Differential reproductive investment in females of Lithodes santolla (DecapodaAnomura) from different regions of southern South America

  1. Díaz-Arce, Natalia 1
  2. Di Salvatore, Pablo 2
  3. Gowland-Sainz, María F. 2
  4. Lovrich, Gustavo A. 2
  1. 1 Research Centre for Experimental Marine Biology & Biotechnology (PIE-UPV/EHU), Universidad del País Vasco/Euskal Herriko Unibertsitatea - AZTI, Marine Research Division - Centro Austral de Investigaciones Científicas (CADIC), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)
  2. 2 Centro Austral de Investigaciones Científicas (CADIC), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)
Aldizkaria:
Scientia Marina

ISSN: 0214-8358

Argitalpen urtea: 2019

Alea: 83

Zenbakia: 4

Orrialdeak: 327-336

Mota: Artikulua

DOI: 10.3989/SCIMAR.04974.31A DIALNET GOOGLE SCHOLAR lock_openSarbide irekia editor

Beste argitalpen batzuk: Scientia Marina

Garapen Iraunkorreko Helburuak

Laburpena

The southern king crab Lithodes santolla experiences low temperatures and unpredictable food conditions, and is under variable fishing pressure. To compare the reproductive investment of females, crabs were captured from three sites (Beagle Channel 55°S, Tierra del Fuego Atlantic coast 52-54°S and San Jorge Gulf 45-47°S). Fecundity, water and lipid contents were measured in midgut gland, ovary and muscle. To assess the maternal investment in the offspring, egg masses were analysed on lipid, protein, water and inorganic matter contents, egg volume and embryo size. Although fecundity was similar among sites, San Jorge Gulf females showed higher water and lower lipid contents in somatic and reproductive organs. The egg mass energy reserves varied among sites, showing the highest lipid values in the Beagle Channel, and the highest protein and inorganic matter content in San Jorge Gulf. Though water content was similar, egg volume and embryo size were higher in San Jorge Gulf. Moreover, maternal size did not correlate with egg volume, embryo size or lipid, protein and inorganic matter content of the eggs. This study suggests that reproductive investment of L. santolla varies among regions exposed to different environmental conditions, such as the quality of food available, denoting a female compensatory mechanism.

Finantzaketari buruzko informazioa

We are indebted to the captain and crew of the RV Puerto Deseado for access to the samples in Tierra del Fuego and San Jorge Gulf and to M. Pérez and L. Pagnossin for their help in sampling in the Beagle Channel. O. Florentín assisted in the laboratory work, and C.P. Fraysse provided suggestions to improve this manuscript. We wish to thank J.M. Txurruka (EHU/ UPV) for technical assistance and lending laboratory facilities for the chemical analysis of protein contents. We thank the two anonymous reviewers for their contributions to improve this paper. This study was funded by the Argentine State through grants from FONCyT PICTs 12-0554 and 16-0142. N. Díaz-Arce was supported by the FiDEX scholarship granted by the Bordeaux University to do her MSc thesis at CADIC. P. Di Salvatore has a postdoctoral fellowship from the Argentine CONICET.

Erreferentzia bibliografikoak

  • Allen R.M., Buckley Y.M., Marshall D.J. 2007. Offspring size plasticity in response to intraspecific competition: an adaptive maternal effect across life-history stages. Am. Nat. 171: 225-237.
  • Ansell A.D. 1974. Seasonal changes in biochemical composition of the bivalve Chlamys septemradiata from the Clyde Sea area. Mar. Biol. 25: 85-99.
  • Babu D.E. 1987. Observations on the embryonic development and energy source in the crab Xantho bidentatus. Mar. Biol. 95: 123-127.
  • Balzi P. 1999. Los hábitos alimenticios de la centolla, Lithodes santolla (Molina) del golfo San Jorge. Natur. Patag. Cs. Biol. 5: 67-87.
  • Balzi P. 2005. Ecología y biología de la reproducción de la centolla Lithodes santolla del golfo San Jorge. Universidad Nacional de la Patagonia “San Juan Bosco”, 150 pp.
  • Bas C.C., Spivak E.D., Anger K. 2007. Seasonal and interpopulational variability in fecundity, egg size, and elemental composition (CHN) of eggs and larvae in a grapsoid crab, Chasmagnathus granulatus. Helgol. Mar. Res. 61: 225.
  • Beninger P.G., Lucas A. 1984. Seasonal variations in condition, reproductive activity, and gross biochemical composition of two species of adult clam reared in a common habitat: Tapes decussatus L. (Jeffreys) and Tapes philippinarum (Adams and Reeve). J. Exp. Mar. Biol. Ecol. 79: 19-37.
  • Bligh E.G., Dyer W.J. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Phys. 37: 911-917.
  • Comoglio L., Amin O. 1996. Natural diet of the southern king crab Lithodes santolla in the Beagle Channel, Tierra del Fuego, Argentina. Biol. Pesq. 25: 51-57.
  • Chang E.S., O’Connor J.D. 1983. Metabolism and transport of carbohydrates and lipids. In: Mantel L.H., Bliss D.E. (eds), The biology of Crustacea. Academic Press, New York, pp. 263-287.
  • Cho C.Y., Slinger S.J., Bayley H.S. 1982. Bioenergetics of salmonid fishes: energy intake, expenditure and productivity. Comp. Biochem. Physiol. Part B 73: 25-41.
  • Dall W. 1975. Indices of nutritional state in the western rock lobster, Panulirus longipes (Milne Edwards). II. Gastric fluid constituents. J. Exp. Mar. Biol. Ecol. 18: 1-18.
  • Di Salvatore P., Gowland-Sainz M., Florentin O., et al. 2019. Effects of fishery practices on fecundity of two lithodid crab species of commercial interest in Southern South America. Fish. Res. 211: 275-281.
  • Firpo C., Wyngaard J., Mauna C., et al. 2017. Estructura poblacional y condición reproductiva de las hembras de centolla (Lithodes santolla) en el sector patagónico central, temporada de pesca 2015-16. Inf. Téc. INIDEP 21: 16.
  • Firpo C., Mauna C., Mango V., et al. 2018. Resultados de la campaña de investigación de centolla (Lithodes santolla) en el área III, al sur del paralelo 48ºS. Inf. Téc. INIDEP 20: 14.
  • Fischer S., Thatje S., Brey T. 2009. Early egg traits in Cancer setosus (Decapoda, Brachyura): effects of temperature and female size. Mar. Ecol. Prog. Ser. 377: 193-202.
  • Folch J., Lees M., Sloane Stanley G. 1957. A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226: 497-509.
  • Góngora M.E., González-Zevallos D., Pettovello A., et al. 2012. Caracterización de las principales pesquerías del golfo San Jorge Patagonia, Argentina. Lat. Am. J. Aquat. Res. 40: 1-11.
  • Gowland-Sainz M.F. 2018. Biología de la reproducción en la centolla Lithodes santolla del Canal Beagle: apareamiento y limitación espermática. PhD thesis, Universidad de Buenos Aires.
  • Gowland-Sainz M.F., Tapella F., Lovrich G.A. 2015. Egg loss in females of two lithodid species following different return-to-the-water protocols. Fish. Res. 161: 77-85.
  • Hadfield M., Strathmann M. 1996. Variability, flexibility and plasticity in life histories of marine invertebrates. Oceanol. Acta 19: 323-334.
  • Hall S., Thatje S. 2009. Global bottlenecks in the distribution of marine Crustacea: temperature constraints in the family Lithodidae. J. Biogeogr. 36: 2125-2135.
  • Hall S., Thatje S. 2011. Temperature-driven biogeography of the deep-sea family Lithodidae (Crustacea: Decapoda: Anomura) in the Southern Ocean. Polar Biol. 34: 363-370.
  • Hamasaki K., Fukunaga K., Maruyama K. 2003. Egg development and incubation period of the swimming crab Portunus trituberculatus (Decapoda: Portunidae) reared in the laboratory. Crust. Res. 32: 45-54.
  • Hjelset A.M., Nilssen E.M., Sundet J.H. 2012. Reduced size composition and fecundity related to fishery and invasion history in the introduced red king crab (Paralithodes camtschaticus) in Norwegian waters. Fish. Res. 121: 73-80.
  • Kattner G., Graeve M., Calcagno J.A., et al. 2003. Lipid, fatty acid and protein utilization during lecithotrophic larval development of Lithodes santolla (Molina) and Paralomis granulosa (Jacquinot). J. Exp. Mar. Biol. Ecol. 292: 61-74.
  • Lovrich G.A., Tapella F. 2014. Southern king crabs. In: Stevens B. (ed), King crabs of the world: biology and fisheries management. CRC Press, Boca Raton, pp. 449-484.
  • Lovrich G.A., Vinuesa J. 1993. Reproductive biology of the false southern king crab (Paralomis granulosa, Lithodidae) in the Beagle Channel, Argentina. Fish. Bull. 91: 664-675.
  • Lovrich G.A., Vinuesa J.H. 1999. Reproductive potential of the lithodids Lithodes santolla and Paralomis granulosa in the Beagle Channel, Argentina. Sci. Mar. 63 (Suppl. 1): 355-360.
  • Lovrich G.A., Thatje S., Calcagno J.A., et al. 2003. Changes in biomass and chemical composition during lecithotrophic larval development of the southern king crab, Lithodes santolla (Molina). J. Exp. Mar. Biol. Ecol. 288: 65-79.
  • Lowry O.H., Rosebrough N.J., Farr A.L., et al. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193: 265-275.
  • Mauna C., Firpo C.A., Mango V., et al. 2017. Campaña de Investigación de centolla (Lithodes santolla), Área III, 2016. INIDEP Inf. Camp. 16/17.
  • Mayrand E., Dutil J.-D., Guderley H. 2000. Changes in muscle of postmoult snow crabs Chionoecetes opilio (O. Fabricius) fed different rations. J. Exp. Mar. Biol. Ecol. 243: 95-113.
  • Militelli M.I., Firpo C., Rodrigues K.A., et al. 2019. Egg production and validation of clutch fullness indices scale of southern king crab, Lithodes santolla, in the Central Patagonian Sector, Argentina (44°-48°S). Fish. Res. 211: 40-45.
  • Moore L.E., Smith D.M., Loneragan N.R. 2000. Blood refractive index and whole-body lipid content as indicators of nutritional condition for penaeid prawns (Decapoda: Penaeidae). J. Exp. Mar. Biol. Ecol. 244: 131-143.
  • Moran A.L., McAlister J.S. 2009. Egg size as a life history character of marine invertebrates: Is it all it’s cracked up to be? Biol. Bull. 216: 226-242.
  • Pérez-Barros P., Tapella F., Romero M.C., et al. 2004. Benthic decapod crustaceans associated to captures of Munida spp. (Decapoda: Anomura) in the Beagle Channel, Argentina. Sci. Mar. 68: 237-246.
  • Pérez-Barros P., Confalonieri V.A., Paschke K., et al. 2015. Incongruence between molecular and morphological characters in the southern king crabs Lithodes santolla and Lithodes confundens (Decapoda: Anomura). Polar Biol. 38: 2097-2107.
  • Phillips F., Privett O.S. 1979. A simplified procedure for the quantitative extraction of lipids from brain tissue. Lipids 14: 590-595.
  • Picklo M.J. 2016. Farmed Fish: A Valuable Source of Lipid Based Nutrients. In: Raatz S.K., Bibus D.M. (eds), Fish and Fish Oil in Health and Disease Prevention. Academic Press, San Diego, pp. 161-167.
  • Racotta I.S., Palacios E., Ibarra A.M. 2003. Shrimp larval quality in relation to broodstock condition. Aquaculture 227: 107-130.
  • Ramirez Llodra E. 2002. Fecundity and life-history strategies in marine invertebrates. Adv. Mar. Biol. 43: 87-170.
  • Ricklefs R.E., Wikelski M. 2002. The physiology/life-history nexus. Trends. Ecol. Evol. 17: 462-468.
  • Ruxton G.D., Houston D.C. 2004. Energetic feasibility of an obligate marine scavenger. Mar. Ecol. Prog. Ser. 266: 59-63.
  • Shakuntala K., Reddy S.R. 1982. Crustacean egg size as an indicator of egg fat/protein reserves. Int. J. Invertebr. Reprod. 4: 381-384.
  • Siikavuopio S.I., Johansson G.S., James P., et al. 2019. Effect of starvation on the survival, injury, and weight of adult snow crab, Chionoecetes opilio. Aquacult. Res. 50: 550-556.
  • Spaargaren D.H., Haefner Jr P.A. 1994. Interactions of ovary and hepatopancreas during the reproductive cycle of Crangon crangon (L.). II. Biochemical relationships. J. Crustac. Biol. 14: 6-19.
  • Stancyk S.E. 1981. Reproductive Ecology of Marine Invertebrates. Univ. South Carolina, Columbia, 284 pp.
  • Stevens B.G., Lovrich G.A. 2014. King crabs of the world: species and distributions. In: Stevens B.G. (ed.) King crabs of the world: Biology and fisheries management. CRC Press, Boca Raton, Florida, pp. 1-30.
  • Stevens B.G., Swiney K.M., Buck L. 2008. Thermal effects on embryonic development and hatching for blue king crab Paralithodes platypus (Brandt, 1850) held in the laboratory, and a method for predicting dates of hatching. J. Shellfish. Res. 27: 1255-1263.
  • Swanepoel H., Lues J.F.R., Venter P. 2016. The contribution of fatty acids to the composition of the total lipids in juvenile Cape hake fillets. J. New Generation Sci. 14: 247-258.
  • Swiney K.M., Long W.C., Eckert G.L., et al. 2012. Red King Crab, Paralithodes camtschaticus, size-fecundity relationship, and interannual and seasonal variability in fecundity. J. Shellfish Res. 31: 925-933.
  • Swiney K.M., Eckert G.L., Kruse G.H. 2013. Does Maternal Size Affect Red King Crab, Paralithodes amtschaticus, Embryo and Larval Quality? J. Crustac. Biol. 33: 470-480.
  • Thatje S., Bacardit R. 2000. Morphological variability in larval stages of Nauticaris magellanica (A. Milne Edwards, 1891) (Decapoda: Caridea: Hippolytidae) from South American waters. Bull. Mar. Sci. 66: 375-398.
  • Thatje S., Schnack-Schiel S., Arntz W.E. 2003. Developmental trade-offs in Subantarctic meroplankton communities and the enigma of low decapod diversity in high southern latitudes. Mar. Ecol. Prog. Ser. 260: 195-207.
  • Thorson G. 1950. Reproductive and larval ecology of marine bottom invertebrates. Biol. Rev. 25: 1-45.
  • Urzúa Á., Paschke K., Gebauer P., et al. 2012. Seasonal and interannual variations in size, biomass and chemical composition of the eggs of North Sea shrimp, Crangon crangon (Decapoda: Caridea). Mar. Biol. 159: 583-599.
  • Varisco M., Colombo J., Di Salvatore P., et al. 2019. Fisheries-related variations in the fecundity of the southern king crab in Patagonia. Fish. Res. 218: 105-111.
  • Vinuesa J.H. 1985. Differential aspects of the southern king crab (Lithodes antarcticus) in two latitudinally separated locations. In: Melteff B. (ed), Proceedings of the International King Crab Symposium. Alaska Sea Grant Report 85-12, University of Alaska, Fairbanks, AK, pp. 267-279.
  • Vinuesa J. 1987. Embryonary development of Lithodes antarcticus Jacquinot (Crustacea, Decapoda, Lithodidae) developmental stages, growth and mortality. Physis 45: 21-29.
  • Vinuesa J.H. 2005. Distribución de crustáceos decápodos y estomatópodos del golfo San Jorge, Argentina. Rev. Biol. Mar. Oceanogr. 40: 7-21.
  • Vinuesa J.H., Labal de Vinuesa M.L. 1998. La gametogénesis de la centolla, Lithodes santolla (Molina, 1782) (Crustacea, Decapoda, Lithodidae). Nat. Pat. 6: 35-49.
  • Webb J.B., Eckert G.L., Shirley T.C., et al. 2007. Changes in embryonic development and hatching in Chionoecetes opilio (snow crab) with variation in incubation temperature. Biol. Bull. 213: 67-75.
  • Wyngaard J.G., Iorio M., Firpo C. 2016. La pesquería de centolla (Lithodes santolla) en la Argentina. In: Boschi E. (ed.), El Mar Argentino y sus recursos pesqueros, 6. INIDEP, pp. 229-250.