattle and various mammals
in the eastern Mediterranean region; the intermediate host is
Bullinus.
The other parasite of man to be mentioned here passes
through a metacercarial phase in a second intermediate host;
it is Paragonimus westermanni which, in the Far East, causes a
serious illness, pulmonary distomatosis. The adult trematode,
localized in the lungs, causes severe hremoptysis. The miracidium
develops in several species of Melania. The cercarire penetrate
various fresh~ater crabs and encyst there; man becomes
infested by swallowing the encysted metacercarire which are
found in these crabs (Potamon obtusipes, Sesarma de haani,
Q
Eriocheir japonicus), one hundred per cent. of them sometimes
being infected. The crabs are the second intermediate host of
the trematode, the first being Melania.

NEMATODA
A certain number of the parasites in this group are also
heteroxenous. Spiroptera obtusa of the mouse begins its develop-
ment in the larvre of the flour beetle, Tenebrio molitor. The
Acuariidre are, as a rule, first parasites of coprophagous insects,
and secQndly of mammals. Spirocerca sanguinolenta and Physo-
cephalus sexalatus thus have as successive hosts Ateuchus sacer
and the dog or jackal.
Ollulanus of the cat lives as a larva in the mouse; Cucullanus
elegans, of the perch has for the first host either Cyclops or a
larva of Agrion; an Ichthyonema of Uranoscopus is, in the first
place, a parasite of Sagitta.
Trichina (=Trichinella) spiralis encysts in the muscles of
mammals (pig, wild boar, rat, etc.) and can remain alive without
developing for several years. When the infected meat is eaten by
man or other lllammal the trichinas are set free in the stomach,
become mature, copulate in the small intestine, and lay their
eggs there. Their larvre break through the intestinal wall and are
then carried in the circulation; finally they encyst in the muscles
of the new host. .
Filarial worms perform complicated migrations which are
only partly known. The guinea worm, Filaria medinensis, which
lives in the subcutaneous tissues of man and may be up to a
 NEMATODA 143
metre in length, with a diameter of one to two millimetres, has
for its intermediate host a copepod, Cyclops coronatus, dis-
covered by Fedzchenko. It enters by the mouth and alimentary
canal and from there passes into the general body cavity
(Roubaud 202). Man becomes infected through swallowing these
crustaceans, but it is necessary for the worm to have undergone
rather a long process of development in them. qperimental
infection of monkeys has been obtained.
A whole series of filarial worms which, as adults, live in the
deeper organs, particularly the lymphatic vessels, and whose
embryos (microfilaria) enclosed in a sheath circulate in the
blood, have an analogous cycle. Such are Filaria bancrofti
( =nocturna) with larvre that circulate during the night and cause
serious illnesses, F. loa (=diurna), F. pertans, F. volvulus, etc.
Of the filarial worms in man, the only one with a completely
known life history is F. bancrofti, discovered in 1877 by
P. Manson.* The intermediate host is a mosquito, Culex
fatigans, that swallows the microfilaria in the blood. In the
stomach of the mosquito these microfilaria divest themselves of
their sheath, pass into the general body cavity and to the muscles
and there undergo a phase of development lasting about a fort-
night, by which time their organs have developed. t They then
migrate into different parts of the mosquito's body and come to
accumulate in the labium. At the moment when the mosquito
bites they are deposited on the skin, through which they quickly
pass without having to make use of the bite, since they can pene-
trate healthy skin.t
Today we know a certain number of parasitic nematodes,
belonging to the family Filariidre, which cause more or less
serious illnesses in man and are transmitted in similar ways.
Here I shall cite only the following: Onchocerca volvulu~, trans-
mitted by the bite of simuliids, and Filaria loa (loa-loa), trans-
mitted by a tabanid, Chrysops.
'" This discovery, apart from its own particular interest, has that of having been
the pomt of departure for the researches which ultimately led to our knowledge
of the cycle of the malaria parasite. Historically, it is the origin of the whole
frUItful series of researches into the illnesses caused by parasites in the blood.
t Culex fatigans is practically the most important vector of Filaria banero/li,
but many other species are capable of carrying it. Brumpt (2, 5th ed. p. 967), in
this connection gives a table containing 30 different species.
t Filaria banero/ti is the cause of many serious pathological conditIOns in man,
especially elephantiasis.
144 PARASITES WHICH CHANGE THEIR HOST

Filaria immitis in the heart of the dog is also transmitted by

culicids; the mechanism is the same as with F. bancrofti, except
that the young worms complete their development in the mal-
pighian tubes of the mosquito. F. grassi, also in the dog, is
transmitted by a tick, Rhipicephalus. Other examples could be
added to these.
GORDIAN WORMS. These aberrant nematodes also under-
take complex migrations, involving as a rule two successive
hosts. We have already had occasion to summarize the essentials
of their life history in connection with the facts of protelean
parasitism.
ACANTHOCEPHALA
These, when adult, are parasites in the intestine of vertebrates,
to which they are fastened by a proboscis provided with numer-
ous rows of hooks. There is no trace of an alimentary canal.
The larval stage is passed in an intermediate host which varies
according to the species: either a crustacean (Asellus, Gamma-
rus, etc.), an insect (Blaps, Cetonia), or a fish.
Such a cycle with an intermediate invertebrate host occurs in
Acanthocephala parasitizing fish or amphibia. But with those
that in the adult state infest birds or terrestrial and aquatic (Pinni-
pedia and Cetacea) mammals, one must allow that there are in
fact two successive intermediate hosts, the first being, as usual,
an arthropod and the second a fish, an amphibian or even a
reptile (snake), which is finally eaten by birds or mammals.
I restrict myself to this general statement without entering into
details of particular cases.

PENTASTOMIDA
These vermiform animals (also known as Linguatulida or
Porocephala) live as parasites in the respiratory passages of
mammals (particularly carnivores) and snakes. Thus Linguatula
serrata is found in the nasal fossre of the dog, and Porocephalus
armillatus in the tracheal artery and lung of large snakes. The
affinities of this group are very obscure. For a long time they
were associated with the arachnid~. Heymons, after extensive
investigation, * contented himself with assigning to them a place
'" In Kiikenthal-Krumbach, Handbuch der Zo%gie, III, 1, 1927, p. 128.
 PROTOZOA 145
between the annelids and the arthropods, in the vicinity of
groups such as the tardigrades and the Onychophora.
They are heteroxenous parasites. The eggs, which are very
numerous, make their exit with the nasal secretions of the host
and contamination takes place on the soil where the eggs are
lying. This is how the many animals are infected that constitute
the intermediate hosts: rabbits, hares, rats, cattle, etc., and also
man (particularly in Africa, with the eggs of Porocephalus
armillatus). The ingested larv<e pass from the gut of that host
into other organs and finally encyst. The parasite becomes adult
when the intermediate host is eaten, either by a carnivorous
mammal (in the case of Linguatula serrata) or by a snake (in the
case of Porocephalus). There it passes via the gut to the respi-
ratory tracts, where growth is completed.

PROTOZOA
Migration with a passage through an intermediate host is no
less widespread in the parasitic Protozoa than in the Metazoa,
particularly in the Sporozoa and Flagellata.
In the gregarines, Leger and Duboscq 103 have shown con-
clusively that the ccelomic gregarines of Crustacea, forming the
genus Aggregata, are no other than the schizogonic members of
a cycle in which sporogony takes place in cephalopods, there
developing into the forms known as Klossia or Eucoccidium,
hitherto considered as Coccidia. In causing the ingestion by
Portunus or Inachus of the sporozoites of Eucoccidium eberthi
from the cuttlefish they induced an intense infestation of Aggre-
gata in the crabs, and were able to follow out all the stages.
The same applies to the intestinal gregarines known as Poro-
spora in decapod Crustacea (lobsters and crabs); their sporo-
zoites are naked and represent only an asexual part of the cycle,
the sexual stages occurring in' bivalve molluscs (Tapes, Solen,
Tellina, Mytilus, Cardium and Donax), where the gregarines live
as parasites described under the name of Nematopsis. In bringing
about the ingestion of Nematopsis by Portunus, Leger and
Duboscq 104, 105 obtained the whole development ofPorospora
(cf. Fig. 56).
These researches of Leger and Duboscq have been extended
by those of P. Hatt 92 on the cycles of Porospora gigantea in
146 PARASITES WHICH CHANGE THEIR HOST
the lobster, and of a corresponding gregarine occurring in a crab,
Eriphia spinifrons, and in various molluscs. Hatt was able to
bring about the infection of Trochocochlea mutabiliswith gymno-
spores of Porospora from the lobster, and that of the mussel,
Mytilus edulis, with Porospora (formerly known as Nematopsis
legeri at this stage) from Eriphia; he then traced the steps of
development in this second host. He described in detail the
penetration of the gymnospores into the gill lamellre of the
mollusc and followed their changes through to the nematopsis

I..
f·

e-
Figure 56. Cycle of Porospora portunidarum (after Leger and
Duboscq).
a, nematopsis stage (in the gills of Cardium edule); b, sporozoite from a
nematopsis just after hatching in the alimentary canal of PorlU1ius
depuralor; c-e, sporozoites attached to the intestinal cells and
developing into sporadins.

stages, and finally succeeded in infecting Crustacea (lobsters

or crabs). This cycle, at the beginning of parasitic life in the
mollusc, includes a phase in which the elements of the gymno-
spores appear in the shape of pairs of minute spheres that Hatt
interprets, not without some reserve, as the pairing of two
bodies equivalent to gametes. The resulting zygotes are said to
become the sporozoites which produce infestation in Crustacea.
It is particularly in the Hremosporidia and the Hremoflagel-
lata that migrations assume paramount importance on account
 PROTOZOA 147
of the pathogenic role of many of these parasites. The study of
these migrations was one of the principal subjects of zoological
research at the beginning of the twentieth century. In general,
amongst the vertebrates, the Hremosporidia multiply asexually
(schizogony) and differentiate into sexual elements (gameto-
cytes) but without the formation of true gametes being achieved.
Such a development only occurs when the gametocytes leave
the blood vessel of the vertebrate. On microscopic examina-
tion of the blood of infected birds or mammals, one sees, after
a few moments, male gametocytes rapidly emitting some
long filaments, which are none other than the micro gametes;
for a long time these were taken to be degenerating forms. It was
at Constantine (Algeria) that A. Laveran first watched under
the microscope the formation of these filaments in the blood
of a malarial sufferer, and he saw that the parasite caused the
illness. It was only in 1897 that McCallum 106, working with
Hermoproteus columber from the pigeon, saw under the micro-
scope these filaments fertilizing the female gametes. Under
natural conditions this development of the gametes and their
pairing is only accomplished in the stomaCh of a biting insect-
mosquito, leech, tick, etc. In this new host the second part of the
cycle is achieved, leading to great numbers of organisms which
are inoculated into vertebrates when they are bitten by the
invertebrate host.
Ronald ROSS115, in 1898, first made known all the com-
ponents of this cycle; he was working with Proteosoma, a bird
parasite, with gamogony in Culex. Shortly afterwards the
researches of Grassi 91 and his pupils exactly reconstituted it
for the closely related parasite, Plasmodium, which causes
human malaria; here the second host is another culicid genus,
Anopheles.
Let us rapidly recapitulate the facts concerning Plasmodium,
which today are classical. The parasites multiply by schizogony
in the red blood corpuscles of man (rosette forms) and there
elaborate" melanin" pigment. After a certain number of genera-
tions of this kind they produce elements of a special nature
(crescents), which are the gametocytes and do not develop
further in the human blood stream; if, however, they are ingested
by an Anopheles sucking blood, they no sooner reach the stomach
of the mosquito than the female gametocytes, or macrogametes,
148 PARASITES WHICH CHANGE THEIR HOST
round up; and the male gametocytes give rise to the fila-
ments or micro gametes (seen by Laveran), which will fertilize
the macrogametes. The resulting zygote (ookinete) is vermiform
and mobile; it breaks through the stomach wall of the mosquito
and encysts (oocyst), causing a hernia on the external wall of
the stomach, which juts into the general body cavity. Within
these oocysts there differentiate immense numbers of filiform
mobile sporozoites, which spread throughout the body of the
mosquito and· invade the salivary glands. They will be inocu-
lated into man when the mosquito bites him. The mechanism of
transmission is clearly somewhat similar to that of Filaria ban-
crofti. Enormous numbers of papers on the Plasmodium cycle
have been published. There is no question of going into the
details of the subject here. Very recently the cycle has been
elucidated in the initial phase of the infestation of the mammalian
host, following on the bite of the mosquito. Infection of this
host is not betrayed by fever until several days have elapsed. It
was recognized by H. E. Shortt and his colleagues 122 that this
latent period corresponds to a first phase of schizogonic
multiplication taking place in the liver. It is after this that
Plasmodium passes into the blood and fever ensues. Fig. 57
shows the whole cycle as known today.
Hamoproteus columba of the pigeon is transmitted by a pupi-
parous "fly, Lynchia maura, which lives on the pigeon, but in this
case the part of the cycle which is accomplished in the inverte-
brate is reduced to the pairing of the gametes; the ookinete does
not leave the stomach of the insect and is inoculated into the
pigeon without having developed. This cycle has been stuoied
in particular by Ed. and Et. Sergent 121 • Hremoproteus nocture of
the little owl is, according to Schaudinn 119, transmitted by
Culex. *
The hremogregarines that are principally found in the blood
of cold-blooded vertebrates have an analogous cycle. The inver-
tebrate host is generally one of the Hirudinea (for Hremogrega-
rinre) or an acarine (Lyponyssus saurarum for Karyolysus
lacertarum). Hepatozoon perniciosum of the rat has for its
invertebrate host an acarine, Lelaps echidninus, a parasite on
• The researches of Schaudinn (1904) on this last parasite achieved fame
because this author was led to suppose that the Hremosporidia, the Hremo-
fiagellata and spirochretes were all identical. But his conclusions must have been
based on a misunderstanding of mixed infections and are no longer valid.
 VECTORS OF PROTOZOA 149
the rat; Leucocytozoon canis has the tick, Rhipicephalus
sanguineus.
The Hremoflagellata are transmitted in much the same way as
the Hremosporidia and the study of the factors involved is now
a matter of exceptional importance on account of the patho-
genic forms; moreover, it is highly complex. Today, one may

Figure 57. Developmental cycle of Plasmodium cynomolgi (after

H. E. Shortt).
A, phase in the lIver, and B, phase in the blood of the mammal host
(schizogony). C, phase in the mosquito (sporogony): 1-9, schizogonic
cycle in the hepatic cells; 10-20, schizogonic cycle in the red corpuscles
in the blood; 21-22, microgametes; 23-24, macrogametes; 25-30,
their development and conjugation in the stomach, e, of the mosquito;
31-34, oocysts and formation ofsporozoites; 35, their passage through
the salivary gland of the mosquito. -

consider it established that there are two categories of trans-

mission. In one of them the invertebrate vector truly deserves
the name of host because there is development of the flagellate
within it before reinoculation, and reinoculation is only possible
after this development has been completed; in the other, the
p.s.-6
 150 PARASITES WHICH CHANGE THEIR HOST

invertebrate is only a mechanical agent in passive transmission.

In the first case the organisms transmitted are specific; in the
second case there is no such limitation.
The invertebrates that transmit the hremoflagellates are natur-
ally bloodsucking species, primarily the biting insects, either
Diptera (flies, Glossina, Stomoxys, Tabanidre, Simulium, Phlebo-
tomus and mosquitoes) or fleas, lice and Hemiptera, and
secondarily the ticks and leeches.
Species of Glossina, the tsetse flies, are the vectors of trypano-
somes which are of the first importance on account of their
pathogenic nature; in the first place, there are Trypanosoma
brucei causing nagana and T. gambiense causing sleeping sick-
ness, and then there are other species such as T. cazalboui
causing souma, and T. pecaudi, etc. The part played by Glossina
was first shown by Bruce in 1894; in exact experiments on
nagana he showed that the transmitting agent was Glossina
morsitans and that big game in Africa acted as a reservoir of the
causative agent. Trypanosoma gambiense, the cause of sleeping
sickness, is principally transmitted by G. pa/palis; but in certain
I regions (Rhodesia) there is another trypanosome, T. rhodiense,
infecting man, transmitted by G. morsitans. T. cazalboui is
transmitted by different species of Glossina. In all these cases
Glossina is the true host in which some development occurs, its
degree varying according to the species. Some authors main-
tain that this development takes place exclusively in the pro-
boscis, others that it is completed in the stomach, whence,
after some delay, the trypanosomes pass either to the prob.oscis,
or else to the salivary glands (this would be the case with try-
panosomes of man). The details of this development are still not
clear. Koch observed a dimorphism which suggested gameto-
cytes to him, but the reality of the phenomenon of sexuality has
not yet been demonstrated.
Trypanosoma lewisi, a non-pathogenic form in the rat, simi-
larly completes its life cycle in a flea, Ceratopsyllusfasciatus, and
perhaps in a louse, Htematopinus spinulosus. T. theileri, in cattle
in the Transvaal, is said to be transmitted by a hippoboscid.
Schizotrypanum cruzi, causing South American trypanosomiasis
in man, has for its intermediate host bloodsucking Hemiptera
of the family Reduviidre (Triatoma, Rhodnius, etc.), with
development analogous to that found in species of Glossina.
 VECTORS OF PROTOZOA 151
Wild animals such as armadillos act as reservoirs of the
organisms.
Trypanosomes of aquatic vertebrates are transmitted through
the agency of leeches (Trypanosoma granulosum of the eel by
Hemiclepsis, T. rajee by Pontobdella, T. inopinatum of the frog
by Helobdella, etc.), as was shown by the researches of Leger
and Brumpt. But with other trypanosomiases invertebrates are
purely mechanical vectors. This is said to be the case with surra
(T. evansi), transmitted by Stomoxys and tabanids, and for
debab (T. berberum) of camels, also transmitted by tabanids.
Stomoxys also spreads the trypanosomiases for which Glossina
is the specific host, as was clearly shown by Bouffard in connec-
tion with souma (T. cazalboui). In the same way mosquitoes can
transmit this infection. Trypanosoma equiperdum, causative agent
of dourine in horses, is directly transmitted across the mucous
membranes at coition, thus differing from all other trypano-
somes. * But it has been possible to transmit it experimentally
by insects.
The leishmaniases (canine leishmania, kala azar in man,
Oriental sore, South American leishmania, etc.), also caused by
flagellates (Leishmania), are usually transmitted by Phlebotomus,
a biting fly belonging to the Psychodidre, a fact first recognized
by Ed. Sergent in Algeria for "clou de Biskra" and also
observed in connection with Oriental sore and most other leish-
maniases, particularly kala azar, the leishmaniasis of the spleen
in infants.t
The transmission of the piroplasmoses (or babesioses) is
effected by acarines, the ticks (Ixodidre), which are true hosts
in which the parasi.te completes its development, and even passes
in the eggs from one generation to another. Moreover, these
acarines transmit other types of disease.
The precise mechanisms of transmission of the different para-
sites are far from uniform and many are still debatable. There
* Koch, however, believes that certain facts of conjugal contagion show that
T. gambiense can be transmItted in the same way.
t Incidental to these data, I shall here relate a curious fact first pointed out by
A. Lafont m Mauritius 484: teemmg numbers of a flagellate, Leptomonas davidi,
caused an infection m the latex of one of the EuphorbIacea:: (Euphorblapilullfera).
It was a truly parasItic disease of the plant, a flagellosis. Out of 114 plants
examined,49 were mfected. Lafont 485 was able to produce experimental trans-
mIssion of the parasite through the bite of a hemIpterous msect, Nysius euphor-
bire, that frequently lives on the plant. ThIS fact is certainly not the only one of
its kind.
152 PARASITES WHICH CHANGE THEIR HOST

may be inoculation in the true sense, by a sucking invertebrate,

or deposition of the parasite on the skin, either in saliva or
excrement, and active or passive penetration, either through
healthy skin or through wounds.
A special question arises in connection with the migrations of
these parasitic Protozoa. With the Metazoa it is obvious that the
definitive or final host is that in which the parasite attains sexual
maturity., In the Protozoa the criterion is much less clear, the
phenomena of sexuality are often completed in stages in each
of two hosts, or are not known. We do not know for certain,
at least up to the present time, the sexual stages of trypano-
somes, and with the Hremosporidia the gametes are really
differentiated in the gametocyte stage in the blood of vertebrates,
but they only complete development and copulate in blood-
sucking invertebrates. Under these conditions, which is the
definitive or main host? Two theories exist. Certain biologists
such as Leger consider, for instance, that the trypanosomes were
originally intestinal parasites of non-biting insects, in the state
of Crithidia or Leptomonas, and that they were modified in biting
and blood-sucking insects, so becoming adapted to the internal
environment of vertebrates; Roubaud supports these ideas.
Minchin, on the contrary, considers the vertebrate to be the
fundamental host in which the trypanosomes were originally
parasites in the intestine and then later in the blood; finally,
they would have passed into blood-sucking insects. Mesnil
supports this last hypothesis on account of the occasions, by
now rather numerous, in which intestinal parasites have been
seen passing into the blood; these are distinct from pathological
cases.
For the Hremosporidia this second hypothesis seems the more
natural; they are derived from Coccidia which were originally
present in the intestine and later in the blood: there are some
types of true Coccidia which, from their situation and even in
their development, indicate the possibility of this transformation.
Their passage through the Culicidre would be a secondary com-
plication of the cycle. The vertebrates would then be the prin-
cipal hosts. The latter term, moreover, is more suitable here
than that of definitive (or provisional) host. If we admit Leger's
hypothesis for hremoflagellates, we see that the migrations, after
having arisen secondarily, can finally disappear as in the
 PARASITIC PLANTS 153
case of dourine, and this must be compared with the suppres-
sion of migration that we have seen in certain species of Hymeno-
lepis, where the tapeworm develops without an intermediate
host and where this type of development is evidently secondary.
Some plant parasites, like those of the animal kingdom, migrate
to successive hosts which are more or less indispensable for the
completion of their whole cycle. The classical example is that of
certain Uredinere the sporophyte of which (with uredospores
and teleutospores) lives on one host, and the gametophyte (with
recidiospores and spermogonia) on another. With Puccinia
gram in is, the rust of wheat, the first host is a cereal, particularly
wheat; the gametophyte, on the contrary, lives on barberry.
 CHAPTER VIII

ADAPTIVE MODIFICATIONS IN THE

REPRODUCTION OF PARASITES

THE examp~es studied in the preceding chapters show how para-

sitism modifies all the organ systems; the reproductive apparatus
is one of those wlllch are most constantly and profoundly
affected. The reproductive function in most parasites undergoes
considerable hypertrophy; to the usual processes of repro-
duction others are frequently added which result in increasing
them. Without introducing any finalist view one may say
that, in fact, reproduction is the goal of' all the functions of
the organism; but, in free-living forms, the activity of the indi-
vidual is to a large extent exercised independently of reproduc-
tion and in the higher animals it even survives it. In parasites, on
the other hand, this function preponderates and all else is
subordinate to it; nothing is retained, one may say, except in so
far as it helps reproduction.
The parasitic life limits the function of reproduction by tying
the parasite closely to the host and thus restricting the usual
possibilities for the meeting of the sexes. On the other hand, it
introduces a new condition into development, that of meeting
the necessary host at a definite time. From these two facts arise
the essential characteristics of reproduction in parasites ..

HERMAPHRODITISM AND CHANGE OF SEX

To the first of these two facts are related the most frequent
modifications of sexuality in parasites; these can be placed in
two principal categories: hermaphroditism and exaggerated
sexual dimorphism.
Hermaphroditism is a very widespread condition in parasites,
whether it existed already in ancestral free-living forms and is
therefore primitive, or whether it appeared secondarily and as
a result of parasitism.' Thus, one may consider as primitive her-
154
 HERMAPHRODITISM AND CHANGE OF SEX 155
maphroditism that of the trematodes and cestodes, the Rhizo-
cephala, even the Hirudinea (the oligochretes are already her-
maphrodite). But in most other groups hermaphroditism is
secondary, as one may see by comparing related forms. In the
Myzostomaria, which are certainly derived from the poly-
chretes, hermaphroditism must have been established or at least
reinforced (for it exists in a more or less rudimentary state in a
certain number of polychretes) by parasitism. Among the iso-
pods, which are essentially unisexual animals, the Cymo-
thoidre sho~ sex reversal, as do also the Cryptoniscidre amongst
the Epicaridre, and there it is obviously a secondary condition.
In the Orthonectidre, with separate and dimorphic sexes, her-
maphroditism is introduced as an equally secondary modifica-
tion (Rhopalura julini, and R. pelseneeri, Stcecharthrum giardi).
In the nematodes, which are normally unisexual, the parasitic
forms include a certain number of hermaphrodite types (Rhab-
donema nigrovenosum, Bradynema rigidum, Allantonema). In the
prosobranch gastropods, where unisexuality is the rule, para-
sitism, as we have seen in certain forms, involves hermaphro-
ditism, particularly in the most degenerate forms (Entoconchidre).
Hermaphroditism is, moreover; a simplification of reproduction
in parasites only if there is self-fertilization, and this is the case
in a certain number of groups such as the cestodes, the Rhizo-
cephala, hermaphrodite Orthonectidre, etc. But change of sex
leads to the utilization of all individuals for egg production and
therefore turns out to be an arrangement that favours the
species; it happens, besides, to converge with the second of the
two conditions referred to earlier, the exaggeration of sexual
dimorphism, to the extent that it has been and still is sometimes
difficult to decide which of the two arrangements one is dealing
with. The exaggeration of sexual dimorphism almost always
consists of gigantism in the female in comparison with the male.
The converse is a rare exception (Bilharzia). But in both cases
the sexes live together; generally then the dwarf male lives on
the female. Thus, the meeting of the sexes is aSsured. Moreover,
the permanent union of the sexes is to be seen even in parasites
that are but little modified and show only slight sexual dimor-
phism, notably in many Crustacea (Ichthyoxenus), even in simple
commensals or inquilines (see Ch. 1). It is the permanent union
of the sexes that is the truly characteristic and fundamental
156 MODIFICATIONS IN REPRODUCTION OF PARASITES

feature; but one may say that from this arise sexual dimorphism
and the dwarfing of the male. These phenomena occur, after all,
for the same reason, in organisms-that are simply sedentary.
One could compile long lists of parasites with intense sexual
dimorphism and with the sexes living in permanent association:
it is so with most of the Epicaridre (Bopyridre, Entoniscidre,
Dajidre), with almost all copepod parasites (excepting Xeno-
clEioma, which is hermaphrodite and self-fertilizing), with the
Ascothoracica, with most parasitic gastropods (Capulidre, Buli-
midre, Entocolax, Pcedophoropus), with different parasitic nema-
todes (e.g., Syngamus trachealis).
In the ,Cryptoniscidre and some of the Myzostomaria the
external aspect of both sexes is similar and precise investiga-
tions have been necessary to show that hermaphroditism really
exists. In the male phase the animal is dwarfed and lives on a
large female, a form into which it will change after having func-
tioned as a male. Practically, it is a dwarf male. Using abundant
material, which was carefully observed in vivo, I was myself able
to follow and make quite certain of the stages of transformation
in several types as the male changed into the female (in Hemio-
niscus, Danalia, Liriopsis, Ancyroniscus). In the special case of
the Myzostomaria all the transitional stages have been found,
from protandrous hermaphroditism, with the simultaneous pre-
sence of two unequally developed glands, to a true change of
sex, as Wheeler established 185, the males having been for a long
time regarded as special individuals, independent of the females. *
The truly characteristic change in sexuality in parasites is,
then, the permanent proximity of the sexes, ensuring fertiliza-
tion, either in unisexual states with a dwarf male living on the
female, or in hermaphroditism, involving a change of sex, as we
have just seen, or by the establishment of a condition allowing
of self-fertilization.
Here I shall mention a fact that is both very curious and unex-
pected in its connection with parasitism, as it occurs in animals
'" In certain parasites (Myzostomaria, Entoniscldre), as well as In some seden-
tary animals (cirripedes), complemental males, in addItion to hermaphrodite
indIviduals, have been described. In each case it is necessary to be sure that these
males will not finally develop into females: the existence of such dwarf males in
the Myzostomaria is not generally admitted nowadays. The existence of males
in the Entoniscidre, accepted by Giard and Bonnier, needs to be investigated
again. The cryptoniscan larvre, which they considered as such, are perhaps merely
young stages of ordinary males.
 PARASITIC MALES IN FISHES 157
that are perfectly free-the abyssal fishes of the family Cera-
tioidea (related to the angler, Lophius piscatorius). There is in
some of these animals a high degree of sexual dimorphism, the
male 'being a dwarf and living as a permanent parasite on the
female. In studying specimens of this family collected by the
Dana, Tate Regan 594 recognized that on some individual
females in three of the species collected (Photocorynus spiniceps,
Edriolynchus schmidti, Ceratius holbolli) there were dwarf males

Figure 58. Dwarf males parasitizing females in the Ceratioidea

(after C. Tate Regan).
A, Ceratias holbolli ~ with ~ attached to its ventral region. B, anatomy
of the male. C, Edriolynchus schmidti, ~ with ~ attached ventrally;
br, gills; e, stomach; mi, mandible; ms, maxilla; IE, resophagus;
p, attaching papilla formed by the tissues of the female; t, testis.

fixed by the mouth to the surface of the female. The contact is

intimate. A perfect continuity of the tissues of both partners,
and especially of their vascular systems, is established. The male
then feeds at the expense of the female. It is an unequivocal case
of parasitism and as complete as could be. Nevertheless, the male
has retained his gills and breathes independently. The achieve-
ment of this paradoxical association is evidently tied up with
the extreme unlikelihood that the sexes would meet if they lived
apart. The males must attach themselves to the females shortly
6*
158 MODIFICA TlONS IN REPRODUCTION OF PARASITES
after hatching from the egg; those that do not succeed in this
probably perish. It would obviously be of great interest to verify
this in living material, but that is practically impossible.

INCREASE IN EGG NUMBERS

The necessity of meeting the right host at the propitious
moment of development and, in forms undertaking migrations,
that of passing successively into different hosts, affects the para-
sites to an even greater degree than the need for ensuring fertili-
zation of the eggs. From these circumstances there arises an
enormous loss of eggs or embryos which, under the usual con-
ditions of reproduction, would rapidly bring about the disap-
pearance of the species. Parasitic forms have then only been able
to maintain themselves by arrangements that compensate for
this extreme degree of mortality in their young.
The simplest and the most widespread of these arrangements
is a considerable increase in the number of eggs produced.
Increase in fecundity is a very general characteristic in parasites
and to a large extent the hypertrophy of the female in com-
parison with the male is due to it. A clear idea of this increase in
fecundity is gained by comparing the contents of the brood
pouch of one of the Epicaridre-tremendously developed and
with the embryos to be counted by thousands-with that in a
normal isopod such as Sphceroma, where there will be scarcely a
hundred or two. Individuals of Sacculina, Lerncea, Xenocce/oma,
all constantly produce large batches of eggs: the egg strings of
parasitic copepods are much longer than those of normal forms.
Egg production in the parasitic nematodes is enormous . .It was
long ago calculated that Ascaris lumbricoides in man annually
produced 64 million eggs, representing 1,700 times its own
weight; a queen bee, which is considered to be endowed with
quite exceptional fertility, annually produces only thirteen times
her weight in eggs. In Sphcerularia bombi, a nematode parasite
of bumble bees, there is produced on the female herself an extro-
version of the uterus, forming an enormous sac to which the
body of the female remains attached as a minute appendage
(Fig. 59A-C); the sac contains a very large nU'mber of embryos.
The related genera Allantonema and Attractonema show similar
arrangements. The -trematodes and cestodes lay eggs con-
 ACCESSORY REPROD-VCTIVE PHASES 159
tinuously and those laid annually by Tania solium have been
estimated at 80 millions.
But an increase in the number of eggs is not the only means
of ensuring compensation for the great loss of larvre and em-
bryos. In a fairly large number of groups there is intercalated in

Figure 59. Spharu/aria bombi.

A, young female showing the uterus, v, beginning to extrovert (x 50).
B, a later stage; the body, s, of the female is very small in comparison
with the extroverted uterus (x 9). C, final stage; the body, s, of the
female is not more than a minute appendage on the uterus, v, in which
the embryos are developing (x 5) (after Leuckart).

the course of the individual's development a phase of repro-

duction depending either on parthenogenesis or on budding.
We shall review the principal examples of this.

ACCESSORY REPRODUCTIVE PHASES

PROTOZOA. In many parasitic types, and notably in the
Sporozoa (Coccidia, Hremosporidia, schizogregarines, etc.),
there is, during the initial phase of infestation of the host,
asexual reproduction leading to very large numbers of indi-
viduals. This is what is termed schizogony. It is a phase of intense
multiplication followed by the sexual phase, termed gamogony,
during which the transfer from one host to the other takes place.
The link between the two phases is far from obvious and cannot
be exactly determined except through experimental infestations.
 160 MODIFICATIONS IN REPRODUCTION OF PARASITES

We shall briefly recall a typical example, that of the Coccidia.

Gamogony was first described in the genus Coccidium, and
schizogony as occurring in a distinct genus, Eimeria. It is to
Schaudinn and Siedlecki 120 that the honour accrues of having
recognized that it was a question of one and the same parasite.
Irrefutable experimental proof was given later by Simond 126 on
Coccidia in the intestine of the rabbit; he induced newly born
rabbits to swallow spores of Coccidium in milk and thus
obtained Eimeria, which multiplied in the gut.
DICYEMIDA. These animals are known to swarm in the
kidney of cephalopods, which they must infest soon after the
latter leave the egg. In young cephalopods they exist as elon-
gated vermiform individuals called nematogens and seem to
mUltiply by entirely asexual means for several generations, as in
schizogony mentioned above. The germ cells of the axial cell
do not, in fact, show any trace of fertilization, nor of the emis-
sion of polar bodies and, indeed, seem to be agamonts, the
process being one of agamogony (equivalent to schizogony). In
the adult cephalopods, on the other hand, where the infection
. is long standing, one finds almost nothing but rhombogens,
which give birth in their axial cell to special individuals called
the infusoriforms, arising from germ cells detached from multi-
cellular clusters termed infusorigens; and these elements, as
Hartmann showed 138, arise from eggs which give off a polar
body and are fertilized. Production of the infusoriforms then
results from a sexual, process, a gamogony; the cells of the
infusorigens are gamonts. The significance of the infusoriforms
cannot be considered as definitely established. Hartmann,
depending principally on an observation of Keppen's, 'who
sketched spermatozoa in them, considers them to be males. But
if one accepts this interpretation the cycle would become even
more paradoxical, for fertilization would take place only for the
production of males. The certain existence of spermatogenesis
in these infusoriforms has still to be established. The other and
more probable interpretation is that the infusoriform is the
vector of the infectionfrom one cephalopod to another; this fits in
with the fact that it is resistant to the external medium, which is
not the case with the vermiform individuals. The observations
of Lameere 139 lend weight to this second interpretation. To
decide the question definitely fresh observations and experi-
 ACCESSOR Y REPRODUCTIVE PHASES 161
ments are needed, in which attempts could be made both to
follow the changes in the internal cells of the infusoriforms out-
side the cephalopods where they are formed, and to infect young
cephalopods as they leave the egg. Although no one has suc-
ceeded in this up to the present, it cannot be considered as an
impossible task. *
However this may be, the cycle in the Dicyemida allows of the
intercalation of a long period of agamogenetic multiplication.
ORTHONECTlDlE. The cycle of their development includes
a phase of asexual reproduction in the host. Let us consider the
case of Rhopalura ophiocomce, which is the best known. The
larvre arising from fertilized eggs penetrate into the genital aper-
tures of the ophiuroid Amphiura squamata. They give birth to
intracellular bodies with one or two nuclei, which become plas-
modia in which the nuclei multiply and where, at their expense,
germ cells differentiate and give rise to sexual individuals, male
or female. These plasmodia constitute a true agamogenesis, such
as that of the Dicyemida. Each larva which succeeds in gaining
a host gives birth in this host to very numerous individuals and
thus compensates for the loss of the larvre that are unsuccessful
(cf. Fig. 48, p. 114).
C<ELENTERATA. In this group asexual multiplication is very
general. Its existence in the parasitic forms is not then significant.
However, it is interesting to note that among the rare parasites
in the group there are several which show precocious asexual
reproduction. Such is the case with Polypodium hydriforme, a
parasite of the eggs of the sturgeon, in the midst of which it
forms tubes that develop as numerous buds, each one
becoming a hydroid polyp. Larval budding is also shown in the
parasitic Narcomedusre (Cunina, Cunoctantha, etc.): the planula
larva lives as a parasite in the manubrium and gastrovascular
system of other medusre of the family Geryonidre (Carma-
rina, etc.) and at a very precocious stage, scarcely more differen-
tiated than the planula, gives rise to a series of buds.
CESTODA. The tapeworm is often considered as a chain of
individuals resulting from strobilization. Each proglottis
,.. The recent researches of H. Nouvel 140 confirm the preceding conclusions
that the infusoriform is the vector between one cephalopod and another, and is
not a male. The so-called spermatozoa that have been reported (Keppen, Hart-
mann) must be the cilia of the cells that hmlt the anterior part of the internal cavity
of the infusoriform.
162 MO_qIFICATIONS IN REPRODUCTION OF PARASITES
encloses, indeed, the group of organs that could characterize an
individual, and is comparable with the group of lower cestodes
or Cestodaria (Amphilina, Gyrocotyle, Caryophyllceus, which are
fish parasites, and Archigetes, a parasite of Tubifex). The
new proglottids form in the initial region of the scolex, in the
vicinity of the zone of attachment to the host, usually called the
head of Tcenia. But the study either of Archigetes, or of the
cysticercoids of Hymenolepis and related types, shows, by the
position of the hooks springing from the hexacanth embryo,
that the point of attachment of tapeworms, and of cestodes in
general, is their posterior extremity and that it is on the latter
that the formation of new segments takes place in cestodes. The
interpretation that the segmentation of the body of Tcenia into
proglottids represents an increase in the number of individuals,
remains subject to these discussions which, at bottom, are more
verbal than real. In fact, from the point of view with which we
are concerned, strobilization presents itself as a highly efficient
process favouring the production of a very large number of eggs.
Above all, once the cestode has become established in its host
this production is continuous over a very long period, during
which the proglottids ripen and detach themselves one by one.*
Thus the whole of egg-laying is not subject to the hazard of a
single batch of embryos; this is an arrangement very well suited
to the conservation of the species and one that we shall find
again in the trematodes and in many nematodes.
But the cestodes have another method of reproduction inter-
calated in the development of the individual after it leaves the
egg. This occurs when the cysticercus;instead of producing only
one scolex, produces a series; from a single hexacanth larva
there is thus derived a number of tapeworms, more or less
perfect. This is accomplished in very various ways: in Tcenia
nilotica (of Cursorius europceus) multiple invaginations develop
in the wall of the cysticercus, known as polycercus, which lives
in lumbricids. The same occurs in the long-established classical
instance of T. ccenurus, the cysticercus of which is usually found
.. This process may be related to the schizogenesis of various oligochretes
(Lumbriculus, Chrelogaster, Nms, etc.) and partIcularly the schizogamy of the
syllids, especially of Autolytus and the Myrianidre, which physiologically corre-
sponds closely enough to proglottis formatIOn and also ensures prolonged dis-
semmatIOn of the genItal products. Giard grouped the facts of this kind under
the rather expressive name of reproductive autotomy.
 ACCESSORY REPRODUCTIVE PHASES 163
in the brain of sheep. The process reaches its culminating point
in T. echinococcus where, as we know, the cysticercus buds off
secondary cysts and sometimes even tertiary cysts, each of which
behaves like a crenurus and gives rise to several scolices. Here it
is possible for very large numbers to be produced and at the
same time to mUltiply in many different organs. A cysticercus
of Glomeris (=Staphylocystis), instead of budding off scolices
by invaginations, produces externally and in grape-like clusters
a series of secondary, vesicular cysts, each one of which develops
a scolex.
There is, moreover, a certain equilibrium between these repro-
ductive processes and the final development of the tapeworm.
In T. echinococcus, where multiplication of the scolices is very
vigorous, the tapeworm itself is very much reduced, possessing
only three or four proglottids: although these are continuously
renewed, egg production must be more restricted than in the
large tapeworms. On the other hand, Tania echinococcus is
gregarious in a high degree, as one might expect from the
development of its cysticercus.
TREMATODA. The endoparasitic trematodes which are
heteroxenous are at the same time digenetic and the reproduc-
tive phenomena occurring during their development are classical.
I shall not stress them here. These phenomena occur in the
sporocyst stage, when numerous redire become differentiated;
there may be several generations of them; the redire themselves
finally give rise to numerous cercarire.
It is necessary to look for the exact significance of the cells
from which the redire and cercarire develop. Is it a matter of
asexual, internal budding, or of larval parthenogenesis (pro-
genesis)? It is the latter interpretation which tends to be ~ccepted
today. In the sporocyst of Distomum duplicatum, a parasite of
Anodonta, Reuss 171 saw redire developing from a single cell;
this gave off a structure which he took to be a polar body, and
it would therefore be equivalent to an oocyte. The most exact
confirmation of this opinion is due to Cary 146, who studied
Diplodiscus subclavatus, parasitizing various amphibia. How-
ever, the drawings given by these workers are not altogether con-
vincing and in any case we are far from being able to find in most
forms the equivalent of what they described. R. Dollfus 148,
who could not succeed in confirming the data of Reuss and
164 MODIFICATIONS IN REPRODUCTION OF PARASITES

Cary, proposes that the internal cells of sporocysts and redire

should be considered as belonging to the linear succession of
germ cells in trematodes, which continue uninterrupted as far
as the cercaria: The formation of redire and cercarire is com-
pared by him to repeated polyembryony, that is to say, to a kind

IV
/11
/I

Figure 60. Gyrodactylus elegans (after Fuhrmann).

0, ovary (ootype); (l!, ovum; t, testis; v, posterior discs with hooks;
I-IV, four successive generations enclosed one within the other.

of budding. But it is the nature of germ plasm to develop, as

a prelude to a new generation, into oocytes and spermatocytes
showing the phenomena of reduction divisions. * In poly-
" The continuity of the germ plasm and the precocity of its evolution are shown
in a striking way In certain ectoparasitic trematodes, such as Gyrodactyius, which
hves on the gills of freshwater fishes and also some saltwater ones, in which one
may see four successive generations enclosed, one within the other (Fig. 60).
Lameere (Precis de Zooiogie, vol. 2, p. 248, 1925) interprets this as polyembryony.
It seems preferable to me to see in it a demonstration of the continuity of the
germ plasm through successive generations.
 ACCESSOR Y REPRODUCTIVE PHASI!S 165
embryony, which we are coming to, the facts are much more
naturally interpreted as corresponding to an asexual process;
that is to say, they have nothing to do with the germ plasm. In
reality the question demands further research.
RHIZOCEPHALA. We have seen already that in some of these
so highly modified parasites there occurs typical asexual repro-
duction, which is especially remarkable in the Crustacea. In
Thompsonia, instead of a single' 'nucleus" differentiating on the
root system, as in Sacculina, a considerable number form, which
fall off periodically and are regenerated. We shall not describe
the process again here. It is equivalent to the production of a
large number of scolices in the cysticercus of a crenurus or an
echinococcus. And here again we find the equilibrium that we
have pointed out in the cestodes. The organization of an indi-
vidual Thompsonia is simplified by comparison with that of
Sacculina. There are no longer nerve ganglia, a pallial cavity, nor
even testes, and there is only one batch of eggs, which must
develop parthenogenetically. * In Peltogaster socialis there is,
very probably, precocious fragmentation in the undifferentiated
internal phase. It is then a question of budding or, if one likes,
of polyembryony, and the process is not peculiar to this species,
since it has been found in a distinct form, Peltogasterella
socialis, in the Pacific. Asexual reproductive phenomena, then,
exist in the Rhizocephala with a certain variation in type, and
we probably do not yet know all the forms they take.
POLYEMBRYONY IN ENTOMOPHAGOUS HYMENOPTERA.
This process, which is so remarkable when one considers the
systematic position of the Hymenoptera, was discovered by
Marchal 302 in the Chalcidoidea and the Proctotrypoidea. It
was studied in detail by him in Encyrtus (=Ageniaspis) fusci-
collis, a parasite of the caterpillars of Hyponomeuta cognatellus,
H. mahalellus and H. padellus. The egg of this encyrtid is laid
in that of the butterfly during July and August; development
starts before the winter but comes to a complete stop, to be
resumed about April. The egg of the parasite is surrounded, as
soon as it begins to develop, with a wall of epithelium belonging
to the host. From the beginning a large nucleus is differentiated,
the paranucleus, very rich in chromatin, which will play a
vegetative and trophic role, and small nuclei which are not
... The larva: hatch directly in the cypris stage.
166 MODIFICATIONS IN REPRODUCTION OF PARASITES

easily stained (Fig. 6lA) and are the true embryonic nuclei. The
paranucleus undergoes very extensive development, becomes
lobed and divided into an infinite number of fragments, while
the embryonic larvre give rise at an early stage to small groups
of cells resembling morulre, each one of which becomes an
embryo (Fig. 6lB). About one hundred are formed in this way.
These embryos develop, like those of the Orthonectidre, in the
middle of a cytoplasmic mass strewn with fragments of the para-
nucleus containing fat. The paranucleus thus plays the part both
of the amnion and of a trophic layer. The whole of the primitive
egg is gradually transformed into a long tube in which the

Figure 61. Polyembryony in Encyrtusfuscicollis (after Marchal).

p, paranucleus; ne, embryonic nuclei; mD, moruliform mass giving rise to
various individuals; k, epithelial sheath of cyst produced by the host,
Hyponomeuta.

embryos are arranged. in line and which continues to be

enveloped in the epithelial cyst of the host. In short, differefu
tiation of the embryos is extremely precocious and is highly
reminiscent of the Orthonectidre and their plasmodia, or of
redire and cercarire in the sporocysts of trematodes.
Polyembryony is an exceptional phenomenon in the parasitic
Hymenoptera, but there must be, however, a fair number of
examples. Marchal found it in another encyrtid, Ageniaspis
testaceiceps, a parasite of the caterpillars of Lithocolletis, also
in a proctotrypoid, Polygnotus minutus, which develops in the
gastric sac of Cecidomyia destructor and of C. avena. In this .
Polygnotus each egg gives rise to about fifty embryos.
 ACCESSORY REPRODUCTIVE PHASES 167
Silvestri recognized polyembryony in Litomastix trunca-
tellus, * a parasite of the caterpillars of P/usia gamma, and here
a single egg produces about 1,000 larvre, without counting a
certain number of abortive ones, called by Silvestri asexual
larvre; these lack the rudiments of gonads and degenerate
without ever metamorphosing. t The details of the process
in Litomastix appear to be rather different from those in
Encyrtus.
Patterson 310 found and studied a certain number of cases of
polyembryony in chalcidoids related to Encyrtus: Litomastix
(= Copidosoma) gelechia, a parasite of Gnorimoschema sali-
naris; Paracopidosomopsis floridanus, a parasite of the cater-
pillar of the white cabbage butterfly, Pieris brassica; Platygaster
rubi, parasitizing the larvre of two Diptera living on conifers
(Sabina). In Paracopidosomopsis he again found the asexual
larvre of Silvestri, the existence of which was doubted by Wheeler,
and he proved, by rearing them in conditions which excluded
the possibility of contamination, that they could not be the
larvre of another ins~t parasite, such as an ichneumonid, which
Wheeler had suggested. t
More recently other cases of polyembryony have been
pointed out amongst the parasitic Hymenoptera, notably in the
Braconidre. H. L. Parker 308 has described it in Macrocentrus
gifuensis, a parasite of the caterpillar of the corn Pyralis;
Paillot 307 has found that it occurs in other species of Macro-
centrus, and in Amicroplus collaris parasitizing the caterpillars of
Euxoa segetum.

* Giard 296 had stated that it must be present in this species, at the time of
Marchal's discovery.
t This suggests that from the start these larva: do not contain the cell derived
from the lIne of germ cells, and It would follow, accordingly, that the initial
groups of cells normally contain both somatic and germinal elements.
t These last researches of Patterson brought up the question of the bearing of
polyembryony on sex determination. In the cases already considered, indeed-
Bugmon had already noted it in Encyrtus fuscicollis before the work of Marchal-
all the individuals issuing from one egg were of the same sex. Sex then appeared
to be determined from the begmning of development and thIs was confirmed by
polyembryony in the armadilloes amongst the mammals. Similarly, Silvestri
observed that in Litomastix truncatellus the fertIlized eggs gave nse to females
and the unfertilIzed eggs exclusively to males. This was not so in the encyrtids
studied by Patterson. In Paracopidosomopsis, for example, out of 177 batches of
eggs studIed, there were 154 III whIch the sexes were mixed (about 84 per cent.),
and analYSIS of the data showed that thIS could not be explained by the simul-
taneous development of several eggs of different sexes in the same host.
168 MODIFICA TIONS IN REPRODUCTION OF PARASITES

DISCUSSION
It follows from the brief preceding review that the processes
of reproduction in individuals after leaving the egg are both
common and very varied in parasitic forms. The result of these
processes is so obviously favourable to the perpetuation of the
species, since it compensates for the destruction of a large
number of larvre which will not reach the necessary host, that
the mind is much attracted towards a teleological explanation.
Quite evidently these are adaptations. But the problem is to
know how they have been achieved and how these modifications
of the development of-the individual have come to ensure the
propagation of the species.
Since we reject, a priori, the teleological interpretation, there
remain two possibilities: either these are pre-adaptations
retained and developed by natural selection, or else-and it is
the solution to which I am drawn-these processes manifest
themselves on account of the conditions in which the egg of the
parasite happens to develop, but without an essential connec-
tion with parasitism or with the need of conserving the species.
We may, indeed, note that none of the processes that have
just been reviewed is peculiar to parasitism, but that almost all
of them recur under ecological conditions which are more or
less comparable, particularly among sedentary animals. We have
already had occasion to make comparisons between these and
parasites. Sedentary animals exhibit a very pronounced ten-
dency towards asexual reproduction. Amongst them it results,
in short, from the effacement and dissociation of individuality.
In free-living animals, which may be considered to have a norma~
type of behaviour, individuality comprises two essential charac-
teristics: one of a physiological nature-the individual is a com-
plex of organs, self-sufficing functionally but indivisible; the
other of a morphological nature-the individual is an indi-
visible whole composed of tissues arising from the development
of an egg. Development provides the conditions which are neces-
sary and sufficient for the formation of the complex organic
individual; between its parts rigid ahd necessary correlations
become established.
The change in conditions resulting from a sedentary life con-
sists, above all, in modifying these correlations, some of which
 DISCUSSION 169
lose their obligatory character while other ones become possible.
Hence the diminution of individuality which is com:q1on in
fixed organisms. Now, the conditions of a sedentary life are
realized in numerous parasites which, in effect, are fixed. In
addition, their very special conditions of nutrition are another
factor in changing the correlations and hence in effacing indi-
viduality, and one may explain, moreover, the existence, apart
from parasites, of certain processes of embryonic reproduction,
which must also be dependent on nutrition. Such is the case
with polyembryony and with the processes which can be
compared with it (formation of redire and cercarire, production
of s.exual individuals in the Orthonectidre). We find them
again in non-parasitic animals where the ovum develops in
a nutritive medium analogous to that which the parasite finds
in the host. It happens in the Cyclostomata (Polyzoa), where
polyembryony was discovered by S. F. Harmer even earlier
than Marchal's discovery of it in Hymenoptera. The eggs
of Crisia, Lichenopora, Tubulipora, etc.,' develop in an ovicell
which plays the part of a nutritive chamber, providing con-
ditions analogous to those which the egg of Encyrtus meets
with in a caterpillar. The polyembryony of some mammals is
certainly connected with the very precocious grafting of the egg
on to the uterine wall and with the conditions of nutrition
which result from it. 1
But it is evident that the phenomena of embryonic reproduc-
tion shown by parasites are not explained by a superficial
analogy of this kind, any more than, for that matter, those of
free-living forms could be. It follows that they must not be
envisaged as necessarily deriving from parasitism in its true
sense and considered as an entity, nor as a response to the
mystical necessity for conserving the species. For they are to
be seen apart from parasitism, under more or less analogous
conditions.
In each case they arise from some special present cause
and, above all, a past one. Marchal, dealing with polyembryony
in Encyrtus and Polygnotus, has sought to analyze it. He
attempted, by blastotomy, to find in the conditions to which the
eggs of the parasites were subjected, the circumstances which
led to the experimental production of polyembryony. He
believed that he had discovered a factor of this nature in the egg
170 MODIFICATIONS IN REPRODUCTION OF PARASITES
of Polygnotus, which, in the stomach of cecidomyid larvre,
undergoes very abrupt osmotic changes and at the same time is
submitted to considerable movement. On the other hand, he
connected polyembryony in Encyrtus with the fact that its
development is arrested during the winter, and that the sub-
division of the embryos takes place in the spring, that is to say,
at the moment when the caterpillar host again begins to feed,
which also involves abrupt osmotic changes in the medium in
which the parasite is plunged. But these suggestions are still
very tentative.
The results pbtained of late with tissue culture also appear
to me to be very suggestive, by showing how the development
of cell types may be modified when one succeeds in substituting
truly novel conditions for those normally found in the organism.
Several processes of asexual reproduction found in parasites
must be the consequence of a similar process occurring naturally,
and they must be envisaged apart from any teleological idea.
Each organism has reacted in its own way, by virtue of its
constitution, that is to say, of internal factors which, linked with
the variety of external conditions resulting from parasitism, has
produced the diversity of examples that we see.
 CHAPTER IX

SPECIFICITY IN PARA-SITES AND MODES

OF HOST INFESTATION

ONE of the characteristics of parasitism and, as we have already

seen, of commensalism is the specificity of these associations;
they always occur between definite species. It is a fact of general
importance, but it allows of subdivisions which we are going to
review. Specificity in parasites is, indeed, not an absolute
characteristic, the expression of a pre-established harmony
between host and parasite; it is relative and contingent.

STRICT SPECIFICITY
There are numerous cases and even extensive groups in
which parasitic specificity is very strict. It is so in the Sporozoa
and particularly in the gregarines. Each host has, as a pIe, its
characteristic gregarines. We, that is, Mesnil and m~elf 592,
observed a very significant example of this in Dodecaceria con-
charum. In the plates of Lithothamnion, where this annelid liv.;;(),
it occurs in three forms that we termed A, B and C; the feeding
habits of these three are precisely similar. Now, B invariably
contains a ccelomic gregarine, Gonospora !ongissima, that is
never found in A and C. *
• I support A. Dehorne's decision 585 to create for form B a new species which
he has named Dodecaceria caulleryi, characterized by the peculiarity of Its spoon-
shaped chretre, by the 10cahzatlOn of Gonospora /ongissima in it, by many details
of histology, and by Its development. Dehorne, who found It at Portel (near
Boulogne-sur-Mer), studied it there and watched the remarkable process of
schizogenesis, III which a segment of the middle region of the body (tetragernrnal
segment) spontaneously generates an individual or even a series of individuals.
Mesnil and I have never seen this proceeding at La Hague. Dehome, for his part,
has never found the epitokal forms which I have had occasion to find in abun-
dance among Dodecaceria caulleryi which is plentiful on limestone blocks
collected by fishermen from the sea bottom in the Straits of Dover; I have also
found these epltokai forms sWlffilIDng freely when I have been fi~hing at night by
the aid of a lamp.
Finally, these different processes (epitoky, schizogenesis) have also been found
on ihe American Atlantic coast by E. A. Martm 591 in a closely related species
described In 1879 by Verrill under the name of Heterocirrus fimbriatus, which
171
172 SPECIFICITY IN PARASITES AND ACCESS TO HOST

In a given family one will frequently find that different species

contain gregarines which are similar in appearance but specifi-
cally distinct. Such are the species of Anchorina in the Capitel-
lidre. Leger and Duboscq 101 made the same observation about
the gregarines in myriapods: "Les Pterocephalus", they said,
, 'se trouvent seulement chez les Scolopendres, les Dactylo-
phorus chez les Cryptops, les Rhopalona chez les Geophiles.
Mais ce qu'il semble encore, ·c'est que chaque espece de Scolo-
pendre a son espece de Pterocephale et meme une simple variete
de Scolopendre aura sa gregarine speciale". E. Hesse 93 came
to similar condQsions for the Monocystidre of lumbricids.
Coccidia and Hremosporidia are as a rule strictly confined to
one particular host. Generally speaking, the hrematozoa one
finds in nature can be identified by the species in which they
occur. However, in the laboratory it is sometimes possible to
inoculate related hosts successfully.
Different groups of parasitic Metazoa show us the same
characters of specificity. Such are the Orthonectidre, and to a
large extent the Dicyemida.
The parasitic Crustacea are also highly specific in their hosts.
Giard and Bonnier considered that there was absolute host
specificity in the Epicaridre. But in the absence of morpho-
logically distinct characters which could be assessed, they gave
different specific names to two epicarids found in distinct hosts.
Systematic carcinologists, such as G. O. Sars and H. J. Hansen,
cr.i.~icized this conception as being too sweeping; the latter
evidently went too far in the other direction since, in a more
recent memoir 245 , he reunited in a single species, CumfPchus
insignis, three epicarids that occur in three distinct genera of
Crustacea; the females are similar, but Hansen himself pointed
out the differences between the males collected from the
different hosts. J. Bonnier, discussing the question, has brought
forward important arguments in favour of specificity. He cites,
for example, the case of the parasitism of Portunus holsatus by
the entoniscid Portunion fraissei, which was a new species
always contains a gregarine identical with Gonospora longissima. These Dode-
caceria were found in Bryozoa collected in Vineyard Sound and Martin recognized
in them a type of polymorphism analogous to what we had seen at La Hague:
a sedentary form (correspondmg to our form A but consisting of both males and
females) without gregannes; a form corresponding to our form B (With epitokal
individuals and gregarines) and a form With asexual reproduction. The chretre
have the same characteristics as those III the European forms. •
 STRICT SPECIFICITY 173
created by Giard and himself although there were no precise
characters by which they could distinguish it from other species
of Portunion, but they always found it in this particular species,
Portunus holsatus. Now, later, they found that the male of this
Portunion was quite distinct, so much so that they made this
species the type of a special genus, Priapion (on account of the
great length of the penis). The same authors, on receiving from
Naples a lot of Callianassa parasitized by Epicaridre and con-
sidered as belonging to a single species, found that the parasites
were of two different sizes: they then carefully examined the
hosts and discovered that these belonged to two species that
were related but distinct, C. subterranea and C. truncata, each
carrying one of the two forms' of parasite. Having carried out
research with large numbers of epicarids on various hosts they
saw that in two related species living side by side, and under the
same conditions, only one was parasitized. Thus, at Wimereux,
Porcellana platycheles often contains a Pleurocrypta, while
P. longicornis never does so. These observations, made on large
numbers and under natural conditions, have a special value,
and are very superior to conclusions drawn from scanty material
in museums.
In order to make sure of the identity of two similar epicarids
found on two hosts A and B, it is desirable to be able to rear
the larvre and infect both hosts ,equally with parasites from one
batch. In practice this is impossible. In applying the criterion of
Giard and Bonnier one may retain doubts on the reality of the
distinction between the two species but, as Bonnier remarks, a
mistake of this kind is preferable to the opposite one, for by
inappropriately uniting two species one suppresses all idea of
careful comparison between them.
The parasitic copepods as a rule show strict specificity. This
is true for the species parasitizing fishes, ascidians and annelids
(Monstrillidre, Xenocadoma, Staurosoma parasiticum on Ane-
monia sulcatum, etc.). With the Rhizocephala Giard applied the
same rule of specificity, identifying species of Sacculina by their
hosts; this practice has not been generally followed, but it could
not really be condemned without practical attempts to produce
experimental infestation of several hosts with nauplii from the
same Sacculina, experiments which, in practice, are difficult to
carry out.
174 SPECIFICITY IN PARASITES AND ACCESS TO HOST
fu the Protista (protozoa, bacteria) parasitic specificity
can be very strict without being reflected in obvious morpho-
logical characters in the parasite; thus Laveran and Mesnil 96
have been led to distinguish between pathogenic trypanosomes,
which are mot:J)hologically similar, by their immunity reactions.
That shows that the morphological criterion may be inadequate
for the separation of parasitic forms and supports the general
idea of the specificity of parasites.

-, MODIFIED SPECIFICITY
There is thus in many cases strict specificity in parasites. Con-
trarily, it is averred that other parasites are to be met with in a
series of distinct hosts; s:eecificity may even present a different
aspect for the same parasite, depending on whether it is a ques-
tion of the intermediate host or the final one in heteroxenous
parasites.
Thus, in the trematodes the molluscan host of the sporocyst is
generally rather strictly specific. For Distomum hepaticum in
Europe, it is almost exclusively Limncea truncatula (=L. minuta);
direct experiments have shown that in L. stagnalis, for example,
the miracidium only passes through the first stages of develop-
ment (cf. Kendall, p. 136, footnote), but in regions other than
Europe different species replace L. truncatula as the host of the
miracidium: L. viator in South America, L. humilis in North
America, etc. Facts of this kind are also known for Schisto-
soma; the miracidium of S. mansoni has Planorbis guada-
iupensis for its host in the Antilles, P. olivaceus and P. centri-
metralis in Brazil, etc. But the definitive host in trematodes is.
much less specific. Distomum hepaticum lis found in a whole
series of mammals. Similarly, it has been possible to infest
various species with cercarire of Schistosoma.
In the cestodes specificity seems also to be stricter for the
cysticercus or the cysticercoid than for the adult; there are,
however, many species in which the cysticerci can develop in
numerous hosts. This is notably so in the case of Tcenia echino-
coccus. On the contrary, host specificity can be strict for the
adult. This was shown in experiments carried out by'Joyeux 158
on Hymenolepis in rodents and man. H. nana in man cannot be
distinguished by any precise morphological character from
 MODIFIED SPECIFICITY 175
H.fraterna (=murina) in the rat and other Muridre. Now, while
it is easy enough to bring about infestation in rats with Hymeno-
lepis eggs from any of their congeners, Hymenolepis eggs from
man constantly fail to develop in these animals. Apparently we
have in this instance two species which are morphologically
aimost identical and localized in different hosts.
Specificity often appears to be less strict in the laboratory
than in nature. Thus, although Hremosporidia are usually
specific under natural conditions, some of them can be inocu-
lated into different species. Natural specificity may be related to
the fact that the conditions suitable for infestation do not occur
in connection with other hosts. At other times infestation of
other hosts may take place but will not be maintained in them.
Thus, under natural conditions, fleas and lice are rather strictly
confined to a definite host, or to a small number of hosts related
to one another, although this is not always so. The human flea,
Pulex irritans, is found on various mammals (dog, cat, fox,
jackal, rat, horse, etc.). One can, moreover, feed one particular
flea on different mammals under laboratory conditions. How-
ever, as Joyeux observed 158, if one begins rearing fleas on a host
which is not the normal one it soon becomes obvious that repro-
duction is going badly and that the whole brood is soon in
jeopardy. In other words, a case of this kind shows that there is
a normal host which provides the most favourable conditions,
and that is why, under natural conditions, the parasite is, as a
rule, found only on this host. Leger and Duboscq 103 came to
this conclusion for Aggregata on crabs. Portunus is more suc-
cessfully infested with spores from cephalopods than are other
genera from which, nevertheless, the parasite can be obtained.
In experiments with Bothriocephalus, Rosen 84 obtained
developing onchospheres in several species of Cyclops and
Diaptomus. But it is in Cyclops, and particularly Cyclops stren-
uus, that development is best completed.
The normal host in nature is not, however, necessarily that in
which the parasite develops most actively. We may, suppose,
as Woodcock has done, that the animals in which pathogenic
species cause acute infections are exceptional hosts and not
the normal ones. The latter must tolerate the parasite as it has
become accustomed to it, and must have acquired immunity
relative to it, but not so the former. It is thus that we can interpret
176 SPECIFICITY IN PARASITES AND ACCESS TO HOST

the very virulent trypanosomiases in domestic animals and in

man. Trypanosoma brucei, for example, the cause of nagana
which does not occur in man but is a disease fatal to most
domestic animals, dog, ass, horse and cattle, cannot be con-
sidered as a normal parasite of these species. Its natural hosts
are big game, such as antelopes, where it exists without causing
serious damage. It is when colonial development has brought;
about the introduction by man of susceptible animals that the
parasite has attacked those species which were not adapted to it.
Surra in cattle and human trypanomiasis must doubtless be con-
sidered as analogous examples. Thus, with these parasites,
specificity is' relative since they can exist in very different
species. Seen from the humr;tn point of view of prophylaxis, the
natural hosts of these pathogenic species constitute what is
called a reservoir of infection. In the case of nagana this reservoir
is constituted by big game, particularly antelopes; for mal de
caderas of horses in South America, caused by Trypanosoma
equinum, the reservoir of infection appears to be a large rodent,
Hydroch(Erus capybara, which, moreover, dies from it.
The specificity of the vectors of these different blood para-
sites is likewise very varied. Thus the malarial parasite of man
is transmitted by Anopheles, but not by Culex, its development
only being able to proceed in the former, and conversely Proteo-
soma (near Plasmodium) in birds develops in Culex. Among the
different species of Anopheles there are some which become
infested more easily than others.
It is clear from the facts brought out in the preceding pages
that parasitic specificity is a very complex matter with aspects
varying very greatly from one case to another, from strict limita-
tion to very great lability.

TROPHIC PROPHYLAXIS
If one considers the struggle against these pathogenic para-
sites from the practical point of view, the question has a multi-
tude of aspects, clearly brought out by Roubaud 384 and not
lacking in paradox. Some of these conclusions are closely con-
nected with the analysis of parasitic specificity and must be
summarized here. Besides, since these opinions are both
ingenious and interesting and were inspired by a factual study
 TROPHIC PROPHYLAXIS 177
undertaken under natural conditions, I shall dwell on them at
some length.
The destruction either of the reservoir of infection or of the
vector when, for example, it is a biting insect such as a Glossina
or Anopheles, may be an impossibility. Moreover, the examina-
tion of facts in nature leads to the conclusion that in at least
some infections such destruction is by no means indispensable.
Thus, endemic malaria has progressively diminished in France
and has almost disappeared without Anopheles having been
exterminated. It was feared that in the 1914-1918 war, when
numerous sufferers from malaria were brought into France, the
disease might develop there. Now, in searching for Anopheles,
it was found that it was extremely widespread in France and
that it had never been uncommon: nevertheless, endemic
malaria had disappeared. This is because it never depended
solely on the presence of Anopheles, but on other factors such as
living conditions, soil cultivation, etc.
To explain facts of this kind and to solve the practical prob-
lems of prophylaxis, Roubaud arrived at a general conception
which he termed the trophic method, or protective nutrition, or,
again, trophic prophylaxis. It consists of satisfying the needs of
the species conveying the dreaded parasite, thus turning it away
from man or from some domestic animal. He conceives this
method as more easily applicable in countries new to human
activity where the faunistic equilibrium has not yet become
solidly stabilized in connection with this activity, than in old
countries where all the equilibria have long been established.
In new regions, the changes in the environment achieved or
provoked by man, and the species that he consciously or uncon-
sciously introduces there, create new relationships.
Thus, in Senegal a termite which ravages the plantations of
groundnuts is by no means a specific parasite of this plant;
outside the zone of cultivation it attacks various other plants;
its localization on the nuts of Arachis is due, according to
Roubaud, to its still finding supplies of water there when the
surrounding soil is completely desiccated. By maintaining a
certain soil humidity at the time when the termite attacks the
nuts which are still green, that is to say, in satisfying its needs,
it can be diverted from the groundnuts; this will be simpler than
to attempt to exterminate the termite itself. Similarly, in certain
178 SPECIFICITY IN PARASITES AND ACCESS TO HOST

zones of tropical countries, drought is said to be the reason why

so many flies are attracted to the eyes of man and animals,
whose lacrymal fluid they can drink; accordingly, this would be
the indirect cause of the common and serious eye diseases in
these regions. Hence the suggestion of turning the flies from
man by offering them water. -
In the same way man could protect himself against biting
insects by providing them with prey that they prefer. In wood-
lands, large cattle or horses, for instance, are attacked by taba-
nids or Glossina to a much greater extent than is man. Roubaud
considers that to many parasites, especially to those living on the
skin, the pig is an animal which offers the same possibilities of
nutrition as man, the epidermis of both being naked. This
simple factor allows of the successful penetration of many para-
sites which are stopped by the hairy covering of other species.
Moreover, this similarity has brought parasites to prey on
man which originally must have been specific to the pig or to
other mammals with bare skin.
Auchmeromyia, the Congo floor maggot, now adapted to the
negro race, must have been in the first place a parasite of mam-
mals with bare skin, such as Phacoch(£rus or Orycteropus, on
which Cht£romyia lives under the same conditions, and Roubaud
has seen this last spread into human dwellings. Similarly, a tick,
Ornithodorus moubata, vector of tick fever, seems, according to
observations made in the Belgian Congo, to be, in Africa, a
natural parasite of mammals with bare skin, such as Phaco-
ch(£rus in whose den it is found, and it resorts to man in pro-
portion to the degree of rarity of its natural host. Ed. and Et.
Sergent have made interesting observations in Algeria on the
(Estrus of sheep. It attacks the eyes and nostrils of the shepherds
in Kabylie, producing a myasis known under the name of
Thimni (Tamne amongst the Tuaregs), and since then it has been
found in very different regions. Now, the incidence of infection
in man varies in inverse proportion to the density of the local
population of sheep. Man is not attacked when the numbers of
sheep are sufficient to ensure the normal egg-laying of the fly.
In the same way, the local incidence of sleeping sickness in
Africa bears no relation to that of Glossina; the converse is often
true, which Roubaud explains by the fact that the normal host
of Glossina is big game and not man. It breeds in the forests,
 TROPHIC PROPHYLAXIS 179
where big game is abundant, and normally does not attack man
there. One of the best means of attracting it openly to one
place is to expose an ass or a horse as a trap. Where these natural
hosts are missing the rare Glossina falls back on man; it is in
such situations that its parasites are best propagated in man
in spite of the rarity of the fly.
The gradual decrease and disappearance of endemic malaria
in France and other European countries, although Anopheles
has not become at all rare, has been studied by Roubaud, espe-
cially in the marshes of the Vendee and in the environs of Paris,
and as a result he explains as follows the facts which had pre-
viously been established by Ed. and Et. Sergent. In the Vendee,
a malarial district, the anophelines enter houses from which
they are absent in the lIe-de-France. What is typical is their
presence in stables. They are there in both regions. But they
swarm in the Vendean stables on account of the extent of the
marshes, which leads to the development of great numbers
of l~rvre. The result is that the mosquitoes do not find a
popUlation of cattle sufficient for them to feed on, and invade
the houses, while in the environs of Paris there are sufficient
cattle and they do not attack man. The cow is, then, a protective
shield for human beings and the improvement in health
achieved in the 19th century is easily understood. The cultiva-
tion, drainage and reclamation of the marshes has diminished
the popUlation of Anopheles to whom the increased numbers of
cattle have offered sufficient prey. Man is thus naturally free
from attack. The problem of prophylaxis thus comes down,
following a happy expression of Roubaud's, to an alimentary
equilibrium in the surrounding fauna. It seems to result, more-
over, from observations made in the suburbs of Paris that, once
adapted to feeding on cattle, Anopheles ceases to attack man.
It so happened that the material studied by Roubaud which
led him to the conclusions just summarized, independently sug-
gested the same sort of problems to C. Wesenburg-Lund
in Denmark, and led him also to similar conclusions-to see in
cattle a protective shield against Anopheles-which, with the
progress of human habitation, has resulted in Denmark, as well
as in France, in determining the regression and then the disap-
pearance of malaria. One reads, then, with the most lively
interest the fourth chapter (pp. 157-195) of Wesenburg-Lund's
180 SPECIFICITY IN PARASITES AND ACCESS TO HOST

great work 327 on the biology of the Danish Culicida:, where it

is clear that his conclusions are almost identical with those of
Roubaud.
These very ingenious ideas, which give us all at least a precise
programme of prophylactic experiments, are of particular
interest for the questions envisaged here in having been sug-
gested by direct observation of nature and, above all, in showing
parasitic specificity as a relative property. They fall in well with
the conception of the normal host previously set out. There are
not rigid 1?re-established relationships between species, but
more or less stable equilibria which are relatively easily dis-
turbed. In virtue of this Lamarckian conception, the environ-
ment recovers in this context the place which suits it, and even
the facts of absolute specificity fall naturally into order as
limiting cases of perfectly stabilized equilibria.

HOST PARASITE EQUILIBRIUM

By their enormous extent and the way in which they deal
directly with the natural environment, the researches into
applied entomology undertaken by the United States Bureau of
Entomology have provided very important data on para-
sitic specificity, as far as entomophagous insects are concerned.
For the most formidable insects there have been instituted, as
we have seen, investigations on an unprecedented scale, and as
the parasites of these insects have appeared to be one of the most
efficacious weapons against them, the problem of parasitic
specificity comes naturally under consideration.
The Bureau of Entomology draws up a special list of the para-
sites of each noxious insect, their habits and their parasites or
hyperparasites-the first being friends, the second enemies,
of man. In organizing these dossiers one sees the complexity of
the relationships which govern the natural expansion of species.
Let us take, for example, the studies made on a cotton weevil,
Anthonomus grandis, which became widespread and was force-
fully dealt with. As early as 1913, it was recognized that there
were 54 species that parasitized this insect. A table relating
to 25 of these parasites (which is reproduced in the book by
P. Marchal already cited) shows that their specificity is very
unequal, at least in the present state of our knowledge. Five
 HOST PARASITE EQUILIBRIUM 181
from among them are known to parasitize respectively from
18 to 12 different species, while ten others are so far known
positively only from Anthonomus grandis, and five also from a
second species.
In researches on two lucerne weevils, Hypera punctata and
Phytonomus posticus, W. R. Thompson 324 established data
which plead in favour of a rather restricted parasitic specificity.
In fact, the two species live in the same fields and in very similar
conditions. Now, of the nine parasites of Phytonomus, only two
occur in Hypera.
The most varied and the most important information has
been obtained in connection with Lymantria dispar (Gipsy Moth)
and Euproctis chrysorrhcea ~Brown Tail Moth), which have
already been referred to. The European parasites of these species,
introduced purposely into the United States, have found them-
selves under new conditions there. Let us consider the tachinids;
their specificity is very variable. Certain species have so far only
been found in Lymantria dispar, while Carcelia excisa is also
known on 24 different hosts, Compsilura concinnata on 51, and
Tachina lavarum on 39.
The case of Parexorista chelonia is of a particular interest.
This fly is found both in America and in Europe, where it
develops in rather varied insects and in particular in Lymantria
chrysorrhcea. Now, the American race of the fly never attacks
the caterpillar of this moth, and it has been found that the fly is
not immune to the urticating properties of the caterpillar. It
happens that the introduction of the European race of Parexo-
rista has not been efficacious because it hybridizes with the
American race and the hybrids behave towards the caterpillar
as the American race does and not as the European one.

RELATIVE SPECIFICITY
All in all, the preceding facts show that one cannot consider
the reciprocal specificity of parasites and their hosts as an abso-
lute and uniform property. It is evidently one of the funda-
mental characteristics of parasitism; but it is essentially relative,
and is displayed in highly variable degrees. There are certainly
many cases where it is very strict, a given parasite never being
met with except in a single host species. But it is no less certain
p.s.-7
182 SPECIFICITY IN PARASITES AND ACCESS TO HOST

that many parasites, under natural conditions, infest several

different species of hosts and sometimes even rather a large
number. Specificity must, then, be considered separately for
each parasitic form.
It is necessary, besides, to distinguish between specificity in
fact and in principle. The first is specificity shown by the direct
observation of natural phenomena; the second that which
results from experiment. The restriction of a parasite to a single
host in nature may simply be due to the absence of circum-
stances in which it could penetrate into other hosts but not to
its being unable to develop in them. We have already quoted
the case of parasites which are localized on mammals with bare
skin, which have easily been induced to infest mammals with
hairy skin simply by partly shaving the latter. On the other hand,
there really exist some parasites, above all endo-parasites, which
can only adjust themselves to the internal environment of a
single species to which they are adapted. This is notably the case
with the hrematozoon of human malaria that cannot be cultured
in any other animal species. *
Even in cases where experimental infestation is obtained in
several species, it is clear, as we have already seen in several
instances, that it is more successful in certain species than in
others. One is thus led to distinguish between normal hosts and
those that are exceptional. On this distinction depends the
usually limited localization of parasites in nature, either on one
definite host or on a small number of hosts. Moreover, when-
ever observations of facts in natural conditions are made .on a
sufficient scale, one meets with parasites that have strayed on
to exceptional hosts. That is particularly true of parasites that
migrate, such as the trematodes or cestodes. Many cysticerci
and metacercarire encyst in hosts which will never be the prey
of an animal in which the adult stage of the parasite could be
reached.
Specificity also results, as Roubaud shows very clearly, from
a progressive adaptation of parasites and their hosts, that is,
from an equilibrium of increasing stability in long-established
faunas. New equilibria and new parasitic associations are
* Except, perhaps, in the anthropoid apes. Mesnil and Roubaud 111 have,
indeed, succeeded in infesting a chimpanzee. Their memoir contains a state-
ment on the specificity of various species of Plasmodium.
 METHODS OF INFESTATION 183
realized when a fauna is disturbed by the introduction of new
forms.
All these problems have their equivalents in~ bacteriology,
where the experimental study of pathogenic organisms has
allowed cases to be handled on a vast scale. Experimental
research into syphilis, for instance, such as has-been made in the
last forty years, has shown that this disease, hitherto con-
sidered as strictly limited to man, can be communicated to
numerous species but that it is far from developing in the same
way in them. It is clear that most of the general facts of bac-
teriology apply to parasitism and it is only for reasons of expe-
diency that they are left out here.
Taken as a whole, the preceding observations, then, lead us
in the last analysis to consider specificity' of parasites as very
real but of a relative order and as the result of an evolution;
they depend on extrinsic conditions encountered in Ore past and
in the present by the species under consideration, and in no way
on a pre-established harmony; there can be no question of
regarding parasites as forms specially conceived by Providence
as complementary to the life of definite hosts.

SPECIFICITY AND ACCESS TO THE HOST

One of the important elements in the problem of parasitic
specificity lies in the factors governing the access of parasites to
their hosts and their penetration into them. The study of these
factors is then complementary to the preceding question. It is
clear that all the methocs by which parasites penetrate cannot
be reviewed. Each species has its special one. But a few examples
will give an idea of the variety and interest of these processes,
and of the part they can playas far as parasitic specificity is con-
cerned. It is with internal parasites that the question principally
arises, although with external ones the problem of access may
be equally interesting. Two chief methods of infestation may be
distinguished: one that is passive and another in which the para-
site plays an active part.
Passive infestation takes place either by the ingestion of spores
or of eggs, or by that of an intermediate host containing the
parasite, or by inoculation through the bite of some vector
organism. If there is ingestion of eggs, spores or cysts the
184 SPECIFICITY IN PARASITES AND ACCESS TO HOST

organism is usually liberated by the action of the digestive juices

of the host on the protective envelopes, and this action implies
a certain specificity which has been shown plainly, for instance,
with the Sporozoa. The spores of gregarines, or of Myxo-
sporidia, only open when acted on by the gastric fluids of certain
hosts, or at least open better then. The organism liberated must
be able to r~sist the action of these fluids and there, again, is a
specificity which is generally limited in extent. Between the
liberation of the organism or of the ingested larva and its arrival
in its finalloc'ation, where development will be completed, there
often occur complicated journeys.
Direct inoculation into the internal medium of the host is the
most perfect method of transmission. The malarial parasite,
Plasmodium malarire, may be taken as an example of this. It
passes from man to the culicid, Anopheles, by suction, undergoes
an elaborate development in the mosquito, ending with the
localization of the sporozoites in the salivary glands and the
proboscis; these organisms are finally inoculated directly into
man. Most of the Hremosporidia are transmitted in an analo-
gous way by various intermediate hosts: mosquitoes, leeches, etc.
But this complete adaptation is not always achieved. Thus,
with Filaria bancrofti, the larvre which have developed in the
mosquitoes do not penetrate into the proboscis, but accumulate
in the labium of the insect. At the moment when the latter bites
they are simply deposited on the skin which they break through
by their own efforts. Here, then, there is passive transport to
the host and active penetration into it. It is the same in a certain
number of cases where blood-sucking insects are the vectors of
the parasite. The latter is deposited by them on the skin with the
saliva or even with excreta, and finally penetrates by means of
an abrasion, excoriation or bite of the insect; this must be
the method of penetration of a certain number of microbes
such as plague bacilli, various spirochretes, particularly that
of recurrent fever which comes into contact with the skin
principally by the crushing of a louse. It is clear, then, that a
number of mechanisms are concerned in the transmission of
parasites by intermediate hosts. '
The ways and means of penetration of parasites not involving
an intermediate host ate, however, much less simple than one
might suppose, as we shall be able to show by'some'examples.
 PENETRATION BY NEMATODES 185
That of Sacculina is typical in this connection and the reality is
quite different from what one could have supposed a priori. For
many internal parasites of invertebrates the method of penetra-
tion is unknown. We do not know how animals such as Fecampia
or the eunicid parasites of annelids enter their hosts. So far, the
penetration of Dicyemida into the kidney of cephalopods has
not been seen.
One of the groups in which the facts are most varied and
unexpected is that of the nematodes, which show extreme diver-
sity in their ways of life, both as parasites and saprophytes, and
also in their localization in their hosts. We have already seen
what is known of species of Filaria in the blood. There is still
a certain number of these parasites whose method of penetra-
tion is unknown. We know nothing yet about the penetration
of parasites such as Eustrongylus visceralis into the kidney of the
dog and different mammals. But even with the intestinal nema-
todes, which appear to penetrate by simple ingestion and to
develop directly in the intestine, the reality is sometimes much
more complex.
Such is the case with Ancylostomum duodenale, the cause of
miners' anremia. For a long time it was believed to be ingested
either in water or in food soiled by the hands. The researches of
Looss 194, confirmed by other workers, showed that this could
not be the most usual method. The eggs evacuated with the
freces develop externally, provided that the temperature is high
enough (hence the localization of the parasite in warm countries
and in mines); the larvre usually penetrate into man through the
skin. Looss happened to'" observe this accidentally on himself,
under conditions in which contamination per os was impossible,
and he carefully proved it. Larvre of Ancylostomum deposited
on damp skin penetrate into it in a few minutes; he established
this particularly on a leg infected an hour before amputation. In
experiments with dogs and monkeys, using A. duodenale and
A. caninum, the larvre were placed on areas of shaved skin
and he was able to follow all the phases of their penetration and
their final journey. As they penetrate they cause irritation and
redness, and, in heavy doses, temporary redema. They pass into
the blood vessels and lymphatics, where some are destroyed by
phagocytosis in the lymphatic ganglia. They reach the heart by
way of the veins, and from there pass to the lungs, in which it is
186 SPECIFICITY IN PARASITES AND ACCESS TO HOST

possible to bring about a heavy infection within a few days.

From the lungs they pass to the trachea and thence to the ceso-
phagus, finally reaching the intestine. Outside, these larvre are
very susceptible to desiccation; a few moments' drought suffices
to kill them, which happens most often on food. On moist skin,
and principally thanks to sweat, they find favourable con-
ditions. In the galleries of mines they easily pass up the damp
walls and from there move on to the hands of miners. This is a
very significant example of the complexity which is sometimes
found in the mechanism of penetration by parasites.
Strongyloides stercoralis follows a similar course, and prob-
ably other nematodes too. Luhe reports, in connection with the
experiments carried out by Looss, that at the autopsy of a
panther he found a lung full of nematodes, probably resulting
from a similar migration.
Ascaris lumbricoides, the common intestinal parasite, has a
no less complicated life history. Stewart 204, then Ransom and
Forster 200 (confirmed further by Yoshida 209, working on rats,
mice, young pigs, rabbits and guinea-pigs) showed that the
larva: emerging from the eggs ingested per os do not develop
directly in the intestine but pass into the intestinal circulation
and after that complete a circuitous course analogous to that of
Ancylostomum, passing through the lung on the way. By
making young pigs ingest large doses of the eggs of A. lumbri-
coides, over a period of two weeks, Ransom and Forster pro-
duced fatal pneumonia in these animals within eight days; at
the autopsy the lung was found to be full of young Ascaris,
while the controls were in good health. At the end of ten days
the worms were found in the mouth and the cesophagus. In·the
rat and mouse the initial stages are the same but infestation is
not completed and goes no further than the mouth. Pig and
man are the normal hosts; in the sheep, which must be an acci-
dental host, intestinal infestations have been obtained. Experi-
ments of this kind show the elasticity of the idea of parasitic
specificity. They indicate, moreover, how many interesting dis-
coveries remain to be made in the domain of parasitism,
concerning the conditions of penetration into the, host.
The life history of Ancylostomum 'will naturally be compared
with that of Schistosoma (=Bilharzia) outlined earlier, in
which the cercaria also passes through the skin.
 PENETRATlON BY DIPTERA 187

MYIASES
The'larvre of flies, which show considerable ecological varia-
tion, ranging from a saprophytic to a strictly parasitic life, also
supply some extremely interesting instances of access to the host.
The tachinids, whose entomophagous larvre play so' impor-
tant a part, as has already been said, reach the host in very
different ways, which Townsend 326 has studied and which he
classifies in the following manner:
1. The laying of eggs on leaves where they are ingested by
the host.-The larva hatches in the gut of the latter and passes
into the general body cavity where it develops in the adipose
tissue. The eggs of these species are small and dark, and only
hatch under the influence of the intestinal fluid of the host
(e.g., Crossocosmia sericarice parasitizing the silkworm; Blephari-
poda scutellata parasitizing Lymantria dispar, etc.).
2. The laying of the eggs on the host.-The egg laid, for
instance, on a young caterpillar hatches fairly quickly and the
larva penetrates into it. In its last larval instar it pierces the body
wall from within, so as to have a respiratory opening. This
method was the earliest known (e.g., Thrixion halidayanum,
studied byqPantel; Parexorista chelonice, parasite of Euproctis
chrysorrha;a).
3. The laying-of larvre which are deposited on the skin of the
host (Dexiida:).
4. The laying of the larvre beneath the skin of the host.-The
female uses the ovipositor to pierce the caterpillar, and intro-
duces the larva under the skin (e.g., Dexodes nigripes, Compsi-
lura coccinata, parasites of Euproctis chrysorrha;a and Lymantria
dispar).
5. The laying of larva: on leaves or stems.-Case of Eupele-
teria magnicornis, which deposits its larvre on branches where it
has recognized (probably by smell) the presence of caterpillars,
the larvre being placed in the track they will take on returning to
the nest. The larvre hook on to the caterpillars as they pass by
and penetrate into them.*
In matters of detail we see curious adaptive characteristics
* The Nycteribidre whIch live on bats also lay larvre, whIch are ready to pupate,
on branches in the neighbourhood of Pteropus but not on the ammal Itself, as
Rodhain and Bequrert 313 described In the case of eyclopodia greeffi.
188 SPECIFICITY IN P ARASlTES AND ACCESS TO HOST
in the eggs and larvre of tachinids relating to these various
conditions. .
I shall show this by referring to Pollenia rudis, which has been
very well investigated by Keilin 299. Here the egg is laid on the
soil. The larva, after hatching, penetrates into a lumbricid,
Allolobophora chlorotica, through the openings of the seminal
vesicles in which it passes the winter and spring. In the month
of May it burrows through the host's tissues to its anterior end
which it perforates, making an opening through which its pos-
terior extremity together with the respiratory openings juts out.
Flies with larvre parasitic on vertebrates (causing myiases)
provide us with numerous data of the most interesting nature.
Some of them are rather saprophytes than parasites, living in
ulcers, doubtless at the expense of the bacteria which multiply
there. They show the beginnings of adaptation to parasitism.
Certain of these larvre are by no means specific, others tend
to be specialized and produce very definite myiases; such
is pycnosoma bezzianum, which lays its eggs on the hairs of
Bovidre and Equidre; the larvre finally burrow into the skin and
cause ulcers; never does the fly lay in already existing ulcers.
Such also are Lucili'a argyrocephala and L. sericata.
Certain species have blood-sucking larvre, living near the host
and coming into contact with it intermittently in order to suck
its blood. This is the case with Auchmeromyia, thoroughly inves-
tigated by Roubaud 316. The larva, the Congo floor maggot, is
biologically tied to the negro race as we have already seen; the
species only maintains itself in settled tribes that sleep on the
bare floor of the cabins. The larvre, inert during the day, leave
the ground at night to suck the blood of the sleepers. They are
not found amongst nomadic tribes. Ch(J!romyia, found in the
burrows of Phacoch(J!rus and Orycteropus, is similarly adapted
to those animals which have bare skin like man. And there exists
a series of flies, Phormia sordida, P. (Protocalliphora) azurea,
and Passeromyia heterochreta, which live in birds' nests at the
expense of their young.
Other flies producing myiases lay eggs on the ground and the
larvre actively seek the host into which they penetrate. Such is
Cordylobia anthropophaga, whose larva, Cayor's worm,* pro-
* Lund's larva, which lives in analogous condit1ons, belongs to another species,
Cordy/ohia (=StasslO) rodhaim.
 PENETRATION BY DIPTERA 189
duces in the depth of the skin of the host (rat, dog, and, in
addition, man) a furunculous tumour with a permanent opening
through which it breathes.
Some of them reach the host in a very curious and indirect
way, being carried by another insect. This is the case with the
South American fly Dermatobia hominis,""w)Jose larva, the
Macaque worm, produces a cutaneous myiasis. It lays its eggs
on insects (Stomoxys, and particularly a culicid, Janthinosoma
lutzi) when they are biting horses. These insects, principally
Janthinosoma, are the agents by which the larva reaches man
(see Neiva 306).
Others lay directly on the host, particularly CEstrus ovis of
sheep which lays during flight on the nostrils or eyes; the larva:
develop in the nasal fossre, producing false staggers. The botfly,
Gastrophilus equi, of horses, lays its eggs on the hair in places
where the horse can lick them. The roughness of the lips during
licking causes the egg to open and set free the larva which, on
reaching the host's mouth, burrows into the epidermis, as
Roubaud 318 has shown, and makes its way by the resophagus
to the stomach, where it completes its growth, fixed to the wall.
It is cast out in the dung at the moment of pupation. The warble
fly of cattle, Hypoderma bovis, which causes sub-cutaneous
tumours on the back in the vicinity of the vertebral column,
does not develop there but penetrates under the same con-
ditions as the botfly of the horse, burrows along the wall of the
resophagus, then follows the diaphragm, crosses the verte-
bral column and finally reaches the skin of the back, where it
causes a sub-cutaneous tumour. The fully developed larva
passes outside when the tumour festers. Certain birds (magpies,
starlings, wagtails) frequently extract and feed on these larva:
by breaking open the tumour.
From these various data relating to the Diptera we come
to the case of the jigger, SarcopsyUa penetrans, a flea whose larva
burrows actively under the skin, mainly of the foot, and
grows there, forming a small swelling which remains open
exteriorly.
These different examples show how the finai position of the
parasite is insufficient in itself to teach us how infestation came
about.

7*
190 SPECIFICITY IN PARASITES AND ACCESS TO HOST

HEREDITARY TRANSMISSION
Another class of facts relating to methods of penetration in
parasites is provided by cases in which infestation is hereditary
and transmitted;b1the egg. We now know a certain number of
examples of Protozoa, bacteria and Protophyta. The most
classical case js that of the Microsporidia, and in particular
that of pebrine, Nosema bombycis, in the silkworm. It was
through noticing that the egg was contaminated by corpuscles
that Pasteur conceived the method of dealing with the eggs,
which allowed of the establishment of healthy broods. Direct
contamination occurs by the mouth, the caterpillar eating leaves
soiled by excrement carrying the spores of the parasite. These
develop in the gut and the Microsporidia penetrate into the
intestinal epithelium, then into the various tissues that they
invade, finally reaching the ovary. It is very probably the same
with many other Microsporidia; Mesnil, for instance, has con-
firmed the presence of spores of Nosema incurvata in the.eggs
of Daphnia obtusa.
Piroplasma is also transmitted in ticks from one generation
to another by infestation of the eggs. Theiler has even estab-
lished that infection can persist throughout two generations
without being renewed by fresh parasites. It is thanks to this
hereditary transmission that bovine piroplasmosis is trans-
mitted; for certain ticks, Boophilus annulatus and B. decoloratus,
do not again leave the animal to which they become attached
in the larval stage and where they have become infected. Trans-
mission can thus only take place through the daughter ticks;
and, moreover, Piroplasma has been found in the eggs. The
same type of hereditary transmission, by Rhipicephalus
sanguineus, occurs in canine piroplasmosis. Spirochretes are also
hereditarily transmitted by ticks, particularly species of Argas.
In the light of recent research the role of ticks in the transmis-
sion of various infections of man and other animals appears to
have a very considerable importance. .
Brumpt has similarly shown that Trypanosoma inopinatum
in the green frog is hereditarily transmitted by the intermediate
host, a leech, Helobdella algira. The leeches, born of an infected
mother and having had no other source of infection, contain
 TRANSMISSION BY THE EGG 191
trypanosomes in the proboscis and the gastric creca. But their
presence in the egg itself has not been established.
Finally, hereditary transmission by the egg plays a major role
in infections which have a particular significance, as we shall
see: we find this in the yeasts (green bodies, pseudova, pseudo-
vitellus) which regularly occur in various groups of insects,
notably the aphids. We only mention them here and will study
them in connection with symbiosis.
 CHAPTER X

RECIPROCAL REACTIONS OF PARASITE

AND HOST

THE effect of parasites on their hosts is a problem of very great

extent, which, in the last instance, includes all the infectious
illnesses and the problems they set us, such, in particular, as
that of immunity. There can be no question of dealing with
them here. In restricting ourselves to non-bacterial parasites it
is evident that the effect depends largely on the circumstances
of parasitism. Many parasites, practically harmless in small
numbers, become formidable and even fatal in the case of a
heavy infestation. Thus some kinds of trichina only cause slight
trouble as a rule, though the ingestion of large numbers of these
nematodes brings about an illness which is rapidly fatal. One
could cite analogous examples for trematodes. The hedgehog,
for instance, harbours some which under ordinary conditions
are inoffensive; such are Distomum leptosomum and D. spinu-
]osum, whose sporocysts live in Helix hortensis and Helix
nemoralis. But when Hofmann 156 fed hedgehogs with infested
individuals of Helix, he produced a heavy fatal infection in them.
In considering infestations which are not acute, one may say
that a parasite, particularly an internal parasite, when once
established on its host forms with it a functional system in a
state of equilibrium, the whole of which is opposed to the
external environment. It is what Giard 586 expressed by the
term complexe heterophysaire, each of the two organisms being
a complexe homophysaire. The equilibrium thus conceived
results from effects and mutual reactions, and we shall examine
the principal types of these.

PARASITES AND FOREIGN BODIES

Since the parasite is primarily a foreign body introduced acci-
dentally into the host, we may expect to see the latter attempt
to eliminate it, or at least to isolate it from the internal environ-
192
 PHAGOCYTOSIS 193
ment, by a cellular or non-cellular barrier, such as is formed
around an inert'body. One may, indeed, cite a certain number of
examples of this. Trichina larvre in muscles are surrounded by a
cyst membrane which is generally calcified. The production of
pearls in molluscs seems to be, at least to a large extent, a reac-
tion of the same nature, for in the middk of most pearls there is
a parasite, most frequently a larva of a trematode or of a ces-
tode. The pallial epithelium, on coming into contact with it, has
secreted a layer of mother of pearl which has isolated it. This
reaction continues and concentric layers are formed and accu-
mulate to constitute the pearl-mother of pearl if the process
remains external and in contact with the shell, a true pearl if the
process is completed within the visceral mass of the mollusc.
The parasitic origin of pearls, recognized in '1852 by de Filippi
in Anodonta, has since then been the subject of numerous works,
notably by Seurat 385 in Tahiti, by Herdman and Hornell in
Ceylon, by L. Jameson'377 on mussels of the French coasts
(Billiers, Morbihan), by R. Dubois, Giard, etc.

PHAGOCYTOSIS IN NORMAL AND ABNORMAL

PARASITES
The production of a membranous cellular envelope around
the parasite is a rather rare phenomenon, at least in the case of
normal parasites; even though amrebocytes accumulate very
rapidly around inert foreign bodies, most normal parasites
living in an internal tmvironment remain free from them. Thus,
as Cuenot has pointed out 89, the crelomic gregarines are never
enveloped by amrebocytes as long as they are in the vegetative
phase.
The formation of an en~elope occurs as soon as they encyst
or even prepare to encyst. Leger 97 showed this perfectly clearly
in the case of Lithocystis schneideri, a gregarine living in the
crelom of a sea urchin, Echinocardium corda tum. Around the
cysts, on the other hand, amrebocytes form enormous blackish
masses. * Metacercarire of trematodes, encysted, for instance,
,.. We, that is, Mesnil and myself 592, nevertheless observed phagocytes
enveloping a crelomic gregarine, Gonospora /ongissima (form B). III Dodecaceria
concharum. But it is possible that the cases in which we saw this phenomenon
were the prelude to the encystment of this gregarine.
194 RECIPROCAL REACTIONS OF PARASITE AND HOST
in annelids, are also surrounded by a thick mantle of amrebo-
cytes, as I have myself seen with cercarire of Echinostomum in
the crelom of Arenicola, the lugworm of anglers. Tn the case of
Entoniscidre (Crustacea, Isopoda, cf. pp. 77-80) the recent
researches of Veillet 277~ too, have shown that the cryptoniscan
larva, immediately after its penetration into the crab that it
infests, is covered over by an envelope of amrebocytes. Simi-
larly with nematodes encysted in the ccelom of lumbricids; thus,

Figure 62. Lithocystis schneideri.

1, phase when the gregarine is free-living and motile (two individuals
entwined) and without a phagocytic sheath in the crelomic fluid of
the urchin Echinocardium cordatum; 2, prelude to the encystment of
two individuals, paired and contracted, and already covered with a
sleeve of phagocytes; 3, some of the phagocytes greatly enlarged
(after Leger).

the larvre of Pollenia rudis are enveloped in winter, during their

resting stage. But when these various parasites are in an active
state they are not surrounded. It appears that normal parasites
possess immunity against amrebocytes and phagocytes. This is
what happens in particular, as a general rule, in entomophagous
parasites. But with abnormal parasites it seems to be otherwise.
Timberlake 388, for example, induced the hyWenopteron
Limnerium validum, which normally parasitizes Hyphantria
cunea, to lay eggs in Euproctis chrysorrhfEa. Now, although very
 RARITY OF PHAGOCYTOSIS 195
many eggs were laid, he found only very few larvre in the cater-
pillars. Most were destroyed or strongly attacked by phago-
cytes. W. R. Thompson 324 found that it was much the same in
Sturmia scutellata, a tachinid normally parasitizing Lymantria
dispar. The eggs of this fly are deposited on leaves which are
finally eaten by the caterpillar; the eggs hatch in the alimentary
canal and the larvre pass from there into the general body
cavity. Thompson fed these Sturmia eggs, on leaves, to various
caterpillars; the larvre developed in members of the Lasiocam-
pidre, but not in caterpillars of Vanessa urtica and Parorgyia
antiqua, where they were found to be attacked by phagocytes.
In these several cases it was unfortunately not possible to deter-
mine .whether the phagocytes attacked healthy larvre or only
those that were dead or had already had their vitality greatly
reduced.
On the whole, it appears that normal parasites do not as a
rule provoke a phagocytic reaction, or else they inhibit it by
appropriate secretions which are not possessed by abnormal
parasites. The absence of reaction in normal parasites is then
doubtless the result of an adaptation of a secretory nature. We
may believe that such a mechanism makes it possible for the
parasite to live in the intestine or internal environment of the
host. It must be able to resist the enzymes and other substances
of this medium. The problem has been solved in the case of
those intestinal parasites which are not digested. According to
Dastre and Stassano 373, tapeworms resist by producing an
antikinase, neutralizing the intestinal kinase and, as a result,
indirectly preventing the action of trypsin. According to
Weinland 394, the substance produced by the parasite must be
an antitrypsin. We have obviously still a great deal to learn
about these matters. A class of new facts of major practical
importance is involved but cannot be dealt with here, the ques-
tion of antibiotic substances, produced in a strictly specific
fashipn by certain fungi. This is a process which is probably
of very great extent, at least in the vegetable kingdom but prob-
ably also in the animal kingdom. We see in the case of penicillin
and streptomycin that it is of the first practical importance and
we are obviously only at the beginning of this new chapter of
biology.
196 RECIP~OCAL REACTIONS OF PARASITE AND HOST

PARASITES AND TOXINS

The apparent effect of many parasites on their hosts is slight,
even extremely slight when one considers the enormous bulk of
many of these parasites in comparison with the host, and the
toll that tltey must take of the food of the latter.
Often they appropriate reserve substances: thus, the entomo-
phagous types do not prevent the caterpillars from developing
and pupating, but the latter have no further material available
for effecting metamorphosis.
It is by means of toxic substances that the action of many
parasites principally makes itself felt. The feverish reaction in
malaria, for example, is produced when after each phase of
reproduction the elaborated toxins are liberated in the blood
through the breaking down of the corpuscles where schizogony
has taken place. The peri-intestinal fluid of Ascaris megalo-
cephala contains a toxic substance which, on contact, provokes
a lively irritation of the cornea and of the naso-pharyngeal
mucous membrane, and it has often happened that zoologists,
after having handled specimens of this Ascaris, have felt its
effects. Weinberg 393, by collecting the peri-intestinal liquid
under aseptic circumstances and injecting it into guinea-pigs,
has shown that it is, indeed, the irritant substance and is very
toxic (a dose of 0·5 cu. mm. rapidly kills a guinea-pig). Dropping
this liquid into the eye of a horse provokes a violent reaction but
not a constant one. According to Weinberg, the horses which are
not sensitive to it are, in general, those that carry a large number
of these worms. There is thus ground for thinking that immu-
nity is established against this Ascaris toxin. Moreover, heavily
infested horses are often thin and their serum contains specific
antibodies. *
Ancylostomum duodenale causes, as we know, a severe
anremia which is often fatal but the mechanism of which is not
yet known. For a long time it was attributed to hremorrhages
provoked by the worm, and L. Lreb and A. J. Smith 379 have
shown that these worms secrete an anti-coagulant substance
apparently connected with a diet of blood. Nevertheless, accord-
ing to Looss 195, they feed not on blood but on debris from
* Sarcosporidia in sheep contain a toxin, sarcocystine, isolated and studied by
Laveran and Mesml 378; it is very active in the rabbit, which is kiIIed by a very
smaIl dose, but it bas only a sh&ht effect on sheep.
 EFFECT ON HOST METABOLISM 197
the mucous membrane and the hremorrhages are incidental in
character. The effect of these worms is said to be due to a toxin.
The anremia caused by Bothriocephalus is also said to be the
result of the action of a toxin, but this seems to be liberated, and
therefore to react, only when the worm is diseased or dead;
the toxin is then able to diffuse. ,
In these various cases the reaction of the host to these toxins is
shown by alterations in the blood. Most of these parasites indeed
cause a more or less intense eosinophilia, seen in the bearer~ of
echinococci, ancylostomes, filarial worms, trichinas, dermal
myiases, etc. Moreover, one can produce this eosinophilia in a
guinea-pig by injecting it with extracts from these different
parasites.
ANTIBODIES. The serum of the hosts of these parasites has
also been found to contain specific antibodies (lysins, precipi-
tins, anaphylactic antibodies) and the existence of these anti-
bodies can become a means of diagnosis, as Weinberg 392 has
shown with echinococcus. In all these cases, however, it is neces-
sary to take into account the possible effect of bacteria intro-
duced by the parasites through the lesions they produce, and to
guard against this cause of error.

THE EFFECT OF THE PARASITE ON THE GENERAL

METABOLISM OF THE HOST
Certain parasites profoundly affect the nutrition of the host
by modifying its metabolism in a remarkable way. Wheeler 398
pointed out a very curious fact of this kind in an American ant,
Pheidole commutata. The workers, parasitized by Mermis, are
hypertrophied; the volume of the abdomen is eight times greater
than the normal; the head, the thorax and all the organs are also
hypertrophied. Wheeler distinguishes these individuals by the
name of macroergates. This hypertrophy is evidently the result
of excessive larval growth brought about by overfeeding due to
the parasite. The parasitized larvre have to be nourished in an
appropriate fashion by the workers.
Sacculina, too, brings about an appreciable modification of
the metabolism of the crab that it infests, as was shown by
the researches of G. Smith 387. In its system of rootlets and at
the expense of the crab's blood, Sacculina elaborates reserve
198 RECIPROCAL REACTIONS OF PARASITE AND HOST

substances which ,in female crabs would be laid down in the

ovaries. The chemistry of the blood differs remarkably in male
and female crabs. In Carcinus memas, normal blood is more or
less colourless except towards moulting when it is pink. In the
female it is yellow when the ovary is approaching maturity; these
two tints denote respectively the presence in the blood of tetro-
nerythrin and lutein. The fat content of the blood is 0·198 per
cent. in females with yellow blood, 0·086 per cent. in males with
pink blood, and 0·059 per cent. in males with colourless blood.
The liver, like the blood, shows considerable and parallel varia-
tion in the fat content, which varies from 4 to 12 per cent., the
largest amount being found in females in which the ovary is
nearly ripe.
Now, in the crabs of both sexes that are carrying Sacculina,
the liver is always very rich in fat and the blood is pink or pale
yellow. The blood of the parasitized males contains a great
excess of fat in comparison with the normal, and approaches
the composition of the female's. Thus, Sacculina causes in the
host, whatever its sex, the development of a metabolism that is
characteristic of the female. * These modifications are reflected
in the crab's morphology, as was shown by Giard 586, who con-
sidered it to be a very common result of parasitism and dealt
with it under the name of parasitic castration.

PARASITIC CASTRATION
In parasitic castration, as Giard conceived it, there are in
reality two sets of facts: on the one hand, actual castration, that
is to say more or less complete atrophy of the gonads caused by
the parasite; on the other hand, a correlated alteration of the
secondary sexual characters leading to the proouction of indi-
viduals more or less intersexual in appearance.
Giard distinguished between direct and indirect castration.
In the former the parasite develops in the genital organs them-
selves, and takes their place; thus an restrid, Cuterebra emascu-
lator, develops in the testes of a squirrel, Tamias listeri; Disto-
mum megastomum destroys the gonads of a crab, Portunus
... In short, Sacculina acts like an ovary on the metabolism of the host and
diverts assimilated substances towards itself. Kellin 299 proposed the term
nutrition dlfviatrice for facts of this order, very widespread amongst entomopha-
gous insects.
 PARASITIC CASTRATION 199
depurator; many trematode sporocysts and redire invade and
destroy the hermaphrodite or unisexual glands of the molluscs
that they infest, either pulmonates or prosobranchs. Amphiura
squamata is sterilized by the orthonectid, Rhopalura ophiocomce,
which develops in the immediate vicinity of the host's ovaries
whose growth is then arrested, but the testes of this herma-
phrodite species are normal. Sacculina checks the develop-
ment of the gonads of crabs, either ovaries or testes, but
castration is not always total, particularly in the male.
Of much more frequent occurrence is indirect parasitic castra-
tion resulting from a distance effect. It is to be seen very generally
in crustaceans that are carrying Epicaridre, as Giard and Bon-
nier were the first to point out. I myself 226 had occasion to see
a very significant example of it in some specimens of Peltogaster
curvatus attached to hermit crabs and parasitized by a crypto-
niscid, Liriopsis pygmcea. During growth, this parasite feeds by
sucking up the host's juices; in the adult stage it feeds no more.
Now, in individuals of Peltogaster carrying Liriopsis, the
oocytes in the ovary are always undergoing degeneration and
appear to have been emptied. This evidently results from the
epicarid's diverting to itself the substances from which the ovary
of the rhizocephalan should be built up; but this state of affairs
terminates when the parasite itself ceases to feed. It is quite easy
to find and recognize specimens of Peltogaster which have pre-
viously carried Liriopsis, as the latter leaves a lasting hole in the
mantle. Now, in these individuals the ovary has regenerated and
regularly ripens its oocytes. Their degeneration was then due to
the diversion of food substances by the epicarid.
Parasitic castration also occurs in plants: either direct castra-
tion by the development of fungi in the floral organs; or, what
is more interesting, indirect castration effected at a distance by
various parasites. These parasites cause nutritional disturb-
ances which act on the whole plant and lead to the virescence of
the parts of the flower, or the transformation of the stamens
and pistil into petals. Molliard 406 has pointed out a certain
number of cases of this kind: Knautia arvensis attacked by Pero-
nospora violacea; Matricaria inodora attacked by Peronospora
radii; Viola sylvatica infested by Puccinia violce; various Umbel-
liferre and Cruciferre under the influence of acarines. In Primula
officinalis the pistil and stamens become petaloid as a result of
200 RECIPROCAL REACTIONS OF PARASITE AND HOST
a fungus invading the roots. So does Scabiosa columbaria, on
stems where the roots bear galls of a nematode, Heterodera.
Molliard put forward the hypothesis that most double flowers,
if not all, result from parasitic associations. This is typical
castration.
The same interpretation may be given to an alteration in an
inflorescence that Giard 374 had pointed out in one of the Com-
positre, Pulicaria dysenterica, and about which he had put for-
ward certain very ingenious suggestions. In some places,
for several years running, one sees stems on which the peri-
pheral flowers of the capitUlum have lost their ligulate form
and are tubular like those of the centre; they present divers other
anomalies: in particular, the flowers of these plants have a
strong tendency towards unisexuality. Now, Molliard 407
observed that in the plants of Pulicaria displaying these anoma-
lies the roots were attacked by a weevil, Baris analis, and it is to
the effect exercised by this parasite that the modifications of the
inflorescences must be attributed. Indeed, these modified stems,
after being rid of their weevils, eventually produce normal
flowers. Molliard has, besides, had occasion to find analogous
modifications which are always connected with the presence of
parasites: a plant of Sinapis arvensis, with virescent flowers,
proved to have weevil larvre in the collar region; larvre of a
weevil, Hylastinus obscurus, were present and ate out long gal-
leries in the equally virescent stems of some plants of Trifolium
repens; they are not found in normal stems. Primula officinalis
and some kinds of Senecio have provided similar data. In par-
ticular, some plants of Senecio jacobcea, with their general aspect
completely modified and their inflorescences altered into c.om-
pact balls without peripheralligules, had their stems mined by
larvre of Lixus.
Let us now consider the alterations in the secondary sexual
characters correlated with parasitic castration. The first of these
cases was pointed out by J. Perez 382 in Hymenoptera of the
genus Andrena, parasitized by Stylops. Members of either sex
lose their distinctive characters to some extent and tend to
acquire those of the opposite sex. In the female, at the same
time, the ovaries atrophy and their oocytes no longer reach
maturity. In the male, only the testis on the side where the para-
, site is situated is altered; the other remains functional. It is to
 PARASITIC CASTRATION 201
be noted that in America these modifications have not been
found in the same parasitic associations.
The most striking case, discovered by Giard 586 and carefully
re-investigated by G. Smith 387, is that of crabs parasitized by
Sacculina. The female scarcely undergoes any modification,
while the male resembles the female type. These modifications
are very variable in extent: they can reach a roint where the
diagnosis of sex becomes very difficult. They aftcct the form of
the abdomen, the independence of its segments, the abdominal
appendages and sometimes also the chelre. Let us take two
examples: Carcinus mcenas and lnachus scorpio (=mauritanicus).

Figure 63. Modifications in the abdomen of Carcinus mamas

(dorsal and ventral aspect) under the influence of Sacculina
(after Giard).
I-I', abdomen of normal female; II-II', that of normal male; III-ill', that
of a male parasitized by Sacculina.
In Carcinus mcenas the abdomen of the female is wide and
rounded and all the segments are quite distinct; the abdomen of
the male is pointed and triangular in form; furthermore, seg-
ments III, IV and V are united into one whole. Now, in males
parasitized by Sacculina these segments become independent
and at the same time the abdomen becomes enlarged and
rounded (Fig. 63).
In Inachus scorpio, of which a special study was made by
G. Smith, working on abundant material collected at Naples,
the facts are still more striking. The shape of the abdomen
differs very considerably in the two sexes, as is the rule in the
oxyrhynchous crabs. That of the male is rectangular and very
202 RECIPROCAL REACTIONS OF PARASITE AND HOST
narrow, that of the female wide and rounded. Now, one finds
males parasitized by Sacculina, in which the abdomen has
assumed the female form. But here the modifications also extend
to the abdominal appendages. The female possesses on each
segment a pair of pinnate appendages, on to which are hooked
the packets of eggs; the male, on the contrary, has only one pair
of copulatory stylets in the anterior region of the abdomen.
Now, amongst the parasitized males, one finds female apperr-
dages in all stage~ of development, as is shown by the top series

Figure 64. The abdomen of Inachus mauritanicus showing modi-

fications due to Sacculina (ventral aspect), after G. Smith.
n, normal individuals;p, parasitized individuals: the males in the first row
and the females in the second.

of drawings in Fig. 64. Certain males have the appendages com-

plete and their true sex can no longer be recognized externally
except by the more or less visible vestiges of the copUlatory
stylets. With some of them dissection is necessary and the
information it provides is sometimes of doubtful value on
account of the atrophy of the testes and the vasa deferentia.
Finally, in the genus Inachus the alteration of characters also
extends to the chelre; those of the male are normally much
stronger than those of the female, but in a certain number of
males parasitized by Sacculina, the chelre are feebly developed
and of the female type.
 PARASITIC CASTRATION 203
On examining crabs which had previously carried a Sacculina
and which may be recognized by an annular scar in the former
region of insertion, Smith found some which had originally been
males and in which the gonads, after the loss of Sacculina, were
undergoing regeneration but contained young oocytes; that is to
say, that the gland then had an orientation towards the female
sex.
I shall cite a further analogous case in the crab Eriocheir
japonicus, studied more rece-ntly by Yo K. Okada and Y. Myia-
shita 261 in Japan. Here again, the males parasitized by Sacculina
showed all stages of modification in the shape of the abdomen
and in the development of the appendages of this region, even
to the extent of completely resembling females. The chelre are
also modified in the female direction and, under the influence of
the parasite, the gonads are greatly reduced in those feminized
males, sometimes being changed into an ovary or a hermaphro-
dite gland. It is clear, then, that these cases occur very generally
in the crabs.
If we relate all these facts to what we have said above on
the metabolism of the crab that is parasitized by Sacculina,
we see that in the male, parallel with the deviation in meta-
bolism, the secondary sexual characters are modified in the
direction of the female sex and that this influence may even
extend as far as a modification of the polarity of the genital
gland itself. *
• One can today classify the preceding modifications as cases of intersexuality, as
defined by Goldschmidt 587 and F_ R_ Lillie. The former, working on the genetics
of Lymanlria dispar (this bombycid, as its specific name indicates, shows sexual
dimorphism very clearly), has pointed out that by appropriate crossing of races
one obtains at will individuals showing a mosaic of male and female characters,
that is to say, gynandromorphs, and that these individuals, from the point of
view of the sexual instmcts, are mtermediate between males and females. He was
able to standardize the dIfferent races and, WIth the help of these data and by
crossing two suitably selected races, to obtain an expected degree of inter-
sexuality, extendmg as far as complete sex reversal in one group of individuals.
Evidently a similar state of affairs occurs in Inachus under the influence of
Sacculina. The changes in the crabs are also comparable with the anomalies shown
by a free-martin, explained by F. R. Lillie 590. Such an. individual is the heifer
twin of a male calf, which, since the days of antiquity, has been known to be
sterile, and which, anatomically, is an intersex, showing a varymg mixture of male
and female characters in the genitalia, with a more or less pronounced deviatIon
towards the male sex. Lillie showed that these deviations were the consequence
of a precocious anastomosis WhiCh, in the case of a twin pregnancy, exceptional
in the cow, established itself between the vessels of the fcetal membranes. Thus,
the female embryo, at a very precocIous stage, IS submitted to the effect of male
blood and the hormones it contains. Under the influence of these hormones there
is inhibition of female characteristics and development of male ones.
204 RECIPROCAL REACTIONS OF PARASITE AND HOST
In pagurids carryingPeltogaster, F. A. Potts has also observed
that the males to some extent take on the characters of the
female, without the converse occurring. Giard had previously
noticed that in male pagurids parasitized by an epicarid,
Phryxus paguri, the abdominal appendages often resemble those
of the female. Rathke, half a century earlier, believed that only
female prawns (Leander) were parasitized by Bopyrus. Now,
actually maJ~s are often parasitized as well, but as a result they
adopt the secondary sexual characters of the female, which
misled Rathke.
Cases of this kind are probably rather widespread in the Crus-
tacea but their discovery and analysis demand precise observa-
tions on abundant material. More recently an English zoologist,
B. W. Tucker (1931), has also observed that, in Upogebia litto-
ralis parasitized by a bopyrid, Gyge branchialis, females were not
modified, whereas in the males the chelre and first abdominal
appendage assumed the characters proper to the female. The
genital glands are reduced and more or less feminized. At the
root of all these changes there must be hormonal activities
released or modified by the action of the parasite, which will
doubtless be better known in the near future.
In some homopterous Hemiptera, Typhlocyba hippocastani
and T. douglasi, parasitized by a hymenopteron, Aphelopus
melaleucus, and by a dipteron, Atelenevra spuria, Giard 586
observed a very marked atrophy of the ovipositor in the females
of both species. In males parasitized by T. hippocastani, the
penis is equally reduced.
In plants one may quote the case of one of the Caryophylla..'
cere, Lychnis dioica: in female stems of specimens of this dire-
cious plant parasitized by Ustilago antherarum, the presence of
the parasite has the effect of inducing the appearance of anthers,
which, moreover, are invaded by the fungus.
The numerous examples of a morphogenetic effect produced
by the gonads through a hormonal mechanism clarify the facts
observed in the case of parasitic castration. There is, however,
an apparent paradox in the data relating to crabs and insects.
For in arthropods experimental castration appears to have no
effect on the secondary sexual characters, even when carried out
very early. But within the mechanisms of the two actions
there are evidently considerable djfferences in the conditions.
 SPECIAL REACTIONS 205
Recent data on the endocrinology of the arthropods open up
numerous fertile perspectives in this connection. *

SPECIAL CASES OF REACTION OF HOSTS TO

PARASITES
At the beginning of the chapter we saw that parasites, at least
when they are active, do not as a rule provoke a phagocytic
reaction. But that is not to say that there is never a cellular
response to their presence. One could cite various examples of
such a response.
Around the egg of entomophagous Hymenoptera a sheath is
formed from the cells of the host, forming an epithelial layer,
which very certainly plays an important part in the exchanges
between host and parasite.
The larva of the timbu fly, Cordylobia anthropophaga, causes
the formation of an open cutaneous tumour (furunculous
myiasis) consisting of a neoplastic proliferation of dermal tissue
around the larva. These cells rest on a kind of cellular puree on
which it feeds and which must not be confused with sup-
puration; there is suppuration only if the larva is diseased or
dies, and if the opening of the tumour closes up (Roubaud 317).
In fishes there is a reaction of the same kind around the glo-
chidium larvre of Unionidre. In a few hours they are encased in
a thick vascular cyst, the elements of which are phagocytized by
the pallial cells of the young mollusc. F. H. Reuling 363 observed
the interesting fact that this reaction of the host does not con-
tinue indefinitely. After two or three successive infestations of
Lepidosteus by glochidium larvre of Lampsilis anodontoides, there
is no further reaction and development is unsuccessful. Using
Micropterus salmonoides, the same author was able to obtain
two massive infestations by glochidium larvre of Lampsilis
luteola, but a third was abortive, resulting in abnormal cysts
from which the parasite was expelled after forty-eight hours,
although infestation succeeded perfectly when glochiqium larvre
* As an example which will render this statement more precise, I shall cite a
very curious case studied by Panouse 263. In removing the eye stalks of prawns
(Leander serratus) he not only produced a reaction in the chromatophores but
caused rapid development of the ovary and thus obtained eggs out of season.
There is, in the eye stalk, an endocrine gland which, directly or indirectly, acts
on the growth of the ovary. It is clear, then, that the parasites, in modifying the
hormonal balance, can act on the genital glands and the secondary sexual
characters.
206 RECIPROCAL REACTIONS OF PARASITE AND HOST
from the same batch were used on fresh controls. Immunity is
thus rapidly acquired by the fish, whose serum then destroys, in
vitro, the tissues of the glochidium, while the serum of fresh con-
trols is without effect.
With certain Protozoa we see localized cellular reactions.
Various Coccidia jtnd gregarines cause hypertrophy of one cell
or of a group of cells. Thus Caryotropha mesnili, a coccidian
parasite of the spermatogonia of an annelid, Polymnia nebulosa,
studied by Siedlecki 125, brings about the hypertrophy of the
cell in which it develops, as well as of its nucleus. Some adjacent
spermatogonia can undergo analogous modifications and fuse

B c
Figure 65. Cellular reactions <:>f the host to Coccidia and gregarines.
A, Caryotropha mesnili (after Siedlecki). B, Clepsidrina davini (after Leger
and Duboscq). C, hypertrophy of an intestinal epithelial cell of Blaps
parasitized by Stylorhynchus /ongicol/is (of which only the epimerite-
is visible) (after Leger and Duboscq).

with the first to form a giant multinucleate cell; the rest of the
group of spermatogonia do not develop normally into sperma-
tozoa but remain in the condition of epithelial cells forming a
compact envelope around the parasite. Here, then, is direct
partial castration.
Analogous cases have been observed in various gregarines.
Pyxinia Jrenzeli, a parasite of the intestinal epithelium of larva!
of Attagenus pellio, produces hypertrophy of the host cell,
followed by atrophy (Laveran and Mesnil). Clepsidrina davini,
in Gryllomorpha, causes the epithelial cells of the intestinal
crypts, to which it is attached, to fuse into a syncytium (Leger
 SPECIAL REACTIONS 207
and Duboscq 100). Hesse 93A has pointed out cases of the same
nature in the gregarines of oligochretes: Monocystis agilis and
Rhynchocystis pilosa act on spermatogonia in the same way as
Caryotropha mesnili. Nematocystis magna hypertrophies the
epithelial cell which supports it. These examples of hypertrophy
have sometimes led to mistakes. The genus Myxocystis, des-
cribed as a type of special parasitic Sporozoa in Limnodrilus,
has been recognized as being only a microsporidian parasite of
the lymphocytes or spermatogonia of the worm, causing hyper-
trophy of the parasitized cell and of its nucleus, and the fusion
of several cells into a giant cell. Various Microsporidia, such as
Nosema anomalum in the stickleback (Stempell), Glugea in
Balanus amaryllis (Ch. Perez), and a species that I have myself
studied in the liver of the sand eel, Ammodytes lanceolatus, pro-
duce giant and polymorphic nuclei at the periphery of the
infected area. Stempell 127 considered them to be an actual part
of the parasite with the significance of vegetative nuclei. It is
more probable that they are elements belonging to the host,
hypertrophied and fused into giant cells. In all likelihood the
same applies to the cell with a large nucleus and a brush-like
border which envelops the cysts of Gilruth .in the stomach of the
sheep, studied by Chatton 86. A sporozoan, Selysina perforans,
of obscure affinities, parasite of an ascidian, Stolonica socialis;
and studied by Duboscq 90, also causes the formation of giant
multinucleate cells by the fusion of cells in large or small
numbers.
In the cells of the sabellid Potamilla torelli invaded by Haplo-
sporidium potamillce (frequently accompanied by a yeast, related
to Monospora in Daphnia) there is a proliferation of peritoneal
endothelium into a sort of papilloma (Caullery and Mesnil 380).
One could add to this series of examples, and it is clear that
we are concerned with the effect of substances continuously
secreted by the parasites.

GALL FORMATION
These very localized cellular reactions lead us naturally to a
type of modification due t~parasites and very widely spread in
plants. I refer to galls. There are some analogous formations
in animals which we shall examine first of all. Giard 586 proposed
208 RECIPROCAL REACTIONS OF PARASITE AND HOST
to give them the name thylac~e (8VAaK£ov purse). According to
whether the parasite is animal or vegetable one may say that it
is a question of zoocecids or phytocecids, of zoothylacies or
phytothylacies.
A certain number of sedentary Myzostomaria, on the pin-
nules of crinoids, cause the formation of cavities with a thick,
calcareous wall and a small external opening, within which they
hide. * Similarly, a copepod, Pionodesmotes phormosoma, studied
by J. Bonnier 2,15, forms a true gall in an abyssal sea urchin,
Phormosoma uranus, with a soft test: in contact with it the test
becomes strongly calcified to form a sphere jutting into the
ccelom (Fig. 66) and contrasting with the general frailty of the
wall of the sea urchin. In these galls there is a narrow opening
through which the hypertrophied female copepod cannot pass;
the male, a great deal smaller, must still be able to make its exit.
H. J. Hansen (1902) found a similar case, that of the copepod
Echinocheres globosus on the sea urchin Caliteria gracilis.
Finally, Mortensen and Stephensen 256 have also pointed out
the formation of a gall by a copepod, Astrochordeuma appen-
diculatum, at the expense of an ophiuroid, Astrocharis gracilis.
A crab, Hapalocarcinus marsupialis, modifies the growth of
one of the Madreporaria, Pocillopora caspitosa, by its presence
at the tips of the branches, where it causes the formation of
cavities in which it remains concealed. This case, pointed out by
Semper, has been thoroughly studied by F. A. Potts 267, who
followed out the gradual development of the cavity in which the
crab dwells; a line of openings persists there, ensuring the circu-
lation of the water. Hapalocarcinus modifies other corals, Seria-
topora hystrix and Sideropora, in the same way. Other crabs of
the genus Cryptochirus similarly inhabit cavities in a massive
polyp, Leptoria, where they live in pairs, the male being much
smaller than the female. t
* Analogous malformations in fossil echinoderms show that this type of para-
sitism is ancient. J. Mercier (1936) pointed out that In the sea urchin Collyrites
dorsalis of the Callovian phase, protuberances of the test were caused by galls
produced by a parasite which he placed near Pionodesmotes (= Castexia douvil/ei).
Parasitism by Myzostomaria appears also to be of long standing (Clark, 1921).
t Let us here recall that, as we have already seen, the parasitic gastropod
molluscs (Megadenus, Sty lifer, etc.) also provoke malformations resembling
galls or thylacles on the echinoderms where they hve (Sty/ifer ce/ebensis on the
starfish Certonardoa, Hirase 343; Megadenus arrhynchus on the starfish Anthe-
noides rugu/osus, Ivanov 345; Megadenus cystico/a on the spines of Dorocidaris
liara, Krehler and Vaney 350).
 GALL FORMATION 209
Giard 586 created the term thylacie in connection with indi-
viduals of Typhlocybq parasitized by Aphelopus melaleucus; the
hymenopteron is indeed carried in a voluminous pocket, placed
laterally on the abdomen.
The pocket in the host, Polycirrus arenivorus, where XenocOJ-
lorna is situated, may also be considered as a gall; the presence

Figure 66. A, fragment of the test (inner face) of Phormosoma

uranus with numerous prominent spherical galls, g, of Pion odes-
motes phormosomce. B, interior aspect of one of the galls with
its external opening and the parasite (~) (after J. Bonnier).

of the. parasite causes the tissues of the annelid to undergo

special proliferation and differentiation.
Finally, one may include amongst temporary galls the forma-
tion of the vascularized cyst in which glochidium larvre develop
in fishes, as well as the tumours of the furunculous myiasis pro-
duced by the larvre of the timbu fly.
210 RECIPROCAL REACTIONS OF PARASITE AND HOST

But this type of reaction remains exceptional and is little

developed amongst animals.
On the contrary, galls are of major importance amongst
plants and are as interesting from the physiological point of
view as they are from the morphological one. I shall restrict
myself here, however, to some remarks of a general nature on
this subject.
Animals that produce galls in plants, the cecidozoa, belong
to various groups. The most important are nematodes (helmin-
thocecids), particularly Heterodera; acarines, principally Erio-
phyes and Phytoptus (phytoptocecids); but, above all, the insects.
Almost all the orders include gall-forming types, but those that
play the most important part are the aphids, Diptera (Cecido-
myidre) and the Hymenoptera. Among these last, the Cynipidre
constitute a vast family, attacking species of Quercus by prefer-
ence and supplying data of great interest to the biologist
(parthenogenesis, polymorphism, etc.); the Tenthredinidre and
the Chalcididre have also very great importance as gall formers. *
Galls are formed at the expense of all parts of the plant: root,
stem, leaves, flowers, buds; each gall former produces as a rule
a definite gall on a fixed part of a given plant. There is usually
very strict specificity between gall formers and plants, a speci-
ficity subject, however, to the same vicissitudes as parasitism in
general. Many gall formers attack only one kind of plant and
are monophagous; others are more or less pleophagous, as we
find with Heterodera radicicola and with a chrytridinid, Pycno-
chytrium aureum, that is known on about one hundred plants.
Sometimes, on the contrary, on very closely related species,
gall formers, without being morphologically distinct, constitute
quite separate physiological races. One can cite, for instance,
the case of Isosoma graminico/a, which is represented by two
distinct races on Triticum repens and T. junceum.
The morphology, structure, dimensions and colour of the
galls are as strictly determined as in normal organs. I refer
the reader to the work of C. Houard 402, who has devoted a
considerable amount of work and careful documentation to
a
galls in the French and in exotic floras. There is precise mor-
* True gall formers must naturally not be confused with the commensals and
inquilines which sometimes live there in great numbers. In the galls produced by
Biorhiza aptera (Cynipidre), 79 parasitic species and 11 commensals have been
enumerated.
 GALL FORMATION 211
phology in galls; in general, they are the result of two processes:
cellular multiplication, or hyperplasia, and a hypertrophy of the
cells and nuclei. We have a very striking example of cellular
hypertrophy in the swelling produced by Heterodera radicicolain
the roots of melon, where the nematode causes the formation of
giant cells, sometimes containing as many as 200 nuclei (Fig. 67).
In general, particularly in parenchyma, the tissues have a
clearly'embryonic character; the cells and nuclei are much larger

Figure 67. Longitudinal section of the root of a melon attacked

by Heterodera radicico/a, H; cp, multinucleate cells (after
Molliard).

than in normal tissues; the chlorophyllic apparatus is reduced;

frequently there is production of anthocyanin. From the chemi-
cal point of view, galls are richer in water than normal tissues,
and also richer in soluble nitrogenous compounds, in starch and
in tannin.
The point which here will interest us most is the mecha-
nism of gall production. It must be noted that galls are only
formed on plant organs that are undergoing development, and
212 RECIPROCAL REACTIONS OF PARASITE AND HOST
that they are only formed by animals in the state of eggs or
larvre. The most natural hypothesis-it had already occurred to
Malpighi in the seventeenth century and is generally admitted
today-is that these structures are due to the action on the plant
of irritant substances, deposited in the tissues by the gall-forming
animal either at the moment when the eggs are laid or in the
course of larval growth. These substances must cause nutritive
material to be diverted from the tissues. One sees, moreover, a
general parallelism between the histological and morphological
differentiations which develop in many galls and those which
result from alterations in plant nutrition due to other causes and
which are expressed, for example, by fasciation or virescence of
the flowers. There is also a good deal that is analogous between
galls and fruit, and this must be based on similar conditions of
nutrition when both of them are being formed. Galls would then
be, in short, the plant's reaction to substances inoculated by
the gall-forming parasite, and their morphology would be deter-
mined by the plant's actual constitution. Gall production occurs
only when there is inoculation into a tissue that is embryonic
in character. After that all the correlations which regulate
the development of the plant itself and which intervene in the
formation of new parts, so determining their symmetry, come'
into play but under modified conditions. Thus, a truly new organ
is produced, whose structure and development depend upon
the intrinsic properties of the plant and are thus determined in
advance.
In spite of the apparent adaptation of the galls to the circum-
stances in which the cecidogenous larvre develop and emerge,
the galls must be considered as a characteristic reaction of the
plant, independently of all finality concerning the parasite. If
there had been, evolutionary adaptation of the one to the other,
one could hardly imagine it other than as a modification in the
irritant action of the parasite as, for instance, a variation in
the substances by which the parasite acts on the plant or in
the nature of the action of these substances.
It is only at a recent date that it has been possible to obtain
some experimental results supporting the preceding hypothesis.
The conditions of gall production certainly involve a very
precise causal mechanism which crude experiments cannot
imitate.
 GALL FORMATION 213
Some very suggestive observations and experiments on this
subject were made first of all by Beijerinck 399 on the galls of
Hymenoptera, and more recently by W. Magnus who, in con-
firming the conclusions of Beijerlnck on certain points, never-
theless diverged from him on others.
Beijerinck studied in particular the galls produced on willow
leaves by Nematus (=Pontania, Tenthredinidre). He noted that
when the insect deposited the egg in the wound she had made
in the plant, she also deposited a droplet of liquid secreted by
abdominal poison glands. According to him, it is this liquid that
causes the formation of the gall, for the latter is produced even
if-as sometimes takes place-the egg is not laid and also when
the egg has been killed by means of a needle. Under these con-
ditions the galls do not attain the normal final dimensions, but
one sees them begin to take shape without the agency of the
egg and of the larva. These experiments have been repeated and
verified by Magnus 405 with various species of Pontania, in par-
ticular P. proxima on Salix amygdalina. Magnus even improved
on them by removing the egg from the plant almost immediately
after it had been laid and without injuring it. He was able
to compare the whole course of events in gall production in
the plants thus treated and in others serving as controls,
in which the egg had been left. Now, in those in which the
egg had been extracted the gall formed well but more slowly
and remained smaller. It develops, then, without the intervention
of the egg itself, or of the larva. It is not so in all galls. According
to the experiments of Magnus with those of the Cynipidre
(Rhodites, Biorhiza) the presence of the egg and of the larva is
necessary.
Beijerinck concluded from his experiments on Pontania that
the determining factor is the secretion deposited by this insect
in the wound on the plant. But when the substance in question
was directly inoculated into the leaves of the willow neither he
nor Magnus succeeded in provoking a reaction of the plant, nor
any definite reaction such as that of the natural gall. That
must depend on the conditions of inoculation. The wound
made in the plant by the insect's ovipositor involves a very
great precision so far as the torn tissues are concerned, and,
consequently, of the cells which react. Magnus, then, does not
consider it as absolutely established that the gall is really the
p.s.-8
214 RECIPROCAL REACTIONS OF PARASITE AND HOST
direct result of the action of a definite chemical substance on the
cells of the plant. For him the wound itself is a decisive factor.
He distinguishes, moreover, two stages in the development of
galls: an initial pha~e in which undifferentiated tissues are
formed by cell multiplication, and a second phase in which
these tissues differentiate. The latter, in all galls, 'would be
constantly dependent on the living and developing larva which
acts through its secretory products. An injection, made once,
of a chemical substance would thus not suffice to bring about
the complete development of a gall.
If the secretions introduced by the parasite are indeed the
effective cause of gall formation, the active substance in them
remains to be discovered. It is natural to think of enzymes, and
it has been proved that various eggs and larvre of gall-forming
animals are, indeed, rich in proteolytic enzymes; this fits in with
the fact that galls contain nitrogenous compounds, particu-
larly in the soluble state and not in the form of proteins. In dis-
cussing these problems Magnus arrived at a hypothesis of a
general nature that I give here on account of the analogy that it
suggests with the conditions of parasitism in animals. The pro-
duction of galls would be the result not of the direct action of
enzymes but of that of substances secreted by the gall-forming
animals, which would prevent or delay the action of the
plant's own enzymes. These would be, in other words, anti-
bodies produced by the parasite and introduced by it into the
plant, and these would modify the conditions of cell metabolism.
The specificity of the antibodies would condition the specificity
of the different galls produced by distinct parasites on the same
plant. For the moment this hypothesis awaits confirmation. .
Whatever may be the exact way in which substances inocu-
lated by the parasite act in the production and the differentia-
tion of galls, it is interesting to point out some positive results
obtained recently without the intervention of gall-forming
organisms, by the introduction into the plant of substances
elaborated by the latter. These results are from work by
Molliard and E. F. Smith.
Molliard's experiments 408 were first performed 'on Rhizo-
bium radicicola on the roots of Leguminosre; it was isolated from
the roots of the bean, in ~ pure culture. The culture liquid,
passed through a porcelain filter, finally served as a_ nutritive
 GALL FORMATION 215
medium for peas which had previously been germinated asepti-
cally on moist cotton wool. Controls were grown under the
same conditions but in spring water. Under the influence of the
Rhizobium culture liquid the roots of the peas showed a hyper-
plasia of the pericycle, and hypertrophy of the cortical cells;
but there was no question of a specific action nor of any con-
siderable changes.
More recently, Molliard 410 succeeded in reproducing, at
least partially, the gall which a cynipid, Aulax papaveris, pro-
duces in certain poppies, Papaver dubium and P. rhaas. This
insect is gregarious. There are as many as 50 larvre in a single
gall. Molliard pounded up a batch of these larvre and, with the
aid of a syringe provided with an asbestos filter so as to obtain
a clear liquid, he injected the product of this pounding into the
middle of the stigmatic platform of a flower bud of the poppies,
on the axis of the pistil. The plant was then protected against
all access by the hymenopteron. After some days the treated
flowers showed hypertrophied placentre, the appearance being
remarkably similar to that of the natural gall. But further
stages, subsequent to this preliminary c,hange, were not obtained
for lack of fresh doses of the irritant substance, which, under
natural conditions, must be the better assured and controlled,
the greater the number of larvre.
E. F. Smith 411, in the United States, carried out a series of
researches, parallel to these preceding ones, on crown galls
produced by Bacterium tumefaciens; he caused substances
elaborated by this bacterium to react on the plant. He cultured
the bacterium on a very simple medium. * After culture, this
medium was found to contain formaldehyde, ammonia, amines,
alcohol, acetone and formic and acetic acids. Smith observes that
many of these substances are amongst those which have been
shown to be the most effective stimulants in experimental par-
thenogenesis carried out by J. Lreb. He painted the buds of the
young plant with these substances, or injected them with it. The
plants utilized were cauliflower, castor oil (Ricinus) and
tomato. But, again, the operation could not be repeated con-
tinuously as it would have been under natural conditions. Smith
* Distilled water with 1 per cent. dextrose and 1 per cent. peptone added, and
sufficient calcium carbonate to neutralize the acids formed which inhibit the
development of the bacterium.
216 RECIPROCAL REACTIONS OF PARASITE AND HOST
obtained tumours which remained small and showed hyper-
plasia of the vessels and hypertrophy of the cells. The cells were
more compact than in normal tissue; they lacked chlorophyll.
Their volume became almost a hundred times that of normal
cells. The changes brought about were thus similar to those
which are characteristic of the natural gall.
In short these results, without establishing the complete
development of the galls, are nevertheless sufficient to justify the
hypothesis from which the experimenters set out, particularly if
one takes into accOl,lnt the difference existing between experi-
mental and natural conditions.
Galls may, then, be considered as the specific reaction of the
young tissues of plants to chemical substances introduced into
these tissues by the cecidogenous organisms. The frequency of
galls on plants and their high degree of differentiation, in con-
trast to the rarity of analogous structures in animals, is doubt-
less only the expression of the predominance, in plants, of local
reactions over general ones. That is clear if one considers the
constitution of both of them, and the difference of the physio-
logical relationship between the parts in both cases, and if, in
particular, one envisages the role of the circulatory system in
animals.
 CHAPTER XI

SYMBIOSIS BETWEEN ANIMALS

AND PLANTS

THE last part of this book will be devoted to the study of

symbiosis. This term was created by A. de Bary in 1879, to
designate the intimate and constant association oftwo organisms
with mutual relationships assuring them of reciprocal benefits.
Eve!} if one lives at the expense of the other and can be con·
sidered as a parasite, its metabolism provides the partner with
more or less essential elements. Symbiosis is the extreme form
of mutualism. Once again we see that a strict continuity exists
between all categories of associations of organisms.
The typical example of symbiotic associations as conceived by
de Bary was the case of the lichens, whose nature had just been
established by Schwendener 578. o. Hertwig 416, extending the
conception to certain associations between animals and plants,
defined symbiosis as the common life, permanent in character,
of organisms that are specifically distinct and ,have com-
plementary needs. As I have said above, the delimitation of
symbiosis and of commensalism, or even of parasitism, is not
always easy. One sometimes brings into it associations such as
those of Eupagurus prideauxi and Adamsia palliata which, on
other occasions, one considers as belonging to mutualism,
while restricting symbiosis to cases where union is particu·
lady intimate. The analysis of examples of symbiosis thus under·
stood will show that it is not always purely mutualistic and that
one of the two associated organisms is in reality more or less
parasitic on the other.
There is also a category of facts which, without really
belonging to symbiosis, can be compared with it in certain
respects and which I shall evoke in this introduction. It concerns
the social animals and particularly societies of insects-the
social Hymenoptera, especially the bees and ants, and the
217
218 SYMBIOSIS
termites. These societies are groups in space of distinct
individuals, apparently independent but in reality united to one
another in fl definite fashion, which involves in each one of them
complementary functions, involving for the group as a whole a
definite collective individuality and at the same time modifying
in a definite direction the structure and fate of each individual.
In short, a kind of symbiosis exists between all the members of
the community.
I shall here restrict myself to pointing out some of the chief
features concerned. The dominant one is the division of labour
amongst the associates, localizing certain functions in definite
categories and stamping them by definite anatomical and phy-
siological characters, so that castes are formed, forming a unity
related to symbiosis itself.
In the most typical societies of bees, ants and termites. the
reproductive function, fundamental property of every indi-
vidual under ordinary circumstances, becomes the privilege of
an individual or a caste. Sex itself results from fertilization or
alternatively from parthenogenetic development of the egg,
leading in the first eventuality to the female sex, in the second to
the male. The males have only an ephemeral existence, their role
being limited to the accomplishment of the act of fertilization.
Reproduction becomes the monopoly of a sole female individual,
the queen; but she, on the contrary, is incapable of leading an
independent life or of rearing her progeny. The supplying of
food to this queen and her larVa! becomes the exclusive business
of a numerous caste of male and female workers who come
to be excluded from the reproductive function by reaso!} of
the atrophy of their gonads, this being determined deliberately
by the quality of the food provided for them in the larval state.
Here is a definite and labile mechanism functioning with perfect
regularity, like a laboratory experiment.
I do not wish to enter here into a detailed examination of the
variations of these processes; 'that would lead to a complete
analysis of the life of social insects, which is outside the scope of
this work. I limit myself to remarking that even if they do not
enter into the category of actual symbiosis ,they are con-
nected with it and that is why I have drawn attention to them on
the threshold of the chapters which follow. We shall study sepa-
rately the different types of symbiosis, grouped according to
 ECTOSYMBIOSIS 219
the degree of intimacy of the connections between the asso-
ciates, and with regard to the nature of the latter.
One is led, indeed, by the constancy of the association
and of the relationships between the associates to consider
as cases of symbiosis the regular association of two definite
species without the fusion of individuals with one another; we
shall designate these associations by the term ectosymbiosis, in
contrast to the typical form of symbiosis, where there is inter-
penetration of the two associates with the formation of a mixed
complex, which we shall call endosymbiosis.
Furthermore, separate chapters will be devoted to symbiosis
between animals and plants and that between two plants. In
the first of these two cases one of the associates is always a ..
microscopic orgap,ism belonging to the lower plants (fungi,
algre or bacteria) or to the Protozoa.

ECTOSYMBIOSIS
ANTS AND FUNGI. Our first example of ectosymbiosis is
provided by ass'ociations between ants and fungi. The American
ants of the genus Atta, called leaf-cutting ants, shred ~eaves into
tiny fragments which they pile up, and on these heaps there regu-
larly develops a mycelium whose hyphre are utilized as food by
these ants. Thus the latter habitually establish mushroom
gardens. These associations have been studied in detail by many
eminent naturalists for three-quarters of a century: Belt, Fritz
MUller and his nephew Alf. Moller 498, H. von Ihering 470,
Goldi 451, Huber 464, etc. Exact determinations have been made
of the fungi so cultivated. The most constant is an agaric,
Rhozites gongylophora, that has been found associated with all
species of Atta. Some other fungi belong to the genera Aptero-
stigma and Cyphomyrmex (Xylariacere). It has been observed
that, when swarming, the ants carry bundles of mycelium in
pockets in the hypopharynx and that when new colonies are
first being formed the queen cultivates the fungus; later, this
task is the business of the workers.
TERMITES AND FUNGI. We find analogous cases in the
termites of the family Metatermitidre, and particularly those of
the genus Odontotermes. The termitarium regularly contains a
mushroom garden. This was observed as early as 1779 by Krenig
220 SYMBIOSIS
and in recent decades has been the subject of very numerous
researches amongst which I should like to make special mention
of those of Doflein 442, Petch 508, lumelle and Perrier de la
Bathie 475-7, and Bugnion 431-2, and more recently those of
Bathellier 425, P. Grasse 453, and R. Heim 462.
The fungi develop on "combs" constructed by the termites
with small balls of excreta; they form a mycelium with
, 'spheres "'. The fungi themselves are agarics, which have been
methodically cultivated by R. Heim, who obtained fructifica-
tions; he made the genus Termitomyces for them. But there are
also some Ascomycetes (Xylaria). It was generally agreed that
in the termitarium the fungi were an essential larval food and
that they were indeed cultivated by the termites. The careful
observations of Grasse 452 run counter to this opinion. Accord-
ing to him the termites use the fungi, mycelium or spheres,
for food only in a very accessory way and these are not one of
their basic foods. One cannot allow that intentional cultivation
occurs. The spores are introduced passively with the plant
debris forming the material of the combs. The conditions of
temperature and humidity are at an optimum for the de-
velopment of the fungus. The culture having thus developed
spontaneously, the combs, as Smeathman had already said at
the end of the 18th century, are nurseries where the termites
deposit their eggs, which there find optimum physical con-
ditions; the larvre, however, do not in fact feed on the
fungus. Their mouth-parts would not allow them to tear the
spheres apart and Grasse was able to prove that nearly all the
latter remain intact. They do not constitute a basic food but
have at most only an accessory value.
It is clear, then, that anthropomorphic tendencies have greatly
exaggerated the precision and purpose of the relations between
termites and fungi. Their constant association with Termitidre
is an undeniable fact; in the etymological sense of the term a
symbiosis exists here, but this does not correspond at all to a
close physiological relationship, and one may suppose that it is
the same for associations between ants and fungi.·
OTHER ASSOCIATIONS OF INSECTS AND FUNGI. Other
regular associations between insects and fungi have been dis-
covered. For instance, the beetle Xyleborus (Bostrichidre) makes
galleries in wood, and these same galleries are habitually covered
 ENDOSYMBIOSIS 221
with the mycelium of fungi sown passively by the insect and
utilized as food by its larvre. It is the same with some other forms
that are equally xylophagous, such as the Platypodidre and the
Lymexylonidre (Hyleccetus) and certain Hymenoptera, the Siri-
cidre. Similarly, in the galls produced by certain Cecidomyidre
in Leguminosre, the internal cavity of the gall is also covered
with a mycelium on which the larvre feed. But it is not neces-
sary to let oneself become involved in finalist interpretations of
these associations, constant and definite though they may be.

ENDOSYMBIOSIS
We now come to the cases in which the two associated
organisms interpenetrate and tend to constitute a more or less
perfect morphological and physiological unit, an endo-
symbiosis.
The number of works which relate to this subject has con-
siderably increased in recent years, resulting in an important
increase in our knowledge and a growing precision in the
analysis of the data. One of the workers who has devoted him-
self to it with the greatest tenacity and penetration is P. Buchner,
who, in addition to numerous studies on particular cases
executed by himself or his pupils, has made a profound and
methodical study of it in his book, Tier und Pjlanze in Symbiose
(1930), and Symbiose der Tiere mit pjlanzlichen Mikroorganismen
(1939), containing substantial important evidence which has
been utilized in the following pages.
PROTOZOA AND INTESTINAL BACTERIA. To begin with
we shall examine a class of facts which is provided for us by
cases of the constant presence of lower organisms, protozoa or
bacteria, in the alimentary canal of the host. Properly speaking,
they are there as parasites, but, through being finally absorbed
by the host or through making an effective contribution to its
nutrition by means of their own metabolism, they may constitute
an essential element in its physiological functioning.
Let us note, first of all, in a very summary fashion, the fact
that in various phytophagous insects such as lamellicorns (cock-
chafers) and Lucanidre amongst beetles, and Tipulidre amongst
Diptera, there is in the larval gut a vast dilatation in which bac-
teria swarm. It has been definitely established that these bacteria,
8*
222 SYMBIOSIS
cultured in vitro, ferment cellulose and thus contribute to the
digestion of this substance in the host. The intestinal dilatations
in which they accumulate are, in fact, fermentation chambers.
The precise interpretation of the role of these symbionts in
the physiology of the organism which houses them presupposes
an extremely thorough knowledge of the host's metabolism
which, in general, we are far from possessing. I shall cite, as a
typical example, the case of the hemipteron, Rhodnius prolixus,
which is the subject of some remarkable researches by Wiggles-
worth 547; the following quotation, which appears to me to be
very suggestive, is borrowed from a recent work by this author
(1948, p. 743): "But the normal Rhodnius always harbours in
its gut a symbiotic bacterium, Actinomyces rhodnii, which is
essential for the nutrition of its host; apparently, it produces
certain vitamins of the B group which are deficient in blood. If
Rhodnius is reared under sterile conditions so as to be freed
from its Actinomyces, it goes into a state of diapause and will not
grow beyond the fourth or fifth instar. Perhaps the vitamins
synthesized by this micro-organism provide the raw material for
the production of the moulting hormone." These few lines
give an idea of the very numerous and important problems,
which are also very complex, that arise out of the facts of
symbiosis in insects and also in other groups. We shall come to
them again in the pages that follow.
INTESTINAL FLAGELLATES OF TERMITES. A particularly
striking example is furnished by the flagellates that swarm in the
alimentary canal of termites, except in those, the Metater-
mitidre, that cultivate fungi. These flagellates are large and highly
differentiated (Polymastigina, Hypermastigina). They have been
the subject of very many papers; amongst recent ones I shall cite
those of Kofoid, Swezy, Cleveland, Hungate, Pierantoni and
Grasse. The hind-gut of the termites forms, as in the cases men-
tioned above, a voluminous sac (especially in the workers) con-
taining a thick, milky liquid in which flagellates and bacteria
abound.
The experimental analysis of the role of flagellates in termite
digestion was carried out in a particularly precise and brilliant
way by Cleveland 435, 436, working on a series of species of
American termites from California and Panama, etc. Each
species ,of termite has its special flagellate fauna and more than
 FLAGELLATES IN TERMITES 223
40 species of these flagellates are known. Their presence is essen-
tially linked up with the digestion of wood. Of the four families
of termites, three (Mastotermitidre, Kalotermitidre and Rhino-
termitidre) are xylophagous and provided with intestinal flagel-
lates, the fourth (Termitidre sensu stricto) being neither xylo-
phagous nor carrying flagellates.
The flagellates, by invagination at their posterior end (Fig. 68),
engulf the particles of wood filling the gut of the termite and
digest them. The termites finally feed on the flagellates them-
selves. The flagellates are thus true symbionts and it is thanks
to them that the termites are able to live indefinitely and repro-
duce on a diet comprising only wood and cellulose (in the form
of cotton wool, for instance). Cleveland established this fact by
breeding experiments carried out for eighteen months and more.
These experiments were made principally on Californian species,
Termopsis angusticollis and Reticulotermes clavipes.
That flagellates are indispensable is shown by experiments on
defaunation. They can be completely eliminated in the following
ways: (1) by incubation, which consists of maintaining the ter-
mites at a temperature of 36° for twenty-four hours; (2) by total
fasting for a sufficient length of time; (3) by oxygenation, that is
to say by placing them in pure oxygen under pressure. By this
last method the death of some species of flagellates results in
30 to 40 minutes when there is a pressure of 35 atmospheres of
oxygen, or in a few days at ordinary atmospheric pressure. * The
termites are resistant for a much longer period; oxygen is forty
to fifty times more toxic to the flagellates than to the termites
themselves.
Different flagellates vary in their resistance to oxygen, so that
by suitably arranged experiments one can eliminate at will this
or that species amongst those that are to be found at anyone
time in the gut of the termite. Thus, in Termopsis there are four
species of flagellates, Trichonympha campanuia, Leydiopsis
spharica, Trichomitis termitidis and Streblomastix strix. By com-
bining defaunation methods of fasting and oxyg~nation, Cleve-
land was able to rid the termites of anyone of these species, or
all four, and finally by submitting the corresponding termites to
• Cleveland carried out analogous defaunation experiments on parasitic intes-
tinal protozoa (CIliates, flagellates) in cockroaches, earthworms, frogs, urodeles
and goldfish. At a pressure of 3'5 atmospheres the cockroaches were resistant for
ninety hours, while their intestinal protozoa died in three and a half hours.
224 SYMBIOSIS

Figure 68. Flagellates in the rectal sac of termHes.

A, JfEnia annectens; B, Trichonympha chartoni; C, Spirotrichonympha
k%idi; D, Oxymonas projector; E, Trichomonas trypanoides; F, Pyrso-
nympha vertens (A-C, E,Fafter Duboscq and Grasse; D, after Kofoid
and Swezy; taken from Noirot and Alliot. Note the particles of
wood within flagellates A-D.
 FLAGELLATES IN TERMITES 225
a definite diet, particularly to one of wood or cellulose, and
seeing whether they could survive under normal conditions, he
was able to determine the part played by each species of
flagellate.
Here let us only say that in the total absence of flagellates the
termites rapidly die off; the same happens if Streblomastix is the
only species in the gut. With Leydiopsis and Trichonympha they
live. These two species are thus true symbionts which, by their
own metabolism, ensure the nutrition of the termite. Analogous
experiments carried out with Reticulitermesflavipes have shown
that the presence of the flagellates is strictly correlated with the

b c
Figure 69. Ingestion of wood by Trichonympha campanula, a
flagellate in the gut of termites (after L. R. Cleveland).
Ingestion takes place by the invagination of the posterior extremity which
engulfs the wood particles.

absorption of wood by the termites. There are, indeed, some

castes which, when adult, lose the ability to shred wood owing
to the structure of their mouth-parts. Correlated with this
there is a loss of flagellates from the intestine; these non-xylo-
phagous castes must then be nourished by other members of the
termitarium.
Interest in these researches of Cleveland has since been revived
by several workers. Let us cite here the observations made by
Pierantoni, who by means of stains analyzed the contents
of the cytoplasm of flagellates and found mitochondria there,
and, furthermore, some symbiotic bacteria which, accord-
ing to him, would hydrolyze the carbohydrates of wood into
226 SYMBIOSIS
soluble sugars. Thus there seems to be symbiosis at two levels
in the termite-flagellate association.
The gut of the termite itself contains numerous free-living
bacteria which must contribute to its nutrition by fixing nitrogen
in the form of proteins.
Termites deprived of their flagellates soon die but may be
saved by being provided with fresh flagellates either by direct
ingestion or by feeding them on the freces of their congeners.
Experiments of this kind have been made by various authors
on lamia annectens and Mesojrenia annectens in Calotermes
flavicollis, and on Trichonympha minor and T. agilis in Reticulo-
termes lucifugus; they confirm the earlier researches of Cleve-
land 437 and of Montalenti 500. Hungate 465-468 has studied the
metabolism of the flagellates in vitro and established that they
digest cellulose; according to him, as well as Pierantoni, while
they are digesting wood in the termite gut they produce sub-
stances such as assimilable glucose which is a source of energy
for the termite. Furthermore, the termite thus consumes the
oxygen which would be fatal to the flagellates. There is, then,
clearly an effective biological symbiosis between the two asso-
ciated organisms. By quantitative experiments in Zootermopsis
Hungate came to the conclusion that on the whole, one third
of the soluble products of digestion is produced by the activity
of the termite and two thirds by symbiotic Protozoa.
How this symbiotic association between termites and flagel-
lates is brought about is what Grasse and Noirot (1945) have
sought to determine in detail. The facts vary somewhat accord-
ing to the groups of termites. In a general way it is possible to
distinguish two types of excrement in these insects, one solid or
sticky and lacking flagellates, and the other liquid and teeming
with these organisms. This last is the proctodeal food. Under the
influence of various stimuli exercised by its congeners, the termite
empties its rectal pouch, and this liquid food is greedily eaten
up. Furthermore, during larval moults and, in Cryptotermes, the
imaginal moult, almost all symbiotic flagellates pass to the ex-
terior. The fresh contamination of individuals defaunated ,by
their moult is achieved by the ingestion ofproctodeal food ejected
by a non-defaunated termite. After this, a large proportion of
the ingested flagellates are digested, which represents an impor-
tant contribution of proteins to the consumer.
 INFUSORIA IN RUMINANTS 227
The preceding statements, although very summary, show that
the termite-flagellate association, while presenting at first sight
all the signs of simple intestinal parasitism, is in reality an effec-
tive physiological symbiosis.
INFUSORIA IN THE PAUNCH OF RUMINANTS. Verte-
brates provide us with some cases of associations which are

Figure 70. Ciliates in the paunch of ruminants (after Doflein).

A, Entodinium caudatum. n, Ophryoscolex caudatus. M, macronucleus;
m, micronucleus; p, peristome; v, contractile vacuole.

analogous to those above; Protozoa or bacteria regularly live

and multiply in the digestive tube of vertebrates and by their
own characteristic physiological activity playa role in digestion
as effective as that of actual food.
The most striking of these cases is that of the ruminant
228 SYMBIOSIS

mammals, but there are analogous instances in other forms such

as the horse, certain rodents (hamster, guinea-pig), and even in
the anthropoid apes.
First of all, let us consider the ruminants. Everyone knows
how their stomach is differentiated into a series of successive
chambers (rumen, reticulum, psalterium and abomasum). In the
rumen, where ingested and triturated vegetable matter first
accumulates, there habitually occur considerable numbers of
ciliates which are of large size, highly differentiated and
belonging to the Ophryoscolecida! (Ophryoscolex, Diplodinium,
Entodinium), the Isotrichida! (Isotrichia) and Enchelidre (Butsch-
lia). Ferber enumerated nineteen species of these ciliates in
sheep. Their numbers have been estimated at about 100,000
per cubic centimetre. This ciliate population is established in
the rumen as soon as lactation ceases, infestation taking place
by means of cysts which had previously been cast out with the
excreta. The rate of reproduction is considerable (at least one
division every twenty-four hours); nevertheless their final num-
bers remain approximately constant. They must therefore either
be regularly evacuated with the freces or digested by the host,
thus providing the latter with a constant and important contri-
bution of proteins. The ciliates themselves live on vegetable
matter contained in the rumen, that is to say, on starch and
on cellulose. This nutrition has recently been the subject of
much work. Trier 542 has shown that the ciliates incorporate
and digest starch for the most part, but also green cell pro-
ducts. Dry straw, on the contrary, does not suit them;. the
rumen of a ewe fed on dry oat straw for four weeks becomes
completely emptied of ciliates. The residues left by their diges-
tion of cellulose are perhaps utilized by the ruminant.
Among the most recent researches on these questions are
those of Hungate 466. He cultured one of these ciliates, Diplo-
dinium (=Eudiplodinium) neglectum, in a medium obtained
from grass and mineral salts and he was able to maintain
these cultures for twenty-two months, in the absence of oxygen
and at a suitable osmotic pressure. These protozoa are strictly
ana!robic. Hungate succeeded in extracting from these cultures
an enzyme that would digest cellulose. This cellulase is at
its optimum activity when the acidity of the medium corre-
sponds to a pH of 5'0, which is equivalent to that of the internal
 INFUSORIA IN RUMINANTS 229
medium of these protozoa. Glucose is the final product of cellu-
lose digestion; an intermediate product is cellobiose, with a corre-
sponding enzyme, cellobiase. From this it follows that Eudiplo-
dinium is in fact an auxiliary agent in ruminant digestion
and that a true symbiotic relationship exists here. Experiments
by other workers show, however, that ruminants defaunated of
ciliates digest almost as much cellulose as those where they are
present in the rumen.
Furthermore, from the rate of reproduction of these ciliates
in cultures, Hungate has calculated that the proteins with which
they provide the host, through themselves being digested,
amount to about 20 per cent. of the ruminants' requirements in
these substances.
Hungate extended the preceding results to the culture of other
species found in the rumen: Eudiplodinium maggii, Diplodinium
(=Polyplastron) multivesiculatum, D. (=Anoplodinium) denticu-
latum and Entodinium caudatum. The first three of these species
also digest cellulose, but not the fourth, nor, moreover, species
of Isotrichia or B1Uschlia. Species of Diplodinium alone, then,
must be regarded as true symbionts.
These results, like those from the work of numerous other
authors (Schwartz, 1925, 1926, Ferber 447, Mangold and his
pupils), the details of which we cannot go into here, show the
complexity of the relationships between the ruminant and its
ciliate popUlation, relationships which may partly be considered
as symbiosis, partly as parasitism.
In the horse the crecum is populated by ciliates and these by
themselves represent a notable contribution of protein. In the
hamster the 'stomach is subdivided into two chambers and
the one next to the resophagus contains ciliates belonging
to the same types that occur in ruminants. In anthropoid apes
the ciliates are localized in the large intestine, and Reichenow
(1920) was able to show that they digest cellulose there, and
after mUltiplying very considerably are finally absorbed by the
host.
ROLE OF BACTERIA. In addition to the role of ciliates in
digestion in these various mammals, bacteria must also be taken
into account. Symbiotic activities have been shown to occur with
them too. Amongst the researches carried out on this subject I
shall cite those of J. Pochon 525-526, who, working on ruminants,
230 SYMBIOSIS
isolated and maintained a pure culture of a cellulolytic bac-
terium, Plectridium cellulolyticum, from the rumen. The cultures
were made in a medium as close as possible to the content of
the rumen, and, in particular, anrerobic. Plectridium cellulolyti-
cum is motile, rod-shaped, ciliated, gram positive, and a faculta-
tive anrerobe; the optimum temperature for its culture is 40° C.
It is only cellulolytic under anrerobic conditions. It is capable of
fermenting various sugars and alcohols under anrerobic con-
ditions; in anrerobic culture it is peptidolytic but not pro-
teolytic. '
Similar questions which arise in certain birds have recently
been dealt with by Mangold and his pupils. In the grain-eating
birds (fowls, pigeons and doves, and forest passerines) there are
paired intestinal creca, of greater or lesser extent, which are
absent in birds of prey. In these creca bacteria assist in the
digestion of cellulose.
ZOOCHLORELL£ AND ZOOXANTHELLlE. A classical and
widespread example of symbiosis is that of zoochlorellre and
zooxanthellre-unicellular algre that are regularly found in the
cytoplasm of various protozoa and in the tissues of inverte-
brates belonging to different groups.
The constant occurrence of green or yellow corpuscles in the
tissues of certain invertebrates was pointed out as early as 1850;
their interpretation as intracellular algre was proposed by Cien-
kowsky434 in 1871, then by Gesa Entz 444 and K. Brandt 428 ; it
was confirmed in particular by Beijerinck 556 in 1890 and by
Dangeard 440. Nevertheless, this opinion was opposed for quite
a long time, notably by E. Ray Lankester. An excellent sum- .
mary of these discussions is to be found in a resume of the sub-
ject which we owe to Bouvier 427.
The yellow bodies (zooxanthelhe) are met with in marine
animals, the green ones (zoochlorellc£) principally in freshwater
organisms. Here are some examples of animals where the¥ are
present:
PROTOZOA. Various naked amrebre (Amceba viridis) and also
shelled ones (Difflugia piriformis, D. nodosa); some Foramini-
fera (Trichosphc£rium sieboldi, Peneroplis pertusus, etc.). A large
number of Radiolaria, notably the Spumellaria (Collozoum,
Sphc£rozoum), and Heliozoa (Acanthocystis, Actinosphc£rium,
Heliophrys, etc.); flagellates (Anisonema viridis, Noctiluca,Lepto-
 ZOOXANTHELLlE AND ZOOCHLORELLlE 231
discus); very numerous ciliates (Paramecium bursaria, Frontonia
leucas, Ophrydium versatile, Stentor polymorphus, Trichodina
patellce, etc.).
SPONGES. Spongi/la viridis.
CCELENTERATES. Hydra viridis, Halecium ophiodes, some
medusre (Cotylorhiza, Sarsia, Rhizostoma), some Siphonophora
(Velella, Porpita), Milleporina, Alcyonaria (gorgonians), Hexa-
corallia (numerous sea anemones), etc.
CTENOPHORA. Euchlora.
TURBELLARIA. Convoluta, Vortex viridis, etc.
ROTIFERA. Ascomorpha helvetica, Itura aurita, etc.
ANNELIDA. Eunice gigantea.
BRYOZOA. Zoobothrium.
MOLLUSCA. Tridacna, Elysia viridis.
The plant nature of these yellow or green bodies, which are
generally spherical with a diameter of 3 to lO/-L, is seen in the
following characters:
1. In structure they are like a unicellular alga: one can actu-
ally recognize a cellulose membrane, a chromatophore which
occupies most of the cytoplasm, a pyrenoid, a nucleus (visible
on staining). There are also starch grains and metachromatic
corpuscles.
2. Their presence is not invariable in most of the cases cited
above. If, indeed, there are some species that are always found
to be infected, such as Hydra viridis, Convoluta, etc., and some
that are nearly always infected, such as Paramecium bursaria,
and Ophrydium versatile, there are others that are only incident-
ally so, or only in certain localities. Individuals of Noctiluca, for
instance, contain zooxanthellre in the Indian Ocean but not in
our seas. Trichodina patellce, heavily infected on the Normandy
coast (Cape de la Hague), is never so at Wimereux.* Thus it
cannot be said that these bodies are organites indispensable to
the species in which they are found. '
3. It has been possible to observe the process of infestation
of the species in which they occur. F. Ie Dantec 487 is noted for
having done this in the case of Paramecium bursaria, after taking
the necessary precautions. After passing a green individual
through several lots of filtered water he crushed it so as to set
• There is a tendency nowadays to regard the species of Trichodina living on
Patella in the two places as distinct.
232 SYMBIOSIS
the zoochlorellre free and then took aParamecium from a colour-
less culture and placed it in the drop containing them. Under
the microscope he watched the ingestion of the zoochlorellre by
this ciliate. They were not digested and he saw them mUltiply by
dividing into four. After a few days the individual Paramecium,
which had been colourless to begin with, was green. Schewia-
koff made an analogous observation with Frontonia leucas, but
.Famintzin 4,,6 contested its authenticity. Doflein 82 has
infested Ammba vespertitio with chlorellre of Frontonia.
Awerintzeff has similarly infested Dileptus anser with those from
Stentor viridis. There are also the experiments carried out by
Pringsheim on the zoochlorellre of Paramecium bursar/a; he was
able to reinfect the ciliates after having blanched them.
4. They can survive for a long time outside the species that
harbours them, as was shown notably by Cienkowsky, Brandt
and Schewiakoff.
5. Their division, very easily seen today in stained material,
was first seen in vivo by numerous observers, namely Beijerinck
and Famintzin. The latter tried to get them to multiply outside
the ciliates. He was only successful after many difficulties. To
do this he crushed a green Paramecium between a slide and a
coverslip. The zoochlorellre tended to adhere to the coverslip
under which he passed a drop of saline (containing 1/1,000 of
potassium acid phosphate and 1/1,000 of ammonium sulphate).
In this medium he saw two successive qmidruple divisions, with
an intervening period of growth.
6. One can deprive the animals of their algre, blanch them,
either by keeping them in darkness for a long time, where tliey
will cast them out, or by a method described by Whitney 545 for
Hydra viridis, which consists of adding 0·5 to 1·5 per cent. of
glycerine to the water containing them. The individual Hydra
blanched in this way flourishes and produces buds; it is
interesting to note that it does not become reinfested when
placed in an aquarium containing green hydras.
They are then indisputably autonomous algre. Beijerinck iden-
tilies the zoochlorellre with a free-living alga, Chiarella vulgaris,
which he has been able to culture in water to which has been
added 8 per cent. gelatine, 0·8 per cent. peptone, 0·2 per cent.
asparagine, and 1 per cent. cane sugar; it is one of the Proto-
coccacere. He once succeeded in culturing zoochlorellre extracted
 ZOOXANTHELLJE AND ZOOCHLORELLJE 233
from ciliates; the culture set up was maintained without diffi-
culty, and was shown to be identical with the free-living'
Chlorella. Famintzin verified these results for free-living
Chlorella which he cultured in saline, as well as for the zoo-
chlorellre of Paramecium bursaria. The zoochlorellre of different
animals are, moreover, not necessarily all of the same species.
Genevois 449 succeeded in culturing the zoochlorellre of various
turbellarians (Dalyella viridis, Typhloplana viridata, Castrata
viridis) and identified them as Chlorella vulgaris. According to
Chodat433 the cultured algre belong to Protococcus and resemble
a species, P. ophrydii, isolated by him from Ophrydium versatile.
Chodat, as we know, was a great specialist in culturing the
lower algre in vitro.
The zooxanthellre are said to be Cryptomonadinere. Schau-
dinn 535 places those from Foraminifera in the genus Crypto-
monas (C. brandti in Trichosphcerium sieboldi, C. schaudinni in
Peneroplis pertusus). Keeble 479 considers the green bodies of
Convoluta viridis to belong to Chlamydomonas, characterized in
the flagellospore stage by four flagella and a stigma.
In the Metazoa natural contamination often occurs even in
the egg, as Hamann observed in Hydra viridis in 1882. It is thus
a hereditary infection. Hadzi 457 saw this same transmission by
the egg in another hydroid, Halecium ophiodes; the zooxan-
thellre, which tint the endodermal cells brown, pass into the
developing oocyte. In the same way there is regular contamina-
tion of the egg in Millepora, according to observations made
by Mangan 490.
But, according to the researches of Keeble and Gamble 478,
in Convoluta viridis, where the algre are constantly present, it is
otherwise. The young individuals of Convoluta, on leaving the
cocoon, are colourless; but green bodies exist on the surface or
in the interior of the cocoons. It must be noted, too, that workers
(Georgevitch, Sekera, von Graff) who have studied the embry-
onic development of Convoluta have not observed the green
bodies during the development of the embryo. By taking young
individuals of Convoluta as soon as they hatched and rearing
them in carefully filtered water Keeble was able to keep them
in a colourless state for a month, while those that were kept in
ordinary sea water became green. By adding green individuals
of Convoluta to a culture that had remained colourless the latter
234 SYMBIOSIS
turned green in three days. When the embryos have hatched,
the empty cocoons become filled after three weeks with small,
green, quadriflagellate bodies (Carteria, a subgenus of Chlamy-
domonas). It follows that Convoluta is infected by green bodies
not with the structure of the adult, but in a flagellate state
which is a great deal smaller and very difficult to see.
According to the observations of Brandt and Famintzin, the
young individuals of Collozoum have no xanthelhe and con-
tamination must be made by very small flagellospores which
have not yet been seen; but once they have reached the state of
yellow bodies in the ciliate or radiolarian, reproduction takes
place by binary or quadruple fission. It seems to be the same
with Trichodina.
Let us consider the nature of the relationships between zoo-
chlorellre or zooxanthellre and their hosts. Clearly there is, in
general, a symbiosis profitable to both. Brandt 428 in particular
has developed this conception. The algre are said to find
effective protection in the animal and to lodge in it in such a
way as still to receive light. Zooxanthellre are particularly com-
mon in pelagic animals with a transparent surface (Radiolaria,
medusre, Ctenophora, etc.); they find carbonic acid in the
animal cell, which is rare in the superficial layers of the sea. On
the other hand, they release oxygen, aiding the respiration of the
animal tissues. They produce starch, which may be utilized
by the animal; or else, since this reserve substance may only be
formed in an insoluble state, the soluble and assimilable pro-
ducts which lead up to it may be directly utilized. The animals
which normally contain yellow or green bodies (Radiolaria,
Convoluta) thus no longer feed directly, but indirectly on the
products of the synthesis performed by their symbiotic algre,
and the latter, on the other hand, can only with difficulty live
in isolation and freedom. Thus there is constituted a new bio-
logical unit, the phytozoon. '
As early as 1889 Famintzin opposed many of Brandt's con-
clusions. According to his observations, and contrary to what
Brandt said, the Spumellaria (Collozoum, etc.) directly ingest
solid prey (even copepods) with the help of their pseudopodia,
not only when they are young and lack xanthellre, but even when
they are adult. And when they are starved, the radiolarians with
xanthellre survive for a long time by digesting the xanthellre
 ZOOXANTHELLJE AND ZOOCHLORELLJE 235
themselves. The starch which has sometimes been observed in
radiolarians comes from these resorbed xanthellre. It is the same
with sea anemones, according to Famintzin. Most animals with
chlorellre or xanthellre lose their colour after a certain time if
they are kept in darkness (ciliates, Hydra and sea anemones
can be decolourized in this way), their algre being cast out in a
brownish and half-digested condition.
Similar conclusions were reached by Keeble and Gamble
working on Convoluta. These authors observed, first of all, that,
contrary to the accepted opinion, this turbellarian ingests solid
bodies (diatoms, algre, spores, bacteria), at least when it is young,
by means of a ventrally situated mouth in the posterior region,
which leads into the parenchyma. It feeds independently and
not by means of the green bodies. There is evidently profound
adaptation of the green bodies to Convoluta. According to
Keeble, the green cells are finally incapable of a free-living
existence, their cell wall atrophies and their nucleus degenerates.
Under normal co.nditions they live thus, but under conditions
of famine they are digested by Convoluta. The relations between
the animal and its green cells are considered to be complex by
these authors, and cannot altogether be described as a symbiosis.
Keeble states that the green cells act as a sort of excretory
system for Convoluta. The relations between green cell and
animal change with their development, passing from a sym-
biotic relationship to one in which the animal is parasitic on the
algal cells.
It follows from all these facts that the association of algre and
animals is not invariably a true symbiosis and that in certain
circumstances the animal lives as a parasite at the expense of its
algre.
Let us note finally that in addition to zoochlorellre and zoo-
xanthellre some Cyanophycere have regularly been found in
certain Protozoa, principally in the rhizopod Paulinella chroma-
tophora, where they are present as curved and elongated
forms. Pascher (1929) maintained these organisms in vitro,
where they divided successfully.
MYCETOMES OF INSECTS. We now come to another cate-
gory of associations between animals and the lower fungi (or
bacteria), which take very various forms and have been princi-
pally studied in recent decades. We shall first examine one of the
236 SYMBIOSIS

earliest known examples of these, the interpretation of which

has gradually become more precise. These are the structures
which are generally known as mycetomes in insects.
It is many years sin~e these mycetomes were first observed,
but they received a definite interpretation only in 1910. As early
as i858 Huxley 469'described in aphids a rather variable organ
situated in the abdomen beside the ovaries (Fig. 71 m), with cells
crammed with inclusions that were generally spherical, resem-
bling ~, vitellus; hence the name pseudo vitellus given to this

Figure 71. Larva of a green-fly, Drepanosiphum platanoides,

showing the green body or mycetome, m (after Balbiani, taken
from Henneguy).

structure. Balbiani 424 studied it a little later and gave it the name
of pseudova, or green body on account of its pigmentation. He
saw, besides, that it was derived from a particular structure,
constantly to be found at the posterior pole of the egg and called
by him the polar mass. Metchnikoff 496 followed out its whole
development and called it the secondary vitellus. This body,
which has been seen by numerous observers, gave rise to the
most diverse hypotheses until its true nature w(!.s established
independently and almost simultaneously by Pierantoni 510 and
Sillc 540. In the inc1usio~s of the green bodies, these authors
 MYCETOMES OF INSECTS 237
recognized yeasts or blastomycetes (Schizosaccharomyces aphi-
dis), which appear thus as living habitually in a stable relation-
ship with the aphids.
Analogous structures were already known in the Coccidre,
and had even been correctly interpreted. They were pointed out,
indeed, by Leydig 489 about 1850, studied by Metchnikoff and
other workers, and it was Putnam who, in 1877, recognized that
they contained plant elements, and this was confirmed, ten years
later, by Moniez 499. In 1"895 Lindner formally identified yeasts
in the coccid Aspidiotus nerii. Vejdovsky (1906), Conte and
Faucheron 439 independently gave the same interpretation,

''''1-;~',
'.~.
:>:.,~.,,:
...
:',';?
',j}
-- co
, .0 .B

Figure 72. Symbiotic yeasts and mycetocytes in Homoptera

(after Pierantoni).
A, two sections showing the penetration of the yeast corpuscles, co, into
the developing oocyte of Icerya purchasi. B, embryo of Icerya
purchasi with its mass, co, of embryonic corpuscles. C, a mycetocyte
of Dactylopius citri, with corpuscles in the form of crescents.

which Pierantoni confirmed by relating them to analogous

structures in the aphids.
Apart from these two groups and under different forms simi-
lar structures occur in the Aleurodidre (where Signoret perceived
them in 1867), the PsyUidre (where they were pointed out by
Metchnikoff), the cicadas and the Cicadellidre.
Let us take a first glance at these facts by studying them in a
coccid, Icerya purchasi, as Pierantoni did, and by following out
the insect's development. In the ovary, at the posterior pole of
the developing oocytes, about a hundred spherical bodies
(Fig. 72A, co) are regularly present; they are very easily stained;
they also occur elsewhere in the general body cavity, and, more
238 SYMBIOSIS

abundantly, in the cytoplasm of large cells forming yellowish

organs situated on' either side of the intestine and limited by a
flattened epithelium. In these organs the corpuscles in question
are actually dividing. Thus they form, at the posterior pole of
all the eggs laid, a constant or polar mass like that seen by
Metchnikoff. At the beginning of embryonic development this
polar mass is enveloped by special cells, called mycetocytes by
Sule; they first adhere to the blastoderm, then fall into the
vitellus. They attach themselves then to the germ band (Fig. nB);
finally they come to be situated dorsally, in the posterior region
of the embryo, 'and divide into two masses, placed on the sides
of the proctodreum, and these will become the yellow bodies
pointed out at the beginning of this description. While this is
taking place the blastomycetes are actively mUltiplying; the
mycetocytes become enormous; their compressed nuclei are
irregular in shape. Although they are crammed with these fungi,
the mycetocytes live and flourish, continuing to divide mitotic-
ally. This mass of cells with their blastomycetes constitutes the
mycetome.
Pierantoni extracted the mycetome of the animal, dissociated
it, and placed the fragments in an 8 per cent. solution of gelatine
to which 20 per cent. beet sugar had been added. At the end of
four days, during which the medium was kept at a temperature
of 15° c., he obtained colonies of saccharomycetes, which he
considered to have been derived from the intracellular bodies,
with a type of budding characteristic of yeasts, even thougb in
the mycetocytes the elements multiply by equaJ division. These
yeasts are rerobic and, moreover, the yellow bodies are abun-
dantly supplied with trachere.
The blastomycetes in the cells are not always spherical; thus,
in Dactylopius citri, they appear as crescents in each mycetocyte
(Fig. nc, co) and are united in clumps in the intracellular
spheres.
The blastomycetes occur in male embryos as well as in female
ones, but in the male the mycetome gradually vanishes.
Buchner 430 completed the investigation by making a direct
study of the mycetome in the different groups of insects cited
below and his observations coincide with those of Pierantoni.
He studied aphids (Drepanosiphum), Coccidre (Lecanium corni),
Aleurodidre (Aleurodes on the maple), Psyllidre (larva of the
 MYCETOMES CONTAINING FUNGI 239
willow psyllid), cicadas (Cicada orni from Japan and Liberia),
and Cicadellidre (Aphrophora salicis). From them he extracted
various blastomycetes, the taxonomic descriptions of which are
given in his memoir (genera Saccharomyces, Oospora, Kermini-
cola, Coccidomyces, etc.), with a note of the cultures that were
made of them. These observations were extended and systema-
tized in his general work 3.
The mycetome shows different arrangements which Buchner
classifies as follows:
1. The least differentiated is that of certain Coccidre, Jassidre
and Fulgoridre, where the blastomycetes are situated in cells
dispersed in the fat body without differentiation of a localized
mycetome (Lecaniidre, Diaspidre). The presence of blasto-
mycetes is none the less constant, whatever may be the source
of the individuals.
2. The second stage is that where there is a differentiated
mycetome (Aphididre, Aleurodidre, Coccidre, Icerya purchasi,
Dactylopius citri) enclosing a single form of blastomycete
(monosymbiont species).
3. Certain species are disymbionts, harbouring simul-
taneously two types of blastomycetes, one in dispersed myceto-
cytes, the other in a differentiated mycetome (in Cicada omi),
where all the cells are fused into an enormous multinucleate
syncytium in the meshes of which the blastomycetes are
situated.
4. Both forms of blastomycetes of a disymbiont species dwell
in two distinct superimposed mycetomes (Cicadellidre, Ptyelus
lineatus).
5. The two mycetomes of the preceding case are fused into
one (Liberian cicada, Psyllidre).
6. Finally, it is possible for three species of blastomycetes to
exist simultaneously, two in a mycetome, the third in a dispersed
mycetocyte (Psyllidre) or even in the same mycetome (Aphalara
calthre).
Whatever the various topographical complications may be,
the general characteristics common to all cases are that infection
is absolutely constant in all localities; that it is transmitted from
one generation in the course of oogenesis; that it is localized
during development in definite cells which finally come to con-
stitute a special organ with a definite structure and position.
240 SYMBIOSIS
The presence of the· mycetome in all the insects enumerated
above is correlated with a way of life that is c'ommon to them,
that of sucking the juices of their food plants.
What, now, are the physiological relations of the blasto-
mycetes and their hosts? All the evidence goes to show that the
former exer,cise no adverse influence on the latter; they have
absolutely no significance as pathogenic organisms. It is no less
evident, moreover, that they find a favourable culture medium
in the mycetocytes as well as excellent means of disseminating
themselves through the reproduction of their hosts.
Sillc put forward the hypothesis that the blastomycetes might
play a part in the breaking down of urates. Pierantoni has
different views. The constancy and precise localization of the
blastomycetes in whole groups of insects' indicate to him that
they fulfil an important physiological function in the host's body.
Now, all the insects in which they are to be seen, and primarily
the aphids, feed on plants from which they extract considerable
quantities of sugary substances and starch. The aphids cannot
even make use of all the sugar they ingest and reject large quan-
tities of it in the form of honey dew; we have seen the relation-
ships which have been established on this account between the
aphids and ants. According to Pierantoni, the blastomycetes
produce enzymes which help in the digestion of sugar, and
they themselves find excellent conditions for nutrition through
the presence of sugar in the tissues. The trachere of the myce-
tome may serve both for supplying oxygen to these rerobic
organisms, and for dispersing carbonic acid. The constant asso-
ciation of blastomycetes with these insects, the character of the.
preceding relationships, and their regular transmission during
oogenesis, constitute for Pierantoni the characteristics of a
physiological hereditary symbiosis.
OTHER EXAMPLES OF SYMBIOSIS IN INSECTS. Numerous
examples of symbiosis between insects and lower organisms,
Protozoa or bacteria, are now known and have been more or
less thoroughly investigated. Work on these problems has multi-
plied in recent decades and has gradually become more precise.
It is not always easy to distinguish a true symbiont from struc-
tures that really belong to the organism containing them. The
essential and distinctive criterion is their culture in vitro; but the
difficulty in this case is to eliminate other organisms of a
 MYCETOMES CONTAINING BACTERIA 241
commonplace character and to be certain that one is indeed
culturing the presumed symbiont.
A first group of facts, which are, moreover, rather numerous,
relates to insects with burrowing larvre which feed on leaves,
seeds, wood or putrefying debris. The symbionts are localized
I in a more or less well-defined fashion within a mycetome of
variable structure. They are usually transmitted from one indi-
vidual to another by contamination ofthe egg, as we saw above.
Such is the case with Dacus olea (Trypetidre), a parasite of the
olive, in which there arise from the gut, in front of the proventri-
culus, four large diverticula swarming with bacteria (Bacterium
savastonoi, Ascobacterium) that also occur in lesions produced
by the insect on the tree. .
Keilin (1921) has also discovered a bacterial symbiosis in a
dipteron, Dasyhelea obscura (Ceratopogoninre), a parasite of the
elm. Symbiosis is intracellular here, as the researches of
Stummer showed. Similar facts are now known in several
families of Coleoptera: Anobiidre, Cerambycidre (where the
symbiotic organism is a saccharomycete), Curculionidre, Bupres-
tidre, Lyctidre and Cucujidre. I shall mention, in particular,
among the very numerous researches carried out on insects,
those of W. Schwarz (1924) on the mycetome of aphids and
Coccidre, in which the various morphological and physiological
aspects of the problems df symbiosis are clearly brought out in
the light of experiment and culture.
One long-discussed case is that of the bacteroids, which are
regularly found swarming in certain cells of the fat body in the
Blattidre. First pointed out by Blochmann 426, these structures
have been interpreted by several authors (Cuenot, Henneguy,
Prenant) as kinds of crystalloids having only a purely external
resemblance to bacteria. Mercier 494, on the other hand,
regarded them as truly symbiotic bacteria and gave them the
name of Bacillus cuenoti; he found them again in the embryo.
By extracting them from embryos still enclosed in oothecre,
taking meanwhile the most rigid precautions against con-
tamination, he succeeded in culturmg them. Javelly, repeating
the experiments, did not, however, obtain any culture and con-
sidered that Mercier had cultured an impurity from the surface
of the ootheca, probably Bacillus subtilis. Buchner, on the con-
trary, believed that it was clearly a question of symbiotic
242 SYMBIOSIS
bacteria which are 'to be found in various Blattidre, indigenous
and exotic. Contamination occurs early in development, by
means of the eggs. This example shows how difficult these
problems are.
The ants provide us with the same kind of data, here, too,
pointed out in the first place by Blochmann (1884) in Campo-
notus ligniperdus, then in Formica fusca. Here it is the cells of
the intestinal wall that are invaded by bacteria. Strindberg
(1913) studied this tissue and concluded for his part that he was
dealing with mitochondria; but Buchner, who repeated this work
with various species of Camponotus, thought that true symbionts
were present; contamination takes place by precocious infection
of the oocytes and is thus also produced in the workers.
Let us note here that apart from insects the same kind of
thing occurs in a prosobranch mollusc, Cyclostoma elegans. As
early as 1858 Claparede studied concretions in' one of its glands,
and Garnault, in 1887, described large cells there, regularly con-
taining, in addition to the concretions, numerous bacteroid
structures. Mercier repeated the work and agreed with Garnault
in considering them to be true bacilli. From the gland, he
obtained a culture in which the elements appeared to be iden-
tical. Recent work (1933-1936), notably by Buchner, has estab-
lished that it is, indeed, a question of bacteria and that here
there is true symbiosis. This has also been found in various other
species of Cyclostoma and in related forms (Annulariidre),
particularly Tudora putre in Cuba and Chondropoma rubrereticu-
latum in Haiti. Symbiotic bacteria have also been found in the
excretory organs of various oligochretes (Lumbricus terrestris)
and Hirudinea (Hirudo medicinalis, Ha!mopsis sanguinea).
Let us remember, too, the authentic existence of symbiotic
fungi in the kidney of Molgula (compound ascidian). Pointed
out by Lacaze-Duthiers, they were studied by Giard and named
Nephromyces by him. More recently, they have been the subject
of research by Buchner at Naples. This worker succeeded in
observing the formation of zoospores and of gametes, but did
not manage to obtain a culture of them, nor to see the onset
of infection in Molgula. The affinities of the fungus are still
uncertain (Oomycetes, <;hytridia1es or Ancylistales).
EXAMPLE OF SYMBIOSIS IN BLOOD-SUCKING ANIMALS.
We hav~ now another series of facts about symbiosis correlated
 YEASTS IN BLOOD-SUCKING ANIMALS 243
with a definite type of life, that of animals feeding on the
blood of vertebrates.
The first example of this kind is provided by a fly, Glossina.
Roubaud 534 studied its symbiotic yeasts, which had already
been pointed out by Stuhlmann. In the adult tsetse fly there is
an area of thickened epithelium in the mid-gut which shows,
macroscopically, greyish spots or bands. Sections at this level
show cells three to five times higher than those nearby, and thus
forming extensive papillre. They are packed with bacillary struc-
tures, 3 to 5t-t in length. These elements, on being freed by the
breaking down of the cells, fall into the lumen of the intestine.
Smears show that they multiply by a budding typical of yeasts
and Roubaud relates them to the Cicadomyces of Sille. The cells
that contain them are then true mycetocytes and these structures
occur with unfailing regularity in all the species of Glossina
studied by Stuhlmann and Roubaud. The latter found them also
in larvre and followed their fate through to pupation. In the
larva, which lives in the maternal uterus, the mycetocytes are
localized at the level of the proventriculus. Roubaud supposes
(without being able to give formal proof) that the yeast is trans-
mitted from one generation to the next, either by the egg, as in
the Hemiptera, or, preferably, by the maternal lacteal secretion
since he has not been able to find any trace of it in the oocytes.
These elements are not abundant in the larvre; they multiply
in the adult when digestion becomes active. Roubaud relates
their presence to the strictly hrematophagous diet of Glossina.
In support of this theory, he makes the observation that one
finds neither yeasts nor mycetocytes in the Stomoxydinre to
which Glossina is related phylogenetically, nor in the Tabanidre,
the Culicidre, larvre of Auchmeromyia, nor species of Lyperosia,
all forms which are not strictly hrematophagous. On the con-
trary, in the Pupipara, a group which is quite distinct in origin
from Glossina but, like it, adapted to strict hrematophagy,
one again finds, by a remarkable instance of convergence,
mycetocytes and yeasts. This was shown by the researches
of Sikora on Melophagus and those of Roubaud on Liptotena
and the Hippoboscidre. Observations of the same nature
have been made on Lynchia maura and on Ornithomyia avi-
cularia, which live on birds and the Nycteribidre (a family of
bats).
244 SYMBIOSIS

There must be then, according to Roubaud, a close correla-

tion between strict lirematophagy and the presence of intestinal
symbionts: the enzymes of the yeasts must facilitate digestion
of proteins and corpuscles of the blood. This suggestion of
Roubaud's finds support today in the fact that a whole series
of symbioses has been found to occur regularly in various other
hrematophagous types. Such is the case with certain Hirudinea
such as Placobdella catenigera and Piscicola geometra, where
the symbionts are situated in the resophageal diverticula. The
same is true of I1-umerous acarines (Gamasidre, Argas, Ornitho-
darus, Ixodes), where the organisms are localized in the mal-
pighian tubes and the intestinal epithelium. These acarines are,
moreover, the vectors of pathogenic organisms (notably
Rickettsia), and propagate diseases such as spotted fever, etc.
The presence of symbiotic micro-organisms thus appears to be
at least a very widespread condition in the animals that live
on the blood of vertebrates.
We find it again in lice (Pediculus humanus capitis, P. humanus
corporis, Phthirius pubis), where it has been studied particularly
by Buchner, and also in insects that feed on keratin, such as the
Mallophaga which live on the feathers of birds (e.g. Dipleurus
baculus on the turtle dove, also studied by Buchner).
ANIMAL LUMINESCENCE AND SYMBIOSIS. Another class
offacts shows a close correlation between symbiosis and animal
luminescence. The latter appears in many different cases to be
determined by the action of symbiotic bacteria transmitted from
one generation to the next.
But it is by no means true to say that all the phenomena
of luminescence originate from symbiosis. There are, first of
all, those which are due to occasional contamination by lumi-
nous bacteria and which fall into the category of simple para-
sitism. Thus we see the decomposing bodies of fishes become
luminescent through certain saprophytic, bacteria developing in
their tissues. Such bacteria can infect the living animal. Thus
Giard and Billet (1889), having found some luminous indi-
viduals of Talitrus (Amphipoda) on the sea shore, recognized
that it was a case of bacterial infection. By cutting,an antenna
on a slide, collecting a drop of the blood and inoculating other
individuals of Talitrus, they saw the latter become luminous,
and were able to repeat the experiment again and again. They
 LUMINESCENCE AND SYMBIOSIS 245
cultured the bacterium itself in a pure state and obtained
luminous cultures. There could be no question here of symbiosis.
It is simply a case of infectious parasitism.
The luminescence of a freshwater prawn, Xiphocaridina
depressa, observed by Yasaki 549 in Japan, belongs to the same
category. This worker recognized that it was caused by a patho-
genic bacterium (vibrion), which could be easily cultured, and
on being inoculated into other Crustacea or insects rendered
them luminescent but killed them rapidly.
Similarly, Issatchenko 471 was able to culture Bacterium
chironomi, which makes chironomids luminous. He observed
some swarms of these insects which were entirely luminoJIs; the
insects rapidly died off and the infection must have been pro-
duced in the larval stage.
Leaving these cases of accidental infection on one side, we
come to those in which luminescence is a normal phenomenon
in a species, either permanent or intermittent in character. One
of the c.hief initial investigators into this phenomenon was
Raphael Dubois. It is necessary in these cases to distinguish
between two categories of facts: luminescence may be an
intrinsic property of the animal or else caused by a symbiotic
bacterium. To the first alternative belong the marine Protozoa,
such as Noctiluca; other planktonic inverfebrates; various
luminous insects, notably the Elateridre such as the cucujo,
Pyrophorus noctiluca, of the Antilles, studied by Dubois; various
abyssal fishes and probably also a bivalve mollusc, Pholas
dactylus, which discharges a luminous liquid into one of its
siphons. In this last animal Dubois was able to isolate two sub-
stances in solution, one being luciferin and the other an enzyme,
[uciferase. The mixing of the two solutions produces light
and these facts have since been extended and confirmed by
Newton Harvey 459. On this basis, Dubois tended to generalize
about the interpretation of animal luminescence. But another
theory, based on many precise researches, has been developed
by Pierantoni, according to whom luminescence in many of the
animals showing it is due to the existence of a constant
symbiosis with photogenic bacteria. He was led to this inter-
pretation by his researches into the mycetomes of insects.
One may admit that both conceptions are valid according to the
cases concerned. The demonstration of luciferin and luciferase
p.s.-9
246 SYMBIOSIS

would be an argument in favour of the first, their absence a pre-

sumption in favour of the second.
Let us now lopk at the facts invoked in support of the
symbiotic interpretation. Pierantoni 511-513 was, first of all,
struck by the parallelism between the structure of the luminous
bodies in Lampyris (a glow-worm) and that of certain mycetomes
of aphids (Aphrophora). In the former animal the luminous
organs are constituted by a parenchyma the cells of which are
crammed with little bacteriform corpuscles possessing the stain-
ing characteristics of bacteria. Furthermore, the egg of the glow-
worm, which is also luminous, contains the same bacteroids.
Starting with the luminous organs of Lampyris, Pierantoni
stated that with peptone agar he obtained cultures of two
different bacteria, but he does not say whether the cultures were
luminous. It remains extremely difficult to affirm that the organ-
isms cultured are indeed the intracellular corpuscles seen in the
first place. The interpretation of luminescence in Lampyris
noctiluca as the result of symbiosis is not generally accepted. It
is firmly opposed by various highly qualified workers, notably
Vogel (1922), Trojan (1929), Novikoff (1939), etc.
LUMINOUS CEPHALOPODS. But the Italian author deve-
loped his researches principally with cephalopods. He has
shown, first of ail, from the morphological point of view, that
there is an intimate tie between the organs known as the acces-
sory nidamental glands and the luminous organs near the anus
and the ink sac. These glands have, in reality, no connection
with the formation of the egg shell and do not emit an actual
secretion. They exist in general only in the females, where they
are next to the true nidamental glands, but they are found also
in the males of certain species (Loligo forbesi). In their most
simple form (Loligo) they consist of a mass of epithelial ducts
embedded in connective tissue, and, within the lumen of
these ducts, a mass of granulations is always to be seen, which,
according to Pierantoni 514, 517, are the bacteria which he
succeeded in culturing. In cuttlefish the structure of the accessory
nidamental gland is complex; indeed, it comprises ducts of three
different colours (white, yellow and orange-red), filled with
bacteria different in appearance in each of the three cases (cocco-
bacilli, bacilli and cocci). There are also many bacteria in the
epithelial cells and the connective tissue. They are said to be
 LUMINOUS CEPHALOPODS 247
present on the surface of the egg when it is laid, and between the
layers of the shell. They would thus be transmitted from one
generation to the next, would be localized and would multiply
in the accessory nidamental gland, which would be a specific
receptacle for them. Cultures of these various bacilli have
been obtained (the bacteriological study was made by Zirpolo)
and those from the yellow ducts are luminescent. Now,
Pierantoni has observed that in female cuttlefish at the mating
season the ventral surface is luminescent, a fact that had not
been noticed earlier.
Let us consider the cephalopods with ventral luminous
organs. Pierantoni was able to study them under favourable

Figure 73. Sections of luminous organs.

A, of Rondeletia minor; E, of Sepio/a intermedia (after Pierantoni);
ep, epidermis; Ie, lens; pg, pigment; rf, reflector; sf, luminous
substance.

circumstances in the Sepiolidre, in which these organs were dis-

covered rather recently (in Rondeletia, Sepiola, Sepietta
oweniana). The accessory nidamental gland (present only in the
female) has just two kinds of ducts (white and red). The light
organs (Fig. 73) which, in the female, occupy the central part
of the gland, are formed of yellow ducts. It seems very probable
that the light organs are a specialized part of this gland in which
the yellow ducts are concentrated. In addition, there is a
reflector below, formed at the expense of muscular tissue, and,
above, a lens develbped from connective tissue. The' ducts of
the light organ, greatly dilated (Fig. 73B), are packed with a
finely granular mass, composed, according to Pierantoni, of bac-
teria and constituting the actual luminous substance. Taking
248 SYMBIOSIS
the most careful precautions, Pierantoni and Zirpolo obtained
cultures which they considered to originate from these cor-
puscles. In cuttlefish broth they form a white film, magnificently
luminescent and emerald green, which illuminates the whole
liquid when it is stirred.
Pierantoni stresses the precautions employed against con-
tamination and the differences in appearance between the cul-
tured bacteria and those luminous ones which are commonly
to be met with on the skin or muscles of cuttlefish and of dead
fish. He concll\des, then, that the luminescence of the Sepiolidce
must be due to symbiotic bacteria localized in the light organ,
which must itself be a result of the differentiation of the accessory
nidamental gland of cuttlefish and squids.
He found that this light organ functions in two ways: by
internal illumination of its substance (symbiotic bacteria), or by
the emission of the contents of its ducts into the surrounding
water, which then itself becomes luminous. The photogenic
bacteria are transmitted from one generation to the next when
the eggs are laid.
There would thus be a hereditary physiological symbiosis
which is probably very general; the Italian author has also
attempted to undertake research into the luminous organs of
deep sea cephalopods, unfortunately difficult to obtain in good
condition. First of all, he made observations on a species
(Charybditeuthis) collected at Messina. The luminescent kernel
of the photogenic organs here" serait toujours constitue par des
cellules remplies de microorganisms transformes par adaptation
a la vie intracellulaire". This interpretation is based on the
study of fixed and stained material. It was not possible to make
cultures and the intracellular situation of the corpuscles con-
sidered as bacteria inevitably raises questions which will
be considered later on. More recently (1924, 1926), Pieran-
toni 519 was able to carry out similar researches m{ an abyssal
myopsid cephalopod, Heteroteuthis dispar; there, 1'00, in a ven-
tralluminous organ occurring in both sexes he found corpuscles
which, according to him, are bacteria.
These various results have, moreover, given rise to rather
lively controversies sustained by several Italian workers
(Puntoni, Mortara 501, Skowron) who dispute the reality of the
bacterial character of the corpuscles in the luminous organs,
 LUMINESCENCE IN PYROSOMA 249
but Pierantoni's conclusions have been confirmed through
independent research by other authors, notably G. Meissner 493,
who obtained cultures of Vibrio pierantonii (starting with the
light organ of Sepiola intermedia) and Coccobacillus pieran-
tonii (from that of Rondeletia minor); moreover, she bases ber
own conclusions on serological data (the finding of antibodies,
etc.). Let us also briefly note the researches carried out in Japan
on Watasenia scintillans by Shima 538, who obtained cultures of
vibrios. These results have, however, been disputed by
Hayashi 461.
We cannot enter here into furtber details on luminous organs
of cephalopods and the discussions which have arisen on the
subject of the reality of symbiotic bacteria. Let us mention that
Buchner gives his support to Pierantoni's conclusions. '
LUMINESCENCE IN PYROSOMA. Problems similar to those
in cephalopods arise in connection with other types of luminous
animals; let us first examine the case of Pyrosoma. The members
of this genus are pelagic tunicates whose transparent colonies,
in the fotm of hollow, cylindrical masses, intermittently give out
a brilliant light, which bas long been known. As early as 1804,
Fr. Peron 507 described the impressive spectacle of this phos-
phorescence of the sea in the Australian Pacific. In each mem-
ber, or blastozoid, of the colony the light organs form a paired
mass on either side of the entrance to the branchial cavity. The
structure and origin of these organs has been thoroughly inves-
tigated by Julin 473-474, beginning with the egg. The point of
origin is in the "test cells" which, in all the tunicates, form
a special envelope round the egg. These are the cells which
give rise to the light organs of the first individuals of the colony,
budded off by the embryo (cyathozoid). The egg itself is luminous
and it is the test cells that shine. Within these cells are
numerous sausage-shaped bodies that Julin interpreted as
mitochondria or chromidia. The study of this material was
repeated by Pierantoni 518, who confirmed Julin's descriptions,
but who regards the intracellular elements noted above as sym-
biotic light-producing bacteria. The test cells are myceto-
cytes which go to form the light organs of the first individuals
of the colony. Pierantoni saw corpuscles within these cells
forming spores, which are passed out and go to contaminate
other mesenchymatous cells; these new mycetocytes, carried by
250 SYMBIOSIS

the circulating blood, will constitute, step by step, the light

organs of the various blastozoids as they are formed by budding.
Moreover, in collaboration with Zirpolo and by taking the most
careful precautions against contamination, Pierantoni was able
to obtain agar cultures of bacterial colonies from the myce-
tocytes. Here, again, there is the obvious objection that it is
very difficult to guarantee the perfect sterility of extracts from

Figure 74. Cells of luminous tissue from Pyrosoma giganteum

with photogenic bacteria (after Pierantoni).
A, luminous cell free in the peripharyngeal sinus, x 1,500. B, the same in
the light organs with spores being formed, x 1,500. C, embryonic
luminous cells with corpuscles undergoing multiplication, x 1,500.
D, formation of spores in the corpuscles, x 2,000.

the light organs, when the cultures are started. When this possi-
bility is taken into account, the conclusions of Pierantoni and
Zirpolo still remain very plausible and they are supported by
Buchner.
The salps are equally luminescent. Buchner has found that in
this group there are symbionts in the cells of the young embryo.
LUMINESCENCE IN FISHES. We know of many cases of
luminescence in fish where the light organs are very varied and
 LUMINESCENCE IN FISHES 251
often highly differentiated, involving reflectors and lenses, and
localized in very different regions of the body. Many of these
luminous fishes are abyssal and accordingly remain practically
outside the possibility of bacterial study. But it has been possible
to deal with these problems in some more accessible species, for
instance, in the Anomalopidre (Anomalops, Photoblepharon)
living in the waters of Pacific atolls, where they have been the
subject of research by Newton Harvey 460. The light organs in
these forms are at the periphery of the eyes. Illumination is con-
tinuous but can be masked by a palpebral fold. The structure of
the organ shows a system of glandular ducts whose cavities are
crammed with luminous bacteria arranged in chains, which can
be cultured on peptone agar.
In Java, Harms 458 found similar structures in a fish, Equula
splendens. Here the luminescent organ forms a ring in the
resophagus at the entrance to the stomach, and it is furnished
with a reflector; the glandular ducts are crammed with bacilli-
form bacteria.
Finally, the luminescent organs in a fish, Monocentrus
japonicus, of the Japanese coasts, have been described by Yo K.
Okada 505; they are continuously luminescent, are situated in
the anterior region of the mandibles and are analogous in
structure to that found in the Anomalopidre: a tubular gland
with an external opening whose cavities are crammed with
highly mobile bacteria (I·5 to 3ft) possessing flagella (vibrios).
If the organ is squeezed, a luminous liquid is squirted out.
Yasaki 550 was able to obtain cultures of these bacteria.
So far, it has not been possible to study the luminous abyssal
fishes when they are alive. From the structures seen in preserved
material it seems clear that many of them have their own source
of light, independent of symbiotic bacteria.
LUMINOUS TERRESTRIAL ANIMALS. In addition to the
work of R. Dubois, mentioned earlier, we should cite that of
Pierantoni who, in his research on the glow-worm, Lampyris
noctiluca, has shown clearly thflt there are corpuscles shaped
like rods or cocci, which he interprets as luminous symbionts.
These bodies occur again in the eggs, which are also luminous,
indicating a regular transmission of symbionts from one genera-
tion to the next. Dubois, it is true, considers these structures as
being not autonomous organisms but intracellular particles
252 SYMBIOSIS

(vacuolides).'Pierantoni obtained cultures on peptone agar, but

they were not luminescent. Pierantoni's interpretation has
excited contradiction (Vogel5 44, Vonwiller), and Buchner
remains uncertain of the nature of the particles in question,
whose culture leaves room for doubt.
Discussions of the same nature were aroused over the pheno-
menon of an oligochrete, Microscolex phosphoreus, emitting a
luminous mucus, whose very body becomes luminescent under
the influence of various stimuli. Pierantoni described symbiotic
bacteria in the tissues, which Cuenot had already observed in
Eisenia rosea and interpreted similarly, while Willem and Minne
considered them to be products of cellular activity. Some
researches by Knop in Buchner's laboratory have led to similar
conclusions. Finally, Skowron, who took the matter up again in
Microscolex phosphoreus, was able to induce luminescence in
these particles, but he did not consider them to be bacteria and
thought that their luminescence resulted from the luciferin-
luciferase reaction of Dubois.
In short, the question remains unanswered, at least in its
general form, and we do not know whether luminescence in
animal tissues is due to the properties of particles actually
belonging to the cell and setting up reactions that bring into play
both an oxydizable substance and an enzyme, or whether it is a
property of symbiotic bacteria.
EXPERIMENTAL RESEARCH ON SYMBIOSIS. It has been
apparent from the mass of data presented in the preceding
pages, very much abbreviated in form and by no means exhaus-
tive, that symbiosis between the Metazoa and the lower plants,
fungi or bacteria, extends over a very vast field and often raises
very complex experimental problems. In a general way, this
symbiosis exists under conditions that are strictly limited. In
numerous cases it occurs in a specialized organ, the mycetome,
formed from particular cells, the mycetocytes, and this organ
develops by a series of equally well-defined processes. There,
we find adaptations whose origin poses, as is always the case,
problems of extreme difficulty. What has brought about the
establishment and permanence of these associations which have
become characteristic of the organism concerned, and are as
precise and stable in their final structure and morphogenesis as
the other elements concerned in the structure of the species?
 EXPERIMENTAL RESEARCH 253
The symbionts in each species are clearly defined; even the
number of mycetocytes is fixed. There are some insects, as
Buchner recognized, which possess two or even several species
of symbionts. The respective proportions of these species are
constant, the numbers of mycetocytes corresponding to each
of them being fixed. The host organism appears as a precise
regulating mechanism of symbiosis, capable in certain cases of
eliminating the symbionts at a definite time by expUlsion or by
lysis.
After a purely descriptive period of researches into these
symbioses we now come to an experimental phase. A series of
investigations of this kind has been undertaken in recent years.

r·
A B c
Figure 75. LarVa! of Sitodrepa panicea ten weeks old.
A, without symbionts. B, without symbionts but fed on dried yeast.
C, control of the same age provided with symbionts (after Koch,
taken from Buchner).

We have already seen a brilliant example in the experiments

carried out by Cleveland and Hungate on flagellates in termites.
To close the present chapter I shall briefly indicate some very
suggestive results.
The type of experiments which is enjoined is to bring about
the suppression of the symbionts and see the consequences
which arise therefrom. This has been done with the larva of
a weevil, Sitodrepa panicea, living on 'flour; its symbionts are
yeasts localized in intestinal creca and the larva becomes infected
at hatching by ingesting the symbionts deposited on the external
surface of the egg when it is laid. It is thus sufficient to sterilize
this surface before the larva hatches, for instance by immersing
9*
254 SYMBIOSIS
it for some moments in a solution of sublimate. By doing
this, A. Koch 481 obtained sterile larvre, which he reared
on an equally sterile food. The consequence was that the growth
of the larvre was almost totally checked. Fig. 75A shows such a
larva at the age of ten weeks, C being a control larva hatched
and reared under normal conditions, and B another sterilized
larva, but one which has been fed on dried yeast; this food is
physiologically equivalent to the symbionts and larvre reared
on it develop in a way that is comparable to that of normal
larvre, undergoing pupation and developing into a reproducing
adult. The yeast provided as food contains B vitamins, which
must normally be provided by the symbionts. The positive role
of the latter is thus clearly shown. It must be the same in the
Anobiidre, the Cerambycidre and other families of beetles.
It would, however, be dangerous to generalize too rapidly, as
witness the case of the cucujid beetle, Oryz«philus surinamensis,
in which the symbionts are localized in cells enclosed in the
general body cavity. Koch 482 succeeded in suppressing the
symbionts in the egg, in the young larva, or even in the adult
females, simply by keeping the insects at a temperature of 36° C.
Animals sterilized in this way remained able to reproduce and
Koch was able to obtain a series of generations in which typical
mycetocytes occurred in their normal position, but were of
smaller size and empty. This example explains how it is that one
occasionally finds, in nature, individuals, or even races, in which
the mycetome is empty. This was observed in an Egyptian race
of the beetle Calandra granaria (Curculionidre) which had
become used to it. Similarly, in an ant, Formica rufa, individuals
born parthenogenetically of workers, ordinarily sterile, possess
a mycetome but no symbionts. In this case the existence of the
mycetome shows that its formation is a process impressed by
heredity on the morphogenesis of the species and not suppressed
by the absence of symbionts.
I shall also mention the very elegant experiments made
by Aschner and Ries 423 on the body louse, Pediculus humanus
corporis. In lice the mycetome is localized in a dorsal diverti-
culum of the foregut. One of these insects is placed on a slide
and compressed very lightly with a mica coverslip pierced
with a tiny hole, the insect being placed so that the mycetome
lies exactly under the hole in the mica. The skin is' then pierced
. RESEARCH ON PEDICULUS 255
with a fine needle and, by pressure, the diverticulum containing
the mycetome is forced outside and can be cut off. Lice so
treated and deprived of the mycetome no longer feed, and ovary
and eggs degenerate. If blood is injected into them by the anus it
is still impossible to save them, although they recover if they are
similarly injected with yeast extracts or bacterial filtrates. The
results of these experiments show that under normal conditions
the symbionts must provide the insect with vitamins that are

.;.z_;..;!!::::!10.._...._ _ _ e
r;q.....:..A-~~....,.::~_m

Figure 76. Louse, Pediculus humanus capitis, 5i!.

e, stomach; m, area of the stomach where the primary rpycetome (here
removed) is situated; m', epithelium of the ovarian ampulla con-
taining the secondary mycetome; m(]!, ovular mycetome (at the base
of the egg, (]!).

not present in the blood and it is possible that here is the deter-
mining cause of the general presence of a mycetome in various
types of hrematophagous animals. The blood that they absorb
does not provide all the substances that are necessary to them,
particularly vitamins.
These few indications suffice to show how fruitful experi-
mental researches, such as have begun to be developed in the
course of recent years, may become in the realm of symbiosis.
 CHAPTER XII

SYMBIOSIS AMONG PLANTS

THE LICHENS. We now come to symbiosis in plants. The most

classical case is that of the lichens. It is so complete that it has
produced plants with a characteristic and well-defined appear-
ance, from which it was possible to make a coherent classi-
fication and structural study without the dual nature of the
plants being suspected, so much so that this last idea was vigo-
rously opposed for a long time.
All lichens result from the association of a fungus and alga.
The mycelium (hypha) of the former forms the colourless part; it
is generally an ascomycete, rarely a basidiomycete. The exact
origin of these fungi is most often still unknown: with a certain
number it has been possible to recognize the family to which
they belong (Xylariacere, Hysteriacere, Patellariacere). The algre,
or gonidia, are most often Protococcacere, sometimes Chroo-
lepidacere; often there is association with Cyanophycere. On the
vegetative portion the reproductive organs are differentiated,
which are either pure fructifications of Discomycetes and
Pyrenomycetes, or similar fructifications into which the alga has
penetrated and which are then termed apothecia. The spores of
the fungus can begin to germinate alone, but the young thallus
very quickly ceases to develop if it does not meet with the
suitable alga.
In addition, many lichens propagate by special organs called
soredia. These are little spherical masses composed of the alga
surrounded by some hyphre. Thus, the association is complete
from the start. The soredia are formed in special organs.
Lichen associations, like all those already discussed, bring
to mind the question of specificity. This is generally strict. It
happens, nevertheless, that the same fungus can accommodate
itself to several very different algre. With each one it then gives
a distinct lichen. Thus Moller 571 showed that a fungUs belonging
to the Basidiomyceres produced a lichen, Cora, with an alga of
. 256
 LICHENS 257
the genus Chroococcus, and a Dictyonema with an alga of the
genus Scytonema. Both lichens can even develop side by side in
the same thallus by parabiosis. Conversely, the same alga can
form different lichens with various fungi; a lichen can even
transform itself into another by the progressive substitution of
the fungus, a process which has received the name of allelositism.
These heterogeneous associations may be localized at limited
places on the same lichen. They then form what are called
cephalodia. Thus, on the lower surface of Solorina saccata, a
lichen with green gonidia, one sees rounded structures, visible
to the naked eye, which are associations of hyphre and Cyano-
phycere.
The dualism of lichens was discovered in 1867 by Schwen-
dener 578. Bornet 561 established the precise anatomical relation-
ships of the gonidia and hyphre. It remained to constitute a
lichen by culturing both components separately and then uniting
them. But isolated cultures of the alga or fungus are very diffi-
cult to make and at that time culture methods were inadequate.
Reess, Stahl and Moller made contributions to this synthesis,
which was achieved in 1889 by G. Bonnier 560 from pure cultures
of both elements; fructifications were obtained on the resulting
lichen. It would be interesting to repeat this demonstration
today with the purity of culture that we can now attain.
The dualism of lichens is now universally recognized. Never-
theless, even in 1913, the Finnish botanist Elfving 565 sought to
show that the hyphre were capable, on their own account, of
producing gonidia and that these, when once formed, could live
isolated in the algal condition. But if dualism is no longer
seriously in question, the relations between t~e two components
are still subject to discussion. The basic fact is that there is a per-
manent union between them and that from this there results an
individualized organism with its characteristic and well-defined
morphology and physiology, and that the two constituents have
great difficulty in living in isolation. Thus we have a collection
of data that clearly corresponds to the idea of symbiosis.
But is it necessary to see in it a perfectly mutualistic sym-
biosis, as is generally believed, each of the components
being a source of balanced and reciprocal advantages for the
other? To affirm this it is essential to know thoroughly the
nutrition of the two plants both in an isolated state and in their
258 SYMBIOSIS AMONG PLANTS
common life. Now, this knowledge is still very incomplete and
the association has so far been regarded in very diverse ways,
which can be summarized under the three following headings:
1. The fungus lives as a parasite at the expense of the alga.
2. The alga is a parasite of the fungus.
3. The association is a mutualistic symbiosis.
1. Schwendener was a partisan of the first theory, which he
developed on lines of imagery. The fungus is the master, the
green algre are the slaves: he goes on to say that it envelops them
as the spider envelops its prey, with a close network of threads
which is gradually transformed into an impenetrable sheath.
But while the spider sucks the blood of its victim and only aban-
dons it when it is dead, the fungus excites the algre taken in its
web to greater activity and even to more intense reproduction;
it thus makes more vigorous growth possible and the whole
colony develops well. The algre kept in slavery are transformed
in a few generations to such a point that they are no longer
recognizable. But in fact these opinions are not justified
by precise physiological studies made on the isolated members
of the association. According to Schwendener, the alga brings
about syntheses starting from the carbon dioxide of the air, the
fungus brings to the alga water and the mineral salts of the soiL
Many authors have shared the view of Schwendener; for
instance, Bornet, G. Bonnier and Warming. The last-named
considers that the alga can live alone, although the fungus needs
the alga and the latter is prevented by the fungus from repro-
ducing by zoospores. The alga is thus parasitized, and Warming
gives the name of helotism to this special type of parasitism;in
which the parasite (the fungus) provides its host (the alga) with
some of its food.
A Russian worker, Daniloff, goes so far as to maintain that
the fungus kills the gonidia by means of a network of hyphre which
penetrate them and absorb their contents, and which he com-
pares to the mycoplasma of EricksQn.
2. The converse theory-that the alga is parasitic on the
fungus-was formulated by Beijerinck 556. This worker did not
succeed in culturing the alga (Cystococcus) of Physcia parietina
when he provided it with nitrogen in the form of nitrate or
ammonia, to which sugar had been added, but he succeeded with
 LICHENS 259
nitrogen in the form of peptone, and here is, according to him,
the link between the alga and fungus: the fungus feeds on ammo-
niacal nitrogen and sugar; the pep tones it produces diffuse
through its cytoplasm and ensure the nutrition of Cystococcus.
Thus the alga actually feeds at the expense of the fungus, at
least as far as nitrogenous substances are concerned. This
opinion has found confirmation in the work of Artari. Accord-
ing to Tobler, the alga also receives some of its carbon from
the fungus, which is saprophytic, and this must make good a
deficiency in its photosynthesis hindered by its difficult situation
in the thallus of the fungus.
3. Between these two conceptions stands the idea of mutual-
istic symbiosis, the principal supporters of which are de Bary,
Reinke and van Tieghem. According to Reinke 576, the rela-
tionship of the alga to the fungus is that of the leaves and
roots of a green plant. The alga (autrophic) synthesizes carbo-
hydrates and borrows from the fungus (heterotrophic) the nitro-
genous and albuminoid material that the latter builds up with
the help of the carbohydrates furnished by the alga; besides
this, the fungus draws up water and mineral substances.
Symbiosis appears in yet a different light from the work of
Monsieur and Madame Moreau 572, namely as an antagonistic
symbiosis, reflecting the ideas of Noel Bernard on orchids,
which we are going to study later, and linked up with the idea
of the parasitism of the alga on the fungus. The aerial thallus of
one of the Peltigeracere-a group specially studied by the
authors-is, according to them, the equivalent of an organ de-
formed by a parasite, such as a gall. This idea must be extended
to all the lichens, whose thalli are equivalent to algocecids, or
algal galls. The lichens would be diseased fungi, injured by a
chronic infection, of a specific nature, which has become
necessary to the species, the infecting agent being an alga.
On ridding ourselves of verbal phantoms we find that the
question is really one of analyzing, by precise experiments, the
relations of the alga and fungus, and of careful comparison of
their behaviour in an isolated state and in association.
As far as the fungus is concerned, these studies are still but
slightly advanced. It has rarely been cultivated successfully in a
pure state. Moller obtained mycelia without gonidia, but they
did not develop reproductive bodies. The germinating spore
260 SYMBIOSIS AMONG PLANTS

must quickly find the right gonidia. On contact with them, as ifby
virtue of a special tropism or taxis, the mycelium forms
swellings which fix the gonidia, surround them and enclose
them. The gonidia seem to be, at least under normal conditions,
the necessary condition for the development of the mycelium.
The fungi of lichens have certainly become closely adapted to
the gonidia and have more or less lost the faculty of living alone.
As for the alga, it lives in isolation more readily, and the
study of it in a solitary state has received considerable stimulus
thanks to the important researches of R. Chodat 563 into the
methods of culturing these organisms in a pure state. But even
these researches emphasize the difficulty of drawing clear con-
clusions as far as lichens are concerned. Chodat, indeed,
observed that most of the lower algre that he cultured, and not
only the gonidia extracted from lichens, are more vigorous if
they are provided with an organic food and not only nitrate or
ammoniacal nitrogen. The preference of the gonidia for nitrogen
supplied in the form of peptone is not then a certain sign of the
parasitism of the alga.
An interesting contrioution to this problem is furnished by
work by A. Letellier 567, a pupil of Chodat, and I shall briefly
summarize his essential results by way of an example. He studied
in pure culture the nutrition of Nostoc peltigem extracted from
Peltigera, that of Cystococcus extracted from Xanthoria parie-
tina, of various kinds of Stichococcus (some free-living and
another from Coniocybe JurJuracea), and that of Coccomyxa
(free-living or coming from a species of Solorina). Letellier
observed, thus, that Nostoc peltigerce is distinct from free-living
Cyanophycere, studied earlier, in its great ability to assimilate
different sugars and in its proteolytic enzymes. In species
of Cystococcus the gonidia have a preferet\ce for assimilating
organic food. Some of the free-living members of the genus
Cystococcus behave in the same way, others prefer an inorganic
nitrogenous food. Gonidia of Stichococcus, from the point of
view of nitrogenous food, seem to be less parasitic in character
than those of certain free-living members of this genus. In the
Coccomyxa group the gonidia prefer an inorganic food, as
regards nitrogen as well as carbon.
There is not, therefore, any fundamental distinction between
the gonidia and their free-living algal congeners. Sometimes the
 MYXOMYCETES 261
former and sometimes the latter are better adapted to an organic
diet. The food relations between the algre and fungi must thus
be very varied. These results indicate the complexity of tb.e
problem and show that it demands numerou~ and extremely
precise studies.
In reality, the lichens result from a long reciprocal adaptation
of fungi and gonidia. Both organisms are modified in this
association and no longer possess their initial characteristics.
MYXOMYCETES. The Myxomycetes provide us with an exam-
ple of symbiosis that can be compared with that of lichens. To
tell the truth, although Myxomycetes are generally regarded as
fungi, their fundamental element is amrebre, in reality rhizopods;
that is to say, they are a part of the animal kingdom, or at the
most they are oil the borders of both kingdoms. The analysis of
symbiosis in thi Myxomycetes is principally due to Pinoy 573.
The Myxomycetes are, in reality, accumulations of amrebre, the
myxamrebre, associated with bacteria. Nadson (1899) and Potts
(1902) had already formulated the opinion that there was sym-
biosis between these two elements. Using culture methods of
great precision, Pinoy worked on Dictyostelium mucoroides
and was able to isolate the bacteria on one hand and the spores
on the other and show that the spores would not germinate in
the absence of bacteria. This myxomycete can only live when
the myxamrebre associate with living bacteria. The myxamrebre
engulf bacteria and digest them in their vacuoles by secreting an
intracellular enzyme (acrasiase) which liquefies gelatin, acting
only in an alkaline medium or a feebly acid one, and resembles
trypsin; its properties recall those of the enzyme isolated by
Mouton from ordinary amrebre. In short, Dictyostelium muco-
roides is parasitic on colonies of micro-organisms (generally of
Bacillus flavescens var. fluorescens).
Pinoy extended these findings to other Myxomycetes of the
same group as the Acrasiere and to those with endospores
(Didymium difforme, D. diffusum), where he recognized that the
sporangia were always contaminated by numerous bacteria of
various kinds. He was successful in culturing them with a single
type of bacterium. -
He also extended these findings to the case of Plasmodiophora
brassicce, which produces cabbage rot. This disease is actually
caused by the bacteria introduced with the myxamrebre. The
 262 SYMBIOSIS AMONG PLANTS

bacteria, finding an extremely favourable medium for develop-

ment in the cells of the cabbage, destroy the roots of the plant
and thus set at liberty the spores of the parasite within the
cells. The bacteria are necessary to the extracellular life of the
parasite and no one has succeeded in making the myxamrebre
live alone.
MYXOBACTERIA. Here I am going to compare the preceding
results with those that Pinoy 574 obtained from the Myxo-
bacteria. In pure culture, these organisms behave like common
bacteria; in other conditions they build up complex structures: in
Chondromyces crocatus there is a branched foot which, towards
its extremity, carries projections terminated by spherical heads
in which ovoid spores are inserted. These structures are com-
posed of strings of bacterial elements ensheathed in a hard
substance of a bright orange-yellow colour. The condition neces-
sary for the formation of these structures, called fructifications,
. is that Chondromyces be associated with a bacterium related to
Micrococcus luteus. On culturing both species together one
sees that Micrococcus is lysed by Chondromyces and the fructifi-
cations form in contact with the area where lysis has occurred.
With other bacteria (B. jiuorescens, B. pyocyaneus) abnormal
forms are obtained, one of which closely resembles Chondro-
myces catenulatus. It is as though one species were transformed
into another.
NODULES IN THE LEGUMINOSAL Another example of
symbiosis in the plant kingdom, equally classical today, is that
of the nodules on the roots of leguminous plants, which cannot
be more than mentioned here; the soil bacteria, which assimilate
atmospheric nitrogen, are incorporated into nodules on the
rootlets and modified into bacteroids whose substance is finally
assimilated by the plant. The benefit which the Leguminosre
exert on the soil has been known from remote times and Liebig
showed that it is based on an increase of nitrogen. Hellriegel
and Willfahrt, in 1888, demonstrated that this is due to sym-
biosis of the plant with soil bacteria which extract nitrogen
from the atmosphere, as Schlresing and Laurent proved. The
bacteria (Bacterium radicicola) were isolated by Beijerinck and
the nodules were produced synthetically by culturing first the
bacteria and secondly the plant in sterilized soil, and then
seeding the former into the soil.
 MYCORRHIZA 263
An analogous symbiosis exists in the alder tree whose roots
also show nodules, produced by Streptomycetacere, and in
various Eleagnacere (Eleagnus, Hippopha).
We also know of nodules produced by symbiotic bacteria on
the leaves of Rubiacere and tropical Myrsinacere under con-
ditions similar to those shown by the Leguminosre. All these
structures are basically very similar to galls and could be con-
sidered as bacteriocecids.
MYCORRHIZA. I shall dwell in greater detail on those ex-
tremely widespread associations called mycorrhiza between
fungi and the roots of arboreal and herbaceous plants.
As early as the middle of the 19th century they were pointed
out and today they are known in a large number of cases: in the
prothallus of certain Hepaticre, in the mosses, in various groups
of vascular cryptograms (prothallus and sporophyte of Lycopo-
diacere-Lycopodium, Psi/otum, Phylloglossum-amongst the
ferns-Ophioglossum), in most perennial plants and trees. In
1881 Kamienski put forward the hypothesis of a symbiosis
between the fungus and its host. This theory was developed
principally after 1885 by Frank 448, who at the same time
showed the great extent and regular occurrence of mycor-
rhizas. He distinguished between ectoCrophic mycorrhizas which
remain external to the roots, around which they form a mycelial
sleeve, and are found principally on forest trees (Coniferre,
Amentacere), and endotrophic mycorrhizas which penetrate into
the cells of the root.
According to Frank, there is a mutualistic symbiosis between
ectotrophic mycorrhizal fungi and plants bearing them. The
fungus is said to be a functional substitute for the root hairs: it
must imbibe from the soil and bring to the plant both mineral
salts and organic nitrogenous food from humus; the plant, for
its part, must yield carbohydrates, which it has built up, to the
fungus. The endotrophic fungus would, in addition, make a
final contribution to the nutrition of the plant in being digested
by it and thus providing it with nitrogenous matter.
Frank's original conception has since been considerably
modified. It is in connection with orchids that these researches
have been most precise in character, and we shall examine them
separately. As far as forest trees are concerned the role of mycor-
rhiza does not appear to be as precise a symbiosis as Frank
264 SYMBIOSIS AMONG PLANTS

suggested. The root hairs are by no means suppressed and

remain functional. The fungus appears to be a parasite, little
harmful and tolerated. A historical survey of research on endo-
trophic forms up to 1904 is given by Gallaud 566 in a thesis
which contains a profound morphological study of these fungi.
Endotrophic mycorrhizal fungi (from what is known of
orchids) appear, according to the characters of their vegetative
parts, to constitute a natural enough group but one whose
affinities remain obscure. On the tip of the mycelial filaments
there are often extra- or intracellular vesicles and, above all,
strongly branched bushy growths or arbuscles, which are speci-
ally characteristic of them and were demonstrated by Gallaud
(Fig. 77). These arbuscles undergo a characteristic type of
degeneration in which the tips of the main growths end in a kind

Figure 77. Intracellular termination (arbusc1e and sporangioles)

of an endotrophic mycorrhiza in Allium sphCl!rocephaium.

of ball or sporangiole. Arbuscles and sporangioles occur in

mycorrhizas of the most varied plants and they are not known
elsewhere. So far, it has not been possible to isolate this mycor-
rhizal fungus and culture it; the systematic position is therefore
unknown. The fungi have certainly been much modified by their
adaptation to a life in association with the tissues of roots.
As for reciprocal reactions of the plant and fungus, we find
that the cells containing the arbusc1es, and those in their neigh-
bourhood, do not contain starch grains. It appears that the
fungus consumes the sugars from which this starch would be
formed. In the arbuscular cells the nucleus swells up, assumes
amreboid contours, shows excess chromatin and sometimes
divides amitotically. As a rule the cell ends by digesting the
fungus. Endotrophic mycorrhizal fungi, in short, take carbo-
 MYCORRHIZA OF ORCHIDS 265
hydrates from their host. Their external communications are, on
the other hand, quite insufficient for one to be able to admit that
they draw an appreciable amount of material from the soil and
bring it to the plant. They feed, then, at the expense of the plant
and behave as parasites. But their effect appears to be confined
to inert organic substances elaborated by the plant, and not to
affect the living substance of the latter, as is the case with truly
parasitic fungi (Uredinere, Peronosporere, etc.). They end by being
phagocytes. Gallaud considers that endotrophic mycorrhizal
fungi are saprophytes, which vegetate in plant tissues without
causing serious damage, but also without assisting the assimila-
tion of the host. It does not seem, then, at least in our present
state of knowledge, that we should regard these associations
between plants and mycorrhizal fungi as a symbiosis.
-These conclusions are, however, not likely to be valid for all
mycorrhizas, an opinion to which one is led by facts con-
cerning those of the orchids and probably also of the lycopods
and Ophioglossum. * -
MYCORRHIZA OF ORCHIDS. The existence of endotrophic
mycorrhizas is general in the orchids and they were pointed out
as early as the middle of the 19th century. In 1846 Reissek saw
the mycelium and tried to culture it. In the course of the next
twenty-five years a series of observers, such as Irmisch, Schacht,
Prillieux, Fabre, Drude, etc., saw them without recognizing
their nature, and it was Kamienski who, in 1881, interpreted
their presence as a symbiosis with the orchid. Wahrlich, in 1889,
showed how widespread they were by finding them in the roots
of all the orchids he examined, approximately 500 species. But
it was No(;H Bernard 217 who showed their importance and their
exact role in the life of the plant.
He proved, indeed, that it was the presence of the fungus that
makes it possible for the seed of the orchid to develop. It ij well
known that these plants, the flower of which is so specialized,
produce very tiny seeds, rudimentary in structure, in enormous
numbers (more than one million per capsule in certain tropical
orchids). They have no albumen and the embryo in them is
undifferentiated, reduced to a mass of cells with a suspensor.
The germination of orchids was unsuccessful during the
,. Additional references on mycorrhlzas in general are given at the end of the
bibliography.
266 SYMBIOSIS AMONG PLANTS

19th century, save in an irregular and empirical manner, and by

methods kept secret. Bernard, who had tried in vain to germinate
the seeds of Neottia nidus-avis, an indigenous orchid lacking
chlorophyll, completely resolved the problem by discovering a
plant of Neottia in which the flower stalk was curved towards
the soil and whose seeds had spontaneously germinated on con-
tact with the earth, even in the,capsule of the fruit. By observing
the young seedlings under the microscope he saw that they had
been invaded by a fungal mycelium and that this extremely pre-
cocious infection occurred at the point of attachment of the
suspensor. The penetration of the fungus thus appeared as the
first phenomenon of germination; in it he saw the determining
cause of the latter and this hypothesis was amply verified.
Thus, the empirical successes and failures of workers were
easily explained. It was, indeed, known that to get the seed to
germinate it was necessary to sow it on the ground of the pot
in which the parent plant had been grown, that is to say, in soil
containing the fungus. With time the germination of orchids in
greenhouses became gradually easier, because the soil there had
gradually become richer in fungi as a result of prolonged culture.
In natural conditions the immense number of seeds compen-
sates, as far as the perpetuation of the species is concerned, for
the loss of numerous embryos which do not meet the fungus
necessary for their development. This is a mechanism parallel
to that shown by animal parasites and one that has the same
consequences.
Bernard also saw the influence that the fungus exercised over
tuber development and even believed that, generally speaking,
the latter was the result of infestation of a subterranean organ
by symbiotic fungi; he showed the coexistence of both facts in
a number of plants. One can, it is true, bring about tuber forma-
tion apart from the presence of fungi. Molliard, for example,
obtained it in radishes by CUltivating them in a solution of glu-
cose in an aseptic medium, but this is not incompatible with
Bernard's explanation.
As far as the role of fungi in orchid germination is concerned,
Bernard 558 demonstrated it experimentally by most careful
methods. He succeeded in isolating and cultivating ,the fungus
in vitro, an achievement which has not yet been successful with
other mycorrhizas.
 GERMINATION OF ORCHIDS 267
Here, in a few words, is his method. He dissected, under a
binocular microscope and in rigorously aseptic conditions, an
infected seedling or root cultured in a sterile tube; and isolated
from the fungus the intracellular mycelial coils (pelotons) which
constitute one of its essential characteristics.·It is thus protected
from all the common moulds or bacteria which would other-
wise smother the mycorrhizal fungus in culture. These coils
are then placed, one by one, by means of a sterile platinum
loop, on a culture medium, where they develop into a sheet,
whose characteristics we shall consider later.
The seeds, gathered aseptically by flaming the capsules and
rapidly plunging them into alcohol before opening them, are
sown in sterile culture tubes of a type customary in bacteriology,
on agar or absorbent cotton wool, to which a decoction of

Figure 78. Seedling of Phalamopsis (at 18 months) grown in a

sterile tube by being sown on cotton wool steeped in a decoction
of saJep with Rhizoctonia mucoroides (after Noel Bernard).

salep* has been added. In these conditions they remain for

months at a time without undergoing modification; or else they
become green and acquire the first stage of differentiation, which
varies according to the species, but always remain rudimentary.
They do not germinate.
But if the mycelium of the fungus which has been cultured
separately is gradually sown into the tubes where the seeds have
remained dormant, the latter develop in a short time. At first
they generally assume the aspect of a small tubercle in the shape
of a spinning top, only producing leaves and roots later, and
comparable to what Treub observed in the lycopods (which
also possess a mycorrhiza) and called a protocorm.
The proto corm then gradually gives rise to the leafy plant. In
this way Bernard regularly obtained the germination of very
many orchids in culture tubes. Fig. 78 shows a specimen of
Phaicenopsis - an epiphytic orchid whose germination was
particularly difficult to obtain-which sprouted under these
* SaJep is a powder obtained by grinding up dried tubers of Orchidace<e.
268 SYMBIOSIS AMONG PLANTS
conditions and which, having been entrusted to an expert and
finally cultivated in soil by ordinary methods, flowered nor-
mally. * Fig. 79 shows seeds and numerous young plants under-
going differentiation. t
Let us return to the fungi themselves. Their growth in the
plant is charactenzed by the formation, in the cells, of compact
coils of filaments. These formations reappear, although rather
rarely, in cultures in vitro. It is not mechanical compression that
determines their formation in the cell. They are just the type
of intracellular growth characteristic of a mycorrhiza, and
Bernard consIders that this is determined by a humoral effect; he
compares the latter to the agglutination of a bacterium by the
serum of a vaccinated animal. No success has been achieved in
obtaining the perfect form of the mycorrhizal fungus, but only
the mycelium. Bernard thinks that all the mycorrhizas of orchids
belong to the same natural group which is adapted to these
plants and which he places in the genus Rhizoctonia. One species
of this genus is common on the potato and forms greenish
sclerotia there. It is considered to be identical with R. violacea
of Tulasne, found on the roots of lucerne and saffron. This
fungus forms intracellular coils, like the endophytes of orchids.
The numerous fungi extracted by Bernard from orchids were
considered by him to constitute three species:
1. Rhizoctonia repens, the most widespread, taken from
numerous genera and species, which is said to be the most primi-
tive form.
2. R. mucoroides, extracted only from the roots of Pha/anopsis
and Yanda, but always found in the plants of these genera, what-
ever their origin.t
3. R. lanuginosa; obtained only from Odontoglossum grande.
Burgeff 562, who repeated Bernard's researches and verified
and confirmed all his principal results, believes in a much greater
specific variety in the fungi. He makes a new group for these
... Towards the bottom of the figure the dots that one sees on the surface of
the agar are the sclerotia of the fungus.
t Quite recent researches by F. Mariat 570 have shown that the addition of
vitamin B to the culture media used by N. Bernard and his followers encourage
the growth and differentiation of embryos of Catlleya. Pyrimidme alone and a
mixture of pynmidme and thiazole act III the same way. It i~ possible that in the
orchid-fungus associatlOn the fungus contrIbutes biological factors of the nature
of vitamins, capable of acting on the growth and dIfferentiation of the embryos.
t Bernard obtained the same fungus from the roots of Ophioglossum, but it
was without effect on the orchids.
 GERMINATION OF ORCHIDS 269
-fungi, the Orcheomycetes, and described 15 species in it. He
considers that each 'species of orchid has its own endophyte. *
Bernard's work is not limited to these results of considerable
practical and theoretical importance. Making use of Rhizoc-
tonia, he was able to analyze thoroughly its role in symbiosis and
establish facts or make suggestions of the greatest interest.
The relationships of the orchids with their mycorrhiza are far
from being constant and uniform. It is quite clear that the rudi-
mentary structure of the seeds is a secondary state, resulting
from an evolution which has gradually made symbiosis neces-
sary and which must be represented by various stages.
And, indeed, amongst the orchids studied by Bernard there is
a species, Bletilla hyacintha, of the Far East, that specialists
(Pfitzer) consider to be primitive from its characters taken as
a whole, and here symbiosis with the fungus is not necesssary
for the germination of the seed. Bernard was able to get the
seedlings to develop aseptically; but then they germinate
differently, without developing the proto corm, and a compari-
son of both types in the same plant allows us to see what the
actual influence of the fungus is on the form of growth. In the
grown plant symbiosis is very intermittent. The rhizome to which
the plant is periodically reduced is free from mycorrhiza; each
year there is a fresh growth of roots, which becom~infested on
their own account. The mycorrhiza then appears as an inter-
mittent and usual infection.
But Bletilla constitutes an exception and in the great majority
of terrestrial and epiphytic orchids the embryo only develops
under the influence of the fungus. In its absence only an outline
of germination is produced; in its presence the latter goes ahead
without delay. In most forms (Cattleya, Cypripedium, Ophry-
dium) symbiosis remains intermittent in the adult state; it is
renewed each year with the growth of the roots and disappears
when they do.
In the Sarcanthinere (Phalanopsis, Vanda) , epiphytes which
Pfitzer considered the most highly evolved of the orchids,
• Burgeif made an extensive study of the properties of these fungi in culture.
They transform sugars (with the help of invertase and maltase), break down
glucosides (by emulsme), produce tyrosmase, do not assimilate free nitrogen but
freely take up organIC mtrogen (of salep), produce proteolytic enzymes, etc.
Bernard recognized that specIes of Rhizoctonia digest cellulose. Indeed, they
disintegrate the absorbent cotton wool on wluch they are often cultured.
270 SYMBIOSIS AMONG PLANTS

germination occurs only with Rhizoctonia mucoroides, and sym-

biosis becomes continuous, the roots here being persistent. This
character attains its maximum in Tamiophyllum.
The terrestrial' orchids show the same degrees of symbiosis
as the epiphytes and it is in Neottia nidus-avis that this type of
growth is carried to its greatest extent. Here, indeed, symbiosis
is absolutely continuous during the whole life of the plant and,
instead of being limited to the roots as in the preceding cases,
it extends to the rhizome. Further, it is directly transmitted
from one generation to the next. When, as frequently happens,
Neottia flowers and fruits underground, the fungi in the rhizome
spread directly into the fruit and infest the seeds, which germi-
nate in situ. At this level, as Bernard remarks, fungus and orchid
practically achieve a new and permanent individuality, com-
parable with that of a lichen.
Thus, in the orchids there are found certain stages of an
evolution in symbiosis reached by several series of forms which
are independent of each other, and Bernard remarks that this
same evolution very probably occurs in other groups, notably
in Ophioglossum and the lycopods, where symbiosis presents
similar characteristics but where it has not yet been studied as
in the orchids.
We find again, indeed, in these plants, either in the gameto-
phyte (prothallus) or in the sporophyte, the same strange facies
of the vegetative parts (tuberization in the prothallus, spin-
ning-top form of seedlings, analogous localization of the fungi)
as in the orchids. So that symbiosis must have been an impor-
tant evolutionary factor in groups which are quite independent
and separate from one another. It would obviously be most
interesting to verify Bernard's ideas on the Ophioglossace<e and
the Lycopodin<e. * .
* Bernard even goes so far as to ask whether symbIOSIS has not been a major
factor in plant evolution, one to which IS due the appearance, deriving from
pnmltive mosses, of plants with perenmal arborescent sporophytes, almost
all infested with mycorrhlza. Annual plants would have returned to this state
by eliminating theIr symbIOtIC fungi. This evolutIOn may have been able to
recur several times. The orchids would represent one of these secondary evolu-
tIOns. These are at present only purely speculatIVe conceptions.
Magrou 569, III a quite recent artlcle, found some confirmation of Bernard's
ideas III observatIOns made on Rhynia, fossil plants m the red sandstone of the
Scottish Devonian, whIch have been compared WIth HepatIca- but which show
In their aXIS, thought to be a stem, some dIfferentIation of vascular tissue, and
can therefore be considered as one of the possible initial forms of vascular plants.
These erect axes of Rhynia and Hornea, borne on an underground rhizome which,
 RHIZOCTONIA 271
One of the most interesting aspects of Bernard's researches,
from the point of view which occupies us here, is the physio-
logical analysis of the relationships of Rhizoctonia and orchids.
Under the conditions in which he cultured the fungi, it hap-
pened, indeed, quite generally that after a long period of culture
in vitro, Rhizoctonia gradually became powerless to make the
seeds germinate. It had become inactive and was totally so after
two or three years of tube culture. But it can be made active
again by being passed through seedlings or seeds. Here we have
a phenomenon that Bernard compares very suggestively, and it
seems very justly, with variations in virulence (attenuation and
augmentation) in bacterial infections.
That led him to study the way in which the fungus grows and
propagates in the orchid, making this investigation either
with the fungus normal to the species, or by bringing about
abnormal associations, for instance, by inoculating Rhizoctonia
mucoroides or R. lanuginosa into species which harbour
R. repens, or vice versa.
The fungus penetrates at definite points of entry, for instance,
the place of attachment of the suspensor" or the base of the
absorbing hairs of the roots. These points are those where the
plant shows the maximum permeability and which play the
principal role in exchanges with the environment. It must be
supposed tl).at these zones excrete soluble substances which, in
culture, attract the fungus and which offer the minimum resist-
ance to its penetration. Rhizoctonia digests pure cellulose. It
only traverses the epidermal cells without forming coils in them.
Each area of penetration, once this has been effected, acquires
an immunity which is opposed to all fresh infection. Thus the
suspensor is only invaded once. Successive infestations must be
made at distinct points of entry.
The appearance of Rhizoctonia in the tissues depends on the
degree of its activity and it is only at a suitable degree that sym-
biosis is established. Thus, either in nature or in cultures, all the
seeds are far from germinating, even when they meet the fungus,
in Hornea lignieri, is formed from segments of a tubercular shape, recall those
descnbed by Treub m certam lycopods. Now, m these tubercles structures have
been seen which have been attributed to a fungus (mycelium without cell walls,
insinuated between the cells and swelhng into vesicles recallmg those that one
sees in mycorrhizas). Magrou saw in this a confirmation of the views of Treub on
the role of the embryonic tubercles in the genesis of vascular plants and of those
of Bernard on the symbiotiC ongm of these organs.
272 SYMBIOSIS AMONG PLANTS
as the seedlings in the tube show (Pig. 79). Symbiosis, to use
Bernard's expression, is on the frontiers of disease.
As we have said, Ritizoctonia only traverses the epidermal
cells and it is in the subjacent parenchyma that it grows with the
very characteristic form of filamentous pelotons in the cells.
But in cases where the seed germinates well, the invasion
remains limited.:' There is always some kind of barrier which
prevents the mycelium from developing at the growing point
and which checks it as growth advances. At the point where
the invasion is checked a proportion of the cells of the orchid's
c·3 c·'4

Jt f:#
(J

• ;
" •• '
",

,_
,'0

Q ••
0 , '.

.. .....
•••
.t 0

(i) •• ' ..

,
o.
0 ,
tJ .
••. :0
~
~ .
0

~"I' ....
.

°0 ~ .••
.0
:.
0
"0'

'.

Fig. 79. Lelio-Cattleya sown in sterile tubes inoculated with

Rhizoctonia of increasing activity, C'l> C'3, C'4 (after Noel
Bernard).

parenchyma play the part of phagocytes (Fig. 80); their nucleus

becomes enlarged (it attains up to 60 times its original volume,
according to Burgeff) and lobed, and the mycelial coils con-
tained in its cells are digested, leaving a residue. * This occurrence
was, moreover, seen by the first observers ofmycorrhiza, such as
Prillieux in 1856, but was not interpreted. Magnus in 1900 and
Shibata in 1902 described this process of digestion. It is, says
Bernard, a true phagocytosis which governs the extent of infec-
tion in symbiosis. The differentiation of the 'nucleus of the
• The formation of sporangioles at the expense of the arbuscles of the endo-
trophic type of mycorrhiza studied by GaUaud, is a similar type of phenomenon.
 PHYSIOLOGY OF MYCORRHIZA 273
phagocytes even precedes the penetration of the fungus into
them and must result from a distance reaction caused by soluble
products or by an enzyme from the mycorrhiza.
Most of the workers, particularly Frank, who observed this
process of digestion before Bernard, considered it to be a matter
of nutrition, essential to the life of plants with endotrophic

Figure 80. Section of a germinating Odontoglossum, showing

the penetration of the suspensor after one month, and the intra-
cellular coiling of Rhizoctonia lanuginosa, as well as its destruc-
tion by phagocytosis; s, stoma; p, absorbing hairs (after Noel
Bernard).
mycorrhizas. According to them the plants were fungivorous
as some are insectivorous, and this digestion was a proof of
mutualistic symbiosis, a compensation for the loss of the carbo-
hydrates consumed by the fungus at the ho_st's expense. But
Bernard clearly established that it has no connection with the
development of the plant. Rhizoctonia does not play a direct
part in the nutrition of orchids.
274 SYMBIOSIS AMONG PLANTS
Phagocytosis is the organism's defensive reaction. If orchids
are infested with abnormal Rhizoctonia, as we have said, or with
inactive Rhizoctonia, either the infestation is rapidly checked by
phagocytes, symbiosis is not established and the seed fails, or
else the plant dies from a generalized invasion of its tissues and
its growing point, without the phagocytic reaction being
observed or at least without its playing a very effective part.
Between the benign infestation, rapidly checked by an' almost
immediate phagocytosis, and a rapidly fatal infestation in which
phagocytosis is insignificant or non-existent, occurs the inter-
mediate case of symbiosis in which phagocytosis is exercised
without, ho",ever, arresting the propagation of the fungus, and
in which, nevertheless, the plant does not.succumb. This sym-
biosis can last throughout life, as in Neottia nidus-avis, or else
be intermittent.
Since the fungus never attains the growing point, the plant
achieves a certain immunity which is the condition of its develop-
ment. The intracellular coiling of Rhizoctonia must, then, be a
phenomenon connected with this immunity; for, in cases of fatal
infection, studied by Bernard, the fungus abandons this type of
growth and from that time the mycelial filaments run in a
straight line, invading all the tissues. The humoral action to
which we have already alluded must be lacking.
Bernard finally sought to understand the way in which mycor-
rhizas act, without invoking either the word or the mystical
conception of symbiosis. He asked himself whether the effective
role of mycorrhizas might not be due to a favourable modifica-
tion that they produce in the intracellular environment. Now, he
was successful in obtaining the germination of certain orchids
without fungi, by sowing seeds on concentrated solutions (agar-
agar or absorbent cotton wool impregnated with a decoction of
strong salep and often with saccharose added). He noted, more-
over, that Rhizoctonia cultured on salep-saccharose caused an
increase in the molecular concentration of the solution employed
(which can be determined by variation in freezing point). It is
possible that their enzymes break up complex molecules into a
larger number of simpler molecules. One can then imagine that
they act in the same way in their intracellular growth and that
they increase the degree of molecular concentration in the sap
of the seedlings into which they penetrate; this condition would
 PHYSIOLOGY OF MYCORRHIZA 275
permit germination. Bernard compares this suggestion with the
production of experimental parthenogenesis in animals by the
use of hypertonic solutions. Although this is hypothetical,
the fact remains that a stronger concentration of solutions
allows the fungus to be dispensed with in the germination of a
certain number of orchid species.
Symbiosis between orchid and mycorrhizal fungus is by no
means a fixed entity, nor a mutualistic association for assisting
both parties. It is a phenomenon of parasitism, an infection, a
constant disease become essential but one which, according to
its degree or its appearance, ensures the development of the
plant, stops it, or even kills the plant. In general biology it is a
chapter of pathology parallel to that of bacterial infections and
not to be distinguished from parasitism.
With this in mind, there is obviously reason to investigate
plants with a similar aspect-Hepaticre (Fegatella), Lycopo-
diacere (Lycopodium, Psi/otum, Phylloglossum), Ophioglossacere.
The generalizations to which N. Bernard has been led from
his magnificent researches on the' orchids have given rise to
numerous discussions. This is, after all, the common lot with all
new ideas. We must greatly regret the premature loss of this
investigator, at once a precise experimentalist and a man of
great vision, who had not time to explore the horizons he
opened up. Recent research tends to determine the physico-
chemical mechanisms which operate in symbiosis, the associa-
tion of two organisms providing one of them with elements,
notably vitamins, that it cannot produce itself. For this aspect,
reference should be made to the works of Magrou and of his
pupil Mariat 568-570. As an example, I shall cite here the fact
that the fungus Spharocybe concentrica (Stelbacere) when cul-
tured alone only fructifies on media containing a B vitamin,
thiazole, but when in association with a red yeast, Rhodotorula
rubra, which builds up thiazole, the fructifications are obtained
without thiazole being added to the culture medium. It is the.
same when Spharocybe is associated with Sordaria finicola
(Sphreriacere).
CONCLUSION. We have thus finished reviewing the principal
groups of facts which are connected with the idea of sym-
biosis. The conclusion emerges that they do not constitute a
clearly distinct category but are related to parasitism and to
276 SYMBIOSIS AMONG PLANTS
commensalism by an intermediate series without showing a
distinct contrast to either.
In classical examples, such as those of the lichens, it is neces-
sary to abandon the idea of a purely mutualistic association
with equivalent reciprocal benefits. It is a conflict between alga
and fungus, habitually and intimately associated, in which the
two organisms have reacted on each other. That is, after all, the
conclusion formulated in 1906 by the Russian botanist Elenkine.
He stated that the mutualistic conception of symbiosis would
have to be replaced by that of an unstable state of equilibrium:
the two associated organisms react differently to the con-
ditions in the external environment and to their variations.
These were not equally favourable to both; and according to
the case in question, the one or the other would dominate.
These variations must remain within the limits in which
neither of the two organisms succumbs, a conception which is
equivalent to that ofN. Bernard: "La symbiose est alafrontiere
de la maladie."
In this association the two organisms react on each other;
there is evolution within the symbiosis, evolution both morpho-
logical and functional, leading finally to new requirements as
in the germination of orchids, or to absolutely new functions
as in the case of yeasts in insects, or luminous bacteria in
cephalopods. These last cases, which Pierantoni called heredi-
tary physiological symbioses, do not appear at first sight to
fit in with the idea of conflict or instability. There is, never-
theless, no doubt that in the first place they were infections of
insects or cephalopods by alien organisms, but the conflict was
terminated by the dominance of one of the organisms over the
other and by a stable equilibrium exactly corresponding to a
novel function. These are the cases which, in the present state
of our knowledge, represent the most complete evolution.
 CHAPTER XIII

IS SYMBIOSIS A PRIMORDIAL
CHARACTERISTIC OF THE CELL?

THE facts of. symbiosis, such as those we have just examined,

form a continuous series and are fairly widespread in nature.
It is sufficient to think of zooxanthellre and zoochlorellre,
of lichens, mycorrhizas, of bacteroids in nodules on roots,
of yeasts in insects, and of luminous bacteria, to the extent
in which their role is definitely recognized. Nevertheless, these
facts remain exceptions in organic life taken as a whole. Normal
life does not necessarily involve these internal associations.
They are a deviation from the normal.
, Now, some years ago a certain number of biologists showed
an inclination to see them in a contrary light, as a funda-
mental form of vital functioning. The cases recalled above would
only be gross and macroscopic examples, in some sense, of what
is the life of the cell; the latter would always be a symbiosis. The
cell, indeed, would swarm with symbiotic micro-organisms to
which would belong the essential metabolic powers.
The idea is not new. It followed an already long series of
hypotheses in which attempts were made to explain heredity and
life by the conception of particles endowed with special pro-
perties. These ideas are to be found methodically set out in the
book by Y. Delage on heredity. Most were purely speculative;
others tended more or less to acquire an objective reality.
Amongst them some, such as the micella! of Nageli, the pangenes
of de Vries, the biophores of Weismann, with which were finally
connected the genes of Johannsen, have played an important
role in contemporary biology because they were conceived in
\ terms of cellular structure, as revealed by the microscope.
They provided, just at that time, a solid material basis for
studies in mendelian heredity. Others, on the contrary, were
conceived in an entirely speculative fashion; such were the
microzymas of B&:hamp. Others, finally, derived from pure
p.s.-lO 277
278 IS SYMBIOSIS A :PRIMORDIAL CHARACTERISTIC?

observation, such as the granules of Altmann 412, which

ultimately be9ame mitochondria; today, these last hold a
place of the first rank in cytological research as well as in the
domain of physiology. For the conception of the cell as the
ultimate morphological unit, Altmann wished to substitute that
of the granule. The granule is an entity which is continuous and
reproduces itself. The aphorism, omnis cellula e cellula, gives
way to omne granulum e granulo. For Altmann the granules are
the intrinsic elements of the organism.
Some years ago another conception was opposed to this one,
that of seeing in the cell primitively distinct organisms and intra-
cellular symbionts which were the substratum of the principal
cellular functions, though originally alien to the cell.
Coliceptions of this kind suggested themselves incidentally to
certain biologists. Raphael Dubois, in his work on animal light
and on colour-producing organs, thought that the seat of these
functions lay in the intracellular corpuscles, vacuolides, to which
he ascribed a great degree of autonomy; he claimed, by reviving
various theories, the paternity of ideas to which systematic
studies on cellular structure had led, and which resembled
his own.
More recently a series of methodical observations and ex-
periments by Pierantoni and Portier* has led to conclusions
which have been set out in a particularly precise fashion. In
the theories formulated it is necessary to distinguish exactly
between what is definite knowledge and what remains debatable
or even ill-founded.
Let us first examine the ideas of Pierantoni, who, in any case,
slightly preceded Portier. They are concerned with researches
into the symbiotic yeasts of insects, the results of which were
indisputable, and which led him to study the light organs in
cephalopods. The first of his conclusions is that luminescence in
Rondeletia and Sepiola is due to symbiotic bacteria, swarming in
the lumen of the glandular ducts of the light organ, occasionally
passing outside, and being regularly inoculated into successive
* GaJipe 415 arrived at the same conclusions through hIs conception of normal
parasitism. According to him, there are mfinitely small bodIes which are normally
essentIal for the regulatIOn of cellular actIvity. They are cha~actenstic of the cell's
functionmg and are to some extent the simplest representation of hfe in
organIZed beings.
GaJipe himself stressed the affinity of these ideas with Bechamp's speculations
on microzymas.
 THEORIES OF PIERANTONI 279
generations by way of the egg. It is obviously very tempting to
try to include in such an explanation the production of light in
the other cephalopods, in Pyrosoma, and in animals in general. In
abyssal cephalopods the light organs are closed; the photogenic
region is a cell complex, more or less syncytial in nature, in
which the granulations swarm that are the seat of the light
phenomena. According to Pierantoni 516, these granules are
bacteria adapted to intracellular life. In researches on Charyb-
diteuthis he says that he saw" a la partie la plus externe de la
masse de l' organe lumineux anal (qui est clos) une couche ou,
avec corpuscules extremement petits, se trouvent aussi des
formes bacillaires (de vrais bacteries) en voie de fragmentation
en grains minuscules; des bacteries qui, en somme, evoluent de la
forme bacillaire a laforme granulaire." But one sees how diffi-
cult it is to give irrefutable proof of such an affirmation which,
nevertheless, is necessary. According to Pierantoni's idea, the
intracellular granulations which seem to be the seat of light
in all luminous animall;, and which correspond to the vacuolids
of Dubois, would then be bacteria become intracellular and
changed into the form of simple granules. Similarly, according
to the researches of Dubois on the formation of the purple in
Murex trunculus, this is formed by "des corpuscules tres petits"
that Dubois calls vacuolides zymasiquesor spMrulese!ementaires,
and "Comment ne pas penser-sur la base de ce qui a ete
expose de la transformation et de l'adaptation des bacteries
photo genes a la constit'ution de la substance photogene
des organes lumineux-a une adaptation analogue possible de
bacteries chromo genes a la fonction de la production des
couleurs?" Pierantoni has undertaken experimental research in
order to prove by means of cultures that the pigmentary granu-
lations are also symbiotic bacteria. All this "place sous un
nouveau jour l'activite des plasmes cellulaires et assignerait aux
inclusions cytoplasmiques et peut-etre a beaucoup des con-
stituants du protoplasme une vie autonome et une activite
specifique, au bem!fice des organismes dans lesquels ils vivent. "
Such are the theories of Pierantoni which clearly tend to
attach to symbiotic organisms adapted to intracellular life a
large number of special functions that occur in animals: func-
tions of luminescence, colour production, pigmentation, etc. It
remains a purely theoretical idea as long as no irrefutable proof
280 IS SYMBIOSIS A PRIMORDIAL CHARACTERISTIC?
is given by the autonomous culture of the granulations in ques-
tion. This has by no means been provided for us at the present
time.
Portier 419 was led to analogous views by researches into xylo-
phagous insects and he formulated them in a much more general
and rigid fashion in his book, Les Symbiotes, published in
1918. The facts and ideas set out in that book gave rise to very
lively controversy at the time when the first French edition of
this present book appeared. Today, one can consider this ques-
tion as settled; the ideas upheld by Portier have been aban-
doned completely. I have nevertheless thought it necessary to
retain the following pages, because they appear to me to illus-
trate a type of question which, in various forms, periodically
recurs, and because the nature of the arguments produced
gives rise to types of discussion whose interest survives the par-
ticular debate and can put our minds on guard against too hasty
interpretations. The fundamental unity of the cell, without in
any way being a dogma, is sufficiently established for it not to
be contested without absolutely·categorical proofs.
For Portier the cell was by no means the fundamental
unit in organisms. It was essentially a symbiotic complex.
It would always be crammed with symbionts indispensable for
effecting organic syntheses, which are none other than mito-
chondria; these would be bacteria adapted' to the symbiotic
intracellular life. The bacteria alone would be autotrophic, that
is, capable of feeding independently. All cells and, consequently,
all animals and plants with a cellular constitution, would be
heterotrophic and would only assimilate through the inter-
mediary of symbiotic bacteria. There is obviously no a priori
impossibility about such a conception; but, as it brings into
question all the fundamental notions of biology, it must be
based on irrefutable proofs. One can affirm without any
hesitation that this is by no means the case.
The starting point of Portier's ideas is to be found in his
Recherches physiologiques sur les champignons entomophytes 51.7.
He believed it established that there was a regular and general
symbiosis between wood-eating insects and fungi of the genus
Isaria. This symbiosis would manifest itself even after death,
with particular distinctness in the Lepidoptera, which very fre·
quently, according to entomologists' saying, turn to fat. This is
 THEORIES OF PORTIER 281
due to the invasion of the corp;e by the mycelium of Isaria,
whose conidia were present before this in the state of symbionts.
The very frequent infection of insects by Isaria is well known,
but it is considered simply as a phenomenon of parasitism.
Metchnikoff, then Giard 450, even tried to make use of these
parasites to produce epizootics on a large scale in the larvre of
harmful insects, particularly in beetroot weevils and cockchafers.
Portier acquired the idea of a constant symbiosis of these
fungi by studying the development of a caterpillar, Nonagria
typhce. That was his starting point. He believed that he found
conidia in the digestive tube of this caterpillar. He found them
again, and drew them, in the intestinal epithelium and in all the
tissues of the adult, inc1u_Ping the eggs by which they were said
to be transmitted to the following generation. But the identifica-
tion of the structures figured as conidia of Isaria remains more
than arguable. Positive proof has not been given and one can
even affirm that the bodies figured, principally on account of the
way in which they stain (cf. Les Symbiotes, Fig. 9, p. 30; Fig. 26,
p. 176), must be spores of Microsporidia whose presence in the
various tissues is very simply explained. All the facts produced
relative to the caterpillar of Nonagria typhce appear as the simple
result of an infestation by a microsporidian of the genus Nosema,
like that of the silkworm by pebrine, and we know well enough
that this last has nothing to do with symbiosis. * The presence of
corpuscles in the oocytes is very natural; it takes one back to the
work of Pasteur on pebrine. It would be very desirable, besides,
that the preceding statement should be verified by work on
Nonagria typhce taken from the localities where Portier studied
it.
As for the other facts pertaining to xylophagous insects, they
appear to me not to have sufficient validity as a basis for the
conception of intracellular symbiosis. The only ones which can
support it are those relating to the yeasts in the mycetome of
Hemiptera (aphids, coccids, etc.) which we have already re-
viewed: these are undoubted but their application is strictly
limited.
* The regular presence of one organism within another is not a sufficient
criterion for assuming that it is a matter of symbiosis. There are indisputable
parasites which occur with absolute regularity. Such is, amongst other cases. the
gregarine Lithocystis sclmeideri in Echinocardium cordatum, which was discussed
earlier.
282 IS SYMBIOSIS A PRIMORDIAL CHARACTERISTIC?
Another basis for Portier's theory-indirect in this case-
would be the impossibility of aseptic life and the necessity
for symbionts, asepsis being taken in the ordinary sense of the
word. The intestine of animals usually contains a rich and varied
flora, sometimes useful, sometimes harmful, and Pasteur con-
sidered it possible that the existence of such a flora was abso-
lutely necessary. It is probable, as we have seen earlier, that in
most animals the intestinal fauna or flora contributes to the
transformation of food substances, and it is even possible that
it plays a regular and important part in this! We are generally
agreed today in attributing such a role to the ciliates in the
paunch of ruminants; and to the trichonymphids of termites,
and we have pointed out, too, the suggestions by Wigglesworth
concerning the intestinal bacteria of Rhodnius prolixus. But the
possibility of an aseptic life is fully established today. It was
achieved under rigorous conditions in mammals by Nuttall and
Thierfelder 504, in spite of the technical difficulties of rearing
them aseptically, and later by Cohendy 438 in Metchnikoff's
laboratory. Such an experiment is very complicated in practice,
and it is clear that reasons of quite a secondary nature render it
precarious. Mme Metchnikoff 497 also reared some frog tad-
poles aseptically, and Wollmann 548 some flies (Calliphora).
Portier 527, too, observed that mining caterpillars-notably
those of Nepticula flosculatella-on hazel trees, are naturally
aseptic as long as they remain beneath the epidermis of the leaf.
But the problem of the aseptic life has been solved practically
and on a large scale by Delcourt and Guyenot 441 with
Drosophila, and their results have been confirmed by such
workers as J. Lreb. Delcourt and Guyenot developed an exact
technique for this, thanks to which breeding could be carried
out regularly-as with a pure culture of a species of bacterium-
and infinitely better than under ordinary conditions. Guyenot 456
pursued this aseptic breeding through neady 50 successive gene-
rations, comprising thousands of individuals, without any
adverse symptoms ever developing.
The interest of these researches is, moreo:ver, not only in the
demonstration of the possibility of the aseptic life. This method,
as Guyenot showed, places the experimenter in possession of
absolutely constant environmental conditions for precise inves-
tigation into fundamental problems of nutrition. Now, in the
 THEORIES OF PORTIER 283
flies raised in this way, none of the symbionts which Portier
considered essential was found.
But, in reality, all that we have just considered deals only with
secondary matters in the theory of symbionts as it was formu-
lated by Portier. The essential point, really, is the dualism in
the constitution of the cell, the existence-absolutely general
-within it of autonomous organisms said to be the mito-
chondria. It would be necessary, then, by extracting mitochon-
dria from the cell and culturing them, to prove that they are
indeed autonomous organisms, bacteria adapted to intracellular
life. Portier declared that this proof was indeed supplied by his
work on various glandular organs of mammals, principally the
testes, in which the mitochondrial apparatus has been much
studied by the cytologists, in seminal lineage. But, in reality,
Portier's experiments relate principally to the peri-testicular
adipose tissue; from this tissue, he obtained-attempting to
work in a stringently aseptic fashion-some cultures which
were said to be those of intracellular symbionts, and he studied
the physical and chemical properties of these organisms.
In point of fact, he did not obtain these cultures regularly,
and the conditions in which they were produced were not suffi-
ciently explained. But a first objection to his interpretation
derives from the fact that the organisms cultured have properties
which are irreconcilable with the hypothesis that they could be
mitochondria.
They were first cultured with paradoxical facility on the
ordinary broth of bacteriologists, to which had been added
5 per cent. glycerine and 1 per cent. potassium nitrate. Now,
we know how difficult it is as a rule to find a medium suit-
able for bacteria adapted to conditions as special as those of
intracellular life. It would, then, be at least surprising that
mitochondria, highly modified forms if they are indeed bacteria,
would let themselves be cultured so easily in an ordinary
medium.
The characters of the culture were no less bizarre. The bacteria
were extremely polymorphic. They were astonishingly resistant
to heat, up to 115° in a moist atmosphere, to 145-150° in a dry
one. The scum, immersed in absolute alcohol and chloroform,
resisted for whole months; on dehydration it could be brought
to boiling point in both these liquids, or heated in acetone to
284 IS SYMBIOSIS A PRIMORDIAL CHARACTERISTIC?

120° in a sealed tube. Finally, these bacteria were motile and

strictly rerobic.
Now, on the contrary, the precise observations of different
workers, notably of Regaud 528 and of Guilliermond 455 , have
taught us that within cells the mitochondria that can be seen
in living tissues without the action of any reagent are extremely
fragile structures; a slight variation in osmotic pressure makes
them swell up and disappear; they do not resist a temperature
over 40°. They are also destroyed by alcohol and acids, even
weak ones. To preserve them, special fixatives are needed, such
as formol. They are homogeneous structures, semi-liquid bodies,
malleable, structureless, whereas bacteria are rigid in form, with
a definite structure and are resistant to the most varied reagents.
When suitably fixed and stained, preparations of mitochondria
show, it is true, an outline reminiscent of bacteria, but it is a
chance resemblance and quite superficial.
Histologists, including Regaud, Guilliermond and Laguesse,
relying on these considerations, have regarded Portier's identifi-
cation as absolutely impossible. The mitochondria are intra-
cellular bodies, being derived perhaps always from each other
by division, certainly playing a considerable role in intracellular
differentiation and synthesis, but with particular properties that
are irreconcilable with those of the bacteria cultured by Portier
and described by him under the name of symbionts.
These properties, as Portier recognized, recall to bacteriolo-
'gists either those of Bacillus subtilis, which might have been
lntroduced in the course of manipulation (the aseptic extraction
of certain organs is extremely difficult to achieve), or those of
;::ommon saprophytes, provided with spores, which occasionally
break through the external or intestinal barriers of the organism
and become immobilized in the form of spores in the organs or
tissues. Control experiments made at the request of the Societe
de Biologie by Portier and Bierry on one side, and L. Martin
and Marchoux on the other, led the four experimenters to the
following conclusions:
1. The passage of pieces of the organs of an animal into a
culture medium is always difficult to achieve with constant
asepsis. It is one of the most difficult operations in bacteriology.
2. A successful culture is not generally obtained from healthy
organs when the pulp oftes"tes is used.
 CONCLUSIONS 285
3. One may find micro-organisms in testes either when work-
ing with whole organs or with large fragments. The presence of
these microbes in the testes is not constant, hence it is impossible
to affirm that they exist normally (C.R.Soc. Bi%gie, vo1. 83,
p. 654, 8th May, 1920).
Consequently, it cannot be considered as established that
normal intracellular micro-organisms have been cultured, still
less mitochondria.
One is no more justified in saying, with Portier (Les Symbiotes,
p. 79), that mitochondria have previously been cultured in vitro,
and referring, as a proof of this, to the bacteroids of the Legu-·
minosre. These have, indeed, been cultured and are autonomous
organisms, ·Myxobacteria. All that they have in common with
mitochondria is that they are intracellular.
The hypothesis of normal and primordial intracellular sym-
biosis, such as Portier proposes, does not rest, then, on authentic
facts established by experiment, and the classical cellular theory
stands in its entirety. That does not dispel all possibility of
reality for ideas of cellular dualism and the existence of autono-
mous intracellular organisms. But they still have to be demon-
strated from start to finish, and, moreover, it is just as natural,
if not more so, to attribute to the cell itself the faculty of
accomplishing the essential functions of life, as to imagine it
powerless and only able to assimilate through the intermediary
of bacteria.
Symbiosis, then, remains for the present an exceptional
phenomenon in multicellular organisms, or in the cell con-
sidered in isolation; we know, as we have had occasion to see,
that it occurs over a very wide field, and it is possible that it
will finally be found to be of even greater extent. In the present
state of our knowledge it in no way represents the fundamental
form of cell life.
CONCLUSION. If one seeks to extract a conclusion from the
collection of facts analyzed in this volume, one comes to see
that no natural distinction exists between them. Commensalism,
parasitism and symbiosis are only categories created by us and
. as soon as they are thoroughly analyzed it is impossible to
delimit them.
Under varied aspects they are only manifestations of the
struggle for life, characterized by specialization in the way in
10*
286 IS SYMBIOSIS A PRIMORDIAL CHARACTERISTIC?
which it is exerted, but deprived of all finality or pre-established
harmony. Those associations survived which balanced their
accounts in a fashion compatible with the existence and per-
petuation of the associates; many others must have arisen
from time to time but have not lasted through failing to satisfy
this necessity.
Where organisms pass from the normal conditions of exist-
ence in free-living forms to those in which they are associates,
they undergo very considerable structural changes sometimes of
enormous extent, which are perhaps the most striking illustra-
tion of the reality of their evolution, and, above all, of the
influence of the environment on the organisms; but the capri-
cious diversity of these transformations indicates that the
evolutionary changes are principally conditioned by the intrinsic
properties of diverse living forms.
The associations which we find in the different forms of com-
mensalism, parasitism and symbiosis involve in the partici-
pating organisms functional activities and special developments
that we do not see in free-living forms. From this arise multiple
problems, not only morphological in character but also, and
perhaps principally, physiological, problems of extreme com-
plexity that we are only beginning to perceive and touch upon,
and of which the interest cannot be exaggerated. Although
points of view will inevitably change, the subject of this book
will long remain topical in biology.
 BIBLIOGRAPHY
(Revision and addenda by translator)
There can be no question here of giving a comprehensive biblio-
graphy of parasitism and symbiosis. In the case of certain completely
parasitic groups, that would mean enumerating all the works pub-
lished on them. This particular index includes the papers cited in this
volume arid certain books or works providing a rapid survey of a
given group of parasites or of a special question. Memoirs or books
containing important bibliographical documentation are indicated
by one or two asterisks.
I GENERAL TEXT-BOOKS
1. BAER, J. G. (1946.) Le parasitisme. Lausanne and Paris.
2. BRUMPT, E. (1936.) Precis de parasitologie. Paris, 5th ed.
3. BUCHNER, P. (1930.) Tier und Pjianze im Symbiose. Berlin, 2nd ed.
4. - - (1939.) Symbiose der Tiere mit pjianzlichen Organismen.
Berlin, Sammlung Goschen, no. 1128.
5. GRASSE, P. P. (1935.) Parasites et parasitisme. Paris (coll. Arm.
Colin).
6. LEUCKART, R. (1889.) Die mensch lichen Parasiten und die von
ihnen herriihrenden Krankheiten. Leipzig and Heidelberg,
2nd ed.
7. LINSTOW, O. VON. (1878.) Compendium der Helminthologie.
Hanover.
8. NEVEU-LEMAIRE, M. (1912.) Parasit%gie des animaux domes-
tiques. Paris.
9. RAILLIET, A. (1895.) Traite de zoologie medicale et agricole.
Paris.
II SPECIAL PERIODICALS
*Annee biologique. (Abstracts.) Paris, 1897-1937.
Archives de parasitologie. Paris, 1898-1912.
**Bulletin de I'Institut Pasteur. Paris, 1903-
Bulletin de la Societe de Pathologie exotique. Paris, 1908-
Zentralblatt fiir Bakteriologie, Parasitenkunde und Infektions-
krankheiten. Jena, 1887-
Journal of Parasitology. Urbana, 1915-
Parasitology. Cambridge, 1908-
Zeitschrift fiir Morphologie und (Eko[ogie die Tiere. Berlin, 1928-
Zeitschrift fiir Parasitenkunde. Jena, 1869-75.

287
288 BIBLIOGRAPHY

III COMMENSALISM
General
10. ALCOCK, A. (1892.) A case of commensalism between a gymno-
blastic anthomedusoid (Stylactis minoi) and a scorprenoid
fish (Minous inermis). Ann. Mag. nat. Hist. (ser. 6), 10.
11. AURlVILLIUS, C. (1889.) Die Maskirung der oxyrrhynchen
Decapoden durch besondere Anpassungen ihres K6rperbaues
vermittelt. Sv. Ak. Handl. Stockholm, 23.
12. BONNIER, J. and PEREZ, C. (1902.) Sur un Crustace commensal
des Pagures Gnathomysis gerlachei n. sp., type d'une famille
nouvelle de Schizopodes. C. R. Acad. Sci. Paris, 134.
13. BOUVIER, E. L. (1895.) Le commensalisme chez certains polypes
madreporaires. Ann. Sci. nat. (Zool.) (ser. 7), 20.
14. - - (1907.) Sur Ie commensalisme d'un Crabe portunien, Ie
Lissocarcinus orbicularis Dana. Bull. Mus. Hist. nat. Paris.
15. - - and SEURAT, L. G. (1905.) Eumedon convictor, Crabe com-
mensal d'un Oursin. C. R. Acad. Sci. Paris, 140.
16. BRUNELLI, G. (1913.) Ricerche etologiche. Osservazioni ed
esperienze sulla simbiosi dei Paguridi e delle Attinie. Zool. Jb.
(Zool.) 34.
*17. BURGER, O. (1903.) Ueber das Zusammenleben von Antholoba
reticulata und Hepatus chilensis. Bioi. Zbl., 23.
18. CHEVREUX, E. (1908.) Sur les commensaux du Bernard-l'ermite.
Bull. Mus. Hist. nat. Paris.
19. COLLIN, B. (1912.) Etude monographique sur les Acinetiens.
Arch. Zool. expo gen., 51, 297-305.
20. COWLES, R. P. (1920.) Transplanting of sea-anemones by
hermit-crabs. Proc. Wash. Acad. Sci., 6.
21. COUPIN, H. (1894.) Sur l'alimentation de deux commensaux
(Nereilepas et Pinnotheres). C. R. Acad. Sci. Paris, 119.
22. COUTlERE, H. (1898.) Note sur les recifs madreporiques de
Djibouti. Bull. Mus. Hist. nat. Paris.
23. - - (1898.) Observations sur quelques animaux des recifs
madreporiques de Djibouti. Ibid.
24. - - (1904.) Note sur Ie commensalisme de l'Arete dorsalis var.
pacificus H. Coutiere, d'apres les notes de M. L. Seurat natu-
raliste, a Rikitea (lIes Gambier). Ibid.
25. DUERDEN, J. E. (1905.) On the habits and reactions of crabs
bearing actinians in their claws. Proc. Zool. Soc. Lond., 2.
26. EMERY, C. (1880.) Le specie del genere Fieras/er del Golfo di
Napoli e regionelimitrofe. Fauna u. Flora Neapel, Monogr. II.
27. ENDERS, H. E. (1905.) Notes on the commensals found in the
tubes of Chcetopterus pergamentaceus. Amer. Nat., 39.
 BIBLIOGRAPHY 289
28. FAURE-FRl3MIET, E. (1906.) Le commensalisme sp6cifique chez
• les Vorticelles d'eau douce. C. R. Soc. BioI. Paris, 61,456-458.
29. - - Le commensalisme des Opercularia. Ibid., 514-515, 583-
585.
30. FAUROT, L. (1895.) Etudes sur l'anatomie, l'histologie et Ie
d6veloppement des Actinies. Arch. Zool. expo gen. (ser. 3), 3.
31. - - (1910.) Etude sur les associations entre les Pagures et les
Actinies: Eupagurus prideauxi Heller et Adamsia palliata
Forbes, Pagurus striatu8 Latreille et Sagartia parasitica Gosse.
Ibid. (ser. 5), 5.
32. GIARD, A. (1882.) Sur un type synthetique d'Annelides (Anop-
lonereis herrmanni) commensal des Balanoglossus. C. R. Acad.
Sci. Paris, 105.
33. GRAVIER, C. (1905.) Sur un Polyno'idien (Lepidasthenia digueti
n. sp.) commensale d'un Balanoglossus du Golfe de Californie.
C. R. Acad. Sci. Paris, 140.
34. HEATH, H. (1910.) The association of a fish with a hydroid.
Bioi. Bull. Woods Hole, 19.
35. JUNGERSEN, H. (1913.) On a new gymnoblastic hydroid (Ichthyo-
codium sarcotretis) epizoic on a new parasitic copepod (Sarco-
tretes scopeli),. infesting Scopelus glacialis Rhdt. Vidensk.
Medd. naturh. Foren. Kbh., 64.
36. LUNEL, G. (1884.) Sur un cas de commensalisme d'un Caranx
et d'une Crambessa. Rec. Zool. suisse, 1.
37. MALAQUIN, A. (1890.) Quelques commensaux du Bernard
l'Ermite. Rev. Bioi. N. Fr., 2.
38. MINCKIEWICZ, R. (1909.) Memoire sur la biologie du Tonnelier
de mer (Phronima sedentaria). Bull. Inst. oceanog. Monaco,
146.
39. - - (1909.) L'instinct du deguisement et Ie choix des couleurs
chez les Crustaces. Rev. gen. Sci. pur. appl., 20.
40. PARKER, G. H. (1926.) The inquiline fish Fierasfer at Key West,
Florida. Proc. nat. Acad. Sci. Wash., 12.
41. PELLEGRIN, J. (1905.) Commensalisme de jeunes Caranx et de
Rhizostomidre. C. R. Ass.fr. Avanc. Sci. (Congr. Cherbourg).
42. PEREZ, C. (1920.) Le complexe ethologique du Spondyle sur les
banes perliers du golfe Persique. C. R. Soc. BioI. Paris, 83.
43. PLATE, L. (1908.) Apogonichthys strombi n. sp., dn symbiotisch
lebender Fisch von den Bahamas. Zool. Anz., 33.
44. POLIMANTI, O. (1911.) Studi di fisiologia etologica. Zool. Jb.
(Zoot), 30.
45. POTTS, F. A. (1915.) The fauna associated with the crinoids of
a tropical coral reef: with especial reference to its colour varia-
tions. Carneg. Inst. Wash. Dept. mar. BioI., 8.
290 BIBLIOGRAPHY
46. SAINT-JOSEPH, de. (1901.) Sur quelques Invertebres marins des
cotes du Senegal. Ann. Sci. nat. (Zool.), (ser. 8), 12.
47. SEMPER, C. (1863, 1864.) Lettres a KreIIiker. Zeits. wiss. Zool.,
13,14.
48. SLUITER, P. (1888.) Ein merkwiirdiger Fall von Mutualismus.
Zool. Anz., 11.
49. - - (1902.) Die Sipunculiden und Echiuriden der Siboga
Expedition. Siboga Exped., Monogr. 25, 19-25.

Myrmecophilous forms
50. BRUES, C. T. (1901.) Two new myrmecophilous genera of aber-
rant Phoridre from Texas. Amer. Nat., 35.
51. BUSGEN, M. (1891.) Der Honigtau. Eine biologische Studie an
Pflanzen und Pflanzenlaiisen. Jena Z. Naturw., 25.
52. CHODAT R. and CARRISSO, L. (1920.) Une nouvelle theorie de
la myrmecophilie. Arch. Sci. phys. nat. Geneve, 37.
53. DONISTHORPE, H. K. Numerous notes on myrmecophilous
animals in the Entomologist's Record and the Journal of
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54. EMERY, C. (1909.) Ueber den Ursprung der dulotischen, para-
sitischen und myrmecophilen Ameisen. Bio!. Zbl., 29.
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turcicus Friv. Zugleich ein Beitrag zur Kentniss der Myrme-
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540. - - (1910.) Pseudovitellus und ahnliche Gewebe der Homop-
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541. THIEL, M. E. (1929.) Zur Frage der Ernahrung der Stein-
korallen und der Bedeutung ihrer Zooxanthellen. Zool.
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542. TRIER, H. (1926.) Der Kohlenhydratstoffwechsel der Pansen-
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11*
318 BIBLIOGRAPHY
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565. ELFVING, F. (1913.) Untersuchungen tiber die Flechten-
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596. STUMPER, R. (1950.) Les associations complexes de fourmis:
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597. - - and Kutter, H. (1950.) Sur Ie stade ultime du parasitisme
social chez les fourrnis atteint par Teleutomyrmex schneideri
n.g., n.sp. C. R. Acad. sci., 231.
598. - - (1951.) Sur l'ethologie du nouveau myrmecobionte Epi-
myrma stumperi Kutter. C. R. Acad. Sci., 233.
 ADDENDA 321
BJORKMAN, E. (1942.) Ueber die Bedingungen der Mykorrhizabildung
bei Kiefer und Fichte. Symbolae Bot. Upsaliensis, 6, pt. 2.
BUTLER, E. J. (1939.) The occurrence and systematic position of the
vesicular-arbuscular type of mycorrhizal fungi. Trans. Brit.
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GAUMANN, E. (1950.) Principles of Plant Infection. English edition
by W. B. Brierley, London.
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stitution und Okologie der Mykorrhizen von Pinus syh'estris L.
und Picea abies (L.) Karst. Mykol. Unters. u. Ber., 2, Cassel.
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rhiza. Jena.
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 INDEX
Numbers m heavy type refer to pages on which there are IllustratIOns.
Aard-vark, see Orycteropus Amll1ba vindlS, 230
AbductIOn by ants, 24-25 Amphtlma, 132, 162
Abothrrum Illjundlbull/m, 131 Amphlpoda, 65
AbsorptiOn organs, 109-13,111 AmphlprlOn, 3
Acacia, 29 AmphWomum subclavatum, 138
- sph(uocephala, 27 Amphulla squamata, 114, 161, 199
Acanthobdella, 37 Anapagurus hyndmanni, 119 t
- paUadma, 37 Anas, 131
Acanthocephala, 37, 144 Anatidre, 138
Acanthocystls, 230 Anceus, 66
AcartlCl,69 Anchlstes miersi, 31
Access to host, 183-91 Anehorma, 172
Accessory reproductive phases, 159-67 Aneylostomum, 139
Acerma cernlla, 138 - eanmum, 185
Acherontla atropos, 17 - duodenale, 38, 185-6, 196
Achreea gnsella, 17 AncyrOlllscus, 156
Acmeta,32 - bonmeri, 83, 84
Acineta tllberosa, 33 Andrella, ·200
AcrasJase, 261 Allelasma squalleola, 34, 90
Acteea, 92 Allemoma su!eatum, 173
Actmoloba retlclilata, 12 Anergates, 23
Actmomyces rhodnll, 222 - atratulus, 26
Actinosphamllm, 230 Angler fish, 157
Acuarudre, 142 Amsonema vmdls, 230
ADAM,306 Annulamdre, 242
Adamsia palliata, 9, 10, 11, 217 Anoblldre, 241
.'Ega, 31 Anodonta, 116, 138, 163, 193
iEgldre, commensalism m, 67 Anomalopldre, 251
Agamogony, 160 Anomalops, 251
AgemaspIS, 165 Anomura, 72, 85
- testacelceps, 166 Anopheles, 147, 176, 177, 179,184
Aggregata, 145, 175 Antelope, 16, 176
Aglossa,50 AnthenOldes rugulosus, 51
Agrion, 142 AnthomYldre, 120
AklS, 129 Anthonomus grandis, 180, 181
Albatross expedition, 61, 63 ANTl-IONY, 47, 306
ALCOCK, 33, 288 AntJblotlc substances, 195
AIcyonana, 34, 35, 231 Anubodles, 197
Alder tree, 263 Anticoagulants, 38, 44, 45
Alepas, 34 AntJklDase, 195
Aleurodes, 238 Antlpathana, 93-4, 100
Aleurodldre, 237-9 Antlpathes ianx, 94, 96
Algocecld, 259 AntitrypSIn, 195
Alimentary equilibrium, 179 Ants, 16-29
AUantonema, 155, 158 - and fungi, 219
AIlellosltJsm, 257 Apanteles ju/vlpes, 122
ALLIOT,224 - glomeralus, 121
Allium spheerocephalum, 264 - lactleolor, 122
Allolobophora chlorollca, 126, 188 APATHY, 38, 308
Alpheldre, 4, 5, 91 Aphalara ealthee, 239
Alpheus, 86, 92 Aphelopus me/aieucus, 204, 209
ALTMANN, 278, 310 Aphldldre, 22, 210, 239
A!ydus ealcaratus, 17 Aphis mazdlradlels, 22
Amazon ant, 26 Aphrodite, 33
Amentacea:, 263 Aphrophora, 246
Amlcroplus collaris, 167 - sailcis, 239 ~
Ammodytes lanceolaills, 207 Apogomchthys strombi, 30
Ammodytidre, 30 Apothecla, 256 .
Amll1ba vespertillO, 232 Apterostlgma, 219
322
 INDEX 323
Arachis, 177 Bacteroids, 241
Arbuscle, 264, 272 BAER,287
Archigetes, 132, 134, 136, 162 Balanoglossus, 6
- appendlculatus, 133 Balanus, 72, 82-3, 87
Aremcola, 139, 194 - amaryllis, 207
Arete dorsabs, 5 - balanoides, 68, 83
Argas, 190, 244 BALBIANI, 236, 3 I I
Armadillo, 151 Baris, analis, 200
ARTARI,259 DE BARY, 217, 259,318
Ascaris lumbricoides, 158, 186 Basidiomycetes, 256
- megalocephala, 196 BATHELLIER, 220,311
ASCHNER, 254, 3Il Bathyactls'symmetrrca, 94, 97'
ASCldw prunum, 63 Bats, 138
Ascobactenum, 241 BAUME-PLUVINEL, 304
Ascomorpha helvetica, 231 BAUR, 57, 59, 306
Ascomycetes, 220 BEcHAMP, 277
Ascomscldre, 83 Beckw albma, 17
Ascothoraclca, 65, 93, 95, 104, 156 BEIJERINCK, 213, 230, 232, 258,262,310,
Ascothorax ophlOctems, 94, 97 318
Asellus, 32, 33, 144 BELT,219
AseptIc hfe, 282 BENECKE, 319
Asexuallarvre, 167 VAN BENEDEN, E , 294
ASPldlOtuS nem, 237 VAN BENEDEN, P J" 128, 130
Aspidoslphon, 5, 6 BEQUAERT, 187, 305
ASpIdophryxus sarsi, 82 BERNARD, E, 47, 306
Ass, 176 BERNARD, N., 259, 265-75, 3"
Astenas calamaria, 94 BIERRY, 284
Asterophlla japonica, 62 BILHARZ, 139
Asticot stage, 79 BdharZIa, see Schist
Astrochans graCIlis, 208 BilharZIOSIS, 139
Astrochordeuma appendlculatum, 208 BILLET,'244
Astropecten multwcanthels, 94
Atelenevra spuna, 204
Atemeles, 18, 19, 23
Ateuchus sacer, 142
Athelges, 72, 73
ATKINS, 75, 77, 80-1, 299
Alta, 28, 219
Altagenus pellio, 206
Altaphlla, I7
Attractonema, 158
Auchmeromyza, 36, 178, 188,243
Aulax papavens, 215
AURNILLlUS, 14, 288
Autolytus, 162
Autotomy, reproductive, 162
AVlcuhdre, 118
AWERINTZEFF,232
AxlUs plectorhynchus, 47
AYERS, 125
Azteca, £!i-9

BabesiOSIS, 151
Baccalaureus argalicorn
- japomcus, 94, 99, 10
- maldlviensls, 94, 10
Bacdlus cuenoti, 241
- jlavescens, 261
- subtlbs, 241, 284
Bactena, luminOUS.
- , symbiotic, 221
Bactenoceclds, 2f
Bactenology, Xl
Bacterium chire
- radlcicola.
- savastonc
- rume/acit
324 INDEX
Bostrichidre, 220 Camel,151
Botfly, 189 CAMERANO, 297
Bothriocephalidre, 131-2. 134 Camponotus itgniperdus, 242
BothrIOcephalus, 130,132, 175, 197 Cancncepon elegans, 69
-latus, 130--1 CANESTIUNI, 303
BOUFFARD, 151 CANTACUZENE, 4
BOUSSINGAULT, 22 CAND,299
BOUVIER, 6, 230, 288, 311 Capillaster mliitiradiata, 51
Bovldre, 188 Capitelhdre, 33, 172
Brachyura, 72 Capulidre, 48-50, 156
Bracomdre, 119, 123, 167 Carabidre, 19
Bradynema rigidum, 155 Caranx melampygus, 4
Bradypus, 28 - trachurus, 4
Branchiophryxus, 72 Carasslus auratus, 137
BRANDT, 230, 232, 234, 311 CARAYON,83
BRATTSTROM, 94, 101, 299 Carcelza eXClsa, 181
Braula, 21 Carcharias, 3
BRAUN,295 Carcmus mtenas, 68, 77-8, 80, 87, 198,
Bream, 131 201
BRECHER, 311 Cardium, 9, 145
BREMENT, 300 - edule, 146
BRINKMANN, 119, 297 Caridid31, 73
BrlSlnga evermanm, 62 CARISSO, 290
'lQCH, 94, 100, 299 Carmarina, 161
Tall Moth, see Euproctls chry- CAROLI, 70, 75. 299
Carp, 133
Cartena, 234
CARY, 163-4,295
Caryophyllacere, 204
Caryophyllaceus, 132, 162
-lallceps, 133
Caryotropha mesnili, 206, 207
Cassis, 10
Castexia douvillei, 208
Castrata vindls, 233
C 'strahon, paraSitic, 198-205
129, 142, 175
~, 129, 138, 142, 145, 176, 179
va, 268-9
• expedition, 33
'\Y, 84, 106, 109, 115, 171,
)7, 292, 294, 295, 297, 300, 309.

11
orm, see Cordy/obia anthro-
~vente,166
166
}24, 210,221

1,75,78
- 160-1, 246-9" 278
}

i4

"50
 INDEX 325
Cestodaria, 131--4, 162 Collozoum, 230, 234
Cetacea, 34, 144 Collyrites dorsalis, 208
Cetonia, 144 Colorado potato beetle, 120
- cardui, 17 Colour choice. 14
- floncola, 17 Colymbus, 131
Cetollinre, 18 Comanthus annulatus, 5
Chtetogaster, 162 Comatulidre, 5
Chretopterus, 6, 7 Commensalism, definition of, I
Chalcldldre, 119, 210 Commoptera, 20
ChalcldOldea, 165 Complemental males, 156
Challenger expedItIOn, 97 ComPSI lura concmnata, 181, 187
Charybditeuthrs, 248, 279 Congo floor maggot, see AuchmeromYIQ
CHATTON, 31, 43,207, 292, 300 Coniferre, 263
Cheimatobta brunnea, 122 ConlOcybe jurjuracea, 260
CHEVREUX, 7, 8,288 CONTE, 237, 312
Chlmrera, 132 Convoluta, 231
Chimpanzee, 182 - vmdls, 233-5
Chmdota prsanii, 57 Copepoda, 65, 104--15, 156
Chironormdre, 138 Copldosoma, 167
Chlamydomonas, 233--4 Cora, 256
Chlamydophrys stercorea, 35 Coracld larva, 130, 131
Chlamydopsis, 18 CordIa, 29
Chlorella vu/gans, 232-3 Cordy/obla anthropophaga, 188, 205,
Chlorogaster, 92 - rodhainr, 188
CHODAT, 29, 233, 260, 290,311,318 Coronu/a, 34
ChtEromYla, 178, 188 COSTANTIN,318
Chondromyces catenulalus, 262 Cothurnia, 32
- crocatus, 262 COTTE,310
Chondropoma:l' ~ ~latul1lJ.42 Cotylorhiza, 231
Chromotrop~, COuPIN, 8, 31, 288
Chroococcus, 257 COUTIERE, 4, 5, 288, 300
Chroolepidacere, 25b COWLES, 10, 288
Chrysops, 143 Crambactls arabica, 3
CHUN,294 Crambessa pa{mipes, 4
Cicada, 237 Crematogaster, 21
Cicada orni, 239 Cnnoniscldre, 83
CicadeIhdre, 237, 239 Crista, 169
Clcadomyces, 243 CrithidIa, 152
CIENKOWSKY, 230, 232, 311' Crossaster, 94
CIliates In rummants, 227-9 Crossocosmla sericarire, 187
Clrolana, 5 Crotophagus, 16
Cmipedla, 33--4, 65, 86 Cruclferre, 199
CLAPAREDE, 242 Crustacea, 145, 172
Clavrger, 23 - , adaptation to parasitism in, 65-107
-longrcorms, 19 CrYPSldomus, 105
- testaceus, 19, 20 Cryptochirus, 208
Clavigennre, 18-19 Cryptocotyle lmgua, 137
CLEVELAND, 222-3, 225-6,253,312 Cryptomonas brandti, 233
Clepsrdrina davini, 206 - schaudmnr, 233
Cleptoblosis, 25 Cryptolliscan Iarvre, 69, 70, 72, 75, 78, 80,
Clrbanarrus misanthropus, 83 83, 156
ClonorchIs smenSIS, 137 Cryptolliscidre, 69, 72, 81-5, 155-6
Clou de Biskra, 151 Cryptops, 172 .
Clymenidae, 7 Cryptotermes, 226
Clytra, 17 Ctenophora, 234
CoaptatlOns, 43 Ctenoscu[um, 49
Coccidre, 239, 241 - hawairense, 61-2
CoccidIa, 145, 152, 159-60, 172 Ctenostomata, 33
CoccidIum, 160 Cucujidre, 241
Coccldomyces, 239 Cucullanus e/egans, 142
Coccobacillus prerantonri, 249 Cue umana mendax, 56
Coccomyxa, 260 CuENOT, 43, 193,241,252,292,308, 319
Ca:iJ!nterata, 161 Culcita, 4, 30
C{ETOpiana, 35 Culex, 147-8, 176
Ca:nurus cerebralis, 129 - jatigans, 143 .
COHENDY, 282, 312 Culicidre, 152, 180, 243
Coleoptera, control of, 120 Cum(Echus insignis, 172
COLLIN, 33, 288 Cunrna, 57, 161
326 INDEX
Cunoctantha, 161 Dendrogaster /udwigii, 102
Curculiollld~, 241 - mUrmanensis, 94,103
Cursorius europl1!us, 162 Den<irogastridre, 94, 101-4
CURTIS, 307 Dendrosomides paguri, 33
Cuterebra emasculator, 198 Dermatobia hominis, 189
Cyamus, 34, 37, 65 Dexiidre, 120, 187
Cyanophyce~, 256-7, 260 Dexodes nigripes, 187
CyathozOId, 249 Diacolax, 49, 56
Cybis/er, 33 Diadema se/osum, 4
Cye/as, 138 DIAKONOW~ 94, 97, 300
Cyc/opodza greeji, 187 Diaplomlls, 175
CyclopOid larva, 124 - gracilis, 131
Cyclops, 32, 129-30, 142 Dlaspidre, 239
- coronatus, 143 Dictyonema, 257
- strenuus, 131, 175 Dictyostellum mucoroides, 261
- viridis, 131 Dlcyemlda, 160-1, 172, 185
Cyclorrhapha, 126 DidymIUm dlfforme, 261
Cyclosfoma e/egans, 242 - dijfusum, 261
Cyclostomata, 169 DijJlugia nodosa, 230 .
Cymodoce, 85 - piriformis, 230
Cymothoa, 69 Digenetic trematodes, 134, 136-42
CymothOidre, 36-7, 66-7, 155 Dileptus anser, 232
Cynipidre, 1I9, 126,210,213 Dimorphic development, 135
Cyphomyrmex, 219 Dimorphism, sexual, 154-8
Cyprina, 31, 116, 138 Dinarda dentala, 17
Cypnnidre, 117, 132 - hagensi, 17
CYPTlpedIUm, 269 Dlpleurus baculus, 244
CYPTls,129 Dlplodmlum, 228-9 ....,
Cypns larva of Myriocladus, 95 - denticu/atum,. 'P - "
- of Sacculma, 87, 88 - mult r - - ......
Cyproniscidre, 72, 83 -neg l
CystlcercOld, 134 Dlplo"i' Jtus, 163
Cysticercus, 128, 134 Di'" ",94
-bovis, 129 DI. )-20, 122, 126, 150, 210
- celJuiosre, 128-9 - > .a,35
- pisiformls, 129-30 Dipl) ,92
Cystococcus, 258-60 DIj1ylia .m caninum, 129-30
Dlscomycetes, 256
Discophrya 'cothumata, 33
- Dactylophorus, 172 - cyblstri, 33
Dactylopius cltl'i, 237-9 - !errum-equinum, 33
Dacus olea, 241 - steinii, 33
Dajldre, 72, 81-3, 156 Disguising mstincts, 14
Dajus, 72 Distomatosis, 142
- mysidis, 82 Distomum ascldia, 138
DalyeUa vIridis, 233 - cygnoldes, 138
Dana expedition, 157 - dup[tcatum, 163
Danalia, 72, 83, 156 - echmatum, 138
DANGEARD, 230, 312 - hepaticum, 136-40, 174
DANILOFF, 258 -Ianceo/atum, 137
Daphnia obtusa, 190 - leptosomum, 138, 192
DARWIN, 22, 24 - macrostomum, 137-8
DASTRE, 195, 308 - megastomum, 198
Dasyhelea obscllra, 241 - nodulosum, 138
Davamea /Tledbergi, 129 - spinu/osum, 138, 192
- te/ragona, 129 Dodecaceria caul/eryi, 171
Debab,151 - concharum, 109, 171-2, 193
Deer, 36 DOFLEIN, 13, 33, 220, 227, 232, 291, 312
Defaunation experiments, 223-6 D~I~I~I~I~I~l~l"
DEHORNE, 171, 320 DO/tUm, 10
Delma blakel, 54 DOLLFus, 163, 295
DELAGE, 87-9, 300 Donax, 145
DELCOURT, 282, 312 - vltIatus, 43
DELPEY, 306 DONISTHORPE, 290
Dendrocometes paradoxus, 33 DORIER, 118, 297
Dendrogasler, 101-2 DorocidaTis tiara, 51, ~08
- arboreseens, 102-3 Dorop),gus, 31
- astericola, 94, 102, 103 Dorylinre, 17
 INDEX 327
Dorylus.20 Elltocolle/,a mirab,lis, 56, 58-9
Double flowers. 200 Entoconchidre, 48-9, 54, 56-62, 64, 155
Dounne. lSI, 153 Entodmium, 228
DRACH, 77, 300 - eaudatium, 227, 229
Drepanosiphum, 238 Entornostraca, 65
- platanoides, 236 Entoniscidre, 72,75-81,84,109,156,194
Dromiacea, 15 Entomscus, 72
Drosophila, 282 Entomophagous insects, 119-26
DRUDE,265 - , development of, 123-6,
DUBOIS, 245, 251-2, 278-9, 310 Entovalva, 46-7
DUBOSCQ, 145-6, 172, 175,207,224,292 - majl1T, 47
Ducks, 138 - mlfabllis, 47
DUERDEN, 12-14, 288 - perrieri, 47
DuiosIs,24 - semperi, 47
Duplorbls caiathurle, 90 ENTZ, 230, 312
Dynamene, 85 Eosinophilia, 197
- b,dentata, 108 Eph,ppodonta macdougal/i, 47
Dytiscus, 32 Eplcand larvre, 69, 75,
- marginaits, 33 Eplcandre, 37, 66,68-85,87, 155-6, 158,
172-3, 199
Eplmyrma, 29
Earthworm, 132 Eplmyrma stumperi, 29
Echmaster, 94 EPIStyizs, 33
-lal/ax, 94 Eplfelphusa catensls, 31
EchmocardlUm cordatum, 6, 47, 94, 101, Epltokal annelIds, 109,171-2
193, 194,281 Eplzoanthus paraslficus, 9, 12
Eehinocheres globosus, 208 Epizoites, 32-5
Echinococcus, 129 EPIZOOtlcs, 281
Echinostomldre, 139 EplECUS pergandei, 26
Echmostomum, ~39" 194 Eqmdre, 188
Echmothnx turca, 5 Equula splendens, 251
Ecitoehara, 23 ERICKSON, 258
Ecitomorpha, 17 Eriochezr japonicus, 142, 146,203
ECltomyza, 20 ETiophyes, 210 .
Eelfon,20,23 Erythrops mlcrophthalma, 82
EctoparasltJc trematodes, 134 EsCHERICH, 19,23,290,312
Ectoprocta, 33 0;:- Euchlora, 231
Ectosymbiosls, :.:19-21 EucoccldlUm, 145
Edriolynchus schmidti, 157 - eberthi, 145
Eel, 151 Eucolla keilmi, 124, 125
Egg numbers in parasites, 158-9 Eud'plodmlum, 228-9
Elmena, 160 - maggu, 229
E,senia rosea, 252 Euizma, 49-51, 53, 56
EISIG, 38, 40-1, 43, 44-6, 297 - capil/astericola, 51
Eland, 16 - d,storta, 51
Eleagnacere, 263 - equestris, 51
Eleagnus, 263 - pollia, 51
ELENKINE, 276, 312 - ptilocrmicola, 51
Elephantiasis, 143 EulImldre, 48-56, 61, 64, 156
ELFVlNG, 257, 319 Eumedon convlctor, 5
Ellobiophrya donacis, 42, 43 Eunice gigantea, 231
Elysia vind,s, 231 Eumcidre, 40, 115-16
EMERY, 17,27,288,290 Eupagurus bernhardus, 7-9
Enchelidre, 228 - meticulosus, 92
Eneyrtusluseieollls, 165, 166, 167, 169-70 - prideauxi, 9-11, 92
ENDERS, 7, 288 ~ Eupeleteria magnicornis, 187
Bndosymbiosls, 221-55 Euphorbia pi/ull/era, 151
Engrauizs, 4 Euplectella aspergillum, 67
Enteroeola, 31 Euproetis ehrysorrhlEa, 121-2. 124, 181,
Enteropsis, 31 187, 194
Enteroxenidre, 61 Eupyrgus paeificus, 62
Enteroxenos, 49, 57, 58, 60, 60--1 Eurytoma, 29
- rentergios, 61 Eustrongylus viseeraizs, 185
Entoeolax, 49, 56-9, 58, 61, 156 Euxoa segetum, 167
- ludwigzi, 57-8
- schiemenzi, 57
- troehodotll!, 57-8, 58 FABRE,265
Entdt:oncha, 49, 57-8, 61 FAMINTZIN. 232-5,312
328 INDEX
Fasciola hepaticum, 136 Gasterosiphon deimatis, 54-6, 55
FAUCHERON,237,312 Gasleroslomum fimbria/um, 138
FAURE-FREMIET, 32-3, 289 Gastrophilus equi, 189
FAUROT,10,289 Gastropods, adaptations to parasitism
FAUSSEK, 117, 306 in,46-64
FEARNSIDES, 309 GAiliIANN, 320
Fecampia, 185 GEAY, 5
FEDZCHENKO, 143 Gebia, 86
Fegatella, 275 Geese, 138
FERBER, 228-9, 312 Genes, 277
Fierasfer, 30-1 GENEVOIS, 233, 312
FIlaria, 185 Geophilus, 172
- bancrofti, 143-4, 148, 184 GEORGEVITCH, 233
- grassi, 144 Gephyrea, 33
- Immitis, 144 Gerardla, 93, 94, 98
-loa, 143 Geryomdre, 161
- medmensis, 142-3 GIARD, 6,13,68-71,74,77,79,80,82,89,
- nocturna, 143 100,156,162,167,172-3,192,198-201,
-'pertans, 143 204,207, 209, 242, 244, 281, 289, 295,
- volvulus, 143 300-1, 304, 313, 320
DE FILIPPI, 193 GIESBRECHT,299
FISCHER,47 GIlruth, cysts of, 207
FISHER, 94, 300 GIPSY moth, see Lymantria dlSpar
FISKE,304 Glochidium larva, 116,117,205-6, 209
Fixation, organs of, 29, 37, 41-4, 117 GlomeTls, 163
Flabellicola, 105 Glossina, 35, 150, 151, 177-9, 243
Flagellata, 145 - morsllans, 150
- , symbiotic, 222-7 - palpabs, 150
Flagellosis, 151 Glugea, 207
Fleas, 36, 130, 150 Glyp/us scalplus, 24
FLEMMING, 116 Gnath,a, 36, 66, 113
FOA,313 • - maxillaris, 67
FOREL, 17, 22, 24, 25 Gnathiidre, 65-7
Formica consoclUS, 25 Gnathomysis geriachei, 8
_ fusca, 19,25, 26,242 Gnathosyllis diplodonta, 42
- incerta, 25 Gnomoniscas, 83
- pratensis, 25 Gnorimoschema salinaris, ,167
_ rufa, 17, 25, 129, 254 Goldfish, 137 .
_ rufibarbis, 20, 25-6 GOLDI, 219, 313
_ sanguinea, 18, 20, 25, 27 GOLDSCHMIDT, 203, 320
- trunclcola, 25 GOMEs. 304
Formicoxenus nitidulus, 17,25 Gonospora longissima, 171-2, 193
FORSTER, 186, 298 GONZALEZ, 140
FOWLER, 93-4, 97, 300 Gordian worms, 118-19. 144
Fox, 175 GordlUs.119
FRANK,263,273,312 VON GRAFF, 233, 295
Free-martin, 203 GRASSE, 220, 222, 224, 226, 287, 313
Frog, 138, 151, 190 GRASSI, 134, 147,292,295,313
Frontonia leucas, 231 GRAVIER, 6, 105, 289
FUHRMANN, 133, 164, 295 Green bodies, 191, 236
Fulgoridre, 239 Gregarines, 145, 171-2. 193, 206-7·
Ground nuts. 177
Gryllomorpha, 206
Galathea, 5, 86 Gudgeon, 131
GALIPE, 278, 310 GuRNEE,21
Gall formation, 126,207-16 GUlLllERMOND, 284, 313
GALLAUD, 264-5, 272, 319 Guinea worm, 142
Galleria melonella, 17 GUYENOT, 202, 312-13
GALLIEN, 135, 295 Gyge branchialis, 204
Gallinacere, 138 Gyrocotyle, 132, 162
Gamasidre,244 Gyrodac/yius eiegans, 164
Gambier Islands, 4, 5
GAMBLE, 233, 235, 314
Gammarus, 32-3, 144 HADZl, 233, 313
GAN1N,124 HAECKEL, 57 ,
GARNAULT, 242 Hamatocieptes /erebellidis, 115
GARNHAM, 294 Hamatopinus spinuiosus, 150
Gasterosiphon, 49, 53, 53-9, 61 Hamocera dana. 110,111
 INDEX 329
Hremotlagellata. 146. 148-50. 152 Heteroteuthis dlspar, 248
Hremogregarma:. 148 Heteroxenous parasites, 127-53
Hremophilous glands. 44-5 Hexacanth embryo, 128, 131, 134
HO!moproteus columbO!, 147-8 Hexacorallia, 231
- noctuO!, 148 HEYMONS, 144
HO!mopsis sangumea, 242 Hippobosca, 36
Ha:mosporidia, 146-9,152,159,172,175, Hippoboscidre, 243
184 Hlpponoe, 31
Halecium ophiodes, 231, 233 HlppophO!, 263
Halzchondna, 34 HlRASE, 63, 208, 306
HallOtls, 31 HIrudinea, 40, 44. 148. 155
HALLEZ, 295 Hirudo medicmalis, 242
HAMANN,233 Histeridre, 18
HANSEN, 172, 208, 301 Histriobdella homari, 34
Hapalocarcinus marsupialls, 5, 208 HOFMANN, 192, 296
Haplosporidllun potamillO!, 207 HOLLANDE, 308
Haplosylliy.£ephalata, 40 Holostomida:, 139
Hare, 145 __ Holothuria curiosa, 47
HARGES,66 Homeopraxy, 124
HARMER, 169, 320 Homochromous commensals, 5
Harmothoe c(J!liata, 7 Hornea, 270-1
HARMS, 25, 116-17, 306, 313 HORNELL, 193
HARTMANN, 160-1,295 Horse, 36, lSI. 175-6, 178, 189
HARVEY, NEWTON, 245, 251, 313 - , immumty m, 196
HATCH,320 Host, defimtive, 127, 152
HATT, 145-6,292 - , intermediate, 127. 152
HAYASHI, 249, 313 Host-parasite eqUlhbrium, 181
HAYCRAFT, 38, 308 Hosts, exceptIOnal. 182
HEATH, 33, 62, 289, 306, 308 HOUARD, 210, 310
HECKERT, 296 , HOVASSE,313
Hedgehog, 138, 192 HOWARD, A. D., 307
HEDING, 58-9, 306 HOWARD, L 0.,304
HElM, 220, 313 HUBER, 22, 219, 290, 313
HellOphrys, 230 HUNGATE, 222. 226, 228-9, 313, 314
HelIozoa, 230 HUXLEY. 236, 314
Helix carthusianella, 129 Hyas, 14
- hortensis, 138, 192 Hydnophytum, 27
- nemoralzs, 138, 192 Hydra. 235
HELLRIEGEL, 262 - VIridis, 231-3
Helobdella, lSI Hydractinia, 9, 33
- alglra, 190 - echmata, 7
Helotism, 258 HydrochO!Tlls capybara, 176
Hemiclepsls, 151 Hydrophllus plceus, 33
Hemiomscldre, 72 Hylaslmus obscurus, 200
Hemioniscus, 156 Hylecll!tus, 221
- balani, 68, 82-5 Hymenolepis, 153, 162
Hemiptera, 35, 150 - brachycephala, 129
HENNEGUY, 241, 303 - dimmuta, 129
HepO!tozoon perniclOsum, 148 - [raterna, 134" 175
Hepaticre, 263, 270, 275 - murina, 134
Hepatus chilensis, 12 - nana, 134, 174-5
HERDMAN, 193 - uncinata, 129
HermaphrodItism, 154-6 Hymenoptera, 119-20, 122-5, 165-70,
Hermit crabs, 7-15, 8 210,213,217-18,221
HERPIN, 47, 306 - , polyembryony in, 165-70
Herpyllobhdre, 104 - , primary larva: of, 125
Herst/iodes, 6 Hypera punctata, 181
HERTWlG, 217, 310 Hyperina medusarum, 4
HESIOD,22 Hypermastigma, 222
HESSE, 66, 172,207,292, 301 Hyperparasltes, 72, 83, 122
HetO!rius, 17-19 Hyphantria cunea, 194
Heterocentrotus mamillatus, 5 Hypoborus ficus, 123-4
Heterocirrus fimbnafus, 171 Hypocoma ascidlarum, 33
Heterocyathus, 5 HypoderO!um conaideum, 138
Heterodera, 200, 210 Hypoderma bovis, 189
- radicicola, 210, 211 Hypono~euta cognatel/us, 165, 166
Heteropsammia, 5 - mahalellus, 165
- cochlea, 6 - padel/us, 165
330 INDEX
Hypsagollus quadricomis, 33 KEEDLE, 233, 235, 314
Hystenacere, 256 KElLIN, 124-6, 188, 198, 241, 298, 304
KELLEY, 320
KENDALL, 136, 174
Icerya purchasi, 121,237 Kentrogon, 88
lchneumonid;:e, 119, 123 KEPPEN, 160-1
Ichthyocodium sarcotreti, '33 Kermlmcola, 239
Ichthyonema, 142 KEYES, 50, 307
Ichthyotomus. 38 Kinase, 195
- sangumarius 40-6, 41, 43 Klossla, 145
Ichthyoxellus, 67, 155 KLUGE,94
VON IHERlNG, 28, 219, 290, 314 Knautia arvensis, 199
Imbauba,28 KNIPOWlTSCH,94, 102,301
Immunity in commensals, 3, 4 KNOP, 252
- in horses, 196 KOCH, 116, 150-1,253-4, 314
Illachus, 145 KOEHLER, 49-52, 54-5, 208, 307
- mauTltamcus, 89, 201, 202. 203 KOENIG, 219
- scorpIO, 89, 201 KOFOID, 222, 224
Infusonforms, 160-1 1(ORSCHELT, 94, 301
Infusongens, 160 1(ossMANN, 79
Ingolf. expeditIOn, 97 1(OVALEVSKY, 297
Inqudmism, 30-5, 46-7 KRAMER,303
- , defimtlOn of, 1 1(UCHENMEISTER, 128
I ntermittent paraSites, 35-36, 1(UKENTHAL, 144, 307
IOlle, 72 1(uNCKEL, D'HERCULAIS, 124
- thoracica, 70, 75-6 1(usTER,310
Iomn;:e, 72-3, 75
IRMISCH, 265
Isaria, 280-1 Labidognathus parasitic us, 115
Isopoda, 65-6, 85 Labrorostratus paraSIticus, 115-16
Isosoma grammicola, 210 LACAZE-DuTHIERS, 93-5, 98-9, 242, 301
Isotrichza, 228 Laemlla setoslssima, 6
Isotnchidre, 228 LAFONT, 151,314
ISSATCHENKO, 245, 314 LAGUESSE, 284, 314
Itura aurita, 231 LAMEERE, 160, 164,295
ITURBE, 140, 296 Lamel/aria, 35, 63
IVANOV, 51-2, 62-3, 307 Lamellarndre, 63
Ixodes, 244 Lame1hbranchs, adaptation to parasitism
Ixodldre, 151 in, 46-7
Lamellicorn beetles, 221
Jackal, 142, 175 Lampsi"s anodontoides, 205
JAMESON, 193, 308 - luteola, 205
JANET, 23, 290 LampYTis, 246
JANICKI, 297 - noctduca, 246, 251
Janthinosoma lutzi, 189 LANG,16
JASCHKE,314 LANKESTER, RAy, 230
Jassid;:e, 239 LaTUS argentatus, 137
JAVELLY, 241 LasidlUlD larva, 118
Jigger, 189 Lasiocampldre, 195
Jamla annectells, 224, 226 Lasius flavus, 19
JOHANNSEN, 277 - !u"ginosus, 17
JORDAN,18,290 - niger, 19
JOST,304 Laura, 100
JOYEUX, 175, 296 - gerardue, 93-4, 98
JULlEN,309 LAURENT, 262
JULIN, 249, 314 Lauridre, 94, 98-9
JUMELLE, 220, 314 LAVALLEE, 115,294
JUNGERSEN, 33, 289 LAVERAN, 147-8, 174, 196, 206, 292, 308
LEACH, 36, 38, 150
Leaf-cuttmg ants, 219
KAISER,297 Leander, 204
Kala azar, 151 Leander serratus, 73, 205
Kalotermltidre, 223 Lecamidre, 239
KAMiENSKI, 263, 265 Lecallium corni, 238
Kamptozoa, 33 - olere, 121
KARAWAlEW, 314 LE CERF, 290
Karyolysus lacertarum, 148 LE DANTEC, 231, 315
KATHARlNER,296 LEFEVRE, 307
 INDEX 331
LEGER, 145-6, 151-2, 172, 175, 193,206, LoEB, J., 215, 282
292 LOEB, L., 38, 298, 308
Leguminosre, 214, 221, 262-3 £olmia medusa, 7
LEIPER, 140, 296 £Oligo forbesi, 246
Leishmaniasis, 151 Lomechusa, 17-19,22-3
Lelaps echidmnus, 148 - strumoi' 18, 20
- equltans, 17 Looss, 1 185-6, 196, 298
Lelio-Cattleya, 272 LophlUS p atorius, 157
Lemna, 33 Loxosoma, 33
Lepas, 31, 87 Lucanidre, 221
Lepldasthenza dlgueti, 6 Lucerne, 268
Lepidoptera, control of, 120 Luciferase, 245, 252
Lepldosteus, 205 Luclfenn, 245, 252
Leptinotarsa decemlineata, 120 Lucilla argyrocephala, 188
Leptodlscus, 230 - serzcata, 188
Leptomonas, 152 Lucinidre, 46
- davld" 151 LUDWIG,307
Lepton, 47 Lugworm, see Arenicola
Leptorza, 208 LUHE, 186,296,319
Leptothorax emersoni, 26 Lumbriculus, 162
- mgriceps, 29 LumbriCUS terrestris, 242
Lernrea, 107, 158 LUMIERE, 310
Lernreodiscus, 86 Luminescence in animals, 244-52
LE Ror, 94, 102,301 - I n cephalopods, 278-9
Lestoblosls, 25 Lund's larva, 188
LETELLIER, 260,319 LUNEL, 4, 289
Leuciscus erythrophthalmus, 138 LUTZ, 140-1, 296
LEUCKART, 159, 287, 296, 298 LWOFF, 43, 292
Leucochloridium paradoxum, 137-8 LycO!na. alcon, 22
Leucocytozoon cams, 149 - euphemus, 22
LEYDIG, 117, 237, 315 Lycrenidre, 21
LeydlOpsis sphO!rica, 223, 225 Lychms dlOlca, 204
Lice, 130, 150, 175 Lycopodlacere, 263, 275
Lichenopora, 169 Lycopodinre, 270
Lichens, 217, 256-61 LycopodIum, 263, 275
LICHTENSTEIN, 123, 304 Lyctldre, 241
LIEBIG,262 Lymantria dispar, 121-2, 181, 187, 195,
Ligula simplicissima, 131 203
LILLIE, 203, 320 Lymexylonidre, 221
LlmnO!a, 33 Lynchia, 36
- humllzs, 174 Lynchia maura, 148,243
- lzmosa, 138 Lyperosla, 243
- minuta, 174 Lyponysslls saurarum, 148
- stagna[zs, 136, 138, 174 Lyslosqllllla, 6
- truncatula, 136, 138, 174
- viator, 174
Limnerium validum, 194 Macaque worm, 189
Limnodrzlus, 207 Macrocentrus gifuensis, 167
Lmckia, 48-9 Macroergates, 197
LINDNER, 237 Macrura,72
Lznguatula serrata, 144-5 MAGNUS, 213-14, 272, 310
Llnguatuhda, 144-5 Magpie 16
LINNAlUS, 22 MAGRou, 270--1, 275, 319
LINSTOW, 287 MalO,14
LINTON, 137, 296 Mal de caderas, 176
Liptotena, 36, 243 Malacobdella, 31
Llriopsidre, 72, 83-4 Malacostraca, 65
Lmopsis, 83, 156 MALAQUIN, 7,40,110,289,301
- pygmO!a, 199 MALARD,47
Lissocarcmus orbicularis, 5 Malaria, 147-8, 179, 184
LlIhocolletis, 166 Males, complemental, 156
LlIhocystls schneideri, 193, 194, 281 - , dwarf, 72, 80, 99, 155-8
LlIomastlx gelechlO!, 167 - , parasitiC, 157
- truncatellus, 167 Mallophaga, 244
L,ttorzna lzttorea, 137 MALPIGHI,212
Llverfluke, see Dlstomllm Man, 36, 128-31, 134, 137-44, 174-5,
L,XUS, 200 177-9, 185-6, 189
Loa-loa, 143 MANDAHL-BARTH, 56, 60--1, 306-7
332 INDEX
MANGAN, 233, 315. Miracidium, 136, 137
MANGOLD, 230 Mitochondria, 283-5
Manna, 22 MIYAlRI, 139,296
MANSON,143 MbBlUS,12
MANSOUR,315 Modifications in paraSites, 36-9
MARCHAL, 124-5, 165-7, 169, 180,304 Molgu/a, 242
MARCHOUX, 284 MbLLER, 219, 256-7, 259,315, 319
Margantana, 116 MOLLIARD, 199, 200, 211, 214-15, 266,
MARIAT, 268, 275, 319 310
Marphysa, 116 Mollusca, adaptations to parasitism in,
MARTIN, E. A. 171-2,320 46-64
MARTIN, L. 284 MONlEz, 237, 315
Mastotermitidre, 223 Monocentrus japonicus, 251
MATHIAS, 139, 296 Monocercus, 129
MATInS, 293 Monocystidre, 172
Matricaria modora, 199 Monocystis agiUs, 207
MAYER,301 MONOD, 66, 301
Mayfly, 138 Monogenetic trematodes, 134-5
MCCALLUM, 147, 293 MonomoYlum salomonis, 26
Measly pork, 128 Monospora,207
Megadenus, 49, 51, 208 Monsfrlila danl1!, 110
- arrhynchus, 51-2, 208 - helgolandica, 110
- cystlcola, 51-2 MonstrillIdre, 108-13, 109, 111, 114-15,
- holothuricola, 51 117, 126, 173
- vlEltzkoWI, 51 Montacuta !errugmosa, 6, 47
Megaptera, 34 MONTALENTI, 226, 315
MEISSNER, 249, 315 MONTGOMERY, 298
Melania, 137, 142 MORDWILKO, 290
- libertina, 138 MOREAU, 259, 319
Melia, 14, 86, 92 MORTARA,248,315
- tesse/ata, 12, 13 MORTENSEN, 47, 208, 301
MeLIN, 320 Motacilla flava, 16
Melophagus, 35, 243 MOToMURA, 296
MeRCIER, 208, 241-2, 293, 307, 315 Mouse, 129, 138, 142
Mergus, 131 MOUTON,261
Mermis, 197 MRAZEK, 133,309
MesNlL, 68, 84, 106, 109, 152, 171, 174, Mucronaba, 49, 52-3, 56
182, 190, 193, 196, 206-7, 292-3, 295, - palmipedis, 52
308, 320 - variablits, 52
MesojlEma annectens, 226 MUDROW,315
Messor barbarus, 25 MULLER, F. 27, 219
MetabolIsm, modificatIOns in, 197-8 MULLER, J. 56, 58, 307
Metacercaria, 139 Muller's bodies, 27
Metacrinus rotundus, 94, 96 Munida tentamana, 119
Metatermltidre, 219, 222 Murex trunculus, 279
METCHNIKOFF, 236-8, 281-2, 315 Muscldre, 36, 130
Metopma pachycondylte, 20, 21 Mutualism, defimtion of, 1
MEYERHOF,137,296 Mya, 31
Mlcana sCintillaris, 17 MYiASHITA, 203, 301-2
Mlcellre, 277 MyiaSIS, 126, 187-9, 209
M,crococcus luteus, 262 Mycetocyte, 237, 238-9, 243, 249, 252
Mlcrodon mutabllis, 17 Mycetomes of Insects, 235-42, 246, 281
Microfilaria, 143 Mycorrhlza, 263-76
Mlcroniscan larvre, 69, 70 MyrlOcladus, cypris larva of, 95
Mlcroniscus, 70 Mynoc/adus arborescens, 94
Micropterus sa/mono Ides, 205 - astropectmis, 94, 102
Mlcroscolex phosphoreus, 252 - ludwlgil, 94
MlcrosporidIa, 190, 281 - okadai, 94, 102, 103
Mlcrozymas, 277-8 Myriotrochus rinkli, 57
Millepora, 233 Myrmecodia, 27
M!lleporina, 231 Myrmecophlla, 17
Mlmeciton, 17 Myrmecophilous insects, 16-27
- pulex, 20, 24 - plants, 27-29
MINCHIN, 152,292 Myrmedoma!unesta,17
Miners' anremla, 185-6 - humeralts, 17
MINKIEWICZ, 14,289 Myrmica, 19
MINNE,252 - brevmodis, 26
Mmous inermism, 33 Myrsinacere, 263
 INDEX 333
Myrus vulgaris, 40, 41 Nycteribidre, 187, 243
Mysis, 83 Nyctotherus, 35
Mytilis, 145 Nysius euphor/Jite, 151
- edulis, 146
Myxobacteria, 262, 285
Myxocystls, 207 OBERTHUR, 22, 291
Myxomycetes, 261-2 Odontoglossum, 273
Myxospondia, 184 - grande, 268
Myzostomarta, 37,40, 155-6, 208 Odontosyllis ctenostoma, 115
Odontotermes, 219
Odostomia, 48
Nabis latlventris, 17 - rissoides, 48, 110
NADSON,261 (Ecophylla smaragdma, 13
NAGAKAWA,296 <Estridre, 38, 120
Nagana, ISO, 176 (Estrus, 178
NAGELI,277 - OVIS, 189
Nais,162 OKADA, Yo K. 93-7, 100, 102-3, 203,
NALEPA,303 251,302,315
Narcomedusre, 161 Oligognathus bonellite, 115
Naucrates ductor, 2 - parasitlcus, 115
Nauphus of Sacculi"", 87, 88 Ollulanus, 142
Nectonema, 118-19 Onchocera volvulus, 143
- munidte, 119 Onchosphere, 128
NEILSON-JONES, 320 Oncomelania nosophora, 141
NEIVA, 189, 304 Oocyst, 148
Nematocystis magna, 207 Oolunete, 148
Nematocysts, 4 Ooneides, 31
- , immumty against, 3 Oospora, 239
Nematoda, heteroxenous, 142-4 Opaizna, 35, 38
Nematogens, 160 Opercularia, 32
Nematopsis, 145 Ophiocten sericeum, 94, 97
- legeri, 146 OphlOdromus herrmanni. 6
Nematus, 213 OphlOglossacere, 270, 275
Neoteny, 132, 134-6 Ophloglossum, 263, 265, 268, 270
Neottia nidus-avis, 266, 270, 274 Ophoseldes, 31
Nephromyces, 242 Ophrydium, 269
Nephropsis, 33 - versatile, 231, 233
Nepticula fiosculatella, 282 Ophryodendron annulatorum, 33
Nereilepas, 21 - serwlante, 33
- fucata, 7-9, 8 Ophryoscolecldre, 35, 228
NEUMANN, 303 Ophryoscolex, 228
NEVEU-LEMAIRE, 287 - caudatus, 227
Newt, 138 Opisthobranchia, 61
DB NIcEVILLE, 21 Orasema, 124
NIENBURG, 319 Orcheomycetes, 269
Nitlduhdre, 18 OrchidS, germmatlon of, 265-75
Noctiluca, 230-1, 245 - , mycorrhlza of, 264, 265-76, 273
Nodules and bacteria, 262-3 Oriental sore, 151
NOE,298 Ornithodorus, 244
NOIROT, 224, 226, 313 - moubata, 178
Nomeus gronovii, 4 OrnithomYla. 36
Nonagria typhte, 281 - aVlculana, 243
NORMAN, 93-4, 97, 301 OrthonectIda:, 1l3-1S, 155,161,166,169,
Nosema, 281 172
- anomalum, 207 Orycteropus, 36, 178, 188
- bombycis, 190 OryzO!phllus surinamensis, 254
- incurvata, 190 OSIDMA, 47, 307
Nostoc peltlgerte, 260 OSTROUMOFF, 293
Notodelphys, 31 Oxpecker, 16
Notonecta, 32 Oxymonas projector, 224
Notophryxus, 72
NOUVEL, 161, 295
NOVIKOFF, 246, 315 Pachycondyla vorax, 20, 21
Novius cardinalzs, 121 Predophoropldre, 48-9, 62
Nudibranchs, 35 Ptedophoropus, 49, 56, 64, 156
Nudiclava monacanthi, 33 - dicO!lobius, 62, 63
NUTrALL, 282, 303,315 Paguridre,2, 7-15,8,11,72-3,119
Nychla Cirrosa, 6 Pagurus angulatus, 9
334 INDEX
Pagurus, asper, 10 Peri/ampus, 124.125
- brevlpes, 8 . PERINGUEY, 19
- deformls, 10 PERON, 249, 316
- longicorpus, 76 Peronospora radII, 199
- pilosimanus, 9, 11 - vlOlacea, 199
- slrlatus, 9 Peronosporere, 265
PAILLOT, 167, 304, 311 PERRIER DE LA BATHIE, 220, 314
Palamonetes, 119 PETCH, 220, 316
Paludina, 33 PETERS, 293
PANCERI,315 Petrarca bathyactidis, 94, 97
Pangenes, 277 Petrarcidre, 94, 97
PANOUSE, 205, 302 PFITZER, 269
PANTEL,187 Phacocharus, 36, 178, 188
Papaver dublUm, 215 PhagocytosIs, 193-5
- rhaas, 215 PhalanopslS, 267-9
Parabiosis, 25, 257 Pheasant, 129
Paracopidosomopsis /loridanus, 167 Pheidole, 19
Paragonimus westermanm, 138, 142 - commutata, 197
Paramecium bursarla, 231-3 Phelba, 12, 14
Parasitism, definitIOn of, 1 Phllobrya, 118
Parasitosylfls, 40 Phlebotomus, 150-1
Parexorista cheloma, 181, 187 Pholas, 31
PARK.ER, G. H. 289 - dactylus, 245
PARKER, H. L. 167, 304 Phormia, 36, 188
Parorchis avltus, 137 - azurea, 188
Parorgyia antiqua, 195 - $ordida, 188
ParthenogenesIs, 163, 210, 215 Phormosoma uranus, 208, 209
Parthenopea, 86 Photoblepharon, 251
PASCHER,235 Photocorynus spmiceps, 157
Passeromyia heterochata, 188 Phromma, 31
PASTEUR, 34, 190,281-2 Phryxldre, 72-6,
Patella, 231 Phryxus, 72-3
PateUanacere, 256 - paguri, 204
PATTERSON, 167, 304 Phthmus PUbiS, 244
Paulmella chromatophora, 235 Phy/loglossum, 263, 275
Paussidre, 18, 19 Phy/lomyza formica, 17
Paussus favler, 19, 20 Phy/loxera, 120
- turcicus, 19 Physa, 138, 140
Pearls, 193 Physalia, 4
Pebrine, 190, 281 Physcia parletma, 258
Pecten, 48 Physocephalus sexalatus, 142
Pedlcellaster, 62 Physogastry, 23-4
Pediculus humanus capitis, 244, 255 Phytocecld, 208
- - corpOTlS, 244, 254, 255 Phytonomus posticus, 181
Pegomyia, 124 Phytoptus, 210
PELLEGRIN, 289 Phytothylacies, 208
PELSENEER, 47-8, 110, 302 Phytozoon, 234
Pelseneerla, 49, 51 PICARD, 123, 304, 320
- media, 51 PIERANTONI, 225-6, 236-8. 240, 245-52,
- minor, 51 276,278-9,316
- profunda, 51 Pierls brasslca, 121, 167
- stylI/era, 51 PIERON, 27, 291
Peltigera, 260 Pig, 128-9, 142, 178, 186
Peltigeracere, 259 Pigeon, 148
Peltogaster, 83, 86, 90, 92, 204 Pike, 130, 138
- curvatus, 199 Pilot fish, 2
- paguri, 91 Pilumnus, 92
- socialis, 92, 165 - hirte/lus, 74
Peltogasterella sociafls, 165 Pmctada margaritijera, 48
Peltogastridre, 92 Pmnepedm, 144 -
Peneroplis pertusus, 230, 233 Pinnotheres pisum, 80
Pentastorruda, 144 Pinnotherion vermlforme, 80
Perch, 131, 138, 142 PINOY, 261-2, 319
PEREZ, CH., 8, 30, 47, 91-2, 119, 207, PlOnodesmotes phormosoma, 208, 209
288-9,293,298,302 PIroplasma, 190
PEREZ, J. 200, 309 Piroplasmosis, 151
Periclimenes, 4 Piscicola geometra. 244
Perigonimus puge/ensu, 33 Pisidium. 138
 INDEX 335
PITOTII, 76, 302 Porpila, 231
PlacentatIOn, parasitic, 112-13, 117, 125 PORTIER, 278, 280-5,311,316
Placobdella catenigera, 244 PorlunlOn, 72
Plague bacillI, 184 - jratSSel, 172
Planidium larvae, 124, 125 - kossmanni, 77, 79, 80
Planorbis, 138, 140 - mrenadls, 68,77-80,77,78,79
- centrimetralts, 174 Portunus, 145, 175
- corneus, 138 - depurator, 146, 198
- guadalupensis, 174 - holsalus, 172, 173
- olivaceus, 141, 174 Polamtlla lorelll, 207
Plant parasItes, mIgrations of, 153 POlamon, 138
Plasmodiophora brasslcre, 261 - obtuslpes, 142
PlasmodIUm, 147-8, 176, 182, 184 POTTS, 261 •
- cynomolgi, 149 POTTS, F. A. 5,40, 91, 204, 208, 289, 297
- malarlre, 184 Pourlalesia jejJreysi, 94, 101
PLAn, 30, 289 Praniza, 66, 67, 108
Plalyarlhrus hojJmannseggii, 17 PRENANT,241
Plalyceras, 49 Priapion, 72, 173
- mopmalum, 50 PRILLIEUX, 265, 272
Plalygasler, 124, 125 Primary larvre of Hymenoptera, 125
- rubi, 167 PTimula o./ficmabs, 199, 200
Plalyonychus lallpes, 77, 80 Princesse-Altce expedItion, 51
Platypodidre, 221 PRINGSHEIM, 232
Pleclridium cellulolylicllm, 230 ProcerCOid larva, 130--132
PlerocercOid larva, 130-2, 133 Proctodeal food, 226
Pleuroerypla, 173 Proctotrypidre, 119, 124
Plusia gamma, 167 Proctotrypoidea, 165
POCHON, 239, 316 Pro geneSIS, 163
Poell/opora, 4, 5 Protelean parasitism, 67, 108-26
- ccespilosa, 208 Proleosoma, 147, 176
l'odascon, 83 Protista, 174
Podasconidre, 83 Protocalbphora, 36, 188
Podocoryne, 9, 33 Protococcacere, 256
Polta involula, 34 ProlococCUs, 233
POLIMANTI, 289 - ophrydli, 233
Pol/ema rudis, 126, 188, 194 Protocorm, 267
Polycercus, 162 Protozoa,35,221-9
Polychretes, adaptation to parasitism in, - , gamogony In, 159
40-46 - , heteroxenous, 145-53
Polyelrrus, 104-7, - , schizogony in, 159, 160
- aremvorus, 106,209 Pselaphidre, 18
Polydecles cupllii/era, 12 Pseudione /raissei, 83
Polydora glQrdi, 109, 110 Pseudogyne, 18
Polyembryony, 164-70 Pseudomyrma, 29
Polyergus rujescens, 26 Pseudo pallium, 51-3, 55-8, 62, 64
Polygnolus mmulus, 166, 169, 170 Pseudosacculus okai, 63
Polymastlgina, 222 Pseudova, 191, 236
Poiymnia nebulosa, 206 Pseudovilellus, 191, 236
Polyonyx, 7 PsillomYla, 20
Polyplaslron, 229 Psilostomidre, 139
Polypodlum hydri/orme, 161 Psilotrema splculigera, 138-9
Polystomum mtegerTlmum, dimorphIc Psi/olum, 263, 275
development in, 135-6 PsychodIdre, 151
Pontania, 213 Psyllidre, 237-8
- proxima, 213 Pterocephalus, 172
Ponlobdella, 151 Pleromalus egregius, 122, 124
Pontoma, 30-1 Pteropus, 187
Pontonndre, 5 Plllocrmus pmnalus, 51
Ponlophllus, 119 Plychodera, 6
Porcellana, 86 Plyelus lineatus, 239
- longlcorms, 173 Puccmia grammis, 153
- platyeheles, 173 - violre, 199
Porcellamdre, 76 Pulex Irrilans, 175
POTlles, 4 - serratipes, 129
Porocephalus armlllalus, 144-5 PullcarlG dysenterica, 200
Porospora, 145 PUNTONl, 248
- gigantea, 145-6 PUTNAM,237
- porlunidarum, 146 Pycnochylrium aureum, 210
336 INDEX
Pycnogonids, 35 Rhodotorula ruhra, 275
Pycnosoma bezzianum, 188 Flhombogens, 160
PYEFINCH, 94, 302 Rhopaiona, 172
Pyralls, 167 Rhopaiura julini, 155
PyramldeJlidre, 48 - ophIOCOmll!, 113, 114, 115, 161, 199
Pyrenomycetes, 256 - peiseneerz, 155 -
PyrimidIne, 268 Rhozites gongyiophora, 219
Pyrophorus nocti/uca, 245 Rhyncocystis pi/osa, 207
Pyrosoma, 31, 249, 279 Rhynia, 270
- glganteum, 250 Rickettsia, 244
Pyrsonympha vertens, 224 RIES, 254, 311, 317
Pyxinia jrenze/i, 206 RILEY, 121
RIpPER,317
Roach,131
Quedius brevis, 17 Robillardia, 49
Quercus, 210 RODHAIN, 187, 305
Rondeietia, 278
- mmor, 247, 249
Rabbit, 129-30, 145 ROSEN, 130-1, 175, 296-7
RadlOlana, 230, 234 Rosenia, 49, 51
RAILLIET, 287 Ross, RONALD, 147. 293
RANDALL, 62, 308 ROTHSCHILD, 137,296
RANSOM, 186,298 ROUBAUD, 143, 152. 176-80, 188-9, 205,
Rat, 129, 142, 145, 149, 175, 189 243-4, 293, 298, 305, 309, 317
RATHKE,204 ROVELLI, 134,295
RaumparasltJsmus, 30 Rubiacere, 263
RAYNER,320 Rummants, bactena in, 229-30
REAMUR,22 - , ciliates In, 227-9
Reciprocal reactions of host and parasite,
192-216
Recurrent fever, 184 SABATINr, 38, 303
RedIa, 136-7, 166 Sabina, 167
Reduviidre, 150 Saccharomyces, 239
REESS, 257, 319 Saccuizna, 83, 85-90, 86, 88, 90, 92-3,
REGAN, 157, 320 104,107,110,112,158,165,173,185,
REGAUD, 284,317 197-9, 201, 202-3
REICHENOW, 229, 317 Saffron, 268
REICHENSPERGER, 319 Sagartza, 12, 14
REINHARD, 76, 80, 302 Sagitta, 142
REINKE, 259, 319 DE SAINT-JOSEPH, 7, 115-16,290,297
REISSEK, 265 Salep, 267
Remora, 2, 3 Salix amygdalina, 213
Reproduction In parasites, 154-70 Salmacina, 110
ReservOIr of infection, 176 Salmonidre, 130
Rellculotermes jiavipes, 223,225 SANSIN, 80, 302
- luczjugus, 226 SARASIN, 50, 54, 308
REUUNG, 205, 308 Sarcanthmere, 269
REUSS, 163, 296 Sarcocystme, 196
REVERBERl, 76, 80, 302 Sarcophagidre, 120
Rhabdonema mgrovenosum, 155 Sarcopsylla penetrans, 189
Rhinoceros, 16 Sarcosporidla, 196
RhmotermltJdre, 223 Sarcotretes scopeli, 33
Rluplcephalus, 144 SARS, 70, 83, 172,299
- sanguineus, 149, 190 Sarsia, 231
Rhizobium radlcicola, 214-15 Scabiosa columbarta, 200
Rhizocephala, 38, 65, 72, 83, 85-93, 112, Scalpellum, 34
155, 165, 173 SCHACHT,265
- reproductIOn In, 165 SCHAUDINN, 148, 160,223,293-4,317
Rhizoctoma, 266-74, SCHEPMAN, 308
- lanuginosa, 268, 271, 273 SCHEWIAKOFF, 232
- mucoroides, 267-8 270-1 SCHIEMENZ, 56-7, 308
- repens, 268, 271 SCIDMKEWITCH, 90
- vlOiacea, 268 SCHIMPER, 27
Rhizostoma, 231 Schistosoma, 186
- cuvleri, 4 - hovis, 142
Rhodztes, 213 . - hll!matoblUm, 138-41, 140
Rhodmus, 150 - japonicus, 141
- proiixus, 222, 282 - mansoni, 141, 174
 INDEX 337
Schistosomidre, 139, 141 SMITH, GEOFFREY, 89, 90, 92, 197, 201-3
Schizogamy, 162 302, 309
SchizogenesIs, 162,171 SMITH, H. S. 125, 305
Schlzosaccharomyces aphidls, 237 Snake, 144-5
Schizotrypanum crUZI, 150 Social insects and symbiosis, 217-18
SCHLOESLlNG, 262 Solaster, 94
SCHMARDA, 42-3 Solen, 145
SCHNEIDER, 317 Solenopsls, 20, 25
SCHWANZWITSCH, 58, 308 -fugax, 17
SCHWARTZ, 229 Solonna, 260
SCHWARTZ, VV. 241, 317 - saccata, 257
SCHWENDENER, 217, 257-8, 319 Sordaria ./inicola, 275
SClOberetw, 47 Soredla, 256
Scolopendra, 172 Souma, 150-1
Scopelus, glacwils, 33 SpeCifiCity In parasites, 171-91
SCOTT, 302 SPENGEL, 115,297
Scutelilsta cyanea, 121 Sphrenacere, 275
Scytonema, 257 Sphcerocybe concentrica, 275
Sea anemone 3,4,9-15,11,13 Sphceroma, 69, 158
SEKERA. 233 Sphreromidre, 85, 108
SelyslIlQ perforam, 207 Sphcerozoum, 230
SEMPER, 5, 31,47, 51,208, 290, 320 Sphcerularla bombi, 158, 159
Senecio jacobcea, 200 Spinax,90
Sepietta owemana, 247 SplO meczmkovlOnus, 115
Sepiola, 278 Spirachtha, 23-4
- mtermedla, 247, 249 - eurymedusa, 23
Sepiolidre, 247-8 Spirocerca sanguinolenta, 142
SERGENT, 148, 151, 178-9,294, 305, Splrochretes, 190
Serlalopora hystrix, 208 Spiroptera obtusa, 142
Sertularia, 33 Splfotrichonympha k%idl, 224
Sesarma, 138 Splenomegaly, 141
- de haani, 142 Spondy/us, 31
SEURAT, 4, 5, 193, 288, 298 Sponglcola, 31
Sex determmatlOn, 75-6, 80 Spongilla VIridis, 231
- reversal, 72, 76, 83, 154-6, 201-3 SporanglOle, 264, 272
Shark, 2, 3 Sporocyst, 136-7, 140
SHARP, 119,303 Sporozoa, 145, 159, 171, 184
Sheep, 129, 136-8, 178, 186, 189 Spumellana, 230, 234
SHIBATA, 272 Stcecharthrum glardi, 155
SHIMA, 249, 317 STAHL, 257,319
SHIPLEY, 303, 309 Staphy/ocyslls, 163
SHORTT, 148-9, 294 STASSANO, 195, 308
Shrew, 129 Slassia, 188
Sibme boncerensls, 124 Staurosoma parasltlcum, 173
Siboga expedition, 7, 52, 115 STEBBING, 299
Sideropora, 208 Stegophryxus hyptius, 76
SIEDLECKI, 160,206,294 Stelbacere, 275
SIGNORET,- 237 Stellaster equeslrls, 51
SIKORA, 243 STEMPELL, 294
Silkworm, 187, 190 Stentor po/ymorphus, 232
SIlpha lcevigata, 129 - vlfldlS, 231
SILVESTRI, 167, 305 STEPHENSEN, 94, 97, 208, 301-2
SIMOND, 160,294 STEWART,186,298
SIMULilDre, 35, 143 Sllchococcus, 260
SimulIUm, 150 Suchopus tremulus, 57, 60
Smapis arvensis, 200 Stickleback, 207
Siphonostoma dlplochaitos, 105 Stolonica soclails, 207
Sipunculus nudus, 47 Stomatome, 28
Si,ex gigas, 123 Stomoxydmre, 243
Sincidre, 221 Stomoxys, 150, 189
Sitodrepa panicea, 253, 254 Stonefiy, 138
SKOWRON, 248, 252 Streblomastlx strix, 223, 225
Slavery in ants, 24-7 Streptomycetacere, 263
Sleeping sickness, 150 Strigea tarda, 138-9
ER, 3, 5, 290 STRINDBERG, 242
SS
THMAN,220
H, A. J. 38, 196, 298, 308
SMITH E. F. 214-15, 310
Strombus, 10
- gigas, 30
Strongyloides #ercoralis, 186
338 INDEX
STRUBELL, 298 Tenebrio molitor, 142
STUHLMANN, 24:> Tenthredinidre, 210, 213
STUMMER,241 Terebellides strO!mi, 115
Sturgeon, 132, 161 Termes bellicosus, 24
Sturmia scutellata, 195 Termites and fungi, 219-20
Stylactls mmoi, 33 - , intestmal flagellates of, 222-7
Stybfer, 49, 53, 56, 64, 208 Tenruudre, 223
- celebensis, 53 Termitobia, 23
- linckite, 53-5, 54 Termltomorpha, 23-4
- slbogte, 53 Termllomyces, 220
Stylocometes digitatus, 33 Termltoxema, 20
Stylops, 200 Termopsis angusticoll,s, 223
Stylorhynchus iongicollis, 206 Tetramorium clespltum, 26, 29
Suberites, 15 Tetrilus arietmus, 17
- domuncula, 14 Thalamita, 86, 92
Succmea putris, 137-9, Thalessor lunator, 123
Suctona, 32-3 Thaumaleus, 109
SULe, 236, 238, 240, 243, 317 THEILER, 190
Sunaristes paguri, 7 THELOHAN,294
Surra, 151, 176 Thiazole, 268, 275
SUSUlCI, 139, 296 THIEL,317
Swans, 138 Thimni,178
SWEZY, 222, 224 THOMAS, A. 0., 50, 308
Sycosoter iavagnei, 123 THOMAS, A. P., 297
Sylhdre, 40, 110 THOMPSON, 181, 195, 305
Sylils gracilis, 109, 110 Thompsoma, 86, 91, 92, 165
Symbiosis, 217-84 THORSON, 8-9
- and evolution In plants, 270 ThrixlOn habdayanum, 187
- and social insects, 217-18 Thyca,48-50,61,64
Symphiles, 17-24 - cTlstallma, 48-9
Synagoga, 96-8 - ectoconcha, 48-50
- metacTlmcola, 94, 96 - stellasteris, 49-50
- mIra, 94, 96-7 Thylacle, 208-9
Synagogidre, 94, 96 Thylacoplethus, 86, 91
Synalpheus brucei, 5, 91 Thyone secreta, 60
Synapta d,gitata, 56-8 Thyonico/a, 49, 60-1
- soplax, 52 - mortensi, 60
Synaptids, 46-7 Thyreostenus biovata, 17
Synechthrans, 17 TiCk, 36, 38, 150, 190
Syngamus trachealls, 156 - fever, 178
Synrecy,2 VAN TIEGHEM, 259
Synreketes, 16-17 TIMBERLAKE, 194, 309
Systropus conopoides, 124 Timbu fiy, see Cordylobia anthropophaga
Tlpuhdre, 221
Toad,138
Tabanidre, 35, 150-1,243 TOBLER, 319
Tachma iavarum, 181 Tokophrya, 33
Tachmidre, 120, 187 TOWNSEND, 187, 305
Tadpole, 135-G Toxins, 196
Ttema, 127-30, 162 Trachlchthys, 3
- cO!nurus, 129, 162 Trachyuropoda bostocki, 17
- echinococcus, 129, 163, 174 TREADWELL, 40
- nilotica, 162 Trematoda, 134-42, 155
- sagmata, 129 - , reproduction in, 163-5
- serrata, 129-30 TREUB, 271, 319
- solium, 128-9, 159 TREVIRANUS, 22
Trenioglossa, 50 TTllenophorus nodulosus, 131
TO!niophyllum, 270 TTlatoma, 150
Talltrus, 244 Trichacls remulus, 125
Tamias IIsteri, 198 TTlchina spiralis, 142
Tamne, 178 TTlchinella, 142
Tapes, 145 TTlchodectes canis, 129
TATE,47 TTlchodma, 32, 234
Teleas, 125 - patellte, 231
Teleutomyrmex schneideri, 29 Tnchome,18
Tellina, 48, 145 Trichomitis termitidis, 223
Teiphusa, 31 Trichomonas trypanoides, 224
Temporary parasitism, 108-26 TTlchonympha agills, 226
 INDEX 339
Trichonympha campanula, 223, 225 Ustilago antherarum, 204
- dUlI/Olll, 224
- minor, 226
Trichophrya salparum, 33 Vacuohdes, 278
Trlchosphamum sieboldl, 230, 233 Vanda, 268-9
Trldacna, 231 Vanessa urticU!, 195
TRIER, 228, 317 VANEY, 49-52, 54-5, 58, 208, 307
Tri/ollUm repens, 200 VEILLET, 68, 75, 77-8, 80-1, 194, 303
Trigla hlrundo, 66 VEJDOVSKY, 237
Trlpylus, 47 Velella, 231
Trlflcum junceum, 210 VERRILL, 118, 171
- repens, 210 VibrIO plerantomi, 249
Trochocochlea mutabilis, 146 VILLOT, 298-9
Trochodota purpurea, 57 VIOla sylvatjca, 199
TROJAN, 246, 317 Vlrescence In flowers, 199
Trophic prophylaxis, 176-80 Vitellus, secondary, 236
TrophoblOsls, 22 VCllLTZKOW, 47
TROUVELOT, 121 VOGEL, 246, 252, 317
Trutta lacustTls, 131 VOIGT,308
Trypanosoma berberum, lSI VONWILLER,252
- brucel, ISO, 176 Vortex viridIs, 231
- cazalboui, 150-1 DE VRIES, 277
- equmum, 176
- equiperdum, 151
- evansi, 151 Wagtail,16
- gambiense, 150-1 W AHRLICH, 265
- granulosum, 151 WALKER,294
- mopmatum, lSI, 190 Warble fly, 189
- lewIsi, 150 WARBURTON,303
- pecaudi, 150 WARD, 119, 309
- rajU!, 151 WARMING, 258,311
- rhodiense, 150 Wart-hog, see Phacocharus
- theileri, 150 WASMANN, 16,22-5,27,291
Trypanosome, 174 Watasenia scintll/ans, 249
Trypetidre, 241 WEINBERG, 38, 196-7, 309
TrypsIn,195 WEJNLAND, 195, 309
Tsetse fly, see Glossina WEISMANN, 277
Tuaregs, 178 WESENBERG-LuND, 179, 306
Tubicmella, 34 Whales, 34
Tubllex, 162 WHEELER, 20, 25-8, 124, 156, 167, 197.
- tubi/ex, 133 291,295, 297, 309
Tubuilpora, 169 Wheeleriella santschll, 26
TUCKER, 204, 302 WHITMAN, 295
Tudora putTe, 242 WHITNEY, 232,317
Turtle dove, 244 WIGGLESWORTH, 222, 282, 311, 318
Turr,291 WILLEM,252
Tyiols, 18 WILLFAHRT, 262
Typhlocyba, 209 WILSON,303
- douglasi, 204 WIREN, 115,297
- hlppocastani, 204 WISNIENSKI, 297
Typhloplana virrdata, 233 WOLLMANN, 282, 318
Typton, 31 WOODCOCK, 175
Woodpecker, 137-8
ULE,291
Ulophysema, 102 Xanthoria parietina, 260
- dresundense, 94, 101 Xenocaloma, 104-7,112-13,156, 158,173,
- pourtaleslU!, 94, 101 209
Umbelhferre, 199 - brumpti, 106
Umo, 116, 117, 138 Xenodusa, 18-19,23
Unionidre, 64, 116-18,205 Xlphocarrdma depressa. 245
Upogebla, 86 XylaTla, 220
- Imoralis, 204 Xylariacere, 219, 256
Uranoscopus, 142 Xyleborus, 220
Urceolarla, 32
Uredlnere, 153, 265
Urothoe mann us, 6 YASAKI, 245, 251, 318
USSOW, 294 Yeasts, symbiotlc, 235-44
340 INDEX
YOSffiDA, 186, 297, 299 Zoobothflum, 231
Yosn, 94,99, 100, 102, 30~ Zoocecld 208,
Zoochlorellre, 230-5
Zootertn0pslS, 226
ZELLER, 135;297 Zoothylacie, 208
ZIRPOLO, 247-8, 250, 318 Zooxanthellre, 230-5