Skip to main content
Log in

Invasive species as a new food source: does a nudibranch predator prefer eating an invasive bryozoan?

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Membranipora membranacea is an invasive bryozoan that was first found in the Gulf of Maine in 1987 and within two years became the dominant organism living on kelps. Membranipora may have become dominant so quickly because it had little competition in a relatively unoccupied niche; however, lack of predation has also probably played a major role. Where Membranipora is native, there is usually a specialist nudibranch predator that keeps the population in check. For example, in European populations, the nudibranch Polycera quadrilineata prefers Membranipora while Onchidoris muricata is known to prefer another bryozoan, Electra pilosa. Electra, Membranipora, and Onchidoris are all now found in the Gulf of Maine while Polycera is not. We tested whether Onchidoris would (1) eat Membranipora at all, (2) eat Membranipora and Electra at different rates, and (3) show a preference for eating Membranipora or Electra when given a choice. We found that Onchidoris does eat Membranipora, and it generally eats Membranipora faster than Electra. However, when given a choice, Onchidoris prefers Electra. Onchidoris typically reproduces in the spring and grows over the fall and winter, but has recently been found reproducing in the winter in New Hampshire. Although it does not survive the winter as well as Electra, Membranipora is the dominant organism living on many macroalgae in the late summer and fall. Thus, the large Membranipora food source now available in the summer and fall may allow Onchidoris to reproduce earlier.

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
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Berman J, Harris L, Lambert W, Buttrick M, Dufresne M (1992) Recent invasions of the Gulf of Maine: three contrasting ecological histories. Conserv Biol 6:435–441

    Article  Google Scholar 

  • Bleakney JS (1996) Sea slugs of Atlantic Canada and the Gulf of Maine. Nimbus Publishing and the Nova Scotia Museum, Halifax, Nova Scotia, 216 pp

    Google Scholar 

  • Brenchley G, Carlton JT (1983) Competitive displacement of native mud snails by introduced periwinkles in the New England intertidal zone. Biol Bull 165:543–558

    Article  Google Scholar 

  • Bruno JF, Fridley JD, Bromberg KD, Bertness MD (2005) Insights into biotic interactions from studies of species invasions. In: Sax DF, Stachowicz JJ, Gaines SD (eds), Species invasions: insights into ecology, evolution and biogeography. Sinauer Associates, Sunderland MA, pp 14–40

    Google Scholar 

  • Byers JE (2000) Competition between two estuarine snails: implications for invasions of exotic species. Ecology 81:1225–1239

    Google Scholar 

  • Cancino JM, Muñoz J, Muñoz M, Orellana MC (1987) Effects of the bryozoan Membranipora tuberculata (Bosc) on the photosynthesis and growth of Gelidium rex Santelices Et Abbott. J Exp Mar Biol Ecol 113:105–112

    Article  Google Scholar 

  • Casey P (2005) Insights into ecology. In: Sax DF, Stachowicz JJ, Gaines SD (eds) Species invasions: insights into ecology, evolution, and biogeography. Sinauer Associates, Inc. Publishers, Sunderland, Massechusetts, pp 9–12

  • Chadwick SR, Thorpe JP (1981) An investigation of some aspects of bryozoan predation by dorid nudibranchs (Mollusca: Opisthobranchia). In: Larwood GP, Nielsen C (eds) Recent and Fossil Bryozoa. Olsen & Olsen, Fredensborg, pp 51–58

  • Chapman AS, Scheibling RE, Chapman ARO (2002) Species introductions and changes in marine vegetation of Atlantic Canada. In: Claudi R, Nantel P, Muckle-Jeffs E (eds), Alien Invaders in Canada’s waters, wetlands, and forests. Natural Resources Canada, Canadian Forest Service Science Branch, Ottawa, pp 133–148

    Google Scholar 

  • Chavanich S, Harris LG (2000) Potential impact of the introduced bryozoan, Membranipora membranacea, on the subtidal snail, Lacuna vincta, in the Gulf of Maine. In: Pederson J (eds), Marine bioinvasions. MIT Sea Grant College Program, Cambridge, MA, pp 157–163

    Google Scholar 

  • Clarke B, Johnson MS, Murray J (1984) The extinction of endemic species by a program of biological control. Pacific Sci 38:97–104

    Google Scholar 

  • Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733

    Article  Google Scholar 

  • Dixon J, Schroeter SC, Kastendiek J (1981) Effects of the encrusting bryozoan, Membranipora membranacea, on the loss of blades and fronds by the giant kelp, Macrocystis pyrifera (Laminariales). J Phycol 17:341–345

    Article  Google Scholar 

  • Grosholz ED, Ruiz GM, Dean CA, Shirley KA, Maron JL, Connors PG (2000) The impacts of a nonindigenous marine predator in a California bay. Ecology 81:1206–1224

    Article  Google Scholar 

  • Gurevitch J, Padilla DK (2004) Are invasive species a major cause of extinctions? Trends Ecol Evol 19:470–474

    Article  PubMed  Google Scholar 

  • Harris LG, Matheison AC (2000) Patterns of range expansion, niche shift and predator acquisition in Codium fagile ssp. tomentosoides and Membranipora membranacea in the Gulf of Maine. In: Pederson J (ed) Marine bioinvasions. MIT Sea Grant College Program, Massachusetts Institute of Technology, Cambridge, MA, pp 46–56

    Google Scholar 

  • Harris LG, Tyrrell MC (2001) Changing community states in the Gulf of Maine: synergism between invaders, overfishing and climate change. Biol Inv 3:9–21

    Article  Google Scholar 

  • Harvell CD (1986) The ecology and evolution of inducible defenses in a marine bryozoan: cues, costs and consequences. Am Natur 128:810–823

    Article  Google Scholar 

  • Havenhand JN, Todd CD (1988) Physiological ecology of Adalaria proxima (Alder Et Hancock) and Onchidoris muricata (Muller) (Gastropoda, Nudibranchia). 1. Feeding, growth, and respiration. J Exp Mar Biol Ecol 118:151–172

    Article  Google Scholar 

  • Herbold B, Moyle PB (1986) Introduced species and vacant niches. Am Natur 128:751–760

    Article  Google Scholar 

  • Hockey PAR, Schurink CV (1992) The invasive biology of the mussel Mytilus galloprovincialis on the Southern African Coast. Trans R Soc S Afr 48:123–139

    Google Scholar 

  • Hurd CL, Durante KM, Chia FS, Harrison PJ (1994) Effect of bryozoan colonization on inorganic nitrogen acquisition by the kelps Agarum fimbriatum and Macrocystis integrifolia. Mar Biol 121:167–173

    Article  Google Scholar 

  • Hurd CL, Durante KM, Harrison PJ (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, Canada. Phycologia 39:435–440

    Article  Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170

    Article  Google Scholar 

  • Lambert WJ (1990) Population ecology and feeding biology of nudibranchs in colonies of the hydroid Obelia genicula. PhD Thesis, Department of Zoology, University of New Hampshire, Durham, NH, pp 189

  • Lambert WJ, Levin PS, Berman J (1992) Changes in the structure of a New England (USA) kelp bed: the effects of an introduced species? Mar Ecol Prog Ser 88:303–307

    Google Scholar 

  • Levin PS, Coyer JA, Petrik R, Good TP (2002) Community-wide effects of nonindigenous species on temperate rocky reefs. Ecology 83:3182–3193

    Google Scholar 

  • Lodge DM (1993) Biological invasions: lessons for ecology. Trends Ecol Evol 8:133–137

    Article  Google Scholar 

  • Mathieson AC, Dawes CJ, Harris LG, Hehre EJ (2003) Expansion of the Asiatic green alga Codium fragile ssp. tomentosoides in the Gulf of Maine. Rhodora 105:1–53

    Google Scholar 

  • Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421:625–627

    Article  PubMed  CAS  Google Scholar 

  • Morgan M, Threlkeld ST, Goldman CR (1978) Impact of the introduction of kokanee Oncorhynchus nerka and opossum shrimp Mysis relicta on a subalpine lake. J Fisher Res Board Canada 35:1572–1579

    Google Scholar 

  • Muñoz J, Cancino JM, Molina MX (1991) Effect of encrusting bryozoans on the physiology of the algal substratum. J Mar Biol Assoc UK 71:877–882

    Article  Google Scholar 

  • Nestler EC, Harris LG (1994) The importance of omnivory in Strongylocentrotus droebachiensis (Muller) in the Gulf of Maine. In: David B, Guille A, Feral J-P, Roux M (eds), Echinoderms through time, A.A. Balkema, Rotterdam, The Netherlands, pp 813–818

    Google Scholar 

  • Oswald RC, Telford N, Seed R, Happey Wood CM (1984) The effect of encrusting bryozoans on the photosynthetic activity of Fucus serratus. Estuarine Coastal Shelf Sci 19:697–702

    Article  Google Scholar 

  • Race M (1982) Competitive displacement and predation between native and introduced mud snails. Oecologia 54:337–347

    Article  Google Scholar 

  • Roughgarden J (1986) Predicting invasions and rates of spread. In: Mooney HA, Drake JA (eds), Ecology of biological invasions of North America and Hawaii. Springer-Verlag, New York, pp 179–188

    Google Scholar 

  • Ryland JS (1976) Physiology and ecology of marine bryozoans. Adv Mar Biol 14:285–443

    Article  Google Scholar 

  • Saier B, Chapman AS (2004) Crusts of the alien bryozoan Membranipora membranacea can negatively impact spore output from native kelps (Laminaria longicruris). Bot Mar 47:265–271

    Article  Google Scholar 

  • Scheibling RE (2000) Species invasions and community change threaten the sea urchin fishery in Nova Scotia. Retrived from http://www.crdpm.umcs.ca/oursin/sesv.htm

  • Scheibling RE, Hennigar AW, Balch T (1999) Destructive grazing, epiphytism, and disease: The dynamics of sea urchin - kelp interactions in Nova Scotia. Can J Fis Aquat Sci 56:2300–2314

    Article  Google Scholar 

  • Seed R (1976) Observations on the ecology of Membranipora (Bryozoa) and a major predator Doridella steinbergae (Nudibranchiata) along the fronds of Laminaria saccharina at Friday Harbor, Washington. J Exp Mar Biol Ecol 24:1–17

    Article  Google Scholar 

  • Simberloff D (1981) Community effects of introduced species. In: Nitecki MH (eds), Biotic crises in ecological and evolutionary time. Academic Press, San Francisco, pp 53–81

    Google Scholar 

  • Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol Inv 1:21–32

    Article  Google Scholar 

  • Stachowicz JJ, Terwin JR, Whitlatch RB, Osman RW (2002) Linking climate change and biological invasions: ocean warming facilitates nonindigenous species invasions. Proc Natl Acad Sci 99:15497–15500

    Article  PubMed  CAS  Google Scholar 

  • Sumi CBT, Scheibling RE (2005) Role of grazing by sea urchins Strongylocentrotus droebachiensis in regulating the invasive alga Codium fragile ssp tomentosoides in Nova Scotia. Mar Ecol Prog Ser 292:203–212

    Google Scholar 

  • Theriault C (2003) Mapping the subtidal distribution of the invasive alga Codium fragile ssp. tomentosoides in coastal waters of Nova Scotia using the Compact Airborne Spectographic Imager (CASI). MSc thesis, Department of Biology, Dalhousie University, Halifax, pp 85

  • Todd CD (1978) Changes in spatial pattern of an intertidal population of nudibranch mollusk Onchidoris muricata in relation to life-cycle, mortality and environmental heterogeneity. J Anim Ecol 47:189–203

    Article  Google Scholar 

  • Todd CD (1979) Reproductive energetics of 2 species of dorid nudibranchs with planktotrophic and lecithotrophic larval strategies. Mar Biol 53:57–68

    Article  Google Scholar 

  • Todd CD (1981) The ecology of nudibranch molluscs. Oceanogr Mar Biol Annu Rev 19:141–234

    Google Scholar 

  • Todd CD (1987) Reproductive energetics and larval strategies of nudibranch mollusks: effects of ration level during the spawning period in Onchidoris muricata (Muller) and Adalaria proxima (Alder and Hancock). Am Malacol Bull 5:293–301

    Google Scholar 

  • Todd CD, Havenhand JN (1989) Nudibranch-bryozoan associations: the quantification of ingestion and some observations on partial predation among Doridoidea. J Molluscan Stud 55:245–259

    Article  Google Scholar 

  • Vermeij GJ (1991) When biotas meet: understanding biotic interchange. Science 253:1099–1104

    Article  PubMed  CAS  Google Scholar 

  • Wing BL, Clendenning KA (1971) Kelp surfaces and associated invertebrates. In: North WJ (ed) The biology of Giant Kelp Beds (Macrocystis) in California. Nova Hedwigia, pp 319–341

  • Yoshioka PM (1982) Role of planktonic and benthic factors in the population dynamics of the bryozoan Membranipora membranacea. Ecology 63:457–468

    Article  Google Scholar 

  • Zaret TM, Paine RT (1973) Species introduction in a tropical lake. Science 182:449–455

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank the Bowdoin College Coastal Studies Center for use of space at the Marine Lab. M. Pizer and anonymous reviewers provided comments that helped improve this paper substantially.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marney C. Pratt.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pratt, M.C., Grason, E.W. Invasive species as a new food source: does a nudibranch predator prefer eating an invasive bryozoan?. Biol Invasions 9, 645–655 (2007). https://doi.org/10.1007/s10530-006-9065-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-006-9065-x

Keywords

Navigation