Increased blubber cortisol in ice-entrapped beluga whales (Delphinapterus leucas)

Abstract

Entrapments of whales in sea ice occur occasionally in the Arctic and often last several weeks or months, resulting in emaciation or death of whales. These events provide a unique opportunity for investigating the physiological response to a prolonged or chronic stress in an otherwise healthy population of marine mammals. By measuring cortisol in blubber, a peripheral tissue, we expect to see a reflection of long-term or chronic stress rather than short-term or acute stress. Adipose tissue should be less subject to rapid changes compared to blood cortisol, reflecting stressors experienced over a longer period of time, and should not be affected by potential stress associated with sampling. We measured blubber cortisol of 29 beluga whales (Delphinapterus
leucas) entrapped in November 2006 in Husky Lakes basin and 26 whales from the same population (Eastern Beaufort Sea) during regular seasonal harvests in July of 2006 and 2007. Mean cortisol concentrations (±SEM) were seven times higher in blubber from entrapped whales (1.76 ± 0.32 ng/g wet weight) compared to whales from regular seasonal harvests (0.26 ± 0.042 ng/g wet weight) and appeared to increase with whale age. Our results provide a measure of blubber cortisol from a prolonged stress and demonstrate blubber cortisol as a useful indicator of longer-term exposure to stress in beluga whales.

Full text

ORIGINAL PAPER
Increased blubber cortisol in ice-entrapped beluga whales
(Delphinapterus leucas)
Marci R. Trana
1
•James D. Roth
1
•Gregg T. Tomy
2
•W. Gary Anderson
1
•
Steven H. Ferguson
1,3
Received: 7 April 2015 / Revised: 18 December 2015 / Accepted: 20 December 2015
ÓSpringer-Verlag Berlin Heidelberg 2015
Abstract Entrapments of whales in sea ice occur occa-
sionally in the Arctic and often last several weeks or
months, resulting in emaciation or death of whales. These
events provide a unique opportunity for investigating the
physiological response to a prolonged or chronic stress in
an otherwise healthy population of marine mammals. By
measuring cortisol in blubber, a peripheral tissue, we
expect to see a reflection of long-term or chronic stress
rather than short-term or acute stress. Adipose tissue should
be less subject to rapid changes compared to blood cortisol,
reflecting stressors experienced over a longer period of
time, and should not be affected by potential stress asso-
ciated with sampling. We measured blubber cortisol of 29
beluga whales (Delphinapterus leucas) entrapped in
November 2006 in Husky Lakes basin and 26 whales from
the same population (Eastern Beaufort Sea) during regular
seasonal harvests in July of 2006 and 2007. Mean cortisol
concentrations (±SEM) were seven times higher in blubber
from entrapped whales (1.76 ±0.32 ng/g wet weight)
compared to whales from regular seasonal harvests
(0.26 ±0.042 ng/g wet weight) and appeared to increase
with whale age. Our results provide a measure of blubber
cortisol from a prolonged stress and demonstrate blubber
cortisol as a useful indicator of longer-term exposure to
stress in beluga whales.
Keywords Delphinapterus leucas Glucocorticoid 
Steroid hormones Stress
Introduction
In the Arctic, seasonal fluctuations in sea ice create a
dynamic landscape where conditions change daily, espe-
cially during spring and fall when freeze-up and melt
occur. During the fall freeze-up, areas of open water close
gradually and occasionally quickly before freezing over
entirely and whales in these areas can become trapped,
unable to access open water (Weaver and Richard 1989;
Heide-Jørgensen et al. 2002; Laidre et al. 2012). Entrap-
ments are more likely in specific areas of the Arctic, such
as inlets, sounds, lakes and straits (Harwood 2007). These
areas are thought to attract whales because of abundant fish
and other prey (Weaver and Richard 1989). Entrapments
occur periodically and are considered a natural event
causing emaciation or death of arctic whales, particularly
monodontids (beluga and narwhal) (Weaver and Richard
1989; Heide-Jørgensen et al. 2002; Laidre et al. 2012).
Beluga whales (Delphinapterus leucas), whose distribution
is limited to the Arctic and Subarctic, are particularly
susceptible to entrapment events because they live in close
&James D. Roth
jim.roth@umanitoba.ca
Marci R. Trana
marcitrana@gmail.com
Gregg T. Tomy
gregg.tomy@umanitoba.ca
W. Gary Anderson
gary.anderson@umanitoba.ca
Steven H. Ferguson
steve.ferguson@dfo-mpo.gc.ca
1
Department of Biological Sciences, 50 Sifton Road,
University of Manitoba, Winnipeg, MB R3T 2N2, Canada
2
Department of Chemistry, 594 Parker Building, University of
Manitoba, Winnipeg, MB R3T 2N2, Canada
3
Fisheries and Oceans Canada, 501 University Crescent,
Winnipeg, MB R3T 2N6, Canada
123
Polar Biol
DOI 10.1007/s00300-015-1881-y

association with sea ice, using it for shelter and refuge from
predators (Huntington 1999; Heide-Jørgensen et al. 2013).
During stressful events (e.g., entrapments), a complex
neuroendocrine system present in all vertebrates stimulates
the release of a series of hormones causing an increase in
glucocorticoid (GC) hormones such as cortisol from the
adrenal gland, the primary GC in marine mammals (Oki
and Atkinson 2004). The release of GC hormones into the
circulation following exposure to short-term stressors is
considered beneficial for organisms (i.e., acute stress)
(Mo
¨stl and Palme 2002) and serves as a physiological
mechanism for mobilizing energy stores and triggering
behaviors that aid in escape or defense (Boonstra 2004).
However, if the stressor persists (i.e., chronic stress),
continued stimulus of the endocrine systems involved can
hinder vital functions, ultimately causing illness, decreased
reproduction and, in worst-case scenarios, death (Boonstra
et al. 1998; Boonstra 2005).
By measuring stress hormones in tissues that reflect
long-term exposure to stressors, it is possible to monitor
changes in the stress experienced by individuals over
prolonged time periods (Davenport et al. 2006; Bortolotti
et al. 2008; Saco et al. 2008; Okuliarova
´et al. 2010). In
pigs, plasma progesterone enters adipose tissue within
16–50 h following release (Hillbrand and Elsaesser 1983),
and other steroid hormones in vertebrates, like cortisol,
may also enter adipose tissue at a similar rate, where they
accumulate over a period of time (Mead 1963). In marine
mammals, collecting blood and saliva requires capture and
often reflects capture stress, while the collection of feces,
although noninvasive, is often difficult and samples can
become contaminated by seawater during collection
(Amaral 2010). Blubber can be collected non-lethally with
the use of remote biopsy and is unlikely to reflect imme-
diate stressors associated with collection (Kellar et al.
2006). Therefore, as with hair (Davenport et al. 2006;
Manenschijn et al. 2011) blubber may indicate whether
prolonged exposure to potential stressors is correlated with
increased blubber cortisol concentration. Factors such as
decreased food availability, social instability or other
environmental changes may be detectable in blubber cor-
tisol concentrations and provide an indication of overall
population health.
Entrapments generally occur over several weeks so we
can use samples collected from entrapped whales to show a
measure of prolonged stress. During entrapments, whales
experience separation from social groups and decreased
food availability, leading to emaciation. As the ice freezes
over, they become exposed to predation by humans and
polar bears until eventually access to the water surface for
breathing is reduced (Porsild 1918; Weaver and Richard
1989). Other than our previous methodological study
(Trana et al. 2015), only one measurement of cortisol from
cetacean blubber has been published, in which short-
beaked common dolphins, Delphinus delphis, exhibited
increased measures of cortisol during beach strandings
(Kellar et al. 2015). Identifying additional measures of
prolonged stress provides support for the use of blubber as
a measure of chronic stress that we can use for comparison
when examining the health of the beluga whale populations
across their range. Therefore, we examined differences in
blubber cortisol between beluga whales trapped in the ice
during freeze-up and beluga whales harvested during
annual subsistence hunts. Subsistence hunt practices of
marine mammals are regulated by several management
plans and agreements for both population sustainability and
humane treatment (Marine Mammal Regulations, SOR/93-
56), so we assume regular beluga harvest events to be
short-term stressors compared to ice entrapment events.
Blubber samples obtained for our study are from different
seasons, but season has been found to have little effect on
blubber cortisol of other marine species (Kellar et al. 2015)
so we assumed no effect of season in our sample group. We
also examined age and sex influences on cortisol from
trapped whales.
Materials and methods
Study area
Husky Lakes, in the northern portion of Northwest Terri-
tories, Canada, are the inner most inlets extending off
Liverpool Bay into the Beaufort Sea (Fig. 1). Some beluga
Fig. 1 Location of the 2006 beluga whale (Delphinapterus leucas)
entrapment, Eastern Beaufort Sea, Husky Lakes, Canada
Polar Biol
123

whales from the Eastern Beaufort Sea population enter
Liverpool Bay in late July or early August and may go
farther inland in some years, entering Husky Lakes (Hig-
don and Ferguson 2012). Beluga whales from this popu-
lation typically begin migrating west to the Bering Sea in
mid-August and early September, but occasionally whales
remain in various basins of Husky Lakes and become
trapped when their only exit to the Arctic Ocean freezes
over (Higdon and Ferguson 2012). In 2006, freeze-up in
Husky Lakes began in September, and 250 whales were
counted at the surface within the lakes during an aerial
survey on September 6th (Fisheries Joint Management
Commission 2008a). On November 14th, following seven
additional whale count surveys that documented the dete-
riorating condition of the whales, most of the original 250
whales were thought to have escaped, and management
actions were taken to cull the remaining 37 entrapped
whales, which were humanely harvested by the local
community between November 15 and 23. A survey the
following summer observed 8 additional whale carcasses
thought to be related to this event, but no samples were
collected (Fisheries Joint Management Commission
2008a).
Sample collection
Blubber samples were collected from whales culled during
the 2006 entrapment event in Husky Lakes immediately
following the humane harvest. Samples were also collected
during the seasonal subsistence harvest from the same
population (Eastern Beaufort Sea) in July of 2006 and
2007. The location on the body where blubber subsamples
were taken was not recorded for any whales used in this
study. Inuit have hunted beluga whales for human and dog
food for over 500 years in the Mackenzie River estuary
(Harwood et al. 2002). Each summer, contemporary hun-
ters from coastal communities hunt from small (ca 5 m
long) aluminum boats and typically harpoon the whale
prior to killing it with a rifle shot to the head or neck (C222
calibers). Hunt duration, from time of pursuit to death, is
regulated and designed to be as quick and humane as
possible (typically 1–2 h). All samples provided by hunters
were frozen and archived at Fisheries and Oceans Canada,
Winnipeg, Manitoba, in -40 °C freezers. A tooth was
extracted from each whale for aging based on one growth
layer group of dentine deposited annually (Luque et al.
2007). Our 1 g subsamples spanned all blubber layers,
from skin to muscle, to avoid variation in cortisol associ-
ated with blubber depth, and we selected samples without
any visible discoloration, which reflects sample degrada-
tion (Trana et al. 2015). We removed outer edges of all
blubber subsections to avoid potential contamination and
freeze-dried samples to remove water.
We extracted cortisol from blubber samples using a
modified version of the Kellar et al. (2006) method for
extracting blubber progesterone and then measured cortisol
concentrations using radioimmunoassay (Trana et al.
2015). We vortexed the freeze-dried blubber samples with
a series of solvent rinses starting with ethanol then acetone
followed by acetonitrile and finally hexane; this removed
cortisol from the lipid rich matrix (see Trana et al. 2015 for
complete details). The extracted sample was dissolved in a
radioimmunoassay (RIA) buffer at 250 lL aliquots/sample.
RIA buffer was composed of 10 mL phosphate buffer
[71.6 g Na
2
HPO
4
2H
2
O, 15.3 g NaH
2
PO
4
2H
2
in 1 L
milli-Q (ultrapure) water], 0.9 g NaCl, 0.5 g bovine serum
albumin and 90 mL milli-Q water. We then added titrated
cortisol (5000 disintegrations per minute) (PerkinElmer,
Waltham, Massachusetts, USA) and 1:3200 dilution of
cortisol antibody (Fitzgerald Industries, Acton, Mas-
sachusetts, product code 20-CR50) to the sample mixture.
According to the manufacturer, cross-reactivity of the
antibody used was 100 % for cortisol, 5.7 % for
11-deoxycortisol, 3.3 % for corticosterone, 36 % for
prednisolone and \0.7 % for cortisone. All assay compo-
nents were the same as those recently validated for mea-
surement of fecal glucocorticoid metabolites in
Richardson’s ground squirrels (Urocitellus richardsonii)
(Hare et al. 2014). After incubation, 100 lL of a charcoal–
dextran buffer solution (2.5 g charcoal, 0.25 g dextran in
50 mL RIA buffer) was added to the mixture. The super-
natant was decanted into scintillation vials mixed with
scintillation fluid (Ultima Gold, PerkinElmer, Waltham,
Massachusetts, USA) and counted for radioactivity for
5 min in a scintillation counter (Tri-Carb
Ò
3110TR, Perk-
inElmer Inc., Waltham, Massachusetts, USA). Each assay
contained a standard concentration curve measured in
triplicate of 10 concentrations ranging from 0.05 to
25 ng mL
-1
. Each sample was run in duplicate (Trana
et al. 2015). Method validation steps included assessing
inter-assay variation (14 %, n=22), intra-assay variation
(6 %, n=20), parallelism (see Trana et al. 2015, Fig. 2),
extraction efficiency (77 ±4 %; mean ±SEM) and sam-
ple quenching (less than 1 %) (Trana et al. 2015).
Data analysis
Statistical analyses were performed in JMP
Ò
10 (SAS
Institute Inc. 2012). Cortisol concentrations were log-
transformed to improve normality. We tested for differ-
ences in cortisol concentrations between the July 2006 and
July 2007 harvest using a ttest. Because our July subsis-
tence harvest samples did not contain any known females,
we tested for sex differences in entrapped whale cortisol
concentrations using a ttest. We then examined the effect
of source (entrapment vs subsistence harvest) and age on
Polar Biol
123

cortisol concentrations in both entrapment and seasonal
harvests using a general linear model. All cortisol values
are reported as mean ±standard error (ng/g of wet weight)
unless otherwise specified.
Results
We measured cortisol concentrations in 29 entrapped whales
(26 males and 3 females), 8 whales harvested in July 2006
(all unknown sex) and 18 whales harvested in July 2007 (12
males and 6 of unknown sex). Samples from the 2006 and
2007 subsistence harvests did not differ in cortisol concen-
tration (t
24
=-0.51, p=0.613), so these samples were
pooled for comparison with entrapped whales. Likewise,
cortisol concentrations did not differ between males
(1.68 ±0.33) and females (2.47 ±1.78) from the entrap-
ment (t
27
=0.39, p=0.697), but our sample size of
females was too low to make strong inferences about sex
differences. We found no interaction between whale age and
source (entrapment event or seasonal harvest; F
1,37
=1.68,
p=0.203), and the model with no interaction term was
highly significant (F
2,38
=13.13, p\0.0001, r
2
=0.408).
Cortisol concentrations in samples from the entrapment
event (1.76 ±0.32) were seven times higher than in samples
from the subsistence harvests (0.25 ±0.04; Fig. 2), and
cortisol appeared to increase with age of whales, but age was
nonsignificant (Fig. 3).
Discussion
The elevated blubber cortisol concentrations from whales
that had been trapped in the ice for over 2 months support
the use of blubber cortisol as an indicator of long-term
stress. While the time difference of exposure to a stressor
between a seasonal harvest event (minutes to hours) and a
gradual enclosure of an ice entrapment event (in this case,
two months) is obvious, we do not know when either event
first initiates the stress response that leads to the release of
cortisol. However, starvation and decreased access to water
surface for breathing are certain to be a perceived threat to
any marine mammal and would fit the definition of a
prolonged (chronic) exposure to stress (Busch and Hay-
ward 2009). Short-term stressors, lasting minutes, are less
likely to become incorporated into peripheral tissues and
are more likely to be regulated prior to peripheral tissue
incorporation through negative feedback regulation. These
feedback loops are thought to help optimize the benefits of
low GC levels and prevent the damage caused by high GC
levels (Busch and Hayward 2009). Additionally, the high
capacity for GC storage in adipose tissue and the slow
Fig. 2 Blubber cortisol concentrations for beluga whales (Delphi-
napterus leucas) from the Husky Lake entrapment in November 2006
(n=29) and Beaufort Sea subsistence harvests in July 2006 (n=18)
and 2007 (n=8). Data were pooled across sexes. Horizontal box
lines are the lower quartile, median and upper quartile values.
Whisker lines indicate the range of concentrations. Ice-entrapped
whales had a sevenfold higher concentration of blubber cortisol than
seasonally harvested whales (F
1,38
=19.85, p\0.0001)
Fig. 3 Cortisol concentrations (log-transformed ng/g wet weight)
plotted against age in years obtained from a single tooth cementum or
dentine growth layer group in male (circle) and female (diamond)
beluga whales (Delphinapterus leucas) from the Husky Lake
entrapment in November 2006 (n=29) and the Beaufort Sea
subsistence harvests in July 2006 (n=26). Cortisol appeared to
increase with age (b=0.0164), but age was nonsignificant
(F
1,38
=4.02, p=0.052)
Polar Biol
123

breakdown or release of cortisol from adipose compared to
blood indicate a longer window of physiological time
unaffected by rapid fluctuations observed in blood (Des-
lypere et al. 1985; Mead et al. 1986; Szymczak et al. 1998;
Galic et al. 2010). The exact mechanism and metabolism of
GCs in adipose tissue are largely unknown. The observed
body condition difference between the hunted whales and
the trapped whales indicates the added stress of starvation.
Cortisol is intended to modulate glucose levels and meta-
bolism so cortisol found in the blubber of entrapped whales
is likely a result of several systems all related to physio-
logical stress (e.g., nutritional stress, potential stress from
social changes and lowered access/competition for
breathing). Starvation is a physiologically stressful event so
body condition has been correlated with increased cortisol
(Macbeth et al. 2012).
The cortisol concentrations we measured in beluga
whale blubber are lower than concentrations obtained from
other cetaceans. Kellar et al. (2015) reported mean values
of 3.99 and 24.3 ng/g in blubber from bycatch and stranded
dolphins, respectively (a sixfold difference between
groups), and although our values were much lower in both
subsistence harvest and entrapped beluga whales (0.25 and
1.79 ng/g, respectively), the difference between groups
was similar (a sevenfold increase in entrapped whales).
Beluga whales have an extremely thick blubber layer that
plays an important role in thermoregulation. When mobi-
lizing energy stores from fat for migration, beluga use fat
surrounding their organs first, to maintain their thick
blubber layer (Brodie 1975; Luque and Ferguson 2009;
Hauser et al. 2014). This difference between monodontids
and other whales may play a role in the lower mean con-
centrations of cortisol in the blubber of beluga whales.
Indeed sampling within the blubber layer can vary in cor-
tisol concentrations (Trana et al. 2015).
Although our control samples were collected at a dif-
ferent time of year than the entrapped samples (July vs
November, respectively), the sevenfold difference in cor-
tisol was much higher than the seasonal differences in
plasma cortisol concentration found in stress-induced har-
bor seals (Gardiner and Hall 1997), suggesting seasonality
alone did not account for these differences. Seasonal
changes in the energetic demands of the environment and
changes in reproductive activity could potentially influence
GC concentrations, which are typically highest during the
breeding season in vertebrates (Romero 2002). If short-
term changes in cortisol levels are less likely in blubber
than in blood, then blubber cortisol levels may not differ
seasonally. In fact, in the only published study examining
seasonality in blubber cortisol, cortisol extracted from
blubber of stranded short-beaked common dolphins did not
vary seasonally (Kellar et al. 2015). Yet plasma cortisol
concentrations vary seasonally in many mammals (Romero
2002; Reeder and Kramer 2005; Romero et al. 2008) and
are often exaggerated in species at higher and lower lati-
tudes (Reeder and Kramer 2005). Regardless, beluga whale
breeding likely occurs in late winter–early spring (Kelley
et al. 2014), outside both sampling time frames in the
present study, so any effect of breeding on our cortisol
results is unlikely. Lastly, blood perfusion rates and
metabolism could differ seasonally due to water tempera-
ture differences (Irving and Hart 1957), but we would
expect this difference to decrease the difference in cortisol
between the two groups rather than inflate the difference.
Water temperature was not measured during the collection
of our samples so we were unable to test for these effects.
Our results suggest a possible relationship between
cortisol and beluga whale age. Cortisol can change with
age because of changes in metabolism, reproductive
activity and senescence and can be significantly elevated in
older individuals when faced with a stressor because
feedback mechanisms do not function as well in older
individuals (Sapolsky et al. 1984). Although the interaction
between age and source (harvest, entrapment) was not
significant, the data appear to suggest that while entrapped
blubber cortisol concentrations may have increased with
age, the relationship was less evident in whales from the
subsistence harvest. Age effects can be exaggerated in
some species during stressful events due to a breakdown in
the hippocampus in older individuals (Sapolsky et al.
1984), but a larger sample size may be needed to determine
whether this age effect occurs in beluga whales only during
extremely stressful events like entrapments. In addition, the
reproductive status of females may affect cortisol concen-
trations in some species, but our sample included only
three known females and differences were not detected
between sexes.
For the 2006 Husky Lake entrapment event, we know
freeze-up began in September and whales harvested in
November appeared by visual observation to be in poor
condition, but no measures of body condition were taken
(Fisheries Joint Management Commission 2008b; Kocho-
Schellenberg 2010; Higdon and Ferguson 2012). As it is
difficult to identify when whales physiologically perceived
the event as a stressor, instigating the initial release of
cortisol, monitoring whale dive (ability to take normal
breaths) and forging behavior in addition to collecting
blubber biopsy samples throughout an entrapment event
would provide an estimate for duration of stress. Beluga
whales are thought to enter the Husky Lakes to feed, so
prey may have been available during the entrapment event
(Harwood 2007). This information would be valuable as a
tool for estimating the effect of stress on individuals that
escape entrapments and would also provide a measure of
time from initial release of cortisol to when it is reflected in
the blubber.
Polar Biol
123

No published data of cortisol incorporation in blubber
exist due in part to the difficult nature of monitoring these
measures in a laboratory setting. Natural entrapments may
provide a situation where cortisol incorporation into adi-
pose tissue could be collected by biopsy dart over the
weeks and months of entrapment. These measures would
show how cortisol incorporates into the blubber over time.
Our cortisol measurements from this event provide a ref-
erence for measuring increased stress in other marine
mammal populations and suggest this method could be
used to measure and compare stress among healthy and
threatened marine mammal populations.
Acknowledgments We thank the faculty, staff and students of
Biological Sciences at University of Manitoba and Fisheries and
Oceans Canada for their assistance in method optimization and
sample acquisition, including: Randi Anderson, Blair Dunn, Olwyn
Friesen, Janet Genz, Ryan McDonald, Lisa Peters, Kerri Pleskach,
Bruno Rosenberg. We would like to thank the laboratory technicians,
Tera Edkins, Maureen Hanzel, Amanda Hoedl and Karlyn McFadyen,
who assisted in processing samples. Our appreciation extends to the
Inuvialuit communities, Fisheries Joint Management Commission,
and Fisheries and Oceans Canada who were responsible for collecting
the samples. Finally, we thank the agencies that provided funding for
this research, including the Molson Foundation, ArcticNet, University
of Manitoba, Fisheries and Oceans Canada and The Natural Science
and Engineering Research Council of Canada.
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