Abstract

The author describes a study of parasites in eastern lowland gorillas (Gorilla beringei graueri) and compares the results with studies of (Gorilla gorilla gorilla) and (Gorilla beringei beringei) to support the discussion of factors that influence the parasite status in these species. Beside environmental conditions and intrinsic host factors the social structure and behaviors of the host social unit may play a role in pathogen spread. If pathogen spread is influenced by social barriers (access to the group members) it will work as an evolutionary force by patterning the behavior of the host. The importance of a holistic approach in conservation medicine is stressed for a better understanding of the complex natural network between individuals, groups, the environment, and their pathogens.

Introduction

Several behaviors may influence the spread of pathogens within and between animal groups. New behavior patterns may evolve in response to exposure to pathogens that minimize the probability of acquiring these organisms and that minimize the pathogenicity of organisms they already harbor. In this study the factors influencing parasite transmission in gorillas are used as an example that may reflect general factors that impact the spread of other pathogens.

Methods

Fecal samples from 56 eastern lowland gorillas (Gorilla beringei graueri; ELG) were collected over a 6-month period of time and were examined for the presence of endoparasites. The gorillas live in four different social groups in the eastern Congolese Kahuzi-Biega National Park. Fecal samples from the park staff and their families were also evaluated quarterly. All feces were processed using the standard Merthiolate-iodine-formalin concentration (MIFC) technique and were examined microscopically. Individual, social group, and ecologic data were collected. The standard deviation in a 90% confidence interval was calculated. Data of the other two subspecies were compared.

Results

The investigated gorilla subspecies show marked differences in the endoparasite prevalence and slight differences in the endoparasite species spectrum (Table 1). The ELG take a middle position between the western lowland gorillas (WLG) (Gorilla gorilla gorilla) and the mountain gorillas (MG) (Gorilla beringei beringei) in their parasite prevalence. ELG share four nematode species and a cestode with MG, whereas they have only one nematode in common with WLG. ELG shed all common parasites much less often than MG and a bit more often than in WLG.

Table 1. The endoparasites of the three gorilla subspecies^1,2,6,10-13

x = found but not quantified, - = not found

Studies of other primate species have shown that the humid conditions found at higher altitudes are more conducive to the development of many parasite life stages than the arid conditions found at lower altitudes. The ELG studied in this investigation were keeping a middle position not only in their parasite spectrum but also in the social structure (group size), demographic factors (population density, habitat size), and ecologic conditions (altitude, rainfall, temperature, humidity) of their habitat.^4,9 While the thin walled nematode species in this investigation seemed to be less influenced by climate seasons and diet, the cestode transmitted by a soil mite and the unspecified larvae (possible Probstmayria) varied clearly with climate seasons and the uptake of different vegetation where they either had more contact with soil or ground vegetation. All three gorilla subspecies have marked different diets, so that their possible contact to infectious stages might vary intensively.

Investigations of park personnel and their families of the Kahuzi-Biega National Park showed a prevalence of helminth infestation of 57% (89% in Uganda).^1,6 The identified spectrum of helminths was not the same as was seen in the gorillas, but all of the parasites found in the park personnel have the potential to infect primates under captive situations. MG live in an area with one of the highest human population densities in the world, while the WLG are surrounded by a population of very low density. The investigated ELG had more regular contact with tourists than WLG and less contact with tourists than MG during the time of the investigation.

The risk of infection for pathogens of social primates has been positively correlated with the group size.⁷ The two larger groups of the ELG studied showed a higher parasite prevalence than was seen in the two smaller groups. The risk of infestation was not directly linear with the number of group members so that other confounding factors could be assumed. The ELG have larger average group sizes than WLG and about the same average group size as MG. The daily ranging length was not positively correlated with the group size as it has been described for MG.¹⁹

The risk of infection is correlated with primate population density. While investigated ELG and WLG live in about the same population density; MG live in a higher population density.⁴

A context between repeated trail, feeding, and sleeping area use and increased parasite prevalence has been found for several primate species.^7,8,16,17 For the ELG, the group with the highest territory overlap and shortest day ranging length had the highest prevalence, those with the longest daily ranging length and the lowest territory overlap had the lowest prevalence. MG have the smallest home range and ELG the largest. The reuse of the same feeding and sleeping areas in intervals where pathogens are still infectious should increase the risk of primary infection and reinfection. MG show a different pattern of feeding patch reuse than ELG. Gorillas do not sleep in the same night nest twice. For ELG and WLG it is proven that they avoid the same nest building sites for at least 54 days, which is longer than the infectious period of all the nematode stages identified in gorillas.^4,6

Parasites can reduce the reproductive success of their hosts.³ As many parasites and their hosts have co-evolved over a long period of time, one should assume the development of infection avoiding or minimizing strategies.^7,8 Only 18% of the ELG defecate in their nests and only 9% have been proven to lay on the feces but the majority of MG defecate in their nests and 73% lay on their feces.^5,9 The risk for the later subspecies to be infected by their mothers with percutaneous transmitted helminths must be higher. Indeed, MG showed a higher prevalence of percutaneous transmitted Strongyloides fuelleborni than ELG, the immature age groups had a marked higher prevalence than the adults.²

The self-medication with plants that contain antiparasitic toxins (e.g., Vernonia amygdalina, Balanites) has been seen in several primate species. ELG have been seen eating a plant that is used by local tribes against parasites.⁶ All of these behavior patterns might be adaptations to different pathogen pressure under different environmental and social conditions.

In this investigation milk-borne transmission as well as an influence of the behavior patterns of the mother on the parasite status of the suckling young seems unlikely, as no correlation between their endoparasite status could be detected. An increase of the prevalence of all endoparasite species from infants to juveniles could be demonstrated. The parasites prevalence of Oesophagostomum and Anoplocephala increased until adulthood, the later has also been described for MG.

Differences in the parasite prevalence between the sexes were slight. Females, especially lactating females, excreted larvae more often than males. Explanations for this can be different feeding strategies. A different helminth egg output of females in different reproductive stages has been found in other primates as well. For pregnant and lactating MG females a higher food intake than non-lactating females could be demonstrated. Also, a post-parturient rise of some strongyles can increase the egg excretion of lactating females.

Higher stress levels might lead to an increased helminth egg output. Investigations of other primates showed that the predictability of the social position in primates reduces stress, which can induce subclinical disease.¹⁵ For female MG no linear hierarchy could be found,¹⁶ they might change between groups several times in their life, which means that they have to reestablish their social position, therefore producing stress and higher parasite loads.

Stuart and Strier (1995) presume that affiliative behavior between group members such as: grooming, genital inspection, and copulation between sexes in certain cycle stages should lead to a rise in contact transmitted pathogens.¹⁸ Silverbacks are the most frequent grooming partners of their females beside their last-born child in MG and ELG, therefore the breeding silverbacks might take a central position in pathogen transmission.¹⁶

Higher parasite loads of the males in primates with a marked sexual dimorphism can be explained with their higher food intake, the higher average age of the silverbacks for those species with an age correlated rising prevalence. ELG silverbacks showed a higher prevalence for Anoplocephala gorillae, and in MG they showed a higher egg output for this helminth species.³ The behavior of male ELG to sleep more often directly on the soil than in nests, should reduce their infection risk with percutaneous transmitted parasites,⁶ as investigations of soil versus grass have shown that the vegetation carried more infectious parasite stages than the soil.

Discussion

Disease is an important ecologic and mortality factor, and was stated the major regulator of primate populations by Schaller.¹⁴ All investigated gorillas were harboring parasites without clinical signs of disease, but for some of the identified parasites an increased in pathogenicity under stressful conditions has been documented. Human impact as well as a reduced territory size can lead to higher stress levels for social primates. Besides that, the alarming infestation of the park staff with parasites should lead to the implementation of a health program for them.

Behavior traits that might reduce infection risks for gorillas could be: the exclusiveness of home ranges, avoidance of proximity to humans, varying ranging patterns (daily ranging length/avoiding of patch reuse) avoiding sleeping sites during the period where the parasites remain infectious and the ingestion of medicinal plants. To give the gorillas the opportunity to express these behaviors, the protected habitat needs to be large and diverse enough to include all these facets. Whereas the needs for the different subspecies can vary markedly, they have not been sufficiently studied for all of them. Investigations on the carrying capacity of protected areas for gorillas have not taken into consideration most of these facts and are therefore questionable. The manager of the veterinary program for wild animals should have a broad insight into the complex interactions of factors that could possibly influence the endangered species health to be able to make sensitive decisions for conservation and health protection.

A multidisciplinary approach combining the knowledge of behavior patterns of a subspecies and the factors influencing the epidemiology is new and challenging in the health management of great apes and can help to give a better insight in the complex network of factors that impact the spread of contact transmitted diseases in this highly endangered species.

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