Listening In on the Past: What Can Otolith d 18 O Values Really Tell Us about the Environmental History of Fishes? Audrey M. Darnaude 1,2 *, Anna Sturrock 2,3 , Clive N. Trueman 3 , David Mouillot 1 , EIMF 4 *, Steven E. Campana 5 , Ewan Hunter 2 1 UMR CNRS-UM2-UM1-IFREMER-IRD 5119 Ecologie des Syste `mes Marins Co ˆ tiers, Montpellier 2 University, Montpellier, France, 2 Centre for Environment, Fisheries and Aquaculture Science, Lowestoft Laboratory, Lowestoft, United Kingdom, 3 Ocean and Earth Science, National Oceanography Centre, University of Southampton, Southampton, United Kingdom, 4 Edinburgh Ion Microprobe Facility, School of GeoSciences, University of Edinburgh, Edinburgh, United Kingdom, 5 Population Ecology Division, Bedford Institute of Oceanography, Dartmouth, Canada Abstract Oxygen isotope ratios from fish otoliths are used to discriminate marine stocks and reconstruct past climate, assuming that variations in otolith d 18 O values closely reflect differences in temperature history of fish when accounting for salinity induced variability in water d 18 O. To investigate this, we exploited the environmental and migratory data gathered from a decade using archival tags to study the behaviour of adult plaice (Pleuronectes platessa L.) in the North Sea. Based on the tag-derived monthly distributions of the fish and corresponding temperature and salinity estimates modelled across three consecutive years, we first predicted annual otolith d 18 O values for three geographically discrete offshore sub-stocks, using three alternative plausible scenarios for otolith growth. Comparison of predicted vs. measured annual d 18 O values demonstrated .96% correct prediction of sub-stock membership, irrespective of the otolith growth scenario. Pronounced inter-stock differences in d 18 O values, notably in summer, provide a robust marker for reconstructing broad-scale plaice distribution in the North Sea. However, although largely congruent, measured and predicted annual d 18 O values of did not fully match. Small, but consistent, offsets were also observed between individual high-resolution otolith d 18 O values measured during tag recording time and corresponding d 18 O predictions using concomitant tag-recorded temperatures and location-specific salinity estimates. The nature of the shifts differed among sub-stocks, suggesting specific vital effects linked to variation in physiological response to temperature. Therefore, although otolith d 18 O in free-ranging fish largely reflects environmental temperature and salinity, we counsel prudence when interpreting otolith d 18 O data for stock discrimination or temperature reconstruction until the mechanisms underpinning otolith d 18 O signature acquisition, and associated variation, are clarified. Citation: Darnaude AM, Sturrock A, Trueman CN, Mouillot D, EIMF, et al. (2014) Listening In on the Past: What Can Otolith d 18 O Values Really Tell Us about the Environmental History of Fishes? PLoS ONE 9(10): e108539. doi:10.1371/journal.pone.0108539 Editor: Heather Patterson, Department of Agriculture, Australia Received January 22, 2014; Accepted August 30, 2014; Published October 3, 2014 Copyright: ß 2014 Darnaude et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: Funders for this work were: (1) European Commission Marie-Curie Intra-European Fellowship Program (MEIF-CT-2003-501391 PlaiceLifeline, EU, 2004- 2005), (2) Natural Environment Research Council (DEFRA contracts MF0152 "Validation and testing of biologically-based movement models for North Sea plaice and implementation in management and assessment", 2003-2007 and DEFRA contract M1102 "Macro-ecology of marine finfish in UK waters", 2007-2012). No additional external funding was received for this study. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * Email: audrey.darnaude@univ-montp2.fr (AMD); jcraven@staffmail.ed.ac.uk (John A. Craven) Introduction Ecological studies in offshore marine ecosystems are often complicated by a lack of information describing the ambient environmental conditions habitually experienced by resident populations. Natural proxies that indirectly record the environ- mental conditions experienced by marine organisms, such as the isotopic ratio of oxygen in biogenic carbonates (expressed as d 18 O values) are therefore particularly valuable for providing long-term ecological insights into marine environments [1]. The isotopic composition of oxygen in biogenic carbonates is influenced by both temperature and the isotopic composition of the ambient water [2]. However, because water d 18 O signature is primarily salinity dependent, it is assumed to remain effectively constant in offshore water masses [3], where the d 18 O values of organisms’ calcified structures is gaining increasing recognition as a proxy for temperature [1]. Since the pioneering study of [4], the isotopic composition of oxygen in fish otoliths (‘‘ear-stones’’) has thus been commonly applied as a proxy for seawater temperature both by ecologists (e.g. [5–7]) and paleontologists (e.g. [8–11]). Otoliths are calcified structures located within the inner ears of teleost fish [12] which grow continuously from birth, forming seasonal accretion increments whose chemical composition reflects ambient water characteristics at the time of deposition, at least for some elements and isotopes [13]. Because otolith material is not resorbed or physiologically altered [12], otoliths offer natural data storage, providing a retrospective, temporally resolved record of lifetime environmental history through their structure and chemistry, often more detailed than the other calcified structures commonly used in aquatic ecology or paleontology [8,14]. The universal presence of teleost fish in aquatic ecosystems, and the ubiquity of otoliths in the fossil record from the late Cretaceous to present [15], gives otoliths enormous potential value in interpret- ing past environmental conditions and understanding current PLOS ONE | www.plosone.org 1 October 2014 | Volume 9 | Issue 10 | e108539