Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Predation as a driver of gastropod distribution in north-eastern New Zealand kelp forests

Debbie J. Freeman A B D and Robert G. Creese A C
+ Author Affiliations
- Author Affiliations

A Leigh Marine Laboratory, University of Auckland, PO Box 349, Warkworth 0941, New Zealand.

B Present address: Department of Conservation, Research and Development Group, PO Box 10-420, Wellington 6143, New Zealand.

C Present address: Port Stephens Fisheries Institute, Locked Bag 1, Nelson Bay, NSW 2315, Australia.

D Corresponding author. Email: dfreeman@doc.govt.nz

Marine and Freshwater Research 62(5) 471-479 https://doi.org/10.1071/MF10259
Submitted: 19 October 2010  Accepted: 1 March 2011   Published: 25 May 2011

Abstract

Gastropods play an important ecological role in kelp forests; however, this role is dependent on where exactly in such communities these animals are located. We assessed the spatial and temporal patterns in the utilisation of available reef and macroalgal substrates by three gastropods in a north-eastern New Zealand kelp (Ecklonia radiata (C. Agardh) J. Agardh, 1848) forest, focusing on predation as a factor influencing these patterns. Although kelp provided a large habitable surface area for gastropods, much of this area was under-utilised. During the day, gastropods on E. radiata were largely confined to the primary laminae. At night, gastropods on the reef migrated into the algal canopy where they occupied regions of the kelp that were not occupied during the day. Over a 36-day period, 93% of the gastropods tethered to the reef were consumed by predators, whereas none tethered in the algal canopy was consumed. We consider that night-time vertical migration and dispersion through the algal canopy may be primarily a response to predation by diurnally feeding fish and nocturnal benthic predators such as lobsters. Our research highlights the importance of considering diel changes in epifaunal distribution and abundance when assessing their ecological role.

Additional keywords: Cantharidus purpureus, Cookia sulcata, distribution, Ecklonia radiata, epifauna, gastropods, kelp, predation, Trochus viridis.


References

Adams, N. M. (1994). ‘Seaweeds of New Zealand.’ (Canterbury University Press: Christchurch, New Zealand.)

Andrew, N. L., and MacDiarmid, A. B. (1991). Interrelations between sea urchins and spiny lobsters in northeastern New Zealand. Marine Ecology Progress Series 70, 211–222.
Interrelations between sea urchins and spiny lobsters in northeastern New Zealand.Crossref | GoogleScholarGoogle Scholar |

Babcock, R. C., Shears, N. T., Alcala, A. C., Barrett, N. S., Edgar, G. J., et al. (2010). Decadal trends in marine reserves reveal differential rates of change in direct and indirect effects. Proceedings of the National Academy of Sciences, USA 107, 18 256–18 261.
Decadal trends in marine reserves reveal differential rates of change in direct and indirect effects.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtl2ktr7E&md5=40b56815a0ec191db62c16d818c53fdaCAS |

Bourdeau, P. E. (2009). Prioritized phenotypic responses to combined predators in a marine snail. Ecology 90, 1659–1669.
Prioritized phenotypic responses to combined predators in a marine snail.Crossref | GoogleScholarGoogle Scholar | 19569380PubMed |

Brown, K. M., and Lodge, D. M. (1993). Gastropod abundance in vegetated habitats: the importance of specifying null models. Limnology and Oceanography 38, 217–225.
Gastropod abundance in vegetated habitats: the importance of specifying null models.Crossref | GoogleScholarGoogle Scholar |

Choat, J. H., and Andrew, N. L. (1986). Interactions amongst species in a guild of subtidal benthic herbivores. Oecologia 68, 387–394.
Interactions amongst species in a guild of subtidal benthic herbivores.Crossref | GoogleScholarGoogle Scholar |

Choat, J. H., and Schiel, D. R. (1982). Patterns of distribution and abundance of large brown algae and invertebrate herbivores in subtidal regions of northern New Zealand. Journal of Experimental Marine Biology and Ecology 60, 129–162.
Patterns of distribution and abundance of large brown algae and invertebrate herbivores in subtidal regions of northern New Zealand.Crossref | GoogleScholarGoogle Scholar |

Christie, H., Jorgensen, N. M., and Norderhaug, K. M. (2007). Bushy or smooth, high or low; importance of habitat architecture and vertical position for distribution of fauna on kelp. Journal of Sea Research 58, 198–208.
Bushy or smooth, high or low; importance of habitat architecture and vertical position for distribution of fauna on kelp.Crossref | GoogleScholarGoogle Scholar |

Christie, H., Norderhaug, K. M., and Fredriksen, S. (2009). Macrophytes as habitat for fauna. Marine Ecology Progress Series 396, 221–233.
Macrophytes as habitat for fauna.Crossref | GoogleScholarGoogle Scholar |

Cole, R. G., and Babcock, R. C. (1996). Mass mortality of a dominant kelp (Laminariales) at Goat Island, northeastern New Zealand. Marine and Freshwater Research 47, 907–911.
Mass mortality of a dominant kelp (Laminariales) at Goat Island, northeastern New Zealand.Crossref | GoogleScholarGoogle Scholar |

Cowles, A., Hewitt, J. E., and Taylor, R. B. (2009). Density, biomass and productivity of small mobile invertebrates in a wide range of coastal habitats. Marine Ecology Progress Series 384, 175–185.
Density, biomass and productivity of small mobile invertebrates in a wide range of coastal habitats.Crossref | GoogleScholarGoogle Scholar |

Creese, R. G. (1988). Ecology of molluscan grazers and their interactions with marine algae in northeastern New Zealand: a review. New Zealand Journal of Marine and Freshwater Research 22, 427–444.
Ecology of molluscan grazers and their interactions with marine algae in northeastern New Zealand: a review.Crossref | GoogleScholarGoogle Scholar |

D’Antonio, C. (1985). Epiphytes on the rocky intertidal red alga Rhodomela larix (Turner) C.Agardh: negative effects on the host and food for herbivores? Journal of Experimental Marine Biology and Ecology 86, 197–218.
Epiphytes on the rocky intertidal red alga Rhodomela larix (Turner) C.Agardh: negative effects on the host and food for herbivores?Crossref | GoogleScholarGoogle Scholar |

Dayton, P. K. (1985). Ecology of kelp communities. Annual Review of Ecology and Systematics 16, 215–245.
Ecology of kelp communities.Crossref | GoogleScholarGoogle Scholar |

Duggins, D. O., Simenstad, C. A., and Estes, J. A. (1989). Magnification of secondary production by kelp detritus in coastal marine ecosystems. Science 245, 170–173.
Magnification of secondary production by kelp detritus in coastal marine ecosystems.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cvjt1agsQ%3D%3D&md5=039d6f1a643454a7b6ad15b77b312e71CAS | 17787876PubMed |

Ebeling, A. W., and Bray, R. N. (1976). Day versus night activity of reef fishes in a kelp forest off Santa Barbara, California. Fishery Bulletin 74, 703–717.

Edgar, G. J. (1990). The influence of plant structure on the species richness, biomass and secondary production of macrofaunal assemblages associated with Western Australian seagrass. Journal of Experimental Marine Biology and Ecology 137, 215–240.
The influence of plant structure on the species richness, biomass and secondary production of macrofaunal assemblages associated with Western Australian seagrass.Crossref | GoogleScholarGoogle Scholar |

Foster, M. S., and Schiel, D. R. (2010). Loss of predators and the collapse of southern California kelp forests: alternatives, explanations and generalizations. Journal of Experimental Marine Biology and Ecology 393, 59–70.
Loss of predators and the collapse of southern California kelp forests: alternatives, explanations and generalizations.Crossref | GoogleScholarGoogle Scholar |

Gaylord, B., Blachette, C. A., and Denny, M. W. (1994). Mechanical consequences of size in wave-swept algae. Ecological Monographs 64, 287–313.
Mechanical consequences of size in wave-swept algae.Crossref | GoogleScholarGoogle Scholar |

Jennings, J. G., and Steinberg, P. D. (1997). Phlorotannins versus other factors affecting epiphyte abundance on the kelp Ecklonia radiata. Oecologia 109, 461–473.
Phlorotannins versus other factors affecting epiphyte abundance on the kelp Ecklonia radiata.Crossref | GoogleScholarGoogle Scholar |

Johnson, C. R., and Mann, K. H. (1986). The importance of plant defense abilities to the structure of subtidal seaweeds communities: the kelp Laminaria longicruris de la Pylaie survives grazing by the snail Lacuna vincta (Montagu) at high population densities. Journal of Experimental Marine Biology and Ecology 97, 231–267.
The importance of plant defense abilities to the structure of subtidal seaweeds communities: the kelp Laminaria longicruris de la Pylaie survives grazing by the snail Lacuna vincta (Montagu) at high population densities.Crossref | GoogleScholarGoogle Scholar |

Jørgensen, N. M., and Christie, H. (2003). Diurnal, horizontal and vertical dispersal of kelp-associated epifauna. Hydrobiologia 503, 69–76.
Diurnal, horizontal and vertical dispersal of kelp-associated epifauna.Crossref | GoogleScholarGoogle Scholar |

Kelly, S., Scott, D., MacDiarmid, A. B., and Babcock, R. C. (2000). Spiny lobster, Jasus edwardsii, recovery in New Zealand marine reserves. Biological Conservation 92, 359–369.
Spiny lobster, Jasus edwardsii, recovery in New Zealand marine reserves.Crossref | GoogleScholarGoogle Scholar |

Klumpp, D. W., Salita-Espinosa, J. S., and Fortes, M. D. (1992). The role of epiphytic periphyton and macroinvertebrate grazers in the trophic flux of a tropical seagrass community. Aquatic Botany 43, 327–349.
The role of epiphytic periphyton and macroinvertebrate grazers in the trophic flux of a tropical seagrass community.Crossref | GoogleScholarGoogle Scholar |

Leber, K. M. (1985). The influence of predatory decapods, refuge and microhabitat selection on seagrass communities. Ecology 66, 1951–1964.
The influence of predatory decapods, refuge and microhabitat selection on seagrass communities.Crossref | GoogleScholarGoogle Scholar |

Lonhart, S. I. (2002). Diel vertical migration of the gastropod Norrisia norrisi on the kelp Macrocystis pyrifera. In ‘Proceedings of the Fifth California Islands Symposium’. (Eds D. H. Browne, H. Chaney and K. Mitchell.) pp. 382–389. (Santa Barbara Museum of Natural History: Santa Barbara, CA.)

Morrison, M., and Carbines, G. (2006). Estimating the abundance and size structure of an estuarine population of the sparid Pagrus auratus, using a towed camera during nocturnal periods of inactivity, and comparisons with conventional sampling techniques. Fisheries Research 82, 150–161.
Estimating the abundance and size structure of an estuarine population of the sparid Pagrus auratus, using a towed camera during nocturnal periods of inactivity, and comparisons with conventional sampling techniques.Crossref | GoogleScholarGoogle Scholar |

Newcombe, E. M., and Taylor, R. B. (2010). Trophic cascade in a seaweed-epifauna-fish food chain. Marine Ecology Progress Series 408, 161–167.
Trophic cascade in a seaweed-epifauna-fish food chain.Crossref | GoogleScholarGoogle Scholar |

Pederson, H. G., and Johnson, C. R. (2006). Predation of the sea urchin Heliocidaris erythrogramma by rock lobsters (Jasus edwardsii) in no-take marine reserves. Journal of Experimental Marine Biology and Ecology 336, 120–134.
Predation of the sea urchin Heliocidaris erythrogramma by rock lobsters (Jasus edwardsii) in no-take marine reserves.Crossref | GoogleScholarGoogle Scholar |

Pérez-Matus, A., and Shima, J. S. (2010). Density- and trait-mediated effects of fish predators on amphipod grazers: potential indirect benefits for the giant kelp Macrocystis pyrifera. Marine Ecology Progress Series 417, 151–158.
Density- and trait-mediated effects of fish predators on amphipod grazers: potential indirect benefits for the giant kelp Macrocystis pyrifera.Crossref | GoogleScholarGoogle Scholar |

Phillips, D. W., and Castori, P. (1982). Defensive responses to predatory seastars by two specialist limpets, Notoacmea insessa (Hinds) and Collisella instabilis (Gould), associated with marine algae. Journal of Experimental Marine Biology and Ecology 59, 23–30.
Defensive responses to predatory seastars by two specialist limpets, Notoacmea insessa (Hinds) and Collisella instabilis (Gould), associated with marine algae.Crossref | GoogleScholarGoogle Scholar |

R Development Core Team (2007). ‘R: A Language and Environment for Statistical Computing.’ (R Foundation for Statistical Computing: Vienna, Austria.)

Rogers, C. N., Williamson, J. E., Carson, D. G., and Steinberg, P. D. (1998). Diel vertical movement by mesograzers on seaweeds. Marine Ecology Progress Series 166, 301–306.
Diel vertical movement by mesograzers on seaweeds.Crossref | GoogleScholarGoogle Scholar |

Shears, N. T., and Babcock, R. C. (2002). Marine reserves demonstrate top-down control of community structure on temperate reefs. Oecologia 132, 131–142.
Marine reserves demonstrate top-down control of community structure on temperate reefs.Crossref | GoogleScholarGoogle Scholar |

Shears, N. T., and Babcock, R. C. (2003). Continuing trophic cascade effects after 25 years of no-take marine reserve protection. Marine Ecology Progress Series 246, 1–16.
Continuing trophic cascade effects after 25 years of no-take marine reserve protection.Crossref | GoogleScholarGoogle Scholar |

Shears, N. T., and Babcock, R. C. (2004a). Community composition and structure of shallow subtidal reefs in northeastern New Zealand. Department of Conservation, Science for Conservation 245, Wellington, New Zealand.

Shears, N. T., and Babcock, R. C. (2004b). Indirect effects of marine reserve protection on New Zealand’s rocky coastal marine communities. Department of Conservation, DOC Science Internal Series 192, Wellington, New Zealand.

Shears, N. T., and Babcock, R. C. (2007). Quantitative description of mainland New Zealand's shallow subtidal reef communities. Department of Conservation, Science for Conservation 280, Wellington, New Zealand.

SPSS (2006). ‘SPSS for Windows 15.0.0.’ (SPSS Inc: Chicago, IL, USA.)

Steinberg, P. D., and van Altena, I. (1992). Tolerance of marine invertebrate herbivores to brown algal phlorotannins in temperate Australasia. Ecological Monographs 62, 189–222.
Tolerance of marine invertebrate herbivores to brown algal phlorotannins in temperate Australasia.Crossref | GoogleScholarGoogle Scholar |

Steneck, R. S., Graham, M. H., Bourque, B. J., Corbett, D., Erlandson, J. M., et al. (2002). Kelp forest ecosystems: biodiversity, stability, resilience and future. Environmental Conservation 29, 436–459.
Kelp forest ecosystems: biodiversity, stability, resilience and future.Crossref | GoogleScholarGoogle Scholar |

Taylor, R. B. (1998). Density, biomass and productivity of animals in four subtidal rocky reef habitats: the importance of small mobile invertebrates. Marine Ecology Progress Series 172, 37–51.
Density, biomass and productivity of animals in four subtidal rocky reef habitats: the importance of small mobile invertebrates.Crossref | GoogleScholarGoogle Scholar |

Taylor, R. B. (1998). Short-term dynamics of a seaweed epifaunal assemblage. Journal of Experimental Marine Biology and Ecology 227, 67–82.
Short-term dynamics of a seaweed epifaunal assemblage.Crossref | GoogleScholarGoogle Scholar |

Taylor, R. B., and Cole, R. G. (1994). Mobile epifauna on subtidal brown seaweeds in northeastern New Zealand. Marine Ecology Progress Series 115, 271–282.
Mobile epifauna on subtidal brown seaweeds in northeastern New Zealand.Crossref | GoogleScholarGoogle Scholar |

Toth, G. B., and Pavia, H. (2002). Intraplant habitat and feeding preference of two gastropod herbivores inhabiting the kelp Laminaria hyperborea. Journal of the Marine Biological Association of the United Kingdom 82, 243–247.
Intraplant habitat and feeding preference of two gastropod herbivores inhabiting the kelp Laminaria hyperborea.Crossref | GoogleScholarGoogle Scholar |

Watanabe, J. M. (1984). The influence of recruitment, competition and benthic predation on spatial distributions of three species of kelp forest gastropods (Trochidae: Tegula). Ecology 65, 920–936.
The influence of recruitment, competition and benthic predation on spatial distributions of three species of kelp forest gastropods (Trochidae: Tegula).Crossref | GoogleScholarGoogle Scholar |

Wells, R. J. D., Steneck, R. S., and Palma, A. T. (2010). Three-dimensional resource partitioning between American lobster (Homarus americanus) and rock crab (Cancer irroratus) in a subtidal kelp forest. Journal of Experimental Marine Biology and Ecology 384, 1–6.
Three-dimensional resource partitioning between American lobster (Homarus americanus) and rock crab (Cancer irroratus) in a subtidal kelp forest.Crossref | GoogleScholarGoogle Scholar |

Williams, B. G., and Dean, I. C. (1989). Timing of locomotor activity in the New Zealand rock lobster, Jasus edwardsii. New Zealand Journal of Marine and Freshwater Research 23, 215–224.
Timing of locomotor activity in the New Zealand rock lobster, Jasus edwardsii.Crossref | GoogleScholarGoogle Scholar |

Willis, T. J., Millar, R. B., and Babcock, R. C. (2003). Protection of exploited fishes in temperate regions: high density and biomass of snapper Pagrus auratus (Sparidae) in northern New Zealand marine reserves. Journal of Applied Ecology 40, 214–227.
Protection of exploited fishes in temperate regions: high density and biomass of snapper Pagrus auratus (Sparidae) in northern New Zealand marine reserves.Crossref | GoogleScholarGoogle Scholar |