ARTICLES

Primates and the Ecology of Their InfectiousDiseases: How will Anthropogenic Change AffectHost-Parasite Interactions?COLIN A. CHAPMAN, THOMAS R. GILLESPIE, AND TONY L. GOLDBERG

Although humans have alwaysshared habitats with nonhuman pri-mates, the dynamics of human-pri-mate interactions are changing radi-cally.7–9 Within the last severaldecades, humans have been responsi-ble for massive, irrevocable changesto primate habitats. Most primates to-day live in anthropogenically dis-turbed habitat mosaics of farmland,human settlements, forest fragments,and isolated protected areas.7 As an-thropogenic habitat change forces hu-mans and primates into closer andmore frequent contact, the risks of in-terspecific disease transmission in-crease.10,11

The importance of these issues isreadily apparent from the many dis-eases that nonhuman primates andhumans presently share (Table 1). Forexample, monkeys are reservoirs forthe yellow fever virus, an arbovirus ofcritical importance to human healthin Africa and South America.12 Otherimportant human viruses stemmingfrom nonhuman primates includeherpesvirus B, SV40 polyomavirus,and various simian retroviruses.13

Among bacterial parasites, Mycobac-terium tuberculosis, the causal agentof tuberculosis, can be transmittedzoonotically, both in captivity and inthe wild.14 Mycobacterium leprae,15

Shigella sp., E. coli, Campylobacter sp.,and Salmonella sp.16 have also causedhuman disease traceable to nonhu-man primates. Parasitic agents sharedwith nonhuman primates include ma-larias (Plasmodium sp.17), Trypano-soma cruzi (the causative agent ofChagas disease18), Giardia, Cryptospo-ridium,19,20 and a variety of gastroin-testinal helminths.21 Malaria is one ofthe best examples of the importanceof human-primate interactions with

The sudden appearance of diseases like SARS (severe acute respiratory syn-drome1), the devastating impacts of diseases like Ebola on both human and wildlifecommunities,2,3 and the immense social and economic costs created by viruseslike HIV4 underscore our need to understand the ecology of infectious diseases.Given that monkeys and apes often share parasites with humans, understandingthe ecology of infectious diseases in nonhuman primates is of paramount impor-tance. This is well illustrated by the HIV viruses, the causative agents of humanAIDS, which evolved recently from related viruses of chimpanzees (Pan troglo-dytes) and sooty mangabeys (Cercocebus atys5), as well as by the outbreaks ofEbola virus, which trace their origins to zoonotic transmissions from local apes.6 Aconsideration of how environmental change may promote contact between hu-mans and nonhuman primates and thus increase the possibility of sharing infec-tious diseases detrimental to humans or nonhuman primates is now paramount inconservation and human health planning.

Colin A. Chapman has conducted field work in the Caribbean and Costa Rica, and now hasestablished a long-term research program in Kibale National Park, Uganda. Trained in bothanthropology and zoology, his research focuses on attempts to understand what determinesthe abundance of primates in a variety of natural and human-modified settings and the impactof primate loss. Having examined nutritional constraints on primate populations, he is nowturning to the examination of whether dietary stress adversely affects resistance to parasiticinfection by reducing the effectiveness of the immune system. If this occurs, nutritional statusand parasitism could have synergistic effects on the host; that is, the individual effects of eachfactor would be amplified when co-occurring. Colin.Chapman@McGill.ca

Thomas R. Gillespie is Director of the Earth and Society Initiative on Emerging Disease andEcosystem Health and a member of the Faculty of Anthropology and Veterinary Pathobiologyat the University of Illinois. His primary research examines how anthropogenic disturbanceaffects primate ecology and behavior, with a focus on primate-parasite and primate-diseasedynamics. trg@uiuc.edu

Tony L. Goldberg is a disease ecologist with a focus on conservation medicine. Trained inanthropology, epidemiology, molecular biology, and veterinary medicine, his research exam-ines the interactions between anthropogenic environmental change and the emergence andevolution of infectious disease in humans, wildlife, and domestic animals. He currently usesmolecular techniques to infer patterns of transmission for viral and bacterial pathogens withinand among host species over complex landscapes and over time. He conducts field work onhumans and nonhuman primates in Africa, as well as on wild fishes and domestic livestockin North America. tlgoldbe@uiuc.edu

Key words: parasites; viruses; pathogens; hunting; logging; climate change; conservation

*Correspondence: Anthropology Department and McGill School of Environment, 855 Sherbrooke St West,McGill University, Montreal, Canada, H3A 2T7. Tel.: �1-514-398-1242; fax: �1-514-398-1643, E-mail:Colin.Chapman@McGill.caDOI 10.1002/evan.20068Published online in Wiley InterScience(www.interscience.wiley.com).

Evolutionary Anthropology 14:134–144 (2005)

Evolutionary Anthropology 14:134 –144 (2005)

respect to current or emerging infec-tious diseases (Box 1).

Such parasites pose significant con-servation risks to nonhuman primatepopulations, many of which are al-ready threatened or endangered byhabitat loss and hunting.7,22 For ex-ample, evidence indicates that be-tween 1983 and 2000 Ebola virus out-breaks contributed to the reduction of

ape population densities by more than50% over a broad geographic scale.2,3

Polio epidemics have caused wide-spread mortality in wild chimpanzeecommunities.23 Gastrointestinal andrespiratory parasites shared betweenmountain gorillas, trackers, and eco-tourists threaten the long-term via-bility of gorilla populations, as wellas the economic sustainability of as-

sociated ecotourism ventures.24,25

Such risks will surely increase as hu-mans continue to encroach uponnonhuman primate habitats, and asrates of forest fragmentation anddegradation in the tropics continueto accelerate.

In this paper, we first discuss thepotential importance of disease as afundamental factor determining non-human primate abundance and sug-gest ways in which population regula-tion can be demonstrated empirically.Second, we review what is knownabout how anthropogenic change canaffect host-pathogen interactions. Weconsider anthropogenic effects on dis-ease emergence at different spatialscales, from local effects, such ashunting, to regional effects, such aslogging and fragmentation, to mul-tiregional effects, such as climatechange. Our goal is to provide aframework for understanding the po-tential importance of infectious dis-ease to the ecology and conservationof primates, and to suggest ways inwhich the scientific community mightapproach the issue (Fig. 1).

DISEASE AND PRIMATEPOPULATION DYNAMICS

A fundamental issue in ecology isdetermining the factors that regulatethe density of animal populations.

TABLE 1. PARASITES EXCHANGED BETWEEN HUMANS AND NONHUMANPRIMATES: THE ROUTE AND DIRECTION OF EXCHANGEa

Parasite Route of Exchange Direction of Exchange

Herpes B Animal bite Nonhuman primate tohuman

Monkey pox Animal bite Nonhuman primate tohuman

Polio virus Fecal, oral Humans to nonhumanprimate

Ebola Hunting &butchering

Nonhuman primate tohuman

Mycobaterium leprae Nasal secretion Among primatesTuberculosis Respiratory droplet Humans to nonhuman

primateMalaria Vector Both directionsFilaria Vector Both directionsYellow Fever Vector Both directionsDracunculiasis Water-mediated Human to nonhuman

primateSchistosomiasis Water-mediated Nonhuman primate to

humanSV40 Vaccinations Nonhuman primate to

humanGastrointestinal parasites Fecal Both directions

a Also see Wolfe and coworkers.90

TABLE 2. HOST RANGE, MORBIDITY, AND MORTALITY ASSOCIATED WITH GASTROINTESTINAL PARASITES INFECTING WILDPRIMATES AND HUMANS IN KIBALE NATIONAL PARK, UGANDA.21,70

Parasite Species (Taxon) Primate Speciesf Morbidity and Mortality

Trichuris sp.a RC, BW, RT, Hu Typically asymptomaticStrongyloides fullebornia RC, BW, RT, Hu Mucosal inflammation, deathStrongyloides stericalisa RC, Hu Mucosal inflammation, deathOesophagostomum

stephanostomumaRC, BW, RT, Hu Severe diarrhea, weight loss, death

Colobenterobius sp.a,e RC, BW Dysentery, enteritis, ulceration, deathEnterobius sp.a,e RT, Hu Dysentery, enteritis, ulceration, deathStreptopharagus sp.a RT Typically asymptomaticAscaris sp.a RC, BW, Hu Intestinal obstruction, deathDicrocoeliidae sp.b BW, RT Typically asymptomaticBertiella sp.c BW, RT, Hu Typically asymptomaticChilomastix mesnilid RT, Hu DiarrheaIodameoba buetscliid RT, Hu Typically asymptomaticGiardia lambliad RT, Hu Enteritis, diarrheaEntamoeba colid RC, BW, RT, Hu Typically asymptomaticEntamoeba histolyticad RC, BW, RT, Hu Hepatic and gastric amoebiasis, death

a Nematoda.b Trematoda.c Cestoda.d Protozoa.e Known to be host specific.f RC � Red colobus; BW � Black-and-white colobus; RT � Redtail guenon; Hu � Human.

ARTICLES Primates and Infectious Diseases 135

This is central to the formulation ofconservation plans; that is, if a factorthat limits a population is known, at-tempts can be made to manage thatparticular factor. Given this, it is sur-prising that so little is known aboutdeterminants of primate abundance.Various potential factors have beenproposed and disease-related mortal-ity is often discussed. However, theimportance of disease either as an in-dependent determinant or as oneworking in conjunction with otherfactors has proven difficult to quan-tify.

Disease and parasites can clearlycause short-term reductions in popu-lation size.26–28 For example, a 50%decline in the howler monkey (Al-ouatta palliata) population on BarroColorado Island, Panama, between1933 and 1951 was attributed to yel-low fever.26 Cheney and coworkers29

found that illness accounted for moredeaths than predation did in onetroop of vervet monkeys (Chlorocebusaethiops) and that lower-ranking indi-viduals were more likely to experiencethe effect of parasites. Chacma ba-boons (Papio ursinus) living in theNamib desert have been found to be

heavily infected by ticks (Rhipicepha-lus); these infections were speculatedto be responsible for more than half(n � 18) of recorded infant deaths.30

Some infants were not able to nursebecause of the number of ticks at-tached to their muzzles. As a finalexample, Rudran and Fernandez-Duque31 have quantified the demo-graphic changes that occurred in apopulation of red howler monkeys (Al-ouatta seniculus) over thirty years andreported a population decline of 74%that was likely due to disease. Theyfound that new groups died out morerapidly than did established groupsand speculated that food shortages oc-curring in the regenerating areas oc-cupied by these new groups contrib-uted to the population crash.

Given that disease and parasites canclearly cause mortality, the questionof interest is: Can disease operate asan independent agent or in conjunc-tion with other factors to regulate pri-mate populations? Based on a 68-month study of howler monkeys(Alouatta palliata) and a parasitic botfly (Alouattamyia baeri), Milton32 con-cluded that the annual pattern ofhowler mortality on Barro Colorado

Island, Panama, resulted from a com-bination of effects, including age,physical condition, and larval burdenof the parasitized individual, whichbecomes critical when the populationexperiences dietary stress. She con-cluded that the lack of growth of thisclosed population over the past 20years apparently resulted, in largepart, from the primary and secondaryeffects of bot-fly parasitism. Shecalled for further study of potentialsynergistic interactions among nutri-tional factors, larval burdens, andhowler monkey physiology. However,observational studies such as this pro-vide only indirect evidence that pri-mate diseases regulate populations.Scott and Dobson33 argued that it isimportant to conduct manipulativeexperiments to determine the inten-sity with which parasites or other fac-tors operate at different populationdensities. They argued that if popula-tions of hosts and pathogen (a patho-genic parasite is one that is the caus-ative agent of a disease) are relativelyconstant, then a lack of statistical cor-relation between the density of a hostand its parasite tells little about whatis structuring the system. For pri-

Box 1. MALARIA

One of the best examples of theclose interactions between a group ofparasites and primates is malaria, aparasite that dramatically affects hu-mans and that potentially can affectnonhuman primate populations. It isestimated that there are 300 to 500million clinical cases of malaria everyyear88 and that it causes 0.7 to 2.7million deaths per year.89 Convertingthis to a more comprehensive statis-tic, a child dies of malaria every 40seconds.88 However, the actual fig-ures are likely to be substantiallyhigher owing to under-reporting anddifficulties of diagnosis.89 If no newcontrol measures are developed, thedeath toll is predicted to double in thenext 20 years.89

The close interactions among a va-riety of primate species and the Plas-modium parasite are illustrated by thefact that there has been frequent

transmission between humans andnonhuman primates. More than 26species of Plasmodium infect pri-mates. Moreover, morphological andmolecular data demonstrate that hu-man and nonhuman primate malariasare spread throughout the phyloge-netic trees,90 suggesting extensiveexchange. There are four major hu-man malaria parasites, Plasmodiumfalciparum, P. vivax, P. ovale, and P.malariae. P. falciparium can infect owland squirrel monkeys; P. vivax infectschimpanzees, P. malaria is thought tohave come from chimpanzees origi-nally and, in South America, has gonefrom humans back into nonhumanprimates, where it is now called P.brasilianum. Little is known about theimpact of P. brasilianum on primatepopulations, but it was found in allfive monkey species captured in arescue operation associated with the

filling of a hydroelectric dam inFrench Guiana.17 P. vivax is thoughtto have been derived from a monkeymalaria strain between 40,000 and60,000 years ago in Southeast Asia.There is even the possibility that anew strain having a global impact willsoon emerge. Singh and coworkers91

used PCR assays to demonstratethat 58% of the people with malaria inKapit division of Malaysian Borneotested positive for P. knowlesi, buthad been misdiagnosed as having P.malaria. The natural hosts of P.knowlesi are long-tailed (M. fascicu-laris) and pig-tailed (M. nemestrina)macaques. If this new strain of ma-laria becomes more widespread, itcould have serious consequences. P.malaria infections are almost neversevere, but P. knowlesi multipliesmore rapidly and infections can bemore serious.92

136 Chapman et al. ARTICLES

mates, such experiments are logisti-cally difficult, but they may be neces-sary to shed light on this issue.34

Gulland35 provided an instructive ex-ample of how to use such experimen-tal approaches on mammals. He stud-ied the interactions of Soay sheep andnematode parasites, demonstratingthat at times of population crashessheep were emaciated, had high nem-atode burdens, and showed signs ofprotein-energy malnutrition. In thefield, sheep treated with antihelminth-ics had lower mortality rates, whileexperimentally infected sheep withhigh parasite loads, but fed nutritiousdiets, showed no sign of malnutrition.

Quantifying patterns of disease prev-alence in nonhuman primate popula-

tions is difficult since, for many para-sites, it is necessary to obtain clinicalsamples from animals to determinetheir infection status. Enteric parasitesare notable exceptions, in that it is pos-sible to diagnose animals by analyzingfecal samples.36 Among enteric para-sites, helminths and protozoans aremost easily characterized in wild non-human primates. These parasites canaffect host survival and reproductiondirectly through pathological effectsand indirectly by reducing host condi-tion.37,38 Severe parasitosis can lead toblood loss, tissue damage, spontaneousabortion, congenital malformations,and death.39 However, less severe infec-tions, which are more common, maydamage nutrition, increase energy ex-

penditure, and impair travel, feeding,predator escape, and competition forresources or mates.37,38 Even upregula-tion of host immunity can reducebreeding success.40 Some parasites ex-tract significant amounts of nutrientsfrom hosts, resulting in marked reduc-tion in energy uptake,41 but others ap-pear to have little or no effect on hostenergetics.42,43 Animal body conditionand reproductive status can be compro-mised when parasites inflict substantialenergetic costs.44 However, parasites donot necessarily induce negative effectsif hosts have adequate energy reservesor nutrient supplies concurrent with in-fection,32,35,42 suggesting that the out-come of host-parasite associations maybe contingent on host nutritional statusand infection severity.

Dietary stress may exacerbate theclinical consequences of parasitic in-fection through immunosuppres-sion.32,45,46 If so, food shortages couldresult in higher parasite burden,which in turn could increase nutri-tional demands on the host and exac-erbate the effects of food shortages. Ifthis occurred, nutritional status andparasitism could have synergistic ef-fects on the host; that is, the individ-ual effects of each factor would beamplified when they co-occur. The in-teractions between nutritional stressand parasitism have been examined inmany laboratory studies42,47 and ahandful of field studies,35,48,49 andhave led to speculation that vertebratepopulations may be influenced by theinteractive effects of food shortageand parasitism.45,50,51 The interactiveeffects of parasitism and nutritionalstatus have rarely been examined innonhuman primates (but see Mil-ton32).

Studies of the interactions of non-human primate nutritional statuswith infectious diseases have beenlimited to eukaryotic parasites largelybecause of the methodological ease ofdiagnosing parasitic infections. How-ever, modern molecular diagnostictools should expand the ability to as-sess primate health noninvasively. Ex-tracting DNA from animal feces isnow commonplace, as is the selectiveamplification of parasite-specific DNAsequences from fecal DNA by poly-merase chain reaction (PCR).52 Meth-ods such as real-time quantitative

Figure 1. Clinical disease is the result of factors operating on the level of the host, thepathogen, and the environment. Human cultural practices and primate life history modifythese factors. For example, the sociality, mating practices, and ranging patterns of nonhu-man primates are known to affect the richness and diversity of their parasitic worm andviruses.87 With respect to how anthropogenic change will effect these interactions, wesuggest that hunting, habitat disturbance (for example, logging and fragmentation), andclimate change (indicated in italics) are the factors that have the greatest potential toresult in change in host-pathogen interactions.

ARTICLES Primates and Infectious Diseases 137

PCR53 now obviate the need for elec-trophoretic gels, significantly speed-ing the diagnostic process. Further-more, such assays provide quantitativeinformation on the concentration oftarget DNA in the original sample,yielding not only presence or absencedata, but also information on infec-tion intensity, which can be useful foranalyses of the temporal course of in-fection.54 These assays can also be“multiplexed,” allowing noninvasivescreening of animals for multiple par-asites simultaneously.55 In addition,thermocyclers with optical capabili-ties, which are necessary for real-timePCR applications, are shrinking insize and weight, while lyophilized re-agents have become available that arestable at room temperature for ex-tended periods, making it possible totransport these new diagnostic toolsto remote field sites.56 Although suchtechnologies are primarily being de-veloped for military and agriculturalapplications, only minor adaptationswould be required for the rapid diag-nosis of primate infectious disease infield settings. It should soon be possi-ble to screen large numbers of pri-mates for a series of parasites in “realtime” at remote field sites, and to gen-erate accurate and precise measure-ments of seasonal variation in infec-tious disease prevalence and intensity.

HOW ANTHROPOGENICCHANGE CAN AFFECT HOST-

PARASITE INTERACTION

As recently as the 1980s, the domi-nant perspective on the treatment andprevention of infectious diseases wasone of optimism.57 Immunization andantibiotics were considered adequatefor combating infectious diseases.This optimism was shaken by the in-creased prevalence of antibiotic-resis-tant bacteria and the emergence andreemergence of diseases such asEbola, HIV, multi-drug-resistant tu-berculosis, malaria, and enterohem-orrhagic E. coli. Infectious diseasesare now viewed as emerging at an ac-celerated rate in human and animalpopulations worldwide.58,59

In 1992 the Institute of Medicine60

recognized this increased rate of dis-ease emergence and identified six fac-tors influencing disease emergence:

changes in human demographics andbehavior; changes in technology andindustry; international travel andcommerce; microbial adaptation;breakdown of public health measures;and environmental change and landuse. With respect to primates, the lastfactor is critical. However, the otherfactors contribute to the rate of spreadof diseases once they emerge. Diseaseemergence most frequently resultsfrom a change in the ecology of host,parasite, or both.61 As anthropogenichabitat change forces humans and an-imals into closer and more frequentcontact, risks of zoonotic diseasetransmission will increase.10 Dobsonand Foufopoulos11 conducted a sur-vey of emerging pathogens of wildlife

in North America and found that hu-man involvement facilitated 55% ofpathogen outbreaks. In only 19% ofthe cases was there no evidence ofhuman influence. We are not aware ofa similar survey for tropical regions,and the data for most regions withendemic primate populations are lim-ited.

We suggest that changes in the ecol-ogy of hosts and parasites can beviewed as occurring on three scales:local, regional, and multiregional.Processes occurring on the local scaleare those that act on individual popu-lations of monkeys, apes, and humansto affect the rates with which they

come into close contact and include,for example, hunting, crop raiding, re-search, and ecotourism. Processes oc-curring on the regional scale are thosethat alter primate habitats to affectdirect and indirect contact rates anddisease transmission patterns (for ex-ample, when forests are logged andfragmented). Finally, processes occur-ring on the multiregional scale arethose that act indirectly on an ecosys-tem-wide level to modify diseasetransmission patterns. Multiregionaleffects would occur, for example, ifclimate change altered forest ecologythroughout the tropics in ways thataffected rates of disease transmissionamong primate populations and spe-cies. We should not assume that themagnitude of effect on primate popu-lations is proportional to the scale ofeffect. For example, disease-associ-ated local processes, such as hunting,might cause the extinction of a highlyendemic primate species morequickly than might multiregional pro-cesses such as climate change. Al-though research at all three levels areimportant, we know the least aboutprocesses occurring at the larger spa-tial scales.

Changes at the Local Scale:Hunting

There is little doubt that when mon-keys, apes, and humans come intophysical contact, the risk of diseasetransmission increases. The huntingand butchering of wild nonhumanprimates leads to extremely close con-tact and will cause humans to comeinto contact with the body fluids ofliving or recently dead nonhuman pri-mates (Fig. 2).

Subsistence and commercial hunt-ing of tropical wildlife are occurringat extremely high, unsustainable lev-els; however, obtaining comprehen-sive data on the extent of harvest isdifficult. Case studies at particular lo-cations indicate that wildlife harvestprovides a major source of food formany local communities. For exam-ple, a market survey in two cities inEquatorial Guinea, West Africa, hav-ing a combined population size of107,000, recorded 4,222 primate car-casses on sale over 424 days.61 Peres62

documented that a single family of

However, modernmolecular diagnostictools should expand theability to assess primatehealth noninvasively.Extracting DNA fromanimal feces is nowcommonplace, as is theselective amplificationof parasite-specific DNAsequences from fecalDNA by polymerasechain reaction (PCR).

138 Chapman et al. ARTICLES

rubber tappers in a remote forest siteof western Brazilian Amazonia killedmore than 200 woolly monkeys (Lago-thrix lagotricha), 100 spider monkeys(Ateles paniscus), and 80 howlers (Al-ouatta seniculus) over 18 months. Themarket for bushmeat is not restrictedto tropical countries where these ani-mals originate. For example, 25 tonsof turtles are exported every weekfrom Sumatra.63 Individuals that huntor butcher these animals risk con-tracting zoonotic infections.

Hunting and butchering of nonhu-man primates is thought to have led tothe origin of two significant emergingdiseases with nonhuman primate zoo-notic origins, AIDS and Ebola (Box 2).Peeters and colleagues64 tested 788monkeys hunted in Cameroon forsimian immunodeficiency virus (SIV),the precursor to HIV. Evidence of SIVinfection was found in 13 of the 16species tested and in 16% of the ani-mals. Wolfe and coworkers8 testedpeople living in Central African forestswho reported having had contact withblood and body fluids of wild nonhu-man primates for simian foamy virus.They found that 1% of these peoplehad antibodies to the virus. In some

regions, a large proportion of ruralcommunities have contact with non-human primates. In remote villages inCameroon, more than 60% of thecommunity reported having butch-ered nonhuman primates, 30%hunted primates, and 11% reportedkeeping primates as pets.9 Monkeypoxwas associated with the hunting of redcolobus monkeys (Procolobus badius)after a localized epidemic emerged inhumans.65

As conservation agencies increas-ingly turn to ecotourism as a strategyto provide local communities withbenefits from protected areas, and asthe number of primate research sitesincreases, so does the possibility oftransmission via these activities. Al-ready, cases have been documented ofprimates in eco-tourist and researchsites contracting infections with likelyhuman origins. For example, in 1966six chimpanzees at Gombe NationalPark, Tanzania, died from a polio-likevirus and six others were paralyzedfor life.25 Also, in 1996, a severe skindisease was documented in gorillas inBwindi Impenetrable National Park,Uganda, and skin biopsy confirmedthe presence of scabies (Sarcoptes sca-

biei).25 Of five troops of baboons stud-ied at Gombe, three were infectedwith schistosomiasis (Schistosomamansoni); the troop having the mostcontact with people showed the high-est prevalence of infection.25 Suchrisks will surely increase as humanscontinue to encroach upon nonhu-man primate habitats.

Changes at the RegionalScale: Logging and ForestFragmentation

Only a handful of studies have pro-vided evidence that habitat distur-bance occurring at the regional scalealters primate-parasite interac-

tions.66–69 If changes at this scale areimportant, this lack of data is unfor-tunate, since this is the scale at whichmanagement practices could be mosteasily implemented.

We have recently completed a seriesof investigations demonstrating thatvarious forms of anthropogenic dis-turbance, specifically selective loggingand forest fragmentation, alter the dy-namics of gastrointestinal parasite in-fection in the human and nonhumanprimate populations in the region ofKibale National Park, Uganda.69–72

We have determined that the preva-lence and richness of gastrointestinalparasite infections were greater for

Figure 2. Hunted mangabey (Lophocebus albigina) for sale along a roadside in CuvetteWest region of the Republic of Congo. Hunting and butchering of non-human primates isthought to have led to the origin of two significant emerging diseases with non-humanprimate zoonotic origins: AIDS and Ebola. Photo by A. M. Kilbourn, WCS.

Already, cases havebeen documented ofprimates in eco-touristand research sitescontracting infectionswith likely humanorigins. For example, in1966 six chimpanzees atGombe National Park,Tanzania, died from apolio-like virus and sixothers were paralyzedfor life.

ARTICLES Primates and Infectious Diseases 139

Box 2. Ebola: A crisis and wake-up call for better understanding of reservoirs and transmission routesW. Karesh and C.A. Chapman

Ebola has been known to the sci-entific community since it was firstidentified in 1976.93,94 Since that timeit has entered into human populationsat least a dozen times in six differentcountries in Equatorial Africa andkilled hundreds of people. But it hasalso had significant impacts on non-human primate populations. Theworst-case scenario in great apesmay have been demonstrated in theMinkebe forest region of northeasternGabon where lowland gorilla andchimpanzee populations have comeclose to disappearing during the pe-riod of the human Ebola outbreaks in1994 and 1996.95 Up to tens of thou-sands of gorillas and chimpanzeesmay have died due to Ebola. Unfortu-nately, no one was working in the re-gion during the human outbreaks tocollect either samples or observa-tions on wildlife to determine conclu-sively if or how Ebola affected the apepopulations. “No one was in the re-gion” is an unfortunate recurrenttheme in Ebola research that has lim-ited our understanding of the ecologyof the pathogen.

Initial fears of catastrophic declines2

led to calls for dramatic action, such ascreating barriers to divide infected pop-ulations.96 Further study, however,yielded more information the type ofconservation action that would be ap-propriate to curb an Ebola outbreak.While the need to anticipate Ebola out-breaks, establish appropriate wildlifemonitoring teams, and educate peopleof the potential dangers of bushmeathave remained constant,97 some initialactions plans have been illustrated topotentially be ineffective.

Three findings deserve specialmention. First, Eric Leroy and col-leagues3 sampled humans and wild-life in five outbreaks and found eightdistinct strains of the virus. The au-thors conclude that these distinctstrains probably diverged over de-cades or even centuries, and poten-tially came from different sources,suggesting a wide distribution of the

virus. The spread of the diseasewithin and between groups of greatapes is still poorly understood. Sec-ond, Leroy et al.98 found the servo-prevalence of Ebola antibody in wildchimpanzees was 12.9%, indicatingboth that wild apes can survive expo-sure, that the Ebola virus is distrib-uted over a large region of centralAfrica, and that the virus was presentin certain regions before the observedoutbreaks. Third, research is startingto explore non-primate natural reser-voirs of the virus. For example, labo-ratory experiments have shown thatsome species of fruit bats and insec-tivorous bats can survive infectionwith the Ebola virus and shed the or-ganism in their excrement.99 Fieldwork in the Central African Republichas found at least fragments of Ebolaviral particles using PCR genetictechniques in rodents,100 and similarwork in the Republic of Congo hasfound the same in bats (E. Leroy, per-sonal communication).

These studies imply a very complexpicture for Ebola virus transmission,

and one that must be understoodquickly if we are to respond in anappropriate timeframe. Clearly thereis a need to take conservation action,such as establishing systems to an-ticipate Ebola outbreaks, monitor,and reduce impacts on wildlife, butthis situation also highlights the im-portance understanding potentialreservoirs and modes of transmis-sion.97 Furthermore, the situation alsopoints to the need to understand howhumans could be altering the ecologyof host-virus interactions. For exam-ple, Morvan and colleagues100 sug-gest that rather than being a virus ofdeep forest, Ebola is actually morecommon in forest peripheries andfragments. Humans are currently cre-ating forest fragments in Central Af-rica at a rapid rate. Similarly, Pinzonet al.101 suggest outbreaks of Ebolahemorrhagic fever are associatedwith dry conditions, raising the ques-tion of how anthropogenically drivenclimate change will effect transmis-sion of this virus to non-human pri-mates and humans alike.

140 Chapman et al. ARTICLES

red-tail monkeys (Cercopithecus asca-nius) in logged than in undisturbedforest. Infective-stage primate para-sites were found at higher densities incanopy and ground vegetation plotsfrom logged compared to undisturbedforest, demonstrating a greater infec-tion risk for humans and nonhumanprimates in logged forest.69

In degraded forest fragments, hu-mans and nonhuman primates over-lap a great deal, and we found tenta-tive evidence that parasites may beshared between Kibale nonhumanprimates and resident humans (Table1). Two parasite genera in particular,Ascaris and Giardia, were found to oc-cur in red colobus monkeys in forestfragments and to have a high preva-lence in the human populations nearthese fragments. These parasites werenever found in more than 2,000 sam-ples from “pristine” areas where peo-ple and primates interact with muchless frequency.68

Most recently, we have documentedthat certain disturbance-related fea-tures of forest fragments are excellentpredictors of infection prevalence inprimates.72 In a five-year study, wecompared patterns of gastrointestinalparasite infection and infection riskamong populations of black-and-white (Colobus guereza) and red colo-bus (Piliocolobus tephrosceles) inhab-iting undisturbed habitats and forestfragments. Our results demonstratethat forest fragmentation alters prev-alence and infection risk and thatthese factors are influenced by hostdensity. We also examined the rela-tionships between forest-fragment at-tributes and infection patterns. Inter-fragment comparisons examiningnine potential factors demonstratedthat tree-stump density, an index ofdegradation, had a strongly positiveinfluence on the prevalence of parasiticnematodes. Both fragment size (nega-tive relationship) and primate popula-tion density (positive relationship) alsopredicted prevalence of some para-sites.72 These results demonstrate thatthe transmission dynamics of gastroin-testinal parasites are affected by the de-gree and nature of anthropogenic dis-turbance of forest fragments.

The exact mechanism leading to al-tered transmission dynamics remainsan area for future study. Perhaps ani-

mals in these disturbed habitats arenutritionally stressed, lowering theirimmune status and making themmore susceptible to gastrointestinalparasites. Alternatively, their re-stricted ranging and increased timespent in any one tree may increase thechances of infection for direct life-cy-cle parasites. Habitat fragmentationmay have led to reduced genetic diver-sity and thus potentially increasedsusceptibility to infectious disease.Likewise, smaller population size inforest fragments may support less ge-netic diversity, reducing the potentialscope of the response to parasites

(Charles Nunn, personal communica-tion). Identifying plausible mecha-nisms is a priority, because only oncea mechanism is identified is it possibleto construct an informed manage-ment plan that includes disease as anintegral component.

The effects that we have docu-mented likely apply to systems otherthan primate gastrointestinal para-sites. Habitat disturbance associatedwith the creation of the Panama Ca-nal, for example, is thought to have

catalyzed the yellow fever outbreakthat occurred at that time in howlermonkeys.73 The use of human cropsand rubbish has been shown to altergastrointestinal parasite communitiesin primates.66,74

Changes at the MultiregionalScale: Climate Change

The larger the geographic scale overwhich host-parasite interactionschange, the greater the number ofpopulations that can potentially be af-fected. Climate is the factor that hasthe greatest potential to influencehost-parasite interaction at this spa-tial scale. Connections betweenweather and disease are well estab-lished. Many diseases occur duringcertain seasons or erupt in associationwith unseasonable conditions. For ex-ample, meningococcal meningitis ep-idemics in sub-Saharan Africa eruptduring the hot dry season and subsidesoon after the onset of the rains.75 Re-cently, Guernier, Hochberg, and Gue-gan76 documented that climatic fac-tors are the most importantdeterminant of the global distributionof human pathogens and that climate,rather than socioeconomic condi-tions, is responsible for the number ofpathogens increasing toward theequator. Nunn and coworkers77 useda data set encompassing 330 parasitespecies and 119 primate hosts to illus-trate the importance of latitude in pre-dicting vector-borne parasite speciesrichness, with higher diversity beingfound in the tropics. Both of thesestudies suggest that the geographicdistribution and prevalence of manyparasites will increase with globalwarming. Human medical profession-als have recently become concernedas to whether global warming willcause increased rates of infectious dis-eases and, with their wealth of clinicaldata, are well ahead of primate ecolo-gists at documenting trends.

The earth’s climate has warmed byapproximately 0.6°C over the past 100years, with two main periods ofwarming (1910–1945 and 1976–present). The 1990s were the warmestdecade on record.78 Recently the sci-entific community has begun to quan-tify ecological responses to climatechange and has realized that somecommunities experience marked

. . . studies suggest thatthe geographicdistribution andprevalence of manyparasites will increasewith global warming.Human medicalprofessionals haverecently becomeconcerned as towhether global warmingwill cause increasedrates of infectiousdiseases and, with theirwealth of clinical data,are well ahead ofprimate ecologists atdocumenting trends.

ARTICLES Primates and Infectious Diseases 141

changes with slight shifts in tempera-ture.78,79 We have recent data demon-strating that climate change is havingan impact on primate populations.Chapman and coworkers80 analyzed a30-year phenology data set fromKibale National Park, Uganda, anddocumented that currently a numberof the most common species rarelyfruit, and that when they do typically�4% of the individuals take part infruiting events. Presently, the Kibaleregion is receiving approximately 300mm more rain than it did at the startof the century, droughts are less fre-quent, the onset of the rainy season isearlier, and the average maximummonthly temperature is 3.5°C hotterthan it was 25 years ago. Contrastingchanges in fruiting patterns over the30 years with differences among foursites with varying rainfall suggeststhat the changes observed in fruitingmay be due to climate change. If cli-mate change does alter fruiting patternsand cause a reduction in food availabil-ity, the susceptibility of nonhuman pri-mates to infectious diseases might becompounded by nutritional stress.

Climate change could affect diseasetransmission by facilitating condi-tions for transmission (for example,increased rainfall will promote trans-mission of waterborne disease); influ-encing the ecology of hosts and vec-tors; or causing resource shifts thatstress primates physiologically.81

With respect to climate change di-rectly affecting disease transmissionrates, heavy rain events have been as-sociated with outbreaks of water-borne diseases in humans. In theUnited States, 68% of waterborne dis-ease outbreaks were preceded by pre-cipitation events above the 80% per-centile.82 Many waterborne pathogensof humans, among them Giardia spp.,Entamoeba histolytica, and E. coli, canalso infect nonhuman primates. Thedanger of such outbreaks will be par-ticularly high for primates that fre-quently interact with water sources af-fected by humans. Given thatprotected areas rarely protect water-sheds,83 even populations well awayfrom the edges of parks are at risk.

Heavy precipitation associated withclimate change may indirectly affectdisease transmission by providingnew breeding sites for vectors such as

mosquitoes. Mosquito-borne diseasesare among the most sensitive to cli-mate shifts, with increased rain andtemperature resulting in increased re-production, increased biting rates,and shortened incubation time. Forexample, with increased rains be-tween 1984 and 1988 in Rwanda therewas a 266% increase in reported ma-laria.75 Malaria incidence is exponen-tially related to temperature, indicat-ing that global climate change couldresult in dramatic increases in ma-laria rates.84 Global warming is likelyto increase the altitudinal range ofmalaria, having an impact on both hu-man and nonhuman primate popula-tions. In Kenya, Shanks and col-leagues85 documented increasedmalaria incidence in high-altitude ar-eas of East Africa and attributed it atleast in part to global warming.

How climate change may stresspopulations will likely be species- andsituation-dependent. However, someeffects are likely to be generalized. In-creased ultraviolet light, which ac-companies atmospheric ozone deple-tion, has been shown to causeimmunosuppression in animals andhumans.75 Heat stress has also beenassociated with an increase in thenumber of human patients admittedfor pulmonary and cardiovascular dis-ease-related problems86 and couldnegatively affect primate populationsin many arid regions. As our studieshave documented, local climatechange in Kibale National Park,Uganda, may disrupt fruiting or flow-ering patterns and place nutritionalstresses on primate populations.80 Wepredict that the overall effect of cli-mate change will be to increase theprevalence and severity of infectiousdisease in most primates.

FUTURE DIRECTIONS

Given the history of the effects ofdisease on nonhuman primate popu-lations, and given a future that willundoubtedly be characterized by in-creasing rates of local and global an-thropogenic habitat change, we seetwo research priorities. First, it will beimportant to understand the relation-ships between infectious disease andprimate demography in relatively un-disturbed systems. Only then will webe able to assess the importance of

parasites as moderators of primatepopulation size and structure under“natural” conditions. Healthy ecosys-tems will consist of the natural com-plement of predators, prey, and para-sites, and only by monitoring healthypopulations can we discover what thatcomplement will be. The unique fea-ture that studies of primates offer overstudies of many other animals is theease of relating the attributes of indi-viduals, such as dominance, nutri-tional stress, and individual parasiteburden, to outcomes such as fitness,survival probability, and reproductivesuccess. Second, once we have quan-tified the effects of specific parasiteson primate populations in undis-turbed habitats, the next step will beto conduct comparative studies of pri-mate populations living in differenttypes of anthropogenically alteredhabitats. If anthropogenic habitat dis-turbance does interact with infectiousdisease, then relationships betweenindividual attributes of primates andhealth or fitness outcomes should dif-fer between disturbed and undis-turbed habitats. Between-site com-parisons should be chosen carefully toexplore the modifying effects of spe-cific anthropogenic disturbances,(such as forest fragmentation with orwithout elevated rates of human con-tact), because the focus will then haveshifted from whether anthropogenichabitat change alters primate-diseaseinteractions to how anthropogenicchange alters primate-disease interac-tions. This, of course, will requiregranting agencies to prioritize long-term studies of primates that includehealth assessment and funding forveterinarians to accompany prima-tologists into the wild.

As new diseases emerge, we caneither react to them and understandthe reasons for their emergence afterthe fact or take a proactive approachand try to understand the principlesthat govern the emergence of novelprimate diseases in general. Weargue that the latter approach ispreferable and has the greatest po-tential to benefit human health, pri-mate health and conservation, andecosystem sustainability in the longterm.

142 Chapman et al. ARTICLES

ACKNOWLEDGMENTS

Colin Chapman’s studies are fundedby the Wildlife Conservation Society,National Science Foundation (USA),Morris Animal Foundation, and Na-tional Science and Engineering Re-search Council (NSERC, Canada).Thomas Gillespie’s studies have beensupported by the National Center forEnvironmental Research of the U.S.Environmental Protection Agency.Tony Goldberg’s studies on primatedisease have been supported by theMorris Animal Foundation, the Wil-liam and Flora Hewlett Foundation,and the University of Illinois Office ofInternational Studies. We thank Lau-ren Chapman, John Fleagle, CharlesNunn, Nathan Wolfe, and three re-viewers for helpful comments on thiswork. We also thank Charles Nunn forproviding us access to unpublishedmaterial.

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