Nectar feeding beyond the tongue: hummingbirds drink using phase-shifted bill opening, flexible tongue flaps and wringing at the tips.

Hummingbirds are the most speciose group of vertebrate nectarivores and exhibit striking bill variation in association with their floral food sources. To explicitly link comparative feeding biomechanics to hummingbird ecology, deciphering how they move nectar from the tongue to the throat is as important as understanding how this liquid is collected. We employed synced, orthogonally positioned, high-speed cameras to describe the bill movements, and backlight filming to track tongue and nectar displacements intraorally. We reveal that the tongue base plays a central role in fluid handling, and that the bill is neither just a passive vehicle taking the tongue inside the flower nor a static tube for the nectar to flow into the throat. Instead, we show that the bill is actually a dynamic device with an unexpected pattern of opening and closing of its tip and base. We describe three complementary mechanisms: (1) distal wringing: the tongue is wrung out as soon as it is retracted and upon protrusion, near the bill tip where the intraoral capacity is decreased when the bill tips are closed; (2) tongue raking: the nectar filling the intraoral cavity is moved mouthwards by the tongue base, leveraging flexible flaps, upon retraction; (3) basal expansion: as more nectar is released into the oral cavity, the bill base is open (phase-shifted from the tip opening), increasing the intraoral capacity to facilitate nectar flow towards the throat.

Come on baby, let's do the twist: the kinematics of killing in loggerhead shrikes.

Shrikes use their beaks for procuring, dispatching and processing their arthropod and vertebrate prey. However, it is not clear how the raptor-like bill of this predatory songbird functions to kill vertebrate prey that may weigh more than the shrike itself. In this paper, using high-speed videography, we observed that upon seizing prey with their beaks, shrikes performed rapid (6-17 Hz; 49-71 rad s-1) axial head-rolling movements. These movements accelerated the bodies of their prey about their own necks at g-forces of approximately 6 g, and may be sufficient to cause pathological damage to the cervical vertebrae and spinal cord. Thus, when tackling relatively large vertebrates, shrikes appear to use inertia of their prey's own body against them.

Functional morphology of hummingbird bill tips: their function as tongue wringers.

Nectarivores are animals that have evolved adaptations to efficiently exploit floral nectar as the main source of energy in their diet. It is well known that hummingbirds can extract nectar with impressive speed from flowers. However, despite decades of study on nectar intake rates, the mechanism by which feeding is ultimately achieved - the release of nectar from the tongue so that it can pass into the throat and be ingested - has not been elucidated. By using microCT scanning and macro high-speed videography we scrutinized the morphology and function of hummingbird bill tips, looking for answers about the nectar offloading process. We found near the bill tip, in an area of strong lateral compression of internal mandibular width, that the tomia (cutting edges of the bill) are thinner, partially inrolled, and hold forward-directed serrations. Aligned with these structures, a prominent pronglike structure projects upward and forward from the internal mandibular keel. Distal to this mandibular prong, another smaller maxillary prong protrudes downwards from the keel of the palate. Four shallow basins occur at the base of the mandibular prong on the mandibular floor. Of these, two are small basins located proximally and at the sides of the mandibular prong. A third, slightly larger basin is positioned distally to the first two and directly under the maxillary prong. And the fourth basin, the largest, is found more proximally where the bill becomes thicker, as seen from the side. We documented that this group of structures is integrated into the area of the bill where tongue extrusion occurs, and we hypothesize that they function to enhance the nectar release at each lick. We suggest that this "wringer", operated by bill and tongue movements, helps to move nectar towards the throat.

Hummingbird tongues are elastic micropumps.

Pumping is a vital natural process, imitated by humans for thousands of years. We demonstrate that a hitherto undocumented mechanism of fluid transport pumps nectar onto the hummingbird tongue. Using high-speed cameras, we filmed the tongue-fluid interaction in 18 hummingbird species, from seven of the nine main hummingbird clades. During the offloading of the nectar inside the bill, hummingbirds compress their tongues upon extrusion; the compressed tongue remains flattened until it contacts the nectar. After contact with the nectar surface, the tongue reshapes filling entirely with nectar; we did not observe the formation of menisci required for the operation of capillarity during this process. We show that the tongue works as an elastic micropump; fluid at the tip is driven into the tongue's grooves by forces resulting from re-expansion of a collapsed section. This work falsifies the long-standing idea that capillarity is an important force filling hummingbird tongue grooves during nectar feeding. The expansive filling mechanism we report in this paper recruits elastic recovery properties of the groove walls to load nectar into the tongue an order of magnitude faster than capillarity could. Such fast filling allows hummingbirds to extract nectar at higher rates than predicted by capillarity-based foraging models, in agreement with their fast licking rates.

Nest-building behavior of Monk Parakeets and insights into potential mechanisms for reducing damage to utility poles.

The Monk Parakeet (Myiopsitta monachus) commonly uses utility poles as a substrate for building large, bulky nests. These nests often cause fires and electric power outages, creating public safety risks and increasing liability and maintenance costs for electric companies. Previous research has focused on lethal methods and chemical contraception to prevent nesting on utility poles and electrical substations. However, implementation of lethal methods has led to public protests and lawsuits, while chemical contraception may affect other than the targeted species, and must be continually reapplied for effectiveness. One non-lethal alternative, nest removal, is costly and may not be a sustainable measure if Monk Parakeet populations continue to grow. In order to identify cost-effective non-lethal solutions to problems caused by Monk Parakeet nesting, we studied their behavior as they built nests on utility poles. Monk Parakeets initiate nests by attaching sticks at the intersection of the pole and electric lines. We found that parakeets use the electric lines exclusively to gain access to the intersection of lines and pole during nest initiation, and continue to use the lines intensively throughout construction. Monk Parakeets also have more difficulty attaching sticks during the early stages of nest construction than when the nest is nearing completion. These findings suggest that intervention during the earlier stages of nest building, by excluding Monk Parakeets from electric lines adjacent to poles, may be an effective, non-lethal method of reducing or eliminating parakeets nesting on, and damaging, utility poles.

The hummingbird tongue is a fluid trap, not a capillary tube.

Hummingbird tongues pick up a liquid, calorie-dense food that cannot be grasped, a physical challenge that has long inspired the study of nectar-transport mechanics. Existing biophysical models predict optimal hummingbird foraging on the basis of equations that assume that fluid rises through the tongue in the same way as through capillary tubes. We demonstrate that the hummingbird tongue does not function like a pair of tiny, static tubes drawing up floral nectar via capillary action. Instead, we show that the tongue tip is a dynamic liquid-trapping device that changes configuration and shape dramatically as it moves in and out of fluids. We also show that the tongue-fluid interactions are identical in both living and dead birds, demonstrating that this mechanism is a function of the tongue structure itself, and therefore highly efficient because no energy expenditure by the bird is required to drive the opening and closing of the trap. Our results rule out previous conclusions from capillarity-based models of nectar feeding and highlight the necessity of developing a new biophysical model for nectar intake in hummingbirds. Our findings have ramifications for the study of feeding mechanics in other nectarivorous birds, and for the understanding of the evolution of nectarivory in general. We propose a conceptual mechanical explanation for this unique fluid-trapping capacity, with far-reaching practical applications (e.g., biomimetics).

Feeding mechanisms: Hummingbird jaw bends to aid insect capture.

The upper jaws of birds, unlike those in many tetrapods, move relative to the skull and are often flexible along their length, whereas the lower jaw (mandible) is usually a rigid structure formed by the fusion of several bones, flexing only where it meets the skull. Here we describe a previously unnoticed mandibular bending movement in hummingbirds, in which the distal half of the mandible is actively flexed downwards and the gape widens to catch flying insects. The hummingbird is thought to have developed a long narrow bill as it specialized in feeding on floral nectar, but the bird's need to supplement its diet with insects must have contributed to the surprising flexibility of its jaw.

Sexual size dimorphism in red-necked phalaropes and functional significance of nonsexual bill structure variation for feeding performance.

Sexual size dimorphism is widespread in shorebirds, yet no tests of the assumption that such size dimorphism extends to functionally significant dimensions of the bill exist. This report presents tests of: (1) the assumption that sexual size dimorphism extends to the feeding structures in sexually size dimorphic bird, and (2) the hypothesis that bill-size variation influences feeding performance in Phalaropus lobatus, the red-necked phalarope. Discriminant function analysis revealed that the sexes of this species can be distinguished on the basis of five body size/bill length variables, but with low accuracy in sexing of females because of misclassification of small females as males. In the shorebird literature, the assumption is generally made that in the absence of selection to the contrary, bill size scales to body size and hence sexual size dimorphism extends to bill size. However, discriminant function analysis of measures from red-necked phalaropes failed to separate the sexes on the basis of either external or internal bill dimensions other than length. Nonetheless, internal dimensions of the upper jaw combined with exposed culmen length explained 86% of the variance in feeding performance of phalaropes; high feeding performance depends on a wide, shallow, complex internal bill structure. This study provides evidence that internal bill dimensions determine feeding performance in a manner consistent with the mechanics of surface tension transport of prey. These results suggest that some dimensions of bill size may be constrained by performance demands and demonstrate that variation in bill morphology has functional consequences. © 1996 Wiley-Liss, Inc.