Different sensitivity to heatwaves across the life cycle of fish reflects phenotypic adaptation to environmental niche

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Highlights

  • Life-cycle assessments are crucial to forecast global change impacts on biota.

  • Heatwave effects were tested in seabreams across their life cycle.

  • Sub-cellular, cellular and whole organism indicators were assessed.

  • The vulnerability of life cycle stages can be ranked as larvae > adults > juveniles.

  • Life-cycle closure may be in jeopardy due to the sensitivity of larvae to heat.

Abstract

Predicting responses of marine organisms to global change requires eco-physiological assessments across the complex life cycles of species. Here, we experimentally tested the vulnerability of a demersal temperate fish (Sparus aurata) to long-lasting heatwaves, on larval, juvenile and adult life-stages. Fish were exposed to simulated coastal (18 °C), estuarine (24 °C) summer temperatures, and heatwave conditions (30 °C) and their physiological responses were assessed based on cellular stress response biomarkers (heat shock protein 70 kDa, ubiquitin, antioxidant enzymes, lipid peroxidation) and phenotypic measures (histopathology, condition and mortality). Life-stage vulnerability can be ranked as larvae > adults > juveniles, based on mortality, tissue pathology and the capacity to employ cellular stress responses, reflecting the different environmental niches of each life stage. While larvae lacked acclimation capacity, which resulted in damage to tissues and elevated mortality, juveniles coped well with elevated temperature. The rapid induction of cytoprotective proteins maintained the integrity of vital organs in juveniles, suggesting adaptive phenotypic plasticity in coastal and estuarine waters. Adults displayed lower plasticity to heatwaves as they transition to deeper habitats for maturation, showing tissue damage in brain, liver and muscle. Life cycle closure of sea breams in coastal habitats will therefore be determined by larval and adult stages.

Introduction

Average global temperature is predicted to increase by 2-6 °C in the next century, owing to anthropogenic climate change (Hansen et al., 2010; IPCC, 2013, 2007). In addition to changes in mean temperatures, extreme events like marine heat waves are predicted to expand in frequency and amplitude as well as spatially, acting as strong selection pressures with severe and possibly irreversible ecological impacts (Grant et al., 2017; Smale et al., 2019; Stillman, 2019). In literature reviews, fish have been pointed out as one of the main taxonomic groups with a high risk of impact under business-as-usual CO2 emission scenarios (Gattuso et al., 2015; Nagelkerken and Connell, 2015). Distributional shifts, abundance changes, altered migration patterns, lower recruitment success, and changes in trophic cascades have already been reported (Nagelkerken and Connell, 2015; Rijnsdorp et al., 2009; Sims et al., 2004; Ullah et al., 2018; Vinagre et al., 2019; Walther et al., 2002). Ultimately, climate warming may lead to a convergence of traits that enable adaptation of fish communities to novel environments. Smaller and fast growing species with a preference for higher temperatures and pelagic water column position should be favored in this new scenario (McLean et al., 2019).

Temperature drives physiological processes in ectotherms (Brett, 1971), affecting metabolic rates, immune responses, growth, reproduction, foraging and performance (Ettinger-Epstein et al., 2007; Motani and Wainwright, 2015; Pittman et al., 2013; Pörtner and Farrell, 2008). In order to cope with environmental change and maintain homeostasis, organisms can modify their gene expression patterns and physiological functions (Hofmann and Todgham, 2010; Logan and Somero, 2011) by up-regulating the minimal stress proteome (Kültz, 2005; Madeira et al., 2017). The main proteins involved in the cellular stress response (CSR) to mitigate cellular damage include i) heat shock proteins, which are chaperones with an adaptive value, repairing denatured proteins upon thermal stress and maintaining the integrity of the protein pool (Feder and Hofmann, 1999; Hofmann and Todgham, 2010; Madeira et al., 2012, Narum and Campbell, 2015; Sørensen et al., 2003), ii) ubiquitin, which targets irreversibly damaged proteins for proteasome degradation preventing cytotoxic aggregations (Hofmann and Somero, 1995; Logan and Somero, 2011; Madeira et al., 2014; Tang et al., 2014), iii) antioxidant enzymes which neutralize ROS (reactive oxygen species) and oxidation products (e.g. lipid peroxides) that arise due to higher metabolic rates at higher temperatures (Bagnyukova et al., 2007; Heise et al., 2006; Lushchak and Bagnyukova, 2006; Vinagre et al., 2012).

Despite the vast literature on thermal eco-physiology of fish, most studies have not considered their complex life cycles, hampering accurate predictions of climate change impacts on fish populations. Successive life stages have different requirements (habitat, food, physiology, size, form, behavior, thermal niche) and therefore climate change is expected to differently affect eco-physiological traits of organisms throughout their life cycles, impacting mostly survival and dispersal processes in larvae and fitness in adults (Kingsolver et al., 2011; Petitgas et al., 2013; Rijnsdorp et al., 2009; Webster et al., 2013). Constraints in oxygen supply capacity related to body size and the development of tissue functional capacity during ontogeny have been hypothesized to cause differences in thermal ranges across the life cycle of fish and thus thermal stress phenomena at systemic and cellular levels (Dahlke et al., 2020; Pörtner et al., 2017; Pörtner and Farrell, 2008). Accordingly, thermal strategies are known to vary across life cycle stages (Truebano et al., 2018) and an ontogenetic shift in temperature tolerance is expected (Pörtner and Farrell, 2008; Rijnsdorp et al., 2009). In general, thermal window widths are narrower for eggs and larvae while increasing in juveniles and becoming constrained again at a large body size (adult stage) (Pörtner and Farrell, 2008; Truebano et al., 2018). Consequently, determining the life history stage(s) most critical for life cycle closure under ocean warming and heat wave scenarios is essential for understanding the consequences and selection pressures imposed by global change upon organisms. Such studies are especially relevant in commercial species considering that fishing reduces genetic variability and alters the structure and thus reproductive capacity of the population (Anderson et al., 2008; Caddy and Agnew, 2003; Ottersen et al., 2006), leading to increased sensitivity of fish stocks to adverse climate conditions (Ottersen et al., 2006; Planque and Fredou, 1999). The scientific community is thus faced with the challenge of projecting the effect of climate forcing on exploited fish species and subsequently design adequate management guidelines, following a climate-smart conservation strategy (Bozinovic and Pörtner, 2015; Kingsolver et al., 2011; Petitgas et al., 2013; Radchuk et al., 2013; Stein et al., 2014).

We hypothesize that plasticity in traits related to thermal physiology is modulated non-linearly in fish species with complex life cycles, in which life stages occupy different environmental niches. Specifically, we aim at disclosing which life stages are most vulnerable to extreme heatwaves by being less metabolically competent to swiftly deploy mechanisms of cellular defense, resulting in deleterious consequences at the whole-organism level and leading to pathophysiological anomalies and increased mortality.

To test our hypothesis, we integrate sub-cellular to whole-organism endpoints to compare the vulnerability and acclimation capacity of fish life cycle stages toward long lasting heat waves using a proxy for common demersal predatory fish, the commercial sea bream Sparus aurata. We chose life-stages that transition from open ocean to coastal and estuarine environments (at larval stage) and that exclusively inhabit shallow coastal waters, lagoons and estuarine environments (juveniles), subsequently moving to coastal and open ocean waters again (growing adults). These life stages have a high probability of exposure to extreme temperatures, not only due to the increase in intensity, duration and frequency of heat waves but also due to the small thermal inertia of shallow habitats. Hence, embryos and spawners were excluded as they only occur in colder open sea waters.

Section snippets

Ethical statement

This study was approved by Direcção Geral de Alimentação e Veterinária and followed EU legislation for animal experimentation (Directive, 2010/63/EU).

Assessment of Sparus aurata's thermal environments

Temperature data were obtained for both coastal and estuarine waters using several tools: 1) studies in Portuguese coastal waters and estuaries (Minho, Douro, Ria de Aveiro, Mondego, Tejo, Sado, Mira, Ria Formosa, Guadiana; data between 1978 and 2005, not continuous - Azevedo et al., 2006; Cabral et al., 2007; Costa, 1990; Coutinho, 2003; Madeira

Assessment of Sparus aurata's thermal environments

Monthly mean sea surface temperature (SST) along the Portuguese coast registered values from 12 (at the Northern coast, Viana do Castelo) to 16 °C (at the Southern coast of Algarve) during the winter months (December to March). Monthly mean ± sd (averaging all locations) was 15.6 ± 0.2 °C in December, 14.8 ± 0.3 °C in January, 13.9 ± 0.6 °C in February, and 14.2 ± 0.4 °C in March (satellite dataset from 2011 to 2015). During summer months (June to September) monthly mean SST ranged from 15 to

Discussion

Accurate predictions of the impacts of climate change on populations and ecosystems ideally require the assessment of thermal tolerance of all life-history stages (Freitas et al., 2010; Levy et al., 2015; Zeigler, 2013). Here, we show that while demersal fish larvae lack the ability to tolerate or acclimate to elevated summer temperatures and heat waves, juveniles were able to cope with all warming scenarios. Larger adult fish survived elevated summer temperatures but were also severely

CRediT authorship contribution statement

Diana Madeira: Investigation, Formal analysis, Data curation, Writing - original draft, Visualization. Carolina Madeira: Investigation, Writing - review & editing. Pedro M. Costa: Methodology, Investigation, Formal analysis, Visualization, Supervision, Resources, Writing - review & editing. Catarina Vinagre: Conceptualization, Methodology, Writing - review & editing, Supervision. Hans-Otto Pörtner: Writing - review & editing. Mário S. Diniz: Conceptualization, Methodology, Validation,

Declaration of competing interest

The authors have no conflicts of interest to declare.

Acknowledgements

Authors would like to thank MARESA for providing S. aurata larvae, juveniles and adults as well as Artemia salina nauplii.

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