Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-26T21:48:05.891Z Has data issue: false hasContentIssue false
  • English
  • Français

Invasive bryozoan alters interaction between a native grazer and its algal food

Published online by Cambridge University Press:  05 March 2013

John M. O'Brien ,
Kira A. Krumhansl  and
Robert E. Scheibling
John M. O'Brien*
Affiliation:
Department of Biology, Dalhousie University, Halifax, Nova Scotia B3H 4J1, Canada
Kira A. Krumhansl
Affiliation:
Department of Biology, Dalhousie University, Halifax, Nova Scotia B3H 4J1, Canada
Robert E. Scheibling
Affiliation:
Department of Biology, Dalhousie University, Halifax, Nova Scotia B3H 4J1, Canada
*
Correspondence should be addressed to: J.M. O'Brien, Department of Biology, Dalhousie University, Halifax, Nova Scotia B3H 4J1, Canada email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The epiphytic bryozoan Membranipora membranacea encrusts the surface of kelp blades, causing recurrent large-scale defoliation events in kelp beds off the Atlantic coast of Nova Scotia, Canada. The gastropod Lacuna vincta grazes kelp, creating perforations that weaken blade tissues and increase the fragmentation rate. We assess the interaction between M. membranacea and L. vincta by measuring the grazing rate of snails on bryozoan-encrusted and non-encrusted kelp (Saccharina latissima) in no-choice and choice experiments in the laboratory conducted in November and December 2010. There was no effect of diet on grazing rate in no-choice experiments. In choice experiments, however, L. vincta grazed significantly more non-encrusted than encrusted kelp (7.1 versus 1.1 mg snail−1 d−1), and grazing rate of non-encrusted kelp was almost twice that in the no-choice experiment (3.8 mg snail−1 d−1), indicating that snails may avoid colonies of M. membranacea on partially encrusted kelp blades. We found no effect of diet on growth, reproduction and survival of snails maintained for four weeks on encrusted or non-encrusted kelp. By concentrating grazing damage on non-encrusted areas of blades, L. vincta may act synergistically with M. membranacea to increase the likelihood of blade breakage and canopy loss. This indirect effect of the invasive bryozoan could augment its direct effect on the standing biomass of native kelp beds and detrital export to adjacent communities.

Keywords

Lacuna vinctaMembranipora membranaceakelpinvasive speciesgrowthsurvivalreproductiongrazingfeeding preferenceindirect effects
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 93 , Issue 5 , August 2013 , pp. 1393 - 1400
Copyright
Copyright © Marine Biological Association of the United Kingdom 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Bangert, R. and Huntly, N. (2010) The distribution of native and exotic plants in a naturally fragmented sagebrush-steppe landscape. Biological Invasions 12, 1627–1640.CrossRefGoogle Scholar
Barber, N.A., Marquis, R.J. and Tori, W.P. (2008) Invasive prey impacts the abundance and distribution of native predators. Ecology 89, 2678–2683.CrossRefGoogle ScholarPubMed
Bax, N., Williamson, A., Aguero, M., Gonzalez, E. and Geeves, W. (2003) Marine invasive alien species: a threat to global biodiversity. Marine Policy 27, 313–323.CrossRefGoogle Scholar
Brown, B.J., Mitchell, R.J. and Graham, S.A. (2002) Competition for pollination between an invasive species (purple loosestrife) and a native congener. Ecology 83, 2328–2336.CrossRefGoogle Scholar
Byers, J.E. (2000) Competition between two estuarine snails: implications for invasions of exotic species. Ecology 81, 1225–1239.CrossRefGoogle Scholar
Carlton, J.T. and Geller, J.B. (1993) The global transport of nonindigenous marine organisms. Science 261, 78–82.CrossRefGoogle Scholar
Chapin, F.S., Zavaleta, E.S., Eviner, V.T., Naylor, R.L., Vitousek, P.M., Reynolds, H.L., Hooper, D.U., Lavorel, S., Sala, O.E., Hobbie, S.E., Mack, M.C. and Diaz, S. (2000) Consequences of changing biodiversity. Nature 405, 234–242.CrossRefGoogle ScholarPubMed
Chavanich, S. and Harris, L.G. (2000) Potential impact of the introduced bryozoan, Membranipora membranacea, on the subtidal snail, Lacuna vincta, in the Gulf of Maine. In Pederson, J. (ed.) Marine bioinvasions: Proceedings of the First National Conference, Massachusetts Institute of Technology, Cambridge, MA, 24–27 January 1999. Cambridge, MA: MIT Sea Grant College Program, pp. 157–163.Google Scholar
Chavanich, S. and Harris, L.G. (2002) The influence of macroalgae on seasonal abundance and feeding preference of a subtidal snail, Lacuna vincta (Montagu) (Littorinidae) in the Gulf of Maine. Journal of Molluscan Studies 68, 73–78.CrossRefGoogle Scholar
Chenelot, H. and Konar, B. (2007) Lacuna vincta (Mollusca, Neotaenioglossa) herbivory on juvenile and adult Nereocystis luetkeana (Heterokontophyta, Laminariales). Hydrobiologia 583, 107–118.CrossRefGoogle Scholar
Dixon, J., Schroeter, S.C. and Kastendiek, J. (1981) Effects of the encrusting bryozoan, Membranipora membranacea, on the loss of blades and fronds by the giant kelp, Macrocystis pyrifera (Laminariales). Journal of Phycology 17, 341–345.CrossRefGoogle Scholar
Dohzono, I., Kunitake, Y.K., Yokoyama, J. and Goka, K. (2008) Alien bumble bee affects native plant reproduction through interactions with native bumble bees. Ecology 89, 3082–3092.CrossRefGoogle ScholarPubMed
Durante, K.M. and Chia, F-S. (1991) Epiphytism on Agarum fimbriatum: can herbivore references explain distributions of epiphytic bryozoans? Marine Ecology Progress Series 7, 279–287.CrossRefGoogle Scholar
Fralick, R.A., Turgeon, K.W. and Mathieson, A.C. (1974) Destruction of kelp populations by Lacuna vincta (Montagu). Nautilus 88, 112–114.Google Scholar
Geiger, W., Alcorlo, P., Baltanás, A. and Montes, C. (2005) Impact of an introduced crustacean on the trophic webs of Mediterranean wetlands. Biological Invasions 7, 49–73.CrossRefGoogle Scholar
Grosholz, E.D. and Ruiz, G.M. (1996) Predicting the impact of introduced marine species: lessons from the multiple invasions of the European green crab Carcinus maenas. Biological Conservation 78, 59–66.CrossRefGoogle Scholar
Grosholz, E.D., Ruiz, G.M., Dean, C.A., Shirley, K.A., Maron, J.L. and Connors, P.G. (2000) The impacts of a nonindigenous marine predator in a California bay. Ecology 81, 1206–1224.CrossRefGoogle Scholar
Hurd, C.L., Durante, K.M. and Harrison, P.J. (2000) Influence of bryozoan colonization on the physiology of the kelp Macrocystis integrifolia (Laminariales, Phaeophyta) from nitrogen-rich and -poor sites in Barkley Sound, British Columbia. Phycologia 39, 435–440.CrossRefGoogle Scholar
Imrie, D.W., Hawkins, S.J. and McCrohan, C.R. (1989) The olfactory–gustatory basis of food preference in the herbivorous prosobranch, Littorina littorea (Linnaeus). Journal of Molluscan Studies 55, 217–225.CrossRefGoogle Scholar
Johnson, C.R. and Mann, K.H. (1986) The importance of plant defense abilities to the structure of subtidal seaweed 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.CrossRefGoogle Scholar
Karez, R., Engelbert, S. and Sommer, U. (2000) ‘Co-consumption’ and ‘protective coating’: two new proposed effects of epiphytes on their macroalgal hosts in mesograzer–epiphyte–host interactions. Marine Ecology Progress Series 205, 85–93.CrossRefGoogle Scholar
Knick, S.T. and Rotenberry, J.T. (1997) Landscape characteristics of disturbed shrubsteppe habitats in southwestern Idaho (U.S.A.). Landscape Ecology 12, 287–297.CrossRefGoogle Scholar
Knip, D.M. and Scheibling, R.E. (2007) Invertebrate fauna associated with kelp enhances reproductive output of the green sea urchin Strongylocentrotus droebachiensis. Journal of Experimental Marine Biology and Ecology 351, 150–159.CrossRefGoogle Scholar
Krumhansl, K.A. and Scheibling, R.E. (2011a) Detrital production in Nova Scotian kelp beds: patterns and processes. Marine Ecology Progress Series 421, 67–82.CrossRefGoogle Scholar
Krumhansl, K.A. and Scheibling, R.E. (2011b) Spatial and temporal variation in grazing damage by the gastropod Lacuna vincta in Nova Scotian kelp beds. Aquatic Biology 13, 163–173.CrossRefGoogle Scholar
Krumhansl, K.A., Lee, J.M. and Scheibling, R.E. (2011) Grazing damage and encrustation by an invasive bryozoan reduce the ability of kelps to withstand breakage by waves. Journal of Experimental Marine Biology and Ecology 407, 12–18.CrossRefGoogle Scholar
Lambert, W.J., Levin, P.S. and Berman, J. (1992) Changes in the structure of a New England (USA) kelp bed: the effects of an introduced species? Marine Ecology Progress Series 88, 303–307.CrossRefGoogle Scholar
Levin, P.S., Coyer, J.A., Petrik, R. and Good, T.P. (2002) Community-wide effects of non-indigenous species on temperate rocky reefs. Ecology 83, 3182–3193.CrossRefGoogle Scholar
Mancinelli, G. and Rossi, L. (2001) Indirect, size-dependent effects of crustacean mesograzers on the rhodophyte Gracilaria verrucosa (Hudson) Papenfuss: evidence from a short-term study in the Lesina Lagoon (Italy). Marine Biology 138, 1163–1173.Google Scholar
Martin, C.W., Valentine, M.M. and Valentine, J.F. (2010) Competitive interactions between invasive Nile Tilapia and native fish: the potential for altered trophic exchange and modification of food webs. PLoS ONE 5, e14395. doi:10.1371/journal.pone.0014395.CrossRefGoogle ScholarPubMed
McDevit, D.C. and Saunders, G.W. (2010) A DNA barcode examination of the Laminariaceae (Phaeophyceae) in Canada reveals novel biogeographical and evolutionary insights. Phycologia 49, 235–248.CrossRefGoogle Scholar
McQuaid, C.D. (1996) Biology of the gastropod family Littorinidae. II. Role in the ecology of the intertidal and shallow marine ecosystems. Oceanography and Marine Biology: an Annual Review 34, 263–302.Google Scholar
Menon, N.R. (1972) Heat tolerance, growth and regeneration in three North Sea bryozoans exposed to different constant temperatures. Marine Biology 15, 1–11.CrossRefGoogle Scholar
Molis, M. (2010) Grazing impact of, and indirect interactions between mesograzers associated with kelp (Laminara digitata). Journal of Phycology 46, 77–84.CrossRefGoogle Scholar
Nestler, E.C. and Harris, L.G. (1994) The importance of omnivory in Strongylocentrotus droebachiensis (Müller) in the Gulf of Maine. In David, B., Guille, A., Féral, J.-P. and Roux, M. (eds) Echinoderms through time: Proceedings of the Eighth International Echinoderm Conference, Dijon, France, 6–10 September 1993. Rotterdam: A.A. Balkema, pp. 813–818.Google Scholar
Nichols, F.E., Thompson, J.K. and Schemel, L.E. (1990) Remarkable invasion of San Francisco Bay (California, USA) by the Asian clam Potamocorbula amurensis. II. Displacement of a former community. Marine Ecology Progress Series 66, 95–101.CrossRefGoogle Scholar
Norton, T.A., Hawkins, S.J., Manley, N.L., Williams, G.A. and Watson, D.C. (1990) Scraping a living: a review of littorinid grazing. Hydrobiologia 193, 117–138.CrossRefGoogle Scholar
Padilla, D.K. (1985) Structural resistance of algae to herbivores. Marine Biology 90, 103–109.CrossRefGoogle Scholar
Padilla, D.K. (2001) Food and environmental cues trigger an inducible offense. Evolutionary Ecology Research 3, 15–25.Google Scholar
Parker, I.M., Simberloff, D., Lonsdale, W.M., Goodell, K., Wonham, M., Kareiva, P.M., Williamson, M.H., Von Holle, B., Moyle, P.B., Byers, J.E. and Goldwasser, L. (1999) Impact: toward a framework for understanding the ecological effects of invaders. Biological Invasions 1, 3–19.CrossRefGoogle Scholar
Peterson, C.H. and Renaud, P.E. (1989) Analysis of feeding preference experiments. Oecologia 80, 82–86.CrossRefGoogle ScholarPubMed
Petren, K. and Case, T.J. (1996) An experimental demonstration of exploitation competition in an ongoing invasion. Ecology 77, 118–132.CrossRefGoogle Scholar
Posey, M.H. (1988) Community changes associated with the spread of an introduced seagrass, Zostera japonica. Ecology 69, 974–983.CrossRefGoogle Scholar
Rodriguez, L.F. (2006) Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur. Biological Invasions 8, 927–939.CrossRefGoogle Scholar
Ruiz, G.M., Carlton, J.T., Grosholz, E.D. and Hines, A.H. (1997) Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent, and consequences. American Zoologist 37, 621–632.CrossRefGoogle Scholar
Saier, B. and Chapman, A.S. (2004) Crusts of the alien bryozoan Membranipora membranacea can negatively impact spore output from native kelps (Laminaria longicruris). Botanica Marina 47, 265–271.CrossRefGoogle Scholar
Scheibling, R.E. and Gagnon, P. (2009) Temperature-mediated outbreak dynamics of the invasive bryozoan Membranipora membranacea in Nova Scotian kelp beds. Marine Ecology Progress Series 390, 1–13.CrossRefGoogle Scholar
Scheibling, R.E., Hennigar, A.W. and Balch, T. (1999) Destructive grazing, epiphytism, and disease: the dynamics of sea urchin–kelp interactions in Nova Scotia. Canadian Journal of Fisheries and Aquatic Sciences 56, 2300–2314.CrossRefGoogle Scholar
Smith, D.A.S. (1973) The population biology of Lacuna pallidula (Da Costa) and Lacuna vincta (Montagu) in North-east England. Journal of the Marine Biological Association of the United Kingdom 53, 143–156.CrossRefGoogle Scholar
Steneck, R.S. and Watling, L. (1982) Feeding capabilities and limitation of herbivorous molluscs: a functional group approach. Marine Biology 68, 299–319.CrossRefGoogle Scholar
Tablado, Z., Tella, J.L., Sánchez-Zapata, J.A. and Hiraldo, F. (2010) The paradox of the long-term positive effects of a North American crayfish on a European community of predators. Conservation Biology 24, 1230–1238.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Travis, J. (1993) Invader threatens Black, Azov Seas. Science 262, 1366–1367.CrossRefGoogle ScholarPubMed
Underwood, A.J. (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge: Cambridge University Press.Google Scholar
Viejo, R.M. and Arrontes, J. (1992) Interaction between mesograzers inhabiting Fucus vesiculosus in Northern Spain. Journal of Experimental Marine Biology and Ecology 162, 97–111.Google Scholar
Vitousek, P.M., D'Antonio, C.M., Loope, L.L. and Westbrooks, R. (1996) Biological invasions as global environmental change. American Scientist 84, 468–478.Google Scholar
Wilcove, D.S., Rothstein, D., Dubow, J., Phillips, A. and Losos, E. (1998) Quantifying threats to imperiled species in the United States. BioScience 48, 607–615.CrossRefGoogle Scholar
Yorke, A.F. and Metaxas, A. (2011) Interactions between an invasive and a native bryozoan (Membranipora membranacea and Electra pilosa) species on kelp and Fucus substrates in Nova Scotia, Canada. Marine Biology 158, 2299–2311.CrossRefGoogle Scholar