Research Group 1: Evolutionary Ecology

THE SPOTTED HYAENA PROJECT

This long-term project studies two ecologically distinct spotted hyena (Crocuta crocuta) populations in the Serengeti ecosystem (Serengeti: Serengeti National Park; and Crater: Ngorongoro Crater). Life histories of several hundred individually known hyenas have been monitored since 1987 in the Serengeti population, and similar data have been obtained from the entire spotted hyena population on the floor of the Ngorongoro Crater since 1996.

The spotted hyena is a model species for testing hypotheses proposed to explain the function, effect on the endocrine system and evolution of several unique traits displayed by this species such as female dominance, the masculinisation of the female clitoris, facultative siblicide, and males that queue for social status. Because the penile clitoris provides females with control over copulation, the spotted hyena is an ideal species for research on sexual conflict and the effect of female mate choice on male mating tactics and male reproductive success.

In the Serengeti, food availability in spotted hyena clan territories is low during many months each year due to the long-distance annual migratory movements of their main prey species (Hofer & East 1995). In contrast, food availability within or in close vicinity of hyena clan territories in the Crater is high all year round (Höner et al. 2005). The Serengeti ecosystem is thus an ideal study site to test ideas concerning the effect of prey abundance on various aspects of hyena ecology and behaviour. Exceptionally high maternal investment and rank related access to food resources make the spotted hyena a model species for research on socially mediated effects of maternal input on offspring survival.

As the most numerous large carnivore in the Serengeti ecosystem, the spotted hyena is an important component of the large carnivore community and plays a cucial role in predator-prey dynamics in both the Serengeti NP and Ngorongoro Crater. Theoretical models of host-pathogen interactions are rarely tested in natural ecosystems, even though pathogens are an important component of ecosystem processes. The sociality, extensive ranging behaviour and broad diet of spotted hyenas make them a useful species for extending our knowledge of host-pathogen research.

Predation of livestock in areas close to the boundary of the Serengeti National Park, and within the Ngorongoro Conservation Area, leads to conflict between spotted hyenas and livestock owners. Currently, the most important cause of mortality among adult spotted hyenas in the Serengeti population is by-catch in wire snares set by game-meat hunters for herbivores.

1. Ecological Processes
2. Evolutionary Biology
3. Hormones and Behaviour
4. Conservation Biology

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Hyena group publications

The backbone of this multi-disciplinary approach is long-term field research in the Serengeti National Park and Ngorongoro Conservation Area. This field research is closely linked to laboratory investigations and the development and application of theoretical models.

More about the ecology of the spotted hyaena

1. Ecological Processes

The impact of food resources on hyena society and individuals

Access to food resources in a hyena territory is determined by social status and because hyena society is female dominated, top ranking females consume more of the food resources with a clan territory than their social subordinates. Preferential access to food permits socially dominant mothers to supply their offspring with milk more often than more subordinate mothers, and as a result their cubs grow faster rate and are more likely to survive (Hofer & East 2003).

When prey abundance in a hyena territory is low, competition for food among clan members increases. This conflict is resolved by dominant hyenas feeding more often ‘at home’ and subordinates foraging outside their ‘home’ territory either locally (Höner et al. 2005) or at distances up to 70km from their ‘home’ territory (Hofer & East 1995). These foraging decisions conform to predictions derived from the ideal free distribution (Höner et al. 2005).

Population dynamics

Predator-prey dynamics

Spotted hyenas are generalist carnivores that hunt and scavenge on a large number of different herbivore species. Substantial long-term changes in the sizes of the main prey populations of hyenas in the Ngorongoro Crater caused hyenas to exhibit a functional response and to kleptoparasitise more food from lions (Panthera leo), their main competitor for food (Höner et al. 2002).

Competition within carnivore communities

In many African ecosystems spotted hyenas and lions are the most numerous large carnivores and due to overlapping diets they often compete for the same food resources. The success of hyenas to kleptoparasitise lions is influenced by the presence of male lions and the ability of hyenas to recruit sufficient group members to appropriate carcasses from female and subadult lions (Höner et al. 2002).

Pathogens

Research on pathogens in wildlife is often confined to single pathogens that cause epidemics, and to periods when epidemics occur and mortality rates are noticeable. Yet, pathogens that cause less conspicuous levels of mortality, or have other fitness consequences may have an important evolutionary and ecological impact on host species and ecosystem dynamics.

Rabies

Long-term monitoring of rabies in the Serengeti National park (NP) has revealed a constant high level of exposure (37%) to rabies and genetic analyses of rabies virus from spotted hyenas inside the Serengeti NP have revealed the presence of the only known non-pathogenic rabies variant in a carnivore species. Serengeti spotted hyenas maintain a variant of the canid serotype 1 virus, and comparison of a 381 bp segment of the N-P gene demonstrates that the hyena variant has a 8.5% sequence divergence from the variant of canid serotype 1 established in the Tanzanian domestic dog population and in other small carnivores in the Serengeti National Park (NP). Despite 37% exposure to rabies among Serengeti hyenas, and demonstration of the presence of the virus using RT-PCR techniques in 13% of Serengeti hyenas, neither infection nor exposure influenced the survival or longevity of individually know spotted hyenas monitored for many years (East et al. 2001). Despite an extensive rabies epidemic among domestic dogs in villages outside but close to the boundaries of the Serengeti NP in 2003 and 2004, no increase in the incidence of rabies occurred among spotted hyenas within the Serengeti NP.

Canine Distemper Virus

Several hundred individually known spotted hyenas in the Serengeti NP have been monitored since 1987, and during this period one epidemic of canine distemper has occurred, causing high mortality in young hyenas in 1993/1994. The genetic variant isolated from spotted hyenas also caused mortality in the lion population (Haas et al. 1996; Carpenter et al. 1998).

Coronavirus

 Recently, a novel strain of coronavirus was found in spotted hyenas in the Serengeti ecosystem. Infection with this virus does not induce obvious clinical signs, and active excretion of virus is mainly confined to young hyenas (East et al. 2004).

Streptococcus

  During a relatively defined period between September 2002 and February 2003, spotted hyenas on the floor of the Ngorongoro Crater showed clinical signs, including swollen heads, abscises on the lower jaw, ataxia and death in some cases. Phenotypic examination and phylogenetic analysis of the 16S rRNA gene of the causative agent of infection revealed a Lancefield group C Streptococcus with a high level of homology to S. equi subsp. ruminatorum, a subspecies of S. equi recently described in domestic sheep (Ovis aries) and goats (Capra hircus) with mastitis in Spain. Strains similar to this bacterium were also isolated from hyenas without obvious clinical signs, and from a sympatric Burchell’s zebra (Equus burchelli), a herbivore species often consumed by hyenas (Höner et al. in press).

spotted hyena with streptococcus infection

2. Evolutionary Biology

Female dominance and virilisation

Traditionally, it has been proposed that selection for androgenised, large, aggressive female spotted hyenas allowed female spotted hyenas to dominate males at food resources. However, as size is not a key factor in determining social dominance in this species, and males are not consistently smaller than females, there is no clear evidence that female dominance was achieved through an increase in female size (East & Hofer 2002).

Although young hyenas of both sexes have elevated levels of androgens at birth, adult female hyenas do not have higher levels of androgens than females in other mammalian species, including humans (Goymann et al. 2001). Thus adult female hyenas are not unusually androgenised.

Finally, the noticeable aspect of spotted hyena behaviour is the low level of aggression among immigrant male hyenas, rather than high aggression among females (Hofer & East 1995).

A possible alternative route to female dominance suggests that because female spotted hyenas have an enlarged penile clitoris, males cannot copulate without the full cooperation of a female. To be able to copulate, a male needs an established amicable relationship with the female, and one important aspect of such a relationship is habitual submission at food resources (East & Hofer 2001).

Female social status

Female spotted hyenas acquire their social status chiefly through the support provided by their mother and other female close relatives during social interactions with clan members. The offspring of dominant females can dominate more subordinate members of the clan because of effective maternal support, whereas offspring of subordinate females do not receive effective maternal support when interacting with clan members of higher social status than their mother. Furthermore, spotted hyenas have a ritualised greeting ceremony during which the subordinate participant erects its enlarged penile clitoris ("pseudo-penis"). By watching greetings, offspring learn whether their mother is dominant or subordinate to the females she greets, and thereby learn to gage their social position (East et al. 1993). Maternal support in social interactions and ritualised greeting ceremonies are both processes that lead to daughters obtaining a social status below that of their mother ("rank inheritance"). Daughters normally retain this position, provided their mother is alive, but lose social rank if their mother dies early (Hofer & East 2003).

Because high social status provides fitness benefits, coalitions of closely related females will fight together to try and increase their status. During such periods of social instability, females suffer elevated levels of physiological stress (Goymann et al. 2001).

Maternal investment

Spotted hyena females nurse their offspring for an exceptionally long period and as the protein and energy contents of their milk is higher than that of most other terrestrial carnivores (Hofer & East 1993c, 1995a), the energy expenditure of lactation is higher in spotted hyenas than in any other African terrestrial carnivores.

As access to food resources within a clan territory is determined by female social status, socially dominant mothers are able to monopolise food resources. When the movement of migratory prey results in a decline in the food abundance within a territory, subordinate mothers have to seek food outside the clan territory more often than dominant mothers (Hofer & East 1993c; Höner et al. 2005). Because dependent young spotted hyenas are housed in a communal den inside the clan territory, subordinate mothers have to cover larger distances than dominant mothers, as they move between their foraging areas and their cubs in the communal den (Hofer & East 1993c).  In accordance with parental care theory, hyena females with high foraging costs (females of low social status) shift the optimal level of maternal input downwards relative to females with low foraging costs (females of high social status) (Hofer & East 1993c, 2003). Mothers that maintain a high level of maternal input obtain the fitness benefit of high cub growth and survival (Hofer & East 2003), and avoid the fitness costs of facultative siblicide (Golla et al. 1999, Wachter et al. 2002).

Sibling rivalry and facultative siblicide

Spotted hyena females usually give birth to one or two cubs. Spotted hyena cubs are, in contrast to offspring from all other carnivores, born with their eyes open and their teeth fully erupt. Cubs of twin litters start competing with each other for access to the mother’s teats and milk immediately after birth. For approximately seven weeks after birth, sibling rivalry is intense (Golla et al. 1999) and during this period dominance relationships between twin littermates are established (Hofer & East 1997).

When mothers have to travel long distances to feed and are absent from the communal den for extended periods, aggression between hyena twin litter siblings can be particularly intense and lead to starvation of the subordinate cub (Hofer & East 1997, Golla et al. 1999). In contrast, aggression between littermates is low when prey abundance within or in close vicinity of the territory is high and mothers nurse their cubs at regular, short intervals (Wachter et al. 2002). Thus, the higher the level of maternal input (in terms of lactation), the lower the level of aggression between hyena twin siblings and the lower the incidence of siblicide. This relationship between the level of maternal input and sibling aggression has been predicted by models on the evolution of facultative siblicide and documented in many bird species.

Also consistent with models on the evolution of facultative siblicide is the finding that monopolisation of milk supply and elimination of the subordinate sibling during periods of low maternal input provides dominant cubs with a substantial increase in fitness in terms of increased growth and survival that may outweigh the costs of aggression and the death of the subordinate sibling (Hofer & East 1993c, 1996).

The immigrant male social queue

Males usually disperse from the group in which they were reared and become an immigrant male in another social group. On immigration, a male takes bottom rank in the immigrant male linear dominance hierarchy. Immigrant males rarely fight for social status, and thus normally increase in social status as those further up the hierarchy die or leave the group. For this reason, males increase in social status as their tenure in a clan increases and for this reason top ranking males are usually relatively old males. The male social hierarchy therefore operates like a queue, and as males normally observe strict queuing conventions it can take a male many years to progress from the bottom of the male hierarchy to the alpha position (East & Hofer 2001).  

Male reproductive success and mating tactics

Because offspring of high ranking females are more likely to survive to adulthood (Hofer and East 2003), males prefer to mate with these top-quality females. High ranking males attempt to monopolise high ranking females, but, as microsatellite profiling of offspring has revealed, such males fail to monopolise paternity (East et al. 2003). This indicates that female spotted hyenas are able to exercise a high degree of mate choice possibly because no male can successfully copulate without the complete cooperation of a female. Females rarely produce offspring sired by males that attempted to coerce or monopolise them, and instead prefer sires that behave in a “friendly” manner. Young females prefer sires with short tenures, while old females prefer long tenured males. These age preferences may allow females to avoid the cost of inbreeding with a close male relative. The reproductive success of a male generally increases with his period of tenure in the clan.

Females use various counter tactics against males that attempt to manipulate their mate choice. Females mate with males when they are not in oestrus, possibly to confuse paternity. Females also mate multiply when they are in oestrus, possibly to compensate for an initial copulation with a poor quality mate (East et al. 2003).

Communication

Spotted hyenas have evolved numerous visual, olfactory and vocal signals to communicate with individuals within their own group, and with individuals from other groups.

Asymmetries in the display of visual signals during ritualised greeting ceremonies permit subordinate spotted hyenas to actively submit to more dominant individuals. A key signal of submission is the erect ‘penis’ in individuals of both sexes. The distribution of greetings among clan members indicates that the value of relationships with different clan members is not equal (East et al. 1993).

Spotted hyenas have a diverse acoustic repertoire, but probably their best known call is the whoop. Whoops signal the identity of the caller, and non-linear vocal phenomena are probably important for individual recognition (East & Hofer 1991a; Peters et al. 2004). Whoops are used to recruit scattered clan members to defend food resources or the communal den, and to help clan members locate each other. High ranking males and females whoop more frequently than subordinates, thus whoops may signal social status (East & Hofer 1991b).

Spotted hyenas have a large anal scent gland at the base of their tails which they use to deposit scent on vegetation during a ritualised behaviour called pasting. Differences in volatile components in spotted hyena scent may signal membership of a social group (Hofer et al. 2001). The wider role of scent in spotted hyena society is currently being investigated.

3. Hormones and Behaviour

Females

Traditionally, it has been suggested that female dominance in spotted hyenas evolved through selection for elevated levels of androgens, leading to large, "hyperaggressive" virilized females that could dominate males at food resources. There is little factual evidence to support this idea. Adult female hyenas in fact do not have elevated levels of androgen in comparison to females in other mammalian species, including humans (Goymann et al. 2001a). Furthermore, female spotted hyenas are not consistently larger than males, and the intensity and frequency of male-male conflict in spotted hyenas is extremely low, rather that female aggression being high (East & Hofer 2002).

females and cubs at communal den

Exposure of spotted hyenas of both sexes to maternal androgens in utero is more likely linked to selection for precocial offspring, primed for sibling rivalry at birth. Rates of aggression are elevated at birth in neonates of both sexes, but decline within weeks birth, provided both members of a twin litter receive sufficient milk from their mother (see Evolutionary Biology: Facultative Siblicide).

Energy expenditure during lactation is exceptionally high in spotted hyenas (see Evolutionary Biology), and the physiological stress associated with lactation may explain why lactating mothers in both the Serengeti and Crater populations have higher concentrations of faecal corticosteroids than non-lactating females (Goymann et al. 2001b). Furthermore, lactating females in the Serengeti have higher levels of corticosteroids than those in the Crater, most probably because Serengeti mothers undertake long-distance foraging trips to distant concentrations of migratory herbivores, while Crater females rarely undertake such long-distance trips.

The linear female dominance hierarchy in a spotted hyena clan is typically stable, but when periods of social instability occur, females experience elevated levels of physiologically stress (Goymann et al. 2001b).

Males

Because immigrant male spotted hyenas queue for social status and rarely engage in physical conflict (see Evolutionary Biology), concentrations of faecal corticosteroids are not correlated with social status, but do increase among males in large clans, possibly reflecting a higher rate of social interactions in large social groups (Goymann et al 2003a).  

A positive correlation between male social status and testosterone levels is expected and often found in social species with high rates of agonistic interactions or when social relationships among males are unstable. In contrast, in the spotted hyena where agonistic interactions among males are rare, and social relationships among queuing immigrant males are stable (see Evolutionary Biology), testosterone levels are not correlated with the male social status. However, immigrant male testosterone levels do rise when males attempt to monopolise access to particular females (Goymann et al. 2003b).

4. Conservation Biology

Conflict with people

Globally, large carnivores are often in conflict with local people. In villages close to the boundary of the Serengeti National Park (NP), ownership of livestock is an index of wealth (Loibooki et al. 2002), and thus the loss of livestock to predators generates conflict.

Extensive offtake of wild herbivores by bushmeat hunters to the west of the Serengeti NP (Hofer et al. 1996) results in a considerable by-catch of spotted hyenas in wire snares set by hunters for herbivores (Hofer et al. 1993). This is because spotted hyenas from territories throughout the Serengeti NP regularly forage in areas containing large concentrations of migratory herbivores, and in the dry season, areas with high densities of herbivores are also likely to contain high densities of wire snares (Nyahongo et al. 2006). Mortality caused by wire snares is the most important cause of mortality among adult hyenas in the Serengeti NP (Hofer et al. 1993).

female spotted hyaena with wire snare around neck

Minimally invasive research

Increasingly, scientists and wildlife managers are seeking ways of obtaining information from wildlife through minimally invasive methods, to avoid research and conservation compromising the Darwinian fitness of individuals and thereby inadvertently decreasing the efficacy of conservation efforts (Hofer & East 1998). In line with this new approach, we have developed and validated a method for assaying glucocorticoids in faeces from spotted hyenas (Goymann et al. 1999) and have applied this method to assess physiological stress in spotted hyenas in the Serengeti ecosystem (see Hormones and Behaviour).

We have also developed methods for the extraction of DNA from faeces and hair samples for use in microsatellite profiling of paternity (Wilhelm et al. 2003, East et al. 2003).

Increasingly, pathogens are seen as an important ecological factor of relevance to conservation. We have demonstrated the value of monitoring the prevalence of pathogens using minimally invasive sampling methods for saliva (East et al. 2001) and faeces (East et al. 2004). Long-term monitoring of pathogens of spotted hyenas in both the Serengeti National Park and Ngorongoro Crater is continuing (see Host-Pathogen Interactions).

Information about the biology, distribution and conservations status of all four extant species of hyenas (spotted hyena Crocuta crocuta; brown hyena Hyaena brunnea; striped hyena Hyaena hyaena; aardwolf Proteles cristatus) can be found in Mills & Hofer (1998).

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