Adaptation and acclimatization to ocean acidification in marine ectotherms: an in situ transplant experiment with polychaetes at a shallow CO₂ vent system

Metabolic rate determines the physiological and life-history performances of ectotherms. Thus, the extent to which such rates are sensitive and plastic to environmental perturbation is central to an organism's ability to function in a changing environment. Little is known of long-term metabolic plasticity and potential for metabolic adaptation in marine ectotherms exposed to elevated pCO₂. Consequently, we carried out a series of in situ transplant experiments using a number of tolerant and sensitive polychaete species living around a natural CO₂ vent system. Here, we show that a marine metazoan (i.e. Platynereis dumerilii) was able to adapt to chronic and elevated levels of pCO₂. The vent population of P. dumerilii was physiologically and genetically different from nearby populations that experience low pCO₂, as well as smaller in body size. By contrast, different populations of Amphiglena mediterranea showed marked physiological plasticity indicating that adaptation or acclimatization are both viable strategies for the successful colonization of elevated pCO₂ environments. In addition, sensitive species showed either a reduced or increased metabolism when exposed acutely to elevated pCO₂. Our findings may help explain, from a metabolic perspective, the occurrence of past mass extinction, as well as shed light on alternative pathways of resilience in species facing ongoing ocean acidification

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

AbstractClimate 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 &amp;gt;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.</jats:p

The effects of elevated temperature and PCO2 on the energetics and haemolymph pH homeostasis of juveniles of the European lobster, Homarus gammarus

Regulation of extracellular acid–base balance, while maintaining energy metabolism, is recognised as an important aspect when defining an organism's sensitivity to environmental changes. This study investigated the haemolymph buffering capacity and energy metabolism (oxygen consumption, haemolymph [l-lactate] and [protein]) in early benthic juveniles (carapace length <40 mm) of the European lobster, Homarus gammarus, exposed to elevated temperature and PCO2. At 13°C, H. gammarus juveniles were able to fully compensate for acid–base disturbances caused by the exposure to elevated seawater PCO2 at levels associated with ocean acidification and carbon dioxide capture and storage (CCS) leakage scenarios, via haemolymph [HCO3−] regulation. However, metabolic rate remained constant and food consumption decreased under elevated PCO2, indicating reduced energy availability. Juveniles at 17°C showed no ability to actively compensate haemolymph pH, resulting in decreased haemolymph pH particularly under CCS conditions. Early benthic juvenile lobsters at 17°C were not able to increase energy intake to offset increased energy demand and therefore appear to be unable to respond to acid–base disturbances due to increased PCO2 at elevated temperature. Analysis of haemolymph metabolites suggests that, even under control conditions, juveniles were energetically limited. They exhibited high haemolymph [l-lactate], indicating recourse to anaerobic metabolism. Low haemolymph [protein] was linked to minimal non-bicarbonate buffering and reduced oxygen transport capacity. We discuss these results in the context of potential impacts of ongoing ocean change and CCS leakage scenarios on the development of juvenile H. gammarus and future lobster populations and stocks. -- Keywords : Developmental physiology ; Ocean acidification ; Ocean warming ; Early benthic juvenile ; Acid–base balance ; Metabolism

Individual and population-level responses to ocean acidification

Ocean acidification is predicted to have detrimental effects on many marine organisms and ecological processes. Despite growing evidence for direct impacts on specific species, few studies have simultaneously considered the effects of ocean acidification on individuals (e.g. consequences for energy budgets and resource partitioning) and population level demographic processes. Here we show that ocean acidification increases energetic demands on gastropods resulting in altered energy allocation, i.e. reduced shell size but increased body mass. When scaled up to the population level, long-term exposure to ocean acidification altered population demography, with evidence of a reduction in the proportion of females in the population and genetic signatures of increased variance in reproductive success among individuals. Such increased variance enhances levels of short-term genetic drift which is predicted to inhibit adaptation. Our study indicates that even against a background of high gene flow, ocean acidification is driving individual- and population-level changes that will impact eco-evolutionary trajectories

Temporal fluctuations in seawater pCO<inf>2</inf> may be as important as mean differences when determining physiological sensitivity in natural systems

Most studies assessing the impactsofocean acidification (OA) onbenthic marine invertebrates have used stable mean pH/pCO2 levelsto highlight variation in the physiological sensitivities in a range of taxa. However, many marine environments experience natural fluctuations in carbonate chemistry, and to date little attempt has been made to understand the effect of naturally fluctuating seawater pCO2 (pCO2sw) on the physiological capacity of organisms to maintain acid-base homeostasis. Here, for the first time, we exposed two species of sea urchin with different acid-base tolerances, Paracentrotus lividus and Arbacia lixula, to naturally fluctuating pCO2sw conditions at shallow water CO2 seep systems (Vulcano, Italy) and assessed their acid-base responses. Both sea urchin species experienced fluctuations in extracellular coelomic fluid pH, pCO2, and [HCO-3] (pHe, pCO2e, and [HCO-3]e, respectively) in line with fluctuations in pCO2sw. The less tolerant species, P. lividus, had the greatest capacity for [HCO-3]e buffering in response to acute pCO2sw fluctuations, but it also experienced greater extracellular hypercapnia and acidification and was thus unabletofully compensate for acid-basedisturbances. Conversely, themore tolerant A.lixula reliedonnon-bicarbonate protein buffering and greater respiratory control. In the light of these findings, we discuss the possible energetic consequences of increased reliance on bicarbonate buffering activity in P. lividus compared with A. lixula and how these differing physiological responses to acute fluctuations in pCO2sw may be as important as chronic responses to mean changes in pCO2sw when considering how CO2 emissions will affect survival and success of marine organisms within naturally assembled systems

Sperm motility and fertilisation success in an acidified and hypoxic environment

The distribution and function of many marine species is largely determined by the effect of abiotic drivers on their reproduction and early development, including those drivers associated with elevated CO2 and global climate change. A number of studies have therefore investigated the effects of elevated pCO2 on a range of reproductive parameters, including sperm motility and fertilisation success. To date, most of these studies have not examined the possible synergistic effects of other abiotic drivers, such as the increased frequency of hypoxic events that are also associated with climate change. The present study is therefore novel in assessing the impact that a hypoxic event could have on reproduction in a future high CO2 ocean. Specifically, this study assesses sperm motility and fertilisation success in the sea urchin Paracentrotus lividus exposed to elevated pCO2 for 6 months. Gametes extracted from these pre acclimated individuals were subjected to hypoxic conditions simulating an hypoxic event in a future high CO2 ocean. Sperm swimming speed increased under elevated pCO2 and decrease under hypoxic conditions resulting in the elevated pCO2 and hypoxic treatment being approximately equivalent to the control. There was also a combined negative effect of increased pCO2 and hypoxia on the percentage of motile sperm. There was a significant negative effect of elevated pCO2 on fertilisation success, and when combined with a simulated hypoxic event there was an even greater effect. This could potentially affect cohort recruitment and in turn reduce the density of this ecologically and economically important ecosystem engineer therefore potentially effecting biodiversity and ecosystem services

The effect of latitude on RNA activities (<i>K</i>_RNA) and RNA concentrations (RNA: protein).

<p>Values represent: <i>Gammarus setosus</i> (closed circles); <i>G. oceanicus</i> (open circles); <i>G. duebeni</i> (closed triangles) and <i>G. locusta</i> (open triangles). (a) Relationship between <i>K</i>_RNA and latitude (y = −0.078x+6.38; r² = 0.52). (b) Relationship between RNA:protein and latitude (y = −0.35x+0.41; r² = 0.17). Lines fitted using least-squares regression. Mean values given ±SEM. In <i>G. setosus</i>: n = 12 at 79°N. In <i>G. oceanicus</i>: n = 13 at 79°N; n = 11 at 70°N; n = 11 at 58°N. In <i>G. duebeni</i>: n = 8 at 70°N; n = 6 at 58°N; and n = 8 at 53°N. In <i>G. locusta</i>: n = 8 at 53°N; n = 7 at 38°N.</p

Whole-animal fractional rates of protein synthesis (<i>k_s</i>) in crustacean species from a range of thermal habitats.

<p>Fractional rates of protein synthesis (<i>k_s</i>) with associated changes in RNA:protein ratios and RNA activities (<i>K</i>_RNA).</p><p>All values scaled to a standard body mass of 1 g wet weight.</p><p>Original values taken from: a <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0060050#pone.0060050-Whiteley2" target="_blank">[8]</a>; b <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0060050#pone.0060050-Robertson1" target="_blank">[10]</a>; c <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0060050#pone.0060050-Robertson2" target="_blank">[11]</a>; d <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0060050#pone.0060050-Intanai1" target="_blank">[58]</a>; e <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0060050#pone.0060050-Mente1" target="_blank">[59]</a>; and f <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0060050#pone.0060050-Whiteley4" target="_blank">[56]</a>.</p

Least-squares regression analysis for the data presented in Fig. 2.

<p>Data represents the relationship between the specific radioactivity of protein-bound phenylalanine and incorporation time as shown in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0060050#pone-0060050-g002" target="_blank">Figs. 2c, d</a>.</p><p>The regression coefficient (b) characterises the rate of incorporation of the radiolabelled amino acid into the protein bound fraction in dpm nmol phenylalanine min⁻¹. <i>p</i>_b (<i>p</i> value) represents the significance of the least-squares regression model, and <i>p</i>_a represents the significance of the variation between the intercept (a) and the origin.</p><p>All vales are means ±SEM.</p

Fractional (<i>k</i>_s; % day⁻¹) and absolute (<i>A</i>_s; mg day⁻¹) rates of protein synthesis in gammarid amphipods.

<p>Values plotted as a function of latitude (a, c) or capture temperatures (b, d). Species are: <i>Gammarus setosus</i> (closed circles); <i>G. oceanicus</i> (open circles); <i>G. duebeni</i> (closed triangles) and <i>G. locusta</i> (open triangles). (a) Relationship between fractional rates of protein synthesis and latitude (y = −0.05x+3.96; r² = 0.39). (b) Relationship between fractional rates of protein synthesis and capture temperature (y = 0.1x+0.02; r² = 0.23). (c) Relationship between absolute rates of protein synthesis and latitude (y = −0.09x+7.32; r² = 0.48). (d) Relationship between absolute rates of protein synthesis and capture temperature (y = 0.21x+−0.84; r² = 0.32). Lines fitted using least-squares regression. Mean values given ±SEM. In <i>G. setosus</i>: n = 12 at 79°N. In <i>G. oceanicus</i>: n = 13 at 79°N; n = 11 at 70°N; n = 11 at 58°N. In <i>G. duebeni</i>: n = 8 at 70°N; n = 6 at 58°N; and n = 8 at 53°N. In <i>G. locusta</i>: n = 8 at 53°N; n = 7 at 38°N.</p