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Received: 2 April 2009 Returned for revision: 27 May 2009 Accepted: 13 July 2009 Published electronically: 29 September 2009
† Background Most tropical and subtropical plants are biotically pollinated, and insects are the major pollinators.
A small but ecologically and economically important group of plants classified in 28 orders, 67 families and
Key words: Angiosperms, nectar-feeding bats, plant phylogeny, pollen dispersal, pollination modes.
Mystacinidae, which is endemic to New Zealand and contains As described in detail by Freeman (1995) and others,
one genus, Mystacina, that is known to visit terrestrial flowers specialized nectar bats in the two families share a common
(Lord, 1991), as being highly evolved for flower-visiting. set of morphological features. These include an elongated
Insectivory is by far the most common feeding mode in bats rostrum, dentition that is reduced in size and number of
and is undoubtedly the ancestral feeding mode in the order teeth, and a long tongue tipped with hair-like papillae which
Chiroptera (Simmons et al., 2008). The two families that is used to collect nectar rapidly during brief flower visits.
contain nectar-feeding bats (hereafter ‘nectar bats’) include Despite sharing these morphological characteristics, pteropo-
Pteropodidae (Old World flying foxes and their relatives), dids and phyllostomids differ in several important aspects
which occurs throughout tropical and subtropical regions of that affect their interaction with flowers. First, glossophagine
Africa including Madagascar, Asia including Indonesia, bats are significantly smaller than their pteropodid counter-
Australia and Papua New Guinea, and Pacific islands, and parts. Mean glossophagine mass is about 14 g (range 7.5 –
Phyllostomidae (American leaf-nosed bats), which inhabits 30 g) compared with 38 g (range 13.2 – 82.2 g) in pteropodids
tropical and subtropical regions of the Americas. These (Fleming and Muchhala, 2008). Second, the range of rostral
two families occur in different suborders of Chiroptera and tongue lengths (relative to overall size) of phyllostomids
(Yinpterochiroptera and Yangochiroptera for pteropodids and is much greater than that of pteropodids (Muchhala, 2006a;
A E
B F
D H
F I G . 1. Portraits of flower-visiting bats. Approximate body masses are in parentheses. (A) Glossophaga soricina (10 g), a basal glossophagine; (B)
Choeronycteris mexicana (16 g), a derived glossophagine; (C) Artibeus jamaicensis (45 g) and (D) Phyllostomus elongatus (60 g), two opportunistic flower-
visiting phyllostomids; (E) Syconycteris australis (20 g) and (F) Eonycteris spelaea (70 g), two specialized nectarivorous pteropodids; (G) Pteropus poliocepha-
lus (750 g) and (H) Epomophorus gambianus (100 g), two opportunistic flower-visiting pteropodids. Photo credits: Merlin D. Tuttle, Bat Conservation
International.
forests; (2) S increases asymptotically with rainfall with a visitors (compared with more specialized (coarse-grained)
plateau of about five species at annual rainfall levels of flower feeding in hummingbirds. Reflecting this last trend, it
2500 mm or more; (3) S in communities of both bats and hum- is common to find several different species of pollen on flower-
mingbirds changes seasonally as latitudinal and altitudinal visiting phyllostomids when captured at night or when pollen on
migrants move into and away from particular habitats; (4) stigmas is identified (e.g. Heithaus et al., 1975; Muchhala et al.,
species of Glossophaga represent the ‘core’ residents in terms 2009). A similar community-level analysis has not been made
of abundance and year-round presence in lowland communities, for pteropodid nectar bats and their Old World avian counter-
and species of Anoura are ‘core’ residents in montane commu- parts [e.g. sunbirds and honeyeaters; but see Fleming
nities; (5) nectar bats are larger in mass and jaw length in dry and Muchhala (2008) for a global analysis of the evolution
habitats than in wet habitats; and (6) average jaw length in of these vertebrates]. Based on their analysis, Fleming
nectar bat communities is positively correlated with average and Muchhala (2008) advocated a ‘three-world’ view concern-
corolla length of bat-pollinated flowers in that community – ing the evolution of vertebrate pollinators and their food
this implies that these bats are generalist (fine-grained) flower plants – the Neotropics, Africa (including Madagascar) and
1020 Fleming et al. — Evolution of bat pollination
A C
B D
Asia/Australasia – rather than a simple New World/Old World nectarivores and frugivores throughout the tropics are often
dichotomy. This trichotomy is more applicable to nectar- food-limited (T. H. Fleming and W. J. Kress, unpubl. res.).
feeding birds than it is to bats, and we will deal only with a Finally, species richness of bat-pollinated plants within New
New World/Old World comparison in this review. and Old World communities is generally similar, averaging
A particularly important result of the Fleming et al. (2005) 11.9 (range 4 – 33 species) in the New World and 16.8
study and one that was extended to Old World nectarivores as (range 4– 28) in the Old World (Fleming, 2005). The species
well as New and Old World avian and chiropteran frugivores richness values of nectar-feeding birds and their food plants
by Fleming (2005) was the relationship between their species are generally higher than those of bats except for Old World
richness and that of their food plants. In the New World, S flowers in which, on average, bat plants slightly outnumber
of both nectar-feeding and frugivorous bats and birds is posi- bird plants at the community level (Fleming, 2005).
tively correlated with S of their food plants. Although the
intercepts of the regression lines for these relationships dif-
fered (higher in frugivores than in nectarivores), the slopes
of the two regressions were the same (about 0.38) and indi- B AT F LOW E R S A N D T H E B A S I C S O F B AT
cated that for both groups, the ratio of plant species to POL L I N AT I O N
animal species is 3 : 1. That is, it takes an average of three
species of flowers or fruits to support one species of vertebrate Bat flowers
nectarivore or frugivore. Fleming (2005) interpreted this Pollination biologists have long recognized a set of plant
relationship to indicate that resource S controls consumer S characteristics (syndromes) that are associated with different
in New World nectarivores and frugivores. Interestingly, a kinds of pollinators. The classic characteristics of bat-
similar correlation does not appear to exist in communities pollinated flowers (the ‘chiropterophilous syndrome’), as
of Old World bat and bird nectar-feeders and fruit-eaters. In described by Faegri and van der Pijl (1979) and modified by
neither group did the regression coefficient differ from zero, Howe and Westley (1988), include nocturnal anthesis, drab
which implies that consumer diversity is not (or is less coloration (i.e. white or green), musty smell, flowers often
likely to be) limited by flower or fruit resource diversity. located on branches or tree trunks (cauliflory) or suspended
This does not imply, however, that populations of these consu- on long stalks (flagelliflory), and tubular or radially symmetri-
mers are not food-limited. A review of data bearing on this cal flowers, often of the ‘shaving brush’ type, that produce
issue clearly indicates that populations of vertebrate relatively large amounts of hexose-rich nectar. Dobat and
Fleming et al. — Evolution of bat pollination 1021
A B C
G H
F I G . 3. Bat-pollinated flowers, corolla or perianth length (when known), and their pollinators. (A) Agave palmeri (Asparagales: Agavaceae), corolla tube 45–
60 mm, glossophagine bats; (B) Musa acuminata (Zingiberales: Musaceae), perianth 70 mm, opportunistic and specialized pteropodid bats; (C) Heliconia solo-
monensis (Zingiberales: Heliconiaceae), perianth 45– 75 mm, specialized pteropodid bats; (D) Canna liliiflora (Zingiberales: Cannaceae), glossophagine bats; (E)
Vriesia sp. (Poales: Bromeliaceae), glossophagine bats; (F) Psittacanthus acinarius (Santalales: Loranthaceae), corolla 50–75 mm, glossophagine bats; (G)
Calyptrogyne ghiesbreghtiana (Arecales: Arecaceae), rachilla 220 mm, opportunistic phyllostomid bats; (H) Phenakospermum guyannense (Zingiberales:
Strelitziaceae), perianth up to 280 mm, opportunistic phyllostomid bats. Photo credits: T. Fleming (A), W. J. Kress (B– E, G, H), C. Geiselman (F).
1022 Fleming et al. — Evolution of bat pollination
A B C
G H
F I G . 4. Bat-pollinated flowers, their corolla or perianth length (when known), and their pollinators. (A) Carnegiea gigantea (Caryophyllales: Cactaceae), corolla
112 mm, opportunistic and specialized phyllostomid bats; (B) Markhamia stipulata (Lamiales: Bignoniaceae), specialized pteropodid bats; (C) Burmeistera cer-
atocarpa (Asterales: Campanulaceae), corolla 13.2 mm, glossophagine bats; (D) Chelonanthus alatus (Gentianales: Gentianaceae), corolla 30–45 mm, glosso-
phagine bats; (E) Lecythis poiteaui (Ericales: Lecythidaceae), androecium 50 mm, glossophagine bats; (F) Hymenaea courbaril (Fabales: Fabaceae), flower
diameter 25 mm, opportunistic and specialized phyllostomid bats; (G) Ceiba pentandra (Malvales: Malvaceae), flower diameter 25–35 mm, opportunistic
and specialized phyllostomids and pteropodids; (H) Caryocar glabrum (Malpighiales: Caryocaraceae), flower diameter 40 mm, opportunistic and specialized
phyllostomid bats. Photo credits: T. Fleming (A, B), C. Geiselman (D), S. Mori (E –H), N. Muchhala (C).
Fleming et al. — Evolution of bat pollination 1023
Peikert-Holle (1985) profusely illustrate these kinds of flowers, australis, however, are known to consume and digest the con-
a few of which are shown in Figs 3 and 4. tents of pollen grains, and it is likely that other nectar bats also
Knowledge of the characteristics of bat flowers has increased have this ability (Howell, 1974; Law, 1992; Herrera and
substantially since the review by Faegri and van der Pijl (1979), Martı́nez del Rı́o, 1998). In general, chiropterophilous
and we now know that such traits as flower colour are far more flowers produce more nectar than those in any other syndrome,
variable among bat-pollinated flowers than previously thought although the amount varies greatly between species from as
(Figs 3 and 4). It remains true, however, that bat flowers little as 10 mL to as much as 15 mL per flower per night
occupy a distinct subset of multivariate floral morphological (van der Pijl, 1961; Cruden et al., 1983; Winter and von
space compared with flowers pollinated by other kinds of Helversen, 2001). Plants pollinated by hovering glossopha-
animals (Ollerton et al., 2009). Bats, like many other kinds of gines, however, can satisfy their pollinators with smaller
pollinators, can be opportunistic flower visitors and sometimes rewards due to their pollinators’ size and energetic efficiencies
visit flowers that do not conform to the classic ‘bat pollination in flower detection and acquisition (von Helversen, 1993). In
syndrome’ (e.g. bee flowers such as Thunbergia grandiflora, contrast to the large amount produced, most nectar from bat
hummingbird-pollinated flowers such as Calliandra laxa, and flowers is rather dilute with sugar concentrations ranging
hummingbird feeders; Lemke, 1985; T.H. Fleming, pers. from 5 to 29 % (von Helversen, 1993). Both nectar amount
1941, 1956, 1961) (Figs 3 and 4). Both visually orientating and a variety of ways. Because they lack the ability to echolocate,
echolocating bats benefit from this arrangement as it allows most pteropodids roost either gregariously in the foliage of
them easily to find, approach and depart from flowers (von canopy trees or solitarily in understorey vegetation rather
Helversen, 1993). Nocturnal anthesis, the opening of flower than in dark caves. Two exceptions are the specialized nectar
buds in the late afternoon or at night, is the second characteristic. bat Eonycteris spelaea, which roosts in caves in colonies of
The flowers of many bat-pollinated plants open early in the a few dozen to thousands of individuals in Malaysia (Start
evening and are viable for only one night (Faegri and van der and Marshall, 1976), and Notopteris macdonaldi of New
Pijl, 1979). Exceptions include flowers of Passiflora mucronata, Caledonia, the Hebrides and Fiji, which forms small colonies
which do not open until after midnight, and those of in caves. Gregarious bats, including canopy-roosting species of
Burmeistera, which remain open for up to 3 d (Sazima and Pteropus and Eidolon which sometimes live in colonies of
Sazima, 1978; Muchhala, 2006b). Together, flower placement hundreds of thousands of bats, and cave-roosting species
away from foliage and nocturnal anthesis are the unifying fea- such as Eonycteris forage as much as 50 km away from their
tures of the bat pollination syndrome while all other character- day roosts and are potentially long-distance pollen carriers
istics discussed above, which provide cues and incentives to (Gould, 1978; Marshall, 1985). Solitary roosting pteropodids,
entice visitation, vary among bat-pollinated species. such as species of Syconycteris and Macroglossus in
movement among plants. For instance, Dick et al. (2008) families where bat-pollination occurs, it is relatively
reported that pollen moved about 18 km between individuals common. The mean number of bat-pollinated genera per
in the bat-pollinated Ceiba pentandra in Brazilian riverine family (median, 1 s.d.) are: basal angiosperms, 1.0 (1.0, 0);
forest habitat. Among arid-zone columnar cacti, between- monocots, 2.3 (1.0, 2.2); basal eudicots, 8.3 (3.5, 10.5);
population genetic structure, as indicated by Wright’s Fst rosids, 3.9 (1.0, 7.1); and asterids, 3.9 (3.0, 3.4) (Kruskal –
index, is lower in bat-pollinated taxa than in insect-pollinated Wallis ANOVA based on medians, W ¼ 8.99, d.f. ¼ 4, P ¼
taxa, which implies that bat-mediated gene flow is greater than 0.061). Families with the highest number of bat-pollinated
that mediated by insects (Hamrick et al., 2002). Similarly, low genera include Fabaceae (30 genera, rosids), Cactaceae (24,
levels of genetic subdivision occur in Phenakospermum basal eudicots), Malvaceae (25, rosids) and Bignoniaceae
guyannenase (Strelitziaceae), a widespread bat-pollinated (15, asterids). The number of bat-pollinated genera in two of
Amazonian megaherb (Roesel et al., 1996). the three largest groups of angiosperms is correlated with the
number of genera per family. Significant positive correlations
occur in rosids ( y ¼ – 038 þ 0.045x, P , 0.01) and monocots
PH YLO GEN ETI C A ND GEO GR APH ICA L ( y ¼ 1.45 þ 0.035x, P , 0.01), but not in asterids, even after
D I S T R I B U T I O N S OF B AT PO L L I N AT I O N the Asteraceae is removed from the analysis (because of its
from Geiselman et al. (2004 and onwards); the basic list of families and number of Old World bat-pollinated genera and species comes from numerous literature sources available upon request from the
For each family the data include: (1) distribution by major plant lineage and order; (2) geographical distribution; (3) total number of genera and species; (4) number of genera and species pollinated
of 67 families (27 %) with bat-pollinated taxa have representa-
contain bat-pollinated genera and species. Sources of data: major angiosperm lineages from Soltis et al. (2005); the basic list of families and number of New World bat-pollinated genera and species
by NW or OW bats; and (5) total number of bat-pollinated genera and proportion of total genera per family that are bat-pollinated. Also indicated in bold type are families that occur on islands that
tives in both hemispheres. We estimate that bat pollination has
0.240
0.429
0.056
0.132
0.007
0.046
0.077
0.009
0.022
0.146
0.041
0.008
0.015
0.059
0.053
0.078
0.007
evolved independently in about 85 % of these families
authors; total number of genera and species per family from APG II (2002 and onwards); island bat families from Silva Taboada (1979), Mickleburgh et al. (1992), Gannon et al. (2005) and
(Table 3) and is clustered in three families of the Myrtales
(Combretaceae, Lythraceae and Onagraceae), although phyl-
lostomid bats are generally minor pollinators in these families
(Table 1). Overall, pteropodid and phyllostomid bats basically
interact with different orders and families of plants. Rather
16
6
3
1
7
3
4
1
6
5
6
2
1
2
3
8
1
than being constrained at deep phylogenetic levels such as
orders, these interactions have evolved independently many
times in different Old and New World plant lineages.
Within each hemisphere bat-pollinated genera can be further
subdivided into those visited by specialized or opportunistic
13
10
5
0
0
3
0
1
3
1
0
0
0
0
2
1
0
168
nectar-feeding bats. A majority of the 159 genera with bat-
0
0
0
0
2
1
0
100
10
14
20
13
3
4
0
0
8
0
3
7
2
1
2
4
2
360
3500
3200
7173
1700
1175
1625
2460
2740
TOTAL
310
130
385
420
11150
800
18
53
87
13
65
57
229
7
415
660
110
147
236
102
148
Cosmopolitan
Cosmopolitan
Cosmopolitan
Cosmopolitan
Cosmopolitan
Cosmopolitan
Cosmopolitan
and family levels are very ‘coarse’ and should not be inter-
Neotropical
Pantropical
Pantropical
Pantropical
Pantropical
Pantropical
Pantropical
Pantropical
Pantropical
Convolvulaceae
Lecythidaceae
Polemoniaceae
Boraginaceae
Gentianaceae
Apocynaceae
Verbenaceae
Acanthaceae
Loganiaceae
Sapotaceae
Lamiaceae
Amborellaceae
Nymphaeaceae
Austrobaileyales Basal
Ceratophyllaceae Angiosperms
Chloranthaceae
Piperales
Canellales
Magnoliales
Laurales
Acorales
Alismatales
Petrosaviaceae
Dioscoreales Monocots
Pandanales
Liliales
Asparagales
Zingiberales
Commelinales
Arecales
Dasypogonaceae
Poales
Ranunculales
F I G . 5. Cladogram showing the evolutionary relationships of orders of angiosperms and the distribution of families containing bat-pollinated taxa among them.
Five types of bat pollination are highlighted: pollination only by New World phyllostomids, pollination only by Old World pteropodids, pollination by both bat
families, and single species pollinated either by New World or Old World bats. Cladogram based on Soltis et al. (2005).
TA B L E 2. Overall distribution of bat pollination among five major lineages of angiosperms by order and family
Orders Families
No. with bat-pollinated No. of independent origins No. with bat-pollinated No. of independent origins
Lineage Total families (%) Total genera (%)
Also indicated are the estimated number of independent origins of bat pollination within these lineages by order and family. The phylogenetic hypothesis
upon which this summary is based comes from T. H. Fleming and W. J. Kress (unpubl. res.). The number of families recognized in this hypothesis and in
Table 1 differ slightly because it does not include Capparaceae.
Fleming et al. — Evolution of bat pollination 1029
TA B L E 3. Distribution of bat pollination among orders and Pteropodids are widely distributed on islands throughout the
families of angiosperms by bat family with an estimate of the Old World tropics as far east as the Cook Islands in the
number of independent origins within plant families Pacific where they often act as ‘keystone’ pollinators and
seed dispersers (Cox et al., 1991; Rainey et al., 1995;
Pteropodids Phyllostomids Banack, 1998). As expected given their wider distribution
No. of No. of families No. of No. of families
among islands, island-dwelling pteropodids interact as pollina-
Lineage orders (% independent) orders (% independent) tors with a greater number of plant families than phyllosto-
mids. Pteropodids on islands visit flowers in 21 of 41 (53 %)
Basal 2 2 (100) 0 0 Old World bat-pollinated families whereas phyllostomids on
angiosperms islands visit flowers in only eight of 44 (18 %) New World bat-
Monocots 3 8 (63) 4 7 (100) pollinated families (Table 1). Plant families pollinated by
Basal 2 2 (100) 2 3 (100)
eudicots island pteropodids are concentrated in the rosids; those polli-
Rosids 7 19 (90) 8 16 (81) nated by phyllostomids are evenly distributed among mono-
Asterids 3 10 (80) 5 16 (81) cots, rosids and asterids. About 90 % of these families have
Totals 17 41 (83) 19 42 (86) pantropical or cosmopolitan distributions. Families with
TA B L E 4. Higher order plant taxa that are associated primarily with bats for pollination
(B) Families with subfamilies or tribes strongly associated with pollinating bats
Family and subfamily or tribe No. of genera/species in family Estimated age of family
Family characteristics include geographical distribution and number of genera/species. Plant data in columns 1 and 2 come from Mabberly (1997) or APG
II. Data on estimated ages of families come from APG II, Barker et al. (2007) and Ricklefs (2006).
* Bird pollination also occurs in these taxa
Asterisks (*) indicate those examples in which evidence for evolutionary transitions appears to be strong; other examples are currently equivocal pending
species-level phylogenies.
results because of the absence of species-level phylogenies. Lagomarsino, C. D. Specht and W. J. Kress, unpubl. res.).
All three potential ancestral pollination modes (insects, birds Similarly, a hummingbird-pollinated species of Burmeistera
and non-volant mammals) are included in these examples, is derived from a bat-pollinated ancestor (Knox et al., 2008).
and generalizations about evolutionary trends are not yet poss- Evidence that bat pollination can give rise to more generalized
ible. We suspect that bat pollination has evolved most com- pollination systems involving birds and insects as well as bats
monly from insect pollination in the Old World [e.g. in the comes from studies of saguaro cacti (Carnegiea gigantea) in
Fabaceae (Mimosoideae) and Myrtaceae]. Flowers pollinated the Sonoran Desert and Aphelandra acanthus in the Andes
by hawkmoths and beetles also appear to be ancestral to bat of Ecuador (Fleming et al., 2001; Muchhala et al., 2009). In
flowers in certain Old World taxa. Although we judge that both of these examples, reduced abundance of bats compared
five of the 11 New World examples in Table 5 are equivocal with other potential pollinators is thought to have selected
(i.e. the immediate ancestor of bat-pollinated taxa is not for a change in floral characteristics (e.g. diurnal flower pres-
clear), there is strong evidence of the evolution of bat entation) that favoured non-chiropteran pollinators.
flowers from bee, moth and hummingbird flowers in the
other six families. It is likely that bat-pollinated taxa have
evolved frequently from hummingbird-pollinated taxa in G E NER AL D ISC USS IO N AN D CO NCL USI ON S
certain New World families of epiphytes (e.g. Bromeliaceae, Bat pollination is relatively uncommon in angiosperms com-
Gesneriaceae), but strong evidence for this awaits phyloge- pared with bird or insect pollination, and overall, it probably
netic studies, as is the case in the Agavaceae and Cactaceae, represents a novel (sensu ‘new’) type of pollination mode for
in which hummingbird pollination is not likely to be ancestral these plants. Bat-pollinated taxa occur in at least 67 families
to bat pollination. and about 250 genera of angiosperms, mostly in advanced
Although bat pollination is usually considered to be a non- evolutionary lineages, particularly in the Zingiberales in
reversible evolutionary specialization (Tripp and Manos, monocots and in the rosids among eudicots. The near
2008), this is not always true. In one case in the primarily absence of bat pollination in the basal angiosperms (only
neotropical genus Heliconia, closely related paleotropical two species) is striking. This pollination mode involves rela-
species are pollinated by either small pteropodid bats or tively large (compared with most insect pollinators), energeti-
by honeyeaters, but not both (Kress, 1985; Pedersen and cally expensive animals that require substantial energetic
Kress, 1999). Recent DNA-based phylogenetic work suggests rewards per flower or inflorescence for attraction. The daily
that honeyeater-pollinated species are derived from the energy budgets of three species of glossophagine bats, for
bat-pollinated species (Kress and Specht, 2005; L. P. example, are 40– 50 kJ whereas those of insects are orders
1032 Fleming et al. — Evolution of bat pollination
of magnitude smaller (Horner et al., 1998; Winter and von problems associated with heterospecific pollen by placing
Helverson, 2001). Bat pollination occurs at night, and the pollen on different parts of the heads of Anoura bats
characteristics of bat-pollinated flowers usually differ substan- (Muchhala and Potts, 2007; Muchhala, 2008).
tially from those of diurnally pollinated flowers in terms of In addition to carrying large amounts of pollen of multiple
timing of floral anthesis, flower colour and size, and nectar genotypes, bats often move pollen substantial distances
odour and volume. The structure of bat-pollinated flowers, between plants, which increases the size of genetic neighbour-
including methods of flower presentation, often differs sub- hoods and reduces levels of genetic subdivision between plant
stantially from those of their non-bat-pollinated ancestors or populations. Data summarized in Ward et al. (2005), for
sister-species (Faegri and van der Pijl, 1979; Dobat and example, indicate that phyllostomid bats carry pollen substan-
Peikert-Holle, 1985; Endress, 1994). Differences in the floral tially longer distances (up to 18 km) within populations of tro-
morphology and biology of species of Musa that are pollinated pical trees than hummingbirds (but not necessarily longer
either by bats or by birds are especially striking. Musa acumi- distances than some insects). Bats are particularly effective
nata, which is pollinated by the specialized pteropodid pollinators for plants that occur at low densities [e.g. in
Macroglossus sobrinus, has pendant infloresences with dark canopy trees in the Bombacaceae s.s., arid-zone columnar
purple bracts and nocturnal flowers that produce a jelly-like cacti (except in the Tehuacan Valley of Mexico where adult
pollination in Bromeliaceae and many other families in pollination is concentrated in the tropical genera with large,
montane regions in South and Central America and the numer- accessible flowers that produce copious amounts of nectar and
ous shifts from insect to hummingbird pollination in many pollen (i.e. Musa, Ensete, Phenakospermum, Heliconia), all
lineages of plants in the montane west of North America adaptations for visitation by large pollinators. Bat pollination
(Grant, 1994; Kessler and Krömer, 2000; Luteyn, 2002). is rare or absent in the ‘ginger families’ with more restrictive
Furthermore, given that bat-pollinated flowers tend to be floral morphology, reduced stamen numbers and smaller nec-
larger and energetically more expensive than bird flowers, taries (i.e. Zingiberaceae, Costaceae, Marantaceae, and
which reflects the generally larger size of nectar-feeding bats Cannaceae; Kress and Specht, 2005). This same pattern – the
compared with nectar-feeding birds worldwide (Fleming and evolution of bat pollination in large-flowered plant lineages –
Muchhala, 2008), selection is more likely to favour the evol- may also be found in the tropical Bombacaceae s.s.,
ution of bird flowers than bat flowers in most situations favour- Bromeliaceae, Gesneriaceae, Malvaceae and possibly
ing a shift from insect to vertebrate pollination. In support of Bignoniaceae (Table 5).
this, many more angiosperm families contain bird-pollinated Bat pollination occurs in about twice as many genera and
genera and species than bat-pollinated taxa (Fleming and species in the New World than in the Old World, despite the
Muchhala, 2008). In the end, although floral and pollinator fact that pteropodid bats, including specialized nectar-feeders,
large flowers. If this is true, then it should be easier for selec- COD A: W HER E DO WE GO FRO M HER E ?
tion to modify insect-pollinated flowers to attract small hover-
Our knowledge about the occurrence of bat pollination in tro-
ing glossophagines than to attract larger non-hovering
pical and subtropical plants has increased substantially in the
phyllostomids or pteropodids. The presence of small hovering
past few decades but there is still much more to be learned
bats (and birds) in the New World has thus expanded the range
on both sides of this fascinating mutualism. On the bat side,
of possible pollinator niches for neotropical plants. The
we need more studies on the foraging behaviour (foraging
absence of such vertebrate pollinators in the Old World has
routes and food choices) of flower-visiting bats. Do these
probably constrained the range of vertebrate pollination
bats forage in an energetically efficient manner, as predicted
niches in angiosperms there.
by optimal foraging theory? Do they routinely rely on spatial
Finally, we note that while the overall species richness of bat-
memory to locate flowering plants? To what extent do foraging
pollinated plants is relatively modest, the ecological and econ-
decisions made by bats conflict with the reproductive interests
omic importance of these plants is considerable. From an eco-
of plants? As one example, the foraging behaviour of the arid-
logical perspective, bat-pollinated plants are conspicuous
zone phyllostomid Leptonycteris curasoae appears to be ener-
members of various New World habitats, including deserts and
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APPENDIX 1
Glossophaga (5), Hylonycteris (1), Leptonycteris (3),
Lichonycteris (1), Lionycteris (1), Lonchophylla (7),
Monophyllus (2), Musonycteris (1), Phyllonycteris (3),
Number of nectar-feeding bats in two families. Indicated first
Platalina (1) and Scleronycteris (1); Ametrida, Artibeus,
are morphologically specialized genera (number of species in
Carollia, Chiroderma, Glyphonycteris, Micronycteris,
parentheses) in bold type followed by genera of opportunistic
Phyllostomus, Platyrrhinus, Rhinophylla, Sturnira,
flower visitors from which pollen has been collected.
Trinycteris, Uroderma and Vampyressa.
Taxonomy follows Simmons (2005).
APPENDIX 3