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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.
... Once the tongue is loaded, and retracted into the hummingbird's mouth, different mechanisms are involved in the middle stageoffloadingand the final stageintraoral transport of nectar up the elongate bill, and swallowing of nectar (stages sensu Cuban et al., 2022). These stages are poorly known and the surrounding hypotheses come mostly from morphological studies. ...
... Nonetheless, the transport of the nectar from the tongue to the pharynx is still concealed inside the keratinized and often melanized beak, and hence thus far it has been a 'black box'. As nectar extraction must often work against gravity (or without its aid), multiple authors have proposed intraoral transport hypotheses (reviewed by Rico-Guevara, 2014;Cuban et al., 2022); briefly summarized as follows. (1) Cohesive pulling: when a structure moves proximally, it uses forces between water molecules to pull fluid attached to its surface (e.g. the tongue retracts, pulling adhered nectar), analogous to dragging a drop over a leaf with your finger. ...
... The first hypotheses on how nectar is moved through the bill to be swallowed date back to the 19th century, with renewed attention in the 1980s and within the last 20 years (reviewed in Rico-Guevara, 2014;Cuban et al., 2022). There seem to be a variety of potential solutions to the fluid dynamics challenge of efficiently and delicately extracting minute amounts of nectar, which often requires thin and elongated beaks and protrusible tongues to reach inside long and tubular flowers . ...
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.
... For example, the hummingbird tongue cannot function as a drinking straw because the grooves are open dorsally, precluding the formation of a pressure gradient . 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 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). ...
Nectar‐feeding birds provide an excellent system in which to examine form‐function relationships over evolutionary time. There are many independent origins of nectarivory in birds, and nectar feeding is a lifestyle with many inherent biophysical constraints. We review the morphology and function of the feeding apparatus, the locomotor apparatus, and the digestive and renal systems across avian nectarivores with the goals of synthesizing available information and identifying the extent to which different aspects of anatomy have morphologically and functionally converged. In doing so, we have systematically tabulated the occurrence of putative adaptations to nectarivory across birds and created what is, to our knowledge, the first comprehensive summary of adaptations to nectarivory across body systems and taxa. We also provide the first phylogenetically informed estimate of the number of times nectarivory has evolved within Aves. Based on this synthesis of existing knowledge, we identify current knowledge gaps and provide suggestions for future research questions and methods of data collection that will increase our understanding of the distribution of adaptations across bodily systems and taxa, and the relationship between those adaptations and ecological and evolutionary factors. We hope that this synthesis will serve as a landmark for the current state of the field, prompting investigators to begin collecting new data and addressing questions that have heretofore been impossible to answer about the ecology, evolution, and functional morphology of avian nectarivory. This article is protected by copyright. All rights reserved.
... Measures of wettability, viscosity and surface tension of fluids imbibed by the bill will help us better understand the mechanics of the bill during nectar feeding, and hummingbirds are an ideal system for such a study on account of their diverse bill shapes. Recent research shows that simple capillary action does not explain the nectar feeding of birds such as hummingbirds, and demonstrates the crucial role probably played by the bill in offloading nectar from the tongue and in generating suction forces to draw nectar to the back of the oral cavity (Cuban et al., 2022). Hummingbirds also use their bills in territorial combat, where rigid, pointed bills perform better. ...
The field of comparative biomechanics examines how form, mechanical properties and environmental interactions shape the function of biological structures. Biomechanics has advanced by leaps and bounds as rapid technological progress opens up new research horizons. In this Review, I describe how our understanding of the avian bill, a morphologically diverse multifunctional appendage, has been transformed by employing a biomechanical perspective. Across functions from feeding to excavating hollows in trees and as a vocal apparatus, the study of the bill spans both solid and fluid biomechanics, rendering it useful to understand general principles across disciplines. The different shapes of the bill across bird species result in functional and mechanical trade-offs, thus representing a microcosm of many broader form-function questions. Using examples from diverse studies, I discuss how research into bird bills has been shaped over recent decades, and its influence on our understanding of avian ecology and evolution. Next, I examine how bill material properties and geometry influence performance in dietary and non-dietary contexts, simultaneously imposing trade-offs on other functions. Following an examination of the interactions of bills with fluids and their role as part of the vocal apparatus, I end with a discussion of the sensory biomechanics of the bill, focusing specifically on the bill-tip mechanosensory organ. With these case studies, I highlight how this burgeoning and consequential field represents a roadmap for our understanding of the function and evolution of biological structures.
Johnson gives an overview of bird pollinators and the plant species they pollinate.
Physical principles and laws determine the set of possible organismal phenotypes. Constraints arising from development, the environment, and evolutionary history then yield workable, integrated phenotypes. We propose a theoretical and practical framework that considers the role of changing environments. This 'ecomechanical approach' integrates functional organismal traits with the ecological variables. This approach informs our ability to predict species shifts in survival and distribution and provides critical insights into phenotypic diversity. We outline how to use the ecomechanical paradigm using drag-induced bending in trees as an example. Our approach can be incorporated into existing research and help build interdisciplinary bridges. Finally, we identify key factors needed for mass data collection, analysis, and the dissemination of models relevant to this framework.
Research that integrates animal behavior theory with mechanics—including biomechanics, physiology, and functional morphology—can reveal how organisms accomplish tasks crucial to their fitness. Despite the insights that can be gained from this interdisciplinary approach, biomechanics commonly neglects a behavioral context and behavioral research generally does not consider mechanics. Here, we aim to encourage the study of “mechanoethology,” an area of investigation intended to encompass integrative studies of mechanics and behavior. Using examples from the literature, including papers in this issue, we show how these fields can influence each other in three ways: 1) the energy required to execute behaviors is driven by the kinematics of movement, and mechanistic studies of movement can benefit from consideration of its behavioral context; 2) mechanics sets physical limits on what behaviors organisms execute, while behavior influences ecological and evolutionary limits on mechanical systems; and 3) sensory behavior is underlain by the mechanics of sensory structures, and sensory systems guide whole-organism movement. These core concepts offer a foundation for mehanoethology research. However, future studies focused on merging behavior and mechanics may reveal other ways by which these fields are linked, leading to further insights in integrative organismal biology.
Despite having a trunk that weighs over 100 kg, elephants mainly feed on lightweight vegetation. How do elephants manipulate such small items? In this experimental and theoretical investigation, we filmed elephants at Zoo Atlanta showing that they can use suction to grab food, performing a behaviour that was previously thought to be restricted to fishes. We use a mathematical model to show that an elephant’s nostril size and lung capacity enables them to grab items using comparable pressures as the human lung. Ultrasonographic imaging of the elephant sucking viscous fluids show that the elephant’s nostrils dilate up to 30 % in radius, which increases the nasal volume by 64 % . Based on the pressures applied, we estimate that the elephants can inhale at speeds of over 150 m s ⁻¹ , nearly 30 times the speed of a human sneeze. These high air speeds enable the elephant to vacuum up piles of rutabaga cubes as well as fragile tortilla chips. We hope these findings inspire further work in suction-based manipulation in both animals and robots.
One of the reasons why flowering plants became the most diverse group of land plants is their association with animals to reproduce. The earliest examples of this mutualism involved insects foraging for food from plants and, in the process, pollinating them. Vertebrates are latecomers to these mutualisms, but birds, in particular, present a wide variety of nectar-feeding clades that have adapted to solve similar challenges. Such challenges include surviving on small caloric rewards widely scattered across the landscape, matching their foraging strategy to nectar replenishment rate, and efficiently collecting this liquid food from well-protected chambers deep inside flowers. One particular set of convergent traits among plants and their bird pollinators has been especially well studied: the match between the shape and size of bird bills and ornithophilous flowers. Focusing on a highly specialized group, hummingbirds, we examine the expected benefits from bill-flower matching, with a strong focus on the benefits to the hummingbird and how to quantify them. Explanations for the coevolution of bill-flower matching include 1) that the evolution of traits by bird-pollinated plants, such as long and thin corollas, prevents less efficient pollinators (e.g., insects) from accessing the nectar, and 2) that increased matching, as a result of reciprocal adaptation, benefits both the bird (nectar extraction efficiency) and the plant (pollen transfer). In addition to nectar feeding, we discuss how interference and exploitative competition also play a significant role in the evolution and maintenance of trait matching. We present hummingbird-plant interactions as a model system to understand how trait matching evolves and how pollinator behavior can modify expectations based solely on morphological matching, and discuss the implications of this behavioral modulation for the maintenance of specialization. While this perspective piece directly concerns hummingbird-plant interactions, the implications are much broader. Functional trait matching is likely common in coevolutionary interactions (e.g., in predator-prey interactions), yet the physical mechanisms underlying trait matching are understudied and rarely quantified. We summarize existing methods and present novel approaches that can be used to quantify key benefits to interacting partners in a variety of ecological systems.
Nectarivorous insects generally adopt suction or lapping to extract nectar from flowers and it is believed that each species exhibits one specific feeding pattern. In recent literature, large groups of nectarivores are classified as either 'suction feeders', imbibing nectar through their proboscis, or 'lappers', using viscous dipping. Honeybees (Apis mellifera) are the well-known lappers by virtue of their hairy tongues. Surprisingly, we found that honeybees also employ active suction when feeding on nectar with low viscosity, defying their classification as lappers. Further experiments showed that suction yielded higher uptake rates when ingesting low-concentration nectar, while lapping resulted in faster uptake when ingesting nectar with higher sugar content. We found that the optimal concentration of suction mode in honeybees coincided with the one calculated for other typical suction feeders. Moreover, we found behavioural flexibility in the drinking mode: a bee is able to switch between lapping and suction when offered different nectar concentrations. Such volitional switching in bees can enhance their feeding capabilities, allowing them to efficiently exploit the variety of concentrations presented in floral nectars, enhancing their adaptability to a wide range of energy sources.
Nectarivorous birds and bird-pollinated plants are linked by a network of interactions. Here I ask how these interactions influence evolution and community composition. I find near complete evidence for the effect of birds on plant evolution. Experiments show the process in action—birds select among floral phenotypes in a population—and comparative studies find the resulting pattern—bird-pollinated species have long-tubed, red flowers with large nectar volumes. Speciation is accomplished in one “magical” step when adaptation for bird pollination brings about divergent morphology and reproductive isolation. In contrast, evidence that plants drive bird evolution is fragmentary. Studies of selection on population-level variation are lacking, but the resulting pattern is clear—nectarivorous birds have evolved a remarkable number of times and often have long bills and brush-tipped or tubular tongues. At the level of the ecological guild, birds select among plant species via an effect on seed set and thus determine plant community composition. Plants simultaneously influence the relative fitness of bird species and thus determine the composition of the bird guild. Interaction partners may give one guild member a constant fitness advantage, resulting in competitive exclusion and community change, or may act as limiting resources that depress the fitness of frequent species, thus stabilizing community composition and allowing the coexistence of diversity within bird and plant guilds.
Expected final online publication date for the Annual Review of Ecology, Evolution, and Systematics, Volume 50 is November 4, 2019. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
Streptognathism (twisted jaw, in Latin) is defined as a voluntary medio-lateral bowing of the mandibular rami by action of the jaw muscles. Gape expansion results from two flexion zones along the mandible, one near the mandibular symphysis (distal) and the other along the posterior third of the bill, approximately below the distal edge of the orbit. Bowing occurs when the bill is open and the rami are twisted and
rotated outward, causing the distal portion of the mandible to bend downward and lateral gape size (intra-ramal space) to enlarge. This expansion is different in hermits (subfamily Phaethorninae) vs. non-hermits (Trochilinae).
Surface tension force plays a vital role when the length scale of a
system is small (i.e., in the micro/nano meter range). In the case of compliant
structures and soft substrates, the competition between interfacial energy and
elastic strain energy in the bulk gives rise to many interesting phenomena.
Elastocapillarity refers to the study of the effects of deformation of flexible
structures or soft substrates under the action of capillary forces. In contrast to
rigid structures/substrates, the liquid surface tension force at the three-phase
contact line could deform compliant structures or soft solids, thus resulting in
interesting dynamics. The elastocapillary interaction between liquid and solid can
give rise to stiction in microstructures, wrapping of droplet by flexible
structures, buckling of fibres, and ridge formation at the contact line of a droplet
on a soft substrate. Besides, recent research has shown that elastocapillarity can
aid in the manipulation of liquid flow through flexible confinements and over soft
substrates. Here, we report an extensive review of the literature on
elastocapillarity mainly focusing on the elastocapillary-based liquid transport. The
research in the field has been broadly classified into three different categories:
liquid flow in compliant microchannels, liquid flow in flexible structures, and
transport of droplets over soft elastic substrates. In each of the above cases,
theoretical understanding of the mechanism responsible for liquid transport, and
experimental studies leading to interesting results and observations are presented
and discussed. Numerical modelling of elastocapillarity phenomena is also presented.
Finally, we discuss the research challenges and future directions in the field of
elastocapillarity-based transport of liquids.
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.
Aim: Among the world’s three major nectar-feeding bird taxa, hummingbirds are the most phenotypically specialized for nectarivory, followed by sunbirds, while the honeyeaters are the least phenotypically specialized taxa. We tested whether this phenotypic specialization gradient is also found in the interaction patterns with their floral resources.
Location: Americas, Africa, Asia and Oceania/Australia.
Methods: We compiled interaction networks between birds and floral resources for 79 hummingbird, nine sunbird and 33 honeyeater communities. Interaction specialization was quantified through connectance (C), complementary specialization (H2’), binary (QB) and weighted modularity (Q), with both observed and null-model corrected values. We compared interaction specialization among the three types of bird–flower communities, both independently and while controlling for potential confounding variables, such as plant species richness, asymmetry, latitude, insularity, topography, sampling methods and intensity.
Results: Hummingbird–flower networks were more specialized than honeyeater–flower networks. Specifically, hummingbird–flower networks had a lower proportion of realized interactions (lower C), decreased niche overlap (greater H2’) and greater modularity (greater QB). However, we found no significant differences between hummingbird– and sunbird–flower networks, nor between sunbird– and honeyeater–flower networks.
Main conclusions: As expected, hummingbirds and their floral resources have greater interaction specialization than honeyeaters, possibly because of greater phenotypic specialization and greater floral resource richness in the New World. Interaction specialization in sunbird–flower communities was similar to both hummingbird–flower and honeyeater–flower communities. This may either be due to the relatively small number of sunbird–flower networks available, or because sunbird–flower communities share features of both hummingbird–flower communities (specialized floral shapes) and honeyeater–flower communities (fewer floral resources). These results suggest a link between interaction specialization and both phenotypic specialization and floral resource richness within bird–flower communities at a global scale.
A complete understanding of the feeding structures is fundamental in order to study how animals survive. Some birds use long and protrusible tongues as the main tool to collect their central caloric source (e.g., woodpeckers and nectarivores). Hummingbirds are the oldest and most diverse clade of nectarivorous vertebrates, being a perfect subject to study tongue specializations. Their tongue functions to intraorally transport arthropods through their long bills and enables them to exploit the nectarivorous niche by collecting small amounts of liquid, therefore it is of vital importance to study its anatomy and structure at various scales. I focused on the portions of the hummingbird tongue that have been shown to be key for understanding their feeding mechanisms. I used histology, transmission and scanning electron microscopy, microCT, and ex-vivo experiments in order to advance the comprehension of the morphology and functioning of the hummingbird feeding apparatus. I found that hummingbird tongues are composed mainly of thin cornified epithelium, lack papillae, and completely fill the internal cast of the rostral oropharyngeal cavity. Understanding this puzzle-piece match between bill and tongue will be essential for the study of intraoral transport of nectar. Likewise, I found that the structural composition and tissue architecture of the tongue groove walls provide the rostral portion of the tongue with elastic properties that are central to the study of tongue-nectar interactions during the feeding process. Detailed studies on hummingbirds set the basis for comparisons with other nectar-feeding birds and contribute to comprehend the natural solutions to collecting liquids in the most efficient way possible.
My research aims to answer the questions: How do hummingbirds feed? And, how do the mechanics of feeding define the limits and adaptive values of feeding behaviors? I meticulously study every step of nectar capture and ingestion. My dissertation chapters are organized following a morpho-functional and feeding sequence approach: 1) Feeding Apparatus Morphology; with emphasis on the understudied morphology of the tongue grooves and bill tongue coupling. 2) Tongue Tip Dynamics; how hummingbird tongues entrap nectar. 3) Tongue Grooves Functioning: how the tongue acts as an elastic micropump while collecting nectar. 4) Bill Tip Mechanics; internal bill structures that aid in offloading nectar from the tongue. 5) Intraoral Transport: how the nectar flows inside the bill to the throat where it can finally be swallowed. My results demonstrate that capillarity equations are unsuitable to calculate energy intake rate, which is the building unit of foraging theories; therefore a development of a new theoretical framework to study hummingbird energetics and foraging ecology is needed. I describe previously unknown methods of tongue-based nectar collection, report undocumented tongue and bill structures, and offer the first test of intraoral transport hypotheses. I followed the scientific method cycle of deduction and induction. To understand the determinants of hummingbird feeding mechanics in an ecological context, I tested biophysical model predictions using data from wild birds. Elucidating the drinking mechanism of hummingbirds will facilitate downstream calculations of the rates at which birds can obtain nectar along several environmental axes (e.g. altitudinal and latitudinal ranges, migrations, corolla morphology, etc.). This will in turn inform how and where the limits of nectar uptake have shaped the distribution, ecology and evolution of hummingbirds. With their enchanting appeal and unique physical capabilities, hummingbirds captivate people of all ages. As such, they serve as ambassadors to the natural world, fostering public appreciation for scientific and conservation efforts aimed at preserving these fascinating birds, and the biodiversity upon which they depend.
To a hummingbird, clusters of flowers on inflorescences represent patches and provide an ideal situation to test prediction of optimal patch-use. The basic question is what decision rule should a hummingbird use to decide whether or not to leave an inflorescence? The hypothesis is that hummingbirds will adopt the decision rule that maximizes their net rate of energy gain while foraging. This hypothesis leads to an analogue of Charnov's marginal value theorem which determines an optimal decision rule. The optimal decision ruleis then used to predict aspects of the hummingbirds' foraging, and these predictions are compared with field data
The optimal decision rule is a function of how much information is used by the hummingbirds. Data indicate that a decision to leave an inflorescence is a function of the number of flowers visited, the number of flowers available on the inflorescence, and the amount of nectar obtained at the last flower. The optimal decision rule was calculated assuming no additional information is used.
Nectarivorous birds and bats have evolved highly specialized tongues to gather nectar from flowers. Here, we show that a nectar-feeding bat, Glossophaga soricina, uses dynamic erectile papillae to collect nectar. In G. soricina, the tip of the tongue is covered with long filamentous papillae and resembles a brush or mop. During nectar feeding, blood vessels within the tongue tip become engorged with blood and the papillae become erect. Tumescence and papilla erection persist throughout tongue retraction, and nectar, trapped between the rows of erect papillae, is carried into the mouth. The tongue tip does not increase in overall volume as it elongates, suggesting that muscle contraction against the tongue's fixed volume (i.e., a muscular hydrostat) is primarily responsible for tip elongation, whereas papilla erection is a hydraulic process driven by blood flow. The hydraulic system is embedded within the muscular hydrostat, and, thus, intrinsic muscle contraction may simultaneously increase the length of the tongue and displace blood into the tip. The tongue of G. soricina, together with the tongues of nectar-feeding bees and hummingbirds, which also have dynamic surfaces, could serve as valuable models for developing miniature surgical robots that are both protrusible and have highly dynamic surface configurations.
Adaptations of the nectar traits in bird-pollinated flowers are amongst the most discussed aspects of floral evolution. In the case of sunbird-pollinated plants, data on nectar traits originate almost exclusively from the South African region and are very scarce for tropical Africa, where paradoxically the highest sunbird diversity occurs. Here we present a study on the nectar properties of a sunbird-pollinated plant, Impatiens sakeriana, growing in the West African mountains, including the nectar production, diurnal changes in the nectar standing crop, the nectar concentrations, the nectar volumes, total sugar amounts and sugar composition. Moreover we compare the nectar traits of I. sakeriana with six other co-flowering insect-visited plant species. Our results showed that many nectar properties, including high volume (approx. 38 μL in flowers unvisited by sunbirds), low sugar concentration (approx. 30% w/w) and high sucrose content (95%), are specific to I. sakeriana, compared to the insect-visited plants. These are in accordance with the most recent theory that nectar properties of the sunbird-pollinated plants are similar to those pollinated by hummingbirds.
We present the results of a combined experimental and theoretical investigation of the dynamics of drinking in ruby-throated hummingbirds. In vivo observations reveal elastocapillary deformation of the hummingbird's tongue and capillary suction along its length. By developing a theoretical model for the hummingbird's drinking process, we investigate how the elastocapillarity affects the energy intake rate of the bird and how its open tongue geometry reduces resistance to nectar uptake. We note that the tongue flexibility is beneficial for accessing, transporting and unloading the nectar. We demonstrate that the hummingbird can attain the fastest nectar uptake when its tongue is roughly semicircular. Finally, we assess the relative importance of capillary suction and a recently proposed fluid trapping mechanism, and conclude that the former is important in many natural settings.
Aim We review several aspects of the structure of regional and local assemblages of nectar-feeding birds and bats and their relationships with food plants to determine the extent to which evolutionary convergence has or has not occurred in the New and Old World tropics.Location Our review is pantropical in extent and also includes the subtropics of South Africa and eastern Australia. Within the tropics, it deals mostly with lowland forest habitats.Methods An extensive literature review was conducted to compile data bases on the regional and local species richness of nectar-feeding birds and bats, pollinator sizes, morphology, and diets. Coefficients of variation (CVs) were used to quantify the morphospace occupied by the various families of pollinators. The extent to which plants have become evolutionarily specialized for vertebrate pollination was explored using several criteria: number and diversity of growth forms of plant families providing food for all the considered pollinator families; the most common flower morphologies visited by all the considered pollinator families; and the number of plant families that contain genera with both bird- and bat-specialized species.Results Vertebrate pollinator assemblages in the New World tropics differ from those in the Old World in terms of their greater species richness, the greater morphological diversity of their most specialized taxa, and the greater degree of taxonomic and ecological diversity and morphological specialization of their food plants. Within the Old World tropics, Africa contains more specialized nectar-feeding birds than Asia and Australasia; Old World nectar-feeding bats are everywhere less specialized than their New World counterparts.Main conclusions We propose that two factors – phylogenetic history and spatio-temporal predictability (STP) of flower resources – largely account for hemispheric and regional differences in the structure of vertebrate pollinator assemblages. Greater resource diversity and resource STP in the New World have favoured the radiation of small, hovering nectar-feeding birds and bats into a variety of relatively specialized feeding niches. In contrast, reduced resource diversity and STP in aseasonal parts of Asia as well as in Australasia have favoured the evolution of larger, non-hovering birds and bats with relatively generalized feeding niches. Tropical Africa more closely resembles the Neotropics than Southeast Asia and Australasia in terms of resource STP and in the niche structure of its nectar-feeding birds but not its flower-visiting bats.
Nectar properties tend to be similar for plants visited by the same kinds of pollinators, and much of the available information on nectar chemistry has been collected in the context of pollination syndromes. These are defined as broad associations between floral features and types of animal pollinators (Faegri & van der Pijl, 1979; Proctor et al., 1996) and are discussed further by Nicolson (2007, Chapter 7 in this volume). Faegri and van der Pijl included nectar volume in their classic descriptions of the various syndromes. The concept was extended to include nectar chemistry (specifically sugar and amino acid content and composition) in the influential reviews of Baker and Baker (1982a 1983b). Herbert and Irene Baker analysed many different substances in nectar and were largely responsible for drawing attention to its chemical complexity. However, the adaptive significance of nectar components has perhaps been overemphasized and is now being examined more critically.
Hummingbirds have two main foraging strategies: territoriality (defending a patch of flowers) and traplining (foraging over routine circuits of isolated patches). Species are often classified as employing one or the other. Not only have these strategies been inconsistently defined within the behavioral literature, but this simple framework also neglects the substantial evidence for flexible foraging behavior displayed by hummingbirds. Despite these limitations, research on hummingbird foraging has explored the distinct avenues of selection that proponents of either strategy presumably face: trapliners maximizing foraging efficiency, and territorialists favoring speed and maneuverability for resource defense. In earlier studies, these functions were primarily examined through wing disc loading (ratio of body weight to the circular area swept out by the wings, WDL) and predicted hovering costs, with trapliners expected to exhibit lower WDL than territorialists and thus lower hovering costs. While these pioneering models continue to play a role in current research, early studies were constrained by modest technology, and the original expectations regarding WDL have not held up when applied across complex hummingbird assemblages. Current technological advances have allowed for innovative research on the biomechanics/energetics of hummingbird flight, such as allometric scaling relationships (e.g., wing area–flight performance) and the link between high burst lifting performance and territoriality. Providing a predictive framework based on these relationships will allow us to reexamine previous hypotheses, and explore the biomechanical trade-offs to different foraging strategies, which may yield divergent routes of selection for quintessential territoriality and traplining. With a biomechanical and morphofunctional lens, here we examine the locomotor and energetic facets that dictate hummingbird foraging, and provide a) predictions regarding the behavioral, biomechanical, and morphofunctional associations with territoriality and traplining; and b) proposed methods of testing them. By pursuing these knowledge gaps, future research could use a variety of traits to help clarify the operational definitions of territoriality and traplining, to better apply them in the field.
A conspicuous feature of extant tetrapods is a movable tongue that plays a role in food uptake, mastication, and swallowing. The tongue is a muscle mass covered by a mucosal sheath, but the tongues of amphibians, reptiles, birds, and mammals are diverse in general morphology and function. For example, in frogs and toads, a component of the musculus genioglossus serves as an intrinsic tongue muscle, with the anterior part of the tongue attached to the floor of the oral cavity. Nevertheless, these features of the tongue have allowed Anurans to diversify and disperse worldwide. On the other hand, the salamander tongue is connected to the oral cavity by a root with a cartilage or a bony skeleton, and it is mainly comprised of projection and retractor muscles. In this respect, the salamander tongue seems more similar to that of reptiles and mammals than to those of frogs and toads. The morphology and function of the tongues of some reptiles, such as chameleons, and some mammals, such as nectar-feeding bats, are examples of extreme specialization. Finally, the tongue has become almost vestigial in a few species of anurans, turtles, and birds. This review summarizes and discusses many specializations of tongue form and function among tetrapods.
We start with a general description of the structure of the feeding apparatus in birds (Sect. 17.1), then we describe the biomechanics of those parts (Sect. 17.2), including a review of contemporary approaches to the study of bird feeding morphology and function. We establish explicit links between form and function, and consequent relations to foraging behaviors. In Sect. 17.3, we systematically explore the vast diversity of bird feeding environments by grouping foraging (searching) and feeding (handling—consumption) mechanisms that birds use on land, air, and water. Each one of these subsections addresses not only what birds eat, but also how they feed. We dedicate a separate Sect. (17.4) to drinking because most birds have to perform this process regardless of their diet, and often using different mechanisms than the ones they use to feed. We then discuss evolutionary forces and patterns in bird feeding (convergences, radiations, trade-offs, etc.), including functions different from handling and ingestion that also act to shape the feeding apparatus in birds (Sect. 17.5).
Nectar-drinking bats and honeybees have tongues covered with hairlike structures, enhancing their ability to take up viscous nectar by dipping. Using a combination of model experiments and theory, we explore the physical mechanisms that govern viscous entrainment in a hairy texture. Hairy surfaces are fabricated using laser cut molds and casting samples with polydimethylsiloxane (PDMS) elastomer. We model the liquid trapped within the texture using a Darcy-Brinkmann-like approach and derive the drainage flow solution. The amount of fluid that is entrained is dependent on the viscosity of the fluid, the density of the hairs, and the withdrawal speed. Both experiments and theory reveal an optimal hair density to maximize fluid uptake.
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.
Contrast imaging studies are routinely performed in avian patients when an underlying abnormality of the gastrointestinal (GI) tract is suspected. Fluoroscopy offers several advantages over traditional radiography and can be performed in conscious animals with minimal stress and restraint. Although birds of prey are commonly encountered as patients, little is known about GI transit times and contrast imaging studies in these species, especially owls. Owls are commonly encountered in zoological, educational, and wildlife settings. In this study, 12 adult barred owls (Strix varia) were gavage fed a 30% weight-by-volume barium suspension (25 mL/kg body weight). Fluoroscopic exposures were recorded at 5, 15, 30, 60, 120, 180, 240, and 300 minutes after administration. Overall GI transit time and transit times of various GI organs were recorded. Median (interquartile range [IQR]) overall GI transit time was 60 minutes (IQR: 19–60 minutes) and ranged from 5–120 minutes. Ventricular and small intestinal contrast filling was rapid. Ventricular emptying was complete by a median of 60 minutes (IQR: 30–120 minutes; range: 30–240 minutes), whereas small intestinal emptying was not complete in 9/12 birds by 300 minutes. Median small intestinal contraction rate was 15 per minute (IQR: 13–16 minutes; range: 10–19 minutes). Median overall GI transit time in barred owls is more rapid than mean transit times reported for psittacine birds and red-tailed hawks (Buteo jamaicensis). Fluoroscopy is a safe, suitable method for investigating GI motility and transit in this species.
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.
© 2015 The Author(s).
Historically, comparative study of the skeleton of hummingbirds has focused on systematics, emphasizing differences between hummingbirds and other birds and only rarely addressing differences within Trochilidae. This monograph covers both approaches, and comparisons within Trochilidaeare framed within recently published, plausible phylogenetic hypotheses. The data are derived mainly from museum collections of anatomical specimens, covering ~256 species of 102 genera of hummingbirds, and 11 genera of other Apodiformes. Although the syringeal skeleton is included, emphasis is on the axial and appendicular skeletons. The first section deals with the syrinx and with skeletal features mainly associated with nectarivory and hovering, emphasizing characters that are unique to hummingbirds within Apodiformes. The syrinx of hummingbirds lies in the neck rather than the thorax and displays a unique bony knob on the surface of the tympanic membrane. During posthatching development, the upper jaw of hummingbirds undergoes metamorphic changes that produce a morphology uniquely adapted for nectarivory within Aves. The ventral bars of the upper jaw lengthen and rotate to become lateral walls of an incompletely tubular bill that is completed by the closed mandibula, and lateral bowing (streptognathism) of the mandibula helps to seal the tube while a bird drinks nectar. Streptognathism of the opened jaw is used in display by some Hermits. The lamellar tip of the tongue required for nectar uptakealso develops after fledging, while young are still fed by the parent. In Trochilines the nasal region changes from its configuration by bone resorption during posthatching development. Cranial kinesis in hummingbirds is poorly documented, but structural differences in the upper jaw of Hermits and Trochilines imply differences in cranial kinesis. The palatum of hummingbirds is distinguished from that of other apodiforms by extreme reduction of the lateral part of the palatinum, greater width of the ventral choanal region, and by a median spine on the vomer. Otherwise the vomer is variable in shape and not compatible with aegithognathism. Among cranial features, the basipterygoid process, lacrimale, and jugale are absent, and the interorbital septum is complete. The hyobranchial apparatus differs from that of other apodiforms in having an epibranchiale that is longer than the ceratobranchiale, and variably elongate in relation to body size. I hypothesize two modes of hyobranchial function-one applicable to moderate protrusion of the tongue (typical nectar eating), and another to extreme protrusion. The pelvis is less strongly supported by the synsacrum, and the proximal portion of the hind limb is more reduced than in other Apodiformes. By contrast, the tarsometatarsus and flexor muscles of the toes are well developed in association with perching and clinging. In the flight mechanism, features uniquely pertinent to hovering are distinguished from those that support stiff-winged flight-the latter common to both swifts and hummingbirds. Hovering is especially dependent on adaptations for axial rotation of the wing at all major joints, and on extreme development in hummingbirds of the unusual wing proportions (short humerus and forearm, and long hand) and enlarged breast muscles found in swifts. Osteological characters of the Oligocene fossil Eurotrochilus that can be compared with modern hummingbirds do not indicate nectarivory or sustained hovering in that taxon In the second section, variations within Trochilidae are described and their distributions within the major clades (Hermits, Topazes, Mangoes, Brilliants, Coquettes, Patagona, Mountain Gems, Bees, and Emeralds) are specified. Most diverse are the jaw mechanism, nasal region and conchae, hyobranchial apparatus, cranial proportions, crests, and pneumatic inflation, structure of the ribcage based on number of ribs attached to the sternum, pectoral girdle, and various humeral characters. Other noteworthy but largely unexplained variation characterizes the hyobranchial apparatus of Heliodoxa, the humerus of the "Pygmornis group" of Phaethornis, sexual dimorphism in numbers of thoracic ribs, and synostosis of phalanges of the foot. Although Hermits display distinctive characters, their subfamily status is uncertain for lack of informative outgroups. Major trochilid clades are either weakly supported or unsupported by uniquely derived characters, but apomorphic variation within Mangoes suggests recognition of an Anthracothorax group of genera, and within Emeralds, a large Amazilia group. Each of the major trochilid clades displays considerable diversity in body size and skeletal characters, and numerous characters show parallel evolution within the family. Intraspecific variation is widespread, and selected examples are highlighted. Patterns of skeletal variations at multiple levels of phylogeny suggest that some variations characterizing higher levels had their origins at the intraspecific level. A list of unsolved problems of functional morphology of the skeleton in hummingbirds is offered. Especially intriguing are the many posthatching changes in development of the feeding mechanism and the challenge of incorporating morphological data and their implications into models of evolution of hummingbird communities. Received 17 September 2012, accepted 8 February 2013.
Although it is evident from Dr. Gadow'.s paper on the Suctorial Ap paratus of Tenuiro.stres* that he is well acquainted with the structure of the tongue of Humming Birds, he merely alluded to this group, and as so much misinformation on this subject is current in ornithological literature, it is hoped that the present paper may beof service in cor-recting some of the many misstatements. The pai)er is based on the examination of the species noted below, and it is probable that the type of tongue herein described will be found to prevail throughout at least the greater portion of the Trochi-li(1(e, and should exceptions exist, they will most likely be found in the Pha'thoniithimc.
Since the work of Lucas 1 there has been little systematic investiga-tion on the tongues of birds, and with the exception of an occasional description the subject has been largely neglected. It is in the hope of reopening interest in the subject that this paper is written. As is well known the tongue is an exceptionally variable organ in the Class Aves, as is to be expected from the fact that it is so inti-mately related with the birds' most important problem, that of obtaining food. For this function it must serve as a probe or spear (woodpeckers and nuthatches), a sieve (ducks), a capillary tube (sunbirds and hummers), a brush (Trichoglossidae), a rasp (vul-tures, hawks, and owls), as a barbed organ to hold slippery prey (penguins), as a finger (parrots and sparrows), and perhaps as a tactile organ in long-billed birds, such as sandpipers, herons, and the like.
A survey of data from tropical and temperate regions confirms that nectars of hummingbird and honeyeater flowers are dilute, especially relative to nectars of bee flowers. We use these data, along with theoretical considerations, to examine three recently proposed hypotheses to explain low concentration of hummingbird nectars. None of the quantitative or qualitative predictions of these three hypotheses appears to be upheld. We discuss possible weaknesses of each hypothesis and then present a general framework which may be useful in generating new hypotheses to explain the evolution of nectar concentration.
XTENSIVE efforts of the writer to find a sound anatomical basis for determining the phylogenetic relationships of passerine families leave it clear that the hazard of adaptive convergence in bird systematics has been underestimated. The present analysis of convergence in the neotropical Honey Creepers (family Coerebidae) offers evidence that this is an artificial group. It appears to be composed, in fact, of nectar-adapted warblers (Parulidae) and nectar-adapted tanagers (Thraupidae) that have evolved convergently because of similarity of diet. The Convergence Hazard in Taxonomy Sound systematic work in the higher categories demands sound criteria for clearly distinguishing between adaptation and phylogeny. The investigator at this level sees phylogeny through a screen of food and niche adaptations which often obscure true relationships. Such classic cases of convergence between Old and New World groups as were recently reviewed by Friedmann (1946) are obvious and constitute no hazard. But convergence between members of closely related groups occupying the same range may be such that the most expert taxonomists are unable to decide the true affinities on the basis of external characters alone (Beecher, 1950). This is no reflection on the taxonomists, who have generally been the first to recognize the problem, referring such moot groups as the Coerebidae to the comparative anatomist for additional evidence. But internal characters are not necessarily more reliable than external ones for indicating phylogeny. They are merely additional clues, often of a very conservative sort, but sometimes capable of adaptive changes as rapid as those known for any external features. Sclater (1886: 1) long ago observed that it was "in some instances difficult to distinguish" the Coerebidae from warblers on the one hand and tanagers on the other. Lucas (1894: 299-309) made an anatomical survey of several of the most important coerebid genera; though he considered his findings confusing and inconclusive, they nevertheless confirmed an opinion many times expressed that the group needed study and was probably heterogeneous. Ridgway (1902: 377) obviously regarded the Coerebidae as close to the Parulidae and Thraupidae. He even removed the 1 The writer is greatly indebted to the United States National Museum, the American Museum of Natural History, and the Chicago Natural History Museum for lending material. For use of specimens in their care or for information or advice, he wishes to thank Alexander
The staple item of diet of Glossopsitta porphyrocephala is pollen. The amount of karri pollen necessary to supply the energy for one bird's basal metabolism of 8.0 kcal/day is supplied by about 500 flowers. The moist papillae on the tongue of the lorikeets enable the birds to collect the dust-like pollen. Less than 1% of the anthers grazed are ingested during the driest months of the year when there is no nectar available. Karri nectar contains sucrose, glucose, fructose, and melibiose and is collected when it flows during the wetter flowering months. It is not a substitute for pollen, which the birds continue to harvest as their source of nitrogen. At the time the birds ingest nectar they accumulate subcutaneous fat. Nectar does not reach the stomach but is held in the crop, which enlarges to accommodate it.
1. The consummatory part of the drinking behaviour of pigeons is studied by a frame-by-frame analysis of high-speed films and X-ray motion pictures. 2. A double-suction or vacuum-pump model is formulated for the mechanics of drinking. Consummatory drinking is a series of similar movement cycles, each transporting one dose of water into the oesophagus. The swallowing movement cycle shows five phases: 1, capillary action of the beak tips; 2, lingual suction; 3, pharyngeal preparation; 4, pharyngeal suction; and 5, oesophageal collection. A double build up of an area of low air pressure occurs. As a result of the retraction of the tongue in the mouth (acting as a piston in a cylinder) low air pressure develops in the buccal cavity and water is sucked into the mouth. Secondly, a lower air pressure area develops in the pharynx as a result of a depression of its floor, so that the water in the mouth is given a momentum caudad, by which it is forced over the larynx into the oesophagus. Neither peristaltic action, nor an alternative lower air pressure area is recorded in the oesophagus. The collection of the swallowed water at the lowest place occurs by gravity. 3. Using the mechanical requirements of the double-suction model the presence and distribution of glands was predicted. As predicted the following glands were found: the gl. lingualis superior et inferior, the gl. mandibularis anterior et posterior, the gl. palatina posterior externa, the gl. cricoarytenoidea and the gl. sphenopterygoidea. 4. The application of a comparator model for the description of the stereotypy of the pecking behaviour for the drinking behaviour showed that the drinking swallowing cycle and the three types of eating swallowing cycles were basically similar. The difference, apart from those of amplitude, was the coupling of the erection of the ventral pharyngeal valves to the pro- and retraction of the linguolaryngeal apparatus. The erection occurs during drinking at the very start of the protraction, but during pecking at the start of the retraction. Further, the consummatory act of drinking is composed of some smaller fixed elementary movement units. These units are fixed for mechanocybernetical reasons. The decision points between these units though masked under normal conditions, were found at the start of the capillary phase and during the preparatory phase by experimental manipulation. 5. A possible evolutionary scenario for the double-suction mechanism is discussed. It is suggested that: 1, the feeding system is maximized for food transport by using the slide-and-glue mechanism rather than using the ancestral catch-and-throw mechanism; that 2, the feeding system was maximized for water transport by using the double-suction mechanism rather than the ancestral tipping-up mechanism; that 3, high selection pressure on fast transport of seeds has occurred and that lack of selection pressure on fast drinking was probable. From this may be concluded that the slide-and-glue mechanism is the primar mechanism and the double-suction secondar. This secondary development is in itself a simple change of coupling of one of the subunits already developed as a pecking submechanism, the erection of the ventral pharyngeal valves. Although this recoupling falls completely within the mechanical boundary conditions of the slide-and-glue mechanism so that no reconstruction of the mechanical part of the system is required, nevertheless some strong selection pressure might be necessary for the evolution of a double-suction mechanism since valve erection was found to be part of different centrally coordinated fixed elementary units in swallowing both during eating and drinking. Such an external selection pressure could not be found. Finally, it was shown that for the explanation of the evolutionary scenario of suction drinking the
The tongues of Australian honeyeaters (Meliphagidae) are broader and more fimbricated at the top than the bifurcated tongues of sunbirds (Nectariniidae) and hummingbirds (Trochilidae); the bills of hummingbirds are more uniformly narrow and taper less markedly towards their tips than those of sunbirds and honeyeaters; and bill curvatures are generally greater for sunbirds and honeycreepers than for hummingbirds. A variety of hummingbirds has straight or even slightly upturned bills; bills for all sunbirds, honeycreepers and honeyeaters are decurved to some extent. Hummingbirds, sunbirds and honeyeaters extract nectar at a similar range of rates, averaging c40 μL s-1 from feeders, and 1-15 μL s-1 from flowers. All tongues collect nectar by capillarity, with licking rates of 6-17 s-1. Bill lengths of nectarivorous birds are similar in all regions, though species of hummingbird have the shortest and longest bills. Rates of nectar extraction decline rapidly once the floral length exceeds bill length. Decurved bills may have evolved in honeyeaters and sunbirds to enable perching birds to reach flowers at the ends of branches more easily. Consistent differences in bill length between the sexes suggest that males and females may exploit different floral resources or different proportions of the same resources. For honeyeaters and sunbirds, males have longer bills than females, but the reverse is true for many hummingbirds. -from Authors
To explore the mechanical determinants of feeding strategies for nectar feeders, we develop a fluid dynamical and behavioral model describing the mechanics and energetics of capillary feeding in hummingbirds. Behavioral and morphological data for Calypte and Archilochus are used to test and illustrate this model. We emphasize the important differences between capillary and suction mechanisms of fluid feeding. Model predictions of nectar intake rates and nectar volumes per lick are consistent with observed values for Calypte anna. The optimal nectar concentration maximizing rate of energy intake depends on tongue morphology and licking behavior. For hummingbirds exhibiting optimal licking behavior, the optimal nectar concentration is 35–40% sucrose for feeding on large nectar volumes. For small nectar volumes, the optimal concentration is 20–25%. The model also identifies certain tongue morphologies and licking frequencies maximizing energy intake, that are consistent with available observations on licking behavior and tongue design in nectar feeding birds. These predictions differ qualitatively from previous results for suction feeding in butterflies.
The model predicts that there is a critical food canal radius above which suction feeding is superior to capillary feeding in maximizing the rate of energy intake; the tongues of most hummingbirds and sunbirds fall above this critical radius. The development of suction feeding by nectarivorous birds may be constrained by the elastic properties of their flexible tongues. Our results show that, in terms of morphology, scaling, and energetics, different mechanisms of feeding on the same food resource can lead to qualitatively different predictions about optimal design and feeding strategies.
We develop a mechanistic model for nectar feeding in butterflies that integrates the two basic components of the feeding process: the fluid dynamics of nectar flow through the food canal and the contractile mechanics of the muscular, cibarial pump. We use the model to predict the relation between rate of energy intake during feeding and nectar concentration. We then identify nectar concentations that maximize energy intake rates (the optimal concentrations). We illustrate the model using measurements of the food canal and cibarium of Pieris butterflies. The model predicts an overall optimal range of nectar concentration of 31–39% sucrose for butterflies, which is in agreement with previously reported laboratory values. The model also predicts an interaction among the geometries of the food canal, the cibarial cavity, and the cibarial muscles, that allows us to identify the combinations of food canal, cibarium, and muscle dimensions that yield the highest rates of energy intake. Nectar-feeding is functionally equivalent in butterflies and hummingbirds: two physically different feeding mechanisms can yield identical energy intake rates. This equivalence results from a mathematical and physical similarity between quasi-steady-state fluid flow in hummingbrid tongues and the force-velocity characteristics of contracting cibarial muscle in butterflies.
Selasphorus flammula (2.4–3.0 g) breeds in the high mountain regions of Costa Rica (up to 3200 m). Its small size together with the cold temperatures results in high energetic demands on the birds. The energetic efficiency with whichSelasphorus could extract nectar fromTropaeolum flowers was estimated by measuring foraging rates at individual flowers and estimating nectar production rates between flower visits. Extraction efficiency was expressed in caloric terms by converting hovering time to caloric expenditure and nectar volume to caloric intake through measurements of nectar concentration.1.
Selasphorus had a low rate of nectar extraction fromTropaeolum flowers. However, bothTropaeolum andSalvia flowers produced nectar that was more concentrated than the nectar from other flowers sampled in the mountain regions of Cost Rica.
2.
The small size of these flowers may preclude providing large volumes of nectar, but the high nectar concentration could increase nectar extraction efficiency. The differences in nectar concentration between flowers probably is related to the strategy used by the flowers to achieve pollination.
3.
Information on mean available nectar volumes for unprotectedSalvia flowers enabled a rough estimate of rate of visitation ofSelasphorus atSalvia and the number of flowers necessary to provide a neutral energy budget. The calculations indicate that a femaleSelasphorus should visit individualSalvia flowers about once every 5 hours. To account for foraging and resting metabolic costs during the day and incubating costs at night, a nesting female should visit about 540 flowers/hr or about 2700 flowers/day.
A model is developed to elucidate the determinants of sugar concentrations in flower nectars. This model analyses the efficiency of sugar intake, or energy flux, which for nectarivores closely approximates the rate of net energy gain. For both steady state and some non-steady flows of nectars, this energy flux is shown to be maximal at particular sugar concentrations referred to here as the maximum flux concentration. Higher concentrations actually yield lower energy intake rates because the concomitant rapid increase in viscosity sharply reduces the rate of fluid intake. For pure sucrose solutions, the maximum flux concentration is 22%. For flower nectars, which are chemically more complex, the maximum flux concentration is predicted to be closer to 26%, using the first viscosity measures obtained for flower nectars. This concentration is shown to be essentially independent of the pollinator's feeding organ morphology and of the type of potential inducing nectar flow. It is proposed that this concentration applies for virtually all pollinators that select nectars with maximal energy flux.
However not all pollinators are expected to select such nectars because this 26% concentration is not necessarily “optimal”. The model predicts that optimal sugar concentrations vary for particular pollinators as a function of two primary factors: (1) the energy flux derived from the nectar, as discussed above, as well as (2) the relative contribution of transit costs to overall foraging costs. Relatively “dilute” nectars, with sugar concentrations close to the maximal flux value, are predicted for flowers pollinated by organisms that minimize feeding time to reduce high feeding costs, such as that of hovering or of exposure to enhanced predation while feeding. More concentrated nectars are predicted for flowers pollinated by nectarivores that incur high foraging transit costs relative to feeding costs.
Flowers pollinated by hovering pollinators, including many hummingbirds, hawkmoths and bats, have nectars with mean sugar concentrations in close accord with the 26% maximum flux concentration predicted. Moreover, these nectars have relatively low concentrations of nonsugar constituents, which increase viscosity and thereby decrease sugar flux. Over 75% of the flowers examined in this study, which are pollinated primarily by territorial hummingbird species, provide nectars that allow sugar uptake with an efficiency of 90% or greater of the maximal value. According to the model, these data suggest that feeding costs of these pollinators far outweigh foraging transit costs. In contrast, the model suggests that flower nectars taken by traplining hummingbirds and by bees, with sugar concentrations significantly above the maximum flux value, reflect the higher costs of foraging flight relative to costs of feeding for these pollinators.
Increasing temperature decreases nectar viscosity, and thereby increases absolute nectar uptake rates sharply. This leads to a number of predictions regarding foraging behavior as well as flower location, orientation, and color. However, the maximum flux concentration is shown to be practically invariable over a wide range of temperatures-increasing by only 2% sugar from 10°C to 30°C. Thus, contrary to previous expectations, little change in average sugar concentrations of flowers pollinated by particular groups of nectarivores is expected from cooler to warmer regions.
Field observations of the adult European skipper, Thymelicus lineola (Ochs), feeding on concentrated nectars (40–65% sucrose) from a variety of flower species led us to question recent literature stating that butterflies feed primarily, and most effectively, on dilute nectars. Rate of sucrose solution intake, volume consumed and feeding duration were measured for males and females at 25 and 35°C under laboratory conditions. As sucrose concentration increased, the volume of solution ingested per meal first increased and then decreased gradually, while sucrose intake was highest at concentrations ≧40%. Females fed more than males at all concentrations >10% while temperature had no significant effect on meal size. Feeding duration increased with concentration, was shorter at 35 than at 25°C, and was longer for females than males.
The rate of volume intake decreased as concentration incresed, but not nearly as rapidly as predicted by earlier models. Rates did not differ between the sexes but were faster at 35 than 25°C. This increase was contributed to equally by a reduction in viscosity and an increase in power output of the cibarial pump. The form of the relations was similar, with maximum rate of sucrose intake occurring at 40% sucrose.
A new mathematical model was developed to describe the rate — concentration relation based on the Hagen-Poiseuille equation for laminar fluid flow through pipes. Our model differs from previous models principally in that the power output of the insect's cibarial pump remains relatively constant while the pressure drop created by the pump to induce suction is highly variable. This change results in a very different feeding rate — sucrose concentration function with the optimal rate of sucrose intake at a concentration of approximately 40%. The model indicates that the same relation should hold for a wide range of proboscis shape and size and type of suction pump, and should therefore be applicable to all other nectar feeders with sucking mouth parts. Independent verifications of the model were carried out by measuring the rate of uptake of sucrose solutions of the adult common armyworm, Pseudaletia unipuncta (Haw.), and of human subjects using a volumetric pipette, both of which gave an excellent fit.
Nectar concentrations which correspond to optimal rates of sucrose intake should be highly preferred by insects with high feeding costs, those which are time-limited, or which are very vulnerable while feeding. High transport costs and severe water stress may shift preferences to higher and lower concentrations respectively.
1.
Understanding avian diet preferences reveals a great deal about the birds’ digestive physiology
and relationships with food plants, and can make a valuable contribution towards directing physiological
and ecological research. Importantly, diet preferences are likely to reflect physiological
constraints and therefore mechanisms of digestion.
2.
We assessed the interaction between diet concentration and sugar-type preferences of three
Australian nectarivorous bird species. Each individual bird was offered paired energetically-equivalent
diets: a sucrose solution and hexose (1 : 1 mixture of glucose : fructose) solution over a range of diet
concentrations from 0·075 to 2 mol L
–1
Sucrose Equivalents (SE).
3.
Similar patterns were found for all three species. Intake on the most dilute diets was insufficient
to maintain energy balance, suggesting that these birds faced physiological constraints on such
diets.
4.
All three species demonstrated a preference for hexose over sucrose when offered dilute diets,
and sucrose (or none) preference on more concentrated diets. The three species differed in terms of
when this switch from hexose to sucrose preference took place. Rainbow lorikeets (Psittacidae,
c.
135 g body mass) demonstrated hexose preference for diets up to and including 0·75 mol L
–1
SE;
sucrose was preferred on 2 mol L
–1
SE diets. Red wattlebirds (Meliphagidae,
c.
105 g) showed
hexose preference on only the most dilute (0·075 mol L
–1
SE) diet, and sucrose preference on 1 and
2 mol L
–1
SE diets. New Holland honeyeaters (Meliphagidae,
c.
22 g) preferred hexose on 0·075 and
0·1 mol L
–1
SE diets, and their selectivity for sucrose was not statistically significant. We suggest that
the switch from hexose preference may be directly related to the digestive capacity of different taxa.
5.
Accumulating evidence suggests similar patterns of sugar preferences in various nectarivorous
bird lineages. A switch from hexose preference on dilute diets to sucrose preference on concentrated
diets has now been shown for hummingbirds, flowerpiercers, sunbirds, honeyeaters and lorikeets.
Hexose preference on dilute diets suggests that reduced digesta retention time and low sugar
concentration influences sucrose hydrolysis efficiency, whilst absorption rate of monosaccharides is
less limiting. Sucrose preference on concentrated diets is more puzzling, but may reflect preference
for diets with lower osmolality. Varying preferences suggest that the co-evolutionary relationships
between birds and nectar sugar composition are likely to be similarly dynamic and situation dependent.