Trophic structure of frugivorous bats in the Neotropics: emergent patterns in evolutionary history

相似文献   

Ecomorphological analysis of trophic niche partitioning in a tropical savannah bat community

The exceptional diversity of neotropical bat communities is sustained by an intricate partitioning of available resources among the member species. Trophical specialization is considered an important evolutionary avenue towards niche partitioning in neotropical phyllostomid bats. From an ancestral insectivorous condition, phyllostomids evolved into highly specialized frugivorous, carnivorous, nectarivorous, piscivorous and even sanguivorous species. Previously, correlations between cranial morphology and trophic ecology within this group have been documented. Here, we examine the evolutionary relationships between bite force and head shape in over 20 species of bats from a single tropical savannah bat community. The results show that bite force increases exponentially with body size across all species examined. Despite the significant differences between large dietary groups using traditional analysis (i.e. non-phylogenetic) and the strong evolutionary correlations between body mass and bite force, phylogenetic analyses indicated no differences in bite performance between insectivorous, omnivorous and frugivorous bats. Comparisons of three species with highly specialized feeding habits (nectarivory, piscivory and sanguivory) with the rest of the species in the community indicate that specialization into these niches comes at the expense of bite performance and, hence, may result in a reduction of the trophic niche breadth.     

Opposed latitudinal patterns of network‐derived and dietary specialization in avian plant–frugivore interaction systems

Latitudinal patterns of biodiversity have been studied for centuries, but it is only during the last decades that species interaction networks have been used to examine the proposed latitudinal gradient of biotic specialization. These studies have given idiosyncratic results, which may either be because of genuine biological differences between systems, different concepts and scales used to quantify biotic specialization or because the methodological approaches used to compare interaction networks were inappropriate. Here we carefully examine the latitudinal specialization gradient using a global dataset of avian plant–frugivore assemblages and interaction networks. In particular, we test whether network‐derived specialization patterns differ from patterns based on assemblage‐level information on avian dietary preferences on specific food types. We found that network‐derived measures of specialization (complementary specialization H₂′ and < d’>, modularity Q) increased with latitude, i.e. frugivorous birds divide the niche of fruiting plants most finely at high latitudes where they also formed more modular interaction networks than at tropical latitudes. However, the strength and significance of the relationship between specialization metrics and latitude was influenced by the methodological approach. On the other hand, assemblage‐level information on avian specialization on fruit diet (i.e. the proportion of obligate frugivorous bird species feeding primarily on fruit) revealed an opposed latitudinal pattern as more bird species were specialized on fruit diet in tropical than in temperate assemblages. This difference in the latitudinal specialization gradient reflects that obligate frugivores require a high diversity of fruit plants, as observed in tropical systems, and fulfil more generalized roles in plant–frugivore networks than bird species feeding on different food types. Future research should focus on revealing the underlying ecological, historical and evolutionary mechanisms shaping these patterns. Our results highlight the necessity of comparing different scales of biotic specialization for a better understanding of geographical patterns of specialization in resource–consumer interactions.     

Trophic structure of a neotropical frugivore community: is there competition between birds and bats?

Summary Dietary overlap and competition between frugivorous birds and bats in the Neotropics have been presumed to be low, but comparative data have been lacking. We determined the diets of volant frugivores in an early successional patch of Costa Rican wet forest over a one month period. Ordination of the diet matrix by Reciprocal Averaging revealed that birds and bats tend to feed on different sets of fruits and that diets differed more among bat species than among bird species. However, there was overlap between Scarlet-rumped Tanagers and three Carollia bat species on fruits of several Piper species which comprised most of the diet of these bats. Day/night exclosure experiments on P. friedrichsthalli treetlets provided evidence that birds deplete the amount of ripe fruit available to bats. These results indicate that distantly related taxa may overlap in diet and compete for fruit, despite the apparent adaptation of animal-dispersed plant species for dispersal by particular animal taxa.     

Why do some,but not all,tropical birds migrate? A comparative study of diet breadth and fruit preference

Annual migrations of birds profoundly influence terrestrial communities. However, few empirical studies examine why birds migrate, in part due to the difficulty of testing causal hypotheses in long-distance migration systems. Short-distance altitudinal migrations provide relatively tractable systems in which to test explanations for migration. Many past studies explain tropical altitudinal migration as a response to spatial and temporal variation in fruit availability. Yet this hypothesis fails to explain why some coexisting, closely-related frugivorous birds remain resident year-round. We take a mechanistic approach by proposing and evaluating two hypotheses (one based on competitive exclusion and the other based on differences in dietary specialization) to explain why some, but not all, tropical frugivores migrate. We tested predictions of these hypotheses by comparing diets, fruit preferences, and the relationships between diet and preference in closely-related pairs of migrant and resident species. Fecal samples and experimental choice trials revealed that sympatric migrants and residents differed in both their diets and fruit preferences. Migrants consumed a greater diversity of fruits and fewer arthropods than did their resident counterparts. Migrants also tended to have slightly stronger fruit preferences than residents. Most critically, diets of migrants more closely matched their preferences than did the diets of residents. These results suggest that migrants may be competitively superior foragers for fruit compared to residents (rather than vice versa), implying that current competitive interactions are unlikely to explain variation in migratory behavior among coexisting frugivores. We found some support for the dietary specialization hypothesis, propose refinements to the mechanism underlying this hypothesis, and discuss how dietary specialization might ultimately reflect past interspecific competition. We recommend that future studies quantify variation in nutritional content of tropical fruits, and determine whether frugivory is a consequence or a cause of migratory behaviour.     

Diet and trophic structure in assemblages of montane frugivorous phyllostomid bats

Neotropical frugivorous bats display a trophic structure composed of bat species with dietary preferences of core plant taxa (Artibeus-Ficus  +  Cecropia, Carollia-Piper, Sturnira- Solanum  +  Piper). This structure is hypothesized to be an ancestral trait, suggesting that similar diets would be observed throughout a species' range. However, most evidence comes from lowlands where data from montane habitats are scarce. In high mountain environments both diversity of bats and plants decreases with altitude; such decline in plant diversity produces less plants to feed from, which should ultimately affect the trophic structure of frugivorous bats in mountain environments. Here, we present a comprehensive review of the diet of frugivorous bats in Neotropical montane environments and evaluate their trophic structure in middle and higher elevations by combining a literature database with field data. We use the concept of modularity to test whether frugivorous montane bats have dietary preferences on core plant taxa. Our database revealed 47 species of montane bats feeding on 211 plant species. We find that the networks are modular, reflecting the trophic structure previously reported. We also found that in highlands the tribe Ectophyllini are Cecropia  +  Cavendishia-specialists rather than Ficus-specialists, and we describe new interactions reflecting 14 species of plants, including three botanical families previously not reported to be consumed by bats.     

Does seed ingestion by bats enhance germination? A new meta‐analysis 15 years later

相似文献   

Palate Variation and Evolution in New World Leaf-Nosed and Old World Fruit Bats (Order Chiroptera)

Two bat families, the leaf-nosed (Phyllostomidae) and fruit bats (Pteropodidae), have independently evolved the ability to consume plant resources. However, despite their similar ages, species richness and the strong selective pressures placed on the evolution of skull shape by plant-based foods, phyllostomids display more craniofacial diversity than pteropodids. In this study, we used morphometrics to investigate the distribution of palate variation and the evolution of palate diversity in these groups. We focused on the palate because evolutionary alterations in palate morphology are thought to underlie much feeding specialization in bats. We hypothesize that the distribution of palate variation differs in phyllostomids and pteropodids, and that the rate of palate evolution is higher in phyllostomids than pteropodids. The results suggest that the overall level of palate integration is higher in adult populations of pteropodids than phyllostomids but that the distribution of palate variation is otherwise generally conserved among phyllostomids and pteropodids. Furthermore, the results are consistent with these differences in palate integration likely having a developmental basis. The results also suggest that palate evolution has occurred significantly more rapidly in phyllostomids than pteropodids. These findings are consistent with a scenario in which the greater integration of the pteropodid palate has limited its evolvability.     

Sources of assimilated protein in five species of New World frugivorous bats

Fruits are N-poor items and their availability in the tropics varies throughout the year. Field and experimental studies debate whether frugivorous bats have to switch to N-rich sources of food during part of the year or if they are able to subsist on a fruit-only diet. Different strategies to meet their N requirements may influence the way in which frugivorous bats partition food resources allowing the coexistence of numerous species in tropical communities. We examined the extent to which five species of frugivorous bats relied on plant and insect sources of assimilated protein using stable-N isotope analysis. We assumed that bats only had access to fruits and insects in our analysis but we also collected fecal samples to examine the presence of other food items. We conducted the study during at least 1 full year depending on the species of bat in a tropical rain forest in southern Mexico. In the five species of bats examined, plant sources (i.e. fruits) provided most of the protein assimilated during the year, although there was a general trend for all species to show a decrease in relative plant contribution at the end of the rainy season and beginning of the dry season. In Artibeus jamaicensis, Uroderma bilobatum and Dermanura phaeotis, plants were still a major source of protein during this period, but in some individuals of Sturnira lilium and Carollia brevicauda insects represented an important contribution to their diet. Fecal samples of most bats presented fruit remains, and insects and pollen were found in small proportions. Bat reproductive activity was detected at the end of the dry season and in the middle of the rainy season, and plants were the major source of protein during this period with the exception of pregnant S. lilum and one pregnant D. phaeotis during the dry season. Our findings showed that frugivorous bats might differ in their strategies to satisfy their N demands with some species relying almost completely on fruits during most of the year and some species switching to insects when fruits were less abundant.     

Fruiting phenology of palms and trees in an Atlantic rainforest land-bridge island

Tropical forests show periods of scarcity and high fruit production in the same year and/or between years. Palms are an important component of Neotropical rainforests and a significant food resource for several frugivores. Therefore, their role as keystone resource may be exacerbated in highly impoverished areas. In Anchieta Island, São Paulo/Brazil, human settlements have modified and impoverished the forest, mainly through overharvesting and the introduction of exotic plants and several mammal species. We assessed the offer of fruits consumed by vertebrate frugivores at this island, the vegetation of which is belonging to the Brazilian Atlantic rainforest. We compared whether the fruiting patterns and fruit fall differ between palms and trees, and discuss the importance of palms as a food resource for frugivores and the implications for Anchieta Island conservation. Phenological patterns were seasonal for both trees and palms; however, the times of fruiting occurrence differed. Fruit fall biomass was at least twice lower than reported for other Atlantic rain forests and was also different between trees and palms. Palms contributed more than 80% of the overall fruit fall biomass. Palms may constitute an alternative food resource in periods of low fruit availability, although they do not provide resources for the entire assemblage of vertebrate frugivores. Energy-rich fruits, such as those produced by palms, may play an important role in the maintenance of frugivore populations in isolated, disturbed environments with a high density of vertebrate frugivores, low diversity of fruiting species and fruit biomass such as those found on Anchieta Island.     

An analysis of diet specialization in frugivorous Pteropus poliocephalus (Megachiroptera) in Australian subtropical rainforest

Abstract The Grey-headed flying fox Pteropus poliocephalus Temminck 1825 is the only mammalian frugivore to occupy substantial areas of the subtropical rainforests of eastern Australia. The composition of the P. poliocephalus diet and diet specialization in the species are therefore pertinent to studies of trophic structure, seed dispersal and evolutionary processes in these forests. During a three-year diet study, P. poliocephalus used fruits from 44 species of canopy and edge plants. Their taxonomically diverse diet was dominated by the Myrtaceae and Moraceae. Dietary specialization by P. poliocephalus was examined using two criteria: the influence of fruit morphology on diet choice and dietary overlap with sympatric avian frugivores. There was no evidence from either approach that they were specialist feeders. Initial analyses comparing the morphological characters of diet fruits with fruits available to P. poliocephalus during the study period showed a preference for white fruits, berries, syconia and fruits with multiple seeds, and avoidance of black fruits and drupes. However, these significant results were not sustained when the confounding effects of correlations between fruit morphology and other traits were considered. All, except the response to berries, could be attributed to either avoidance by P. poliocephalus of secondary compounds in the Lauraceae or selection for the beneficial phenology of Ficus. Dietary overlap with frugivorous birds was notably high and the fruit diet of P. poliocephalus formed a subset of the avian diet. Associations between fruit colour, size and protective mechanisms have been documented in other rainforest areas and have been proposed as indicators of coadaptive relationships between vertebrate frugivores and their diet plants. However, these associations were not apparent in the morphological characters of fleshy fruits from Australian subtropical rainforest trees. An explanatory hypothesis of primarily avian influence on fruit traits is presented.     

Differences in Growth Generate the Diverse Palate Shapes of New World Leaf-Nosed Bats (Order Chiroptera,Family Phyllostomidae)

New World leaf-nosed bats (Family Phyllostomidae) display incredible craniofacial diversity that is associated with their broad range of dietary preferences. The short and broad palates of highly frugivorous bats are functionally linked to high bite forces, and the long and narrow palates of nectarivorous bats to flower feeding. Although the functional correlates and evolutionary history of shape variation in phyllostomid palates are beginning to be understood, the specific developmental processes that govern palate diversification remain unknown. To begin to resolve this issue, this study quantified palate morphology in seven phyllostomid species from a range of developmental stages and in adults. This sample includes species with short and broad, long and narrow, and intermediate palate shapes, and thereby covers the range of palate shapes displayed by phyllostomids. Results indicate that while initial palate shape (i.e., width vs. length) varies among species, the pattern of this variation does not match that observed in adults. In contrast, the relative growth of palate width and length in developing phyllostomids and the ratio of these axes in adults are significantly correlated. These and other results suggest that evolutionary alterations in patterns of palate growth have governed the diversification of palate shapes in adult phyllostomids. This implies that the diverse palate shapes of phyllostomids are the result of relatively subtle evolutionary changes in later rather than earlier development events.     

Seasonal dietary niche contraction in coexisting Neotropical frugivorous bats (Stenodermatinae)

Tropical dry forests are characterized by punctuated seasonal precipitation patterns that drive primary production and the availability of fruits, seeds, flowers, and insects throughout the year. In environments in which the quantity and quality of food resources varies seasonally, consumers should adjust their foraging behavior to maximize energy intake while minimizing overlap with competitors during periods of low food availability. Here, we investigated how the diets of frugivorous bats in tropical dry forests of NW Mexico varied in response to seasonal availability and how this affected dietary overlap of morphologically similar species. We performed stable isotope analyses to understand temporal and interspecific patterns of overall isotopic niche breadth, trophic position, and niche overlap in the diet of six frugivorous species of closely related New World leaf-nosed bats (family Phyllostomidae, subfamily Stenodermatinae). We estimated seasonal changes in resource abundance in two complementary ways: (a) vegetative phenology based on long-term remote sensing data and (b) observational data on food availability from previously published insect and plant fruiting surveys. In all species, there was a consistent pattern of reduced isotopic niche breadth during periods of low food availability. However, patterns of niche overlap varied between morphologically similar species. Overall, results from our study and others suggest that seasonal food availability likely determines overall dietary niche breadth in Phyllostomidae and that despite morphological specialization, it is likely that other mechanisms, such as opportunistic foraging and spatiotemporal niche segregation, may play a role in maintaining coexistence rather than simply dietary displacement.     

Tropical Secondary Forest Management Influences Frugivorous Bat Composition,Abundance and Fruit Consumption in Chiapas,Mexico

Most studies on frugivorous bat assemblages in secondary forests have concentrated on differences among successional stages, and have disregarded the effect of forest management. Secondary forest management practices alter the vegetation structure and fruit availability, important factors associated with differences in frugivorous bat assemblage structure, and fruit consumption and can therefore modify forest succession. Our objective was to elucidate factors (forest structural variables and fruit availability) determining bat diversity, abundance, composition and species-specific abundance of bats in (i) secondary forests managed by Lacandon farmers dominated by Ochroma pyramidale, in (ii) secondary forests without management, and in (iii) mature rain forests in Chiapas, Southern Mexico. Frugivorous bat species diversity (Shannon H’) was similar between forest types. However, bat abundance was highest in rain forest and O. pyramidale forests. Bat species composition was different among forest types with more Carollia sowelli and Sturnira lilium captures in O. pyramidale forests. Overall, bat fruit consumption was dominated by early-successional shrubs, highest late-successional fruit consumption was found in rain forests and more bats consumed early-successional shrub fruits in O. pyramidale forests. Ochroma pyramidale forests presented a higher canopy openness, tree height, lower tree density and diversity of fruit than secondary forests. Tree density and canopy openness were negatively correlated with bat species diversity and bat abundance, but bat abundance increased with fruit abundance and tree height. Hence, secondary forest management alters forests’ structural characteristics and resource availability, and shapes the frugivorous bat community structure, and thereby the fruit consumption by bats.     

Intrinsic and extrinsic factors affecting dietary specialization in Neotropical frugivorous bats

相似文献   

Use of Fruit Essential Oils to Assist Forest Regeneration by Bats

Frugivorous bats can be attracted with essential oils from ripe chiropterochoric fruit. We evaluated the efficiency of these oils to attract bats in degraded areas within the Atlantic Rain Forest, particularly pasture and agricultural land. We hypothesized that induction units (IUs), each containing a rubber septum impregnated with oil, would have more bat activity than their respective control units (CUs; without the oil). To test this hypothesis we monitored bat flight activity with night‐vision infrared visors in eight IU and CU from August 2006 to July 2007. We also verified the probability of arrival of chiropterochoric seeds by analyzing the diet of bats captured in a neighboring forest area. Our initial hypothesis that units with odor would lead to greater bat activity was confirmed. Results indicated a rich community of fruit‐eating bats, and dietary analysis revealed a huge potential for dispersion of a vast amount of seeds from different plant species at the IU. Although our study does not reveal with certainty which bat species are attracted to the oil, the flying patterns coincide with those described for the foraging behavior of fruit‐eating phyllostomids. Furthermore, the fact that the bats spend more time flying around the odor source compared to flying time around CU suggest an increase in seed rain. Taken together, these results suggest that the use of essential oils from chiropterochoric fruits induces a qualitative and quantitative increase in seed dispersal in areas that otherwise would not be frequently visited by frugivorous bats.     

Trophic structure in a large assemblage of phyllostomid bats in Panama

Bats of the family Phyllostomidae are fundamental components of Neotropical mammalian diversity and display the greatest dietary diversity seen in any mammalian family. We studied trophic structure in a species-rich local assemblage of phyllostomids for which dietary data were collected during 10 years on Barro Colorado Island, Panama. Correspondence analysis of >3800 dietary records from 30 syntopic species showed a structure supporting traditional divisions of animalivorous and phytophagous phyllostomids. Putatively omnivorous species actually grouped among the latter. Phytophagous phyllostomids separated into Piper -specialists, Ficus -specialists, and eclectic plant eaters which in turn were the main consumers of flower products. Discrete dietary groups were compatible with several clades of the two current phylogenetic hypotheses of phyllostomids. We show that the trophic structure of the local contemporary assemblage is largely conservative with respect to traceable ancestral habits, strongly suggesting that overall trophic structure was likely determined historically.     

Speciation and coevolution: an interpretation of frugivory phenomena

Evolutionary considerations of frugivory must account for patterns of diversity and abundance of both frugivorous vertebrates (especially pulp-eaters) and of plants producing zoochorous fruits. Analysis of the diet and behavior of representative species of frugivores from the tropical forests of French Guiana (seven species of bird and eight mammals) allowed their degree of specialization for frugivory to be assessed. Analysis of the flora associated with these species showed that genera associated with specialized vertebrates had the greatest species richness. This pattern suggests that plant animal co-evolution occurs in a step-wise fashion with short transitory phases of animal and plant evolution followed by long periods of stability.     

When did plants become important to leaf‐nosed bats? Diversification of feeding habits in the family Phyllostomidae

A great proportion of bats of the New World family Phyllostomidae feed on fruit, nectar and pollen, and many of them present adaptations to feed also on insects and small vertebrates. So far, attempts to examine the diversification of feeding specialization in this group, and particularly the evolution of nectarivory and frugivory, have provided contradictory results. Here we propose a molecular phylogenetic hypothesis for phyllostomids. On the basis of a matrix of feeding habits that takes into account geographical and seasonal variation, we tested different hypotheses of the evolution of feeding specializations in the group. We find strong support for the evolutionary model of a direct dietary diversification from insectivory. The estimates of divergence times of phyllostomid bats and the reconstruction of ancestral states with a Bayesian approach support the parallel evolution of frugivory in five lineages and of nectarivory in three lineages during the Miocene. On the basis of these findings, and recent dietary studies, we propose that during the evolution of phyllostomids switches to new feeding mechanisms to access to abundant and/or underexploited resources provided selective advantages that favoured the appearance of ecological innovations independently in different lineages of the family. We did not find evidences to support or reject the hypothesis that the insectivorous most recent common ancestor of all phyllostomids was also phytophagous.     

Convergence in community structure and dietary adaptation in Australian possums and gliders and Malagasy lemurs

Abstract The possums and gliders of Australia and the lemurs of Madagascar are ideally suited for investigation of radiation and convergence in arboreal mammal communities because of their long history of independent radiation in similar biophysical environments. Possum and glider communities at 22 sites in Australia and lemur communities at 18 sites in Madagascar were compared to evaluate patterns of community and species convergence in two shared habitats (evergreen and deciduous monsoon rainforests) and three derived habitats (Australian eucalypt forests and heaths, and Malagasy thorn scrubs). Arboreal mammals were classified into five dietary guilds for comparison of community structure and species adaptation. There is little evidence of convergence in trophic structure at the community level, but strong evidence of convergence in dietary adaptation at the species and niche level. Malagasy rainforest communities were characterized by a higher proportion of frugivore-folivores, and Australian rainforest and moist eucalypt communities by a higher proportion of folivores and folivore-frugivores. Possum and glider communities in temperate eucalypt forests and heaths supported a higher proportion of nectarivores and exudivores. Overall species richness was significantly higher in Madagascar. Four hypotheses are erected to account for these differences. The relative scarcity of frugivores in Australian evergreen rainforests is accounted for by the predominance of bird-dispersed fruits, and fruiting phenologies unsuitable for mammal exploitation and dispersal. Higher folivore diversity in Australian evergreen rainforests is associated with a more pronounced seasonal shortage of edible fruits and new leaf, which has increased dependence on mature leaf. Folivore species richness is greatest in Australian moist eucalypt forests where structural complexity, sustained by serai responses to wildfire, permits a high level of vertical segregation. Increased nectarivory and exudivory in Australian temperate eucalypt forests and heaths is associated with Mediterranean winter rainfall regimes, which permit year round exudate production, and not with the absence of nectar feeding bats as previously supposed. A lower overall species richness in Australian rainforests is attributed to a longer history of contraction and fragmentation by anthropogenic fires (monsoon rainforests) and Pleistocene climatic change (tropical evergreen rainforests). A high degree of convergence is apparent between genera occupying folivore and wood gouging niches, in terms of gastrointestinal morphology (e.g. Pseudocheirus-Lepilemur) and dental morphology (e.g. Dactylopsila-Daubentonia). Divergences are most apparent in adaptations associated with frugivory, including larger body size, diurnality, and bipedal suspension and leaping modes of locomotion (in Eulemur spp.). This study highlights the importance of founding effects, competition from other vertebrate taxa, coevolution between animals and their food plants, and differences in biophysical environments, as determinants of mammalian radiation and convergence.