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Introduced predator elicits population-specific responses from prey

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Abstract

Predator induced responses by prey can reduce risk, however, newly introduced predators may not elicit the same predator responses, thus making prey more vulnerable to these new predators. Therefore, examining responses of different prey populations of the same species to a non-native predator may provide novel insights for the evolution of predator recognition. Here, we tested the response of three populations of a low-dispersing marine gastropod (Littorina saxatilis) to chemical cues from a native crab predator (Dyspanopeus sayi) and a newly introduced crab predator (Hemigrapsus sanguineus). Using geometric morphometrics to study shell shape changes, we found that snails from all populations responded similarly to the native predator but differed in their response to the non-native predator. Snails from two of the three populations elicited no response to H. sanguineus, while the other population produced a more rotund shell, similar to their response to the native predator. Shell shape response in snails exposed to the native predator was different from those fed a reduced diet, suggesting that these anti-predator responses are active changes to shell morphology and not a by-product of reduced feeding in the presence of predators as suggested by other studies. Lastly, there were innate population shell shape differences, suggesting possible distinct ecotypes for Littorina saxatilis in North America as seen in European populations. Overall, populations differed in their response to an invasive predator indicating that evolution of predator recognition can differ between populations of the same species with similar co-existent history with the invader.

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References

  • Adams DC, Rohlf FJ, Slice DE (2004) Geometric morphometrics: ten years of progress following the ‘revolution’. Ital J Zool 71(1):5–16

    Google Scholar 

  • Anson JR, Dickman CR (2013) Behavioral responses of native prey to disparate predators: naiveté and predator recognition. Oecologia 171:367–377

    PubMed  Google Scholar 

  • Appleton RD, Palmer AR (1988) Water-borne stimuli released by predatory crabs and damaged prey induce more predator-resistant shells in a marine gastropod. Proc Natl Acad Sci USA 85:4387–4391

    CAS  PubMed  Google Scholar 

  • Archer SK, Crowl TA (2014) Retention of learned predator recognition in an endangered sucker Chasmistes liorus liorus. Aquat Biol 20(3):195–202

    Google Scholar 

  • Barshaw DE, Lavalli KL (1988) Predation upon postlarval lobsters Homarus americanus by cunners Tautogolabrus adspersus and mud crabs Neopanope sayi on three different substrates: eelgrass, mud and rocks. Mar Ecol Prog Ser 48(2):119–123

    Google Scholar 

  • Bible JM, Griffith KR, Sanford E (2017) Inducible defenses in Olympia oysters in response to an invasive predator. Oecologia 183(3):809–819

    PubMed  Google Scholar 

  • Bookstein FL (1991) Morphometric tools for landmark data: geometry and biology. Cambridge University Press, Cambridge

    Google Scholar 

  • Boulding EG, José Rivas M, González-Lavín N, Rolán-Alvarez E, Galindo J (2017) Size selection by a gape-limited predator of a marine snail: insights into magic traits for speciation. Ecol Evol 7:674–688

    PubMed  Google Scholar 

  • Bourdeau PE (2009) Prioritized phenotypic responses to combined predators in a marine snail. Ecology 90:1659–1669

    PubMed  Google Scholar 

  • Bourdeau PE (2010) Cue reliability, risk sensitivity and inducible morphological defense in a marine snail. Oecologia 162:987–994

    PubMed  Google Scholar 

  • Bourdeau PE, Johansson F (2012) Predator-induced morphological defences as a by-products of prey behaviour: a review and prospectus. Oikos 121:1175–1190

    Google Scholar 

  • Bourdeau PE, O’Connor NJ (2003) Predation by the nonindigenous Asian shore crab Hemigrapsus sanguineus on macroalgae and molluscs. Northeast Nat 10:319–334

    Google Scholar 

  • Bourdeau PE, Padilla DK (2019) Cue specificity of predator-induced phenotype in a marine snail: is a crab just a crab? Mar Biol 166:84. https://doi.org/10.1007/s00227-019-3526-0

    Article  Google Scholar 

  • Brown GE, Rive AC, Ferrari MC, Chivers DP (2006) The dynamic nature of antipredator behavior: prey fish integrate threat-sensitive antipredator responses within background levels of predation risk. Behav Ecol Sociobiol 61(1):9–16

    Google Scholar 

  • Conde-Padín P, Grahame JW, Rolán-Alvarez E (2007) Detecting shape differences in species of the Littorina saxatilis complex by morphometric analysis. J Molluscan Stud 73:147–154

    Google Scholar 

  • Conner JK, Hartl DL (2004) A primer of ecological genetic. Sunderland, Massachusetts

    Google Scholar 

  • Cox JG, Lima SL (2006) Naiveté and an aquatic–terrestrial dichotomy in the effects of introduced predators. Trends Ecol Evol 21(12):674–680

    PubMed  Google Scholar 

  • DeWitt TJ, Robinson BW, Wilson DS (2000) Functional diversity among predators of a freshwater snail imposes an adaptive trade-off for shell morphology. Evol Ecol Res 2(2):129–148

    Google Scholar 

  • Duffy JE, Hay ME (1994) Herbivore resistance to seaweed chemical defense: the roles of mobility and predation risk. Ecology 75(5):1304–1319

    Google Scholar 

  • Edgell TC, Neufeld CJ (2008) Experimental evidence for latent developmental plasticity: intertidal whelks respond to a native but not an introduced predator. Biol Lett 4:385–387

    PubMed  PubMed Central  Google Scholar 

  • Fell PE, Olmstead NC, Carlson E, Jacob W, Hitchcock D, Silber G (1982) Distribution and abundance of macroinvertebrates on certain Connecticut tidal marshes, with emphasis on dominant molluscs. Estuaries 5(3):234–239

    Google Scholar 

  • Ferrari MC, Sih A, Chivers DP (2009) The paradox of risk allocation: a review and prospectus. Anim Behav 78(3):579–585

    Google Scholar 

  • Fisk D, Latta LC, Knapp RA, Pfrender ME (2007) Rapid evolution in response to introduced predators I: rates and patterns of morphological and life-history trait divergence. BMC Evol Biol. https://doi.org/10.1186/1471-2148-7-22

    Article  PubMed  PubMed Central  Google Scholar 

  • Freeman AS, Byers JE (2006) Divergent induced responses to an invasive predator in marine mussel populations. Science 313(5788):831–833

    CAS  PubMed  Google Scholar 

  • Fruciano C (2016) Measurement error in geometric morphometrics. Dev Genes Evol 226(3):139–158

    PubMed  Google Scholar 

  • Fuller R, Berglund A (1996) Behavioral responses of a sex-role reversed pipefish to a gradient of perceived predation risk. Behav Ecol 7(1):69–75

    Google Scholar 

  • Gelšvartas J (2005) Geometric morphometrics. http://homepages.inf.ed.ac.uk/rbf/CVonline/LOCAL_COPIES/AV0910/gelsvartas.pdf. Accessed 02 July 2020

  • Giles N, Huntingford FA (1984) Predation risk and inter-population variation in antipredator behaviour in the three-spined stickleback, Gasterosteus aculeatus L. Anim Behav 32(1):264–275

    Google Scholar 

  • Granovitch AI, Yagunova EB, Maximovich AN, Sokolova IM (2009) Elevated female fecundity as a possible compensatory mechanism in response to trematode infestation in populations of Littorina saxatilis (Olivi). Int J Parasitol 39(9):1011–1019

    CAS  PubMed  Google Scholar 

  • Hammer Ø, Harper DA, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):9

    Google Scholar 

  • Harvell CD (1998) Genetic variation and polymorphism in the inducible spines of a marine bryozoan. Evolution 52(1):80–86

    PubMed  Google Scholar 

  • Havel JE, Dodson SI (1984) Chaoborus predation on typical and spined morphs of Daphnia pulex: behavioral observations. Limnol Oceanogr 29:487–494

    Google Scholar 

  • Helfman GS, Winkelman DL (1997) Threat sensitivity in bicolor damselfish: effects of sociality and body size. Ethology 103(5):369–383

    Google Scholar 

  • Hollander J, Butlin RK (2010) The adaptive value of phenotypic plasticity in two ecotypes of a marine gastropod. BMC Evol Biol 10:333

    PubMed  PubMed Central  Google Scholar 

  • Hooks AP, Padilla DK (2014) Prey responses to the presence of a native and nonnative predator. J Exp Mar Biol Ecol 461:209–215

    Google Scholar 

  • Hughes RN (1995) Resource allocation, demography and the radiation of life histories in rough periwinkles (Gastopoda). Hydrobiology 309:1–14

    Google Scholar 

  • Januszkiewicz AJ, Robinson BW (2007) Divergent walleye (Sander vitreus)-mediated inducible defenses in the centrarchid pumpkinseed sunfish (Lepomis gibbosus). Biol J Linn Soc 90(1):25–36

    Google Scholar 

  • Johannesson K (2003) Evolution in Littorina: ecology matters. J Sea Res 49:107–117

    Google Scholar 

  • Johannesson B, Johannesson K (1996) Population differences in behaviour and morphology in the snail Littorina saxatilis: phenotypic plasticity or genetic differentiation? J Zool 240(3):475–493

    Google Scholar 

  • Johannesson K, Rolán-Alvarez E, Ekendahl A (1995) Incipient reproductive isolation between two sympatric morphs of the intertidal snail Littorina saxatilis. Evolution 49(6):1180–1190

    PubMed  Google Scholar 

  • Johannesson K, Rolán-Alvarez E, Erlandsson J (1997) Growth rate differences between upper and lower shore ecotypes of the marine snail Littorina saxatilis (Olivi) (Gastropoda). Biol J Linn Soc 61:267–279

    Google Scholar 

  • Kawecki TJ (2000) Adaptation to marginal habitats: contrasting influence of the dispersal rate on the fate of alleles with small and large effects. Proc R Soc Lond 267(1450):1315–1320

    CAS  Google Scholar 

  • Kess T, Boulding EG (2019) Genome-wide association analyses reveal polygenic genomic architecture underlying divergent shell morphology in Spanish Littorina saxatilis ecotypes. Ecol Evol 9(17):9427–9441

    PubMed  PubMed Central  Google Scholar 

  • Kess T, Galindo J, Boulding EG (2018) Genomic divergence between Spanish Littorina saxatilis ecotypes unravels limited admixture and extensive parallelism associated with population history. Ecol Evol 8(16):8311–8327

    PubMed  PubMed Central  Google Scholar 

  • Kimbro DL, Grosholz ED, Baukus AJ, Nesbitt NJ, Travis NM, Attoe S, Coleman-Hulbert C (2009) Invasive species cause large-scale loss of native California oyster habitat by disrupting trophic cascades. Oecologia 160(3):563–575

    PubMed  Google Scholar 

  • Kocovsky PM, Adams JV, Bronte CR (2009) The effect of sample size on the stability of principal components analysis of truss-based fish morphometrics. Trans Am Fish Soc 138(3):487–496

    Google Scholar 

  • Kuehne LM, Olden JD (2012) Prey naivety in the behavioural responses of juvenile Chinook salmon (Oncorhynchus tshawytscha) to an invasive predator. Freshw Biol 57(6):1126–1137

    Google Scholar 

  • Large SI, Smee DL (2010) Type and nature of cues used by Nucella lapillus to evaluate predation risk. J Exp Mar Biol Ecol 396(1):10–17

    Google Scholar 

  • Ledesma ME, O’Connor NJ (2001) Habitat and diet of the non-native crab Hemigrapsus sanguineus in southeastern New England. Northeast Nat 8(1):63–78

    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

    Google Scholar 

  • Linting M, Van Os BJ, Meulman JJ (2011) Statistical significance of the contribution of variables to the PCA solution: an alternative permutation strategy. Psychometrika 76(3):440–460

    Google Scholar 

  • Mäkinen T, Panova M, Johannesson K, Tatarenkov A, Appelqvist C, Andre C (2008) Genetic differentiation on multiple spatial scales in an ecotype-forming marine snail with limited dispersal: Littorina saxatilis. Biol J Linn Soc 94(1):31–40

    Google Scholar 

  • McDermott JJ (1998) The western Pacific brachyuran (Hemigrapsus sanguineus: grapsidae), in its new habitat along the Atlantic coast of the United States: geographic distribution and ecology. ICES J Mar Sci 55:289–298

    Google Scholar 

  • Mistri M (2004) Predatory behavior and preference of a successful invader, the mud crab Dyspanopeus sayi (Panopeidae), on its bivalve prey. J Exp Mar Biol Ecol 312(2):385–398

    Google Scholar 

  • Nizinski MS (2003) Annotated checklist of decapod crustaceans of Atlantic coastal and continental shelf waters of the United States. Proc Biol Soc Wash 116(1):96–157

    Google Scholar 

  • Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2013) Package ‘vegan’. Commun Ecol Package Version 2(9):1–295

    Google Scholar 

  • Palmer R (1990) Effect of crab effluent and scent of damaged conspecifics on feeding, growth, and shell morphology of the Atlantic dogwhelk Nucella lapillus (L.). Hydrobiologia 193:155–182

    Google Scholar 

  • Pardo LM, Johnson LE (2005) Explaining variation in life-history traits: growth rate, size, and fecundity in a marine snail across an environmental gradient lacking predators. Mar Ecol Prog Ser 296:229–239

    Google Scholar 

  • Pardo LM, Johnson LE (2006) Influence of water motion and reproductive attributes on movement and shelter use in the marine snail Littorina saxatilis. Mar Ecol Prog Ser 315:177–186

    Google Scholar 

  • Quensen JF III, Woodruff DS (1997) Associations between shell morphology and land crab predation in the land snail. Funct Ecol 11:464–471

    Google Scholar 

  • R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • Reid DG (1993) Barnacle-dwelling ecotypes of three British Littorina species and the status of Littorina neglecta Bean. J Mollus Stud 59(1):51–62

    Google Scholar 

  • Reid DG (1996) Systematics and evolution of Littorina. The Ray Society, London, p 463p

    Google Scholar 

  • Relyea RA (2002) Local population differences in phenotypic plasticity: predator induced changes in wood frog tadpoles. Ecol Monogr 72(1):77–93

    Google Scholar 

  • Rohlf FJ, Marcus LF (1993) A revolution in morphometrics. Trends Ecol Evol 8:129–132

    Google Scholar 

  • Rolán-Alvarez E, Johannesson K, Erlandsson J (1997) The maintenance of a cline in the marine snail Littorina saxatilis: the role of home site advantage and hybrid fitness. Evolution 51(6):1838–1847

    PubMed  Google Scholar 

  • Rolán-Alvarez E, Carvajal-Rodríguez A, de Coo A, Cortés B, Estévez D, Ferreira M, González R, Briscoe AD (2015) The scale-of-choice effect and how estimates of assortative mating in the wild can be biased due to heterogeneous samples. Evolution 69(7):1845–1857

    PubMed  Google Scholar 

  • Selden R, Johnson AS, Ellers O (2009) Waterborne cues from crabs induce thicker skeletons, smaller gonads and size-specific changes in growth rate in sea urchins. Mar Biol 156(5):1057–1071

    PubMed  PubMed Central  Google Scholar 

  • Sih A (1980) Optimal behavior: can foragers balance two conflicting demands? Science 210(4473):1041–1043

    CAS  PubMed  Google Scholar 

  • Sih A, Bolnick DI, Luttbeg B, Orrock JL, Peacor SD, Pintor LM, Preisser E, Rehage JS, Vonesh JR (2010) Predator–prey naïveté, antipredator behavior, and the ecology of predator invasions. Oikos 119(4):610–621

    Google Scholar 

  • Sokolova I (1995) Influence of trematodes on the demography of Littorina saxatilis (Gastropoda:Prosobranchia:Littorinidae) in the White Sea. Dis Aquat Organ 21:91–101

    Google Scholar 

  • Stankowich T, Blumstein DT (2005) Fear in animals: a meta-analysis and review of risk assessment. Proc R Soc B Biol Sci 272(1581):2627–2634

    Google Scholar 

  • Strieb MD, Bricelj VM, Bauer SI (1995) Population biology of the mud crab, Dyspanopeus sayi, an important predator of juvenile bay scallops in Long Island (USA) eelgrass beds. J Shellfish Res 14:347–357

    Google Scholar 

  • Tollrian R, Harvell CD (eds) (1999) The ecology and evolution of inducible defenses. Princeton University Press, Princeton

    Google Scholar 

  • Trussell GC, Nicklin M (2002) Cue sensitivity, inducible defense, and trade-offs in a marine snail. Ecology 83:1635–1647

    Google Scholar 

  • Watanabe A (2018) How many landmarks are enough to characterize shape and size variation? PLoS ONE 13(6):e0198341

    PubMed  PubMed Central  Google Scholar 

  • Yamada SB (1989) Are direct developers more locally adapted than planktonic developers? Mar Biol 103(3):403–411

    Google Scholar 

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Acknowledgements

We thank the Padilla Lab group for their assistance in this project. We thank Steve Abrams for his help with experimental set up, Flax Marine Lab for the use of facilities, and the Crane Neck Association for access to sample site. We thank Jim Rohlf for his help in the analysis of the geometric morphometric data. The project was supported by Sigma Xi grants-in-aid awarded to Alexandra Hooks and a National Science Foundation grant IOS-0920032 awarded to Dr. Dianna Padilla. We would also like to thank two anonymous reviewers for providing insightful comments that contributed to the improvement of this manuscript.

Funding

Funding was provided through Sigma Xi grants-in-aid to Alexandra Hooks and was also supported by NSF Grant IOS-0920032 to Dianna K. Padilla.

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  1. Department of Biological Science, Florida State University, Tallahassee, FL, 32304, USA

    Alexandra P. Hooks

  2. Department of Ecology and Evolution, Stony Brook, NY, 11794-5245, USA

    Alexandra P. Hooks & Dianna K. Padilla

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  1. Alexandra P. Hooks
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DKP and APH designed the study. APH performed the research, collected data, and analyzed the data with help from DKP. APH wrote the first draft of the manuscript, and both authors contributed to manuscript revisions.

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Correspondence to Alexandra P. Hooks.

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Hooks, A.P., Padilla, D.K. Introduced predator elicits population-specific responses from prey. Biol Invasions 23, 477–490 (2021). https://doi.org/10.1007/s10530-020-02376-5

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