Skip to main content
Log in

Habitat complexity impacts persistence and species interactions in an intertidal whelk

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Although experiments have shown that habitat structure may influence the distribution of species and species interactions, these effects are still not commonly integrated into studies of community dynamics. Since habitat structure often varies within and among communities, this may limit our understanding of how various factors influence communities. Here, we examined how mussel bed complexity (the presence and thickness of mussel layers) influenced the persistence of whelks (Nucella emarginata) and interactions with a top predator (ochre sea stars, Pisaster ochraceus) and prey (mussels, Mytilus californianus). Results from a mark–recapture experiment indicate that whelk recapture rates are higher in more complex habitats, and laboratory experiments demonstrate that habitat complexity affects whelk feeding, growth, and nonconsumptive interactions with a keystone predator. Habitat complexity therefore has direct effects on species and also may lead to trade-offs among feeding, refuge, and other factors, potentially influencing the distribution of whelks and the effects of both whelks and sea stars on intertidal communities. These results demonstrate that habitat structure may play an important role in intertidal communities and other habitats and should be further considered in the experimental design of future studies of community dynamics.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Baber MJ, Babbitt KJ (2004) Influence of habitat complexity on predator–prey interactions between the fish (Gambusia holbrooki) and tadpoles of Hyla squirella and Gastrophryne carolinensis. Copeia 2004:173

    Article  Google Scholar 

  • Beck MW (2000) Separating the elements of habitat structure: independent effects of habitat complexity and structural components on rocky intertidal gastropods. J Exp Mar Biol Ecol 249:29–49

    Article  Google Scholar 

  • Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White J-SS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135

    Article  Google Scholar 

  • Borthagaray AI, Carranza A (2007) Mussels as ecosystem engineers: their contribution to species richness in a rocky littoral community. Acta Oecol 31:243–250

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trends Ecol Evol 18:119–125

    Article  Google Scholar 

  • Buschbaum C, Dittmann S, Hong J-S, Hwang I-S, Strasser M, Thiel M, Valdivia N, Yoon S-P, Reise K (2008) Mytilid mussels: global habitat engineers in coastal sediments. Helgol Mar Res 63:47–58

    Article  Google Scholar 

  • Connell JH (1961) Influence of interspecific competition and other factors on distribution of barnacle Chthamalus stellatus. Ecology 42:710–723

    Article  Google Scholar 

  • Crawley MJ (2007) The R book, 1st edn. Wiley, West Sussex

    Book  Google Scholar 

  • Crowder LB, Cooper WE (1982) Habitat structural complexity and the interaction between bluegills and their prey. Ecology 63:1802–1813

    Article  Google Scholar 

  • Davenport J, Moore P, LeComte E (1996) Observations on defensive interactions between predatory dogwhelks, Nucella lapillus (L) and mussels, Mytilus edulis L. J Exp Mar Biol Ecol 206:133–147

    Article  Google Scholar 

  • Day R, Barkai A, Wickens P (1991) Trapping of 3 drilling whelks by 2 species of mussel. J Exp Mar Biol Ecol 149:109–122

    Article  Google Scholar 

  • Diehl S (1992) Fish predation and benthic community structure: the role of omnivory and habitat complexity. Ecology 73:1646

    Article  Google Scholar 

  • Eklov P, Werner EE (2000) Multiple predator effects on size-dependent behavior and mortality of two species of anuran larvae. Oikos 88:250–258

    Article  Google Scholar 

  • Ferner MC, Smee DL, Weissburg MJ (2009) Habitat complexity alters lethal and non-lethal olfactory interactions between predators and prey. Mar Ecol Prog Ser 374:13–22

    Article  Google Scholar 

  • Firstater FN, Hidalgo FJ, Lomovasky BJ, Ramos E, Gamero P, Iribarne OO (2010) Habitat structure is more important than nutrient supply in modifying mussel bed assemblage in an upwelling area of the Peruvian coast. Helgol Mar Res 65:187–196

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Gingold R, Mundo-Ocampo M, Holovachov O, Rocha-Olivares A (2010) The role of habitat heterogeneity in structuring the community of intertidal free-living marine nematodes. Mar Biol 157:1741–1753

    Article  Google Scholar 

  • Gosnell JS, Gaines SD (2012) Keystone intimidators in the intertidal: non-consumptive effects of a keystone sea star regulate feeding and growth in whelks. Mar Ecol Prog Ser 450:107–114

    Article  Google Scholar 

  • Grabowski JH (2004) Habitat complexity disrupts predator-prey interactions but not the trophic cascade on oyster reefs. Ecology 85:995–1004

    Article  Google Scholar 

  • Grabowski JH, Hughes AR, Kimbro DL (2008) Habitat complexity influences cascading effects of multiple predators. Ecology 89:3413–3422

    Article  Google Scholar 

  • Griffin JN, Jenkins SR, Gamfeldt L, Jones D, Hawkins SJ, Thompson RC (2009) Spatial heterogeneity increases the importance of species richness for an ecosystem process. Oikos 118:1335–1342

    Article  Google Scholar 

  • Holt RD, Grover J, Tilman D (1994) Simple rules for interspecific dominance in systems with exploitative and apparent competition. Am Nat 144:741–771

    Article  Google Scholar 

  • Irlandi EA (1994) Large- and small-scale effects of habitat structure on rates of predation: how percent coverage of seagrass affects rates of predation and siphon nipping on an infaunal bivalve. Oecologia 98:176–183

    Article  Google Scholar 

  • Kohn AJ, Leviten PJ (1976) Effect of habitat complexity on population density and species richness in tropical intertidal predatory gastropod assemblages. Oecologia 25:199–210

    Article  Google Scholar 

  • Koivisto ME, Westerbom M (2010) Habitat structure and complexity as determinants of biodiversity in blue mussel beds on sublittoral rocky shores. Mar Biol 157:1463–1474

    Article  Google Scholar 

  • Langellotto G, Denno R (2004) Responses of invertebrate natural enemies to complex-structured habitats: a meta-analytical synthesis. Oecologia 139:1–10

    Article  Google Scholar 

  • Lubchenco J (1978) Plant species diversity in a marine intertidal community: importance of herbivore food preference and algal competitive abilities. Am Nat 112:23–39

    Article  Google Scholar 

  • McConnell CL (2003) Individual Feeding Behavior of a Marine Gastropod, Nucella emarginata, in Southern California. Master thesis, University of California, Los Angeles

  • Menge BA (2000) Recruitment vs. postrecruitment processes as determinants of barnacle population abundance. Ecol Monogr 70:265–288

    Article  Google Scholar 

  • Menge BA, Lubchenco J, Ashkenas LR (1985) Diversity, heterogeneity and consumer pressure in a tropical rocky intertidal community. Oecologia 65:394–405

    Article  Google Scholar 

  • Menge BA, Berlow EL, Blanchette CA, Navarrete SA, Yamada SB (1994) The keystone species concept—variation in interaction strength in a rocky intertidal habitat. Ecol Monogr 64:249–286

    Article  Google Scholar 

  • Menge BA, Blanchette C, Raimondi P, Freidenburg T, Gaines S, Lubchenco J, Lohse D, Hudson G, Foley M, Pamplin J (2004) Species interaction strength: testing model predictions along an upwelling gradient. Ecol Monogr 74:663–684

    Article  Google Scholar 

  • Navarrete SA (1996) Variable predation: effects of whelks on a mid-intertidal successional community. Ecol Monogr 66:301

    Article  Google Scholar 

  • Navarrete SA, Menge BA (1996) Keystone predation and interaction strength: interactive effects of predators on their main prey. Ecol Monogr 66:409–429

    Article  Google Scholar 

  • Norling P, Kautsky N (2008) Patches of the mussel Mytilus sp are islands of high biodiversity in subtidal sediment habitats in the Baltic Sea. Aquat Biol 4:75–87

    Google Scholar 

  • O’Donnell M (2008) Reduction of wave forces within bare patches in mussel beds. Mar Ecol Prog Ser 362:157–167

    Article  Google Scholar 

  • Paine RT (1966) Food web complexity and species diversity. Am Nat 100:65–75

    Article  Google Scholar 

  • Paine RT (1974) Intertidal community structure—experimental studies on relationship between a dominant competitor and its principal predator. Oecologia 15:93–120

    Article  Google Scholar 

  • Paine RT (1976) Size-limited predation: an observational and experimental approach with the Mytilus-Pisaster interaction. Ecology 57:858

    Article  Google Scholar 

  • Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42

    Article  CAS  Google Scholar 

  • Petes LE, Mouchka ME, Milston-Clements RH, Momoda TS, Menge BA (2008) Effects of environmental stress on intertidal mussels and their sea star predators. Oecologia 156:671–680

    Article  Google Scholar 

  • Petraitis PS (1987) Immobilization of the predatory gastropod, Nucella lapillus, by its prey, Mytilus edulis. Biol Bull 172:307–314

    Article  Google Scholar 

  • Pincebourde S, Sanford E, Helmuth B (2008) Body temperature during low tide alters the feeding performance of a top intertidal predator. Limnol Oceanogr 53:1562–1573

    Article  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, R Development Core Team (2010) nlme: linear and nonlinear mixed effects models

  • Preisser EL, Bolnick DI (2008) The many faces of fear: comparing the pathways and impacts of nonconsumptive predator effects on prey populations. PLoS ONE 3:e2465

  • R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  • Relyea RA (2003) How prey respond to combined predators: a review and an empirical test. Ecology 84:1827–1839

    Article  Google Scholar 

  • Robles CD, Desharnais RA, Garza C, Donahue MJ, Martinez CA (2009) Complex equilibria in the maintenance of boundaries: experiments with mussel beds. Ecology 90:985–995

    Article  Google Scholar 

  • Robles CD, Garza C, Desharnais RA, Donahue MJ (2010) Landscape patterns in boundary intensity: a case study of mussel beds. Landsc Ecol 25:745–759

    Article  Google Scholar 

  • Sanders D, Nickel H, Grützner T, Platner C (2008) Habitat structure mediates top-down effects of spiders and ants on herbivores. Basic Appl Ecol 9:152–160

    Article  Google Scholar 

  • Sanford E (1999) Regulation of keystone predation by small changes in ocean temperature. Science 283:2095–2097

    Article  CAS  Google Scholar 

  • Sanford E (2002a) Water temperature, predation, and the neglected role of physiological rate effects in rocky intertidal communities. Integr Comp Biol 42:881–891

    Article  Google Scholar 

  • Sanford E (2002b) The feeding, growth, and energetics of two rocky intertidal predators (Pisaster ochraceus and Nucella canaliculata) under water temperatures simulating episodic upwelling. J Exp Mar Biol Ecol 273:199–218

    Article  Google Scholar 

  • Smith JR, Fong P, Ambrose RF (2006) Long-term change in mussel (Mytilus californianus Conrad) populations along the wave-exposed coast of southern California. Mar Biol 149:537–545

    Article  Google Scholar 

  • Suchanek TH (1994) Temperate coastal marine communities: biodiversity and threats. Am Zool 34:100–114

    Google Scholar 

  • Tokeshi M, Romero L (1995) Filling a gap: dynamics of space occupancy on a mussel-dominated subtropical rocky shore. Mar Ecol Prog Ser 119:167–176

    Article  Google Scholar 

  • Trussell GC (1997a) Phenotypic selection in an intertidal snail: effects of a catastrophic storm. Mar Ecol Prog Ser 151:73–79

    Article  Google Scholar 

  • Trussell GC (1997b) Phenotypic plasticity in the foot size of an intertidal snail. Ecology 78:1033–1048

    Article  Google Scholar 

  • Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin JM, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395

    Article  CAS  Google Scholar 

  • Warton D, Hui F (2010) The arcsine is asinine: the analysis of proportions in ecology. Ecology 92:3–10

    Article  Google Scholar 

  • Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New York

    Google Scholar 

  • Wieters EA, Salles E, Januario SM, Navarrete SA (2009) Refuge utilization and preferences between competing intertidal crab species. J Exp Mar Biol Ecol 374:37–44

    Article  Google Scholar 

  • Wilkinson EB, Feener DH (2007) Habitat complexity modifies ant-parasitoid interactions: implications for community dynamics and the role of disturbance. Oecologia 152:151–161

    Article  Google Scholar 

  • Zuur AF (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

Download references

Acknowledgments

We would like to thank Jessica Beatty, Jennifer Chiu, James Jelks, Kylie Langlois, Teal Riege, Taylor Scott, and Louise Stevenson for their aid in completing this project. Input from Sarah Teck and Elizabeth Hoaglund improved the project and manuscript, as did input from two anonymous reviewers.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J. Stephen Gosnell.

Additional information

Communicated by F. Bulleri.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stephen Gosnell, J., DiPrima, J.B. & Gaines, S.D. Habitat complexity impacts persistence and species interactions in an intertidal whelk. Mar Biol 159, 2867–2874 (2012). https://doi.org/10.1007/s00227-012-2047-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-012-2047-x

Keywords

Navigation