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Margaritifera Auricularia (Spengler, 1793) in France

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Margaritifera Auricularia (Spengler, 1793) in France UNIVERSITÉ DE TOURS ÉCOLE DOCTORALE « Sciences de la société : Territoires, Économie, Droit » UMR CNRS 7324-CITERES UNIVERSIDAD AUTÓNOMA DE MADRID FACULTAD DE BIOLOGIA THÈSE présentée par : Joaquín SOLER GIRBES soutenue le : 20 décembre 2018 pour obtenir le grade de : Docteur de l’université de Tours Discipline/ Spécialité : Sciences de l’Environnement/Ecologie et el título de Doctor en BIOLOGÍA por la Universidad Autónoma de Madrid Conservation ecology of Margaritifera auricularia (Spengler, 1793) in France THÈSE co-dirigée par : M. WANTZEN Karl Matthias Professeur et Chaire UNESCO, Université de Tours M. ARAUJO Rafael Docteur, Museo de Ciencias Naturales-CSIC, Madrid, Espagne RAPPORTEURS : M GEIST Jürgen Professeur, Technische Universität München, Allemagne Mme. ONDINA Paz Professeur, Universidad de Santiago de Compostela, Espagne JURY : M. ARAUJO Rafael Docteur, Museo de Ciencias Naturales-CSIC, Madrid, Espagne Mme. BAUDRIMONT, Magali Professeur, Université de Bordeaux M. GEIST Jürgen Professeur, Technische Universität München, Allemagne Mme. ONDINA Paz Professeur, Universidad de Santiago de Compostela, Espagne M. PINCEBOURDE Sylvain Professeur, Université de Tours M. WANTZEN Karl Matthias Professeur et Chaire UNESCO, Université de Tours Acknowledgments/Remerciements This work would not have been possible without the help of countless people to whom I would like to express my sincere gratitude here. To Rafael Araujo for co-directing this thesis and for supporting me during all phases of this work. Thank you for everything you have taught me about freshwater mussels and for giving me the opportunity to resume research. Thank you for hosting me at the Museum and, above all, thank you for your friendship. To Matthias Wantzen for co-directing this thesis and giving me the opportunity to do it. Thank you very much for sharing your extensive knowledge in fluvial ecology. Thank you for your support, for the discussions and suggestions and for your contagious enthusiasm. To Ángel Luque, for being my thesis tutor at the Universidad Autónoma de Madrid. For all your efforts and advice. This thesis has been sponsored by the LIFE Project 'LIFE13 BIO / FR / 001162 Conservation of the Giant Pearl Mussel in Europe'. The technical and personal resources were financed by this project and the thesis corresponds to a large extent to the research outlined in the project proposal. Thank you to Nina Richard, Laure Morisseau, Yann Guerez and all the people who, despite the difficulties, have made it possible. Especially many thanks to Philippe Jugé. Without him I would not have been able to survive the troubled waters. Thank you for your moral support and for your friendship, and also thanks for your commitment in the work and for all the technical solutions and great ideas, of which this thesis is largely indebted. Many thanks also to Carmen Jugé for her hospitality and sympathy. This thesis has been provided under the auspices of the UNESCO Chair "Fleuves et Patrimoine (River Culture)" by Karl M. Wantzen. Thanks also to UMR CITERES for hosting the project and supporting this thesis. Thanks to the University of Tours and especially to Veronica Serrano, and Stephanie Gosset for their support. To the Museo Nacional de Ciencias Naturales de Madrid to welcome me and especially to all the friends who have made me feel at home: Bea, Javi, Lola, Annie, Iván, Violeta, David, "la prima", Paula, Óscar, Jesús , Pepe, Marian, Mario, Anna, Victoria, Carolina, Nacho and many others. 3 I also want to show my gratitude to the researchers that I have met throughout this thesis and from whom I have learned many interesting things. Thanks to Catherine Boisneau of the University of Tours for sharing with me her extensive knowledge of freshwater fish and Michele de Monte for your availability and help. To Stephane Rodrigues and Coraline Wintenberger for their guidance on fluvial sedimentology and for their hospitality. Thanks to Jürgen Geist, Bernhard Stoeckle and the rest of the members of the Molecular Biology laboratory of the Aquatische Systembiologie chair of the Technical University of Munich for their wonderful welcome and enthusiastic collaboration. Thanks to all the freshwater mussel conservation programs that I had the good fortune to visit in Lugo, Zaragoza, Banyoles and Brittany for opening their doors and teaching me the ins and outs of captive breeding. To Paz, Catuxa, Keiko, Marie and Pierre Yves for sharing your experience. Thanks to Miquel, Carles, Gerard, Ramón and the rest of the team for how much I learned and for making my stay in Banyoles one of the most beautiful moments of this time. Thanks to all the people who have participated in the fieldwork. To the members of Gemosclera and the Club Plongé of Chinon for having collaborated selflessly in the samplings, most of the time under harsh and dangerous conditions. To the team of Logrami, Biotope and of the Fishing Federations that collaborated in the electrofishing surveys and to Vienne Nature and Valentin Viennot that helped me in the Vienne and Creuse surveys. Thanks to Ana, Yannick and Paula for reviewing parts of the manuscripts. And to all the friends that have made my stay in Tours an unforgettable experience: "el berberecho", Eli, Pili, Jean Baptiste, Serena, Lillo, Edu, Laura, Edu, Maria Angeles, Romeo, Frederic, Helena, Tierry, Kity, Dom, Paloma, Diego, Alex, los Mata and many other Spanish and Italian expatriate friends in Tours. Thanks also to Sam, los Flakis and the Berthom brothers. To my family, because without them I would not know how to explain myself and especially my sister and my parents, who have taught me to persevere and believe that a better and fairer world is possible. The last words of thanks are for Bea. Without your love I could not have gotten here. Thank you for having accompanied me during a good part of my life, and for all your support and patience during this thesis period. 4 Abstract Among the many victims of global biodiversity loss in the Anthropocene, the giant freshwater pearl mussel Margaritifera auricularia is one of the most endangered species. Originally occurring in many European rivers, M. auricularia is a relict species now restricted to a few ageing population in France and Spain, in which natural reproduction is almost absent. The general goal of this thesis was to improve the knowledge of the conservation status of the M. auricularia French populations, their reproductive biology and the early life stages of the species. Despite harboring approximately 90% of the world population, these French populations have been little studied before. To achieve these objectives, the bibliography and museum collections were revised and the populations of the Charente, Vienne and Creuse rivers, considered the most important ones in France, were studied. On historical times, Margaritifera auricularia was present in the Rhine in France and Germany, the Seine and the Rhône in France, the Po in Italy and the Tagus in Spain, where the species is now believed to be extirpated. Today, M. auricularia is considered restricted to five watersheds in France and Spain (Loire, Charente, Garonne, Adour and Ebro), representing a range contraction of about a 90% in the last two centuries. Recruitment is very scarce in all populations although evidences of an important recent recruitment were found during the present study in the Vienne and Creuse rivers, constituting the most notable event of M. auricularia recent reproduction reported so far. The current lack of recruitment does not seem to be related to the infertility of the specimens. Ova and developing embryos were found throughout the month of March in the Charente and Creuse populations, and the beginning of glochidial release occurred in early to mid-April. Compared with the Spanish populations, the reproductive period begins some weeks later, likely due to differences in water temperature. Development from first cleavage to glochidial maturity took 25-37 days and the estimated number of larvae per gravid mussel was around 2,000,000. As the vast majority of freshwater mussel species, Margaritifera auricularia depends on fishes to host larvae until their metamorphosis into juveniles. The discovery of three new host species (Gasterosteus aculeatus, Petromyzon marinus and the exotic Silurus glanis) increases the number of known physiological hosts to eight species from five different families, indicating that M. auricularia has a more host generalist behavior than previously expected. This is the 5 first time that a lamprey has been tested and used as a possible host for a freshwater bivalve belonging to the Unionoida Order. The potential use of Petromyzon marinus to reinforce M. auricularia populations along its entire geographic range may help to counteract the decline of the species. All currently known Margaritifera auricularia hosts have a notable tolerance to salinity. This pattern could have arisen early in its evolution because of the potential advantage for dispersion that diadromous species confer. However, anthropogenic causes, such as dam construction and degradation of water quality and habitat, have led to a severe decline of most migratory fish species in Europe during the last two centuries. Although other causes may have contributed to the overall decline of M. auricularia, the loss of hosts seems to be a main factor. The utilization of M. auricularia by Rhodeus amarus, a cyprinid fish that spawns in the mantle cavity of freshwater mussels resulting in a fitness cost for the mussels, was also discovered in the present Thesis. The extensive expansion of this bitterling species, and the reduction in fitness that it could cause on mussels, may be problematic for species facing extinction risk especially in areas inhabited by spatially restricted mussel species. The juvenile breeding of Margaritifera auricularia is a difficult task and although the survival results are still very low, it seems that the use of an initial laboratory phase with the newborn juveniles reared in detritus boxes can offer more successful results than the direct cultivation of juveniles into raceways.
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