Understanding the process of growth in cephalopods
Natalie A. MoltschaniwskyjA School of Aquaculture, Tasmanian Aquaculture and Fisheries Institute, University of Tasmania, Locked Bag 1370, Launceston, Tas. 7250, Australia.
B Email: natalie.moltschaniwskyj@utas.edu.au
Marine and Freshwater Research 55(4) 379-386 https://doi.org/10.1071/MF03147
Submitted: 19 September 2003 Accepted: 23 March 2004 Published: 22 June 2004
Abstract
Many cephalopod species grow throughout their lifetime. Critically, this means that they lack an asymptotic phase of growth, when, for a substantial part of the lifetime, growth slows and body size increases minimally. Understanding the form of the growth curve requires an understanding of the growth processes operating at several biological levels including the relative growth of organs, muscle fibre production and growth, and at the level of proximal composition and protein synthesis. There are key differences in growth processes between fish and cephalopods; cephalopods have a sac-like body form that provides greater surface area for respiration, continuous production of new muscle fibres that ensures a supply of somatic material for growth, and high retention of synthesised protein. These characteristics provide process-orientated explanations for non-asymptotic growth in cephalopods. However, differences found in growth curves of laboratory-reared animals (two-phase growth curve) and of wild animals (single growth curve) suggests that future work will be needed to resolve this paradox. We need to determine the generality of growth processes observed to date, and how biotic and abiotic factors modify these processes during the lifetime of the animals.
Extra keywords: muscle fibres, proximal composition, relative growth, reproduction, whole animal.
Acknowledgments
This review benefited from many conversations and discussions with several of my colleagues and two anonymous referees. I would like to thank, in particular, Gretta Pecl for her valuable comments and willingness to discuss ideas over the years.
Arkhipkin, A. I. (2004). Diversity in growth and longevity in short-lived animals: squid of the Suborder Oegopsida. Marine and Freshwater Research 55, 341–355.
Arkhipkin, A. I. , and Fetisov, A. A. (2000). Population structure and growth of the squid Illex illecebrosus (Cephalopoda: Ommastrephidae) off Nova Scotia, north-west Atlantic. Journal of the Marine Biological Association of the UK 80, 367–368.
| Crossref | GoogleScholarGoogle Scholar |
Arkhipkin, A. I. , Jereb, P. , and Ragonese, S. (2000). Growth and maturation in two successive seasonal groups of the short-finned squid, Illex coindetii from the Strait of Sicily (central Mediterranean). ICES Journal of Marine Science 57, 31–41.
| Crossref | GoogleScholarGoogle Scholar |
Bone, Q. , Pulsford, A. , and Chubb, A. D. (1981). Squid mantle muscle. Journal of the Marine Biological Association of the UK 61, 327–342.
Boucher-Rodoni, R. (1989). Oxygen uptake and ammonia excretion by Nautilus macromphalus. Comptes rendus de l’Academie des Sciences 309, 173–179.
Boucher-Rodoni, R. , and Mangold, K. (1988). Comparative aspects of ammonia excretion in cephalopods. Malacologia 29, 145–151.
Brodziak, J. K. T. , and Macy, W. K. (1996). Growth of long-finned squid, Loligo pealei, in the northwest Atlantic. Fishery Bulletin 94, 212–236.
Castro, B. G. , Garrido, J. L. , and Sotelo, C. G. (1992). Changes in composition of digestive gland and mantle muscle of the cuttlefish Sepia officinalis during starvation. Marine Biology 114, 11–20.
Clarke, A. , Rodhouse, P. G. , Holmes, L. J. , and Pascoe, P. L. (1989). Growth rate and nucleic acid ratio in cultured cuttlefish Sepia officinalis (Mollusca: Cephalopoda). Journal of Experimental Marine Biology and Ecology 133, 229–240.
| Crossref | GoogleScholarGoogle Scholar |
Clarke, A. , Rodhouse, P. G. , and Gore, D. J. (1994). Biochemical composition in relation to the energetics of growth and sexual maturation in the ommastrephid squid Illex argentinus. Philosophical Transactions of the Royal Society of London B 344, 201–212.
Forsythe, J. W. (1993). A working hypothesis of how seasonal change may impact the field growth of young cephalopods. In (Eds. T. Okutani, R. K. O’Dor and T. Kubodera) pp. 133–143. (Tokai University Press: Tokyo, Japan.)
Forsythe, J. W. (2004). Accounting for the effect of temperature on squid growth in nature: from hypothesis to practice. Marine and Freshwater Research 55, 331–339.
Forsythe, J. W. , Walsh, L. S. , Turk, P. E. , and 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. Marine Biology 138, 103–112.
| Crossref | GoogleScholarGoogle Scholar |
Fox-Smith, T. (2002). Protein-nitrogen Flux in the Southern Dumpling Squid Euprymna tasmanica. BSc (Hons) Thesis. (University of Tasmania: Hobart, Australia.)
Frescura, M. , and Hodgson, A. N. (1992). The fine structure of the columellar muscle of some gastropod molluscs. The Veliger 35, 308–315.
García-Berthou, E. (2001). On the misuse of residuals in ecology: testing regression residuals vs. the analysis of covariance. Journal of Animal Ecology 70, 708–711.
| Crossref | GoogleScholarGoogle Scholar |
Hanson, J. , and Lowy, J. (1957). Structure of smooth muscles. Nature 180, 906–909.
Hatfield, E. M. C. (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, 27–40.
| Crossref | GoogleScholarGoogle Scholar |
Hatfield, E. M. C. , Rodhouse, P. G. , and Barber, D. L. (1992). Production of soma and gonad in maturing female Illex argentinus (Mollusca: Cephalopoda). Journal of the Marine Biological Association of the UK 72, 281–291.
Hawkins, A. J. S. (1985). Relationships between synthesis and breakdown of protein, dietary absorption and turnovers of nitrogen and carbon in the blue mussel Mytilus edulis. Oecologia 66, 42–49.
Hayes, J. P. and Shonkwiler, J. S. (2001). Morphometric indicators of body condition: worthwhile or wish thinking? In (Ed J. R. Speakman) pp. 8–38. (Cambridge University Press: Cambridge, UK.)
Ho, J. , 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, 421–426.
Houlihan, D. F. (1991). Protein turnover in ectotherms and its relationships to energetics. In (Ed R. Gilles) pp. 1–43. (Springer-Verlag: Berlin, Germany.)
Houlihan, D. F. , Hall, S. J. , Gray, C. , and Noble, B. S. (1988). Growth rates and protein turnover in Atlantic cod, Gadus morhua. Canadian Journal of Fisheries and Aquatic Sciences 45, 951–964.
Houlihan, D. F. , McMillan, D. N. , Agnisola, C. , Trara Genoino, I. , and Foti, L. (1990). Protein synthesis and growth in Octopus vulgaris. Marine Biology 106, 251–259.
Houlihan, D. F., Mathers, E. M. and Foster, A. (1993). Biochemical correlates of growth rate in fish. In (Eds. J. C. Rankin, F. B. Jensen and T. Kubodera) pp. 45–71. (Chapman and Hall: London, UK.)
Houlihan, D. F. , Kelly, K. , and Boyle, P. R. (1998). Correlates of growth and feeding in laboratory-maintained Eledone cirrhosa (Cephalopoda: Octopoda). Journal of the Marine Biological Association of the UK 78, 919–932.
Hoyle, K. (2002). ‘Growth and Life-history of Octopus pallidus: Effects of Seasonal Temperature Change.%rsquo; BSc (Hons) Thesis. (University of Tasmania: Hobart, Australia.)
Jackson, G. D. (1994). Application and future potential of statolith increment analysis in squids and sepioids. Canadian Journal of Fisheries and Aquatic Sciences 51, 2612–2625.
Jackson, G. D. (2004). Advances in defining the life histories of myopsid squid. Marine and Freshwater Research 55, 357–365.
Jackson, G. D. , and Mladenov, P. V. (1994). Terminal spawning in the deepwater squid Moroteuthis ingens (Cephalopoda: Onychoteuthidae). Journal of Zoology 234, 189–201.
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, 747–754.
| Crossref | GoogleScholarGoogle Scholar |
Jackson, G. D., Arkhipkin, A. I., Bizikov, V. A. and Hanlon, R. T. (1993). Laboratory and field corroboration of age and growth from statoliths and gladii of the loliginid squid Sepioteuthis lessoniana (Mollusca: Cephalopoda In (Eds. T. Okutani, R. K. O’Dor and T. Kubodera) pp. 189–199. (Tokai University Press: Tokyo, Japan.)
Jackson, G. D. , Forsythe, J. W. , Hixon, R. F. , and Hanlon, R. T. (1997). Age, growth, and maturation of Loliguncula brevis (Cephalopoda: Loliginidae) in the northwestern Gulf of Mexico with a comparison of length-frequency versus statolith age analysis. Canadian Journal of Fisheries and Aquatic Sciences 54, 2907–2919.
| Crossref | GoogleScholarGoogle Scholar |
Koueta, N. , and Boucaud-Camou, E. (1999). Food intake and growth in reared early juvenile cuttlefish Sepia officinalis L. (Mollusca Cephalopoda). Journal of Experimental Marine Biology and Ecology 240, 93–109.
| Crossref | GoogleScholarGoogle Scholar |
Koueta, N. , Castro, B. G. , and Boucaud-Camou, E. (2000). Biochemical indices for instantaneous growth estimation in young cephalopod Sepia officinalis L. ICES Journal of Marine Science 57, 1–7.
| Crossref | GoogleScholarGoogle Scholar |
Madan, J. J. , and Wells, M. J. (1966). Cutaneous respiration in Octopus vulgaris. The Journal of Experimental Biology 199, 2477–2483.
Martínez, P. , and Moltschaniwskyj, N. A. (1999). Description of growth in the tropical cuttlefish Sepia elliptica using muscle tissue. Journal of the Marine Biological Association of the UK 79, 317–321.
| Crossref | GoogleScholarGoogle Scholar |
McGrath Steer, B. (2003). Flexibility in Reproductive Strategies of Squid: A Case Stud Using the Arrow Squid Nototodarus gouldi from southeastern Australia. PhD Thesis. (University of Tasmania: Hobart, Australia.)
Moltschaniwskyj, N. A. (1994). Muscle tissue growth and muscle fibre dynamics in the tropical loliginid squid Photololigo sp. (Cephalopoda: Loliginidae). Canadian Journal of Fisheries and Aquatic Sciences 51, 830–835.
Moltschaniwskyj, N. A. (1995). Multiple spawning in the tropical squid Photololigo sp.: what is the cost in somatic growth? Marine Biology 124, 127–135.
Moltschaniwskyj, N. A. , and Jackson, G. (2000). Growth and tissue composition as a function of feeding history in juvenile cephalopods. Journal of Experimental Marine Biology and Ecology 253, 229–241.
| Crossref | GoogleScholarGoogle Scholar |
Moltschaniwskyj, N. A. , and Martínez, P. (1998). Effect of temperature and food levels on the growth and condition of juvenile Sepia elliptica (Hoyle 1885): an experimental approach. Journal of Experimental Marine Biology and Ecology 229, 289–302.
| Crossref | GoogleScholarGoogle Scholar |
Moltschaniwskyj, N. A. , and Semmens, J. M. (2000). Limited use of stored energy reserves for reproduction by the tropical loliginid squid Photololigo sp. Journal of Zoology 251, 307–313.
| Crossref | GoogleScholarGoogle Scholar |
Mommsen, T. P. , Ballantyne, J. , MacDonald, D. , Gosline, J. , and Hochachka, P. W. (1981). Analogues of red and white muscle in squid mantle. Proceedings of the Royal National Academy of Science, USA 78, 3274–3278.
O’Dor, R. K. , and Hoar, J. A. (2000). Does geometry limit squid growth? ICES Journal of Marine Science 57, 8–14.
| Crossref | GoogleScholarGoogle Scholar |
O’Dor, R. K. , and Wells, M. J. (1978). Reproduction versus somatic growth: hormonal control in Octopus vulgaris. The Journal of Experimental Biology 77, 15–31.
O’Dor, R. K. , Mangold, K. , Boucher-Rodoni, R. , Wells, M. J. , and Wells, J. (1984). Nutrient absorption, storage and remobilization in Octopus vulgaris. Marine Behaviour and Physiology 11, 239–258.
Pauly, D. (1998). Why squid, though not fish, may be better understood by pretending they are. South African Journal of Marine Science 20, 47–58.
Pecl, G. , and Moltschaniwskyj, N. (1997). Changes in muscle structure associated with somatic growth in Idiosepius pygmaeus, a small tropical cephalopod. Journal of Zoology, London 242, 751.
Pecl, G. , and Moltschaniwskyj, N. (1999). Somatic growth processes: how are they modified in captivity? Proceedings of the Royal Society of London. Series B. Biological Sciences 266, 1133–1139.
| Crossref | GoogleScholarGoogle Scholar |
Pecl, G. T. (2000). ‘Comparative Life-history of Tropical and Temperate Sepioteuthis Squids in Australian Waters.’ PhD Thesis. (James Cook University: Townsville, Australia.)
Pierce, G. J. , Key, L. N. , Boyle, P. R. , Siegert, K. J. , Goncalves, J. M. , Porteiro, F. M. , and Martins, H. R. (1999). RNA concentration and the RNA to protein ratio in cephalopod tissues: sources of variation and relationship with growth rate. Journal of Experimental Marine Biology and Ecology 237, 185–201.
| Crossref | GoogleScholarGoogle Scholar |
Preuss, T. , Lebaric, Z. N. , and Gilly, W. F. (1997). Post-hatching development of circular mantle muscles in the squid Loligo opalescens. The Biological Bulletin 192, 375–387.
Rodhouse, P. G. (1998). Physiological progenesis in cephalopod molluscs. The Biological Bulletin 195, 17–20.
Rodhouse, P. G. , and Hatfield, E. M. C. (1990). Dynamics of growth and maturation in the cephalopod Illex argentinus de Castellanos, 1960 (Teuthoidea: Ommastrephidae). Philosophical Transactions of the Royal Society of London 329, 229–241.
Rowlerson, A. and Veggetti, A. (2001). Cellular mechanisms of post-embryonic muscle growth in aquaculture. In (Ed I. Johnston) pp. 103–140. (Academic Press: San Diego, USA.)
Segawa, S. , and Hanlon, R. T. (1988). Oxygen-consumption and ammonia excretion rates in Octopus maya, Loligo forbesi and Lolliguncula brevis (Mollusca, Cephalopoda). Marine Behaviour and Physiology 13, 389.
| Crossref | GoogleScholarGoogle Scholar |
Semmens, J. M. (1998). An examination of the role of the digestive gland of two loliginid squids, with respect to lipid: storage or excretion? Proceedings of the Royal Society of London. Series B. Biological Sciences 265, 1685–1690.
| Crossref | GoogleScholarGoogle Scholar |
Semmens, J. M. , and Moltschaniwskyj, N. A. (2000). An examination of variable growth in the loliginid squid Sepioteuthis lessoniana: a whole animal and reductionist approach. Marine Ecology Progress Series 193, 135–141.
Semmens, J. M. , Pecl, G. T. , Villanueva, R. , Jouffre, D. , Sobrino, I. , Wood, J. B. , and Rigby, P. R. (2004). Understanding octopus growth: patterns, variability and physiology. Marine & Freshwater Research 55, 367–377.
Suryanarayanan, H. , and Alexander, K. M. (1971). Fuel reserves of molluscan muscle. Comparative Biochemistry and Physiology 40A, 55–60.
Suthers, I. M. , Fraser, A. , and Frank, K. T. (1992). Comparison of lipid, otolith and morphometric condition indices of pelagic juvenile cod Gadus morhua from the Canadian Atlantic. Marine Ecology Progress Series 84, 31–40.
Tait, R. W. (1986). Aspects Pysiologiques de la Senescence Post Reproductive chez Octopus vulgaris. PhD Thesis. (University of Paris: Paris, France.)
Voss, G. L. (1983). A review of cephalopod fisheries biology. Memoirs of the National Museum of Victoria 44, 229–241.
Weatherley, A. H. (1990). Approaches to understanding fish growth. Transactions of the American Fisheries Society 119, 662–672.
Wootton, R. (1990). Reproduction. In pp. 159–195. (Chapman and Hall: New York, USA.)