An integrated investigation of the effects of ocean acidification on adult abalone (Haliotis tuberculata)

Abstract

Ocean acidification (OA) and its subsequent changes in seawater carbonate chemistry are threatening the survival of calcifying organisms. Due to their use of calcium carbonate to build their shells, marine molluscs are particularly vulnerable. This study investigated the effect of CO2-induced OA on adult European abalone (Haliotis tuberculata) using a multi-parameter approach. Biological (survival, growth), physiological (pHT of haemolymph, phagocytosis, metabolism, gene expression), and structural responses (shell strength, nano-indentation measurements, Scanning electron microscopy imaging of microstructure) were evaluated throughout a 5-month exposure to ambient (8.0) and low (7.7) pH conditions. During the first 2 months, the haemolymph pH was reduced, indicating that abalone do not compensate for the pH decrease of their internal fluid. Overall metabolism and immune status were not affected, suggesting that abalone maintain their vital functions when facing OA. However, after 4 months of exposure, adverse effects on shell growth, calcification, microstructure, and resistance were highlighted, whereas the haemolymph pH was compensated. Significant reduction in shell mechanical properties was revealed at pH 7.7, suggesting that OA altered the biomineral architecture leading to a more fragile shell. It is concluded that under lower pH, abalone metabolism is maintained at a cost to growth and shell integrity. This may impact both abalone ecology and aquaculture.

Acid–base balance in the hæmolymph of European abalone (Haliotis tuberculata) exposed to CO2-induced ocean acidification

“…Reduced growth in shell length and alterations of the shell microstructure were observed in juvenile abalone exposed to pH T 7.6, which correspond to projected pH values expected for 2100 (IPCC, 2014;Gattuso et al, 2015). Since these pH conditions corresponded to an aragonite saturation state below 1, it was concluded that the effects on shell growth and integrity were principally caused by direct aragonite dissolution within the abalone shell (Auzoux-Bordenave et al, 2020). Additional effects on the organic periostracum and nacre structure suggested that other processes involved in shell biomineralization, such as matrix protein production and enzymatic activities, would also be influenced by changes in seawater pH.…”

“…Additional effects on the organic periostracum and nacre structure suggested that other processes involved in shell biomineralization, such as matrix protein production and enzymatic activities, would also be influenced by changes in seawater pH. Avignon et al (2020) demonstrated significant effects on growth in shell length, microstructure and resistance in adult H. tuberculata exposed to pH T 7.7. Although the aragonite saturation was above 1 (1.24) here, the effects on shell integrity were partly attributed to direct effects on aragonite dissolution.…”

“…Several studies focusing on early life-history stages of abalone, especially larvae, have demonstrated adverse effects of elevated pCO 2 , such as reduced survival, developmental delay, body and shell abnormalities and reduced mineralization (Byrne et al, 2011;Crim et al, 2011;Guo et al, 2015;Kimura et al, 2011;Onitsuka et al, 2018;Wessel et al, 2018;Zippay and Hofmann, 2010). Impacts of OA on shell calcification and integrity have been well studied on various stages of H. tuberculata, from larvae to juveniles and adults (Wessel et al, 2018;Auzoux-Bordenave et al, 2020;Avignon et al, 2020). Reduced growth in shell length and alterations of the shell microstructure were observed in juvenile abalone exposed to pH T 7.6, which correspond to projected pH values expected for 2100 (IPCC, 2014;Gattuso et al, 2015).…”

“…Low rates of metabolism typically correlate with lower concentrations of ion transport proteins (such as Na + /K + and H + -ATPases, Gibbs and Somero, 1990), suggesting reduced capacities of acid-base balance and a poor ability to compensate for changes in acid-base status (Fabry et al, 2008;Pörtner et al, 2004;Melzner et al, 2009;Parker et al, 2013). In adult H. tuberculata under OA stress, the haemolymph extracellular pH was reported to be 0.1 pH unit lower in individuals subjected to pH T 7.7, compared with those maintained in pH T 8.0, suggesting that abalone only poorly compensate for the pH decrease of their extracellular fluid if at all (Avignon et al, 2020).…”

Effects of elevated temperature andpCO2 on the respiration, biomineralization and photophysiology of the giant clamTridacna maxima

“…Among marine calcifying molluscs (e.g. oysters, mussels, giant clams, abalones, limpets) negative impacts of temperature and p CO 2 have been demonstrated on the survival, growth, biomineralization processes and other key physiological functions on different stages of their life cycle ( Bougrier et al , 1995 ; Kurihara, 2008 ; McClintock et al , 2009 ; Gazeau et al , 2010 ; Welladsen et al , 2010 ; Melzner et al , 2011 ; Rodolfo-Metalpa et al , 2011 ; Schwartzmann et al , 2011 ; Talmage and Gobler, 2011 ; Liu et al , 2012 ; Watson et al , 2012 ; Kurihara et al , 2013 ; Fitzer et al , 2014 ; Le Moullac et al , 2016a , b ; Meng et al , 2018 ; Wessel et al , 2018 ; Avignon et al , 2020 ). However, effects of each stressor and their potential synergetic effect on giant clam’s physiology are still poorly understood.…”