Hostname: page-component-848d4c4894-75dct Total loading time: 0 Render date: 2024-05-24T23:46:53.925Z Has data issue: false hasContentIssue false

The effect of temperature on growth of early life stages of the common squid Loligo vulgaris

Published online by Cambridge University Press:  27 February 2012

A. Moreno*
Instituto Nacional de Recursos Biológicos, INRB/L–IPIMAR, Avenida Brasília, 1400-038 Lisboa, Portugal
G.J. Pierce
University of Aberdeen, Oceanlab, Main Street, Newburgh, Aberdeenshire, AB41 6AA, UK
M. Azevedo
Instituto Nacional de Recursos Biológicos, INRB/L–IPIMAR, Avenida Brasília, 1400-038 Lisboa, Portugal
J. Pereira
Instituto Nacional de Recursos Biológicos, INRB/L–IPIMAR, Avenida Brasília, 1400-038 Lisboa, Portugal
A.M.P. Santos
Instituto Nacional de Recursos Biológicos, INRB/L–IPIMAR, Avenida Brasília, 1400-038 Lisboa, Portugal
Correspondence should be addressed to: A. Moreno, Instituto Nacional de Recursos Biológicos, INRB/L–IPIMAR, Avenida Brasília, 1400-038 Lisboa, Portugal email:


The squid Loligo vulgaris has an extended spawning season within the upwelling system off north-west Portugal, and its paralarvae may thus develop under a wide range of environmental conditions. Both temperature and salinity are expected to affect the metabolism of young squid and we tested their effects on growth during the embryonic and post-hatching phase, based on measurements of growth increments in statoliths of juveniles and adults, using generalized additive models. There was no evidence that statolith increments representing early growth become unreadable in adult statoliths. Variability in the statolith size at hatching was weakly but significantly related to the variables in the model. On the other hand, the effects on statolith growth of both sea surface temperature and of sea bottom temperature were significant during early post-hatching life. Thicker increments are deposited in the statoliths of squid living under higher temperatures, which results in summer hatchers having larger statoliths at the age of 90 days. Inspection of the statolith accretion pattern, using a piecewise linear regression method, revealed an ontogenetic shift in increment width, which may be an indication of the age of transition from paralarva to juvenile. On this basis, it is suggested that the planktonic stage lasts 60 or 90 days, depending on whether the paralarvae lived at higher (>15°C) or lower (<15°C) sea surface temperatures. The life strategy under warmer conditions potentially favours survival by reducing the duration of the vulnerable planktonic phase.

Research Article
Copyright © Marine Biological Association of the United Kingdom 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)



Arístegui, J., Álvarez-Salgado, X.A., Barton, E.D., Figueiras, F.G., Hernández-León, S., Roy, C. and Santos, A.M.P. (2006) Oceanography and fisheries of the Canary Current/Iberian region of the eastern North Atlantic. In Brink, K.H. and Robinson, A.R. (eds) The sea. Volume 14B: the global coastol ocean. Cambridge, MA: Harvard University Press, pp. 877931.Google Scholar
Arkhipkin, A.I. (2004) Diversity in growth and longevity in short-lived animals: squid of the suborder Oegopsina. Marine and Freshwater Research 55, 341355.Google Scholar
Arkhipkin, A.I. (2005) Statoliths as ‘black boxes’ (life recorders) in squid. Marine and Freshwater Research 56, 573583.CrossRefGoogle Scholar
Boavida-Portugal, J., Moreno, A., Gordo, L. and Pereira, J. (2010) Environmentally adjusted reproductive strategies in females of the commercially exploited common squid Loligo vulgaris . Fisheries Research 106, 193198.Google Scholar
Boeuf, G. and Payan, P. (2001) How should salinity influence fish growth? Comparative Biochemistry and Physiology Part C 130, 411423.Google Scholar
Boletzky, S.v. (2003) Biology of early life stages in cephalopod molluscs. Advances in Marine Biology 44, 143203.Google Scholar
Boyle, P.R., Pierce, G.J. and Hastie, L.C. (1995) Flexible reproductive strategies in the squid Loligo forbesi . Marine Biology 121, 501508.Google Scholar
Brodziak, J.K.T. and Macy, W.K. (1996) Growth of long-finned squid, Loligo pealei, in the Northwest Atlantic. Fisheries Bulletin 94, 212236.Google Scholar
Campana, S.E. and Neilson, J.D. (1985) Microstructure of fish otoliths. Canadian Journal of Fisheries and Aquatic Sciences 42, 10141032.CrossRefGoogle Scholar
Cinti, A., Barón, P.J. and Rivas, A.L. (2004) The effects of environmental factors on the embryonic survival of the Patagonian squid Loligo gahi . Journal of Experimental Marine Biology and Ecology 313, 225240.Google Scholar
Cunha, M.E. (2001) Physical control of biological processes in a coastal upwelling system: comparison of the effects of coastal topography, river run-off and physical oceanography in the northern and southern parts of western Portuguese coastal waters. PhD thesis. Faculdade de Ciências da Universidade de Lisboa, Lisboa, Portugal.Google Scholar
Durholtz, M.D., Lipinski, M.R. and Field, J.G. (2002) Laboratory validation of periodicity of incrementation in statoliths of the South African chokka squid Loligo vulgaris reynaudii (d'Orbigny, 1845): a re-evaluation. Journal of Experimental Marine Biology and Ecology 279, 4159.Google Scholar
Forsythe, J.W. (1993) A working hypothesis of how seasonal temperature change may impact the field growth of young cephalopods. In Okutani, T., O'Dor, R.K. and Kubodera, T. (eds) Recent advances in fishery biology. Tokyo: Tokai University Press, pp. 133143.Google Scholar
Forsythe, J.W. (2004) Accounting for the effect of temperature on squid growth in nature: from hypothesis to practice. Marine and Freshwater Research 55, 331339.Google Scholar
González, A.F., Otero, J., Pierce, G.J. and Guerra, A. (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, 11191127.Google Scholar
Gu, C. and Wahba, G. (1991) Minimizing GCV/GML scores with multiple smoothing parameters via the Newton method. SIAM Journal on Scientific and Statistical Computing 12, 383398.CrossRefGoogle Scholar
Hastie, T. and Tibshirani, R. (1990) Generalized additive models. London: Chapman & Hall.Google Scholar
Hatfield, E. (2000) Do some like it hot? Temperature as a possible determinant of variability in the growth of the Patagonian squid, Loligo gahi (Cephalopoda: Loliginidae). Fisheries Research 47, 2740.Google Scholar
Jackson, G.D. and Domeier, M.L. (2003) The effects of an extraordinary El Niño/La Niña event on the size and growth of the squid Loligo opalescens off Southern California. Marine Biology 142, 925935.Google Scholar
Jackson, G.D. and Moltschaniwskyj, N.A. (2002) Spatial and temporal variation in growth rates and maturity in the Indo-Pacific squid Sepioteuthis lessoniana (Cephalopoda: Loliginidae). Marine Biology 140, 747754.Google Scholar
Moreno, A. (2002) Morfologia e micro-estrutura dos estatólitos de lula, Loligo vulgaris: metodologias de determinação de idades. Relatórios Científicos e Técnicos do Instituto de Investigação das Pescas e do Mar 86, 146.Google Scholar
Moreno, A., Pereira, J., Arvanitidis, C., Robin, J.P., Koutsoubas, D., Perales-Raya, C., Cunha, M.M., Balguerías, E. and Denis, V. (2002) Biological variation of Loligo vulgaris (Cephalopoda: Loliginidae) in the eastern Atlantic and Mediterranean. Bulletin of Marine Science 71, 515534.Google Scholar
Moreno, A., Pereira, J. and Cunha, M.M. (2005) The effect of time of hatching in age and size at maturity of Loligo vulgaris . Aquatic Living Resources 18, 377384.Google Scholar
Moreno, A., Azevedo, M., Pereira, J. and Pierce, G.J. (2007) Growth strategies in the squid Loligo vulgaris from Portuguese waters. Marine Biology Research 3, 4959.Google Scholar
Moreno, A., Dos Santos, A, Piatkowski, U., Santos, A.M.P. and Cabral, H. (2009) Distribution of cephalopod paralarvae in relation to the regional oceanography of the western Iberia. Journal of Plankton Research 31, 7391.Google Scholar
Muggeo, V.M.R. (2003) Estimating regression models with unknown break-points. Statistics in Medicine 22, 30553071.Google Scholar
Muggeo, V.M.R. (2008) Segmented: an R Software to Fit Regression Models with Broken-Line Relationships. RNews 8/1, 2025.Google Scholar
O'Dor, R.K. and Webber, D.M. (1986) The constraints on cephalopods: why squid aren't fish. Canadian Journal of Zoology 64, 15911605.Google Scholar
Pecl, G.T. and Jackson, G.D. (2008) The potential impacts of climate change on inshore squid: biology, ecology and fisheries. Reviews in Fisheries Biology and Fisheries 18, 373385.Google Scholar
Pilar-Fonseca, T., Campos, A., Afonso-Dias, M., Fonseca, P. and Mendes, B. (2009) Fleet segmentation of the Portuguese coastal trawl fishery: a contribution to fisheries management. International Council for the Exploration of the Sea (CM Papers and Reports), CM 2009/O:29, 17 pp.Google Scholar
Preuss, T., Lebaric, Z.N. and Gilly, W.F. (1997) Post-hatching development of circular mantle muscles in the squid Loligo opalescens. Biology Bulletin. Marine Biological Laboratory, Woods Hole 192, 375387.Google Scholar
Rocha, F. and Guerra, A. (1999) Age and growth of two sympatric squids Loligo vulgaris and Loligo forbesi, in Galician waters (north–west Spain). Journal of the Marine Biological Association of the United Kingdom 79, 697707.Google Scholar
Semmens, J.M., Pecl, G.T., Gillanders, B.M., Waluda, C.M., Shea, E.K., Jouffre, D., Ichii, T., Zumholz, K., Katugin, O.N., Leporati, S.C. and Shaw, P.W. (2007) Approaches to resolving cephalopod movement and migration patterns. Reviews in Fisheries Biology and Fisheries 17, 401423.Google Scholar
Sen, H. (2005a) Temperature tolerance of loliginid squid (Loligo vulgaris Lamarck, 1798) eggs in controlled conditions. Turkish Journal of Fisheries and Aquatic Sciences 5, 5356.Google Scholar
Sen, H. (2005b) Incubation of European squid (Loligo vulgaris Lamarck, 1798) eggs at different salinities. Aquaculture Research 36, 876881.CrossRefGoogle Scholar
Shea, E.K. and Vechione, M. (2002) Quantification of ontogenetic discontinuities in three species of oegopsid squids using model II piecewise linear regression. Marine Biology 140, 971979.Google Scholar
Sponaugle, S. (2010) Otolith microstructure reveals ecological and oceanographic processes important to ecosystem-based management. Environmental Biology of Fishes 89, 221238.Google Scholar
Steer, M.A., Pecl, G. and Moltschaniwskyj, N.A. (2003) Are bigger calamary Sepioteuthis australis hatchlings more likely to survive? A study based on statolith dimensions. Marine Ecology Progress Series 261, 175182.Google Scholar
Thompson, J.T. and Kier, W.M. (2001) Ontogenetic changes in fibrous connective tissue organization in the oval squid, Sepioteuthis lessoniana Lesson, 1830. Biology Bulletin 201, 136153.Google Scholar
Vidal, E.A.G., DiMarco, F.P. and Wormuth, J.H. (2002) Optimizing rearing conditions of hatching loliginid squid. Marine Biology 140, 117127.Google Scholar
Villanueva, R. (2000a) Differential increment-deposition in embryonic statoliths of loliginid squid Loligo vulgaris . Marine Biology 137, 161168.Google Scholar
Villanueva, R. (2000b) Effect of temperature on statolith growth of the European squid Loligo vulgaris during early life. Marine Biology 136, 449460.Google Scholar
Villanueva, R., Arkhipkin, A., Jereb, P., Lefkaditou, E., Lipinski, M.R., Perales-Raya, C., Riba, C and Rocha, F. (2003) Embryonic life of the loliginid squid Loligo vulgaris: comparison between statoliths of Atlantic and Mediterranean populations. Marine Ecology Progress Series 253, 197208.CrossRefGoogle Scholar
Villanueva, R., Moltschaniwskyj, N.A. and Bozzano, A. (2007) Abiotic influences on embryo growth: statoliths as experimental tools in the squid early life history. Reviews in Fisheries Biology and Fisheries 17, 101110.Google Scholar
Wood, S.N. (2000) Modelling and smoothing parameter estimation with multiple quadratic penalties. Journal of the Royal Statistical Society—Series B: Statistical Methodology 62, 413428.Google Scholar
Wooster, W., Bakun, A. and McLain, D. (1976) The seasonal upwelling cycle along the eastern boundary of the North Atlantic. Journal of Marine Research 34, 131141.Google Scholar
Zuur, A.F., Ieno, E.N. and Elphick, C.S. (2010) A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 1, 314.CrossRefGoogle Scholar