Nutritional stress and body condition in the Great
Gray Owl (Strix nebulosa) during winter irruptive
migrations
Gary R. Graves, Seth D. Newsome, David E. Willard, David A. Grosshuesch,
William W. Wurzel, and Marilyn L. Fogel
Abstract: The largest irruptive migration of the Great Gray Owl (Strix nebulosa Forster, 1772) recorded since 1831 oc-
curred in Minnesota, USA, during the winter of 2004?2005. We tested the hypothesis that morphometric indicators of nutri-
tional stress covary with stable isotope signatures in a sample of 265 owls killed by vehicle collisions. The ratio of carbon
to nitrogen in muscle (C/Nmuscle) was shown to be a reliable proxy of nutritional stress. d13C values for liver and muscle
were significantly higher in owls in poor condition, reflecting the depletion of lipid reserves in fasting individuals. On the
other hand, d15N values for liver and muscle were marginally lower or unchanged in owls in poor condition. Stomachs of
emaciated owls were less likely to contain prey, implying that many nutritionally stressed individuals were too weak to hunt
and were near the tipping point of irreversible fasts. In a broader context, sexual differences in the correlative relationships
between stable isotope signatures, C/N, and body condition suggest that the consequences of reversed sexual size dimor-
phism extend to physiological processes during the nonbreeding season.
Key words: body mass index, Great Gray Owl (Strix nebulosa), carbon, nitrogen, C/N, fasting, Minnesota, reversed sexual
size dimorphism, stable isotopes, starvation.
R?sum? : La plus importante migration irruptive de chouettes lapones (Strix nebulosa Forster, 1772) signal?e depuis
1831 s?est produite au Minnesota (?tats-Unis), durant l?hiver de 2004?2005. Nous avons test? l?hypoth?se selon laquelle les
variations d?indicateurs morphom?triques de stress nutritif seraient corr?l?es ? celles de la signature des isotopes stables
dans un ?chantillon de 265 chouettes mortes des suites de collisions avec des v?hicules. Il est d?montr? que le rapport
carbone?azote dans les muscles (C/Nmuscle) est un indicateur substitutif fiable du stress nutritif. Le fait que les valeurs de
d13C pour le foie et les muscles ?taient significativement plus ?lev?es pour les chouettes en mauvais ?tat t?moigne de l?ap-
pauvrissement des r?serves de lipides dans les individus ? jeun. Par contre, les valeurs de d15N pour le foie et les muscles
?taient l?g?rement plus faibles ou inchang?es dans les chouettes en mauvais ?tat. La probabilit? de trouver des proies dans
l?estomac de chouettes ?maci?es ?tait moins grande, ce qui indique que de nombreux individus soumis ? un stress nutritif
?taient trop faibles pour chasser et s?approchaient de limite du je?ne irr?versible. Dans un contexte plus large, les diff?rences
sexuelles des corr?lations entre la signature des isotopes stables, C/N et l??tat corporel sugg?rent que le dimorphisme sexuel
invers? de la taille a une incidence sur les processus physiologiques durant la p?riode internuptiale.
Mots?cl?s : indice de masse corporelle, chouette lapone (Strix nebulosa), carbone, azote, C/N, je?ne, Minnesota,
dimorphisme sexuel invers? de la taille, isotopes stables, famine.
[Traduit par la R?daction]
Received 26 January 2012. Accepted 10 April 2012. Published at www.nrcresearchpress.com/cjz on 19 June 2012.
G.R. Graves. Department of Vertebrate Zoology, MRC-116, National Museum of Natural History, Smithsonian Institution, P.O. Box
37012, Washington, DC 20013-7012, USA; Center for Macroecology, Evolution and Climate, University of Copenhagen, DK-2100,
Copenhagen ?, Denmark.
S.D. Newsome. Carnegie Institution of Washington, Geophysical Laboratory, 5251 Broad Branch Road Northwest, Washington,
DC 20015, USA; Department of Zoology and Physiology, University of Wyoming, 1000 East University Avenue, Department 3166,
Laramie, WY 82071, USA.
D.E. Willard. Zoology Department, Field Museum, 1400 South Lake Shore Drive, Chicago, IL 60605-2496, USA.
D.A. Grosshuesch. Superior National Forest, 2020 West Hwy 61, Grand Marais, MN 55604, USA.
W.W. Wurzel. Carnegie Institution of Washington, Geophysical Laboratory, 5251 Broad Branch Road Northwest, Washington, DC 20015,
USA; State University of New York College of Environmental Science and Forestry, SUNY-ESF, 1 Forestry Drive, Syracuse, NY 13210,
USA.
M.L. Fogel. Carnegie Institution of Washington, Geophysical Laboratory, 5251 Broad Branch Road Northwest, Washington, DC 20015,
USA.
Corresponding author: Gary R. Graves (e-mail: gravesg@si.edu).
787
Can. J. Zool. 90: 787?797 (2012) doi:10.1139/Z2012-047 Published by NRC Research Press
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Introduction
The most spectacular irruptive migrations observed among
Holarctic birds are arguably performed by the Great Gray
Owl (Strix nebulosa Forster, 1772), a low-density species of
the boreal forests of Eurasia and North America (Nero 1980;
Mikkola 1983; Cramp 1985). The underlying cause of irrup-
tive movements in this species was shrouded in mystery
through the mid-20th century (Bent 1938). This behavior is
now thought to be triggered by periodic population fluctua-
tions of microtine rodents, which constitute the bulk of the
owl?s diet (Nero 1980; Mikkola 1983; Cramp 1985; Bull and
Duncan 1993; Newton 2002, 2006; Cheveau et al. 2004).
Owls spatially track pulses in microtine populations and may
breed in widely separated locations in successive years. Indi-
viduals may winter near breeding sites or in locations hun-
dreds of kilometres south of the normal breeding range in
response to geographic patterns of vole abundance. Since the
first documented irruptive migration in North America in
1831 (Audubon 1838), more than 30 irruptions have been re-
corded south of the boreal forest in eastern North America
(Bull and Duncan 1993; Svingen and Lind 2005). The largest
recorded irruptive migration occurred during the winter of
2004?2005, when at least 5200 owls were observed, banded,
or found dead in Minnesota (USA), with smaller numbers re-
ported from Wisconsin (USA), Michigan (USA), Ontario
(Canada), and Quebec (Canada) (Svingen and Lind 2005).
The number reported in Minnesota alone represented roughly
17% of the North American population, recently estimated at
30 000 individuals (Rich et al. 2004).
A spectrum of hypotheses concerning the fates of irruptive
populations of Great Gray Owls can be synthesized from nat-
ural history observations (Bent 1938; Nero 1980; Nero and
Copland 1981; Mikkola 1983; Bull and Duncan 1993; Svin-
gen and Lind 2005; Graves and Niemi 2006). The more opti-
mistic hypotheses suppose that a majority of individuals
survive the winter and return in good nutritional condition to
their breeding grounds when spring arrives. At the other end
of the continuum, irruptive migrations may be one-way trips,
with most owls succumbing to starvation, predation, and ac-
cidental death. The latter scenario would have significant im-
plications for the population ecology of the Great Gray Owl
and the population genetics of the species as well if there is
strong natural selection for body size or if migratory irrup-
tions involve only parts of the breeding range. In truth, most
irruptive migrations occur in remote areas with low human
densities and few roads, making it difficult to mark individu-
als, track their movements, or monitor survivorship over ex-
tended time periods. Consequently, the geographic origin of
irruptive migrants, their physiological condition, and the pro-
portion that survive to the following breeding season are un-
known.
The large number of specimens salvaged during the 2004?
2005 irruption provided an unparalleled opportunity to deter-
mine if body condition was linked to stable carbon (d13C)
and nitrogen (d15N) isotope values of liver and muscle tissue.
Stable isotope analysis has emerged as a powerful tool in
ecological research because of the predictable relationship
between assimilated food and the isotopic composition of bi-
ological tissues (DeNiro and Epstein 1978; Estep and Dab-
rowski 1980; Hobson et al. 1999; Macko et al. 1983). Stable
isotope ratios are widely used by animal ecologists as indica-
tors of body condition (Hobson et al. 1993; Cherel et al.
2005; Mekota et al. 2006) and as tools to reconstruct diet
(Chamberlain et al. 2005), trophic niche width (Bearhop et
al. 2004; Mart?nez del Rio et al. 2009a), and food-web struc-
ture (Estep and Dabrowski 1980; Hobson and Welch 1992).
However, much remains to be learned about the physiological
processes that influence isotopic discrimination in metabol-
ically active tissues, and in particular, the effects of food and
water deprivation on stable isotope ratios (Kelly 2000; Ru-
benstein and Hobson 2004; Mart?nez del Rio et al. 2009b).
The large series of salvaged specimens also permitted us to
investigate the relationship between body condition and re-
versed sexual size dimorphism (RSD), where males are
smaller than females. Great Gray Owls exhibit the most ex-
treme RSD observed among Holarctic owls (Earhart and
Johnson 1970; Mueller 1986). Nearly two dozen hypotheses
have been proposed for the evolution of RSD in raptorial
birds (Earhart and Johnson 1970; Amadon 1975; Andersson
and Norberg 1981; Jehl and Murray 1986; Korpim?ki 1986;
Lundberg 1986; Mueller 1986, 1990; Hakkarainen and Kor-
pim?ki 1991; Bildstein 1992; Kr?ger 2005). These can be
roughly classified as (i) ecological hypotheses pertaining to
niche partitioning and prey size, (ii) reproductive and physio-
logical hypotheses, and (iii) behavioral hypotheses related to
sexual dominance and pair formation. Although the volumi-
nous literature on RSD in raptors has grown markedly in re-
cent decades, there is still no consensus on the selective
factors responsible for its evolution and maintenance.
We tested the hypothesis that morphometric indicators of
nutritional stress covary with stable carbon (d13C) and nitro-
gen (d15N) isotope values of liver and muscle tissue in a sam-
ple of 265 Great Gray Owls killed by vehicle collisions. We
also tested several related hypotheses. First, did owls experi-
ence progressive starvation at the population level during the
winter irruption (November through April)? If true, then the
proportion of salvaged owls in poor body condition should
have increased during the irruptive cycle. We also considered
the ?fasting endurance? hypothesis for RSD proposed by
Lundberg (1986), who suggested that female owls are se-
lected for larger body size and fasting endurance, whereas
males are selected for smaller body size and hunting effi-
ciency. If larger body size is advantageous during resource-
driven irruptive migrations, then body condition of females
should, on average, be measurably better than that of males.
Finally, we tested the hypothesis that the ability to capture
prey is related to body condition. We predict that the stom-
achs of emaciated owls would be less likely to contain prey.
Materials and methods
Specimen salvage and preparation
Extraordinary numbers of Great Gray Owls began to ap-
pear in northern Minnesota in November 2004. A few breed
in Minnesota (Bull and Duncan 1993), but the vast majority
were assumed to have immigrated from Ontario and Mani-
toba. The magnitude of the historic irruption was not appa-
rent until later in the winter when daily counts along some
census routes exceeded 100 individuals on at least 13 days
between 19 January and 20 March 2005 (Svingen and Lind
2005). This species exhibits little fear of humans and fre-
788 Can. J. Zool. Vol. 90, 2012
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quently perches on fence posts, road signs, and telephone
poles near roadsides (Nero 1980). Indeed, most specimens
salvaged during the 2004?2005 migration were recovered as
frozen carcasses along roads, presumably killed by collision
with vehicles. A minimum of 767 specimens were picked up
dead or injured in Minnesota (Svingen and Lind 2005),
mostly from northeastern counties (Aitkin, Carlton, Crow
Wing, Lake, Itasca, Pine, St. Louis). This total was an order
of magnitude larger than the number salvaged during any of
the previous 10 irruptive migrations in Minnesota. The extent
to which salvaged specimens represent random population
samples is unknown.
Salvaged carcasses were dated, labeled with locality data,
placed in plastic bags, stored in freezers, and eventually
transferred to the Field Museum (FM), Chicago, Illinois, for
preparation. Necropsy revealed that most individuals were
killed by collisions with vehicles, whereas others showed no
signs of physical trauma. We could not determine the date of
death, but we assumed that large dark-colored carcasses
(length 68 cm; wing span 130 cm) on snow would be quickly
scavenged by foxes (Vulpes vulpes (L., 1758)), coyotes
(Canis latrans Say, 1823), gray wolves (Canis lupus L.,
1758), and ravens (Corvus corax L., 1758). Thus, it is likely
that most intact frozen carcasses were salvaged within a few
days of death.
Specimens were weighed to the nearest gram, prepared as
rounded study skins and partial skeletons (generally the trunk
and femora), or as complete skeletons. The term ?body mass?
is used throughout the paper, although our measurements
were technically weights (Lidicker 2008). We classified sal-
vaged specimens into two unambiguous age classes based on
plumage characters: (1) yearlings in their first winter and
(2) adults in their second or later winter. The 2004?2005 ir-
ruptive migration was composed almost entirely of adults.
Only 2 out of the 265 specimens analyzed in this study were
yearlings. We pooled yearlings and adults in the analyses.
Although Great Gray Owls often commence breeding during
late winter, none of the salvaged owls was in breeding condi-
tion (no gonadal enlargement) at the time of death.
Analyses of stomach contents provided additional insight
on the potential link between body condition and the ability
to capture prey. Stomach contents (1223 prey items) were ex-
amined in 585 specimens (258 males, 327 females; Table 1).
Whole or partially digested food items (exclusively small
mammals) were preserved as skeletons and hair samples.
Prey retention rates in the stomachs of Great Gray Owls are
unknown, but the presence of hair and bone likely indicates
the consumption of prey within 48 h of death (Andrews
1990).
Subcutaneous body fat of owls (Table 1) was classified at
necropsy: (1) emaciated (no fat; sunken breast muscle; keel
very evident); (2) no fat (breast muscle normal but no fat evi-
dent); (3) traces of fat (small amounts of fat around edge of
furculum); (4) light fat (a bit of fat filling the bottom of the
furculum area; little on other parts of body); (5) moderate fat
(substantial solid fat deposits in furculum region; some fat on
flanks and pelvic area); (6) heavy fat (fat bulging out of fur-
cular cleft; also significant fat in pelvic region); and (7) ex-
tremely fat (subcutaneous fat covering body, sometimes as
thick as 6 mm in pelvic area; covering breast and up into
neck). All fat classifications were scored by D.E.W. Bulk
samples of liver and pectoral muscle were preserved in
100% ethanol from the same industrial stock. All specimens
were deposited in the research collections of the FM.
Body mass index (BMI)
Five axial and two appendicular skeletal characters were
measured to the nearest 0.1 mm with digital calipers. Owing
to bone breakage, a substantial number of specimens lacked
1?3 skeletal values. Sample sizes for skeletal metrics varied
in males (n = 116?138) and females (n = 116?125). We re-
stricted the data set to specimens with complete measure-
ments for (i) sternum length (medially, from the manubrium
to the caudal edge of the sternum), (ii) keel length (the dis-
tance from the carinal apex to the caudal edge of the ster-
num), (iii) coracoid length, and (iv) femur length. The
sternum supports the principal flight muscles (pectoralis and
supracoracoideus), which compose as much as 25% of lean
body mass in owls (Hartman 1961).
To provide a direct morphological comparison of males
and females, we performed a principal components analysis
(PCA) on the aforementioned skeletal measurements for the
pooled sample of males (n = 138) and females (n = 125).
The first principal component (PC1) extracted from a correla-
tion matrix of untransformed variables was used as a measure
of overall body size, unbiased by the nutritional condition of
the owl or its stomach contents. All component loadings were
highly positive (>0.93) and PC1 explained 89.4% of the total
variance in body size. We constructed a BMI by regressing
body mass on PC1 scores (from the pooled sample of males
and females) with ordinary least squares regression (OLS).
The residuals (BMI) represent observed deviations in body
mass from values predicted from PCA I (skeletal size).
Strongly negative BMI values indicate emaciated individuals
in poor condition, whereas strongly positive BMI values indi-
cate owls in good condition with substantial subcutaneous fat
deposits.
Stable isotope analyses
We analyzed the nitrogen (d15N) and carbon (d13C) iso-
topic composition of liver and pectoral muscle, which exhibit
contrasting rates of metabolism and protein synthesis (Hob-
son and Clark 1992; Bauchinger and McWilliams 2009) and
provide data on the physiology of wintering owls at different
temporal scales. Given that turnover rates scale allometrically
to the ?0.25 power of body mass (Carleton and Mart?nez del
Rio 2005), isotope signatures of owl liver likely represent re-
sources incorporated over relatively short time frames (1?
2 weeks), whereas those of muscle reflect resources incorpo-
rated over moderately longer periods (3?5 weeks).
Liver and pectoral muscle samples were removed from
ethanol, repeatedly rinsed in distilled water, and freeze-dried.
Lipids were not extracted because we wanted to test the rela-
tionship between body condition and C/N of bulk tissues,
which has been shown to be a reliable proxy for intramuscu-
lar and hepatic lipid stores and nutritional stress (Hayashi
1983; Okumura et al. 2002; Post et al. 2007). Preservation
in ethanol can result in significant changes in carbon and ni-
trogen isotope signatures of bulk tissues, largely through hy-
drolysis of 13C-depleted lipids and proteins (Sarakinos et al.
2002; Sweeting et al. 2004; Kelly et al. 2006). Experimental
tests on a variety of animal tissues indicate that preservation
Graves et al. 789
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effects are rapid and relatively insensitive to ethanol concen-
tration (e.g., 70% vs. 100%). At the time of isotope analysis,
all tissue samples had been stored in ethanol taken from the
same stock and held under similar conditions for >12 months.
Thus, isotope values should be broadly comparable within
tissue type.
Approximately 0.5 mg of powdered tissue samples was
sealed in clean tin capsules for isotopic analysis. Carbon
(d13C) and nitrogen (d15N) isotope values were determined
using a Carlo Erba elemental analyzer (NC 2500; Carlo
Erba, Milan, Italy) interfaced with a Thermo-Finnegan Delta
Plus XL mass spectrometer (Carnegie Institution of Washing-
ton, Washington, D.C., USA).
Isotopic results are expressed as d values (Craig 1961):
d13C or d15N = 1000 ? [(Rsample/Rstandard) ? 1], where Rsample
and Rstandard are the 13C/12C or 15N/14N ratios of the sample
and standard, respectively. We used Vienna ? Pee Dee Be-
lemnite limestone (V?PDB) for carbon and atmospheric N2
for nitrogen as standards. The units are expressed as parts
per thousand, or per mil (?). The within-run standard devia-
tion of an acetalinide standard was ?0.2? for both d13C and
d15N values. We also measured the atomic C/N of liver
(C/Nliver) and muscle (C/Nmuscle) from each specimen.
Statistical analyses
We approached the investigation of body condition in a
hierarchical fashion, beginning with simple correlation analy-
sis (Pearson?s correlation coefficients; r) to investigate the
bivariate relationships among continuous variables. Two-
sample Student?s t tests (pooled variance) were used to com-
pare mean values of males and females. Chi-square tests were
used to evaluate 2 ? 2 frequency tables. Spearman?s rank
correlation coefficients (rS) were used to evaluate the strength
of the relationship between BMI and categorical body fat
scores recorded during specimen preparation. Because etha-
nol preservation may affect tissues differentially, we did not
directly compare mean isotope values of liver and muscle.
We then used a simple general linear model (GLM) to in-
vestigate the relationship between BMI and two predictor
variables (sex, date of salvage). Two candidate models were
examined, one with an interaction term (sex ? date of sal-
vage) and one without. The simpler model presented in the
results had a lower Akaike?s information criterion (AIC)
score (Akaike 1974). All P values are two-tailed (a = 0.05).
Results
Size and body condition
Great Gray Owls exhibit significant RSD in body mass
and skeletal size. The largest female (1750 g) was threefold
larger than the smallest male (582 g) by body mass. Accord-
ingly, males (body mass: 582?1208 g, 895 ? 164 g (mean ?
SD); n = 138) were significantly lighter than females (body
mass: 664?1750 g, 1143 ? 221 g; n = 125; t = 10.36, P <
0.0001). RSD was also evident in PC1 factor scores extracted
from the correlation matrix of skeletal variables (Fig. 1).
Skeletal size of males (PC1: ?2.28 to 0.57, ?0.81 ? 0.50
(mean ? SD); n = 138) was significantly smaller than in fe-
males (PC1: ?0.57 to 2.37, 0.88 ? 0.58; n = 125; t = 25.60,
P < 0.0001).
Males and females did not differ in categorical measures of
subcutaneous fat (seven-point scale) recorded during speci-
men preparation (Mann?Whitney U = 8618, P = 0.92;
Fig. 2). Fat scores were highly correlated with body mass in
males (n = 138; rS = 0.90, P < 0.0001) and females (n =
124; rS = 0.89, P < 0.0001) but were uncorrelated with date
of salvage in males (n = 138; rS = 0.04, P = 0.56) and fe-
males (n = 124; rS = 0.03, P = 0.76). Thirty-three percent
of males and 28% of females had body masses lower than
the minimum values listed for the species in Bull and Dun-
can (1993), indicating that a substantial fraction of the sal-
vaged specimens were in poor body condition.
BMI scores, which are the residuals from OLS regression
of body mass (g) on PC1 scores, were highly correlated with
fat scores (rS = 0.89, P < 0.0001; Fig. 2). BMI scores of fe-
males (?457 to 681, 35 ? 233 (mean ? SD); n = 125) were
significantly higher than those of males (?353 to 320, ?31 ?
165; n = 138; t = 2.67, P = 0.008; Fig. 1). BMI scores were
uncorrelated with date of salvage in males (n = 138; r =
0.00, P = 0.97) and in females (n = 125; r = 0.09, P =
0.33; Fig. 3). Salvage dates for males and females did not
differ significantly (t = 0.53, P > 0.05).
C/N of bulk tissue
C/Nliver values (mean ? SD) were 4.9 ? 0.6 (n = 132) for
males and 4.7 ? 0.5 (n = 116) for females. C/Nliver was un-
correlated with BMI scores and salvage date (Table 2,
Fig. 4). C/Nmuscle values (mean ? SD) were 4.4 ? 0.5 (n =
131) for males and 4.4 ? 0.5 (n = 116) for females. C/Nmuscle
Table 1. Stomach contents (empty or contained prey) and fat scores of salvaged
Great Gray Owls (Strix nebulosa) (n = 585 specimens) in Minnesota during the
2004?2005 irruptive migration.
Males Females
Fat scores Empty
Contained
prey* % empty Empty
Contained
prey* % empty
1 47 7 87 47 10 82
2 15 18 45 13 22 37
3 9 17 35 5 23 18
4 13 40 25 12 41 23
5 8 24 25 21 59 26
6 12 44 21 16 42 28
7 1 3 25 4 12 25
Note: See text for definitions of fat scores.
*Including hair and bone.
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was uncorrelated with salvage date but was positively corre-
lated with BMI scores (Table 2, Fig. 4).
Stable carbon isotopes
d13Cliver values from the pooled sample of males and fe-
males ranged from ?28.0? to ?19.2? (?25.8? ? 1.3?,
mean ? SD; n = 263). There was no difference between
males and females in d13Cliver values (n = 265; t = 1.81, P =
0.07). d13Cliver values were uncorrelated with date of salvage
(Table 2). On the other hand, d13Cliver values were negatively
correlated with BMI scores in males but not in females (Ta-
ble 2, Fig. 5). d13Cliver values were negatively correlated with
C/Nliver in males (n = 132; r = 0.29, P = 0.001) and in fe-
males (n = 116; r = 0.21, P = 0.02; Fig. 6).
d13Cmuscle values from the pooled sample of males and fe-
males ranged from ?27.8? to ?20.6? (?25.5? ? 1.1?,
mean ? SD; n = 263). There was no difference between fe-
males and males in d13Cmusclevalues (n = 263; t = 0.42, P =
0.68). d13Cmuscle values were uncorrelated with date of sal-
vage but were highly negatively correlated with BMI scores
(Table 2, Fig. 5). d13Cmuscle values were negatively correlated
with C/Nmuscle in males (n = 131; r = ?0.61, P < 0.0001)
and in females (n = 116; r = 0.40, P = 0.0001; Fig. 6).
Stable nitrogen isotopes
d15Nliver values from the pooled sample of males and fe-
males ranged from 5.0? to 11.6? (8.2? ? 1.0?, mean ?
SD; n = 263). There was no difference between males and
females in d 15Nliver values (n = 263; t = 0.80, P = 0.43).
d15Nliver values were uncorrelated with date of salvage (Ta-
ble 2). However, d15Nliver values were positively correlated
with BMI scores in males but not in females (Table 2,
Fig. 7). d15Nliver values were uncorrelated with C/Nliver in
males (n = 132; r < 0.01, P = 0.96) and in females (n =
116; r = ?0.03, P = 0.79).
d15Nmuscle values for the pooled sample of males and fe-
males ranged from 3.1? to 9.5? (6.3? ? 0.9?, mean ?
SD; n = 263). There was no difference between males and
females in d15Nmuscle values (n = 263; t = 1.41, P = 0.16).
d15Nmuscle values were uncorrelated with date of salvage in
males (Table 2). d15Nmuscle values were positively correlated
with BMI scores in males but not in females (Table 2,
Fig. 7). d15Nmuscle values were positively correlated with
C/Nmuscle in males (n = 131; r = 0.19, P = 0.03) and in fe-
males (n = 116; r = 0.22, P = 0.02).
Multivariate predictors of BMI
The GLM model explained only 3% of the variance in
BMI (Table 3). As expected from bivariate correlation coeffi-
cients (Table 2), sex had a significant effect on BMI scores.
However, there was no evidence that the proportion of owls
in poor body condition increased over the course of the win-
ter (Table 3, Fig. 3).
Stomach contents and body condition
Mammalian prey items (whole prey, bone, or hair) were
found in the stomachs of 362 (62%) out of 585 salvaged
Fig. 1. Relationship between body mass index (BMI) and body size
(first principal component, PC1) of Great Gray Owls (Strix nebu-
losa) salvaged during the 2004?2005 irruptive migration in Minne-
sota. Males and females are represented by ? and ?, respectively.
Fig. 2. Box plots depicting the relationship between body mass in-
dex (BMI) and body fat scores (1 = emaciated; 7 = extremely fat) in
Great Gray Owls (Strix nebulosa) salvaged during the 2004?2005
irruptive migration in Minnesota. Males (n = 140) are represented
by shaded boxes and females (n = 125) by unshaded boxes. The
bottom and top of the boxes represent the 25th and 75th percentiles,
respectively; the horizontal line indicates the median; and the whis-
kers represent the extreme values. Negative BMI scores represent
emaciated individuals.
Fig. 3. Relationship between body mass index (BMI) and salvage
date (day 1 equals 1 November 2004) of male (?; n = 140) and fe-
male (?; n = 125) Great Gray Owls (Strix nebulosa) obtained dur-
ing the 2004?2005 irruptive migration in Minnesota.
Graves et al. 791
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specimens (Table 1). The five most abundant prey species ac-
counted for 96% of the identified items: meadow vole (Mi-
crotus pennsylvanicus (Ord, 1815)) (78.6%), common shrew
(Sorex cinereus Kerr, 1792) (5.9%), arctic shrew (Sorex arcti-
cus Kerr, 1792) (4.8%), mole shrew (Blarina brevicauda
(Say, 1823)) (4.2%), and southern red-backed vole (Cleth-
rionomys gapperi (Vigors, 1830)) (2.5%). Owls with empty
stomachs had significantly lower fat scores than owls with
prey in their stomachs (n = 262; t = ?8.85, P < 0.0001).
Likewise, individuals with empty stomachs had significantly
lower BMI scores (n = 263; t = ?9.90, P < 0.0001). How-
ever, males were no more likely to have empty stomachs
than females (c2 = 0.26, P = 0.61).
Discussion
Fasting and measures of nutritional condition
Birds and mammals experience three physiological phases
Table 2. Pearson?s correlation coefficients for body mass index (BMI), date of salvage,
C/N, and carbon and nitrogen isotope values for liver and muscle of Great Gray Owls
(Strix nebulosa) salvaged during the 2004?2005 irruption.
BMI Date of salvage
Males n Females n Males n Females n
C/Nliver ?0.05 132 ?0.16 116 ?0.11 132 0.14 116
C/Nmuscle 0.56 131 0.54 116 0.15 131 0.08 116
d13Cliver ?0.48 138 ?0.26 125 ?0.02 138 0.04 125
d13Cmuscle ?0.63 138 ?0.45 125 ?0.17 138 ?0.05 125
d15Nliver 0.27 138 0.10 125 0.12 138 0.08 125
d15Nmuscle 0.27 138 0.17 125 ?0.04 138 0.09 125
Note: Correlation coefficients in boldface type are significant at a < 0.05, adjusted for the number
of simultaneous tests (P = 0.05/24 = 0.002).
Fig. 4. Relationship between body mass index (BMI) and C/N of liver and muscle of male (?) and female (?) Great Gray Owls (Strix neb-
ulosa) salvaged during the 2004?2005 irruptive migration in Minnesota.
Fig. 5. Relationship between body mass index (BMI) and d13C values of liver and muscle of male (?) and female (?) Great Gray Owls
(Strix nebulosa) salvaged during the 2004?2005 irruptive migration in Minnesota.
792 Can. J. Zool. Vol. 90, 2012
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as fasting progresses (Castellini and Rea 1992; Wang et al.
2006; Karasov and Mart?nez del Rio 2007; McCue 2010).
After feeding ceases, glycogen stores are depleted over a pe-
riod of hours and fatty acids are released from adipose tissue
as a precursor to phase I. Following this short period of fast-
ing adjustment, gluconeogenesis of amino acids from muscle
protein, ketogenesis of ketone bodies, and glycerol from adi-
pose tissue supply the energy needed for brain and organ
function. As phase II progresses, the proportion of lipids fu-
eling metabolism increases markedly while protein catabo-
lism declines or remains minimal. The shift from prolonged
fasting to what is usually referred to as starvation occurs be-
tween phase II and phase III. Protein is metabolized to main-
tain organ function in phase III after lipid reserves are
depleted in phase II. Death ensues when vital organ function
can no longer be sustained through protein metabolism. The
ability to reverse a prolonged fast in phase III may vary sig-
nificantly among taxa.
There have been no experimental studies of fasting in
strigid owls, but the physiological responses of birds and
mammals to food deprivation (references in McCue 2010),
especially those of the distantly related Barn Owl (Tyto alba
(Scopoli, 1769)) (Handrich et al. 1993; Thouzeau et al. 1997,
1999), provide a context in which the body condition and sta-
ble isotope signatures of Great Gray Owls may be inter-
preted.
Of the 265 salvaged Great Gray Owls analyzed in this
study, 28% of females and 33% of males had body masses
lower than the minimum values listed for the species by Bull
and Duncan (1993). This suggests that prolonged fasting and
starvation may occur in a significant fraction of owls during
irruptive migrations. However, the proportion of owls in poor
Fig. 6. Relationship between C/N and d13C values of liver and muscle of male (?) and female (?) Great Gray Owls (Strix nebulosa) salvaged
during the 2004?2005 irruptive migration in Minnesota.
Fig. 7. Relationship between body mass index (BMI) and d15N values of liver and muscle of male (?) and female (?) Great Gray Owls
(Strix nebulosa) salvaged during the 2004?2005 irruptive migration in Minnesota.
Table 3. Effects of sex and salvage date on body mass index (BMI) of Great Gray Owls
(Strix nebulosa) salvaged during the 2004?2005 irruptive migration in Minnesota.
Source Type III sums of squares df Mean squares F P
Sex 277 985 1 277 985 6.93 0.009
Date of salvage 36 696 1 36 696 0.92 0.34
Error 10 424 545 260 40 094
Graves et al. 793
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body condition did not increase over the course of the winter.
Fat and emaciated individuals were salvaged each month
from December through May. The significant number of sal-
vaged specimens with substantial fat deposits indicates that
good nutritional condition was no safeguard against acciden-
tal death.
Fat scores were positively correlated with BMI scores,
which were derived from skeletal measurements and body
mass. These in turn were positively correlated with C/N of
muscle (Fig. 4), but not in liver, which has a substantially
higher metabolism. This suggests that lipid reserves in
muscle of emaciated individuals were greatly reduced or ex-
hausted. Overall, our results suggest that C/N of muscle may
serve as a general indicator of nutritional condition in owls,
with higher C/N indicative of greater lipid reserves (Okumura
et al. 2002; Post et al. 2007; Ehrich et al. 2010). This assay is
more convenient and less invasive than other methods for
quantifying nutritional condition, such as the measurement
of bone marrow (Thouzeau et al. 1997) or whole body
homogenization followed by lipid extraction (Baduini et al.
2001).
Stable isotope markers
Food manipulation experiments with captive birds and
monitoring of fasting wild birds have shown that food restric-
tion produces an increase (Cherel et al. 2005; Williams et al.
2007), a decrease (Hatch et al. 1995), or no effect (Hobson et
al. 1993; Kempster et al. 2007) on d13C values of blood or
muscle tissues. These analyses included lipid-extracted tis-
sues (Hobson et al. 1993; Kempster et al. 2007) and tissues
in which the lipid content was unaltered (Cherel et al. 2005;
Williams et al. 2007). Because of experimental constraints
and animal welfare protocols, the degree of food deprivation
observed in some of these studies was relatively minor com-
pared with the fasting experienced by many of the owls in the
present study. Other experiments (reviewed in McCue and
Pollock 2008) have reported elevated d13C values in tissues
of starving lycosid spiders (Oelbermann and Scheu 2002),
migratory locusts (Locusta migratoria (L., 1758)) fed on
low-quality diets (Webb et al. 1998), and Nile tilapia (Oreo-
chromis niloticus (L., 1758)) fed a below-maintenance diet
(Gaye-Siessegger et al. 2007).
In general, lipids are depleted in 13C relative to carbohy-
drates and proteinaceous tissues (Tieszen et al. 1983; Kelly
2000; Teece and Fogel 2007); thus, d13C values of bulk tis-
sues may become more positive after endogenous glycogen,
a storage carbohydrate, and lipids are catabolized during ex-
tended fasts. Our data exhibit the expected trend in that ema-
ciated, presumably starving, owls had significantly higher
d13C values for liver and muscle than individuals with high
fat scores. The strongly negative association of d13C values
with fat scores was also mirrored in the relationship between
d13C values and BMI (Fig. 5) and between d13C values and
C/N (Fig. 6).
Nutritional stress and starvation often result in elevated
d15N values in the tissues of birds and mammals (Gloutney
et al. 1999; Hobson et al. 1993; Cherel et al. 2005; Fuller et
al. 2005; Mekota et al. 2006). Enrichment of 15N during fast-
ing occurs when endogenous tissue proteins are catabolized
as a source of amino acids, which undergo deamination or
transamination to produce 15N-depleted NH3. In birds, 15N-
depleted NH3 is directly excreted or converted to uric acid as
a waste product for excretion, leaving a pool of enriched
amino acids to be synthesized into proteins (Macko et al.
1986). Some experimental feeding studies, however, have
shown an insignificant or mixed relationship between food
deprivation and d15N values in growing chicks (Kempster et
al. 2007; Williams et al. 2007; Sears et al. 2009). Kempster
et al. (2007) suggested there may be a threshold effect in
which significant changes in isotopic composition may only
be observed during periods of extreme starvation when en-
dogenous protein stores are being catabolized for metabolism
(e.g., phase III). The interpretation and generalization of re-
sults, however, are complicated by the fact that recent experi-
ments were conducted on rapidly growing juveniles, rather
than adults, and that ?diet-restricted? individuals were fed
enough to permit body mass to marginally increase during
the experiment to comply with animal welfare protocols
(e.g., Kempster et al. 2007, Williams et al. 2007, Sears et al.
2009). For animals that have completed their growth, the pre-
ponderance of evidence suggests that tissues which maintain
significant protein synthesis (e.g., liver) will exhibit elevated
d15N values if protein is catabolized during an extreme fast
(Mart?nez del Rio et al. 2009b).
One notable finding in our study was that d 15N values for
muscle and liver were uncorrelated or slightly positively cor-
related with BMI scores. Instead of exhibiting higher d15N
values, the pooled sample of emaciated males and females
(fat score = 1, n = 58) had slightly lower d15N values than
owls in good condition (fat scores = 6?7, n = 55). This find-
ing runs counter to the expectation of nitrogen enrichment in
emaciated or starved individuals documented in several stud-
ies (Hobson et al. 1993, 1997; Cherel et al. 2005; Fuller et al.
2005; Mekota et al. 2006). To detect a shift in d15N, however,
new muscle or liver proteins would need to be synthesized
from a pool of amino acids with an enriched 15N content de-
rived from the catabolization of endogenous protein during
phase III (Balter et al. 2006).
Our data provide no evidence for a systemic pattern of ni-
trogen enrichment in emaciated owls. This suggests that d15N
enrichment of muscle and liver tissue may not be a hallmark
of starvation in this species. However, it is possible that met-
abolically active tissues (e.g., blood), other than liver and
muscle, experienced d15N enrichment in emaciated owls
(Mart?nez del Rio et al. 2009b). Also, it is possible that owls
recycle nitrogenous constituents during uric acid formation
which are then used to synthesize new protein without the
telltale signature of d15N enrichment. Experimental studies
have shown that the distantly related Barn Owl has the ability
to recover after body mass losses of up to 30% during phase
II of starvation (Handrich et al. 1993). Although strigid owls
may have similar physiological capacities, the fact that nearly
a third of the Great Gray Owl specimens analyzed in our
study had body masses lower than the minimum values listed
for males (825 g) and females (1025 g) by Bull and Duncan
(1993) indicates that fasting-mediated mortality may be com-
mon during irruptive migrations.
RSD and body condition
Our data provide weak support for the ?fasting endurance?
hypothesis for the evolution of RSD in owls proposed by
Lundberg (1986). Lundberg?s (1986) hypothesis was built on
794 Can. J. Zool. Vol. 90, 2012
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an extensive body of literature documenting increases in fast-
ing endurance with increasing body mass in birds and mam-
mals (Calder 1974; Boyce 1979; Lindstedt and Boyce 1985).
The breeding biology of Great Gray Owls is similar to that of
several other boreal strigids in that nesting is often initiated
when heavy snow still blankets the landscape (Mikkola
1983; Nero 1980; Bull and Duncan 1993). Females alone in-
cubate the eggs during the month-long incubation period and
perform all the brooding for the first 2?3 weeks after hatch-
ing (Nero 1980; Mikkola 1983). The smaller male feeds the
female and provisions the nestlings. The ?fasting endurance?
hypothesis posits that large females with greater fat stores
may have a selective advantage if prey is delivered at long
and unpredictable intervals. Female Great Gray Owls, which
are substantially larger in skeletal size and body mass than
males, exhibited significantly higher BMI scores. On average,
females were 3.1% heavier than expected from skeletal size
and males were 3.6% lighter than expected. Sexual differen-
ces in the correlation between BMI and carbon and nitrogen
isotope signatures suggest that the consequences of RSD ex-
tend to the physiological markers of body condition as well
(Table 2).
In conclusion, Great Gray Owls engaged in irruptive mi-
grations exhibit wide variation in body conditions, ranging
from emaciated individuals in the throes of starvation to ap-
parently healthy individuals with ample fat deposits. De-
creases in tissue lipid concentrations during the later stages
of phase II fasting may result in higher d13C values but lower
elemental C/N. Our results suggest that C/N of muscle may
serve as a general indicator of nutritional condition in owls,
with higher C/N indicative of greater lipid reserves. Although
emaciated owls lacked one of the expected hallmarks of
severe starvation, the enrichment of nitrogen isotopes,
stomach-content data from a larger sample of salvaged owls
(Table 1) indicate that emaciated individuals were in a preca-
rious nutritional state. Approximately 85% of emaciated owls
(fat score = 1) had empty stomachs compared with 25% of
owls with moderate to high fat scores (4?7). This suggests
that the ability to obtain prey was significantly compromised
by poor body condition. Furthermore, owls in the final stages
of starvation may be unable to digest prey because of gastro-
intestinal deficiencies (Handrich et al. 1993). Although owls
may be able to recover from prolonged fasting (Handrich et
al. 1993; Thouzeau et al. 1997, 1999), the low percentage of
emaciated Great Gray Owls that had recently fed in this study
suggests that many were in irreversible fasts.
Acknowledgements
For salvaging speciments, we thank C. Henderson, J. Hines,
M. Hamady, K. Haws, P. Perry, K. Woizeschke, J. Welsh,
M. Minchak, S. Wilson, and R. Staffon (all from the Minne-
sota Department of Natural Resources), J. Lind (from Natural
Resources Research Institute), and J. Goggin (from Raptor
Research Center). T. Gnoske and M. Hennen of the Field
Museum helped with specimen preparation. E. Snyder,
C. Mancuso, and B. O?Connor provided laboratory assis-
tance. The manuscript was significantly improved by com-
ments on earlier drafts by John Whiteman and two
anonymous reviewers. G.R.G was supported by the Wetmore
Fund (National Museum of Natural History, Smithsonian In-
stitution) and G.R.G. and S.D.N were supported by the Wal-
cott Fund (National Museum of Natural History, Smithsonian
Institution). S.D.N was also supported by the National Sci-
ence Foundation (ATM-0502491), Carnegie Institution of
Washington, and the W.M. Keck Foundation (072000).
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