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Intertidal crustaceans use seaweed-derived chemical cues to mitigate predation risk

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Abstract

As predation is a primary driver of mortality, the need to minimize predation risk can shape prey behavior, influencing habitat selection and investment in vigilance. As structurally complex habitats can reduce predation risk, prey within heterogeneous environments may have evolved sensory abilities to locate them. In temperate rocky intertidal systems, fucoid seaweeds are a main source of structural complexity and can provide shelter for small organisms. This study examined the effects of predation risk on habitat selection in a tide pool-dwelling shrimp, Palaemon affinis, specifically testing whether predation risk drives preferences for fucoid seaweeds and if shrimps use chemical cues to locate fucoid-rich habitats. While tide pools with and without fucoids were equally abundant, P. affinis densities were >3 times higher in pools containing fucoids. The relationship between P. affinis and fucoids appears to be related to predation risk with P. affinis exhibiting a preference for fucoid microhabitats when a potential predator was present. Shrimps could distinguish between olfactory signatures from tide pools with and without fucoids and the odor of fucoids from other marine algae, suggesting that chemical cues are used to identify these structurally complex habitats. In addition to reducing predation risk, fucoid-rich habitats may provide better access to essential resources and reduce exposure to other biotic and abiotic stressors. This study shows that prey organisms can rapidly modify habitat use based on ambient predation risk, with olfactory cues used to identify the shelter characteristics of different habitats.

Significance statement

Predation is the major source of mortality for most animal species. For this reason, animals may have evolved ways to minimize predation risk by modifying their behavior. In this study, we show that small tide pool-dwelling shrimps modify their habitat use in response to predators, using chemical cues to locate and identify structurally complex habitats that could reduce predation risk when this risk is high.

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References

  • Almany GR (2004) Does increased habitat complexity reduce predation and competition in coral reef fish assemblages? Oikos 106:275–284

    Article  Google Scholar 

  • Al-Maslamani I, Walton MEM, Kennedy HA, Al-Mohannadi M, Le Vay L (2013) Are mangroves in arid environments isolated systems? Life-history and evidence of dietary contribution from inwelling in a mangrove-resident shrimp species. Estuar Coast Shelf Sci 124:56–63

    Article  Google Scholar 

  • Anderson O (1984) Optimal foraging by largemouth bass in structured environments. Ecology 65:851–861

    Article  Google Scholar 

  • Ashelby CW, De Grave S, Johnson ML (2013) The global invader (Decapoda, Palaemonidae): an interrogation of records and a synthesis of data. Crustaceana 86:594–624

    Article  Google Scholar 

  • Atema J (2012) Aquatic odor dispersal fields: opportunities and limits of detection, communication and navigation. In: Bronmark C, Hansson L-A (eds) Chemical ecology in aquatic systems. Oxford University Press, Oxford, pp 1–18

    Chapter  Google Scholar 

  • Beck DD, Jennings RD (2003) Habitat use by gila monsters: the importance of shelters. Herpetol Monogr 17:111–129

    Article  Google Scholar 

  • Berthelsen AK, Hewitt JE, Taylor RB (2015) Biological traits and taxonomic composition of invertebrate assemblages associated with coralline turf along an environmental gradient. Mar Ecol Prog Ser 530:15–27

    Article  Google Scholar 

  • Binckley CA, Resetarits WJ (2005) Habitat selection determines abundance, richness and species composition of beetles in aquatic communities. Biol Lett 1:370–374

    Article  PubMed  PubMed Central  Google Scholar 

  • Bishop MJ, Byers JF (2015) Predation risk predicts use of a novel habitat. Oikos 124:1225–1231

    Article  Google Scholar 

  • Brooker RM, Dixson DL (2016) Assessing the role of olfactory cues in the early life history of coral reef fish: current methods and future directions. In: Shulte B (ed) Chemical signals in vertebrates 13. Springer, New York, pp 7–31

    Google Scholar 

  • Brooker RM, Dixson DL (2017) Comparable cross-taxa risk perception via chemical cues in marine and freshwater crustaceans. Mar Fresh Res In Press

  • Brooker RM, Munday PL, McLeod IM, Jones GP (2013) Habitat preferences of a corallivorous reef fish: predation risk versus food quality. Coral Reefs 32:613–622

    Article  Google Scholar 

  • Burger J, Howe MA, Hahn DC, Chase J (1977) Effects of tide cycles on habitat selection and habitat partitioning by migrating shorebirds. Auk 94:743–758

    Article  Google Scholar 

  • Connell JH (1972) Community interactions on marine rocky intertidal shores. Annu Rev Ecol Syst 3:169–192

    Article  Google Scholar 

  • Connell SD, Anderson MJ (1999) Predation by fish on assemblages of intertidal epibiota: effects of predator size and patch size. J Exp Mar Biol Ecol 241:15–29

    Article  Google Scholar 

  • Creel S, Winnie JA Jr (2005) Responses of elk herd size to fine-scale spatial and temporal variation in the risk of predation by wolves. Anim Behav 69:1181–1189

    Article  Google Scholar 

  • Derby C, Sorensen P (2008) Neural processing, perception, and behavioral responses to natural chemical stimuli by fish and crustaceans. J Chem Ecol 34:898–914

    Article  CAS  PubMed  Google Scholar 

  • Dixson DL, Jones GP, Munday PL, Planes S, Pratchett MS, Srinivasan M, Syms C, Thurrold SR (2008) Coral reef fish smell leaves to find island homes. Proc R Soc B Biol Sci 275:2831–2839

    Article  Google Scholar 

  • Erickson AA, Paul VJ, Van Alstyne KL, Kwiatkowski LM (2006) Palatability of macroalgae that use different types of chemical defenses. J Chem Ecol 32:1883–1895

    Article  CAS  PubMed  Google Scholar 

  • Forsman JT, Mönkkönen M, Korpimäki E, Thomson RL (2013) Mammalian nest predator feces as a cue in avian habitat selection decisions. Behav Ecol 24:262–266

    Article  Google Scholar 

  • Fretwell SD, Lucas HL (1969) On territorial behavior and other factors influencing habitat distribution in birds: I. Theoretical development. Acta Biotheor 19:16–36

    Article  Google Scholar 

  • Futuyma DJ, Moreno G (1988) The evolution of ecological specialization. Annu Rev Ecol Syst 19:207–233

    Article  Google Scholar 

  • Gerlach G, Atema J, Kingsford MJ, Black KP, Miller-Sims V (2007) Smelling home can prevent dispersal of reef fish larvae. Proc Natl Acad Sci U S A 104:858–863

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gilliam JF, Fraser DF (1987) Habitat selection under predation hazard: test of a model with foraging minnows. Ecology 68:1856–1862

    Article  Google Scholar 

  • Hacker SD, Steneck RS (1990) Habitat architecture and the abundance and body-size-dependent habitat selection of a phytal amphipod. Ecology 71:2269–2285

    Article  Google Scholar 

  • Halliday WD, Blouin-Demers G (2014) Red flour beetles balance thermoregulation and food acquisition via density-dependent habitat selection. J Zool 294:198–205

    Article  Google Scholar 

  • Hay ME (2009) Marine chemical ecology: chemical signals and cues structure marine populations, communities, and ecosystems. Annu Rev Mar Sci 1:193–212

    Article  Google Scholar 

  • Hay M (2011) Crustaceans as powerful models in aquatic chemical ecology. In: Breithaupt T, Thiel M (eds) Chemical communication in crustaceans. Springer, New York, pp 41–62

    Google Scholar 

  • Heather BD, Robertson HA (1996) The field guide to the birds of New Zealand. Viking, Auckland

    Google Scholar 

  • Heck KL Jr, Wilson KA (1987) Predation rates on decapod crustaceans in latitudinally separated seagrass communities: a study of spatial and temporal variation using tethering techniques. J Exp Mar Biol Ecol 107:87–100

    Article  Google Scholar 

  • Hicks GRF (1977) Observations on substrate preference of marine phytal harpacticoids (Copepoda). Hydrobiologia 56:7–9

    Article  Google Scholar 

  • Hipfner JM, Elner RW (2013) Sea-surface temperature affects breeding density of an avian rocky intertidal predator, the black oystercatcher Haematopus bachmani. J Exp Mar Biol Ecol 440:29–34

    Article  Google Scholar 

  • Holmlund MB, Peterson CH, Hay ME (1990) Does algal morphology affect amphipod susceptibility to fish predation? J Exp Mar Biol Ecol 139:65–83

    Article  Google Scholar 

  • Huey RB (1991) Physiological consequences of habitat selection. Am Nat 137:S91–S115

    Article  Google Scholar 

  • Huggett J, Griffiths CL (1986) Some relationships between elevation, physicochemical variables and biota of intertidal rock pools. Mar Ecol Prog Ser 29:189–197

    Article  Google Scholar 

  • Jenkins SR (2005) Larval habitat selection, not larval supply, determines settlement patterns and adult distribution in two chthamalid barnacles. J Anim Ecol 74:893–904

    Article  Google Scholar 

  • Kennedy M, Gray RD (1993) Can ecological theory predict the distribution of foraging animals? A critical analysis of experiments on the ideal free distribution. Oikos 68:158–166

    Article  Google Scholar 

  • Krause J, Godin JGJ (1996) Influence of prey foraging posture on flight behavior and predation risk: predators take advantage of unwary prey. Behav Ecol 7:264–271

    Article  Google Scholar 

  • Lasley-Rasher RS, Rasher DB, Marion ZH, Taylor RB, Hay ME (2011) Predation constrains host choice for a marine mesograzer. Mar Ecol Prog Ser 434:91–99

    Article  Google Scholar 

  • Lecchini D, Planes S, Galzin R (2007) The influence of habitat characteristics and conspecifics on attraction and survival of coral reef fish juveniles. J Exp Mar Biol Ecol 341:85–90

    Article  Google Scholar 

  • Lesutienė J, Gasiūnaitė ZR, Reda Strikaitytė R, Žilienė R (2014) Trophic position and basal energy sources of the invasive prawn Palaemon elegans in the exposed littoral of the SE Baltic Sea. Aquat Invasions 9:37–45

    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 

  • Lovell PG, Ruxton GD, Langridge KV, Spencer KA (2013) Egg-laying substrate selection for optimal camouflage by quail. Curr Biol 23:260–264

    Article  CAS  PubMed  Google Scholar 

  • Martin TE (1998) Are microhabitat preferences of coexisting species under selection and adaptive? Ecology 79:656–670

    Article  Google Scholar 

  • McIvor CC, Odum WE (1988) Food, predation risk, and microhabitat selection in a marsh fish assemblage. Ecology 69:1341–1351

    Article  Google Scholar 

  • McNett BJ, Rypstra AL (2000) Habitat selection in a large orb-weaving spider: vegetational complexity determines site selection and distribution. Ecol Entomol 25:423–432

    Article  Google Scholar 

  • Mittelbach GG (1981) Foraging efficiency and body size: a study of optimal diet and habitat use by bluegills. Ecology 62:1370–1386

    Article  Google Scholar 

  • Montgomery JC, Tolimieri N, Haine OS (2001) Active habitat selection by pre-settlement reef fishes. Fish Fish 2:261–277

    Article  Google Scholar 

  • Moody AL, Houston AI, McNamara JM (1996) Ideal free distributions under predation risk. Behav Ecol Sociobiol 38:131–143

    Article  Google Scholar 

  • Munday PL, Dixson DL, Donelson JM, Jones GP, Pratchett MS, Devitsina GV, Døving KJ (2009) Ocean acidification impairs olfactory discrimination and homing ability of a marine fish. Proc Natl Acad Sci U S A 106:1848–1852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nemeth R (1998) The effect of natural variation in substrate architecture on the survival of juvenile bicolor damselfish. Environ Biol Fish 53:129–141

    Article  Google Scholar 

  • Nicholson MC, Bowyer RT, Kie JG (1997) Habitat selection and survival of mule deer: tradeoffs associated with migration. J Mammal 78:483–504

    Article  Google Scholar 

  • Paul VJ, Cruz-Rivera E, Thacker RW (2001) Chemical mediation of macroalgal herbivore interactions: ecological and evolutionary perspectives. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC Press, Baton rouge, pp 227–265

    Google Scholar 

  • Pawlik JR (1992) Chemical ecology of the settlement of benthic marine invertebrates. Oceanogr Mar Biol 30:273–335

    Google Scholar 

  • Rasher DB, Stout EP, Engel S, Shearer TL, Kubanek J, Hay ME (2015) Marine and terrestrial herbivores display convergent chemical ecology despite 400 million years of independent evolution. Proc Natl Acad Sci U S A 112:12110–12115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Resetarits WJ, Binckley CA (2013) Is the pirate really a ghost? Evidence for generalized chemical camouflage in an aquatic predator, pirate perch Aphredoderus sayanus. Am Nat 181:690–699

    Article  PubMed  Google Scholar 

  • Reynolds PL, Sotka EE (2011) Non-consumptive predator effects indirectly influence marine plant biomass and palatability. J Ecol 99:1272–1281

    Article  Google Scholar 

  • Richardson LR, Yaldwyn JC (1958) A guide to the natant decapod crustacea (shrimps and prawns) of New Zealand. Tuatara 7:17–41

    Google Scholar 

  • Rizzari JR, Frisch AJ, Hoey AS, McCormick MI (2014) Not worth the risk: apex predators suppress herbivory on coral reefs. Oikos 123:829–836

    Article  Google Scholar 

  • Romanuk TN, Kolasa J (2002) Environmental variability alters the relationship between richness and variability of community abundances in aquatic rock pool microcosms. Ecoscience 9:55–62

    Article  Google Scholar 

  • Sotka EE, Hay ME, Thomas JD (1999) Host-plant specialization by a non-herbivorous amphipod: advantages for the amphipod and costs for the seaweed. Oecologia 118:471–482

    Article  Google Scholar 

  • Taylor RB, Cole RG (1994) Mobile epifauna on subtidal brown seaweeds in northeastern New Zealand. Mar Ecol Prog Ser 115:271–282

    Article  Google Scholar 

  • Truchot JP, Duhamel-Jouve A (1980) Oxygen and carbon dioxide in the marine intertidal environment: diurnal and tidal changes in rockpools. Respir Physiol 39:241–254

    Article  CAS  PubMed  Google Scholar 

  • Trussell G, Ewanchuk P, Bertness M, Silliman B (2004) Trophic cascades in rocky shore tide pools: distinguishing lethal and nonlethal effects. Oecologia 139:427–432

    Article  PubMed  Google Scholar 

  • Vail AL, McCormick MI (2011) Metamorphosing reef fishes avoid predator scent when choosing a home. Biol Lett 7:921–924

    Article  PubMed  PubMed Central  Google Scholar 

  • Vaudo JJ, Heithaus MR (2013) Microhabitat selection by marine mesoconsumers in a thermally heterogeneous habitat: behavioral thermoregulation or avoiding predation risk? PLoS ONE 8, e61907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Werner EE, Hall DJ (1988) Ontogenetic habitat shifts in bluegill: the foraging rate-predation risk trade-off. Ecology 69:1352–1366

    Article  Google Scholar 

  • Winnie J, Creel S (2007) Sex-specific behavioural responses of elk to spatial and temporal variation in the threat of wolf predation. Anim Behav 73:215–225

    Article  Google Scholar 

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Authors and Affiliations

  1. School of Marine Science and Policy, University of Delaware, Lewes, DE, 19958, USA

    Rohan M. Brooker & Danielle L. Dixson

  2. School of Biology, Georgia Institute of Technology, Atlanta, GA, 30318, USA

    Rohan M. Brooker & Danielle L. Dixson

  3. School of Marine Science and Policy, University of Delaware, Newark, DE, 19716, USA

    Danielle L. Dixson

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  1. Rohan M. Brooker
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  2. Danielle L. Dixson
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Correspondence to Danielle L. Dixson.

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Communicated by T. Breithaupt

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Brooker, R.M., Dixson, D.L. Intertidal crustaceans use seaweed-derived chemical cues to mitigate predation risk. Behav Ecol Sociobiol 71, 47 (2017). https://doi.org/10.1007/s00265-017-2275-7

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  • DOI: https://doi.org/10.1007/s00265-017-2275-7

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