Lamellose Axial Shell Sculpture Reduces Gastropod Vulnerability to Sea Star Predation.
The form of shell sculpture varies enormously among marine gastropods, ranging from none (smooth shells) to rounded ridges (axial or spiral), flattened blades (e.g., varices, lamellae), stout knobs, and long, delicate spines (Vermeij. 1995). Such sculpture is generally thought to reduce vulnerability to predation (Vermeij, 1978). For example, all forms of sculpture increase the effective diameter of a shell, which can reduce vulnerability to smaller-sized or gape-limited predators (Carter, 1967; Vermeij. 1978; Palmer, 1979). Pronounced varices reduce vulnerability to shell-peeling crabs (Donovan et al., 1999) because the varices reinforce the outer lip of a shell (Vermeij, 1978, 1982). Stout spines or knobs reduce vulnerability to shell-crushing fishes by increasing shell diameter and distributing crushing force more widely over the shell surface (Palmer, 1979). However, the functional significance of axial lamellae--a distinctive type of shell sculpture found in Epitoniidae and several subfamilies of Muricidae (Webster and Vermeij, 2017)--remains puzzling. Such lamellae, which are distinct from true varices (Webster and Vermeij, 2017), appear to be so delicate as not to add much mechanical integrity to a shell. So the question arises: Do such axial lamellae affect vulnerability to predators?
Marine gastropods are commonly eaten by sea stars (Underwood. 1979), and many have behavioral defenses against them, including escape responses (Bullock, 1953; Feder. 1963; Schmitt, 1981) and withdrawal into the shell (Markowitz, 1980; Watanabe, 1983; Bourdeau, 2009; Miner et al., 2013). Sea stars digest snail tissue without crushing or breaking the shell (Watanabe, 1983; Donovan et al., 1999), so shell sculpture might not seem to be an effective defense. However, sculpture does change the effective size, the shape, and the texture of snail shells, and some types of sculpture do appear to affect predation by sea stars on other snail species: removal of pronounced varices increases vulnerability of Ceratostoma foliation (Donovan et al., 1999), and periostracal hairs may interfere with sea star predation, although this effect was quite weak (Iyengar et al., 2008). Nonetheless, defenses provided by external shell morphology against sea star predation are much less well understood than for shell-breaking predators (Donovan et al., 1999). We therefore tested whether axial lamellae in the dogwhelk Nucella lamellosa (Gmelin, 1791) affected feeding success of a predatory sea star, Pisaster ochraceus (Brandt, 1835).
Nucella lamellosa is a well-studied, developmentally plastic intertidal gastropod that exhibits a wide range of shell form, depending on the conditions under which it grows (Spight. 1973; Kitching, 1976; Appleton and Palmer, 1988; Bourdeau, 2012). In Barkley Sound, British Columbia, Canada, and in the San Juan Islands, Washington, it co-occurs widely with P. ochraceus in low- and intermediate-exposure rocky intertidal environments (ON and ARP, pers. obs.). In the presence of shell-breaking crabs or damaged conspecifics, it produces a thicker-shelled, smooth morph with enhanced apertural teeth (Appleton and Palmer, 1988; Bourdeau, 2009) that reduces vulnerability to predation by crabs (Palmer, 1985). The morphological responses of N. lamellosa to sea star predators are more subtle but are reported to include a more elongate shell (Bourdeau, 2009) and greater retractability (Bourdeau, 2009; Miner et al., 2013). In the absence of these risk stimuli, N. lamellosa produces a thinner shell that often bears conspicuous axial lamellae on the outer surface (Appleton and Palmer, 1988). Although thinner shells facilitate more rapid growth (Palmer, 1981) and are therefore beneficial in the absence of predators, the functional significance of prominent lamellae remains unknown. We therefore conducted a laboratory prey-preference experiment where the predatory sea star P. ochraceus was allowed to choose among three shell forms of N. lamellosa: lamellose, artificially smooth, and naturally smooth. Experimental removal of shell sculpture is a useful technique for studying its role in predator defense (Palmer, 1979; Donovan et al., 1999; Iyengar et al., 2008), and it does not appear to change the attractiveness (smell or taste) of snails to sea star predators (Donovan et al., 1999). We hypothesized that N. lamellosa with lamellose shells would be eaten less frequently by P. ochraceus than snails with artificially or naturally smooth shells because sea stars would be less able to grasp securely or manipulate effectively a shell with such a complex, irregular surface.
Materials and Methods
Collection, shell measurement, and manipulation
Organisms were collected haphazardly by hand near the Bamfield Marine Sciences Centre (BMSC) in south Barkley Sound, British Columbia, Canada, in October and November 2015. All organisms were held in sea tables with running seawater at BMSC. Thin-shelled, lamellose Nucella lamellosa (Gmelin. 1791) were collected from the Ross Islets (48.872176, - 125.162113), and naturally smooth, thick-shelled N. lamellosa were collected from Grappler Inlet (48.832247, - 125.114820). Snails were fed Balanus glandula on small stones ad libitum prior to the experiment. Medium-sized Pisaster ochraceus (Brandt, 1835) (central disk radii 15.7-35.4 mm, measured from mouth to armpit) were collected from Dixon Island (48.852243, -125.122373) and fed Mytilus trossulus ad libitum but were starved for 13 days prior to the experiment to maximize hunger.
A Dremel (Racine. WI) 7700 tool was used to artificially grind off lamellae on randomly selected lamellose N. lamellose without damaging the integrity of the shell wall. Snails were dipped in seawater frequently during grinding to prevent overheating and allowed two days to recover before the experiment began. Shells of naturally smooth snails were not modified. We did not include a "grinding" control group (grinding the surface of naturally smooth-shelled snails) to test for effects of shell grinding per se on sea star consumption for two reasons: (a) because a prior study suggested that such mock removal of shell surface features had no effect on consumption of the snail Ceratostoma foliatum by another sea star (Pycnopodia helianthoides) (Donovan et al., 1999), and (b) because of the additional work required to collect, mark, and measure an additional ~100 snails within the limited time available to perform the experiments.
Shell dimensions were measured to the nearest 0.1 mm with digital calipers. Outer body-whorl diameters (excluding the lamellae) were selected to be comparable for all three treatment groups (mean [+ or -] SD and range in mm; n = 64 for each): lamellose, 20.4 [+ or -] 1.85, 16.4-25.2; artificially smooth, 20.8 [+ or -] 1.82, 16.5-25.2; naturally smooth, 20.6[+ or -] 1.72, 16.9-25.4. Differences among these groups were not significant (ANOVA, [F.sub.2,189] = 1.05, P = 0.35). Because of differences in shell shape between lamellose and naturally smooth shells, shell lengths did differ by about 10% among the three treatment groups (mean [+ or -] SD and range in mm; n = 64 for each): lamellose, 38.6 [+ or -] 3.91, 26.1-46.8; artificially smooth, 37.9 [+ or -] 3.90, 27.2-45.8; naturally smooth, 34.5 [+ or -] 3.34, 27.9-40.6. These differences were significant (ANOVA, [F.sub.2,189] = 22.05, P < 0.001). Because some snails can recede too deeply into their shell for their operculum to be visible, total wet weight of snails was recorded to the nearest 0.01 g with a digital balance, to allow us to confirm a predation event via a significant weight loss after being eaten.
The experiment was conducted at BMSC in sea tables receiving a constant flow of seawater. Individual P. ochraceus were randomly placed into a covered plastic container (28 cm x 19.5 cm x 14 cm) perforated to allow water flow and were allowed one hour to acclimate. One snail of each shell type--lamellose, artificially smooth, and naturally smooth (Fig. 1)--was introduced in random order at equal distance from the sea star. All three snails in a single container had the same actual shell widths ([+ or -]2 mm). Containers were checked every 3-12 hours for evidence of predation. Snails were confirmed to have been consumed by comparing dead wet weight to initial live wet weight. Significantly--to ensure that each trial was a true and independent replicate--the remaining two uneaten snails were removed from the container following a confirmed predation event, and three new snails were introduced to the same sea star. This protocol was repeated over 20 days, during which a total of 64 sets of 3 snails (total = 192) were introduced to the sea stars.
A Pearson's chi-squared test was conducted on the total number of snails of each shell type consumed, to test whether shell types were consumed equally. This test assumed that predation events were independent (i.e., each shell type had a 0.33 probability of being eaten). In addition, 95% confidence intervals (CIs) on the total number of snails of each shell type consumed were bootstrapped by randomly resampling counts of snails of each shell type eaten by individual sea stars 10.000 times with replacement (Tibshirani and Leisch, 2015). Total observed counts were compared to the number expected to be consumed if all shell types were frequently consumed equally. A Fisher's exact test was conducted on the number of each shell type consumed by individual sea stars to determine whether there was any nonrandom association among individual sea stars and shell types consumed. Graphing and analyses were done using RStudio, version 3.1.0 (R Core Team. 2014). Bootstrapping was done using the R package "bootstrap," version 2015.2 (Tibshirani and Leisch, 2015).
Sixty-one Nucella lamellosa were consumed by the 13 Pisaster ochraceus over 20 days: 8 lamellose, 22 artificially smooth, and 31 naturally smooth (Fig. 2). Sea stars consumed between one and eight snails each (Table 1). Snails of each shell type were not eaten equally (Pearson's [X.sup.2] = 13.2, df = 2, P = 0.0014). The number of each shell type expected to be consumed if P. ochraceus exhibited no preference was one-third of all snails consumed (20.3 individuals). The 95% CI bootstrapped on the total number of each shell type consumed did not overlap this expected value for lamellose snails, while artificially smooth and naturally smooth snails did not differ significantly from expected (Fig. 2). A Fisher's exact test revealed no significant variation in the number of each shell type consumed among individual sea stars (P = 0.27).
Functional significance of lamellose axial shell sculpture
Our results suggest that the lamellae themselves of Nucella lamellosa shells, rather than other aspects of shell morphology, effectively reduce vulnerability to sea star predation. Previous work on the direct mechanism of defense against shell-entry predators suggests that certain shell morphs allow for deeper withdrawal of soft tissue (Markowitz, 1980; Watanabe, 1983; Bourdeau, 2009; Miner et al., 2013) or that a lighter shell allows for less energetically costly escape (Bourdeau, 2009). However, our inclusion of the artificially smooth treatment suggests that lamellae directly reduce vulnerability to sea star predation because artificially smooth snails would have had similar withdrawal depth and theoretically less costly movement. External sculpture also appears to reduce the vulnerability of other marine gastropods to sea stars (Donovan et al., 1999: Iyengar et al., 2008). Although we did not specifically measure withdrawal depth, we believe that our assumption that lamellose and artificially smooth snails would have similar withdrawal depths is warranted for two reasons. First, shell length is a good predictor of body weight in N. lamellosa (Palmer, 1981). Second, lamellose and artificially smooth snails were collected from the same source population. Naturally smooth snails might have had different withdrawal depths, because they were collected from a different source population, so the small difference in consumption rates between naturally and artificially smooth shells might have been affected by this.
Our experimental design, which replaced all three shell types after any one individual snail had been consumed, ensured that each predation event for an individual sea star was truly independent. Although prey choice by sea stars may be affected by previous choices, a similar study (Donovan et al., 1999) found no evidence for learned preference or avoidance of artificially altered marine gastropod prey by another sea star predator. Pisaster ochraceus does appear to show some conditioned preferential feeding, but conditioning required a study more than four times longer in duration than ours and used different prey species with different morphologies (Landenberger, 1968). Our conclusion that lamellae reduce sea star preference is further supported by a Fisher's exact test showing no statistically significant association between shell types consumed and individual sea stars (P = 0.27).
Lamellar sculpture may reduce vulnerability to sea stars via two different mechanisms. First, and we think more likely, lamellae create a more complex and irregular surface that may be more difficult for sea stars to grasp and manipulate with their podia. Second, lamellae create a larger effective size: actual maximum diameters of shells with lamellae were larger than those with lamellae experimentally removed, because all three snails in each trial were matched for actual body-whorl diameter ([+ or -]2 mm), which did not include lamellae. Naturally smooth shells had a naturally shorter shell length than lamellose shells when matched by width, which also suggests that size may be a factor. A larger effective size could deter predators such as sea stars that cannot capture or manipulate larger prey effectively.
The literature provides few clues about which mechanism might be more likely to reduce Pisaster feeding success: more complex surface topography or larger effective size of the shell. The effects of surface texture on podia tenacity are mixed. Individual sea star podia attached significantly less strongly to a mussel shell than a glass surface (Flammang and Walker, 1997). However, both sea stars and sea urchins had a higher total tenacity per podium on an artificially roughened plastic surface compared to a smooth one, although this difference disappeared once the greater surface area of the roughened surface under a podium was taken into account (Santos et al., 2005). Regardless, the topographical scale of the "rough" surface in both of these studies was small ([much less than] 1 mm) and considerably less than that provided by lamellar sculpture (up to 5 mm); and the scale of the surface texture is likely to have a big impact on tenacity (Dodou et al., 2011). Patterns of prey-size preferences by sea stars are also mixed. Pisaster ochraceus seem to prefer larger barnacle prey (Menge and Menge, 1974). But adults also consume significantly more small mussels than medium or large ones, a pattern reversed in juveniles (Gooding and Harley, 2015). Furthermore, sea stars preferred smaller prey when feeding on infaunal bivalves but preferred larger epifaunal prey when feeding on urchins and sand dollars (Gaymer et al., 2004). Both studies suggest that prey are chosen to provide the most energy per unit handling time (Gaymer et al., 2004; Gooding and Harley, 2015).
Functional significance of shell developmental plasticity in Nucella lamellosa
Nucella lamellosa is the first, and arguably best-studied, example of developmental plasticity in gastropod shells (Appleton and Palmer. 1988: Bourdeau, 2009, 2012, 2015: Miner et al., 2013). Our results add an important new piece of evidence for the adaptive nature of this plasticity: in habitats where shell-breaking crabs are rare, thin shells with lamellose sculpture may be less vulnerable to predation by sea stars. Therefore, plastic defenses in N. lamellosa, including shell thickness (Bourdeau, 2012), apertural teeth (Appleton and Palmer, 1988), and lamellose sculpture (this study), all appear to be adaptive, depending on which risk is greater in a multipredator environment that includes crabs and sea stars. Intriguingly, in southeast Alaska populations of N. lamellosa outside the geographic range of the shell-breaking crab Cancer productus, the thin-shelled lamellose phenotype persists in a wide range of habitats--including protected shores--that would normally only have the thick-shelled, smooth form (ARP, pers. obs.). Our results demonstrate that the lamellose phenotype is less vulnerable to sea star predation, emphasizing that heterogeneous predation pressure over multipredator environments could be an important selective force influencing the evolution of plasticity in N. lamellosa. While genetic differences are also bound to influence the evolution of phenotypic plasticity, ecophenotypic variation in gastropod shells in response to multiple predators may explain geographic and temporal variation in shell morphology (Appleton and Palmer, 1988; Palmer, 1990). Although the geographic distribution and function of the thicker-shelled smooth morph of N. lamellosa is well understood, to our knowledge this is the first study to demonstrate a functional explanation for the presence and distribution of the lamellose phenotype.
Our results raise a number of testable questions. First, additional experiments on "graspability" of lamellose and experimentally smoothed shells (e.g., the force required to remove a shell from a sea star's grip) would be required to test whether lamellae reduce vulnerability to sea stars by reducing the ability of sea stars to grasp and manipulate the shell or by increasing effective size. Given the impressive degree of phenotypic plasticity in the shells of N. lamellosa (Appleton and Palmer. 1988), it would be interesting to test whether larger lamellae are grown in the presence of sea star predators. The potential for sea star-induced lamellar growth is not unrealistic, because lamellar growth is highly variable (Webster and Palmer, 2016). and N. lamellosa shells meet the prerequisites for evolution of inducible defense (Tollrian and Harvell, 1999): (1) the selective pressure of P. ochraceus predation is variable (Miner et al., 2013); (2) P. ochraceus provides a reliable cue (Bourdeau, 2009; Miner et al., 2013); (3) lamellae are an effective defense (this study); and (4) trade-offs exist among the costs and benefits of different forms in habitats with different predators. Furthermore, developmentally plastic induction of lamellae would support an active and adaptive direct response to predator cues (Appleton and Palmer. 1988: Palmer. 1990). rather than a passive and indirect reduced feeding and predator avoidance behavioral response (Bourdeau et al., 2015 and references therein), a debate that persists regarding other shell traits.
We thank Nicole Webster for advice on collecting and feeding snails; Tao Eastham, Erin Hornell, Chris Neufeld, and three reviewers for thoughtful comments on this manuscript; Allan Roberts for advice regarding data analysis; and the staff and fall program at the Bamfield Marine Sciences Centre for the support in field and laboratory work that greatly facilitated this project.
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OWEN MAVSON (1,4,*), ROKZANNA BASF (2,4,[dagger]), AND A. RICHARD PALMER (3,4)
(1) Department of Biology, University of Victoria, Victoria, British Columbia V8P 5C2, Canada; (2) Faculty of Science, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada; (3) Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada; and Bamfield Marine Sciences Centre, 100 Pachena Road, Bamfield, British Columbia VOR 1BO, Canada
(*) To whom correspondence should be addressed. Present address: Bamfield Marine Sciences Centre, 100 Pachena Road. Bamfield. British Columbia VOR 1B0, Canada. E-mail: firstname.lastname@example.org.
[dagger] Present address: St. George's University of London, Cranmer Terrace, London SW17 ORE, United Kingdom.
Abbreviations: BMSC, Bamfield Marine Sciences Centre; CI. confidence interval.
Received 13 October 2017: Accepted 22 May 2018; Published online 23 July 2018.
Table 1 Number of lamellose, artificially smooth, and naturally smooth Nucella lamellosa consumed and a total of all shell types consumed by each of 13 individual Pisaster ochraceus P. ochraceus Lamellose Artificially smooth Naturally smooth Total 1 0 2 3 5 2 0 2 6 8 3 1 3 3 7 4 1 0 6 7 5 0 3 1 4 6 1 1 2 4 7 1 3 1 5 8 0 2 3 5 9 0 0 1 1 10 0 1 0 1 11 0 2 3 5 12 3 1 1 5 13 1 2 1 4 Total 8 22 31 61
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|Author:||Mavson, Owen; Basf, Rokzanna; Palmer, A. Richard|
|Publication:||The Biological Bulletin|
|Date:||Aug 1, 2018|
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