Energetic Benefits of Sociality Offset the Costs of Parasitism in a Cooperative Mammal

We thank the owners for access to their property for animal capture and KwaZulu-Natal Nature Conservation Service for issuing the capture permit. This research was funded by the NRF-SAR Chair for Mammalian Behavioural Ecology and Physiology to NCB and University of Pretoria PDRF's to MS and HL. Many assistants were involved with fieldwork but we would especially like to thank Marietjie Oosthuizen and Craig Jackson for their help. This research was funded by the Department of Science and Technology/National Research Foundation-South African Research Chairs Initiative Chair for Mammalian Behavioural Ecology and Physiology to N.C.B. and University of Pretoria Postdoctoral Research Fellowships to M.S. and H.L. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.Peer reviewedPublisher PD

Determinants of helminth infection in a subterranean rodent, the Cape dune mole-rat (Bathyergus suillus)

The helminth fauna of the largest bathyergid, the Cape molerat (Bathyergus suillus) was studied throughout an entire calendar year. The species richness encountered was low, with only 3 species of nematodes (Longistriata bathyergi, Mammalakis macrospiculum, and Trichostrongylus sp.) and 2 species of cestodes (Taenia sp. and Rodentolepis sp.). At less than 10%, the prevalence for all helminths species was similarly low and may be a result of the solitary lifestyle and the subterranean habitat exploited by this rodent. Clear seasonal patterns were apparent for the most common nematode (L. bathyergi), and prevalence and abundance were highest among non-pregnant females compared to males and pregnant females. Dispersal patterns associated with the mating system of the host could explain this pattern. In contrast, the prevalence of the most common cestode (Taenia sp.) was neither determined by season nor host sex, suggesting that foraging habits may constantly expose B. suillus to this parasite.http://asp.unl.edu/index.php?option=com_content&view=article&id=39&Itemid=48ab201

Possible modulatory effects of male cues and social system on luteinizing hormone and pituitary sensitivity in two African mole-rats

The current study set out to investigate the potential effects of olfactory stimuli on the basal circulating levels of luteinizing hormone (LH) and the response of the pituitary to an exogenous gonadotropin-releasing hormone (GnRH) challenge in two mole-rat species with induced ovulation but contrasting mating and social systems. Females were either kept in isolation, allowed only olfactory and auditory contact or in physical contact with a male. Basal LH as well as pituitary challenged LH blood samples were collected after six hours. Post-challenge LH levels were significantly elevated compared to baseline levels in both species. However, neither basal nor post-challenge LH levels differed significantly between treatments for females of either species. At the same time, while baseline LH was comparable between the two species, post-challenge levels were significantly greater for the solitary species. Our findings negate a modulatory role of male cues on LH levels but suggest increases in pituitary sensitivity in the solitary species. This could enhance reproductive success in species with only sporadic encounters between the sexes and merits further studies in other species.The National Research Foundation. N.C.B. acknowledges funding for a DST-NRF SARChI Chair of Mammalian Behavioural Ecology and Physiology. H.L. acknowledges a postdoctoral research fellowship from the University of Pretoria.http://www.bioone.org/loi/afzoab201

Temporal segregation between dung-inhabiting beetle and fly species

The coexistence of ecologically similar species (i.e. species utilizing the same resource) is a major topic in ecology. Communities are assembled either through the biotic interactions of ecologically similar species, e.g. competition, or by the abiotic separation of species along gradients of environmental conditions. Here, we investigated the temporal segregation, succession and seasonality of dung-inhabiting Coleoptera and Diptera that utilize an identical resource in exactly the same way. The data were collected from two temperate pastures, one in the United Kingdom and the second in the Czech Republic. There was no evident temporal separation between ecologically similar coleopterous or dipterous taxa during succession. In contrast, these two orders were almost perfectly separated seasonally in both combined and site-specific datasets. Flies were most abundant in the summer, and beetles were more abundant in the spring and autumn. Ecologically similar beetles and flies also displayed seasonal separation in both combined and site-specific data. Analyses within site-specific data sets revealed such a separation at both the order and species level. Season is therefore the main temporal axis separating ecologically similar species of dung-inhabiting insects in temperate habitats, while succession aggregates species that may have similar environmental tolerances (to e.g. dung moisture). This separation between ecologically similar taxa of beetles and flies may be attributable to either competition-based niche separation or to temperature tolerance-based habitat filtering, since flies have peak activity in warmer months while beetles have peak activity in cooler months

Natural parasite infection affects the tolerance but not the response to a simulated secondary parasite infection

Parasites deplete the resources of their host and can consequently affect the investment in competing traits (e.g. reproduction and immune defence). The immunocompetence handicap hypothesis posits that testosterone (T) mediates trade-offs between parasite defence and reproductive investment by suppressing immune function in male vertebrates while more recently a role for glucocorticoids (e.g. cortisol (C)) in resource allocation has been suggested. These hypotheses however, have not always found support in wild animals, possibly because most studies focus on a single parasite species, whereas infections with multiple parasites are the rule in nature. We measured body mass, T- and C-levels of wild male highveld mole-rats (Cryptomys hottentotus pretoriae) naturally uninfected or infected with a cestode (Mathevotaenia sp.) right after capture. Subsequently, we injected animals subcutaneously with a lipopolysaccharide (LPS) to simulate a bacterial infection and recorded changes in body mass, food intake, haematological parameters and hormone levels. As a control, animals were injected with saline. Natural infection neither affected initial body mass nor C-levels, whereas infected males had significantly reduced T-levels. We observed significant reductions in food intake, body mass and T in response to LPS but not saline while C increased. However, this response did not vary with infection status. In contrast, final body mass and some haematological parameters were significantly lowered in infected males. Our results suggest that naturally infected males are able to compensate for resource depletion by physiological adjustments. However, this leaves them less tolerant to the challenges of a secondary infection.The Department of Science and Technology/National Research Foundation South African Research Chair for Behavioural Ecology and Physiology to NCB and HL acknowledges funding through a Research Fellowship by the University of Pretoria.http://www.plosone.orgam201

Reproductive status and testorene among females in cooperative mole-rat societies

Sexual selection acts on traits that increase reproductive success. Variation in reproductive success is often higher among males than females. Consequently, sexual selection has been studied extensively in males while its possible role in females has only recently attracted considerable attention. In some cooperatively breeding species females compete intensely for reproductive opportunities and may thereby have evolved 'male-like' traits such as increased intra-sexual aggression and exaggerated secondary sexual traits. The expression of the latter tends to be testosterone-dependent in male vertebrates but whether this is also the case among females remains poorly understood. Here, we compare two cooperatively breeding mole-rat species (Natal, Cryptomys hottentotus natalensis, and Damaraland mole-rats, Fukomys damarensis) in which a single female monopolises reproduction through behavioural and physiological suppression, respectively, to evaluate the effect of female intra-sexual competition. Consistent with the hypothesis that intra-sexual competition has shaped patterns of testosterone (T) secretion among females in these species, we show that (i) female T levels in both species are significantly higher among breeding (BFs) (who may face the highest degree of intra-sexual competition) compared to non-breeding females (NBFs), (ii) that T levels in both species are significantly higher when access to unrelated males can be assumed to be greatest (i.e., wet season), and (iii) that the average female T levels are a full order of magnitude higher in the absence of a physiological mechanism of reproductive suppression. Together, our results suggest a role for intra-sexual competition in shaping patterns of T secretion among females of the social mole-rats and raise the possibility of a modulatory role for the mode of reproductive suppression on competition-related traits in females.HL and NCB are indebted to the University of Pretoria and the NRF for funding while AJY acknowledges a research grant from Magdalene College, Cambridge, ASAB and NERC.http;//www.elsevier.com/locate/ygcenhb201

Non-invasive assessment of glucocorticoid and androgen metabolite levels in cooperatively breeding Damaraland mole-rats (Fukomys damarensis)

Dominant females of cooperative breeding species often use aggression to suppress reproduction of subordinate females, resulting in subordinates experiencing stress-related increases in glucocorticoid levels, which may cause reproductive down-regulation. This would suggest a general pattern with higher glucocorticoid levels in subordinate compared to dominant individuals; however, the opposite was found in a number of cooperatively breeding species. Furthermore, breeding females of the cooperatively breeding Damaraland mole-rats (Fukomys damarensis) exhibit very high androgen concentrations during the wet season, presumably to support their breeding monopoly. Hormone analysis in Damaraland mole-rats have typically been measured using plasma and urine, but faecal analysis offers additional advantages especially for field studies on this species. The present study examines the suitability of Damaraland mole-rat faecal samples for determining glucocorticoid metabolite (fGCM) and androgen metabolite (fAM) concentrations using enzyme immunoassays. Using these assays, we further evaluated the effects of breeding status on fGCM and fAM concentrations in wild-caught and captive Damaraland mole-rats. Wild-caught breeding and non-breeding males and females exhibited no differences in fAM concentrations. Immunoreactive fGCM concentrations were only high in male breeders and comparatively low in non-breeders and breeding females. Concentrations of fAMs and fGCMs were similar in captive males and females, but fAM concentrations were elevated in captive compared to wild-caught individuals, which may be related to a higher reproductive activity due to removal from the breeding female. The relatively uniform fAM and fGCM concentrations found in wild-caught mole-rats may be explained by a stable colony structure during the dry season during which this study was conducted. Limited dispersal opportunities result in lower aggression and stress levels within a colony and as a result lower fAM and fGCM concentrations.A South African Research Chair of Mammalian Behavioural Ecology and Physiology awarded to Nigel C. Bennett by DST and NRF. K. Medger and H. Lutermann acknowledge funding by the University of Pretoria.http://www.elsevier.com/locate/ygcen2019-09-15hj2018Anatomy and PhysiologyMammal Research InstituteZoology and Entomolog

Sex ratio variation in a eusocial mammal, the Damaraland mole-rat, Fukomys damarensis

Sex allocation theory predicts that mothers benefit from adjusting the sex ratio of their offspring in relation to their offspring's future reproductive success. In cooperative breeders, parents are expected to bias the sex ratio in relation to their current need for help and the benefit received from helpers of each sex as proposed by the local resource enhancement (LRE) and helper repayment hypotheses (HR). Consequently, as group size increases, sex ratios are expected to be biased towards the sex that is more likely to disperse to avoid competition as proposed in the local resource competition hypothesis (LRC). The current study aimed to investigate helper effects on breeder fecundity and offspring sex ratio adjustments in a eusocial mammal the Damaraland mole-rat Fukomys damarensis. Both sexes equally contribute to helping in this species, but breeding dispersal is male biased. We found no evidence for helper effects on maternal body mass and litter size. Offspring sex ratio was not affected by maternal mass or litter size. However, the probability of male pups to be born increased with the number of female helpers and decreased with the number of male helpers. In addition, the number of male pups in a litter increased significantly with the number of female but not male helpers, while no helper effects were apparent for the number of female pups born. Hence, our data suggest that the mechanisms underlying the LRE, HR and LRC may operate simultaneously in the study species.The National Research Foundation and the University of Pretoria.http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1469-79982015-10-30hj201

Energetic benefits of sociality offset the costs of parasitism in a cooperative mammal

Sociality and particularly advanced forms of sociality such as cooperative breeding (living in permanent groups with reproductive division of labour) is relatively rare among vertebrates. A suggested constraint on the evolution of sociality is the elevated transmission rate of parasites between group members. Despite such apparent costs, sociality has evolved independently in a number of vertebrate taxa including humans. However, how the costs of parasitism are overcome in such cases remains uncertain. We evaluated the potential role of parasites in the evolution of sociality in a member of the African mole-rats, the only mammal family that exhibits the entire range of social systems from solitary to eusocial. Here we show that resting metabolic rates decrease whilst daily energy expenditure and energy stores (i.e. body fat) increase with group size in social Natal mole rats (Cryptomys hottentotus natalensis). Critically, larger groups also had reduced parasite abundance and infested individuals only showed measurable increases in energy metabolism at high parasite abundance. Thus, in some circumstances, sociality appears to provide energetic benefits that may be diverted into parasite defence. This mechanism is likely to be self-reinforcing and an important factor in the evolution of sociality.Conceived and designed the experiments: HL MS. Performed the experiments: HL MS. Analyzed the data: HL MS JRS. Contributed reagents/materials/analysis tools: JRS NCB. Wrote the paper: HL MS NCB JRS.This research was funded by the Department of Science and Technology/National Research Foundation-South African Research Chairs Initiative Chair for Mammalian Behavioural Ecology and Physiology to N.C.B. and University of Pretoria Postdoctoral Research Fellowships to M.S. and H.L. We thank the owners for access to their property for animal capture and KwaZulu-Natal Nature Conservation Service for issuing the capture permit. This research was funded by the NRF-SAR Chair for Mammalian Behavioural Ecology and Physiology to NCB and University of Pretoria PDRF’s to MS and HL.www.plosone.orgam2013ab201

Evidence for interspecific interactions in the ectoparasite infracommunity of a wild mammal

BACKGROUND : Co-infection with multiple parasite species is commonly observed in nature and interspecific interactions are likely to occur in parasite infracommunities. Such interactions may affect the distribution of parasites among hosts but also the response of infracommunities to perturbations. However, the response of infracommunities to perturbations has not been well studied experimentally for ectoparasite communities of small mammal hosts. METHODS : In the current study we used experimental perturbations of the ectoparasite infracommunity of sengis from Africa. We suppressed tick recruitment by applying an acaride and monitored the effects on the ectoparasite community. RESULTS : Our treatment affected the target as well as two non-target species directly. The experimental removal of the dominant tick (Rhipicephalus spp.) resulted in increases in the abundance of chiggers and lice. However, while these effects were short-lived in chiggers, which are questing from the environment, they were long-lasting for lice which spend their entire life-cycle on the host. In addition, the recruitment rates of some ectoparasite species were high and did not always correspond to total burdens observed. CONCLUSION : These findings indicate that infracommunity interactions may contribute to patterns of parasite burdens. The divergent responses of species with differing life-history traits suggest that perturbation responses may be affected by parasite life-history and that the ectoparasite infracommunity of sengis may lack resilience to perturbations. The latter observation contrasts with the high resilience reported previously for endoparasite communities and also suggests that anti-parasite treatments can affect the distribution of non-target species.NRF, the DST-NRF SARChI Chair of Behavioural Ecology and Physiology and the University of Pretoria.http://www.parasitesandvectors.comhb201