Impact of Simian Immunodeficiency Virus Infection on Chimpanzee Population Dynamics

Abstract

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.

High Prevalence of Simian Immunodeficiency Virus Infection in a Community of Savanna Chimpanzees

“…However, SIVcpz is also an important pathogen in its own right, since it causes significant morbidity and mortality in its chimpanzee host (6,15,37). Recent natural history studies in Gombe National Park in western Tanzania showed that infected chimpanzees have a 10-to 16-fold increased risk of death compared to uninfected chimpanzees (15).…”

“…To screen wildliving populations for SIVcpz infection, our laboratory has developed diagnostic methods that detect virus-specific antibodies and nucleic acids in fecal and urine samples with high sensitivity and specificity (16,41,42). These noninvasive methods, combined with genotyping approaches for species confirmation and individual identification (5,15,37,47,50), have enabled analyses of wild-living chimpanzee populations throughout central Africa. Molecular epidemiological studies have shown that SIVcpz is endemic in both central and eastern chimpanzees, with virus-positive communities identified throughout their habitats (43,44).…”

“…Molecular epidemiological studies have shown that SIVcpz is endemic in both central and eastern chimpanzees, with virus-positive communities identified throughout their habitats (43,44). Surprisingly, however, the distribution of SIVcpz in wild-living populations is uneven, with high prevalence rates (30% to 50%) in some communities and rare or absent infection in others (15,16,19,37,41,49). While the reasons for this sporadic distribution remain to be determined, it is clear that the infection status of any one community cannot be predicted but has to be determined empirically.…”

Origin of the HIV-1 group O epidemic in western lowland gorillas

“…Thus, SIVgor could have once been present across a larger geographic area but may have led to the extinction of certain gorilla populations. SIVcpz has been shown to have a substantive negative impact on the health, reproduction, and survival of chimpanzees in the wild, and has caused the decline of at least one chimpanzee community (25,27). Thus, studies on additional infected and uninfected gorilla populations are required to determine the impact of SIVgor on gorilla survival (17).…”

Assessment of Chimpanzee Nest Detectability in Drone-Acquired Images

“…Several studies have documented the impact of habitat loss [2][3][4], poaching [5][6][7] and infectious disease [8,9] on wild populations. In Tanzania, 75% woodland vegetation than the closed riverine forest.…”