Apes in fiction: does the content of novels reflect primatological knowledge?

Novels about great apes and humans continue to be consistently popular with the reading public, sometimes reaching best-seller status. Media reviews of these books rarely comment on their primatological roots, nor do primatological journals review them. In a non-quantitative, pilot study, I scrutinize six prominent novels, in terms of three questions: How do the novels make use of primatology? What aspects of primatology do they use? How accurate is their use of primatology? Such novels overwhelmingly concentrate on language, with intelligence and sexuality lagging far behind; other topics, such as culture or technology, receive little or no attention. Apes in nature are rarely mentioned. Inaccuracies abound, even at the most basic level of primatological knowledge that easily could be remedied. Both authors and primatologists would benefit from more informative interaction before publication.

Cumulative culture in nonhumans: overlooked findings from Japanese monkeys?

Cumulative culture, generally known as the increasing complexity or efficiency of cultural behaviors additively transmitted over successive generations, has been emphasized as a hallmark of human evolution. Recently, reviews of candidates for cumulative culture in nonhuman species have claimed that only humans have cumulative culture. Here, we aim to scrutinize this claim, using current criteria for cumulative culture to re-evaluate overlooked qualitative but longitudinal data from a nonhuman primate, the Japanese monkey (Macaca fuscata). We review over 60 years of Japanese ethnography of Koshima monkeys, which indicate that food-washing behaviors (e.g., of sweet potato tubers and wheat grains) seem to have increased in complexity and efficiency over time. Our reassessment of the Koshima ethnography is preliminary and nonquantitative, but it raises the possibility that cumulative culture, at least in a simple form, occurs spontaneously and adaptively in other primates and nonhumans in nature.

Non-dietary analytical features of chimpanzee scats.

Non-dietary aspects of ape scats such as scat weight and diameter are correlated with age and sex of defaecator for gorillas and orangutans. Defaecation rates of primates, including apes, illuminate their role as primary seed dispersers. We assess if non-dietary features of scats for East African chimpanzees (Pan troglodytes schweinfurthii) reveal such insights for members of the Kanyawara community in Kibale National Park, Uganda. Our objective is to see if such data yield useful perspectives for future census work on unhabituated chimpanzees, that is, what can scats tell us about a wild study population, beyond diet? We followed ten adults from this community, as well as travelling parties, comparing observed vs. unobserved defaecations, and collected data on scat weight and dimensions, defaecation rate, scat encounter rate, and interval between defaecations. Few non-dietary features of chimpanzee scats significantly differentiated sex or age of the defaecator, but total scat length and height distinguished adults from juveniles/infants. Defaecation rates and distance travelled were similar for adult males and females, indicating the importance of both sexes as potential primary seed dispersers. Observed travelling parties vs. non-observed travelling parties yielded similar data, indicating the potential to assess party size from scat encounter rates over a set distance. We provide detailed measurements of scat dimensions for this ape taxon which previously have been lacking. This research builds upon prior work by recording more in-depth data for focal subjects and travelling parties on defaecation and scat encounter rates. The findings presented should assist in the interpretation of scat data when censusing unhabituated chimpanzees.

Reflections in the rainforest: full-length mirrors facilitate behavioral observations of unhabituated, wild chimpanzees.

We describe behaviors of unhabituated wild chimpanzees in Gabon during repeated encounters with large mirrors installed permanently in their home range. Movement in proximity to the mirrors triggered video cameras that recorded the scene. Data are presented for 51 mirror encounters spanning a 3-year period. After initial wariness, mirror-directed aggressive behaviors were common, especially in adult males, but aggression gradually diminished and eventually almost completely ceased. Focusing on the two mirrors that elicited most reactions, the percentage of chimpanzees showing tension or anxiety also decreased across encounters. These mirrors elicited a range of socio-sexual behaviors interpreted as having a reassurance function, especially when group-level tension appeared high. Chimpanzees also occasionally directed these behaviors towards their own reflection. Despite increasing habituation and positive attraction to the mirrors, none of the chimpanzees displayed signs of self-recognition. We conclude that a combination of large mirrors and video traps can provide valuable information about unhabituated, semi-terrestrial primates in their natural habitat, by inducing the primates to stay in one place for longer than they might otherwise do.

Field studies of Pan troglodytes reviewed and comprehensively mapped, focussing on Japan's contribution to cultural primatology.

Field studies done over decades of wild chimpanzees in East, Central and West Africa have yielded impressive, cumulative findings in cultural primatology. Japanese primatologists have been involved in this advance from the outset, over a wide variety of topics. Here I review the origins and development of field studies of Pan troglodytes, then assess their progress based on analogy between cultural primatology and cultural anthropology, through four stages: natural history, ethnography, ethnology, and intuition. Then, I focus on six topics that continue to yield informative debate: technology, universals, nuanced variation, archaeology, applied primatology, and ecology. Finally, I offer a map of sites of field study of wild chimpanzees. It is clear that Japanese primatologists have made a significant contribution to East-West scientific exchange, especially at the field sites of Bossou and Mahale.

Non-human primates avoid the detrimental effects of prenatal androgen exposure in mixed-sex litters: combined demographic, behavioral, and genetic analyses.

Producing single versus multiple births has important life history trade-offs, including the potential benefits and risks of sharing a common in utero environment. Sex hormones can diffuse through amniotic fluid and fetal membranes, and females with male littermates risk exposure to high levels of fetal testosterone, which are shown to have masculinizing effects and negative fitness consequences in many mammals. Whereas most primates give birth to single offspring, several New World monkey and strepsirrhine species regularly give birth to small litters. We examined whether neonatal testosterone exposure might be detrimental to females in mixed-sex litters by compiling data from long-term breeding records for seven primate species (Saguinus oedipus; Varecia variegata, Varecia rubra, Microcebus murinis, Mirza coquereli, Cheirogaleus medius, Galago moholi). Litter sex ratios did not differ from the expected 1:2:1 (MM:MF:FF for twins) and 1:2:2:1 (MMM:MMF:MFF:FFF for triplets). Measures of reproductive success, including female survivorship, offspring-survivorship, and inter-birth interval, did not differ between females born in mixed-sex versus all-female litters, indicating that litter-producing non-human primates, unlike humans and rodents, show no signs of detrimental effects from androgen exposure in mixed sex litters. Although we found no evidence for CYP19A1 gene duplications-a hypothesized mechanism for coping with androgen exposure-aromatase protein evolution shows patterns of convergence among litter-producing taxa. That some primates have effectively found a way to circumvent a major cost of multiple births has implications for understanding variation in litter size and life history strategies across mammals.

Vertical bipedal locomotion in wild bearded capuchin monkeys (Sapajus libidinosus).

When carrying objects, nonhuman primates often show bipedal locomotion. Studies of primate bipedality, however, in both nature and captivity, have concentrated on locomotion on horizontal substrates, either terrestrially or arboreally. No observational or experimental study seems to have looked at non-horizontal bipedality, yet we show here that it occurs often in nature in Sapajus libidinosus, the bearded capuchin monkey. The context is transport of small food items from source to site of consumption, in which the monkeys usually carry handfuls of maize kernels over several meters' distance, both on the ground and in the trees. Most impressively, over a fifth of such bouts are done vertically, when the tree trunk is fully upright. Such vertical bipedality, with or without transport, apparently has not been reported before.

Tools to tipple: ethanol ingestion by wild chimpanzees using leaf-sponges.

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.

Apes in the Anthropocene: flexibility and survival.

We are in a new epoch, the Anthropocene, and research into our closest living relatives, the great apes, must keep pace with the rate that our species is driving change. While a goal of many studies is to understand how great apes behave in natural contexts, the impact of human activities must increasingly be taken into account. This is both a challenge and an opportunity, which can importantly inform research in three diverse fields: cognition, human evolution, and conservation. No long-term great ape research site is wholly unaffected by human influence, but research at those that are especially affected by human activity is particularly important for ensuring that our great ape kin survive the Anthropocene.

Snakes as hazards: modelling risk by chasing chimpanzees.

Snakes are presumed to be hazards to primates, including humans, by the snake detection hypothesis (Isbell in J Hum Evol 51:1-35, 2006; Isbell, The fruit, the tree, and the serpent. Why we see so well, 2009). Quantitative, systematic data to test this idea are lacking for the behavioural ecology of living great apes and human foragers. An alternative proxy is snakes encountered by primatologists seeking, tracking, and observing wild chimpanzees. We present 4 years of such data from Mt. Assirik, Senegal. We encountered 14 species of snakes a total of 142 times. Almost two-thirds of encounters were with venomous snakes. Encounters occurred most often in forest and least often in grassland, and more often in the dry season. The hypothesis seems to be supported, if frequency of encounter reflects selective risk of morbidity or mortality.

Chimpanzees prey on army ants at Seringbara, Nimba Mountains, Guinea: predation patterns and tool use characteristics.

Chimpanzees are renowned for their use of foraging tools in harvesting social insects and some populations use tools to prey on aggressive army ants (Dorylus spp.). Tool use in army ant predation varies across chimpanzee study sites with differences in tool length, harvesting technique, and army ant species targeted. However, surprisingly little is known about the detailed ecology of army ant predation. We studied army ant predation by chimpanzees (Pan troglodytes verus) at the Seringbara study site in the Nimba Mountains, Guinea (West Africa), over 10 years (2003-2013). We investigated chimpanzee selectivity with regards to army ant prey species. We assessed the temporal variation in army ant-feeding and examined whether army ant predation was related to rainfall or ripe fruit availability. Moreover, we examined whether chimpanzees showed selectivity regarding plant species used for tool manufacture, as well as the relationship between tool species preference and tool collection distance. Lastly, we measured tool properties and investigated the use of tool sets and composite tools in army ant predation. Seringbara chimpanzees preyed on one army ant species (D. nigricans) more often than expected based on encounter rates, which may be explained by the overlap in altitudinal distribution between chimpanzees and D. nigricans. Army ant predation was not related to rainfall or fruit availability. Chimpanzees were selective in their choice of tool materials and collected their preferred tool species (Alchornea hirtella) from greater distances than they did other species. Lastly, Seringbara chimpanzees used both tool sets and composite tools (tree perch) in army ant predation. Tool types (dig vs. dip) differed in width and strength, but not length. Tool composites were found at 40% of ant-feeding sites. Our study sheds new light on the ecology of army ant predation and provides novel insights into chimpanzee selection of army ant prey and tool species.

Grips and hand movements of chimpanzees during feeding in Mahale Mountains National Park, Tanzania.

It has long been assumed that stone tool making was a major factor in the evolution of derived hominin hand morphology. However, stresses on the hand associated with food retrieval and processing also have been recognized as relevant early hominin behaviors that should be investigated. To this end, chimpanzee food manipulation was videotaped in the Mahale Mountains National Park, Tanzania. Grips and hand movements by 39 chimpanzees were analyzed for arboreal and terrestrial feeding involving 10 food-types and associated vegetation. It was predicted that (1) new grips would be found that had not been observed in captivity, (2) forceful precision grips would be absent from the repertoire, as in captivity, and (3) precision handling would be observed. New grips involving the full thumb and buttressed index finger, and a new integrated pattern of grips and forceful hand movements were discovered, associated with feeding on large fruits and meat. Participation of the full thumb in these grips, rather than the distal thumb and fingers, throws light on feeding behaviors that may have become increasingly significant factors in the evolution of derived hominin thumb morphology. The proximal thumb stabilizes food with the flexed index finger against the pull of the teeth and provides leverage in breaking food into portions. Isolated qualitative observations of possibly forceful pinch by the thumb and side of the index finger highlight the need for comparative quantitative data to test whether humans are unique in forceful precision gripping capability. Precision handling was not seen.

Chimpanzees (Pan troglodytes verus) and their mammalian sympatriates: Mt. Assirik, Niokolo-Koba National Park, Senegal.

In intact, mosaic ecosystems, chimpanzees are sympatric with a wide range of other mammals, which may be predators, prey, or competitors. We delve beyond the nominal data of species lists to interval-level data on 35 medium-bodied and large-bodied mammals encountered at a hot, dry, and open field site in far West Africa. Frequency of encounter, habitat where found, and number of individuals encountered are analysed for species for which enough data were accumulated. Further, we compare findings over three periods (1976-1979, 2000, 2012). Species most often encountered were those normally classed as typical savanna forms. Even a crude classification into forest, woodland, and grassland ecotypes yields differences in species likely to meet apes. Comparison of encounter rates over time was surprisingly congruent, although not all species seen in the 1970s survived to the 2000s. Overall, Assirik's mammalian fauna is comparable to palaeo-faunal guilds sympatric with various extinct hominins.

Selective insectivory at Toro-Semliki, Uganda: comparative analyses suggest no 'savanna' chimpanzee pattern.

Chimpanzee (Pan troglodytes) insectivory across Africa is ubiquitous. Insects provide a significant nutritional payoff and may be important for chimpanzees in dry, open habitats with narrow diets. We tested this hypothesis at Semliki, Uganda, a long-term dry study site. We evaluated prospects for insectivory by measuring insect abundance along de novo transects and trails, monitoring social insect colonies, and surveying available raw materials for elementary technology. We determined the frequency and nature of insectivory through behavioral observation and fecal analysis. We then compared our results with those from 15 other long-term chimpanzee study sites using a cluster analysis. We found that Semliki chimpanzees are one of the most insectivorous populations studied to date in terms of frequency of consumption, but they are very selective in their insectivory, regularly consuming only weaver ants (Oecophylla longinoda) and honey and bees from hives of Apis mellifera. This selectivity obtains despite having a full range of typical prey species available in harvestable quantities. We suggest that Semliki chimpanzees may face ecological time constraints and therefore bias their predation toward prey taxa that can be quickly consumed. Geographical proximity correlated with the results of the cluster analysis, while rainfall, a relatively gross measure of environment, did not. Because broad taxonomic groups of insects were used in analyses, prey availability was unlikely to have a strong effect on this pattern. Instead, we suggest that transmission of cultural knowledge may play a role in determining chimpanzee prey selection across Africa. Further study is needed to test these hypotheses.

The 'other faunivory' revisited: Insectivory in human and non-human primates and the evolution of human diet.

The role of invertebrates in the evolution of human diet has been under-studied by comparison with vertebrates and plants. This persists despite substantial knowledge of the importance of the 'other faunivory', especially insect-eating, in the daily lives of non-human primates and traditional human societies, especially hunters and gatherers. Most primates concentrate on two phyla, Mollusca and Arthropoda, but of the latter's classes, insects (especially five orders: Coleoptera, Hymenoptera, Isoptera, Lepidoptera, Orthoptera) are paramount. An insect product, bees' honey, is particularly important, and its collection shows a reversal of the usual sexual division of labor. Human entomophagy involves advanced technology (fire, containers) and sometimes domestication. Insectivory provides comparable calorific and nutritional benefits to carnivory, but with different costs. Much insectivory in hominoids entails elementary technology used in extractive foraging, such as termite fishing by chimpanzees. Elucidating insectivory in the fossil and paleontological record is challenging, but at least nine avenues are available: remains, lithics, residues, DNA, coprolites, dental microwear, stable isotopes, osteology, and depictions. All are in play, but some have been more successful so far than others.