Asexual Reproduction in Pygospio elegans Claparede (Annelida, Polychaeta) in Relation to Parasitism by Lepocreadium setiferoides (Miller and Northup) (Platyhelminthes, Trematoda)

7 Pages·2001·3.4 MB·

by  Dean G Mccurdy

Reference: Bin/. Bull. 201: 45-51. (August 2001)
Asexual Reproduction in Pygospio elegans Claparede
(Annelida, Polychaeta) in Relation to Parasitism by
and
Lepocreadium setiferoides (Miller Northup)
(Platyhelminthes, Trematoda)
DEAN G. McCURDY*
Coastal Studies Center, 6775 College Station, Bowdoin College. Brunswick, Maine 04011-8465
Abstract. Life-history theory predicts that parasitized hosts gration; Folstad et ai, 1991). removal of parasites before
should alter their investment in reproduction in ways that they cause damage (e.g.. grooming; Leonard et ai, 1999),
maximize host reproductive success. I examined the timing of and immunological defense (e.g., encapsulation; Kraaije-
asexual reproduction (fragmentation and regeneration) in the veld and Godfray. 1997). There is increasing evidence that
polychaete annelid Pygospio elegans experimentally exposed hosts may also exhibit life-history adaptations to minimize
to cercariae ofthe trematode Lepocreadium setiferoides. Con- the impacts ofparasites on reproductive success (Minchella
sistent with adaptive host response, polychaetes that became and LoVerde, 1981; Polak and Starmer, 1998; McCurdy et
infected by metacercariae of trematodes fragmented sooner ai, 1999, 2000a). Life-history responses of hosts after ex-
than unexposedcontrols. Parasites were notdirectly associated posure to parasites represent reallocationsofenergy in ways
with fission in that exposed polychaetes that did not become that increase reproductive success relative to non-responses.
infected also fragmented earlier than controls. For specimens This type of reaction has been termed an adaptive host
ofP. elegans that were not exposed to trematodes, new frag- response (Minchella, 1985; Forbes, 1993). Unlike avoid-
ments thatcontained original headswere largerthan those that ance or resistance to parasites, life-history responses pose
contained original tails, whereas original head and tail frag- little or no maintenance costs to hosts (i.e., no cost when
mentsdidnotdifferinsizeforinfectedpolychaetes. In infected parasites are absent) because the hosts do not alter their life
specimens, metacercariae were equally represented in original histories until they come into contact with parasites (Min-
head and tail fragments and were more likely to be found in chella, 1985). Specifically, in systems where parasites pose
whichever fragment was larger. Despite early reproduction, greater costs to host energy budgets over time (decreasing
parasitism was still costly because populations of P. elegans future reproductive potential to a greaterextent than current
exposed to parasites were smaller than controls when mea- reproduction), hostsareexpectedtorespond to infectionsby
sured 8 weeks laterandbecause exposure tocercariae reduced hastening their onset ofreproduction. This response occurs,
survivorshipofnewlydividedpolychaetes.Takentogether, my forexample, in intertidal amphipods infected by trematodes
results suggest that early fragmentation is a host response to (McCurdy et ai, 1999, 2()()0a). Although the reproductive
minimize costs associated with parasitism. success of hosts that respond through life-history variation
is lower than that of hosts not exposed to parasites, it is
Introduction
greater than that of infected hosts that fail to respond (Mc-
Hosts respond to parasitism in a number of ways, which Curdy et ai, 2001).
include avoidance of parasites in space or time (e.g.. mi- To date, tests of the hypothesis of the adaptive host
response have been confined to hosts that reproduce sexu-
ally (Minchella and LoVerde, 1981; Polak and Starmer,
Received 19 October 2000; accepted 10 April 2001. 1998; McCurdy et ai, 1999, 2000a). However, the re-
*Current address: Department of Biology, Albion College, Albion,
Michigan 49224. sponses ofsexual hosts can be difficult to interpret because
E-mail: dmccurdy<s1albion.edu selection may act differently on males and females to max-
45
46 D. G. McCURDY
imize reproductive success (Zuk, 1990), and because of larvae; Morgan et ai. 1999), so I examined polychaetes for
factors specific to sexual mating systems (e.g., mate avail- evidence of sexual reproduction as a possible response to
ability and choice: McCurdy et til.. 2000b: but see Min- parasitism. For infected polychaetes, the advantages ofsex-
chella and LoVerde, 1981, for an exception). As a result, ual reproduction might include enhanced dispersal of off-
host investment in reproduction (reproductive effort) is as- spring (Chia et ui. 1996) possibly away from infected
sessed, but the actual consequences of this investment (re- snails and increased genetic variation (Lively, 1996). In
productive success) are difficult to quantify (Perrin et ai, fact, the evolution and maintenance of sexual reproduction
1996: McCurdy et ai. 2000a). have been explained as a host response to parasitism be-
I tested for adaptive host response in an asexual spionid cause sex is more likely to produce individuals that are able
polychaete, Pygospio elegans. This species is common in toescape parasitism overevolutionary timescales (reviewed
intertidal mudflats and sandflats throughout the Northern by Hurst and Peck, 1996).
Hemisphere (Anger, 1984). Adults ofthis species construct In addition to investigating host responses to parasitism,
tubes in the sediment and feed on detritus and phytoplank- I assessed the impact of parasitism by Lepocreadium setif-
ton (Angeretai. 1986). Asexual reproduction in P. elegans eroides on the asexual reproductive success of P. elegans
is accomplished through transverse fragmentation, followed over an 8-week period. I also assessed the costs of parasit-
by rapid regeneration of missing components (Rasmussen, ism to survivorshipand regeneration ofpolychaetes that had
1953; Hobson and Green, 1968; Gibson and Harvey, 2000). previously been cut into two fragments, mimicking the
Wilson ( 1985) found that asexual reproduction in P. elegans fragmentation that results from asexual reproduction or sub-
is density- and resource-dependent in that populations grew lethal predation (Woodin, 1982: Zajac, 1995). In all cases, I
larger when polychaetes were housed at low densities or considered two additional possibilities, other than adaptive
provided with augmented levels of food. The impacts of host response, to explain observed changes in host behavior
parasitism on asexual reproduction and regeneration, how- and development in relation to parasitism. First, such
ever, have not been investigated in this or other species of changes might have been due to adaptations of parasites to
polychaetes. increase transmission rates (parasite manipulation; Poulin et
I investigated life-history responses of P. elegans to par- ai. 1994). This possibility is particularly relevant to the
asitism by exposing polychaetes to cercariae of the trema- parasite-host system I studied because there is evidence for
todeLepocreadiwn setiferoides. During the spring and sum- parasite manipulation by cercariae and metacercariae of
mer, cercariae emerge from mud snails, Ilyanassa obsoleta, another trematode that parasitizes Ilyanassa obsoleta (Cur-
and infect spionid polychaetes as second-intermediatehosts; tis, 1987; McCurdy et ai. 1999, 2000a). Second, observed
winter flounder, Pseudopleuronectes americanus, serve as changes in behavior might have been due to side effects of
final hosts of the parasite (Martin. 1938; McCurdy et ai. infection that are not adaptive for the host or parasite
2000c). In their polychaete host, trematodes do not repro- (Poulin, 1995).
duce. However, unlike many species of trematodes that
emerge from /. obsoleta, metacercariae ofL. setiferoides do Materials and Methods
not simply encyst within their second-intermediate hosts,
butcontinue togrow anddevelop forseveral weeks (Martin. Collections and infection protocols
1938; McCurdy, pers. obs.). Thus, the costs ofparasitism to I collected specimensofPygospioelegans from a mudflat
the energy budgets of polychaete hosts are expected to between Wyer and Orr's Islands, Harpswell, Maine
increase over time after infection. (4347'N, 6958'W). This mudflat is located in Casco Bay,
Gulfof Maine, and has semidiurnal tides that range from 2
Predictions to 4 in (Born. 1999). I chose to sample at the Wyer-Orr's
mudflat because densities of P. elegans were high there
If Pygospio elegans responds to parasitism through life- (>20,000 m~2), but Ilyanassa obsoleta and its associated
history variation. I predicted that polychaetes would frag- cercarial parasites were rare (<0.25 snails m"2), minimiz-
ment soon after infection, before parasitism becomes costly. ing the likelihood that polychaetes used inexperiments were
P. elegans also exhibits flexibility in asexual reproduction, already infected. I collected polychaete tubes in the mid-
as individual polychaetes may fragment into more than five intertidal zone by sieving the top 5 cm of mud (500-jum
pieces (Rasmussen, 1953; Gibson and Harvey. 2000). In mesh) and transported tubes to the nearby running-seawater
light of this fact, I also expected that newly infected laboratory at the Coastal Studies Center of Bowdoin Col-
polychaetes might minimize the impacts of parasitism by lege for sorting. I retained only undamaged, entire adult
isolating infection in small fragmentsoreven lose infections polychaetes (>2 mm) that were not about to fragment
by dividing across infected segments. In addition, P. el- (detectable because P. elegans constricts just prior to fis-
egans may also reproduce sexually (including poecilogo- sion; Gibson and Harvey. 2000).
nous development, with planktotrophic and adelophagic To obtain cercarial trematodes for experiments. I col-
PARASITISM AND ASEXUAL REPRODUCTION 47
lected specimens of /. obsoleta from throughout the inter- for all groups were non-normal. I then applied Dunn's
tidal zone at Strawberry Creek. Great Island, Maine method tocompare differences among medians (Zar, 1996).
(4349'N. 6958'W). This mudflat is located 2.5 km from To investigate how exposure to parasites affected the
the Wyer-Orr's mudflat and supports high densities of /. reproductive success of P. elegans, I randomly housed 18
obsoleta (>10 m~2). In the laboratory. I housed 550 mud sets of 10 polychaetes (hereafter referred to as populations
snails in separate 9-oz plastic cups with 125 ml of filtered of polychaetes) in separate dishes and exposed half of the
seawater(55 ^im, 31 ppt, 23 C). I retained only large snails sets to cercariae of trematodes (housing conditions for
(>15 mm. tip of apex to lip of siphonal canal) because polychaetes were asdescribed above). Because the infection
previous studies have shown that the prevalence of Lepo- status ofpolychaetes that died during this experiment could
creadium setiferoides increases with shell height of snails not be determined without disturbing surviving polychaetes,
(Curtis. 1997; McCurdy el ai. 2000c). After 30 h. I exam- I assessed rates of experimental and background infection
ined each cup for cercariae of L. setiferoides (identified by randomly removing two sentinel populations after 3
using McDermott, 1951). combined cercarial-infested sea- days: a population of polychaetes that had been exposed to
water from cups of six snails that had shed cercariae, and cercariae, and a population ofunexposed polychaetes. Rates
pipetted 20 ml ofthe solution into each dish that contained of infection at that time represented maximum levels that
a polychaete that was to be exposed. Unexposed could occur because cercariae ofL. setiferoides survive for
polychaetes each received 20 ml of seawater from six cups less than 48 h outside a host (Stunkard, 1972). After 8
that contained snails that did not shed cercariae (confirmed weeks. I removed the remaining dishes and processed each
by dissection, as cercarial release is a poor indicator of population by counting the number of polychaetes retained
infection status; Curtis and Hubbard. 1990). aftersieving (425-jam mesh) and dissectingeach polychaete
to determine its infection status.
To assess survivorship and regenerative ability of newly
Experiments divided polychaetes in relation to parasitism. I cut 59
polychaetes into two fragments and exposed 30 pairs of
To investigate the impact of parasites on the timing of fragments to cercariae. Cutting each polychaete resulted in
asexual reproduction, I individually housed 52 adult speci- a smooth, clean blastema similar to that resulting from
mens of P. elegans in 150-ml custard dishes filled with sublethal predation or asexual fragmentation (Gibson and
unfiltered seawater with or without cercariae (18 C. 16 h Harvey. 2000; pers. obs.). To mimic conditions in nature,
light day"1). After 24 h. I transferred each polychaete to a where newly fragmented polychaetes generally remain in
new dish filled with seawater and lined with defaunated the same burrow during regeneration (Gudmundsson, 1985;
mud (prepared by passing mud through a425-ju.m sieve and Gibson and Harvey, 2000). I individually housed original
heating it to 70 C). Every 24 h, I suspended each dish from head and tail fragments togetherin adish with seawaterand
a harness and determined the status of each polychaete by mud (housing conditions as described above). To avoid
observing its tube (or tubes) through the bottom of its dish disturbing fragments (as above), I assessed initial rates of
with the aidofa fiber-optic illuminatorand 10X magnifying infection at 3 days after exposure or non-exposure by re-
loupe. Polychaetes could easily be observed because they moving and dissecting randomly chosen sentinel pairs of
constructed tubes that opened against the bottoms of their exposed fragments (/; =: 10 polychaetes) and unexposed
=
dishes. Polychaetes were fed the pea-flower-based supple- fragments (n 10 polychaetes). At 10 days after exposure
ment Liquifry Marine (Interpet Inc.; Brown el ai, 1999) or non-exposure. I removed all remaining fragments, mea-
= ~
every 3 days (concentration 1 drop 1 ') following a sured their lengths, and determined their infection status.
complete change of water. I removed polychaetes from the
experiment when they died or fragmented, and I measured Results
the relaxed length ofall fragments with an ocular microme- Parasitism and hostfragmentation
ter (nearest 0.1 mm; Gudmundsson. 1985). I then dissected
each fragment to determine if it was infected by trematode In the experiment investigating the impact oftrematodes
metacercariae and compared median time-to-fragmentation on the timing ofasexual reproduction in Pygospio elegans,
among exposed but uninfected. exposed and infected, and parasite prevalence was low (42.3% ofpolychaetes exposed
=
unexposed polychaetes. In making this comparison. I sepa- became infected; n 26). Asexual fragmentation always
rated exposed but uninfected polychaetes from unexposed yielded two fragments; one containing the original head and
ones because ofthe possibility that host response might be thorax and a second containing the original tail (see Gibson
associated with indirect cues associated with parasitism and Harvey, 2000, foradescription ofbodycomponents). In
(i.e., response might not require an actual infection to oc- all cases, polychaetes fragmented within 24 h ofobservable
cur). To compare time-to-fragmentation. I applied a non- constrictions. Time-to-fragmentation differed between ex-
parametric Kruskal-Wallis ANOVA because the residuals posed and infected, exposed but uninfected. and unexposed
48 D. G. McCURDY
30
PARASITISM AND ASEXUAL REPRODUCTION 49
Curdy et til., 20()0c). As a result, thousands ofcercariae are
shed in areas where infections are most likely to occur.
Additional information on the infection process ofL. setif-
crnitles is necessary to determine whether polychaetes de-
tect cercariae, and whether the exposure-related response
resulted from the presence of cercariae or from failed at-
I tempts at penetration. There is evidence from otherparasite-
cAC host systems that invertebrates can detect and exhibit anti-
parasite behaviors to minimize the likelihood of infection
(e.g.. Leonard et al.. 1999).
Early fragmentation of P. elegans is unlikely to be a
parasite adaptation, because it apparently does not increase
transmission rates for cercariae or metacercariae. Specifi-
Heads Tails cally, fragmentation was not associated with increased sus-
Originalfragments ceptibility to parasitism: most polychaetes fragmented after
Figure 2. Proportions (95% confidence intervals) of original head free-living cercariae would have (>48 h; Stunkard, 1972).
andtail fragments ofindividualsofPygospioelegans thatsurvivedfor 10 For metacercariae. residing in small fragments would not
daysin the laboratory followingexposureornon-exposuretocercariae of appear to benefit transmission to final hosts, because floun-
tthhee btarresm.atode Lepocreatl/iuii .fciiti'i-niilfs. Sample sizes are shown above der select prey at larger sizes relative to conspecifics, and
even small differences in prey size preference can pro-
foundly influence the energy budgets of predators foraging
2.71 0.19: exposed tails: x SE = 2.49 0.28; f(22) = on mudflats (MacDonald and Green. 1986: Boates and
0.63. NS). Smith, 1989; Keats. 1990). To assess whether early frag-
mentation is actually adaptive for parasites or hosts, the
Discussion consequences of early fragmentation could be further ex-
Parasitism and hostfragmentation plored by constructing a model derived from empirical
observations of parasites, their intermediate hosts, and the
In support of the hypothesis of adaptive host response I predators that are their final hosts. This approach was used
foundthat specimens ofPygospio elegans infected by meta- recently to show that the early onset ofreceptivity to mating
cercariae ofLepocreadium setiferoides hastened their onset observed in females of the amphipod Corophium volntator
of asexual reproduction relative to unexposed controls. By infected by the trematode G\naecotyla adunca resulted in
doing so, polychaetes may be expected to achieve greater greater reproductive success for the amphipods than ifthey
reproductive success than if they had failed to respond had waited to become receptive at the optimal time for
because of increasing costs associated with parasitism over uninfected females (McCurdy et al., 2001).
time (Forbes, 1993). However, my observation that early I found no evidence that fragmentation of P. elegans
fragmentation also occurred in exposed polychaetes that served to isolate or remove metacercariae, in that fission
remained uninfected complicates this interpretation. In a produced only two fragments, the smaller of which almost
study that separated hosts by exposure and infection status, never contained metacercariae. It is unclear whether the
Minchella and Loverde ( 1981 ) found that freshwater snails greater presence of metacercariae in larger fragments is
of the species Biomphalaria glahrata increased their rates adaptive for the parasite or its host or whether larger frag-
ofearly egg laying when infected by Schistosoma mansoni, ments merely represent larger targets for parasites. Meta-
but that the rates forexposed but uninfected individuals and cercariae might benefit from residing in larger fragments
unexposed controls did not differ. These authors argued that because of the availability of additional resources for para-
only infected snails responded because successful parasit- site development or the possibility ofa greater transmission
ism was associated with a high cost to future reproduction rate to final hosts (as stated above, flounder tend to select
(castration). larger prey). If residing in larger fragments is parasite-
For individuals ofP. elegans exposed to, but not infected mediated, the observation that metacercariae develop near
by, cercariae. early reproduction could still be an adaptive the site of initial penetration (Stunkard. 1972; pers. obs)
host response ifexposure to cercariae in nature is a reliable indicates that the mechanism does not involve movements
indicator that costly infections will soon result (Minchella. by metacercariae through the host coelom and into larger
1985). Support forthis ideacomes fromthe observation that fragments. Fragmentation couldalsobe interpreted as a host
Ilyanassa obsoleta infected by L. setiferoides, although response: If larger fragments are better able to tolerate
uncommon across mudflats, can remain for several months stresses associated with parasitism, the result wouldbe a net
in small patches where some P. elegans are found (Mc- reproductive benefit to hosts. In fact, host response need not
50 D. G. McCURDY
be exclusive of benefits to parasites, depending on the Acknowledgments
timingofaltered behaviorofinfected hosts (McCurdy etai.
1999). Simulated parasites such as Sephadex beads (Suwan- I thank Glenys Gibson forher suggestions on experimen-
chaichinda and Paskewitz. 1998) could be used to help tal design and Mark Forbes for our many discussions about
separate effects mediated by the parasite from those medi- life-history theory. Funding was provided by postdoctoral
ated by the host. Experiments with simulated parasites fellowships from the Natural Sciences and Engineering Re-
would provide cues to the host that it has become infected search Council of Canada and the Coastal Studies Center,
Bowdoin
while removing the possibility of parasite manipulation. College.
Across all experiments, I found no evidence for onset of
sexual reproduction, observing neither eggs nor spermato- Literature Cited
phores. Seasonal constraints may have precluded sexual
reproduction, which usually occurs only during the winter Angetiro,nVt.o1i9t8s4.geogRreapprhoidcuacltioornigiinnPayngdosptoioenevleigraonnsme(nStpailonciodnadei)tiionnsr:elaa-
in P. elegans (Rasmussen, 1953; Gudmundsson, 1985; Wil- preliminary report. Fortschr. Zoo/. 29: 45-51.
son, 1985). However, even if the polychaetes had shown Anger, K.. V. Anger, and E. Hagmeier. 1986. Laboratory studies on
evidence of sexual reproduction, this tactic might be ex- larvalgrowthofPolydoraligni, Polydoraci/iata, andPygospioelegans
pected to increase reproductive success only if mates were (Polychaeta: Spionidae). Helgol. Meeresunters. 40: 377-395.
Boates, J. S., and P. C. Smith. 1989. Crawling behaviour of the am-
available; an unlikely event given the rarity of parasites in phipod. Corophium vohitatorand foraging by semipalmated sandpip-
natural populations of P. elegans (above). ers. Culidri.\ pusilia. Can. J. Zoo/. 67: 457-462.
Born, M. A. 1999. Tidelog: Northern New England Edition. Pacific
Publishers. Bolinas. CA.
Parasitism and host asexual reproductive success Brey, T. 1991. Interactions in soft bottom benthic communities: quanti-
aveIrfaogeu,nd8t%hatofevceenrcaarliaoewtlheavtelaosfienxglpeossunraeiltoshceedrscairnia3e0(ohn) steualtneitgveaernss.as(4pP5eo:cltys3c0ho1af-e3tb1ae6)h.aavnidoMuracionmtahebaslutrhfiaccae(dBeipvoalsviita)f.eeHdeelrgsol.PyMgeoesrpei-o
reduced the asexual reproductive success of P. elegans Brown, R. J.. M. Conradi, and M. H. Depledge. 1999. Long-term
(45%, measured in populations 8 weeks after exposure). In exposureto4-nonylphenol affectssexual differentiationandgrowthof
a related finding from another experiment, both head and the amphipod Corophium volutator(Pallas, 1766). Sri'. TotalEnviron.
233: 77-X8.
tail fragments were less likely to survive to complete regen- Chia, F. S., G. Gibson, and P. V. Qian. 1996. Poecilogony as a
eration than were unexposed fragments. Direct effects of reproductive strategy ofmarine invertebrates. Oceanol. Acta 19: 203-
parasitism are not sufficient to account for these results 208.
given that few exposed polychaetes actually became in- Curtis, L. A. 1987. Vertical distribution ofan estuarine snail alteredby
fected in eitherexperiment. One possibility is to explain the a parasite. Science 235: 1509-1511.
Curtis,L. A. 1997. Ilvanassaobsoleta(Gastropoda)asahostfortrema-
reduced reproductive success of exposed but uninfected todes in Delaware estuaries. J. Parasitol. 83: 793-803.
hosts as the result ofa trade-off between host reproductive Curtis,L.A.,and K. M. K. Hubhard. 1990. Trematodeinfectionsina
effort and costly activities associated with defenses against gastropod host misrepresented by observing shed cercariae. J. Exp.
parasites. Recent work has shown that hosts exposed to Mar. Bwl. Ecol. 143: 131-137.
parasites may trade off energy used in reproduction for Folstad, I.,A. C. Nilssen, O. Halvorsen,and J. Andersen. 1991. Par-
behaviors or immune responses to resist parasites (Sheldon Ja.siZte<>a/v.oi6d9a:nc2e4:23t-he24c2a9u.seofpost-calvingmigrationsinRangifer?Can.
and Verhulst, 1996; Leonard et ai, 1999). Forbes, M. R. L. 1993. Parasitism and host reproductive effort. Oikos
Regardless ofthe underlying causes, the dramatic reduc- 67: 444-450.
tion in reproductive success ofP. elegans after exposure to Gibson, G. I)., and J. M. L. Harvey. 2000. Morphogenesis during
cercariae has implications for natural populations of this asexual reproduction in Pygospio elegans Claparede (Annelida.
species and for soft-bottom intertidal communities. Pygos- GudPmoulnycdhsasetoan).. BHi.ol.19B8u5l.l. 1L9i9f:e h4i1s-t4o9ry.patterns ofpolychaete species of
pio elegans often dominates such communities, and thus the Family Spionidae. J. Mar. Biol. Assoc. UK65: 93-111.
can directly affect the distribution and abundance of other Hobson, K. D.. and R. H. Green. 1968. Asexual and sexual reproduc-
infauna (Wilson, 1983: Brey, 1991; Kube and Powilleit, tion of Pygospio elegans (Polychaeta) in Barnstable Harbor. Massa-
1997). In addition, it ispossiblethat parasitismofP. elegans chusetts. Biol. Bull. 135: 410 (abstract).
Hurst,L.D.,andJ.R.Peck. 1996. Recentadvancesinunderstandingof
may influence the structure of intertidal communities by
the evolution and maintenance ofsex. Trends Ecol. Evol. 11: 46-52.
altering or creating engineering functions in hosts. Engi- Keats, D. VV. 1990. FoodofwinterflounderPseudopleuronectesameri-
neering functions are those that produce new habitat as a ciinii.i in a seaurchin dominated community in eastern Newfoundland
result ofchanges in behaviors or life history associated with (Canada1. Mar. Ecol. Prog. Ser. 60: 13-22.
parasitism (Thomas et ai, 1999). Clearly, researchers Kraaijeveld, A. R.,and C.J. Godfray. 1997. Trade-offbetween para-
should consider the impacts ofparasites on the ecology and st>iatsoticdr.reNsaitsutarnece38a9n:d2l7a8rv-a2l80c.ompetitive ability in Drosophi/a melano-
evolution of the reproductive strategies of marine inverte- Kube.J.,and M. Powilleit. 1997. Factorscontrollingthedistributionof
brates and on the structure of infaunal communities. Maren;.elleria cf. viridis. Pvgospio e/egans and Strehlospio shrubsoli
PARASITISM AND ASEXUAL REPRODUCTION 51
(Polychaeta: Spionidae) in the southern Baltic Sea, with special atten- Sheader. 1999. Evidence for poecilogony in Pygospio elegans
tion fortheresponsetoaneventofhypoxia.Aquat. Ecol.31: 187-198. (Polychaeta: Spionidae). Mar. Ecol. Prog. Ser. 178: 121-132.
Leonard,N., M. R. Forbes,and R. L. Baker. 1999. EffectsofLimno- Perrin, N., P. Christie, and H. Richner. 1996. On host lite-history
charesamericana(Hydrachnidia: Limnochandae)mitesonlifehistory response to parasitism. Oikos 75: 317-210.
traitsandgroomingbehaviourofitsdamselflyhost,Enallagmaebrium Polak,M.,and W.T.Starmer. 1998. Parasite-inducedriskofmortality
(Odonata: Coenagrionidae). Can. J. Zool. 77: 1615-1622. ele\ates reproductiveeffort inDrosophila. Proc. R. Soc. Land. B265:
Lively, C. M. 1996. Host-parasite coevolution and sex: Do interactions 2197-2201.
between biological enemies maintain genetic variation and cross-fer- Poulin. R. 1995. "Adaptive" changes in behaviour of parasitized ani-
tilization? Bioscience 46: 107-114. mals: acritical review. Int. J. Parasitol. 25: 1371-1383.
Macdonald,J. S.,and R. H. Green. 1986. Foodresource utilizationby Poulin. R.. J. Brodeur, and J. Moore. 1994. Parasite manipulation of
live henthic feeding fish in Passamaquoddy Bay, New Brunswick behaviour: should hosts always lose? Oikos 70: 479 1-84.
(Canada). Can. J. Fish. Aquat. Sci. 43: 1534-1546. Rasmussen. E. 1953. Asexual reproduction in PygospioelegansClapa-
Martin. \V. E. 1938. Studies on trematodes of Woods Hole: the life rede (Polychaeta sedentaria). Nature 171: 1161-1162.
cycle ofLepocreadium setiferoides (Miller and Northup). Allocreadi- Sheldon, B. C.,and S. Verhulst. 1996. Ecological immunology: costly
idae. and the description ofCt-rcuria cumingiae N. Sp. Biol. Bull. 75: parasite defenses and trade-offs in evolutionary ecology. TrendsEcol.
463-474. Evfil. 11: 317-321.
McCurdy. D. G., M. R. Forbes, and J. S. Boates. 1999. Testing Stunkard,H.VV. 1972. Observationsonthemorphologyandlife-history
alternative hypotheses for variation in amphipod behaviour and life of the digenetic trematode, Lepocreadium setiferoides (Miller and
McChuirstdoyry,iDn.rGe.l,atMio.nRt.o pFaorrabseist,isam.ndIntJ..JS..PBaoraatseist.ol2.02090:a.100M1a-l1e00a9m.phi- SuwaNonrcthhauipc.hi1n9d2a6).MCa.r,tiann.d19S3.8.M.BioPl.asBkuelwli.tz1.42:1939286.-33E4f.fects of larval
pods increase their mating effort before behavioural manipulation by nutrition, adult body size, and adult temperature on the ability of
McCturredmayt,odDe.s.G.C,anJ..SJ..BZooaotle.s,78a:nd60M6.-6R1.2.Forbes.2000b. Reproductive ThoAJm.naoMspe,hde.Fl.e,EsnRt.goamPmooblui.laien3.5(:DTi.1p5tde7er-a1M:6e1Ce.uiliisc,idJ.aeG)uteogmaenl,anainzdeSFe.pRheandaeuxd.b1e9ad9s9..
synchrony in the intertidal amphipod Corophium volutator. Oikos 88: Parasitesandecosystemengineering: whatrolescouldtheyplay?Oikos
301-308.
84: 167-171.
McCurdy, D. G., J. S. Boates. and M. R. Forbes. 2000c. Spatial Wilson. \V. H., Jr. 1983. The role ofdensity dependence in a marine
distribution of the intertidal snail llyanassa obsolete! in relation to infaunal community. Ecologv64: 295-306.
parasitismbytwospeciesoftrematodes. Can.J. Zoo/. 78: 1137-1143. Wilson. W. H., Jr. 1985. Food limitation ofasexual reproduction in a
McCurdy, D. G.,J. S. Boates,and M. R. Forbes. 2001. An empirical spionid polychaete. Int. J. Invertcbr. Reprod. Dev. 8: 61-65.
model of the optimal timing of reproduction for female amphipods Woodin, S. A. 1982. Browsing: important in marine sedimentary envi-
infected by trematodes. J. Parasitol. 87: 24-31. ronments? Spionid polychaete examples. J. Mar. Biol. Assoc. UK60:
McDermott, J. J. 1951. Larval trematode infection in Nassa obsoleta 35-45.
(Say),from NewJerseywaters. Ph.D. dissertation. RutgersUniversity. Zajac. R. N. 1995. Sublethal predation on Polydora comuta
Newark, NJ. (Polychaeta: Spionidae): patterns oftissue loss in a field population.
Minchella. D.J. 1985. Host life-history variation in responsetoparasit- predator functional response and potential demographic impacts. Mar.
ism. Parasitology 90: 205-216. Biol. 123: 531-541.
Minchella, D. J.,and C. M. LoVerde. 1981. A cost ofincreased early Zar, J. H. 1996. Biostatistical Analysis. Prentice-Hall, Upper Saddle
reproductive effort in the snail Biomphalaria glabrata. Am. Nat- 118: River. NJ.
876-881. Zuk, M. 1990. Reproductive strategies and disease susceptibility: an
Morgan,T.S.,A.D.Rogers,G.L.J.Paterson,L. E. Hawkins,and M. evolutionary viewpoint. Pamsitol. Today 6: 231-233.