Journal of Comparative Physiology B

, Volume 184, Issue 1, pp 55–64 | Cite as

Developmental and physiological challenges of octopus (Octopus vulgaris) early life stages under ocean warming

  • Tiago Repolho
  • Miguel Baptista
  • Marta S. Pimentel
  • Gisela Dionísio
  • Katja Trübenbach
  • Vanessa M. Lopes
  • Ana Rita Lopes
  • Ricardo Calado
  • Mário Diniz
  • Rui RosaEmail author
Original Paper


The ability to understand and predict the effects of ocean warming (under realistic scenarios) on marine biota is of paramount importance, especially at the most vulnerable early life stages. Here we investigated the impact of predicted environmental warming (+3 °C) on the development, metabolism, heat shock response and antioxidant defense mechanisms of the early stages of the common octopus, Octopus vulgaris. As expected, warming shortened embryonic developmental time by 13 days, from 38 days at 18 °C to 25 days at 21 °C. Concomitantly, survival decreased significantly (~29.9 %). Size at hatching varied inversely with temperature, and the percentage of smaller premature paralarvae increased drastically, from 0 % at 18 °C to 17.8 % at 21 °C. The metabolic costs of the transition from an encapsulated embryo to a free planktonic form increased significantly with warming, and HSP70 concentrations and glutathione S-transferase activity levels were significantly magnified from late embryonic to paralarval stages. Yet, despite the presence of effective antioxidant defense mechanisms, ocean warming led to an augmentation of malondialdehyde levels (an indicative of enhanced ROS action), a process considered to be one of the most frequent cellular injury mechanisms. Thus, the present study provides clues about how the magnitude and rate of ocean warming will challenge the buffering capacities of octopus embryos and hatchlings’ physiology. The prediction and understanding of the biochemical and physiological responses to warmer temperatures (under realistic scenarios) is crucial for the management of highly commercial and ecologically important species, such as O. vulgaris.


Global warming Cephalopods Octopus Early life stages Metabolism Heat shock response Lipid peroxidation 



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.

Supplementary material

360_2013_783_MOESM1_ESM.doc (46 kb)
Supplementary material 1 (DOC 45 kb)


  1. Agarraberes FA, Dice JF (2001) Protein translocation across membranes. Biochim Biophys Acta 1513:1–24PubMedCrossRefGoogle Scholar
  2. Anestis A, Lazou A, Pörtner HO, Michaelidis B (2007) Behavioural, metabolic and molecular stress responses of the marine bivalve Mytilus galloprovincialis during long-term acclimation at increasing ambient temperature. Am J Physiol Reg Integr Comp Physiol 293:R911–R921CrossRefGoogle Scholar
  3. Atkinson D, Sibly RM (1997) Why are organisms usually bigger in colder environments? Making sense of a life history puzzle. Trend Ecol Evol 12:235–239CrossRefGoogle Scholar
  4. Bartol IK, Krueger PS, Stewart WJ, Thompson JT (2009) Pulsed jet dynamics of squid hatchlings at intermediate Reynolds numbers. J Exp Biol 212:1506–1518PubMedCrossRefGoogle Scholar
  5. Boletzky SV (1974) Elevage de Céphalopodes en aquarium. Vie Milieu 24:309–340Google Scholar
  6. Boletzky SV (1987) Embryonic phase. In: Boyle PR (ed) Cephalopod life cycles. Academic Press, London, pp 5–31Google Scholar
  7. Bouchaud O (1991) Energy consumption of the cuttlefish Sepia officinalis (mollusca: cephalopoda) during embryonic development, preliminary results. Bull Mar Sci 49:333–340Google Scholar
  8. Boyle P, Rodhouse PG (2005) Cephalopods. Ecology and fisheries. Blackwell Publishing, OxfordGoogle Scholar
  9. Buckley BA, Gracey AY, Somero GN (2006) The cellular response to heat stress in the goby Gillichthys mirabilis: a cDNA microarray and protein-level analysis. J Exp Biol 209:2660–2677PubMedCrossRefGoogle Scholar
  10. 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 Ann Rev 49:1–42Google Scholar
  11. Calado R, Vitorino A, Dionísio G, Dinis MT (2007) A recirculated maturation system for marine ornamental decapods. Aquaculture 263:68–74CrossRefGoogle Scholar
  12. 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
  13. Cronin ER, Seymour RS (2000) Respiration of the eggs of the giant cuttlefish Sepia apama. Mar Biol 136:863–870CrossRefGoogle Scholar
  14. Fink AL (1999) Chaperone-mediated protein folding. Phys Rev 79:425–449Google Scholar
  15. Forsythe JW (1993) A working hypothesis of how seasonal temperature change may impact the field growth of young cephalopods. In: Okutami T, O’Dor RK, Kubodera T (eds) Recent advances in cephalopod fisheries biology. Japan Tokai University Press, Tokyo, pp 133–143Google Scholar
  16. Forsythe JW, Van Heukelem WF (1987) Growth. In: PR B (ed) Cephalopod life cycles, vol II: comparative reviews. UK Academic Press, London, pp 135–156Google Scholar
  17. Frydman J (2001) Folding of newly translated proteins in vivo: the role of molecular chaperones. Annu Rev Biochem 70:603–647PubMedCrossRefGoogle Scholar
  18. Garrido C, Gurbuxani S, Ravagnan L, Kroemer G (2001) Heat shock proteins: endogenous modulators of apoptotic cell death. Biochem Biophys Res Comm 286:433–442PubMedCrossRefGoogle Scholar
  19. Gething MJ (1997) Guidebook to molecular chaperones and protein-folding catalysts. Oxford University Press, New YorkGoogle Scholar
  20. Gutowska MA, Melzner F (2009) Abiotic conditions in cephalopod (Sepia officinalis) eggs: embryonic development at low pH and high pCO2. Mar Biol 156:515–519CrossRefGoogle Scholar
  21. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139PubMedGoogle Scholar
  22. Halliwell B, Gutteridge JMC (1989) Free radicals in biology and medicine. Clarendon Press, OxfordGoogle Scholar
  23. Hartl FU (1996) Molecular proteins in cellular protein folding. Nature 381:571–580PubMedCrossRefGoogle Scholar
  24. Hofmann GE, Somero GN (1996) Protein ubiquitination and stress protein synthesis in Mytilus trossulus occurs during recovery from tidal emersion. Mol Mar Biol Biotech 5:175–184Google Scholar
  25. Kamler E (2008) Resource allocation in yolk-feeding fish. Rev Fish Biol Fisheries 18:143–200CrossRefGoogle Scholar
  26. Kurihara H (2008) Effects of CO2-driven ocean acidification on the early development stages of invertebrates. Mar Ecol-Prog Ser 373:275–284CrossRefGoogle Scholar
  27. Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68:253–278PubMedCrossRefGoogle Scholar
  28. Mangold K, Boletsky SV (1973) New data on reproductive biology and growth of Octopus vulgaris. Mar Biol 19:7–12CrossRefGoogle Scholar
  29. McMahon JJ, Summers WC (1971) Temperature effects on the developmental rate of squid (Loligo pealei) embryos. Biol Bull 141:561–567CrossRefGoogle Scholar
  30. Melzner F, Bock C, Pörtner HO (2006) Temperature-dependent oxygen extraction from the ventilatory current and the costs of ventilation in the cephalopod Sepia officinalis. J Comp Physiol B 176:607–621PubMedCrossRefGoogle Scholar
  31. 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 31:73–91CrossRefGoogle Scholar
  32. Naef A (1928) Fauna and Flora of the Bay of Napoles: Cephalopoda embryology. Part I vol II Monographia. Zoological Station, NapolesGoogle Scholar
  33. Njemini R, Demanet C, Mets T (2005) Comparison of two ELISAs for the determination of Hsp70 in serum. J Immunol Method 306:176–182CrossRefGoogle Scholar
  34. O’Dor RK (1998) Can understanding squid life-history strategies and recruitment improve management? S Afr J Mar Sci 20:193–206Google Scholar
  35. Oliveira UO, Araújo ASR, Belló-Klein A, da Silva RSM, Kucharski LC (2005) Effects of environmental anoxia and different periods of reoxygenation on oxidative balance in gills of the estuarine crab Chasmagnathus granulata. Comp Biochem Physiol B 140:51–57PubMedCrossRefGoogle Scholar
  36. Oosthuizen A, Roberts MJ, Sauer WHH (2002) Temperature effects on the embryonic development and hatching of the squid, Loligo vulgaris reynaudii. Bull Mar Sci 71:619–632Google Scholar
  37. Osovitz CJ, Hofmann GE (2005) Thermal history-dependent expression of the hsp70 gene in purple sea urchins: biogeographic patterns and the effect of temperature acclimation. J Exp Mar Biol Ecol 327:134–143CrossRefGoogle Scholar
  38. Parra G, Villanueva R, Yúfera M (2000) Respiration rates in late eggs and early hatchlings of common octopus, Octopus vulgaris. J Mar Biol Ass UK 80:557–558CrossRefGoogle Scholar
  39. Pimentel MS, Trübenbach K, Faleiro F, Boavida-Portugal J, Repolho T, Rosa R (2012) Impact of ocean warming on the early ontogeny of cephalopods: a metabolic approach. Mar Biol 159:2051–2059CrossRefGoogle Scholar
  40. Pörtner HO (2002) Climate change and temperature dependent biogeography: systemic to molecular hierarchies of thermal tolerance in animals. Comp Biochem Physiol A 132:739–761CrossRefGoogle Scholar
  41. Pörtner HO, Farrell AP (2008) Physiology and climate change. Science 322:690–691PubMedCrossRefGoogle Scholar
  42. Prosser CL, Heath JE (1994) Environment and metabolic animal physiology. Wiley-Liss, New YorkGoogle Scholar
  43. 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 74:149–173CrossRefGoogle Scholar
  44. Roberts M, Sauer WHH (1994) Environment: the key to understanding the South African chokka squid (Loligo vulgaris reynaudii) life cycle and fishery? Antarct Sci 6:249–258CrossRefGoogle Scholar
  45. Rodhouse PG, Nigmatullin CM (1996) Role as consumers. Philos Roy Soc B 351:1003–1022CrossRefGoogle Scholar
  46. Rosa R, Seibel BA (2008) Synergistic effects of climate-related variables suggest future physiological impairment in a top oceanic predator. Proc Nat Acad Sci USA 105:20776–20780PubMedCrossRefGoogle Scholar
  47. Rosa R, Gonzalez L, Dierssen HM, Seibel BA (2012a) Environmental determinants of latitudinal-size trends in cephalopod mollusks. Mar Ecol Prog Ser 464:153–165Google Scholar
  48. Rosa R, Pimentel M, Boavida-Portugal J, Teixeira T, Trübenbach K, Diniz MS (2012b) Ocean warming enhances malformations, premature hatching, metabolic suppression and oxidative stress in the early life stages of a keystone invertebrate. PLoS ONE 7:e38282PubMedCentralPubMedCrossRefGoogle Scholar
  49. Rosa R, Graham P, O′Dor R (2013a) Advances in squid biology, ecology and fisheries, vol I. Myopsid squids. Nova Publishers, New York, in pressGoogle Scholar
  50. Rosa R, Graham P, O′Dor R (2013b) Advances in squid biology, ecology and fisheries, vol II. Oegopsid squids. Nova Publishers, New York, in pressGoogle Scholar
  51. Rosa R, Trübenbach K, Repolho T, Pimentel M, Faleiro F, Boavida-Portugal J, Baptista M, Dionísio G, Leal M, Calado R, Pörtner HO (2013c) Lower hypoxia thresholds of cuttlefish life stages living in a warm acidified ocean. Proc R Soc B 280:20131695PubMedCrossRefGoogle Scholar
  52. Sakurai Y, Bower JR, Nakamura Y, Yamamoto S, Watanabe K (1996) Effect of temperature on development and survival of Todarodes pacificus embryos and paralarvae. Am Malacol Bull 13:89–95Google Scholar
  53. Santos MB, Clarke MR, Pierce GJ (2001) Assessing the importance of cephalopods in the diets of marine mammals and other top predators: problems and solutions. Fish Res 52:121–139CrossRefGoogle Scholar
  54. Seibel BA (2007) On the depth and scale of metabolic rate variation: scaling of oxygen consumption rates and enzymatic activity in the Class Cephalopoda (Mollusca). J Exp Biol 210:1–11PubMedCrossRefGoogle Scholar
  55. Seibel BA, Rosa R, Trueblood L (2007) Cephalopod metabolism as a function of body size. In: Olson RJ, Young JW (eds) The role of squid in open ocean ecosystems. Global ocean ecosystem dynamics—climate impacts on oceanic top predators. GLOBEC Report 24, pp 9–10Google Scholar
  56. Şen H (2003) Kalamar (Loligo vulgaris Lamarck, 1798) yumurtalarının embriyonik gelişimi ve inkübasyonu. Izmir, TürkiyeGoogle Scholar
  57. Şen H (2004) A preliminary study on the effects of salinity on egg development of European squid (Loligo vulgaris Lamarck, 1798). Israeli J Aquacult Bamidgeh 56:95–101Google Scholar
  58. Şen H (2005) Temperature tolerance of loliginid squid (Loligo vulgaris Lamarck, 1798) eggs in controlled conditions. Turkish J Fish Aquat Sci 5:53–59Google Scholar
  59. Somero GN (2005) Linking biogeography to physiology: evolutionary and acclimatory adjustments of thermal limits. Front Zool 2:1–9PubMedCentralPubMedCrossRefGoogle Scholar
  60. Stadtman ER (1992) Protein oxidation and aging. Science 257:1220–1226PubMedCrossRefGoogle Scholar
  61. Tucker JWJ (1998) Marine fish culture. Kluwer Academic Publishers, MassachusettsCrossRefGoogle Scholar
  62. Turner RL, Lawrence JM (1979) Volume and composition of echinoderm eggs: implications for the use of egg size in life-history models. In: Stancyk SE (ed) Reproductive ecology of marine invertebrates. University of South Carolina Press, Columbia, pp 25–40Google Scholar
  63. Uchiyama M, Mihara M (1978) Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem 86:271–278PubMedCrossRefGoogle Scholar
  64. Vecchione M (1991) Observations on the paralarval ecology of a euryhaline squid, Lolliguncula brevis (Cephalopoda: Loliginidae). Fish Bull (US) 89:515–521Google Scholar
  65. Vidal EAG, DiMarco FP, Wormuth JH, Lee PG (2002) Influence of temperature and food availability on survival, growth and yolk utilization in hatchling squid. Bull Mar Sci 71:915–931Google Scholar
  66. Villanueva R (2000) Effect of temperature on statolith grow of the European squid Loligo vulgaris during early life. Mar Biol 136:449–460CrossRefGoogle Scholar
  67. Villanueva R, Nozais C, Boletzky SV (1995) The planktonic life of octopuses. Nature 377:107. doi: 10.1038/377107a0 CrossRefGoogle Scholar
  68. Villanueva R, Arkhipkin A, Jereb P, Lefkaditou E, Lipinski MR, Perales-Raya C, Riba J, Rocha F (2003) Embryonic life of the loliginid squid Loligo vulgaris: comparison between statoliths of Atlantic and Mediterranean populations. Mar Ecol Prog Ser 253:197–208CrossRefGoogle Scholar
  69. Wachter BD, Wolf G, Richard A, Decleir W (1988) Regulation of respiration during juvenile development of Sepia officinalis (Mollusca: Cephalopoda). Mar Biol 97:365–371CrossRefGoogle Scholar
  70. Waluda CM, Rodhouse PG, Trahan PN (2001) Surface oceanography of the inferred hatching grounds of Illex argentinus (Cephalopoda: Ommastrephidae) and influences on recruitment variability. Mar Biol 139:671–679CrossRefGoogle Scholar
  71. Wolf G, Verheyen E, Vlaeminck A, Lemaire J, Decleir W (1985) Respiration of Sepia officinalis during embryonic and early juvenile life. Mar Biol 90:35–39CrossRefGoogle Scholar
  72. Wood JB, O’Dor RK (2000) Do larger cephalopods live longer? Effects of temperature and phylogeny on interspecific comparisons of age and size at maturity. Mar Biol 136:91–99CrossRefGoogle Scholar
  73. Worms J (1983) Loligo vulgaris. In: Boyle PR (ed) Cephalopod life cycles. Academic Press, London, pp 143–157Google Scholar
  74. Zielinski S, Pörtner HO (2000) Oxidative stress and antioxidative defense in cephalopods: a function of metabolic rate or age? Comp Biochem Physiol B 125:147–160PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Tiago Repolho
    • 1
  • Miguel Baptista
    • 1
  • Marta S. Pimentel
    • 1
  • Gisela Dionísio
    • 1
    • 2
  • Katja Trübenbach
    • 1
  • Vanessa M. Lopes
    • 1
  • Ana Rita Lopes
    • 1
  • Ricardo Calado
    • 2
  • Mário Diniz
    • 3
  • Rui Rosa
    • 1
    Email author
  1. 1.Laboratório Marítimo da Guia, Centro de OceanografiaFaculdade de Ciências da Universidade de LisboaCascaisPortugal
  2. 2.Departamento de Biologia, CESAMUniversidade de AveiroAveiroPortugal
  3. 3.Faculdade de Ciências e TecnologiaUniversidade Nova de LisboaCaparicaPortugal

Personalised recommendations