Earth-Science Reviews 169 (2017) 132–145 Contents lists available at ScienceDirect Earth-Science Reviews journal homepage: www.elsevier.com/locate/earscirev Invited review Shelled pteropods in peril: Assessing vulnerability in a high CO2 ocean ⁎ MARK Clara Mannoa, ,1, Nina Bednaršekb,1, Geraint A. Tarlinga, Vicky L. Pecka, Steeve Comeauc, Deepak Adhikarid, Dorothee C.E. Bakkere, Eduard Bauerfeindf, Alexander J. Bergang, Maria I. Berningh, Erik Buitenhuisi, Alice K. Burridgej,k, Melissa Chiericil, Sebastian Flöterm, Agneta Franssonn, Jessie Gardnera, Ella L. Howeso,p, Nina Keulq, Katsunori Kimotor, Peter Kohnerth, Gareth L. Lawsong, Silke Lischkas, Amy Maast, Lisette Mekkesj,k, Rosie L. Oakesu, Corinne Pebodyv, Katja T.C.A. Peijnenburgj,k, Miriam Seifertf, Jennifer Skinnerw, Patricia S. Thibodeaux, Deborah Wall-Palmery, Patrizia Ziveriz,aa a British Antarctic Survey, Natural Environmental Research Council, High Cross, Madingley Road, Cambridge, CB3 0ET, UK b University of Washington, Joint Institute for the Study of the Atmosphere and Ocean, 3737 Brooklyn Ave NE, Seattle, WA 98105, USA c The University of Western Australia, School of Earth and Environment, ARC Centre in Coral Reef Studies, Crawley, Western Australia 6009, Australia d School of Civil and Environmental Engineering, Georgia Institute of Technology, 790 Atlantic Drive, Atlanta, GA 30339, USA e Centre for Ocean and Atmospheric Sciences, School of Environmental Sciences, University of East Anglia, Norwich NR4 7TJ, UK f HGF-MPG Group for Deep Sea Ecology and Technology, Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany g Biology Department Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA h Zoologische Staatssammlung München, Münchhausenstr. 21, 81247 München, Germany i Tyndall Centre for Climate Change Research, School of Environmental Sciences, University of East Anglia, Norwich NR4 7TJ, UK j Naturalis Biodiversity Center, P.O. Box 9517, 2300 RA Leiden, The Netherlands k Institute for Biodiversity and Ecosystem Dynamics (IBED), University of Amsterdam, P.O. Box 94248, 1090 GE Amsterdam, The Netherlands l Institute of Marine Research, PO Box 6404, 9294 Tromsø, Norway m GEOMAR Helmholtz Centre for Ocean Research Kiel, Wischhofstr. 1-3D, 24148 Kiel, Germany n Norwegain Polar Institute, Fram Centre, 9296 Tromsø, Norway o Sorbonne Universités, UPMC Univ Paris 06, CNRS-INSU, Laboratoire d'Océanographie de Villefranche, 181 chemin du Lazaret, F-06230 Villefranche-sur-mer, France p Marine Biogeosciences, Alfred-Wegener-Institut Helmholtz-Zentrum für Polar- und Meeresforschung, Am Handelshafen 12, D-27570 Bremerhaven, Germany q Institute of Geosciences, Marine Climate Research, Christian-Albrechts-Universität zu Kiel, Ludewig-Meyn Str. 10, 24118 Kiel, Germany r Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Japan s GEOMAR Helmholtz Centre for Ocean Research Kiel, Düsternbroker Weg 20, 24105 Kiel, Germany t Bermuda Institute of Ocean Sciences, St. George's, Bermuda GE 01, Bermuda u Department of Geosciences, The Pennsylvania State University, University Park, PA 16802, USA v National Oceanography Centre, Southampton SO14 3ZH, UK w Sir Alister Hardy Foundation for Ocean Science, The Laboratory, Citadel Hill, Plymouth PL1 2PB, UK x Virginia Institute of Marine Science, College of William & Mary, Gloucester Pt., VA 23062, USA y School of Geography, Earth and Environmental Sciences, Plymouth University, Drake Circus, Plymouth PL4 8AA, UK z Institute of Environmental Science and Technology (ICTA), Autonomous University of Barcelona (UAB), 08193 Bellaterra, Catalan, Spain aa Institution for Research and Advanced Studies (ICREA), 08010 Barcelona, Pg. Lluís Companys 23, Spain ARTICLE INFO ABSTRACT Keywords: The impact of anthropogenic ocean acidification (OA) on marine ecosystems is a vital concern facing marine Euthecosomatous pteropods scientists and managers of ocean resources. Euthecosomatous pteropods (holoplanktonic gastropods) represent Ocean acidification an excellent sentinel for indicating exposure to anthropogenic OA because of the sensitivity of their aragonite Calcifying organisms shells to the OA conditions less favorable for calcification. However, an integration of observations, experiments Marine ecosystem and modelling efforts is needed to make accurate predictions of how these organisms will respond to future Carbonate chemistry changes to their environment. Our understanding of the underlying organismal biology and life history is far from complete and must be improved if we are to comprehend fully the responses of these organisms to the multitude of stressors in their environment beyond OA. This review considers the present state of research and understanding of euthecosomatous pteropod biology and ecology of these organisms and considers promising new laboratory methods, advances in instrumentation (such as molecular, trace elements, stable isotopes, ⁎ Corresponding author. E-mail address: [email protected] (C. Manno). 1 Both authors equally contributed to the text. http://dx.doi.org/10.1016/j.earscirev.2017.04.005 Received 22 August 2016; Received in revised form 31 March 2017; Accepted 7 April 2017 Available online 08 April 2017 0012-8252/ © 2017 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/BY-NC-ND/4.0/). C. Manno et al. Earth-Science Reviews 169 (2017) 132–145 palaeobiology alongside autonomous sampling platforms, CT scanning and high-quality video recording) and novel field-based approaches (i.e. studies of upwelling and CO2 vent regions) that may allow us to improve our predictive capacity of their vulnerability and/or resilience. In addition to playing a critical ecological and biogeochemical role, pteropods can offer a significant value as an early-indicator of anthropogenic OA. This role as a sentinel species should be developed further to consolidate their potential use within marine environmental management policy making. ff 1. Introduction tions, experiments and modelling. This demands a coordinated e ort from a wide range of disciplines throughout the international scientific Anthropogenic ocean acidification (OA) poses a serious, global community. threat to marine ecosystems and the services they provide. Its potential In June 2015, an international workshop was held at the British “ influence on marine fisheries has led to anthropogenic OA being Antarctic Survey in Cambridge to consider the Response of shelled ” increasingly appreciated as a pressing societal concern, and a top pteropods to OA . It was attended by scientists from biomechanical research priority (Rudd, 2014). Many international programmes and engineering, ocean carbonate chemistry, geology, palaeontology, bio- projects are now investigating the impacts of anthropogenic OA on geochemistry, taxonomy, physiology and ecology. The aim of the marine biodiversity and its wider implications. The international workshop was to consolidate progress made so far in pteropod research advisory groups IOC-UNESCO and OSPAR-ICES recommended that and to identify knowledge gaps and future research needs. future studies into marine ecosystems should focus on species that are Here, we present the outcomes from the workshop which consider particularly sensitive to anthropogenic OA since these species can indicate when and where the first impacts will occur. Continuous uptake of about a third of anthropogenically produced carbon dioxide (CO2) since 1750 (Le Quéré et al., 2015), combined with ocean warming and increased freshwater run-off in high latitude regions, are predicted to cause major changes in seawater chemistry. Anthropogenic carbon dioxide emissions induce OA, where pH and the concentration of carbonate ions decrease, resulting in shoaling of the Calcium Carbonate (CaCO3) saturation horizon (Feely et al., 2009). Ocean pH has already declined by 0.1 unit since pre-industrial times and is predicted to fall another 0.3 unit by 2100 (Caldeira and Wickett, 2003). These changes are likely to affect marine calcifiers, in turn altering biodiversity, trophic interactions and large-scale marine bio- geochemical processes (Fabry et al., 2008). Euthecosomatous pteropods (holoplanktonic shelled marine gastro- pods) have been identified as candidates for indicating the onset of anthropogenic OA, since the shells of species in the vulnerable polar and sub-polar regions have been demonstrated to be particularly prone to dissolution (Comeau et al., 2010a; Lischka and Riebesell 2012). Euthecosomatous pteropods are a cosmopolitan group widely distrib- uted in the world's oceans. They are otherwise known as “sea butterflies” because they flap their wing-like parapodia to “fly” through the water. Euthecosomatous shells are relatively small, ranging from less than a millimetre to a few centimetres in length (Lalli and Gilmer, 1989) and are made from aragonite, a metastable and relatively soluble form of biogenic CaCO3 (Mucci, 1983). Pteropods are an important ecological as well as biogeochemical component of the marine ecosys- tem. They are a major food source of carnivorous zooplankton, commercially exploited fishes, such as cod, salmon, herring, mackerel, and a number of higher predators, such as seabirds, polar cod and whales (Lalli and Gilmer, 1989; Hunt et al., 2008; Falk-Petersen et al., 2001). From a biogeochemical point of view, pteropods play an important role in the direct export of organic carbon and carbonate to the deep ocean through the sinking