Trophic Interactions: Similarity of Parasitic Castrators to Parasitoids

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
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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 history
featuresof insectparasitoidsand crustaceanparasiticcastrators
suggeststhattheseare similar trophicphenomena,distinctfromparasitismand predation.A
parasitoidconsumesonlyone hostduringits lifetime;parasiticcastrators
cause thereproductive
deathofonlyonehost.Sincepopulationdensities
ofmanyinsectspeciesare regulated
byparasitoids,
parasiticcastrators
mayalso playan important
rolein hostpopulationregulation.
Parasitoidsof insectsand parasiticcastrators
of crustaceans
(1) in singleinfections
alwayskill thehost;whereaslone parasitesdo notaffecthostviability;
and predators
killmanyprey;
or increasinglikelihood
(2) do notcauseincreasingpathology
in multipleinfections;
ofmortality
whereasparasitesoftenhave an additiveimpact;
(3) do notcauseincreasing
damagein mixedspeciesinfections;
whereasmixedparasiteinfections
oftenhave interactive
negativeeffects;
(4) usuallyhavemechanisms
toreduceoreliminatemultiple
infections;
whereas
multipleinfections
are commonfeaturesofparasitesystems;
(5) also showreduced
frequencies
ofmixedspeciesinfections;
whereas
suchinfections
are common
amongparasitespecies;
(6) are oftentaxonomically
relatedtotheirhosts;whereasparasitesrarely
closely
are and predators
varyin thisrespect;
(7) are oftenlessthanone orderto a few ordersof magnitudesmaller(byweight)than their
hosts;whereasparasitesare severalto manyordersof magnitudesmaller;and predatorsrange
fromsimilar-sized
toseveralordersofmagnitudelargerthantheirprey;
(8) showstrong
withtheirhosts;whereas
positivesizecorrelations
parasitesshownosizecorrelation
withtheirhosts;and onlyrelatively
small predators
are sometimes
correlated
by size withtheir
prey;
are killedor castratedbyobligatehyperparasitoids
(9) frequently
and hypercastrators;
whereas
parasitesrarelyhave hyperparasites;
(10) sometimes
act as facultativehyperparasitoids
or hypercastrators;
whereasparasitesvery
rarelyact so;
(11) parasitoidsand oftencastrators
mostcommonly
attackveryyounghosts;whereasparasitism
and predationare veryvariablewithrespecttoage of thehost(prey);and
(12) oftencause precocioushostdevelopment;
whereasparasitesrarelyaffecthostmaturation
processes.
Some insectparasitoidscastratetheirhostsbeforekillingthem;somecrustaceans
are ultimately
consumedbytheircastrators.
Parasitoidand castratorsystems
not involvinginsector crustaceanhostsare briefly
reviewed.
These trophicinteractions
may be morewidespreadthan is generallyconsidered.Hydatidcyst
diseaseis regardedas theonlyparasitoidaffliction
ofhumans.
*PresentAddress:Department
ofZoology,University
ofFlorida,Gainesville,Florida32611
129
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130
P
THE QUARTERLY REVIEW OF BIOLOGY
INTRODUCTION
ARASITIC castration
maybe regard-
ed as a specialized mode of predation.
In the general case, each castrator
causes the reproductivedeath of one
and onlyone host.Viewed in thissense,
the population consequences of parasiticcastration may be remarkablyanalogous to those of
the parasitoid insects.Parasitoid insectsundergo their larval development within the eggs,
larvae, pupae, or adults of other insects,almost
invariablyconsuming the host in the process
(see Doutt, 1959, for an excellent review). A
single parasitoid is thus responsible for the
consumptionof one and only one host during
its lifetime.
The role of insect parasitoids in regulating
hostabundance has been demonstratedin many
laboratoryand fieldstudies(Varley,1947; Huffaker and Kennett, 1966; Van den Bosch,
Schlinger,Lagace, and Hall, 1966; and many
others). A minority view holds that insect
parasitoids are of limited importance in the
population regulation of insect hosts (Andrewarthaand Birch, 1954).
The basis of the significantpart played by
the entomophagous parasitoids in the control
ofhostpopulationslies in theefficientsearching
abilityof the parasitoids at low host densities
and in the density-dependentresponse of the
parasitoidsto increasinghostnumbers.If parasitic castratorsof Crustacea operate in a like
manner, then parasiticcastrationis implicated
as an extremelyimportantpart of the system
of population regulationforcrustaceanspecies.
Regulationof crustaceanpopulations by parasitic castrationhas not been studied. Only a
fewhostspecies have been sampled wellenough
to allow accurate densityestimates.In none of
these have the population dynamics of the
parasiticcastratorsand theirhostsbeen studied
concomitantlyto establisha correlationbetween
hostand parasitedensitychanges. Investigation
of density-dependentmechanismsin host-parasite interactionsinvolving parasitic castration
mustawaitaccess to suitablelaboratorysystems.
Unfortunately,the life histories of both the
crustacean hosts and their parasites are sufficientlycomplex not to have permittedroutine
rearing of more than one generation in the
laboratory.
Despite the inadequacy of knowledge regard-
[VOLUME
49
ing the effectof parasitic castration on host
populations,I hypothesizethatifcastratorsare
efficientdensity-dependentpredatorsconsuming one preyper individual,as do insectparasitoids, then there should be many analogous
features evident when parasitic castrators of
crustaceans are compared with insect parasitoids. Some of these parallel featuresare likely
to be of great importance in the biology of
these parasite-host (predator-prey) systems.
The hypothesisthat parasitic castrators may
have an impact on their hosts' populations
comparable to that demonstrated for insect
parasitoidsis testedby the comparison of similaritiesof the two systems(Table 1). The differencesbetween castratorsand parasitoids as
a class of trophicinteractions,when compared
witheithertrueparasites(such as monogeneans,
adult digeneans and cestodes,manynematodes,
most protozoans, or fishcopepods), or predators (such as many insects,vertebrates,prosobranch gastropods, spiders, turbellarians,or
coelenterates)are also indicatedin Table 1. The
parasite-hosttrophicrelationshipbetweenpopulations of larval digeneans and cestodes and
theirintermediatehosts are seen in almost all
respects to be similar to that of either the
castratoror parasitoid systemor both. These
relationshipswillbe analyzed elsewhere (Kuris,
in prep.). One should bear in mind that when
large categories of animals are treated in such
tersefashion,exceptionsto everygeneralization
may be broughtforth.Still,the generalitiesdo
fitthe large majorityof each group of interactions.
COMPARISON OF CRUSTACEAN CASTRATORS, INSECT
PARASITOIDS, TYPICAL PARASITES, AND GENERALIZED
PREDATORS
This section is a documentationand discussion of Table 1. To preventthe vast literature
fromoverwhelminga work of this sort,I have
resorted to the frequentcitationof recent reviewsand monographsforthe ample literature
on insectparasitoids.Exceptional studies,cases
which the reviewer did not seem to endorse,
and cases where my own interpretationof the
work in question disagrees with that of the
reviewerare cited fromthe primaryliterature.
As for the castrationliterature,which has not
been well reviewedand forwhich my generalizationsmayconsequentlybe subjectto question,
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JUNE
1974]
PARASITIC CASTRATORS AND PARASITOIDS
I have provided more abundant citations.Scientificnomenclaturehas been updated in many
places, but I have no pretension of having
satisfieda consensus of modern specialists in
the range of organismsbroughtintothisdiscussion. My use of suprageneric taxa is uneven
and is intended merely to permit readers of
diverse intereststo place unfamiliarorganisms.
The terse comments regarding generalized
predators and typical parasites are my own,
but I regardthemas being widelyheld opinions
if parasitoidsand castratorsare excluded from
those categories.Section numberingbelow follows that of Table 1.
1. Outcomeofa SingleAct
Infectionby one parasitoid almost invariably
resultsin the death of the host (Doutt, 1959).
Parasiticcastrationresults in the reproductive
death of the host. Sometimesa host may outlive
thecastratorand recoverits reproductivecapabilities(Caullery, 1908; Miyashita,1941; Pike,
1960; Kuris, in prep.). Such post-castration
broodsare oftensmallwithregardto size-specific fecunditycurves (Pike, 1960; Kuris, in prep.)
and likely do not have much impact on the
rate of increase of host populations, as Cole
(1954) argues. A single typicalparasite causes
no reduction in host viability;a lone predator
consumes many prey.
2. SummationEffects:MultipleInfectionbya
SingleSpecies
131
simultaneously infected by two species of
parasitoids.Occasionallybothparasitoidsperish
owingto unsuccessfulcompetitionor host overexploitation(Salt, 1961). For parasiticcastrators
no increasein castrationof the hostsis indicated
for mixed species infections(Reverberi, 1943;
review,Veillet, 1945). Mixed species infection
oftypicalparasitesfrequentlycauses an increase
in theireffectsupon the host.
4. Density-Dependent
or Regulatory
Effects
upon
theHost Population
Density-dependencehas been demonstrated
in some cases involvinginsectparasitoids. The
manner of control and its importance have
sometimesbeen contested.I suspect thiseffect
applies likewiseto parasiticcastratorsof Crustacea.
There is insufficient
evidence to permitgeneralization in this matterin respect to typical
parasites; it is likelythat the effectis variable.
Because of the over-dispersion of parasites
withinhost populations, the death of heavily
infected hosts, and the higher reproductive
potential of parasites, the regulation of host
population size is considered to be an essential
featureof parasitismby Crofton(1971) (larval
Acanthocephala are used as examples). AlthoughCrofton(1971) does show how over-dispersed parasite populations will lead to some
host mortality,the percentage of such heavily
infectedhostslikelyto die increasesslowlywith
increases in mean parasite density.This is an
inherent property of approximately negative
binomial host-parasitefrequency distributions
generated by parasitologicallyrealistic factors
(see Crofton,1971). Croftonalso failsto distinguish parasitoids and castrators from typical
parasites. His frequency distributionanalysis
applies only to the latter organisms. Parasites
at low densitiesdo not lower the fitnessof their
hosts. Density-dependence has been demonstratedfor many generalized predators.
Multiple infection (the superparasitismof
entomologists)bymost parasitoidspecies usually does not produce any additive effect in
pathogenicityto the individual host. Rarely,
multipleinfectionresultsin prematuredestructionof the host (Dogiel, Polyanski,and Kheisin,
1962). Multipleinfectionby parasiticcastrators
neither speeds up castration effectsnor produces additional deleterious effects (Veillet,
1945; Hartnoll, 1967; Kuris, in prep.). Multiple
parasitismbygeneralized parasitesis frequently 5. OutcomeofMultiple
(Single-Species)Infections
importantand may lead to a reduction in host
in Respectto theParasite(Predator)
viability.
Multiple infection rarely occurs, and less
often
succeeds among solitaryinsectparasitoids
3. SummationEffects:MixedSpeciesInfections
(Salt, 1961; Force and Messenger, 1964; BurThere are usuallyno additiveaspectsin terms nett,1967; and many others). Usually only one
of host viabilityand pathologywhen hosts are parasitoid adult emerges per infection.Ordi-
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THE QUARTERLY REVIEW OF BIOLOGY
132
[VOLUME 49
TABLE 1
A summarized
comparison
of thebiologicalfeaturesof insectparasitoids,crustaceanparasiticcastrators,
typicalparasites,and generalizedpredators
BIOLOGICAL
FEATURE
1. Outcome of a
single act
INSECT
PARASITOIDS
resultsin death of
the host
2. Summationeffects: usually none
superinfectionby
single species
PARASITIC
CASTRATORS
TYPICAL
PARASITES
resultsin reproduc- no reductionin
tive death of the
host viability
host
always none
GENERALIZED
PREDATORS
a single predator
consumes many
prey
frequentlyimpor- does not apply
tant,leading to a reduction in host
viability
3. Summationeffects: usually none
mixed infections
none indicated
frequent
does not apply
4. Density-dependent demonstratedin
effectson host
many cases
populations
suspected herein
variable
variable,demonstratedin many
cases
5. Superinfectionas it usuallyonly one
affectsparasite
parasitoid emerges
(predator)
(except gregarious
species)
usually rarer than multipleinfections does not apply
expected; often
common
only two parasitic
isopods may mature
per host
6. Outcome of mixed- usually only one
species infections survives;firstto arrive commonlydestroyslater animals
oftenless frequent many mixed infec- does not apply
than expected; in
tions normally
one case the second coexist
arrivalcauses the
death of the first
castrator
7. Densityof parasite at high densities
commonlyverylow variable,often high almost invariably
(predator) relative parasitoid is impli- occasionallyhigh
low
to host
cated as a host population control
agent; low and high
densitiescommon
8. Taxonomic rela12% of all insect
tionshipbetween
species are parasihost (prey) and par- toids of other inasite (predator)
sects; sometimes
host and parasitoid
are in same family
3% of all crustacean veryrare within
species are castra- same phylum
tors of others
crustaceans; a
number of castrators and hosts belong to the same
order, and in one
example, to the
same family
variable
9. Other taxa affect- mermithidnemaing hosts in like
todes, nematomanner
morphs
coccidians,digen- does not apply
ean trematodes,
metacercariae,dinoflagellates,nematomorphs,ellobiopsids, fecampid
turbellarians,fungi,
cestodes
does not apply
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JUNE
PARASITIC CASTRATORS AND PARASITOIDS
1974]
133
TABLE 1 (continued)
BIOLOGICAL
FEATURE
INSECT
PARASITOIDS
PARASITIC
CASTRATORS
TYPICAL
PARASITES
GENERALIZED
PREDATORS
10. Host (prey)
specificity
most are moderately host-specific;
some species with
low or high specificity
typicallyhighlyspe- variable; often
cific;a few have low highlyspecific
or moderate degrees of specificity
variable; oftenvery
unselectivein terms
of prey species
11. Size of mature
parasite (predator)
stage in relationto
size of the mature
host (prey) stage
parasitoid oftenless
than one order of
magnitude smaller
than host
castratoroftenless
than one order of
magnitude smaller
than host
ranges frompredator similarin size to
prey to predator
several orders of
magnitudelarger
than prey
parasite several
orders of magnitude smaller than
host
12. Correlationof size positivecorrelation positivecorrelation
of individual para- demonstrated
demonstrated
site withindividual
host
no correlationex- typicallynot correcept in cases involv-lated; sometimesa
ing intermediate positivecorrelation
hosts
13. Obligate
hyperparasites
frequent;usually
Hymenoptera
rare; Microsporida does not apply
most oftenreported; usually involving intermediate
host of the primary
parasite
14. Facultative
hyperparasites
many cases known a few examples
known
15. Host (prey) age at
infection
usually early in life, many early in life, variable
some intermediate, some restrictedto
few in adult
adults, others
variable
variable
16. Host maturity
parasitoid may induce premature
pupation
does not apply
many reported;
usually Isopoda
veryrare
a few species cause rarelyif ever
host precocityor
effectshost
hyperfeminization maturation
narily,the initial oviposition results in emergence. Subsequent larvae are killed by combat
or are physiologicallysuppressed (Messenger,
1964). Salt (1961) has regarded these happenings as the logical outcome for systemshaving
a fixed food supply (the host). Some species
regularlypermitthe emergence of larvae from
more thanone oviposition(i.e., theyare gregarious) (King and Rafai, 1970). In bothgregarious
and nongregarious species, mechanisms exist
wherebythe frequencyof multiple oviposition
is so stronglyreduced (King and Rafai, 1970)
thatmultipleinfectionis feltto be unimportant
in the fieldpopulationsof solitaryspecies (Force
and Messenger, 1964). In a few well-studied
species multiple infection is unknown (Force
and Messenger, 1964).
does not apply
Multiple infectionsare usually much rarer
than randomlyexpected for most entoniscids,
bopyrids,and sacculinids (Veillet, 1945; Altes,
1962; Hartnoll, 1967; and others) and for a
(Chatton,
dinoflagellate(Blastulidiumcontortum)
1920; Cattley, 1948). The presence of one
parasite prevents concurrentestablishmentof
subsequentinfectivestagesencountered(Giard,
1888). In systems in which more than one
parasite may infecta given host, maturation
is oftenlimitedto onlytwoadults (Shiino, 1942;
Veillet, 1945; Kuris, 1971). At least for the
bopyrids and entoniscids,the upper limit of
two coincides with the maximum number of
sitesbased on the morphologicalconfigurations
of host and parasite. Gregarious species are
known, and include most of the parasitic din-
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134
THE QUARTERLY REVIEW OF BIOLOGY
oflagellates(Chatton, 1920) and some sacculinids (Hartnoll, 1967). Polyembryony,resulting
in the production of many progeny from a
single infection,is a regular featureof the life
cycle of certain chalcid wasps (Askew, 1971)
and some Rhizocephala (Veillet,1945; Hartnoll,
1967; Bocquet-Vedrine and Parent, 1973).
Among typical parasites many examples of
multipleinfectionare known, at least some of
which are due to simultaneous acquisition of
more than one parasite (such as by way of
ingestion of an intermediate host harboring
several intermediateinfectivestages). Multiple
infectionis sometimeslimitedby already established parasites (premunition) or host responses. Polyembryonyoccurs in many helminths(see reviewof parthenogenesisbyCable,
1971). Many of his examples are drawn from
the insect-parasitizingnematodes and larval
digeneans, both of whichare herein implicated
as parasitoidsand castratorsrespectively.
Multiple attack by generalized predators is
rare,but does occur, forexample, among social
Carnivora and Primates.
[VOLUME
49
(Schad, 1963; Petter, 1966) have been described. Sometimes competitiondoes result in
unexpectedlylow frequencies of mixed infections. Mixed-species predator attacks on individual prey organismsrarelyoccur.
7. DensityofParasite(Predator)Relativeto Host
(Prey)
Both very low (less than 2% infected) and
high densities (25-90+%) are commonly recorded (e.g., Price, 1970). Huffaker (1971)
notes that to exert a controllinginfluence on
host populations, the parasitoid must have a
high density relative to its host: Densities of
many castrators of crustaceans are very low
(Bourdon, 1960, 1963, 1964). Occasionally,
both withregard to season (Gifford,1934) and
locality(Veillet,1945; Bourdon, 1963; Hartnoll,
1967; Heath, 1971; Born, pers. commun.) the
percentage of infectionmay range from 25 to
75 per cent. Some populationsof the entoniscid
isopod, Portunionconformis,
in the grapsid crab,
Hemigrapsusoregonensis,
reach infectionlevels
of 92 per cent (Kuris, unpub.). Such castrated
populations are most probably maintained by
6. Outcomeof Mixed-Species
Infectioms
immigrationfromother localities.
(A mixed-speciesinfectionis the symparasitism Typical parasiteshave a wide range of densiof Dogiel, Polyanski,and Kheisin, 1962; the tiesper host.Oftensuch densitiesare farhigher
superparasitism
of Noble and Noble, 1964; the than the densities reached by the majorityof
of entomologists-see Askew, parasitoid and castratorpopulations. Patterns
multiparasitism
1971).
of infectionoftypicalparasiteslead to frequency
Among insectparasitoids,typically(i.e., soli- distributionsof the parasite load that approxitary parasitoids), only one individual of one matenegativebinomialexpansions (Li and Hsu,
species can surviveto emergence. Usually the 1951; Crofton, 1971; Pennycuick, 1971b).
firstto arrive destroysthe subsequent arrivals These result in very high absolute densities of
(Fisher,1962). Rarely,bothmaysurvive,or both parasites in the total population at a given
perish because of host overexploitation(Salt, percentageof infection,in comparisonto either
1961). Mixed infectionsof parasitic castrators castratoror parasitoid populations.
of Crustacea are oftenfound to be less frequent
Generalized predatorsalmostinvariablyhave
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 inAn estimated 12 per cent of all insectspecies
teraction is akin to hyperparasitism.Mixed are parasitoidsof otherinsects(calculated from
infections may also occur randomly (Altes, informationgiven in Askew, 1971). Sometimes
1962).
hymenopterousparasitoids attack species beMany mixed infectionsof typical parasites longing to the same familyof parasitoids.
An estimated 3 per cent of all crustacean
normally coexist. Nematode species flocks
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JUNE
1974]
PARASITIC CASTRATORS AND PARASITOIDS
species are castratorsof other Crustacea (calculated frominformationgivenin Watermanand
Chace, 1960). A number of instancesof castrationwithinthe same order are known(Carayon,
1942; Bocquet-Vedrine, 1961, 1967; Bourdon,
1967) and at least one example withinthe same
family (Caroli, 1946; Catalano and Restivo,
1965).
For both the Insecta and the Crustacea, their
respectiveparasitoid and castratorfaunas are
dominated by species of the same taxonomic
class (see below for exceptions). Possiblythese
taxa are preadapted for this relationship.
Parasitoidsand castratorsare veryfinelyatuned
to theirhosts' life histories.Since key features
of insect life histories,such as diapause and
metamorphosis,are under the controlof endocrinesystems,itseems reasonable to expect that
insect parasitoids can either "read" (e.g.,
Schoonhoven, 1962) or "direct" (e.g., Johnson,
1965) these systems.In like manner, molting
ofbopyridisopods in synchronywiththeirhosts
(Caroli, 1927; Tchernigovtzeff,1960; pers. observ.) and the feminization of male hosts
througheffectson theandrogenicgland (Veillet
and Graf, 1958) probably represent "reading"
and "direction"of crustacean hosts.
Generalized parasites very rarely parasitize
hosts withinthe same phylum.The taxonomic
relationshipbetweengeneralized predatorsand
theirprey is variable.
9. OtherTaxa Affecting
Host in a Like Manner
Manymermithoidand steinernematidnematodes (Welch, 1965) and nematomorphsprobably have a parasitoid effectupon theirorthopteranhosts.For reasons as yetunknown,insects
are very susceptible to one-on-one predation
systems.
Non-crustacean parasitic castrators of
Crustacea include the coccidian Aggregata(see
Smith,1905), digenean trematodemetacercaria
(Noble and Noble, 1964), dinoflagellates(Chatton, 1920; Cattley,1948), Nematomorpha (Perez, 1927; Born, 1967), the enigmatic Ellobiopsidae (Chatton, 1920; Fage, 1940; Wickstead, 1963; Hoffman and Yancey, 1966;
Mauchline, 1966), fecampid turbellarians
(Mouchet, 1931; Baylis, 1949; Christensenand
Kanneworff,1965; Kanneworffand Christensen, 1966), cestode procercoids(Mueller, 1966),
135
and fungi (Johnson,1958). For unknown reasons, crustaceans are subject to castration by
membersof several differenttaxa.
Judgementas to whether many species of
Microsporidabelong in both of the above categories is reserved until relationshipsbetween
the numberof spores involvedin transmission,
reproduction within the host, pathology, and
mortalityare betterunderstood. If the size of
the initial inoculum does not determine the
outcomeof theinfections,thenI would consider
the appropriate species to be parasitoids or
castratorsrather than parasites. Certainly for
some species (Veber and Jasic, 1961) the pathology is dosage-dependent. For similar reasons, most Microsporida and other protozoan
pathogens are omittedfromTables 1 to 3.
I stressthe factthattheseverydiversegroups
of organisms, especially the mermithids,nematomorphs,insectparasitoids,dinoflagellates,
fecampids,copepods, isopods, and rhizocephalans, all share virtuallyevery aspect of the
detailed comparison summarized in Table 1.
The exigencies of the parasitoid-castrator
process seem to force narrow strategiclimitations on parasitoidsand castrators.
10. Host (Prey)Specificity
In the followingdiscussionhigh host specificitymeans one or twocloselyrelated hosts exist;
low host specificitymeans that dozens of hosts
exist,oftenbelonging to separate families.
Insect parasitoidsare moderatelyhost-specific, such specificitybeing primarilybehaviorally
and ecologically determined (Doutt, 1959).
Some species, such as Nasonia vitripennis
(Whiting, 1967), have a low degree of host-specificity.
Parasiticcastratorsare typicallyhighlyhostspecific.Epicaridean isopods are classicallyregarded as strictlyhost-specific(Giard and Bonnier, 1887; Bonnier, 1900), although it is likely
that much of this specificityis ecologically influenced. A few species have a low degree of
in the field; for example, Hehost-specificity
abdominalishas been recorded from
miarthrus
22 hosts (Pike, 1960).
Typical parasites have variable degrees of
but often are highly host-spehost-specificity,
cific. Generalized predators also have varying
but are often very
degrees of prey-specificity,
unselectivein termsof prey species.
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136
THE QUARTERLY REVIEW OF BIOLOGY
11. Size (Weight)oftheMatureParasite
(Predator)Stage in RelationtotheSize of the
MatureHost (Prey)Stage
Insectparasitoidsare fromone to a feworders
of magnitudesmallerthantheirhosts-i.e., they
are of relativelylarge size (Doutt, 1959). Parasiticcastratorshave a similarsize range relative
to their hosts. Typical parasites, in contrast,
are severalto nianyordersof magnitudesmaller
than their hosts. Generalized predators range
in size frombeing about the same size as their
preytobeingseveralordersof magnitudelarger
than theirprey.
12. CorrelationbetweentheSize of theIndividual
Parasite(Predator)and Its Individual Host (Prey)
The parasite-host(predator-prey)size correlation should be envisaged between animals
at a similarstage in life historywhenever discrete stages occur-e.g., only fourth instar
parasitoidlarvae should be compared witheach
other.The strongestcorrelationswillof course
be betweenhostsize and relativelymaturestages
of parasitoid or castrator.In the cases of parasitoids,castrators,and parasites it seems most
reasonable to regard host size as the independent variable. Positivecorrelationsresult from
parallel growth of both members of the interactingpair. For predator-preysystems,the
predator's size is usually regarded as the
independentvariable as size of the preyusually
involves some selection on the part of the
predator.
Positivecorrelationbetweenhostand parasitoid size has been demonstrated(Askew, 1971).
Host and castrator size are likewise typically
positivelycorrelated (Pike, 1960; Allen, 1966;
Samuelsen, 1970; Kuris, 1971; by inference,
Giard and Bonnier, 1887; Morris, 1948). Size
of typicalparasitesis usuallynot correlatedwith
hostsize, except in instancesinvolvingintermediate hosts. Prey are often not correlated with
predator size (e.g. Galbraith,1967; Moran and
Fishelson,1971). When positivecorrelationsdo
occur (for a good example, see Menge, 1972),
the correlationis usually weaker than that seen
in the parasitoid or castratorsystems(compare
with Pike, 1960). Predator-preysystemswith
similarrelativesizes (see Section 11 above) are
those in which individual predator-preysize
correlationsare found.
[VOLUME
49
13. Hyperparasites
(Obligate)
Hyperparasitoidsare frequentlyreported in
insectparasitoid systems.They are usually hymenopterous species. Several examples are
given in Askew (1971). These may play a role
in disruptionof the controlof host populations
by the primaryparasitoids.Hypercastratorsare
known for a number of parasitic castrators.
They are usuallyisopods-for example, liriopsids on sacculinids (Pike, 1961), Cabiropson
Pseudione (Carayon, 1942), Gnomoniscuson
Podascon (Caullery, 1952), and perhaps the
copepod Paranicothoe
found in theemptybrood
pouch of bopyrid isopod hosts (Carton, 1970).
Stromberg,however (pers. commun.), believes
that, in general, the cryptoniscineisopods are
true hyperparasites,not hypercastrators.
Interestingly,
the only previous referenceto
the resemblance between parasitic castrators
and insectparasitoidsseems to be thatof Perez
(1931), whose manycontributionsto crustacean
biology have often been overlooked by later
writers. Working with the hypercastrator,
Liriopsispygmaea,on Peltogaster
paguri, a primary castratorof Eupagurusbernhardus,
Perez
(1931) observed that the observed Peltogaster
population was sterilizedby an epidemic of the
hypercastrator.He noted the similarityof the
phenomenon to the effectof hyperparasitoids
on insectprimaryparasitoids.
Hyperparasitesof typical parasites are very
rare, the most commonly reported being microsporidians (Dissanaike, 1957; Canning and
Basch, 1968). It is significantthat several of
thesemicrosporidiansparasitizelarval stages of
helminthsin the intermediatehost (see below).
in microThe haplosporidian, Urosporidium,
phallid metacercariae (Couch and Newman,
1969) fitsthis pattern.
14. Hyperparasites
(Facultative)
Many hymenopteransare known to be either
primaryparasitoids or hyperparasitoids.Some
species, upon completion of a hyperparasitic
phase resultingin thedestructionof the original
primaryparasitoid,completetheirdevelopment
as parasitoids of the original host (e.g., Price,
1970). In some arrhenotokousprimaryparasitic
species, larval males, only, develop as
hyperparasites,often conspecifically.Females,
however, are only primary parasites (Doutt,
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JUNE
1974]
PARASITIC CASTRATORS AND PARASITOIDS
1959; Kennett,Huffaker,and Finney, 1966).
A fewexamples of facultativehypercastration
are known.Caroli (1946) reportsthatthe young
bopyridPseudioneeuxinicaspends the earlypart
of itslifeon the bopyrid Gygebranchialis.Upon
thedeath of Gyge,P. euxinicabecomes a primary
parasite of the host, Upogebia littoralis.The
gradual destructionof a previously infecting
sacculinidbyentoniscids,coupled withthe nonrandom prevalenceof mixed infectionsof these
species (Veillet, 1945; Miyashita, 1941) lends
thissituationsome of the qualities of facultative
hyperparasitism.Altes (1962) feels that Cryptoniscuspaguri,a hypercastratorof Septosaccus
rodriquezi,
may sometimesbe a parasite of the
primaryhost,Clibanariuserythropus.
The dwarf,
hyperparasiticmales that typicallyaccompany
female Epicaridea do not merit consideration
here because there is no evidence that they
harm the female. In fact, they may not feed
at all. No examples of facultativehyperparasites
are known,but the apparent ingestionof some
protozoan parasites by digenetic trematodes
(Dogiel, Polyanski,and Kheisin, 1962), may be
judged as rare, comparable examples.
137
16. Host Maturity
Several insect parasitoids have been noted
to induce premature pupation in their insect
hosts (Varley and Butler, 1933). Among parasiticcastrators,Cryfitoniscus
pagurusmay cause
precocious developmentof infestedSeptosaccus
rodriquezi(Altes, 1962). Reinhard (1956) notes
thathyperfeminization,
theappearance of adult
characteristicson small female hosts, is an
oft-reportedeffectof sacculinization. Typical
parasites rarely,if ever, cause precocious host
maturity.
CASTRATORS OF INSECTS, PARASITOIDS
OF CRUSTACEA
The functionalsimilarityof parasitoid and
castratorsystemson theirinsectand crustacean
host populations is further suggested by an
interestingturnabout.Some insect species are
subject to parasitic castration prior to their
parasitoid-induceddeath (Table 2), and some
crustaceansare essentiallyconsumed by organisms which were initially merely castrators
(Table 3).
Inspection of Table 2 shows that for most
castrator-insect
host systems,the cessation of
15. Age ofHost at Time ofInfection
reproductiveactivityis 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 nemestrinidparasitoids are known. Pupal parasitoids are orthopteransystem,the outcome of the paracommon, but adult-infectingparasitoids are site-hostinteractionis variable; sometimes the
infrequent (Doutt, 1959). Salt (1968) has host survives, sometimes it does not. Some
proposed that invasion of young hosts leads tylenchoidnematodesand mostStrepsipteraare
to the acquisition of the proper surface "im- close to nonlethalcastrators,the host's lifespan
munologicalpassport."Infectingyounganimals rarely being shortened. As the crustacean
gives the parasitoid time to act as a chronic castratorscontrolthehost'sreproductivesystem
throughthehost'sendocrinesystem(Veilletand
destructor.
Amongparasiticcastrators,mostbopyridsare Graf,1958), so does theaphelenchoid nematode
consideredto attackonlyyounghosts(Carayon, parasite of Bombus,Sphaerulariabombi,by caus1943; 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 castralinidsalso seem to settlepreferentially
on juve- tors,a single Sphaerulariaelicitsthe full castranile hosts (Veillet, 1945). The time of infection tionresponse, 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
porttheoryis held to be applicable to castrators, parasitoid-likeaction (Table 3), also provides
some insight.Like the vast majorityof insect
too.
a fecampidturbellarian,
Typical parasites and generalized predators parasitoids,Kronborgia,
vary greatlywith regard to the phase of the killsitshostupon emergenceof the adult worm.
life historyof the host attacked.
AlthoughKanneworff(1965) demonstratesthat
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THE QUARTERLY REVIEW OF BIOLOGY
138
the castrationeffectis of greater importance,
this is, in part, a parasitoid-hostrelationship.
The terrestrialsuccess of the oniscoid isopods
undoubtedlyexposed them to infectionby the
[VOLUME
49
parasitoidinsects.Examination of other terrestrial and semiterrestrialcrustacean taxa may
wellprovidemoreexamples ofinsectparasitoids
that affectcrustaceans.
TABLE 2
on theirinsecthosts
Some organisms
havinga castrator
effect
CASTRATOR(S)
Cestoda
Dilepidids
Nematoda
Mermithids
Mermithids
Many tylenchoidsand
aphelenchoids
Heterotylenchus
pavlovskii(tylenchoid)
Nematomorpha
Insecta
Strepsiptera
Hymenoptera
some braconids
Diptera
nemestrinids,some
calliphoridsand
muscids
REMARKS
HOST(S)
REFERENCE
ants
castrate;many morphologicaleffects;behave as social parasites;
superinfectionmay cause an
additive response
Plateaux, 1972
ants
chironomids,
simuliids,others
intercastes
intersexes;gonads affected;kill
upon emergence
Welch, 1965
Welch, 1965
Coleoptera, Lepidoptera, Diptera,
Hymenoptera
fleas
reduce fecundity;rarelykill
Welch, 1965
castrates;killson emergence
Welch, 1965
Orthoptera
castrates;killson emergence
Dorier, 1965
Hymenoptera,
Hemiptera, some
Thysanura,
Orthoptera
castrates;usually doesn't kill
hosts; males feminized,females
masculinized
Askew, 1971
weevils
castrates;killson emergence
Loan and Holdaway,
1961
Acridoidea
usually castratesbefore killingon
emergence; some only reduce
fecundity;lethal
Greathead, 1963
TABLE 3
on theircrustaceanhosts
Organismshavinga parasitoideffect
PARASITOID(S)
HOST(S)
Fungus
Metschnikowia
(yeast)
REMARKS
REFERENCE
Copepoda, Cladocera, Artemia
causes host's death
Fize, Manier, and
Maurand, 1970
Turbellaria
Kronborgiaamphipodicola
Ampeliscamacrocephala
castrationprecedes death
upon emergence
Christensenand
Kanneworff,1965
Diptera
Tachinidae
terrestrialisopods
typicalparasitoid effect
Askew, 1971
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JUNE
PARASITIC CASTRATORS AND PARASITOIDS
1974]
139
TABLE 4
Parasitoid-like
phenomenainvolvinghostsotherthancrustaceans
and insects
PARASITOID
HOST(S)
Microsporida
Pleistophora
Pereziaeurytremae
Haplosporida
Urosporidum
crescens
TrematodaDigenea
hyperparasitoidof metacercariae
in Callinectes
Couch and Newman,
1969
hydatidcystsin intermediate
hosts resultingfromsingle infections typicallyreduce host
viability
Rausch and Schiller,
1956; Schiller, 1966
reproduces withinhost; causes
some castrationeffectsbefore
killinghost
Chernin, 1962
castratehost before killingupon
emergence
Dorier, 1965; Sahli,
1972
medusa graduallyconsumed
Martinand Brinkmann, 1963
Nematoda
Daubaylia
Mollusca
freshwaterpulmonates
Nematomorpha
Arthropoda
millipedes,
centipedes,
whip-scorpions
MolluscaOpisthobranchia
Phyllirhoe
CoelenterataHydrozoa
Zanclea
Cephalopyge
Nanomia
Diptera
tachinids
phorids
sciomyzids
Acarina
Histiotomamurchiei
REFERENCE
Canning and Basch,
1968
Platyhelminthes-Cestoda Mammalia
Echinococcus
humans, voles,
sheep, and
other herbivores
Hymenoptera
REMARKS
Nematoda
Metoncholaimus host, marine; infectionalways
scissus
terminal;authors suggest Microsporida-nematodeinfections
are more common than previously expected
Trematodahyperparasitoidof larvae in snails
Digenea
Hopper, Meyers,and
Cefalu, 1970
probablysimilarto Phyllirhoe,
but Sentz-Braconnotand
may possiblyconsume more than Carre, 1966
one host to complete development
Arthropoda
ticks,mites,
spiders,
pseudoscorpions
typicalparasitoid process
Askew, 1971
centipedes
millipedes
Mollusca
freshwaterand
terrestrial
typicalparasitoid process
uncertain
Askew, 1971
Picard, 1930
Annelida
earthworm
many species are predators,some Berg, 1964; Bratt,
are typicalparasitoids; suggested Knutson, Foote, and
as biocontrolagents
Berg, 1969
an egg parasitoid
Oliver, 1962
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THE QUARTERLY REVIEW OF BIOLOGY
140
[VOLUME 49
TABLE 5
Parasiticcastration-like
phenomenainvolvinghostsotherthancrustaceans
or insects
CASTRATOR
HOST(S)
Sporozoa
Mackinnoniatubificis
Microsporida
Nosemafrenzelinae
Pleistophora
ovariae
Haplosporida
charletti
Urosporidium
Cestoda
Catenotaenia
dendritica
Ciliatea
EchinodermataAsteroidea
Asteriasrubens
stellarum
Orchitophrya
Mesozoa
Orthonectida
REMARKS
AnnelidaOligochaeta
Tubifextubifex destroysgonad
Sporozoa-Gregarinia
Frenzelinaconpreventssporogonyaftersyzygy;
formis
pre-reproductivegrowthnormal
Pisces-Cyprinidae
Notemigonus
partial castration;possibly
crysoleucas
enhances somatic growth
Echinodermata
Ophiuroida
CoelenterataHydrozoa
Peachia quinquecapitata
Phialidium
REFERENCE
Janiszewska,1967
Leger and Dubosq,
1909
Summerfeltand
Warner, 1970
hypercastrator
Dollfus, 1943
mostlyin male hosts; may only
be partial castration;possible
role in population control
Vevers, 1951
typicallyrender host gonads
nonfunctional
Giard, 1888; Caullery
and Lavallee, 1912;
Fontaine, 1968
Coelenterata-Anthozoa
Turbellaria
Oikiocolax
plagiostomorum
Trematoda-Digenea
most sporocystand
redial stages
Bucephatusmytili
sporocysts
gymnophalinemetacercariae
a temporarycastrator,sometimes Spaulding, 1972
a parasitoid; ectoparasitic,feeding on gonads of medusa; host
may die afteranemone leaves;
gonads can regenerate
Turbellaria
Plagiostomum
sp.
Reisinger, 1930 (from
Jennings,1971)
Gastropoda
acute castrationappears to be the
rule; sometimessecondarysexual
characteristicsaffectedand behavioral changes; prolonged life
or gigantismsuggested for some
infections;sometimesreduce host
viability;mixed species infections
rare-one species eliminates
competitoreither indirectlyor
throughdirect predation
Rothschild,1941;
Wright,1966; K0ie,
1969; Lim and Heyneman, 1972; Kuris,
1973.
Bivalvia
destroysgonad, infected
hosts larger
Breton, 1970
sometimesgonad destroyed
Paine, 1963
Brachiopoda
Glottidiapyramidata
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JUNE
1974]
PARASITIC CASTRATORS AND PARASITOIDS
141
TABLE 5 (continued)
CASTRATOR
HOST(S)
Cestoda
pseudophyllidpleroceroids
Pisces
Cyprinidae,
Gasterosteus
Nematoda
Mammanidula
asperocutis
Mammalia
Sorex
Annelida
Myzostomida
Echinodermata
Crinoidea
Mollusca-Gastropoda
Entoconchamirabilis
Holothuroidea
Crustacea-Copepoda
monstrilloids
Xenocoeloma
Annelida
Syllidae
Polycirrus
Mytilicola
Sarcotretes
scopeli
Crustacea-Cirripedia
Ascothoracica
Anelasmasqualicola
Bivalvia
Mytilus
Pisces
Myctophidae
Echinodermata
Echinoidea, Asteroidea
Pisces-Elasmobranchia
Etmopterus
spinax
REMARKS
destroygonad; may reduce
host viability;causes many
behavioral changes
REFERENCE
Arme and Owen, 1967;
Arme, 1968; Pennycuick, 1971a
infectlactatingmammaries,pre- Okhotina and
vent nursing; high infectionrates Nadtochy, 1970
accompany high host density
suggestingrole in population
regulation; a castratorin the
sense that it eliminateshost's
reproductivecapabilities
some species cause partial
castration
Prenant, 1959
Giard, 1888
fecundityreduced
gonad reduction
Malaquin, 1901;
Boquet, BoquetVedrine, and
l'Hardy, 1968
Mann, 1967
preventsgonadal maturity;no
Gj0saeter, 1971
effecton secondarysexual characters; parasitizedanimals slightly smaller than theirage class
destroysor greatlyreduces
gonads
Brattstr6m,1936;
Achituv, 1970
hosts ovaries become inactive,
testesprobablyfunctional;
increased mortalityof
parasitized sharks
Hickling, 1963
Crustacea-Brachyura
Pinnotheres
Bivalvia
castrationand even sex reversal
Hornell and Southwell,
of infectedhosts; female crab size 1909; Awati and Rai,
correlatedwithhost size
1931; Atkins,1926;
Berner, 1952
Pisces
Jordanicus
Holothuroidea
eats gonads; extentand permanence of effectsuncertain
Trott, 1970
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142
THE QUARTERLY REVIEW OF BIOLOGY
PARASITOID AND CASTRATOR SYSTEMS IN THE ANIMAL
KINGDOM
Even withthe exclusion of larval trematodes,
cestodes,and acanthocepthalans(to be covered
in detail in Kuris, in prep.), parasitoid systems
(Table 4) and castrator systems (Table 5)
operate on a surprisinglydiverse list of host
systems.
Parasitoids of non-insects are very poorly
known, excepting the detailed studies on the
Sciomyzidae by Berg (1964) and coworkers.
Mostoftheinteractionsplaced in Table 4 should
be regarded as tentative.Of interestagain, the
specialized hymenopterous and dipterous
parasitoids have invaded most non-insectterrestrialarthropod taxa. Again, the inclusion of
protozoan infectionsin thislistis speculative.
Castration effectsseem to occur more frequently and in a greater taxonomic diversity
of systemsthan do parasitoid effects.Table 5
providesa listof castratorsrangingfromProtozoa to Brachyuraand Gastropoda,a listof hosts
from Protozoa to Mammalia. Orchitophyra
in
Asteriasand Mammanidulain Sorexhave both
been suggestedas being involvedin host population control (Vevers, 1951; Okhotina and
Nadtochy,1970). Indeed, the mammarynematode infection rate appears to be densitydependent.
Larval trematodescommonlycastrate(Kuris,
1973) and sometimeskill(Sturrockand Webbe,
1971) their snail hosts. The snail-trematode
trophicinteractionsatisfiesmostof the biological featuresof parasitoid and castratorsystems
given in Table 1. The similarityof snail-trematode to insect pest-parasitoidtrophic interactionshas already been proposed (Kuris, 1973).
Consequences ofmixedspecieslarvaltrematode
infections(see reviewsby Lim and Heyneman,
1972; Lie, 1973) are much like mixed parasitoid
infections.Biological controlof schistosomiasis
through competitiveexclusion by trematodes
withredial generationsis theoreticallyfeasible
(Kuris, 1973).
In some cases parasitic castration has been
shown to be accompanied by prolonged life
or gigantismofthehost,or byboth.This curious
parasite-induced syndrome-castration, prolonged life, and gigantism-occurs in snails
harboring certain larval trematodes (Rothschild, 1941), in male pea crabs infected with
Pinnotherion
(Mercierand Poisson, 1929), possi-
[VOLUME
49
bly in minnows castrated by Microsporida
(Summerfeltand Warner, 1970) and pelagic
copepods castrated by Blastulidiumcontortum
(Cattley,1948; but not Chatton, 1920). If the
"replacement" of the ovary by the parasite
results in an energeticallyless expensive total
system,as is suggestedby data on Hemigrapsus
oregonensiscastrated by Portunion conformis
(Kuris and Lawlor, in prep.) then gigantism
or increased survivorshipof parasitized hosts,
or both,should not be unexpected. Summerfelt
and Warner (1970) also take this viewpoint.
If a castratorhas a positive effecton its host's
viabilityor growth (or both), the increased
production of castrator offspringbecause of
prolongedlifeand the stronglyhostsize-specific
fecundityschedules of many of the castrators
would seem to be strongselectivefactorsfavoring the castrationpathology.Rothschild(1938)
recognizedthe selectiveadvantage of large snail
size to cercarialproduction.Castratorsof intermediate hosts,where the transmissioninvolves
ingestion of that host by the definitivehost,
would not be expected to energetically"conserve" intermediatehosts. Walkeyand Meakin
(1970) indicate that larval Schistocephalus
are
quite costlyto theirsticklebackhosts.
Argumentsraised concerningthe loss of the
host's progeny to future parasite generations
tacitlyand unnecessarilyinvokegroup selection.
Mechanisms to reduce pathological effects
characterizethose parasites for which the pathologydoes not improvethe survivalor reproductive success of the parasiteson hand.
Drastic modificationsin host behavior sometimes accompany parasitizationby parasitoids
and castrators. Braconid parasitoids prevent
diapause in some insect hosts (Varley and
Butler, 1933). Sacculinized Carcinusbehave as
reproductive females, migrating to shallow
waterand showingegg-carebehavior (Rasmussen, 1959). Ants harboring dicrocoelid tapeworm larvae act as social parasites,always requestingfood fromunparasitizedworkers(Plateaux, 1972). Sticklebackscarrying advanced
cestodeplerocercoidsswimnear thesurfaceand
are thus easy prey for bi&ds(Arme and Owen,
1967). Poinar and van der Laan (1972) show
that infected queen bumblebee "eternal
seekers" do not complete their hibernation
flight,but continueto flylow over the ground,
stoppingbrieflyto dig littlepits in the soil and
release Sphaerulariainfectivelarvae. The classic
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JUNE
1974]
PARASITIC CASTRATORS AND PARASITOIDS
143
host behavioral modificationis caused by the significant.In these parasitized populations,
sporocystof Leucochlori&ium,
a brightlycolored prevention of reproduction in early breeding
active form in snail tentacles-essentially a periods has a more suppressiveeffecton popusemaphore systemto attractbirds-the defini- lationthandoes the preventionof reproduction
tivehosts(Noble and Noble, 1964). In the latter (by death) in laterperiods.
In brief, on the basis of the sharp resemthree cases the host becomes littlemore than
a parasitoid-guided missile system,operating blances betweenparasiticcastratorsand parasitto complete the life cycle of the parasitoid in oids outlined above, I conclude that castration
act. Such gross modifications phenomena may be importantcomponents of
a self-destructive
of host behavior rarelyoccur under the influ- population regulationsystemsformanymarine
ence of true parasites.
organisms. Malacostracan Crustacea are conA few interactingsystemscombine parasitic sidered to be particularlysubjectto such castracastration with the shortened host life span tion systems. Parasitic crustaceans are often
characteristicof parasitoids.The fecampid tur- discovered to exert a castrationeffecton their
causes such effectson its hosts,crustacean or otherwise.
bellarian, Kronborgia,
Further elucidation of the role of parasitic
amphipod host (Kanneworff, 1965). Gordiaceans and mermithid nematodes also cause castratorsin the regulationof crustacean host
castration;death of the host followsupon the populations must await long-termdensitysamemergence of the parasite (Dorier, 1965; The- pling programs for both host and castrator
odorides, 1965). The bizarre relationship be- populations, or the domesticationof suitable
tween the parasiticbarnacle, Anelasma,and its laboratory systems.The comparative analysis
deep-sea shark host Etmopterus
seems also to assembledhere suggeststhatthe regulatoryrole
be of thisnature. Hickling(1963) makes a good of castratorsmay be considerable.
case fortheprematuredemise of the parasitized
host. The nematode Daubaylia produces some
castrationeffectspriorto overwhelmingitssnail
ACKNOWLEDGEMENTS
host (Chernin, 1962). Possible differentialmorI thank Cadet H. Hand, John E. Simmons,
tality of parasitically castrated hosts is also
suggested in the data of Gj0saeter (1971) for WilliamE. Hamner, Donald Heyneman, Mario
myctophidsinfectedby thecopepod, Sarcotretes. Baudouin, John Vandermeer, Daniel Janzen,
In agreement with Kanneworff (1965), I Stephen Hubbell, and especially Carl B. Hufregard castrationof the host as having a more fakerforcriticalreviewof thismanuscript.John
importanteffecton 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 reproductiveeffortwould be postdoctoralfellowships.
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ALTES,J. 1962. Sur quelques parasiteset hyperparasitesde Clibanariuserythropus
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ACHITUV,
C. 1968. Effectsof the plerocercoid larva of
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