Heather E. Watts

Altered behaviour in spotted hyenas associated with increased human activity

To investigate how anthropogenic activity might affect large carnivores, we studied the behaviour of spotted hyenas (Crocuta crocuta) during two time periods. From 1996 to 1998, we documented the ecological correlates of space utilization patterns exhibited by adult female hyenas defending a territory at the edge of a wildlife reserve in Kenya. Hyenas preferred areas near dense vegetation but appeared to avoid areas containing the greatest abundance of prey, perhaps because these were also the areas of most intensive livestock grazing. We then compared hyena behaviour observed in 1996‐98 with that observed several years earlier and found many differences. Female hyenas in 1996‐98 were found farther from dens, but closer to dense vegetation and to the edges of their territory, than in 1988‐90. Recent females also had larger home ranges, travelled farther between consecutive sightings, and were more nocturnal than in 1988‐90. Finally, hyenas occurred in smaller groups in 1996‐98 than in 1988‐90. We also found several changes in hyena demography between periods. We next attempted to explain differences observed between time periods by testing predictions of hypotheses invoking prey abundance, climate, interactions with lions, tourism and livestock grazing. Our data were consistent with the hypothesis that increased reliance on the reserve for livestock grazing was responsible for observed changes. That behavioural changes were not associated with decreased hyena population density suggests the behavioural plasticity typical of this species may protect it from extinction.

Society, demography and genetic structure in the spotted hyena

Spotted hyenas (Crocuta crocuta) are large mammalian carnivores, but their societies, called ‘clans’, resemble those of such cercopithecine primates as baboons and macaques with respect to their size, hierarchical structure, and frequency of social interaction among both kin and unrelated group‐mates. However, in contrast to cercopithecine primates, spotted hyenas regularly hunt antelope and compete with group‐mates for access to kills, which are extremely rich food sources, but also rare and ephemeral. This unique occurrence of baboon‐like sociality among top‐level predators has favoured the evolution of many unusual traits in this species. We briefly review the relevant socio‐ecology of spotted hyenas, document great demographic variation but little variation in social structure across the species’ range, and describe the long‐term fitness consequences of rank‐related variation in resource access among clan‐mates. We then summarize patterns of genetic relatedness within and between clans, including some from a population that had recently gone through a population bottleneck, and consider the roles of sexually dimorphic dispersal and female mate choice in the generation of these patterns. Finally, we apply social network theory under varying regimes of resource availability to analyse the effects of kinship on the stability of social relationships among members of one large hyena clan in Kenya. Although social bonds among both kin and non‐kin are weakest when resource competition is most intense, hyenas sustain strong social relationships with kin year‐round, despite constraints imposed by resource limitation. Our analyses suggest that selection might act on both individuals and matrilineal kin groups within clans containing multiple matrilines.

Fecal glucocorticoids reflect socio-ecological and anthropogenic stressors in the lives of wild spotted hyenas

Our aim was to identify natural and anthropogenic influences on the stress physiology of large African carnivores, using wild spotted hyenas (Crocuta crocuta) as model animals. With both longitudinal data from a single social group, and cross-sectional data from multiple groups, we used fecal glucocorticoids (fGC) to examine potential stressors among spotted hyenas. Longitudinal data from adult members of a group living on the edge of the Masai Mara National Reserve, Kenya, revealed that fGC concentrations were elevated during two periods of social upheaval among adults, especially among younger females; however, prey availability, rainfall, and presence of lions did not influence fGC concentrations among hyenas. Our results suggested that anthropogenic disturbance in the form of pastoralist activity, but not tourism, influenced fGC concentrations among adult male hyenas; rising concentrations of fGC among males over 12 years were significantly correlated with increasing human population density along the edge of the groups home range. As hyenas from this social group were frequently exposed to anthropogenic disturbance, we compared fGC concentrations among these hyenas with those obtained concurrently from hyenas living in three other groups undisturbed by pastoralist activity. We found that fGC concentrations from the undisturbed groups were significantly lower than those in the disturbed group, and we were able to rule out tourism and ecological stressors as sources of variation in fGC among the populations. Thus it appears that both social instability and anthropogenic disturbance, but not the ecological variables examined, elevate fGC concentrations and represent stressors for wild spotted hyenas. Further work will be necessary to determine whether interpopulation variation in stress physiology predicts population decline in groups exposed to intensive anthropogenic disturbance.

ECOLOGICAL DETERMINANTS OF SURVIVAL AND REPRODUCTION IN THE SPOTTED HYENA

Abstract Large carnivores play a key role in the structuring and dynamics of many ecosystems, yet the factors influencing dynamics of carnivore populations themselves are often poorly understood. Spotted hyenas (Crocuta crocuta) are the most abundant large carnivores in many African ecosystems. We describe demographic patterns in a population of spotted hyenas observed continuously for 15.5 years, and assess the effects of per capita prey availability, interspecific competition, rainfall, anthropogenic disturbance, and disease on 2 key determinants of population dynamics: reproduction and survival. Annual reproduction, survival of juveniles (i.e., recruitment to adulthood), and mortality of adults varied among years of the study. Per capita prey availability and group size both had positive effects on reproduction, whereas interspecific competition with lions had a negative effect. Competition with lions and rainfall both had negative effects on survival of juveniles. We suggest that the negative effect of rainfall on survival may be mediated by increased rates of human–carnivore conflict during periods of heavy rain, although human population size did not influence survival or reproduction directly. Disease had no substantial effect on this hyena population, despite occurrence of at least 2 disease outbreaks among sympatric carnivores during the study. By focusing on demographic processes that determine population growth (i.e., survival and reproduction), this study highlights the importance of both top-down and bottom-up forces acting on populations of large carnivores. These findings also add to a growing literature suggesting that interspecific competition may be more important than previously recognized in the dynamics of populations of large carnivores.

Post-weaning maternal effects and the evolution of female dominance in the spotted hyena

Mammalian societies in which females dominate males are rare, and the factors favouring the evolution of female dominance have yet to be clearly identified. We propose a new hypothesis for the evolution of female dominance and test its predictions with empirical data from the spotted hyena (Crocuta crocuta), a well-studied species characterized by female dominance. We suggest that constraints imposed by the development of a feeding apparatus specialized for bone cracking, in combination with the intensive feeding competition characteristic of spotted hyenas, led to the evolution of female dominance. Specifically, we propose that protracted development of the feeding apparatus in young hyenas led to selection for increased aggressiveness in females as a compensatory mechanism for mothers to secure food access for their young after weaning. Our analyses yielded results consistent with this hypothesis. Morphological and behavioural measurements indicate that skull development is indeed protracted in this species; spotted hyenas do not achieve adult skull size or feeding performance capabilities until after sexual maturity. The period between weaning and completed skull development is particularly challenging, as indicated by high mortality. Finally, maternal presence between weaning and full skull maturity, as well as the relative ability of females to aggressively displace conspecifics from food, are important determinants of offspring survival.

Evolution of environmental cue response mechanisms: adaptive variation in photorefractoriness.

Appropriate timing of transitions between annual cycle stages (reproduction, plumage molt, migration) is critical to fitness for birds living in temporally varying environments. Environmental cue response systems permit birds to orchestrate these transitions. This paper focuses on how photorefractoriness and one neuroendocrine correlate of it (GnRH system plasticity) have evolved to permit appropriate timing of the transition from breeding to plumage molt. Photorefractoriness is defined by two criteria. Criterion 1: photoinduced gonadal regression occurs without any decline in photoperiod. Criterion 2: photoinduced gonadal regression cannot be reversed by increased photoperiod, even continuous light. Through a comparative approach we show that: (1) Loss of Refractoriness Criterion 1 and of GnRH system down-regulation appear to represent adaptive specializations favoring highly temporally flexible or continuous breeding, (2) Refractoriness Criteria 1 and 2 are not always concordant, and Criterion 2 in particular is not well-correlated with degree of temporal reproductive flexibility, (3) occurrence of some cue response traits are better-explained by phylogenetic relationships among taxa than by current reproductive schedules (seasonal, flexible, opportunistic), (4) substantial temporal flexibility can be achieved in a variety of ways besides adaptive modifications of refractoriness, such as relaxation of long-day requirements for reproductive development, and enhancement of non-photic cue responsiveness. These comparisons also highlight fundamental similarities between some of the most opportunistic species and seasonal breeders, such as an autumn reproductive hiatus during molt. Even in the face of substantial environmental unpredictability, selection may often strongly favor regular scheduling of particularly critical life cycle stages such as plumage molt.

Non-photoperiodic regulation of reproductive physiology in the flexibly breeding pine siskin (Spinus pinus)

In order to time reproduction to coincide with favorable conditions, animals use environmental cues to up- and down-regulate the reproductive axis appropriately. Although photoperiodic cues are one of the best studied of such environmental cues, animals also attend to others such as temperature, food availability, rainfall and social cues. Such non-photic cues are expected to be particularly important for tropical species and temperate-zone species that exhibit flexible or opportunistic breeding schedules. In this study, we investigate the use of non-photic cues, specifically food availability and social cues, to time the initiation of reproductive development in the pine siskin (Spinus pinus), a temperate-zone songbird with a flexible breeding schedule. Following winter solstice, males were housed on a 12L:12D photoperiod with either access to a preferred food, a potential mate (social cue), or both. Control birds received only maintenance diet and no mate. Access to a preferred food had a significant positive effect on testis size and circulating luteinizing hormone (LH). However, we found no effect of social treatment on reproductive development. The effect of the food treatment on reproductive development did not appear to result from effects on body mass or fat, as neither measure differed across treatments. The food treatment influenced not only reproductive physiology, but also reproductive behavior in this species, as access to seeds had a positive effect on affiliation of pairs. This study demonstrates that food is a potent stimulus for the initiation of reproductive development in pine siskins.

Seasonal expression of migratory behavior in a facultative migrant, the pine siskin

The vast majority of what is known about migration comes from studies of obligate migration—regular and predictable “to-and-fro” seasonal movements. Much less is known about facultative migration, which occurs less predictably in space and time. Here, we use pine siskins (Spinus pinus), nomadic and irruptive finches, as a captive model to advance our understanding of facultative migration. Building on approaches used to study obligate migration, we investigate whether pine siskins exhibit migratory restlessness in captivity, similar to obligate migrants, and whether pine siskins express a seasonal pattern of migratory behavior. Pine siskins exhibited nocturnal migratory restlessness that was remarkably similar to that in obligate migrants; it was characterized by jumping and wing whirring behavior that was preceded by a period of quiescence. This behavior was expressed seasonally, peaking in the spring, when free-living pine siskins frequently migrate. As in many obligate migrants, migratory restlessness in pine siskins coincided with elevated body condition and showed minimal overlap with body molt. Although pine siskins are both nocturnal and diurnal migrants, patterns of diurnal activity did not mirror patterns of nocturnal activity and were more difficult to interpret. Free-living pine siskins frequently migrate in the fall, but in captivity showed no clear pattern of fall migratory restlessness. We suggest that this could reflect a relatively predictable and programmed spring migration and a more facultative fall migration.Significance statementMigrations are undertaken by a diverse array of animals and are important to the functioning of many ecosystems. The goal of this study was to shed light on an important, but understudied form of migration: facultative migration. Facultative migrations occur less predictably than the better-studied “to-and-fro” seasonal migrations of obligate migrants. Using a songbird, the pine siskin, as a model, we sought to determine if pine siskins express a migratory state in captivity and whether pine siskins exhibit a seasonal pattern of migratory behavior. We found that pine siskins showed behavioral and physiological changes associated with a migratory state, which were remarkably similar to those in obligate migrants. Pine siskins showed seasonal changes in migratory behavior in the study that suggest that this species has a predictable and programmed spring migratory period and a much more flexible fall migration.

Understanding variation in migratory movements: A mechanistic approach

Spatial and temporal fluctuations in resource availability have led to the evolution of varied migration patterns. In order to appropriately time movements in relation to resources, environmental cues are used to provide proximate information for timing and the endocrine system serves to integrate these external cues and behavioral and physiological responses. Yet, the regulatory mechanisms underlying migratory timing have rarely been compared across a broad range of migratory patterns. First, we offer an updated nomenclature of migration using a mechanistic perspective to clarify terminology describing migratory types in relation to ecology, behavior and endocrinology. We divide migratory patterns into three types: obligate, nomadic, and fugitive. Obligate migration is characterized by regular and directed annual movements between locations, most commonly for breeding and overwintering, where resources are predictable and sufficient. Nomadic migrations occur less predictably than do obligate migrations as animals make use of potentially rich but ephemeral resources that occur unpredictably in space or time. Fugitive migrations move animals away from an area in response to severe disruption of environmental conditions and occur as part of an emergency life history stage. We also consider partially migratory populations, which include a mix of sedentary and migratory individuals; the movement patterns of partial migrants are expected to fall into one of the three types above. For these various forms of migration, we review our understanding of the environmental cues and endocrine mechanisms that underlie the expression of a migratory state. Several common hormonal mechanisms exist across the varied migratory forms, but there are also important areas where further investigations are needed in order to gain broad insight into the origin of movements and the diversity of migratory patterns. We propose that taking a comparative approach across the migratory types that considers endocrine mechanisms will advance a new understanding of migration biology.

Variation among individuals in photoperiod responses: Effects of breeding schedule, photoperiod, and age-related photoperiodic experience in birds.

Many organisms use environmental cues to regulate reproductive function in order to time reproduction to coincide with favorable environmental conditions. Whereas we understand much about how environmental cues are used to time reproduction, we know relatively little about variation among individuals in responsiveness to environmental cues. However, this variation among individuals may represent a crucial component of a populations capacity to respond to changing environmental conditions. In this study, we quantify variation among individuals in photoperiod responsiveness of the avian reproductive system and investigate three potential underlying sources of this variation in environmental cue responsiveness. Specifically, we tested whether age-related photoperiodic experience, strength of the photoperiodic cue (day length), and degree of flexibility in breeding schedule influenced the degree of variation observed in experimental studies of seven species of cardueline finches. Overall, we found a high degree of variation among individuals in photoperiod response, and this was influenced by experimental photoperiod and breeding schedule. As experimental photoperiod became longer, the degree of variation declined. Opportunistic breeders showed greater variation in response compared with more seasonal breeders. We found no effect of age-related photoperiodic experience in one species for which we could examine this factor. The results of this study highlight the extent to which individuals can vary in their response to environmental cues and point to both species ecology and characteristics of the cue as important influences on the degree of this variation.