Abstract
> <br> Behavioral modifications have been observed in many insects as a result of parasitism or
> pathogens.&nbsp; Altered behaviors can include changes in activities which result in the insect being more <br> conspicuous to predation.  The insect may also alter its body temperature, foraging or oviposition time
> and location, or respond to environmental or mate stimuli differently.&nbsp; These alterations in behavior <br> may represent a wide range of underlying mechanisms with many possible outcomes for parasite and
> host (Moore and Gotelli 1990).&nbsp; Induced behavioral alterations could have arisen for the following <br> reasons as given by Horton and Moore (1993):  the modifications could be natural selection benefiting
> the host, natural selection benefiting the parasite or pathogen, or a consequence of pathology benefiting <br> neither the host nor the parasite or pathogen.
> <br> Many hypotheses have been introduced to explain how the modified behaviors evolved.  These
> theories include kin selected-host suicide, enhanced parasite transmission and survival, and host <br> defense.   Kin selected-host suicide, which may be a behavior of bumblebee workers infected with
> parasitoids, results in behavior changes of the host that increase the host's predation risk with the hope <br> of protecting uninfected kin.   The insects rely on inclusive fitness, that is fitness gained through the
> replication of copies of an individual's genes carried in others through the result of their own actions.&nbsp; <br> Enhanced parasite transmission is thought to consist of behaviors induced by the parasite on the host
> which increase the chances of the parasite entering its final host.&nbsp; This type of behavior may be <br> characteristic of several cockroach species whose behavior becomes more conspicuous to predation
> when infected.&nbsp; Parasites may also alter host behavior in order to increase the parasite's chances of <br> survival, as in aposematic caterpillars and aphids infected with their respective parasitoids.   That is,
> the behavioral change may cause the host to be less susceptible to predation, thereby increasing the <br> chances of parasitoid development and survival.   Host defense is best demonstrated by those insects who
> exhibit behavioral fever in response to a pathogen.&nbsp; By choosing microhabitats which are warmer, the <br> host is able to effectively protect itself from the pathogen by inducing physiological fever.  Examples of
> behavioral fever have been documented in the grasshopper, the cricket, the Madagascar cockroach, the <br> tenebrionid beetle, and the house fly.
> <br> Although Poulin (1995) warns against defining these behaviors as adaptations, many of the
> behaviors do appear to have some adaptive value.&nbsp; The following is a review of several articles <br> demonstrating behavioral modifications of insects to parasitic and pathogenic infections.
> <br> Introduction
> <br> Parasites are known to alter the behavior of the animals in which they live.  This behavioral
> alteration can make the host more conspicuous to predators than uninfected individuals are.&nbsp; Altered <br> behaviors can also include choosing different microhabitats, dietary items, and displaying different
> social status, competitive ability, attractiveness to mates, and activity levels from uninfected <br> conspecifics (Moore and Gotelli 1990).  Changes in microhabitat preference in parasitized insects that
> constitute an altered behavior include seeking higher elevations, seeking exposed locations, seeking <br> concealed locations, changes in reaction to light, nocturnal insects displaying diurnal activity, changes
> in temperature regime, or changes in foraging or oviposition sites (Horton and Moore 1993).<br>
> There are many hypotheses as to why parasitized animals would exhibit behavioral changes.&nbsp; The <br> behaviors could be described as (1) beneficial to the parasite,  making the intermediate host more
> susceptible to predation and allowing the parasite to be transmitted to the definitive host.&nbsp; This <br> susceptibility to predation is only advantageous however, if the parasite is in an intermediate host
> which is preyed upon by the final host, and if the parasite has developed to its infective stage.&nbsp; &quot;By far <br> the majority of documented parasite-induced changes in host behavior thought to be parasite
> adaptations are believed to enhance parasite transmission&nbsp; from host to host&quot; (Poulin 1995).&nbsp; The <br> behaviors may also be beneficial to the pathogen.  The changes may cause better dispersal of an air-
> borne pathogen or enhance the pathogens growth rate.&nbsp; (2) The modified behavior may be beneficial to <br> the host.    From the intermediate host's perspective behaviors such as choosing different locations or
> lighting regimes could constitute induced physiological fever (behavioral fever) and exist as an <br> mechanism to fight off the parasite.   Such situations would have arisen by natural selection to benefit
> the host.&nbsp; Behavioral fever has&nbsp; been observed for several insects infected with protozoans, endotoxins, <br> or bacterial pyrogens.  This behavior would be considered host defense (Horton and Moore 1993). 
> Other explanations for altered behavior due to parasitism include kin selected-host suicide.&nbsp; In host <br> suicide the host behaves in such a way as to increase the probability of death by predation in order to
> lower the risk of parasite infection for other members of the host species (Smith Trail 1980).&nbsp; (3) <br> Other modifications of behavior could not be adaptive to the host or the parasite, but rather the
> response to the pathological effects of the parasite (Robb and Reid 1996).<br>
> Changes in host behavior are often reported in scientific literature and are attributed as being <br> adaptive for the parasite or for the host.  Poulin (1995) suggests however that defining an adaptation
> deserves more rigorous criteria than what has been presented in the past.&nbsp; Accordingly, alterations in <br> host behavior following infection can be defined as adaptations only if they meet certain criteria: "(1)
> they must be complex; (2) they must show signs of a purposive design; (3) they are more likely to be <br> adaptations if they have arisen independently in several lineages of hosts or parasites; and (4) they
> must be shown to increase the fitness of either the host or the parasite&quot; (Poulin 1995).&nbsp; Poulin <br> (1995) indicates that few host-parasite relationships display all of these criteria.  Although many
> show a purposive design, few are complex, and the fitness benefits for most are still ambiguous.&nbsp; <br>
> The following is a review of the more recent works in the area of behavioral alterations <br> observed in insects.  This review has been split into two sections: modified behaviors induced by
> parasitism and modified behaviors induced by endotoxins.&nbsp; In each section examples of behavioral <br> modifications are included for a variety of insects.  Also included is a hypothesis on the adaptive value of
> the behavior: beneficial to host (host defense, and kin selected-host suicide),&nbsp; beneficial to parasite, or <br> a result of pathology with no adaptive value to host or parasite.
> <br> Discussion
> <br> Modified behaviors induced by parasitism
> <br> Stamp (1981) observed parasitized and nonparasitized aposematic caterpillars (the Baltimore
> checkerspot Euphydryas phaeton Drury).&nbsp; She examined the level of mortality of the parasitoids <br> (Apanteles euphydryidis Muesebeck) in order to test the hypothesis of host suicide, that parasitized
> caterpillars advertise themselves to their predators which increases the survivorship of their <br> nonparasitized siblings.  For the host suicide hypothesis to hold, certain restrictions would have to be
> met: the parasitized host should be unable to reproduce, kin should be gregarious, possibilities should <br> exist that the developing parasite would eventually parasitize the kin, and the changes in the host
> behavior should decrease the hosts survivorship (Horton and Moore 1993).&nbsp; Her observations did not <br> support a kinship protection-host suicide hypothesis.  Rather, the behavior of the caterpillar seemed to
> be induced by and beneficial to the parasitoid.&nbsp;&nbsp; The caterpillars, by acting differently, were actually <br> increasing their survivorship as well as the survivorship of the parasitoid by allowing the parasitoid
> to escape predation and hyperparasitism.<br>
> The parasitic wasp Aphidius nigripes, an endoparasitoid of the potato aphid Macrosiphum <br> euphorbiae, completes its pupal development within the mummified aphid host (Brodeur and McNeil
> 1989).&nbsp; Brodeur and McNeil (1989) not only showed that parasitized hosts behaved differently than <br> unparasitized hosts did, but that the behavior depended on the developmental stage of the parasitoid. 
> Aphids containing diapausing parasitoids tended to mummify in concealed areas, while aphids containing <br> nondiaposing parasitoids remained on the leaf near food and other possible aphid hosts.  The aphid hosts
> of diaposing parasitoids, which were preparing to overwinter,&nbsp; sought out protected areas, away from <br> possible physiological and mechanical damage.  The diaposing parasitoids were also able to avoid adverse
> climatic conditions and reduce the chances of hyperparasitism by concealing themselves and their host.&nbsp; <br> This shows one of the more clear examples of a parasite altering the host's behavior in order to
> increase its survivorship.<br>
> The altered behaviors observed in several cockroach species also seem to support the parasite <br> survival hypothesis.  Parasitism affected substrate use and activity in the cockroach species studied
> (Moore et al. 1994).&nbsp; Infected male brown cockroaches, Periplaneta brunnea, spent more time on <br> white horizontal surfaces than did uninfected cockroaches (Carmichael and Moore 1991).  Moore and
> Gotelli (1992) observed decreased travel velocity and distance, and increased use of horizontal <br> substrates for two species of cockroach, Periplaneta americana and Blattella germanica, infected with
> the acanthocephalan Moniliformis moniliformis.&nbsp;&nbsp; They attributed three possible factors to the shift in <br> substrate use: cockroaches on horizontal surfaces may be more susceptible to predation (a behavior
> beneficial to the parasite), reduced sexual sensitivity because cockroaches usually stand on vertical <br> surfaces to enhance the ability to contact females (altered sexual selection behavior), and using
> horizontal surfaces may require less energy than clinging on to vertical surfaces (a behavior reflecting <br> the possible pathological constraints on energy level of the host). 
> <br> Moore and Gotelli (1996) also looked at the phylogeny of behavior modifications in several
> cockroach species to further test the possibility that the behavioral changes were adaptive.&nbsp; The fact <br> that phylogenetic analysis of the components of behavioral alterations in many cockroach species to
> infection were not always shared by close relatives was encouraging, according to Moore and Gotelli <br> (1996).  It supports the hypothesis that there exists a possible adaptive value at the species level to
> the altered behavior conferred on either the cockroach or the parasitic acanthocephalan.&nbsp; They maintain <br> that "if behavioral alterations result from physiological disruptions (neurological, hemolymph
> components, and so on) in one cockroach species, we would expect such alterations to be shared more <br> readily by close relatives than distant ones, regardless of the adaptive nature of those alterations in
> every association&quot; (Moore and Gotelli 1996).&nbsp; This corresponds with Poulin's (1995) criteria that <br> behaviors are more likely to be adaptations if they have arisen in several lineages independently.  
> <br> Robb and Reid (1996) were interested in determining whether or not the flour beetle's,
> Tribolium confusum, behavioral modifications were due to pathology caused by the parasite, <br> Hymenolepis diminuta, or if the parasite altered the intermediate host's behavior as an adaptive
> manipulation.&nbsp; Their findings indicated that both mated status and infection affected the survivorship of <br> the host, infected mated females surviving less than both infected virgin beetles and uninfected beetles. 
> Behavior, however, was only altered significantly by infection of the parasite and not by mated status.&nbsp; <br> They concluded that behavior did not appear to be a pathological response to the parasite but rather
> supported the hypothesis of&nbsp; the host's behavior being modified by the parasite.&nbsp; However, in Zuk's <br> (1988) experiment on parasitized crickets, the findings suggest pathological consequences to
> parasitism.&nbsp;&nbsp; Male parasitized crickets produced fewer spermatophores and had lower mating success <br> than uninfected males did.  This is one example of how sexual selection was affected in an insect host due
> to the pathological consequences of the parasite load.<br>
> Bumblebees, Bombus spp., on the other hand appear to have successfully mastered the use of <br> altered behavior for their own advantage.  Mueller and Schmid-Hempel (1993) reported that the
> parasitized worker bumblebees stayed in the field overnight instead of returning to the nest.&nbsp; These <br> workers spent significantly more time in cold areas than did nonparasitized workers.  The cold
> temperatures experienced by the bumblebees retarded parasitoid development and decreased the <br> parasitoid's survival chances.  The parasitized worker's colony benefited from the prolonged foraging in
> the cold night air, and the worker had a prolonged life span as a result of the reduced development rate <br> of the parasitoid.  Poulin (1992) argues that these changes in behaviors of parasitized bumblebee
> workers are likely to be an adaptive response of the host resulting in greater inclusive fitness.&nbsp; He <br> notes that this may be one of the few examples of Smith Trail's (1980) kin selected-host suicide
> hypothesis in practice in nature.<br>
> In certain instances, however, where it has been shown that a parasitized animal could benefit <br> from behavioral modifications, there may be no adaptation.  For example, in nematode-parasitized
> Drosophila high temperatures had deleterious effects on the parasites.&nbsp; But when given a choice of <br> temperature in a thermal gradient, neither species of D. falleni nor D. neotestacea modified their
> behavior in favor of the higher temperature (behavioral fever) (Ballabeni et al. 1995).&nbsp; <br>
> Modified behavior induced by endotoxins<br>
> A host would benefit if, by altering its behavior, it could effectively harm the parasite.&nbsp; Many <br> ectotherms respond to a parasite by changing their microhabitat in such a way as to elevate their own
> body temperature (Horton and Moore 1993).&nbsp;&nbsp; By doing so the animal exhibits behavioral fever.&nbsp; <br> Recent literature on insects infected with endotoxins indicates that the host insect is able to use
> behavioral fever to its advantage against microsporidian protozoan, intracellular prokaryotes, <br> bacterial endotoxins or prostaglandins, and fungus.  The  adaptive value of behavioral fever to pathogens
> can be expressed in three ways:&nbsp; fever may be an adaptation of the host as a defense against the pathogen, <br> a modification of the host by the pathogen to enhance growth, dispersal, and survival of the pathogen, or
> merely a side effect of infection and benefiting neither host not pathogen (Boorstein and Ewald 1987). <br>
> Boorstein and Ewald (1987) inoculated grasshoppers Melanoplus sanguinipes with the <br> microsporidian protozoan Nosema acridophagus and showed that their preferred temperature increased. 
> By maintaining the grasshoppers at both febrile and nonfebrile temperatures they were able to show <br> that the febrile temperatures benefited the infected grasshoppers in survival and growth.  There is a
> cost to the fever, and febrile uninfected animals were negatively affected in growth.&nbsp; However, for an <br> infected animal these costs were outweighed by the benefits.  Infected insects maintained at nonfebrile
> temperatures had significantly lower fecundity, survival, and growth rates than controls.&nbsp; Fever was <br> beneficial to the infected animals in that they lacked significant differences from controls in fecundity,
> survival, and growth.<br>
> Crickets Gryllus bimaculatus exhibit&nbsp; behavioral fever in response to infection with <br> Rickettsiella grylli, a chlamydia-like pathogen (Louis 1986).   When allowed to regulate their own
> temperature in a thermal gradient, infected insects chose higher temperatures than noninfected insects <br> did.  This higher temperature caused the pathogen to degenerate.
> <br> Two different insects display behavioral fever to endotoxins, specifically purified
> lipopolysaccharides isolated from E. Coli.&nbsp; Lipopolysaccharides, components of the cell wall of Gram-<br> negative bacteria (Bronstein and Conner 1984), are potent pyrogens (McClain et al. 1988) that elicit
> a sequence of host-defense responses in animals.&nbsp; Bronstein and Conner (1984) conducted a study of <br> endotoxin-induced behavioral fever in the Madagascar cockroach Gromphadorhina portentosa. 
> Lipopolysaccharide-W was injected into the insect and the mean temperature preference was 3.6 <br> degrees higher than that for control cockroaches.  Also, the tenebrionid beetle Onymacris plana was
> observed by McClain et al. in 1988 to develop behavioral fever in response to lipopolysaccharide <br> injection and sought higher preferred temperatures in a gradient.  To be certain that the body
> temperature was indeed affected by the position of the beetle on the thermal gradient, thermocouples <br> were implanted in the thoracic musculature. 
> <br> A final example of behavioral fever is the modification in temperature preference induced in
> house flies Musca domestica when infected with the fungi Entomophthora muscae (Watson et al. 1992).&nbsp; <br> In experiments where flies were not given a choice of temperature, higher temperatures increased the
> survival period of the infected flies.&nbsp; In thermal gradients the flies preferred the higher temperatures, <br> exhibited behavioral fever, and were able to eliminate the pathogen using heat therapy.
> <br> With few exceptions, ectothermic animals, like endotherms will develop fevers in response to
> injections of endotoxins or other pyrogenic substances as a result of the animal &quot;feeling&quot; cold and <br> selecting a warmer microclimate (Kluger et al. 1996).  Kluger et al. suggests that febrile responses
> are most likely adaptive because if they weren't, than &quot;it would be unlikely that this energetically <br> expensive phenomenon would have persisted for millions of years in so many groups of animals".  With
> the exception of the bumblebee worker, most other insects are harmed by pathogens when their body <br> temperature is lowed and protected when they develop fevers (Kluger et al. 1996).  Kluger et al. also
> indicates that this observation and the fact that fevers are highly regulated, that they follow a <br> relatively common sequence of events within the body, both support the argument that fever has
> evolved as a host defense response.&nbsp; <br>
> Conclusion<br>
> Insects alter their behavior when they are under the stress of infection by parasites or <br> pathogens.  Such behavioral changes include seeking out warmer or cooler temperatures, changing their
> microhabitat, and acting more conspicuously.&nbsp; Many times the behavior will increase the probability <br> that the insect will be preyed upon.  This is often attributed as an adaptation of the parasite to alter its
> host's behavior in order to increase its transmission to a final host.&nbsp; It is also often the case that the <br> host insect will harm the parasite or pathogen by changing its behavior, such as increasing its body
> temperature, as seen in many of the insects infected with endotoxins.&nbsp;&nbsp; Seeking out warmer <br> environments in order to induce a physiological fever constitutes a behavioral fever and has been shown
> to effectively protect the insect from the pathogen.&nbsp; Whether some adaptations favor the parasite's <br> survival or the host's is still unclear in many of the parasite-host relationships.  Further studies are
> necessary, as Poulin (1995) suggests, in order to critically determine whether a behavior is adaptive.&nbsp; <br> It is important to determine the fitness costs of behavioral modification, the phylogeny of the behavior
> among close and distant relatives,&nbsp; and the pathological changes caused by the parasite and the effects <br> that those changes may have on host behavior.
> <br> References
> <br> Ballabeni, P., H. Benway, and J. Jaenike. 1995. Lack of Behavioral Fever in Nematode-Parasitized
> Drosophila. Journal of Parasitology 81(5): 670-674.<br>
> Boorstein, S.M., and P.W. Ewald.&nbsp; 1987. Costs and Benefits of Behavioral Fever Melanoplus sanguinipes <br> Infected By Nosema acridophagus. Physiological Zoology 60(5): 586-595.
> <br> Brodeur J., and J.N. McNeil. 1989. Seasonal Microhabitat Selection by an Endoparasite Through
> Adaptive Modification of Host Behavior. Science 244: 226-228.<br>
> Bronstein, S.M., and W.E. Conner. 1984. Endotoxin-Induced Behavioral Fever in Madagascar <br> Cockroach, Gromphadorhina portentosa. Journal of Insect Physiology 30(4): 327-330.
> <br> Carmichael, L.M., and J. Moore. 1991. A Comparison of Behavioral Alterations in the Brown Cockroach,
> Periplaneta brunnea, and the American Cockroach, Periplaneta americana, Infected With the <br> Acanthocephalan, Moniliformis moniliformis. Journal of Parasitology 77(6): 931-936.
> <br> Gotelli, N.J., and J. Moore. 1992. Altered Host Behavior in a Cockroach- Acanthocephalan Association. 
> Animal Behavior 43: 949-959.<br>
> Horton, D.R., and J. Moore. 1993. Behavioral Effects of Parasites and Pathogens in Insect Hosts. In: <br> Parasites and Pathogens of Insects (Ed. by N.E. Beckage, S.N. Thompson, and B.A. Federici), pp. 107-
> 124. San Diego: Academic Press.<br>
> Kluger, M.J., W. Kozak, C.A. Conn, L.R. Leon, and D. Soszynski. 1996. The Adaptive Value of Fever. <br> Infectious Disease Clinics of North America 10(1): 1-21.
> <br> Louis, C., M. Jourdan, and M. Cabanac. 1986. Behavioral Fever and Therapy in a Rickettsia-Infected
> Orthoptera. American Journal of Physiology 250: R991-R995. <br>
> McClain, E., P. Magnuson, and S.J. Warner. 1988. Behavioral Fever in a Namib Desert Tenebrionid <br> Beetle, Onymacris plana. Journal of Insect Physiology 34(4): 279-284.
> <br> Moore, J., M. Freehling, and N.J. Gotelli. 1994. Altered Behavior in Two Species of Blattid Cockroaches
> Infected With Moniliformis moniliformis (Acanthocephala). Journal of Parasitology 80(2): 220-223.<br>
> Moore, J. and N.J. Gotelli. 1990. A Phylogenetic Perspective on the Evolution of Altered Behaviors: a <br> Critical Look at the Manipulation Hypothesis. In: Parasitism and Host Behavior (Ed. by C.J. Barnes and
> J.M. Behnke), pp. 193-233. London: Taylor &amp; Francis.<br>
> Moore, J. and N.J. Gotelli. 1996. Evolutionary Patterns of Altered Behavior and Susceptibility in <br> Parasitized Hosts. Evolution 50(2): 807-819.
> <br> Mueller, C.B., and P. Schmid-Hempel. 1993. Exploitation of Cold Temperature as Defense Against
> Parasitoids in Bumblebees. Nature 363: 65-67.<br>
> Poulin, R. 1992. Altered Behavior in Parasitized Bumblebees: Parasite Manipulation or Adaptive <br> Suicide? Animal Behavior 44: 174-176.
> <br> Poulin, R. 1995. "Adaptive" Changes in the Behavior of Parasitized Animals: A Critical Review.
> International Journal of Parasitology 25(12): 1371-1383.<br>
> Robb, T., and M.L. Reid. 1996. Parasite-Induced Changes in the Behavior of Cestode-Infected Beetles: <br> Adaptation or Simple Pathology? Canadian Journal of Zoology 74: 1268-1274.
> <br> Smith Trail, D.R. 1980. Behavioral Interactions Between Parasites and Hosts: Host Suicide and the
> Evolution of Complex Life Cycles. The American Naturalist 116(1): 77-91.<br>
> Stamp, N.E. 1981. Behavior of Parasitized Aposematic Caterpillars: Advantageous to the Parasitoid or <br> the Host? The American Naturalist 118(5): 715-725.
> <br> Watson, D.W., B.A. Mullens, and J.J. Petersen. 1992. Behavioral Fever Response of Musca domestica
> (Diptera: Muscidae) to Infection by Entomophthora muscae (Zygomycetes: Entomophthorales). Journal <br> of Invertebrate Pathology 61: 10-16.
> <br> Zuk, M. 1988. Parasite Load, Body Size, and Age of Wild-Caught Male Field Crickets (Orthoptera:
> Gryllidae): Effects on Sexual Selection.&nbsp; Evolution 42(5): 969-976.<br>