Bat breath reveals metabolic substrate use in free-ranging vampires

We analysed the stable carbon isotope ratio in exhaled CO₂ (δ¹³C_breath) of free-ranging vampires to assess the type of metabolized substrate (endogenous or exogenous substrate) and its origin, i.e. whether the carbon atoms came from a C₄ food web (grass and cattle) or the C₃ food web in which they were captured (a rainforest remnant and its mammals). For an improved understanding of factors influencing the δ¹³C_breath of vampires, we conducted feeding experiments with captive animals. The mean δ¹³C_breath of starved bats was depleted in ¹³C in relation to the diet by 4.6‰ (n = 10). Once fed with blood, δ¹³C_breath levelled off within a short time approximately 2.2‰ above the stable carbon isotope signature of the diet. The median time required to exchange 50% of the carbon atoms in exhaled CO₂ with carbon atoms from the ingested blood was 18.6 min (mean 29.5 ± 19.0 min, n = 5). The average δ¹³C of wing membrane and fur in free-ranging vampire bats suggested that bats almost exclusively foraged for cattle blood during the past weeks. The δ¹³C_breath of the same bats averaged −19.1‰. Given that all free-ranging vampires were starving and that the δ¹³C of cattle was more in enriched in ¹³C by 5–6‰ than the δ¹³C_breath of vampires, we conclude that the vampire bats of our study metabolised fat that was predominantly built from carbon atoms originating from cattle blood. Since δ¹³C of wing membrane and fur integrates over weeks and months respectively and δ¹³C_breath over hours and days, we also conclude that vampire bats of the studied population consistently ignored rainforest mammals and chose cattle as their prey during and prior to our study.     

Studying Animal Diets In Situ Using Portable Stable Isotope Analyzers

I assessed the usefulness of a portable stable isotope analyzer for assigning animals to food chains of tropical ecosystems. Based on the stable carbon isotope ratio of the animals' breath (δ¹³C _breath ), it was possible to distinguish between the isotopically distinct food chains of fruit-eating bats and blood-eating vampire bats. Portable instruments for the analysis of δ¹³C _breath may improve our ability to quantify animal diets, because they are accurate and cheap, and most importantly they can be used in situ .     

Social Grooming in Bats: Are Vampire Bats Exceptional?

Evidence for long-term cooperative relationships comes from several social birds and mammals. Vampire bats demonstrate cooperative social bonds, and like primates, they maintain these bonds through social grooming. It is unclear, however, to what extent vampires are special among bats in this regard. We compared social grooming rates of common vampire bats Desmodus rotundus and four other group-living bats, Artibeus jamaicensis, Carollia perspicillata, Eidolon helvum and Rousettus aegyptiacus, under the same captive conditions of fixed association and no ectoparasites. We conducted 13 focal sampling sessions for each combination of sex and species, for a total of 1560 presence/absence observations per species. We observed evidence for social grooming in all species, but social grooming rates were on average 14 times higher in vampire bats than in other species. Self-grooming rates did not differ. Vampire bats spent 3.7% of their awake time social grooming (95% CI = 1.5–6.3%), whereas bats of the other species spent 0.1–0.5% of their awake time social grooming. Together with past data, this result supports the hypothesis that the elevated social grooming rate in the vampire bat is an adaptive trait, linked to their social bonding and unique regurgitated food sharing behavior.     

Reciprocal altruism in bats and other mammals

In this paper five conditions are specified which must be met before reciprocal altruism, rather than kin selection, should be invoked. Four purported mammalian examples— social grooming in coati, cluster position in roosting pallid bats, information exchange among greater spear-nosed bats, and blood regurgitation among vampire bats—are examined to determine if reciprocal altruism is necessary to plausibly explain each situation. Results from a computer simulation which apportions the relative selective advantage of vampire bat food sharing to kin selection and reciprocal altruism are then presented. The results demonstrate that the increase in individual survivorship due to reciprocal food sharing events in this species provides a greater increase in inclusive fitness than can be attributed to aiding relatives. This analysis suggests that reciprocal altruism can be selectively more important than kin selection when altruistic behaviors in a relatively large social group occur frequently and provide a major fitness benefit to the recipient even when that recipient is related to the donor.     

Non-kin cooperation in bats

Many bats are extremely social. In some cases, individuals remain together for years or even decades and engage in mutually beneficial behaviours among non-related individuals. Here, we summarize ways in which unrelated bats cooperate while roosting, foraging, feeding or caring for offspring. For each situation, we ask if cooperation involves an investment, and if so, what mechanisms might ensure a return. While some cooperative outcomes are likely a by-product of selfish behaviour as they are in many other vertebrates, we explain how cooperative investments can occur in several situations and are particularly evident in food sharing among common vampire bats (Desmodus rotundus) and alloparental care by greater spear-nosed bats (Phyllostomus hastatus). Fieldwork and experiments on vampire bats indicate that sharing blood with non-kin expands the number of possible donors beyond kin and promotes reciprocal help by strengthening long-term social bonds. Similarly, more than 25 years of recapture data and field observations of greater spear-nosed bats reveal multiple cooperative investments occurring within stable groups of non-kin. These studies illustrate how bats can serve as models for understanding how cooperation is regulated in social vertebrates.     

Bioecological Drivers of Rabies Virus Circulation in a Neotropical Bat Community

Introduction

In addition to the commonly accepted importance of the vampire bat in the maintenance and transmission of the rabies virus (RABV) in South America, RABV infection of other species is widely evidenced, challenging their role in the viral cycle.

Methodology / Principles findings

To identify the bioecological drivers of RABV circulation in neotropical bat communities, we conducted a molecular and serological survey on almost 1,000 bats from 30 species, and a 4-year longitudinal survey in two colonies of vampire bats in French Guiana. RABV was molecularly detected in a common vampire and in a frugivorous bat. The sequences corresponded to haematophagous bat-related strains and were close to viruses circulating in the Brazilian Amazon region. Species’ seroprevalence ranged from 0 to 20%, and the risk of seropositivity was higher in bats with a haematophagous diet, living in monospecific colonies and in dense forests. The longitudinal survey showed substantial temporal fluctuations, with individual waves of seroconversions and waning immunity. The high prevalences observed in bat communities, in most habitats and in species that do not share the same microhabitats and bioecological patterns, the temporal variations, and a rather short period of detectable antibodies as observed in recaptured vampires suggest (i) frequent exposure of animals, (ii) an ability of the infected host to control and eliminate the virus, (iii) more relaxed modes of exposure between bats than the commonly assumed infection via direct contact with saliva of infected animals, all of which should be further investigated.

Conclusions / significance

We hypothesize that RABV circulation in French Guiana is mainly maintained in the pristine forest habitats that may provide sufficient food resources to allow vampire bats, the main prevalent species, to survive and RABV to be propagated. However, on the forest edge and in disturbed areas, human activities may induce more insidious effects such as defaunation. One of the ecological consequences is the disappearance of resources for tertiary or secondary consumers. Populations of vampires may then shift to alternative resources such as cattle, domestic animals and humans. Therefore, a good forest status, allowing both a dilution effect in highly rich bat communities and the maintenance of large populations of medium-sized and large mammals used as prey by vampires, should prevent their migration to anthropized areas.     

The Role of Fruits and Insects in the Nutrition of Frugivorous Bats: Evaluating the Use of Stable Isotope Models1

We estimated the relative contribution of fruits and insects as sources of dietary protein in two species of Neotropical frugivorous bats (Artibeus jamaicensis and Sturnira lilium) using stable carbon and nitrogen isotope analyses. An insectivorous species (Pteronotus parnellii) was also included for comparison. We found constant patterns in stable carbon and nitrogen isotope composition in blood that separated the two species of frugivorous bats from the insectivorous bat. When we used these isotopic values (combined with those of dietary fruits and insects) to estimate the percent contribution of fruits and insects to the diet of the bats, we obtained different results, depending on assumptions and model adopted. We tested models using both 8“N and 8′³C results simultaneously and separately and further used diet‐tissue fractionation factors of 3%o for nitrogen and 1 and 3.5%o for carbon. We found that a carbon‐based model with a diet‐blood enrichment factor of 3.5%o produced the most parsimonious results. The model estimated that A. jamaicensis and S. lilium obtained most of their protein requirements from fruits, whereas P. parnellii fed mostly on insects. No sexual or seasonal variations in the diet of the two frugivorous species were detected. We found no evidence that the diet of sexually active females differed from that of nonsexually active females in the two species of frugivorous bats. We suggest that future studies better define isotopic fractionation between diet and tissues of bats using captive rearing and controlled diets.     

Social foraging in vampire bats is predicted by long-term cooperative relationships

Stable social bonds in group-living animals can provide greater access to food. A striking example is that female vampire bats often regurgitate blood to socially bonded kin and nonkin that failed in their nightly hunt. Food-sharing relationships form via preferred associations and social grooming within roosts. However, it remains unclear whether these cooperative relationships extend beyond the roost. To evaluate if long-term cooperative relationships in vampire bats play a role in foraging, we tested if foraging encounters measured by proximity sensors could be explained by wild roosting proximity, kinship, or rates of co-feeding, social grooming, and food sharing during 21 months in captivity. We assessed evidence for 6 hypothetical scenarios of social foraging, ranging from individual to collective hunting. We found that closely bonded female vampire bats departed their roost separately, but often reunited far outside the roost. Repeating foraging encounters were predicted by within-roost association and histories of cooperation in captivity, even when accounting for kinship. Foraging bats demonstrated both affiliative and competitive interactions with different social calls linked to each interaction type. We suggest that social foraging could have implications for social evolution if “local” within-roost cooperation and “global” outside-roost competition enhances fitness interdependence between frequent roostmates.

A combination of captive experiments and proximity sensing in the wild show that social bonds in vampire bats that are typically defined by cooperative interactions within the roost also extend beyond the roost and may provide benefits during foraging.     

Food sharing in vampire bats: reciprocal help predicts donations more than relatedness or harassment

Common vampire bats often regurgitate food to roost-mates that fail to feed. The original explanation for this costly helping behaviour invoked both direct and indirect fitness benefits. Several authors have since suggested that food sharing is maintained solely by indirect fitness because non-kin food sharing could have resulted from kin recognition errors, indiscriminate altruism within groups, or harassment. To test these alternatives, we examined predictors of food-sharing decisions under controlled conditions of mixed relatedness and equal familiarity. Over a 2 year period, we individually fasted 20 vampire bats (Desmodus rotundus) and induced food sharing on 48 days. Surprisingly, donors initiated food sharing more often than recipients, which is inconsistent with harassment. Food received was the best predictor of food given across dyads, and 8.5 times more important than relatedness. Sixty-four per cent of sharing dyads were unrelated, approaching the 67 per cent expected if nepotism was absent. Consistent with social bonding, the food-sharing network was consistent and correlated with mutual allogrooming. Together with past work, these findings support the hypothesis that food sharing in vampire bats provides mutual direct fitness benefits, and is not explained solely by kin selection or harassment.     

Intranasal oxytocin increases social grooming and food sharing in the common vampire bat Desmodus rotundus

Intranasal oxytocin (OT) delivery has been used to non-invasively manipulate mammalian cooperative behavior. Such manipulations can potentially provide insight into both shared and species-specific mechanisms underlying cooperation. Vampire bats are remarkable for their high rates of allogrooming and the presence of regurgitated food sharing among adults. We administered intranasal OT to highly familiar captive vampire bats of varying relatedness to test for an effect on allogrooming and food sharing. We found that intranasal OT did not have a detectable effect on food-sharing occurrence, but it did increase the size of regurgitated food donations when controlling for dyad and amount of allogrooming. Intranasal OT in females increased the amount of allogrooming per partner and across all partners per trial, but not the number of partners. We also found that the peak effect of OT treatments occurred 30–50 min after administration, which is consistent with the reported latency for intranasal OT to affect relevant brain areas in rats and mice. Our results suggest that intranasal OT is a potential tool for influencing dyadic cooperative investments, but measuring prior social relationships may be necessary to interpret the results of hormonal manipulations of cooperative behavior and it may be difficult to alter partner choice in vampire bats using intranasal OT alone.     

Social benefits of non-kin food sharing by female vampire bats

Regurgitations of blood among vampire bats appear to benefit both direct and indirect fitness. To maximize inclusive fitness, reciprocal food sharing should occur among close kin. Why then do females with kin roost-mates help non-kin? We tested the hypothesis that helping non-kin increases a bat''s success at obtaining future donations by expanding its network of potential donors. On six occasions, we individually fasted 14 adult females and measured donations from 28 possible donors. Each female was fasted before, during and after a treatment period, when we prevented donations from past donors (including 10 close relatives) by simultaneously fasting or removing them. This experiment was designed to detect partner switching and yielded three main results. First, females received less food when we prevented donations from a past donor versus a control bat. Donors within a group are therefore not interchangeable. Second, the treatment increased the variance in donors'' contributions to food received by subjects, suggesting the possibility of alternative responses to a partner''s inability to reciprocate. Finally, bats that fed more non-kin in previous years had more donors and received more food during the treatment. These results indicate that a bat can expand its network of possible donors by helping non-kin.     

Trophic niche changes associated with habitat fragmentation in a Neotropical bat species

Habitat fragmentation could alter ecological traits including species trophic habits. Here, we used carbon and nitrogen stable isotope ratios to establish differences in isotopic niche width and food resource use between forest fragments and the continuous forest for the phyllostomid frugivorous bat Artibeus lituratus. Using mist nests, we captured bats from two forest fragments and two sites in continuous forest, and sampled from each individual captured three body tissues with contrasting turnover rates (skin, muscle, and liver). Samples were collected between February and March (austral summer) and between August and September (austral winter). In addition, in each sampling site and season we collected potential food resources (fruits and insects) consumed by our A. lituratus. Our findings indicate that A. lituratus had a predominantly omnivorous diet, with high consumption of insects during summer in forest fragments. The increasing consumption of insects in these fragments seems to have led to a wider isotopic niche, in relation to the continuous forest. Because A. lituratus is typically a seed disperser, changes in trophic habits in the forest fragments from frugivory to insectivory may diminish their role in forest regeneration. Abstract in Portuguese is available with online material.     

Stable isotopes in southern rockhopper penguins: foraging areas and sexual differences in the non-breeding period

Southern rockhopper penguins (Eudyptes chrysocome chrysocome) have experienced severe population declines across their distribution area, potentially in response to bottom-up effects following elevated sea surface temperatures, changes in the food web and prey availability. We conducted stable isotope analysis to compare trophic levels and distribution patterns in the non-breeding period over three consecutive years, and between males and females, using egg membranes, blood cells and feathers of parent birds. Tissues representing the non-breeding season had lower ??¹³C values than prey sampled around the Falklands and red blood cells from breeding rockhopper penguins. In contrast, ??¹⁵N values were higher in red blood cells from the end of winter compared to those from the breeding season and compared to feathers. This indicated that rockhopper penguins left the Falkland Island area in the non-breeding season and foraged either around Burdwood Bank further south, or over the Patagonian Shelf. In winter, only males took more prey of higher trophic level than females. Inter-annual differences in isotopic values partly correlated with sea surface temperatures. However, as prey isotope samples were collected only in 1?year, inter-annual differences in penguin isotopic values may result from different foraging sites, different prey choice or different isotopic baseline values. Our study highlights the potential for stable isotope analyses to detect seasonal and gender-specific differences in foraging areas and trophic levels, while stressing the need for more sampling of isotopic baseline data.     

The Conflict between Cheetahs and Humans on Namibian Farmland Elucidated by Stable Isotope Diet Analysis

Large areas of Namibia are covered by farmland, which is also used by game and predator species. Because it can cause conflicts with farmers when predators, such as cheetahs (Acinonyx jubatus), hunt livestock, we assessed whether livestock constitutes a significant part of the cheetah diet by analysing the stable isotope composition of blood and tissue samples of cheetahs and their potential prey species. According to isotopic similarities, we defined three isotopic categories of potential prey: members of a C4 food web with high δ¹⁵N values (gemsbok, cattle, springhare and guinea fowl) and those with low δ¹⁵N values (hartebeest, warthog), and members of a C3 food web, namely browsers (eland, kudu, springbok, steenbok and scrub hare). We quantified the trophic discrimination of heavy isotopes in cheetah muscle in 9 captive individuals and measured an enrichment for ¹⁵N (3.2‰) but not for ¹³C in relation to food. We captured 53 free-ranging cheetahs of which 23 were members of groups. Cheetahs of the same group were isotopically distinct from members of other groups, indicating that group members shared their prey. Solitary males (n = 21) and males in a bachelor groups (n = 11) fed mostly on hartebeest and warthogs, followed by browsers in case of solitary males, and by grazers with high δ¹⁵N values in case of bachelor groups. Female cheetahs (n = 9) predominantly fed on browsers and used also hartebeest and warthogs. Mixing models suggested that the isotopic prey category that included cattle was only important, if at all, for males living in bachelor groups. Stable isotope analysis of fur, muscle, red blood cells and blood plasma in 9 free-ranging cheetahs identified most individuals as isotopic specialists, focussing on isotopically distinct prey categories as their food.     

Social grooming in the common vampire bat,Desmodus rotundus

Grooming patterns among 65 common vampire bats in hollow tree day roosts were studied by behavioural sampling techniques during a 15-month period. Self-grooming occurred more than social grooming in response to ectoparasites since the proportion of time spent self-grooming and the amount of ectoparasite infestation covaried positively among tree roosts while the time spent grooming others was independent of roots and ectoparasite level. Rates of social grooming were not independent of the sex of participants due to infrequent social grooming by adult males. Two variables, the level of relatedness and a measure of roosting association, which previously were shown to predict food sharing by regurgitation, correlated positively with the rate of social grooming. Since social grooming occurred more often than expected before a regurgitation and correlated with regurgitation frequency, it is suggested that this behaviour facilitates identification of food sharing partners by enabling a grooming bat to monitor other animals' potential for giving or receiving blood.     

Vampire bats exhibit evolutionary reduction of bitter taste receptor genes common to other bats

The bitter taste serves as an important natural defence against the ingestion of poisonous foods and is thus believed to be indispensable in animals. However, vampire bats are obligate blood feeders that show a reduced behavioural response towards bitter-tasting compounds. To test whether bitter taste receptor genes (T2Rs) have been relaxed from selective constraint in vampire bats, we sampled all three vampire bat species and 11 non-vampire bats, and sequenced nine one-to-one orthologous T2Rs that are assumed to be functionally conserved in all bats. We generated 85 T2R sequences and found that vampire bats have a significantly greater percentage of pseudogenes than other bats. These results strongly suggest a relaxation of selective constraint and a reduction of bitter taste function in vampire bats. We also found that vampire bats retain many intact T2Rs, and that the taste signalling pathway gene Calhm1 remains complete and intact with strong functional constraint. These results suggest the presence of some bitter taste function in vampire bats, although it is not likely to play a major role in food selection. Together, our study suggests that the evolutionary reduction of bitter taste function in animals is more pervasive than previously believed, and highlights the importance of extra-oral functions of taste receptor genes.     

Effects of Sexual Dimorphism and Landscape Composition on the Trophic Behavior of Greater Prairie-Chicken

Partitioning of ecological niche is expected in lekking species that show marked sexual size dimorphism as a consequence of sex-specific ecological constraints. However, niche partitioning is uncertain in species with moderate sexual dimorphism. In addition, the ecological niche of a species may also be affected by landscape composition; particularly, agricultural fragmentation may greatly influence the trophic behavior of herbivores. We studied trophic niche variation in Greater Prairie-Chickens (Tympanuchus cupido), a grouse species that shows moderate sex-dimorphism. Greater Prairie-Chickens are native to tallgrass prairies of North America, although populations persist in less natural mosaics of cropland and native habitats. We used stable isotope analysis of carbon and nitrogen in blood, claws and feathers to assess seasonal differences in trophic niche breadth and individual specialization between male and female Greater Prairie-Chickens, and between birds living in continuous and fragmented landscapes. We found that females showed broader niches and higher individual specialization than males, especially in winter and autumn. However, differences between females and males were smaller in spring when birds converge at leks, suggesting that females and males may exhibit similar feeding behaviors during the lekking period. In addition, we found that birds living in native prairies showed greater annual trophic variability than conspecifics in agricultural mosaic landscapes. Native habitats may provide greater dietary diversity, resulting in greater diversity of feeding strategies.     

Inherent variation in stable isotope values and discrimination factors in two life stages of green turtles

Abstract We examine inherent variation in carbon and nitrogen stable isotope values of multiple soft tissues from a population of captive green turtles Chelonia mydas to determine the extent of isotopic variation due to individual differences in physiology. We compare the measured inherent variation in the captive population with the isotopic variation observed in a wild population of juvenile green turtles. Additionally, we measure diet-tissue discrimination factors to determine the offset that occurs between isotope values of the food source and four green turtle tissues. Tissue samples (epidermis, dermis, serum, and red blood cells) were collected from captive green turtles in two life stages (40 large juveniles and 30 adults) at the Cayman Turtle Farm, Grand Cayman, and analyzed for carbon and nitrogen stable isotopes. Multivariate normal models were fit to the isotope data, and the Bayesian Information Criterion was used for model selection. Inherent variation and discrimination factors differed among tissues and life stages. Inherent variation was found to make up a small portion of the isotopic variation measured in a wild population. Discrimination factors not only are tissue and life stage dependent but also appear to vary with diet and sea turtle species, thus highlighting the need for appropriate discrimination factors in dietary reconstructions and trophic-level estimations. Our measures of inherent variation will also be informative in field studies employing stable isotope analysis so that differences in diet or habitat are more accurately identified.     

Ectoparasite Raymondia lobulata infestation in relation to the reproductive cycle of its host--the greater false vampire bat Megaderma lyra

To study variation of infestations by the bat fly Raymondia lobulata (Diptera: Streblidae) on the greater false vampire bat Megaderma lyra (Chiroptera: Megadermatidae), we captured individual bats at their day roost in the south of India and recorded their rate of infestation continuously for a year. All examined bats (n = 72 individuals, 202 captures) were infested with parasites (n = 3,008). However, the recorded intensity of infestation (range 1-33) was gender-related and statistically higher in females than in males (F(1, 200) = 304.45, P < 0.001). Furthermore, pregnant and lactating females had greater parasite loads than non-reproductive females and males (F(1, 63) = 23.34, P < 0.001 and F(1, 37) = 78.07, P < 0.001, respectively). No significant differences were observed between males either during mating and non-mating periods or breeding and non-breeding seasons. Analysis of the relationship between parasite infestation and the reproductive status of bats revealed that pregnant and lactating females with pups were more vulnerable hosts for parasites. Our results also suggest a well-developed coevolutionary strategy for synchronized reproduction within the host-parasite relationship and add to our understanding of how host sex and reproductive status shape the dynamics of parasitism.