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Stock structure of the English Channel common cuttlefish Sepia officinalis (Linnaeus, 1758) during the reproduction period

Published online by Cambridge University Press:  28 July 2015

Michaël Gras ,
Georges Safi ,
Hugo Lebredonchel ,
Jérôme Quinquis ,
Éric Foucher ,
Noussithé Koueta  and
Jean-Paul Robin
Michaël Gras*
Affiliation:
BOREA, UMR CNRS 7208, IRD 207, UPMC, MNHN, UCBN, 14032 Caen, France Université de Caen Basse-Normandie, UMR BOREA: Biologie des ORganismes et des Ecosystèmes Aquatiques, Esplanade de la paix, CS 14032, 14032 Caen, France
Georges Safi
Affiliation:
BOREA, UMR CNRS 7208, IRD 207, UPMC, MNHN, UCBN, 14032 Caen, France Université de Caen Basse-Normandie, UMR BOREA: Biologie des ORganismes et des Ecosystèmes Aquatiques, Esplanade de la paix, CS 14032, 14032 Caen, France
Hugo Lebredonchel
Affiliation:
BOREA, UMR CNRS 7208, IRD 207, UPMC, MNHN, UCBN, 14032 Caen, France Université de Caen Basse-Normandie, UMR BOREA: Biologie des ORganismes et des Ecosystèmes Aquatiques, Esplanade de la paix, CS 14032, 14032 Caen, France
Jérôme Quinquis
Affiliation:
Ifremer, Laboratoire Ressources Halieutiques, Avenue du Général de Gaulle, BP 32, 14520 Port-en-Bessin, France
Éric Foucher
Affiliation:
Ifremer, Laboratoire Ressources Halieutiques, Avenue du Général de Gaulle, BP 32, 14520 Port-en-Bessin, France
Noussithé Koueta
Affiliation:
BOREA, UMR CNRS 7208, IRD 207, UPMC, MNHN, UCBN, 14032 Caen, France Université de Caen Basse-Normandie, UMR BOREA: Biologie des ORganismes et des Ecosystèmes Aquatiques, Esplanade de la paix, CS 14032, 14032 Caen, France
Jean-Paul Robin
Affiliation:
BOREA, UMR CNRS 7208, IRD 207, UPMC, MNHN, UCBN, 14032 Caen, France Université de Caen Basse-Normandie, UMR BOREA: Biologie des ORganismes et des Ecosystèmes Aquatiques, Esplanade de la paix, CS 14032, 14032 Caen, France
*
Correspondence should be addressed to: M. Gras, BOREA, UMR CNRS 7208, IRD 207, UPMC, MNHN, UCBN, 14032 Caen, France and Université de Caen Basse-Normandie, UMR BOREA: Biologie des ORganismes et des Ecosystèmes Aquatiques, Esplanade de la paix, CS 14032, 14032 Caen, France email: [email protected]
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Abstract

Within the English Channel, the common cuttlefish Sepia officinalis is a semelparous species for which a 2-year life cycle was exclusively described in the 1980s. In the 1990s, new research indicated that whilst a 2-year life cycle was still evident for females and the large majority of males, a small proportion of males were actually maturing at only 1 year of age. Since 1980, the interest of French and UK fishers for this resource has increased and it is nowadays one of the most important demersal species of the area and is considered to be fully exploited. From the start of the 20th century, fishing effort and sea surface temperatures have increased in the English Channel and have probably impacted the life history traits of S. officinalis. A 2-year sampling programme was undertaken at French landing sites of the English Channel during the reproduction season in 2010 and 2011 to estimate if the proportion of 1-year-old mature animals has changed. Age determination was carried out by coupling polymodal decomposition and lipofuscin measurement. Size-at-maturity for each year and each sex was estimated by fitting a binomial error GLM. Results highlight that a variable percentage of males and females belonging to the first cohort are mature and that size-at-maturity was lower than that observed in the 1990s. Finally, different parameters, such as temperature and fishing pressure are explored to discuss changes in life history traits suggesting that cuttlefish could be an indicator of the temperature regime shift in the English Channel.

Keywords

Sepia officinalisEnglish Channellife history traitsmaturitywarmingfishing pressure
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 96 , Issue 1: Oceans and Human Health , February 2016 , pp. 167 - 176
Copyright
Copyright © Marine Biological Association of the United Kingdom 2015 

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References

REFERENCES

Araújo, J.N., Mackinson, S., Ellis, J.R. and Hart, P.J.B. (2005) An Ecopath model for the Western English Channel ecosystem with an exploration of its dynamic properties. Science Series Technical Report, CEFAS Lowestoft, no. 125, 45 pp.Google Scholar
Beaugrand, G. (2009) Decadal changes in climate and ecosystems in the North Atlantic Ocean and adjacent seas. Deep Sea Research Part II: Topical Studies in Oceanography 56, 656–673.CrossRefGoogle Scholar
Beaugrand, G. and Reid, P.C. (2003) Long-term changes in phytoplankton, zooplankton and salmon related to climate. Global Change Biology 9, 801–817.CrossRefGoogle Scholar
Bettencourt, V. and Guerra, A. (2001) Age studies based on daily growth increments in statoliths and growth lamellae in cuttlebone of cultured Sepia officinalis. Marine Biology 139, 327–334.Google Scholar
Bianchi, G., Gislason, H., Graham, K., Hill, L., Jin, X., Koranteng, K., Manickchand-Heileman, S., Paya, I., Sainsbury, K., Sanchez, F. and Zwanenburg, K. (2000) Impact of fishing on size composition and diversity of demersal fish communities. ICES Journal of Marine Science 57, 558–571.CrossRefGoogle Scholar
Bluhm, B.A. and Brey, T. (2001) Age determination in the Antarctic shrimp Notocrangon antarcticus (Crustacea: Decapoda), using the autofluorescent pigment lipofuscin. Marine Biology 138, 247–257.CrossRefGoogle Scholar
Boletzky, S. (1983) Sepia officinalis. In Boyle, P.R. (ed.) Cephalopod life cycles, Vol. 1. Species accounts. London: Academic Press, pp. 31–52.Google Scholar
Boucaud-Camou, E. and Boismery, J. (1991) The migrations of the cuttlefish (Sepia officinalis L.) in the English Channel. In Boucaud-Camou, E. (ed.) La seiche/The cuttlefish. Caen: Centre de publication de l'Université de Caen Basse-Normandie, pp. 179–189.Google Scholar
Boucaud-Camou, E., Koueta, N., Boismery, J. and Medhioub, A. (1991) The sexual maturity of Sepia officinalis L. from the Bay of Seine. In Boucaud-Camou, E. (ed.) La seiche/The cuttlefish. Caen: Centre de publication de l'Université de Caen Basse-Normandie, pp. 141–151.Google Scholar
Boyle, P.R. and Pierce, G.J. (1994) Fishery biology of the Northeast Atlantic squid. Fisheries Research 21, 1–314.CrossRefGoogle Scholar
Boyle, P.R. and Rodhouse, P.G. (2005) Cephalopods: ecology and fisheries. New York, NY: Wiley.CrossRefGoogle Scholar
Campana, S.E. (1990) How reliable are growth back-calculations based on otoliths? Canadian Journal of Fisheries and Aquatic Sciences 47, 2219–2227.CrossRefGoogle Scholar
Carpentier, A., Martin, C.S. and Vaz, S. (2009) Channel habitat atlas for marine resource management, final report/Atlas des habitats des ressources marines de la Manche orientale CHARM II. Boulogne-sur-Mer: Ifremer, 626 pp.Google Scholar
Castro, B.G., Guerra, A. and Jardón, C.M.F. (1991) Variations in digestive gland weights of Sepia officinalis and Sepia elegans through their life cycles. In Boucaud-Camou, E. (ed.) La seiche/The cuttlefish. Caen: Centre de publication de l'Université de Caen Basse-Normandie, pp. 99–104.Google Scholar
Challier, L., Dunn, M.R. and Robin, J.-P. (2005) Trends in age-at-recruitment and juvenile growth of cuttlefish, Sepia officinalis, from the English Channel. ICES Journal of Marine Science 62, 1671–1682.CrossRefGoogle Scholar
Challier, L., Pierce, G.J. and Robin, J.-P. (2006) Spatial and temporal variation in age and growth in juvenile Loligo forbesi and relationships with recruitment in the English Channel and Scottish waters. Journal of Sea Research 55, 217–229.CrossRefGoogle Scholar
Challier, L., Royer, J. and Robin, J.-P. (2002) Variability in age-at-recruitment and early growth in English Channel Sepia officinalis described with statolith analysis. Aquatic Living Resources 15, 303–311.CrossRefGoogle Scholar
Choe, N. and Deibel, D. (2009) Statolith diameter as an age indicator in the planktonic tunicate Oikopleura vanhoeffeni: variability in age-specific growth patterns in Conception Bay, Newfoundland. Journal of Experimental Marine Biology and Ecology 375, 89–98.CrossRefGoogle Scholar
Coelho, M.L. and Martins, M.C. (1991) Preliminary observations on the biology of Sepia officinalis in Ria Formosa, Portugal. In Boucaud-Camou, E. (ed.) La seiche/The cuttlefish. Caen, France: Centre de publication de l'Université de Caen Basse-Normandie, pp. 131–140.Google Scholar
Coelho, M.L., Quintela, J., Bettencourt, V., Olavo, G. and Villa, H. (1994) Population structure, maturation patterns and fecundity of the squid Loligo vulgaris from southern Portugal. Fisheries Research 21, 87–102.CrossRefGoogle Scholar
Domingues, P.M., Bettencourt, V. and Guerra, A. (2006) Growth of Sepia officinalis in captivity and in nature. Vie et Milieu – Life & Environment 56, 109–120.Google Scholar
Doubleday, Z.A. and Semmens, J.M. (2011) Quantification of the age-pigment lipofuscin in known-age octopus (Octopus pallidus): a potential tool for age determination. Journal of Experimental Marine Biology and Ecology 397, 8–12.CrossRefGoogle Scholar
Dunn, M.R. (1999a) Aspects of the stock dynamics and exploitation of cuttlefish, Sepia officinalis (Linnaeus, 1758), in the English Channel. Fisheries Research 40, 277–293.CrossRefGoogle Scholar
Dunn, M.R. (1999b) The exploitation of selected non–quota species in the English Channel. PhD thesis. University of Portsmouth, UK.Google Scholar
Engelhard, G. and Heino, M. (2004) Maturity changes in Norwegian spring-spawning herring Clupea harengus: compensatory or evolutionary responses? Marine Ecology Progress Series 272, 245–256.CrossRefGoogle Scholar
Gauvrit, E., Le Goff, R. and Daguzan, J. (1997) Reproductive cycle of the cuttlefish, Sepia officinalis (L.) in the northern part of the Bay of Biscay. Journal of Molluscan Studies 63, 19–28.CrossRefGoogle Scholar
Gauvrit, E., Pinczon Du Sel, G., Blanc, A. and Daguzan, J. (1998) Detection of cross-mating between two generations of the cuttlefish Sepia officinalis by sperm reservoir analysis. Journal of Molluscan Studies 64, 1–9.CrossRefGoogle Scholar
Gras, M. (2013) Contribution des frayères côtières au recrutement du stock de seiche Sepia officinalis de Manche: lien entre le succès de la phase pré–recrutée et l'abondance de la ressource. PhD thesis. Université de Caen Basse-Normandie, France.Google Scholar
Gras, M., Roel, B.A., Coppin, F., Foucher, E. and Robin, J.-P. (2014) A two-stage biomass model to assess the English Channel cuttlefish (Sepia officinalis L.) stock. ICES Journal of Marine Science 71, 2457–2468.CrossRefGoogle Scholar
Grift, R.E., Rijnsdorp, A.D., Barot, S., Heino, M. and Dieckmann, U. (2003) Fisheries-induced trends in reaction norms for maturation in North Sea plaice. Marine Ecology Progress Series 257, 247–257.CrossRefGoogle Scholar
Guenette, S. and Gascuel, D. (2012) Shifting baselines in European fisheries: the case of the Celtic Sea and Bay of Biscay. Ocean and Coastal Management 70, 10–21.CrossRefGoogle Scholar
Guerra, A. (2006) Ecology of Sepia officinalis. Vie et Milieu – Life & Environment 56, 97–107.Google Scholar
Guerra, A. and Castro, B.G. (1988) On the life-cycle of Sepia officinalis in the Ria de Vigo. Cahiers de Biologie Marine 29, 395–405.Google Scholar
Hawkins, S.J., Southward, A.J. and Genner, M.J. (2003) Detection of environmental change in a marine ecosystem-evidence from the western English Channel. Science of the Total Environment 310, 245–256.CrossRefGoogle Scholar
Hill, K.T. and Womersley, C. (1991) Critical aspects of fluorescent age-pigment methodologies: modification for accurate analysis and age assessments in aquatic organisms. Marine Biology 109, 1–11.CrossRefGoogle Scholar
Ho, J.D., Moltschaniwskyj, N.A. and Carter, C.G. (2004) The effect of variability in growth on somatic condition and reproductive status in the southern calamary Sepioteuthis australis. Marine and Freshwater Research 55, 423–428.CrossRefGoogle Scholar
ICES (2010) Report of the Workshop on Sexual Maturity Staging of Cephalopods (WKMSCEPH). ICES CM 2010/ACOM:49. Technical report, ICES, Livorno, Italy.Google Scholar
Jackson, L.E., Kurtz, J.C. and Fisher, W.S. (2000) Evaluation guidelines for ecological indicators. EPA/620/R-99/005. U.S. Environmental Protection Agency, Office of Research and Development Technical Report May, Research Triangle Park, NC.Google Scholar
Ju, S.J., Secor, D.H. and Harvey, H.R. (1999) Use of extractable lipofuscin for age determination of blue crab Callinectes sapidus. Marine Ecology Progress Series 185, 171–179.CrossRefGoogle Scholar
Kantoussan, J., Ecoutin, J.-M., Fontenelle, G., Thiaw, O.T., Tito de Morais, L. and Laë, R. (2009) The relevance of size parameters as indicators of fishery exploitation in two West African reservoirs. Aquatic Ecology 43, 1167–1178.CrossRefGoogle Scholar
Le Goff, R. and Daguzan, J. (1991) Growth and life cycles of the cuttlefish Sepia officinalis L. (Mollusca: Cephalopoda) in South Brittany (France). Bulletin of Marine Science 49, 341–348.Google Scholar
Le Goff, R., Gauvrit, E., Pinczon Du Sel, G. and Daguzan, J. (1998) Age group determination by analysis of the cuttlebone of the cuttlefish Sepia officinalis L. in reproduction in the Bay of Biscay. Journal of Molluscan Studies 64, 183–193.CrossRefGoogle Scholar
Mangold, K. (1966) Sepia officinalis de la mer Catalane. Vie et Milieu – Life & Environment 17, 961–1012.Google Scholar
Mangold, K. (1987) Reproduction. In Boyle, P.R. (ed.) Cephalopod life cycles, Vol. 1. Species accounts. London: Academic Press, pp. 157–200.Google Scholar
Mangold-Wirz, K. (1963) Biologie des céphalopodes benthiques et nectoniques de la Mer Catalane. Vie et Milieu – Life & Environment 13, 1–285.Google Scholar
Mc Dougall, A. (2004) Assessing the use of sectioned otoliths and other methods to determine the age of the centropomid fish, barramundi (Lates calcarifer) (Bloch), using known-age fish. Fisheries Research 67, 129–141.CrossRefGoogle Scholar
Molfese, C., Beare, D. and Hall-Spencer, J.M. (2014) Overfishing and the replacement of demersal finfish by shellfish: an example from the English Channel. PLoS ONE, 9, 1–10. doi: 10.1371/journal.pone.0101506.CrossRefGoogle ScholarPubMed
Moreno, A., Azevedo, M., Pereira, J.A. and Pierce, G.J. (2007) Growth strategies in the squid Loligo vulgaris from Portuguese waters. Marine Biology Research 3, 49–59.CrossRefGoogle Scholar
Moreno, A., Morais da Cunha, M.M. and Pereira, J.M.F. (1994) Population biology of veined squid (Loligo forbesi) and European squid (Loligo vulgaris) from the Portuguese coast. Fisheries Research 21, 71–86.CrossRefGoogle Scholar
Moreno, A., Pereira, J.A. and Morais da Cunha, M. (2005) Environmental influences on age and size at maturity of Loligo vulgaris. Aquatic Living Resources 18, 377–384.CrossRefGoogle Scholar
Neige, P. (2006) Morphometrics of hard structures in cuttlefish. Vie et Milieu – Life & Environment 56, 121–127.Google Scholar
Newman, S.J. (2002) Growth rate, age determination, natural mortality and production potential of the scarlet seaperch, Lutjanus malabaricus Schneider 1801, off the Pilbara coast of north-western Australia. Fisheries Research 58, 215–225.CrossRefGoogle Scholar
Olsen, E.M., Heino, M., Lilly, G.R., Morgan, M.J., Brattey, J., Ernande, B. and Dieckmann, U. (2004) Maturation trends indicative of rapid evolution preceded the collapse of northern cod. Nature 428, 932–935.CrossRefGoogle ScholarPubMed
Pierce, G.J., Allcock, L., Bruno, I., Bustamante, P., Gonzalez, A.F., Guerra, A., Jereb, P., Lefkaditou, E., Malham, S., Moreno, A., Pereira, J.A., Piatkowski, U., Rasero, M., Sanchez, P., Santos, M.B.N., Santurtun, M., Seixas, S., Sobrino, I. and Villanueva, R. (2010) Cephalopod biology and fisheries in Europe. ICES Cooperative Research Report no. 303, Copenhagen, Denmark.Google Scholar
Pilling, G., Grandcourt, E.M. and Kirkwood, G.P. (2003) The utility of otolith weight as a predictor of age in the emperor Lethrinus mahsena and other tropical fish species. Fisheries Research 60, 493–506.CrossRefGoogle Scholar
Pingree, R.D. (1980) Physical oceanography of the Celtic Sea and English Channel. In Banner, F.T., Collins, M.B. and Massie, K.S. (eds) The North-West European shelf seas: the sea bed and the sea in motion 2. Physical and chemical oceanography, and physical resources, Vol. 24, Part B. Amsterdam: Elsevier, pp. 415–465.Google Scholar
Portail CHARM III–Interreg IV, © (2012) Atlas des pêcheries de Manche, Channel fisheries atlas. Engelhard, G., Vignot, C., Leblond, E., Lesueur, M., Guitton, J. (eds). http://charm-project.org/fr/outils/atlas-des-pecheries/atlas-des-pecheries-outils.Google Scholar
Reznick, D., Lindbeck, E. and Bryga, H. (1989) Slower growth results in larger otoliths: an experimental test with guppies (Poecilia reticulata). Canadian Journal of Fisheries and Aquatic Sciences 46, 108–112.CrossRefGoogle Scholar
Robin, J.-P., Roberts, M., Zeidberg, L., Bloor, I., Rodriguez, A., Briceño, F., Downey, N., Mascaró, M., Navarro, M., Guerra, A., Hofmeister, J., Barcellos, D.D., Lourenço, S.A.P., Roper, C.F.E., Moltschaniwskyj, N.A., Green, C.P. and Mather, J. (2014) Transitions during cephalopod life history: the role of habitat, environment, functional morphology and behaviour. Advances in Marine Biology 67, 361–437.CrossRefGoogle ScholarPubMed
Rodhouse, P.G., Symon, C. and Hatfield, E.M.C. (1992) Early life cycle of cephalopods in relation to the major oceanographic features of the southwest Atlantic Ocean. Marine Ecology Progress Series 89, 183–195.CrossRefGoogle Scholar
Royer, J., Pierce, G.J., Foucher, E. and Robin, J.-P. (2006) The English Channel stock of Sepia officinalis: modelling variability in abundance and impact of the fishery. Fisheries Research 78, 96–106.CrossRefGoogle Scholar
Saulquin, B. and Gohin, F. (2010) Mean seasonal cycle and evolution of the sea surface temperature from satellite and in situ data in the English Channel for the period 1986–2006. International Journal of Remote Sensing 31, 4069–4093.CrossRefGoogle Scholar
Sheehy, M.R.J., Shelton, P.M.J., Wickins, J.F., Belchier, M. and Gaten, E. (1996) Ageing the European lobster Homarus gammarus by the lipofuscin in its eyestalk ganglia. Marine Ecology Progress Series 143, 99–111.CrossRefGoogle Scholar
Shin, Y.-J. and Rochet, M.-J. (1998) A model for the phenotypic plasticity of North Sea herring growth in relation to trophic conditions. Aquatic Living Resources 11, 315–324.CrossRefGoogle Scholar
Shin, Y.-J., Rochet, M.-J., Jennings, S., Field, J.G. and Gislason, H. (2005) Using size-based indicators to evaluate the ecosystem effects of fishing. ICES Journal of Marine Science 62, 384–396.CrossRefGoogle Scholar
Smith, P.J. (1994) Genetic diversity of marine fisheries resources. Possible impacts of fishing. FAO Fisheries Technical Paper no. 344, Rome, Italy.Google Scholar
Southward, A.J., Boalch, G.T. and Maddock, L. (1988) Fluctuations in the herring and pilchard fisheries of Devon and Cornwall linked to change in climate since the 16th century. Journal of the Marine Biological Association of the United Kingdom 68, 423–445.CrossRefGoogle Scholar
Southward, A.J. and Roberts, E.K. (1987) One hundred years of marine research at Plymouth. Journal of the Marine Biological Association of the United Kingdom 67, 465–506.CrossRefGoogle Scholar
Wang, J., Pierce, G.J., Boyle, P.R., Denis, V., Robin, J.-P. and Bellido, J.M. (2003) Spatial and temporal patterns of cuttlefish (Sepia officinalis) abundance and environmental influences – a case study using trawl fishery data in French Atlantic coastal, English Channel, and adjacent waters. ICES Journal of Marine Science 60, 1149–1158.CrossRefGoogle Scholar
Zielinski, S. and Portner, H.-O. (2000) Oxidative stress and antioxidative defence in cephalopods: a function of metabolic rate or age? Comparative Biochemistry and Physiology Part B 125, 147–160.CrossRefGoogle ScholarPubMed