Peter D. Walsh

Catastrophic ape decline in western equatorial Africa

Because rapidly expanding human populations have devastated gorilla (Gorilla gorilla) and common chimpanzee (Pan troglodytes) habitats in East and West Africa, the relatively intact forests of western equatorial Africa have been viewed as the last stronghold of African apes. Gabon and the Republic of Congo alone are thought to hold roughly 80% of the worlds gorillas and most of the common chimpanzees. Here we present survey results conservatively indicating that ape populations in Gabon declined by more than half between 1983 and 2000. The primary cause of the decline in ape numbers during this period was commercial hunting, facilitated by the rapid expansion of mechanized logging. Furthermore, Ebola haemorrhagic fever is currently spreading through ape populations in Gabon and Congo and now rivals hunting as a threat to apes. Gorillas and common chimpanzees should be elevated immediately to ‘critically endangered’ status. Without aggressive investments in law enforcement, protected area management and Ebola prevention, the next decade will see our closest relatives pushed to the brink of extinction.

Ebola Outbreak Killed 5000 Gorillas

Over the past decade, the Zaire strain of Ebola virus (ZEBOV) has repeatedly emerged in Gabon and Congo. Each human outbreak has been accompanied by reports of gorilla and chimpanzee carcasses in neighboring forests, but both the extent of ape mortality and the causal role of ZEBOV have been hotly debated. Here, we present data suggesting that in 2002 and 2003 ZEBOV killed about 5000 gorillas in our study area. The lag between neighboring gorilla groups in mortality onset was close to the ZEBOV disease cycle length, evidence that group-to-group transmission has amplified gorilla die-offs.

Wave-like spread of Ebola Zaire

In the past decade the Zaire strain of Ebola virus (ZEBOV) has emerged repeatedly into human populations in central Africa and caused massive die-offs of gorillas and chimpanzees. We tested the view that emergence events are independent and caused by ZEBOV variants that have been long resident at each locality. Phylogenetic analyses place the earliest known outbreak at Yambuku, Democratic Republic of Congo, very near to the root of the ZEBOV tree, suggesting that viruses causing all other known outbreaks evolved from a Yambuku-like virus after 1976. The tendency for earlier outbreaks to be directly ancestral to later outbreaks suggests that outbreaks are epidemiologically linked and may have occurred at the front of an advancing wave. While the ladder-like phylogenetic structure could also bear the signature of positive selection, our statistical power is too weak to reach a conclusion in this regard. Distances among outbreaks indicate a spread rate of about 50 km per year that remains consistent across spatial scales. Viral evolution is clocklike, and sequences show a high level of small-scale spatial structure. Genetic similarity decays with distance at roughly the same rate at all spatial scales. Our analyses suggest that ZEBOV has recently spread across the region rather than being long persistent at each outbreak locality. Controlling the impact of Ebola on wild apes and human populations may be more feasible than previously recognized.

Molecular epidemiology of simian immunodeficiency virus infection in wild-living gorillas.

ABSTRACT Chimpanzees and gorillas are the only nonhuman primates known to harbor viruses closely related to HIV-1. Phylogenetic analyses showed that gorillas acquired the simian immunodeficiency virus SIVgor from chimpanzees, and viruses from the SIVcpz/SIVgor lineage have been transmitted to humans on at least four occasions, leading to HIV-1 groups M, N, O, and P. To determine the geographic distribution, prevalence, and species association of SIVgor, we conducted a comprehensive molecular epidemiological survey of wild gorillas in Central Africa. Gorilla fecal samples were collected in the range of western lowland gorillas (n = 2,367) and eastern Grauer gorillas (n = 183) and tested for SIVgor antibodies and nucleic acids. SIVgor antibody-positive samples were identified at 2 sites in Cameroon, with no evidence of infection at 19 other sites, including 3 in the range of the Eastern gorillas. In Cameroon, based on DNA and microsatellite analyses of a subset of samples, we estimated the prevalence of SIVgor to be 1.6% (range, 0% to 4.6%), which is significantly lower than the prevalence of SIVcpzPtt in chimpanzees (5.9%; range, 0% to 32%). All newly identified SIVgor strains formed a monophyletic lineage within the SIVcpz radiation, closely related to HIV-1 groups O and P, and clustered according to their field site of origin. At one site, there was evidence for intergroup transmission and a high intragroup prevalence. These isolated hot spots of SIVgor-infected gorilla communities could serve as a source for human infection. The overall low prevalence and sporadic distribution of SIVgor could suggest a decline of SIVgor in wild populations, but it cannot be excluded that SIVgor is still more prevalent in other parts of the geographical range of gorillas.

Recent Common Ancestry of Ebola Zaire Virus Found in a Bat Reservoir

Identifying a natural reservoir for Ebola virus has eluded researchers for decades [1,2]. Recently, Leroy et al. presented the most compelling evidence to date that three species of fruit bats (Hypsignathus monstrosus, Epomops franqueti, and Myonycteris torquata) may constitute a long-missing wildlife reservoir for Ebola virus Zaire (EBOVZ) [3]. These bats, caught near affected villages at the Gabon–Congo border, appear to have been asymptomatically infected and, in seven cases, yielded virus sequences that closely matched those found in the human outbreaks happening about the same time. Leroy et al.s phylogenetic analysis of the partial sequences of the viral polymerase (L) gene derived from humans and bats emphasized the interspecific relationships to related filoviruses. Here, we show that (1) despite their short length (265 bp), these sequences also provide critical information about the intraspecific history of EBOVZ, and (2) based on the genetic data available so far, the association of the virus with fruit bats in the sampled area can only be traced back a few years. Consistent with previous analysis using glycoprotein (GP) gene sequences [4], results for the L gene show that viruses amplified from more recently collected samples appear to be direct descendents of viruses seen during previous outbreaks. This relationship is not only apparent for viruses found in 1976–1995 compared with those found in 2001–2003, but also within the latter group (Figure 1). In essence, this means that all genetic variation seen thus far in EBOVZ, including virus amplified from fruit bats, appears to be the product of mutations that have accumulated within the last 30 years. Finding such strong evidence for temporal structure by chance seems highly unlikely, especially given the concordance with our earlier results from the GP gene [4]. Although the lack of any mutational differences between the sequences Mayinga 1976 and Kikwit 1995 is perplexing in this context, it is most likely a stochastic artifact due to the short length of the sequence considered. Full-length sequences are available for both these isolates, which over the entire genome are 1.2% different. Over 19 years this yields an ad hoc evolutionary rate estimate of 6.2 × 10−4 substitutions per site per year, close to the rate we had previously estimated for the GP gene (~8.0 × 10−4) [4] and to the point estimate for all partial L sequences in the current analysis (1.1 × 10−3; 95% highest posterior density interval: 6.3 × 10−7 to 2.4 × 10−3). Thus, even though the L sequences are rather short, they yield evolutionary rate estimates similar to the longer GP sequences. Figure 1 Maximum Likelihood Tree from Partial L Sequences of Ebola Virus Zaire The temporal structure visible in the L gene genealogy implies that all viruses sampled from both humans and bats between 2001 and 2003 can be traced back to a very recent common ancestor, by which we mean a recent coalescence of genetic lineages, not an ancestral alternative reservoir species. In fact, according to our phylogenetic estimate, the partial L sequence of this genetic ancestor would have looked identical to that sampled from infected humans during outbreaks in late 2001 and early 2002 (Entsiami and Mendemba, Figure 1), suggesting that this ancestor could not be much older. This is in agreement with the previous analysis of the GP gene, which indicated that all viruses sampled from outbreaks since 2001 had a most recent common ancestor in 1999 (confidence region: 1998–2000) [4]. While these findings do not question whether fruit bats may represent a wild reservoir for EBOVZ, they do raise important issues. If the three identified fruit bat hosts were the natural reservoir for EBOVZ, the recent common ancestry of all sequences derived from them so far is surprising because, at least at first sight, it seems to contradict the idea of a long-established association of bat and virus. The most reasonable explanation for this result is that the virus experienced a recent genetic bottleneck. We present three alternative scenarios of what could have caused such a bottleneck. One possibility is that somewhere around 1999, the total number of infected bats within the sampled area became extremely small (likely much less than the peak 23% incidence determined by Leroy et al.). Under such a scenario, the most recent common ancestor could not be traced back further into the past because an extremely small, effective viral population size has caused the descendents of all but one of the previously existing viral lineages to be lost. Since no trapping study on bats was undertaken before 2001, we could not directly address this issue. However, some epidemiological and virological observations may account for this situation. The need to apply the very sensitive nested PCR to detect viral RNA suggests a very low viral load in organs of infected bats. Furthermore, the presence of a high prevalence rate of seropositive bats (16.7%, 4/24) compared with only 3.2% (2/63) that were PCR positive (but seronegative) just three months after the appearance of the first human cases in Mendemba, Gabon, indicates that viral replication within bats may be highly restricted and possibly only taking place prior to the onset of the host immune response. Especially if infections are synchronized, for example, by some environmental trigger, this may lead to periods with an extremely small number of productively infected bats, repeatedly forcing the virus population through a genetic bottleneck. Alternatively, the recent common ancestor could be explained by infected bats introducing the virus into the EBOVZ-affected area of Gabon and Congo around 1999. Previous results for the GP gene actually support this hypothesis by revealing a consistent signature of geographic spread within the spatial, temporal, and genetic data for EBOVZ over the last 30 years [4]. Similar genetic patterns associated with local founder events followed by spatial spread have also been documented from rabies virus in wildlife host populations [5]. Some observed epidemiological changes in sampled bat populations over time may also support this hypothesis. Leroy et al. found that during the first visit to one of their sampling locations, 23% (7/31) of the bats were PCR positive, whereas 0% (0/10) were seropositive. At a second visit five months later, these numbers had changed to 2% (4/184) and 8% (12/160) [3]. Again, no bats were positive by both PCR and serology. Though other factors may also explain these opposing trends, the observed temporal pattern is consistent with an infection wave moving through the sampled population, resulting in a high proportion of infectious individuals at first, followed by an increased proportion of seropositive animals. Given that the three implicated fruit bat species may not be the only reservoir for EBOVZ, as Leroy et al. were already careful to point out [3], another possible explanation for the existence of a common viral ancestor in the recent past is that the virus was introduced to these fruit bats around the same time it affected other wildlife populations and emerged in humans. It is important to note that this scenario does not rule out bats as reservoir species, a hypothesis for which there is additional independent support [6]. Instead, it would imply that the primary reservoir of EBOVZ, whether it involves additional bat species or representatives of other taxonomic groups, has yet to be found. We expect that distinguishing between these possible scenarios will become increasingly easier as more temporal, spatial, and genetic data are generated. Additional viral sequences from infected fruit bats and large-scale serological prevalence in bat populations both within and outside the affected area should give some much needed answers regarding the dynamics of the virus in its wild reservoir. Together with other viral sequences in human cases and vulnerable animal species, and a better understanding of the factors associated with its emergence in human and wildlife populations, these combined approaches will hopefully lead to new and more successful strategies for preventing and controlling outbreaks of EBOVZ in the near future.

Potential for Ebola Transmission between Gorilla and Chimpanzee Social Groups

Over the past decade Ebola hemorrhagic fever has emerged repeatedly in Gabon and Congo, causing numerous human outbreaks and massive die‐offs of gorillas and chimpanzees. Why Ebola has emerged so explosively remains poorly understood. Previous studies have tended to focus on exogenous factors such as habitat disturbance and climate change as drivers of Ebola emergence while downplaying the contribution of transmission between gorilla or chimpanzee social groups. Here we report recent observations on behaviors that pose a risk of transmission among gorilla groups and between gorillas and chimpanzees. These observations support a reassessment of ape‐to‐ape transmission as an amplifier of Ebola outbreaks.

Using Dung to Estimate Gorilla Density: Modeling Dung Production Rate

There is an urgent need for information on western gorilla population sizes and distribution to improve present and plan future conservation actions. Researchers traditionally have estimated gorilla densities on the basis of nest counts despite demonstrated variation in nest production and decay rates. The variation may lead to large biases in estimates of gorilla abundance. We investigated the use of an alternate index of gorilla abundance, via defecation data collected from habituated gorillas at Bai Hokou, Central African Republic. Our sample of 274/370 defecation events/dung piles produced a production rate of ca. 5 dung piles/d: comparable to previous estimates based on much smaller sample sizes. Heuristic models that failed to account for imperfect dung pile detection produced a lower defecation rate estimate than that of a maximum likelihood model that explicitly modeled detection probability. Generalized linear modeling (GLM) showed that dung pile production rate was strongly linked to rainfall, suggesting that failure to correct for seasonal variation in dung pile production rates could lead to substantial biases in gorilla abundance estimates. In our study, failing to distinguish between the number of defecation events and the number of dung piles produced would lead to a ca. 31% overestimate of true gorilla numbers. The use of dung as an index of gorilla abundance shows potential, but more fieldwork and modeling on seasonal variation in dung production rates is required.

Action needed to prevent extinctions caused by disease.

Your News in Brief item ‘Cancer forces Tasmanian devil onto endangered list’ highlights the plight of this carnivorous marsupial (Sarcophilus harrisii), driven towards extinction by devil facial-tumour disease, which is contagious

Monitoring population decline: can transect surveys detect the impact of the Ebola virus on apes?

In 2004 the Ebola virus caused a drastic decline in western gorilla Gorilla gorilla abundance at Lokoue Bai, a clearing in Odzala National Park, Republic of Congo. This decline was detected by observations of gorillas visiting the clearing. We confirm that the sympatric chimpanzee Pan troglodytes population was also affected by the Ebola outbreak, and test whether the decline in the ape population would have been detected with line-transect surveys, the most commonly used wildlife monitoring methodology in Central Africa. We also evaluate the potential of transect surveys for describing the extent and pinpointing the timing of drastic population declines when this information is not known from other evidence. Both nest survey using the marked nest count method and standing stock survey of other signs of ape presence (dung, feeding remains, prints) were able to detect the decline. However, only nests and dung were reliable indices for estimating the magnitude of the decline and accurately pinpointing the timing. It was necessary to pool data across many survey replicates because of small samples sizes. Our results suggest that transects methods are able to detect drastic changes in ape abundance but that large sample sizes are necessary to achieve adequate statistical power. We therefore recommend that those intending to use transect methods as tools for monitoring large forest mammals evaluate in advance how much effort will be necessary to detect meaningful changes in animal abundance.

Origin of the human malaria parasite Plasmodium falciparum in gorillas

Plasmodium falciparum is the most prevalent and lethal of the malaria parasites infecting humans, yet the origin and evolutionary history of this important pathogen remain controversial. Here we develop a single-genome amplification strategy to identify and characterize Plasmodium spp. DNA sequences in faecal samples from wild-living apes. Among nearly 3,000 specimens collected from field sites throughout central Africa, we found Plasmodium infection in chimpanzees (Pan troglodytes) and western gorillas (Gorilla gorilla), but not in eastern gorillas (Gorilla beringei) or bonobos (Pan paniscus). Ape plasmodial infections were highly prevalent, widely distributed and almost always made up of mixed parasite species. Analysis of more than 1,100 mitochondrial, apicoplast and nuclear gene sequences from chimpanzees and gorillas revealed that 99% grouped within one of six host-specific lineages representing distinct Plasmodium species within the subgenus Laverania. One of these from western gorillas comprised parasites that were nearly identical to P. falciparum. In phylogenetic analyses of full-length mitochondrial sequences, human P. falciparum formed a monophyletic lineage within the gorilla parasite radiation. These findings indicate that P. falciparum is of gorilla origin and not of chimpanzee, bonobo or ancient human origin.