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
Accessed: 10-06-2015 23:11 UTC
Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at http://www.jstor.org/page/
info/about/policies/terms.jsp
JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content
in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship.
For more information about JSTOR, please contact [email protected].
The University of Chicago Press is collaborating with JSTOR to digitize, preserve and extend access to The Quarterly Review
of Biology.
http://www.jstor.org
This content downloaded from 128.111.90.61 on Wed, 10 Jun 2015 23:11:30 UTC
All use subject to JSTOR Terms and Conditions
TROPHIC INTERACTIONS: SIMILARITY OF PARASITIC
CASTRATORS TO PARASITOIDS
BY ARMAND M.
KURIS*
ZoologyDepartment,
University
of California,Berkeley,
and Bodega Marine Laboratory,
Bodega Bay, California
ABSTRACr
An analysisof life 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
This content downloaded from 128.111.90.61 on Wed, 10 Jun 2015 23:11:30 UTC
All use subject to JSTOR Terms and Conditions
130
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,
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
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-
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
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
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
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-
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
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
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
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.
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
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,
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
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
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
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
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
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
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
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
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
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
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
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
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 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.
LIST OF LITERATURE
Y. 1970. Studies on the reproduction and
distributionof AsterinaburtoniGray and A. wega
Perrier (Asteroidea) in the Red Sea and the
eastern Mediterranean. Israel J. Zool., 18: 329342.
ALLEN, J. A. 1966. Notes on the relationshipof the
bopyrid parasite Hemiarthrusabdominalis(Kr0yer) withits hosts. Crustaceana,10: 1-6.
ALTES,J. 1962. Sur quelques parasiteset hyperparasitesde Clibanariuserythropus
(Latreille)en Corse.
Bull. Soc. Zool. France.,87: 88-97.
ANDREWARTHA, H. G., and L. C. BIRCH. 1954. The
Distributionand Abundance of Animals. Univ.
Chicago Press, Chicago.
ACHITUV,
C. 1968. Effectsof the plerocercoid larva of
a pseudophyllidean cestode, Ligula intestinalis,
on the pituitarygland and gonads of its host.
Biol. Bull., 134: 15-25.
ARME, C., and R. W. OWEN. 1967. Infectionsof the
aculeatusL.,
three-spinedstickleback,Gasterosteus
with the plerocercoid larvae of Schistocephalus
solidus(Muller, 1776), with special reference to
pathologicaleffects.Parasitology,
57: 301-314.
and __.
1968. Occurrence and pathology of
__,
Ligula intestinalis
infectionsin British fishes. J.
Parasitol.,54: 272-280.
R. R. 1971. ParasiticInsects.AmericanElsevier,
AsKuEw,
New York.
ARME,
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
144
THE QUARTERLY REVIEW OF BIOLOGY
ATKINS, D. 1926. The moulting stages of the pea
[VOLUME
49
BRETON, G. 1970. Une epizootie 'a larvesde Bucephalus
crab (Pinnotheres
pisum).J. Mar. Biol. Assoc.U.K.,
mytiliCole, affectantles populations naturelles
14: 475-493.
et cultivees de MytilusedulisL. de la region de
AWATI,P. R., and H. S. RAI. 1931. Ostrea cucullata.
Coutances (Manche). ComptesRend. Acad. Sci.
Imd.Zool. Mem.,3: 1-107.
(Paris), 271: 1049-1052.
BAYLIS, H. A. 1949. Fecampiaspiralis,a cocoon-form- BURNETT, T. 1967. Aspectsof the interactionbetween
ing parasiteof the antarcticisopod Serolisschytiei.
a chalcid parasite and its aleurodid host. Can.
Proc.Linn. Soc. London,161: 64-71.
J. Zool.,45: 539-578.
BERG,C. 0. 1964. Snail controlin trematode diseases:
CABLE, R. M. 1971. Parthenogenesisin parasitichelthepossiblevalue ofsciomyzidlarvae,snail-killing
minths.Am. Zool., 11: 267-272.
Diptera. Adv. Parasitol.,2: 259-309.
CANNING, E. U., and P. F. BASCH.1968. Perezia helBERNER,L. 1952. Biologie de Pinnotheres
pisumPenn.
minthorum
sp. nov., a microspordianhyperpara(Decapode, Brachyoure). Bull. Soc. Zool. France,
site of trematode larvae from Malaysian snails.
77: 344-349.
Parasitology,
58: 341-348.
BocQuET,C., J.BOCQUET-VEDRINE,and J.-P. L'HARDY. CARAYON, J. 1942. Sur les Epicarides du Bassin
1968. Analysedes rapportsdu copepode parasite
d'Arcachon (I re note). Bull. Soc. Zool. France,67:
Xenocoelomaalleni (Brumpt) et de son hote Poly174-180.
cirruscaliendrumClapariede. Cah. Biol. Mar., 9:
.-1943. Sur les Epicarides du Bassin d'Arcachon
256-296.
(2e note). Bull. Soc. Zool. France,68: 43-48.
BocQuET-VLDRINE, J. 1961. Monographie de Chthama- CAROLL, E. 1927. La muta nei Caridei infestatide
lophilusdelageiJ. Boc.-Wd., Rhizocephale paraBopiridi. R.C. Ass. UnioneZool. Ital., 15: 70-72.
sitede Chthamalusstellatus
.- 1946. Un bopyride parassita di altro bopyride.
(Pol.). Cah. Biol. Mar.,
2: 455-593.
Pubbl.Staz. Zool. Napoli, 20: 61-65.
. 1967. Un nouveau Rhizocephale parasite de
CARTON, Y. 1970. Le genre Paranicothoe,
un nouveau
Cirripede: Microgasterbalani n. gen., n. sp.
representantde la famille des Nicothoidae. J.
ComptesRend.Acad. Sci. (Paris),265: 1630-1632.
Parasitol.,56(4) Sect. 11(1): 47-48.
BOCQUET-VkDRINE,J.,and J.PARENT. 1973. Le parasiCATALANO, N., and F. RESTIVO. 1965. Ulteriorinotizie
tisme multiple du cirripede opercule Balanus
sulla Pseudioneeuxinicaparassita di UpogebialitimprovisusDarwin par le Rhizocephale Boschtoralis,a Napoli. Pubbl. Staz. Zool. Napoli, 34:
maella balani (J. Bocquet-V6drine). Arch. Zool.
203-210.
CATTLEY, J.G. 1948. Sex-reversalin copepods. Nature,
Exp. Gin., 113: 239-244.
BONNIER, J. 1900. Les Bopyridae. Trav. Sta. Zool.
161: 937.
8: 1-396.
Wimereux,
CAULLERY, M. 1908. Recherches sur les Liriopsidae,
BORN, J. W. 1967. Palaemonetesvulgaris(Crustacea,
Epicarides cryptonisciensparasites des RhizoceDecapoda) as host for the juvenile stage of
phales. Mittr.Zool. Stat.Neapel., 18: 583-643.
Nectonemagracile(Nematomorpha). J. Parasitol., _
- 1952. Parasitismand Symbiosis.
Trans. by A. M.
53: 793-794.
Lysaght.Sidgwickand Jackson,London.
BOURDON, R. 1960. Rhizocephales et Isopodes paraCAULLERY, M., and A. LAVALLEE. 1912. Recherches
sites des Decapodes marcheurs de la Baie de
surle cycleevolutifdes Orthonectides.Les phases
Quiberon. Bull. Soc. Sci. Nancy,19: 134-153.
initiales dans l'infection experimentale de
. 1963. Epicarides et Rhizocephales de Roscoff.
l'Ophiure, Amphiura squamata par Rhopalura
Cah. Biol. Mar., 4: 415-434.
ophiocomaeGiard. Bull. Sci. France Belg., 46:
. 1964. Epicarides et Rhizocephales du Bassin
139-171.
d'Arcachon. Proc.-Verb.
Soc. Linn. Bordeaux,101:
CHArrON, E. 1920. Les Pieridiniensparasites. Mor51-65.
phologie, reproduction, ethologie. Arch. Zool.
. 1967. Sur quelques nouvelles especes de CaExp. Gin., 59: 1-475.
biropsidae (Isopoda, Epicaridea). Bull. Mus. Nat. CHERNIN, E. 1962. The unusual life-history
of DaubayHist. Natur.,38: 846-868.
lia potomaca (Nematoda, Cephalobidae) in
BRATr, A. D., L. V. KNUTSON, B. A. FOOTE, and C.
Australorbis
glabratusand in certain other fresh0. BERG. 1969. Biology of Pherbellia(Diptera:
water snails. Parasitology,
52: 459-481.
Sciomyzidae). Mem.CornellUniv.Agric.Exp. Sta., CHRISTENSEN, A. M., and B. KANNEWORFF. 1965. Life
404: 1-246.
historyand biology of Kronborgiaamphipodicola
BRATTSTROM,H. 1936. Ulophysemaorisundenseeine
Christensenand Kanneworff(Turbellaria, Neorneue Artder Ordnung Cirripedia Ascothoracica.
habdocoela). Ophelia,2: 237-252.
Ark.Zool.,28: 1-10.
COLE, L. C. 1954. The population consequences of
. 1937. On the genus Ulophysema
Brattstr6mwith
life historyphenomena. Quart. Rev. Biol., 29:
a descriptionof a new species fromEast Green103-137.
land. Meddel.om Grdnland,118(7): 1-23.
COUCH, J. A., and M. W. NEWMAN. 1969. Role of
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
145
a hyperparasite(Urosporidium)in the dispersal HATFINGEN, R. 1956. Beitrage zur Biologie von
of microphallidmetacercariafromthe blue crab.
SphaerulariabombiLeon Dufour (1837). Zentr.
J. Parasitol.,55 suppl.: 54.
Bakt. Parasitenk.Abt. II, 109: 236-249.
CROFTON,H. D. 1971. A quantitative approach to HARTNOLL, R. G. 1967. The effects of sacculinid
parasitism.Parasitology,
62: 179-193.
parasites on two Jamaican crabs. J. Linn. Soc.
DISSANAIKE,
A. S. 1957. Protozoa hyperparasiticin
London(Zool.), 46: 275-296.
helminths with some observations on Nosema HEATH, J. R. 1971. Seasonal changes in a population
helminthorum
Moniez, 1887. J. Helminth.,31:
of Sacculina carcini Thompson (Crustacea:
47-64.
Rhizocephala) in Scotland.J.Exp.Mar. Biol. Ecol.,
DOGIEL,V. A., Yu. I. POLYANSKI,
6: 15-22.
and E. M. KHEISIN.
1962. GeneralParasitology.
Trans. by Z. Kabata, HICKLING, C. F. 1963. On a small deep-sea shark
1964. Oliver and Boyd, Edinburgh.
Etmopterus
spinax L., and its cirripede parasite
DOLLFUS, R. PH. 1943. Hyperparasitismeet castration
Anelasmasqualicola(Loven). J. Linn. Soc. London
parasitaire par une Sporozoaire chez une Ces(Zool.),45: 17-24.
tode. ComptesRend. Acad. Sci. (Paris), 217: 270HOFFMAN, E. G., and R. M. YANCEY. 1966. Ellobiopsi272.
dae of Alaskan coastal waters. Pacific Sci., 20:
A. 1965. Classe des Gordiaces. In P. -P. Grasse
DORIER,
70-78.
(ed.), Traite de Zoologie: Anatomie,Systematique, HOPPER, B. E., S. P. MEYEIRS, and R. CEFALU. 1970.
Biologie, IV(3) [Nimathelminthes(N6mathodes,
Microsporidianinfectionof a marine nematode
Gordiaces)Rotifires,Gastrotriches,
scissus.J. Invert.Pathol.,16: 371Metoncholaimus
Kinorhynques],
p. 1201-1222. Masson, Paris.
377.
DouTr, R. L. 1959. The biologyof parasiticHymen- HORNELL, J.,and T. SOUTHWELL. 1909. Description
optera. Ann. Rev. Entomol.,4: 161-182.
of a new species of Pinnoteresfrom Placuna
FAGE,L. 1940. Sur le determinismedes caractieres
placenta.In A Reportto theGovernment
of Baroda
sexuels secondaires des Lophogastrides (Cruson theMarineZoologyofOkhamandalin Kattiawar,
Pt. 1, pp. 99-102. London.
taces-Mysidaces).Comptes
Rend.Acad. Sci. (Paris),
HUFFAKER, C. B. 1971. The phenomenon of predation
211: 335-337.
FISHER,R. C. 1962. The effectof multiparasitismon
and its roles in nature. In P. J. den Boer, and
G. R. Gradwell (eds.), Dynamicsof Populations,
populations of two parasites and their host.
Ecology,43: 314-316.
p. 327-343. Centre forAgriculturalPublications
FIZE, A., J. -F. MANIER, and J. MAURAND. 1970. Sur
and Documentations,Wageningen.
un cas d'infestationdu Copepode Eurytemora
velox HUFFAKER, C. B., and C. E. KENNET-1. 1966. Some
(Lillj.) par une levure du genre Metschnikowia
aspects of assessing the efficiencyof natural
(Kamienski). Ann. Paras. Hum. Comp.,45: 357enemies. Can. Entomol.,101: 425-447.
363.
JANISZEWSKA,J. 1967. Mackinnonia
tubificisJaniszewska
FONTAINE, A. R. 1968. A new ophiuroid host for
1963 (Coccidiomorpha) fromthe body cavityof
Rhopalura ophiocomae Giard (Orthonectida:
Tubifextubifex
(Muell.). Zool. Polon.,17: 241-257.
Mesozoa). J. Parasitol.,54: 1251-1252.
JENNINGS, J. B. 1971. Parasitismand commensalism
FORCE, D. C., and P. S. MESSENGER. 1964. Fecundity,
in the Turbellaria. Adv. Parasitol.,9: 1-32.
reproductive rate, and innate capacity for in- JOHNSON, B. 1965. Premature breakdown of the
crease of three parasitiesof Therioaphismaculata
prothoracicglands in parasitizedaphids. Nature,
(Buckton). Ecology,45: 706-715.
206: 958-959.
GALBRAITH, M. G. 1967. Size-selectivepredation on
JOHNSON, T. W. 1958. A fungus parasite in ova of
Daphnia by rainbow trout and yellow perch.
the barnacle Chthamalusfragilisdenticulata.Biol.
Trans. Am. Fish. Soc., 96: 1-10.
Bull., 114: 205-214.
GIARD, A. 1888. La castration parasitaire, nouvelles
KANNEWORFF, B., and A. M. CHRISTENSEN. 1966. Kronrecherches.Bull. Sci. FranceBelg., 19: 13-45.
borgiacaridicolasp. nov. an endoparasiticturbelGIARD, A., and J. BONNIER. 1887. Contributionsa
larian from North Atlanticshrimps. Ophelia,3:
l'etude des Bopyriens. Trav. Sta. Zool. Wimereux,
65-80.
5: 1-252.
KANNEWORFF, E. 1965. Life cycle, food, and growth
GIFFORD, J. 1934. Life historyof Argeiapauperatafrom
of the amphipod AmpeliscamacrocephalaLiljeCragofranciscorum.
M.A. Thesis, Leland Stanford
borg fromthe 0resund. Ophelia,2: 305-318.
Jr. Univ.
KENNETT, C. E., C. B. HUFFAKER, and G. L. FINNEY.
1966. The role of an autoparasitic aphelinid,
GJ0SAETER, J. 1971. Sarcotretes
scopeli, a lernaeid
Coccophagoidesutilis Doutt, in the control of
copepod new to Norway. Sarsia, 46: 97-100.
Parlatoriaoleae (Colvee). Hilgardia, 37: 255-282.
GREATHEAD, D. J. 1963. A reviewof the insectenemies
of Acridoidea (Orthoptera). Trans. Roy.Entomol. KING, P. E., and J. RAFAI. 1970. Host discrimination
in a gregarious parasitoid Nasonia vitripennis
Soc. London,114: 437-517.
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
146
THE QUARTERLY REVIEW OF BIOLOGY
(Walker) (Hymenoptera: Pteromalidae). J. Exp.
Biol., 53: 245-254.
K0IE, M. 1969. On the endoparasites of Buccinum
undatumL. with special referenceto the trematodes. Ophelia,6: 251-279.
KURIS, A. M. 1971. Population interactionsbetween
a shore crab and two symbionts.Ph.D. Thesis,
Univ. California,Berkeley.
. 1973. Biological control: implications of the
analogybetweenthe trophicinteractionsof insect
pest-parasitoidand snail-trematodesystems.Exp.
Parasitol.,33: 365-379.
LtGER, L., and 0. DUBOSQ.1909. Surun Microsporidie
parasite d'une Gregarine. ComptesRend. Acad.
Sci. (Paris), 148: 733-734.
Li, S. Y., and H. F. Hsu. 1951. On the frequency
distributionof parasitichelminthsin their naturallyinfectedhosts. J. Parasitol.,37: 32-41.
LIE, K. J. 1973. Larval trematodeantagonism:principles and possible applicationsas a control method. Exp. Parasitol.,33: 343-349.
LIM, H.-K., and D. HEYNEMAN. 1972. Intramolluscan
inter-trematodeantagonism: a review of factors
influencing the host-parasite system and its
possible role in biologicalcontrol.Adv. Parasitol.,
10: 192-268.
LOAN,C., and R. G. HOLDAWAY. 1961. Microctonus
aethiops(Nees) and Perilitusrutilus(Nees) (Hymenoptera: Braconidae), European parasites of
Sitonaweevils (Coleoptera: Curculionidae). Can.
Entomol.,93: 1057-1078.
MALAQUIN, A. 1901. Le parasitismeevolutifdes Monstrillides(Crustaces Copepodes). Arch.Zool. Exp.
Ge'n,29: 81-232.
MANN, H. 1967. The significanceof the copepods
as parasites on sea animals used economically.
Proc.Symp.CrustaceaMar. Biol. Assoc.India Symp.,
Ser. 2(3): 1156-1160.
MARTIN, R., and R. BRINKMAN. 1963. Zum Brutparasitismus von Phyllirhoe
bucephalaPer. et Les. auf
der Medusa Zanclea costataGegenb. Pubbl. Staz.
Zool. Napoli, 33: 206-223.
MAUCHLINE, J. 1966. Thalassomyces
fagei,an ellobiopsid
parasiteof the euphausiid crustacean Thysanoessa
raschi.J. Mar. Biol. Assoc. U.K., 46: 531-539.
MENGE, B. A. 1972. Foraging strategyof a starfish
in relationto actual preyavailabilityand environmental predictiability.Ecol. Monogr.,42: 25-50.
MERCIER, L., and R. POISSON.1929. Alteration des
certainscaracteres sexuels secondaires du male
de Pinnotheres
pisumparasite par un Entoniscien.
Bull. Soc. Zool. France,54: 301-304.
MESSENGER, P. S. 1964. Use of lifetablesin a bioclimatic
study of an experimental aphid-braconid wasp
host-parasitesystem.Ecology,45: 119-131.
MIYASHITA, Y. 1941. Observations on an entoniscid
parasiteof Eriocheirjaponicusde Haan, Entionella
fluviatilisn.g., n. sp. Jap.J. Zool.,9: 251-267.
49
[VOLUME
MORAN, S. L., and L. FISHELSON. 1971. Predation of
a sand-dwelling mysid crustacean Gastrosaccus
sanctusby plover birds(Charadriidae). Mar. Biol.,
9: 63-64.
MORRIS, J. A. 1948. Studies on the host-parasite
relationshipof Probopyrus
pandalicola(Packard).
CatholicUniv. Am. Biol. Stud.,8: 1-20.
MOUCHET, S. 1931. Spermatophores des Crustaces
Decapodes Anomoures et Brachyoureset castration parasitairechez quelques Pagures. Ann. Sta.
Oce'anogr.Salammbo,6: 1-203.
MUELLER,J. F. 1966. The laboratorypropagation of
Spirometra
mansonoides
(Mueller, 1935) as an experimentaltool. VII. Improved techniques and
additional notes on the biology of the parasites
(Cestoda). J. Parasitol.,52: 437-443.
NOBLE, E. R., and G. A. NOBLE. 1964. Parasitology.
The Biologyof Animal Parasites.2nd ed. Lea &
Febiger, Philadelphia.
OKHOTINA, M. V., and E. V. NADTOCHY. 1970. Effect
of Mammanidulaasperocutis
Sadovskaja in Skrjabin, Sihobalova and Sulc, 1954 (Nematoda), on
the population size of shrewsof the genus Sorex.
Acta Parasitol.Polon.,18: 81-84.
OLIVER, J. H. 1962. A mite parasitic in the cocoons
of earthworms.J. Parasitol.,48: 120-123.
PAINE, R. T. 1963. Ecology of the brachipod Glottidia
pyramidata.
Ecol. Monogr.,33: 187-213.
PALM,N. B. 1948. Normal and pathologicalhistology
of the ovaries in BombusLatr. withnotes on the
hormonal interrelationships
between the ovaries
and the corpora allata. Opuscula Ent. Suppl., 7:
1-101.
PENNYCUICK,L. 1971a. Quantitative effectsof three
species of parasites on a population of threespined sticklebacks,Gasterosteus
aculeatus.J. Zool.,
165: 143-162.
.- 1971b. Frequency distributionsof parasites in
a population of three-spinedsticklebacks,Gasterosteus
aculeatusL., withparticularreferenceto
the negative binomial distribution.Parasitology,
63: 389-406.
PEREZ, CH. 1927. Sur le parasitisme protelien du
Nectonema.ComptesRend. Acad. Sci. (Paris), 185:
226-227.
.- 1931. Notes sur les Epicarides et les Rhizoceet
phales des cotes de France. VII. Peltogaster
Liriopsis.Bull. Soc. Zool. France,56: 509-512.
A. 1966. Equilibre des especes dans les popuPETTER,
lations de Nematodes parasites de colon des
tortues terrestres.Mim. Mus. Nat. Hist. Natur.
Se'r.A, Zool.,39: 1-252.
PICARD, F. 1930. Sur le parasitisme d'un Phoride
(Megaselia cuspidataSchmitz) aux depens d'un
Myriapode. Bull. Soc. Zool. Fr., 55: 180-183.
PIKE, R. B. 1960. The biologyand post-larvaldevelopment of the bopyrid parasites Pseudioneaffinis
abdominalis(Kroyer)
G. 0. Sars and Hemiarthrus
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
147
(= Phryxusabdominalis(Kroyer)). J. Linn. Soc.
. 1968. The resistance of insect parasitoids to
London(Zool.), 44: 239-251.
the defence reactions of their hosts. Biol. Rev.,
. 1961. Observationson the Epicaridea obtained
43: 200-233.
fromhermitcrabs in Britishwaters,with notes SAMUELSEN,T. J. 1970. Peltogaster
curvatusKossman,
on the longevityof the host species. Ann. Mag.
a rhizocephalan parasite new to the Norwegian
Natur. Hist., 13(4): 225-240.
fauna, with notes on the synonymyof one of
PLATEAUX, L. 1972. Sur les modificationsproduites
the hosts, Pagurus prideauxiLeach. Sarsia, 43:
chez un fourmi par la presence d'un parasite
81-86.
Cestode. Ann. Sci. Nat. Zool. 12 Se'r.,14: 203-220.
SCHAD,G. A. 1963. Niche diversification
in a parasitic
POINAR, G. O., and P. A. VANDER LAAN. 1972. Morspecies flock. Nature,198: 404-406.
phology and life historyof Sphaerulariabombi. SCHILLER, E. L. 1966. Observations on some hostNematologica,18: 239-252.
parasite relationshipsamong Arctic wildlife.In
PRENANT,M. 1959. Classe des Myzostomides.In P.-P.
J. E. McCauley (ed.), Host-ParasiteRelationships,
Grasse (ed.), Trait6 de Zoologie:Anatomie,Systepp. 127-143. Oregon State University Press,
matique,Biologie,V(1), p. 714-784. Masson, Paris.
Corvallis.
PRICE, P. W. 1970. CharacteristicspermittingcoexisSCHOONHOVEN,L. M. 1962. Diapause and the physioltence among parasitoids of a sawflyin Quebec.
ogy of host-parasitesynchronizationin Bupalus
Ecology,51: 445-454.
piniariusL. (Geometridae) and Eucarceliarutilla
RASMUSSEN, E. 1959. Behavior of sacculinized shore
Vill. (Tachinidae). Arch.Neerl.Zool.,15: 111-174.
crabs (Carcinus maenas Pennant). Nature, 183:
SENTZ-BRACONNOT,E., and C. CARRE. 1966. Sur la
479-480.
biologie du Nudibranche pelagique Cephalopyge
RAUSCH, R., and E. L. SCHILLER. 1956. Studies on the
trematoides.Parasitism sur le Siphonophore
helminth fauna of Alaska. XXV. The ecology
Nanomia bijuga,nutrition,developpement. Cah.
and public health significance of Echinococcus
Biol. Mar., 7: 31-38.
sibiricensisRausch and Schiller, 1954, on St.
SHIINO, S. M. 1942. On the parasitic isopods of the
Lawrence Island. Parasitology,
familyEntoniscidaeespeciallythose found in the
46: 395-419.
REINHARD, E. G. 1956. Parasiticcastrationof Crustavicinityof Seto. Mem. Coll. Sci. KyotoSer. B.,
cea. Exp. Parasitol.,5: 79-107.
17: 37-76.
REINHARD,E. G., and F. W. BUCKERIDGE. 1950. The
SMITH,G. W. 1905. Note on a gregarine (Aggregata
effect of parasitism by an entoniscid on the
inachi n. sp.) which may cause the parasitic
secondary sexual characters of Pagurus longicastrationof its host (Inachus dorsettensis).
Mitt.
carpus.J. Parasitol.,35: 131-138.
Zool. Sta. Neapel, 17: 406-410.
REISINGER,
E. 1930. Zum ductus genito-intenstinalis SPAULDING,J. G. 1972. The life cycle of Peachia quinProblem i. Uber primare Geschechtstraktdarmquecapitata,an anemone parasitic on medusae
verbendungenbei rhabdocoelen Turbellarien. Z.
during its larval development. Biol. Bull., 143:
Morphol.Okol. Tiere, 16: 49-73.
440-453.
REVERBERI,G. 1943. Sul significatodella "castrazione STURROCK,R. F., and G. WERBE. 1971. The application
parassitaria." La trasformazionedel sesso nei
of catalyticmodels to schistosomiasisin snails.
Crostacei parassitatida Bopiridi e da Rizocefali.
J. Helminthol.,
45: 189-200.
Pubbl.Staz. Zool. Napoli, 19: 225-316.
SUMMERFELT,R. C., and M. C. WARNER. 1970. GeoROTHSCHILD, M. 1938. Further observations on the
graphicaldistributionand host-parasiterelationeffectof trematode parasites on Peringia ulvae
ships of Plistophoraovariae(Microsporida, Nose(Pennant, 1777). Novit.Zool.,41: 84-102.
matidae) in Notemigonus
crysoleucas.
J. Wildl.Dis.,
. 1941. Observationson the growthand trema6: 457-465.
tode infectionsof Peringiaulvae, Pennant, 1777 TCHERNIGOVTZEFF,
C. 1960. Nouvelles observationssur
in a pool in the Tamar saltings,Plymouth.Parala mue de Bopyrusfougerouxi,
Isopode parasite
33: 406-415.
sitology,
de Leanderserratus
(Pennant). ComptesRend.Acad.
SAHLI, F. 1972. Modificationsdes caracteres sexual
Sci. (Paris)., 250: 185-189.
secondaires males chez les Iulidae (Myriapoda, THtODORIDES, J. 1965. Ordre des Enoplides (EnopliDiplopoda) sous l'influencede Gordiaces parada). Superfamille des Mermithoidea Wiulker,
sites. ComptesRend. Acad. Sci. (Paris), 274: 9001924. In P.-P. Grasse' (ed.), Traite de Zoologie:
903.
Anatomie, Systematique,Biologie, IV(2) [NeSALT, G. 1941. The effectsof hosts on their insect
mathelminthes(Nematodes)] p. 681-704. Masparasites. Biol. Rev., 16: 239-264.
son, Paris.
. 1961. Competition among insect parasitoids. TROTT1, L. B. 1970. Contributionsto the biology of
Symp.Soc. Exp. Biol., 15: 96-119.
carapid fishes(Paracanthopterygii:Gadiformes).
. 1963. The defense reactionsof insectsto metaUniv. Calif. Publ. Zool.,89: 1-60.
zoan parasites. Parasitology,
VAN DEN BOSCH, R., E. J. SCHLINGER,C. F. LAGACE,
53: 527-642.
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
148
THE QUARTERLY REVIEW OF BIOLOGY
[VOLUME
49
and J. C. HALL. 1966. Parasitismof Acyrthosiphon
L. II. Parasitizationof the gonads by the ciliate
pisumby Aphidius smithi,a density-dependent
Orchitophryastellarum
Cepiede. J. Mar. Biol. Assoc.
process in nature (Homoptera: Aphidae) (HyU.K., 29: 619-624.
menoptera:Aphidiidae). Ecology,
47: 1049-1055.
WALKEY, M., and R. H. MEAKIN. 1970. An attempt
VARLEY, G. C. 1947. The naturalcontrolof population
to balance the energy budget of a host parasite
balance in the knapweed gall-fly(Urophorajasystem.J. Fish Biol., 2: 361-372.
caena). J. Anim. Ecol., 16: 138-187.
WATERMAN, T. H., and F. A. CHACE. 1960. General
VARLEY, G. C., and C. G. BUTLER. 1933. The acceleracrustacean biology. In T. H. Waterman (ed.),
tionof developmentof insectsby parasites.ParaThe Physiology
of Crustacea,Vol. 1, pp. 1-33.
sitology,
25: 263-268.
Academic Press, New York.
VEBER, J.and J.JAsIC.1961. Microsporidiaas a factor
WELCH, H. E. 1965. Entomophilic nematodes. Ann.
in reducing the fecundityof insects. J. Insect
Rev. Entomol.,10: 275-302.
Pathol.,3: 103-111.
WHITING, A. R. 1967. The biology of the parasitic
VEILLET, A. 1945. Recherches sur le parasitismedes
wasp Mormoniellavitripennis
(=Nasonia brevicorCrabes et des Galath6es par les Rhizocephales
nis) (Walker). Quart. Rev. Biol., 42: 333-406.
et les Epicarides. Ann. Inst. Oceanogr. Monaco, WIcKsTEAD, J. H. 1963. A new record of Ellobiopsis
22: 193-341.
chattoni
(Flagellata incertae
sedis)and itsincidence
VEILLET, A., and F. GRAF. 1958. Degenerescence de
in a population of Undinnelavulgarisvar. major
la glande androgene des Crustaces Decapodes
(Crustacea Copepoda). Parasitology,
53: 293-296.
parasites par les Rhizocephales. Bull. Soc. Sci. WRIGHT, C. A. 1966. The pathogenesisof helminths
Nancy(n.s.), 18: 123-127.
in the Mollusca. Helm. Abstr.,35: 207-224.
VEVERS, H. G. 1951. The biology of Asteriasrubens
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