MAMMALIAN BIOLOGY

A review of the diet of the common vampire bat () in the context of anthropogenic change
Brown N and Escobar LE
The common vampire bat () maintains a diverse, sanguivorous diet, utilizing a broad range of prey taxa. As anthropogenic change alters the distribution of this species, shifts in predator-prey interactions are expected. Understanding prey richness and patterns of prey selection is, thus, increasingly informative from ecological, epidemiological, and economic perspectives. We reviewed diet and assessed the geographical, taxonomical, and behavioral features to find 63 vertebrate species within 21 orders and 45 families constitute prey, including suitable host species in regions of invasion outside ' range. Rodentia contained the largest number of species utilized by , though cattle were the most commonly reported prey source, likely linked to the high availability of livestock and visibility of bite wounds compared to wildlife. Additionally, there was tendency to predate upon species with diurnal activity and social behavior, potentially facilitating convenient and nocturnal predation. Our review highlights the dietary heterogeneity of across its distribution. We define as a generalist predator, or parasite, depending on the ecological definition of its symbiont roles in an ecosystem (i.e., lethal vs. non-lethal blood consumption). In view of the eminent role of in rabies virus transmission and its range expansion, an understanding of its ecology would benefit public health, wildlife management, and agriculture.
Exploring (Rodentia, Muridae) as a possible species complex using geometric morphometrics on dental morphology
Hulme-Beaman A, Cucchi T, Evin A, Searle JB and Dobney K
Taxonomic uncertainties in the genus persist due to among-species morphological conservatism coupled with within-species environmental variation in morphology. As a result, this genus contains a number of possible cryptic species. One important example can be found in , where morphological studies indicate it is a possible species complex. Genetic studies of (limited to analysis of mitochondrial DNA) have been inconclusive, but do indicate such subdivision. Here we use geometric morphometrics to explore this possible species complex by analysing the dental traits of 48 specimens from New Guinea and neighbouring regions. We find separate molar morphologies for Bougainsville Island, central New Guinea and west New Guinea which cannot be easily explained by different environmental factors (climate, precipitation and altitude), strongly suggesting the existence of a number of evolutionarily distinct taxa within what is currently called thus supporting previous suggestions that is a species complex. Our findings demonstrate the potential of advanced morphological analyses in identifying separate species, contrary to the claims of morphological conservatism. Future analyses should combine geometric morphometrics with genetic analyses over the species range and include sub-fossil specimens from the Bismarck archipelago and Solomon Islands to resolve the evolutionary history of .
Original biological and ecological data on the endemic Chinese jumping mouse Eozapus setchuanus (Pousargues, 1896)
Quéré JP, Raoul F, Aniskin V, Durette-Desset MC and Giraudoux P
Effect of sex and reproductive status on the immunity of the temperate bat
Ruoss S, Becker NI, Otto MS, Czirják GÁ and Encarnação JA
Studies of immunity in bat species are rare. However, it is important to determine immunological variations to identify factors influencing the health status of these endangered mammals from an evolutionary, ecological, conservation, and public health point of view. Immunity is highly variable and can be influenced by both internal (e.g. hormone levels, energy demand) and external factors (e.g. pathogens, climate). As bats have some peculiar ecological, energetic, and putative immunological characteristics, they are outstanding study organisms for ecoimmunological studies. We tested if (i) female bats have a higher immunity than males similar to most other mammalian species and (ii) individuals differ according to their energy demand (e.g. reproductive status). To study these questions, we sampled female and male with different reproductive states and estimated their bacterial killing activity, hemolysis/hemagglutination titer, immunoglobulin G (IgG) concentration, and total and differential white blood cell counts. These methods characterize the cellular and humoral branches of both the adaptive and the innate immune responses of these individuals. Reproductively active males had lower cellular immunity compared to non-reproductive individuals. Pregnant females had increased IgG concentrations while hemolysis was enhanced during lactation. No clear trade-off between immunity and reproduction was found; instead immunity of males and female bats seems to be modulated differently due to varying hormonal and energetic states. Our data suggest that both adaptive and innate immunity as well as individual differences (i.e. sex and reproductive state) need to be considered to get a comprehensive overall picture of immunity in wild mammals.
Canine distemper virus may affect European wild cat populations in Central Spain
Candela MG, Pardavila X, Ortega N, Lamosa A, Mangas JG and Martínez-Carrasco C
The main objective of this brief communication is to inform about the exposure to certain pathogens of interest for mesocarnivores in wildcats () that inhabit a human-domestic-wild ecotone located in a Natural Park (Serranía de Cuenca, Central Spain). Blood and mucosal swabs (nasal, conjunctival and rectal) samples were collected from nine alive animals to detect canine distemper virus (CDV), parvovirus (CPV/FPV), feline leukaemia virus (FeLV), feline coronavirus (FCoV), feline immunodeficiency virus (FIV), , and ELISA, immunochromatograpy, microscopy agglutination test and PCR assays were used. The results show the first worldwide detection of exposure of wildcats to L. (3 positive/9 analysed) and the first detection of exposure to CVD (7/9), of carriers ofC (2/9) and of fecal spreading of CPV-FPV (2/9) in wildcats in Spain. Exposure to T. and CPV-FPV was detected in 5 of the 9 wildcats analysed, and to FelV in 4 of 9. No FIV, FCoV, and were detected. The results reveal the circulation of pathogens among the wildcat population studied, but more vigilance is needed for an accurate assessment of the impact of these pathogens on the health status of this population.
Research trends on bats in China: A twenty-first century review
Feijó A, Wang Y, Sun J, Li F, Wen Z, Ge D, Xia L and Yang Q
In this century, China has sustained unparalleled economic development, leading to exponentially growing investments in scientific research. Yet, the demand for research-funding is large and tracing the current knowledge is a key step to define priority research topics. In this same span, studies on bats in China have uncovered an overlooked diversity and revealed novelties in bats' evolutionary history and life-history aspects. All this 21st-century knowledge, however, is scattered and a large part is concealed from most of the international scientific community in Mandarin-language articles. Here, we summarize the post-millennium (2000-2017) research on bats in China and point out trends and future directions based on neglected topics, groups, and regions. In addition, we provide an up-to-date list of bat species in China. We retrieved 594 publications related to bats in China, nearly half were written in Mandarin. At least 147 bat species are present in China, which places it among the most bat-rich countries in the world. There was a significant positive trend on the number of publications, from 12.5 annual average in 2000-2005 to 46.5 in recent years, reflecting the Chinese economic-scientific development in this century. We found marked taxonomic and spatial biases. Half of the studies in this century focused on , and , and the southern and eastern provinces were the most studied. Systematic/taxonomy and Ecology were the predominant topics post-millennium, whereas only 10 articles have clear conservation-driven goals. Our review shows that the majority of studies were focused on the least concern, cave-dweller species, and on bat-rich provinces. Future projects should address the effects of human-modified landscapes on bat community to define proper conservation actions. We discuss some priority actions and projects that will help to enhance bat protection in China.
Patterns of activity rhythms of invasive coypus inferred through camera-trapping
Mori E, Andreoni A, Cecere F, Magi M and Lazzeri L
Studies on activity rhythms are pivotal for the management of invasive alien species, as they provide basic insights into species basic ecology and may increase the success of control programs. The coypu , introduced from South America for fur farms, has become one of the most invasive rodents in Europe. Introduced coypus may affect crop productions, as well as natural vegetation and the breeding success of wading birds. In this study, we examined activity data collected through intensive camera-trapping in three Italian areas, including two natural areas in Northern and Central Italy, and a suburban area in Central Italy. Coypus were mostly diurnal in areas characterised by low predator pressure and, at night, they are mostly active in bright moonlight. Conversely, where predators, human pressure or numerical control programmes are present, coypus remarkably shift their behaviour towards crepuscular and night hours. In these last areas, nocturnal activity increased as moonlight decreased, possibly to reduce predation risk or encounters with humans. Where winter temperature are low, diurnal habits may have developed as a physiological adaptation and a strategy to preserve energy, potentially achieving a cost/effective thermal balance.
First evaluation of the population structure, genetic diversity and landscape connectivity of the Endangered Arabian tahr
Ross S, Costanzi JM, Al Jahdhami M, Al Rawahi H, Ghazali M and Senn H
The Arabian tahr () occurs only in the mountains of northern Oman and the United Arab Emirates. The species is classified as Endangered due to its small declining population. In this study, we combined genetic and landscape ecology techniques in order to inform landscape scale conservation and genetic management of Arabian tahr. Using 540 base pairs of mitochondrial control region in a dataset of 53 samples, we found eight haplotypes, which fell into two haplogroups. Population genetic analysis using a panel of 14 microsatellite loci also showed a weak, but significant division. Analyses of landscape connectivity supported the genetic results showing poor connectivity between populations in the far south of the study area and those in the north. The most likely location of corridors connecting Arabian tahr populations were identified. Many corridors between tahr populations are impeded by multi-lane highways and restoration of these connections is required to maintain population viability of Arabian tahr. Owing to limited genetic samples outside of Wadi Sareen, further sampling is needed to elucidate both mtDNA and the nuclear structure of Arabian tahr more fully. Our study provides a toolkit that may be used for future genetic and connectivity monitoring of the Arabian tahr population.
Insular dwarfism in horses from the Aegean Sea and the Japanese archipelago
Ming KM, Le Verger K, Geiger M, Schmelzle T, Georgalis GL, Shimbo G, Sasaki M, Ohdachi SD and Sánchez-Villagra MR
The horse () varieties from Skyros and Rhodes islands (Greece) in the Aegean archipelago are extremely small, reaching shoulder heights of only about 1 m. Furthermore, the Japanese archipelago is home to eight small, native horse breeds. We investigated the evolutionary morphology and provided a review of historical documentations of these horses of cultural interest in Greece and Japan, thus providing a comparison of the independent evolution of small size in islands. We integrate cranial data from historical literature with data from newly gathered and curated skulls and analyse a measurement dataset featuring various domestic and mainland horse breeds and varieties. We use non-invasive imaging to study and measure 3D models of the bony labyrinth, housing the inner ear, and the braincase endocast. When considering the effects of allometry by regressing each PC1 scores (for each set of measurements) with the cranial geometric mean from linear measurements as a body size proxy, we show that size explains a large amount of the shape variation in horse crania, the bony labyrinths and brain endocasts. We found high intrabreed variation in all the analysed datasets. Globally, there are at least 30 distinct horse populations on islands, offering the chance to further study processes of convergence in morphological divergence and evaluate the effect of drift and the environment.
No short-term effect of handling and capture stress on immune responses of bats assessed by bacterial killing assay
Strobel S, Becker NI and Encarnação JA
Ecoimmunology of wild animals becomes increasingly important. However, there are methodical limitations, especially when working on small mammals, e.g. small sample volume and acute stress associated with capture, handling and sampling that can influence immune parameters. The plasma bacterial killing assay measures innate humoral immune responses, mainly complement activity. It is a powerful tool with many methodical advantages. To avoid investigation of artefacts in future ecoimmunological studies the influence of acute stress on the bacterial killing activity was assessed. Bats (, = 9) were repeatedly sampled in three time intervals up to 97 min after capture. Bacterial killing activity against was measured using a microplate absorbance reader. Bacterial killing activity was not influenced by capture, handling and sampling. Hence, released stress hormones did not affect circulating complement activity. To conclude, the plasma bacterial killing assay is reliable and efficient ecoimmunological tool in wildlife studies even of small mammals.
Bat selfies: photographic surveys of flying bats
Rydell J, Russo D, Sewell P, Seamark ECJ, Francis CM, Fenton SL and Fenton MB
The recent pandemic and other environmental concerns have resulted in restrictions on research and surveys involving capture and handling bats. While acoustic surveys have been widely used as an alternative survey method, in this study, we show how photographic surveys can offer an important contribution to study and survey bats. We outline approaches, using high speed flash and automated trip beams to obtain photos of flying bats of sufficient quality for reliable identification of species. We show, through a series of examples of setups and photographs, that photography is effective for surveying bats at a variety of sites, where bats roost, drink, and forage. We note, however, that photographic surveys cannot replace capture in all situations. In addition, although photographing bats is less invasive than capturing them, it can involve disturbance, so we stress the importance of minimizing the impact of such operations on bats.
Multispecies facial detection for individual identification of wildlife: a case study across ursids
Clapham M, Miller E, Nguyen M and Van Horn RC
To address biodiversity decline in the era of big data, replicable methods of data processing are needed. Automated methods of individual identification (ID) via computer vision are valuable in conservation research and wildlife management. Rapid and systematic methods of image processing and analysis are fundamental to an ever-growing need for effective conservation research and practice. Bears (ursids) are an interesting test system for examining computer vision techniques for wildlife, as they have variable facial morphology, variable presence of individual markings, and are challenging to research and monitor. We leveraged existing imagery of bears living under human care to develop a multispecies bear face detector, a critical part of individual ID pipelines. We compared its performance across species and on a pre-existing wild brown bear dataset (), to examine the robustness of convolutional neural networks trained on animals under human care. Using the multispecies bear face detector and retrained sub-applications of , we prototyped an end-to-end individual ID pipeline for the declining Andean bear . Our multispecies face detector had an average precision of 0.91-1.00 across all eight bear species, was transferable to images of wild brown bears (AP = 0.93), and correctly identified individual Andean bears in 86% of test images. These preliminary results indicate that a multispecies-trained network can detect faces of a single species sufficiently to achieve high-performance individual classification, which could speed-up the transferability and application of automated individual ID to a wider range of taxa.
Gray squirrels consume anthropogenic food waste most often during winter
Rimbach R, Butler G, Gupte PR, Jäger J, Parker C and Pontzer H
Urban habitats provide wildlife with predictable, easily accessible and abundant food sources in the form of human food waste. Urban eastern gray squirrels () are commonly observed feeding in trash bins, but we lack data regarding the type, quantity and seasonal changes in food waste usage. We observed five trash bins on an urban university campus during four different observation periods. We recorded the time squirrels spent on and inside trash bins and type of retrieved food items. We also recorded ambient temperature, human presence and trash bin filling. Moreover, we determined changes in squirrel population density in a natural and three anthropogenic habitats during the same periods. Trash bins were fuller when human presence was higher. The higher human presence, the more squirrels went on and inside the bin, but there was no effect on number of retrieved food items. Trash bin usage by squirrels decreased when ambient temperature and bin filling increased. Most food items were retrieved during the coldest observation period, a period of high human presence, and the majority of retrieved food items were starchy foods (e.g., bread, French fries). The relationship between the number of squirrels observed along transects and a measure of urbanization, the normalized difference built-up index, was negative in periods with high ambient temperatures and positive in periods with low ambient temperatures, indicating winter may be less challenging in urban areas, likely facilitated by the availability of anthropogenic food sources, allowing a higher level of activity throughout winter.
The value of individual identification in studies of free-living hyenas and aardwolves
Spagnuolo OSB, Lemerle MA, Holekamp KE and Wiesel I
From population estimates to social evolution, much of our understanding of the family Hyaenidae is drawn from studies of known individuals. The extant species in this family (spotted hyenas, , brown hyenas, , striped hyenas, , and aardwolves, ) are behaviorally diverse, presenting an equally diverse set of logistical constraints on capturing and marking individuals. All these species are individually identifiable by their coat patterns, providing a useful alternative to man-made markings. Many studies have demonstrated the utility of this method in answering a wide range of research questions across all four species, with some employing a creative fusion of techniques. Despite its pervasiveness in basic research on hyenas and aardwolves, individual identification has rarely been applied to the conservation and management of these species. We argue that individual identification using naturally occurring markings in applied research could prove immensely helpful, as this could further improve accuracy of density estimates, reveal characteristics of suitable habitat, identify threats to population persistence, and help to identify individual problem animals.
Assessing social structure: a data-driven approach to define associations between individuals
Tavares SB, Whitehead H and Doniol-Valcroze T
Our interpretation of animal social structures is inherently dependent on our ability to define association criteria that are biologically meaningful. However, association thresholds are often based upon generalized preconceptions of a species' social behaviour, and the impact of using these arbitrary definitions has been largely overlooked. In this study we suggest a probability-based method for defining association thresholds using lagged identification rates on photographic records of identifiable individuals. This technique uses a simple model of emigration/immigration from photographable clusters to identify the time-dependent lag value between identifications of two individuals that corresponds to approximately 75% probability of being in close spatial proximity and likely associating. This lag value is then used as the threshold to define associations for social analyses. We applied the technique to a dataset of northern resident killer whales () in the Northeast Pacific and tested its performance against two arbitrary thresholds. The probabilistic association maximized the variation in association strengths at different levels of the social structure, in line with known social patterns in this population. Furthermore, variability in inferred social structure metrics generated by different association criteria highlighted the consequential effect of choosing arbitrary thresholds. Data-driven association thresholds are a promising approach to study populations without the need to subjectively define associations in the field, especially in societies with prominent fission-fusion dynamics. This method is applicable to any dataset of sequential identifications where it can be assumed that associated individuals will tend to be identified in close proximity.
Sensitivity of bats to urbanization: a review
Russo D and Ancillotto L
In this article we review the current knowledge of the effects of urban expansion on bats and assess the potential of these mammals as bioindicators of urbanization. The response of bats to this process is highly species-specific: some species tolerate urban habitat or are even favoured by its roosting or foraging opportunities, others are affected by the loss or fragmentation of key natural habitat, or by the physical and chemical pollution associated with urbanization. Species responses generally translate into altered community structures, with few markedly dominating species. We propose different hypothetical models of bat fitness along an urbanization gradient and discuss why bat population density may not be an effective fitness proxy to assess the reactions of these mammals to urban expansion. We also suggest that urban habitat may act as an ecological trap even for apparently synurbic species. Overall, bat sensitivity to urbanization makes these mammals promising candidates to track the effects of this process of land use change on the biota, but more studies, specifically tailored to explore this role, are needed.
Association patterns and community structure among female bottlenose dolphins: environmental, genetic and cultural factors
Marfurt SM, Allen SJ, Bizzozzero MR, Willems EP, King SL, Connor RC, Kopps AM, Wild S, Gerber L, Wittwer S and Krützen M
Social structuring from assortative associations may affect individual fitness, as well as population-level processes. Gaining a broader understanding of social structure can improve our knowledge of social evolution and inform wildlife conservation. We investigated association patterns and community structure of female Indo-Pacific bottlenose dolphins () in Shark Bay, Western Australia, assessing the role of kinship, shared culturally transmitted foraging techniques, and habitat similarity based on water depth. Our results indicated that associations are influenced by a combination of uni- and biparental relatedness, cultural behaviour and habitat similarity, as these were positively correlated with a measure of dyadic association. These findings were matched in a community level analysis. Members of the same communities overwhelmingly shared the same habitat and foraging techniques, demonstrating a strong homophilic tendency. Both uni- and biparental relatedness between dyads were higher within than between communities. Our results illustrate that intraspecific variation in sociality in bottlenose dolphins is influenced by a complex combination of genetic, cultural, and environmental aspects.
Preliminary evidence for a forestomach washing mechanism in llamas ()
Hatt JM, Codron D, Richter H, Kircher PR, Hummel J and Clauss M
Dust and grit are ingested by herbivores in their natural habitats along with the plants that represent their selected diet. Among the functions of the rumen, a washing of ingesta from adhering dust and grit has recently been demonstrated. The putative consequence is a less strenuous wear on ruminant teeth by external abrasives during rumination. The same function should theoretically apply to camelids, but has not been investigated so far. We fed six llamas () a diet of grass hay and a lucerne-based pelleted food in which fine sand had been included at about 8% of ingredients, for ad libitum consumption for 6 weeks. Subsequently, animals were slaughtered and content of the different sections of the gastrointestinal tract was sampled for the analysis of dry matter (DM), total ash, and acid detergent insoluble ash (ADIA, a measure for silica). Additionally, two of the animals were subjected to whole-body computer tomography (CT) after death in the natural sternal resting position. No clinical problems or macroscopic changes in the faeces were observed during the experimental period. The results indicate an accumulation of ADIA in the C3 compartment of the stomach complex, in particular in the posterior portion that is the equivalent of the abomasum in ruminants. By contrast, contents of the C1, from which material is recruited for regurgitation and rumination, were depleted of ADIA, indicating that the contents had largely been washed free of sand. The washing effect is an unavoidable side effect of the flotation- and sedimentation-based sorting mechanisms in the ruminant and the camelid forestomachs. In theory, this should allow ruminants and camelids to live in similar habitats as nonruminant herbivores at lower degrees of hypsodonty.
Digestive anatomy and diet of free-ranging maned wolf ()
Silva BC, de Oliveira LA, Clauss M, Costa CG, de Oliveira Marques Alexandre L and Duque-Correa MJ
The maned wolf () is the largest of the currently extant ten species of South American canids and is a monotypic taxon in the genus , currently classified as Near Threatened by the IUCN. Here we report the anatomy of the gastrointestinal tract (GIT) of 12 free-ranging maned wolves (10 adults, six females, four males, and two juvenile males), nutritional analyses of the gastrointestinal tract (stomach, small, and large intestine) of eight individuals (six females and two males), and the macroscopical examination of the stomach contents of eight individuals (four adult females, two adult males, and two juvenile males). The general anatomy and the dimensions of the maned wolf`s GIT resembled that of other canids. The results of the dietary analyses reported in this study are similar to previously reported data for the species, confirming its omnivorous nature. Vertebrates were found in all stomachs, representing 42.5% of the total dietary mass. Vegetable material was also present in all stomachs, accounting for half of the total dietary mass (50.5%). Anthropogenic material, including cooked rice, glass, and ceramic fragments, were retrieved from the stomach of one individual; such opportunistic feeding behavior has been previously reported. When compared to other Carnivora species classified as omnivores, including the red fox () and the raccoon dog (), these 'omnivorous' carnivores ingest distinctively higher levels of fiber compared to purely faunivorous Carnivora. This information might be important for feeding these species in settings.