Acclimatization to winter conditions is an essential prerequisite for the survival of small birds in the northern temperate zone. Changes in photoperiod, ambient temperature and food availability trigger seasonal physiological and behavioral acclimatization in many passerines. Seasonal trends in metabolic parameters are well known in avian populations from temperate environments; however, the physiological and biochemical mechanisms underlying these trends are incompletely understood. In this study, we used an integrative approach to measure variation in the thermogenic properties of the male Silky Starling (Sturnus sericeus) at different levels or organization, from the whole organism to the biochemical. We measured body mass (Mb), basal metabolic rate (BMR), energy budget, the mass of selected internal organs, state 4 respiration and cytochrome c oxidase (COX) activity in the heart, liver and muscle.
Methods
Oxygen consumption was measured using an open-circuit respirometry system. The energy intake of the birds were then determined using an oxygen bomb calorimeter. Mitochondrial state 4 respiration and COX activity in heart, liver and pectoral muscle were measured with a Clark electrode.
Results
The results suggest that acclimatization to winter conditions caused significant change in each of the measured variables, specifically, increases in Mb, organ mass, BMR, energy intake and cellular enzyme activity. Furthermore, BMR was positively correlated with body mass, energy intake, the mass of selected internal organs, state 4 respiration in the heart, liver and muscle, and COX activity in the heart and muscle.
Conclusions
These results suggest that the male Silky Starlingos enhanced basal thermogenesis under winter conditions is achieved by making a suite of adjustments from the whole organism to the biochemical level, and provide further evidence to support the notion that small birds have high phenotypic plasticity with respect to seasonal changes.
Interactions between avian obligate brood parasites and
their hosts remain one of the most robust examples of
coevolutionary arms races (Davies, 2000;
Stoddard and Stevens, 2010; Kilner and Langmore, 2011). The best
studied and historically most prominent example of
such interactions is the evolved mimicry of host eggs
by parasites (Moksnes and Røskaft 1995; Cherry et al., 2007a; Moskát et al., 2008, 2010;
Spottiswoode and Stevens, 2010; Soler et al., 2012). Despite the extensive
similarities in the appearance of host and parasitic eggs
(Grim, 2005), many host species possess the ability
to discriminate between own and foreign eggs (Stoddard and Stevens, 2011). Much attention has recently
been given to the functional roles of light wavelengths
beyond the human perceptual range in avian egg discrimination, including the role of the shorter, ultraviolet
(UV) wavelengths (< 400 nm) (e.g. Honza et al., 2007), to which different species of birds within distantly related lineages are varyingly sensitive (e.g. Ödeen and
Håstad, 2003; Machovsky Capuska et al., 2011; Aidala
et al., 2012). For example, UV-reflectance is important
in recognizing and rejecting foreign eggs in the Blackcap (Sylvia atricapilla) (Honza and Polačiková, 2008)
and the Song Thrush (Turdus philomelos) (Honza et al., 2007). However, comparatively less emphasis has been
given to describing the visual sensitivities, UV or otherwise, of avian obligate brood parasites themselves.
Describing the visual sensitivities of specific bird species is vital, especially because the avian visual world
differs substantially from that of humans. For example, unlike trichromatic humans, who possess only three
classes of cone photoreceptor, birds possess five classes, four of which are directly responsible for color perception (Hunt et al., 2009). The short wavelength-sensitive
type 1 (SWS1) photoreceptor, which is responsible for
short-wavelength light detection, differs in its maximal
sensitivity depending on the amino acids present at
key 'spectral tuning' sites 86, 90, and 93 (following the
bovine Bos taurus rhodopsin numbering) (Wilkie et al., 2000; Yokoyama et al., 2000; Shi et al., 2001). Of these, amino acid residue 90 is particularly important for
mediating the degree of UV-sensitivity in avian species
(Wilkie et al., 2000; Hunt et al., 2009). Those species
possessing serine at site 90 (S90) are designated as having violet-sensitive (VS) pigments with a maximal sensitivity > 400 nm, and those possessing cysteine (C)90
are designated as having UV-sensitive (UVS) pigments
with a maximal sensitivity < 400 nm (Hart, 2001). Site
90 is also highly conserved, with S90 proposed to be
the ancestral state in all birds (Yokoyama and Shi, 2000;
Hunt et al., 2009), though recent analyses of basal paleognaths (which were not included in these earlier analyses) including extinct moa from New Zealand, predicted a uniform UVS SWS1 for all ratites and tinamou
allies (Aidala et al., 2012). Therefore, it is likely that C90
has (re-)evolved independently several times among
avian lineages (Hunt et al., 2009; Ödeen et al., 2010;
Machovsky Capuska et al., 2011; Ödeen et al., 2011, Aidala et al. 2012). Because microspectrophotometric
and genetic data are in accord with one another in avian
taxa for which both types of data are available (i.e. those
possessing S90 have VS SWS1 opsins and those possessing C90 have UVS SWS1 opsins), DNA sequencing of
the SWS1 opsin gene therefore permits accurate assessment of the degree of UV-sensitivity in any given avian
species (Ödeen and Håstad, 2003) before the need for
invasive and terminal physiological experimentation
to confirm the sequence-based predictions (Aidala and Hauber, 2010).
Much of the work on the functional role of UVreflectance and sensitivity in brood parasitic birds has
focused on explaining the lack of eggshell color-based
egg rejection to seemingly non-mimetic parasitic eggs.
Cherry and Bennett's (2001) UV-matching hypothesis
suggests that matching host/parasitic egg reflectance
along a UV-green opponency (which humans cannot
see) may explain the lack of rejection in acceptor host
species. Empirical support for this hypothesis, however, is equivocal. For example, blocking-the UV-reflectance
of Great-spotted Cuckoo (Clamator glandarius) eggs
does not affect rejection in Common Magpies (Pica
pica) (Avilés et al., 2006). However, the UVS/VS SWS1
sensitivity in this parasite-impacted host species has
not been described, although other Corvidae species
are predicted to be VS based on SWS1 DNA sequencing
(Ödeen and Håstad, 2003). More critically, no apparent
relationship between accepter/rejecter status and UVS/
VS SWS1 sensitivity appears to exist among hosts of the
North American generalist brood parasite, the Brownheaded Cowbird (Molothrus ater) and many of its hosts
(Underwood and Sealy, 2008; Aidala et al., 2012).
The degree of UV egg
color-matching/UV light sensitivity in New Zealand obligate brood parasite-host
systems is not yet described using reflectance spectrophotometric or avian perceptual
modeling data. The endemic Grey Warbler (Gerygone igata) is an ac-cepter
host of the local subspecies of the native Shin-ing Cuckoo (in Australia, called the Shining-bronze Cuckoo; Chalcites [Chrysococcyx] lucidus)
(McLean and Waas, 1987; also reviewed in Grim, 2006). In turn, the Whitehead (Mohoua
albicilla), Yellowhead (M. ochro-cephala), and Brown Creeper (M.
novaeseelandiae) are endemic hosts of the also endemic Long-tailed
Cuckoo (Urodynamis [Eudynamis] taitensis) (Payne, 2005). The Whitehead
and Yellowhead are both considered accept-er hosts (McLean and Waas, 1987;
Briskie, 2003), while the Brown Creeper ejects artificial Long-tailed Cuckoo
eggs at a rate of 67% (Briskie, 2003). DNA sequencing of the SWS1 photoreceptor
in the Grey Warbler and the Whitehead predicted a VS and a UVS SWS1 maximal
sensitivity, respectively (Aidala et al., 2012), whereas the predicted
sensitivities of their respective parasites are not well known.
Compared
to the large amount of effort spent char-acterizing the visual sensitivities of
host species, those of brood parasites themselves, especially to UV-wavelengths, have received considerably less attention. To
date, the SWS1 sensitivities have not been described in
any Cuculiformes species, although a study measuring
UV-reflectance in feather patches of 24 of 143 (17%)
total cuckoo species showed that 5 of the species (21%
of those measured) showed peaks in UV-reflectance
(Mullen and Pohland, 2008). As there are increasingly
more known inter-and intra-order variations in avian
UV-sensitivity (Ödeen and Håstad, 2003;
Machovsky Capuska et al., 2011; Aidala et al., 2012; Ödeen et al., 2012), and because visual systems among closely related
species may vary widely, and are likely to reflect speciesspecific sensory ecologies (Machovsky Capuska et al., 2012), reliance on species for which SWS1 sensitivity
data are available even within a lineage to approximate
the degree of UV-sensitivity may be inaccurate.
Characterization
of the UV-sensitivities of brood parasitic species is important for several
reasons. First, it will allow for stronger analysis of comparative per-ceptual
coevolution between hosts and parasites (An-derson et al., 2009). For example, recent egg color work using spectrophotometric measurements across the entire
avian visible range have provided new insights into the direction of
coevolutionary processes between hosts and parasites. Great Reed Warblers (Acrocephalus
arundinaceus) are more likely to reject mimetic Com-mon Cuckoo (Cuculus
canorus) eggs when this hosts?own eggs exhibit higher intraclutch
variation, a finding not in line with traditional predictions of
coevolution-ary theory, but validated by spectrophotometric mea-surements of
host eggs (Cherry et al., 2007a; see also Antonov et al., 2012). Similarly, Common Cuckoos may preferentially parasitize host nests with eggs more closely
resembling their own, also out of line with the theoretical assumption that
female cuckoos randomly choose local nests to parasitize (Cherry et al., 2007b). Second, describing the visual sensitivities of brood parasitic cuckoo
species will better inform studies ex-amining cuckoo-cuckoo competition
(Brooker et al., 1990) over host nesting sites using visual modeling analyses.
Third, it will allow for more accurate analysis of VS/UVS SWS1 opsin ancestral
states among avian species (Hunt et al., 2009; Aidala et al., 2012). Here, we
report the predicted maximal sensitivities of the SWS1 opsins in two New
Zealand native brood parasitic cuck-oos based on DNA sequencing of the SWS1 'pectral
tuning?region. In keeping with the general theoretical framework that host egg
rejection selects for egg color matching, and in turn, favors
UV-sensitivity in hosts, which in turn selects for UV-sensitivity in parasites, we expect the Shining Cuckoo that parasitizes the VS-pre-dicted Grey Warbler to
possess VS SWS1 opsins and the Long-tailed Cuckoo that parasitizes the
UVS-predicted Whitehead to possess UVS SWS1 opsins.
Methods
We collected ~100 μL blood samples that were stored
in Queen's lysis buffer from live Shining Cuckoos captured in mistnets during our field studies on avian hostparasite interactions (Anderson et al., 2009). We also
obtained tissue samples from frozen Long-tailed Cuckoos that died from migration-related window-collisions
and were stored in the Auckland Museum collection
(Gill and Hauber, 2012). Our collecting protocols were
approved by governmental and institutional animal research committees. Total genomic DNA was extracted
from tissue samples stored in ethanol using the DNeasy
Blood and Tissue Kit (Qiagen) according to manufacturer's instructions. DNA concentration (ng·μL–1) was
estimated using Nanodrop spectrophotometer.
Forward primers SU149a (Shining Cuckoo) or SU193
(Long-tailed Cuckoo) and reverse primer SU306b
(Ödeen and Håstad, 2003), modified to include M13-
tails, were used to sequence the SWS1 opsin gene. PCR
amplifications were carried out in 25 μL reaction volumes of 60 mmol·L–1 Tris-HCl ph 8.5, 15 mmol·L–1
(NH4)2SO4, 2.5 mmol·L–1 MgCl2, 0.3 mmol·L–1 of each
dNTP, 0.2 μmol·L–1 of each primer and 0.5 U of Platinum Taq polymerase (Invitrogen). Thermal cycling followed conditions outlined in Ödeen and Håstad (2003)
and was conducted in an ABI GeneAmp 9700 thermocycler.
An Exo/SAP treatment was used to purify PCR products: 5 μL PCR product was added to 0.2 μL of Exo I (GE
Healthcare), 0.1 μL Shrimp Alkaline Phosphatase (GE
Healthcare) and 1.7 μL UltraPure water (Invitrogen). We
incubated mixtures for 30 min at 37℃, then for 15 min
at 80℃ to ensure enzyme inactivation. A BigDye Terminator Cycle Sequencing kit v3.1 (Applied Biosystems)
was used to sequence samples in both directions with
M13 forward and reverse primers. Each sequencing reaction consisted of 1 μL BigDye Terminator Mix, 3.5 μL
5× sequencing buffer, 0.2 μmol·L–1 primer, 1 μL DMSO
and 2 μL PCR product. Agencourt CleanSeq (Beckman
Coulter) was used according to manufacturer's instructions to purify sequencing reactions and analyzed using an ABI 3100 automated sequencer. Chromas Pro (Technelysium Pty. Ltd.) was used to edit sequences following
which they were exported to BioEdit (Hall, 1999) for
alignment and translation.
Results
The two Shining Cuckoo samples generated a sequence
length of 119 base pairs (bp) each. The two Long-tailed
Cuckoo samples generated a sequence length of 74 bp
each. All sequences have been made available on GenBank (Accession numbers HM159121–HM159124).
We detected no intraspecific or intrafamilial variation
in either the gene or amino acid sequences, except for
the codons at residue 95; however, both of these code
for the amino acid phenylalanine (Table 1). We found
only two ambiguities in one Long-tailed Cuckoo sample, whereas the other Long-tailed Cuckoo possessed
the same codons and amino acid residues as the two
Shining Cuckoo samples (Table 1). After alignment, all
samples possessed S86, S90, and T93, which predict VS
for both of these cuckoo species' SWS1 opsin photoreceptors.
Table
1.
Predicted VS/UVS SWS1 opsin state of two New Zealand cuckoo species based on SWS1 amino acid sequences. Passerine
host species are shown below each cuckoo species and were adapted from Aidala et al. (2012). Spectral tuning sites 86, 90, and 93 are
underlined.
This is the first study to report on the sequence of SWS1
receptors and to predict short-wavelength visual sensitivities of New Zealand's brood parasitic native Shining
Cuckoos and endemic Long-tailed Cuckoos. Substituting S for A at amino acid residue 86 (A86S substitution)
produces a short-wave shift of 1 nm, a T93V substitution produces a long-wave shift of 3 nm, and a C90S
substitution produces a 35 nm long-wave shift in the
UVS SWS1 opsin of the Budgerigar (Melopsittacus undulatus) (Wilkie et al. 2000). The same C90S substitution in the Zebra Finch (Taeniopygia guttata) produces
a similar-magnitude long-wave shift of SWS1 maximal
sensitivity from 359 to 397 nm (Yokoyama et al., 2000).
Thus, despite possessing S86 and T93 in both species, the presence of S90 predicts that the SWS1 maximal
sensitivities of our cuckoo samples should be well within the visible-violet portion of the light spectrum, or VS
(Table 1).
This finding is contradictory to our original prediction that only the Long-tailed Cuckoo should possess
UVS SWS1 opsins due to the predicted UVS SWS1 of
its Whitehead host (in contrast with the VS SWS1 of
the Shining Cuckoo's Grey Warbler host; Table 1). Accordingly, we did not observe a distinct pattern between
predicted SWS1 sensitivities of our cuckoo samples and
those of their hosts. Both the Grey Warbler and Whitehead are non-ejector hosts of the Shining and Longtailed Cuckoos respectively, yet these host species differ
in their predicted SWS1 maximal sensitivities; DNA
sequencing of the SWS1 photoreceptor gene predicted
a VS SWS1 in the Grey Warbler but a UVS SWS1 in the
Whitehead (Aidala et al., 2012). Predicted sensitivities of the other two Long-tailed Cuckoo hosts, the
non-ejector Yellowhead, and the artificial egg-ejecting
Brown Creeper are not yet described from molecular
sequencing data. Also undocumented is the degree of
physical or perceptual host-parasite egg color matching, in the UV-portion specifically, and in the avianvisible spectrum overall, in these two host-parasite systems. Nonetheless, human-visible assessment suggests some level of mimicry between Long-tailed Cuckoos
and their hosts (Briskie, 2003), whereas the dark Shining
Cuckoo's eggs may be cryptic, and not mimetic, in the
enclosed nests of the Grey Warbler hosts (see Langmore
et al., 2009).
An alternative to perceptual coevolutionary processes mediating the detection of parasitic eggs in New
Zealand hosts is that the cost of accepting parasitic eggs
might be offset by recognizing and rejecting parasitic
cuckoo chicks (Davies, 2000). Despite a lack of direct
behavioral or sensory data in our focal systems, there is
evidence of parasitic chick detection and ejection based
on visual appearance in the closely related Australian
Large-billed Gerygone (Gerygone manirostris)/Little
Bronze-cuckoo (Chalcites [Chrysococcyx] minutillus)
(Sato et al., 2010) and Superb Fairy-wren (Malurus cyaneus)/Shining Cuckoo host-parasite systems (Langmore
et al., 2003; see also Langmore et al., 2011). Further, there is evidence of evolved call-matching of the begging calls of Grey Warblers by Shining Cuckoo chicks
based on both sound recordings (McLean and Waas, 1987) and comparative phylogenetic inference (Anderson et al., 2009). Similarly, McLean and Waas (1987)
noted and Ranjard et al. (2010) provided bioacoustic
evidence for the evolved similarity between the begging
calls of the Long-tailed Cuckoo and its Mohoua spp.
hosts. Other parasitic cuckoo-host systems, including
the Horsefield's Bronze-cuckoo (Chalcites [Chrysococcyx] basalis) and its Superb Fairy-wren (Malurus cyaneus) hosts (Langmore et al., 2003, 2008; Colombelli-Negrel et al., 2012), the Diederick Cuckoo (Chrysococcyx
caprius) and its hosts, and the Koel (Eudynamis scolopacea) and its House Crow (Corvus splendens) hosts have
also been shown to have similar begging calls (reviewed
in Grim, 2006).
Characterizing the visual sensitivities of diverse avian
lineages, including parasitic cuckoo species, is an important step in understanding the coevolution of visual
perception/parasitic egg rejection behaviors in hostparasite interactions and sensory ecology. These studies
form the basis for future visual modeling and sensoryphysiological studies for more accurate description of
the perceptual systems of focal cuckoo species. Future
studies should investigate the behavioral significance
of egg color matching in driving sensory coevolution
using appropriate visual perceptual modeling analyses
of both host and parasitic species (Aidala and Hauber, 2010). Additional Cuculiformes species should also be
included in future analyses in order to better describe
the degree of V/UV-matching in host-parasite egg color
mimicry and its perception and the ecological variables
that may drive or hinder the evolution of UV-sensitivity
amongst parasitic and non-parasitic cuckoos (Krüger et al., 2009).
Acknowledgments
All field work was conducted in accordance
with local animal ethics rules and regulations in New Zealand
and the University of Auckland. We thank Brian Gill for
providing tissue samples of Long-tailed Cuckoos at the Auckland
Museum and Andrew Fidler for advice on sequencing. We also
thank the many volunteers for assistance in field work, and
two anonymous reviewers for the helpful comments on our
manuscript. This research was funded by the US National Science
Foundation and the Graduate Center of the City University of
New York (to ZA and to MEH), a Foundation for Research, Science, and Technology postdoctoral fellowship (to MGA), and
the National Geographic Society, the PSC-CUNY grant scheme, and the Human Frontier Science Program (to MEH).
Bao HH, Liang QJ, Zhu HL, Zhou XQ, Zheng WH, Liu JS. Metabolic rate and evaporative water loss in the silky starling (Sturnus sericeus). Zool Res. 2014;35:280-6.
Brand MD, Turner N, Ocloo A, Else PL, Hulbert AJ. Proton conductance and fatty acyl composition of liver mitochondria correlates with body mass in birds. Biochem J. 2003;376:741-8.
Burness GP, Ydenberg RC, Hochachka PW. Interindividual variability in body composition and resting oxygen consumption rates in breeding tree swallows Tachycineta bicolor. Physiol Zool. 1998;71:247-56.
Chamane SC, Downs CT. Seasonal effects on metabolism and thermoregulation abilities of the red-winged starling (Onychognathus morio). J Therm Biol. 2009;34:337-41.
Christians JK. Controlling for body mass effects: Is part-whole correlation important? Physiol Biochem Zool. 1999;72:250-3.
Clapham JC. Central control of thermogenesis. Neuropharmacology. 2012;63:111-23.
Cooper SJ. Seasonal energetics of mountain chickadees and juniper titmice. Condor. 2000;102:635-44.
Cooper SJ. Daily and seasonal variation in body mass and visible fat in mountain chickadees and juniper titmice. Wilson J Ornithol. 2007;119:720-4.
Daan S, Masman D, Groenewold A. Avian basal metabolic rates: their association with body composition and energy expenditure in nature. Am J Physiol. 1990;259:R333-40.
Dawson WR, Carey C. Seasonal acclimatization to temperature in cardueline finches I. Insulative and metabolic adjustments. J Comp Physiol B. 1976;112:317-33.
Dawson WR, Marsh RL. Winter fattening in the American Goldfinch and the possible role of temperature in its regulation. Physiol Zool. 1986;59:353-69.
Dawson WR, Marsh RL, Buttemer WA, Carey C. Seasonal and geographic variation of cold resistance in house finches. Physiol Zool. 1983;56:353-69.
Diamond JM. Evolution of biological safety factors: a cost/benefit analysis. In: Weibel ER, Taylor CR, Bolis L, editors. Principles of animal design. Cambridge: Cambridge University Press; 1998. p. 21-7.
Doucette LI, Geiser F. Seasonal variation in thermal energetics of the Australian owlet-nightjar (Aegotheles cristatus). Comp Biochem Physiol. 2008;151A:615-20.
Estabrook RW. Mitochondrial respiratory control and polarographic measurement of ADP/O ratio. In: Estabrook RW, Pullman ME, editors. Methods in enzymes, X. New York: Academic Press; 1967. p. 41-7.
Guillemette M, Butler PJ. Seasonal variation in energy expenditure is not related to activity level or water temperature in a large diving bird. J Exp Biol. 2012;215:3161-8.
Hammond KA, Szewczak J, Król E. Effects of altitude and temperature on organ phenotypic plasticity along an altitudinal gradient. J Exp Biol. 2001;204:1991-2000.
Hegemann A, Matson KD, Versteegh MA, Tieleman BI. Wild skylarks seasonally modulate energy budgets but maintain energetically costly inflammatory immune responses throughout the annual cycle. PLoS ONE. 2012;7:e36358.
Hill RW. Determination of oxygen consumption by use of the paramagnetic oxygen analyzer. J Appl Physiol. 1972;33:261-3.
Hu SN, Zhu YY, Lin L, Zheng WH, Liu JS. Temperature and photoperiod as environmental cues affect body mass and thermoregulation in Chinese bulbuls, Pycnonotus sinensis. J Exp Biol. 2017;220:844-55.
Kelly JP. Behavior and energy budgets of belted kingfishers in winter. J Field Ornithol. 1998;69:75-84.
Kersten M, Piersma T. High levels of energy expenditure in shorebirds; metabolic adaptations to an energetically expensive way of life. Ardea. 1987;75:175-87.
Klaassen M, Oltrogge M, Trost L. Basal metabolic rate, food intake, and body mass in cold- and warm-acclimated Garden Warblers. Comp Biochem Phys A. 2004;137A:639-47.
Li XS, Wang DH. Seasonal adjustments in body mass and thermogenesis in Mongolian gerbils (Meriones unguiculatus): the roles of short photoperiod and cold. J Comp Physiol B. 2005;175:593-600.
Li YG, Yang ZC, Wang DH. Physiological and biochemical basis of basal metabolic rates in Brandt's voles (Lasiopodomys brandtii) and Mongolian gerbils (Meriones unguiculatus). Comp Biochem Phys A. 2010;157:204-11.
Liknes ET, Swanson DL. Seasonal variation in cold tolerance, basal metabolic rate, and maximal capacity for thermogenesis in white-breasted nuthatches Sitta carolinensis and downy woodpeckers Picoides pubescens, two unrelated arboreal temperate residents. J Avian Biol. 1996;27:279-88.
Liknes ET, Swanson DL. Phenotypic flexibility in passerine birds: seasonal variation of aerobic enzyme activities in skeletal muscle. J Therm Biol. 2011;36:430-6.
Liknes ET, Scott SM, Swanson DL. Seasonal acclimatization in the American goldfinch revisited: to what extent to metabolic rates vary seasonally? Condor. 2002;104:548-57.
Liu JS, Li M. Phenotypic flexibility of metabolic rate and organ masses among tree sparrows Passer montanus in seasonal acclimatization. Acta Zool Sin. 2006;52:469-77.
Liu JS, Li M, Shao SL. Seasonal changes in thermogenic properties of liver and muscle in tree sparrows Passer montanus. Acta Zool Sin. 2008;54:777-84.
MacKinnon J, Phillipps K. A field guide to the birds of China. London: Oxford University Press; 2000.
Maria S, Swanson DL, Cheviron ZA. Regulatory mechanisms of metabolic flexibility in the dark-eyed junco (Junco hyemalis). J Exp Biol. 2015;218:767-77.
McKechnie AE. Phenotypic flexibility in basal metabolic rate and the changing view of avian physiological diversity: a review. J Comp Physiol B. 2008;178:235-47.
McKechnie AE, Swanson DL. Sources and significance of variation in basal, summit and maximal metabolic rates in birds. Curr Zool. 2010;56:741-58.
McKechnie AE, Wolf BO. The allometry of avian basal metabolic rate: good predictions need good data. Physiol Biochem Zool. 2004;77:502-21.
McKechnie AE, Freckleton RP, Jetz W. Phenotypic plasticity in the scaling of avian basal metabolic rate. Proc R Soc Lond B. 2006;273:931-7.
McNab BK. The relationship among flow rate, chamber volume and calculated rate of metabolism in vertebrate respirometry. Comp Biochem Physiol A. 2006;145:287-94.
McNab BK. Ecological factors affect the level and scaling of avian BMR. Comp Biochem Physiol A. 2009;152:22-45.
Piersma T, Bruinzeel L, Drent R, Kersten M, Van der Meer J, Wiersma P. Variability in basal metabolic rate of a long-distance migrant shorebird (Red Knot, Calidris canutus) reflects shifts in organ sizes. Physiol Zool. 1996;69:191-217.
Piersma T, Drent J. Phenotypic flexibility and the evolution of organismal design. Trends Ecol Evol. 2003;18:228-33.
Petit M, Lewden A, Vézina F. How dose flexibility in body mass composition relate to seasonal changes in metabolic performance in a small passerine wintering at northern latitude? Physiol Biochem Zool. 2014;87:539-49.
Petit M, Clavijo-Baquet S, Vézina F. Increasing winter maximal metabolic rate improves intrawinter survival in small birds. Physiol Biochem Zool. 2017;90:166-77.
Rising JD, Hudson JW. Seasonal variation in the metabolism and thyroid activity of the black-capped chickadee (Parus atricapillus). Condor. 1974;76:198-203.
Schmidt-Nielsen K. Animal physiology: adaptation and environment. London: Cambridge University Press; 1997.
Smit B, McKechnie AE. Avian seasonal metabolic variation in a subtropical desert: basal metabolic rates are lower in winter than in summer. Funct Ecol. 2010;24:330-9.
Southwick EE. Seasonal thermoregulatory adjustments in white-crowned sparrows. Auk. 1980;97:76-85.
Starck JM, Rahmaan GHA. Phenotypic flexibility of structure and function of the digestive system of Japanese quail. J Exp Biol. 2003;206:1887-97.
Stokkan KA, Mortensen A, Blix AS. Food intake, feeding rhythm, and body mass regulation in Svalbard rock ptarmigan. Am J Physiol. 1986;251:R264-7.
Sundin U, Moore G, Nedergaard J, Cannon B. Thermogenin amount and activity in hamster brown fat mitochondria: effect of cold acclimation. Am J Physiol. 1987;252:R822-32.
Swanson DL. Seasonal variation in cold hardiness and peak rates of coldinduced thermogenesis in the dark-eyed junco (Junco hyemalis). Auk. 1990;107:561-6.
Swanson DL. Seasonal adjustments in metabolism and insulation in the darkeyed junco. Condor. 1991a;93:538-45.
Swanson DL. Substrate metabolism under cold stress in seasonally acclimatized dark-eyed juncos. Physiol Zool. 1991b;64:1578-92.
Swanson DL. Are summit metabolism and thermogenic endurance correlated in winter—acclimatized passerine birds? J Comp Physiol B. 2001;171:475-81.
Swanson DL. Seasonal metabolic variation in birds: functional and mechanistic correlates. In: Thompson CF, editor. Current ornithology. Berlin: Springer; 2010. p. 75-129.
Swanson DL, Garland T Jr. The evolution of high summit metabolism and cold tolerance in birds and its impact on present-day distribution. Evolution. 2009;63:184-94.
Swanson DL, Liknes ET. A comparative analysis of thermogenic capacity and cold tolerance in small birds. J Exp Biol. 2006;209:466-74.
Swanson DL, McKechnie AE, Vézina F. How low can you go? An adaptive energetic framework for interpreting basal metabolic rate variation in endotherms. J Comp Physiol B. 2017;Suppl 1:1-18.
Swanson DL, Zhang Y, Liu JS, Merkord CL, King MO. Relative roles of temperature and photoperiod as drivers of metabolic flexibility in dark-eyed juncos. J Exp Biol. 2014;217:866-75.
Tieleman BI, Williams JB, Buschur ME, Brown CR. Phenotypic variation of larks along an aridity gradient: are desert birds more flexible? Ecology. 2003;84:1800-51.
Vézina F, Jalvingh K, Dekinga A, Piersma T. Acclimation to different thermal conditions in a northerly wintering shorebird is driven by body massrelated changes in organ size. J Exp Biol. 2006;209:3141-54.
Vézina F, Jalvingh KM, Dekinga A, Piersma T. Thermogenic side effects to migratory disposition in shorebirds. Am J Physiol. 2007;292:R1287-97.
Wang JM, Zhang YM, Wang DH. Seasonal thermogenesis and body mass regulation in plateau pikas (Ochotona curzoniae). Oecologia. 2006a;149:373-82.
Wang JM, Zhang YM, Wang DH. Seasonal regulations of energetics, serum concentrations of leptin, and uncoupling protein 1 content of brown adipose tissue in root voles (Microtus oeconomus) from the Qinghai-Tibetan plateau. J Comp Physiol B. 2006b;176:663-71.
Weathers WW. Climatic adaptation in avian standard metabolic rate. Oecologia. 1979;42:81-9.
Webster MD, Weathers WW. Seasonal changes in energy and water use by verdins, Auriparus flaviceps. J Exp Biol. 2000;203:3333-44.
Wiersma P, Muñoz-Garcia A, Walker A, Williams JB. Tropical birds have a slow pace of life. Proc Natl Acad Sci USA. 2007;104:9340-5.
Wiesinger H, Heldmaier G, Buchberger A. Effect of photoperiod and acclimation temperature on nonshivering thermogenesis and GDP-binding of brown fat mitochondria in the Djungarian hamster Phodopus s. sungorus. Pflugers Arch Eur J Physiol. 1989;413:667-72.
Wikelski M, Spinney L, Schelsky W, Scheuerlein A, Gwinner E. Slow pace of life in tropical sedentary birds: a common-garden experiment on four stonechat populations from different latitudes. Proc R Soc Lond B. 2003;270:2383-8.
Williams J, Tieleman BI. Flexibility in basal metabolic rate and evaporative water loss among hoopoe larks exposed to different environmental temperatures. J Exp Biol. 2000;203:3153-9.
Wu MS, Xiao YC, Yang F, Zhou LM, Zheng WH, Liu JS. Seasonal variation in body mass and energy budget in Chinese bulbuls (Pycnonotus sinensis). Avian Res. 2014;5:4.
Wu MX, Zhou LM, Zhao LD, Zhao ZJ, Zheng WH, Liu JS. Seasonal variation in body mass, body temperature and thermogenesis in the Hwamei, Garrulax canorus. Comp Biochem Physiol A. 2015;179:113-9.
Zhang YP, Liu JS, Hu XJ, Yang Y, Chen LD. Metabolism and thermoregulation in two species of passerines from south-eastern China in summer. Acta Zool Sin. 2006;52:641-7.
Zhang ZQ, Wang DH. Seasonal changes in thermogenesis and body mass in wild Mongolian gerbils (Meriones unguiculatus). Comp Biochem Physiol. 2007;148:346-53.
Zhao L, Zheng LY, Zhang W, Huang DF, Xu Y, Liu JS. Daily cyclic variation of metabolism and thermoregulation in the silky starling. Chin J Zool. 2013;48:269-77.
Zhao LD, Wang RM, Wu YN, Wu MS, Zheng WH, Liu JS. Daily variation in body mass and thermoregulation in male Hwamei (Garrulax canorus) at different seasons. Avian Res. 2015;6:4.
Zheng WH, Liu JS, Jang XH, Fang YY, Zhang GK. Seasonal variation on metabolism and thermoregulation in Chinese bulbul. J Therm Biol. 2008a;33:315-9.
Zheng WH, Li M, Liu JS, Shao SL. Seasonal acclimatization of metabolism in Eurasian tree sparrows (Passer montanus). Comp Biochem Physiol A. 2008b;151:519-25.
Zheng WH, Fang YY, Jang XH, Zhang GK, Liu JS. Comparison of thermogenic character of liver and muscle in Chinese bulbul Pycnonotus sinensis between summer and winter. Zool Res. 2010;31:319-27.
Zheng WH, Lin L, Liu JS, Xu XJ, Li M. Geographic variation in basal thermogenesis in little buntings: relationship to cellular thermogenesis and thyroid hormone concentrations. Comp Biochem Physiol A. 2013a;164:240-6.
Zheng WH, Lin L, Liu JS, Pan H, Cao MT, Hu YL. Physiological and biochemical thermoregulatory responses of Chinese bulbuls Pycnonotus sinensis to warm temperature: phenotypic flexibility in a small passerine. J Therm Biol. 2013b;38:483-90.
Zheng WH, Liu JS, Swanson DL. Seasonal phenotypic flexibility of body mass, organ masses, and tissue oxidative capacity and their relationship to RMR in Chinese bulbuls. Physiol Biochem Zool. 2014a;87:432-44.
Zheng WH, Li M, Liu JS, Shao SL, Xu XJ. Seasonal variation of metabolic thermogenesis in Eurasian tree sparrows Passer montanus over a latitudinal gradient. Physiol Biochem Zool. 2014b;87:704-18.
Zhou LM, Xia SS, Chen Q, Wang RM, Zheng WH, Liu JS. Phenotypic flexibility of thermogenesis in the Hwamei (Garrulax canorus): responses to cold acclimation. Am J Physiol. 2016;310:R330-6.
Table
1.
Predicted VS/UVS SWS1 opsin state of two New Zealand cuckoo species based on SWS1 amino acid sequences. Passerine
host species are shown below each cuckoo species and were adapted from Aidala et al. (2012). Spectral tuning sites 86, 90, and 93 are
underlined.
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