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Behavioral Adaptations to Pathogens and Parasites: Five Strategies

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Behavioral Adaptations to Pathogens and Parasites: Five Strategies Neuroscience & BiobehavioralReviews, Vol. 14, pp. 273-294. o Pergamon Press plc, 1990. Printed in the U.S.A. 0149-7634/90 $3.00 + .00 Behavioral Adaptations to Pathogens and Parasites: Five Strategies BENJAMIN L. HART Department of Physiological Sciences, School of Veterinary Medicine University of California, Davis, Davis, CA 95616 Received 21 December 1988 HART, B. L. Behavioral adaptations to pathogens and parasites: Five strategies. NEUROSCI BIOBEHAV REV 14(3) 273-294, 1990.--The ever present threat of viral, bacterial, protozoan and metazoan parasites in the environment of wild animals is viewed as responsible for the natural selection of a variety of behavioral patterns that enable animals to survive and reproduce in this type of environment. Several lines of research, some quite recent, point to five behavioral strategies that vertebrates utilize to increase their personal or inclusive fitness in the face of parasites (broadly defined to include pathogens). These are: 1) avoidance of parasites; 2) controlled exposure to parasites to potentiate the immune system; 3) behavior of sick animals including anorexia and depression to overcome systemic febrile infections; 4) helping sick animals; 5) sexual selection for mating partners with the genetic endowment for resistance to parasites. The point is made that to consider a behavioral pattern as having evolved to serve a parasite control function the parasite or causative agent should be shown to adversely impact the animal's fitness and the behavior in question must be shown to help animals, or their offspring or group mates, in combating their exposure, or reducing their vulnerability, to the parasite. Parasites Pathogens Evolution Feeding behavior Sexual behavior Maternal behavior Grooming TO many the most profound theme in our current understanding of examine many examples of behavioral patterns that appear to animal behavior is the influence of natural selection shaping reflect adaptations to the threat of parasites and pathogens. The behavioral patterns. Whether looking at experiential influences or different types of behavioral patterns that animals use to avoid, those reflecting a more direct genetic endowment, there is a focus control or eliminate parasites from their bodies can be divided into on the strategies or coping mechanisms, such as those used in five strategies or categories. The first strategy comprises behav- predator avoidance or resource utilization, which enable animals ioral patterns that enable animals to avoid or minimize their to survive into reproductive adulthood and assure survival of their exposure to parasites. The second strategy is controlled exposure offspring. The fact that animals must avoid predators and acquire by which animals may expose themselves (or offspring) to small resources in order to survive to reproductive age and successfully samples of particular parasites or pathogens to facilitate develop- rear young, shapes various aspects of social, feeding, and repro- ment of the body's immunological competence. The third strategy ductive behavior. The concept presented in this paper is that the relates to the behavioral patterns of anorexia and depression that existence of disease-causing viruses and bacteria, as well as animals show when they are febrile with an infectious disease. The external and internal parasites, represent major forces shaping behavior of sick animals can be viewed as facilitating the fever behavior that are perhaps as profound as the forces having to do response in suppressing microbial infections and increasing the with predation or resource utilization. Wildlife biologists are animal's chance of recovery from the illness. A fourth strategy is familiar with a variety of naturally occurring disease epidemics the behavior of some animals in helping sick group mates or kin. that have had devastating effects on animal populations (57, 58, Finally, as the fifth strategy, animals may select mates on the basis 215). Although relatively rare, these phenomena provide powerful of providing offspring with the genetic basis for effective parasite examples of potential costs of disease-causing organisms when and disease control. behavioral and immunological responses do not adequately protect One can apply the general rules of inclusive fitness (I00) to the animals. Anderson and May (6) point to accumulating evidence behavioral adaptations related to pathogens and parasites just as in that parasites (broadly defined to include viruses, bacteria, proto- other behavioral systems. The efforts an animal may expend in zoans, helminths and arthropods) play a role analogous to that of preserving its own life and reproductive potential will extend to the predators and resource limitation in constraining the growth of offspring, in protecting them from parasites and in possibly animal populations. In studying and observing animals that live in helping sick or injured kin to survive. The concept of parasite relatively clean laboratories, field stations and domestic environ- control strategies focuses on the welfare of individual animals ments, and that are vaccinated against diseases and medically sufficient to assure survival of their offspring to reproductive age. treated when sick, it is easy to forget that animals evolved and This does not imply that individuals remain parasite- or disease- thrived in environments with an array of parasites long before free; it is clear that animals do sometimes succumb to disease and human protective measures were available. parasitism. In some instances parasites may be carded at a load In this paper I will address theoretical issues dealing with the which does not cause any noticeable decrement in health, but role of animal behavior in the control of parasitism or disease and might play a role when there are extreme demands on an animal's 273 274 HART resources such as in escaping from predators or undergoing to the differential effects of microparasites, macroparasites, para- nutritional stress. As in predator avoidance strategy, the fact that sitoids and predators on the stability of their host populations and an animal may eventually succumb to parasites does not mean that influences in regulating the population dynamics of hosts. the parasite control strategies are not adaptive. Similarly, the There are two requirements for accepting a particular behavior display of such behavioral strategies does not require the parasites as having a parasite control function. One is that the parasites in be always present. question should be shown to have a detrimental effect on the host's After going into some general issues about relations between fitness. The cost in fitness from an infectious, microparasitic parasites or pathogens and their hosts, I will discuss parasite- disease that kills an animal, or makes it susceptible to predation, related behavioral adaptations under each of the five strategies. is self-evident. As for macroparasites, a few lice or fleas may not This paper is written primarily with the student of animal behavior be harmful, but an overwhelming number may kill an animal. An in mind. However, an equal emphasis could be directed to intermediate parasite load may affect growth rate. Some macro- investigators interested in ecology or animal disease epidemiol- parasites may severely affect an animal only in times of nutrition ogy. If parasites are an unappreciated force from the standpoint of or socially related stress or in conjunction with other demands such behavioral science, then from the standpoint of ecology, epidemi- as lactating, fighting with a conspecific, or escaping from a ology, microbiology, and parasitology, behavior is an equally predator. Not to be overlooked is the cumulative effect of several unappreciated factor in how animals cope in an environment types of macroparasites, none of which alone may present a teeming with pathogenic viruses, bacteria and parasites. measurable cost to fitness. A parasite load in the laboratory may be studied in isolation from other parasites and thus not be represen- tative of the actual costs to an animal in the wild. In the section on GENERAL ISSUES OF HOST-PARASITEINTERACTIONS the avoidance strategy experimental findings on the costs of Before examining the specific strategies of behavior and macroparasites are reviewed. control of parasites, some general issues should be discussed. One The second requirement for accepting a behavior as having a of these is the coevolution of host-parasite relationships. In some parasite control function, and one which is basically the theme of instances parasites appear to have evolved behavioral strategies this review, is that the behavior in question should be shown to be themselves to counteract behavioral patterns that hosts use to avoid effective in helping an animal, or its offspring or group mates, to parasites. The predator-prey model is quite applicable here (266). avoid or remove the parasites or decrease their vulnerability to For example, fleas can jump with impressive speed and are thus parasites. Virtually any parasite control behavior will represent less likely to be dislodged by the grooming or scratching of the some cost in fitness to an animal as reflected in energy utilized, host which functions to eliminate fleas. Nasal bot flies that deposit distraction from predator vigilance or loss of feeding time. larvae in the nasal cavities of deer display ambush-like behavior Theoretically, the greater the cost of the parasite control behavior, that has the effect of counteracting
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