Does thermal history influence the tolerance of temperate gorgonians to future warming?
Introduction
Temperature is a key environmental factor that affects organisms at all organization levels by controlling their physiological and ecological processes (Calosi et al., 2008). As the mean and extreme temperatures increase in marine systems, the likelihood of the survival of a species or of a population is partially related to their physiological capacity to tolerate elevated temperatures (Hutchins, 1947). Differences in temperature tolerances between organisms can identify individual and ecological characteristics of “winners” and “losers” in a climate change context (Somero, 2010).
Marine benthic habitats, such as tropical and temperate reefs, are socially and economically important because they contribute crucial ecosystem services to the global economy (Costanza et al., 1997). However, these habitats suffer from dramatic increases in mass mortality events and diseases associated with ocean warming (Harvell et al., 1999, 2002; Doney et al., 2012). Among the most affected organisms are sessile invertebrate species, which play important roles in the structure and function of their habitats. Since organisms tend to have thermal tolerances that reflect the environment in which they are found, it is not surprising that recent research has focused on analyzing the thermal responses of marine invertebrates (species and/or populations) to different temperature regimes across varying temporal and spatial scales (Helmuth et al., 2002; Somero, 2005; Oliver and Palumbi, 2011). Several tropical invertebrate species and populations living in environments that have rapid thermal fluctuations and high maximum temperatures exhibit higher thermal tolerances than invertebrate species and populations living under more moderate temperature conditions (Warner et al., 1996; Castillo and Helmuth, 2005; Middlebrook et al., 2008; Oliver and Palumbi, 2011). However, the relationship between thermal history and thermal tolerance has rarely been examined in subtidal marine macroinvertebrates.
The Mediterranean Sea is one of the fastest warming regions affected by climate change (Bindoff et al., 2007; Burrows et al., 2011), and it has been greatly impacted by several human-mediated threats since ancient times (Coll et al., 2010). Moreover, the Mediterranean marine ecosystem, similar to other subtidal temperate ecosystems, experiences a narrower range of daily thermal fluctuations than intertidal reefs, where most of the thermal tolerance studies have been conducted. Given these facts, the Mediterranean Sea represents an excellent natural laboratory for exploring the responses of temperate marine biota impacted by climate change. The results of such explorations may provide new insights into the role of thermal histories on the resistance of marine invertebrates to thermal stress.
Several studies have provided evidence that thermal stress affects the growth, survival and physiology of zooxanthellate and azooxanthellate cnidarians inhabiting Mediterranean Sea subtidal reefs (Garrabou et al., 2009; Calvo et al., 2011). However, these studies have rarely examined the potential differential thermal tolerances at both inter- and intraspecific levels. The few studies that are available have considered the differences between shallow and deep populations from a single location and between populations dwelling in the coldest areas of the NW Mediterranean Sea (Rodolfo-Metalpa et al., 2006; Linares et al., 2008; Torrents et al., 2008; Coma et al., 2009; Ferrier-Pagès et al., 2009; Bensoussan et al., 2010; Pey et al., 2011).
This study focused on the temperate zooxanthellate gorgonian E. singularis, one of the species most affected by thermal anomalies in the NW Mediterranean Sea during the last few decades (Cerrano et al., 2000; Coma et al., 2006; Garrabou et al., 2009). In previous thermal tolerance studies, shallow E. singularis populations displayed a relatively high thermal tolerance. These populations only exhibited sublethal physiological effects after long-term exposure at 26 °C (Ferrier-Pagès et al., 2009; Previati et al., 2010), and they only suffered extensive damage when temperatures rose above 28 °C (Pey et al., 2011). As for other Mediterranean species, the E. singularis populations examined reside in the coldest areas of the NW Mediterranean Sea, such as the Gulf of Lions (Bensoussan et al., 2010; www.t-mednet.org). However, E. singularis populations are distributed throughout the entire Mediterranean Sea, and they experience contrasting thermal conditions. Here, we investigated the role of thermal history on the thermal stress responses of the temperate gorgonian E. singularis. In contrast to previous studies, we examined the populations dwelling in the warmest and the coldest areas of the NW Mediterranean Sea to experimentally test the hypothesis that they had differential thermal tolerance resistances.
Section snippets
Study locations
This study examined two populations of white gorgonian E. singularis that displayed differential thermal environments and were located in two areas of the NW Mediterranean Sea basin: the Medes Islands (L'Estartit, NE Spain) and Menorca Island (Balearic Islands, Spain) (Fig. 1a). Both populations, separated by approximately 230 km, exhibited different mortality responses during the two largest mass mortality events recorded in the Mediterranean Sea (recorded in 1999 and 2003), which were caused
Results
Daily mean temperature cycles showed contrasting conditions in the two study locations at 20–25 m, the intermediate depth that E. singularis inhabited (Fig. 2a). Although maximum temperatures recorded varied per year (Fig. 2a), Menorca Island had much warmer temperatures (maximum temperatures of 27 °C) than the North Catalan Coast (Medes Islands, maximum temperatures of 25.1 °C). In the waters around the Medes Islands, summertime temperatures were generally below 23 °C and rarely reached
Discussion
The results obtained from our experiments demonstrated differential thermotolerances of Eunicella populations subjected to hyperthermal conditions (upper thermal limits of 28 and 29 °C for the Medes Islands and Menorca Island populations, respectively). Although the lethal temperatures reported in this study have not been recorded at the depths where E. singularis dwell in both areas (Bensoussan et al., 2010; www.t-mednet.org), the differential response to the same hyperthermal conditions
Conclusions
Our study is one of the first to provide evidence on the role of thermal histories in shaping thermotolerance responses of Mediterranean marine invertebrate species dwelling under contrasting temperature regimes. The differential response of populations to the same hyperthermal conditions (a 1 °C temperature differential between the first appearances of tissue necrosis in the two populations examined) support the hypothesis that populations dwelling in warmer waters, such as on Menorca Island,
Acknowledgments
The authors are grateful to all the staff of the ZAE at the Institut de Ciències del Mar for assistance with aquarium experiments. We thank the entire staff of the “Reserva Marina del Nord de Menorca” and the “Reserva Marina de les Illes Medes” for their continuous support. We also thank Nathaniel Bensoussan (Ipso Facto Company) for his help in temperature data treatment. The study was funded by the Spanish Ministry of Economy and Innovation through the Biorock project (CTM2009–08045), the
References (46)
- et al.
High resolution characterization of northwest Mediterranean coastal waters thermal regimes: to better understand responses of benthic communities to climate change
Estuarine Coast Shelf Science
(2010) - et al.
Mass mortality of marine invertebrates: an unprecedented event in the Northwestern Mediterranean
Comptes Rendus de l'Académie des Sciences – Series III – Sciences de la Vie
(2000) - et al.
Depth-dependant thermotolerance of the symbiotic Mediterranean gorgonian Eunicella singularis: evidence from cellular stress markers
Journal of Experimental Marine Biology and Ecology
(2011) - et al.
Oxygen consumption in Mediterranean octocorals under different temperatures
Journal of Experimental Marine Biology and Ecology
(2010) - et al.
Anomalies thermiques dans les eaux du golfe de Marseille durant l’été 1999. Une explication partielle de la mortalité d’invertébrés fixés
Comptes Rendus de l'Académie des Sciences – Series III – Sciences de la Vie
(2000) - et al.
Upper thermal thresholds of shallow vs. deep populations of the precious Mediterranean red coral Corallium rubrum (L.): assessing the potential effects of warming in the NW Mediterranean
Journal of Experimental Marine Biology and Ecology
(2008) A new method for non-parametric multivariate analysis of variance
Austral Ecology
(2001)- et al.
PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods
(2008) - et al.
Thermodependent bacterial pathogens and mass mortalities in temperate benthic communities: a new case of emerging disease linked to climate change
Global Change Biology
(2007) - et al.
Protein expression and genetic structure of the coral Porites lobata in an environmentally extreme Samoan back reef: does host genotype limit phenotypic plasticity?
Molecular Ecology
(2010)
Observations: oceanic climate change and sea level
The pace of shifting climate in marine and terrestrial ecosystems
Science
Thermal tolerance, acclimatory capacity and vulnerability to global climate change
Biology Letters
Impact of climate change on Mediterranean marine ecosystems: the case of the Catalan Sea
Climate Research
Influence of thermal history on the response of Montastraea annularis to short-term temperature exposure
Marine Biology
A catastrophic mass-mortality episode of gorgonians and other organisms in the Ligurian Sea (northwestern Mediterranean), summer 1999
Ecology Letters
PRIMER V6: User Manual/Tutorial
The biodiversity of the Mediterranean sea: estimates, patterns, and threats
PLoS ONE
Global warming-enhanced stratification and mass mortality events in the Mediterranean
Proceedings of the National Academy of Sciences United States of America
Consequences of a mass mortality in populations of Eunicella singularis (Cnidaria: Octocorallia) in Menorca (NW Mediterranean)
Marine Ecology Progress Series
Food availability promotes rapid recovery from thermal stress in a scleractinian coral
Coral Reefs
The value of the world's ecosystem services and natural capital
Nature
Effets du changement climatique sur les écosystèmes littoraux de la Mer Méditerranée Nord-occidentale: étude de la relation entre les conditions de température et la réponse biologique pendant les événements de mortalité massive
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