Resolution of a paradox: Hummingbird flight at high elevation does not come without a cost

Abstract

Flight at high elevation is energetically demanding because of parallel reductions in air density and oxygen availability. The hovering flight of hummingbirds is one of the most energetically expensive forms of animal locomotion, but hummingbirds are nonetheless abundant at high elevations throughout the Americas. Two mechanisms enhance aerodynamic performance in highelevation hummingbirds: increase in wing size and wing stroke amplitude during hovering. How do these changes in morphology, kinematics, and physical properties of air combine to influence the aerodynamic power requirements of flight across elevations? Here, we present data on the flight performance of 43 Andean hummingbird species as well as a 76-taxon multilocus molecular phylogeny that served as the historical framework for comparative analyses. Along a 4,000-m elevational transect, hummingbird body mass increased systematically, placing further aerodynamic demands on high-elevation taxa. However, we found that the minimum power requirements for hovering flight remain constant with respect to elevation because hummingbirds compensate sufficiently through increases in wing size and stroke amplitude. Thus, high-elevation hummingbirds are not limited in their capacity for hovering flight despite the challenges imposed by hypobaric environments. Other flight modes including vertical ascent and fast forward flight are more mechanically and energetically demanding, and we accordingly also tested for the maximum power available to hummingbirds by using a load-lifting assay. In contrast to hovering, excess power availability decreased substantially across elevations, thereby reducing the biomechanical potential for more complex flight such as competitive and escape maneuvers.animal flight ͉ aerodynamic power requirements ͉ hummingbird phylogeny H ummingbirds are the only vertebrates capable of sustained hovering, a highly strenuous form of locomotion requiring extraordinary levels of metabolic power input (1) and mechanical power output (2). Because oxygen availability and air density decrease at higher elevations, hovering flight in alpine habitats is particularly challenging. From an aerodynamic perspective, it is therefore surprising that hummingbirds are most diverse in the Andes and reach elevations as high as 5,000 m (3, 4).Body mass, wing size and shape, wingbeat frequency, and wing stroke amplitude are important morphological and biomechanical parameters underlying hovering flight performance (5), and are likely to be the targets of selection along an elevational gradient (6). Because mass-specific induced power requirements in hovering flight are proportional to the square root of wing loading (5), high-elevation hummingbirds would benefit aerodynamically by being smaller and by having larger wings relative to low-elevation taxa. Aerodynamic theory also predicts that the mass-specific induced power requirements of hovering are inversely proportional to the square root of stroke amplitude (5). Thus, increase in this kinematic parameter should yie...

Flight Performance and Competitive Displacement of Hummingbirds across Elevational Gradients

“…WDL decreased across elevations but did not differ between territorial and nonterritorial hummingbirds (table 3). Burst power output also decreased with increasing elevation, as was reported previously for the power margin (ratio of burst power output to the power output of sustained hovering) of a larger sample of Peruvian hummingbirds (Altshuler et al 2004c). Unlike WDL, burst power output was influenced by community role (table 3).…”

“…An analysis of the load-lifting performance of the Andean taxa has been published previously (Altshuler et al 2004c), and only a brief description of the protocol will be given below. Complete load-lifting data were available for 347 individual Peruvian hummingbirds from 43 taxa, but corresponding behavioral data were available for only a subset of these (see "Results").…”

“…Behavioral observations were made for 29 hummingbird taxa in Peru with sufficient data for classification into one Altshuler et al (2004bAltshuler et al ( , 2004c, with site-specific data presented here. Sample sizes (n) are for the total number of individuals of each taxon at each site for which aerodynamic power data were available.…”

“…The flight performance of Peruvian hummingbirds was measured using a load-lifting protocol to assess the maximum short-term performance, also known as burst capacity . A larger analysis of the biomechanical data has been published previously (Altshuler et al 2004c).…”

Energetics and longevity in birds

“…It was not possible to create tips for each species, therefore some tips represent genus. In addition, the phylogeny for the order Trochiliformes was difficult to find; therefore they were placed into hummingbird clades: Mangoes, Coquettes, Brilliants, Mountain Gems, Bees and Emeralds, with a separate tip for the giant hummingbird (Patagona gigas) (taxonomic position based on Altshuler et al 2004). …”