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Conservation and DiseaseROBERT M. MAYBiology DepartmentPrinceton UniversityPrinceton, New Jersey, 08544USA

In developed countries over the past 50 years and more,a combination of better nutrition, better hygiene, anti-biotics and other chemotherapeutic agents, and pro-grams of immunization have almost eradicated morbid-i ty and mortality resulting from infectious diseases. Thesmallpox virus is now extinct in the wild (and no con-servationist mourned this act; our concerns change signas we move from very large organisms to microorgan-isms). Scarlet fever and diphtheria, which carried offheroines in so many Victorian novels-and in Victorianreal life-are rarely heard of today. Vaccination has re-moved polio from essentially all developed countries,and measles, whooping cough, rubella and other child-hood infections seem on the road to local extinction inmany. Whereas hookworm and other parasitic infec-tions were endemic in the southern regions of the Unit-ed States in the early years of this century, most peoplein developed countries today would react with horrorto the thought of harboring a couple of intestinal orother parasites. Although heavy burdens of such para-sites continue to afllict many people in developingcountries, not the least of the reasons why HIV/AIDSsoappalls us, I think, is that in developed countries wehave come to believe a life free from any serious effectsof viral, bacterial, protozoan or helminth infections is anatural state, to which we have some kind of entitle-ment.

Nothing could be further from the truth. As empha-sized by Haldane (1949), infectious diseases have un-doubtedly been the main agents of morbidity and mor-tality (and thus the dominant selective forces) in humanpopulations at least for the past 10,000 years. In com-bination with malnutrition, infectious diseases are stillthe main cause of the dramatic differences between sur-vivorship curves in developed and developing countries(Bradley, 1974). To put it another way, current esti-mates are that 30% of HIV infections go on to producedeath from AIDS (although this number may rise as28

longer runs of data accumulate) which can be comparedwith the 30% case-mortality associated with smallpoxinfections that were, until recently, endemic in mostparts of the world.

Given the conspicuous role that diseases have played,and in many parts of the world continue to play, inhuman demography, it is surprising that ecologists havegiven so little attention to the way diseases may affectthe distribution and abundance of other animals andplants. Until recently, for example, ecology textbookshad chapters discussing how vertebrate and inverte-brate predators may influence prey abundance, but inmost cases you will search the index in vain for mentionof infectious diseases. I think this is partly because ecol-ogists find four- and six-legged predators more engag-ing, partly because pathogenic organisms (like decom-posers, another category of organisms neglected bymost ecologists) are relatively hard to see and thus tostudy, and partly because veterinarians and wildlifemanagers understandably tend to focus on individualsick animals rather than on population aspects of infec-tion.

The past few years have, however, seen an upsurge inefforts to document the effects that viral, bacterial, pro-tozoan and helminth infections may have on the distri-bution and abundance of animal populations in the lab-oratory and-more importantly-in the field (forreviews, see Anderson and May, 1978, 1979 or Toft,1986). These studies have many implications for con-servation biology, some of which are widely recognizedand others not. It therefore seemed a good idea to holda symposium on Conservation and Disease at the firstannual meeting for the Society for Conservation Biolo-gy , and to publish the four papers presented at thatsymposium in this issue of the journal.

The first paper, by Marilyn Scott, reviews evidence forthe ways in which infectious diseases may influence theecology of animal populations. In particular, Scott gives

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a sympathetic but critical account of the view held bysome wildlife biologists that diseases have little effect onthe demography of natural populations.

I believe much remains to be learned about how in-fectious diseases affect the persistence and distributionof animal populations, and that there are likely to bemany implications for the design of natural parks andrefuge areas. Very generally, many natural systems ap-pear to be held in some rough, long-term balance by theshifting dynamics of prey-predator, plant-herbivore,host-pathogen and other interactions among many dif-ferent patches. In these circumstances, the dynamicalbehavior of many populations may be different in a re-serve-even a very large reserve-than in the originallylarger whole from which the reserve is carved out. Thenonlinear nature of host-pathogen associations, withtheir threshold effects whereby endemic or epidemicinfections can be maintained or spread at high host den-sities but not at low densities, makes these associationsespecially likely to be affected by changes in spatialscale or other disturbances. One possible explanationfor the outbreak of canine distemper among the (lastremaining?) population of black-footed ferrets, whosehistory is recounted by Tom Thorne and ElizabethWilliams, could be that such epidemics came and wentamong sub-populations, depending on their changingdensities, in the pristine mosaic of ferret populationsthat embraced a fair fraction of North America betweenthe Rocky Mountains and the Great Plains (May, 1986).If this speculation is correct, we could have an examplewhere a disease that may have played a regulatory roleamong shifting patches in a larger ecosystem becomesan agent of extinction as the host range contracts. Suchshifting balances between carnivorous hosts and dis-eases arise in other situations of interest to conserva-tionists. Thus silver-backed jackal populations on theSerengeti appear to have exhibited an increase in aver-age density (and a contraction of average territory size)over the past few years, followed very recently by acrash that seems to be associated with an infectiousdisease (probably canine distemper; Moehlman, 1983).Wild dogs on the Serengeti are also known to have suf-fered from periodic outbreaks of disease during the past30 years (again probably canine distemper).

Human activities,which are ultimately responsible foressentially all conservation problems, can interact withdisease agents in subtle ways. In their symposium paper,David Rogers and Sarah Randolph show that the originalpatterns of settlement by humans in sub-SaharanAfricahad the effect of minimizing contact with tsetse flies(which are vectors for trypanosomiasis), while leavingtrypanosomiasis endemic among the original ungulatefauna. These cultural practices not only permitted muchof the pre-human ecosystem to persist alongside ex-panding human settlement, but they also provided a bar-rier to colonization by Arabs and other early invaders.

European invaders, however, set in train changes thatcontinue to have much greater impact on natural eco-systems, as the interplay between introduced and nativeherbivores has been altered by changing patterns of set-tlement and tsetse control. Rogers and Randolph em-phasize that trypanosomiasis was, until relatively re-cently, an important factor in helping to preservenatural ecosystems.Other examples where diseases gwe rise to conflictsof interest between human activities and wildlife areless subtle. Thus thousands of badgers have been gassedin their dens in Britain because they are reservoirs forbovine tuberculosis (TB), which affects the dairy cattleover whose pastures badgers roam at night (Andersonand Trewhella, 1985). Although the exisiting policy issound from a narrowly epidemiological standpoint,other methods of controlling bovine TB are possible;the bill, however, would tend to be paid by differentpeople. By the same token, when and if rabies is re-introduced into Britain there will be pressures to im-plement tentative plans for eradicating fox populationsin southern Britain (rather than, or as well as, vaccinat-ing dogs and cats), giving another instance where dis-ease poses difficult conflicts of interest for conservationbiologists.

The problems of disease among small (and often un-naturally crowded) populations in zoos and reserves arefamiliar, but continue to pose hard questions. Theseproblems may arise from new diseases or from old dis-eases in new settings. Tourism,or even the presence ofresearchers, can be a factor in introducing or spreadingsuch infections. As touched on by Thorne and Williamsin discussing the program of captive breeding of black-footed ferrets, the problems of disease in small popula-tions are often exacerbated by the associated geneticimpoverishment of the population. More broadly, onceit is conceded that infectious diseases are likely to beimportant agents of natural selection, many fundamentalquestions about the ecological significance of geneticdiversity, and about the effects of populationbottlenecks in reducing such diversity, assume newsignificance for conservation biologists (Hamilton,1982; May and Anderson, 1983; OBrien et al., 1985;Ralls and Ballou, 1988).

The problems of introduced or endemic diseases cansometimes pose uncomfortable ethical questions for re-searchers studying natural populations. For example,should a study group of chimpanzees in the wild bevaccinated against poliomyelitis, or should a polio out-break be left to run its natural course? The question(which has arisen in practice) can be further compli-cated by uncertainties as to whether the infection wasintroduced by contacts with humans or whether it oc-curred naturally in such populations. More generally,we can ask whether we should ideally aim to preservepopulations in natural association with their parasites

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and pathogens, or whether we should try to keep them-like humans in developed countries-unnaturally freefrom infectious diseases. This latter question is rarelyasked, much less answered.

These issues shade into those addressed in the paperby Andy Dobson, who askswhether infectious diseasesmay provide a sharp tool for deliberately eradicatingspecies that are unwanted invaders. Deliberate or acci-dental introductions of rats, cats, goats and other ani-mals, particularly to previously isolated islands, havecaused much destruction of native flora and fauna, andare responsible for the endangered status of many spe-cies. Dobson shows how the epidemiological propertiesof many viral, bacterial, protozoan or helminth patho-gens can make them magic bullets, affecting targetspecies but not others; he also surveys the many pre-cautions that should accompany the use of such weap-ons.

In short, infectious diseases are important in the ecol-ogy and biogeography of many species, and they arecorrespondingly important in conservation biology. Weare beginning to understand some, but by no means all,the many biological difficulties that diseases can causein the preservation of species and the management ofreserves. More intractable are the political problemsthat arise when programs designed to control diseaseamong humans or their livestock result directly or indi-rectly in the destruction of wildlife. Ethical questionsconcerning the control or eradication of disease in stud-ied populations or in reserves remain largely unasked,nor can such questions be answered until we have abetter undertanding of the ways in which infectious dis-eases influence individual behavior, population dynam-ics, community structure, and biogeographical patterns.References and NotesAnderson, R. M., and R. M. May. 1978.Regulation and stabilityof host-parasite population interactions. J Anim Ecol47:219-247; 249-267.

Anderson, R. M., and R. M. May. 1979. Population biology ofinfectious diseases. Nature 280:361-367; 455-461.Anderson, R.M., and R M . Trewhella. 1985. Population d ynamics of the badger (Meies meies) and the epidemiology ofbovine tuberculosis (Mycobactmurnbouis). Phil Trans RoySOC B310527-381.Bradley, D. J. 1974. Stability in host-parasite systems. Pages71-87 in M. B. Usher and M. H. Williamson, editors. EcologicdStability. Chapman and Hall, London.Hamilton,W. D. 1982.Pathogens as causes of genetic diversityin their host populations. Pages 269-296 in R M. Andersonand R. M. May, editors. Population Biology of Infectious Dis-ease Agents. Springer-Verlag, New York.Haldane, J.B.S. 1949. Disease and evolution. LaRicerca SciSuppl 19:68-76.May, R. M. 1986.The cautionary tale of the black-footed ferret.Nature 320:13-14.May, R. M. and R. M. Anderson. 1983. Epidemiology and ge-netics in the coevolution of parasites and hosts. Proc Roy SocB219:281-3 13 .Moehlman, P. D. 1983. Socioecology of silver-backed (andgolden jackals). Pages 423-438 in J. F. Eisenberg and D. G.Kleiman, editors. Recent Avances in the Study of MammalianBehavior. Special Publ. No. 7:Am Soc Mammal.OBrien, S.J., et al. 1985.Genetic basis for species vulnerabilityin the cheetah. Science 227:1428-1434.Ralls, K, and J. Ballou. 1988. Estimates of lethal equivalentsand the cost of inbreeding in mammals. Conservation Biology(in press).Toft, C.A. 1986. Communities of species with parasitic life-styles. Pages 445-463 in J. Diamond and T.J. Case, editors.Community Ecology. Harper & Row, New York.

Conservation BiologyVolume 2, No. 1, March 1988