Natural geochemical markers reveal environmental history and population royalsocietypublishing.org/journal/rsif connectivity of common cuttlefish in the Atlantic Ocean and Mediterranean Sea Research Jay R. Rooker1, R. J. David Wells1, Piero Addis2, Haritz Arrizabalaga3, Miguel Baptista4, Giovanni Bearzi5, Michael A. Dance6, Igaratza Fraile3, Cite this article: Rooker JR et al. 2020 7 1 8 Natural geochemical markers reveal Thomas Lacoue-Labarthe , Jessica M. Lee , Persefoni Megalofonou , environmental history and population Rui Rosa4, Ignacio Sobrino9, António V. Sykes10 and Roger Villanueva11 connectivity of common cuttlefish in the 1Department of Marine Biology, Texas A&M University, 1001 Texas Clipper Road, Galveston, TX 77553, USA Atlantic Ocean and Mediterranean Sea. 2Department of Environmental and Life Science, University of Cagliari, Via Fiorelli 1, 09126 Cagliari, Italy J. R. Soc. Interface 17: 20200309. 3AZTI, Marine Research, Basque Research and Technology Alliance (BRTA), Herrera Kaia, Portualdea z/g, http://dx.doi.org/10.1098/rsif.2020.0309 20110 Pasaia – Gipuzkoa, Spain 4MARE - Marine and Environmental Sciences Centre, Laboratório Marítimo da Guia, Faculdade de Ciências, Universidade de Lisboa, Lisboa, Avenida Nossa Senhora do Cabo 939, 2750-374 Cascais, Portugal 5Dolphin Biology and Conservation, Cordenons, Pordenone, Italy 6Department of Oceanography and Coastal Sciences, Louisiana State University, 2255 Energy, Coast and Received: 29 April 2020 Environment Building, Baton Rouge, LA 70803, USA Accepted: 7 July 2020 7Littoral Environnement et Sociétés (LIENSs) - UMR 7266 Bâtiment ILE, 2, rue Olympe de Gouges, 17000 La Rochelle, France 8Department of Biology, National and Kapodistrian University of Athens,15784 Athens, Greece 9Instituto Español de Oceanografía, Puerto Pesquero s/n, 11006, Cádiz, Spain 10Center of Marine Sciences, Universidade do Algarve Campus de Gambelas, 8005-139 Faro, Portugal Subject Category: 11Institut de Ciències del Mar (CSIC), Passeig Maritim 37-49, 08003 Barcelona, Spain Life Sciences–Chemistry interface JRR, 0000-0002-5934-7688; RJDW, 0000-0002-1306-0614; IS, 0000-0001-9747-017X; AVS, 0000-0002-5207-0612; RV, 0000-0001-8122-3449 Subject Areas: environmental science, biogeochemistry Natural markers (δ13Candδ18O stable isotopes) in the cuttlebones of the European common cuttlefish (Sepia officinalis) were determined for individuals Keywords: collected across a substantial portion of their range in the Northeast Atlantic Ocean (NEAO) and Mediterranean Sea. Cuttlebone δ13Candδ18Owerequanti- cephalopod, migration, cuttlefish, fied for core and edge material to characterize geochemical signatures geochemistry, population structure associated with early ( juvenile) and recent (sub-adult/adult) life-history periods, respectively. Regional shifts in cuttlebone δ13Candδ18Ovalueswere detected across the 12 sites investigated. Individuals collected from sites in δ13 δ18 Author for correspondence: the NEAO displayed more enriched Cand O values relative to sites in the Mediterranean Sea, with the latter also showing salient differences in Jay R. Rooker both markers among western, central and eastern collection areas. Classification e-mail: [email protected] success based on cuttlebone δ13Candδ18O values to four geographical regions Downloaded from https://royalsocietypublishing.org/ on 07 May 2021 (NEAO, western, central and eastern Mediterranean Sea) was relatively high, suggesting that environmental conditions in each region were distinct and pro- duced area-specific geochemical signatures on the cuttlebones of S. officinalis. A modified δ13Candδ18O baseline was developed from sites proximal to the Strait of Gibraltar in both the NEAO and Mediterranean Sea to assess potential mixing through this corridor. Nearly, all (95%) of δ13Candδ18O signatures of S. officinalis collected in the area of the NEAO closest to the Strait of Gibraltar (Gulf of Cadiz) matched the signatures of specimens collected in the western Mediterranean, signifying potential movement and mixing of individuals through this passageway. This study extends the current application of these geochemical markers for assessing the natal origin and population connectivity of this species and potentially other taxa that inhabit this geographical area. Electronic supplementary material is available online at https://doi.org/10.6084/m9.figshare. c.5073446. © 2020 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited. 2 45° N royalsocietypublishing.org/journal/rsif 40° N 35° N J. R. Soc. Interface 30° N 10° W 0° 10° E 20° E 30° E Figure 1. Map of collection sites (n = 12) for Sepia officinalis in the Northeast Atlantic Ocean and Mediterranean Sea. Sites grouped into four major geographical 17 areas: Northeast Atlantic Ocean, NEAO (Bay of Biscay to Gulf of Cadiz), western Mediterranean Sea, W-MED (Alboran Sea to Balearic Sea), central Mediterranean Sea, : 20200309 C-MED (Ligurian Sea to Adriatic Sea), eastern Mediterranean Sea, E-MED (Ionian Sea to Aegean Sea). Yellow symbol (diamond) indicates the collection region in close proximity to the Strait of Gibraltar (Gulf of Cadiz) that was used to assess potential movement of individuals between the NEAO and W-MED. 1. Background tool for predicting the natal origin, movement and population connectivity of cuttlefish [14]. The European common cuttlefish (Sepia officinalis) is an impor- The aim of the present study was to characterize regional tant fishery resource throughout the Mediterranean Sea and variation in the geochemistry of cuttlebones of S. officinalis adjacent waters of the Northeast Atlantic Ocean (NEAO) across a large section of its range in the NEAO and Mediterra- [1,2]. Due to large temporal shifts in the abundance and recruit- nean Sea. A common class of natural markers (stable C and O ment of S. officinalis, particularly for high-yield fisheries in isotope ratios) was employed to determine whether distinct certain areas (e.g. English Channel, Bay of Biscay [1]), there is geochemical gradients exist within the Mediterranean Sea and renewed interest in their movement ecology and population areas outside this basin in the NEAO. We quantified δ13Cand connectivity [3]. This is primarily due to the fact that δ18O values for core and edge portions of the cuttlebone to con- spatio-temporal shifts in distribution of marine organisms, trast signatures and regional discrimination of habitats used particularly spawning stock biomass (SSB), can have profound during early (natal) and recent (time of collection) life-history implications for the management of harvested fisheries [4]. periods, respectively. Multiple locations were sampled within Current knowledge on the movement of S. officinalis is limited, each of four major geographical regions investigated (NEAO preventing the implementation of conservation measures (e.g. and western, central, and eastern Mediterranean Sea), and – time area closures) for protecting highly suitable habitat or key regional discrimination (classification success) was determined areas used by spawning adults. Several different approaches for both cuttlebone core and edge signatures. We then used have been used to clarify the movements and home range of δ13 δ18 cuttlebone core ( CCORE and OCORE) values to predict the S. officinalis, including conventional tagging [5], acoustic teleme- natal origin of sub-adult/adult S. officinalis collected from a try [6] and spatial shifts in catch from fishery-dependent data potential mixing area at the juncture between the NEAO [7]. More recently, Dance et al. [8] used natural tracers in cuttle- and Mediterranean Sea. The spatial configuration of distinct bones to investigate small-scale habitat shifts of this species in Downloaded from https://royalsocietypublishing.org/ on 07 May 2021 geochemical provinces within areas investigated provides the Adriatic Sea. While earlier studies have shed important important insights into the suitability of these natural markers light on the habitat use and movement of S. officinalis,expand- for addressing related ecological questions (ontogenetic habitat ing the geographical scope of our knowledge on population shifts) as well as population connectivity within the NEAO and connectivity is critical to their management. Mediterranean Sea. Cuttlefish (class Cephalopoda) are characterized by the presence of an aragonitic internal shell (cuttlebone), and this gas-filled structure serves as a buoyancy control mechan- ism [9–11]. Similar to other biogenic carbonates found in 2. Methods cephalopods (statoliths) and fishes (otoliths), these aragonitic structures accrete material in a predictable manner and the Sepia officinalis were collected between February 2013 and February 2014 across several locations in the NEAO and Mediterranean Sea, microstructure retains information that records the timing with samples falling into four major geographical regions: NEAO of deposition [12]. In addition, the chemistry of material [Bay of Biscay to Gulf of Cadiz], western Mediterranean Sea, accreted in cuttlebones and other biogenic carbonates reflects W-MED [Alboran Sea to Balearic Sea], central Mediterranean, ambient elemental or isotopic concentrations in seawater, and C-MED [Ligurian Sea to Adriatic Sea], eastern Mediterranean, thus serve as natural markers for retrospective determination E-MED [Ionian Sea to Aegean Sea]