Exposure to strange adults does not cause pregnancy disruption or infanticide in the gray-tailed vole

A widely accepted paradigm in mammalian behavioral biology is that exposure to unfamiliar males causes pregnancy disruption in female rodents (commonly known as the Bruce effect). This behavioral phenomenon has been demonstrated in the laboratory with at least 12 species of rodents, primarily within the genus Microtus, and is supposedly an adaptation that provides male perpetrators with reproductive access to females, and functions, for females, as a counterstrategy to infanticide. However, neither the Bruce effect nor its adaptive significance have been tested experimentally in the field. In a controlled field study, we exposed reproducing female gray-tailed voles (Microtus canicaudus) to treatments in which males were removed and replaced by either unfamiliar males or females, and found no significant differences in intervals between parturitions, number of pregnancies, and juvenile recruitment among the treatment and control animals. Thus, we conclude that neither the Bruce effect nor infanticide occurred differentially as a consequence of the treatments in gray-tailed voles. Multimale mating to confuse paternity, and postpartum estrus resulting in simultaneous pregnancy and lactation may deter infanticide and functionally negate any benefits of pregnancy disruption in gray-tailed voles and perhaps other murid rodents with similar mating systems. In light of our results, we recommend field verification for other species of murid rodents that exhibit the Bruce effect in the laboratory before the results are applied to evolutionary theory. Received: 12 May 1998 / Accepted after revision: 6 September 1998     

The functional significance of infanticide in a population of California ground squirrels (Spermophilus beecheyi)

Naturally-occurring infanticide was observed in a population of California ground squirrels (Spermophilus beecheyi). In four seasons, 40 infanticides were observed. All victims were post-emergent pups. Of 37 killings in which the killer was sexed 36 were by females. All infanticidal females were mothers at the time they killed, but in no case was a mother seen to kill or harm her own young. The victim was cannibalized in 22 cases and taken immediately into the killer’s burrow in 16 others. In no case did killers gain access to the victimized mother’s burrow or territory and female pups were not killed preferentially over males. In light of evolutionary explanations, infanticide in this population may best fit the resource exploitation hypothesis, in which killers commit infanticide to gain a nutritional benefit. Resource competition is a possible auxiliary explanation, since any time a female kills unrelated young she is eliminating possible competitors to her own offspring. This behavior could confer a fitness advantage on killers or it could be an adaptively neutral, alternative feeding strategy. More data are necessary to distinguish between these hypotheses. Received: 26 January 1995/Accepted after revision: 9 September 1995     

Individual differences in the mechanisms underlying the onset and maintenance of paternal behavior and the inhibition of infanticide in the monogamous biparental California mouse,Peromyscus californicus

Virgin male Peromyscus californicus tend to behave infanticidally or nonparentally towards pups, whereas virtually all males exhibit parental behavior following birth of their own young. Most males (65–75%) living with their pregnant partner attacked or ignored unfamiliar pups and did not become parental (behave parentally) prior to birth of their young. However, a significant minority of males (34%) living with their partner became parental after just 24 h of postcopulatory cohabitation with the female and remained parental throughout their mate's pregnancy. Males that were infanticidal before the birth of their young became parental only after their young were born. The presence of the mother was necessary for the postpartum maintenance of paternal behavior and the inhibition of infanticide in males that were infanticidal prepartum. In contrast, males that were paternal prior to birth of their young continued to be paternal after birth, even in the absence of postpartum contact with the mother. Thus, different mechanisms are involved in the inhibition of infanticide and the onset and maintenance of paternal behavior. Correspondence to: D.J. Gubernick     

Infant care,infanticide, and female reproductive strategies in polygynous groups of common marmosets (Callithrix jacchus)

Reproduction in marmoset and tamarin groups is typically restricted to a single dominant female, but it is unclear why subordinate females tolerate delayed reproduction. The presence of two breeding females in free-ranging groups of common marmosets (Callithrix jacchus) presented a unique opportunity to examine differences in the reproductive strategies of dominant and subordinate females. Three groups were monitored for 12–18 months at a forest reserve in northeastern Brazil. Data on infant care were collected during two consecutive all-day follows every 10 days until the infants were 2 months old. Carrying patterns for infants born to dominant females were similar to those observed in groups containing a single breeding female. All group members over 5 months of age participated in infant care, and dominant females allowed some group members to carry their infants from the 1 st day of life. In contrast, subordinate females were protective of their offspring and were their sole caretakers for at least a week following birth. One infant born to a subordinate was killed in an attack involving the dominant female. Overall, dominant females gave birth to more infants and had higher infant survival than did subordinate breeding females. subordinate females were successful in rearing young only when the timing of births was such that they did not overlap with the dependency period of infants born to the dominant female. These patterns suggest that subordinate females may face resource competition, especially over access to helpers. In times of severe competition, subordinate females that delay reproduction may be avoiding a wasted reproductive effort.     

Vigilance in wild Thomas's langurs (Presbytis thomasi ): the importance of infanticide risk

This study examines vigilance as a behavioural indicator of the importance of infanticide risk by comparing the infanticide avoidance hypothesis with the predation avoidance and mate defence hypotheses for wild Thomas's langurs (Presbytis thomasi) in Sumatra. We found that all individuals were more vigilant in situations of high predation risk, i.e. lower in the trees and in the absence of neighbours. Females were also more vigilant on the periphery of the group. However, there were variations in vigilance levels that could not be accounted for by the predation avoidance hypothesis. Males without infants showed higher levels of vigilance in areas of home range overlap than in non-overlap areas during the early phase of their tenure, strongly suggesting mate defence. In these areas of home range overlap where Thomas's langur groups can interact, males may attack females and infants, and so the infanticide risk for males and females with infants is likely to be high in these areas. Only females with infants, but not males with infants or females without infants, showed higher vigilance levels in overlap areas than in non-overlap areas; in addition, in overlap areas, females with an infant were more vigilant than females without an infant, while this was not the case in non-overlap areas. Both females and males with infants were more vigilant high in the trees than at medium heights in overlap areas but not elsewhere. These findings can only be explained by the infanticide avoidance hypothesis. In contrast to predator attacks, infanticidal male attacks come from high in the canopy, and only occur in overlap areas. There was a significant sex difference in vigilance, but males were only more vigilant than females without an infant, and not more vigilant than females with an infant. We conclude that vigilance varied mainly in relation to the risk of predation and infanticide. Mate competition only played a role for males during the early phase of their tenure. Predation risk seems to offer the best explanation for vigilance for all individuals in the absence of infants. Both predation risk and infanticide risk played a role for females and males with infants. Received: 4 April 1998 / Accepted after revision: 6 September 1998     

The evolution of female social relationships in nonhuman primates

Considerable interspecific variation in female social relationships occurs in gregarious primates, particularly with regard to agonism and cooperation between females and to the quality of female relationships with males. This variation exists alongside variation in female philopatry and dispersal. Socioecological theories have tried to explain variation in female-female social relationships from an evolutionary perspective focused on ecological factors, notably predation and food distribution. According to the current “ecological model”, predation risk forces females of most diurnal primate species to live in groups; the strength of the contest component of competition for resources within and between groups then largely determines social relationships between females. Social relationships among gregarious females are here characterized as Dispersal-Egalitarian, Resident-Nepotistic, Resident-Nepotistic-Tolerant, or Resident-Egalitarian. This ecological model has successfully explained differences in the occurrence of formal submission signals, decided dominance relationships, coalitions and female philopatry. Group size and female rank generally affect female reproduction success as the model predicts, and studies of closely related species in different ecological circumstances underscore the importance of the model. Some cases, however, can only be explained when we extend the model to incorporate the effects of infanticide risk and habitat saturation. We review evidence in support of the ecological model and test the power of alternative models that invoke between-group competition, forced female philopatry, demographic female recruitment, male interventions into female aggression, and male harassment. Not one of these models can replace the ecological model, which already encompasses the between-group competition. Currently the best model, which explains several phenomena that the ecological model does not, is a “socioecological model” based on the combined importance of ecological factors, habitat saturation and infanticide avoidance. We note some points of similarity and divergence with other mammalian taxa; these remain to be explored in detail. Received: 30 September 1996 / Accepted after revision: 20 July 1997     

Ecological and social determinants of spacing behaviour in desert baboon groups

This paper investigates the determinants of individual spacing behaviour in a desert baboon population (Papio cynocephalus ursinus). Patterns of neighbour proximity and neighbour density were examined among adults in four groups under different ecological and social conditions (through instantaneous sampling during focal follows). Initial analysis of these data shows that (1) the use of vertical substrates (refuges such as tall trees and cliff faces) can confound patterns of spacing, and (2) individual differences in spacing can depend on the spatial scale over which it is measured. To minimise these substrate and scale effects, this analysis focuses on animals which are off refuges and examines spacing behaviour through its underlying statistical `dimensions' (identified through factor analysis). Analysis of these dimensions indicates that sex, group size, activity-habitat and female reproductive state can all have independent effects on spacing: (1) males are more dispersed than females in smaller groups, (2) male and female dispersion increases with time spent in foraging habitats, and (3) female dispersion is reduced during lactation. According to the hypotheses tested, these results indicate that feeding competition only affects spacing behaviour during foraging while predation risk plays little or no role in spacing. Most aspects of spacing behaviour are best explained by male reproductive strategies and their social repercussions. Received: 25 May 1998 / Accepted after revision: 18 July 1998     

Behavioral and demographic changes following the loss of the breeding female in cooperatively breeding marmosets

Recent models of the evolution and dynamics of family structure in cooperatively breeding vertebrates predict that the opening of breeding vacancies in cooperatively breeding groups will result in (1) dispersal movements to fill the reproductive position, and (2) within-group conflict over access to reproduction. We describe the behavioral and demographic changes that followed the creation of breeding vacancies in three wild groups of cooperatively breeding common marmosets (Callithrix jacchus). Replacement of the breeding female was rapid when no adult females remained in the group, but did not occur for several months when other adult females were present. Aggression of adult animals towards same-sex potential immigrants was associated with a period of reduced affiliation, increased intragroup agonism, no intragroup sexual behavior, and frequent extragroup copulations. This ended with the fissioning of groups along sexual lines. After replacement, multiple males copulated with multiple females and vice versa, with no increases in sexually related aggression. Female-female conflict was resolved through infanticide. The lack of direct conflict between males is consistent with cooperative polyandry. After a breeding vacancy appeared, marmoset groups showed conflict of interests among group members similar to those shown by cooperatively breeding birds, but they used different behavioral mechanisms to resolve those conflicts. Our data provide important evidence from a cooperatively breeding mammal to support Emlen’s model for the evolution of vertebrate families, but they suggest that species-specific inter- and intrasexual competitive strategies should be considered before the model can be applied to other cooperatively breeding vertebrates. Received: 23 November 1999 / Received in revised form: 28 March 2000 / Accepted: 1 April 2000     

Conspecific threat,predation avoidance,and resource defense: implications for grouping in langurs

Data on langur (Presbytis entellus) populations were gathered from the literature to test the importance of three selective pressures in determining group size and composition: predation pressure, intergroup resource defense, and conspecific threat. There were no detectable difference in the size of groups in populations facing nearly intact predator communities compared to those populations where predators were severely reduced in number or absent, although there was a trend for the number of adult males per group to increase in areas with nearly intact predator communities. Using population density as an indirect measure of the frequency of intrusions into a group’s home range and thereby as an index of the demographic pressure favoring resource defense, we predicted that higher densities would result in larger defensive coalitions and higher numbers of females per group. This prediction was not upheld. Our third selective pressure, conspecific threat, encompasses those selective forces resulting from physical attack on females, infants, and juveniles. Our index of conspecific threat uses the number of non-group males divided by the number of bisexual groups, because in langurs, the major source of conspecific threat derives from non-group males who, following group take-over, kill infants, wound females, and expel juveniles from groups. This index of conspecific threat was strongly related to the mean number of resident females, was weakly related to the mean group size, but was not related to the number of males in the group. In addition, as predicted, populations with a high index of conspecific threat had higher levels of juvenile expulsion. These analyses were corroborated by a simulation model which used a computer-generated series of null populations to calculate expected slopes of immatures regressed on adult females. These randomly generated populations, matched to means and ranges of real populations, allowed us to determine if deviations of the observed slopes from the expected null slopes could be explained by variation in predation pressure, population density, or conspecific threat. We found no evidence that predation pressure was associated with decreases in immature survival in smaller groups, as would be predicted by the predation-avoidance hypothesis. We found no evidence that immature survival was compromised by small group size in high-density populations, as would be predicted by the resource-defense hypothesis. However, as the index of conspecific threat increased, groups with larger numbers of females were more successful than groups with fewer females in reducing mortality or expulsion of immatures. Overall, conspecific threat received the strongest support as a selective pressure influencing langur group size and composition, suggesting that this selective pressure should be evaluated more widely as a factor influencing composition of animal groups. Received: 23 January 1995/Accepted after revision: 18 February 1996     

Higher rate of nest loss among primary than secondary females: infanticide in the great reed warbler?

An individually marked population of great reed warblers Acrocephalus arundinaceus was studied between 1984 and 1991 in South Central Sweden. The fates of 279 nests were analysed for the 25 days following clutch initiation. The average frequency of nest loss (43%) did not differ significantly between years or between four periods of the breeding season. After a breeding failure, 70% of the females laid a replacement clutch, most of them together with the same male. On polygnous territories, males assisted the female who first hatched young regardless of her initial mating status (Fig. 2). According to the acutal status of the females attending the nests, for each day nests were classified as being of either monogamous (M), primary (P) or secondary (S) status. From egg-laying to fledging the rate of nest loss decreased among nests of primary status whereas it increased among nests of monogamous and secondary status. During the egg-laying period, the rate of nest loss was 3 times higher among nests of primary than among nests of monogamous and secondary status (Fig. 3). Thus, the high loss level among nests of primary status during the laying period was closely associated with the presence of a female with a less advanced nest on the territory. All nests were situated in reed beds above deep water and most of them at a height at which possible inter-specific nest predators would have caused disturbance to the nest itself. The suspicion that secondary females committed sexually selected infanticide was supported by an experiment with dummy eggs that revealed bill peck markings identical to those obtained from great reed warblers (Fig. 4).