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

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

Epigenetic signatures of social status in wild female spotted hyenas (Crocuta crocuta)

In mammalian societies, dominance hierarchies translate into inequalities in health, reproductive performance and survival. DNA methylation is thought to mediate the effects of social status on gene expression and phenotypic outcomes, yet a study of social status-specific DNA methylation profiles in different age classes in a wild social mammal is missing. We tested for social status signatures in DNA methylation profiles in wild female spotted hyenas (Crocuta crocuta), cubs and adults, using non-invasively collected gut epithelium samples. In spotted hyena clans, female social status influences access to resources, foraging behavior, health, reproductive performance and survival. We identified 149 differentially methylated regions between 42 high- and low-ranking female spotted hyenas (cubs and adults). Differentially methylated genes were associated with energy conversion, immune function, glutamate receptor signalling and ion transport. Our results provide evidence that socio-environmental inequalities are reflected at the molecular level in cubs and adults in a wild social mammal

11-2001 Newsletter

Minnesota State University, Mankato, Library Services Newsletter for November 2001

Landscape Structures Affect Risk of Canine Distemper in Urban Wildlife

Urbanization rapidly changes landscape structure worldwide, thereby enlarging the human-wildlife interface. The emerging urban structures should have a key influence on the spread and distribution of wildlife diseases such as canine distemper, by shaping density, distribution and movements of wildlife. However, little is known about the role of urban structures as proxies for disease prevalence. To guide management, especially in densely populated cities, assessing the role of landscape structures in hampering or promoting disease prevalence is thus of paramount importance. Between 2008 and 2013, two epidemic waves of canine distemper hit the urban red fox (Vulpes vulpes) population of Berlin, Germany. The directly transmitted canine distemper virus (CDV) causes a virulent disease infecting a range of mammals with high host mortality, particularly in juveniles. We extracted information about CDV serological state (seropositive or seronegative), sex and age for 778 urban fox carcasses collected by the state laboratory Berlin Brandenburg. To assess the impact of urban landscape structure heterogeneity (e.g., richness) and shares of green and gray infrastructures at different spatial resolutions (areal of 28 ha, 78 ha, 314 ha) on seroprevalence we used Generalized Linear Mixed-Effects Models with binomial distributions. Our results indicated that predictors derived at a 28 ha resolution were most informative for describing landscape structure effects (AUC = 0.92). The probability to be seropositive decreased by 66% (0.6 to 0.2) with an increasing share of gray infrastructure (40 to 80%), suggesting that urbanization might hamper CDV spread in urban areas, owing to a decrease in host density (e.g., less foxes or raccoons) or an absence of wildlife movement corridors in strongly urbanized areas. However, less strongly transformed patches such as close-to-nature areas in direct proximity to water bodies were identified as high risk areas for CDV transmission. Therefore, surveillance and disease control actions targeting urban wildlife or human-wildlife interactions should focus on such areas. The possible underlying mechanisms explaining the prevalence distribution may be increased isolation, the absence of alternative hosts or an abiotic environment, all impairing the ability of CDV to persist without a host

Verhaltensmechanismen und endokrine Reaktionen

Rivalry between littermates can be intense as dominant siblings often obtain a greater share of food and thereby major fitness benefits in terms of growth and survival. When food provided by parents is insufficient, dominants may kill their subordinate siblings, either by physical damage or through enforced starvation. This “facultative siblicide” occurs in many birds and at least one mammal: the spotted hyena (Crocuta crocuta). This thesis focused on the behavioural mechanisms and the endocrine responses to sibling rivalry in twin litters of the spotted hyena. I first studied rivalry in a framework of interactions between dominant and subordinate siblings. Dominants skewed access to maternal milk in their favour, but hungry and less submissive subordinates decreased the extent of the skew in favour of dominants. I found compelling evidence that females are better competitors - and hence potentially more likely to commit siblicide - than males. This probably explains why more “at risk” hungry subordinates raised with a dominant sister were more assertive than hungry subordinates raised with a dominant brother. Trained “winner and loser effects” were involved in the emergence of the within-litter dominance relationship and dominance reversals occurred in 7% of the litters. A key finding of this chapter was that dominants do not exert complete control over their siblings’ access to milk. Glucocorticoids are often used as a measure of stress in vertebrates. I detail the validation of a method to detect faecal glucocorticoid metabolites (fGCM) in spotted hyenas. The enzyme-immunoassay successfully measured increased concentrations of fGCM after adrenocorticotropic hormone challenges in two captive spotted hyenas and after anaesthesia of another captive spotted hyena. A radiometabolism study showed that the assay mostly detected metabolites with a polarity higher than cortisol and metabolites that eluted between cortisol and corticosterone. I then investigated an age effect on fGCM concentrations in juveniles. I expected juveniles to experience a more unpredictable and hence more stressful environment when younger than when older, and found that young juveniles indeed had significantly higher fGCM concentrations than when they were older. Social subordination and hunger are often stressful. I tested whether subordinates were more stressed than dominant siblings. I found that young subordinates had higher fGCM concentrations than young dominants, probably because subordinates have less access to milk and therefore are hungrier than dominants, and subordinates are trained into submission by their dominant sibling. I also found that dominant females were more stressed than dominant males, probably because they were confronted by unpredictable, assertive siblings, whereas dominant males were not. This is the first study that combines behavioural and endocrine data from a long-term study on a mammalian species to explore in detail the link between behavioural and physiological responses to intense sibling rivalry.Die Rivalität zwischen Geschwistern eines gleichen Wurfes kann intensiv sein, da dominante Geschwister oft einen größeren Anteil der Nahrung erhalten und damit enorme Fitness-Vorteile in Bezug auf Wachstum und Überleben haben. Wenn die durch die Eltern gelieferte Nahrung nicht ausreicht, um einen ganzen Wurf erfolgreich aufzuziehen, kann es passieren, dass dominante Geschwister ihre untergeordneten Geschwister töten, entweder durch physische Schäden oder durch Nahrungsentzug. Diese "fakultative Brutreduktion" tritt in vielen Vogelarten und mindestens einer Säugetierart - der Tüpfelhyäne (Crocuta crocuta) – auf. Meine Doktorarbeit untersucht die Verhaltensmechanismen und die endokrinen Reaktionen der Geschwisterrivalität in Zwillingswürfen bei der Tüpfelhyäne. Zuerst habe ich Geschwisterrivalität in einem Rahmen von Wechselwirkungen zwischen dominanten und untergeordneten Geschwistern studiert. Dominante Geschwister verwehren den Unterwürfigen den Zugang zur Muttermilch zu ihren Gunsten, jedoch konnten hungrige und weniger unterwürfige Geschwister diesen Nachteil zugunsten der Dominanten verringern. Ich liefere überzeugende Beweise, dass weibliche Geschwister stärkere Konkurrenten als männliche sind- und deswegen eventuell ein höheres Potential haben, ihre Geschwister zu töten. Das erklärt höchstwahrscheinlich warum „gefährdetere“ unterwürfige Geschwister mit einer dominanten Schwester durchsetzungsfähiger sind, als die hungrigen unterwürfigen Geschwister, die mit einem dominanten Bruder aufgezogen werden. Geschulte „Gewinner und Verlierer Effekte“ waren bei der Entstehung von Dominanzbeziehungen zwischen dominanten und untergeordneten Geschwistern beteiligt und eine Umkehr der Dominanz trat bei 7.0% der Zwillingswürfe auf. Eine wichtige Erkenntnis aus diesem Kapitel ist, dass die Dominanten nicht die absolute Kontrolle über den Zugang ihrer Geschwister zur Muttermilch ausüben. Glukokortikoide werden gewöhnlich als ein Maß für den Stress bei Wirbeltieren verwendet. Ich beschreibe die Validierung einer Methode zur Messung von fäkalen Glukokortikoidmetaboliten (fGCM) von Tüpfelhyänen. Der Enzym- Immunoassay dokumentierte erfolgreich erhöhte Konzentrationen von fGCM nach der experimentellen Zuführung von Adrenocorticotropen Hormon (ACTH) bei zwei Tüpfelhyänen in und nach der Anästhesie bei einer weiteren Tüpfelhyäne in menschlicher Obhut. Eine Radiometabolismus-Studie zeigte, dass der Immunoassay vorwiegend Metabolite mit einer Polarität höher als Cortisol und Metabolite, die zwischen Cortisol und Corticosteron eluierten, nachweist. Schließlich habe ich einen Alterseffekt auf die fGCM Konzentrationen von juvenilen Tüpfelhyänen untersucht. Dabei erwartete ich, dass Jungtiere eine weniger vorhersagbare und deswegen stressigere Umwelt erleben, als wenn sie älter sind, und stellte fest, dass junge Jungtiere höhere Konzentrationen von fGCM hatten als die gleichen Jungtiere, wenn sie älter waren. Soziale Unterwerfung und Nahrungsentzug führen oft zu erhöhtem Stress. Ich habe untersucht, ob untergeordnete Geschwister mehr gestresst sind als dominante. In Übereinstimmung mit meiner Vorhersage fand ich, dass junge untergeordnete Individuen höhere fGCM als junge dominante aufwiesen, wahrscheinlich, weil untergeordnete weniger Zugang zur Milch und somit mehr Hunger erlebten und weil sie in der Rolle der Unterwerfung „trainiert“ waren. Wie ebenfalls erwartet, fand ich, dass dominante Weibchen mehr Stress als dominante Männchen erlebten, wahrscheinlich, weil sie mit durchsetzungsfähigeren subdominanten Geschwistern konfrontiert wurden als dominante Männchen. Dies ist die erste Langzeitstudie, die sowohl Daten zum Verhalten als auch zur Endokrinologie bei einer Säugerspezies betrachtet, um im Detail den Zusammenhang zwischen Verhalten und physiologischen Reaktionen bei intensiver Geschwisterrivalität zu erforschen

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

Epigenomics and gene regulation in mammalian social systems

Social epigenomics is a new field of research that studies how the social environment shapes the epigenome and how in turn the epigenome modulates behavior. We focus on describing known gene–environment interactions (GEIs) and epigenetic mechanisms in different mammalian social systems. To illustrate how epigenetic mechanisms integrate GEIs, we highlight examples where epigenetic mechanisms are associated with social behaviors and with their maintenance through neuroendocrine, locomotor, and metabolic responses. We discuss future research trajectories and open questions for the emerging field of social epigenomics in nonmodel and naturally occurring social systems. Finally, we outline the technological advances that aid the study of epigenetic mechanisms in the establishment of GEIs and vice versa

Long‐term reproductive costs of snare injuries in a keystone terrestrial by‐catch species

Extensive bushmeat hunting is a major threat to wildlife conservation worldwide, particularly when unselective methods such as wire snares kill target and non-target species (by-catch). Animals that escape from snares have injuries of varying severity, with effects on performance that are largely unknown, as most studies typically focus on immediate mortality caused by snaring. Here, we assessed the life-history costs of debilitating snare injuries in individually known female spotted hyenas Crocuta crocuta in three clans in the Serengeti National Park, Tanzania. This keystone predator is a regular by-catch of illegal bushmeat hunting of herbivores in the Serengeti ecosystem. We monitored individuals which escaped from snares between May 1987 and March 2020 and survived long enough to return to their clan territories from commuting trips in the park and surrounding protected areas. Snares that inflicted debilitating injuries on females did not reduce longevity but did delay age at first reproduction and reduced both litter size and offspring survival to the age of 1 year. This long-term decrease in reproductive performance likely resulted from increased inflammatory and immune responses to the snare injury and/or a decreased ability to travel the long distances necessary to feed on migratory herbivores. While our results are based on a relatively small sample of females with debilitating injuries, they suggest that the total population-level costs of wire snares in terrestrial by-catch species may be underestimated and that future studies may need to account for the potential reproductive costs of sublethal snare injuries

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