Skip to main content

Advertisement

SpringerLink
Log in

Relative importance of habitat attributes to predation risk in a temperate reef fish

  • Published:
Environmental Biology of Fishes Aims and scope Submit manuscript

Abstract

Complex habitats serve as a refuge by impeding predator movement and the detection and capture of prey. The attributes that make up these habitats often covary and are difficult to evaluate. The purpose of our study was to understand how attributes of habitat structure contribute to the survival of a temperate rocky reef fish, the bluebanded goby, Lythrypnus dalli. We first used natural substrata (rock) and then artificial standardized habitat units (SHUs) to explore attributes that likely reduce predation of L. dalli. Survival was positively related to the size of rock, but multiple attributes covaried, including rugosity, interstitial space between rocks, total surface area, rock height, and the number of rocks per plot. Using SHUs, we manipulated gap distance (to limit predator access) and potential refuge volume (interstitial space) orthogonally between artificial ‘rocks’ while controlling other habitat attributes. Degree of predator access (PA) was more influential on survival of individuals when combined with low interstitial space (IS) than high, but a combination of low IS and low PA was necessary for consistently high survival. We also conducted a behavioral laboratory experiment to ascertain whether the distribution of L. dalli among configurations of habitat differed in the presence and absence of an important predator, the kelp bass, Paralabrax clathratus. Individuals selected habitat configurations with low spacing between structures, consistent with survival patterns observed in the field. Our study indicates that habitat attributes vary in their importance to survival, but their combined effects may be greater than those of any single attribute.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aguirre JD, McNaught DC (2011) Habitat modification affects recruitment of abalone in Central New Zealand. Mar Biol 158:505–513

    Article  Google Scholar 

  • Allen LG, Bouvier LS, Jensen RE (1992) Abundance, diversity, and seasonality of cryptic fishes and their contribution to a temperate reef fish assemblage off Santa Catalina Island, California. Bull South Calif Acad Sci 91:55–69

    Google Scholar 

  • Almany GA (2004) Differential effects of habitat complexity, predators and competitors on abundance of juvenile and adult coral reef fishes. Oecologia 141:105–113

    Article  PubMed  Google Scholar 

  • Alvarez-Filip L, Dulvy NK, Gill JA, Cote IM, Watkinson AR (2009) Flattening of Caribbean coral reefs: region-wide declines in architectural complexity. P Roy Soc B-Biol Sci 276:3019–3025

    Article  Google Scholar 

  • Anderson TW (2001) Predator responses, prey refuges, and density-dependent mortality of a marine fish. Ecology 82:245–257

    Article  Google Scholar 

  • Bartholomew A (2002a) Faunal colonization of artificial seagrass plots: the importance of surface area versus space size relative to body size. Estuaries 25:1045–1052

    Article  Google Scholar 

  • Bartholomew A (2002b) Total cover and cover quality: predicted and actual effects on a predator’s foraging success. Mar Ecol Prog Ser 227:1–9

    Article  Google Scholar 

  • Bartholomew A, Diaz RJ, Cicchetti G (2000) New dimensionless indices of structural habitat complexity: predicted and actual effects on a predator’s foraging success. Mar Ecol Prog Ser 206:45–58

    Article  Google Scholar 

  • Behrents KC (1983) The comparative ecology and interactions between two sympatric gobies (Lythrypnus dalli and Lythrypnus zebra). University of Southern California, Dissertation

    Google Scholar 

  • Behrents KC (1987) The influence of shelter availability on recruitment and early juvenile survivorship of Lythrypnus dalli Gilbert (Pisces: Gobiidae). J Exp Mar Biol Ecol 107:45–59

    Article  Google Scholar 

  • Bell SS, McCoy ED, Mushinsky HR (1991) Habitat structure: the physical arrangement of objects in space. Chapman and Hall, London

    Book  Google Scholar 

  • Bell SS, Brooks RA, Ellis WE (2003) Structural spading and the determination of habitat complexity: examining the Bartholomew et al. (2000) index. Mar Ecol Prog Ser 248:293–295

    Article  Google Scholar 

  • Beukers JS, Jones GP (1997) Habitat complexity modifies the impact of piscivores on a coral reef fish population. Oecologia 114:50–59

    Article  Google Scholar 

  • Booth DJ, Brosnan DM (1995) The role of recruitment dynamics in rocky shore and coral reef fish communities. Adv Ecol Res 26:309–385

    Article  Google Scholar 

  • Brunton BJ, Booth DJ (2003) Density- and size-dependent mortality of a settling coral-reef damselfish (Pomacentrus moluccensis Bleeker). Oecologia 137:377–384

    Article  PubMed  Google Scholar 

  • Caley MJ, St John J (1996) Refuge availability structures assemblages of tropical reef fishes. J Anim Ecol 65:414–428

    Article  Google Scholar 

  • Chalfoun AD, Martin TE (2009) Habitat structure mediates predation risk for sedentary prey: experimental tests of alternative hypotheses. J Anim Ecol 78:497–503

    Article  PubMed  Google Scholar 

  • Claudet J, Pelletier D (2004) Marine protected areas and artificial reefs: a review of the interactions between management and scientific studies. Aquat Living Resour 17:129–138. doi:10.1051/alr:2004017

    Article  Google Scholar 

  • Claudet et al. (2008) Marine reserves: size and age do matter. Ecol Lett 11:481–489. doi:10.1111/j.1461-0248.2008.01166.x

    Article  PubMed  Google Scholar 

  • Connell SD, Jones GP (1991) The influence of habitat complexity on postrecruitment processes in a temperate reef fish population. J Exp Mar Biol Ecol 151:271–294

    Article  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 

  • Dickman CR (1992) Predation and habitat shift in the house mouse, Mus domesticus. Ecology 73:313–322

    Article  Google Scholar 

  • Downes BJ, Lake PS, Schreiber ESG, Glaister A (1998) Habitat structure and regulation of local species diversity in a stony, upland stream. Ecol Monogr 68:237–257

    Article  Google Scholar 

  • Dunn DC, Halpin PN (2009) Rugosity-based regional modeling of hard-bottom habitat. Mar Ecol Prog Ser 377:1–11

    Article  Google Scholar 

  • Forrester GE, Steele MA (2000) Variation in the presence and cause of density-dependent mortality in three species of reef fishes. Ecology 81:2416–2427

    Article  Google Scholar 

  • Forrester GE, Steele MA (2004) Predators, prey refuges, and the spatial scaling of density-dependent mortality. Ecology 85:1332–1342

    Article  Google Scholar 

  • García-Charton JA, Pérez-Ruzafa A (1998) Correlation between habitat structure and a rocky reef fish assemblage in the southwestern Mediterranean. Mar Ecol 19:111–128

    Article  Google Scholar 

  • García-Charton JA, Pérez-Ruzafa A (1999) Ecological heterogeneity and the evaluation of the effects of marine reserves. Fish Res 42:1–20

    Article  Google Scholar 

  • García-Charton JA, Pérez-Ruzafa A (2001) Spatial pattern and the habitat structure of a Mediterranean rocky reef fish local assemblage. Mar Biol 138:917–934

    Article  Google Scholar 

  • García-Charton JA, Pérez-Ruzafa A, Sánchez-Jerez P, Bayle-Sempere JT, Reñones O, Moreno D (2004) Multi-scale spatial heterogeneity, habitat structure, and the effect of marine reserves on western Mediterranean rocky reef fish assemblages. Mar Biol 144:161–182

    Article  Google Scholar 

  • Gilbert CH (1890) A preliminary report on the fishes collected by the streamer ‘albatross’ on the Pacific coast of North America during the year 1989, with descriptions of twelve new general and ninety-two new species. Proc US Natl Mus 13:49–126

    Article  Google Scholar 

  • Gotceitas V, Colgan P (1989) Predator foraging success and habitat complexity: quantitative test of the threshold hypothesis. Oecologia 80:158–166

    Article  Google Scholar 

  • Guidetti P, Verginella L, Viva C, Odorico R, Boero F (2005) Protection effects on fish assemblages, and comparison of two visual-census techniques in shallow artificial rocky habitats in the northern Adriatic Sea. J Mar Biol Assoc UK 85:247–255

    Article  Google Scholar 

  • Guidetti et al. (2008) Italian marine reserve effectiveness: does enforcement matter? Biol Conserv 141:699–709. doi:10.1016/j.biocon.2007.12.013

    Article  Google Scholar 

  • Gullström M, Berkström C, Öhman M, Bodin M, Dahlberg M (2011) Scale-dependent patterns of variability of a grazing parrotfish (Leptoscarus vaigiensis) in a tropical seagrass-dominated seascape. Mar Biol 158:1483–1495

    Article  Google Scholar 

  • Hackradt CW, Felix-Hackradt FC, García-Charton JA (2011) Influence of habitat structure on fish assemblage of an artificial reef in southern Brazil. Mar Environ Res 72:235–247

    Article  CAS  PubMed  Google Scholar 

  • Harrell WC, Fuhlendorf SD (2002) Evaluation of habitat structural measures in a shrubland community. J Range Manag 55:488–493

    Article  Google Scholar 

  • Hartney KB, Grorud KA (2002) The effect of sea urchins as biogenic structures on the local abundance of a temperate reef fish. Oecologia 131:506–513

    Article  Google Scholar 

  • Heck KL Jr, Wetstone GS (1977) Habitat complexity and invertebrate species richness and abundance in tropical seagrass meadows. J Biogeogr 4:135–142

    Article  Google Scholar 

  • Hixon MA, Beets JP (1993) Predation, prey refuges, and the structure of coral-reef assemblages. Ecology 63:77–101

    Google Scholar 

  • Hovel KA, Lipcius RN (2001) Habitat fragmentation in a seagrass landscape: patch size and complexity control blue crab survival. Ecology 82:1814–1829

    Article  Google Scholar 

  • Humphries AT, La Peyre MK, Decossas GA (2011) The effect of structural complexity, prey density, and “predator-free space” on prey survivorship at created oyster reef mesocosms. PLoS One. doi:10.1371/journal.pone.0028339

    Google Scholar 

  • Johnson DW (2006) Predation, habitat complexity, and variation in density-dependent mortality of temperate reef fishes. Ecology 87:1179–1188

    Article  PubMed  Google Scholar 

  • Johnson DW (2007) Habitat complexity modifies post-settlement mortality and recruitment dynamics of a marine fish. Ecology 88:1716–1725

    Article  PubMed  Google Scholar 

  • Jones GP (1988) Experimental evaluation of the effects of habitat structure and competitive interactions on the juveniles of two coral reef fishes. J Exp Mar Biol Ecol 123:115–126

    Article  Google Scholar 

  • Kopp K, Wachlevski M, Eterovick PC (2006) Environmental complexity reduces tadpole predation by water bugs. Can J Zool 84:136–140

    Article  Google Scholar 

  • Kovalenko KE, Thomaz SM, Warfe DM (2012) Habitat complexity: approaches and future directions. Hydrobiologia 685:1–17

    Article  Google Scholar 

  • Kuffner IB, Brock JC, Grober-Dunsmore R, Bonito VE, Hickey TD, Wright CW (2007) Relationships between reef fish communities and remotely sensed rugosity measurements in Biscayne National Park, Florida, USA. Environ Biol Fish 78:71–82

    Article  Google Scholar 

  • Levin PS (1993) Habitat structure, conspecific presence and spatial variation in the recruitment of a temperate reef fish. Oecologia 94:176–185

    Article  Google Scholar 

  • Lubchenco J, Palumbi SR, Gaines SD, Andelman S (2003) Plugging a hole in the ocean: the emerging science of marine reserves. Ecol Appl 13:S3–S7

    Article  Google Scholar 

  • Malone JC, Forrester GE, Steele MA (1999) Effects of subcutaneous microtags on the growth, survival, and vulnerability to predation of small reef fishes. J Exp Mar Biol Ecol 237:243–253

    Article  Google Scholar 

  • Manatunge J, Asaeda T, Priyadarshana T (2000) The influence of structural complexity on fish-zooplankton interactions: a study using artificial submerged macrophytes. Environ Biol Fish 58:425–438

    Article  Google Scholar 

  • Mandelik Y, Jones M, Dayan T (2003) Structurally complex habitat and sensory adaptations mediate the behavioural responses of a desert rodent to an indirect cue for increased predation risk. Evol Ecol Res 5:501–515

    Google Scholar 

  • Mattila J, Heck KL Jr, Millstein E, Miller E, Gustafsson C, Williams S, Byron D (2008) Increased habitat structure does not always provide increased refuge from predation. Mar Ecol Prog Ser 361:15–20. doi:10.3354/meps07392

    Article  Google Scholar 

  • McClanahan TR, Arthur R (2001) The effect of marine reserves and habitat on populations of east African coral reef fishes. Ecol Appl 11:559–569

    Article  Google Scholar 

  • McCoy ED, Bell SS (1991) Habitat structure: the evolution and diversification of a complex topic. In: Bell SS, McCoy ED, Mushinsky HR (eds) Habitat structure: the physical arrangement of objects in space. Chapman and Hall, London, pp. 281–299

    Google Scholar 

  • McElhinny C, Gibbons P, Brack C, Bauhus J (2005) Forest and woodland stand structural complexity: its definition and measurement. For Ecol Manag 218:1–24. doi:10.1016/j.foreco.2005.08.034

    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 

  • Miller DJ, Lea RN (1972) Guide to the coastal marine fishes of California; California fish bulletin number 157. Calif Dept Fish Game, Sacramento

    Google Scholar 

  • Moksnes PO, Heck KL Jr (2006) Relative importance of habitat selection and predation for the distribution of blue crab megalopae and young juveniles. Mar Ecol Prog Ser 308:165–181

    Article  Google Scholar 

  • Monaco ME, Friedlander AM, Caldow C, Christensen JD, Rogers C, Beets J, Miller J, Boulon R (2007) Characterising reef fish populations and habitats within and outside the US Virgin Islands coral reef National Monument: a lesson in marine protected area design. Fish Manag Ecol 14:33–40

    Article  Google Scholar 

  • Moore EC, Hovel KA (2010) Relative influence of habitat complexity and proximity to patch edges on seagrass epifaunal communities. Oikos 119:1299–1311

    Article  Google Scholar 

  • Nagelkerken I, De Schryver AM, Verweij MC, Dahdouh-Guebas F, Van Der Velde G, Koedam N (2010) Differences in root architecture influence attraction of fishes to mangroves: a field experiment mimicking roots of different length, orientation, and complexity. J Exp Mar Biol Ecol 396:27–34

    Article  Google Scholar 

  • Osenberg CW, St. Mary CM, Wilson JA, Lindberg WJ (2002) A quantitative framework to evaluate the attraction-production controversy. ICES J Mar Sci 59:S214–S221. doi:10.1006/jmsc.2002.1222

    Article  Google Scholar 

  • Pirtle JL, Stoner AW (2010) Red king crab (Paralithodes camtschaticus) early post-settlement habitat choice: structure, food, and ontogeny. J Exp Mar Biol Ecol 393:130–137

    Article  Google Scholar 

  • Rilov G, Figueira WF, Lyman SJ, Crowder LB (2007) Complex habitats may not always benefit prey: linking visual field with reef fish behavior and distribution. Mar Ecol Prog Ser 329:225–238

    Article  Google Scholar 

  • Risk MJ (1972) Fish diversity on a coral reef in the Virgin Islands. Atoll Res Bull 153:1–6

    Article  Google Scholar 

  • Ryer CH, Stoner AW, Titgen RH (2004) Behavioral mechanisms underlying the refuge value of benthic habitat structure for two flatfishes with differing anti-predator strategies. Mar Ecol Prog Ser 268:231–243

    Article  Google Scholar 

  • Scharf FS, Manderson JP, Fabrizio MC (2006) The effects of seafloor habitat complexity on survival of juvenile fishes: species-specific interactions with structural refuge. J Exp Mar Biol Ecol 335:167–176

    Article  Google Scholar 

  • Schmitt RJ, Holbrook SJ (1985) Patch selection by juvenile black surfperch (Embiotocidae) under variable risk: interactive influence of food quality and structural complexity. J Exp Mar Biol Ecol 85:269–285

    Article  Google Scholar 

  • Schofield P (2003) Habitat selection of two gobies (Microgobius gulosus, Gobiosoma robustum): influence of structural complexity, competitive interactions, and presence of a predator. J Exp Mar Biol Ecol 288:125–137

    Article  Google Scholar 

  • Sebens KP (1991) Habitat structure and community dynamics in marine benthic systems. In: Bell SS, McCoy ED, Mushinsky HR (eds) Habitat structure, the physical arrangement of objects in space. Chapman and Hall, New York, pp. 211–233

    Chapter  Google Scholar 

  • Shima JS, Osenberg CW (2003) Cryptic density dependence: effects of covariation between density and site quality in reef fish. Ecology 84:46–52

    Article  Google Scholar 

  • Shima JS, Osenberg CW, St Mary CM (2008) Quantifying site quality in a heterogeneous landscape: recruitment of a reef fish. Ecology 89:86–94

    Article  PubMed  Google Scholar 

  • Shoji J, Sakiyama K, Hori M, Yoshida G, Hamaguchi M (2007) Seagrass habitat reduces vulnerability of red sea bream Pagrus major juveniles to piscivorous fish predator. Fish Sci 73:1281–1285

    CAS  Google Scholar 

  • Shumway CA, Hofmann HA, Dobberfuhl AP (2007) Quantifying habitat complexity in aquatic ecosystems. Freshw Biol 52:1065–1076. doi:10.1111/j.1365-2427.2007.01754.x

    Article  Google Scholar 

  • Sih A (1997) To hide or not to hide? Refuge use in a fluctuating environment. Trends Ecol Evol 12:375–376. doi:10.1016/S0169-5347(97)87376-4

    Article  CAS  PubMed  Google Scholar 

  • St Mary CM (1997) Sequential patterns of sex allocation in simultaneous hermaphrodites: do we need models that specifically incorporate this complexity? Am Nat 150:73–97

    Article  CAS  PubMed  Google Scholar 

  • Steele MA (1996) Effects of predators on reef fishes: separating cage artifacts from effects of predation. J Exp Mar Biol Ecol 198:249–267

    Article  Google Scholar 

  • Steele MA (1997a) The relative importance of processes affecting recruitment of two temperate reef fishes. Ecology 78:129–145

    Article  Google Scholar 

  • Steele MA (1997b) Population regulation by post-settlement mortality in two temperate reef fishes. Oecologia 112:64–74

    Article  Google Scholar 

  • Steele MA (1998) The relative importance of predation and competition in two reef fishes. Oecologia 115:222–232

    Article  Google Scholar 

  • Steele MA (1999) Effects of shelter and predators on reef fishes. J Exp Mar Biol Ecol 233:65–79

    Article  Google Scholar 

  • Tupper M, Boutilier RG (1997) Effects of habitat on settlement, growth, predation risk and survival of a temperate reef fish. Mar Ecol Prog Ser 151:225–236

    Article  Google Scholar 

  • Verdonschot RCM, Peeters ETHM (2012) Preference of larvae of Enallagma cyathigerum (Odonata: Coenagrionidae) for habitats of varying structural complexity. Eur J Entomol 109:229–234

    Article  Google Scholar 

  • Walker BK, Jordan LKB, Spieler RE (2009) Relationship of reef fish assemblages and topographic complexity on southeastern Florida Coral reef habitats. J Coast Res 53:39–58

    Article  Google Scholar 

  • Warfe DM, Barmuta LA (2004) Habitat structural complexity mediates the foraging success of multiple predator species. Oecologia 141:171–178

    Article  PubMed  Google Scholar 

  • Warfe DM, Barmuta LA, Wotherspoon S (2008) Quantifying habitat structure: surface convolution and living space for species in complex environments. Oikos 117:1764–1773

    Article  Google Scholar 

  • Warner RR, Swearer SE, Caselle JE (2000) Larval accumulation and retention: implications for the design of marine reserves and essential fish habitat. B Mar Sci 66:821–830

    Google Scholar 

  • Werner EE, Gilliam JF, Hall DJ, Mittelbach GG (1983) An experimental test of the effects of predation risk on habitat use in fish. Ecology 64:1540–1548

    Article  Google Scholar 

  • Williams SE, Marsh H, Winter J (2002) Spatial scale, species diversity, and habitat structure: small mammals in Australian tropical rain forest. Ecology 83:1317–1329

    Article  Google Scholar 

Download references

Acknowledgments

We thank S. Boom, E. Floyd, N. Bakkour, and J. Young for their tireless assistance in the field, D. Deutschman and M. Edwards for statistical advice, and B. Hentschel and J. Mahaffy for reviewing the manuscript. We especially thank K.A. Miller for her logistical support, C. Gramlich for her patience and diving expertise, and J. Zimmer for his proficiency in construction of materials. This study was funded through a graduate internship at the Wrigley Marine Science Center (to C.A.G.) and by a scholarship from the San Diego, California chapter of Achievement Rewards for College Scientists (to C.A.G.). Additional support was provided by grants to T.W.A. from the National Undersea Research Program, West Coast and Polar Regions Center (UAF(CA)-03-02), the National Institute for Undersea Science and Technology (05-07-006), and the National Science Foundation (OCE-0331895). We cite permission to collect and utilize study organisms from the California Department of Fish and Wildlife and commitment to ethical procedures required by CDFW and San Diego State University at the time this research was conducted. Contribution No. 253 of the University of Southern California Wrigley Institute for Environmental Studies.

Author information

Authors and Affiliations

  1. Department of Biology and Coastal and Marine Institute, San Diego State University, San Diego, California, 92182-4614, USA

    Christine A. Gregor & Todd W. Anderson

  2. San Diego State University, 5500 Campanile Dr, San Diego, CA, 92182-4614, USA

    Todd W. Anderson

Authors
  1. Christine A. Gregor
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Todd W. Anderson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Todd W. Anderson.

Appendix

Appendix

ᅟ

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gregor, C.A., Anderson, T.W. Relative importance of habitat attributes to predation risk in a temperate reef fish. Environ Biol Fish 99, 539–556 (2016). https://doi.org/10.1007/s10641-016-0496-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10641-016-0496-7

Keywords

Search

Navigation