Trophic Interactions: Similarity of Parasitic Castrators to 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

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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 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 (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 affliction of humans.

*PresentAddress: Department of Zoology,University of Florida,Gainesville, Florida 32611

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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 , laboratoryand fieldstudies (Varley, 1947; Huf- most protozoans, or 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 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 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,

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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 in theireffects upon the host. predators and typical parasites are my own, but I regard themas being widelyheld opinions 4. Density-Dependentor RegulatoryEffects upon if parasitoidsand castratorsare excluded from theHost Population those categories. Section numberingbelow fol- lows that of Table 1. Density-dependencehas been demonstrated in some cases involvinginsect parasitoids. The 1. Outcomeof a Single Act manner of control and its importance have sometimesbeen contested. I suspect this effect Infectionby one parasitoid almost invariably applies likewiseto parasiticcastrators of Crusta- resultsin the death of the host (Doutt, 1959). cea. Parasitic castrationresults in the reproductive There is insufficientevidence to permitgen- death of the host. Sometimesa host may outlive eralization in this matter in respect to typical the castratorand recoverits reproductivecapa- parasites; it is likelythat the effectis variable. bilities(Caullery, 1908; Miyashita,1941; Pike, Because of the over-dispersion of parasites 1960; Kuris, in prep.). Such post-castration within host populations, the death of heavily broods are oftensmall withregard to size-specif- infected hosts, and the higher reproductive ic fecunditycurves (Pike, 1960; Kuris, in prep.) potential of parasites, the regulation of host and likely do not have much impact on the population size is considered to be an essential rate of increase of host populations, as Cole feature of parasitismby Crofton (1971) (larval (1954) argues. A single typicalparasite causes Acanthocephala are used as examples). Al- no reduction in host viability;a lone predator though Crofton(1971) does show how over-dis- consumes many prey. persed parasite populations will lead to some host mortality,the percentage of such heavily 2. SummationEffects: Multiple Infection by a infectedhosts likelyto die increases slowlywith Single Species increases in mean parasite density. This is an inherent property of approximately negative Multiple infection (the superparasitismof binomial host-parasitefrequency distributions entomologists)by most parasitoidspecies usual- generated by parasitologicallyrealistic factors ly does not produce any additive effect in (see Crofton,1971). Croftonalso failsto distin- pathogenicityto the individual host. Rarely, guish parasitoids and castrators from typical multipleinfection results in prematuredestruc- parasites. His frequency distributionanalysis tionof the host (Dogiel, Polyanski,and Kheisin, applies only to the latter organisms. Parasites 1962). Multipleinfection by parasiticcastrators at low densitiesdo not lower the fitnessof their neither speeds up castration effectsnor pro- hosts. Density-dependence has been demon- duces additional deleterious effects (Veillet, stratedfor many generalized predators. 1945; Hartnoll, 1967; Kuris, in prep.). Multiple parasitismby generalized parasitesis frequently 5. Outcomeof Multiple(Single-Species) Infections importantand may lead to a in reduction host in Respectto theParasite (Predator) viability. Multiple infection rarely occurs, and less 3. SummationEffects: Mixed Species Infections oftensucceeds among solitaryinsect parasitoids (Salt, 1961; Force and Messenger, 1964; Bur- There are usuallyno additiveaspects in terms nett,1967; and many others). Usually only one of host viabilityand pathology when hosts are parasitoid adult emerges per infection.Ordi-

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TABLE 1 A summarizedcomparison of thebiological features of insectparasitoids, crustacean parasitic castrators, typicalparasites, and generalizedpredators

BIOLOGICAL INSECT PARASITIC TYPICAL GENERALIZED FEATURE PARASITOIDS CASTRATORS PARASITES PREDATORS 1. Outcome of a resultsin death of resultsin reproduc- no reduction in a single predator single act the host tive death of the host viability consumes many host prey 2. Summation effects: usually none always none frequentlyimpor- does not apply superinfectionby tant,leading to a re- single species duction in host viability 3. Summationeffects: usually none none indicated frequent does not apply mixed infections 4. Density-dependent demonstratedin suspected herein variable variable, demon- effectson host many cases stratedin many populations cases 5. Superinfectionas it usually only one usually rarer than multipleinfections does not apply affectsparasite parasitoid emerges expected; often common (predator) (except gregarious only two parasitic species) isopods may mature per host 6. Outcome of mixed- usually only one often less frequent many mixed infec- does not apply species infections survives;first to ar- than expected; in tions normally rive commonlyde- one case the second coexist stroyslater animals arrivalcauses the death of the first castrator 7. Densityof parasite at high densities commonlyvery low variable, often high almost invariably (predator) relative parasitoid is impli- occasionallyhigh low to host cated as a host pop- ulation control agent; low and high densitiescommon 8. Taxonomic rela- 12% of all insect 3% of all crustacean veryrare within variable tionshipbetween species are parasi- species are castra- same phylum host (prey) and par- toids of other in- tors of others asite (predator) sects; sometimes crustaceans; a host and parasitoid number of castra- are in same family tors and hosts be- long to the same order, and in one example, to the same family 9. Other taxa affect- mermithidnema- coccidians,digen- does not apply does not apply ing hosts in like todes, nemato- ean trematodes, manner morphs metacercariae,di- noflagellates,ne- matomorphs,ello- biopsids, fecampid turbellarians,fungi, cestodes

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TABLE 1 (continued)

BIOLOGICAL INSECT PARASITIC TYPICAL GENERALIZED FEATURE PARASITOIDS CASTRATORS PARASITES PREDATORS 10. Host (prey) most are moderate- typicallyhighly spe- variable; often variable; often very specificity ly host-specific; cific; a few have low highlyspecific unselectivein terms some species with or moderate de- of prey species low or high speci- grees of specificity ficity 11. Size of mature parasitoid often less castratoroften less parasite several ranges from preda- parasite (predator) than one order of than one order of orders of magni- tor similarin size to stage in relation to magnitude smaller magnitude smaller tude smaller than prey to predator size of the mature than host than host host several orders of host (prey) stage magnitude larger than prey 12. Correlationof size positivecorrelation positivecorrelation no correlationex- typicallynot corre- of individual para- demonstrated demonstrated cept in cases involv-lated; sometimesa site withindividual ing intermediate positivecorrelation host hosts 13. Obligate frequent; usually many reported; rare; Microsporida does not apply hyperparasites usually most often report- ed; usually involv- ing intermediate host of the primary parasite 14. Facultative many cases known a few examples veryrare does not apply hyperparasites known 15. Host (prey) age at usually early in life, many early in life, variable variable infection some intermediate, some restrictedto few in adult adults, others variable 16. Host maturity parasitoid may in- a few species cause rarelyif ever does not apply duce premature host precocityor effectshost pupation hyperfeminization maturation narily,the initial oviposition results in emer- Multiple infectionsare usually much rarer gence. Subsequent larvae are killed by combat than randomlyexpected for most entoniscids, or are physiologicallysuppressed (Messenger, bopyrids,and sacculinids (Veillet, 1945; Altes, 1964). Salt (1961) has regarded these happen- 1962; Hartnoll, 1967; and others) and for a ings as the logical outcome for systemshaving dinoflagellate(Blastulidium contortum) (Chatton, a fixed food supply (the host). Some species 1920; Cattley, 1948). The presence of one regularlypermit the emergence of larvae from parasite prevents concurrent establishmentof more than one oviposition(i.e., theyare gregar- subsequentinfective stages encountered (Giard, ious) (King and Rafai, 1970). In both gregarious 1888). In systems in which more than one and nongregarious species, mechanisms exist parasite may infect a given host, maturation wherebythe frequencyof multiple oviposition is oftenlimited to onlytwo adults (Shiino, 1942; is so stronglyreduced (King and Rafai, 1970) Veillet, 1945; Kuris, 1971). At least for the thatmultiple infection is feltto be unimportant bopyrids and entoniscids, the upper limit of in the fieldpopulations of solitaryspecies (Force two coincides with the maximum number of and Messenger, 1964). In a few well-studied sitesbased on the morphologicalconfigurations species multiple infection is unknown (Force of host and parasite. Gregarious species are and Messenger, 1964). known, and include most of the parasitic din-

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oflagellates(Chatton, 1920) and some sacculin- (Schad, 1963; Petter, 1966) have been de- ids (Hartnoll, 1967). Polyembryony,resulting scribed. Sometimes competitiondoes result in in the production of many progeny from a unexpectedly low frequencies of mixed infec- single infection,is a regular feature of the life tions. Mixed-species predator attacks on indi- cycle of certain chalcid wasps (Askew, 1971) vidual prey organismsrarely occur. and some Rhizocephala (Veillet,1945; Hartnoll, 1967; Bocquet-Vedrine and Parent, 1973). 7. Densityof Parasite(Predator) Relative to Host Among typical parasites many examples of (Prey) multipleinfection are known, at least some of which are due to simultaneous acquisition of Both very low (less than 2% infected) and more than one parasite (such as by way of high densities (25-90+%) are commonly re- ingestion of an intermediate host harboring corded (e.g., Price, 1970). Huffaker (1971) several intermediateinfective stages). Multiple notes that to exert a controllinginfluence on infectionis sometimeslimited by already estab- host populations, the parasitoid must have a lished parasites (premunition) or host re- high density relative to its host: Densities of sponses. Polyembryonyoccurs in many hel- many castrators of crustaceans are very low minths(see reviewof parthenogenesisby Cable, (Bourdon, 1960, 1963, 1964). Occasionally, 1971). Many of his examples are drawn from both withregard to season (Gifford,1934) and the insect-parasitizingnematodes and larval locality(Veillet, 1945; Bourdon, 1963; Hartnoll, digeneans, both of whichare herein implicated 1967; Heath, 1971; Born, pers. commun.) the as parasitoidsand castratorsrespectively. percentage of infectionmay range from 25 to Multiple attack by generalized predators is 75 per cent. Some populationsof the entoniscid rare, but does occur, forexample, among social isopod, Portunionconformis, in the grapsid , Carnivora and Primates. Hemigrapsusoregonensis, reach infectionlevels of 92 per cent (Kuris, unpub.). Such castrated 6. Outcomeof Mixed-SpeciesInfectioms populations are most probably maintained by immigrationfrom other localities. (A mixed-speciesinfection is the symparasitism Typical parasiteshave a wide range of densi- of Dogiel, Polyanski, and Kheisin, 1962; the tiesper host. Often such densitiesare farhigher superparasitismof Noble and Noble, 1964; the than the densities reached by the majorityof multiparasitismof entomologists-see Askew, parasitoid and castrator populations. Patterns 1971). of infectionof typicalparasites lead to frequency Among insect parasitoids,typically (i.e., soli- distributionsof the parasite load that approxi- tary parasitoids), only one individual of one matenegative binomial expansions (Li and Hsu, species can survive to emergence. Usually the 1951; Crofton, 1971; Pennycuick, 1971b). firstto arrive destroysthe subsequent arrivals These result in very high absolute densities of (Fisher, 1962). Rarely,both may survive, or both parasites in the total population at a given perish because of host overexploitation (Salt, percentageof infection,in comparison to either 1961). Mixed infectionsof parasitic castrators castratoror parasitoid populations. of Crustacea are often found to be less frequent Generalized predatorsalmost invariably have than expected on the basis of random infective low population densities compared to the behavior patterns (Chatton, 1920; Reinhard densitiesof theirprey, even when these systems and Buckeridge, 1950; data from Bourdon, are implicatedin population control. 1960; Altes, 1962). Sometimesmixed infections are more numerous than expected (Veillet, 8. TaxonomicRelationship between Host (Prey) 1945; Bourdon, 1960). In at least one such case and Parasite(Predator) the second arrival often causes the death of the earlier castrator (Veillet, 1945). This in- An estimated 12 per cent of all insect species teraction is akin to hyperparasitism. Mixed are parasitoidsof otherinsects (calculated from infections may also occur randomly (Altes, informationgiven in Askew, 1971). Sometimes 1962). hymenopterous parasitoids attack species be- Many mixed infectionsof typical parasites longing to the same familyof parasitoids. normally coexist. species flocks An estimated 3 per cent of all crustacean

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species are castratorsof other Crustacea (calcu- and fungi (Johnson, 1958). For unknown rea- lated frominformation given in Watermanand sons, crustaceans are subject to castration by Chace, 1960). A number of instancesof castra- members of several differenttaxa. tionwithin the same order are known(Carayon, Judgement as to whether many species of 1942; Bocquet-Vedrine, 1961, 1967; Bourdon, Microsporidabelong in both of the above cate- 1967) and at least one example withinthe same gories is reserved until relationshipsbetween family (Caroli, 1946; Catalano and Restivo, the number of spores involvedin transmission, 1965). reproduction within the host, pathology, and For both the Insecta and the Crustacea, their mortalityare betterunderstood. If the size of respectiveparasitoid and castrator faunas are the initial inoculum does not determine the dominated by species of the same taxonomic outcomeof theinfections, then I would consider class (see below for exceptions). Possiblythese the appropriate species to be parasitoids or taxa are preadapted for this relationship. castratorsrather than parasites. Certainly for Parasitoidsand castratorsare veryfinely atuned some species (Veber and Jasic, 1961) the pa- to their hosts' life histories.Since key features thology is dosage-dependent. For similar rea- of insect life histories,such as diapause and sons, most Microsporida and other protozoan metamorphosis,are under the controlof endo- pathogens are omittedfrom Tables 1 to 3. crine systems,it seems reasonable to expect that I stressthe factthat these verydiverse groups insect parasitoids can either "read" (e.g., of organisms, especially the mermithids,ne- Schoonhoven, 1962) or "direct" (e.g., Johnson, matomorphs,insect parasitoids, dinoflagellates, 1965) these systems.In like manner, molting fecampids,copepods, isopods, and rhizocepha- of bopyridisopods in synchronywith their hosts lans, all share virtuallyevery aspect of the (Caroli, 1927; Tchernigovtzeff,1960; pers. ob- detailed comparison summarized in Table 1. serv.) and the feminization of male hosts The exigencies of the parasitoid-castrator througheffects on theandrogenic gland (Veillet process seem to force narrow strategiclimita- and Graf, 1958) probably represent "reading" tions on parasitoidsand castrators. and "direction"of crustacean hosts. Generalized parasites very rarely parasitize hosts withinthe same phylum.The taxonomic 10. Host (Prey)Specificity relationshipbetween generalized predatorsand their prey is variable. In the followingdiscussion high host specific- itymeans one or two closelyrelated hosts exist; low host specificitymeans that dozens of hosts 9. OtherTaxa AffectingHost in a Like Manner exist,often belonging to separate families. Insect parasitoidsare moderatelyhost-specif- Many mermithoidand steinernematidnema- ic, such specificitybeing primarilybehaviorally todes (Welch, 1965) and nematomorphsproba- and ecologically determined (Doutt, 1959). bly have a parasitoid effectupon theirorthop- Some species, such as Nasonia vitripennis(Whit- teranhosts. For reasons as yetunknown, insects ing, 1967), have a low degree of host-specificity. are very susceptible to one-on-one predation Parasitic castratorsare typicallyhighly host- systems. specific.Epicaridean isopods are classicallyre- Non-crustacean parasitic castrators of garded as strictlyhost-specific (Giard and Bon- Crustacea include the coccidian Aggregata(see nier, 1887; Bonnier, 1900), although it is likely Smith,1905), digenean trematodemetacercaria that much of this specificityis ecologically in- (Noble and Noble, 1964), dinoflagellates(Chat- fluenced. A few species have a low degree of ton, 1920; Cattley,1948), (Pe- host-specificityin the field; for example, He- rez, 1927; Born, 1967), the enigmatic Ello- miarthrusabdominalis has been recorded from biopsidae (Chatton, 1920; Fage, 1940; Wick- 22 hosts (Pike, 1960). stead, 1963; Hoffman and Yancey, 1966; Typical parasites have variable degrees of Mauchline, 1966), fecampid turbellarians host-specificity,but often are highly host-spe- (Mouchet, 1931; Baylis, 1949; Christensenand cific. Generalized predators also have varying Kanneworff,1965; Kanneworffand Christen- degrees of prey-specificity,but are often very sen, 1966), cestode procercoids(Mueller, 1966), unselectivein termsof prey species.

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11. Size (Weight)of theMature Parasite 13. Hyperparasites(Obligate) (Predator)Stage in Relationto theSize of the MatureHost (Prey)Stage Hyperparasitoidsare frequentlyreported in insect parasitoid systems.They are usually hy- Insectparasitoids are fromone to a feworders menopterous species. Several examples are of magnitudesmaller than their hosts-i.e., they given in Askew (1971). These may play a role are of relativelylarge size (Doutt, 1959). Para- in disruptionof the controlof host populations siticcastrators have a similarsize range relative by the primaryparasitoids. Hypercastrators are to their hosts. Typical parasites, in contrast, known for a number of parasitic castrators. are severalto nianyorders of magnitudesmaller They are usually isopods-for example, liriop- than their hosts. Generalized predators range sids on sacculinids (Pike, 1961), Cabirops on in size frombeing about the same size as their Pseudione (Carayon, 1942), Gnomoniscuson preyto being severalorders of magnitudelarger Podascon (Caullery, 1952), and perhaps the than theirprey. copepod Paranicothoefound in the emptybrood pouch of bopyrid isopod hosts (Carton, 1970). Stromberg,however (pers. commun.), believes 12. Correlationbetween the Size of theIndividual that, in general, the cryptoniscineisopods are Parasite(Predator) and Its Individual Host (Prey) true hyperparasites,not hypercastrators. The parasite-host (predator-prey)size cor- Interestingly,the only previous referenceto relation should be envisaged between animals the resemblance between parasitic castrators at a similar stage in life historywhenever dis- and insectparasitoids seems to be thatof Perez crete stages occur-e.g., only fourth instar (1931), whose manycontributions to crustacean parasitoidlarvae should be compared witheach biology have often been overlooked by later other. The strongestcorrelations will of course writers. Working with the hypercastrator, be betweenhost size and relativelymature stages Liriopsispygmaea, on Peltogasterpaguri, a pri- of parasitoid or castrator.In the cases of para- mary castratorof Eupagurus bernhardus,Perez sitoids,castrators, and parasites it seems most (1931) observed that the observed Peltogaster reasonable to regard host size as the indepen- population was sterilizedby an epidemic of the dent variable. Positivecorrelations result from hypercastrator.He noted the similarityof the parallel growth of both members of the in- phenomenon to the effectof hyperparasitoids teractingpair. For predator-preysystems, the on insect primaryparasitoids. predator's size is usually regarded as the Hyperparasites of typical parasites are very independent variable as size of the prey usually rare, the most commonly reported being mi- involves some selection on the part of the crosporidians (Dissanaike, 1957; Canning and predator. Basch, 1968). It is significantthat several of Positivecorrelation between host and parasit- these microsporidiansparasitize larval stages of oid size has been demonstrated(Askew, 1971). helminthsin the intermediatehost (see below). Host and castrator size are likewise typically The haplosporidian, Urosporidium,in micro- positivelycorrelated (Pike, 1960; Allen, 1966; phallid metacercariae (Couch and Newman, Samuelsen, 1970; Kuris, 1971; by inference, 1969) fitsthis pattern. Giard and Bonnier, 1887; Morris, 1948). Size of typicalparasites is usuallynot correlatedwith 14. Hyperparasites(Facultative) hostsize, except in instancesinvolving interme- diate hosts. Prey are often not correlated with Many hymenopteransare known to be either predator size (e.g. Galbraith,1967; Moran and primaryparasitoids or hyperparasitoids.Some Fishelson, 1971). When positivecorrelations do species, upon completion of a hyperparasitic occur (for a good example, see Menge, 1972), phase resultingin the destructionof the original the correlationis usually weaker than that seen primaryparasitoid, complete their development in the parasitoid or castratorsystems (compare as parasitoids of the original host (e.g., Price, with Pike, 1960). Predator-preysystems with 1970). In some arrhenotokousprimary parasitic similarrelative sizes (see Section 11 above) are species, larval males, only, develop as those in which individual predator-prey size hyperparasites,often conspecifically.Females, correlationsare found. however, are only primary parasites (Doutt,

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1959; Kennett,Huffaker, and Finney, 1966). 16. Host Maturity A fewexamples of facultativehypercastration Several are known.Caroli (1946) reportsthat the young insect parasitoids have been noted to induce premature bopyridPseudione euxinica spends the early part pupation in their insect hosts (Varley and Butler, 1933). Among para- of its lifeon the bopyrid Gygebranchialis. Upon thedeath of Gyge,P. euxinicabecomes a primary sitic castrators,Cryfitoniscus pagurus may cause precocious development of infestedSeptosaccus parasite of the host, Upogebia littoralis.The rodriquezi gradual destructionof a previously infecting (Altes, 1962). Reinhard (1956) notes that sacculinidby entoniscids,coupled withthe non- hyperfeminization,the appearance of adult random prevalenceof mixed infectionsof these characteristicson small female hosts, is an species (Veillet, 1945; Miyashita, 1941) lends oft-reportedeffect of sacculinization. Typical if thissituation some of the qualities of facultative parasites rarely, ever, cause precocious host maturity. hyperparasitism.Altes (1962) feels that Cryp- toniscuspaguri, a hypercastratorof Septosaccus rodriquezi,may sometimesbe a parasite of the primaryhost, Clibanarius erythropus. The dwarf, CASTRATORS OF INSECTS, PARASITOIDS OF CRUSTACEA hyperparasiticmales that typicallyaccompany female Epicaridea do not merit consideration The functional similarityof parasitoid and here because there is no evidence that they castratorsystems on theirinsect and crustacean harm the female. In fact, they may not feed host populations is further suggested by an at all. No examples of facultativehyperparasites interestingturnabout. Some insect species are are known,but the apparent ingestionof some subject to parasitic castration prior to their protozoan parasites by digenetic trematodes parasitoid-induceddeath (Table 2), and some (Dogiel, Polyanski,and Kheisin, 1962), may be crustaceansare essentiallyconsumed by organ- judged as rare, comparable examples. isms which were initially merely castrators (Table 3). Inspection of Table 2 shows that for most 15. Age of Host at Time of Infection castrator-insecthost systems,the cessation of reproductiveactivity is a prelude to death of Insect parasitoids usually infect their hosts the host followingemergence of the parasitoid. early in life (Salt, 1963). Many egg and larval In some systems, such as the nemestrinid- parasitoids are known. Pupal parasitoids are orthopteransystem, the outcome of the para- common, but adult-infectingparasitoids are site-hostinteraction is variable; sometimes the infrequent (Doutt, 1959). Salt (1968) has host survives, sometimes it does not. Some proposed that invasion of young hosts leads tylenchoidnematodes and mostStrepsiptera are to the acquisition of the proper surface "im- close to nonlethalcastrators, the host's life span munologicalpassport." Infecting young animals rarely being shortened. As the crustacean gives the parasitoid time to act as a chronic castratorscontrol the host'sreproductive system destructor. throughthe host's endocrine system (Veillet and Among parasiticcastrators, most bopyrids are Graf,1958), so does theaphelenchoid nematode considered to attackonly young hosts(Carayon, parasite of Bombus,Sphaerularia bombi, by caus- 1943; Pike, 1960, 1961). A few species may ing degeneration of the corpora allata (Palm, be restrictedto adult hosts (Pike, 1961). Saccu- 1948). Again in parallel withcrustacean castra- linids also seem to settlepreferentially on juve- tors,a single Sphaerulariaelicits the full castra- nile hosts (Veillet, 1945). The time of infection tion response, and the pathologyis not additive by entoniscids appears to be relativelyunre- with superinfection (Hattingen, 1956, from strictedby the age of the host (Veillet, 1945; Welch, 1965). The reciprocal relationship, Kuris, 1971). Salt's (1968) immunologicalpass- wherein crustaceans are killed through a port theoryis held to be applicable to castrators, parasitoid-likeaction (Table 3), also provides too. some insight. Like the vast majorityof insect Typical parasites and generalized predators parasitoids,Kronborgia, a fecampidturbellarian, vary greatlywith regard to the phase of the killsits host upon emergenceof the adult worm. life historyof the host attacked. AlthoughKanneworff (1965) demonstratesthat

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the castrationeffect is of greater importance, parasitoidinsects. Examination of other terres- this is, in part, a parasitoid-hostrelationship. trial and semiterrestrialcrustacean taxa may The terrestrialsuccess of the oniscoid isopods well providemore examples of insectparasitoids undoubtedlyexposed them to infectionby the that affectcrustaceans.

TABLE 2 Some organismshaving a castratoreffect on theirinsect hosts

CASTRATOR(S) HOST(S) REMARKS REFERENCE Dilepidids castrate; many morphologicalef- Plateaux, 1972 fects;behave as social parasites; superinfectionmay cause an additive response Nematoda Mermithids ants intercastes Welch, 1965 Mermithids chironomids, intersexes;gonads affected;kill Welch, 1965 simuliids,others upon emergence Many tylenchoidsand Coleoptera, Lepi- reduce fecundity;rarely kill Welch, 1965 aphelenchoids doptera, Diptera, Hymenoptera Heterotylenchuspav- fleas castrates;kills on emergence Welch, 1965 lovskii(tylenchoid) Nematomorpha Orthoptera castrates;kills on emergence Dorier, 1965 Insecta Strepsiptera Hymenoptera, castrates;usually doesn't kill Askew, 1971 Hemiptera, some hosts; males feminized,females Thysanura, masculinized Orthoptera Hymenoptera some braconids weevils castrates; killson emergence Loan and Holdaway, 1961 Diptera nemestrinids,some Acridoidea usually castratesbefore killingon Greathead, 1963 calliphoridsand emergence; some only reduce muscids fecundity;lethal

TABLE 3 Organismshaving a parasitoideffect on theircrustacean hosts

PARASITOID(S) HOST(S) REMARKS REFERENCE Fungus Metschnikowia(yeast) Copepoda, Clado- causes host's death Fize, Manier, and cera, Artemia Maurand, 1970 Turbellaria Kronborgiaamphipo- Ampeliscamacro- castrationprecedes death Christensenand dicola cephala upon emergence Kanneworff,1965 Diptera Tachinidae terrestrialisopods typicalparasitoid effect Askew, 1971

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TABLE 4 Parasitoid-likephenomena involving hosts other than crustaceans and insects

PARASITOID HOST(S) REMARKS REFERENCE Microsporida Nematoda Pleistophora Metoncholaimus host, marine; infectionalways Hopper, Meyers,and scissus terminal;authors suggest Mi- Cefalu, 1970 crosporida-nematodeinfections are more common than previous- ly expected Pereziaeurytremae - hyperparasitoidof larvae in snails Canning and Basch, Digenea 1968 Haplosporida Urosporidumcrescens Trematoda- hyperparasitoidof metacercariae Couch and Newman, Digenea in Callinectes 1969 Platyhelminthes-Cestoda Mammalia Echinococcus humans, voles, hydatidcysts in intermediate Rausch and Schiller, sheep, and hosts resultingfrom single infec- 1956; Schiller, 1966 other herbi- tions typicallyreduce host vores viability Nematoda Daubaylia freshwaterpul- reproduces withinhost; causes Chernin, 1962 monates some castrationeffects before killinghost Nematomorpha Arthropoda castratehost before killingupon Dorier, 1965; Sahli, millipedes, emergence 1972 centipedes, whip-scorpions Mollusca- Coelenterata- Opisthobranchia Hydrozoa Phyllirhoe Zanclea medusa gradually consumed Martin and Brink- mann, 1963

Cephalopyge Nanomia probably similarto Phyllirhoe,but Sentz-Braconnotand may possiblyconsume more than Carre, 1966 one host to complete develop- ment

Hymenoptera Arthropoda typicalparasitoid process Askew, 1971 ticks,mites, spiders, pseudo- scorpions Diptera tachinids centipedes typicalparasitoid process Askew, 1971 phorids millipedes uncertain Picard, 1930 Mollusca sciomyzids freshwaterand many species are predators,some Berg, 1964; Bratt, terrestrial are typicalparasitoids; suggested Knutson, Foote, and as biocontrolagents Berg, 1969 Acarina Annelida Histiotomamurchiei earthworm an egg parasitoid Oliver, 1962

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TABLE 5 Parasiticcastration-like phenomena involving hosts other than crustaceans or insects

CASTRATOR HOST(S) REMARKS REFERENCE Sporozoa Annelida- Oligochaeta Mackinnoniatubificis Tubifextubifex destroysgonad Janiszewska,1967 Microsporida Sporozoa-Gregarinia Nosemafrenzelinae Frenzelinacon- preventssporogony after syzygy; Leger and Dubosq, formis pre-reproductivegrowth normal 1909 Pisces-Cyprinidae Pleistophoraovariae Notemigonus partial castration;possibly Summerfeltand crysoleucas enhances somatic growth Warner, 1970 Haplosporida Cestoda Urosporidiumcharletti Catenotaenia hypercastrator Dollfus, 1943 dendritica Ciliatea Echinodermata- Asteroidea Orchitophryastellarum Asteriasrubens mostlyin male hosts; may only Vevers, 1951 be partial castration;possible role in population control Mesozoa Echinodermata Orthonectida Ophiuroida typicallyrender host gonads Giard, 1888; Caullery nonfunctional and Lavallee, 1912; Fontaine, 1968 Coelenterata-Anthozoa Coelenterata- Hydrozoa Peachia quinquecapitata Phialidium a temporarycastrator, sometimes Spaulding, 1972 a parasitoid; ectoparasitic,feed- ing on gonads of medusa; host may die afteranemone leaves; gonads can regenerate Turbellaria Turbellaria Oikiocolax Plagiostomumsp. Reisinger, 1930 (from plagiostomorum Jennings,1971) Trematoda-Digenea most sporocystand Gastropoda acute castrationappears to be the Rothschild,1941; redial stages rule; sometimessecondary sexual Wright,1966; K0ie, characteristicsaffected and be- 1969; Lim and Heyne- havioral changes; prolonged life man, 1972; Kuris, or gigantismsuggested for some 1973. infections;sometimes reduce host viability;mixed species infections rare-one species eliminates competitoreither indirectlyor throughdirect predation Bucephatusmytili Bivalvia destroysgonad, infected Breton, 1970 sporocysts hosts larger Brachiopoda gymnophalinemeta- Glottidiapyra- sometimesgonad destroyed Paine, 1963 cercariae midata

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TABLE 5 (continued)

CASTRATOR HOST(S) REMARKS REFERENCE Cestoda Pisces pseudophyllidplero- Cyprinidae, destroygonad; may reduce Arme and Owen, 1967; ceroids Gasterosteus host viability;causes many Arme, 1968; Penny- behavioral changes cuick, 1971a Nematoda Mammalia Mammanidula Sorex infectlactating mammaries, pre- Okhotina and asperocutis vent nursing; high infectionrates Nadtochy, 1970 accompany high host density suggestingrole in population regulation; a castratorin the sense that it eliminateshost's reproductivecapabilities Annelida Echinodermata Myzostomida Crinoidea some species cause partial Prenant, 1959 castration

Mollusca-Gastropoda Entoconchamirabilis Holothuroidea Giard, 1888 Crustacea-Copepoda Annelida monstrilloids Syllidae Malaquin, 1901; Xenocoeloma Polycirrus fecundityreduced Boquet, Boquet- Vedrine, and l'Hardy, 1968 Bivalvia Mytilicola Mytilus gonad reduction Mann, 1967 Pisces Sarcotretesscopeli Myctophidae preventsgonadal maturity;no Gj0saeter, 1971 effecton secondary sexual char- acters; parasitized animals slight- ly smaller than theirage class Crustacea-Cirripedia Echinodermata Ascothoracica Echinoidea, As- destroysor greatlyreduces Brattstr6m,1936; teroidea gonads Achituv, 1970

Pisces-Elasmo- branchia Anelasmasqualicola Etmopterusspin- hosts ovaries become inactive, Hickling, 1963 ax testesprobably functional; increased mortalityof parasitized sharks Crustacea-Brachyura Pinnotheres Bivalvia castrationand even sex reversal Hornell and Southwell, of infectedhosts; female crab size 1909; Awati and Rai, correlated with host size 1931; Atkins,1926; Berner, 1952 Pisces Jordanicus Holothuroidea eats gonads; extent and perma- Trott, 1970 nence of effectsuncertain

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PARASITOID AND CASTRATOR SYSTEMS IN THE bly in minnows castrated by Microsporida KINGDOM (Summerfeltand Warner, 1970) and pelagic copepods castrated by Blastulidiumcontortum Even withthe exclusion of larval trematodes, (Cattley, 1948; but not Chatton, 1920). If the cestodes,and acanthocepthalans(to be covered "replacement" of the ovary by the parasite in detail in Kuris, in prep.), parasitoid systems results in an energeticallyless expensive total (Table 4) and castrator systems (Table 5) system,as is suggested by data on Hemigrapsus operate on a surprisinglydiverse list of host oregonensiscastrated by Portunion conformis systems. (Kuris and Lawlor, in prep.) then gigantism Parasitoids of non-insects are very poorly or increased survivorshipof parasitized hosts, known, excepting the detailed studies on the or both,should not be unexpected. Summerfelt Sciomyzidae by Berg (1964) and coworkers. and Warner (1970) also take this viewpoint. Most of theinteractions placed in Table 4 should If a castratorhas a positive effecton its host's be regarded as tentative.Of interestagain, the viabilityor growth (or both), the increased specialized hymenopterous and dipterous production of castrator offspringbecause of parasitoids have invaded most non-insect ter- prolongedlife and the stronglyhost size-specific restrialarthropod taxa. Again, the inclusion of fecundityschedules of many of the castrators protozoan infectionsin this list is speculative. would seem to be strongselective factors favor- Castration effectsseem to occur more fre- ing the castrationpathology. Rothschild (1938) quently and in a greater taxonomic diversity recognizedthe selectiveadvantage of large snail of systemsthan do parasitoid effects.Table 5 size to cercarialproduction. Castrators of inter- providesa listof castratorsranging from Proto- mediate hosts,where the transmissioninvolves zoa to Brachyuraand Gastropoda, a listof hosts ingestion of that host by the definitivehost, from Protozoa to Mammalia. Orchitophyrain would not be expected to energetically"con- Asteriasand Mammanidulain Sorexhave both serve" intermediatehosts. Walkeyand Meakin been suggested as being involvedin host popu- (1970) indicate that larval Schistocephalusare lation control (Vevers, 1951; Okhotina and quite costlyto their sticklebackhosts. Nadtochy, 1970). Indeed, the mammarynema- Argumentsraised concerningthe loss of the tode infection rate appears to be density- host's progeny to future parasite generations dependent. tacitlyand unnecessarilyinvoke group selection. Larval trematodescommonly castrate (Kuris, Mechanisms to reduce pathological effects 1973) and sometimeskill (Sturrock and Webbe, characterizethose parasites for which the pa- 1971) their snail hosts. The snail-trematode thologydoes not improvethe survivalor repro- trophicinteraction satisfies most of the biologi- ductive success of the parasites on hand. cal featuresof parasitoid and castratorsystems Drastic modificationsin host behavior some- given in Table 1. The similarityof snail-trema- times accompany parasitizationby parasitoids tode to insect pest-parasitoidtrophic interac- and castrators. Braconid parasitoids prevent tions has already been proposed (Kuris, 1973). diapause in some insect hosts (Varley and Consequences of mixed species larvaltrematode Butler, 1933). Sacculinized Carcinusbehave as infections(see reviewsby Lim and Heyneman, reproductive females, migrating to shallow 1972; Lie, 1973) are much like mixed parasitoid water and showingegg-care behavior (Rasmus- infections.Biological control of schistosomiasis sen, 1959). Ants harboring dicrocoelid tape- through competitiveexclusion by trematodes worm larvae act as social parasites, always re- with redial generations is theoreticallyfeasible questingfood fromunparasitized workers (Pla- (Kuris, 1973). teaux, 1972). Sticklebackscarrying advanced In some cases parasitic castration has been cestode plerocercoidsswim near thesurface and shown to be accompanied by prolonged life are thus easy prey for bi&ds(Arme and Owen, or gigantismof thehost, or byboth. This curious 1967). Poinar and van der Laan (1972) show parasite-induced syndrome-castration, pro- that infected queen bumblebee "eternal longed life, and gigantism-occurs in snails seekers" do not complete their hibernation harboring certain larval trematodes (Roths- flight,but continue to flylow over the ground, child, 1941), in male pea infected with stoppingbriefly to dig littlepits in the soil and Pinnotherion(Mercier and Poisson, 1929), possi- release Sphaerulariainfective larvae. The classic

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 143 host behavioral modificationis caused by the significant.In these parasitized populations, sporocystof Leucochlori&ium,a brightly colored prevention of reproduction in early breeding active form in snail tentacles-essentially a periods has a more suppressiveeffect on popu- semaphore systemto attractbirds-the defini- lation than does the preventionof reproduction tivehosts (Noble and Noble, 1964). In the latter (by death) in later periods. three cases the host becomes little more than In brief, on the basis of the sharp resem- a parasitoid-guided missile system,operating blances betweenparasitic castrators and parasit- to complete the life cycle of the parasitoid in oids outlined above, I conclude that castration a self-destructiveact. Such gross modifications phenomena may be importantcomponents of of host behavior rarelyoccur under the influ- population regulationsystems for many marine ence of true parasites. organisms. Malacostracan Crustacea are con- A few interactingsystems combine parasitic sidered to be particularlysubject to such castra- castration with the shortened host life span tion systems. Parasitic crustaceans are often characteristicof parasitoids.The fecampid tur- discovered to exert a castrationeffect on their bellarian, Kronborgia,causes such effectson its hosts,crustacean or otherwise. amphipod host (Kanneworff, 1965). Gordia- Further elucidation of the role of parasitic ceans and mermithid nematodes also cause castratorsin the regulation of crustacean host castration;death of the host followsupon the populations must await long-termdensity sam- emergence of the parasite (Dorier, 1965; The- pling programs for both host and castrator odorides, 1965). The bizarre relationship be- populations, or the domestication of suitable tween the parasitic , Anelasma,and its laboratory systems. The comparative analysis deep-sea shark host Etmopterusseems also to assembled here suggeststhat the regulatoryrole be of thisnature. Hickling (1963) makes a good of castratorsmay be considerable. case forthe premature demise of the parasitized host. The nematode Daubaylia produces some castrationeffects prior to overwhelmingits snail ACKNOWLEDGEMENTS host (Chernin, 1962). Possible differentialmor- tality of parasitically castrated hosts is also I thank Cadet H. Hand, John E. Simmons, suggested in the data of Gj0saeter (1971) for WilliamE. Hamner, Donald Heyneman, Mario myctophidsinfected by the copepod, Sarcotretes. Baudouin, John Vandermeer, Daniel Janzen, In agreement with Kanneworff (1965), I Stephen Hubbell, and especially Carl B. Huf- regard castrationof the host as having a more fakerfor critical review of thismanuscript. John importanteffect on the host population than W. Born, Larry Lawlor, Jon Standing, Bonnie does the ultimate death of the afflictedhost. Dalzell, and Gene Miller provided additional Upon release of the worm, the host is old and illuminating discussions. This work was often past the period when its contributionto supported in part by NIH predoctoral and the population's reproductive effortwould be postdoctoralfellowships.

LIST OF LITERATURE

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