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Locomotion and Energetics of Divergent Foraging Strategies in Hummingbirds: A Review
Abstract
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.
... Furthermore, recent studies have revealed a pronounced departure from near-neighbour mating in plant species that interact with bird pollinators (Krauss et al., 2009(Krauss et al., , 2017Bezemer et al., 2019). Bird pollinators can promote non-near-neighbour mating through movements at broad spatial scales (Krauss et al., 2017), extensive pollen carry-over (Wessinger, 2020), nongrooming behaviour (Rhodes et al., 2017) and agonistic interactions with other pollinators (Sargent et al., 2021). ...
... Thus, we infer that these pollinators primarily adopt complete trapline foraging and occasionally engage in sample-and-shift trapline foraging. We argue that trapline foraging pollinators are not constrained to a single foraging tactic; rather, complete and sample-and-shift trapline foraging represents a continuum that depends on the physiological requirements of pollinators, the density of flowering individuals, the resource renewal schedule and agonistic interactions with other pollinators (Sargent et al., 2021). For example, intense pollinator competition and limited nectar resources reduce the efficiency of sample-and-shift trapline foraging, as this particular tactic increases search times and travel costs relative to complete trapline foraging (Ohashi & Thomson, 2005). ...
... That is, the fine-scale spatial pattern of particular pollinator foraging tactics can account for an important driver of the complete scope of plant mating system parameters. Thus, it is important to extend beyond a broad classification paradigm of pollinator foraging behaviour (Sargent et al., 2021) and conceptualize the fine-scale spatial pattern of particular pollinator foraging tactics. ...
Resolving the consequences of pollinator foraging behaviour for plant mating systems is a fundamental challenge in evolutionary ecology. Pollinators may adopt particular foraging tactics: complete trapline foraging (repeated movements along a fixed route), sample‐and‐shift trapline foraging (a variable route that incorporates information from previous experiences), and territorial foraging (stochastic movements within a restricted area). Studies that integrate these pollinator foraging tactics with plant mating systems are generally lacking. We investigate the consequences of particular pollinator foraging tactics for Heliconia tortuosa. We combine parentage and sibship inference analysis with simulation modeling to: (1) estimate mating system parameters; (2) infer the foraging tactic adopted by the pollinators; and (3) quantify the impact of pollinator foraging tactics on mating system parameters. We found high outcrossing rates, ubiquitous multiple paternity, and a pronounced departure from near‐neighbour mating. We also found that plants repeatedly receive pollen from a series of particular donors. We infer that the pollinators primarily adopt complete trapline foraging and occasionally engage in sample‐and‐shift trapline foraging. This enhances multiple paternity without a substantial increase in near‐neighbour mating. The particular pollinator foraging tactics have divergent consequences for multiple paternity and near‐neighbour mating. Thus, pollinator foraging behaviour is an important driver of the ecology and evolution of plant mating systems.
... A major difference between non-territorial and territorial feeding strategies is in space usage [53]. Specifically, territoriality involves frequent feeds from a small region of space, while nonterritorial strategies are more dispersed. ...
... For non-territorial birds, we expect a positive relationship between feed frequency and number of stations visited. By contrast, territorial behaviour should be associated with low number of stations visited but high feed frequency [53]. A preliminary analysis of all individuals found a nonlinear, hump-shaped relationship-the number of stations visited appeared to increase from low-to mid-level feed frequencies, but then decreased from mid-to high-level feed frequencies, suggesting that both non-territorial and territorial strategies exist in the population. ...
... In contrast with this hypothesis, we found that even though androchrome females and males have similar coloration, they differ in morphology, physiology and behaviour. Furthermore, we did not find any difference between the two female types in measures that are known to be associated with divergent feeding strategies in hummingbirds, including burst power, body size, wing load and wing shape [34,53]. Therefore, our results are inconsistent with the prediction that both androchrome females and males are co-dominant over heterochromes [23]. ...
Female-limited polymorphisms, where females have multiple forms but males have only one, have been described in a variety of animals, yet are difficult to explain because selection typically is expected to decrease rather than maintain diversity. In the white-necked jacobin (Florisuga mellivora), all males and approximately 20% of females express an ornamented plumage type (androchromic), while other females are non-ornamented (heterochromic). Androchrome females benefit from reduced social harassment, but it remains unclear why both morphs persist. Female morphs may represent balanced alternative behavioural strategies, but an alternative hypothesis is that androchrome females are mimicking males. Here, we test a critical prediction of these hypotheses by measuring morphological, physiological and behavioural traits that relate to resource-holding potential (RHP), or competitive ability. In all these traits, we find little difference between female types, but higher RHP in males. These results, together with previous findings in this species, indicate that androchrome females increase access to food resources through mimicry of more aggressive males. Importantly, the mimicry hypothesis provides a clear theoretical pathway for polymorphism maintenance through frequency-dependent selection. Social dominance mimicry, long suspected to operate between species, can therefore also operate within species, leading to polymorphism and perhaps similarities between sexes more generally.
... Here, we provide new terms to focus on two widely observed and presumably mutually exclusive behavioral strategies thought to maximize net energy gain, and which have consequences for plant reproductive success: (1) stationary interference (formerly "territoriality"), in which individuals stay within a resource patch and use aggressive behaviors to interfere with attempts of different nectarivores to access the patch and (2) traveling exploitation (formerly "traplining"), in which individuals forage on resources scattered across the landscape, traveling among foraging areas in a particular sequence (e.g., Stiles 1975;Feinsinger and Colwell 1978;Tello-Ramos et al. 2015, see Kamath andWesner 2020;Sargent et al. 2021) for a discussion on the controversies and semantic problems with the prior terms). These new terms describe both the predominant landscape range and the type of competition associated with these ends of the spectrum of behavioral strategies. ...
... This is because interfering with the foraging of competitors is most useful when competitors can access the resource as easily as the interferer, resulting in agonistic interactions collectively known as interference competition . Conversely, when foraging on a specific plant species carries a net positive benefit for only well-matched nectarivores, the focal pollinator is released from the need to defend nectar resources from all possible nectarivores (see Sargent et al. 2021). The net energy gain is thus maximized by visiting only flowers with a good match, regardless of their spatial proximity and thus a traveling exploitation strategy may be favored, in which pollinators visit plants scattered across a broad range (Ohashi and Thomson 2009;Buatois and Lihoreau 2016). ...
... In other words, videography permits us to contrast null expectations of plant-hummingbird interactions based exclusively on bill-corolla matching, with the actual interactions occurring in natural communities and thus the conditions influencing bill-corolla coevolution. Finally, by combining videography and quantification of nectar extraction performance with the wealth of knowledge about hummingbird aerodynamics and energetics in the context of floral foraging (Sargent et al. 2021, it becomes possible to quantify net energy gain, the key benefit of trait matching for the hummingbird. Altogether, these quantitative and mechanistic approaches make hummingbird-plant interactions a model system for studying the benefits of functional trait matching for both plant and pollinator and, more generally, the drivers of coevolution. ...
One of the reasons why flowering plants became the most diverse group of land plants is their association with animals to reproduce. The earliest examples of this mutualism involved insects foraging for food from plants and, in the process, pollinating them. Vertebrates are latecomers to these mutualisms, but birds, in particular, present a wide variety of nectar-feeding clades that have adapted to solve similar challenges. Such challenges include surviving on small caloric rewards widely scattered across the landscape, matching their foraging strategy to nectar replenishment rate, and efficiently collecting this liquid food from well-protected chambers deep inside flowers. One particular set of convergent traits among plants and their bird pollinators has been especially well studied: the match between the shape and size of bird bills and ornithophilous flowers. Focusing on a highly specialized group, hummingbirds, we examine the expected benefits from bill-flower matching, with a strong focus on the benefits to the hummingbird and how to quantify them. Explanations for the coevolution of bill-flower matching include 1) that the evolution of traits by bird-pollinated plants, such as long and thin corollas, prevents less efficient pollinators (e.g., insects) from accessing the nectar, and 2) that increased matching, as a result of reciprocal adaptation, benefits both the bird (nectar extraction efficiency) and the plant (pollen transfer). In addition to nectar feeding, we discuss how interference and exploitative competition also play a significant role in the evolution and maintenance of trait matching. We present hummingbird-plant interactions as a model system to understand how trait matching evolves and how pollinator behavior can modify expectations based solely on morphological matching, and discuss the implications of this behavioral modulation for the maintenance of specialization. While this perspective piece directly concerns hummingbird-plant interactions, the implications are much broader. Functional trait matching is likely common in coevolutionary interactions (e.g., in predator-prey interactions), yet the physical mechanisms underlying trait matching are understudied and rarely quantified. We summarize existing methods and present novel approaches that can be used to quantify key benefits to interacting partners in a variety of ecological systems.
... Previous reviews combining ecological and evolutionary perspectives on hummingbird pollination have mainly surveyed hummingbird morphological and behavioural diversity in foraging contexts (Feinsinger & Colwell, 1978;Stiles, 1995;Abrahamczyk & Kessler, 2015) and, more recently, linked these topics to the biomechanics of flight and nectar extraction (Altshuler & Dudley, 2002;Rico-Guevara et al., 2021;Sargent, Groom & Rico-Guevara, 2021). Numerous reviews have also addressed the evolution of bird-mediated pollination more generally (Stiles, 1978a(Stiles, , 1981Cronk & Ojeda, 2008;Pauw, 2019) or summarized the physiology and behaviour of nectarivorous birds as a whole (Carpenter, 1987;Nicolson & Fleming, 2003, 2014. ...
... Although Hermits (subfamily Phaethornithinae) generally appear loyal to a single foraging strategy (i.e. have rarely been observed defending feeding territories: Stiles, 1975Stiles, , 1985, species within the Trochilinae subfamily are not "shackled to their roles" (Feinsinger & Colwell, 1978, p. 784). Rather, these hummingbirds adjust their strategy depending on community context and the spatiotemporal availability of nectar (reviewed by Sargent et al., 2021). For example, when floral resources are not valuable or clumped enough to make territory defence energetically worthwhilesuch as in the afternoon, when nectar secretion rate slowsterritorial hummingbirds may abandon their perches (Stiles & Wolf, 1970;Cotton, 1998b;Temeles et al., 2005;Justino, Maruyama & Oliveira, 2012). ...
The ecological co-dependency between plants and hummingbirds is a classic example of a mutualistic interaction: hummingbirds rely on floral nectar to fuel their rapid metabolisms, and more than 7000 plant species rely on hummingbirds for pollination. However, threats to hummingbirds are mounting, with 10% of 366 species considered globally threatened and 60% in decline. Despite the important ecological implications of these population declines, no recent review has examined plant–hummingbird interactions in the wider context of their evolution, ecology, and conservation. To provide this overview, we (i) assess the extent to which plants and hummingbirds have coevolved over millions of years, (ii) examine the mechanisms underlying plant–hummingbird interaction frequencies and hummingbird specialization, (iii) explore the factors driving the decline of hummingbird populations, and (iv) map out directions for future research and conservation. We find that, despite close associations between plants and hummingbirds, acquiring evidence for coevolution (versus one-sided adaptation) is difficult because data on fitness outcomes for both partners are required. Thus, linking plant–hummingbird interactions to plant reproduction is not only a major avenue for future coevolutionary work, but also for studies of interaction networks, which rarely incorporate pollinator effectiveness. Nevertheless, over the past decade, a growing body of literature on plant–hummingbird networks suggests that hummingbirds form relationships with plants primarily based on overlapping phenologies and trait-matching between bill length and flower length. On the other hand, species-level specialization appears to depend primarily on local community context, such as hummingbird abundance and nectar availability. Finally, although hummingbirds are commonly viewed as resilient opportunists that thrive in brushy habitats, we find that range size and forest dependency are key predictors of hummingbird extinction risk. A critical direction for future research is to examine how potential stressors – such as habitat loss and fragmentation, climate change, and introduction of non-native plants – may interact to affect hummingbirds and the plants they pollinate.
... Examples of these potential effects include physiological and biomechanical constraints on flight performance [10,11] due to a reduction in oxygen availability and atmospheric pressure with elevation, which affect aerial agonistic [12] and display manoeuvres [13], as well as the potential cost of ornaments such as elongated tails [14]. Habitats may affect sexual dimorphism in feeding apparati when there is differential resource distribution leading to divergence in foraging strategies [15] and food niche partitioning between sexes [8,16]. Habitat structure may also affect how songs are transmitted and perceived, yielding different optima for acoustic broadcasting [17][18][19][20]. ...
Traits that exhibit differences between the sexes have been of special interest in the study of phenotypic evolution. Classic hypotheses explain sexually dimorphic traits via intra-sexual competition and mate selection, yet natural selection may also act differentially on the sexes to produce dimorphism. Natural selection can act either through physiological and ecological constraints on one of the sexes, or by modulating the strength of sexual/social selection. This predicts an association between the degree of dimorphism and variation in ecological environments. Here, we characterize the variation in hummingbird dimorphism across ecological gradients using rich databases of morphology, colouration and song. We show that morphological dimorphism decreases with elevation in the understorey and increases with elevation in mixed habitats, that dichromatism increases at high altitudes in open and mixed habitats, and that song is less complex in mixed habitats. Our results are consistent with flight constraints, lower predation pressure at high elevations and with habitat effects on song transmission. We also show that dichromatism and song complexity are positively associated, while tail dimorphism and song complexity are negatively associated. Our results suggest that key ecological factors shape sexually dimorphic traits, and that different communication modalities do not always evolve in tandem.
... Because hummingbird species generally adhere to a single foraging mode (Feinsinger & Colwell, 1978;Stiles, 1985; but see Sargent et al., 2021), phenological types may be effective filters of the local pollinator community, further promoting floral specialization in the eucentropogonids. As with floral shape, phenological types are thought to evolve either via competition for pollination or selection against interspecific pollen transfer (Kessler et al., 2020;Primack, 1985;Rathcke & Lacey, 1985). ...
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.
... In more concentrated nectar, the bird acquires more calories per microliter, but the increased viscosity reduces the volumetric uptake rate (μl s −1 ). Ultimately, nectarivores are expected to use energy gain rates (cal s −1 ), which are influenced by the coupling between floral/nectar characteristics and the nectarivore's morphology/mechanics, to make foraging decisions Sargent et al., 2021). Therefore, understanding the process of how nectar-feeding birds drink, and the links between mechanisms and ecology (e.g. ...
Nectar-feeding birds employ unique mechanisms to collect minute liquid rewards hidden within floral structures. In recent years, techniques developed to study drinking mechanisms in hummingbirds have prepared the groundwork for investigating nectar feeding across birds. In most avian nectarivores, fluid intake mechanisms are understudied or simply unknown beyond hypotheses based on their morphological traits, such as their tongues, which are semi-tubular in sunbirds, frayed-tipped in honeyeaters and brush-tipped in lorikeets. Here, we use hummingbirds as a case study to identify and describe the proposed drinking mechanisms to examine the role of those peculiar traits, which will help to disentangle nectar-drinking hypotheses for other groups. We divide nectar drinking into three stages: (1) liquid collection, (2) offloading of aliquots into the mouth and (3) intraoral transport to where the fluid can be swallowed. Investigating the entire drinking process is crucial to fully understand how avian nectarivores feed; nectar-feeding not only involves the collection of nectar with the tongue, but also includes the mechanisms necessary to transfer and move the liquid through the bill and into the throat. We highlight the potential for modern technologies in comparative anatomy [such as microcomputed tomography (μCT) scanning] and biomechanics (such as tracking BaSO4-stained nectar via high-speed fluoroscopy) to elucidate how disparate clades have solved this biophysical puzzle through parallel, convergent or alternative solutions.
... If animals are under selection to balance the energetic costs and benefits of their movements (i.e., their behaviors), then mechanistic studies of these movements, and the structures that produce them, are most valid when couched in the appropriate behavioral context. Sargent et al. (2021) contextualize studies on aerodynamics and energetics of hummingbirds with seemingly opposed behavioral strategies, namely stationary interference and traveling exploitation. Also in this lens of mechanoethology, Rico-Guevara et al. (2021) connect hummingbird bill morphology with the energetic costs and benefits of foraging on flowers with different morphologies, all while considering hummingbird behavior, ecology, and evolution. ...
Research that integrates animal behavior theory with mechanics—including biomechanics, physiology, and functional morphology—can reveal how organisms accomplish tasks crucial to their fitness. Despite the insights that can be gained from this interdisciplinary approach, biomechanics commonly neglects a behavioral context and behavioral research generally does not consider mechanics. Here, we aim to encourage the study of “mechanoethology,” an area of investigation intended to encompass integrative studies of mechanics and behavior. Using examples from the literature, including papers in this issue, we show how these fields can influence each other in three ways: 1) the energy required to execute behaviors is driven by the kinematics of movement, and mechanistic studies of movement can benefit from consideration of its behavioral context; 2) mechanics sets physical limits on what behaviors organisms execute, while behavior influences ecological and evolutionary limits on mechanical systems; and 3) sensory behavior is underlain by the mechanics of sensory structures, and sensory systems guide whole-organism movement. These core concepts offer a foundation for mehanoethology research. However, future studies focused on merging behavior and mechanics may reveal other ways by which these fields are linked, leading to further insights in integrative organismal biology.
A dominance hierarchy is the set of ranks occupied by species within an assemblage. Species with a high position within the dominance hierarchy tend to dominate subordinate species in contests for access to resources. In hummingbirds, greater weight and wing disc loading have been associated with highest ranks within the dominance hierarchy. Nevertheless, the limit to which the difference between the weight of contending species represents a competitive advantage has not yet been determined. Here, we determined the dominance hierarchy of a hummingbird assemblage exploiting the most abundant floral resource (Palicourea padifolia, Rubiaceae) in a cloud forest of central Veracruz, Mexico. Specifically, we tested whether species weight and wing disc loading influence the dominance hierarchy. Additionally, we tested whether the flowers visited per foraging bout increases with species weight and dominance. We further tested whether weight, wing disc loading, and the genetic relatedness between contenders influenced the dominance relationships in species-pair interactions. Our results indicate that the hierarchy is positively influenced by weight. Hummingbirds visited similar number of flowers regardless their weight or their dominance. Nevertheless , the probability that the heaviest contender won contests was positively associated with the differences of weight and genetic relatedness between contenders. Contrarily, the probability that the contender with greatest wing disc loading won contests was positively associated with differences of weight and negatively associated with the relatedness between contenders. However, these models only explained between 22% and 34% of the variation, respectively. Our results demonstrate that the weight was the major contributor to high dominance values. However, future studies should include (1) the temporal variability of the weight and (2) experimental predictor variables such the burst power of the hummingbirds to evaluate its effects on the dynamics of dominance hierarchies in hummingbird assemblages. All the hummingbird species present in the studied assemblage have developed wide behavioral mechanisms that compensate their morphological differences, which allow them to coexist, even when they compete for the access to the same resource.
One of the reasons why flowering plants became the most diverse group of land plants is their association with animals to reproduce. The earliest examples of this mutualism involved insects foraging for food from plants and, in the process, pollinating them. Vertebrates are latecomers to these mutualisms, but birds, in particular, present a wide variety of nectar-feeding clades that have adapted to solve similar challenges. Such challenges include surviving on small caloric rewards widely scattered across the landscape, matching their foraging strategy to nectar replenishment rate, and efficiently collecting this liquid food from well-protected chambers deep inside flowers. One particular set of convergent traits among plants and their bird pollinators has been especially well studied: the match between the shape and size of bird bills and ornithophilous flowers. Focusing on a highly specialized group, hummingbirds, we examine the expected benefits from bill-flower matching, with a strong focus on the benefits to the hummingbird and how to quantify them. Explanations for the coevolution of bill-flower matching include 1) that the evolution of traits by bird-pollinated plants, such as long and thin corollas, prevents less efficient pollinators (e.g., insects) from accessing the nectar, and 2) that increased matching, as a result of reciprocal adaptation, benefits both the bird (nectar extraction efficiency) and the plant (pollen transfer). In addition to nectar feeding, we discuss how interference and exploitative competition also play a significant role in the evolution and maintenance of trait matching. We present hummingbird-plant interactions as a model system to understand how trait matching evolves and how pollinator behavior can modify expectations based solely on morphological matching, and discuss the implications of this behavioral modulation for the maintenance of specialization. While this perspective piece directly concerns hummingbird-plant interactions, the implications are much broader. Functional trait matching is likely common in coevolutionary interactions (e.g., in predator-prey interactions), yet the physical mechanisms underlying trait matching are understudied and rarely quantified. We summarize existing methods and present novel approaches that can be used to quantify key benefits to interacting partners in a variety of ecological systems.
An animal's maneuverability will determine the outcome of many of its most important interactions. A common approach to studying maneuverability is to force the animal to perform a specific maneuver or to try to elicit maximal performance. Recently, the availability of wider-field tracking technology has allowed for high-throughput measurements of voluntary behavior, an approach that produces large volumes of data. Here, we show how these data allow for measures of inter-individual variation that are necessary to evaluate how performance depends on other traits, both within and among species. We use simulated data to illustrate best practices when sampling a large number of voluntary maneuvers. Our results show how the sample average can be the best measure of inter-individual variation, whereas the sample maximum is neither repeatable nor a useful metric of the true variation among individuals. Our studies with flying hummingbirds reveal that their maneuvers fall into three major categories: simple translations, simple rotations and complex turns. Simple maneuvers are largely governed by distinct morphological and/or physiological traits. Complex turns involve both translations and rotations, and are more subject to inter-individual differences that are not explained by morphology. This three-part framework suggests that different wingbeat kinematics can be used to maximize specific aspects of maneuverability. Thus, a broad explanatory framework has emerged for interpreting hummingbird maneuverability. This framework is general enough to be applied to other types of locomotion, and informative enough to explain mechanisms of maneuverability that could be applied to both animals and bio-inspired robots.
Unpredictable movement can provide an advantage when animals avoid predators and other threats. Previous studies have examined how varying environments can elicit unpredictable movement, but the intrinsic causes of complex, unpredictable behavior are not yet known. We addressed this question by analyzing >200 hours of flight performed by hummingbirds, a group of aerial specialists noted for their extreme agility and escape performance. We used information theory to calculate unpredictability based on the positional entropy of short flight sequences during 30-min and 2-hour trials. We show that a bird′s entropy is repeatable, with stable differences among individuals that are negatively correlated with wing loading: birds with lower wing loading are less predictable. Unpredictability is also positively correlated with a bird′s overall acceleration and rotational performance, and yet we find that moment-to-moment changes in acceleration and rotational velocities do not directly influence entropy. This indicates that biomechanical performance must share an underlying basis with a bird′s ability to combine maneuvers into unpredictable sequences. Contrary to expectations, hummingbirds achieve their highest entropy at relatively slow speeds, pointing to a fundamental trade-off whereby individuals must choose to be either fast or unpredictable.
Cities act as biological filters on native biodiversity, selecting for traits allowing species to use urban resources, which may modify the phylogenetic structure and composition of biotic assemblages. Although many studies about urban filtering have included bird communities, few have focused on diverse and specialized groups, such as hummingbirds. Here, we investigate if: (1) the urbanization process may have modified the phylogenetic and phenotypic structure of regional hummingbird assemblages in five cities along the Trans-Mexican Volcanic Belt in central Mexico, and (2) hummingbird species in urban environments have been filtered through the selection of particular morphological traits. We measured eight morphological traits related to the ability of hummingbird species to use resources, three of which (wing chord, culmen and bill curvature) were retained for phenotypic analyses. We estimated phylogenetic (MPD, mean pairwise distance, and MNTD, mean nearest taxon distance) and phenotypic structure values (pMPD and pMNTD) in regional and urban hummingbird assemblages, which allowed us to assess significant phylogenetic structure and phenotypic similarity among coexisting species, respectively. We also calculated phylogenetic signal to determine if traits are labile or conserved. We performed generalized linear mixed-effect models and a classification and regression tree analysis to determine which traits explained species’ presence in urban environments. Our results showed that urbanization modified the phylogenetic structure from a random pattern in regional assemblages towards more overdispersed values in urban assemblages, while phenotypic structure values changed either towards clustering or overdispersion in the different cities. Regression tree analyses showed that traits related to body-size and bill culmen may influence the presence of different hummingbird species in cities. Our results show that the urbanization process may change the phylogenetic and phenotypic structure of hummingbird assemblages, favoring species with generalist morphologies (intermediate body-sizes and relatively longer bills).
Schuchmann, K.L., Kirwan, G.M. & Boesman, P. (2020). Green-tailed Goldenthroat (Polytmus theresiae). In:
del Hoyo, J., Elliott, A., Sargatal, J., Christie, D.A. & de Juana, E. (eds.). Handbook of the Birds of the
World Alive. Lynx Edicions, Barcelona. (retrieved from https://www.hbw.com/node/55477).
Animal-mediated pollination is essential for the maintenance of plant reproduction, especially in tropical ecosystems, where pollination networks have been thought to have highly generalized structures. However, accumulating evidence suggests that not all floral visitors provide equally effective pollination services, potentially reducing the number of realized pollinators and increasing the cryptic specialization of pollination networks. Thus, there is a need to understand how different functional groups of pollinators influence pollination success. Here, we examined whether patterns of contemporary pollen-mediated gene flow in Heliconia tortuosa are consistent with the foraging strategy of its territorial or traplining hummingbird pollinators. Territorial hummingbirds defend clumps of flowers and are expected to transfer pollen locally. In contrast, traplining hummingbirds forage across longer distances, thereby increasing pollen flow among forest fragments, and are thought to repeatedly visit particular plants. If trapliners indeed visit the same plants repeatedly along their regular routes, this could lead to a situation where neighboring plants sample genetically distinct pollen pools. To test this hypothesis, we genotyped 720 seeds and 71 mother plants from 18 forest fragments at 11 microsatellite loci. We performed TwoGener analysis to test pollen pool differentiation within sites (among neighboring plants within the same forest fragment: Φ
SC
) and between sites (among forest fragments: Φ
CT
). We found strong, statistically significant pollen pool differentiation among neighboring mother plants (Φ
SC
= 0.0506), and weaker, statistically significant differentiation among sites (Φ
CT
= 0.0285). We interpret this pattern of hierarchical pollen pool differentiation as the landscape genetic signature of the foraging strategy of traplining hummingbirds, where repeatable, long-distance, and high-fidelity routes transfer pollen among particular plants. Although H. tortuosa is also visited by territorial hummingbirds, our results suggest that these pollinators do not contribute substantially to successful pollination, highlighting differences in realized pollination efficiency. This cryptic reduction in the number of realized pollinators potentially increases the vulnerability of pollination success to the decline of populations of traplining hummingbirds, which have been shown to be sensitive to forest fragmentation. We conclude that maintaining habitat connectivity to sustain the foraging routes of trapliners may be essential for the maintenance of pollen-mediated gene flow in human-modified landscapes.
We explored the relationship between wing morphology and flight behavior with respect to sex and age in five species of North American hummingbirds. We first measured the length, chord or “width,“ and area of entire hummingbird wing planforms. We then calculated additional parameters of wing shape and size, including aspect and shape ratios, degree of taper or “pointedness,“ wing loading, and wing disc loading (WDL). Wings of adult males are not only shorter but also more narrow and tapered than those of adult or immature females; immature males have larger wings and lower WDL, more like those of females. A proposed relationship between WDL and territorial behavior and dominance is not supported, given that adult and immature males show similar feeding territoriality outside the breeding season but females rarely do. The more extreme and divergent wings of adult males probably reflect sexual selection in connection with aerial displays that include species-specific sound effects given during the breeding season. North American species are unusual among hummingbirds in showing reversed sexual size-dimorphism (males smaller, with relatively shorter wings), a feature shared with some other small hummingbirds, notably the “Pygmornis“ hermits. Attempts to explain hummingbird foraging and territorial behavior on the basis of differences in WDL have failed because many aspects of wing morphology, physiology, and flight behavior were not taken into account. Several wing parameters appear more related to other modes of flight than to strategies of nectar exploitation, and the morphology of any given wing represents a compromise between the often conflicting aerodynamic demands of different flight modes. Understanding hummingbird flight will require broad comparative studies of wing morphology and wingbeat kinematics in relation to flight behavior, and new theoretical models and experimental data will be needed to elucidate physiological and aerodynamic mechanisms underlying forward flight and maneuvering.
Morfología Alar y Comportamiento de Vuelo de Unas Especies de Colibríes de Norteamérica
A key component of individual fitness is the ability to manage energy stores in response to variable resource availability, but because directly measuring energy budgets is difficult, daily energy management is rarely measured. Hummingbirds' energy management is relatively simple to model compared to other endotherms because they have high mass‐specific metabolic rates and store little fat. We determined which aspects of the hummingbird daily energy budget (i.e. thermoregulation, daytime activity costs, night‐time costs) change at the individual level in response to environmental variation. We found that daily energy expenditure varied threefold in two populations of broad‐billed hummingbirds (Cynanthus latirostris). Our model indicated the energy budget was distributed in the following proportions: daytime activity, 59% (range 22%–84%); thermoregulation, 23% (11%–32%); basal metabolism, 7% (3%–16%); and night‐time energy, 17% (6%–37%). Activity costs were higher at the hotter, homogeneous site and during the early‐wet season at both sites. Increased daily energy expenditure was related to decreased nectar availability and not significantly related to temperature or bird mass. With climate change, the indirect energetic costs of shifting resources could have greater impacts on endotherm energy budgets than direct costs such as thermoregulation. Increased foraging and activity costs could decrease the energy available to birds for somatic repair and reproduction, potentially causing differential fitness across seasons and sites. A plain language summary is available for this article. Plain Language Summary
Morphological trait matching between species affects resource partitioning in mutualistic systems. Yet, the determinants of spatial variation in trait matching remain largely unaddressed. Here, we generate a hypothesis that is based on the geographical distributions of species morphologies. To illustrate our hypothesis, as a study system we use hummingbirds in the tropical Andes. Hummingbirds with specialized morphologies (i.e., long or curved bills) may forage on flowers that are inaccessible to hummingbirds with generalized bill morphologies (i.e., small‐to‐medium‐sized bills with no curvature), yet the vast majority of hummingbirds have generalized bill morphologies. Thus, we propose that trait matching across space is determined by the distribution of morphological specialists. In the Andes, we observe the richness of specialized hummingbird morphotypes to peak at high and low elevations. Therefore, we hypothesize that trait matching should be most influential in predicting pairwise interactions at high and low elevations. We illustrate our hypothesis by field observations along an elevational gradient in Podocarpus National Park (Ecuador). Using Bayesian hierarchical modeling of interaction frequencies in combination with network analyzes, we found that hummingbirds at high and low elevations contributed to resource partitioning by foraging on morphologically close‐matching flowers. Moreover, at high and low elevations, hummingbirds with specialized morphologies showed a stronger tendency to visit close‐matching flowers than morphological non‐specialists did. In contrast, at mid‐elevations, hummingbirds were not attracted to morphologically close‐matching flowers. These results suggest that the spatial distribution of specialized morphotypes determines trait matching and the partitioning of interactions within hummingbird–plant communities.
Abstract in Spanish is available with online material.
Mutualistic interactions are powerful drivers of biodiversity on Earth that can be represented as complex interaction networks that vary in connection pattern and intensity. One of the most fascinating mutualisms is the interaction between hummingbirds and the plants they visit. We conducted an exhaustive search for articles, theses, reports, and personal communications with researchers (unpublished data) documenting hummingbird visits to flowers of nectar-rewarding plants. Based on information gathered from 4532 interactions between 292 hummingbird species and 1287 plant species, we built an interaction network between nine hummingbird clades and 100 plant families used by hummingbirds as nectar resources at a continental scale. We explored the network architecture, including phylogenetic, morphological, biogeographical, and distributional information. As expected, the network between hummingbirds and their nectar plants was heterogeneous and nested, but not modular. When we incorporated ecological and historical information in the network nodes, we found a generalization gradient in hummingbird morphology and interaction patterns. The hummingbird clades that most recently diversified in North America acted as generalist nodes and visited flowers with ornithophilous, intermediate and non-ornithophilous morphologies, connecting a high diversity of plant families. This pattern was favored by intermediate morphologies (bill, wing, and body size) and by the low niche conservatism in these clades compared to the oldest clades that diversified in South America. Our work is the first effort exploring the hummingbird-plant mutualistic network at a continental scale using hummingbird clades and plant families as nodes, offering an alternative approach to exploring the ecological and evolutionary factors that explain plant-animal interactions at a large scale.
As functional morphologists, we aim to connect structures, mechanisms, and emergent higher-scale phenomena (e.g., behavior), with the ulterior motive of addressing evolutionary patterns. The fit between flowers and hummingbird bills has long been used as an example of impressive co-evolution, and hence hummingbirds’ foraging behavior and ecological associations have been the subject of intense study. To date, models of hummingbird foraging have been based on the almost two-centuries-old assumption that capillary rise loads nectar into hummingbird tongue grooves. Furthermore, the role of the bill in the drinking process has been overlooked, instead considering it as the mere vehicle with which to traverse the corolla and access the nectar chamber. As a scientific community, we have been making incorrect assumptions about the basic aspects of how hummingbirds extract nectar from flowers. In this article, we summarize recent advances on drinking biomechanics, morphological and ecological patterns, and selective forces involved in the shaping of the hummingbird feeding apparatus, and also address its modifications in a previously unexpected context, namely conspecific and heterospecific fighting. We explore questions such as: how do the mechanics of feeding define the limits and adaptive consequences of foraging behaviors? Which are the selective forces that drive bill and tongue shape, and associated sexually dimorphic traits? And finally, what are the proximate and ultimate causes of their foraging strategies, including exploitative and interference competition? Increasing our knowledge of morphology, mechanics, and diversity of hummingbird feeding structures will have implications for understanding the ecology and evolution of these remarkable animals.
Intra and interspecific competition for nectar play an important role in hummingbird communities. Larger sized species usually exclude smaller species from the rich floral resources. However, it has been recently postulated that the competitive advantages of a large body size decline as the evolutionary distance between the contending species increases. In this study, we analyzed dominance hierarchy dynamics in a hummingbird assemblage in central Mexico. By monitoring hummingbird territories established in three plant species through 1 year, we assessed the effects of energy within territories and the territory owners identity in the frequency of inter and intraspecific encounters.
We also evaluated if these factors affect the dominance of larger species when they compete against smaller distantly related contenders. Our results show that their frequency of intraspecific encounters was related with the identity of the territory’s owner. On the contrary, the frequency of interspecific encounters was related with both the territory and the identity of the territory’s owner. We did not find a significant difference between the number of encounters dominated by larger and smaller species and their contenders. However, the increase in genetic distance between contenders was positively associated with a higher frequency of encounters dominated by small hummingbirds.
Our results showed that the ecological factors and evolutionary relationships among
contenders play important roles in the dominance hierarchy dynamics.
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.
Flying animals of different masses vary widely in body proportions, but the functional implications of this variation are often unclear. We address this ambiguity by developing an integrative allometric approach, which we apply here to hummingbirds to examine how the physical environment, wing morphology and stroke kinematics have contributed to the evolution of their highly specialised flight. Surprisingly, hummingbirds maintain constant wing velocity despite an order of magnitude variation in body weight; increased weight is supported solely through disproportionate increases in wing area. Conversely, wing velocity increases with body weight within species, compensating for lower relative wing area in larger individuals. By comparing inter-and intraspecific allometries, we find that the extreme wing area allometry of hummingbirds is likely an adaptation to maintain constant burst flight capacity and induced power requirements with increasing weight. Selection for relatively large wings simultaneously maximises aerial performance and minimises flight costs, which are essential elements of humming bird life history.
Hummingbirds are important pollinators of many native Neotropical plants but their abundance and diversity in landscapes dominated by intensive human uses such as agriculture have rarely been examined, despite such land-uses prevailing in the tropics. We examined how tropical deforestation affects hummingbird community structure in premontane forest patches embedded in a tropical countryside of Coto Brus Canton, Costa Rica. We captured hummingbirds in fourteen landscapes representing a gradient in patch size and forest amount, and tested for the effects of these variables on (1) hummingbird captures at flowers (pollinator availability); (2) species richness; and (3) filtering of functional traits. After accounting for sampling effects, both hummingbird availability and species richness declined by 40% and 50%, respectively, across the gradient in deforestation that we observed (9–66% forest within 1000 m). Focal patch size was the strongest predictor, even after statistically accounting for the amount of forest and matrix composition of landscapes. These reductions in availability and richness were well predicted by functional traits; morphologically specialized species with the capacity to transport long-distance outcrossed pollen and low functional redundancy within the pollinator network showed the greatest sensitivity to landscape change. We hypothesize that declines in hummingbird availability, diversity, and functional traits are important mechanisms driving the observed pollen limitation of ornithophilous flowers in fragmented tropical landscapes. Efforts to conserve large forest patches and enhance matrix permeability are critical for maintaining forest hummingbird communities and pollination services under current and predicted deforestation regimes.
The majority of the world's living primates inhabit lowland tropical rainforests, a diverse and often challenging habitat type to navigate. The large collection of field-based research has demonstrated the incredible behavioral and dietary flexibility among primate species when coping with food resources that vary both temporally and spatially across seasons. Finding prey items, whether they are insects or plant parts, is challenging, and thus primates have evolved a variety of adaptations to obtain sufficient energy for survival. This entry discusses the cognitive and sensory mechanisms used by primates to find food, why they may include certain items in the diet while ignoring others, and social factors that may influence diet selection.
The study of animals in the wild offers opportunities to collect relevant information on their natural behavior and abilities to perform ecologically relevant tasks. However, it also poses challenges such as accounting for observer effects, human sensory limitations, and the time intensiveness of this type of research. To meet these challenges, field biologists have deployed camera traps to remotely record animal behavior in the wild. Despite their ubiquity in research, many commercial camera traps have limitations, and the species and behavior of interest may present unique challenges. For example, no camera traps support high-speed video recording. We present a new and inexpensive camera trap system that increases versatility by separating the camera from the triggering mechanism. Our system design can pair with virtually any camera and allows for independent positioning of a variety of sensors, all while being low-cost, lightweight, weatherproof, and energy efficient. By using our specialized trigger and customized sensor configurations, many limitations of commercial camera traps can be overcome. We use this system to study hummingbird feeding behavior using high-speed video cameras to capture fast movements and multiple sensors placed away from the camera to detect small body sizes. While designed for hummingbirds, our application can be extended to any system where specialized camera or sensor features are required, or commercial camera traps are cost-prohibitive, allowing camera trap use in more research avenues and by more researchers.
During flight, hummingbirds achieve the maximum aerobic metabolism rates within vertebrates. To meet such demands, these birds have to take in as much energy as possible, using strategies such as selecting the best food resources and adopting behaviors that allow the greatest energy gains. We tested whether hummingbirds choose sources that have higher sugar concentrations, and investigated their behaviors near and at food resources. The study was conducted at Atlantic forest remnant in Brazil, between June and December 2012. Four patches were provided with artificial feeders, containing sucrose solutions at concentrations of 5%, 15%, 25% and 35% weight/volume. Hummingbird behaviors were recorded using the ad libitum method with continuous recording of behaviors. The following species were observed: the Brazilian ruby Clytolaema rubricauda (Boddaert, 1783), Violet-capped woodnymph Thalurania glaucopis (Gmelin, 1788), Scale-throated hermit Phaethornis eurynome (Lesson, 1832), White-throated hummingbird Leucochloris albicollis (Vieillot, 1818), Versicoloured emerald Amazilia versicolor (Vieillot, 1818), Glittering-bellied emerald Chlorostilbon lucidus (Shaw, 1812) and other Phaethornis spp. C. rubricauda, P. eurynome and Phaethornis spp. visited the 35%-sucrose feeders more often, while the T. glaucopis visited the 25%-sucrose feeders more often. L. albicollis and A. versicolor visited more often solutions with sugar concentration of 15%. C. lucidus visited all patches equally. Three behavioral strategies were observed: 1) C. rubricauda and T. glaucopis exhibited interspecific and intraspecific dominance; 2) the remaining species exhibited subordinance to the dominant hummingbirds, and 3) P. eurynome and Phaethornis spp. adopted a hide-and-wait strategy to the dominant hummingbird species. The frequency of aggressive behaviors was correlated with the time the hummingbird spent feeding, and bird size. Our results showed that hummingbirds can adopt different strategies to enhance food acquisition; that more aggressive species feeding more than less aggressive species; and that the birds, especially if they were dominant species, visited high quality food resources more often.
High-elevation habitats offer ecological advantages including reduced competition, predation, and parasitism [1]. However, flying organisms at high elevation also face physiological challenges due to lower air density and oxygen availability [2]. These constraints are expected to affect the flight maneuvers that are required to compete with rivals, capture prey, and evade threats [3-5]. To test how individual maneuvering performance is affected by elevation, we measured the free-flight maneuvers of male Anna's hummingbirds in a large chamber translocated to a high-elevation site and then measured their performance at low elevation. We used a multi-camera tracking system to identify thousands of maneuvers based on body position and orientation [6]. At high elevation, the birds' translational velocities, accelerations, and rotational velocities were reduced, and they used less demanding turns. To determine how mechanical and metabolic constraints independently affect performance, we performed a second experiment to evaluate flight maneuvers in an airtight chamber infused with either normoxic heliox, to lower air density, or nitrogen, to lower oxygen availability. The hypodense treatment caused the birds to reduce their accelerations and rotational velocities, whereas the hypoxic treatment had no significant effect on maneuvering performance. Collectively, these experiments reveal how aerial maneuvering performance changes with elevation, demonstrating that as birds move up in elevation, air density constrains their maneuverability prior to any influence of oxygen availability. Our results support the hypothesis that changes in competitive ability at high elevations are the result of mechanical limits to flight performance [7].
Background
Territory owners usually defeat intruders. One explanation for this observation is the uncorrelated asymmetry hypothesis which argues that contests might be settled by an arbitrary convention such as “owners win.” We studied the effect of territorial residency on contest asymmetries in the white-eared hummingbird (Hylocharis leucotis) in a fir forest from central Mexico.
Methods
Twenty white-eared male adult hummingbird territories were monitored during a winter season, recording the territorial behavior of the resident against intruding hummingbirds. The size and quality of the territory were related to the probability that the resident would allow the use of flowers by the intruder. Various generalized models (logistical models) were generated to describe the probabilities of victory for each individual resident depending on the different combinations of three predictor variables (territory size, territory quality, and intruder identity).
Results
In general, small and low quality territory owners tend to prevent conspecific intruders from foraging at a higher rate, while they frequently fail to exclude heterospecific intruders such as the magnificent hummingbird (Eugenes fulgens) or the green violetear hummingbird (Colibri thalassinus) on any territory size. Our results showed that the identity of the intruder and the size and quality of the territory determined the result of the contests, but not the intensity of defense.
Discussion
Initially, the rule that “the resident always wins” was supported, since no resident was expelled from its territory during the study. Nevertheless, the resident-intruder asymmetries during the course of a day depended on different factors, such as the size and quality of the territory and, mainly, the identity of the intruders. Our results showed that flexibility observed in contest tactics suggests that these tactics are not fixed but are socially plastic instead and they can be adjusted to specific circumstances.
Specialization of species in interaction networks influences network stability and ecosystem functioning. Spatial and temporal variation in resource availability may provide insight into how ecological factors, such as resource abundance, and evolutionary factors, such as phylogenetically conserved morphological traits, influence specialization within mutualistic networks. We used independent measures of hummingbird abundance and resources (nectar), information on hummingbird traits and plant-hummingbird interactions to examine how resource availability and species' morphology influence the specialization of hummingbirds in three habitat types (forest, shrubs, cattle ranch) sampled over 10 sessions across two years in the southern Andes of Ecuador. Specialization of hummingbird species in the networks was measured by three indices: d' (related to niche partitioning), generality (related to niche width) and PSI (related to pollination services). Specialization indices d', generality and PSI of hummingbird species were influenced by resource availability. All indices indicated that specialization of hummingbirds increased when the availability of resources decreased. Variation in d' was also explained by an interaction between resource availability and bill length; hummingbirds with a long bill switched from being more specialized than other species when resource availability was low to being similarly specialized when availability was high. Overall, our results highlight the importance of ecological and evolutionary factors determining the specialization of species in interaction networks. We demonstrate in particular that ecological gradients in resource availability cause substantial changes in consumers' foraging behavior contingent on their morphology. Changes in pollinator specialization along resource gradients can have impacts on ecosystem functions, such as pollination by animals.
Costly interactions between species that arise as a by-product of ancestral similarities in communication signals are expected to persist only under specific evolutionary circumstances. Territorial aggression between species, for instance, is widely assumed to persist only when extrinsic barriers prevent niche divergence or selection in sympatry is too weak to overcome gene flow from allopatry. However, recent theoretical and comparative studies have challenged this view. Here we present a large-scale, phylogenetic analysis of the distribution and determinants of interspecific territoriality. We find that interspecific territoriality is widespread in birds and strongly associated with hybridization and resource overlap during the breeding season. Contrary to the view that territoriality only persists between species that rarely breed in the same areas or where niche divergence is constrained by habitat structure, we find that interspecific territoriality is positively associated with breeding habitat overlap and unrelated to habitat structure. Furthermore, our results provide compelling evidence that ancestral similarities in territorial signals are maintained and reinforced by selection when interspecific territoriality is adaptive. The territorial signals linked to interspecific territoriality in birds depend on the evolutionary age of interacting species, plumage at shallow (within-family) timescales, and song at deeper (between-family) timescales. Evidently, territorial interactions between species have persisted and shaped phenotypic diversity on a macroevolutionary timescale.
Torpor is an important energy saving strategy in some small birds, but it has rarely been studied in natural field conditions. We compared torpor use across 43 wild‐caught individuals of eight hummingbird species across sites with different natural temperature regimes. Most laboratory studies focus on the relationship between metabolic rate and temperature, but our aim was to evaluate what environmental factors most influence hummingbird nighttime energy management under natural conditions. We found that the probability of an individual entering torpor was weakly correlated with mass but unrelated to nighttime temperature and that hummingbirds at both warm, tropical and cooler, temperate sites used torpor. Energy savings in torpor were maximized as ambient temperatures approached a species’ minimum body temperature, consistent with laboratory studies; energy savings ranged between 65‐92% of energy per hour in torpor compared to normothermy. However, regardless of the degree of energy savings in torpor, variation in total nighttime energy expenditure was most significantly influenced by torpor bout duration. Lab studies largely assess the effect of temperature on torpor use, but our findings indicate that other environmental conditions are more important in determining hummingbirds’ total nighttime energy expenditure under natural temperature cycles. Our results show that a small endotherm's nighttime energy management in its natural habitat is more affected by torpor bout duration, which is linked to photoperiod, than by temperature. This result suggests that in their natural environments hummingbirds are able to save energy in torpor across a range of nighttime temperatures, indicating that they may have sufficient physiological flexibility to tolerate climatic variation.
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Within‐clade allometric relationships represent standard laws of scaling between energy and size, and their outliers provide new avenues for physiological and ecological research. According to the metabolic level boundaries hypothesis, metabolic rates as a function of mass are expected to scale closer to 0.67 when driven by surface‐related processes (e.g., heat or water flux), while volume‐related processes (e.g., activity) generate slopes closer to one. In birds, daily energy expenditure (DEE) scales with body mass (M) in the relationship log (DEE) = 2.35 + 0.68 * log (M), consistent with surface‐level processes driving the relationship. However, taxon‐specific patterns differ from the scaling slope of all birds. Hummingbirds have the highest mass‐specific metabolic rates among all vertebrates. Previous studies on a few hummingbird species, without accounting for the phylogeny, estimated that the DEE‐body mass relationship for hummingbirds was log (DEE) = 1.72 + 1.21 * log (M). Contrary to theoretical expectations, this slope greater than 1 indicates that larger hummingbirds are less metabolically efficient than smaller hummingbirds. We collected DEE and mass data for 12 hummingbird species, which, combined with published data, represented 17 hummingbird species in eight of nine hummingbird clades over a six‐fold size range of body size (2.7 ‐ 17.5 g). After accounting for phylogenetic relatedness, we found daily energy expenditure scales with body mass as log (DEE) = 2.04 + 0.95 * log (M). This slope of 0.95 is lower than previously estimated for hummingbirds, but much higher than the slope for all birds (0.68). The high slopes of torpor, hovering and flight potentially explain the high interspecific DEE slope for hummingbirds compared to other endotherms.
We observed territorial Purple-throated Caribs (Eulampis jugularis) on three Heliconia morphs (H. caribaea and the red-green and green morphs of H. bihai) on the island of St. Lucia, West Indies, to examine how calculated costs and benefits compared with observed patterns of Heliconia use. Across the three years of our study, H. caribaea territories defended by Purple-throated Carib males were significantly smaller in area and had higher densities of flowers than red-green H. bihai territories, and both kinds of Heliconia territories defended by males were smaller and had higher densities of flowers than the green H. bihai territory maintained by a female. In the period (0630 to 1400 hours) during which birds maintained territories, total maintenance costs were more than met by energy obtained from territories, but only 2 of 13 territories provided sufficient nectar to meet birds' energy requirements for 24 h. Birds supplemented their energy intake from Heliconia territories by foraging at flowers in the rainforest canopy, and the percentage of time a territorial bird spent foraging in the canopy was inversely correlated with energy production on its Heliconia territory. The smaller territory areas and higher flower densities of H. caribaea territories lowered males' foraging time and energy costs per flower on H. caribaea as compared with red-green H. bihai territories, theoretically allowing them to meet their energy demands in less time and at lower cost. Males' estimated foraging time and energy costs were greatest at the green morph of H. bihai; compared with females, they would save a higher proportion of time and energy by foraging at H. caribaea and the red-green morph of H. bihai. That asymmetry between males and females in relative gains from foraging at each of the three Heliconia morphs may further reinforce resource partitioning between them, in addition to differences in size and fighting abilities.
Economía de Forrajeo y Territorialidad en la Especie Sexualmente Dimórfica Eulampis jugularis en Tres Formas de Heliconia
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.
Animals that feed from resources that are constant in space and that refill may benefit from repeating the order in which they visit locations. This is a behavior known as traplining, a spatial phenomenon. Hummingbirds, like other central‐place foragers, use short traplines when moving between several rewarding sites. Here we investigated whether traplining hummingbirds also use relevant temporal information when choosing which flowers to visit. Wild rufous hummingbirds that were allowed to visit three artificial flower patches in which flowers were refilled 20 minutes after they had been depleted, repeated the order in which they visited the three patches. Although they tended to visit the first two patches sooner than 20 minutes, they visited the third patch at approximately 20 minutes intervals. The time between visits to the patches increased across the experiment, suggesting that the birds learned to wait longer before visiting a patch. The birds appeared to couple the sequential pattern of a trapline with temporal regularity, to some degree. This suggests that there is a temporal component to the repeated spatial movements flown by foraging wild hummingbirds.
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The majority of the world's living primates inhabit lowland tropical rainforests, a diverse and often challenging habitat type to navigate. The large collection of field‐based research has demonstrated the incredible behavioral and dietary flexibility among primate species when coping with food resources that vary both spatially and temporally. Finding prey items, whether they are insects or plant parts, is challenging, and thus primates have evolved a variety of adaptations to acquire sufficient energy for survival. This entry discusses the cognitive and sensory mechanisms used by primates to find food, why they may include certain items in the diet while ignoring others, and social factors that may influence diet selection.
Wing kinematics and morphology are influential upon the aerodynamics of flight. However, there is a lack of studies linking these variables to metabolic costs, particularly in the context of morphological adaptation to body size. Furthermore, the conversion efficiency from chemical energy into movement by the muscles (mechanochemical efficiency) scales with mass in terrestrial quadrupeds, but this scaling relationship has not been demonstrated within flying vertebrates. Positive scaling of efficiency with body size may reduce the metabolic costs of flight for relatively larger species. Here, we assembled a dataset of morphological, kinematic, and metabolic data on hovering hummingbirds to explore the influence of wing morphology, efficiency, and mass on hovering metabolic rate (HMR). We hypothesize that HMR would decline with increasing wing size, after accounting for mass. Furthermore, we hypothesize that efficiency will increase with mass, similarly to other forms of locomotion. We do not find a relationship between relative wing size and HMR, and instead find that the cost of each wingbeat increases hyperallometrically while wingbeat frequency declines with increasing mass. This suggests that increasing wing size is metabolically favourable over cycle frequency with increasing mass. Further benefits are offered to larger hummingbirds owing to the positive scaling of efficiency.
Making quick turns
Hummingbirds are well known for their impressive maneuvering during flight. Dakin et al. used a computer vision approach to characterize the details of flight in >200 hummingbirds from 25 species (see the Perspective by Wainwright). Larger species had enhanced agility owing to increased muscle mass. In all species, muscles dictated transitional movement, whereas wing shape facilitated sharp turns and rapid rotations. Species, and individuals within species, played on their strengths by combining inherent traits and learned skills.
Science , this issue p. 653 ; see also p. 636
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.
Using red knots (Calidris canutus) as a model, we determined how changes in mass and metabolic activity of organs relate to temperature-induced variation in metabolic performance. In cold-acclimated birds, we expected large muscles and heart, improved oxidative capacity and lipid transport, and we predicted that this would explain variation in maximal thermogenic capacity (Msum). We also expected larger digestive and excretory organs in these birds and predicted that this would explain variation in basal metabolic rate (BMR). Knots kept at 5°C were 20% heavier and maintained 1.5 times more body fat than individuals kept at thermoneutrality (25°C). Cold-acclimated birds also had a BMR up to 32% higher and a Msum 16% higher than birds at 25°C. Organs were larger in the cold, with muscles and heart being 9-20% heavier and digestive and excretory organs being 21-36% larger than at thermoneutrality. Rather than the predicted digestive and excretory organs, the cold-induced increase in BMR correlated with changes in mass of the heart, pectoralis and carcass. Msum varied positively with the mass of the pectoralis, supracoracoideus and heart, highlighting the importance of muscles and cardiac function in cold endurance. Cold-acclimated knots also expressed upregulated capacity for lipid transport across mitochondrial membranes in their pectoralis and leg muscles, higher lipid catabolism capacity in their pectoralis muscles and elevated oxidative capacity in their liver and kidney. These adjustments may have contributed to BMR through changes in metabolic intensity. Our results also suggest indirect constraints on thermogenic capacity through limited cardiac capacity.
Coexistence between ecologically similar species can promote competition for resources. Hummingbirds (Aves: Trochilidae) are nectarivorous birds that usually coexist in sympatry, and visit flowers using different foraging behaviors and levels of aggressiveness as a strategy to diminish resource competition. Here, we describe the dynamics in territorial and dominance behaviors in a hummingbird community inhabiting a highland during winter in Western Mexico. We explored in natural conditions how foraging strategies and dominance status of the hummingbirds was influenced by community species composition, sex, age and size of the individuals, floral abundance, and nectar resource availability. The community studied was composed of 11 species (four residents, three altitudinal migrants, three latitudinal migrants), and all possible combinations of dominance and territoriality were found. Differences in the dominance status and foraging behavior were related to the species, sex, age and body size of the individuals, as well as the number of flowers in the patches, and the abundance of the migratory species over time. The aggressive and territorial species preferred the places with more flowers, and started the majority of the interactions attacking even birds that did not visited the flowers. The subordinate non-territorial hummingbirds visited floral patches of different sizes, did not start aggressive interactions and when they were involved in one, this occurred during their visits to the territorial hummingbird's flowers. Hummingbird dominance changed during the winter and at the end of the season, when the latitudinal migrant species left our study site, the resident species were more abundant, dominant and territorial. Dominance status and foraging behavior, together with floral preferences and the spatial distribution of nectar resources, acted as mechanisms organizing this hummingbird community.
Despite recent advances in our understanding of animal flight, the
biomechanical determinants of maneuverability in birds are poorly
understood. It is thought that maneuverability is influenced by
morphological features such as body mass, wing size, and wing
shape, as well as by physiological traits such as muscle capacity. This
hypothesis has not been evaluated for any animal because large
numbers of measurements of free flight maneuvers from the same
individuals have been lacking. We recorded a large number of flight
sequences for 20 Anna's hummingbirds (Calypte anna) in a flight
chamber to determine if an individual's maneuvering performance is
1) repeatable across trials, 2) associated with morphology, burst
muscle capacity, or both, and 3) influenced by the presence of a
competitor. Using a multi-camera tracking system, we analyzed
performance metrics based on body position and orientation. Most
measures were highly repeatable. Burst muscle capacity was
associated with most performance metrics, such that birds with
higher burst capacity flew with faster velocities, accelerations, and
rotations, and performed more demanding complex turns. Wing
morphology predicted only a few performance metrics, such that
birds with higher wing aspect ratio had higher centripetal
acceleration and performed more arcing turns. In the presence of a
competitor, birds exhibited faster changes in pitch and altered the
types of complex turns used, but surprisingly, they had lower
horizontal accelerations. Collectively, these results indicate that burst
muscle capacity is a key predictor of maneuverability, and that body
angular velocity and arcing turns are associated with competition in
flight.
This example is provided so that non-theorists may see actual applications of the theory previously described. The Dickcissel sex ratio is employed as an indirect index of suitability. A sex ratio index was found to be correlated positively with density. This is consistent with the hypothesis that territorial behavior in the males of this species limits their density. This study provides a valid example of how the problem can be approached and offers a first step in the eventual identification of the role of territorial behavior in the habitat distribution of a common species.