International Journal of Primatology, Vol. 16, No.

4, 1995

Primates and Parasites: A Case for a

Multidisciplinary Approach
Michael D. Stuart1 and Karen B. Strier2
Received January 31, 1994; revised August 30, 1994; accepted October 20, 1994

Examinations of primate parasitic infections can inform both primatologists

and parasitologists about evolutionary and ecological relationships.
Interspecific, intraspecific, and interindividual variation in parasitic infections
may correlate with environmental, demographic, behavioral, and human
variables. Understanding these relationships is particularly important for
conservation management issues for endangered species. We describe
techniques for the noninvasive collection and preservation of fecal samples
from wild primates and the salvaging of parasitological information from
primate hosts in the field.
KEY WORDS: primates; parasites; coevolution; field techniques; preservation; multidisciplinary approach.

INTRODUCTION

Examination of primate parasitic infections is one of the most promising areas for multidisciplinary research because of the insights that
comparative parasitic data can provide into primate sociality and habitat
use (Freeland, 1976, 1980; Hausfater and Watson, 1976). Understanding
the coevolutionary relationships that many parasites have established with
their primate hosts can also provide insights into phylogenetic and speciation events. These relationships are extremely complex, and oversimplification can lead to misinterpretations or the acceptance of unsubDepartment of Biology, University of North Carolina at Asheville, Asheville, North Carolina
28804.
Department of Anthropology, University of Wisconsin-Madison, Madison, Wisconsin 53706.

0164-0291/95/0800-0577$07.50/00 1995 Plenum Publishing Corporation

578

Stuart and Strier

stantiated conclusions. The risk is increased when results from one primate
population are extrapolated to other populations in different environments,
to other primate species with different social systems, or to other parasitic
species with different life cycles. Direct life cycles, indirect life cycles, intermediate hosts, and varying levels of host specificity must all be examined
independently. As the number of endangered primate species increases due
to tropical habitat disturbance, consideration of all potential sources of information about primates has become increasingly important to make
informed conservation decisions as well as to understand their natural history. It is therefore essential that primatologists be familiar with basic
parasitological concepts and how they can and cannot be applied in primate
studies. We provide an overview of primate-parasite coevolutionary and
behavioral and ecological relationships that may be helpful to primatologists ("fable I). We conclude with a discussion of basic methods for the field

Table I. Basic Parasitological Terminology, Standardized by the American Society of Parasitologists (Schmidt and Roberts, 1989; Margolis et at., 1982)
Density
Habitat
Incidence

Infrapopulation
Intensity
Locality
Mean intensity
Prevalence
Relative density or
Abundance
Site or Location
Suprapopulation

The number of individuals of a particular parasitic species per unit

area, volume, or weight of infected tissue
The chemical and physical environment and spatial location of the
parasite within the host
The number of new cases of a parasitic infection appearing in a
population within a given time period divided by the number of
uninfected individuals in the population at the beginning of the time
period, usually expressed as a percentage. This term has often been
confused with prevalence but should not be used since the numbers
of uninfected individuals are rarely known in wild populations
All individuals of a particular parasitic species occurring in a single
host
The number of individuals of a particular parasitic species in each
infected host; usually expressed as a numerical range
The geographic place of capture or collection of the host
The total number of individuals of a particular parasitic species in a
sample of a host species divided by the number of infected host
individuals in the sample
The number of individuals of a host species infected with a particular
parasitic species divided by the number of hosts examined; usually
expressed as a percentage
Prevalence times mean intensity or the total number of individuals of
a particular parasitic species in a sample of hosts divided by all
individuals of the host species examined (infected and uninfected
hosts combined)
The particular tissues, organs, or part of the host in which a parasite
was found
All individuals of a particular parasitic species in all stages of
development in all hosts in an ecosystem

Primates and Parasites

579

collection of parasitic data from wild primates for researchers not previously trained in parasitological techniques.
Parasito1ogical terminology been standardized by the American Society
of Parasitologists. A brief overview of the more commonly used terms has
been abstracted here from Schmidt and Roberts (1989). Those wishing a
more complete description of terms are referred to Margolis et 01. (1982).

COEVOLUTIONARY RELATIONSHIPS

The idea of host-parasite coevolution and simultaneous speciation has

long been one of the important unifymg concepts of parasitology and has
been formalized as a series of rules (Xible 11). Observed correlations between a number of host and parasitic tam have been used to postulate a
variety of theories of host evolution and zoogeographical distribution patterns. Examples include temnocephalid turbellarians on crustaceans (von
Ihering, 18911, sucking lice of mammals (Ewing, 1926), Opalina and frogs
(Metcalf, 1929, 1940), biting lice and birds (Kellogg, 1913; Harrison, 1914;
Hopkins, 19421, metastrongylid nematodes in mammals (Dougherty, 1949),
plagiorchioid digeneans and frogs (Brooks, 19771, pinworms and primates
(Brooks and Glen, 19821, and skin bacteria on primates (Kloos, 1979; 1983).
Brooks (1979) cautioned that two distinct processes, coaccommodation
and cospeciation, have often been labeled inappropriately as coevolution.
Accordingly, coaccommodation-the process of reconciliation between
parasite and host, which permits coexistence-must be distinguished from
cospeciation. Cospeciation, in turn, must be distinguished by whether speciation of a parasitic population occurs in conjunction with or because of
lhble 11. "Rules" in the Study of Host-Parasite Coevolution (After Brooks, 1979)
Farenholz' rule
Szidat's rule
Manter's rules

Eichler's Rule

Parasitic phylogeny mirrors host phylogeny

The more primitive the host, the more primitive the parasites that
it harbors
Parasites evolve more slowly than their hosts do
The longer the association with a host group, the greater specificity
exhibited by the parasitic group
A host species harbors the largest number of parasitic species in
the area where it has resided the longest, so if the same or two
closely related species of hosts exhibit a disjunct distribution and
possess similar parasite faunas, the areas in which the hosts occur
must have been contiguous at a past time
The more genera of parasites a host harbors, the larger the
systematic group to which the host belongs.

580

Stuart and Strier

host speciation or independently, by becoming established either in a different host species or in a different site in or on the same host.
Consideration of modern ecological and evolutionary principles suggests that application of these generalized rules or concepts may not always
be justified. Inglis (1965) pointed out potential problems in using hostparasite records to substantiate theories of specific evolutionary pathways.
First, the data used in these analyses may be incomplete, either because
surveys on parasites are often superficial or scanty or because host records
may be questionable, as in the case of human parasites found in monkeys
kept in captivity (Collet et al., 1986). Second, many parasites are not markedly host specific. A striking exception is that of the pinworms-members
of the nematode family Oxyuridae-which are highly host specific in the
Primates, including Homo sapiens (Brooks and Glen, 1982). Third, parasitism could have arisen independently many times under different conditions,
implying that two parasitic species living side by side may not have invaded
the host species at the same time, and that different parasitic species may
be at different levels of adaptation to the host. Fourth, the presence or
absence of an intermediate host in a life cycle could affect the level of
cospeciation with the definitive host. Finally, the presence or absence of a
given parasitic species in a particular host may reflect ecological factors,
such as exposure through diet or habits, or whether or not a suitable niche
is available within the body of the host, rather than coevolution per se.
Thus, birds and ground squirrels that nest underground together share fleas
despite their distant ancestry, while feather structure, rather than phylogenetic relationships, may control mallophagan (chewing lice) occurrence.
Furthermore, all animals feeding on the same intermediate host potentially
represent equal opportunities for colonization.
An additional problem in interpreting parasitic occurrence in a particular group of primate hosts is the typical parasitic pattern of overdispersion.
The nonrandom distribution of a parasitic species in its hosts means that,
in terms of parasitic numbers, the variance is greater than the mean. Some
host individuals will carry many individual parasites of a particular species,
many host individuals will have a few parasites, and some host individuals
will not have any parasites of that species. Various factors may account for
the overdispersion pattern observed in parasites. Hosts may differ in their
susceptibility to parasitic infection, both interspecifically and by age, sex, and
size or dominance rank (Hausfater and Watson, 1976). The host's health or
immune status can affect individual susceptibility. Differences in behavior
may expose some individuals or groups more than others. Local conditions
may vary for the parasite leading to differential exposure-e.g., heat vs. humidity and egg~larvalsurvivorship)-as well as for the host-e.g., availability
and exploitation of anthelminthic agents in diet. Indeed, almost any factor

Primates and Parasites

581

that generates heterogeneity in individuals or populations of hosts can lead

to variation in parasitic infections and an overdispersed pattern of infection.
Despite these caveats, Brooks' parsimony analysis provides a valuable
method for using parasitic data to evaluate evolutionary events within the
framework of a scientifically rigorous methodology (Wiley et at., 1991;
Brooks and McLennan, 1991; and Brooks and McLennan, 1993). Via this
approach, parasitic data have been employed to provide a robust time estimate of the origin of a taxon in the absence of a fossil record and to plot
biogeographic origins (Brooks, 1992), to obtain a measure of biodiversity
and to infer refugia (Gardner and Campbell, 1992), and to clarify the recent
nature of a series of colonizing and speciation events in Holarctic birds
and mammals (Hoberg, 1992). Glen and Brooks (1985, 1986), Brooks
(1988) and O'Connor (1984,1988) have profitably applied this methodology
to questions pertaining to primate biogeography and distribution. These
analyses illustrate how the appropriate use of parasitic data can contribute
to an understanding of diverse evolutionary phenomena.
ECOLOGICAL AND BEHAVIORAL RELATIONSHIPS

Ecological and behavioral factors complicate coevolutionary analyses,

but it is precisely the patterns of parasitic overdispersal based on primate
host heterogeneity that make the integration of parasitological and primatological data so informative. Unfortunately, some researchers tend to view
parasites merely as medical problems or as hideous invaders along for a
free ride. By definition, parasitism is a level of symbiotic relationship between two species: in this case, the parasite and its primate host. In the
original sense of the term, symbiotic relationships can range from obligatory
mutualism to commensalism to parasitism. Some may benefit the primate
host, some may cause no problems, others may cause problems only under
conditions of stress, and some may be highly pathogenic. Each species of
organism found in a primate's body can reflect both an ecological and an
evolutionary adjustment to the relationship, and therefore, each relationship must be viewed independently. However, from both an evolutionary
and an ecological perspective, it is clear that parasites and primates are
two components of a single greater ecological entity; whatever one symbiote
does will inevitably effect the other. Veterinary studies on domestic livestock (Dobson, 1964; Brunsdon and Vlassoff, 1971; Dunsmore, 1971) have
established that circulating hormones during estrus and lactation can influence the development and egg production of parasites. The same effects
are almost certain to occur with parasites of primates. Hosts have evolved
a number of parasitic avoidance behaviors, suggesting that natural selection

582

Stuart and Strier

pressures to control parasitic infections have played an important role in

primate behavioral evolution (Hart, 1990).
Quantification of differences in parasitic prevalence can help primatologists to identify behavioral or ecological constraints that may be
affecting particular populations, groups, genealogies, or individuals in different ways. Conversely, the behavioral patterns that primatologists
routinely observe in their study subjects can help parasitologists to interpret
variation in parasitic distributions. A review of the comparative parasitic
data available for primates indicates that some ecological and behavioral
relationships between primates and parasites can be widely generalized
across species, while others appear to be highly specific to particular cases.
Distinguishing between such generalized and specialized relationships, and
the interacting effects between different variables, will require additional
data from a greater diversity of species.
Comparative Parasite Data in Primates
Parasitic Habiliq. Moist conditions appear to promote opportunities for
reinfection and a higher prevalence of parasitic infections, perhaps because
many ova and larvae excreted in feces survive better in humid environments
than in arid ones (Hausfater and Meade, 1982). Comparative studies of
chimpanzees and baboons [Pan iroglodytes and Papio anubis (McGrew et al.,
198911, mantled howling monkeys Wlouatta palliata (Stuart et al., 1990)], and
muriquis [Brachyteles arachnoides (Stuart et al., 1993)l show consistently
higher prevalences of parasitic infections in primate populations inhabiting
more humid environments. This may be an artifact of greater species richness, but even within the same population, the prevalence of strongylid infection in mantled howling monkeys was four times higher in groups
occupying riverine forest habitats than in groups from tropical dry forest
habitats (Stuart et al., 1990). Conversely, arid conditions with isolated standing water sources (oases) will probably promote contamination of drinking
sources and higher infection levels. This is certainly true of human populations and the guinea worm (Dracunculus medinensis) but has only recently
begun to be investigated in wild primate populations. The consistent results
from these studies emphasize the importance of evaluating habitat effects
on parasitic viability and primate parasitic infections.
Differential Opportunities for Parasitic Pansmission. Increased contact
with hosts or infected fecal material at high population densities should
facilitate the transmission of parasites, but it is difficult to separate the
effects of differences in primate densities and habitats on parasitic infections. For example, the higher prevalence of parasitic infection among

Primates and Parasites

583

baboons and chimpanzees at Gombe National Park compared to those at

Mt. Asserik may correspond to the higher population densities of both primates, as well as less arid conditions, at Gombe (McGrew et al., 1979).
Mantled howling monkeys at La Pacifica in Costa Rica had higher population densities and a greater prevalence of parasitic infections than those
at Santa Rosa National Park (Stuart et al., 1990). Contrarily, among muriquis the population with the lowest density had the greatest number of
parasitic species (Stuart et al., 1993). The fact that this population lived in
the most humid of the four habitats from which muriquis were sampled
suggests that parasite viability in different habitats may be a better predictor
of parasitic infection than primate density.
Freeland's (1976) hypothesis that primate group sizes might be constrained by the risks of transmission of infectious pathogens has received
mixed support. Appleton et al. (1986) found a lower prevalence of parasitic
infections in smaller baboon troops in the Drakensberg Mountains than in
larger groups that range at lower altitudes. Similarly, group size and enteric
parasite infections covaried among three baboon troops sampled at Gombe
National Park (McGrew et al., 1986). Malarial infection rate is correlated
with body weight and group size among Amazonian primates (Davies et
al., 1991). However, in a comparison of four muriqui populations, the largest group with the most cohesive grouping patterns had the lowest level of
intestinal helminth infections (Stuart et al., 1993). The absence of parasites
in the feces of sympatric brown howling monkeys (Alouatta fusca), which
occur in small groups, suggests that primate parasites may be rare, or absent altogether in this habitat, rendering the effects of group size on
infectious parasitic transmission irrelevant in this case.
Behavioral differences among individuals within primate groups may
affect their differential exposure to infectious parasites. In particular, social
interactions that involve contact or close proximity may increase the opportunities for infectious transmission. Accordingly, higher levels of parasites
might be expected in individuals that participate in such social interactions
more often. In a study of yellow baboons (Papio cynocephalus), Hausfater
and Watson (1976) found that high ranking males and sexually cycling females passed greater numbers of parasitic eggs than did subordinate males
and anestrous females, respectively. The reasons for these individual differences are not yet understood, but it is possible that more frequent grooming,
sexual inspections, or copulations among these individuals may explain the
observed variation in parasitic infections. It is also possible that physiological
differences between dominant and subordinate males, or cycling and anestrous females, affect the suitability of different individuals as parasitic hosts.
More integrated knowledge of parasitic and host behavioral biology, as well
as the effects of habitats on parasites, is clearly needed.

Stuart and Strier

5a4

Primate Behavioral Defenses. Primate habitat use and ranging patterns,

as well as mate choice, may be influenced by the risk of parasitic infection?
but such behavioral strategies appear to be highly specific and may be affected by confounding variables. A longitudinal study of yellow baboons
(Hausfater and Meade, 1982) indicated that avoidance of contaminated
sleeping sites was more marked during the rainy season than during the
dry season, presumably because the risk of infectious transmission was
higher during the rainy season when ova and larvae were less vulnerable
to desiccation. Freeland (19801, however, attributed the more restricted
ranging behavior of mangabeys (Cercmebus albigena) during the rainy season to the fact that heavy rains wash away contaminated feces from sleeping
areas and reduce the probability of infection.
Frequent relocation of foraging bases? precluding fecal accumulation
and constant exposure, may be related to the observation that human populations with nomadic subsistence patterns have a lower prevalence of
parasitic infection than more sedentary groups do (Chernela and Thatcher,
1989). Riverine troops of mantled howling monkeys, which have a greater
tendency to repeatedly use specific pathways, also have a higher prevalence
of parasites than troops that avoid contaminated pathways (Stuart et al.,
1990). In both human and nonhuman primate cases? it is difficult to determine whether minimizing the risk of contact with pathogens is a
consequence or a cause of differential foraging patterns.
The availability and exploitation of plants containing anthelminthic
agents by primates may also account for variation in parasitic infections
(Freeland, 197% Price et al., 1986). The nonnutritional use of plants with
demonstrated anthelminthic activity has been observed in two populations of
chimpanzees (Wrangham and Nishida, 1983; Huffman and S e f i ? 1989). Baboons inhabiting riverine areas with a high prevalence of Schistosoma also
feed selectively on Balanites berries, which are known to contain a saponin
that might indirectly affect the maturation of the worm (Phillips Conroyy
1986). Btablishing whether and how such bioactive compounds are metabolized by the primates that ingest them, and their effects on primate parasites,
is critical to interpreting these sugestive findings. This is clearly another area
for which further research into primate and parasitic relationship is needed.
INTERACTIONS AMONG V W L E S
It is evident from this brief review that the difficulties in teasing apart
the factors that lead to variation in primate parasitic infections are immense. Not only are parasite-host relationships complexy but also more
than one variable may operate on both parasites and hosts at any given

Primates and Parasites

585

time. The potential for such interacting effects between variables is especially high when human proximity or human activities are involved.
Primates that live in close proximity to humans may be infected
through contact with human feces, at least by parasites with a zoonotic
potential (Collet et al., 1986). Even without direct human contact, human
activities that disturb natural habitats create a mosaic of environments that
can also lead to variation in primate parasitic infections. Cutting of climax
forest may increase mosquito habitat and increase opportunities for malarial transmission. Primate populations suffering from severe habitat
disturbance may be restricted to a small area with greater opportunities
for infectious transmission of other parasites as well. Alternatively, disruption of complex ecological relationships between primates and parasites,
possibly through elimination of intermediate hosts, may lead to a lower
prevalence of infection than occurs in undisturbed populations.
The effects of human activities on primate parasitic infections must
be considered, along with other potentially confounding variables, before
understanding variability in primate-parasite relationships will be possible.
For example, among muriquis the highest levels of parasitic infection, in
terms of both number of parasitic species and percentage of infected hosts,
was detected in the population inhabiting the least disturbed-and most
humid-site (Stuart et al., 1993). Similarly, the higher parasitic infections
in mantled howling monkeys occupying riverine forest compared to those
in dry forest (Stuart et al., 1990) might be a consequence of (a) dietary
differences, if intermediate hosts such as insects are ingested along with
leaves at greater frequencies in riverine forest; (b) differences in ranging
patterns between the two habitats, which may lead to differences in fecal
contamination and contact, or (c) the greater viability of parasites in the
more humid riverine habitats. Ongoing studies by Stuart at La Pacifica, a
working cattle ranch in northwestern Costa Rica, suggest that even within
groups of relatively long-lived primates such as howling monkeys, the patterns of parasitic infection change with time and with recruitment of new
individuals into the host group.
FIELD COLLECTIONS

It should be clear that parasitology cannot be considered a silver bullet

or a panacea for understanding primate behavioral and ecological variation.
The difficulties of interpreting observed relationships between the many variables that may affect primate and parasitic distributions with the comparative
data presently available are compounded by the fact that the life cycles of
many parasites are still poorly known, particularly those that are endemic to

Stuart and Strier

586

endangered primates, and by the limitations of identifying parasitic species

solely from primate fecal samples. Nonetheless, the ease and economy, in
both time and money, of collecting primate fecal samples make them a relatively inexpensive means to collect parasitic data. That fecal samples also can
be obtained in a noninvasive way makes them the only source of parasitic
data for many endangered species. Furthermore, the potential value of parasitic data as a means to evaluate consenation management decisions and
habitat quality for endangered primates renders it almost obligatory for researchers to collect these data while it is still feasible to do so.
Fresh fecal material can be collected in the process of other behavioral
sampling, presemed, and shipped to a laboratory for subsequent analyses.
However useful, fecal collections are limited vis-2-vis the types of data that
can be retrieved. In cases of natural death or an accidental death while
capturing subjects for study or relocation, field primatologists may have
rare, but significant opportunities to contribute to knowledge of primates
and parasites if they are familiar with preparatory and presemative techniques and if they have included the basic supplies in their field kits.
We review a few basic principles of parasitology and the reasons behind the selection of certain techniques that will enable the primatologist
to salvage important parasitic specimens in a field situation. Fecal collection
tubes, basic preservation solutions, a box of microscopic slides and
coverslips, a dissection kit, a few vials, and latex gloves are the only essential
(and inexpensive) supplies involved (Pritchard and Kruse, 1982; Ash and
Orihel, 1987; Price, 1994).
Fecal Collections

Fecal samples, presemed in 10% formalin, can be analyzed easily for

the presence or absence of parasites and parasitic eggs or lamae. Identification of parasitic eggs, larvae, and oocysts from wild primates can be
difficult. Therefore, we urge more collaborative studies between primatologists and parasitologists, in which each specialist can use the expertise of
the other. Several useful parasitic identification guides for humans and for
domestic animals are available but, to the best of our knowledge, none has
been prepared for use with wild primates. Because feces do not require
freezing if presemed in solution, they can be easily transported as ordinary
baggage. Indeed, in the United States, fecal samples, even if obtained from
endangered primates, are classified by the U.S. Department of the Interior
as animal by-products and are, therefore, not subject to the same customs
restrictions as blood samples and body parts. However, the U. S. Department of Agriculture (USDA) and the Centers for Disease Control are

Primates and Parasites

587

responsible for control of imported materials of potential danger to domestic livestock and humans respectively. Giardia, Entamoeba, and
Enterobius vermicularis are potentially zoonotic and subject to control. At
this time, the USDA is not concerned with primate parasites and formalin
preservative will kill potential pathogens to the satisfaction of CDC. However, a telephone call to either agency will ease the potential for
time-delaying consultations with local agency representatives when trying
to clear customs on return to the United States. The same contact with
responsible agencies in other countries will be equally appropriate no matter what the researcher's country of origin. Internal permission to collect
and transport samples within host countries may also apply and obviously
any necessary permits should be obtained from the appropriate sources in
advance. Effective 1 January 1995, the International Air Transport Association and the U.S. Department of Transportation have implemented new
regulations for packaging all biological and diagnostic specimens containing
infectious materials. These rules and the interpretation of regulations by
USDA, CDC, and the U.S. Fish and Wildlife Service are subject to revision
and should be verified before collecting samples.
Fecal collection schedules may vary depending on the frequency with
which different primate species defecate, the quantity of material excreted,
and the degree of habituation and individual recognition available. Ideal
collections are made systematically, from recognized individuals that defecate in discrete areas. Samples should be collected over the course of an
annual cycle to detect the effects of climate, rainfall, and both parasite and
primate life cycles on infections. However, even temporally isolated samples
collected from unidentified individuals can provide useful information
about the presence or absence of different parasite species in a population.
Every effort should be made to get uncontaminated samples from isolated
and identified individuals. The date, time, and consistency of the sample,
and as much information about the individual providing the sample-sex,
age, dominance status, reproductive condition [estrous cycle, pregnancy,
and lactation-should be recorded.
Ideal fecal collecting vials are plastic with screw tops. Buffered 10%
formalin and polyvinyl alcohol (PVA) are the standard preservatives for fecal
samples. Several companies sell convenient premeasured two-vial systems,
with one vial containing forrnalin and the other PVA. The forrnalin gives
good preservation to helminth or worm eggs, while the PVA reduces damage
and distortion to single-celled protozoan trophs and cysts. A two-vial system
is definitely the best option, particularly to obtain usable protozoan samples.
We have tried vials from several different companies and found them all to
be effective under field conditions. Purchase of empty vials, caps, and sporks
combined with preparation of a stock solution of 10% buffered formalin

588

Stuart and Strier

and PVA is less expensive but can be inconvenient. While it is best to prepare and to carry your preservatives with you, in an emergency, comn~ercial
formaldehyde (37% formalin) can often be purchased locally and diluted at
a ratio of 9 parts water to 1 part formaldehyde.
Blood Samples
If blood is being taken from captured primates or as part of a necropsy,
a last drop can be squeezed from the needle onto the end of a clean microscopic slide. Hold a second slide at a 20-40' angle and push it across
the first slide, dragging the blood with it to make a thin smear. Practice is
required to become efficient at making good blood slides so make as many
as possible with the sample available until a consistent level of proficiency
is obtained. Air-dry and label with the host subject's individual number. If
the slides need to be held for more than 2 days before staining, we suggest
that they be dipped for 1 to 2 min in alcohol, preferably absolute methanol,
for fixing and then air-dried. Blood smears can be important to measure
the presence and prevalence of various species of primate malaria, trypanosomes, and microfilaria.
Before starting a blood survey, one should be aware of the potential
for zoonotic spread of simian viruses, particularly with African primates,
some of which may cause fatal infections in humans (Preston, 1992).
Ectoparasites and Pinworms
Arthropod and ectoparasites-fleas, lice, ticks-and pinworms should
be collected whenever live captures or necropsy opportunities permit.
Ectoparasites can be collected by searching the animals' fur and preserved
by simply dropping them into 70% ETOH and storing the vial with the
appropriate data. Clearing the exoskeleton and mounting should wait until
return to a laboratory.
Pinworms are especially common in many primate species but the eggs
are not often seen in fecal analysis. Presumably the female worm lays her
eggs in the perianal region in the same fashion as the human pinworm,
Enterobius vermicularis. As with humans, the surest method of detecting
their presence is first to stick a small piece of clear tape to the perianal
region and then seal the tape against a glass microscope slide. These slides
must be examined immediately since no preservative is applied. The presence of clear, asymmetrical-flattened on one side-eggs is a certain
indication of the worms. Pinworms also often pass in the feces when primates become excited. They may be picked out of fecal material or

Primates and Parasites

589

preserved along with the feces with a note on their presence so they can
be strained out later.
Salvaging Parasites from Primate Corpses
Helminthic parasites-flukes, tapeworms, roundworms, and thornyheaded worms-are identified by structures seen in the adult worms.
Identification of parasites by their eggs in the feces is often tentative at
best because of the similarity of egg shape and size in many parasitic species
and because the eggs may appear differently in various hosts, depending
on the length of time they are retained in the host gut (Stuart et al., 1993).
In addition, many primate species and localities have not been adequately
surveyed for parasites. The parasitologist analyzing fecal samples from the
field may see an unusual type of egg with no means to refer it back to an
adult worm. Adult helminths are more difficult to preserve in an appropriate manner than fecal samples are, but the value of these specimens
will usually justify the effort.
Digenea. Digeneans (flukes, trematodes) are flatworms in the lumen
of many organs of the body, including intestines, ducts of the liver, gall
bladder and pancreas, lungs, bladder, and pelvic blood veins. Eggs are usually operculated and often golden when viewed under the microscope.
When exposed to preservative fluids, adult digeneans and most other types
of worms contract to such an extent that identification is often difficult
and sometimes impossible. Therefore, immediately after discovery, transfer
the living worms in a drop of water to a microscopic slide. Lightly lay a
coverslip on top of the worms and use a paper towel or absorbent material
to draw out the water beneath one side of the coverslip while introducing
preservative via diffusion on the other side. A warm alcohol-formalin-acetic acid solution ( M A ) is the preferred fixative. A stock solution is easily
prepared by combining 6 parts of commercial formalin with 50 parts of
95% ethanol (ETOH), 4 parts of glacial acetic acid, and 40 parts of distilled
water. AFA is a good general killing and fixing agent, with the additional
advantage that the solution can be used for short-term storage. After the
worms have soaked for -30 min, transfer to a vial of M A . Try to replace
the M A with 70% ETOH within 24 to 48 hr if possible.
Cestoidea. Cestodes (tapeworms) are usually in the small intestine,
though larval stages may be encysted in the musculature or viscera of intermediate or accidental hosts. Tapeworms are often quite long and flattened
with gradually maturing proglottids or segments. Eggs are microscopic, variously shaped, may be in packets, and may have visible embryonic hooks.
The adult worm is usually attached to the host gut with a scolex armed with

Stuart and Strier

590

hooks, suckers, or both. It is important to retain the scolex in the preservative process as it is used in identification. Pry or cut loose the mucosa of
the gut if necessary to be certain the scolex will be saved. Like flukes, tapeworms contract when exposed to preservative, making identification difficult.
If refrigeration is available, a worm can be relaxed in chilled tap water for
several hours before preservation. Alternatively, you may drape the entire
worm over a stick or probe so its own weight extends the proglottids. Then
drip hot AFA down the length of the worm for preservation. The AFA solution should be hot to the touch but not boiling. As with the digeneans,
transfer to 70% ETOH within 24 to 48 hr.
Nematoda. Nematodes (roundworms) are the most common and diverse
of primate parasites. They are in the lumen or encysted in almost any organ
or tissue in the body. They vary from nonpathogenic to very pathogenic and
have diverse life cycles. Many of the more dangerous roundworms have a
somatic phase in the life cycle in which they travel through the host body
before maturing. As might be expected, the eggs of the species that pass
through the digestive system are also varied in appearance. They may be
operculated or nonoperculated, i.e., having a cap, larvated or nonlarvated,
oval or round, thin-walled, thick-walled, and clear or golden. The most common species are clear, relatively thin-walled, and ovoid. Some species have
larvae that hatch in the feces before they pass from the body.
Nematodes present special difficulties with identification since the body
plan is basically a tube within a tube. Identification depends on fine details
of lip structures and reproductive structures. Nematodes also present special
problems in preservation because they have a protective cuticle that makes
penetration of the preservative somewhat difficult and because they have only
longitudinal muscles, which causes them to curl as they die. All the worms
from one host site should be collected and then dropped alive into hot 70%
ETOH. Like AFA, the ethanol should be hot to the touch but not boiling.
It both causes the worm to straighten and penetrates the cuticle for preservation. The worms can then be stored in the 70% ETOH, with a few drops
of glycerin added to prevent drying if the vial leaks or the alcohol evaporates.
Final Considerations
Because of their close phylogenetic relationship to humans, there are
serious risks in handling primates and their tissues and fluids. Hepatitis,
Herpes B, tuberculosis, SIY giardiasis, amoebiasis, and a variety of relatively newly described simian viruses represent potentially fatal zoonotic
infections. It is imperative that every primatologist be cognizant of the risks
associated with working with primates and take appropriate preventive pre-

Primates and Parasites

591

cautions. Always wear latex gloves when collecting samples, particularly

blood or tissues during necropsy. Practice making blood smears before leaving for the field. Field researchers might wish to bank a serum sample of
their own blood before leaving for the field as a baseline reference in the
event that they become ill through zoonotic transmission.
The same sorts of courtesies that apply to field primatologists are also
appropriate when primate parasites are collected while conducting research
in another country. Many countries, such as Brazil, have excellent facilities
for parasitological research and may be able to assist in parasitic identification. If a primate dies and a field necropsy is performed, it is appropriate
to deposit the skin and skeleton with a host country institution. It is equally
courteous to prepare extra parasitic slides which can be deposited at the
same institution. While not all countries have the institutions or the facilities for maximum utilization or care of these materials, many do, and the
courtesy will make all subsequent research easier. Cooperation with the
institutions within the country of origin can also eliminate the need for
multiple host collections for different types of studies.
Parasites and vials of feces are like every other type of scientific specimen: they are worthless without the appropriate data. Memory is as unreliable regarding a vial of parasites as it is regarding a primate's behavior.
Keep a log with unique numbers for each sample, preferably correlated with
the host's ID. Record as much information about the host, the environment,
and the climatic conditions as possible. Recall that overdispersal is the normal pattern for parasite populations. Detailed observations by the researcher
in the field may hold the key to understand the ecological relationship between that particular parasitic species and its primate host.

ACKNOWLEDGMENTS

We thank Sharon Patton and Charles Faulkner of the Department of

Environmental Practice, College of Veterinary Medicine, University of Tennessee, Kenneth Glander, Duke University Primate Center, Durham, North
Carolina, and the late Robert W. Edwards, Parasitic Disease Institute,
Carrboro, North Carolina, for their review and valuable suggestions.

REFERENCES
Appleton, C. C., Henzi, S. P., Whiten, A., and Byrne, R. (1986). The gastrointestinal parasites
of Papio ursinus from the Drakensberg Mountains, Republic of South Africa. Int. J.
Prirnatol. 7: 449-456.

592

Stuart and Strier

Ash, L. R., and Orihel, T. C. (1987). Parasites: A Guide to Laboratory Procedures and
Identification, American Society of Clinical Pathologists Press, Chicago.
Brooks, D. R. (1977). Evolutionary history of some plagiorchioid trematodes of anurans. Syst.
Zool. 26: 277-289.
Brooks, D. R. (1979). Testing the context and extent of host-parasite coevolution. Syst. Zool.
28: 299-307.
Brooks, D. R. (1988). Macroevolutionary comparisons of host and parasite phylogenies.A m u .
Rev. Ecol. Syst. 19: 235-259.
Brooks, D. R. (1992). Origins, diversification, and historical structure of the helminth fauna
inhabiting neotropical freshwater stingrays (Potamotrygonidae).J. Parasitol. 78: 588-595.
Brooks, D. R., and Glen, D. R. (1982). Pinworms and primates: A case study in coevolution.
Proc. Helminthol. Soc. Wash. 49: 76-85.
Brooks, D. R., and McLennan, D. A. (1991). Phylogeny, Ecology and Behavior: A Research
Program in Comparative Biology, University of Chicago Press, Chicago.
Brooks, D. R., and McLennan, D. A. (1993). Parascript: Parasites and the Language of
Evolution, Smithsonian Institution Press, Washington, DC.
Brunsdon, R. V., and Vlassoff, A. (1971). The post-parturient rise: A comparison of the
pattern and relative generic composition of strongyle egg output from lactating and
non-lactating ewes. New Zeal. Vet. J. 19: 19-25.
Chernela, J. M., and Thatcher, V. E. (1989). Comparison of parasite burdens in two native
Amazonian populations. Med. Anthropol. 10: 279-285.
Collet, J. Y., Galdikas, B. M. R,Sugardjito, J. , and Jojosudharmo, S. (1986). A coprological
study of parasitism in orangutans (Pongo pygmaeus) in Indonesia. J. Med. Primatol. 15:
121-129.
Davies, C. R., Ayres, J. M., Dye, C., and Deane, L. M. (1991). Malaria infection rate of
Amazonian primates increases with body weight and group size. Funct. Ecol. 5: 655-662.
Dobson, C. (1964). Host endocrine interactions with nematode infections. I. Effects of sex,
gonadectomy, and thyroidectomy on experimental infections in lambs. Exp. Parasitol. 14:
200-212.
Dougherty, E. C. (1949). The phylogeny of the nematode family Metastrongylidae Leiper
(1909): A correlation of host and symbiote evolution. Parasitology 39: 222-234.
Dunsmore, J. D. (1971). Influence of host hormones on nematode parasitism in rabbits,
Oryctolagus cuniculus (L.). Austral. J. Zool. 19: 121-128.
Ewing, H. E, (1926). A revision of the American lice of the genus Pediculus, together with
a consideration of the significance of their geographical and host distribution. Proc. US.
Nail. Mus. 68: 1-30.
Freeland, W. J. (1976). Pathogens and the evolution of primate sociality. Biotropica 8: 12-24.
Freeland, W. J. (1980). Mangabey (Cercocebus albigena) movement patterns in relation to
food availability and fecal contamination. Ecology 61: 1297-1303.
Gardner, S. L., and Campbell, M. L. (1992). Parasites as probes for biodiversity. J. Parasitol.
78: 596-600.
Glen, D. R., and Brooks, D. R. (1985). Phylogenetic relationships of some strongylate
nematodes of primates. Proc. Helminthol. Soc. Wash. 52: 227-236.
Glen, D. R., and Brooks, D. R. (1986). Parasitological evidence pertaining to the phylogeny
of the hominoid primates. Bio. J. Linn. Soc. 27: 331-354.
Harrison, L. (1914). The Mallophaga as a possible clue to bird phylogeny. Austral. Zool. 1:
1-11.
Hausfater, G., and Meade, B. J. (1982). Alteration of sleeping groves by yellow baboons (Papio
cynocephalus) as a strategy for parasite avoidance. Primates 23(2): 287-297.
Hausfater, G., and Watson, D. F. (1976). Social and reproductive correlates of parasite ova
emissions by baboons. Nature 262: 688-689.
Hoberg, E. P. (1992). Congruent and synchronic patterns in biogeography and speciation
among seabirds, pinnipeds, and cestodes. J. Parasitol. 78: 601-615.
Hopkins, G. H. E. (1942). The Mallophaga as an aid to the classification of birds. Ibis 6:
94-106.

Primates and Parasites

593

Huffman, M. A., and Seifu, M. (1989). Observations on the illness of and consumption of a
possibly medicinal plant, Vemonia amygdalina (Del.), by a wild chimpanzee in the Mahale
Mountains National Park, Tanzania. Primates 30: 51-63.
Inglis, W. 0. (1965). Patterns of evolution in parasitic nematodes. Symp. Br. Soc. Parasitol.
3: 79-124.
Kellogg, V. L. (1913). Distribution and species-forming of ectoparasites. Am. Nat. 47: 129-158.
Kloos, W.E. (1979). Evidence for deoxyribonucleotide sequence divergence between
staphylococci living on human and other primate skin. Curr. Microbiol. 3: 167-172.
Kloos, W. E. (1983). Deoxyribonucleotide sequence divergence between Staphylococcus cohnii
subspecies populations living on primate skin. Curr. Microbiol. 8: 115-121.
Margoli, L., Esch, G. W., Holmes, J. C., Kuris, A. M., and Shad, G.A. (1982). The use of
ecological terms in parasitology. f. Parasitol. 68: 131-133.
McGrew, W. C., Tutin, C. E. G., Collins, D. A., and File, S. K. (1989). Intestinal parasites
of sympatric Pan troglodytes and Papio spp. at two sites: Gombe (Tanzania) and Mt.
Assirik (Senegal). Am. J. Primatol. 17: 147-155.
Metcalf, M. M. (1929). Parasites and the aid they give in problems of taxonomy, geographical
distribution, and paleogeography. Smithson. Misc. Collect. 81: 1-36.
Metcalf, M. M. (1940). Further studies on the opalinid ciliate infusorians and their hosts.
Roc. U S . Natl. M u . 87: 465-634.
O'Connor, B. M. (1984). Co-evolutionary patterns between astigmatid mites and primates. In
Griffiths, D. E., and Bowman, C. E. (eds.), Acarology Q Vol. 1, Ellis Horwood, Chicester,
England, pp. 19-28.
O'Connor, B. M. (1988). Host associations and coevolutionary relationships of astigmatid mite
parasites of New World primates. I. Families Psoroptidae and Audycoptidae. Fieldiana
39: 245-260.
Phillips-Conroy, J. E. (1986). Baboons, diet, and disease: food plant selection and
schistosomiasis. In Taub, D. M., and King, F. A. (eds.), Current Perspectives in Primate
Social Dynamics, Van Nostrand, New York, pp. 287-304.
Preston, R. (1992). Crisis in the hot zone. The New Yorker Oct. 26: 58 et seq.
Price, D. L. (1994). Procedure Manual for the Diagnosis of Intestinal Parasites, CRC Press,
Boca Raton, FL.
Price, P. W., Westoby, M., Rice, B., Atsatt, P. R., Fritz, R. S., Thompson, J. N., and Mobley,
K. (1986). Parasite mediation in ecological interactions.Ann. Rev. Ecol. Syst. 17: 487-505.
Pritchard, M. H., and Kruse, G. 0. W. (1982). The Collection and Preservation of Animal
Parasites, University of Nebraska Press, Lincoln, NE.
Schmidt, G. D., and Roberts, L. S. (1989). Foundations of Parasitology, 4th ed., Times
Mirror/Mosby College, St. Louis, MO.
Stuart, M. D., Greenspan, L. L., Glander, K. E., and Clarke, M. R. (1990). A coprological
survey of parasites of wild mantled howling monkeys, Alouatta palliata palliata. f. Wildlife
Dis. 26(4): 547-549.
Stuart, M. D., Strier, K. B., and Pierberg, S. M. (1993). A coprological survey of parasites of
wild muriquis, Brachyteles arachnoides, and brown howling monkeys, Alouatta fusca. J.
Helminthol. Soc. Wash. 60: 111-115.
von Ihering, H. (1891). On the ancient relations between New Zealand and South America.
Trans. Proc. New Zeal. Inst. 24: 431-445.
Wiley, E. O., Seigel-Causey, D., Brooks, D. R., and Funk, V. A. (1991). The Compleat Cladist,
a Primer of Phylogenetic Procedures, University of Kansas Museum of Natural History,
Special Publication No. 19, Lawrence.
Wrangham, R. W., and Nishida, T. (1983). Aspilia spp. leaves: A puzzle in the feeding
behaviour of wild chimpanzees. Primates 24: 276-282.