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Trophic Interactions: Similarity of Parasitic Castrators to Parasitoids Author(S): Armand M Trophic Interactions: Similarity of Parasitic Castrators to Parasitoids Author(s): Armand M. Kuris Source: The Quarterly Review of Biology, Vol. 49, No. 2 (Jun., 1974), pp. 129-148 Published by: The University of Chicago Press Stable URL: http://www.jstor.org/stable/2820942 Accessed: 10-06-2015 23:11 UTC Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at http://www.jstor.org/page/ info/about/policies/terms.jsp JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. The University of Chicago Press is collaborating with JSTOR to digitize, preserve and extend access to The Quarterly Review of Biology. http://www.jstor.org This content downloaded from 128.111.90.61 on Wed, 10 Jun 2015 23:11:30 UTC All use subject to JSTOR Terms and Conditions TROPHIC INTERACTIONS: SIMILARITY OF PARASITIC CASTRATORS TO PARASITOIDS BY ARMAND M. KURIS* ZoologyDepartment, University of California,Berkeley, and Bodega Marine Laboratory, Bodega Bay, California ABSTRACr An analysisof life historyfeatures of insectparasitoids and crustaceanparasitic castrators suggeststhat theseare similar trophicphenomena, distinct from parasitism and predation.A parasitoidconsumes only one hostduring its lifetime;parasitic castrators cause the reproductive deathof only one host.Since population densities of many insect species are regulatedby parasitoids, parasiticcastrators may also playan importantrole in hostpopulation regulation. Parasitoidsof insectsand parasiticcastrators of crustaceans (1) in singleinfections always kill thehost; whereas lone parasitesdo notaffect host viability; and predatorskill many prey; (2) do notcause increasingpathology or increasinglikelihood of mortality in multipleinfections; whereasparasites often have an additiveimpact; (3) do notcause increasingdamage in mixedspecies infections; whereas mixed parasite infections oftenhave interactivenegative effects; (4) usuallyhave mechanisms to reduce or eliminate multiple infections; whereas multiple infections are commonfeatures of parasite systems; (5) also showreduced frequencies of mixed species infections; whereas such infections are common amongparasite species; (6) are oftentaxonomically closely related to theirhosts; whereas parasites rarely are and predators varyin thisrespect; (7) are oftenless than one orderto a few ordersof magnitudesmaller (by weight)than their hosts;whereas parasites are severalto manyorders of magnitudesmaller; and predatorsrange fromsimilar-sized to severalorders of magnitudelarger than their prey; (8) showstrong positive size correlations with their hosts; whereas parasites show no sizecorrelation withtheir hosts; and onlyrelatively small predatorsare sometimescorrelated by size with their prey; (9) frequentlyare killedor castratedby obligate hyperparasitoids and hypercastrators;whereas parasitesrarely have hyperparasites; (10) sometimesact as facultativehyperparasitoids or hypercastrators;whereas parasites very rarelyact so; (11) parasitoidsand oftencastrators most commonly attack very young hosts; whereas parasitism and predationare veryvariable with respect to age of thehost (prey); and (12) oftencause precocioushost development; whereas parasites rarely affect host maturation processes. Some insectparasitoids castrate their hosts before killing them; some crustaceans are ultimately consumedby their castrators. Parasitoidand castratorsystems not involvinginsect or crustaceanhosts are brieflyreviewed. These trophicinteractions may be morewidespread than is generallyconsidered. Hydatid cyst diseaseis regardedas theonly parasitoid affliction of humans. *PresentAddress: Department of Zoology,University of Florida,Gainesville, Florida 32611 129 This content downloaded from 128.111.90.61 on Wed, 10 Jun 2015 23:11:30 UTC All use subject to JSTOR Terms and Conditions 130 THE QUARTERLY REVIEW OF BIOLOGY [VOLUME 49 INTRODUCTION ing the effectof parasitic castration on host populations,I hypothesizethat if castrators are P ARASITIC castrationmay be regard- efficientdensity-dependent predators consum- ed as a specialized mode of predation. ing one prey per individual,as do insectparasi- In the general case, each castrator toids, then there should be many analogous causes the reproductivedeath of one features evident when parasitic castrators of and onlyone host.Viewed in thissense, crustaceans are compared with insect parasi- the population consequences of parasiticcastra- toids. Some of these parallel featuresare likely tion may be remarkablyanalogous to those of to be of great importance in the biology of the parasitoid insects.Parasitoid insectsunder- these parasite-host (predator-prey) systems. go their larval development within the eggs, The hypothesis that parasitic castrators may larvae, pupae, or adults of other insects,almost have an impact on their hosts' populations invariablyconsuming the host in the process comparable to that demonstrated for insect (see Doutt, 1959, for an excellent review). A parasitoidsis tested by the comparison of simi- single parasitoid is thus responsible for the laritiesof the two systems(Table 1). The dif- consumptionof one and only one host during ferences between castratorsand parasitoids as its lifetime. a class of trophicinteractions, when compared The role of insect parasitoids in regulating witheither true parasites (such as monogeneans, hostabundance has been demonstratedin many adult digeneans and cestodes,many nematodes, laboratoryand fieldstudies (Varley, 1947; Huf- most protozoans, or fish copepods), or preda- faker and Kennett, 1966; Van den Bosch, tors (such as many insects,vertebrates, proso- Schlinger,Lagace, and Hall, 1966; and many branch gastropods, spiders, turbellarians,or others). A minority view holds that insect coelenterates)are also indicatedin Table 1. The parasitoids are of limited importance in the parasite-hosttrophic relationship between pop- population regulation of insect hosts (An- ulations of larval digeneans and cestodes and drewarthaand Birch, 1954). their intermediatehosts are seen in almost all The basis of the significantpart played by respects to be similar to that of either the the entomophagous parasitoids in the control castratoror parasitoid systemor both. These of hostpopulations lies in theefficient searching relationshipswill be analyzed elsewhere (Kuris, abilityof the parasitoids at low host densities in prep.). One should bear in mind that when and in the density-dependentresponse of the large categories of animals are treated in such parasitoidsto increasinghost numbers. If para- tersefashion, exceptions to everygeneralization sitic castratorsof Crustacea operate in a like may be brought forth.Still, the generalitiesdo manner, then parasitic castrationis implicated fitthe large majorityof each group of interac- as an extremelyimportant part of the system tions. of population regulationfor crustacean species. Regulation of crustacean populations by par- COMPARISON OF CRUSTACEAN CASTRATORS, INSECT asitic castrationhas not been studied. Only a PARASITOIDS, TYPICAL PARASITES, AND GENERALIZED fewhost species have been sampled well enough PREDATORS to allow accurate densityestimates. In none of these have the population dynamics of the This section is a documentationand discus- parasiticcastrators and theirhosts been studied sion of Table 1. To prevent the vast literature concomitantlyto establisha correlationbetween fromoverwhelming a work of this sort,I have host and parasitedensity changes. Investigation resorted to the frequentcitation of recent re- of density-dependentmechanisms in host-para- viewsand monographs for the ample literature site interactionsinvolving parasitic castration on insectparasitoids. Exceptional studies,cases mustawait access to suitablelaboratory systems. which the reviewer did not seem to endorse, Unfortunately,the life histories of both the and cases where my own interpretationof the crustacean hosts and their parasites are suffi- work in question disagrees with that of the cientlycomplex not to have permittedroutine reviewerare cited fromthe primaryliterature. rearing of more than one generation in the As for the castrationliterature, which has not laboratory. been well reviewedand forwhich my generali- Despite the inadequacy of knowledge regard- zationsmay consequently be subject to question, This content downloaded from 128.111.90.61 on Wed, 10 Jun 2015 23:11:30 UTC All use subject to JSTOR Terms and Conditions JUNE 1974] PARASITIC CASTRATORS AND PARASITOIDS 131 I have provided more abundant citations.Sci- simultaneously infected by two species of entificnomenclature has been updated in many parasitoids.Occasionally both parasitoids perish places, but I have no pretension of having owing to unsuccessfulcompetition or host over- satisfieda consensus of modern specialists in exploitation(Salt, 1961). For parasiticcastrators the range of organismsbrought into this discus- no increasein castrationof the hostsis indicated sion. My use of suprageneric taxa is uneven for mixed species infections(Reverberi, 1943; and is intended merely to permit readers of review,Veillet, 1945). Mixed species infection diverse intereststo place unfamiliarorganisms. of typicalparasites frequently causes an increase The terse comments regarding generalized
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