Abstract
Sepiolid paralarvae are poorly studied, at least in part, because of the difficulty of accurate identification using morphological analysis. To unravel the biodiversity of sepiolid paralarvae collected in the Ría de Vigo during the upwelling season (2012–2014), and to overcome the difficulties of traditional identification, sepiolid paralarvae were identified by amplifying the barcoding gene cytochrome c oxidase subunit I (COI). In addition, morphometric analysis (Generalised Lineal Models, GLM and Discriminant Analysis, DA) was used to identify morphometric patterns useful for paralarval species identification. Genetic barcoding successfully identified 34 Sepiola pfefferi, 31 Rondeletiola minor, 30 Sepiola tridens, 4 Sepiola atlantica, 2 Sepietta neglecta and 1 Sepiola ligulata. COI analysis also allowed us to infer that the paralarvae of the three most abundant species belonged to the same populations independently of the year sampled. GLM suggested that total length (statistically different among the three species) and tentacle length (statistically larger in S. pfefferi from the other two species) were good variables to distinguish among species. DA succeeded in separating S. pfefferi from S. tridens, but R. minor overlapped along the first axes with both species, decreasing the accurate classification rate to 67%.
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References
Altschul, S. F., 2014. BLAST Algorithm eLS. Wiley, Chichester: 1–4.
Álvarez-Salgado, X. A., F. G. Figueiras, F. F. Perez, S. Groom, E. Nogueira, A. V. Borges, L. Chou, C. G. Castro, G. Moncoiffé, A. F. Ros, A. E. J. Miller, M. Frankignoulle, G. Savidge & R. Wollast, 2003. The Portugal coastal counter current off NW Spain: new insights on its biogeochemical variability. Progress in Oceanography 56: 281–321.
Anderson, F., A. Pilsits, S. Clutts, V. Laptikhovsky, G. Bello, E. Balguerias, M. Lipinski, C. Nigmatulin, J. Pereira, U. Piatkowski, J.-P. Robin, A. Salman & M. Tasende, 2008. Systematics of Alloteuthis (Cephalopoda:Loliginidae) based on molecular and morphometric data. Journal of Experimental Marine Biology and Ecology 364: 99–109.
Aristegui, J., X. A. Álvarez-Salgado, E. D. Barton, F. G. Figueiras, S. Hernández-León, C. Roy & A. M. P. Santos, 2004. Oceanography and fisheries of the Canary current—Iberian region of the eastern North Atlantic. In Robinson, A. R. & K. H. Brink (eds), The Sea. Harvard University Press, Cambridge: 877–932.
Arkhipkin, A. I. & H. Bjørke, 1999. Ontogenetic changes in morphometric and reproductive indices of the squid Gonatus fabricii (Oegopsida, Gonatidae) in the Norwegian Sea. Polar Biology 22: 357–365.
Bandelt, H. J., P. Forster & A. Röhl, 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16: 37–48.
Bello, G. & V. Biagi, 1995. How benthic are sepiolids? Bulletin de l’Institut Oceanographique Numero Special 16 (Monaco).
Bello, G. & P. Paparella, 2003. Scar-bearing cuttlebones in wild-collected Sepia orbignyana (Cephalopoda: Sepiidae) and the effects of scar occurrence on morphometric relationships. Berliner Paläobiol. Abh 3: 13–18.
Bello, G. & A. Salman, 2015. Description of a new sepioline species, Sepiola boletzkyi sp. nov. (Cephalopoda : Sepiolidae), from the Aegean Sea. European Journal of Taxonomy 1912: 1–12.
Boletzky, S. V., 1974. The larvae of Cephalopoda: a review. Thalassia Jugoslavica 10: 45–76.
Boletzky, S. V., 2003. Biology of early life stages in cephalopod molluscs. In Advances in Marine Biology. Elsevier Masson SAS.
Borges, T. C., 1990. Discriminant analysis of geographic variation in hard structures of Todarodes sagittatus (Lamarck 1798) from North Atlantic Ocean. ICES 1990 Shell.Symp./Paper no. 44: 433–440.
Box, G. E. P. & D. R. Cox, 1964. An analysis of transformations. Journal of the Royal Statistical Society. Series B (Methodological) 26: 211–252.
Boyle, P. & P. Rodhouse, 2005. Cephalopods: Ecology and Fisheries. Blackwell Publishers, Hoboken.
Bucklin, A., S. B. Smolenack, A. M. Bentley & P. H. Wiebe, 1997. Gene flow patterns of the euphausiid, Meganyctiphanes norvegica in the NW Atlantic based on mtDNA sequences for cytochrome b and cytochrome oxidase I. Journal of Plankton Research 19: 1763–1781.
Bucklin, A., D. Steinke & L. Blanco-Bercial, 2011. DNA barcoding of marine metazoa. Annual Review of Marine Science 3: 471–508.
Conde-Padín, P., J. W. Grahame & E. Rolán-Alvarez, 2007. Detecting shape differences in species of the Littorina saxatilis complex by morphometric analysis. Journal of Molluscan Studies 73: 147–154.
Czudaj, S., J. Pereira, A. Moreno, U. Saint-Paul & R. Rosa, 2013. Distribution and reproductive biology of the lentil bobtail squid, Rondeletiola minor (Cephalopoda: Sepiolidae) from the Portuguese Atlantic Coast. Marine Biology Research 9: 802–808.
de Heij, A. & J. Goud, 2010. Sepiola tridens spec. nov., an overlooked species (Cephalopoda, Sepiolidae) living in the North Sea and north-eastern AtlanticOcean. Basteria 74: 51–62.
Diekmann, R. & U. Piatkowski, 2002. Early life stages of cephalopods in the Sargasso Sea: distribution and diversity relative to hydrographic conditions. Marine Biology 141: 123–130.
Diekmann, R. & U. Piatkowski, 2004. Species composition and distribution patterns of early life stages of cephalopods at Great Meteor Seamount (subtropical North-east Atlantic). Archive of Fishery and Marine Research 51: 115–131.
Doubleday, Z. A., T. A. A. Prowse, A. Arkhipkin, G. J. Pierce, J. Semmens, M. Steer, S. C. Leporati, S. Lourenço, A. Quetglas, W. Sauer & B. M. Gillanders, 2016. Global proliferation of cephalopods. Current Biology Elsevier 26: R406–R407.
Excoffier, L., G. Laval & S. Schneider, 2005. Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1: 47–50.
Falcon, L. I., M. Vecchione & C. F. E. Roper, 2000. Paralarval gonatid squids (Cephalopoda: Oegopsida) from the Mid-North Atlantic Ocean. Proceedings of the Biological Society of Washington 113: 532–541.
Felsenstein, J., 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791.
Folmer, O., M. Black, W. Hoeh, R. Lutz & R. Vrijenhoek, 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3: 294–299.
Fu, Y. X., 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915–925.
Galarza, A., J. Hidalgo, G. Ocio & P. Rodríguez, 2008. Sexual size dimorphism and determination of sex in Atlantic yellow-legged gulls Larus michahellis lusitanius from Northern Spain. Ardeola 55: 41–47.
Gebhardt, K. & T. Knebelsberger, 2015. Identification of cephalopod species from the North and Baltic Seas using morphology, COI and 18S rDNA sequences. Helgoland Marine Research 69: 259–271.
González, A. F., M. Rasero & A. Guerra, 1994. Preliminary study of Illex coindetii and Todaropsis eblanae (Cephalopoda:Ommastrephidae) in northern Spanish Atlantic waters. Fisheries Research 21: 115–126.
González, A. F., J. Otero, A. Guerra, R. Prego, F. J. Rocha & A. W. Dale, 2005. Distribution of common octopus and common squid paralarvae in a wind-driven upwelling area (Ria of Vigo, northwestern Spain). Journal of Plankton Research 27: 271–277.
González, A. F., J. Otero, G. J. Pierce & A. Guerra, 2010. Age, growth, and mortality of Loligo vulgaris wild paralarvae: implications for understanding of the life cycle and longevity. ICES Journal of Marine Science 67: 1119–1127.
Goodall-Copestake, W. P., G. A. Tarling & E. J. Murphy, 2012. On the comparison of population-level estimates of haplotype and nucleotide diversity: a case study using the gene cox1 in animals. Heredity 109: 50–56.
Grimpe, G., 1921. Teuthologische Mitteilungen VIII. Die Sepiolinen der Nordsee. Zoologischer Anzeiger 53: 1–12.
Groenenberg, D. S. J., J. Goud, A. De Heij & E. Gittenberger, 2009. Molecular phylogeny of North Sea Sepiolinae (Cephalopoda: Sepiolidae) reveals an overlooked Sepiola species. Journal of Molluscan Studies 75: 361–369.
Guerra, A., 1986. Sepiolinae (mollusca, cephalopoda) de la Ría de Vigo. Iberus 6: 175–184.
Guerra, A., P. Sánchez & F. Rocha, 1994. The Spanish fishery for Loligo: recent trends. Fisheries Research 21: 217–230.
Guerra, Á., J. Hernández-Urcera, M. E. Garci, M. Sestelo, M. Regueira, Á. F. González, M. Cabanellas-Reboredo, M. Calvo-Manazza & B. Morales-Nin, 2014. Dwellers in dens on sandy bottoms: Ecological and behavioural traits of Octopus vulgaris. Scientia Marina 78: 405–414.
Guerra, A., J. Hernández-Urcera, M. E. Garci, M. Sestelo, M. Regueira, A. F. Gonzalez, M. Cabanellas-Reboredo, M. Calvo-Manazza & B. Morales-Nin, 2015. Spawning habitat selection by Octopus vulgaris: new insights for a more effective management of this resource. Fisheries Research 167: 313–322.
Inniss, L., A. Simcock, A. Y. Ajawin, A. C. Alcala, P. Bernal, H. P. Calumpong, P. E. Araghi, S. O. Green, P. Harris, O. K. Kamara, K. Kohata, E. Marschoff, G. Martin, B. P. Ferreira, C. Park, R. A. Payet, J. Rice, A. Rosenberg, R. Ruwa, J. T. Tuhumwire, S. Van Gaever, J. Wang & J. M. Węsławski, 2016. The First Global Integrated Marine Assessment World Ocean Assessment I.
Jereb, P. & C. F. E. Roper, 2005. Cephalopods of the world. An annotated and illustrated catalogue of cephalopod species known to date. Volume Chambered nautiluses and sepioids (Nautilidae, Sepiidae, Sepiolidae, Sepiadariidae, Idiosepiidae and Spirulidae). Food and Agriculture Organization of the United Nations.
Jereb, P., A. Mazzola & M. Di Stefano, 1997. Sepiolinae (Mollusca : Cephalopoda) from the Strait of Sicily. Scientia Marina 61: 459–470.
Lefkaditou, E. & P. Kaspiris, 2005. Distribution and abundance of sepiolids (Mollusca: Cephalopoda) off the north-eastern Greek coasts. Belgian Journal of Zoology 135: 199–204.
Lefkaditou, E., C. Papaconstantinou & K. Anastasopoulou, 1999. Juvenile cephalopods collected in the midwater macroplankton over a trench in the Aegean Sea (Northeastern Mediterranean). Israel Journal of Zoology 45: 395–405.
Lefkaditou, E., C. S. Tsigenopoulos, C. Alidromiti & J. Haralabous, 2012. On the occurrence of Alloteuthis subulata in the Eastern Ionian Sea and its distinction from the sympatric Alloteuthis media. Journal of Biological Research 17: 169–175.
Librado, P. & J. Rozas, 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452.
Moreno, A., A. Dos Santos, U. Piatkowski, A. M. P. Santos & H. Cabral, 2009. Distribution of cephalopod paralarvae in relation to the regional oceanography of the western Iberia. Journal of Plankton Research 31: 73–91.
Moreno, A., G. J. Pierce, M. Azevedo, J. Pereira & A. M. P. Santos, 2012. The effect of temperature on growth of early life stages of the common squid Loligo vulgaris. Journal of the Marine Biological Association of the United Kingdom 92: 1619–1628.
Neige, P. & S. Boletzky, 1997. Morphometrics of the shell of three Sepia species (Mollusca: Cephalopoda): intra- and interspecific variation. Zoologische Beitraege. 38: 137–156.
Nesis, K. N., 1982. Кpaткий oпpeдeлитeль гoлoвoнoгиx мoллюcкoв Mиpoвoгo oкeaнa. Cephalopods of the world: a short key for identification of cephalopods of the World. VAAP Agency of the Russian for light food industry. Publishing House, Moscow.
Nesis, K. N., 1993. Cephalopods of seamounts and submarine ridges. In Okutani, T., R. K. O’dor & T. Kubodera (eds), The Recent Advances in Cephalopod Fishery Biology. Tokai University Press, Shimizu: 365–373.
Orsi Relini, L. & M. Bertuletti, 1989. Sepiolinae (mollusca, cephalopoda) from the Ligurian sea. Vie et Milieu 39: 183–190.
Otero, J., X. A. Alvarez-Salgado, Á. F. Gónzalez, A. Miranda, S. B. Groom, J. M. Cabanas, G. Casas, B. Wheatley & A. Guerra, 2008. Bottom-up control of common octopus Octopus vulgaris in the Galician upwelling system, northeast Atlantic Ocean. Marine Ecology Progress Series 362: 181–192.
Pérez-Gándaras Pedrosa, G., 1980. Cefalópodos del Mar de Galicia. Vigo.
Pérez-Losada, M., M. J. Nolte, K. A. Crandall & P. W. Shaw, 2007. Testing hypotheses of population structuring in the Northeast Atlantic Ocean and Mediterranean Sea using the common cuttlefish Sepia officinalis. Molecular Ecology 16: 2667–2679.
Piatkowski, U., 1998. Modern target sampling techniques provide new insights into the biology of early life stages of pelagic cephalopods. Biologia Marina Mediterranea 5: 260–272.
Pierce, G. J., L. C. Hastie, A. Guerra, R. S. Thorpe, F. G. Howard & P. R. Boyle, 1994a. Morphometric variation in Loligo forbesi and Loligo vulgaris: regional, seasonal, sex, maturity and worker differences. Fisheries Research 21: 127–148.
Pierce, G. J., R. S. Thorpe, L. C. Hastie, A. S. Brierley, Á. Guerra, P. R. Boyle & R. Amieson, 1994b. Geographic variation in Loligo forbesi in the Northeast Atlantic Ocean: analysis of morphometric data and tests of casual hypotheses. Marine Biology 119: 541–547.
Pierce, G. J., V. D. Valavanis, A. Guerra, P. Jereb, L. Orsi-Relini, J. M. Bellido, I. Katara, U. Piatkowski, J. Pereira, E. Balguerias, I. Sobrino, E. Lefkaditou, J. Wang, M. Santurtun, P. R. Boyle, L. C. Hastie, C. D. MacLeod, J. M. Smith, M. Viana, A. F. González & A. F. Zuur, 2008. A review of cephalopod-environment interactions in European Seas. Hydrobiologia 612: 49–70.
Pita, P., D. Fernández-Vidal, J. Garcíaa-Galdo & R. Muíño, 2016. The use of the traditional ecological knowledge of fishermen, cost-effective tools and participatory models in artisanal fisheries: towards the co-management of common octopus in Galicia (NW Spain). Fisheries Research 178: 4–12.
Posada, D. & K. A. Crandall, 2001. Intraspecific gene genealogies: trees grafting into networks. Trends in Ecology and Evolution 16: 37–45.
Rocha, F., A. Guerra, R. Prego & U. Piatkowski, 1999. Cephalopod paralarvae and upwelling conditions off Galician waters (NW Spain). Journal of Plankton Research 21: 21–33.
Rodrigues, M., M. E. Garci, J. S. Troncoso & A. Guerra, 2011. Seasonal abundance of the Atlantic bobtail squid Sepiola atlantica in Galician waters (NE Atlantic). Marine Biology Research 7: 812–819.
Rodrigues, M., M. E. Garcí, J. S. Troncoso & A. Guerra, 2010. Burying behaviour in the bobtail squid Sepiola atlantica (Cephalopoda: Sepiolidae). Italian Journal of Zoology 77: 247–251.
Rosa, R., K. Trübenbach, M. S. Pimentel, J. Boavida-Portugal, F. Faleiro, M. Baptista, G. Dionísio, R. Calado, H. O. Pörtner & T. Repolho, 2014. Differential impacts of ocean acidification and warming on winter and summer progeny of a coastal squid (Loligo vulgaris). The Journal of experimental biology 217: 518–525.
Roura, A., 2013. Ecology of planktonic cephalopod paralarvae in coastal upwelling ecosystems. PhD Dissertation. University of Vigo.
Roura, Á., Á. F. González, K. Redd & Á. Guerra, 2012. Molecular prey identification in wild Octopus vulgaris paralarvae. Marine Biology 159: 1335–1345.
Roura, A., X. A. Álvarez-Salgado, A. F. González, M. Gregori, G. Rosón, J. Otero & A. Guerra, 2016. Life strategies of cephalopod paralarvae in a coastal upwelling system (NW Iberian Peninsula): Insights from zooplankton community and spatio-temporal analyses. Fisheries Oceanography 25: 241–258.
Saitou, N. & M. Nei, 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4: 406–425.
Shaw, P. W., G. J. Pierce & P. R. Boyle, 1999. Subtle population structuring within a highly vagile marine invertebrate, the veined squid Loligo forbesi, demonstrated with microsatellite DNA markers. Molecular Ecology 8: 407–417.
Silva, A., 2003. Morphometric variation among sardine (Sardina pilchardus) populations from the northeastern Atlantic and the western Mediterranean. ICES Journal of Marine Science 3139: 1352–1360.
Song, H., J. E. Buhay, M. F. Whiting & K. A. Crandall, 2008. Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proceedings of the National Academy of Sciences of the United States of America 105: 13486–13491.
Strugnell, J., M. Norman, J. Jackson, A. J. Drummond & A. Cooper, 2005. Molecular phylogeny of coleoid cephalopods (Mollusca: Cephalopoda) using a multigene approach; the effect of data partitioning on resolving phylogenies in a Bayesian framework. Molecular Phylogenetics and Evolution 37: 426–441.
Strugnell, J. M. & A. R. Lindgren, 2007. A barcode of life database for the Cephalopoda? Considerations and concerns. Reviews in Fish Biology and Fisheries 17: 337–344.
Sweeney, M. J., C. F. E. Roper, K. M. Mangold & M. R. Clarke, 1992. “Larval” and juvenile cephalopods: a manual for their identification. Smithsonian Contributions to Zoology, Washington DC 513: 282.
Tajima, F., 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585–595.
Tamura, K. & M. Nei, 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial-DNA in humans and chimpanzees. Molecular Biology and Evolution 10: 512–526.
Tamura, K., G. Stecher, D. Peterson, A. Filipski & S. Kumar, 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729.
Tasende, M., F. Quintero, Arnáiz, R. Bañón, J. M. Campelos, F. Lamas, & A. Gancedo, 2005. La pesquería de calamar (Loligo vulgaris) y puntilla (Alloteuthis spp) con boliche en las Rías Baixas gallegas (1999-2003).
Turan, C. & D. Yaglioglu, 2009. Population identification of common cuttlefish (Sepia officinalis) inferred from genetic, morphometric and cuttlebone chemistry data in the NE Mediterranean Sea. Scientia Marina 74: 77–86.
Voss, G., 1955. The Cephalopoda obtained by the Harvard-Havana Expedition off the coast of Cuba in 1938–39. Bulletin of Marine Science of the Gulf and Caribbean 5: 81–115.
Young, R. E. & R. F. Harman, 1988. Larva, paralarva and subadult in cepalopod terminology. Malacologia 29: 201–207.
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Funding was provided by Ministerio de Economía y Competitividad (Grant Nos. CTM-2011- 25929 and BES – 2012-055651), Fundación Barrié (Grant No. Postdoctoral Grant), and La Trobe University (Grant No. RFWE).
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Guest editors: Erica A. G. Vidal, Ian G. Gleadall & Natalie Moltschaniswskyi / Advances in Cephalopod Ecology and Life Cycles
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Measures undertaken in all sepiolid paralarvae: dorsal mantle length (DML), total length (TL), eye distance (ED) and tentacle length (TeL). Supplementary material 1 (TIFF 25684 kb)
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Graphic representation of the values of the two discriminant equations and the group centroids. Supplementary material 2 (TIFF 34471 kb)
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Olmos-Pérez, L., Roura, Á., Pierce, G.J. et al. Sepiolid paralarval diversity in a regional upwelling area of the NE Atlantic. Hydrobiologia 808, 57–70 (2018). https://doi.org/10.1007/s10750-017-3186-3
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DOI: https://doi.org/10.1007/s10750-017-3186-3