Abstract
Intertidal organisms are often assumed to live close to their thermal limits, and have emerged as potential early indicators of the effects of climate change. We compared our survey of the 2004–2006 geographic distribution of the barnacle Semibalanus balanoides to its distribution in 1872, 1955, 1963, 1971, and 1985, from surveys by Fischer, Crisp, Fischer-Piette, Barnes, Powell, and Southward. The southern geographic limit has retreated 300 km in France since 1872, at a rate of 15 to 50 km per decade. We compared our 2006 survey of the geographic distribution of the polychaete Diopatra neapolitana to its distribution in 1893–1923, from surveys by Saint-Joseph and Fauvel, and its distribution in 1969–1976 from surveys by Glémarec. The northern geographic limit of this species has advanced 300 km in France since 1893 at similar rates to Semibalanus. We used NOAA weather reanalysis data and our mechanistic simulation model of intertidal animal body temperatures to hindcast the thermal environmental change near historical geographic limits in Europe for the past 55 years. Results indicate that changes in the southern limit of S. balanoides are due to intolerance of winter body temperatures above 10°C, leading to reproductive failure. Results for Diopatra are ambiguous: based on the northern extension of its range, either cold winters or cool summers limit its range, while gaps in its distribution are consistent with limitation by cooler summer conditions. The parallel shifts of D. neapolitana on sedimentary shores and Semibalanus on rocky shores suggest that similar climatic factors control the geographic limits of both species. The intertidal zone is a model system for examining the effects of climate change on biogeographic change both because of the rapidity of its response, and because the rich historical record allows direct tests of hypotheses.
Similar content being viewed by others
References
Alvarez, I., M. de Castro, M. Gomes-Gesteira & R. Prego, 2005. Inter- and intra-annual analysis of the salinity and temperature evolution in the Galician Rías Baixas-ocean boundary (northwest Spain). Journal of Geophysical Research 110: C04008.
Anadón, R. & E. Anadón, 1973. Primera cita para España del phylum Phoronida. Boletín de la Real Sociedad Española de Historia Natural (Biología) 71: 193–200.
Barnes, H., 1958. Regarding the southern limits of Balanus balanoides (L). Oikos 9: 139–157.
Barnes, H., 1963. Light, temperature and the breeding of Balanus balanoides. Journal of the Marine Biological Association of the United Kingdom 43: 717–727.
Barnes, H. & M. Barnes, 1966. Ecological and zoogeographical observations on some of the common intertidal cirripedes of the coasts of the western European mainland in June-September, 1963. In Barnes, H. (ed.), Some Contemporary Studies in Marine Science. Allen & Unwin, London: 83–105.
Barnes, H. & M. Barnes, 1976. The rate of development of the embryos of Balanus balanoides (L.) from a number of European and American populations and the designation of local races. Journal of Experimental Marine Biology and Ecology 24: 251–269.
Barnes, H. & H. T. Powell, 1966. Notes on the occurrence of Balanus balanoides, Elminius modestus, Fucus serratus, and Littorea littoralis at Arcachon, France, in 1963 and 1964. In Barnes, H. (ed.), Some Contemporary Studies in Marine Science. Allen & Unwin, London: 107–111.
Barnes, H. & R. L. Stone, 1972. Suppression of penis development in Balanus balanoides (L.). Journal of Experimental Marine Biology and Ecology 9: 303–309.
Barnes, H., M. Barnes & W. Klepal, 1972. Some cirripedes of the French Atlantic coast. Journal of Experimental Marine Biology and Ecology 8: 187–194.
Beaugrand, G., P. C. Reid, F. Ibañez & M. Edwards, 2002. Reorganization of North Atlantic marine copepod biodiversity and climate. Science 296: 1692–1694.
Boaventura, D., P. Ré, L. C. da Fonseca & S. J. Hawkins, 2002. Intertidal rocky shore communities of the continental Portuguese coast: analysis of distribution patterns. Marine Ecology 23: 69–90.
Cabioch, L., F. Gentil, R. Glaçon & C. Retière, 1977. Le macrobenthos des fonds meubles de la Manche: distribution générale et écologie. In Keegan, B. F., P. O’Ceidigh & P. J. S. Boaden (eds), Biology of Benthic Organisms. Pergamon, Oxford: 115–128.
Crisp, D. J. & E. Fischer-Piette, 1959. Repartition des principales espèces intercotidales de la côte atlantique française en 1954–1955. Annales de l’Institut Océanographique de Monaco 36: 275–287.
Crisp, D. J. & B. S. Patel, 1969. Environmental control of the breeding of three boreo-arctic cirripedes. Marine Biology 2: 283–295.
Crisp, D. J. & A. J. Southward, 1958. The distribution of intertidal organisms along the coasts of the English Channel. Journal of the Marine Biological Association of the United Kingdom 37: 157–208.
Davenport, J., M. S. Berggren, T. Brattegard, N. Brattenborg, M. Burrows, S. Jenkins, D. McGrath, R. MacNamara, J.-A. Sneli, G. Walker & S. Wilson, 2005. Doses of darkness control latitudinal differences in breeding date of the barnacle Semibalanus balanoides. Journal of the Marine Biological Association of the United Kingdom 85: 59–63.
Drévès, L., 2001. Effets climatiques sur les écosystèmes marins. Exemple du recrutement des crustacés cirripèdes sur la côte ouest du Cotentin. Hydroécologie Appliquée 13: 101–112.
Drévès, L., L. Lampert, J. Martin, C. Abernot-le Gac, F. Dagault, J.-D. Gaffet & I. Schlaich, 2005. Surveillance écologique et halieutique du site électronucléaire de Flamanville, Année 2004. Ifremer Report RST.DOP/LER/05.02.
Etter, R. J., 1988. Physiological stress and color polymorphism in the intertidal snail Nucella lapillus. Evolution 42: 660–680.
Evans, R. G., 1954. The intertidal ecology of some localities on the Atlantic coast of France. Journal of Animal Ecology 45: 245–271.
Faure, G., 1969. Bionomie et écologie de la macrofaune des substrats meubles de la cote charentaise. Tethys 1: 751–778.
Fauvel, P. L. A., 1923. Polychètes errantes. Faune de France 5: 488 pp.
Fischer, P., 1872. Crustaces, podophthalmaires et cirrhipèdes du départment de la Gironde et des côtes du Sud-Ouest de la France. Actes de la Société Linnéenne de Bordeaux 28: 405–438.
Fischer-Piette, E., 1932. Repartition des principales espèces fixées sur les rochers battus des côtes et des îles de la Manche, de Lannion à Fécamp. Annales de l’Institut Océanographique de Monaco 12: 105–213.
Fischer-Piette, E., 1955. Repartition, le long des côtes septentrionales de l’Espagne, des principales espèces peuplant les rochers intercotidaux. Annales de l’Institut Océanographique de Monaco 31: 37–124.
Fischer-Piette, E. & M. Prenant, 1956. Distribution des cirripedes intercotidaux d’Espagne septentrionale. Bulletin du Centre d’Etudes et Recherches Scientifiques Biarritz 1: 7–19.
Fischer-Piette, E. & M. Prenant, 1957. Quelques données ecologiques sur les cirripedes intercotidaux du Portugal, de l’Espagne du sud et du nord du Maroc. Bulletin du Centre d’Etudes et Recherches Scientifiques Biarritz 1: 361–368.
Flater, D., 2006. X-Tide. http://www.flaterco.com/xtide.
Foster, B.A., 1969. Tolerance of high temperatures by some intertidal barnacles. Marine Biology 4: 326–332.
Garcia-Soto, C., R. D. Pingree & L. Valdés, 2002. Navidad development in the southern Bay of Biscay: climate change and swoddy structure from remote sensing and in situ measurements. Journal of Geophysical Research 107: C8, 3118, doi:10.1029/2001JC001012.
Gilman, S. E., D. S. Wethey & B. Helmuth, 2006. Variation in the sensitivity of organismal body temperature to climate change over local and geographic scales. Proceedings of the National Academy of Sciences 103: 9560–9565.
Glémarec, M., 1979. Les fluctuations temporelles des peuplements benthiques liées aux fluctuations climatiques. Oceanologica Acta 2: 365–371.
Hansen, J., M. Sato, R. Ruedy, K. Lo, D. W. Lea & M. Medina-Elizade, 2006. Global temperature change. Proceedings of the National Academy of Sciences 103: 14288–14293.
Harrison, S. J. & A. P. Phizacklea, 1987. Vertical temperature gradients in muddy intertidal sediments in the Forth estuary, Scotland. Limnology and Oceanography 32: 954–963.
Helmuth, B. S. T., 1999. Thermal biology of rocky intertidal mussels: quantifying body temperatures using climatological data. Ecology 80: 15–34.
Helmuth, B., N. Mieszkowska, P. Moore & S. J. Hawkins, 2006. Living on the edge of two worlds: forecasting the response of rocky intertidal ecosystems to climate change. Annual Review of Ecology, Evolution, and Systematics 37: 373–404.
Hutchins, L. W., 1947. The bases for temperature zonation in geographical distribution. Ecological Monographs 17: 325–335.
Jansen, J. M., A. E. Pronker, S. W. Bonga & H. Hummel, 2007. Macoma balthica in Spain, a few decades back in climatic history. Journal of Experimental Marine Biology and Ecology 334: 161–169.
Kalnay, E., M. Kanamitsu, R. Kistler, W. Collins, D. Deaven, L. Gandin, M. Iredell, S. Saha, G. White, J. Woollen, Y. Zhu, M. Chelliah, W. Ebisuzaki, W. Higgins, J. Janowiak, K.C. Mo, R. Ropelewski, J. Wang, A. Leetmaa, R. Reynolds, R. Jenne & D. Joseph, 1996. The NCEP/NCAR 40–year reanalysis project. Bulletin of the American Meteorological Society 77: 437–471.
Kendall, M. A., M. T. Burrows, A. J. Southward & S. J. Hawkins, 2004. Predicting the effects of marine climate change on the invertebrate prey of the birds of rocky shores. Ibis 146: 40–47.
Koutsikopoulos, C., P. Beillois, C. Leroy & F. Taillefer, 1998. Temporal trends and spatial structures of the sea surface temperature in the Bay of Biscay. Oceanologica Acta 21: 335–344.
Lafont, A., 1871. Note pour servir a la faune de la Gironde contenant la liste des animaux marins dont la présence a été constatée a Arcachon pendant les annés 1869–1870. Actes de la Societé Linnéene de Bordeaux 28: 237–280.
Lagardère, F., 1971(1972a). Les fonds de pêche de la côte ouest de l’ile d’Oléron. Cartographie bionomique. II. Remarques systématiques, biologiques et écologiques. Tethys 3: 265–281.
Lagardère, F., 1971(1972b). Les fonds de pêche de la côte ouest de l’ile d’Oléron. Cartographie bionomique. III.—Les peuplements benthiques. Tethys 3: 507–538.
Lewis, J. R., 1964. The Ecology of Rocky Shores. English Universities Press. London.
Lima, F., N. Queiroz, P. A. Ribeiro, S. J. Hawkins & A. M. Santos, 2006. Geographic expansion of a marine gastropod, Patella rustica Linnaeus, 1758, and its relation with unusual climatic events. Journal of Biogeography 33: 812–822.
Mangum, C. P. & C. D. Cox, 1971. Analysis of the feeding response in the onuphid polychaete Diopatra cuprea (Bosc). Biological Bulletin 140: 215–229.
Mangum, C. P., S. L. Santos & W. R. Rhodes Jr., 1968. Distribution and feeding in the onuphid polychaete, Diopatra cuprea (Bosc). Marine Biology 2: 33–40.
Margalet, J. L. & M. J. Navarro, 1992. Mapas de distribución de algas marinas de la Península Ibérica. II. Ascophyllum nodosum (L.) Le Jolis, Pelvetia canaliculata (L.) Decne. et Thur. e Himanthalia elongata (L.) S. F. Gray. Botanica Complutensis 17: 117–132.
Margalet, J. L., T. Almaraz, M. J. Navarrro & I. M. Pérez-Ruzafa, 1993. Mapas de distribución de algas marinas de la Península Ibérica. III. Fucus ceranoides L., F. serratus L., F. spiralis L. y F. vesiculosus L. (Fucales, Fucophyceae). Botanica Complutensis 18: 267–290.
Mieszkowska, N., M. A. Kendall, S. J. Hawkins, R. Leaper, P. Williamson, N. J. Hardman-Mountford & 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.
Montaudouin, X. & P.-G. de Sauriau, 2000. Contribution to a synopsis of marine species richness in the Pertuis Charentais Sea with new insights in soft-bottom macrofauna of the Marennes-Oléron Bay. Cahiers de Biologie Marine 41: 181–222.
Moreira, J., P. Quintas & J. Troncoso, 2006. Spatial distribution of soft-bottom polychaete annelids in the Ensenada de Baiona (Ría de Vigo, Galicia, north-west Spain). Scientia Marina 70S3: 217–224.
Myers, A. C., 1972. Tube-worm-sediment relationships of Diopatra cuprea (Polychaeta, Onuphidae). Marine Biology 17: 350–356.
Parmesan, C., N. Ryrholm, C. Stefanescu, J. K. Hill, C. D. Thomas, H. Descimon, B. Huntley, L. Kaila, J. Kullberg, T. Tammaru, W. J. Tennet, J. A. Thomas & M. Warren, 1999. Poleward shifts in geographical ranges of butterfly species associated with regional warming. Nature 399: 579–583.
Parmesan, C. & G. Yohe, 2003. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421: 37–42.
Rayner, N. A., D. E. Parker, E. B. Horton, C. K. Folland, L. V. Alexander, D. P. Powell, E. C. Kent & A. Kaplan, 2003. Global analysis of sea surface temperature, sea ice, and night marine air temperatures since the late nineteenth century. Journal of Geophysical Research 108, D14, 4407.
Saint-Joseph, 1898. Les annelids polychetes des côtes de France (Manche et Océan). Annales des Sciènces Naturelles Zoologie Ser 8(5): 209–464.
Savageau, C., 1897. Note préliminaire sur les Algues marines du golfe de Gascogne. Journal de Botanique 11: 166, 175, 202, 207, 252, 263, 275, 301, 307.
Simkanin, C., A. Power, A. Myers, D. McGrath, A. Southward, N. Mieszkowska, R. Leaper & R. O’Riordan, 2005. Using historical data to detect temporal changes in the abundances of intertidal species on Irish shores. Journal of the Marine Biological Association of the United Kingdom 85: 1329–1340.
Southward, A. J., 1958. Note on the temperature tolerance of some intertidal marine animals in relation to environmental temperatures and geographical distribution. Journal of the Marine Biological Association of the United Kingdom 37: 49–66.
Southward, A. J., 1963. Distribution of some plankton animals in the English Channel and approaches. III. Theories about long term biological changes, including fish. Journal of the Marine Biological Association of the United Kingdom 43: 1–29.
Southward, A. J., 1991. 40 years of changes in species composition and population-density of barnacles on a rocky shore near Plymouth. Journal of the Marine Biological Association of the United Kingdom 71: 495–513.
Southward, A. J. & D. J. Crisp, 1954. Distribution of certain intertidal animals around the Irish Coast. Proceedings of the Royal Irish Academy 57: 1–29.
Southward, A. J., S. J. Hawkins & M. Burrows, 1995. Seventy years’ observations of changes in distribution and abundance of zooplankton and intertidal organisms in the western English Channel in relation to rising sea temperature. Journal of Thermal Biology 20: 127–155.
Southward, A. J., O. Langmead, N. J. Hardman-Mountford, J. Aiken, G. T. Boalch, P. R. Dando, M. J. Genner, I. Joint, M. A. Kendall, N. C. Halliday, R. P. Harris, R. Leaper, N. Mieszkowska, R. D. Pingree, A. J. Richardon, D. W. Sims, T. Smith, A. W. Walne & S. J. Hawkins, 2005. Long-term oceanographic and ecological research in the Western English Channel. Advances in Marine Biology 47: 1–105.
Vermeij, G. J., 1971. Temperature relationships of some tropical Pacific intertidal gastropods. Marine Biology 10: 308–314.
Wethey, D. S., 2002. Biogeography, competition, and microclimate: the barnacle Chthamalus fragilis in New England. Integrative and Comparative Biology 42: 872–880.
Woodin, S. A., 1974. Polychaete abundance patterns in a marine soft-sediment environment: the importance of biological interactions. Ecological Monographs 44:171–187.
Xunta de Galicia, 2006. Consellería de Pesca y Asuntos Marítimos. Orden de 18 de abril de 2006 por la que se reglan los planes de explotación específicos para poliquetos y se prueban los planes para la explotación de poliquetos en el litoral de Galicia para el año 2006. Diario Oficial de Galicia 80: 6.615. http://www.xunta.es/Doc/Dog2006.nsf/FichaContenido/C452?OpenDocument.
Acknowledgments
Supported by grants from NASA (NNG04GE43G) and NOAA (NA04NOS4780264). We thank Brian Helmuth, Jerry Hilbish, Venkat Lakshmi, Sarah Gilman, Nova Mieszkowska, Sierra Jones, Kyle Aveni-Deforge, Sarah Berke, Lindsay Brin and Alan Southward for stimulating discussions. Sarah Berke and Nova Mieszkowska provided assistance in the field. Two anonymous reviewers, Fernando Lima, Teresa Cruz, and Ruth O’Riordan provided helpful suggestions and information on additional literature.
Author information
Authors and Affiliations
Corresponding author
Additional information
Guest editors: J. Davenport, G. Burnell, T. Cross, M. Emmerson, R. McAllen, R. Ramsay & E. Rogan
Challenges to Marine Ecosystems
Rights and permissions
About this article
Cite this article
Wethey, D.S., Woodin, S.A. Ecological hindcasting of biogeographic responses to climate change in the European intertidal zone. Hydrobiologia 606, 139–151 (2008). https://doi.org/10.1007/s10750-008-9338-8
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-008-9338-8