Akbar Zubaid

Resource partitioning in rhinolophoid bats revisited

Abstract We assessed the ecomorphological structure of a guild of rhinolophoid bats in a Malaysian rainforest first described by Heller and von Helversen (1989). These authors found that the distribution of echolocation call frequencies used by 12 syntopic species was more even than expected from allometric relationships or in randomly generated communities, and that the observed minimal ratio was greater than expected by chance alone. In this study we were able to expand their guild to 15 species, but in doing so it became apparent that call frequencies might be less evenly distributed across the total frequency range than previously proposed. We replicated Heller and von Helversen’s (1989) analyses with the full 15-species complement but were unable to support their suggestion that rhinolophoid bats exhibit resource partitioning through differences in frequency bands. We adopted a multivariate approach and incorporated measures of body size and wing morphology into the analysis. We used phylogenetic autocorrelation to ensure that the species were statistically independentand principal component analysis to describe the morphological space occupied by the 15 species in the community and four additional species representing the extremes of phenotypic variation. We derived interspecific Euclidean distances and tested the mean values and SDs of these distances against those of 100 guilds of ”synthetic” species created randomly within the principal component space. The guild of Rhinolophoidea was not distributed randomly in multivariate space. Instead we found evidence of morphological overdispersion of the most similar species, which suggests niche differentiation in response to competition. Less similar species were nearer in morphological space than expected, and we suggest this is a consequence of ecological constraints on parameter combinations. Despite this underdispersion, many of the more distant neighbours were evenly rather than randomly spaced or clumped in morphospace, suggesting that, given the environmental constraints on morphology, species in this guild do experience limits to their similarity. Finally, we tested the influence of the relative abundance of species on morphological displacement, and found no evidence that abundant, spatially correlated species reduce interspecific overlap in morphological space.

Chemical ecology of fruit bat foraging behavior in relation to the fruit odors of two species of paleotropical bat-dispersed figs (Ficus hispida and Ficus scortechinii)

We investigated the fruit odors of two bat-dispersed fig species in the Paleotropics, in relation to the foraging behavior of fruit bats, to test the following hypotheses: 1) fruit odor plays a critical role for detection and selection of ripe figs by fruit bats; 2) bat-dispersed fig species are characterized by the same, or similar, chemical compounds; and 3) total scent production, in bat-dispersed figs, increases when fruits ripen. We performed bioassays to test the effect of both natural and synthetic fig fruit odors on the foraging behavior of the short-nosed fruit bat (Cynopterus brachyotis)—an important disperser of figs within the study area. Fruit bats responded to both visual and chemical (olfactory) cues when foraging for figs. However, the strongest foraging reaction that resulted in a landing or feeding attempt was almost exclusively associated with the presence of a ripe fruit odor—either in combination with visual cues or when presented alone. Fruit bats also used fruit odors to distinguish between ripe and unripe fruits. By using gas chromatography (GC) and GC/mass spectrometry (MS), a total of 16 main compounds were identified in the ripe fruit odor of Ficus hispida and 13 in the ripe fruit odor of Ficus scortechinii—including alcohols, ketones, esters, and two terpenes. Additional compounds were also recorded in F. hispida, but not identified—four of which also occurred in F. scortechinii. Total scent production increased in both species when fruits ripened. Both natural and synthetic fruit odors resulted in feeding attempts by bats, with no feeding attempts elicited by unscented controls. Reaction rates to natural fruit odors were higher than those to synthetic blends.

Comparative population structure of Cynopterus fruit bats in peninsular Malaysia and southern Thailand

The extent to which response to environmental change is mediated by species‐specific ecology is an important aspect of the population histories of tropical taxa. During the Pleistocene glacial cycles and associated sea level fluctuations, the Sunda region in Southeast Asia experienced concurrent changes in landmass area and the ratio of forest to open habitat, providing an ideal setting to test the expectation that habitat associations played an important role in determining species’ response to the opportunity for geographic expansion. We used mitochondrial control region sequences and six microsatellite loci to compare the phylogeographic structure and demographic histories of four broadly sympatric species of Old World fruit bats in the genus, Cynopterus. Two forest‐associated species and two open‐habitat generalists were sampled along a latitudinal transect in Singapore, peninsular Malaysia, and southern Thailand. Contrary to expectations based on habitat associations, the geographic scale of population structure was not concordant across ecologically similar species. We found evidence for long and relatively stable demographic history in one forest and one open‐habitat species, and inferred non‐coincident demographic expansions in the second forest and open‐habitat species. Thus, while these results indicate that Pleistocene climate change did not have a single effect on population structure across species, a correlation between habitat association and response to environmental change was supported in only two of four species. We conclude that interactions between multiple factors, including historical and contemporary environmental change, species‐specific ecology and interspecific interactions, have shaped the recent evolutionary histories of Cynopterus fruit bats in Southeast Asia.

Habitat structure, wing morphology, and the vertical stratification of Malaysian fruit bats (Megachiroptera: Pteropodidae)

This study investigated the vertical stratification of Old World fruit bats (Chiroptera: Pteropodidae) in relation to habitat structure and wing morphology, in a lowland Malaysian rain forest. In total, 352 fruit bats of eight species were captured within the subcanopy of the structurally complex old-growth forest during 72 306 m 2 mist net hours of sampling. Fruit bat species that were grouped in relation to capture height were also grouped in relation to wing morphology - with those species predicted to have more manoeuvrable flight (i.e. lower wing-loadings and lower aspect-ratios) captured in increasingly cluttered airspaces. Thus, small differences in wing morphology are likely to be ecologically significant to the vertical stratification of bats. Hence, habitat heterogeneity may be a key factor promoting fruit bat species diversity in old-growth palaeotropical forests.

Food habits of Cynopterus brachyotis (Muller) (Chiroptera: Pteropodidae) in Peninsular Malaysia

Information on the feeding habits of the lesser dog-faced fruit bat, Cynopterus brachyotis, was obtained by the collection of food remains directly beneath daytime and feeding roosts. The bats were found to feed on the fruits of 54 plant species, the leaves of 14 species and the flower parts of four species. The seasonal phenological differences among congeneric plant species led to a steady production of fruit throughout the year and the data suggest that Ficus spp. are a key compon- ent in the diet. Judging from its wide selection of fruits, C. brachyotis, is considered to be an important seed disperser. Folivory in C. brachyotis appears to be more common than previously thought. Of the leaves consumed by the bats, seven spe- cies belonged to the family Leguminosae, followed by Myrtaceae, Moraceae, Rhizo- phoraceae and Euphorbiaceae. Fruits, in general, provide an energy-rich diet for phytophagous bats but most are low in protein. In contrast, leaves consumed by bats have a relatively high protein content. We suggest that folivory (by leaf fractionation) should be energetically more advantageous than the ingestion of large amounts of low protein fruit or the active pursuit of mobile insects.

Molecular phylogeny of hipposiderid bats from Southeast Asia and evidence of cryptic diversity

Old World leaf-nosed bats (Hipposideridae) are among the most widespread and ecologically diverse groups of insectivorous bats in the Old World tropics. However, phylogenetic relationships in Hipposideridae are poorly resolved at both the generic and species levels, and deep genetic divergence within several Southeast Asian species suggests that current taxonomy underestimates hipposiderid diversity in this region. We used mitochondrial and nuclear sequence data to conduct the first extensive molecular phylogenetic analysis of Southeast Asian hipposiderid bats. Inclusion of multiple samples per taxon allowed testing for evidence of evolutionarily distinct lineages within taxa currently defined as single species. In contrast to earlier phylogenies based on morphometrics, molecular data support monophyly of Hipposideros, but are ambiguous regarding the monophyly of Hipposideridae. With a few exceptions, molecular data also support currently recognized species groups classified by qualitative morphological characters. Widespread paraphyly and polyphyly within many currently recognized species of Hipposideros indicates that evolutionary diversity in the genus is underrepresented by current nomenclature. Comparison of available morphological and echolocation data suggest that both geographic isolation and ecological selection have contributed to the diversification of Southeast Asian hipposiderid bats.

Social organization and genetic structure: insights from codistributed bat populations

The impact of ecology and social organization on genetic structure at landscape spatial scales, where gene dynamics shape evolution as well as determine susceptibility to habitat fragmentation, is poorly understood. Attempts to assess these effects must take into account the potentially confounding effects of history. We used microsatellites to compare genetic structure in seven bat species with contrasting patterns of roosting ecology and social organization, all of which are codistributed in an ancient forest habitat that has been exceptionally buffered from radical habitat shifts. Over one thousand individuals were captured at foraging sites and genotyped at polymorphic microsatellite loci. Analyses of spatially explicit genotype data revealed interspecies differences in the extent of movement and gene flow and genetic structure across continuous intact forest. Highest positive genetic structure was observed in tree‐roosting taxa that roost either alone or in small groups. By comparison, a complete absence of genetic autocorrelation was noted in the cave‐roosting colonial species across the study area. Our results thus reveal measurable interspecies differences in the natural limits of gene flow in an unmodified habitat, which we attribute to contrasting roosting ecology and social organization. The consequences of ecology and behaviour for gene flow have important implications for conservation. In particular, tree‐roosting species characterized by lower vagility and thus gene flow will be disproportionally impacted by landscape‐scale forest clearance and habitat fragmentation, which are prevalent in the study region. Our method also highlights the usefulness of rapid sampling of foraging bats for assaying genetic structure, particularly where roosting sites are not always known.

A new species of Kerivoula (Chiroptera: Vespertilionidae) from peninsular Malaysia

ABSTRACT A new species of small Kerivoula is described from peninsular Malaysia. It is similar in size and form to Kerivoula hardwickii Miller 1898 or K. intermedia Hill and Francis 1984, but is distinguished by its distinctive colouration — dorsal fur has extensive black bases with shiny golden tips, ventral fur has dark grey bases with whitish-buff tips — as well as several characters of dentition and skull shape. Sequence analysis of the first 648 base pairs of cytochrome oxidase I gene (DNA barcode) indicates a divergence of at least 11% from all other species of Kerivoula, a difference comparable to that between other species of Kerivoula.

Morphological and ecological correlates of coexistence in malaysian fruit bats (Chiroptera: Pteropodidae)

Abstract Niche theory predicts that coexisting species should differ ecologically, morphologically, or behaviorally in ways that minimize competition. We used an ecomorphological approach to determine how coexisting species in the Old World fruit bat genus, Cynopterus, assort in morphological and ecological space. The study was conducted in peninsular Malaysia where 4 species of Cynopterus are broadly sympatric. Interspecific separation in resource use was estimated along 3 main axes: habitat, based on abundance across a habitat gradient at 2 sites; trophic niche, inferred from a suite of cranial and postcranial characters; and locomotory behavior and efficiency, inferred from wing morphology. Habitat associations, overall size, and the size and shape of the trophic apparatus were all important in separating 2 or more species, whereas interspecific differences in wing morphology were minor. In combination, the results of this study suggest that relatively minor separation among Cynopterus species pairs along single axes of resource use is sufficient to counteract overlap on other axes, and permit the coexistence of potential competitors.

Phylogenetic relationships of the Asian palm civets (Hemigalinae & Paradoxurinae, Viverridae, Carnivora)

The Viverridae (Mammalia, Carnivora), one of the least studied groups of carnivorans, include two subfamilies of Asian palm civets: Hemigalinae and Paradoxurinae. The relationships between and within these two subfamilies have never been thoroughly tested using an extensive molecular sample set. In this study, we gathered sequences of four genes (two mitochondrial: Cytochrome b and ND2 and two nuclear: beta-fibrinogen intron 7 and IRBP exon 1) for eight of the eleven extant species representing these two subfamilies. The results showed that: (1) the Asian palm civets (Hemigalinae and Paradoxurinae) have a single origin and form the sister-group of the (Genettinae+Viverrinae) clade, (2) the Hemigalinae (including the otter civet Cynogale bennettii) are monophyletic, (3) the Paradoxurinae are monophyletic and (4) the small-toothed palm civet (Arctogalidia trivirgata) is an early offshoot within the Paradoxurinae. Using a relaxed molecular clock analysis, the differentiation of the (Hemigalinae+Paradoxurinae) was inferred to occur in the Late Oligocene/Early Miocene.