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CHAPTER 9 Ecological consequences of manipulative parasites

K evin D . L afferty and A rmand M . Kuris

9. 1 Introduction studied manipulative infectious agents are trophically transmitted parasites in their prey inter- Parasitic “puppet masters”, with their twisted, self- mediate hosts. and parasitic castrators serving life history strategies and impressive evolu- can also manipulate host behavior, but for different tionary takeovers of host minds, capture the purposes and with different implications. Several imagination of listeners—even those that might not studies of manipulative parasites conclude with normally fi nd the topic of appealing phrases such as “may ultimately infl uence commu- (which includes most everyone). A favorite anecdote nity structure” ( Kiesecker and Blaustein 1999 ), yet concerns the trematode Leucochloridium paradoxum few demonstrate ecological effects. Here, we con- migrating to the eyestalks of its intermediate host sider the conditions under which manipulative par- snail and pulsating its colored body, presumably to asites might have a substantial ecological effect in attract the predatory birds that are the fi nal hosts for nature and highlight those for which evidence exists the worm. Identifying a parasite as “manipulative” (see also Chapter 10 ). infers that a change in host behavior or appearance Some changes in host behavior can result from is a direct consequence of the parasite’s adaptive pathological side effects that do not increase or can actions that, on average, will increase the fi tness of even decrease parasite fi tness, or can result from an the parasite. The list of parasites that manipulate adaptive response (e.g., a defensive response) by their hosts is long and growing. Holmes and Bethel the host to minimize the fi tness cost of the infec- ( 1972 ) presented the earliest comprehensive review tious agent (Poulin 1995 ). For instance, the females and brought the subject to mainstream ecologists. of some species of phorid fl ies oviposit an egg Over two decades ago, Andy Dobson (1988 ) listed behind the head of an . The fl y larva penetrates seven cestodes, seven trematodes, ten acanthocepha- the host cuticle and develops inside the head, soon lans, and three nematodes that manipulated host causing the ant to decapitate itself. The phorid con- behavior. Fifteen years later, Janice Moore (2002 ) tinues to feed on the tissues in the detached head, fi lled a book with examples. The fi ve infectious completes its development, pupates, and emerges trophic strategies, typical parasites (macroparasites), as an adult through an opening at the base of the pathogens, trophically transmitted parasites, para- head. The presence of phorids disrupts worker ant sitic castrators, and parasitoids (Kuris and Lafferty activities, and a colony under attack engages in a 2000 ; Lafferty and Kuris 2002 , 2009 ) can modify host frenzied, disoriented suite of behaviors, so much so behavior, but the likelihood that a parasite manipu- that colonies of fi re (Solenopsis spp.) fail to lates behavior differs among strategies. The most thrive in the presence of phorids ( Feener and Brown studied infectious agents, non-trophically transmit- 1995 ). Perhaps the best documented example of the ted pathogens and macroparasites, have enormous ecological effect of defensive behaviors against public health, veterinary, and wildlife disease impor- infectious agents comes from research on cleaner tance, yet few manipulate host behavior. The best-

158 OUP CORRECTED PROOF – FINAL, 05/14/12, SPi

ECOLOGICAL CONSEQUENCES OF MANIPULATIVE PARASITES 159 wrasses such as Labroides dimidiatus on coral reefs Several studies have measured the magnitude of (Grutter et al. 2003 ). Infested fi sh visit cleaners sev- manipulation by contrasting the behaviors or the eral times a day, and the diversity of fi shes decreases susceptibility to predation of infected and unin- on patch reefs after removing cleaner wrasses. fected hosts. A review of eight studies found that Many large predators and herbivores choose not to parasites of prey increased predation rates by a fac- visit patch reefs lacking cleaners. Hence, fi shes try tor of 1.62 to 7.5 ( Dobson 1988 ). These estimates are to reduce ectoparasite abundance and this alters the sensitive to sampling without replacement, sug- structure of fi sh communities among reefs. Hosts gesting such values might be underestimates can alter spatial patterns of foraging to avoid infec- ( Lafferty and Morris 1996 ). A trematode metacer- tion (e.g., leading to ungrazed “roughs” in pastures) caria that encysts on the brain of killifi sh has per- and increase the time spent grooming, as opposed haps the strongest effect documented in the to other activities, such as watching for predators literature. At average parasite intensities, infected ( Hart 1990 ). Such examples, though interesting in killifi sh are 30 times more likely to be eaten by birds, their own right, are not the subject of this review. a value much higher than the four-fold increase in the frequency of conspicuous behaviors observed in 9.2 What makes a manipulator important the aquarium ( Lafferty and Morris 1996 ). In other ecologically? words, a parasite-induced change in behavior can lead to an even greater change in transmission. Several factors can determine if a manipulative par- If manipulation is intensity-dependent (as it can asite will have ecological effects. (1) Changes to host be for typical parasites and trophically transmitted individuals should scale with the strength of manip- parasites), the behavior of the host depends on ulation. (2) A high incidence of infection will have a both the per-parasite manipulation and parasite greater effect on the host population. (3) Parasites intensity. In their mathematical models of mac- that infect common or otherwise important hosts roparasite manipulators, Dobson and Keymer are more able to leave a mark on ecological com- (1985 ) defi ned manipulation as α, a per-parasite munities. Unfortunately, we cannot yet evaluate multiplier of predation risk to fi nal hosts such that, how many parasites are manipulative or have for no manipulation α = 1, and, if a single parasite strong effects, use common hosts, or have high inci- doubles the risk of predation, α = 2. Intensity can dence. Further, assessments of the “importance” of make up for strength if manipulation is intensity the ecological role of potential hosts are available dependent. The per-parasite effect translates to for only a few communities. changes in behavior as a power function of inten- Strong manipulations should benefi t the parasite. sity (αIntensity ), meaning that parasites with small In mathematical models, the probability that a para- individual effects can, as a group, alter behavior if site can invade a host population increases with the they reach high intensities. For instance, a weak strength of manipulation (Dobson 1988 ). Strong manipulation of α = 1.0025 by a single trematode manipulation also has consequences for host popu- metacercaria can lead to a thirty-fold increase in lations. For models of a trophically transmitted predation risk for killifi sh because infected hosts parasite, manipulation decreases the equilibrium have a mean intensity of 1,400 metacercariae in the abundance of prey, whereas the abundance of pred- brain case ( Lafferty and Morris 1996 ). Intensity- ators increases with manipulation ( Lafferty 1992 ). dependent manipulation can also lead to a high This suggests that the ecological effects of manipu- prevalence of the parasite in the intermediate host lation will increase with the magnitude of the population because predators are not as likely to behavioral changes associated with parasitism. remove hosts with low intensity infections. Limited access to physiological systems that infl u- An indirect way to evaluate the strength of ence host behavior, energetic costs of manipulation, manipulation from fi eld data is to examine the and host counter-adaptations will constrain the shape of the frequency distribution of parasites in strength of manipulation. the host population. Although most typical para- OUP CORRECTED PROOF – FINAL, 05/14/12, SPi

160 HOST MANIPULATION BY PARASITES sites have an “aggregated” or negative binomial California and Baja California (Kuris et al. 2008 ). In distribution (Crofton 1971 ), the distribution of three case studies below, we explore what happens manipulative parasites in prey hosts appears less when common parasites strongly manipulate hosts aggregated because the tail end of the distribution with important roles in ecosystems. is truncated (e.g., Adjei et al. 1986 ; Shaw et al. 2010 ; Lafferty and Morris 1996 ; Crofton 1971 ; Joly and 9.3 Parasitic castrators and parasitoids Messier 2004 ), suggesting that manipulation deliv- as host behavior manipulators ers the most infected prey to predators. For aggre- gated distributions fi tted to a negative binomial Parasitic castrators and parasitoids can take over distribution, the lower the k -value, the greater the the identity of their hosts. Once the parasite pre- degree of aggregation, with k < 1 considered highly vents reproduction of the host (and this often hap- aggregated (Shaw et al. 1998 ). Compiling data from pens soon after infection), the genotype of the host Shaw et al. ( 1998 ), for 40 typical parasites and troph- no longer matters. If manipulation is weak or ically transmitted parasites in their predator hosts, absent, parasites can compete with the uninfected mean k = 0.41, whereas for 10 trophically transmit- host population ( Lafferty 1993 ). The intensity of this ted parasites in their prey intermediate hosts known competition depends on how similarly infected and or prone to behavior modifi cation, mean k = 1.30. uninfected hosts use resources. Manipulation can, Therefore, reduced aggregation appears to be a gen- therefore, reduce competition for castrators and eral feature of manipulative parasites. parasitoids. The ecological role played by manipulative par- If or castrator life histories differ from asites should increase with the frequency that those of their hosts, host behaviors can change after hosts become infected. For parasitoids, castrators, infection. Such changes can cause the host to occupy and predator hosts, parasite prevalence is a good a different niche where it might interact differently measure of abundant manipulation. However, for with its potential consumers, prey, and competitors. manipulated prey hosts infected with trophically For instance, immigration of castrated snails adds a transmitted parasites, intense manipulation new phenotype to a community. As an example, decreases prevalence because predators remove when infected with a heterophyid trematode, the hosts soon after infection ( Lafferty 1992 ). For snail, Batillaria cumingi, moves lower in the inter- example, larval acanthocephalans that cause ter- tidal habitat ( Miura et al. 2006 ). Submergence seems restrial isopods to leave shelter are rare in the fi eld adaptive for the parasite’s life history because het- because starlings eat infected isopods soon after erophyid cercariae shed from these snails seek to the behavioral change ( Moore 1984 ). Therefore, in penetrate fi shes. In another example, freshwater many cases, it can be challenging to determine snails (Physa acuta ) castrated by certain trematodes how abundant manipulation is just by looking at abandon their refuge under leaf litter and rise to the parasite prevalence. Incidence is a far better met- surface, perhaps improving the success of cercariae ric, but one that is harder to measure. shed by these snails but also increasing their risk of Indirect effects can result from a manipulative predation by birds (Bernot 2003 ). In both cases, parasite if the host plays an important role in the abundant infected snails occupy a new ecological ecosystem. Some hosts are too rare or do not have a niche. disproportionate effect on the ecosystem. Other Parasitic castrators can alter host-feeding rates hosts do not interact much with other potential with potential indirect effects on lower trophic lev- predators or competitors. However, abundant or els. On rocky shores along the east coast of North interactive hosts can play important roles in ecosys- America, the most common intertidal snail, Littorina tems. For example, the effect of the strong manipu- littorea, has important impacts on algal communi- lator, Euhaplorchis californiensis, is magnifi ed in ties and can be frequently parasitized by larval importance because its killifi sh host is often the trematodes. Infected snails graze less, increasing most common fi sh in the estuarine systems of colonization by ephemeral algae in areas where the OUP CORRECTED PROOF – FINAL, 05/14/12, SPi

ECOLOGICAL CONSEQUENCES OF MANIPULATIVE PARASITES 161 parasite is more prevalent (Wood et al. 2007 ). In track tagged fi sh, monitoring their diet and growth contrast, Physa acuta infected with Posthodiplostomum rate. Charr, like most stream-dwelling salmonids, minimum graze more than do uninfected snails, feed on aquatic invertebrates as well as terrestrial reducing periphyton biomass by 20% when the insects that fall into the stream from the surround- prevalence of infected snails exceeds 50% ( Bernot ing forest ( Kawaguchi et al. 2003 ). This diet changes and Lamberti 2008 ). This intensifi ed grazing also in the late summer and fall when fi sh start consum- alters the species composition of the periphyton ing terrestrial camel crickets (Tachycines spp.). community. These opposite effects of castrators on Takuya Sato noticed that several of the crickets grazing rates illustrate how the ecological conse- eaten by trout had once hosted nematomorph quences of manipulation can vary among worms, Gordionus chinensis, in their abdomens (Sato parasites. et al. 2008 ). Nematomorphs are parasitoids with a complex life cycle. Non-feeding nematomorph adults live in 9.3.1 Nematomorphs, endangered charr, streams and produce larval worms that infect and crickets in Japanese streams aquatic insects such as mayfl ies. Mayfl ies leave the Japanese fi sheries biologists are making a dedicated stream and metamorphose into short-lived adults. effort to protect the Kirikuchi charr (a trout), However, the larval nematomorphs stay alive inside Salvelinus leucomaenis japonicas ( Fig. 9.1 ). Threatened the mayfl y carcasses that fall to the forest fl oor, by over-fi shing and habitat destruction, the charr infecting crickets that scavenge the infected car- occurs in a few remaining watersheds (Sato 2007 ). casses. As it matures in the cricket, a growing To understand how to save the charr, biologists nematomorph consumes almost all non-essential

Figure 9.1 Hypothesized effects of a nematomorph worm on a Japanese stream ecosystem. In the left panel, the parasite is absent and charr forage on a sparse prey base of benthic . In the right panel, adult nematomorph worms mate in the stream. Their larvae infect larval insects and leave the stream as the insects mature and disperse into the forest. Crickets scavenging on dead insects ingest the larvae, and become the second host. As the worm matures in the cricket, it drives its host from the forest into the stream, attracting predation by charr. Such crickets provide 60% of the charr’s energetic intake. Satiated by crickets, the charr eat fewer benthic insects, resulting in a higher production of adult insects that leave the stream for the forest. Artwork K. D. Lafferty. See also Plate 14. OUP CORRECTED PROOF – FINAL, 05/14/12, SPi

162 HOST MANIPULATION BY PARASITES fats and reproductive organs. Then comes a consid- and become predators and prey for terrestrial ani- erable challenge. Nematomorphs are aquatic as mals ( Sato et al. 2011a ). adults, yet crickets are terrestrial. A dramatic behav- ioral manipulation solves this problem; the worm 9.4 Trophically transmitted parasites causes the cricket to seek water (Thomas et al. 2002 ) as host behavior manipulators (see also Chapter 2 ). Infected crickets jump into the stream, and the mature nematomorph worm Trophic transmission is a common life history strat- explodes through the anus of the cricket. The para- egy for parasites and seems to select for manipula- sitoid leaves its dying host twitching on the surface tion. For most parasites, a common cause of death and swims away to fi nd a mate. Charr attack insects is probably predation of the host ( Johnson et al. falling into the stream and many consume the worm 2010 ). However, some parasites have adaptations along with the cricket ( Sato et al. 2008 ). This must to survive predation and use the predator as the have been a long-standing obstacle in the evolution next host in the life cycle. At worst, parasitizing a of nematomorphs because the worms escape from predator makes the best of a bad situation. However, the cricket’s predators by squirming out through if the predator is large and long-lived, the parasite their gills, mouth, or anus ( Ponton et al. 2006 ). can extend its lifespan and have increased access to Realizing that nematomorphs were driving crick- food (Lafferty 1999 ). Alternatively, parasites of ets into streams, Sato et al. ( 2011a ) measured the predatory hosts might fi nd it advantageous to add contribution of manipulated crickets to the annual prey hosts to their life cycle (Choisy et al. 2003 ). energy budget of the charr population. They Prey are more abundant than their predators and pumped charr stomachs, divided the prey into sev- are therefore more likely to contact a free-living eral categories, and estimated the caloric content of infectious stage of the parasite. The predator host the prey every month. The researchers set out baited then unintentionally contacts the parasite as it traps in the forest for crickets and also measured the hunts for prey. For either evolutionary pathway, a rate that insects fell into the stream. Crickets were trophically transmitted parasite will benefi t from common year round in the forest; however, infec- increasing predation rates on infected prey so long tions with nematomorphs occurred in the summer as the parasite delays manipulation until its matu- and fall. Infected crickets were 20 times more likely ration and can focus increased predation on suita- to fall into streams than were uninfected crickets, ble predatory hosts. Next, we provide two examples confi rming that the worm altered cricket behavior, of how manipulation by trophically transmitted and explaining the seasonal pulse of food for charr. parasites might have ecological effects. Sato et al. ( 2011a ) found that crickets delivered to the stream by nematomorphs contributed an amaz- 9.4.1 Tapeworms, wolves, moose, and forests ing 60% of the charr’s annual calories. This endan- on Isle Royale gered fi sh might even depend on the nematomorph for its long-term persistence in Japan. Unfortunately Moose (Alces alces) probably fi rst crossed the 30 kil- for charr, the nematomorph is less prevalent in the ometers to Isle Royale, in Lake Superior from the conifer plantations that are increasingly replacing mainland around 1900, increasing in number due to native forest ( Sato et al. 2011b ). There are other an abundance of food and absence of wolves (Canis potential indirect effects of the nematomorph ( Sato lupus ) ( Fig. 9.2 ). Population explosions led to peri- et al. 2011a ). The nematomorph moves a substantial ods of over-grazing and mass starvation. In 1949, amount of energy from the forest to the stream. In wolves colonized the island over a rare ice bridge return, satiated by crickets, charr consume fewer and began to reduce the number of moose. Since aquatic insects. This shifts energy from the stream 1958, ecologists such as David Mech and Rolf back to the forest because many surviving aquatic Peterson have studied this 540 square-kilometer insects, such as mayfl ies and damselfl ies, metamor- outdoor laboratory (see the comprehensive book by phose into fl ying adults that move back to the forest Peterson 1995 ). They have found that many outside OUP CORRECTED PROOF – FINAL, 05/14/12, SPi

ECOLOGICAL CONSEQUENCES OF MANIPULATIVE PARASITES 163

Figure 9.2 Hypothesized effects of a tapeworm on the Isle of Royale ecosystem. In the left panel, the parasite is absent, and wolves have a hard time persisting on moose. Moose, unchecked by predators, over-graze the forest. Right panel, the adult worms of Echinococcus granulosus live in the intestines of wolves where they cause little pathology. Tapeworm eggs contaminate the soil and are incidentally ingested by moose. Larval tapeworms form hydatid cysts in the lungs of moose. Wolves can more easily prey on infected moose, reducing the abundance of the moose population and allowing re-vegetation of the island. Artwork K. D. Lafferty. See also Plate 15.

forces affect the success of wolves and moose. For E. granulosus in wolves ranges from 14–72% instance, an increase in moose density followed an ( Rausch 1995 ). epidemic of canine parvovirus that almost extir- The debilitating effects of hydatid cysts likely make pated wolves in the 1990s. The moose over-grazed it easier for wolves to kill moose. Evidence for this is the forests and again began to starve. In poor condi- indirect. Hunters shoot more infected moose earlier in tion, the moose suffered from an outbreak of ticks, the hunting season ( Rau and Caron 1979 ), and heavily and extreme cold weakened their health even more. infected moose are less common than expected ( Joly At the same time, the wolf population began to and Messier 2004 ), suggesting hunters or predators rebound. This back and forth pattern results in cycles remove infected individuals from herds. of wolves tracking the abundance of moose, offset How might manipulation by this tapeworm alter by about a decade. the Isle Royale ecosystem? Simple mathematical On Isle Royale, the tapeworm, Echinococcus models hypothesize that there could be situations granulosus, uses moose as the intermediate host where wolves could not persist on moose as prey and wolves as the fi nal host. Moose ingest tape- without the assistance of the debilitating parasite worm eggs from soil and water contaminated ( Hadeler and Freedman 1989 ). More recent models with wolf feces. Larval tapeworms form large, have suggested that manipulative parasites do not debilitating hydatid cysts in the lungs, braincase, affect the invasion criteria for a predator popula- liver, and other organs of the intermediate host. tion. This is because at the moment of fi rst contact Wolves acquire the tapeworms when they eat an between a predator and prey population, the prey infected moose. In the wolf, the small adult tape- population is uninfected and unmanipulated worms live in the intestine and cause no measur- ( Fenton and Rands 2006 ). In other words, for wolves able harm. Throughout its range, prevalence of to benefi t from infected moose, the wolves must OUP CORRECTED PROOF – FINAL, 05/14/12, SPi

164 HOST MANIPULATION BY PARASITES

fi rst bring the parasite with them and establish the sities of thousands per square meter, supporting a life cycle. On Isle Royale, the initial pack of wolves recreational and commercial harvest ( Hartill et al. encountered an uninfected moose population and 2005 ). As the most abundant component of the bio- wolves established without the initial help of the mass on these fl ats, cockles are also a common parasite. However, it is probable that the presence resource for birds, fi shes, and ( Thompson of the tapeworm enables wolves to drive the moose et al. 2005 ). population to lower levels than would be possible Cockle shells can protrude from the sediment, without the tapeworm in the system. Consequently, creating a habitat for several epibionts, including an the tapeworm might indirectly favor forests on Isle anemone (Anthopleura aureoradiata), chitons, the Royale. A further theoretical effect of a parasite that estuarine Elminius modestus , tubicolous increases susceptibility to predation is an increase amphipods, and serpulid worms ( Thomas et al. in oscillations between predator and prey ( Fenton 1998 ). Exposed shells also are substrates for algae and Rands 2006 ), suggesting that the tapeworm that support a small limpet, Notoacmea helmsi . In the could infl uence the period and amplitude of the bays of New Zealand, there are few alternative nat- moose–wolf cycle seen on Isle Royale. ural substrates for this rich and distinctive epibiont community, and the provision of novel habitat makes A. stutchburyi an “ecosystem engineer” 9.4.2 Trematodes, cockles, limpets, and ( Thomas et al. 1998 ). anemones in New Zealand mudfl ats Pied oystercatchers (Haematopus ostralegus fi n- On the mudfl ats of New Zealand, the most notice- schi) foraging on the mudfl ats carry adult trema- able inhabitant is the “cockle”, Austrovenus stutch- tode worms in their intestines. For many buryi ( Stewart and Creese 2002 ) ( Fig. 9.3 ). This little trematode species in New Zealand mudfl ats, the neck clam reaches 6 cm in width and can attain den- fi rst intermediate host snails are either

Figure 9.3 Hypothesized effects of a trematode on a New Zealand mudfl at ecosystem. In the left panel, cockles burrow into the sediment with only their siphons protruding. In the right panel, adult trematodes live in the intestine of shorebirds. Birds defecate trematode eggs onto the mudfl at where they infect an estuarine snail as the fi rst intermediate host. Trematode cercariae emerge from the snail and then seek out a cockle as a second intermediate host, forming a cyst in the foot. Infected cockles have impaired digging abilities, making them easier prey for birds. Raised above the mud surface, the cockles provide hard substrate for a community of invertebrates and algae. Artwork K. D. Lafferty. See also Plate 16. OUP CORRECTED PROOF – FINAL, 05/14/12, SPi

ECOLOGICAL CONSEQUENCES OF MANIPULATIVE PARASITES 165

Zeacumantus subcarinatus or Cominella glandi- the prey hosts. In prey hosts, all are either neuro- formis. Trematode cercariae emerge from the tropic (e.g., T. gondii , B. procyonis), or infect the infected snail and then encyst in a second inter- lungs, diaphragm, or other key organs needed for mediate host (which varies among trematode stamina (e.g., Echinococcus spp. T. solium , Trichinella species), and the life cycle is completed when an spp.). Their ability to modify host behavior, either oystercatcher eats an infected second intermedi- through involvement with brain chemistry or mus- ate host. Two trematode genera (Curtuteria and cle physiology, probably makes hosts less wary or Acanthoparyphium) with six cryptic species use more risk tolerant, or impairs escape responses (see the cockle as a second intermediate host, encyst- Chapter 3 ). A combination of negligible host specifi - ing in the tip of the foot (Babirat et al. 2004 ). city and increased susceptibility to predators ena- Key to the understanding of this system was the bles these parasites to be widespread. For instance, discovery that the trematodes, by encysting in the T. gondii infects any warm-blooded vertebrate (ter- foot, reduce the burrowing ability of the cockles, restrial or aquatic) as an intermediate host on every thereby stranding them on the surface where they continent (Tenter et al. 2000 ). Infections with T. gon- become easy prey for oystercatchers ( Thomas and dii can be prevalent, sometimes with substantial Poulin 1998 ). The trematodes, therefore, are the pathology (Dubey and Beattie 1988 ). Such a com- mechanism by which the cockles increase the avail- mon and sizeable manipulation suggests T. gondii able substrate for epibionts to colonize. In addition, has the potential for large-scale ecological effects. by digging less, infected cockles modify properties Similarly, Baylisascaris procyonis infects more than of the sediment, which alters infaunal communities 100 species of potential prey for raccoons and is (Mouritsen and Poulin 2005 ). Two types of evidence common in North America and Europe (Kazacos show a clear cause-effect relationship between the 2001 ). Echinococcus multilocularis occurs throughout trematode and changes to the ecosystem. arctic ecosystems (Rausch 1995 ) and Trichinella spp. Experimentally increasing or decreasing the number infections build through the food chain via car- of stranded cockles alters the mudfl at community nivory and carrion feeding (Pozio et al. 1992 ). These ( Mouritsen and Poulin 2005 ). Also, by comparing parasites meet the criteria for having strong ecologi- 17 sheltered bays around Otago Harbour, Mouritsen cal effects. and Poulin ( 2010 ) showed that spatial variation in trematode infections was associated with corre- 9.6 Testing for the ecological effects sponding variation in the intertidal community. It of manipulative parasites appears that New Zealand mudfl ats would have less biodiversity without these manipulative A research program on the ecological effects of parasites. manipulative parasites will require collaboration between ecologists and parasitologists. Ecologists 9.5 The ecological reach of host behavior identify free-living species that play important roles manipulators in ecosystems. Parasitologists can then search these important hosts for parasites that are abundant and Where might we fi nd other cases where manipula- have the ability to manipulate host behavior. tive parasites have ecological effects? Some wide- Together, ecologists and parasitologists could con- spread infectious wildlife diseases with major duct studies that link behavioral changes to ecologi- human public health concerns can manipulate the cal effects. behavior of their prey hosts. The most notable of The hypothesized ecological role of Echinococcus these are Toxoplasma gondii and other two-host coc- granulosus indicates the importance of working in cidians, taeniid tapeworms such as Taenia solium , T. systems like Isle Royale where indirect effects cas- multiceps , and Echinococcus spp., the raccoon round- cade through the food web. The prediction that the worm, Baylisascaris procyonis, and Trichinella species. tapeworm could indirectly affect forest growth These parasites often have low host specifi city for comes from substantial observational work on the OUP CORRECTED PROOF – FINAL, 05/14/12, SPi

166 HOST MANIPULATION BY PARASITES prevalence of the tapeworm in moose and wolves, species potentially connected to the stranding of the potential effect of the parasite on moose, the parasitized cockles on the mudfl at surfaces. These effect of moose on vegetation, and the effect of efforts have resulted in this system being the most wolves on moose. This system is simple enough to cited example of how parasites can affect explore with mathematical models, which can ecosystems. reveal additional predictions (e.g., about increased The Japanese nematomorph study indicates how cycling). Carnivore reintroduction programs manip- non-parasitologists can reveal effects of parasites. ulate the presence of wolves and parasites and Through careful and repeated quantifi cation of might lend insight into the effect of E. ganulosus at charr stomach contents, anomalies were discovered other locations. Wolves and other large carnivores that pointed to the role of the nematomorphs. These have been extirpated from large areas of their biologists were focused on the fl ow of energy among former ranges and are sometimes reintroduced ecosystems, and were thus able to discover the dra- (such as into Yellowstone National Park in 1995). matic contribution of parasitized crickets to the diet Before initiating such programs, it should be possi- of endangered charr. ble to determine if parasites such as E. granulosus are circulating in the ecosystem. Because hydatid 9.7 Conclusions disease has severe human health consequences, vet- erinarians involved in relocations treat wolves at Numerous studies have shown that the direct effects least twice with antihelminth drugs to eliminate of parasitism signifi cantly affect populations, com- tapeworms. Reintroductions, therefore, are an munity structure, and ecosystem energetics (e.g., opportunity to observe wolf–prey dynamics with- Hudson et al. 1998 ; Waldie et al. 2011 ; Lafferty et al. out E. granulosus . Specifi cally, comparing dynamics 2006; Kuris et al. 2008 ; Hechinger et al. 2011 ). In in worm-free areas with source areas where the addition, manipulative parasites are more than just worm occurs could indicate how this tapeworm entertaining cocktail party anecdotes. They can affects forest ecosystems. Other species might be exert effects across hierarchical ecological levels. more tractable for studying the ecological effects of Those that have strong manipulative effects on their manipulative tapeworms. E. multilocularis , for hosts can alter aspects of the distribution and abun- instance, uses smaller carnivores like foxes and coy- dance of their host populations. If parasitism is otes as fi nal hosts and rodents as intermediate hosts. common, effects on the host population can be One could explore how the presence or absence of strong. If the host is common or interacts with other this tapeworm across island habitats affects species in the system, indirect effects on the food predator–prey dynamics. web could occur through the alteration of trophic Research on the New Zealand cockle required a cascades, creation of new habitats, or new niches, or variety of approaches. Observations of stranded, by altering the fl ow of energy among habitats. It fouled cockles combined with parasitological will be a while before we have a systematic under- investigations led to the hypothesis that the para- standing of the importance of manipulative para- site manipulated the cockle in a way that altered sites at the ecosystem level. Further insight into the the ecosystem. Researchers also studied across effects of manipulative parasites will require chal- many sites, permitting an understanding of how lenging experiments and observations, ideally with variation in parasitism drove changes to the eco- strong collaboration among parasitologists and system. This system was amenable to experimenta- ecologists. tion because the behavioral manipulation could be mimicked in the laboratory and fi eld, as could par- Acknowledgements asitization rates (by manipulating snail densities). Finally, by creating a food web for the system We thank R. Hechinger, K. Miles, R. Poulin, T. Sato, ( Thompson et al. 2005 ), researchers had a model for J. Shaw, S. Sokolow, K. Weinersmith, and S. Weinstein various direct and indirect relationships among for valuable discussion of these ideas. OUP CORRECTED PROOF – FINAL, 05/14/12, SPi

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