Bat pollination is relatively uncommon in angiosperms compared with bird or insect pollination, and overall, it probably represents a novel (sensu
‘new’) type of pollination mode for these plants. Bat-pollinated taxa occur in at least 67 families and about 250 genera of angiosperms, mostly in advanced evolutionary lineages, particularly in the Zingiberales in monocots and in the rosids among eudicots. The near absence of bat pollination in the basal angiosperms (only two species) is striking. This pollination mode involves relatively large (compared with most insect pollinators), energetically expensive animals that require substantial energetic rewards per flower or inflorescence for attraction. The daily energy budgets of three species of glossophagine bats, for example, are 40–50 kJ whereas those of insects are orders of magnitude smaller (Horner et al., 1998
; Winter and von Helverson, 2001
). Bat pollination occurs at night, and the characteristics of bat-pollinated flowers usually differ substantially from those of diurnally pollinated flowers in terms of timing of floral anthesis, flower colour and size, and nectar odour and volume. The structure of bat-pollinated flowers, including methods of flower presentation, often differs substantially from those of their non-bat-pollinated ancestors or sister-species (Faegri and van der Pijl, 1979
; Dobat and Peikert-Holle, 1985
; Endress, 1994
). Differences in the floral morphology and biology of species of Musa
that are pollinated either by bats or by birds are especially striking. Musa acuminata
, which is pollinated by the specialized pteropodid Macroglossus sobrinus
, has pendant infloresences with dark purple bracts and nocturnal flowers that produce a jelly-like nectar containing 22–25 % sugar. In contrast, the diurnal flowers of M. salaccensis
, which are pollinated by sunbirds, occur on erect infloresences with pink–purple bracts and produce relatively dilute nectar of 18–21 % sugar (Itino et al., 1991
What are the evolutionary advantages of bat pollination that have led to the independent evolution of this pollination mode in numerous plant lineages? In what ways does bat pollination differ fundamentally from that of insect or bird pollination? We propose that bats differ from insects and birds in at least two ways that affect their effectiveness as pollinators: (1) they often carry large amounts of pollen on their bodies and deposit a large number of pollen grains on stigmas per flower visit and (2) they routinely carry pollen substantial distances among flowers. Muchhala (2006b)
compared pollen deposition on flowers of nine species of Burmeistera
by glossophagine bats and hummingbirds and found that bats deposited about 22 times more pollen on stigmas, on average, than hummingbirds. Likewise, Molina-Freaner et al. (2003)
reported that the glossophagine bat Leptonycteris curasoae
deposited a few thousand to over 20000 pollen grains per night on stigmas of the columnar cactus Pachycereus pringlei
. Deposition of large numbers of pollen grains per stigma can be advantageous to plants for at least two reasons: (1) it ensures that enough pollen is available per flower to fertilize all ovules and (2) it fosters strong pollen–pollen competition for access to ovules.
In addition to depositing large amounts of pollen on plant stigmas, bats also deposit conspecific pollen grains of several different genotypes (i.e. different potential fathers) on stigmas. In bat-pollinated Pachira quinata
, for instance, the number of pollen fathers in fruits from trees in continuous forest in Costa Rica was 2–3 compared with 1–2 pollen fathers per fruit in trees in forest fragments; levels of biparental inbreeding (i.e. mating between close relatives) were higher in the forest fragment trees than in the continuous forest (Fuchs et al., 2003
). Multiple sires per fruit have also been reported in other neotropical bat-pollinated trees, including Caryocar brasiliense
, Ceiba pentandra
and Hymenaea courbaril
(Collevatti et al., 2001
; Dunphy et al., 2004
; Lobo et al., 2005
). Bats also commonly carry more than one species of pollen on their bodies while foraging (e.g. Heithaus et al., 1975
; von Helversen and Winter, 2003
; Muchhala, 2006b
; Muchhala et al., 2009
) but whether this interferes significantly with pollination is not currently known. Sympatric species of Burmeistera
avoid potential problems associated with heterospecific pollen by placing pollen on different parts of the heads of Anoura
bats (Muchhala and Potts, 2007
; Muchhala, 2008
In addition to carrying large amounts of pollen of multiple genotypes, bats often move pollen substantial distances between plants, which increases the size of genetic neighbourhoods and reduces levels of genetic subdivision between plant populations. Data summarized in Ward et al. (2005)
, for example, indicate that phyllostomid bats carry pollen substantially longer distances (up to 18 km) within populations of tropical trees than hummingbirds (but not necessarily longer distances than some insects). Bats are particularly effective pollinators for plants that occur at low densities [e.g. in canopy trees in the Bombacaceae s.s.
, arid-zone columnar cacti (except in the Tehuacan Valley of Mexico where adult cactus densities can exceed 1000 per ha; Valiente-Baunet et al., 1996
) and agaves, and epiphytes in general (e.g. Tschapka, 2004
)]. Ashton (1998)
noted that in Bornean forests, consistently rare species of canopy trees with large fruit such as certain legumes, Neesia
are pollinated by large, low-fecundity and long-lived animals such as pteropodid bats and Xylocopa
bees. In the genus Durio
, species in subgenus Boscia
are abundant small subcanopy or canopy trees that are pollinated by meliponine bees whereas species in the subgenus Durio
are low-density canopy trees whose flowers are bat-pollinated. Theoretically, chronically low-density, animal-pollinated plants are expected to provide larger energy rewards per flower to attract pollinators than high-density plants (Heinrich and Raven, 1972
). This could pre-adapt some low-density plants for pollination by bats and other long-distance pollinators.
If bats are such good pollinators, why are bat-pollinated flowers not more common among angiosperms? The answer to this question probably involves the costs and benefits of bat pollination to plants relative to those associated with other modes of pollination in addition to phylogenetic constraints such as flower size. Costs involved in bat pollination in terms of resources invested in flowers, inflorescences, nectar and pollen are likely to be substantial. In his survey of nectar production in a Costa Rican dry tropical forest, for example, Opler (1983)
showed that floral biomass and nectar volume of bat-pollinated flowers differed from those of flowers pollinated by hummingbirds, bees and butterflies (but not hawkmoths) by several orders of magnitude. Similarly, Fleming (2002)
reported that among cactus flowers, bat-pollinated species generally produced 8–20 times more calories of nectar per flower than those pollinated by hawkmoths and hummingbirds. These data suggest that bat flowers are energetically expensive, which probably represents a significant constraint to their evolution when energy for flower production is limited.
A second constraint to the evolution of bat flowers is the general phylogenetic conservatism of flower evolution in angiosperms. Insect pollination is ancestral in many families of angiosperms, and pollination by birds or bats is derived. Unless environmental conditions such as low temperatures in mountains reduce the abundance or reliability of insects (Cruden 1972
), selection favouring a shift from insect to vertebrate pollination is not likely to occur. Examples of these kinds of shifts include the preponderance of hummingbird pollination in Bromeliaceae and many other families in montane regions in South and Central America and the numerous shifts from insect to hummingbird pollination in many lineages of plants in the montane west of North America (Grant, 1994
; Kessler and Krömer, 2000
; Luteyn, 2002
). Furthermore, given that bat-pollinated flowers tend to be larger and energetically more expensive than bird flowers, which reflects the generally larger size of nectar-feeding bats compared with nectar-feeding birds worldwide (Fleming and Muchhala, 2008
), selection is more likely to favour the evolution of bird flowers than bat flowers in most situations favouring a shift from insect to vertebrate pollination. In support of this, many more angiosperm families contain bird-pollinated genera and species than bat-pollinated taxa (Fleming and Muchhala, 2008
). In the end, although floral and pollinator conservatism probably prevails in angiosperms, the evolution of pollination systems can also be opportunistic so that many plant families have evolved derived modes of pollination involving vertebrates. Although birds appear to be the vertebrates of choice as pollinators for many plant families, probably because of their abundance, diversity and generally small size, bats clearly offer some advantages as pollinators. As a result, bat pollination has evolved numerous times across angiosperm phylogeny.
Besides its evolutionary implications, long-distance pollination by bats also has important conservation implications. Human disturbance in the tropics and elsewhere often fragments plant populations and increases the distance between conspecifics. Without long-distance pollinators, plants with self-compatible or mixed mating systems are likely to experience higher rates of self-fertilization within habitat fragments than plants in continuous forests. Isolated self-incompatible plants (the most common mating system in tropical plants; Bawa, 1992
) will fare even worse because they require pollen from another plant to set any fruit and seeds at all. Studies of canopy trees in continuous and fragmented forests in Brazil, Costa Rica, Mexico and Puerto Rico provide support for these generalizations (Gribel et al., 1999
; Collevatti et al., 2001
; Fuchs et al., 2003
; Quesada et al., 2003
; Dunphy et al., 2004
). Thus, bat pollination, along with pollination by other kinds of long-distance pollinators, can serve to ‘rescue’ plants from some of the adverse effects of habitat fragmentation.
About 85 % of the cases of bat pollination appear to have evolved independently at the level of angiosperm family. A particularly striking example of this pattern is the occurrence of bat-pollinated flowers in only one hemisphere or the other in many pantropically distributed plant families. An exception to this pattern occurs in the monocot order Zingiberales in which bat pollination is widespread among related families. The common occurrence of bat pollination in the monocots, and especially the Zingiberales, may be due to the concentration of many of these taxa in the tropics, particularly the large succulent and/or arborescent species in which bat pollination almost exclusively occurs. Of the seven families of monocots in which more than a single species is bat-pollinated (Table ), all are exclusively tropical in distribution. In addition, many of these same taxa have large flowers (Strelitziaceae) and/or large floral displays (Agavaceae, Arecaceae, Pandanaceae) in closely related taxa that are bird- or insect-pollinated. In the Zingiberales, bat pollination is concentrated in the tropical genera with large, accessible flowers that produce copious amounts of nectar and pollen (i.e. Musa
), all adaptations for visitation by large pollinators. Bat pollination is rare or absent in the ‘ginger families’ with more restrictive floral morphology, reduced stamen numbers and smaller nectaries (i.e. Zingiberaceae, Costaceae, Marantaceae, and Cannaceae; Kress and Specht, 2005
). This same pattern – the evolution of bat pollination in large-flowered plant lineages – may also be found in the tropical Bombacaceae s.s.
, Bromeliaceae, Gesneriaceae, Malvaceae and possibly Bignoniaceae (Table ).
Bat pollination occurs in about twice as many genera and species in the New World than in the Old World, despite the fact that pteropodid bats, including specialized nectar-feeders, are likely to be significantly older evolutionarily than specialized nectar-feeding phyllostomids. One reason for this is that the neotropical angiosperm flora is much richer in species, genera and families than are the floras of Africa, Asia and Australasia (Whitmore, 1998
; Morley, 2000
). But this explanation only begs the question, why is the neotropical flora richer than those in other tropical areas? Gentry's (1982)
widely cited explanation for this emphasized the importance of Andean orogeny as a generator of exceptional plant species diversity, particularly among understorey shrubs, epiphytes and palmettos of Gondwanan ancestry. Andean-associated families such as Bromeliaceae, Campanulaceae, Cactaceae, Gesneriaceae, Marcgraviaceae and Solanaceae are relatively rich in bat-pollinated genera and/or species. Only bat-pollinated canopy trees in the Bombaceae s.s.
and Fabaceae are not strongly associated with the Andes. Interestingly, whereas hummingbirds have radiated extensively in the Andes (Bleiweiss, 1998a
; McGuire et al., 2007
), the same is not true for glossophagine bats in which species of only 1–2 genera (e.g. Anoura
) occur at mid- to high elevations (Koopman, 1981
). All hummingbirds have the capacity to undergo torpor while glossophagine bats do not (McNab, 2002
; but see Kelm and von Helversen, 2007
). The ability to undergo torpor and to reduce energy demands significantly while still maintaining high body temperatures when active has enabled hummingbirds to radiate extensively under conditions of low ambient temperatures and flowers that offer low energetic rewards in the Andes (Altshuler et al., 2004
). The inability to undergo torpor has probably constrained the radiation of glossophagine bats in montane environments.
Another reason for the higher diversity of bat-pollinated plants in the Neotropics than in the Paleotropics probably reflects the small size and hovering ability of glossophagines. Large, non-hovering pteropodids and their New World counterparts, non-glossophagine phyllostomid bats, often visit large, sturdily built flowers many of which are exserted well away from foliage on erect stalks or long pendants (Figs –). In contrast, small hovering glossophagines often visit small, delicate flowers that may or may not be exserted well away from foliage. The ability to hover has allowed these bats to interact with small flowers produced by a wider range of growth habits, including epiphytes and shrubs that produce small flowers as well as large-flowered canopy trees, than pteropodids (Fleming and Muchhala, 2008
). We assume that it is cheaper for plants to produce small flowers than large flowers. If this is true, then it should be easier for selection to modify insect-pollinated flowers to attract small hovering glossophagines than to attract larger non-hovering phyllostomids or pteropodids. The presence of small hovering bats (and birds) in the New World has thus expanded the range of possible pollinator niches for neotropical plants. The absence of such vertebrate pollinators in the Old World has probably constrained the range of vertebrate pollination niches in angiosperms there.
Finally, we note that while the overall species richness of bat-pollinated plants is relatively modest, the ecological and economic importance of these plants is considerable. From an ecological perspective, bat-pollinated plants are conspicuous members of various New World habitats, including deserts and other arid to semi-arid habitats (e.g. columnar cacti and paniculate agaves) and dry and wet tropical forests (e.g. canopy trees of the Bombacaceae s.s.
). Similarly, members of the Bombacaceae s.s.
are conspicuous members of certain African and Madagascan habitats, and species of Sonneratia
are important members of south-east Asian mangrove communities. From an economic perspective, many of these same taxa or their cultivated relatives have considerable monetary value. For example, fruits of bat-pollinated columnar cacti are widely harvested in many parts of the Americas (Yetman 2007
), and tequila, which is derived from Agave tequilana
, is a major cultural icon and agricultural industry in Mexico. Ceiba pentandra
is an important source of fibre worldwide, and species of neotropical Ochroma
are renowned for their lightweight wood. In south-east Asia, economically important fruits come from bat-pollinated Durio zibethinus
and two species of Parkia
, and bat-pollinated species of Eucalyptus
are important timber trees in Australia (Fujita and Tuttle, 1991
). Although domestic bananas (Musa
species) produce fruit parthenocarpically, their wild relatives are bat-pollinated (and dispersed).
In conclusion, bat pollination has evolved independently in many advanced orders and families of angiosperms. It is particularly common in lowland habitats throughout the tropics but is also common in arid tropical and subtropical habitats in the New World, particularly in the Agavaceae and Cactaceae. As noted above, a number of ecologically or commercially important tropical trees, especially those in the Bombacaceae s.s., as well as many large herbaceous or arborescent plants in the monocot order Zingiberales are bat-pollinated. In the New World tropics, many epiphytes in the Bromeliaceae, Cactaceae and Gesneriaceae rely on bats for pollination. The evolution of bat-pollinated lineages probably began in the Miocene, well after the first appearance of families that currently contain many such lineages. Bat pollination is thus derived in most plant groups, and its evolution has entailed significant changes in the timing of anthesis, morphology, biochemistry and physiology of flowers. We propose that bat pollination has been particularly likely to evolve in plants that occur in chronically low densities and that from a conservation viewpoint it is a particularly valuable adaptation in landscapes in which plant populations have recently become fragmented owing to habitat destruction. The loss of nectar-feeding bats in tropical and subtropical habitats would probably have profound ecological and evolutionary effects on their food plants and on the plant communities in which they occur.