The Behavior of Parasitized Animals Author(s): Janice Moore Source: BioScience, Vol. 45, No. 2 (Feb., 1995), pp.

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The

Behavior of

Animals Parasitized

When an ant ... is not an ant

Janice Moore

was studying an ant, Leptothorax nylanderi, that lives in rotten wood, when he noticed that it had some strange nestmates (Plateaux 1972). The queens and workers of L. nylanderi are typically reddish yellow with large, blackishbrown abdominal bands; the males are blackish brown in color. The unusual nestmates were golden yellow and much smaller (Figure 1). They were generally tolerated, did not move around much, rarely foraged, and usually solicited food from the larger, darker workers. Unlike L. nylanderi, the yellow ants did not flee when disturbed. Plateaux concluded that these ants were a species of social parasite, and he began dissections in preparation for describing the new species. At that point, he realized that all the yellow ants contained an immature stage of a tapeworm, the cestode Anomotaenia brevis. This cestode has a typical complex life cycle in which immature stages live in an intermediate host (in this case, an ant), which must be eaten by a final host (in this case, the spotted woodpecker) before the parasite can mature and reproduce in the final host, releasing eggs into the host's feces. Plateaux then recognized that the yellow ants were, in fact, conspecifics of the larger, dark ants, and he

renchbiologistLuc Plateaux

Parasites can so greatly alter a host's behavior that they change its ecological function
attributed the changes in color and behavior to the parasitic worm. The infected ants, which tended to remain in a disturbed nest, would be more likely than their scurrying nestmates to be devoured by a natural predator, such as a woodpecker, in whose intestine the parasite could mature and release eggs in feces for the next round of ant infectionsfrom the tapeworm's point of view, a satisfying cycle. The point to remember here, in addition to the tapeworm's presumed happy ending, is that the parasitized ants differ so much in behavior and appearance from their uninfected nestmates that a skilled scientist was prepared to treat them as a new species. The L. nylanderi-A. brevis story is not just a novelty. It is possible that parasitized animals are frequently so altered compared with their uninfected conspecifics that they well may be the functional equivalents of different species. While they may not always look as unusual as infected L. nylanderi do, more often than not they differ from uninfected counterparts in traits like activity levels, microhabitat choices, foraging behavior, odor, phototaxis, or social

and sexual behavior. Thus, their function in a population, community, or ecosystem may differ considerably from that of conspecifics. In addition, while such alterations often benefit the parasite by increasing transmission, there are also cases where the opposite occurs: transmission is not enhanced, and if the observed changes have a beneficiary, it seems to be the host.

Enhanced transmission
In the L. nylanderi-A. brevis association, it is quite possible that unusual coloration, together with sluggish movement, enhances transmission of the parasite to the next host. Enhanced transmission is frequently hypothesized to be the adaptive consequence of alterations in reasonable parasitized animals-a expectation (Combes 1991). For instance, acanthocephalans (thornyheaded worms) are adults in the intestines of vertebrates, where they produce eggs that are disseminated with the final hosts' feces. When eaten by an arthropod intermediate host, the egg hatches and the larval stage burrows into the hemocoel, where it develops to a stage that is infective for the final host. Acanthocephalans can alter behavior in intermediate hosts, which then become more susceptible to predation. For example, unlike uninfected counterparts, an aquatic isopod, Asellus intermedius, infected with Acanthocephalus dirus was lightcolored and hyperactive, and it attempted to crawl up the sides of the

Janice Moore is a professor in the Biology Departmentat Colorado State University, Fort Collins, CO 80523. ? 1995 American Institute of Biological Sciences. February 1995

89

aquarium and over the leaf litter it contained. In aquarium experiments, creek chubs (Semotilus atromaculatus) ate significantly more infected than uninfected isopods (see Combes 1991, Moore and Gotelli 1990, for review).' Are these active, parasitized animals seeking food? Hechtel and colleagues (1993) reported that infected isopods spent significantly more time

substrate and in areas of relatively low humidity than did uninfected .? *;*...'. ..J. . _ isopods. They were also less likely -' l to be found under overhangingshelter. In the field and in aviary tests, Europeanstarlings(Sturnusvulgaris; Figure 3) preyed upon infected isopods more frequentlythan would be predicted on the basis of their frequency in the isopod population (Moore and Gotelli 1990). Unlike larval acanthocephalans, which live in the hemocoel of arthropods, the larval trematode, Microphallus papillorobustus, encysts in the nervous systems of two species of Gammarus. There it induces photophilia in animals that are usually photophobic. Consequently, infected gammarids were more than twice as likely as uninfected animals were to be eaten by the gull (Larus cachinnans), a potential final host. Another trematode, Maritrema subdolum, does not itself invade the nervous system but can co-occur with M. papillorobustus in gammarids.It may benefit from the behavioralchanges induced by the other parasite (Moore and Gotelli 1990). Poulin et al. (1992) found that when the cestode Eubothrium salvelini reached the developmental stage where it is infective to the final host (brook trout, Salvelinus fontinalis), its intermediate hostcopepod Cyclops vernalis-began to swim more often and was more . :/% ? :'% .? : ........ ...:....... likely to be eaten, compared with uninfected copepods. Larvae of the mosquito Aedes aegypti that contained more than three immature . The dark ants contrast with the light-colored intercastes female Figure parasitthe parasittrematodes(Plagiorchisnoblei) were light-colorentercastes ized by by the the tapeworm tapeworm Choale anotaenia unicornawith unicornata. Photo:Laurent Pe'ru. Choanotaenia ized less active than uninfected mosquitoes and spent more time near the
on top of 2-centimeter disks made of leaves rather than under them. Because the leaves could be accessed as food from either side, the authors concluded that the infected isopods' increased activity and exposure were not due to increased demands for energy and thus increased foraging. Such behavioral changes observed in the laboratory may well have ecological consequences in free-living Terrestrial isopods populations. (Armadillidium vulgare) infected with the acanthocephalan Plagiorhynchus cylindraceus (Figure 2) spent more time on light-colored surface of the water, where they were ingested by meadow voles (Microtus pennsylvanicus), a final host. (They were not, however, subject to increased guppy [Poecilia reticulata] predation.) In addition, there are examples of altered behavior in which increased predation has not been a demonstrated outcome but is assumed to be probable (Moore and Gotelli 1990). On the other hand, not all parasites-or all developmental stages of a parasite-alter host behavior. The amphipods Gammarus lacustris and Hyalella azteca showed no be-

'In an effort to abbreviate the bibliography, review papers have been cited where possible; readers are urged to consult these for primary sources.

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havioral changes when infected with the cestode Lateriporus spp. or with developing stages of acanthocephalans; they remained photophobic, and their evasive responses were normal, consisting of diving and burrowing upon disturbance. Infective stages (cystacanths) of Polymorphus paradoxus (Acanthocephala) in G. lacustris, however, caused a positive reaction to light (as did cystacanths of Polymorphus marilis and Corynosoma constrictur in H. azteca). Infection with P. paradoxus cystacanths was also associated with a clinging response to disturbance; instead of diving, the infected amphipods clung to vegetation, sticks, and even potential predators. The result was that in laboratory tests, predators ate more infected than uninfected amphipods. Although cystacanths of all three parasites are visible and bright orange or red, the behavior and not the appearance is what is critical in this predator-prey interaction; if similar spots were painted on uninfected amphipods, they did not suffer increased predation (Moore and Gotelli 1990). Enhanced transmission also may be associated with altered behavior in the absence of predation-mediated transmission. For example, parasite-induced behavioral alterations can enhance transmission via host dispersal or hematophagy. When parasitized by Gynaecotyla adunca, the snail Ilyanassa obsoleta (Figure 4) increased the time it spent in the high intertidal during nocturnal low tides. Curtis (1990) hypothesized that such a habitat shift allowed the release of larval trematodes in the vicinity of the next intermediate host, a semiterrestrial crustacean. While some parasites are transmitted by being eaten, others enter new hosts when the current host feeds, which is often the case for parasites transmitted by hematophagous insects. Vector foraging may be modified by parasites (reviewed in James and Rossignol 1991, Moore 1993). Although not a ubiquitous phenomenon (Li et al. 1992), increased probing for blood, which can enhance transmission (e.g., Kelly and Edman 1992), has been demon-

Figure 2. The larva (cystacanth) of Plagiorhynchus cylindraceus is a large parasite in its terrestrial isopod host. (The white dot on pillbug is a reflection.) Photo: Janice Moore. associations. A number of parasites that use hematophagous insects as vectors (e.g.,Leishmania in sandflies [e.g., Lutzomyia longipalpis], Trypanosoma spp. in tsetse flies [Glossina pallidipes] and triatomine bugs [Rhodnius prolixus and Rhodnius robustus], and malaria and LaCrosse virus in mosquitoes; Figure 5) seem to have converged on this alteration. Mechanisms thought to induce such behavior range from parasites physically blocking the mechanoreceptors that monitor blood flow as the insect feeds (e.g., trypanosomes) to the reduction of salivary enzymes that assist mosquitoes when locating blood (e.g., malaria). Parasiteinduced behavioral alterations are frequently consistent with a hypothesis of enhanced transmission, which can be true whether transmission is accomplished by such diverse means as predation, host dispersal, or hematophagy. Nonetheless, there are cases of altered behavior that do not necessarily support the transmission hypothesis.

eficial for the parasite. On the moors of northern England, the nematode Trichostrongylus tenuis has only one host-the red grouse, Lagopus lagopus. Hudson et al. (1992) concluded that infection predisposes incubating females to predation; infected birds were located by scent-trained dogs more frequently than were birds that had been treated and were rid of their parasites. Because T. tenuis disrupts caecal tissue, causing substantial pathology, infected females may produce conspicuous caecal feces, whereas healthy females do not produce caecal feces during spring incubation. Increased predation upon infected grouse cannot benefit the parasite, which is shedding eggs in grouse feces and which will die if consumed by a grouse predator. There are other cases of parasitized animals being subject to both altered behavior and the possibility of increased predation without transmission occurring. In general, altered behavior and resulting predation do not assist transmission when they coincide in single-host life cycles. However, it is tempting to speculate that altered behavior might result in such transmission to predators (which may be final hosts) when it occurs in complex life cycles. Such hypotheses require the scrutiny of experimental examination.

Alternative explanations
Unfortunately, although the idea of altered behavior as adaptive for parasite transmission is a reasonable hypothesis, it obviously does not pertain to all examples of altered behavior and, even when it might be applicable, it is difficult to test in many associations. Consider the so-called brainworm, the larval stage of the trematode Dicrocoelium dendriticum, which encysts in a depression between the roots of subesophageal nerves leading to the mouthparts of the ant, Formica nigricans. As the temperature decreases and their nestmates return to the nest, these infected ants sink their mandibles into blades of grass and remain there overnight, presumably included in the forage of final host ungulates grazing at dawn. Variations on this theme occur in at least 91

When transmission is not enhanced

One of the challenges for evolutionary biologists is to discriminate between adaptations and other expressions of pathology when observing the behavior of parasitized animals. For instance, while behavioral alterations may increase the risk of predation, not all predation is ben-

strated in several vector-parasite

February 1995

two other dicrocoelid-ant associations, and in all of these cases, predation by the final host seems likely but is difficult to demonstrate (reviewed in Moore and Gotelli 1990). Ants infected with the fungus Entomophthora are also known to crawl up on vegetation (Spindleret al. 1986). While this action disperses the fungal spores to the wind, predation on such an accessible ant might not be advantageous for the fungus, depending upon its fate in the predator's digestive tract. The altered behavior might, however, be advantageous for the insect host, especially if exposure results in higher body temperatures. Such a behavioral fever (therapeutic selection of unusually warm microhabitats) can increase the survivorship of flies infected with a congeneric fungus. There is also evidence in crickets (Gryllus bimaculatus) infected with Rickettsiella grylli and grasshoppers(Melanoplus sanguinipes) infected with Nosema acridophagusthat parasitizedinsects choose warmer temperatures than do uninfectedones and thus increase their survival (reviewed in Horton and Moore 1993, Moore and Gotelli 1990). The availability of days that allow grasshoppers to bask may set geographic limits on the range of the fungus Entomophaga grylli and its effect on grasshopperpopulation levels (Horton and Moore 1993). Thus, behaviors such as crawling up, while increasing predation risk, and in some cases, the probability of parasite transmission, might also benefit a host. Fever is not limited to insects (Cabanac 1990, Kluger 1991). Several workers have reported that fish infected with immature stages of solidus) tapeworms(Schistocephalus prefer warmer water (see review by Moore and Gotelli 1990). LoBue and Bell (1993) discovered a population of three-spined sticklebacks (Gasterosteus aculeatus) that become demelanized,with exceedingly melanized eyes, when parasitized by S. solidus. Parasitized fish are actually more buoyant than unparasitized fish, and LoBue and Bell suggested that they would suffer increased predation. Because surface water often tends to be warmer
than deeper layers, temperature too

Figure 3. The starling nestling that begs more vigorously may indeed get more food-and more food-transmittedparasites. Before fledging, heavy nestlings tend to have more Plagiorhynchus cylindraceus. Photo: John Rotenberry. may affect the parasite-host association. In contrast, some animals respond to parasites by moving into colder conditions. The freshwater snail Biomphalaria glabrata infected with the trematode Schistosoma mansoni preferred lower temperatures where parasite development was inhibited (Lefcort and Bayne 1991). Bumblebees (Bombus terrestris) parasitized by conopid flies exhibited a preference for cold temperatures compared with uninfected conspecifics. In the field, they remained out of the nest at night, in colder microhabitats. Cold temperatures retarded parasitoid development (Muller and Schmid-Hempel 1993). Thermoregulation might also be related to other changes believed to increase host conspicuousness to substrate predators-hyperactivity, color choice, or changes in color or size, for instance (Horton and Moore 1993). [Note that because humans are highly visual, most evaluations of conspicuousness are based on changes that can be seen. Examples of alterations that would affect other senses-grouse scent, for instanceare extremely rare. Probably they have not been sought and perhaps are not noticeable to human investigators.] Thus, even in complex life cycles, altered behavior may not always have a single explanation (Moore and Gotelli 1990). There are more described cases of

altered behavior itself than there are demonstrations of, say, enhanced transmission or, for that matter, enhanced defense. In general, the behavioral phenomena lend themselves to a straightforward investigation more readily than do their epidemiological consequences. When tests of the transmission hypothesis are not feasible, the ontogeny of behavioral shifts may be informative. For instance, behavioral alterations in an acanthocephalan-gammarid system coincided with infectivity of the parasite to the final host. Thus, even if enhanced predation had not been demonstrated, this example would be a strong argument for a benefit to the parasite (Hurd and Fogo 1991, Moore and Gotelli 1990, Poulin et al. 1992, Tierney et al. 1993). Meanwhile, although the beneficiary of parasite-induced alterations may not always be obvious, what is increasingly clear is the ubiquity of behavioral alterations associated with parasitism.

Behavioral effects on uninfected animals

Can hosts avoid parasites? There have been few investigations of this possibility (but see Lafferty 1992). Lozano (1991) suggested that the diets of potential hosts could be influenced by parasites if the hosts avoided parasitized foods or chose medicinal foods-a defensive diet to parallel other forms of defensive behavior (see below). Moore (1983) found that isopods tended to avoid eating starling feces that contained acanthocephalan eggs. On the other hand, Evans et al. (1992) found that the beetle (Tribolium confusum) intermediate host of Hymenolepis diminuta was more attracted to rat feces containing the cestode's eggs than to uninfected feces; the same may be true of cockroaches (Periplaneta americana) confronted with uninfected rat feces and feces from rats parasitized by the acanthocephalan, Moniliformis moniliformis.2 Jarecka (1961) observed that parasite eggs themselves might be
2L. M. Carmichael, 1991, personal observaCO.

tion. Colorado StateUniversity,Fort Collins,

92

BioScience Vol. 45 No. 2

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attractive food items. Some cestode eggs resembled diatoms, complete with small stripes, and they seemed to appeal to ostracod intermediate hosts that normally ingested diatoms. Other eggs were shaped in ways that favored settling on water plants that were eaten by intermediate hosts. Cestode species that produced heavier eggs used benthic crustacean intermediate hosts; species with floating eggs used swimming hosts. Size also limited which hosts could ingest the cestode eggs. Demonstrations of the avoidance of parasitized intermediate hosts are also rare. Macoma balthica, a bivalve, usually burrows, but some individuals migrate just beneath the surface of the sand, creating visible tracks. Trematode-infected M. balthica can invariably be found at the end of such tracks. They are much less common among burrowing conspecifics, which in addition often occur lower in the intertidal than the infected mollusks do. Therefore, infected M. balthica should be easily accessible to predators. One oyster catcher (Haemotopus ostralegus) routinely rejected heavily infected clams, however. It is not clear how the oyster catcher knew to avoid them, but the white sporocysts are clearly visible once a valve is removed (Lim and Green 1991, reviewed in Moore and Gotelli 1990). Feces can be a source of parasites, and some animals avoid fecal matter. For instance, young cattle preferentially graze in areas not contaminated by cattle feces and the nematode Dictyocaulus viviparous. Primate movement patterns are consistent with a hypothesis of fecal contamination avoidance (Moore and Gotelli 1990). Brown and Brown (1992) hypothesized that ectoparasites may be a more important cause of dispersal than previously recognized. They observed that while cliff swallow (Hirundo pyrrhonota) young usually return to natal colonies, individuals that are heavily parasitized by fleas (Ceratophyllus celsus) and swallow bugs (Oeciacus vicarius) disperse to non-natal colonies. Warble fly (Hypoderma tarandi) has been suggested as a possible cause of postcalving migration in Rangifer tarandus (Folstad et al. 1991). February 1995

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Black-spotted sticklebacks (Gasterosteus wheatlandi) alter habitat usage and spend more time in open water when the parasitic branchiuran, Argulus canadensis, is present in vegetated areas (reviewed in Hart 1990, Moore and Gotelli 1990). Sticklebacks form larger, more inclusive shoals in response to the presence of A. canadensis (Poulin and Fitzgerald 1989). Starlings use nesting materials that repel ectoparasitic insects (Clark 1990). Ants adjust the time of foraging and the size of foragers that are sent out in order to avoid losses to parasitoids (reviewed in Moore and Gotelli 1990, Orr 1992). Ungulates are especially notable in their avoidance of insect pests (Mooring and Hart 1992). Cattle frequently bunch (reviewed in Hart 1990, Ralley et al. 1993), and horses may shift habitats and form tempo(Duncan and rary associations Cowtan 1980, Rutberg 1987). The principle of the selfish herd applies to insect as well as predator avoidance (Hamilton 1971, Mooring and Hart 1992): animals-especially centrally located animals-fare better in such groups. Even zebra stripes may be an adaptation that reduces attractiveness for tsetse flies (reviewed in Moore 1993).

(Acyrthosiphon pisum) have been used extensively to explore the notion of defending kin by suicidal behavior on the part of parasitized relatives (e.g., McAllister et al. 1990). Changes in the behavior of yet other aphids are thought to protect the parasitoid from hyperparasitism (Brodeur and McNeil 1992). While lethargy may benefit a host striving to eliminate a pathogen (Hart 1990), it also can invite further transmission. Hematophagous insects often face the daunting prospect of highly defensive hosts. Defensive host behavior can strongly influence the choice of host species and individual (Moore 1993, Scott et al. 1988). This defensive behavior itself can be modified by parasites (Moore and Gotelli 1990). Mice infected with Plasmodium spp. (the causative agents of malaria) became lethargic and reduced antimosquito behavior at times when the blood-

Who benefits?
Beneficiaries of altered behavior are not always obvious. A behavioral alteration that seems to harm the host may ultimately benefit the host genotype if host kin are protected (Smith Trail 1980). Pea aphids

Figure 5. This engorged mosquito is finishing a meal of human blood. Photo: Marc Klowden.

93

inevitable: one study found no evidence for such preference on the point of the mosquitoes for humans that were hosts to a mild, asymptomatic malaria (reviewed in Moore 1993). Thus, while lethargy may benefit a host striving to eliminate a pathogen (Hart 1990), it also can invite further transmission. Defensive behavior is but one of many ways that animals attempt to avoid parasites;in otherwords, parasites influence not only the behavior of their own hosts but also the behavior of animals as they attempt not to become hosts. Must all behavioral changes benefit host or parasite? When M. balthica crawls near the surface of the sand, it may be responding to direct manipulation by its trematode parasite, or it may be seeking to satisfy increased oxygen needs imposed by the parasite. Is such an altered behavior a parasite manipulation or is it a host making the best of a bad situation? Under conditions of low oxygen, sticklebacks (Pungitius pungitius)
94

Parasites may also influence what hosts eat. Bumblebees containing conopid parasitoids did not choose the same flowers that uninfected bees did (Muller and Schmid-Hempel 1992). Trematode infections may alter dietary preferences among snails. Although many of these nutritional shifts cannot currently be said to benefit parasite or host, there is evidence that chimpanzees (Pan troglodytes) may ingest some plant parts for medicinal purposes-they may handle them in unusual ways, eat very small amounts, and restrict usage to times of obvious malaise. Figure 6. Standing on a bare, black hill, these horses may be avoiding insects that These plants are often known for are abundant at a nearby creek. Photo: Janice Moore. their ethnomedicinal value (reviewed in Hart 1990, Newton and Nishida borne parasite was most infective to parasitizedby S. solidus spend more 1990). mosquitoes. When given a choice, time at the surface of the water than Dietary shifts may also ensue if mosquitoes were more likely to feed do uninfected fish and return more parasites affect host competitive on these malarious mice. readily to the surface when fright- ability. Sticklebacks, if parasitized Baylis and Nambiro (1993) in- ened away by an image of a preda- with either S. solidus or Glugea ferred a reduction in defensive be- tor. Are they more easily preyed anomala, a protozoan, ceased to havior in cattle infected with upon by the next host? If so, to what display their usual preference for Trypanosomacongolense when they extent can increased oxygen de- the larger of two size classes of prey; found that although there was no mands of the host be seen as a para- in fact, when both parasites were difference in the attractiveness of site adaptation? (Moore and Gotelli present, the fish preferred the smaller infected and uninfected cattle, the 1990; see also Holmes and Zohar of the two prey classes, perhaps betsetse fly experienced 75% more 1990 for a review of pathology as- cause of decreased competitive abilsuccess feeding on infected hosts. sociated with host behavior.) The ity (reviewed in Moore and Gotelli Again, such modifications are not difference between the two condi- 1990).

tions is not always clear; after all, virulence itself has been subjected to natural selection over the history of host-parasite associations. Parasitizedhosts may differ from uninfected animals in their requirements for resources such as food, as well as oxygen. Anorexia is common among infected vertebrates. Gammarus pulex infected with Pomphorhnychus laevis ate much less than controls (Brownand Pascoe 1989), as did rainbow trout (Oncorhynchus mykiss) infected with a hemoflagellate (Cryptobia salmositica; Lowe-Jinde and Zimmerman 1991). Hart (1990, 1992) viewed anorexia in homeotherms as part of a constellation of adaptiveresponses that assisted in physiological defense against infectious organisms. Schistosome-infected B. glabrata, on the other hand, increased quantity and altered timing of feeding relative to uninfected snails, while trout hosts of the nematode Truttaedacnitis truttae did not alter food intake (reviewed in Moore and Gotelli 1990).

Other behavioralchanges
Parasites can also affect social behavior in a multitude of other ways (Moller et al. 1993). By virtue of their roles as castrators or indicators of mate quality, parasites can influence the ability to acquire mates or produce young, and they even may have played a major role in the evolution of sex itself (see Clayton 1991, Hamilton et al. 1990, and Zuk 1992 for recent reviews). There have been reports of parasitized animals becoming either less or more aggressive. Toxoplasma infections in mice favored dominance and increased aggression, a result that Arnold et al. (1990) suggested fit a general lack of wariness that characterizes much of the behavior of such infected mice. Oh the other hand, mice infected with Trichinella

gyrus were subordinate to uninfected mice (Moore and Gotelli 1990). Schall and Houle (1992) found that malarious lizards (Sceloporus

spiralis or Heligmosomoides poly-

BioScienceVol. 45 No. 2

occidentalis) chased other lizards less and did not posture as aggressively as did uninfected lizards. Xenophobia among primates may reflect an evolutionary history of parasite avoidance (reviewed in Moore and Gotelli 1990). Price et al. (1988) have reviewed the literature indicating that parasites can influence the outcome of competition between host species. They noted that parasitism may be responsible for some of the extinctions that have accompanied biotic mixing-a prime example is the decimation of human populations in the New World during its colonization by Europeans. Human behavior is certainly not exempt from the influence of parasites. Sorry, a drink with dinner is not likely to protect you from trichinosis (Campbell 1977). On the other hand, Edman (1988) has suggested that large-scale changes in human behavior accompanying the development of agriculture may have encouraged several vectors to shift from rodent or bird blood sources to more predictable humans. These behaviors include various aspects of water storage and irrigation, habitat modification, and shifts in availability of alternative hosts. A judicious look at these and other possibilities may lead us to policies that could decrease the incidence of vector-borne diseases. Human marriage systems also may have responded to increased pathogen stress with increases in polygyny (Low 1990). In modern times, parasitism can affect several aspects of mental development in children, either directly or indirectly (Kvalsvig et al. 1991). Ewald (1988) proposed that cultural vectors (e.g., hospital attendants) can have the same epidemiological and evolutionary effects as biological vectors such as insects.

Conclusions
Parasitism can have a wide variety of effects on host animals. Parasitized animals may respond differently from uninfected conspecifics to stimuli such as light, heat, colors, and mates. Their activity, appearance, and size may be altered. They may be distributed differently and February 1995

may be the source of altered sounds or smells. Their social role is changed, and they use resources differently. In particular, foraging can be altered both quantitatively and qualitatively. Parasites affect a variety of dominance interactions and may shift competitive outcomes between animals. Even unparasitized animals may exhibit behavioral alterations when trying to avoid parasites. Some of these altered behaviors appear to be adaptations for increased transmission. Others may be part of an overall host defensive strategy. In some cases, the outcome may shift between these two possibilities, depending upon environmental conditions. The alterations may be caused by gross pathology or by subtle biochemical and neurophysiological changes that are still poorly understood. What is clear is that parasites alter the distribution and abundance of animals-not only through the obvious influences of malaise and mortality but also by creating subpopulations of individuals that differ from normal in their behavior. The implications for the rest of biology are far-reaching. If parasitized animals forage differently, how is nutrient flow affected? If competitive interactions are influenced, how does the presence or absence of a parasite affect community structure? What are the switches that some parasites have found that reverse responses to a simple stimulus such as light? Do the vectors that spread disease also prefer microhabitats that differ from uninfected conspecifics, and if so, can this difference be used to target infected subpopulations and enhance vector control and avoidance? When you see a snail move through the intertidal or observe a terrestrial isopod crawl across the sidewalk, what organism is at the controls-the snail, the isopod, or a parasite?

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Acknowledgments
I am grateful for the support of NSF DEB-9119414 while I wrote this article. Larry Curtis, Marc Klowden, and Laurent Peru generously shared photographs of their research organisms with me.

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