Elsevier

Marine Environmental Research

Volume 92, December 2013, Pages 95-101
Marine Environmental Research

The impact of rising sea temperature on innate immune parameters in the tropical subtidal sea urchin Lytechinus variegatus and the intertidal sea urchin Echinometra lucunter

https://doi.org/10.1016/j.marenvres.2013.09.005Get rights and content

Highlights

  • Two species of tropical echinoids were exposed to different temperatures and periods.

  • Tropical echinoids were exposed to 20, 25 and 30 °C for 24 h, 2, 7 and 14 days.

  • Immunological response was compromised in Lytechinus variegatus but not in Echinometra lucunter.

  • Two coelomocytes types were described as heat stress markers for L. variegatus.

  • E. lucunter showed to be more adapted to elevated temperatures.

Abstract

Ocean temperatures are rising throughout the world, making it necessary to evaluate the impact of these temperature changes on sea urchins, which are well-known bioindicators. This study evaluated the effect of an increase in temperature on the immune response of the subtidal Lytechinus variegatus and the intertidal Echinometra lucunter sea urchins. Both species were exposed to 20 (control), 25 and 30 °C temperatures for 24 h, 2, 7 and 14 days. Counting of coelomocytes and assays on the phagocytic response, adhesion and spreading of coelomocytes were performed. Red and colorless sphere cells were considered biomarkers for heat stress. Moreover, a significant decrease in the phagocytic indices and a decrease in both cell adhesion and cell spreading were observed at 25 and 30 °C for L. variegatus. For E. lucunter, the only alteration observed was for the cell proportions. This report shows how different species of sea urchins respond immunologically to rising temperatures.

Introduction

Studies on temperature started with Fourier (1827), who first described the Earth's temperature. Arrhenius (1896) was the first to speculate about whether variations in the atmospheric concentration of carbon dioxide have contributed to long-term variations in climate.

Despite the large amount of publications concerning the theme of global warming, articles that emphasize the effects of climatic changes on marine ecosystems account for less than 5% of these publications. The oceans cover 71% of the Earth and absorb approximately a third of all carbon dioxide produced by human activities; thus, they have enormous importance for the regulation of the planet's climate (Rahmstorf et al., 2007). There is clear evidence that ocean temperatures have been increasing over the years (Trenberth, 2010).

Temperature plays a central and vital role on the biological processes of all organisms. It impacts the rate of enzymatic reactions, membrane transport and substance diffusion. A moderate increase in temperature can provoke alterations to the metabolic rate of an organism, resulting in fundamental changes in biological processes, such as growth and reproduction. Previous studies reported that temperature influences sea urchin fertilization and early development (Rupp, 1973, Sewell and Young, 1999, Tyler et al., 2000, Byrne et al., 2009); larval survival (Roller and Stickle, 1993) and feeding, digestion and absorption (Klinger et al., 1986).

Marine ecosystems have a fundamental ecological role for the planet, and the impacts caused by human activities seem to cause irreversible alterations on its ecology. Such impacts include decreases in ocean productivity, changes to the marine food chain, reduction of the number of marine species and increases in diseases in the marine environment (Hoegh-Guldberg and Bruno, 2010).

For this reason, investigations into the effect of increasing sea water temperature on the innate immune system of a marine model would be extremely useful for better understanding the mechanisms by which global warming operate on a particular animal class.

Sea urchins are benthonic animals with limited moving capacity, as demonstrated by Pearse (2006); thus, environmental changes impact them greatly, and for this reason, Kobayashi and Okamura (2004) classified them as excellent bioindicators. Furthermore, sea urchins have a phylogenetic position that approaches chordates, justifying their use in innate immune studies (Litman et al., 2005, Hibino et al., 2006, Silva, 2013).

The literature has described four types of coelomocytes for sea urchins: phagocytic amoebocytes, vibratile cells, red sphere cells and white sphere cells (Johnson, 1971, Bertheussen and Seljelid, 1978, Mangiaterra and Silva, 2001). Phagocytic amoebocytes (PA) are used as a tool to evaluate the innate immune response in sea urchins exposed to biotic and abiotic factors (Borges et al., 2002).

Tropical species present wider thermal tolerance windows when compared to temperate and polar species (Pötner, 2002). Nevertheless, thermal tolerance windows differ between species depending on the range of the environmental temperature. Lytechinus variegatus tolerate a field temperature up to 35 °C briefly (Beddingfield, 1997). Higher temperatures can cause mass mortality episodes in this species (Meyer and Birkeland, 1974 and Rivera, 1978 reviewed in Watts et al., 2013). By contrast, Echinometra lucunter is an intertidal species that was classified by Hendler et al. (1995) as a species that highly tolerates wide oscillations in temperatures. Understanding how both species respond immunologically to thermal stress will improve the understanding of thermal tolerance in these tropical echinoid species.

The aim of this study was to evaluate the effect of sea water increase in temperature on the innate immune system of two different tropical sea urchin species: the subtidal L. variegatus and the intertidal E. lucunter.

Section snippets

Animal collection and maintenance

Tropical sea urchins of the species L. variegatus (n = 65) and E. lucunter (n = 65) (males and females) were collected from sites near the Marine Biology Center of University of Sao Paulo (CEBIMar-USP), northern coast of Sao Paulo State (23°49.530′S, 045°26.394′W), by autonomous diving at depths of 3–6 m during the winter of 2009. The sampling and all experiments were in accordance with Brazilian legislation and were approved by IBAMA (License number: Sisbio 27922-1).

Sea urchins were kept in a

Results

The coelomocytes differential counting showed a significant increase in colorless sphere cells (CSC) (P < 0.05) in L. variegatus exposed to 25 °C for two days when compared to the control group at the same period; the same was observed after seven days of exposure. Additionally, an increase of red sphere cells (RSC) was observed after acute and chronic exposure, with a very significant increase under 25 °C after two days (P < 0.01), seven and 14 days (P < 0.05). The same was observed under

Discussion

Our results mainly indicate that two distinct tropical species respond differently to rising sea temperature. L. variegatus seemed to be more susceptible to thermal stress, presenting alterations in cell counting, innate immune parameters and coelomocyte adhesion and spreading. However, the species E. lucunter presented changes only in cell counting at some exposure periods and temperatures and did not show changes in any of the other parameters measured. These differences between the two

Conclusion

The present work demonstrated how rising sea temperature influences the innate immune response in two species of tropical sea urchins. L. variegatus presented alterations in cell counting, innate immune parameters and coelomocyte adhesion and spreading. However, the species E. lucunter presented only alterations in cell counting after some periods of exposure to different temperatures. Such differences can be explained by the particular habitats of these species. More studies on the molecular

Acknowledgments

The authors express their acknowledgments to CEBIMar-USP for their support with the animal collection and experiments and to grants 2011/06044-4 and 2011/15612-6, São Paulo Research Foundation (FAPESP) and to CAPES for the scholarship.

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