Generalist versus specialist strategies of plasticity: snail responses to predators with different foraging modes
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Freshwater Biology (2014) 59, 1101–1112 doi:10.1111/fwb.12332
Generalist versus specialist strategies of plasticity: snail
responses to predators with different foraging modes
JASON T. HOVERMAN*, RICKEY D. COTHRAN† AND RICK A. RELYEA†
*Department of Forestry and Natural Resources, Purdue University, West Lafayette, IN, U.S.A.
†
Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA, U.S.A.
SUMMARY
1. Phenotypic plasticity is a common adaptation to environmental heterogeneity, and theory predicts
that the evolution of constitutive versus plastic strategies should depend on the frequency of alterna-
tive environments, the magnitude of constraints and the costs of plasticity per se. However, it is
unclear how species should evolve when they experience more than two environments that favour
divergent phenotypes, particularly when they have absolute constraints on their morphology.
2. We examined the plasticity of three freshwater snail species (Helisoma anceps, H. campanulata and
H. trivolvis) in response to three environments: (i) no predator; (ii) shell-invading water bugs (Belos-
toma flumineum) and (iii) shell-crushing crayfish (Orconectes rusticus). We found distinct responses by
each snail species to the predator treatments. Helisoma anceps starts with a relatively low, narrow and
thick shell that becomes lower and thicker in response to crayfish but is unresponsive to water bugs.
In contrast, H. campanulata starts with a relatively high, wide and thin shell that becomes lower and
wider in response to water bugs but is unresponsive to crayfish. Helisoma trivolvis starts with a shell
of intermediate height and width while the predators induce defences in different directions.
3. These results suggest that H. trivolvis has a generalist plastic strategy while H. anceps and H. cam-
panulata have specialised plastic strategies orientated against a single type of predator at the potential
cost of being unable to respond to others.
4. We then performed predation trials to determine predator preferences using a mixture of the three
species. After 2 weeks of exposure to crayfish cues, H. anceps had higher survival than both H. trivol-
vis and H. campanulata with uncaged crayfish. After 2 weeks of exposure to water bug cues, both
H. trivolvis and H. campanulata had higher survival than H. anceps with uncaged water bugs. When
predation trials were conducted after 5 weeks of exposure to predator cues, H. trivolvis and H. cam-
panulata reached a size refuge from both predators and this shifted predation pressure to H. anceps.
5. Collectively, these results suggest that closely related prey species with different absolute con-
straints in their morphology had different defences that are either specialised or generalised to alter-
native environments.
Keywords: functional tradeoff, gastropod, inducible defence, phylogeny, selection
and substantial variation in the expression of phenotypic
Introduction
plasticity can exist among closely related species
Natural selection in heterogeneous environments may (Harvell, 1991; Kusch, 1993; Colbourne, Hebert & Taylor,
lead to the evolution of phenotypic plasticity, defined as 1997; Van Buskirk, 2002; Berendonk, Barraclough &
the ability of a single genotype to produce different Barraclough, 2003). However, the evolution of plasticity
phenotypes in response to different environments may be constrained by several mechanisms. For
(Schlichting & Pigliucci, 1998; Pigliucci, 2001). example, absolute constraints (sensu Brakefield, 2006)
Phenotypic plasticity exists in many species and in arise because the basic body plans of species are quite
response to a wide range of environmental conditions, ‘difficult’ to change by natural selection (i.e. new traits
Correspondence: Jason T. Hoverman, Department of Forestry and Natural Resources, Purdue University, West Lafayette, IN 47907, U.S.A.
E-mail: jhoverm@purdue.edu
© 2014 John Wiley & Sons Ltd 11011102 J. T. Hoverman et al.
that break the constraint may be deleterious). Addition- how they respond to shell-invading versus shell-crush-
ally, allocation tradeoffs can occur when resource limita- ing predators (Dewitt, 1998; Hoverman & Relyea, 2008,
tion constrains simultaneous investment in multiple 2009; Bourdeau, 2009). Thus, interspecific differences in
traits (Dewitt, 1998; Auld, Agrawal & Relyea, 2010). expansion rate, coupled with constraints on shell thick-
These constraints, combined with the amount of envi- ness, could influence patterns of phenotypic plasticity
ronmental heterogeneity experienced by a species over and phenotypic diversification of snail species (Edgell &
time or space, can drive the evolution of different mean Miyashita, 2009).
phenotypes in closely related species (i.e. averaged We examined the inducible defences of three closely
across all environments), as well as different directions related planorbid snails (Helisoma trivolvis, H. anceps and
and magnitudes of phenotypic plasticity (Van Tienderen, H. campanulata; Fig. 1) to determine how these snails
1991; Dewitt, Sih & Wilson, 1998; Schlichting & Pigliucci, respond to predators with different foraging modes,
1998; Pigliucci, 2001; Van Kleunen & Fischer, 2007; Auld given the absolute constraints and allocation tradeoffs
et al., 2010). Because closely related species are likely to that limit shell morphology. The three snail species
be similar in biochemical, physiological and structural occur together in semipermanent to permanent water-
constraints, comparative studies have the potential to bodies, where they encounter a diversity of predators
identify a core set of constraints that may limit the including water bugs, crayfish and fish (Hoverman et al.,
expression of environmentally induced traits, which 2011). In a series of studies, we have explored the
may bias evolution towards ‘fixed’ solutions to environ- responses of H. trivolvis to different predators (Hover-
mental heterogeneity (Pfennig et al., 2010). man, Auld & Relyea, 2005; Hoverman & Relyea, 2007a,b,
The inducible defences of freshwater snails represent 2008, 2009). In the presence of the water bug Belostoma
an ideal system to assess how absolute constraints and flumineum, H. trivolvis invests in shell coiling but the
allocation tradeoffs may influence the divergent evolu- aperture remains relatively small because of their
tion of plasticity across species. For example, shell geom- moderate expansion rate; this reduces the ability of the
etry creates constraints on shell shape. The shells of bug to reach the snail’s soft tissues when withdrawn
most gastropods can be described using three parame- inside the shell. In contrast, H. trivolvis forms thicker
ters: expansion rate (W), translation (T) and distance (D) shells in the presence of the crayfish Orconectes rusticus,
of the generating curve from the axis of coiling (Raup, which reduces the predator’s ability to crack or crush
1962; Rice, 1998). Physical relationships among these the shell.
shell parameters limit shell shape (i.e. not all regions of In contrast to the extensive research on H. trivolvis,
morphospace can be achieved) and therefore affect the there appear to be no studies on the predator-induced
range of options for morphological defences against var- morphology of H. campanulata and H. anceps. Among the
ious predators. For example, species with rapid shell three species, the main difference in shell shape is the
expansion rates (i.e. a coiling tube that rapidly increases rate of shell expansion (Raup, 1962). Visual inspection
in diameter) produce shells with relatively large aper- suggests that the expansion rate is low for H. campanula-
tures, which are more vulnerable to predators that enter
the shell. However, these species can invest more in
shell thickness, a defence against shell-crushing preda-
tors, because fewer coils around the central axis are
needed to increase overall body size (Raup, 1962). Alter-
natively, snails with slow expansion rates generate shells
with relatively small apertures that are difficult to enter,
although such shells are typically thinner because more
coils around the central coiling axis are required to grow
to a particular body size (Raup, 1962). In addition to
absolute constraints on shell geometry, snails also Fig. 1 Left side (i.e. spire) view of Helisoma anceps, H. campanulata
face allocation tradeoffs (Dewitt & Langerhans, 2003; and H. trivolvis. These three species differ in the rate at which the
Hoverman & Relyea, 2007a, 2009); for instance, there can diameter of the shell increases with each rotation around the
be a tradeoff between investing a limited amount of coiling axis (termed w; Raup, 1962); w is low for H. campanulata,
intermediate for H. trivolvis and high for H. anceps, respectively. As
shell material to thickness or coiling (Russell-Hunter, a consequence of variation in w, H. anceps exhibits a relatively large
1978; Kemp & Bertness, 1984; Brodersen & Madsen, aperture for a given body mass, whereas H. campanulata exhibits a
2003). As a result, snails commonly face tradeoffs in relatively small aperture.
© 2014 John Wiley & Sons Ltd, Freshwater Biology, 59, 1101–1112Defensive strategies of Helisoma snails 1103
ta, intermediate for H. trivolvis and high for H. anceps. of pond water, containing periphyton, phytoplankton
Consequently, H. campanulata has a relatively small shell and zooplankton, to sustain food for snails and maintain
aperture relative to its overall size, whereas H. trivolvis water quality. Each pool received 100 juvenile snails of
has an intermediate aperture and H. anceps has a rela- the appropriate species. Initial mean mass 1 SD of
tively large aperture. Additionally, shell thickness also H. trivolvis, H. anceps or H. campanulata was 2.0
appears to differ among species; shells are relatively 1.4 mg, 1.2 0.6 mg and 1.5 0.9 mg, respectively. For
thick for H. anceps, intermediate for H. trivolvis, and rela- each snail species, 20 snails were set aside to assess mor-
tively thin for H. campanulata (Osenberg & Mittelbach, tality due to handling; 24-h survival was 100%.
1989; Brown, 1998). After adding the snails, we placed a single predator
These differences in basic shell geometry and thick- cage into each pool. The cages were made from corru-
ness might constrain the predator-induced defences of gated pipes (10 cm long 9 10 cm diameter) capped with
each species, resulting in differences in predation risk by shade cloth. For caged predator treatments, we added
shell-invading versus shell-crushing predators. For one water bug or crayfish to each cage. Caged predators
example, because H. anceps has a thick shell and a high emit water-borne chemical cues, which provide the
shell expansion rate, it should be well defended against opportunity for prey to detect and respond to predators
shell-crushing predators but vulnerable to shell-invading without reducing prey density (Chivers & Smith, 1998).
predators. Because H. campanulata has a thin shell with a The caged predators were fed 300 mg of snail biomass
low shell expansion rate, it should be well defended (total wetmass including shells, two to five snails) of the
against shell-invading predators but vulnerable to crush- appropriate snail species three times per week. Based on
ing predators. To test these hypotheses experimentally, previous research, this amount of consumed snail bio-
we assessed the phenotypic responses of the snails to mass by the predators is sufficient to elicit phenotypic
water bugs or crayfish and then examined the relative responses in H. trivolvis (Hoverman & Relyea, 2007b,
susceptibility of each snail species to the predators. 2008, 2009). The predators consumed all the snails
between feedings. To equalise disturbance, we briefly
lifted the cages in the no-predator treatment from the
Methods water and then returned them. We placed a shade cloth
lid over each pool to prevent colonisation by insects and
Induction experiment
amphibians.
The goal of the induction experiment was to assess During the experiment, we observed that the spe-
predator-induced morphology in the three Helisoma spe- cies varied greatly in growth rates; growth was fast in
cies. We collected ~100 adults of H. trivolvis, H. anceps H. trivolvis, intermediate in H. campanulata and slow in
and H. campanulata from ponds near the University of H. anceps. Because analyses of morphological plasticity
Pittsburgh’s Pymatuning Laboratory of Ecology (PLE) in are sensitive to differences in mass, we decided to take
Linesville, PA. These ponds contain both water bugs down the experimental units for each species at different
(Belostoma flumineum) and crayfish (Orconectes rusticus). times so that they were similar in mass at the end of the
For each snail species, 10 individuals were placed into experiment. Although this approach resulted in differ-
each of 10 culture pools filled with 100 L of well water. ences among the species in duration of predator expo-
Egg deposition began immediately and continued until sure, our previous work with H. trivolvis found that the
the adults were removed after 2 weeks. Upon hatching, magnitude of predator-induced morphological change is
snails were fed rabbit food ad libitum until the experi- relatively constant over ontogeny (Hoverman & Relyea,
ment began. 2007a, 2009). For H. trivolvis, H. campanulata and
In a mesocosm experiment, we examined the effects of H. anceps, the experiment was ended after 14, 21 and
caged predators on the growth and morphology of each 39 days, respectively. On each date, all surviving snails
species. We designed a completely randomised, factorial were removed and preserved in 10% formalin. In one
experiment composed of three predator treatments (no experimental unit, all the H. campanulata died and this
predator, caged water bug [B. flumineum], or caged cray- was excluded from analyses. For the remaining experi-
fish [O. rusticus]) crossed with the three snail species. mental units, survival was high (>95%) and did not
These nine treatments were replicated eight times for a differ among caged predator treatments or snail species
total of 72 experimental units. (predator, F2,63 = 0.7, P = 0.499; species, F2,63 = 0.3,
The experimental units were 90-L pools filled with P = 0.706; interaction, F4,63 = 1.3, P = 0.274). For each
well water. We added 10 g of rabbit food and an aliquot experimental unit, 10 individuals were randomly
© 2014 John Wiley & Sons Ltd, Freshwater Biology, 59, 1101–11121104 J. T. Hoverman et al.
selected and dried at 60 °C for 24 h. Each individual assess the significance of the 10 correlations that were
was then weighed to the nearest mg (total dry mass conducted.
included shell and tissue) and measured for shell width
and height, and aperture width and height using digital
Predation trials
imaging software (Optimas Co., Bothell, WA, U.S.A.).
We also measured the shell thickness of each snail at the For the predation trials, the objective was to test preda-
leading edge of the aperture using digital calipers. tor preference for the different snail species after
To examine the effects of our caged predator treat- defences in response to the cues of water bugs or cray-
ments on snail morphology, we began by assessing the fish had been induced. Pilot experiments indicated that
allometric relationship between each shell dimension the two species of predators were capable of consuming
and log10-transformed mass. While there was no rela- all three species of snails when they were small and of
tionship between shell thickness and mass for each spe- similar mass (i.e. ~50 mg dry mass; R.D. Cothran et al.
cies, the remaining shell dimensions showed positive unpublished data), but the key issue is the predation
relationships with mass. To account for these allometric risk when predators are given a choice of all three spe-
relationships, we used analysis of covariance (ANCO- cies that have been exposed to predator cues for the
VA) with mass as a covariate and snail species and same amount of time. Because the species differ not
predator treatment as main effects. A critical assumption only in relative shape but also in size (i.e. they grow at
in the ANCOVA procedure is that the treatments share different rates), the predation trials tested how the
a common regression slope and our data met this entire suite of traits affects relative predation risk when
assumption (tests of interactions with mass all a predator is given a choice among the three snail spe-
P ≥ 0.171). From the ANCOVA, we used the estimated cies. In short, the predation trials were designed to
marginal means and residuals from within-treatment assess differences in predation risk using the typical
regressions to calculate a mass-adjusted value for each variation in size and shape of snails that would occur
individual. Using all the measured individuals in the in nature.
ANCOVA, we had ample power to capture the allomet- For each snail species, we collected 100 adult snails
ric relationship between shell dimensions and mass. For from the E.S. George Reserve in Livingston County, MI,
each shell dimension, we then calculated the mean size- U.S.A. The three species were collected from a single
adjusted shell dimensions for each experimental unit pond (Crane pond) that contained both predators (Hov-
and used these means as the morphological response erman et al., 2011). For each snail species, we divided
variables. Because shell thickness did not covary with individuals equally among five 100-L wading pools (i.e.
mass, we calculated the mean shell thickness for the 20 per pool) and allowed them to deposit egg masses
snails from each experimental unit and this served as for 2 weeks. After hatching, the juvenile snails were fed
the response variable. rabbit food ad libitum until the start of the experiment.
We used a multivariate analysis of variance (MANO- Water bugs and crayfish were collected from local ponds
VA) to analyse the effect of caged predators and snail and housed in the laboratory, where they were fed
species on final mass, mass-adjusted shell dimensions snails weekly until used in the predation trials.
(shell width and height, and aperture width and height) For each snail species, we created water bug- and
and shell thickness. The data were normally distributed, crayfish-induced snails by raising them in 90-L wading
and variances were equal across treatments. Significant pools (n = 6 for each snail species and predator combi-
multivariate effects were followed by univariate tests. nation, for a total of 36 pools). These pools contained
When univariate tests were significant, we conducted either a caged crayfish or a caged water bug and were
mean comparisons using Tukey’s HSD test. We also con- set up identically to the pools used in the induction
ducted correlation analyses to examine the relationships experiment. We added 60, 1-week-old snails of the
between the morphological traits and assess whether appropriate species to each pool.
allocation tradeoffs were evident across snail species We tested the snails for their relative susceptibility to
and predator treatments. For each pairwise combination a given predator after being exposed to predator cues
of the five morphological traits, we calculated the Pear- for 2 weeks (i.e. juvenile snails) and again after 5 weeks
son product–moment correlation coefficient across the (i.e. adult snails). For each snail species and predator
nine experimental treatments. We used the mean trait combination, we collected 20 snails from each of the six
value for each experimental unit in the analysis induction pools and combined them for a total of 120
(N = 71). We used a Bonferroni-corrected a = 0.005 to snails that could be randomly assigned to predation
© 2014 John Wiley & Sons Ltd, Freshwater Biology, 59, 1101–1112Defensive strategies of Helisoma snails 1105
trials. We randomly selected a subsample of snails from Table 1 Results of a MANOVA (Wilks’ k with F approximations)
each treatment combination to test for species differ- on the effects of snail species and caged predator species on snail
mass, shell and aperture shape, and shell thickness. Univariate tests
ences in mass (mg oven-dried mass including shell). (P-values) are shown for both main effects and their interaction
Using these induced animals, we randomly selected
10 individuals from each of the three snail species and Multivariate tests d.f. F P
added the combined 30 animals to each experimental Species 12,114 198.71106 J. T. Hoverman et al.
Fig. 2 The effects of caged predator
treatments on the dry mass, size-adjusted
shell morphology and shell thickness of
Helisoma anceps, H. campanulata and
H. trivolvis. Data are means 1 SE. For
each species, treatments sharing lower
case letters are not significantly different
from each other based on pairwise com-
parisons using Tukey’s HSD test
(P > 0.05).
were also positive associations between shell width, the largest species followed by H. campanulata and
shell height and aperture height (r ≥ 0.526, P ≤ 0.001, H. anceps (pairwise comparisons between H. trivolvis and
n = 71). The remaining correlations were not significant the other two species both P < 0.001; between H. anceps
(P ≥ 0.029; Bonferroni-corrected a = 0.005). and H. campanulata P = 0.053).
Survival depended on the species of snail and the
species of predator (snail species-by-predator type
Predation trials after 2 weeks of exposure to predator cues
interaction: F2,17 = 13.0, P < 0.001; Fig. 4b). As a result,
We examined the susceptibility of the three Helisoma we split the data set by predator species to test for dif-
species after being induced by water bugs or crayfish ferences in vulnerability among the three snail species.
for 2 weeks. Following 2 weeks of induction, there was Survival with uncaged water bugs differed among the
no effect of predator species on snail mass (F1,53 = 1.9, three species (F2,8 = 11.0, P = 0.005; Fig. 4b). Compared
P = 0.178), and there was no interaction between snail with H. anceps, H. trivolvis and H. campanulata were
species and predator species (F2,53 = 0.4, P = 0.706). about three times more likely to survive (P = 0.003 and
However, the three snail species did differ in mass P = 0.012, respectively). Survival did not differ between
(F2,53 = 161.1, P < 0.001; Fig. 4a); Helisoma trivolvis was H. campanulata and H. trivolvis (P = 0.678). Survival with
© 2014 John Wiley & Sons Ltd, Freshwater Biology, 59, 1101–1112Defensive strategies of Helisoma snails 1107
(a) (a)
(b)
(b)
(c)
(c)
Fig. 3 The association between shell thickness and shell shape
[shell width (a), shell height (b) and aperture height (c)] across the
nine experimental treatments. For each snail species (Helisoma an-
ceps, H. campanulata and H. trivolvis), the trait means are presented
for the experimental units within each predator treatment (no pred-
ator, caged water bugs and caged crayfish).
Fig. 4 Mass and survival of Helisoma anceps, H. trivolvis and
uncaged crayfish was marginally non-significant among H. campanulata in the predation trials after 2 and 5 weeks of induc-
the three snail species (F2,8 = 3.8, P = 0.069). Helisoma tion. The three species were either induced by caged water bugs
anceps was 1.5 times more likely to survive than H. cam- and then subjected to predation by lethal water bugs or induced by
caged crayfish and then subjected to predation by lethal crayfish:
panulata (P = 0.075). All other pairwise comparisons
(a) mass of each species of snail at the start of a predation trial
were insignificant (all P ≥ 0.12). (closed symbols are 2 weeks and open symbols are 5 weeks), (b)
survival of induced snails against lethal crayfish or lethal water
bugs following 2 weeks of predator induction, (c) survival of
Predation trials after 5 weeks of exposure to predator cues induced snails against lethal crayfish or lethal water bugs following
5 weeks of predator induction. Data are means 1 SE.
After being induced by predators for 5 weeks, we again
compared the mass and survival of the three snail spe- observed after 2 weeks of induction, H. trivolvis was
cies. In regard to mass, there was no effect of predator largest followed by H. campanulata and H. anceps (all
(F1,54 = 1.5, P = 0.23) and no interaction between snail pairwise comparisons P < 0.001).
species and predator species (F2,54 = 0.4, P = 0.693). Snail survival depended on the predator that was
However, the three snail species differed in mass present (F2,17 = 5.1, P = 0.018; Fig. 4c); therefore, we split
(F2,54 = 133.28, P < 0.001; Fig. 4a); similar to the pattern the data set by predator. Survival in the presence of
© 2014 John Wiley & Sons Ltd, Freshwater Biology, 59, 1101–11121108 J. T. Hoverman et al.
uncaged water bugs differed among the three snail inducing predator, but the lack of response to the alter-
species (F2,8 = 168, P < 0001). None of the H. anceps native predator might increase risk in the presence of
survived, whereas survival was high for H. campanulata that predator (a hypothesis later tested in the predation
and H. trivolvis (comparisons against H. anceps: both trials).
P < 0.001; H. campanulata versus H. trivolvis: P = 1.0). The differences in morphological responses to water
Survival with uncaged crayfish also differed among the bugs between the species appear to reflect the geometric
three snail species (F2,8 = 158, P < 0.001). Few H. anceps constraints of shell shape. While all three species have
survived, whereas most of the H. campanulata and H. tri- planospiral coiling, H. campanulata and H. trivolvis have
volvis did (comparisons with H. anceps: both P < 0.001; low expansion rates, so the diameter of their coiled tube
H. campanulata versus H. trivolvis: P = 0.486). increases only gradually as whorls are added. In contrast,
H. anceps has a high expansion rate, so the diameter of its
coiled tube increases substantially as more whorls are
Discussion
added. Consequently, H. campanulata and H. trivolvis can
We found that Helisoma trivolvis, H. anceps and H. cam- respond to water bugs by increasing shell width (i.e. rap-
panulata all expressed predator-induced plasticity, yet idly growing a longer coiled tube) because this places the
they exhibited individual responses to the predators. aperture of the shell further away from the soft tissue of
The responses of H. trivolvis to caged predators were the snail, without substantially increasing the size of the
consistent with previous research on this species aperture; this makes it harder for a water bug to reach
(Hoverman et al., 2005; Hoverman & Relyea, 2007b). and pierce the soft tissues. If H. anceps was to respond to
When exposed to water bug cues, they formed wider water bugs in this manner, the soft tissue would be fur-
shells (i.e. coiled more) but aperture size did not change. ther from the aperture, but the aperture would also
These responses enable H. trivolvis to withdraw into its become much larger and easier for a water bug to enter
shell, which reduces the water bug’s ability to access the and pierce the soft tissues. This geometric constraint of
snail’s soft tissues (Hoverman & Relyea, 2009). They H. anceps may explain its lack of morphological response
formed thicker shells when exposed to crayfish cues, to water bugs.
which reduces shell-crushing or chipping by crayfish The existence of allocation tradeoffs is an underlying
(Hoverman & Relyea, 2009). Given the adaptive value of assumption of phenotypic plasticity (Schlichting & Pig-
these responses for H. trivolvis and the co-occurrence of liucci, 1998; Tollrian & Harvell, 1999; Pigliucci, 2001).
H. anceps and H. campanulata with the same predators, Using correlation analyses, we found strong evidence for
we predicted similar phenotypic responses across the allocation tradeoffs across the experimental treatments;
snail species. However, the morphology of H. anceps and investment in shell thickness was negatively correlated
H. campanulata changed in response to one or the other with investment in shell shape. Thus, in addition to geo-
predator but not to both. Helisoma anceps responded to metric constraints on shell shape, snails face allocation
crayfish by forming thicker shells, narrower shells and tradeoffs that constrain their ability to invest simulta-
apertures, and lower shells and apertures; however, neously in shell thickness and shape. These results are
there was no response to water bugs. Helisoma campanu- consistent with previous work in marine snails. For
lata responded to water bugs by forming wider and instance, Trussell & Nicklin (2002) found a negative asso-
lower shells and low apertures, although there was no ciation between shell length and thickness in Littorina
response to crayfish. Although there were no obtusata. This allocation tradeoff appears to be driven by
morphological responses in H. anceps and H. campanulata competing demands for calcium, such that thicker shells
when exposed to water bugs and crayfish, respectively, can only be produced when investment in shell length is
mass did change. Specifically, H. anceps was smaller reduced (Palmer, 1981; Kemp & Bertness, 1984).
with caged water bugs while H. campanulata was larger As a consequence of allocation tradeoffs, snails are
with caged crayfish. Thus, both species did detect these faced with a fundamental tradeoff between responses to
predators, but morphology did not respond. Interest- shell-entering and shell-crushing predators. In H. trivol-
ingly, the predator-specific morphological responses vis, the induction of wider shells, by extending the length
observed in H. anceps and H. campanulata to crayfish and of the coiled tube, makes it more difficult for water bugs
water bugs, respectively, are similar to many of the to enter the aperture and pierce the soft tissue (Hoverman
adaptive responses observed in H. trivolvis. Thus, the & Relyea, 2009). However, this comes at the cost of
responses of H. anceps to crayfish, and the responses of reduced investment in shell thickness, which makes the
H. campanulata to water bugs, might reduce risk to each shell more vulnerable to crushing predators such as
© 2014 John Wiley & Sons Ltd, Freshwater Biology, 59, 1101–1112Defensive strategies of Helisoma snails 1109 crayfish. Similarly, the body plan of H. campanulata is well relative predation risk. In this trial, all three species were suited to defence against water bugs, because it can rap- within a mass range that could be consumed by either idly grow a long, thin tube that makes it difficult for water predator (R.D. Cothran et al., unpublished data), but the bugs to reach the soft tissue. However, this strategy leaves survival of each snail species with uncaged crayfish or few resources for thickening the shell making H. campanu- water bugs was strongly associated with the observed lata vulnerable to crushing predators such as crayfish. In changes in mass and morphology. When crayfish- other freshwater and marine snails, research has also doc- induced snails were exposed to crayfish, survival was umented contrasting responses to predators with diver- high for H. anceps, intermediate for H. trivolvis and low gent foraging modes that appear to be driven by for H. campanulata. This was particularly interesting allocation tradeoffs (Dewitt, Robinson & Wilson, 2000; because H. anceps was the smallest of the three species, Bourdeau, 2009). For instance, Bourdeau (2009) showed yet it was the best defended against crayfish. When that the marine snail, Nucella lamellosa, forms thick, round water bug-induced snails were exposed to water bugs, shells when exposed to shell-crushing crabs but elongate survival was low for H. anceps and high for H. trivolvis shells with shell-entry seastars. Thus, morphological and H. campanulata. Comparing the mass of H. trivolvis defences in snails appear to be driven by a fundamental and H. campanulata, the latter was considerably smaller, tradeoff between shell thickness and shape. yet its morphological defences against water bugs were Our study focussed on morphological responses to pre- stronger. In contrast, H. campanulata and H. anceps were dators, yet behavioural responses have also been more similar in mass, yet H. campanulata had better observed in H. trivolvis and other snails (Dewitt, Sih & survival, further confirming that the morphological Hucko, 1999; Turner, Bernot & Boes, 2000; Hoverman responses to water bug cues provided H. campanulata et al., 2005; Hoverman & Relyea, 2007b). Behavioural with effective defences against water bugs. These results responses often involve spatial avoidance, such that snails are consistent with the argument that snails with move into areas that provide shelter (e.g. rock refuges) or relatively wider shells are better defended against water are difficult for the predator to reach (e.g. the water sur- bugs and snails with thicker shells are better defended face). In our previous work, we did not detect behaviour- against crayfish. al responses to water bugs because this predator is After being exposed to predator cues for 5 weeks, we capable of foraging for snails throughout the water col- observed that H. trivolvis and H. campanulata had umn and under ‘refuges’ (Hoverman et al., 2005; Hover- very high survival with both uncaged predators while man & Relyea, 2007b). However, snails often move H. anceps had very low survival. The main driver of towards the water surface or above the water line in the these contrasting outcomes of predation with time presence of crayfish (Hoverman et al., 2005), although appears to be the occurrence of size refuges from preda- such responses are not always observed (Hoverman & tion. We have previously shown that adult H. trivolvis Relyea, 2007b). As crayfish are largely benthic, this behav- can reach a size refuge against both water bugs and iour can reduce the probability of encounter. While crayfish, regardless of their shell phenotype (Hoverman behaviour was not quantified in our experiments, it is & Relyea, 2009). Thus, it appears that H. trivolvis and possible that it could play an important role in the H. campanulata exceeded the size required to reach a ref- defences of these snails. For instance, several studies have uge from both predators, whereas H. anceps was still demonstrated trait compensation, where individuals with vulnerable. As a result, it appears that the inability of poorly formed morphological defences display strong either predator to consume H. trivolvis and H. campanu- behavioural responses to predators (Dewitt et al., 1999; lata shifted all of the predation pressure to H. anceps, Rundle & Br€ onmark, 2001; Cotton, Rundle & Smith, 2004; thereby causing much lower survival of this species. In Rundle et al., 2004). Thus, it is possible that H. campanula- short, when the snails of any species are within a vul- ta and H. anceps could display anti-predator behaviours nerable size range, morphological defences are impor- in the presence of crayfish and water bugs, respectively, tant for reducing predation risk, but when a species compensating for their vulnerable shell morphology. achieves a size refuge, the morphology of the large spe- Additional research is necessary to explore whether cies becomes unimportant to predation risk and preda- behavioural responses are employed by these species. tion can become more intense on the small species in The results of the predation trials conducted after the community; even when the small species has a 2 weeks of exposure to the cues of water bugs or defended phenotype. One of the limitations of our crayfish demonstrated how the phenotypes of the snails, experimental design was that we used a narrow size when all three species were combined, affected their range for each predator species. Although there is little © 2014 John Wiley & Sons Ltd, Freshwater Biology, 59, 1101–1112
1110 J. T. Hoverman et al.
variation in the size of adult water bugs, crayfish can of possibilities: specialised defences against a shell-crush-
attain a larger size than represented in our study. As ing predator, specialised defences against a shell-invading
adults, crayfish tend to shift to more herbivorous diets, predator and generalised, flexible defences against both
but their greater size does allow them to feed on larger predators. Theory predicts that a population should
macroinvertebrates (Lodge & Lorman, 1987; Lodge et al., evolve either fixed or plastic phenotypes depending on
1994). Because larger crayfish can consume larger prey, the costs and benefits of alternative phenotypes and the
it is possible that the results of the predation trials after frequency of alternative environments (Pfennig et al.,
5 weeks of induction would be different if larger cray- 2010). However, our work suggests that species can
fish were selected for the experiment. However, if snails become somewhat specialised to a given environment, yet
were not in a size refuge from predation, we would still maintain some plasticity. This may reflect a condition
expect the results to be similar to the outcome observed in which the plasticity has not yet achieved fixation for a
in the predation trials after 2 weeks of induction. constitutive defence. Alternatively, it may simply be that
While predation is a common threat for freshwater each specialist most commonly experiences the presence
snails that has been hypothesised to affect patterns in or absence of one type of predator over space and time
species richness, species abundance and community (e.g. environments containing either no predators or a
structure (Lodge et al., 1987; Dillon, 2000), our shell-crushing predator) but rarely experiences the other
understanding of how inducible defences contribute to type of predator (e.g. a shell-invading predator). In such a
patterns in species distribution and abundance remains scenario, there would be little selective pressure to evolve
limited. Theory suggests that species with inducible responses to the other type of predator. While more
defences against a number of predators (i.e. generalists) research needs to be conducted on this system to under-
should be more broadly distributed than species that stand how selection shapes the evolution of phenotypic
specialise for a particular predator (Agosta & Klemens, plasticity, it is clear that an understanding of absolute
2008). We find support for this prediction for snail meta- constraints on body shape, combined with knowledge of
communities in Michigan, U.S.A. (Hoverman et al., allocation tradeoffs, can provide critical insights into the
2011). Helisoma trivolvis is the most broadly distributed mechanisms that produce interspecific variation in the
of the three species with a range that spans temporary expression of phenotypic plasticity and patterns of
ponds to permanent lakes, H. campanulata is found in phenotypic diversification.
semi-permanent ponds to lakes, and H. anceps is only
found in a subset of lakes. Across this habitat gradient,
Acknowledgments
there is also a gradient in predator composition; water
bugs are more frequently found in temporary and We thank N. Diecks, B. French, D. Jones, P. Monahan, P.
semipermanent ponds, while crushing predators such as Noyes and A. Stoler for their assistance with the
crayfish and fish are more common in permanent lakes experiment and S. Bagnull for measuring the snails. This
(Hoverman et al., 2011). In addition to predation, work was supported by a National Science Foundation
however, factors such as habitat size, hydroperiod and grant to RAR, and grants from the Conchologists of
competition can structure snail assemblages (Lodge America, the Pennsylvania Academy of Science, and
et al., 1987; Dillon, 2000; Hoverman et al., 2011). Sigma Xi to JTH.
Freshwater habitats also vary in abiotic conditions that
could influence the interaction between snails and their
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