Emily Otali

Eviction and dispersal in co-operatively breeding banded mongooses (Mungos mungo)

The mode by which individuals disperse, and the cost of dispersal, are of great importance in attempts to understand variation in reproductive skew in animal societies. In this paper we report detailed information on dispersal and pack formation in banded mongooses Mungos mungo. Six pack fission events were recorded among 11 packs over 22 months. Pack fission occurred under two distinct circumstances. First, groups of individuals were evicted from their natal group as a result of intense aggression from other group members. A small fraction of group members was responsible for most of the aggression. Both sexes helped to attack and evict individuals from the group, and both males and females were driven out of their natal groups en masse. The second mode of pack fission occurred when groups of same-sex individuals left their natal group voluntarily to join dispersing individuals of the opposite sex, thereby forming new packs. Dispersing groups were more frequently involved in fights with rival packs of mongooses compared to established groups, and in one instance these fights seemed to be responsible for severe injury and increased mortality among members of a dispersing group. The observations of eviction provide one line of evidence that the presence of subordinates is sometimes detrimental to dominants, contrary to the assumptions of concession models of reproductive skew.

THE EFFECTS OF REFUSE FEEDING ON BODY CONDITION, REPRODUCTION, AND SURVIVAL OF BANDED MONGOOSES

Abstract We investigated the effect of refuse feeding on body condition, reproductive success, and survival in banded mongooses (Mungos mungo). Data were collected from 231 mongooses in 3 refuse-feeding groups and 311 mongooses in 8 non–refuse-feeding groups within Queen Elizabeth National Park, Uganda. Refuse-feeding adults were heavier and in better physical condition than non–refuse-feeding adults. Refuse-feeding females carried more fetuses than non–refuse-feeding females, but no difference was found in conception rate, number of emerging young, or number of independent young per female between refuse-feeding and non–refuse-feeding females. Male young in refuse-feeding groups had higher mortality than all other young. These findings show that for this social carnivore, access to garbage dumps had significant but contrasting effects on components of fitness but no overall effect on evolutionary fitness.

The Foraging Costs of Mating Effort in Male Chimpanzees (Pan troglodytes schweinfurthii)

Costs of mating effort can affect the reproductive strategies and lifetime fitness of male primates, but interspecific and interindividual variation in the magnitude and distribution of costs is poorly understood. Male costs have primarily been recognized in seasonally breeding species that experience concentrated periods of mating competition. Here, we examine foraging costs associated with male mating effort in chimpanzees (Pan troglodytes schweinfurthii), a polygynandrous species, in which mating opportunities occur intermittently throughout the year. To quantify male feeding, aggression, and mating, we conducted focal follows on 12 males in a wild community (Kanyawara, Kibale National Park, Uganda) for 11 mo. Males fed less on days when high-value mating opportunities (estrous parous females) were available than on days without any mating opportunities. Reductions in feeding time were related to increased rates of aggression and copulation, indicating that the proximate cause of changes in male foraging was mating effort. Surprisingly, however, there was no relationship between dominance rank and the extent to which feeding time was reduced. High costs of mating effort may reduce the degree of reproductive skew and limit the use of possessive tactics in chimpanzees. We suggest that male bonding in chimpanzees may be favored not only for its benefits but because intragroup competition is so costly. Our results complement the available data on mammals, and primates in particular, by showing that mating effort can have measurable foraging costs even in species, in which breeding is aseasonal and only moderately skewed.

Faster reproductive rates trade off against offspring growth in wild chimpanzees.

Significance Life history theory predicts that organisms can increase their fitness either by producing many offspring or by producing fewer, high-quality offspring. This “quality–quantity” trade-off is expected to be particularly salient for species such as humans that have extended offspring investment, but it may be obscured by cultural mechanisms, such as provisioning. We found strong evidence for quality–quantity trade-offs in chimpanzees, a closely related species with extensive maternal investment. Immature wild chimpanzees that were relatively young when their next sibling was born remained smaller throughout their juvenile years. Chimpanzee mothers with more resources appear to invest in faster reproduction rather than in more robust offspring. This strategy may have set the stage for rapid reproduction and postweaning investment in the human species. Life history theory predicts a trade-off between offspring quality and quantity. Among large-bodied mammals, prolonged lactation and infant dependence suggest particularly strong potential for a quality–quantity trade-off to exist. Humans are one of the only such species to have been examined, providing mixed evidence under a peculiar set of circumstances, including extensive nutritional provisioning by nonmothers and extrasomatic wealth transmission. Here, we examine trade-offs between reproductive rate and one aspect of offspring quality (body size) in wild chimpanzees (Pan troglodytes schweinfurthii), a species with long periods of infant dependence and little direct provisioning. Juvenile lean body mass, estimated using urinary creatinine excretion, was positively associated with the interval to the next sibling’s birth. These effects persisted into adolescence and were not moderated by maternal identity. Maternal depletion could not explain poor offspring growth, as older mothers had larger offspring, and low maternal energy balance during lactation predicted larger, not smaller, juvenile size. Instead, our data suggest that offspring growth suffers when mothers wean early to invest in new reproductive efforts. These findings indicate that chimpanzee mothers with the resources to do so prioritize production of new offspring over prolonged investment in current offspring.

Coincident Tick Infestations in the Nostrils of Wild Chimpanzees and a Human in Uganda

Ticks in the nostrils of humans visiting equatorial African forests have been reported sporadically for decades, but their taxonomy and natural history have remained obscure. We report human infestation with a nostril tick in Kibale National Park, Uganda, coincident with infestation of chimpanzees in the same location with nostril ticks, as shown by high-resolution digital photography. The human-derived nostril tick was identified morphologically and genetically as a nymph of the genus Amblyomma, but the mitochondrial 12S ribosomal RNA or the nuclear intergenic transcribed spacer 2 DNA sequences of the specimen were not represented in GenBank. These ticks may represent a previously uncharacterized species that is adapted to infesting chimpanzee nostrils as a defense against grooming. Ticks that feed upon apes and humans may facilitate cross-species transmission of pathogens, and the risk of exposure is likely elevated for persons who frequent ape habitats.

Lethal Respiratory Disease Associated with Human Rhinovirus C in Wild Chimpanzees, Uganda, 2013

We describe a lethal respiratory outbreak among wild chimpanzees in Uganda in 2013 for which molecular and epidemiologic analyses implicate human rhinovirus C as the cause. Postmortem samples from an infant chimpanzee yielded near-complete genome sequences throughout the respiratory tract; other pathogens were absent. Epidemiologic modeling estimated the basic reproductive number (R0) for the epidemic as 1.83, consistent with the common cold in humans. Genotyping of 41 chimpanzees and examination of 24 published chimpanzee genomes from subspecies across Africa showed universal homozygosity for the cadherin-related family member 3 CDHR3-Y529 allele, which increases risk for rhinovirus C infection and asthma in human children. These results indicate that chimpanzees exhibit a species-wide genetic susceptibility to rhinovirus C and that this virus, heretofore considered a uniquely human pathogen, can cross primate species barriers and threatens wild apes. We advocate engineering interventions and prevention strategies for rhinovirus infections for both humans and wild apes.

Predation by female chimpanzees: Toward an understanding of sex differences in meat acquisition in the last common ancestor of Pan and Homo

Among modern foraging societies, men hunt more than women, who mostly target relatively low-quality, reliable resources (i.e., plants). This difference has long been assumed to reflect human female reproductive constraints, particularly caring for and provisioning mates and offspring. Long-term studies of chimpanzees (Pan troglodytes) enable tests of hypotheses about the possible origins of human sex differences in hunting, prior to pair-bonding and regular provisioning. We studied two eastern chimpanzee communities (Kasekela, Mitumba) in Gombe, Tanzania and one (Kanyawara) in Kibale, Uganda. Relative to males, females had low hunting rates in all three communities, even where they encountered red colobus monkeys (the primary prey of chimpanzees) as often as males did. There was no evidence that clinging offspring hampered female hunting. Instead, consistent with the hypothesis that females should be more risk-averse than males, females at all three sites specialized in low-cost prey (terrestrial/sedentary prey at Gombe; black and white colobus monkeys at Kanyawara). Female dominance rank was positively correlated with red colobus hunting probability only at Kasekela, suggesting that those in good physical condition were less sensitive to the costs of possible failure. Finally, the potential for carcass appropriation by males deterred females at Kasekela (but not Kanyawara or Mitumba) from hunting in parties containing many adult males. Although chimpanzees are not direct analogs of the last common ancestor (LCA) of Pan and Homo, these results suggest that before the emergence of social obligations regarding sharing and provisioning, constraints on hunting by LCA females did not necessarily stem from maternal care. Instead, they suggest that a risk-averse foraging strategy and the potential for losing prey to males limited female predation on vertebrates. Sex differences in hunting behavior would likely have preceded the evolution of the sexual division of labor among modern humans.

How do human activities influence the status and distribution of terrestrial mammals in forest reserves

Tropical forests support a rich biodiversity of terrestrial mammals, yet our knowledge of the conservation of forest reserves is lacking. We investigate the relationship between human activities and the abundance of medium-sized terrestrial mammals within 4 forest reserves in Uganda. These reserves allow firewood collection, timber cutting, gardening, and pole cutting. Illegal hunting also takes place. We found a general decline in terrestrial mammal signs in the reserves compared to the better protected adjacent Kibale National Park. Signs of aardvarks, bushbucks, bush pigs, duikers (blue and red), giant pangolin, giant forest hogs, porcupines, and jackals are still present in some of our reserves.

Risk factors for respiratory illness in a community of wild chimpanzees (Pan troglodytes schweinfurthii)

Respiratory illnesses have caused significant mortality in African great ape populations. While much effort has been given to identifying the responsible pathogens, little is known about the factors that influence disease transmission or individual susceptibility. In the Kanyawara community of wild chimpanzees, respiratory illness has been the leading cause of mortality over 31 years, contributing to 27% of deaths. Deaths were common in all age groups except juveniles. Over 22 years of health observations, respiratory signs were rare among infants and most common among older adults of both sexes. Respiratory signs were also common among males during the transition to adulthood (ages 10–20 years), particularly among those of low rank. Respiratory signs peaked conspicuously in March, a pattern that we could not explain after modelling climatic factors, group sizes, diet or exposure to humans. Furthermore, rates of respiratory illness in the chimpanzees did not track seasonal rates of illness in the nearby village. Our data indicate that the epidemiology of chimpanzee respiratory illness warrants more investigation but clearly differs in important ways from humans. Findings on individual susceptibility patterns suggest that respiratory signs are a robust indicator for investigating immunocompetence in wild chimpanzees.

Remembering Jerry Lwanga: A Perspective from His Colleagues

Tony L. Goldberg · Samuel Angedakin · Gilbert M. Isabirye Basuta · Michelle Brown · Thomas M. Butynski · Colin A. Chapman · Lauren Chapman · Sholly Gunter · Innocent Kato · Jean-Michel Krief · Sabrina Krief · Joanna E. Lambert · Kevin E. Langergraber · John C. Mitani · Martin N. Muller · Sherry V. Nelson · Patrick Omeja · Emily Otali · Kevin B. Potts · Elizabeth A. Ross · Jessica M. Rothman · Carolyn Rowney · Eric Sande · Thomas T. Struhsaker · Dennis Twinomugisha · David P. Watts · Geoffrey Weny · Richard W. Wrangham