3
Biogeography and Conservation
Vincent S.F.T. Merckx, Erik F. Smets,
and Chelsea D. Specht
3.1
Introduction
There is hardly a region in the world where
mycoheterotrophy does not occur. As far as we
know, all orchid species are dependent on fungi
during germination and early development and
are therefore classified as initial mycoheterotrophs (Chap. 1). Orchidaceae have a
worldwide distribution and occur in almost every
terrestrial ecosystem apart from deserts and permafrosts. The distribution of fully mycoheterotrophic species, however, is much more
restricted and often shows intriguing patterns.
Fully mycoheterotrophic flowering plants almost
exclusively inhabit closed-canopy forests, and
the majority of species occur in the tropical
regions of the world. Many families and genera
of mycoheterotrophic plants have remarkably
widespread distributions that cross major dispersal barriers, and several botanists have suggested
V.S.F.T. Merckx (*)
Naturalis Biodiversity Center, Leiden University,
P.O. Box 9514, 2300 RA Leiden, The Netherlands
e-mail: vincent.merckx@naturalis.nl
E.F. Smets
Naturalis Biodiversity Center, Leiden University,
P.O. Box 9514, 2300 RA Leiden, The Netherlands
Laboratory of Plant Systematics, KU Leuven,
3001 Leuven, Belgium
C.D. Specht
Department of Plant and Microbial Biology,
University of California Berkeley, Berkeley,
CA 94720, USA
that these widespread lineages must be ancient
(Engler 1888; Malme 1896; Jonker 1938;
Rübsamen 1986; Leake 1994). In addition, the
distribution ranges of mycoheterotrophic plants
often show wide gaps (“disjunctions”). The
mycoheterotrophic genus Thismia (Thismiaceae)
even holds the status of what Robert Thorne considered one of the strangest distribution patterns
in flowering plants (Thorne 1972), with two
allegedly related species: one in northern USA
and the sister species in Australia and
New Zealand.
At local scale, the distribution of mycoheterotrophs is often highly patterned.
Mycoheterotrophs can be extremely scarce, and
some genera and species are known from only a
few localities. It is not always clear whether this
reflects true rarity or the plant’s ability to remain
unnoticed by collectors. Even in well-collected
areas, the ephemeral nature of mycoheterotrophs
makes their discovery challenging. In addition,
some tropical species seem to have intriguingly
fragmented distribution ranges, which, in some
cases, appears to be linked with postulated glacial rainforest refugia (Cheek and Williams 1999;
Franke 2004). Despite this rarity, certain localities and habitats seem to be more suited for
mycoheterotroph survival: both in tropical and
temperate zones, there is a tendency of unrelated
species to grow together (e.g., Wallace 1975;
Maas and Rübsamen 1986).
In general terms, the study of biogeography
includes two distinct components. First, the distribution of species is determined by historical
V.S.F.T. Merckx (ed.), Mycoheterotrophy: The Biology of Plants Living on Fungi,
DOI 10.1007/978-1-4614-5209-6_3, © Springer Science+Business Media New York 2013
103
104
factors. Historical biogeography attempts to infer
how evolutionary, geological, and climatic events
have shaped the distribution of a particular lineage.
Molecular phylogenetic hypotheses and divergence time estimates are particularly useful to
test hypotheses in this context (de Queiroz 2005;
Renner 2005). Unfortunately, the lack of a rigid
phylogenetic framework still prevents inference
of the historical biogeography of many mycoheterotrophic lineages. Nevertheless, the limited
data that is available now allows us to evaluate
the origin of the distribution patterns or disjunctions at least for a few mycoheterotrophic clades.
In addition to historical events, the distribution of
a species is also determined by ecological aspects.
Mycoheterotrophic species seem to show very
specific preferences toward certain (micro)habitats, a matter we discuss in detail below. In this
context, the use of molecular techniques for the
identification of root-inhabiting fungi has brought
a new and interesting ecological association to
the forefront of mycoheterotrophic biogeography. As many mycoheterotrophs show specialization toward narrow clades of fungi, it is often
hypothesized that the distribution of their host
fungi is a major determinant for the distribution
of the plants. The study of the biogeography of
fungi is still in its infancy, and to date, only a few
studies have tested this hypothesis in detail.
However, the development of next-generation
sequencing techniques provides promising prospects to resolve such questions in the upcoming
years.
Understanding distribution patterns is also
essential for effective species conservation
(Whittaker et al. 2005). The rapid and extensive
destruction of habitats, particularly in the tropics,
has become a serious threat to native biotas.
Mycoheterotrophic plants are often restricted to
areas that experience exceptional loss of habitat,
and due to their localized distributions, many
species are extremely vulnerable to extinction.
Some species may already be on the brink of
extinction, and only drastic conservation efforts
can prevent their disappearance.
Here we provide a detailed overview of the
global distribution of mycoheterotrophic plants.
This overview is considerably biased toward
angiosperm mycoheterotrophs, although we also
V.S.F.T. Merckx et al.
discuss in short the distribution patterns observed in
nonangiosperm lineages where mycoheterotrophy
is mostly restricted to the gametophytes of lycophytes, ferns, and gymnosperms. The occurrence
of mycoheterotrophy in nonangiosperm gametophytes remains poorly studied, thus preventing
an in-depth discussion of their distribution and
habitat preferences. The taxonomy and species
numbers of the lineages discussed here are based
on the information provided in Chap. 2. It is
important to note that the majority of the species
discussed here are only putative full mycoheterotrophs. The assumption that a species fully
relies on mycoheterotrophy is, in most cases,
based on the fact that leaves are absent and chlorophyll is lacking. However, the precise characterization of a species’ trophic strategy requires
careful investigation, which has been carried out
for only very few species. Also, new species and
localities are constantly discovered. Thus, our
observations, particularly about number of species, are subject to change. Nevertheless, it is
unlikely that undiscovered species and localities
represent significant dissimilarities to the general
patterns described here.
3.2
Distribution of Nonangiosperm
Mycoheterotrophs
3.2.1
Liverworts
The only non-seed plant species with a completely mycoheterotrophic life cycle is the liverwort Aneura mirabilis. The species has been
recorded from England, Germany, France,
Portugal, Russia, Scandinavia, and Greenland.
A liverwort species supposedly related to Aneura
mirabilis is described from Costa Rica, but it
remains unknown whether this species is a full
mycoheterotroph (Crum and Bruce 1996; Wickett
and Goffinet 2008).
3.2.2
Clubmosses
The genera Huperzia and Lycopodiella, with
respectively fully mycoheterotrophic and putatively partially mycoheterotrophic gametophytes,
3
Biogeography and Conservation
have a true cosmopolitan distribution, although
the diversity of Lycopodiella is highest in the
New World and Australasia. Species of
Lycopodium occur in temperate and tropical
zones as well, but in the tropics, Lycopodium is
restricted to montane regions.
3.2.3
Ferns
The gametophytes of Botrychium and
Ophioglossum species (Ophioglossaceae) are
achlorophyllous and thus putatively mycoheterotrophic. Both genera have a cosmopolitan
distribution. The gametophytes of the only other
Ophioglossaceae species, Helminthostachys
zeylanica and Mankyua chejuense, have not been
studied in detail. The former occurs in India and
Sri Lanka, Southeast Asia, Japan, and Australasia,
and the latter genus is endemic to Cheju Island
(Korea).
Species of the two Psilotaceae genera Psilotum
and Tmesipteris have subterranean mycoheterotrophic gametophytes. Psilotum has a pantropical
distribution, with one species extending into temperate areas. Tmesipteris occurs in Southeast
Asia, Australasia, Pacific, and New Zealand.
The gametophyte of Stromatopteris moniliformis (Gleicheniaceae), which is endemic to New
Caledonia, is achlorophyllous as well and thus presumably mycoheterotrophic. Mycoheterotrophic
gametophytes are also observed in species of the
105
genus Actinostachys (Schizaeaceae), which are
native to tropical America, Southeast Asia, and
temperate regions in the southern hemisphere.
3.2.4
Gymnosperms
The remarkable Parasitaxus usta (Podocarpaceae)
is the only achlorophyllous gymnosperm, but its
mycoheterotrophic status remains doubtful. It is
only found growing near or on the New
Caledonian sickle pine (Falcatifolium taxoides),
which occurs in dense evergreen rainforest on
New Caledonia and the adjacent Île des Pins
(Feild and Brodribb 2005; Eckenwalder 2009).
3.3
Distribution of Fully
Mycoheterotrophic
Angiosperms
3.3.1
Tropical Regions
The majority of fully mycoheterotrophic angiosperms—ca. 75% of all species—occur in the
tropical zone (“tropics”) between the Tropic of
Cancer and the Tropic of Capricorn. This zone is
dominated by tropical rainforest, the preferred
habitat of mycoheterotrophs (Fig. 3.1). Tropical
rainforest is the most diverse of all plant communities and occurs in areas with a warm wet climate without pronounced cold or dry seasons.
Fig. 3.1 Global distribution of tropical rainforest (black) in 2003. Map based on information obtained from NASA
Earth Observations (2011)
106
V.S.F.T. Merckx et al.
Table 3.1 Approximate numbers of fully mycoheterotrophic angiosperm species, genera, and families for the main
tropical regions discussed here
Families
Genera
Species
Central and
South America
7
24
84
Africa and
Madagascar
6
19
52
Southwest India
and Sri Lanka
4
10
17
Southeast Asia
9
29
169
Australasia
7
17
78
Pacific
Islands
3
9
17
Numbers of species and genera are based on data from Chap. 2. Not all species included in this overview grow in tropical
rainforest. Ericaceous mycoheterotrophs in tropical America and Asia, for example, are mainly restricted to coniferous
and mixed forests at high elevations
Tropical rainforest is dominated by broad-leaved
evergreen trees, and its multistoried canopy prevents light from penetrating to the forest floor.
The vast majority of tropical tree species form
arbuscular mycorrhizas (AM), and AM interactions are the most common mycorrhizal associations in tropical rainforests (Smith and Read
2008). Most tropical mycoheterotrophic plants
are associated with arbuscular mycorrhizal fungi,
although mycoheterotrophic interactions involving ectomycorrhizal fungi (Orchidaceae and
Ericaceae) and saprotrophic fungi (Orchidaceae)
are also common. Ectomycorrhizal associations
were long considered to be rare in the tropics, but
we now know that at least three lineages of tropical trees form ectomycorrhizal associations
(Alexander and Lee 2005). The most notable
exception to the AM dominance in tropical forest
is found in Southeast Asia. Rainforests in
Southeast Asia are among the most diverse plant
communities in the world and are characterized
by high abundance of trees in the family
Dipterocarpaceae, which are known to form associations with ectomycorrhizal fungi (Lee 1990).
While tropical rainforests on different continents are physiognomically very similar, their
floras have little in common. This reflects their
distinct geological and evolutionary histories
(Morley 2000). In our overview, we adopt six
major rainforest regions, loosely based on
Primack and Corlett (2005): (1) Central and
South America, (2) Africa and Madagascar,
(3) India and Sri Lanka, (4) Southeast Asia,
(5) Australasia, and (6) the Pacific Islands.
Biologically, these regions can be subdivided
into smaller areas, and we distinguish several
smaller rainforest blocks in our discussion of
each major region.
Mycoheterotrophs are represented in all these
tropical rainforest regions, but their diversity is
not equally distributed among the regions
(Table 3.1). Southeast Asia contains by far the
largest number of fully mycoheterotrophic species. On higher taxonomic level, the differences
in diversity between the regions are less pronounced (Table 3.1), although there is little
floristic overlap between the regions and many
species and genera are endemic to a particular
region.
3.3.2
Central and South America
Half of the world’s current tropical rainforests are
in South and Central America (Morley 2000;
Primack and Corlett 2005), together referred to
as the “Neotropics” or New World tropics (as
opposed to the Paleotropics or Old World tropics). Centered on the Amazon River basin in
northern and central Brazil and extending to the
western foothills of the Andes and up into southern Mexico along the isthmus of Panama, the
neotropical forests form the largest block of continuous rainforest on Earth (Fig. 3.2). The adjacent basin of the Orinoco River drains eastern
Colombia and Venezuela and contains a large
rainforest that extends into French Guiana,
Surinam, and Guyana (“the Guianas”), sharing
many characteristics with the Amazon River
basin. A distinct patch of rainforest, the Brazilian
Atlantic Forest (Mata Atlântica), runs along the
coast of southeast Brazil from Recife in the north
to Sao Paulo in the south. Due to excessive logging,
less than 5% of the original Mata Atlântica
remains; however, this forest still retains a high
level of taxonomic diversity and endemism.
3
Biogeography and Conservation
107
Fig. 3.2 Occurrence of rainforest in the Neotropics (black)
In Central America, rainforests extend from the
Pacific coast of northwest South America to
southernmost Mexico. Many larger islands of the
West Indies were covered by rainforest as well,
but very little of that forest now remains.
In comparison with Old World (paleotropical)
tropical forests, neotropical rainforests are characterized by a high species diversity of trees belonging to the families Vochysiaceae, Bignoniaceae,
Lecythidaceae, and Chrysobalanaceae. Another
distinct feature of neotropical rainforests is the
prominent presence of Bromeliaceae, which are
the preeminent group of neotropical epiphytes
(Primack and Corlett 2005). With an estimated
90,000 species of higher plants, the neotropical
region is more species rich than the Paleotropics
(Prance 1994). In terms of fully mycoheterotrophic
plant species, however, the Neotropics contain
only about a quarter of the number of species
found in the Paleotropics (Table 3.1), with the
flora of tropical America including ca. 80 species
of fully mycoheterotrophs. The paucity of fully
mycoheterotrophic species of orchids in the
Neotropics is the main reason for this discrepancy.
Despite the enormous diversity of tropical New
World orchids, only seven species are achlorophyllous versus 17 species in tropical Africa and
ca. 135 in tropical Asia.
With the exception of mycoheterotrophic
Iridaceae (Madagascar), Petrosaviaceae (Southeast
Asia), and Polygalaceae (Southeast Asia and
Australasia), all angiosperm families with fully
mycoheterotrophic species are present in the
Neotropics. Of the 24 neotropical genera of mycoheterotrophic flowering plants, 17 are endemic:
Apteria, Dictyostega, Hexapterella, Marthella,
108
and Miersiella (Burmanniaceae); Arachnitis
(Corsiaceae);
Lacandonia,
Peltophyllum,
Soridium, Triuris, and Triuridopsis (Triuridaceae);
Degranvillea, Pogoniopsis, Uleiorchis, and
Wullschlaegelia
(Orchidaceae);
Tiputinia
(Thismiaceae); and Voyriella (Gentianaceae). The
Neotropics are also an important center of diversity for Voyria (Gentianaceae), Gymnosiphon
(Burmanniaceae), and Thismia (Thismiaceae).
Although some neotropical mycoheterotrophic
plant species are endemic to a restricted region,
many species are widely distributed. Apteria
aphylla (Burmanniaceae), for example, occurs
from southern USA and the West Indies in the
north to Paraguay and southern Brazil in the
south (Maas et al. 1986). A similar distribution is
observed in Voyria aphylla (Gentianaceae) (Maas
and Ruyters 1986).
3.3.2.1 Central America
Many South American mycoheterotrophs reach
their northern distribution limit in the rainforests
of Central America. Central American forests also
contain a few endemic mycoheterotrophic species,
including Lacandonia schismatica (Triuridaceae),
Gymnosiphon panamensis (Burmanniaceae), and
Voyria kupperi (Gentianaceae). The only mycoheterotrophic orchids that grow in the rainforests
of Central America are species of Wullschlaegelia
(Orchidaceae). In terms of species richness, the
floras of Panama and Costa Rica contain perhaps
slightly more mycoheterotrophic species than
other countries in Central America consistent with
their increased species richness relative to surrounding regions.
Central America is also an important center of
diversity for the orchid genera Hexalectris and
Corallorhiza, which reach their southernmost
distributions here. However, these mycoheterotrophs do not grow in rainforests but are found in a
variety of habitats ranging from coniferous forest
to mixed scrub forests and desert canyons
(Salazar and Freudenstein 1998; Kennedy and
Watson 2010). Central American coniferous forests at higher elevations are also home to
Hypopitys monotropa and Monotropa uniflora
(Ericaceae). The latter species reaches its southernmost distribution in the montane forests of
V.S.F.T. Merckx et al.
Colombia (Wallace 1975). The distribution range
of these species does not overlap with any rainforest species.
3.3.2.2 West Indies
The West Indies lack many groups of mycoheterotrophs that are found on continental South
and Central America (e.g., Triuridaceae,
Thismiaceae, Voyriella, and most Burmanniaceae
genera). But species of Apteria, Corallorhiza,
Gymnosiphon, Voyria, and Wullschlaegelia that
are found in nearby continental forests have been
recorded on many islands of the West Indies.
Trinidad harbors a number of additional continental species (Dictyostega orobanchoides,
Hexapterella gentianoides, and Gymnosiphon
divaricatus) most likely as a result of its proximity to mainland South America. The rare monotypic genus Marthella (Burmanniaceae) is
endemic to Trinidad.
3.3.2.3 Guianas and Amazonia
In South America, the Guianas are an important
center of diversity for many mycoheterotrophic
genera, in particular for Voyria and Voyriella
(Gentianaceae), Gymnosiphon (Burmanniaceae),
and Sciaphila (Triuridaceae). Degranvillea dermaptera (Orchidaceae) and Thismia saülensis
(Thismiaceae) are endemic to this region. The
adjacent Amazon rainforest is home to a high
diversity of mycoheterotrophs, and several species are endemic to this region: Sciaphila rubra,
S. oligantha, S. corymbosa, Triuridopsis peruviana (Triuridaceae), and the enigmatic species
Tiputinia foetida and Thismia melanomitra
(Thismiaceae) from Amazonian Ecuador. Many
other mycoheterotrophs from the Amazon rainforest also occur in adjacent regions, particularly
in the Guianas, Venezuela, and Colombia. There
is little doubt that the forests of the Amazon Basin
harbor many species that have yet to be
discovered.
3.3.2.4 Southern Neotropics
Further to the south, many tropical mycoheterotrophic plants reach the edge of their distribution ranges in northern Paraguay and Bolivia.
Contrarily, Arachnitis uniflora (Corsiaceae)
3
Biogeography and Conservation
109
Fig. 3.3 Distribution of tropical rainforest (black) in Africa and Madagascar
reaches its most northern distribution in highaltitude rainforests of Bolivia that resemble the
habitat of this species’ southern Patagonian populations in Argentina and Chile (Ibisch et al. 1996).
3.3.2.5 Atlantic Forest
The Atlantic Forest (Mata Atlântica) on the
Atlantic coast of Brazil is another important
region for mycoheterotrophic plant diversity and
has a high level of endemism: many species of
Thismia (Thismiaceae) are endemic to this region
(Maas et al. 1986), and the Mata Atlântica harbors the only known populations of Lacandonia
brasiliana, Peltophyllum caudatum, Triuris alata
(Triuridaceae), Voyria obconica (Gentianaceae),
and Pogoniopsis nidus-avis (Orchidaceae). The
Atlantic Forest is severely affected by habitat
destruction, and many of these species are threatened with extinction.
3.3.3
Africa and Madagascar
Africa contains the second largest block of tropical rainforest, centered on the Congo River basin
and continuing on the coast of the Gulf of Guinea
to Sierra Leone but with a gap in the vicinity of
Togo (the Dahomey Gap) (Fig. 3.3) (Morley 2000;
White 2001). Tropical rainforest in East Africa is
mostly restricted to small “islands,” mainly centered on mountains. While these East African
patches of rainforest cover only a small area, they
contain a high percentage of endemic species due
to their prolonged isolation from the forests of
West and Central Africa. In Madagascar, tropical
rainforest is mostly restricted to a 120 km-wide
band along the eastern coast (Mittermeier et al.
1999), but due to intensive human activity, only
very little of this forest remains today.
African rainforests are generally dryer, lower,
and more open than rainforests found elsewhere
(Morley 2000). They are relatively poor in plant
species when compared with neotropical and
Asian rainforests, a feature that has been attributed to the degrading effect of significant climatic
changes during the Cenozoic and, more recently,
to Pleistocene climatic fluctuations, although
other factors such as human impact may have
contributed as well (Plana 2004). African rainforests are particularly poor in palms and Lauraceae
110
as well as in epiphytes and woody vines in general.
The flora of tropical Africa is also notably poor in
orchids, and it has been estimated that only 15%
of the world’s orchids occur in tropical Africa
compared to 41% in tropical America and 34% in
tropical Asia and New Guinea (Primack and
Corlett 2005). Tropical Africa has always been
considered relatively poor in number of mycoheterotrophic plant species (Leake 1994), but
recent new discoveries started to alter this image
(Cheek 2003a, b; Cheek et al. 2003, 2008; Franke
2004; Sainge et al. 2005; Cheek and Vanderburgt
2010; Cribb et al. 2010). Over 50 species of fully
mycoheterotrophic plants are now known from
Africa (including Madagascar) (Table 3.1). When
compared to the total number of higher plants
from tropical Africa (ca. 45,000; Beentje et al.
1994), the percentage of mycoheterotrophic species in the flora of Africa is not lower than that of
the Neotropics, where ca. 80 species of mycoheterotrophs are recorded for an estimated 90,000
higher plants (Prance 1994). The continuous
description of new taxa also illustrates the fact
that certain areas in Africa remain undercollected
and poorly characterized and that new discoveries, particularly from rainforests in Central
Africa, are anticipated.
The mycoheterotrophic species from Africa
and Madagascar belong to 19 genera, of
which Afrothismia (Thismiaceae), Auxopus,
Brachycorythis (Orchidaceae), Kupea, Kihansia,
Seychellaria (Triuridaceae), and Geosiris
(Iridaceae) are endemic. In general, the distribution of mycoheterotrophs in tropical Africa seems
to be more patterned than in the Neotropics,
as many species have very restricted distribution ranges. Exceptional widespread species
include Exochaenium oliganthum (Gentianaceae),
Didymoplexis africana, Eulophia galeoloides,
and Epipogium roseum (Orchidaceae).
3.3.3.1 West and Central Africa
The main African rainforest block is centered in
the Congo Basin and extends from the East
African Albertine Rift mountains to the Atlantic
Ocean in the West (Plana 2004). This rainforest
region is known as the Lower Guinea Region.
The Lower Guinea Region has a high diversity of
V.S.F.T. Merckx et al.
mycoheterotrophic plants, and many mycoheterotrophs in Burmanniaceae, Orchidaceae,
Thismiaceae, and Triuridaceae are endemic to
this region (Cheek and Williams 1999; Franke
2007). These endemics include Afrothismia spp.,
Oxygyne triandra (Thismiaceae), Auxopus
letouzeyi, Gastrodia africana (Orchidaceae),
Kupea martinetugei, and Sciaphila ledermannii
(Triuridaceae). The latter species is also found on
the islands in the Gulf of Guinea along with
Epipogium roseum (Orchidaceae) (Daniel 2010).
A smaller western block of West African rainforest is found in the Upper Guinea Region, from
Sierra Leone to Ghana (Plana 2004). This area is
generally less diverse in mycoheterotrophs compared to the Lower Guinea Region. Afrothismia
is remarkably absent from this region. Other
mycoheterotrophs are generally shared with the
Lower Guinea Region, including Campylosiphon
congestus, Gymnosiphon longistylus, G. bekensis
(Burmanniaceae), Auxopus macranthus, A. kamerunensis, Epipogium roseum (Orchidaceae),
Exochaenium oliganthum, and Voyria primuloides (Gentianaceae). The species Sciaphila
africana and Gymnosiphon samoritoureanus are
endemic to the Upper Guinea Region.
3.3.3.2 East Africa
Rainforests in East Africa consist of small patches
of forest on the East African mountains between
about 1,200 and 2,500 m altitude. These “islands”
of rainforests are generally surrounded by dry
woodland (Primack and Corlett 2005). Although
the total area of these rainforest patches is small,
those on older mountains have potentially provided a stable habitat for a long period of time
and have been isolated from the forests of West
and Central Africa for millions of years. As a
result, many of the plant and animal species are
endemic to these mountains. Recent discoveries
have stressed the importance of the coastal East
African forests for mycoheterotrophic plant
diversity (Cheek 2006). Gymnosiphon usambaricus
(Burmanniaceae), Afrothismia baerae, A. mhoroana (Thismiaceae), Seychellaria africana,
Kihansia jonii, and Kupea lovettii (Triuridaceae)
are endemic to the region, and most of these species are known from very few restricted localities.
3
Biogeography and Conservation
Kihansia jonii and Kupea lovettii, for example,
have only been recorded at the Kihansi River
Gorge in Tanzania (Cheek 2003b).
3.3.3.3 Madagascar
In Madagascar, mycoheterotrophs are restricted
to the humid lowland forests along the eastern
coastal strip and the subhumid forests above
600–800 m elevation. The flora of Madagascar
largely evolved in isolation, and this explains the
high level of endemism of mycoheterotrophic
plants. Indeed, all fully mycoheterotrophic plant
species that occur in Madagascar (and the adjacent Comores) are endemics. The Malagasy flora
also includes one endemic mycoheterotrophic
plant genus: Geosiris (Iridaceae), with one species known from Madagascar and the Comores
and another species endemic to the island of
Mayotte (Goldblatt and Manning 2010). Other
mycoheterotrophic species are Gymnosiphon
danguyanus, G. marieae (Burmanniaceae),
Seychellaria madagascariensis (Triuridaceae),
Auxopus madagascariensis, Galeola humblotii,
and Gastrodia madagascariensis (Orchidaceae),
although the generic identity of the latter has
been disputed and this species may belong to
Didymoplexis (Cribb et al. 2010). Another
Gastrodia species (G. similis) is known from a
single collection on La Réunion. With only eight
species, Madagascar is rather poor in mycoheterotrophic plants, and most genera that occur
on the east coast of Africa are absent from
Madagascar (e.g., Afrothismia, Kupea, Kihansia).
Another notable absence is that of the orchid
Epipogium roseum, which has a widespread distribution in continental Africa, India and Sri
Lanka, Southeast Asia, Australasia, and the
Pacific Islands. In contrast, the genus Seychellaria,
recorded from Madagascar, the Seychelles, and
Tanzania, provides an interesting biogeographic
link between Madagascar and continental Africa,
perhaps indicating its potential for dispersal
between Madagascar and the mainland. On the
other hand, Galeola, for which one species is
known from Madagascar and the Comores, is
absent from continental Africa but is widespread
in Southeast Asia. A biogeographic link between
Madagascar and India/Southeast Asia is observed
111
in several groups of organisms, including lizards
(Macey et al. 2000), birds (Cooper et al. 2001),
and amphibians (Bossuyt and Milinkovitch
2001), and is indicative of the geological past in
which Madagascar separated from the IndiaSeychelles landmass several tens of millions of
years after its separation from Africa (Storey
et al. 1995).
3.3.4
India and Sri Lanka
India has a long but very narrow strip of rainforest running parallel to the west coast along the
crest of the Western Ghats (Fig. 3.4). The southwest of the island of Sri Lanka supports rainforest as well. Southern India and Sri Lanka are
separated by the relatively shallow Palk Strait,
which allowed for intensive biotic interchange
during the Pleistocene ice ages. As a result, Sri
Lanka and the Western Ghats have very similar
biota, although for some groups of fauna, differences are somewhat more pronounced than
expected (e.g., Bossuyt et al. 2004). The rainforest of India and Sri Lanka has a vivid geological
history and probably underwent more changes
than any other rainforest region. The Indian Plate
began to drift away from eastern Gondwana in
the Early Cretaceous. While the Indian Plate
drifted close to the African plate, it received diverse
Late Cretaceous elements of the African tropical
flora and lost temperate elements of the eastern
Gondwanan gymnosperm flora (Morley 2000).
The dramatic latitudinal and climatic changes that
affected the Indian Plate during the Late Cretaceous
and Tertiary, as it traveled from Gondwana and
then collided with Asia, caused massive extinctions in its biota. Today, the Western Ghats–Sri
Lanka rainforest covers only a very small area and
is considered as a biodiversity hotspot under severe
threat: 45.6% of the plant species that occur here
are endemics (Myers et al. 2000).
This region contains ca. 17 fully mycoheterotrophic
species
within
families
Burmanniaceae, Orchidaceae, Thismiaceae, and
Triuridaceae. Almost half of the mycoheterotrophic species from the Western Ghats–Sri
Lanka hotspot are found nowhere else, while the
112
V.S.F.T. Merckx et al.
Fig. 3.4 Distribution of tropical rainforest (black) in India and Sri Lanka
widespread genera Galeola (Orchidaceae) and
Gymnosiphon (Burmanniaceae) are remarkably
absent from the southern India flora. In addition,
apart from the single species in the endemic
genus Hyalisma (Triuridaceae) and the widespread species Aphyllorchis montana, Epipogium
roseum (Orchidaceae), and Burmannia championii (Burmanniaceae) (Mesta et al. 2011), the
Western Ghats and Sri Lanka have no mycoheterotrophic species in common, indicating a
high degree of local endemism in this region. For
example, the enigmatic Haplothismia exannulata
(Thismiaceae) is endemic to the Western Ghats
and is only known from two restricted populations
(Sasidharan and Sujanapal 2000). The rainforest
of South India is also a habitat for three mycoheterotrophic Burmannia species: B. candelabrum,
B. indica, and B. stricta. However, the latter two
species are endemic to Southwest India. The
Western Ghats also contains at least five mycoheterotrophic orchid species, of which two are
endemic to the region (Didymoplexis seidenfadenii and Gastrodia silentvalleyana). In Sri
Lanka, many Southeast Asian mycoheterotrophic
species reach their westernmost distributions
(e.g., Sciaphila secundiflora, S. tenella, Cyrtosia
javanica, and Eulophia zollingeri). The island
contains at least two endemic mycoheterotrophic
species: Thismia gardneriana (Thismiaceae) and
Gastrodia zeylanica (Orchidaceae).
The flora of India contains many other mycoheterotrophic species than those mentioned above,
but all of these occur in the far northeastern state of
Assam (e.g., Burmannia nepalensis, Sciaphila khasiana, Chamaegastrodia shikokiana, Cymbidium
macrorhizon, Eulophia zollingeri, Erythrorchis
altissima, Galeola falconeri, Odontochilus asraoa,
Aphyllorchis spp., Yoania spp.). Biogeographically,
these species have more in common with South
China and Southeast Asia than with the Western
Ghats–Sri Lanka rainforests.
3.3.5
Southeast Asia
Southeast Asia has one of the most complex geological histories in the world. The region has
developed by the interaction of the Pacific, India–
Australia, Eurasia, and several smaller tectonic
plates, and as a result of this complicated past,
several distinct centers of biological diversity can
be identified within a small geographic range
(Hall 1998; Sodhi et al. 2004). Until recently,
rainforest covered most of the Malay Peninsula,
3
Biogeography and Conservation
113
Fig. 3.5 Distribution of tropical rainforest (black) in tropical Asia and tropical Australasia. The barrier between
Southeast Asia and Australasia is shown with a black line
Borneo, Sumatra, and Java (Fig. 3.5). This region
is often referred to as “Sundaland,” after the surrounding Sunda continental shelf. Lowland rainforest in this area has suffered considerably from
human activity, particularly on Java. North of
Sundaland rainforest extends into mainland Asia,
including most of Cambodia, Laos, and Vietnam,
and much of Thailand and Myanmar. However, due
to the rain shadow of several long north–south
mountain chains, most of the interior of Thailand
and Myanmar is too dry to support rainforest.
Farther north, rainforest covers South China and
the southern tip of Taiwan, although most has
now been cleared. The rainforests of Southeast
Asia extend westward through Myanmar into
Northeast India. Eastward rainforest covers
Sulawesi and many of the smaller islands between
Borneo and New Guinea (“Wallacea”) (Fig. 3.5).
As a whole, the tropical forests of Southeast Asia
include four biodiversity hotspots (Indo-Burma,
Sundaland, the Philippines, Wallacea) containing
high concentrations of endemic species and
undergoing immense and rapid habitat loss
(Myers et al. 2000; Sodhi et al. 2004).
Southeast Asian rainforests can be characterized as “dipterocarp forests,” with a canopy dominated by large trees of the family Dipterocarpaceae.
Dipterocarps are particularly important forest
elements of the Malay Peninsula, Borneo, Java,
Sumatra, and the wetter parts of the Philippines.
The dipterocarp forests of Southeast Asia are
extremely rich in mycoheterotrophic plants.
Except for Iridaceae mycoheterotrophs, all angiosperm families with fully mycoheterotrophic species are represented in Southeast Asia. Orchids
are particularly species rich, with over 100 fully
mycoheterotrophic species. The region is a center
of diversity for mycoheterotrophic orchids of the
genera Aphyllorchis, Gastrodia, Didymoplexis,
Didymoplexiella, Cyrtosia, Lecanorchis, and
Galeola. It is the only part of the world where
fully mycoheterotrophic orchids of the genera
114
Cystorchis,
Platanthera,
Silvorchis,
Kalimantanorchis, and Tropidia can be found.
Other mycoheterotrophic orchids from Southeast
Asia belong to Erytrorchis, Pseudovanilla,
Chamaegastrodia, Odontochilus, Cephalanthera,
Epipogium, Eulophia, and Stereosandra. The
poorly known ericaceous genus Cheilotheca,
which contains two mycoheterotrophic species,
is also endemic to Southeast Asia: Cheilotheca
species occur in pine and oak forest at high elevations, and therefore, their distribution does not
overlap with other tropical mycoheterotrophs.
The region is also a major center of diversity
for arbuscular mycorrhizal mycoheterotrophs in
Burmanniaceae, Petrosavia (Petrosaviaceae),
Epirixanthes (Polygalaceae), Thismiaceae, and
Triuridaceae. The distribution of many genera of
mycoheterotrophic plants from tropical Southeast
Asia extends into the subtropics, mostly into
subtropical China and Japan (e.g., Thismia,
Sciaphila, Gymnosiphon, Andruris, Exacum,
Petrosavia, Cyrtosia, Erythrorchis, Lecanorchis,
Aphyllorchis, Gastrodia, Odontochilus, and
Didymoplexiella). But many mycoheterotrophs
from Southeast Asia are also found in Australasian
rainforest, and a few species extend their distribution
into Oceania. Particularly widespread species
include Aphyllorchis montana, Didymoplexis
pallens, Stereosandra javanica, Epipogium
roseum, and Eulophia zollingeri.
3.3.5.1 Indochina
The rainforests of mainland Southeast Asia
(“Indochina” or “Indo-Burma”) are located in
Cambodia, Laos, Vietnam, Myanmar, Singapore,
Thailand, and South China (southeastern Tibet,
southern Yunnan, Guangxi, southwestern
Guangdong, Taiwan, and Hainan), although at
higher latitudes, these rainforests are gradually
replaced by monsoon and subtropical forests
(Zhu 1997; Morley 2000). The area is rich in
fully mycoheterotrophic plants, and the mycoheterotrophic flora consists of a mix of genera
that are widespread in tropical Southeast Asia
with genera that have a more temperate distribution. The majority of fully mycoheterotrophic
species found here are orchids, and the region is
an important center of diversity for the genera
V.S.F.T. Merckx et al.
Cyrtosia,
Galeola,
Lecanorchis,
Chamaegastrodia, and Odontochilus. Several
species in these genera are endemic to the region.
The Old World species of mycoheterotrophic
Cephalanthera orchids are restricted to mainland
Southeast Asia. Apart from Orchidaceae, mainland Southeast Asia contains full mycoheterotrophs that belong to Burmannia, Gymnosiphon
(Burmanniaceae), Petrosavia (Petrosaviaceae),
Thismia (Thismiaceae), Sciaphila (Triuridaceae),
Exacum (Gentianaceae), and Epirixanthes
(Polygalaceae). Corsiopsis (Corsiaceae) is
endemic to the region; the only described species, C. chinensis, is known from a single collection from a subtropical forest in Guangdong,
southern China (Zhang et al. 1999).
3.3.5.2 Sundaland
The major areas of rainforest of the Sundaland
region are located in Borneo, Java, Sumatra, and
Peninsular Malaysia. Sixty percent of the 25,000
plant species recorded from this region are
endemic, but with natural habitat disappearing
at an alarming rate, Sundaland is one of the
most threatened rainforest areas of the world
(Myers et al. 2000). This area is home to the most
species-rich plant communities on Earth and is
likewise one of the richest regions for fully
mycoheterotrophic plants. The diversity of mycoheterotrophic orchids is particularly remarkable,
with a high number of species of Aphyllorchis and
Gastrodia. It is also a center of diversity for
Didymoplexiella and Didymoplexis, and the mycoheterotrophic orchid genera Kalimantanorchis,
Tropidia, and Silvorchis are endemic to Sundaland.
Orchid genera Cyrtosia, Erytrorchis, Galeola,
Pseudovanilla, Cystorchis, Epipogium, Eulophia,
and Stereosandra are represented in this region by
mycoheterotrophic species as well.
Sundaland rainforests are also rich in arbuscular mycorrhizal mycoheterotrophs. These belong
to Burmannia and Gymnosiphon (Burmanniaceae),
Andruris, Sciaphila (Triuridaceae), Epirixanthes
(Polygalaceae),
Exacum
(Gentianaceae),
Petrosavia (Petrosaviaceae), and Thismia
(Thismiaceae). Several of these species are
endemic to Sundaland, or even to a particular
island within the Sundaland region. Of the three
3
Biogeography and Conservation
major islands, Borneo has by far the highest
diversity of fully mycoheterotrophic species. The
flora of Borneo contains at least 62 mycoheterotrophic species, which is more than the
number of species known from all of tropical
Africa. Endemism on Borneo is high and particularly pronounced in Orchidaceae and Thismiaceae:
at least 16 species of mycoheterotrophic orchids
are endemic to Borneo (Aphyllorchis kemulensis,
A. siantanensis, A. spiculaea, Cystorchis saprophytica, Didymoplexis latilabris, Didymoplexiella
borneensis , D. cinnabarina , D. forcipata ,
D. kinabaluensis, Gastrodia grandilabris, G.
sahabensis, G. spathulatha, Platanthera saprophytica, Kalimantanorchis nagamasui, Tropidia
saprophytica, and T. connata). All seven Thismia
species recorded on the island are also endemic.
The island of Java is also rich in mycoheterotrophs. The orchid genus Silvorchis is found nowhere
else, and several Didymoplexis and Gastrodia
species are endemic to Java as well.
3.3.5.3 Philippines
Until a few centuries ago, at least 95% of the
Philippines was covered by tropical rainforest
(Heaney and Regalado 1998). Today, only 3% of
that rainforest remains, mainly in montane areas,
and the Philippines has the questionable honor of
being the second “hottest” diversity hotspot on
Earth (Myers et al. 2000). The flora of the
Philippines has fewer plant species than
Sundaland and Indochina (which cover larger
areas) but includes ca. 24 species of fully mycoheterotrophic angiosperms. Six species of
Sciaphila (Triuridaceae) are native to the
Philippines, but only a single mycoheterotrophic
Burmannia species (B. nepalensis) and remarkably no Gymnosiphon species have been
recorded for the Burmanniaceae. Epirixanthes
(Polygalaceae), found throughout Australasia and
Sundaland, is also absent. Mycoheterotrophic
orchids from the Philippines are of the genera
Cyrtosia, Erythrorchis, Galeola, Lecanorchis,
Pseudovanilla,
Cystorchis,
Aphyllorchis,
Didymoplexis, Epipogium, Eulophia, Gastrodia,
and Stereosandra. Endemic mycoheterotrophs
are Aphyllorchis halconensis, Didymoplexis
philippinensis, Pseudovanilla philippinensis
115
(Orchidaceae), Exacum loheri (Gentianaceae),
and Thismia gigantea (Thismiaceae).
3.3.5.4 Wallacea
Wallacea includes the island of Sulawesi, the
Maluku Islands, and the Lesser Sunda Islands.
The area is one of the most geologically complex
regions in the world. The islands originated from
land fragments that rifted from Gondwana at different geological time periods, and they were
never physically connected to Southeast Asia
(“Wallace’s Line”) (Audley-Charles 1983). Due
to their prolonged isolation, each island evolved
highly endemic faunas, but the proximity of
Sundaland caused a large influx of tropical
Southeast Asian plants, which started during the
mid-Miocene. The flora of Wallacea contains an
estimated 10,000 species, of which ca. 1,500 are
endemic (Myers et al. 2000). Ca. 21 species of
mycoheterotrophic plants are known from
Wallacea. Most of them have distribution ranges
that include other parts of Southeast Asia,
Australasia, or both: Burmannia lutescens ,
B. championii, Gymnosiphon aphyllus, G. papuanus (Burmanniaceae), Sciaphila arfakiana,
S. corniculata, S. densiflora, S. tenella (Triuridaceae),
Petrosavia stellaris (Petrosaviaceae), Cyrtosia
javanica, Cystorchis aphylla, Didymoplexis
micradenia, Epipogium roseum, and Eulophia
zollingeri (Orchidaceae). Gymnosiphon minahassae,
Pseudovanilla ternatensis, Galeola nudifolia,
Aphyllorchis acuminata, A. angustipetala,
A. gracilis, and Gastrodia celebica are endemic
to the region. Remarkably, in Wallacea there are
no records of Thismia, a genus that is otherwise
widespread in Southeast Asia and Australasia.
3.3.6
Australasia
Most of the island of New Guinea is covered by
what is now the third largest and most intact rainforest area of the world (Primack and Corlett
2005). Australia also supports a small area of
rainforest in the northeast, along the coast between
Cooktown and Townsville (Fig. 3.5). The geological history of New Guinea and Australia differs from that of Southeast Asia: New Guinea and
116
Australia are located on the Australian plate,
while the rest of the Southeast Asian tropical forest is located on the Asian plate. The midMiocene collision of the Australian and Asian
plate caused a large influx of Asian rainforest
plants into New Guinea. The absence of a dry
land connection prevented a similar influx of vertebrates. As a result, the composition of the flora
of New Guinea is relatively similar to that of
Southeast Asian rainforests, while their vertebrate
faunas are very different. The rainforests of
Australia were much less affected by the postMiocene influx of Asian plants. The flora of
Australian rainforests contains more Gondwanian
and Australian components as well as more early
diverging angiosperm families, such as
Winteraceae, Eupomatiaceae, Monimiaceae,
Lauraceae, and Cunoniaceae (Primack and Corlett
2005). Rainforests in New Guinea do contain
Dipterocarpaceae trees, but they are much less
dominant than in Southeast Asian rainforests.
Australasian rainforests harbor a high diversity
of mycoheterotrophic plants, although the total
number of mycoheterotrophic species is considerably lower than the number of species recorded
from Southeast Asia (Table 3.1). Australasian
mycoheterotrophs are part of seven different
flowering plant families: Burmanniaceae,
Thismiaceae,
Triuridaceae,
Corsiaceae,
Polygalaceae, Orchidaceae, and Gentianaceae.
Ca. 30 species belong to Orchidaceae—which is
lower than the number of mycoheterotrophic
orchids from Southeast Asia, but still high compared to the number of species occurring in Africa
and the Neotropics. Reflecting their general
floristic overlap, Australasian rainforests share
many genera and species of mycoheterotrophs
from rainforests in Southeast Asia and Oceania.
A notable exception is the genus Corsia
(Corsiaceae), of which all 25 species are endemic
to Australasia. Conversely, Southeast Asian mycoheterotrophic
species
of
Petrosavia
(Petrosaviaceae),
Cyrtosia,
Erythrorchis,
Cystorchis,
Odontochilus,
Platanthera,
Cephalanthera, Didymoplexiella, Tropidia, and
Yoania (Orchidaceae) do not occur in Australasia.
For mycoheterotrophic Orchidaceae, the
region is an important center of diversity for
V.S.F.T. Merckx et al.
Pseudovanilla, Lecanorchis, and Aphyllorchis.
The orchid genera Galeola, Didymoplexis,
Epipogium,
Eulophia,
Gastrodia,
and
Stereosandra are also represented by fully
mycoheterotrophic species. Arbuscular mycorrhizal mycoheterotrophs in Australasia belong to
the genera Burmannia, Gymnosiphon (Burmanniaceae), Thismia (Thismiaceae), Sciaphila,
Andruris (Triuridaceae), Epirixanthes (Polygalaceae), Exacum (Gentianaceae), and Corsia
(Corsiaceae).
3.3.6.1 New Guinea
By far the largest part of Australasian rainforest is
found on New Guinea, and this is where most
Australasian mycoheterotrophs occur. The world’s
second largest island is home to arbuscular mycorrhizal species of Burmannia, Epirixanthes,
Exacum, Gymnosiphon, Andruris, Sciaphila, and
Thismia. The island is also the center of diversity
of the little-known genus Corsia (Corsiaceae),
where 23 of the 25 described species occur as
endemics. Mycoheterotrophic orchids belong to
the genera Galeola, Lecanorchis, Pseudovanilla,
Aphyllorchis,
Didymoplexis,
Epipogium,
Eulophia, and Gastrodia. In addition to the 23
species of Corsia, island endemics include
Aphyllorchis elata, A. exilis, A. torricellensis,
Didymoplexis torricellensis, Gastrodia crassisepala , G. papuana , Lecanorchis bicarinata ,
L. ciliolata, L. neglecta, Pseudovanilla gracilis,
P. vanilloides (Orchidaceae), Burmannia micropetala, Thismia appendiculata, Andruris wariana, Sciaphila quadribullifera, S. papillosa,
Gymnosiphon affinis, G. oliganthus, and
G. pauciflorus.
3.3.6.2 Australia
Tropical rainforest once covered Australia, but as
a result of the continued northward drift of
Australia, coupled with global climatic cooling,
the climate of Australia became much drier in the
Middle and Late Miocene and Late Pliocene,
resulting in a withdrawal of tropical rainforests
from all but the northeast coast region of
Queensland. This tiny tip of tropical rainforest
contains ca. 15 species of mycoheterotrophic
angiosperms in the genera Aphyllorchis, Andruris,
3
Biogeography and Conservation
117
Corsia, Didymoplexis, Epipogium, Eulophia,
Gastrodia, Pseudovanilla, and Thismia. Endemic
mycoheterotrophs are Thismia yorkensis, Corsia
dispar, Andruris australasica, Aphyllorchis
anomala, A. queenslandica, Didymoplexis
pachystomoides, Gastrodia crebrifolia, G. queenslandica, and G. urceolata.
micradenia, D. pallens, Dipodium squamatum,
Epipogium roseum, and Gastrodia cunninghamii
(Orchidaceae) (van de Meerendonk 1984;
Govaerts et al. 2011).
3.3.6.3 New Caledonia and Vanuatu
The Southwest Pacific Island group of New
Caledonia is also part of Australasia, and the
region is recognized as a global biodiversity
“hotspot” (Myers et al. 2000), with a very high
degree of plant endemism (Jaffré et al. 1998).
New Caledonia formed part of the eastern margin
of Gondwana, until it became separated by the
Tasman Sea about 90 million years ago (Ma)
(Wilford and Brown 1994). Thus, the flora of
New Caledonia results from a Gondwanan origin
and mainly evolved in isolation (Jaffré 1992),
although volcanic islands between Australia and
the New Caledonian region could have facilitated
plant migration during the Neogene (Wilford and
Brown 1994), and island chains are also implicated along the Norfolk and Reinga Ridges
toward New Zealand during this time (Herzer
et al. 1997). In contrast to the continental origin
of New Caledonia, the Vanuatu archipelago is
oceanic in origin, and its development results
from tectonic events ranging from 11.2 to 2.0 Ma
(Kroenke and Rodda 1984). The flora of New
Caledonia includes relatively few mycoheterotrophic plants, and none of them are
endemic to the region except for the sole putative
mycoheterotrophic gymnosperm Parasitaxus
usta. New Caledonian mycoheterotrophic
flowering plants include three Triuridaceae species ( Sciaphila densi fl ora , S. corallophyton,
and S. corniculata) and three orchids
(Didymoplexis micradenia, Dipodium squamatum, and Epipogium roseum). Burmanniaceae are
absent from the flora of New Caledonia, but the
mycoheterotroph Burmannia lutescens occurs on
the neighboring Vanuatu archipelago (Yohan
Pillon, pers. comm.), which represents the easternmost distribution record for the family. Other
Vanuatu mycoheterotrophs are Sciaphila arfakiana, S. aneitensis (Triuridaceae), Didymoplexis
The islands in the Pacific Ocean are composed
mostly of volcanic emergents and coral atolls that
arose from the sea in geologically recent times,
many of them in the Pleistocene. They were created either by hotspot volcanism or as island arcs
pushed upward by the collision and subduction of
tectonic plates. The islands range from tiny islets,
sea stacks, and coral atolls to large mountainous
regions containing complex ecosystems. Only
these larger islands harbor tropical rainforests
that are potential habitats for mycoheterotrophs.
The flora of the islands is comprised entirely
from long-distance dispersal events and is generally characterized by a low diversity but high
endemism (Carlquist 1967). For mycoheterotrophic plants, only a few widespread species in Burmanniaceae, Triuridaceae, and
Orchidaceae have been able to colonize some
islands. Burmanniaceae are only present on the
Caroline Islands, where Burmannia ledermannii,
Gymnosiphon aphyllus, G. papuanus, and G.
okamotoi occur. The latter is endemic to the
islands. For Triuridaceae, Sciaphila arfakiana
and S. consimilis have been recorded on Fiji (van
de Meerendonk 1984). The latter species is widespread in Southeast Asia and is also found on the
Caroline Islands, together with S. corallophyton
and S. multiflora. Triuridaceae reach their easternmost distribution on Futuna, where the widespread Sciaphila aneitensis occurs. In
Orchidaceae,
the
widespread
species
Didymoplexis micradenia occurs on the Marianas,
Niue, Samoa, Tonga, Wallis–Futuna, and Caroline
Islands, D. pallens is known from Niue,
Stereosandra javanica from Samoa, and
Epipogium roseum from Fiji. None of these species are endemic to the region. In contrast,
Pseudovanilla ponapensis is only known from
the Caroline Islands, and Pseudovanilla anomala
is endemic to Fiji, but it is unclear whether these
3.3.7
Pacific Islands
118
V.S.F.T. Merckx et al.
species are (partial) mycoheterotrophs. There are
no records of mycoheterotrophic plants from
French Polynesia and Hawaii. Whether this is the
result of their isolated position or the absence of
certain habitat characteristics necessary for the
establishment of mycoheterotrophic plants
remains unknown.
3.3.8
v
Temperate Regions
Similarly to the tropics, mycoheterotrophs in
temperate regions are mainly restricted to forests.
In temperate regions, forest coverage mainly
consists of coniferous, deciduous, or mixed forests, and all these forest types provide habitats for
mycoheterotrophic plants. Temperate forests predominantly occur in the northern hemisphere,
although the southern hemisphere has small
pockets of temperate forest as well. Temperate
forests of the northern hemisphere are located in
eastern North America, western North America,
Europe (including southwestern Asia), and eastern Asia (Fig. 3.6). Many flora and fauna elements have a disjunct distribution across these
forest regions, which is illustrated by the similarities of biotas between eastern North America
and temperate Asia (Wen 1999; Donoghue et al.
2001). This current disjunct distribution has been
attributed to the historical existence of a widespread evergreen vegetation type (“boreotropical” forest) earlier during the Tertiary, when
warm and wet climatic conditions prevailed over
northern latitudes (Milne and Abbott 2002). In
response to climatic cooling from the start of the
Oligocene, deciduous elements moved southward forming a northern hemisphere flora (the
“mixed mesophytic forest”) that contained a mix
of deciduous and evergreen trees with increasing
numbers of associated understory herbs (Tiffney
1985; Milne and Abbott 2002). During the Late
Miocene to Pliocene, global temperatures
dropped and the flora retreated, leading to
increased extinction particularly in western North
America. Further depauperation of the flora
occurred during the Quaternary glaciations,
which had a strong impact on the European flora
(Milne and Abbott 2002; Donoghue and Smith
2004).
In the southern hemisphere, temperate forests
are restricted to small patches in southern South
America, South Africa, Australia, and New
Zealand. These forests are thought to have originated from southern temperate Gondwanan
floristic elements. The sequential breakup of
Gondwana started 165 Ma ago and resulted in a
successive division of the ancestral biota. However,
there has been a documented exchange of plants
between the major landmasses following their
breakup; for example, trans-Tasman dispersal
between Australia and New Zealand appears to
be quite common (Hill 2004; Sanmartin and
Ronquist 2004).
The diversity of mycoheterotrophic plants in
temperate regions is lower than in the tropics,
with temperate mycoheterotrophs mainly belonging to Ericaceae and Orchidaceae. In contrast to
the dominance of arbuscular mycorrhizal mycoheterotrophs in the tropics, mycoheterotrophic
interactions in temperate regions generally rely
on ectomycorrhizal fungi. Nevertheless, many
predominantly tropical arbuscular mycorrhizal
mycoheterotrophic families extend their distribution into subtropical and even temperate regions,
particularly in Asia (e.g., Thismia, Petrosavia,
Sciaphila).
3.3.9
North America
North America contains a large variety of
different forest types, providing habitat for a
very distinct group of mycoheterotrophs. Of a
total of 30 fully mycoheterotrophic species in
North America, only the two widespread species
Hypopitys monotropa and Monotropa uniflora
(Ericaceae) occur outside North America, indicating a high level of continental endemism. The
distribution of the partial mycoheterotroph
Corallorhiza trifida (Orchidaceae) extends only
into temperate Eurasia. North American forests
are particularly rich in ericaceous mycoheterotrophs: with the exception of Cheilotheca and
Monotropastrum, all genera of ericaceous mycoheterotrophs occur here. Many Ericaceae genera
are endemic to North America (Monotropsis,
Pterospora), most occurring only in western
North America (Pityopus, Allotropa, Hemitomes,
3
Biogeography and Conservation
119
Fig. 3.6 Distribution of coniferous and mixed forest (black) in the temperate parts of the northern hemisphere.
Map based on information obtained from NASA Earth Observations (2011)
Pleuricospora, Sarcodes). The only fully mycoheterotrophic species in Pyrola (Ericaceae), P.
aphylla, is also endemic to North America.
North American mycoheterotrophic orchids
include Cephalanthera austiniae, all Corallorhiza
species, all Hexalectris species, and the partial
mycoheterotroph Liparis liliifolia. As far as is
known, these mycoheterotrophs are associated with ectomycorrhizal fungi. In contrast, the
North American partially mycoheterotrophic
Gentianaceae species of Bartonia and Obolaria
are associated with arbuscular mycorrhizal fungi
(Cameron and Bolin 2010). The full mycoheterotroph Thismia americana (Thismiaceae),
which has been recorded from a prairie near
Chicago, was probably also associated with
arbuscular mycorrhizal fungi (see further). This
species is probably extinct.
3.3.10 Europe
The temperate forests of Europe are less diverse
in plant species than those of North America.
This difference has been explained by greater
survival of plant species in North America during
the Quaternary glaciation, although some evidence indicates that floristic differentiation
between Europe and North America started in
the late Tertiary (Davis 1983). The diversity of
mycoheterotrophic plants in Europe is likewise
significantly lower than that of North America
and temperate Asia. The coniferous, mixed, and
deciduous forests of Europe harbor only seven
mycoheterotrophic species, the ericaceous
Hypopitys monotropa and six orchid species:
Neottia nidus-avis , Limodorum abortivum ,
L. rubriflorum, L. trabutianum, Corallorhiza
trifida, and Epipogium aphyllum. The distribution range of some of these species extends into
North Africa and temperate Asia.
3.3.11 Temperate Asia
In temperate Asia, mycoheterotrophic flowering
plants occur in coniferous, mixed, and deciduous
forests. Toward the south, there is a transition
from temperate through subtropical forests into
the tropical rainforest of Indochina, allowing for
influx of tropical mycoheterotrophic groups.
Typical temperate elements are the genera
Hypopitys and Monotropa (Ericaceae), of which
both monotypic species are present in temperate
Asia. Other ericaceous mycoheterotrophs
Monotropastrum humile and M. sciaphilum occur
in the subtropical zones of Asia. There is a relatively large diversity of fully mycoheterotrophic
orchids in temperate and subtropical Asia. With
about 13 species, Neottia is particularly species
120
rich. Five species of Aphyllorchis, a genus with a
center of diversity in tropical Asia, are found in
South and Central China and Tibet. All tree species of Epipogium are found in temperate and
subtropical Asia as well. Yoania japonica and
Y. prainii are also present in the subtropical zone
of Asia, as well as Risleya atropurpurea. In addition, the distribution of a few Burmannia
(Burmanniaceae) species extends into Central
China, Assam, and Nepal (e.g., B. nepalensis,
B. wallichii, B. itoana, B. cryptopetala,
B. chinensis).
3.3.12 Japan
The flora of Japan includes a large number of
mycoheterotrophic plants. The wet subtropical
evergreen forest in southern Japan is a habitat for
many species of arbuscular mycoheterotrophs
that belong to genera with a mainly tropical distribution: Burmannia, Thismia, Petrosavia,
Andruris, and Sciaphila. Three species of
Oxygyne (Thismiaceae) have been discovered in
these forests as well, which is remarkable since
the only other species of the genus is recorded
from Cameroon. With ca. 25 species, the Japanese
flora is also rich in fully mycoheterotrophic
Orchidaceae. Genera with a mainly tropical distribution, as well as genera from temperate Asia,
are represented in Japan. Japanese mycoheterotrophic orchids include Cyrtosia septentrionalis, Erythrorchis altissima, Lecanorchis spp.,
Chamaegastrodia shikokiana, Odontochilus poilanei, Aphyllorchis montana, Cymbidium macrorhizon, Didymoplexiella siamensis, Epipogium
japonicum, E. roseum, Eulophia zollingeri,
Gastrodia spp., Neottia spp., Stereosandra javanica, and Yoania spp. Lastly, three ericaceous
mycoheterotrophs
Hypopitys
monotropa,
Monotropa uniflora, and Monotropastrum humile
occur in Japan as well.
3.3.13 South Chile and Argentina
Temperate forests in southern South America are
located on the Pacific coast of southern Chile, on
V.S.F.T. Merckx et al.
the west-facing slopes of the southern Chilean
coast range, and the Andes Mountains in both
Chile and Argentina down to the southern tip of
South America (Patagonia). These wet Nothofagus
forests are home to Arachnitis uniflora
(Corsiaceae), an arbuscular mycorrhizal mycoheterotroph that also occurs in tropical Bolivia
and on the Falkland Islands (Ibisch et al. 1996).
3.3.14 South Africa
In South Africa, forests have a patchy distribution
and occur in frost-free areas with more than 725 mm
rainfall during the wet season. Indigenous forest is
the smallest biome in South Africa (Eeley et al.
1999). Only two mycoheterotrophic orchid species
have been recorded from the South African flora.
Didymoplexis verrucosa is endemic to KwaZuluNatal. Gastrodia sesamoides, which occurs natively
in South and East Australia, was introduced to
South Africa and is naturalized in the Cape Province
near Kirstenbosch (Linder and Kurzweil 1999;
Linder et al. 2005; Cribb et al. 2010).
3.3.15 Temperate Australia, Tasmania,
and New Zealand
The forests of temperate Australia and Tasmania
comprise ca. eight species of mycoheterotrophic
orchids, and all of them are endemic to this
region. Cryptostylis hunteriana, Burnettia cuneata, and Dipodium roseum are endemic to southeast Australia, and the latter two also occur in
Tasmania. Erythrorchis cassythoides and
Dipodium variegatum are endemic to East
Australia, and Gastrodia lacista is endemic to
western Australia. Temperate Australia is also the
only place in the world where the enigmatic
underground orchid, Rhizanthella, is found.
Three species of Rhizanthella are known: R. gardneri from southwest Australia and R. slateri and
R. omissa from southeast Australia. In southwest
Australia, Rhizanthella is found growing in much
drier habitats than the eastern Australian species.
The temperate rainforests and wet sclerophyll
forests in New South Wales, Victoria, and
3
Biogeography and Conservation
Tasmania are also home to the arbuscular mycorrhizal mycoheterotroph Thismia rodwayi
(Thismiaceae). Another Thismia species,
T. clavarioides, is only known from Morton
National Park in New South Wales.
In New Zealand, mycoheterotrophs only occur
on the North Island, mostly in coniferous podocarp
forests and broadleaf evergreen forests. Apart from
Thismia rodwayi (Thismiaceae) and Danhatchia
australis (Orchidaceae), which also occurs in
Australia, all New Zealand mycoheterotrophs
are endemic and belong to Orchidaceae:
Corybas cryptanthus, Gastrodia cunninghamii,
and G. minor (Moore and Edgar 1970).
3.4
Biogeographic Patterns
3.4.1
General Patterns of Diversity
Most fully mycoheterotrophic angiosperms occur
in the tropics, and—in terms of the number of
species—Southeast Asia is the most important
region. Southeast Asia contains more than twice
121
the number of mycoheterotrophic species found
in the Neotropics (Table 3.1). This difference is
remarkable but is almost solely the result of the
high number of mycoheterotrophic orchid species in Southeast Asia (Fig. 3.7). Indeed, the flora
of the Neotropics includes only seven species of
mycoheterotrophic orchids. With 17 species, the
diversity of orchid species in Africa and
Madagascar is only slightly higher. In tropical
Asia, the mycoheterotrophic orchid diversity
peaks, with 27 species in Australasia and ca. 100
species in Southeast Asia. Most of these species
belong to species-poor genera, although a few
genera, such as Lecanorchis, Aphyllorchis, and
Gastrodia, are particularly species rich.
Mycoheterotrophic orchids associate with saprotrophic or ectomycorrhizal fungi, while tropical
tree species are generally associated with arbuscular mycorrhizal fungi (Smith and Read 2008).
However, in Southeast Asia—and to a lesser
extent also in Australasia—tropical forests are
dominated by Dipterocarpaceae trees which are
known to form associations with ectomycorrhizal
fungi (Lee 1990). These mycorrhizal networks
Fig. 3.7 Comparison of the species richness between major rainforest regions for arbuscular mycorrhizal (AM)
mycoheterotrophs and mycoheterotrophic Orchidaceae, which associate with ectomycorrhizal and saprotrophic fungi
122
are potential “hosts” for ectomycorrhizal mycoheterotrophic orchids: indeed, mycoheterotrophic
orchids from a dipterocarp forest in Thailand have
been found to obtain carbon from dipterocarps
through shared ectomycorrhizal fungi (Roy
et al. 2009). Thus, it is possible that the dominance
of ectomycorrhizal trees in Asian rainforests
explains the high number of mycoheterotrophic
orchids in these forests.
Differences between major rainforest regions
in the number of arbuscular mycorrhizal mycoheterotrophs are less pronounced. The Neotropics
have the most species, but in comparison with
floras of Southeast Asia and Australasia, which
have in general less plant species but also cover a
smaller area, species diversity of AM mycoheterotrophs is more pronounced in tropical Asia
(Fig. 3.7). However, the Neotropics are home to
19 genera of AM mycoheterotrophs, Africa and
Madagascar have 12 genera of AM mycoheterotrophs, and Southeast Asia and Australasia
only have nine and eight genera, respectively,
or ten when considered as one area. Generic
diversity in the Neotropics is particularly high
in Burmanniaceae and Triuridaceae (Table 3.2).
It has been hypothesized that Burmanniaceae
originated in South America (or western
Gondwana) and only reached the Old World during the Eocene (Merckx et al. 2008). The early
diversification of Burmanniaceae in the
Neotropics may explain the comparatively high
number of genera in this region.
In the temperate zone, East Asia and Japan are
the most species-rich regions for mycoheterotrophic plants. Their floras contain a mix of
temperate and subtropical elements and are particularly rich in fully mycoheterotrophic orchids.
Influx from the tropics probably also explains the
high number of arbuscular mycorrhizal mycoheterotrophs in these regions (e.g., species of
Burmannia, Thismia, Sciaphila, Petrosavia). The
number of mycoheterotrophic species in North
America is only slightly lower than in Asia and
Japan. The diversity of Ericaceae in North
America is remarkable, and the region is also
relatively rich in mycoheterotrophic orchids (e.g.,
Corallorhiza, Hexalectris). The diversity of
mycoheterotrophs in Europe is relatively low.
V.S.F.T. Merckx et al.
Besides a few mycoheterotrophic orchids,
European forests only contain the most widespread ericaceous mycoheterotroph Hypopitys
monotropa and no arbuscular mycorrhizal species. Perhaps this is due to the lack of an historical connection with tropical floras, restricting all
present-day mycoheterotrophic plants to be relictual elements of taxa with an ancient boreotropical distribution.
In the southern hemisphere, the much higher
proportion of sea to land creates conditions favoring temperate rainforest on west-facing coasts
(Beard 1990). The identity of mycoheterotrophic
plants in these forests is very different from that
of their northern hemisphere counterparts, and the
species diversity is lower. Most mycoheterotrophs
in the forests of the southern hemisphere belong
to groups with mainly tropical distributions, indicating independent tropical origins of the southern hemisphere mycoheterotrophs. Southern
hemisphere mycoheterotrophs include both species that are living on arbuscular mycorrhizal
fungi (Thismia, Arachnitis) and orchids linked
with ectomycorrhizal or saprotrophic fungi, but
mycoheterotrophic Ericaceae are absent from the
southern hemisphere.
3.4.2
Widespread Distributions
A few tropical mycoheterotrophic families are particularly widespread. Burmanniaceae and
Triuridaceae can be found in all rainforest regions
of the world (Table 3.2). Thismiaceae have a similar distribution but are absent from Madagascar
and the Pacific Island region. Mycoheterotrophic
Gentianaceae and Orchidaceae are also found in
nearly all tropical regions, but their mycoheterotrophic species have evolved independently
in different lineages. These lineages show little
overlap in their distribution ranges, and it is likely
that mycoheterotrophy has evolved on different
continents independently. At the genus level,
Sciaphila (Triuridaceae) has the most widespread
distribution, and it is only absent from East Africa,
Madagascar, and Southwest India. However,
in these regions, Triuridaceae are represented
by Seychellaria and Hyalisma, which may be
3
Biogeography and Conservation
Table 3.2 List of families with fully mycoheterotrophic species present in each rainforest region
Central and South America
Burmanniaceae (8/24)
Corsiaceae (1/1)
Ericaceae (1/2)
Gentianaceae (2/19)
Orchidaceae (4/7)
Thismiaceae (2/14)
Triuridaceae (6/17)
Africa and Madagascar
Burmanniaceae (3/10)
Gentianaceae (2/2)
Iridaceae (1/2)
Orchidaceae (7/17)
Thismiaceae (2/13)
Triuridaceae (4/8)
India and Sri Lanka
Burmanniaceae (1/4)
Orchidaceae (4/7)
Thismiaceae (2/2)
Triuridaceae (2/3)
Southeast Asia
Burmanniaceae (2/15)
Corsiaceae (1/1)
Ericaceae (1/2)
Gentianaceae (1/4)
Orchidaceae (21/99)
Petrosaviaceae (1/3)
Polygalaceae (1/5)
Thismiaceae (1/24)
Triuridaceae (2/15)
Australasia
Burmanniaceae (2/8)
Corsiaceae (1/26)
Gentianaceae (1/1)
Orchidaceae (9/28)
Polygalaceae (1/2)
Thismiaceae (1/3)
Triuridaceae (2/12)
Pacific Islands
Burmanniaceae (2/4)
Orchidaceae (5/8)
Triuridaceae (2/5)
For each family the number of present genera/species is indicated between brackets
123
124
V.S.F.T. Merckx et al.
congeneric with Sciaphila. Gymnosiphon
(Burmanniaceae) is extremely widespread in the
tropics as well, yet has not been recorded in India,
Sri Lanka, and Australia. The distribution of
Burmannia (Burmanniaceae) is also pantropical,
although the genus is represented in East Africa
and Madagascar by chlorophyllous species only.
There is only one fully mycoheterotrophic
Burmannia species in the Neotropics, which limits
the South American distribution range of
Burmannia mycoheterotrophs. In Orchidaceae,
there are no tropical mycoheterotrophic genera that
occur both in the Old and the New World, although
a few Old World genera are extremely widespread
(e.g., Epipogium, Didymoplexis, Eulophia).
In the temperate zones, Monotropoideae
(Ericaceae) are extremely widespread, spanning
the entire northern temperate region and extending
into the tropics both in South America and Southeast
Asia. Hypopitys is the most widespread genus
of this group, and its distribution is almost identical
to the entire Monotropoideae. Corallorhiza
(Orchidaceae) is also widespread and occurs both
in the temperate zone of the Old and the New
World. In the Old World, however, the genus is represented only by C. trifida, which retains chlorophyll but obtains most of its carbon from fungi.
Mycoheterotrophic Neottia species (Orchidaceae)
also have a widespread distribution, ranging from
Europe and North Africa into Asia and Japan.
3.4.3
occurs throughout tropical Africa, India and Sri
Lanka, South China, Japan, Southeast Asia,
Australasia, and the Pacific Islands. Remarkably,
Epipogium roseum has not been reported from
Madagascar. Another widespread mycoheterotrophic orchid is Didymoplexis pallens,
which occurs from Afghanistan to India, Southeast
Asia, Australasia, and the Pacific Islands. The distribution of Eulophia zollingeri is only slightly
more restricted and covers Sri Lanka, South
China, Southeast Asia, Japan, and Australasia.
Hypopitys monotropa (Ericaceae) and the partial mycoheterotroph Corallorhiza trifida have
boreotropical distributions that cover almost the
entire northern temperate region. The distribution of Monotropa uniflora is slightly more
restricted as this species is absent from Europe
and most of temperate Asia. The orchid Epipogium
aphyllum is extremely widespread in the temperate regions of Europe, Asia, and Japan but is not
known from North America.
While widespread species in the Neotropics are
members of lineages that are associated with
arbuscular mycorrhizal fungi (e.g., Apteria
aphylla, Voyria aphylla), widespread species in
the Paleotropics are generally orchids that are
associated with saprotrophic fungi (e.g., Epipogium
roseum, Eulophia zollingeri). Widespread northern temperate species are all associated with ectomycorrhizal fungi (e.g., Hypopitys monotropa,
Monotropa uniflora, Corallorhiza trifida,
Epipogium aphyllum).
Widespread Species
While many species of mycoheterotrophic plants
have restricted distributions (see “Rarity”), some
species have remarkable widespread distribution
ranges. In the Neotropics, Apteria aphylla
(Burmanniaceae)
and
Voyria
aphylla
(Gentianaceae) are particularly widespread, and
their distribution almost completely overlaps with
that of the entire neotropical rainforest biome.
However, the Old World tropics are home to species with an even wider distribution especially
given the challenges to dispersal across Old World
tropical forests. The orchid species Epipogium
roseum has the most widespread distribution of
all tropical mycoheterotrophic plants. The species
3.4.4
Disjunct Distribution Patterns
The distributions of a few groups of mycoheterotrophic plants show remarkable disjunctions (i.e., distributions that are geographically
separated). On familial level, the distribution of
Corsiaceae is intriguing: Arachnitis grows in
Argentina, Chile, Bolivia, and the Falkland
Islands, Corsia has its center of diversity in New
Guinea and the Solomon Islands, and Corsiopsis
was collected once in southern China (Fig. 3.8a).
A Southern American–Australasian–Chinese disjunction is unusual in flowering plants, although
similar patterns are observed at both familial
3
Biogeography and Conservation
125
Fig. 3.8 Examples of disjunct distribution patterns in
mycoheterotrophic plants. (a) The distribution of Corsiaceae.
The large dot represents the single locality of Corsiopsis.
Note the disjunct distribution of Arachnitis in South
America. (b) The trans-Atlantic distribution of Voyria
(Gentianaceae). (c) Species of Oxygyne (Burmanniaceae)
have only been found in Cameroon and Japan. (d) Galeola
(Orchidaceae) is widespread in Southeast Asia and
Australasia, but one species is endemic to Madagascar and
the Comores. See text for further discussion
(Stylidiaceae; Good 1974) and generic (Coriaria;
Coriariaceae) level (van Balgooy 1966; Zhang
et al. 1999). The South American–Australasian
disjunction (Arachnitis–Corsia) in the family has
been hypothesized to result from a Gondwanan
tectonic link through Antarctica (Zhang et al.
1999). However, there is doubt that all genera of
Corsiaceae are closely related (Neyland and
Hennigan 2003; Petersen et al. 2006), and molecular phylogenetic studies are needed to resolve
this issue.
At the generic level, disjunct distributions
are quite common in full mycoheterotrophs.
An interesting disjunct pattern is observed in
Voyria (Gentianaceae), which comprises 18 species from tropical South and Central America and
one species from tropical West Africa (Fig. 3.8b).
It has been hypothesized that this pattern is either
the result of a long-distance dispersal event or the
relictual distribution of a previously continuous,
boreotropical distribution across the North
Atlantic (Albert and Struwe 1997). Due to the
estimated origin of the Gentianaceae (ca. 50 Ma;
Yuan et al. 2003), it is unlikely that this distribution is caused by ancient continental drift
(vicariance). The small dustlike seeds of Voyria
make a dispersal event plausible, although Albert
and Struwe (1997) note that the seeds of the
African Voyria species and its presumed neotropical sister species are not among the most highly
modified for wind dispersal compared to other
species in the genus. Also, a scenario of migration through Laurasia during the Eocene (e.g.,
Davis et al. 2002) cannot be excluded. Disjunct
relationships between Africa and the Neotropics
are not uncommon. Very similar South American–
West African disjunctions are present in the plant
families Rapateaceae and Bromeliaceae, which
have been explained as the result of long-distance
dispersal events rather than continental drift
(Givnish et al. 2004; Renner 2004).
In Thismiaceae, some notable disjunct distribution patterns are found in Thismia and Oxygyne.
Thismia is widespread in tropical South America,
Southeast Asia, and Australasia but is absent
from Africa. The occurrence of Thismia in the
Chicago area, many thousands of kilometers from
other Thismia populations, still remains unexplained (see below). The distribution of Oxygyne,
with records only from Cameroon and Japan,
also represents an extreme case of a geographic
disjunction unique in flowering plants (Fig. 3.8c).
126
However, this distribution pattern has to be interpreted with caution as the relationships between
the African and Japanese specimens of Oxygyne
are in need of close investigation.
In Triuridaceae, Seychellaria occurs in
Madagascar, the Seychelles, the Comores, and
Eastern Africa (Tanzania). Vollesen (1982) suggested that this distribution pattern results from
the breakup of Gondwana during the Cretaceous.
But Madagascar and Africa have been separated
since ca. 120 Ma (Rabinowitz et al. 1983; Ali and
Aitchison 2008), and most African–Malagasy
plant disjunctions have been explained by dispersal (Yoder and Nowak 2006). Thus, dispersal by
wind or water (Renner 2004; Ali and Huber
2010), perhaps aided by the occurrence of land
bridges (McCall 1997), may offer a more plausible explanation for the current distribution of
Seychellaria. Other Triuridaceae genera have disjunct distribution ranges as well, although the
pattern may be influenced by collecting bias:
Kupea occurs both in Cameroon and Tanzania,
but the genus was only recently discovered, and it
is possible that populations exist connecting these
two regions. The South American genus Triuris
has a patchy distribution with large gaps between
collection sites, but this also may reflect a sampling artifact rather than its actual distribution.
Geographic disjunctions are also observed in
several mycoheterotrophic lineages within
Orchidaceae. Species of Galeola, which are all
putative full mycoheterotrophs, occur in tropical
forests in Southeast Asia and New Guinea.
However, one species, G. humboltii, is endemic
to Madagascar and the Comoros (Fig. 3.8d). The
achlorophyllous species of Cephalanthera occur
as disjunct between North America and Southeast
Asia, but the distribution of achlorophyllous
Cephalanthera species overlaps with that of the
achlorophyllous species and also covers intervening areas. It is not yet clear whether full
mycoheterotrophy arose more than once in the
genus. In this case, the apparent disjunct distribution may in fact be indicative of multiple origins
of mycoheterotrophy in a particular lineage.
In Australia, Rhizanthella gardneri from
western Australia is separated from its relatives
R. omissa and R. slateri in southeastern Australia
V.S.F.T. Merckx et al.
by 3,500 km of desert. Dixon (2003) suggests
that Rhizanthella may have been present in the
paratropical forests that once covered the
Australian continent. These forests disappeared
when the climate of Australia became much drier
in the Middle and Late Miocene and Later
Pliocene, possibly separating Rhizanthella populations to their current distribution.
Lastly, in liverworts, the mycoheterotrophic
species Aneura mirabilis (Aneuraceae) occurs in
northwestern Europe and Greenland. A species
thought to be closely related to Aneura mirabilis
has been reported from Costa Rica providing an
interesting disjunction (Crum and Bruce 1996).
However, it remains to be confirmed if the species
from Costa Rica is the closest relative of Aneura
mirabilis or if this disjunct distribution is also the
result of convergent evolution of mycoheterotrophy in Aneura.
At the species level, it is mainly tropical
mycoheterotrophic species that have disjunct distributions. In many cases (e.g., tropical species in
Thismiaceae and Triuridaceae), these may represent sampling artifacts because the species are
known from only very few collections. A few
“real” disjunctions are notable. Thismia rodwayi
(Thismiaceae) occurs on Tasmania, mainland
Australia (Victoria, New South Wales, and
Queensland), and the North Island of New
Zealand. This distribution may be the result of
long-distance seed dispersal but can also be interpreted as a relict of a widespread ancestor (e.g.,
Heads 2009). It is doubtful whether there still is
genetic exchange between the populations on different landmasses. Another disjunction can be
found in the distribution of Arachnitis uniflora
(Corsiaceae), where Bolivian populations are
separated from populations in southern Argentina,
southern Chile, and the Falkland Islands by a
2,000–km-broad-belt of vegetation types that are
clearly unsuitable habitat for Arachnitis: the
Atacama desert, high mountain deserts and grasslands of the Andes, dry forests, the shrubby
“monte” vegetation, and the Patagonian grasslands (Ibisch et al. 1996). While recent longdistance dispersal remains a possible explanation
for this pattern, Ibisch et al. (1996) hypothesized
that the current gap was bridged along the Andes
3
Biogeography and Conservation
by islands of montane forests during glacial times
(18,000–19,000 years ago (ya)) allowing
Arachnitis to migrate into Bolivian tropical montane forests when the postglacial era started
(10,000–11,000 ya) (Ibisch et al. 1996).
Hypopitys monotropa and Monotropa uniflora
(Ericaceae) have remarkable transoceanic distribution ranges as well: the two species are found
in temperate zones on both sides of the Pacific
Ocean. Monotropa uniflora grows in large parts
of North America extending into montane regions
of Central and South America. It also occurs in
Asia, where it is found in Japan, southern China,
India to Nepal, and Bhutan (Wallace 1975).
Hypopitys monotropa has an even wider distribution that mainly overlaps with that of M. uniflora
but also includes temperate Europe. Thorne
(1972) categorized this distribution as “circumboreal.” Although there are no divergence time
estimates for these species, migration through
Beringia, a land bridge that connected North
America and temperate Asia at various times during the Pleistocene ice ages, seems the most
likely explanation for this distribution pattern
(Donoghue and Smith 2004).
The partial mycoheterotroph Corallorhiza
trifida (Orchidaceae) also has a circumboreal distribution, while all other Corallorhiza species are
restricted to the New World. Corallorhiza trifida
is not the earliest diverging species in the genus
(Freudenstein and Senyo 2008; Barrett and
Freudenstein 2008) and possibly dispersed through
Beringia, similar to the dispersal hypothesized for
both Monotropa and Hypopitys (see above).
3.5
Biogeographic History
3.5.1
Distributions of Families
and Genera: Vicariance Versus
Long-Distance Dispersal
In his treatment of the Burmanniaceae, Adolf
Engler noted the transoceanic distribution of
several genera and assumed that these genera
must be extremely old: “Aus dem Vorkommen der
Gattungen Burmannia, Gymnosiphon, Dictyostega
und Thismia in der alten und neuen Welt ergiebt
127
sich, dass die Familie der Burmanniaceae sehr
hohen Alters sein muss und dass höchstwahrscheinlich in der Tertiärperiode ihre
Verbreitung sich bis nach den Polen hin erstreckt
hat” (Engler 1888, p. 46). Written at a time when
the Earth’s geography was assumed to have been
stable, ancient dispersal across the poles seemed
the only possible explanation for the widespread
distribution of these genera. In 1915, the German
meteorologist Alfred Wegener published his theory of continental drift (Wegener 1915), although,
due to the lack of convincing mechanisms that
might have caused the movement and splitting of
huge landmasses, his theory only became widely
accepted in the 1960s after the discovery of plate
tectonics. From that time, the fragmentation of
Gondwana became an appealing explanation for
the widespread and disjunct distribution patterns
observed in many groups of plants (Raven and
Axelrod 1974) and has been used to explain the
disjunct distribution of Corsiaceae (Zhang et al.
1999) and Seychellaria (Vollesen 1982). However,
the application of molecular dating of lineage
divergences has suggested that most cases of
transoceanic distributions are unlikely to be the
result of tectonic vicariance simply because the
lineages are too young to have been dispersed
through ancient land connections (Renner 2004;
de Queiroz 2005).
The lack of fossil data and hypotheses of phylogenetic relationships have prevented detailed
studies on the biogeographic histories of most
mycoheterotrophic groups to date. There is only
one series of fossils that may be assigned to an
extant mycoheterotrophic lineage. These fossils
are from the Late Cretaceous (about 90 Ma) and
were found in New Jersey (Gandolfo et al. 1998).
A phylogenetic analysis based on morphological
characters placed the two fossil genera Mabelia
and Nuhliantha within extant Triuridaceae
(Gandolfo et al. 2002). However, it remains questionable whether these plants were in fact mycoheterotrophic because the fossilized material only
consists of flowers (Gandolfo et al. 2002).
Moreover, the fossilized pollen lacks distinctive
features of pollen of extant members of the
Triuridaceae (Furness et al. 2002). If the fossils
represent genuine remnants of Triuridaceae, they
128
V.S.F.T. Merckx et al.
Fig. 3.9 Geological area cladogram showing the progressive breakup of Gondwana. Vertical lines indicate collisions between landmasses. South America is shown twice
to illustrate its separation from both Africa and Antarctica.
Representations of landmasses are not drawn to scale.
Cladogram modified from Sanmartin and Ronquist (2004)
and Cox and Moore (2010). 1 Age estimate from Gandolfo
et al. (2002). Fossils were found in North America
(Laurasia). 2 Mean molecular clock estimate taken from
Merckx et al. (2008). 3 Molecular clock estimates of crown
node ages of Orchidaceae subfamilies taken from Ramirez
et al. (2007). 4 Mean molecular clock estimate from
Merckx et al. (2010a). In this study, Thismia is paraphyletic and includes Haplothismia and Tiputinia
show that the family occurred at higher latitudes
than today, at least during the Late Cretaceous
when the climate was warmer than present. Also,
if major Triuridaceae lineages had diverged by the
Late Cretaceous, the breakup of Gondwana may
have played a significant role in the distribution of
the family (Fig. 3.9). Nevertheless, the occurrence
of Sciaphila species on isolated oceanic islands
(e.g., Bonin, see Fosberg and Sachet 1980; Fiji,
see van de Meerendonk 1984) indicates that longdistance dispersal is certainly an important factor
in the widespread distribution of this genus and
probably for Triuridaceae in general.
In the absence of fossil data, divergence time
estimates for biogeographic reconstructions can
be obtained through broadscale molecular clock
analyses which allow for inclusion of fossil data
from distant groups or by using secondary calibration points. These strategies have been used
to investigate the biogeographic history of
Burmanniaceae (Merckx et al. 2008). The obtained
age estimates suggest that Burmanniaceae genera
are relatively ancient and diverged from each
other during the Cretaceous probably in South
America. However, the obtained hypothesis suggests that the widespread genera Burmannia and
Gymnosiphon reached their transoceanic distribution range during the Eocene, when the breakup
of Gondwana was well under way (Fig. 3.9). This
demonstrates that both genera obtained their
3
Biogeography and Conservation
current pantropical distribution by dispersal,
probably aided by various land bridges. In particular, dispersal of Burmannia and Gymnosiphon
out of South America may have been possible by
“boreotropical” migration routes: during the
Eocene, global temperatures peaked, and tropical
vegetation occurred at high latitudes. This allowed
for migration of tropical flora between the
Neotropics and the Paleotropics over the “North
Atlantic Land Bridge” (Tiffney 1985; Davis et al.
2002). The disjunct distribution of Voyria
(Gentianaceae) between the Neotropics and
Africa has also been explained as a relict of an
ancient boreotropical distribution (Albert and
Struwe 1997; see above). Similarly, molecular
clock analyses suggest a Cretaceous origin for
Thismiaceae, but diversification occurred well
after the breakup of Gondwana, rendering a
“Gondwanian aborigine” explanation for its
widespread distribution unlikely (Merckx and
Bidartondo 2008; Merckx et al. 2010a; Fig. 3.9).
In Orchidaceae, mycoheterotrophy evolved
multiple times independently in subfamilies
Vanilloideae, Orchidoideae, and Epidendroideae,
all of which diversified after the start of the
breakup of Gondwana (Ramirez et al. 2007;
Fig. 3.9; Chap. 5). Thus, any mycoheterotrophic
genus in Orchidaceae with a distribution that
covers multiple Gondwanan fragments must have
acquired their distribution through dispersal
rather than vicariance. The widespread genus
Gastrodia, for instance, with a distribution that
covers tropical Africa, Madagascar, Southeast
Asia, Australasia, and the Pacific Islands, belongs
to the Epidendroideae. Gastrodia therefore
diverged and diversified after the breakup of
Africa, Madagascar, and India (Fig. 3.9) and must
have migrated by long-distance dispersal. Similar
observations can be made for widespread genera
Didymoplexis, Galeola, Epipogium, Eulophia,
and Gastrodia. In addition, distributions that
include oceanic islands must have been the result
of long-distance dispersal (e.g., Stereosandra).
In conclusion, widespread lineages of mycoheterotrophic plants are generally too young to
have acquired their distribution by tectonic vicariance. In some cases, temporary land bridges may
have aided migration between fragments of
129
Gondwana. However, we hypothesize that transoceanic dispersal has been the most important
factor in the widespread distributions of mycoheterotrophic plants. Most mycoheterotrophic
plants produce large amounts of small dustlike
seeds which promotes dispersal and increases the
likelihood of reaching suitable microsites for
recruitment (Eriksson and Kainulainen 2011).
3.5.2
Species Distributions
Only few phylogeographic studies on fully mycoheterotrophic plants have been carried out. Recent
phylogeographic studies on Hypopitys monotropa
in North America (Beatty and Provan 2011a) and
Europe (Beatty and Provan 2011b) provide the
first detailed hypotheses about the glacial history
of a mycoheterotrophic plant species (see also
Chap. 6). Population genetic data and ecological
niche modeling suggest that the current east–west
disjunct distribution of H. monotropa in North
America results from the existence of separate
eastern and western refugia during the last glaciation. In Europe, H. monotropa probably recolonized northern Europe from refugia in the Balkans
and southern Europe, a scenario that is suggested
for many European taxa (Provan and Bennett
2008). The high species diversity of mycoheterotrophic plants in tropical postulated glacial
refugia (see further) suggests that glacial and
interglacial cycles that characterized the
Quaternary period (ca. 2.6 Ma to present) have
had a significant effect on the distributions of
tropical mycoheterotrophic species as well.
3.6
Habitat Characteristics
3.6.1
Light
Most mycoheterotrophic plants grow in forests
with a dense overstory that produces deep shade.
Probably due to the lack of light, these microhabitats often have little or no herbaceous ground flora
(Leake 1994; Cheek and Williams 1999). Since
mycoheterotrophs do not require light to grow,
the occurrence of most of these plants to deeply
130
V.S.F.T. Merckx et al.
shaded sites lacking herbaceous autotrophs suggests their mode of life evolved to provide escape
from competitive exclusion in the shaded conditions of forest understory habitats (Bidartondo
et al. 2004). Indeed, in partially mycoheterotrophic
orchids, it has been shown that low light levels
result in strong mycoheterotrophy, while higher
irradiances successively drive the orchids toward
autotrophy (Preiss et al. 2010).
3.6.2
Water
Besides their preference for low-light habitats,
the availability of water seems an important
feature for mycoheterotrophic plant habitats.
Bakshi (1959) noted that Pterospora is particularly associated with moist soils. Summerhayes
(1951) assumed that a moist but well-drained soil
is thought to favor the fungal symbiont of
Epipogium aphyllum. Mycoheterotrophic plants
from tropical rainforests seem to prefer local
habitats with very moist soils as well (Maas et al.
1986; Cheek and Williams 1999). Moreover,
some species are often found near perennial or
seasonable streams (Maas et al. 1986; Cheek and
Williams 1999; Taylor and Roberts 2011). In
Africa, areas with a high diversity of mycoheterotrophic plants seem to overlap with postulated rainforest refugia (Cheek and Ndam 1996).
The occurrence of these refugia is strongly correlated with rainfall as well (Linder 2001), indicating minimal seasonality and a stable, moist
environment year-round. In general, mycoheterotrophs seem to prefer habitats with high
rainfall and short dry seasons. For example, on
Mount Kupe, one of the richest sites for mycoheterotrophic plants in Africa, annual rainfall
exceeds 4,000 mm with only 3 months with less
than 100 mm precipitation (Hofer et al. 2000).
Similarly, Reserva Ducke in Brazil receives over
2,000 mm of rainfall and has a dry season of 3
months (Iriondo and Latrubesse 1994; ter Steege
et al. 2003). There is some evidence that mycoheterotrophic plants are sensitive to desiccation.
In dry summers, the flowering stems of Monotropa
uniflora, Hypopitys monotropa, and Neottia
nidus-avis suffer severely from drought and often
fail to expand before drying out (Snetselaar and
Whitney 1990; Leake 1994). Klooster and Culley
(2009) observed that a drought in the summer
and fall of 2007 likely contributed to the overall
decline in reproductive effort and output of
Monotropa with some populations experiencing
100% floral abortion.
3.6.3
Soil Types
Both in temperate and tropical zones, mycoheterotrophic plants occur on a variety of soil
types, including organic soils, clay, loam, and
white sand (Wallace 1975; Maas et al. 1986;
Maas and Ruyters 1986). They generally prefer
acidic soils. Reported soil pH values for mycoheterotrophic habitats in temperate regions range
from 5.2 to 6.2 (Wallace 1975; Gebauer and
Meyer 2003; Bougoure et al. 2008), but Merckx
et al. (2010b) reported a soil pH of 3.8 at a tropical rainforest site in French Guiana where
Dictyostega and Voyria species were found.
Mycoheterotrophs are often found in places with
a thick layer of decaying leaf litter (Graham 1953;
Paul 1964; Van Royen 1972; Richards 1976;
Maas and Ruyters 1986). In some cases, their
flowers fail to emerge through this layer, for
example, Monotropsis (Copeland 1939), Thismia
rodwayi (Campbell 1968), Epipogium and Neottia
spp. (Davies et al. 1988). Rhizanthella species
remain entirely underground when flowering and
fruiting (George 1980).
The roots of some species, for example, Voyria
rosea and Campylosiphon purpurascens, can
penetrate the soil to a depth of 20 cm and more
(Maas et al. 1986; VSFTM pers. oberv.).
Contrarily, the roots of a few species (e.g., Voyria
aphylla, V. flavescens, V. primuloides, Afrothismia
foertheriana) are entirely located in the uppermost soil strata, which consists of lose decaying
leaf litter (Franke 2002; Franke et al. 2004;
VSFTM and CDS pers. observ.).
3.6.4
Elevation
Mycoheterotrophic plants occur from sea level to
montane forests generally up to 2,000 m. In North
America, Monotropoideae can occur up to
3
Biogeography and Conservation
4,000 m (Wallace 1975). In the Neotropics,
Apteria, Dictyostega, and Gymnosiphon species
are sometimes found above 2,000 m (Maas et al.
1986). In East Africa, mycoheterotrophs often
occur at high elevations; Epipogium roseum is
recorded from Mount Kilimanjaro at 2,500 m
(Cheek and Williams 1999). In New Guinea, species of Corsia generally inhabit forests between
900 and 1,500 m, extending into the upper part of
lowland forest and into montane forest (Van
Royen 1972).
3.6.5
Plant Communities
Mycoheterotrophic plants occur in a variety of
forest communities. In temperate zones,
Monotropoideae occur in forests dominated by
conifers (pines and cypress), beech, and oak
(Wallace 1975; Ogura-Tsujita et al. 2009).
Similarly, fully mycoheterotrophic orchids are
generally found in forests dominated by pines,
beech, and oak trees (Gebauer and Meyer 2003;
Bidartondo et al. 2004; Zimmer et al. 2008;
Taylor and Roberts 2011). These forests tend to
have higher pH soils than other temperate forest
habitats.
Information on plant communities is purely
anecdotal for species that occur in the tropics. In
the Neotropics, species of Gymnosiphon
(Burmanniaceae) are often found in Mora forest
(Maas et al. 1986). In West Africa, Afrothismia
(Thismiaceae) occurs in proximity of a wide variety of rainforest trees, including species of Cola,
Diospyros, and Tabernaemontana (Franke 2004;
Sainge et al. 2005; Dauby et al. 2007). Tropical
mycoheterotrophic orchid species of Aphyllorchis
and Cephalanthera have been found in Fagaceae
and Dipterocarpaceae forest in Thailand (Roy
et al. 2009). In Southeast Asia, mycoheterotrophic
plants are sometimes found in bamboo thickets,
for example, Epirixanthes (Chen et al. 2008),
Thismia (Chantanaorrapint 2008), and Gastrodia
confusa (Ogura-Tsujita et al. 2009).
Arbuscular mycorrhizal mycoheterotrophs are
sometimes reported from forest communities
dominated by ectomycorrhizal trees. In New
Guinea, species of Corsia (Corsiaceae), for example, are mostly found in beech and oak forests
131
(Van Royen 1972). In Southeast Asia, species of
Thismia are often collected from forest dominated
by Dipterocarpaceae or Fagaceae trees (Jarvie
1996; Yang et al. 2002; Tsukaya and Okada 2005).
In Japan, Oxygyne shinzatoi (Thismiaceae) has
been found in Castanopsis forest (Yokoyama
et al. 2008). However, in Argentina, Arachnitis
uniflora (Corsiaceae) was found to link with the
same arbuscular mycorrhizal fungi as Osmorhiza
chilensis (Apiaceae), Austrocedrus chilensis
(Cupressaceae), and Nothofagus dombeyi
(Nothofagaceae) (Bidartondo et al. 2002). The
latter species had been previously reported as
ectomycorrhizal (Fontenla et al. 1998).
A very strong preference toward a particular
plant community is observed for the underground
orchid Rhizanthella gardneri (Orchidaceae),
which only occurs in Melaleuca uncinata thickets
in West Australia (Bougoure et al. 2008). In
Tasmania, Thismia rodwayi (Thismiaceae) is
always found in wet forest dominated by
Eucalyptus trees (Wapstra et al. 2005).
3.6.6
Exceptional Habitats
There are plenty of exceptions to the general habitat preferences listed above. In the Neotropics,
Apteria aphylla (Burmanniaceae) and several
Voyria species (Gentianaceae) are known to occur
in wet grasslands and savannas (Maas et al. 1986).
Arachnitis (Corsiaceae) has been recorded on the
treeless East Falkland Island, “growing in sand
amongst rocks on an eroded sandstone ridge”
(Cribb et al. 1995). In Africa, mycoheterotrophic
Brachycorythis orchids occur in woodland and
wooded grassland (Cheek and Williams 1999).
Monotropoideae are often found in open vegetations, such as dune slacks (Wallace 1975; Leake
1994). The enigmatic species Thismia americana
(Thismiaceae) was discovered in the margin of a
grass field (Pfeiffer 1914), and the western underground orchid Rhizanthella gardneri grows in
shrublands, in habitats of low-nutrient availability and high light levels (Bougoure et al. 2008).
Hexalectris spicata (Orchidaceae) occurs in
diverse habitats: from swamps to oak canyons
rising out of the desert (Luer 1975). And while
mycoheterotrophic species are usually terrestrial,
132
V.S.F.T. Merckx et al.
Voyria spruceana and V. aphylla (Gentianaceae)
have been found growing as epiphytes up to 30 m
high in trees in Colombia (Groenendijk et al.
1997). Burmannia kalbreyeri (Burmanniaceae) is
also known to grow epiphytically, but this species
retains chlorophyll and has well-developed leaves
(Maas et al. 1986). Lastly, several species of
Sciaphila (Triuridaceae) are often found growing
on termite nests (van de Meerendonk 1984; Maas
and Ruyters 1986), and Franke (2002) reported a
specimen of Voyria flavescens (Gentianaceae)
growing top of a termite mound of Embiratermes
neothenicus (Isoptera, Nasutitermitinae).
3.6.7
Population Size
Even within suitable habitats, populations of
mycoheterotrophic plants are mostly thinly
scattered. Population sizes are usually small, with
less than 15 individuals per population, but plants
can only be detected when aboveground parts are
present (flowering and fruiting stages), so the
actual population size is difficult to determine. In
some cases, populations of over hundreds of
flowering specimens have been reported (e.g.,
Gymnosiphon Cheek and Williams 1999;
Burmannia Fensham 1993).
3.6.8
Co-occurrence
Many authors have noted that different species of
mycoheterotrophs (often from different families),
both in temperate and tropical zones, have the
tendency to grow together (e.g., van der Pijl 1934;
Jonker 1938; Van Royen 1972; van de Meerendonk
1984; Maas and Rübsamen 1986; Cheek and
Williams 1999). Indeed, after a mycoheterotrophic
plant is spotted in a forest, closer inspection of
the area will often reveal other species growing
close by (Maas et al. 1986; Cheek and Williams
1999). There is no explanation for this phenomenon. A few authors have suggested that cooccurring mycoheterotrophs are possibly sharing
the same mycorrhizal fungus (Cheek and
Williams 1999; Cheek 2003b) but no evidence
has been found to support this. In contrast,
Merckx et al. (2010b) sampled specimens of
Voyria aphylla (Gentianaceae) and Dictyostega
orobanchoides (Burmanniaceae) co-occurring at
a rainforest plot in French Guiana and found that
they were associated with nonoverlapping AMF
lineages. A specimen of Campylosiphon purpurascens (Burmanniaceae) that occurred at this spot
was found to utilize distinct fungal lineages as
well (VM, unpublished data). Similarly, Courty
et al. (2011) identified distinct lineages of arbuscular mycorrhizal fungi in roots of Voyria aphylla
(Gentianaceae),
Apteria
aphylla,
and
Gymnosiphon sp. (Burmanniaceae) growing at a
site in Guadeloupe. Interestingly, many patches
of rainforest in French Guiana that are rich in
mycoheterotrophic
Burmanniaceae
and
Gentianaceae are also inhabited by the mycoheterotrophic orchid Wullschlaegelia calcarata
(Orchidaceae) (VSFTM pers. oberv.), yet
Wullschlaegelia is associated with saprotrophic
fungi (Martos et al. 2009), while Burmanniaceae
and Gentianaceae exploit arbuscular mycorrhizal
mycorrhiza. In the temperate forests of Northwest
America, different species of ericaceous mycoheterotrophs are often found growing together
(Wallace 1975) but are each specialized on different mycorrhizal fungi (Bidartondo and Bruns
2001, 2002). Similarly, Taylor and Bruns (1999)
investigated the mycorrhizal associations of the
mycoheterotrophic orchids Corallorhiza maculata and C. mertensiana over a wide geographic
range and found that they never shared fungal
species, even when growing intermixed. In these
cases, co-occurrence of mycoheterotrophs cannot
be explained by specialization on the same “host”
fungus. The pattern may reflect access to different resources by different fungal taxa and thus
would result from competition rather than convergence. Plant sister species that occur in sympatry but grow with different fungal lineages may
result from a speciation process driven by mycorrhizal specialization (Chap. 5). Other factors that
may cause co-occurrence of mycoheterotrophs
include similar preferences of mycoheterotrophs
and/or their associated mycorrhizal fungi toward
certain microhabitats or similar dispersal biases.
3
Biogeography and Conservation
3.7
Biodiversity Hotspots
A few localities are notorious for their high number of mycoheterotrophic species. For example,
Mount Kupe in Southwest Cameroon is often
cited as the richest site for mycoheterotrophic
plants in Africa (Cheek and Cable 1997; Franke
2004). Two decades of intensive surveys on the
slopes of this mountain have revealed twelve different mycoheterotrophic species, including two
Afrothismia species yet to be described (Franke
2007; Moses N. Sainge, pers. comm.). Therefore,
Mount Kupe is home to about one-fourth of all
mycoheterotrophic species known from continental tropical Africa. The adjacent Mount Cameroon
has a comparable diversity of mycoheterotrophic
plants, although some species may be extinct due
to extensive habitat destruction (Schlechter 1906;
Cheek and Williams 1999; Franke et al. 2004).
Mount Kupe and Mount Cameroon are part of the
Lower Guinea rainforest region, which is a center
of diversity and endemism for mycoheterotrophic
plants (see above) and for flowering plants in
general (Linder 2001; Plana 2004). The stunning
diversity of plants in this region can be explained
by modern patterns in rainfall seasonality, while
the high level of endemism is probably related to
paleoclimatic fluctuations, and the area has likely
served as a rainforest refugium during glacial
maxima (Linder 2001; Plana 2004). In Africa,
centers of diversity of mycoheterotrophic plants
all occur in areas that have been thought to be
glacial refugia. Since many mycoheterotrophic
plants are vulnerable to disturbance, have very
narrow habitat preferences, and seem to have very
slow dispersal rates, it has been proposed that
mycoheterotrophic plants may be suitable indicators of Pleistocene rainforest refugia (Cheek and
Ndam 1996; Cheek and Williams 1999).
Another mycoheterotrophic plant “hotspot” is
the Reserva Ducke near Manaus (Brazil). In an
area of only 100 km2, no less than 22 mycoheterotrophic species have been found, or over
25% of the total species diversity of mycoheterotrophic plants in the Neotropics. Two species of Triuridaceae (Sciaphila oligantha and
S. rubra) are endemic to the reserve (Ribeiro et al.
1999; Maas and Rübsamen 1986; Maas and Maas
133
2005). The Reserva Ducke is characterized by an
extremely high diversity of flowering plants
(Ribeiro et al. 1999). Patterns of tree diversity in
the Amazon rainforest have been linked to soil gradients and the current climate, and particularly
rainfall seasonality (ter Steege et al. 2003, 2006),
although recent research has indicated that paleoclimate probably had a much greater effect on current patterns of tree diversity than current climate
(Hoorn et al. 2010; ter Steege et al. 2010). Indeed,
the high diversity of plant species found in Reserva
Ducke has been attributed to its position at the contact point among several Tertiary and Quaternary
refugia, indicating that its diversity may have been
enhanced by the coalescence of the distributions of
former allopatric species in this area (Oliveira and
Daly 1999; Oliveira and Mori 1999).
The most species-rich locality of mycoheterotrophic plants in Southeast Asia is Mount
Kinabalu in Malaysian Borneo. Since botanical
explorations on the slopes of the 4,095 m high
mountain started in the second half of the
nineteenth century, 29 species of fully mycoheterotrophic plants have been recorded. These
include 16 species of orchids, of which
Didymoplexiella kinabaluensis and Gastrodia
spathulata (formerly Neoclemensia spathulata)
have not been found elsewhere (Wood et al.
2011). Burmanniaceae and Thismiaceae are both
represented with two fully mycoheterotrophic
species, Triuridaceae with five species,
Polygalaceae with three fully mycoheterotrophic
species, and Petrosaviaceae with a single species
(Beaman and Beaman 1998; Beaman and
Anderson 2004). Mount Kinabalu is ca. 1.5 million years old and therefore comparatively young
in geological terms. The flora is exceptionally
diverse with a high percentage of endemicity
(Wong and Phillipps 1996; Wood et al. 2011).
The high diversity of plant species on Mount
Kinabalu has been attributed by the occurrence
of a wide range of soil types and climatic conditions. The endemic species of Mount Kinabalu
may be relicts of ancient, more widespread distribution ranges, or recent species that result from
rapid adaptive radiation, catastrophic selection
and drift, and dispersal of propagules from distant and neighboring mountain systems (Wong
and Phillipps 1996).
134
V.S.F.T. Merckx et al.
Other areas with high numbers of mycoheterotrophic species include Saül (French
Guiana) (Clarke and Funk 2005) and Mabura
(Guyana) (Ek and ter Steege 1997). In temperate
Northwest America, mainly in the coastal areas
of northern California, Oregon, and Washington,
there are many small “hotspots” where distribution ranges of several Monotropoideae species
overlap (Wallace 1975).
Molecular clock evidence indicates that
Burmanniaceae and Thismiaceae have Cretaceous
origins and major diversification began shortly
after the mass extinctions at the K/T boundary,
suggesting that glacial periods may have had a
significant influence on their current distributions
(Merckx and Bidartondo 2008; Merckx et al.
2008). In addition, these analyses indicate that
speciation events within mycoheterotrophic
Dioscoreales lineages predate the Pleistocene
glaciations. Based on this evidence, it seems that
during glacial maxima rainforest refugia have
acted as “museums” of ancient lineages of mycoheterotrophic Dioscoreales rather than as speciation “engines” (see Plana 2004). However,
mycoheterotrophic species of other families that
are endemic to a particular hotspot may result
from recent speciation events. For example, several species of orchids endemic to Mount
Kinabalu have evolved from vertical altitudinal
radiation of lowland congeners or dispersal from
neighboring mountain systems most likely after
the uplift of the mountain (1.5 million years ago)
and can be considered as “neoendemics”
(Barkman and Simpson 2001; Wood et al. 2011).
The endemic mycoheterotrophic orchids of
Mount Kinabalu may therefore be recent species
as well. Thus, hotspots of mycoheterotrophic
plant diversity may be both “museums” and “cradles” of diversity.
3.8
Endemism and Rarity
Mycoheterotrophic plants are seldom found in
high abundances. That does not mean that all species are rare. Some species have wide distribution
ranges and occur in a variety of habitat types
(e.g., Hypopitys monotropa, Epipogium roseum).
But even widespread mycoheterotrophs may still
be extremely rare on a local scale. Epipogium
aphyllum, for example, has a widespread distribution in temperate Eurasia, but on a local scale,
it is often considered to be extremely rare. In
Britain, it has been frequently described as the
rarest orchid and even as Britain’s rarest plant
(Taylor and Roberts 2011). In addition, many
mycoheterotrophs seem to have very limited distribution ranges and/or have extremely low abundances (e.g., known from very few populations).
For example, most neotropical Thismia species
are only known from one or two collections
(Maas et al. 1986). A large number of African
mycoheterotrophs are also known from only one
or two localities (e.g., species in the genera
Afrothismia, Kupea, Kihansia, Oxygyne, Auxopus,
and Gastrodia). Similarly, the enigmatic underground orchid (Rhizanthella gardneri) is known
from only a handful of sites in Southwest
Australia (Bougoure et al. 2008). Numerous other
mycoheterotrophic species from all continents
share this apparent rarity.
It is important to note that our knowledge
about the occurrence of fully mycoheterotrophic
plants may be considerably biased by the plants’
ability to remain unnoticed by collectors. Many
species, particularly those from tropical rainforests, are only known from remote areas where
botanical inventories have yet to be carried out.
Moreover, mycoheterotrophs can only be spotted
when they are flowering or fruiting, mostly for a
short period of time only and often in the wet season, when few botanists are eager or able to enter
the forest. The rest of the year, they remain underground hiding from discovery, and they may not
even flower each year. We lack detailed information on the phenology of most mycoheterotrophs,
but, for example, in the ghost orchid (Epipogium
aphyllum), it has been observed that populations
can disappear for up to 30 years between successive flowering episodes at the same site (Leake
1994). This suggests that some mycoheterotrophs
may have very cryptic flowering cycles. Finally,
mycoheterotrophs are generally very difficult to
spot due to their small size and hyaline coloration. They often fail to protrude above the dense
leaf litter and remain covered by fallen leaves,
3
Biogeography and Conservation
135
Fig. 3.10 Number of species in a selection of mycoheterotrophic genera that occur in the tropics (Thismia,
Sciaphila, Gymnosiphon, Aphyllorchis, Lecanorchis, and
Afrothismia) and their year of publication. Data based on
the World Checklist of Selected Plant Families (2010)
even when flowering. It is little wonder that
mycoheterotrophs are often spotted by mushroom
hunters or by a botanist during a sanitary break;
some species may be more abundant than we presume because we just fail to find them even when
actively looking for them. The fact that new species are constantly being described and thus
escaped discovery for a long time illustrates the
secret nature of mycoheterotrophs (Fig. 3.10).
Some new species were spotted only after
extensive long-term monitoring. Notorious is the
discovery of two new Afrothismia (Thismiaceae)
species in Korup Forest Dynamic Plot in
Cameroon (Sainge and Franke 2005; Sainge et al.
2005). This 50-ha plot was established in 1994
and is constantly monitored, yet two Afrothismia
species escaped discovery for almost a decade,
despite the fact that a path through the plot was
also going through one of the Afrothismia populations (Franke 2007). The spectacular species
Tiputinia foetida (Thismiaceae), with a flower of
5 cm in diameter, was discovered in 2005 in a
biological station in Ecuador growing within a
meter of the path linking the station’s dining hall
to the laboratory (Woodward et al. 2007).
The influence of collection effort has been
addressed for the rare species Thismia rodwayi
(Roberts et al. 2003; Wapstra et al. 2005). From
its discovery in 1890 until 2002, there were only
five records of T. rodwayi in Tasmania (Roberts
et al. 2003). Since the discovery of two specimens at a new site in Tasmania, subsequent
searches on this and other sites with similar habitat characteristics revealed a total of 110 T. rodwayi flowers (Roberts et al. 2003), and T. rodwayi
is now known from 26 sites from 7 disparate
locations in Tasmania (Wapstra et al. 2005)
(Fig. 3.11). Although these numbers certainly do
not upgrade T. rodwayi to a common species, it
can be concluded that it is at least more abundant
136
V.S.F.T. Merckx et al.
Fig. 3.11 Distribution of Thismia rodwayi (Thismiaceae)
in Tasmania. (a) A flower of T. rodwayi. (b) Known distribution of Thismia rodwayi based on records before 2002.
(c) Distribution of T. rodwayi based on all records up to
2005. Maps adapted from Roberts et al. (2003) and
Wapstra et al. (2005)
than presumed by previous collections. As
standard biological inventories failed to encounter T. rodwayi (Roberts et al. 2003), another
conclusion that can be drawn from this study is
that this species, and other inconspicuous mycoheterotrophs, can only be reliably recorded by
targeted surveys. Because very few botanists
search tropical rainforests specifically for mycoheterotrophic plants, the majority of collections
result from chance encounters, hence explaining
the lack of collections for so many known mycoheterotrophic species. The few intensive searches
for mycoheterotrophic plants that have been carried out lead, in many cases, to the discovery of
unexpected mycoheterotrophic plant diversity or
even to the discovery of undescribed taxa (e.g.,
Franke 2007).
Despite the probable impact of collection
effort, there is no doubt that the paucity of records
for many mycoheterotrophic species is the result
of “real” rarity and high local endemism
(Kruckeberg and Rabinowitz 1985). This is obvious for species that are part of well-known floras
(e.g., Epipogium aphyllum in Britain, Thismia
americana in North America). In lesser-known
tropical regions, differences in rarity among species are becoming more obvious with targeted
collecting. Comparing herbarium records between
species with similar habit, it becomes clear that
some species are encountered more frequently
than others (Fig. 3.12). In the Neotropics, for
example, there is a very pronounced difference in
collection frequency between mycoheterotrophic
Burmanniaceae and Gentianaceae on the one
hand and Thismiaceae and Triuridaceae on the
other. This can only be explained by differences
in distribution and abundance. According to
Harper (1981), rare plant species can be classified
based on space, group, or time relatedness. Spacelimited species may be locally abundant but only
occur in a limited number of sites. Their distributions may be restricted due to high niche
specificity or dispersal barriers. These species are
often local endemics. Group-dependent species
occupy a specialized niche with a limited distribution, associated with certain ecotypes often at
ecological frontiers for species. Rarity in timedependent species results from fluctuations in
population numbers following adverse sporadic
or cyclical events, such as drought or fire (Swarts
and Dixon 2009). Most rare mycoheterotrophic
species seem to belong to the first and second categories, although time-dependent rarity may
occur as well.
The influence of abiotic factors on the distribution of mycoheterotrophic plants remains to be
determined. The fact that (rare) mycoheterotrophs of different species are often found growing
at the same site, but in association with different
fungi, possibly indicates that distribution of
mycoheterotrophic species, or their associated
fungi, is restricted by adaptations to similar
3
Biogeography and Conservation
137
Fig. 3.12 The number of herbarium records cited in the
Flora Neotropica for a selection of neotropical
Burmanniaceae (Apteria aphylla, Gymnosiphon divaricatus, Miersiella umbellata) and Triuridaceae (Sciaphila
albescens, Peltophyllum luteum). Data obtained from
Maas et al. (1986) and Maas and Rübsamen (1986). For
comparison, the habit of each species drawn at the same
scale is shown above
microhabitats. These microhabitats can be
characterized by certain abiotic factors such as
soil type, humidity, and water availability.
Alternatively, this pattern of co-occurrence may
be explained by similar dispersal and colonization patterns.
Next to abiotic factors, biotic dependency may
play an important role in the distribution range
and abundance of mycoheterotrophic plants
(Fig. 3.13). As fully mycoheterotrophic plants
are completely dependent on their (often very
specific) associated fungi, the availability of these
fungi will be essential for the plant’s establishment. Mycoheterotrophs that are specialized on
rare fungi may thus be a priori severely limited in
their distribution range. The range of the fungi
may be restricted to certain abiotic habitat
requirements and dispersal barriers (see further).
In addition, some mycorrhizal fungi may also
show specificity toward particular autotrophic
plants. This can create a very complex tripartite
biotic dependency for a mycoheterotrophic plant.
For example, Rhizanthella gardneri is associated
with a specific fungus, which is possibly only
able to form ectomycorrhizas with Melaleuca
uncinata (Bougoure et al. 2009). Furthermore, it
is possible that the host fungus is not always able
to serve as a suitable host for a mycoheterotrophic
plant. Theoretically, a mycoheterotrophic plant
will only successfully grow and reproduce if its
associated fungus is able to provide enough carbon from coassociated trees or, in case of saprotrophic fungi, from dead material. For obligate
mycorrhizal fungi, this may be influenced by the
size of their network and the number, age, and
identity of its associated autotrophic plants.
Competition between different fungus species
may influence their ability to allocate nutrients as
well (Bever et al. 2009).
Specificity to aboveground biotic interactions
may also induce rarity (Swarts and Dixon 2009).
Specialized pollination systems, in a manner similar to the level of specialization in mycorrhizal
associations, may play a role in causing rarity in
138
V.S.F.T. Merckx et al.
Fig. 3.13 Primary biotic agents that may limit the abundance and distribution of mycoheterotrophic plants.
Overlap indicates potential biological dependency of the
mycoheterotroph on that factor. See text for further discussion. Figure based on Swarts and Dixon (2009)
mycoheterotrophs. It has been hypothesized that
mycoheterotrophic plants that show high
specificity in their mycorrhizal interactions probably have generalist pollination syndromes and/or
exhibit autogamous self-pollination due to the
evolutionary instability inherent to specializing
on two lineages (Bidartondo 2005). We know little about the pollination strategy of mycoheterotrophic plants, but support for Bidartondo’s
hypothesis concerning absence of specialized
pollination syndromes has been found for mycoheterotrophic orchids (Dressler 1981; Benzing
and Atwood 1984; Arditti 1992; Molvray et al.
2000) and mycoheterotrophic plants in general
(Leake 1994). However, detailed studies on the
reproductive biology of Hypopitys, Monotropa,
and Monotropsis (Klooster and Culley 2009) and
Voyria (Hentrich et al. 2010) revealed the presence of outcrossing and specialization in pollination interactions (see Chap. 7). Therefore, it is
possible that, in some cases, both pollinator and
fungal specificity affects the distribution mycoheterotrophic plants (Waterman and Bidartondo
2008). Comparative population approaches
(Thompson 2005), where both mycorrhizas and
reproductive traits for multiple populations of a
single mycoheterotrophic species are examined,
are needed to explore the effect of both mutualisms on the distribution of mycoheterotrophs.
A recent study has addressed this interaction for
achlorophyllous orchids of the tribe Coryciinae,
which show specificity both in pollinators and
associated fungi (Waterman et al. 2011).
Interestingly, when orchids were subjected to
transplant experiments, it was found that effective
pollination does not occur outside native regions,
whereas effective fungi can be recruited. This
strongly suggests that pollination specificity has
more influence on the local distribution of the
species than does mycorrhizal specificity.
However, it can be argued that mycorrhizal selection pressure is less influential for initially mycoheterotrophic plants than for full mycoheterotrophs
that completely rely on the allocation of adequate
nutrients from the fungi for their entire life cycle.
Finally, specialization toward seed dispersal
agents may limit plant distributions as well. This
factor seems to have little impact on mycoheterotrophs, which produce large amounts of
dust seeds that are presumably dispersed by wind
(Leake 1994; Eriksson and Kainulainen 2011).
However, the dust seeds of orchids generally
3
Biogeography and Conservation
disperse only over short distances, and long-distance dispersal seems to be rare (Diez 2007;
Jacquemyn et al. 2007). In Voyria, there is evidence of endozoochory (Hentrich et al. 2010),
and seed dispersal of the rare underground orchid
Rhizanthella gardneri is thought the carried out
by a native mammal that is now extirpated from
all known localities of the orchid (Dixon 1991).
Therefore, limitations to seed dispersal cannot be
ruled out as a determining factor in the distribution of mycoheterotrophic plants.
3.9
Extinct Species
According to the IUCN Red List, a taxon is
extinct when there is no reasonable doubt that the
last individual has died. A taxon is presumed
extinct when exhaustive surveys in known and/or
expected habitat, at appropriate times (diurnal,
seasonal, annual), throughout its historical range
have failed to record an individual (IUCN 2010).
Since many mycoheterotrophic species, particularly those occurring in tropical rainforests, grow
in inaccessible areas and are extremely difficult
to spot (see above), it is impossible to declare any
mycoheterotrophic species as extinct with
confidence. Even when the type locality is
destroyed and a species has not been seen for
many decades, it is still possible that other populations escaped discovery. Sometimes species
have been rediscovered after a notably long hiatus. Haplothismia exannulata (Thismiaceae) was
rediscovered at its type locality in India in 2000,
49 years after its discovery and only a few years
after being declared “extinct” (Sasidharan and
Sujanapal 2000). The second collection of
Thismia clavigera (Thismiaceae) was made 115
years after the first and over 1,000 km from the
type locality (Stone 1980).
Despite these rediscoveries, many other rare
species have not been collected for a remarkably
long period of time. For some, it remains plausible they have escaped extinction. For example,
Marthella trinitatis (Burmanniaceae) is only
known from Mount Tucuche on Trinidad and was
last collected in 1898 (Maas et al. 1986). But
large patches of undisturbed forests are still
139
present on Mt. Tucuche, retaining the possibility
of a rediscovery of this species (Paul Maas, pers.
comm.). In other cases, however, chances for survival of the species seem grim because the type
locality and surrounding habitat has been
destroyed. One of the most famous, now
destroyed, localities is the “Alto Macahé” near
Nova Friburgo (Rio de Janeiro), which is part of
the coastal rainforest of southeast Brazil. In the
nineteenth century, John Miers and Auguste
Glaziou collected many remarkable mycoheterotrophic plants at this location. As a result,
Alto Macahé is the type locality of Peltophyllum
caudatum (Triuridaceae), Thismia fungiformis,
T. caudata, T. macahensis, T. janeirensis, and
T. glaziovii (Thismiaceae). Of these species, only
Thismia janeirensis and T. glaziovii were later
collected at another location. All other species
have not been recorded since the type collection,
and because 95% of the original Mata Atlântica
rainforest has been replaced by farmland (Prance
et al. 2000; Murray-Smith et al. 2009), little hope
remains that these species escaped extinction
(Maas et al. 1986). A similar fate was suffered by
the endemics of Mount Cameroon, where most of
the forest has been replaced by farmland, thereby
destroying the type localities of Oxygyne triandra, Afrothismia pachyantha, A. winkleri
(Thismiaceae), and Burmannia densiflora
(Burmanniaceae) (Schlechter 1906, 1921). The
latter two species were later found at other nearby
locations, but Oxygyne triandra and Afrothismia
pachyantha have not been collected for more
than 100 years and may be extinct.
Arguably, the most mysterious of all mycoheterotrophic plant discoveries is that of Thismia
americana (Thismiaceae). This tiny plant was
discovered in August 1912 by Norma E. Pfeiffer
in a low prairie near Chicago, Illinois (USA)
(Pfeiffer 1914). Thismia americana was observed
at this locality for several subsequent summers
and was probably last seen in 1916. The type
locality of Thismia americana has been replaced
by an industrial complex, and numerous attempts
to relocate this enigmatic species have been
unsuccessful. Therefore, the species is currently
listed as “possibly extinct” (Lewis 2002). Thismia
species are generally found in the leaf litter of
140
V.S.F.T. Merckx et al.
moist tropical rainforests in South and Central
America, Southeast Asia, and Australasia,
although some species occur in subtropical and
temperate rainforests in Japan, Australia, and
northern New Zealand. While this widespread
distribution indicates that there is considerable
variety in ecological preferences among Thismia
species, the occurrence of a Thismia species in a
prairie in temperate North America, more than
3,500 km from the nearest Thismia site (southern
Costa Rica), is truly remarkable. The average
temperature in the Chicago area lowers to −5°C
during winter, by far the lowest temperature for
any Thismiaceae site. This led Pfeiffer (1914) to
the suggestion that the plant was perennial and
that the underground parts of the plant were able
to hibernate. Based on morphological similarities, it has been suggested that the closest known
relative of T. americana is T. rodwayi from
Australia and New Zealand (Jonker 1938; Maas
et al. 1986; but see Thiele and Jordan 2002),
forming one of the “most anomalous disjunctions
known in flowering plants” (Thorne 1972,
p. 407). Was this Thismia population the result of
a human introduction, a recent long-distance dispersal, or the last remnant of an ancient boreotropical Thismia distribution? Unless the plant is
rediscovered, this mystery will remain unsolved.
Many people assume that the species is still present in the area. The only certainty is that if
T. americana still exists, it is extremely difficult
to find. In a letter to Prof. Warren H. Wagner in
1956, Pfeiffer recalled that it took her 3 h to relocate the plants when she returned to the exact
same spot shortly after her first discovery.
3.10
Distribution of Host Fungi
The distribution of mycoheterotrophic plants is
strongly geographically patterned both on global
and local scales. This may be the result of constraints imposed by the physical environment or
the biogeographic history of the plant lineages
(see above). However, as many mycoheterotrophic
plants show specificity toward narrow lineages of
fungi (see Chaps. 5 and 7), an obvious question
emerges: is the distribution of mycoheterotrophic
plants also limited by the distribution of their
associated fungi?
On a broad geographic scale, a correlation
between the distributions of mycoheterotrophs
and their host fungi seems apparent. Arbuscular
mycorrhizal mycoheterotrophs are almost exclusively found in tropical forests, where the native
trees form arbuscular mycorrhizal associations.
In contrast, ectomycorrhizal mycoheterotrophic
orchids and Ericaceae species are mainly
restricted to temperate forests where ectomycorrhizal associations are predominantly formed by
the native tree species. Forests of Southeast Asia,
with their pronounced diversity of mycoheterotrophic orchids, are dominated by large
trees of the family Dipterocarpaceae which are
known to form associations with ectomycorrhizal
fungi (Lee 1990; Moyersoen 2006). Indeed, species of Aphyllorchis and Cephalanthera mycoheterotrophs have been shown to use
ectomycorrhizal fungi to obtain carbon from
dipterocarps (Roy et al. 2009), and it is likely that
many other mycoheterotrophic orchids from
tropical Asia rely on similar associations.
A few ericaceous mycoheterotrophs do occur
at tropical latitudes: Cheilotheca is restricted to
Southeast Asia, and the distribution of the mostly
temperate Monotropa uniflora reaches as far
south as Colombia (Wallace 1975). However,
tropical ericaceous mycoheterotrophs grow in
pine, beech, and oak forests at high elevations
where the presence of ectomycorrhizal fungi
allows the establishment of these species.
Interestingly, there are several reports of arbuscular mycorrhizal mycoheterotrophs growing in
forests dominated by ectomycorrhizal trees (see
above). In these cases, the arbuscular mycorrhizal
“host” is likely associated with arbuscular mycorrhizal understory plants.
On a finer spatial scale, the relation between
mycoheterotroph and fungus distributions is a
much more complicated issue. Why are some
mycoheterotrophs rare, even when their habitat is
relatively common (e.g., Rhizanthella)? Are these
mycoheterotrophs associated with “rare” fungi,
and is their distribution limited by that of the fungus? In contrast to the obvious distribution limitations of specialized holoparasitic plants imposed
3
Biogeography and Conservation
by their host plant range, the relationship between
the distribution range of mycoheterotrophic
plants and their associated fungi is far less obvious. A major obstacle to assess this question is
our lack of detailed knowledge of the distribution
ranges of fungi. Historically, the assumption that
fungi and other eukaryotic microorganisms have
“global” geographic ranges was widely accepted.
This would imply that the distributions of fungi
are independent of biogeography and if conditions are right, the appropriate fungi will appear
(de Candolle 1820). Similar environments, tropical rainforests, for example, would thus harbor
similar fungi, and the potential distribution of
mycoheterotrophic plants would be constrained
by the physical environment rather than the distribution of their associated fungi. Recently, the
assumption that “every fungus is everywhere”
has been challenged by molecular studies of historical biogeography, ecology, and population
genetics of fungi (Taylor et al. 2006; Lumbsch
et al. 2008; Öpik et al. 2010; Peay et al. 2010a).
These studies show that although some fungi are
capable of long-distance dispersal (Moncalvo
and Buchanan 2008), the actual distributions of
most species reflect the same major dispersal barriers (e.g., oceans and mountains) that drive
vicariance events in other organisms (James et al.
1999; Matheny et al. 2009). Geographic patterning is also evident at a more local scale (Collier
and Bidartondo 2009; Peay et al. 2010b). This
implies that the actual distribution of fungi is not
necessarily equal to the potential distribution and
that mycoheterotrophs that are specialized on
particular fungi may fail to invade new areas
solely because their obligate host fungi are not
present. However, evidence that availability of
fungi poses a real limitation to the distribution
ranges of some mycoheterotrophic plants is not
eminent. One speculative example for this phenomenon may be presented by the Hawaiian
Islands. Despite the presence of seemingly suitable habitats, mycoheterotrophic plants are absent
from the flora of Hawaii. In addition, only three
species of orchids are native to the Hawaiian
Islands, a surprisingly small number for a tropical region (Ziegler 2002). This is remarkable,
because the small dust seeds of orchids seem
141
ideal for long-distance dispersal by air, and both
mycoheterotrophic and green orchids are found
on remote Pacific Islands like Vanuatu, Fiji, and
Samoa. Carlquist (1980) hypothesized that orchid
seeds may not be resistant to freezing temperatures of the upper air layers or that the pollination
requirements of potential colonizing species are
not met. Another possible explanation for the
scarcity of orchids—and the absence of mycoheterotrophic plants in general—in Hawaii may
be the absence of suitable fungi necessary for
their establishment. Similarly, a limited number
of suitable ectomycorrhizal plants may explain
the absence neottioid orchids in the Macaronesian
region (Liebel et al. 2010).
On a smaller geographic scale, there is evidence that the rarity of the full mycoheterotroph
Pterospora andromedea (Ericaceae) in eastern
North America is influenced by the distribution
and rarity of its fungal symbiont. A recent study by
Hazard et al. (2011) showed that P. andromedea
from the east coast of North America consists of a
single haplotype that grows only with a single narrow lineage of Rhizopogon fungi. This fungal lineage appears to be rare in eastern white pine
forests, and this may be a contributing factor to the
rarity of eastern P. andromedea plants. In contrast,
in western North America, five haplotypes of
P. andromedea have been identified, and these
haplotypes show preference for either Rhizopogon
salebrosus or R. arctostaphyli, even when they cooccur (Bidartondo and Bruns 2002). Kjøller and
Bruns (2003) found that these fungus species are
common in the soil spore bank of the Sierra
National Forest in western North America, where
P. andromedea is common as well. Similarly, the
initial mycoheterotroph Caladenia huegelii, a rare
terrestrial orchid from Australia, partners with a
specific Sebacinales fungus, which is ecologically
efficacious only under a highly limited range of
habitat and environmental conditions. Thus, rarity
of this orchid species is potentially caused by a
high degree of mycorrhizal specialization (Swarts
et al. 2010). A similar study on species of Drakaea
orchids from western Australia showed that all
species show high mycorrhizal specificity and germinate only in a particular microhabitat. However,
within this microhabitat, rare and common species
142
exhibit no difference in germination rates, and
both germinate in suitable habitat not currently
occupied. The extreme rarity of some Drakaea
species is therefore attributed to their highly
specific pollination systems rather than their mycorrhizal specificity (Phillips et al. 2011).
A putative case of plant rarity induced by the
rarity of a specific fungal symbiont is the distribution of the western underground orchid
(Rhizanthella gardneri), which is only known
from five sites in Southwest Australia (Bougoure
et al. 2008). Rhizanthella gardneri is found in
Melaleuca uncinata shrublands, in habitats of
low-nutrient availability and high light levels.
However, comparison between Rhizanthella sites
revealed that R. gardneri can tolerate a range of
habitat conditions and may be more widespread
than previously thought, given that there are
extensive areas of Melaleuca thickets with similar habitat characteristics across Southwest
Australia (Bougoure et al. 2008). Underground
orchids are extremely difficult to find, and thus,
additional populations may remain to be discovered. However, Rhizanthella orchids seem to be
linked with Melaleuca uncinata plants by a
specific Ceratobasidium fungus (Bougoure et al.
2009). A possible explanation for the scarcity of
Rhizanthella populations compared to the wide
range of sites that appear to be suitable habitat may
be found in the availability of the required fungus.
Similarly, the rarity of Petrosavia sakuraii in the
understory of Japanese cypress plantations—a
common vegetation type in Japan—may be the
result of a preference of the mycoheterotroph
toward specific and range-restricted fungi
(Yamato et al. 2011).
These observations suggest that mycorrhizal
specificity may play an important role in both the
global and local distribution of mycoheterotrophic
plants, in addition to other biogeographic and
ecological factors. However, it must be noted that
for mycoheterotrophic plants, host specificity
does not necessarily lead to restricted geographic
ranges. The mycoheterotrophic orchid Eulophia
zollingeri has an extremely wide distribution in
tropical and subtropical Asia, yet individuals
from seven populations in Japan, Myanmar, and
Taiwan were found to associate with the same
V.S.F.T. Merckx et al.
narrow lineage of fungi related to Psathyrella
candolleana (Coprinaceae). Based on this observation, the authors conclude that a mycoheterotrophic plant can achieve a wide distribution
even with a high mycorrhizal specificity, so long
as the fungal partner is widely distributed (OguraTsujita and Yukawa 2008).
3.11
Threats
3.11.1 Value of Diversity
Mycoheterotrophic plants do not have a direct
economical value. They are not useful for consumption or for pharmaceutical purposes with
the only exception being Gastrodia elata
(Orchidaceae), used in Chinese traditional medicine (Xu and Guo 2000). Mycoheterotrophs are
not essential ecological components of forest
habitats; however, their presence in forest ecosystems may offer an indirect economical value
through recreational services for humans. While
few people will actually visit forests only to see
mycoheterotrophic plants, most will be intrigued
when they encounter one due to their exceptional
and often mysterious habit. Rare plants hardly
ever reach the status as a “flagship” species, such
as the Galápagos tortoise or the giant panda, but
they certainly add an unusual biological aspect to
an ecosystem that can be appreciated by visitors.
Apart from this value, mycoheterotrophic plants
present a unique model system to study mycorrhizal mutualisms and ecological symbioses in
general. Their inability to fix carbon through
photosynthesis clearly shows the potential of
mycorrhizal fungi to transport carbon, and perhaps other nutrients, between plants. This has led
to the discovery of partial mycoheterotrophic
plants. In addition, mycoheterotrophic plants
offer excellent research opportunities to study the
evolution of multipartite symbioses.
Like all organisms, mycoheterotrophic plants
carry a certain “existence value” (Primack 2008).
Existence value can be defined as the amount that
people are willing to pay to prevent species from
going extinct, habitats from being destroyed, and
genetic variation from being lost (Martín-Lopez
3
Biogeography and Conservation
et al. 2007). As a unique part of their ecosystems
(deciduous forests, rainforests, savannas, etc.),
their presence contributes to the existence value
that is attached to these ecosystems. In addition,
their rarity is sometimes used in favor of protection of specific areas. An example is Kupea martinetugei (Triuridaceae), which is often used to
support conservation efforts for the threatened
rainforest on Mount Kupe in Cameroon (Cheek
et al. 2004; Baird 2006). The genus Kihansia
(Triuridaceae) is one of the endemics of the
Kihansi River Gorge in Tanzania, and its presence draws attention to the necessity of conservation efforts for protection of this severely
threatened habitat (Davis and Mvungi 2004).
Also, the charismatic underground orchids of
Australia are often featured to highlight conservation necessity (Swarts and Dixon 2009). And
Thismia americana still helps to protect native
prairie in the Calumet area near Chicago, USA,
even though it was last seen almost 100 years ago
(Chew 2004).
Lastly, fully mycoheterotrophic plants offer
serious potential for horticulture. “Exceptional”
plants, such as rare orchids and carnivorous plants,
have always generated interest from plant enthusiasts. Indeed, commercial growing of rare or bizarre
plants is a profitable business. If the difficulties of
culturing fully mycoheterotrophic plants can be
overcome, these “ghost plants” will find their way
into the greenhouses of orchid collectors but may
also attract the attention of the average consumer
looking for an extraordinary plant.
3.11.2 Habitat Destruction
The major threat for the existence of mycoheterotrophic plants is habitat destruction. This is
the inevitably result of the expansion of human
populations and human activities. Habitat destruction is the primary cause of the loss of biodiversity in terrestrial ecosystems (Pimm and Raven
2000). It is likely that most of the original habitat
of some tropical mycoheterotrophic species has
already been destroyed. The distribution of many
mycoheterotrophic plants overlaps with the biodiversity “hotspots” assigned by Myers et al.
143
(2000). These areas comprise exceptional concentrations of endemic species and are undergoing exceptional loss of habitat. Particularly
strongly affected are the Philippines and IndoBurma, where less than 5% of the primary vegetation is retained (Myers et al. 2000). For
mycoheterotrophic plants, endemism is particularly
pronounced in the biodiversity hotspots of
Sundaland, the Western Ghats and Sri Lanka,
Madagascar, the Eastern Arc and Coastal Forests
of Tanzania/Kenya, West Africa, and the Atlantic
Forest in Brazil. These areas rank among the
“hottest” hotspots with the highest number of
endemics and the most severe habitat loss (Myers
et al. 2000). The effect of habitat loss on mycoheterotrophic plant diversity is probably best
illustrated by Brazil’s Atlantic Forest, where only
5% of the original vegetation remains (MurraySmith et al. 2009; Fig. 3.14). Several Thismiaceae
and Triuridaceae species are only known from
this biodiversity hotspot. Because most of the
historical localities of these species are now
destroyed, little hope remains for their survival
(Maas et al. 1986; Maas and Rübsamen 1986).
Apart from habitat destruction, habitat fragmentation is an important factor that contributes to
the loss of biodiversity in ecosystems. Habitat fragments are not only isolated from one another by a
highly modified or degraded landscape, but edges
of each fragment experience an altered set of environmental conditions, referred to as “edge effects”
(Primack 2008). It remains unclear how this affects
diversity of mycoheterotrophic plants, but effects
may be profound. It can be assumed that various
edge effects, such as a lower canopy density, lower
relative humidity, and lower soil-moisture content
(Laurance et al. 2002), will have significant
influence on the occurrence of mycoheterotrophic
plants. Their occurrence may be even more
influenced by the availability of their host fungi.
Little is known about the effect of fragmentation,
isolation, and concurrent edge effects on the
belowground diversity. A few studies have shown
that ectomycorrhizal fungal species richness is
significantly reduced on smaller and more isolated habitat fragments in temperate (Peay et al.
2007, 2010b) and tropical forests (Tedersoo et al.
2007). Similar observations have been made for
144
V.S.F.T. Merckx et al.
Fig. 3.14 The original distribution of the Atlantic Forest in Brazil in 1500 ad and its distribution in the 1990s. Adapted
from Morellato and Haddad (2000)
saprotrophic fungi (Penttilä et al. 2006). For ectomycorrhizal fungi, species composition may be
very different at edges (Dickie and Reich 2005).
All these factors may influence host availability
and thus successful establishment for mycoheterotrophic plants. Mycoheterotrophic plants
that are specialized on particular “rare” fungi may
thus be in jeopardy if habitat size proves to be a
strong determinant of fungal richness.
Even without destruction or fragmentation,
ecosystems can suffer from human activities
causing pollution. Pollution that impacts plant
and fungal diversity is commonly caused by pesticides, sewage, fertilizers from agricultural
fields, industrial chemicals and wastes, emissions
from factories and automobiles, and sediment
deposits from eroded hillsides (Relyea 2005).
Pollution can significantly alter plant species
richness, and there is no doubt that its negative
impact will affect mycoheterotrophic plants as
well (Brandle et al. 2001; Stevens et al. 2004).
3.11.3 Global Climate Change
The emission of greenhouse gasses has been
steadily increasing over the past 100 years. There
is convincing scientific evidence that the increased
levels of greenhouse gasses produced by human
activity have affected the world’s climate and
ecosystems already and that these effects will
increase in the future (Primack 2008). Global
surface temperatures have increased by 0.6°C
during the last century and are likely to increase
by 2–4°C by 2100 (Solomon et al. 2007). This
global warming will affect a complete set of climate characteristics, leading to a global climate
change. The effect of global climate change on
3
Biogeography and Conservation
rainforests remains poorly known. Different rainforest regions may experience different effects. It
is expected that there is severe risk of forest
retreat, especially in eastern Amazonia, Central
America, and parts of Africa, but there are also
indications for potential of expansion in other
regions, for example, around the Congo Basin
(Malhi et al. 2009; Zelazowski et al. 2011).
Global climate change may be especially harmful for montane forests and their associated mycoheterotrophs. The vegetation zonation on tropical
mountains is strongly controlled by temperature.
A 3°C warming would result in temperature
zones moving 500 m vertically up the mountain,
permitting lowland plants to migrate upward and
eliminating the species in the highest zones
(Pounds et al. 1999; Foster 2001). In the northern
temperate zone, it is expected that global warming-induced changes in the ratio of extinctions
and colonizations at the northern and southern
boundaries of species ranges will result in northward range shifts for many species. However,
given the current landscape fragmentation of forest habitats and the short time period involved,
colonization will be very difficult for most forest
plant species, and their survival will depend on
their environmental tolerance. Plants with low
environmental tolerance may be replaced by
mobile generalist species invading from the south
(McKinney and Lockwood 1999; Honnay et al.
2002). The fragmented distribution patterns of
many mycoheterotrophic plant species suggests
slow dispersal rates and/or high ecological
specificity. Therefore, we hypothesize that temperate mycoheterotrophic plants are particularly
vulnerable to global climate change. At least for
one mycoheterotrophic species, Hypopitys
monotropa in Europe, the impact of global climate
change has been estimated using species distribution modeling based on projected future climate
(Beatty and Provan 2011b). The results indicate
that climate change will have substantial impact
on the distribution range of the species, with a loss
of southern and central European populations, and
a potential northward expansion. Finally, there is
no doubt that global climate change will affect
diversity on all levels, including diversity of mycorrhizal fungi (Bellgard and Williams 2011).
145
Changes in community structures of mycorrhizal
fungi may have an indirect effect on the occurrence of mycoheterotrophic plants as well.
3.11.4 Disturbance
It is unclear whether (limited) human disturbance,
such as selective logging, is a threat for mycoheterotrophs. It is often noted that mycoheterotrophic species prefer areas that have been
devoid of disturbance in recent history (Cheek
and Williams 1999; Taylor and Roberts 2011).
This seems to suggest that mycoheterotrophic
plants are sensible to disturbance or that recolonization of areas that have been prone to disturbance
is slow. However, little research has been done on
this issue. Bergman et al. (2006) studied the distribution of the mycoheterotrophic orchid
Wullschlaegelia calcarata in a rainforest in Puerto
Rico and concluded that its occurrence is correlated with land use history as the orchid was most
abundant in areas which had been minimally
impacted by human activity. Fensham (1993)
reported that a fully mycoheterotrophic Burmannia
species on Bathurst Island, Australia, prefers
monsoon forest sites that are cleared of leaf litter
by seasonal flooding, but their occurrence is negatively influenced by disturbance by pigs.
However, in Tasmania, Thismia rodwayi often
occurs at sites that have been subject to intensive
and relatively recent forest activities, including
clear-cutting and regeneration burns (Roberts
et al. 2003). Similarly, there are many records of
mycoheterotrophs that have been collected from
secondary forests (Maas and Rübsamen 1986;
Maas and Ruyters 1986; Lok et al. 2009; Cheek
and Vanderburgt 2010; Klooster and Culley 2010;
Pendry 2010). In Japan, the rare mycoheterotroph
Petrosavia sakuraii occurs in Chamaecyparis
obtusa plantations (Yamato et al. 2011). Eulophia
zollingeri is frequently found in the introduced
Calliandra calothyrsus forest in Java (Comber
1990). Therefore, at least some species are able to
withstand moderate disturbance or have the ability to migrate into areas that have been affected
by human activities. A key factor in the recolonization of secondary forests may be the presence
146
V.S.F.T. Merckx et al.
of preferred host fungi, although other factors
such as the presence of specific pollinators, seed
dispersal barriers, or abiotic requirements may be
of importance as well.
Herbivory may also have a negative impact on
reproductive success of mycoheterotrophs
(Klooster and Culley 2009; Taylor and Roberts
2011). Thus, introduction of herbivores into
mycoheterotrophic plant habitats could pose
potential threat for the local distribution of mycoheterotrophs. Finally, rare mycoheterotrophic
plants may suffer from overzealous botanists,
who collect specimens and trample populations
during searches (Taylor and Roberts 2011).
3.11.5 Vulnerable Taxa
Only a dozen of mycoheterotrophic plant species
are featured in the IUCN Red List (2010). Those
that are listed are all categorized as “threatened”
and range from “vulnerable” to “critically endangered.” Unfortunately, this low number illustrates
the incomplete state of the list rather than the
absence of vulnerability of mycoheterotrophic
species. Due to the continuing loss of rainforest
area, it can be assumed that many rainforest
mycoheterotrophs are at risk of extinction. In
particular, species that are known from only a
few localities, close to human settlements or outside protected areas, and species with a very limited distribution ranges and small population
sizes are threatened. More intensive studies on
the occurrence and distribution of mycoheterotrophic plants, particularly in the tropics,
are urgently needed to assess the conservation
status of these species. At the current rate of habitat destruction in the tropics, it is likely that some
mycoheterotrophic plant species become extinct
before they are even discovered.
3.12
Conservation
3.12.1 Habitat Conservation
Protecting populations is the key to preserving
species. The best and most straightforward
strategy to protect mycoheterotrophic plants is to
protect the habitats in which they occur. Large
parks are probably the only way to preserve complete rainforest ecosystems, but smaller rainforest
reserves can also play a valuable role in the protection of rainforest species. Besides legal protection, investments in management are essential to
preserve the biodiversity within protected areas.
3.12.2 Inventory and Monitoring
Our knowledge about the abundance and ecology
of most species of mycoheterotrophs remains
very poor. Only through careful inventories and
observations in the field can the true status of a
species and its habitat be determined. In addition,
because flowering times of mycoheterotrophic
plants can be cryptic, the conservation status of a
species can only be established by studying populations over time. Detailed inventory studies
and long-term ecological monitoring often lead
to the discovery of new populations and new species, stressing the importance of these types of
studies as well as our limited knowledge about
mycoheterotrophic plant distributions (e.g.,
Roberts et al. 2003; Franke 2007; Cheek and
Vanderburgt 2010).
3.12.3 Establishing New Populations
Conservation of rare and endangered species can
be supported by establishing new populations. It
is unclear whether this strategy is applicable to
rare mycoheterotrophic plants. Seed germination
of fully mycoheterotrophic orchids and Ericaceae
has been achieved by burying seed packages near
ectomycorrhizal trees (McKendrick et al. 2000b;
Bidartondo and Bruns 2001; Bidartondo 2005),
showing the possibility of introducing (or reintroducing) mycoheterotrophs into existing suitable habitats. However, given the paucity of
knowledge on ecological requirements of mycoheterotrophs (mycorrhiza, pollinators, etc.), only
crude assessments can be made to ensure a site is
suitable for introduction of a species. Given the
high ecological specificity of many mycoheterotrophic species, establishing new populations may be extremely difficult. Translocation of
3
Biogeography and Conservation
mycoheterotrophic plants from natural populations into new sites either as propagated seeds or
as adult plants is likely to lead to failure due to
the breakage of vital mycorrhizal connections,
but if attempted, one should take care to fully
characterize the existing mycoheterotrophic flora
of the transplant area in order to avoid any negative impacts on existing mycoheterotroph
populations.
3.12.4 Ex Situ Conservation
The best strategy for the conservation of biodiversity is the preservation of existing ecosystems.
However, if the last remaining populations of a
rare and endangered species are too small to
maintain the species, if they are declining despite
conservation efforts, or if the remaining individuals are found outside protected areas, then in
situ—or on-site—preservation may not be effective. It is likely that the only way species in such
circumstances can be prevented from going
extinct is to maintain individuals in artificial conditions under human supervision (Primack 2008).
The worlds’ botanic gardens are a safe house for
many plant species: about 80,000 species of plants
are currently being cultivated (Guerrant et al.
2004), and several of these species are extinct in
the wild. Botanic gardens thus play a key role in
plant conservation, and this aspect should become
even more important in the future. However, due
to the complexity of their mode of life, cultivation
of mycoheterotrophic plants remains problematic
and, in most cases, currently impossible. There
are several reports of successful germination and
subsequent development of mycoheterotrophic
orchids. Umata (1995, 1999) reported successful
in vitro germination and formation of lateral roots
of Erythrorchis altissima. Gastrodia elata and
Epipogium roseum have been in vitro germinated
and grown up to the formation of flowers (Xu and
Mu 1990; Xu and Guo 2000; Yagame et al. 2007).
In these experiments, the orchids germinated and
grew in media that were inoculated with saprotrophic fungi, presumably closely related or identical to those with which the plants grow in nature.
Asymbiotic germination to and cultivation to
flowering stage have been reported for Cymbidium
147
macrorhizon (as Cymbidium nipponicum) and
Didymoplexis pallens (Mizuno et al. 1991; Irawati
2002). Successful long-term cultivation of mycoheterotrophs that are associated with fungi that
are mycorrhizal with surrounding trees has not
been achieved to date. Bruns and Read (2000)
were able to germinate seeds of Sarcodes and
Pterospora (Ericaceae) in vitro with ectomycorrhizal Rhizopogon fungi, which were isolated
from mature plants in nature, but further development of seedlings could not be accomplished.
Adult plants of Thismia rodwayi, Afrothismia
winkleri, and A. foertheriana (Thismiaceae) have
been grown for considerable amounts of time
after transplantation from the field to the laboratory, but it remains unclear whether an effective
tripartite symbiosis (mycoheterotroph–fungus–
autotroph) was achieved under these conditions
(Wood 2010; Franke, pers. comm.; VM pers.
obs.). Establishment of such tripartite symbioses
have been successfully accomplished in microcosm studies linking naturally germinated seedlings of the partial mycoheterotroph Corallorhiza
trifida and seedlings of Betula and Salix trees by
a shared mycorrhizal fungus (McKendrick et al.
2000a). Similar microcosm experiments successfully linked Aneura mirabilis and Betula seedlings by a shared mycorrhizal fungus (Read et al.
2000). Nevertheless, more research is urgently
needed to investigate ex situ cultivation possibilities for mycoheterotrophs.
Ex situ seedling culture and subsequent reintroduction into appropriate habitats have been
successfully achieved for orchids (e.g.,
McKendrick 1995; Yam et al. 2010) and may
similarly be used for conservation purposes of
mycoheterotrophic plants. However, there is a
potential danger to this approach. It is observed
that some orchids are able to germinate and
develop ex situ with a wider range of mycorrhizal
fungi than those found in natural populations
(Masuhara and Katsuya 1994; Perkins and
McGee 1995). Similar observations have been
made for the germination of mycoheterotrophic
Ericaceae (Bruns and Read 2000; Bidartondo
2005). Introducing these plants into natural habitats will also lead to the introduction of an “alien”
fungus with potential ecological harm (Zettler
et al. 2005).
148
3.13
V.S.F.T. Merckx et al.
Conclusions
Mycoheterotrophic plants are found in all forest
biomes of the world and show a pronounced preference for damp habitats with primary forest and
a closed canopy cover. The diversity of mycoheterotrophic flowering plants peaks in the
tropics and is particularly high in Southeast Asia.
Many families, genera, and species of mycoheterotrophic plants have a widespread distribution that covers multiple continents. Evidence
from molecular clock analyses suggests that most
widespread lineages are too young to have
acquired their distribution before the breakup of
Gondwana. While some transoceanic distribution
may be explained by migration over temporary
land bridges, oceanic dispersal probably played
the most important role in the acquisition of
widespread distributions. Due to their minute
habit and ephemeral occurrence, mycoheterotrophic plants are not often found and collected. For many species, the paucity of records
is also the result of extreme rarity and high local
endemism. The rarity of mycoheterotrophic
plants is probably related to particular habitat
preferences. High specificity toward particular
lineages of fungi may significantly limit the dispersal potential of mycoheterotrophs, although
specificity toward other biotic (pollinators, dispersal agents, plant communities) and abiotic
factors (humidity, soil composition) may be
influential as well. The continuous destruction of
their habitats and the increase of global temperatures threaten many species with extinction, and
a few species may already have disappeared. The
protection of their habitats is the best and currently the only way for the effective conservation
of mycoheterotrophic plants.
References
Albert VA, Struwe L (1997) Phylogeny and classification
of Voyria (saprophytic Gentianaceae). Brittonia
49:466–479
Alexander IJ, Lee SS (2005) Mycorrhizas and ecosystem
processes in tropical rain forest: implications for diversity. In: Burslem DFRP, Pinard MA, Hartley SE (eds)
Biotic interactions in the tropics: their role in the
maintenance of species diversity. Cambridge
University Press, New York, pp 165–203
Ali JR, Aitchison JC (2008) Gondwana to Asia: plate tectonics, paleogeography and the biological connectivity of the Indian sub-continent from the Middle
Jurassic through latest Eocene (166–35 Ma). Earth Sci
Rev 88:145–166
Ali JR, Huber M (2010) Mammalian biodiversity on
Madagascar controlled by ocean currents. Nature
463:653–656
Arditti J (1992) Fundamentals of orchid biology. Wiley,
New York
Audley-Charles MG (1983) Reconstruction of eastern
Gondwanaland. Nature 306:48–50
Baird D (2006) Newsletter of the UK Darwin Initiative,
Issue 6. http://darwin.defra.gov.uk/newsletter/DARWIN_
NEWS_6.pdf
Bakshi TS (1959) Ecology and morphology of Pterospora
andromedea. Bot Gaz 120:203–217
Barkman TJ, Simpson BB (2001) Origin of high-elevation
Dendrochilum species (Orchidaceae) endemic to Mount
Kinabalu, Sabah. Malaysia Syst Bot 26:658–669
Barrett CF, Freudenstein JV (2008) Molecular evolution
of rbcL in the mycoheterotrophic coralroot orchids
(Corallorhiza
Gagnebin,
Orchidaceae).
Mol
Phylogenet Evol 47:665–679
Beaman JH, Anderson C (2004) The plants of Mount
Kinabalu. 5: Dicotyledon families Magnoliaceae to
Winteraceae. Natural History Publications (Borneo),
Kota Kinabalu
Beaman JH, Beaman RS (1998) The plants of Mount
Kinabalu: 3 gymnosperms and non-orchid monocotyledons. Natural History Publications (Borneo), Kota
Kinabalu
Beard JS (1990) Temperate forests of the southern hemisphere. Vegetatio 89:7–10
Beatty GE, Provan J (2011a) Phylogeographic analysis of
North American populations of the parasitic herbaceous plant Monotropa hypopitys L. reveals a complex
history of range expansion from multiple late glacial
refugia. J Biogeogr 38:1585–1599
Beatty GE, Provan J (2011b) Comparative phylogeography of two related plant species with overlapping
ranges in Europe, and the potential effects of climate
change on their intraspecific genetic diversity. BMC
Evol Biol 11:29
Beentje HJ, Adams B, Davis SD, Hamilton AC (1994)
Regional overview: Africa. In: Davis SD, Heywood
VH, Hamilton AC (eds) Centres of plant diversity.
IUCN Publication Unit, Cambridge, pp 101–148
Bellgard S, Williams S (2011) Response of mycorrhizal
diversity to current climatic changes. Diversity 3:8–90
Benzing DH, Atwood JT (1984) Orchidaceae: ancestral
habitats and current status in forest canopies. Syst Bot
9:155–1665
Bergman E, Ackerman J, Thompson J, Zimmerman J
(2006) Land-use history affects the distribution of the
saprophytic orchid Wullschlaegelia calcarata in Puerto
Rico’s tabonuco forest. Biotropica 38:492–499
3
Biogeography and Conservation
Bever JD, Richardson SC, Lawrence BM, Holmes J,
Watson M (2009) Preferential allocation to beneficial
symbiont with spatial structure maintains mycorrhizal
mutualism. Ecol Lett 12:13–21
Bidartondo MI (2005) The evolutionary ecology of mycoheterotrophy. New Phytol 167:335–352
Bidartondo MI, Bruns TD (2001) Extreme specificity in
epiparasitic Monotropoideae (Ericaceae): widespread
phylogenetic and geographic structure. Mol Ecol
10:2285–2295
Bidartondo MI, Bruns TD (2002) Fine-level mycorrhizal
specificity in the Monotropoideae (Ericaceae): specificity
for fungal species groups. Mol Ecol 11:557–569
Bidartondo MI, Burghardt B, Gebauer G, Bruns TD, Read
DJ (2004) Changing partners in the dark: isotopic and
molecular evidence of ectomycorrhizal liaisons
between forest orchids and trees. Proc R Soc Lond B
271:1799–1806
Bidartondo MI, Redecker D, Hijri I, Wiemken A, Bruns
TD, DomÌnguez L, Sérsic A, Leake JR, Read DJ
(2002) Epiparasitic plants specialized on arbuscular
mycorrhizal fungi. Nature 419:389–392
Bougoure JJ, Brundrett M, Brown A, Grierson PF (2008)
Habitat characteristics of the rare underground orchid.
Aust J Bot 56:501–511
Bougoure JJ, Ludwig M, Brundrett M, Grierson PF (2009)
Identity and specificity of the fungi forming
mycorrhizas
with
rare,
mycoheterotrophic
Rhizanthella gardneri (Orchidaceae). Mycol Res 113:
1097–1106
Bossuyt F, Meegaskumbura M, Beenaerts N, Gower DJ,
Pethiyagoda R, Roelants K, Mannaert A, Wilkinson
M, Bahir MM, Manamendra-Arachchi K, Ng PKL,
Schneider CJ, Oommen OV, Milinkovitch MC (2004)
Local endemism within the western Ghats-Sri Lanka
biodiversity hotspot. Science 306:479–481
Bossuyt F, Milinkovitch MC (2001) Amphibians as indicators of Early Tertiary “Out-of-India” dispersal of
vertebrates. Science 292:93–95
Brandle M, Amarell U, Auge H, Klotz S, Brandl R (2001)
Plant and insect diversity along a pollution gradient:
understanding species richness across trophic levels.
Biodivers Conserv 10:1497–1511
Bruns TD, Read DJ (2000) In vitro germination of nonphotosynthetic, mycoheterotrophic plants stimulated
by fungi isolated from the adult plants. New Phytol
148:335–342
Cameron DD, Bolin JF (2010) Isotopic evidence of partial
mycoheterotrophy in the Gentianaceae: Bartonia virginica and Obolaria virginica as case studies. Am J
Bot 97:1272–1277
Campbell EO (1968) An investigation of Thismia rodwayii F. Muell and its associated fungus. Trans R Soc
N Z Bot 3:209–219
Carlquist S (1967) The biota of long-distance dispersal. V.
Plant dispersal to the Pacific Islands. Bull Torr Bot
Club 64:129–162
Carlquist S (1980) Hawaii. A natural history, 2nd edn. SB
Printers, Honolulu
149
Chantanaorrapint S (2008) Thismia angustimitra
(Thismiaceae), a new species from Thailand. Blumea
53:524–526
Cheek M (2003a) A new species of Afrothismia
(Burmanniaceae) from Kenya. Kew Bull 58:951–955
Cheek M (2003b) Kupeaeae, a new tribe of Triuridaceae
from Africa. Kew Bull 58:939–949
Cheek M (2006) African saprophytes: new discoveries.
In: Ghanzafar SA, Beentje HJ (eds) Taxonomy and
ecology of African plants, their conservation and sustainable use. Royal Botanic Gardens, Kew, pp
693–697
Cheek M, Cable S (1997) Plant inventory for conservation management: the Kew Earthwatch programme in
Western Cameroon, 1993–1996. In: Doolan S (ed)
African rainforest and the conservation of biodiversity,
Proceedings of the Limbe Conference, 17–24 January
1997. Limbe Botanic Garden, Limbe, Cameroon,
pp 29–38
Cheek M, Ndam N (1996) Saprophytic flowering plants
of Mount Cameroon. In: van der Maesen LJG, van der
Burgt XM, van Medenbach de Rooy JM (eds) The biodiversity of African plants. Kluwer Academic
Publishers, Dordrecht, pp 612–617
Cheek M, Pollard BJ, Darbyshire I, Onana J-M, Wild C
(2004) The plants of Kupe, Mwanenguba and the
Bakossi Mountains, Cameroon: a conservation checklist. Kew Publishing, Kew
Cheek M, Vanderburgt X (2010) Gymnosiphon samoritoureanus (Burmanniaceae) a new species from Guinea,
with new records of other achlorophyllous heteromycotrophs. Kew Bull 65:83–88
Cheek M, Williams S (1999) A review of African saprophytic flowering plants. In: Timberlake J, Kativu S
(eds) African plants: biodiversity, taxonomy. Royal
Botanic Gardens, Kew, pp 39–49
Cheek M, Williams S, Brown A (2008) Gymnosiphon
marieae sp. nov. (Burmanniaceae) from Madagascar, a
species with tepal-mediated stigmatic extension. Nord
J Bot 26:230–234
Cheek M, Williams S, Etuge M (2003) Kupea martinetugei, a new genus and species of Triuridaceae
from western Cameroon. Kew Bull 58:225–228
Chen S, Ma H, Parnell JAN (2008) Polygalaceae. Missouri
Botanical Garden, St. Louis, MO & Harvard University
Herbaria, Cambridge, MA. Published on the Internet
http://www.efloras.org. Accessed June 2011
Chew R (2004) Thismia americana. A mystery that still
haunts—and helps—the Calumet region. Chicago
Wilderness Magazine. Published online http://www.
chicagowildernessmag.org/issues/summer2004/
thismia.html
Clarke HD, Funk VA (2005) Using checklists and collections data to investigate plant diversity: II. An analysis
of five florulas from northeastern South America. Proc
Acad Nat Sci Phil 154:29–37
Collier F, Bidartondo MI (2009) Waiting for fungi: the
ectomycorrhizal invasion of lowland heathlands. J Ecol
97:950–963
150
Comber JB (1990) Orchids of java. Royal Botanic
Gardens, Kew
Cooper A, Lalueza-Fox C, Anderson S, Rambaut A,
Austin J, Ward R (2001) Complete mitochondrial
genome sequences of two extinct moas clarify ratite
evolution. Nature 409:704–707
Copeland HF (1939) The structure of Monotropsis and the
classification of the Monotropoideae. Madroño
5:105–119
Courty P-E, Walder F, Boller T, Ineichen K, Wiemken A,
Rousteau A, Selosse M-A (2011) C and N metabolism
in mycorrhizal networks and mycoheterotrophic plants
of tropical forests: a stable isotope analysis. Plant
Physiol 156:952–961
Cox CB, Moore PD (2010) Biogeography. An ecological
and evolutionary approach, 8th edn. Wiley, Hoboken
Cribb P, Fischer E, Killmann D (2010) A revision of
Gastrodia (Orchidaceae: Epidendroideae, Gastrodieae)
in tropical Africa. Kew Bull 65:315–321
Cribb P, Wilkin P, Clements M (1995) Corsiaceae: a new
family for the Falkland Islands. Kew Bull 50:
171–172
Crum H, Bruce J (1996) A new species of Cryptothallus
from Costa Rica. Bryologist 99:433–438
Daniel DF (2010) Sciaphila ledermannii (Triuridaceae), a
biogeographically significant holosaprophyte newly
reported from Príncipe in the Gulf of Guinea. Proc Cal
Acad Sci 15:617–622
Dauby G, Parmentier I, Stévart T (2007) Afrothismia gabonensis sp. nov. (Burmanniaceae) from Gabon. Nord J
Bot 25:268–271
Davies P, Davies J, Huxley A (1988) Wild orchids of
Britain and Europe. The Hogarth Press, London
Davis CC, Bell CD, Mathews S, Donoghue MJ (2002)
Laurasian migration explains Gondwanan disjunctions: evidence from Malpighiaceae. Proc Natl Acad
Sci USA 99:6833–6837
Davis AP, Mvungi EF (2004) Two new and endangered
species of Coffea (Rubiaceae) from the Eastern Arc
Mountains (Tanzania) and notes on associated conservation issues. Bot J Linn Soc 146:237–245
Davis MB (1983) Quaternary history of deciduous forests
of eastern North America and Europe. Ann Missouri
Bot Gard 70:550–563
de Candolle A (1820) Essai élementaire de géographie
botanique. In: Lomolino MV, Sax DF, Brown JH (eds)
Foundations of biogeography. University of Chicago
Press, Chicago, pp 28–48
de Queiroz A (2005) The resurrection of oceanic dispersal
in historical biogeography. Trends Ecol Evol 20:68–73
Dickie IA, Reich PB (2005) Ectomycorrhizal fungal communities at forest edges. J Ecol 93:244–255
Diez JM (2007) Hierarchical patterns of symbiotic orchid
germination linked to adult proximity and environmental gradients. J Ecol 95:159–170
Dixon KW (1991) Seeder/clonal concepts in Western
Australian orchids. In: Wells TCE, Willems JH (eds)
Population ecology of terrestrial orchids. SPB
Academic Publishing, The Hague, pp 111–124
V.S.F.T. Merckx et al.
Dixon KW (2003) Rhizanthella gardneri. Orchidaceae.
Curtis’s Bot Mag 20:94–100
Donoghue MJ, Bell CD, Li J (2001) Phylogenetic patterns
in northern hemisphere plant geography. Int J Plant
Sci 162:S41–S52
Donoghue M, Smith S (2004) Patterns in the assembly of
temperate forests around the Northern Hemisphere.
Philos Trans R Soc Lond B 359:1633–1644
Dressler RL (1981) The orchids. Harvard University
Press, London
Eckenwalder JE (2009) Conifers of the world. Timber
Press, Portland
Eeley HAC, Lawes MJ, Piper SE (1999) The influence of
climate change on the distribution of indigenous forest
in KwaZulu-Natal, South Africa. J Biogeogr
26:595–617
Ek RC, ter Steege H (1997) The flora of the Mabura Hill
area, Guyana. In: Ek RC (ed) Botanical diversity in the
tropical rainforest of Guyana. Tropenbos-Guyana
Series. Koeltz Scientific Books, Koenigstein, pp 1–85
Engler HGA (1888) Burmanniaceae. In: Engler HGA,
Prantl K (eds) Die Natürlichen Pflanzenfamilien, 1st
edn. W. Engelmann, Leipzig, pp 44–51
Eriksson O, Kainulainen K (2011) The evolutionary ecology of dust seeds. Perspect Plant Ecol Evol Syst 13:
73–87
Feild TS, Brodribb TJ (2005) A unique mode of parasitism in the conifer coral tree Parasitaxus ustus
(Podocarpaceae). Plant Cell Environ 28:1316–1325
Fensham RJ (1993) The impact on pig rooting on populations of Burmannia sp., a rare rainforest herb on
Bathurst Island. Proc Roy Soc Queensland 103:5–12
Fontenla S, Godoy R, Rosso P, Havrylenko M (1998)
Root associations in Austrocedrus forests and seasonal
dynamics of arbuscular mycorrhizas. Mycorrhiza 8:
29–33
Fosberg F, Sachet M (1980) A new Sciaphila (Triuridaceae)
from the Palau Islands. Pac Sci 34:25–26
Foster P (2001) The potential negative impacts of global
climatic change on tropical montane cloud forests.
Earth Sci Rev 55:73–106
Franke T (2002) The myco-heterotrophic Voyria flavescens
(Gentianaceae) and its associated fungus. Mycol Prog
1:367–376
Franke T (2004) Afrothismia saingei (Burmanniaceae,
Thismieae), a new myco-heterotrophic plant from
Cameroon. Syst Geogr Pl 74:27–33
Franke T (2007) Miscellaneous contributions to the taxonomy and mycorrhiza of AMF- exploiting mycoheterotrophic plants. PhD. thesis. München: Fakultät
für Biologie der Ludwig-Maximilians-Universität
Franke T, Sainge MN, Agerer R (2004) A new species of
Afrothismia (Burmanniaceae; tribe: Thismieae) from
the western foothills of Mount Cameroon. Blumea
49:451–456
Freudenstein JV, Senyo DM (2008) Relationships and
evolution of matK in a group of leafless orchids
(Corallorhiza and Corallorhizinae; Orchidaceae:
Epidendroideae). Am J Bot 94:498–505
3
Biogeography and Conservation
Furness CA, Rudall P, Eastman A (2002) Contribution of
pollen and tapetal characters to the systematics of
Triuridaceae. Plant Syst Evol 235:209–218
Gandolfo MA, Nixon KC, Crepet WL (2002) Triuridaceae
fossil flowers from the Upper Cretaceous of New
Jersey. Am J Bot 89:1940–1957
Gandolfo MA, Nixon KC, Crepet WL, Sevenson DW
(1998) Oldest known fossils of monocotyledons.
Nature 394:532–533
Gebauer G, Meyer M (2003) 15N and 13C natural abundance of autotrophic and myco- heterotrophic orchids
provides insight into nitrogen and carbon gain from
fungal association. New Phytol 160:209–223
George AS (1980) Rhizanthella gardneri R. S. Rogers the
underground orchid of Western Australia. Am Orchid
Soc Bull 49:631–646
Givnish TJ, Millam KC, Evans TM, Hall JC, Pires JC,
Berry PE, Sytsma KJ (2004) Ancient vicariance or
recent long-distance dispersal? Inferences about phylogeny and South American-African disjunctions in
Rapateaceae and Bromeliaceae based on ndhF
sequence data. Int J Plant Sci 165:S35–S54
Goldblatt P, Manning JC (2010) Geosiris albiflora
(Geosiridoideae), a new species from the Comoro
Archipelago. Bothalia 40:169–171
Good R (1974) The geography of flowering plants, 4th
edn. Longman, London
Govaerts R, Pfahl J, Campacci MA, Holland Baptista D,
Tigges H, Shaw J, Cribb P, George A, Kreuz K, Wood
J (2011) World Checklist of Orchidaceae. The Board
of Trustees of the Royal Botanic Gardens, Kew.
Published on the Internet; http://www.kew.org/wcsp/.
Accessed 26 May 2011
Graham R (1953) Epipogium aphyllum Sw. in
Buckinghamshire. Watsonia 3:33
Guerrant EO, Havens K, Maunder M (2004) Ex situ conservation of species survival in the wild. Island Press,
Washington, DC
Groenendijk JP, van Dulmen ATJ, Bouman F (1997) The
“forest fl oor” saprophytes Voyria spruceana and
V. aphylla (Gentianaceae) growing as epiphytes in
Colombian Amazonia. Ecotropica 3:129–131
Hall R (1998) The plate tectonics of Cenozoic SE Asia
and the distribution of land and sea. In: Hall R,
Holloway JD (eds) Biogeography and geological
evolution of SE Asia. Backhuys Publishers, Leiden,
pp 99–131
Harper JL (1981) The meaning of rarity. In: Synge H (ed)
The biological aspects of rare plant conservation.
Wiley, New York, pp 189–203
Hazard C, Lilleskov EA, Horton TR (2011) Is rarity of
pinedrops (Pterospora andromedea) in eastern North
America lined to rarity of its unique fungal symbiont?
Mycorrhiza 22:393–402
Heads M (2009) Inferring biogeographic history from
molecular phylogenies. Biol J Linn Soc 98:757–774
Heaney LR, Regalado JG (1998) Vanishing treasures of
the Philippine rain forest. University of Chicago Press,
Chicago
151
Hentrich H, Kaiser R, Gottsberger G (2010) The reproductive biology of Voyria (Gentianaceae) species in
French Guiana. Taxon 59:867–880
Herzer RH, Chaproniere GCH, Edwards AR, Hollis CJ,
Pelletier B, Raine JI, Scott GH, Stag-Poole V, Strong
CP, Symonds P, Wilson GJ, Zhu H (1997) Seismic
stratigraphy and structural history of the Reinga Basin
and its margins, southern Norfolk Ridge system. New
Zeal J Geol Geophys 40:425–451
Hill R (2004) Origins of the southeastern Australian vegetation. Philos Trans R Soc B 359:1537–1549
Hofer U, Bersier LF, Bocard D (2000) Ecotones and gradient as determinants of herpetofaunal community
structure in the primary forest of Mount Kupe.
Cameroon J Trop Ecol 16:517–533
Honnay O, Verheyen K, Butaye J, Jacquemyn H, Bossuyt
B, Hermy M (2002) Possible effects of habitat fragmentation and climate change on the range of forest
species. Ecol Lett 5:525–530
Hoorn C, Wesselingh F, ter Steege H, Bermudez M, Mora
A, Sevink J, Sanmartin I, Sanchez-Meseguer A,
Anderson C, Figueiredo J, Jamaerillo C, Riff D,
Negri F, Hooghiemstra H, Lundberg J, Stadler T,
Särkinen T, Antonelli A (2010) Amazonia through
time: Andean uplift, climate change, landscape
evolution, and biodiversity. Science 330:927–931
Ibisch PL, Neinhuis C, Rojas NP (1996) On the biology,
biogeography, and taxonomy of Arachnitis Phil nom.
cons. (Corsiaceae) in respect to a new record from
Bolivia. Willdenowia 26:321–332
Irawati HJ (2002) Seed germination of the mycotrophic
orchid, Didymoplexis pallens. In Proceedings of the
17th World Orchid Conference. Natural History
Publications, Kota Kinabalu, p 299–301
Iriondo M, Latrubesse EM (1994) A probable scenario for
a dry climate in Central Amazonia during the Late
Quaternary. Quat Int 21:121–128
IUCN (2010) IUCN Red List of Threatened Species.
Version
2010.3.
http://www.iucnredlist.org.
Downloaded on 02 Sep 2010
Jacquemyn H, Brys R, Vandepitte K, Honnay O, RoldánRuiz I, Wiegand T (2007) A spatially explicit analysis
of seedling recruitment in the terrestrial orchid Orchis
purpurea. New Phytol 176:448–459
Jaffré T (1992) Floristic and ecological diversity of the
vegetation on ultramafic rocks in New Caledonia. In:
Baker AJM, Proctor J, Reeves RD (eds) The vegetation of ultramafic (serpentine) soils. Intercept Ltd,
Andover, pp 101–107
Jaffré T, Bouchet P, Veillon J-M (1998) Threatened plants
of New Caledonia: is the system of protected areas
adequate? Biodivers Conserv 7:109–135
James TY, Porter D, Hamrick JL, Vilgalys R (1999)
Evidence for limited intercontinental gene flow in the
cosmopolitan mushroom, Schizophyllum commune.
Evolution 53:1665–1677
Jarvie JK (1996) Thismia lauriana (Burmanniaceae), a
new species from Central Kalimantan. Blumea
41:257–259
152
Jonker FP (1938) A monograph of the Burmanniaceae.
Meeded Bot Mus Herb Rijks Univ Utrecht 51:1–279
Kennedy AH, Watson LE (2010) Species delimitations
and phylogenetic relationships within the fully mycoheterotrophic Hexalectris (Orchidaceae). Syst Bot
35:64–76
Kjøller R, Bruns TD (2003) Rhizopogon spore bank communities within and among California pine forests.
Mycologia 95:603–616
Klooster M, Culley T (2009) Comparative analysis of the
reproductive ecology of Monotropa and Monotropsis:
two mycoheterotrophic genera in the Monotropoideae.
Am J Bot 96:1337–1347
Klooster M, Culley T (2010) Population genetic structure
of the mycoheterotroph Monotropa hypopitys L.
(Ericaceae) and differentiation between red and yellow color forms. Int J Plant Sci 171:167–174
Kroenke LW, Rodda P (1984) Cenozoic tectonic development of the Southwest Pacific. United Nations Economic
and Social Commission, Committee for Co-ordination
of Joint Prospecting for Mineral Resources in South
Pacific Offshore Areas (CCOP/SOPAC)
Kruckeberg AR, Rabinowitz D (1985) Biological aspects
of endemism in higher-plants. Annu Rev Ecol Syst
16:447–479
Laurance WF, Lovejoy TE, Vasconcelos HL, Bruna EM,
Didham RK, Stouffer PC, Gascon C, Bierregaard RO,
Laurance SG, Sampaio E (2002) Ecosystem decay of
Amazonian forest fragments: a 22-year investigation.
Conserv Biol 16:605–618
Leake JR (1994) The biology of myco-heterotrophic
(‘saprophytic’) plants. New Phytol 127:171–216
Lee SS (1990) The mycorrhizal association of the
Dipterocarpaceae in the tropical rain forests of
Malaysia. Ambio 19:383–385
Lewis DQ (2002) Burmanniaceae Blume—Burmannia
family. In: Argus GW, Gandhi K, Goldblatt P, Hess
WJ, Kiger RW, Strother JL, Utech FH, Zarucchi JL
(eds) Flora of North America, vol. 26: Magnoliophyta:
Liliidae: Liliales and Orchidales. Oxford University
Press, New York, pp 486–489
Liebel HT, Bidartondo MI, Preiss K, Segreto R, Stöckel
M, Rodda M, Gebauer G (2010) C and N stable isotope signatures reveal constraints to nutritional modes
in orchids from the Mediterranean and Macaronesia.
Am J Bot 97:903–912
Linder HP (2001) Plant diversity and endemism in subSaharan tropical Africa. J Biogeogr 28:169–182
Linder HP, Kurzweil H (1999) Orchids of southern Africa.
Balkema, Rotterdam
Linder HP, Kurzweil H, Johnson DD (2005) The Southern
African orchid flora: composition, sources and endemism. J Biogeogr 32:29–47
Lok AFSL, Ang WF, Tan HTW (2009) The status of
Gastrodia javanica (Bl.) Lindl. in Singapore. Nat Sing
2:415–419
Luer CA (1975) The native orchids of the United States
and Canada excluding Florida. New York Botanical
Garden, New York
V.S.F.T. Merckx et al.
Lumbsch HT, Buchanan PK, May TW, Mueller GM
(2008) Phylogeography and biogeography of fungi.
Mycol Res 112:423–424
Maas H, Maas PJM (2005) Flora da Reserva Ducke,
Amazonas, Brasil: Burmanniaceae. Rodriguésia 56:
125–130
Maas PJM, Maas-van de Kamer H, van Benthem J,
Snelders HCM, Rübsamen T (1986) Burmanniaceae.
Fl Neotrop 42:1–189
Maas PJM, Rübsamen T (1986) Triuridaceae. Fl Neotrop
40:1–55
Maas PJM, Ruyters P (1986) Voyria and Voyriella (saprophytic Gentianaceae). Fl Neotrop 41:1–93
Macey JR, Schulte JA II, Larson A, Ananjeva NB, Wang
Y, Pethiyagoda R, Rastegar-Pouyani N, Papenfuss TJ
(2000) Evaluating trans-Tethys migration: an example
using acrodont lizard phylogenetics. Syst Biol
49:233–256
Malhi Y, Aragao LEOC, Galbraith D, Huntingford C,
Fisher R, Zelazowski P, Sitch S, McSweeney C,
Meir P (2009) Exploring the likelihood and mechanism of a climate-change-induced dieback of the
Amazon rainforest. Proc Natl Acad Sci USA 106:
20610–20615
Malme GOA (1896) Die Burmannien der ersten
Regnel’schen Expedition. Bih Kongl Svenska Vetensk
Akad Handl 22:1–32
Martín-Lopez B, Montes C, Benayas J (2007) The noneconomic motives behind the willingness to pay for
biodiversity conservation. Biol Conserv 139:67–82
Martos F, Dulormne M, Pailler T, Bonfante P, Faccio A,
Fournel J, Dubois M-P, Selosse M-A (2009)
Independent recruitment of saprotrophic fungi as mycorrhizal partners by tropical achlorophyllous orchids.
New Phytol 184:668–681
Masuhara G, Katsuya K (1994) In situ and in vitro
specificity between Rhizoctonia spp. and Spiranthes
sinensis (Persoon.) Ames. var. amoena (M. Beiberstein)
Hara (Orchidaceae). New Phytol 127:711–718
Matheny PB, Aime MC, Bougher NL, Buyck B, Desjardin
DE, Horak E, Kropp BR, Lodge DJ, Soytong K,
Trappe JM, Hibbett DS (2009) Out of the palaeotropics? Historical biogeography and diversification of the
cosmopolitan ectomycorrhizal mushroom family
Inocybaceae. J Biogeogr 36:577–592
McCall RA (1997) Implications of recent geological
investigations of the Mozambique Channel for the
mammalian colonization of Madagascar. Proc R Soc
Lond B 264:663–665
McKendrick SL (1995) The effects of herbivory and vegetation on laboratory-raised Dactylorhiza praetermissa (Orchidaceae) planted into grassland in southern
England. Biol Conserv 73:215–220
McKendrick SL, Leake JR, Read DJ (2000a) Symbiotic
germination and development of myco-heterotrophic
plants in nature: transfer of carbon from ecto-mycorrhizal Salix repens and Betula pendula to the orchid
Corallorhiza trifida through shared hyphal connections. New Phytol 145:539–548
3
Biogeography and Conservation
McKendrick SL, Leake JR, Taylor DL, Read DJ (2000b)
Symbiotic germination and development of mycoheterotrophic plants in nature: ontogeny of Corallorhiza
trifida and characterization of its mycorrhizal fungi.
New Phytol 145:523–537
McKinney ML, Lockwood JL (1999) Biotic homogenization: a few winners replacing many losers in the next
mass extinction. Trends Ecol Evol 14:450–453
Merckx V, Bidartondo MI (2008) Breakdown and delayed
cospeciation in the arbuscular mycorrhizal mutualism.
Proc R Soc Lond B 275:1029–1035
Merckx V, Chatrou LW, Lemaire B, Sainge MN, Huysmans
S, Smets EF (2008) Diversi fi cation of mycoheterotrophic
angiosperms:
evidence
from
Burmanniaceae. BMC Evol Biol 8:178–194
Merckx V, Huysmans S, Smets E (2010a) Cretaceous origins of myco-heterotrophic lineages in Dioscoreales.
In: Seberg O, Petersen G, Barfod AS, Davis J (eds)
Diversity, phylogeny, and evolution in the monocotyledons. Århus University Press, Århus, pp 39–53
Merckx V, Stöckel M, Fleischmann A, Bruns TD, Gebauer
G (2010b) 15N and 13C natural abundance of two
mycoheterotrophic and a putative partially mycoheterotrophic species associated with arbuscular mycorrhizal fungi. New Phytol 188:590–596
Mesta DK, Hegde HV, Upadhya V, Kholkute SD (2011)
Burmannia championii Thwaites (Dioscoreales:
Burmanniaceae), a new addition to the flora of
Karnataka. J Threat Taxa 3:1465–1468
Milne RI, Abbott RJ (2002) The origin and evolution of
tertiary relict floras. Adv Bot Res 38:281–314
Mittermeier RA, Myers N, Gil PR, Mittermeier CG (1999)
Hotspots: earth’s biologically richest and most endangered terrestrial ecoregions. Cemex, Conservation
International and Agrupacion Sierra Madre, Monterrey
Mizuno N, Hiyama I, Higuchi H (1991) Aseptic culture,
in vitro flowering, and in vitro fruiting of a mycoparasitic orchid, Cymbidium nipponicum. In Proceedings
of NIOC’91. NIOC, Nagoya, p 141–143
Molvray M, Kores PJ, Chase MW (2000) Polyphyly of
mycoheterotrophic orchids and functional influences
on floral and molecular characters. In: Wilson KL,
Morrison DA (eds) Monocots: systematics and evolution. CSIRO, Melbourne, pp 441–447
Moncalvo JM, Buchanan PK (2008) Molecular evidence
for long distance dispersal across the southern hemisphere in the Ganoderma applanatum-australe species complex (Basidiomycota). Mycol Res
112:425–436
Moore LB, Edgar E (1970) Flora of New Zealand. Volume
II. Indigenous Tracheophyta—Monocotyledons except
Graminae. First electronic edition, Landcare Research,
June 2004. Transcr. A.D. Wilton, and I.M.L. Andres.
http://FloraSeries.LandcareResearch.co.nz. Accessed
10 May 2011
Morellato LPC, Haddad CFB (2000) Introduction: the
Brazilian Atlantic Forest. Biotropica 32:786–792
Morley RJ (2000) Origin and evolution of tropical rain
forests. Wiley, New York
153
Moyersoen B (2006) Pakaraimaea dipterocarpacea is
ectomycorrhizal, indicating an ancient Gondwanaland
origin for the ectomycorrhizal habit in Dipterocarpaceae.
New Phytol 172:753–762
Murray-Smith C, Brummit NA, Oliveira-Filho AT,
Bachman S, Moat J, Lughada EM, Lucas EJ (2009)
Plant diversity hotspots in the Atlantic coastal forests
of Brazil. Conserv Biol 23:151–163
Myers N, Mittelmeier RA, Mittelmeier CG, da Fonseca
GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858
NASA Earth Observations (2011) http://neo.sci.gsfc.nasa.
gov/. Accessed May 2011
Neyland R, Hennigan M (2003) A phylogenetic analysis
of large-subunit (26 S) ribosome DNA sequences suggests that the Corsiaceae are polyphyletic. New Zeal J
Bot 41:1–11
Ogura-Tsujita Y, Gebauer G, Hashimoto T, Umata H,
Yukawa T (2009) Evidence for novel and specialised
mycorrhizal parasitism: the orchid Gastrodia confusa
gains carbon from saprotrophic Mycena. Proc R Soc
Lond B 267:761–767
Ogura-Tsujita Y, Yukawa T (2008) High mycorrhizal
specificity in a widespread mycoheterotrophic plant
Eulophia zollingeri (Orchidaceae). Am J Bot
95:93–97
Oliveira AA, Daly DC (1999) Geographic distribution of
tree species occurring in the region of Manaus, Brazil:
implications for regional diversity and conservation.
Biodivers Conserv 8:1245–1259
Oliveira AA, Mori SA (1999) A central Amazonian terra
firme forest. I. High tree species richness on poor soils.
Biodivers Conserv 8:1219–1244
Öpik M, Vanatoa A, Vanatoa E, Moora M, Davison J,
Kalwij JM, Reier U, Zobel M (2010) The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi
(Glomeromycota). New Phytol 188:223–241
Paul VN (1964) Epipogium aphyllum. Reading Nat
16:29–30
Peay KG, Bidartondo MI, Arnold A (2010a) Not every
fungus is everywhere: scaling to the biogeography of
fungal–plant interactions across roots, shoots and ecosystems. New Phytol 185:878–882
Peay KG, Bruns TD, Kennedy PG, Bergemann SE,
Garbelotto M (2007) A strong species-area relationship for eukaryotic soil microbes: island size matters
for ectomycorrhizal fungi. Ecol Lett 10:470–480
Peay KG, Garbelotto M, Bruns TD (2010b) Evidence of
dispersal limitation in soil microorganisms: isolation
reduces species richness on mycorrhizal tree islands.
Ecology 91:3631–3640
Pendry CA (2010) Epirixanthes compressa Pendry, a new
mycoheterotrophic species of Polygalaceae from
Thailand. Thai For Bull 38:184–186
Penttilä R, Lindgren M, Miettinen O, Rita H, Hanski I
(2006) Consequences of forest fragmentation for polyporous fungi at two spatial scales. Oikos 114:
225–240
154
Perkins AJ, McGee PA (1995) Distribution of the orchid
mycorrhizal fungus Rhizoctonia solani, in relation to
its host, Pterostylis acuminata, in the field. Aust J Bot
43:565–575
Petersen G, Seberg O, Davis JI, Goldman DH, Stevenson
DW, Campbell LM, Michelangeli FA, Specht CD,
Chase CW, Fay MF, Pires JC, Freudenstein JV, Hardy
CR, Simmons MP (2006) Mitochondrial data in monocot phylogenetics. In: Columbus JT, Friar EA, Porter
JM, Prince LM, Simpson MG (eds) Monocots: comparative biology and evolution (excluding Poales).
Rancho Santa Ana Botanic Garden, Claremont, pp
52–62
Pfeiffer NE (1914) Morphology of Thismia americana.
Bot Gaz 57:122–135
Phillips RD, Barrett MD, Dixon KW, Hopper SD (2011)
Do mycorrhizal symbioses cause rarity in orchids? J
Ecol 99:858–869
Pimm SL, Raven P (2000) Extinction by numbers. Nature
403:843–845
Plana V (2004) Mechanisms and tempo of evolution in the
African Guineo-Congolian rainforest. Philos Trans R
Soc Lond B 359:1585–1594
Pounds JA, Fogden MPL, Campbell JH (1999) Biological
response to climate change on a tropical mountain.
Nature 398:611–615
Prance GT (1994) A comparison of the efficacy of higher
taxa and species numbers in the assessment of biodiversity in the Neotropics. Philos Trans R Soc Lond B
345:89–99
Prance GT, Beentje H, Dransfield J, Johns R (2000) The
tropical flora remains undercollected. Ann Missouri
Bot Gard 87:67–71
Preiss K, Adam IK, Gebauer G (2010) Irradiance governs
exploitation of fungi: fine-tuning of carbon gain by
two partially mycoheterotrophic orchids. Proc R Soc
Lond B 277:1333–1336
Primack RB (2008) A primer of conservation biology, 4th
edn. Sinauer Associates, Sunderland
Primack RB, Corlett RT (2005) Tropical rainforests: an
ecological and biogeographical comparison. Blackwell
Publishing, Malden
Provan J, Bennett K (2008) Phylogeographic insights into
cryptic glacial refugia. Trends Ecol Evol 23:564–571
Rabinowitz PD, Coffin MF, Falvey D (1983) The separation of Madagascar and Africa. Science 220:67–69
Ramirez SR, Gravendeel B, Singer RB, Marshall CR,
Pierce NE (2007) Dating the origin of the Orchidaceae
from a fossil orchid with its pollinator. Nature
448:1042–1045
Raven PH, Axelrod DI (1974) Angiosperm biogeography
and past continental movements. Ann Missouri Bot
Gard 61:539–673
Read DJ, Duckett JG, Francis R, Ligrone R, Russell A
(2000) Symbiotic fungal associations in ‘lower’ land
plants. Philos Trans R Soc Lond B 355:815–831
Relyea RA (2005) The impact of insecticides and herbicides on the biodiversity and productivity of aquatic
communities. Ecol App 15:618–627
V.S.F.T. Merckx et al.
Renner S (2004) Plant dispersal across the tropical Atlantic
by wind and sea currents. Int J Plant Sci
165:S23–S33
Renner SS (2005) Relaxed molecular clocks for dating
historical plant dispersal events. Trends Plant Sci
10:550–558
Ribeiro JELS, Hopkins MJG, Vicentini A, Sothers CA,
Costa MAS, Brito JM, Souza MAD, Martins LH,
Lohmann LG, Assunção PA, Pereira EC, Silva CF,
Mesquita MR, Procópio LC (1999) Flora da Reserva
Ducke: Guia de identificação das plantas vasculares de
uma floresta de terrafirme na Amazônia Central.
Instituto Nacional de Pesquisas da Amazônia, Manaus
Richards PW (1976) The tropical rain forest. University
Press, Cambridge
Roberts N, Wapstra M, Duncan F, Woolley A, Morley J,
Fitzgerald N (2003) Shedding some light on Thismia
rodwayi F. Muell. (fairy lanterns) in Tasmania: distribution, habitat and conservation status. Pap Proc Roy
Soc Tasmania 137:55–66
Roy M, Whatthana S, Richard F, Vessabutr S, Selosse
M-A (2009) Mycoheterotrophic orchids from Thailand
tropical dipterocarpacean forests associate with a
broad diversity of ectomycorrhizal fungi. BMC Biol
7:51
Rübsamen T (1986) Morphologische, embryologische
und systematische Untersuchungen an Burmanniaceae
und Corsiaceae (Mit Ausblick auf die OrchidaceaeApostasioideae). Diss Bot 902:1–310
Sainge MN, Franke T (2005) A new species of Afrothismia
(Burmanniaceae) from Cameroon. Nordic J Bot
23:299–303
Sainge MN, Franke T, Agerer R (2005) A new species of
Afrothismia (Burmanniaceae, tribe Thismieae) from
Korup National Park, Cameroon. Willdenowia 35:
287–291
Salazar GA, Freudenstein JV (1998) Identity and
typification of Corallorhiza punctata and C. bulbosa
(Orchidaceae). Taxon 47:51–54
Sanmartin I, Ronquist F (2004) Southern hemisphere biogeography inferred by event-based models: plant versus animal patterns. Syst Biol 53:216–243
Sasidharan N, Sujanapal P (2000) Rediscovery of
Haplothismia exannulata Airy Shaw (Burmanniaceae)
from its type locality. Rheedea 10:131–134
Schlechter R (1906) Burmanniacae africanae. Bot Jahrb
Syst 38:137–143
Schlechter R (1921) Die Thismieae. Notizbl Bot Gart
Berlin-Dahlem 8:31–45
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd
edn. Academic, London
Snetselaar KM, Whitney KD (1990) Fungal calcium
oxalate in mycorrhizae of Monotropa uniflora. Can J
Bot 68:533–543
Sodhi NS, Koh LP, Brook BW, Ng PKL (2004) Southeast
Asia biodiversity: an impending disaster. Trends Ecol
Evol 19:654–660
Solomon S, Qin D, Manning M, Chen Z, Marquis M,
Averyt KB, Tignor M, Miller HL (2007) Contribution
3
Biogeography and Conservation
of Working Group I to the Fourth Assessment Report
of the Intergovernmental Panel on Climate Change.
University Press, Cambridge
Stevens CJ, Dise NB, Mountford JO, Gowing DJ (2004)
Impact of nitrogen deposition on species richness of
grasslands. Science 303:1876–1879
Stone B (1980) Rediscovery of Thismia clavigera (Becc.)
F.v.M. (Burmanniaceae). Blumea 26:419–425
Storey M, Mahoney JJ, Saunders AD, Duncan RA, Kelley
SP, Coffin MF (1995) Timing of hot spot-related volcanism and the breakup of Madagascar and India.
Science 267:852–855
Summerhayes VS (1951) Wild orchids of Britain. Collins,
London
Swarts ND, Dixon KW (2009) Terrestrial orchid conservation in the age of extinction. Ann Bot 104:
543–556
Swarts ND, Sinclair EA, Francis A, Dixon KW (2010)
Ecological specialization in mycorrhizal symbiosis
leads to rarity in an endangered orchid. Mol Ecol
19:3226–3242
Taylor DL, Bruns TD (1999) Population, habitat and
genetic correlates of mycorrhizal specialization in the
‘cheating’ orchids Corallorhiza maculata and
C. mertensiana. Mol Ecol 8:1719–1732
Taylor L, Roberts D (2011) Biological flora of the British
Isles: Epipogium aphyllum Sw. J Ecol 99:878–890
Taylor JW, Turner E, Townsend JP, Dettman JR, Jacobson
D (2006) Eukaryotic microbes, species recognition
and the geographic limitation of species: examples
from the kingdom fungi. Philos Trans R Soc Lond B
361:1947–1963
Tedersoo L, Suvi T, Beaver K, Koljalg U (2007)
Ectomycorrhizal fungi of the Seychelles: diversity patterns and host shifts from the native Vateriopsis seychellarum (Dipterocarpaceae) and Intsia bijuga
(Caesalpiniaceae) to the introduced Eucalyptus robusta
(Myrtaceae), but not Pinus caribea (Pinaceae). New
Phytol 175:321–333
ter Steege H, Pitman NC, Phillips OL, Chave J, Sabatier
D, Duque A, Molino JF, Prévost MF, Spichiger R,
Castellanos H, von Hildebrand P, Vásquez R (2006)
Continental-scale patterns of canopy tree composition
and function across Amazonia. Nature 443:444–447
ter Steege H, Amazon Tree Diversity Network, RAINFOR
(Amazon Forest Inventory Network) (2010)
Contributions of current and historical processes to
patterns of tree diversity and composition of the
Amazon. In: Hoorn C, Wesselingh F (eds) Amazonia:
landscape and species evolution. Wiley, Oxford,
p 349–359
ter Steege H, Pitman N, Sabatier D (2003) A spatial model
of tree a-diversity and tree density for the Amazon.
Biodivers Conserv 12:2255–2277
Thiele KR, Jordan P (2002) Thismia clavarioides
(Thismiaceae), a new species of fairy lantern from
New South Wales. Telopea 9:765–771
Thompson JN (2005) The geographic mosaic of coevolution. University of Chicago Press, Chicago
155
Thorne RF (1972) Major disjunctions in the geographic
ranges of seed plants. Quart Rev Biol 47:365–411
Tiffney BH (1985) The Eocene North Atlantic land bridge:
its importance in Tertiary and modern phytogeography
of the Northern Hemisphere. J Arnold Arbor
66:243–273
Tsukaya H, Okada H (2005) Thismia mullerensis
(Burmanniaceae), a new species from Muller Range,
Central Kalimantan. Acta Phytotax Geobot 56:129–133
Umata H (1995) Seed germination of Galeola altissima,
an achlorophyllous orchid, with aphyllophorales fungi.
Mycoscience 36:369–372
Umata H (1999) Germination and growth of Erythrorchis
ochobiensis (Orchidaceae) accelerated by monokaryons and dikaryons of Lenzites betulinus and Trametes
hirsute. Mycoscience 40:367–371
van Balgooy MMJ (1966) Coriaria L. In: van Steenis
CGGJ, van Balgooy MMJ (eds) Pacific plant areas,
vol 2. Rijksherbarium/Hortus Botanicus, Leiden,
pp 122–123
van de Meerendonk JPM (1984) Triuridaceae. Fl Males
Ser 1(10):109–121
van der Pijl L (1934) Die Mykorrhiza von Burmannia und
Epirrhizanthes und die Fortflanzung ihres Endophyten.
Rec Trav Bot Ned 31:701–779
Van Royen P (1972) Sertulum Papuanum 17. Corsiaceae
of New Guinea and surrounding areas. Webbia
27:223–255
Vollesen K (1982) A new species of Seychellaria
(Triuridaceae). Kew Bull 36:733–736
Wallace GD (1975) Studies of the Monotropoideae
(Ericaceae): taxonomy and distribution. Wasmann J
Biol 33:1–88
Wapstra M, French B, Davies N, O’Reilly-Wapstra J,
Peters D (2005) A bright light on the dark forest floor:
observations on fairy lanterns Thismia rodwayi F.
Muell. (Burmanniaceae) in Tasmanian forests.
Tasmanian Nat 127:2–18
Waterman RJ, Bidartondo MI (2008) Deception above,
deception below: linking pollination and mycorrhizal
biology of orchids. J Exp Bot 59:1085–1096
Waterman RJ, Bidartondo MI, Stofberg J, Combs J,
Gebauer G, Savolainen V, Barraclough TG, Pauw A
(2011) The effects of above- and belowground mutualisms on orchid speciation and coexistence. Am Nat
177:E54–E68
Wegener A (1915) Die Entstehung der Kontinente und
Ozeane. Vieweg, Braunschweig
Wen J (1999) Evolution of eastern Asian and eastern
North American disjunct distributions in flowering
plants. Annu Rev Ecol Syst 30:421–455
White LJT (2001) The African rain forest: climate and
vegetation. In: Weber W, White LJT, Vedder A,
Naughton-Trevers L (eds) African rain forest ecology:
an interdisciplinary perspective. Yale University Press,
New Haven, pp 3–29
Whittaker RJ, Araulo MB, Paul J, Ladle RJ, Watson JEM,
Willis KJ (2005) Conservation biogeography: assessment and prospects. Divers Distr 11:3–23
156
Wickett NJ, Goffinet B (2008) Origin and relationships of
the myco-heterotrophic liverwort Cryptothallus mirabilis Malmb. (Metzgeriales, Marchantiophyta). Bot J
Linn Soc 156:1–12
Wilford GE, Brown PJ (1994) Maps of late MesozoicCenozoic Gondwana break-up: some palaeogeographical implications. In: Hill RS (ed) History of the
Australian vegetation: cretaceous to recent. Cambridge
University Press, Cambridge, pp 5–13
Wong KM, Phillipps A (1996) Kinabalu, summit of
Borneo. The Sabah Society, Kota Kinabalu
Wood J (2010) Initial observations of seed and fruit development in Thismia rodwayi (Fairy Lanterns). Tasm
Nat 132:78–80
Wood JJ, Beaman TE, Lamb A, Chew C, Beaman JH
(2011) The orchids of Mount Kinabalu, vol 1. Natural
History Publications, Kota Kinabalu
Woodward CL, Berry PE, Maas-van de Kamer H,
Swing K (2007) Tiputinia foetida, a new mycoheterotrophic genus of Thismiaceae from Amazonian
Ecuador, and a likely case of deceit pollination. Taxon
56:157–162
Xu JT, Guo SX (2000) Retrospect on the research of the
cultivation of Gastrodia elata, a rare traditional
Chinese medicine. Chinese Med J 113:686–692
Xu JT, Mu C (1990) The relation between growth of
Gastrodia elata protocorms and fungi. Acta Bot Sin
32:26–31
Yagame T, Yamato M, Mii M, Suzuki A, Iwase K (2007)
Developmental processes of achlorophyllous orchid,
Epipogium roseum: from seed germination to flowering
under symbiotic cultivation with mycorrhizal fungus.
J Plant Res 120:229–236
Yam T, Chua J, Tay F, Ang P (2010) Conservation of
the native orchids through seedling culture and
reintroduction—a Singapore experience. Bot Rev
76:263–274
Yamato M, Yagame T, Shimomura N, Iwase K,
Takahashi H, Ogura-Tsujita Y, Yukawa T (2011)
Specific arbuscular mycorrhizal fungi associated
V.S.F.T. Merckx et al.
with
non-photosynthetic
Petrosavia
sakuraii
(Petrosaviaceae). Mycorrhiza 21:631–639
Yang SZ, Saunders RMK, Hsu CJ (2002) Thismia taiwanensis sp. nov. (Burmanniaceae tribe Thismieae):
first record of the tribe in China. Syst Bot 27:
485–488
Yoder A, Nowak M (2006) Has vicariance or dispersal
been the predominant biogeographic force in
Madagascar? Only time will tell. Annu Rev Ecol Evol
Syst 37:405–431
Yokoyama J, Koizumi Y, Yokota M, Tsukaya H (2008)
Phylogenetic position of Oxygyne shinzatoi
(Burmanniaceae) inferred from 18S rDNA sequences.
J Plant Res 121:27–32
Yuan Y-M, Wohlhauser S, Möller M, Chassot P, Mansion
G, Grant J, Küpfer P, Klackenberg J (2003) Monophyly
and relationships of the tribe Exaceae (Gentianaceae)
inferred from nuclear ribosomal and chloroplast DNA
sequences. Mol Phylogenet Evol 28:500–517
Zhang D, Saunders RM, Hu C-M (1999) Corsiopsis chinensis gen. et sp. nov. (Corsiaceae): first record of the
family in Asia. Syst Bot 24:311–314
Zhu H (1997) Ecological and biogeographical studies on
the tropical rain forest of south Yunnan, SW China
with a special reference to its relation with rain forests
of tropical Asia. J Biogeogr 24:647–662
Zelazowski P, Mahli Y, Huntingford C, Sitch S, Fisher J
(2011) Changes in the potential distribution of humid
tropical forests on a warmer planet. Philos Trans R
Soc Lond A 369:137–160
Zettler LW, Perlman S, Dennis DJ, Hopkins SF, Poulter
SB (2005) Symbiotic germination of a federally
endangered Hawaiian endemic, Platanthera holochila
(Orchidaceae), using a mycobiont from Florida: a conservation dilemma. Selbyana 26:269–276
Ziegler AC (2002) Hawaiian natural history, ecology, and
evolution. University of Hawaii Press, Honolulu
Zimmer K, Meyer C, Gebauer G (2008) The ectomycorrhizal specialist orchid Corallorhiza trifida is a partial
myco-heterotroph. New Phytol 178:395–400