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Ligament, Hinge, and Shell Cross-Sections of the Atlantic Surfclam

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Ligament, hinge, and shell cross-sections of the Atlantic surfclam (Spisula solidissima): Promising marine environmental archives in NE North America Pierre Poitevin, Julien Thébault, Bernd R. Schoene, Aurelie Jolivet, Pascal Lazure, Laurent Chauvaud To cite this version: Pierre Poitevin, Julien Thébault, Bernd R. Schoene, Aurelie Jolivet, Pascal Lazure, et al.. Ligament, hinge, and shell cross-sections of the Atlantic surfclam (Spisula solidissima): Promising marine en- vironmental archives in NE North America. PLoS ONE, Public Library of Science, 2018, 13 (6), pp.e0199212. 10.1371/journal.pone.0199212. hal-02401178 HAL Id: hal-02401178 https://hal.archives-ouvertes.fr/hal-02401178 Submitted on 28 May 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. RESEARCH ARTICLE Ligament, hinge, and shell cross-sections of the Atlantic surfclam (Spisula solidissima): Promising marine environmental archives in NE North America Pierre Poitevin1*, Julien TheÂbault1, Bernd R. SchoÈne2, AureÂlie Jolivet3, Pascal Lazure4, Laurent Chauvaud1 a1111111111 1 Universite de Bretagne Occidentale, Laboratoire des Sciences de l'Environnement Marin (UMR6539 UBO/ CNRS/IRD/Ifremer), PlouzaneÂ, France, 2 Institute of Geosciences, University of Mainz, Johann-Joachim- a1111111111 Becher-Weg 21, Mainz, Germany, 3 TBM environnement/Somme, Technopole Brest-Iroise, PlouzaneÂ, a1111111111 France, 4 Ifremer, Laboratoire d'OceÂanographie Physique et Spatiale (UMR6523 CNRS/Ifremer/IRD/UBO), a1111111111 PlouzaneÂ, France a1111111111 * [email protected] Abstract OPEN ACCESS Citation: Poitevin P, TheÂbault J, SchoÈne BR, Jolivet The Atlantic surfclam (Spisula solidissima) is a commercially important species in North A, Lazure P, Chauvaud L (2018) Ligament, hinge, American waters, undergoing biological and ecological shifts. These are attributed, in part, and shell cross-sections of the Atlantic surfclam to environmental modifications in its habitat and driven by climate change. Investigation of (Spisula solidissima): Promising marine shell growth patterns, trace elements, and isotopic compositions require an examination of environmental archives in NE North America. PLoS ONE 13(6): e0199212. https://doi.org/10.1371/ growth lines and increments preserved in biogenic carbonates. However, growth pattern journal.pone.0199212 analysis of S. solidissima is challenging due to multiple disturbance lines caused by environ- Editor: Geerat J. Vermeij, University of California, mental stress, erosion in umbonal shell regions, and constraints related to sample size and UNITED STATES preparation techniques. The present study proposes an alternative method for describing Received: February 9, 2018 chronology. First, we analyzed growth patterns using growth lines within the shell and hinge. To validate the assumption of annual periodicity of growth line formation, we analyzed the Accepted: June 4, 2018 oxygen isotope composition of the outer shell layer of two specimens (46Ê54'20"N; 56Ê Published: June 14, 2018 18 18'58"W). Maximum δ Oshell values occurred at the exact same location as internal growth Copyright: © 2018 Poitevin et al. This is an open lines in both specimens, confirming that they are formed annually and that growth ceases access article distributed under the terms of the during winter. Next, we used growth increment width data to build a standardized growth Creative Commons Attribution License, which permits unrestricted use, distribution, and index (SGI) time-series (25-year chronology) for each of the three parts of the shell. Highly reproduction in any medium, provided the original significant correlations were found between the three SGI chronologies (p < 0.001; 0.55 < τ author and source are credited. < 0.68) of all specimens. Thus, ligament growth lines provide a new method of determining Data Availability Statement: All data files are ontogenetic age and growth rate in S. solidissima. In a biogeographic approach, the shell available from the Zenodo database (DOI: 10.5281/ growth performance of S. solidissima in Saint-Pierre and Miquelon was compared to those zenodo.1242929, 10.5281/zenodo.1242892, 10. 5281/zenodo.1242821). in other populations along its distribution range in order to place this population in a temporal and regional context. Funding: This work was supported by the EC2CO program MATISSE of the CNRS INSU, the Cluster of Excellence LabexMER, and the LIA BeBEST CNRS INEE. This research was carried out as part of the Ph.D. thesis of Pierre Poitevin for the University of Western Brittany with a French PLOS ONE | https://doi.org/10.1371/journal.pone.0199212 June 14, 2018 1 / 17 Spisula solidissima sclerochronology Ministry of Higher Education and Research grant. Introduction the funder (TBM environnement/Somme) provided support in the form of salaries for the author The Atlantic surfclam (Spisula solidissima) is the largest bivalve in the western North Atlantic, AureÂlie Jolivet (A.J.) and the specific roles of this reaching a maximum length of 226 mm (commercial minimum size: 120 mm in USA and 90 author are articulated in the "author contributions" mm in Canada) and longevity of 37 years in the Middle Atlantic Bight population [1]. S. soli- section. The funders had no role in study design, dissima is a commercially important species in Canada and the US Exclusive Economic Zone data collection and analysis, decision to publish, or (EEZ). The US fishery represents nearly 75% of Atlantic surfclam global landings between preparation of the manuscript. 1965 and 2011. In 2011, approximately 20 000 tons of Atlantic surfclam meats were landed, Competing interests: One author is affiliated with 93% of which came from the US EEZ, corresponding to nominal revenues of $29 million, mak- TBM environnement/Somme. This does not alter ing this fishery one of the most valuable single species fisheries in the US [2]. our adherence to all PLOS ONE policies on sharing data and materials. S. solidissima is a good example of a commercially important species undergoing biological and ecological changes that have been attributed to increased bottom water temperature, the fishery activity, or a combination of both [3±8]. These data are measured within the accretion- ary hard parts of the clam [9±11]. Shell growth, a variable that integrates multiple physical and biological factors, represents an integrative approach to monitoring the impact of environ- mental changes in S. solidissima populations along a geographic gradient during the last few decades [7, 12±14]. Previous studies have reported that S. solidissima is an aragonitic bivalve [15] that forms one growth line per year during fall [9]. Based on this observation, different methods have been used to measure growth rates in Atlantic surfclam shells, including the size distribution of single cohorts [16], analysis of growth increments following mark-and-recapture experiments using different labeling techniques [17], external shell growth line measurements [18], internal growth line analysis in shell cross-sections [1], and elemental and stable oxygen isotope analyses [19± 21]. However, disturbance rings caused by storms, thermal stress, predators, diseases, spawning, gonad development, and dredging are often indistinguishable from (periodic) annual growth lines, leading to unreliable results [9, 22]. Further limitations occur in older specimens, in which it is sometimes a bit more difficult to resolve the most recently formed growth lines and the umbonal region may be eroded. In addition, the cutting, polishing, and examination proce- dures are considered to be time-consuming [19]. In order to resolve some of these problems, [19] proposed another method for determining the age and growth rate using internal growth lines preserved in the chondrophore, a structure that is particularly well developed in members of the Mactridae family. This method, which was improved by John W. Ropes [23, 24], is still used every 2±3 years on surfclams sampled in the framework of the NEFSC clam surveys [2]. Although this method has solved the problems related to outer shell layer degradation and the time required, the problems related to disturbance lines persist [24]. The present study analyzed growth lines present in the outer layer of the shell and the chon- drophore and compared them to those readily observed in the internal ligament (resilium) of Atlantic surfclam shells. A strong relationship has been identified between growth patterns in the shell and ligament in several bivalve species, including Placopecten magellanicus, Pedum spondyloideum, Radiolites angeoides, and Crassostrea gigas [25±29]. S. solidissima has two phys- ically separated ligaments: a small external uncalcified ligament (tensilium) and a larger inter- nal partially calcified ligament (resilium) attached to the chondrophore [30]. In the rest of this article the hinge ligament refers to the elastic part composed of oriented aragonite crystals in a protein matrix that connects the shell valves dorsally (resilium). Our study focused on S. soli- dissima from Saint-Pierre
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