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Assessment of Biological Invasions Phenomena in Reptiles of Mediterreanean Islands

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Assessment of Biological Invasions Phenomena in Reptiles of Mediterreanean Islands Assessment of biological invasions phenomena in reptiles of Mediterreanean islands: a biogeographic, genetic and ecological perspective. D Iolanda Raquel Silva Rocha Doutoramento em Biodiversidade, Genética e Evolução Departamento de Biologia 2018 Orientador Miguel A. Carretero, Professor Auxiliar e Investigador, Faculdade de Ciências, CIBIO/InBIO Universidade do Porto Coorientador Gentile Francesco Ficetola, Professor Associado e Investigador, University of Milano; LECA – Laboratoire d’Écologie Alpine (University Grenoble-Alpes) Coorientador Daniele Salvi, Professor Associado e Investigador, University of L’Aquila; CIBIO/InBIO (Universidade do Porto) Nota Previa´ Na elaborac¸ao˜ desta tese, e nos termos do numero´ 2 do Artigo 4 do Regulamento Geral dos Ter- ceiros Ciclos de Estudos da Universidade do Porto e do Artigo 31 do Decreto-Lei 74/2006, de 24 de Marc¸o, com a nova redac¸ao˜ introduzida pelo Decreto-Lei 230/2009, de 14 de Setembro, foi efe- tuado o aproveitamento total de um conjunto coerente de trabalhos de investigac¸ao˜ ja´ publicados ou submetidos para publicac¸ao˜ em revistas internacionais indexadas e com arbitragem cient´ıfica, os quais integram alguns dos cap´ıtulos da presente tese. Tendo em conta que os referidos trabalhos foram realizados com a colaborac¸ao˜ de outros autores, o candidato esclarece que, em todos eles, participou ativamente na sua concec¸ao,˜ na obtenc¸ao,˜ analise´ e discussao˜ de resultados, bem como na elaborac¸ao˜ da sua forma publicada. A instituic¸ao˜ de origem da candidata foi a Faculdade de Cienciasˆ da Universidade do Porto, tendo o trabalho sido realizado sob orientao do Doutor Miguel A. Carretero, Professor Auxiliar no Departamento de Biologia da Faculdade de Cienciasˆ da Univer- sidade do Porto e Investigador Principal do Centro de Investigac¸ao˜ em Biodiversidade e Recursos Geneticos´ (CIBIO-InBio) e sob co-orientac¸ao˜ do Doutor Daniele Salvi, Professor Associado na Uni- versidade de L’Aquila e Investigador do CIBIO/InBIO. A instituic¸ao˜ de acolhimento foi o Laboratoire d’Ecologie Alpine (LECA), sob a coorientac¸ao˜ do Professor Doutor Gentile Francesco Ficetola. O trabalho laboratorial foi realizado no CIBIO-InBio, no LECA e Serveis Cientifico-Tecnics` (University of Barcelona, Spain) Este trabalho foi apoiado pela Fundac¸ao˜ para a Cienciaˆ e Tecnologia (FCT) atraves´ da atribuic¸ao˜ da bolsa de doutoramento (SFRH/BD/95745/2013). i ii Acknowledgements After climbing this mountain, I have to acknowledge that I did not climb it alone. First, I have to thank to my every-day support Nuno Abreu who had nothing but patiente and love during all the long PhD road. I would like to thank my supervisors Miguel A. Carretero, Daniele Salvi and G. Francesco Ficetola for accepting me as their student and for all the help and advices through all these 4 years. Your knowledge, support and discussions allowed me to take this thesis to a safe port. I also have to thank my friends and colleagues from life, CIBIO/InBio and LECA. A special thanks for those who help me through the way either by discussing or supporting me, either by joking around and talk about nothing with me. Thank you, Joana Mendes and Alex Cortada, for all the fun and help during the fieldwork. Thank you, all the crew from Milan for the amazing fieldwork month. And the ones always present, my personal believers: ´Iris Sampaio, Vanessa Modesto, Patr´ıcia Lopes, Marisa Almeida, Beatriz Tome,´ Mafalda Ferreira, Alexandra Silva, Veronica´ Gomes, Ceres Barros, Joao˜ Braga, Joao˜ Maia and Telma Azevedo. Obrigado pai, Lu´ıs Rocha, e mae,˜ Alexandrina Rocha, por estarem sempre presentes e me apoiarem, sem reservas, as minhas aventuras. Vocesˆ sao˜ os melhores. I also would like to thank Fundac¸ao˜ para a Cienciaˆ e Tecnologia (FCT) for granting a PhD scholarship (SFRH/BD/95745/2013), under the Programa Operacional Potencial Humano - Quadro de Referenciaˆ Estrategico´ Nacional funds (POPH-QREN) from the European Social Fund (ESF) and Ministerio´ Portuguesˆ da Educac¸ao˜ e Ciencia.ˆ iii iv “How to get the best of it all? One must conquer, achieve, get to the top; one must know the end to be convinced that one can win the end - to know there’s no dream that mustn’t be dared. Is this the summit, crowning the day? How cool and quiet! We’re not exultant; but delighted, joyful; soberly astonished. Have we vanquished an enemy? None but ourselves. Have we gained success? That word means nothing here. Have we won a kingdom? No. and yes. We have achieved an ultimate satisfaction. fulfilled a destiny. To struggle and to understand - never this last without the other; such is the law. ” George Mallory Climbing Everest: The Complete Writings of George Mallory v vi Abstract The movement of species across suitable areas occur naturally according to species’ dispersal abil- ities, but since humans started to explore the world, they also started to translocate species to a place where they could not arrive by their own means, thus reshaping the world’s biota. In a fraction of cases, such organisms establish naturalized populations in the new range, expand and eventually become detrimental to native species. As a result, biological invasions already represent one of the major causes of biodiversity loss, but at the same time, they provide an opportunity to deepen our knowledge regarding key ecological and evolutionary questions. The Mediterranean basin is the result of a complex history encompassing profound geologi- cal processes, climatic shifts, and biogeographical interchanges harbouring one of the world’s bio- diversity hotpots. It has been also a meeting point of several civilizations, with a long history of human-biota interaction which makes it a good model to study different layers of biological invasions phenomena. Mediterranean islands, in particular, can represent a live laboratory to test evolutionary and ecological hypothesis, due to their geographic isolation and limited number and taxa of organ- isms that can naturally colonize these ecosystems. These features, on the other hand, make island ecosystems particularly vulnerable to biological invasions. Reptiles are a vertebrate group particularly vulnerable to biological invasions but at the same time one of the groups that are more introduced. The long history of interactions between humans and reptiles in Mediterranean islands has caused a mix of multiple ancient and recent introductions of non-native species. Such history makes it difficult to distinguish between alien and native species on this region. At the same time, the diversity of islands together with repeated introduction events provide an excellent opportunity to investigate factors related to introductions and success of alien species in new environments. The main aim of this thesis is to determine the patterns and to infer the main drivers of bi- ological invasions on reptiles’ of Mediterranean Islands at different levels, using a combination of biogeographic, ecologic and genetic tools. First, we focused on the broad Mediterranean basin; we combined genetic, distribution and biological data on Mediterranean reptiles together with island information, to identify the factors promoting the presence of alien reptiles on islands, considering human-related, geographic and species traits. A literature review on native/alien status of reptiles on more than 900 Mediterranean islands was also incorporated in the database. Spatially-explicit mod- els show a complex signal of geographic features, species traits and human-related factors. A reptile record is most likely to be alien if the species feeds on plants and is present on island’s populations vii far from the native range and with large human population size. Furthermore, traditional data sources underestimate the frequency of alien reptiles in Mediterranean islands and the use of genetic infor- mation to assess the status of populations provides a more accurate representation of the factors related to alien populations. Second, we narrowed the study scale to one ‘paradigmatic’ archipelago, the Balearic Islands: here alien reptiles exceed the number of native reptile species and mutliple alien snake species have been recently introduced, endangering the few native species present. We used phylogenetic approaches combined with other information sources (literature and direct observations) to identify the origin and introduction pathways of the four introduced snake species (Hemorrhois hippocrepis, Malpolon monspessulanus, Macroprotodon mauritanicus and Rhinechis scalaris). We also used eco- logical niche models to deduce their patterns of invasion and expansion based on current and future suitability. Iberian Peninsula is the potential origin for most of the alien populations. However, the low phylogeographic structure of these species prevented the identification of more precise source- areas. Ecological niche models’ show a current low habitat suitability in the Balearic Islands, but with tendency to increase significantly in the next few decades under climate change scenarios. From direct observations and spatial analyses, we identified as the most common pathway, the nursery trade, especially of olive tree importation from the Iberian Peninsula. Third, we focused on the Italian Wall lizard, Podarcis sicula, introduced in several places in the world, from the Mediterranean region to North America, where is frequently invasive and so a good model to understand the history and traits that make a reptile succeed in different systems. Avail- able studies support an invasive behavior
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