Torpor is an energy-saving strategy used by warm-blooded animals, including birds and small mammals. Similar to hibernation, although shorter in duration, torpor is a state of minimal activity, low body temperatures and reduced metabolism that helps animals conserve energy in unfavorable conditions. Some animals use torpor to survive times when food is not readily available. Hummingbirds, for example, eat nectar all day long to meet their high energy needs, but must build fat reserves to see them through their overnight fast. If they go to sleep with too little fat, they can descend into torpor to stretch out that limited energy supply and survive until morning.

Many hummingbirds migrate to areas with warmer weather, where food remains available, for the winter months. The ruby-throated hummingbird (Archilochus colubris), for example, travels over 5,000 kilometers in its fall migration. Like most long-distance migrants, ruby-throated hummingbirds increase their fat stores before departing, using these stores to fuel their journey. It is thought that this bird may use torpor as a way to accelerate fat build up before its annual migration. However, it remained unclear whether hummingbirds switched from using torpor strictly in energy emergencies, to using it as strategy to prepare for migration.

To shed light on this question, Eberts, Guglielmo and Welch investigated when, why and how hummingbirds save energy using torpor during the summer, and whether there are seasonal shifts in their use of torpor coinciding with migration. Eberts, Guglielmo and Welch hypothesized that a bird would initiate daily torpor if its energy stores fall below a critical level during the night, but that they may abandon this threshold (triggering torpor at higher fat levels) in late summer as a way to spare energy and gain fat before their annual migration.

To test their hypotheses, Eberts, Guglielmo and Welch tracked body composition, food intake, energy expenditure and torpor use throughout summer in a group of captive ruby-throated hummingbirds. In the middle of the summer, the birds entered torpor and remained torpid for longer when they went to sleep with low fat stores. In late summer, however, the same birds were more likely to enter torpor at consistent times and when they had higher fat stores. Eberts, Guglielmo and Welch also observed that the more time birds spent in torpor, the more fat they gained. This suggests that in late summer, hummingbirds switch from using torpor as a survival strategy to using it to maximize energy savings before migration.

These results clearly define the physiological rules governing torpor use in hummingbirds. They also support the long-standing assumption that torpor helps migratory species save energy and accumulate fat stores before long-haul flights.

Facultative hypothermia is an energy conservation strategy that allows many mammalian and some avian species to survive periods of resource unavailability or to optimize their energy budgets in certain environments or life stages (McKechnie and Lovegrove, 2002; Ruf and Geiser, 2015). During facultative hypothermia, metabolic rates and body temperatures are reduced to varying extents across species and environmental conditions (Ruf and Geiser, 2015). As some of the smallest avian species, hummingbirds (Trochilidae) are known for their ability to use daily torpor, a deep, short-term form of facultative hypothermia, to cope with energetic challenges they face daily and throughout their annual cycle (Carpenter, 1974; Hainsworth et al., 1977).

Studies that have investigated the use of torpor in hummingbirds in relation to food availability and body mass suggest that torpor initiation is controlled by an endogenous mechanism sensitive to an energy-store threshold (Hainsworth et al., 1977; Hiebert, 1992; Powers et al., 2003). This model predicts that a bird will initiate torpor if its energy stores reach critically low levels with enough time remaining in the night to achieve net energy savings. Hummingbirds typically rewarm 1–2 hr before sunrise, so they rarely enter torpor after approximately 75% of the night has elapsed; even if critically low energy levels are reached late in the night, birds may avoid entering torpor at this point if the energetic benefits are outweighed by the potential costs (e.g. predation, moult delay) (Bouma et al., 2010; Carr and Lima, 2013; Hainsworth et al., 1977; Hiebert, 1992; Hiebert, 1990). Previous studies also suggest that the function of torpor shifts seasonally, from an energy emergency survival mechanism to an energy-storage maximization strategy during migration (Carpenter and Hixon, 1988; Hiebert, 1993). However, this threshold has not been repeatedly and accurately measured in individual birds spanning life history stages, and the relationship between torpor use and the components of body composition (fat and lean mass) remains unclear.

We explored torpor use in ruby-throated hummingbirds (Archilochus colubris), which breed in eastern North America in the early and mid-summer, and migrate to wintering grounds in Mexico and Central America in the late summer. In the breeding period, birds maintain relatively lean body compositions to optimize aerial agility, important for successful courtship displays and competitive interactions that allow them to maintain secure access to food resources (Altshuler et al., 2010; Hou and Welch, 2016). But like most long-distance migrants, ruby-throated hummingbirds substantially increase their body mass prior to migratory departure to fuel their journey (Hou and Welch, 2016).

We repeatedly and non-invasively quantified the relationship between torpor and endogenous energy stores (fat) in ruby-throated hummingbirds to investigate the underlying rules of torpor use during the breeding and migration periods. We predicted that in the breeding period, when birds reached a low energy-store threshold before 75% of the night had elapsed, they would enter torpor to avoid complete energy depletion, and that birds that remained normothermic until this point would not enter torpor if it would not achieve net energy savings. We also predicted that this threshold would be abandoned in the late summer to facilitate premigratory fattening. Furthermore, we predicted that in the breeding period, torpor use would be primarily driven by evening fat content and the rate at which those energy reserves were used, and that in the migration period, the amount of torpor used would be driven primarily by night length, allowing the birds to spare a maximum amount of fat stores, irrespective of longer late-summer nights.

We measured the torpor use and body composition of captive adult (and one juvenile) male ruby-throated hummingbirds (n = 16; capture mass: 2.5–3.2 g) that experienced semi-natural photoperiods, on 158 focal bird-nights throughout the summer. On all days and nights, the birds experienced air temperatures of approximately 20°C (19.7°C ± 0.0°C) to control for the potential effect of air temperature as a proximate cue for torpor use. We used respirometry to calculate rates of energy expenditure and the rate of oxidation of stored fat, and quantitative magnetic resonance (QMR) to measure body composition (Guglielmo et al., 2011; Lighton, 2008). We identified the start of torpor entry and arousal by evaluating the slope of each smoothed ${\displaystyle {\acute{\mathrm{V}}}_{{\mathrm{O}}_2}}$ trace, and we calculated the fat content at the time of torpor entry as the amount of evening fat (g) minus the estimated amount of fat expenditure prior to torpor entry, divided by the morning body mass.

We aimed to determine the rules governing the use of torpor and whether these differed throughout the summer. We evaluated changes in the relationships between evening body composition and torpor occurrence, torpor duration, time of torpor entry, fat content at torpor entry, and amount of energy expended before torpor entry, within and among periods of consistent change in body mass. We also evaluated the influence of night length on these variables. To specifically investigate the role of torpor in driving premigratory increases in body mass, we evaluated the effects of mean torpor duration and mean daily food consumption on the amount of mass gained and duration of the fattening period.

Ruby-throated hummingbirds exhibit substantial shifts in body composition and use of torpor between the summer breeding period and the migration period as a means to achieve premigratory fat gains (Table 1). In the summer, torpor is sensitive to critically low endogenous energy reserves; however, when the birds fatten for migration, this rule is abandoned, and the birds enter torpor with high levels of fat. While it does not appear that torpor initiation in the migration period is simply sensitive to a high energy threshold, the abandonment of the emergency threshold indicates that the rules governing torpor use are dependent on life history stage, and that hummingbirds may employ torpor as part of various energy management strategies throughout the annual cycle.

In the summer breeding period, ruby-throated hummingbirds reserve torpor for times when they face critically low fat stores during the night. At air temperatures of 20°C, which free-living birds commonly experience, torpor initiation is primarily driven by instantaneous fat stores. On nights when they started with lower evening fat stores birds depleted energy stores to critically low levels earlier in the night, and thus remained torpid longer, irrespective of night length. These results support the hypotheses that torpor use is sensitive to a low, consistent threshold of fat during the breeding period, and that torpor is an energy emergency survival strategy mechanism that protects hummingbirds from depleting energy stores during the night or before they can reach their first meal in the morning (Hainsworth et al., 1977; Hiebert, 1992; Powers et al., 2003).

The birds obeyed the average threshold on the clear majority of focal nights (47 out of 55 nights). On eight nights, 6 of the 13 fattener birds either crossed the threshold and did not enter torpor, or entered torpor without ever crossing the threshold, but we argue it is not surprising that there were a few exceptions to the threshold rule. The threshold could occasionally be overridden to remain normothermic despite reaching critical energy levels if extended bouts of torpor on subsequent nights impede regenerative processes associated with normothermy and sleep, or increase risk of predation (Bouma et al., 2010; Carr and Lima, 2013; Hiebert, 1990). Similarly, we and other researchers have observed hummingbirds prematurely rewarming after inadvertent light or noise disturbances, which suggests that the threshold override and emergency arousal mechanisms could be related (A. Shankar, E. Eberts, personal observations). Although we did not observe any obvious signs of greater stress in some individuals than others, it is also possible that some birds (e.g. those that were more recently captured) were more sensitive to handling and confinement in the respirometry chamber and therefore initiated torpor despite not having depleted fat levels to the threshold level (Hiebert et al., 2000). Furthermore, although temperature, precipitation, and food availability were controlled in this study, these factors would likely affect free-living hummingbirds’ torpor use decisions by effecting the amount of fat the birds start each night with and the rate that they expend that fat (Hainsworth et al., 1977; McGuire et al., 2021). For example, the birds were fasted to ensure accurate body composition measurements, but if the birds were allowed to eat during the last 2 hr of the day, it is likely that they would have amassed larger evening fat stores and therefore would have entered torpor later in the night or not at all (Eberts et al., 2019). Additionally, the level of the energy-store threshold could be modulated in response to anticipated energy demand. For instance, free-living birds at our study site during the breeding period experienced minimum nighttime air temperatures between 10°C and 25°C (London International Airport, Ontario, Canada). At colder temperatures, normothermic hummingbirds would need to sustain a higher resting metabolic rate and may therefore anticipate an energy emergency earlier in the night (Hiebert, 1990). While these factors likely play a role in the complex decision-making that governs free-living hummingbird torpor use during the breeding season, our evidence strongly supports the existence of an ‘adipostat’ mechanism that initiates compensatory physiological changes depending on the instantaneous level of endogenous energy stores (Boyer and Barnes, 1999; Powers et al., 2003).

The patterns and role of torpor use drastically shifts as hummingbirds accumulate fat stores prior to migration. Contrary to the breeding period, torpor propensity and torpor duration were primarily driven by night length rather than evening fat content, and torpor entry, energy expenditure before torpor entry, and overnight fat loss did not vary with night length. Instead of initiating torpor to survive the night whenever they reach a critically low threshold, hummingbirds appear to enter torpor after a consistent amount of time, so that they expend a predictable amount of energy and achieve greater energy savings as they experience progressively longer nights in the late summer. This suggests that during the migration period, birds maximize their time in torpor, but must remain normothermic for a consistent period of time, perhaps accounting for the time it takes to process their final evening meal and their blood sugar declines to a level allowing for torpor initiation (Eberts et al., 2019). This normothermic period could also allow the birds to achieve sufficient sleep before entering torpor when the regenerative and immunological benefits of sleep are unlikely to occur (Bouma et al., 2010). Overall, the seasonal change in torpor use, from a survival strategy initiated by an ‘adipostat’ mechanism to a more routine use of torpor to maximize energy savings and build fat stores prior to migration, shows that torpor is a critical energy management strategy that allows migratory hummingbirds to balance fuel supply and demand during a particular season. Similar torpor use patterns have been well studied in mammals, though studies investigating avian endocrine mechanisms are needed to elucidate the proximate factors of torpor initiation across taxa.

The similarities between the life histories of North American hummingbirds and bats provide an important lens through which to interrogate the ultimate drivers of torpor use throughout the annual cycle (McGuire et al., 2012). Using torpor while roosting could allow both hummingbirds and bats animals to maintain high fuel stores when feeding opportunities are constrained by migratory priorities. Unlike most nocturnal migrant birds that can replenish fuel stores during the day, ruby-throated hummingbirds are diurnal migrants that do not forage at night. In an opposite but parallel manner, North American bats migrate at night when they would otherwise forage and do not forage during the day. In both of these types of animals, foraging, migrating, and sleeping can be mutually exclusive endeavors, but torpor can allow them to conserve energy and avoid making extended refueling stopovers (McGuire et al., 2014). While we did not study free-living birds while they migrated, the drastic shift in the relationship between hummingbird body composition and torpor use, and of the link between torpor duration and mass gains in the late summer compellingly support the ‘torpor-assisted migration’ hypothesis (Carpenter and Hixon, 1988; Hiebert, 1993; Hou and Welch, 2016; McGuire et al., 2012).

The magnitude and timing of fattening in our captive birds resembled those documented in some free-living ruby-throated hummingbirds (present study: 0.58 ± 0.05 g, 19.6% ± 1.6% over 10 ± 1 days; Hou and Welch, 2016: ~ 0.65 g, or 17% over 4 days). However, not all birds in this study showed such substantial body mass changes; there was continuous variation in magnitude and duration of fattening within the fattener birds, and three non-fattener birds maintained relatively lean body compositions throughout the study period. The ranges in magnitude and timing of fattening are not surprising because hummingbirds are asocial birds that do not migrate in flocks, and we would not expect them to have finely synchronized timing of migratory preparation, especially in the absence of natural ecological cues. Furthermore, our captive birds varied in wing feather wear and activity level, suggesting that the amount of fat they could deposit was limited by how much extra weight they could carry, determined by wing morphology, pectoral mass, and power output (Chai, 1997; Dakin et al., 2020). These interindividual differences could also reflect disparate energy management strategies observed among free-living individuals. For example, a study examining migratory paths of juveniles suggested that adults take a more direct route than individuals (Zenzal and Moore, 2016). These disparate migratory strategies could be driven by differences in competitive abilities or experience from previous migratory journeys (Carpenter et al., 1993b; Carpenter et al., 1993a; Hou and Welch, 2016; Kodric-Brown and Brown, 1978; Welch et al., 2008). This hypothesis is supported by the fact that one of the three non-fattener birds was the only juvenile in our study, and ongoing work is investigating potential age/sex class differences in an ecologically relevant context.

This is the first study to non-terminally and repeatedly sample the body composition of individuals to accurately define a consistent rule governing torpor use in hummingbirds: birds will enter torpor when their fat stores reach a consistently low fat threshold (5%), during life history stages where a relatively lean body composition is advantageous. This rule may explain the typically low degree of torpor use in dominant individuals and large species, and the more frequent use of torpor in subordinate individuals and smaller species (Powers et al., 2003). Moreover, our study is consistent with the long standing, but heretofore unproven, assumptions of the key role of torpor in premigratory fattening and in refueling at migratory stopover sites. Hummingbirds dramatically shift their rules for torpor use and enter torpor at high fat levels during times when it is advantageous to accumulate excess energy stores. These findings demonstrate the versatility of torpor as an energy management mechanism throughout the annual cycle and have important implications for understanding the physiological basis of torpor initiation.

All data is available in the main text or the supplementary materials. Analyses reported in this article can be reproduced using the data and code provided by Eberts et al., 2021.

1. 1. Eberts E
   2. Guglielmo C
   3. Welch Jr K

   (2021) Dryad Digital Repository

   Data from: Reversal of the adipostat control of torpor during migration in hummingbirds.

   https://doi.org/10.5061/dryad.p8cz8w9qg

1. 1. Altshuler DL
   2. Dudley R
   3. Heredia SM
   4. McGuire JA

   (2010) Allometry of hummingbird lifting performance

   The Journal of Experimental Biology 213:725–734.

   https://doi.org/10.1242/jeb.037002

   • PubMed
   • Google Scholar
2. 1. Bakdash JZ
   2. Marusich LR

   (2017) Repeated Measures Correlation

   Frontiers in Psychology 8:00456.

   https://doi.org/10.3389/fpsyg.2017.00456

   • Google Scholar
3. 1. Bates D
   2. Mächler M
   3. Bolker B
   4. Walker S

   (2015) Fitting Linear Mixed-Effects Models Using lme4

   Journal of Statistical Software 67:i01.

   https://doi.org/10.18637/jss.v067.i01

   • Google Scholar
4. 1. Bouma HR
   2. Carey HV
   3. Kroese FGM

   (2010) Hibernation: the immune system at rest?

   Journal of Leukocyte Biology 88:619–624.

   https://doi.org/10.1189/jlb.0310174

   • PubMed
   • Google Scholar
5. 1. Boyer BB
   2. Barnes BM

   (1999) Molecular and Metabolic Aspects of Mammalian Hibernation

   BioScience 49:713–724.

   https://doi.org/10.2307/1313595

   • Google Scholar
6. 1. Carpenter FL

   (1974) Torpor in an andean hummingbird: its ecological significance

   Science 183:545–547.

   https://doi.org/10.1126/science.183.4124.545

   • PubMed
   • Google Scholar
7. 1. Carpenter FL
   2. Hixon MA

   (1988) A New Function for Torpor: Fat Conservation in a Wild Migrant Hummingbird

   The Condor 90:373–378.

   https://doi.org/10.2307/1368565

   • Google Scholar
8. 1. Carpenter FL
   2. Hixon MA
   3. Russell RW
   4. Paton DC
   5. Temeles EJ

   (1993a) Interference asymmetries among age-sex classes of rufous hummingbirds during migratory stopovers

   Behavioral Ecology and Sociobiology 33:297–304.

   https://doi.org/10.1007/BF00172927

   • Google Scholar
9. 1. Carpenter FL
   2. Hixon MA
   3. Temeles EJ
   4. Russell RW
   5. Paton DC

   (1993b) Exploitative compensation by subordinate age-sex classes of migrant rufous hummingbirds

   Behavioral Ecology and Sociobiology 33:305–312.

   https://doi.org/10.1007/BF00172928

   • Google Scholar
10. 1. Carr JM
    2. Lima SL

    (2013) Nocturnal hypothermia impairs flight ability in birds: a cost of being cool

    Proceedings of the Royal Society B 280:20131846.

    https://doi.org/10.1098/rspb.2013.1846

    • Google Scholar
11. 1. Chai P

    (1997)

    Hummingbird hovering energetics during moult of primary flight feathers

    The Journal of Experimental Biology 200:1527–1536.

    • PubMed
    • Google Scholar
12. 1. Dakin R
    2. Segre PS
    3. Altshuler DL

    (2020) Individual variation and the biomechanics of maneuvering flight in hummingbirds

    The Journal of Experimental Biology 223:jeb161828.

    https://doi.org/10.1242/jeb.161828

    • PubMed
    • Google Scholar
13. 1. Eberts E
    2. Dick M
    3. Welch K

    (2019) Metabolic Fates of Evening Crop-Stored Sugar in Ruby-Throated Hummingbirds (Archilochus colubris)

    Diversity 11:9.

    https://doi.org/10.3390/d11010009

    • Google Scholar
14. 1. Guglielmo CG
    2. McGuire LP
    3. Gerson AR
    4. Seewagen CL

    (2011) Simple, rapid, and non-invasive measurement of fat, lean, and total water masses of live birds using quantitative magnetic resonance

    Journal of Ornithology 152:75.

    https://doi.org/10.1007/s10336-011-0724-z

    • Google Scholar
15. 1. Hainsworth FR
    2. Collins BG
    3. Wolf LL

    (1977) The Function of Torpor in Hummingbirds

    Physiological Zoology 50:215–222.

    https://doi.org/10.1086/physzool.50.3.30155724

    • Google Scholar
16. 1. Hiebert SM

    (1990) Energy Costs and Temporal Organization of Torpor in the Rufous Hummingbird (Selasphorus rufus)

    Physiological Zoology 63:1082–1097.

    https://doi.org/10.1086/physzool.63.6.30152634

    • Google Scholar
17. 1. Hiebert SM

    (1992) Time-dependent thresholds for torpor initiation in the rufous hummingbird (Selasphorus rufus)

    Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 162:249–255.

    https://doi.org/10.1007/BF00357531

    • PubMed
    • Google Scholar
18. 1. Hiebert SM

    (1993) Seasonal Changes in Body Mass and Use of Torpor in a Migratory Hummingbird

    The Auk 110:787–797.

    https://doi.org/10.2307/4088634

    • Google Scholar
19. 1. Hiebert SM
    2. Salvante KG
    3. Ramenofsky M
    4. Wingfield JC

    (2000) Corticosterone and nocturnal torpor in the rufous hummingbird (Selasphorus rufus)

    General and Comparative Endocrinology 120:220–234.

    https://doi.org/10.1006/gcen.2000.7555

    • PubMed
    • Google Scholar
20. 1. Hou L
    2. Welch KC

    (2016) Premigratory ruby-throated hummingbirds, Archilochus colubris, exhibit multiple strategies for fuelling migration

    Animal Behaviour 121:87–99.

    https://doi.org/10.1016/j.anbehav.2016.08.019

    • Google Scholar
21. 1. Kodric-Brown A
    2. Brown JH

    (1978) Influence of Economics, Interspecific Competition, and Sexual Dimorphism on Territoriality of Migrant Rufous Hummingbirds

    Ecology 59:285–296.

    https://doi.org/10.2307/1936374

    • Google Scholar
22. Book

    1. Lighton JRB

    (2008) Measuring Metabolic Rates: A Manual for Scientists

    Oxford University Press.

    https://doi.org/10.1093/acprof:oso/9780195310610.001.0001

    • Google Scholar
23. 1. McGuire L.P
    2. Guglielmo CG
    3. Mackenzie SA
    4. Taylor PD

    (2012) Migratory stopover in the long-distance migrant silver-haired bat, Lasionycteris noctivagans

    The Journal of Animal Ecology 81:377–385.

    https://doi.org/10.1111/j.1365-2656.2011.01912.x

    • PubMed
    • Google Scholar
24. 1. McGuire LP
    2. Jonasson KA
    3. Guglielmo CG
    4. Bartell PA

    (2014) Bats on a Budget: Torpor-Assisted Migration Saves Time and Energy

    PLOS ONE 9:e115724.

    https://doi.org/10.1371/journal.pone.0115724

    • Google Scholar
25. 1. McGuire L.P
    2. Johnson EM
    3. Frick WF
    4. Boyles JG

    (2021) Temperature alone is insufficient to understand hibernation energetics

    Journal of Experimental Biology 224:1–6.

    https://doi.org/10.1242/jeb.239772

    • Google Scholar
26. 1. McKechnie AE
    2. Lovegrove BG

    (2002) Avian Facultative Hypothermic Responses: A Review

    The Condor 104:705–724.

    https://doi.org/10.1093/condor/104.4.705

    • Google Scholar
27. 1. Powers DR
    2. Brown AR
    3. Van Hook JA

    (2003) Influence of normal daytime fat deposition on laboratory measurements of torpor use in territorial versus nonterritorial hummingbirds

    Physiological and Biochemical Zoology 76:389–397.

    https://doi.org/10.1086/374286

    • PubMed
    • Google Scholar
28. Software

    1. R Development Core Team

    (2020) R: A Language and Environment for Statistical Computing, version 2.6.2

    R Foundation for Statistical Computing, Vienna, Austria.

    https://www.R-project.org/
29. 1. Ruf T
    2. Geiser F

    (2015) Daily torpor and hibernation in birds and mammals

    Biological Reviews of the Cambridge Philosophical Society 90:891–926.

    https://doi.org/10.1111/brv.12137

    • PubMed
    • Google Scholar
30. 1. Shankar A
    2. Schroeder RJ
    3. Wethington SM
    4. Graham CH
    5. Powers DR

    (2020) Hummingbird torpor in context: duration, more than temperature, is the key to nighttime energy savings

    Journal of Avian Biology 51:1–14.

    https://doi.org/10.1111/jav.02305

    • Google Scholar
31. 1. Welch KC Jr
    2. Herrera M LG
    3. Suarez RK

    (2008) Dietary sugar as a direct fuel for flight in the nectarivorous bat Glossophaga soricina

    The Journal of Experimental Biology 211:310–316.

    https://doi.org/10.1242/jeb.012252

    • PubMed
    • Google Scholar
32. 1. Wolf BO
    2. Mckechnie AE
    3. Schmitt CJ
    4. Czenze ZJ
    5. Johnson AB
    6. Witt CC

    (2020) Extreme and variable torpor among high-elevation Andean hummingbird species

    Biology Letters 16:20200428.

    https://doi.org/10.1098/rsbl.2020.0428

    • Google Scholar
33. 1. Zenzal TJ
    2. Moore FR

    (2016) Stopover biology of Ruby-throated Hummingbirds (Archilochus colubris) during autumn migration

    The Auk 133:237–250.

    https://doi.org/10.1642/AUK-15-160.1

    • Google Scholar

Author details

1. Erich R Eberts

   1. Department of Biological Sciences, University of Toronto Scarborough, Toronto, Canada
   2. Department of Ecological and Evolutionary Biology, University of Toronto, Toronto, Canada

   Contribution

   Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Project administration, Software, Visualization, Writing – original draft, Writing – review and editing

   For correspondence

   erich.eberts@mail.utoronto.ca

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-4259-8752

2. Christopher G Guglielmo

   Department of Biology, Advanced Facility for Avian Research, University of Western Ontario, London, Canada

   Contribution

   Conceptualization, Formal analysis, Methodology, Resources, Supervision, Writing – review and editing

   Competing interests

   No competing interests declared

3. Kenneth C Welch

   1. Department of Biological Sciences, University of Toronto Scarborough, Toronto, Canada
   2. Department of Ecological and Evolutionary Biology, University of Toronto, Toronto, Canada

   Contribution

   Conceptualization, Formal analysis, Funding acquisition, Methodology, Resources, Supervision, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-3283-6510

• 1,990

  views

• 255

  downloads

• 11

  citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.