Evolutionary ecology of interactions between plants and nectar-feeding birds across scales

Abstract

University of Washington Abstract Evolutionary ecology of interactions between plants and nectar-feeding birds across scales Amanda E. Hewes Chair of the Supervisory Committee: Alejandro Rico-Guevara Department of Biology Plant-pollinator interactions constitute a fantastic system to investigate how ecological and evolutionary processes influence each other. In this dissertation I use honeyeaters (Aves, Meliphagidae), the second-most speciose clade of vertebrate pollinators and an avian family native to Australasia, as a study system to investigate (1) how bird and plant phenotypes interact to determine the outcomes of plant-pollinator interactions and (2) how these interactions can lead to evolutionary consequences such as adaptation, specialization, and coevolution. Chapter 1 begins with a survey of the evidence for convergence in morphology and function across roughly twenty lineages of specialized avian nectarivores. By reviewing the literature on morphological and functional adaptations for nectarivory in these taxa, I found that the feeding apparatus (bill, tongue, hyoid) exhibits the most convergent morphology, and is more commonly modified than the locomotor apparatus (wings and legs) or the digestive and renal systems. This work also illuminated the knowledge gaps that exist in our basic understanding of how birds adapt to nectarivory and provided suggestions for future research.Chapter 2 focuses on the process of nectar feeding in honeyeaters, as one of the primary biophysical challenges faced by nectar-feeding birds is efficient extraction of small nectar volumes from flowers. This chapter uses a biomechanics approach, including high-speed videography and kinematic analyses, across five species to answer the question of how honeyeaters use their brush-tipped tongues to capture nectar. I found that nectar is primarily captured via surface tension between the bristles at the tip of the tongue, a mechanism called fluid trapping, rather that via fluid flow through the grooved body of the tongue. Using fluid trapping as the primary mechanism of nectar capture could be what allows honeyeaters to visit flowers with a wide range of nectar presentations (i.e., nectar volume, sugar concentration). Chapter 3 follows by examining the degree to which hyolingual morphology (the size and shape of the tongue and the bony support called the hyoid) varies across honeyeater species, and whether that morphology correlates with the degree of dietary dependance on nectar. This work employs diverse techniques such as linear morphometrics, anatomical characterization, histology, and computer tomography (CT scans) to provide the most comprehensive survey of this type performed in any bird family. I found that there are six distinct tongue types across honeyeaters, some of which are restricted to particular genera that warrant their own biomechanical analysis of feeding due to their seeming morphological incompatibility with nectar feeding via fluid trapping. Additionally, two aspects of tongue morphology – tongue length and the proportion of the tongue that is bristled – were positively correlated with increased reliance on nectar. These macroevolutionary patterns make sense in light of the biomechanical analysis from Chapter 2, as a longer tongue can access a wider range of flowers in the environment and probe deeper into flowers, while a larger bristled portion of the tongue allows more surface area for nectar collection via fluid trapping. Chapter 4 zooms out beyond the tongue-nectar interface to examine the outcomes of honeyeater-plant interactions in the field. This chapter asks how morphological matching between a honeyeater’s bill and a flower determines pollen transfer between flowers (pollen load acquired from anthers and pollen deposited at floral stigmas) and the feeding efficiency of birds (microliters of nectar consumed per second). In this work I found that honeyeater species differ in their pollination and feeding efficiency at flowers, but that a worse bill-flower match was only correlated with less pollen deposition, not with pollen load or feeding efficiency. The finding that increased morphological matching does not facilitate greater feeding and pollination efficiency of honeyeaters is a surprising insight that pushes us to reevaluate the coevolutionary mechanistic rationale of bird pollination systems. Finally, Chapter 5 uses a community ecology framework to consider how plant traits and interspecific interactions between honeyeater species could influence patterns of bird visitation to plants. This work quantified the honeyeater community composition and nectar resources (as kilojoules of energy per flower and number of flowers produced) at two sympatric species of Australian flowering plants. I found that the two plant species supported significantly different honeyeater communities. The lower-reward plant species (i.e., fewer kilojoules produced per flower and fewer flowers produced) attracted a higher number of small-bodied honeyeater species and was almost never visited by larger species. There were also fewer birds visiting and fewer aggressive interactions at this low-reward plant. These differences in community composition of honeyeater visitors is likely because smaller birds, having lower energetic demands than large species, get relatively more caloric gain from the low-reward plant while avoiding the risk of competition and aggression presented by the high-reward plant species. In summary, this dissertation studies honeyeater-plant interactions across spatial and temporal scales using an integrative approach. This work has filled several knowledge gaps about honeyeater-plant interactions, such as the fact that honeyeaters drink nectar via fluid trapping and have evolved longer, more bristled tongues as an adaptation to increased nectarivory. Broadly, this dissertation illustrates that interdisciplinary research is necessary to holistically investigate the evolutionary ecology of any animal pollination system and provides methods and a conceptual framework with which to do so.