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1.  Lack of Evidence of Simian Immunodeficiency Virus Infection Among Nonhuman Primates in Taï National Park, Côte d’Ivoire: Limitations of Noninvasive Methods and SIV Diagnostic Tools for Studies of Primate Retroviruses 
It is now well established that the human immunodeficiency viruses, HIV-1 and HIV-2, are the results of cross-species transmissions of simian immunodeficiency viruses (SIV) naturally infecting nonhuman primates in sub-Saharan Africa. SIVs are found in many African primates, and humans continue to be exposed to these viruses by hunting and handling primate bushmeat. Sooty mangabeys (Cercocebus atys) and western red colobus (Piliocolobus badius badius) are infected with SIV at a high rate in the Taï Forest, Côte d’Ivoire. We investigated the SIV infection and prevalence in 6 other monkey species living in the Taï Forest using noninvasive methods. We collected 127 fecal samples from 2 colobus species (Colobus polykomos and Procolobus verus) and 4 guenon species (C. diana, C. campbelli, C. petaurista, and C. nictitans). We tested these samples for HIV cross-reactive antibodies and performed reverse transcriptase-polymerase chain reactions (RT-PCR) targeting the gag, pol, and env regions of the SIV genome. We screened 16 human microsatellites for use in individual discrimination and identified 4–6 informative markers per species. Serological analysis of 112 samples yielded negative (n=86) or uninterpretable (n=26) results. PCR analysis on 74 samples confirmed the negative results. These results may reflect either the limited number of individuals sampled or a low prevalence of infection. Further research is needed to improve the sensitivity of noninvasive methods for SIV detection.
doi:10.1007/s10764-010-9466-7
PMCID: PMC3742091  PMID: 23950618
Microsatellites; Nonhuman primates; Noninvasive sampling; Serologic assays; SIV
2.  High Prevalence, Coinfection Rate, and Genetic Diversity of Retroviruses in Wild Red Colobus Monkeys (Piliocolobus badius badius) in Taï National Park, Côte d'Ivoire▿  
Journal of Virology  2010;84(15):7427-7436.
Simian retroviruses are precursors of all human retroviral pathogens. However, little is known about the prevalence and coinfection rates or the genetic diversity of major retroviruses—simian immunodeficiency virus (SIV), simian T-cell lymphotropic virus type 1 (STLV-1), and simian foamy virus (SFV)—in wild populations of nonhuman primates. Such information would contribute to the understanding of the natural history of retroviruses in various host species. Here, we estimate these parameters for wild West African red colobus monkeys (Piliocolobus badius badius) in the Taï National Park, Côte d'Ivoire. We collected samples from a total of 54 red colobus monkeys; samples consisted of blood and/or internal organs from 22 monkeys and additionally muscle and other tissue samples from another 32 monkeys. PCR analyses revealed a high prevalence of SIV, STLV-1, and SFV in this population, with rates of 82%, 50%, and 86%, respectively. Forty-five percent of the monkeys were coinfected with all three viruses while another 32% were coinfected with SIV in combination with either STLV or SFV. As expected, phylogenetic analyses showed a host-specific pattern for SIV and SFV strains. In contrast, STLV-1 strains appeared to be distributed in genetically distinct and distant clades, which are unique to the Taï forest and include strains previously described from wild chimpanzees in the same area. The high prevalence of all three retroviral infections in P. b. badius represents a source of infection to chimpanzees and possibly to humans, who hunt them.
doi:10.1128/JVI.00697-10
PMCID: PMC2897606  PMID: 20484508
3.  The formation of red colobus-diana monkey associations under predation pressure from chimpanzees. 
It is generally assumed that most primates live in monospecific or polyspecific groups because group living provides protection against predation, but hard evidence is scarce. We tested the antipredation hypothesis with observational and experimental data on mixed-species groups of red colobus (Procolobus badius) and diana monkeys (Cercopithecus diana) in the Taï National Park, Ivory Coast. Red colobus, but not diana monkeys, are frequently killed by cooperatively hunting chimpanzees. Association rates peaked during the chimpanzees' hunting season, as a result of changes in the behaviour of the red colobus. In addition, playbacks of recordings of chimpanzee sounds induced the formation of new associations and extended the duration of existing associations. No such effects were observed in reaction to control experiments and playbacks of leopard recordings.
PMCID: PMC1688237  PMID: 9061972
4.  Forest Elephant Crisis in the Congo Basin  
PLoS Biology  2007;5(4):e111.
Debate over repealing the ivory trade ban dominates conferences of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES). Resolving this controversy requires accurate estimates of elephant population trends and rates of illegal killing. Most African savannah elephant populations are well known; however, the status of forest elephants, perhaps a distinct species, in the vast Congo Basin is unclear. We assessed population status and incidence of poaching from line-transect and reconnaissance surveys conducted on foot in sites throughout the Congo Basin. Results indicate that the abundance and range of forest elephants are threatened from poaching that is most intense close to roads. The probability of elephant presence increased with distance to roads, whereas that of human signs declined. At all distances from roads, the probability of elephant occurrence was always higher inside, compared to outside, protected areas, whereas that of humans was always lower. Inside protected areas, forest elephant density was correlated with the size of remote forest core, but not with size of protected area. Forest elephants must be prioritised in elephant management planning at the continental scale.
Author Summary
Forest elephants, perhaps a distinct species of African elephant, occur in the forests of West and Central Africa. Compared to the more familiar savannah elephant of Eastern and Southern Africa, forest elephant biology and their conservation status are poorly known. To provide robust scientific data on the status and distribution of forest elephants to inform and guide conservation efforts, we conducted surveys on foot of forest elephant abundance and of illegal killing of elephants in important conservation sites throughout Central Africa. We covered a combined distance of over 8,000 km on reconnaissance walks, and we systematically surveyed a total area of some 60,000 km2 under the auspices of the Monitoring of the Illegal Killing of Elephants (MIKE) programme. Our results indicate that forest elephant numbers and range are severely threatened by hunting for ivory. Elephant abundance increased with increasing distance from the nearest road, and poaching pressure was most concentrated near roads. We found that protected areas have a positive impact on elephant abundance, probably because management interventions reduced poaching rates inside protected areas compared to non-protected forest. Law enforcement to bring the illegal ivory trade under control, and effective management and protection of large and remote national parks will be critical if forest elephants are to be successfully conserved.
A systematic survey of 68,000 km2 throughout Central Africa reveals that the forest elephant--distinct from the savannah elephant--is severely threatened by poaching, despite a near universal ban of trade in ivory.
doi:10.1371/journal.pbio.0050111
PMCID: PMC1845159  PMID: 17407383
5.  A Population Accounting Approach to Assess Tourism Contributions to Conservation of IUCN-Redlisted Mammal Species 
PLoS ONE  2012;7(9):e44134.
Over 1,000 mammal species are red-listed by IUCN, as Critically Endangered, Endangered or Vulnerable. Conservation of many threatened mammal species, even inside protected areas, depends on costly active day-to-day defence against poaching, bushmeat hunting, invasive species and habitat encroachment. Many parks agencies worldwide now rely heavily on tourism for routine operational funding: >50% in some cases. This puts rare mammals at a new risk, from downturns in tourism driven by external socioeconomic factors. Using the survival of individual animals as a metric or currency of successful conservation, we calculate here what proportions of remaining populations of IUCN-redlisted mammal species are currently supported by funds from tourism. This proportion is ≥5% for over half of the species where relevant data exist, ≥15% for one fifth, and up to 66% in a few cases. Many of these species, especially the most endangered, survive only in one single remaining subpopulation. These proportions are not correlated either with global population sizes or recognition as wildlife tourism icons. Most of the more heavily tourism-dependent species, however, are medium sized (>7.5 kg) or larger. Historically, biological concern over the growth of tourism in protected areas has centered on direct disturbance to wildlife. These results show that conservation of threatened mammal species has become reliant on revenue from tourism to a previously unsuspected degree. On the one hand, this provides new opportunities for conservation funding; but on the other, dependence on such an uncertain source of funding is a new, large and growing threat to red-listed species.
doi:10.1371/journal.pone.0044134
PMCID: PMC3440393  PMID: 22984467
6.  The Price of Play: Self-Organized Infant Mortality Cycles in Chimpanzees 
PLoS ONE  2008;3(6):e2440.
Chimpanzees have been used extensively as a model system for laboratory research on infectious diseases. Ironically, we know next to nothing about disease dynamics in wild chimpanzee populations. Here, we analyze long-term demographic and behavioral data from two habituated chimpanzee communities in Taï National Park, Côte d'Ivoire, where previous work has shown respiratory pathogens to be an important source of infant mortality. In this paper we trace the effect of social connectivity on infant mortality dynamics. We focus on social play which, as the primary context of contact between young chimpanzees, may serve as a key venue for pathogen transmission. Infant abundance and mortality rates at Taï cycled regularly and in a way that was not well explained in terms of environmental forcing. Rather, infant mortality cycles appeared to self-organize in response to the ontogeny of social play. Each cycle started when the death of multiple infants in an outbreak synchronized the reproductive cycles of their mothers. A pulse of births predictably arrived about twelve months later, with social connectivity increasing over the following two years as the large birth cohort approached the peak of social play. The high social connectivity at this play peak then appeared to facilitate further outbreaks. Our results provide the first evidence that social play has a strong role in determining chimpanzee disease transmission risk and the first record of chimpanzee disease cycles similar to those seen in human children. They also lend more support to the view that infectious diseases are a major threat to the survival of remaining chimpanzee populations.
doi:10.1371/journal.pone.0002440
PMCID: PMC2426927  PMID: 18560519
7.  Shoot, shovel and shut up: cryptic poaching slows restoration of a large carnivore in Europe 
Poaching is a widespread and well-appreciated problem for the conservation of many threatened species. Because poaching is illegal, there is strong incentive for poachers to conceal their activities, and consequently, little data on the effects of poaching on population dynamics are available. Quantifying poaching mortality should be a required knowledge when developing conservation plans for endangered species but is hampered by methodological challenges. We show that rigorous estimates of the effects of poaching relative to other sources of mortality can be obtained with a hierarchical state–space model combined with multiple sources of data. Using the Scandinavian wolf (Canis lupus) population as an illustrative example, we show that poaching accounted for approximately half of total mortality and more than two-thirds of total poaching remained undetected by conventional methods, a source of mortality we term as ‘cryptic poaching’. Our simulations suggest that without poaching during the past decade, the population would have been almost four times as large in 2009. Such a severe impact of poaching on population recovery may be widespread among large carnivores. We believe that conservation strategies for large carnivores considering only observed data may not be adequate and should be revised by including and quantifying cryptic poaching.
doi:10.1098/rspb.2011.1275
PMCID: PMC3259920  PMID: 21849323
state–space models; poaching; wolf; Canis lupus; conservation
8.  The Effect of Climate Fluctuation on Chimpanzee Birth Sex Ratio 
PLoS ONE  2012;7(4):e35610.
Climate and weather conditions, such as the North Atlantic Oscillation, precipitation and temperature influence the birth sex ratio (BSR) of various higher latitude species, including deer, elephant seals or northern human populations. Although, tropical regions show only little variation in temperature, climate and weather conditions can fluctuate with consequences for phenology and food resource availability. Here, we evaluate, whether the BSR of chimpanzees, inhabiting African tropical forests, is affected by climate fluctuations as well. Additionally, we evaluate, if variation in consumption of a key food resource with high nutritional value, Coula edulis nuts, is linked to both climate fluctuations and variation in BSR. We use long-term data from two study groups located in Taï National Park, Côte d'Ivoire to assess the influence of local weather conditions and the global climate driver El Niño Southern Oscillation (ENSO) on offspring sex. Côte d'Ivoire has experienced considerable climate variation over the last decades, with increasing temperature and declining precipitation. For both groups we find very similar time windows around the month of conception, in which offspring sex is well predicted by ENSO, with more males following low ENSO values, corresponding to periods of high rainfall. Furthermore, we find that the time spent cracking and feeding on Coula nuts is strongly influenced by climate conditions. Although, some of our analysis suggest that a higher proportion of males is born after periods with higher nut consumption frequency, we cannot conclude decisively at this point that nut consumption may influence shifts in BSR. All results combined suggest that also chimpanzees may experience climate related shifts in offspring sex ratios as response to climate fluctuation.
doi:10.1371/journal.pone.0035610
PMCID: PMC3338517  PMID: 22563387
9.  Full-Length Genome Characterization of a Novel Simian Immunodeficiency Virus Lineage (SIVolc) from Olive Colobus (Procolobus verus) and New SIVwrcPbb Strains from Western Red Colobus (Piliocolobus badius badius) from the Taï Forest in Ivory Coast▿  
Journal of Virology  2008;83(1):428-439.
Simian immunodeficiency viruses (SIVs) are found in an extensive number of African primates and humans continue to be exposed to these viruses by hunting and handling of primate bushmeat. Full-length genome sequences were obtained from SIVs derived from two Colobinae species inhabiting the Taï forest, Ivory Coast, each belonging to a different genus: SIVwrc from western red colobus (Piliocolobus badius badius) (SIVwrcPbb-98CI04 and SIVwrcPbb-97CI14) and SIVolc (SIVolc-97CI12) from olive colobus (Procolobus verus). Phylogenetic analysis showed that western red colobus are the natural hosts of SIVwrc, and SIVolc is also a distinct species-specific lineage, although distantly related to the SIVwrc lineage across the entire length of its genome. Overall, both SIVwrc and SIVolc, are also distantly related to the SIVlho/sun lineage across the whole genome. Similar to the group of SIVs (SIVsyk, SIVdeb, SIVden, SIVgsn, SIVmus, and SIVmon) infecting members of the Cercopithecus genus, SIVs derived from western red and olive colobus, L'Hoest and suntailed monkeys, and SIVmnd-1 from mandrills form a second group of viruses that cluster consistently together in phylogenetic trees. Interestingly, the divergent SIVcol lineage, from mantled guerezas (Colobus guereza) in Cameroon, is also closely related to SIVwrc, SIVolc, and the SIVlho/sun lineage in the 5′ part of Pol. Overall, these results suggest an ancestral link between these different lentiviruses and highlight once more the complexity of the natural history and evolution of primate lentiviruses.
doi:10.1128/JVI.01725-08
PMCID: PMC2612338  PMID: 18922864
10.  The consequences of crowned eagle central-place foraging on predation risk in monkeys. 
The African crowned eagle (Stepahnoaetus coronatus) is the primary predator for arboreal primates throughout sub-Saharan forests. Monkeys typically respond with alarm calls when they are aware of the presence of crowned eagles and such calls can be considered a corollary of predation risk within primate groups. Alarm calls from six species of monkeys were recorded across the home range of an eagle pair in Taï National Park, Côte d'Ivoire. Spatial and temporal variation in primate alarm calling was found to be related to eagle ranging behaviour according to the predictions of central-place foraging models. Radio-tracking data indicate that eagle activity is higher in the centre of their home range and monkey alarm-calling rates are correspondingly elevated near eagle nests as opposed to farther away. Alarm-calling rates are also temporally coupled with measures of eagle activity. There were considerable differences between the species in both rates and spatial patterns of alarm calling. The variation we measure in predation risk is expected to have consequences at the behavioural and population level.
doi:10.1098/rspb.2002.2098
PMCID: PMC1691090  PMID: 12350267
11.  DNA marker technology for wildlife conservation 
Use of molecular markers for identification of protected species offers a greater promise in the field of conservation biology. The information on genetic diversity of wildlife is necessary to ascertain the genetically deteriorated populations so that better management plans can be established for their conservation. Accurate classification of these threatened species allows understanding of the species biology and identification of distinct populations that should be managed with utmost care. Molecular markers are versatile tools for identification of populations with genetic crisis by comparing genetic diversities that in turn helps to resolve taxonomic uncertainties and to establish management units within species. The genetic marker analysis also provides sensitive and useful tools for prevention of illegal hunting and poaching and for more effective implementation of the laws for protection of the endangered species. This review summarizes various tools of DNA markers technology for application in molecular diversity analysis with special emphasis on wildlife conservation.
doi:10.1016/j.sjbs.2011.03.002
PMCID: PMC3730548  PMID: 23961128
Biodiversity; Conservation; Endangered animals; Fingerprinting; Molecular markers; Wildlife
12.  A New Variant of the Capsule 3 Cluster Occurs in Streptococcus pneumoniae from Deceased Wild Chimpanzees 
PLoS ONE  2011;6(9):e25119.
The presence of new Streptococcus pneumoniae clones in dead wild chimpanzees from the Taï National Park, Côte d'Ivoire, with previous respiratory problems has been demonstrated recently by DNA sequence analysis from samples obtained from the deceased apes. In order to broadenour understanding on the relatedness of these pneumococcal clones to those from humans, the gene locus responsible for biosynthesis of the capsule polysaccharide (CPS) has now been characterized. DNA sequence analysis of PCR fragments identified a cluster named cps3Taï containing the four genes typical for serotype 3 CPS, but lacking a 5′-region of ≥2 kb which is degenerated in other cps3 loci and not required for type 3 biosynthesis. CPS3 is composed of a simple disaccharide repeat unit comprising glucose and glucuronic acid (GlcUA). The two genes ugd responsible for GlcUA synthesis and wchE encoding the type 3 synthase are essential for CPS3 biosynthesis, whereas both, galU and the 3′-truncated gene pgm are not required due to the presence of homologues elsewhere in the genome. The DNA sequence of cps3Taï diverged considerably from those of other cps3 loci. Also, the gene pgmTaï represents a full length version with a nonsense mutation at codon 179. The two genes ugdTaï and wchETaï including the promoter region were transformed into a nonencapsulated laboratory strain S. pneumoniae R6. Transformants which expressed type 3 capsule polysaccharide were readily obtained, documenting that the gene products are functional. In summary, the data indicate that cps3Taï evolved independent from other cps3 loci, suggesting the presence of specialized serotype 3 S. pneumoniae clones endemic to the Taï National Park area.
doi:10.1371/journal.pone.0025119
PMCID: PMC3182177  PMID: 21969869
13.  Receiving Post-Conflict Affiliation from the Enemy's Friend Reconciles Former Opponents 
PLoS ONE  2010;5(11):e13995.
The adaptive function of bystander initiated post-conflict affiliation (also: consolation & appeasement) has been debated for 30 years. Three influential hypotheses compete for the most likely explanation but have not previously been tested with a single data set. The consolation hypothesis argues that bystander affiliation calms the victim and reduces their stress levels. The self-protection hypothesis proposes that a bystander offers affiliation to either opponent to protect himself from redirected aggression by this individual. The relationship-repair hypothesis suggests a bystander can substitute for a friend to reconcile the friend with the friend's former opponent. Here, we contrast all three hypotheses and tested their predictions with data on wild chimpanzees (Pan troglodytes verus) of the Taï National Park, Côte d'Ivoire. We examined the first and second post-conflict interactions with respect to both the dyadic and triadic relationships between the bystander and the two opponents. Results showed that female bystanders offered affiliation to their aggressor friends and the victims of their friends, while male bystanders offered affiliation to their victim friends and the aggressors of their friends. For both sexes, bystander affiliation resulted in a subsequent interaction pattern that is expected for direct reconciliation. Bystander affiliation offered to the opponent's friend was more likely to lead to affiliation among opponents in their subsequent interaction. Also, tolerance levels among former opponents were reset to normal levels. In conclusion, this study provides strong evidence for the relationship-repair hypothesis, moderate evidence for the consolation hypothesis and no evidence for the self-protection hypothesis. Furthermore, that bystanders can repair a relationship on behalf of their friend indicates that recipient chimpanzees are aware of the relationships between others, even when they are not kin. This presents a mechanism through which chimpanzees may gain benefits from social knowledge.
doi:10.1371/journal.pone.0013995
PMCID: PMC2981571  PMID: 21085592
14.  A New Flavivirus and a New Vector: Characterization of a Novel Flavivirus Isolated from Uranotaenia Mosquitoes from a Tropical Rain Forest▿ † 
Journal of Virology  2009;83(9):4462-4468.
A novel flavivirus was isolated from Uranotaenia mashonaensis, a mosquito genus not previously known to harbor flaviviruses. Mosquitoes were caught in the primary rain forest of the Taï National Park, Côte d'Ivoire. The novel virus, termed nounané virus (NOUV), seemed to grow only on C6/36 insect cells and not on vertebrate cells. Typical enveloped flavivirus-like particles of 60 to 65 nm in diameter were detected by electron microscopy in the cell culture supernatant of infected cells. The full genome was sequenced, and potential cleavage and glycosylation sites and cysteine residues were identified, suggesting that the processing of the NOUV polyprotein is similar to that of other flaviviruses. Phylogenetic analyses of the whole polyprotein and the NS3 protein showed that the virus forms a distinct cluster within the clade of mosquito-borne flaviviruses. Only a distant relationship to other known flaviviruses was found, indicating that NOUV is a novel lineage within the Flaviviridae.
doi:10.1128/JVI.00014-09
PMCID: PMC2668441  PMID: 19224998
15.  Pasteurella multocida Involved in Respiratory Disease of Wild Chimpanzees 
PLoS ONE  2011;6(9):e24236.
Pasteurella multocida can cause a variety of diseases in various species of mammals and birds throughout the world but nothing is known about its importance for wild great apes. In this study we isolated P. multocida from wild living, habituated chimpanzees from Taï National Park, Côte d'Ivoire. Isolates originated from two chimpanzees that died during a respiratory disease outbreak in 2004 as well as from one individual that developed chronic air-sacculitis following this outbreak. Four isolates were subjected to a full phenotypic and molecular characterisation. Two different clones were identified using pulsed field gel electrophoresis. Multi Locus Sequence Typing (MLST) enabled the identification of previous unknown alleles and two new sequence types, ST68 and ST69, were assigned. Phylogenetic analysis of the superoxide dismutase (sodA) gene and concatenated sequences from seven MLST-housekeeping genes showed close clustering within known P. multocida isolated from various hosts and geographic locations. Due to the clinical relevance of the strains described here, these results make an important contribution to our knowledge of pathogens involved in lethal disease outbreaks among endangered great apes.
doi:10.1371/journal.pone.0024236
PMCID: PMC3169569  PMID: 21931664
16.  The impact of armed conflict on protected-area efficacy in Central Africa 
Biology Letters  2007;3(3):299-301.
What determines the vulnerability of protected areas, a fundamental component of biodiversity conservation, to political instability and warfare? We investigated the efficacy of park protection at Garamba National Park (Democratic Republic of Congo) before, during and after a period of armed conflict. Previous analysis has shown that bushmeat hunting in the park increased fivefold during the conflict, but then declined, in conjunction with changes in the sociopolitical structures (social institutions) that controlled the local bushmeat trade. We used park patrol records to investigate whether these changes were facilitated by a disruption to anti-poaching patrols. Contrary to expectation, anti-poaching patrols remained frequent during the conflict (as bushmeat offtake increased) and decreased afterwards (when bushmeat hunting also declined). These results indicate that bushmeat extraction was determined primarily by the social institutions. Although we found a demonstrable effect of anti-poaching patrols on hunting pressure, even a fourfold increase in patrol frequency would have been insufficient to cope with wartime poaching levels. Thus, anti-poaching patrols alone may not always be the most cost-effective means of managing protected areas, and protected-area efficacy might be enhanced by also working with those institutions that already play a role in regulating local natural-resource use.
doi:10.1098/rsbl.2007.0010
PMCID: PMC2464688  PMID: 17360251
conservation biology; protected areas; armed conflict
17.  Primate DNA suggests long-term stability of an African rainforest 
Ecology and Evolution  2012;2(11):2829-2842.
Red colobus monkeys, due to their sensitivity to environmental change, are indicator species of the overall health of their tropical rainforest habitats. As a result of habitat loss and overhunting, they are among the most endangered primates in the world, with very few viable populations remaining. Traditionally, extant indicator species have been used to signify the conditions of their current habitats, but they have also been employed to track past environmental conditions by detecting previous population fluctuations. Kibale National Park (KNP) in Uganda harbors the only remaining unthreatened large population of red colobus. We used microsatellite DNA to evaluate the historical demography of these red colobus and, therefore, the long-term stability of their habitat. We find that the red colobus population throughout KNP has been stable for at least ∼40,000 years. We interpret this result as evidence of long-term forest stability because a change in the available habitat or population movement would have elicited a corresponding change in population size. We conclude that the forest of what is now Kibale National Park may have served as a Late Pleistocene refuge for many East African species.
doi:10.1002/ece3.395
PMCID: PMC3501634  PMID: 23170217
Coalescent theory; conservation biology; historical demography; microsatellites; red colobus
18.  Protected-Area Boundaries as Filters of Plant Invasions 
Conservation Biology  2011;25(2):400-405.
Abstract
Human land uses surrounding protected areas provide propagules for colonization of these areas by non-native species, and corridors between protected-area networks and drainage systems of rivers provide pathways for long-distance dispersal of non-native species. Nevertheless, the influence of protected-area boundaries on colonization of protected areas by invasive non-native species is unknown. We drew on a spatially explicit data set of more than 27,000 non-native plant presence records for South Africa's Kruger National Park to examine the role of boundaries in preventing colonization of protected areas by non-native species. The number of records of non-native invasive plants declined rapidly beyond 1500 m inside the park; thus, we believe that the park boundary limited the spread of non-native plants. The number of non-native invasive plants inside the park was a function of the amount of water runoff, density of major roads, and the presence of natural vegetation outside the park. Of the types of human-induced disturbance, only the density of major roads outside the protected area significantly increased the number of non-native plant records. Our findings suggest that the probability of incursion of invasive plants into protected areas can be quantified reliably.
Límites de Áreas Protegidas como Filtros para la Invasión de Plantas
Resumen
Los usos de suelo alrededor de áreas protegidas proporcionan propágulos para la colonización de estas áreas por especies no nativas, y los corredores entre las redes de áreas protegidas y los sistema fluviales proporcionan medios para la dispersión a larga distancia de especies no nativas. Sin embargo, se desconoce la influencia de los límites del área protegida sobre la colonización de áreas protegidas por especies invasoras no nativas. Utilizamos un conjunto de datos espacialmente explícitos con más de 27,000 registros de la presencia de especies de plantas no nativas en el Parque Nacional Kruger en Sudáfrica para examinar el papel de los límites en la prevención de la colonización de áreas protegidas por especies no nativas. El número de registros de plantas invasoras no nativas disminuyó rápidamente más allá de 1500 m dentro del parque; por lo tanto, consideramos que el límite del parque impidió la dispersión de plantas no nativas. El número de plantas invasoras no nativas dentro del parque fue una función de la escorrentía de agua, la densidad de caminos principales y la presencia de vegetación natural fuera del parque. De los tipos de perturbación humana inducida, solo la densidad de caminos principales fuera del área protegida incrementó el número de registros de plantas no nativas. Nuestros hallazgos sugieren que la probabilidad de incursión de plantas invasoras hacia áreas protegidas puede ser cuantificada confiablemente.
doi:10.1111/j.1523-1739.2010.01617.x
PMCID: PMC3085078  PMID: 21166715
barriers to invasion; Kruger National Park; non-native invasive species; overland water flow; protected-area boundary; barreras contra invasión; especies invasoras no nativas; flujo de agua superficial; límite de área protegida; Parque Nacional Kruger
19.  The Status of Wildlife in Protected Areas Compared to Non-Protected Areas of Kenya 
PLoS ONE  2009;4(7):e6140.
We compile over 270 wildlife counts of Kenya's wildlife populations conducted over the last 30 years to compare trends in national parks and reserves with adjacent ecosystems and country-wide trends. The study shows the importance of discriminating human-induced changes from natural population oscillations related to rainfall and ecological factors. National park and reserve populations have declined sharply over the last 30 years, at a rate similar to non-protected areas and country-wide trends. The protected area losses reflect in part their poor coverage of seasonal ungulate migrations. The losses vary among parks. The largest parks, Tsavo East, Tsavo West and Meru, account for a disproportionate share of the losses due to habitat change and the difficulty of protecting large remote parks. The losses in Kenya's parks add to growing evidence for wildlife declines inside as well as outside African parks. The losses point to the need to quantify the performance of conservation policies and promote integrated landscape practices that combine parks with private and community-based measures.
doi:10.1371/journal.pone.0006140
PMCID: PMC2702096  PMID: 19584912
20.  Sexual Differences in Chimpanzee Sociality 
Scientists usually attribute sexual differences in sociality to sex-specific dispersal patterns and the availability of kin within the social group. In most primates, the dispersing sex, which has fewer kin around, is the less social sex. Chimpanzees fit well into the pattern, with highly social philopatric males and generally solitary dispersing females. However, researchers in West Africa have long suggested that female chimpanzees can be highly social. We investigated whether chimpanzees in the Taï Forest (Côte d’Ivoire) exhibit the expected sexual differences in 3 social parameters: dyadic association, party composition, and grooming interactions. Though we found a significant sexual difference in each of the 3 parameters, with males being more social than females, the actual values do not reveal striking differences between the sexes and do not support the notion of female chimpanzees as asocial: females had dyadic association indices comparable to mixed-sex dyads, spent ca. 82% of their time together with other adult chimpanzees, and had a comparable number of grooming partners. Further, female associations can be among the strongest bonds within the community, indicating that both sexes can have strongly favored association partners. The findings are in contrast to reports on East African chimpanzees, the females of which are mainly solitary and rarely interact with other females. Our results suggest that researchers cannot generally regard chimpanzee females as asocial and need to redefine models deriving patterns of sociality from dispersal patterns to integrate the possibility of high female sociality in male philopatric systems.
doi:10.1007/s10764-007-9230-9
PMCID: PMC2758377  PMID: 19816541
association; chimpanzee; sex differences; sociality
21.  New Streptococcus pneumoniae Clones in Deceased Wild Chimpanzees▿  
Journal of Bacteriology  2007;189(16):6085-6088.
In wild chimpanzees in the Taï National Park, Côte d'Ivoire, sudden deaths which were preceded by respiratory problems had been observed since 1999. Two new clones of Streptococcus pneumoniae were identified in deceased apes on the basis of multilocus sequence typing analysis and ply, lytA, and pbp2x sequences. The findings suggest that virulent S. pneumoniae occurs in populations of wild chimpanzees with the potential to cause infections similar to those observed in humans.
doi:10.1128/JB.00468-07
PMCID: PMC1952052  PMID: 17586649
22.  Partial Molecular Characterization of Two Simian Immunodeficiency Viruses (SIV) from African Colobids: SIVwrc from Western Red Colobus (Piliocolobus badius) and SIVolc from Olive Colobus (Procolobus verus) 
Journal of Virology  2003;77(1):744-748.
In order to study primate lentivirus evolution in the Colobinae subfamily, in which only one simian immunodeficiency virus (SIV) has been described to date, we screened additional species from the three different genera of African colobus monkeys for SIV infection. Blood was obtained from 13 West African colobids, and HIV cross-reactive antibodies were observed in 5 of 10 Piliocolobus badius, 1 of 2 Procolobus verus, and 0 of 1 Colobus polykomos specimens. Phylogenetic analyses of partial pol sequences revealed that the new SIVs were more closely related to each other than to the other SIVs and especially did not cluster with the previously described SIVcol from Colobus guereza. This study presents evidence that the three genera of African colobus monkeys are naturally infected with an SIV and indicates also that there was no coevolution between virus and hosts at the level of the Colobinae subfamily.
doi:10.1128/JVI.77.1.744-748.2003
PMCID: PMC140619  PMID: 12477880
23.  National Park Development in China: Conservation or Commercialization? 
Ambio  2011;41(3):247-261.
The rapid development of parks and ecotourism in China has attracted worldwide attention, not only for the beauty of the landscape that the parks are protecting but also for their abundant and often unique biodiversity. However, in some areas, the development of ecotourism has actually led to the degradation of local ecological, economic, and social systems. Using National Forest Parks for demonstration, this article analyzes the current political, institutional, legal, environmental, and economic issues concerning National Parks in China, and examines their potential future development. Although the intention of National Park systems in China is to raise environmental quality, and to protect biodiversity and social livelihoods, their success has varied. Future success will be measured by their capacity to reduce poverty, to promote long-term rehabilitation of wildlife habitats, and to simultaneously protect Chinese culture and biodiversity.
doi:10.1007/s13280-011-0194-9
PMCID: PMC3357853  PMID: 22038320
National Parks; Conservation; Natural resources; Degradation; Ecotourism; China
24.  A Century of Change in Kenya's Mammal Communities: Increased Richness and Decreased Uniqueness in Six Protected Areas 
PLoS ONE  2014;9(4):e93092.
The potential for large-scale biodiversity losses as a result of climate change and human impact presents major challenges for ecology and conservation science. Governments around the world have established national parks and wildlife reserves to help protect biodiversity, but there are few studies on the long-term consequences of this strategy. We use Kenya as a case study to investigate species richness and other attributes of mammal communities in 6 protected areas over the past century. Museum records from African expeditions that comprehensively sampled mammals from these same areas in the early 1900's provide a baseline for evaluating changes in species richness and community structure over time. We compare species lists assembled from archived specimens (1896–1950) to those of corresponding modern protected areas (1950–2013). Species richness in Kenya was stable or increased at 5 out of 6 sites from historical to modern times. Beta-diversity, in contrast, decreased across all sites. Potential biases such as variable historical vs. modern collection effort and detection of small-bodied, rare, and low-visibility species do not account for the observed results. We attribute the pattern of decreased beta diversity primarily to increased site occupancy by common species across all body size classes. Despite a decrease in land area available to wildlife, our data do not show the extinctions predicted by species-area relationships. Moreover, the results indicate that species-area curves based solely on protected areas could underestimate diversity because they do not account for mammal species whose ranges extend beyond protected area boundaries. We conclude that the 6 protected areas have been effective in preserving species richness in spite of continuing conversion of wild grasslands to cropland, but the overall decrease in beta diversity indicates a decline in the uniqueness of mammal communities that historically characterized Kenya's varied landscape.
doi:10.1371/journal.pone.0093092
PMCID: PMC3981716  PMID: 24718262
25.  Tourism and the Conservation of Critically Endangered Frogs 
PLoS ONE  2012;7(9):e43757.
Protected areas are critical for the conservation of many threatened species. Despite this, many protected areas are acutely underfunded, which reduces their effectiveness significantly. Tourism is one mechanism to promote and fund conservation in protected areas, but there are few studies analyzing its tangible conservation outcomes for threatened species. This study uses the 415 IUCN critically endangered frog species to evaluate the contribution of protected area tourism revenue to conservation. Contributions were calculated for each species as the proportion of geographic range inside protected areas multiplied by the proportion of protected area revenues derived from tourism. Geographic ranges were determined from IUCN Extent of Occurrence maps. Almost 60% (239) of critically endangered frog species occur in protected areas. Higher proportions of total range are protected in Nearctic, Australasian and Afrotopical regions. Tourism contributions to protected area budgets ranged from 5–100%. These financial contributions are highest for developing countries in the Afrotropical, Indomalayan and Neotropical regions. Data for both geographic range and budget are available for 201 critically endangered frog species with proportional contributions from tourism to species protection ranging from 0.8–99%. Tourism's financial contributions to critically endangered frog species protection are highest in the Afrotropical region. This study uses a coarse measure but at the global scale it demonstrates that tourism has significant potential to contribute to global frog conservation efforts.
doi:10.1371/journal.pone.0043757
PMCID: PMC3440435  PMID: 22984440

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