Michael A. Huffman

Animal self-medication and ethno-medicine: exploration and exploitation of the medicinal properties of plants

Early in the co-evolution of plant-animal relationships, some arthropod species began to utilize the chemical defences of plants to protect themselves from their own predators and parasites. It is likely, therefore, that the origins of herbal medicine have their roots deep within the animal kingdom. From prehistoric times man has looked to wild and domestic animals for sources of herbal remedies. Both folklore and living examples provide accounts of how medicinal plants were obtained by observing the behaviour of animals. Animals too learn about the details of self-medication by watching each other. To date, perhaps the most striking scientific studies of animal self-medication have been made on the African great apes. The great ape diet is often rich in plants containing secondary compounds of non-nutritional, sometimes toxic, value that suggest medicinal benefit from their ingestion. Chimpanzees (Pan troglodytes), bonobos (Pan paniscus) and gorillas (Gorilla gorilla) are known to swallow whole and defecate intact leaves. The habit has been shown to be a physical means of purging intestinal parasites. Chimpanzees and man co-existing in sub-Saharan Africa are also known to ingest the bitter pith of Vernonia amygdalina for the control of intestinal nematode infections. Phytochemical studies have demonstrated a wide array of biologically-active properties in this medicinal plant species. In light of the growing resistance of parasites and pathogens to synthetic drugs, the study of animal self-medication and ethno-medicine offers a novel line of investigation to provide ecologically-sound methods for the treatment of parasites using plant-based medicines in populations and their livestock living in the tropics.

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.

Current evidence for self-medication in primates: A multidisciplinary perspective

The study of self-medication in non-human primates sheds new light on the complex interactions of animal, plant and parasite. A variety of non-nutritional plant secondary compounds and nutrient-poor bark is found in the primate diet, but little is yet known about the possible medicinal consequences of their ingestion. Recent studies of the African great apes support a hypothesis in progress that the non-nutritional ingestion of certain plant species aid in the control of parasite infection and provide relief from related gastrointestinal upsets. Detailed behavioral, pharmacological and parasitological investigations of two such behaviors, bitter pith chewing and leaf swallowing, have been conducted on three East African chimpanzee populations, but they are now known to occur widely among all chimpanzee subspecies, as well as bonobos and lowland gorillas. For both bitter pith chewing and leaf swallowing, selection of the same plant species tends to occur among neighboring groups of same ape species. These local cultural traditions of plant selection may be transmitted when females of the same species transfer into non-natal groups. However, selection of the same plant species or species of related plant genera by two sympatric ape species or between regional populations of great ape subspecies strongly suggests a common criteria of medicinal plant selection. This and the intriguing observa- tion that the same medicinal plant is selected by apes and humans with similar illnesses provide insight into the evolution of medicinal behavior in modern humans and the possible nature of self-medication in early hominids. The occurrence of these and other specific self-medicative behaviors, such as fur rubbing and geophagy, in primates and other animal taxa suggest the existence of an underlying mechanism for the recognition and use of plants and soils with common medicinal or functional properties. Yrbk Phys Anthropol 40:171-200, 1997. r 1997 Wiley-Liss, Inc.

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.

Self-Medicative Behavior in the African Great Apes: An Evolutionary Perspective into the Origins of Human Traditional Medicine

by observing a similarly sick young porcupineingest the roots ofthe plant.Before these opportune obser-vations,Babu Kalunde and the people ofhis village hadavoided this plant,which they knew to be highly poisonous.After telling the villagers his story ofthe porcupine,however—and taking small doses ofthe plant himself—he persuadedthem to use the plant on the sick.To this day,the WaTongweuse the roots ofmulengelele as medicine.Babu’s grandson,Mohamedi Seifu Kalunde,now a respected elder and healerhimself,uses this plant to also treat gonorrhea and syphilis.By comparison with Babu,scientists are latecomers to thestudy ofanimal self-medication and its possible applicationsfor modern medicine.In recent years,however,a growing bodyofscientific evidence has been gathered in support ofanimalself-medication,or zoopharmacognosy (Huffman 1997).Starting with chance observations ofa sick chimpanzee in 1987(Huffman and Seifu 1989),Mohamedi and I have worked to-gether with a growing group ofcollaborators to learn howchimpanzees in the wild deal with parasites and what their be-havior can tell us about treating other diseases.Unnecessary for nutrition,growth,or reproduction,the sec-ondary compounds in a plant have evolved to give protectionfrom insect and mammalian predators.Whereas ecologistswho study animal foraging behavior focus on how animalscope with these secondary compounds in their diet (Freelandand Janzen 1974,Glander 1975,1982,Hladik 1977,Janzen1978,Wrangham and Waterman 1981),the basic premise ofzoopharmacognosy is that animals utilize these secondarycompounds to medicate themselves.Taking a broader per-spective,we are interested in putting these lessons ofevolu-tionary medicine to practical use for humans (Huffman andSeifu 1989,Ohigashi et al.1994,Plotkin 2000).Much ofthe plant material that is consumed by animals inthe wild contains an array ofsecondary compounds.Johns(1990) argues that the herbal medicines and modern phar-maceuticals used by humans today have replaced the non-nutritive chemicals commonly present in our primate an-cestors’diets.In this light,the nonnutritive components ofitems ingested by African great apes—and,indeed,all

Molecular ecology and natural history of Simian foamy virus infection in wild-living chimpanzees

Identifying microbial pathogens with zoonotic potential in wild-living primates can be important to human health, as evidenced by human immunodeficiency viruses types 1 and 2 (HIV-1 and HIV-2) and Ebola virus. Simian foamy viruses (SFVs) are ancient retroviruses that infect Old and New World monkeys and apes. Although not known to cause disease, these viruses are of public health interest because they have the potential to infect humans and thus provide a more general indication of zoonotic exposure risks. Surprisingly, no information exists concerning the prevalence, geographic distribution, and genetic diversity of SFVs in wild-living monkeys and apes. Here, we report the first comprehensive survey of SFVcpz infection in free-ranging chimpanzees (Pan troglodytes) using newly developed, fecal-based assays. Chimpanzee fecal samples (n = 724) were collected at 25 field sites throughout equatorial Africa and tested for SFVcpz-specific antibodies (n = 706) or viral nucleic acids (n = 392). SFVcpz infection was documented at all field sites, with prevalence rates ranging from 44% to 100%. In two habituated communities, adult chimpanzees had significantly higher SFVcpz infection rates than infants and juveniles, indicating predominantly horizontal rather than vertical transmission routes. Some chimpanzees were co-infected with simian immunodeficiency virus (SIVcpz); however, there was no evidence that SFVcpz and SIVcpz were epidemiologically linked. SFVcpz nucleic acids were recovered from 177 fecal samples, all of which contained SFVcpz RNA and not DNA. Phylogenetic analysis of partial gag (616 bp), pol-RT (717 bp), and pol-IN (425 bp) sequences identified a diverse group of viruses, which could be subdivided into four distinct SFVcpz lineages according to their chimpanzee subspecies of origin. Within these lineages, there was evidence of frequent superinfection and viral recombination. One chimpanzee was infected by a foamy virus from a Cercopithecus monkey species, indicating cross-species transmission of SFVs in the wild. These data indicate that SFVcpz (i) is widely distributed among all chimpanzee subspecies; (ii) is shed in fecal samples as viral RNA; (iii) is transmitted predominantly by horizontal routes; (iv) is prone to superinfection and recombination; (v) has co-evolved with its natural host; and (vi) represents a sensitive marker of population structure that may be useful for chimpanzee taxonomy and conservation strategies.

CHAPTER 13 – Acquisition of Innovative Cultural Behaviors in Nonhuman Primates: A Case Study of Stone Handling, a Socially Transmitted Behavior in Japanese Macaques

The question of whether or not animals have culture, and if they do have, how does animal culture differs from that of humans has long been a topic of interest and debate. The pioneering studies of Japanese macaques have brought the biologists closer to answering these questions and have played a significant part in bringing to light the importance of social learning in nonhuman primates. To date, all newly acquired cultural behaviors reported in Japanese macaques have in common the fact that they are subsistence oriented and thus provide direct benefits to the user in daily feeding activities. Monkeys who wash sweet potatoes, dip them in salt, or separate sand from wheat, are benefiting from their efforts. It is possible that the observations of direct benefits acquired by individuals from practice of these behaviors actually encourage their wide diffusion. While not every socially learned behavior is or has to be adaptive, the propensity to learn and adopt new behaviors surely is adaptive in most circumstances. Perhaps someday because of the experience gained from stone handling, a new behavior of adaptive value to the troop will arise. However, in its present state stone handling, rather than being the means to an end, appears to be rewarding in itself.

Reproductive parameters of female Japanese macaques: Thirty years data from the arashiyama troops, Japan

Over a 30-year period from 1954 to 1983, 975 live births were recorded for Japanese macaque females at the Iwatayama Monkey Park, Arashiyama, Japan. Excluding unknown birth dates, primiparous mothers gave birth to 185 infants (182 cases with age of mother known) and multiparous mothers gave birth to 723 infants (603 cases with age of mother known). The peak month of birth was May with 52.3% of the total births occurring during the period. Multiparous females who had not given birth the previous year did so earlier than multiparous females who had given birth the previous year and also earlier than primiparous females. Among the females who had given birth the previous year, females whose infant had died gave birth earlier than females who had reared an infant the previous year. The offspring sex ratio (1:0.97) was not significantly different from 1:1, and revealed no consistent association with mothers age. Age-fecundity exhibited a humped curve. The annual birth rate was low at the age of 4 years but increased thereafter, ranging between 46.7% and 69.0%, at between 5 and 19 years of age, but again decreased for females between 20 and 25 years of age. Some old females displayed clear reproductive senescence. The infant mortality within the first year of age was quite low (10.3%) and the neonatal (less than 1 month old) mortality rate accounted for 49.0% of all infant deaths. There was no significant difference between the mortality rates of male and female infants. A females rank-class had no apparent effect on the annual birth rate, infant mortality, and offspring sex ratio. These long-term data are compared with those from other primate populations.

Stone-play of Macaca fuscata in Arashiyama B troop: Transmission of a non-adaptive behavior

Stone-play, a directly non-adaptive behavior, was observed in the free-ranging Arashiyama B troop of Japanese macaques near Kyoto, Japan. Stone-play was classified into eight types characterized by gathering, picking up, scattering about, rolling in hands, rubbing in hands, clacking, carrying, or cuddling, of stones. The behavior, first observed in 1979, spread throughout 49% (n=236) of the troop by 1984. Infants and juveniles of both sexes accounted for 80% (n=92), while the remaining 20% were young adult males (6) and females (6) or adult females (11). Unlike other reported cases of novel cultural behaviors, this non-adaptive behavior initially diffused among younger individuals and was then later transmitted in form of tradition from these individuals to their offspring or younger sibs and playmates.

Monkeys in the Middle: Parasite Transmission through the Social Network of a Wild Primate

In wildlife populations, group-living is thought to increase the probability of parasite transmission because contact rates increase at high host densities. Physical contact, such as social grooming, is an important component of group structure, but it can also increase the risk of exposure to infection for individuals because it provides a mechanism for transmission of potentially pathogenic organisms. Living in groups can also create variation in susceptibility to infection among individuals because circulating levels of immunosuppressive hormones like glucocorticoids often depend on an individual’s position within the group’s social structure. Yet, little is known about the relative roles of socially mediated exposure versus susceptibility in parasite transmission among free-living animal groups. To address this issue, we investigate the relationship between host dominance hierarchy and nematode parasite transmission among females in a wild group of Japanese macaques (Macaca fuscata yakui). We use social network analysis to describe each individual female’s position within the grooming network in relation to dominance rank and relative levels of infection. Our results suggest that the number of directly-transmitted parasite species infecting each female, and the relative amount of transmission stages that one of these species sheds in faeces, both increase with dominance rank. Female centrality within the network, which shows positive associations with dominance hierarchy, is also positively associated with infection by certain parasite species, suggesting that the measured rank-bias in transmission may reflect variation in exposure rather than susceptibility. This is supported by the lack of a clear relationship between rank and faecal cortisol, as an indicator of stress, in a subset of these females. Thus, socially mediated exposure appears to be important for direct transmission of nematode parasites, lending support to the idea that a classical fitness trade-off inherent to living in groups can exist.