Leaf-swallowing by chimpanzees: A behavioral adaptation for the control of strongyle nematode infections

Swallowing whole leaves by chimpanzees and other African apes has been hypothesized to have an antiparasitic or medicinal function, but detailed studies demonstrating this were lacking. We correlate for the first time quantifiable measures of the health of chimpanzees with observations of leaf-swallowing in Mahale Mountains National Park, Tanzania. We obtained a total of 27 cases involving the use ofAspilia mossambicensis (63%),Lippia plicata (7%),Hibiscus sp. (15%),Trema orientalis (4%), andAneilema aequinoctiale (11%), 15 cases by direct observation of 12 individuals of the Mahale M group. At the time of use, we noted behavioral symptoms of illness in the 8 closely observed cases, and detected single or multiple parasitic infections (Strongyloides fulleborni, Trichuris trichiura, Oesophagostomum stephanostomum) in 10 of the 12 individuals. There is a significant relationship between the presence of whole leaves (range, 1–51) and worms of adultO. stephanostomum (range, 2–21) in the dung. HPLC analysis of leaf samples collected after use showed that thiarubrine A, a compound proposed to act as a potent nematocide in swallowingAspilia spp., was not present in leaves ofA. mossambicensis or the three other species analyzed. Alternative nematocidal or egg-laying inhibition activity was not evident. Worms ofO. stephanostomum were recovered live and motile from chimpanzee dung, trapped within the folded leaves and attached to leaf surfaces by trichomes, though some were moving freely within the fecal matter, suggesting that the physical properties of leaves may contribute to the expulsion of parasites. We review previous hypotheses concerning leaf-swallowing and propose an alternative hypothesis based on physical action.     

Chimpanzee predation in the Mahale mountains from August 1979 to May 1982

Fifty-four episodes of predatory behavior of wild chimpanzees were recorded in Mahale, western Tanzania, from August 1979 to May 1982. The chimpanzees most frequently hunt in two seasons, during May, and from August to December. Longer-term fecal analysis indicates that predation frequency is significantly higher in the dry than in the rainy season. The seasonality of predation might be the result of the sum of various ecological factors, at least one of which is the birth season of the prey species. Most of the prey are juvenile blue duiker, bushbuck, bushpig, red colobus, and red-tailed monkeys. Sex difference is recognized in the prey selection and in the hunting method employed. Apparent local difference in the predatory behavior between Mahale and Combe chimpanzees (in Mahale,females hunt more frequently, and blue duiker is the most frequent prey) can be understood in terms of the difference either in the observation methods or in the faunal diversity and density. Other aspects of predatory behavior also are reported.     

Observations on the illness and consumption of a possibly medicinal plantVernonia amygdalina (Del.), by a wild chimpanzee in the Mahale Mountains National Park,Tanzania

Detailed observations on the consumption ofVernonia amygdalina (Del.), a naturally occurring plant of known ethnomedicinal value, by an adult female chimpanzee (Pan troglodytes schweinfurthii) of M-group in the Mahale Mountains, Tanzania were made. Chewing the pith of several shoots, she sucked out and swallowed the astringent, bitter tasting juice; spitting out the fibrous remains. The female was followed during this period for 11 hr, over two consecutive days, and was recognized to be in irregular health at the time of consumption, exhibiting signs of lethargy, lack of appetite, and irregularity of bodily excretions. The low frequency and lack of seasonality in the usage of this plant suggest that it is sought after for reasons other than as a food source. These factors suggest that for chimpanzees, the consumption of this plant is primarily medicinal. The symptoms displayed by the female are the same as those experienced by people throughout tropical Africa who utilize this plant as a medicinal treatment for them. Interactions between the female and others suggest that they too were aware of her condition and coordinated their activities with the female and her infant.     

Leaf-swallowing in Nigerian chimpanzees: evidence for assumed self-medication

A field study in Gashaka, Nigeria, adds the fourth subspecies of chimpanzee, Pan troglodytes vellerosus, to the list of African ape populations in which leaf-swallowing occurs. Unchewed herbaceous leaves of Desmodium gangeticum (Leguminosae-Papilionoideae) were recovered in 4% of 299 faecal samples of wild chimpanzees and clumps of sharp-edged grass leaves in 2%. The ingestion is believed to serve self-medicatory purposes because the leaves had a rough surface or were sharp-edged (which could be related to parasite control through a self-induced increase of gut motility), were not chewed, were excreted whole (indicating that they were not ingested for nutritional purposes), leaf-swallowing was restricted to the rainy season (during which time parasite re-infections are more common), and parasitic worms (Oesophagostomum stephanostomum) were found together with the leaves. Submitted to: Primates, May 2005; revision: 26 Oct 2005     

A preliminary note on the intestinal parasites of wild chimpanzees in the Mahale Mountains,Tanzania

Feces of wild chimpanzees in the Mahale Mountains, Tanzania, were inspected for intestinal parasites under a compound microscope. Eggs or larvae ofOesophagostomum, Strongyloides, Trichuris, Prosthenorchis, andBertiella were found. Intestinal nematodes significantly increased in the mid-rainy season. This finding supports (or, at least, is not in conflict with) the hypothesis thatAspilia leaves which are occasionally swallowed by chimpanzees may function as a vermicide, since ingestion of such leaves also increases significantly in the mid-rainy season.     

Population Dynamics of Wild Bonobos (Pan paniscus) at Wamba

We analyzed population dynamics and birth seasonality of wild bonobos at Wamba, Democratic Republic of the Congo, based on 20 years of observations (1976–1996). Wamba Bonobo infant mortality is much lower than that reported for chimpanzees. This seemes to be related to several socioecological characteristics of bonobos: the use of abundant fruit and herbaceous foods, larger food patch size, female feeding priority, and the absence of infanticide. The mean interval between live births of 4.8 years is shorter than those reported for chimpanzees, and some females simultaneously carried and nursed two successive offspring. Mother–offspring conflicts, such as refusal of suckling attempts and interference with mothers' copulation, which are common in chimpanzees, are rare in Wamba bonobos. A birth peak seems to occur during the light rainy season from March to May, just after the season with the least rainfall. This timing of births is similar to those reported for chimpanzee populations, and might benefit both mother and offspring by maximizing the amount of time before the next dry season.     

Predation on mammals by chimpanzees in the montane forest of Kahuzi, Zaire

The rate of predation on mammals by chimpanzees was determined from carcasses and from fecal specimens found on fresh trails during a 16-month period in the montane forest of Kahuzi-Biega National Park, Zaire. A unit-group of semi-habituated chimpanzees, composed of 22 – 23 individuals including 8 adult or adolescent males, appeared to kill about 18 – 30 mammalian prey (16 – 28Cercopithecus monkeys) per year, if the multiple kills by chimpanzees were not considered. A juvenile l'Hoest's monkey was recorded for the first time as the prey of chimpanzees in this study. Predation occurred in the late dry and the early rainy seasons, when the diversity of ripe fruits was the highest during the year. The Kahuzi chimpanzees tended to kill mammals less frequently but to killCercopithecus monkeys more frequently than chimpanzees in other habitats. The absence of red colobus monkeys, which are the most frequent prey in Gombe, Mahale, and Tai, might be responsible for the low predation rate. However, the estimated rate of predation onCercopithecus monkeys is the highest record among various chimpanzee habitats. At least 11 – 18% of theCercopithecus population seemed to be lost annually as a result of being killed by chimpanzees. Chimpanzees may be the most important predators on these monkeys in the absence of leopards at Kahuzi. The examination of fecal samples and carcasses suggested that adult (probably male) or adolescent chimpanzees tended to eat juvenile or subadult monkeys most frequently, as is also seen for chimpanzees in Gombe, Mahale, and Tai.     

Do bonobos copulate more frequently and promiscuously than chimpanzees?

The copulatory activities of bonobos (Pan paniscus) of Wamba, Zaire, were compared with those of chimpanzees (P. troglodytes schweinfurthii) of Mahale, Tanzania. The copulation rates of adult male bonobos were equal to or lower than those of adult male chimpanzees. The copulation rates of adult female bonobos were approximately equal to those of adult female chimpanzees who were in maximal genital swelling, but it should be much higher than those of the adult female chimpanzees throughout the birth interval. The copulation rates of adolescent male bonobos were lower than those of adolescent male chimpanzees, whereas the copulation rates of adolescent female bonobos were much higher than those of adolescent female chimpanzees. It was suggested that the bonobos of Wamba did not copulate more promiscuously than did the chimpanzees of Mahale. The female bonobos may show “receptivity”, whereas female chimpanzees may show rather “proceptivity”.     

Preharvest seed infection byAspergillus flavus group fungi and subsequent aflatoxin contamination in groundnuts in relation to soil types

Preharvest seed infection byAspergillus flavus and aflatoxin contamination in selected groundnut genotypes (fourA. flavus-resistant and fourA. flavus-susceptible) were examined in different soil types at several locations in India in 1985–1990. Undamaged mature pods were sampled at harvest and seed examined forA. flavus infection and aflatoxin content in two or more trials at ICRISAT Center on light sandy soils and red sandy loam soils (Alfisols), and on Vertisols, at Anantapur on light sandy soils, and at Dharwad and Parbhani on Vertisols. Rainy season trials (1985–1989) were all rainfed. Post-rainy season trials were irrigated; late-season drought stress (90 days after sowing (DAS) until harvest at 125 DAS) was imposed in the 1987/88 and 1989/90 seasons.A. flavus infection and aflatoxin contamination levels were much lower in seed of all genotypes from Vertisols than in seed from Alfisols across locations and seasons. Vertisols also had significantly lower populations ofA. flavus than Alfisols. There were no marked differences between light sandy soils and red sandy loam soils (Alfisols) in respect of seed infection byA. flavus and aflatoxin contamination. Significant interactions between genotypes and soil types were evident, especially in theA. flavus-susceptible genotypes. Irrespective of soil types,A. flavus-resistant genotypes showed lower levels of seed infection byA. flavus and other fungi than didA. flavus-susceptible genotypes. The significance of the low preharvest aflatoxin risk in groundnuts grown on Vertisols is highlighted.ICRISAT Journal Article No. JA 1122     

Host age,sex, and reproductive seasonality affect nematode parasitism in wild Japanese macaques

Parasites are characteristically aggregated within hosts, but identifying the mechanisms underlying such aggregation can be difficult in wildlife populations. We examined the influence of host age and sex over an annual cycle on the eggs per gram of feces (EPG) of nematode parasites infecting wild Japanese macaques (Macaca fuscata yakui) on Yakushima Island. Five species of nematode were recorded from 434 fecal samples collected from an age-structured group of 50 individually recognizable macaques. All parasites exhibited aggregated EPG distributions. The age–infection profiles of all three directly transmitted species (Oesophagostomum aculeatum, Strongyloides fuelleborni, and Trichuris trichiura) exhibited convex curves, but concavity better characterized the age–infection curves of the two trophically transmitted species (Streptopharagus pigmentatus and Gongylonema pulchrum). There was a male bias in EPG and prevalence of infection with directly transmitted species, except in the prevalence of O. aculeatum, and no sex bias in the other parasites. Infection with O. aculeatum showed a female bias in prevalence among young adults, and additional interactions with sex and seasonality show higher EPG values in males during the mating season (fall) but in females during the birth season (spring). These patterns suggest that an immunosuppressive role by reproductive hormones may be regulating direct, but not indirect, life-cycle parasites. Exposure at an early age may trigger an immune response that affects all nematodes, but trophically transmitted species appear to accumulate thereafter. Although it is difficult to discern clear mechanistic explanations for parasite distributions in wildlife populations, it is critical to begin examining these patterns in host species that are increasingly endangered by anthropogenic threats.     

Physiological activities and the active constituents of potentially medicinal plants used by wild chimpanzees of the Mahale mountains,Tanzania

Potential medicinal plants for wild chimpanzees have been studied in order to discover their physiologically active compounds. Tests of the physiological activity of 3 plant species—Vernonia amygdalina, Aspilia mossambicensis, andFicus exasperata—indicate that they contain a variety of active compounds. From one species,V. amygdalina, an antitumor agent and 2 possible antitumor promoters are identified. Furthermore, steroid glucosides were isolated as the bitter substances. These structurally new compounds are expected to exhibit a number of significant physiological activities. The chemical investigation of possible medicinal plants used by chimpanzees should be helpful in recovering naturally occurring compounds of medicinal significance for human use.     

Chimpanzees' (Pan troglodytes) choice of prey among termites (macrotermitinae) in western Tanzania

This study examines factors affecting chimpanzees' preying on termites, especially their choice of prey species. Regular surveys of a large sample of termite-mounds in the Mahale Mountains, Tanzania, confirmed that chimpanzees of B Group obtainedMacrotermes, which were relatively uncommon, by the use of fishing-tools, but ignored the much more abundantOdontotermes. This preference appeared to reflectMacrotermes' more extended swarming period, greater accessibility, larger size, and less noxious taste than the soldiers ofOdontotermes. Similar factors probably underly the chimpanzees' choice ofMacrotermes at Gombe, butPseudacanthotermes spiniger are also common there, and their absence from the diet is less easily explained. In contrast, the chimpanzees of K Group at Mahale prey mainly onP. spiniger;Macrotermes are apparently absent, andP. spiniger appear to be more abundant, accessible, and palatable than the alternativeOdontotermes.     

Chimpanzees' choices of prey between two sympatric species ofMacrotermes in the Campo Animal Reserve,Cameroon

Details are presented relating to chimpanzees' choices between two sympatric species of termites,Macrotermes lillijeborgi andM. vitrialatus, as food in the Campo Animal Reserve, southwest Cameroon, West Africa. An attempt was made to determine the various factors that affected such choices. The two species of termites seemed to have almost the same value in terms of ecological factors. However, chimpanzees fed almost exclusivelyonM. lillijeborgi, using digging sticks and fisching probes, during the study period which extended from the end of August to the middle of January, with their feeding activity showing peak at the beginning of the rainy season. By contrast,M. vitrialatus was rarely eaten in spite of the ease with which such prey could be obtained, namely, by desctruction of termite mounds by hand, without the need for tools. The reason that the chimpanzees discriminated between the two species of termite cannot be explained in terms of ecological factors such as size of prey, seasonal differences in termite activity, etc. Sticks used as tools were fairly uniform in size and character, mainly because of physical constraints related to the structure of termite mounds, and the brush-like ends of sticks seemed to be incidentaly byproducts of the chimpanzee's choice of plant species. Ecological factors could provide chimpanzees with a basis for the use of some kind of tool and help them modify it, while other factors, for example, something akin to leisure or the chimpanzee's interest in use of a tool, could provide an opportunity for inventing some tool-using behavior or for maintaining such behavior. These different factors, not being exclusive of one another, might affect the invention and maintenance of tool using-behavior at different phases. It is possible that chimpanzee's choice of prey may not always be the most efficient or appropriate in a given ecological situation.     

雷州半岛尾叶桉和湿加松人工林的蒸腾耗水规律

为正确认识大径材桉树及湿加松耗水规律,为地区人工林树种选择、栽培及抚育提供指导,应用TDP热扩散探针技术,对10年生尾叶桉和湿加松树干液流进行连续监测,并同步测定各气象因子,分析了雷州半岛地区尾叶桉和湿加松蒸腾耗水的日变化特征和季节变化规律,并与气象因子建立了相关模型。结果表明:尾叶桉和湿加松边材液流均表现出典型的昼高夜低的单峰型日变化特征,各月平均液流速率不同,且旱雨季差异显著;其中峰值尾叶桉雨季(0.127 cm/min)和旱季(0.096 cm/min)分别是湿加松雨季和旱季的1.30倍和1.57倍;日平均液流速率尾叶桉雨季(0.045 cm/min)和旱季(0.033 cm/min)分别是湿加松雨季和旱季的1.27倍和1.54倍;启动时间和迅速下降时间雨季两树种间差异不大,但旱季尾叶桉要提前湿加松约1—1.5 h启动,并晚0.5—1 h迅速下降。影响两树种边材液流速率的主要气象因子相同。尾叶桉人工林年平均单株日耗水量为12.79 L/d,是湿加松的1.33倍,林分蒸腾耗水量尾叶桉(582.16 mm)和湿加松(483.24 mm),分别占同期年降雨量的34.2%和28.4%,且两树种旱雨季蒸腾耗水量均雨季显著大于旱季。     

Winter grass cover crop effects on nematodes and yields of double cropped soybean

Rye (Secale cereale L.), wheat (Triticum aestivum L.), and annual ryegrass (Lolium multiflorum Lam.) are commonly double cropped with soybean (Glycine max L.). Recent greenhouse studies have shown variability in plant-parasitic nematode response to cool season grass species and cultivars. However, subsequent soybean performance was not affected by previous annual ryegrass cultivar in the green-house. The objective of this research was to determine whether winter cover crop species or cultivars affected nematode populations and subsequent performance of soybean in teh field. Four cultivars of annual ryegrass, wheat, and rye, and a fallow control were seeded on a Suffolk sandy loam (fine-loamy, siliceous, thermic Typic Hapuldult) soil in each of three years. Nematode-susceptible soybeans were seeded following forage removal. Soil samples for nematode counts were taken immediately before soybean harvest each year. In another experiment, one cultivar each of annual ryegrass, wheat, and rye, and a fallow control were followed by three soybean cultivars selected for differing nematode susceptibility. Grass cultivars did not affect nematode populations under succedding soybean. The only nematodes affected by grass species in either experiment were Pratylenchus spp., Heterodera glycines Ichinohe, and Tylenchorhynchus claytoni (Kofoid and White) Chitwood. Nematode population means were usually low following ryegrass and high following the fallow control. High soybean yields followed the fallow control, and low soybean yields followed annual ryegrass.     

Arbuscular mycorrhizal fungi and plant symbiosis in a saline-sodic soil

The seasonality of arbuscular mycorrhizal (AM) fungi–plant symbiosis in Lotus glaber Mill. and Stenotaphrum secundatum (Walt.) O.K. and the association with phosphorus (P) plant nutrition were studied in a saline-sodic soil at the four seasons during a year. Plant roots of both species were densely colonized by AM fungi (90 and 73%, respectively in L. glaber and S. secundatum) at high values of soil pH (9.2) and exchangeable sodium percentage (65%). The percentage of colonized root length differed between species and showed seasonality. The morphology of root colonization had a similar pattern in both species. The arbuscular colonization fraction increased at the beginning of the growing season and was positively associated with increased P concentration in both shoot and root tissue. The vesicular colonization fraction was high in summer when plants suffer from stress imposed by high temperatures and drought periods, and negatively associated with P in plant tissue. Spore and hyphal densities in soil were not associated with AM root colonization and did not show seasonality. Our results suggest that AM fungi can survive and colonize L. glaber and S. secundatum roots adapted to extreme saline-sodic soil condition. The symbiosis responds to seasonality and P uptake by the host altering the morphology of root colonization.     

Newly acquired feeding habits among the chimpanzees of the Mahale Mountains National Park,Tanzania

The M group chimpanzees (Pan troglodytes schweinfurthii) of the Mahale Mountains National Park, Tanzania, began to feed on three agricultural fruit species, guava, mango and lemon. It took them 7–8 years until they began to taste these fruits since the villagers left the park area in 1974. Although adult chimpanzees are conservative in their feeding habits, they are capable of rapidly acquiring new feeding habits, or new traditions, once they notice that the food is suitable.     

A case of unusually early postpartum resumption of estrous cycling in a young female chimpanzee in the wild

A case of unusually early postpartum resumption of estrous cycling (<7 months) was recorded for a young, presumably primiparous female in the M group of chimpanzees (Pan troglodytes schweinfurthii) in the Mahale Mountains National Park, western Tanzania. The female showed estrous cycling while lactating her infant, and mated with young and low-ranking males as well as with the alpha male.     

Factors Affecting Party Size in Chimpanzees of the Mahale Mountains

We studied factors affecting party size and composition of wild chimpanzees at Mahale (M group) over an 11-month period. Parties with 1–5 individuals were most frequent (37.8%; 153/405 parties); they included 94.7% of all male parties (n = 76) and 81.3% of all female parties (n = 75). The median of monthly values was the standard for analysis. We divided the year into four periods based on the median size of monthly bisexual parties (30.9 individuals; includes both males and females): monthly bisexual party sizes were larger in May–June (period II) and October–January (period IV) and smaller in February–April (period I) and July–September (period III). Only bisexual parties changed in size with period. The number of fruit items (=species) eaten was fewer in periods II and IV when abundance per item appeared to be great. The sizes of bisexual parties, which included cycling females with maximal anogenital swelling, were larger, and their representation (%) in all bisexual parties was greater in periods III and IV. The numbers of both cycling females and cycling females with maximal anogenital swelling were also larger in periods III and IV. The percentage of cycling females with maximal anogenital swelling was greater in periods II and III. The results of this study and those of Nishida (1979) suggest that seasonal variation in party size of Mahale chimpanzees maintains a relatively consistent annual cycle. The factors assumed to affect party sizes are fruit availability and the presence of cycling females with maximal anogenital swelling.