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Marine Biology

, Volume 158, Issue 10, pp 2299–2311 | Cite as

Interactions between an invasive and a native bryozoan (Membranipora membranacea and Electra pilosa) species on kelp and Fucus substrates in Nova Scotia, Canada

  • Alana F. Yorke
  • Anna MetaxasEmail author
Original Paper

Abstract

Most research on biological invasions to date has focused on the population dynamics of very successful and disruptive introduced species; however, additional knowledge of the biology of the native species is essential for understanding interactions between the two and may reveal factors that limit invasion success. The invasive bryozoan Membranipora membranacea interacts with native Electra pilosa on two substrates in northwest Atlantic subtidal habitats: highly dynamic and fast-growing kelps; and smaller, more stable, and slow-growing fucoid algae. We quantified the relative abundance and evaluated encounter outcomes in different seasons of these two bryozoans on kelp and Fucus at four sites in Nova Scotia. We also examined the effects of substrate (kelp, Fucus), temperature (7, 10, 13°C), and food (limited, unlimited) on growth rates of E.pilosa in laboratory experiments and using field manipulations. We compared our findings on factors affecting the growth of E. pilosa to those on M. membranacea obtained in similar and thus directly comparable experiments from a previous study. The proportional abundance of M.membranacea was greater than that of E. pilosa on kelps, but the opposite was observed on Fucus. Competitive standoffs between the two bryozoans were more frequent than expected, with no differences recorded between substrates; most encounters were won by M. membranacea. Growth of E.pilosa was faster on Fucus than kelp, decreased with increasing temperature only on Fucus, and was not affected by food. Growth rate of E. pilosa in all treatments was slower than that previously measured for M.membranacea. Faster growth and strong overgrowth abilities likely interact on kelps to ensure success of the invasive bryozoan. Success can be limited by low space availability, which in turn restricts growth rate, and consequently, colony size, such as on fucoid substrates. The incorporation of alternative contexts into invasion research can reveal factors involved in the resilience of native communities.

Keywords

Nova Scotia Colony Size Subtidal Habitat Kelp Species Unlimited Food 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

Research was conducted with field assistance from J. Lindley, M. Saunders, S. Watanabe, K. Dinning, M. Lloyd, K. Krumhansl, C. Feehan, and A. Roy and laboratory assistance from K. Dinning, M. Saunders, J. Short, and A. Roy. We thank the staff of the Dalhousie University Aquatron facility for laboratory space and equipment. R. E. Scheibling provided comments on an earlier version of the manuscript. This research was supported by a Natural Sciences and Engineering Research Council (NSERC) Discovery grant to AM, and a NSERC Canada Graduate Scholarship, a Killam Predoctoral Fellowship, and a Dalhousie University President’s Award to AY.

References

  1. Bayer MM, Cormack RM, Todd CD (1994) Influence of food concentration on polypide regression in the marine bryozoan Electra pilosa (L.) (Bryozoa: Cheilostomata). J Exp Mar Biol Ecol 178(1):35–50CrossRefGoogle Scholar
  2. Bell JJ, Barnes DKA (2003) The importance of competitor identity, morphology and ranking methodology to outcomes in interference competition between sponges. Mar Biol 143(3):415–426CrossRefGoogle Scholar
  3. 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(3):435–441CrossRefGoogle Scholar
  4. Best MA, Thorpe JP (1986) Effects of food particle concentration on feeding current velocity in six species of marine bryozoa. Mar Biol 93(2):255–262CrossRefGoogle Scholar
  5. Buss LW (1980) Competitive intransitivity and size-frequency distributions of interacting populations. Proc Natl Acad Sci USA 77(9):5355–5359CrossRefGoogle Scholar
  6. Buss LW, Jackson JBC (1979) Competitive networks: nontransitive competitive relationships in cryptic coral reef environments. Am Nat 113(2):223–234CrossRefGoogle Scholar
  7. 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 (ed) Marine bioinvasions: Proceedings of the first national conference. MIT Sea Grant College Program, Cambridge, pp 157–163Google Scholar
  8. Connell JH (1961a) Effects of competition, predation by Thais lapillus, and other factors on natural populations of the barnacle Balanus balanoides. Ecol Monogr 31(1):61–104CrossRefGoogle Scholar
  9. Connell JH (1961b) The influence of interspecific competition and other factors on the distribution of the barnacle Chthamalus stellatus. Ecology 42(4):710–723CrossRefGoogle Scholar
  10. Connolly SR, Muko S (2008) Space preemption, size-dependent competition, and the coexistence of clonal growth forms. Ecol Soc Am 84(11):2979–2988Google Scholar
  11. Dayton PK (1971) Competition, disturbance, and community organization: the provision and subsequent utilization of space in a rocky intertidal community. Ecol Monogr 41(4):351–389CrossRefGoogle Scholar
  12. 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(4):341–345CrossRefGoogle Scholar
  13. Fridley JD, Stachowicz JJ, Naeem S, Sax DF, Seabloom EW, Smith MD, Stohlgren TJ, Tilman D, Von Holle B (2007) The invasion paradox: reconciling pattern and process in species invasions. Ecology 88(1):3–17CrossRefGoogle Scholar
  14. Gerard VA, Mann KH (1979) Growth and production of Laminaria longicruris (Phaeophyta) populations exposed to different intensities of water movement. J Phycol 15(1):33–41CrossRefGoogle Scholar
  15. Grosholz ED (2002) Ecological consequences of coastal invasions. Trends Ecol Evol 17(1):22–27CrossRefGoogle Scholar
  16. Hermansen P, Larsen PS, Riisgård HU (2001) Colony growth rate of encrusting marine bryozoans (Electra pilosa and Celleporella hyalina). J Exp Mar Biol Ecol 263(1):1–23CrossRefGoogle Scholar
  17. Jackson JBC (1979) Overgrowth competition between encrusting cheilostome ectoprocts in a Jamaican cryptic reef environment. J Anim Ecol 48(3):805–823CrossRefGoogle Scholar
  18. Johnson CR, Mann KH (1988) Diversity, patterns of adaptation, and stability of Nova Scotian kelp beds. Ecol Monogr 58(2):129–154CrossRefGoogle Scholar
  19. Konar B, Iken K (2005) Competitive dominance among sessile marine organisms in a high arctic boulder community. Polar Biol 29(1):61–64CrossRefGoogle Scholar
  20. Lambert W, 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(2):303–307CrossRefGoogle Scholar
  21. Levin PS, Coyer JA, Petrik R, Good TP (2002) Community-wide effects of nonindigenous species on temperate rocky reefs. Ecology 83(11):3182–3193CrossRefGoogle Scholar
  22. Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10(3):689–710CrossRefGoogle Scholar
  23. Mann KH (1972) Ecological energetics of the seaweed zone in a marine bay on the Atlantic coast of Canada. II. Productivity of the seaweeds. Mar Biol 14(3):199–209Google Scholar
  24. Manriquez PH, Cancino JM (1996) Bryozoan-macroalgal interactions: do epibionts benefit? Mar Ecol Prog Ser 138:189–197CrossRefGoogle Scholar
  25. McCook LJ, Chapman ARO (1991) Community succession following massive ice-scour on an exposed rocky shore: effects of Fucus canopy algae and of mussels during late succession. J Exp Mar Biol Ecol 154(2):137–169CrossRefGoogle Scholar
  26. Menon NR (1972) Heat tolerance, growth and regeneration in three North Sea bryozoans exposed to different constant temperatures. Mar Biol 15(1):1–11CrossRefGoogle Scholar
  27. Menon NR (1974) Clearance rates of food suspension and food passage rates as a function of temperature in two North Sea bryozoans. Mar Biol 24(1):65–67CrossRefGoogle Scholar
  28. Metaxas A, Scheibling RE (1996) Spatial heterogeneity of phytoplankton assemblages in tidepools: effects of abiotic and biotic factors. Mar Ecol Prog Ser 130(1):179–199CrossRefGoogle Scholar
  29. Nikulina EA, Hanel R, Schäfer P (2007) Cryptic speciation and paraphyly in the cosmopolitan bryozoan Electra pilosa—impact of the tethys closing on species evolution. Mol Phylogenet Evol 45(3):765–776CrossRefGoogle Scholar
  30. O’Connor RJ, Seed R, Boaden PJS (1979) Effects of environment and plant characteristics on the distribution of bryozoa in a Fucus serratus L. community. J Exp Mar Biol Ecol 38:151–178CrossRefGoogle Scholar
  31. O’Connor RJ, Seed R, Boaden PJS (1980) Resource space partitioning by the bryozoa of a Fucus serratus L. community. J Exp Mar Biol Ecol 45:117–137CrossRefGoogle Scholar
  32. O’Dea A, Okamura B (1999) Influence of seasonal variation in temperature, salinity and food availability on module size and colony growth of the estuarine bryozoan Conopeum seurati. Mar Biol 135(4):581–588CrossRefGoogle Scholar
  33. Okamura B (1988) The influence of neighbors on the feeding of an epifaunal bryozoan. J Exp Mar Biol Ecol 120(2):105–123CrossRefGoogle Scholar
  34. Okamura B (1992) Microhabitat variation and patterns of colony growth and feeding in a marine bryozoan. Ecology 73(4):1502–1513CrossRefGoogle Scholar
  35. Russ GR (1982) Overgrowth in a marine epifaunal community: competitive hierarchies and competitive networks. Oecologia 53(1):12–19CrossRefGoogle Scholar
  36. Saunders M, Metaxas A (2007) Temperature explains settlement patterns of the introduced bryozoan Membranipora membranacea in Nova Scotia, Canada. Mar Ecol Prog Ser 344:95–106CrossRefGoogle Scholar
  37. Saunders M, Metaxas A (2008) High recruitment of the introduced bryozoan Membranipora membranacea is associated with kelp bed defoliation in Nova Scotia, Canada. Mar Ecol Prog Ser 369:139–151CrossRefGoogle Scholar
  38. Saunders MI, Metaxas A (2009a) Effects of temperature, size, and food on the growth of Membranipora membranacea in laboratory and field studies. Mar Biol 156(11):2267–2276CrossRefGoogle Scholar
  39. Saunders MI, Metaxas A (2009b) Population dynamics of a nonindigenous epiphytic bryozoan Membranipora membranacea in the western North Atlantic: effects of kelp substrate. Aquat Biol 8:83–94CrossRefGoogle Scholar
  40. Scheibling RE, Gagnon P (2006) Competitive interactions between the invasive green alga Codium fragile ssp. tomentosoides and native canopy-forming seaweeds in Nova Scotia (Canada). Mar Ecol Prog Ser 325:1–14CrossRefGoogle Scholar
  41. Scheibling RE, Gagnon P (2009) Temperature-mediated outbreak dynamics of the invasive bryozoan Membranipora membranacea in Nova Scotian kelp beds. Mar Ecol Prog Ser 390:1–13CrossRefGoogle Scholar
  42. Sieburth JM (1969) Studies on algal substances in the sea. III. The production of extracellular organic matter by littoral marine algae. J Exp Mar Biol Ecol 3(3):290–309CrossRefGoogle Scholar
  43. Stachowicz JJ, Byrnes JE (2006) Species diversity, invasion success, and ecosystem functioning: disentangling the influence of resource competition, facilitation, and extrinsic factors. Mar Ecol Prog Ser 311:251–262CrossRefGoogle Scholar
  44. Steinberg PD, de Nys R (2002) Chemical mediation of colonization of seaweed surfaces. J Phycol 38:621–629CrossRefGoogle Scholar
  45. Steinberg PD, de Nys R, Kjelleberg S (2001) Chemical mediation of surface colonization. In: McClintock JB, Baker JB (eds) Marine chemical ecology. CRC Press, Boca Raton, pp 355–387Google Scholar
  46. Walters LJ, Wethey DS (1986) Surface topography influences competitive hierarchies on marine hard substrata: a field experiment. Biol Bull 170(3):441–449CrossRefGoogle Scholar
  47. Watanabe S, Scheibling RE, Metaxas A (2009) Contrasting patterns of spread in interacting invasive species: Membranipora membranacea and Codium fragile off Nova Scotia. Biol Invasions 12(7):2329–2342CrossRefGoogle Scholar
  48. Wilcove DS, Rothstein D, Dubow J, Phillips A, Losos E (1998) Quantifying threats to imperiled species in the United States. Bioscience 48(8):607–615CrossRefGoogle Scholar
  49. Zar JH (1999) Biostatistical analysis. Prentice-Hall, NJGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Department of BiologyDalhousie UniversityHalifaxCanada
  2. 2.Department of OceanographyDalhousie UniversityHalifaxCanada

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