Shifting Paradigms in the Mechanics of Nectar Extraction and Hummingbird Bill Morphology

Abstract

As functional morphologists, we aim to connect structures, mechanisms, and emergent higher-scale phenomena (e.g., behavior), with the ulterior motive of addressing evolutionary patterns. The fit between flowers and hummingbird bills has long been used as an example of impressive co-evolution, and hence hummingbirds’ foraging behavior and ecological associations have been the subject of intense study. To date, models of hummingbird foraging have been based on the almost two-centuries-old assumption that capillary rise loads nectar into hummingbird tongue grooves. Furthermore, the role of the bill in the drinking process has been overlooked, instead considering it as the mere vehicle with which to traverse the corolla and access the nectar chamber. As a scientific community, we have been making incorrect assumptions about the basic aspects of how hummingbirds extract nectar from flowers. In this article, we summarize recent advances on drinking biomechanics, morphological and ecological patterns, and selective forces involved in the shaping of the hummingbird feeding apparatus, and also address its modifications in a previously unexpected context, namely conspecific and heterospecific fighting. We explore questions such as: how do the mechanics of feeding define the limits and adaptive consequences of foraging behaviors? Which are the selective forces that drive bill and tongue shape, and associated sexually dimorphic traits? And finally, what are the proximate and ultimate causes of their foraging strategies, including exploitative and interference competition? Increasing our knowledge of morphology, mechanics, and diversity of hummingbird feeding structures will have implications for understanding the ecology and evolution of these remarkable animals.

The craniomandibular anatomy of the early archosauriformEuparkeria capensisand the dawn of the archosaur skull

“…Since its initial development as at least three structures with separate origins [8], the skull has evolved in myriad directions, becoming extensively modified to yield such disparate forms as the highly kinetic cranium of snakes [9], and the much reduced cartilaginous structure seen in sharks [7]. The archosaur skull, in particular, has also seen extensive modification from its presumed initial form, yielding forms as varied as the edentulous elongated beak of hummingbirds [10], the immensely powerful jaws of hypercarnivorous theropods [11] and the uniquely flexible grazing-adapted skull of ornithischians [12]. An increased importance of vision over olfaction is in particular seen in flying archosaurs (birds and pterosaurs) [13], corresponding to the relatively larger postrostral region (and thus reduced face) connected with miniaturization and paedomorphosis in birds and their immediate relatives [14,15].…”

Nectar larceny in the trainbearers (Lesbia, Trochilidae)

“…The hypothesis that the latter trait, serration of tomia, affects nectar robbing ability and efficiency remains broadly untested. Recent studies suggest that the presence of serrations is sexually dimorphic, with greater or exclusive expression in males, and that this feature could instead be shaped by a role in plumage preening or fighting, especially male territorial defense (Rico-Guevara et al, 2019).…”

“…Consequently, it will be difficult to accumulate a great weight of evidence that exclusively support or detracts from this hypothesis. Nevertheless, it is instructive that many other specialized piercers, such as the Wedge-billed Hummingbird (Schistes geoffroyi and Purple-crowned fairy Heliothryx barroti, fail to present sexually dimorphic serrations (Rico-Guevara et al, 2019). A systematic search of nectar feeding mode, along with a number of predictors, and coupled with careful studies of feeding behavior and morphology, are likely to be most persuasive in examining the validity and generality of the Ornelas hypothesis.…”

“…Although species such as flower piercers (Diglossa, Passeriformes) are widely known to depend on nectar larceny, there are many reports of illegitimate visits by hummingbirds (Lara and Ornelas, 2001;Gonzalez and Loiselle, 2016). Some morphological characteristics of hummingbirds, including bill length and tomial serrations, are thought to be particularly closely associated with nectar larceny (Ornelas 1994, but see Rico-Guevara et al 2019).…”

“…Our highly preliminary analyses find that floral larceny is surprisingly common, at least ca. 40%, and that secondary robbing may be more common among hummingbirds than is generally appreciated, further complicating the proposed association between tomial serrations and mode of nectar foraging (Ornelas, 1994;Rico-Guevara et al, 2019).…”