SHELL SHAPE AND TISSUE WITHDRAWAL DEPTH IN 14 SPECIES OF TEMPERATE INTERTIDAL SNAIL TIMOTHY C. EDGELL 1,2 AND TETSUTO MIYASHITA 1,2 1
Bamfield Marine Sciences Centre, 100 Pachena Road, Bamfield, BC, Canada V0R 1B0; and Department of Biological Sciences, University of Alberta, Edmonton, AB, Canada T6G 2E9
2
(Received 1 October 2008; accepted 24 February 2009)
ABSTRACT Predation is an important selective agent in the evolution of gastropod shell form. The adaptive value of shell elongation, however, has received relatively little attention in the context of predation. Arguments for its functional significance include the hypothesis that shell elongation facilitates soft tissue withdrawal inside the shell, thus elongation may improve fitness when predation by shell entry is intense. Here we ask whether species with more elongate shells also retract more deeply, a longheld assertion that until now lacked empirical support. To do this, we measured shell elongation (shell height divided by breadth) and soft-tissue withdrawal depth (angular retraction) in 14 species of temperate marine snail, covering a wide range of shell forms. Results show shell elongation to be a good predictor of angular retraction across genera and distantly related species. However, the elongation-retraction relationship was not apparent in comparisons among closely related species (specifically, species of Nucella and Littorina), nor were there such relationships among individuals within species (except, perhaps, within a few species having high shell-shape diversity). Competing arguments for the functional significance of shell elongation are discussed, as is the potential role of environment in affecting shell elongation and withdrawal depth independently.
INTRODUCTION The importance of predation in the evolution of shell form among molluscs is widely acknowledged. Marine gastropods, for example, have evolved elaborate shell characters like tubercules, apertural teeth and thickened walls to defend against gape-limited shell swallowers, apertural-lip peelers and crushers (Zipser & Vermeij, 1978; Palmer, 1979; Bertness & Cunningham, 1981; Reimchen, 1982; Schindel, Vermeij & Zipser, 1982). Predation by shell entry (whereby predators insert an appendage into the shell and extract prey flesh) is perhaps the least studied mode of molluscivory, yet is used widely by molluscivores including birds, sea stars and decapods (Vermeij, 1987: 145). Apertural occlusion can reflect adaptation to shell-entry predation, because narrow or small apertures defend against shell-entry predators by limiting the entry depth of a predator’s probing appendage (DeWitt, Robinson & Wilson, 2000). However, species with large, round apertures (characteristic of temperate, marine gastropods) are also faced with shell-entering predators (Bauer, 1913; Hiatt, 1948; Ebling et al., 1964; Johannesson, 1986; Rochette, Doyle & Edgell, 2007; Edgell & Rochette, 2008; Edgell et al., 2008); thus apertural occlusion may not always reflect the prominence of shell-entry predation in natural populations. Shell elongation (in those that maintain round, unobstructed apertures) may enlighten our understanding of anti-entry adaptation, because elongation is thought to facilitate deeper soft-tissue withdrawal depth (Vermeij 1987: 220), the latter being a demonstrably adaptive defence against shell-entering crabs (Edgell et al., 2008). However, the suggestion that gastropods with more elongated shells also retract more deeply into them lacks empirical support. To test if such a relationship exists, we measured shell elongation and soft-tissue withdrawal depth (angular retraction) in 14 species of temperate, intertidal snail, including members of seven families and covering a wide Correspondence: T.C. Edgell; e-mail:
[email protected]
range of shell forms (Fig. 1, Table 1). Results indicate that shell elongation is positively correlated with tissue-withdrawal depth across genera and species, but not within species lacking appreciable variability in shell form. Competing arguments for the functional significance of shell elongation are discussed, as is the potential role of the environment in affecting elongation and angular retraction independently.
MATERIALS AND METHODS Collections Fourteen species of marine gastropod, representing seven families, were collected from intertidal shores in Pacific and Atlantic Canada (Fig. 1, Table 1). Species from Pacific Canada, from various locations near Bamfield, British Columbia (498190 N, 1258190 W): Amphissa columbiana (8.40–19.74 mm shell height SH), Bittium eschrichtii (8.13–15.71 mm SH), Calliostoma canaliculatum (9.23–19.42 mm SH), Littorina scutulata (6.54– 11.83 mm SH), L. sitkana (5.44–15.48 mm SH), Lirabuccinum dirum (13.78–31.29 mm SH), Nucella canaliculata (16.16–27.51 mm SH), Nucella lamellosa (14.70–47.88 mm SH), Nucella ostrina (13.44– 23.59 mm SH), Ocinebrina interfossa (8.91–17.97 mm SH), Ocinebrina lurida (10.52–18.22 mm SH) and Tegula funebralis (7.20–25.92 mm SH). Species from Atlantic Canada, near St Andrews, New Brunswick (458040 N, 678020 W): L. obtusata (4.76–14.32 mm SH) and L. littorea (5.98–16.17 mm SH).
Measures of shell, and tissue-withdrawal depth Shell height and breadth were measured to the nearest 0.01 mm using dial calipers, with shells in the standard position described by Reid (1996). Shell elongation was calculated as shell height divided by breadth (Fig. 1), a dimensionless metric that allows comparison of shell shape regardless of differences in overall shell size.
Journal of Molluscan Studies (2009) 75: 235–240. Advance Access Publication: 8 May 2009 # The Author 2009. Published by Oxford University Press on behalf of The Malacological Society of London, all rights reserved.
doi:10.1093/mollus/eyp018
T. C. EDGELL AND T. MIYASHITA
Figure 1. Line drawings of the intertidal gastropods used in this study, in order of increasing shell elongation. A. Tegula funebralis. B. Calliostoma canaliculatum. C. Littorina obtusata. D. Littorina littorea. E. Littorina sitkana. F. Littorina scutulata. G. Nucella osterina. H. Nucella lamellosa (a sculptured morph and a smooth morph). I. Nucella canaliculata. J. Lirabuccinum dirum. K. Ocinebrina lurida. L. Amphissa columbiana. M. Ocinebrina interfossa. N. Bittium eschrichtii, showing measurement of shell height and breadth. Scale bars ¼ 5 mm. Table 1. Summary of regression lines, describing the relationship between shell elongation (height/breadth) and angular retraction (y ¼ angular retraction; x ¼ shell elongation). Group analysis
R2
Family
n
Equation (slope)x þ (intercept)
P
Shape (sum variance)
Amphissa columbiana (1)
Columbellidae
13
(65.79)x þ (25.60)
0.05
2.08 1023
Bittium eschrichtii (2)
Cerithidae
40
(20.35)x þ (198.19)
,0.001
0.98
1.87 1023
Calliostoma canaliculatum (1)
Calliostomatidae
20
(244.63)x þ (181.69)
0.055
0.32
0.55 1023
Littorina scutulata (2)
Littorinidae
40
(33.23)x þ (74.55)
0.170
0.008*
1.56 1023
Littorina sitkana (2)
Littorinidae
35
(238.10)x þ (172.26)
0.067
0.13
0.74 1023
Littorina obtusata (1)
Littorinidae
24
(30.56)x þ (97.77)
0.005
0.73
n/a
Littorina littorea (1)
Littorinidae
24
(273.03)x þ (219.60)
0.060
0.25
n/a
Lirabuccinum dirum (3)
Buccinidae
42
(58.30)x þ (34.73)
0.089
0.06
1.29 1023
Nucella canaliculata (2)
Muricidae
40
(246.39)x þ (186.57)
0.057
0.14
0.65 1023
Nucella lamellosa (3)
Muricidae
60
(54.53)x þ (67.82)
0.135
0.004*
3.40 1023
Nucella ostrina (4)
Muricidae
62
(34.87)x þ (45.20)
0.022
0.25
0.97 1023
Ocinebrina interfossa (1)
Muricidae
20
(254.59)x þ (302.88)
0.190
0.06
2.49 1023
Ocinebrina lurida (1)
Muricidae
22
(25.40)x þ (168.82)
0.001
0.89
1.12 1023
Tegula funebralis (2)
Turbinidae
40
(65.02)x þ (79.06)
0.188
0.005*
2.91 1023
8
(31.38)x þ (96.53)
0.73
0.007**
Within species (no. of populations)
Among genera (Fig. 3A)
0.308
Among species (Fig. 3B)
14
(31.85)x þ (92.05)
0.46
0.008**
Among species and populations (Fig. 3C)
26
(33.03)x þ (85.28)
0.37
0.001**
Shell-shape diversity was computed for each species as the summed variance of all principal components, minus the first principal component that explained primarily differences in size. *Significant when a ¼ 0.013. **When a ¼ 0.011 (following Benjamini & Hochberg, 1995).
Soft-tissue withdrawal depth was measured as the angular distance of retraction, following Edgell & Rochette (2008; see also Edgell et al., 2008); like our metric of shell elongation, angular retraction measurements are independent of overall shell size. While submerged (to avoid trapping of air bubbles), snails were prodded aggressively with forceps to simulate the attack of a shell-entering predator. Prodding of the snail’s operculum and any exposed flesh, and scraping of the inside shell wall, continued until the snail stopped withdrawing more deeply into its shell. Locating the snail’s fully withdrawn position inside of its shell was done by shining a diffuse laserpointer in through the shell aperture, making the snail’s body position visible via the translucence of the shell wall. The closest point of the snail body to the outer mid-point of the
apertural lip was marked on the outside surface of the shell wall. With retraction distance marked, snails were frozen. Upon thawing, a needle was inserted into the shell as deeply as it would go while keeping the needle shaft in contact with the outer mid-point of the shell lip. Angular distance of retraction was measured relative to the trajectory of the needle’s penetration. With needle in place, each shell was photographed, parallel to the plane of the aperture (apex pointing away from lens) and perpendicular to the axis of the needle. The angular distance of retraction was then measured at the mid-point of the needle (where in contact with the columella, inside the shell), from mid-lip to the point that marked the position of the retracted snail (Fig. 2). 236
SHELL SHAPE AND ANGULAR RETRACTION
Figure 2. Schematic drawings to indicate the method of measuring angular retraction depth (u). Depicted here is Littorina sitkana. Apical view (left) shows the point of the maximum withdrawal (arrow head); shaded area represents the space vacated by the snail, lit by a laser pointer. Broken line represents the extension of the line of sight (needle trajectory) used for measurement of angular retraction (u); mid-point of line of sight is equal distance from both sides of the shell.
Regression analyses tested for a relationship between shell elongation and angular retraction (1) for each species individually (samples pooled for multi-site collections) and (2) across genera (n ¼ 8), species (n ¼ 14) and populations of species (n ¼ 26), by calculating mean elongation and mean angular retraction for each group. Moreover, because species and genera differed markedly in size (e.g. individuals of L. scutulata had shell heights 6.54 –11.83 mm, whereas Nucella lamellosa had shell heights 14.70–47.88 mm), we also tested for correlations between (1) shell height and elongation, and (2) shell height and angular retraction, a necessary step given the relationships between elongation and angular retraction (Fig. 3) could be confounded by group-level differences in shell size. Moreover, to mitigate the potentially confounding effect of taxon on the structuring of the elongation-retraction relationships shown in Figure 3 (i.e. not all genera were represented by the same number of species), trait correlations were explored further within the genera that contained adequate samples for regression analysis (i.e. three or more species): Littorina (n ¼ 4 species, n ¼ 6 populations) and Nucella (n ¼ 3 species, n ¼ 9 populations).
Interspecific shell-shape diversity Shell-shape diversity was computed for each species as the summed variance of all but the first principal component, scaled for the percent of variance explained by each component (Foote, 1992, 1997). Variance from the first component (87.6% of total) was excluded to remove the effect of size from our shape index; loadings on the second and subsequent components were unlikely to carry information on differences in shell size since they were highly dissociated between the variables (Bookstein, 1989). In other words, for second and subsequent components, eigenvalue loadings (for shell height, shell breadth, aperture height and aperture width) differed significantly in magnitude and positive/negative direction, an expected result if components were to detect differences in shell shape instead of size (Bookstein, 1989). By contrast, eigenvalue loadings in the first component had very similar magnitudes and were all positive (data not shown), an expected result since all variables (shell height, shell breadth, aperture height, aperture width) co-vary positively with overall shell size. Principal component analysis (variance-covariance matrix) was performed using log-transformed shell measurements that describe overall shell shape: shell height, shell breadth, aperture height (longest dimension within the apertural lip, parallel to the columella) and aperture width (maximum dimension with the apertural lip, perpendicular to aperture height). L. littorea and L. obtusata were excluded because only shell height and width measurements were available.
Figure 3. Mean angular retraction as a function of mean shell elongation in temperate intertidal gastropods. Data grouped by: A. Genera, n ¼ 8; B. Species, n ¼ 14; C. Species and populations of species, n ¼ 23. All regression slopes were different from zero (P 0.009). Standard error of the mean is smaller than symbols.
RESULTS The relationship between shell elongation and angular retraction was statistically significant in three species after adjusting a, the probability of Type I error, for multiple comparisons (Benjamini & Hochberg, 1995; Table 1): Littorina scutulata, Nucella lamellosa and Tegula funebralis. For one of these species, Nucella lamellosa, variation in angular retraction was more strongly correlated with variation in shell height (R 2 ¼ 0.37, P , 0.0001, n ¼ 60) than to elongation (R 2 ¼ 0.14, P ¼ 0.004, n ¼ 60), but shell height was also correlated strongly with elongation (R 2 ¼ 0.31, P , 0.0001, n ¼ 60), making their independent contributions to retraction difficult to parse. Comparisons of shell elongation and angular retraction across genera, species and populations of species were positive and significant (Fig. 3A–C): across genera (R 2 ¼ 0.73, P ¼ 0.007, n ¼ 8), across species (R 2 ¼ 0.46, P ¼ 0.008, n ¼ 14) and across populations of species (R 2 ¼ 0.37, P ¼ 0.001, n ¼ 26). However, there was no relationship between elongation and 237
T. C. EDGELL AND T. MIYASHITA angular retraction among species within the genus Littorina (species R 2 ¼ 0.19, P ¼ 0.57, n ¼ 4; populations of species R 2 ¼ 0.15, P ¼ 0.44, n ¼ 6) or Nucella (species R 2 ¼ 0.012, P ¼ 0.93, n ¼ 3; populations of species R 2 ¼ 0.10, P ¼ 0.40, n ¼ 9). Correlations between shell elongation and angular retraction (depicted in Fig. 3) were independent of group-level differences in shell size (shell height, SH). This was true across genera (n ¼ 8; elongation R 2 ¼ 0.006, P ¼ 0.86; angular retraction R 2 ¼ 0.09, P ¼ 0.48), across species (n ¼ 14; elongation R 2 ¼ 0.05, P ¼ 0.46; angular retraction R 2 ¼ 0.0005, P ¼ 0.94) and across populations of species (n ¼ 26; elongation R 2 ¼ 0.03, P ¼ 0.39; angular retraction R 2 ¼ 0.002, P ¼ 0.82). With the exception of L. scutulata, those species showing a significant relationship between shell elongation and angular retraction also tended to have greater shell-shape diversity (Table 1).
2007). In other words, inferences about shell-crushing defence (based on shell thickness) confound inferences about shell-entry defence (based on aperture occlusion). Here we show that species with more elongate shells also withdraw more deeply into their shells (Fig. 1). Shell elongation (a conspicuous, fossilized and easily measured trait) may therefore be a valuable alternative to aperture occlusion as a morphologybased predictor of anti-entry defence. Furthermore, shellcrushing and shell-entry should select for shell elongation in opposite directions, thus removing any confounding response to shell-crushing predation (cf. narrow or occluded apertures): elongate shells, while giving poor defence against shell crushers because the oldest and thinnest whorls are exposed (Zipser & Vermeij, 1978; Seeley, 1986; Edgell & Neufeld, 2008), are theoretically good for defending against shell-probing predators because they allow for deeper tissue withdrawal. To test this hypothesis would entail comparative shell-entry predation experiments across taxa with diverse shell forms. The among-group trends (depicted in Fig. 3A–C) seem to be driven largely by genus-level differences in elongation and angular retraction (Fig. 3A), since similar comparisons among species within genera (namely, the three species of Nucella and the four species of Littorina) showed no similar relationships between elongation and retraction (P 0.44). This genus-level effect presents an obstacle for our main inference because, in the absence of an elongation-retraction covariance between closely related species, we cannot reasonably expect selection in an ancestral population to have resulted in the among-species differences we now see between extant species. Moreover, because elongation and retraction generally do not co-vary within a single species (except, perhaps, within species having high shell-shape diversity, see Table 1) it is difficult to envisage a selection regime whereby the preservation of either elongate shells or deep soft-tissue retractors drives a concurrent change in the other trait. As for the northern Atlantic gastropod L. obtusata, average angular retraction differs significantly among populations despite no discernable differences in shell shape (i.e. maximum mean angular retraction is 1208 vs minimum 608, in a comparison of 12 populations; Edgell et al., 2008). Furthermore, variability in withdrawal depth can sometimes be a function of local environment (i.e. via phenotypic plasticity), such as (1) the presence or absence of predation cues (i.e. L. obtusata increases angular retraction when exposed to crab effluent, but Nucella lamellosa does not; TCE, unpublished data, following protocols described in Edgell & Neufeld, 2008), (2) the degree of individual satiation (i.e. L. obtusata starved for 14 days have greater angular retraction than conspecifics fed ad libitum; TCE, unpublished data) or (3) reproductive state (e.g. egg-bearing females may be less able to retract deeply). These latter two assertions imply that maximum withdrawal depth is governed by a physical constraint, imposed by a finite shell volume on a largely incompressible body—smaller bodies (e.g. starved snails and females devoid of eggs) may withdraw deeper than larger bodies. Similarly, shell elongation can be explained in part by ecotypic variation; in L. littorea shells develop to be more elongate when resources are plentiful and growth rate is fast (Kemp & Bertness, 1984). Interestingly, species showing a significant relationship between shell elongation and angular retraction typically have greater intraspecific variance in shell shape (with the exception of L. scutulata, Table 1), suggesting low shell-shape diversity may preclude natural selection (for deeper withdrawal depths) from driving the evolution of more elongate shells. Hypotheses unrelated to predation may also explain spatial and temporal differences in shell elongation. Graus (1974) found a higher incidence of globose shells at temperate than tropical latitudes, and proposed globosity at higher (colder) latitudes reflects economical use of costly shell material – per unit of shell
DISCUSSION Adaptations of predators for shell-crushing (e.g. larger, more powerful claws and jaws), and of gastropods for resistance to crushing (e.g. thicker, heavier shells), consist of hard parts that are easily measured and conspicuous in both fossil and modern animals, facilitating the study of shell-crushing predation across evolutionary and ecological timescales (Palmer, 1979; Bertness & Cunningham, 1981; Reimchen, 1982; Vermeij, 1982; Seeley, 1986; Dietl, 2003). For example, from the Silurian to the Cenozoic (about 420 million years) molluscivores adapted for the shell-crushing habit diversified together with gastropods having internally thickened shells (Vermeij, 1987: 187, 218). On a much shorter timescale, that of an individual’s lifetime, many living gastropods produce thicker, heavier shells when exposed to effluent from a shell-crushing predator (Appleton & Palmer, 1988; Trussell & Smith, 2000; Freeman & Byers, 2006); demonstrably, added shell thickness or weight is an adaptive defence against shell-crushing predators (e.g. Lowell et al., 1994; Edgell & Neufeld, 2008). In contrast, adaptations for shell-entry (e.g. in predators: eversible stomachs of sea stars, or probing behaviours by crabs), and entry-resistance (e.g. in gastropods: soft-tissue withdrawal depth) comprise non-fossilized traits that are generally cryptic unless observed directly in living specimens. The relative ease of discerning shell-crushing traits over shell-entry traits is reflected in the former’s disproportionate appearance in the studies of mollusc-molluscivore ecology and evolution. For example, a literature review (Edgell, 2007) revealed 90 of 113 studies about decapod-gastropod interactions, dating to Bauer (1913), focused on shell-crushing. In the 22 studies where shell-entry appeared, it was typically as a narrative, unlike the largely quantitative approach to studying the evolutionary ecology of shell-crushing (Edgell, 2007). Shell-entry predation is nonetheless important in the ecology of some modern decapod-gastropod pairs, warranting greater consideration in the natural history of gastropods’ anti-predator evolution (Johannesson, 1986; DeWitt et al., 2000; Rochette et al., 2007; Edgell et al., 2008). Although tissue-withdrawal depth (angular retraction) is a strong predictor of survivorship when snails are attacked by shell-entering crabs (Edgell et al., 2008), withdrawal depth is practically impossible to measure on dead specimens. Aperture occlusion also predicts survivorship (DeWitt et al., 2000; Edgell et al., 2008), thus aperture size (a fossilized trait) is understandably a better endpoint than withdrawal depth for studying the macroevolution of shell-entry defence when direct measures of withdrawal are impractical (e.g. fossils, shell collections). A difficulty with using aperture size, however, is that shell thickness and aperture size are correlated characters—as shells thicken internally, apertures become smaller (Brookes & Rochette, 238
SHELL SHAPE AND ANGULAR RETRACTION BROOKES, J.I. & ROCHETTE, R. 2007. Mechanism of a plastic phenotypic response: predator-induced shell thickening in the intertidal gastropod Littorina obtusata. Journal of Evolutionary Biology, 20: 1015– 1027. DEWITT, T.J., ROBINSON, B.W. & WILSON, D.S. 2000. Functional diversity among predators of a freshwater snail imposes an adaptive trade-off for shell morphology. Evolutionary Ecology Research, 2: 129–148. DIETL, G.P. 2003. Coevolution of a marine gastropod predator and its dangerous bivalve prey. Biological Journal of the Linnean Society, 80: 409–436. EBLING, F.J., KITCHING, J.A., MUNTZ, L. & TAYLOR, C.M. 1964. The Ecology of Lough Ine: experimental observations of the destruction of Mytilus edulis and Nucella lapillus by crabs. Journal of Animal Ecology, 33: 73–82. EDGELL, T.C. 2007. Evidence of ecological and evolutionary interactions between an exotic crab Carcinus maenas and two species of Littorina snail in the northwest Atlantic. PhD thesis, University of New Brunswick. EDGELL, T.C., BRAZEAU, C., GRAHAME, J.W. & ROCHETTE, R. 2008. Simultaneous defense against shell entry and shell crushing in a snail faced with the predatory shorecrab, Carcinus maenas. Marine Ecology Progress Series, 371: 191– 198. EDGELL, T.C. & NEUFELD, C.J. 2008. Experimental evidence for latent developmental plasticity: intertidal whelks respond to a native but not an introduced predator. Biology Letters, 4: 385– 387. EDGELL, T.C. & ROCHETTE, R. 2008. Differential snail predation by an exotic crab and the geography of shell-claw covariance in the northwest Atlantic. Evolution, 62: 1216–1228. FOOTE, M. 1992. Paleozoic record of morphological diversity in blastozoan echinoderms. Proceedings of National Academy of Sciences of the USA, 89: 7325–7329. FOOTE, M. 1997. The evolution of morphological diversity. Annual Review of Ecology and Systematics, 28: 129– 152. FREEMAN, A.S. & BYERS, J.E. 2006. Divergent induced responses to an invasive predator in marine mussel populations. Science, 313: 831–833. GRAUS, R.R. 1974. Latitudinal trends in the shell characteristics of marine gastropods. Lethaia, 7: 303–334. HIATT, R.W. 1948. The biology of lined shore crab, Pachygrapsus crassipes Randall. Pacific Science, 2: 135–213. JOHANNESSON, B. 1986. Shell morphology of Littorina saxatilis Olivi: the relative importance of physical factors and predation. Journal of Experimental Marine Biology and Ecology, 102: 183– 195. KEMP, P. & BERTNESS, M.D. 1984. Snail shape and growth rates: evidence for plastic shell allometry in Littorina littorea. Proceedings of the National Academy of Sciences of the USA, 81: 811–813. LOWELL, R.B., FLETCHER, C.R., GRAHAME, J.W. & MILL, P.J. 1994. Ontogeny of shell morphology and shell strength of the marine snails Littorina obtusata and Littorina mariae: different defense strategies in a pair of sympatric, sibling species. Journal of Zoology, London, 234: 149–164. MALONE, P.G. & DODD, J.R. 1967. Temperature and salinity effects on calcification rate in Mytilus edulis and its paleoecological implications. Limnology and Oceanography, 12: 432– 436. PALMER, A.R. 1979. Fish predation and the evolution of gastropod shell sculpture: experimental and geographic evidence. Evolution, 33: 697–713. REID, D.G. 1996. Systematics and evolution of Littorina. Ray Society, London. REIMCHEN, T.E. 1982. Shell size divergence in Littorina mariae and L. obtusata and predation by crabs. Canadian Journal of Zoology, 60: 687–695. ROCHETTE, R., DOYLE, S.P. & EDGELL, T.C. 2007. Interaction between an invasive decapod and a native gastropod: predator foraging tactics and prey architectural defenses. Marine Ecology Progress Series, 330: 179– 188. SEELEY, R.H. 1986. Intense natural selection caused a rapid morphological transition in a living marine snail. Proceedings of the National Academy of Sciences of the USA, 83: 6897– 6901.
mass, globose shells maximize internal shell volume (Kemp & Bertness, 1984) and calcium carbonate is more soluble (i.e. less bio-available) in colder water (Malone & Dodd, 1967). This hypothesis does not explain, however, why both globose and elongate morphologies exist sympatrically in temperate regions (e.g. Fig. 1). Alternatively, predation may be an important factor in determining shell length, but not necessarily via shell-entry predation. As stated above, shells may evolve from elongate to globose under intense, shell-crushing predation, because elongate shells expose their thinnest, most vulnerable whorls to predators, unlike globose shells that protect old whorls with newer, thicker shell growth (Seeley, 1986). Predation experiments corroborate this latter hypothesis; shell-crushing crabs target older, more vulnerable shell whorls when fed Nucella lamellosa whelks with experimentally thickened apertural margins (Edgell & Neufeld, 2008).
CONCLUSION Gastropod species with more elongate shells also withdraw more deeply into their shells and thus, for the purpose of interspecific comparison, shell elongation is a suitable proxy for withdrawal depth. However, this same relationship does not necessarily apply when comparing individuals of a species, probably because of low intraspecific variation in shell shape. This latter finding presents problems for the hypothesis that, within species, selection for deeper withdrawal of tissues drives the evolution of more elongate shells, showing that a better understanding of the costs and benefits associated with variability in these traits is needed. Previous experimental work suggests that deeper withdrawal enhances survivorship in the face of shell-entering predators (Edgell et al., 2008), and more globose shells enhance survivorship against shell-crushing predators (Seeley, 1986; Edgell & Neufeld, 2008); therefore, a functional trade-off between elongate (deep retractors) and globose shells presents a challenge for malacologists interested in how predation shapes the diversity of gastropod shell form. Future efforts should consider the ecology of both shell-entry and shell-crushing predation to achieve this goal.
ACKNOWLEDGEMENTS Special thanks to A.R. Palmer for funding and helpful discussion, and to E.G. Boulding and two anonymous reviewers for constructive criticism. TM thanks J. and K. Miyashita, K. Andressen, C. Bates (and students), B. Cameron, M. Bein, C. Deland, T. Eastham, E. Grebeldinger, C. Neufeld, L. Hammond,A. Saunders, and D. Wong for logistical support. Authors contributed equally. Figures 1 and 2 by TM. Funded by a Natural Sciences and Engineering Research Council Discovery grant (A7245) to A.R. Palmer.
REFERENCES APPLETON, R.D. & PALMER, A.R. 1988. Water-borne stimuli released by predatory crabs and damaged prey induce more predator-resistant shells in a marine gastropod. Proceedings of the National Academy of Sciences of the USA, 85: 4387– 4391. BAUER, V. 1913. Notizen aus einem biologischen laboratorium am Mittelmeer. International Review of Hydrobiology and Hydrogrpha, 6: 31–37. BENJAMINI, Y. & HOCHBERG, Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, Series B, 57: 289–300. BERTNESS, M.D. & CUNNINGHAM, C. 1981. Crab shell-crushing predation and gastropod architectural defense. Journal of Experimental Marine Biology and Ecology, 50: 213–230. BOOKSTEIN, F.L. 1989. Size and shape: a comment on semantics. Systematic Zoology, 38: 173– 180.
239
T. C. EDGELL AND T. MIYASHITA VERMEIJ, G.J. 1982. Phenotypic evolution in a poorly dispersing snail after arrival of a predator. Nature, 299: 349–350. VERMEIJ, G.J. 1987. Evolution and Escalation: An Ecological History of Life. Princeton University Press, NJ, USA. ZIPSER, E & VERMEIJ, G.J. 1978. Crushing behavior of tropical and temperate crabs. Journal of Experimental Marine Biology and Ecology, 31: 155–172.
SCHINDEL, D.E., VERMEIJ, G.J. & ZIPSER, E. 1982. Frequencies of repaired shell fractures among the Pennsylvanian gastropods of North-central Texas. Journal of Paleontology, 56: 729–740. TRUSSELL, G.C. & SMITH, L.D. 2000. Induced defenses in response to an invading crab predator: an explanation of historical and geographic phenotypic change. Proceedings of the National Academy of Sciences of the USA, 97: 2123– 2127.
240
