Download Echinostoma revolutum parasitism of Lymnaea elodes snails

Oecologia (1998) 115:188±195
Ó Springer-Verlag 1998
Robert E. Sorensen á Dennis J. Minchella
Parasite in¯uences on host life history:
Echinostoma revolutum parasitism of Lymnaea elodes snails
Received: 5 September 1997 / Accepted: 19 November 1997
Abstract Using ®eld surveys and experimental infections, we investigated the in¯uence of a trematode parasite on life history traits of adult Lymnaea elodes snails.
We found that parasitism signi®cantly a€ected the
growth, fecundity, and survival of host snails. Within
®ve of the six natural L. elodes populations we sampled,
shell length of echinostome-infected hosts was
signi®cantly greater than for uninfected conspeci®cs.
Furthermore, we show that gigantism occurs among
experimentally infected snails due to an accelerated
growth rate and size-selective mortality following an
Echinostoma revolutum infection. The fecundity of infected snails sharply decreased beginning at 3 weeks post
exposure (PE) and all egg production eventually ceased
for most hosts by 5±6 weeks PE. Energy constraints,
imposed by parasite development, alter the host energy
budget. Early in the infection, parasite depletion of host
energy reserves reduces host reproduction, but sucient
resources remain to allow accelerated host growth.
Mortality was increased among host snails at two distinct stages: shortly after exposure and several weeks
after cercariae were ®rst released. We did not observe
tissue degradation in snails during the ®rst 4 weeks after
exposure to the parasite, but destruction of host tissues
was noted among snails dying later in the infection.
Key words Host life history á Parasitism á Gigantism á
Echinostoma á Lymnaea
Introduction
An organism's di€erential investment into growth, reproduction, and survival de®nes its life history strategy.
Allocation trade-o€s exist between these processes such
R.E. Sorensen (&) á D.J. Minchella
Department of Biological Sciences, Purdue University,
West Lafayette, IN 47907, USA
E-mail: [email protected]; Fax: +1-765-494-0876
that energy channeled to any one of them is unavailable
to the remaining two components (Stearns 1976, 1992).
The lifetime reproductive success of an organism is a
manifestation of the life history traits expressed by that
organism throughout its life. Interspeci®c interactions,
such as predation (Crowl and Covich 1990) and competition (Brown 1982), in¯uence life history traits; likewise, parasitism shapes individual host life history
strategies (Sousa 1983; Minchella 1985). Price (1980)
elegantly emphasized the potential relationship between
parasitism and host life history strategies, but researchers have just begun to elucidate this interaction during
the last decade (Esch and Fernandez 1994; Michalakis
and Hochberg 1994). By utilizing ®eld collections and
experimental trematode infections of Lymnaea elodes, a
common freshwater snail, we assessed parasite in¯uences
on host growth, fecundity, and survival.
Parasites impose direct ®tness costs on their hosts by
stealing nutrients normally used for host life processes
(Toft 1991). Trematodes are a diverse group of endoparasites requiring at least two hosts: a mollusc and a
vertebrate. Intramolluscan trematode parasitism is frequently associated with the alteration of a host's growth,
fecundity, or survival; yet, few clear patterns exist (reviewed in Thompson 1997). The results vary depending
upon several factors, including: (1) the speci®c hostparasite combination (Minchella and LoVerde 1983;
Schrag and Rollinson 1994), (2) host age (Loker 1979;
Kuris 1980; Keas and Esch 1997), (3) the life span and
typical reproductive pattern of the host (Sousa 1983;
Curtis 1995), and (4) whether the experiments were
conducted in a laboratory or in the ®eld (McClelland
and Bourns 1969; Fernandez and Esch 1991). However,
in the midst of these host response variations, there
appears to be one common outcome among molluscs
following trematode infection: an eventual elimination
of host reproductive output, often termed ``parasitic
castration'' (Wright 1971; Malek and Cheng 1974).
For uninfected freshwater snails, the production of
energetically expensive egg masses occurs at the expense
of body growth (Geraerts and Joosse 1984) and adult life
189
span (Calow 1978). To a larval trematode, host reproduction diverts resources away from its own development,
and potentially limits the size and stability of the parasite's
habitat (Bayne and Loker 1987); thus, it is not surprising
that trematodes castrate their snail hosts. The intrinsic
interdependence existing among the growth, fecundity,
and survival components of a life history strategy suggests
that parasitic castration could a€ect the resulting growth
and survival of individual hosts. Increased host size,
termed ``gigantism,'' commonly coincides with trematode
parasitism (Keymer and Read 1991).
Parasitic castration typically begins 2±3 weeks after
infection. The cause of this reduction in fecundity may
depend upon the type of intramolluscan larval stages that
prevail in the trematode life cycle. There are two types of
intramolluscan stages of trematodes, sporocysts and
rediae, both of which function to produce additional life
cycle stages asexually within the host mollusc. Sporocysts
lack ambulatory musculature and absorb host nutrients
via their tegument. Rediae, with their muscular pharynx
and primitive gut, actively consume and digest host
tissues while moving throughout infected hosts.
Most detailed studies of life history consequences for
infected snails have focused on trematodes that possess
sporocysts as the ®nal intramolluscan stage (Pan 1965;
McClelland and Bourns 1969; Minchella and LoVerde
1981; Schrag and Rollinson 1994); therefore, relatively
little is known about host life history traits associated
with trematodes using redial larvae. This study utilizes
L. elodes snails and Echinostoma revolutum, a ubiquitous
old world trematode that develops rediae stages in pulmonate snails belonging to the genus Lymnaea (Kanev
1994). We address three questions. (1) Do natural populations of echinostome-infected L. elodes show evidence
of gigantism? (2) In controlled laboratory infections,
does E. revolutum impact the growth, fecundity and/or
survival of L. elodes snails? (3) If parasitic infection alters host life history traits, what is the temporal pattern
of this change; furthermore, can life history trade-o€s
explain this outcome?
of reproduction (Eisenberg 1970; Brown et al. 1985); however, the
life history traits of this species vary with population density, nutrient availability, and habitat permanence (Eisenberg 1966; Hunter
1975; Brown et al. 1985). Voltinism, growth rate, and size at maturity increase in permanent productive habitats, whereas, life span
and reproductive rate are greatest in vernal, densely populated
habitats. Because L. elodes is simultaneously hermaphroditic, it can
reproduce through either self-insemination or outcrossing.
The trematode, E. revolutum, has a complex three-host life cycle
and adults use avian species, primarily waterfowl, as de®nitive
hosts (Kanev 1994). E. revolutum adults, occupying the posterior
digestive tract of infected birds, produce eggs that give rise to a
free-living stage, called a miracidium, that infects L. elodes snails in
northern Indiana, USA (Sorensen et al. 1997). Miracidia of
E. revolutum that successfully infect L. elodes produce three distinct
asexual stages of the parasite, a mother sporocyst and two subsequent redial stages. The second redial generation produces an infective, free-living cercarial stage that exits the host snail and forms
metacercariae in another aquatic host, typically another snail
(Beaver 1937). Metacercariae develop into adults when ingested by
a suitable vertebrate host.
Field survey studies
Between 12 July and 9 August 1995, we collected L. elodes from six
wetlands in northern Indiana to assess the prevalence of echinostome parasitism within various snail populations. Five of these sites
± pond A, pond B, pond 39, Merry Lea Pond, and Garwood Pond
± are located within Whitley County, Ind., whereas Shock Lake is
in Kosciusko County, Ind. These six wetlands present a range of
size, permanence, predominant vegetation, and nutrient productivity characteristics (Table 1). Two of these sites (pond A and
pond B) have been previously studied (Brown et al. 1985; Minchella
et al. 1985).
L. elodes tend to reside on vegetation and detritus near the
water surface, so we surveyed each study population using a single,
haphazard collection of adult-sized L. elodes found on submerged
and emergent subtrates. The number of snails collected at each site
varied between 24 and 482 depending upon their abundance at the
time of collection. All collected snails were isolated in small Syracuse dishes for 12 h under 700 ft-c of illumination to check for
emerging echinostome cercariae (see Minchella et al. 1985). We also
measured snail size, from the tip of the spire to the base of the body
whorl to the nearest 0.01 mm with a digital caliper because shell
length was shown to be a reliable indicator of snail condition in
previous studies (Hunter 1975; Rollo and Hawryluk 1988).
Snail life history traits following experimental infections
Materials and methods
Snail and trematode descriptions
The snail L. elodes ( ˆ L. palustris ˆ Stagnicola palustris ˆ
S. elodes) is a common, freshwater pulmonate snail that inhabits a
variety of ephemeral and permanent lentic systems. L. elodes is
typically described as an annual species with a semelparous pattern
Table 1 Environmental characteristics of the six sites where
echinostome-infected and uninfected Lymnaea elodes snails
were collected during 1995 in
northern Indiana, USA
E. revolutum cercariae were obtained from the infected snails collected during the survey portion of this study in order to experimentally infect snails in the laboratory. Parasites were maintained
in the laboratory by passage through chickens (Gallus gallus dom.)
and their natural host snails (Sorensen et al. 1997).
We collected 500 L. elodes snails, ranging in size from 12 to
23 mm, on 17 June 1996 from Shock Lake. These snails were individually isolated under illumination twice (18±20 June and 2±3
Pond
Hectares
Permanence
Vegetation type
Productivity
Pond B
Merry Lea
Pond 39
Garwood
Pond A
Shock Lake
<0.1
<0.1
0.4
0.4
1.6
2.0
Temporary
Semipermanent
Temporary
Semipermanent
Temporary
Permanent
Grasses
Deciduous
Deciduous
Deciduous
Deciduous
Grasses
Low
Intermediate
Intermediate
Intermediate
Intermediate
High
190
July) to identify snails that were releasing trematode cercariae.
Infected snails were removed from the study population and uninfected snails were housed in several aquaria until 3 July 1996. The
overall prevalence of patent trematode infections among these
snails was 5%; three trematode species were detected: E. revolutum
(48%), an unidenti®ed trematode possessing amphistome cercariae
(32%), and an unidenti®ed spirorchid species (20%). No multiple
infections were observed among these snails.
On 3 July 1996, 118 of the uninfected Shock Lake L. elodes,
ranging in size from 17.52 to 22.63 mm, were each isolated in 400ml glass jars to determine their weekly egg production. All snails
were fed green leaf lettuce ad libitum throughout the experiment
and their water was replaced every 7 days with aged well water. On
11 July 1996, snails were separated into two treatment groups:
control snails (n ˆ 26, xsize SE ˆ 19:47 0:87, xfecundity SE ˆ
92:38 59:74), and E. revolutum-exposed snails (n ˆ 92,
xsize SE ˆ 19:47 0:07, xfecundity SE ˆ 96:18 40:70).
All
snails were placed individually into 10-ml vials containing 9 ml of
aged well water. For the snails in the exposed treatments, we added
ten miracidia to the vial. Control snails received no additional
treatment beyond the isolation into vials. All snails were left in vials
for 4 h and then returned to their 400-ml jar.
We recorded the shell length, fecundity, and mortality of all
snails for 15 weeks. Snail size was measured once each week. Egg
masses were removed from the snail jars twice a week throughout
the study period and the number of eggs in each mass was recorded.
Because growth of L. elodes decreases with age and size (Brown
et al. 1985; R.E. Sorensen, unpublished observations), weekly sizedependent growth increments were calculated for all snails according to: growth(t, t)1) ˆ (sizet ) sizet)1)/sizet)1.Whenever a
snail died, it was necropsied to determine its infection status. We
estimated the quantity of rediae and metacercariae present and
assessed the overall condition of the ovotestis/digestive gland
(ODG) region, the site where E. revolutum larvae develop.
We isolated all snails beginning at 3 weeks post exposure (PE)
and twice each week thereafter to ensure that no prepatently infected snails were included in the study populations. The 49 days
between the collection date of these snails and the 3-week PE
shedding date provided ample time to ensure that the remaining
snails contained no prepatant infections, because the trematodes
present at this site all reach the cercariae stage in less than 7 weeks.
In subsequent snail isolations, when cercariae were observed, a
qualitative estimate was made of the number of cercariae present.
Once the infection status of snails was determined based on
release of cercariae or the presence of rediae, they were classi®ed as
either infected (INF), exposed but uninfected (EBU), or control
(CTL); prior to this, they were classi®ed as exposed (EXP) or CTL.
Statistical analyses
We used parametric tests provided the assumptions of normality and
homoscedasticity were met, otherwise we employed non-parametric
procedures. An a of 0.05 was used to evaluate statistical signi®cance,
except when sequential tests were performed, in which case a ``tablewide'' a-value was calculated (Rice 1989). Because previous studies
have shown that life history characteristics vary from pond to pond
for L. elodes and because size heteroscedasticity existed at several of
Table 2 Mean size of echinostome-infected and uninfected L.
elodes snails collected during
1995 at various sites in northern
Indiana, USA (values in parentheses are sample sizes)
Pond
Pond A
Pond B
Merry Lea
Pond 39
Garwood
Shock Lake
Date
July 12
July 12
July 13
July 14
August 9
August 9
the sites across the infected and uninfected snails, we utilized the
appropriate t-tests (either assuming equal variances or unequal
variances) to assess di€erences in mean size for ®eld-collected snails
in the two infection classes for each of the six collection sites rather
than a two-way ANOVA. However, factorial ANOVA tests were
used to test hypotheses involving di€erences at a single point in time
among the experimentally infected snails. When multiple pairwise
comparisons were involved in the ANOVA, the Bonferroni/Dunn
post hoc procedure was used to evaluate di€erences between means.
We employed repeated-measures pro®le analysis, MANOVAR
(Potvin et al. 1990), when sequential data were collected on the same
individuals over time (von Ende 1993).
We employed non-parametric tests (Mann-Whitney U and
Kruskal-Wallis) on snail size data after 3 weeks PE and on
fecundity data after 5 weeks PE because those data violated
parametric assumptions after that time. When Kruskal-Wallis tests
showed signi®cant di€erences, we conducted multiple pairwise nonparametric comparisions (Zar 1984). We tested for associations
between exposure group and infection status or mortality status
with G-tests.
Results
Field survey studies
Based on the release of echinostome cercariae during
isolation, 267 (32.4%) of the snails collected from the six
populations possessed patent echinostome infections.
The prevalence of echinostome infections ranged from
57.6% at Merry Lea Pond to 17.1% at Shock Lake
(Table 2). The prevalence of echinostome infections was
related to the predominant vegetation type with a
greater proportion of infected snails being found in
ponds with deciduous vegetation dispersed throughout
the littoral zones when compared to sites inhabited
primarily by grass species, such as Typhus (G ˆ 12.86,
P < 0.001).
The mean size of echinostome-infected snails was
signi®cantly larger than that of uninfected L. elodes at
®ve of the six wetlands (Table 2). Infected and uninfected groups of snails from Shock Lake had equal mean
sizes, and these snails were more than 5 mm smaller than
the average size of snails at the other study sites
(Table 2). When we compared the size distributions for
infected and uninfected snails from Garwood Pond and
Shock Lake, we found that all the infected snails at
Garwood Pond were larger than the mean size for uninfected snails at that site, whereas infected snails from
Shock Lake were distributed across the range of sizes for
uninfected snails (Fig. 1).
Mean snail size (mm)
Infected
Uninfected
24.27
28.23
29.15
21.23
22.21
14.37
20.87
24.03
25.81
18.67
19.17
14.38
(170)
(8)
(19)
(50)
(8)
(12)
(312)
(30)
(14)
(128)
(16)
(58)
t
df
P
9.72
3.58
3.27
4.25
2.49
0.01
169
36
13
49
21
68
<0.001
0.001
0.003
<0.001
0.021
0.989
191
Snail life history traits following experimental infections
Snail infection and mortality
cercariae were released over a 2-h period (<50). During
later weeks, the number of rediae and cercariae that were
observed increased by one to two orders of magnitude.
The growth of the rediae population had a strong negative in¯uence on the ODG as rediae apparently consumed ODG tissue, causing its size and structural
integrity to decrease over time. The ODG of most hosts
that died after 7 weeks PE was virtually destroyed. With
the increasing number of cercariae being produced by
these rediae, there was a corresponding increase in the
number of metacercariae present in their hosts. Because
snails were individually isolated, cercariae released from
the host reentered the snail's heart and kidney tissues
producing a superinfection.
We ®rst detected E. revolutum larvae at 29 days PE when
two necropsied L. elodes snails contained rediae. Echinostome cercariae were ®rst observed during snail isolations at 32 days PE. Based on the eventual release of
cercariae or the presence of rediae, it was determined
that 56.5% (52) of the EXP snails became infected with
E. revolutum. There was no relationship between initial
snail size and infection status.
E. revolutum miracidia increased mortality of EXP
L. elodes relative to control snails during the early stages
of infection (G ˆ 6.2, P ˆ 0.013). Between weeks 1
and 4 PE, 14.1% of the EXP and 7.7% of the CTL snails
died. All of the CTL snails that died did so during the
®rst week PE, whereas the EXP snails died throughout
the 4-week period PE.
E. revolutum infection also decreased host survival
after 4 weeks PE (Fig. 2). INF snails showed signi®cantly higher mortality than uninfected snails (both
EBU and CTL combined) at 6, 7, and 8 weeks PE
(G ˆ 5.3, P ˆ 0.02; G ˆ 14.3, P < 0.001; G ˆ 18.4,
P < 0.001, respectively). The EBU L. elodes survived at
rates comparable to CTL snails (Fig. 2). No INF snails
survived beyond 10 weeks (Fig. 2); furthermore, the
proportion of INF snails that survived through the 8th
week PE was signi®cantly smaller than the proportion of
surviving EBU and CTL snails (G ˆ 16.7, P < 0.001).
Necropsies of infected snails and cercariae release
patterns showed common trends over time. After 29
days, we found few rediae (<30) in the ODG and few
An E. revolutum infection had a strong e€ect on L. elodes
fecundity; egg production decreased sharply beginning
at 3 weeks PE (Fig. 3). INF snails had signi®cantly
lower weekly egg output compared to the two uninfected
snail classes (EBU and CTL) at 5 weeks PE
(F2,92 ˆ 23.71, P < 0.001; infected x ˆ 31:97, uninfected x ˆ 234:25, control x ˆ 146:59). Mean fecundity
values for EBU and CTL snails did not di€er during that
time period. The reduction in egg production among
parasitized snails continued, and fewer hosts laid eggs
over time until eventually all egg production ceased after
7 weeks PE (Fig. 3).
Among snails in the two uninfected classes (EBU and
CTL), fecundity was variable beyond 3 weeks PE, but
there was a general negative trend as time increased
Fig. 1 Size distribution of echinostome-infected and uninfected
Lymnaea elodes snails collected 10 August 1995 at Garwood Pond
(A) and on 9 August 1995 at Shock Lake marsh (B). The mean size of
uninfected snails at Garwood Pond and Shock Lake is 19.17 mm and
14.37 mm, respectively
Fig. 2 Percent survival of L. elodes snails at 4±15 weeks following
exposure to Echinostoma revolutum miracidia. Infection status was
based on rediae or cercariae presence after autopsies of dead snails or
isolation of live snails under illumination at 4±7 weeks post exposure.
Data points do not re¯ect deaths that occured 0±4 weeks post
exposure
Snail fecundity
192
Fig. 3 Average fecundity of L. elodes snails in three treatment groups
following exposure to E. revolutum miracidia. No infected snails
survived beyond week 10. Error bars display the standard error of the
estimate of mean weekly fecundity for each group
Fig. 4 Average size of L. elodes snails in three experimental groups.
No infected snails survived beyond week 10. Error bars display the
standard error of the estimated mean size for each group
(Fig. 3). Most of these snails continued to lay eggs
throughout the experiment. For instance, 13 of the 18
EBU and CTL snails that survived until week 15 PE
were still producing eggs at that time.
P ˆ 0.005). After 9 weeks PE, the EBU snails were
>1 mm larger than CTL snails, on average, and this
di€erence increased slightly by week 15 (Fig. 4).
Either divergent shell growth rates or size-speci®c
mortality could have yielded mean size di€erences
among snails in the treatment groups. To test for growth
rate di€erences across treatments, the size-dependent
weekly growth increment was calculated for weeks 3
through 8 PE. We found signi®cant di€erences in weekly
growth rate for all weeks except week 5 PE (for weeks
3, 4, 6±8, H > 9.0, F < 0.04; for week 5, H ˆ 4.7,
P ˆ 0.09). Subsequent multiple comparisons showed
that INF snails increased their shell length to a greater
extent than either the EBU or CTL snails during weeks
3 and 4 PE (Q ˆ 3.3, P < 0.005 and Q ˆ 3.3,
P < 0.05, respectively). Beyond this time, EBU snails
added shell material more quickly than the INF snails
(Q ˆ 3.3, P < 0.005; Q ˆ 2.9, P < 0.05; Q ˆ 3.5,
P < 0.005, for weeks 6, 7, and 8, respectively); thus, the
increase in mean size of INF snails relative to EBU or
CTL snails beyond week 5 PE was caused by size-speci®c mortality, not by an increased growth rate. Larger
INF snails survived longer than smaller INF snails in
weeks 5 and 7 PE (U ˆ 25.0, P ˆ 0.014 and
U ˆ 132.0, P ˆ 0.015, respectively). This e€ect was
not found in the EBU and CTL snails.
Snail growth
The average shell length of snails in the three groups
(INF, EBU, and CTL) increased over time through 3
weeks PE as shown by the Wilks' lambda test associated
with a MANOVAR phase analysis of a time e€ect
(F3,99 ˆ 86.70, P < 0.0001). Furthermore, di€erences
in growth rate were not observed between the snails in
the three experimental groups because no time experimental group e€ect was noted during this 3-week period
(F6,198 ˆ 0.31, P ˆ 0.93). After 3 weeks PE, however,
the mean size for INF snails increased rapidly compared
to either EBU and CTL snails (Fig. 4). At 6 weeks PE, a
signi®cant size di€erence between INF, EBU, and CTL
snails was noted (H ˆ 8.9, P < 0.001). Multiple pairwise comparisons showed that INF snails were signi®cantly larger than either EBU (Q ˆ 2.7, P < 0.05) and
CTL snails (Q ˆ 3.2, P < 0.005). This di€erence in
mean shell length among the three groups remained
throughout the 10 weeks PE that INF snails survived
(Fig. 4). INF snails were nearly 1 mm larger, on average, than snails in the EBU and CTL classes at 5 weeks,
and >2 mm larger at 10 weeks PE.
Altered growth patterns were also observed among
EBU snails beyond 5 weeks PE. Mean shell length of
EBU snails was always greater than that of CTL snails
(Fig. 4). At week 9 PE, EBU snails were signi®cantly
larger than CTL snails (time treatment, F1,9 ˆ 2.674,
Discussion
Parasitism by E. revolutum has a signi®cant in¯uence on
L. elodes growth, fecundity, and survival. We found that
snails exposed to E. revolutum su€ered increased mortality compared to control snails. Furthermore, infected
193
snails showed size-speci®c mortality favoring larger individuals, grew faster early in the infection, and displayed reduced fecundity relative to uninfected snails.
Snail infection and mortality
Both exposure to and infection by E. revolutum markedly reduced L. elodes survival as also demonstrated in
several other freshwater trematode-snail systems (Anderson and May 1979; Loker 1979; Kuris 1980;
Minchella and LoVerde, 1981). We detected two phases
of host mortality: during the prepatent stage (weeks
0±4), and several weeks postpatency (Fig. 2). Host
mortality during the prepatent stage may have resulted
from increased energetic demands of host defense, or
from starvation, because tissue degradation was not
obvious. In contrast, mortality of older snails involved
tissue degradation. Superinfection with metacercariae is
another potential cause of reduced survival in host snails
during the late stages of infection; however, little is
known about the relationship between metacercariae
burden and mortality (Beaver 1937).The function of host
immune responses was not investigated here, but initiation of these responses must be energetically demanding and the cost may depend upon the number of
miracidia or metacercariae that enter the snail (Bayne
and Loker 1987).
Snail fecundity
Trematode parasitism typically decreases the fecundity
of hosts during the patent stages of an infection. Our
results demonstrate that ``parasitic castration'' occurs in
this parasite-host system (Fig. 3). The precise cause of
this reduction is unknown, but it seems unlikely that
physical destruction of host tissues is the sole mechanism
(Wilson and Denison 1980), since few (<30) rediae were
found in necropsied snails that died early in patency.
Furthermore, the digestive gland and ovotestis of snails
displayed no evidence of damage until later in the patency (5+ weeks). These results parallel those of Cheng
et al. (1973), who concluded that chemical factors rather
than physical damage were the cause of ``parasitic castration'' in Ilyanassa obsoleta snails infected with the
sporocyst trematode, Zoogonus rubellus.
During the early stages of an infection (0±4 weeks),
before reproductive tissues become damaged, it is possible that snail fecundity is reduced in this host-parasite
system simply because of a reduction in the amount of
energy accessible to the snail given the energetic demands associated with parasitism. Rollo and Hawryluk
(1988) showed that uninfected L. elodes snails fed a lowquality diet spent more time foraging and reduced the
amount of energy allocated to reproduction relative to
snails on a high-quality control diet. It has been shown
that schistosome infections reduce the glucose and
amino acid levels of host snails in a manner similar to
starvation (Christie et al. 1974; Stanislawski et al. 1979;
Trede and Becker 1982); therefore, if echinostome infections deplete host resources, the reduction in nutrient
availability may provide the impetus for altered fecundity patterns among infected L. elodes.
Minchella and LoVerde (1981) documented a process
whereby schistosome-infected snails compensate for future reproductive losses due to parasitism by increasing
their fecundity during the prepatent period of an infection. More recently, this ``fecundity compensation''
mechanism has been reported in two other schistosome
systems involving distantly related planorbid and lymnaeid snail hosts (Thornhill et al. 1986; Schallig et al.
1991). We found no evidence of ``fecundity compensation'' among E. revolutum-infected L. elodes snails; the
mean number of eggs laid per week by infected snails did
not exceed that of uninfected or control snails during the
prepatent period. Although few detailed studies of other
trematode systems are available for comparison, it appears that ``fecundity compensation'' may be limited to
trematode systems that utilize sporocysts as the predominant intramolluscan stage. Thus, schistosomes may
mimic the conditions of Rollo and Hawryluk's (1988)
intermediate-quality diet which yielded a temporary increase in snail reproduction relative to well-fed individuals. Energy usage by E. revolutum rediae may not leave
sucient host resources to elicit a ``fecundity compensation'' response. Therefore, energy depletion/allocation
processes could explain the apparent incongruity between precastration fecundity among schistosome- and
echinostome-infected snails.
Snail growth
Brown et al. (1988) demonstrated a positive relationship
between the prevalence of trematode infections and snail
size among three populations of L. elodes in Indiana.
The same relationship holds at ®ve of the six sites we
surveyed, as the shell length of echinostome-infected
L. elodes was signi®cantly greater than that of uninfected
L. elodes (Table 2, Fig. 1). Baudoin (1975) presented six
alternative hypotheses to explain the positive correlation
between host size and the prevalence of infection. These
hypotheses involve three basic mechanisms: increased
host growth rates, di€erential host mortality rates, and
size-speci®c infection preferences of parasites. Our data
suggest that no single hypothesis accounts for gigantism
in this system. The signi®cant increase in adult host size
that occurred as a result of the experimental infections
(Fig. 4) supports the growth rate hypothesis during early
stages of a trematode infection and the size-speci®c
mortality hypothesis later in the infection. It remains to
be determined whether or not age-speci®c infection rates
are involved in this system, as shown by Curtis (1995)
with trematode-infected I. obsoleta.
Sousa (1983) predicted that among short-lived,
semelparous mollusc species, gigantism will occur following trematode parasitism because excess host energy
194
reserves are made available by ``parasitic castration.''
This prediction requires that the energetic demands of
parasitism are less than the costs of reproduction in the
absence of parasitism (Bourns 1974). Data presented
here support Sousa (1983) and Bourns (1974) by showing that L. elodes growth rates increase concurrently
with depressed fecundity (Figs. 3, 4). This outcome
suggests that host growth increases early in an infection
because larval parasite development extracts sucient
energy to reduce host fecundity, but not so much that
growth is prevented. In that sense, increased growth
following an E. revolutum infection can be considered a
manifestation of the trade-o€ between L. elodes fecundity and growth.
Three evolutionary hypotheses have been proposed as
ultimate causes of gigantism among sterilized adult
hosts: a parasite advantage, a host advantage, or a consequence of the life history trade-o€ between host growth
and fecundity (Dawkins 1982; Minchella 1985; Minchella
et al. 1985). In many cases, these alternative hypotheses
cannot be clearly distinguished by considering only the
proximate outcome of parasite-host interactions due to
the inextricable link between host fecundity and growth.
Also, it may be dicult to unambiguously assign ®tness
costs and bene®ts experienced by hosts or parasites following a change in the host's life history. We feel that the
host advantage hypothesis is supported by the elevated
growth of our exposed but uninfected snails relative to
control snails because exposure to miracidia in the absence of an infection elicits enhanced growth rates among
exposed snails.
Growth is presumably the predominant energy demand for juvenile gastropods; as a result, infected immature snails should grow more slowly than uninfected
conspeci®cs (Sousa 1983). This prediction has been supported in several studies of infected lymnaeid snails
(Zischke 1967; Loker 1979). For instance, Zischke (1967)
demonstrated that uninfected, juvenile L. elodes grow
more rapidly than individuals harboring echinostome
infections. On the other hand, our results indicate that an
increase in shell length occurs in adult snails following
infection. Therefore, within natural L. elodes populations,
it is likely that infected, immature L. elodes grow slower,
on average, than uninfected conspeci®cs, while parasitized adult snails grow faster than uninfected snails.
It seems incongruous that gigantism was not observed among naturally infected Shock Lake snails, but
it was observed among the experimentally infected snails
which originated from Shock Lake. The age-speci®c
parasite in¯uence on L. elodes growth rates helps explain
the lack of gigantism among infected snails collected
during the 1995 survey at Shock Lake. This site is a
productive, permanent wetland that provides L. elodes
with the conditions to allow a cohort to reach reproductive maturity during their ®rst year; thus, when
sampled, this population contained both mature
(15 mm) and immature members of the 1995 cohort. It
could be that snails infected prior to maturity su€ered
reduced growth rates, whereas snails infected as adults
experienced increased growth rates. Thus, under these
environmental conditions, a bimodal distribution of
host size would be expected, and the mean values for
these two size distributions would bracket the mean size
of uninfected snails. The net e€ect of these two agespeci®c processes would be a similarity in mean size for
infected and uninfected snails, as we found. This process
requires that the infected L. elodes were parasitized
during the summer we collected them. This appears
likely based on the reduced survival shown by our experimentally infected snails and by prevalence surveys
for an ecologically similar freshwater pulmonate, Helisoma trivolvis, that show echinostome parasitism peaking in late summer and waning throughout the winter
(Schmidt and Fried 1997).
Evidence of age-speci®c growth rates was not found
at our other collection sites because their ephemerality
and limited productivity prevents new cohorts from
reaching adult size by the time the survey collections
were made. In other words, the snails collected at the
sites where gigantism was detected were members of the
previous year's cohort rather than snails produced during 1995. Presumably, these hosts became infected following maturity which led to increased growth following
``parasitic castration'' and the e€ects of size-speci®c
mortality. This outcome demonstrates a potential bias
that can result when considering the impact of trematode infections on host growth in natural populations
(Fernandez and Esch 1991). In nature, the variability of
host growth rates may increase markedly following
parasitism if the growth rates of mature and immature
individuals are a€ected di€erently.
Acknowledgements This work was supported by the Purdue Research Foundation, Sigma Xi, and the Alton A. Lindsey Graduate
Fellowship. We thank P.J.C. Sorensen for invaluable assistance
with the experimental work. Furthermore, we appreciate the
thoughtful advice o€ered by Peter Fauth, Richard Howard, Je€rey
Lucas, and two anonymous reviewers who greatly improved the
clarity of this manuscript.
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