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.     

Carcass size shapes the structure and functioning of an African scavenging assemblage

The particle size of the food resource strongly determines the structure and dynamics of food webs. However, the ecological implications of carcass size variation for scavenging networks structure and functioning have been largely overlooked. Here we investigate differences in scavenging patterns due to carcass size in a complex vertebrate scavenger community, Hluhluwe‐iMfolozi Park, South Africa, while taking into account seasonality. We monitored the consumption of three types of experimental carcasses: ‘small’ (< 10 kg), ‘medium’ (10–100 kg) and ‘large’ (> 100 kg). We employed general lineal models to explore the influence of carcass size on 1) scavenging network structure (scavenger species richness per carcass) and 2) functioning (carcass detection time, consumption time, consumption rate and percentage of carrion consumed). We also tested whether the structure of the scavenging network of each carcass size was nested, i.e. whether the scavenging assemblage in species‐poor carcasses was a subset of the assemblage consuming species‐rich carcasses. We found strong evidence indicating that carcass size is a major factor governing the associated scavenger assemblage. Scavenger species richness per carcass and carcass consumption time and rate increased with carcass size, while carcass detection time and percentage of carrion biomass consumed were negatively related to carcass size. Strikingly, most of the carrion biomass was consumed by facultative scavengers, represented by large mammalian carnivores, rather than by obligate scavengers (i.e. vultures). Scavenging network nestedness tended to be higher at larger carcasses, and nestedness was sensitive to the removal of the most connected species in the network (spotted hyena) rather than vultures. When comparing scavenging and predation assemblages, crucial size‐dependent differences emerge. Also, we identified a traditionally ignored mechanism by which hunting large prey could be relatively less profitable for predators, namely the costs associated with competition from scavengers and decomposers.     

The role of griffon vultures Gyps africanus and Gyps ruppellii as scavengers

In the Serengeti, predator kills formed from 8 to 45 % of the carcasses that griffon vultures fed upon, the remaining carcasses coming from animals that had died from other causes. But since vultures obtained only very small amounts of food from predator kills, they had to rely for their food supply chiefly on the carcasses that were derived from other causes. In the Serengeti the large proportion of migratory ungulates prevent the mammalian predators from building up to a population size that can be responsible for a large proportion of ungulate mortality. It is estimated that the mammalian predators only take about one quarter of the potential food supply available for carnivores. The remaining ungulates die from various other causes, and so provide food for scavengers which varies in abundance and location with the seasons. This is a food supply which mammalian scavengers cannot easily use but griffon vultures, with their adaptations for gliding flight, are able to exploit it. These vultures therefore exploit a basically different food supply from predators and probably evolved as scavengers of migratory ungulate populations.     

Effects of vulture exclusion on carrion consumption by facultative scavengers

Vultures provide an essential ecosystem service through removal of carrion, but globally, many populations are collapsing and several species are threatened with extinction. Widespread declines in vulture populations could increase the availability of carrion to other organisms, but the ways facultative scavengers might respond to this increase have not been thoroughly explored. We aimed to determine whether facultative scavengers increase carrion consumption in the absence of vulture competition and whether they are capable of functionally replacing vultures in the removal of carrion biomass from the landscape. We experimentally excluded 65 rabbit carcasses from vultures during daylight hours and placed an additional 65 carcasses that were accessible to vultures in forested habitat in South Carolina, USA during summer (June–August). We used motion‐activated cameras to compare carrion use by facultative scavenging species between the experimental and control carcasses. Scavenging by facultative scavengers did not increase in the absence of competition with vultures. We found no difference in scavenger presence between control carcasses and those from which vultures were excluded. Eighty percent of carcasses from which vultures were excluded were not scavenged by vertebrates, compared to 5% of carcasses that were accessible to vultures. At the end of the 7‐day trials, there was a 10.1‐fold increase in the number of experimental carcasses that were not fully scavenged compared to controls. Facultative scavengers did not functionally replace vultures during summer in our study. This finding may have been influenced by the time of the year in which the study took place, the duration of the trials, and the spacing of carcass sites. Our results suggest that under the warm and humid conditions of our study, facultative scavengers would not compensate for loss of vultures. Carcasses would persist longer in the environment and consumption of carrion would likely shift from vertebrates to decomposers. Such changes could have substantial implications for disease transmission, nutrient cycling, and ecosystem functioning.     

Interactive effects of obligate scavengers and scavenger community richness on lagomorph carcass consumption patterns

Carrion consumption patterns in vertebrate scavenger communities may be influenced by several interacting factors. We assessed the effects of the number of scavenger species and the presence of obligate scavengers (vultures) on carcass detection and consumption times, and the structure (nestedness) of the scavenger assemblage by exploring consumption patterns of lagomorph carcasses provided experimentally. Carcass detection and consumption times were strongly inversely related to vulture presence, whereas scavenger richness had a low contribution, except when interacting with vulture presence. However, none of the scavenger communities presented a nested pattern, perhaps because of the small size of lagomorphs, which prevents large numbers of scavengers and interspecific interactions occurring at one carcass. Our results suggest that scavenger species richness, especially the presence of vultures, increases scavenging efficiency.     

A dead giveaway: Foraging vultures and other avian scavengers respond to auditory cues

Carrion represents an unpredictable and widely distributed primary food source for vultures and other avian scavengers. Avian scavengers in African savanna ecosystems are reported to rely exclusively on visual stimuli to locate carcasses. However, carnivores’ predation of large mammalian herbivores and subsequent competition for access to the carcass can result in considerable noise, often audible over long distances and for prolonged periods. Vultures and other avian scavengers may therefore detect and respond to these auditory cues, as do the mammalian carnivores alongside which vultures have coevolved, but this has not been investigated to date. Working in the Serengeti ecosystem, Tanzania, we used diurnal auditory broadcasts to simulate predation and competitive carnivore feeding interactions. Based on the current understanding of avian scavenger ecology, we hypothesized that avian responses to call‐in stations would be evoked exclusively by visual, rather than auditory, cues. We therefore predicted that (a) the arrival of avian scavengers at call‐in stations should be preceded and facilitated by mammalian carnivores and that (b) the arrival of avian scavengers would be positively correlated with the number of mammalian scavengers present, which would increase detectability. We recorded 482 birds during 122 separate playback events. In 22% of these instances, avian scavengers arrived first, ruling out responses based exclusively on visual observations of mammalian carnivores, thereby contradicting our first prediction. Furthermore, the first avian arrivals at survey sessions were inversely related to the number of hyenas and jackals present, contradicting our second prediction. Since no bait or carcasses were used during the experiments, these responses are indicative of the birds’ ability to detect and respond to audio stimuli. Our findings challenge the current consensus of sensory perception and foraging in these species and provide evidence that avian scavengers have the ability to use sound to locate food resources.     

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.     

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.     

Trophic Facilitation or Limitation? Comparative Effects of Pumas and Black Bears on the Scavenger Community

Scavenging is a widespread behaviour and an important process influencing food webs and ecological communities. Large carnivores facilitate the movement of energy across trophic levels through the scavenging and decomposition of their killed prey, but competition with large carnivores is also likely to constrain acquisition of carrion by scavengers. We used an experimental approach based on motion-triggered video cameras at black-tailed deer (Odocoileus hemionus columbianus) carcasses to measure the comparative influences of two large carnivores in the facilitation and limitation of carrion acquisition by scavengers. We found that pumas (Puma concolor) and black bears (Ursus americanus) had different effects on their ecological communities. Pumas, as a top-level predator, facilitated the consumption of carrion by scavengers, despite significantly reducing their observed sum feeding times (165.7 min±21.2 SE at puma kills 264.3 min±30.1 SE at control carcasses). In contrast, black bears, as the dominant scavenger in the system, limited consumption of carrion by scavengers as evidenced by the observed reduction of scavenger species richness recorded at carcasses where they were present (mean = 2.33±0.28 SE), compared to where they were absent (mean = 3.28±0.23 SE). Black bears also had large negative effects on scavenger sum feeding times (88.5 min±19.8 SE at carcasses where bears were present, 372.3 min±50.0 SE at carcasses where bears were absent). In addition, we found that pumas and black bears both increased the nestedness (a higher level of order among species present) of the scavenger community. Our results suggest that scavengers have species-specific adaptions to exploit carrion despite large carnivores, and that large carnivores influence the structure and composition of scavenger communities. The interactions between large carnivores and scavengers should be considered in future studies of food webs and ecological communities.     

Temporal resource partitioning mediates vertebrate coexistence at carcasses: The role of competitive and facilitative interactions

Unravelling how biodiversity is maintained despite species competition for shared resources has been a central question in community ecology, and is gaining relevance amidst the current biodiversity crisis. Yet, we have still a poor understanding of the mechanisms that regulate species coexistence and shape the structure of assemblages in highly competitive environments such as carrion pulsed resources. Here, we study how large vertebrates coexist in scavenger assemblages by adapting their diel activity at large ungulate carcasses in NW Spain. We used camera traps to record vertebrate scavengers consuming 34 carcasses of livestock and hunted wild ungulates, which allowed us to assess also differences regarding carcass origin. To evaluate temporal resource partition among species, we estimated the overlap of diel activity patterns and the mean times of each scavenger at carcasses. We recorded 16 species of scavengers, 7 mammals and 9 birds, and found similar richness at both types of carcasses. Birds and mammals showed contrasting diel activity patterns, with birds using carcasses during daytime (mean= 11:38 h) and mammals mostly at night (23:09 h). The unimodal activity patterns of scavengers showed asynchronous peaks among species. Subordinate species modified their activity patterns at carcasses used by apex species to reduce temporal overlap. Also, diel activity patterns of vultures closely followed those of corvids, suggesting facilitation processes in which corvids would enhance carcass detection by vultures. Two mammal species (12.5%) increased nocturnality at carcasses of hunted ungulates, which could be a response to human disturbance. Our results suggest that both temporal segregation and coupling mediate the coexistence of large vertebrates at carcasses. These mechanisms might lead to richer scavenger assemblages and thereby more efficient ones in driving critical ecosystem functions related to carrion consumption, such as energy and nutrient recycling and biodiversity maintenance.     

Bone crushing carnivores and their significance to osteodystrophy in griffon vulture chicks

The natural removal of 89 ungulate carcasses by predators and scavengers was monitored in various wildlife reserves and ranching areas of South Africa. Carnivores responsible for the bone remains were determined. Spotted hyaenas and, to a lesser extent, Brown hyaenas, were the only carnivores that regularly chewed bones. When hyaenas were absent, months of weathering were required before the smaller bones became disarticulated and able to be removed by vultures. The bone-collecting behaviour and related aspects of breeding of two species of griffon vulture were studied at five different nesting colonies in southern Africa—one Cape vulture colony and one White-backed vulture colony in or near wildlife reserves, as well as two Cape vulture colonies and one White-backed vulture colony in ranching land. A total of 2825 bones was found in or below the vulture nests. These bones were categorized and measured. Hyaena-produced bone fragments were found only in the colonies in the wild areas—none of the 387 chicks examined here had osteodystrophy (metabolic bone disease). By contrast, in the ranching areas, vultures collected larger and less fragmented bones. Many Cape vulture chicks had osteodystrophy (130 of 1917 examined), as did two White-backed vulture chicks (of 196 examined). In 1977, artificial feeding stations, 'restaurants' where carcass skeletons were crushed, were established for Cape vultures. Since then, the incidence of osteodystrophy has declined from 17% to 2–5% in 1983. It is clear that bone fragments are an essential dietary requirement, providing calcium for correct skeletal growth of griffon vulture chicks.     

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.     

Pattern and process in the distribution of North American freshwater fish

Published species lists were analysed to determine the contributions of dispersal, habitat preference, river channel size, body size, and glacial history to large‐scale patterns in freshwater fish species richness in North America, north of central Mexico. Total species richness declines to the north and west but the pattern for endemics differs from that of widespread species. Mississippi Basin regions are more species rich than more isolated, coastal, regions. Richness declines more rapidly with increasing latitude in riverine specialist than in habitat generalist species. Levels of endemism are greatest in species found in small‐ to medium‐sized river channels. The strong Rapoport effect, more marked in migratory than resident species, is correlated with habitat preference, channel size, and glacial history. Body size increases with latitude, largely as a result of a trend from small resident to large migrant species. In unglaciated regions, ancestral species survived in large habitats because these are longer‐lived, more extensive, less isolated and more stable than headwaters, permitting larger populations and lower extinction levels. Reduced levels of gene flow in small, peripheral, channels isolated by larger downstream habitats have resulted in the production of many, small range, small‐bodied species. The latitudinal richness gradient is a consequence of speciation and extinction events in unglaciated faunas and an increasing domination of faunas by generalist, large bodied, large channel, recolonizing species in more northern regions. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 46–61.     

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.     

Dry wildebeest carcasses in the African savannah: the utilization of a unique resource

Utilization of dry wildebeest carcasses by spotted hyaena in an African savannah setting is investigated. Four transects of varying length (3–10 km) were located in the Maasai Mara National Reserve, Kenya. Measuring carcass weight changes biweekly over a period of 9 months monitored hyaena use of dry wildebeest carcasses. Nutrient quality of dry carcasses (skin and bone) and of flesh was analysed in the laboratory using the material collected in the field. Contrary to common expectation, carcass weight change was significantly higher when the migrants were present in the Reserve than when they were absent in all transects monitored. This is thought to indicate greater carcass utilization during periods of relative prey scarcity caused by the migratory herd movements within the Reserve, and perhaps, the territorial nature of spotted hyaenas. Nutrient analysis indicated that dry carcasses contain significant amounts of protein, carbohydrates and minerals, although lacking in fats compared with flesh. The opportunistic nature and evolution of a digestive physiology in this species capable of utilizing dry carcasses appears to have important adaptive value in an environment frequented by thousands of migrant herbivores for short periods every year.     

Niche variation and the maintenance of variation in body size in a burying beetle

1. In burying beetles (Nicrophorinae), body size is known to provide both a fecundity advantage (in females) and successful resource defence (in males and females). Despite this, considerable variation in body sizes is observed in natural populations. 2. A possible explanation for the maintenance of this variation, even with intra‐ and inter‐specific resource competition, is that individuals might assort according to body size on different‐sized breeding resources. 3. We tested prediction that ‘bigger is always better’, in the wild and in the laboratory, by experimentally manipulating combinations of available breeding‐resource size (mouse carcasses) and competitor's body size in Nicrophorus vespilloides (Herbst 1783). 4. In the field, large female beetles deserted small carcasses, without breeding, more often than they did larger carcasses, but small females used carcasses indiscriminately with respect to size. In the laboratory, large beetles reared larger broods (with more offspring) on larger carcasses than small beetles, but on small carcasses small beetles had a reproductive advantage over large ones. Offspring size covaried with carcass size independently of parental body size. 5. The present combined results suggest breeding resource value depends on an individual's body size, and variation in body size is environmentally induced: maintained by differences in available carcass sizes. This produces a mechanism by which individual specialisation leads to an increase in niche variation via body size in these beetles.     

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.     

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.     

Vultures acquire information on carcass location from scavenging eagles

Vultures are recognized as the scroungers of the natural world, owing to their ecological role as obligate scavengers. While it is well known that vultures use intraspecific social information as they forage, the possibility of inter-guild social information transfer and the resulting multi-species social dilemmas has not been explored. Here, we use data on arrival times at carcasses to show that such social information transfer occurs, with raptors acting as producers of information and vultures acting as scroungers of information. We develop a game-theoretic model to show that competitive asymmetry, whereby vultures dominate raptors at carcasses, predicts this evolutionary outcome. We support this theoretical prediction using empirical data from competitive interactions at carcasses. Finally, we use an individual-based model to show that these producer–scrounger dynamics lead to vultures being vulnerable to declines in raptor populations. Our results show that social information transfer can lead to important non-trophic interactions among species and highlight important potential links among social evolution, community ecology and conservation biology. With vulture populations suffering global declines, our study underscores the importance of ecosystem-based management for these endangered keystone species.     

Antibiotics threaten wildlife: circulating quinolone residues and disease in Avian scavengers

Antibiotic residues that may be present in carcasses of medicated livestock could pass to and greatly reduce scavenger wildlife populations. We surveyed residues of the quinolones enrofloxacin and its metabolite ciprofloxacin and other antibiotics (amoxicillin and oxytetracycline) in nestling griffon Gyps fulvus, cinereous Aegypius monachus and Egyptian Neophron percnopterus vultures in central Spain. We found high concentrations of antibiotics in the plasma of many nestling cinereous (57%) and Egyptian (40%) vultures. Enrofloxacin and ciprofloxacin were also found in liver samples of all dead cinereous vultures. This is the first report of antibiotic residues in wildlife. We also provide evidence of a direct association between antibiotic residues, primarily quinolones, and severe disease due to bacterial and fungal pathogens. Our results indicate that, by damaging the liver and kidney and through the acquisition and proliferation of pathogens associated with the depletion of lymphoid organs, continuous exposure to antibiotics could increase mortality rates, at least in cinereous vultures. If antibiotics ingested with livestock carrion are clearly implicated in the decline of the vultures in central Spain then it should be considered a primary concern for conservation of their populations.