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Ecologia D'ostracodes Ecologia d’ostracodes simbionts (Entocytheridae) de carrancs invasors a Europa Tesi doctoral Alexandre Mestre Pérez Ecologia d’ostracodes simbionts (Entocytheridae) de carrancs invasors a Europa Ecology of symbiotic ostracods (Entocytheridae) inhabiting invasive crayfish in Europe Tesi doctoral 2014 Alexandre Mestre Pérez Departament de Microbiologia i Ecologia Universitat de València Programa de Doctorat en Biodiversitat i Biologia Evolutiva 2014 Ecologia d’ostracodes simbionts (Entocytheridae) de carrancs invasors a Europa Doctorand: Alexandre Mestre Pérez Directors: Francesc Mesquita Joanes Juan Salvador Monrós González La imatge de la portada està composada a partir de la foto d’un carranc de riu americà Pacifas- tacus leniusculus i una foto al microscopi electrònic (feta per Burkhard Scharf) d’una còpula d’ostracodes entocitèrids pertanyents a l’espècie Uncinocythere occidentalis, la qual s’ha tro- bat associada a poblacions exòtiques europees de P. leniusculus en aquest treball. Tesi presentada per Alexandre Mestre Pérez per optar al grau de Doctor en Biologia per la Universitat de València. Firmat: Alexandre Mestre Pérez Tesi dirigida pels doctors Francesc Mesquita Joanes Juan Salvador Monrós González Professors titulars d’Ecologia Universitat de València Firmat: Francesc Mesquita Joanes Firmat: Juan S. Monrós González Aquest treball ha estat finançat per un projecte del Ministeri de Ciència i In- novació (ECOINVADER, CGL2008-01296/BOS) i una beca predoctoral ("Cinc Segles") de la Universitat de València. A ma mare, a mon pare i al meu germà Agraïments Em considere molt afortunat i estic molt agraït d’haver gaudit, durant el llarg camí d’aprenentatge que representa la tesi, d’unes condicions excel lents per poder · desenvolupar aquest treball. En primer lloc, he tingut dos directors, Francesc Mesquita i Juan Monrós, que han sabut conduir-me, baix el meu punt de vista, d’una manera molt encertada, marcant-me molt bé el camí a seguir i, al mateix temps, donant-me marge de llibertat per desenvolupar idees pròpies. He d’agrair als dos la confiança que han tingut en mi, sobretot Juan que, des de que el conec, sempre m’ha recolzat en la investigació, i em va motivar per iniciar la tesi. També vull agrair els coneixements que m’han aportat els dos sobre totes les fases de la investigació i el seu esforç per donar a aquest treball la millor qualitat possible. En referència al darrer aspecte, he de destacar a Francesc Mesquita que, amb molta paciència, m’ha ajudat a resoldre infinitats de dubtes i m’ha ensenyat a ser millor investigador. I què dir dels companys del departament? Laia Zamora, Olivier Schmit, Josep Antoni Aguilar, Andreu Escrivà, Andreu Castillo, Lluis Valls, Carla Olmo, Maria Antón, Juan Rueda, Jose Antonio Gil-Delgado, Antonio Sanz, Javi Armengol, Romina Liberto i Susana Romo; tots ells m’han ajudat d’alguna o altra manera, en tasques de mostreig o de laboratori, consells tècnics, proveïment d’espai de treball o material, recolzament anímic o bé, simplement, m’han fet la vida laboral en el departament més plaent amb la seua companyia, gràcies a tot(e)s!. Per la seua implicació més directa, vull agrair especialment a Josep Antoni Aguilar, Jose Antonio Gil-Delgado, Juan Rueda i Andreu Castillo la seua contribució a la tesi. Ma tia, Alexandra Pérez, que és una artista, em va ajudar amb el disseny de la portada. Vull donar les gràcies als meus dos tutors d’estada a la LSU i a la Universitat de Sheffield, per haver-me acollit i haver-me ajudat en tot el que vaig necessitar: Bill Kelso and Roger Butlin, thank you very much! També agraesc als tècnics del TAB LAB de Sheffield, Andy Kruppa i Gavin Horsburgh, la seua gran ajuda i assessorament, d’ells vaig aprendre moltíssim. He de fer menció a tota la gent que va contribuir a la meua adaptació a la vida en Sheffield: Juan Galindo, Maria vii AGRAÏMENTS José Rivas, Yung Wa Sin, Camille Jan, Nicolas Santkin, Ricardo Romero, Daniel Leocadio, Pawel Lee, Julián Merino, Virginia Loza, Mauricio Carter, Paz Durán, Steeves Buckland, Charilaos Pilides, Emma Morley i Laura Brettell. I el mateix he de dir de la gent de Baton Rouge: Robert Romaire, Mike Kaller, Will Sheftal i Allison McKiernan, Chris Bonvillain, Kevin kyle, Charlie Brown, Noel Novelo, Kouassi Da Costa, Rafael Cuevas, Mauricio Toscano, Washington da Silva (and the rest of members of my soccer team). moltes gràcies a tot(e)s vosaltres. Una cosa que m’ha sorprès molt gratament de la tesi ha sigut la predisposició que ha tingut molta gent d’altres institucions a col laborar en la nostra inves- · tigació: David Baldry, Husamettin Balkis, Joan Carles Casanova, Adam Ellis, Karsten Grabow, Göran Klobuˇcar, Antonín Kouba, Sergi López, Ivana Maguire, Andreas Martens, Aysegül Mülayim, Alex Ribas, Burkhard Scharf, Menno Soes. Moltes gràcies a tot(e)s vosaltres. Agraesc, també, el suport dels governs de les comunitats autònomes de Andalucía, Extremadura, Castilla La Mancha, Castilla León, Navarra, Aragó, Illes Balears, Catalunya i el Pais Valencià, a l’hora de proporcionar-nos els permisos necessaris per mostrejar, al ministeri de Ciència i Innovació, per haver contribuït al finançament d’aquest treball, a través del Projecte ECOINVADER (CGL2008-01296/BOS), i a la Universitat de València, per la beca predoctoral que em va concedir. Finalment, vull concloure aquest apartat, com no, destacant el suport de la meua família, que m’han demostrat sempre estar al meu costat. viii Resum Els entocitèrids són una família d’ostracodes (Crustacea), majoritàriament d’origen americà, ectosimbionts (bàsicament comensals) d’altres crustacis, principalment decàpodes d’aigua dolça. Les darreres dècades, els carrancs natius europeus s’han vist perjudicats per la inva- sió de carrancs exòtics, degut a fenòmens d’exclusió competitiva i transmissió de simbionts parasitaris. En la present tesi, hem avaluat la presència d’entocitèrids associats a carrancs de riu (natius i exòtics) a Europa. Hem contribuït a sentar unes bases bibliogràfiques i metodològiques per a l’estudi dels entocitèrids. S’ha analitzat l’especificitat d’hoste d’En- tocytheridae i el patró latitudinal de riquesa de les espècies americanes del grup. També hem estudiat els factors abiòtics i biòtics que afecten la distribució i els paràmetres pobla- cionals d’un entocitèrid exòtic. Finalment, hem testat la transmissió d’entocitèrids exòtics a carrancs de riu europeus sota condicions experimentals. Per primera vegada, hem regis- trat la presència a Europa de dues espècies d’entocitèrids exòtics (Ankylocythere sinuosa i Uncinocythere occidentalis) associats a carrancs de riu invasors d’origen americà (Procam- barus clarkii i Pacifastacus leniusculus). Hem aportat una base de dades georeferenciada d’escala global d’accés lliure i gratuït per a la comunitat científica, els llistats actualitzats de les espècies i la bibliografia del grup, i informació pràctica per l’establiment de protocols de mostreig d’entocitèrids. Hem pogut constatar que l’especialització en una única espècie d’hoste no és majoritària en els entocitèrids. D’altra banda, els entocitèrids americans mos- tren un patró inhabitual de distribució de riquesa d’espècies amb la latitud, probablement, relacionat amb el vincle evolutiu amb els seus hostes. El nostre model de simbiont, A. sinuo- sa, suposadament no parasitari, s’ajustà a tres patrons generals en ecologia de poblacions de macroparàsits, suggerint que algunes regles poblacionals establertes en paràsits podrien ser regles més generals dels simbionts. Les poblacions exòtiques d’ A. sinuosa es veieren marca- dament afectades per les condicions climàtiques i limnològiques, mostrant que alguns grups particulars de simbionts poden ser especialment sensibles a la variabilitat ambiental, per exemple els ectosimbionts d’aigua dolça no parasitaris, com els entocitèrids. D’acord amb els nostres resultats, l’expansió d’un simbiont exòtic com A. sinuosa podria veure’s afectada per filtres espacials restrictius deguts a limitacions climàtiques del simbiont, els quals im- plicarien la pèrdua del simbiont en aquelles àrees envaïdes per l’hoste afectades pels filtres. Finalment, hem confirmat la transmissió de l’entocitèrid exòtic, A. sinuosa, a un carranc de riu natiu europeu, sota condicions experimentals. Per tant, seria convenient avaluar experi- mentalment el grau d’amenaça real per a la conservació del carranc europeu que suposaria l’esdeveniment en cas d’ocórrer en la natura. ix Resumen Los entocitéridos son una familia de ostrácodos (Crustacea), mayoritariamente de origen americano, ectosimbiontes (básicamente comensales) de otros crustáceos, principalmente decápodos de agua dulce. Durante las últimas décadas, los cangrejos de río nativos europeos se han visto perjudicados por la invasión de cangrejos exóticos, debido a fenómenos de ex- clusión competitiva y transmisión de simbiontes parasitarios. En la presente tesis, hemos evaluado la presencia de entocitéridos asociados a cangrejos de río (nativos y exóticos) en Eu- ropa. Hemos contribuido a sentar unas bases bibliográficas y metodológicas para el estudio de los entocitéridos. Se han analizado la especificidad de hospedador de los Entocytheridae y el patrón latitudinal de riqueza del grupo. También hemos estudiado los factores abióticos y bióticos que afectan a la distribución y los parámetros poblacionales de un entocitérido exó- tico. Finalmente, hemos testado la transmisión de entocitéridos exóticos a cangrejos de río europeos bajo condiciones experimentales. Por primera vez, hemos registrado la presencia en Europa de dos especies
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