Anna Mosser

Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz

African primates are naturally infected with over 40 different simian immunodeficiency viruses (SIVs), two of which have crossed the species barrier and generated human immunodeficiency virus types 1 and 2 (HIV-1 and HIV-2). Unlike the human viruses, however, SIVs do not generally cause acquired immunodeficiency syndrome (AIDS) in their natural hosts. Here we show that SIVcpz, the immediate precursor of HIV-1, is pathogenic in free-ranging chimpanzees. By following 94 members of two habituated chimpanzee communities in Gombe National Park, Tanzania, for over 9 years, we found a 10- to 16-fold higher age-corrected death hazard for SIVcpz-infected (n = 17) compared to uninfected (n = 77) chimpanzees. We also found that SIVcpz-infected females were less likely to give birth and had a higher infant mortality rate than uninfected females. Immunohistochemistry and in situ hybridization of post-mortem spleen and lymph node samples from three infected and two uninfected chimpanzees revealed significant CD4+ T-cell depletion in all infected individuals, with evidence of high viral replication and extensive follicular dendritic cell virus trapping in one of them. One female, who died within 3 years of acquiring SIVcpz, had histopathological findings consistent with end-stage AIDS. These results indicate that SIVcpz, like HIV-1, is associated with progressive CD4+ T-cell loss, lymphatic tissue destruction and premature death. These findings challenge the prevailing view that all natural SIV infections are non-pathogenic and suggest that SIVcpz has a substantial negative impact on the health, reproduction and lifespan of chimpanzees in the wild.

Can parks protect migratory ungulates? The case of the Serengeti wildebeest

The conservation of migratory species can be problematic because of their requirements for large protected areas. We investigated this issue by examining the annual movements of the migratory wildebeest, Connochaetes taurinus, in the 25000 km2 Serengeti-Mara Ecosystem of Tanzania and Kenya. We used Global Positioning System telemetry to track eight wildebeest during 1999–2000 in relation to protected area status in different parts of the ecosystem. The collared wildebeest spent 90% of their time within well-protected core areas. However, two sections of the wildebeest migration route – the Ikoma Open Area and the Mara Group Ranches – currently receive limited protection and are threatened by poaching or agriculture. Comparison of current wildebeest migration routes to those recorded during 1971–73 indicates that the western buffer zones appear to be used more extensively than in the past. This tentative conclusion has important repercussions for management and needs further study. The current development of community-run Wildlife Management Areas as additional buffer zones around the Serengeti represents an important step in the conservation of this UNESCO World Heritage Site. This study demonstrates that detailed knowledge of movement of migratory species is required to plan effective conservation action.

Group formation stabilizes predator-prey dynamics

Theoretical ecology is largely founded on the principle of mass action, in which uncoordinated populations of predators and prey move in a random and well-mixed fashion across a featureless landscape. The conceptual core of this body of theory is the functional response, predicting the rate of prey consumption by individual predators as a function of predator and/or prey densities. This assumption is seriously violated in many ecosystems in which predators and/or prey form social groups. Here we develop a new set of group-dependent functional responses to consider the ecological implications of sociality and apply the model to the Serengeti ecosystem. All of the prey species typically captured by Serengeti lions (Panthera leo) are gregarious, exhibiting nonlinear relationships between prey-group density and population density. The observed patterns of group formation profoundly reduce food intake rates below the levels expected under random mixing, having as strong an impact on intake rates as the seasonal migratory behaviour of the herbivores. A dynamical system model parameterized for the Serengeti ecosystem (using wildebeest (Connochaetes taurinus) as a well-studied example) shows that grouping strongly stabilizes interactions between lions and wildebeest. Our results suggest that social groups rather than individuals are the basic building blocks around which predator–prey interactions should be modelled and that group formation may provide the underlying stability of many ecosystems.

Group territoriality and the benefits of sociality in the African lion, Panthera leo

We analysed 38 years of data on 46 lion prides in the Serengeti National Park, Tanzania, and found that territorial competition directly affected critical components of female fitness and that larger prides gained and maintained access to the highest-quality habitat. Neighbours had a significant negative effect on female reproductive success and survival, and larger prides were significantly more likely to maintain control of disputed areas and to improve the quality of their territories. Adult females were significantly less likely to be alone when a pride had more neighbours, suggesting sensitivity to risk of encounter. In most cases, the effects of intergroup territorial competition were associated only with prides that had not recently split (i.e. that were not closely related). Overall, males were more important in group-territorial competition than expected, and female mortality and wounding rates were significantly associated with male neighbours, suggesting that males may use lethal aggression to tip the balance of power in favour of their prides. Within the Felidae, only lions are consistently gregarious, and our research illustrates that numerical advantage in territorial competition is a primary benefit of group living in lions and may have been important in the evolution of lion sociality.

Impact of Simian Immunodeficiency Virus Infection on Chimpanzee Population Dynamics

Like human immunodeficiency virus type 1 (HIV-1), simian immunodeficiency virus of chimpanzees (SIVcpz) can cause CD4+ T cell loss and premature death. Here, we used molecular surveillance tools and mathematical modeling to estimate the impact of SIVcpz infection on chimpanzee population dynamics. Habituated (Mitumba and Kasekela) and non-habituated (Kalande) chimpanzees were studied in Gombe National Park, Tanzania. Ape population sizes were determined from demographic records (Mitumba and Kasekela) or individual sightings and genotyping (Kalande), while SIVcpz prevalence rates were monitored using non-invasive methods. Between 2002–2009, the Mitumba and Kasekela communities experienced mean annual growth rates of 1.9% and 2.4%, respectively, while Kalande chimpanzees suffered a significant decline, with a mean growth rate of −6.5% to −7.4%, depending on population estimates. A rapid decline in Kalande was first noted in the 1990s and originally attributed to poaching and reduced food sources. However, between 2002–2009, we found a mean SIVcpz prevalence in Kalande of 46.1%, which was almost four times higher than the prevalence in Mitumba (12.7%) and Kasekela (12.1%). To explore whether SIVcpz contributed to the Kalande decline, we used empirically determined SIVcpz transmission probabilities as well as chimpanzee mortality, mating and migration data to model the effect of viral pathogenicity on chimpanzee population growth. Deterministic calculations indicated that a prevalence of greater than 3.4% would result in negative growth and eventual population extinction, even using conservative mortality estimates. However, stochastic models revealed that in representative populations, SIVcpz, and not its host species, frequently went extinct. High SIVcpz transmission probability and excess mortality reduced population persistence, while intercommunity migration often rescued infected communities, even when immigrating females had a chance of being SIVcpz infected. Together, these results suggest that the decline of the Kalande community was caused, at least in part, by high levels of SIVcpz infection. However, population extinction is not an inevitable consequence of SIVcpz infection, but depends on additional variables, such as migration, that promote survival. These findings are consistent with the uneven distribution of SIVcpz throughout central Africa and explain how chimpanzees in Gombe and elsewhere can be at equipoise with this pathogen.

Environmental and individual drivers of animal movement patterns across a wide geographical gradient

Within the rapidly developing field of movement ecology, much attention has been given to studying the movement of individuals within a subset of their populations occupied range. Our understanding of the effects of landscape heterogeneity on animal movement is still fairly limited as it requires studying the movement of multiple individuals across a variety of environmental conditions. Gaining deeper understanding of the environmental drivers of movement is a crucial component of predictive models of population spread and habitat selection and may help inform management and conservation. In Ontario, woodland caribou (Rangifer tarandus caribou) occur along a wide geographical gradient ranging from the boreal forest to the Hudson Bay floodplains. We used high-resolution GPS data, collected from 114 individuals across a 450000 km(2) area in northern Ontario, to link movement behaviour to underlying local environmental variables associated with habitat permeability, predation risk and forage availability. We show that a great deal of observed variability in movement patterns across space and time can be attributed to local environmental conditions, with residual individual differences that may reflect spatial population structure. We discuss our results in the context of current knowledge of movement and caribou ecology and highlight potential applications of our approach to the study of wide-ranging animals.

Optimal group size, dispersal decisions and postdispersal relationships in female African lions

We used 40 years of long-term data to test whether dispersal decisions of female African lions, Panthera leo, are sensitive to variations in pride size, interpride competition and the quality of their natal territory. Per capita reproductive success reached a maximum at 3–6 females on the open grass plains of the Serengeti and at 3–11 females in the woodlands. Approximately 50% of female cohorts dispersed when potential pride size exceeded the habitat-specific optimum, whereas only 9% of cohorts dispersed at smaller pride sizes. Cohorts of one to two females rarely dispersed, especially in high-density habitats. Thus, pride size typically remained within the range that maximized individual reproductive success. In the high-density woodland habitat, females were less likely to disperse from prides that were surrounded by large numbers of unrelated females, as would be predicted on the basis of habitat saturation. However, the number of unrelated neighbours did not affect dispersal decisions of females living in the sparsely occupied plains habitat. After pride fission, daughters settled closer to their mothers in areas where there were greater numbers of unrelated female neighbours, but territories were just as exclusive as between unrelated neighbouring prides. Maternal prides in high-quality areas shared a greater percentage of their territory with descendant prides, but this tolerance diminished as relatedness declined through time.

Space‐use behaviour of woodland caribou based on a cognitive movement model

Movement patterns offer a rich source of information on animal behaviour and the ecological significance of landscape attributes. This is especially useful for species occupying remote landscapes where direct behavioural observations are limited. In this study, we fit a mechanistic model of animal cognition and movement to GPS positional data of woodland caribou (Rangifer tarandus caribou; Gmelin 1788) collected over a wide range of ecological conditions. The model explicitly tracks individual animal informational state over space and time, with resulting parameter estimates that have direct cognitive and ecological meaning. Three biotic landscape attributes were hypothesized to motivate caribou movement: forage abundance (dietary digestible biomass), wolf (Canis lupus; Linnaeus, 1758) density and moose (Alces alces; Linnaeus, 1758) habitat. Wolves are the main predator of caribou in this system and moose are their primary prey. Resulting parameter estimates clearly indicated that forage abundance is an important driver of caribou movement patterns, with predator and moose avoidance often having a strong effect, but not for all individuals. From the cognitive perspective, our results support the notion that caribou rely on limited sensory inputs from their surroundings, as well as on long-term spatial memory, to make informed movement decisions. Our study demonstrates how sensory, memory and motion capacities may interact with ecological fitness covariates to influence movement decisions by free-ranging animals.

Wolves adapt territory size, not pack size to local habitat quality

1. Although local variation in territorial predator density is often correlated with habitat quality, the causal mechanism underlying this frequently observed association is poorly understood and could stem from facultative adjustment in either group size or territory size. 2. To test between these alternative hypotheses, we used a novel statistical framework to construct a winter population-level utilization distribution for wolves (Canis lupus) in northern Ontario, which we then linked to a suite of environmental variables to determine factors influencing wolf space use. Next, we compared habitat quality metrics emerging from this analysis as well as an independent measure of prey abundance, with pack size and territory size to investigate which hypothesis was most supported by the data. 3. We show that wolf space use patterns were concentrated near deciduous, mixed deciduous/coniferous and disturbed forest stands favoured by moose (Alces alces), the predominant prey species in the diet of wolves in northern Ontario, and in proximity to linear corridors, including shorelines and road networks remaining from commercial forestry activities. 4. We then demonstrate that landscape metrics of wolf habitat quality - projected wolf use, probability of moose occupancy and proportion of preferred land cover classes - were inversely related to territory size but unrelated to pack size. 5. These results suggest that wolves in boreal ecosystems alter territory size, but not pack size, in response to local variation in habitat quality. This could be an adaptive strategy to balance trade-offs between territorial defence costs and energetic gains due to resource acquisition. That pack size was not responsive to habitat quality suggests that variation in group size is influenced by other factors such as intraspecific competition between wolf packs.

Asynchronous food-web pathways could buffer the response of Serengeti predators to El Niño Southern Oscillation

Understanding how entire ecosystems maintain stability in the face of climatic and human disturbance is one of the most fundamental challenges in ecology. Theory suggests that a crucial factor determining the degree of ecosystem stability is simply the degree of synchrony with which different species in ecological food webs respond to environmental stochasticity. Ecosystems in which all food-web pathways are affected similarly by external disturbance should amplify variability in top carnivore abundance over time due to population interactions, whereas ecosystems in which a large fraction of pathways are nonresponsive or even inversely responsive to external disturbance will have more constant levels of abundance at upper trophic levels. To test the mechanism underlying this hypothesis, we used over half a century of demographic data for multiple species in the Serengeti (Tanzania) ecosystem to measure the degree of synchrony to variation imposed by an external environmental driver, the El Niño Southern Oscillation (ENSO). ENSO effects were mediated largely via changes in dry-season vs. wet-season rainfall and consequent changes in vegetation availability, propagating via bottom-up effects to higher levels of the Serengeti food web to influence herbivores, predators and parasites. Some species in the Serengeti food web responded to the influence of ENSO in opposite ways, whereas other species were insensitive to variation in ENSO. Although far from conclusive, our results suggest that a diffuse mixture of herbivore responses could help buffer top carnivores, such as Serengeti lions, from variability in climate. Future global climate changes that favor some pathways over others, however, could alter the effectiveness of such processes in the future.