Skip to main content

Advertisement

SpringerLink
Log in

Impact of ocean warming on the early ontogeny of cephalopods: a metabolic approach

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The impact of a realistic warming scenario on the metabolic physiology of early cephalopod (squid Loligo vulgaris and cuttlefish Sepia officinalis) life stages was investigated. During exposure to the warming conditions (19 °C for the western coast of Portugal in 2100), the increase in oxygen consumption rates throughout embryogenesis was much steeper in squid (28-fold increase) than in cuttlefish (11-fold increase). The elevated catabolic activity–accelerated oxygen depletion within egg capsules, which exacerbated metabolic suppression toward the end of embryogenesis. Squid late-stage embryos appear to be more impacted by warming via metabolic suppression than cuttlefish embryos. At all temperature scenarios, the transition from encapsulated embryos to planktonic paralarvae implied metabolic increments higher than 100 %. Contrary to the nektobenthic strategy of cuttlefish newborns, the planktonic squid paralarvae rely predominantly on pulsed jet locomotion that dramatically increases their energy requirements. In the future, hatchlings will require more food per unit body size and, thus, feeding intake success will be crucial, especially for squid with high metabolic rates and low levels of metabolic reserves.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aitken JP, O’Dor RK (2004) Respirometry and swimming dynamics of the Australian cuttlefish Sepia apama. Mar Freshw Behav Physiol 37:217–234

    Google Scholar 

  • Aitken JP, O’Dor RK, Jackson GD (2005) The secret life of the giant cuttlefish Sepia apama (Cephalopoda): behaviour and energetics in nature revealed through radio acoustic positioning and telemetry (RAPT). J Exp Mar Biol Ecol 320:77–91

    Google Scholar 

  • Bartol IK, Krueger PS, Stewart WJ, Thompsonn JT (2009) Pulsed jet dynamics of squid hatchlings at intermediate Reynolds numbers. J Exp Biol 212:1506–1518

    Google Scholar 

  • Boidron-Metairon IF (1995) Larval nutrition. In: Edward LMc (ed) Ecology of marine invertebrate larvae. CRC Press, Boca Raton, pp 223–248

    Google Scholar 

  • Boletzky SV (1994) Embryonic development of cephalopods at low temperatures. Antarct Sci 6(2):139–142

    Google Scholar 

  • Bouchaud O (1991) Energy consumption of the cuttlefish Sepia officinalis (Mollusca: Cephalopoda) during embryonic development, preliminary results. Bull Mar Sci 49(1–2):333–340

    Google Scholar 

  • Boyle P, Rodhouse P (2005) Cephalopods: ecology and fisheries. Blackwell Science, Oxford 452 pp

    Google Scholar 

  • Brante A (2006) An alternative mechanism to reduce intracapsular hypoxia in ovicapsules of Fusitriton oregonensis (Gastropoda). Mar Biol (Berl) 149:269–274

    Google Scholar 

  • Brante A, Fernández M, Viard F (2008) Effect of oxygen conditions on intracapsular development in two calyptraeidae species with different modes of larval development. Mar Ecol Prog Ser 368:197–207

    Google Scholar 

  • Byrne M (2011) Impact of ocean warming and ocean acidification on marine invertebrate life history stages: vulnerabilities and potential for persistence in a changing ocean. Ocean Mar Biol Annu Rev 49:1–42

    Google Scholar 

  • Cronin ER, Seymour RS (2000) Respiration of the eggs of the giant cuttlefish Sepia apama. Mar Biol 136:863–870

    Google Scholar 

  • De Wachter B, Wolf G, Richard A, Decleir W (1988) Regulation of respiration during juvenile development of Sepia officinalis (Mollusca: Cephalopoda). Mar Biol 97:365–371

    Google Scholar 

  • Denton EJ, Gilpin-Brown JB (1961a) The buoyancy of the cuttlefish, Sepia officinalis (L.). J Mar Biol Assess UK 41:319–342

    Google Scholar 

  • Denton EJ, Gilpin-Brown JB (1961b) The effect of light on the buoyancy of the cuttlefish. J Mar Biol Assess UK 41:343–350

    Google Scholar 

  • Fioroni P (1990) Our recent knowledge of the development of the cuttlefish (Sepia officinalis). Zool Anz 224:1–25

    Google Scholar 

  • Frederich M, Pörtner HO (2000) Oxygen limitation of thermal tolerance defined by cardiac and ventilatory performance in spider crab, Maja squinado. Am J Physiol 279:1531–1538

    Google Scholar 

  • Gutowska MA, Melzner F (2009) Abiotic conditions in cephalopod (Sepia officinalis) eggs: embryonic development at low pH and high pCO2. Mar Biol 156:515–519

    CAS  Google Scholar 

  • Hu MY, Sucré E, Charmantier-Daures M, Charmantier G, Lucassen M, Himmerkus N, Melzner F (2010) Localization of ion-regulatory epithelia in embryos and hatchlings of two cephalopods. Cell Tissue Res 339(3):571–583

    CAS  Google Scholar 

  • Hu MY, Yung-Che T, Stumpp M, Gutowska MA, Kiko R, Lucassen M, Melzner F (2011) Elevated seawater PCO2 differentially affects branchial acid-base transporters over the course of development in the cephalopod Sepia officinalis. Am J Physiol Regul Integr Comp Physiol 301:R1700–R1709

    CAS  Google Scholar 

  • Kamler E (1992) Early life history of fish: an energetic approach. Chapman and Hall, London

    Google Scholar 

  • Katersky RS, Carter CG (2007) High growth efficiency occurs over a wide temperature range for juvenile barramundi Lates calcarifer fed a balanced diet. Aquaculture 272:444–450

    Google Scholar 

  • Kurihara H (2008) Effects of CO2-driven ocean acidification on the early developmental stages of invertebrates. Mar Ecol Prog Ser 373:275–284

    CAS  Google Scholar 

  • Lemaire J (1971) Etude du développenaent embryonnaire de Sepia officinalis L., Thèse Doctorat 3 ème cycle. Université de Lille, France, p 70

    Google Scholar 

  • Mangold-Wirz K (1963) Biologie des céphalopods benthiguis et nectonigues de la mer catalane. Vie Millieu 13(Suppl):285

    Google Scholar 

  • Marvel MR, Fisher KC (1948) Developmental changes in the viability of squid embryos after subjection to cyanide. Biol Bull 94:45–54

    CAS  Google Scholar 

  • McMahon JJ, Summers WC (1971) Temperature effects on the development rate of squid (Loligo pealei) embryos. Biol Bull 141:561–567

    Google Scholar 

  • Moran AL, Woods HA (2007) Oxygen in egg masses: interactive effects of temperature, age, and egg-mass morphology on oxygen supply to embryos. J Exp Biol 210:722–731

    CAS  Google Scholar 

  • Moreno A, Pereira J, Cunha M (2005) Environmental influences on age and size at maturity of Loligo vulgaris. Aquat Living Resour 18:377–384

    Google Scholar 

  • Moreno A, dos Santos A, Piatkowski U, Santos AMP, Cabral H (2009) Distribution of cephalopod paralarvae in relation to the regional oceanography of the western Iberia. J Plankton Res 31:73–91

    Google Scholar 

  • Naef A (1928) Die cephalopoden. Fauna et Flora di Golfo del Napoli Monographia 35(2):186–194

    Google Scholar 

  • Nixon M, Mangold K (1998) The early life of Sepia officinalis, and the contract with that of Octopus vulgaris (Cephalopoda). J Zool Lond 245:407–421

    Google Scholar 

  • O’Dor RK, Webber DM (1986) The constraints on cephalopods: why squid aren’t fish. Can J Zool 64:1591–1605

    Google Scholar 

  • O’Dor RK, Webber DM (1991) Invertebrate athletes: trade—offs between transport efficiency and power density in cephalopod evolution. J Exp Biol 160:93–112

    Google Scholar 

  • O’Dor RK, Wells MJ (1987) Energy and nutrient flow. In: Boyle PR (ed) Cephalopod life cycles, comparative reviews, vol 2. Academic Press, London, pp 109–133

    Google Scholar 

  • Pechenick JA (1987) Environmental influences on larval survival and development. In: Giese AC et al (eds) Reproduction of marine invertebrates, vol IX. Blackwell Scientific Publications, New York, pp 551–608

    Google Scholar 

  • Pechenick JA, Eyster LS, Widdows J, Bayne BL (1990) The influence of food concentration and temperature on growth and morphological differentiation of blue mussel Mytilus edulis L. larvae. J Exp Mar Biol Ecol 136:47–64

    Google Scholar 

  • Pecl GT, Jackson GD (2008) The potential impacts of climate change on inshore squid: biology, ecology and fisheries. Rev Fish Biol Fish 18:373–385

    Google Scholar 

  • Pörtner HO (2001) Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwissenschaften 88:137–146

    Google Scholar 

  • Pörtner HO (2002) Environmental and functional limits to muscular exercise and body size in marine invertebrates athletes. Comp Biochem Physiol A 133:303–321

    Google Scholar 

  • Pörtner HO, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315:95–97

    Google Scholar 

  • Pörtner HO, Mark FC, Bock C (2004) Oxygen limited thermal tolerance in fish? Answers obtained by nuclear magnetic resonance techniques. Resp Physiol Neurobiol 141:243–260

    Google Scholar 

  • Pörtner HO, Langenbuch M, Michaelidis B (2005) Synergistic effects of increased CO2, temperature and hypoxia on marine animals. J Geophys Res 110:C09S10

    Google Scholar 

  • Relvas P, Barton ED, Dubert J, Oliveira PB, Peliz A, da Silva JCB, Santos AMP (2007) Physical oceanography of the western Iberia ecosystem: latest views and challenges. Prog Oceanogr 74:149–173

    Google Scholar 

  • Rosa R, Seibel BA (2008) Synergistic effects of climate-related variables suggest future physiological impairment in a top oceanic predator. Proc Natl Acad Sci USA 105:20776–20780

    CAS  Google Scholar 

  • Rosa R, Seibel BA (2010) Metabolic physiology of the Humboldt squid, Dosidicus gigas: implications for vertical migration in a pronounced oxygen minimum zone. Progr Oceanogr 86:72–80

    Google Scholar 

  • Rosa R, Dierssen HM, Gonzalez L, Seibel BA (2008) Large-scale diversity patterns of cephalopods in the Atlantic open ocean and deep-sea. Ecology 89:3449–3461

    Google Scholar 

  • Rosa R, Trueblood L, Seibel BA (2009) Ecophysiological influence on scaling of aerobic and anaerobic metabolism of pelagic Gonatid squids. Physiol Biochem Zool 82:19–429

    Google Scholar 

  • Rosa R, Pimentel MS, Boavida-Portugal J, Teixeira T, Trübenbach K, et al. (2012) Ocean warming enhances malformations, premature hatching, metabolic suppression and oxidative stress in the early life stages of a keystone squid. PLoS ONE 7(6): e38282. doi:10.1371/journal.pone.0038282

  • Santos FD, Forbes K, Moita R (2002) Climate change in Portugal scenarios. Impacts and adaptation measures-siam project. Gradiva, Lisbon

    Google Scholar 

  • Sasaki GC, Capuzzo JM, Biesiot P (1986) Nutritional and bioenergetic consideration in development of the American lobster Homarus americanus. Can J Fish Aquat Sci 43:2311–2319

    CAS  Google Scholar 

  • Seibel BA, Dymowska A, Rosenthal J (2007) Metabolic temperature compensation and coevolution of locomotory performance in pteropod molluscs. Integr Comp Biol 47:880–891

    Google Scholar 

  • Steer MA, Moltschaniwskyj NA, Jordan AR (2003) Embryonic development of southern calamari (Sepioteuthis australis) within the constraints of an aggregated egg mass. Mar Freshw Res 54:217–226

    Google Scholar 

  • Thorp JH, Covich AP (2001) Ecology and classification of North American freshwater invertebrates. Academic Press, San Diego, CA, pp 315–399

    Google Scholar 

  • Tian Y (2009) Interannual–interdecadal variations of spear squid Loligo bleekeri abundance in the southwestern Japan Sea during 1975–2006: impact of the trawl fishing and recommendations for management under the different climate regimes. Fish Res 100:78–85

    Google Scholar 

  • Wang T, Overgaard J (2007) The heartbreak of adapting to global warming. Science 315:49–50

    CAS  Google Scholar 

  • Ward P, Boletzky SV (1984) Shell implosion depth and implosion morphologies in three species of Sepia (Cephalopoda) from the Mediterranean Sea. J Mar Biol Assoc UK 64:955–966

    Google Scholar 

  • Webber DM, Aitken JP, O’Dor RK (2000) Costs of locomotion and vertic dynamics of cephalopods and fish. Physiol Biochem Zool 73:651–662

    CAS  Google Scholar 

  • Wells J, Hanlon RT, Lee PG, Dimarco FP (1988) Respiratory and cardiac performance in Lolliguncula brevis (Cephalopoda, Myopsida): the effects of activity, temperature and hypoxia. J Exp Biol 138:17–36

    Google Scholar 

  • Wolf G, Verheyen E, Vlaeminck A, Lemaire J, Decleir W (1985) Respiration of Sepia officinalis during embryonic and early juvenile life. Mar Biol 90:35–39

    Google Scholar 

  • Woods HA (1999) Egg-mass size and cell size: effects of temperature on oxygen distribution. Am Zool 39:244–252

    Google Scholar 

  • Woods HA, Hill RI (2004) Temperature-dependent oxygen limitation in insect eggs. J Exp Biol 207:2267–2276

    Google Scholar 

Download references

Acknowledgments

The Portuguese Foundation for Science and Technology (FCT) supported this study through project grants PTDC/BIA-BEC/103266/2008 and PTDC/MAR/0908066/2008 to R. Rosa.

Author information

Authors and Affiliations

  1. Laboratório Marítimo da Guia, Centro de Oceanografia, Faculdade de Ciências da Universidade de Lisboa, Av. Nossa Senhora do Cabo, 939, 2750-374, Cascais, Portugal

    Marta S. Pimentel, Katja Trübenbach, Filipa Faleiro, Joana Boavida-Portugal, Tiago Repolho & Rui Rosa

Authors
  1. Marta S. Pimentel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Katja Trübenbach
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Filipa Faleiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Joana Boavida-Portugal
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tiago Repolho
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rui Rosa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rui Rosa.

Additional information

Communicated by H. O. Pörtner.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pimentel, M.S., Trübenbach, K., Faleiro, F. et al. Impact of ocean warming on the early ontogeny of cephalopods: a metabolic approach. Mar Biol 159, 2051–2059 (2012). https://doi.org/10.1007/s00227-012-1991-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-012-1991-9

Keywords

Search

Navigation