Early-life adversity predicts performance and fitness in a wild social carnivore

1. Studies on humans indicate that encountering multiple sources of adversity in childhood increases the risk of poor long-term health and premature death. Far less is known about cumulative effects of adversity during early life in wildlife. 2. Focusing on the spotted hyena Crocuta crocuta, a social mammal with small litters, extensive maternal care, slow development and access to resources determined by social rank, we determined the contribution of ecological, maternal, social and demographic factors during early life on performance and fitness, and tested whether the impact of early-life adversity is cumulative. 3. Using longitudinal data from 666 female hyenas in the Serengeti National Park, we determined the early growth rate, survival to adulthood, age at first reproduction (AFR), lifetime reproductive success (LRS) and longevity. We fitted multivariate models in which we tested the effects of environmental factors on these performance measures. We then constructed a cumulative adversity index and fitted models to test the effect of this index on each performance measure. Finally, the value of cumulative adversity models was tested by comparing them to multivariate and single-effect models in which the effect of each environmental factor was considered separately. 4. High maternal rank decreased the AFR of daughters. Singleton and dominant cubs had higher growth rate than subordinate cubs, and singletons also had a higher survival chance to adulthood than subordinates. Daughters of prime age mothers had a higher growth rate, longevity and LRS. Little and heavy rainfall decreased survival to adulthood. Increasing numbers of lactating female clan members decreased growth rate, survival to adulthood and LRS. Cumulative adversity negatively affected short-term performance and LRS. Multivariate models outperformed cumulative adversity and single-effect models for all measures except for AFR and longevity, for which single-effect models performed better. 5. Our results suggest that in some wildlife populations the combination of specific conditions in early life may matter more than the accumulation of adverse conditions as such

Diet of the Golden Jackal (Canis aureus) and Silver-Backed Jackal (Canis mesomelas) in the Southern Part of the Serengeti Ecosystem, Tanzania: A Comparative Study

Habitat and food resource partitioning are predicted to facilitate the coexistence of similar-sized carnivores. The golden jackal (Canis aureus) and silver-backed jackal (Canis mesomelas) are similar-sized canids that respectively inhabit grassland and woodland in the Serengeti ecosystem, Tanzania. As information on the diet and food-intake of these two species in this ecosystem is limited, we aimed to compare the diet and food-intake of these canids in the wet and dry seasons, using data from focal samples of foraging behaviour and scat analysis. We predicted dietary differences between these species, seasonal differences within species and peak food intake when breeding. Result of a logistic regression considering insect and small mammal remains in scats revealed dietary differences both between species and within-species seasonal differences. Results of a censored regression model on the estimated weigh of food intake by foraging individuals indicated that intake was highest during the breeding season of each species, which occurs in the wet season in golden jackals and the dry-season in silver-backed jackals. Our study provides new insights on differences in the foraging ecology of these two jackal species in the Serengeti ecosystem. Keywords:    Canis aureus; Canis mesomelas, diet, Serengeti ecosystem, season

Climate change does not decouple interactions between a central-place-foraging predator and its migratory prey

Little is known about potential cascading effects of climate change on the ability of predators to exploit mobile aggregations of prey with a spatiotemporal distribution largely determined by climatic conditions. If predators employ central-place foraging when rearing offspring, the ability of parents to locate sufficient prey could be reduced by climate change. In the Serengeti National Park, Tanzania, migratory species dominate mammalian herbivore biomass. These migratory herds exploit nutrient-rich vegetation on the southern plains in the rainy season and surface water in the northwest in the dry season. Female spotted hyenas Crocuta crocuta breed throughout the year and use long-distance central-place-foraging “commuting trips” to migratory herds to fuel lactation for ≥12 months. Changes in rainfall patterns that alter prey movements may decrease the ability of mothers to locate profitable foraging areas and thus increase their overall commuting effort, particularly for high-ranking females that have priority of access to food resources within their clan territory and thus less commuting experience. In hyena clan territories, this may be reflected by a decrease in migratory herd presence and a decrease in the presence of lactating females, as maternal den presence represents the opposite of commuting effort. We investigated the strength of the relationship between rainfall volume, migratory herd presence in three hyena clan territories, and the responses of lactating females to this climate/prey relationship in terms of maternal den presence, using an observation-based dataset spanning three decades. The probability of migratory herd presence in hyena clan territories increased with the amount of rainfall 2 months earlier, and maternal den presence increased with migratory herd presence. Rainfall volume substantially increased over 30 years, whereas the presence of migratory herds in hyena clans and the strength of the relationship between rainfall and migratory herd presence decreased. Hyenas thus adjusted well to the climate change-induced decreased the presence of migratory herds in their territories, since maternal den presence did not decrease over 30 years and still matched periods of high prey abundance, irrespective of female social status. These results suggest a high plasticity in the response of this keystone predator to environmental variability

Genetic Diversity, Latency and Co-Infections

Alphaherpesviruses are highly prevalent in equine populations and co- infections with more than one of these viruses’ strains frequently diagnosed. Lytic replication and latency with subsequent reactivation, along with new episodes of disease, can be influenced by genetic diversity generated by spontaneous mutation and recombination. Latency enhances virus survival by providing an epidemiological strategy for long-term maintenance of divergent strains in animal populations. The alphaherpesviruses equine herpesvirus 1 (EHV-1) and 9 (EHV-9) have recently been shown to cross species barriers, including a recombinant EHV-1 observed in fatal infections of a polar bear and Asian rhinoceros. Little is known about the latency and genetic diversity of EHV-1 and EHV-9, especially among zoo and wild equids. Here, we report evidence of limited genetic diversity in EHV-9 in zebras, whereas there is substantial genetic variability in EHV-1. We demonstrate that zebras can be lytically and latently infected with both viruses concurrently. Such a co- occurrence of infection in zebras suggests that even relatively slow-evolving viruses such as equine herpesviruses have the potential to diversify rapidly by recombination. This has potential consequences for the diagnosis of these viruses and their management in wild and captive equid populations. View Full- Tex

Measuring faecal epi-androsterone as an indicator of gonadal activity in spotted hyenas (Crocuta crocuta)

Enzyme immunoassays (EIA) that measure faecal testosterone metabolites (fTM) are useful tools to monitor gonadal activity. The aim of this study was to validate an “in-house” epiandrosterone EIA to monitor fTM in spotted hyenas. FTM were characterised in a male and a female hyena that each received an injection of 3H-testosterone. High-performance liquid chromatography (HPLC) analyses revealed a cluster of highly polar enzyme-hydrolysable hormone metabolite conjugates. We performed hydrolysis using β-glucuronidase to deconjugate metabolites and improve sensitivity of the assay. Because β-glucuronidase from Helix pomatia has been reported to bias testosterone measurements in some species, we compared the enzymatic activity of the commonly used β-glucuronidase extracted from H. pomatia with the same enzyme from Escherichia coli. Our results showed that β-glucuronidases from both sources produced similar results from spotted hyena faeces. We therefore hydrolysed samples with H. pomatia enzymes. HPLC analyses also demonstrated that following hydrolysis the epiandrosterone EIA measured significant amounts of immunoreactive metabolites corresponding to radiolabelled metabolites in both sexes. Additionally, HPLC and GC-MS analyses confirmed the presence of epiandrosterone in faeces of spotted hyenas. The biological relevance of the epiandrosterone EIA was validated by demonstrating (1) a significant increase in fTM levels in response to a testosterone injection within 16 h, (2) no biological responsiveness to an adrenocorticotropic hormone (ACTH) injection and (3) significant differences in fTM levels between juvenile males and adult immigrant males in a free-ranging wild population. Our results clearly demonstrate that the epiandrosterone EIA is a reliable non-invasive method to monitor gonadal activity in spotted hyenas.Funded by a joint “Collaboration in the field of sustainable management of wildlife populations” grant (SUA 10/020) of the International Bureau of the German Federal Ministry for Education and Research (BMBF) and the National Research Council of South Africa, and the Leibniz Institute for Zoo & Wildlife Research (IZW).http://www.plosone.orgam201

Infanticide by Adult Females Causes Sexual Conflict in a Female-Dominated Social Mammal

Infanticide by adult females includes any substantial contribution to the demise of young and inevitably imposes fitness costs on the victim’s genetic fathers, thereby generating sexual conflict with them. Few if any studies have quantified the impact of infanticide by females on male reproductive success, the magnitude of sexual conflict this causes and possible counterstrategies males use against infanticidal females. We examine these topics in spotted hyena (Crocuta crocuta) clans, where females socially dominate breeding males and strong female mate-choice is independent of male social status. We consider two causes of infanticide by females, violent attacks on cubs and fatal maternal neglect. Violent attacks are predicted during periods of social instability at the top of the female linear dominance hierarchy and victims are expected to predominantly have mothers above median rank. Fatal maternal neglect, when starving litters are abandoned, is associated with monopolization of food in clan territories by high-ranking females, and victims are predicted to have mothers below median rank. Female perpetrators of violent attacks are expected to reduce the reproductive success of the fathers of their victims more than perpetrators of fatal maternal neglect. We tested these predictions using 30 + years of data (54 recorded violent attacks, 43 cases of fatal maternal neglect, DNA profiling of 1,671 individuals). Using long-term observations at communal dens we investigated whether males use counterstrategies against infanticide reported in other mammals. Due to female social dominance over breeding males, strong female mate-choice and prolonged offspring dependence on lactation in spotted hyenas, we predicted that these counterstrategies were unlikely to be used by males against females, thus no incidences of them were likely to be observed. Our results revealed that breeding males lost cubs to violent attacks at all stages of their reproductive tenure and to perpetrators with whom they did not sire offspring. Amongst known sources of paternity loss, violent attacks comprised 12.2% and maternal neglect 9.8% of cases. Violent attacks significantly reduced offspring production rates of breeding males, suggesting that infanticide by females generates sexual conflict. As predicted, no evidence of males using counterstrategies against infanticide by females were observed

The Effect of Reduced Water Availability in the Great Ruaha River on the Vulnerable Common Hippopotamus in the Ruaha National Park, Tanzania

In semi-arid environments, ‘permanent’ rivers are essential sources of surface water for wildlife during ‘dry’ seasons when rainfall is limited or absent, particularly for species whose resilience to water scarcity is low. The hippopotamus (Hippopotamus amphibius) requires submersion in water to aid thermoregulation and prevent skin damage by solar radiation; the largest threat to its viability are human alterations of aquatic habitats. In the Ruaha National Park (NP), Tanzania, the Great Ruaha River (GRR) is the main source of surface water for wildlife during the dry season. Recent, large-scale water extraction from the GRR by people upstream of Ruaha NP is thought to be responsible for a profound decrease in dry season water-flow and the absence of surface water along large sections of the river inside the NP. We investigated the impact of decreased water flow on daytime hippo distribution using regular censuses at monitoring locations, transects and camera trap records along a 104km section of the GRR within the Ruaha NP during two dry seasons. The minimum number of hippos per monitoring location increased with the expanse of surface water as the dry seasons progressed, and was not affected by water quality. Hippo distribution significantly changed throughout the dry season, leading to the accumulation of large numbers in very few locations. If surface water loss from the GRR continues to increase in future years, this will have serious implications for the hippo population and other water dependent species in Ruaha NP

Data from: Trade-offs in lactation and milk intake by competing siblings in a fluctuating environment

Income breeders which forage without their offspring in attendance should adjust nursing frequency and the quantity and composition of milk to prevailing ecological conditions, and increase the quantity or quality of milk transferred if the frequency of nursing visits declines. When milk delivery to a litter is insufficient, sibling competition should skew milk consumption in favor of dominant litter members. We quantified milk nutritional composition and gross energy density, nursing bout durations, per capita milk transfer (kg), and milk transfer rate (g/min) per nursing bout in singletons and twins in a social carnivore, the spotted hyena. In our study population, the energetic cost of lactation is rank dependent and particularly high because large fluctuations in local prey abundance necessitate long-distance foraging, reducing nursing frequency and intensifying sibling competition, more frequently for low-ranking than high-ranking females. Females increased milk gross energy density, driven by fat content, and increased nursing bout durations as nursing frequency declined. Milk transfer increased as social status declined. Females below median rank also increased milk transfer as nursing frequency declined. Milk transfer was independent of nursing frequency in females above median rank and higher for singletons than cubs in twin litters. Dominant siblings achieved significantly higher amounts and rates of milk transfer than their paired subordinate littermates; this bias increased as sibling competition intensified. Our results show how the interplay between ecological and social constraints determines the quality and quantity of milk transferred, and how socially dominant siblings use aggression to skew milk intake in their favor