Revista de Biología Tropical ISSN Impreso: 0034-7744 ISSN electrónico: 2215-2075

OAI: https://revistas.ucr.ac.cr/index.php/rbt/oai
Effect of temperature on morphology and reproduction of sea urchin, Arbacia dufresnii (Echinodermata: Echinoidea)
PDF (Español (España))
HTML (Español (España))

Keywords

echinoid; thermal experiment; gametogenesis; gonadal production; physiology.
equinoideos; experimento térmico; gametogénesis; producción gonadal; fisiología

How to Cite

Ancin, B.-L., Epherra, L., & Rubilar, T. (2021). Effect of temperature on morphology and reproduction of sea urchin, Arbacia dufresnii (Echinodermata: Echinoidea). Revista De Biología Tropical, 69(S1), S154–S170. https://doi.org/10.15517/rbt.v69iSuppl.1.46346

Abstract

Introduction: The increase in atmospheric CO2 values and the consequent warming of seawater constitute stressors for marine ecosystems, renovating interest in echinoid physiology. The echinoid Arbacia dufresnii is a widely studied species with a wide distribution in the North Patagonian gulfs. Objective: Evaluate the effect of seawater temperature on its morphology and reproduction. Methods: Individuals were exposed for 10 weeks (April-June 2016) to three temperature treatments (13 °C control, 15 °C and 17 °C) according to the current conditions of seawater and the expected values for the next century. At the end of the experiment, diameter and weight of the whole individual and of its internal organs were statistically and histologically analyzed. Results: Individuals exposed to higher temperatures died in greater numbers. The control, and the 17 °C treatment, had no changes in dry gonad and intestine weights. However, the 15 °C group had wider diameter of test and a higher dry weight of gonads and intestine. At this temperature, the gonadal stages for males were similar to the environment, but females had more advanced stages. Conclusions: Temperature of 15°C could be optimal for assimilating food and obtaining energy. Gonads and intestine would be showing changes in the short term, unlike the calcified organs (test and Aristotle’s lantern).

https://doi.org/10.15517/rbt.v69iSuppl.1.46346
PDF (Español (España))
HTML (Español (España))

References

Avnimelech, Y. (2006). Bio-filters: the need for a new comprehensive approach. Aquacultural Engineering, 34(3), 172-178.

Azad, A.K., Pearce, C.M. & McKinley, R.S. (2011). Effects of diet and temperature on ingestion, absorption, assimilation, gonad yield, and gonad quality of the purple sea urchin (Strongylocentrotus purpuratus). Aquaculture, 317(1), 187-196.

Bates, W.R. (2005). Environmental factors affecting reproduction and development in ascidians and other protochordates. Canadian Journal of Zoology, 83(1), 51-61.

Bernasconi, I. (1953). Monografía de los Equinoideos argentinos. Anales del Museo de Historia Natural, 6(2), 1-58.

Bishop, C. & Watts, S. (1992). Biochemical and morphometric study of growth in the stomach and intestine of the echinoid Lytechinus variegatus (Echinodermata). Marine Biology, 114(3), 459-467.

Böttger, S.A. & McClintock, J.B. (2009). The effects of chronic inorganic and organic phosphate exposure on bactericidal activity of the coelomic fluid of the sea urchin Lytechinus variegatus (Lamarck) (Echinodermata: Echinoidea). Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 150(1), 39-44.

Böttger, S., McClintock, J. & Klinger, T. (2001). Effects of inorganic and organic phosphates on feeding, feeding absorption, nutrient allocation, growth and righting responses of the sea urchin Lytechinus variegatus. Marine Biology, 138(4), 741-751.

Brierley, A.S. & Kingsford, M.J. (2009). Impacts of climate change on marine organisms and ecosystems. Current Biology, 19(14), 602-614.

Brogger, M., Martinez, M. & Penchaszadeh, P. (2010). Reproduction of the sea urchin Arbacia dufresnii (Echinoidea: Arbaciidae) from Golfo Nuevo, Argentina. Journal of the Marine Biological Association of the United Kingdom, 90(7), 1405-1409.

Brogger, M., Gil, D.G., Rubilar, T., Martínez, M.I., Díaz de Vivar, M.E., Escolar, M., . . . Tablado, A. (2013). Echinoderms from Argentina: Biodiversity, distribution and current state of knowledge. In J.J. Alvarado & F.A. Solís-Marin (Eds.), Echinoderm Research and Diversity in Latin America (pp. 359-402). Berlín: Springer Heidelberg.

Byrne, M. (2010). Impact of climate change stressors on marine invertebrate life histories with a focus on the Mollusca and Echinodermata. In J. Yu & A. Henderson (Eds.), Climate Alert: Climate Change Monitoring and Strategy (pp. 142-185). Sydney: University of Sydney Press.

Byrne, M., Andrew, N., Worthington, D. & Brett, P. (1998). Reproduction in the diadematoid sea urchin Centrostephanus rodgersii in contrasting habitats along the coast of New South Wales, Australia. Marine Biology, 132(2), 305-318.

Byrne, M., Prowse, T.A.A., Sewell, M.A., Dworjanyn, S.A., Williamson, J.E. & Vaitilington, D. (2008) Maternal provisioning for larvae and larval provisioning for juveniles in the toxopneustid sea urchin Tripneustes gratilla. Marine Biology; 55, 473-482.

Byrne, M., Ho, M., Selvakumaraswamy, P., Nguyen, H.D., Dworjanyn, S.A. & Davis, A.R. (2009). Temperature, but not pH, compromises sea urchin fertilization and early development under near-future climate change scenarios. Proceedings of the Royal Society of London B: Biological Sciences, 276(1663), 1883-1888.

Byrne, M. & Przeslawski, R. (2013). Multistressor impacts of warming and acidification of the ocean on marine invertebrate life histories. Integrative and Comparative Biology, 53(4), 582-596.

Clemente, S., Lorenzo-Morales, J., Mendoza, J., López, C., Sangil, C., Alves, F., . . . Hernández, J. (2014). Sea urchin Diadema africanum mass mortality in the subtropical eastern Atlantic: role of waterborne bacteria in a warming ocean. Marine Ecology Progress Series, 506, 1-14.

Cohen-Rengifo, M., García, E., Hernández, C.A., Hernández, J.C. & Clemente, S. (2013). Global warming and ocean acidification affect fertilization and early development of the sea urchin Paracentrotus lividus. Cahiers de Biologie Marine, 54, 667-675.

Delorme, N.J. & Sewell, M.A. (2016). Effects of warm acclimation on physiology and gonad development in the sea urchin Evechinus chloroticus. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 198, 33-40.

Dellatorre, F.G., Pisoni, J.P., Barón, P.J. & Rivas, A.L. (2012). Tide and wind forced nearshore dynamics in Nuevo Gulf (Northern Patagonia, Argentina): Potential implications for cross-shore transport. Journal of Marine Systems, 96, 82-89.

Dupont, S. & Thorndyke, M. (2009). Impact of CO2-driven ocean acidification on invertebrate early life-history-What we know, what we need to know and what we can do. Biogeosciences Discussions, 6(2), 3109-3131.

Ebert, T., Hernandez, J. & Russell, M. (2011). Problems of the gonad index and what can be done: analysis of the purple sea urchin Strongylocentrotus purpuratus. Marine Biology, 158(1), 47-58.

Edwards, M. & Richardson, A.J. (2004). Impact of climate change on marine pelagic phenology and trophic mismatch. Nature, 430(7002), 881.

Epherra, L. (2010). Ciclo bioquímico del erizo verde en costas del Golfo Nuevo, Patagonia. (Tesis de licenciatura). Universidad Nacional de la Patagonia San Juan Bosco, Argentina.

Epherra, L. (2016). Evaluación del impacto de invertebrados herbívoros nativos sobre el alga invasora Undaria pinnatifida: Arbacia dufresnii (Echinodermata: Echinoidea) como modelo de estudio. (Tesis de doctorado). Universidad Nacional de Mar del Plata, Argentina.

Epherra, L., Gil, D.G., Rubilar, T., Pérez-Gallo, S., Reartes, M.B. & Tolosano, J.A. (2015). Temporal and spatial differences in the reproductive biology of the sea urchin Arbacia dufresnii. Marine and Freshwater Research, 66(4), 329-342.

Fenaux, L., Malara, G., Cellario, C., Charra, R. & Palazzoli, I. (1977). Evolution des constituants biochimiques des principaux compartiments de l’oursin Arbacia lixula (L.) au cours d’un cycle sexuel et effets d’un jeûne de courte durée au cours de la maturation sexuelle. Journal of Experimental Marine Biology and Ecology, 28(1), 17-30.

Fernández, J., Chaar, F., Epherra, L., González-Aravena, J.M. & Rubilar, T. (2021). Embryonic and larval development is conditioned by sea water temperature and maternal origin in the sea urchin Arbacia dufresnii (Echinodermata: Echinoidea). Revista Biología Tropical.

González, R.A., Díaz, F., Licea, A., Re, A.D., Sánchez, L.N. & García-Esquivel, Z. (2010). Thermal preference, tolerance and oxygen consumption of adult white shrimp Litopenaeus vannamei (Boone) exposed to different acclimation temperatures. Journal of Thermal Biology, 35(5), 218-224.

Gooding, R.A., Harley, C.D. & Tang, E. (2009). Elevated water temperature and carbon dioxide concentration increase the growth of a keystone echinoderm. Proceedings of the National Academy of Sciences, 106(23), 9316-9321.

Gouda, H. & Agatsuma, Y. (2020). Effect of high temperature on gametogenesis of the sea urchin Strongylocentrotus intermedius in the Sea of Japan, northern Hokkaido, Japan. Journal of Experimental Marine Biology and Ecology, 525, 151324.

Harianto, J., Nguyen, H.D., Holmes, S.P. & Byrne, M. (2018). The effect of warming on mortality, metabolic rate, heat-shock protein response and gonad growth in thermally acclimated sea urchins (Heliocidaris erythrogramma). Marine Biology, 165(6), 96.

Harrold, C. & Pearse, J.S. (1987). The ecological role of echinoderms in kelp forests. Echinoderm studies, 2, 137-233.

Hendler, G. (2013). Recent mass mortality of Strongylocentrotus purpuratus (Echinodermata: Echinoidea) at Malibu and a review of purple sea urchin kills elsewhere in California. Bulletin, Southern California Academy of Sciences, 112(1), 19-37.

Hernández, M., Bückle, F., Guisado, C., Barón, B. & Estavillo, N. (2004). Critical thermal maximum and osmotic pressure of the red sea urchin Strongylocentrotus franciscanus acclimated at different temperatures. Journal of Thermal Biology, 29(4-5), 231-236.

Hochachka, P. & Somero, G. (2002). Biochemical adaptation, mechanism and process in physiological evolution. New York, USA: Oxford University Press.

Holland, N.D. (2013). Digestive system Developments in Aquaculture and Fisheries Science (Vol. 38). Ciudad, País: Elsevier.

Hughes, A.D., Kelly, M.S., Barnes, D.K., Catarino, A.I. & Black, K.D. (2006). The dual functions of sea urchin gonads are reflected in the temporal variations of their biochemistry. Marine Biology, 148(4), 789-798.

IPCC. (2013). Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. T.F. Stocker et al. (Eds.). United Kingdom, New York USA: Cambridge University Press.

IPCC. (2014). Climate change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the fifth assessment report of the Intergovernmental Panel on Climate Change. R.K. Pachauri & L.A. Meyer (Eds.). Geneva, Switzerland: IPCC.

James, P., Siikavuopio, S. & Mortensen, A. (2015). Sea urchin aquaculture in Norway. In N.P Brown, S.D. (Eds.), Echinoderm Aquaculture (pp. 147-173). New York, USA: Wiley.

Johnstone, J., Nash, S., Hernandez, E. & Rahman, M.S. (2019). Effects of elevated temperature on gonadal functions, cellular apoptosis, and oxidative stress in Atlantic sea urchin Arbacia punculata. Marine Environmental Research, 149, 40-49.

Kemp, J. & Britz, P. (2008). The effect of temperature on the growth, survival and food consumption of the east coast rock lobster Panulirus homarus rubellus. Aquaculture, 280(1), 227-231.

Kino, S. (2010). Reproduction and early life history of sea urchins, Arbacia dufresnei and Pseudechinus magellanicus, in Chiloé Island and Reloncaví Sound, Chile. Aquaculture Science, 58(1), 65-73.

Kurihara, H. & Shirayama, Y. (2004). Effects of increased atmospheric CO2 on sea urchin early development. Marine Ecology Progress Series, 274, 161-169.

Lawrence, A.J. & Soame, J.M. (2004). The effects of climate change on the reproduction of coastal invertebrates. Ibis, 146, 29-39.

Lawrence, J.M. & Ellwood, A. (1991). Simultaneous allocation of resources to arm regeneration and to somatic and gonadal production in Luidia clathrata (Say) (Echinodermata: Asteroidea). In T. Yanagisawa, T., I. Yasumasu, C. Oguro, N. Suzuki & T. Motokawa, (Eds), Biology of Echinodermata (pp. 543-548). Netherlands: Balkema.

Lawrence, J.M., Lawrence, A. & Giese, A. (1966). Role of the gut as a nutrient-storage organ in the purple sea urchin (Strongylocentrotus purpuratus). Physiological Zoology, 39(4), 281-290.

Lawrence, J.M., Cao, X., Chang, Y., Wang, P., Yu, Y., Lawrence, A.L. & Watts, S.A. (2009). Temperature effect on feed consumption, absorption, and assimilation efficiencies and production of the sea urchin Strongylocentrotus intermedius. Journal of Shellfish Research, 28(2), 389-395.

Lawrence, J.M., Lawrence, A.L. & Watts, S.A. (2013). Feeding, Digestion and Digestibility of Sea Urchins. In J.M: Lawrence (Ed), Sea Urchins: Biology and Ecology (pp. 135-150). Amsterdam: Elsevier Science.

Lessios, H., Cubit, J., Robertson, D., Shulman, M., Parker, M., Garrity, S. & Levings, S. (1984). Mass mortality of Diadema antillarum on the Caribbean coast of Panama. Coral Reefs, 3(4), 173-182.

McCullagh, P. (1984). Generalized linear models. European Journal of Operational Research, 16(3), 285-292.

McElroy, D., Nguyen, H. & Byrne, M. (2012). Respiratory response of the intertidal seastar Parvulastra exigua to contemporary and near-future pulses of warming and hypercapnia. Journal of Experimental Marine Biology and Ecology, 416, 1-7.

McGaw, I.J., Clifford, A.M. & Goss, G.G. (2015). Physiological responses of the intertidal starfish Pisaster ochraceus, (Brandt, 1835) to emersion at different temperatures. Journal of Experimental Marine Biology and Ecology, 468, 83-90.

Olive, P. (1995). Annual breeding cycles in marine invertebrates and environmental temperature: probing the proximate and ultimate causes of reproductive synchrony. Journal of Thermal Biology, 20(1-2), 79-90.

Paine, R.T. (1966). Food web complexity and species diversity. The American Naturalist, 100(910), 65-75.

Parra, M., Rubilar, T., Latorre, M., Epherra, L., Gil, D.G. & Díaz de Vivar, M.E. (2015). Nutrient allocation in the gonads of the sea urchin Arbacia dufresnii in different stages of gonadal development. Invertebrate Reproduction & Development, 59(1), 26-36.

Pérez, A.F., Gil, D.G. & Rubilar, T. (2014). Echinodermata. In J.A. Calcagno (Ed.), Los invertebrados Marinos (pp. 295-316). Buenos Aires, Argentina: Vazquez Mazzini.

Pisoni, J., Dellatorre, F. & Rivas, A. (2017). Temperatura del mar en la estación oceanográfica muelle Luis Piedrabuena durante el periodo 2011-2016. Argentina: Centro Nacional Patagónico. Informe técnico.

Przeslawski, R., Ahyong, S., Byrne, M., Woerheide, G. & Hutchings, P. (2008). Beyond corals and fish: the effects of climate change on noncoral benthic invertebrates of tropical reefs. Global Change Biology, 14(12), 2773-2795.

R Core Team. (2014). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Retrieved from

Rubilar, T. & Crespi-Abril, A. (2017). Does Echinoderm research deserve an ethical consideration? Revista de Biología Tropical, 65(1), 11-22.

Rubilar, T., Epherra, L., Deias-Spreng, J., Díaz de Vivar, M.E., Avaro, M., Lawrence, A. & Lawrence, J. (2016). Ingestion, absorption and assimilation efficiencies, and production in the sea urchin Arbacia dufresnii fed a formulated feed. Journal of Shellfish Research, 35, 1083-1093.

Russell, M.P. (1998). Resource allocation plasticity in sea urchins: rapid, diet induced, phenotypic changes in the green sea urchin, Strongylocentrotus droebachiensis (Müller). Journal of Experimental Marine Biology and Ecology, 220(1), 1-14.

Sanford, E. (2002). Water temperature, predation, and the neglected role of physiological rate effects in rocky intertidal communities. Integrative and Comparative Biology, 42(4), 881-891.

Santos, P.M., Albano, P., Raposo, A., Ferreira, S.M., Costa, J.L. & Pombo, A. (2020). The effect of temperature on somatic and gonadal development of the sea urchin Paracentrotus lividus (Lamarck, 1816). Aquaculture, 528, 735487.

Sastre-Perelló, M. (2018). Influencia de la temperatura en la ecología de los herbívoros invertebrados dominantes del litoral mediterráneo (Paracentrotus lividus y Arbacia lixula) (Tesis de maestría). Universitat de les Illes Balears, España.

Scheibling, R. & Hatcher, B. (2007). Ecology of Strongylocentrotus droebachiensis. In J.M Lawrence (Ed.), Developments in Aquaculture and Fisheries Science (Vol. 37, pp. 353-392). Amsterdam: Elsevier Science BV.

Siikavuopio, S.I. (2009). Green sea urchin (Strongylocentrotus droebachiensis, Müller) in aquaculture: the effects of environmental factors on gonad growth. (Doctoral dissertation). University of Tromsø. Norway.

Siikavuopio, S.I., Christiansen, J.S. & Dale, T. (2006). Effects of temperature and season on gonad growth and feed intake in the green sea urchin (Strongylocentrotus droebachiensis). Aquaculture, 255(1-4), 389-394.

Siikavuopio, S.I., Mortensen, A. & Christiansen, J.S. (2008). Effects of body weight and temperature on feed intake, gonad growth and oxygen consumption in green sea urchin, Strongylocentrotus droebachiensis. Aquaculture, 281(1), 77-82.

Siikavuopio, S.I., James, P., Lysne, H., Sæther, B.S., Samuelsen, T.A. & Mortensen, A. (2012). Effects of size and temperature on growth and feed conversion of juvenile green sea urchin (Strongylocentrotus droebachiensis). Aquaculture, 354, 27-30.

Uthicke, S., Liddy, M., Nguyen, H. & Byrne, M. (2014). Interactive effects of near-future temperature increase and ocean acidification on physiology and gonad development in adult Pacific sea urchin, Echinometra sp. Coral Reefs, 33(3), 831-845.

Walker, C.W. (1982). Nutrition of gametes. In M. Jangoux & J.M: Lawrence (Eds), Echinoderm nutrition (pp. 449-468). Netherlands: Balkema.

Walker, C.W., Lesser, M. & Unuma, T. (2013). Sea urchin gametogenesis–structural, functional and molecular/genomic biology. In J.M: Lawrence (Ed), Sea Urchins: Biology and Ecology (pp. 25-43). Amsterdam: Elsevier Science.

Wangensteen, O.S., Turon, X., Casso, M. & Palacín, C. (2013). The reproductive cycle of the sea urchin Arbacia lixula in northwest Mediterranean: potential influence of temperature and photoperiod. Marine Biology, 160(12), 3157-3168.

Watts, S.A., Hofer, S.C., Desmond, R.A., Lawrence, A.L. & Lawrence, J.M. (2011). The effect of temperature on feeding and growth characteristics of the sea urchin Lytechinus variegatus fed a formulated feed. Journal of Experimental Marine Biology and Ecology, 397(2), 188-195.

White, P.A., Kalff, J., Rasmussen, J.B. & Gasol, J.M. (1991). The effect of temperature and algal biomass on bacterial production and specific growth rate in freshwater and marine habitats. Microbial ecology, 21(1), 99-118.

Wilson, I. & Gamble, M. (2002). The hematoxylins and eosin. In J. Bancroft & M. Gamble (Eds.), Theory and practice of histological techniques (pp. 125-138). London, United Kingdom: Elsevier.

Zamora, L.N. & Jeffs, A.G. (2012). Feeding, metabolism and growth in response to temperature in juveniles of the Australasian sea cucumber, Australostichopus mollis. Aquaculture, 358, 92-97.

Zárate, E.V., Díaz de Vivar, M.E., Avaro, M.G., Epherra, L. & Sewell, M.A. (2016). Sex and reproductive cycle affect lipid and fatty acid profiles of gonads of Arbacia dufresnii (Echinodermata: Echinoidea). Marine Ecology Progress Series, 551, 185-199.

Zhao, C., Zhang, L., Qi, S., Shi, D., Yin, D. & Chang, Y. (2018). Multilevel effects of long-term elevated temperature on fitness related traits of the sea urchin Strongylocentrotus intermedius. Bulletin of Marine Science, 94(4), 1483-1497.

Comments

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

Downloads

Download data is not yet available.