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Size-effect, asymmetry, and small-scale spatial variation in otolith shape of juvenile sole in the Southern North Sea

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Abstract

While otolith shape analysis can provide a valuable tool for discriminating between fish populations, factors which may influence otolith shape, such as the effect of size, directional asymmetry in growth, and local environmental conditions, are often unknown. Here, we analyzed differences in otolith shape across three size classes of age-0 common sole Solea solea L. from nursery grounds off the Belgian coast and in the Wadden Sea. Across size classes, form-factor decreased and roundness remained consistently high in both nursery grounds, while ellipticity increased in the Belgian nursery. Directional asymmetry between left and right otoliths measured by Fourier coefficients accounted for 0.96 and 7.2% of the variance when comparing otoliths overall, and for each size class, respectively. Within the Belgian nursery, results were consistent across sampling years and locations. In addition, otolith shape was marginally different between nursery grounds, but highly variable within nursery grounds. A small divergent group, which seems partly related to fish size, was noted at both spatial and temporal scales. Based on these results and before embarking on a study of population structure using otolith shape in age-0 common sole, we recommend testing for directional asymmetry and fish size effects across the entire region of interest.

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References

  • Amara, R., F. Lagardère & Y. Desaunay, 1993. Seasonal distribution and duration of the planktonic stage of Dover sole, Solea solea, larvae in the Bay of Biscay: an hypothesis. Journal of Fish Biology 43: 17–30.

    Article  Google Scholar 

  • Anken, R. H., M. Beier & H. Rahmann, 2002. Influence of hypergravity on fish inner ear otoliths: I. Developmental growth profile. Advances in Space Research 30: 721–725.

    Article  CAS  PubMed  Google Scholar 

  • Burt, G. J. & R. S. Millner, 2008. Movements of sole in the Southern North Sea and Eastern English Channel from tagging studies (1955–2004). Science Series Technical Report, Vol. 143. Cefas, Lowestoft: 1–44.

  • Cadrin, S. X., A. L. Kerr & S. Mariani (eds), 2014. Stock Identification Methods: Applications in Fishery Science. Academic, Amsterdam.

    Google Scholar 

  • Campana, S. E., 2005. Otolith elemental composition as a natural marker of fish stocks. In Stock Identification Methods. Academic, Burlington: 227–245.

    Chapter  Google Scholar 

  • Campana, S. E. & J. M. Casselman, 1993. Stock discrimination using otolith shape analysis. Canadian Journal of Fisheries and Aquatic Sciences 50: 1062–1083.

    Article  Google Scholar 

  • Capoccioni, F., C. Costa, J. Aguzzi, P. Menesatti, A. Lombarte & E. Ciccotti, 2011. Ontogenetic and environmental effects on otolith shape variability in three Mediterranean European eel (Anguilla anguilla, L.) local stocks. Journal of Experimental Marine Biology and Ecology 397: 1–7.

    Article  Google Scholar 

  • Cardinale, M., P. Doering-Arjes, M. Kastowsky & H. Mosegaard, 2004. Effects of sex, stock, and environment on the shape of known-age Atlantic cod (Gadus morhua) otoliths. Canadian Journal of Fisheries and Aquatic Sciences 61: 158–167.

    Article  Google Scholar 

  • Costanza, R., R. d’Arge, R. De Groot, S. Farber, M. Grasso, B. Hannon, K. Limburg, S. Naeem, R. V. O’Neill, J. Paruelo, R. J. Raskin, P. Sutton & M. van den Belt, 1998. The value of ecosystem services: putting the issues in perspective. Ecological Economics 25: 67–72.

    Article  Google Scholar 

  • Crampton, J. S., 1995. Elliptic Fourier shape analysis of fossil bivalves: some practical considerations. Lethaia 28: 179–186.

    Article  Google Scholar 

  • Cuveliers, E., A. Geffen, J. Guelinckx, J. Raeymaekers, J. Skadal, F. Volckaert & G. Maes, 2010. Microchemical variation in juvenile Solea solea otoliths as a powerful tool for studying connectivity in the North Sea. Marine Ecology Progress Series 401: 211–220.

    Article  CAS  Google Scholar 

  • Cuveliers, E. L., M. H. D. Larmuseau, B. Hellemans, S. L. N. A. Verherstraeten, F. A. M. Volckaert & G. E. Maes, 2012. Multi-marker estimate of genetic connectivity of sole (Solea solea) in the North-East Atlantic Ocean. Marine Biology 159: 1239–1253.

    Article  CAS  Google Scholar 

  • Degraer, S., E. Verfaillie, W. Willems, E. Adriaens, M. Vincx & V. Van Lancker, 2008. Habitat suitability modelling as a mapping tool for macrobenthic communities: an example from the Belgian part of the North Sea. Continental Shelf Research 28: 369–379.

    Article  Google Scholar 

  • Diopere, E., A. Cariani, S. Vandamme, J. Van Houdt, F. Tinti, F. A. M. Volckaert, FISHPOPTRACE Consortium & G. E. Maes, 2018. Seascape genetics of a flatfish reveals local selection under high levels of gene flow. ICES Journal of Marine Science 75: 675–689.

    Article  Google Scholar 

  • Gagliano, M. & M. I. McCormick, 2004. Feeding history influences otolith shape in tropical fish. Marine Ecology Progress Series 278: 291–296.

    Article  Google Scholar 

  • Gonzalez-Salas, C. & P. Lenfant, 2007. Interannual variability and intraannual stability of the otolith shape in European anchovy Engraulis encrasicolus (L.) in the Bay of Biscay. Journal of Fish Biology 70: 35–49.

    Article  Google Scholar 

  • Hüssy, K., 2008. Otolith shape in juvenile cod (Gadus morhua): ontogenetic and environmental effects. Journal of Experimental Marine Biology and Ecology 364: 35–41.

    Article  Google Scholar 

  • Jung, A., R. Dekker, M. Germain, C. Philippart, J. Witte & H. van der Veer, 2017. Long-term shifts in intertidal predator and prey communities in the Wadden Sea and consequences for food requirements and supply. Marine Ecology Progress Series 579: 37–53.

    Article  Google Scholar 

  • Kaplan, D. M., M. Cuif, C. Fauvelot, L. Vigliola, T. Nguyen-Huu, J. Tiavouane & C. Lett, 2017. Uncertainty in empirical estimates of marine larval connectivity. ICES Journal of Marine Science 74: 1723–1734.

    Article  Google Scholar 

  • Kotoulas, G., F. Bonhomme & P. Borsa, 1995. Genetic structure of the common sole Solea vulgaris at different geographic scales. Marine Biology 122: 361–375.

    Article  Google Scholar 

  • Kuhl, F. P. & C. R. Giardina, 1982. Elliptic Fourier features of a closed contour. Computer Graphics and Image Processing 18: 236–258.

    Article  Google Scholar 

  • Lacroix, G., G. E. Maes, L. J. Bolle & F. A. M. Volckaert, 2013. Modelling dispersal dynamics of the early life stages of a marine flatfish (Solea solea L.). Journal of Sea Research 84: 13–25.

    Article  Google Scholar 

  • Lagardère, F. & H. Troadec, 1997. Age estimation in common sole Solea solea larvae: validation of daily increments and evaluation of a pattern recognition technique. Marine Ecology Progress Series 155: 223–237.

    Article  Google Scholar 

  • Le Pape, O. & N. Cognez, 2016. The range of juvenile movements of estuarine and coastal nursery dependent flatfishes: estimation from a meta-analytical approach. Journal of Sea Research 107: 43–55.

    Article  Google Scholar 

  • Le Pape, O., F. Chauvet, S. Mahévas, P. Lazure, D. Guérault & Y. Désaunay, 2003. Quantitative description of habitat suitability for the juvenile common sole (Solea solea, L.) in the Bay of Biscay (France) and the contribution of different habitats to the adult population. Journal of Sea Research 50: 139–149.

    Article  Google Scholar 

  • Legendre, P. & L. Legendre (eds), 2012. Numerical Ecology, Vol. 24. Elsevier, Amsterdam: 1006 pp.

    Google Scholar 

  • Lombarte, A., G. J. Torres & B. Morales-Nin, 2003. Specific Merluccius otolith growth patterns related to phylogenetics and environmental factors. Journal of the Marine Biological Association of the UK 83: 277–281.

    Article  Google Scholar 

  • Lychakov, D. V. & Y. T. Rebane, 2005. Fish otolith mass asymmetry: morphometry and influence on acoustic functionality. Hearing Research 201: 55–69.

    Article  CAS  PubMed  Google Scholar 

  • Mahé, K., C. Oudard, T. Mille, J. Keating, P. Gonçalves, L. W. Clausen, G. Petursdottir, H. Rasmussen, E. Meland, E. Mullins, J. K. Pinnegar, Å. Hoines & V. M. Trenkel, 2016. Identifying blue whiting (Micromesistius poutassou) stock structure in the Northeast Atlantic by otolith shape analysis. Canadian Journal of Fisheries and Aquatic Sciences 73: 1363–1371.

    Article  Google Scholar 

  • Mapp, J., E. Hunter, J. Van Der Kooij, S. Songer & M. Fisher, 2017. Otolith shape and size: the importance of age when determining indices for fish-stock separation. Fisheries Research 190: 43–52.

    Article  Google Scholar 

  • Mérigot, B., Y. Letourneur & R. Lecomte-Finiger, 2007. Characterization of local populations of the common sole Solea solea (Pisces, Soleidae) in the NW Mediterranean through otolith morphometrics and shape analysis. Marine Biology 151: 997–1008.

    Article  Google Scholar 

  • Mille, T., K. Mahé, M. C. Villanueva, H. De Pontual & B. Ernande, 2015. Sagittal otolith morphogenesis asymmetry in marine fishes. Journal of Fish Biology 87: 646–663.

    Article  CAS  PubMed  Google Scholar 

  • Morat, F., 2011. Influence des apports rhodaniens sur les traits d’histoire de vie de la sole commune (Solea solea) : apports de l’étude minéralogique et chimique des otolithes. Thèse de doctorat, spécialité Océanographie, Université Aix Marseille II, Marseille: 308 pp.

  • Morat, F., Y. Letourneur, J. Dierking, C. Pécheyran, G. Bareille, D. Blamart & M. Harmelin-Vivien, 2014. The great melting pot. Common sole population connectivity assessed by otolith and water fingerprints. PLoS ONE 9(1): e86585.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Morat, F., P. Gibert, N. Reynaud, B. Testi, P. Favriou, V. Raymond, G. Carrel & A. Maire, 2017. Spatial distribution, total length frequencies and otolith morphometry as tools to analyse the effects of a flash flood on populations of roach (Rutilus rutilus). Ecology of Freshwater Fish 27: 421–432.

    Article  Google Scholar 

  • Neves, V., D. Silva, F. Martinho, C. Antunes, S. Ramos & V. Freitas, 2018. Assessing the effects of internal and external acoustic tagging methods on European flounder Platichthys flesus. Fisheries Research 206: 202–208.

    Article  Google Scholar 

  • OSPAR Commission (ed.), 2000. Region 2: Greater North Sea. OSPAR Commission, London.

    Google Scholar 

  • Pawson, M. G. & S. Jennings, 1996. A critique of methods for stock identification in marine capture fisheries. Fisheries Research 25: 203–217.

    Article  Google Scholar 

  • Philippe, K., L. Christophe, C. Gwenaelle, H. Xavier, G. Alain, V. Sandrine, Martin Canterbury Christ Church University, W. Mike & C. Andre, 2006. Spatial patterns and GIS habitat modelling of Solea solea, Pleuronectes flesus and Limanda limanda fish larvae in the Eastern English Channel during the spring. Scientia Marina 11: 147–157.

    Google Scholar 

  • Pinsky, M. L., P. Saenz-Agudelo, O. C. Salles, G. R. Almany, M. Bode, M. L. Berumen, S. Andréfouët, S. R. Thorrold, G. P. Jones & S. Planes, 2017. Marine dispersal scales are congruent over evolutionary and ecological time. Current Biology 27: 149–154.

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team, 2011. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.

    Google Scholar 

  • Rabaut, M., M. Audfroid Calderón, L. Van de Moortel, J. van Dalfsen, M. Vincx, S. Degraer & N. Desroy, 2013. The role of structuring benthos for juvenile flatfish. Journal of Sea Research 84: 70–76.

    Article  Google Scholar 

  • Rohlf, F. J. & J. W. Archie, 1984. A comparison of Fourier methods for the description of wing shape in mosquitoes (Diptera: Culicidae). Systematic Biology 33: 302–317.

    Google Scholar 

  • Russell, F. S. (ed.), 1976. The eggs and planktonic stages of British marine fishes. Academic, London: 524 pp.

    Google Scholar 

  • Thorrold, S. R., C. Latkoczy, P. K. Swart & C. M. Jones, 2001. Natal homing in a marine fish metapopulation. Science (New York, NY) 291: 297–299.

    Article  CAS  Google Scholar 

  • Tuset, V. M., I. J. Lozano, J. A. González, J. F. Pertusa & M. M. García-Díaz, 2003. Shape indices to identify regional differences in otolith morphology of comber, Serranus cabrilla (L., 1758). Journal of Applied Ichthyology 19: 88–93.

    Article  Google Scholar 

  • Van der Land, M. A., 1991. Distribution of flatfish eggs in the 1989 egg surveys in the southeastern North Sea, and mortality of plaice and sole eggs. Netherlands Journal of Sea Research 27: 277–286.

    Article  Google Scholar 

  • Van der Veer, H., J. Koot, G. Aarts, R. Dekker, W. Diderich, V. Freitas & J. Witte, 2011. Long-term trends in juvenile flatfish indicate a dramatic reduction in nursery function of the Balgzand intertidal, Dutch Wadden Sea. Marine Ecology Progress Series 434: 143–154.

    Article  Google Scholar 

  • Van Hoey, G., S. Degraer & M. Vincx, 2004. Macrobenthic community structure of soft-bottom sediments at the Belgian Continental Shelf. Estuarine, Coastal and Shelf Science 59: 599–613.

    Article  Google Scholar 

  • Vieira, A. R., A. Neves, V. Sequeira, R. B. Paiva & L. S. Gordo, 2014. Otolith shape analysis as a tool for stock discrimination of forkbeard (Phycis phycis) in the Northeast Atlantic. Hydrobiologia 728: 103–110.

    Article  Google Scholar 

  • Vignon, M. & F. Morat, 2010. Environmental and genetic determinant of otolith shape revealed by a non-indigenous tropical fish. Marine Ecology-Progress Series 411: 231–241.

    Article  Google Scholar 

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Acknowledgements

Special thanks to K. Vanhalst (Institute for Agricultural and Fisheries Research, ILVO), the crew of RV Simon Stevin and RV Belgica, L. Bolle (Wageningen Marine Research), the crew of RV Stern, and the B-FishConnect Team for sampling. We are grateful to E. De Keyser, H. Christiansen, F. M. Heindler, F. Calboli (KU Leuven), B. Ernande (Ifremer), G. Lacroix (Royal Belgian Institute of Natural Sciences, RBINS), A. Vanden Bavière, J. Robbens (ILVO), and M. R. Siskey (Stony Brook University) for constructive comments. The B-FishConnect Project was funded by the Research Foundation: Flanders (Project Number G.0702.13N). Thanks also to three anonymous reviewers, who provided many helpful comments.

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The datasets generated and analyzed during the current study are available from the corresponding author on reasonable request.

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Correspondence to Sophie Delerue-Ricard.

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Guest editors: Steven J. Degraer, Vera Van Lancker, Silvana N.R. Birchenough, Henning Reiss & Vanessa Stelzenmüller / Interdisciplinary research in support of marine management

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10750_2018_3736_MOESM1_ESM.eps

Supplementary material 1 Fig. S1 Cluster dendrogram of the similarity distances of the Fourier coefficients of ten randomly chosen otoliths of juvenile sole, based on Ward’s distance. Picture numbers range from 1 to 40, with four consecutive pictures (e.g., 1–4, 5–8, etc.) being from the same otolith (EPS 562 kb)

10750_2018_3736_MOESM2_ESM.eps

Supplementary material 2 Fig. S2 Boxplot of roundness for 314 age-0 sole juveniles of sole at three size classes for each dataset (BE2013, BE2014 and NL2014) (EPS 89 kb)

10750_2018_3736_MOESM3_ESM.eps

Supplementary material 3 Fig. S3 Cluster dendrogram of the similarity distances of the Fourier coefficients of the juvenile sole sampled at the Belgian and Wadden Sea nursery grounds in 2014 (a) and at the Belgian nursery in 2013 and 2014 (b) using a complete hierarchical clustering method, based on Ward’s distance (EPS 309 kb)

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Delerue-Ricard, S., Stynen, H., Barbut, L. et al. Size-effect, asymmetry, and small-scale spatial variation in otolith shape of juvenile sole in the Southern North Sea. Hydrobiologia 845, 95–108 (2019). https://doi.org/10.1007/s10750-018-3736-3

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