Variation in the demography and social structure of spotted hyenas across their range
Spotted hyenas occupy an extraordinarily diverse array of habitats in sub-Saharan Africa, including savanna, deserts, swamps, woodland and montane forest. Densities of spotted hyenas vary by orders of magnitude among these habitats. In the deserts of southern Africa, hyena densities can be as low as one hyena per hundred square kilometres (Tilson & Henschel 1986; Mills 1990). The highest population densities reported for this species occur on the prey-rich savannah plains of Kenya and Tanzania (e.g. Kruuk 1972; Frank 1986; Höner et al. 2005; Watts & Holekamp 2008; Watts & Holekamp 2009), and surprisingly, in the montane forest of Aberdare National Park in Kenya (Sillero-Zubiri & Gottelli 1992); in these areas, densities of spotted hyenas often exceed one animal per square kilometer. However, across 23 study populations the mean density was 0.45 hyenas/km2, ranging from 0.009 to 1.65 hyenas/km2 (Holekamp & Dloniak 2010).
The home ranges occupied by clans of spotted hyenas also vary enormously with population density (Fig. 2B). Home range size for clans studied throughout sub-Saharan Africa ranges from 13 to 1 065 km2, with a mean of 169 km2 (Holekamp & Dloniak 2010). As population density and the number of hyenas per clan increase, home range size decreases, although this relationship is non-linear (Fig. 2B: r2 = 0.562, P = 0.0001, following log transformation of both variables). This pattern of decreasing home range size with increasing population density is similar to that found in other mammalian carnivores (e.g. Trewhella et al. 1988). This pattern is also consistent with the hypothesis that habitat carrying capacity for hyenas, as reflected in both clan size and population density, is limited by food availability (Mills 1990). Indeed, in most parts of Africa, clan size increases with local prey density (Trinkel et al. 2006). However, in the Serengeti, large aggregations of migratory herbivores within commuting distance of hyena territories permit a decoupling of clan size from prey availability within the territory per se (Hofer & East 1993a; b). Furthermore, in the island-like habitat on the floor of Ngorongoro Crater, mean size of seven resident clans was more closely related to overall prey availability in the Crater than to that in the territory of any particular clan (Höner et al. 2005).
The small clans inhabiting the deserts of southern Africa usually contain only one or two matrilines (e.g. Mills 1990) and a single immigrant male, whereas the large clans in the prey-rich plains of eastern Africa may contain over 10 matrilines and several immigrant males (e.g. Frank 1986). Among adult clan members, sex ratios are at least slightly female-biased in most well-studied populations (Table 1) and average 1.8 adult females for every adult male. On average, clan membership is roughly evenly split between immature and mature individuals (Table 1).
Of all the adult males present in a clan at a particular time, adult natal males generally comprise 25–40%, and the rest are immigrants (Holekamp & Smale 1998; Höner et al. 2005, 2007). Figure 3 shows temporal variation over 22 years in the composition of one large clan in Kenya. Relative representation in the clan of each demographic sub-group remains surprisingly stable over time. Clan size reached its apex in 2010, after 2 years of severe drought in Kenya, during which the Talek hyenas had frequent access to dead cattle as well as their normal prey base.
Figure 3. Long-term variation in the composition of one large clan in Kenya, the Talek clan. Here monthly mean composition of the clan is averaged within year, from 1988 to 2010.
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Effects of social rank on female fitness
The nature of the food resources on which spotted hyenas rely creates a competitive environment that shapes hyena social relationships. Individual hyenas experience strong direct and indirect selection to assist their kin in attaining and maintaining social rank and the resources to which their rank entitles them (Smith et al. 2010). Because an adult’s social status determines its priority of access to food during competitive interactions over kills (Fig. 4), rank has profound effects on hyenas’ intake of calories and nutrients (Holekamp & Smale 2000; Hofer & East 2003). Furthermore, high social rank also permits adult female spotted hyenas to reduce energy expenditures demanded by long-distance travel to remote feeding sites (Fig. 4). For example, subordinate females in Kenya are far less likely than dominant females to forage in the central prey-rich areas of the clan’s territory (Boydston et al. 2003). Where females often hunt migratory antelope outside the boundaries of the clan’s territory, as in the Serengeti, low-ranking females need to commute to distant prey much more frequently than do high-ranking females (Hofer & East 1993a; b) The relatively high ratio of energy gain to energy loss enjoyed by high-ranking female hyenas has important consequences with respect to reproductive success and life-history traits (Fig. 4).
The age at which females first bear young is strongly correlated with maternal rank, with daughters of the alpha female first giving birth at around 2.5 years of age, and daughters of the lowest-ranking females doing so at 5–6 years of age (Holekamp et al. 1996; Hofer & East 2003). Although rank does not affect litter size in hyenas, perhaps because females typically have only two functional nipples, inter-litter intervals are much shorter among dominant than subordinate females, and dominants are more frequently able to support pregnancy and lactation concurrently. Therefore the annual rate of cub production is substantially higher among dominant than subordinate females (Holekamp et al. 1996). Maternal rank affects the likelihood that cubs will survive to reproductive maturity, and it also has a pronounced effect on longevity among adult females; daughters of high-ranking females live longer than do daughters of low-ranking females (Watts et al. 2009). Because both birthrates and survivorship are so much greater among high- than low-ranking hyenas (Watts et al. 2009), dominant hyenas tend to have many more surviving kin in the population at any given time than do subordinates (Figs. 1, 5), and thus they enjoy a much larger network of potential allies, should the need for those arise (e.g. Van Horn et al. 2004a; Smith et al. 2010). Because high-ranking females start breeding earlier, live longer, and produce more surviving cubs per unit time, we have observed as much as a fivefold difference in lifetime reproductive success between the highest- and lowest-ranking females in our Kenyan study populations (Holekamp & Smale 2000). Thus a female’s social rank has enormously important fitness consequences. These effects, as they have accrued over 30 years, are shown in Fig. 5 for 19 adult females present in the Talek clan in 1979 (Frank 1983).
Figure 5. Rank-related variation in fitness among adult female spotted hyenas. Cells in the 1979 column (from Frank 1983) represent 19 adult females present in the Talek clan that year, shown in descending rank order. Cells in the 1989, 1999, & 2009 columns represent descendants of those original 19 females, and their proportional representation in the clan. Gray triangles represent extinction events for entire matrilines. Numbers of adult females present in the clan have ranged from 13 to 25 during this period.
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When L. G. Frank (1986) began working with the Talek clan in 1979, he knew nothing about genealogical relationships among adult females, but he was able to discern their rank relationships based on outcomes of agonistic interactions, as described in ‘Methods’. In Fig. 5, each of the 19 adult females present in the clan in 1979 is assigned a different cell in the leftmost column, arranged in descending rank order, and cells in subsequent columns represent this female and her descendants, or her descendants alone. Of 19 adult females originally present in the Talek study clan in 1979 (Frank 1983, 1986), only four had living descendants among the 22 adult females present in the clan in 2009 (Fig. 5). The alpha female in 1979, who then represented only 5% of the adult female population, gave rise to over half the current adult females. Furthermore, the descendants of the 1979 alpha and beta females together now comprise nearly 80% of the adult female population. Although it can be seen here that high-ranking females clearly enjoy a large fitness advantage over subordinates, it is also clear from Fig. 5 that the relatively low-ranking matriline deriving from female F40 persists over many generations despite the energetic handicaps with which its members must cope. This suggests that chance may play an important role in determining which subordinate matrilines persist over extended time periods.
Patterns of relatedness within and among hyena clans and populations
The pattern apparent in Fig. 5 might lead the uninformed reader to expect that hyena clans should be relatively recently derived from a single high-ranking ancestor, and that natal clan-mates might therefore be expected to be closely related to one another. However, our data show clearly that this is not the case. Estimated average R values for the Talek clan fit expectations among dyads of known genealogical relationships (Fig. 6). Average genetic relatedness among natal members of the Talek clan was extremely low (R = 0.011 ± 0.002, Van Horn et al. 2004a; Fig. 6), and similar to R values for males immigrating into the Talek clan from myriad neighbouring clans (mean R values among adult immigrant males was 0.009 ± 0.007; Van Horn et al. 2004a; Fig. 6). Nevertheless, Van Horn et al. (2004a) found that average relatedness is greater within than among matrilines of spotted hyenas, even across successive generations, but also that relatedness is diluted across generations within matrilines. Finally, the decline in mean R values across territorial boundaries separating neighboring hyena clans (Fig. 7) suggests that most successful dispersal by male hyenas occurs to nearby clans. This is consistent with dispersal distances documented for radio-collared males born in our study clans (Smale et al. 1997; Boydston et al. 2005).
Figure 6. Pairwise R values within the Talek clan of any two natal animals, any two resident immigrants and four types of close kin: mothers and cubs (momcub), sires and cubs (sirecub), full-sibling pairs (fullsib) and half-sibling pairs (halfsib). Sample sizes indicate number of R values. Mean values are presented ±SE. Reproduced with permission from Van Horn et al. (2004a).
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Figure 7. Pairwise R values for natal animals from the Talek clan and six other clans are shown in relation to the number of clan borders separating spotted hyenas; there are no clan borders separating members of the same clan. Sample sizes indicate number of R values. Mean values are presented ±SE. Reproduced with permission from Van Horn et al. (2004a).
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Although the hyena populations in the Masai Mara and Amboseli are currently quite similar with respect to many demographic characteristics (e.g. Table 1), their recent population histories differ markedly. Whereas our Mara hyena study population has remained consistently large since at least the late 1970s, with a density of at least 0.86 hyenas/km2 (Frank 1986), the population in Amboseli National Park experienced a demographic bottleneck during the 1970s and 1980s, in which a large population was reduced to approximately 50 individuals (C. Moss, personal communication; Faith & Behrensmeyer 2006), representing a population density of only 0.13 hyenas/km2. The bottleneck appears to have lasted approximately 25 years; based on an estimated generation time for spotted hyenas of 5.7 years (Watts et al. 2011), the bottleneck thus spanned roughly four generations. In the mid-1990’s, the Amboseli population exploded in size, likely resulting from changes in the local prey base and extirpation of the local lion population by pastoralists, and reached a population density of 1.65 hyenas/km2 by 2003–2005 (Watts & Holekamp 2008). Despite these historical differences between parks, patterns of relatedness among natal animals were remarkably similar between Amboseli and the Mara (Watts et al. 2011). As in the Mara, average relatedness was higher among Amboseli clan-mates than among hyenas born and living in adjacent clans. Moreover, we found no differences between the populations in measures of genetic diversity (Watts et al. 2011). Although the social and genetic make-up of the ancestors of the current Amboseli population are unknown, the relatively low levels of relatedness and high levels of genetic diversity in Amboseli indicate it is unlikely that they are descended from a group of closely related individuals.
The patterns of relatedness apparent in both our Mara and Amboseli populations conform to the theoretical expectation (Lukas et al. 2005) that mean relatedness among natal clan members should be similar to that among immigrants. These patterns in spotted hyenas are likely shaped by at least five factors. First, social structuring by matrilines within clans, and by clans within populations, most likely facilitates the maintenance of genetic diversity among natal hyenas (Sugg et al. 1996). Second, clan sizes in both our Mara and Amboseli study populations are quite large, and the number of possible dyads per clan increases exponentially with the number of clan members (Lukas et al. 2005). High average relatedness among natal individuals is only expected in very small groups (Lukas et al. 2005). Third, mean R values are affected by the proportion of related dyads present in a clan at any give time, and this is relatively small compared to the total number of dyads present. For example, when we used data from Smith et al. (2010) to calculate and classify the number of dyadic pairs present in the clan for a large cohort (N = 31) of adult females, we found 222 adult female dyads present concurrently in the Talek clan from 1996 through 2000. Of these, only 11% (N = 25 dyads) were close kin (R = 0.462 ± 0.028), and 16% (N = 36 dyads) were distant kin (R = 0.279 ± 0.040); thus nearly three quarters of the 222 female dyads (73%, N = 161 dyads) were non-kin (R = −0.228 ± 0.006). Fourth, in both Mara and Amboseli populations, patterns of relatedness are undoubtedly affected by male dispersal behaviour. Specifically, immigration into each clan of males from multiple neighbouring clans contributes to low average relatedness within clans, as well as to the maintenance of genetic variation. Furthermore, male spotted hyenas emigrate at high rates (East & Hofer 2001; Boydston et al. 2005), causing a regular influx of paternal genes via dispersing males. Male spotted hyenas also exhibit great behavioural plasticity (Mills & Hofer 1998; Boydston et al. 2003b; Hayward 2006; Kolowski & Holekamp 2009), which probably facilitates their dispersal across potential barriers, including areas with substantial anthropogenic activity. Consequently, it is highly likely that there was migration into the Amboseli population from surrounding areas, and just a few migrants into a small population can be sufficient to maintain or restore genetic variation (Keller et al. 2001; Vilàet al. 2003; Hogg et al. 2006). Finally, the low mean relatedness among natal animals in our study populations is likely caused in part by relatively low reproductive skew among resident male hyenas (Engh et al. 2002; Holekamp & Engh 2009). We discuss effects of dispersal and skew patterns further below.
Effects of dispersal, mate choice and reproductive skew on patterns of relatedness
Although male spotted hyenas are highly mobile, and physically capable of traveling long distances quite quickly (e.g. Hofer & East 1993a), their ability to join new clans is evidently constrained by the severe aggression directed at potential immigrants by resident immigrant males (Smale et al. 1997; Boydston et al. 2001; Szykman et al. 2003). Most habitats in which spotted hyenas occur appear to be saturated such that clan territories form a mosaic covering the entire landscape (Kruuk 1972; Boydston et al. 2001). Each territorial border is thus a potential barrier to dispersal. Most males successfully engaging in natal dispersal immigrate into clans separated from their natal ranges by only one or two territorial borders (Smale et al. 1997; Boydston et al. 2005; Höner et al. 2010). In contrast to lions and other carnivores in which coalitions of related males often disperse together (e.g. Pusey & Packer 1987; Caro 1994), male spotted hyenas disperse alone, such that resident immigrant males represent a true mélange of clans, and accordingly, relatedness among immigrants is extremely low (Van Horn et al. 2004a; also see Fig. 6).
Although the mating system of the spotted hyena is polygynous, matings are not monopolized by high-ranking males, and aggressive contest competition appears to have little influence on male reproductive success (Engh et al. 2002; East et al. 2003). This is in marked contrast to the situation in most other gregarious mammals (e.g. Hoelzel et al. 1999; Di Fiore 2003; Alberts et al. 2006), where reproductive success is strongly correlated with fighting ability and intra-sexual rank. Instead, the strongest determinants of reproductive success among male spotted hyenas are dispersal status, length of residence as immigrants in new clans after dispersal, the number of young females present in the clan when immigrants first arrive there, and female choice of mates (Engh et al. 2002; East et al. 2003; Höner et al. 2007; Van Horn et al. 2008). Adult natal male hyenas are socially dominant to immigrant males, and most of them show strong sexual interest in clan females (Holekamp & Smale 1998), yet they sire only 3% of cubs in their natal clans. By contrast, immigrants sire 97% of cubs, indicating that females prefer to mate with immigrants over adult natal males (Engh et al. 2002; Van Horn et al. 2008). Among resident immigrant males, social rank is correlated with male reproductive success, but regression analysis showed that tenure in the clan predicts this far better than does male rank (Engh et al. 2002). Immigrants do not typically begin to sire offspring until they have resided in their new clan for 1 or 2 years, during which time they occupy the lowest rank positions in the male queue (Engh et al. 2002; East et al. 2003).
To quantify reproductive skew, paternity was assigned to 71 cubs as in Engh et al. (2002). These cubs were conceived from 14 July 1987 to 7 June 2000; they were the offspring of 29 females and 20 males. All but one cub was the offspring of an immigrant male. An additional 33 adult natal males and 26 immigrant males did not sire any cubs. Although the reproductive benefit per female hyena ranged from 1 to 7 cubs, the skew observed among the 29 females was not significantly different from that expected at random (B = −0.0067, P = 0.991) or through equal accrual of benefits (i.e. the lower 95% CI = −0.0131 < 0), and it is clear that the production of cubs was not monopolized (i.e. the upper 95% CI = 0.0006 < 0.976). Presumably the degree of skew observed among Talek females is due largely to variation in lifespan among the adult females (also see Swanson et al. 2011). The range in number of offspring was greater among males than females (1–15 cubs per male), and the reproductive skew among the 79 males was statistically greater than that expected through random accrual of benefits (B = 0.0544, P = 0.0001), or equal accrual of benefits (i.e. the lower 95% CI = 0.0323 > −0.0136), but reproduction was not monopolized by any single male (i.e. the upper 95% CI = 0.0843 < 0.9835). Reproductive skew among male spotted hyenas was thus lower than among males of most other polygynous species for which B has been quantified (Table 2), perhaps because role reversed sexual dimorphisms in body size and dominance status are so rare in other mammals (Holekamp & Engh 2009). Interestingly, as in spotted hyenas, collared peccaries are sexually monomorphic, and in greater horseshoe bats, females are larger than males, and in both these species, B values are quite low, as they are in spotted hyenas.
Table 2. Reproductive skew (B) among polygnous male mammals
|Species||B1||B range2||Sample size||Reference|
|Mountain gorilla, Gorilla beringei||0.38||0.34–0.43||4 groups, 22 males||(Bradley et al. 2005)|
|White-faced capuchin, Cebus capucinus||0.24||0.13–0.40||8 groups, 58 males||(Muniz et al. 2010)|
|European badger, Meles meles||0.18||−0.062–0.63||25 groups||(Dugdale et al. 2008)|
|Rhesus macaque, Macaca mulatta||0.08||0.08–0.08||2 groups||(Dubuc et al. 2011, Widdig et al. 2004)|
|Spotted hyena, Crocuta crocuta||0.05||n/a||1 group, 79 males||Current study|
|Greater horseshoe bat, Rhinolophus ferrumequinum||0.02||n/a||1 group||(Rossiter et al. 2006)|
|Collared peccary, Pecari tajacu||0.01||−0.10–0.33||6 groups, 25 males||(Cooper et al. 2011)|
Female choice of mates appears to be the key determinant of patterns of paternity in this species. At least 40% of female spotted hyenas mate with multiple males during any given oestrous period, and 25–40% of twin litters are multiply sired (Engh et al. 2002; East et al. 2003). Males of all ranks sire offspring, but surprisingly, the alpha male in each immigrant cohort generally sires fewer cubs than do males in lower rank positions (Engh et al. 2002). Immigrant male rank is not correlated with age, and immigrants as old as 18 years have high-quality sperm and ejaculates (Curren LJ, Weldele ML, Holekamp KE 2011, unpublished electroejaculation data.), so their fertility does not appear to decline as they age. Thus the fact that alpha males sire relatively few cubs suggests an important role for female choice in determining reproductive success among males. Not only do females clearly prefer immigrant males over adult natal males, but they also frequently choose lower-ranking immigrants over the alpha male in the immigrant queue (Engh et al. 2002; Van Horn et al. 2008). High-ranking male hyenas cannot monopolize reproduction if females prefer not to mate with them. Absolute female control over mating has thus reduced selection for male fighting ability, and has led to low levels of combat among resident immigrant males, and to the evolution of a male social queue (East & Hofer 2001; East et al. 2003).
Given the powerful influence of female mate choice in spotted hyenas, it appears that males have been obliged to develop strategies to maximize their reproductive success that supplement or replace male–male combat. We find much heavier reliance in this species than in most other mammals on alternative modes of sexually selected interactions, such as endurance rivalry (e.g. queuing, East & Hofer 2001), and sperm competition may also play an important role in spotted hyenas (Curren LJ, Weldele ML, Holekamp KE 2011, unpublished electroejaculation data.). Female dominance and male-like genitalia make sexual coercion impossible in this species (East et al. 1993; Frank 1997). Instead, each female determines whether or not a single male will monopolize her during a given estrous period, and if so, which male this will be. Females can tolerate or refuse male mating attempts according to their own reproductive interests, and this unusual degree of female control appears to reduce the strength of the relationship between social status and reproductive success among males.
Preliminary data from our long-term study indicate that female spotted hyenas tend to produce paternally unrelated offspring. For example, despite persistent availability of individual males during successive reproductive cycles, females seldom permit a single male to sire more than one of their litters. In all known cases where sires were still present in the clan when a female conceived her next litter after successfully weaning at least one member of her last litter, only 3 of 30 females, bearing 4 of 49 litters and having one to four chances to remate, ever chose to mate again with a sire of one of their earlier litters. One result of this apparent tendency to have new males sire each successive litter is that large clans are characterized by networks of kin comprised mostly of mothers, offspring and maternal half-siblings sired by different males. In the final section of this paper, we assess the dynamics and stability of kin associations within the clan’s overall social network, and inquire how these vary with resource availability.
Effects of kinship and prey abundance on social network structure
Social scientists have long-recognized the importance of social network theory in explaining human social organizations (reviewed by Newman 2003b), but formal social network theory has only recently been applied to explain the structuring of animal societies (Krause et al. 2007; Croft et al. 2008; Wey et al. 2008; Sih et al. 2009). Although human social networks are often characterized by homophily, with individuals preferentially associating with others that possess traits similar to their own (e.g. McPherson et al. 2001; Newman 2003a), we do not yet know if this is true among kin-biased network structures of wild animals (but see Smith et al. 2010; Wey & Blumstein 2010; Wiszniewski et al. 2010; Wolf & Trillmich 2008). Within spotted hyena clans, dyadic patterns of association reflect social preferences (e.g. Holekamp et al. 1997a; Szykman et al. 2001; Smith et al. 2007). For example, patterns of association predict the extent to which hyenas engage in affiliative behaviours such as greeting and coalition formation (Smith et al. 2010, 2011). Hyenas are also most tolerant of close associates, withholding aggression from these group-mates both at and away from food (Smith et al. 2007). However, it remains unclear to what extent dyadic preferences generate subgroup cliques or communities, which in turn might structure the social group as a whole. Understanding such processes is important for identifying the levels of selection acting to maintain sociality in general, and cooperation in particular, among group-living animals (Croft et al. 2004; West & Gardner 2007). Moreover, many workers assume that relationships among individual members of vertebrate social groups reflect long-term strategic interests of individual group members (e.g. Silk et al. 2006a,b, 2010). Although such relationships should theoretically be resilient in the face of short-term fluctuations in ecological conditions, recent evidence has called this notion into question (Henzi et al. 2009). Instead, it is possible that individuals only base social preferences on the immediate value of the commodities offered by potential trading partners (e.g. Noë & Hammerstein 1994; Barrett et al. 1999). Furthermore, such effects have never been explored in mammalian carnivores. Here we applied social network theory to assess the dynamics and stability of kin associations among natal animals within our Talek study clan.
We inquired specifically about the extent to which members of distinct matrilines within hyena clans represent differentiated cliques or subgroups comprised of individuals who are more closely connected to one another than to members of other subgroups within the clan. Because maternal kin occupy similar social ranks (Fig. 1) and function as important social allies to one another (Engh et al. 2002; Wahaj & Holekamp 2006; Smith et al. 2010), we predicted that maternal kin would generally form stronger ties than non-kin within their social networks. Because feeding competition is intense in this species and promotes the tendency for hyenas to spend time away from group-mates (Kruuk 1972; Tilson & Hamilton 1984; Frank 1986; Smith et al. 2008), we also expected that social relationships among hyenas would respond dynamically to changes in resource abundance. That is, hyenas should maintain the strongest ties with clan members when feeding competition is relaxed during periods of abundant prey, as indicated by our biweekly prey censuses.
Overall, our social network analysis revealed that the Talek clan is a dynamic social group comprised of kin-based subgroups, which in turn are comprised of individuals in multiple life-history stages. The strength of each hyena’s ties within its social network decreased significantly as it progressed through each successive life history stage; this was particularly striking among natal males (Kruskal–Wallis test: H2,395 = 161.2, P < 0.0001, Fig. 8). On average, den-dependent cubs (N = 136) had significantly stronger ties to clan-mates than did den-independent subadults (N = 151) or natal adults (Fig. 8; N = 108, Mann–Whitney U-tests: Z = −9.27 and −11.1, respectively, P < 0.00001 for both). Moreover, subadults were more strongly connected to clan-mates than were adult hyenas (Z = −9.27, P < 0.00001). We detected no sex difference in strength of connections involving den-dwelling cubs (NM = 70, NF = 66) or subadults (NM = 76, NF = 75) within their social networks (Z = 0.77 and 1.88, P = 0.44 and 0.12, respectively), but adult females (N = 62) were significantly more strongly connected within the clan than were adult natal males (N = 46, Z = 4.34, P = 0.00001). Therefore, we pooled data from males and females for subsequent analysis involving cubs and subadults, but performed separate analyses for adults of each sex. In general, individuals in all three life history stages preferentially maintained social connections with maternal kin over non-kin (Fig. 8). That is, cubs, subadults, and adults were more strongly connected to maternal kin than to non-kin, as indicated by significantly greater standardized strength within, than between, matrilines (Z ≥ 0.49, and P ≤ 0.000001 for all cases).
Figure 8. Mean ± SE standardized strength of social relationships, a measure of the tendency for individual natal hyenas to associate with other natal hyenas. Relationships depicted are limited to those among natal animals that were concurrently alive with maternal kin (based on matriline membership) and non-kin during periods of low (February–May, October–January) and high (June–September) prey abundance as a function of each focal hyena’s life history stage. Standardized strength among den cubs (N = 136) and subadults (N = 151) were statistically similar between the sexes, but adult females (N = 62) maintained stronger social ties than did adult natal males (N = 46) within their social networks. Immigrant males were excluded from this analysis. Letters above bars indicate statistically significant differences for matched comparisons (see text) after correcting for multiple testing at P < 0.05.
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In addition to kinship, prey abundance also influences inter-individual relationships among natal hyenas, as illustrated by the networks within a single “cohort” of natal animals from a year-long period (Fig. 9). This cross-sectional analysis extends the longitudinal data in Fig. 5, by showing that even after excluding den cubs, members of the alpha matriline still have far more kin available as social allies than do natal animals from low-ranking matrilines (Fig. 9). Importantly, despite the fission-fusion nature of their society, individual hyenas maintain stable group membership by fostering both direct ties to preferred companions (Fig. 8) and indirect ties to clan-mates with whom they rarely come into direct contact (Fig. 9).
Figure 9. Variation in social networks within the Talek clan during periods of low (A and C) and high (B) prey abundance. Each matriline present in the clan during this 12-month period is assigned a unique number. The highest possible matriline rank is 1. Large nodes represent adults and small nodes represent subadults. Line darkness is directly proportional to the strength of the association index (tie) between each connected pair of hyenas. Den-dwelling cubs were not included in these networks because their relationships did not significantly vary between periods of low and high prey abundance (Fig. 8).
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Among both subadults and adults, but not among den-dwelling cubs, network dynamics varied predictably in response to variation in local prey abundance (Fig. 9). Both maternal kin (Z = 0.16) and non-kin (Z = 0.88) maintained strong ties with den-dwelling cubs irrespective of prey abundance (Wilcoxon Sign-Ranks Test: P ≥ 0.379 for both, Fig. 8). However, both subadults and adults were more strongly socially connected to maternal kin during periods of relative prey abundance than during periods of prey scarcity (Wilcoxon Sign-Ranks Test: Z ≥ 2.58 and P ≤ 0.01 for all comparisons), and their connections to non-kin were also stronger during periods of high than low prey (Z ≥ 3.13 and P ≤ 0.001 for all). Thus subadults and adults were more strongly connected to clan-mates during times when competition for food was least intense; however, regardless of prey availability, they remained more strongly connected to their relatives than to non-kin.
Our finding that hyenas maintain differentiated relationships with preferred social companions throughout the year differs from that of Henzi et al. (2009), whose social network analysis of two cohorts of female chacma baboons (Papio hamadryas ursinus) suggested that companionships identified during times of food scarcity were replaced by casual acquaintanceships when food was plentiful, and that the strength of social relationships declined as food abundance increased. In contrast, our data demonstrate that hyenas were most strongly connected to social partners during periods when food was most abundant, indicating that social relationships among hyenas are constrained by feeding competition. Interestingly, in this respect, hyena networks more closely resembles those of honeybees (Apis mellifera) and European shore crabs (Carcinus maenas) than those of Chacma baboons. Among honeybees, network density increased with food abundance (Naug 2008). Similarly, in the otherwise non-social shore crab, partner number (node degree) and clique size increased when dispersed food was experimentally clumped (Tanner & Jackson 2011). Among spotted hyenas, the positive relationship between network density and prey abundance might be mediated either by improved payoffs from information exchange when food is abundant or by the stronger need to forage solitarily when prey are relatively scarce.