Feeding plasticity more than metabolic rate drives the productivity of economically important filter feeders in response to elevated CO2 and reduced salinity

Abstract

Climate change driven alterations in salinity and carbonate chemistry are predicted to have significant implications particularly for northern costal organisms, including the economically important filter feeders Mytilus edulis and Ciona intestinalis. However, despite a growing number of studies investigating the biological effects of multiple environmental stressors, the combined effects of elevated pCO2 and reduced salinity remain comparatively understudied. Changes in metabolic costs associated with homeostasis and feeding/digestion in response to environmental stressors may reallocate energy from growth and reproduction, affecting performance. Although these energetic trade-offs in response to changes in routine metabolic rates have been well demonstrated fewer studies have investigated how these are affected by changes in feeding plasticity. Consequently, the present study investigated the combined effects of 26 days’ exposure to elevated pCO2 (500 µatm and 1000 µatm) and reduced salinity (30, 23, and 16) on the energy available for growth and performance (Scope for Growth) in M. edulis and C. intestinalis, and the role of metabolic rate (oxygen uptake) and feeding plasticity [clearance rate (CR) and absorption efficiency] in this process. In M. edulis exposure to elevated pCO2 resulted in a 50% reduction in Scope for Growth. However, elevated pCO2 had a much greater effect on C. intestinalis, with more than a 70% reduction in Scope for Growth. In M. edulis negative responses to elevated pCO2 are also unlikely be further affected by changes in salinity between 16 and 30. Whereas, under future predicted levels of pCO2C. intestinalis showed 100% mortality at a salinity of 16, and a >90% decrease in Scope for Growth with reduced biomass at a salinity of 23. Importantly, this work demonstrates energy available for production is more dependent on feeding plasticity, i.e. the ability to regulate CR and absorption efficiency, in response to multiple stressors than on more commonly studied changes in metabolic rates.

Energetic context determines species and community responses to ocean acidification

“…Experiments that simultaneously manipulate food supply and CO 2 can help determine if higher energetic supply can modify the outcome of acidification‐driven energetic trade‐offs. Energetic trade‐offs in response to stress can be inferred by identifying decreases in non‐maintenance organismal performance metrics (e.g., growth, activity, reproduction, storage), increases in maintenance costs (e.g., metabolic rate) or direct changes in ATP allocation (Kooijman 2010, Sokolova et al 2012, Rastrick et al 2018). It is likely that performance metrics that relate more directly to energy use and allocation will be more influenced by food addition.…”

Contrasting responses to salinity and future ocean acidification in arctic populations of the amphipod Gammarus setosus

“…An elevation in pCO2 in the laboratory had no effect on Na + /K + ATPase activities, or on CEA, but it did increase haemolymph osmolality, and resulted in lower rates of oxygen uptake in amphipods from all populations. Unlike previous studies, there were no interactions between pCO2 and salinity (Rastrick et al, 2018a;Whiteley et al, 2018). The relevance of the independent effects of salinity and pCO2 on amphipod osmoregulatory capacity and the likely repercussions on energy budgets and fitness is discussed below.…”

“…The predicted future elevated pCO2 level of 1000 µatm (RCP8.5 2100 pCO2 projection; Van-Vuuren et al, 2011) was achieved by continuously bubbling a premixed air-CO2 gas mixture into each of the replicate high CO2 treatment tanks separately. A pCO2 of 1000 µatm was controlled at each salinity as explained by Rastrick et al (2018a). In summary, predetermined seawater pH levels, adjusted for temperature, salinity and total alkalinity (AT) for each treatment were calculated using free access CO2SYS (Lewis and Wallace 1998;(30 = pH 7.643;23 = pH 7.567).…”

Respiratory quotient and the stoichiometric approach to investigating metabolic energy substrate use in aquatic ectotherms

“…Salinity has a profound influence on the performance of aquatic ectotherms such as larval development, growth and respiratory metabolism (Boeuf & Payan 2001;Morash & Alter 2016;Rastrick et al 2018). Many euryhaline ectotherms experience large salinity changes during their lifecycle (Boeuf & Payan 2001;Rastrick et al 2018). For example, ectotherms inhabiting coastal estuaries and tide pools (Iverson et al 1989;Boeuf & Payan 2001) and some special species, such as salmon and eel, whose lifecycle involves migration between freshwater and seawater environments (Boeuf & Payan 2001).…”

“…Many euryhaline ectotherms experience large salinity changes during their lifecycle (Boeuf & Payan 2001; Rastrick et al . 2018). For example, ectotherms inhabiting coastal estuaries and tide pools (Iverson et al .…”