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Wilson
Bull., 107(2), 1995, pp. 296-305
PLASMA CORTICOSTERONE LEVELS IN TWO
SPECIES OF
ZONOTRICHIA
SPARROWS UNDER
CAPTIVE AND FREE-LIVING CONDITIONS
PETER P MARRA,’ KEVIN T.
LAMPE,~,’ AND BRUCE L. TEDFORD~,~
ABSTRACT.-We
compared the daily plasma corticosterone (B) profiles in captive and
free-living White-throated Sparrows
(Zonotrichia albicollis)
and White-crowned Sparrows
(Z.
leucophrys)
during their non-breeding period. Neither sparrow species exhibited signif-
icant die1 rhythms in the levels of corticosterone in captivity or under natural conditions,
although the variations were suggestive of a rhythm. In each species, secretory profiles
differed significantly between captive and free-living birds with mean B levels being 2-3
times higher in captive birds than in free-living individuals, despite the fact that captives
had been “acclimated” for 35 days prior to sampling. Furthermore, mean B levels were
two to four times higher in White-throated Sparrows under captive and free-living conditions
than in White-crowned Sparrows under the same conditions. Our results indicate the need
to use caution when (1) extrapolatin g such data obtained from captive individuals to those
under natural conditions and (2) extrapolating data regarding B from one species to another.
Received 28 July 1994, accepted I Dec. 1994.
Environmental stimuli may affect the concentrations and secretory pat-
terns of hormones, such as the “stress-related” corticosteroid hormones,
which can dictate physiological changes in organisms. In birds, the prin-
cipal corticosteroid hormone is corticosterone (hereafter “B”) (Assen-
macher 1973). Perception of stressful stimuli markedly enhances the rate
of B secretion through the actions of adrenal cortical stimulating hormone
(ACTH), resulting in increased levels of B in the blood (Siegel 1971,
1980). In birds, this cause-effect relationship has been shown to occur in
response to a variety of stressors (for review see Harvey et al. 1984),
including thirst and starvation (Freeman et al. 1980, Scott et al. 1982),
pollution (Holmes and Gorsline 1980), weather and temperature (Brown
and Nestor 1973, Wingfield 1988), capture, handling and immobilization
(Edens and Siegel 1975; Wingfield et al. 1982; Wingfield et al. 1992) and
social stress (Gross and Siegel 1973, Satterlee et al. 1982).
Much of the current data on avian B profiles has been obtained from
studies involving domesticated species or from wild species maintained
in captivity (see references above). Data obtained from such studies are
presumed to be similar to those which would be obtained from birds in
’ Museum of Natural Science, 119 Foster Hall, Louisiana State Univ., Baton Rouge, Louisiana 70803.
Present address: Dept. of Biological Sciences, Dartmouth College, Hanover, New Hampshire 03755.
2 Dept. of Zoology and Physiology, Louisiana State Univ., Baton Rouge, Louisiana 70803.
3 Present address: Smithkline Beecham, Swedeland Rd., King of Prussia, Pennsylvania 19406.
4 Present address: Depts. of Veterinary Physiology, Pharmacology and Toxicology, School of Veterinary
Medicine, Louisiana State Univ., Baton Rouge, Louisiana 70803.
296
Marra et al. * CORTICOSTERONE LEVELS IN
ZONOTRICHZA
297
nature. Since confinement itself or exposure to humans may be a stressor
which might elevate B concentrations (Suarez and Gallup 1982, Hem-
sworth and Barnett 1989), especially in wild birds, the validity of these
extrapolations needs to be tested. Determination of basal B levels is im-
portant in order to evaluate properly stress induced increases of B as well
as for interspecific comparisons. Our first objective was to determine the
basal B profiles of two species of sparrows (genus Zonotrichia) under
natural conditions and compare these levels to birds acclimatized to cap-
tivity.
Seasonal variations in the recurring daily secretory profile of B have
been observed in at least two avian species, the White-throated Sparrow
(Z. albicollis) (Dusseau and Meier 1971) and the Garden Warbler (Sylvia
borin) (Schwab1 et al. 1991). Based on Dusseau and Meier’s (1971) find-
ings, Meier and Fivizzani (1975) proposed that the daily variations in B
concentration occurring in different seasons reflects the dynamics of neu-
roendocrine mechanisms which directly control various aspects of sea-
sonality in migratory birds, including premigratory fattening, migratory
readiness, and breeding condition. Meier’s hypothesis is supported pri-
marily by studies of White-throated Sparrows maintained under captive
conditions. In a similar study of the closely related White-crowned Spar-
row (Z. leucophrys), Vleck et al. (1980) did not detect a recurring daily
variation of B concentration. Thus, the second objective of our study was
to compare the daily secretory profiles of B of these two congeners.
METHODS
White-throated Sparrows were mist-netted near Baton Rouge, Louisiana, on 24 and 25
January 1987 and placed in an outdoor aviary at Louisiana State University, Baton Rouge.
White-crowned Sparrows were mist-netted near Charlotte, Texas, between 31 January and
2 February 1987, transported to Baton Rouge on 2 February, and placed in separate sections
of the aviary housing the White-throated Sparrows. Both species were residing on their
wintering grounds when captured. The outdoor aviaries in which the captive sparrows were
maintained measured 6 X 4 X 4 m and were exposed to the natural local climate and
photoperiod. At no time were birds exposed to any direct artificial lighting. Each enclosure
held approximately 15 birds and contained numerous perches and abundant cover. A total
of approximately 60 birds of each species were held in captivity for these experiments.
During the acclimation period the aviary was entered only briefly once every three days to
replenish food and water supplies. Water and a commercial bird seed (millet, sunflower
seeds, corn mash) were provided ad libitum on the floor of the cage.
All birds were maintained under these conditions for approximately 35 days prior to
having blood drawn for B assay (30-35 days is often used as an acclimation period prior
to sampling captive wild birds). Blood samples were collected from captive White-throated
Sparrows between 4 and 6 March and captive White-crowned Sparrows between 10 and 16
March. On each day, blood samples were collected from birds during six l-h time periods
(02:0&03:00, 06:00-07:00, 10:00-l l:OO, 14:00-15:00, 18:00-19:00, and 22:00-23:OO). In-
dividual birds were selected for blood collection by allowing a few individuals from a larger
298
THE WILSON BULLETIN
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Vol.
107, No. 2, June 1995
group of birds to disperse passively to unoccupied sections of the aviary where they were
netted. Generally, only two birds were sampled during each of the one-hour time periods
per day, and sampling was done in more than one of the periods per day. This procedure
permitted us to cause only minimal disturbance to the main group of birds and to the target
bird prior to sampling blood. No bird was sampled more than once, and only those blood
samples which were obtained within 60 set of our initial effort to net a bird were assayed
for B. Using only samples withdrawn during the initial 60 set ensures that blood B levels
do not reflect the stress of capture and handling associated with the blood sampling pro-
cedure (Wingfield et al. 1982, Schwab1 et al. 1991). Blood was drawn by heart puncture,
placed in heparinized tubes and kept on ice until plasma isolation.
For both species, blood samples were obtained from free-living birds at the same location
where captive birds had been previously captured. Samples were collected during four one-
hour time periods, beginning at first light and ending at dark (06:00-07:00, 10:00-l l:OO,
14:00-
1.5:00,
18:00-l 9:OO). Free-living White-throated Sparrows were collected between 25
February and 4 March and free-living White-crowned Sparrows between 7 and 9 March
1987. Individuals were collected from wintering flocks using .410 or .22 gauge bird shot.
All possible efforts were taken to minimize disturbing birds while approaching flocks prior
to collection and only one bird was collected in a particular flock per day to insure no
residual stress from our prior disturbance. Blood samples were obtained by heart puncture
within 60 set of downing a bird, placed in heparinized tubes, and kept on ice until isolating
and freezing plasma (within 2 h of collection). Birds were sexed by inspection of gonads
and were deposited as specimens in the Louisiana State Univ. Museum of Natural Science.
Plasma was isolated from whole blood by centrifugation (10,000 X g for 60 set), decanted
and frozen at -20°C until assayed for B. The B concentration of each sample was deter-
mined by a single batch radioimmunoassay (Satterlee et al. 1980). For assay protocol, sen-
sitivity, extraction efficiency, and specific-binding properties see Satterlee et al. (1980).
Statistical comparisons were made by ANOVA or Student’s t-test,
RESULTS
The concentration of B ranged from 4.2 k 1.3 ng/ml (mean t SE)
(06:OO h, N = 6) to 9.5 k 2.4 ng/ml (18:OO h, N = 7) in free-living
White-throated Sparrows and from 13.8 k 5.3 ng/ml (06:OO h, N = 6)
to 3 1.3 + 8.4 ng/ml (02:OO h, N = 6) in captive White-throated Sparrows
(Fig. 1). In White-crowned Sparrows the plasma B concentrations ranged
from 0.6 k 0.2 ng/ml (14:00 h, N = 6) to 1.6 + 1 .O ng/ml (06:OO h, N
= 7) in free-living birds and 3.1 2 1 .l ng/ml (18:00 h, N = 6) to 6.3
+- 2.5 ng/ml (06:OO h, N = 6) in captives (Fig. 1 b). Despite variations,
there were no significant differences in B levels among time periods for
either captive (F5,30 =
1.039,
P <
0.50) or free (F3,** = 1.1044,
P >
0.50)
FIG. 1. Corticosterone (B) concentration (means and SE) by time of day for free-living
and captive White-throated Sparrows and White-crowned Sparrows. Each point represents
a sample of six individuals (except 10:00 and 18:OO in captive White-throated Sparrows, N
= 7; and 06:OO and IO:00 in captive White-crowned Sparrows, N = 7). Note different scales
on the y-axis.
Marra et al.
l
CORTICOSTERONE LEVELS IN
ZONOTRICHIA
299
WHITE-THROATED SPARROWS
I
0 !
I
I
I
I
I I
0600 1000
1400 1800 2200
0200
10 ,
6-
6-
4-
2-
WHITE-CROWNED SPARROWS
0600 1000 1400
1800
2200 0200
TIME OF DAY
300
THE WILSON BULLETIN
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Vol.
107, No. 2, June 199.5
TABLE
1
DAILY MEAN CORTICOSTERONE (NC/ML) FOR CAPTIVE AND FREE-LIVING WHITE-THROATED
AND WHITE-CROWNED SPARROWS (N = SAMPLE SIZE)
spcc,es
White-throated Sparrow
White-crowned Sparrow
FIee-l,Vlllg
Captive
mean k
SE mean t SE
6.68 t 1.0 16.45 2 2.9
N = 26 N = 24
1.16 -+ 0.3 4.93 f 1.0
N = 26 N = 24
“Species dlffered significantly
under both treatments
both between and withm specie\,
P < 0.001, t-test.
White-throated Sparrows, or captive (F5,29 = 0.336,
P >
0.75) or free
(FXZ
= 0.5275,
P <
0.75) White-crowned Sparrows when tested by
ANOVA. Furthermore there were no significant differences between B
concentrations of males and females of either species.
Mean plasma B concentrations differed significantly between captive
and free-living birds of the same species at most sampling times (Fig. 1)
(t-test;
P <
0.05). Corresponding values differed between captive and
free-living birds, on average, by 260% for White-throated Sparrows and
by 460% for White-crowned Sparrows (Fig. I). A single daily-mean plas-
ma B concentration was calculated for each experimental group by taking
the mean of all values obtained between 06:OO and 18:O0. B values from
the 22:00-23:00 and 02:00-03:OO sample periods were not included in
the daily-mean B concentration for captive birds since these comparable
values were not available for free-living birds. The daily-mean B con-
centration was 250% and 430% greater in captive White-throated and
White-crowned Sparrows than in their respective free-living counterparts
(Table 1) (White-throated Sparrows, T = 3.20,
P <
0.003; White-crowned
Sparrows, T = 3.75,
P <
0.0008).
Interspecific differences in daily-mean B concentration between these
closely related congeners were also significant (Table 1). The daily-mean
B concentration in free-living White-throated Sparrows was 580% greater
than in free-living White-crowned Sparrows (T = 3.64,
P <
0.0009), and
330% greater in captive White-throated Sparrows than in captive White-
crowned Sparrows (T = 5.37,
P <
0.00002).
DISCUSSION
Recurring daily variations in plasma B concentration have been de-
tected in four domesticated species: Turkey (Meleagris
gaZlopavo;
Davis
and Siopes 1988), Japanese Quail (Coturnix
coturnix;
Boissin and Assen-
macher 1970, Assenmacher and Boissin 1972), Rock Dove
(Columba
Marra
et al.
l
CORTICOSTERONE LEVELS IN
ZONOTRICHIA
301
livia;
Joseph and Meier 1973), and Domestic Fowl
(Gallus domesticus;
Webb and Mashaly 1985, Lauber et al. 1987). Similar variation was de-
tected in two wild species maintained in captivity, White-throated Spar-
row (Dusseau and Meier 1971, Meier and Fivizzani 1975) and Garden
Warbler (Schwab1 et al. 1991), but was not present in another wild spe-
cies, the White-crowned Sparrow (Vleck et al. 1980). The occurrence of
daily variations in plasma B levels in some species poses a problem for
investigators if the levels of B are not consistently assessed at the same
phase of the daily secretory profile. Furthermore, the fact that a daily
variation of B concentration occurs in some species and is absent in others
raises questions regarding the physiological significance of such hormone
cycles. The period of the annual cycle also needs to be considered. We
examined B levels at only one stage of the annual cycle which could very
well explain our lack of significance.
Total plasma B concentration, as measured in the present study, in-
cludes B which is protein-bound and the bioactive fraction which is not
protein-bound. It is possible that the plasma concentration of bioactive B
could vary somewhat independently of the total plasma B concentration.
However, Meier et al. (1978) examined this possibility in captive White-
throated Sparrows and found that both total and bound plasma B varied
similarly during the day. A close correlation between changes in plasma
B level and relative concentration of protein-bound B has been observed
in other species as well (Siegel et al. 1976, Kovacs and PCczely 1983).
Significant daily variations of plasma B concentrations were not de-
tected in captive sparrows of either species in this study. This observation
is in accord with the findings of Vleck et al. (1980) for captive White-
crowned Sparrows. However, our data are suggestive of a daily variation
in B for both species.
At present, the cause of the differences of B concentration between
captive and free-living birds of both species is unknown. To minimize
external factors that might contribute to differences in B levels, we ex-
amined B concentrations in each experimental group of birds at the same
times of day, and at the same time of year. Furthermore, free-living and
captive birds of each species were sampled from the same locations.
Despite these precautions, we found highly significant differences in
plasma B concentrations between captive and free-living birds for both
species. This overall difference between captive and free-living birds is
most likely due to increased ACTH release, possible due to a decreased
level of B-feedback on corticotropin releasing factor (CRF) or increased
adrenal sensitivity to ACTH, perhaps due to captive stress. Sustained
differences in adrenal sensitivity to ACTH have been demonstrated in
populations of chickens (Edens and Siegel 1975, Siegel 1973).
302
THE WILSON BULLETIN
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Vol.
107, No. 2, June IY95
The differences in daily-mean B concentration between captive and
free-living birds of the same species were especially surprising, given the
length of the acclimation period. Wingfield et al.
(1982)
demonstrated a
decrease in B levels after an acclimation period of two to three weeks for
White-crowned Sparrows kept in small cages with one, two, or three
individuals per cage. Our data suggest that our captive birds never fully
“acclimated.” In addition to the artificial stress imposed, there may have
been additional social stressors of being in a confined space with other
individuals. It is also possible that there was a residual stress effect from
prior disturbances in the aviary, although we tried to minimize these as
much as possible. Also, despite efforts to cause minimal disturbance, we
may have induced some stress response during the sampling periods. One
other possible explanation for the high B concentrations in “acclimated”
birds may be change in diet. However, we don’t believe that this was the
case since seeds are the primary food for these sparrows in winter. There
is no evidence to suggest that B concentrations are altered after subtle
changes in diet. Furthermore, we did not observe any overt behavioral or
physiological adversity in either species during the study period.
Although B concentrations were significantly different between captive
and free-living birds, it is difficult to assess the biological significance of
these differences in magnitude. Studies investigating the response of B to
natural stressors in the wild and the potential impact that these resulting
elevated B levels have on general fitness are long overdue.
The significant difference in B levels between these two congeners was
unexpected. Both species are comparable in size, occupy similar habitats,
and seem to exhibit similar behaviors while on the wintering grounds (I?
P Marra, pers. obs.). Furthermore, all birds were sampled at the same
time of year at similar latitudes, and sample populations in both cases
consisted of nearly equal numbers of male and female birds. Also, al-
though we detected a species difference in the magnitude of increase in
B levels owing to captivity, it seems unlikely that the difference found
between free-living White-throated and White-crowned sparrows is
“stress-related,” unless these two species are continually subject to dif-
ferent degrees of stress in the wild. It is possible that the interspecific
differences in B concentration reflect differences between the metabolic
states of these species, perhaps caused by differences in habitat use, food
availability, or reproductive readiness.
Given the dissimilarities among the daily profiles of B in the four
experimental groups of birds examined, it seems unlikely that a particular
secretory profile of plasma B serves a central role in determining the
seasonal condition of these birds, at least at this phase of the annual cycle.
This does not mean that a die1 rhythm of B and other neurotransmitters
Murra et al. * CORTICOSTERONE LEVELS IN
ZONOTRICHIA
303
is not involved in establishing seasonality in birds. It is possible that a
die1 rhythm of plasma B is prominent at other phases of the annual cycle.
Seasonal variations in plasma B levels have indeed been observed in
several species (Meier and Fivizzani 1975, Wingfield et al. 1982, Hissa
et al. 1983, Meier and Russo 1984, Wingfield 1985, Rehder et al. 1986).
To our knowledge, this is the first study in which daily profiles of
plasma B have been compared between congeners, directly between birds
in the wild and those maintained in captivity. Our results indicate signif-
icant differences not only between captive and free-living individuals
within a species but also between congeners. Therefore, we suggest that
extrapolations concerning B data be made with extreme caution. Further-
more, despite the lack of a significant daily variation of concentration,
plasma B concentrations should be assessed, either at the same time or
during predetermined times of day.
ACKNOWLEDGMENTS
The Frank M. Chapman Fund of the American Museum of Natural History funded this
research. We thank Charles Schweppe for use of his property in Texas to conduct this study.
A. H. Meier, J. V. Remsen, and D. Satterlee provided advice and use of their labs. Thanks
to S. Cardiff and D. Dittman for help in collecting blood samples in Texas. This manuscript
was improved by comments from S. Baird, R. Holberton, R. T. Holmes, J. I. Lovette, R. C.
McClung, A. M. Perrault, C. M. Vleck, J. C. Wingfield, and one anonymous reviewer.
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