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Evolution of Ecological Diversity in the Neotropical Tanagers of the Genus

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Evolution of Ecological Diversity in the Neotropical Tanagers of the Genus Louisiana State University LSU Digital Commons LSU Doctoral Dissertations Graduate School 2003 Evolution of ecological diversity in the neotropical tanagers of the genus Tangara (Aves: Thraupidae) Kazuya Naoki Louisiana State University and Agricultural and Mechanical College, [email protected] Follow this and additional works at: https://digitalcommons.lsu.edu/gradschool_dissertations Recommended Citation Naoki, Kazuya, "Evolution of ecological diversity in the neotropical tanagers of the genus Tangara (Aves: Thraupidae)" (2003). LSU Doctoral Dissertations. 2021. https://digitalcommons.lsu.edu/gradschool_dissertations/2021 This Dissertation is brought to you for free and open access by the Graduate School at LSU Digital Commons. It has been accepted for inclusion in LSU Doctoral Dissertations by an authorized graduate school editor of LSU Digital Commons. For more information, please [email protected]. EVOLUTION OF ECOLOGICAL DIVERSITY IN THE NEOTROPICAL TANAGERS OF THE GENUS TANGARA (AVES: THRAUPIDAE) A Dissertation Submitted to the Graduate Faculty of the Louisiana State University and Agricultural and Mechanical College in partial fulfillment of the requirements for the degree of Doctor of Philosophy in The Department of Biological Sciences by Kazuya Naoki B.S., Universidad de Costa Rica, 1996 August 2003 ACKNOWLEDGMENTS Many people and institutions in many countries helped make this dissertation possible. First I thank my parents and my sister in Japan to understand and support my interests in tropical biology for last 14 years. Even though I have failed to get in touch with them frequently, they always showed great comprehension on my passion and love to nature and offered to support me in all possible ways. I thank my advisor, J. V. Remsen Jr. (Van), for many, many advices at critical moments of my Ph.D. for last six years. Without his help, I would not have finished my Ph.D. I also thank my graduate committee: Frederick H. Sheldon, J. Michael Fitzsimons, Kyle E. Harms, James P. Geaghan, and L. Lee Southern for their time and support. At LSU I benefited greatly from fellow graduate students. Funding for fieldwork was provided by the following organizations: the National Geographic Society, the Cooper Ornithological Society, the Wilson Ornithological Society, the American Ornithologists’ Union, the American Museum of Natural History, the Louisiana State University Museum of Natural Science, SigmaXi, LSU Dept. Biological Sciences. Many people made my fieldwork possible. In Ecuador, I am grateful to M. Moreno Espinosa (Museo Ecuatoriano de Ciencias Naturales) and S. Lasso (Ministerio de Medio Ambiente) for help in obtaining the research permit. I thank L. Chaves, M. Jácome (Fundación Ornitológica del Ecuador), Francisco and Fernando Sornoza for providing advice and field assistance; E. Freire, H. Vargas, E. Narváez, Elsa Toapanta, and J. C. Ronquillo (Herbario Nacional del Ecuador) for identification of plant samples; and E. Bastídas and V. Zak for kindly allowing me to work in their reserve and private property. Many people in Mindo helped me in various aspects of the research. I especially thank Hugolino and Alicia Oñate, Efraín Toapanta, ii Fundación Pacaso y Pacaso, and Amigo de la Naturaleza. N. Krabbe, P. Greenfield, and J. C. Matthew shared observation on natural history of tanagers. In Costa Rica, I thank Julio E. Sánchez, Hernan Araya, Leonardo Chavez, and Andres Vega for helping us to find a study site and also provided logistic support. Don Beche, Doña Lucia, Don Wiliam, and Doña Estrella in Tausito offered us a shelter, meals, and great friendship during the fieldwork. Don Beto Chavez Mora and Don Leonel of Reserva Biológica El Copal let us use their reserve for the study. Don Beto and his family also helped our fieldwork and offered their companionship. Armando Estrada of Museo Nacional de Costa Rica kindly identified all the plant samples. Marco Tulio kindly made slides for Naoki’s talk presented for Asociación Ornitológica de Costa Rica. I also thank Ministerio del Ambiente y Energia for permitting to conduct this research in Costa Rica. I thank Maria Isabel Gómez and Ernesto Carman for collaboration in fieldwork. In Bolivia, I thank Carmen Quiroga, Omar Rocha, James Aparicio, Alvaro Garritanos (Colección Boliviana de Fauna), Sebastian Herzog, Bennett Hennesy (Armonia) for giving me indispensable advise in conducting fieldworks. Omar Martinez and M. Isabel Gómez kindly accompanied me into the fields. Finally, I want to thank M. Isabel Gómez and her family for their kindness and hospitality. iii TABLE OF CONTENTS ACKNOWLEDGMENTS ..............................................................................................................ii ABSTRACT......................................................................................................................……...…v CHAPTER 1 INTRODUCTION ..........................................................................……............................1 2 DICHOTOMOUS DIFFERENCES IN RESOURCE USE AMONG OMNIVOROUS TANGARA TANAGERS ….............…….....................……..5 3 THE RELATIVE IMPORTANCE OF ARTHROPODS AND FRUITS IN FORAGING BEHAVIOR OF TANGARA TANAGERS ….....…......……..73 4. SEASONAL CHANGES IN FORAGING ECOLOGY OF TANGARA TANAGERS IN COSTA RICA: FOOD-TYPE DEPENDENT RESOURCE PARTITIONING AND TEMPORAL VARIATION.......................................…...……..83 5 EVOLUTION OF ECOLOGICAL DIFFERENCES IN TANGARA TANAGERS ….....…..........…..........…..........…..........…..........…..............109 6 SUMMARY AND CONCLUSION .….......…..........…..........…........………......…….142 REFERENCES ………………………………………………………………………………...154 APPENDIX 1 DATA FOR ARTHROPOD FORAGING …………………………………………….163 2 DATA FOR FRUIT FORAGING …………………….……………………………….167 3 DATA FOR HABITAT USE ……………………………………..…..………….….…175 4 DATA FOR ELEVATIONAL DISTRIBUTION (M) .…….…………………….……177 VITA ………………………………………………………………………………………...…179 iv ABSTRACT The origin and maintenance of biological diversity has been one of the fundamental issues in biology. However, the evolution of ecological traits that affect species coexistence and species diversity is poorly known. My research aimed to investigate the evolution of species- specific ecological and morphological traits and to understand the process of ecological diversification and species coexistence in Tangara tanagers (Thraupidae) by using phylogenetic comparative methods. Tangara is the largest avian genus in the New World with 50 recognized species. As many as ten species of Tangara are found sympatrically in the same Andean cloud forest, and many syntopic species travel together in mixed-species flocks. The distribution of Tangara covers all of subtropical and tropical America from sea level to tree line; thus, Tangara species show a wide range of habitat preferences as well as strong variation in number of coexisting species and species combinations. Like many other species of tanagers, Tangara species are omnivorous; their diet consists of both insects and fruit. I collected extensive ecological and behavioral data at six study sites to quantify ecological differences among sympatric species. I measured museum skins and skeletons to define morphospace of each taxon. DNA sequences were used to build a molecular phylogeny, which reveals the speciation pattern. I combined ecological data, morphological data, distributional data from literature, and a molecular phylogeny by two phylogenetic analytical methods to elucidate evolution of ecological diversity among 25 Tangara taxa. Permutational phylogenetic regression analyses showed significant phylogenetic effects for arthropod foraging, but not for fruit foraging, habitat use, and elevational distribution. A disparity-through-time plot showed that the relative disparity of arthropod foraging decreased more rapidly than the other niche axes. These analyses revealed diverse evolutionary patterns unique to each niche axis. The relative strength of phylogenetic v effects, frequency of homoplasy, mode of evolution, and association with morphology differed substantially among the four niche axes. Fruit foraging and habitat specialization showed the greatest ecological plasticity in relation to phylogeny, and the variation in microhabitat preference in arthropod foraging associated with species-specific attack maneuver was the most conservative and consistent with the phylogeny. vi CHAPTER 1 INTRODUCTION One of the fundamental goals in biology is to explain the pattern and origin of biological diversity (Hutchinson 1959; Magurran and May 1999; Ricklefs and Schluter 1993; Rosenzweig 1995). Most attempts to do so have been conducted at small temporal scales. Such studies have examined how local ecological processes, such as competition, predation, mutualism, and resource availability, influence local community structure (McPeek and Miller 1996; Schluter and Ricklefs 1993). Community diversity, however, is determined not only by local but also by regional processes, such as species formation, dispersal, and extinction (Ricklefs 1987; Ricklefs and Schluter 1993). Hence, the incorporation of evolutionary thinking is one of the most urgent tasks in the study of biological diversity (McPeek and Miller 1996; Ricklefs and Schluter 1993; Rosenzweig 1995; Tokeshi 1999). Conventional ecological approaches through direct observations or through field experiments can reveal short-term changes in ecological traits, such as habitat choice, diet selection, and geographical distribution, which are crucial to understanding the
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