Ricardo Rafael dos Santos Ceia INSECT PREDATION BY BIRDS IN MEDITERRANEAN OAK WOODLANDS AND ITS IMPORTANCE IN THE CONTROL OF DEFOLIATOR PESTS Tese de Doutoramento em Biociências, ramo de especialização em Ecologia, orientada por Jaime Albino Ramos e apresentada no Departamento de Ciências da Vida da Universidade de Coimbra Fevereiro 2016 Insect predation by birds in Mediterranean oak woodlands and its importance in the control of defoliator pests Thesis submitted for the degree of Doctor of Philosophy in Biosciences (scientific area of Ecology) presented to the University of Coimbra, supervised by Jaime Albino Ramos. Ricardo Rafael dos Santos Ceia Department of Life Sciences University of Coimbra Coimbra | 2016 This thesis was supported by: Fundação para a Ciência e a Tecnologia (FCT) PhD grant attributed to Ricardo S. Ceia (SFRH/BD/78813/2011) MARE – Marine and Environmental Sciences Centre University of Coimbra The following manuscripts resulted from this thesis: Ceia RS, Ramos JA (2014) Birds as predators of cork and holm oak pests. Agroforestry Systems DOI:10.1007/s10457-014-9749-7 Ceia RS, Ramos JA (2015) Effects of dominant tree species on insectivorous birds breeding in Mediterranean oak woodlands. Bird Study DOI:10.1080/00063657.2015.1136264 Ceia RS, Ramos JA. Numerical and functional responses of tree-foraging passerines to larval outbreaks of two defoliator species in cork oak woodlands. Submitted to Biological Control Ceia RS, Machado RA, Ramos JA. Caterpillar predation by three hole-nesting passerine species and experimental increase of their densities in Mediterranean oak woodlands. Submitted to European Journal of Forest Research To my parents ACKNOWLEDGEMENTS Regardless of the lonesome investigation process that involves every researcher, the thesis here presented to you was only made possible thanks to the contribution of various persons and institutions. Without their help my research would not have been possible. In these few lines I wish to thank the support of all the people that joined me in this process, as well as those who demonstrated their interest on this work. First and foremost, I wish to express my deepest gratitude to Jaime Ramos, my supersupervisor, for all his long-lasting irreplaceable mentorship. Throughout these years, he has thaught me the ways of science with passion and motivation, fostering both my personal and professional growth. I do hope to have rewarded his efforts through my work as expected. As a friend, I truly thank him for the confidence placed in me and, together with his wife, Lúcia, for the recurring and exceptionally warm hospitality they have given me in Coimbra and elsewhere. As far as the early development of this work is concerned, I am particularly thankful to Luis García Quintanilla, whose reference letter supported both my application to a FCT grant and my enrolment in the PhD in Biosciences at the University of Coimbra, and to Teresa Gonçalves, Miguel Bugalho and Rúben Heleno (as well as to my brother, Filipe) for their suggestions on this thesis project. I also acknowledge the expertise advice from Angela Turner on the ligature technique. I am extremely grateful to Maria Teresa Varela and José Vilhena (Herdade do Adaíl), Rita Bonacho and Mário Rosa (Herdade do Areeiro e Caneira), José Frederico Fonseca (Sociedade Agrícola da Serra e Amendoeira Lda.) and, especially, Alfredo Sendim (Sociedade Agrícola do Freixo do Meio, S.A.) which gave permission for fieldwork in their properties and provided logistic support. I thank also Associação de Produtores Florestais do Concelho de Coruche e Limítrofes (APFC) and Associação de Produtores Florestais do Vale do Sado (ANSUB), in the respective persons of Conceição Santos Silva and Pedro Silveira, for easing the contact with property owners. I am truly thankful to Rui Machado, whose MSc thesis I had the pleasure to supervise during this thesis, for his collaboration in hundreds of enjoyable hours of fieldwork, for his qualified laboratory work, for his friendship, inexhaustible enthusiasm and commitment. I was very fortunate for having been assisted by such exceptionally talented young researcher and I expect to return the favour during his auspicious scientific career. 9 I am likewise indebted to Mónica Lima (University of Évora) for the many technical skills in insect identification she has passed to me with unwavering dedication and patiente. I also thank Gonçalo Costa (Instituto Superior de Agronomia) and Tiago Magalhães (Universidade de Trás-os-Montes e Alto Douro) for their help with insect identifications. Special thanks to “Gabi” for lending a binocular microscope to my home office. Additionally, I sincerely acknowledge the valuable help given by Vítor Paiva on statistical analyses and the suggestions by Peter Adamík and anonymous referees which greatly improved earlier versions of manuscripts. Finnaly, I do not know how to put into words my huge and sincere gratitude to my office mates, Rafael and Marisa (my son and his mother, respectively) for sharing their endless love with me during the almost endless hours of this work. 10 TABLE OF CONTENTS Abstract 13 Resumo 15 General Introduction 17 Chapter 1 33 Birds as predators of cork and holm oak pests Chapter 2 55 Effects of dominant tree species on insectivorous birds breeding in Mediterranean oak woodlands Chapter 3 75 Numerical and functional responses of tree-foraging passerines to larval outbreaks of two defoliator species in cork oak woodlands Chapter 4 93 Ceterpillar predation by three hole-nesting passerine species and experimental increase of their densities in Mediterranean oak woodlands General Discussion 111 References 123 Appendix A 153 Parasitoids and insect predators of cork and holm oak pests Appendix B 159 Other results from this PhD thesis 11 12 ABSTRACT A systematic investigation on insect predation by birds was conducted in Mediterranean oak woodlands of southwestern Iberian Peninsula with the purpose of assessing the services provided by insectivorous birds in the control of cork oak (Quercus suber) and holm oak (Q. rotundifolia) pests, particularly defoliators. Through a literature review concerning foraging ecology and diet of breeding, wintering and resident birds in southwestern Iberian Peninsula, twenty-six species were listed as potential regular predators of the main cork and holm oak pests. A strong interaction was found between bird foraging guilds and the biology of consumed pests: ground-foragers prey on overwintering pupae and larvae of seed-borers, tree-foragers prey on eggs, larvae and pupae of defoliator and wood-boring pests, and aerial-sweepers prey on airborne imagines. Regarding defoliators, spring-summer was recognized as the period when bird predation is supposed to have the greatest impact on their populations because caterpillars, throughout their development on foliage, are highly vulnerable to predation by various tree-foraging passerine species which occur in high densities and are widespread in Mediterranean oak woodlands. Such prediction was validated in the field at the same time that tree selection between cork oak and holm oak by insectivorous birds was studied with respect to dominant tree species of Mediterranean oak woodlands. Approximately 95% of arthropod predation by birds on trees was carried out by only seven passerine species, which, by themselves, represented more than 60% of total bird abundance: blue tit (Cyanistes caeruleus), great tit (Parus major), crested tit (Lophophanes cristatus), chaffinch (Fringilla coelebs), Sardinian warbler (Sylvia melanocephala), nuthatch (Sitta europaea) and short-toed treecreeper (Certhia brachydactyla). Local scale variation in cork oak- and holm oak-dominance had little effect on breeding bird communities, although bark-gleaners moderately preferred cork oak. It was also suggested, via statistical modeling of the time spent by foraging birds on each tree, that some characteristics regarding morphology, phenology and physiological condition of cork and holm oak trees can be used to predict habitat quality for insectivorous forest birds. Numerical and functional responses of the tree-foraging guild to localized larval outbreaks of two major defoliator pests – gypsy moth (Lymantria dispar) and the sawfly Periclista andrei – in cork oak woodlands were compared with a non-infested control. Four species evidenced positive responses to defoliator outbreaks: densities of nuthatch Abstract | 13 and chaffinch were higher in the outbreak areas of gypsy moth and P. andrei, respectively (numerical responses), and blue tits and crested tits spent a significantly larger amount of time foraging on trees infested with gypsy moth (functional responses). These results are consistent with predictions of the generalist predator hypothesis and drawed attention to the importance of natural biological control by birds, namely through density-dependent mechanisms of pest regulation. Bird predation on defoliator caterpillars was estimated in non-outbreak conditions, through identification of food given to nestlings by three hole-nesting passerine species which forage on different niches of trees: blue tit (Cyanistes caeruleus; foliage-gleaner), great tit (Parus major; bark-foliage-gleaner) and nuthatch (Sitta europaea; bark-gleaner). Their specific roles were compared using breeding densities, size and composition of preyed caterpillars and provisioning rates to nestlings reared in nest-boxes. Caterpillars were the most, or second-most, common prey consumed by nestlings of the three species.