Accessible Requires Authentication Published by De Gruyter August 8, 2013

Changes in brown seaweed distributions in Lough Hyne, SW Ireland: a long-term perspective

Cynthia D. Trowbridge, Colin Little, Brittney Dlouhy-Massengale, Penny Stirling and Graham M. Pilling
From the journal Botanica Marina

Abstract

Distributions of brown seaweeds (Phaeophyceae: Fucales, Laminariales and Tilopteridales) were surveyed in 2011 in Europe’s first marine reserve, Lough Hyne in SW Ireland, and compared with distributions from three historical surveys (1930, 1955 and 1980). The most salient phycological differences were the incursion of the low intertidal and shallow subtidal species Fucus serratus, Himanthalia elongata and Saccharina latissima into the north basin of the marine reserve after the recent mass mortality of the purple urchin (Paracentrotus lividus). Monitoring surveys (1990–2012) at ten sites in the lough indicated that populations of S. latissima peaked in 1994, abruptly crashed in 1996 and then slowly recovered. As well as documenting the expansion of kelp, our annual, whole-lough snorkel surveys (2004–2012) demonstrated the recent proliferation of the introduced Sargassum muticum and native Cystoseira foeniculacea. Although the causal role of top-down factors (fishing ban and/or urchin population crash), bottom-up factors (nutrient enhancement), climatic variables (warming vs. episodic cooling) and pathogens (urchin and algal) is being widely debated, decadal-scale and inter-annual changes are clearly detectable and most consistent with a release from herbivory within the marine protected area.


Corresponding author: Cynthia D. Trowbridge, Oregon Institute of Marine Biology, PO Box 5389, Charleston, OR 97420, USA

We are grateful to Declan O’Donnell and Patrick Graham of the National Parks and Wildlife Service for permission to carry out scientific research in the Lough Hyne Marine Reserve. We are particularly grateful for help received from the late warden of the lough, John Bohane, and we were much helped by information and assistance from our UCC colleague Rob McAllen and many European colleagues. Hal Ross and the Hunrunrs provided continual encouragement and support throughout the project. Over the period of the surveys, we are indebted to the following colleagues (listed alphabetically) for their field help: K. Bennett, M. Consalvey, T. Crowe, T. Horton, A. Laferriere, J. Lord, A. Miles, D. Morritt, M. Paulling, S. Phillips, S. Schroeder, L. Teagle, J. Thain, V. Thain, G. Williams and M. Wolf. We thank two anonymous reviewers and Matt Dring for their valuable and constructive comments on an earlier draft of this paper. This material is based upon work partially supported by the U.S. National Science Foundation under Grant No. 0211186 and 1130978-OISE as well as the National Parks and Wildlife Service of Ireland. Any opinions, findings and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation.

References

Andrew, N.L. 1991. Changes in subtidal habitat following mass mortality of sea urchins in Botany Bay, New South Wales. Austr. J. Ecol. 16: 353–362. Search in Google Scholar

Andrews, J.H. 1977. Observations on the pathology of seaweeds in the Pacific Northwest. Can. J. Bot. 55: 10191027. Search in Google Scholar

Barry, J.P., C.H. Baxter, R.D. Sagarin and S.E. Gilman. 1995. Climate-related, long-term faunal changes in a California rocky intertidal community. Science 267: 672–675. Search in Google Scholar

Bishop, G. 2003. The ecology of the rocky shores of Sherkin Island – A twenty-year perspective. Sherkin Island Marine Station, Sherkin Island, County Cork, Ireland. pp. 305. Search in Google Scholar

Capasso, E., S.R. Jenkins, M. Frost and H. Hinz. 2010. Investigation of benthic community change over a century-wide scale in the western English channel. J. Mar. Biol. Assoc. U.K. 90: 1161–1172. Search in Google Scholar

Díez, I., A. Santolaria and J.M. Gorostiaga. 2003. The relationship of environmental factors to the structure and distribution of subtidal seaweed vegetation of the western Basque coast (N Spain). Estuar. Coast. Shelf Sci. 56: 1041–1054. Search in Google Scholar

Ebling, F.J., M.A. Sleigh, J.F. Sloane and J.A. Kitching. 1960. The ecology of Lough Ine. VII. Distribution of some common plants and animals of the littoral and shallow sublittoral regions. J. Ecol. 48: 29–53. Search in Google Scholar

Ellertsdóttir, E. and A.F. Peters. 1997. High prevalence of infection by endophytic brown algae in populations of Laminaria spp. (Phaeophyceae). Mar. Ecol. Prog. Ser. 146: 135–143. Search in Google Scholar

Eriksson, B.K., G. Johansson and P. Snoeijs. 1998. Long-term changes in the sublittoral zonation of brown algae in the southern Bothnian Sea. Eur. J. Phycol. 33: 241–249. Search in Google Scholar

Eriksson, B.K., G. Johansson and P. Snoeijs. 2002. Long-term changes in the macroalgal vegetation of the inner Gullmar Fjord, Swedish Skagerrak coast. J. Phycol. 38: 284–296. Search in Google Scholar

Frid, C.L.J. and J.A. Kitching. 1988. The Laminaria forest of Barloge Creek, Lough Hyne, Ireland, with special reference to the importance of wave action. Irish Nat. J. 22: 463–469. Search in Google Scholar

Gachon, C.M.M., T. Sime-Ngando, M. Strittmatter, A. Chambouvet and G.H. Kim. 2010. Algal diseases: spotlight on a black box. Trends Plant Sci. 15: 633–640. Search in Google Scholar

Göransson, P. 2002. Petersen’s benthic macrofauna stations revisited in the Öresund area (southern Sweden) and species composition in the 1990s – signs of decreased biological variation. Sarsia 87: 263–280. Search in Google Scholar

Guiry, M.D. and G.M. Guiry. 2012. AlgaeBase. World-Wide Electronic Publication, National University of Ireland, Galway. Available at: http://www.algaebase.org (accessed November 23, 2012). Search in Google Scholar

Hanel, R. 2002. Recovery of fucacean associations and associated fish assemblages in the vicinity of Rovinj, Istrian coast, northern Adriatic Sea. Period. Biol. 104: 159–163. Search in Google Scholar

Hawkins, S.J., L.B. Firth, M. McHugh, E.S. Poloczanska, R.J.H. Herbert, M.T. Burrows, M.A. Kendall, P.J. Moore, R.C. Thompson, S.R. Jenkins, D.W. Sims, M.J. Genner and N. Mieszkowska. 2013. Data rescue and re-use: recycling old information to address new policy concerns. Mar. Pol. 42: 91–98. Search in Google Scholar

Helmuth, B., N. Mieszkowska, P. Moore and S.J. Hawkins. 2006. Living on the edge of two changing worlds: forecasting the responses of rocky intertidal ecosystems to climate change. Ann. Rev. Ecol. Evol. Syst. 37: 373–404. Search in Google Scholar

Jessopp, M. 2011. Nutrient enrichment and increased phytoplankton biomass in Lough Hyne. Is Lough Hyne eutrophic? In: (J. Davenport and R. McAllen, eds.) Lough Hyne Marine Reserve @ 30. A conference reflecting on the past, present and future directions of research at the lough. School of BEES, June 3, 2011. University College Cork, County Cork, Ireland. p. 17. Search in Google Scholar

Johansson, G., B.K. Eriksson, M. Pedersén and P. Snoeijs. 1998. Long-term changes of macroalgal vegetation in the Skagerrak area. Hydrobiologia 385: 121–138. Search in Google Scholar

Johnson, M.P., M.J. Costello and D. O’Donnell. 1995. The nutrient economy of a marine inlet: Lough Hyne, south west Ireland. Ophelia 41: 137–151. Search in Google Scholar

Johnson, M.P., M. Jessopp, O.R. Mulholland, C. McInerney, R. McAllen, A.L. Allcock and T.P. Crowe. 2008. What is the future for marine protected areas in Irish waters? Proc. Royal Irish Acad., B 108: 9–15. Search in Google Scholar

Kautsky, N., H. Kautsky, U. Kautsky and M. Waern. 1986. Decreased depth penetration of Fucus vesiculosus (L.) since the 1940’s indicates eutrophication of the Baltic Sea. Mar. Ecol. Prog. Ser. 28: 1–8. Search in Google Scholar

Kitching, J.A. 1987. Ecological studies at Lough Hyne. Adv. Ecol. Res. 17: 115–189. Search in Google Scholar

Kitching, J.A. and F.J. Ebling. 1961. The ecology of Lough Ine. XI. The control of algae by Paracentrotus lividus (Echinoidea). J. Anim. Ecol. 30: 373–383. Search in Google Scholar

Kitching, J.A. and V.M. Thain. 1983a. The ecological impact of the sea urchin Paracentrotus lividus (Lamarck) in Lough Ine, Ireland. Phil. Trans. R. Soc. Lond., B 300: 513–552. Search in Google Scholar

Kitching, J.A. and V.M. Thain. 1983b. Erratum: the ecological impact of the sea urchin Paracentrotus lividus (Lamarck) in Lough Ine, Ireland. Phil. Trans. R. Soc. Lond., B 301: 429. Search in Google Scholar

Kitching, J.A., A. McLeod, L. Muntz, T. Norton, F.J. Ebling, J. Gamble, K. Hiscock and R. Hoare. 1974. Work in progress at Lough Ine. Proc. Challenger Soc. 4: 39. Search in Google Scholar

Larkum, A.W.D. 1972. Frond structure and growth in Laminaria hyperborea. J. Mar. Biol. Assoc. U.K. 52: 405–418. Search in Google Scholar

Larkum, A.W.D. and T.A. Norton. 1968. An investigation of the vertical distribution of seaweeds in the Whirlpool area of Lough Ine. Br. Phycol. Bull. 3: 601–602. Search in Google Scholar

Lein, T.E., K. Sjøtun and S. Wakili. 1991. Mass-occurrence of a brown filamentous endophyte in the lamina of the kelp Laminaria hyperborea (Gunnerus) Foslie along the southwestern coast of Norway. Sarsia 76: 187193. Search in Google Scholar

Lima, F.P., P.A. Ribeiro, N. Queiroz, S.J. Hawkins and A.M. Santos. 2007. Do distributional shifts of northern and southern species of algae match the warming pattern? Global Change Biol. 13: 2592–2604. Search in Google Scholar

Little, C. 2011. Dabbling in the waters: 55 years in Lough Hyne’s intertidal and shall subtidal. In: (J. Davenport and R. McAllen, eds.) Lough Hyne Marine Reserve @ 30. A conference reflecting on the past, present and future directions of research at the lough. School of BEES, June 3, 2011. University College Cork, County Cork, Ireland. p.12. Search in Google Scholar

Little C., D. Morritt and P. Stirling. 1992. Changes in the shore fauna and flora of Lough Hyne. Irish Nat. J. 24: 87–95. Search in Google Scholar

Lundälv, T., C.S. Larsson and L. Axelsson. 1986. Long-term trends in algal-dominated rocky subtidal communities on the Swedish west coast – a transitional system? Hydrobiologia 142: 81–95. Search in Google Scholar

Maggs, C.A., M.T. Freamhainn and M.D. Guiry. 1983. A study of the marine algae of subtidal cliffs in Lough Hyne (Ine), Co. Cork. Proc. R. Irish Acad., 83B: 251–266. Search in Google Scholar

Mieszkowska, N., M.A. Kendall, S.J. Hawkins, R. Leaper, P. Williamson, N.J. Hardman-Mountford and A.J. Southward. 2006. Changes in the range of some common rocky shore species in Britain – a response to climate change? Hydrobiologia 555: 241–251. Search in Google Scholar

Miller, R.J. 1985. Succession in sea urchin and seaweed abundance in Nova Scotia, Canada. Mar. Biol. 84: 275–286. Search in Google Scholar

Navarrete, S.A., S. Gelcich and J.C. Castilla. 2010. Long-term monitoring of coastal ecosystems at Las Cruces, Chile: defining baselines to build ecological literacy in a world of change. Rev. Chil. Hist. Nat. 83: 143–157. Search in Google Scholar

Norton, T.A. 1969. Growth form and environment in Saccorhiza polyschides. J. Mar. Biol. Assoc. U.K. 49: 1025–1045. Search in Google Scholar

Norton, T.A. 1977. The value in ecological experimentation of paired species with contrasting distributions. Br. Phycol. J. 12: 121–122. Search in Google Scholar

Norton, T.A. 1978. The factors influencing the distribution of Saccorhiza polyschides in the region of Lough Ine. J. Mar. Biol. Assoc. U.K. 58: 527–536. Search in Google Scholar

Norton, T.A., K. Hiscock and J.A. Kitching. 1977. The ecology of Lough Ine: XX. The Laminaria forest at Carrigathorna. J. Ecol. 65: 919–941. Search in Google Scholar

O’Sullivan, D. and M. Emmerson. 2011. Marine reserve designation, trophic cascades and altered community dynamics. Mar. Ecol. Prog. Ser. 440: 115–125. Search in Google Scholar

Oliveira, E.C. and Y. Qi. 2003. Decadal changes in a polluted bay as seen from its seaweed flora: the case of Santos Bay in Brazil. AMBIO 32: 403–405. Search in Google Scholar

Paine, R.T. and A.C. Trimble. 2004. Abrupt community change on a rocky shore – biological mechanisms contributing to the potential formation of an alternative state. Ecol. Lett. 7: 441–445. Search in Google Scholar

Pearse, J.S. and A.H. Hines. 1979. Expansion of a central California kelp forest following the mass mortality of sea urchins. Mar. Biol. 51: 83–91. Search in Google Scholar

Peters, A.F. and B. Schaffelke. 1996. Streblonema (Ectocarpales, Phaeophyceae) infection in the kelp Laminaria saccharina (Laminariales, Phaeophyceae) in the western Baltic. Hydrobiologia 326/327: 111–116. Search in Google Scholar

Rees, T.K. 1931. Preliminary observations on the Phaeophyceae of Lough Hyne (Ine). J. Ecol. 19: 439–448. Search in Google Scholar

Rees, T.K. 1935. The marine algae of Lough Ine. J. Ecol. 23: 69–133. Search in Google Scholar

Renouf, L.P.W. 1931. Preliminary work of a new biological station (Lough Ine, Co. Cork, I.F.S.). J. Ecol. 19: 410–438. Search in Google Scholar

Renouf, L.P.W. and T. K. Rees. 1932. A note on experiments concerned with biotic factors of the sea-shore. Ann. Bot. 46: 1061–1062. Search in Google Scholar

Rindi, F. and M.D. Guiry. 2004. A long-term comparison of the benthic algal flora of Clare Island, County Mayo, western Ireland. Biodivers. Conserv 13: 471–492. Search in Google Scholar

Rindi, F., M.D. Guiry and C. Maggs. 2002. Checklist of the benthic marine algae of Clare Island. In: (A. Myers, ed.) New survey of Clare Island. Vol. 3: Marine intertidal ecology. Royal Irish Academy, Dublin. pp. 189–205. Search in Google Scholar

Roos, C., O. Rönnberg, J. Berglund and A. Alm. 2005. Long-term changes in macroalgal communities along ferry routes in a northern Baltic archipelago. Nord. J. Bot. 23: 247–259. Search in Google Scholar

Sagarin, R.D., J.P. Barry, S.E. Gilman and C.H. Baxter. 1999. Climate-related change in an intertidal community over short and long time scales. Ecol. Monogr. 69: 465–490. Search in Google Scholar

Sagarin, R.D., W.F. Gilly, C.H. Baxter, N. Burnett and J. Christensen. 2008. Remembering the Gulf: changes to the marine communities of the Sea of Cortez since the Steinbeck and Ricketts expedition of 1940. Front. Ecol. Environ. 6: 372–379. Search in Google Scholar

Scheibling, R. 1986. Increased macroalgal abundance following mass mortalities of sea urchins (Strongylocentrotus droebachiensis) along the Atlantic coast of Nova Scotia. Oecologia 68: 186–198. Search in Google Scholar

Simkanin, C., A.M. Power, A. Myers, D. McGrath, A. Southward, N. Mieszkowska, R. Leaper and R. O’Riordan. 2005. Using historical data to detect temporal changes in the abundances of intertidal species on Irish shores. J. Mar. Biol. Assoc. U.K. 85: 1329–1340. Search in Google Scholar

Svane, I. and F. Gröndahl. 1988. Epibioses of Gullmarsfjorden: an underwater stereophotographical transect analysis in comparison with the investigations of Gislén in 1926-29. Ophelia 28: 95–110. Search in Google Scholar

Taylor, R.B., M.A. Morrison and N.T. Shears. 2011. Establishing baselines for recovery in a marine reserve (Poor Knights Islands, New Zealand) using local ecological knowledge. Biol. Conserv. 144: 3038–3046. Search in Google Scholar

Thibaut, T., S. Pinedo, X. Torras and E. Ballesteros. 2005. Long-term decline of the populations of Fucales (Cystoseira spp. and Sargassum spp.) in the Albères coast (France, North-western Mediterranean). Mar. Pollut. Bull. 50: 1472–1489. Search in Google Scholar

Trowbridge C.D., C. Little, G.M. Pilling, P. Stirling and A. Miles. 2011. Decadal-scale changes in the shallow subtidal benthos of an Irish marine reserve. Bot. Mar. 54: 497–506. Search in Google Scholar

Received: 2013-4-9
Accepted: 2013-7-4
Published Online: 2013-08-08
Published in Print: 2013-08-01

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