Karin Schneeberger

Reciprocal cooperation between unrelated rats depends on cost to donor and benefit to recipient

BackgroundAlthough evolutionary models of cooperation build on the intuition that costs of the donor and benefits to the receiver are the most general fundamental parameters, it is largely unknown how they affect the decision of animals to cooperate with an unrelated social partner. Here we test experimentally whether costs to the donor and need of the receiver decide about the amount of help provided by unrelated rats in an iterated prisoners dilemma game.ResultsFourteen unrelated Norway rats were alternately presented to a cooperative or defective partner for whom they could provide food via a mechanical apparatus. Direct costs for this task and the need of the receiver were manipulated in two separate experiments. Rats provided more food to cooperative partners than to defectors (direct reciprocity). The propensity to discriminate between helpful and non-helpful social partners was contingent on costs: An experimentally increased resistance in one Newton steps to pull food for the social partner reduced the help provided to defectors more strongly than the help returned to cooperators. Furthermore, test rats provided more help to hungry receivers that were light or in poor condition, which might suggest empathy, whereas this relationship was inverse when experimental partners were satiated.ConclusionsIn a prisoners dilemma situation rats seem to take effect of own costs and potential benefits to a receiver when deciding about helping a social partner, which confirms the predictions of reciprocal cooperation. Thus, factors that had been believed to be largely confined to human social behaviour apparently influence the behaviour of other social animals as well, despite widespread scepticism. Therefore our results shed new light on the biological basis of reciprocity.

Rain increases the energy cost of bat flight

Similar to insects, birds and pterosaurs, bats have evolved powered flight. But in contrast to other flying taxa, only bats are furry. Here, we asked whether flight is impaired when bat pelage and wing membranes get wet. We studied the metabolism of short flights in Carollia sowelli, a bat that is exposed to heavy and frequent rainfall in neotropical rainforests. We expected bats to encounter higher thermoregulatory costs, or to suffer from lowered aerodynamic properties when pelage and wing membranes catch moisture. Therefore, we predicted that wet bats face higher flight costs than dry ones. We quantified the flight metabolism in three treatments: dry bats, wet bats and no rain, wet bats and rain. Dry bats showed metabolic rates predicted by allometry. However, flight metabolism increased twofold when bats were wet, or when they were additionally exposed to rain. We conclude that bats may not avoid rain only because of sensory constraints imposed by raindrops on echolocation, but also because of energetic constraints.

Inflammatory challenge increases measures of oxidative stress in a free-ranging, long-lived mammal

SUMMARY Oxidative stress – the imbalance between reactive oxygen species (ROS) and neutralising antioxidants – has been under debate as the main cause of ageing in aerobial organisms. The level of ROS should increase during infection as part of the activation of an immune response, leading to oxidative damage to proteins, lipids and DNA. Yet, it is unknown how long-lived organisms, especially mammals, cope with oxidative stress. Bats are known to carry a variety of zoonotic pathogens and at the same time are, despite their high mass-specific basal metabolic rate, unusually long lived, which may be partly the result of low oxidative damage of organs. Here, we asked whether an immune challenge causes oxidative stress in free-ranging bats, measuring two oxidative stress markers. We injected 20 short-tailed fruit bats (Carollia perspicillata) with bacterially derived lipopolysaccharide (LPS) and 20 individuals with phosphate-buffered saline solution (PBS) as a control. Individuals injected with LPS showed an immune reaction by increased white blood cell count after 24 h, whereas there was no significant change in leukocyte count in control animals. The biological antioxidant potential (BAP) remained the same in both groups, but reactive oxygen metabolites (ROMs) increased after treatment with LPS, indicating a significant increase in oxidative stress in animals when mounting an immune reaction toward the inflammatory challenge. Control individuals did not show a change in oxidative stress markers. We conclude that in a long-lived mammal, even high concentrations of antioxidants do not immediately neutralise free radicals produced during a cellular immune response. Thus, fighting an infection may lead to oxidative stress in bats.

Measures of the Constitutive Immune System Are Linked to Diet and Roosting Habits of Neotropical Bats

Ecological and social factors are central in the emergence and transmission of infectious diseases, thus bearing the potential for shaping a species’ immune functions. Although previous studies demonstrated a link between social factors and the cellular immune system for captive mammals, it is yet poorly understood how ecological factors are connected with the different branches of the immune system in wild populations. Here, we tested how variation in aspects of the constitutive cellular and humoral immune system of free ranging bats is associated with two ecological factors that likely influence the putative risk of species to become infected by parasites and pathogens: diet and shelter. We found that white blood cell counts of 24 syntopic Neotropical bat species varied with the species’ diet and body mass. Bats that included at least partially vertebrates in their diet exhibited the highest white blood cell counts, followed by phytophagous and insectivorous species, which is in agreement with the assumption that the immune system varies with the pathogen transmission risk of a trophic level. The soluble part of the constitutive immune response, assessed by an in vitro bacterial killing assay, decreased with increasing roost permanence. Our results suggest that the ecology is an important factor in the evolution of the immune system in bats and probably also other mammals.

Immune Profile Predicts Survival and Reflects Senescence in a Small, Long-Lived Mammal, the Greater Sac-Winged Bat ( Saccopteryx bilineata )

The immune system imposes costs that may have to be traded against investment of resources in other costly life-history traits. Yet, it is unknown if a trade-off between immunity and longevity occurs in free-ranging mammals. Here, we tested if age and survival, two aspects associated with longevity, are linked to immune parameters in an 8 g bat species. Using a combination of cross-sectional and longitudinal data, we assessed whether total white blood cell (WBC) counts, bacterial killing ability of the plasma (BKA) and immunoglobulin G (IgG) concentration change with age. Furthermore, we asked if these immune parameters impose costs resulting in decreased survival probabilities. We found that WBC counts decreased with age both within and among individuals. IgG concentrations were higher in older individuals, but did not change with age within individuals. Furthermore, individuals with above average WBC counts or IgG concentration had lower probabilities to survive the next six months. High WBC counts and IgG concentrations may reflect infections with parasites and pathogens, however, individuals that were infected with trypanosomes or nematodes showed neither higher WBC counts or IgG concentrations, nor was infection connected with survival rates. BKA was higher in infected compared with uninfected bats, but not related to age or survival. In conclusion, cellular (WBC) and humoral (IgG) parts of the immune system were both connected to age and survival, but not to parasite infections, which supports the hypothesis that energetically costly immunological defences are traded against other costly life-history traits, leading to a reduced lifespan in this free-ranging mammal.

Frugivory is associated with low measures of plasma oxidative stress and high antioxidant concentration in free-ranging bats

Oxidative stress—an imbalance between reactive pro- and neutralising antioxidants—damages cell structures and impairs fitness-relevant traits such as longevity and reproduction. Theory predicts that feeding on diets with high antioxidant content such as fruits should reduce oxidative stress; however, there is no support of this idea in free-ranging mammals. Bats cover a large variety of ecological niches, and therefore, we asked if measures of oxidative stress are lower in species with fruit diets. We measured reactive oxygen metabolites (ROM) representing total pro-oxidants produced and antioxidants in the plasma of 33 Neotropical bat species. Species with a fruit diet showed the lowest level of ROM and the highest concentration of antioxidants, followed by omnivorous and animalivorous species. Potentially, frugivorous species ingest more antioxidants with food and thus are able to neutralise more pro-oxidants than species not feeding on fruits, resulting in an overall lower level of oxidative stress. We therefore showed for the first time that measures of oxidative stress vary according to diets in free-ranging mammals.

Circulating white blood cell counts in captive and wild rodents are influenced by body mass rather than testes mass, a correlate of mating promiscuity

Summary Comparative studies of captive primates and carnivores have shown a positive correlation between total white blood cell (WBC) counts and the level of inferred mating promiscuity (e.g. using testes mass). This correlation has been interpreted to support the ‘sexually transmitted diseases (STDs)’ hypothesis, which states that differential spread of STDs is caused by variation in mating behaviour which shapes baseline aspects of the immune system in mammals. In the present study, we tested the STDs hypothesis in rodents using 28 species from free-ranging and 9 species from captive populations. We compiled data set for the 9 studies of captive rodent populations from the International Species Information System (ISIS) and gathered 136 studies of wild populations from the literature. Using phylogenetic generalized least-squares statistical models considering non-independence resulting from shared ancestry, we confirmed that species with greater adult body mass averaged across sexes had elevated total WBC and differential WBC (neutrophils and lymphocytes) counts and that captive animals presented higher lymphocyte counts than free-ranging ones. However, we found that the total and differential WBC counts did not covary with the residual testes mass – a correlate of mating promiscuity. The results suggest that selection pressures caused by STDs may strongly vary among taxonomic groups. In order to determine the drivers of immunological variation among mammals, further comparative immunological studies including a wide range of taxonomic groups and socio-ecological variables should be performed and we recommend doing so by primarily focusing on free-ranging animals.

Zoonotic Viruses and Conservation of Bats

Many of the recently emerging highly virulent zoonotic diseases have a likely bat origin, for example Hendra, Nipah, Ebola and diseases caused by coronaviruses. Presumably because of their long history of coevolution, most of these viruses remain subclinical in bats, but have the potential to cause severe illnesses in domestic and wildlife animals and also humans. Spillovers from bats to humans either happen directly (via contact with infected bats) or indirectly (via intermediate hosts such as domestic or wildlife animals, by consuming food items contaminated by saliva, faeces or urine of bats, or via other environmental sources). Increasing numbers of breakouts of zoonotic viral diseases among humans and livestock have mainly been accounted to human encroachment into natural habitat, as well as agricultural intensification, deforestation and bushmeat consumption. Persecution of bats, including the destruction of their roosts and culling of whole colonies, has led not only to declines of protected bat species, but also to an increase in virus prevalence in some of these populations. Educational efforts are needed in order to prevent future spillovers of bat-borne viruses to humans and livestock, and to further protect bats from unnecessary and counterproductive culling.

Do female Norway rats form social bonds

Social bonds reflect specific and enduring relationships among conspecifics. In some group-living animals, they have been found to generate immediate and long-term fitness benefits. It is currently unclear how important and how widespread social bonds are in animals other than primates. It has been hypothesized that social bonds may help in establishing stable levels of reciprocal cooperation. Norway rats (Rattus norvegicus) reciprocate received help to an unrelated social partner. It is hitherto unknown, however, whether this cooperative behaviour is based on the establishment of social bonds among involved individuals. Norway rats live in social groups that can be very large; hence, without bonds, it may be difficult to keep track of other individuals and their previous behaviour, which is a precondition for generating evolutionarily stable levels of cooperation based on direct reciprocity. Here we tested whether wild-type female rats form bonds among each other, which are stable both over time and across different contexts. In addition, we scrutinized the potential influence of social rank on the establishment of bonds. Despite the fact that the hierarchy structure within groups remained stable over the study period, no stable social bonds were formed between group members. Apparently, social information from consecutive encounters with the same social partner is not accumulated. The lack of long-term social bonds might explain why rats base their decisions to cooperate primarily on the last encounter with a social partner, which may differ from other animals where cooperation is based on the existence of long-term social bonds.Significance statementSocial bonds have been hypothesized to favour reciprocal cooperation. Norway rats reciprocate help received from a social partner, but it is hitherto unclear whether they form social bonds that might further such cooperative behaviour. Here we tested whether female Norway rats engage in social relationships with a same-sex partner, which are stable over time and across contexts. In contrast to the hypothesized existence of bonds among long-term group members, our results provide no evidence that rats form specific social relationships. Rather than accumulating social information into social bonds, rats apparently base their decision to cooperate merely on the outcome of recent encounters.

Multidimensionality of Chemical Information in Male Greater Sac-Winged Bats (Saccopteryx bilineata)

The complexity of social signals is thought to depend on the complexity of social systems, but evidence from wild animals is scarce. Here, we investigated the chemical information provided by individual male greater sac-winged bats (Saccopteryx bilineata), a small, long-lived neotropical bat species with a harem-polygynous mating system. We analysed the chemical fingerprints of wing-sac liquids that are displayed by males in front of females. Specifically, we tested if fingerprints of 45 males included information about age (adult, juvenile), year of sampling, and distance between colonies. We confirmed age-specific differences in male-specific substances, but show furthermore that chemical fingerprints correlate with year of collection and distance between colonies. Thus, the wing-sac chemistry of male S. bilineata conveys a multitude of information, which can potentially be used by conspecifics, especially by females to assess the status of potential mates. Our study provides evidence for a multidimensionality of chemical information in a free-ranging mammal with high social complexity.