Understanding patterns and processes in plant–hummingbird mutualistic networks in the Neotropics Dissertation for attaining the PhD degree of Natural Sciences submitted to the Faculty of Biology of the Johann Wolfgang Goethe University in Frankfurt am Main by María Alejandra Maglianesi from Santa Fe, Argentina Frankfurt 2014 (D 30) i Faculty of Biology of the Johann Wolfgang Goethe University accepted as a dissertation. Dean: Prof. Dr. rer. nat. Meike Piepenbring First reviewer: Prof. Dr. Katrin Böhning-Gaese Second reviewer: Prof. Dr. Alexandra-Maria Klain Date of disputation: ___________________ ii TABLE OF CONTENTS 1. SUMMARY ............................................................................................................ 1 2. INTRODUCTION .................................................................................................... 3 2.1 Biotic interactions in ecological communities .................................................. 3 2.2 Plant–pollinator mutualistic networks ……………………....................................... 4 2.3 Functional structure of pollinator communities …………………………….…………….. 6 2.4 Why specialization in ecological networks matters? ………………………………….... 7 2.5 Mechanisms underlying ecological specialization …..……………………….............. 8 2.6 Potential and realized interactions in plant–pollinator networks .................. 9 2.7 Plant–hummingbird interactions ...................................................................... 10 3. STRUCTURE OF THE THESIS AND RESEARCH QUESTIONS …………….….……….......... 11 3.1 Thesis structure ……………………………..……………………………..…….……………………….. 11 3.2 Research questions …………………………………..…………………………………...…….…..….. 11 3.2.1 Do the functional structure and specialization in plant–hummingbird 12 networks change across elevation? ………………….….………......................................... 3.2.2 How do the morphological traits of interacting species shape plant– 12 hummingbird interactions? ………………….….………...................................................... 3.3.3 How do the floral morphology and competition among hummingbirds 13 influence the foraging preferences of the birds on artificial and natural flowers? .. 4. RESEARCH AREA AND STUDY SYSTEM ……………………….….…..…….......................... 14 4.1 Research area and data collection ……………………………………………………………….. 14 4.2 Study system ………………………………………………………………………………………………… 18 4.2.1 Hummingbirds ……………………………………………………………………………………………. 18 4.2.2 Hummingbird–visited plants …………………………………………………………………..….. 20 5. RESULTS AND DISCUSSION ................................................................................... 22 5.1 Functional structure and specialization in plant–hummingbird networks 22 along an elevational gradient ........................................................................... iii 5.1.1 Functional structure of hummingbird assemblages varies across elevation .. 22 5.1.2 Hummingbird specialization decreases with elevation ………………………………. 23 5.2 Influence of morphological traits on patterns of interactions in plant- 24 hummingbird networks ..................................................................................... 5.2.1 Ecological specialization is associated with morphological traits in plant– 24 hummingbird networks ...................................................................................... 5.2.2 The role of trait matching in shaping plant–hummingbird interactions …….. 25 5.3 Combining experimental and observational approaches to understand 26 patterns of plant–pollinator interactions ……………………………………………………… 5.3.1 Interaction niche of hummingbird species under experimental conditions … 27 5.3.2 Interaction niche of hummingbird species under natural conditions ………….. 28 6. CONCLUSIONS ...................................................................................................... 29 7. ZUSAMMENFASSUNG .......................................................................................... 31 8. ACKNOWLEDGEMENTS ...................................................................................... 37 9. REFERENCES ......................................................................................................... 39 10. APPENDICES ....................................................................................................... 52 Appendix 1: Functional structure and specialization in tropical plant– 53 hummingbird interaction networks across elevations ............................................. Appendix 2: Morphological traits determine specialization and resource use in 81 plant–hummingbird networks in the Neotropics ..................................................... Appendix 3: Different foraging preferences of hummingbirds on artificial and 121 natural flowers reveal mechanisms structuring plant–pollinator interactions …….. Appendix 4: List of hummingbird species recorded at the study sites .................... 152 Appendix 5: List of plant species recorded at the study sites .................................. 154 Appendix 6: Curriculum vitae .................................................................................. 158 iv Summary 1. SUMMARY Ecological communities are organized in complex ecological networks where species relate to each other through different types of interactions. The mutually beneficial interactions between plants and their animal pollinators have a pervasive influence in community dynamics and have contributed to the generation of Earth’s biodiversity. Hence, a profound knowledge of how plant–pollinator networks are structured is essential to understand evolution, the maintenance of biodiversity and the consequences of species extinction. Functional traits of species influence patterns of interactions in pollination networks. Trait–based analysis can reveal processes structuring mutualistic networks and ecological communities. However, at present there are few studies that link species functional traits with patterns of interactions in plant–pollinator networks, especially in the tropics. I investigated patterns in functional structure and specialization in plant– hummingbird mutualistic networks across elevations and the processes driving these patterns in three tropical forests of Costa Rica. I quantified different metrics of functional community structure based on three morphological traits (bill length, bill curvature and body mass) of hummingbird species at three elevations. I used pollen carried by mist–netted hummingbird individuals to construct plant–hummingbird networks at the individual and species level at each elevation. My results show consistent patterns in the functional structure of hummingbird assemblages and specialization of hummingbird species and individuals across elevations. Hummingbird assemblages varied from being functionally even and over–dispersed in the lower elevations to uneven and clustered in high–elevation environments. Accordingly, hummingbird species and individuals were more specialized at low and mid elevations than at the highest elevation. I used recent advances in the analysis of quantitative networks to assess the importance of morphological traits in shaping plant–hummingbird interactions. First, I tested the effects of the three avian morphological traits and abundance on ecological specialization of hummingbird species. Second, I analyzed whether interaction strength in the networks was associated with the degree of trait matching between corresponding pairs of morphological traits in plant and hummingbird species. Third, I 1 Summary explored whether trait matching between interacting species was related to resource handling times by hummingbird species. I found strong and significant associations between interaction strength and the degree of trait matching in corresponding morphological traits of hummingbird and plant species. Moreover, the degree of trait matching was negatively associated with the handling time of nectar resources by hummingbirds. Finally, I used experimental and observational data to explore the foraging preferences of hummingbird species for artificial and natural flowers with specific morphology. Hummingbird species visiting artificial feeders with unlimited nectar preferred short artificial flowers over long–straight and long–curved flowers. Under natural conditions, however, co–occurring hummingbird species preferred to feed on plant species with floral traits matching their bill morphology. Overall, my results suggest different processes and mechanisms underlying patterns of functional community structure and interactions in plant–hummingbird mutualistic networks. Even and over–dispersed hummingbird assemblages at the lower elevations suggest a high level of floral resource partitioning leading to specialized plant– hummingbird interactions. In contrast, an uneven and clustered functional structure of the hummingbird assemblage in the highlands may result from environmental filtering in generalized hummingbird interactions. My findings highlight the crucial role of morphological traits for structuring plant–hummingbird networks and that patterns of interactions are closely associated with morphological matches between plant and hummingbird species. Additional factors however, such as competition for resources, are also important and may enforce patterns of niche segregation between co– occurring hummingbird species in natural communities. Trait–based analyses of quantitative networks combined with experimental and observational approaches are essencial for a comprehensive understanding