ArticleLiterature Review

Hummingbird foraging and the relation between bioenergetics and behaviour

November 2002
Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology 133(2):335-43

Source
PubMed

Authors:

University of British Columbia

Because of their small size and expensive mode of flight, hummingbirds display some of the highest known mass-specific rates of aerobic metabolism among vertebrates. High enzymatic flux capacities through pathways of carbohydrate and long-chain fatty acid oxidation indicate that either substrate can fuel flight. Although hummingbirds are known to rely on fat to fuel migratory flight, short foraging bouts are fueled by the oxidation of carbohydrate, not fat. This allows birds refueling at meadows during migration to deposit fat at higher rates and avoids the energetic inefficiency that results from synthesizing fat from dietary sugar, and then breaking down the fat to fuel foraging flight. On cold mornings in subalpine meadows, refueling hummingbirds achieve net energy gain despite the high energetic costs of thermoregulation and flight. In doing so, they sustain the highest known time-averaged metabolic rates among vertebrates. However, low sucrose concentrations, provided in volumes large enough to allow the maintenance of energy balance at low temperature, result in energy deficit and mass loss. The problem of disposing of dietary water at low ambient temperature when intake rates are elevated suggests that the kidneys may be involved in establishing the upper limit to intake rates and, therefore, maximum sustained metabolic rates. It is suggested that hummingbird behaviour and metabolism have coevolved to maximize net energy gain. Further, the energetics of hummingbird thermoregulation and flight may have influenced the evolution of sucrose content in floral nectar.

Sugar and protein digestion in flowerpiercers and hummingbirds: A comparative test of adaptive convergence

Article

Full-text available

May 2004

Flowerpiercers are the most specialized nectar-feeding passerines in the Neotropics. They are nectar robbers that feed on the sucrose-rich diet of hummingbirds. To test the hypothesis that flowerpiercers have converged with hummingbirds in digestive traits, we compared the activity of intestinal enzymes and the gut nominal area of cinnamon-bellied flowerpiercers (Diglossa baritula) with those of eleven hummingbird species. We measured sucrase, maltase, and aminopeptidase-N activities. To provide a comparative context, we also compared flowerpiercers and hummingbirds with 29 species of passerines. We analyzed enzyme activity using both standard allometric analyses and phylogenetically independent contrasts. Both approaches revealed the same patterns. With the exception of sucrase activity, hummingbirds' digestive traits were indistinguishable from those of passerines. Sucrase activity was ten times higher in hummingbirds than in passerines. Hummingbirds and passerines also differed in the relationship between intestinal maltase and sucrase activities. Maltase activity was two times higher per unit of sucrase activity in passerines than in hummingbirds. The sucrase activity of D. baritula was much lower than that of hummingbirds, and not unlike that expected for a passerine of its body mass. With the exception of aminopeptidase-N activity, the digestive traits of D. baritula were not different from those of other passerines.

Metabolic substrate use and the turnover of endogenous energy reserves in Broad-tailed Hummingbirds (Selaphorus platycercus)

Article

Full-text available

Aug 2006

We fed broad-tailed hummingbirds (Selasphorus platycercus) diets of contrasting carbon isotope composition and measured changes in the delta(13)C of expired breath through time. By measuring the delta(13)C in the breath of fed and fasted birds we were able to quantify the fraction of metabolism fueled by assimilated sugars and endogenous energy reserves. These measurements also allowed us to estimate the fractional turnover of carbon in the hummingbirds' energy reserves. When hummingbirds were feeding, they fueled their metabolism largely ( approximately 90%) with assimilated sugars. The rate of carbon isotope incorporation into the energy reserves of hummingbirds was higher when birds were gaining as opposed to losing body mass. The average residence time of a carbon atom in the hummingbirds' energy reserves ranged from 1 to 2 days.

Comportamiento territorial y preferencias de forrajeo del colibrí migratorio Selasphorus rufus dentro de un sitio invernal

Thesis

Full-text available

Feb 2012

Las comunidades de colibríes han sido estudiadas en relación con sus recursos alimenticios desde hace cinco décadas. Se ha establecido que el principal factor que determina los patrones de abundancia y diversidad de las comunidades de colibríes es la abundancia de las flores que visitan. Así, se ha postulado que la separación ecológica de los nichos puede darse por diversos procesos que pueden ser morfológicos, fisiológicos o incluso conductuales. Otros factores de importancia son las fenologías florales y la migración; sobre todo en regiones altamente estacionales como el Noroeste de México donde un gran número de especies de colibríes son migratorias y existe una gran fluctuación de los recursos florales a lo largo del año. En el presente trabajo de tesis se abordaron cuatro estudios con la comunidad de colibríes en el Noroeste de México y como el uso de los recursos florales influencia su comportamiento, sus patrones migratorios así como la estructura de sus comunidades. En primer capítulo, determinamos como la conducta y la dominancia influyen en la distribución de los recursos a nivel local. Donde encontramos que el comportamiento agresivo de los colibríes puede estructurar la comunidad y la jerarquía de dominancia está directamente relacionada con el tamaño corporal y no presenta relación con la carga del disco alar o el estatus migratorio. Además, el nivel de dominancia de cada especie está relacionada con la calidad del recurso floral. En mi segundo capítulo, evaluamos los patrones de fenología migratoria de dos especies de colibríes (Selasphorus rufus y Amazilia beryllina) y si abundancia floral a los patrones estacionales de abundancia de dos especies de colibríes (Selasphorus rufus y Amazilia beryllina). Los resultados muestran que la especie que presenta una ruta migratoria más larga no presenta cambios anuales en su migración (S. rufus), a diferencia de la especie con migración más corta que puede ajustar su migración anual en relación a la cantidad de recursos presentes en cada sitio visitado (A. beryllina). La migración de S. rufus por la región de estudio coincide con la floración de Salvia iodantha. Siendo S. iodantha la principales fuentes de alimento de S. rufus de la región templada del Noroeste de México. En tercer capítulo, determinamos si existe una preferencia por un tipo de planta en particular utilizando como modelo a dos especies de colibríes de mayor abundancia en la región y de diferente estatus migratorio (S. rufus y A. beryllina). Encontramos que S. rufus se alimento de la especie con la cual coincide su migración en condiciones naturales y en exclusión experimental. A diferencia de A. beryllina, especie que cambio su preferencia en condiciones naturales y al ser ensayada en forma experimental en condiciones de exclusión. Así, la preferencia de un colibrí depende de múltiples factores donde destacan la calidad de los recursos florales, el estatus migratorio así como la jerarquía de dominancia de cada especie de colibrí. Por último en el cuarto capítulo, se analizaron tres comunidades de colibríes en un gradiente altitudinal y las plantas de las que se alimentan, utilizando la teoría de redes de interacción mutualista. Encontramos que la topología de las redes de interacción cambia en el gradiente altitudinal y que la mayoría de las especies de colibríes las encontramos en dos pisos altitudinales pero desempeñaron papeles diferentes en cada sitio de muestreo. Otro resultado importante fue que las especies núcleo en cada red de interacciones fueron plantas ornitófilas y no ornitófilas. Por último determinamos que la abundancia de colibríes migratorios latitudinales está correlacionada con el número de interacciones así como con los enlaces entre colibríes y plantas.

Bird Migration in South America: The Fork-tailed Flycatcher (Tyrannus savana) as a Case Study

Chapter

Apr 2019

Bird migration in South America is highly diverse, with some species migrating solely within the tropical latitudes, others migrating between tropical wintering grounds and south-temperate breeding grounds, and yet other migrating within south-temperate latitudes of the continent. Until recently, bird migration in South America was virtually ignored; however, a growing body of research is shedding new light into the timing, routes, and overall migratory strategies employed by birds that migrate within this vast continent. The unique geographic and climatic context of South America (i.e., no oceanic or mountain barriers and a buffered oceanic climate) likely results in a distinct set of tradeoffs between seasonal life-history demands of migration, reproduction, and molt. Nevertheless, we still understand very little about the mechanisms underpinning such relationships throughout the annual cycle of migratory birds on the continent, and how they ultimately influence the evolution of bird migration in South America. In this chapter, we (1) provide a brief description of bird migration patterns in South America, (2) review the current state of knowledge about the drivers of songbird migration on the continent, particularly those resulting from research on the Fork-tailed Flycatcher (Tyrannus savana), and (3) suggest future avenues for research to understand the mechanisms driving these patterns.

A Reappraisal of the Fruit-Taking and Fruit-Handling Behaviors of Neotropical Birds

Chapter

Apr 2019

Research on the fruit-taking and fruit-handling behaviors of birds flourished in the 1980s when empirical observations and experimental studies revealed that the feeding techniques of birds affect which fruits they eat and, ultimately, which seeds they disperse. Recent calls to incorporate natural history aspects into empirical studies and theoretical models to improve our understanding of the seed dispersal process bring some fresh air to the topic, given its potential to influence fruit choice by birds. Here we compile information scattered in the literature, some of which hard to access, to reveal broad patterns of fruit-taking and fruit-handling behaviors observed in the wild for 197 bird species representing a wide spectrum of the bird phylogeny (117 genera, 26 families). We tested the influence of phylogeny on fruit-taking and fruit-handling behaviors, and also investigate the previously unexplored relationship between the flexibility in fruit-taking and fruit-handling behaviors with body size and degree of frugivory (i.e., a measure of the importance of fruits in the diet). We are ultimately interested in stimulating further studies that incorporate the often neglected behaviors used by birds to take and handle fruits to investigate the reciprocal ecological and evolutionary consequences between frugivorous birds and plants.

Visual and Acoustic Communication in Neotropical Birds: Diversity and Evolution of Signals

Chapter

Apr 2019

Animal communication is a key feature of intra- and inter-specific interactions in nature. Vocalizations and plumage coloration are two of the most exploited signaling pathways among birds and they have an important role in sexual selection and reproductive isolation. The evolution of vocal and visual signals and their efficiency to confer information are influenced by many factors, such as the signaler’s morphology, the environment in which these are transmitted, or the sensitivity of either intended or unintended receivers like potential predators. In this chapter we review the diversity of visual and vocal signals among Neotropical birds which have been less studied than their counterparts from other biogeographic realms. The particularities they may present are not “exceptions,” but opportunities to gain a better understanding of avian communication and the factors influencing its evolution.

Behavioral Ecology of Neotropical Birds

Book

Jan 2019

This book covers central aspects of behavioral ecology, including sexual selection, social and genetic mating systems, cooperative breeding, brood parasitism, brood reduction, migration, personalities and communication. Over the past several years, Neotropical bird species from temperate to tropical latitudes of South America have been extensively studied, yielding valuable insights into the evolutionary mechanisms that drive their behavioral traits. In this book, international experts provide a general overview of main behavioral aspects. They also present the main findings of their work, including experimental approaches to testing the most accepted behavioral theory in their model systems. In closing, they propose new theoretical frameworks and future research directions. As such, the book provides a comprehensive and updated guide for all researchers, students and professionals whose work involves the study and management of birds across the Neotropical region.

Perspectives on the Study of Field Hummingbird Cognition in the Neotropics

Chapter

Full-text available

Apr 2019

Cognitive abilities are pivotal to the performance of traits that are closely related to fitness. However, the selective regimes shaping the evolution of cognition, and differences in individual cognitive performance under different environmental conditions have been poorly studied. The rich environmental heterogeneity and biodiversity in the Neotropics present a compelling scenario where to study the functional and mechanistic links in the evolution of cognition. On the other hand, hummingbirds are a particularly interesting group in which to examine cognitive performance in the free-living animals. Their diet, mainly composed by nectar of flowers, varies in concentration, composition, and rate of renewal. These variables are easy to manipulate in the field, presenting excellent options for experimental setup. We explored cognitive performance in hummingbird species occurring in diverse environments. Overall, hummingbird species in the Neotropics showed similar cognitive abilities than species in the Nearctic region; however, our conclusions are limited by the few studies that have been carried out. Among different habitats, environmental heterogeneity seems to drive the development of cognitive abilities, however mediated by individual traits such as sex and social status. This could explain why, across all the studies, we observed important individual differences in cognitive performance. In our opinion, the role of these variables should be further assessed by integrating physiological traits, such as endocrine levels and energy balance. Thus, integrative and comparative studies in hummingbirds in the Neotropics could shed light on the different selective pressures that might have shaped the evolutionary trajectory of avian cognition.

Body mass as a supertrait linked to abundance and behavioral dominance in hummingbirds: A phylogenetic approach

Article

Full-text available

Feb 2019

Body mass has been considered one of the most critical organismal traits, and its role in many ecological processes has been widely studied. In hummingbirds, body mass has been linked to ecological features such as foraging performance, metabolic rates, and cost of flying, among others. We used an evolutionary approach to test whether body mass is a good predictor of two of the main ecological features of humming‐ birds: their abundances and behavioral dominance. To determine whether a species was abundant and/or behaviorally dominant, we used information from the literature on 249 hummingbird species. For abundance, we classified a species as “plentiful” if it was described as the most abundant species in at least part of its geographic distri‐ bution, while we deemed a species to be “behaviorally dominant” when it was de‐ scribed as pugnacious (notably aggressive). We found that plentiful hummingbird species had intermediate body masses and were more phylogenetically related to each other than expected by chance. Conversely, behaviorally dominant species tended to have larger body masses and showed a random pattern of distribution in the phylogeny. Additionally, small‐bodied hummingbird species were not considered plentiful by our definition and did not exhibit behavioral dominance. These results suggest a link between body mass, abundance, and behavioral dominance in hum‐ mingbirds. Our findings indicate the existence of a body mass range associated with the capacity of hummingbird species to be plentiful, behaviorally dominant, or to show both traits. The mechanisms behind these relationships are still unclear; how‐ ever, our results provide support for the hypothesis that body mass is a supertrait that explains abundance and behavioral dominance in hummingbirds.

Sugar Metabolism in Hummingbirds and Nectar Bats

Article

Full-text available

Jul 2017

Hummingbirds and nectar bats coevolved with the plants they visit to feed on floral nectars rich in sugars. The extremely high metabolic costs imposed by small size and hovering flight in combination with reliance upon sugars as their main source of dietary calories resulted in convergent evolution of a suite of structural and functional traits. These allow high rates of aerobic energy metabolism in the flight muscles, fueled almost entirely by the oxidation of dietary sugars, during flight. High intestinal sucrase activities enable high rates of sucrose hydrolysis. Intestinal absorption of glucose and fructose occurs mainly through a paracellular pathway. In the fasted state, energy metabolism during flight relies on the oxidation of fat synthesized from previously-ingested sugar. During repeated bouts of hover-feeding, the enhanced digestive capacities, in combination with high capacities for sugar transport and oxidation in the flight muscles, allow the operation of the “sugar oxidation cascade”, the pathway by which dietary sugars are directly oxidized by flight muscles during exercise. It is suggested that the potentially harmful effects of nectar diets are prevented by locomotory exercise, just as in human hunter-gatherers who consume large quantities of honey.

Nutrients Metabolizability of Nectar for Long-Term Maintenance of Amazilia amazilia and Effect of a Dietary Fiber Source

Article

Full-text available

Jan 2015

A review of the energetics of pollination biology

Article

May 2013
J COMP PHYSIOL B

Pollination biology is often associated with mutualistic interactions between plants and their animal pollen vectors, with energy rewards as the foundation for co-evolution. Energy is supplied as food (often nectar from flowers) or as heat (in sun-tracking or thermogenic plants). The requirements of pollinators for these resources depend on many factors, including the costs of living, locomotion, thermoregulation and behaviour, all of which are influenced by body size. These requirements are modified by the availability of energy offered by plants and environmental conditions. Endothermic insects, birds and bats are very effective, because they move faster and are more independent of environmental temperatures, than are ectothermic insects, but they are energetically costly for the plant. The body size of endothermic pollinators appears to be influenced by opposing requirements of the animals and plants. Large body size is advantageous for endotherms to retain heat. However, plants select for small body size of endotherms, as energy costs of larger size are not matched by increases in flight speed. If high energy costs of endothermy cannot be met, birds and mammals employ daily torpor, and large insects reduce the frequency of facultative endothermy. Energy uptake can be limited by the time required to absorb the energy or eliminate the excess water that comes with it. It can also be influenced by variations in climate that determine temperature and flowering season.

Stoking the Brightest Fires of Life Among Vertebrates

Article

Full-text available

Jun 2009

Hummingbirds and nectarivorous bats in flight display some of the high-est rates of aerobic metabolism among vertebrates. Analysis of the pathway of oxygen, i.e., the "oxygen transport cascade", reveals the concerted upregulation of capacities for O 2 flux from the external environment, through the respiratory and cardiovascular systems, into muscle mitochondria. Pathways for aerobic energy metabolism are highly conserved, but enzymatic capacities for carbohydrate and fatty acid oxidation, as well as for aerobic ATP synthesis, are also upregulated in concert. Despite evidence indicating sufficient capacities for fatty acid oxidation to support hovering, repeated bouts of hover-feeding in hummingbirds and nectar bats involve the oxidation of carbohydrate. Recent studies reveal that recently ingested sugar directly fuels flight, giving rise to the concept of the "sucrose oxidation cas-cade". The ecological and bioenergetic advantages conferred by sugar oxidation during foraging are discussed.

Diel variations in plasma glucose concentrations of Malachite Sunbirds Nectarinia famosa

Article

Full-text available

Jul 2009

Plasma glucose concentrations in birds are much higher than those in mammals of similar body mass, and they are thought to be kept more or less constant. We investigated plasma glucose concentrations of Malachite Sunbirds (Nectarinia famosa) to determine whether there was a circadian rhythm in plasma glucose and whether plasma glucose concentrations rose at lower temperatures. We explored the possibility that glycogenolysis and gluconeogenesis might be used by birds before daylight to generate body heat during arousal from torpor or from overnight adaptive heterothermy. Plasma glucose concentration of Malachite Sunbirds were relatively high, between 13.6 and 21.4mmol/L. Plasma glucose concentrations were higher at 5°C than at 25°C, and generally lower during the scotophase, particularly in the early hours of the morning. Therefore, it appears that Malachite Sunbirds are not increasing plasma glucose concentrations during arousal from torpor or to increase scotophase body temperature levels to photophase levels. It is apparent that these nectarivorous birds have a circadian variation in plasma glucose concentrations that is affected by ambient temperature and feeding patterns.

The sugar oxidation cascade: Aerial refueling in hummingbirds and nectar bats

Article

Full-text available

Jan 2011
J EXP BIOL

Most hummingbirds and some species of nectar bats hover while feeding on floral nectar. While doing so, they achieve some of the highest mass-specific V(O(2)) values among vertebrates. This is made possible by enhanced functional capacities of various elements of the 'O(2) transport cascade', the pathway of O(2) from the external environment to muscle mitochondria. Fasted hummingbirds and nectar bats fly with respiratory quotients (RQs; V(CO(2))/V(O(2))) of ~0.7, indicating that fat fuels flight in the fasted state. During repeated hover-feeding on dietary sugar, RQ values progressively climb to ~1.0, indicating a shift from fat to carbohydrate oxidation. Stable carbon isotope experiments reveal that recently ingested sugar directly fuels ~80 and 95% of energy metabolism in hover-feeding nectar bats and hummingbirds, respectively. We name the pathway of carbon flux from flowers, through digestive and cardiovascular systems, muscle membranes and into mitochondria the 'sugar oxidation cascade'. O(2) and sugar oxidation cascades operate in parallel and converge in muscle mitochondria. Foraging behavior that favours the oxidation of dietary sugar avoids the inefficiency of synthesizing fat from sugar and breaking down fat to fuel foraging. Sugar oxidation yields a higher P/O ratio (ATP made per O atom consumed) than fat oxidation, thus requiring lower hovering V(O(2)) per unit mass. We propose that dietary sugar is a premium fuel for flight in nectarivorous, flying animals.

Using stable isotopes in hummingbird breath to estimate reliance on supplemental feeders

Article

Full-text available

Feb 2023

Understanding the ecological consequences of supplemental feeding to both hummingbirds and the plants they pollinate is complicated by logistical challenges associated with assessing relative dietary resource use with commonly applied observational methods. Here, we describe the results of research conducted to assess the relative use of feeder and flower nectar by Broad‐tailed (Selasphorus platycercus) and Rufous hummingbirds (Selasphorus rufus) using two distinct methodological variations to measure the δ13C values of exhaled CO2. Because of the relatively quick time in which both species switch from exogenous to endogenous resources to fuel metabolism, our experiment allowed us to assess resource use at two timescales. Our results suggest variability in the relative contributions of the two dietary sources within and among species and timescales, with most birds employing a mixture of feeder and flower sugars as fuel sources. This diversity in relative resource use may mitigate potential negative effects of supplemental feeding on hummingbirds and their plant symbionts. Posterior distributions for the isotopic composition of exhaled CO2 in fed birds (δ13C0; first column), the isotopic composition of exhaled CO2 in fasted birds (δ13C∞; second column), and associated overlap for Broad‐tailed and Rufous hummingbirds. Y axis values represent frequencies from 10,000 Markov chain Monte Carlo samples, with higher frequencies representing greater numbers of individuals likely to employ a particular dietary resource or mixture. Vertical dotted lines and vertical dashed lines represent the 85% highest posterior density intervals for δ13C0 and δ13C∞, respectively.

Prevalencia de malaria en colibrís (Trochilidae) en los bosques montanos del sur de Ecuador

Thesis

Full-text available

Dec 2012

Anahi Cosky Paca-Condori

Se capturaron 137 individuos de colibrís entre los cuales se identificaron 17 especies, 7 con infección por malaria aviaria. Mediante la regresión por contraste independiente, se encontró una relación positiva entre peso promedio de las especies y prevalencia de infección por malaria aviaria. Por primera vez, se presentan datos de infección por malaria para las especies Adelomyia melanogenis, Coeligena iris, Boissoneaua mathewsii, Lafresnaya lafresnayi, Methallura tyrianthina y Heliangelus viola. Las especies más comunes en el muestreo fueron Coeligena iris y A. melanogenis y la prevalencia de infección en la primera (78%; N = 23) fue bastante mayor que en la segunda (13%; N = 23). No se pudo rechazar la hipótesis nula de que la probabilidad de prevalencia está relacionada al sexo. Finalmente, se encontró una diferencia significativa entre las medias del nivel de policromatófilos en individuos infectados y no infectados de Coeligena iris, pero no para A. melanogenis, muy posiblemente porque el numero muestral era reducido.

Floral phenology of an Andean bellflower and pollination by buff‐tailed sicklebill hummingbird

Article

Full-text available

Jun 2022

The Andean bellflowers comprise an explosive radiation correlated with shifts to specialized pollination. One diverse clade has evolved with extremely curved floral tubes and is predicted to be pollinated exclusively by one of two parapatric species of sicklebill hummingbirds (Eutoxeres). In this study, we focused on the floral biology of Centropogon granulosus, a bellflower thought to be specialized for pollination by Eutoxeres condamini, in a montane cloud forest site in southeastern Peru. Using camera traps and a pollination exclusion experiment, we documented E. condamini as the sole pollinator of C. granulosus. Visitation by E. condamini was necessary for fruit development. Flowering rates were unequivocally linear and conformed to the “steady‐state” phenological type. Over the course of >1800 h of monitoring, we recorded 12 E. condamini visits totaling 42 s, indicating traplining behavior. As predicted by its curved flowers, C. granulosus is exclusively pollinated by buff‐tailed sicklebill within our study area. We present evidence for the congruence of phenology and visitation as a driver of specialization in this highly diverse clade of Andean bellflowers. Specialized pollination is thought to drive niche partitioning in plants and hummingbirds. Floral curvature is one mode by which specialization is thought to operate, but many pollinator species are elusive and understudied. In this study, we document, for the first time, specialized pollination in the rarely seen buff‐tailed sicklebill hummingbird and the Andean bellflower Centropogon granulosus. Photograph taken by Gloria Jilahuanco (Asociación para la Conservación del Valle de Kosñipata, APCONK). Photo used with permission.

Locomotion and Energetics of Divergent Foraging Strategies in Hummingbirds: A Review

Article

Jun 2021

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.

Feeding ecology of the Green-cheeked Parakeet, Pyrrhura molinae (Psittaciformes, Psittacidae), in a subtropical forest of Argentina

Article

Full-text available

Feb 2021

Although there are studies on certain aspects of the feeding ecology of several species of Neotropical parrots, there is scarce ecological information about Pyrrhura molinae-a Psittacidae species which is widely distributed in South America and abundant in the Yungas of Argentina. For two years (May 2014 to June 2016), the composition and seasonal variation in the Green-cheeked Parakeet diet in the Yungas Piedmont forest in Jujuy, Argentina were examined. Furthermore, fruiting phenology tran-sects were established to evaluate food resource availability and the patterns of food resource used by the Green-cheeked Parakeet. In 214 food plant trees, it was found that flower and dry fruit availability was highest in the dry season, and fleshy fruit production peaked in the wet season, but these phenology patterns for aged plant species suggest that there were no significant differences in food availability. The consumption of 18 plant species was recorded, being Celtis iguanaea (30.73%) and Trema micrantha (22.01%) the most consumed species. In terms of food items, fruits were the most consumed items, followed by seeds and flowers and, to a lesser extent, nectar and leaves. Levins' niche Analía Benavídez et al. 206 breadth showed varying levels of diet specialisation amongst seasons, which was narrower (B = 0.28) in the wet season, indicating specialisation in diet during this season. There was a medium overlap in parakeet diet between seasons (Morisita Index = 0.59). We did not find a statistically significant relationship between resource availability and food use, but expansion and contraction in Levins Index and variation in food items consumed throughout the year and season demonstrate high flexibility in the diet. Like other congeners, the Green-cheeked Parakeet has a flexible diet that could be adjusted to the seasonal availability of food resources. These data may contribute to the design of conservation plans for the species and its habitat.

Hummingbird (Aves: Trochilidae) assemblage using resources from the exotic African tuliptree, Spathodea campanulata (Bignoniaceae) in a Neotropical altered environment, southeastern Brazil

Article

Full-text available

Feb 2020
Braz J Biol

The non-native African tuliptree, Spathodea campanulata (P. Beauv), is widely distributed in altered Neotropical environments, where hummingbirds are important pollinators. We investigated the assemblage of hummingbirds which fed on its nectar and described their behavior, to understand possible influences of the exotic tree on the territorial behavior in an altered environment in southeastern Brazil. Seven species fed on flower resources, mainly Eupetomena macroura (Gmelin, 1788), Amazilia lactea (Lesson, 1832), and Florisuga fusca (Vieillot, 1817). Visiting time was positive correlated with number of flowers accessed, but in most visits, hummingbirds get the nectar by pillage, instead of frontal access. Flower availability varied throughout months; however, we found no evidence of significative correlation between available flowers and number of agonistic encounters. Despite a high number of animal-plant interactions and a strong territorialism of some species observed in African tuliptree foraging site, there may be other plants at local scale influencing the behavioral patterns observed.

Diet of Neotropical parrots is independent of phylogeny but correlates with body size and geographical range

Article

Full-text available

Jul 2018

Hummingbirds and bumble bees exposed to neonicotinoid and organophosphate insecticides in the Fraser Valley, British Columbia, Canada

Article

Full-text available

Jul 2018

To measure exposure to neonicotinoid and other pesticides in avian pollinators, we made novel use of cloacal fluid and fecal pellets from rufous (Selasphorus rufus) and Anna's (Calypte anna) hummingbirds living near blueberry fields in the Fraser River Valley and Vancouver Island, British Columbia, Canada. To examine on‐farm exposure to pesticides in invertebrate pollinators, we also collected bumble bees native to Canada (Bombus mixtus, Bombus flavifrons, and Bombus melanopygus), their pollen, and blueberry leaves and flowers from within conventionally sprayed and organic blueberry farms. By sites and sample type, the results reported in the present study represent pooled samples (n = 1). In 2015 to 2016, the combined concentration of the neonicotinoid insecticides imidacloprid, thiamethoxam, and clothianidin detected in hummingbird cloacal fluid from sites near conventionally sprayed blueberry fields was 3.63 ng/mL (ppb). Among the 18 compounds measured in fecal pellets, including one neonicotinoid (imidacloprid), only piperonyl butoxide was detected (1.47–5.96 ng/g). Piperonyl butoxide is a cytochrome P450 inhibitor applied with some insecticides to increase their toxic efficacy. Only diazinon was detected in bumble bees (0.197 ng/g), whereas diazinon (1.54–1.7 ng/g) and imidacloprid (up to 18.4 ng/g) were detected in pollen collected from bumble bees including the bees from organic sites located near conventionally sprayed blueberry farms. Imidacloprid was also detected at 5.16 ng/g in blueberry flowers collected 1 yr post spray from 1 of 6 conventionally sprayed blueberry farms. Environ Toxicol Chem 2018;9999:1–10.

Spatial memory is as important as weapon and body size for territorial ownership in a lekking hummingbird

Article

Full-text available

Jan 2018

Advanced cognitive abilities have long been hypothesized to be important in mating. Yet, most work on sexual selection has focused on morphological traits and its relevance for cognitive evolution is poorly understood. We studied the spatial memory of lekking long-billed hermits (Phaethornis longirostris) and evaluated its role in lek territory ownership, the magnitude of its effect compared to phenotypic traits expected to influence sexual selection, and whether its variation is indicated in the structure of mating vocal signal. Spatial memory (the ability to recall the position of a rewarding feeder) was compared between “territorial” and “floater” males. Interestingly, although spatial memory and body size both positively affected the probability of lek territory ownership, our results suggest a stronger effect of spatial memory. Bill tip length (used as weapon in agonistic interactions) also showed a positive but smaller effect. Load lifting during vertical flight, a measure of physical performance relevant to agonistic interactions, had no effect on territory ownership. Finally, both body size and spatial memory were indicated in the structure of male song: body size negatively correlated with song lowest frequency, while spatial memory positively predicted song consistency. Together, our findings lend support for cognition as a sexual selection target.

Impacts of nectar robbing on the foraging ecology of a territorial hummingbird

Article

Jan 2018

While the effects of nectar robbing on plants are relatively well-studied, its impacts from the perspective of the pollinators of robbed plants is not. Numerous studies do consider the impacts of robbing on pollinator visitation to robbed plants, but rarely do they focus on its scaled-up impacts on individual pollinator behavior. We used radio telemetry to track the spatial and behavioral responses of the territorial hummingbird Aglaeactis cupripennis to experimental nectar-robbing over a period of several days. Simulated nectar robbing impacted foraging behavior by increasing territory area, distance flown, and reliance on novel food resources, especially small-bodied flying insects. We did not observe any impact on the amount of time individuals spent foraging, nor did we observe territory abandonment. These findings indicate that nectar robbing may impose a significant energetic cost on pollinators via increased flight distances and shifts towards potentially less profitable food resources, and demonstrate the importance of quantifying the indirect effects of nectar robbing on pollinators in addition to plants.

Sweeteners and health: Findings from recent research and their impact on obesity and related metabolic conditions

Article

Mar 2016

Few topics in nutrition engender more controversy than added sugars in general, and fructose-containing sugars in particular. Some investigators have argued that added sugars are associated with increased risk of obesity, cardiovascular disease, diabetes, non-alcoholic fatty liver disease and even sugar ‘addiction’. Other investigators have questioned the scientific basis for all of these assertions. This debate has extended far beyond the scientific community into various media outlets including the internet and other non-refereed venues often with heated rhetoric and little science. Against this backdrop, a group of experts and researchers in the metabolism and health effects of added sugars presented a symposium ‘Sweeteners and Health: Findings from Recent Research and their Impact on Obesity and Related Metabolic Conditions’ at the European Congress on Obesity on 7 May 2015. The papers in this supplement are based on the presentations made at this meeting. The current article is intended to serve as an Introduction to this supplement.

Physiological handling of dietary fructose-containing sugars: Implications for health

Article

Full-text available

Mar 2016

Fructose has always been present in our diet, but its consumption has increased markedly over the past 200 years. This is mainly due to consumption of sucrose or high-fructose corn syrup in industrial foods and beverages. Unlike glucose, fructose cannot be directly used as an energy source by all cells of the human body and needs first to be converted into glucose, lactate or fatty acids in the liver, intestine and kidney. Because of this specific two-step metabolism, some energy is consumed in splanchnic organs to convert fructose into other substrates, resulting in a lower net energy efficiency of fructose compared with glucose. A high intake of fructose-containing sugars is associated with body weight gain in large cohort studies, and fructose can certainly contribute to energy imbalance leading to obesity. Whether fructose-containing foods promote obesity more than other energy-dense foods remains controversial, however. A short-term (days-weeks) high-fructose intake is not associated with an increased fasting glycemia nor to an impaired insulin-mediated glucose transport in healthy subjects. It, however, increases hepatic glucose production, basal and postprandial blood triglyceride concentrations and intrahepatic fat content. Whether these metabolic alterations are early markers of metabolic dysfunction or merely adaptations to the specific two-step fructose metabolism remain unknown.

Differences in nectar use potential in a guild of birds: a gut’s view

Article

Full-text available

Jan 2012
ORNITOL NEOTROP

Jorge E. Schondube

Nectar-feeding birds have been used as models to study both community and physiological ecol- ogy. However these two areas have not been linked in the past. Physiological ecologists have found that the mechanisms by which nectar sugars are assimilated can impose limits to the food intake of nectar-feeding animals, affecting their behavior in the field. In this study I quantified the ability to digest sucrose of a community of 10 nectar-feeding birds from the highlands of Western Mexico (7 hummingbirds, 2 warblers and 1 flower- piercer). I used a mathematical model to predict the birds’ maximal capacity to assimilate sucrose, and linked these predictions with ecological parameters. I compared the birds’ predicted maximal rate of energy intake with their field metabolic rates (FMRs) estimated from allometric equations, and with their food intake. Humming- birds’ predicted maximal energy intake was either equal to or greater than their expected FMRs. In these birds, maximal digestive capacities exceeded observed food intake by 10 to 70%. The three species of passerines presented different results. Flowerpiercers (Diglossa baritula) and Nashville Warblers (Vermivora ruficapilla) had predicted maximal energy intake values within the lower 95% confidence interval of their predicted FMRs, and predicted energy intakes of Orange-crowned Warblers (V. celata) were lower than their FMRs. Flowerpierc- ers ingested roughly the same amount of sucrose as expected a priori from intestinal enzyme measurements. Digestion of sucrose seems to limit ingestion rate in passerines but not in hummingbirds. Although V. celata individuals feed heavily on flowers at the study site, my analysis indicates that they need to focus on plant spe- cies that produce hexose-rich nectars and/or complement their diet with insects. I suggest that knowledge of interspecific variation in digestive capacities can inform community-level studies of resource use.

Does Environmental Heterogeneity Promote Cognitive Abilities?

Article

Full-text available

Jun 2015
INTEGR COMP BIOL

In the context of global change the possible loss of biodiversity has been identified as a major concern. Biodiversity could be seriously threatened as a direct consequence of changes in availability of food, changing thermal conditions, and loss and fragmentation of habitat. Considering the magnitude of global change, an understanding of the mechanisms involved in coping with a changing environment is urgent. We explore the hypothesis that species and individuals experiencing highly variable environments are more likely to develop a wider range of responses to handle the different and unpredictable conditions imposed by global change. In the case of vertebrates, the responses to the challenges imposed by unpredictable perturbations ultimately are linked to cognitive abilities allowing the solving of problems, and the maximization of energy intake. Our models were hummingbirds, which offer a particularly compelling group in which to examine the functional and mechanistic links between behavioral and energetic strategies in individuals experiencing different degrees of social and environmental heterogeneity. © The Author 2015. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email: journals.permissions@oup.com.

THE EFFECTS OF FOREST MANAGEMENT ON HABITAT QUALITY FOR BLACK BEARS IN THE SOUTHERN APPALACHIAN MOUNTAINS

Article

Melissa Jo Reynolds

Elements of episodic-like memory in free-living hummingbirds, energetic consequences

Article

May 2011

Episodic memory has been described as the ability to recall personal past events, involving what, where and when an event has been experienced. Cognitive abilities like learning and memory are pivotal to the performance of many behavioural traits such as food procurement. Nectar, the primary food of hummingbirds, is dispersed in hundreds of flowers and varies in concentration and renewal rate. Therefore, a hummingbird that can remember elements of episodic-like memory such as what, where and when the nectar becomes available will have a higher energy rate of intake when compared to random foraging. We conducted a field experiment with green-backed firecrown hummingbirds, Sephanoides sephaniodes. We assessed the ability to recall the location, nectar quality and renewal rate of the most rewarding flowers among several less rewarding flowers with identical visual cues. Hummingbirds were able to remember the most profitable nectar sources and flower position and adjust their visits to nectar renewal interval. Cognitive performance varied among individuals, implying up to 6.3-fold differences in energy gain. Our results strongly suggest that hummingbirds use cognitive abilities to exploit nectar sources efficiently and, therefore, that cognitive abilities are potentially tied to survival probability.

Short-term energy regulation in nectar-feeding birds: The response of Whitebellied Sunbirds (Nectarinia talatala) to a midday fast

Article

Sep 2005
FUNCT ECOL

Small nectar‐feeding birds have high energy turnover and must respond rapidly to changes in food concentration or feeding opportunities. A previous study showed that Rufous Hummingbirds ( Selasphorus rufus ) were unable to adjust their intake rates after a midday fast and thus ended the day with energy deficits that necessitated the use of torpor. We examined the ability of Whitebellied Sunbirds ( Nectarinia talatala ) to cope with a similar loss of foraging time (lights out from 10.00 h to 12.00 h). During the experiment, birds were kept at 10 °C and fed 20% w/w sucrose solution. In contrast to hummingbirds, sunbirds increased their rate of afternoon feeding following the fast, consuming 14·3 ± SD 10·0% ( n = 8) more than on the afternoon of the control day, and maintaining evening body mass at control levels. However, morning body mass on the third day was significantly lower than on the previous 2 days, indicating that compensation for reduced feeding time was probably incomplete. Nectar‐feeding birds show varied and flexible responses to energy challenges.

Inter-specific variation in avian responses to human disturbance

Article

Sep 2005
J APPL ECOL

Increasing urbanization and recreational activities around and within biodiversity hotspots require an understanding of how to reduce the impacts of human disturbance on more than a single species; however, we lack a general framework to study multiple species. One approach is to expand on knowledge about the theory of anti‐predator behaviour to understand and predict how different species might respond to humans. We reviewed the literature and found that only 21% of studies that used a behavioural approach to study human disturbance focused on multiple species. These studies identified a number of potential predictive variables. We developed a simulation model that investigates interspecific variation in different parameters of disturbance with variation in human visitation. We found that fitness‐related responses, such as the quantity of food consumed by a species, are relatively sensitive to the distance at which animals detect humans, the frequency of disturbance by humans and the interaction of these factors, but are less sensitive to other characteristics. We examined avian alert distance (the distance animals first orientated to an approaching threat, a proxy for detection distance) across 150 species, controlling for phylogenetic effects. We found that larger species had greater alert distances than smaller species, which could increase local spatial and temporal limitations on suitable habitat with increasing human visitation. Synthesis and applications . Our results suggest that body size could be a potential predictor of responses to human disturbance across species, and could be used by managers to make conservation decisions regarding levels of human visitation to a protected site. We suggest that three things are essential to develop predictive models of how different species will respond to human disturbance. First, multiple indicators of disturbance should be studied to select those with lower intraspecific variation for a given study system. Secondly, the species‐specific nature of responses should be identified. Thirdly, life history, natural history and other correlates with these species‐specific responses must be assessed.

Nectar-feeding bats fuel their high metabolism directly with exogenous carbohydrates

Article

Full-text available

Aug 2007
FUNCT ECOL

Summary 1. Mammals usually derive energy from metabolizing fat and glycogen stores combined with exogenous food. Nectarivorous bats mostly consume a diet low in both fat and proteins but rich in simple carbohydrates. Metabolizing exogenous carbohydrates directly to fuel their high mass-specific metabolic rate would save the energetic costs of lipogenesis and gluconeogenesis for nectarivorous bats. Therefore, we expected nectarivorous bats to switch to exogenous carbohydrates rapidly when available and use them predominantly instead of fat or glycogen. 2. We first investigated the rate of fractional incorporation of dietary sugars into the pool of metabolized substrates in Glossophaga soricina by measuring the change in 13 C enrichment of exhaled CO 2 ( δ 13 C breath ) when animals were fed glucose, fructose or sucrose that was isotopically distinct from their normal diet. Second, we performed a diet-switch experiment to estimate the turnover rate of fat tissue. 3. When fed with sugars, the δ 13 C breath converged quickly on the isotope signature of the ingested sugars, indicating an almost exclusive use of dietary carbohydrates. The time for a 50% carbon isotope exchange in exhaled CO 2 equalled 9, 13 and 14 min for fructose, glucose and sucrose, respectively. Nectarivorous bats fuelled 82% of their metabolism with exogenous carbohydrate when fed with fructose, 95% when fed with glucose and 77% when fed with sucrose. Bats depleted 50% of their fat stores each day. 4. Although nectarivorous bats consumed most of their body fat each day, this was still barely enough to sustain their diurnal metabolism. The fractional incorporation rates of dietary sugars into the pool of metabolized substrates in G. soricina are the fastest rates ever found in a mammal.

Hummingbirds Fuel Hovering Flight with Newly Ingested Sugar

Article

Full-text available

Sep 2011
PHYSIOL BIOCHEM ZOOL

We sought to characterize the ability of hummingbirds to fuel their energetically expensive hovering flight using dietary sugar by a combination of respirometry and stable carbon isotope techniques. Broadtailed hummingbirds (Selasphorus platycercus) were maintained on a diet containing beet sugar with an isotopic composition characteristic of C3 plants. Hummingbirds were fasted and then offered a solution containing cane sugar with an isotopic composition characteristic of C4 plants. By monitoring the rates of CO2 production and O2 consumption, as well as the stable carbon isotope composition of expired CO2, we were able to estimate the relative contributions of carbohydrate and fat, as well as the absolute rate at which dietary sucrose was oxidized during hovering. The combination of respirometry and carbon isotope analysis revealed that hummingbirds initially oxidized endogenous fat following a fast and then progressively oxidized proportionately more carbohydrates. The contribution from dietary sources increased with each feeding bout, and by 20 min after the first meal, dietary sugar supported ∼74% of hovering metabolism. The ability of hummingbirds to satisfy the energetic requirements of hovering flight mainly with recently ingested sugar is unique among vertebrates. Our finding provides an example of evolutionary convergence in physiological and biochemical traits among unrelated nectar-feeding animals.

The Integration of Behaviour into Comparative Physiology

Article

Full-text available

Sep 2005

Comparative physiology has traditionally focused on the physiological responses of animals to their physicochemical environment. In recent years, awareness has increased among physiologists of the potential for behavioural factors, such as the social environment of the animal, to affect physiological condition and responses. This recognition has led to an emerging trend within the field toward using multidisciplinary approaches that incorporate both behavioural and physiological techniques. Research areas in which the integrated study of behaviour and physiology has been particularly fruitful include the physiology of the social environment, sensory physiology and behaviour, and physiological constraints on behavioural ecology. The manner in which incorporating behavioural considerations has informed the physiological data collected is discussed for each of these areas using specific examples.

Hummingbirds Fuel Hovering Flight with Newly Ingested Sugar

Article

Full-text available

Nov 2006

We sought to characterize the ability of hummingbirds to fuel their energetically expensive hovering flight using dietary sugar by a combination of respirometry and stable carbon isotope techniques. Broadtailed hummingbirds (Selasphorus platycercus) were maintained on a diet containing beet sugar with an isotopic composition characteristic of C3 plants. Hummingbirds were fasted and then offered a solution containing cane sugar with an isotopic composition characteristic of C4 plants. By monitoring the rates of CO2 production and O2 consumption, as well as the stable carbon isotope composition of expired CO2, we were able to estimate the relative contributions of carbohydrate and fat, as well as the absolute rate at which dietary sucrose was oxidized during hovering. The combination of respirometry and carbon isotope analysis revealed that hummingbirds initially oxidized endogenous fat following a fast and then progressively oxidized proportionately more carbohydrates. The contribution from dietary sources increased with each feeding bout, and by 20 min after the first meal, dietary sugar supported approximately 74% of hovering metabolism. The ability of hummingbirds to satisfy the energetic requirements of hovering flight mainly with recently ingested sugar is unique among vertebrates. Our finding provides an example of evolutionary convergence in physiological and biochemical traits among unrelated nectar-feeding animals.

EFECTO DE LA CAPACIDAD DIGESTIVA SOBRE UNA COMUNIDAD DE COLIBRÍES

Thesis

Full-text available

Nov 2014

Omar Maya

The Hummingbird Collection of the Natural History and Science Museum of the University of Porto (MHNC-UP), Portugal

Article

Full-text available

Jul 2021

Background The Hummingbird (Family Trochilidae) Collection of the Natural History and Science Museum of the University of Porto (MHNC-UP) is one of the oldest collections of this family harboured in European museums. Almost 2,000 specimens, that encompass most of the taxonomic diversity of this family, were collected in the late 19th Century. The collection is relevant due its antiquity and because all specimens were bought from the same provider, mainly as mounted specimens, for a Portuguese private collection of Neotropical fauna. In the early 20th Century, it was donated to the Museum that is now the MHNC-UP. New information The information about the majority of these specimens is now available for consultation on the GBIF platform after curation of all specimens and digital cleaning of the associated metadata. In the process, hundreds of non-catalogued specimens were found and taxonomic and spatial information was updated for many of the specimens.

Vigilance behaviors of Ruby-throated Hummingbirds (Archilochus colubris) reflect elevated risk of competitive interactions with vespine wasps

Article

Feb 2021

An Unusual Amino Acid Substitution Within Hummingbird Cytochrome c Oxidase Alters a Key Proton-Conducting Channel

Article

Full-text available

May 2020

Hummingbirds in flight exhibit the highest mass-specific metabolic rate of all vertebrates. The bioenergetic requirements associated with sustained hovering flight raise the possibility of unique amino acid substitutions that would enhance aerobic metabolism. Here, we have identified a non-conservative substitution within the mitochondria-encoded cytochrome c oxidase subunit I (COI) that is fixed within hummingbirds, but not among other vertebrates. This unusual change is also rare among metazoans, but can be identified in several clades with diverse life histories. We performed atomistic molecular dynamics simulations using bovine and hummingbird COI models, thereby bypassing experimental limitations imposed by the inability to modify mtDNA in a site-specific manner. Intriguingly, our findings suggest that COI amino acid position 153 (bovine numbering system) provides control over the hydration and activity of a key proton channel in COX. We discuss potential phenotypic outcomes linked to this alteration encoded by hummingbird mitochondrial genomes.

Flower attractiveness traits are affected differently by florivores in Tibouchina clavata (Pers.) Wurdack

Chapter

Full-text available

Jan 2019

Habitat- und Nahrungswahl

Chapter

Jan 2006

Peter Kappeler

Grundfunktionen und Verhalten

Chapter

Jan 2006

Peter Kappeler

Habitat- und Nahrungswahl

Chapter

Jan 2017

Peter Kappeler

Habitat- und Nahrungswahl

Chapter

Jan 2012

Peter Kappeler

Jedes Tier muss regelmäßig Nahrung zu sich nehmen, um die energetischen Grundlagen für Wachstum, Aufrechterhaltung der Grundfunktionen und Reproduktion zu gewährleisten. Daher kommt der Suche, Auswahl, Verteidigung und Aufnahme von Nahrung im Verhaltensrepertoire der meisten Arten eine wichtige Funktion beim tagtäglichen Überleben zu. Dabei muss ein Individuum zunächst ein geeignetes Habitat wählen und darin nach Futter suchen. Bei der Wahl des Futterplatzes muss dabei das Prädationsrisiko einerseits und die Intensität der Nahrungskonkurrenz durch Artgenossen andererseits berücksichtigt werden. In diesem Zusammenhang muss ein Tier auch entscheiden, ob es seine Nahrungsressourcen gegebenenfalls gegen Konkurrenten verteidigt. Wenn ein geeigneter Futterplatz gefunden ist, stellt sich die Frage, wie lange dieser genutzt werden sollte, bevor ein neuer gesucht wird. Beim Fressen an einer Stelle muss ein Tier außerdem entscheiden, welche der verfügbaren Nahrungseinheiten es auswählt und tatsächlich nutzt. In diesem Zusammenhang kommt es zu zahlreichen Interaktionen zwischen Tieren und Pflanzen, mit weit reichenden evolutiven Konsequenzen. Ob eine Art selbst als Räuber und/oder Beute in der Nahrungspyramide agiert, hat zudem eine Vielzahl von Konsequenzen für ihr jeweiliges Sozialverhalten (→ Kapitel 6.3).

Grundfunktionen und Verhalten

Chapter

Jan 2012

Peter Kappeler

Verhalten und Physiologie eines Organismus sind eng aufeinander abgestimmt, um ein Tier in einem regulierten Gleichgewichtszustand zu halten. Ein geregelter Energie- und Wasserhaushalt oder die Thermoregulation stellen wichtige Aspekte des Wohlergehens und der Überlebensfähigkeit dar, die einen qualitativ großen Anteil des Verhaltens eines Tieres in Anspruch nehmen können. Allerdings sind diese Verhaltensweisen selten spektakulär und werden daher bei der Diskussion der physiologischen Grundlagen in den entsprechenden Arbeiten oder Lehrbüchern oft vernachlässigt. Ähnliches gilt für Verhaltensaspekte der Stressverminderung oder Pathogenabwehr. In diesem Zusammenhang ist auf der Ebene des Organismus auch die Budgetierung von Ruhe- und Aktivitätsphasen sowie die strategische Einteilung von Zeit und Energie für bestimmte Aktivitäten relevant. Welche Rolle das Verhalten in diesen Kontexten spielt, ist in diesem Kapitel dargestellt.

Premigratory fat metabolism in hummingbirds: A Rumsfeldian approach

Article

Full-text available

Jun 2013

R.K. Suarez

Hummingbird migration is a remarkable feat, given the small body sizes of migratory species, their high metabolic rates during flight and the long distances traveled using fat to fuel the effort. Equally remarkable is the ability of premigratory hummingbirds in the wild to accumulate fat, synthesized from sugar, at rates as high as 10% of body mass per day. This paper summarizes, using Rumsfeldian terminology, "known knowns" concerning the energetics of hummingbird migration and premigratory fattening. Energy metabolism during hover-feeding on floral nectar is fueled directly by dietary sugar through the pathway recently named the "sugar oxidation cascade". However, flight without feeding for more than a few minutes requires shifting to fat as a fuel. It is proposed that behavior and metabolic fuel choice are coadapted to maximize the rate of fat deposition during premigratory fattening. The hummingbird liver appears to possess extraordinarily high capacities for fatty acid synthesis. The analysis of "known knowns" leads to identification of "known unknowns", e. g., the fates of dietary glucose and fructose, the regulation of fat metabolism and metabolic interactions between liver and adipose tissue. The history of science behooves recognition of "unknown unknowns" that, when discovered serendipitously, might shed new light on fundamental mechanisms as well as human pathological conditions.

Aggression, body condition, and seasonal changes in sex-steroids in four hummingbird species

Article

Oct 2014

Hummingbirds present a unique combination between extremely high life costs and a number of efficient adaptations to fuel these demands. In addition to cognitive abilities, territorial hummingbirds display aggressive behaviors that allow for access to better food resources. In year-round territorial species, male–male territorial aggression is similar between breeding and non-breeding seasons; however, the endocrine mechanisms underlying control of territoriality during these distinct seasonal periods may differ. In many species, testosterone (T) triggers increased aggression during the breeding season whereas territoriality in the non-breeding season can be regulated by circulating the biologically inert sex steroid precursor dehydroepiandrosterone (DHEA) and converting it to T in target tissues. The seasonal hormonal regulation of hummingbird territorial behavior has heretofore been unknown. Our goal was to assess seasonal changes in sex steroids, territorial aggression levels, and body condition during reproductive and non-reproductive seasons in hummingbirds. To validate the use of cloacal fluid (CF) for the study of sex steroids, steroid levels in plasma and CF were correlated in Sephanoides sephaniodes. During the reproductive season, Calypte. anna, Archilochus alexandri, and Selasphorus rufus males showed high levels of T that were positively correlated with aggression, but the relationship between T and body condition was not consistent across species. As expected, T levels in females were significantly lower than in males in all seasons, however still detectable. During the non-reproductive season, CF DHEA of Calypte anna was high and positively correlated with aggressive behaviors and body condition. Our results suggest that hummingbirds display aggressive behaviors that could be linked to different hormones during the breeding and non-breeding seasons.

Estrategias de extracción de néctar por pinchaflores (Aves: Diglossa y Diglossopis) y sus efectos sobre la polinización de plantas de los altos Andes

Article

Full-text available

Jan 2007

Sandra Victoria Rojas-Nossa

The flowerpiercers (Aves: Diglossa and Diglossopis) have been considered parasites of hummingbird- flower interactions because they are highly specialized nectar robbers. Nevertheless, there are documented cases where these birds realize legitimate visits to extract nectar and apparently function as pollinators of some plants. I studied some ecological aspects of these two strategies of nectar extraction by four species of flowerpiercers in the Colombian Eastern Andes. I analyzed different morphological characteristics of birds and flowers relevant to their interaction, quantified the frequency of use of both strategies by identifying the marks left by the bills on the corollas and analyzed pollen loads from the bodies of flowerpiercers. The morphology of the maxillary hook, the position of the flower and the length of the corolla were the most important characteristics determining the strategy of extraction used by the birds. The species with the shortest bill and the most strongly curved hook (Diglossa albilatera) preferred to rob the nectar while a species with long bill and less pronounced hook (Diglossopis cyanea) used both strategies in equal proportions. Tubular and erect flowers with long corollas and a high caloric production were robbed with high intensity. The flowerpiercers transported pollen from plants with pendant flowers and medium to short corollas that they visited legitimately. They could be important pollinators of native and introduced plants in high Andean ecosystems as Macleania rupestris, Brachyotum strigosum, Axinaea macrophylla, Eucalyptus globulus, Gaiadendron punctatum and Clusia multiflora.

The Integration of Osmoregulation and Energy Balance in Hummingbirds

Article

Full-text available

Nov 1990
Physiol Zool

The hummingbird's high metabolism requires efficient extraction of energy and nutrients from a dilute food source that is passing rapidly through the gastrointestinal (GI) tract. The ability of the hummingbird to efficiently process and excrete such large volumes of water must surely entail structural or functional specializations of the kidney and GI tract. The rate of water flux and nutrient extraction efficiency are also influenced, however, by the animal's feeding behavior. Because meal size affects the passage rate of food through the digestive tract (and, therefore, assimilation efficiency), feeding frequency and the amount of nectar consumed per feeding bout will affect the efficiency of nutrient absorption. Ultimately, the water and nutrient content of the nectar produced by the plants should reflect the ability of the hummingbird pollinator to balance its required intake of energy and electrolytes with its ability to excrete the accompanying water load. The simultaneous regulation of water and energy balance in hummingbirds consequently involves the complex integration of renal and intestinal functions and of these physiological processes with behavior and ecology. -from Authors

Biphasic Mass Gain in Migrant Hummingbirds: Body Composition Changes, Torpor, and Ecological Significance

Article

Full-text available

Jun 1993

Body mass of migrant Rufous Hummingbirds (Selasphorus rufus) on refueling stopovers increased on average from 3.2 to 4.6 g over a period ranging from several days to 3 wk. In birds arriving with body masses below ≈3.5 g, the initial period of mass gain was very slow. This slow gain was not explained by energy costs associated with territory establishment or learning to secure food, since it occurred even in years when nectar resources were superabundant and territoriality was nearly nonexistent. Data on body composition indicate that mass gain up to ≈3.5 g was due to deposition of nonlipid body components, which we hypothesize to be proteins involved in rebuilding muscle catabolized during the last stage of the recent migratory flight. Following the initial phase of slow mass gain, an accelerating rise in body mass consisted entirely of lipid gain. On average, overnight mass loss decreased prior to migration, suggesting that nocturnal torpor facilitated lipid deposition. The slow phase of mass gain is a potentially important constraint on migrating hummingbirds, because if they deplete their fat stores and allow their body mass to fall below 3.5 g, they incur a substantial cost in terms of greatly increased time spent on the subsequent stopover.

Time and energy constraints and the relationship between currencies in foraging theory

Article

Full-text available

Mar 1994

Measured foraging strategies often cluster around values that maximize the ratio of energy gained over energy spent while foraging (efficiency), rather than values that would maximize the long-term net rate of energy gain (rate). The reasons for this are not understood. This paper focuses on time and energy constraints while foraging to illustrate the relationship between efficiency and rate-maximizing strategies and develops models that provide a simple framework to analyze foraging strategies in two distinct foraging contexts. We assume that while capturing and ingesting food for their own use (which we term feeding), foragers behave so as to maximize the total net daily energetic gain. When gathering food for others or for storage (which we term provisioning), we assume that foragers behave so as to maximize the total daily delivery, subject to meeting their own energetic requirements. In feeding contexts, the behavior maximizing total net daily gain also maximizes efficiency when daily intake is limited by the assimilation capacity. In contrast, when time available to forage sets the limit to gross intake, the behavior maximizing total net daily gain also maximizes rate. In provisioning contexts, when daily delivery is constrained by the energy needed to power self-feeding, maximizing efficiency ensures the highest total daily delivery. When time needed to recoup energetic expenditure limits total delivery, a low self-feeding rate relative,to the rate of energy expenditure favors efficient strategies. However, as the rate of self-feeding increases, foraging behavior deviates from efficiency maximization in the direction predicted by rate maximization. Experimental manipulations of the rate of self-feeding in provisioning contexts could be a powerful tool to explore the relationship between rate and efficiency-maximizing behavior.

Territory Area, Flower Density, and Time Budgeting in Hummingbirds: An Experimental and Theoretical Analysis

Article

Full-text available

Sep 1983

While migrating southward each summer along the Sierra Nevada Mountain Range in California, nectar-feeding rufous hummingbirds Selasphorus rufus establish feeding territories within isolated meadows. The effect of variable food density upon territory area and time budgeting was studied by controlled removals and additions of flowers of Castilleja linariaefolia within the territories of immature birds. Within one day following a 50% decrease in flower density: 1) territory area usually about doubled, resulting in 2) the number of defended flowers remaining similar to the premanipulation value; 3) foraging time increased significantly from 21% to 26% of the day as the result of 4) a significant increase in foraging bout duration, with 5) bout frequency remaining unchanged; 6) daily sitting time decreased significantly from 76% to 71% of the day; and 7) daily defense time did not change significantly at 3% of the day. These patterns reversed within 1 day following subsequent experimental increases in flower density. Findings suggest that, in response to short-term variations in food availability, migrant hummingbirds are capable of adjusting territory size and time budgeting in a manner consistent with maximizing daily net energy gain. -from Authors

Specialization by territorial hummingbirds on experimentally enriched patches of flowers: Energetic profitability and learning

Article

Full-text available

Feb 2011
CAN J ZOOL

On unmanipulated hummingbird feeding territories, time spent foraging in patches was directly proportional to the number of flowers they contained. After we added nectar to the flowers in some patches, foraging increased in those patches, decreased in other patches, and decreased overall relative to control conditions. Specialization on enriched patches and reduction in foraging effort quantitatively reflected the energy we added, but the reduced effort had little effect on overall energy expenditure. Nevertheless, rates of net energy intake increased under enrichment, because gross intake rates increased. These experiments provide evidence that hummingbirds allocate effort among patches, using memory of relative patch quality when they initiate bouts of foraging. The strongest evidence is that individuals begin each day of foraging as if it were the previous day. On mornings after control days, birds foraged among patches as they had the day before, even though there was an (undiscovered) bonanza on their territories. On mornings after days of enrichment, however, whether or not a patch was enriched again, birds specialized on it at first. If the patch was enriched again, they continued to exploit it; if not, they reverted to normal patterns of allocation.

A New Function for Torpor: Fat Conservation in a Wild Migrant Hummingbird

Article

Full-text available

May 1988

Laboratory studies of torpor in small endotherms suggest that body temperature is lowered periodically only when the animal is energetically stressed. Almost no data exist on the use and importance of torpor outside laboratory situations. We have monitored the daily energy state of hummingbirds in the field. A rare observation of a torpid individual whose energy state and ecological situation were well-documented showed that migrant hummingbirds may use torpor when they are very fat and not presently energetically stressed. In this case, torpor may be a mechanism to conserve the energy stored for later use on migration.

Metabolism of flying hummingbirds

Article

Full-text available

Apr 1979
IBIS

Karl-L. Schuchmann

Field Metabolic Rate and Food Consumption by Free-Living Anna's Hummingbirds (Calypte anna)

Article

Full-text available

Nov 1988
Physiol Zool

We measured CO₂ production and water flux using doubly labeled water in wild Anna's hummingbirds living in the Santa Ana Mountains of Southern California during autumn (September) of 1981. The estimated field metabolic rate (FMR) of a hummingbird maintaining a constant body mass (mean 4.48 g) is about 32 kJ/day, which is 5.2 times basal metabolic rate (BMR). Metabolic rates during daylight hours were about 6.8 X BMR, less than one-half that expected for an Anna's hummingbird in continuous hovering flight. We estimated nighttime metabolism to be near 2.1 X BMR, which is about what would be expected for a normothermic, resting bird experiencing cool air temperatures (as low as 15 C) but much higher than expected if torpor were employed. Water influx was about 164% of body mass per day in birds maintaining a constant mass. Most of this water intake was in the form of sucrose solution from feeders in the area, but some probably came from insects eaten by the birds. Hummingbirds probably did not drink liquid water from streams or ponds during the measurement period.

Patterns of Lipid Storage and Utilization in Birds

Article

Full-text available

Sep 1976

Charles R. Blem

Nowhere among the vertebrates does the capability for storing and using triglyceride as an energy reserve exceed the level found in the class Aves. Adult avian depot fats are composed largely of 16- and 18-carbon fatty acids and are mostly unsaturated. Variation in fatty acid composition among species may be attributed to dietary differences and physiological state of the bird. Storage occurs mainly by addition of lipid to adipocyte vacuoles without an increase in cell number. Daily cycles of fat deposition and use are of greater amplitude at higher latitudes, but in general the lipid stored during the day will only provide energy for the overnight fast plus a few daylight hours. Storage levels may be minimized due to the disadvantages of increased wing-loading. A variety of behavioral, physiological and morphological adaptations may be used to reduce the need for overnight energy reserves. Migratory fattening is largely a function of migration speed, magnitude of barriers to be crossed and aerodynamic considerations. Lipid reserves are greatest in eggs of precocial birds and are retained longer in precocial young. Adaptive strategies of fat deposition in young birds are related largely to the ability of adults to feed young before and after fledging.

Mitochondrial respiration in hummingbird flight muscles

Article

Full-text available

Jul 1991

Respiration rates of muscle mitochondria in flying hummingbirds range from 7 to 10 ml of O2 per cm3 of mitochondria per min, which is about 2 times higher than the range obtained in the locomotory muscles of mammals running at their maximum aerobic capacities (VO2max). Capillary volume density is higher in hummingbird flight muscles than in mammalian skeletal muscles. Mitochondria occupy approximately 35% of fiber volume in hummingbird flight muscles and cluster beneath the sarcolemmal membrane adjacent to capillaries to a greater extent than in mammalian muscles. Measurements of protein content, citrate synthase activity, and respiratory rates in vitro per unit mitochondrial volume reveal no significant differences between hummingbird and mammalian skeletal muscle mitochondria. However, inner membrane surface areas per unit mitochondrial volume [Sv(im,m)] are higher than those in mammalian muscle. We propose that both mitochondrial volume densities and Sv(im,m) are near their maximum theoretical limits in hummingbirds and that higher rates of mitochondrial respiration than those observed in mammals are achieved in vivo as a result of higher capacities for O2 delivery and substrate catabolism.

Fuel selection in rufous hummingbirds: ecological implications of metabolic biochemistry. Proceedings of the National Academy of Science U S A

Article

Full-text available

Jan 1991

Hummingbirds in flight display the highest rates of aerobic metabolism known among vertebrates. Their flight muscles possess sufficient maximal activities of hexokinase and carnitine palmitoyltransferase to allow the exclusive use of either glucose or long-chain fatty acids as metabolic fuels during flight. Respiratory quotients (RQ = VCO2/VO2) indicate that fatty acid oxidation serves as the primary energy source in fasted resting birds, while subsequent foraging occurs with a rapid shift towards the use of carbohydrate as the metabolic fuel. We suggest that hummingbirds building up fat deposits in preparation for migration behave as carbohydrate maximizers (or fat minimizers) with respect to the metabolic fuels selected to power foraging flight.

Oxygen Consumption During Hover-Feeding in Free-Ranging Anna Hummingbirds

Article

Full-text available

Aug 1986

Rates of oxygen consumption during hover-feeding of wild, unrestrained, adult male Anna hummingbirds (Calypte anna) were measured with an artificial outdoor feeder converted into a respirometer mask. A computer sampled changes in O2 concentration in air drawn through the mask, automatically detecting the presence of a hummingbird from a drop in the O2 concentration, and photoelectrically timing the duration over which the feeder functioned as a mask. Birds coming to the feeder were weighed on a trapeze perch suspended from a force transducer. Feeding bouts consisted of sallies which carried the head in and out of the feeding mask about once a second. The volume of O2 consumed per feeding sally was linearly related to the length of the sally. The energy cost of hover-feeding in five hummingbirds, mean mass 4.6 g, was 41.5 +/- 6.3 ml O2 g-1 h-1.

Glucose absorption by a nectarivorous bird: The passive pathway is paramount

Article

Full-text available

Aug 1994
Am J Physiol

We tested the hypothesis that most sugar absorption across the small intestine's brush border is normally by a mediated pathway, i.e., the Na(+)-glucose cotransporter. In nectar-eating rainbow lorikeets (Trichoglossus haematodus, 120 g), we measured mediated D-glucose uptake in vitro using the everted-sleeve technique. The apparent Michaelis constant (7.7 mM) was similar to that observed in hummingbirds and other birds in general. Maximal mediated D-glucose uptake summed along the entire length of intestine (48 cm) was not notably high (5.34 mumol/min) when compared with other avian species and was an order of magnitude too low to explain observed rates of glucose absorption in vivo (54.5 mumol/min). This implied that nonmediated glucose absorption predominated, and independent verification of that was sought. We applied a pharmacokinetic technique to measure in vivo absorption of L-glucose, the stereoisomer that does not interact with the Na(+)-glucose cotransporter. Eighty percent of L-glucose that was ingested was absorbed, confirming that nonmediated absorption can be substantial. We discuss how equating L-glucose absorption with passive D-glucose absorption depends on certain assumptions regarding the relative importance of diffusive and convective passive flux. In either case, the conclusion about the relative importance of passive absorption should still hold.

Relationships between enzymatic flux capacities and metabolic flux rates in muscles: nonequilibrium reactions in muscle glycolysis. Proceedings of the National Academy of Science U S A

Article

Full-text available

Jul 1997

The rules that govern the relationships between enzymatic flux capacities (Vmax) and maximum physiological flux rates (v) at enzyme-catalyzed steps in pathways are poorly understood. We relate in vitro Vmax values with in vivo flux rates for glycogen phosphorylase, hexokinase, and phosphofructokinase, enzymes catalyzing nonequilibrium reactions, from a variety of muscle types in fishes, insects, birds, and mammals. Flux capacities are in large excess over physiological flux rates in low-flux muscles, resulting in low fractional velocities (%Vmax = v/Vmax x 100) in vivo. In high-flux muscles, close matches between flux capacities and flux rates (resulting in fractional velocities approaching 100% in vivo) are observed. These empirical observations are reconciled with current concepts concerning enzyme function and regulation. We suggest that in high-flux muscles, close matches between enzymatic flux capacities and metabolic flux rates (i.e., the lack of excess capacities) may result from space constraints in the sarcoplasm.

Mitochondrial function in flying honeybees (Apis mellifera): Respiratory chain enzymes and electron flow from complex III to oxygen

Article

Full-text available

Apr 2000

The biochemical bases for the high mass-specific metabolic rates of flying insects remain poorly understood. To gain insights into mitochondrial function during flight, metabolic rates of individual flying honeybees were measured using respirometry, and their thoracic muscles were fixed for electron microscopy. Mitochondrial volume densities and cristae surface densities, combined with biochemical data concerning cytochrome content per unit mass, were used to estimate respiratory chain enzyme densities per unit cristae surface area. Despite the high content of respiratory enzymes per unit muscle mass, these are accommodated by abundant mitochondria and high cristae surface densities such that enzyme densities per unit cristae surface area are similar to those found in mammalian muscle and liver. These results support the idea that a unit area of mitochondrial inner membrane constitutes an invariant structural unit. Rates of O(2) consumption per unit cristae surface area are much higher than those estimated in mammals as a consequence of higher enzyme turnover rates (electron transfer rates per enzyme molecule) during flight. Cytochrome c oxidase, in particular, operates close to its maximum catalytic capacity (k(cat)). Thus, high flux rates are achieved via (i) high respiratory enzyme content per unit muscle mass and (ii) the operation of these enzymes at high fractional velocities.

Ambient Temperature and the Daily Energetics of Two Species of Hummingbirds, Calypte anna and Selasphorus rufus

Article

Jul 1979
Physiol Zool

Anna (Calypte anna) and rufous (Selasphorus rufus) hummingbirds exhibited regular diurnal changes in body mass, locomotor activity (flight time and frequency), and feeding activity (frequency and consumption) at ambient temperatures () from 38 to -1 C. Body mass of both species increased gradually throughout the day and amounted to increases of as much as 16.4% in C. anna (7 C) and 10.8% in S. rufus (22 C). These changes in body mass were related to marked decreases in flight expenditure in the afternoon: birds of both species flew only 15%-47% as frequently after midday as they did in the morning at all temperatures. Of these afternoon flights, a higher percentage were directed toward feeding. Calypte anna increased daily mass gain (DMG) with exposure to cold (DMG = 0.01 + 0.49) by simultaneously increasing energy intake and reducing flight expenditures. Selasphorus rufus, which did not significantly increase in energy intake at below 21 C, had approximately constant DMG at from 28 to -1 C. However, overnight mass loss (OML) of S. rufus decreased when birds were exposed to cold (OML = -0.004 + 0.36), while OML of C. anna increased at low (OML = 0.006 + 0.09). Reduction of overnight expenditures at low by S. rufus may be attributed to longer torpor periods than were exhibited by C. anna. These two hummingbird species employed different strategies for maintenance of positive energy balance in this study: C. anna behaviorally regulated energy stores, maximizing daily net energy gain by manipulating both energy gains and expenditures; S. rufus relied more on physiological means (i.e., torpor) to conserve energy overnight. The latter species either behaviorally does not or physically cannot (under the conditions of this experiment) increase its daily energy stores at low .

Flight thermogenesis and energy conservation in hovering hummingbirds

Article

Apr 1998

As the smallest homeotherms, hummingbirds suffer from low thermal inertia and high heat loss. Flapping flight is energetically expensive, and convective cooling due to wing and air movements could further exacerbate energy drain. Energy conservation during flight is thus profoundly important for hummingbirds. The present study demonstrates that heat produced by flight activity can contribute to thermoregulatory requirements in hovering hummingbirds. The rate of oxygen consumption, as an indicator of metabolic cost, was measured during hover-feeding and compared with that during perch-feeding. In hover-feeding, oxygen consumption increased only moderately between 35 and 5 degrees C in contrast to the sharp increase during perch-feeding over the same temperature range. This result suggests that heat produced by contraction of the flight muscles substituted for regulatory thermogenesis to accommodate for heat loss during temperature. With declining air temperatures, the mechanical power requirements of hovering decreased slightly, but metabolic costs increased moderately. As a result, the mechanical efficiency of the muscle in converting metabolic power to mechanical power was I educed. Changes in wingbeat kinematics also accompanied the reduction in muscle efficiency. Wingbeat frequency increased but stroke amplitude decreased when hovering in the cold, suggesting thermoregulatory roles for the flight muscles. Hovering hummingbirds modulated their wingbeat frequency within a narrow range, reflecting the physical constraints of tuning to a natural resonant frequency with an elastic restoring force. We hypothesize that, by forcing the resonant system of the wings and thorax to oscillate at different frequencies, muscle contraction in the cold generates more heat at the expense of mechanical efficiency. This mechanism of modulating the efficiency of muscle contraction and heat production allows flying hummingbirds to achieve energy conservation at low air temperatures.

Oxygen Consumption of Torpid, Resting, Active, and Flying Hummingbirds

Article

Apr 1963
Physiol Zool

Robert C. Lasiewski

Respiratory Properties of Blood and Myoglobin in Hummingbirds

Article

Mar 1987
Physiol Zool

Blood respiratory properties were studied in several species of Brazilian hummingbirds. Three species, Melanotrochilus fuscus, Eupetomena macroura, and Amazilia versicolor, were studied with respect to O₂-Hb equilibrium curves and effect of pH and temperature. O₂ equilibrium of purified hemolyzates and myoglobin solutions from pectoral muscle were studied for Melanotrochilusfuscus. Hematocrit, hemoglobin content, and myoglobin concentration were studied for 11 species. Hematocrits averaged 56.3%; corresponding O₂ capacity was 22.1 vol%, and MCHC 27.0%. Average blood 02 affinity for the three species was 44.0 mmHg at pH 7.40 and 39 C. The Bohr coefficient ø was -0.39. The Hill plots were nonlinear and had increasing n-values at higher 02 saturations. The influence of temperature on the O₂-Hb equilibrium of whole blood was moderate, expressed by ΔH values of 7.0-8.0 Kcal mol⁻¹ The data are discussed with focus on the rapid changes in O₂ uptake and body temperature in hummingbirds associated with entry and arousal from torpor and the high O₂ uptakes of hovering flight. Hummingbird blood shows a very high unloading efficiency for 02. The increase in n-value at higher O₂ saturation is important because it prevents arterial desaturation during flight and nocturnal hypothermia.

Sauerstoffverbrauch von kolibris (Colibri coruscans und C. thalassinus) beim horizontalflug

Article

Jan 1985

M. Berger

Insect Flight Energetics

Chapter

Jan 1981

Tim Casey

Due to the central importance of energy metabolism to several physiological systems, data for the flight metabolism of insects has been reviewed from a variety of standpoints in the past few years. The prodigious quantities of heat produced as a by-product of flight activity has necessitated consideration of flight metabolism in reviews of insect thermoregulation (Heinrich, 1974; Kammer and Heinrich, 1978; May, 1979; Bartholomew, 1981; Kammer, 1981; Heinrich, this volume). Similarly, the interrelation between flight metabolism and contraction of the flight muscles (Pringle, 1968; Kammer and Rheuben, this volume; Josephson, 1981) and in biochemical functioning of the insect flight motor (Kammer and Heinrich, 1978; Heinrich, 1981) have recently been examined. Finally, the mechanical characteristics and power requirements of flying insects should directly affect the levels of energy metabolism of insects during flight (Weis-Fogh, 1972, 1975; Kammer and Heinrich, 1978; Nachtigall, this volume; see also symposia edited by Wu et al. 1975; Rainey, 1976; Pedley, 1977; Nachtigall, 1980).

Food Passage and Intestinal Nutrient Absorption in Hummingbirds

Article

Jul 1986
AUK

We studied adaptations of digestive physiology that permit Rufous (Selasphorus rufus) and Anna's hummingbirds (Calypte anna) to absorb sugar-water meals rapidly and efficiently. As measured with soluble markers, transit times (<15 min) and mean retention times (ca. 48 min) of meals in the hummingbird digestive tract are brief compared with values for most other vertebrates. Glucose is extracted with an efficiency of 97%. We describe a new method, employing double isotope dilution, for measuring crop-emptying kinetics. Based on this method, the crop empties half of a meal in ca. 4 min and all of the meal in 15-20 min. Rufous and Anna's hummingbirds may be energy maximizers limited by crop emptying times, rather than foraging-time minimizers. This would explain why hummingbirds spend a majority of each hour sitting rather than feeding. The intestine's passive permeability to glucose is the lowest of any vertebrate studied to date. This may be an adaptation to prevent solute loss from the blood in the face of high fluid transit rates through the intestine. Active transport accounts for essentially all intestinal glucose absorption. Compared with intestines of other vertebrates, the glucose absorption sites of hummingbird intestines have normal binding constants but are present at extremely high densities. Comparisons of hummingbirds, chickens, and shrikes suggest that intestinal absorption rates for amino acids are independent of trophic habits in birds as in other vertebrate classes, but that sugar absorption decreases in the sequence herbivore > omnivore > carnivore.

Maximum Metabolic Rate, Thermal Insulation and Aerobic Scope in a Small-Sized Chilean Hummingbird (Sephanoides sephanoides)

Article

Oct 1995

Francisco Bozinovic

Flight Energy and Estimated Flight Ranges of Some Migratory Birds

Article

Oct 1961

Seasonal allocation of time and energy resources in birds

Article

Jan 1974

J. R. King

Energy Costs and Temporal Organization of Torpor in the Rufous Hummingbird (Selasphorus rufus)

Article

Nov 1990
Physiol Zool

Sara Hiebert

Continuous records of nighttime O₂ consumption ( $\dot{V}o_{2}$ )from rufous hummingbirds (Selasphorus rufus) were used to determine O₂ consumption during normothermic nighttime rest, entry into torpor, steady-state torpor, and arousal from torpor over a range of air temperatures ( $T_{a}$ )from - 1° to 24° C. Whereas entry into torpor occurred anytime during the first 9.5 h of the 12-h night, arousals were consistently initiated within 2.5 h of the end of the night in the absence of known environmental cues. During normothermic rest, $\dot{V}o_{2}$ was inversely related to $T_{a}$ over the entire temperature range. During steady-state torpor, $\dot{V}o_{2}$ reached its lowest value at a $T_{a}$ of approximately 8° C (= $T_{a\dot{V}o_{2}min}$ ). The measured minimum body temperature ( $T_{bmin}$ ) was approximately 13° C The comparatively low values of $T_{bmin}$ and $T_{a\dot{V}o_{2}min}$ for this temperate-zone migrant species may represent an adaptation for surviving low nighttime $T_{a}'s$ in nature. Duration of the entryphase was inversely related to $T_{a}$ , but linear regression showed that total O₂ consumption (Vo₂) during entry was not systematically related to $T_{a}$ . Total oxygen consumption during arousal was inversely related to $T_{a}$ , but duration of the arousalphase peaked at approximately 8° C, decreasing at both lower and higher $T_{a}'s$ . Calculations using these data show that, at $T_{a}'s$ likely to be encountered at night in nature, rufous hummingbirds can save energy by entering torpor even if they arouse immediately without an intervening period ofsteady-state torpor.

Energetics of hummingbird foraging at low ambient temperature

Article

Jan 1999
CAN J ZOOL

Because of their small size and the high energetic costs of hovering and forward flight, hummingbirds achieve the highest mass-specific metabolic rates known among vertebrates. Rufous hummingbirds (Selasphorus rufus) stop to refuel on floral nectar in subalpine meadows as they migrate south from British Columbia to Mexico. In such habitats they face the challenges of achieving daily net energy gain despite the high energetic costs of flight and thermoregulation at near-freezing morning temperatures. Hummingbirds provided with 15 or 20% sucrose while subjected to these conditions for 4 h in the laboratory did not remain in energy balance and lost mass. However, they achieved energy balance or net energy gain on 30% sucrose. Because these sucrose concentrations are within the range observed in the nectar of hummingbird-visited flowers, the results suggest that the energetic cost of thermoregulation may influences the coevolution of hummingbirds and flowers. Hummingbirds maintaining energy balance at low ambient temperature via high foraging frequencies and high rates of energy intake can sustain average metabolic rates of about 250 W/kg over a 4-h period. These are the highest metabolic rates known among vertebrates at which rates of dietary energy intake equal rates of energy expenditure.

Energetics of hummingbird foraging at low ambient temperature

Article

Feb 1999
CAN J ZOOL

Because of their small size and the high energetic costs of hovering and forward flight, hummingbirds achieve the highest mass-specific metabolic rates known among vertebrates. Rufous hummingbirds (Selasphorus rufus) stop to refuel on floral nectar in subalpine meadows as they migrate south from British Columbia to Mexico. In such habitats they face the challenge of achieving daily net energy gain despite the high energetic costs of flight and thermoregulation at near-freezing morning temperatures. Hummingbirds provided with 15 or 20% sucrose while subjected to these conditions for 4 h in the laboratory did not remain in energy balance and lost mass. However, they achieved energy balance or net energy gain on 30% sucrose. Because these sucrose concentrations are within the range observed in the nectar of hummingbird-visited flowers, the results suggest that the energetic cost of thermoregulation may influence the coevolution of hummingbirds and flowers. Hummingbirds maintaining energy balance at low ambient temperature via high foraging frequencies and high rates of energy intake can sustain average metabolic rates of about 250 W/kg over a 4-h period. These are the highest metabolic rates known among vertebrates at which rates of dietary energy intake equal rates of energy expenditure.

Limits and constraints in the scaling of oxidative and glycolytic enzymes in homeotherms

Article

Feb 2011
CAN J ZOOL

It is now empirically well established that basal and maximum rates of O2 uptake in homeotherms scale approximately to the 0.75 power; log–log plots of mass-specific metabolic rates versus body mass yield slopes of −0.20 to 0.25. Recent studies of 10 mammalian species and 1 hummingbird species indicate that marker enzymes of mitochondrial metabolism (citrate synthase, for example) scale inversely with body mass. Hummingbirds and shrews are near the upper limit in the degree to which the oxidative capacity of heart and skeletal muscles can be elevated; further increases in mitochondrial volume densities would sacrifice myofilament or sarcoplasmic reticulum volume densities. Whales weighing about 105 kg may be near the limit at the opposite extreme because their mass-specific resting metabolic rates are predicted to be approaching those of hypometabolic ectotherms. In contrast to oxidative enzyme scaling patterns, enzymes normally operative in muscle anaerobic glycolysis, such as lactate dehydrogenase, scale directly with body mass. Hummingbirds and shrews are considered to have reduced muscle lactate dehydrogenase levels near a lower limit commensurate with buffering of cytosolic redox, a distinctly aerobic lactate dehydrogenase function. How much anaerobic glycolytic potential can be packed into muscle cells in the largest mammals is unknown; this upper limit appears to be set by a compromise between myofilament volume densities and the combined volume densities of glycogen granules, intracellular buffering components, and glycolytic enzymes.

Capricious mountain weather: a driving variable in hummingbird territorial dynamics

Article

Feb 2011
CAN J ZOOL

A violent summer hailstorm destroyed a large proportion of flowers in one of several meadows in a small mountain basin. This decimation of the resource base resulted in a dramatic decrease in the number of fall migrant rufous hummingbirds holding territories there, supporting the hypothesis that hummingbird populations closely track their food supplies. We found no evidence that the individuals displaced by the hailstorm established territories in neighboring meadows, and we therefore concluded that these individuals were forced into suboptimal habitats nearby or emigrated from the basin.

Quantitative analysis of the respiratory system of the house sparrow, budgerigar and violet-eared hummingbird

Article

Nov 1981
Respir Physiol

Martina Dubach

In the house sparrow, the budgerigar and the violet-eared hummingbird the volumes of the lungs and air sacs are estimated from silicone casts. The quantitative composition of the lungs and of their compartments are measured on lung slices, the relative volumes of the parabronchi on histological sections, and the volume composition of the blood-air capillary network of the parabronchi on electron micrographs. On electron micrographs the exchange surface and the thickness of the air-blood diffusion barrier are also measured. From these data the morphological membrane diffusion capacity is calculated and related to several organ weights. The volume of the lungs and air sacs makes up to 14–22% of the total body volume, the lungs only 2.3–2.9%. The exchange surface varies from 61 cm2/g (budgerigar) over 70 cm2/g (house sparrow) to 99 cm2/g (violet-eared hummingbird). The very thin barrier in these small birds results in a membrane diffusion capacity of 0.122 in budgerigars up to 0.271 ml O2/mm Hg·min·min·g in violet-eared hummingbirds. The various parameters are compared with those of corresponding mammals, and the quantitative advantages of the avian respiratory system are discussed.

Oxygen and the Upper Limits to Animal Design and Performance

Article

Apr 1998

R.K. Suarez

Mass-specific rates of aerobic metabolism VO2/Mb) scale in inverse proportion to body mass (Mb). Thus, small hummingbirds display the highest VO2/Mb known among vertebrates. Among all animals, higher VO2/Mb values are known only in flying insects. The high body-mass-specific rates of metabolism seen in hummingbirds are made possible by high lung O2 diffusing capacities, cardiac outputs, ratios of capillary surface area to muscle fiber surface area, mitochondrial volume densities, cristae surface densities and concentrations of enzymes involved in energy metabolism. Current evidence from control analyses of O2 transport through the respiratory and cardiovascular systems and of metabolic fluxes through pathways of energy metabolism indicates shared control of maximum flux rates among multiple steps (i.e. the absence of single rate-limiting steps). This supports the suggestion that functional capacities at each step in linear pathways or processes are matched to each other, and provides an explanation for why the up-regulation of functional capacities has occurred at virtually all steps in the evolution of the smallest vertebrate homeotherms. Flying insects make use of a tracheal system for O2 transport and, like hummingbirds, possess a highly up-regulated biochemical machinery for substrate oxidation. Studies of hummingbirds and honeybees reveal closer matches between biochemical flux capacities and maximum physiological flux rates than in animals capable of lower maximum VO2/Mb. It is proposed that the upper limits to functional capacities set the upper limit to VO2/Mb. This upper limit to aerobic metabolic rate may contribute, along with other factors, towards establishing the lower limit to vertebrate homeotherm size.

On the temperature-dependency of optimal nectar concentration for birds

Article

Jun 1979

William A. Calder

In addition to the crucial need for energy balance, the metabolically-intense hummingbirds must maintain osmotic homeostasis by regulating salt and fluid balance. Hypothetically, flowers which have coevolved with pollination by hummingbirds could provide both energy and water balance simultaneously if they produced nectars of appropriate concentrations which depend upon environmental temperature. To the extent that this has not completely adjusted, hummingbirds exposed to cold and hot extremes in temperature will have problems of water excess or deficiency, respectively.

Capillary-to-fiber geometry and mitochondrial density in hummingbird flight muscle

Article

Aug 1992
Respir Physiol

We investigated structural characteristics for high O2 flux in hummingbird flight muscle, i.e. the most O2 demanding skeletal muscle per unit tissue mass among vertebrates. Pectoralis and supracoracoideus muscles of 3-4 g hummingbirds (Selaphorus rufus) were perfusion fixed in situ, processed for electron microscopy and analyzed by morphometry. Small fiber size (group mean +/- SE, 201 +/- 14 microns 2 at 2.1 microns sarcomere length), large capillary length per fiber volume (8947 +/- 869 mm-2) and high mitochondrial volume density per volume of muscle fiber (34.5 +/- 0.9%) were characteristic features of the muscles. Considering capillary supply and mitochondrial volume on an individual fiber basis showed that the size of the capillary-to-fiber interface (i.e. capillary surface per fiber surface) was also high in the muscles. Comparison with mammalian hindlimb pointed to a major role of the size of the capillary-to-fiber interface in providing a great potential for O2 flux rate from capillary to muscle fiber mitochondria in hummingbird flight muscle.

Hummingbird Flight - Sustaining the Highest Mass-Specific Metabolic Rates among Vertebrates

Article

Jul 1992
Experientia

R.K. Suarez

Resting and maximal mass-specific metabolic rates scale inversely with body mass. Small hummingbirds achieve the highest known mass-specific metabolic rates among vertebrate homeotherms. Maximal capacities for O2 and substrate delivery to muscle mitochondria, as well as mitochondrial oxidative capacities in these animals may be at the upper limits of what are structurally and functionally possible given the constraints inherent in vertebrate design. Such constraints on the evolutionary design of functional capacities may play an important role in determining the lower limits to vertebrate homeotherm size and the upper limits to mass-specific metabolic rate.

Sustained metabolic scope

Article

Apr 1990

Sustained metabolic rates (SusMR) are time-averaged metabolic rates that are measured in free-ranging animals maintaining constant body mass over periods long enough that metabolism is fueled by food intake rather than by transient depletion of energy reserves. Many authors have suggested that SusMR of various wild animal species are only a few times resting (basal or standard) metabolic rates (RMR). We test this conclusion by analyzing all 37 species (humans, 31 other endothermic vertebrates, and 5 ectothermic vertebrates) for which SusMR and RMR had both been measured. For all species, the ratio of SusMR to RMR, which we term sustained metabolic scope, is less than 7; most values fall between 1.5 and 5. Some of these values, such as those for Tour de France cyclists and breeding birds, are surely close to sustainable metabolic ceilings for the species studied. That is, metabolic rates higher than 7 times RMR apparently cannot be sustained indefinitely. These observations pose several questions: whether the proximate physiological causes of metabolic ceilings reside in the digestive tract's ability to process food or in each tissue's metabolic capacity; whether ceiling values are independent of the mode of energy expenditure; whether ceilings are set by single limiting physiological capacities or by coadjusted clusters of capacities (symmorphosis); what the ultimate evolutionary causes of metabolic ceilings are; and how metabolic ceilings may limit animals' reproductive effort, foraging behavior, and geographic distribution.

Biosynthetic capacity of hummingbird liver

Article

Dec 1988
Am J Physiol

Hummingbirds have one of the highest mass-specific metabolic rates among vertebrate animals. High activities of pyruvate carboxylase (an enzyme involved in gluconeogenesis) and acetyl-CoA carboxylase (an enzyme involved in fatty acid synthesis) in hummingbird liver indicate that biosynthetic capacity is adjusted to cope with the high metabolic fuel requirements imposed by small size and hovering flight. This high biosynthetic capacity is supported by a correspondingly high oxidative capacity, as judged qualitatively by the abundance of mitochondria in electron micrographs and quantitatively by the presence of high citrate synthase activity (a Krebs cycle enzyme). To support their high metabolic fuel requirements, hummingbirds may possess the most biosynthetically active livers in nature.

Maximum activities of key glycolytic and oxidative enzymes in human muscle from differently trained individuals

Article

Jan 1987

1. The maximum activities of hexokinase, 6-phosphofructokinase and oxoglutarate dehydrogenase, together with capillary density and fibre composition, have been measured in muscle from male and female untrained, medium-trained and well trained individuals. 2. The activity of hexokinase was almost identical in muscle from the three groups, whereas that of 6-phosphofructokinase decreased and that of oxoglutarate dehydrogenase increased with increased training. Values of maximum rate of O2 uptake (VO2, max) were also measured and were 21% higher in medium-trained and 49% higher in well trained compared to untrained individuals, whereas oxoglutarate dehydrogenase activities were 39% and 90% higher respectively. 3. There was a good positive correlation between the activity of oxoglutarate dehydrogenase and the percentage of type I fibres but the correlation between VO2, max and oxoglutarate dehydrogenase activity was less good. Changes in the values of VO2, max represent the effects on the circulatory and respiratory system whereas those in oxoglutarate dehydrogenase represent local effects of endurance training.

Structural and Functional Limits to Oxidative Metabolism: Insights from Scaling

Article

Feb 1987

C R Taylor

Metabolic sources of energy for hummingbird flight

Article

Oct 1986
Am J Physiol

It has been known for some two decades that hovering flight in hummingbirds is the most energetically expensive muscle work known among vertebrates, but the metabolic support for such work has never been clarified. Measurement of the maximum activities of key enzymes of carbohydrate, fat, and amino acid catabolism in flight muscle and heart of rufous hummingbirds (Selasphorus rufus) reveals that the high ATP requirements of short-term hovering flight can only be supported by the oxidation of carbohydrate. Fat oxidation can support a substantially lower maximum rate of ATP turnover, indicating that this process can power only the lower +.++energetic requirements of long-term forward or migratory flight. Mitochondria isolated from flight muscle oxidize pyruvate and palmitoyl-CoA equally well. The inhibition of pyruvate oxidation by palmitoyl-CoA oxidation provides a mechanism by which fat oxidation inhibits carbohydrate oxidation in the transition from short- to long-term flight.

Digestive physiology is a determinant of foraging bout frequency in hummingbirds

Article

Mar 1986

Hummingbirds are among the smallest endothermic vertebrates. Because they forage by energetically costly hovering, and because weight-specific basal metabolic rates increase with decreasing body size, their basal and active metabolic rates are among the highest recorded. Hummingbirds fuel these metabolic requirements mainly with highly concentrated sugar in nectar, which they extract rapidly and efficiently by an unknown mechanism. It is especially puzzling that, despite their high energy requirements, hummingbirds spend only approximately 20% of their waking hours feeding, but 75% perched and apparently doing nothing. Here we report the first measurement of nutrient absorption by hummingbird intestine and present a new method for measuring crop-emptying times. We find that hummingbird intestine has the highest active glucose transport rate and lowest passive glucose permeability reported for any vertebrate. Crop-emptying time may limit feeding-bout frequency and could largely account for the time spent perched.

Design and performance of muscular systems: An overview

Article

Apr 1985

E R Weibel

For a general physiologist, A.V. Hill's definition that 'muscle is a machine that converts chemical to mechanical energy at constant temperature' is still a valid concept. But it is clearly not sufficient to tell us how muscles are used to perform a variety of different functions, such as locomotion, pumping blood through the circulation or air into the lung, or even catching prey and ingesting food. Muscles must be organized in a proper way, they must be operated in a well controlled fashion, and they need fuel which must be supplied according to needs. The 'muscular system' can thus be defined as the concerted action of molecular events permitting the generation of mechanical force, with the biochemical and physiological functions of energy supply under the control of the nervous systems. Because of the dependence of all parts of the system on all others, any part can in principle limit the performance of the entire system. One important question is therefore to see how the various parts react when the demands on the system are altered, in other words, to see how malleable the system is.

Hummingbird foraging and the relation between bioenergetics and behaviour

Abstract

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