- Email: [email protected]
Spotted hyaenas: The importance of being dominant
TREE vol. 2, no. 4, April
SpottedHyaenas: TheImportance of BeingDominant Kelly J. Stewart Behavioural dominance is a widespread phenomenon in social mammals. An individual’s dominance rank within a hierarchy reflects its competitive ability relative to that of other group members and is generally based on age or size. However in primates, notably Macaca spp., and Cercopithecus Papio spp. aethiops (macaques, baboons and vervet monkeys) female dominance hierarchies are based on a system of ‘inheritance’ of maternal dominance rank. That is, in contests with peers, immature animals have a dominance rank that is proportional to their mother’s. In adulthood, daughters, who generally remain for life in the group of their birth (whereas most sons emigrate at maturity), assume ranks just below those of their mothers, with the result that closely related females rank adjacent to each other’-3. As a consequence, the different lineages (a female and her descendants) within a group are also ranked with respect to one another. This system arises largely through in third-party support contests, usually from close relatives4a5. Thus, a female’s competitive ability is based not so much on individual characteristics as on her cooperative associations with others. Many social mammals live in groups consisting of related females, but in none except primates has inheritance of maternal dominance rank through social means been described. However, a recent study of spotted hyaenas (Crocuta crocuta) demonstrates some striking similarities in dominance systems between carnivores and these social primates”. Spotted hyaenas live in large communities (clans), the members of which share a range or territory. They are primarily active predators, as opposed to scavengers, hunting feeding communally on and medium-sized to large ungulates7-g. Females normally remain in the clan of their birth, whereas males disperse when juvenile or subadult and are nomadic until they join another clan7rg. Until recently, little was known about the internal organization of clans, or about the hyaena’s mating system. Frank6s7 conducted a four-year study of 60430 individually recogKelly Stewart is at the University of Cambridge Sub-department of Animal Behaviour, High Street, Madingley, Cambridge CB38AA, UK. 88
nized hyaenas in one clan in Kenya’s Masai Mara Reserve. He judged dominance rank by the direction of aggression at kills where more than five hyaenas were feeding. (This represents an extremely competitive situation: the carcass of any animal smaller than a buffalo Syncerus cafferwas usually reduced to a skeleton in 30 minutes.) Dominance correlated highly with time spent feeding at kills, reflecting the ability of an animal to exclude others from a rapidly dwindling carcass. Among females, dominance relations were linear and stable and, as in many primates, were based on maternal rank. Thus, adult and subadult daughters were able to dominate all those animals whom their mother dominated. There was little aggression involving cubs, but they had priority of access at kills in direct relation to their mother’s rank. The system appeared to be based more on maternal support during feeding competition than on genetically inherited traits, such as aggressiveness. For example, one subadult fell in rank after its mother died. Within lineages, dominance was positively correlated with age, except that the youngest cubs had priority of access over older siblings. Unlike daughters, when sons became subadults their competitive ability was no longer related to maternal rank; instead, they fell to the bottom of the male hierarchy and subsequently emigrated. Exceptions to this were the sons of the alpha female (see below). Several studies of primates have found positive correlations between female dominance rank and offspring survival, female fertility, or bothlo. Because high-ranking hyaena mothers obtain more food, and their cubs not only have priority of access but also start eating meat at an earlier age, one might expect these females to raise more surviving offspring than do subordinate animals. However, Frank found no relation between number of cubs surviving to one year and dominance rank of the mother. Nevertheless, higher ranking females did have significantly shorter birth intervals than subordinate ones. Possibly, high offspring mortality due to predation, which was random with respect to rank, may have swamped the slight advantage of more frequent breeding, at least over the short term. Frank argues that the reproductive advantage to high rank might lie 6
1986,
Elsewr
1987
more in the quality of a female’s sons than in the number of offspring she produces. It has been known since Kruuk’s pioneering work on spotted hyaenas* that females dominate males, although they are not appreciably larger than males. Frank shows that the only exceptions were the dominant female’s sons who, even as subadults, outranked all adults, male and female. Perhaps as a result of this, these dominant sons remained in the clan significantly longer than did lower ranking offspring and they emigrated only when they had become sexually mature. Having emigrated, the sons of dominant females may be more likely than others to become the alpha male in whatever clan they join. Male dominance is not significantly related to body size or length of residence in a clan, but appears to be due to individual characteristics like aggressiveness and lack of submission to adult females. Frank speculates that such characters might develop during maturation when, from an early age, the alpha female’s sons experience dominance over all other females. Because the spotted hyaena’s mating system is highly polygynous, with the alpha male performing nearly all the mating, high rank for a male can have huge reproductive pay-offs. Finally, this study of spotted hyaenas suggests possible answers to the puzzle of female dominance over males, a phenomenon rare among mammals and unknown in other social carnivores. Morphologically and physiologically, it is clearly related to the syndrome of virilism in spotted hyaenas, i.e. the bizarre masculinization of females’ genitalia and high levels of circulating androgens in female foetuses and adults11,12. What selection pressures might have led to female dominance over males? Frank suggests that the answer lies in the species’ feeding ecology and the consequent importance of priority of access in feeding competition. Perhaps because of the competitive nature of their feeding, female spotted hyaenas do not carry food back to their dependent young as does the brown hyaena (Hyaena a cooperative breeder brunnea), which forages alone on small, dispersed items9,l3. Furthermore, regurgitation of food to cubs does not occur in the Hyaenidae, probably because of rapid passage of food through the stomach*e9. Thus, adequate nourishment for lactating females and cubs depends on their ability to compete at carcasses with Science
Publkhers
8 V
Amsterdam
0169%5347’86.%0
200
TREE vol. 2, no. 4, April
1987
adults of both sexes. Considering only the Hyaenidae, Frank postulates that when the ancestral Crocuta moved from a Hyaena-like niche of scavenging and solitary foraging to one of active predation and communal feeding on a limited and very localized resource, feeding competition increased dramatically. The result was intense selection pressure for females to have priority of access at kills and ensure the same for their cubs. As a consequence, females became more and more aggressive and ultimately, this increased aggressiveness (mediated by androgen levels) resulted in females’ dominance over males. It has been suggested
primates, competition high-quality resources
that in for clumped, has not only
Bryophytes abound in a wide variety of habitats, and despite their low stature play a significant role in many ecosystems. Earlier views of bryophytes as being ‘evolutionary failures’ are being questioned since the discovery of high genetic variability in those species and populations which have been studied. At the same time, there is growing evidence that in many taxa the maintenance of populations is almost completely dependent on asexual propagation; sexual reproduction may result in an enormous spore output, but from spores in the field establishment seems to be very difficult. The remarkably rapid fine-scale dynamics found in many bryophgte populations may play a role in the maintenance of genetkal variability; it may also partly determine community diversity. Bryophytes are encountered in almost all habitats on land and in many freshwater habitats. They may be apparent for only a few weeks of the year, as in deserts’, or compose permanent banks more than 5000 years old’. In bogs and many polar ecosystems they are the main primary producers, and in montane rain forests the large biomass of epiphytic bryophytes decisively influences water retention in whole watersheds3. In the temperate zones bryophytes are usually less prominent, but they may still decisively affect seedling establishment4, emergence and H.1 During and 6.F van Tooren are at the Department of Plant Ecology, Lange Nieuwstraat 106.3512 PN Utrecht. The Netherlands. (I, 1986
Elsrv
ilr Science
PubI~slws
B \’ Amsterdam
resulted in clear-cut dominance relations, but has favoured long-term alliances among relatives, enabling them to outcompete other conspecifics14, and in some cases leading to a system of inheritance of rank. The similarities in social organization between Crocuta and Old World primates could be due partly to similarities in the importance of being dominant in feeding competition, and the value of cooperation in such competition. References 1 Chapais, B. and Schulman, S.R. (1980) J. Thear. Biol. 82,47-89 2 Hausfater. G., Altmann, J. and Altmann, S. (1982) Science 217,752-755 3 Horrocks, J. and Hunte, W. (1983) Anim. Behav. 31,772-782
4 Cheney, D.L. (1977) Behav. Ecol. Sociobiol. 2,303-318 5 Datta, S.B. (1983) in Primafe Social Relafionships (Hinde, R.A., ed.), pp. 93103, Blackwell Scientific Publications 6 Frank, L.G. (1986) Anim. Behav. 34, 1510-1527 7 Frank, L.G. (1986) Anim. Behav. 34, 1500-1509 8 Kruuk, H. (1972) TheSpottedHyena:A Study of Predation and Social Behavior, Chicago University Press 9 Mills, M.G.L. (1985) Nature316,61-62 IO Fedigan, L.M. (1983) Yearb. Phys. Anthropol. 28,853-859 11 Gould, S.J. (1981) Nat. Hisr. 90, 16-20 12 Frank, L.G., Davidson, J.M. and Smith, E.R. (1985) J. Zoo/. 206,525-531 13 Owens, D.D. and Owens, M.J. (1985) Nature 308,843-845 14 Wrangham, R.W. (1980) Behaviour71, 262-299
RecentDevelopmentsin Bryophyte PopulationEcology H.J. During and B.F. van Tooren nutrient relationships5, and other processes in an ecosystem. In recent years, a number of significant contributions have been made in the fields of ecophysiology and population biology of bryophytes. Since several excellent reviews on physiological ecology have appeared recently (e.g. Ref. 6, and see Box 1I, our main focus will be on population ecology. Sexual reproduction About half of all bryophyte species are dioecious. Among the monoecious plants, the sexual organs may be distributed in a variety of ways, sometimes even within the same specie+. Gamete dispersal distances are very low; different methods yield estimates of 2-5 cm for most species tested; only in species with specialized ‘splashcup’ male inflorescences (Fig. 31 may dispersal reach 0.2-l .O m (Ref. 81. Monoecious species clearly run a high risk of inbreeding. Selfincompatibility has not yet been shown to occur in bryophytes, but several less absolute mechanisms promoting outbreeding have been found, mostly involving temporal separation of the sexesa.
0169-5347!86:$0
200
Studies using isoenzymes and chromosome markers show that genetic variability within populations may be considerable, in fact as large as in flowering plant populations9-‘I. If a species has recently invaded a new area, however, variation is much lower’” and genets occur in a coarse-grained pattern’ I. Apparently, the finegrained pattern of many gene& growing closely intermingled is reached only after a long time. allocation has Reproductive never been measured for a bryophyte. Qualitatively, however, obvious differences exist. Small acrocarpic (erect-growing) genera (Fig. 51 such as Ephemerum and Pottia usually bear a sporophyte many times heavier than the supporting gametophyte, whereas many large pleurocarps (mosses with prostrate growth form; see Fig. 4) occasionally produce a few sporophytes. Spore output per sporophyte is in the range of 50 000-600000 in many moss species with spores of 15-25 pm; in mosses with somewhat larger spores, numbers are in the range 5000-10000 per sporo(liverworts), phyte. Among hepatics spore output is low in many Marchantiales (with spores of 89
SpottedHyaenas: TheImportance of BeingDominant Kelly J. Stewart Behavioural dominance is a widespread phenomenon in social mammals. An individual’s dominance rank within a hierarchy reflects its competitive ability relative to that of other group members and is generally based on age or size. However in primates, notably Macaca spp., and Cercopithecus Papio spp. aethiops (macaques, baboons and vervet monkeys) female dominance hierarchies are based on a system of ‘inheritance’ of maternal dominance rank. That is, in contests with peers, immature animals have a dominance rank that is proportional to their mother’s. In adulthood, daughters, who generally remain for life in the group of their birth (whereas most sons emigrate at maturity), assume ranks just below those of their mothers, with the result that closely related females rank adjacent to each other’-3. As a consequence, the different lineages (a female and her descendants) within a group are also ranked with respect to one another. This system arises largely through in third-party support contests, usually from close relatives4a5. Thus, a female’s competitive ability is based not so much on individual characteristics as on her cooperative associations with others. Many social mammals live in groups consisting of related females, but in none except primates has inheritance of maternal dominance rank through social means been described. However, a recent study of spotted hyaenas (Crocuta crocuta) demonstrates some striking similarities in dominance systems between carnivores and these social primates”. Spotted hyaenas live in large communities (clans), the members of which share a range or territory. They are primarily active predators, as opposed to scavengers, hunting feeding communally on and medium-sized to large ungulates7-g. Females normally remain in the clan of their birth, whereas males disperse when juvenile or subadult and are nomadic until they join another clan7rg. Until recently, little was known about the internal organization of clans, or about the hyaena’s mating system. Frank6s7 conducted a four-year study of 60430 individually recogKelly Stewart is at the University of Cambridge Sub-department of Animal Behaviour, High Street, Madingley, Cambridge CB38AA, UK. 88
nized hyaenas in one clan in Kenya’s Masai Mara Reserve. He judged dominance rank by the direction of aggression at kills where more than five hyaenas were feeding. (This represents an extremely competitive situation: the carcass of any animal smaller than a buffalo Syncerus cafferwas usually reduced to a skeleton in 30 minutes.) Dominance correlated highly with time spent feeding at kills, reflecting the ability of an animal to exclude others from a rapidly dwindling carcass. Among females, dominance relations were linear and stable and, as in many primates, were based on maternal rank. Thus, adult and subadult daughters were able to dominate all those animals whom their mother dominated. There was little aggression involving cubs, but they had priority of access at kills in direct relation to their mother’s rank. The system appeared to be based more on maternal support during feeding competition than on genetically inherited traits, such as aggressiveness. For example, one subadult fell in rank after its mother died. Within lineages, dominance was positively correlated with age, except that the youngest cubs had priority of access over older siblings. Unlike daughters, when sons became subadults their competitive ability was no longer related to maternal rank; instead, they fell to the bottom of the male hierarchy and subsequently emigrated. Exceptions to this were the sons of the alpha female (see below). Several studies of primates have found positive correlations between female dominance rank and offspring survival, female fertility, or bothlo. Because high-ranking hyaena mothers obtain more food, and their cubs not only have priority of access but also start eating meat at an earlier age, one might expect these females to raise more surviving offspring than do subordinate animals. However, Frank found no relation between number of cubs surviving to one year and dominance rank of the mother. Nevertheless, higher ranking females did have significantly shorter birth intervals than subordinate ones. Possibly, high offspring mortality due to predation, which was random with respect to rank, may have swamped the slight advantage of more frequent breeding, at least over the short term. Frank argues that the reproductive advantage to high rank might lie 6
1986,
Elsewr
1987
more in the quality of a female’s sons than in the number of offspring she produces. It has been known since Kruuk’s pioneering work on spotted hyaenas* that females dominate males, although they are not appreciably larger than males. Frank shows that the only exceptions were the dominant female’s sons who, even as subadults, outranked all adults, male and female. Perhaps as a result of this, these dominant sons remained in the clan significantly longer than did lower ranking offspring and they emigrated only when they had become sexually mature. Having emigrated, the sons of dominant females may be more likely than others to become the alpha male in whatever clan they join. Male dominance is not significantly related to body size or length of residence in a clan, but appears to be due to individual characteristics like aggressiveness and lack of submission to adult females. Frank speculates that such characters might develop during maturation when, from an early age, the alpha female’s sons experience dominance over all other females. Because the spotted hyaena’s mating system is highly polygynous, with the alpha male performing nearly all the mating, high rank for a male can have huge reproductive pay-offs. Finally, this study of spotted hyaenas suggests possible answers to the puzzle of female dominance over males, a phenomenon rare among mammals and unknown in other social carnivores. Morphologically and physiologically, it is clearly related to the syndrome of virilism in spotted hyaenas, i.e. the bizarre masculinization of females’ genitalia and high levels of circulating androgens in female foetuses and adults11,12. What selection pressures might have led to female dominance over males? Frank suggests that the answer lies in the species’ feeding ecology and the consequent importance of priority of access in feeding competition. Perhaps because of the competitive nature of their feeding, female spotted hyaenas do not carry food back to their dependent young as does the brown hyaena (Hyaena a cooperative breeder brunnea), which forages alone on small, dispersed items9,l3. Furthermore, regurgitation of food to cubs does not occur in the Hyaenidae, probably because of rapid passage of food through the stomach*e9. Thus, adequate nourishment for lactating females and cubs depends on their ability to compete at carcasses with Science
Publkhers
8 V
Amsterdam
0169%5347’86.%0
200
TREE vol. 2, no. 4, April
1987
adults of both sexes. Considering only the Hyaenidae, Frank postulates that when the ancestral Crocuta moved from a Hyaena-like niche of scavenging and solitary foraging to one of active predation and communal feeding on a limited and very localized resource, feeding competition increased dramatically. The result was intense selection pressure for females to have priority of access at kills and ensure the same for their cubs. As a consequence, females became more and more aggressive and ultimately, this increased aggressiveness (mediated by androgen levels) resulted in females’ dominance over males. It has been suggested
primates, competition high-quality resources
that in for clumped, has not only
Bryophytes abound in a wide variety of habitats, and despite their low stature play a significant role in many ecosystems. Earlier views of bryophytes as being ‘evolutionary failures’ are being questioned since the discovery of high genetic variability in those species and populations which have been studied. At the same time, there is growing evidence that in many taxa the maintenance of populations is almost completely dependent on asexual propagation; sexual reproduction may result in an enormous spore output, but from spores in the field establishment seems to be very difficult. The remarkably rapid fine-scale dynamics found in many bryophgte populations may play a role in the maintenance of genetkal variability; it may also partly determine community diversity. Bryophytes are encountered in almost all habitats on land and in many freshwater habitats. They may be apparent for only a few weeks of the year, as in deserts’, or compose permanent banks more than 5000 years old’. In bogs and many polar ecosystems they are the main primary producers, and in montane rain forests the large biomass of epiphytic bryophytes decisively influences water retention in whole watersheds3. In the temperate zones bryophytes are usually less prominent, but they may still decisively affect seedling establishment4, emergence and H.1 During and 6.F van Tooren are at the Department of Plant Ecology, Lange Nieuwstraat 106.3512 PN Utrecht. The Netherlands. (I, 1986
Elsrv
ilr Science
PubI~slws
B \’ Amsterdam
resulted in clear-cut dominance relations, but has favoured long-term alliances among relatives, enabling them to outcompete other conspecifics14, and in some cases leading to a system of inheritance of rank. The similarities in social organization between Crocuta and Old World primates could be due partly to similarities in the importance of being dominant in feeding competition, and the value of cooperation in such competition. References 1 Chapais, B. and Schulman, S.R. (1980) J. Thear. Biol. 82,47-89 2 Hausfater. G., Altmann, J. and Altmann, S. (1982) Science 217,752-755 3 Horrocks, J. and Hunte, W. (1983) Anim. Behav. 31,772-782
4 Cheney, D.L. (1977) Behav. Ecol. Sociobiol. 2,303-318 5 Datta, S.B. (1983) in Primafe Social Relafionships (Hinde, R.A., ed.), pp. 93103, Blackwell Scientific Publications 6 Frank, L.G. (1986) Anim. Behav. 34, 1510-1527 7 Frank, L.G. (1986) Anim. Behav. 34, 1500-1509 8 Kruuk, H. (1972) TheSpottedHyena:A Study of Predation and Social Behavior, Chicago University Press 9 Mills, M.G.L. (1985) Nature316,61-62 IO Fedigan, L.M. (1983) Yearb. Phys. Anthropol. 28,853-859 11 Gould, S.J. (1981) Nat. Hisr. 90, 16-20 12 Frank, L.G., Davidson, J.M. and Smith, E.R. (1985) J. Zoo/. 206,525-531 13 Owens, D.D. and Owens, M.J. (1985) Nature 308,843-845 14 Wrangham, R.W. (1980) Behaviour71, 262-299
RecentDevelopmentsin Bryophyte PopulationEcology H.J. During and B.F. van Tooren nutrient relationships5, and other processes in an ecosystem. In recent years, a number of significant contributions have been made in the fields of ecophysiology and population biology of bryophytes. Since several excellent reviews on physiological ecology have appeared recently (e.g. Ref. 6, and see Box 1I, our main focus will be on population ecology. Sexual reproduction About half of all bryophyte species are dioecious. Among the monoecious plants, the sexual organs may be distributed in a variety of ways, sometimes even within the same specie+. Gamete dispersal distances are very low; different methods yield estimates of 2-5 cm for most species tested; only in species with specialized ‘splashcup’ male inflorescences (Fig. 31 may dispersal reach 0.2-l .O m (Ref. 81. Monoecious species clearly run a high risk of inbreeding. Selfincompatibility has not yet been shown to occur in bryophytes, but several less absolute mechanisms promoting outbreeding have been found, mostly involving temporal separation of the sexesa.
0169-5347!86:$0
200
Studies using isoenzymes and chromosome markers show that genetic variability within populations may be considerable, in fact as large as in flowering plant populations9-‘I. If a species has recently invaded a new area, however, variation is much lower’” and genets occur in a coarse-grained pattern’ I. Apparently, the finegrained pattern of many gene& growing closely intermingled is reached only after a long time. allocation has Reproductive never been measured for a bryophyte. Qualitatively, however, obvious differences exist. Small acrocarpic (erect-growing) genera (Fig. 51 such as Ephemerum and Pottia usually bear a sporophyte many times heavier than the supporting gametophyte, whereas many large pleurocarps (mosses with prostrate growth form; see Fig. 4) occasionally produce a few sporophytes. Spore output per sporophyte is in the range of 50 000-600000 in many moss species with spores of 15-25 pm; in mosses with somewhat larger spores, numbers are in the range 5000-10000 per sporo(liverworts), phyte. Among hepatics spore output is low in many Marchantiales (with spores of 89