Nectar-feeding bird and bat niches in two worlds: pantropical comparisons of vertebrate pollination systems

Aim We review several aspects of the structure of regional and local assemblages of nectar‐feeding birds and bats and their relationships with food plants to determine the extent to which evolutionary convergence has or has not occurred in the New and Old World tropics. Location Our review is pantropical in extent and also includes the subtropics of South Africa and eastern Australia. Within the tropics, it deals mostly with lowland forest habitats. Methods An extensive literature review was conducted to compile data bases on the regional and local species richness of nectar‐feeding birds and bats, pollinator sizes, morphology, and diets. Coefficients of variation (CVs) were used to quantify the morphospace occupied by the various families of pollinators. The extent to which plants have become evolutionarily specialized for vertebrate pollination was explored using several criteria: number and diversity of growth forms of plant families providing food for all the considered pollinator families; the most common flower morphologies visited by all the considered pollinator families; and the number of plant families that contain genera with both bird‐ and bat‐specialized species. Results Vertebrate pollinator assemblages in the New World tropics differ from those in the Old World in terms of their greater species richness, the greater morphological diversity of their most specialized taxa, and the greater degree of taxonomic and ecological diversity and morphological specialization of their food plants. Within the Old World tropics, Africa contains more specialized nectar‐feeding birds than Asia and Australasia; Old World nectar‐feeding bats are everywhere less specialized than their New World counterparts. Main conclusions We propose that two factors – phylogenetic history and spatio‐temporal predictability (STP) of flower resources – largely account for hemispheric and regional differences in the structure of vertebrate pollinator assemblages. Greater resource diversity and resource STP in the New World have favoured the radiation of small, hovering nectar‐feeding birds and bats into a variety of relatively specialized feeding niches. In contrast, reduced resource diversity and STP in aseasonal parts of Asia as well as in Australasia have favoured the evolution of larger, non‐hovering birds and bats with relatively generalized feeding niches. Tropical Africa more closely resembles the Neotropics than Southeast Asia and Australasia in terms of resource STP and in the niche structure of its nectar‐feeding birds but not its flower‐visiting bats.     

The role of frugivorous bats in tropical forest succession

Discussion of successional change has traditionally focused on plants. The role of animals in producing and responding to successional change has received far less attention. Dispersal of plant propagules by animals is a fundamental part of successional change in the tropics. Here we review the role played by frugivorous bats in successional change in tropical forests. We explore the similarities and differences of this ecological service provided by New and Old World seed-dispersing bats and conclude with a discussion of their current economic and conservation implications. Our review suggests that frugivorous New World phyllostomid bats play a more important role in early plant succession than their Old World pteropodid counterparts. We propose that phyllostomid bats have shared a long evolutionary history with small-seeded early successional shrubs and treelets while pteropodid bats are principally dispersers of the seeds of later successional canopy fruits. When species of figs (Ficus) are involved in the early stages of primary succession (e.g. in the river meander system in Amazonia and on Krakatau, Indonesia), both groups of bats are important contributors of propagules. Because they disperse and sometimes pollinate canopy trees, pteropodid bats have a considerable impact on the economic value of Old World tropical forests; phyllostomid bats appear to make a more modest direct contribution to the economic value of New World tropical forests. Nonetheless, because they critically influence forest regeneration, phyllostomid bats make an important indirect contribution to the economic value of these forests. Overall, fruit-eating bats play important roles in forest regeneration throughout the tropics, making their conservation highly desirable.     

Convergent evolution of sunbird pollination systems of Impatiens species in tropical Africa and hummingbird systems of the New World

The bird pollination systems of the New and Old Worlds evolved independently, and differ in many aspects. New World plants are often presented as those adapted to hovering birds while Old World plants to perching birds. Most Neotropical studies also demonstrate that in hummingbird species rich assemblages, only a small number of highly specialized birds exploits the most specialized plants with long corollas. Nevertheless, recent research on bird–plant pollination interactions suggest that sunbird pollination systems in the Old World have converged more with the highly specialized hummingbird pollination systems than previously thought. In this study we focus on the pollination systems of the bird pollination syndrome Impatiens species on Mt. Cameroon, West Africa. We show that despite the high diversity of sunbirds on Mt. Cameroon, only Cyanomitra oritis appear to be important pollinator of all Impatiens species. This asymmetry indicates the absence of pair wise co‐evolution and points to a diffuse co‐evolutionary process resulting in guilds of highly specialized plants and birds; a situation well known from hummingbirds and specialized plant communities of the New World. Additionally, the herbaceous habits of Impatiens species, the frequent adaptations to pollination by hovering birds, and the habitat preference for understory in tropical forests or epiphytic growth, resemble the highly specialized Neotropical plants. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115 , 127–133.     

Phosphoenolpyruvate Carboxykinase 1 Gene (Pck1) Displays Parallel Evolution between Old World and New World Fruit Bats

Bats are an ideal mammalian group for exploring adaptations to fasting due to their large variety of diets and because fasting is a regular part of their life cycle. Mammals fed on a carbohydrate-rich diet experience a rapid decrease in blood glucose levels during a fast, thus, the development of mechanisms to resist the consequences of regular fasts, experienced on a daily basis, must have been crucial in the evolution of frugivorous bats. Phosphoenolpyruvate carboxykinase 1 (PEPCK1, encoded by the Pck1 gene) is the rate-limiting enzyme in gluconeogenesis and is largely responsible for the maintenance of glucose homeostasis during fasting in fruit-eating bats. To test whether Pck1 has experienced adaptive evolution in frugivorous bats, we obtained Pck1 coding sequence from 20 species of bats, including five Old World fruit bats (OWFBs) (Pteropodidae) and two New World fruit bats (NWFBs) (Phyllostomidae). Our molecular evolutionary analyses of these sequences revealed that Pck1 was under purifying selection in both Old World and New World fruit bats with no evidence of positive selection detected in either ancestral branch leading to fruit bats. Interestingly, however, six specific amino acid substitutions were detected on the ancestral lineage of OWFBs. In addition, we found considerable evidence for parallel evolution, at the amino acid level, between the PEPCK1 sequences of Old World fruit bats and New World fruit bats. Test for parallel evolution showed that four parallel substitutions (Q276R, R503H, I558V and Q593R) were driven by natural selection. Our study provides evidence that Pck1 underwent parallel evolution between Old World and New World fruit bats, two lineages of mammals that feed on a carbohydrate-rich diet and experience regular periods of fasting as part of their life cycle.     

Untangling latitudinal richness gradients at higher taxonomic levels: familial perspectives on the diversity of New World bat communities

Aims (i) To describe at the level of local communities latitudinal gradients in the species richness of different families of New World bats and to explore the generality of such gradients. (ii) To characterize the relative effects of changes in the richness of each family to the richness of entire communities. (iii) To determine differences in the rate and direction of latitudinal gradients in species richness within families. (iv) To evaluate how differences among families regarding latitudinal gradients in species richness influence the latitudinal gradient in species richness of entire communities. Location Continental New World ranging from the northern continental United States (Iowa, 42° N) to eastern Paraguay (Canindeyú, 24° S). Methods Data on the species composition of communities came from 32 intensively sampled sites. Analyses focused on species richness of five of nine New World bat families. Multivariate analysis of variance and discriminant function analysis determined and described differences among temperate, subtropical, and tropical climatic zones regarding the species richness of bat families. Simple linear regression described latitudinal gradients in species richness of families. Path analysis was used to describe: (i) the direct effect of latitude on species richness of communities, (ii) the indirect effects of latitude on the species richness of communities through its effect on the species richness of each family, (iii) the relative effects of latitude on the species richness of bat families, and (iv) the relative contribution of each family to variation in the species richness of communities. Results Highly significant differences among climatic zones existed primarily because of a difference between the temperate zone and the tropical and subtropical zones combined. This difference was associated with the high number of vespertilionids in the temperate zone and the high number of phyllostomids in the tropical and subtropical zones. Latitudinal gradients in species richness were contingent on phylogeny. Although only three of the five families exhibited significant gradients, all families except for the Vespertilionidae exhibited indistinguishable increases in species richness with decreases in latitude. The Emballonuridae, Phyllostomidae and Vespertilionidae exhibited significant latitudinal gradients whereby the former two families exhibited the classical increase in species richness with decreasing latitude and the latter family exhibited the opposite pattern. Variation in species richness of all families contributed significantly to variation in the species richness of entire communities. Nonetheless, the Phyllostomidae made a significantly stronger contribution to changes in species richness of communities than did all other families. Much of the latitudinal gradient in species richness of communities could be accounted for by the effects of latitude on the species richness of constituent families. Main conclusions Ecological and evolutionary differences among higher taxonomic units, particularly those differences involving life‐history traits, predispose taxa to exhibit different patterns of diversity along environmental gradients. This may be particularly true along extensive gradients such as latitude. Nonetheless, species rich taxa, by virtue of their greater absolute rates of change, can dominate and therefore define the pattern of diversity at a higher taxonomic level and eclipse differences among less represented taxa in their response to environmental gradients. This is true not only with respect to how bats drive the latitudinal gradient in species richness for all mammals, but also for how the Phyllostomidae drives the latitudinal gradient for all bats in the New World. Better understanding of the mechanistic basis of latitudinal gradients of diversity may come from comparing and contrasting patterns across lower taxonomic levels of a higher taxon and by identifying key ecological and evolutionary traits that are associated with such differences.     

Roles of Birds and Bats in Early Tropical-Forest Restoration

Restoration of tropical forest depended in large part on seed dispersal by fruit-eating animals that transported seeds into planted forest patches. We tested effectiveness of dispersal agents as revealed by established recruits of tree and shrub species that bore seeds dispersed by birds, bats, or both. We documented restoration of dispersal processes over the first 76 months of experimental restoration in southern Mexico. Mixed-model repeated-measures randomized-block ANOVAs of seedlings recruited into experimental controls and mixed-species plantings from late-secondary and mature forest indicated that bats and birds played different roles in the first years of a restoration process. Bats dispersed pioneer tree and shrub species to slowly regenerating grassy areas, while birds mediated recruitment of later-successional species into planted stands of trees and to a lesser extent into controls. Of species of pioneer trees and shrubs established in plots, seven were primarily dispersed by birds, three by bats and four by both birds and bats. Of later-successional species recruited past the seedling stage, 13 were of species primarily dispersed by birds, and six were of species dispersed by both birds and bats. No later-successional species primarily dispersed by bats established in control or planted plots. Establishment of recruited seedlings was ten-fold higher under cover of planted trees than in grassy controls. Even pre-reproductive trees drew fruit-eating birds and the seeds that they carried from nearby forest, and provided conditions for establishment of shade-tolerant tree species. Overall, after 76 months of cattle exclusion, 94% of the recruited shrubs and trees in experimental plots were of species that we did not plant.     

Relation of fig fruit characteristics to fruit-eating bats in the New and Old World tropics

Abstract. Long-term studies of a Panamanian fig community have revealed that the figs separate into two major groups based on distinct patterns in fruit characteristics including fruit size, colour, scent and synchrony of ripening. Furthermore, these differences can be linked to sensory, morphological and behavioural capabilities of the figs' primary dispersers. One group of figs attracts primarily bats; the other group is visited mainly by birds. Whereas fruits of 'bat' figs span a wide range of size classes, ripen synchronously and remain green(ish) when ripe, all fruits of 'bird' figs have small fruit which ripen asynchronously and turn red when ripe. Among 'bat' figs, fruit size is correlated with body size of the bats that prefer them. Based on the consistent differences between 'bat' and 'bird' fig fruits in Panama we expect similar patterns in Old World figs. Furthermore, since fig-eating bats of the Old World differ in morphology, behaviour and sensory capabilities from fig-eating bats of the New World we speculate that these differences should be reflected in differences in fruit characteristics of Old and New World 'bat' figs. Personal observations and literature reports of Old World bats and figs are consistent with our predictions.     

Latitudinal gradients of species richness: a test of the geographic area hypothesis at two ecological scales

The geographic area hypothesis advances area as the primary cause of latitudinal gradients in diversity. The greater area of tropical zones, it suggests, stimulates speciation, inhibits extinction, and leads to increased species richness compared to the situation in smaller temperate and boreal zones. Because bats exhibit exceptionally strong latitudinal gradients of richness at multiple spatial scales in the New World, they are an appropriate system with which to test the geographic area hypothesis. We used range maps for 250 species of New World bats to estimate species richness in biogeographic zones at two hierarchical spatial scales: biome types and provinces. We then conducted a series of regression analyses to evaluate the ability of area to account for latitudinal gradients in species richness. However, spillover (zonal bleeding) of tropical species into extra-tropical zones may mask the species-area relationship and alter perceptions of the latitudinal gradient. To address this issue, we conducted additional analyses excluding tropical species, using a series of increasingly inclusive definitions of tropical ranges. Ecogeographic zones of the New World are not larger at tropical versus extra-tropical latitudes. Moreover, spillover of tropical species into ecogeographic zones within extra-tropical regions generally does not diminish the association between richness and area. Nonetheless, the latitudinal gradient of species richness is strong and significant at both ecogeographic scales. Clearly, area does not drive the latitudinal gradient of bat species richness in the New World. In fact, area represents a source of noise rather than a dominant signal at the focal scale of biome types and provinces in the Western Hemisphere.     

Plants and insects in early old-field succession: comparison of an English site and an American site

The plant and insect communities of early, secondary succession beginning with bare ground in an Old World site (southern Britain) and a New World site (Iowa, U.S.A.) shared a number of characteristics. Both sites showed similar temporal patterns of plant species cover and species richness, although overall richness was greater at the Old World site. Annuals dominated at both sites during the first year of succession and were largely replaced by perennials in the second year. Monocotyledons were more abundant at the Old World site, especially in the second year. The two sites differed markedly in the contribution of native and introduced plant species, with the Old World site dominated by natives and the New World site by alien plant species. Insect herbivore load was greater at the Old World site, when expressed in terms of structural complexity of the vegetation, suggesting that there may be major differences in the influence of herbivores on the direction and rate of succession at the two sites.     

Intestinal disaccharidases in five species of phyllostomoid bats.

1. Intestinal disaccharidases were studied in nectarivorous (Leptonycteris curasoae and Glossophaga soricina), frugivorous (Artibeus jamaicensis and Sturnira lilium), and insectivorous (Pteronotus personatus) adult bats. 2. Adult bats lacked measurable lactase activity. With the exception of trehalase activity, which was present only in P. personatus, nectar- and fruit-eating bats exhibited higher disaccharidase activities standardized by intestinal nominal area than insect-eating P. personatus. 3. Maltase and sucrase activities were significantly linearly correlated. 4. Apparent affinity of sucrase varied almost 5-fold among species. This variation may reflect unstirred layer effects resulting from sucrase being a membrane bound enzyme rather than differences in the "true" affinity of sucrase in solution. 5. Passerine birds showed higher maltase activity per unit of sucrase activity than bats and hummingbirds. Maximal sucrase and maltase activities standardized per intestinal nominal area are 1.5-2 times higher in hummingbirds than in nectar-feeding bats.     

Old World fruit bats can be long-distance seed dispersers through extended retention of viable seeds in the gut

Seed dispersal and pollination by animals play a crucial role in the maintenance of forest ecosystems worldwide. Frugivorous bats are important pollen and seed dispersers in both the Palaeo- and Neotropics, and at least 300 plant species are known to rely on Old World fruit bats (Megachiroptera, Pteropodidae) for their propagation. However, rapid food transit times (generally less than 30 minutes) in frugivorous bats have been thought to limit their ability to disperse seeds to just a few tens of kilometres. Here we demonstrate regular daytime (greater than 12 hours) retention of food and viable fig seeds (Ficus, Moraceae) in the gut of the Old World fruit bat Cynopterus sphinx: a behaviour not previously reported for any frugivorous bat. Field observations indicate that this behaviour also occurs in other genera. Old World fruit bats are highly mobile and many species undertake considerable foraging and migration flights. Our findings indicate that Old World fruit bats have the potential to disperse small seeds hundreds of kilometres. This necessitates a reappraisal of their importance in transporting zoochorous seeds to remote areas and facilitating gene flow between isolated populations of plants, both within mainlands and across ocean barriers.     

Insights into the structure of plant-insect communities: Specialism and generalism in a regional set of non-pollinating fig wasp communities

Insects show a multitude of symbiotic interactions that may vary in degree of specialization and structure. Gall-inducing insects and their parasitoids are thought to be relatively specialized organisms, but despite their ecological importance, the organization and structure of the interactions they establish with their hosts has seldom been investigated in tropical communities. Non-pollinating fig wasps (NPFW) are particularly interesting organisms for the study of ecological networks because most species strictly develop their offspring within fig inflorescences, and show a multitude of life history strategies. They can be gall-makers, cleptoparasites or parasitoids of pollinating or of other non-pollinating fig wasps. Here we analysed a set of non-pollinating fig wasp communities associated with six species of Ficus section Americanae over a wide area. This allowed us to investigate patterns of specialization in a diverse community composed of monophagous and polyphagous species. We observed that most NPFW species were cleptoparasites and parasitoids, colonizing figs several days after oviposition by pollinators. Most species that occurred in more than one host were much more abundant in a single preferential host, suggesting specialization. The food web established between wasps and figs shows structural properties that are typical of specific antagonistic relationships, especially of endophagous insect networks. Two species that occurred in all available hosts were highly abundant in the network, suggesting that in some cases generalized species can be more competitive than strict specialists. The Neotropical and, to a lesser extent, Afrotropical NPFW communities seem to be more generalized than other NPFW communities. However, evidence of host sharing in the Old World is quite limited, since most studies have focused on particular taxonomic groups (genera) of wasps instead of sampling the whole NPFW community. Moreover, the lack of quantitative information in previous studies prevents us from detecting patterns of host preferences in polyphagous species.     

Global patterns in peatmoss biodiversity

DNA sequence data from the nuclear ribosomal internal transcribed spacers (ITS) and the trnL-trnF chloroplast DNA regions were used to quantify geographical partitioning of global biodiversity in peatmosses (Sphagnum), and to compare patterns of molecular diversity with patterns of species richness. Molecular diversity was estimated for boreal, tropical, Neotropical, nonboreal (tropical plus Southern Hemisphere), Old World and New World partitions, based on a total of 436 accessions. Diversity was partitioned among geographical regions in terms of combined nuclear and chloroplast sequence data and separately for the ITS and trnL-trnF data sets. Levels of variation were estimated using phylogenetic diversity (PD), which incorporates branch lengths from a phylogenetic tree, and the number of polymorphic nucleotide sites. Estimates of species richness suggest that peatmoss diversity is higher in New World than Old World regions, and that the Neotropics constitute a "hotspot" of diversity. Molecular estimates, in contrast, indicate that peatmoss biodiversity is almost evenly divided between New and Old World regions, and that the Neotropics account for only 20-35% of global peatmoss diversity. In general, levels of tropical and boreal peatmoss molecular diversity were comparable. Two species, S. sericeum from the Old World tropics and S. lapazense from Bolivia, are remarkably divergent in nucleotide sequences from all other Sphagna and together account for almost 20% of all peatmoss diversity, although they are represented by only three of the 436 accessions (0.7%). These species clearly demonstrate the nonequivalence of species biodiversity value.     

Cloning and Molecular Evolution of the Aldehyde Dehydrogenase 2 Gene (Aldh2) in Bats (Chiroptera)

Old World fruit bats (Pteropodidae) and New World fruit bats (Phyllostomidae) ingest significant quantities of ethanol while foraging. Mitochondrial aldehyde dehydrogenase (ALDH2, encoded by the Aldh2 gene) plays an important role in ethanol metabolism. To test whether the Aldh2 gene has undergone adaptive evolution in frugivorous and nectarivorous bats in relation to ethanol elimination, we sequenced part of the coding region of the gene (1,143 bp, ~73 % coverage) in 14 bat species, including three Old World fruit bats and two New World fruit bats. Our results showed that the Aldh2 coding sequences are highly conserved across all bat species we examined, and no evidence of positive selection was detected in the ancestral branches leading to Old World fruit bats and New World fruit bats. Further research is needed to determine whether other genes involved in ethanol metabolism have been the targets of positive selection in frugivorous and nectarivorous bats.     

Spatial distribution of understory fruit-eating birds and fruiting plants in a neotropical lowland wet forest

Spatial distribution of fruit-eating birds and fruiting shrubs of the Melastomataceae and Rubiaceae were examined on a 10 ha plot in tropical lowland wet forest of Costa Rica. Many plant species and most birds exhibited considerable spatial variation in their occurrence on the plot, as indicated by the distribution patterns of shrubs with ripe fruits and captures in mist nets, respectively. In many cases, captures of fruit-eating birds were correlated with abundance of fruiting plants, particularly for species that rely heavily on fruits. In general, fruit-eating birds concentrated their use of the plot to areas rich in fruiting shrubs. This differential use of certain areas likely results in differential visitation to fruiting plants located in these areas and in a heterogeneous dissemination of seeds into the habitat.     

The myriad consequences of hunting for vertebrates and plants in tropical forests

Humans hunt forest vertebrates throughout the tropics. Many preferred game species consume flowers, fruit, seeds and/or leaves, and these interactions will cause their harvest to ramify through forests. Three related issues will determine how severely the harvest of forest vertebrates influences the plant community. First, the types of species selected by hunters and the intensity of the harvest will determine which vertebrates are removed and which remain. Second, the possible presence of ecologically similar, non-game species able to expand their activities to fulfill the ecological role of heavily exploited species will determine how severely the harvest disrupts ecological relationships between the community of forest vertebrates and the community of forest plants. Finally, hunters will alter plant species composition if the harvest of vertebrates differentially affects mutualists or pests of particular plant species. Hunters will also alter plant diversity if the harvest of vertebrates disrupts ecological mechanisms that permit plant species to coexist. I examine hunter selectivity, the intensity of the hunt, possible compensation by non-game species, and the types and strengths of interactions among game species and plants for tropical forests to determine when and where these outcomes occur.     

EVOLUTIONARY AND BIOGEOGRAPHIC ORIGINS OF HIGH TROPICAL DIVERSITY IN OLD WORLD FROGS (RANIDAE)

Differences in species richness between regions are ultimately explained by patterns of speciation, extinction, and biogeographic dispersal. Yet, few studies have considered the role of all three processes in generating the high biodiversity of tropical regions. A recent study of a speciose group of predominately New World frogs (Hylidae) showed that their low diversity in temperate regions was associated with relatively recent colonization of these regions, rather than latitudinal differences in diversification rates (rates of speciation–extinction). Here, we perform parallel analyses on the most species-rich group of Old World frogs (Ranidae; ∼1300 species) to determine if similar processes drive the latitudinal diversity gradient. We estimate a time-calibrated phylogeny for 390 ranid species and use this phylogeny to analyze patterns of biogeography and diversification rates. As in hylids, we find a strong relationship between the timing of colonization of each region and its current diversity, with recent colonization of temperate regions from tropical regions. Diversification rates are similar in tropical and temperate clades, suggesting that neither accelerated tropical speciation rates nor greater temperate extinction rates explain high tropical diversity in this group. Instead, these results show the importance of historical biogeography in explaining high species richness in both the New World and Old World tropics.     

The evolution of bat pollination: a phylogenetic perspective

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 about 528 species of angiosperms are pollinated by nectar-feeding bats. From a phylogenetic perspective this is a derived pollination mode involving a relatively large and energetically expensive pollinator. Here its ecological and evolutionary consequences are explored.

Scope and Conclusions

This review summarizes adaptations in bats and plants that facilitate this interaction and discusses the evolution of bat pollination from a plant phylogenetic perspective. Two families of bats contain specialized flower visitors, one in the Old World and one in the New World. Adaptation to pollination by bats has evolved independently many times from a variety of ancestral conditions, including insect-, bird- and non-volant mammal-pollination. Bat pollination predominates in very few families but is relatively common in certain angiosperm subfamilies and tribes. We propose that flower-visiting bats provide two important benefits to plants: they deposit large amounts of pollen and a variety of pollen genotypes on plant stigmas and, compared with many other pollinators, they are long-distance pollen dispersers. Bat pollination tends to occur in plants that occur in low densities and in lineages producing large flowers. In highly fragmented tropical habitats, nectar bats play an important role in maintaining the genetic continuity of plant populations and thus have considerable conservation value.