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Is a Health Ecosystem One That is Rich in Parasites

Is a Health Ecosystem One That is Rich in Parasites

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Published by: Renz L. Salumbre on Mar 18, 2011
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Is a healthy ecosystem one that isrich in parasites?
Peter J. Hudson
, Andrew P. Dobson
and Kevin D. Lafferty
Center for Infectious Disease Dynamics, Penn State University, University Park, PA 16802, USA
Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544-1013, USA
Western Ecological Research Center, US Geological Survey, Marine Science Institute, University of California, Santa Barbara,CA 93106, USA
Historically, the role of parasites in ecosystem function-ing has been considered trivial because a cursoryexamination reveals that their relative biomass is lowcompared with that of other trophic groups. Howeverthere is increasing evidence that parasite-mediatedeffects could be significant: they shape host populationdynamics, alter interspecific competition, influenceenergy flow and appear to be important drivers ofbiodiversity. Indeed they influence a range of ecosystemfunctions and have a major effect on the structure ofsome food webs. Here, we consider the bottom-up andtop-down processes of how parasitism influencesecosystem functioning and show that there is evidencethat parasites are important for biodiversity andproduction; thus, we consider a healthy system to beone that is rich in parasite species.Introduction
In a classic paper 40 years ago, Robert Paine found thatwhen he removed the predatory starfish
Pisaster ochra-ceus
from the rocks at Mukkaw Bay, Washington,
mussels expanded their range downward,dramatically outcompeting many other sessile species forspace[1]. This elegant experiment set the scene forexamining how predators could shape communitystructure. Twenty years later, in the first issue of 
[2], two of us explored how parasites differed frompredators and examined how they shaped communitystructure as a result of their intimate association withtheir host. At that time, experimental data on host–pathogen interactions in the wild were limited, althoughreconstruction of data on rinderpest showed how theinvasion of a pathogen could have repercussions through-out the whole community. When rinderpest invaded thewild ungulate community of the Serengeti in 1892, itreduced the abundance of several species and this alteredinterspecific competition, modified vegetation structureand changed fire regimes.Researchnowrangesfromdetailedlong-termstudiesof specific host–parasite systems through to attempts toquantify the diversity and biomass of parasite species infood webs. In many respects, it is not surprising how thisfield has taken off because, just as our article[2]waspublished, Cathy Toft wrote an important paper[3]showing that half of all biodiversity might compriseparasitic species. More recently, two texts published thatexamine aspects of how parasitism can shape community,and ecosystem, ecology[4,5]. The accumulating evidenceindicates that, as parasite species diversity increases,ecosystem functioning improves. At first, this seemscounterintuitive, given that parasites reduce host fitnessand can threaten endangered species; alternatively,parasites can also be beneficial in the promotion of biodiversity. Here, we explore the role of parasites incommunities and ecosystem functioning and address thequestion ‘Is a healthy ecosystem one that is rich inparasites?’ This begs the additional question ‘What is ahealthy ecosystem?’ and this we address inBox 1. Wefollow the criteria laid down by Costanza and Mageau[6]that a healthy ecosystem is one that persists, maintainsvigor, organization and resilience to change. We provideevidence to show that many of these features arise fromboth the bottom-up and top-down processes that aremediated by parasites. We argue that the past 20 yearshaveseenalargeincreaseinourunderstandingoftherolethat parasites have in community organization. Wesuspect that the next 20 years will see a sharpappreciation of the role they have in ecosystem processes.
Parasite processes and community consequences
There is now substantial evidence that parasites signi-ficantly reduce host fitness in the wild, interact with otherpopulation processes and shape community structure[7].Intheoriginalarticle[2],wediscussedthedynamicsofredgrouse
Lagopus lagopus scoticus
in relation to theirinfections with a gastrointestinal nematode and a vector-borne flavivirus that causes Louping ill. More detailedstudies have since revealed how the parasites areembedded in a larger food web and how food quality,predationandcompetition[8]interactwiththebehaviorof the birds[9]to generate a Pandora’s Box of nonlineardynamics that reflect the large variation in cycle periodandamplitudeobservedinthenaturaltimeseries[10].Wenow appreciate that, by starting from a simple under-standing of interactions at the parasite–host and vector–host level, we can build up to an understanding of thebroad-scale influences of parasites on community
Corresponding author:
Hudson, P.J. (pjh18@psu.edu).Available online 18 May 2006
TRENDS in Ecology and Evolution 
Vol.21 No.7 July 2006
www.sciencedirect.com0169-5347/$ - see front matter Published by Elsevier Ltd. doi:10.1016/j.tree.2006.04.007
dynamics. At regional spatial scales, we also nowappreciate how climatic conditions can synchronize thetransmission of parasites across populations and that thisprocess can bring populations into synchrony[11]. In thisrespect, the parasites not only provide organization andvigor in that they influence interspecific interactions,but also act to destabilize the dynamics so that whenclimatic conditions bring populations into synchrony,this destabilization can result in widespread outbreaksof disease, leading to increased extinction risk andreduced resilience.Studies are now beginning to illustrate how parasite-mediated effects that act on individuals can also influencecommunitystructure andworkings. Forexample,detailedstudies of trematodes that infect the foot tissue of the
Austrovenus stutchburyi
cockle have shown that theparasites interfere with how the cockle uses its foot tomove and burrow after it has been dislodged[12].Experimental field studies show that these parasiteshave an indirect effect on the sediment disturbance,profoundly influencing the structure and functioning of the soft-bodied animal communities. This is becauseepifaunal organisms benefit from the increased surfacestructure, and the infauna are influenced by changes inthe hydrodynamics that determine the particle compo-sition in the upper sediment[13]. Interestingly, theseconsequences for community structure and function are aresultoftrait-mediatedindirecteffectsofparasitism.Sucheffects can have a profound influence on ecosystemfunctioningbecausetheparasitesaltertheratesoftrophicenergy ow and, simultaneously, parasitetransmission[14].Further evidence of the importance of parasites inshaping community structure comes from studies of invasive species, where two significant papers[15,16]have shown that invaders escape from their parasites intheirnativerange(reviewed in[17]).Releasefromnaturalenemies could subsequently aid the performance of aninvader. For example, detailed studies of the invasivegreen crab
Carcinus maenas
show that, when it invades anew habitat, it leaves behind part of its parasitecommunity, grows larger and becomes more abundant[18]. In the case of invasive plants in the USA, there is anegative correlation between pathogen diversity and thenumber of States recording the plant as an invasive pest,suggesting that invasive species become pests when theirparasites are absent[16]. In a sense, parasites are toinvaders as kryptonite is to Superman: the advantagegained by their absence helps reveal the magnitude of their handicapping influence.
Generalist parasites, apparent competition andextinction
Generalist parasites that infect diverse host species canalso have important and dramatic effects on communitystructure because parasite transmission between speciesand parasite-induced effects are invariably asymmetrical.Given that host species differ in their susceptibility andtolerance to parasites, one species might add moreinfective stages of the parasite to the shared pool of infective stages than does the other. Sensitive species aremore likely to succumb to the pathogens that aremaintained in abundance by tolerant species and thisleads, ultimately, to local host extinction. Thus, apparentcompetition can act through parasitism when levels of infection depend primarily on the rate at which theparasites flow from a tolerant species to a sensitivespecies,ratherthanonthedensityofthesensitivespecies.Detailed studies of the shared parasite
Heterakis galli-narum
in pheasants and partridges show that the fitnessof a single infective stage entering a pheasant is 100 timesgreater than a similar stage entering a partridge[19]because the parasite is more likely to establish, growbigger and produce more infective stages in pheasants.Given that the partridges suffer reduced fitness fromparasites, the presence of pheasants could increaseinfection in partridges and lead indirectly to theirlocalized extirpation[19].Parasite-induced competitive exclusion can occur whena rare spill-over event results in a serious epidemic. Forexample, an itinerant dog wandering into the home rangeof Ethiopian wolves
Canis simensis
in 2003 resulted in anoutbreak of rabies that killed 38 wolves,
10% of theglobal population[20]. Although extinction from parasit-ism alone appears rare, it is still a matter of concern,because parasitism can reduce numbers in a population toa size where there is an increased extinction risk from allthe stochastic processes that affect small populations[21].
Box 1. What is a healthy ecosystem?
Health is a vague term that often conjures up images of ‘humanhealth’, where we think of the disease-free status of the individual, apristine condition without illness and with good prospects of continued survival. By contrast, the term ‘ecosystem health’ isfocused on the functioning of a whole community; therefore theterm must embrace the overall performance and persistence of thesystem. Thus, a healthy ecosystem is one that persists, maintainsvigor (productivity), organization (biodiversity and predictability)and resilience (time to recovery)[6].We often think of pristine ecosystems, such as the Serengeti, asbeing healthy because the species composition has persisted for atleast 1000 years and, if perturbed, would no doubt lead to the loss of several charismatic species. Yet, if we examine the herbivores (e.g.wildebeest and zebra) or the carnivores (e.g. lions and hyenas), wewould find that these animals harbor high levels of parasiteprevalence and species richness, with most hosts infected withgastrointestinal nematodes, ticks and bacteria. Not only are thehosts heavily infected, but the parasites also link the differenttrophiclevels (e.g. herbivore–carnivore) given that the tapeworm larvaeinhabiting the muscles of the herbivores develop into adults incarnivores. These long chains of multispecies connections canstabilize the community structure in ways that increase resilienceand that might help persistence[48]. Counting the parasitic speciespresent can also double the species richness of the ecosystem[49].The abiding image of a healthy ecosystem is therefore one inwhich the biodiversity of free-living organisms is shadowed by theparasites, where each host is a habitat patch to be colonized andexploited.Thiscontrastswithrecentlydisturbedorinvadedsystems,where parasitic diversity is often reduced. For example, whenmolluscs invade and replace native snails in coastal marshes, theydisrupt the life cycle of many digenean trematodes, removing thehosts that are essential for the completion of a complex life cycle[50]. The absence of trematodes might lead to competition amongprey species released from parasitism and be detrimental topiscivorous birds, as parasite-free fish might be harder to catch[51,52].
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In reality, there are few documented cases of extinction byparasitism; for example, a microsporidian was found tohave eliminated the last captive population of the landsnail
Partula turgida
[22]even though the host had beenwiped out in the wild as a consequence of the introductionof alien species. There is also evidence for the role of theintroduced avian malaria in the disappearance of severalspecies of Hawaiian birds but once again this has beenexacerbated by the rooting behavior of feral pigs, whichproduces suitable breeding habitat for the mosquitoes[23].Furthermore,morethan100speciesoffroghavegoneextinct in the past ten years probably as a result of theinteraction between climate change, anthropogenicfactors and a chytrid fungal pathogen[24]; this givescause for concern about how these factors might interactand influence the future of other species. In most caseswhere parasitesarethought tohave hada rolein aspeciesdecline, the pathogen has spilled over from one hostspecies into another species where there is little coevolu-tionary history, the wild animal equivalent of an emerginghuman disease. Such effects are not going to benefitecosystem functioning but it is interesting to consider theduality of parasites in the ecosystem and the tension thatthespecialistspecieshaveinincreasingandthegeneralistparasites have in reducing community organization.
Specialist parasites and biodiversity
Density-dependent transmission and host specificity cangenerate a causal link between parasitism and biodiver-sity. In the last section, we discussed the evidence thatgeneralist parasites can reduce biodiversity through theprocess of apparent competition, but specialist parasitescan act to increase biodiversity. The Janzen–Connellhypothesis[25,26]proposes that high biodiversity inrainforests occurs because strong levels of local fre-quency-dependent predation reduce the probability thatplants of the same species will establish in the vicinity of aparent tree[27]. Although both Janzen and Connellindividually proposed seed predators as the mechanismdriving this effect, anincreasing bodyof evidence suggeststhat specialized fungal pathogens produce a strongJanzen–Connell effect not only in tropical[28], but alsoin temperate forests[29]as well as other habitats[30]. This effect is analogous to the Red Queen Hypothesis,because parasites maintain species diversity within aguild similar to how parasites can select for geneticdiversity within a population[31]. Thus, the growingevidence suggests that parasites have a major impact onecosystem health through their impact on drivingbiodiversity and ecosystem organization.Detailed studies by David Tilman and colleagues atCedar Creek, USA have illustrated how reduced biodi-versity can lead to reduced productivity[32]. Host-specificpathogens, such as some rust species, impact theproductivity of grasslands by damaging photosyntheticability and root production[33]. When species biodiversityfalls but total plant abundance is held constant, specialistpathogens have a bigger effect because the higher hostdensity of remaining species increases the transmission of the specialized rust between individuals[34]. In the wild,this effect would increase biodiversity by limiting theabundance of the most common species. Interestingly, therust affects major ecosystem functioning and could helpexplain the findings of Tilman
et al.
[32]that lowbiodiversity reduces primary productivity. This evidenceleads us to suppose that parasites have an important rolein influencing ecosystem vigor, although the crucial nextstep would be to partition how much of this reducedproductivity occurs through the effects oparasitism alone.In addition to the effect of parasites on host diversity,parasite communities should reflect the hosts that areavailable to them. Given that many parasites are hostspecific, a community rich with hosts should also be onethat is rich with parasites. For this reason, a diverse andabundant community of parasites might be reflective of adiverse and abundant community of hosts. Thus, we areleft with the apparent quandary that a diverse andhealthy ecosystem should also be one with many parasites[35]. This is a consequence of the ability of pathogens todiversify host communities and the dependence of parasite diversity on host diversity.
Parasites in food webs
David Marcogliese and others have made the cogentargument that one aspect of community ecology whereparasites have been missing is food webs[36–38]. Giventhat food webs envelop most paradigms in communityecology, the lack of parasites in food webs could precludetheir general consideration by community ecologists.Nevertheless, parasites are embedded in food webs and afood-web perspective helps indicate how disease mightindirectly affect non-host species via trophic links. Forinstance, the Iberian lynx
is currently attheedge of extinction because rabbit hemorrhagic diseasevirus has wiped out the rabbits on which it depends[39].Parasites can also be affected by changes in food-webstructure; for example, harvesting lobsters increases theabundance of their sea urchin prey, which, whenabundant, are more likely to experience bacterialepidemics[40].Although there is substantial information about therole of parasitoids in food webs[41], there are fewer dataand fewer insights into to the role of parasites, and onlyrecently have fairly complete lists of parasite species beenadded to empirical food webs. Some obvious effects of incorporating parasites include increases to speciesrichness, chain length and the number of links[42].More surprisingly, a recent food web of the CarpinteriaSalt Marsh in California finds that parasites dramaticallyincrease connectance and nestedness (Figure 1 [42]).Increases in connectance and nestedness should alterstability in food webs, suggesting that parasites have animportant role in food web structure.
Parasites and ecosystems
Insummary,parasitesappeartohaveanimportantroleininfluencing vigor and organization within communitiesbut what are the parasite-mediated effects that areimportant?Certainlytheirimpactonreducinghostfitnessand modifying competitive and trophic interactionsamong species have profound effects on the abundance of 
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