Effects of ocean acidification with pCO2 diurnal fluctuations on survival and larval shell formation of Ezo abalone, Haliotis discus hannai
Introduction
Ocean acidification (OA) is the process of sustained absorption of anthropogenic carbon dioxide (CO2) by the ocean (Caldeira and Wickett, 2003) that has been progressing rapidly since the Industrial Revolution. Elevated partial pressure of CO2 (pCO2) in seawater reduces pH (Caldeira and Wickett, 2003) and carbonate ion (CO32−) availability (Gattuso and Buddemeier, 2000, Feely et al., 2004, Gazeau et al., 2007, Kurihara, 2008) and, consequently, significantly affects marine organisms and ecosystems. Most marine organisms with calcium carbonate (CaCO3) skeletons or shells, such as mollusks, crustaceans, and echinoderms, are particularly susceptible to OA because the reduced pH and carbonate ion availability in seawater generally decrease the calcification rate and/or increase dissolution of CaCO3 structures (e.g., Riebesell et al., 2000, Feely et al., 2004). Moreover, physiological activities of marine animals, such as cellular functions and calcification, are mediated by disturbances and compensatory adjustments in acid–base status (e.g., Pörtner, 2008, Pörtner, 2012, Wittmann and Pörtner, 2013). Thus, it is believed that increasing CO2 in ambient seawater due to progressive OA depresses metabolism and physiological activities by disturbing acid–base status and differential acid–base regulation within various body fluid compartments (Pörtner, 2012, Wittmann and Pörtner, 2013).
Many benthic invertebrates in coastal areas, including calcified organisms (calcifiers) are directly used by humans as fishery resources, and they play important roles in energy/nutrient flow and ecosystem functioning. Most marine invertebrates are poikilosmotic animals with low capacity to regulate acid–base balance and have less osmoregulatory ability compared with those of vertebrate animals (Kokubo, 1962); thus, they are vulnerable to rapid increases in anthropogenic CO2, particularly during early life stages when internal physiological control is developing. Some groups of calcifiers, such as echinoderms, gastropods, and bivalves, show lower survival (Talmage and Gobler, 2009, Talmage and Gobler, 2011, Van Colen et al., 2012), retarded growth (Michaelidis et al., 2005, Shirayama and Thornton, 2005, Talmage and Gobler, 2011), and downsizing/malformation of the shell and skeletogenesis (Parker et al., 2009, Talmage and Gobler, 2009, Sheppard Brennand et al., 2010, Byrne et al., 2011, Kimura et al., 2011, Doo et al., 2012, Van Colen et al., 2012, Onitsuka et al., 2014, Tahil and Dy, 2016) in response to elevated seawater pCO2. In contrast, several animals have nonlinear, neutral, or even positive reactions to elevated pCO2 (e.g. Ries et al., 2009). Ultimately, the effects of increasing CO2 in seawater likely vary among phyla, species, growth stage, latitude, and habitat (e.g. Watson et al., 2012).
The actual responses of animals to OA may be more complex under a natural environment including various biological and physicochemical phenomena. Seawater pCO2 (pH) fluctuates diurnally in the ocean (Borges and Frankignoulle, 1999, Delille et al., 2009, Buapet et al., 2013, Cornwall et al., 2013, Onitsuka et al., 2014), which is generally driven by primary producers decreasing pCO2 (increasing pH) in seawater during the day via photosynthesis and increasing pCO2 (decreasing pH) at night via respiration (Buapet et al., 2013). For example, photosynthesis and respiration by macroalgae in kelp beds lead to marked pCO2 diurnal fluctuations (Delille et al., 2009), which are larger than the pCO2 change projected for open ocean waters due to OA by 2100 (Cornwall et al., 2013). However, most experimental studies that have examined the effects of OA on marine organisms have manipulated seawater pCO2 or pH to a steady level predicted for the future. These studies have increased the understanding of how organisms respond to OA, but may have overlooked the importance of natural fluctuations in seawater pCO2 on organismal response. Some studies have reported that diurnal variations in seawater pCO2 affect the responses of marine animals to elevated pCO2 (Clark and Gobler, 2016, Jarrold et al., 2017). Clark and Gobler (2016) showed that acidified and/or hypoxia condition produced reduced survival, slowed growth and delayed development of larval bivalves, and then diurnal fluctuation of the pH and/or dissolved oxygen (DO) did not fully mitigate the negative effects of hypoxia and/or acidification on the larvae. In contrast, Jarrold et al. (2017) demonstrated that diurnal pCO2 cycles can substantially reduce the severity of behavioral abnormalities in coral reef fish caused by elevated seawater pCO2. These results suggest that the responses of marine animals to increased and/or diurnal fluctuations in pCO2 are highly species-specific. No information is available on how diurnal fluctuating pCO2 affect the performance of most marine animals or how these fluctuations affect the responses of animals to increases in pCO2 level due to progressive OA. Thus, incorporating the diurnal pCO2 fluctuations that occur in the natural environment into OA-simulation experiments will help us better understand the changes in marine organisms and communities in an acidified ocean.
The objective of this study was to investigate the effects of OA in relation to diurnal cycles of pCO2 on early life stages of Ezo abalone, Haliotis discus hannai. Abalone are an important coastal fishery resource worldwide and a target aquaculture species, and are also dominant grazers with relatively high biomass in coastal rocky reefs and exert great influences on food-web structures, energy/nutrient flow, and functioning of coastal ecosystems. Thus, understanding how abalone respond to increases and diurnal fluctuations in seawater pCO2 will provide clues about changes in other benthic invertebrates and ecosystem structure/function in coastal rocky reefs, as well as the prospects for sustainability of natural abalone stocks. Some previous studies that evaluated the effects of OA on abalone species under static pCO2 (pH) conditions reported that elevated pCO2 seawater negatively affects fertilization rate (Kimura et al., 2011), embryogenesis and hatching rate (Kimura et al., 2011, Tahil and Dy, 2016), survival (Crim et al., 2011, Kimura et al., 2011, Tahil and Dy, 2016), and larval shell morphology (Byrne et al., 2011, Crim et al., 2011, Kimura et al., 2011), compared with those in abalone species held in ambient natural seawater. Kimura et al. (2011) showed that static pCO2 seawater < 1100 μatm (pH > 7.68) has no significant negative effect on fertilization, development, survival, or larval shell size of H. discus hannai, whereas highly-elevated pCO2 [1650 (pH 7.49) and 2150 μatm pCO2 (pH 7.41)) has adverse effects. These results suggest that there is a threshold level of pCO2 between 1100 and 1650 μatm in which the early life stages of H. discus hannai are seriously affected. In natural habitats, H. discus hannai are generally competent to settle within a few days after fertilization, and then most larvae settled promptly on coastal reefs within a week after fertilization (Takami et al., 2006). Thus, diurnal fluctuations of pCO2 in the coastal water can have considerable effect on abalone in early life. In this study, we focused on the period in the formation of larval shell, which will be particularly susceptible to reduced pH and carbonate ion availability in seawater by OA (e.g. Riebesell et al., 2000, Feely et al., 2004). To determine whether there is the threshold pCO2 level in seawater that causes severe deterioration in early development and shell formation of abalone and how diurnal fluctuating pCO2 interact with the responses of larval abalone to constant pCO2 conditions, we reared larval abalone H. discus hannai under a series of constant and diurnally fluctuated pCO2 treatments in the two different experiments. The aim of the first experiment was to determine how mean level and/or diurnal fluctuations of seawater pCO2 affect early development and shell formation of larval abalone. If seawater TCO2 balance in a day through photosynthesis/respiration of organisms were similar in future, magnitude of diurnally fluctuating pCO2 become larger with increasing of mean pCO2 level. Thus, the second experiment aimed how magnitude of diel pCO2 cycles, which were designed based on TCO2 scale, affect to the abalone performance.
Section snippets
Rearing apparatus
Experiments were conducted at two onshore laboratories located at the Ezo abalone habitats in Shiogama and Miyako cities (Fig. S1, Table 1). Seawater was pumped from a subtidal intake situated near the laboratories, filtered through a cartridge filter (0.5-μm mesh), and pumped into a 150-L tank. The seawater temperature was controlled at ∼20 °C just before introduction into the CO2 manipulation system. The effects of diurnal fluctuations in seawater pCO2 on larval abalone malformation and
Treatment conditions
The chemical and physical conditions used in the experiments are summarized in Table 2. In Exp. I, pCO2 in all pCO2-constant treatments was maintained within 90 μatm of the target value (Fig. 2), and the pCO2 values were distinguishable and clearly separated between the treatments. Seawater pCO2 in the 800 ± 400 and 1200 ± 400 μatm pCO2 treatments changed in the ranges of 420.3–1189.0 and 707.1–1537.1 μatm, respectively (Fig. 2, Table 2). The gap in pH between the seawater reservoir and the
Discussion
In this study, we found that the negative effects on survival, and larval shell formation of H. discus hannai tended to be greater with increasing pCO2 in the experimental seawater, and then were further strengthened when pCO2 fluctuated diurnally, particularly at pCO2 > 1100 μatm.
Larval mortality and malformation rates as well as shell length in the 800 ± 400 μatm treatment of Exp. I were not different from those in the 450 and 800 μatm pCO2 treatments (Fig. 4). Additionally, no great
Conclusion
This study showed that seawater with highly elevated pCO2 has negative effects on survival and shell formation of larval H. discus hannai, and that there is a pCO2 threshold producing serious negative effects. It was also suggested that the pCO2 threshold would be associated with Ω-aragonite in the seawater. Our experiments demonstrated that diurnal fluctuations in seawater pCO2 within 800 μatm (±400 μatm pCO2) below the threshold level had no significant effects on early development of H.
Acknowledgments
We thank Mr. S. Saito helped maintenance of the AICAL system and abalone rearing. This study was supported by JSPS KAKENHI [Grant Number 23241017, 26220102].
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2022, Marine Environmental ResearchCitation Excerpt :As with most marine molluscs, abalone have a pelago-benthic life cycle with a larval planktonic stage followed by a critical metamorphosis into benthic juveniles, making them highly sensitive to environmental changes (Byrne et al., 2011). Several studies have also focused on early life stages of abalone, especially larvae, demonstrating adverse effects of elevated CO2, 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). More recently, Kavousi et al. (2021) investigated the combined effects of OA and ocean warming on H. tuberculata larvae in a full factorial experiment.