Linking energy budget to physiological adaptation: How a calcifying gastropod adjusts or succumbs to ocean acidification and warming

https://doi.org/10.1016/j.scitotenv.2020.136939Get rights and content

Highlights

  • Energetics and shell properties of gastropods were measured under future climate.

  • Ocean warming increased the feeding rate and hence energy budget of gastropods.

  • The boosted energy budget was linked to increased shell growth and shell strength.

  • Ocean acidification caused these positive effects of warming to become negative.

  • Energy budget determined the adjustability of shell building process in calcifiers.

Abstract

Accelerating CO2 emissions have driven physico-chemical changes in the world's oceans, such as ocean acidification and warming. How marine organisms adjust or succumb to such environmental changes may be determined by their ability to balance energy intake against expenditure (i.e. energy budget) as energy supports physiological functions, including those with adaptive value. Here, we examined whether energy budget is a driver of physiological adaptability of marine calcifiers to the near-future ocean acidification and warming; i.e. how physiological energetics (respiration rate, feeding rate, energy assimilation and energy budget) relates to adjustments in shell growth and shell properties of a calcifying gastropod (Austrocochlea concamerata). We found that ocean warming boosted the energy budget of gastropods due to increased feeding rate, resulting in faster shell growth and greater shell strength (i.e. more mechanically resilient). When combined with ocean acidification, however, the gastropods had a substantial decrease in energy budget due to reduced feeding rate and energy assimilation, leading to the reduction in shell growth and shell strength. By linking energy budget to the adjustability of shell building, we revealed that energy availability can be critical to determine the physiological adaptability of marine calcifiers to the changing oceanic climate.

Introduction

Anthropogenic CO2 emissions have caused detectable changes in the oceanic climate, where ocean acidification and warming are expected to threaten the survival of marine organisms (Kroeker et al., 2013; Nagelkerken and Connell, 2015). However, growing evidence reveals that some of them are able to adapt and thrive in the naturally acidified and warmed oceans (Wernberg et al., 2013; Uthicke et al., 2016; Connell et al., 2017; Leung et al., 2019a). Understanding why marine organisms adjust or succumb to the changing oceanic climate is necessary to predict their population responses and contributions to future marine ecosystems. Energy homeostasis may be central to the physiological adaptability of individuals and hence their persistence to the changing oceanic climate (Sokolova et al., 2012). Indeed, survival may be determined by an individual's capacity to acquire the energy needed to support physiological adjustments to acidifying and warming oceans (Calosi et al., 2017). Here, we use “adaptive response” as any physiological adjustment that improves individual performance during environmental change (Lekevičius and Loreau, 2012). Recognizing physiological energetics might shed light on the adaptive responses of organisms to the changing oceanic climate, and ultimately their fitness and survival.

Ocean acidification is considered detrimental to marine calcifiers (e.g. corals, brachiopods, bivalves, gastropods and sea urchins) because the reduced pH and carbonate saturation state of seawater may hinder the production of calcareous shells or skeletons (Orr et al., 2005). Changes in seawater carbonate chemistry also elevate the energy cost of calcification and possibly undermine shell building (Spalding et al., 2017). In contrast to this expectation, some marine calcifiers are able to maintain, or even enhance, shell growth and shell strength under ocean acidification (Ries et al., 2009; Leung et al., 2017a, Leung et al., 2017b, Leung et al., 2019a; Kawahata et al., 2019), indicating their adaptive potential. Indeed, they can exhibit compensatory mechanisms to buffer the impacts of ocean acidification by modifying shell properties (e.g. mineral composition and crystallinity, Ries, 2011; Leung et al., 2017a) or chemistry of calcifying fluid (e.g. calcium ion concentration, DeCarlo et al., 2018). Since these adaptive responses are fuelled by metabolic energy, physiological performance (e.g. aerobic metabolism, feeding performance and energy assimilation) that determines energy budget (i.e. the balance between energy intake and expenditure) may govern the adaptability of marine calcifiers to the changing oceanic climate.

Energy budget can also be modulated by ocean warming because temperature is a key driver of physiological performance and its effects depend on the thermal tolerance of marine organisms (Pörtner, 2012; Leung et al., 2019b), which can be indicated by critical thermal maximum (CTmax, Lutterschmidt and Hutchison, 1997). If marine organisms are exposed to suboptimal temperatures (i.e. below Topt), elevating seawater temperature will likely increase their physiological performance, energy budget and growth. As such, ocean warming may indirectly strengthen the adaptability of marine calcifiers to ocean acidification. However, elevating seawater temperature may also breach physiological tolerance where optimal temperatures are exceeded (Leung et al., 2017c, Leung et al., 2018, Leung et al., 2019b; Pörtner et al., 2017), so that ocean warming may not always buffer the costs of ocean acidification via the energetic pathway. To elucidate whether ocean warming promotes or dampens the adaptability of marine calcifiers to ocean acidification, it is necessary to examine the link among physiological performance, energy budget and shell properties.

Here, we assessed whether energy budget is associated with physiological adaptability of marine calcifiers to ocean acidification, using a gastropod (Austrocochlea concamerata) as the study species. We hypothesized that (1) the physiological performance (respiration rate, feeding rate and energy assimilation), energy budget and growth of gastropods are boosted by ocean warming when the temperature is far below their upper thermal threshold (i.e. CTmax); (2) ocean acidification reduces the positive effects of warming; and (3) responses of gastropods to ocean acidification are diminished (i.e. reduced shell growth, mechanical resilience, organic matter content and crystallinity) when energy budget decreases, and vice versa. By linking energy budget to the adjustability of shell building, this study provides critical insights into whether energy availability can determine the physiological adaptability of marine calcifiers to the changing oceanic climate.

Section snippets

Collection of specimens

Mature individuals of gastropod Austrocochlea concamerata (shell length: 13–17 mm) were collected in May (Austral autumn) from the rocky shore at Marino Rocks (35°20′39″S, 138°30′30″E), South Australia. This herbivorous gastropod is abundant from the middle to lower intertidal, suggesting their important contribution to the trophic dynamics in the habitat. In the laboratory, they were allowed to acclimate in a plastic tank (1 m × 40 cm × 30 cm) filled with natural seawater under ambient

Results

The food ingestion rate of A. concamerata was raised by elevated temperature, but such positive effect was not observed when combined with elevated pCO2 (Fig. 1a, Table S2). This same pattern was also observed for absorption rate, except that the negative effect of elevated pCO2 was greater at elevated temperature due to the lower assimilation efficiency (Fig. 1b and c, Table S2). Respiration rate was upregulated by both elevated pCO2 and temperature in isolation, but such effect of elevated

Discussion

Energy is the common currency to fuelling various physiological processes and activities, which can be fundamental to the adaptability of organisms to climate change. We found that the predicted future oceanic climate (i.e. ocean acidification and warming) reduced the physiological performance and hence energy budget of a gastropod, which in turn undermined its capacity for shell building. Hence, energy surplus appears critical to the fitness of marine organisms in the future oceans.

Ocean

Conclusion

Marine organisms are expected to be weakened by ocean acidification and warming, but growing evidence reveals their adaptive potential. Energy availability may determine the adaptability of marine organisms because energy can be used to support adaptive responses to the changing oceanic climate. As such, their ability to balance energy intake against expenditure for maintaining physiological functions may be critical. Here, we reveal that ocean warming increased the physiological performance,

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

Support was provided by the Fundamental Research Funds for the Central Universities (SWU118105), IPRS Scholarship from the University of Adelaide to JYSL, Australian Research Council Discovery Program grant to BDR and SDC (DP150104263), and ARC Future Fellowship to SDC (FT0991953).

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