WISCU-R-02-013 C2

Shelldamage in salt marshperiwinkles Littorariairrorata [Say,1S22]! and resistanceto future attacksby blue crabs Calli nectessapidus I Rathbun, 1S96]!

Ben K. Greenfield*,David B. Lewis, and JeffersonT. Hinke CenterFor Limnology, University of Wisconsin,680 North Park Street, Madison, Wisconsin 53706, U. S.A,

Ahtstraet:Unsuccessful predation bythe blue crab [Rathbuu, 1896]! on periwinkle snails Liitoraria irroram [Say, 18221!could result in shelldamage aud the subsequent development of a visibleshell scar, We experimentally determined whether scarred L. irroratuare moreor lessresistant to bluecrab predation than unscarred individuals. We simultaneouslypresented equal numbers of similar-sizedscarred aud unscarred snailsto individualblue crabs aud recorded the number of eachtype of snailconsumed. We alsocompared shell attributes of scarredaud unscarred snails fromtwo marsh sites on Sapelo Island, Georga, U. S.A. Crabsconsumed significantly more unscarred than scarred snails, suggesting that unscarred snails are more easily accessed.This pattern was more pronouncedwhen the snailswere close to the maximumedible size. Measurementsindicated thai the shells of scarredsnails had significantly thicker lips than those of unscarredsnails, These results demonstrate thatshell scars correlate with greater predation resis- ence in L. irrorata.

Key WOrds:predation, Lirmrariu, Callinectes, shell repair, salt marsh

Animals have evolved a variety of defensivernor- Turner et al., 1999!. Morphological adaptations that phological traits that confound the capture and handling increasehandling time may ultimatelyreduce predation efforts of their predators.Morphological adaptationscan risk. In environments with high predation risk, natural derive from natural selection for a particular structure or selection has resulted in some snail developing trait, or from plastic morphologicalresponses to encounters thick shells, narrow apertures,and reduced spires. These with risk Verrneijet a/., 1981;Dodson, 1989!. Although traits increasehandling difficulty for crushing predators not extensive, most research on plastic morphological such as crabs Vermeij and Covich, 1978; Paltner, 1979; responsesfocuses on how organismsadapt after sensing Bertness and Cunningham, 1981!. At time scales much chemical cues that signal the presence of a predator shorterthan that of natural selection,individual snails may Appleton and Palmer, 1988; Dodson et al., 1994; Lewis develop stronger shells in response to chemical cues and Magnuson, 1999; Trussell and Smith, 2000!. Iri this releasedby the feeding activities of decapods Appleton paper,we examineanother mechanism by which the mor- and Palmer, 1988;Trussell and Smith, 2000!, althoughthis phology of prey might respondto predationrisk. We inves- processis not universal Lewis andMagnuson, 1999!. tigate whether prey morphology is distinct betweenprey For marsh periwinkles irrorata [Say, thathave had injurious, nonlethal encounters with a preda- 1822]!, behavioral adaptationsreduce predator encounter tor versusprey that havenot beenpreviously injured. In the rates Hamilton, 1976; Warren, 1985; Dix and Hamilton, caseof repair following an injury, the defensivecapacity of 1993!. Morphological antipredatoryadaptations, however, any damagedstructures may be compromisedor improved. have not been demonstratedfor L irrorata. For example, Snails display a wide range of behavioral and mor- Blundon and Vermeij 983! comparedthe shell strengthof phologicalantipredatory adaptations Appleton and Palmer, L. irrorata that had survivedprevious attempts at predation 1988; Covich et al., 1994; Lewis and Magnuson, 1999; by blue crabs Callinectes saptdus [Rathbun, 1896]!, as indicatedby scarson the shell Vermeij, 1978!, with snails *Current address:Sau Francisco Estuary Institute, 7770 PardeeLane, Oakland,California 94621,U. S. A., [email protected] lacking any indication of ever encountering a predator, ¹Curreut address: Center for Environmental Studies, Arizona State Pressingthe ultimate body whorl with an Instron testing University, 907 South Mill Avenue, Suite 907, Tempe, Arizona 85287, device, they found no difference in shell strengthbetween U. S. A. the two classes of snail, Crabs employ many forms of

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141 142 AMER. MALAC, BULL. 17/2! 002!

attack when foraging on snails Hamilton, 1976; Bertness crabs more readily consumed scmed or unscarred snails. and Cunningham,1981; Vermeij, 1982a!.For example,C. We collected all experitnental Littoraria irrorata from a sapidus prey on relatively large snails by progressively 180 mz region of Dean Creek Marsh, SapeloIsland, chipping away at the aperturelip, ratherthan applying force Georgia,USA. We measuredsnail shell length to the near- to the ultimate body whorl Schindler et al., 1994!. We est rnillirneter with calipers, and examined snails for the investigatehere whether the presenceof a scar correlates presence of a scar a jagged line associated with a visible with snail vulnerability to crab predation. indentationin the shell!,The snails used in feedingexperi- Predation pressure by crabs on snails and injury ments ranged in size from 14 to 22 tnm. We collected crabs rates of snails are greater at lower elevation sites within a from South End Creek Marsh and from the coastal beach given marsh Schindler et al1994!, and this difference southeastof DeanCreek. We transferredcrabs to a large may have consequencesfor shell rnorphometry. Larger flow-through holding tank and conditioned them to the lab- crabs,which have higher predation success rates for a given oratory environmentfor at least 48 hr, during which time sized snail, may occur at lower elevation marshes they were not fed. After the acclimationperiod, individual Schindler er a/1994!. To evaluatethe general effect of crabs were transferred to separate flow-through glass scarring on morphometryacross disparate sites, we exam- aquaria. ined the effect of scar presenceon rnorphometryat both a We conducted33 feedingexperiments using 13 low and a high elevation site. To evaluate the effect of scar- crabs to 6 experimentsper crab; Table 1!. In eachexperi- ring on predation success across a range of predator ment, we simultaneouslypresented an individual crab with strengths, we examined predator successacross a wide 10 snails of equal length, 5 that had shell scars and 5 that range of crab and snail sizes. did not. We continuedan individual feedingexperiment Blue crabsdisplay size preferencesand will discard until the crab had consumed at least 3 snails or had ceased snails that are too large to handle Hamilton, 1976; feedingfor at least15 min. After completionof an experi- Schindler er al., 1994!, As the crab carapacewidth / snail ment, we recorded the number of remaining scarredand shell length ratio crab / snail size ratio! increases above unscarredsnmls. A number of experimentsusing separate 6.4, most snails I e crushedand consumedby crabs.Below crabsin separateaquaria were conducted simultaneously. this ratio i.e., when a snail is relatively large for a given We did not reusesnails for any experimentand we removed crab! there is a linear decrease in the likelihood of a shell from our analysisexperiments in which crabs did not con- being crushed Schindleret al., 1994!.We predict that if the sume any snails. presenceof a scar influencesthe vulnerability of snails to To determinewhether scarring status influenced the predation, this effect would be manifest below crab / snail numberof snailsconsumed, we ran a G-teston the pooled size ratios of 6.4. Below this ratio, subtle differences in data from the 33 experiments Sokal and Rohlf, 1995!. morphologywill havediscernable effects on vulnerability Becausecrabs were presented with 10 snailsin eachexperi- to successful attack. Above this ratio all snails would be extremelyvulnerable, independent of scarringstatus. We conducted laboratory tests and morphometric Table1. Blue crabcarapace width mm!, snail shelllength mm!, and measurementsto determinewhether the presenceof a scar total number of snails presentedto each crab. In each experiment,five in the shells of Littoraria irrorata correlates with differen- scarredand five unscarredsnails were presented.When more than one experimentwas performed at a givensize, the numberof experimentsis tial predation successby Callinecressapidtts. To test the listed in parentheses. null hypothesisthat scarring does not correlate with crab predationsuccess, we investigatedwhether blue crabscon- CarapaceWidth mm! Snail Sizes mm! Total Numberof sumed significantly more scarred or unscarred snails of Number of Experiments! SnailsPresented similar size. To determineif relative consumptionrate was 82.2 16 10 related to crab size, snail size, or crab/snail size ratio, we 86.7 14, 15, 16! 40 investigated whether differences were more apparentfor 102.2 14!, 16!, 17! 60 specific subsetsof the experimentalpopulations. Finally, 106.8 17, 18 20 we measured aperture and lip characteristics of scarred and 113.5 17, 18! 30 unscarred L. irrorara to identify differences in shell traits 118.3 19, 20 20 119.2 17!, 18! 40 between scarred and unscarred snails. 121 18,21 20 124.2 17, 18 20 METHODS 129.7 19 10 132.4 20, 21 20 Consumption comparison 133 15,20 20 134.6 We conductedan experiment to test whether blue 20, 22 20 GREENFIELD ET AL.: SHELL DAMAGE AND RESISTANCETO ATTACKS 143 ment, for the G-test we define each individual snail as an We used general linear models to determine the rela- observation,generating a total samplesize of 330 observa- tive importanceof collectionsite and scarringstatus on tions. We compared the total number of scarred and aperturelength, aperture width, aperture area, and lip thick- unscarredsnails eaten with the null hypothesisthat equal ness Draper and Smith, 1998!.These morphologicaltraits numbersof eachwould be consumed.We usedheterogene- scale with overall shell length see Results section!. ity G-teststo evaluatewhether consumption of snailsby Therefore, we first de-trended the data for the effect of individual crabsdeviated significantly from the experimen- length by fitting a linear regressionof each trait vs. shell tal crabpopulation, or whetherthe consumption of snailsby length and then taking the residuals.For each trait, these individual crabs varied among experiments Sokal and residualswere checked for nortnalityand then analyzed as a Rohlf, 1995!. functionof site,scarring status, and the sitex scarringsta- We recognizedthat scarring statusmight not affect tus interaction. crab predationsuccess for very small, easily crushedsnails. Thus, we intentionally conductedmultiple experiments RESULTS aboveand below a critical crab/ snail size ratio .4!, deter- mined experimentally by Schindler et al. 994!. We also Consumptioncomparison intentionally used a broad range of crab and snail sizes in In all experitnents combined, 165 scarred and 165 order to separately examine the effect of crab and snail size. unscarredsnails were presentedto the blue crabs.Of these, In total, we conducted15 experimentsabove and 18 experi- the crabsate 76 scarredand 98 unscarredsnails, a signifi- ments below the critical size ratio. We also examined the cant difference p < 0.025; Table 2!. When the crab or snail resultsfor statisticalsignificance when data were separately populationwas exaininedby size, crabsate more unscarred pooled by mediansnail or crab size. The median sizes 8 thanscarred snails, but the patternwas only significantfor mm for snailsand 115 mm for crabs!are sizes at whichpre- small < 18 mm! snails Table2!. No heterogeneitywas dation success by Calli'nectes sapidus on L. irrorata observedbetween individual crabs and the entireexperi- changessignificantly e.g., seetable 3 in Westand Williams mental population.Furthermore, no heterogeneitywas [1986] and fig. 9 in Schindleret aL [1994]!. found betweentrials, indicating that crab behaviorwas con- sistent among trials. Shell morphometry Crabs consumed fewer scarred snails in trials when We compared shell characteristics of 257 unscarred the crab to snail size ratio was small Fig. 1!. Individual G and 48 scmed snails collectedfrom a site with high preda- tests indicated significance for the low size ratio but not for tion risk and a site with low predationrisk, All snailswere thehigh sizeratio crabs Table2!. In trialscharacterized by coilectedin lateOctober, 1999. The site with highpredation high body size ratios i.e. relatively small snails!, predation risk, LighthouseMarsh, is locatedalong the shoreof Doboy rates were uniformly high at around60%, with only an 8% Sound,a sourceof crabsfor theseintertidal inarshes. By decrease for scarred snails, contrast, predation risk is reduced at North End Marsh, a higher elevation site located at the headwaters of Dean Shellmorphome try Creek about 3 km from Doboy Sound Schindler et al., Aperture length, aperturewidth, aperturearea, and 1994!. We captured and measured 113 unscarred snails and 27 scarredsnails from LighthouseMarsh and 144 unscarred and 21 scarred snails from North End Marsh, We measured Table 2. Consumptionpercent differences percentof unscarredsnails shell traits to the nearest0.01 mm using a dial caliper.The consumedminus the percentof scarredsnails consumed! and G-test resultsfor all trialsattd for subsetsof thesample categorized according to attributesmeasured were shell length, aperturelength, aper- snailshell length large> 18 mm> small!,crab carapace width large> turewidth, and lip thickness see axis orientations in figure 115mm> small!, and crab/ snail sizeratio, 1 of Janson and Sundberg [1983]!. Aperture length and width were the distances between the inner surfaces of the SampleType N! ConsumptionPercent G Difference aperturealong theseaxes. For lip thickness,measurements Unscarred- Scarred! were collected at least three times on separaterandom]y selectedlocations 1 nuninside the lip edgeand the inini- Alt Trials 30! 13 5,90* Large Snails60! 10 mum value was recorded, Particular traits were occasional- 1,60 Small Snails70! lg 5 37s ly, and inadvertently, not measured for a few snails, result- Large Crabs70! 13 2.87 ing in a sample size of between 297 and 305 measured Small Crabs60! 15 3.62 snailsper trait. In addition,we estimatedthe shapeof the Crab/ Snail Size Ratio < 6.4 80! 19 6.46* apertureas an ellipse, and calculatedaperture area from the Crab/ Snail Size Ratio > 6.4 50! 8 0.98 measurementsof aperturelength and width. " inthcatessignificance at ct = 0.025 144 AMER. MALAC. BULL. 17 I/2! 002!

80 following discussion,we further evaluatethese hypotheses. Our data suggestthat snails that have experienced 60 predation attetnptshave shells with an improved capacity C Q for defense.This improvementprobably lies in the increase LU in lip thickness,but does not derive from any changesin 2 40 at aperture shape. Apertures were shorter on scarred snails. In oQ Q. some cases, however, apertures were also wider. These 20 changesin apertureshape result in no net changein aper- ture area. Consequently, scarring status likely has little effect on a crab'sability to insert its chelaeinto the aperture in attempts to chip the shell. Chelae insertion is more fre- All Snails Relatively Relatively LargeSnails Small Snails quently used by crabs to access large snails Schindler er al., 1994!.Therefore, the more significantdifference in pre- Fig. 1. The percentageof all snailseaten N = 330X and the percentageof dation success between scarred and unscarred snails below relatively large N = 1 ! and relatively small N = 150! snailseaten. Thc 18 mm than above 18 mm supports the hypothesis that relatively large snailshave a crab/ snail size ratio below 6.4 and the rela- tively smansnails have a crab/ snail sizeratio above6.4. chelaeinsertion successdoes not dependon scarringstatus. Increase in the thickness of the aperture lip, howev- er, would influence a crab's ability to chip a snail shell. Our 2 lip thickness all scaledpositively with shell length R data provide evidence for the hypothesisthat thicker lips 0.87, 0.79, 0.85, and 0.67, respectively;linear regressionp endow snails with greater resistanceto predation. In the < 0.001 in all cases!. Probability plots indicated that all field, snails with scarshad thickerlips, and in our experi- four sets of residuals followed a normal distribution. After ment, snails with scars were eaten less frequently. removing the effect of shell length, we determined the Furthermore, Blundon and Vermeij 983! demonstrate that interactive effect of site high vs. Iow predation risk! and overall strengthof the shell's body whorl doesnot signifi- scarringstatus on eachof thesethree shell traits. Aperture cantly differ betweenscarred and unscarredsnails, impli- length was reduced in snails collected from I ighthouse cating a more isolated morphological mechanism, such as Marsh p < 0.001!, the site with high predation risk. and differences in lip thickness. was reduced in snails bearing a scar p = 0.039; Fig, 2A!. The increased lip thickness of scarred snails could The interactive effect of site and scarring status was not result from at least two mechanisms. First, scarred snails significant at p = 0.05. may haveinherited greater resistance, regardless of scarring There was an interactive effect of site and scarring status,as evidencedby their survival of a previouspreda- status on aperture width p = 0.017!. On scarred snails, tion attempt. In other words, the scarredpopulation repre- aperture width was increased at Lighthouse Marsh, where sents the skewed result of natural selection due to removal predation risk was allegedly higher. By contrast,the aper- of weak shelled individuals from the entire population ture width of scarred snails was reduced at the site with low Vermeij, 1982b; Johannesson and Johannesson, 1996!. predation risk, North End Marsh Fig, 2B!, Second, morphological response» may be induced by Variability in aperture area was not explained by unsuccessful attacks. A scarring event may lead to the site, scarring status, or their interaction p > 0.05; Fig. 2C!. development of antipredatory morphology in individual Finally, lip thickness was greater at the site with snails Appleton and Palmer,1988!. This hypothesisis sup- high predation risk p = 0.016!, and was greater on snails ported by the work of Trussell and Smith 000!, who hearing a scar p = 0,023; Fig. 2D!. There was no interac- demonstrate shell thickening of Lfttorina obfusata in tive effect on lip thickness. responseto predator effluent across a wide geographic range. Regardless of the mechanism, because Littoraria irrorafa exhibit a planktonic larval stage Bingham, 1972!, DISCUSSION spatial variation in lip thickness would only be maintained by adult exposure to predation gradients after settlement. The blue crabs used in this experiment ate signifi- Our data also suggest that snail shell attributes are cantly more unscarredthan scarred snails. Additionally, influenced by predation risk regardless of whether an indi- scarred snails had thicker lips and differently shaped aper- vidual snail is attacked.Snails collected from Lighthouse tures than unscarred snails. Integration of these results sug- Marsh, where predationrisk is high, had shorter apertures gests two hypotheses: first, following an attack, repair and thicker lips than snails collected from the less risky results in a shell with an improved defensive capacity; sec- North End Marsh site. Both scarred and unscarred snails ond, lip thickness is inversely related to vulnerability. In the demonstrated this pattern. Snails may have differed GREENFIELD ET AL.: SHELL DAMAGE AND RESISTANCE TO ATTACKS 145

0.1 C l0 C D

Qe 00 0.0

tt! -0.1 R -0.1tn Q 0

-0.2 -0.2 LH NE LH NE Site Site

0.3 0.10

g 0.2 t:

0.1 ~ 0.05

0.0

I! to -0.1 tn 0.00 C rg 8 D -0.2

-0.3 0.05 LH LH NE Site Site Fig. 2. Relationshipsof traitsof snailshens with site LighthouseMarsh, LH - highpredation risk; North End Marsh, NE - low predationrisk! andscarring status open bar scarred;dark bar - unscarred!.A site with highpredation risk LighthouseMarsh, LH! anda lowpredation risk site NorthEnd Marsh, NE! weresampled for scarredand unscarred snails. Shell traits include A! aperturelength numberof snails,N = 305!, B! aperturewidth N = 300!, C! aper- ture area N = 300!, and D! lip thickness N = 297!. Bars indicatethe least-squaresmeans of an ANOVA of shell trait as an interactivefunction of site and scarringstatus. Error bars = 1SE. Data are the residuals from a linearregression of shelltrait vs.shell length. between sites in these morphological traits for two reasons. Differences in the vulnerability of scarred and First, selective pressureswould be greater at Lighthouse unscarred snails were particularly evident when snails were Marsh. Second,snails may respondto chemicalcues indica- close to the maximum edible size i.e. when the crab / snail tive of risk that are releasedby crabs Trussell and Smith, size ratio was less than 6.4!. This is consistent with Elner 2000!. We only have one site apiececharacterized by high and Hughes' 978! demonstration that for crabs, the cost and low predationrisk. Thus, we submit only as a sugges- of handling prey changesmore rapidly at high prey sizes. tion that periwinkle morphologyresponds to predationrisk In the context of optimal foraging theory Pyke et al., in the absence of an actual scar-inducing encounter. 1977!, our results suggest that the difference in overall Nevertheless, natural selection for improved defensive energetic gain between scarred and unscarred snails is most capacity is a pervasive,widespread process in gastropod- pronounced at the maximum edible snail size. At this size decapodsystems e.g., Kitching andLockwood, 1974!. ratio, the subtle morphometricdifferences associated with 146 AMER. MALAC, BULL, 17/2! 002! scarring have the greatest effect. J, M, Culp. 1994. Non-visual communicationin freshwaterben- There are several possible consequencesof shell thos: an overview. Journal of the /VorthAmerican Benthological Society 13:268-282. damage for Littoraria irrorata. First, as noted above, Draper,N. R. and H. Smith. 1998,Applied RegressionAnalysis, 3rd Ed. scarred snails have thicker lips than unscarred snails. This Wiley-lnterscience,New York. 706 pp. increased lip thickness may be a barrier to efficient con- Elner, R, W, and R. N. Hughes.1978. Energy maximizationin the diet of sumptionby blue crabs.Second, snails may suffer a trade- the shore crab, Carcinus maenas. Journal nf Ecology 47:103-116. off betweenrepairing the shell and various physiological Hamilton, P. V. 1976. Predation on Littorina irrorata Molluscs: processes.For instance,the energetic cost of repair lnay ! by Callinectes sapidus Crustacea: Portunidae!. compromise reproductive output and growth. Stahl and Bulletin of Marine Science26:403-409. Lodge 990!, however, found no such trade-off in one Janson,K. and P. Sundberg.1983. Multivariate morphomehicanalysis of two varieties of Littorina saxatilis from the Swedishwest coast. freshwaterspecies, and inferred that populationgrowth was /ttarine Biology 74:49-53, not compromisedby nonlethalinjuries. Third, it is possible Johannesson,B. and K. Johannesson.1996. Population differences in that increasesin lip thicknessassociated with scarringmay behaviourand morphologyin the snail Littorina saxatilis: pheno- reducesoft tissuemass, causing a reductionin the energetic typic plasticity or genetic differentiation? Journal of Zoology 240:475-493. value of snails for crabs. Kitching, J. A. and J. Lockwood. 1974.Observations on shell form and its ecological significance in thaisid gastropods of the genus Lepsiellain New Zealand,Marine Biology 28:131-144. Lewis, D. B. and J. J. Magnuson. 1999. Intraspecific gastropod shell ACKNOWLEDGMENTS strength variation among north temperate lakes. Canudian Journal of Fisheriesand Aquatic Sciences56:1687-1695, We thank J. F. Kitchell, D. K. Padilla, T. F., Essington, A. I. Palmer,A. R. 1979.Fish predationand the evolution of gasnopodshell Pollard, T. B. Johnson,B. Foreman,and T. O*Keefefor helpful feedback sculpture: Experimental and geographic evidence. Evolution on experimental design and analysis. R. Derrig-Green and G. G. Sass 33:697-713. assistedwith field work. The commentsof C. J. Harvey, S. R. Carpenter, Pyke, G. H., H. R. Pulliam, and E, L. Chamov. 1977.Optimal foraging: A J. F. Kitchell and two anonymousreviewers improved the manuscript.R. selectivereview of theory and tests.Quarterly Reviewof Biology T. Kneib, of the University of GeorgiaMarine Institute,graciously provid- 52:137-154. ed laboratoryfacilities. This work was funded in part by the University of Schindler, D. E., B. M. Johnson,N. A. MacKay, N. Bouwes, and J. F. Wisconsin Sea Grant Institute under grants from the National Sea Grant Kitchell. 1994. Crab: snail size-structuredinteractions and salt CollegeProgram, National Oceanicand AtmosphericAdministration, U,S, marshpredation gradients. Oecologia 97;49-61. Departmentof Commerce,and 1'romthe Stateof Wisconsin.Federal grant Sokal, R. R. and F. J. Rohlf. I 995,Biometry, 3rd Ed. Freeman,New York. number NA86RG0047, project number E/E-39-SE. Additional financial 887 pp. Stahl, T, and D. M. Lodge. 1990.Effect of experimentallyinduced shen assistance was provided by U.S. EPA STAR Fellowships B. K. damage on mortality, reproduction, and growth in Helisoma Greenfield and D. B. Lewis! and the NSF IGERT program B. K. trivolvis Say, 1816!.The Ãauti /us 104:92-95, Greenfield and J. T. Hinke!, Finally, the Sapelo Island 1998 Cooking Trussett,G. C. and L. D. Smith. 2000. Induceddefenses in responseto an Committee facilitated the study of foraging strategies that efficiently invading crab predator: An explanation of historical and geo- accessestuarine invertebrates. graphic phenotypicchange. Proceedings of the /VationalAcademy of Sciences97:2123-2127. Turner, A. M., S. A. Fetterolf, and R. J. Bemot. 1999.Predator identity LITERATURE CITED and consumerbehavior: differential effects of fish and crayfish on the habitatuse of a freshwatersnail, Oecologia118:242-247. Appleton, R. D. and A. R. Palmer. 1988.Water-borne stimuli releasedby Vermeij, G. J. 1978. Biogeographyand Adaptation: Patterns of Marine predatorycrabs and damagedprey induce more predator-resistant Life, Harvard University Press,Cambridge, . 332 shells in a marine gastropod. Proceedings of the t/ationa/ PP Academyof Sciences85:4387-4391, Vermeij, G. J. 1982a.Gastropod shell form, breakage,and repair in rela- Bertness,M. D. and C, Cunningham.1981. Crab shell-crushingpredation tion to predationby the crab Calappa.Malacologi a 23:1-12. and gastropod architectural defense. Journal of Experimenta/ Venneij, G. J. 1982b.Environmental change and the evolutionaryhistory Marine Biology and Ecology50:213-230. of the periwinkle Littorina littorea! in . Evolution Bingham, F. O. 1972. Several aspects of the reproductive biology of 36:561-580. Littorina irrorata Gastropoda!.The /Vautilus 86:8-10. Vermeij, G. J. and A. P. Covich. 1978. Coevolution of freshwater gas- Blundon, J. A. and G. J. Vermeij, 1983. Effect of shell repair on shell tropodsand their predators.American /Vaturalist 112:833-843. strength in the gastropod Littorina irrorata. Marine Biology Vermeij, G. J., D. E. Schindler, and E. Zipser. 1981. Predationthrough 76:41-45. geological time: Evidence from gastropod shell repair. Science Covich, A. P., T. A. Crowl, J. E. Alexander,Jr., and C. C. Vaughn, 1994, 214:1024-1026. Predator-avoidanceresponses in freshwater decapod-gastropod Warren,J. H. 1985.Climbing as an avoidancebehaviour in the salt marsh interactionsmediated by chemical stimuli. Journal of the Worth periwinkle, Littorina irrorata Say!. Journal of Experimental A merican Benthological Society 13:283-290. Matine Biology and Ecology 89:11-28. Dix, T. L, and P, V. Hamilton. 1993.Chemically mediatedescape behav- West,D. I.. and A. H. Williams. 1986. Predationby Callinectessapidus ior in the marsh periwinkle Littoraria irrorata Say. Journal of Rathbun! within Spanina alterniflora Loisel! marshes.Journal ExperimentalMari ne Biology and Ecology 166;135-149, of ExperimentalMarine Biology and Ecology 100:75-95. Dodson,S. I. 1989.Predator-induced reaction norms. BioScience39:447- 452. 9htCaf ittugttJSurintaccentance: 10 december 2001 Dodson,S. I., T, A. Crowl, B. L. Peckarsky,L. B. Kats, A. P. t ovtcb-~~