Comparative Biochemistry and Physiology Part A 125 (2000) 317 – 324
www.elsevier.com/locate/cbpa
Effects of capture on adrenal steroid and vasopressin
concentrations in free-ranging bottlenose dolphins
(Tursiops truncatus)
Rudy M. Ortiz *, Graham A.J. Worthy
Department of Marine Biology, Physiological Ecology and Bioenergetics Lab, Texas A&M Uni6ersity at Gal6eston, Gal6eston,
TX 77551, USA
Received 6 June 1999; received in revised form 8 December 1999; accepted 20 December 1999
Abstract
Marine mammals are routinely caught in the wild in an effort to monitor their health. However, capture-associated
stress could potentially bias various biochemical parameters used to monitor the health of these wild caught animals.
Therefore, the effects of capture were quantified by measuring plasma adrenal steroids and arginine vasopressin (AVP)
in free-ranging bottlenose dolphins (Tursiops truncatus) (n= 31). Total capture and restraint times were also correlated
to hormone concentrations to quantify the effects of capture. Significant, positive correlations between corticosterone
and cortisol (R= 0.752; P B0.0001), and between corticosterone and aldosterone (R = 0.441; P= 0.045) were demonstrated. Significant correlations between capture and restraint time and hormone levels were not observed. Animals
restrained for less than 20 min exhibited hormone levels similar to those for animals restrained for more than 20 min.
The positive correlations among the adrenal steroids suggest that release of these steroids was stimulated by adrenocorticotropin (ACTH). The lack of a correlation between cortisol and AVP indicates that AVP did not influence
ACTH-induced cortisol release in this situation. The study suggests that (1) a typical hypothalamic-pituitary-adrenal axis
is present in these animals, and (2) the relatively short capture and restraint times did not induce a significant
neuroendocrine stress response. © 2000 Elsevier Science Inc. All rights reserved.
Keywords: AVP; Aldosterone; Cortisol; Corticosterone; Glucocorticoids; Marine mammals; Stress
1. Introduction
Free-ranging animals are routinely captured in
order to monitor the health status of that particu-
* Corresponding author. Present address: Department of
Biology, A316 Earth & Marine Sciences, UC-Santa Cruz,
Santa Cruz, CA 95064, USA. Tel.: + 1-831-4594133; fax:
+1-831-4595353.
E-mail address: [email protected] (R.M. Ortiz)
lar population as well as for research purposes
(O’Shea and Rathbun, 1985; Scott et al., 1990;
Ortiz and Worthy, 1993; Hansen and Wells,
1996). Assessing the condition of animals in the
wild and their use in research is, undoubtedly, of
great importance for properly managing their
populations, especially if the species is endangered
(Marsh and Anderson, 1983). However, the capture of free-ranging animals could potentially induce a stress response, which may bias some
results. Although difficult to define, certain behav-
1095-6433/00/$ - see front matter © 2000 Elsevier Science Inc. All rights reserved.
PII: S 1 0 9 5 - 6 4 3 3 ( 0 0 ) 0 0 1 5 8 - 6
318
R.M. Ortiz, G.A.J. Worthy / Comparati6e Biochemistry and Physiology, Part A 125 (2000) 317–324
iors or physiological responses may be used to
provide some indication of stress, such as excessive movement (Vingerhoets et al., 1996) or increased glucocorticoids (Axelrod and Reisine,
1984). However, data quantifying the physiological effects of capturing free-ranging marine mammals is limited, which necessitates further
evaluations of stress-related parameters to provide
better indications of such activities on these
animals.
From a physiological perspective, physical
stressors stimulate the hypothalamic-pituitaryadrenal (HPA) axis resulting in elevated adrenal
steroids such as cortisol, corticosterone and aldosterone (Sakellaris and Vernikos-Danellis, 1975;
Axelrod and Reisine, 1984; Vingerhoets et al.,
1996). In mammals, the hypothalamic peptide,
corticotropin release factor (CRF), stimulates the
release of the pituitary derived protein, adrenocorticotropin (ACTH), which in turn induces the
secretion of adrenocorticoids (glucocorticoids and
mineralocorticoids) (Axelrod and Reisine, 1984;
McFarlane et al., 1995). However, ACTH secretion may also be stimulated by elevated vasopressin (AVP) during stressful conditions (Wade,
1984; McFarlane et al., 1995). In response to
stress, circulating glucose concentrations are increased due primarily to elevated glucocorticoids
(Tataranni et al., 1996). Alterations in ionic and
osmotic homeostasis in response to stress may
also be associated with the increased catabolic
activity induced by elevated glucocorticoids.
Aside from ACTH stimulation, aldosterone is
also released in response to decreased plasma
Na+ and Na+:K+ ratio via the renin-angiotensinaldosterone system (RAAS) (Morris, 1981). Although AVP and aldosterone contribute
significantly to osmoregulation in mammals, these
hormones, along with the glucocorticoids, may
provide a reliable index for assessing the possibility of capture-induced stress in free-ranging
animals.
Therefore, the present study was conducted to
examine the relationship among the concentrations of adrenal steroids and AVP in free-ranging
bottlenose dolphins (Tursiops truncatus) in an attempt to quantify the neuroendocrine response of
capture in these animals. The effects of capture
were also examined by quantifying the relationships between total capture time and restraint
time and hormone levels.
2. Materials and methods
2.1. Animals
Thirty-one (17 males, 14 females, 85–252 kg)
Atlantic bottlenose dolphins were captured off the
coast of Beaufort, North Carolina (34°45%N,
76°40%W). Free-ranging dolphins were captured
by net encirclement, and total capture and restraint times were recorded. For our purposes,
total capture time was the time from which the
net was first set to the time the blood sample was
taken, and restraint time was the time from which
the animal was first restrained to the time the
blood sample was taken. A heparinized blood
sample was collected from the flukes as previously
described (Scott et al., 1990; Hansen and Wells,
1996; St. Aubin et al., 1996). Samples were immediately placed on ice until they could be centrifuged, usually within two hours. Following
centrifugation, plasma was separated, placed in
cryovials, and frozen for later analysis.
2.2. Radioimmunoassays
Validations for all assays were conducted by
determining the percent recovery of cold hormone
from dolphin plasma pools and the degree of
parallelism of serially diluted pools. Vasopressin
levels were determined using a commercially available kit (Diagnostic Systems Laboratories, Inc.,
Webster, TX) with a modified extraction procedure. In brief, 0.5–0.8 ml of plasma was extracted
with 2 ml of chilled 98% ethanol, reconstituted
with 0.8 ml of phosphate buffer (pH 7.4), and
assayed in duplicate. An extraction efficiency of
75.2% was determined for this method, and final
concentrations corrected for the extraction efficiency. Recovery of cold AVP was 91.3% and
serially diluted samples were parallel to the standard curve. Samples were run in one assay with
an intra-assay % coefficient of variability B 8.3%.
Plasma aldosterone, cortisol, and corticosterone
were measured using commercially available kits
(aldosterone and cortisol from Diagnositc Products Corp., Los Angeles, CA, and corticosterone
from ICN, Costa Mesa, CA). Recovery of cold
aldosterone, cortisol, and corticosterone was 96.2,
94.4, and 95.5%, respectively. Serially diluted
samples for the three assays were parallel to the
standard curve. Intra- and inter-assay % coefficient of variability were B2.2% for aldosterone.
R.M. Ortiz, G.A.J. Worthy / Comparati6e Biochemistry and Physiology, Part A 125 (2000) 317–324
All samples analyzed for cortisol and corticosterone were completed in the same assay with an
intra-assay% coefficient of variability of 2.0% and
10.1%, respectively.
2.3. Electrolytes and osmolality
Electrolyte concentrations were previously reported (Hansen and Wells, 1996). Plasma osmolality was determined using a vapor pressure
osmometer (Fiske, Norwood, MA). Glucose was
measured using a clinical auto-analyzer (Roche
Diagnostics, Somerville, NJ).
2.4. Statistics
Correlations were determined using a simple
regression to determine the equation of the line
and a Fisher’s R to Z-test to determine the significance of the relationship (P B0.05). The effect of
time on measured concentrations was examined
by (1) using the mean restraint time and mean
capture time as a grouping index (i.e. restraint
time groups: B 20 min vs. \20 min and total
capture time groups: B 36 min and \ 36 min),
and (2) comparing concentrations from animals in
the first 25% of times to those in the last 25% of
times. All statistical tests were performed using
StatView for the Macintosh (Abacus Concepts,
1992).
3. Results
Values for all samples for a particular parameter were averaged to determine a mean for the
319
population since gender and body mass effects
were not observed. All plasma parameters are
summarized in Table 1.
In some instances, the plasma volume was insufficient to complete all analyses as indicated by
a sample size less than 31. Significant and positive
correlations between cortisol and corticosterone
(R= 0.752; PB 0.0001), and between corticosterone and aldosterone (R= 0.441; P = 0.0452)
were demonstrated (Fig. 1). Although not significant at PB 0.05, cortisol and aldosterone demonstrated a positive correlation as well (Fig. 1).
Glucocorticoids and glucose, aldosterone and
Na+ and Na+:K+ ratio, cortisol and AVP, and
AVP and plasma osmolality all did not exhibit
significant correlations (P\ 0.10).
Neither total capture time nor restraint time
was correlated with any of the measured parameters. Blood parameters from animals with restraint times B 20 min were similar to those from
animals with restraint times \ 20 min (Table 2).
The same was observed for animals with total
capture times B 36 min and total capture times
\36 min (Table 2). Blood parameters from animals in the first quarter of restraint and total
capture times were similar to those from animals
in the last quarter of times (Table 3).
4. Discussion
Physical stressors have been shown to stimulate
the HPA axis resulting in elevated plasma concentrations of gluco- and mineralocorticoids (Axelrod and Reisine, 1984). The positive correlations
among the adrenocorticoids in the present study
Table 1
Plasma constituents from free-ranging bottlenose dolphins caught off the coast of Beaufort, NC
Plasma constituent
n
Mean
9S.D.
Range
AVP (pg/ml)
Aldosterone (pg/ml)
Cortisol (F) (mg/dl)
Corticosterone (B) (ng/ml)
F:B (mg/mg)
Osmolality (mOsm/l)
Na+ (mmol/l)a
K+ (mmol/l)a
Na+:K+ (mmol/mmol)
Glucose (mg/dl)
28
30
31
22
22
31
31
31
31
22
3.3
234
2.8
7.4
4.7
341
154
4.1
37.5
94
0.6
134
1.0
4.7
1.8
9
3.2
0.2
2.3
22.4
2.3–5.1
25–456
1.0–5.6
2.1–17.7
2.1–9.4
324–366
148–161
3.7–4.6
33.6–43.2
61–135
a
Values obtained from Hansen and Wells (1996). ‘n’ refers to a single measurement for a single dolphin with a maximum of 31. AVP,
vasopressin.
320
R.M. Ortiz, G.A.J. Worthy / Comparati6e Biochemistry and Physiology, Part A 125 (2000) 317–324
Fig. 1. Correlations among plasma adrenal steroids from free-ranging bottlenose dolphins caught off the coast of Beaufort, NC. Top,
Cortisol versus Corticosterone, Middle: Corticosterone versus Aldosterone, Bottom: Cortisol versus Aldosterone. Correlations were
significant at P B 0.05.
R.M. Ortiz, G.A.J. Worthy / Comparati6e Biochemistry and Physiology, Part A 125 (2000) 317–324
321
Table 2
Comparisons of plasma parameters (mean 9 SEM) for dolphins between restraint times B versus \20 min and between total capture
times B versus \36 min
Restraint timea (min)
B20
n
AVP (pg/ml)
Aldosterone (pg/ml)
Cortisol (mg/dl)
Corticosterone (ng/ml)
Osmolality (mOsm/l)
Na+ (mmol/l)
K+ (mmol/l)
Na+:K+ (mmol/mmol)
Glucose (mg/dl)
17
3.2 9 0.1
228.3 937.8
2.8 9 0.2
6.89 1.2
344.39 2.0
154.6 9 0.9
4.1 9 0.1
37.59 0.6
86.6 9 4.9
Total capture time (min)
\20
11
3.6 90.2
252.7 937.1
2.9 90.3
9.2 92.0
338.1 92.6
154.5 90.8
4.1 9 0.1
37.9 9 0.6
97.8 9 7.6
B36
19
3.2 9 0.1
253.5 9 32.7
2.9 90.2
7.5 9 1.2
343.8 9 1.8
154.5 9 0.8
4.2 90.1
37.2 9 0.6
87.79 4.4
\36
12
3.590.2
199.8935.3
2.790.3
7.292.0
337.79 2.7
154.390.8
4.19 0.1
37.990.6
103.5910.1
a
Restraint times were not available for three animals resulting in a sample size of 28. No significant differences were detected within
each time group. AVP, vasopressin.
Table 3
Comparisons of plasma parameters (mean 9 SEM) for dolphins between the first quarter versus the last quarter of restraint times and
total capture times
Restraint timea
first 25%
n
Time (min)
AVP (pg/ml)
Aldosterone (pg/ml)
Cortisol (mg/dl)
Corticosterone (ng/ml)
Osmolality (mOsm/l)
Na+ (mmol/l)
K+ (mmol/l)
Na+:K+
Glucose (mg/dl)
8
10.690.9
3.29 0.2
200.49 63.2
2.59 0.3
5.49 1.0
347.29 3.1
155.19 1.2
4.2 90.1
36.790.7
91.995.6
Total capture timeb
last 25%
8
32.0 9 4.2
3.3 90.2
240.9 935.3
2.5 9 0.2
7.1 91.9
339.2 93.1
153.9 90.5
4.1 9 0.1
38.0 9 0.7
87.6 97.8
first 25%
8
23.59 1.3
3.0 90.2
307.9 960.4
2.6 90.2
7.8 9 1.9
347.893.1
155.49 1.2
4.19 0.1
38.1 9 0.7
81.0 97.3
last 25%
9
52.4 9 4.7
3.3 90.2
224.7 938.4
2.6 90.4
8.1 92.6
338.4 9 2.8
154.4 9 1.0
4.1 90.1
38.0 9 0.5
104.8 9 13.6
First and last quarter of restraint times were defined by B14 and \24 min, respectively.
First and last quarter of total capture times were defined by B27 and \41 min, respectively. No significant differences were
detected between first and last quarters within each time group. AVP, vasopressin.
a
b
suggest ACTH-induced stimulation of these
steroids. The fact that aldosterone was not correlated to plasma Na+ or to Na+:K+ ratio suggests
that this steroid was not stimulated by osmotic
effects at the time of sampling. The lack of a
correlation between cortisol and AVP suggests
that AVP did not influence ACTH release in this
situation.
Elevated serum aldosterone concentrations
have previously been shown in dolphins to be
correlated with increased blood sampling time
after capture (St. Aubin et al., 1996). However, in
the present study none of the reported blood
parameters were positively correlated with either
restraint time or total capture time. Also, the
restraint and total capture time schemes used in
the present study for comparative purposes did
not produce significant group differences for any
of the measured blood parameters suggesting that,
on the whole, the restraint and total capture times
in the present adequately abated a significant
neuroendocrine stress response. However, the correlations among the adrenal steroids suggest that
some animals may have exhibited a stress response. The correlations among the adrenal
steroids also suggest that ACTH-induced the
stimulation of these adrenocorticoids. Only 13%
of the animals whose measured concentrations
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R.M. Ortiz, G.A.J. Worthy / Comparati6e Biochemistry and Physiology, Part A 125 (2000) 317–324
represented the upper ends of the correlation
curves had higher levels than those reported for
semidomesticated dolphins (St. Aubin et al.,
1996). The lack of a correlation between either
glucocorticoid and glucose further suggests the
absence of an acute capture stress response within
the time frame of the captures in the present
study. Glucose concentrations measured in the
present study are similar to those previously reported for ‘unstressed’ captive dolphins (Thomson
and Geraci, 1986) and West Indian manatees
(Trichechus manatus) (O’Shea and Rathbun, 1985;
Ortiz et al., 1998). Collectively, the data suggest
that the dolphins in the present study did not
exhibit a significant neuroendocrine stress
response.
Although cortisol is the primary glucocorticoid
in most mammals, the presence of corticosterone
in adrenocortical tissue of pinnipeds (de Roos and
Bern, 1961; Sangalang and Freeman, 1976) and
cetaceans (Carballeira et al., 1987) has been detected. In plasma, corticosterone has been measured in pinnipeds by double isotope derivative
analysis (DIDA) (Sangalang and Freeman, 1976)
and by fluorometric analysis in cetaceans (Seal
and Doe, 1965). Previously reported (Seal and
Doe, 1965) plasma corticosterone in a bottlenose
dolphin (60 ng/ml) and a fin whale (Balenoptera
physalus) (21 ng/ml) are approx. eight- and threefold greater, respectively, than that of the mean in
the present study. This discrepancy in values may
reflect a difference in analytical techniques and
does not necessarily reflect the releasable pool in
bottlenose dolphins. A cortisol:corticosterone ratio of 5:1 in bottlenose dolphins has previously
been reported (Thomson and Geraci, 1986), which
is consistent with the mean ratio (4.7) measured in
the present study.
Along with elevated glucocorticoids, increasing
aldosterone concentrations could also be an indicator of a possible stress response. An increasing
trend in aldosterone levels as a function of time
following capture has been shown in dolphins (St.
Aubin et al., 1996). In manatees, a significant
increase in plasma aldosterone in response to oral
intubation was observed (Ortiz et al., 1998). However, a majority (97%) of the measurements in the
present study, as with cortisol, was within the
previously reported range, in which the authors
concluded that the captured dolphins did not
elicit signs of distress (St. Aubin et al., 1996).
Although ionic stimulation of aldosterone release
has been demonstrated in marine mammals (Ortiz
et al., 1998), the lack of a correlation between
plasma aldosterone and Na+ in the present study
suggests that the observed range of aldosterone
concentrations were not ionically induced at the
time of sampling.
The fact that plasma Na+ and aldosterone were
not correlated may not be surprising since Na+ is
generally maintained within a narrow range indicating its tight regulation under homeostatic conditions (Morris, 1981). However, during stressful
conditions, osmotic and ionic homeostasis can be
disrupted due largely to an increased catabolic
state resulting from elevated glucocorticoids
(Watlington et al., 1988). For example, serum K+
concentrations in dugongs (Dugong dugon) doubled within 20 min of capture which the authors
suggested was the result of capture myopathy (or
capture stress) (Marsh and Anderson, 1983). Indices of capture stress such as elevated K+, creatinine, glucose, urea, and various liver enzymes
measured in blood samples taken approximately
one hour after capture were not different between
wild and captive West Indian manatees (O’Shea
and Rathbun, 1985). Electrolytes and Na+:K+
ratio in the present study are similar to those
previously reported for captive (Thomson and
Geraci, 1986) and free-ranging dolphins (Ortiz
and Worthy, 1993) and captive and free-ranging
manatees (O’Shea and Rathbun, 1985; Ortiz et al.,
1998). Therefore, the narrow ranges in plasma
osmolality, Na+, K+, and Na+:K+ ratio observed in the present study as well as their similarity to other marine mammals indicate a state of
ionic and osmotic homeostasis and a lack of
capture stress.
The contribution of AVP to the observed correlations among the adrenal steroids is difficult to
discern from the data. In mammals, CRF alone,
but not AVP alone has been shown to stimulate
ACTH release (McFarlane et al., 1995), therefore
the lack of a correlation between AVP and cortisol in the present study suggests that AVP was
not likely involved in the release of ACTH. Osmotic stimulation of AVP in marine mammals has
been suggested (Skog and Folkow, 1994; Ortiz et
al., 1998), however the lack of a correlation between AVP and plasma osmolality suggests that
AVP release within the blood sampling time
frame in the present study was not osmotically
stimulated. The observed concentrations of AVP
are similar to those previously reported for other
R.M. Ortiz, G.A.J. Worthy / Comparati6e Biochemistry and Physiology, Part A 125 (2000) 317–324
free-ranging dolphins (Ortiz and Worthy, 1993),
pinnipeds (Ortiz et al., 1996; Zenteno-Savin and
Castellini, 1998) and manatees (Ortiz et al., 1998).
In conclusion, the lack of correlations between
restraint and total capture times and the measured
plasma parameters suggest that the capture times
in the present study did not induce significant
changes in the measured parameters. Also, the
correlations among the adrenocortical steroids
suggest that the HPA axis is functional in bottlenose dolphins and responds in a manner similar
to terrestrial mammals. Although the release of
these steroids was likely induced by ACTH, the
concentrations of these adrenocorticoids suggest
that within the sampling time frame of the present
study, the majority of dolphins did not exhibit a
significant neuroendocrine stress response. The
lack of a glucocorticoid-glucose correlation and
the maintenance of osmotic and ionic homeostasis
further suggest a lack of a physiological stress
response to capture within the present time of
capture. Although data on corticosterone concentrations are limited for marine mammals, corticosterone concentrations may provide another
parameter by which to evaluate the role of the
adrenal gland in marine mammals under varying
physiological conditions. The contribution of
AVP to the HPA axis warrants further investigation. Therefore, it would appear that blood sampling within 40 min of the initiation of capture of
free-ranging bottlenose dolphins does not induce
a physiological stress response, which in turn
should not bias other physiological studies of
these animals in the wild.
Acknowledgements
Authors wish to thank L. Hansen and H.
Rhinehart for providing plasma samples. We
thank Dr C.E. Wade for his review of a draft of
this manuscript. Captures were conducted under
N.M.F.S. permits to LH.
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