Skip to main content
×
Home

Essence of the patterns of cover and richness of intertidal hard bottom communities: a pan-European study

  • Jonne Kotta (a1), Helen Orav-Kotta (a1), Holger Jänes (a1), Herman Hummel (a2), Christos Arvanitidis (a3), Pim Van Avesaath (a2), Guy Bachelet (a4), Lisandro Benedetti-Cecchi (a5), Natalia Bojanić (a6), Serena Como (a7), Stefania Coppa (a7), Jennifer Coughlan (a8), Tasman Crowe (a8), Martina Dal Bello (a5), Steven Degraer (a9), Jose Antonio Juanes De La Pena (a10), Valentina Kirienko Fernandes De Matos (a11), Free Espinosa (a12), Sarah Faulwetter (a3), Matt Frost (a13), Xabier Guinda (a10), Emilia Jankowska (a14), Jérôme Jourde (a15), Francis Kerckhof (a9), Nicolas Lavesque (a4), Jean-Charles Leclerc (a16) (a17), Paolo Magni (a7), Christina Pavloudi (a3), Maria Luiza Pedrotti (a18), Ohad Peleg (a19), Angel Pérez-Ruzafa (a20), Araceli Puente (a10), Pedro Ribeiro (a11), Gil Rilov (a19), Maria Rousou (a21), Tomas Ruginis (a22), Teresa Silva (a23), Nathalie Simon (a16) (a17), Isabel Sousa-Pinto (a24), Jesús Troncoso (a25), Jan Warzocha (a26) and Jan Marcin Weslawski (a14)...
Abstract

Coastal ecosystems are highly complex and driven by multiple environmental factors. To date we lack scientific evidence for the relative contribution of natural and anthropogenic drivers for the majority of marine habitats in order to adequately assess the role of different stressors across the European seas. Such relationship can be investigated by analysing the correlation between environmental variables and biotic patterns in multivariate space and taking into account non-linearities. Within the framework of the EMBOS (European Marine Biodiversity Observatory System) programme, hard bottom intertidal communities were sampled in a standardized way across European seas. Links between key natural and anthropogenic drivers and hard bottom communities were analysed using Boosted Regression Trees modelling. The study identified strong interregional variability and showed that patterns of hard bottom macroalgal and invertebrate communities were primarily a function of tidal regime, nutrient loading and water temperature (anomalies). The strength and shape of functional form relationships varied widely however among types of organisms (understorey algae composing mostly filamentous species, canopy-forming algae or sessile invertebrates) and aggregated community variables (cover or richness). Tidal regime significantly modulated the effect of nutrient load on the cover and richness of understorey algae and sessile invertebrates. In contrast, hydroclimate was more important for canopy algae and temperature anomalies and hydroclimate separately or interactively contributed to the observed patterns. The analyses also suggested that climate-induced shifts in weather patterns may result in the loss of algal richness and thereby in the loss of functional diversity in European hard bottom intertidal areas.

Copyright
Corresponding author
Correspondence should be addressed to: J. Kotta, Estonian Marine Institute, University of Tartu, Tallinn, Estonia Email: jonne@sea.ee
References
Hide All
Abrams P.A. (1995) Monotonic or unimodal diversity-productivity gradients: what does competition theory predict? Ecology 76, 20192027.
Armstrong R.L. and Knowles K. (2010) ISLSCP II global sea ice concentration. In Hall F.G., Collatz G., Meeson B., Los S., De Colstoun E.B. and Landis D. (eds) ISLSCP initiative II collection. Data set. Available online [http://daac.ornl.gov/] from Oak Ridge, Tennessee, USA: Oak Ridge National Laboratory Distributed Active Archive Center. doi: 10.3334/ORNLDAAC/981.
Arnold M., Teagle H., Brown M.P. and Smale D.A. (2016) The structure of biogenic habitat and epibiotic assemblages associated with the global invasive kelp Undaria pinnatifida in comparison to native macroalgae. Biological Invasions 18, 661676.
Bird C.E., Franklin E.C., Smith C.M. and Toonen R.J. (2013) Between tide and wave marks: a unifying model of physical zonation on littoral shores. PeerJ 1, e154.
Bonsdorff E. and Pearson T.H. (1999) Variation in the sublittoral macrozoobenthos of the Baltic Sea along environmental gradients: a functional group approach. Australian Journal of Ecology 24, 312326.
Britton-Simmons K.H. (2006) Functional group diversity, resource preemption and the genesis of invasion resistance in a community of marine algae. Oikos 113, 395401.
Bulleri F., Benedetti-Cecchi L., Cusson M., Maggi E., Arenas F., Aspden R., Bertocci I., Crowe T.P., Davoult D., Eriksson B.K., Fraschetti S., Golléty C., Griffin J., Jenkins S.R., Kotta J., Kraufvelin P., Molis M., Sousa Pinto I., Terlizzi A., Valdivia N. and Paterson D.M. (2012) Temporal stability of European rocky shore assemblages: variation across a latitudinal gradient and the role of habitat-formers. Oikos 121, 18011809.
Conley D.J., Carstensen J., Aigars J., Axe P., Bonsdorff E., Eremina T., Haahti B.M., Humborg C., Jonsson P., Kotta J., Lännegren C., Larsson U., Maximov A., Rodriguez Medina M., Lysiak-Pastuszak E., Remeikaité-Nikiené N., Walve J., Wilhelms S. and Zillén L. (2011) Hypoxia is increasing in the coastal zone of the Baltic Sea. Environmental Science and Technology 45, 67776783.
Connell S.D. and Irving A.D. (2008) Integrating ecology with biogeography using landscape characteristics: a case study of subtidal habitat across continental Australia. Journal of Biogeography 35, 16081621.
Copertino M.S., Connell S.D. and Cheshire A. (2005) Prevalence and production of turf-forming algae on a temperate subtidal coast. Phycologia 43, 241248.
Crowder L. and Norse E. (2008) Essential ecological insights for marine ecosystem-based management and marine spatial planning. Marine Policy 32, 772778.
Crowe T.P., Cusson M., Bulleri F., Davoult D., Arenas F., Aspden R., Benedetti-Cecchi L., Bevilacqua S., Davidson I., Defew E., Fraschetti S., Golléty C., Griffin J.N., Herkül K., Kotta J., Migné A., Molis M., Nicol S.K., Noël L.M.-L.J., Sousa Pinto I., Valdivia N., Vaselli S. and Jenkins S.R. (2013) Large-scale variation in combined impacts of canopy loss and disturbance on community structure and ecosystem functioning. PLoS ONE 8, e66238.
Dal Bello M., Leclerc J.-C., Benedetti-Cecchi L., Arvanitidis C., van Avesaath P., Bachelet G., Bojanić N., Como S., Coppa S., Coughlan J., Crowe T., Degraer S., Espinosa F., Faulwetter S., Frost M., Guinda X., Ikauniece A., Jankowska E., Jourde J., Kerckhof F., Kotta J., Lavesque N., de Lucia A., Magni P., Fernandes de Matos V.K., Orav-Kotta H., Pavloudi C., Pedrotti M.L., Peleg O., de la Pena J.A.J., Puente A., Ribeiro P., Rigaut-Jalabert F., Rilov G., Rousou M., Rubal M., Ruginis T., Pérez-Ruzafa A., Silva T., Simon N., Sousa-Pinto I., Troncoso J., Warzocha J., Weslawski J.M. and Hummel H. (2016) Consistent patterns of spatial variability between Atlantic and Mediterranean rocky shores. Journal of the Marine Biological Association of the United Kingdom, In press.
Danovaro R., Canals M., Gambi C., Heussner S., Lampadariou N. and Vanreusel A. (2009) Exploring benthic biodiversity patterns and hotspots on European margin slopes. Oceanography 22, 1625.
Dayton P.K. (1971) Competition, disturbance, and community organization: the provision and subsequent utilization of space in a rocky intertidal community. Ecological Monographs 41, 351389.
Dayton P.K. (1975) Experimental evaluation of ecological dominance in a rocky intertidal algal community. Ecological Monographs 45, 137159.
Denny M.W., Miller L.P., Stokes M.D., Hunt L.J.H. and Helmuth B.S.T. (2003) Extreme water velocities: topographical amplification of wave-induced flow in the surf zone of rocky shores. Limnology and Oceanography 48, 18.
Diez I., Secilla A., Santolaria A., and Gorostiaga J.M. (1999) Phytobenthic intertidal community structure along an environmental pollution gradient. Marine Pollution Bulletin 38, 463472.
Elith J., Graham C.H., Anderson R.P., Dudík M., Ferrier S., Guisan A., Hijmans R.J., Huettmann F., Leathwick J.R., Lehmann A., Li J., Lohmann L.G., Loiselle B.A., Manion G., Moritz C., Nakamura M., Nakazawa Y., Mc Overton J.C.M., Peterson Townsend A., Phillips S.J., Richardson K., Scachetti-Pereira R., Schapire R.E., Soberón J., Williams S., Wisz M.S. and Zimmermann N.E. (2006) Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29, 129151.
Elith J., Kearney M. and Phillips S. (2010) The art of modelling range-shifting species. Methods in Ecology and Evolution 1, 330342.
Elith J., Leathwick J.R. and Hastie T. (2008) A working guide to boosted regression trees. Journal of Animal Ecology 77, 802813.
Espinosa-Romero M.J., Chan K.M.A., McDaniels T. and Dalmer D.M. (2011) Structuring decision-making for ecosystem-based management. Marine Policy 35, 575583.
Field C.B., Behrenfeld M.J., Randerson J.T. and Falkowski P. (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281, 237240.
Golléty C., Migné A. and Davoult D. (2008) Benthic metabolism on a sheltered rocky shore: role of the canopy in the carbon budget. Journal of Phycology 44, 11461153.
Gorostiaga J.M. and Diez I. (1996) Changes in the sublittoral benthic marine macroalgae in the polluted area of Abra de Bilbao and proximal coast (Northern Spain). Marine Ecology Progress Series 130, 157167.
Goulletquer P., Gros P., Boeuf G. and Weber J. (2014) Biodiversity in the marine environment. Amsterdam: Springer.
Guenther R.J. and Martone P.T. (2014) Physiological performance of intertidal coralline algae during a simulated tidal cycle. Journal of Phycology 50, 310321.
Halpern B.S., Walbridge S., Selkoe K.A., Kappel C.V., Micheli F., D'Agrosa C., Bruno J.F., Casey K.S., Ebert C., Fox H.E., Fujita R., Heinemann D., Lenihan H.S., Madin E.M.P., Perry M.T., Selig E.R., Spalding M., Steneck R. and Watson R. (2008) A global map of human impact on marine ecosystems. Science 319, 948952.
Hastie T., Tibshirani R. and Friedman J.H. (2009) The elements of statistical learning: data mining, inference, and prediction. New York, NY: Springer-Verlag.
Hawkins S.J. and Hartnoll R.G. (1985) Factors determining the upper limits of intertidal canopy-forming algae. Marine Ecology Progress Series 20, 265271.
Heaven C.S. and Scrosati R.A. (2008) Benthic community composition across gradients of intertidal elevation, wave exposure, and ice scour in Atlantic Canada. Marine Ecology Progress Series 369, 1323.
Helmuth B. and Denny M.W. (2003) Predicting wave exposure in the rocky intertidal zone: do bigger waves always lead to larger forces? Limnology and Oceanography 48, 13381345.
Herkül K., Kotta J., Kutser T. and Vahtmäe E. (2013) Relating remotely sensed optical variability to marine benthic biodiversity. PLoS ONE 8, e55624.
Holyoak M., Leibold M.A., Moquet N., Holt R.D. and Hoopes M.F. (2005) Metacommunities: a framework for large-scale community ecology. In Holyoak M., Leibold M.A., Moquet N. and Holt R.D. (eds) Metacommunities: spatial dynamics and ecological communities. Chicago, IL: University of Chicago Press, pp. 134.
Hoogwijk M., Faaij A., van den Broek R., Berndes G., Gielen D. and Turkenburg W. (2003) Exploration of the ranges of the global potential of biomass for energy. Biomass and Bioenergy 25, 119133.
Howarth R.W., Billen G., Swaney D., Townsend A., Jaworski N., Lajtha K., Downing J.A., Elmgren R., Caraco N., Jordan T., Berendse F., Freney J., Kudeyarov V., Murdoch P. and Zhu Z-L. (1996) Regional nitrogen budgets and riverine N & P fluxes for the drainages to the North Atlantic Ocean: natural and human influences. Biogeochemistry 35, 75139.
Hubbert M.K. (1949) Energy from fossil fuels. Science 109, 103109.
Johnston E.L., Keough M. and Qian P. (2002) Maintenance of species dominance through pulse disturbances to a sessile marine invertebrate assemblage in Port Shelter, Hong Kong. Marine Ecology Progress Series 226, 103114.
Jutterström S., Andersson H.C., Omstedt A. and Malmaeus J.M. (2014) Multiple stressors threatening the future of the Baltic Sea–Kattegat marine ecosystem: implications for policy and management actions. Marine Pollution Bulletin 86, 468480.
Kaiser M.J., Attrill M.J., Jennings S., Thomas D.N., Barnes D.K.A., Brierley A.S., Hiddink J.G., Kaartokallio H., Polunin N.V.C. and Raffaelli D.G. (2011) Marine ecology: processes, systems, and impacts. Oxford: Oxford University Press.
Karydis M. and Kitsiou D. (2012) Eutrophication and environmental policy in the Mediterranean Sea: a review. Environmental Monitoring and Assessment 184, 49314984.
Kotta J., Kutser T., Teeveer K., Vahtmäe E. and Pärnoja M. (2013) Predicting species cover of marine macrophyte and invertebrate species combining hyperspectral remote sensing, machine learning and regression techniques. PLoS ONE 8, e63946.
Kotta J., Möller T., Orav-Kotta H. and Pärnoja M. (2014) Realized niche width of a brackish water submerged aquatic vegetation under current environmental conditions and projected influences of climate change. Marine Environmental Research 102, 88101.
Kotta J. and Witman J. (2009) Regional-scale patterns. In Wahl M. (ed.) Marine hard bottom communities. Berlin: Springer-Verlag, pp. 8999.
Kraufvelin P., Ruuskanen A.T., Nappu N. and Kiirikki M. (2007) Winter colonisation and succession of filamentous macroalgae on artificial substrates and possible relationships to Fucus vesiculosus settlement in early summer. Estuarine Coastal and Shelf Science 72, 665674.
Lima F.P., Ribeiro P.A., Queiroz N., Hawkins S.J. and Santos A.M. (2007a) Do distributional shifts of northern and southern species of algae match the warming pattern? Global Change Biology 13, 25922604.
Lima F.P., Ribeiro P.A., Queiroz N., Xavier R., Tarroso P., Hawkins S.J. and Santos A.M. (2007b) Modelling past and present geographical distribution of the marine gastropod Patella rustica as a tool for exploring responses to environmental change. Global Change Biology 13, 20652077.
Long R.D., Charles A. and Stephenson R.L. (2015) Key principles of marine ecosystem-based management. Marine Policy 57, 5360.
Maestre F.T., Quero J.L., Gotelli N.J., Escudero A., Ochoa V., Delgado-Baquerizo M., García-Gómez M., Bowker M.A., Soliveres S., Escolar C., García-Palacios P., Berdugo M., Valencia E., Gozalo B., Gallardo A., Aguilera L., Arredondo T., Blones J., Boeken B., Bran D., Conceição A.A., Cabrera O., Chaieb M., Derak M., Eldridge D.J., Espinosa C.I., Florentino A., Gaitán J., Gatica M.G., Ghiloufi W., Gómez-González S., Gutiérrez J.R., Hernández R.M., Huang X., Huber-Sannwald E., Jankju M., Miriti M., Monerris J., Mau R.L., Morici E., Naseri K., Ospina A., Polo V., Prina A., Pucheta E., Ramírez-Collantes D.A., Romão R., Tighe M., Torres-Díaz C., Val J., Veiga J.P., Wang D. and Zaady E. (2012) Plant species richness and ecosystem multifunctionality in global drylands. Science 335, 214218.
Menge B.A. and Sutherland J.P. (1987) Community regulation: variation in disturbance, competition and predation in relation to environmental stress and recruitment. American Naturalist 130, 730757.
Narayanaswamy B.E., Coll M., Danovaro R., Davidson K., Ojaveer H. and Renaud P.E. (2013) Synthesis of knowledge on marine biodiversity in European Seas: from census to sustainable management. PLoS ONE 8, e58909.
Orav-Kotta H. and Kotta J. (2004) Food and habitat choice of the isopod Idotea baltica in the northeastern Baltic Sea. Hydrobiologia 514, 7985.
Pedersen M.F. and Borum J. (1996) Nutrient control of algal growth in estuarine waters. Nutrient limitation and the importance of nitrogen requirements and nitrogen storage among phytoplankton and species of macroalgae. Marine Ecology Progress Series 142, 261272.
Peterson A.T. (2003) Predicting the geography of species’ invasions via ecological niche modeling. Quarterly Review of Biology 78, 419433.
Råberg S. and Kautsky L. (2007) A comparative biodiversity study of the associated fauna of perennial fucoids and filamentous algae. Estuarine, Coastal and Shelf Science 73, 249258.
Ramos E., Puente A., Guinda X. and Juanes J.A. (2016a) A hierarchical classification system along the NE Atlantic coast: focusing on the local scale (Cantabria, N Spain). European Journal of Phycology, in press. doi: 10.1080/09670262.2016.1221469.
Ramos E., Puente A. and Juanes J. (2016b) An ecological classification of rocky shores at a regional scale: a predictive tool for management of conservation values. Marine Ecology 37, 311328.
RDC Team (2013) R: a language and environment for statistical computing. Vienna: The R Foundation for Statistical Computing. Available at: http://www.r-project.org/.
Rees H.L., Pendle M.A., Waldock R., Limpenny D.S. and Boyd S.E. (1999) A comparison of benthic biodiversity in the North Sea, English Channel, and Celtic Seas. ICES Journal of Marine Science 56, 228246.
Ricklefs R.E. and Schluter D. (1993) Species diversity: regional and historical influences. In Ricklefs R.E. and Schluter D. (eds) Species diversity in ecological communities: historical and geographical perspectives. Chicago, IL: University of Chicago Press, pp. 350364.
Roy K., Jablonski D., Valentine J.W. and Rosenberg G. (1998) Marine latitudinal diversity gradients: tests of causal hypotheses. Proceedings of the National Academy of Sciences USA 95, 36993702.
Russell R., Wood S.A., Allison G. and Menge B.A. (2006) Scale, environment and trophic status: the context dependency of community saturation in rocky intertidal communities. American Naturalist 167, E158E170.
Sandman A.N., Wikström S.A., Blomqvist M., Kautsky H. and Isaeus M. (2013) Scale-dependent influence of environmental variables on species distribution: a case study on five coastal benthic species in the Baltic Sea. Ecography 36, 354363.
Schiele K., Darr A., Zettler M.L., Berg T., Blomqvist M., Daunys D., Jermakovs V., Korpinen S., Kotta J., Nygård H., von Weber M., Voss J. and Warzocha J. (2016) Rating species sensitivity throughout gradient systems – a consistent approach for the Baltic Sea. Ecological Indicators 61, 447455. doi: 10.1016/j.ecolind.2015.09.046.
Smale D.A., Burrows M.T., Evans A.J., King N., Sayer M.D.J., Yunnie A.L.E. and Moore P.J. (2016) Linking environmental variables with regional-scale variability in ecological structure and standing stock of carbon within kelp forests in the United Kingdom. Marine Ecology Progress Series 542, 7995.
Smale D.A., Burrows M.T., Moore P., O'Connor N. and Hawkins S.J. (2013) Threats and knowledge gaps for ecosystem services provided by kelp forests: a northeast Atlantic perspective. Ecology and Evolution 3, 40164038.
Smale D.A. and Wernberg T. (2013) Extreme climatic event drives range contraction of a habitat-forming species. Proceedings of the Royal Society B 280, 20122829.
Soberon J. and Peterson A.T. (2005) Interpretation of models of fundamental ecological niches and species’ distributional areas. Biodiversity Informatics 2, 110.
Stackhouse P.W. and Gupta S.K. (2012) ISLSCP II cloud and meteorology parameters. In Hall F.G., Collatz G., Meeson B., Los S., De Colstoun E.B. and Landis D. (eds) ISLSCP Initiative II Collection. Data set. Available online [http://daac.ornl.gov/] from Oak Ridge, Tennessee, USA: Oak Ridge National Laboratory Distributed Active Archive Center. doi: 10.3334/ORNLDAAC/1073.
Stephenson T.A. and Stephenson A. (1972) Life between tidemarks on rocky shores. San Francisco, CA: WH Freeman.
Tett P., Gilpin L., Svendsen H., Erlandsson C.P., Larsson U., Kratzer S., Fouilland E., Janzen C., Lee J.-Y., Grenz C., Newton A., Ferreira J.G., Fernandes T. and Scory S. (2003) Eutrophication and some European waters of restricted exchange. Continental Shelf Research 23, 16351671.
Thorner J., Kumar L. and Smith S.D.A. (2014) Impacts of climate-change-driven sea level rise on intertidal rocky reef habitats will be variable and site specific. PLoS ONE 9, e86130.
Tomanek L. and Helmuth B. (2002) Physiological ecology of rocky intertidal organisms: a synergy of concepts. Integrative and Comparative Biology 42, 771775.
Underwood A.J. (1978) A refutation of critical tidal levels as determinants of the structure of intertidal communities on British shores. Journal of Experimental Marine Biology and Ecology 33, 261276.
Underwood A.J. and Jernakoff P. (1981) Effects of interactions between algae and grazing gastropods on the structure of a low-shore intertidal algal communities. Oecologia 48, 221233.
Valiela I., Mcclelland J., Hauxwell J., Behr P.J., Hersh D. and Foreman K. (1988) Macroalgal blooms in shallow estuaries: controls and ecophysiological and ecosystem consequences. Limnology and Oceanography 42, 11051118.
Wernberg T., Smale D.A., Tuya F., Thomsen M.S., Langlois T.J., de Bettignies T., Bennett S. and Rousseaux C.S. (2013) An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nature Climate Change 3, 7882.
Wernberg T., Thomsen M.S., Tuya F., Kendrick G.A., Staehr P.A. and Toohey B.D. (2010) Decreasing resilience of kelp beds along a latitudinal temperature gradient: potential implications for a warmer future. Ecology Letters 13, 685694.
Weslawski J.M., Wiktor J. Jr and Kotwicki L. (2010) Increase in biodiversity in the arctic rocky littoral, Sorkappland, Svalbard, after 20 years of climate warming. Marine Biodiversity 40, 123130.
Whittaker R.O. (1974) Communities and ecosystems. New York, NY: Macmillan.
Wikström S.A. and Kautsky L. (2007) Structure and diversity of invertebrate communities in the presence and absence of canopy-forming Fucus vesiculosus in the Baltic Sea. Estuarine Coastal and Shelf Science 72, 168176.
Zacharias M.A. and Roff J.C. (2001) Explanations of patterns of intertidal diversity at regional scales. Journal of Biogeography 28, 471483.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Journal of the Marine Biological Association of the United Kingdom
  • ISSN: 0025-3154
  • EISSN: 1469-7769
  • URL: /core/journals/journal-of-the-marine-biological-association-of-the-united-kingdom
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 12
Total number of PDF views: 88 *
Loading metrics...

Abstract views

Total abstract views: 650 *
Loading metrics...

* Views captured on Cambridge Core between 4th October 2016 - 25th November 2017. This data will be updated every 24 hours.