potential mechanisms that individuals may use to prevent infanticide. ... Key words: infanticide, mammals, cannibalism, competition, adoption, sexual selection, ...
Biol. Rev. (1998), 73, pp. 321–346
Printed in the United Kingdom # Cambridge Philosophical Society
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Strategies and counterstrategies to infanticide in mammals LUIS A. EBENSPERGER* Department of Biology, Boston University, 5 Cummington Street, Boston, MA 02215, U.S.A. (Received 6 May 1997 ; revised 17 March 1998 ; accepted 31 March 1998)
ABSTRACT I analyse and summarize the empirical evidence in mammals supporting alternative benefits that individuals may accrue when committing nonparental infanticide. Nonparental infanticide may provide the perpetrator with nutritional benefits, increased access to limited resources, increased reproductive opportunities, or it may prevent misdirecting parental care to unrelated offspring. The possibility that infanticide is either a neutral or maladaptive behaviour also is considered. I devote the second half of this article to reviewing potential mechanisms that individuals may use to prevent infanticide. These counterstrategies include the early termination of pregnancy, direct aggression by the mother against intruders, the formation of coalitions for group defence, the avoidance of infanticidal conspecifics, female promiscuity, and territoriality. I evaluate the support for each benefit and counterstrategy across different groups of mammals and make suggestions for future research. Key words : infanticide, mammals, cannibalism, competition, adoption, sexual selection, pregnancy block, maternal aggression, group defence, promiscuity, territoriality.
CONTENTS I. Introduction .............................................................................................................................. II. Explanations of infanticide........................................................................................................ (1) The predation hypothesis ................................................................................................... (2) The resource competition hypothesis .................................................................................. (3) The adoption avoidance hypothesis.................................................................................... (4) The sexual selection hypothesis .......................................................................................... (5) Nonadaptive explanations .................................................................................................. III. Mechanisms to prevent infanticide............................................................................................ (1) Pregnancy termination ....................................................................................................... (2) Maternal aggression............................................................................................................ (3) Group defence..................................................................................................................... (4) Avoidance of infanticidal individuals.................................................................................. (5) Promiscuity ......................................................................................................................... (6) Territoriality ....................................................................................................................... IV. Conclusions................................................................................................................................ V. Acknowledgements .................................................................................................................... VI. References .................................................................................................................................
322 322 322 325 327 328 330 330 330 331 332 333 333 334 335 337 337
* Present address : Departamento de Ecologı! a, Facultad de Ciencias Biolo! gicas, Universidad Cato! lica de Chile, Casilla 114-D, Santiago, Chile.
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Luis A. Ebensperger
I. INTRODUCTION
II. EXPLANATIONS OF INFANTICIDE
Nonparental infanticide, or the killing of immature infants by conspecifics other than the parents, occurs in a wide variety of animal taxa, from invertebrates to vertebrates (Hausfater & Hrdy, 1984 ; Elgar & Crespi, 1992 ; Parmigiani & vom Saal, 1994). Among mammals, infanticide has been noted either in the wild or under laboratory conditions in at least 91 species (or subspecies), including artiodactyls, carnivores, perissodactyls, primates, chiropterans, rodents and insectivores (Table 1). Most explanations for nonparental infanticide rely on potential benefits to the perpetrator (Hrdy, 1979 ; Sherman, 1981 ; Hausfater & Hrdy, 1984 ; Pierotti, 1991). Thus, infanticide may provide the perpetrator with nutritional gains after cannibalizing the victims (i.e. the predation hypothesis), or it may allow individuals to gain access to limited resources, including food, nest sites or space (i.e. the resource competition hypothesis). Further, infanticide also may be a strategy to avoid the provision of parental care to unrelated young (the adoption avoidance hypothesis). In the case of male killers, infanticide might be committed to obtain increased access to breeding females (i.e. the sexual selection hypothesis). Finally, nonadaptive explanations to infanticide consider its occurrence as a pathological or neutral behaviour. Because nonparental infanticide reduces the inclusive fitness of the victim’s parents (Chapman & Hausfater, 1979 ; Packer et al., 1988), parents are expected to evolve strategies to prevent infanticide (Chapman & Hausfater, 1979 ; Butynski, 1982 ; Hiraiwa-Hasegawa, 1988). As a result, several mechanisms have been proposed to function as counterstrategies to prevent infanticide (Hrdy, 1979 ; Hausfater, 1984). They may include the direct attack (either by single individuals or by group coalitions) or the avoidance of infanticidal animals. More subtle responses may include promiscuity, territoriality, or the early termination of pregnancy. Recent reviews of mammalian infanticide have limited their analysis to particular orders or to particular benefits and counterstrategies (Elwood, 1992 ; Bartlett, Sussman & Cheverud, 1993). Thus, a more comprehensive overview that considers evidence from all groups in which infanticide has been noted is not available. The objective of this article is to provide such a review. For each benefit or counterstrategy, I identify key predictions and analyse how the available evidence supports or rejects these expectations within different groups of mammals.
(1) The predation hypothesis Infanticide may simply be a mechanism to obtain food resources (Hrdy, 1979). Predictions of the predation hypothesis include that (1) infanticide should be followed by the consumption of the infant by the killer, and (2) it should be more frequent among energy-stressed individuals. Obtaining food is unlikely to be a general explanation of infanticide among primates as nonparental infanticide is rarely followed by cannibalism (Hiraiwa-Hasegawa, 1992). One main exception to this rule is the common chimpanzee, Pan troglodytes, in which infanticidal males and females consume their victims (Hiraiwa-Hasegawa, 1992 ; HiraiwaHasegawa & Hasegawa, 1994). Reports showing that small to medium sized mammals (including other primates) are regularly hunted and eaten by chimpanzees (see Hiraiwa-Hasegawa, 1992 and references therein), give support to the idea that food acquisition could be one benefit of infanticide among these pongids. A few other cases of primate infanticide and cannibalism include chacma baboons, Papio ursinus (Saayman, 1971) and redtail monkeys, Cercopithecus ascanius (Struhsaker, 1977). Nutritional benefits may influence infanticide among terrestrial carnivores. The killing and consumption of young individuals by adult males has been recorded among ursids (Troyer & Hensel, 1962 ; Taylor, Larsen & Schweinsburg, 1985 ; Mattson, Knight & Blanchard, 1992 ; Olson, 1993), hyenids (Kruuk, 1972), mustelids (Sargeant et al., 1982), and felids (Elsey, 1954 ; Lesowski, 1963). Nutritional benefits are probably important to infanticide in rodents (although see Ylo$ nen, Koskela & Mappes, 1997). Female infanticide followed by cannibalism occurs in several sciurids such as blacktailed prairie dogs, Cynomys ludovicianus (Hoogland, 1985, 1995), yellow-bellied marmots, Marmota flaviventris (Armitage, Johns & Andersen, 1979), California ground squirrels, Spermophilus beecheyi (Trulio et al., 1986 ; Trulio, 1996) and Columbian ground squirrels, S. columbianus (Hare, 1991), and in murids such as Mongolian gerbils, Meriones unguiculatus (Elwood, 1980), golden hamsters, Mesocricetus auratus (Marques & Valenstein, 1976), white-footed mice, Peromyscus leucopus (Wolff & Cicirello, 1989, 1991), and deer mice, P. maniculatus (Wolff & Cicirello, 1991). The consumption of infants is more common among pregnant and lactating females (DeLong, 1978 ; Balfour, 1983 ; Trulio et al., 1986 ;
Infanticide in mammals
323
Table 1. Reported cases of nonparental infanticide in mammals (Type of observation indicates if reports were made on wild (W) or captive (C) animals. The gender of killers is indicated by l (male) and m (female) symbols ; a combination indicates cases in which both sexes are similarly infanticidal and the ! } " signs are used in cases in which both sexes commit infanticide but one gender is significantly more infanticidal than the other. Question marks indicate cases in which the identity of perpetrators is uncertain.) Type of observation
Infanticidal sex
Sources
W C
l m
Bartos & Madlafousek (1994) Packard et al. (1990)
W W W C C W† C W W
ml* m m? m m l l m l
Felis concolor Felis lynx Felis pardalis Halichoerus grypus Helogale undulata Lycaon pictus Meles meles Mephitis mephitis Mirounga angustirostris Mirounga leonina Monachus schauinslandi Nasua nasua Neophoca cinerea Otaria byronia Panthera leo
W W W‡ W W W C W W W W W W W W
l ? l ml m m m l ml ml m? l l l l
Panthera pardus jarvisi Panthera tigris Phocarctos hookeri Ursus americanus Ursus arctos
W W W W W
l l l l? l
Ursus maritimus Lagomorpha Oryctolagus cuniculus Perissodactyla Equus quagga Primates Alouatta caraya Alouatta palliata Alouatta seniculus
W
l
Doidge et al. (1984) Le Boeuf et al. (1972) Camenzind (1978) Corbett (1988) McLeod (1990) Kruuk (1972) Estes (1989) Bruemmer (1994) Macdonald et al. (1987), Kerby & Macdonald (1988) Hornocker (1970) Elsey (1954) Emmons (1988) Coulson & Hickling (1964) Rasa (1994) van Lawick (1973) Kruuk (1989) Sargeant et al. (1982) Le Boeuf et al. (1972), Le Boeuf & Briggs (1977) Le Boeuf et al. (1972), McCann (1982) Bonness (1990) Russell (1981) Bruemmer (1994) Campagna et al. (1988) Packer & Pusey (1984), Caro & BorgerhoffMulder (1989) Bailey (1993) Schaller (1967) Marlow (1975) Lecount (1982) Troyer & Hensel (1962), Mattson et al. (1992), Olson (1993) Taylor et al. (1985), Kolenosky (1987)
C, W
m"l
Mykytowycz & Dudzinski (1972), Ku$ nkele (1992)
C
l
Duncan (1982)
W W W
l l l
Callithrix jacchus
W
m
Rumiz (1990) Clarke (1983) Crocket & Sekulic (1984), Agoramoorthy & Rudran (1995) Digby (1995)
Species Artiodactyla Cervus elaphus Tayassu tajacu Carnivora Arctocephalus gazella Callorhinus ursinus Canis latrans Canis lupus dingo Canis lupus pallipes Crocuta crocuta Enhydra lutris Eumetopias jubatus Felis catus
Luis A. Ebensperger
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Table 1. (cont.) Type of observation
Infanticidal sex
Cebus olivaceus Cercopithecus ascanius Cercopithecus mitis Cercopithecus campbelli Colobus badius Colobus guereza Gorilla gorilla beringei Homo sapiens Lemur catta Macaca fascicularis
W W W W W W‡ W W W C
l l l l l l l ml l m?l
Macaca fuscata Macaca mulatta Macaca radiata Macaca sylvana Pan troglodytes
W W C† C W
l l m l ml
Papio anubis Papio cynocephalus
W W
l l
Papio ursinus Papio hamadryas Presbytis cristata Presbytis entellus
W C W‡ W
l l l l
W‡ W‡ C, W
l l l
Valderrama et al. (1990) Struhsaker (1977) Butynski (1982) Luong & Galat (1979) Struhsaker & Leland (1985) Rudran (1973) Fossey (1984), Watts (1989) Daly & Wilson (1984), Hrdy (1994) Hood (1994) Angst & Thommen (1977), van Noordwijk (1985), Wheatley et al. (1996) Hiraiwa-Hasegawa & Hasegawa (1994) Angst & Thommen (1977), Ciani (1984) Silk et al. (1981) Angst & Thommen (1977) Goodall (1977), Nishida & Kawanaka (1985), Hamai et al. (1992) Collins et al. (1984) Shopland (1982), Pereira (1983), Collins et al. (1984) Saayman (1971), Collins et al. (1984) Rijksen (1981) Wolf & Fleagle (1977) Sugiyama (1965), Hrdy (1974), Newton (1986), Sommer (1987) Oates (1977) Wright (1988) Angst & Thommen (1977), Mori et al. (1997)
C
?
Greenhall (1965), Joermann (1988)
C C C, W W C C C W W C
ml ml ml m"l m"l m§ m, l ? m, l ? l m"l
Mesocricetus auratus
C
m
Microtus agrestis Microtus pennsylvanicus
C C, W
m§ ml
Mus musculus (laboratory stocks) Mus musculus (wild stocks)
C
m!l
C
ml
Neotoma lepida Ondatra zibethicus
C W‡
m? ?
Porter & Doane (1978), Makin & Porter (1984) Wilson et al. (1993) Ylo$ nen et al. (1997) Hoogland (1985, 1995) Mallory & Brooks (1978, 1980) Ku$ nkele & Hoeck (1989) Arvola et al. (1962), Semb-Johansson et al. (1979) Armitage et al. (1979), Brody & Melcher (1985) Coulon et al. (1995) Elwood (1977, 1980), Elwood & Ostermeyer (1984 a) Goldman & Swanson (1975), Marques & Valenstein (1976) Agrell (1995) Louch (1956), Caley & Boutin (1985), Thomas (1988) Gandelman (1972 a), Svare & Mann (1981), Parmigiani et al. (1989), Perrigo et al. (1993) Southwick (1955), Perrigo et al. (1993), vom Saal et al. (1995), Jakubowski & Terkel (1982), Soroker & Terkel (1988) Fleming (1979) Errington (1961, 1963), Caley & Boutin (1985)
Species
Presbytis senex Propithecus diadema edwarsi Theropithecus gelada Chiroptera Desmodus rotundus Rodentia Acomys cahirinus Apodemus sylvaticus Clethrionomys glareolus Cynomys ludovicianus Dicrostonyx groenlandicus Galea musteloides Lemmus lemmus Marmota flaviventris Marmota marmota Meriones unguiculatus
Sources
Infanticide in mammals
325
Table 1. (cont.)
Species Peromyscus californicus Peromyscus leucopus Peromyscus maniculatus Phodopus sungorus Rattus norvegicus Spermophilus armatus Spermophilus beecheyi Spermophilus beldingi Spermophilus columbianus Spermophilus parryii Spermophilus townsendii Spermophilus tridecemlineatus Scandentia Tupaia belangeri
Type of observation
Infanticidal sex
C C, W C, W C C W W W W
ml m"l m"l ml m!l ? m ml ml
W W W
l l? l
Gubernick (1994) Wolff (1986), Wolff & Cicirello (1991) Wolff & Cicirello (1991) Gibber et al. (1984) Calhoun (1962), Jakubowski & Terkel (1985 a) Balph (1984) Trulio et al. (1986), Trulio (1996) Sherman (1981) Steiner (1972), Balfour (1983), Waterman (1984), Hare (1991) Holmes (1977), McLean (1983) Alcorn (1940) Vestal (1991)
C
?
Stralendorff (1982)
Sources
* Infanticide by males was inferred from postmortem examination. † Direct attack was observed and the authors stated that injuries were likely to have been fatal without human intervention. ‡ Infanticide was not directly observed. § Individuals of the opposite sex were not examined.
Thomas, 1988 ; Hare, 1991 ; Wolff & Cicirello, 1991 ; Schultz & Lore, 1993 ; Hoogland, 1995 ; Trulio, 1996), which might be expected since lactation is the most energy demanding period within the reproductive cycle of eutherian mammals (Gittleman & Thompson, 1988 ; Bronson, 1989). Male rodents also may derive nutritional benefits from infanticide as the consumption of recently killed infants by infanticidal males has been noted in gerbils (Elwood & Ostermeyer, 1984 b), rats (Paul & Kupferschmidt, 1975), marmots (Armitage et al., 1979) and several ground squirrels (Alcorn, 1940 ; Sherman, 1981 ; McLean, 1983 ; Vestal, 1991). Additional support for the predation hypothesis in rodents is provided by field studies showing that cannibalism is correlated negatively with food availability (Holmes, 1977). Further, the diets of most species in which infanticide and cannibalism have been noted include some fraction of animal matter (Elwood, 1992). Predation by adult rodents on the infants or adults of other rodent species may occur (DeLong, 1966 ; Rood, 1970 ; Ewer, 1971 ; Paul & Kupferschmidt, 1975 ; J. O. Wolff, 1985 a ; Elwood & Ostermeyer, 1986). Finally, food deprivation has been shown to increase the frequency of infanticide and cannibalism in Mongolian gerbils (Elwood & Ostermeyer, 1984 b), Norway rats, Rattus norvegicus (Paul & Kupferschmidt, 1975),
house mice, Mus musculus (Svare & Bartke, 1978), and common voles, Microtus arvalis (Litvin et al., 1977). In the case of the house mice, however, the motivational and neurohumoral basis for pup-killing behaviour is similar to that of intermale aggression but different from that of predatory attack, which suggests that male infanticide in this species is more likely a form of intraspecific aggression rather than an expression of intraspecific predation (Parmigiani & Palanza, 1991).
(2) The resource competition hypothesis The resource competition hypothesis states that infanticide may provide the perpetrator or its offspring with increased access to physical resources such as food, nesting sites, or space (Rudran, 1973 ; Hrdy, 1979 ; Sherman, 1981). Thus, the death of an infant will increase the access to limited resources by the killer or its descendants (Hrdy, 1979). In addition, infanticide is expected to be more prevalent under conditions when resources are more limited, such as under food scarcity and high population density (Butynski, 1982). Also, infanticidal individuals should selectively kill infants of the sex most likely to become competitors for the perpetrator or its offspring.
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The resource competition model may apply to some cases such as the common marmoset Callithrix jacchus. Within marmoset groups, subordinate nonreproductive female helpers increase the weaning success of infants born to dominant females, and infanticide involves the killing of subordinate female’s infants by the dominant female (Digby, 1995). Thus, infanticide may provide dominant females with increased access to limited resources such as helpers and food. This argument is supported by correlational evidence showing that subordinate females successfully raise offspring only when the birth of their infants does not overlap with the birth of infants born to dominant females during early lactation (when competition for access to helpers is probably more intense) ; when it occurs, infants of subordinates do not survive (Digby, 1995). This hypothesis does not seem to apply in other studies in which infanticide is not related to population density or to the level of food resources (Butynski, 1982 ; Crocket & Sekulic, 1984 ; Struhsaker & Leland, 1985). A situation similar to that described in marmosets may apply to some group-living carnivores (Packer & Pusey, 1984). Dominant female wolves, Canis lupus pallipes (McLeod, 1990), dwarf mongooses, Helogale undulata (Rasa, 1994), dingos, Canis lupus dingo (Corbett, 1988), wild dogs, Lycaon pictus (van Lawick, 1973), and probably badgers, Meles meles (Kruuk, 1989) may suppress reproduction by subordinate females of the same group by killing their newborns. As a consequence, subordinate females may help rear and suckle the offspring of the dominant female (Corbett, 1988 ; Rasa, 1994). As noted above, successful breeding by subordinate females occurs only when their infants do not overlap with the preweaning period of infants born to the dominant female (Frame et al., 1979 ; Packer & Pusey, 1984). Among African lions, Panthera leo, it has been suggested that after the takeover of a pride by a new male coalition, incoming males kill the cubs sired by the previous male coalition in order to eliminate feeding competitors for their future offspring (Pusey & Packer, 1994). Although this hypothesis is supported by the observation that the presence of older cubs may depress the survival of younger cubs within the same cohort (Bertram, 1975), no confirmatory data of this effect are available for successive cohorts sired by different male coalitions (Pusey & Packer, 1994). Competition for burrows has been suggested to be the cause of female infanticide in rabbits, Oryctolagus cuniculus (Ku$ nkele, 1992). Female rabbits kill infants
Luis A. Ebensperger and juveniles from unrelated females and dead individuals are not cannibalized (Mykytowycz & Dudzinski, 1972 ; Ku$ nkele, 1992). Evidence that burrows are limited comes from observations of females fighting over access to underground nests (Ku$ nkele, 1992). In addition, the burrow of a female whose litter has been killed can be taken over by other females (Ku$ nkele, 1992). Although this evidence supports the resource competition hypothesis, the adoption avoidance model (see below) cannot be ruled out, as newborns may survive infanticidal attacks and become adopted by an attacking female (Ku$ nkele, 1992). Among rodents, some support to the resource competition hypothesis comes from observations on S. beldingi. In this species, adult resident females are the main perpetrators of infanticide, and they seldom consume their victims (Sherman, 1981). As expected, females losing their litters to predators or conspecifics move to new sites, and females that kill usually establish their territories near their victim’s burrows (Sherman, 1981). However, among sciurids such as C. ludovicianus, S. beecheyi and S. beldingi, females do not direct their infanticidal attacks solely at female offspring (Sherman, 1981 ; Hoogland, 1995 ; Trulio, 1996). Among these rodents, only the females remain in the maternal territory area and represent future competitors to other females (Greenwood, 1980 ; Dobson, 1982). Contrary to the resource competition hypothesis, female S. beecheyi and S. columbianus that kill the litters of other females do not gain access to the victimized mother’s burrow or territory (Balfour, 1983 ; Hare, 1991 ; Trulio, 1996). McLean (1983) invoked competition for resources to explain infanticide committed by immigrant males of S. parryii. Males of this species are suggested to kill infants to decrease competition for food and access to females the following breeding season. Nonetheless, information on the fate of infanticidal males and their offspring during the next breeding season is not available to evaluate this possibility. Competition for space has also been suggested in P. leucopus and P. maniculatus. Females of both species are territorial against other females and they are the most common perpetrators of infanticide (Wolff & Cicirello, 1989, 1991). However, the frequency of infanticide by resident females does not increase at high densities when competition for nest sites is probably high (Wolff & Cicirello, 1991), and an increased access by infanticidal females (or their offspring) to the territories of their victimized females has not been noted. In fact, since females usually consume their victims (Wolff & Cicirello, 1989,
Infanticide in mammals 1991), the predation hypothesis seems a more parsimonious explanation for infanticide in Peromyscus species. (3) The adoption avoidance hypothesis Sherman (1981) and Elwood & Ostermeyer (1984 a) have suggested that individuals may commit infanticide as a strategy to avoid adopting and providing parental care to unrelated offspring (Pierotti & Murphy, 1987 ; Pierotti, 1991). The adoption avoidance hypothesis predicts that infanticide should be committed mostly (but not exclusively) by the sex that bears the primary costs of adoption (Pierotti, 1991). Among mammals, lactation is the most energetically expensive phase of parental care (Gittleman & Thompson, 1988 ; Bronson, 1989), so females particularly are expected to be infanticidal. Furthermore, infanticide should be more frequent in species in which nursing females are unable to recognize their own from unrelated offspring, but only under conditions where victims can clearly be identified as nonfilial (modified from Pierotti, 1991). Female primates are usually noninfanticidal (Table 1), which makes it unlikely that infanticide could be related to the provision of parental care to unrelated offspring within this group. A potential exception could be infanticide by female marmosets. Alloparental behaviour and adoption of nonfilial offspring is common in marmosets (Riedman, 1982), which raises the possibility that dominant females kill infants born to subordinate females to avoid nursing nonfilial infants. In contrast to primates, female infanticide seems more common among some social carnivores (Table 1). Among these mammals, infanticide is frequently committed by dominant females to suppress reproduction by subordinate females, and adoption and alloparental behaviour of nonfilial offspring by the females, including dominant females, occurs (van Lawick, 1973 ; Macdonald & Moehlman, 1982 ; Packer, Lewis & Pusey, 1992). At present, the possibility that dominant females of social carnivores commit infanticide to avoid nursing nonfilial infants born to subordinate females rather than to decrease food competition cannot be ruled out. Stronger support for the adoption avoidance hypothesis comes from observations on female aggression and infanticide in pinnipeds. Among these carnivores, female infanticide and aggression against unrelated infants often occurs when a pup becomes separated from its mother and it attempts
327
to suckle milk from another lactating female (Coulson & Hickling, 1964 ; Le Boeuf, Whiting & Gantt, 1972 ; Marlow, 1975 ; Reiter, Panken & Le Boeuf, 1981 ; McCann, 1982 ; Doidge, Croxall & Baker, 1984 ; Bonness, 1990 ; Bruemmer, 1994). Upon the attempt of an unfamiliar pup to suckle, lactating females (other than the mother) react aggressively and bite the pups. This may result in the fracture of a pup’s skull or jaws, and in extensive external lacerations that may cause pups to die (Le Boeuf et al., 1972 ; Le Boeuf & Briggs, 1977). The adoption avoidance hypothesis as an explanation to female infanticide in pinnipeds is further supported by the high rates of adoption and nursing of unrelated infants observed among many phocid and some otariid females (Riedman, 1990 ; Packer et al., 1992). Circumstantial evidence supporting the adoption avoidance hypothesis in rodents includes field and laboratory (e.g. cross-fostering of infants) studies that show a high potential of lactating females to adopt and provide parental care for unrelated infants. Species in which females are infanticidal (Table 1) and apparently unable to discriminate between their own and nonfilial infants, when nursing infants, include spiny mice, Acomys cahirinus (Porter & Doane, 1978), brown lemmings, Lemmus lemmus (de Kock & Rohn, 1972), meadow voles, Microtus pennsylvanicus (McShea & Madison, 1984 ; Sheridan & Tamarin, 1986), house mice (Sayler & Salmon, 1971 ; Ko$ nig, 1989, 1994), desert woodrats, Neotoma lepida (Fleming, 1979), white-footed mice (Hawkins & Cranford, 1992 ; Jacquot & Vessey, 1994), deer mice (Hansen, 1957 ; Hawkins & Cranford, 1992 ; Millar & Derrickson, 1992), blacktailed prairie dogs (Hoogland, Tamarin & Levy, 1989), Belding’s ground squirrels (Sherman, 1980), Columbian ground squirrels (Hare, 1991), and the cavy, Galea musteloides (Ku$ nkele & Hoeck, 1995). Female meadow voles even seem unable to discriminate the infants of other species (McGuire, 1988 ; Thomas, 1988 ; also see Hawkins & Cranford, 1992). Laboratory observations show that females kill unrelated young mostly when sexually inexperienced, pregnant, or after weaning their own litters, but rarely when they are lactating (Richards, 1966 ; Peters & Kristal, 1983 ; Elwood & Ostermeyer, 1984 a ; McCarthy & von Saal, 1985 ; Soroker & Terkel, 1988 ; Manning et al., 1995). This is consistent with the expectation that females should commit infanticide only when unrelated offspring can be clearly distinguished from filial young. In house mice (Sayler & Salmon, 1971) and the cavy
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(Ku$ nkele, 1987, cited in Ku$ nkele & Hoeck, 1989), lactating females mainly attack infants that do not match with the age of their own young, adopting and nursing those of similar age. Among sciurids in which females kill infants while lactating, they mostly do so before young mingle (Sherman, 1981 ; Hare, 1991 ; Hoogland, 1985). An exception to this is in the California ground squirrel, where most victims of infanticide by lactating females are post-emergent infants (Trulio, 1996). Elwood (1992) suggested that committing infanticide to prevent adoption could be expected in precocial rather than altricial species ; in the former, infants are mobile and may attempt to obtain nursing from nonrelatives. Laboratory observations show that lactating females of altricial species that encounter unrelated pups in an unfamiliar place may retrieve them (Fleming, 1979 ; L. A. Ebensperger, personal observations). Whether this situation occurs under wild conditions needs to be examined. (4) The sexual selection hypothesis Hrdy (1977, 1979) suggested that males may kill infants to destroy another male’s offspring and increase their own chances of mating. The sexual selection hypothesis requires that (1) infanticidal males should not kill offspring they have sired, (2) the elimination of offspring should shorten the interbirth period of the victimized females, and (3) infanticidal males should mate and sire the subsequent offspring of the mother of the infant killed (Hrdy, 1979 ; Sommer, 1994). Although still debated (Bartlett et al., 1993 ; Sussman, Cheverud & Bartlett, 1994), the idea that increased reproductive opportunities could be a major benefit of infanticide among nonhuman primates is generally supported (Hiraiwa-Hasegawa, 1988 ; Hrdy, Janson & van Schaik, 1994). Within primates, infanticide is usually perpetrated by the males (Table 1) : infanticide is committed either by a male who has recently taken over a group of breeding females (Hrdy, 1974 ; Oates, 1977 ; Struhsaker, 1977 ; Butynski, 1982 ; Sommer & Mohnot, 1985 ; Rumiz, 1990), by a male who has gained breeding status in his group (Clarke, 1983 ; Ciani, 1984 ; Struhsaker & Leland, 1985 ; Tarara, 1987 ; Watts, 1989), or by a male who has recently immigrated into the group (Wolf & Fleagle, 1977 ; Collins, Busse & Goodall, 1984 ; Crockett & Sekulic, 1984 ; van Noordwijk, 1985 ; Wright, 1988 ; Borries, 1997). Thus, killed infants are usually preweaned infants unrelated to the infanticidal male (Hrdy,
Luis A. Ebensperger 1974 ; Butynski, 1982 ; Collins et al., 1984 ; Sommer & Mohnot, 1985 ; Struhsaker & Leland, 1985 ; Sommer, 1987 ; Watts, 1989 ; Hood, 1994 ; Borries, 1997) ; but see Rijksen, 1981 ; Valderrama, Srikosamatara & Robinson, 1990). An intriguing exception to this pattern is within-group infanticide by common chimpanzees, where the victim’s mother often has mated with most males (including the killers) in the group (Hamai et al., 1992 ; although see Nishida & Kawanaka, 1985). That the elimination of infants shortens the interbirth period of the victimized females is supported by observations showing that mothers whose infants are killed resume sexual receptivity significantly sooner than mothers whose infants survive (Hrdy, 1974 ; Angst & Thommen, 1977 ; Butynski, 1982 ; Clarke, 1983 ; Collins et al., 1984 ; Crockett & Sekulic, 1984 ; Struhsaker & Leland, 1985 ; Sommer, 1987 ; Agoramoorthy & Mohnot, 1988 ; Watts, 1989 ; Borries, 1997). The sexual selection hypothesis is further supported by cases in which the killer male subsequently mates and sires the next offspring of the victimized female (Hrdy, 1974 ; Struhsaker, 1977 ; Sommer & Mohnot, 1985 ; Struhsaker & Leland, 1985 ; Sommer, 1987 ; Agoramoorthy & Mohnot, 1988 ; Watts, 1989 ; Agoramoorthy & Rudran, 1995). However, the model is not supported by cases in which the infanticidal males either do not mate with the victim’s mother (Boggess, 1979 ; Goodall, 1977 ; Butynski, 1982 ; Ciani, 1984 ; Valderrama et al., 1990) or do not mate at all (Agoramoorthy & Rudran, 1995). Besides primates, strong evidence supporting the sexual selection hypothesis comes from observations carried out on African lions, Panthera leo. Among these felids, groups of females are defended by a male coalition against other male groups. However, when a lion pride is taken over by a new band of males, the new male coalition usually kills all dependent cubs (Bertram, 1975 ; Packer & Pusey, 1984). Females whose cubs have been killed resume sexual receptivity sooner than they would if their cubs survived, and they mate with most males of the new coalition (Packer & Pusey, 1983 a, b, 1984). Thus, males sire cubs approximately eight months sooner than they would if they spared the cubs of the previous males (Packer & Pussey, 1984). Sexually selected infanticide also may occur among leopards, Panthera pardus jarvisi, where males have been reported to kill a female’s cubs and sire the female’s next offspring (Bailey, 1993). Among other carnivores, reproductive advantages have been invoked in polar bears, Ursus maritimus. However, this
Infanticide in mammals suggestion is based on scattered observations of a female that is suspected to have copulated with a male that recently killed her cubs (Taylor et al., 1985). The sexual selection hypothesis might apply to feral horses, Equus quagga. In horses, the killing of unrelated foals by male stallions takes place when males are added to the herds for the first time. However, infanticide ceases if killer males are kept with a breeding herd and allowed to breed (Duncan, 1982). Obtaining reproductive advantage frequently is considered the main explanation for male infanticide in murid rodents (vom Saal & Howard, 1982 ; Huck, 1984 ; Wolff & Cicirello, 1989, 1991 ; Elwood, 1992). Indeed, there is considerable evidence demonstrating the existence of different mechanisms allowing males to kill unrelated instead of filial infants. They include the direct recognition of pups (Paul, 1986 ; Makin & Porter, 1984 ; El-Haddad, Millar & Xia, 1988), or the use of indirect clues such as association with previous sexual partners (Huck, Soltis & Coopersmith, 1982 ; Webster, Gartshore & Brooks, 1981), location of infants (McCarthy & vom Saal, 1986 a), or simply a physiological change induced by recent mating and cohabitation with a female (Elwood, 1977, 1980, 1985, 1986 ; Labov, 1980 ; Webster et al., 1981 ; Brooks & Schwarzkopf, 1983 ; Gibber, Piontkewitz & Terkel, 1984 ; Makin & Porter, 1984 ; Jakubowski & Terkel, 1985 b ; McCarthy & vom Saal, 1986 b ; Brown, 1986 ; Mennella & Moltz, 1988 ; Soroker & Terkel, 1988 ; Parmigiani, 1989 ; Elwood & Kennedy, 1991 ; Palanza & Parmigiani, 1991 ; Coopersmith & Lenington, 1996 ; Palanza et al., 1996). Under field conditions, male infanticide in white-footed mice and deer mice typically is committed by individuals who are recent immigrants to a particular area (i.e. are unlikely to have sired any offspring in the area ; Wolff & Cicirello, 1989, 1991). In semi-natural populations of house mice, male infanticide involves territorial males killing infants outside their own territories, and nonterritorial males that have not sired any offspring (Manning et al., 1995). Together, these observations suggest that male rodents kill infants unlikely to have been sired by them. The additional requirement of the sexual selection hypothesis, i.e. that infanticide reduces the interbirth period of the females, also seems supported in murid rodents. In captivity, most male collared lemmings, Dicrostonyx groenlandicus (Mallory & Brooks, 1978), meadow voles (Webster et al., 1981), house mice (vom Saal & Howard, 1982 ; McCarthy & vom Saal,
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1986 b ; Coppersmith & Lenington, 1996), and Norway rats (Mennella & Moltz, 1988) that are introduced into the cage of an unfamiliar female and her neonates, attack and kill the pups. If allowed to stay and mate with the victim’s dam, these infanticidal males produce their own offspring sooner than males who do not eliminate the female’s original litter. Implantation (i.e. gestation) in murid rodents can be delayed by lactation and the presence of infants (Mantalenakis & Ketchel, 1966 ; Elwood & Ostermeyer, 1984 a ; Mennella & Moltz, 1988). Moreover, increased numbers of pups being suckled in gerbils results in fewer pups being produced in the next litter (Elwood & Ostermeyer, 1984 a). Thus, killing pups brings forward the date of birth of a litter and may result in more young sired by the infanticidal male (Elwood & Ostermeyer, 1984 a). Finally, the only available evidence showing that upon eliminating a female’s previous litter a male subsequently mates and sires the later offspring of that female comes from observations made of a seminatural population of house mice. Under these conditions, territorial males were observed to kill pups of females outside their territories and sire the next litter of the victimized females (Manning et al., 1995). Compared to murid rodents, the sexual selection hypothesis seems less likely to explain male infanticide in sciurids (ground squirrels and marmots) and other seasonally breeding mammals (but see Borries, 1997). In most sciurids in which infanticide by adult males has been recorded, the females come into oestrus once per year and the elimination of their litters does not cause them to resume their sexual receptivity until the next breeding season (Sherman, 1981 ; McLean, 1983 ; Hoogland, 1985 ; Vestal, 1991 ; Coulon et al., 1995). Thus, males can hardly increase their opportunities to reproduce by killing a female’s litter (Hiraiwa-Haegawa, 1988). Moreover, modelling shows that a lag between the death of a female’s offspring and her next conception may make infanticide untenable as a male reproductive strategy (Chapman & Hausfater, 1979 ; Hausfater, 1984). Nonetheless, the possibility that in some cases killer males still enhance their chances of breeding with the victimized females during the following breeding season needs to be examined. Red deer, Cervus elaphus could be one such case. Among seasonally breeding red deer, infanticide of unrelated calves is committed by males that take over a group of females (Bartos & Madlafousek, 1994). As a result, a new dominant male seems to benefit from infanticide as fecundity of victimized
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females increases in the season following replacement of their alpha stag (Bartos & Madlafousek, 1994). Evidence from seasonal breeding mammals suggests that reproductive failure one year can increase a female’s chance of success in the following year (McLean, 1983 ; Hoogland, 1985 ; Pereira & Weiss, 1991 ; Bartos & Madlafousek, 1994 ; Coulon et al., 1995). (5) Nonadaptive explanations A final category of explanation for infanticide considers that this behaviour is either neutral or maladaptive (i.e. pathological). Infanticide might result from selection for some other behaviour (e.g. general aggressiveness), be an accidental occurrence, or be the result of disturbances in the physical (e.g. habitat reduction) or social (e.g. due to high-density conditions) environment of individuals (Calhoun, 1962 ; Smith, 1974 ; Curtin & Dolhinow, 1978 ; Boggess, 1979 ; Rijksen, 1981 ; Ciani, 1984 ; Sussman et al., 1994). The most compelling evidence supporting a nonadaptive scenario for infanticide comes from pinnipeds. Infanticide by male otariids and phocids occurs during disputes for the access to females between harem-holding males and subordinate males. Under these conditions, pups are accidentally crushed by combatant males (Coulson & Hickling, 1964 ; Le Boeuf et al., 1972 ; Marlow, 1975 ; Le Boeuf & Briggs, 1977 ; McCann, 1982 ; Doidge et al., 1984). In addition, infants may die from physical injuries caused by abductions from subadult males (Le Boeuf et al., 1972 ; Marlow, 1975 ; Campagna, Le Boeuf & Cappozzo, 1988). Apparently pup abduction (along with the resulting death of infants) is an epiphenomenon of male sexual motivation : pups are used by males as females substitutes to redirect their frustrated sexual and aggressive motivations (Campagna et al., 1988). Male abductors typically bite pups on the neck and back, and attempt copulation with them (Campagna et al., 1988). No benefits are apparent from pup abduction ; abducting males do not gain access to the breeding area or attract the attention of breeding females, including the victim’s dam, and they do not cannibalize dead infants (Campagna et al., 1988). Infanticide in rodents also has been considered as aberrant, attributed to conditions of overcrowding (Southwick, 1955 ; Louch, 1956 ; Calhoun, 1962 ; Semb-Johansson, Wiger & Engh, 1979). However, such a suggestion comes from studies made on confined populations kept under seminatural con-
Luis A. Ebensperger ditions in which the identity of killers and the precise circumstances (i.e. the possibility of evaluating potential benefits) of infanticide usually are not recorded (Southwick, 1955 ; Calhoun, 1962 ; SembJohansson et al., 1979). Further, explanations of infanticide based on overcrowding should probably be ruled out as field-recorded infanticide seems unrelated to local density of conspecifics (Dobson, 1990 ; Wolff & Cicirello, 1991 ; Hoogland, 1995). Similarly, there is no evidence that infanticide is accidental or results from poor habitat conditions (Sherman, 1981 ; Hoogland, 1995). Among primates, a nonadaptive explanation of infanticide due to disturbances is unlikely to apply to cases in which infanticide occurs in populations that are neither at unusually high densities nor subjected to habitat alterations (Struhsaker, 1977 ; Butynski, 1982 ; Clarke, 1983 ; Crockett & Sekulic, 1984 ; Struhsaker & Leland, 1985 ; Newton, 1986 ; Valderrama et al., 1990 ; Agoramoorthy & Rudran, 1995 ; Borries, 1997). Similarly, nonadaptive explanations for infanticide can hardly explain regularities associated with its occurrence such as sex biases of the victims (Sommer, 1987 ; HiraiwaHasegawa & Hasegawa, 1994) or the fact that only unrelated infants are killed (Hrdy et al., 1994). Theoretical considerations using game theory also fail to support the hypothesis that infanticide is a nonadaptive behaviour. Thus, it seems essential that infanticide has to be associated with some direct or indirect resource benefits in order to invade a noninfanticidal population (Glass, Holt & Slade, 1985 ; Tuomi, Agrell & Mappes, 1997). III. MECHANISMS TO PREVENT INFANTICIDE
(1) Pregnancy termination Pregnancy termination (also referred to as ‘ pregnancy block ’, ‘ Bruce effect ’, or ‘ abortion ’) initially was observed in house mice (Bruce, 1959, 1960). Exposing recently inseminated females to an unfamiliar male (or to his odour) may prevent implantation and cause a return to oestrus 4–5 days later. Pregnancy block may occur either before implantation or by mid-to-late pregnancy in the same species (Stehn & Richmond, 1975 ; Storey & Snow, 1990 ; Storey, 1994), and it has been recorded both under laboratory and wild conditions in carnivores (Bertram, 1975), primates (Small, 1982 ; Pereira, 1983 ; Mori & Dunbar, 1985 ; Agoramoorthy et al., 1988 ; Colmenares & Gomendio, 1988), rodents (Bruce, 1960 ; Chipman
Infanticide in mammals & Fox, 1966 ; Clulow & Clarke, 1968 ; Terman, 1969 ; Milligan, 1976 ; Kenney, Evans & Dewsbury, 1977 ; Mallory & Clulow, 1977 ; Labov, 1981 a ; Schadler, 1981 ; Stehn & Jannett, 1981 ; Heske & Nelson, 1984 ; Huck, 1984), and ungulates (Berger, 1983). Among other potential functions (Schwagmeyer, 1979 ; Labov, 1981 a ; Huck, 1984), pregnancy block may prevent waste of additional investment on infants that may be killed by invading or strange males (Hrdy, 1979 ; Schwagmeyer, 1979 ; Labov, 1980, 1981 a ; Mallory & Brooks, 1980). This hypothesis predicts (1) a direct correlation between the rate of pregnancy termination and the risk of infanticide, and (2) that under similar conditions of infanticidal risk, females that interrupt their pregnancies should wean more offspring than females who retain their former pregnancies. Evidence from rodents supports a positive association between the incidence of pregnancy block and the risk of infanticide. In house mice, dominant males are infanticidal more frequently than are subordinate males (Huck et al., 1982 ; Elwood, 1986), and, as expected, dominant males are more likely than subordinates to cause pregnancy block (Huck, 1982 ; but see Lebov, 1981 b). Infanticidal male house mice are more likely to induce pregnancy block than are noninfanticidal males, which suggests an ability of females to evaluate differences in the risk of infanticide on their litters should pregnancy not be interrupted (Huck, 1984 ; Elwood & Kennedy, 1990). In the case of golden hamsters, Mesocricetus auratus, females are more infanticidal than males (Marques & Valenstein, 1976) and the Bruce effect is caused more frequently by females than males (Huck, Bracken & Lisk, 1983 ; Huck, 1984). Apparently, females can use odour as well as behavioural (e.g. level of aggression) cues from conspecifics to make such a discrimination (Storey, 1986 ; Storey & Snow, 1990 ; de Catanzaro et al., 1995). In the presence of an unfamiliar male, female house mice and meadow voles can successfully rear more pups if the original fetuses are reabsorbed (Elwood & Kennedy, 1990 ; Storey & Snow, 1990 ; but see Storey, 1994). Although these results are consistent with the idea that pregnancy block is a strategy to prevent losses to infanticide, predators and other potentially stressful factors also may cause pregnancy disruptions in female rodents (de Catanzaro & MacNiven, 1992), which suggests that pregnancy block may be part of a more general strategy to prevent the waste of energy in producing offspring likely to be lost. Among a few primates and perissodactyls (and
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maybe in lions ; Bertram, 1975), abortion by pregnant females has been observed to occur either when one-male groups are taken over by new males or after the attainment of top-ranking dominance status by previously low ranking males living in multimale groups (Berger, 1983 ; Pereira, 1983 ; Mori & Dunbar, 1985 ; Agoramoorthy et al., 1988 ; Colmenares & Gomendio, 1988). These observations are in agreement with the fact that males that are recent immigrants or that have taken over a group of females are typically infanticidal. However, the fact that females typically copulate with the new male after these abortions (Berger, 1983 ; Mori & Dunbar, 1985 ; Colmenares & Gomendio, 1988) also suggests that pregnancy termination might be part of a mechanism of intersexual selection (Storey, 1994). A female could abort the offspring previously sired by a low-quality male to be inseminated by a higher quality male. (2) Maternal aggression Among many mammals, the frequency and intensity of agonistic behaviour by females increases during late gestation and lactation (Ostermeyer, 1983 ; Maestripieri, 1992). The most frequently cited explanation for heightened aggression by lactating females is that it would serve to protect their offspring from infanticidal conspecifics (Svare, 1977 ; Paul, 1986 ; Huck, 1984 ; Parmigiani, 1986 ; Parmigiani et al., 1994). If so, (1) maternal aggression should target those individuals that are the most likely attackers of preweaned infants, (2) the intensity of maternal aggression should increase with the number of vulnerable offspring, and (3) increased aggressiveness by a nursing female should result in a lower probability of her infants being attacked by conspecifics. Regarding prediction (1), lactating female house mice (Parmigiani, 1984 ; Parmigiani, Palanza & Brain, 1989 ; Parmigiani et al., 1994 ; vom Saal et al., 1995 ; Palanza et al., 1996), golden hamsters (Wise & Ferrante, 1982), desert woodrats, Neotoma lepida (Fleming, 1979) and wood mice, Apodemus sylvaticus (Wilson, Elwood & Montgomery, 1993) are selective in chasing and attacking the conspecific gender most likely to kill preweaned pups. Among primates, lactating Japanese macaque females, Macaca fuscata direct their aggression against young females (Troisi et al., 1988), which may be expected from the fact that potentially harmful treatment of infants comes from nulliparous young females that kidnap other female’s infants to practice their maternal skills (Silk,
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1980 ; Collins et al., 1984 ; Troisi et al., 1988). Selective aggression of females is also influenced by the infanticidal propensity of individuals within genders. Female house mice and meadow voles are more likely to attack and direct more harmful bites against infanticidal and more aggressive males than to noninfanticidal and less aggressive males of the same reproductive status (Parmigiani, Sgoifo & Mainardi, 1988 a ; Parmigiani et al., 1988 b ; Elwood, Nesbitt & Kennedy, 1990 ; Storey & Snow, 1990). Among ringtailed lemurs Lemur catta, females with nursing young selectively attack immigrant males that could not be the sires of their current infants, and that are therefore, potentially infanticidal (Pereira & Weiss, 1991). Different studies on rodents and pinnipeds suggest that the presence of vulnerable infants is essential for the expression of postpartum aggression in the females. Aggression by lactating female rodents against potentially infanticidal intruders decreases if their pups are removed experimentally (Gandelman, 1972 b ; Svare & Gandelman, 1973 ; Svare, 1977 ; Erskine, Barfield & Goldman, 1973 a ; Al-Maliki et al., 1980 ; Gandelman & Simon, 1980 ; Giordano, Siegel & Rosenblatt, 1984 ; Mayer et al., 1987 ; Elwood et al., 1990 ; Maestripieri & Alleva, 1990 ; but see Paul, Gronek & Politch, 1980 ; Albert et al., 1987), and the level of maternal aggression is restored if litters are returned to their mothers (Svare & Gandelman, 1973 ; Erskine et al., 1978 a ; Gandelman & Simon, 1980 ; Giordano et al., 1984). Moreover, the intensity of maternal aggression by female house mice increases with the size of their litters (Maestripieri & Alleva, 1990 ; Maestripieri & RossiArnaud, 1991). The presence of infants also influences maternal aggression among female pinnipeds. Aggression by female northern fur seals, Callorhinus ursinus and California sea lions, Zalophus californianus increases as the distance between mothers and their pups decreases (Maestripieri, 1992), and the number of aggressive encounters initiated and won by female northern elephant seals, M. angustirostris decreases after they lose their pups (Ribic, 1988). Evidence supporting the key expectation that maternal aggression should result in a higher likelihood of infant survival seems equivocal. In northern elephant seals, pups of females that are aggressive and active in defending their pups against conspecific females are less likely to be bitten by other females compared with pups of less aggresive cows (Christenson & Le Boeuf, 1978 ; McCann, 1982). As a result, pups of more aggressive females
enjoy a higher probability of survival until weaning age (Christenson & Le Boeuf, 1978 ; Ribic, 1988). In contrast, neonatal survival is not correlated with the overall level of aggression exhibited by lactating females in South American fur seals, Arctocephalus australis (Harcourt, 1991). Similarly, direct aggression by lactating female primates is usually unsuccessful in preventing male infanticide (Mohnot, 1971 ; Watts, 1989). Some laboratory studies on rodents have shown that maternal aggression can be successful in defending litters from potentially infanticidal intruders (Fleming, 1979 ; Takushi et al., 1983 ; Giordano et al., 1984 ; Flannelly & Flannelly, 1985 ; J. O. Wolff, 1985 a ; Storey & Snow, 1987 ; Maestripieri & Alleva, 1990 ; vom Saal et al., 1995). However, many others report that females are only able to delay but not prevent infanticide (Mallory & Brooks, 1980 ; Brooks & Schwarzkopf, 1983 ; J. O. Wolff, 1985 a ; Mennella & Moltz, 1988 ; Parmigiani et al., 1988 a, 1989 ; Elwood et al., 1990 ; Wilson et al., 1993 ; Palanza & Parmigiani, 1994 ; Palanza, Parmigiani & vom Saal, 1994). Providing dams with protected nests having a narrow entrance or the use of a more complex cage arrangement during testing to stimulate more natural conditions (Elwood et al., 1990) does not improve the success of females in defending their pups (Erskine, Denenberg & Goldman, 1978 b ; Palanza & Parmigiani, 1994 ; Palanza et al., 1994 ; Ebensperger, 1998 a ; for an exception see J. O. Wolff, 1985 a). A rather low efficiency of maternal aggression to prevent infanticide in rodents also has been noted under seminatural and natural conditions (Steiner, 1972 ; Armitage et al., 1979 ; McLean, 1982, 1983 ; Michener, 1983 ; Brody & Melcher, 1985 ; Manning et al., 1995). (3) Group defence An additional mechanism by which individuals may prevent infanticide is by means of the formation of coalitions, such that groups of individuals cooperate to repel infanticidal conspecifics (Hrdy, 1977 ; Packer & Pusey, 1983 a ; Lewis & Pusey, 1997). A key prediction of this hypothesis is that vulnerability of infants to potential intruders should decrease with the number of partners participating in their defence. Among African lions, infanticide is committed mainly by groups of males that attempt to take over the females of other male groups (Packer & Pusey, 1984). Female lion groups are more successful in defending their cubs against groups of males com-
Infanticide in mammals pared to solitary females (Packer, Scheel & Pusey, 1990), and females in prides of two to seven females suffer lower rates of male takeovers (i.e. infanticide) than do solitary females (Packer et al., 1988). Playback experiments have revealed that alien male lions are more reluctant to approach playbacks of three females roaring than that of single females, which suggests that maternal groups may also, by roaring in chorus, minimize the chances of encounters with strange (i.e. potentially infanticidal) males (Grinnell & McComb, 1996). After the mating season, male coatis, Nasua nasua, are excluded and treated aggressively by groups of females (Russell, 1981). Male coatis have been observed to cannibalize juveniles (Russell, 1981). The formation of groups to protect young from conspecifics and predators also has been suggested in other carnivores (Camenzind, 1978 ; East, Hofer & Turk, 1989). Among primates the formation of aggressive coalitions against potentially infanticidal males has been documented in Hanuman langurs, Presbytis entellus (Sugiyama, 1965 ; Mohnot, 1971 ; Hrdy, 1974 ; Sommer, 1987 ; Agoramoorthy & Mohnot, 1988), redtail monkeys, Cercopithecus ascanius schmidti (Struhsaker, 1977), blue monkeys, Cercopithecus mitis (Butynski, 1982), red colobus, Colobus badius (Struhsaker & Leland, 1985), baboons, Papio spp. (Collins et al., 1984), red howler monkeys, Alouatta seniculus (Crocket & Sekulic, 1984), capuchin monkeys, Cebus olivaceus (Valderrama et al., 1990), and ringtailed lemurs, Lemur catta (Pereira & Izard, 1989). These coalitions may involve the participation of males (possibly sires) and females (usually relatives of the mother) (Hrdy, 1979 ; Sommer, 1987 ; Struksaker & Leland, 1987). However, primate coalitions are effective in delaying infanticide but rarely in preventing it (Sugiyama, 1967 ; Mohnot, 1971 ; Hrdy, 1977 ; Itani, 1982 ; Crockett & Sekulic, 1984 ; Struhsaker & Leland, 1985 ; Sommer, 1987 ; Agorammorthy & Mohnot, 1988 ; Valderrama et al., 1990). Only in the blue monkey have groups of females been recorded effectively to prevent attacks by infanticidal males (Butynski, 1982). The relatively low success of primate coalitions in preventing infanticide does not support the hypothesis that permanent associations between individuals (e.g. male–female) generally is an adaptation to reduce the risk of infanticide (van Schaik & Kappeler, 1997 ; Sterck, Watts & van Schaik, 1997)). Group defence of infants also may occur in rodents. Female house mice usually from communal nests (Southwick, 1969 ; Sayler & Salmon, 1971 ;
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Wilkinson & Baker, 1988), which may provide protection from conspecific intruders. Under laboratory conditions, females nesting in pairs can be successful in attacking and repelling male and female intruders (Parmigiani, 1986 ; Maestripieri & RossiArnaud, 1991). As a result, infanticide in singlemother nests tends to be twice that observed in communally nesting females of semi-natural populations (Manning et al., 1995). Among Belding’s ground squirrels, related females living in close proximity successfully defend their litters by cooperatively chasing away conspecific intruders (Sherman, 1980). In contrast, pairs of female arctic ground squirrels are rarely successful in chasing infanticidal males (McLean, 1983). (4) Avoidance of infanticidal individuals It has been suggested that females with infants threatened by infanticidal males also may avoid these individuals (Hrdy, 1974, 1977 ; Butynski, 1982 ; Sommer, 1987 ; Sterck, 1998). If so, the infants of nursing females that avoid potential killers should be less frequently attacked compared with those of lactating females staying closer to infanticidal conspecifics. Evidence for such an increased benefit to avoiding females is very limited. After male takeovers, Hanuman langur females may leave their natal group temporarily to travel with ousted males or even attempt to follow a male who has left one troop to take over another (Hrdy, 1977). After male takeovers of prides, mother lions may follow their older cubs to new areas, temporarily becoming nomads (Packer & Pusey, 1983 a). Among rodents, female squirrels and marmots may move their litters away when their territories have been taken over by infanticidal males (McLean, 1983 ; Coulon et al., 1995). By doing so, female alpine marmots have been recorded to successfully wean their infants (Coulon et al., 1995). (5) Promiscuity By mating with several males, females may confuse paternity of their litters and persuade males to tolerate their young once born (Hrdy, 1974, 1977, 1979). Females may confuse paternity by copulating with more than one male during the regular period of oestrus or after conception (i.e. ‘ pseudoestrus ’). In both cases, (1) female promiscuity should increase with the risk of infanticide and (2) infanticidal males should not kill the offspring of previous sexual partners (Hrdy, 1979). Since mating activity, including promiscuous mating, may involve costs to
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the females (Daly, 1978 ; Dewsbury, 1982 ; Magnhagen, 1991 ; Elgar & Wedell, 1996), and mating with noninfanticidal males provides no benefits in terms of a reduced probability of infanticide, (3) females should prefer potentially infanticidal males rather than noninfanticidal males as sexual partners (Birkhead & Møller, 1992 ; Hood, 1994). Finally, (4) the litters of more promiscuous females should be less likely to be attacked by males than those of less promiscuous females. Among primates, evidence supporting the promiscuity hypothesis is equivocal. Prediction (1) seems supported by reports of increased female sexual activity, including mating with multiple males, during the occurrence of male infanticide compared with times at which infanticide does not occur (Struhsaker & Leland, 1985), or after male takeovers (Mohnot, 1971 ; Mori & Dunbar, 1985). Upon the arrival of strange males, pregnant female baboons, Papio hamadryas may shorten their gestation period and resume sexual receptivity sooner after parturition (Colmenares & Gomendio, 1988). On the other hand, postconception mating seems to be rare in female red howler monkeys, and correspondingly, infants born to females that were pregnant during the takeover did not survive (Crockett & Sekulic, 1984). That males should not kill infants born to previous sexual partners is supported by observations showing that infants born after their mothers have mated with infanticidal males during pregnancy (i.e. infanticidal males could not be the sires) usually are not attacked and survive (Hrdy, 1974 ; Struhsaker & Leland, 1985 ; Watts, 1989). In contrast, infants whose mothers do not copulate with new male leaders are attacked and killed by them (Agoramoorthy & Rudran, 1995). However, other studies report females to have mated with infanticidal males but whose infants also were attacked by these males once born (Boggess, 1979 ; Sommer, 1987 ; Crockett & Sekulic, 1984 ; Nishida & Kawanaka, 1985 ; Agoramoorthy & Mohnot, 1988 ; Hamai et al., 1992). Mating preferences for potentially infanticidal males by female primates have been detected during experimental introductions of strange males into forest enclosures. Under these conditions, female lemurs prefer to copulate with recently introduced (immigrant) males even though these copulations are unlikely to result in fertilizations (Pereira & Weiss, 1991). In contrast, female langurs do not discriminate between past sires and incoming (infanticidal) males during takeovers (Sommer, 1987). Some support to the
expectation that offspring born to less promiscuous females, should suffer a higher risk of infanticide than infants born to more promiscuous females is provided by observations on red howler monkeys. Postconception mating by females of this species is rare, and as expected, infants born to females that were pregnant during the takeover usually do not survive (Crockett & Sekulic, 1984 ; Agoramoorthy & Rudran, 1995). A similar situation has been noted in African lions (Packer & Pusey, 1983 b). The possibility that females might use promiscuity to prevent male infanticide also has been suggested in rodents (Wolff, 1989 ; Wolff & Cicirello, 1989). Under semi-natural conditions, female Norway rats (Calhoun, 1962), house mice (Reimer & Petras, 1967 ; R. J. Wolff, 1985 ; Potts, Manning & Wakeland, 1991), and Mongolian gerbils (AI gren, 1976) visit and mate with neighbouring males, which might be a strategy to reduce the probability of infanticide later on. To date, only one study reports a potential relationship between the occurrence of postconception oestrus and the risk of infanticide (i.e. prediction 1 above). Among water voles, Arvicola terrestris, pregnant females that move their nest location into the home range of a new male, but not females who stay within their original male’s range, were detected to mate (Jeppsson, 1986). Thus, pregnant water voles might mate with the resident male to prevent infanticide (Jeppsson, 1986). Although this case is suggestive, the precise identity of the pregnant females’ sexual partners is not known with certainty, and infanticide has not yet been reported in water voles. The expectation that infanticidal male rodents should not kill the offspring of previous sexual partners is supported by the observation that male house mice introduced into the cage of either their previous mate or a strange female are more likely to kill pups in the cage of a strange female, even if it contains foster pups actualy fathered by the test male (Huck et al., 1982). However, several other studies have failed to replicate these results (Brooks & Schwarzkopf, 1983 ; McCarthy & vom Saal, 1986 b ; Parmigiani, 1989 ; Elwood & Kennedy, 1991). The observation that female meadow voles and house mice do not prefer infanticidal over noninfanticidal conspecific males as potential mating partners fails to support prediction 3 (Ebensperger, 1998 b). (6) Territoriality An additional strategy that individuals could use to prevent infanticide is defending a territory such that
Infanticide in mammals potential intruders are kept away from vulnerable infants. This model, also known as the pup defence hypothesis, has been invoked to explain female territoriality among rodents (Sherman, 1981 ; Webster & Brooks, 1981 ; McLean, 1983 ; Michener, 1983 ; Brooks, 1984 ; Wolff, 1993). The pup defence hypothesis predicts that (1) territoriality should be directed against all conspecifics likely to commit infanticide. In addition, (2) territory defence should be more intense at the time when infants are more vulnerable, and in places closest to the nest burrow (Wolff, 1993). Further, (3) nests or burrows containing nursing infants should be located in the centre (i.e. away from conspecific neighbours) rather than in the periphery of a territory, and (4) the probability of a female losing infants to conspecifics should decrease with territory size or intensity of territorial defence. Among rodents, some support for prediction (1) comes from a fit between the identity of infanticidal intruders and the target of territoriality. Thus, both males and females may commit infanticide among Belding’s ground squirrels (Sherman, 1980, 1981), black-tailed prairie dogs (Hoogland, 1985, 1995), and wild house mice (Soroker & Terkel, 1988), and as expected, both male and female conspecifics are excluded from the territory of lactating females (Sherman, 1981 ; Chovnick et al., 1987 ; Hoogland, 1995). However, discordance between the identity of infanticidal intruders and the target of territoriality is frequent. Infanticide in Columbian ground squirrels is committed by the females (Hare, 1991), but female territoriality is directed equally against males and females (Festa-Bianchet & Boag, 1982 ; Murie & Harris, 1994). Similarly, the male (not female) arctic ground squirrels (McLean, 1983) and alpine marmots (Coulon et al., 1995) are infanticidal but female territoriality is directed against other females rather than males (McLean, 1982 ; Arnold, 1990). In arctic ground squirrels, however, male rather than female territoriality may prevent infanticide (McLean, 1983). Among wood mice (Wilson et al., 1993), meadow voles (Thomas, 1988), white-footed mice (Wolff & Cicirello, 1991), and deer mice (Wolff & Cicirello, 1991), both male and females kill pups, but females in all these species are territorial only against other females (Madison, 1980 ; Wolff, 1985 b ; Wolton, 1985). With a few exceptions, the intensity of female territoriality increases during pregnancy, peaks during early to mid lactation, and decreases after the weaning of infants (Ostermeyer, 1983 ; Maestripieri, 1992). Also, female territoriality is more intense close
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to the females’ nest site rather than in the periphery of their territories (Wolff, Freeberg & Dueser, 1983 ; Murie & Harris, 1994). However, nests of breeding females are not necessarily located in the core as opposed to the periphery of their territories (Brooks & Banks, 1971 ; Wolton, 1985 ; Ribble & Salvioni, 1990). Evidence showing a negative relationship between the size of a territory or the intensity of territory defence and the risk of infanticide is limited. Only among Belding’s squirrels is the size of the territory of a lactating female inversely correlated with the probability of losing infants to infanticide (Sherman, 1981). More often, female rodents restrict their activities to a small portion of their territory, around their nest during lactation (Brooks & Banks, 1971 ; Madison, 1978 ; Festa-Bianchet & Boag, 1982 ; Wilkinson & Baker, 1988 ; Koskela, Mappes & Ylo$ nen, 1997), suggesting that protection of infants may not require excluding conspecifics from a larger area. The pup defence hypothesis also might apply to other mammals. In particular, southern sea lion, Otaria byronia, pups of females remaining in colonies are more protected from harassment and infanticide by subordinate males than those of females forming solitary breeding male–female pairs (Campagna et al., 1992). It seems that by excluding subordinate males from the harem territory, dominant haremholding males provide indirect protection to the females and their pups (Campagna et al., 1992). The role that infant protection against conspecifics may have in the territorial behaviour of other carnivores and mammalian groups (for primates see van Schaik & Dunbar, 1990), still needs to be evaluated.
IV. CONCLUSIONS
Among benefits to infanticide, nutritional gains are probably involved in the killing of infants by male and female rodents. The applicability of the predation hypothesis to primates (e.g. common chimpanzee) and terrestrial carnivores still needs to be evaluated. Measuring the abundance, distribution and renewability of food resources and how these variables correlate with the frequency of infanticide may help to test the predation hypothesis further. That the resource competition hypothesis might explain the occurrence of infanticide among some primates, carnivores and lagomorphs needs to be evaluated along with the adoption avoidance model as an alternative hypothesis. Among rodents, most
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evidence supporting a scenario of competition for resources comes only from the behaviour of female Belding’s ground squirrels. Showing that infanticidal animals obtain resources previously used by their victim’s sires is essential to provide a case for the resource competition hypothesis. The most compelling evidence supporting the idea that individuals commit infanticide to avoid misdirecting parental care to unrelated offspring comes from the infanticidal behaviour of female pinnipeds. In contrast, evidence for this hypothesis among other groups such as carnivores, a few primates, and rodents is largely circumstantial and also consistent with alternative interpretations. Future studies testing this model need to show that infanticidal individuals enjoy a lower risk of adopting unrelated infants compared with noninfanticidal animals. The killing of infants by males to obtain reproductive advantages seems well supported in primates and African lions. In the future, long-term studies should focus on monitoring the reproductive behaviour of the killers and the victim’s mother. Estimates of paternity are required to assess reproductive benefits to infanticidal males. The possibility that sexually selected infanticide takes place among male rodents (particularly Muridae) still needs further examination. In particular, studies measuring fitness benefits in terms of increased mating opportunities or of speeded birth of their own infants by infanticidal males with their victim’s dams under wild or semi-natural conditions (Manning et al., 1995) are strongly needed. Nonadaptive explanations for infanticide (and for any other behaviour) are difficult to accept as some new untested benefit always could be invoked to explain the behaviour of interest. Currently, nonadaptive explanations for infanticide may apply to infant killing by male pinnipeds. Testing for correlations between infanticide and some other phenotypic features should be investigated to test the possibility that infanticide resulted from selection for some other characteristic, including predation, territoriality or aggression (Johns & Maxwell, 1997). Among potential counterstrategies to infanticide, pregnancy block may function as such in some rodents. However, the significance of pregnancy termination within other groups (e.g. primates) still needs to be studied. In particular, contrasting the fitness of females that terminate their pregnancies with those that do not do so when dealing with infanticidal conspecifics are needed. Circumstances, other than the presence of infanticidal conspecifics, that also result in females terminating their
Luis A. Ebensperger pregnancies should be considered as they may provide additional clues to the adaptive bases of this phenomenon. Preventing infanticide is perhaps the most common explanation offered for the enhanced aggression exhibited by lactating females. Overall, however, maternal aggression seems ineffective in saving infants from conspecific attacks, which questions the validity of the above interpretation. One possibility is that even though maternal aggression is rarely effective in preventing infanticide, it still pays for a female to defend her litter aggressively as occasionally she will succeed. Alternatively, females may use maternal aggression together with other counterstrategies simultaneously. If so, maternal aggression could have been selected as part of a suite of different strategies (Parmigiani et al., 1994). Evidence suggests that the formation of coalitions to defend infants aggressively is common and relatively effective among African lions and some rodents (house mice, Belding’s squirrels). In contrast, group defence of infants is rarely an efficient strategy against infanticide among primates. Overall, more studies are needed to confirm the relationship between coalition size and infant survival among group-forming species where attacks on infants by conspecifics (not necessarily resulting in infanticide) are rather common. The avoidance of infanticidal individuals is considered less often compared with other potential counterstrategies to infanticide. Future studies should concentrate on monitoring the weaning success of females that move actively after the arrival of infanticidal conspecifics and that of females that stay. This issue is particularly relevant as pregnant or lactating females that move to new sites (to avoid infanticide in their former location) are likely to find strange conspecifics which may decrease the value of changing location as a useful tactic to prevent infanticide. Promiscuity (including pseudooestrus) is often cited as a counterstrategy to infanticide. The promiscuity hypothesis seems partly supported among some primates and rodents. In the case of primates, however, males do not always tolerate infants of previous sexual partners. Clearly, more information that includes direct observations of copulations and estimates of paternity before, during, and after episodes of infanticide are needed. Among rodents, comparing the weaning success of females that differ in the extent of promiscuity are essential to test this model. Mating with multiple males may serve several functions other than
Infanticide in mammals preventing infanticide (Birkhead & Møller, 1992 ; O’Connell & Cowlishaw, 1994), so showing results not predicted by alternative hypotheses is critical to provide a strong case for a functional relationship between the risk of infanticide and promiscuity. Defending a territory to protect offspring is an attractive hypothesis. However, evidence supporting this model is still limited to a few species of rodents and it is largely correlational in nature. As in the case of promiscuity, territoriality may serve functions other than protecting infants from conspecifics (Ostfeld, 1990 ; Koskela et al., 1997), so studies should be designed to distinguish among two or more alternatives. Moreover, infanticide may be a consequence rather than a cause of territoriality (Tuomi et al., 1997). Overall, supporting evidence for individual benefits and counterstrategies to infanticide varies considerably among and within different groups of mammals. The possibility that this variation reflects a situation in which benefits of, and counterstrategies against, infanticide differ across species and ecological contexts needs to be separated from an alternative situation in which this variation simply reflects a bias in the number of studies attempting to assess particular benefits and counterstrategies. In fact, among potential benefits of infanticide by male primates, the sexual selection hypothesis is by far the most commonly examined and, correspondingly, the most supported model. Future studies measuring benefits of infanticide, as well as those examining mechanisms to prevent it, need to consider different possibilities simultaneously. On the one hand, killers might achieve different benefits simultaneously. For instance, a female could kill the offspring of another female to usurp the burrow previously owned by the victim’s mother and also benefit after cannibalizing the victims. Similarly, individuals (particularly the females) may use different strategies (or a combination of them) to prevent infanticide. Which particular strategy is chosen will depend both on the potential costs as well as on physiological and social constraints involved. Thus, maternal aggression may be extremely costly to female lions that have been observed to be seriously injured or even killed by infanticidal males (Packer & Pusey, 1983 a). Under these conditions, the formation of cooperative alliances to repel conspecifics might be a more viable option in the case of social species. On the other hand, confusing paternity by multiple mating may not be an option to females living in one-male (as opposed to multi-male) groups (Hausfater, 1984),
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