Alpha male chimpanzee grooming patterns: implications for dominance "style".

In social primates, individuals use various tactics to compete for dominance rank. Grooming, displays and contact aggression are common components of a male chimpanzee's dominance repertoire. The optimal combination of these behaviors is likely to differ among males with individuals exhibiting a dominance "style" that reflects their tendency to use cooperative and/or agonistic dominance tactics. Here, we examine the grooming behavior of three alpha male chimpanzees at Gombe National Park, Tanzania. We found that (1) these males differed significantly in their tendency to groom with other males; (2) each male's grooming patterns remained consistent before, during and after his tenure as alpha, and (3) the three males tended to groom with high- middle- and low-ranking partners equally. We suggest that body mass may be one possible determinant of differences in grooming behavior. The largest male exhibited the lowest overall grooming rates, whereas the smallest male spent the most time grooming others. This is probably because large males are more effective at physically intimidating subordinates. To achieve alpha status, a small male may need to compensate for reduced size by investing more time and energy in grooming, thereby ensuring coalitionary support from others. Rates of contact aggression and charging displays conformed to this prediction, suggesting that each male exhibited a different dominance "style."

Causes of death in the Kasekela chimpanzees of Gombe National Park, Tanzania.

Understanding the rates and causes of mortality in wild chimpanzee populations has important implications for a variety of fields, including wildlife conservation and human evolution. Because chimpanzees are long-lived, accurate mortality data requires very long-term studies. Here, we analyze 47 years of data on the Kasekela community in Gombe National Park. Community size fluctuated between 38 and 60, containing 60 individuals in 2006. From records on 220 chimpanzees and 130 deaths, we found that the most important cause of mortality in the Kasekela community was illness (58% of deaths with known cause), followed by intraspecific aggression (20% of deaths with known cause). Previous studies at other sites also found that illness was the primary cause of mortality and that some epidemic disease could be traced to humans. As at other study sites, most deaths due to illness occurred during epidemics, and the most common category of disease was respiratory. Intraspecific lethal aggression occurred within the community, including the killing of infants by both males and females, and among adult males during the course of dominance-related aggression. Aggression between communities resulted in the deaths of at least five adult males and two adult females in the Kasekela and Kahama communities. The frequency of intercommunity violence appears to vary considerably among sites and over time. Intercommunity lethal aggression involving the Kasekela community was observed most frequently during two periods. Other less common causes of death included injury, loss of mother, maternal disability, and poaching.

Using retrospective health data from the Gombe chimpanzee study to inform future monitoring efforts.

Disease outbreaks, either in isolation or in concert with other risk factors, can pose serious threats to the long-term persistence of mammal populations, and these risks become elevated as population size decreases and/or population isolation increases. Many chimpanzee study sites are increasingly isolated by loss of habitat due to human encroachment, and managers of parks that contain chimpanzees perceive that disease outbreaks have been and continue to be significant causes of mortality for chimpanzees. Major epidemics at Gombe National Park include suspected polio in 1966; respiratory diseases in 1968, 1987, 1996, 2000, and 2002; and sarcoptic mange in 1997. These outbreaks have led park managers and researchers working in Gombe to conclude that disease poses a substantial risk to the long-term survival of Gombe's chimpanzee population. We surveyed behavioral data records spanning 44 years for health-related data and found a combination of standardized and nonstandardized data for the entire period. Here we present the types of data found during the survey, discuss the usefulness of these data in the context of risk assessment, and describe how our current monitoring effort at Gombe was designed based on our findings.

Egalitarianism in female African lions.

Because most cooperative societies are despotic, it has been difficult to test models of egalitarianism. Female African lions demonstrate a unique form of plural breeding in which companions consistently produce similar numbers of surviving offspring. Consistent with theoretical predictions from models of reproductive skew, female lions are unable to control each other's reproduction because of high costs of fighting and low access to each other's newborn cubs. A female also lacks incentives to reduce her companions' reproduction, because her own survival and reproduction depend on group territoriality and synchronous breeding. Consequently, female relationships are highly symmetrical, and female lions are "free agents" who only contribute to communal care when they have cubs of their own.

Noninvasive paternity assignment in Gombe chimpanzees.

The relative success of chimpanzee male mating strategies, the role of male dominance rank and the success of inbreeding avoidance behaviour can only be assessed when paternities are known. We report the probable paternities of 14 chimpanzees included in a long-term behavioural study of chimpanzees (Pan troglodytes schweinfurthii) at Gombe National Park, Tanzania. DNA samples were collected noninvasively from shed hair and faeces and genotyped using 13-16 microsatellite loci characterized in humans. All 14 offspring could be assigned to fathers within the community. While there is a positive relationship between male rank and reproductive success, we demonstrate that a range of male mating strategies (possessiveness, opportunistic mating and consortships) can lead to paternity across all male ranks. Several adult females were at risk of breeding with close male relatives. Most successfully avoided close inbreeding but in one case a high-ranking male in the community mated with his mother and produced an offspring. In contrast to recent data on chimpanzees (P. t. verus) from the Taï forest, Côte d'Ivoire, no evidence of extra-group paternity was observed in our study. Reanalysis of Taï data using a likelihood approach casts doubt on the occurrence of extra-group paternity in that community as well.

Mortality rates among wild chimpanzees.

In order to compare evolved human and chimpanzees' life histories we present a synthetic life table for free-living chimpanzees, derived from data collected in five study populations (Gombe, Taï, Kibale, Mahale, Bossou). The combined data from all populations represent 3711 chimpanzee years at risk and 278 deaths. Males show higher mortality than females and data suggest some inter-site variation in mortality. Despite this variation, however, wild chimpanzees generally have a life expectancy at birth of less than 15 years and mean adult lifespan (after sexual maturity) is only about 15 years. This is considerably lower survival than that reported for chimpanzees in zoos or captive breeding colonies, or that measured among modern human hunter-gatherers. The low mortality rate of human foragers relative to chimpanzees in the early adult years may partially explain why humans have evolved to senesce later than chimpanzees, and have a longer juvenile period.

The influence of dominance rank on the reproductive success of female chimpanzees.

Female chimpanzees often forage alone and do not display obvious linear dominance hierarchies; consequently, it has been suggested that dominance is not of great importance to them. However, with the use of data from a 35-year field study of chimpanzees, high-ranking females were shown to have significantly higher infant survival, faster maturing daughters, and more rapid production of young. Given the foraging behavior of chimpanzees, high rank probably influences reproductive success by helping females establish and maintain access to good foraging areas rather than by sparing them stress from aggression.

Development of cooperative territoriality in juvenile lions.

African lions, Panthera leo, engage in many cooperative activities including hunting, care of young, and group territoriality, but the contribution of juvenile lions to these activities has never been documented. Here we present experimental evidence that juvenile lionesses make a gradual transition to group-territorial defence between weaning (8 months) and sexual maturity (42 months). When challenged by simulated intruders played from a loud-speaker, juvenile females (but not males) become progressively more likely to join the adult females in territorial defence with age, and their behaviour is affected by both the number of defending adults and the number of intruders. We interpret the ability of juveniles to assess relative numbers as an adaptation for assessing the risk of territorial conflict according to their own fighting ability, and the ability of their pride of successfully defend the territory. The difference between the sexes reflects the greater value of the natal territory to philopatric females. Adult females display a variety of strategies when defending the territory, including unconditional and conditional forms of cooperation. We show here that individuals display the rudiments of these strategies as juveniles.

Inbreeding avoidance in animals.

The phenomenon of inbreeding depression is well documented and behavioral adaptations for inbreeding avoidance have been described. However, there is debate over whether inbreeding depression is always an important selective force on behavior. Here, we summarize recent evidence for inbreeding depression under natural conditions, review inbreeding avoidance mechanisms, and discuss how these are influenced by social structure. We also examine the idea that animals have evolved mechanisms to avoid outbreeding.

Female lions can identify potentially infanticidal males from their roars.

Despite evidence from several bird, fish and mammal species that listeners can discriminate between the vocalizations of familiar and unfamiliar adult conspecifics, direct links between discriminatory abilities and fitness benefits have been difficult to identify. In free-ranging populations of African lions (Panthera leo), females with cubs face a substantial threat from one particular category of unfamiliar individuals: infanticidal males. Here we use playback experiments to demonstrate that females with cubs can distinguish immediately between roars from their own resident males (the fathers of the cubs) and those from unfamiliar, potentially infanticidal males. Although they remain relaxed when played roars from resident males, they immediately become agitated on hearing unfamiliar males and retreat rapidly with their cubs if the latter have reached about 4.5 months of age. These responses are not simply a function of the roarers being unfamiliar, for when played the roars of unfamiliar females, females with cubs consistently approach the loudspeaker. Furthermore, females often move toward the cubs in response to playbacks of unfamiliar males but not in response to playbacks of unfamiliar females or resident males. Our results suggest how females with cubs might, by quickly detecting and categorizing unfamiliar intruders within their territory, protect their cubs from infanticidal males and expel intruding females. Distinguishing between individuals on the basis of their vocal characteristics could therefore confer direct fitness benefits on discriminating lionesses.

Hormonal characteristics of free-ranging female lions (Panthera leo) of the Serengeti Plains and Ngorongoro Crater.

Pituitary responses to gonadotrophin-releasing hormone (GnRH) and prolactin and steroid secretory profiles were examined in two populations of adult, female lions in the Serengeti (one outbred in the Serengeti Plains and one inbred in the Ngorongoro Crater) to determine whether reductions in genetic variability adversely affected endocrine function. GnRH-induced gonadotrophin secretion was also examined after adrenocorticotrophic hormone (ACTH) treatment to determine whether acute increases in serum cortisol altered pituitary function. Anaesthetized lions were administered (i) saline i.v. after 10 and 100 min of blood sampling, (ii) saline at 10 min and GnRH (1 micrograms kg-1 body weight) after 100 min; or (iii) ACTH (3 micrograms kg-1) at 10 min and GnRH after 100 min of sampling. Basal serum cortisol and basal and GnRH-induced gonadotrophin secretion were similar (P > 0.05) between females of the Ngorongoro Crater and Serengeti Plains. After ACTH, serum cortisol increased two- to threefold over baseline values and the response was unaffected (P > 0.05) by location. ACTH-induced increases in serum cortisol had no effect on subsequent basal or GnRH-stimulated luteinizing hormone (LH) or follicle-stimulating hormone (FSH) secretion. Overall mean serum progesterone concentrations ranged from 0.2 to 5.4 ng ml-1 with the exception of four females (two in the Serengeti and two in the Crater; progesterone range, 18.4-46.5 ng ml-1) that were presumed pregnant (three of these females were observed nursing cubs several weeks later).(ABSTRACT TRUNCATED AT 250 WORDS)

Analytical DNA fingerprinting in lions: parentage, genetic diversity, and kinship.

The application of hypervariable minisatellite genomic families to the reconstruction of population genetic structure holds great promise in describing the demographic history and future prospects of free-ranging populations. This potential has not yet been realized due to unforeseen empirical constraints associated with the use of heterologous species probes, to theoretical limitations on the power of the procedure to track genic heterozygosity and kinship, and to the absence of extensive field studies to test genetic predictions. We combine here the technical development of feline-specific VNTR (variable number tandem repeat) families of genetic loci with the long-term demographic and behavioral observations of lion populations of the Serengeti ecosystem in East Africa. Minisatellite variation was used to quantify the extent of genetic variation in several populations that differed in their natural history and levels of inbreeding. Definitive parentage, both maternal and paternal, was assessed for 78 cubs born in 11 lion prides, permitting the assessment of precise genealogical relationships among some 200 lions. The extent of DNA restriction fragment sharing between lions was empirically calibrated with the coefficient of relatedness, r, in two different populations that had distinct demographic histories. The results suggest that reliable estimates of relative genetic diversity, of parentage, and of individual relatedness can be achieved in free-ranging populations, provided the minisatellite family is calibrated in established pedigrees for the species.

Developmental changes in pituitary-gonadal function in free-ranging lions (Panthera leo leo) of the Serengeti Plains and Ngorongoro Crater.

Pituitary-gonadal function was examined in male lions free-ranging in the Serengeti Plains or geographically isolated in the Ngorongoro Crater of Tanzania. Lions were classified by age as adult (6.1-9.8 years), young adult (3.3-4.5 years) or prepubertal (1.4-1.6 years, Serengeti Plains only). Each animal was anaesthetized and then bled at 5-min intervals for 100 min before and 140 min after i.v. administration of saline or GnRH (1 micrograms/kg body weight). Basal serum LH and FSH concentrations were similar (P greater than 0.05) among age classes and between locations. In Serengeti Plains lions, net LH peak concentrations after GnRH were approximately 35% greater (P less than 0.05) in prepubertal than in either adult or young adult animals. GnRH-stimulated LH release was similar (P greater than 0.05) between adult and young adult lions, and these responses were similar (P greater than 0.05) to those measured in Ngorongoro Crater lions. Basal and GnRH-stimulated testosterone secretion was higher (P less than 0.05) in adult than in young adult lions and lowest (P less than 0.05) in prepubertal lions. Age-class differences in testosterone production were related directly to the concentrations of LH receptors in the testis (P less than 0.05). Basal and GnRH-stimulated testosterone secretion and gonadotrophin receptor concentrations within age classes were similar (P greater than 0.05) between lions of the Serengeti Plains and Ngorongoro Crater. Lower motility and higher percentages of structurally abnormal spermatozoa were observed in electroejaculates of young adult compared to adult Serengeti Plains males (P less than 0.05) and were associated with decreased steroidogenic activity. In contrast, there were no age-related differences in ejaculate characteristics of Ngorongoro Crater lions. Seminal quality in the Crater population was poor in adult and young adult animals and was unrelated to alterations in pituitary or testicular function. In summary, only seminal quality in adult male lions was affected by location, whereas age significantly affected both basal and GnRH-stimulated testosterone secretion and seminal quality (Serengeti Plains only) in sexually mature males. The striking seminal/endocrine differences among pride (breeding) males of different ages raises questions about the impact of age on individual reproductive performance in this species.

Sex-biased dispersal and inbreeding avoidance in birds and mammals.

Sex differences in dispersal distance are widespread in birds and mammals, but the predominantly dispersing sex differs consistently between the classes. There has been persistent debate over the relative importance of two factors - intrasexual competition and inbreeding avoidance - in producing sex-biased dispersal, and over the sources of the difference in dispersal patterns between the two classes. Recent studies cast new light on these questions.

Female aggression and male membership in troops of Japanese macaques and olive baboons.

A detailed comparison of Macaca fuscata and Papio anubis reveals that female aggression to males has an effect on male association with females in both species, but only in M. fuscata do females appear to be able to limit the number of males in their troop. It is suggested that this is the reasons why 'solitary' males are commonly reported in M. fuscata, but rare in P. anubis, and may be related ultimately to the different degrees of sexual dimorphism in the two species.