Non-invasive monitoring of glucocorticoid metabolites in brown hyaena (Hyaena brunnea) feces

The brown hyaena (Hyaena brunnea) is the least known of the large predators of southern Africa. The current IUCN status of the brown hyaena is “Near Threatened”, and there are conservation concerns related to a general lack of biological knowledge of the species. For instance, a better knowledge of the responses to environmental and social stressors would improve our abilities to sustainably manage brown hyaena populations in both captive and free‐ranging environments. We conducted adrenocorticotrophic hormone (ACTH) challenges in one female and one male adult brown hyaena at Lion Park Zoo, South Africa, to validate measurements of glucocorticoid metabolites (GCM) in brown hyaena feces via an enzyme immunoassay (EIA). We also measured gastrointestinal transit times (GIT times) and the GCM degradation in feces left in ambient temperature for up to 32 hr to more reliably assess the use of this assay as a tool for non‐invasive glucocorticoid measurements. Intramuscular injections of synthetic ACTH yielded GCM levels of 388% (female) and 2,682% (male) above baseline with peak increases occurring 25‐ to 40‐hr after injection. The time delay of fecal GCM excretion approximately corresponded with food transit time in the brown hyaenas. Fecal GCM levels declined significantly over time since defecation. Our results provided a good validation that fecal GCMs accurately reflect circulating glucocorticoid stress hormones in brown hyaenas, but we highlight that samples have to be frozen immediately after defecation to avoid bias in the measurements as a result of bacterial degredation. Zoo Biol 30:451–458, 2011. © 2010 Wiley‐Liss, Inc.     

Feeding and social behaviour of the striped hyaena (Hyaena vulgaris Desmarest)*

Observations are presented on food, foraging behaviour, ranging and some social behaviour patterns of the striped hyaena; these observations are compared with similar ones on spotted hyaenas. Striped hyaenas are more omnivorous than spotted ones, scavenging a great deal and eating insects, fruits and small vertebrate prey. However, the diets of the two species have several food species in common, and there is competition in the relatively small area where the geographical ranges and habitats of the two hyaenas overlap. Striped hyaenas are solitary, and they show several behavioural adaptations to this. The relationship between the hyaenas' social organization and resource exploitation is discussed.     

The Lion King and the Hyaena Queen: large carnivore interactions and coexistence

Interactions among species, which range from competition to facilitation, have profound effects on ecosystem functioning. Large carnivores are of particular importance in shaping community structure since they are at the top of the food chain, and many efforts are made to conserve such keystone species. Despite this, the mechanisms of carnivore interactions are far from understood, yet they are key to enabling or hindering their coexistence and hence are highly relevant for their conservation. The goal of this review is thus to provide detailed information on the extents of competition and facilitation between large carnivores and their impact in shaping their life histories. Here, we use the example of spotted hyaenas (Crocuta crocuta) and lions (Panthera leo) and provide a comprehensive knowledge of their interactions based on meta‐analyses from available literature (148 publications). Despite their strong potential for both exploitation and interference competition (range and diet overlap, intraguild predation and kleptoparasitism), we underline some mechanisms facilitating their coexistence (different prey‐age selection and scavenging opportunities). We stress the fact that prey abundance is key to their coexistence and that hyaenas forming very large groups in rich ecosystems could have a negative impact on lions. We show that the coexistence of spotted hyaenas and lions is a complex balance between competition and facilitation, and that prey availability within the ecosystem determines which predator is dominant. However, there are still many gaps in our knowledge such as the spatio‐temporal dynamics of their interactions. As both species' survival becomes increasingly dependent on protected areas, where their densities can be high, it is critical to understand their interactions to inform both reintroduction programs and protected area management.     

Feeding ecology and its influence on social organization in Brown hyenas (Hyaena brunnea, Thunberg) of the Central Kalahari Desert

(1) Observations are presented on the diet, feeding habits, hunting and foraging behaviour of Brown hyaenas of the Central Kalahari. (2) The remains of kills left by other predators are the single most important food item in the Brown hyaena's diet. The diet also consists of small scavenged items, small prey such as rodents which the hyaena itself kills, and wild fruits. (3) Brown hyaenas hunt and scavenge small items solitarily, but congregate for communal scavenging of the large kills left by other predators. (4) Individual hyaenas are not territorial and there is great overlap in home ranges. They use common pathways and frequently meet to socialize while foraging. (5) Resident adults form a group with a social hierarchy maintained through neck-biting, muzzle-wrestling, chasing, and other social interactions. Subadult hyaenas often leave the group when approximately 22 months old. (6) Brown hyaenas have a complex system of communication including visual displays, social interactions, vocalizations, and extensive pasting. These are described. (7) Since carrion is an important source of food, Brown hyaenas have developed distinct relationships with other predators and these are described. (8) In conclusion, the Brown hyaena exhibits a highly flexible social system, foraging and hunting small items solitarily and congregating for the common utilization of a large carcass. The social organization is therefore influenced by the feeding ecology.     

Behavioural mechanisms in territory and group maintenance of the brown hyaena,Hyaena brunnea,in the southern Kalahari

Most brown hyaenas (Hyaena brunnea) in the southern Kalahari live in small social groups which inhabit large territories, but the members of a group forage solitarily. The remainder of the population comprise dispersing subadults and nomadic adult males. Aggression is most marked between animals of the same sex from neighbouring territories and in its extreme takes the form of neck-biting. Interactions between group living hyaenas and nomads are less aggressive. Little evidence for a dominance hierarchy amongst group members was obtained and little aggression between group members was observed. Group cohesion is maintained through the greeting ceremony, allogrooming and possibly some forms of muzzle-wrestling. Muzzle-wrestling also seems to be particularly implicated in subadult recruitment and expulsion which are important in regulating group size.     

Limiting factors of Striped Hyaena,Hyaena hyaena,distribution and densities across climatic and geographical gradients (Mammalia: Carnivora)

Few previous studies on the factors that affect Striped Hyaena (Hyaena hyaena Linnaeus, 1758) occurrence and densities were done on geographically unrelated populations using different methodologies. In Israel, hyaenas occur throughout the country's steep climatic and geographical gradients, presenting a unique opportunity to study densities and habitat use across adjacent ecosystems using a unified methodology and test previous conceptions regarding the species’ habitat selection. We collected hyaena abundance-absence data using 1440 camera traps placed at 80 sites (2012– 2016). Site location ranged from hyper-arid deserts to dense Mediterranean shrubland. We assessed the effect of climate, habitat structure, elevation, geomorphological attributes (proxy for den availability), and anthropogenic development (proximity to settlements and agriculture) on hyaena densities using N-mixture models. Hyaena densities were negatively affected by anthropogenic development, and were limited by den availability. Hyaena densities did not follow a climatic or geographic gradient. Densities were highest at hyper-arid deserts and Mediterranean coastal shrublands. Despite the former conception that hyaenas prefer semi-arid open habitats and avoid extreme deserts and dense vegetation, we show that hyaenas use and even thrive in these habitats when geomorphological conditions are suitable and resources are available.     

A seasonal feast: long-term analysis of feeding behaviour in the spotted hyaena (Crocuta crocuta)

The feeding behaviour of the Talek clan of spotted hyaenas in the Masai Mara National Reserve, Kenya, was monitored continuously for 7 years. Talek hyaenas adapted to large temporal variations in prey abundance by being opportunistic predators. During the first half of the year, the hyaenas fed on resident ungulates, and their diet consisted mainly of topi and Thomson's gazelles. Upon arrival of the migratory herds of wildebeest and zebra from the Serengeti, Talek hyaenas switched to feeding on the wildebeest which provided them with a superabundance of food for about 3 months. After the migratory animals returned to the Serengeti, Talek hyaenas experienced a period of reduced prey abundance due to the temporary dispersion of resident ungulates. At this time hyaenas hunted the few remaining wildebeest, and also increased their use of the remaining resident animals. Although Talek hyaenas were generally opportunistic in their feeding behaviour, they did exhibit clear dietary preference for larger prey species, particularly wildebeest. Finally, carrion comprised only 5% of the biomass consumed by Talek hyaenas, the lowest proportion of carrion in the diet of any Crocuta population studied to date.     

The scent-marking behaviour of the spotted hyaena Crocuta crocuta in the southern Kalahari

All hyaenas scent mark their territories by smearing grass stems with paste from their subcaudal scent glands and by depositing faeces at latrines, but they adopt different strategies in terms of how they disperse these scent marks in their territories. For example, brown hyaenas living in the southern Kalahari deposit pastes and latrines throughout the whole of their territory, while spotted hyaenas living in the Ngorongoro Crater of East Africa place their scent marks strictly along the territorial borders. We have argued elsewhere (Gorman & Mills, 1984) that these different strategies are not species-specific but are instead adaptive responses to local conditions. Here, we use data from a population of spotted hyaenas, living in small clans and large territories in the Kalahari, to test the hypothesis that hinterland marking is a response to the problem of marking a very large territory with a limited amount of scent and within a limited time budget.     

Social dominance and feeding patterns of spotted hyaenas

In some parts of East Africa, spotted hyaenas (Crocuta crocuta) live in large groups and at high population densities, and scramble competition among clan members during feeding at large carcasses is reported. By contrast, spotted hyaenas in the Namib Desert of southwestern Africa live in small groups and at low densities. When assembled at carcasses, Namib Desert spotted hyaenas show linear dominance hierarchies. Adult females outrank adult males and usually feed one at a time or with their dependent offspring. Feeding rates at small carcasses in the Namib Desert are approximately equal to those reported in East Africa, but at large carcasses Namib Desert spotted hyaenas show linear dominance hierarchies. Adult females outrank adult males and usually feed one at a time or with their dependent offspring. Feeding rates at small carcasses in the Namib Desert are approximately equal to those reported in East Africa, but at large carcasses Namib Desert spotted hyaenas feed significantly more slowly. Thus lower-ranking individuals eventually gain access to large carcasses but are excluded from smaller ones. We relate these patterns of food consumption to possible evolutionary pathways to social hunting by spotted hyaenas.     

Space and resource use by brown hyenas Hyaena brunnea in the Namib Desert

Two clans of brown hyenas were studied on the arid chilly Namib Desert coast where very large seal colonies are present. Carcasses from seals were abundant during summer and autumn following the seal pupping season, and scarce in winter and spring. Hyenas fed predominantly on carcasses. Members of one clan of three hyenas obtained most of their food along 3 km of coastline adjacent to the seal colonies. The other clan of nine individuals obtained food from an area along 6 km of coastline north of the seal colonies. Although carcasses were usually scavenged, seal pups were seen to be killed on occasions. Time spent foraging was not affected by carcass availability. Territories of the two clans overlapped and individual home-range size varied from 31.9 to 220 km². Food availability apparently had no influence on foraging activities but the dispersal of food affected territory and group sizes. Over abundance of food results in the maintenance of territories extending beyond the distribution of food. The shape and area of these territories may result from the cultural inheritance of space.     

Optimal hunting group size: the need for lions to defend their kills against loss to spotted hyaenas

This paper presents preliminary evidence that kleptoparasitism by spotted hyaenas may influence optimal hunting group size of lions. In the absence of adult male lions, hyaenas can drive female and subadult lions off their kills provided they outnumber the lions by a factor of four. Hence the larger the group of lions on the kill, the greater their chance of defending their food against invading hyaenas. At Savuti, where there was a shortage of adult male lions, the groups of female and subadult lions lost almost 20% of their food to hyaenas. Losses were most frequent for those living in small groups. These lions were often satiated by the time the hyaenas acquired the kill, so the hyaenas did not cause immediate need, yet constituted a constant energy drain on lions by forcing them to hunt more frequently. The implications of these observations for modelling optimal hunting group size of lions are discussed.     

Weather dependent behaviour of captive striped hyaenas (Hyaena hyaena)

The frequencies of 4 behaviour patterns (lying down, comfort movements, scent-marking and social time) of two captive striped hyaenas collected by the one-zero-sampling method on 16 observations between May and December 1974 at the Zurich Zoological Garden were correlated with the local equivalent temperature (T_eq). The frequencies of lying down and comfort movements increased with higher T_eq (positive correlation), while scent-marking decreased (negative correlation). Social time was not affected by the prevailing thermal conditions.     

Patterns of scavenger arrival at cheetah kills in Serengeti National Park Tanzania

Scavenging by large‐bodied vertebrates is observed in many ecosystems but has rarely been quantified. Here we document the timing and order of scavenger arrival at 639 cheetah kills in Serengeti National Park, Tanzania, focusing on ecological and heterospecific factors that may impact detectability of carcasses. We found that small‐, medium‐ and large‐sized vultures, jackals, spotted hyaenas and lions were more likely to be present at the carcasses of large‐bodied than small‐bodied prey. Lions and spotted hyaenas were less likely to locate kills in tall grass; medium‐sized vultures were likely to arrive before both large‐ and small‐sized vultures. Spotted hyaenas and vultures were likely to be present at kills simultaneously. Despite numerous anecdotal accounts, we did not find that hyaenas use alighting vultures as a means of locating food. Our findings show that environmental variables and other scavenger species strongly influence scavenger arrival at carcasses in this ecosystem.     

Factors affecting group size and territory size of the Brown hyaena, Hyaena brunnea in the southern Kalahari

The paper describes how the dispersion pattern of food affects group size and territory size in the brown hyaena in different ways. Territory size is affected by the distribution of the food, group size by the quality of the food in the territory.     

Dyadic associations reveal clan size and social network structure in the fission–fusion society of spotted hyaenas

Estimating the size and dynamics of populations is of paramount importance in ecology. In species with uniquely marked individuals, capture–recapture methods can be used to establish population size and to explore associations between individuals. However, very few studies have used cameras traps to focus on group composition in social carnivores, despite being of particular interest in species characterised by “fission–fusion” formation of sub-groups. Here, we provide estimates of (a) population size, (b) density, (c) clan size, (d) association patterns and (e) social network structure in spotted hyaenas (Crocuta crocuta) based on images from camera traps deployed at waterholes on Ongava Game Reserve (northern Namibia). In a 15 week study period, we identified 32 individuals. Dyadic associations and the resulting social network showed that all but two hyaenas associated directly or indirectly with each other, indicating the presence of one clan of at least 30 individuals, resulting in a density of 8.1 hyaenas/100 km². We found a very high variability in the tendency of individuals to associate with others. This study confirms a highly dynamic fission–fusion society in spotted hyaenas. We argue that camera traps can provide relevant insights into large carnivore social network structure where associations between individuals are difficult to observe directly.     

The predicament of the African wild dog,Lycaon pictus,is less precarious than claimed

In a paper published fifteen years ago, Gorman et al. (Nature 391 , 479–481) made precise claims about how sensitive the African wild dog is to kleptoparasitism by spotted hyaenas Crocuta crocuta and lions Panthera leo. These claims are regularly referred to in the literature, and so far, they have remained unchallenged. However, careful perusal of their paper and analysis of the available data on energy intake and expenditure by wild dogs show that their claims are unfounded. Contrary to Gorman et al., wild dogs can usually take loss of food by kleptoparasitism in their stride. We present the calculations of the energy budget of wild dogs that remain implicit in the paper by Gorman et al.     

Activity patterns of reintroduced lion Panthera leo and spotted hyaena Crocuta crocuta in the Addo Elephant National Park, South Africa

Africa's large predator guild competes for a limited food resource base. To minimize the degree of competition, we hypothesized that the two largest members of this guild and its fiercest competitors, the lion and the spotted hyaena, would partition their activity patterns to avoid interacting. We used 96‐h continuous follows of focal animal(s) to determine when the six radio‐collared lions and eight radio‐collared spotted hyaenas, reintroduced into Addo Elephant National Park in 2003/2004, were active using a binomial measure of activity which was defined as movements >100 m during each hourly period. Contrary to our predictions, lions and hyaenas did not partition their activity times, probably because of their current low population densities. Both species exhibited a crepuscular activity pattern although hyaenas were far less active during daylight. A sub‐adult lioness minimized competitive interactions by becoming diurnal. This is likely to be a common strategy for lions that have been expelled from their natal pride to become nomadic, as it allows them to minimize kleptoparasitic and agonistic interactions from competitively dominant conspecifics and competitors. The increase in testosterone that occurs in males upon reaching sexual maturity, darkens their pelage and causes them to be more directly impacted by the heat, and thereby affords females an opportunity to escape from males during hot temperatures. Similarly, the longer pelage of young hyaenas restricts their activity to the cooler night‐time.     

How much does a spotted hyaena eat? Perspective from the Namib Desert

The amount of food consumed by a clan of spotted hyaenas in the Namib desert was determined gravimetrically for 19 nights and the amount consumed by each individual was calculated according to its feeding time budget. At large, fleshy ungulate carcasses, each adult clan member ate about 8.7kg nightly, except for the bottom-ranking male, who obtained only half that amount per night. Skin and bone remains were consumed at a slower rate of 2kg/hyaena/night. Medium-sized ungulates were devoured rapidly so that each hyaena obtained more during such feeding nights than at large carcasses. Over a 29 day period, a hyaena clan consumed five cacasses at a rate of 4.0kg/hyaena/day, which compared well with previous estimates of average daily consumption in large social carnivores studied elsewhere. Annually, sixteen Namib hyaenas ate some 4.8% of the ungulate bio-mass, removing, in terms of numbers 14.3% of the gemsbok and 2.2% of the mountain zebra. This depletion did not appear to limit these populations.     

Vertical distribution and substrate preference of brown trout in a littoral zone

Synopsis We studied vertical distribution, substrate preference and food choice of brown trout, Salmo trutta, from benthic gillnet catches at four littoral sampling locations in a Norwegian hydroelectric reservoir. The sampling locations had different bottom substrates; at one location the bottom substrate consisted of sand, while at the other three, substrates consisted of stones ranging 2–5 cm, 10–30 cm and 30–150 cm in diameter, respectively. Small-sized (< 160 cm) and intermediate-size (164–269 mm) brown trout were mainly caught close to the bottom (0–0.5 m above). Small-sized brown trout were caught in the highest frequency at the location with substrate consisting of 10–30 cm large stones. Intermediate-sized brown trout were also caught in highest frequency at this location, but were also caught in a high frequency at the location with sandy substrate. In contrast, the catches of large-sized ( 270 mm) brown trout did not vary with distance from the bottom or with substrate coarseness. The most important food items for the brown trout were aquatic insects, surface insects, Eurycercus lamellatus and crustacean zooplankton, mainly Daphnia longispina, Bythotrephes longimanus, and Holopedium gibberum. In accordance with the differences in vertical distribution, benthic food was more important to small than to large brown trout. We argue that small brown trout stayed close to the bottom to reduce aggressive behaviour from larger specimens, and that small brown trout were therefore more dependent on benthic food items. We also argue that the observed differences in substrate preference between the size groups of brown trout is explained by variation in access to shelter, visual isolation between individuals and benthic feeding conditions between locations.     

Prey preferences of the spotted hyaena (Crocuta crocuta) and degree of dietary overlap with the lion (Panthera leo)

Spotted hyaenas Crocuta crocuta were once considered mere scavengers; however, detailed research revealed that they are very efficient predators. Information on what spotted hyaenas actually prefer to prey on and what they avoid is lacking, as well as the factors that influence prey selection. Data from 14 published and one unpublished study from six countries throughout the distribution of the spotted hyaena were used to determine which prey species were preferred and which were avoided using Jacobs' index. The mean of these values for each species was used as the dependent variable in multiple regression, with prey abundance and prey body mass as predictive variables. In stark contrast to the rest of Africa's large predator guild, spotted hyaenas do not preferentially prey on any species. Also surprisingly, only buffalo, giraffe and plains zebra are significantly avoided. Spotted hyaena most prefer prey within a body mass range of 56–182 kg, with a mode of 102 kg. The dietary niche breadth of the spotted hyaena is similar to that of the lion Panthera leo , and the two species have a 58.6% actual prey species overlap and a 68.8% preferred prey species overlap. These results highlight the flexible and unselective nature of spotted hyaena predation and are probably a reason for the species' success throughout its range, despite a large degree of dietary overlap with lions.