![Average changes in body mass, food intake, and nitrogen (N) balance in Hermit Thrushes and White-throated Sparrows in the nonmigratory state (n = 20 and n = 22, respectively) that ingested different amounts of protein. Brackets along the x-axis show the four dietary protein groups (3.6%, 6.7%, 9.7%, and 12.8%) that were used to produce this range in dietary N intake. Changes in N balance as a function of N intake by Hermit Thrushes and White-throated Sparrows are described by the equations y = 0.430x − 22.82 (R 2 = 0.75, n = 20) and y = 0.358x − 16.44 (R 2 = 0.63, n = 22), respectively. (A) Horizontal shaded area depicts the average (± 90% confidence interval [CI]) change in body mass of birds in steady state (Hermit Thrush, n = 20; White-throated Sparrow, n = 22) during the 14 days prior to the start of total-collection trials. Horizontal dashed lines and surrounding shaded area depict (B and E) food intake and (C and F) N balance (± 90% CI) of birds in the nonmigratory state that consumed adequate dietary protein (≥9.7% protein) during the total-collection trials.](https://www.researchgate.net/profile/Scott-Mcwilliams-2/publication/239732176/figure/fig2/AS:667857302061063@1536240997561/Average-changes-in-body-mass-food-intake-and-nitrogen-N-balance-in-Hermit-Thrushes_Q320.jpg)
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PROTEIN REQUIREMENTS OF AN OMNIVOROUS AND A GRANIVOROUS
SONGBIRD DECREASE DURING MIGRATION
R.—Muchas aves canoras son frugívoras estacionalmente: se alimentan principalmente de frutos durante la migración
y de insectos o semillas durante los períodos no migratorios. Estudios previos han sugerido que la mayoría de los frutos silvestres
podrían tener un contenido proteico inadecuado para las aves. Para evaluar el valor nutricional de los frutos es necesario conocer
los requerimientos proteicos de las aves en relación con la composición de los frutos disponibles. Evaluamos las predicciones de dos
hipótesis: () las diferencias interespecíficas en los requerimientos de proteína de las aves están relacionadas con sus estrategias de
forrajeo y () los requerimientos proteicos de las aves aumentan con la demanda, por ejemplo durante los períodos migratorios del
ciclo anual. Medimos los requerimientos proteicos de la especie omnívora Catharus guttatus y de la granívora Zonotrichia albicollis
durante estadíos migratorios y no migratorios del ciclo anual y comparamos los resultados con estimados publicados para otras especies
de aves canoras. En el estadío no migratorio, ambas especies comieron menos, perdieron masa corporal y presentaron un balance de
nitrógeno más negativo al reducirse el contenido proteico en la dieta. En el estadío migratorio, los individuos de C. guttatus perdieron
masa corporal y presentaron un balance de nitrógeno menor, pero no disminuyeron la ingesta de alimento con las disminuciones en
la proteína. Los individuos de Z . albicollis no cambiaron su masa corporal, ingesta de alimento, ni balance de nitrógeno al reducirse
la proteína. Ambas especies presentaron menores requerimientos proteicos durante la migración (. mg N día− y . mg N día−,
respectivamente) que durante los períodos no migratorios (. mg N día− and . mg N día−, respectivamente) al ser alimentadas
con una dieta que contenía . kJ g−. Estos hallazgos podrían explicar parcialmente cómo es que las aves pueden reaprovisionarse
ingiriendo alimentos limitados en proteína, como los frutos, durante la migración.
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e Auk 127(4):850−862, 2010
e American Ornithologists’ Union, 2010.
Printed in USA.
e Auk, Vol. , Number , pages −. ISSN -, elect ronic ISSN -. by e American Ornit hologists’ Union. All rights reserved. Please direct
all requests for permission to photocopy or reproduce article content throug h the Universit y of Califor nia Press’s Rights and Permissions website, http://ww w.ucpressjourna ls.
com/reprintInfo.asp. DOI : ./au k..
Los Requerimientos Proteicos de un Ave Canora Omnívora y una Granívora
Disminuyen Durante la Migración
Li L L i e A. LA n g L o i s 1 A n d sc o t t R. McWi L L i A M s
Department of Natural Resources Science, University of Rhode Island, Kingston , Rhode Island 02881, USA
A.—Many songbirds are seasonally frugivorous and eat primarily fruit during migration and insects or seeds during
nonmigratory periods. Previous work has suggested that most wild fruits may have inadequate protein for birds. Assessing the
nutritional adequacy of fruit requires knowing the protein requirements of birds in relation to the composition of available fruits. We
tested predictions of two hypotheses: () interspecific differences in protein requirements of birds are related to their foraging strategy;
and () protein requirements of birds increase with demand, for example during migratory periods of the annual cycle. We measured the
protein requirements of the omnivorous Hermit rush (Catharus guttatus) and the granivorous White-throated Sparrow (Zonotrichia
albicollis) during nonmigratory and migratory stages of the annual cycle and compared the results with published estimates for other
songbird species. In the nonmigratory state both species ate less, lost body mass, and had more negative nitrogen balance as dietary
protein decreased. In the migratory state Hermit rushes lost body mass and had lower nitrogen balance but did not reduce food intake
as dietary protein decreased, whereas White-throated Sparrows did not change body mass, food intake, or nitrogen balance as dietary
protein decreased. Both species had lower protein requirements during migration (. mg N day− and . mg N day−, respectively)
than during nonmigratory periods (. mg N day− and . mg N day−, respectively) when fed a diet containing . kJ g−. ese
findings may partially explain how birds can adequately refuel on protein-limited foods such as fruits during migration. Received
December , accepted April .
Key words: Catharus guttatus, fruit, Hermit rush, migration, nitrogen balance, protein requirements, songbirds, White-throated
Sparrow, Zonotrichia albicollis.
1E-mail: lillieal@mail.uri.edu
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B
refuel at stopover sites during migration, and
the quality and quantity of foods at these sites can influence the
rate at which fat and protein stores are replenished (Schaub and
Jenni a, Bairlein , Piersma , Pierce and McWilliams
) and, hence, the pace of migration (Schaub and Jenni b).
Many songbirds in temperate eastern North America and western
Europe switch from eating mostly insects during spring and sum-
mer to eating mostly fruit during autumn migration (Herrera ,
Le ve y a nd K ar aso v , B ai rl ein , K la si ng ). S easo na l f ru-
givory may benefit birds during autumn migration because fruits
are often abundant at stopover sites and are a relatively high-energy
food (Herrera , Bairlein , Bairlein and Simons , Smith
et al. ). Songbirds select habitats with greater fruit densities
while at stopover sites during autumn migration (Parrish ,
Herrera , Takanose and Kamitani ), and songbirds that
ate more fruit fattened at faster rates while at stopover sites with
greater fruit densities (Parrish , Smith and McWilliams ).
However, wild fruits offer consumers mostly simple carbohydrates
or fats, relatively little protein, much seed bulk and water content,
and a mixture of secondary compounds (Herrera , Johnson
et al. , Witmer ). us, fruits may provide adequate en-
ergy but inadequate protein for birds during migration, especially
compared with alternative foods such as insects, seeds, and grains
(Herrera , Jordano , Levey and Karasov ). A primary
focus of the present study is to determine whether wild fruits can
satisfy the protein requirements of migratory songbirds.
Berthold () proposed that the protein content of fruit
may limit its consumption by omnivorous songbirds. For example,
captive Garden Warblers fed only fruit were unable to maintain
body mass, whereas those fed fruit supplemented with protein
maintained or increased body mass (Berthold ; scientific
names of all bird species are given in Table ). Many other experi-
ments have also shown that fruit may be nutritionally inadequate
in that birds were unable to maintain body mass while eating only
fruit for several days (Izhaki and Safriel , Levey and Karasov
, Izhaki , Bairlein ). Witmer () demonstrated
that highly frugivorous birds such as Cedar Waxwings were able
to maintain body mass on synthetic diets with only .% protein
but that more omnivorous thrush species were unable to maintain
body mass on the same diets. Pryor et al. () and Singer ()
also suggested that frugivorous birds may have lower nitrogen re-
quirements as adaptations to their low-protein diets. erefore,
interspecific differences in the protein requirements of songbird
species may be related to their feeding strategy.
Protein requirements of birds may also depend on their phys-
iological state (Koutsos et al. a). For example, the protein re-
quirements of female birds increase during egg laying (Robbins
), and chicks need more protein during growth than adults
require for maintenance (Roudybush and Grau , Koutsos et
al. b). Murphy and King () estimated that the protein
requirement of White-crowned Sparrows during molt was %
above their minimum maintenance requirement. Protein require-
ments may increase during migration because protein can be
catabolized as a fuel and water source, especially when fat reserves
are depleted (Klaassen , Bauchinger and Biebach , Jenni
and Jenni-Eiermann ). us, protein requirements are unlikely
to be fixed for a given bird but instead may change with nutritional
demands across the annual cycle.
Our study tested predictions of two related hypotheses: ()
interspecific differences in protein requirements of birds is related
to their foraging strategy; and () protein requirements of birds
increase with demand, for example during migratory periods of
the annual cycle. To test these hypotheses, we measured the pro-
tein requirements of two passerine species, the White-throated
Sp ar row and th e He rm it ru sh, duri ng non mi gr ato ry an d m igra -
tory periods of their annual cycles and compared these estimated
protein requirements with published estimates for other songbird
species. We selected the White-throated Sparrow and Hermit
rush as focal species for our study because these birds are simi-
lar in body mass (on average, g and g, respectively), both are
seasonally frugivorous but to different extents (fruits composed
% of diet during autumn migration in Hermit rushes and
% in White-throated Sparrows; Parrish ), and they differ in
general foraging strategy during nonmigratory periods (omnivo-
rous Hermit rush, granivorous W hite-throated Sparrow). We
predicted that the more seasonally frugivorous Hermit rush
(Jones and Donovan ) would have lower protein requirements
than the less seasonally frugivorous White-throated Sparrow
(Falls and Kopachena ) but that the protein requirements of
both species would be higher than those of other migratory birds
that eat mostly fruit year-round. We also predicted that the pro-
tein requirements of both species would increase during the mi-
gratory period as protein turnover (Pennycuick , Schwilch et
al. ) and metabolic rate increased (Scott et al. , Piersma
). We also determined the extent to which the protein avail-
ability of wild fruits in southern New England satisfies the esti-
mated protein requirements of these two migratory songbirds and
other species.
Me t h o d s
Capture and maintenance of birds.—White-throated Sparrows
(n = ) and Hermit rushes (n = ) were captured using mist
nets during fall migration in in Kingston, Rhode Island
(°′N, °′W). e birds were transferred to indoor facilities
and housed individually in stainless-steel cages ( × × cm)
at constant temperature (°C) and a constant photoperiod rep-
resentative of natural photoperiod at capture ( h light: h dark
[L:D]; lights on at hours). During the -week acclima-
tion period, birds were provided ad libitum food and water along
with about to mealworms (Tenebrio molitor) each day.
e nutrient composition of the acclimation diet (diet A) was
similar to that of many natural high-carbohydrate fruits (.%
carbohydrates, .% protein, and .% fats; Table ). Casein and
L-crystalline amino acids were the sole source of dietary protein.
is agar-based mash diet is similar to the semisynthetic banana-
based diet of Denslow et al. (), with modifications as de-
scribed in Afik et al. () and Podlesak and McWilliams ().
e composition of the essential amino acids was based on the
semisynthetic diets described in Murphy and King () that sat-
isfy the maintenance requirements of White-crowned Sparrows
(Murphy ). Body mass was measured daily (±. g), and birds
remained in good health.
Maintenance diets and experiment.— Af ter th e -we ek a ccl i-
ma ti on p er io d, w e o ffer ed bi rd s on ly th e ac cl im at ion di et (no mea l-
worms) for the next weeks. We randomly assigned birds to one
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re plic ate s ( –) we re m ea sur ed as ne ede d u nti l e ach samp le’s co ef-
ficient of variation (CV) was <% for samples with <% nitrogen
(N) or until CV was <% for samples with >% N. We measured
energy content of food and feces using a Parr Isoperibol Oxy-
gen Bomb Calorimeter.
We estimated daily apparent metabolizable energy (AME;
kJ day−) as follows: AME = (F × FE) − (D × DE), where F is amount
of food consumed (g dry mass [DM] day−), FE is food energy den-
sity (kJ g− DM), D is amount of feces (g DM day-), and DE is feces
energy density (kJ g− DM). e efficiency of dietary energy utili-
zation was estimated as AME divided by gross energy content of
ingested food (Servello et al. ). We estimated nitrogen bal-
anc e (m g da y−) as the N intake minus N lost in urine and feces; the
equation is as follows: N balance = (F × FN) − (D × DN), where F is
amount of food consumed (g DM day−), FN is nitrogen content of
the foo d (m g N g− DM), D i s a mou nt o f fe ce s (g DM d ay−), and DN
is nitrogen content of the feces (mg N g− DM) (Murphy ).
Photoperiod stimulation and migration experiment.—
Because birds have a strong circadian and circannual rhythm, we
used both photoperiod stimulation (exposure to longer days) and
time of year to induce the migratory state (Bairlein , Bairlein
and Gwinner , Gauthreaux , Helm and Gwinner ).
In general, the migratory state is associated with a significant in-
crease in nightly activity, hyperphagia, and body mass (Bairlein
and Gwinner ). On March , four Hermit rushes and
four White-throated Sparrows were randomly assigned to a con-
trol group, placed in a separate room, and maintained on the same
constant light levels (L:D; lights on at hours). ree
birds were excluded prior to the migratory-state experiment be-
cause they did not maintain body mass. Light levels for the treat-
ment birds ( Hermit rushes and White-throated Sparrows)
were then incrementally changed over days from L:D to a
photoperiod representative of spring at the Rhode Island latitude
(L:D; lights on at hours). Treatment and control birds
were fed the acclimation diet (diet A), and we measured body mass
and food intake daily. is allowed us to determine when treat-
ment birds increased body mass and food intake as expected for
birds in the migratory state. We determined that a bird was in the
migratory state when its body mass increased by at least % within
– days (King and Farner ). For simplicity we designated
birds that underwent premigration hyperphagia and fattening as
“in migratory state,” because actual migration did not take place.
e control birds ( Hermit rushes and White-throated Spar-
rows) exposed to constant light levels did not significantly change
in body mass (t = −., df = , P = . and t = −., df = , P =
., respectively), and so, as expected, they never transitioned
into the migratory state. However, these nonsignificant results
must be cautiously interpreted because of the small sample size.
Nineteen of birds ( Hermit rushes and White-
throated Sparrows) exposed to longer day length increased their
body mass by, on average, . ± .% within – days (or, on av-
erage, . ± . g for Hermit rushes, t = −., df = , P = .;
and . ± . g for White-throated Sparrows, t = −., df = , P <
.). e birds that did not increase body mass did not par-
ticipate in the remainder of the experiment. Once we determined
that birds were in the migratory state, we assigned them sequen-
tially to one of the three diet groups used during the maintenance
experiment (B, C, D; Table ). e acclimation diet (diet A) was not
of four diet groups that differed in dietar y protein and carbohy-
drate concentration (diet A: .%, .%; diet B: .%, .%; diet
C: .%, .%; and diet D: .%, .%, respectively). e dietary
protein concentrations were chosen so that birds in some groups
(diets A and B) were fed diets with adequate protein whereas birds
in other groups (diets C and D) were fed diets with inadequate pro-
tein given the protein requirements of White-crowned Sparrows
(Murphy ). Diets were isocaloric because we replaced proteins
(casein; Table ) with carbohydrates (glucose) and these two ma-
cronutrients have similar energy density (protein: . kJ g−, car-
bohydrate: . kJ g−; Schmidt-Nielsen ).
We conducted -day total-collection trials (Murphy ,
Robbins ) for each diet group for both species during the th
week of captivity. Birds were transferred from the maintenance
diet (diet A) to their respective group diets on day of the total-
collection trials. At hours each day during these -day trials
we measured each bird’s body mass, provided each bird with ad libi-
tum fresh food, a nd weighed the food that remained from the pre-
vious day. We also collected all feces produced by each bird during
the previous h, along with samples of food offered and remain-
ing. Al l samples were stor ed frozen at −°C for later a naly sis.
We dried the samples of remaining food at °C until sample
mass was constant (~ week). e samples of offered food and feces
that were used for measuring protein content were freeze-dried to
constant mass ( days) to ensure that nitrogen was not lost dur-
ing drying. Dried samples were homogenized using mortar and
pestle. Nitrogen concentration in .- to .-mg subsamples was
measured using a Carlo-Erba NA Series II elemental ana-
lyzer attached to a continuous-flow isotope-ratio Micromass Op-
tima spectrometer (F-IRMS). Urea and powdered dogfish muscle
(DORM-) reference material (National Research Council, Insti-
tute for Environmental Chemistry, Ottawa) were used as work-
ing standards for nitrogen concentration analysis. Additional
tA b L e 1. Composition of the acclimation diet (diet A). The other three
experimental diets were the same as this acclimation diet except that glu-
cose replaced casein as dietary protein was decreased.
Ingredients
Dry mass
(%)
Wet mass
(%)
Glucose (g) 59.5 17.9
Caseina (g ) 10.0 3.0
Amino acid mixb ( g) 2.8 0.8
Vitamin and mineral mixc (g ) 2.5 0.8
Salt mixd (g) 5.5 1.7
Cellulosee (g) 5.0 1.5
NaHCO3f (g) 1.5 0.5
Choline chloridef (g ) 0.2 0.1
Olive oilg ( g) 8.0 2.4
Agarh (g ) 5.0 1.5
Water (g or mL) 0 70.0
a
Casein (high N): U.S. Biochemical, Cleveland, Ohio.
b
Amino acid mix: Fisher Scientific, Pittsburg, Pennsylvania; Murphy and King 1982.
c
AIN-76 Vitamin and Mineral Mix, ICN Biomedicals, Irvine, California.
d
Salt mix: Briggs-N Salt mixture, ICN Biomedicals.
e
Celufil-hydrolyzed: U.S. Biochemical.
f
NaHCO3 and choline chloride supplied by Fisher Scientific.
g
Botticelli brand olive oil.
h
Agar bacteriological grade: U.S. Biochemical.
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tA b L e 2. Body mass and food intake (means ± SD) of control (nonmigratory-state) and treatment (migratory-state) Hermit
Thrushes and White-throated Sparrows before and after we changed the daily photoperiod to induce the migratory state.
Body mass (g) Wet food intake (g)
Species Before After
aBefore Aftera
Hermit Thrush Control (n = 4) 30.6 ± 0.7 31.3 ± 1.2 21.1 ± 3.5 24.4 ± 0.8
Treatment (n = 9) 32.1 ± 2.7 34.9 ± 2.7** 22.1 ± 3.6 28.3 ± 4.4*
White-throated Control (n = 4) 25.6 ± 2.0 27.3 ± 2.2 21.6 ± 1.9 22.9 ± 1.0
Sparrow Treatment (n = 10) 24.9 ± 2.0 27.7 ± 1.8** 17.5 ± 2.2 25.7 ± 1.7 *
Note: *Significant paired t-test (P < 0.05) comparing body mass and food intake before and after change in photoperiod.
** Significant paired t-test (P < 0.001) comparing body mass and food intake before and after change in photoperiod.
a Control birds were kept at 12L:12D while treatment birds were changed from 12L:12D to 16L:8D.
tested during the migratory experiment, to increase sample size for
the other three diet groups. We conducted -day total-collection
trials on experimental birds in the migratory state while simulta-
neously conducting total-collection trials on control birds of the
same species. is procedu re resulted in t he experimenta l
birds starting their -day total-collection trials – days after
the change in day length. All birds were fed diet A prior to the
start of the -day total-collection trials, and diet B, C, or D there-
after. We conducted total-collection trials on control birds over
the same period in order to compare treatment and control birds
on the same days.
Statistical analysis.—We used paired t-tests to determine the
effect of photoperiod stimulation on body mass and food intake
in control and treatment birds. General-linear-model repeated-
measures analysis was used to estimate changes in body mass, food
intake, and N balance in control birds throughout the migratory-
state experiment to determine whether they remained in the non-
migratory state. Linear mixed modeling (LMM) was used to
determine the effect of treatment, day, and their interaction on
N balance for all birds in the nonmigratory and migratory states.
Multiple covariance structures of LMM were analyzed to deter-
mine the most accurate model on the basis of Hurvich and Tsai’s
information criterion (Lindsey and Jones ). For simplicity, we
report degrees of freedom rounded to the nearest whole number.
We used analysis of variance (ANOVA) to determine the effect of
bird species, physiological state, and dietary protein on N balance,
food intake, change in body mass, feces excretion, percent N in fe-
ces, and AME for each species on day of the migratory- and non-
migratory-state experiments. We also used ANOVA to compare
percent energy utilization among birds fed protein-sufficient diets
(diet B) for both species in the nonmigratory and migratory states.
We used a conservative P value (.) for Levene’s test of homoge-
neity of variance because of the robustness of the ANOVA model;
all reported statistical analyses satisfied the assumptions of nor-
mality and homogeneity of variance among treatment groups. We
estimated protein requirements on the basis of linear regressions
of N balance on N intake (mg) for birds on all four diets in the non-
m ig ra to ry -s ta te ex pe ri me nt an d d ie ts B, C, a nd D in t he m i gr at or y-
state experiment. We used t-tests to compare slope and elevation
(y-intercept) parameters from these regression equations for the
two species in different physiological states (Sokal and Rohlf ).
Values are reported as means ± SD, and the significance level was
set at P ≤ .. All statistical analyses were conducted with SPSS,
version ., for Macintosh (SPSS, Chicago, Illinois).
Re s u l t s
Confirmation of experimental design.—We first determined
whether the birds were acclimated to the experimental diets by
day of the -day trials. As the birds acclimated to the diets, the
N balance of Hermit rushes in the nonmigratory and migratory
states changed over the days (F = ., df = and , P = .
and F = ., df = and , P = ., respectively), whereas the N
balance of White-throated Sparrows changed while in the migra-
tory state (F = ., df = and , P = .) but not while in the
nonmigratory state (F = ., df = and , P = .). Given these
changes in N balance across the -day trials, we focus the remain-
der of our analyses for both the nonmigratory- and migratory-
state experiments on the third day of the -day trials because this
reduces the potential effects of previous diets and because the
birds had, by then, been acclimated to the experimental diets for
several days. Murphy () measured protein requirements in
birds for a - to -day period and concluded that the first days
were the most accurate because birds fed low-protein diets there-
after catabolized body protein. We assume that any bias associ-
ated with the birds not being fully acclimated to the experimental
diets by day was equally represented across treatment groups
and therefore would not change the relative differences in the esti-
mated protein requirements of these groups.
We increased day length for treatment birds and then moni-
tored their body mass and food intake to verif y that this change
in daily photoperiod induced the migratory state. As expected,
body mass and daily food intake of treatment birds significantly
increased within days from the onset of increased day-length
exposure (Hermit rush: t = −., df = , P = . and t = −.,
df = , P = ., respectively; White-throated Sparrow: t = −.,
df = , P < . a nd t = −. , d f = , P < ., respectively; Table ),
whereas body mass and daily food intake of control birds exposed
to constant day length did not change significantly over the same
period (Hermit rush: t = −., df = , P = . and t = −.,
df = , P = ., respectively; White-throated Sparrow: t = −.,
df = , P = . a nd t = −., d f = , P = ., respectively; Table ).
We calculated the statistical power to detect a -g change in food
intake and a .-g change in body mass (treatment effects reported
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in Table ), assuming α = . and using the estimated within-
group variance from our experiment. e power in this case was
– % fo r fo od i nt ake an d – % for body -ma ss c ha nge in co n-
trol Hermit rushes and White-throated Sparrows. us, we can
be –% certain of detecting this magnitude of change in food
intake and body mass for the two species at the % level of sig-
nificance. Because we conducted migration experiments in series
over days, we compared body mass, food intake, and N balance
of control birds between days , , and to verify that control
birds remained in the nonmigratory state. As expected, control
birds did not significantly change in body mass (Hermit rush:
F = ., df = and , P = .; White-throated Sparrow: F =
., df = and , P = .), food intake (Hermit rush: F =
., df = and , P = .; White-throated Sparrow: F = .,
df = and , P = .), or N balance (Hermit rush: F = .,
df = and , P = .; White-throated Sparrow: F = ., df =
and , P = .) during the -day experimental period. However,
sample sizes of control birds were small, so these results should be
interpreted cautiously.
Interspecific and physiological-state comparisons.—W h ite-
throated Sparrows had more positive N balance and higher food
intake, and lost less body mass on day of the total-collection tri-
als, than Hermit rushes fed the same diets (species effect: F =
., df = and , P = .; F = ., df = and , P < .; and
F = ., df = and , P = ., respectively). In general, birds of
both species in the migratory state had more positive N balance
and higher food intake than, and similar change in body mass as,
birds in the nonmigratory state (state effect: F = ., df = and
, P < .; F = ., df = and , P < .; and F = ., df =
and , P = ., respectively). However, interpretation of species
and physiological-state differences in N balance was complicated
be ca use we d etec te d si gn ifi can t i nte rac ti ons amon g sp ec ies , ph ys -
iological state, and diet (species*diet effect: F = ., df = and ,
P = .; state*diet interaction: F = ., df = and , P = .).
By contrast, interpretation of species and physiological-state dif-
ferences in food intake and body mass were simpler because these
in te rac ti on s we re n ot s ig ni fic ant (P > . in all cases). erefore, we
report the remainder of the results separately for Hermit rushes
and White-throated Sparrows in the migratory and nonmigratory
states, so that we can consider these interactions and also because
this allows us to include data from all diet groups (four diets for the
nonmigratory-state experiment and three diets for the migratory-
state experiment).
Nonmigratory-state Experiment
Nitrogen balance, food intake, and body mass for birds in the non-
migratory state.—In general, birds lost body mass, ate less, and
were in negative N balance as dietary protein decreased (Fig. ).
Hermit rushes and White-throated Sparrows lost, on average,
. ± . g and . ± . g and ate . ± . g and . ± . g, respec-
tively, when fed diets with <% protein, whereas the two species
gained or maintained body mass and ate significantly more when
fed the highest-protein diets (diet effect on body mass: F = .,
df = and , P = . and F = ., df = and , P < ., re-
spectively; diet effect on food intake: F = ., df = and , P <
. and F = ., df = and , P < ., respectively; Fig. ).
Hermit rushes and White-throated Sparrows that were fed <%
protein also produced less feces (F = ., df = and , P = .
and F = ., df = and , P < ., respectively) and had lower
percent N in their feces (F = ., df = and , P < . and
F = ., df = and , P < ., respectively) than those fed
higher-protein diets. However, this reduction in N excretion did
not compensate for the lower N intake, in that Hermit rushes
and White-throated Sparrows that were fed <% protein had a more
negative N balance than those fed the higher dietary protein (F =
., df = and , P < . and F = ., df = and , P = .,
respectively; Fig. C, F).
Protein requirements, minimum nitrogen requirements,
and total endogenous nitrogen losses of birds in the nonmigratory
state.—Protein requirements of birds in the nonmigratory state
were estimated from the regression of N balance on N intake for
all four diet groups on day of the experiment (Fig. C, F). We
estimated that the protein requirement of Hermit rushes in
the nonmigratory state was mg protein day− (. mg N ×
.), or ~.% protein for a diet containing . kJ AME g− DM.
Minimum nitrogen requirement (MNR) was calculated from the
regression equation as the dietary N intake that supports N equi-
librium (Allen and Hume ). e MNR of Hermit rushes
was . mg N kg−. day−. We estimated that the protein re-
quirement of White-throated Sparrows in the nonmigratory state
was mg protein day− (. mg N × .), or ~.% protein
for a diet containing . kJ AME g− DM, and that the MNR
of White-throated Sparrows was . mg N kg−. day−. Total
endogenous nitrogen loss (TENL) was calculated by regressing
N balance (N input − N output) against N intake and extrapolat-
ing to zero N intake. Our estimates of TENL in Hermit rushes
and White-throated Sparrows were . mg N kg−. day− and
. mg N kg−. day−, respectively. We detected no significant
difference between regressions (Fig. C, F) estimating the protein
requirements of Hermit rushes and White-throated Sparrows
in the nonmigratory state (slope: t = ., df = , P = .; eleva-
tion: t = ., df = , P = .), so these results for each species
are reported only for comparative purposes. In a separate section
below we report estimates of MNR from a common regression for
these birds in the nonmigratory state because we detected no
significant differences in MNR between species.
En er gy u ti liz at ion and m et abo liz ed ene rg y of b ird s in th e no n-
migratory state.—Hermit rushes and White-throated Spar-
rows in the nonmigratory state that were fed .% dietary protein
had significantly higher AME than birds fed lower dietary pro-
tein (F = ., df = and , P = . and F = ., df = and ,
P < ., respectively; Table ). Energy density of feces was less
in Hermit rushes fed the highest-protein diet (F = ., df =
and , P = .), whereas it did not differ among dietar y groups
in W hite-throated Sparrows (F = ., df = and , P = .).
Hermit rushes fed the lowest dietary protein had significantly
lower energy utilization (AME/gross energy content of ingested
food) than birds fed higher levels of protein (F = ., df = and
, P = .), although this was the one comparison for which
there was heterogeneity in variance between diet groups (Levene’s
test, P = .). Energy utilization in White-throated Sparrows
differed significantly between diet groups (F = ., df = and
, P < .). Overall, AME was similar between species (F = .,
df = and , P = .), whereas energy utilization was greater
in W hite-throated Sparrows than in Hermit rushes (F = .,
df = a nd , P = .). We excluded from these estimates of AME
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fig . 1. Average changes in body mass, food intake, and nitrogen (N) balance in Hermit Thrushes and White-throated Sparrows in the nonmigratory
state (n = 20 and n = 22, respectively) that ingested different amounts of protein. Brackets along the x-axis show the four dietary protein groups (3.6%,
6.7%, 9.7%, and 12.8%) that were used to produce this range in dietary N intake. Changes in N balance as a function of N intake by Hermit Thrushes
and White-throated Sparrows are described by the equations y = 0.430 x − 22.82 (R2 = 0.75, n = 20) and y = 0.35 8x − 16.44 (R2 = 0.63, n = 22), respec-
tively. (A) Horizontal shaded area depicts the average (± 90% confidence interval [CI]) change in body mass of birds in steady state (Hermit Thrush,
n = 20; White-throated Sparrow, n = 22) during the 14 days prior to the start of total-collection trials. Horizontal dashed lines and surrounding shaded
ar ea d epic t (B a nd E ) foo d in tak e an d (C a nd F ) N ba lance (± 90% CI) of birds in the nonmigratory state that consumed adequate dietary protein (≥9.7%
protein) during the total-collection trials.
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tA b L e 3. Apparent metabolizable energy intake (AME ± SD, kJ day−1) and energy utilization (percentage ±
SD, kJ day−1) of Hermit Thrushes and White-throated Sparrows in the nonmigratory and migratory states
when fed one of four diets with different amounts of protein.
Nonmigratory stateaMigratory state
Dietary
protein (%)
Hermit
Thrush
White-throated
Sparrow
Hermit
Thrush
White-throated
Sparrow
Apparent metabolizable energy intake
12.8 70.8 ± 9.6 A93.1 ± 28.5 A — —
9.7 48.4 ± 8.5 B57.8 ± 7. 8 B96.1 ± 12.6 119.5 ± 13. 8
6.7 46.8 ± 5.5 B44.3 ± 5.9 B101.8 ± 6.4 124. 3 ± 22.3
3.6 28.3 ± 24.9 B45.8 ± 8.8 B82.9 ± 16.3 115 .4 ± 31. 8
Energy utilization
12.8 84.1 ± 1.3 A86.6 ± 2.1 A — —
9.7 78.2 ± 1.6 A82.7 ± 1.4 B88.5 ± 0.7 90.1 ± 0.7
6.7 79.3 ± 1.7 A80.2 ± 2.7 B90.4 ± 1.3 89.1 ± 4.1
3.6 64.9 ± 14.7 B86.9 ± 0.5 A90.3 ± 0.8 91.6 ± 1.7
aFor Hermit Thrushes and White-throated Sparrows in the nonmigratory state, rows with different letters denote signifi-
cant differences between diets for each species (Tukey’s test, P < 0.05). There were no significant differences in A ME
between diet groups for Hermit Thrushes and White-throated Sparrows in the migratory state.
and energy utilization two Hermit rushes in diet group D that
were not in energy balance on day because of low food intake.
Migratory-state Experiment
Nitrogen balance, food intake, and body mass of birds in the mi-
gratory state.—Body mass of Hermit rushes fed diets with <%
protein dropped, on average, . ± . g, whereas those fed more
dietary protein maintained body mass (F = ., df = and ,
P = . ; Fi g. A). Wh ite -th ro ate d Sp ar row s lo st , on ave rag e, . ±
. g of body mass when fed the sa me range of dietary protein
and changed similarly across diet groups (F = ., df = and ,
P = .; Fig. D). On each of the three diets the birds had similar
food intake (Hermit rush: F = . , df = an d , P = .; Fig. B;
White-throated Sparrow: F = ., df = and , P = .; Fig. E)
and produced similar amounts of feces (Hermit rush: F = .,
df = and , P = .; White-throated Sparrow: F = ., df =
and , P = .). Percent N in feces decreased in White-throated
Sparrows fed <% protein (F = ., df = and , P = .),
wh ere as p erc ent N in f ece s d id n ot c han ge in Her mi t r us hes fed
the same range of dietary protein (F = ., df = and , P = .).
Hermit rushes fed the lowest dietary protein had a less positive
N balance than Hermit rushes fed the higher dietary protein
(F = ., df = and , P < .; Fig. C). e same trend was
apparent in White-throated Sparrows, but the difference in N bal-
ance between diet groups was not significant (F = ., df = and ,
P = .; Fig. F).
Protein requirements, minimum nitrogen requirements, and
total endogenous nitrogen losses of birds in the migratory state.—
Protein requirements of birds in the migratory state were esti-
mated from the regression of N balance on N intake for the three
diet groups (B, C, and D) on day of the experiment (Fig. C, F).
e protein requirement of Hermit rushes in the migrator y
state was . mg protein day− (. mg N × .), or ~.% pro-
te in for a d ie t co nta in in g . kJ AM E g− DM. e MNR of Hermit
rushes was . mg N kg−. day−. We estimated that the pro-
tein requirement of White-throated Sparrows in the migratory
state was . mg protein day− (. mg N × .), or ~.% pro-
tein for a diet containing . kJ AME g− DM. e MNR of White-
throated Sparrows was . mg N kg−. day−. Our estimate of
TENL in Hermit rushes and White-throated Sparrows was
. mg N kg− . day− and . mg N kg−. day−, respectively.
We detected no difference in either the slopes (t = ., df = ,
P = .) or the elevations (t = ., df = , P = .) of the re-
gression equations (Fig. C, F) that estimated the protein require-
ments of Hermit rushes and W hite-throated Sparrows in the
migratory state, so these results for each species are reported only
for comparative purposes. In a separate section below we report
estimates of MNR from a common regression for these birds in
the migratory state and compare them with those of birds in the
nonmigratory state.
Energy utilization and metabolized energy of birds in the
migratory state.—Both Hermit rushes and White-throated
Sparrows in the migratory state that were fed different levels of
dietary protein had similar AME and energy utilization (Hermit
rush: F = ., df = and , P = . a nd F = ., df = and ,
P = ., respectively; White-throated Sparrow: F = ., df =
and , P = . and F = ., df = and , P = ., respectively;
Table ). Overall, White-throated Sparrows had greater AME
than Hermit ru shes (F = ., df = and , P = .), whereas
energy utilization did not differ between species (F = ., df =
and , P = .). ese differences in AME (kJ day−) between
species are accentuated when the smaller body mass and, hence,
higher mass-specific metabolic rate of White-throated Spar-
rows are considered (e.g., for the .% protein diet in birds in the
nonmigratory state, the adjusted AME [kJ day− body mass−.]
was % higher in White-throated Sparrows [.] than in Her-
mit rushes [.], compared with the % higher AME [kJ/day]
shown in Table ).
Comparison of protein requirements of birds in the nonmigra-
tory and migratory states.—As noted above, because there were
no significant differences in slope and elevation from the regres-
sions for each species in the nonmigratory or migratory state, we
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fig . 2. Average changes in body mass, food intake, and nitrogen (N) balance in Hermit Thrushes and White-throated Sparrows in the migratory state
(n = 9 and n = 10, respectively) that ingested different amounts of protein. Brackets along the x-axis show the three dietary protein groups (3.6%,
6.7%, and 9.7%) that were used to produce this range in dietary N intake. Changes in N balance as a function of N intake by Hermit Thrushes and
White-throated Sparrows are described by the equations y = 0.567x − 5.25 (R2 = 0.85, n = 9) and y = 0.599x − 9.47 (R2 = 0.74, n = 10), respectively.
(A) Horizontal shaded area depicts the average (± 90% confidence interval [CI]) change in body mass of birds in steady state (Hermit Thrush, n = 20;
White-throated Sparrow, n = 22) during the 14 days prior to the start of total-collection trials in the nonmigratory-state experiments. Horizontal dashed
lines an d s ur roundi ng shaded ar ea depic t ( B and E) foo d int ake and (C and F) N b alance (± 90% CI) of birds in the migratory state that consumed
adequate dietary protein (9.7% protein) during the total-collection trials.
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calculated common regression equations for birds in each state.
e regressions differed significantly between states and demon-
strated that birds had lower protein requirements in the migratory
state than in the nonmigratory state (slope: t = . , d f = , P = .;
elevation: t = ., df = , P < .; Fig. ). We estimated that
the protein requirement of White-throated Sparrows and Hermit
rushes in the nonmigratory state was . mg protein day−
(. mg N × .), or ~.% protein for a diet containing . kJ
AME g− DM. We estimated that the protein requirement of
White-throated Sparrows and Hermit rushes in the migratory
st ate wa s . mg prot ei n da y− ( . mg N × .), or ~.% protein
for a diet containing . kJ AME g− DM.
A comparison of birds fed adequate protein (diet B) indicated
that birds in the migratory state had greater dietary energy uti-
lization than those in the nonmigratory state (F = ., df =
and , P < .) and that White-throated Sparrows had greater
dietary energy utilization than Hermit rushes (F = ., df =
and , P < .). Greater dietary energy utilization in migratory-
state birds was associated with higher food intake (F = ., df =
and , P < .), whereas percent N in feces and amount of feces
produced did not differ between states (F = ., df = and , P =
. and F = ., df = and , P = ., respectively).
Changes in body mass of birds during -day trials in both
physiological states were compared to determine whether protein
accretion might account for the differences in protein require-
ments of birds in the migratory versus the nonmigratory state.
Hermit rushes and White-throated Sparrows lost, on average,
. ± . g body mass during the -day collection trails (day effect:
F = ., df = and , P < .), although the extent of mass
loss differed by bird species (day*species interaction: F = .,
df = and , P = . ) a nd p hys iol og ica l s tat e (d ay* sta te in tera c-
tion: F = ., df = and , P < .). In the nonmigratory state,
Hermit rushes lost, on average, . ± . g during the -day trials,
and White-throated Sparrows lost, on average, . ± . g. In the
migratory state, Hermit rushes lost only . ± . g during the
-day trials, and White-throated Sparrows lost only . ± . g.
ese results simplify the interpretation of N requirements across
species and physiological state because they demonstrate that
birds in the nonmigratory and migratory states were not accumu-
lating protein or fat stores while we measured N balance.
di s c u s s i o n
P ro te in re q ui re me nt s of bi rd s i n r e la ti on t o t he ir fo ra g in g s tr at e gy .—
Our results were not consistent with the hypothesis that the protein
requirements of the more seasonally frugivorous Hermit rushes
were lower than those of the less frugivorous White-throated Spar-
rows. Foeken et al. () similarly found that a more frugivorous
hornbill species in the genus Aceros did not differ in protein re-
quirements from a more carnivorous hornbill species in the genus
Bucorvus. We found that MNR was similar in Hermit rushes
and White-throated Sparrows in the nonmigratory state and was
within the range of –, mg kg−. day− estimated for other
passerines in previous studies (Table ). Our MNR estimates for
the Hermit rush were higher than published estimates for other
omnivores such as the American Robin, yet lower than that for
the Wood rush. Our MNR estimates for the White-throated
Sparrow were higher than those for other granivores such as the
White-crowned Sparrow, yet lower than that for the granivorous
American Tree Sparrow. Likewise, our estimated TENL for the
Hermit rush was similar to those for the Wood rush and Eu-
ropean Starling, and our estimated TENL for the White-throated
Sparrow was similar to that for the White-crowned Sparrow. In
general, the studies of highly frugivorous birds published to date
(Table ) have consistently shown that their protein requirements
are lower than those of omnivores and granivores, including our
estimates for Hermit rushes and White-throated Sparrows in
the nonmigratory state.
Our estimates of the protein requirements of Hermit
Thrushes (. mg N day−) and W hite-throated Sparrows
(. mg N day−) in the nonmigratory state are higher than
those predicted from allometric equations that were based on
to species of songbirds (range in body mass: –, g) other
than Hermit rushes and White-throated Sparrows. Tsahar et
al.’s () allometric equation for omnivorous birds (MNR =
. mg N kg−. day−) predicts MNRs of . mg N day− and
. mg N day− for Hermit rushes and White-throated Spar-
rows, respectively. Robbins’s () equation for birds in general
(MNR = mg N kg−. day−) predicts MNRs of . mg N day−
and . mg N day− for Hermit rushes and White-throated
Sparrows, respectively. is suggests a need for more studies
such as ours that empirically measure protein requirements of a
diversity of birds so that more accurate allometric models can be
developed.
Protein requirements of birds change with physiological
state.—Birds ate significantly more food in the migratory state
than in the nonmigratory state, whereas N excreted per day was
similar in both states. Consequently, birds in the migratory state
had a more positive N balance than birds in the nonmigratory
state. Hyperphagia is well documented in birds during premigra-
tory fattening periods and migration (King and Farner ). Pre-
vious captive studies found that migratory birds increased their
fig . 3. Nitrogen (N) balance as a function of N intake by Hermit Thrushes
and White-throated Sparrows in the nonmigratory state (solid line) is de-
scribed by the equation y = 0.387x − 19.36 (R2 = 0.68, n = 42), and N bal-
ance as a function of N intake by Hermit Thrushes and White-throated
Sparrows in the migratory state (broken line) is described by the equation
y = 0.579x − 7.01 (R2 = 0.78, n = 19) .
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energy intake by –%, on average, when hyperphagic, com-
pared with the nonmigratory state (Bairlein ). We found
that daily energy intake in migratory-state Hermit rushes and
White-throated Sparrows increased by .% and .%, respec-
tively, compared with the nonmigratory state. Because increased
daily food and energy intake also increased N intake and was as-
sociated with no change in dry mass of feces excreted or percent
N in feces, birds in the migratory state were able to retain more ni-
trogen, and, hence, their dietary protein requirements decreased.
In other words, for a given N intake, birds in the migratory state
were able to extract more N and had a more positive N balance
than birds in the nonmigratory state (Fig. ). To our knowledge,
the present study is the first to quantify protein requirements of
the same songbird species in both the migratory and the nonmi-
gratory states.
Lower protein requirements of birds in the migratory state
were associated with an increase in energy utilization in birds fed
adequate protein diets (diet B). Furthermore, energy utilization in-
creased, on average, .% in Hermit rushes and .% in White-
throated Sparrows from the nonmigratory to the migratory state.
Increases in energy utilization have been documented in birds
during migration (Bairlein , Johnson et al. ). Energy utili-
zation may play an important role in migrant birds that subsist on
protein-deficient diets such as wild fruits.
Our estimates of MNR and TENL were remarkably lower for
Hermit rushes and White-throated Sparrows in the migratory
state than for those in the nonmigratory state. Both species were
in po sit ive N ba la nc e du ri ng t he m ig rato ry stat e, s o we must inte r-
pret these estimates of protein requirements with caution given
that this involved extrapolating to zero N balance. However, in
support of our findings, Roxburg and Pinshow () found no
significant difference between estimates of endogenous N loss ex-
trapolated from regression of N intake versus N excretion and the
actual values measured. Furthermore, because several birds fed
diets with the lowest dietary protein approached N equilibrium (N
balance ≤ mg N day−) and the regression equations explained
the majority of the variance (Hermit rush, R = .; White-
throated Sparrow, R = .), we are confident that the protein re-
quirements of these two species were lower in the migratory state
than in the nonmigratory state. Dietary N intake that supports
a zero N balance is the standard method of MNR measurement
(Murphy , Allen and Hume ), although birds are not al-
ways able to maintain body mass at N equilibrium (Brice and Grau
, Murphy ). Protein accretion and N loss other than in
urine and feces can explain a portion of this variation and, thus,
contribute to N requirements (Murphy ); however, it is un-
likely that our birds accrued protein stores given that they lost, on
average, .–. g body mass during the -day trials.
Ecological implications.—Contrary to our prediction that
dietary nutrient requirements would increase during migration,
we found that birds in the migratory state had lower protein re-
quirements than those in the nonmigratory state. Our findings
support Bairlein’s () and Murphy’s () hypothesis that the
protein requirements of birds may change seasonally and Klas-
ing’s () statement that birds with high rates of food intake are
able to satisfy daily protein requirements on diets with lower pro-
tein concentrations. Our results are also similar to those of Bair-
lein (), who found that Garden Warblers in the nonmigratory
tA b L e 4. Maintenance nitrogen requirements (MNR; mg N kg− 0.75 day−1 ) and total endogenous nitrogen losses (TENL; mg N kg−0.75 day−1) of bird
species during the nonmigratory state.
Species
Body mass
(g) MNR TENL Source
Granivores
Budgerigar (Melopsittacus undulatus)42 381 260 Pryor 2003
White-crowned Sparrow (Zonotrichia leucophrys)28 563 215 Calculated from Murphy 1993
House Sparrow (Passer domesticus)27 1,141 884 Weglarczyk 1981
White-throated Sparrow (Zonotrichia albicollis)a26 710 253 Present study
American Tree Sparrow (Spizella arborea arborea)b18 1,146 — Calculated from Martin 1968
Zebra Finch (Taeniopygia guttata)12 403 153 Allen and Hume 2001
Omnivores
African Gray Parrot (Psittacus erithacus erithacus)b500 491 — Kamphues et al. 1997
Amazon parrots (Amazona spp.)413 304 173 Westfahl et al. 2008
European Starling (Sturnus vulgaris)72 584 319 Tsahar et al. 2005a
American Robin (Turdus migratorius)66 484 197 Witmer 1998
Wood Thrush (Hylocichla mustelina)47 911 258 Witmer 1998
Hermit Thrush (Catharus guttatus)c31 719 309 Present study
Garden Warbler (Sylvia borin)b20 1,188 — Calculated from Bairlein 1987
Frugivores
Hornbill (Aceros sp.)b2,399 387 — Foeken et al. 2008
Pesquet’s Parrot (Psittrichas fulgidus)757 320 50 Pryor 2003
Tristram’s Grackle (Onychognathus tristrami)115 125 101 Tsahar et al. 2005b
Yellow-vented Bulbul (Pycnonotus xanthopygos)36 99 75 Tsahar et al. 2005b
Cedar Waxwing (Bombycilla cedrorum)35 264 69 Witmer 1998
aMNR and TENL for White-throated Sparrows in the migratory state: 244.2 mg kg−0.75 day−1 and 146.3 mg kg−0.75 day−1, respectively.
bTENL was not reported.
cMNR and TENL for Hermit Thrushes in the migratory state: 125.2 mg kg−0.75 day−1 and 71.1 mg kg−0.75 day −1, respectively.
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state were unable to maintain body mass when fed only fruits yet
were able to maintain body mass when fed the same fruits during
the premigratory fattening period. Lower protein requirements of
birds during migration may enable them to adequately refuel when
feeding on low-protein fruits during migration and could explain,
in part, why so many migratory birds seasonally switch from in-
sect to fruit consumption during migration (Berthold ).
Wild fruits vary in energy and protein composition (Fig. ),
and only some of these fruits may satisfy the protein requirements
of birds in the nonmigratory state, whereas most would satisfy
protein requirements during migration. Smith et al. () used
equations for Wood rush (Witmer ) and for species of
omnivores (Tsahar et al. ) to estimate protein requirements
of migratory songbirds and concluded that many fruits available
at stopover sites cannot satisfy their need for protein. However,
our results suggest that migrant birds have lower protein require-
ments than those estimated for the same birds in the nonmigra-
tory state. erefore, fruits previously considered protein-deficient
resources for migratory birds may satisfy their protein require-
ments. However, our conclusions ignore the potentially complex
interactions between secondary compounds in fruits and pro-
tein requirements (Witmer ), and these should be taken into
consideration. Our findings help resolve the apparent paradox of
seasonal frugivory: birds during migration may switch to eating
fruits with less protein because the hyperphagia associated with
the migr at ory s tate in bir ds f unc ti ona ll y re duce s t hei r d iet ar y pro -
tein requirements.
Ac k n o w l e d g M e n t s
We thank K. Winiarski for data analysis of the nitrogen content
of samples and the Environmental Protection Agency, Narragan-
sett, Rhode Island, for generously allowing use of their mass spec-
trometer. D. Tacey, H. Krohn, and M. Petrarca helped with care
and maintenance of the captive birds, and H. Krohn helped with
sample preparation and laboratory work. We are grateful to A.
Smith for help with statistical analyses and J. Bolser for support.
We thank U. Bauchinger and H. Biebach for their comments that
made this a better manuscript. is work was supported by the
University of Rhode Island (URI) Agricultural Experiment Station
(RIAES- to S.R.M.; contribution no. ) and the National
Science Foundation (IBN- to S.R.M.). Animal husbandry
procedures were approved by the URI Institutional Animal Care
and Use Committee (no. AN--).
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tolacca americana, 9 = Elaeagnus umbellata, 10 = Viburnum acerifolium,
11 = Smilax rotundifolia, 12 = Aronia prunifolia, 13 = Sambucus canadensis,
14 = Vitis labrusca, 15 = Prunus virginiana, 16 = Lonicera japonica, 17 =
Rosa virginiana, 18 = Aronia arbutifolia, 19 = Vaccinium corymbosum,
and 20 = Rubus occidentalis.
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