Reviews in Fish Biology and Fisheries

, Volume 18, Issue 4, pp 373–385 | Cite as

The potential impacts of climate change on inshore squid: biology, ecology and fisheries

Article

Abstract

Squid are important components of many marine ecosystems from the poles to the equator, serving as both important predators and prey. Novel aspects of their growth and reproduction mean that they are likely to play an important role in the changing oceans due to climate change. Virtually every facet of squid life-history examined thus far has revealed an incredible capacity in this group for life-history plasticity. The extremely fast growth rates of individuals and rapid rates of turnover at the population level mean that squid can respond quickly to environmental or ecosystem change. Their ‘life-in-the-fast-lane’ life-style allows them to rapidly exploit ‘vacuums’ created in the ecosystem when predators or competitors are removed. In this way, they function as ‘weeds of the sea’. Elevated temperatures accelerate the life-histories of squid, increasing their growth rates and shortening their life-spans. At first glance, it would be logical to suggest that rising water temperatures associated with climate change (if food supply remains adequate) would be beneficial to inshore squid populations and fisheries—growth rates would increase, life spans would shorten and population turnover would accelerate. However, the response of inshore squid populations to climate change is likely to be extremely complex. The size of hatchlings emerging from the eggs becomes smaller as temperatures increase and hatchling size may have a critical influence on the size-at-age that may be achieved as adults and subsequently, population structure. The influence of higher temperatures on the egg and adult stages may thus be opposing forces on the life-history. The process of climate change will likely result in squids that hatch out smaller and earlier, undergo faster growth over shorter life-spans and mature younger and at a smaller size. Individual squid will require more food per unit body size, require more oxygen for faster metabolisms and have a reduced capacity to cope without food. It is therefore likely that biological, physiological and behavioural changes in squid due to climate change will have far reaching effects.

Keywords

Cephalopods Loliginids Environment Population dynamics Life-history Phenology 

Notes

Acknowledgements

We would like to thank Alan Jordan and Jeremy Lyle for constructive comments on this paper, Sean Tracey for producing the figures and Jason Bedelph for technical assistance. GTP was supported by Australian Research Council Linkage Grant LP0347556.

References

  1. Agnew DJ, Hill SL, Beddington JR, Purchase LV, Wakeford RC (2005) Sustainability and management of southwest Atlantic squid fisheries. Bull Mar Sci 76(1):579–593Google Scholar
  2. Alford RA, Jackson GD (1993) Do cephalopods and larvae of other taxa grow asymptotically? Am Nat 141(5):717–728CrossRefPubMedGoogle Scholar
  3. Arkhipkin A (1995) Age, growth and maturation of the European squid Loligo vulgaris (Myopsida, Loliginidae) on the West Saharan Shelf. J Mar Biolog Assoc UK 75:593–604Google Scholar
  4. Arkhipkin AI, Nekludova N (1993) Age, growth and maturation of the loliginid squid Alloteuthis africana and A. subulata on the West Africa Shelf. J Mar Biolog Assoc UK 73:949–961Google Scholar
  5. Augustyn CJ, Lipinski MR, Sauer WHH, Roberts MJ, Mitchell-Innes BA (1994) Chokka squid on the Agulhas Bank: life history and ecology. S Afr J Sci 90:143–154Google Scholar
  6. Bailey KM, Houde ED (1989) Predation on eggs and larvae of marine fishes and the recruitment problem. Adv Mar Biol 25:1–83CrossRefGoogle Scholar
  7. Barón PJ (2002) Embryonic development of Loligo gahi and modeling of hatching frequency distributions in Patagonia. Bull Mar Sci 71(1):165–173Google Scholar
  8. Beaugrand G, Reid PC (2003) Long-term changes in phytoplankton, zooplankton and salmon related to climate. Global Change Biol 9:801–817CrossRefGoogle Scholar
  9. Beddington JR, Rosenberg AA, Crombie JA, Kirkwood GP (1990) Stock assessment and the provisions of management advice for the short fin squid fishery in Falkland Islands waters. Fish Res 8:351–365CrossRefGoogle Scholar
  10. Boletzky S (1994) Embryonic development of cephalopods at low temperatures. Antarc Sci 6(2):139–142Google Scholar
  11. Boyle PR (1990) Cephalopod biology in the fisheries context. Fish Res 8:303–321CrossRefGoogle Scholar
  12. Boyle PR, Boletzky SV (1996) Cephalopod populations: definition and dynamics. Phil Trans R Soc Lond B 351:985–1002CrossRefGoogle Scholar
  13. Boyle PR, Noble L, Emery AM, Craig S, Black KD, Overnell J (2001) Development and hatching in cephalopod eggs: a model system for partitioning environmental and genetic effects on development. In: Atkinson D, Thorndyke M (eds) Environment and animal development: genes, life histories and plasticity. BIOS Scientific Publishers Ltd., Oxford, pp 251–267Google Scholar
  14. Boyle P, Rodhouse P (2005) Cephalopods: ecology and fisheries. Blackwell Publishing, OxfordGoogle Scholar
  15. Brett JR (1979) Environmental factors and growth. In: Hoar WS, Randall DJ, Brett JR (eds), Fish physiology. Academic Press, LondonGoogle Scholar
  16. Brodziak JKT, Macy WK III (1996) Growth of long-finned squid, Loligo pealei, in the northwest Atlantic. Fish Bull 94:212–236Google Scholar
  17. Caddy JF, Rodhouse PG (1998) Cephalopod and groundfish landings: evidence for ecological change in global fisheries? Rev Fish Biol Fish 8:431–444CrossRefGoogle Scholar
  18. Cinti A, Barón PJ, Rivas AL (2004) The effects of environmental factors on the embryonic survival of the Patagonian squid Loligo gahi. J Exp Mar Biol Ecol 313:225–240CrossRefGoogle Scholar
  19. Clark RA, Fox C, Viner D, Livermore M (2003) North Sea cod and climate change—modelling the effects of temperature on population dynamics. Global Change Biol 9(11):1669–1680CrossRefGoogle Scholar
  20. Clarke MR (1987) Cephalopod biomass estimation from predation. In: Boyle PR (ed) Cephalopod life cycles vol II comparative reviews. Academic Press, London, pp 221–238Google Scholar
  21. Clarke A (2003) Costs and consequences of evolutionary temperature adaptation. Trends Ecol Evol 18(11):573–581CrossRefGoogle Scholar
  22. Daufresne M, Roger MC, Capra H, Lamouroux N (2003) Long-term changes within the invertebrate and fish communities of the Upper Rhône River: effects of climatic factors. Global Change Biol 10(1):124–140CrossRefGoogle Scholar
  23. Easterling DR, Meehal GA, Parmesan C, Changnon SA, Karl TR, Mearns LO (2000) Climate extremes: observations, modelling and impacts. Science 289:2068–2074PubMedCrossRefGoogle Scholar
  24. Forsythe JW (2004) Accounting for the effect of temperature on squid growth in nature: from hypothesis to practice. Mar Freshw Res 55:331–339CrossRefGoogle Scholar
  25. Forsythe JW (1993) A working hypothesis of how seasonal temperature change may impact the field growth of young cephalopods. In: Okutani T, O’Dor RK, Kubodera T (eds) Recent advances in cephalopod fisheries biology. Tokai University Press, Tokyo, pp 133–143Google Scholar
  26. Forsythe JW, Van Heukelem WF (1987) Growth. In: Boyle PR (ed), Cephalopod life cycles. Academic Press, London, pp 135–156Google Scholar
  27. Forsythe JW, Walsh LS, Turk PE, Lee PG (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 138:103–112CrossRefGoogle Scholar
  28. Forsythe JW, Hanlon RT (1989) Growth of the Eastern Atlantic squid, Loligo forbesi Streenstrup (Mollusca: Cephalopoda). Aquac Fish Manage 20:1–14Google Scholar
  29. Gowland FC, Boyle P, Noble LR (2002) Morphological variation provides a method of estimating thermal niche in hatchlings of the squid Loligo forbesi (Mollusca: Cephalopoda). J Zool 258:505–513CrossRefGoogle Scholar
  30. Guerra A, González AF, Rocha F (2002) Appearance of the common paper nautilus Argonauta argo related to the increase of the sea surface temperature in the north-eastern Atlantic. J Mar Biol Assoc UK 82:855–858CrossRefGoogle Scholar
  31. Hanlon RT, Kangas N, Forsythe JW (2004) Egg-capsule deposition and how behavioural interactions influence spawning rate in the squid Loligo opalescens in Monterey Bay, California. Mar Biol 145:923–930CrossRefGoogle Scholar
  32. Hanlon RT, Messenger JB (1996) Cephalopod behaviour. Cambridge University Press, CambridgeGoogle Scholar
  33. 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). Fish Res 47:27–40CrossRefGoogle Scholar
  34. Ho JD, Moltschaniwskyj NA, Carter CG (2004) The effect of variability in growth on somatic condition and reproductive status in the southern calamary Sepioteuthis australis. Mar Freshw Res 55:423–428CrossRefGoogle Scholar
  35. Hughes L (2000) Biological consequences of global warming: is the signal already apparent? Trends Ecol Evol 15(2):56–61PubMedCrossRefGoogle Scholar
  36. Jackson GD (2004) Advances in defining the life histories of myopsid squid. Mar Freshw Res 55:357–365CrossRefGoogle Scholar
  37. Jackson GD, Domeier M (2003) The effects of an extraordinary El Niño/La Niña event on the size and growth of the squid Loligo opalescens off Southern California. Mar Biol 142:925–935Google Scholar
  38. Jackson GD, O’Dor RK (2001) Time, space and the ecophysiology of squid growth, life in the fast lane. Vie Milieu 51(4):205–215Google Scholar
  39. Jackson GD, Moltschaniwskyj NA (2001a) The influence of ration level on growth and statolith increment width of the tropical squid Sepioteuthis lessoniana (Cephalopoda: Loliginidae): an experimental approach. Mar Biol 138:819–825CrossRefGoogle Scholar
  40. Jackson GD, Moltschaniwskyj NA (2001b) Temporal variation in growth rates and reproductive parameters in the small near-shore tropical squid Loliolus noctiluca; is cooler better? Mar Ecol Prog Ser 218:167–177CrossRefGoogle Scholar
  41. Jackson GD, Moltschaniwskyj NA (2002) Spatial and temporal variation in growth rates and maturity in the Indo-Pacific squid Sepioteuthis lessoniana (Cephalopoda: Loliginidae). Mar Biol 140:747–754CrossRefGoogle Scholar
  42. Jackson GD, Pecl GT (2003) The dynamics of the summer spawning population of the loliginid squid Sepioteuthis australis in Tasmania, Australia—a conveyor belt of cohorts. ICES J Mar Sci 60:290–296CrossRefGoogle Scholar
  43. Knouft JH (2002) Regional analysis of body size and population density in stream fish assemblages: testing predictions of the energetic equivalence rule. Can J Fish Aquat Sci 59:1350–1360CrossRefGoogle Scholar
  44. Lee PG (1994) Nutrition of cephalopods: fueling the system. Mar Freshw Behav Physiol 25:35–51Google Scholar
  45. Maxwell MR, Hanlon RT (2000) Female reproductive output in the squid Loligo pealei: multiple clutches and implications for a spawning strategy. Mar Ecol Prog Ser 199:159–170CrossRefGoogle Scholar
  46. Maxwell MR, Henry A, Elvidge CD, Safran J, Hobson VR, Nelson I, Tutle BT, Dietz JB, Hunter JR (2004) Fishery dynamics of the California market squid (Loligo opalescens), as measured by satellite remote sensing. Fish Bull 102:661–670Google Scholar
  47. Meyers RA, Worm B (2003) Rapid worldwide depletion of predatory fish communities. Nature 423:280–283CrossRefGoogle Scholar
  48. Moltschaniwskyj NA, Pecl GT (2003) Small-scale spatial and temporal patterns of egg production by the temperate loliginid squid Sepioteuthis australis. Mar Biol 142:509–516Google Scholar
  49. Moltschaniwskyj NA, Pecl GT, Lyle J (2002) The effect of short temporal fishing closures to protect spawning southern calamary populations from fishing pressure in Tasmania, Australia. Bull Mar Sci 70(1):501–514Google Scholar
  50. Moreno A M Azevedo J Pereira GJ Pierce (2007) Growth strategies in the squid Loligo vulgaris from Portuguese waters. Mar Biol Res 3(1):49–59CrossRefGoogle Scholar
  51. Natsukari T, Tashiro M (1991) Neritic squid resources and cuttlefish resources in Japan. Mar Behav Physiol 18:149–226CrossRefGoogle Scholar
  52. O’Dor RK, Webber DM (1986) The constraints on cephalopods: why squid aren’t fish. Can J Zool 64:1591–1605CrossRefGoogle Scholar
  53. O’Dor RK (1992) Big squid in big currents. S Afr J Mar Sci 12:225–235Google Scholar
  54. O’Dor RK, Wells MJ (1987) Energy and nutrient flow. In: Boyle PR (ed), Cephalopod life cycles. Academic Press, London, pp 109–133Google Scholar
  55. Oosthuizen A, Roberts MJ, Sauer W (2002). Temperature effects on the embryonic development and hatching success of the squid Loligo vulgaris reynaudii. Bull Mar Sci 71(2):619–632Google Scholar
  56. Pauly D (1998) Why squid, though not fish, may be better understood by pretending they are. S Afr J Mar Sci 20:47–58Google Scholar
  57. Pecl GT (2000) Comparative life history of tropical and temperate Sepioteuthis squids in Australian waters. PhD Thesis, James Cook University of North Queensland, AustraliaGoogle Scholar
  58. Pecl GT (2001) Flexible reproductive strategies in tropical and temperate Sepioteuthis squids. Mar Biol 138:93–101CrossRefGoogle Scholar
  59. Pecl GT (2004) The in situ relationships between season of hatching, growth and condition in the southern calamary squid, Sepioteuthis australis. Mar Freshw Res 55:429–438CrossRefGoogle Scholar
  60. Pecl GT, Steer MA, Hodgson KE (2004a) The role of hatchling size in generating the intrinsic size-at-age variability of cephalopods: extending the Forsythe hypothesis. Mar Freshw Res 55:387–394CrossRefGoogle Scholar
  61. Pecl GT, Moltschaniwskyj NA, Tracey S, Jordan A (2004b) Inter-annual plasticity of squid life-history and population structure: ecological and management implications. Oecologia 139:515–524PubMedCrossRefGoogle Scholar
  62. Pecl GT, Tracey SR, Semmens JM, Jackson GD (2006) Use of acoustic telemetry for spatial management of southern calamary, Sepioteuthis australis, a highly mobile inshore squid species. Mar Ecol Prog Ser 328:1–15CrossRefGoogle Scholar
  63. Raya CP, Balguerías E, Fernández-Núñez MM, Pierce GJ (1999). On reproduction and age of the squid Loligo vulgaris from the Saharan Bank (north-west African coast). J Mar Biol Assoc UK 79:111–120CrossRefGoogle Scholar
  64. Roberts MJ, Rodhouse P, O’Dor R, Sakarai Y (1998) A global perspective on environmental research on squid. ICES CM. 1998/M:27Google Scholar
  65. Roberts MJ (2005) Chokka squid (Loligo vulgaris reynaudii) abundance linked to changes in South Africa’s Agulhas Bank ecosystem during spawning and the early life cycle. ICES J Mar Sci 62(1):33–55CrossRefGoogle Scholar
  66. Rodhouse PG, Nigmatullin C (1996) Role as consumers. Phil Trans R Soc Lond 351:1003–1022CrossRefGoogle Scholar
  67. Roemmich D, McGowan JA (1995) Climatic warming and the decline of zooplankton in the California current. Science 267:1324–1326PubMedCrossRefGoogle Scholar
  68. Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds A (2003) Fingerprints of global warming on wild plants and animals. Nature 421:57–60PubMedCrossRefGoogle Scholar
  69. Sauer WHH, Smale MJ, Lipinski MR (1992) The location of spawning grounds, spawning and schooling behaviour of the squid Loligo vulgaris reynaudii (Cephalopoda: Myopsida) off the Eastern Cape Coast, South Africa. Mar Biol 114:97–107Google Scholar
  70. Schön P-J, Sauer WHH, Roberts MJ 2002) Environmental influences on spawning aggregations and jig catches of chokka squid Loligo vulgaris reynaudii: A black box approach. Bull Mar Sci 71(2):783–800Google Scholar
  71. Schneider SH (2001) What is ‘dangerous’ climate change? Nature 411:17–19PubMedCrossRefGoogle Scholar
  72. Segawa S (1990) Food consumption, food conversion and growth rates of the oval squid Sepioteuthis lessoniana by laboratory experiments. Nippon Suisan Gakkai Shi 56(2):217–222Google Scholar
  73. Segawa S (1995) Effect of temperature on oxygen consumption of juvenile oval squid Sepioteuthis lessoniana. Fish Sci 61(5):743–746Google Scholar
  74. Seibel BA, Fabry VJ (2003) Marine biotic response to elevated carbon dioxide. Adv Appl Biodivers Sci 4:59–67Google Scholar
  75. Seibel BA, Thuesen EV, Childress JJ, Gorodezky LA (1997) Decline in pelagic cephalopod metabolism with habitat depth reflects differences in locomotory efficiency. Biol Bull 192:262–278CrossRefGoogle Scholar
  76. Shaw PW, Pierce GJ, Boyle PR (1999) Subtle population structuring within a highly vagile marine invertebrate, the veined squid Loligo forbesi, demonstrated with microsatellite DNA markers. Mol Ecol 8:407–417CrossRefGoogle Scholar
  77. Sims D, Genner M, Southward A, Hawkins S (2001) Timing of squid migration reflects North Atlantic climate variability. Proc R Soc Lond B 268:2607–2611CrossRefGoogle Scholar
  78. Steer MA, Pecl GT, Moltschaniwskyj NA (2003a) Are bigger calamary Sepioteuthis australis hatchlings more likely to survive? A study based on statolith dimensions. Mar Ecol Prog Ser 261:175–182CrossRefGoogle Scholar
  79. Steer MA, Moltschaniwskyj NA, Jordan AR (2003b) Embryonic development of southern calamary (Sepioteuthis australis) within the constraints of an aggregated egg mass. Mar Freshw Res 54:217–226CrossRefGoogle Scholar
  80. Steer MA, Moltschaniwskyj NA Nichols DS, Miller M (2004) The role of temperature and maternal ration in embryo survival: using the dumpling squid Euprymna tasmanica as a model. J Exp Mar Biol Ecol 307:73–89CrossRefGoogle Scholar
  81. Triantafillos L (2004) Effects of genetic and environmental factors on growth of southern calamary, Sepioteuthis australis from southern Australia and northern New Zealand. Mar Freshw Res 55:439–446CrossRefGoogle Scholar
  82. Triantafillos L, Adams M (2001) Allozyme analysis reveals a complex population structure in the southern calamary, Sepioteuthis australis, from Australia and New Zealand. Mar Ecol Prog Ser 212:193–209CrossRefGoogle Scholar
  83. Veit R, McGowan J, Ainley D, Wahl T, Pyle P (1997) Apex marine predator declines ninety percent in association with changing oceanic climate. Global Change Biol 3(1):23–28CrossRefGoogle Scholar
  84. Vidal EAG, DiMarco FP, Wormorth JH, Lee PG (2002) Influence of temperature and food availability on survival, growth and yolk utilization in hatchling squid. Bull Mar Sci 71(2):915–931Google Scholar
  85. Villanueva R (2000) Effect of temperature on statolith growth of the European squid Loligo vulgaris during early life. Mar Biol 136:449–460CrossRefGoogle Scholar
  86. Visser ME, Both C (2005) Shifts in phenology due to global climate change: the need for a yardstick. Proc R Soc B 272:2561–2569PubMedCrossRefGoogle Scholar
  87. Walther GR, Post E, Convey P, Menzel A, Parmesan C, Nbeebee T, Fromentin JM, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395PubMedCrossRefGoogle Scholar
  88. Wells MJ, Clarke A (1996) Energetics: the costs of living and reproducing for an individual cephalopod. Phil Trans R Soc Lond B 351:1083–1104CrossRefGoogle Scholar
  89. Welch DW, Ishida Y, Nagasawa K (1998) Thermal limits and ocean migrations of sockeye salmon (Oncorhynchus nerka): long-term consequences of global warming. Can J Fish Aquat Sci 55:937–948CrossRefGoogle Scholar
  90. Yang WT, Hixon RF, Turk PE, Krejci ME, Hulet WH, Hanlon RT (1986) Growth, behaviour and sexual maturation of the market squid Loligo opalescens cultured throughout the life cycle. Fish Bull 84:771–798Google Scholar
  91. Yeatman J, Benzie JAH (1994) Genetic structure and distribution of Photololigo spp. in Australia. Mar Biol 118:79–87CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  1. 1.Tasmanian Aquaculture and Fisheries InstituteUniversity of TasmaniaHobartAustralia
  2. 2.Institute of Antarctic and Southern Ocean StudiesUniversity of TasmaniaHobartAustralia

Personalised recommendations