On the feeding biomechanics of nectarivorous birds

Abstract

Nectar-feeding birds employ unique mechanisms to collect minute liquid rewards hidden within floral structures. In recent years, techniques developed to study drinking mechanisms in hummingbirds have prepared the groundwork for investigating nectar feeding across birds. In most avian nectarivores, fluid intake mechanisms are understudied or simply unknown beyond hypotheses based on their morphological traits, such as their tongues, which are semi-tubular in sunbirds, frayed-tipped in honeyeaters and brush-tipped in lorikeets. Here, we use hummingbirds as a case study to identify and describe the proposed drinking mechanisms to examine the role of those peculiar traits, which will help to disentangle nectar-drinking hypotheses for other groups. We divide nectar drinking into three stages: (1) liquid collection, (2) offloading of aliquots into the mouth and (3) intraoral transport to where the fluid can be swallowed. Investigating the entire drinking process is crucial to fully understand how avian nectarivores feed; nectar-feeding not only involves the collection of nectar with the tongue, but also includes the mechanisms necessary to transfer and move the liquid through the bill and into the throat. We highlight the potential for modern technologies in comparative anatomy [such as microcomputed tomography (μCT) scanning] and biomechanics (such as tracking BaSO4-stained nectar via high-speed fluoroscopy) to elucidate how disparate clades have solved this biophysical puzzle through parallel, convergent or alternative solutions.

Variable evidence for convergence in morphology and function across avian nectarivores

“…Once morphology is quantified, open-source programs and packages can be used to construct a morphospace, quantify whether lineages occupy different adaptive peaks or have converged on a single adaptive peak Mahler et al, 2013), compare models of trait evolution, and assess the evolutionary relationships between morphology and diet/ecological factors (e.g., Pagel & Meade, 2006;Paradis et al, 2004;Paradis & Schliep, 2019;Pennell et al, 2014;Revell, 2012;Stayton, 2015). Phylogenetic comparative methods at this scale are now possible thanks to efforts to produce a comprehensive avian phylogeny (www.birdtree.org, Rubolini et al, 2015) and the fact that family-level phylogenies are becoming increasingly available for all lineages of avian nectarivores Finally, in conjunction with improving our understanding of morphological evolution, it is also critical to continue investigating how differences in morphology result in functional differences across avian nectarivores (Cuban et al, 2022), as function is the interface between morphology and the environment, and thus the target of selection (Arnold, 1983). The work done by Dakin et al (2018) to analyze the correlation between maneuverability and particular features of the locomotor apparatus (e.g., wing loading) among hummingbirds provides a template for how these morphofunctional studies can be conducted and applied at the macroevolutionary scale.…”

“…Many researchers have been interested in studying the biomechanics of the nectarloading process, how it varies with tongue morphology and nectar traits, and tying that to larger processes like foraging behavior and bird−plant coevolution (e.g., Hainsworth, 1973;Heyneman, 1983;Kim et al, 2011;Kingsolver & Daniel, 1983). The only taxon for which the feeding biomechanics have been empirically investigated is hummingbirds, but there are hypotheses in the literature for many other taxa (reviewed by Cuban et al, 2022).…”

“…For example, the hummingbird tongue cannot function as a drinking straw because the grooves are open dorsally, precluding the formation of a pressure gradient (Cuban et al, 2022). While the possible feeding mechanisms are expected to be determined primarily by tongue morphology, it is also relevant to consider the fact that mechanisms differ in efficiency across nectar concentrations and volumes (e.g., capillary filling vs. active suction; Cuban et al, 2022; Kim et al, 2011; Wei et al, 2020) due to their varying sensitivity to nectar traits like viscosity and surface tension. The interplay of evolutionary constraint on tongue morphology and the physical traits of nectar likely work together to determine the most efficient nectar loading mechanism out of those that are possible.…”

“…Many researchers have been interested in studying the biomechanics of the nectar‐loading process, how it varies with tongue morphology and nectar traits, and tying that to larger processes like foraging behavior and bird−plant coevolution (e.g., Hainsworth, 1973; Heyneman, 1983; Kim & Bush, 2012; Kim et al, 2011; Kingsolver & Daniel, 1983). The only taxon for which the feeding biomechanics have been empirically investigated is hummingbirds, but there are hypotheses in the literature for many other taxa (reviewed by Cuban et al, 2022). Based on the fact that the hummingbird tongue consists of two tubular grooves, it was originally hypothesized that the tongue functioned like a capillary tube (Kim & Bush, 2012; Kim et al, 2012; Kingsolver & Daniel, 1983; Lucas, 1891, 1895), but based on extensive high‐speed videography in wild hummingbirds of many species, we now know that different regions of the hummingbird tongue aid in nectar uptake in highly dynamic ways.…”

“…Nectarivory is a foraging niche that has evolved in many vertebrate lineages (e.g., Eifler, 1995; Fleming & Muchhala, 2008; Fleming et al, 2005; Olesen & Valido, 2003), defining nectarivore as “an animal that has specialized to consume floral nectar, which exhibits morphological, physiological, and behavioral adaptations for nectar feeding” (Cuban et al, 2022). Throughout their evolutionary history, birds have been prolific in their exploitation of nectar resources (Burns et al, 2003; Pauw, 2019).…”