Shunji Gotoh

Seasonal trends in intestinal nematode infection and medicinal plant use among chimpanzees in the Mahale Mountains, Tanzania

A longitudinal study of nematode infection in chimpanzees was conducted between 1989 and 1994 on the M group chimpanzees of the Mahale Mountains National Park, Tanzania during two annual dry and rainy season periods and a third rainy season. Chemical and physical antiparasite properties of medicinal plant use against the strongyle nematodeOesophagostomum stephanostomum have recently been reported at Mahale. Here, the incidence of nematode infections were analyzed for seasonal trends to elucidate the possible influence of parasite infection on previously reported seasonality of medicinal plant use and to test the hypothesis that the use of these plants is stimulated byO. stephanostomum. The number of chimpanzees infected byO. stephanostomum was significantly higher in the rainy season than in the dry season of both 1989–1990 and 1991–1992. However, the incidence ofTrichuris trichura andStrongyloides fuelleborni showed no seasonality. Reinfection of individuals byO. stephanostomum occurred in synchrony with annual variation in rainfall: there was a sharp rise in the occurrence of new infections per individual within one to two months after the beginning of the first heavy rains of the season. This pattern coincides with the reproductive cycle of this nematode species.O. stephanostomum (95%) infections were associated significantly more frequently with medicinal plant use than eitherT. trichiura (50%) orS. fuelleborni (40%) infections. These observations are consistent with previous reports for the increased use of these plants during the rainy season and are consistent the hypothesis that medicinal plant use is stimulated byO. stephanostomum infection.

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.

AGE-RELATED CHANGES IN THE LIPOFUSCIN ACCUMULATION OF BRAIN AND HEART

Lipofuscin is the end-product of intracellular lipid peroxidation and the accumulation results from the cellular metabolism during aging (life stage). We suggested that the accumulation of cardiac lipofuscin was dependent on the specific metabolic rate of mammals. Slower rate of cardiac lipofuscin accumulation (against absolute lifespan) was observed in the animals of larger body size. The rate of cardiac lipofuscin accumulation was correlated with the specific metabolic rate, and inversely correlated with the brain weight of mammals. The first appearance of lipofuscin granules was 8 weeks of age in the hippocampus and in the thalamus. In the case of cerebral cortex (laminae III), lipofuscin granules were first found at 3-month-old rats. The rate of lipofuscin accumulation was the highest in the hippocampus (y = 0.286x - 0.099, r = 0.963) among the three regions examined. In the case of cerebral cortex and thalamus, the slower rate of lipofuscin accumulation was observed (y = 0.072x - 0.14, r = 0.797 for cerebral cortex; y = 0.067X - 0.14, r = 0.953 for thalamus). It is noticed that the most abundant accumulation and the highest rate of lipofuscin accumulation are the hippocampus. Even the hippocampus, the rate and the magnitude of lipofuscin accumulation was low as compared with cardiac muscles. From these results, it is suggested that brains have better protective system against oxidative stress than other organs do.

High prevalence of infection with Entamoeba dispar, but not E. histolytica, in captive macaques

Abstract A total of 268 nonhuman primates (20 species) kept in the Primate Research Institute, Kyoto University, Japan, were surveyed for intestinal amebas. Total positive rates as based on the presence of cysts in the stool following formalin-ether sedimentation were as follows: Entamoeba histolytica/E. dispar, 53%; E. coli, 34%; E. hartmanni, 34%; Iodamoeba buetschlii, 25%; Endolimax nana, 8%; and E. chattoni, 3%. Positive rates were higher in Old World monkeys and lower in New World monkeys. All the 141 E. histolytica/E. dispar-positive animals were Macaca monkeys. The E. histolytica/E. dispar-positive samples were analyzed by polymerase chain reaction (PCR) for identification of E. histolytica and E. dispar. E. dispar DNA was detected in 137 samples, whereas no E. histolytica DNA was seen. Zymodeme analysis and reactivity to monoclonal antibodies of cultured trophozoites also supported the presence of E. dispar and the absence of E. histolytica. When the sera of 93 macaques were examined by an indirect fluorescent antibody test, only 3 animals proved to be positive for E. histolytica, showing the lowest titer. These results demonstrate that infection with E. dispar, but not E. histolytica, is predominant in macaques.

Yersinia pseudotuberculosis infection in breeding monkeys: detection and analysis of strain diversity by PCR

In the last three decades, several monkeys reared in outdoor/indoor–outdoor breeding colonies and cages of the Primate Research Institute, Kyoto University, died of yersiniosis caused by Yersinia pseudotuberculosis, necessitating introduction of a method to detect the bacteria rapidly and thus allow preventive measures to be undertaken. A rapid nested polymerase chain reaction (PCR) method for identification of Y. pseudotuberculosis in fecal samples and a random amplified polymorphic DNA (RAPD)‐PCR approach for distinguishing between bacterial strains were therefore developed. Yersinia pseudotuberculosis isolates from monkey specimens were found to be classifiable into several types. To determine the source of infection, hundreds of fecal samples of wild rats, pigeons, and sparrows were collected from around the breeding colonies and cages, and subjected to PCR analyses. Yersinia pseudotuberculosis was detected in 1.7% of the fecal samples of wild rats. The DNA fingerprints of the bacteria revealed by RAPD‐PCR were the same as that of one strain isolated from macaques, suggesting the wild rat to be a possible source of infection.

Regional differences in the infection of wild Japanese macaques by gastrointestinal helminth parasites.

A coprological survey of gastrointestinal parasites in wild Japanese macaques (Macaca fuscata), from 14 natural habitats was done. Ova of five nematode species (Trichuris trichiura, Strongyloides fuelleborni, Streptopharagus pigmentatus, Oesophagostomum aculeatum, andGongylonema species) and a worm of the cestode species,Bertiella studieri, were detected. Some differences found in rates of infection by sex were observed in the 14 areas. Differences based on age were found in only troops in which the infection rates ofStrongyloides fuelleborni, Streptopharagus pigmentatus, andTrichuris trichiura were higher in the juvenile monkeys. The number of parasite species was related to the geographical and climatic conditions of the habitat of the troop: troops living in areas cold in winter were infected by fewer parasite species than those in southern warmer areas.

Accumulation of cardiac lipofuscin in crab-eating monkeys (Macaca fasicularis): The same rate of lipofuscin accumulation in several species of primates

Previously, we have reported that the aging process begins at sexual maturation (Nakano, M. et al., Mech. Ageing Dev., 52 (1990) 93-106). In this paper, we reported the cardiac lipofuscin accumulation of crab-eating monkeys. The first appearance of cardiac lipofuscin was around sexual maturation, and the rate of accumulation in crab-eating monkey was 0.45. Several primates which have different life spans show the same rate of lipofuscin accumulation in the life stage. Namely, even in a different life span, the amount of lipofuscin accumulation in a given period of life such as puberty, middle age, old age was the same. From these results, it is suggested that the amount of lipofuscin accumulation is the same in the life span of primates having different life spans.

A cytogenetic study on congenital limb malformations in the Japanese monkey (Macaca fuscata)

A cytogenetic investigation was performed on 88 Japanese monkeys (Macaca fuscata) with abnormal limbs from 11 free-ranging provisioned troops including nine individuals with abnormalities indistinguishable as to whether they were congenital or injurious. All of the monkeys with abnormal limbs including the nine questionable individuals had the same karyotypes as those of normal individuals. The chromosome number was 42, consisting of 20 bi-arm autosome pairs and a submetacentric X-chromosome and Y-chromosome. The ninth chromosome pair, which was the only chromosome pair with remarkable secondary constriction, displayed length polymorphism of the centromeric C-band and secondary constriction in both deformed and normal monkeys. These kinds of variants have also been commonly found in other monkey species, which have almost the same karyotype as the Japanese monkey and have not been reported to show frequent occurrence of limb malformation. We concluded therefore that chromosomal abnormalities could be excluded from the main causal factors for limb malformations of the Japanese monkey.

A Population-Genetic Study of Crab-Eating Macaques (Macaca fascicularis) on the Island of Angaur, Palau, Micronesia

Blood protein polymorphisms of an introduced population of the crab-eating macaques on Angaur Island, Palau, Micronesia, were examined electrophoretically to assess genetic variability. Results showed a high degree of genetic heterozygosity and some distinctive features in the genetic constitution of this island population. Negative evidence is presented regarding ancestry from a single pair of macaques. Their origin is discussed in relation to the genetic structure of the present population.

One-trial long-lasting food-aversion learning in wild Japanese monkeys (Macaca fuscata)

We examined how Japanese monkeys in the wild formed an aversion to food which had been paired with poison. Ten monkeys of various ages and both sexes were chosen as subjects from 105 members of the Shiga-A1 troop at Jigokudani in Shiga Heights in Japan. We gave almond nuts to each subject. Once a monkey ate 10-20 almond nuts, he was captured and moved into an injection cage. Seven experimental subjects were injected intravenously with cyclophosphamide (20 mg/kg). Three control subjects received the same treatment except that they were injected with physiological saline. About 1 hour later, all subjects were released into the troop. The tests for conditioned aversions were conducted during the next 2 days. In the tests, the experimental subjects would not eat almond nuts, while the control subjects showed no hesitation in eating them. Five of the seven experimental subjects retained perfectly the aversion to almond nuts in tests conducted 1 month and 3 months later. The one-trial long-lasting food-aversion learning shown by the wild Japanese monkeys is discussed in terms of their feeding strategy. These results also suggest that food-aversion conditioning has potential as a nonlethal method for controlling crop-raiding monkeys.