Junker, J., Petrovan, S., Arroyo-RodrÍguez, V., Boonratana, R., Byler, D., Chapman, C., Chetry, D., Cheyne, S., Cornejo, F., CortÉs-Ortiz, L., Cowlishaw, G., Christie, A., Crockford, C., Torre, S., De Melo, F., Fan, P., Grueter, C., GuzmÁn-Caro, D., Heymann, E., Herbinger, I., Hoang, M., Horwich, R., Humle, T., Ikemeh, R., Imong, I., Jerusalinsky, L., Johnson, S., Kappeler, P., Kierulff, M., KonÉ, I., Kormos, R., Le, K., Li, B., Marshall, A., Meijaard, E., Mittermeier, R., Muroyama, Y., Neugebauer, E., Orth, L., Palacios, E., Papworth, S., Plumptre, A., Rawson, B., Refisch, J., Ratsimbazafy, J., Roos, C., Setchell, J., Smith, R., Sop, T., Schwitzer, C., Slater, K., Strum, S., Sutherland, W., Talebi, M., Wallis, J., Wich, S., Williamson, E., Wittig, R. and KÜhl, H. (2020). A Severe Lack of Evidence Limits Effective Conservation of the World’s Primates. BioScience [Online]. Available at: https://doi.org/10.1093/biosci/biaa082.
Threats to biodiversity are well documented. However, to effectively conserve species and their habitats, we need to know which conservation interventions do (or do not) work. Evidence-based conservation evaluates interventions within a scientific framework. The Conservation Evidence project has summarized thousands of studies testing conservation interventions and compiled these as synopses for various habitats and taxa. In the present article, we analyzed the interventions assessed in the primate synopsis and compared these with other taxa. We found that despite intensive efforts to study primates and the extensive threats they face, less than 1% of primate studies evaluated conservation effectiveness. The studies often lacked quantitative data, failed to undertake postimplementation monitoring of populations or individuals, or implemented several interventions at once. Furthermore, the studies were biased toward specific taxa, geographic regions, and interventions. We describe barriers for testing primate conservation interventions and propose actions to improve the conservation evidence base to protect this endangered and globally important taxon.
Dendup, P., Humle, T., Bista, D., Penjor, U., Lham, C. and Gyeltshen, J. (2020). Habitat requirements of the Himalayan red panda (Ailurus fulgens) and threat analysis in Jigme Dorji National Park, Bhutan. Ecology and Evolution [Online]. Available at: https://doi.org/10.1002/ece3.6632.
Understanding the influence of anthropogenic disturbances on species’ habitat use and distribution is critical to conservation managers in planning effective conservation strategies and mitigating the impact of development. Few studies have focused on the Himalayan red panda (Ailurus fulgens) in Bhutan. This study aimed to assess the habitat requirements and threats to this endangered species in the Khamaed sub-district of the Jigme Dorji National Park, Bhutan. We employed a transect walk and plot-sampling survey design across two seasons, i.e. winter and spring. In total, we surveyed 84 x 50 m radius circular plots along 51 km of existing trails within a 25.4 km2 study area. At 500 m intervals, we established plots at random distances and direction from the trail. We recorded direct sightings (n = 2) and indirect signs (n = 14), such as droppings and footprints as evidence of red panda presence within an altitudinal range of 2,414 – 3,618 m. We also noted 21 tree and 12 understory species within plots with red panda evidence; the dominant tree species was the Himalayan hemlock (Tsuga dumosa) and the Asian barberry (Berberis asiatica) as an understory species. Red panda presence showed a significant positive association with distance to water sources and fir forests. Plant disturbance and infrastructure, such as power transmission lines, were identified as prominent anthropogenic threats in the study area. Based on our findings, we recommend the development and implementation of local forest management plans, livestock intensification programs and strict application of environmental impact assessment regulations to promote the conservation of the red panda in the region.
Duonamou, L., Konate, A., Djego-Djossou, S., Mensah, G., Xu, J. and Humle, T. (2020). Consumer perceptions and reported wild and domestic meat and fish consumption behavior during the Ebola epidemic in Guinea, West Africa. PeerJ [Online] 8. Available at: http://dx.doi.org/10.7717/peerj.9229.
The handling, capturing, butchering, and transportation of wildmeat can increase the risk of zoonoses, including the Ebola virus disease (EVD). Guinea, West Africa, experienced a catastrophic outbreak of EVD between 2013-2016. This study aimed to understand local people’s sources of information concerning EVD, their perceptions of potential wildlife carriers of EVD and their meat and fish consumption behavior during this period. A semi-structured questionnaire was administered to 332 participants in two urban centers (N=209) and three villages (N=123) between January 3 to March 30, 2015 in the prefecture of Lola in southeastern Guinea. Chi-square analyses revealed that, in rural areas, awareness missions represented the main source of information about EVD (94.3%), whereas in urban settings such missions (36.1%), as well as newspapers (31.6%) and radio (32.3%) were equally mentioned. Bats (30.1% and 79.4%), chimpanzees (16.3% and 48.8%) and monkeys (13.0% and 53.1%) were the most commonly cited potential agents of EVD in both rural and urban areas respectively, while the warthog (2.3% rural and 6.5% urban), crested porcupine (1.7% rural and 10.7% urban), duiker (1.19% rural and 2.6% urban) and the greater cane rat (1.1% rural and 9.5% urban) were also cited but to a lesser extent. However, 66.7% of rural respondents compared to only 17.2% in the urban area did not consider any of these species as potential carriers of the Ebola virus. Nonetheless, a fifth of our respondents reported not consuming any of these species altogether during the EVD outbreak. Among all seven faunal groups mentioned, a significant reduction in reported consumption during the Ebola outbreak was only noted for bats (before: 78.3% and during: 31.9%) and chimpanzees (before: 31.6% and during: 13.5%). Automatic Chi-Square Interaction Detection (CHAID) analysis revealed that the belief that bats or chimpanzees were associated with EVD or not had a significant effect respectively on their non-consumption or continued consumption during the EVD outbreak. However, only 3.9% of respondents reported shifting to alternative protein sources such as domestic meat or fish specifically to avoid EVD. Only 10.8% reported consuming more domestic meat during the EVD outbreak compared with before; affordability and availability were the main reported reasons for why people did not consume more domestic meat and why two thirds reported consuming more fish. While increased domestic meat consumption was linked to the belief that duikers, the most commonly consumed wildmeat before the epidemic, were associated with EVD, increased fish consumption was not predicted by any EVD related factors. Our study revealed deep-rooted false beliefs among rural respondents and constraints when it comes to access to alternative protein sources such as domestic meat. Our findings emphasize the urgent need for greater consideration of the relationship between socio-economic context, food security, and public health.
Mubemba, B., Chanove, E., Mätz-Rensing, K., Gogarten, J., Düx, A., Merkel, K., Röthemeier, C., Sachse, A., Rase, H., Humle, T., Banville, G., Tchoubar, M., Calvignac-Spencer, S., Colin, C. and Leendertz, F. (2020). Yaws Disease Caused by Treponema pallidum subspecies pertenue in Wild Chimpanzee, Guinea, 2019. Emerging Infectious Diseases [Online] 26. Available at: http://dx.doi.org/10.3201/EID2606.191713.
Yaws-like lesions are widely reported in wild African great apes, yet the causative agent has not been confirmed in affected animals. We describe yaws-like lesions in a wild chimpanzee in Guinea for which we demonstrate infection with Treponema pallidum subsp. pertenue. Assessing the conservation implications of this pathogen requires further research.
Bryson‐Morrison, N., Beer, A., Gaspard Soumah, A., Matsuzawa, T. and Humle, T. (2020). The macronutrient composition of wild and cultivated plant foods of West African chimpanzees (Pan troglodytes verus ) inhabiting an anthropogenic landscape. American Journal of Primatology [Online]. Available at: https://doi.org/10.1002/ajp.23102.
Agricultural expansion encroaches on tropical forests and primates in such landscapes frequently incorporate crops into their diet. Understanding the nutritional drivers behind crop‐foraging can help inform conservation efforts to improve human‐primate coexistence. This study builds on existing knowledge of primate diets in anthropogenic landscapes by estimating the macronutrient content of 24 wild and 11 cultivated foods (90.5% of food intake) consumed by chimpanzees (Pan troglodytes verus) at Bossou, Guinea, West Africa. We also compared the macronutrient composition of Bossou crops to published macronutrient measures of crops from Bulindi, Uganda, East Africa. The composition of wild fruits, leaves, and pith were consistent with previous reports for primate diets. Cultivated fruits were higher in carbohydrates and lower in insoluble fiber than wild fruits, while wild fruits were higher in protein. Macronutrient content of cultivated pith fell within the ranges of consumed wild pith. Oil palm food parts were relatively rich in carbohydrates, protein, lipids, and/or fermentable fiber, adding support for the nutritional importance of the oil palm for West African chimpanzees. We found no differences in the composition of cultivated fruits between Bossou and Bulindi, suggesting that macronutrient content alone does not explain differences in crop selection. Our results build on the current understanding of chimpanzee feeding ecology within forest‐agricultural mosaics and provide additional support for the assumption that crops offer primates energetic benefits over wild foods.
Dore, K., Hansen, M., Klegarth, A., Fichtel, C., Koch, F., Springer, A., Kappeler, P., Parga, J., Humle, T., Colin, C., Raballand, E., Huang, Z., Qi, X., Di Fiore, A., Link, A., Stevenson, P., Stark, D., Tan, N., Gallagher, C., Anderson, C., Campbell, C., Kenyon, M., Pebsworth, P., Sprague, D., Jones-Engel, L. and Fuentes, A. (2020). Review of GPS Collar Deployments and Performance on Nonhuman Primates. Primates [Online] 61:373-387. Available at: https://doi.org/10.1007/s10329-020-00793-7.
Over the past twenty years, GPS collars have emerged as powerful tools for the study of nonhuman primate (hereafter, "primate") movement ecology. As the size and cost of GPS collars have decreased and performance has improved, it is timely to review the use and success of GPS collar deployments on primates to date. Here we compile data on deployments and performance of GPS collars by brand and examine how these relate to characteristics of the primate species and field contexts in which they were deployed. The compiled results of 179 GPS collar deployments across 17 species by 16 research teams show these technologies can provide advantages, particularly in adding to the quality, quantity, and temporal span of data collection. However, aspects of this technology still require substantial improvement in order to make deployment on many primate species pragmatic economically. In particular, current limitations regarding battery lifespan relative to collar weight, the efficacy of remote drop-off mechanisms, and the ability to remotely retrieve data need to be addressed before the technology is likely to be widely adopted. Moreover, despite the increasing utility of GPS collars in the field, they remain substantially more expensive than VHF collars and tracking via handheld GPS units, and cost considerations of GPS collars may limit sample sizes and thereby the strength of inferences. Still, the overall high quality and quantity of data obtained, combined with the reduced need for on-the-ground tracking by field personnel, may help defray the high equipment cost. We argue that primatologists armed with the information in this review have much to gain from the recent, substantial improvements in GPS collar technology.
Seaman, D., Bernard, H., Ancrenaz, M., Coomes, D., Swinfield, T., Milodowski, D., Humle, T. and Struebig, M. (2019). Densities of Bornean orang‐utans ( Pongo pygmaeus morio ) in heavily degraded forest and oil palm plantations in Sabah, Borneo. American Journal of Primatology [Online]. Available at: https://doi.org/10.1002/ajp.23030.
The conversion of forest to agriculture continues to contribute to the loss and fragmentation of remaining orang‐utan habitat. There are still few published estimates of orang‐utan densities in these heavily modified agricultural areas to inform range‐wide population assessments and conservation strategies. In addition, little is known about what landscape features promote orang‐utan habitat use. Using indirect nest count methods, we implemented surveys and estimated population densities of the Northeast Bornean orang‐utan (Pongo pygmaeus morio) across the continuous logged forest and forest remnants in a recently salvage‐logged area and oil palm plantations in Sabah, Malaysian Borneo. We then assessed the influence of landscape features and forest structural metrics obtained from LiDAR data on estimates of orang‐utan density. Recent salvage logging appeared to have a little short‐term effect on orang‐utan density (2.35 ind/km 2), which remained similar to recovering logged forest nearby (2.32 ind/km 2). Orang‐utans were also present in remnant forest patches in oil palm plantations, but at significantly lower numbers (0.82 ind/km 2) than nearby logged forest and salvage‐logged areas. Densities were strongly influenced by variation in canopy height but were not associated with other potential covariates. Our findings suggest that orang‐utans currently exist, at least in the short‐term, within human‐modified landscapes, providing that remnant forest patches remain. We urge greater recognition of the role that these degraded habitats can have in supporting orang‐utan populations, and that future range‐wide analyses and conservation strategies better incorporate data from human‐modified landscapes.
Garriga, R., Marco, I., Casas-Díaz, E., Acevedo, P., Amarasekaran, B., Cuadrado, L. and Humle, T. (2019). Factors influencing wild chimpanzee (Pan troglodytes verus) relative abundance in an agriculture-swamp matrix outside protected areas. PLOS ONE [Online] 14:e0215545. Available at: https://doi.org/10.1371/journal.pone.0215545.
Human population growth and anthropogenic activities are exacerbating pressures on biodiversity globally. Land conversion is aggravating habitat fragmentation and non-human primates are increasingly compelled to live in forest-agricultural mosaics. In Sierra Leone, more than half of the wild chimpanzee population (Pan troglodytes verus) occurs outside protected areas and competes for resources with farmers. Our study area, in the Moyamba district in south-western Sierra Leone, is practically devoid of forest and is dominated by cultivated and fallow fields, swamps and mangroves. In this region, traditional slash-and-burn agriculture modifies annually the landscape, sparing swamps and mangroves and semi-domesticated oil palms (Elaeis guineensis). This study aimed to explore ecological and anthropogenic factors influencing chimpanzee relative abundance across this highly degraded and human-impacted landscape. Between 2015 and 2016, we deployed 24 camera traps systematically across 27 1.25x1.25 km grid cells. Cameras were operational over a period of 8 months. We used binomial iCAR models to examine to what extent anthropogenic (roads, settlements, abandoned settlements and human presence) and habitat variables (swamps, farmland and mangroves) shape chimpanzee relative abundance. The best model explained 43.16% of the variation with distance to roads and swamps emerging as the best predictors of chimpanzee relative abundance. Our results suggest that chimpanzees avoid roads and prefer to maintain proximity to swamps. There was no significant effect of settlements, abandoned settlements, mangroves or human presence. It appears that chimpanzees do not avoid areas frequented by people; although, our findings suggest temporal avoidance between the two species. We highlight the importance of studying chimpanzee populations living in anthropogenic habitats like agricultural-swamp matrixes to better understand factors influencing their distribution and inform conservation planning outside protected areas.
Garriga, R., Marco, I., Casas-Díaz, E., Amarasekaran, B. and Humle, T. (2018). Perceptions of challenges to subsistence agriculture, and crop foraging by wildlife and chimpanzees Pan troglodytes verus in unprotected areas in Sierra Leone. Oryx [Online] 53:761-774. Available at: https://dx.doi.org/10.1017/S0030605316001319.
The 2009–2010 Sierra Leone National Chimpanzee Census Project estimated there was a population of 5,580 chimpanzees Pan troglodytes verus distributed across the country, with > 50% occurring outside protected areas. The census also highlighted the significance of competition between people and chimpanzees for resources in areas dominated by farming activities where wild chimpanzees forage on crops. We selected four study areas in two districts in Sierra Leone with high chimpanzee density in habitats dominated by agriculture, far from any protected areas. Our objectives were to assess farmers’ perceptions of the main challenges to their agricultural yields, and the wildlife involved in crop foraging, and their perceptions of chimpanzees in particular, as well as the main crop protection measures used. We conducted 257 semi-structured interviews with local farmers across the four study areas. We found that (1) farmers reported wild animals as the main challenge to their agricultural practices; (2) most complaints concerned cane rats Thryonomys swinderianus, which targeted almost all crop types, especially rice and cassava; (3) chimpanzees reportedly targeted 21 of the 23 crop types cultivated, but did so less often than cane rats, focusing particularly on oil palm, cassava and domestic fruits; (4) overall, chimpanzees were not among the top three most destructive animals reported; (5) chimpanzees were generally perceived as being more destructive than dangerous and as having declined since before the civil war; and (6) the main crop protection measure employed was fencing interspersed with traps. Our findings show the importance of investigating farmers’ perceptions to inform the development of appropriate conservation strategies aimed at promoting coexistence of people and wildlife in degraded landscapes.
Neufuss, J., Robbins, M., Baeumer, J., Humle, T. and Kivell, T. (2018). Manual skills for food processing by mountain gorillas in Bwindi Impenetrable National Park, Uganda. Biological Journal of the Linnean Society [Online] 127:543-562. Available at: https://doi.org/10.1093/biolinnean/bly071.
Although gorillas rarely use tools in the wild, their manipulative skills during plant processing may be similar to those of other tool-using great apes. Virunga mountain gorillas are known for the complexity in their methods of thistle and nettle plant preparation in the wild. However, there has been no comparable data on food processing in the population of mountain gorillas from the Bwindi Impenetrable National Park, Uganda. We investigated the manual actions and hand grips used when accessing edible parts of two hard-to-process plants defended by stinging hairs, epidermis or periderm (i.e., peel of Urera hypselodendron and pith of Mimulopsis arborescens) and one undefended plant (i.e., leaves of Momordica foetida) in 11 Bwindi wild mountain gorillas (Gorilla beringei beringei) using video records ad libitum. Similar to thistle feeding by Virunga gorillas, Bwindi gorillas used the greatest number of manual actions for the most hard-to-process plant (U. hypselodendron), the actions were ordered in several key stages and organised hierarchically. The demands of processing plant material elicited 19 different grips and variable thumb postures, of which three grips were new and 16 grips have either been previously reported or show clear similarities to grips used by other wild and captive African apes and humans. Moreover, our study only partly supports a functional link between diet and hand morphology in mountain gorillas and suggests that the gorilla hand is best adapted to forceful grasping that is required for both manipulation and arboreal locomotion.
Neufuss, J., Robbins, M., Baeumer, J., Humle, T. and Kivell, T. (2018). Gait characteristics of vertical climbing in mountain gorillas and chimpanzees. Journal of Zoology [Online] 306:129-138. Available at: https://doi.org/10.1111/jzo.12577.
Biomechanical analyses of arboreal locomotion in great apes in their natural environment are scarce and thus attempts to correlate behavioural and habitat differences with variations in morphology are limited. The aim of this study was to investigate the gait characteristics of vertical climbing in mountain gorillas (Gorilla beringei beringei) and chimpanzees (Pan troglodytes) in a natural environment to assess differences in the climbing styles that may relate to variation in body size. We investigated temporal variables (i.e., cycle duration, duty factors, and stride frequency) and footfall sequences (i.e., diagonal vs. lateral sequence gaits) during vertical climbing (both ascent and descent) in 11 wild mountain gorillas and compared these data to those of eight semi-free-ranging chimpanzees, using video records ad libitum. Comparisons of temporal gait parameters revealed that largebodied mountain gorillas exhibited a longer cycle duration, lower stride frequency and generally a higher duty factor than smaller-bodied chimpanzees. While both apes were similarly versatile in their vertical climbing performance in the natural environment, mountain gorillas most often engaged in diagonal sequence/diagonal couplet gaits and chimpanzees most often used lateral sequence/diagonal couplet gaits. This study revealed that mountain gorillas adapt their climbing strategy to accommodate their large body mass in a similar manner previously found in captive western lowland gorillas, and that chimpanzees are less variable in their climbing strategy than has been documented in captive bonobos.
Neufuss, J., Robbins, M., Baeumer, J., Humle, T. and Kivell, T. (2017). Comparison of hand use and forelimb posture during vertical climbing in mountain gorillas (Gorilla beringei beringei) and chimpanzees (Pan troglodytes). American Journal of Physical Anthropology [Online] 164:651-664. Available at: http://dx.doi.org/10.1002/ajpa.23303.
Objectives: Studies on grasping and limb posture during arboreal locomotion in great apes in their natural environment are scarce and thus, attempts to correlate behavioral and habitat differences with variation in morphology are limited. The aim of this study is to compare hand use and forelimb posture during vertical climbing in wild, habituated mountain gorillas (Gorilla beringei beringei) and semi-free-ranging chimpanzees (Pan troglodytes) to assess differences in the climbing styles that may relate to variation in hand or forelimb morphology and body size.
Materials and methods: We investigated hand use and forelimb posture during both ascent and descent vertical climbing in 15 wild mountain gorillas and eight semi-free-ranging chimpanzees, using video records obtained ad libitum.
Results: In both apes, forelimb posture was correlated with substrate size during both ascent and descent climbing. While climbing, both apes used power grips and diagonal power grips, including three different thumb postures. Mountain gorillas showed greater ulnar deviation of the wrist during vertical descent than chimpanzees, and the thumb played an important supportive role when gorillas vertically descended lianas.
Discussion: We found that both apes generally had the same grip preferences and used similar forelimb postures on supports of a similar size, which is consistent with their overall similarity in hard and soft tissue morphology of the hand and forelimb. However, some species-specific differences in morphology appear to elicit slightly different grasping strategies during vertical climbing between mountain gorillas and chimpanzees.
Bryson-Morrison, N., Tzanopoulos, J., Matsuzawa, T. and Humle, T. (2017). Activity and Habitat Use of Chimpanzees (Pan troglodytes verus) in the Anthropogenic Landscape of Bossou, Guinea, West Africa. International Journal of Primatology [Online]:1-21. Available at: http://dx.doi.org/10.1007/s10764-016-9947-4.
Many primate populations inhabit anthropogenic landscapes. Understanding their long-term ability to persist in such environments and associated real and perceived risks for both primates and people is essential for effective conservation planning. Primates in forest–agricultural mosaics often consume cultivars to supplement their diet, leading to potentially negative encounters with farmers. When crossing roads, primates also face the risk of encounters with people and collision with vehicles. Chimpanzees (Pan troglodytes verus) in Bossou, Guinea, West Africa, face such risks regularly. In this study, we aimed to examine their activity budget across habitat types and the influence of anthropogenic risks associated with cultivated fields, roads, and paths on their foraging behavior in noncultivated habitat. We conducted 6-h morning or afternoon follows daily from April 2012 to March 2013. Chimpanzees preferentially used forest habitat types for traveling and resting and highly disturbed habitat types for socializing. Wild fruit and crop availability influenced seasonal habitat use for foraging. Overall, chimpanzees preferred mature forest for all activities. They showed a significant preference for foraging at >200 m from cultivated fields compared to 0–100 m and 101–200 m, with no effect of habitat type or season, suggesting an influence of associated risk. Nevertheless, the chimpanzees did not actively avoid foraging close to roads and paths. Our study reveals chimpanzee reliance on different habitat types and the influence of human-induced pressures on their activities. Such information is critical for the establishment of effective land use management strategies in anthropogenic landscapes.
Leendertz, S., Wich, S., Ancrenaz, M., Bergl, R., Gonder, M., Humle, T. and Leendertz, F. (2016). Ebola in great apes – current knowledge, possibilities for vaccination, and implications for conservation and human health. Mammal Review [Online]. Available at: http://dx.doi.org/10.1111/mam.12082.
Ebola virus disease (EVD) is a threat to human health and to the survival of African great apes. The disease has led to major population declines in chimpanzees Pan troglodytes and gorillas Gorilla gorilla, and infected great apes play an important role as sources of human EVD outbreaks. The threat posed by EVD raises the question whether vaccination of wild apes is an effective strategy to reduce the occurrence and impact of this disease.
We review the current knowledge about EVD in great apes and document the link between outbreaks in apes and in humans, mainly via bushmeat consumption. We discuss the need for control strategies, such as vaccination, and describe aspects of primate behaviour, virus biology, vaccine composition, and vaccination principles that need to be considered when making management decisions about great ape vaccination. Finally, we identify gaps in the understanding of Ebola ecology and highlight surveillance and research that can aid the survival of great apes and reduce human exposure to Ebola virus.
The severe impact of EVD indicates the need for efficient monitoring and, ultimately, control of Ebola. However, the unknown reservoir and unpredictable emergence of Ebola, the elusive nature of great apes, and the lack of licensed and suitable vaccines represent major hurdles for such control. Public education about zoonotic diseases and monitoring of great ape health are both important strategies. Experts should also discuss the feasibility of developing safe vaccines that can be delivered efficiently to large populations of elusive wild apes in their natural remote habitats. This review provides a platform for further interdisciplinary discussions, so that management plans can be discussed and adjusted according to possible future changes in the development, availability and cost of vaccines, the status of EVD, knowledge about Ebola ecology, and opinion on wildlife vaccination.
Wilson, V., Weiss, A., Humle, T., Morimura, N., Udono, T., Idani, G., Matsuzawa, T., Hirata, S. and Inoue-Murayama, M. (2016). Chimpanzee Personality and the Arginine Vasopressin Receptor 1A Genotype. Behavior Genetics [Online]:1-12. Available at: http://dx.doi.org/10.1007/s10519-016-9822-2.
Polymorphisms of the arginine vasopressin receptor 1a (AVPR1a) gene have been linked to various measures related to human social behavior, including sibling conflict and agreeableness. In chimpanzees, AVPR1a polymorphisms have been associated with traits important for social interactions, including sociability, joint attention, dominance, conscientiousness, and hierarchical personality dimensions named low alpha/stability, disinhibition, and negative emotionality/low dominance. We examined associations between AVPR1a and six personality domains and hierarchical personality dimensions in 129 chimpanzees (Pan troglodytes) living in Japan or in a sanctuary in Guinea. We fit three linear and three animal models. The first model included genotype, the second included sex and genotype, and the third included genotype, sex, and sex × genotype. All personality phenotypes were heritable. Chimpanzees possessing the long form of the allele were higher in conscientiousness, but only in models that did not include the other predictors; however, additional analyses suggested that this may have been a consequence of study design. In animal models that included sex and sex × genotype, chimpanzees homozygous for the short form of the allele were higher in extraversion. Taken with the findings of previous studies of chimpanzees and humans, the findings related to conscientiousness suggest that AVPR1a may be related to lower levels of impulsive aggression. The direction of the association between AVPR1a genotype and extraversion ran counter to what one would expect if AVPR1a was related to social behaviors. These results help us further understand the genetic basis of personality in chimpanzees.
Neufuss, J., Humle, T., Cremaschi, A. and Kivell, T. (2016). Nut-cracking behaviour in wild-born, rehabilitated bonobos (Pan paniscus): a comprehensive study of hand preference, hand grips and efficiency. American Journal of Primatology [Online] 79. Available at: http://dx.doi.org/10.1002/ajp.22589.
There has been an enduring interest in primate tool-use and manipulative abilities, most often with the goal of providing insight into the evolution of human manual dexterity, right-hand preference, and what behaviours make humans unique. Chimpanzees (Pan troglodytes) are arguably the most well-studied tool-users amongst non-human primates, and are particularly well-known for their complex nut-cracking behaviour, which has been documented in several West African populations. However, their sister-taxon, the bonobos (Pan paniscus), rarely engage in even simple tool-use and are not known to nut-crack in the wild. Only a few studies have reported tool-use in captive bonobos, including their ability to crack nuts, but details of this complex tool-use behaviour have not been documented before. Here, we fill this gap with the first comprehensive analysis of bonobo nut-cracking in a natural environment at the Lola ya Bonobo sanctuary, Democratic Republic of the Congo. Eighteen bonobos were studied as they cracked oil palm nuts using stone hammers. Individual bonobos showed exclusive laterality for using the hammerstone and there was a significant group-level right-hand bias. The study revealed 15 hand grips for holding differently sized and weighted hammerstones, 10 of which had not been previously described in the literature. Our findings also demonstrated that bonobos select the most effective hammerstones when nut-cracking. Bonobos are efficient nut-crackers and not that different from the renowned nut-cracking chimpanzees of Bossou, Guinea, which also crack oil palm nuts using stones.
Bryson-Morrison, N., Matsuzawa, T. and Humle, T. (2016). Chimpanzees in an Anthropogenic Landscape: Examining Food Resources across Habitat Types at Bossou, Guinea, West Africa. American Journal of Primatology [Online] 78:1237-1249. Available at: http://dx.doi.org/10.1002/ajp.22578.
Many primate populations occur outside protected areas in fragmented anthropogenic landscapes. Empirical data on the ecological characteristics that define an anthropogenic landscape are urgently required if conservation initiatives in such environments are to succeed. The main objective of our study was to determine the composition and availability of chimpanzee (Pan troglodytes verus) food resources across fine spatial scales in the anthropogenic landscape of Bossou, Guinea, West Africa. We examined food resources in all habitat types available in the chimpanzees’ core area. We surveyed resource composition, structure and heterogeneity (20 m × 20 m quadrats, N = 54) and assessed temporal availability of food from phenology trails (total distance 5951 m; 1073 individual trees) over 1 year (2012–2013). Over half of Bossou consists of regenerating forest and is highly diverse in terms of chimpanzee food species; large fruit bearing trees are rare and confined to primary and riverine forest. Moraceae (mulberries and figs) was the dominant family, trees of which produce drupaceous fruits favored by chimpanzees. The oil palm occurs at high densities throughout and is the only species found in all habitat types except primary forest. Our data suggest that the high densities of oil palm and fig trees, along with abundant terrestrial herbaceous vegetation and cultivars, are able to provide the chimpanzees with widely available resources, compensating for the scarcity of large fruit trees. A significant difference was found between habitat types in stem density/ha and basal area m2/ha of chimpanzee food species. Secondary, young secondary, and primary forest emerged as the most important habitat types for availability of food tree species. Our study emphasizes the importance of examining ecological characteristics of an anthropogenic landscape as each available habitat type is unlikely to be equally important in terms of spatial and temporal availability of resources.
Humle, T. (2016). Franco-Japanese and other collaborative contributions to understanding chimpanzee culture at Bossou and the Nimba Mountains. Primates [Online] 57:339-348. Available at: http://dx.doi.org/10.1007/s10329-016-0536-0.
The Japanese approach to science has permitted theoretical leaps in our understanding of culture in non-human animals and challenged human uniqueness, as it is not embedded in the Western traditional dualisms of human/animal and nature/culture. This paper highlights the value of an interdisciplinary approach and combining methodological approaches in exploring putative cultural variation among chimpanzees. I focus particularly on driver ants (Dorylus sp.) and oil palm (Elaeis guineensis) consumption among the Bossou and Nimba chimpanzees, in south-eastern Guinea at the border with Côte d’Ivoire and Liberia, and hand use across different tool use tasks commonly witnessed at Bossou, i.e. ant-dipping, nut-cracking, pestle-pounding, and algae-scooping. Observed variation in resource use was addressed across differing scales exploring both within- and between-community differences. Our findings have highlighted a tight interplay between ecology, social dynamics and culture, and between social and individual learning and maternal contribution to tool-use acquisition. Exploration of hand use by chimpanzees revealed no evidence for individual-level hand or community-level task specialisation. However, more complex types of tool use such as nut-cracking showed distinct lateralization, while the equivalent of a haptic manual action revealed a strong right hand bias. The data also suggest an overall population tendency for a right hand preference. As well as describing these sites’ key contributions to our understanding of chimpanzees and to challenging our perceptions of human uniqueness, this paper also highlights the critical condition and high levels of threats facing this emblematic chimpanzee population, and several questions that remain to be addressed. In the spirit of the Japanese approach to science, I recommend that an interdisciplinary and collaborative research approach can best help us to challenge perceptions of human uniqueness and to further our understanding of chimpanzee behavioural and social flexibility in the face of local social, ecological and anthropogenic changes and threats to their survival.
Rust, N., MacMillan, D., Tzanopoulos, J. and Humle, T. (2016). Why Has Human–Carnivore Conflict Not Been Resolved in Namibia?. Society & Natural Resources [Online] 29:1079-1094. Available at: http://dx.doi.org/10.1080/08941920.2016.1150544.
Human–wildlife conflict has historically been portrayed as a management problem where solutions lie in technical changes or financial incentives. However, recent research shows many conflicts stem from social, economic, and political drivers. We undertook qualitative data collection on livestock farms to determine whether relationships between farmers and their workers affected frequency of reported livestock depredation in Namibia. We found that the conflict was affected by social and economic inequalities embedded in the previous apartheid regime. Macro- and microlevel socioeconomic problems created an environment where livestock depredation was exacerbated by unmotivated farm workers. Poor treatment of workers by farmers resulted in vengeful behaviors, such as livestock theft and wildlife poaching. Successfully addressing this situation therefore requires recognition and understanding of its complexity, rather than reducing it to its most simplistic parts
Hockings, K., Bryson-Morrison, N., Carvalho, S., Fujisawa, M., Humle, T., McGrew, W., Nakamura, M., Ohashi, G., Yamanashi, Y., Yamakoshi, G. and Matsuzawa, T. (2015). Tools to tipple: ethanol ingestion by wild chimpanzees using leaf-sponges. Royal Society open science [Online] 2:150150-150150. Available at: http://dx.doi.org/10.1098/rsos.150150.
African apes and humans share a genetic mutation that enables them to effectively metabolize ethanol. However, voluntary ethanol consumption in this evolutionary radiation is documented only in modern humans. Here, we report evidence of the long-term and recurrent ingestion of ethanol from the raffia palm (Raphia hookeri, Arecaceae) by wild chimpanzees (Pan troglodytes verus) at Bossou in Guinea, West Africa, from 1995 to 2012. Chimpanzees at Bossou ingest this alcoholic beverage, often in large quantities, despite an average presence of ethanol of 3.1% alcohol by volume (ABV) and up to 6.9% ABV. Local people tap raffia palms and the sap collects in plastic containers, and chimpanzees use elementary technology—a leafy tool—to obtain this fermenting sap. These data show that ethanol does not act as a deterrent to feeding in this community of wild apes, supporting the idea that the last common ancestor of living African apes and modern humans was not averse to ingesting foods containing ethanol.
Wich, S., Garcia-Ulloa, J., Kühl, H., Humle, T., Lee, J. and Koh, L. (2014). Will Oil Palm’s Homecoming Spell Doom for Africa’s Great Apes?. Current Biology [Online] 24:1659-1663. Available at: http://dx.doi.org/10.1016/j.cub.2014.05.077.
Expansion of oil palm plantations has led to extensive wildlife habitat conversion in Southeast Asia [ 1 ]. This expansion is driven by a global demand for palm oil for products ranging from foods to detergents [ 2 ], and more recently for biofuels [ 3 ]. The negative impacts of oil palm development on biodiversity [ 1, 4, 5 ], and on orangutans (Pongo spp.) in particular, have been well documented [ 6, 7 ] and publicized [ 8, 9 ]. Although the oil palm is of African origin, Africa’s production historically lags behind that of Southeast Asia. Recently, significant investments have been made that will likely drive the expansion of Africa’s oil palm industry [ 10 ]. There is concern that this will lead to biodiversity losses similar to those in Southeast Asia. Here, we analyze the potential impact of oil palm development on Africa’s great apes. Current great ape distribution in Africa substantially overlaps with current oil palm concessions (by 58.7%) and areas suitable for oil palm production (by 42.3%). More importantly, 39.9% of the distribution of great ape species on unprotected lands overlaps with suitable oil palm areas. There is an urgent need to develop guidelines for the expansion of oil palm in Africa to minimize the negative effects on apes and other wildlife. There is also a need for research to support land use decisions to reconcile economic development, great ape conservation, and avoiding carbon emissions.
Humle, T., Duffy, R., Roberts, D., Sandbrook, C., St. John, F. and Smith, R. (2014). Biology’s drones: undermined by fear. Science [Online] 344:1351-1351. Available at: http://dx.doi.org/10.1126/science.344.6190.1351-a.
Kormos, R., Kormos, C., Humle, T., Lanjouw, A., Rainer, H., Victurine, R., Mittermeier, R., Diallo, M., Rylands, A. and Williamson, E. (2014). Great Apes and Biodiversity Offset Projects in Africa: The Case for National Offset Strategies. PLoS ONE [Online] 9:e111671. Available at: http://dx.doi.org/10.1371/journal.pone.0111671.
The development and private sectors are increasingly considering “biodiversity offsets” as a strategy to compensate for their negative impacts on biodiversity, including impacts on great apes and their habitats in Africa. In the absence of national offset policies in sub-Saharan Africa, offset design and implementation are guided by company internal standards, lending bank standards or international best practice principles. We examine four projects in Africa that are seeking to compensate for their negative impacts on great ape populations. Our assessment of these projects reveals that not all apply or implement best practices, and that there is little standardization in the methods used to measure losses and gains in species numbers. Even if they were to follow currently accepted best-practice principles, we find that these actions may still fail to contribute to conservation objectives over the long term. We advocate for an alternative approach in which biodiversity offset and compensation projects are designed and implemented as part of a National Offset Strategy that (1) takes into account the cumulative impacts of development in individual countries, (2) identifies priority offset sites, (3) promotes aggregated offsets, and (4) integrates biodiversity offset and compensation projects with national biodiversity conservation objectives. We also propose supplementary principles necessary for biodiversity offsets to contribute to great ape conservation in Africa. Caution should still be exercised, however, with regard to offsets until further field-based evidence of their effectiveness is available.
Fragaszy, D., Biro, D., Eshchar, Y., Humle, T., Izar, P., Resende, B. and Visalberghi, E. (2013). The fourth dimension of tool use: temporally enduring artefacts aid primates learning to use tools. Philosophical Transactions of the Royal Society B: Biological Sciences [Online] 368. Available at: http://dx.doi.org/10.1098/rstb.2012.0410.
All investigated cases of habitual tool use in wild chimpanzees and capuchin monkeys include youngsters encountering durable artefacts, most often in a supportive social context. We propose that enduring artefacts associated with tool use, such as previously used tools, partly processed food items and residual material from previous activity, aid non-human primates to learn to use tools, and to develop expertise in their use, thus contributing to traditional technologies in non-humans. Therefore, social contributions to tool use can be considered as situated in the three dimensions of Euclidean space, and in the fourth dimension of time. This notion expands the contribution of social context to learning a skill beyond the immediate presence of a model nearby. We provide examples supporting this hypothesis from wild bearded capuchin monkeys and chimpanzees, and suggest avenues for future research.
Yamamoto, S., Humle, T. and Tanaka, M. (2013). Basis for Cumulative Cultural Evolution in Chimpanzees: Social Learning of a More Efficient Tool-Use Technique. PLoS ONE [Online] 8:e55768. Available at: http://dx.doi.org/10.1371/journal.pone.0055768.
Background: The evidence for culture in non-human animals has been growing incrementally over the past two decades. However, the ability for cumulative cultural evolution, with successive generations building on earlier achievements, in non-human animals remains debated. Faithful social learning of incremental improvements in technique is considered to be a defining feature of human culture, differentiating human from non-human cultures. This study presents the first experimental evidence for chimpanzees' social transmission of a more efficient tool-use technique invented by a conspecific group member. Methodology/Principal Findings: The chimpanzees were provided with a straw-tube, and spontaneously demonstrated two different techniques in obtaining juice through a small hole: "dipping" and "straw-sucking". Both the "dipping" and "straw-sucking" techniques depended on the use of the same tool (straw-tube) for the same target (juice) accessible from exactly the same location (small hole 1 cm in diameter). Therefore the difference between "dipping" and "straw-sucking" was only in "technique". Although the two techniques differed significantly in their efficiency, their cognitive and perceptuo-motor complexity were comparable. All five chimpanzees who initially performed the "dipping" technique switched to using the more efficient "straw-sucking" technique upon observing a conspecific or human demonstrate the more proficient alternate "straw-sucking" technique. Conclusions/Significance: The social learning mechanism involved here was clearly not local or stimulus enhancement, but imitation or emulation of a tool-use technique. When there is no biologically relevant difference in cognitive or perceptuo-motor complexity between two techniques, and when chimpanzees are dissatisfied with their own technique, chimpanzees may socially learn an improved technique upon close observation of a proficient demonstrator. This study provides important insights into the cognitive basis for cumulative culture in chimpanzees, and also suggests possible conditions in which cumulative cultural evolution could arise even in non-human animals.
Ongman, L., Colin, C., Raballand, E. and Humle, T. (2013). The "Super Chimpanzee": The ecological dimensions of rehabilitation of orphan chimpanzees in Guinea, West Africa. Animals [Online] 3:109-126. Available at: http://dx.doi.org/10.3390/ani3010109.
To date few studies, especially among non-human primates, have evaluated or monitored rehabilitation effectiveness and identified key species-specific behavioral indicators for release success. This four-months study aimed to identify behavioral indicators of rehabilitation success among ten infant and juvenile orphaned chimpanzees cared for in peer groups at the Centre for Conservation of Chimpanzees (CCC), Guinea, West Africa. Behavioral data focused on foraging skills and activity budget. During bush-outings, rehabilitants spent on average nearly a quarter of their activity budget foraging, resting or traveling, respectively. Neither age, sex, the level of abnormal behaviors demonstrated upon arrival nor human contact during bush-outings predicted individual dietary knowledge. However, individuals who spent more time arboreal demonstrated a greater dietary breadth than conspecifics who dwelled more terrestrially. Although our data failed to demonstrate a role of conspecific observation in dietary acquisition, we propose that the mingling of individuals from different geographical origins may act as a catalyst for acquiring new dietary knowledge, promoted by ecological opportunities offered during bush-outings. This "Super Chimpanzee" theory opens up new questions about cultural transmission and socially-biased learning among our closest living relatives and provides a novel outlook on rehabilitation in chimpanzees.
Humle, T., Garriga, R., Cuadrado, L., Rankin, E., Marco, I., Casas-Díaz, E., Acevedo, P., Colin, C. and Amarasekaran, B. (2019). Understanding The Impacts Of Deforestation And Road Infrastructure Development On Chimpanzees Outside Protected Areas. In: 8th European Federation for Primatology Meeting. Karger. Available at: https://www.efp-psgb2019.com/Abstracts_EFP-PSGB2019.pdf.
The majority of the critically endangered chimpanzees (Pan troglodytes verus) occur outside protected areas. Ensuring their long-term survival in such areas implies addressing people-chimpanzee coexistence challenges. Using origin data of confiscated chimpanzees from two chimpanzee sanctuaries in West Africa, i.e. the Chimpanzee Conservation Center (CCC), Guinea and the Tacugama Chimpanzee Sanctuary, Sierra Leone, and forest loss data from 2001 to 2015, we highlight how deforestation exacerbates interactions between people-chimpanzees and acts as a driver for the killing and capture of chimpanzees in the region. Finally, we present results from a systematic camera trapping survey (24 camera traps deployed across 27 1.25x1.25 km grids) conducted in the Moyamba district in south-western Sierra Leone in an area dominated by subsistence agricultural activities and practically devoid of forest. We employed a hierarchical Bayesian framework accounting for spatial autocorrelation to explore ecological and anthropogenic factors influencing chimpanzee relative abundance across the landscape. Our findings revealed that chimpanzees in such landscapes, where people are relatively tolerant of their presence, tend to avoid roads, including untarmacked secondary roads, and prefer to range in close proximity to more intact habitats such as swamps. Unexpectedly, they showed no preference for abandoned settlements where fruit orchard persist. Finally, although chimpanzees in this area did not avoid human settlements or areas frequented by people, areas of spatial overlap between the two species revealed temporal divergence in utilization. Altogether, these studies emphasize the urgent need to understand better factors that influence chimpanzee abundance and distribution outside protected areas, especially in the context of the rate of forest loss, and for aligning land use planning and infrastructure development to serve both the needs of people and chimpanzees.
Cuadrado, L., Garriga, R., Amarasekaran, B. and Humle, T. (2019). UAV Technology as an Effective Tool to Assess Chimpanzee Abundance in Degraded Landscapes. In: 8th European Federation for Primatology Meeting. Karger. Available at: https://www.efp-psgb2019.com/Abstracts_EFP-PSGB2019.pdf.
Estimating population size and density of a population of a species are essential to inform conservation management strategies and land-use planning. However, some landscapes dominated by fallow areas pose great challenges when it comes to traditional transect surveys. Unmanned aerial vehicle (UAV) and camera trapping technologies have demonstrated great potential when it comes to surveying wildlife. In this study, we employed camera trapping in combination with spatially explicit capture-recapture (SECR) models for estimating chimpanzee (Pan troglodytes verus) numbers in a non-protected area in the Moyamba district in south-western Sierra Leone, ca. 90 square kilometres. We estimated trapping rate per 1.25 km square grids across the target area based on a systematic layout of camera traps (N=30). In this environment practically devoid of forest, chimpanzees only nest in semi-domesticated oil palms (Elaeis guineensis) which are prevalent in the landscape. Due to the nesting specificity of the chimpanzees in this area, we were readily able to estimate nest density per grid and across the entire target area using drone imagery based on a sampling regime of 3 missions (200 meter square each) within each sample grid. We compared these abundance estimates with those generated from the SERC model and individual chimpanzee identification. Our study reveals that drone imagery data yields equivalent results and can effectively estimate chimpanzee population parameters across such degraded landscapes. The application of UAV technology in such environments can serve to inform conservation and land-use planning for chimpanzees, especially in areas prone to infrastructure and industrialized agricultural development.
Bryson-Morrison, N., Beer, A., Matsuzawa, T. and Humle, T. (2017). Sex Differences, Seasonality, and Macronutrient Balancing in the Diet of Chimpanzees Inhabiting a Forest-Agricultural Mosaic. In: 7th Congress of the European Federation of Primatology. Karger. Available at: https://www.karger.com/Article/PDF/479094.
Many primates face spatial and temporal fluctuations in food availability, which can significantly affect their ability to meet nutritional requirements. Anthropogenic disturbances and influences, such as agriculture, human presence and infrastructures, can further impact seasonal food availability, dietary composition and nutrition. Primates residing in anthropogenic landscapes often incorporate cultivars into their diets. However, the nutritional drivers behind cultivar consumption are poorly understood. We examined variations in chimpanzee (Pan troglodytes verus) macronutrient intake from wild and cultivated foods between sexes and seasons over a 1year period in Bossou, Guinea. We used the geometric framework of nutrition to examine proportional contributions of macronutrients to the diet and nutrient balancing. We conducted
continuous focal observations of adult individuals ( n = 10) to record all feeding bouts and conducted nutritional analyses of plant foods (25 wild species; 11 cultivated species). We found no sex differences in chimpanzees for wild or cultivated food or macronutrient intakes; however, females showed higher intakes of total food (i.e. wild and cultivated combined), digestible fibre (NDF), and protein when controlling for metabolic body mass. There were no differences in wild or cultivated food intake between seasons; however, lipid and protein intake from cultivars were higher when wild fruit availability was low. Chimpanzees maintained a constant proportional intake of protein while allowing carbohydrates and lipid intakes to vary. Furthermore, they were
able to maintain a consistent balance of protein to non-protein (carbohydrates, lipids, and NDF) energy across the year. Our results suggest that Bossou chimpanzees suffered little seasonal constraints in food quality or availability since they were able to combine their consumption of available wild and cultivated foods to achieve a balanced diet. These findings contribute significantly to our understanding of primate nutritional requirements and their ability to meet these in disturbed environments.
Neufuss, J., Robbins, M., Baeumer, J., Humle, T. and Kivell, T. (2017). Comparison of Hand Use and Forelimb Mechanics of Vertical Climbing in Wild Mountain Gorillas and Free-Ranging Chimpanzees. In: 7th European Federation for Primatology Meeting. Available at: https://www.karger.com/Article/PDF/479094.
Biomechanical analyses of great ape arboreal locomotion in a natural environment are scarce, thus limiting attempts to correlate behavioural and habitat differences with variation in skeletal morphology. Vertical climbing is a crucial locomotor and foraging strategy of great apes and the hands are critically important to maintaining stability on irregular, arboreal substrates. However, little is known about arboreal grips and hand postures, or how these might vary with forelimb posture during vertical climbing on natural substrates of different sizes. This is particularly true of mountain gorillas, which are considered the least arboreal of all African apes and for which the characteristics of vertical climbing have not yet been studied. The aim of this study was to compare temporal kinematics of hand and forelimb use during vertical climbing in wild, habituated mountain gorillas (Gorilla beringei beringei) of the Bwindi Impenetrable Forest (Uganda) and sanctuary chimpanzees (Pan troglodytes) of the Chimfunshi Wildlife Orphanage Trust (Zambia) to assess differences in climbing styles that may relate to variation in hand or forelimb morphology and body mass. We investigated hand and forelimb posture coupled with temporal gait parameters during vertical climbing (both ascent and descent) in 15 mountain gorillas and eight chimpanzees, using video records ad libitum. In both apes, forelimb posture was correlated with substrate size during both ascent and descent climbing. Both apes used power grips and a diagonal power grip, involving three different thumb postures. Gorillas showed greater ulnar deviation of the wrist during climbing than chimpanzees, and the thumb played an important supportive role when vertically descending compliant substrates in gorillas. Comparisons of temporal gait parameters indicated that large-bodied gorillas exhibited significant longer cycle duration, lower stride frequency and generally a higher duty factor than chimpanzees. This study revealed that wild mountain gorillas adapt their climbing strategy to accommodate their large body mass in a similar manner found in captive western lowland gorillas, but that our sanctuary chimpanzees showed less variation in their climbing strategy within a natural environment than has been documented in captive bonobos
Neufuss, J., Humle, T., Deschner, T., Robbins, M., Sirianni, G., Boesch, C. and Kivell, T. (2015). Diversity of Hand Grips and Laterality in Wild African Apes. In: 6th European Federation for Primatology Meeting, XXII Italian Association of Primatology Congress. KARGER, pp. 329-329. Available at: http://dx.doi.org/10.1159/000435825.
Comparative studies of primate grasping and manipulative behaviours in captivity have
highlighted, among others, two human abilities that are generally considered unique compared
with other primates: (1) the use of forceful precision and power squeeze grips involving the use
of the thumb, and (2) a species-wide dominant use of one hand (usually the right hand), known
as laterality. However, recent research has highlighted a diversity of precision and power grips in
general among many non-human primates, and there is much debate around the potential for
population-level or species-wide laterality in non-human primates. The majority of this research
to date has been done on captive primates performing specific manipulative tasks, which may
bias or confound these species comparisons. Comparatively little research has been done on hand
use in wild primates, especially during natural, non-manipulative activities, including locomotion.
Here, we investigate hand use during locomotor and non-locomotor behaviours in wild
mountain gorillas ( Gorilla beringei beringei , Bwindi Impenetrable National Park, Uganda), wild
chimpanzees ( Pan troglodytes verus , Taï National Park, Cote d’Ivoire) and chimpanzees kept under
semi-natural conditions ( Pan troglodytes ssp., Chimfunshi Wildlife Trust, Zambia). Preliminary
results propose that hand grips are similar between gorillas and chimpanzees during the
manipulation of common object types. Bwindi gorillas show various hand use strategies during
the processing of several plant foods. Chimfunshi chimpanzees also use forceful precision grips
during daily manipulative tasks, suggesting that this is not a uniquely human ability.
Humle, T. and Konate, A. (2015). Primates and Bushmeat Hunting Around the High Niger National Park, Guinea, West Africa: Drivers and Patterns of Change. In: 6th European Federation for Primatology Meeting, XXII Italian Association of Primatology Congress. pp. 298-298. Available at: http://www.dx.doi.org/ 10.1159/000435825.
Bushmeat hunting contributes to the decline of primate species across Africa; however, few
studies have explored how such practises change over time in specific localities and how changes
in land-use patterns and economic drivers may enhance threats to primates in Muslim dominated
areas where, traditionally, primates are spared from such trade. The Haut Niger National
Park (HNNP) is one of only two national parks in the Republic of Guinea. The park is one of the
last remaining important formations of dry forest-savannah mosaics in West Africa and is a site
of high conservation priority for ungulates and the western subspecies of chimpanzee. This study
aimed to: (1) estimate the diversity and abundance of animal species sold for consumption across
several markets in and around the HNNP, (2) analyse the evolution of the bushmeat trade since
the mid-1990s, and (3) identify the players and drivers of the commercial bushmeat trade in the
area. Local market assessments were conducted across four village markets and in Faranah, one
of the closest urban areas abutting the HNNP. We successfully identified 5,807 wildlife carcasses
of 46 species and 22 families on markets surveyed over a 7 month period spanning both the dry
and wet seasons. In addition, semi-structured interviews with hunters, farmers and people involved
in the bushmeat trade helped identify more recent drivers of the bushmeat trade in the
HNNP. Our results indicated an increase in diversity of species targeted and the influence of
crop-foraging and local microcredit systems in exacerbating the presence of primate species sold
at bushmeat stalls in urban areas. Finally, whilst identifying key recommendations and gaps for
future research, this study emphasises the growing risks facing primates as targets for bushmeat
where people depend on agriculture and natural resource extraction for subsistence. This study
complied with the International Primatological Society (IPS) Guidelines for the Use of Nonhuman
Primates in Research.
Humle, T., Garriga, R., McKenna, A. and Amarasekaran, B. (2014). The interface between wild chimpanzee culture, land use management and agricultural development: the case of the oil palm. In: International Primatological Society, 25th Congress. Available at: http://www.internationalprimatologicalsociety.org/meetings.cfm.
The oil palm (Elaeis guineensis) is a common and sometimes predominant feature of many West African landscapes. In countries such as Guinea and Sierra Leone, wild or feral oil palms often dominate fallow and cultivated fields, as well as abandoned or recent human settlements; they also thrive in gallery and secondary forests. We will highlight here the extent to which wild chimpanzees differ in their cultural use and dependence on the oil palm. Across Africa, many wild chimpanzee communities make use of oil palm parts for feeding and nesting purposes. People also traditionally depend on the oil palm for a range of purposes including among others cooking, soap and wine making and construction for both subsistence and commercial purposes. Increasing global demand for oil palm is rapidly changing the landscape to include both large and small scale plantations. We used data gathered as part of a nationwide survey of chimpanzees as well as from more focused studies in areas reporting high levels of human-wildlife interactions to assess 1) the extent of competition in the use of oil palm between people, chimpanzees and other wildlife and 2) relative perceptions concerning competition for the oil palm between chimpanzees and people. We discuss the implication of these patterns with respect to land use management and agricultural development in West Africa.
Humle, T., Colin, C., Danaud, C., Laurans, M. and Raballand, E. (2014). Post-release monitoring of chimpanzees in Guinea, West Africa. In: International Primatological Society, 25th Congress. Available at: http://www.internationalprimatologicalsociety.org/meetings.cfm.
Great ape rehabilitation centres across Africa continue to witness an increase in residents, often orphans of the bushmeat and pet trade or victims of people’s intolerance towards sharing resources and space with their closest living relatives. As wild populations decline, releasing individuals back to the wild is increasingly perceived as a viable conservation option. However, few projects have ever released African Great Apes successfully, and information on predictors of rehabilitation and release success remain scarce. The Chimpanzee Conservation Center (CCC) in the High Niger National Park is the only sanctuary caring for chimpanzee orphans in Guinea, West Africa. In 2008, in view to reinforce the wild chimpanzee population of the HNNP and to enhance park protection, the CCC released 6 male and 6 female chimpanzees into the main core area of the park. Five of those individuals have since settled at the release site and continue to be monitored. In 2011, the CCC successfully added 2 adult females to this resident group. Post-release monitoring of released individuals involves distance monitoring using simple VHF and/or ARGOS and GPS store-on-board radio collars. GIS data generate information on release individuals’ social dynamics, habitat preferences, day and home range use. Our results highlight the costs and benefits of employing different post-monitoring tracking technologies and how these act to inform release success.
Soumah, A., Humle, T. and Matsuzawa, T. (2014). Oil Palm Use Among the People and Wild Chimpanzes of Bossou, Guinea, West Africa. In: International Primatological Society, 25th Congress. Available at: http://www.internationalprimatologicalsociety.org/meetings.cfm.
The oil palm (Elaeis guineensis) originated in West Africa and occurs widely across large expanses of landscape, as well as more widely across Central and Eastern Africa. In Guinea, West Africa, the oil palm can be found commonly across vast mosaics of fallow areas, cultivated fields, riverine areas, forest fragments and around human settlements. Where it occurs, this palm species appears to act as a keystone resource for both people and chimpanzees; chimpanzee communities across West Africa may use the oil palm for nesting and/or for feeding purposes, while it provides people with numerous products of immense domestic and commercial value. One particular well known example of such sympatry where resource sharing of the oil palm has been well documented is the long term chimpanzee field site of Bossou in Southeastern Guinea. In this study, we surveyed regularly over the course of a period of 2 years, 200 oil palms located at the forest edge in the core area of the Bossou chimpanzee community. We recorded evidence of use among both people and chimpanzees to evaluate the impact on palm productivity and survival. Finally, we argue that people and chimpanzee in the locality effectively share this common resource and to date in cultural ways that favor co-existence.
Vanlangendonck, N., Colin, C., Laurans, M., Raballand, E. and Humle, T. (2013). The Socio-Ecological Adaptation of Released Chimpanzees in Guinea, West Africa. In: 5th Congress of the European Federation for Primatology. Karger. Available at: https://www.eva.mpg.de/documents/Karger/Crockford_Chimpanzees_FoliaPrim_2013_1840658.pdf.
Throughout their range across Africa, chimpanzees (Pan troglodytes) are threatened with
extinction due to habitat destruction, disease and unsustainable levels of hunting and capture, in spite of being protected by national and international laws. In recent years, the bush meat and the pet trade have resulted in a significant increase in the number confiscated orphan chimpanzees. The Chimpanzee Conservation Centre (CCC), located in the High Niger National Park (HNNP), is the only Pan African Sanctuary Alliance (PASA)-accredited sanctuary caring for chimpanzee orphans in Guinea, West Africa. This sanctuary has been rehabilitating confiscated chimpanzees since 1997. With the aim of reinforcing the wild chimpanzee population of the HNNP and to enhance park protection, the CCC, in 2008, released a first group of 12 chimpanzees into the Mafou core area of the park. Five of those individuals have since settled at the release site and continue to be monitored. In August 2011, the CCC was able to re-enforce this resident group with the successful addition of 2 adult females. Post-release monitoring of these individuals involved distance monitoring using simple VHF and/or ARGOS and GPS store-on-board radio collars. Here, we present data downloaded in 2011–2012 from the GPS store-on-board collars of 2 adult males and these 2 additional adult females. These data allowed us to analyse their social dynamics, party composition, habitat preferences, day range and home range use. Our results indicate that these females integrated successfully into the resident group and that the behaviour of these wild-born released orphan chimpanzees mirrors that of wild counterparts inhabiting similar savannah dominated landscapes, suggesting that they have adapted appropriately to their release conditions.
Humle, T., von Cramon-Taubadel, N. and Lycett, S. (2013). The Bootstrapping Dimensions of Culture in Chimpanzees. In: 5th Congress of the European Federation for Primatology. pp. 289-289. Available at: http://dx.doi.org/10.1159/000354129.
Vanlangendonck, N., Guttierrez-Espeleta, G. and Humle, T. (2013). Assessment of the Consequences of Anthropogenic Pressures on Alouatta palliata and Ateles geoffroyi Physiology in Northern Costa Rica. In: 5th Congress of the European Federation for Primatology. Karger, pp. 340-340. Available at: http://dx.doi.org/10.1159/000354129.
Previous studies have shown a positive relationship between proximity to humans or habitat fragmentation and parasitic levels in non-human primates (NHPs). However, to date few have explicitly explored links between parasite load and stress conditions. To better understand the links between parasite prevalence and NHP immune system efficiency and stress levels, faecal samples of Alouatta palliata and the critically endangered Ateles geoffroyi geoffroyi were non-invasively collected in northern Costa Rica. We investigated whether the presence of gastrointestinal parasites was related to the abundance of hormones (cortisol and testosterone). Samples were gathered across three areas differing in the frequency and diversity of human presence, i.e. around the Caño Palma Biological Station, near villages and at ecotourism sites. Two grams of each faecal sample were stored in a sugar saturated solution with 10% formalin to conserve the parasites; the remaining matter was dried to preserve DNA and steroid hormones. The samples enabled the quantification of parasites as well as testosterone and cortisol levels using ELISA as proxies of general health status and stress levels. Data on parasite abundance and hormone levels were contrasted across the two species and the three different sampling areas. Furthermore, we assessed the genetic exchange among the different groups of primates sampled. We genetically analysed the samples using 12 microsatellites previously validated by the University of Costa Rica. We verified whether transmission of parasites among the groups could be possible concomitant to the genetic exchange. This study aimed to better understand and assess the impact of human factors on NHP health and across NHPs with different socio-ecological characteristics.
Bryson-Morrison, N. (2017). Habitat Use and Nutrition of Chimpanzees in an Anthropogenic Landscape: A Case Study in Bossou, Guinea, West Africa.
Human population increases and an expanding agricultural frontier are driving tropical deforestation. As a result, many primates are increasingly found outside of protected areas in highly-disturbed environments in close proximity to humans. A better understanding of primate species adaptability to human pressures and the ability of anthropogenic landscapes to support viable populations in the long-term is critical for effective conservation efforts. By focusing on the chimpanzee (Pan troglodytes verus) community in the anthropogenic landscape of Bossou, Guinea, West Africa, I aimed to 1) empirically describe the composition and availability of chimpanzee resources across fine spatial scales, 2) examine chimpanzee use and activity budget across available habitat types and in relation to anthropogenic pressures and risks, 3) determine the macronutrient composition of wild and cultivated chimpanzee foods, and 4) investigate chimpanzee macronutrient intake and balancing from wild and cultivated foods.
To examine objective 1, I undertook quadrat vegetation surveys and phenology surveys to spatially and temporally quantify chimpanzee food resources in all available habitat types. Bossou is largely composed of regenerating forest and the scarcity of large fruit bearing trees is offset by a high diversity of wild and cultivated chimpanzee food species. Moraceae (mulberries and figs) is the dominant family, trees of which produce drupaceous fruits favoured by chimpanzees. The oil palm, which provides the chimpanzees with year-round food resources, occurs at high densities throughout Bossou. Mature and secondary forests are the most important habitat types for food species availability. Overall, these results emphasise the importance of examining ecological characteristics of an anthropogenic landscape as each available habitat type is unlikely to be equally important in terms of spatial and temporal availability of resources.
To examine objective 2, I conducted behavioural follows to record chimpanzee activities and habitat use across all forest and highly disturbed habitat types, and foraging locations in non-cultivated habitat in relation to anthropogenic pressures i.e. cultivated fields and roads and paths. Chimpanzees preferentially use forest habitat types for travelling and resting and highly disturbed habitat types for socialising. The availability of wild fruit and crops influences seasonal habitat use for foraging. The chimpanzees rely heavily on a small patch of mature forest, rich in food species and with low human presence, irrespective of season and activity. The chimpanzees avoid foraging in non-cultivated habitat within 200 m of cultivated fields, with no effect of habitat type or season, suggesting an influence of associated risk. Nevertheless, they did not actively avoid foraging close to roads and paths. These results reveal chimpanzee reliance on different habitat types and the influence of human-induced pressures on their activities.
To examine objective 3, I used standard wet chemistry procedures to estimate the macronutrient content of wild and cultivated chimpanzee foods. The composition of wild fruit, leaves and pith are consistent with previous reports for primate diets. Cultivars are generally higher in carbohydrates and lower in fibre than wild foods, while wild foods are higher in protein. Oil palm food parts are rich in energy, carbohydrates, protein, lipids and/or fermentable fibre fractions; adding nutritional support for the importance of oil palms for chimpanzees in anthropogenic landscapes. These results build on current understanding of chimpanzee feeding ecology and nutrition within forest-agricultural mosaics and provide further empirical evidence that cultivars offer primates energetic benefits over most wild plant foods.
To examine objective 4, I used the macronutrient composition of foods and recorded chimpanzee intakes of wild and cultivated foods during focal follows. Diet composition and macronutrient intakes vary little between the sexes; however females have higher total foods (i.e. wild and cultivated combined), digestible fibre (NDF), and protein intakes when controlling for metabolic body mass. There are no differences in wild or cultivated food intake between seasons; however lipid and protein intake from cultivars, and most likely oil palm food parts, is higher during the fruit scarce season. The chimpanzees maintain their proportional intake of protein while allowing carbohydrate and lipid intakes to vary. Furthermore, they were able to achieve a consistent balance of protein to non-protein (carbohydrates, lipids, and NDF) energy across the year. These results suggest the chimpanzees suffer little seasonal constrains in food quality or availability and are able to combine their consumption of available wild and cultivated foods to achieve a balanced diet.
Overall, this thesis provides new insights into the ecology of anthropogenic landscapes, the influence of human pressures on chimpanzee habitat use and behaviours, and the role of cultivars in chimpanzee foraging strategies and in allowing them to meet their nutritional requirements. Such information is important for informing conservation initiatives aimed at balancing the needs of people and chimpanzees that share space and resources within anthropogenic landscapes.
Moss, A. (2017). The Educational Value of Zoos and Aquariums.
Zoos and aquariums are some of the most-visited institutions, with around 700 million visits made to them globally each year. They are, in a basic sense, simply repositories of living biodiversity. However, the justifications for the continued existence of zoos have evolved since their inception in the late 18th and early 19th centuries, and nearly all now position themselves as organisations focussed on the conservation of the world's remaining biodiversity. Public education of visitors is seen as, and is claimed to be, a central role in achieving this mission. Until relatively recently, very little was known about the impacts of zoo-based education. In this thesis, I will argue that good, progressive zoos and aquariums can and do achieve positive educational impacts on the people that visit them. Using a combination of structured observational methods and traditional social survey designs, I have explored the relative popularity of zoo animals, assessed the tolerance of zoo visitors to different environmental education themes, and have conducted the first fully global evaluation of zoo education impacts. In brief, I found that taxonomic group (mammals), increasing body size and activity levels were significant predictors of visitor interest in zoo animals, giving zoo professionals an evidence base to make decisions regarding education programming and exhibit design. Zoo visitors were also found to be, in the main, accepting to education content that reached beyond animal-based themes. This gives zoo educators the evidence to support their efforts to design and deliver more diverse programmes that cover wider environmental education themes. Finally, from a global survey of more than 5,000 visitors to 26 zoos and aquariums, I concluded that people tend to end their visit with a significantly greater understanding of what biodiversity is, as well as the ways that they personally can help protect it. The links between these two knowledge strands were, however, found to be less strong than predicted, leading to a discussion around the significance of the role of knowledge in catalysing human behaviour change. Aside from demonstrating their own positive educational impact, the wider implication of this research is that zoos and aquariums can also show that they are helping to achieve global biodiversity targets; namely, UN Aichi Biodiversity Target 1. From this, I will argue that the educational role of zoos should be considered as a more influential contributor to biodiversity conservation, and society more generally, than has previously been accepted.
Neufuss, J. (2017). Hand Use and Posture During Manipulative Behaviours and Arboreal Locomotion in African Apes.
The skill with which primates use their hands to explore and interact with the environment sets them apart from most other mammals. The non-human primate hand serves an important functional role during not only terrestrial and arboreal locomotion, but also enhanced grasping and manipulative behaviours. Understanding how living primates use their hands for these various functions is fundamental for understanding the order Primates and the evolution of humans within this order. While bipedalism and the extraordinary manipulative abilities of our human hand for manufacturing stone tools are considered to be unique, their origins remain controversial. Understanding this evolutionary shift in human hand use from locomotion to manipulation requires comparative studies of hand use in our closest living relatives, the African apes (chimpanzees, bonobos and gorillas). To date, however, little research has been done on African ape daily hand use, including both locomotor and manipulative behaviours, especially in natural environments. This dissertation will address this gap by conducting detailed studies of hand use and posture during two complex manipulative behaviours (i.e., plant-processing, nut-cracking) and arboreal locomotion (i.e., vertical climbing) in the natural environment of African apes.
I conducted the first comprehensive analysis of bonobo palm oil nut-cracking in a natural environment at the Lola ya Bonobo sanctuary, Democratic Republic of the Congo. All eighteen bonobos showed exclusive laterality for using the hammerstone and there was a significant group-level right-hand bias. The study revealed 15 hand grips for holding differently-sized and -weighted hammerstones, 10 of which had not been previously described in the literature. The findings also demonstrated that bonobos select the most effective hammerstones when nut-cracking and that bonobos, despite rarely using tools in the wild, can be efficient nut-crackers with a skill level that is similar to palm oil nut-cracking chimpanzees of Bossou, Guinea.
I further provided the first insights into the manual skills of Bwindi mountain gorillas by examining hand-use strategies, hand grips, and hand-preference (i.e., laterality) during the processing of three different plants. Two of these plants are woody-stemmed plants for which the food is more challenging to access in comparison to leaves, lacking physical defenses that are relatively simple to process. Bwindi gorillas used the greatest number of hand actions to process the most complex plant food (i.e., peel-processing) similar to complex thistle feeding by Virunga mountain gorillas. The manipulative actions were ordered in several key stages organised hierarchically. The demands of manipulating natural foods elicited 19 different hand grips and variable thumb postures, of which three grips were new and 16 grips have either been previously reported or show clear similarities to grips used by other wild and captive African apes and humans. A higher degree of lateralisation was elicited for the most complex behaviour of peel-processing but the strength of laterality was only moderate, suggesting that peel-processing is not as complex as thistle leaf-processing by Virunga gorillas.
Finally, I examined for the first time hand use, forelimb posture and gait chacteristics during vertical climbing in wild, habituated mountain gorillas (Gorilla beringei) of the Bwindi Impenetrable National Park, Uganda, and semi-free-ranging chimpanzees (Pan troglodytes) of the Chimfunshi Wildlife Orphanage Trust, Zambia, both within a natural environment. This research revealed that both apes used power grips and a diagonal power grip, involving three different thumb postures. Gorillas showed greater ulnar deviation of the wrist during climbing than chimpanzees, and the thumb played an important supportive role when vertically descending compliant substrates in gorillas. Comparisons of temporal gait parameters showed that large-bodied gorillas exhibited significant longer cycle duration, lower stride frequency and generally a higher duty factor than chimpanzees. This quantitative analysis revealed that mountain gorillas adapt their climbing strategy to accommodate their large body mass in a similar manner found in captive western lowland gorillas, and that chimpanzees showed less variation in their climbing strategy than has been documented in captive bonobos. In summary, this study demonstrates the importance of forceful hand grips and the variable use of the thumb relative to substrate size in both ape species, and particularly in large-bodied mountain gorillas as they face more biomechanical challenges during vertical climbing than smaller-bodied chimpanzees.
Together, this dissertation provides new insights into the functional link between hand morphology and behaviour in African apes in their natural environments that may ultimately generate more informed reconstructions of fossil hominin locomotor and manipulative behaviours. Furthermore, this research shows that the suite of "unique human grips" or "unique human manipulative abilities" that have typically defined humans is getting much smaller the more we learn about African apes, particularly in their complex natural environment where the hand has to adjust to varying foods and arboreal substrates, and where individuals have ample opportunity to learn and develop high manipulative skills.
Rust, N. (2015). Understanding the Human Dimensions of Coexistence Between Carnivores and People: A Case Study in Namibia.
Many carnivore populations were in decline throughout much of the 20th century, but due to recent conservation policies, their numbers are stabilising or even increasing in
some areas of the world. This, compounded with human population growth, has caused increased livestock depredation by carnivores, which threatens farmer livelihoods, particularly those in developing countries such as Namibia. How to resolve this so-called “conflict” between carnivores and livestock farmers remains challenging, in part because some mitigation strategies have proven somewhat ineffective or unacceptable. By using a case-study approach on the commercial farmlands of northcentral Namibia, I aimed to understand the complexity of the human dimensions affecting coexistence between carnivores and people in an unprotected working landscape. Specifically, my objectives were to 1) develop a participatory decisionmaking exercise to analyse the views of stakeholders on how they would like carnivores to be managed in unprotected lands, 2) understand how the media framed
financial incentives to improve human-carnivore coexistence, and 3) determine if there were any underlying social, economic or political causes of negative human-carnivore
interactions on commercial livestock farms.
To answer objective 1, I developed a new decision-making exercise that combined Q-methodology and the Delphi technique to determine whether a diverse group of stakeholders could agree on how to manage carnivores on commercial farmland. A strong agreement was reached by participants: providing conservation education and training on livestock husbandry were acceptable and effective ways to improve coexistence with carnivores. This new also method highlighted areas of disagreement between stakeholders and showed that there were two different narratives on how carnivores should be managed. This method could be used by policy makers to help with participatory decision-making for resolving other
To answer objective 2, I undertook content analysis of national newspapers to determine how the media framed articles on financial incentives to mitigate this conservation conflict. The most common (30%) financial incentive discussed was compensation - many (61%) of these articles framed compensation positively.
However, upon categorising these articles into those where respondents were enrolled in compensation schemes compared with those who were not, a clear pattern emerged: articles were more likely (89%) to be framed ambivalently or negatively when respondents had experience of this financial incentive compared with respondents that did not. These results can help conservationists plan more effective communication interventions and anticipate issues that can affect the success of mitigation strategies.
To answer objective 3, I undertook eight months of participant observation on livestock farms and interviewed 69 respondents and found that reported livestock depredation was associated with increased instances of poaching of wildlife and stealing of livestock. This association appeared to be partly due to farmer-worker relations: when employees felt happy, respected and were paid a liveable wage, they were incentivised to perform well in their job. This resulted in livestock that were managed more effectively and therefore less likely to be killed by predators. Furthermore, these well-paid employees were not incentivised to steal or poach to supplement their income, which limited the extent of game poaching and livestock theft on the farm. These findings underline the fact that this conservation conflict is extremely complicated, driven by many social, economic and political factors that may not be apparent initially.
In conclusion, this thesis has found that the conflict between carnivores and livestock farmers is a truly wicked problem, affected by a multitude of complex layers.
Only by exploring the entangled web of drivers will we ever begin to create positive, lasting change for both people and predators. Niki Rust © 2015