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The effect of wave action, prey type, and foraging time on growth of the predatory snail Nucella lapillus (L.)
Journal
Marine Biology and Ecology 196 (1996) 341-356
of Experimental
JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY
The effect of wave action, prey type, and foraging time on growth of the predatory snail Nucda ZapiZZus(L.) Ron J. Etter Biology Department,
University
of Massachusetts, 100 Morrissey Blvd., Boston, MA 0.2125, USA
Received 2 February 1995; revised 28 June 1995; accepted 27 July 1995
Abstract Growth rates of intertidal snails vary among populations differentially exposed to wave action; individuals from sheltered habitats typically grow more quickly than do those from more exposed coasts. A series of field and laboratory experiments were conducted to separate the genetic and phenotypic components of this variation in Nucella lapillus (L.) and to investigate the extent to which prey type and foraging time, which also vary across the wave-exposure gradient, affect growth. Juvenile and adult whelks were reciprocally transplanted between an exposed and a protected shore and subsequent growth followed. Independent of origin, whelks grew more on the sheltered shore. By contrast, growth rates for snails from exposed and protected shores were similar when reared under uniform conditions in the laboratory. Together these findings suggest that the variation observed in nature does not represent genetic differentiation, but reflects the influence of proximal factors that depress growth on wave-swept shores. Growth rates of juveniles from exposed and protected shores maintained in the laboratory on a diet of an overabundance of (1) barnacles, (2) mussels, (3) both, and (4) both, but only 67% of the time, indicated that prey type and foraging time affect growth. Whelks grew best on a diet of mussels, either singly or in combination with barnacles, grew less on barnacles alone. and least when foraging time was restricted. Because growth rates on specific prey in the laboratory were opposite the observed trend in nature, variation in prey across the exposure gradient cannot be invoked to account for the difference in growth between N. fapillus from exposed and protected shores. The slower growth rates when foraging time was restricted are consistent with the notion that wave energies on exposed coasts depress growth by limiting foraging time or by reducing foraging efficiency. Keywords:
Growth;
Intertidal;
Life-history;
0022-0981/96/$15.00 @ 1996 Elsevier SSDI 0022-0981(95)00139-5
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Nucella;
Wave-action
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1. Introduction Intraspecific variation in life histories is ubiquitous in nature and several theoretical models have been developed to predict under what selective pressures particular characteristics might evolve (reviewed in Stearns, 1992). Variation in life histories may be due to genetic differences among individuals, phenotypic plasticity induced by environmental variation or a combination of both (e.g. Reznick, 1982; Berven and Gill, 1983; Brown, 1983, 1985; Stearns, 1983; Travis, 1983; Allan, 1984; Scheiner and Goodnight, 1984; Crow1 and Covich, 1990; Lafferty, 1993; Dugan et al., 1994, Wellborn, 1994). It is essential to sort out the relative contribution of plastic and genetic variation because evolutionary arguments regarding the adaptive significance of life history variation are moot until the extent of genetic variation has been identified (Stearns, 1976, 1977). Although it is difficult to test the mechanisms underlying genetic differentiation in life histories for organisms with long generation times, those forces affecting the plastic components of variation are more amenable to experimental verification (Stearns, 1980; Berven, 1982; Crow1 and Covich, 1990) and are perhaps equally important in understanding life history variation (Stearns and Koella, 1986; Baird et al., 1987; Berrigan and Charnov, 1994; Berrigan and Koella, 1994). The rocky intertidal snail Nucella lapillus (L.) exhibits remarkable variability in its life history traits among populations differentially exposed to wave action (Etter, 1989). Whelks from wave-swept shores grow more slowly, mature at a smaller size, suffer higher mortality, and produce many more offspring than do conspecifics at more sheltered habitats. Similar patterns have been observed in a number of other intertidal snails (Hughes and Roberts, 1981; Janson, 1982, 1983; Atkinson and Newbury, 1984; Brown and Quinn, 1988: Behrens Yamada, 1989). Although this variation fits accepted schemes of life history evolution, it is unclear to what extent the variation represents genetic differentiation or phenotypic plasticity. We are equally nescient of the proximal forces that shape variation in these life histories. The work described in this paper was designed to determine to what extent differences in growth rates among snails from different exposure regimes were due to genetic or environmental influences, and experimentally test the plausibility of a variety of hypotheses invoked to account for the interhabitat variation in growth. The growth rate of an organism is an essential feature of its life history. Because growth rates can influence fitness in several ways, it is often used as a surrogate for fitness, especially in snails (Palmer, 1983; Moran et al., 1984; Brown and Quinn, 1988; West, 1988; Burrows and Hughes, 1990). For example, because fecundity is typically a positive function of size (Spight et al., 1974; Spight and Emlen, 1976; Palmer, 1983; Crothers, 1985), faster growing snails have the potential to produce more offspring at any particular age. Small snails are also generally more vulnerable to predation than are large snails (Feare, lY66: Richardson and Brown, 1992). For N. lapillus, once it attains a size that exceeds 15mm, mortality due to predation is low (Etter, 1988b). The growth rate therefore determines the amount of time N. lapillus is vulnerable to predation. Recent
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343
theoretical and empirical work has shown that by altering reaction norms, growth rates can have important direct and indirect affects on other life history traits (Stearns and Koella 1986; Berrigan and Charnov, 1994; Berrigan and Koella, 1994). An understanding of the forces modulating growth rates may yield important insights into variation in other life history traits. The variation in growth rates of N. lupillus among shores differentially exposed to wave action may reflect a variety of factors including genetic differentiation, the relative density and quality of food, foraging efficiency and/or energy allocation to other needs (e.g. maintenance and reproduction). These putative influences are, of course, not mutually exclusive. I consider the importance of three potential factors. Nucellu lupillus lacks a dispersal stage in its life cycle and adults have a small (
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341L.156
Therefore, the slower growth on wave-swept shores may reflect a diet high in mussels. To determine the importance of prey type in affecting growth rates, juvenile and adult whelks were fed a diet of barnacles, Semibalanus balanoides (L.), and mussels, Myths edulis L. and subsequent growth followed.
2. Methods 2.1. Reciprocal
transplant experiment
Whelks for the reciprocal transplant experiment were collected from an exposed (No Name Point, Nahant, MA) and a protected shore (Mackeral Cove, Beverly, MA), returned to the laboratory and maintained in water tables supplied with running seawater. Juveniles were collected in May, but collection of adults was delayed until June. By June, most whelks had finished depositing egg capsules, and thus transferring adults between an exposed and protected shore at this time would limit the extent of unnatural gene flow among populations. An entire size range of whelks was collected from each site and, based on size, individuals were classified as either juveniles (exposed 515 mm, protected 520 mm) or adults (exposed ~19 mm, protected ~24 mm). The specific size used to separate juveniles from adults in each population was selected based on the typical size at which whelks begin to mature in each population (Etter, 1989). Snails were tagged and the maximum shell length (~0.05 mm) recorded. Shell length was measured with vernier calipers as the maximum distance between the shell apex and the tip of the siphonal canal. After marking, exposed morphs were separated into two groups; (1) approximately two-thirds were returned to a separate exposed shore (Bennett Head, Nahant, MA) ( = residents). and (2) the other third were transferred to a protected shore (a separate shore at Mackerel Cove) ( = transferred). Tagged individuals from the protected shore were treated in a similar manner. Rather than release half the whelks at each site as is typical of reciprocal transplant experiments, slightly more were used at the exposed shore to offset the higher mortality rates suffered by whelks at this site (Etter, 1989). The only exception to this procedure was for exposed juveniles which were equally split between the exposed and protected shore. The rationale for an equal split in this case was that I expected mortality rates of exposed juveniles to be high on the protected shore because they tend to possess thin. pigmented shells increasing their vulnerability to the greater physiological stress (Etter, 198Sb) and the more intense predation (Kitching et al., 1966; Menge, 1983) on protected shores. A quantity of whelk biomass similar to the biomass released was removed from each site to prevent artificially increasing biomass. All tagged whelks were recollected in October, and their shell lengths recorded. Growth rates were estimated from changes in shell length over the duration of the experiment. Shell length was used to estimate growth because, in a separate analysis, it provided results similar to total weight, shell weight, or body weight
345
R. Etter I J. Exp. Mar. Biol. Ecol. 196 (1996) 341-3_f6
(Etter, within
1989). ANCOVA as described below and between shores and morphs.
2.2. Prey type and foraging
was used to compare
growth
rates
time experiment
Whelks for the prey quality and foraging time experiments were collected from an exposed shore (No Name Point) at Nahant, MA and a protected shore in Beverly, MA (Mackerel Cove). They were returned to the laboratory and sorted into juvenile and adult snails as described above. The adults were further divided into males and females based on the presence of a penis or a capsule gland, respectively. All individuals were tagged and maintained completely submerged in seawater tables without food for 1 wk prior to the start of the experiment. Twenty-four cages were constructed from plastic freezer containers (18 X 13.1 X 8.2 cm) by cutting windows in each panel of the container and covering the windows with nitex screen (mesh size =l mm) to permit water flow. Each cage was provided with one of four treatments; an overabundance of (1) barnacles, (B), (2) mussels (M), (3) both mussels and barnacles (MBH), and (4) both mussels and barnacles, but only 67% of the time (MBL). For each treatment, a full size range of prey from both habitats was provided. Barnacles were added by placing small rocks covered with Semibalanus balanoides in a cage and mussels (Mytilus edulis) were introduced into the cages individually and on small rocks where possible. Regardless of the prey type, all cages received one or more rocks to more closely resemble natural substrata. The procedure for the MBL treatment was to alternate between an overabundance of prey for 10 days and no prey for 5 days to simulate foraging restricted by wave action. Nucella typically forages only when immersed, although if it has begun to feed it will continue during low tide. Foraging stops when snails are emersed or during high wave energies usually associated with storms (Burrows and Hughes, 1989). By allowing snails to feed for 10 days and then removing prey for 5 days, I simulated how foraging might be restricted by storms that occur on a frequency of twice each month. The 5-day restriction is meant to reflect the increase in wave energy prior to a storm (1 day), during the storm (1.5 days) and the residual surge after a storm has passed (2.5 days). The shell length of each snail was measured and 10 juveniles, 5 males and 5 females placed in each cage. There were 6 replicate cages per feeding treatment; into half of the cages exposed morphs were added, and the remaining 3 received protected morphs. The experimental design consisted of four feeding treatments (prey type and foraging time) X two morphs (exposed or protected) X three replicates. All cages were completely submerged in a water table supplied with continuously flowing seawater. Cages were checked weekly and new prey added where necessary. The seawater was drawn from the shallow subtidal at Nahant and maintained at ambient temperature and salinity. Although the water flowed through the tables, there was no current or wave energy. The flow characteristics in the water tables resemble what snails might experience in tidepools on a very protected shore.
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Monthly changes in shell length were used as estimates of growth rates and several questions were addressed by comparing growth rates among snails. First, growth rates of juveniles reared on different diets were compared to establish whether prey type or foraging time influenced growth. Only juveniles were employed in estimating the quality of prey or the effect of foraging time on growth because, after maintenance requirements are satisfied, juveniles devote all net energy to growth whereas adults may not (Palmer, 1983). Second, to determine if exposed and protected morphs differ in growth rate when fed a specific diet, juvenile growth was compared between morphs for each experimental treatment. Adults were not used in a similar analysis because initial size differed between exposed and protected adults. Both of the above comparisons were computed for the entire experimental period (3 months) as well as for each month to investigate any temporal components in these relationships that emerged due to ingestive conditioning (Dunkin and Hughes, 1984; Hughes and Dunkin, 1984a,b; Stickle et al., 1985) or in response to changes in water temperature (Stickle et al., 1985). Third, to further investigate temporal components, growth rates of juveniles reared on a particular feeding regime were compared among months separately for exposed and protected morphs. The remaining questions were primarily concerned with possible genetic differences in growth rates among whelks and thus comparisons were made across all diets. Feeding treatments were pooled because the variability in prey type or foraging time more accurately reflects what a population of whelks as a whole might experience in nature over a specified period of time; certain individuals may only encounter mussels, others only barnacles and some both prey but either at high (MBH) or low densities (MBL). Fourth, the genetic component of variation in growth was estimated by comparing juvenile growth rates between morphs reared under similar laboratory conditions. Finally, growth rates were also compared between males and females separately for exposed and protected snails to detect differences in growth between sexes. ANCOVA on regression lines fit to modified Ford-Walford plots where growth over an interval is regressed on initial size, were used to compare all growth rates (Etter, 1989). The slope of the regression line represents the growth schedule for a particular population and the asymptotic size is given by the intersection of the regression line with the x-axis. Therefore, the slope can also be viewed as the rate at which individuals approach their asymptotic size. The displacement of the regression line (or its elevation) represents the size specific growth rate, i.e. the amount an individual initially size x will grow over the period from t to f + 1.
3. Results 3.1. Reciprocal
transplant
There was a clear environmental effect on growth rates of juvenile snails, independent of their habitat of origin (Table 1). Protected shores supported the
R. Etrer I .I. Exp. Mar. Bid.
Ecol. I96 (1996) 341-356
347
Table 1 The results of a two-way ANCOVA comparing juvenile growth rates in the reciprocal transplant experiment. The covariate was initial size of the snails Source
df
Morph Shore Size 1 Morph. Shore Morph * Size 1 Shore. Size 1 Morph. Shore. Size 1 Residual
Mean square
,F-value
p-value
12.491 53.743 50iJ.973 38.936 5.468 15.241 27.785 5.476
2.281 9.814 91.483 7.110 0.999 2.783 5.074
0.1349 0.0024 O.Ooa1 0.0093 0.3206 0.0991 0.0270
most rapid growth rates in juvenile whelks (Fig. 1). Exposed morphs reared on a protected shore increased in shell length by -9 mm whereas those remaining on an exposed shore increased by only 6 mm. Similarly, protected morphs reared on the protected shore grew more than twice as much as those reared on the exposed shore. There was no overall effect of morph, where snails originated from, but there was a sig~i~cant interaction between morph and shore (Table 1). Although protected morphs grew more than exposed morphs on the protected shore, there was no difference in growth between the morphs on the exposed shore (Fig. 1). Comparisons of growth between exposed and protected morphs within sites should be interpreted cautiously though, because the initial size of the juveniles differed slightly and growth rates are size dependent (Etter, 1989); i.e. differences
Juveniles
16
-r
7
EP
E%
Pe
PP
Morph/Shore Fig. 1. Growth increments for juvenile transplanted between shores and their E = exposed), lower case letters refer to are from an ANCOVA and have been bars = 95% confidence limits.
whelks from an exposed or protected shore reciprocally controls. Uppercase letters refer to morph (P = protected, the habitat the snails were reared in. The growth increments adjusted to the mean of the covariate (initial size). Error
348 Table 2 The results experiment.
R. Etter
I .I. Exp.
Mar.
Bid.
Ed.
of a two-way ANCOVA comparing adult The covariate was initial size of the snails
Source
df
Mean
Morph Shore Size 1 Morph. Shore Morph. Size 1 Shore Size 1 Morph Shore. Size Residual
I
4.253 2.789 112.664 I .x54 3.670 1.621 1.258 I.086
1
I 1 1 1 1 266
I
196 (1996)
growth
square
341-36
rates
in the
reciprocal
transplant
F-value
p-value
3.915 2567 1 I .657
0.0489 0.1 103 0.0007 0.1926 0.0672 0.2230 0.2828
1.706 3.378 1.492 1.158
in growth may simply reflect different growth potentials due to differences in initial size. For adults, there was a slight morph effect (Table 2), exposed morphs tended to grow more than protected (Fig. 2). This primarily reflects the negative growth of protected morphs reared on the exposed shore. Again, because the initial size of the adults differed, comparisons among morphs should be interpreted cautiously. There was no shore effect and the interaction term between morph and shore was not significant. The lack of significance here probably reflects the lower growth rates associated with large adult Nucella (Etter, 1989). The rank order of the
Adults G
1.6
s u
_^ 1
l-E3 T
T
-0.6 . EP
E0
Pe
PP
Morph/Shore Fig. 2. Growth increments transplanted between shores
for adult whelks and their controls.
from Other
an exposed or protected shore details are the same as described
reciprocally in Fig. 1.
R. Etter
means were the negative
I J. Exp. Mar. Biol. Ecol. 196 (1996) 341-356
similar between the adults and juveniles. growth of the protected adults transferred
3.2. Prey type and foraging
349
The only exception being to the exposed shore.
time
In the laboratory, there was also no morph effect suggesting exposed and protected morphs grew at similar rates under uniform conditions (Table 3). There was a strong effect due to the feeding treatments. Both prey type and foraging time influenced the growth rate of exposed and protected juveniles (Fig. 3). Diets that included mussels either alone (M) or in combination with barnacles (MBH) promoted the most rapid growth, whereas a restriction of the time available for foraging suppressed growth rates considerably. In fact, despite being supplied a high growth diet of mussels and barnacles, exposed and protected juveniles grew least when foraging time was reduced 33%. This suggests that dogwhelks are unable to compensate for less foraging time by feeding at a faster rate during periods which are more conducive to feeding. A diet consisting solely of barnacles supported an intermediate growth rate. When analyzed monthly, growth rates differed between morphs maintained on a particular diet (Fig. 4). For each diet, protected morphs tended to grow more than exposed morphs during June, the opposite was true for July and August. When summed over the summer (June-August) however, exposed and protected morphs tended to grow at similar rates (Fig. 3). A comparison between the sexes indicated that male and female whelks from
Table 3 The results experiment.
of a three-way ANCOVA comparing juvenile The covariate was initial size of the snails
Source
df
Mean
Prey Month Morph Size 1 Prey. Size 1 Month. Size 1 Morph. Size 1 Prey. Month Mont. Morph Prey. Morph Preyy Month. Size 1 Month. Morph. Size1 Prey. Morph Size 1 Pre Month. Morph Prey. Month Morphy . Size 1 Residual
3 2 1 1 3 2 1 6 2 3 6 2 3 6 6 654
10.639 8.201 2.105 25.466 5.864 6.073 1.964 1.956 0.239 0.887 1.727 1.023 0.549 3.363 2.616 1.000
square
growth
rates
in the laboratory
F-value
p-value
10.639 8.201 2.105 25.464 5.864 6.073 1.964 1.956 0.239 0.887 1.726 1.023 0.549 3.363 2.616
0.0001 0.0003 0.1473 0.0001 0.0006 0.0024 0.1615 0.0698 0.7876 0.4474 0.1122 0.3602 0.6489 0.0028 0.0163
feeding
R. Eiter
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10
9
6
7
6
~
5
E
M
MBH
MBL
Prey Fig. 3. Growth increments over the summer (90 days) protected shore maintained on a diet of an overabundance barnacles (MBH), and mussels and barnacles but only 67% are from an ANCOVA and have been adjusted to the bars = 95% confidence limits.
r
T
June
1
IJB rnM n MBH
Cl
Exposed
Protected
for juvenile whelks from an exposed or of barnacles (B), mussels (M), mussels and of the lime (MBL). The growth increments mean of the covariate (initial size). Error
MBL
-r
T
I
Exposed
Protected
July
Protected
EXp0S-d
August
Fig. 4. Monthly growth increments for juvenile whelks from an exposed or protected shore maintained on a diet of an overabundance of barnacles (B), mussels (M). mussels and barnacles (MBH), and mussels and barnacles but only 67% of the time (MBL). The growth increments are from an ANCOVA and have been adjusted to the mean of the covariate (initial size). Error bars = 95% confidence limits.
R. Etter Table 4 The results experiment.
I J. Exp. Mar. Biol. Ecol.
of a two-way ANCOVA comparing adult The covariate was initial size of the snails
196 (1996) 341-356
growth
rates
in the
351
laboratory
Source
df
Mean square
F-value
p-value
Gender Morph Size 1 Gender. Morph Gender. Size 1 Morph. Size 1 Gender. Morph Residual
1 1 1 1 1 1 1 191
0.402 2.750 3.127 0.818 0.573 1.628 0.915 0.333
1.206 8.250 9.382 2.453 1.719 4.886 2.746
0.2735 0.0045 0.0025 0.1189 0.1914 0.0283 0.0991
Size 1
feeding
both habitats grew at similar rates (Table 4). The gender effect and the interaction of gender with morph were not significant indicating that growth rates did not differ between the sexes for either exposed or protected morphs.
4. Discussion Growth rates of whelks reciprocally transplanted between an exposed and a protected shore are extremely plastic and demonstrate that differences in growth between whelks from shores differentially exposed to wave action do not reflect genetic differentiation, but appear to be causally related to environmental forces that depress growth on wave-swept shores. Brown and Quinn (1988) observed similar results for three rocky intertidal gastropods, N. emarginatu, Coflisella digitalis, and Collisella scabra, and suggested that the lower growth rates on exposed coasts resulted from the direct impact of waves which reduced foraging efficiency. Reduced foraging time was also invoked for the depressed growth of Littorina rudis ( = saxatilis) from exposed coasts (Roberts and Hughes, 1980), although a more recent study indicates that much of the variation in growth of L. saxatilis represents genetic differentiation (Janson, 1982). Circumstantial evidence for the foraging efficiency hypothesis derives from reduced feeding rates observed on wave-swept shores for two muricids, N. lapillus (Menge, 1978b), and Morula marginalba (Moran, 1985) the lower proportion of snails foraging when wave energies are high (Hughes and Drewett, 1985; Burrows and Hughes, 1989) and the decrease in prey and tissues consumed in laboratory experiments where snails were exposed to wave simulators (Richardson and Brown, 1990). However, the direct affect on growth rates has not been established. It is possible that differences in feeding rates do not translate into differences in growth rates. For instance, although snails on exposed coasts consume fewer prey, they may have a higher assimilation efficiency or may simply consume more of the prey tissues. In fact, a number of studies have found that tissue consumption rates do not differ between snails feeding on exposed and protected shores (Menge, 1978a; Richar-
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dson and Brown, 1990) or that consumption is actually greater on exposed shores (Burrows and Hughes, 1990). A more direct link was established in this study through laboratory experiments limiting the amount of time available for foraging. Inhibiting foraging for a 5-day period twice each month depressed growth rates considerably providing evidence that slower growth rates on exposed shores may in part reflect reduced foraging time imposed by periods of heavy wave action. This is particularly impressive in that typical foraging bouts by N. lupillus on exposed and protected shores last l-2 days and are punctuated by non-feeding periods ranging from 1 to more than 6 days depending on the type and size of prey consumed during foraging (Hughes and Drewett, 1985). Apart from limiting the time available for foraging, wave action may also influence foraging efficiency by extending the amount of time necessary to handle a particular prey item. Chronic jostling by the hydromechanical forces that develop during breaking waves may impede the inspection, boring or ingesting phases of feeding and thereby decrease predator efficiency. It is likely that both foraging time and foraging efficiency are affected by wave action, but the relative impact on each will vary spatially and temporally with the intensity of wave action and the availability of prey. Prey type had a significant effect on growth rates but the laboratory results were opposite the observed patterns in nature. Mussels promoted the fastest growth in the laboratory. Growth rates therefore should be greater on exposed coasts where whelks would prey primarily on mussels. However, snails grew least on the exposed shore and best on the protected shore where their diet would consist primarily of barnacles. The disparity between the field and laboratory results suggests that variation in growth between exposed and protected shores is not explicable in terms of variation in the types of prey available to N. lupillus. Furthermore, the forces evoking differences in growth rates must counteract the opposite effect on growth imposed by prey type. The higher growth rates supported by mussels in these experiments is in contrast to previous studies on prey value in Nucella where barnacles typically supported maximum growth (Palmer, 1983; Burrows and Hughes, 1990). It is unclear why the disparity exists, however, one possible explanation may be that growth was measured over a much longer period in this study. In Palmer’s (1983) experiments growth was measured over a 28-day period, while Burrows and Hughes (1990) followed growth for only 14 days. When analyzed on a monthly basis, the value of a particular feeding regime in this study varied (Fig. 4). For example, growth of the exposed morphs indicated that barnacles ranked third in June, but were not significantly different from the feeding regimes supporting the highest growth (M or MBH) in August. A similar pattern is apparent for the growth of protected morphs between July and August. Prey value estimated from monthly growth rates may reflect short-term temporal changes in the nutritional quality of a particular prey item. Longer term experiments may provide more consistent measures of prey value. In any event, the temporal variation in growth underscores the importance of conducting growth experiments for more than 30 days.
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353
Although high mortality in the experimental populations precluded measuring the response of other life history components to the experimental treatments (an unusually high water temperature around Nahant, MA killed most of the field and laboratory snails early in September), growth rates are often correlated with other such components, and are commonly assumed to be positively correlated with fitness (Schoener, 1971; Charnov, 1976; Hughes, 1979). For instance, an increase in food density promoted more rapid growth in N. Zumeflosa which resulted in a larger spawn (Spight, 1974). Palmer (1983) found a negative correlation between growth and age at maturity, and a positive correlation between growth and number of egg capsules deposited for both N. canalicufutu and N. emarginata. From the present analysis it is clear that faster growth rates resulted in a larger size at maturity. Many exposed yearlings reared for 3-5 months under conditions that promote high growth rates exceeded the size at which individuals from their population typically mature (15-19 mm, Etter, 1989) and yet showed no outward signs of maturation. However, the relationship between size and fecundity demonstrated in other populations of N. lapiflus (Crothers, 1985) and in other 1976; Palmer, closely related muricids (Spight et al., 1974; Spight and Emlen, 1983) is more tenuous. Nucella lupillus from exposed shores produced about four times as many offspring than did protected females, despite the significantly smaller size of the former (Etter, 1989). Thus, the positive correlation between size and fecundity in muricids may only hold within populations. Stearns and Koella (1986) demonstrated theoretically and empirically that growth rates can have important consequences for age and size at maturity. Variation in growth rates moved organisms along a trajectory within an age vs. size at maturity space that resulted in a highly plastic phenotype. The results were supported by several empirical examples and suggested most organisms should mature at neither a fixed age nor size. Both field and laboratory results indicate that N. lapillus does not mature at a fixed size. Many exposed yearlings reared on the protected shore or in the laboratory with an overabundance of food exceeded the size at which members of their population typically mature, but exhibited no outward signs of maturation. This suggests size at maturity is not genetically determined, but is a consequence of the growth environment before the onset of sexual maturation. The results presented here also suggest (at least for N. fupillus) that whelks continue to grow after reaching maturity. Most adults, in both the laboratory and field experiments, continued growing, albeit slowly, under benign conditions. Thus, asymptotic size is probably set by extrinsic factors within the local environment such as energetic constraints (Sebens, 1982) or mortality induced by hydromechanical forces generated by breaking waves (Denny et. al., 1985). Our understanding of the forces that shape variation in growth rates of intertidal snails among shores differentially exposed to wave action remains fragmentary. We need to determine exactly how energy is partitioned among the competing demands of growth, reproduction and maintenance. For example, exposed morphs produce about four times as many offspring as protected morphs (Etter 1989) which presumably requires a greater energy investment. Does this increased energy investment contribute to or account for the slower growth rates?
354
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Growth in N. lapillus is highly plastic and influenced by both prey type and foraging time. The slower growth on exposed shores may in part reflect reduced foraging time, but does not appear to be due to prey type. Only a more detailed analysis of energy allocation will allow us to determine more specifically why growth varies among exposure regimes, but it is clear that reducing the time available for foraging can result in slower growth.
Acknowledgments I thank K. Brown, K. Boss, W. Bossert, M. Patterson, M. Rex, K. Sebens, R. Turner and an anonymous reviewer for their comments on a previous version of this paper. I also thank K. Sebens for providing laboratory and computer facilities at Northeastern University’s Marine Science Center.
References Allan, J.D., 1984. Life history variation in a freshwater copepod: Evidence from population crosses. Evolution, Vol. 38, pp. 280-291. Atkinson, W.D. and SF. Newbury. 1984. The adaptations of the rough winkle Littorinu rudis to desiccation and dislodgement by wind and waves. J. Anim. Ed., Vol. 53, pp. 933106. Baird, D., L. Linton and R. Davies, 1987. Life-history flexibility as a strategy for survival in a variable environment. Funct. Ed., Vol. 1, pp. 45-48. Behrens Yamada, S., 1989. Are direct developers more locally adapted than planktonic developers? Mar. Bid.. Vol. 103, pp. 403-411. Berrigan, D. and E.L. Charnov, 1994. Reaction norms for age and size at maturity in response to temperature: a puzzle for life historians. Oikos. Vol. 70. pp. 474-478. Berrigan, D. and J.C. Koella. 1994. The evolution of reaction norms simple models for age and size at maturity. J. Evolut. Biol, Vol. 7. pp. 549-566. Berven, K.A., 1982. The genetic basis of altitudinal variation in the wood frog, Rann sylvatica. II. An experimental analysis of larval development. Oecologia (Berlin). Vol. 52, pp. 360-369. Berven, K.A. and D.E. Gill, 1983. Interpreting geographic variation in life-history traits. Am. Zoo!.. Vol. 23, pp. 85-97. Brown, K.M., 1983. Do life history tactics exist at the intraspecific level? Data from fresh water snails. Am. Nat.,Vol. 121, pp. 871-879. Brown, K.M., 1985. Intraspecific life history variation in a pond snail: the roles of population divergence and phenotypic plasticity. Evolution. Vol. 39, pp. 387-395. Brown, K.M. and J.F. Quinn, 1988. The effect of wave action on growth in three species of intertidal gastropods. Oecologia (Berlin), Vol. 75, pp. 420-425. Burrows, M. and R. Hughes, 1989. Natural foraging of the dogwhelk. Nucella lapillus (Linnaeus); The weather and whether to feed. .I. Mall. Sturi.,Vol. 55, pp. 285-295. Burrows, M.T. and R.N. Hughes, 1990. Variation in growth and consumption among individuals and populations of dogwhelks, Nucella-Lapillus - a link between foraging behaviour and fitness. J. Anim. Ecol., Vol. 59, pp. 723-742. Charnov, E.L., 1976. Optimal foraging: attack strategy of a mantid. Am. Nat., Vol. 110, pp. 141-151. Crothers, J.H.. 1985. Dog-whelks: An introduction to the hiology of Nucdla lapillus (L.). Field Stud.. Vol. 6, pp. 291-360. Crowl, T.A. and A.P. Covich. 1990. Predator-induced life-history shifts in a freshwater snail. Science, Vol. 247, pp. 949-951.
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Denny, M.W., T.L. Daniel and M.A.R. Koehl, 1985. Mechanical limits to size in wave swept organisms. Ecol. Monogr., Vol. 55, pp. 69-102. Dugan, J.E., D.M. Hubbard and A.M. Wenner, 1994. Geographic variation in life history of the sand crab, Emerita analoga (Stimpson) on the California coast: relationships to environmental variables. J. Exp. Mar. Biol. Ecol., Vol. 181, pp. 255-278. Dunkin, S. de B. and R.N. Hughes, 1984. Behavioural components of prey-selection by dogwhelks, Nucella lapillus (L.). feeding on barnacles, Semibalanus balanoides (L.) in the laboratory. J. Exp. Mar. Biol. Ecol., Vol. 79, pp. 91-103. Etter, R.J., 1988a. Asymmetrical developmental plasticity in an intertidal snail. Evolution, Vol. 42, pp. 322-334. Etter, R.J., 1988b. Physiological stress and color polymorphism in the intertidal snail Nucella lapillus. Evolution, Vol. 42, pp. 660-680. Etter, R.J., 1989. Life history variation in the intertidal snail Nucella lapillus across a wave-exposure gradient. Ecology, Vol. 70, pp. 1857-1876. Feare, C.J., 1966. The winter feeding of the Purple Sandpiper. Br. Birds,Vol. 59, pp. 165-179. Hughes, R.N., 1979. Optimal diets under the energy maximization premise: The effects of recognition time and learning. Am. Nat., Vol. 113, pp. 209-221. Hughes, R.N. and D. Drewett 1985. A comparison of the foraging behaviour of dogwhelks, Nucella lapillus (L.), feeding on barnacles or mussels on the shore. J. Mollusc. Stud.,Vol. 51, pp. 73-77. Hughes, R.N. and S. de B. Dunkin 1984a. Behavioural components of prey-selection by dogwhelks, Nucella lapillus (L.) feeding on mussels, Mytilus edulis L., in the laboratory. J. Exp. Mar. Biol. Ecol., Vol. 77, pp. 45-68. Hughes, R.N. and S. de B. Dunkin, 1984b. Effect of dietary history on selection of prey, and foraging behaviour among patches of prey, by the dogwhelk, Nucella lapillus (L.). J. Exp. Mar. Biol. Ecol., Vol. 79, pp. 159-172. Hughes, R.N. and D.J. Roberts, 1981. Comparative demography of Littorina rudis L. nigrolineata and L. neritoides on three contrasted shores in North Wales. J. Anim. Ecol.,Vol. 50, pp. 251-268. Janson, K., 1982. Genetic and environmental effects on the growth rate of Littorina saxatilis. Mar. Biol., Vol. 69, pp. 73-78. Janson, K., 1983. Selection and migration in two distinct phenotypes of Littorina saxatilis in Sweden. Oecologia (Berlin), Vol. 59, pp. 58-61. Kitching, J.A., L. Muntz and F.J. Ebling, 1966. The ecology of Lough Ine. XV The ecological significance of shell and body forms in Nucella. J. Anim. Ecol.,Vol. 35, pp. 113-126. Lafferty, K.D., 1993. The marine snail, Cerithidea californica, matures at smaller sizes where parasitism is high. Oikos, Vol. 68, pp. 3-11. Menge, B.A., 1976. Organization of the New England rocky intertidal community role of predation competition and environmental heterogeneity. Ecol. Monogr., Vol. 46, pp. 355-393. Menge, B.A., 1978,. Predation intensity in a rocky intertidal community. Relation between predator foraging activity and environmental harshness. Oceologia (Berlin), Vol. 34, pp. 1-16. Menge, B.A., 1978b. Predation intensity in a rocky intertidal community: effect of an algal canopy, wave action and desiccation on predator feeding rates. Oceologia (Berlin), Vol. 34, pp. 17-35. Menge, B.A., 1983. Components of predation intensity in the low zone of the New England rocky intertidal region. Oceologia (Berlin), Vol. 58, pp. 141-155. Menge, J.L., 1974. Prey selection and foraging period of the predaceous rocky intertidal snail, Acanthina punctulata. Oecologia (Berlin), Vol. 17, pp. 293-316. Moran, M.J., 1985. Distribution and dispersion of the predatory intertidal gastropod Morula marginalba. Mar. Ecol. Prog. Ser., Vol. 22, pp. 41-52. Moran, M.J., P.G. Fairweather and A.J. Underwood, 1984. Growth and mortality of the predatory intertidal whelk Morula maginalba Blainville (Muricidae): the effects of different species of prey. J. Exp. Mar. Biol. Ecol., Vol. 75, pp. 1-17. Palmer, A.R., 1983. Growth rate as a measure of food value in thaidid gastropods: assumptions and implications for prey morphology and distribution. J. Exp. Mar. Biol. Ecol., Vol. 73, pp. 95-124. Petraitis, P.S., 1987. Factors organizing rocky intertidal communities of New England herbivory and predation in sheltered bays. J. Exp. Mar. Biol. Ecol.,Vol. 109, pp. 117-136.
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Reznick, D., 1982. The impact of predation on life history evolution in Trinidadian guppies. Evolution. Vol. 36, pp. 160-177. Richardson, T.D. and K.M. Brown., 1990. Wave exposure and prey size selection in an intertidal predator. .I. Exp. Mar. Biol. Ecol.,Vol. 142, pp. 10.5-120. Richardson. T.D. and K.M. Brown, 1992. Predation risk and feeding in an intertidal predatory snail. J. Exp. Mar. Biol. Ecol.,Vol. 163, pp. 169-182. Roberts, D.J. and R.N. Hughes. 1980. Growth and reproductive rates of Littorina rudis from three contrasted shores in North Wales, IJK. Mar. Biol.. Vol. S8, pp. 47754. Scheiner, S.M. and C.J. Goodnight, 1984. The comparison of phenotypic plasticity and genetic variation in populations of the grass Danrhoniu spicata. Evolution. Vol. 38. pp. 845-855. Schoener, T.W., 1971. The theory of feeding strategies. Annu. Rev. Ecol. Syst., Vol. 2. pp. 369-404. Sebens, K.P., 1982. The limits to indeterminate growth: an optimal size model applied to passive suspension feeders. Ecology. Vol. 63, pp. 209-222. Spight, T.M.. 1974. Sizes of populations of a marine snail. Ecology. Vol. 55. pp. 712-729. Spight, T.M. and J.M. Emlen, 1976. Clutch sizes of two marine snails with a changing food supply. Ecology, Vol. 57. pp. 1162-117X. Spight, T.M., C. Birkeland and A. Lyons, 1974. Life histories of large and small murexes (Prosohranchia: Muricidae). Mu. Biol., Vol. 24, pp. 22Y-242. Stearns, SC., 1976. Life history tactics: A review of the ideas. Q. Rev. Biol..Vol. 51. pp. 3-47. Stearns, SC., 1977. The evolution of life-history traits: A critique of the theory and a review of the data. Annu. Rev. Ecol. Cyst.. Vol. 8, pp. 145-171. Stearns, SC., 1980. A new view of life-history evolution. Oikos. Vol. 35, pp. 266-281. Stearns, SC., 1983. The evolution of life-history traits in mosquitofish since their introduction to Hawaii in 1905: Rates of evolution, heritabilities and developmental plasticity. Am. Zool.. Vol. 23. pp. 65-76. Stearns, S.C. and J.C. Koella, 1986. The evolution of phenotypic plasticity in life-history traits: predictions of reaction norms for age and size at maturity. Evolution, Vol. 40, pp. X93-913. Stickle, W.B., M.N. Moore and B.L. Bayne, 198.5. Effects of temperature, salinity and aerial exposure on predation and lysosomal stability of the dogwhclk Thuis (Nucrlltr) lapillus (L.). J. Exp. Mar. Biol. Ecol., Vol. 93, pp. 235-258. Travis. J., 1983. Variation in development patterns of larval anurans in temporary ponds. 1. Persistent variation within a Hyla gratiosa population. Evolurion, Vol. 37. pp. 4966512. Vadas. R.L., 1977. Preferential feeding: An optimization strategy in sea urchins. Ecol. Monogr.. Vol. 47, pp. 337-37 1. West, L., 1986. Interindividual variation in prey selection by the snail Nucella (= 7’hais) emarginafa. Ecology, Vol. 67, pp. 798-809. West, L.. 1988. Prey selection by the tropical snail Thais melonrs: a study of interindividual variation. Ecology, Vol. 69, pp. 1X39-1854.
Marine Biology and Ecology 196 (1996) 341-356
of Experimental
JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY
The effect of wave action, prey type, and foraging time on growth of the predatory snail Nucda ZapiZZus(L.) Ron J. Etter Biology Department,
University
of Massachusetts, 100 Morrissey Blvd., Boston, MA 0.2125, USA
Received 2 February 1995; revised 28 June 1995; accepted 27 July 1995
Abstract Growth rates of intertidal snails vary among populations differentially exposed to wave action; individuals from sheltered habitats typically grow more quickly than do those from more exposed coasts. A series of field and laboratory experiments were conducted to separate the genetic and phenotypic components of this variation in Nucella lapillus (L.) and to investigate the extent to which prey type and foraging time, which also vary across the wave-exposure gradient, affect growth. Juvenile and adult whelks were reciprocally transplanted between an exposed and a protected shore and subsequent growth followed. Independent of origin, whelks grew more on the sheltered shore. By contrast, growth rates for snails from exposed and protected shores were similar when reared under uniform conditions in the laboratory. Together these findings suggest that the variation observed in nature does not represent genetic differentiation, but reflects the influence of proximal factors that depress growth on wave-swept shores. Growth rates of juveniles from exposed and protected shores maintained in the laboratory on a diet of an overabundance of (1) barnacles, (2) mussels, (3) both, and (4) both, but only 67% of the time, indicated that prey type and foraging time affect growth. Whelks grew best on a diet of mussels, either singly or in combination with barnacles, grew less on barnacles alone. and least when foraging time was restricted. Because growth rates on specific prey in the laboratory were opposite the observed trend in nature, variation in prey across the exposure gradient cannot be invoked to account for the difference in growth between N. fapillus from exposed and protected shores. The slower growth rates when foraging time was restricted are consistent with the notion that wave energies on exposed coasts depress growth by limiting foraging time or by reducing foraging efficiency. Keywords:
Growth;
Intertidal;
Life-history;
0022-0981/96/$15.00 @ 1996 Elsevier SSDI 0022-0981(95)00139-5
Science
Nucella;
Wave-action
B.V All rights
reserved
342
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1. Introduction Intraspecific variation in life histories is ubiquitous in nature and several theoretical models have been developed to predict under what selective pressures particular characteristics might evolve (reviewed in Stearns, 1992). Variation in life histories may be due to genetic differences among individuals, phenotypic plasticity induced by environmental variation or a combination of both (e.g. Reznick, 1982; Berven and Gill, 1983; Brown, 1983, 1985; Stearns, 1983; Travis, 1983; Allan, 1984; Scheiner and Goodnight, 1984; Crow1 and Covich, 1990; Lafferty, 1993; Dugan et al., 1994, Wellborn, 1994). It is essential to sort out the relative contribution of plastic and genetic variation because evolutionary arguments regarding the adaptive significance of life history variation are moot until the extent of genetic variation has been identified (Stearns, 1976, 1977). Although it is difficult to test the mechanisms underlying genetic differentiation in life histories for organisms with long generation times, those forces affecting the plastic components of variation are more amenable to experimental verification (Stearns, 1980; Berven, 1982; Crow1 and Covich, 1990) and are perhaps equally important in understanding life history variation (Stearns and Koella, 1986; Baird et al., 1987; Berrigan and Charnov, 1994; Berrigan and Koella, 1994). The rocky intertidal snail Nucella lapillus (L.) exhibits remarkable variability in its life history traits among populations differentially exposed to wave action (Etter, 1989). Whelks from wave-swept shores grow more slowly, mature at a smaller size, suffer higher mortality, and produce many more offspring than do conspecifics at more sheltered habitats. Similar patterns have been observed in a number of other intertidal snails (Hughes and Roberts, 1981; Janson, 1982, 1983; Atkinson and Newbury, 1984; Brown and Quinn, 1988: Behrens Yamada, 1989). Although this variation fits accepted schemes of life history evolution, it is unclear to what extent the variation represents genetic differentiation or phenotypic plasticity. We are equally nescient of the proximal forces that shape variation in these life histories. The work described in this paper was designed to determine to what extent differences in growth rates among snails from different exposure regimes were due to genetic or environmental influences, and experimentally test the plausibility of a variety of hypotheses invoked to account for the interhabitat variation in growth. The growth rate of an organism is an essential feature of its life history. Because growth rates can influence fitness in several ways, it is often used as a surrogate for fitness, especially in snails (Palmer, 1983; Moran et al., 1984; Brown and Quinn, 1988; West, 1988; Burrows and Hughes, 1990). For example, because fecundity is typically a positive function of size (Spight et al., 1974; Spight and Emlen, 1976; Palmer, 1983; Crothers, 1985), faster growing snails have the potential to produce more offspring at any particular age. Small snails are also generally more vulnerable to predation than are large snails (Feare, lY66: Richardson and Brown, 1992). For N. lapillus, once it attains a size that exceeds 15mm, mortality due to predation is low (Etter, 1988b). The growth rate therefore determines the amount of time N. lapillus is vulnerable to predation. Recent
R. Etter
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343
theoretical and empirical work has shown that by altering reaction norms, growth rates can have important direct and indirect affects on other life history traits (Stearns and Koella 1986; Berrigan and Charnov, 1994; Berrigan and Koella, 1994). An understanding of the forces modulating growth rates may yield important insights into variation in other life history traits. The variation in growth rates of N. lupillus among shores differentially exposed to wave action may reflect a variety of factors including genetic differentiation, the relative density and quality of food, foraging efficiency and/or energy allocation to other needs (e.g. maintenance and reproduction). These putative influences are, of course, not mutually exclusive. I consider the importance of three potential factors. Nucellu lupillus lacks a dispersal stage in its life cycle and adults have a small (
344
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I J. Exp.
Mar.
Rid.
Ed.
1% (1996)
341L.156
Therefore, the slower growth on wave-swept shores may reflect a diet high in mussels. To determine the importance of prey type in affecting growth rates, juvenile and adult whelks were fed a diet of barnacles, Semibalanus balanoides (L.), and mussels, Myths edulis L. and subsequent growth followed.
2. Methods 2.1. Reciprocal
transplant experiment
Whelks for the reciprocal transplant experiment were collected from an exposed (No Name Point, Nahant, MA) and a protected shore (Mackeral Cove, Beverly, MA), returned to the laboratory and maintained in water tables supplied with running seawater. Juveniles were collected in May, but collection of adults was delayed until June. By June, most whelks had finished depositing egg capsules, and thus transferring adults between an exposed and protected shore at this time would limit the extent of unnatural gene flow among populations. An entire size range of whelks was collected from each site and, based on size, individuals were classified as either juveniles (exposed 515 mm, protected 520 mm) or adults (exposed ~19 mm, protected ~24 mm). The specific size used to separate juveniles from adults in each population was selected based on the typical size at which whelks begin to mature in each population (Etter, 1989). Snails were tagged and the maximum shell length (~0.05 mm) recorded. Shell length was measured with vernier calipers as the maximum distance between the shell apex and the tip of the siphonal canal. After marking, exposed morphs were separated into two groups; (1) approximately two-thirds were returned to a separate exposed shore (Bennett Head, Nahant, MA) ( = residents). and (2) the other third were transferred to a protected shore (a separate shore at Mackerel Cove) ( = transferred). Tagged individuals from the protected shore were treated in a similar manner. Rather than release half the whelks at each site as is typical of reciprocal transplant experiments, slightly more were used at the exposed shore to offset the higher mortality rates suffered by whelks at this site (Etter, 1989). The only exception to this procedure was for exposed juveniles which were equally split between the exposed and protected shore. The rationale for an equal split in this case was that I expected mortality rates of exposed juveniles to be high on the protected shore because they tend to possess thin. pigmented shells increasing their vulnerability to the greater physiological stress (Etter, 198Sb) and the more intense predation (Kitching et al., 1966; Menge, 1983) on protected shores. A quantity of whelk biomass similar to the biomass released was removed from each site to prevent artificially increasing biomass. All tagged whelks were recollected in October, and their shell lengths recorded. Growth rates were estimated from changes in shell length over the duration of the experiment. Shell length was used to estimate growth because, in a separate analysis, it provided results similar to total weight, shell weight, or body weight
345
R. Etter I J. Exp. Mar. Biol. Ecol. 196 (1996) 341-3_f6
(Etter, within
1989). ANCOVA as described below and between shores and morphs.
2.2. Prey type and foraging
was used to compare
growth
rates
time experiment
Whelks for the prey quality and foraging time experiments were collected from an exposed shore (No Name Point) at Nahant, MA and a protected shore in Beverly, MA (Mackerel Cove). They were returned to the laboratory and sorted into juvenile and adult snails as described above. The adults were further divided into males and females based on the presence of a penis or a capsule gland, respectively. All individuals were tagged and maintained completely submerged in seawater tables without food for 1 wk prior to the start of the experiment. Twenty-four cages were constructed from plastic freezer containers (18 X 13.1 X 8.2 cm) by cutting windows in each panel of the container and covering the windows with nitex screen (mesh size =l mm) to permit water flow. Each cage was provided with one of four treatments; an overabundance of (1) barnacles, (B), (2) mussels (M), (3) both mussels and barnacles (MBH), and (4) both mussels and barnacles, but only 67% of the time (MBL). For each treatment, a full size range of prey from both habitats was provided. Barnacles were added by placing small rocks covered with Semibalanus balanoides in a cage and mussels (Mytilus edulis) were introduced into the cages individually and on small rocks where possible. Regardless of the prey type, all cages received one or more rocks to more closely resemble natural substrata. The procedure for the MBL treatment was to alternate between an overabundance of prey for 10 days and no prey for 5 days to simulate foraging restricted by wave action. Nucella typically forages only when immersed, although if it has begun to feed it will continue during low tide. Foraging stops when snails are emersed or during high wave energies usually associated with storms (Burrows and Hughes, 1989). By allowing snails to feed for 10 days and then removing prey for 5 days, I simulated how foraging might be restricted by storms that occur on a frequency of twice each month. The 5-day restriction is meant to reflect the increase in wave energy prior to a storm (1 day), during the storm (1.5 days) and the residual surge after a storm has passed (2.5 days). The shell length of each snail was measured and 10 juveniles, 5 males and 5 females placed in each cage. There were 6 replicate cages per feeding treatment; into half of the cages exposed morphs were added, and the remaining 3 received protected morphs. The experimental design consisted of four feeding treatments (prey type and foraging time) X two morphs (exposed or protected) X three replicates. All cages were completely submerged in a water table supplied with continuously flowing seawater. Cages were checked weekly and new prey added where necessary. The seawater was drawn from the shallow subtidal at Nahant and maintained at ambient temperature and salinity. Although the water flowed through the tables, there was no current or wave energy. The flow characteristics in the water tables resemble what snails might experience in tidepools on a very protected shore.
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196 (1996) .741-36
Monthly changes in shell length were used as estimates of growth rates and several questions were addressed by comparing growth rates among snails. First, growth rates of juveniles reared on different diets were compared to establish whether prey type or foraging time influenced growth. Only juveniles were employed in estimating the quality of prey or the effect of foraging time on growth because, after maintenance requirements are satisfied, juveniles devote all net energy to growth whereas adults may not (Palmer, 1983). Second, to determine if exposed and protected morphs differ in growth rate when fed a specific diet, juvenile growth was compared between morphs for each experimental treatment. Adults were not used in a similar analysis because initial size differed between exposed and protected adults. Both of the above comparisons were computed for the entire experimental period (3 months) as well as for each month to investigate any temporal components in these relationships that emerged due to ingestive conditioning (Dunkin and Hughes, 1984; Hughes and Dunkin, 1984a,b; Stickle et al., 1985) or in response to changes in water temperature (Stickle et al., 1985). Third, to further investigate temporal components, growth rates of juveniles reared on a particular feeding regime were compared among months separately for exposed and protected morphs. The remaining questions were primarily concerned with possible genetic differences in growth rates among whelks and thus comparisons were made across all diets. Feeding treatments were pooled because the variability in prey type or foraging time more accurately reflects what a population of whelks as a whole might experience in nature over a specified period of time; certain individuals may only encounter mussels, others only barnacles and some both prey but either at high (MBH) or low densities (MBL). Fourth, the genetic component of variation in growth was estimated by comparing juvenile growth rates between morphs reared under similar laboratory conditions. Finally, growth rates were also compared between males and females separately for exposed and protected snails to detect differences in growth between sexes. ANCOVA on regression lines fit to modified Ford-Walford plots where growth over an interval is regressed on initial size, were used to compare all growth rates (Etter, 1989). The slope of the regression line represents the growth schedule for a particular population and the asymptotic size is given by the intersection of the regression line with the x-axis. Therefore, the slope can also be viewed as the rate at which individuals approach their asymptotic size. The displacement of the regression line (or its elevation) represents the size specific growth rate, i.e. the amount an individual initially size x will grow over the period from t to f + 1.
3. Results 3.1. Reciprocal
transplant
There was a clear environmental effect on growth rates of juvenile snails, independent of their habitat of origin (Table 1). Protected shores supported the
R. Etrer I .I. Exp. Mar. Bid.
Ecol. I96 (1996) 341-356
347
Table 1 The results of a two-way ANCOVA comparing juvenile growth rates in the reciprocal transplant experiment. The covariate was initial size of the snails Source
df
Morph Shore Size 1 Morph. Shore Morph * Size 1 Shore. Size 1 Morph. Shore. Size 1 Residual
Mean square
,F-value
p-value
12.491 53.743 50iJ.973 38.936 5.468 15.241 27.785 5.476
2.281 9.814 91.483 7.110 0.999 2.783 5.074
0.1349 0.0024 O.Ooa1 0.0093 0.3206 0.0991 0.0270
most rapid growth rates in juvenile whelks (Fig. 1). Exposed morphs reared on a protected shore increased in shell length by -9 mm whereas those remaining on an exposed shore increased by only 6 mm. Similarly, protected morphs reared on the protected shore grew more than twice as much as those reared on the exposed shore. There was no overall effect of morph, where snails originated from, but there was a sig~i~cant interaction between morph and shore (Table 1). Although protected morphs grew more than exposed morphs on the protected shore, there was no difference in growth between the morphs on the exposed shore (Fig. 1). Comparisons of growth between exposed and protected morphs within sites should be interpreted cautiously though, because the initial size of the juveniles differed slightly and growth rates are size dependent (Etter, 1989); i.e. differences
Juveniles
16
-r
7
EP
E%
Pe
PP
Morph/Shore Fig. 1. Growth increments for juvenile transplanted between shores and their E = exposed), lower case letters refer to are from an ANCOVA and have been bars = 95% confidence limits.
whelks from an exposed or protected shore reciprocally controls. Uppercase letters refer to morph (P = protected, the habitat the snails were reared in. The growth increments adjusted to the mean of the covariate (initial size). Error
348 Table 2 The results experiment.
R. Etter
I .I. Exp.
Mar.
Bid.
Ed.
of a two-way ANCOVA comparing adult The covariate was initial size of the snails
Source
df
Mean
Morph Shore Size 1 Morph. Shore Morph. Size 1 Shore Size 1 Morph Shore. Size Residual
I
4.253 2.789 112.664 I .x54 3.670 1.621 1.258 I.086
1
I 1 1 1 1 266
I
196 (1996)
growth
square
341-36
rates
in the
reciprocal
transplant
F-value
p-value
3.915 2567 1 I .657
0.0489 0.1 103 0.0007 0.1926 0.0672 0.2230 0.2828
1.706 3.378 1.492 1.158
in growth may simply reflect different growth potentials due to differences in initial size. For adults, there was a slight morph effect (Table 2), exposed morphs tended to grow more than protected (Fig. 2). This primarily reflects the negative growth of protected morphs reared on the exposed shore. Again, because the initial size of the adults differed, comparisons among morphs should be interpreted cautiously. There was no shore effect and the interaction term between morph and shore was not significant. The lack of significance here probably reflects the lower growth rates associated with large adult Nucella (Etter, 1989). The rank order of the
Adults G
1.6
s u
_^ 1
l-E3 T
T
-0.6 . EP
E0
Pe
PP
Morph/Shore Fig. 2. Growth increments transplanted between shores
for adult whelks and their controls.
from Other
an exposed or protected shore details are the same as described
reciprocally in Fig. 1.
R. Etter
means were the negative
I J. Exp. Mar. Biol. Ecol. 196 (1996) 341-356
similar between the adults and juveniles. growth of the protected adults transferred
3.2. Prey type and foraging
349
The only exception being to the exposed shore.
time
In the laboratory, there was also no morph effect suggesting exposed and protected morphs grew at similar rates under uniform conditions (Table 3). There was a strong effect due to the feeding treatments. Both prey type and foraging time influenced the growth rate of exposed and protected juveniles (Fig. 3). Diets that included mussels either alone (M) or in combination with barnacles (MBH) promoted the most rapid growth, whereas a restriction of the time available for foraging suppressed growth rates considerably. In fact, despite being supplied a high growth diet of mussels and barnacles, exposed and protected juveniles grew least when foraging time was reduced 33%. This suggests that dogwhelks are unable to compensate for less foraging time by feeding at a faster rate during periods which are more conducive to feeding. A diet consisting solely of barnacles supported an intermediate growth rate. When analyzed monthly, growth rates differed between morphs maintained on a particular diet (Fig. 4). For each diet, protected morphs tended to grow more than exposed morphs during June, the opposite was true for July and August. When summed over the summer (June-August) however, exposed and protected morphs tended to grow at similar rates (Fig. 3). A comparison between the sexes indicated that male and female whelks from
Table 3 The results experiment.
of a three-way ANCOVA comparing juvenile The covariate was initial size of the snails
Source
df
Mean
Prey Month Morph Size 1 Prey. Size 1 Month. Size 1 Morph. Size 1 Prey. Month Mont. Morph Prey. Morph Preyy Month. Size 1 Month. Morph. Size1 Prey. Morph Size 1 Pre Month. Morph Prey. Month Morphy . Size 1 Residual
3 2 1 1 3 2 1 6 2 3 6 2 3 6 6 654
10.639 8.201 2.105 25.466 5.864 6.073 1.964 1.956 0.239 0.887 1.727 1.023 0.549 3.363 2.616 1.000
square
growth
rates
in the laboratory
F-value
p-value
10.639 8.201 2.105 25.464 5.864 6.073 1.964 1.956 0.239 0.887 1.726 1.023 0.549 3.363 2.616
0.0001 0.0003 0.1473 0.0001 0.0006 0.0024 0.1615 0.0698 0.7876 0.4474 0.1122 0.3602 0.6489 0.0028 0.0163
feeding
R. Eiter
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10
9
6
7
6
~
5
E
M
MBH
MBL
Prey Fig. 3. Growth increments over the summer (90 days) protected shore maintained on a diet of an overabundance barnacles (MBH), and mussels and barnacles but only 67% are from an ANCOVA and have been adjusted to the bars = 95% confidence limits.
r
T
June
1
IJB rnM n MBH
Cl
Exposed
Protected
for juvenile whelks from an exposed or of barnacles (B), mussels (M), mussels and of the lime (MBL). The growth increments mean of the covariate (initial size). Error
MBL
-r
T
I
Exposed
Protected
July
Protected
EXp0S-d
August
Fig. 4. Monthly growth increments for juvenile whelks from an exposed or protected shore maintained on a diet of an overabundance of barnacles (B), mussels (M). mussels and barnacles (MBH), and mussels and barnacles but only 67% of the time (MBL). The growth increments are from an ANCOVA and have been adjusted to the mean of the covariate (initial size). Error bars = 95% confidence limits.
R. Etter Table 4 The results experiment.
I J. Exp. Mar. Biol. Ecol.
of a two-way ANCOVA comparing adult The covariate was initial size of the snails
196 (1996) 341-356
growth
rates
in the
351
laboratory
Source
df
Mean square
F-value
p-value
Gender Morph Size 1 Gender. Morph Gender. Size 1 Morph. Size 1 Gender. Morph Residual
1 1 1 1 1 1 1 191
0.402 2.750 3.127 0.818 0.573 1.628 0.915 0.333
1.206 8.250 9.382 2.453 1.719 4.886 2.746
0.2735 0.0045 0.0025 0.1189 0.1914 0.0283 0.0991
Size 1
feeding
both habitats grew at similar rates (Table 4). The gender effect and the interaction of gender with morph were not significant indicating that growth rates did not differ between the sexes for either exposed or protected morphs.
4. Discussion Growth rates of whelks reciprocally transplanted between an exposed and a protected shore are extremely plastic and demonstrate that differences in growth between whelks from shores differentially exposed to wave action do not reflect genetic differentiation, but appear to be causally related to environmental forces that depress growth on wave-swept shores. Brown and Quinn (1988) observed similar results for three rocky intertidal gastropods, N. emarginatu, Coflisella digitalis, and Collisella scabra, and suggested that the lower growth rates on exposed coasts resulted from the direct impact of waves which reduced foraging efficiency. Reduced foraging time was also invoked for the depressed growth of Littorina rudis ( = saxatilis) from exposed coasts (Roberts and Hughes, 1980), although a more recent study indicates that much of the variation in growth of L. saxatilis represents genetic differentiation (Janson, 1982). Circumstantial evidence for the foraging efficiency hypothesis derives from reduced feeding rates observed on wave-swept shores for two muricids, N. lapillus (Menge, 1978b), and Morula marginalba (Moran, 1985) the lower proportion of snails foraging when wave energies are high (Hughes and Drewett, 1985; Burrows and Hughes, 1989) and the decrease in prey and tissues consumed in laboratory experiments where snails were exposed to wave simulators (Richardson and Brown, 1990). However, the direct affect on growth rates has not been established. It is possible that differences in feeding rates do not translate into differences in growth rates. For instance, although snails on exposed coasts consume fewer prey, they may have a higher assimilation efficiency or may simply consume more of the prey tissues. In fact, a number of studies have found that tissue consumption rates do not differ between snails feeding on exposed and protected shores (Menge, 1978a; Richar-
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dson and Brown, 1990) or that consumption is actually greater on exposed shores (Burrows and Hughes, 1990). A more direct link was established in this study through laboratory experiments limiting the amount of time available for foraging. Inhibiting foraging for a 5-day period twice each month depressed growth rates considerably providing evidence that slower growth rates on exposed shores may in part reflect reduced foraging time imposed by periods of heavy wave action. This is particularly impressive in that typical foraging bouts by N. lupillus on exposed and protected shores last l-2 days and are punctuated by non-feeding periods ranging from 1 to more than 6 days depending on the type and size of prey consumed during foraging (Hughes and Drewett, 1985). Apart from limiting the time available for foraging, wave action may also influence foraging efficiency by extending the amount of time necessary to handle a particular prey item. Chronic jostling by the hydromechanical forces that develop during breaking waves may impede the inspection, boring or ingesting phases of feeding and thereby decrease predator efficiency. It is likely that both foraging time and foraging efficiency are affected by wave action, but the relative impact on each will vary spatially and temporally with the intensity of wave action and the availability of prey. Prey type had a significant effect on growth rates but the laboratory results were opposite the observed patterns in nature. Mussels promoted the fastest growth in the laboratory. Growth rates therefore should be greater on exposed coasts where whelks would prey primarily on mussels. However, snails grew least on the exposed shore and best on the protected shore where their diet would consist primarily of barnacles. The disparity between the field and laboratory results suggests that variation in growth between exposed and protected shores is not explicable in terms of variation in the types of prey available to N. lupillus. Furthermore, the forces evoking differences in growth rates must counteract the opposite effect on growth imposed by prey type. The higher growth rates supported by mussels in these experiments is in contrast to previous studies on prey value in Nucella where barnacles typically supported maximum growth (Palmer, 1983; Burrows and Hughes, 1990). It is unclear why the disparity exists, however, one possible explanation may be that growth was measured over a much longer period in this study. In Palmer’s (1983) experiments growth was measured over a 28-day period, while Burrows and Hughes (1990) followed growth for only 14 days. When analyzed on a monthly basis, the value of a particular feeding regime in this study varied (Fig. 4). For example, growth of the exposed morphs indicated that barnacles ranked third in June, but were not significantly different from the feeding regimes supporting the highest growth (M or MBH) in August. A similar pattern is apparent for the growth of protected morphs between July and August. Prey value estimated from monthly growth rates may reflect short-term temporal changes in the nutritional quality of a particular prey item. Longer term experiments may provide more consistent measures of prey value. In any event, the temporal variation in growth underscores the importance of conducting growth experiments for more than 30 days.
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Although high mortality in the experimental populations precluded measuring the response of other life history components to the experimental treatments (an unusually high water temperature around Nahant, MA killed most of the field and laboratory snails early in September), growth rates are often correlated with other such components, and are commonly assumed to be positively correlated with fitness (Schoener, 1971; Charnov, 1976; Hughes, 1979). For instance, an increase in food density promoted more rapid growth in N. Zumeflosa which resulted in a larger spawn (Spight, 1974). Palmer (1983) found a negative correlation between growth and age at maturity, and a positive correlation between growth and number of egg capsules deposited for both N. canalicufutu and N. emarginata. From the present analysis it is clear that faster growth rates resulted in a larger size at maturity. Many exposed yearlings reared for 3-5 months under conditions that promote high growth rates exceeded the size at which individuals from their population typically mature (15-19 mm, Etter, 1989) and yet showed no outward signs of maturation. However, the relationship between size and fecundity demonstrated in other populations of N. lapiflus (Crothers, 1985) and in other 1976; Palmer, closely related muricids (Spight et al., 1974; Spight and Emlen, 1983) is more tenuous. Nucella lupillus from exposed shores produced about four times as many offspring than did protected females, despite the significantly smaller size of the former (Etter, 1989). Thus, the positive correlation between size and fecundity in muricids may only hold within populations. Stearns and Koella (1986) demonstrated theoretically and empirically that growth rates can have important consequences for age and size at maturity. Variation in growth rates moved organisms along a trajectory within an age vs. size at maturity space that resulted in a highly plastic phenotype. The results were supported by several empirical examples and suggested most organisms should mature at neither a fixed age nor size. Both field and laboratory results indicate that N. lapillus does not mature at a fixed size. Many exposed yearlings reared on the protected shore or in the laboratory with an overabundance of food exceeded the size at which members of their population typically mature, but exhibited no outward signs of maturation. This suggests size at maturity is not genetically determined, but is a consequence of the growth environment before the onset of sexual maturation. The results presented here also suggest (at least for N. fupillus) that whelks continue to grow after reaching maturity. Most adults, in both the laboratory and field experiments, continued growing, albeit slowly, under benign conditions. Thus, asymptotic size is probably set by extrinsic factors within the local environment such as energetic constraints (Sebens, 1982) or mortality induced by hydromechanical forces generated by breaking waves (Denny et. al., 1985). Our understanding of the forces that shape variation in growth rates of intertidal snails among shores differentially exposed to wave action remains fragmentary. We need to determine exactly how energy is partitioned among the competing demands of growth, reproduction and maintenance. For example, exposed morphs produce about four times as many offspring as protected morphs (Etter 1989) which presumably requires a greater energy investment. Does this increased energy investment contribute to or account for the slower growth rates?
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Growth in N. lapillus is highly plastic and influenced by both prey type and foraging time. The slower growth on exposed shores may in part reflect reduced foraging time, but does not appear to be due to prey type. Only a more detailed analysis of energy allocation will allow us to determine more specifically why growth varies among exposure regimes, but it is clear that reducing the time available for foraging can result in slower growth.
Acknowledgments I thank K. Brown, K. Boss, W. Bossert, M. Patterson, M. Rex, K. Sebens, R. Turner and an anonymous reviewer for their comments on a previous version of this paper. I also thank K. Sebens for providing laboratory and computer facilities at Northeastern University’s Marine Science Center.
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