Temporal Variation in Insect-eating by Chimpanzees and Gorillas in Southeast Cameroon: Extension of Niche Differentiation

I studied insect-foraging strategies of great apes and aimed to define niche differentiation in their insect diet. I investigated seasonality in fruit-, foliage-, insect-, and meat-eating by great apes in southeast Cameroon via indirect methods and measured activity and nest densities of insect prey. I used a multinomial logistic regression to analyze the data. Gorilla and chimpanzee insect-, ant-, and termite-eating does not correlate with rainfall. Ant- and nonwinged termite-eating by chimpanzees increased in periods of succulent fruit scarcity and provided protein and energy, which might have compensated for the protein-low foliage eaten then. The apes ate winged termites when succulent fruit was abundant. Ant and winged termite consumption by gorillas correlates positively with that of chimpanzees. Ant-eating by gorillas increased when fruit was scarce, but was also associated with temporal ant activity and nest density. Both ape species also encountered more ant nests and trails in that period, as they predominantly foraged for herbs in vegetation types with high ant availability. In contrast, fruit-eating correlates positively with nonwinged termite-eating by gorillas, but again temporal prey availability is also associated. Termites might have provided 1) supplemental iron when tannin-rich fruits were eaten or 2) antidiarrheal properties when gorillas ate too much laxative fruit. Termite-eating by both ape species is not associated with spatial termite availability. In conclusion, there is niche differentiation in their insect diet. Based on the trade-off between foraging effort and nutritional gain, chimpanzees use a high-energy and gorillas a low-energy strategy when feeding on termites, but both use a low-energy strategy when feeding on ants. However, more information on the consumption of ant larvae is necessary to define niche differentiation in their ant diet.     

Insect-eating by sympatric Lowland gorillas (Gorilla g. gorilla) and chimpanzees (Pan t. troglodytes) in the Lopé Reserve,Gabon

Sympatric populations of lowland gorillas (Gorilla gorilla gorilla) and chimpanzees (Pan troglodytes troglodytes) in the Lopé Reserve in central Gabon consumed insects at similar average frequencies over a 7-year period (30% versus 31% feces contained insect remains). Data came mostly from fecal analysis supplemented by observation and trail evidence. The weaver ant (Oecophylla longinoda) was the species eaten most frequently by both gorillas and chimpanzees. Other species of insects wore eaten but there was virtually no overlap: Chimpanzees used tools to eat Apis bees (and their honey) and two large species of ants; gorillas ate three species of small ants. Thus, despite their shared habitat, the esources utilized were not identical as gorillas do not show the tool-use “technology” of chimpanzees. The frequency of insect-eating by both species of ape varied seasonally and between years but in different ways. This variation did not seem to be related to the ratio of fruit to foliage in their diets. Gorillas of all age-classes ate insects at similar rates. Comparisons with insectivory by other populations of gorillas indicate differences exist. Mountain gorillas (Gorilla g. beringei) in the Virunga Volcanoes, Rwanda, consume thousands of invertebrates daily, eating them inadvertently with handfuls of herbaceous foods but they deliberately ingest insect-foods only rarely. Lowland gorillas at Lopé habitually ate social insects, and their selective processing of herbaceous foods probably minimizes inadvertent consumption of other invertebrates. Gorillas at Belinga in northeastern Gabon, 250 km from Lop6, ate social insects at similar rates but ignored weaver ants in favor of Cubitermes sulcifrons, a small species of termite that occurs at Lopé but was not eaten by gorillas. This indicates that local traditions similar to those reported for chimpanzees also exist amongst populations of gorillas. © 1992 Wiley-Liss, Inc.     

Food Preferences Among Captive Western Gorillas (Gorilla gorilla gorilla) and Chimpanzees (Pan troglodytes)

I used a zoological park setting to address food preferences among gorillas (Gorilla gorilla gorill) and chimpanzees (Pan troglodytes). Gorillas and chimpanzees are different sizes, and consequently, have been traditionally viewed as ecologically distinct. Sympatric western gorillas and chimpanzees have proved difficult to study in the wild. Limited field data have provided conflicting information about whether gorillas are fundamentally different from chimpanzees in diet and behavior. Fruit eating shapes the behavior of most apes, but it is unclear whether the large-bodied gorillas are an exception to this rule, specifically whether they are less selective and more opportunistic fruit eaters than chimpanzees are. My research provides experimental observational data to complement field data and to better characterize the diets and food preferences of the African apes. During laboratory research at the San Francisco Zoological Gardens, I examined individual and specific differences in food preferences of captive gorillas and chimpanzees via experimental paired-choice food trials with foods that varied in nutritional content. During the study, I offered 2500 paired-food choices to 6 individual gorillas and 2000 additional pairs to them as a group. I also proffered 600 food pairs to 4 individual chimpanzees. Despite expectations of the implications of body size differences for diet, gorillas and chimpanzees exhibited similar food preferences. Both species preferred foods high in non-starch sugars and sugar-to-fiber ratios, and low in total dietary fiber. Neither species avoided foods containing tannins. These data support other suggestions of African apes sharing a frugivorous adaptation.     

Nutritional composition of actual and potential insect prey for the Kasekela chimpanzees of Gombe National Park,Tanzania

Humans, all great ape species, and some lesser apes consume insects. Insects can provide comparable nutritional yields to meat on a gram‐for‐gram basis and may serve as an important source of energy, fat, protein, minerals, and vitamins for hominoids. Although potential insect prey are abundant in ape habitats, patterns of insectivory are not consistent across species or populations. Efforts to understand these patterns are complicated by a lack of nutritional data. We collected samples of insects consumed by the Kasekela chimpanzee community of Gombe National Park, Tanzania, as well as of some insects found within the community range and ignored by these chimpanzees but known to be preyed upon by Pan elsewhere. We determined the gross energy (GE), estimated metabolizable energy (ME), fat, protein, fiber, and ash content of these samples following standard methodologies. We use these data to test the hypothesis that Kasekela chimpanzees choose insect prey (at least in part) based on energy and/or macronutrient content. On a fresh‐weight, per‐gram basis, the insect prey consumed by Kasekela chimpanzees had significantly higher fat and lower ash content than other assayed insects, and on a fresh‐weight, per‐foraging‐unit (“per‐insect,” “per‐dip,” or “per‐nest”) basis were significantly higher in GE, fat, and protein. On a per‐gram basis, the assayed insects were generally comparable in energy and macronutrients to wild vertebrate meat. We conclude that Kasekela chimpanzees do favor insects that are high in energy, fat, and protein, and that the potential macronutrient yields from some forms of insectivory are not trivial. © 2012 Wiley Periodicals, Inc.     

Diet and seasonal changes in sympatric gorillas and chimpanzees at Kahuzi–Biega National Park

Based on 8 years of observations of a group of western lowland gorillas (Gorilla beringei graueri) and a unit-group of chimpanzees (Pan troglodytes schweinfurthii) living sympatrically in the montane forest at Kahuzi–Biega National Park, we compared their diet and analyzed dietary overlap between them in relation to fruit phenology. Data on fruit consumption were collected mainly from fecal samples, and phenology of preferred ape fruits was estimated by monitoring. Totals of 231 plant foods (116 species) and 137 plant foods (104 species) were recorded for gorillas and chimpanzees, respectively. Among these, 38% of gorilla foods and 64% of chimpanzee foods were eaten by both apes. Fruits accounted for the largest overlap between them (77% for gorillas and 59% for chimpanzees). Gorillas consumed more species of vegetative foods (especially bark) exclusively whereas chimpanzees consumed more species of fruits and animal foods exclusively. Although the number of fruit species available in the montane forest of Kahuzi is much lower than that in lowland forest, the number of fruit species per chimpanzee fecal sample (average 2.7 species) was similar to that for chimpanzees in the lowland habitats. By contrast, the number of fruit species per gorilla fecal sample (average 0.8 species) was much lower than that for gorillas in the lowland habitats. Fruit consumption by both apes tended to increase during the dry season when ripe fruits were more abundant in their habitat. However, the number of fruit species consumed by chimpanzees did not change according to ripe fruit abundance. The species differences in fruit consumption may be attributed to the wide ranging of gorillas and repeated usage of a small range by chimpanzees and/or to avoidance of inter-specific contact by chimpanzees. The different staple foods (leaves and bark for gorillas and fig fruits for chimpanzees) characterize the dietary divergence between them in the montane forest of Kahuzi, where fruit is usually scarce. Gorillas rarely fed on insects, but chimpanzees occasionally fed on bees with honey, which possibly compensate for fruit scarcity. A comparison of dietary overlap between gorillas and chimpanzees across habitats suggests that sympatry may not influence dietary overlap in fruit consumed but may stimulate behavioral divergence to reduce feeding competition between them.     

Food preferences of wild mountain gorillas

Determining the nutritional and phenolic basis of food preference is important for understanding the nutritional requirements of animals. Preference is a measure of which foods would be consumed by an animal if there was no variation in availability among food items. From September 2004 to August 2005, we measured the food preferences of four wild mountain gorilla groups that consume foliage and fruit in Bwindi Impenetrable National Park, Uganda, to determine what nutrients and phenols are preferred and/or avoided. To do so, we asked the following questions: (1) Which plant species do the gorillas prefer? (2) Considering the different plant parts consumed of these preferred species, what nutrients and/or phenols characterize them? (3) Do the nutritional and phenolic characteristics of preferred foods differ among gorilla groups? We found that although some species were preferred and others were not, of those species found in common among the different group home ranges, the same ones were generally preferred by all groups. Second, all groups preferred leaves with relatively high protein content and relatively low fiber content. Third, three out of four groups preferred leaves with relatively high sugar amounts. Fourth, all groups preferred pith with relatively high sugar content. Finally, of the two groups tested, we found that the preferred fruits of one group had relatively high condensed tannin and fiber/sugar contents, whereas the other group's preferred fruits were not characterized by any particular nutrient/phenol. Overall, there were no differences among gorilla groups in nutritional and phenolic preferences. Our results indicate that protein and sugar are important in the diets of gorillas, and that the gorillas fulfil these nutritional requirements through a combination of different plant parts, shedding new light on how gorillas balance their diets in a variable environment. Am. J. Primatol. 70:927–938, 2008. © 2008 Wiley‐Liss, Inc.     

Hand Preference for a Novel Bimanual Coordinated Task During Termite Feeding in Wild Western Gorillas (<Emphasis Type="Italic">Gorilla gorilla gorilla</Emphasis>)

Although the level of handedness in humans varies cross-culturally, humans are generally described as right-handed, which has been considered a uniquely human trait. Recently, captive chimpanzees (Pan troglodytes) have been shown to exhibit right-hand preference when performing bimanual but not unimanual tasks. Less clear is whether this pattern also occurs in wild chimpanzees and other African apes. Using videos (N = 49) of six wild western gorillas (Gorilla gorilla gorilla) feeding on termites at the Mondika Research Center (Republic of Congo), we tested whether they exhibit hand preference when performing unimanual, i.e., reaching for termite mound pieces; bimanual, i.e., “termite tapping”: rhythmically shaking a piece of termite mound with the dominant hand and collecting the termites in the other hand tasks; or hand transfer prior to bimanual tasks, i.e., transferring a piece of termite mound from one hand to the other. All individuals exhibited exclusive hand preference when performing the bimanual tasks, with five of six gorillas preferring the right hand. Conversely, most individuals did not show any manual preference during the unimanual task. In addition, hand preference during hand transfer revealed clear hand dominance of similar strength and direction of those shown for the bimanual task, suggesting that this measure is as sensitive as the bimanual task itself. Thus, we propose “termite feeding” as a novel task to be considered in future hand-preference studies in wild western gorillas. Our results are in concordance with those for chimpanzees and captive gorillas showing hemispheric specialization for bimanual actions in apes.     

Nutritional quality of gorilla diets: consequences of age,sex, and season

We tested the effects of age, sex, and season on the nutritional strategies of a group of mountain gorillas (Gorilla beringei) in the Bwindi Impenetrable National Park, Uganda. Through observations of food intake of individual gorillas and nutritional analyses of dietary components over different seasons and environments, we estimated nutrient intake and evaluated diet adequacy. Our results suggest that the nutritional costs of reproduction and growth affect nutrient intake; growing juveniles and adult females ate more food and more protein per kilogram of metabolic body mass than did silverbacks. The diets of silverback males, adult females, and juveniles contained similar concentrations of protein, fiber, and sugar, indicating that adult females and juveniles did not select higher protein foods than silverbacks but rather consumed more dry matter to ingest more protein. Juveniles consumed more minerals (Ca, P, Mg, K, Fe, Zn, Mn, Mo) per kilogram of body mass than adult females and silverback males, and juveniles consumed diets with higher concentrations of phosphorous, iron, and zinc, indicating that the foods they ate contained higher concentrations of these minerals. Seasonally, the amount of food consumed on a dry weight basis did not vary, but with increased frugivory, dietary concentrations of protein and fiber decreased and those of water-soluble carbohydrates increased. Energy intake did not change over the year. With the exception of sodium, gorillas ate diets that exceeded human nutrient requirements. A better understanding of the relative importance of food quantity and quality for different age–sex classes provides insights into the ways in which gorillas may be limited by food resources when faced with environmental heterogeneity.     

The role of taste in food selection by African apes: implications for niche separation and overlap in tropical forests

Ripe fruit eating shapes the behavior of most of the apes. Gorillas (Gorilla gorilla) and chimpanzees (Pan troglodytes) are very different sizes and, consequently, have been traditionally viewed as ecologically distinct, but few studies have explored the behavioral and physiological foundations of their diets. Debate continues on the extent that large-bodied gorillas may be less selective and more opportunistic fruit eaters than chimpanzees. Taste responses have been predicted to relate to body size and digestive strategies. This study employs laboratory research on taste perception and discrimination among captive zoo-housed chimpanzees and relates it to previous work on gorillas to better characterize diets and niche separation among these apes. During the captive trials, differences were recorded in consumption patterns of water and varying concentrations of dilute aqueous fructose (sweet) and tannic acid solutions (astringent), compounds commonly found in wild foods. The chimpanzees exhibited similar preference thresholds for fructose (50 mM) to other primates studied. They exhibited slightly lower inhibition thresholds for tannic acid solutions than gorillas, but higher than smaller primates studied to date. These preliminary findings suggest that tannin tolerance may well be mediated by body size, though possible species differences in salivary proteins or other sensory differences remain to be explored. This research furthers our efforts to understand the roles of body size and physiological adaptations in shaping diet and niche separation of chimpanzees and gorillas.     

Effects of drugs on nutrition

Drugs can increase nutrient requirements through various mechanisms and if these requirements are not met by dietary modification or provision of nutrient supplements, deficiency disease will result. Commoner nutritional effects of drugs consist in the insidious development of hypovitaminoses; other serious nutritional consequences of drug intake include growth impairment and, in the case of vitamin antagonists, poisoning through interference with metabolic processes dependent on the activity of vitamins or coenzymes. Interactions may exist between pharmacologic agents and nutrients with respect to their absorption, transport, metabolism and excretion. Single drugs can cause nutrient depletion by more than one mechanism and multiple drug regimens can deplete nutrient stores by a synergistic effect. Risks of drug-induced malnutrition with drugs increase with dose and duration of intake, marginal diets and co-existence of disease which increases requirements for the same nutrients that are affected by the drug.     

Interactions between zoo‐housed great apes and local wildlife

Although there are published reports of wild chimpanzees, bonobos, and orangutans hunting and consuming vertebrate prey, data pertaining to captive apes remain sparse. In this survey‐based study, we evaluate the prevalence and nature of interactions between captive great apes and various indigenous wildlife species that range into their enclosures in North America. Our hypotheses were threefold: (a) facilities housing chimpanzees will report the most frequent and most aggressive interactions with local wildlife; (b) facilities housing orangutans and bonobos will report intermediate frequencies of these interactions with low levels of aggression and killing; and (c) facilities housing gorillas will report the lowest frequency of interactions and no reports of killing local wildlife. Chimpanzees and bonobos demonstrated the most aggressive behavior toward wildlife, which matched our predictions for chimpanzees, but not bonobos. This fits well with expectations for chimpanzees based on their natural history of hunting and consuming prey in wild settings, and also supports new field data on bonobos. Captive gorillas and orangutans were reported to be much less likely to chase, catch and kill wildlife than chimpanzees and bonobos. Gorillas were the least likely to engage in aggressive interactions with local wildlife, matching our predictions based on natural history. However unlike wild gorillas, captive gorillas were reported to kill (and in one case, eat) local wildlife. These results suggest that some behavioral patterns seen in captive groups of apes may be useful for modeling corresponding activities in the wild that may not be as easily observed and quantified. Furthermore, the data highlight the potential for disease transmission in some captive settings, and we outline the associated implications for ape health and safety. Am. J. Primatol. 71:458–465, 2009. © 2009 Wiley‐Liss, Inc.     

Nucleotide diversity in gorillas

Comparison of the levels of nucleotide diversity in humans and apes may provide valuable information for inferring the demographic history of these species, the effect of social structure on genetic diversity, patterns of past migration, and signatures of past selection events. Previous DNA sequence data from both the mitochondrial and the nuclear genomes suggested a much higher level of nucleotide diversity in the African apes than in humans. Noting that the nuclear DNA data from the apes were very limited, we previously conducted a DNA polymorphism study in humans and another in chimpanzees and bonobos, using 50 DNA segments randomly chosen from the noncoding, nonrepetitive parts of the human genome. The data revealed that the nucleotide diversity (pi) in bonobos (0.077%) is actually lower than that in humans (0.087%) and that pi in chimpanzees (0.134%) is only 50% higher than that in humans. In the present study we sequenced the same 50 segments in 15 western lowland gorillas and estimated pi to be 0.158%. This is the highest value among the African apes but is only about two times higher than that in humans. Interestingly, available mtDNA sequence data also suggest a twofold higher nucleotide diversity in gorillas than in humans, but suggest a threefold higher nucleotide diversity in chimpanzees than in humans. The higher mtDNA diversity in chimpanzees might be due to the unique pattern in the evolution of chimpanzee mtDNA. From the nuclear DNA pi values, we estimated that the long-term effective population sizes of humans, bonobos, chimpanzees, and gorillas are, respectively, 10,400, 12,300, 21,300, and 25,200.     

Insectivory by Gorilla gorilla gorilla in Southeast Cameroon

Our study extends quantitative analyses of insect-eating by gorillas (Gorilla gorilla gorilla) to Cameroon. During a 2-mo period (May–June 2001), we recorded and analyzed feeding traces on plants and insects and in gorilla feces. We found 180 feeding traces, 17% of which involved insectivory. Seventy-eight percent of the fecal samples (n = 36) contained insects. Ants were found in 61% of the samples, termites in 39%, while 56% of the samples contained remains of other insects. We added 14 new species to the known insect diet of western lowland gorillas. Overall, social insects are predominant. The choice of prey by the Ntonga gorillas gives new clues for the existence of cross-cultural differences among gorilla populations. A comparison of the overall frequency of insectivory with those at other sites in Central Africa indicate a possible effect of forest disturbance on the insectivorous behavior of gorillas. The study suggests the existence of temporal variation in ant- and termite-eating by gorillas.     

Foraging profiles of sympatric lowland gorillas and chimpanzees in the Lopé Reserve, Gabon.

Comparison of the diets of sympatric gorillas and chimpanzees allows an analysis of niche separation between these two closely related species. Qualitatively, their diets are similar, being dominated by an equally diverse array of fruit species complemented with vegetative plant parts, seeds and insects. Gorillas eat more vegetative plant parts than do chimpanzees, but niche separation is most obvious in periods of fruit scarcity when the two species show different strategies that reduce competition for food. Their abilities to overcome mechanical and physical plant defences appear to differ, as gorillas are able to subsist entirely on abundant vegetative foods. Chimpanzees show social adjustment, foraging alone or in small groups, to reduce intra-specific competition for scarce fruit resources. Thus it seems that subtle physiological differences have far-reaching repercussions, defining potential evolutionary pathways for social organization and allowing sufficient niche separation between species.     

A carnivorous plant fed by its ant symbiont: a unique multi-faceted nutritional mutualism

Scarcity of essential nutrients has led plants to evolve alternative nutritional strategies, such as myrmecotrophy (ant-waste-derived nutrition) and carnivory (invertebrate predation). The carnivorous plant Nepenthes bicalcarata grows in the Bornean peatswamp forests and is believed to have a mutualistic relationship with its symbiotic ant Camponotus schmitzi. However, the benefits provided by the ant have not been quantified. We tested the hypothesis of a nutritional mutualism, using foliar isotopic and reflectance analyses and by comparing fitness-related traits between ant-inhabited and uninhabited plants. Plants inhabited by C. schmitzi produced more leaves of greater area and nitrogen content than unoccupied plants. The ants were estimated to provide a 200% increase in foliar nitrogen to adult plants. Inhabited plants also produced more and larger pitchers containing higher prey biomass. C. schmitzi-occupied pitchers differed qualitatively in containing C. schmitzi wastes and captured large ants and flying insects. Pitcher abortion rates were lower in inhabited plants partly because of herbivore deterrence as herbivory-aborted buds decreased with ant occupation rate. Lower abortion was also attributed to ant nutritional service. The ants had higher δ(15)N values than any tested prey, and foliar δ(15)N increased with ant occupation rate, confirming their predatory behaviour and demonstrating their direct contribution to the plant-recycled N. We estimated that N. bicalcarata derives on average 42% of its foliar N from C. schmitzi wastes, (76% in highly-occupied plants). According to the Structure Independent Pigment Index, plants without C. schmitzi were nutrient stressed compared to both occupied plants, and pitcher-lacking plants. This attests to the physiological cost of pitcher production and poor nutrient assimilation in the absence of the symbiont. Hence C. schmitzi contributes crucially to the nutrition of N. bicalcarata, via protection of assimilatory organs, enhancement of prey capture, and myrmecotrophy. This combination of carnivory and myrmecotrophy represents an outstanding strategy of nutrient sequestration.     

Hand preferences for coordinated bimanual actions in 777 great apes: implications for the evolution of handedness in hominins

Whether or not nonhuman primates exhibit population-level handedness remains a topic of considerable scientific debate. Here, we examined handedness for coordinated bimanual actions in a sample of 777 great apes including chimpanzees, bonobos, gorillas, and orangutans. We found population-level right-handedness in chimpanzees, bonobos and gorillas, but left-handedness in orangutans. Directional biases in handedness were consistent across independent samples of apes within each genus. We suggest that, contrary to previous claims, population-level handedness is evident in great apes but differs among species as a result of ecological adaptations associated with posture and locomotion. We further suggest that historical views of nonhuman primate handedness have been too anthropocentric, and we advocate for a larger evolutionary framework for the consideration of handedness and other aspects of hemispheric specialization among primates.     

Selective logging, habitat quality and home range use by sympatric gorillas and chimpanzees: a case study from an active logging concession in Southeast Cameroon

We examined range use by great apes during logging activities and investigated associations between local variations in ape abundance and changes in the structure of the habitat or in the availability of fruits after disturbances. We carried out two annual censuses of western lowland gorilla (G. g. gorilla) and chimpanzee populations (Pan t. troglodytes) in an active logging concession in Southeast Cameroon. The results suggest that gorillas may adapt their range use to avoid most recently logged compartments, while chimpanzees appear to be more spatially resilient to logging. In our study site, selective logging affected 10% of the forest. After logging, gorillas nested in all types of vegetation, while chimpanzees nested exclusively in mixed mature forest. Fruit availability was not affected by logging and did not explain the distribution of ape nests in the study area.     

Species-Specific Effects of Ant Inhabitants on Bromeliad Nutrition

Predator activities may lead to the accumulation of nutrients in specific areas of terrestrial habitats where they dispose of prey carcasses. In their feeding sites, predators may increase nutrient availability in the soil and favor plant nutrition and growth. However, the translocation of nutrients from one habitat to another may depend on predator identity and diet, as well as on the amount of prey intake. Here we used isotopic (¹⁵N) and physiological methods in greenhouse experiments to evaluate the effects of the identity of predatory ants (i.e., the consumption of prey and nest sites) on the nutrition and growth of the bromeliad Quesnelia arvensis. We showed that predatory ants with protein-based nutrition (i.e., Odontomachus hastatus, Gnamptogenys moelleri) improved the performance of their host bromeliads (i.e., increased foliar N, production of soluble proteins and growth). On the other hand, the contribution of Camponotus crassus for the nutritional status of bromeliads did not differ from bromeliads without ants, possibly because this ant does not have arthropod prey as a preferred food source. Our results show, for the first time, that predatory ants can translocate nutrients from one habitat to another within forests, accumulating nutrients in their feeding sites that become available to bromeliads. Additionally, we highlight that ant contribution to plant nutrition may depend on predator identity and its dietary requirements. Nest debris may be especially important for epiphytic and terrestrial bromeliads in nutrient-poor environments.