Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-27T22:13:16.576Z Has data issue: false hasContentIssue false
  • English
  • Français

Seasonal patterns of investment in reproductive and somatic tissues in the squid Loligo forbesi

Published online by Cambridge University Press:  23 December 2005

Jennifer M. Smith ,
Graham J. Pierce ,
Alain F. Zuur  and
Peter R. Boyle
Jennifer M. Smith
Affiliation:
Department of Zoology, School of Biological Sciences, University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, UK
Graham J. Pierce
Affiliation:
Department of Zoology, School of Biological Sciences, University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, UK
Alain F. Zuur
Affiliation:
Highland Statistics Ltd., 6 Laverock Road, Newburgh, Aberdeenshire, AB41 6FN, UK
Peter R. Boyle
Affiliation:
Department of Zoology, School of Biological Sciences, University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, UK
Get access

Abstract

Despite many previous studies on the life history of the squid Loligo forbesi, the roles of internal and external factors in growth and maturation have not previously been investigated in detail. The present study takes advantage of the availability of statistical techniques, namely generalised additive models, which permit simultaneous evaluation of the effects of multiple explanatory variables while avoiding the need to assume linear relationships. This has the further advantage that the size of body parts can be entered directly into the models rather than expressed as indices (e.g., gonado-somatic index). The present analysis is based on measurements taken from monthly market samples during 1989-1991 and aims to infer patterns of reproductive and somatic investment though comparison of large numbers of individuals at different (post recruit) life-cycle stages. Results indicate that, once the effect of body size is removed, gonad weight in both sexes is affected by month and digestive gland weight, consistent with seasonal triggering of maturation, and with energy for gonad growth being derived from food. There is also evidence of a negative relationship between somatic and ovary growth in females, possibly indicating remobilisation of somatic tissue to grow the ovary. In males, relationships between variables tended to have more complex forms, probably related to the existence of two or more growth patterns leading to different sizes at maturity. As found in previous work, maturation begins around 1-2 months earlier in males, suggesting that sensitivity to external triggers is controlled by a sex-dependent internal factor.

Keywords

Life-historyMaturationGeneralised additive modelsSquidLoligo forbesi
Type
Research Article
Information
Aquatic Living Resources , Volume 18 , Issue 4: Environmental Effects on Cephalopod Life History and Fisheries , October 2005 , pp. 341 - 351
Copyright
© EDP Sciences, IFREMER, IRD, 2005

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.)

References

Arkhipkin, A.I., Laptikhovsky, V.V., Nigmatullin, C.M., Bespyatykh, A.V., Murzov, S.A., 1998, Growth, reproduction and feeding of the tropical squid Ornithoteuthis antillarum (Cephalopoda, Ommastrephidae) from the central-east Atlantic. Sci. Mar. 62, 273-288. CrossRef
Arkhipkin, A.I., Silvanovich, N.V., 1997, Age, growth and maturation of the squid Martialia hyadesi (Cephalopoda, Ommastrephidae) in the south-west Atlantic. Antarct. Sci. 9, 373-380. CrossRef
Bellido, J.M., Pierce, G.J., Wang, J., 2001, Modelling intra-annual variation in abundance of squid Loligo forbesi in Scottish waters using generalised additive models. Fish. Res. 52, 23-39. CrossRef
Boyle, P.R., Pierce, G.J., 1994, Fishery biology of the Northeast Atlantic squid. Fish. Res. 21, 1-16. CrossRef
Boyle, P.R., Pierce, G.J., Hastie, L.C., 1995, Flexible reproductive strategies in the squid Loligo forbesi. Mar. Biol. 121, 501-508. CrossRef
Cleveland W.S., 1993, Visualizing Data. AT&T Bell Laboratories, Murray Hill, NJ.
Collins, M.A., Burnell, G.M., Rodhouse, P.G., 1995a, Age and growth of the squid Loligo forbesi (Cephalopoda: Loliginidae) in Irish waters. J. Mar. Biol. Assoc. UK 75, 605-621. CrossRef
Collins, M.A., Burnell, G.M., Rodhouse, P.G., 1995b, Recruitment, maturation and spawning of Loligo forbesi Steenstrup (Cephalopoda: Loliginidae) in Irish waters. ICES J. Mar. Sci. 52, 127-137. CrossRef
Collins, M.A., Burnell, G.M., Rodhouse, P.G., 1995c, Reproductive strategies of male and female Loligo forbesi (Cephalopoda: Loliginidae). J. Mar. Biol. Assoc. UK 75, 621-634. CrossRef
Collins, M.A., Boyle, P.R., Pierce, G.J., Key, L.N., Hughes, S.E., Murphy, J., 1999, Resolution of multiple cohorts in the Loligo forbesi population from the west of Scotland. ICES J. Mar. Sci. 56, 500-509. CrossRef
Forsythe, J.W., 2004, Accounting for the effect of temperature on squid growth in nature: from hypothesis to practice. Mar. Freshw. Res. 55, 331-339. CrossRef
Forsythe, J.W., Walsh, L.S., Turk, P.E., Lee, P.G., 2001, Impact of temperature on juvenile growth and age at first egg-laying of the Pacific reef squid Sepioteuthis lessoniana reared in captivity. Mar. Biol. 138, 103-112. CrossRef
Fox J., 2000, Multiple and Generalized Nonparametric Regression. Sage Publications, Inc., Ontario.
Fox J., 2002, An R and S-Plus Companion to Applied Regression. Sage Publications, Inc., Ontario.
Gabr, H.R., Hanlon, R.T., Hanafy, M.H., El-Etreby, S.G., 1999a, Reproductive versus somatic tissue allocation in the cuttlefish Sepia dollfusi Adam (1941). Bull. Mar. Sci. 65, 159-173.
Gabr, H.R., Hanlon, R.T., El-Etreby, S.G., Hanafy, M.H., 1999b, Reproductive versus somatic tissue growth during the life cycle of the cuttlefish Sepia pharaonis Ehrenberg, 1831. Fish. Bull. 97, 802-811.
Guerra, A., Castro, B.G., 1994, Reproductive-somatic relationships in Loligo gahi (Cephalopoda: Loliginidae) from the Falkland Islands. Antarct. Sci. 6, 175-178. CrossRef
Guerra, A., Rocha, F., 1994, The life history of Loligo vulgaris and Loligo forbesi (Cephalopoda: Loliginidae) in Galician waters (NW Spain). Fish. Res. 21, 43-70. CrossRef
Hanlon R.T., Messenger J.B., 1992, Cephalopod Behaviour. Cambridge University Press.
Hastie T., Tibshirani R.J., 1990, Generalized Additive Models. London, Chapman and Hall/CRC.
Hatfield, E.M.C., Rodhouse, P.G., Barber, D.L., 1992, Production of soma and gonad in maturing female Illex argentinus (Mollusca: Cephalopoda). J. Mar. Biol. Assoc. UK 72, 281-291. CrossRef
Ho, J.D., Moltschaniwskyj, N.A., Carter, C.G., 2004, The effect of variability in growth on somatic condition and reproductive status in the southern calamary Sepioteuthis australis. Mar. Freshw. Res. 55, 423-428. CrossRef
Houlihan, D.F., Kelly, K., Boyle, P.R., 1998, Correlates of growth and feeding in laboratory-maintained Eledone cirrhosa (Cephalopoda: Octopoda). J. Mar. Biol. Assoc. UK 78, 919-932. CrossRef
Jackson, G.D., Forsythe, J.W., Hixon, R.F., Hanlon, R.T., 1997, Age, growth, and maturation of Lolliguncula brevis (Cephalopoda: Loliginidae) in the northwestern Gulf of Mexico with a comparison of length-frequency versus statolith age analysis. Can. J. Fish. Aquat. Sci. 54, 2907-2919. CrossRef
Jackson, G.D., Moltschaniwskyj, N.A., 2002, Spatial and temporal variation in growth rates and maturity in the Indo-Pacific squid Sepioteuthis lessoniana (Cephalopoda: Loliginidae). Mar. Biol. 140, 747-754.
Lum-Kong, A., Pierce, G.J., Yau, C., 1992, Timing of spawning and recruitment in Loligo forbesi (Cephalopoda: Loliginidae) in Scottish waters. J. Mar. Biol. Assoc. UK 72, 301-311. CrossRef
Mangold K., 1987, Reproduction. In: Boyle P.R. (Ed.) Cephalopod Life Cycles. Comparative Reviews, Vol. II. London, Academic Press, pp. 157-200.
Moreno, A., Cunha, M.M., Pereira, J.M., 1994, Population biology of veined squid (Loligo forbesi) and European squid (Loligo vulgaris) from the Portuguese coast. Fish. Res. 21, 71-86. CrossRef
Pierce, G.J., Boyle, P.R., Hastie, L.C., Key, L., 1994a, The life history of Loligo forbesi (Cephalopoda: Loliginidae) in Scottish waters. Fish. Res. 21, 17-41. CrossRef
Pierce, G.J., Hastie, L.C., Guerra, A., Thorpe, R.S., Howard, F.G., Boyle, P.R., 1994b, Morphometric variation in Loligo forbesi and Loligo vulgaris: regional, seasonal, sex, maturity and worker differences. Fish. Res. 21, 127-148. CrossRef
Pierce, G.J., Zuur, A.F., Smith, J.M., Santos, M.B., Bailey, N., Chen, C.-S., Boyle, P.R., 2005, Interannual variation in life-cycle characteristics of the veined squid (Loligo forbesi) in Scottish (UK) waters. Aquat. Living Resour. 18, 327-340. CrossRef
Porteiro, F.M., Martins, H R., 1994, Biology of Loligo forbesi Steenstrup, 1856 (Mollusca: Cephalopoda) in the Azores: sample composition and maturation of squid caught by jigging. Fish. Res. 21, 103-114. CrossRef
Quinn G.P., Keough M.J., 2002, Experimental Design and Data Analysis for Biologists. Cambridge University Press.
Rocha, F., Guerra, A., González, A.F., 2001, A review of reproductive strategies in cephalopods. Biol. Rev. 76, 291-304. CrossRef
Rodhouse, P.G., Symon, C., Hatfield, E.M.C., 1992, Early life cycle of cephalopods in relation to the major oceanographic features of the southwest Atlantic Ocean. Mar. Ecol. Prog. Ser. 89, 183-195. CrossRef
Ryan B.F., Joiner B.L., Ryan T.A., Jr., 1985, Minitab Handbook, 2nd edn. Duxbury Press, Boston.
Semmens, J.M., Moltschaniwskyj, N.A., 2000, An examination of variable growth in the loliginid squid Sepioteuthis lessoniana: a whole animal and reductionist approach. Mar. Ecol. Prog. Ser. 193, 135-141. CrossRef
Thorpe, R.S., 1976, Biometric analysis of geographic variation and racial affinities. Biol. Rev. 51, 407-452. CrossRef
Waluda, C.M., Pierce, G.J., 1998, Temporal and spatial patterns in the distribution of squid Loligo spp. in the United Kingdom waters. S. Afr. J. Mar. Sci. 20, 323-336. CrossRef
Waluda, C.M., Trathan, P.N., Rodhouse, P.G., 1999, Influence of oceanographic variability on recruitment in the Illex argentinus (Cephalopoda: Ommastrephidae) fishery in the south Atlantic. Mar. Ecol. Prog. Ser. 183, 159-167. CrossRef
Wood, S.N., 2000, Modelling and smoothing parameter estimation with multiple quadratic penalties. J. R. Statist. Soc. B 62, 413-428. CrossRef
Wood, S.N., 2004, Stable and efficient multiple smoothing parameter estimation for generalized additive models. J. Am. Statist. Assoc. 99, 637-686. CrossRef
Young, I.A.G., Pierce, G.J., Daly, H.I., Santos, M.B., Key, L.N., Bailey, N., Robin, J.P., Bishop, A.J., Stowasser, G., Nyegaard, M., Cho, S.K., Rasero, M., Pereira, J.M.F., 2004, Application of depletion methods to estimate stock size in the squid Loligo forbesi in Scottish waters (UK). Fish. Res. 69, 211-227. CrossRef