Department of Biology, MSC02-3030, 1 University of New Mexico, Albuquerque 87131-0001

Mystery of the lowland Giant Hummingbirds (Patagona gigas) of central Chile

Blake-Nuttall Fund Report – 2016 Grant

Jessie Williamson, Ph.D. Student Department of Biology and Museum of Southwestern Biology

University of New Mexico, Albuquerque Project Overview

Andean hummingbirds have narrow elevational distributions (500-1,500 m in amplitude) as a result of their specialized hemoglobin, which is genetically optimized to bind oxygen at low atmospheric pressures (Graham et al. 2009; Projecto-Garcia et al. 2013). As such, few elevational generalist hummingbird species exist. The Giant Hummingbird (Patagona gigas) – the largest hummingbird in the world – defies this tendency. It is distributed from sea level to ~4,500 m in the Andes (Fernández et al. 2011; Fig. 1), but it only occurs at sea level where the southern subspecies, P. g. gigas, breeds in central Chile (Estades et al. 2008). Furthermore, P. g. gigas is migratory and it does not winter at sea level. This raises the question: At what latitude and altitude do lowland Giant Hummingbirds winter? Objective

I set out to describe migratory connections between Giant Hummingbird breeding and wintering populations using ultra-light geolocators. Value to Ornithology

This study will identify where lowland Giant Hummingbirds winter (latitude and altitude) for the first time. Additionally, this research will begin to characterize the diversity of migratory and life history strategies within this ancient, monotypic lineage, which are unresolved in the literature. In doing so, I hope to provide clues about how differences in migratory behavior, combined with cryptic genetic adaptation to different seasonal elevational distributions, might lead to genetic isolation and speciation. Results will stimulate ecological questions about migration timing

Fig. 1. Distribution of the Giant Hummingbird.

P. g. peruvianaYear-round

P. g. gigasSummer

(P!b;ind / W" 0:03, CI: −0.212, 0.147) species. Reserve power, the

difference in the allometries of maximum and hoveringpower, therefore declines in large individuals, but not largespecies. Overall, there is a decline in the production of burstvertical force relative to expended power in larger individuals, andalthough larger individuals proportionately expend the samemaximum power during burst performance, they produce lessrelative force.

DiscussionIn principle, hummingbirds could adopt any one of multiplestrategies to support changes in body weight during flight (Eq.(2)), expressed as movement to lower elevations with higher airdensity (ρ), increase in wing area (S), increase in wing velocity(U ) or adaptation of wing morphology and kinematics (CV ). Thepotential contribution of each strategy differs; for instance, anorder of magnitude in air density to support an order of mag-nitude in body weight is not possible. Each strategy may alsoentail tradeoffs, such as sacrificing potential habitats (air densityallometry) or reconfiguring the wing (force coefficient allometry).We find that the allometry of force production among and withinhummingbird species is solely a function of changes in the allo-metries of wing area and wing velocity. Among species, increasingweight support is provided exclusively by increasing wing areaand maintaining constant wing velocity, whereas within species,weight support is provided both by increasing wing area andvelocity. The advantage of maintaining constant wing velocity isapparent from Eq. (4), which shows that when bU ¼ 0, expendedpower is only a function of the load factor, or reciprocally, themaximum load factor is only a function of the maximum avail-able muscle power. The dependence on positive wing velocityallometry within species thus results in degrading burst forcecapabilities and escalating cost of flight in larger individuals. Theextreme wing area allometry among hummingbird speciesappears to be an evolutionary strategy to mitigate the

performance and energetic disadvantages that would arise if thebody plan of large species was extrapolated from intraspecificpatterns.

The emergence of this extreme allometry among humming-birds is likely due to pressures of their energetically demandinghovering flight and territoriality, frequently engaging conspecificsand confamilials in aerial bouts9, 21. Selection can therefore beexpected to favour constant or minimally-increasing routineflight costs and burst aerial performance, which is supported bythe weight independence of specific daily energy expenditure(DEE*) among hummingbird species24, DEE! / W" 0:03. Asobserved, the force allometric pattern within species cannot bescaled up across the size range of hummingbirds without incur-ring severe penalties to both flight costs and burst forces. Main-taining burst performance margins could entail adaptation of theflight musculature, as may occur in other flying animals25, 26 butthe invariance of maximum available power among and withinspecies suggests that hummingbirds’ specialised muscles4, 24 havereached the physiological limits of performance. Hummingbirdsmust therefore reduce energetic demand rather than supply, andincreasing relative wing area is the simplest solution that bothminimises flight costs and maximises performance.

Force allometry is a flexible method for examining the func-tional context of allometric variation in wing area. The approachcan be applied among and within species to gain insight into theenergetic and performance consequences of divergent forcegeneration strategies. Separating the problem into its constituentcomponents (Eqs. (2) and (4)) and then comparing the resultingexponents provides a framework for evaluating both the func-tional and statistical relevance of hypothesised allometries. Thislinear separation allows disparate data sets to be merged toprovide consistent inference. Perhaps the most important insightfrom our framework is a shift in emphasis from single exponentsintended to explain variation across all clades, to a nuanced viewof possibly clade-specific balancing of weight-supporting strate-gies, including the possible contributions of the force

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Body weight, W (g m s–2)

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Body weight, W (g m s–2)20 40 80 160 320

a b

c d

Fig. 3 Allometric divergence among and within species. We contrast the slopes of wing area (a), wing velocity (b), load factor (c) and induced powerrequirements (d). The slope of each variable on body weight among species is shown in black, and each was calculated allowing for phylogenetic non-independence and measurement error. Individual records are shown along with the mean within-species slope fit through the respective empirical speciesmeans. Symbols denote collector. Individual observations and within-species slopes are coloured and shaded by species within clade, according to thecartoon phylogeny at right (colours as in Fig. 1). Sample sizes are provided in Supplementary Table 1

NATURE COMMUNICATIONS | DOI: 10.1038/s41467-017-01223-x ARTICLE

NATURE COMMUNICATIONS |8: �1047� |DOI: 10.1038/s41467-017-01223-x |www.nature.com/naturecommunications 5

Department of Biology, MSC02-3030, 1 University of New Mexico, Albuquerque 87131-0001

and location of stopover sites, as well as evolutionary questions about gene flow among Patagona populations along the extent of their Andean distribution. Project Advances

To date, we have deployed 55 light-level geolotors on lowland-breeding Giant Hummingbirds in central Chile (Fig. 2). For each individual captured, we take morphological measurements, and samples of blood and feathers for use in genetic and physiology research. Additionally, in collaboration with the Universidad Pontificia Católica de Chile, we have trained two students (one undergraduate Chilean student, and one post-baccalaureate American student) in ornithological field techniques. We maintain strong positive relationships with our local partners and government offices (Servicio Agrícola y Ganadero; SAG) in Valparaíso Region, and remain optimistic about future permitting, collaboration, and fieldwork. Future Plans

I will return to Chile in Fall 2018 to recapture individuals and recover geolocators. I am in the process of analyzing DNA from exported blood and feather samples (manuscript in preparation) that will form the basis of one of my dissertation chapters. Acknowledgements

We thank Alfredo Zelada, Lisa N. Barrow, Andrew B. Johnson, Margarita Espinoza, Javier Reinoso, Tim Farkas, Thomas Valqui, Benito Rosende, Paxton Cruz, Henry Streby, Gunnar Kramer, James Fox, Dmitri Skandalis and Douglas Altshuler (hummingbird illustrations), Centro de Ornitología y Biodiversidad (CORBIDI), UNM Biology MBF (George Rosenberg). This research was supported by the Nuttall Ornithological Club (Blake-Nuttall Fund), National Science Foundation (NSF DEB-1146491), American Museum of Natural History (Frank M. Chapman Memorial Fund), and the UNM Graduate & Professional Student Association and Biology Graduate Student Association Grants.

Fig. 2. Giant Hummingbird with geolocator backpack.

Department of Biology, MSC02-3030, 1 University of New Mexico, Albuquerque 87131-0001

Works Cited Estades CF, Vukasovic MA, Tomasevic JA, Desert N (2008) Giant Hummingbirds (Patagona gigas)

Ingest Calcium-rich Minerals. Wilson J Ornithol 120:651–653. doi: 10.1676/07-054.1 Fernández MJ, Dudley R, Bozinovic F (2011) Comparative energetics of the giant hummingbird

(Patagona gigas). Physiol Biochem Zool 84:333–40. doi: 10.1086/660084 Graham CH, Parra JL, Rahbek C, McGuire JA (2009) Phylogenetic structure in tropical

hummingbird communities. Proc Natl Acad Sci 106:19673–19678. doi: 10.1073/pnas.0912879107

Projecto-Garcia J, Natarajan C, Moriyama H, et al (2013) Repeated elevational transitions in hemoglobin function during the evolution of Andean hummingbirds. Proc Natl Acad Sci 110:1–6. doi: 10.1073/pnas.1315456110