M. Corrie Schoeman

GENETIC AND PHENOTYPIC DIFFERENCES BETWEEN SOUTH AFRICAN LONG-FINGERED BATS, WITH A GLOBAL MINIOPTERINE PHYLOGENY

Abstract The Natal long-fingered bat (Miniopterus natalensis) and lesser long-fingered bat (M. fraterculus) are morphologically almost indistinguishable and occur sympatrically over much of their southern African range. This raises the possibility that they are sister taxa. We employed a multidisciplinary approach to examine their taxonomic relationship to one another and to other Miniopterus species, whose global phylogeny requires review. We examined echolocation, morphological, and dietary differences between M. natalensis and M. fraterculus, as well as both nuclear and mitochondrial DNA variation between them in the context of a phylogeny incorporating 13 Miniopterus species and subspecies. Despite similarities in their morphology and distribution, M. natalensis and M. fraterculus echolocate at peak frequencies separated by 12 kHz, and both nuclear and mitochondrial DNA markers confirm they are distinct species. Analysis of cytochrome-b (Cytb) sequences further indicates that M. fraterculus and M. natalensis are not sister taxa; M. fraterculus appears to be more closely related to the greater long-fingered bat (M. inflatus). Examination of the global taxonomy of Miniopterus confirms that Schreiberss long-fingered bat (M. schreibersii) forms a paraphyletic species complex. Furthermore, the miniopterine bats are divided into 2 geographically isolated monophyletic groups, one containing African and European species, and the other taxa from Australasia and Asia. Cytb sequence divergence also suggests that M. natalensis is distinct from the European M. schreibersii. These results support the elevation of M. natalensis to full species rank.

The relative influence of competition and prey defenses on the phenotypic structure of insectivorous bat ensembles in southern Africa

Deterministic filters such as competition and prey defences should have a strong influence on the community structure of animals such as insectivorous bats that have life histories characterized by low fecundity, low predation risk, long life expectancy, and stable populations. We investigated the relative influence of these two deterministic filters on the phenotypic structure of insectivorous bat ensembles in southern Africa. We used null models to simulate the random phenotypic patterns expected in the absence of competition or prey defences and analysed the deviations of the observed phenotypic pattern from these expected random patterns. The phenotypic structure at local scales exhibited non-random patterns consistent with both competition and prey defense hypotheses. There was evidence that competition influenced body size distribution across ensembles. Competition also influenced wing and echolocation patterns in ensembles and in functional foraging groups with high species richness or abundance. At the same time, prey defense filters influenced echolocation patterns in two species-poor ensembles. Non-random patterns remained evident even after we removed the influence of body size from wing morphology and echolocation parameters taking phylogeny into account. However, abiotic filters such as geographic distribution ranges of small and large-bodied species, extinction risk, and the physics of flight and sound probably also interacted with biotic filters at local and/or regional scales to influence the community structure of sympatric bats in southern Africa. Future studies should investigate alternative parameters that define bat community structure such as diet and abundance to better determine the influence of competition and prey defences on the structure of insectivorous bat ensembles in southern Africa.

The relative influence of competition and prey defences on the trophic structure of animalivorous bat ensembles

Deterministic filters such as competition and prey defences should have a strong influence on the community structure of animals like animalivorous bats which have life histories characterized by low fecundity, low predation risk, long life expectancy and stable populations. We investigated the relative influence of these two deterministic filters on the trophic structure of animalivorous bat assemblages in South Africa. We used null models to test if patterns of dietary overlap were significantly different from patterns expected by chance and multivariate analyses to test the correlations between diet and phenotype (body size, wing morphology and echolocation). We found little evidence that competition structured the trophic niche of coexisting bats. Contrary to predictions from competition, dietary overlap between bats of ensembles and functional groups (open-air, clutter-edge, and clutter foragers) were significantly higher than expected by chance. Instead, we found support for the predictions of the allotonic frequency hypothesis: there were significant relationships between peak echolocation frequency and the proportion of moths in the diets of bats at local and regional scales, and peak echolocation frequency was the best predictor of diet even after we controlled for the influence of body size and phylogeny. These results suggest that echolocation frequency and prey hearing exert more influence on the trophic structure of sympatric animalivorous bats than competition. Nonetheless, differential habitat use and sensory bias may also be major determinants of trophic structure because these are also correlated with frequencies of bat calls.

CRYPTIC SPECIES IN AN INSECTIVOROUS BAT, SCOTOPHILUS DINGANII

Abstract In recent years many cryptic bat species have been unmasked by differences in their echolocation calls. The yellow house bat (Scotophilus dinganii) is 1 of 3 species of Scotophilus currently described in southern Africa and is distinguished from the other 2 species by its size and yellow venter. Here we use genetic, morphological, and echolocation call data to show the existence of a cryptic species. We found that S. dinganii consists of 2 forms, one that uses a peak echolocation frequency of 44 kHz and the other a peak frequency of 33 kHz. Both forms have yellow venters. The 44-kHz phonic type is up to 15% smaller than the 33-kHz phonic type and differed genetically by an average cytochrome-b (Cytb) sequence divergence of 3.3%. Furthermore, combined phylogenetic analyses of Cytb and control region sequences indicate that the 2 phonic types are reciprocally monophyletic, suggesting that they are sibling species.

Correlated genetic and ecological diversification in a widespread southern African horseshoe bat.

The analysis of molecular data within a historical biogeographical framework, coupled with ecological characteristics can provide insight into the processes driving diversification. Here we assess the genetic and ecological diversity within a widespread horseshoe bat Rhinolophus clivosus sensu lato with specific emphasis on the southern African representatives which, although not currently recognized, were previously described as a separate species R. geoffroyi comprising four subspecies. Sequence divergence estimates of the mtDNA control region show that the southern African representatives of R. clivosus s.l. are as distinct from samples further north in Africa than they are from R. ferrumequinum, the sister-species to R. clivosus. Within South Africa, five genetically supported geographic groups exist and these groups are corroborated by echolocation and wing morphology data. The groups loosely correspond to the distributions of the previously defined subspecies and Maxent modelling shows a strong correlation between the detected groups and ecoregions. Based on molecular clock calibrations, it is evident that climatic cycling and related vegetation changes during the Quaternary may have facilitated diversification both genetically and ecologically.

A recent inventory of the bats of Mozambique with documentation of seven new species for the country

The bat fauna of Mozambique is poorly documented. We conducted a series of inventories across the country between 2005 and 2009, resulting in the identification of 50 species from 41 sites. Of these, seven species represent new national records that increase the country total to 67 species. These data include results from the first detailed surveys across northern Mozambique, over an area representing almost 50% of the country. We detail information on new distribution records and measurements of these specimens. Special attention is paid to the Rhinolophidae, because these include several taxa that are currently in a state of taxonomic confusion. Furthermore, we also present some notes on taxonomy, ecology and echolocation calls. Finally, we combine modelled distributions to present predicted species richness across the country. Species richness was lowest across the coastal plain, to the east and far north, and is predicted to increase in association with rising altitude and higher topographic unevenness of the landscape.

Do deterministic processes influence the phenotypic patterns of animalivorous bat ensembles at urban rivers

Although urbanization is perhaps the most damaging, persistent, and rapidly expanding form of anthropogenic pressure on natural ecosystems, data on the patterns and processes of sympatric bat species in urban landscapes are relatively scant. We quantified the packing and dispersion of sympatric animalivorous bats based on flight and echolocation parameters at two urban rivers in Durban, South Africa. We used null models to test if the observed phenotypic patterns deviated significantly from the random patterns expected in the absence of competition or prey defences at ensemble and functional group scales. As we predicted, species packing increased in the species-rich ensemble comprising many morphologically similar species that grouped together, with a few morphologically distinct species dispersed further away. Furthermore, we found evidence that competition influenced flight patterns of the open-air bats at the species-rich river ensemble, and prey defences influenced echolocation patterns of coexisting bats at the ensemble and functional group scales. However, non-deterministic processes such as habitat structure and the physics of sound and flight probably mediated these deterministic processes to influence the phenotypic structure of sympatric bats in urban landscapes.

Haematological and genotoxic responses in an urban adapter, the banana bat, foraging at wastewater treatment works

Wastewater Treatment Works (WWTWs) are a ubiquitous feature of the urban landscape. The Banana Bat, Neoromicia nana specifically exploits the high abundance of chironomid midge prey available at WWTWs but these populations also have higher levels of non-essential metals (Cd, Cr and Ni) in their tissues than bats foraging at unpolluted sites. Pollutant exposure may elicit primary physiological responses such as DNA damage and haematological changes. We investigated whether pollutant exposure from foraging at WWTWs impacts haematological and genotoxic parameters in N. nana. We compared four measures of haematological/genotoxic damage between N. nana foraging at three WWTWs and two unpolluted sites located in KwaZulu-Natal, South Africa: DNA damage measured by the Comet assay, total antioxidant capacity as indicated by the FRAP assay, chromosomal aberration indicated by micronuclei formation and blood oxygen capacity based on haematocrits. There was significantly higher DNA damage in N. nana at WWTWs than in bats from unpolluted sites, suggesting inadequate repair to double stranded DNA breaks. In addition, WWTW bats had a significantly lower antioxidant capacity than bats from unpolluted sites. This suggests that bats at WWTWs may have a diminished capacity to cope with the excess reactive oxidative species (ROS) produced from pollutants such as metals. There was no increase in micronucleus frequency in WWTW bats, indicating that cellular functioning has not yet been disrupted by chemical exposure. Haematocrits, however, were significantly higher in WWTW bats, possibly due to erythrocyte production in response to certain pollutants. Thus, effects of pollutant exposure in bats foraging at WWTWs elicit sub-lethal haematological and genotoxic responses which may pose serious long-term risks. This provides evidence that WWTWs, that are aimed to remove pollutants from the environment, can themselves act as a source of contamination and pose a threat to animals exploiting these habitats.

Diversity of Bats in the Soutpansberg and Blouberg Mountains of Northern South Africa: Complementarity of Acoustic and Non-Acoustic Survey Methods

We surveyed bats at 30 localities in the Soutpansberg and Blouberg Mountains within the newly proclaimed Vhembe Biosphere Reserve (VBR) of northern South Africa, based on ANABAT acoustic recordings (63 nights) conducted in parallel with captures of 260 individuals from harp traps (29 trap-nights) and mist nets (54 trap-nights), and searches of ten day-roosts and two night-roosts. Twenty-four species of bats were captured, or positively identified from roosts, out of 44 species previously recorded for the VBR. For those species captured during the study and one additional commonly recorded species, Chaerephon ansorgei, which was not captured, we compiled a library of ANABAT call parameters for reference calls, based on released bats or bats emerging from known-species roosts. Reference calls were obtained from the study area where possible, or from the closest possible site in the savanna region of southeastern Africa. Using principal component analysis and plots of frequency histograms of selected parameters, we investigated the extent to which reference calls of different species could be distinguished on call parameters. Complete separation was obtained for most species but certain species-pairs or trios showed overlap, particularly amongst molossid bats. Accurate identification of unknown calls was complicated by natural intraspecific variation in echolocation call structure due to habitat and behaviour in our species-rich study area. We advocate a conservative approach whereby species-pairs or groups with overlapping calls are treated as single ‘species’. Such underestimation can be partly corrected using rarefaction approaches, as illustrated by data collected from Blouberg Nature Reserve. Particularly when surveying bats in species-rich areas such as the eastern savannas of southern Africa, both acoustic and capture-based surveys are necessary to accurately estimate true species richness. From our capture data and roost searches, we recorded nine to 14 species at four west—east, grouped localities defined by this study. Adding acoustic data using a conservative approach to classify overlapping species-pairs or trios, we obtained minimum richness estimates of 15 to 21 species, values which were close to those predicted by a recent macro-ecological model. We found no evidence for a west—east increase in richness with increasing precipitation as predicted by coarse-scale macroecological predictions.

Cross-species chromosome painting in bats from Madagascar: the contribution of Myzopodidae to revealing ancestral syntenies in Chiroptera

The chiropteran fauna of Madagascar comprises eight of the 19 recognized families of bats, including the endemic Myzopodidae. While recent systematic studies of Malagasy bats have contributed to our understanding of the morphological and genetic diversity of the island’s fauna, little is known about their cytosystematics. Here we investigate karyotypic relationships among four species, representing four families of Chiroptera endemic to the Malagasy region using cross-species chromosome painting with painting probes of Myotis myotis: Myzopodidae (Myzopoda aurita, 2n = 26), Molossidae (Mormopterus jugularis, 2n = 48), Miniopteridae (Miniopterus griveaudi, 2n = 46), and Vespertilionidae (Myotis goudoti, 2n = 44). This study represents the first time a member of the family Myzopodidae has been investigated using chromosome painting. Painting probes of M. myotis were used to delimit 29, 24, 23, and 22 homologous chromosomal segments in the genomes of M. aurita, M. jugularis, M. griveaudi, and M. goudoti, respectively. Comparison of GTG-banded homologous chromosomes/chromosomal segments among the four species revealed the genome of M. aurita has been structured through 14 fusions of chromosomes and chromosomal segments of M. myotis chromosomes leading to a karyotype consisting solely of bi-armed chromosomes. In addition, chromosome painting revealed a novel X-autosome translocation in M. aurita. Comparison of our results with published chromosome maps provided further evidence for karyotypic conservatism within the genera Mormopterus, Miniopterus, and Myotis. Mapping of chromosomal rearrangements onto a molecular consensus phylogeny revealed ancestral syntenies shared between Myzopoda and other bat species of the infraorders Pteropodiformes and Vespertilioniformes. Our study provides further evidence for the involvement of Robertsonian (Rb) translocations and fusions/fissions in chromosomal evolution within Chiroptera.