Northeastern Naturalist Vol. 24, No. 3 H.N. Adams IV and A.S. Freeman 2017 289 2017 NORTHEASTERN NATURALIST 24(3):289–299 Local Variation in Egg-capsule Size in New England Populations of Nucella lapillus (Atlantic Dogwhelk) Halvor N. Adams IV1 and Aaren S. Freeman1,* Abstract - Nucella lapillus (Atlantic Dogwhelk) deposits egg capsules on solid, intertidal substrates across the North Atlantic. This study investigated whether regional geographic variation or local wave-exposure affect the size of Dogwhelk egg capsules. Over 3 years, we evaluated whether Dogwhelks from wave-exposed and wave-protected sites in Massachusetts and mid-coast Maine differed in their egg-capsule size. Our results indicate that egg capsules collected from wave-exposed sites in Maine were smaller than egg capsules from wave-protected sites in Maine, but the size of egg capsules from Massachusetts did not vary with wave-exposure. These patterns in egg-capsule size coincide with Dogwhelk size from the same sites. Despite the positive correlation between the sizes of adult Dogwhelks and the egg capsules collected, wave-protected Dogwhelks from Massachusetts showed plasticity in the size of egg capsules produced but those from Maine did not. The Massachusetts Dogwhelk’s greater plasticity in egg-capsule size highlights important local variation in control of reproductive investment and may accommodate fluctuations in desiccation stress and future climate change. Introduction An organism’s reproductive investment may be constrained by abiotic and biotic factors across its geographic range (Kokita 2004, Lardies and Castilla 2001). Generally, organisms must balance energetic allocations with survival and reproduction (Bayne et al. 1983, Clarke 1987, Monaco et al. 2010, Tinkle and Hadley 1975). In this study, we explored local and regional variation in egg-capsule size in the marine snail Nucella lapillus (L.) (Atlantic Dogwhelk, or Dogwhelk). The Dogwhelk is an intermediate consumer found on a range of wave-exposed and wave-protected rocky intertidal shores from New York and north, across Greenland/ Iceland, to northern Europe (Crothers 1985, Day et al. 1993, Etter 1989). Dogwhelks are oviparous and deposit multiple eggs between March and June in protective vase-shaped egg capsules (~7 mm x 3–4 mm) attached to sheltered refuges in the intertidal zone (Crothers 1985, Feare 1971, Fretter and Graham 1994, Pechenik 1983). Over 1000 egg capsules can be massed together, depending on abiotic conditions and the female’s size and nutritional state (Lloyd and Gosselin 2007); egg-capsule clustering lowers the rate of predation on individual egg capsules (Crothers 1985, Rawlings 1990). Heterogeneity in wave action has local effects on the population structure of Nucella spp. Whelks found on wave-protected shores tend to have thicker shells (reflecting the need for protection from shell-breaking predation); a higher 1Adelphi University, 1 South Avenue, Garden City, NY 11530. *Corresponding author - afreeman@adelphi.edu. Manuscript Editor: Melisa Wong Northeastern Naturalist 290 H.N. Adams IV and A.S. Freeman 2017 Vol. 24, No. 3 proportion of adults; lower pedal-surface area; lower tenacity; faster growth; and lower production of egg capsules, which contain fewer eggs per female than those found on wave-exposed shores (Boulding et al. 1999; Crothers 1985; Etter 1987, 1989, 1996; Freeman and Hamer 2009; Hughes and Taylor 1997). Several factors related to wave-exposure may influence reproductive investment by Nucella spp., including desiccation, predation, and hatchling mortality (Bayne 1968, Etter 1989, Pardo and Johnson 2006). The Dogwhelk demonstrates plasticity in egg-capsule deposition. Dogwhelks from wave-exposed shores may offset for high hatchling mortality by depositing twice as many capsules, with twice as many hatchlings per capsule, but with much smaller hatchlings (relative to conspecifics from wave-protected shores; Etter 1989). Wave-protected Dogwhelks tend to lay larger capsules than wave-exposed dogwhelks, with more embryos per egg capsule that benefit from the increased reproductive investment by rapidly attaining a size refuge (Etter 1989, 1989; H.N. Adams, pers. observ.). The latter strategy illustrates a trend among marine invertebrates in which juveniles with a large initial body size are more likely to survive environmental stress than small individuals (Gosselin and Rehak 2007). If this wave-exposed versus wave-protected plasticity is similar across latitudinal gradients then it may be a response to similar selection pressures, and the Dogwhelk may respond similarly to anthropogenic disturbances. Although the influence of wave action on Nucella spp.’s ecological interactions has been demonstrated on local scales (Crothers 1985; Etter 1989, 1996; Freeman and Hamer 2009; Gosselin and Rehak 2007) and across geographic regions (Freeman et al. 2014, Large and Smee 2013, Matassa and Trussell 2015), the influence of wave exposure on the Dogwhelk’s reproduction across geographic regions has not been explored. Owing to limited intergenerational dispersal, Dogwhelks may be physiologically, morphologically, and behaviorally adapted to local or regional intertidal conditions, wave exposure, desiccation, and thermal stress (Menge and Sutherland 1987, Pardo and Johnson 2006). On local scales, Dogwhelks respond to wave action through phenotypic plasticity or local adaptation of reproductive investment (Etter 1989, 1996). The purpose of our research was to investigate the influence of wave-action gradients nested within latitudinal gradients on the reproductive investment of Dogwhelks. In this investigation, we sought to determine if Dogwhelks collected from wave-exposed and wave-protected sites in Massachusetts and mid-coast Maine produced different-sized egg capsules. If large egg capsules mitigate desiccation stress and provide the greatest advantage at wave-protected (more desiccated) sites (Bayne 1968), we might expect a greater disparity between waveexposed and wave-protected egg capsules near the southern end of the Dogwhelk’s distribution, where heat stress is more intense (Bertness et al. 1999). In addition, egg-capsule production may be labile and respond to abiotic conditions if selection pressure does not strongly canalize the trait (Via 1993). If egg-capsule size is not plastic, we would expect Dogwhelks from both regions and wave-exposures to produce similar-sized capsules in situ and in the laboratory. Northeastern Naturalist Vol. 24, No. 3 H.N. Adams IV and A.S. Freeman 2017 291 Methods Field-site description and collection During 2012, 2013, and 2014 we collected Dogwhelks and their egg capsules at similar times of the year (between 24 June and 14 July) from 2 sites in Massachusetts (Cape Cod Canal and Manomet) and 3 sites in Maine (Georgetown, Kresge, and Chamberlain) (Fig. 1). We selected sites to allow for collection from both wave-exposed and wave-protected rocky intertidal shores at each site. In order to sample Dogwhelks and egg capsules, we placed a 15-m transect tape in the midintertidal zone parallel to the shoreline. We randomly selected 10 points along the transect line and searched the area closest to the random point until we discovered Dogwhelk egg capsules, usually within 0.5 m to 1 m of the point. We centered a 0.25-m2 quadrat on the egg capsules and counted, collected, and placed in meshsided containers for later morphological measurements any Dogwhelks in the quadrat. We carefully cut the egg capsules from the substrate and placed them in labeled vials filled with 95% ethanol for transport back to the lab. In 2014, in addition to collecting egg capsules, we transported adult Dogwhelks to the Darling Marine Center (DMC), in Walpole, ME, and placed them in a flowing-seawater table. The adult Dogwhelks were kept in fully submerged metal cages with barnacle-covered rocks and monitored daily until they deposited egg capsules on the rocks. Our intention was to determine if Dogwhelks responded plastically to wave exposure by Figure 1. Map of New England showing sites where we collected Dogwhelk adults and egg capsules. See text for details. Collections took place on the following dates: 14 July 2013 and 8 July 2014 at Cape Cod Canal, 13 July 2013 and 8 July 2014 at Manomet, 26 June 2012 and 1 July 2014 at Georgetown, 24 June 2012 and 2 July 2014 at Kresge, and 25 June 2012 and 3 July 2014 at Chamberlain. Northeastern Naturalist 292 H.N. Adams IV and A.S. Freeman 2017 Vol. 24, No. 3 removing them from all wave action and measuring egg-capsule deposition. However, because this was a “common garden” experiment, we could not also match the thermal conditions at each site of origin. We assumed that because Dogwhelks are an intertidal species that experiences wide daily changes in temperature, thermal conditions during the summer at DMC would not inhibit reproduction or affect egg-capsule deposition. We removed newly deposited egg capsules and placed them in labeled vials filled with 95% ethanol for later morphological measurements. Dogwhelks from wave-exposed shores of the following sites did not deposit egg capsules in the laboratory: Cape Cod Canal, Manomet, and Chamberlain. Preparation and photography In 2012, 2013, and 2014, we randomly selected 3 undamaged, field-collected Dogwhelk egg capsules from each quadrat (10 quadrats per site) for measurement of “field” egg-capsule size. In 2014, we selected for measurement of “laboratory” egg-capsule size the first 5 undamaged Dogwhelk egg capsules deposited in the lab from each site. All egg-capsule measurements were conducted as follows: we placed the intact egg capsules in a petri dish on a metric ruler under a Zeiss Stemi 2000-C dissecting microscope and photographed them at ~5x magnification using a Jenoptik ProgRes Speed XT core 3 camera and Jenoptik ProgRes CapturePro 2.8.5 image capture program (Jenoptik Company, Bethesda, MD). We employed ImageJ software to analyze the Dogwhelk egg-capsule photographs and to measure their length (from the capsule-stalk junction to the edge of the capsule plug) and maximum width (perpendicular to the length-axis) (Etter 1989). Statistical analysis We calculated from the length and width measurements the volume of each egg capsule collected in 2012, 2013, and 2014 using the formula: V = (4/3) (π) (ab2), where a and b are the egg-capsule length x 0.5 and width x 0.5, respectively (Pechenik 1983). We analyzed egg-capsule volumes and individual Dogwhelk shell lengths (collected from 2012, 2013, and 2014; square-root transformed) using two-way ANOVAs with region and wave exposure treated as fixed factors, and year, quadrat x site x region, and site x region as random factors. We employed post-hoc Tukey’s tests to compare volumes or lengths within region and within wave-exposure type for ANOVAs with significant interactions. Although we compared egg-capsule volumes using square-root transformed values, we produced our graphs from identical ANOVA models of untransformed values. In order to determine if egg-capsule volume was determined by local variation in Dogwhelk size, we performed a linear regression of shell length against squareroot transformed egg-capsule volume (both were average values from each quadrat). In order to determine if egg capsule volume was a canalyzed response that persisted after we removed Dogwhelks from their habitat, we compared the volumes of egg capsules deposited in the lab in 2014 to those collected from the field in 2014. Dogwhelks from wave-exposed sites in Massachusetts did Northeastern Naturalist Vol. 24, No. 3 H.N. Adams IV and A.S. Freeman 2017 293 not lay eggs in the lab; thus, it was necessary to perform 2 separate ANOVAs to determine the influences of region and wave exposure on egg-capsule volume (square-root transformed). The first ANOVA included only wave-protected sites and determined if regional Dogwhelk populations differed in plasticity of their egg-capsule volume. In this ANOVA, region (ME or MA) and field/lab were fixed factors, and we considered quadrat x site x region and site x region as random factors. A second ANOVA included only Maine sites and determined if egg-capsule volume was affected by wave exposure, where eggs were deposited (field or lab), or an interaction of these factors. The second 2-way ANOVA included wave exposure and field/lab as fixed factors, and quadrat x site as a random factor. The comparisons of interest in the latter analyses were the 2 comparisons between lab- and field-deposited egg capsules (within region or wave exposure); thus, we set a critical P-value of 0.025 in post-hoc comparisons (Sokal and Rholf 1995). All statistical analyses were conduced using JMP 12.0. For random, nested effects JMP estimates the denominator mean squares and the degrees of freedom using the Satterthwaite’s method, resulting in fractional degrees of freedom.. Results Dogwhelk egg capsules from wave-exposed sites in Maine had a smaller volume than egg capsules from wave-protected sites in Maine. However, egg capsules from wave-exposed and wave-protected sites in Massachusetts, egg capsules from waveprotected sites in Maine and Massachusetts, and egg capsules from wave-exposed sites in Maine and Massachusetts did not differ in volume (Table 1, Fig. 2A). Size distributions of adults followed similar patterns to egg capsules. Dogwhelks from wave-exposed and wave-protected sites in Maine were smaller than those from respective sites in Massachusetts, and Dogwhelks from wave-exposed sites in Maine were smaller than those from wave-protected sites in Maine, but wave-exposed and wave-protected Dogwhelks from Massachusetts did not differ (Table 1, Fig. 2B). The similar patterns of egg-capsule deposition and adult size belie the positive relationship between Dogwhelk size (averaged within quadrats) and the size of egg capsules (square-root transformed) (n = 206, square-root transformed egg-case Table 1. Two-way ANOVA of egg-capsule volume and shell length of Dogwhelks collected from Maine and Massachusetts (region). In addition to the fixed factors shown in the tables—year, quadrat x site x region, and site x region were included as random factors but are not shown. Source df F-ratio P-value Dogwhelk egg-capsule volume Region 1, 3.225 1.185 0.3509 Wave exposure 1, 163.9 10.522 0.0014 Region x Wave exposure 1, 163.9 16.520 less than 0.0001 Dogwhelk shell length Region 1, 3.069 14.364 0.0310 Wave exposure 1, 109.2 63.243 less than 0.0001 Region x wave exposure 1, 109.2 40.348 less than 0.0001 Northeastern Naturalist 294 H.N. Adams IV and A.S. Freeman 2017 Vol. 24, No. 3 volume = [0.0976 + 0.0025] [average Dogwhelk length]; R2 = 0.3165, P < 0.0001). Although this relationship is highly significant, it explains ju st 31.7% of the variation affecting egg-capsule size, suggesting that other factors may also be important in determining egg-capsule size. When we compared the sizes of egg capsules deposited in the lab to those deposited in the field in 2014, we f ound that Dogwhelks from Massachusetts deposited smaller egg capsules in the lab than in the field, while Dogwhelks from Maine deposited similar-sized egg capsules in the lab and field (Table 2, Fig. 3A). Dogwhelks from wave-protected sites in Maine deposited larger egg capsules than those from wave-exposed sites in Maine, and this pattern was not altered when egg capsules were deposited in the lab (i.e., there was no effect of field/lab; Table 2, Fig. 3B). In the 2014 samples, Dogwhelks from Massachusetts were larger than those from Maine (ANOVA region: F1,54 = 8.2949, P = 0.0057), and although there was a difference in the volume of egg capsules deposited in the lab versus the field (above), there was no difference in size between Dogwhelks Figure 2. (A) Volume of Dogwhelk egg mass collected from sites in Massachusetts and Maine. (B) Shell length of Dogwhelks collected from quadrats where we collected egg capsules for volume determinations. Letters represent results of Tukey HSD tests; bars with shared letters are not significantly different. Error bars indicate ± \1 SE. Table 2. Two-way ANOVAs of volumes of Dogwhelk egg capsules collected from field sites and those deposited in a lab setting by whelks collected from the various field sites. The between-region ANOVA (Maine and Massachussetss) includes quadrat x site x region and site x region as random variables. The within-region ANOVA (Maine) includes quadrat x site as a random variable. Random variables are not shown in the REML results below. Whelks deposited eggs in the lab only in 2014; thus, only data from field or lab capsules from 2014 were used in these ana lyses. Source df F-ratio P-value Egg capsules from wave-protected sites in Maine and Massachusetts Region 1, 3.015 3.657 0.1513 Field/lab 1, 37.57 7.508 0.0093 Region x field/lab 1, 37.57 7.394 0.0098 Egg capsules from sites in Maine Field/lab 1, 46.13 0.807 0.3737 Wave exposure 1, 50.15 7.735 0.0076 Field/lab x wave exposure 1, 46.13 1.357 0.2501 Northeastern Naturalist Vol. 24, No. 3 H.N. Adams IV and A.S. Freeman 2017 295 depositing capsules in the field versus those depositing egg capsules in the lab (all P > 0.14; data not shown), indicating that size differences in Dogwhelks does not explain the size differences in deposited egg capsules. Discussion In this study, we found that the size and plasticity in Dogwhelk egg-capsule deposition varied across and within regions in New England. Variation in wave exposure likely influenced the difference in egg-capsule volume between Massachusetts and Maine; wave-exposed capsules from Maine were smaller than wave-protected capsules from Maine. The tendency for large Dogwhelks to produce large egg capsules is noteworthy (Crothers 1985); however, it does not explain the plasticity in egg-capsule sizes we observed. Although wave-protected Dogwhelks from Maine did not alter the volume of their egg capsules in response to environmental conditions (i.e., being moved to a lab), wave-protected Dogwhelks from Massachusetts deposited smaller egg capsules in lab than in the field. Several factors may influence these egg-capsule deposition patterns, including differences in abiotic factors between sites and regions, predation, and differing levels of plasticity (or canalization) in control of egg-capsule deposition. The patterns of egg-capsule size from our Massachusetts sites were very similar to those observed by Etter (1989). Egg capsules collected from a wave-protected shore in Nahant, MA, were the same size as those collected from an exposed shore, but Dogwhelks taken from the wave-protected shore deposited smaller capsules in the laboratory than those from the wave-exposed site (Etter 1989). Whelk egg capsules reduce the lethal threat of desiccation and low-salinity stress (Moran and Emlet 2001, Pechenik et al. 1984), and Dogwhelks in southern New England likely require larger egg capsules to buffer the desiccation stress associated with higher temperatures (Bayne 1968, Bertness et al. 1999). Snails in wave-exposed environments in Maine are buffered from temperature increases and desiccation Figure 3. (A) Volume of field-collected egg capsules (from wave-protected sites in Maine) or laboratory-deposited egg capsules (deposited by Dogwhelks collected from wave-protected sites). Massachusetts Field > Massachusetts Laboratory (P = 0.0027). (B) Volume of egg capsules collected from wave-protected sites and those laid in the lab by Dogwhelks collected from respective sites in 2014. No wave-exposed whelks from Massachusetts laid eggs in the lab. Error bars indicate ± 1 SE. Northeastern Naturalist 296 H.N. Adams IV and A.S. Freeman 2017 Vol. 24, No. 3 by consistent splashing from wave action (Etter 1989, Freeman and Hamer 2009, Large and Smee 2013). The differences in wave action between our wave-exposed and wave-protected sites in Massachusetts were substantially less than the differences between our wave-exposed and wave-protected sites in Maine; however, the sites in Nahant used by Etter (1989) had strong contrasts in wave exposure. Although not documented here, it is possible that higher wave intensity at waveexposed sites in Maine may have removed the large egg capsules, resulting in generally larger egg capsules at wave-protected sites in Maine (Fig. 2A). Furthermore, while egg capsules from wave-protected sites in Maine were larger than those from wave-exposed sites (Fig 2A), wave-exposed whelks did not compensate by producing more egg capsules; rather, we found more egg capsules per Dogwhelk at wave-protected sites than at wave-exposed sites (3.5 ± 0.2 SE and 2.3 ± 0.3 SE, respectively; H.N. Adams IV and A.S. Freeman, unpubl. data). Dogwhelks from areas with a lower magnitude difference between wave-exposed and wave-protected sites may experience less-reliable relief from desiccation stress. The pattern of Massachusetts Dogwhelks exhibiting greater plasticity in capsule size is consistent with the Dogwhelks producing larger egg capsules to mitigate the impact of desiccation; the lab-deposited egg capsules were continuously submerged in a sea table and were not threatened with desiccation. If viewed as an adaptation to variable stresses (Via 1993), the Massachusetts populations may possess greater plasticity due to greater variability in desiccation or predation than northern conspecifi cs. Abiotic and seasonality differences between Maine and Massachusetts may also affect the Dogwhelk’s phenology and parental investment. Dogwhelks at southern sites may begin depositing egg capsules earlier in the season, and the egg capsules we collected in Massachusetts may have been older than those from Maine. However, our observations are still valid because egg-capsule volume is established when adult females deposit egg capsules and does not change once the conchiolin sheath hardens (Crothers 1985). Both predation and desiccation follow similar patterns and are expected to be more intense at low-flow, wave-protected sites (Leonard et al. 1998, Menge 1978) and at lower latitudes than at higher latitudes (Bertness et al. 1999). While physical characteristics like spire length and egg-capsule thickness promote resistance to predation (Rawlings 1994, Schwab and Allen 2014), it is not clear if large egg capsules offset mortality due to more intense predation (Monaco et al. 2010, Rawlings 1990). Finally, although Dogwhelks from Massachusetts generally produced fewer egg capsules, wave-exposed whelks from Massachusetts did not deposit egg capsules in the lab. Dogwhelks from Massachusetts were placed in sea tables under conditions more similar to the Maine sites and, thus, may have been more stressed than conspecifics from Maine. Stress may have affected the whelk’s ability to deposit egg capsules or the size of egg capsules they deposited. These factors are confounded and their influence on egg-capsule size is not clear. Further work is needed to determine if regional or local (wave-exposed/protected) differences in predation, seasonality, or desiccation correlate with our observed egg-capsule patterns. The Dogwhelk’s reproduction and development is influenced by temperature, wave action, and other abiotic factors (Boulding et al. 1999; Crothers 1985; Etter Northeastern Naturalist Vol. 24, No. 3 H.N. Adams IV and A.S. Freeman 2017 297 1989, 1996; Freeman and Hamer 2009; Hughes and Taylor 1997). Both processes will likely be impacted by global climate change, sea temperature increases, and future alteration of storm intensity, or range-shift of prey populations (Harley 2011, O’Connor 2009). Our biogeographic comparison suggests that some Dogwhelk populations possess lability in egg-capsule deposition (Massachusetts populations can alter egg-capsule size, but Maine populations do not). Such lability may be locally or regionally adapted to abiotic factors such as wave exposure and desiccation, and may allow some populations to accommodate future climate change. Acknowledgments We thank E. Dernbach and H. Louima for assistance collecting Dogwhelks, S. Grace, J. Factor, S. Corman, J. Lord, R. Whitlatch, and R. Osman for assistance identifying possible Dogwhelk collection sites, and T. Miller, L. Healy, R. Downs, and other personnel at the Darling Marine Center for logistical support. Financial support came from the Biology Department at Adelphi University, Horace G. McDonell, and the McDonell Research Fellowship, and the Benjamin Cummins/MACUB Research Grant. Literature Cited Bayne, C.J. 1968. A study of the desiccation of egg capsules of eight gastropod species. Journal of Zoology 155:401–411. Bertness, M.D, G.H. Leonard, J.M. Levine, and J.F. Bruno. 1999. Climate-driven interactions among rocky intertidal organisms caught between a rock and a hot place. Oecologia 120:446–450. Boulding, E.G., M. Holst, and V. Pilon. 1999. Changes in selection on gastropod shell size and thickness with wave-exposure on northeastern Ppacific shores. Journal of Experimental Marine Biology and Ecology 232:217–239. Clarke, A. 1987. Temperature, latitude, and reproductive effort. Marine Ecology Progress Series 38:89–99. Crothers, J.H. 1985. Dog-whelks: An introduction to the biology of Nucella lapillus (L.). Field Studies 6:291–360. Day, A.J., H.P. Leinaas, and M. Anstensrud. 1993. Allozyme differentiation of populations of the Ddogwhelk Nucella lapillus, (L.): The relative effects of geographic distance and variation in chromosome number. Biological Journal of the Linnean Society 51:257–277. Etter. R.J.. 1989. Life- history variation in the intertidal snail Nucella lapillus across a wave-exposure gradient. Ecology 70:1857–1876. Etter, R.J. 1996. The effect of wave action, prey type, and foraging time on growth of the predatory snail Nucella lapillus (L.). Journal of Experimental Marine Biology and Ecology 196:341–356. Feare, C.J. 1971. The adaptive significance of aggregation behaviour in the Ddogwhelk, Nucella lapillus (L.). Oecologia 7:117–126. Freeman, A.S., and C.E. Hamer. 2009. The persistent effect of wave exposure on TMIIs and crab predation in Nucella lapillus. Journal of Experimental Marine Biology and Ecology 372:58–63. Freeman, A.S., E. Dernbach, C. Marcos, and E. Koob. 2014. Biogeographic contrast of Nucella lapillus responses to Carcinus maenas. Journal of Experimental Marine Biology and Ecology 452:1–8. Northeastern Naturalist 298 H.N. Adams IV and A.S. Freeman 2017 Vol. 24, No. 3 Fretter, V., and A. Graham. 1994. British Prosobranch Molluscs: Their Functional Anatomy and Ecology. Vol 161. The Ray Society, London, UK. 820 pp. Gosselin, L.A., and R. Rehak. 2007. Initial juvenile size and environmental severity: Influence of predation and wave exposure on hatching size in Nucella ostrina. Marine Ecology Progress Series 339:143–155. Harley, C.D.G. 2011. Climate change, keystone predation, and biodiversity loss. Science 334:1124–1127. Hughes, R.N., and M.J. Taylor. 1997. Genotype–environment interaction expressed in the foraging behavior of Dogwhelks, Nucella lapillus (L.), under simulated environmental hazard. Proceedings of the Royal Society B: Biological Sciences 264:417–422. Kokita, T. 2004. Latitudinal compensation in female reproductive rate of a geographically widespread reef fish. Environmental Biology of Fishes. 71:213–22 4. Lardies, M.A., and J.C. Castilla. 2001. Latitudinal variation in the reproductive biology of the commensal crab Pinnaxodes chilensis (Decapoda: Pinnotheridae) along the Chilean coast. Marine Biology 139:1125–1133. Large, S.I., and D.L. Smee. 2013. Biogeographic variation in behavioral and morphological responses to predation risk. Oecologia 171:961–969 Leonard, G.H., J.M. Levine, P.R. Schmidt, and M.D. Bertness. 1998. Flow-driven variation in intertidal community structure in a Maine estuary. Ecology 79:1395–1411. Lloyd, M.J., and L.A. Gosselin. 2007. Role of maternal provisioning in controlling interpopulation variation in hatching size in the marine snail Nucella ostrina. Biological Bulletin 213: , 316–324. Matassa, C.M., and G.C. Trussell. 20154. Effects of predation risk across a latitudinal temperature gradient. Oecologia 177:775–784. Menge, B.A. 1978. Predation intensity in a rocky inter-tidal community: Relation between predator foraging activity and environmental harshness. Oecologia 34:1–16. Menge, B.A., and J.P. Sutherland. 1987. Community regulation: Variation in disturbance, completion, and predation in relation to environmental stress and recruitment. American Naturalist 130:730–775. Monaco, C.J., K.B. Brokordt, and C.F. Gaymer. 2010. Latitudinal thermal-gradient effect on the cost of living of the intertidal Porcelain Ccrab, Petrolisthes granulosus. Aquatic Biology 9:23–33. Moran, A.L., and R.B. Emlet. 2001. Offspring size and performance in variable environments: Ffield studies on a marine snail. Ecology 82:1597–1612. O’Connor, M.I. 2009. Warming strengthens an herbivore–plant interaction. Ecology 90:388–398. Pardo, L.M., and L.E. Johnson. 2006. Influence of water motion and reproductive attributes on movement and shelter use in the marine snail Littorina saxatilis. Marine Ecology Progress Series 315:177–186. Pechenik, J.A. 1983. Egg capsules of Nucella lapillus (L.) protect against low-salinity stress. Journal of Experimental Marine Biology and Ecology 71:165–179. Pechenik, J.A., S.C. Chang, and A. Lord. 1984. Encapsulated development of the marine prosobranch gastropod Nucella lapillus. Marine Biology 78:223–239. Rawlings, T.A. 1990. Associations between egg-capsule morphology and predation among populations of the marine gastropod Nucella emarginata. Biological Bulletin 179:312–325. Rawlings, T.A. 1994. Encapsulation of eggs by marine gastropods: Effect of variation in capsule form on the vulnerability of embryos to predation. Evolution 48:1301–1313. Northeastern Naturalist Vol. 24, No. 3 H.N. Adams IV and A.S. Freeman 2017 299 Schwab D.B., and J.D. Allen. 2014. Size-specific maternal effects in response to predator cues in an intertidal snail. Marine Ecology Progress Series 499:127–141. Sokal, R.R., and F.J. Rohlf. 1995. Biometery: The Principles and Practice of Statistics in Biological Research. Freeman and Company, New York, NY. 887 pp. Tinkle, D.W., and N.F. Hadley. 1975. Lizard reproductive effort: Caloric estimates and comments on its evolution. Ecology 56:427–434. Via, S. 1993. Adaptive phenotypic plasticity: Target or by-product of selection in a variable environment? American Naturalist 142:352–365.