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Physiological response to warming in intertidal macroalgae with different thermal affinity

https://doi.org/10.1016/j.marenvres.2021.105350Get rights and content

Highlights

  • Photosynthesis of cold-affinity algae was less responsive than respiration to warming.

  • Warm-affinity showed similar responsiveness for both rates.

  • Relative responsiveness of both rates may be indicative of warming susceptibility.

Abstract

Changes in the abundance and distribution of seaweeds have been reported worldwide. In Northwest Iberia, cold and warm affinity seaweeds have respectively decreased and increased their abundance. To improve our understanding of their vulnerability to future warming scenarios, the effects of warming on the photosynthetic and respiratory performance of seaweeds with cold-water (Fucus serratus and Vertebrata lanosa) and warm-water (Padina pavonica and Gigartina pistillata) affinities were compared in a highly resolved temperature gradient (7–31 °C) under controlled laboratory conditions. While neither the optimum temperature nor the photosynthetic rate at the optimum temperature showed consistent differences between water affinity groups, the temperature dependence of net photosynthesis was significantly higher in the warm-affinity group. Photosynthesis was less responsive than respiration to warming in cold-affinity seaweeds while both rates showed similar responsiveness in warm-affinity ones, suggesting that the relative responsiveness of respiration and photosynthesis to temperature may be indicative of warming susceptibility.

Introduction

Climate change has been distorting marine ecosystems in the last decades, leading to the collapse of some species (Hoegh-Guldberg and Poloczanska, 2017; Mieszkowska and Sugden, 2016). In particular, warming seawater is disrupting the abundance and distribution of many organisms worldwide (Burrows et al., 2014, 2019). For example, several studies indicate that many seaweeds are changing their range and abundance along the European coast in the last decades (Barrientos et al., 2020; Díez et al., 2012; Fernández, 2016; Gallon et al., 2014; Lima et al., 2007; Piñeiro-Corbeira et al., 2016). As seen in other temperate regions, cold-water seaweeds have retreated their range northwards, while warm-water ones have expanded their presence further north (Lima et al., 2007; Wernberg et al., 2011a, 2011b, 2012). Understandably, these changes have been linked to warming seawater given the role of temperature as main determinant of the geographical range of these species (Lüning, 1990).

Surface temperature is projected to rise in the next decades and warming will likely exceed 2 °C by the end of the 21st century, unless greenhouse gas emissions are stringently curbed (Intergovernmental Panel on Climate Change, 2014). Seaweeds are thermo-conformer organisms and environmental temperature profoundly influences their enzymatic processes and metabolic functions such as photosynthesis and respiration (Hurd et al., 2014; Ji et al., 2016; Piñeiro-Corbeira et al., 2018). Hence, these metabolic processes can be used as indicators of stress (Hurd et al., 2014; Piñeiro-Corbeira et al., 2018; Wernberg et al., 2016), and the ecophysiological response of seaweeds to thermal stress could assist us to anticipate how the conditions expected for the next decades will affect them (Colvard et al., 2014). Furthermore, some studies suggest that the sensitivity of seaweeds to warming might be inferred from the temperature dependence of processes such as respiration and photosynthesis (Eggert and Wiencke, 2000; Kübler and Davison, 1995; Piñeiro-Corbeira et al., 2018; Staehr and Wernberg, 2009). The latter can be characterized by the Boltzmann-Arrhenius model derived from chemical kinetics, in which the slope of the Boltzmann-Arrhenius equation, with its sign reversed, is known as the activation energy (Ea) and expresses the temperature dependence (Gillooly et al., 2001; Sibly et al., 2012). Unlike the commonly used Q10, Ea is temperature independent because it avoids the distortion introduced by parameterizing in 10 °C increments (Brown et al., 2004; Gillooly et al., 2001; Sibly et al., 2012).

Previous research in Northwest Iberian Peninsula found that the relative sensitivity of photosynthesis and respiration to warming matched the recent decadal changes in abundance recorded in eight seaweeds with different temperature affinities (Piñeiro-Corbeira et al., 2018). This was interpreted as evidence that assessing the temperature dependence of photosynthesis and respiration with short-term experiments may serve as a biomarker of the potential vulnerability of some seaweeds to the consequences of water warming. Promising as it may seem, further evidence is required to ascertain the generality of this relationship. Here, we contribute to building this further evidence by examining the temperature response of four other seaweeds common to the Northwest Iberian Peninsula.

Section snippets

Species selection and sample collection

The experimental plan included brown and red seaweeds evenly partitioned into two temperature affinity groups, taking thermal affinity as a proxy of their potential sensitivity to seawater warming. In all cases, the selected seaweeds are common in the Northwest Iberian Peninsula and can be readily assigned to a thermal affinity group based on their native range. Thus, the brown Fucus serratus (Linnaeus) and the red Vertebrata lanosa (Linnaeus) are northern seaweeds whose range extends from the

Results and discussion

Photosynthesis (both NPmax and GPmax) showed the typical hump-shaped response except for GPmax in the warm-affinity P. pavonica, which showed no evidence of decrease even at the warmest temperatures used in this study (28 °C, 31 °C) (Fig. 1). Like F. vesiculosus in Piñeiro-Corbeira et al. (2018), GPmax rates in the small brown P. pavonica surpassed the values recorded in any of the other three seaweeds, especially at temperatures above 12 °C. Actually, the upper end of GPmax values recorded in

Author contributions

LDA: Resources, Investigation, Formal analysis, Writing-original draft; RB: Conceptualization, Methodology, Formal analysis, Supervision, Funding acquisition; IP: Resources, Investigation, Formal analysis; CPC: Conceptualization, Resources, Methodology, Formal analysis, Supervision. All authors: Writing-Review & Editing final draft.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

We acknowledge funding from Xunta de Galicia (Axudas para a consolidación e estruturación de unidades de investigación competitivas do SUG, grants ED431D 2017/20, ED431B 2018/49. LDA acknowledges the funding received through the scholarships program of Ministerio de Educación Superior Ciencia y Tecnología of Dominican Republic (MESCyT) and Fundación Propagas. IP acknowledges funding to the European Cooperation in Science and Technology (COST) through a grant within the COST Action CA15121,

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