The Future of Benthic Indicators: Moving up to the Intertidal

Abstract

The use of benthic indicators has increased dramatically during the last decades. The number of articles published on the subject, as well as the number of citations, has been particularly increasing since the early 90’s, notably in relation with the implementation of directives for the management of aquatic/marine ecosystems such as the Water Framework Directive and the Marine Strategy Framework Directive. Current benthic indicators suffer from severe drawbacks and their practical use is still discussed and might have reached a dead end. Indicators based on species composition are not totally satisfactory, mainly because they exhibit a high spatio-temporal variability (e.g. variable at both seasonal and pluri-annual scales) and are user-dependent (e.g. divergent results from US orEuropeexperts.) In turn, modifications of behaviour, metabolism, phenotype or stable isotopes composition in invertebrates usually occur at short time scales, compared to detectable changes in community composition, and makes their use particularly relevant as indicators of perturbation. It is argued in this paper that these functional indicators might be relatively quickly implemented in the intertidal, and represent an effective alternative to current benthic indicators.

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N. Spilmont, "The Future of Benthic Indicators: Moving up to the Intertidal," Open Journal of Marine Science, Vol. 3 No. 2A, 2013, pp. 76-86. doi: 10.4236/ojms.2013.32A008.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] M. L. Parry, O. F. Canziani, J. P. Palutikof, P. J. van der Linden and C. E. Hanson, “Climate Change 2007: Impacts, Adaptation and Vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change,” Cambridge University Press, Cambridge, 2007.
[2] P. M. Chapman, “Global Climate Change Means Never Going Home Again,” Marine Pollution Bulletin, Vol. 62, No. 11, 2011, pp. 2269-2270. doi:10.1016/j.marpolbul.2011.08.031
[3] X. Durrieu de Madron, C. Guieu, R. Sempéré, P. Conan, D. Cossa, F. d’Ortenzio, C. Estournel, F. Gazeau, C. Rabouille, L. Stemmann, S. Bonnet, F. Diaz, P. Koubbi, O. Radakovitch, M. Babin, M. Baklouti, C. BanconMontigni, S. Belviso, N. Bensoussan, B. Bonsang, I. Bouloubassi, C. Brunet, J.-F. Cadiou, F. Carlotti, M. Chami, S. Charmasson, B. Charrière, J. Dachs, D. Doxaran, J.-C. Dutay, F. Elbaz-Poulichet, M. Eléaume, F. Eyrolles, C. Fernandez, S. Fowler, P. Francour, J. C. Gaertner, R. Galzin, S. Gasparini, J.-F. Ghiglione, J.-L. Gonzalez, C. Goyet, L. Guidi, K. Guizien, L.-E. Heimbürger, S. H. M. Jacquet, W. H. Jeffrey, F. Joux, P. Le Hir, K. Leblanc, D. Lefèvre, C. Lejeusne, R. Lemé, M.-D. Loye-Pilot, M. Mallet, L. Méjanelle, F. Mélin, C. Mellon, B. Mérigot, P.-L. Merle, C. Migon, W. L. Miller, L. Mortier, B. Mostajir, L. Mousseau, T. Moutin, J. Para, T. Pérez, A. Petrenko, J.-C. Poggiale, L. Prieur, M. Pujo-Pay, PulidoVillena, P. Raimbault, A. P. Rees, C. Ridame, J.-F. Rontani, D. Ruiz Pino, M. A. Sicre, V. Taillandier, C. Tamburini, T. Tanaka, I. Taupier-Letage, M. Tedetti, P. Testor, H. Thébault, B. Thouvenin, F. Touratier, J. Tronczynski, C. Ulses, F. Van Wambeke, V. Vantrepotte, S. Vaz and R. Verney, “Marine Ecosystems’ Responses to Climatic and Anthropogenic Forcings in the Mediterranean,” Progress in Oceanography, Vol. 91, No. 2, 2011, pp. 97-166. doi:10.1016/j.pocean.2011.02.003
[4] C. J. M. Philippart, R. Anadón, R. Danovaro, J. W. Dippner, K. F. Drinkwater, S. J. Hawkins, T. Oguz, G. O’Sullivan and P. C. Reid, “Impacts of Climate Change on European Marine Ecosystems: Observations, Expectations and Indicators,” Journal of Experimental Marine Biology and Ecology, Vol. 400, No. 1-2, 2011, pp. 52-69. doi:10.1016/j.jembe.2011.02.023
[5] B. S. Halpern, S. Walbridge, K. A. Selkoe, C. V. Kappel, F. Micheli, C. D’Agrosa, J. F. Bruno, K. S. Casey, C. Ebert, H. E. Fox, R. Fujita, D. Heinemann, H. S. Lenihan, E. M. P. Madin, M. T. Perry, E. R. Selig, M. Spalding, R. Steneck and R. Watson, “A Global Map of Human Impact on Marine Ecosystems,” Science, Vol. 319, No. 5865, 2008, pp. 948-952. doi:10.1126/science.1149345
[6] I. Rombouts, G. Beaugrand, L. F. Artigas, J.-C. Dauvin, F. Gevaert, E. Goberville, D. Kopp, S. Lefebvre, C. Luczak, N. Spilmont, M. Travers-Trolet, C. M. Villanueva and R. R. Kirby, “Tools to Derive Indicators of Marine Ecosystem Structure and Functioning: Case Studies Using Direct Observations and Modelling Methods,” Ecological Indicators, Vol. 24, 2013, pp. 353-365. doi:10.1016/j.ecolind.2012.07.001
[7] S. Bevilacqua, S. Fraschetti, L. Musco, G. Guarnieri and A. Terlizzi, “Low Sensitiveness of Taxonomic Distinctness Indices to Human Impacts: Evidences Across Marine Benthic Organisms and Habitat Types,” Ecological Indicators, Vol. 11, No. 2, 2011, pp. 448-455. doi:10.1016/j.ecolind.2010.06.016
[8] R. J. Diaz, M. Solan and R. M. Valente, “A Review of Approaches for Classifying Benthic Habitats and Evaluating Habitat Quality,” Journal of Environmental Management, Vol. 73, No. 3, 2004, pp. 165-181. doi:10.1016/j.jenvman.2004.06.004
[9] S. Birk, W. Bonne, A. Borja, S. Brucet, A. Courrat, S. Poikane, A. Solimini, W. van de Bund, N. Zampoukas and D. Hering, “Three Hundred Ways to Assess Europe’s Surface Waters: An Almost Complete Overview of Biological Methods to Implement the Water Framework Directive,” Ecological Indicators, Vol. 18, No. 1, 2012, pp. 31-41. doi:10.1016/j.ecolind.2011.10.009
[10] G. Van Hoey, A. Borja, S. Birchenough, L. Buhl-Mortensen, S. Degreaer, D. Fleisher, F. Kerckhof, P. Magni, I. Muxika, H. Reiss, A. Schroder and M. Zettler, “The Use of Benthic Indicators in Europe: From the Water Framework Directive to the Marine Strategy Framework Directive,” Marine Pollution Bulletin, Vol. 60, No. 12, 2010, pp. 2187-2196. doi:10.1016/j.marpolbul.2010.09.015
[11] D. A. Smale, T. J. Langlois, G. A. Kendrick, J. J. Meeuwig and E. S. Harvey, “From Fronds to Fish: The Use of Indicators for Ecological Monitoring in Marine Benthic Ecosystems, with Case Studies from Temperate Western Australia,” Reviews in Fish Biology and Fisheries, Vol. 21, No. 3, 2011, pp. 311-337. doi:10.1007/s11160-010-9173-7
[12] J.-C. Dauvin, S. Alizier, C. Rolet, A. Bakalem, G. Bellan, J. L. Gomez Gesteira, S. Grimes, J. A. de-la-Ossa-Carretero and Y. Del-Pilar-Ruso, “Response of Different Benthic Indices to Diverse Human Pressures,” Ecological Indicators, Vol. 12, No. 1, 2012, pp. 143-153. doi:10.1016/j.ecolind.2011.03.019
[13] J.-C. Dauvin, G. Bellan and D. Bellan-Santini, “Benthic Indicators: From Subjectivity to Objectivity—Where Is the Line?” Marine Pollution Bulletin, Vol. 60, No. 7, 2010, pp. 947-953. doi:10.1016/j.marpolbul.2010.03.028
[14] U. Heink and I. Kowarik, “What Are Indicators? On the Definition of Indicators in Ecology and Environmental Planning,” Ecological Indicators, Vol. 10, No. 3, 2010, pp. 584-593. doi:10.1016/j.ecolind.2009.09.009
[15] A. Borja, J. Franco and V. Perez, “A Marine Biotic Index to Establish the Ecological Quality of Soft-Bottom Benthos within European Estuarine and Coastal Environments,” Marine Pollution Bulletin, Vol. 40, No. 12, 2000, 1100-1114. doi:10.1016/S0025-326X(00)00061-8
[16] R. M. Warwick, “The Level of Taxonomic Discrimination Required to Detect Pollution Effects on Marine Benthic Communities,” Marine Pollution Bulletin, Vol. 19, No. 6, 1988, pp. 259-268. doi:10.1016/0025-326X(88)90596-6
[17] A. Borja and D. M. Dauer, “Assessing the Environmental Quality Status in Estuarine and Coastal Systems: Comparing Methodologies and Indices,” Ecological Indicators, Vol. 8, No. 4, 2008, pp. 331-337. doi:10.1016/j.ecolind.2007.05.004
[18] I. Muxika, A. Borja and W. Bonne, “The Suitability of the Marine Biotic Index (AMBI) to New Impact Sources Along European Coasts,” Ecological Indicators, Vol. 5, No. 1, 2005, pp. 19-31. doi:10.1016/j.ecolind.2004.08.004
[19] F. Salas, J. M. Neto, A. Borja and J. C. Marques, “Evaluation of the Applicability of a Marine Biotic Index to Characterize the Status of Estuarine Ecosystems: The Case of Mondego Estuary (Portugal),” Ecological Indicators, Vol. 4, No. 3, 2004, pp. 215-225. doi:10.1016/j.ecolind.2004.04.003
[20] R. Pinto, J. Patricio, A. Baeta, B. D. Fath, J. M. Neto and J. C. Marques, “Review and Evaluation of Estuarine Biotic Indices to Assess Benthic Condition,” Ecological Indicators, Vol. 9, No. 1, 2009, pp. 1-25. doi:10.1016/j.ecolind.2008.01.005
[21] M. Mabe and M. Amin, “Growth Dynamics of Scholarly and Scientific Journals,” Scientometrics, Vol. 51, No. 1, 2001, pp. 147-162. doi:10.1023/A:1010520913124
[22] P. O. Larsen and M. von Is, “The Rate of Growth in Scientific Publication and the Decline in Coverage Provided by Science Citation Index,” Scientometrics, Vol. 84, No. 3, 2010, pp. 575-603. doi:10.1007/s11192-010-0202-z
[23] M. W. Neff and E. A. Corley, “35 Years and 160,000 Articles: A Bibliometric Exploration of the Evolution of Ecology,” Scientometrics, Vol. 80, No. 3, 2009, pp. 657-682. doi:10.1007/s11192-008-2099-3
[24] J.-P. Gattuso, N. A. Dawson, C. M. Duarte and J. J. Middelburg, “Patterns of Publication Effort in Coastal Biogeochemistry: A Bibliometric Survey (1971 to 2003),” Marine Ecology Progress Series, Vol. 294, 2005, pp. 9-22. doi:10.3354/meps294009
[25] J. Sun, M. H. Wang and Y.-S. Ho, “A Historical Review and Bibliometric Analysis of Research on Estuary Pollution,” Marine Pollution Bulletin, Vol. 64, No. 1, 2012, pp. 13-21. doi:10.1016/j.marpolbul.2011.10.034
[26] H. Yi and W. Jie, “A Bibliometric Study of the Trend in Articles Related to Eutrophication Published in Science Citation Index,” Scientometrics, Vol. 89, No. 3, 2011, pp. 919-927. doi:10.1007/s11192-011-0479-6
[27] F. Ibanez, J.-M. Fromentin and J. Castel, “Application of the Cumulated Function to the Processing of Chronological Data in Oceanography,” Comptes Rendus de l’Académie des Sciences Série III—Sciences de la Vie—Life Sciences, Vol. 316, 1993, pp. 745-748.
[28] I. Karakassis, P. D. Dimitriou, N. Papageorgiou, E. T. Apostolaki, N. Lampadariou and K. D. Black, “Methodological Considerations on the Coastal and Transitional Benthic Indicators Proposed for the Water Framework Directive,” Ecological Indicators, Vol. 29, 2013, pp. 26-33. doi:10.1016/j.ecolind.2012.12.020
[29] T. Bacci, B. Trabucco, S. Marzialetti, V. Marusso, S. Lomiri, D. Vani and C. V. Lamberti, “Taxonomic Sufficiency in Two Case Studies: Where Does It Work Better?” Marine Ecology, Vol. 30, No. Suppl. 1, 2009, pp. 13-19. doi:10.1111/j.1439-0485.2009.00324.x
[30] J. A. de-la-Ossa-Carretero, N. Simboura, Y. Del-PilarRuso, M. A. Pancucci-Papadopoulou, F. Giménez-Casualduero and J. L. Sánchez-Lizaso, “A Methodology for Applying Taxonomic Sufficiency and Benthic Indices in Two Mediterranean Areas,” Ecological Indicators, Vol. 23, 2012, pp. 232-241. doi:10.1016/j.ecolind.2012.03.029
[31] H. Teixeira, A. Borja, S. B. Weisberg, J. A. Ranasinghe, D. B. Cadien, D. M. Dauer, J.-C. Dauvin, S. Degraer, R. J. Diaz, A. Grémare, I. Karakassis, R. J. Llansó, L. L. Lovell, J. C. Marques, D. E. Montagne, A. Occhipinti-Ambrogi, R. Rosenberg, R. Sardá, L. C. Schaffner and R. G. Velarde, “Assessing Coastal Benthic Macrofauna Community Condition Using Best Professional Judgement— De-veloping Consensus Across North America and Europe,” Marine Pollution Bulletin, Vol. 60, No. 4, 2010, pp. 589-600. doi:10.1016/j.marpolbul.2009.11.005
[32] A. Afli, R. Ayari and S. Zaabi, “Ecological Quality of Some Tunisian Coast and Lagoon Locations, by Using Benthic Community Parameters and Biotic Indices,” Estuarine, Coastal and Shelf Science, Vol. 80, No. 2, 2008, pp. 269-280. doi:10.1016/j.ecss.2008.08.010
[33] H. Blanchet, N. Lavesque, T. Ruellet, J.-C. Dauvin, P.-G. Sauriau, N. Desroy, C. Desclaux, M. Leconte, G. Bachelet, A.-L. Janson, C. Bessineton, S. Duhamel, J. Jourde, S. Mayot, S. Simon and X. de Montaudouin, “Use of Biotic Indices in Semi-Enclosed Coastal Ecosystems and Transitional Waters Habitats—Implications for the Implementation of the European Water Framework Directive,” Ecological Indicators, Vol. 8, No. 4, 2008, pp. 360-372. doi:10.1016/j.ecolind.2007.04.003
[34] A. Borja, D. M. Dauer, R. Díaz, R. J. Llansó, I. Muxika, J. G. Rodríguez and L. Schaffner, “Assessing Estuarine Benthic Quality Conditions in Chesapeake Bay: A Comparison of Three Indices,” Ecological Indicators, Vol. 8, No. 4, 2008, pp. 395-403. doi:10.1016/j.ecolind.2007.05.003
[35] A. Borja, J. G. Rodríguez, K. Black, A. Bodoy, C. Emblow, T. F. Fernandes, J. Forte, I. Karakassis, I. Muxika, T. D. Nickell, N. Papageorgiou, F. Pravoni, K. Sevastou, P. Tomassetti and D. Angel, “Assessing the Suitability of a Range of Benthic Indices in the Evaluation of Environmental Impact of Fin and Shellfish Aquaculture Located in Sites Across Europe,” Aquaculture, Vol. 293, No. 3-4, 2009, pp. 231-240. doi:10.1016/j.aquaculture.2009.04.037
[36] N. Lavesque, H. Blanchet and X. de Montaudouin, “Development of a Multimetric Approach to Assess Perturbation of Benthic Macrofauna in Zostera noltii Beds,” Journal of Experimental Marine Biology and Ecology, Vol. 368, No. 2, 2009, pp. 101-112. doi:10.1016/j.jembe.2008.09.017
[37] R. Simonini, V. Grandi, G. Massamba-N’Siala, M. Lotti, G. Montarani and D. Prevedelli, “Assessing the Ecological Status of North-Western Adriatic Sea within the European Framework Directive: A Comparison of Bentix, AMBI and M-AMBI Methods,” Marine Ecology, Vol. 30, No. 2, 2009, pp. 241-254. doi:10.1111/j.1439-0485.2009.00281.x
[38] S. J. Ware, H. L. Rees, S. E. Boyd and S. N. Birchenhough, “Performance of Selected Indicators in Evaluating the Consequences of Dredged Material Relocation and Marine Aggregate Extraction,” Ecological Indicators, Vol. 9, No. 4, 2009, pp. 704-718. doi:10.1016/j.ecolind.2008.09.010
[39] S. Grimes, T. Ruellet, J.-C. Dauvin and Z. Boutida, “Ecological Quality Status of the Soft-Bottom Communities on the Algerian Coast: General Patterns and Diagnosis,” Marine Pollution Bulletin, Vol. 60, No. 11, 2010, pp. 1969-1977. doi:10.1016/j.marpolbul.2010.07.032
[40] A. Borja, E. Barbone, A. Basset, G. Borgensen, M. Brkljacic, M. Elliott, J. M. Garmendia, J. C. Marques, K. Mazik, I. Muxika, J. M. Neto, K. Norling, J. G. Rodríguez, I. Rosati, B. Rygg, H. Teixeira and A. Trayanova, “Response of Single Benthic Metrics and MultiMetric Methods to Anthropogenic Pressure Gradients, in Five Distinct European Coastal and Transitional Ecosystems,” Marine Pollution Bulletin, Vol. 62, No. 3, 2011, pp. 499-513. doi:10.1016/j.marpolbul.2010.12.009
[41] C. Murani and M. Mistri, “Ecological Status Assessment and Response of Benthic Communities to Environmental Variability: The Valli di Comacchio (Italy) as a Case Study,” Marine Environmental Research, Vol. 81, 2012, pp. 53-61. doi:10.1016/j.marenvres.2012.08.008
[42] F. Salas, C. Marcos, J. M. Neto, J. Patrício, A. PérezRuzafa and J. C. Marques, “User-Friendly Guide for Using Benthic Ecological Indicators in Coastal and Marine Quality assessment,” Ocean and Coastal Management, Vol. 49, No. 5-6, 2006, pp. 308-331. doi:10.1016/j.ocecoaman.2006.03.001
[43] H. Reiss and I. Kroncke, “Seasonal Variability of Benthic Indices: An Approach to Test the Applicability of Different Indices for Ecosystem Quality Assessment,” Marine Pollution Bulletin, Vol. 50, No. 12, 2005, pp. 1490-1499. doi:10.1016/j.marpolbul.2005.06.017
[44] J.-C. Dauvin, G. Bachelet, A.-L. Barillé, H. Blanchet, X. de Montaudouin, N. Lavesque and T. Ruellet, “Benthic Indicators and Index Approaches in the Three Main Estuaries along the French Atlantic Coast (Seine, Loire and Gironde),” Marine Ecology, Vol. 30, No. 2, 2009, pp. 228-240. doi:10.1111/j.1439-0485.2008.00274.x
[45] I. Kroncke and H. Reiss, “Influence of Macro-Fauna Long-Term Natural Variability on Benthic Indices Used in Ecological Quality Assessment,” Marine Pollution Bulletin, Vol. 60, No. 1, 2010, pp. 58-68. doi:10.1016/j.marpolbul.2009.09.001
[46] J. E. Fitch and T. P. Crowe, “Effective Methods for Assessing Ecological Quality in Intertidal Soft-Sediment Habitats,” Marine Pollution Bulletin, Vol. 60, No. 10, 2010, pp. 1726-1733. doi:10.1016/j.marpolbul.2010.06.027
[47] E. Quiroga, P. Ortiz, B. Reid and D. Gerdes, “Classification of the Ecological Quality of the Aysen and Bker Fjords (Patagonia, Chile) Using Biotic Indices,” Marine Pollution Bulletin, Vol. 68, No. 1-2, 2013, pp. 117-126. doi:10.1016/j.marpolbul.2012.11.041
[48] J. A. de-la-Ossa-Carretero, Y. del-Pilar-Ruso, F. Giménez-Casalduero and J. L. Sánchez-Lizaso, “Testing BOPA Index in Seawage Affected Soft-Bottom Communities in the North-Western Mediterranean,” Marine Pollution Bulletin, Vol. 58, No. 3, 2009, 332-340. doi:10.1016/j.marpolbul.2008.10.017
[49] R. Bermejo, J. J. Vergaga and I. Hernández, “Application and Reassessment of the Reduces Species List Index for Macroalgae to Assess the Ecological Status under the Water Framework Directive in the Atlantic Coast of Southern Spain,” Ecological Indicators, Vol. 12, No. 1, 2012, pp. 46-57. doi:10.1016/j.ecolind.2011.04.008
[50] J.-C. Dauvin and T. Ruellet, “Polychaete/Amphipod Ratio Revisited,” Marine Pollution Bulletin, Vol. 55, No. 1-6, 2007, pp. 215-224.
[51] J.-C. Dauvin and T. Ruellet, “The Estuarine Quality Paradox: Is It Possible to Define an Ecological Quality Status for Specific Modified and Naturally Stressed Estuarine Ecosystems?” Marine Pollution Bulletin, Vol. 59, No. 1-3, 2009, pp. 38-47. doi:10.1016/j.marpolbul.2008.11.008
[52] R. Gaspar, L. Pereira and J. M. Neto, “Ecological Reference Conditions and Quality States of Marine Macroalgae sensu Water Framework Directive: An Example from the Intertidal Rocky Shores of the Portuguese Coastal Waters,” Ecological Indicators, Vol. 19, 2012, pp. 24-38. doi:10.1016/j.ecolind.2011.08.022
[53] J. M. Neto, R. Gaspar, L. Pereira and J. C. Marques, “Marine Macroalgae Assessment Tool (MarMAT) for Intertidal Rocky Shores. Quality Assessment under the Scope of the European Water Framework Directive,” Ecological Indicators, Vol. 19, 2012, pp. 39-47. doi:10.1016/j.ecolind.2011.09.006
[54] I. Díez, M. Bustamante, A. Santolaria, J. Tajadura, N. Muguerza, A. Borja, I. Muxika, J. I. Saiz-Salinas and J. M. Gorostiaga, “Development of a Tool for Assessing the Ecological Quality Status of Intertidal Coastal Rocky Assemblages, within Atlantic Iberian Coasts,” Ecological Indicators, Vol. 12, No. 1, 2011, 58-71. doi:10.1016/j.ecolind.2011.05.014
[55] A. S. Alves, H. Adao, T. J. Ferrero, J. C. Marques, M. J. Costa and J. Patrício, “Benthic Meiofauna as Indicator of Ecological Changes in Estuarine Ecosystems: The Use of Nematodes in Ecological Quality Assessment,” Ecological Indicators, Vol. 24, 2013, pp. 462-475. doi:10.1016/j.ecolind.2012.07.013
[56] V. M. P. Bouchet, E. Alve, B. Rygg and R. J. Telford, “Benthic Foraminifera Provide a Promising Tool for Ecological Quality Assessment of Marine Waters,” Ecological Indicators, Vol. 23, 2012, pp. 66-75. doi:10.1016/j.ecolind.2012.03.011
[57] S. Donnici, R. Serandrei-Barbero, M. Bonardi and M. Sperle, “Benthic Foraminifera as Proxies of Pollution: The Case of Guanabara Bay (Brazil),” Marine Pollution Bulletin, Vol. 64, No. 10, 2012, 2015-2028. doi:10.1016/j.marpolbul.2012.06.024
[58] M. Balsamo, F. Semprucci, F. Frontalini and R. Coccioni, “Meiofauna as a Tool for Marine Ecosystem Biomonitoring,” In: A. Cruzado, Ed., Marine Ecosystems, InTech, Rijeka, 2012, pp. 77-104. doi:10.5772/34423
[59] M. Elliott, “Marine Science and Management Means Tackling Exogenic Unmanaged Pressures and Endogenic Managed Pressures—A Numbered Guide,” Marine Pollution Bulletin, Vol. 62, No. 4, 2011, pp. 651-655. doi:10.1016/j.marpolbul.2010.11.033
[60] B. Beliaeff and D. Pelletier, “A General Framework for Indicator Design and Use with Application to the Assessment of Coastal Water Quality and Marine Protected Area Management,” Ocean and Coastal Management, Vol. 54, No. 1, 2011, pp. 84-92. doi:10.1016/j.ocecoaman.2010.10.037
[61] E. Goberville, G. Beaugrand, B. Sautour and P. Tréguer, “Evaluation of Coastal Perturbations: A New Mathematical Procedure to Detect Changes in the Reference State of Coastal Systems,” Ecological Indicators, Vol. 11, No. 5, 2011, pp. 1290-1300. doi:10.1016/j.ecolind.2011.02.002
[62] C. Luczak and N. Spilmont, “Are the Eastern and Western Basins of the English Channel Two Separate Ecosystems? Get Back in Line with Some Cautionary Comments,” Marine Pollution Bulletin, Vol. 64, No. 7, 2012, pp. 1318-1319. doi:10.1016/j.marpolbul.2012.05.006
[63] J.-C. Dauvin, “Response by Dauvin to correspondence by Christophe Luczak and Nicolas Spilmont on ‘Are the Eastern and Western Basins of the English Channel Two Separate Ecosystems? Get back in Line with Some Cautionary comments’,” Marine Pollution Bulletin, Vol. 64, No. 11, 2012, 2615-2616. doi:10.1016/j.marpolbul.2012.07.004
[64] G. Allison, “The Influence of Species Diversity and Stress Intensity on Community Resistance and Resilience,” Ecological Monographs, Vol. 74, 2004, pp. 117-134. doi:10.1890/02-0681
[65] J. Hellou, “Behavioural Ecotoxicology, an ‘Early Warning’ Signal to Assess Environmental Quality,” Environmental Science and Pollution Research, Vol. 18, No. 1, 2011, pp. 1-11. doi:10.1007/s11356-010-0367-2
[66] B. Helmuth, C. D. G. Harley, P. M. Halpin, M. O’Donnell, G. E. Hofmann and C. A. Blanchette, “Climate Change and Latitudinal Patterns of Intertidal Thermal Stress,” Science, Vol. 298, No. 5595, 2002, pp. 1015-1017. doi:10.1126/science.1076814
[67] C. D. G. Harley, “Climate Change, Keystone Predation, and Biodiversity Loss,” Science, Vol. 334, No. 6059, 2011, pp. 1124-1127. doi:10.1126/science.1210199
[68] D. Madeira, L. Narciso, H. N. Cabral and C. Vinagre, “Thermal Tolerance and Potential Impacts of Climate Change on Coastal and Estuarine Organisms,” Journal of Sea Research, Vol. 70, 2012, pp. 32-41. doi:10.1016/j.seares.2012.03.002
[69] D. Raffaelli and S. Hawkins, “Intertidal Ecology,” Chapman & Hall, London, 1996. doi:10.1007/978-94-009-1489-6
[70] W. Klaassen and N. Spilmont, “Inter-Annual Variability of CO2 Exchanges between an Emersed Tidal Flat and the Atmosphere,” Estuarine, Coastal and Shelf Science, Vol. 100, 2012, pp. 18-25. doi:10.1016/j.ecss.2011.06.002
[71] H. Thomas, Y. Bozec, K. Elkalay and H. J. M. de Baar, “Enhanced Open Ocean Storage of CO2 from Shelf Sea Pumping,” Science, Vol. 304, No. 5673, 2004, pp. 1005-1008. doi:10.1126/science.1095491
[72] F. E. Muller-Karger, R. Varela, R. Thunell, R. Luerssen and J. J. Walsh, “The Importance of Continental Margins in the Global Carbon Cycle,” Geophysical Research Letters, Vol. 32, No. 1, 2005, Article ID: L01602. doi:10.1029/2004GL021346
[73] J. H. Connell, “The Influence of Intra-Specific Competition and Other Factors on the Distribution of the Barnacle Chthamalus stellatus,” Ecology, Vol. 42, No. 4, 1961, 710-723. doi:10.2307/1933500
[74] R. T. Paine, “The Pisaster-Tegula Interaction: Prey Patches, Predator Food Preferences and Intertidal Community Structure,” Ecology, Vol. 50, No. 6, 1969, pp. 950-961. doi:10.2307/1936888
[75] A. J. Underwood, “Comparative Studies on the Biology of Nerita atramentosa Reeve, Benbicium nancum (Lamarck) and Cellana tramoserica (Sowerby) (Gastropoda: Prosobranchia) in S.E. Australia,” Journal of Experimental Marine Biology and Ecology, Vol. 18, No. 2, 1975, pp. 153-172. doi:10.1016/0022-0981(75)90071-4
[76] F. Colijn, “Light Absorption in the Waters of the EmsDollard Estuary and its Consequences for the Growth of Phytoplankton and Microphytobenthos,” Netherlands Journal of Sea Research, Vol. 15, No. 2, 1982, 196-216. doi:10.1016/0077-7579(82)90004-7
[77] G. C. Jensen, P. S. McDonald and D. A. Armstrong, “East Meets West: Competitive Interactions between Green Crab Carcinus maenas, and Native and Introduced Shore Crab Hemigrapsus spp,” Marine Ecology Progress Series, Vol. 225, 2002, pp. 251-262. doi:10.3354/meps225251
[78] W. L. Whitlow, “Changes in Survivorship, Behavior, and Morphology in Native Soft-Shell clams Induced by Invasive Green Crab Predators,” Marine Ecology, Vol. 31, No. 3, 2010, pp. 418-430.
[79] A. C. Jackson and J. McIlvenny, “Coastal Squeeze on Rocky Shores in Northern Scotland and Some Possible Ecological Impacts,” Journal of Experimental Marine Biology and Ecology, Vol. 400, No. 1-2, 2011, pp. 314-321. doi:10.1016/j.jembe.2011.02.012
[80] A. B. Aloy, B. M. Vallelo, Jr and M. A. Juinio-Menez, “Increased Plastic Litter Cover Affects the Foraging Activity of the Sandy Intertidal Gastropod Nassarius pullus,” Marine Pollution Bulletin, Vol. 62, No. 8, 2011, pp. 1772-1779. doi:10.1016/j.marpolbul.2011.05.021
[81] C. V. M. Araújo, J. Blasco and I. Moreno-Garrido, “Measuring the Avoidance Behaviour Shown by the Snail Hydrobia ulvae Exposed to Sediment with a Known Contamination Gradient,” Ecotoxicology, Vol. 21, No. 3, 2012, pp. 750-758. doi:10.1007/s10646-011-0835-6
[82] J. D. Nuez, M. V. Laitano and M. Cledón, “An Intertidal Limpet Species as a Bioindicator: Pollution Effects Reflected by Shell Characteristics,” Ecological Indicators, Vol. 14, No. 1, 2012, pp. 178-183. doi:10.1016/j.ecolind.2011.07.015
[83] B. Manachini, V. Arizza, A. Rinaldi, V. Montalto and G. Sarà, “Eco-Physiological Response of Two Marine Bivalves to Acute Exposition to Commercial Bt-Based Pesticide,” Marine Environmental Research, Vol. 83, 2013, pp. 29-37. doi:10.1016/j.marenvres.2012.10.006
[84] S. Melatunan, P. Calosi, S. D. Rundle, A. J. Moody and S. Widdicombe, “Exposure to Elevated Temperature and PCO2 Reduces Respiration Rate and Energy Status in the Periwinkle Littorina littorea,” Physiological and Biochemical Zoology, Vol. 84, No. 6, 2011, pp. 583-594. doi:10.1086/662680
[85] K. L. de la Haye, J. I. Spicer, S. Widdicombe and M. Briffa, “Reduced pH Sea Water Disrupt Chemo-Responsive Behaviour in an Intertidal Crustacean,” Journal of Experimental Marine Biology and Ecology, Vol. 412, 2012, pp. 134-140. doi:10.1016/j.jembe.2011.11.013
[86] C. Chapperon and L. Seuront “Behavioral Thermoregulation in a Tropical Gastropod: Links to Climate Change Scenarios,” Global Change Biology, Vol. 17, No. 4, 2011, pp. 1740-1749. doi:10.1111/j.1365-2486.2010.02356.x
[87] S. R. Cartwright and C. A. Williams, “Seasonal Variation in Utilization of Biogenic Microhabitats by Littorinid Snails on Tropical Rocky Shores,” Marine Biology, Vol. 159, No. 10, 2012, pp. 2323-2332. doi:10.1007/s00227-012-2017-3
[88] E. K. Fly, C. J. Monaco, S. Pincebourde and A. Tullis, “The Influence of Intertidal Location and Temperature on the Metabolic Coast of Emersion in Pisaster ochraceus,” Journal of Experimental Marine Biology and Ecology, Vol. 422-423, 2012, pp. 20-28. doi:10.1016/j.jembe.2012.04.007
[89] S. G. Cheung, H. Y. Wai and P. K. S. Shin, “Fatty Acid Profiles of Benthic Environment Associated with Artificial Reefs in Subtropical Hong Kong,” Marine Pollution Bulletin, Vol. 60, No. 2, 2010, 303-308. doi:10.1016/j.marpolbul.2009.12.001
[90] K. Grangeré, S. Lefebvre and J. L. Blin, “Spatial and Temporal Dynamics of Biotic and Abiotic Features of Temperate Coastal Ecosystems as Revealed by a Combination of Ecological Indicators,” Estuarine, Coastal and Shelf Science, Vol. 108, 2012, pp. 109-118. doi:10.1016/j.ecss.2012.02.020
[91] N. G. Barr, B. D. Dudley, K. M. Rogers and C. D. Cornelisen, “Broad-Scale Patterns of Tissue-δ15N and Tissue-N Indices in Frondose Ulva spp.; Developing a National Baseline Indicator of Nitrogen-Loading for Coastal New Zealand,” Marine Pollution Bulletin, Vol. 67, No. 1-3, 2013, pp. 203-216. doi:10.1016/j.marpolbul.2012.11.033
[92] N. Spilmont, A. Migné, L. Seuront and D. Davoult, “Short-Term Variability of Intertidal Benthic Community Production during Emersion and the Implication in Annual Budget Calculation,” Marine Ecology Progress Series, Vol. 333, 2007, pp. 95-101. doi:10.3354/meps333095
[93] A. Migné, N. Spilmont, G. Boucher, L. Denis, C. Hubas, M.-A. Janquin, M. Rauch and D. Davoult, “Annual Budget of Benthic Production in Mont Saint-Michel Bay Considering Cloudiness, Microphytobenthos Migration, and Variability of Respiration Rates With Tidal Conditions,” Continental Shelf Research, Vol. 29, No. 19, 2009, pp. 2280-2285. doi:10.1016/j.csr.2009.09.004
[94] N. Spilmont, A. Migné, A. Lefebvre, L. F. Artigas, M. Rauch and D. Davoult, “Temporal Variability of Intertidal Benthic Metabolism under Emersed Conditions in an exposed Sandy Beach (Wimereux, Eastern English Channel, France),” Journal of Sea Research, Vol. 53, No. 3, 2005, pp. 161-167. doi:10.1016/j.seares.2004.07.004
[95] C. Hubas and D. Davoult, “Does Seasonal Proliferation of Enteromorpha sp. Affect the Annual Benthic Metabolism of a Small Macrotidal Estuary? (Roscoff Aber Bay, France),” Estuarine, Coastal and Shelf Science, Vol. 70, No. 1-2, 2006, pp. 287-296. doi:10.1016/j.ecss.2006.06.019
[96] N. Spilmont, L. Denis, L. F. Artigas, F. Caloin, L. Courcot, A. Créach, N. Desroy, F. Gevaert, P. Hacquebart, C. Hubas, M.-A. Janquin, Y. Lemoine, C. Luczak, A. Migné, M. Rauch and D. Davoult, “Impact of the Phaeocystis globosa Spring Bloom on the Intertidal Benthic Compartment in the Eastern English Channel: A Synthesis,” Marine Pollution Bulletin, Vol. 58, No. 1, 2009, pp. 55-63. doi:10.1016/j.marpolbul.2008.09.007
[97] A. Migné, V. Ouisse, C. Hubas and D. Davoult, “Freshwater Seepages and Ephemeral Macroalgae Proliferation in an Intertidal Bay: II. Effect on Benthic Biomass and Metabolism,” Estuarine, Coastal and Shelf Science, Vol. 92, No. 1, 2012, pp. 161-168. doi:10.1016/j.ecss.2010.12.023
[98] N. Valvidia, C. Golléty, A. Migné, D. Davoult and M. Molis, “Stressed but Stable: Canopy Loss Decreased Species Synchrony and Metabolic Variability in an Intertidal Hard-Bottom Community,” PloS One, Vol. 7, No. 5, 2012, Article ID: e36541. doi:10.1371/journal.pone.0036541
[99] C. Golléty, D. Davoult and F. Gentil, “Secondary Production, Calcification and CO2 Fluxes in the Cirripedes Chtalamus montagui and Elminius modestus,” Oecologia, Vol. 155, No. 1, 2008, pp. 133-142. doi:10.1007/s00442-007-0895-8
[100] R. C. Thompson, T. P. Crowe and S. J. Hawkins, “Rocky Intertidal Communities: Past Environmental Changes, Present Status and Predictions for the Next 25 Years,” Environmental Conservation, Vol. 29, No. 2, 2002, pp. 168-191. doi:10.1017/S0376892902000115
[101] J. E. Fitch and T. P. Crowe, “Combined Effects of Temperature, Inorganic Nutrients and Organic Matter on Ecosystem Processes in Intertidal Sediments,” Journal of Experimental Marine Biology and Ecology, Vol. 400, No. 1-2, 2011, pp. 257-263. doi:10.1016/j.jembe.2011.02.005
[102] S. Pincebourde, E. Sanford, J. Casas and B. Helmuth, “Temporal Coincidence of Environmental Stress Events Modulates Predation Rates,” Ecology Letters, Vol. 15, No. 7, 2012, pp. 680-688. doi:10.1111/j.1461-0248.2012.01785.x
[103] T. Meziane, L. Bodineau, C. Retiere, and G. Thoumelin, “The Use of Lipid Markers to Define Sources of Organic Matter in Sediment and Food Web of the Intertidal Salt-Marsh-Flat Ecosystem of the Mont-Saint-Michel Bay, France,” Journal of Sea Research, Vol. 38, No. 1-2, 1997, pp. 47-58. doi:10.1016/S1385-1101(97)00035-X
[104] J. R. Kelly and R. E. Scheibling, “Fatty Acids as Dietary Tracers in Benthic Food Webs,” Marine Ecology Progress Series, Vol. 446, 2012, pp. 1-22. doi:10.3354/meps09559
[105] D. D. Baldocchi, “Assessing the Eddy Covariance Technique for Evaluating Carbon Dioxide Exchange Rates in Ecosystems: Past, Present and Future,” Global Change Biology, Vol. 9, No. 4, 2003, pp. 479-492. doi:10.1046/j.1365-2486.2003.00629.x
[106] P. Polsenaere, E. Lamaud, V. Lafon, J.-M. Bonnefond, P. Bretel, B. Delille, J. Deborde, D. Loustau and G. Abril, “Spatial and Temporal CO2 Exchanges Measured by Eddy Correlation over a Temperate Intertidal Flat and Their Relationships to Net Ecosystem Production,” Biogeosciences, Vol. 9, 2012, pp. 249-268. doi:10.5194/bg-9-249-2012
[107] J. P. Cohn, “Citizen Science: Can Volunteers do Real Research?” BioScience, Vol. 58, No. 3, 2008, pp. 192-197. doi:10.1641/B580303
[108] J. Silvertown, “A New Dawn for Citizen Science,” Trends in Ecology and Evolution, Vol. 24, No. 9, 2009, pp. 467-471. doi:10.1016/j.tree.2009.03.017
[109] D. G. Delaney, C. D. Sperling, C. S. Adams and B. Leung, “Marine Invasive Species: Validation of Citizen Science and Implications for National Monitoring Networks,” Biological Invasions, Vol. 10, No. 1, 2008, pp. 117-128. doi:10.1007/s10530-007-9114-0

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