Abstract
Biofouling on cultivated kelp in open sea conditions is a challenge when fouling species such as the encrusting bryozoans Membranipora membranacea and Electra pilosa develop colonies that cover the surface of the kelp lamina. The bryozoan colonies make the flexible lamina brittle and susceptible to breakage and reduce the commercial value of the biomass for both human consumption and industrial applications. The development of the bryozoan fouling on cultivated Saccharina latissima in temperate coastal waters was studied at two locations in Norway from April to September. The time of settling and development of colonies of M. membranacea and E. pilosa were characterized. Sampling of bryozoan larvae abundance at the cultivation locations showed that the bryozoan colonies settled on the cultivated kelp in mid-June at both locations, followed by a rapid colony growth during late June and July. In August and September, the kelp was highly degraded by the bryozoan coverage and highly subjected to breakage of the lamina. Membranipora membranacea was the most prevailing of the two species. Although abundant at all cultivation depths, the results showed a decrease in bryozoan coverage with increasing depth. From a commercial point of view, S. latissima deployed in temperate Norwegian coastal waters in winter should be harvested in early June to avoid the negative impact from bryozoan fouling.
References
Abelson A (1997) Settlement in flow: Upstream exploration of substrata by weakly swimming larvae. Ecology 78:160–166
Andersen GS, Steen H, Christie H, Fredriksen S, Moy FE (2011) Seasonal patterns of sporophyte growth, fertility, fouling, and mortality of Saccharina latissima in Skagerrak, Norway: Implications for forest recovery. Jf Mar Biol 2011:1–8
Bartsch I, Wiencke C, Bischof K, Buchholz CM, Buck BH, Eggert A, Feuerpfeil P, Hanelt D, Jacobsen S, Karez R, Karsten U, Molis M, Roleda MY, Schubert H, Schumann R, Valentin K, Weinberger F, Wiese J (2008) The genus Laminaria sensu lato: recent insights and developments. Eur J Phycol 43:1–86
Bates D, Maechler M, Bolker BM, Walker S (2014) lme4: Linear mixed-effect models using Eigen and S4. 1.0.6 edn
Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White J-SS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York
Christie H, Norderhaug KM, Fredriksen S (2009) Macrophytes as habitat for fauna. Mar Ecol Prog Ser 396:221–233
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
Fletcher RL (1995) Epiphytism and fouling in Gracilaria cultivation: an overview. J Appl Phycol 7:325–333
Forbord S, Skjermo J, Arff J, Handå A, Reitan KI, Bjerregaard R, Lüning K (2012) Development of Saccharina latissima (Phaeophyceae) kelp hatcheries with year-round production of zoospores and juvenile sporophytes on culture ropes for kelp aquaculture. J Appl Phycol 24:393–399
Gendron L, Tamigneaux É (2008) Expériences de culture de l'algue brune Saccharina longicruris en 2007: essais en bassin et en mer au large de Paspébiac et de Grande-Riviere (Québec). Rapp Tech Can Sci Halieut Aquat vol 2820. Direction régionale des Sciences, Pêches et Océans Canada, Institut Maurice-Lamontagne
Handå A, Forbord S, Wang X, Broch OJ, Dahle SW, Størseth TR, Reitan KI, Olsen Y, Skjermo J (2013) Seasonal-and depth-dependent growth of cultivated kelp (Saccharina latissima) in close proximity to salmon (Salmo salar) aquaculture in Norway. Aquaculture 414:191–201
Hayward PJ, Ryland JS (1995) Handbook of the marine fauna of North-West Europe. Oxford University Press, Oxford
Hepburn CD, Hurd CL, Frew RD (2006) Colony structure and seasonal differences in light and nitrogen modify the impact of sessile epifauna on the giant kelp Macrocystis pyrifera (L.) C Agardh. Hydrobiologia 560:373–384
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
Krumhansl KA, Lee JM, Scheibling RE (2011) Grazing damage and encrustation by an invasive bryozoan reduce the ability of kelps to withstand breakage by waves. J Exp Mar Biol Ecol 407:12–18
Lutaud G (1961) Contribution to the study of budding and growth in colonies of the cheilostome bryozoan Membranipora membranacea. Ann Soc Roy Zool Belgique 91:157–199
Menon N (1972) Heat tolerance, growth and regeneration in three North Sea bryozoans exposed to different constant temperatures. Mar Biol 15:1–11
Peteiro C, Freire Ó (2013) Epiphytism on blades of the edible kelps Undaria pinnatifida and Saccharina latissima farmed under different abiotic conditions. J World Aquacult Soc 44:706–715
R Core Team (2013) R: A language and environment for statistical computing, 302nd edn. Foundation for Statistical Computing, Vienna
Rasband WS (1997–2014) ImageJ. 1.47v edn. U.S. National Institutes of Health, Bethesda, Maryland, US
RStudio (2012) RStudio: Integrated development environment for R, 098501st edn. RStudio, Boston
Ryland JS (1962) The association between polyzoa and algal substrata. J Anim Ecol 31:331–338
Ryland JS (1965) Polyzoa (Bryozoa). Order Cheilostomata, cyphonautes larvae. In: Fiches d'identification du zooplancton, vol 107. Conseil Internat. pour l'Exploration de la Mer, Copenhagen, p 6
Ryland JS, Stebbing ARD (1971) Settlement and orientated growth in epiphytic and epizoic bryozoans. In: Crisp D (ed) Fourth European marine biology symposium. Cambridge University Press, Cambridge, pp 105–123
Saier B, Chapman AS (2005) Crusts of the alien bryozoan Membranipora membranacea can negatively impact spore output from native kelps (). Bot Mar 47:265–271
Saunders M, Metaxas A (2008) High recruitment of the introduced bryozoan Membranipora membranacea is associated with kelp bed defoliation in Nova Scotia, Canada. Ma Ecol Prog Ser 369:139–151
Saunders M, Metaxas A (2009) Population dynamics of a nonindigenous epiphytic bryozoan Membranipora membranacea in the western North Atlantic: effects of kelp substrate. Aquat Biol 8:83–94
Seed R, O'Connor RJ (1981) Community organization in marine algal epifaunas. Ann Rev Ecol Systemat 12:49–74
Sjøtun K (1993) Seasonal lamina growth in two age groups of Laminaria saccharina (L.) Lamour. in western Norway. Bot Mar 36:433–441
Yorke AF, 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. Mar Biol 158:2299–2311
Yoshioka PM (1982) Predator-induced polymorphism in the bryozoan Membranipora membranacea (L.). J Exp Mar Biol Ecol 61:233–242
Acknowledgments
This study was a part of the project EXPLOIT, funded by the Research Council of Norway (project no. 216201/E40). Thanks to the Institute of Marine Research and Seaweed Energy Solutions (SES) for providing environmental data (current speed and directions) at the location in Western Norway and Mid-Norway, respectively. We are grateful to Marine Harvest and SES for kindly providing research facilities and vessels and for all their practical support. We would also thank the reviewers for their constructive and helpful feedback.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Førde, H., Forbord, S., Handå, A. et al. Development of bryozoan fouling on cultivated kelp (Saccharina latissima) in Norway. J Appl Phycol 28, 1225–1234 (2016). https://doi.org/10.1007/s10811-015-0606-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-015-0606-5