The smallest avian genomes are found in hummingbirds

It has often been suggested that the genome sizes of birds are constrained relative to other tetrapods owing to the high metabolic demands of powered flight and the link between nuclear DNA content and red blood cell size. This hypothesis predicts that hummingbirds, which engage in energy-intensive hovering flight, will display especially constrained genomes even relative to other birds. We report genome size measurements for 37 species of hummingbirds that confirm this prediction. Our results suggest that genome size was reduced before the divergence of extant hummingbird lineages, and that only minimal additional reduction occurred during hummingbird diversification. Unlike in some other avian taxa, the small amount of variation observed within hummingbirds is not explained by variation in respiratory and flight-related parameters. Unexpectedly, genome size appears to have increased in four unrelated hummingbird species whose distributions are centred on humid forests of the upper-tropical elevational zone on the eastern slope of the Andes. This suggests that the secondary expansion of the genome may have been mediated by biogeographical and demographic effects.     

The power of feeder-mask respirometry as a method for examining hummingbird energetics

Many birds spend important portions of their time and energy flying. For this reason, quantification of metabolic rates during flight is of crucial importance to understanding avian energy balance. Measurement of organismal gas exchange rates using a mask enclosing the whole head or respiratory orifices has served as an important tool for studying animal energetics because it can free the rest of the body, permitting movement. Application of so-called “mask respirometry” to the study of avian forward flight energetics presents unique challenges because birds must be tethered to gas analysis equipment thus typically necessitating use of a wind tunnel. Resulting potential alterations to a study organism's behaviour, physiology, and aerodynamics have made interpretation of such studies contentious. In contrast, the study of hovering flight energetics in hummingbirds using a specialized form of mask respirometry is comparatively easy and can be done without a wind tunnel. Small size, hovering flight, and a nectarivorous diet are characteristics shared by all hummingbird species that make these birds ideally suited for this approach. Specifically, nectar feeders are modified to function as respirometry masks hummingbirds voluntarily respire into when hover-feeding. Feeder-mask based respirometry has revealed some of the highest vertebrate metabolic rates in hovering hummingbirds. In this review I discuss techniques for the successful measurement of metabolic rate using feeder-mask respirometry. I also emphasize how this technique has been used to address fundamental questions regarding avian flight energetics such as capacities for fuel use and mechanisms by which ecology, behaviour and energy balance are linked.     

Of hummingbirds and helicopters: hovering costs, competitive ability, and foraging strategies

Wing morphology and flight kinematics profoundly influence foraging costs and the overall behavioral ecology of hummingbirds. By analogy with helicopters, previous energetic studies have applied the momentum theory of aircraft propellers to estimate hovering costs from wing disc loading (WDL), a parameter incorporating wingspan (or length) and body mass. Variation in WDL has been used to elucidate differences either among hummingbird species in nectar-foraging strategies (e.g., territoriality, traplining) and dominance relations or among gender-age categories within species. We first demonstrate that WDL, as typically calculated, is an unreliable predictor of hovering (induced power) costs; predictive power is increased when calculations use wing length instead of wingspan and when actual wing stroke amplitudes are incorporated. We next evaluate the hypotheses that foraging strategy and competitive ability are functions of WDL, using our data in combination with those of published sources. Variation in hummingbird behavior cannot be easily classified using WDL and instead is correlated with a diversity of morphological and physiological traits. Evaluating selection pressures on hummingbird wings will require moving beyond wing and body mass measurements to include the assessment of the aerodynamic forces, power requirements, and power reserves of hovering, forward flight, and maneuvering. However, the WDL-helicopter dynamics model has been instrumental in calling attention to the importance of comparative wing morphology and related aerodynamics for understanding the behavioral ecology of hummingbirds.     

The Role of Flower Width in Hummingbird Bill Length‐Flower Length Relationships1

Observations of hummingbirds feeding at flowers longer or shorter than their bills seem to contradict the view that bill lengths of hummingbirds evolved in concert with the lengths of their flowers. Recent experiments, however, indicate that a hummingbird's ability to feed at artificial flowers of different lengths depends on the widths of the flowers. We examined if the broad range of flower lengths visited by many hummingbird species can be explained by the widths of the flowers. We predicted that both short‐ and long‐billed hummingbirds would include long, wide flower species in their diets, but that short‐billed hummingbirds would not include long, narrow flower species because nectar in these species might be beyond the reach of their bills. If so, the slope of the regression for flower width versus flower length should be smaller for flower species visited by longer‐billed hummingbirds relative to those visited by shorter‐billed hummingbirds. Analyses of data sets for some North American and Monteverde hummingbirds and their food plants were consistent with this prediction, and bill lengths were significantly correlated with the slopes of the regressions of flower width versus length for seven hummingbird species. Comparisons of observed flower use by some Monteverde hummingbird species to flower assemblages generated at random suggest that these significant regressions were not simply a result of allometric relationships between flower lengths and widths, but in some cases reflected active choice by the birds. The two hummingbird–flower data sets also differed significandy in the scaling of corolla width relative to corolla length. In particular, the Monteverde data set contained a large number of long, narrow flower species, which we suggest is a consequence of a different floral evolutionary history and association with long‐billed hummingbird species. The evolutionary effects of hummingbirds and their flowers upon one another are more complex than has generally been realized, and a consideration of corolla length jointly with other floral characters may improve our understanding of hummingbird‐flower relationships.     

The role of size and dominance in the feeding behaviour of coexisting hummingbirds

Interspecific competition can strongly influence community structure and limit the distribution and abundance of species. One of the main factors that determine hummingbird community structure is competition for food. The temporal and spatial distribution of nectar has a strong impact on hummingbird assemblages, shaping foraging niches according to hummingbird dominance and foraging strategy. We investigated whether body size and the degree of aggressive dominance influence feeding behaviour of hummingbirds in a temperate forest in northwestern Mexico (El Palmito, Mexico) when winter migrant hummingbirds are present in the community. First, we determined the dominance status of hummingbirds and evaluated the relationship between dominance and body mass, wing disc loading and migratory status. Secondly, we determined how hummingbird species used plant species differently. Thirdly, we examined whether the most dominant hummingbird species defended floral patches with more energy and/or with a larger number of flowers. At each flower patch, hummingbird species, number of hummingbird interactions, feeding time and number of flowers present were recorded. The total number of calories available within each floral patch was also determined. Our results demonstrate that the dominance hierarchy of 13 hummingbird species (migratory and resident) was correlated with body size but not wing disc loading, and that members of the hummingbird community showed a clear separation in resource use (by plant species). Hummingbirds at the top of the dominance hierarchy defended and fed on the best flower patches, defined by the quantity of calories available. Hence, the feeding behaviour of hummingbirds at El Palmito depends on the abundance of plant species used by hummingbirds and on the amount of energy available from each flower patch. Thus, hummingbird body size, aggressive dominance and defence of quality flower patches determines niche partitioning among species.     

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

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 hummingbirds: 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 distribution, while we deemed a species to be “behaviorally dominant” when it was described 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 hummingbirds. 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; however, our results provide support for the hypothesis that body mass is a supertrait that explains abundance and behavioral dominance in hummingbirds.     

BIRD EGGSHELL IN DOMINICAN AMBER

Abstract:  Here we report an eggshell in Dominican amber, representing the first vertebrate egg in any amber deposit. The eggshell is compared with present-day eggs of lizards, snails and birds. Based on the surface structure and type of shell breakage, it appears that the most likely candidate is a bird, and with that consideration, an avian group that produces eggs similar to the fossil in shape, size and colouration is the Trochilidae (hummingbirds). Several possible explanations of how the fossil could be preserved in amber are provided. If indeed a hummingbird was involved, this discovery would represent the first New World record of a fossil trochilid.     

Hummingbirds have a greatly enlarged hippocampal formation

Both field and laboratory studies demonstrate that hummingbirds (Apodiformes, Trochilidae) have exceptional spatial memory. The complexity of spatial-temporal information that hummingbirds must retain and use daily is probably subserved by the hippocampal formation (HF), and therefore, hummingbirds should have a greatly expanded HF. Here, we compare the relative size of the HF in several hummingbird species with that of other birds. Our analyses reveal that the HF in hummingbirds is significantly larger, relative to telencephalic volume, than any bird examined to date. When expressed as a percentage of telencephalic volume, the hummingbird HF is two to five times larger than that of caching and non-caching songbirds, seabirds and woodpeckers. This HF expansion in hummingbirds probably underlies their ability to remember the location, distribution and nectar content of flowers, but more detailed analyses are required to determine the extent to which this arises from an expansion of HF or a decrease in size of other brain regions.     

New specimens of the early Oligocene Old World hummingbird Eurotrochilus inexpectatus

New specimens of the early Oligocene (32 million years ago) stem group hummingbird Eurotrochilus inexpectatus Mayr, 2004, are described from the type locality Frauenweiler in Southern Germany. One of these is the second slab of the holotype, whose existence has been hitherto unknown. The new fossils add significantly to our knowledge of the morphology of E. inexpectatus and allow more detailed comparisons with other stem and crown group Trochilidae. A new apomorphy of the clade (Eurotrochilus + crown group Trochilidae) is described. With species successively more closely related to the crown group, the temporal sequence of stem group hummingbirds in Europe indicates an Old World origin of Pan-Trochilidae. E. inexpectatus is the earliest long-beaked stem group hummingbird with hovering capabilities, and absence of modern-type hummingbirds before the early Oligocene may provide a maximum age for the origin of hummingbird-pollinated plants and the colonization of the New World by modern-type stem group hummingbirds.     

Hummingbird foraging and the relation between bioenergetics and behaviour

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.     

An Assemblage of Hummingbird-pollinated Flowers in a Montane Forest in Southeastern Brazil

Relationships between ornithophilous flowers and hummingbirds have been little studied in southern South America, where hummingbird species richness is low. We studied an ornithophilous flower assemblage and the hummingbird pollinators in a montane forest in southeastern Brazil. Twenty-three native hummingbird-pollinated plant species in 21 genera and 14 families were observed. Bromeliaceae, Fabaceae, Gesneriaceae, and Lobeliaceae are represented by more than one species within the assemblage. Flower shapes vary from narrow tube to bowl-shape, but tubular flowers prevail. The variety of flower shapes and sizes results in diverse pollen placement on the body parts of hummingbird visitors, although pollen is deposited mostly on the bill. Sugar concentration in nectar averages 22.1%, and nectar volume per flower averages 16.9 μl. The plant populations bloom for one month to year-round, and their flowering approaches the steady-state pattern. Four flower subsets may be defined within the assemblage, each subset related to the bill size and foraging habits of the most frequent bird visitor. Of the six species of hummingbirds recorded at the study site, four are common and largely resident. The four hummingbirds differ in bill size, body mass, and favoured foraging sites, attributes which reflect their favoured flower subsets. One hermit and one trochiline hummingbird share most of the flower species they use, these two birds being the major pollinators within the flower assemblage. This montane forest community may be viewed as medium-rich in ornithophilous flower species and poor in hummingbird species.     

Energy expenditure in Crocidurinae shrews (Insectivora): is metabolism a key component of the insular syndrome?

A cascade of morphological, ecological, demographical and behavioural changes operates within island communities compared to mainland. We tested whether metabolic rates change on islands. Using a closed circuit respirometer, we investigated resting metabolic rate (RMR) of three species of Crocidurinae shrews: Suncus etruscus, Crocidura russula, and C. suaveolens. For the latter, we compared energy expenditure of mainland and island populations. Our measurements agree with those previously reported for others Crocidurinae: the interspecific comparison (ANCOVA) demonstrated an allometric relation between energy requirements and body mass. Energy expenditure also scaled with temperature. Island populations (Corsica and Porquerolles) of C. suaveolens differed in size from mainland (gigantism). A GLM showed a significant relationship between energy expenditure, temperature, body mass and locality. Mass specific RMR allometrically scales body mass, but total RMR does not significantly differ between mainland and island, although island shrews are giant. Our results are consistent with other studies: that demonstrated that the evolution of mammalian metabolism on islands is partially independent of body mass. In relation to the insular syndrome, we discuss how island selective forces (changes in resource availability, decrease in competition and predation pressures) can operate in size and physiological adjustments.     

Respiratory evaporative water loss during hovering and forward flight in hummingbirds

Hummingbirds represent an end point for small body size and water flux in vertebrates. We explored the role evaporative water loss (EWL) plays in management of their large water pool and its use in dissipating metabolic heat. We measured respiratory evaporative water loss (REWL) in hovering hummingbirds in the field (6 species) and over a range of speeds in a wind tunnel (1 species) using an open-circuit mask respirometry system. Hovering REWL during the active period was positively correlated with operative temperature (T_e) likely due to some combination of an increase in the vapor-pressure deficit, increase in lung ventilation rate, and reduced importance of dry heat transfer at higher T_e. In rufous hummingbirds (Selasphorus rufus; 3.3 g) REWL during forward flight at 6 and 10 m/s was less than half the value for hovering. The proportion of total dissipated heat (TDH) accounted for by REWL during hovering at T_e > 40 °C was < 40% in most species. During forward flight in S. rufus the proportion of TDH accounted for by REWL was ~ 35% less than for hovering. REWL in hummingbirds is a relatively small component of the water budget compared with other bird species (< 20%) so cutaneous evaporative water loss and dry heat transfer must contribute significantly to thermal balance in hummingbirds.     

Land use change has stronger effects on functional diversity than taxonomic diversity in tropical Andean hummingbirds

Land use change modifies the environment at multiple spatial scales, and is a main driver of species declines and deterioration of ecosystem services. However, most of the research on the effects of land use change has focused on taxonomic diversity, while functional diversity, an important predictor of ecosystem services, is often neglected. We explored how local and landscape scale characteristics influence functional and taxonomic diversity of hummingbirds in the Andes Mountains in southern Ecuador. Data was collected in six landscapes along a land use gradient, from an almost intact landscape to one dominated by cattle pastures. We used point counts to sample hummingbirds from 2011 to 2012 to assessed how local factors (i.e., vegetation structure, flowering plants richness, nectar availability) and landscape factors (i.e., landscape heterogeneity, native vegetation cover) influenced taxonomic and functional diversity. Then, we analyzed environment – trait relationships (RLQ test) to explore how different hummingbird functional traits influenced species responses to these factors. Taxonomic and functional diversity of hummingbirds were positively associated with landscape heterogeneity but only functional diversity was positively related to native vegetation coverage. We found a weak response of taxonomic and functional diversity to land use change at the local scale. Environment‐trait associations showed that body mass of hummingbirds likely influenced species sensitivity to land use change. In conclusion, landscape heterogeneity created by land use change can positively influence hummingbird taxonomic and functional diversity; however, a reduction of native vegetation cover could decrease functional diversity. Given that functional diversity can mediate ecosystem services, the conservation of native vegetation cover could play a key role in the maintenance of hummingbird pollination services in the tropical Andes. Moreover, there are particular functional traits, such as body mass, that increase a species sensitivity to land use change.     

Projected changes in elevational distribution and flight performance of montane Neotropical hummingbirds in response to climate change

The hovering flight of hummingbirds is one of the most energetically demanding forms of animal locomotion and is influenced by both atmospheric oxygen availability and air density. Montane Neotropical hummingbirds are expected to shift altitudinally upwards in response to climate change to track their ancestral climatic regime, which is predicted to influence their flight performance. In this study, we use the climate envelope approach to estimate upward elevational shifts for five Andean hummingbird species under two climate change scenarios. We then use field‐based data on hummingbird flight mechanics to estimate the resulting impact of climate change on aerodynamic performance in hovering flight. Our results show that in addition to significant habitat loss and fragmentation, projected upwards elevational shifts vary between 300 and 700 m, depending on climate change scenario and original mean elevation of the target species. Biomechanical analysis indicates that such upwards elevational shifts would yield a～2–5° increase in wing stroke amplitude with no substantial effect on wingbeat frequency. Overall, the physiological impact of elevational shifts of <1000 m in response to climate change is likely to be small relative to other factors such as habitat loss, changes in floristic composition, and increased interspecific competition.     

Rates of water turnover and energy expenditure of free-living male common seals (Phoca vitulina)

The water and energy metabolism of free-living male common seals ( Phoca vitulina ) during the mating season was investigated using labelled water methods. All three seals, which were captured on two occasions, were in negative energy balance during the study. The daily energy expenditure of one animal, estimated using doubly-labelled water was 52·5 MJ. This is equivalent to six times the basal metabolic rate predicted from Kleiber's (1975) allometric equation. Rates of water turnover were slightly lower than predicted from the allometric equation of Richmond, Langham & Trujillo (1962). The observed rates of water turnover and energy expenditure are considerably higher than those of seals which fast during the mating season, and are consistent with the observed differences in behaviour between males of the common seal and other pinniped males during mating.     

Pollination networks and functional specialization: a test using Lesser Antillean plant–hummingbird assemblages

Network analysis has in recent years improved our understanding of pollination systems. However, there is very little information about how functionally specialized plants and pollinators interact directly and indirectly in pollination networks. We have developed a parameter, Functional specialization index, to quantify functional specialization in pollination networks. Using this parameter, we examined whether different sized hummingbirds visit a distinct set of flowers in five hummingbird-pollinated plant assemblages from the Lesser Antilles, obtaining a simple relationship between hummingbird body size, network parameter and ecological function. In the Lesser Antilles, functionally specialized hummingbird pollination is distinct for plant species pollinated by the largest hummingbird species, whereas the pollination niche gradually integrates with the insect pollinator community as hummingbird body size decreases. The network approach applied in this study can be used to validate functional specialization and community-level interdependence between plants and pollinators, and it is therefore useful for evaluating and predicting plant resilience to pollinator loss, presently a global concern.     

Intraspecies variation in avian energy expenditure: correlates and constraints

Data on energy expenditure by 553 individuals of 28 species of small bird (10–150 g) are presented. All estimates of energy expenditure were obtained using the doubly-labelled water technique. Intraspecies variation in daily energy expenditure was found to be positively correlated with brood provisioning rates, percentage of time flying and the frequency of non-resting activity. Correlations were also shown with body-mass, body-size and several environmental factors. Published data on basal metabolic rates (BMR) sometimes differed substantially from estimates either made specifically as part of the studies considered here or calculated from allometric equations. For the purpose of interspecific comparisons, specific estimates of BMR are to be preferred. When expressed as a function of BMR, energy expenditures of free-living birds ranged from 1 + to 7 + times BMR with a mode at 3 +. Values of daily energy expenditure exceeding 4 times BMR were found in up to 48% of species and 30% of individuals, so that, contrary to earlier suggestions, 4 times BMR is not a universal upper limit to the sustained work rate of small birds. Observed upper limits tended to be higher in species with energy-expensive foraging habits. Energy expended by breeding birds is likely to involve a balance between the benefits a greater expenditure has for offspring production and any fitness penalty associated with the high level of energy expediture which nest provisioning involves.     

Active and resting metabolism in birds: allometry, phylogeny and ecology

Variation in resting metabolic rate is strongly correlated with differences in body weight among birds. The lowest taxonomic level at which most of the variance in resting metabolic rate and body weight is evident for the sample is among families within orders. The allometric exponent across family points is 0.67. This exponent accords with the surface area interpretation of metabolic scaling based on considerations of heat loss. Deviations of family points from this allometric line are used to examine how resting metabolic rates differ among taxa, and whether variation in resting metabolic rate is correlated with broad differences in ecology and behaviour. Despite the strong correlation between resting metabolic rate and body weight, there is evidence for adaptive departures from the allometric line, and possible selective forces are discussed.
The allometric scaling of active metabolic rate is compared with that of resting metabolic rate. The allometric exponents for the two levels of energy expenditure differ, demonstrating that active small-bodied birds require proportionately more energy per unit time above resting levels than do active large-bodied birds. No consistent evidence was found to indicate that the different methods used to estimate active metabolic rate result in systematic bias. Birds require more energy relative to body size when undertaking breeding activities than at other stages of the annual cycle.     

Energy limitation of hummingbird populations in tropical and temperate communities

Summary Regular censuses were conducted at both a temperate alpine and a tropical lowland site to determine seasonal changes in the composition of hummingbird communities and the availability of their food. From these data we calculated the total daily energy demand by the hummingbirds (Daily Energy Expenditure; DEE) and the daily energy supply available from floral nectar (Daily Energy Production; DEP) for each community census. Despite differences in habitat type and hummingbird community structure between these two sites, the hummingbird populations were often at or near carrying capacity. On average, all of the daily nectar production was cropped by the birds. We suggest that the supply/demand economics of coevolved mutualisms favour the evolution of complete resource use.