Douglas L. Altshuler

Phylogenetic Systematics and Biogeography of Hummingbirds: Bayesian and Maximum Likelihood Analyses of Partitioned Data and Selection of an Appropriate Partitioning Strategy

Hummingbirds are an important model system in avian biology, but to date the group has been the subject of remarkably few phylogenetic investigations. Here we present partitioned Bayesian and maximum likelihood phylogenetic analyses for 151 of approximately 330 species of hummingbirds and 12 outgroup taxa based on two protein-coding mitochondrial genes (ND2 and ND4), flanking tRNAs, and two nuclear introns (AK1 and BFib). We analyzed these data under several partitioning strategies ranging between unpartitioned and a maximum of nine partitions. In order to select a statistically justified partitioning strategy following partitioned Bayesian analysis, we considered four alternative criteria including Bayes factors, modified versions of the Akaike information criterion for small sample sizes (AIC(c)), Bayesian information criterion (BIC), and a decision-theoretic methodology (DT). Following partitioned maximum likelihood analyses, we selected a best-fitting strategy using hierarchical likelihood ratio tests (hLRTS), the conventional AICc, BIC, and DT, concluding that the most stringent criterion, the performance-based DT, was the most appropriate methodology for selecting amongst partitioning strategies. In the context of our well-resolved and well-supported phylogenetic estimate, we consider the historical biogeography of hummingbirds using ancestral state reconstructions of (1) primary geographic region of occurrence (i.e., South America, Central America, North America, Greater Antilles, Lesser Antilles), (2) Andean or non-Andean geographic distribution, and (3) minimum elevational occurrence. These analyses indicate that the basal hummingbird assemblages originated in the lowlands of South America, that most of the principle clades of hummingbirds (all but Mountain Gems and possibly Bees) originated on this continent, and that there have been many (at least 30) independent invasions of other primary landmasses, especially Central America.

Molecular Phylogenetics and the Diversification of Hummingbirds

The tempo of species diversification in large clades can reveal fundamental evolutionary mechanisms that operate on large temporal and spatial scales. Hummingbirds have radiated into a diverse assemblage of specialized nectarivores comprising 338 species, but their evolutionary history has not, until now, been comprehensively explored. We studied hummingbird diversification by estimating a time-calibrated phylogeny for 284 hummingbird species, demonstrating that hummingbirds invaded South America by ∼22 million years ago, and subsequently diversified into nine principal clades (see [5-7]). Using ancestral state reconstruction and diversification analyses, we (1) estimate the age of the crown-group hummingbird assemblage, (2) investigate the timing and patterns of lineage accumulation for hummingbirds overall and regionally, and (3) evaluate the role of Andean uplift in hummingbird speciation. Detailed analyses reveal disparate clade-specific processes that allowed for ongoing species diversification. One factor was significant variation among clades in diversification rates. For example, the nine principal clades of hummingbirds exhibit ∼15-fold variation in net diversification rates, with evidence for accelerated speciation of a clade that includes the Bee, Emerald, and Mountain Gem groups of hummingbirds. A second factor was colonization of key geographic regions, which opened up new ecological niches. For example, some clades diversified in the context of the uplift of the Andes Mountains, whereas others were affected by the formation of the Panamanian land bridge. Finally, although species accumulation is slowing in all groups of hummingbirds, several major clades maintain rapid rates of diversification on par with classical examples of rapid adaptive radiation.

Aerodynamic forces of revolving hummingbird wings and wing models

A central challenge to the study of animal aerodynamics has been the measurement of forces generated by flapping wings. Relative to wings of other birds, hummingbird wings are of particular interest in that the smaller species operate in more viscous regimes (5000 < Re < 10 000) for which substantial drag and reduced lift:drag coefficients might be expected. Lift and drag forces were measured on mounted hummingbird wings and wing models spinning in continuous tipwise revolution about the wing base. Lift coefficients tended to increase as wing models became more realistic (i.e. with sharpened leading edges and with substantial camber). Lift:drag ratios of real wings were substantially higher than those of wing models, suggesting morphological contributions of feathers to lift enhancement and drag reduction. At Re= 5000, high values of the lift:drag ratio (8–16) at low angles of attack suggest that wings of hummingbirds are exceptionally good at producing lift.

Kinematics of hovering hummingbird flight along simulated and natural elevational gradients

SUMMARY Hovering flight is one of the most energetically demanding forms of animal locomotion. Despite the cost, hummingbirds regularly hover at high elevations, where flight is doubly challenging because of reduced air density and oxygen availability. We performed three laboratory experiments to examine how air density and oxygen partial pressure influence wingbeat kinematics. In the first study, we experimentally lowered air density but maintained constant oxygen partial pressure. Under these hypodense but normoxic conditions, hummingbirds increased stroke amplitude substantially and increased wingbeat frequency slightly. In the second experiment, we maintained constant air density but decreased oxygen partial pressure. Under these normodense but hypoxic conditions, hummingbirds did not alter stroke amplitude but instead reduced wingbeat frequency until they could no longer generate enough vertical force to offset body weight. In a final combined experiment, we decreased air density but increased oxygen availability, and found that the wingbeat kinematics were unaffected by supplemental oxygen. We also studied hovering and maximally loaded flight performance for 43 hummingbird species distributed along a natural elevational gradient in Peru. During free hovering flight, hummingbirds showed increased stroke amplitude interspecifically at higher elevations, mirroring the intra-individual responses in our first laboratory experiment. During loaded flight, hummingbirds increased both wingbeat frequency and wing stroke amplitude by 19% relative to free-flight values at any given elevation. We conclude that modulation of wing stroke amplitude is a major compensatory mechanism for flight in hypodense or hypobaric environments. By contrast, increases in wingbeat frequency impose substantial metabolic demands, are only elicited transiently and anaerobically, and cannot be used to generate additional sustained lift at high elevations.

Novel interactions of non-pollinating ants with pollinators and fruit consumers in a tropical forest

Abstract The tropical ants Ectatomma ruidum and E. tuberculatum (Formicidae) regularly patrol leaves, flowers, and fruits of the understory shrub, Psychotria limonensis (Rubiaceae), on Barro Colorado Island, Panama. Ant and pollinator exclusion experiments elucidated both positive and negative effects of ant attendance on plant reproductive success, including pollination, fruit set, fruit loss, and fruit removal. Ants did not pollinate flowers but did contribute to higher pollination success, probably by increasing the relocation frequency of winged pollinators and thus the rate of flower visitation. Ants also prevented fruit loss to herbivorous insects which were common during the early stages of fruit development. Thus, ant attendance strongly improved both pollination and fruit set whereby plants with ants set more fruit per flower and also lost fewer fruits during fruit maturation. In contrast, ants had a negative effect on the removal of ripe fruits by avian frugivores. Thus, ant attendance has a non-trivial influence on plant reproduction, this interaction being beneficial at some stages of the plant reproductive cycle and carrying costs at another stage. A tight ecological or co-evolved relationship between these Ectatomma spp. and P. limonensis is unlikely given that ant attendance of plants is detrimental to fruit removal.

The physiology and biomechanics of avian flight at high altitude

Many birds fly at high altitude, either during long-distance flights or by virtue of residence in high-elevation habitats. Among the many environmental features that vary systematically with altitude, five have significant consequences for avian flight performance: ambient wind speeds, air temperature, humidity, oxygen availability, and air density. During migratory flights, birds select flight altitudes that minimize energy expenditure via selection of advantageous tail- and cross-winds. Oxygen partial pressure decreases substantially to as little as 26% of sea-level values for the highest altitudes at which birds migrate, whereas many taxa reside above 3000 meters in hypoxic air. Birds exhibit numerous adaptations in pulmonary, cardiovascular, and muscular systems to alleviate such hypoxia. The systematic decrease in air density with altitude can lead to a benefit for forward flight through reduced drag but imposes an increased aerodynamic demand for hovering by degrading lift production and simultaneously elevating the induced power requirements of flight. This effect has been well-studied in the hovering flight of hummingbirds, which occur throughout high-elevation habitats in the western hemisphere. Phylogenetically controlled studies have shown that hummingbirds compensate morphologically for such hypodense air through relative increases in wing size, and kinematically via increased stroke amplitude during the wingbeat. Such compensatory mechanisms result in fairly constant power requirements for hovering at different elevations, but decrease the margin of excess power available for other flight behaviors.

Take-off mechanics in hummingbirds (Trochilidae).

SUMMARY Initiating flight is challenging, and considerable effort has focused on understanding the energetics and aerodynamics of take-off for both machines and animals. For animal flight, the available evidence suggests that birds maximize their initial flight velocity using leg thrust rather than wing flapping. The smallest birds, hummingbirds (Order Apodiformes), are unique in their ability to perform sustained hovering but have proportionally small hindlimbs that could hinder generation of high leg thrust. Understanding the take-off flight of hummingbirds can provide novel insight into the take-off mechanics that will be required for micro-air vehicles. During take-off by hummingbirds, we measured hindlimb forces on a perch mounted with strain gauges and filmed wingbeat kinematics with high-speed video. Whereas other birds obtain 80–90% of their initial flight velocity using leg thrust, the leg contribution in hummingbirds was 59% during autonomous take-off. Unlike other species, hummingbirds beat their wings several times as they thrust using their hindlimbs. In a phylogenetic context, our results show that reduced body and hindlimb size in hummingbirds limits their peak acceleration during leg thrust and, ultimately, their take-off velocity. Previously, the influence of motivational state on take-off flight performance has not been investigated for any one organism. We studied the full range of motivational states by testing performance as the birds took off: (1) to initiate flight autonomously, (2) to escape a startling stimulus or (3) to aggressively chase a conspecific away from a feeder. Motivation affected performance. Escape and aggressive take-off featured decreased hindlimb contribution (46% and 47%, respectively) and increased flight velocity. When escaping, hummingbirds foreshortened their body movement prior to onset of leg thrust and began beating their wings earlier and at higher frequency. Thus, hummingbirds are capable of modulating their leg and wingbeat kinetics to increase take-off velocity.

A higher-level taxonomy for hummingbirds

In the context of a recently published phylogenetic estimate for 151 hummingbird species, we provide an expanded informal taxonomy, as well as a formal phylogenetic taxonomy for Trochilidae that follows the precepts of the PhyloCode, but remains consistent with the hierarchical nomenclature of the Linnaean system. We compare the recently published phylogenetic hypothesis with those of prior higher-level and more taxonomically circumscribed phylogenetic studies. We recommend the recognition of nine new clade names under the PhyloCode, eight of which are consistent with tribes and one with a subfamily under the Linnaean system.

Flight Performance and Competitive Displacement of Hummingbirds across Elevational Gradients

Hummingbirds, with their impressive flight ability and competitive aerial contests, make ideal candidates for applying a mechanistic approach to studying community structure. Because flight costs are influenced by abiotic factors that change systematically with altitude, elevational gradients provide natural experiments for hummingbird flight ecology. Prior attempts relied on wing disc loading (WDL) as a morphological surrogate for flight performance, but recent analyses indicate this variable does not influence either territorial behavior or competitive ability. Aerodynamic power, by contrast, can be derived from direct measurements of performance and, like WDL, declines across elevations. Here, I demonstrate for a diverse community of Andean hummingbirds that burst aerodynamic power is associated with territorial behavior. Along a second elevational gradient in Colorado, I tested for correlated changes in aerodynamic power and competitive ability in two territorial hummingbirds. This behavioral analysis revealed that short‐winged Selasphorus rufus males are dominant over long‐winged Selasphorus platycercus males at low elevations but that the roles are reversed at higher elevations. Several lines of evidence support the hypothesis that the burst rather than sustained aerodynamic performance mediates competitive ability at high elevation. A minimum value for burst power may be required for successful competition, but other maneuverability features gain importance when all competitors have sufficient muscle power, as occurs at low elevations.

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.