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

Phenomics as an approach to Comparative Developmental Physiology

The dynamic nature of developing organisms and how they function presents both opportunity and challenge to researchers, with significant advances in understanding possible by adopting innovative approaches to their empirical study. The information content of the phenotype during organismal development is arguably greater than at any other life stage, incorporating change at a broad range of temporal, spatial and functional scales and is of broad relevance to a plethora of research questions. Yet, effectively measuring organismal development, and the ontogeny of physiological regulations and functions, and their responses to the environment, remains a significant challenge. “Phenomics”, a global approach to the acquisition of phenotypic data at the scale of the whole organism, is uniquely suited as an approach. In this perspective, we explore the synergies between phenomics and Comparative Developmental Physiology (CDP), a discipline of increasing relevance to understanding sensitivity to drivers of global change. We then identify how organismal development itself provides an excellent model for pushing the boundaries of phenomics, given its inherent complexity, comparably smaller size, relative to adult stages, and the applicability of embryonic development to a broad suite of research questions using a diversity of species. Collection, analysis and interpretation of whole organismal phenotypic data are the largest obstacle to capitalising on phenomics for advancing our understanding of biological systems. We suggest that phenomics within the context of developing organismal form and function could provide an effective scaffold for addressing grand challenges in CDP and phenomics

Comparative phenomics: a new approach to study heterochrony

Understanding the links between development and evolution is one of the major challenges of biology. ‘Heterochronies’, evolutionary alterations in the timings of development are posited as a key mechanism of evolutionary change, but their quantification requires gross simplification of organismal development. Consequently, how changes in event timings influence development more broadly is poorly understood. Here, we measure organismal development as spectra of energy in pixel values of video, creating high-dimensional landscapes integrating development of all visible form and function. This approach we termed ‘Energy proxy traits’ (EPTs) is applied alongside previously identified heterochronies in three freshwater pulmonate molluscs (Lymnaea stagnalis, Radix balthica and Physella acuta). EPTs were calculated from time-lapse video of embryonic development to construct a continuous functional time series. High-dimensional transitions in phenotype aligned with major sequence heterochronies between species. Furthermore, differences in event timings between conspecifics were associated with changes in high-dimensional phenotypic space. We reveal EPTs as a powerful approach to considering the evolutionary importance of alterations to developmental event timings. Reimagining the phenotype as energy spectra enabled continuous quantification of developmental changes in high-dimensional phenotypic space, rather than measurement of timings of discrete events. This approach has the possibility to transform how we study heterochrony and development more generally

Stage-Specific Changes in Physiological and Life-History Responses to Elevated Temperature and Pco2 during the Larval Development of the European Lobster Homarus gammarus (L.)

An organism’s physiological processes form the link between its life-history traits and the prevailing environmental conditions, especially in species with complex life cycles. Understanding how these processes respond to changing environmental conditions, thereby affecting organismal development, is critical if we are to predict the biological implications of current and future global climate change. However, much of our knowledge is derived from adults or single developmental stages. Consequently, we investigated the metabolic rate, organic content, carapace mineralization, growth, and survival across each larval stage of the European lobster Homarus gammarus, reared under current and predicted future ocean warming and acidification scenarios. Larvae exhibited stage-specific changes in the temperature sensitivity of their metabolic rate. Elevated Pco2 increased C∶N ratios and interacted with elevated temperature to affect carapace mineralization. These changes were linked to concomitant changes in survivorship and growth, from which it was concluded that bottlenecks were evident during H. gammarus larval development in stages I and IV, the transition phases between the embryonic and pelagic larval stages and between the larval and megalopa stages, respectively. We therefore suggest that natural changes in optimum temperature during ontogeny will be key to larvae survival in a future warmer ocean. The interactions of these natural changes with elevated temperature and Pco2 significantly alter physiological condition and body size of the last larval stage before the transition from a planktonic to a benthic life style. Thus, living and growing in warm, hypercapnic waters could compromise larval lobster growth, development, and recruitment. -- Keywords : Homarus gammarus ; ocean warming ; ocean acidification ; life history ; larval development ; seafood

Disentangling the counteracting effects of water content and carbon mass on zooplankton growth

Abstract Zooplankton vary widely in carbon percentage (carbon mass as a percentage of wet mass), but are often described as either gelatinous or non-gelatinous. Here we update datasets of carbon percentage and growth rate to investigate whether carbon percentage is a continuous trait, and whether its inclusion improves zooplankton growth models. We found that carbon percentage is continuous, but that species are not distributed homogenously along this axis. To assess variability of this trait in situ, we investigated the distribution of biomass across the range of carbon percentage for a zooplankton time series at station L4 off Plymouth, UK. This showed separate biomass peaks for gelatinous and crustacean taxa, however, carbon percentage varied 8-fold within the gelatinous group. Species with high carbon mass had lower carbon percentage, allowing separation of the counteracting effects of these two variables on growth rate. Specific growth rates, g (d−1) were negatively related to carbon percentage and carbon mass, even in the gelatinous taxa alone, suggesting that the trend is not driven by a categorical difference between these groups. The addition of carbon percentage doubled the explanatory power of growth models based on mass alone, demonstrating the benefits of considering carbon percentage as a continuous trait

Will giant polar amphipods be first to fare badly in an oxygen-poor ocean? Testing hypotheses linking oxygen to body size

Respirometry A.Comparing closed and semi-open respirometer techniques. B.VO2 and body mas

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

Does sex really matter? Explaining intraspecies variation in ocean acidification responses

This is the author accepted manuscript. The final version is available from [the Royal Society via the DOI in this record.There is another ORE record for this publication: http://hdl.handle.net/10871/33286Ocean acidification (OA) poses a major threat to marine ecosystems globally, having significant ecological and economic importance. The number and complexity of experiments examining the effects of OA has substantially increased over the past decade, in an attempt to address multi-stressor interactions and long-term responses in an increasing range of aquatic organisms. However, differences in the response of males and females to elevated pCO2 have been investigated in fewer than 4% of studies to date, often being precluded by the difficulty of determining sex non-destructively, particularly in early life stages. Here we highlight that sex can significantly impact organism responses to OA, differentially affecting physiology, reproduction, biochemistry and ultimately survival. What is more, these impacts do not always conform to ecological theory based on differential resource allocation towards reproduction, which would predict females to be more sensitive to OA owing to the higher production cost of eggs compared with sperm. Therefore, non-sex-specific studies may overlook subtle but ecologically significant differences in the responses of males and females to OA, with consequences for forecasting the fate of natural populations in a near-future ocean.R.P.E was funded by BBSRC grants (BB/N013344/1 and BB/M017583/1) awarded to R.W.W. W.D was funded by a FSBI Internship Award. A.M.Q acknowledges funding from NERC-DEFRA Marine Ecosystems Research Programme (NE/L003279/1)

A novel application of motion analysis for detecting stress responses in embryos at different stages of development.

Motion analysis is one of the tools available to biologists to extract biologically relevant information from image datasets and has been applied to a diverse range of organisms. The application of motion analysis during early development presents a challenge, as embryos often exhibit complex, subtle and diverse movement patterns. A method of motion analysis able to holistically quantify complex embryonic movements could be a powerful tool for fields such as toxicology and developmental biology to investigate whole organism stress responses. Here we assessed whether motion analysis could be used to distinguish the effects of stressors on three early developmental stages of each of three species: (i) the zebrafish Danio rerio (stages 19 h, 21.5 h and 33 h exposed to 1.5% ethanol and a salinity of 5); (ii) the African clawed toad Xenopus laevis (stages 24, 32 and 34 exposed to a salinity of 20); and iii) the pond snail Radix balthica (stages E3, E4, E6, E9 and E11 exposed to salinities of 5, 10 and 15). Image sequences were analysed using Sparse Optic Flow and the resultant frame-to-frame motion parameters were analysed using Discrete Fourier Transform to quantify the distribution of energy at different frequencies. This spectral frequency dataset was then used to construct a Bray-Curtis similarity matrix and differences in movement patterns between embryos in this matrix were tested for using ANOSIM

Moderate reductions in dissolved oxygen may compromise performance in an ecologically-important estuarine invertebrate

Coastal ecosystems, including estuaries, are increasingly pressured by expanding hypoxic regions as a result of human activities such as increased release of nutrients and global warming. Hypoxia is often defined as oxygen concentrations below 2 mL O2 L−1. However, taxa vary markedly in their sensitivity to hypoxia and can be affected by a broad spectrum of low oxygen levels. To better understand how reduced oxygen availability impacts physiological and molecular processes in invertebrates, we investigated responses of an estuarine amphipod to an ecologically-relevant level of moderate hypoxia (~2.6 mL O2 L−1) or severe hypoxia (~1.3 mL O2 L−1). Moderate hypoxia elicited a reduction in aerobic scope, and widespread changes to gene expression, including upregulation of metabolic genes and stress proteins. Under severe hypoxia, a marked hyperventilatory response associated with maintenance of aerobic performance was accompanied by a muted transcriptional response. This included a return of metabolic genes to baseline levels of expression and downregulation of transcripts involved in protein synthesis, most of which indicate recourse to hypometabolism and/or physiological impairment. We conclude that adverse ecological effects may occur under moderate hypoxia through compromised individual performance and, therefore, even modest declines in future oxygen levels may pose a significant challenge to coastal ecosystems