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Similarity in predator-specific anti-predator behavior in ecologically distinct limpet species, Scurria viridula (Lottiidae) and Fissurella latimarginata (Fissurellidae)

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Abstract

Many marine gastropods show species-specific behavioral responses to different predators, but less is known about the mechanisms influencing differences or similarities in specific responses. Herein, we examined whether two limpet species, Scurria viridula (Lamarck, 1819) and Fissurella latimarginata (Sowerby, 1835), show species- and size-specific similarities or differences in their reaction to predatory seastars and crabs. Both S. viridula and F. latimarginata reacted to their main seastar predators with escape responses. In contrast, both limpets did not flee from common crab predators, but, instead, fastened to the rock. All tested size classes of both limpet species reacted in a similar way, escaping from seastars, but clamping onto the rock in response to crabs. Limpets could reach velocities sufficient to outrun their specific seastar predators, but they were not fast enough to escape crabs. Experiments with limpets of different shell conditions (with and without shell damage) indicated that F. latimarginata with a damaged shell showed “accommodation movements” (slow movements away from stimulus) in response to predatory crabs. In contrast, intact F. latimarginata and all S. viridula (intact and damaged) clamped the shell down to the substratum. The response details suggest that the keyhole limpet F. latimarginata is more sensitive to predators (faster reaction time, longer escape distances, and higher proportion of reacting individuals) than S. viridula, possibly because the morphology of F. latimarginata (the relationship of its shell size and structure to its total body size) makes this species more vulnerable to predation. Our study suggests that chemically mediated effects of seastar and crab predators result in contrasting behavioral responses of both limpet species, independent of their habitat and morphology. Despite the different characteristics of the limpet species and the identity of predators, the limpets react in comparable ways to similar predator types.

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References

  • Aguilera MA, Valdivia N, Broitman B (2013) Spatial niche differentiation and coexistence at the edge: co-occurrence distribution patterms in Scurria limpets. Mar Ecol Prog Ser 483:185–198

    Article  Google Scholar 

  • Ansell AD (1969) Escape responses of three Indian molluscs. Veliger 12:157–159

    Google Scholar 

  • Bancala F (2009) Function of mucus secretion by lamellose ormer, Haliotis tuberculata lamellosa, in response to starfish predation. Anim Behav 78:1189–1194

    Article  Google Scholar 

  • Barahona M, Navarrete S (2010) Movement patterns of the seastar Heliaster helianthus in central Chile: relationship with environmental conditions and prey availability. Mar Biol 157:647–661

    Article  Google Scholar 

  • Bertness MD, Cunningham C (1981) Crab shell-crushing predation and gastropods architectural defense. J Exp Mar Biol Ecol 50:213–230

    Article  Google Scholar 

  • Branch GM (1985) The impact of predation by kelp gulls Larus dominicanus on the sub-antarctic limpet Nacella delesserti. Polar Biol 4:171–177

    Article  Google Scholar 

  • Brock KM, Bednekoff PA, Pafilis P, Foufopoulos P (2015) Evolution of antipredator behavior in an island lizard species, Podarcis erhardii (Reptilia: Lacertidae): the sum of all fears? Evolution 69:216–231

    Article  Google Scholar 

  • Cedeño J, Voltzow J, Fetcher N (1996) Morphological differences between the pedal musculature of patellogastropod and fissurellid limpets. Veliger 39:164–172

    Google Scholar 

  • Cohen J (1988) Statistical power analysis for the behavioral sciences, Second edn. Lawrence Erlbaum Associated Publishers, Mahwah, New Jersey, USA, p 551

    Google Scholar 

  • Coleman RA, Browne M, Theobald T (2004) Aggregation as defense: limpet tenacity changes in response to simulated predator attack. Ecology 85:1153–1159

    Article  Google Scholar 

  • Dalby JE, Elliot JK, Ross DM (1987) The swim response of the actinian Stomphia didemon to certain asteroids: distributional and phylogenetic implications. Can J Zool 66:2484–2491

    Article  Google Scholar 

  • Dalesman S, Rundle SD, Cotton PA (2009) Crawl-out behaviour in response to predation cues in an aquatic gastropods: insights from artificial selection. Evol Ecol 23:907–918

    Article  Google Scholar 

  • Dayton PK, Rosenthal RJ, Mahen LC, Antezana T (1977) Population structure and foraging biology of the predaceous Chilean asteroid Meyenaster gelatinosus and the escape biology of its prey. Mar Biol 39:361–370

    Article  Google Scholar 

  • Dee LE, Witman JD, Brandt M (2012) Refugia and top-down control of the pencil urchin Eucidaris galapaguensis in the Galápagos marine reserve. J Exp Mar Biol Ecol 416–417:135–143

    Article  Google Scholar 

  • Donovan D, Baldwin J, Carefoot T (1999) The contribution of anaerobic energy to gastropod crawling and a re-estimation of minimum cost of transport in the abalone, Haliotis kamtschatkana (Jonas). J Exp Mar Biol Ecol 235:273–284

    Article  Google Scholar 

  • Escobar JB, Navarrete SA (2011) Risk recognition and variability in escape responses among intertidal molluskan grazers to the sun star Heliaster helianthus. Mar Ecol Prog Ser 421:151–161

    Article  Google Scholar 

  • Espoz C, Castilla JC (2000) Escape responses of four Chilean intertidal limpets to seastars. Mar Biol 137:887–892

    Article  Google Scholar 

  • Espoz C, Lindberg DR, Castilla JC, Simison WB (2004) Los patelogastrópodos intermareales de Chile y Perú. Rev Chil Hist Nat 77:257–283

    Article  Google Scholar 

  • Feder HM (1963) Gastropod defensive responses and their effectiveness in reducing predation by starfishes. Ecology 40:505–512

    Article  Google Scholar 

  • Feder HM (1972) Escape responses in marine invertebrates. Sci Am 227:93–100

    Article  CAS  Google Scholar 

  • Fernández M, Blanco M, Ruano-Chamorro C, Subida MD (2017) Reproductive output of two benthic resources (Fissurella latimarginata and Loxechinus albus) under different management regimes along the coast of central Chile. Lat Am J Aquat Res 45:391–402

    Article  Google Scholar 

  • Ferrari MCO, Wisenden BD, Chivers DP (2010) Chemical ecology of predator-prey interactions in aquatic systems: a review and prospectus. Can J Zool 88:698–724

    Article  Google Scholar 

  • Formanowicz DR, Brodie ED (1988) Predation risk and forager escape tactics. Anim Behav 36:1836–1860

    Article  Google Scholar 

  • Freeman AS (2007) Specificity of induced defenses in Mytilus edulis and asymmetrical predator deterrence. Mar Ecol Prog Ser 334:145–153

    Article  Google Scholar 

  • Garrity SD, Levings SC (1983) Homing to scars as a defense against predators in the pulmonate limpet Siphonaria gigas (Gastropoda). Mar Biol 72:319–324

    Article  Google Scholar 

  • Gaymer CF, Himmelman JH (2008) A keystone predatory sea star in the intertidal zone is controlled by a higher-order predatory sea star in the subtidal zone. Mar Ecol Prog Ser 370:143–153

    Article  Google Scholar 

  • Geller JB (1982) Chemically mediated avoidance response of a gastropod, Tegula funebralis (A. Adams), to a predatory crab Cancer antennarius (Stimpson). J Exp Mar Biol Ecol 65:19–27

    Article  Google Scholar 

  • Grosholz ED (2005) Recent biological invasion may hasten invasional meltdown by accelerating historical introductions. Proc Natl Acad Sci USA 102:1088–1091

    Article  CAS  Google Scholar 

  • Guderley HE, Himmelman JH, Nadeau M, Cortes HP, Tremblay I, Janssoone X (2015) Effect of different predators on the escape response of Placopecten magellanicus. Mar Biol 162:1407–1415

    Article  Google Scholar 

  • Himmelman JH, Guderley HE, Duncan PF (2009) Responses of the saucer scallop Amusium balloti to potential predators. J Exp Mar Biol Ecol 378:58–61

    Article  Google Scholar 

  • Iwasaki K (1993) Analyses of limpet defense and predator offense in the field. Mar Biol 116:277–289

    Article  Google Scholar 

  • Kikuchi T, Dol T (1987) Defensive escape response of two trochid sand snail species of the genus Umbonium: the effect of species-specific escape response to asteroid predators. Publ Amakusa Mar Biol Lab 9:47–65

    Google Scholar 

  • Kirk RE (1996) Practical significance: a concept whose time has come. Educ Psychol Meas 56:746–759

    Article  Google Scholar 

  • Lam KKY (2002) Escape responses of intertidal gastropods on a subtropical rocky shore in Hong Kong. J Moll Stud 68:297–306

    Article  Google Scholar 

  • Lima SL (1998) Nonlethal effects in the ecology of predator-prey interactions. Bioscience 48:25–34

    Article  Google Scholar 

  • Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640

    Article  Google Scholar 

  • Lindberg DR (1991) Marine biotic interchange between the northern and southern hemispheres. Paleobiology 17:308–324

    Article  Google Scholar 

  • Mahon AR, Amsler CD, McClintock JB, Baker BJ (2002) Chemo-tactile predator avoidance responses of the common Antarctic limpet Nacella concinna. Polar Biol 25:469–473

    Google Scholar 

  • Manzur T, Navarrete SA (2011) Scales of detection and escape of the sea urchin Tetrapygus niger in interactions with the predatory sun star Heliaster helianthus. J Exp Mar Biol Ecol 407:302–308

    Article  Google Scholar 

  • Manzur T, Vidal F, Pantoja JF, Fernández M, Navarrete SA (2014) Behavioural and physiological responses of limpet prey to a seastar predator and their transmission to basal trophic levels. J Anim Ecol 83:923–933

    Article  Google Scholar 

  • Markowska M, Kidawa A (2007) Encounters between Antarctic limpets, Nacella concinna, and predatory sea stars, Lysasterias sp., in laboratory and field experiments. Mar Biol 151:1959–1966

    Article  Google Scholar 

  • McLean JH (1984) Systematics of Fissurella in the Peruvian and Magallanic Faunal Provinces. Natural History Museum of Los Angeles County, Los Angeles. Contrib Sci 354:70

    Google Scholar 

  • Menge BA (1982) Effects of feeding on the environment: Asteroidea. In: Jangoux M, Lawrence JM (eds) Echinoderm nutrition. Balkema, Rotterdam, pp 521–551

    Google Scholar 

  • Mercurio KS, Palmer AR, Lowell RB (1985) Predator-mediated microhabitat partitioning by two species of visually cryptic, intertidal limpets. Ecology 66:1417–1425

    Article  Google Scholar 

  • Miller LP, Harley CDG, Denny MW (2009) The role of temperature and desiccation stress in limiting the local-scale distribution of the owl limpet, Lottia gigantea. Funct Ecol 23:756–767

    Article  Google Scholar 

  • Navarrete S, Manzur T (2008) Individual- and population-level responses of a keystone predator to geographic variation in prey. Ecology 89:2005–2018

    Article  Google Scholar 

  • Olejnik S, Algina J (2003) Generalized Eta and Omega squared statistics. Measures of effect size for some common research designs. Psychol Methods 8:434–447

    Article  Google Scholar 

  • Paine RT (1969) The PisasterTegula interaction: prey patches, predator food preference and intertidal community structure. Ecology 50:950–961

    Article  Google Scholar 

  • Phillips DW (1978) Chemical mediation of invertebrate defensive behaviors and the ability to distinguish between foraging and inactive predators. Mar Biol 49:237–243

    Article  Google Scholar 

  • Powers SP, Kittinger JN (2002) Hydrodynamic mediation of predator-prey interactions: differential patterns of prey susceptibility and predator success explained by variation in water flow. J Exp Mar Biol Ecol 273:171–187

    Article  Google Scholar 

  • Pruitt NJ, Stachowicz JJ, Sih A (2012) Behavioral types of predator and prey jointly determine prey survival: potential implications for the maintenance of within-species behavioral variation. Am Nat 179:217–227

    Article  Google Scholar 

  • R Development Core Team R (2018) R: a language and environment for statistical computing. R Found Stat Comput. http://dx.doi.org/10.1007/978-3-540-74686-7

  • Rochette R, Dill LM (2000) Mortality, behavior and the effects of predators on the intertidal distribution of littorinid gastropods. J Exp Mar Biol Ecol 253:165–191

    Article  CAS  Google Scholar 

  • Rochette R, McNeil JN, Himmelman JH (1996) Inter- and intra-population variations in the response of the whelk Buccinum undatum to the predatory astreroid Leptasterias polaris. Mar Ecol Prog Ser 142:193–201

    Article  Google Scholar 

  • Rochette R, Dill LM, Himmelman JH (1997) A field test of threat sensitivity in a marine gastropod. Anim Behav 54:1053–1062

    Article  CAS  Google Scholar 

  • Rochette R, Arsenault DJ, Justome B, Himmelmann JH (1998) Chemically-mediated predator-recognition learning in a marine gastropod. Ecoscience 5:353–360

    Article  Google Scholar 

  • Rochette R, Maltais M, Dill LM, Himmelman JH (1999) Interpopulation and context-related differences in responses of a marine gastropod to predation risk. Anim Behav 57:977–987

    Article  CAS  Google Scholar 

  • San-Martin A, Rovirosa J, Gaete K, Olea A, Ampuero J (2009) Mantle defensive response of marine pulmonate Trimusculus peruvianus. J Exp Mar Biol Ecol 376:43–47

    Article  Google Scholar 

  • Seeley RH (1986) Intense natural selection caused a rapid morphological transition in a living marine snail. Proc Nat Acad Sci USA 83:6897–6901

    Article  CAS  Google Scholar 

  • Sih A, Englund G, Wooster D (1998) Emergent impacts of multiple predators on prey. Trends Ecol Evol 13:350–355

    Article  CAS  Google Scholar 

  • Smee DL, Weissburg MJ (2002) Clamming up: environmental forces diminish the perceptive ability of bivalve prey. Ecology 87:1587–1598

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry. The principles and practice of statistics in biological research. W.H. Freeman, San Francisco, p 859

    Google Scholar 

  • Stapley J (2004) Do mountain log skinks (Pseudomoia entrecasteauxii) modify their behaviour in the presence of two predators? Behav Ecol Sociobiol 56:185–189

    Article  Google Scholar 

  • Tokeshi M, Romero L (1995) Quantitative analysis of foraging behaviour in a field population of the South American sun–star Heliaster helianthus. Mar Biol 122:297–303

    Google Scholar 

  • Trussell GC (1996) Phenotypic plasticity in an intertidal snail: the role of a common crab predator. Evolution 50:448–454

    Article  Google Scholar 

  • Trussell GC, Ewanchuk PJ, Bertness MD (2003) Trait-mediated effects in rocky intertidal food chains: predator risk cues alter prey feeding rates. Ecology 84:629–640

    Article  Google Scholar 

  • Turner AM, Turner SE, Lappi HM (2006) Learning, memory and predator avoidance by freshwater snails: effects of experience on predator recognition and defensive strategy. Anim Behav 72:1443–1450

    Article  Google Scholar 

  • Urriago JD, Himmelman JH, Gaymer CF (2011) Responses of the black sea urchin Tetrapygus niger to its sea-star predators Heliaster helianthus and Meyenaster gelatinosus under field conditions. J Exp Mar Biol Ecol 399:17–24

    Article  Google Scholar 

  • Urriago JD, Himmelman JH, Gaymer CF (2012) Sea urchin Tetrapygus niger distribution on elevated surfaces represents a strategy for avoiding predatory sea stars. Mar Ecol Prog Ser 444:85–95

    Article  Google Scholar 

  • Vance SA, Peckarsky BL (1997) The effect of mermithid parasitism on predation of nymphal Baetis bicaudatus (Ephemeroptera) by invertebrates. Oecologia 110:147–152

    Article  Google Scholar 

  • Vermeij GJ (2016) The limpet form in gastropods: evolution, distribution and implications for the comparative study of history. Biol J Linn Soc 120:22–37

    Google Scholar 

  • Vermeij GJ, Schindel DE, Zipser E (1981) Predation through geological time: evidence from gastropod shell repair. Science 214:1024–1026

    Article  CAS  Google Scholar 

  • Weissburg M, Smee DL, Ferner MC (2014) The sensory ecology of non-consumptive predator effects. Am Nat 184:141–157

    Article  Google Scholar 

  • West K, Cohen A, Baron M (1991) Morphology and behavior of crabs and gastropods from Lake Tanganyika, Africa: implications for lacustrine predator-prey coevolution. Evolution 45:589–607

    Article  Google Scholar 

  • Williams GA, Morritt D (1995) Habitat partitioning and thermal tolerance in a tropical limpet, Cellana grata. Mar Ecol Prog Ser 124:89–103

    Article  Google Scholar 

  • Wong MC, Barbeau MA (2003) Effects of substrate on interactions between juvenile sea scallops (Placopecten magellanicus Gmelin) and predatory sea stars (Asterias vulgaris Verrill) and rock crabs (Cancer irroratus Say). J Exp Mar Biol Ecol 287:155–178

    Article  Google Scholar 

  • Zimmer RK, Butman CA (2000) Chemical signaling processes in the marine environment. Biol Bull 198:168–187

    Article  CAS  Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extension in ecology with R, 2nd edn. Springer, New York

    Book  Google Scholar 

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Acknowledgements

We are most grateful to S. Boltaña and I. Hinojosa for their help in the field, and to C. Correa who kindly provided the velocity data for M. gelatinosus. Our special thanks go to J. Long, who gave many helpful comments on an early version of the manuscript. This manuscript was substantially improved by numerous constructive comments from four anonymous reviewers and the editors. We greatly appreciate the critical review provided by T. Manzur who commented on the final version of the manuscript, and we thank L. Eastman for editing the English of the final manuscript.

Funding

MAA was financed by FONDECYT #1160223 and PAI-CONICYT #79150002, and MT received support through FONDECYT #1161383 during the writing of the manuscript

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MT and MW conceived the study. MW conducted the field and laboratory experiments. MAA reanalyzed all data and led the writing of the revised manuscript, which had been initially prepared by MT and MW.

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Correspondence to Martin Thiel.

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Aguilera, M.A., Weiß, M. & Thiel, M. Similarity in predator-specific anti-predator behavior in ecologically distinct limpet species, Scurria viridula (Lottiidae) and Fissurella latimarginata (Fissurellidae). Mar Biol 166, 41 (2019). https://doi.org/10.1007/s00227-019-3485-5

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