Skip to main content
Log in

Paralarvae of Octopus vulgaris Type II are stenohaline conformers: relationship to field distribution and dispersal

  • CEPHALOPOD ECOLOGY AND LIFE CYCLES
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

The degree of euryhalinity of cephalopod planktonic paralarvae potentially affects the dispersal capacity and distributional range of species. Herein, we tested the hypothesis that O. vulgaris Type II paralarvae would show some tolerance to seawater dilution, evaluated from integrated field and laboratory experiments. Paralarvae were collected from zooplankton samples (salinities of 30.3–32.6), in the Paraná Bay Estuarine Complex (PBEC), Southern Brazil. In the laboratory, they were exposed to salinities of 28, 30, 33, 35 (control), and 37, from 15 min to 24 h. Survival ranged from 60 to 83%, 73–100%, and 100% at salinity of 28, 30, and 33–37, respectively. Body fluid osmolality (BFO), body water content (BWC), and ninhydrin-positive substances (NPS, amino acids) were quantified at salinities of 33, 35, and 37 (with 100% survival). BFO was always isosmotic to the external medium. BWC and the high NPS concentration remained unchanged in all salinities. Thus, these paralarvae tolerate some deviation from seawater salinity, displaying osmoconforming behavior, maintain body hydration, and show high ability of tissue volume/water regulation in short periods of time. Presumably, this physiological capacity of paralarvae might be one factor allowing their dispersal and survival along environments with moderate deviations from seawater salinity.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Amado, E. M., C. A. Freire & M. M. Souza, 2006. Osmoregulation and tissue water regulation in the freshwater red crab Dilocarcinus pagei (Crustacea, Decapoda), and the effect of waterborne inorganic lead. Aquatic Toxicology 79(1): 1–8.

    Article  CAS  PubMed  Google Scholar 

  • Amado, E. M., L. R. Souza-Bastos, E. A. G. Vidal, T. S. Leite & C. A. Freire, 2015. Different abilities to regulate tissue hydration upon osmotic challenge in vitro, in the cephalopods Octopus vulgaris and O. insularis. Marine and Freshwater Behaviour and Physiology 48(3): 205–211.

    Article  CAS  Google Scholar 

  • Amor, M. D., M. D. Norman, A. Roura, T. S. Leite, I. G. Gleadall, A. Reid, C. Perales-Raya, C. C. Lu, J. C. Silvey, E. A. G. Vidal, F. Hochberg, X. Zheng & J. M. Strugnell, 2016. Morphological assessment of the Octopus vulgaris species complex evaluated in the light of molecular-based phylogenetic inferences. Zoologica Scripta 46(3): 275–288.

    Article  Google Scholar 

  • Cinti, A., P. J. Barón & A. L. Rivas, 2004. The effects of environmental factors on the embryonic survival of the Patagonian squid Loligo gahi. Journal of Experimental Marine Biology and Ecology 313: 225–240.

    Article  Google Scholar 

  • Chamberlin, M. E. & K. Strange, 1989. Anisosmotic cell volume regulation: a comparative view. American Journal of Physiology 257: C159–C173.

    Article  CAS  PubMed  Google Scholar 

  • Chapela, A., Á. F. González, E. G. Dawe, F. J. Rocha & Á. Guerra, 2006. Growth of common octopus (Octopus vulgaris) in cages suspended from rafts. Scientia Marina 70(1): 121–129.

    Article  Google Scholar 

  • Clark, M. E., 1968. Free amino acid levels in the coelomic fluid and body wall of polychaetes. The Biological Bulletin 134: 35–47.

    Article  Google Scholar 

  • D’Aniello, A., L. Strazzullo, G. D’Onofrio & M. Pischetola, 1986. Electrolytes and nitrogen compounds of body fluids and tissues of Octopus vulgaris Lam. Journal of Comparative Physiology B 156(4): 503–509.

    Article  Google Scholar 

  • D’Aniello, A., G. DʼOnofrio, M. Pischetola, et al., 1989. Effect of pH, salinity and Ca2+, Mg2+, K+ and SO4 2+ ions on hatching and viability of Loligo vulgaris embryo. Comparative Biochemistry and Physiology A 94: 477–481.

    Article  Google Scholar 

  • De Eguileor, M., M. G. Leonardi, A. Grimaldi, G. Tettamanti, L. Fiandra, B. Giordana, R. Valvassori & G. Lanzavecchia, 2000. Integumental amino acid uptake in a carnivorous predator mollusc (Sepia officinalis, Cephalopoda). Tissue and Cell 32(5): 389–398.

    Article  PubMed  Google Scholar 

  • Deaton, L. E., 2001. Hyperosmotic volume regulation in the gills of the ribbed mussel, Geukensia demissa: rapid accumulation of betaine and alanine. Journal of Experimental Marine Biology and Ecology 260: 185–197.

    Article  CAS  PubMed  Google Scholar 

  • Deaton, L., 2008. Osmotic and ionic regulation in molluscs. In Evans, D. H. (ed.), Osmotic and ionic regulation: cells and animals. CRC Press, New York.

    Google Scholar 

  • Delgado, M., J. I. Gairín, R. Carbó & C. Aguilera, 2010. Growth of Octopus vulgaris (Cuvier, 1797) in tanks in the Ebro Delta (NE Spain): effects of temperature, salinity and culture density. Scientia Marina 75(1): 53–59.

    Article  Google Scholar 

  • Evans, D. H., 2008. Osmotic and ionic regulation: cells and animals. CRC Press, New York.

    Book  Google Scholar 

  • Foster, C., E. M. Amado, M. M. Souza & C. A. Freire, 2010. Do osmoregulators have lower capacity of muscle water regulation than osmoconformers? A study on decapod crustaceans. Journal of Experimental Zoology A 313: 80–94.

    Google Scholar 

  • Fox, D. L., 1941. Changes in the tissue chloride of the California mussel in response to heterosmotic environments. The Biological Bulletin 80(1): 111–129.

    Article  CAS  Google Scholar 

  • Freire, C. A., E. M. Amado, L. R. Souza, M. P. T. Veiga, J. R. S. Vitule, M. M. Souza & V. Prodocimo, 2008. Muscle water control in crustaceans and fishes as a function of habitat, osmoregulatory capacity, and degree of euryhalinity. Comparative Biochemistry and Physiology A 149: 435–446.

    Article  Google Scholar 

  • Freire, C. A., L. R. Souza-Bastos, E. M. Amado, V. Prodocimo & M. M. Souza, 2013. Regulation of muscle hydration upon hypo-or hyper-osmotic shocks: differences related to Invasion of the freshwater habitat by decapod crustaceans. Journal of Experimental Zoology A 319: 297–309.

    Article  CAS  Google Scholar 

  • Gilles, R., 1987. Volume regulation in cells of euryhaline invertebrates. Current Topics in Membranes and Transport 30: 205–247.

    Article  CAS  Google Scholar 

  • González, A. F., J. Otero, A. Guerra, R. Prego, F. J. Rocha & M. Dale, 2005. Distribution of common octopus and common squid paralarvae in a wind-driven upwelling area (Ria of Vigo, Northwestern Spain). Journal of Plankton Research 27: 271–277.

    Article  Google Scholar 

  • Haimovici, M. & J. A. Perez, 1991. Coastal cephalopod fauna of southern Brazil. Bulletin of Marine Science 49(1–2): 221–230.

    Google Scholar 

  • Hendrix, J. P., W. H. Hulet & M. J. Greenberg, 1981. Salinity tolerance and the responses to hypoosmotic stress of the bay squid Lolliguncula brevis, a euryhaline cephalopod mollusc. Comparative Biochemistry and Physiology A 69(4): 641–648.

    Article  Google Scholar 

  • Hermosilla, C., F. Rocha & V. D. Valavanis, 2011. Assessing Octopus vulgaris distribution using presence-only model methods. Hydrobiologia 670(1): 35–47.

    Article  CAS  Google Scholar 

  • Hoyaux, J., R. Gilles & C. Jeuniaux, 1976. Osmoregulation in molluscs of the intertidal zone. Comparative Biochemistry and Physiology A 53: 361–365.

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hu, M. Y., Y. C. Tseng, M. Stumpp, M. A. Gutowska, R. Kiko, M. Lucassen & F. Melzner, 2011. Elevated seawater PCO2 differentially affects branchial acid-base transporters over the course of development in the cephalopod Sepia officinalis. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 300(5): R1100–R1114.

    Article  CAS  PubMed  Google Scholar 

  • Hu, M. Y., P. P. Hwang & Y. C. Tseng, 2015. Recent advances in understanding trans-epithelial acid-base regulation and excretion mechanisms in cephalopods. Tissue Barriers 3(4): e1064196.

    Article  PubMed  PubMed Central  Google Scholar 

  • Iglesias, P., P. Picón, M. Nande, M. J. Lago, J. J. Otero, V. Trujillo & J. Iglesias, 2016. Effect of low salinity on survival and ingested food of the common octopus, Octopus vulgaris Cuvier, 1797. Journal of Applied Aquaculture 28(3): 267–271.

    Article  Google Scholar 

  • Kinne, R. K., 1993. The role of organic osmolytes in osmoregulation: from bacteria to mammals. Journal of Experimental Zoology 265(4): 346–355.

    Article  CAS  PubMed  Google Scholar 

  • Kirschner, L. B., 1991. Water and Ions. In Prosser, C. L. (ed.), Environmental and Metabolic Animal Physiology. Comparative Animal Physiology. Wiley-Liss, New York: 13–107.

    Google Scholar 

  • Lang, F., 2007. Mechanisms and significance of cell volume regulation. Journal of the American College of Nutrition 26: 6135–6235.

    Article  Google Scholar 

  • Mazzini, F. S., 2013. Descrição hidrográfica e caracterização da dinâmica populacional de Octopus vulgaris no Complexo Estuarino de Paranaguá, Paraná. Universidade Federal do Paraná, Brasil. Dissertação de Mestrado em Sistemas Costeiros e Oceânicos: 58.

    Google Scholar 

  • Nabhitabhata, J., P. Asawangkune, S. Amornjaruchit & P. Promboon, 2001. Tolerance of eggs and hatchlings of neritic cephalopods to salinity changes. Phuket Marine Biological Center Special Publication 25(1): 91–99.

    Google Scholar 

  • Paulij, W. P., R. H. Bogaards & J. M. Denucé, 1990. Influence of salinity on embryonic development and the distribution of Sepia officinalis in the Delta Area (South Western part of The Netherlands). Marine Biology 107: 17–23.

    Article  Google Scholar 

  • Pechenik, J. A., 1999. On the advantages and disadvantages of larval stages in benthic marine invertebrate life cycles. Marine Ecology Progress Series 177: 269–297.

    Article  Google Scholar 

  • Péqueux, A., 1995. Osmotic regulation in crustaceans. Journal of Crustacean Biology 15: 1–60.

    Article  Google Scholar 

  • Perretti, C. T. & M. Sedarat, 2016. The influence of the El Niño Southern Oscillation on paralarval market squid (Doryteuthis opalescens). Fisheries Oceanography 25(5): 491–499.

    Article  Google Scholar 

  • Pierce, S. K., 1971. A source of solute for volume regulation in marine mussels. Comparative Biochemistry and Physiology A 38: 619–635.

    Article  CAS  Google Scholar 

  • Pierce, S. K., 1982. Invertebrate cell volume control mechanisms: a coordinated use of intracellular amino acids and inorganic ions as osmotic solute. The Biological Bulletin 163: 405–419.

    Article  CAS  Google Scholar 

  • Robertson, J. D., 1953. Further studies on ionic regulation in marine invertebrates. Journal of Experimental Biology 30(2): 277–296.

    CAS  Google Scholar 

  • Robertson, J. D., 1949. Ionic regulation in some marine invertebrates. Journal of Experimental Biology 26(2): 182–200.

    CAS  PubMed  Google Scholar 

  • Roura, A., A. X. Álvarez-Salgado, A. F. González, M. Gregori, G. Rosón, J. Otero & A. Guerra, 2016. Life strategies of cephalopod paralarvae in a coastal upwelling system (NW Iberian Peninsula): insights from zooplankton community and spatio-temporal analyses. Fisheries Oceanography 25: 241–258.

    Article  Google Scholar 

  • Sadok, S., R. F. Uglow & S. J. Haswell, 1997. Haemolymph and mantle fluid ammonia and ninhydrin positive substances variations in salinity-challenged mussels (Mytilus edulis L.). Journal of Experimental Marine Biology and Ecology 211(2): 195–212.

    Article  CAS  Google Scholar 

  • Sakamoto, T., S. Ogawa, Y. Nishiyama, C. Akada, H. Takahashi, T. Watanabe, H. Minakata & H. Sakamoto, 2015. Osmotic/ionic status of body fluids in the euryhaline cephalopod suggest possible parallel evolution of osmoregulation. Scientific Reports 5: 14469.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salvador, B. & J. G. F. Bersano, 2017. Zooplankton variability in the subtropical estuarine system of Paranaguá Bay, Brazil, in 2012 and 2013. Estuarine, Coastal and Shelf Science 199: 1–13. https://doi.org/10.1016/j.ecss.2017.09.019.

    Article  Google Scholar 

  • Santos, I. A., G. C. Castellano & C. A. Freire, 2013. Direct relationship between osmotic and ionic conforming behavior and tissue water regulatory capacity in echinoids. Comparative Biochemistry and Physiology A 164: 466–476.

    Article  CAS  Google Scholar 

  • Sen, H., 2004. A preliminary study on the effects of salinity on egg development of European squid (Loligo vulgaris Lamarck 1798). Israeli Journal of Aquaculture-Bamidgeh 56: 93–99.

    Google Scholar 

  • Shumway, S. E., P. A. Gabbott & A. Youngson, 1977. The effect of fluctuating salinity on the concentrations of free amino acids and ninhydrin-positive substances in the adductor muscles of eight species of bivalve molluscs. Journal of Experimental Marine Biology and Ecology 29: 131–150.

    Article  CAS  Google Scholar 

  • Valverde, J. C., S. Martínez-Llorens, A. T. Vidal, M. Jover, C. Rodríguez, J. Estefanell, J. I. Gairín, P. M. Domingues, C. J. Rodríguez & B. G. García, 2013. Amino acids composition and protein quality evaluation of marine species and meals for feed formulations in cephalopods. Aquaculture International 21(2): 413–433.

    Article  CAS  Google Scholar 

  • Veiga, M. P. T., S. M. Gutierre, G. C. Castellano & C. A. Freire, 2016. Tolerance of high and low salinity in the intertidal gastropod Stramonita brasiliensis (Muricidae): behaviour and maintenance of tissue water content. Journal of Molluscan Studies 82: 154–160.

    Google Scholar 

  • Verween, A., M. Vincx & S. Degraer, 2007. The effect of temperature and salinity on the survival of Mytilopsis leucophaeata larvae (Mollusca, Bivalvia): the search for environmental limits. Journal of Experimental Marine Biology and Ecology 348(1): 111–120.

    Article  Google Scholar 

  • Vidal, E. A. G. & S. V. Boletzky, 2014. Loligo vulgaris and Doryteuthis opalescens. In Iglesias, J., L. Fuentes & R. Villanueva (eds.), Cephalopod Culture. Springer, Netherlands: 271–313.

    Chapter  Google Scholar 

  • Vidal, E. A. G., L. Fuentes & L. B. Silva, 2010. Defining Octopus vulgaris populations: a comparative study of the morphology and chromatophore pattern of paralarvae from Northeastern and Southwestern Atlantic. Fisheries Research 106: 199–208.

    Article  Google Scholar 

  • Vidal, E. A. G., R. Villanueva, J. P. Andrade, I. G. Gleadall, J. Iglesias, N. Koueta, S. Segawa, B. Grasse, R. M. Franco-Santos, C. B. Albertin, C. Caamal-Monsreal, M. E. Chimal, E. Edsinger-Gonzales, P. Gallardo, C. Pabic, C. Pascual, K. Roumbedakis & J. Wood, 2014. Cephalopod culture: current status of main biological models and research priorities. In Vidal, E. A. G. (ed.), Advances in Marine Biology. Oxford Press, Oxford: 1–98.

    Google Scholar 

  • Villanueva, R., J. Riba, C. Ruız-Capillas, A. V. González & M. Baeta, 2004. Amino acid composition of early stages of cephalopods and effect of amino acid dietary treatments on Octopus vulgaris paralarvae. Aquaculture 242(1): 455–478.

    Article  CAS  Google Scholar 

  • Villanueva, R., E. A. G. Vidal, F. Á. Fernández-Álvarez & J. Nabhitabhata, 2016. Early mode of life and hatchling size in cephalopod molluscs: influence on the species distributional ranges. PLoS ONE 11(11): e0165334.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wehner, F., H. Olsen, H. Tinel, E. Kinne-Saffran & R. K. H. Kinne, 2003. Cell volume regulation: osmolytes, osmolyte transport, and signal transduction. Reviews of Physiology, Biochemistry and Pharmacology 148: 1–80.

    Article  CAS  PubMed  Google Scholar 

  • Willmer, P., G. Stone & I. Johnston, 2005. Environmental physiology of animals, 2nd ed. Blackwell Science, Oxford.

    Google Scholar 

  • Wright, D. A., E. M. Setzler-Hamilton, J. A. Magee, V. S. Kennedy & S. P. McIninch, 1996. Effect of salinity and temperature on survival and development of young zebra (Dreissena polymorpha) and quagga (Dreissena bugensis) mussels. Estuaries 19(3): 619–628.

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank the assistance of Ivan Gavioli, Lorena Nascimento, Mariana Aguirre, and Thiago Sachetto during the lower salinity experiments. This study was funded by the Brazilian National Research Council - CNPq (PhD fellowship grant awarded to GCC (# 141213/2013-2), and research grants awarded to CAF (# 306630/2011-7) and to EAGV (# 485653/2012-5 and 311183/2014-0). Authors also wish to thankfully acknowledge the substantial contributions made by the anonymous reviewers, as well as the Associate Editor handling this manuscript, Dr. Jörg Dutz.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Carolina Arruda Freire.

Additional information

Guest editors: Erica A. G. Vidal, Ian G. Gleadall & Natalie Moltschaniswskyi / Advances in Cephalopod Ecology and Life Cycles

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Castellano, G.C., da Veiga, M.P.T., Mazzini, F.S. et al. Paralarvae of Octopus vulgaris Type II are stenohaline conformers: relationship to field distribution and dispersal. Hydrobiologia 808, 71–82 (2018). https://doi.org/10.1007/s10750-017-3458-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-017-3458-y

Keywords

Navigation