Pre-Dispersal Seed Predation by Weevils (Curculio Spp.): the Role of Host-Specificity, Resource Availability and Environmental Factors
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Pre-dispersal seed predation by weevils (Curculio spp.): The role of host-specificity, resource availability and environmental factors Harold Arias-LeClaire Aquesta tesi doctoral està subjecta a la llicència Reconeixement- NoComercial – CompartirIgual 4.0. Espanya de Creative Commons. Esta tesis doctoral está sujeta a la licencia Reconocimiento - NoComercial – CompartirIgual 4.0. España de Creative Commons. This doctoral thesis is licensed under the Creative Commons Attribution-NonCommercial- ShareAlike 4.0. Spain License. Pre-dispersal seed predation by weevils (Curculio spp.) The role of host-specificity, resource availability and environmental factors HAROLD ARIAS-LECLAIRE Barcelona, 2018 Pre-dispersal seed predation by weevils (Curculio spp.): The role of host-specificity, resource availability and environmental factors This page intentionally left blank Pre-dispersal seed predation by weevils (Curculio spp.): The role of host-specificity, resource availability and environmental factors Harold Arias-LeClaire Barcelona, 2018 This page intentionally left blank Pre-dispersal seed predation by weevils (Curculio spp.): The role of host-specificity, resource availability and environmental factors Harold Arias-LeClaire Thesis to be eligible for the Doctor degree and submitted in fulfillment of the requirements of Academic Doctoral program in Biodiversity with the supervision and approval of Dr. Josep Maria Espelta Morral Dr. Raúl Bonal Andrés Universitat de Barcelona Barcelona, 2018 This page intentionally left blank Facultat de Biologia Department de Biologia Evolutiva, Ecologia i Ciències Ambientals Pre-dispersal seed predation by weevils (Curculio spp.): The role of host-specificity, resource availability and environmental factors Research memory presented by Harold Arias-LeClaire for the degree of Doctor at the Universitat de Barcelona Biodiversity Program with the approval of Dr. Josep Maria Espelta Morral and Dr. Raúl Bonal Andrés thesis advisors and Dr. Santiago Sabaté Jorba supervisor Harold Arias-LeClaire Doctoral student Dr. Josep Maria Espelta Morral Thesis advisor Researcher at Centre de Recerca Ecològica i Aplicacions Forestals Dr. Raúl Bonal Andrés Thesis advisor Researcher at Departamento Ingeniería Medio Agronómico y Forestal Universidad de Extremadura Dr. Santiago Sabaté Jorba Thesis supervisor Researcher at Departament de Biologia Evolutiva, Ecologia i Ciències Ambientals Universitat de Barcelona Barcelona, 2018 This page intentionally left blank Arias-LeClaire, Harold (2018). Pre-dispersal seed predation by weevils (Curculio spp.): The role of host-specificity, resource availability and environmental factors Doctoral thesis. Academic Doctoral program in Biodiversity conducted under the emphasis in Biodiversity conservation and management. Universitat de Barcelona, Barcelona, Catalunya. Key words: Corylus avellana, Granivory, Mediterranean oak forests, plant–animal interactions, Quercus spp., rainfall stochasticity, resource pulses. This thesis has been conducted in the Center for Ecological Research and Forestry Applications (Centre de Recerca Ecològica i Aplicacions Forestals CREAF, UAB Campus de Bellaterra, Barcelona) with the support of NOVFORESTS project and scholarship as work permit by Universidad Estatal a Distancia (UNED, Mercedes de Montes de Oca, Costa Rica). This page intentionally left blank Acknowledgment “La Vita è Bella” I place on record, my sincere thanks you to my advisors Dr. Espelta - Tete and Dr. Bonal - Raul, I take this opportunity to express my genuine gratitude for their invaluable help, outstanding patience, and encouragement. I am thankful and indebted to them for sharing remarkable expertise and valuable direction. Their advice and guidance helped me in my research and writing of this thesis. Also, my thanks to Dr. Santiago Sabaté for his instruction and work as supervisor. Thanks to Marcos, Enrique, and Alberto for all their work as coauthors and friendship shared. I wish to express my thanks to CREAF for providing me access to the laboratory and research facilities. My sincere thanks also go to the projects NOVFORESTS (CGL2012-33398) and BEEMed (014 SGR 913430), particularly to Dr. Joan Pino and the research group, without this support it would not have been possible to conduct this research. Thanks to Marta and Magda for all their help. I thank all the fellows in the lab and field mates, Pau, Iraima, Marina, Guille, Ana, David and Helena for the discussions and for the shared work. My sincere thanks also to Daniel García, partner in field campaigns, coauthor and very good friend. Also, I thank the Biology Faculty (UB) professors for their helpful and inspiring support, Dra. Mª Jose Lopez, Dr. Pedro Moral, Dr. Gustavo Llorente and Dra. Emilia Gutierrez. I place on record, my sense of gratitude to all, who directly or indirectly, have lent their hand in this venture. To Dra. Dolors Vinyoles thank you very much for the support and encouragement in the final stage. I must express my very profound and heartfelt gratitude to my family for supporting me throughout writing this thesis and my life in general. My sincere thanks to my brother Edgar for the valuable grammatical revision in the final versions of this thesis. Particularly I am deeply grateful to my wife Nancy, supportive partner in this journey as always on so many ventures we have gone through side by side. She is a lighthouse in my life, thank you for providing me with unfailing support and continuous encouragement throughout these years and through the process of researching and writing this thesis. This accomplishment would not have been possible without you. I also thank my Mother and Stepfather for their unceasing help, advice and supporting me spiritually, as well thanks to my Parents in law for constant encouragement and attention. Thank you, God, for blessing me with what is necessary to complete my Doctoral study! And finally, last but by no means least, I would like to dedicate this thesis to my kids Oriana, Daniel, David, Josué and Joel but specially on behalf of the loving memory of my brother and my father. Adrián and Papa, I deeply wish you were here to share with you this achievement. Sincerely “gracias totales” HAL …Live long and prosper! Table of contents Summary 1 Resumen 2 Chapter I. General introduction 3 Research objectives 13 General introduction references 15 Directors reports Impact factor of published articles 21 Contribution of the doctorate in the published articles 22 Published Research Articles Chapter II. The role of seed size, phenology, oogenesis and host 25 distribution in the specificity and genetic structure in seed weevils (Curculio spp.) in mixed forests. Chapter III. Beyond predator satiation: Masting but also the effects of 43 rainfall stochasticity on weevils drive acorn predation. Chapter IV. General discussion 59 General conclusions 69 General discussion references 71 Epilogue 77 This page intentionally left blank Summary Pre-dispersal seed predation (PDSP, hereafter) significantly reduces plant reproductive output. The negative effects on plant fitness have triggered the development of different strategies to protect the seeds and/or reduce the impact of PDSP. These strategies, in turn, have promoted insect trophic specialization by means of morphological, physiological and behavioral adaptations. The close relationship between specialist insects and their host plants conditions insect community assemblage and population dynamics. Specialization would favour multi-species co-occurrence according to the Competitive Exclusion Principle, as different species cannot use the same limited resources. At the same time, specificity makes these species strongly dependent on a particular trophic resource, so that host plant population dynamics may lead to bottom-up forces influencing insect numbers. In this Thesis, I have studied the consequences of trophic specialization on species assemblage and demography in the most prevalent pre-dispersal predators of oak Quercus spp., chestnuts Castanea sativa and hazelnut Corylus avellana seeds, namely the weevils of the genus Curculio (Coleoptera: Curculionidae). Using DNA barcoding I could identify larvae infesting the seeds to the species level and hence assess resource partitioning among Curculio spp. in oak-hazelnut mixed forests. These forests were distributed along a latitudinal gradient in which the degree of overlap in the timing of seeding between the two species differed. The results showed that there was a strict host-based segregation, as the species found in hazelnuts was never recorded on oak acorns and vice versa. Contrary to other studies, segregation of seed parasites was not driven by seed size, as the seeds of both plants were large enough to host the larvae of any species. Rather, co-existence was more likely modulated by the combination of time partitioning, and probably by dissimilarities in dispersal- dormancy strategies among weevils. The timing of oogenesis differs among Curculio spp. and does the timing of seeding between oaks and hazelnuts. Early maturing hazelnuts are thus exploited only by Curculio nucum, as its eggs mature earlier too. Such specialization on a patchily distributed host plant conditioned its population genetics, as gene-flow between populations showed restrictions undetected in the other Curculio spp. that fed on the widespread oaks. Regarding the bottom-up effects of food availability on insect numbers we assessed that, as expected, irregular seed crops (masting) conditions weevil population dynamics