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First published online October 7, 2008
Journal of Experimental Biology 211, 3249-3257 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.020610
Thermal tolerance in bottlenose dolphins (Tursiops truncatus)
1 US Navy Marine Mammal Program, Space and Naval Warfare Systems Center, 53560
Hull Street, San Diego, CA 92152, USA
2 Biomimetica Santee, CA 92071, USA
* Author for correspondence (e-mail: yeates{at}biology.ucsc.edu)
Accepted 13 August 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: bottlenose dolphin, Tursiops truncatus, thermoregulation, energetics, lower critical temperature
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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).
Bottlenose dolphins range from southern Nova Scotia southward to Patagonia and
the tip of South Africa in the Atlantic Ocean, and along both sides of the
Pacific Ocean from northern Japan and central California southward to
Australia, Chile and New Zealand (Wells
and Scott, 1999; Wells et al.,
1990). Bottlenose dolphins have been observed at more extreme
pole-ward latitudes, as far as 76°N
(McBrearty et al., 1986), but
such sightings are typically considered extralimital. Notable exceptions are
populations that live along the UK coasts (57°N)
(Bristow, 2004;
Hammond and Thompson, 1991;
Wilson et al., 1997). Dolphins
reside in the waters around the UK year round but with seasonal fluctuations
in the number of animals present; during the winter and spring, when the water
temperatures are at their lowest, the number of animals decreases
(Wilson et al., 1997;
Wood, 1998).
Variations in water temperature and prey availability have been postulated
as two factors that influence the distribution and seasonal movements of
dolphins (Shane et al., 1986;
Gaskin, 1968). Distinguishing
the relative importance of each of these factors is a difficult task. Although
water temperature and habitat selection are related in some dolphin species
(Bräger et al., 2003;
Maze and Wursig, 1999;
Barco et al., 1999;
Zolman, 2002), dolphin
distributions and water temperature appear to be co-related to seasonal
redistributions of prey species
(Bräger, 1993;
Bräger et al., 2003;
Maze and Wursig, 1999;
Wells et al., 1990). For
example, bottlenose dolphin distribution extended northward along the
Californian coast during some El Niño years
(Wells et al., 1990). During
these ocean-warming periods, the range of the dolphins' prey species also
extended northward, making it difficult to determine whether the dolphins
primarily responded to the redistribution of prey, or whether both they and
the prey were primarily responding to the warmer water conditions.
Differentiating the relative influence of prey distribution and water
temperature on dolphin habitat utilization requires an understanding of
dolphin thermal limits. The lower critical temperature (LCT) defines the
temperature at which an increase in the metabolic rate is required to
compensate for an increasing amount of heat lost to the environment, i.e. it
defines the lower limit of the range of thermoneutrality
(Schmidt-Nielsen, 1997).
Determining the LCT of the bottlenose dolphin provides a physiological context
within which to evaluate dolphin habitat utilization as a function of water
temperature. Empirical measurements of the LCT in bottlenose dolphins are few
(Williams et al., 2001). By
measuring the basal metabolic rate of three adult male bottlenose dolphins,
Williams and colleagues were able to determine a mean LCT of 5.9°C. This
average value provides the only published LCT for bottlenose dolphins to date.
Because the data from all of the animals were pooled, the impact of individual
animal size on the LCT is unknown. Further quantification of LCT as a function
of body mass is warranted since mass has been positively related to cold water
habitation by bottlenose dolphins (Ross
and Cockcroft, 1990).
Air temperature may also influence dolphin thermal limits. Dolphins, unlike
most terrestrial mammals and pinnipeds (seals and sea lions), lack nasal
turbinates (Hillenius, 1992).
In most terrestrial mammals, the bony nasal turbinates help to warm and
humidify inhaled air prior to reaching the lungs, diminishing the loss of heat
from the core that is required to warm the lung air
(Jackson and Schmidt-Neilsen,
1964). Lacking nasal turbinates, dolphins exposed to cold air
would be required to warm air within the lung via heat transfer from
associated tissues and may need to rely on regional increases in blood flow to
combat the drying of the pulmonary mucosa
(Baile et al., 1987). The
exposure of lung epithelia to cold air could potentially affect epithelial
performance and integrity, and the loss of heat from the core of the body
could increasingly challenge thermal balance if coupled with cold water
temperatures.
In this study we assessed the lower critical water temperature and the
effects of cold air inhalation for five Atlantic bottlenose dolphins
(Tursiops truncatus) acclimated to a mid-latitude climate. The
dolphins, housed in open water pens within San Diego Bay, are acclimated to
the coastal water temperatures of southern California and provide the
opportunity to obtain information on thermal tolerance applicable to
conspecifics within the same region. Wild Pacific bottlenose dolphins (also
Tursiops truncatus) along the coast of California are generally found
from the central coast (
38°N) southward; bottlenose dolphins have
been observed as far north as Washington State (46°N), although these
sightings are considered extralimital
(Ferrero and Tsunoda, 1989).
The results of this study provide insight on the tolerance of bottlenose
dolphins to cold water and air, thus permitting the relative importance of
environmental temperatures to be related to habitat utilization.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The dolphins were housed at SSC San Diego in floating net pens within San Diego Bay. Water temperatures in San Diego Bay were obtained from a buoy moored inside San Diego Bay (Station ID: 9410170, latitude 32°42.8'N, longitude 117°10.4'W) that is operated by the National Oceanographic Data Center. All dolphins had been previously trained for short transports between the net enclosure and pools. Animals were fed a mixed diet of herring (Clupea harengus), mackerel (Scomber scombrus) and capelin (Mallotus villosus) and were supplemented with vitamins (Mazuri® Tabs, PMI Nutrition International, Richmond, IN, USA). Animals were weighed weekly to the nearest 0.5 kg during the period of the study using a hanging crane scale (Challenger 2, Model 3360, Measurement Systems International, Seattle, WA, USA; Table 1). For each animal, blubber depth was measured weekly at two dorsal, two lateral and two ventral body sites (Fig. 1). Blubber depth measurements were made from the skin surface to the blubber muscle interface using a SonoSite Titan portable imaging ultrasound (SonoSite, Bothell, WA, USA) with a C60 (5–2 MHz), 60 mm broadband transducer and at 0.01 cm resolution. Measurements were made with the animal in the water while the animal voluntarily presented itself for the ultrasound measurements. Natural skin markings on the dolphins were used to consistently identify measurement sites for repeated ultrasound measurements. Dorsal (D1, D2) measurements were taken approximately 1 cm to the right of midline, whereas lateral (L1, L2) measurements were taken along the corresponding lateral midline (i.e. halfway between the ventral and dorsal surfaces). Ventral sites (V1, V2) were taken midline, approximately 10 cm cranial and caudal of the umbilicus.
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Oxygen consumption
Oxygen consumption
(
O2)
measurements were conducted while the dolphins were housed in the ECF. Of the
five dolphins, two (Tt1, Tt2) were transported to the ECF and remained there
for a period of 10 days. Two (Tt4, Tt5) were transported to the ECF for
3–4 day periods with 3–4 days between pool sessions until testing
across all Tw was completed. Testing was completed on
these dolphins within 30 days of the first measurement. Water temperature was
decreased gradually overnight while the dolphins resided in the pool. On
return trips to the pool (before a 3–4 day residency) water temperature
was preset to the test temperature. The largest difference between the ambient
ocean temperature and the experimental pool temperature experienced by these
animals was 9°C. Dolphin Tt3 was transported from the net pens (water
temperature range, 12.9–17.9°C) to the ECF on a daily basis. Pool
water was cooled to testing temperature prior to the arrival of the dolphin at
the ECF. The maximum temperature difference between the net pens and pool
temperature this dolphin experienced occurred in February and was
15.2°C.
The dolphins were trained to rest quietly under a clear acrylic metabolic dome (112 cmx76 cmx44.5 cm) for 10–20 min to permit the collection of respiratory gases. The metabolic dome floated on top of the water and was sealed against the water surface through the suction created by the flow of air through the dome (see below). A rope restraint connected the dome to the side of the pool and prevented the dome from being pulled underwater by the air flow. A neoprene-covered plate was mounted on the interior of the dome for the animal to bite onto and to help maintain its position while resting under the dome.
The respirometry system was calibrated daily with dry, ambient air (20.95%
O2) and weekly using dry nitrogen gas (100% dry N2). The
flow of calibration gases into the dome was controlled by a ball flow meter
(Cole Palmer Instrument Company, Vernon Hills, IL, USA) that was accurate to
within 2% of flow. The theoretical fraction of O2 leaving the dome
was calculated (Davis et al.,
1985; Fedak et al.,
1981) and compared with measured values from the oxygen
analyzer.
Metabolic rates were estimated from
O2 as measured
by the open flow respirometry methods of Williams and colleagues
(Williams et al., 2001). Air
was pulled through the metabolic dome at a rate of 190–300 l
min–1 (depending on animal mass) by a mass flow controller
(Flow Kit 500, Sable Systems International, Henderson, NV, USA). A sub-sample
of dome exhaust was dried (Drierite, WA Hammond Drierite Company, Xenia, OH,
USA) and scrubbed of CO2 (Sodasorb, WR Grace and Company,
Cambridge, MA, USA) and dried again prior to entering the oxygen analyzer
(FOXBOX, Sable Systems International). Oxygen content of the subsample was
logged on a laptop computer every 1 s. Flow rates were corrected to STPD
(standard temperature and pressure, dry) and gas contents were converted to
oxygen consumption rates using equation 4b of Withers
(Withers, 1977) with fasting
respiratory quotient (RQ) assumed to be 0.85
(Schmidt-Nielsen, 1997).
Steady-state resting
O2 was estimated
by selecting the most level 5 min section of continuous data points (Expedata,
Sable Systems International).
Since fish were utilized as positive reinforcement for the completion of
research behaviors, the potential impact of the heat increment of feeding on
the timing of O2
measurements was assessed. One dolphin (Tt3) was trained for daily transports
to and from the ECF and tested once daily over a 3 week period. Oxygen
consumption measurements were conducted at thermoneutrality
(Tw=15°C, Ta=20°C) after
feeding with 1.4 kg of capelin. Measurements were taken on separate days at
30, 40, 45, 55, 120, 170, 180 and 230 min following the feed. These data were
then compared with resting metabolic rates (RMR) obtained after an overnight
fast and used to determine the minimum time required for an animal to return
to a fasting RMR following a maximum fish reward of 1.4 kg of capelin. The
O2 reached a
peak value at 50 min following the consumption of 1.4 kg of capelin, when
it was 57.1% over the mean resting oxygen consumption rate
(Fig. 2). Thereafter,
O2 declined
steadily towards the resting level and returned to fasting oxygen consumption
rates within 180 min of the feeding. This time was subsequently used as the
minimum time between a
O2 measurement
and any feeding prior to the measurement. Feedings prior to a
O2 measurement
were always limited to 1.4 kg of capelin or less.
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Animals that remained in the ECF continuously were tested twice daily;
animals were fasted overnight prior to morning testing and for a minimum of 3
h between morning and afternoon sessions. Fish rewards for morning tests were
limited to 1.4 kg of capelin or less. The dolphin that was transported daily
was provided with a fish reward (
1.4 kg capelin) for the transport to the
ECF. Testing of this animal occurred at a minimum of 3 h following the
consumption of the last fish provided as a reward. Dolphins were exposed to
Tw varying from 0.2 to 18°C. Water temperature was
gradually decreased 1–2°C overnight (12–14 h) prior to testing
the following morning. Elevations in the RMR as a function of
Tw were used to define the lower critical water
temperature (LCTw) for each dolphin (see `Analyses' below).
Additional testing was conducted on two of the dolphins (Tt3 and Tt4) to
determine the influence of cold inspired air on the LCT. For these animals,
the Tw was raised 3°C above their individual
LCTw and the Ta dropped. Air temperature varied
from –2.4 to 17.8°C and was reduced by 2–3°C between
sessions. Air temperature was returned to ambient between sessions, but each
subject was exposed to the test Ta for a minimum of 3 h
prior to the measurement of
O2. Given the
stable Tw, a LCT for air
LCTat was determined, where t is the
temperature of the water at the time of testing.
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As a proxy for core body temperature, deep colonic temperature was taken in
the pens on
non-O2 trial
days as well as in the ECF immediately following oxygen consumption trials.
Rectal temperature was taken at 25 cm depth (TR25) for all
dolphins and for a sub-set of dolphins (Tt2, Tt3) at both 25 and 15 cm depth
(TR15). These positions in the colon place the points of
measurement within the countercurrent heat exchanger (25 cm)
(Rommel et al., 1994)
associated with the testes and posterior to the countercurrent heat exchanger
(15 cm) (Rommel et al., 1994).
Measurements were taken using a pliable rectal probe with a thermocouple
(Traceable® digital thermometer accuracy ±0.05°C, Control
Company, Friendswood, TX, USA). Rectal temperature was recorded once the
temperature reading was stable for a period of 30 s.
Blood chemistry
Prior work has suggested that some hematological values may vary as a
function of cold exposure and may be related to either the pathophysiology of
cold stress or adaptation to cold exposure (e.g.
Chun and Harris, 1978). In
order to investigate whether there were any systematic variations in standard
blood chemistries related to cold exposure, animals were trained to present
their flukes voluntarily for blood sampling at the end of an exposure period.
Mixed arterial–venous blood samples were drawn from vessels on the
ventral surface of the dolphin's fluke. When possible, sample collection was
performed every 2–3 days for dolphins that remained in the ECF for 10
days (Tt1 and Tt2), and was performed at each temperature exposure for the
dolphin that was transported to and from the ECF daily (Tt3). Sample
collection was irregular for the remaining two animals (Tt4 and Tt5) due to a
more staggered pool residency schedule; only one blood sample was collected
from Tt5 during the study. Samples were drawn into chilled 7.5 ml serum and 4
ml sodium heparin blood collection tubes (Becton Dickinson, Franklin Lakes,
NJ, USA) and immediately centrifuged for 10 min at 1509g.
Serum samples were sent to Quest Diagnostics (San Diego, CA, USA) and
replicate samples were analyzed on a Stat Profile© Critical Care Xpress
system (Nova Biomedical, Waltham, MA, USA). Each sample was processed to
determine pH, hematocrit (Hct), hemoglobin content (Hb), electrolyte levels,
glucose, lactate and blood urea nitrogen (BUN).
Analyses
Prior to determination of the LCTw,
O2 values
measured in afternoon and morning trials were compared for each animal using
Student's paired t-test to determine whether the timing of the trials
affected the O2.
The LCTw for each dolphin was determined by performing a segmented
linear regression with breakpoint (Yeager
and Ultsch, 1989) using
O2 as the
dependent variable and Tw as the independent variable.
Using this approach, the data were divided into two sets by a breakpoint
within the range of Tw to which the animals were exposed.
The breakpoint was calculated as the division that results in the minimization
of the squared errors for the two linear models (example given in
Fig. 3). The same approach was
used for determining the LCTta but with
Ta used as the independent variable. Regression analysis
was used to determine whether core body temperature or respiration rate was
related to Tw and to look for relationships between blood
chemistry values and either Tw or Ta.
The latter analysis was completed for all of the animals except Tt5 since only
one blood sample was obtained from this animal during the study.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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O2 measurements
taken in the morning and the afternoon trials were similar (paired
t-tests; Tt1, t=0.13, P=0.90; Tt2,
t=–1.33, P=0.21; Tt4, t=1.19,
P=0.14; Tt5, t=2.33, P=0.5); therefore, morning and
afternoon trials were combined in the calculation of LCTw for each
dolphin. For all dolphins, a near-linear increase in
O2 occurred at
decreasing temperatures below the LCTw (for example, see
Fig. 3). LCTw
demonstrated a curvilinear relationship with mass, with the LCTw
increasing rapidly below an animal mass of 180 kg
(Fig. 4;
r2=0.64). LCTw ranged from 5.5 to 10.6°C
(Table 1) and was related to
body mass following the equation:
 | (1) |
187 kg. The highest LCTw did not belong
to the smallest animal. It occurred in the only female dolphin tested (Tt5),
which was also the oldest dolphin tested (33 years).
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No LCTa could be determined for the two dolphins exposed to
decreasing Ta while being maintained at
Tw slightly above the LCTw, even though
Ta values below –2°C were obtained within the
ECF. Variability in
O2 measurements
was high across the range of Ta tested, and although no
significant relationship between Ta and
O2 was found,
linear regression analysis suggested there was a slight trend of increasing
metabolic rate with reductions in Ta
(Fig. 5; Tt3,
r2=0.15, P=0.07; Tt4,
r2=0.11, P=0.1). The slopes of these
relationships were not significantly different from one another
(F=0.002, P=0.98, d.f.=43) nor were they significantly
different from zero (Tt3, P=0.07; Tt4, P=0.09).
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For the two dolphins (Tt2, Tt3) sampled at both 25 and 15 cm depth, mean rectal temperature at 15 cm depth measured while each animal was in its respective thermoneutral zone was 36.6±0.25°C (Tt3, N=29) and 36.5±0.52°C (Tt2, N=21). The overall range at 15 cm was 35.2–37.5°C across water temperatures ranging from 0.2 to 22.5°C. There was a significant positive linear relationship between water temperature and TR 15 in both dolphins (Tt3, r2=0.24, P=0.0009; Tt2, r2=0.56, P<0.0001) and paired t-tests indicated there was a significant difference between 15 and 25 cm depth in both dolphins (Tt3, P<0.001, t=4.3, d.f.=41, mean difference=–0.13; Tt2, P<0.0001, t=6.19, d.f.=22, mean difference=–0.43). Overall, TR25 was warmer than TR15 with the temperature difference between the two sites decreasing with increasing water temperature.
Blubber depth
Blubber depth demonstrated a non-uniform distribution with the lateral
site, L2, being significantly thinner than the dorsal and ventral sites
(ANOVA, all pair-wise comparisons P<0.01, post-hoc Tukey
test) but not significantly different from L1 (P=0.07). Individual
mean blubber depths for each site and the means for each site across all
dolphins are presented in Table
2. There was no relationship between individual mean blubber depth
and acclimation temperature or LCTw.
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Blood chemistry
Most of the blood chemistry parameters showed no relationship to variations
in Tw or Ta and there was no
indication of pathological consequences of the cold exposures. However, in one
animal that remained in the pool for all of the cold exposures and
measurements (Tt1), a significant inverse relationship between Hct and
Tw existed (Tt1: P=0.04,
r2=0.81). For Tt1, the Hct was 9% higher at the coldest
Tw than at the warmest Tw. A similar
trend was observed for the other animal that resided in the pool for the
duration of the experiment (Tt2: P=0.14,
r2=0.72), but an insufficient number of samples were
collected at the coldest exposure temperatures to fully explore this
relationship. Still, the Hct at the coldest Tw for which a
blood sample was collected was 13% higher than that at the warmest
Tw.
Respiration rate
Across all dolphins, respiration rate ranged from 4 to 45 breaths over a 5
min period and depended on Tw and Ta.
Respiration rate increased with decreasing Tw in four of
the five dolphins (Tt2, N=177, Tw
range=3.0–19.2°C, P<0.001, r2=0.20;
Tt3, N=103, Tw range=0.2–8.3°C,
P<0.001, r2=0.14; Tt4, N=192,
Tw range= 3.9–17.9°C, P<0.001,
r2=0.19; Tt5, N=155, Tw
range=4.6–16.8, P=0.04, r2=0.30). For the
two dolphins exposed to cold air, respiration rate also increased with
decreasing Ta (Tt3, N=78, Ta
range=–2.4–16.1°C, P<0.001,
r2=0.17; Tt4, N=138, Ta
range= 1.7–17.5°C, P<0.001,
r2=0.24).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). The average mass of the dolphins involved in the study
by Williams and colleagues was reported to be 148.6 kg, which is 30 kg
less than the smallest animal tested in this study. These results at first
seem contradictory as it would be expected that smaller animals would have a
higher LCTw. However, the RMR of the dolphins in the study by
Williams and colleagues was 63% higher than that measured here. The
differences are unlikely to be due to the acclimation temperatures, which were
similar between studies, but may exist because of the different methodologies
employed, different physical characteristics of the individual dolphins or the
ages of the animals tested. The dolphins tested by Williams and colleagues
were held in a `metabolic box' for the measurements, which effectively
constrains the animal and may have contributed to an acute stress response
that elevated the metabolic measurements
(Williams et al., 2001).
Alternatively, the animals may not have been completely mature (ages are not
provided in their study) and the blubber composition may have been different.
Within odontocetes, the chemical composition and depth of blubber are known to
vary with ontogeny, time of year and diet
(Costa and Williams, 1999;
Dunkin et al., 2005;
Koopman, 2007;
Montie et al., 2008;
Samuel and Worthy, 2005;
Struntz et al., 2004), and
these factors can affect the thermal conductivity of the blubber layer
(Dunkin et al., 2005;
Meagher et al., 2008).
Complex nasal turbinates occur in nearly all mammals with the exception of
cetaceans and some primates (for a review, see
Hillenius, 1992). Nasal
turbinates provide a surface for exchange of heat and water. They function to
warm and humidify ambient air during inhalation prior to reaching the alveoli
and to cool exhaled air and reduce respiratory water loss via
condensation. This respiratory heat exchange has been postulated to help to
retain body warmth and it is bypassed (i.e. panting) to facilitate cooling in
some mammals (Baker, 1982).
Although no LCTa could be determined for two dolphins maintained at
a constant water temperature slightly above the LCTw, a trend of
increasing O2
and variance in
O2 as air
temperature decreased was observed (Fig.
5). Anecdotally, along with this trend, a change in breath
`quality' was observed as the air decreased in temperature; breaths became
short and shallow compared with the deep breaths observed at ambient air
temperatures. Variations in breathing patterns may be expected if the
inhalation of smaller amounts of cold air serves to protect the pulmonary
mucosa from cold-related trauma, drying and alterations in lung mechanics
(Baile et al., 1987;
Jammes et al., 1983). If so,
then the contribution of inhaled cold air to the thermal budget of a
bottlenose dolphin is probably relatively minor in comparison to the impact of
water temperature for the temperature range measured in this study.
An increase in Hct was observed in the two dolphins that remained in the
pools for the duration of the experiment. These animals had the longest
uninterrupted exposures to cold water temperatures of the five dolphins
studied. This pattern was not observed in the animal that was moved back and
forth to the pool on a daily basis and insufficient samples were taken from
the animals that remained in the pools for 3 days at a time to determine
whether the trend was observed in them. An increase in Hct with decreasing
water temperature was previously observed in bottlenose dolphins under similar
temperature exposure conditions (Chun and
Harris, 1978). Over a 13 day period, three bottlenose dolphins
were maintained in a temperature-controlled facility while the water
temperature was reduced from approximately 17.2 to 3.3°C. During this
period, the Hct of the dolphins increased from 5% to 12%, which is comparable
to the 9% and 13% increase observed in this study. It is feasible that the
increase in Hct reflects an increase in oxygen-carrying capacity through the
proliferation of red blood cells, as the oxygen-carrying capacity and
viscosity of blood have been observed to increase in other mammals under
relatively short cold acclimation periods
(Mercer et al., 1999;
Viscor et al., 2003).
Alternatively, the increase in Hct could reflect cold-induced dehydration, as
has been observed in rats (Sun et al.,
1999). However, no other potential indicators of dehydration were
observed in the dolphins involved in this study.
Although deep colonic temperature was significantly related to water
temperature in three dolphins (Tt1, Tt2, Tt3) and in both dolphins in which
rectal temperature was measured at 15 cm (Tt2, Tt3), the magnitude of the
decrease in core body temperature with declining water temperature was less
than 1.5°C and all body temperatures were within what is considered normal
for the bottlenose dolphin (Hampton et
al., 1971; Pabst et al.,
2002; Pabst et al.,
1995). None of the animals approached what would be considered
hypothermic body temperature. The present study may be compared with a study
in which a male and female dolphin were housed in the Thames River (New
London, CT, USA) from November 1983 to January 1984
(Scronce and Bowers, 1985).
During the stay, water temperature ranged from 1 to 15°C and air
temperature ranged from –18 to 16°C. Both animals exhibited a
relationship between water temperature and core body temperature similar to
that observed in some of the animals in this study. The larger male dolphin,
whose mass varied from 220 to 241 kg during the residency, exhibited a mean
core body temperature of 34.8°C during the coldest water temperatures. The
female, whose mass varied from 207 to 214 kg, demonstrated a drop in core body
temperature to 31.8°C during the coldest water periods. Because of the
hypothermia experienced by this dolphin, she was moved to a heated enclosure
where she regained normothermy (Scronce
and Bowers, 1985). It is important to note that during these
periods of coldest water, which lasted several weeks, the air temperature was
also consistently between –18 and 0°C and provided a prolonged cold
exposure of greater magnitude than was attempted in this study.
In dolphins, regional colonic temperatures are influenced by a
countercurrent heat exchange system (CCHE) consisting of a network of vascular
structures running from the dorsal fin and fluke to the region surrounding the
intra-abdominal testes where it acts to regulate the temperature of the testes
(Rommel et al., 1992;
Rommel et al., 1994;
Pabst et al., 1995). Regional
temperatures within the colon may vary depending on total body length,
activity state and thermal environment
(Rommel et al., 1994;
Pabst et al., 1995). Colonic
temperatures in this study were measured in resting dolphins at two depths, 25
cm (within the CCHE) and 15 cm (posterior to the CCHE). In warmer water
exposures (Tw>16.0°C;) the temperature at the two
measurement sites was generally similar, being within 0.2°C. However, when
the water temperature was cooled, the difference between the two sites
increased, with the measurement site within the CCHE being warmer than the
site posterior to the CCHE. Other researchers have used linear arrays of five
to seven thermocouples placed 5 cm apart to measure colonic temperature in
dolphins resting in water temperature ranging from 28.6 to 33.0°C
(Rommel et al., 1994) and 25
to 26°C (Pabst et al.,
1995). Under these conditions colonic temperature measured within
the CCHE was 0.2–0.7°C and 0.2–0.9°C cooler than that
measured outside the CCHE. By comparison, the water temperatures experienced
by the dolphins in the present study were up to 32.8°C cooler than in
previous studies. Under cooler environmental conditions, the vessels in the
extremities, dorsal fin and fluke would shut down in order to conserve heat
(Scholander and Sheville,
1955) and may explain the comparatively warmer temperatures within
the CCHE than at the site 10 cm posterior. Thus, in resting dolphins, the
differences in TR25 and TR15 measured
in this study may be explained by an overall thermal shell effect, i.e. a
thermal gradient that reflects an increase in heat storage from the skin
surface to the core of the animal.
Relationship of LCTw to habitat utilization
Past work has demonstrated that the population size of dolphins residing at
the high latitudes of the United Kingdom diminishes during the coldest times
of the year (Wilson et al.,
1997; Wood, 1998).
Given the potential dependence of the LCTw on mass and that some
animals remain resident during the coldest portions of the year, it would be
worth determining which members of a population remain resident when the
environmental temperatures are coldest. It may be that dolphins of small mass,
particularly neonates and adolescents, are of insufficient size to tolerate
extended periods of time in water temperatures below the LCTw and
thus relocate to warmer water during the coldest times of the year. Logically,
it would follow that attending adults, particularly nursing females, might
relocate as well. Under such conditions it is predicted that dolphins
remaining in high latitude regions during the time of coldest water
temperatures would be adults, possibly with a bias toward adult males. Future
monitoring of high-latitude resident populations should strive to distinguish
between the seasonal age and sex composition of the population to test this
hypothesis.
Following the 1982–1983 El Niño, changes in residency patterns
along the coast of western North America indicated that oceanographic events
influenced the distribution of coastal bottlenose dolphins, resulting in a
northward range extension into central California (Hansen and Defran, 1993;
Wells et al., 1990). A small
population of bottlenose dolphins continues to reside in this region even
though the water temperature has returned to normal (Caretta et al., 2007).
The range of bottlenose dolphins along the west coast of the United States
appears northward limited at this point, just south of San Francisco
(Carretta et al., 2007). If
comparable to dolphins in this study, the average yearly water temperature
along the west coast of the United States would appear to be tolerable
throughout the year for wild coastal bottlenose dolphins with masses greater
than 187 kg; the lower range of average water temperature reported for the
west coast of the United States ranges from 5.6 to 21.1°C (United States
National Oceanographic Data Center:
http://www.nodc.noaa.gov).
For dolphins exceeding this mass, the potential northward range along the
Pacific coast of the United States would not appear to be limited by water
temperature. Certainly, there are periods of time during which water
temperature would briefly (i.e. of the order of days) drop below the
LCTw of these larger dolphins. However, such drops would not
preclude utilization of the environment, but may require an increase in energy
acquisition to offset any increase in thermoregulatory costs.
One might expect that larger dolphins (with lower LCTw) would
range northward to reduce intraspecific competition for resources, while water
temperature would restrict the movements of smaller dolphins (with higher
LCTw) to the southern California region. However, the current
estimated population size for coastal bottlenose dolphins on the Pacific coast
of the United States is approximately 323 animals and has remained relatively
stable for the past 20 years (Dudzik et
al., 2006). Given the small population size, it seems unlikely
that intraspecific competition for food would be sufficient to promote a
northward expansion. Similarly, if reproductive age females tend to remain in
waters that are within the thermoneutral zone of attended offspring, it would
not benefit males to expand their ranges northward at the cost of reproductive
opportunity. It is interesting to note that the northernmost range use by
Atlantic coastal bottlenose dolphins is seasonally varied. Dolphins are not
typically observed north of Chesapeake Bay during the winter months, when
water temperatures are below 9.5°C, and seasonally migrate southward as
water and air temperature begin to cool
(Barco et al., 1999;
Read et al., 2003;
Torres et al., 2005). If the
LCTw of Atlantic coastal bottlenose dolphins is comparable to or
higher than that measured for dolphins in this study, such water temperatures
are probably outside the LCTw of smaller dolphins, particularly
adolescents and neonates. This may, in part, explain the seasonal southward
migration pattern observed in populations along the mid-Atlantic coast of the
US (Barco et al., 1999;
Kenney, 1990;
Torres et al., 2005).
Two common hypotheses presented to explain the distributional limits of
bottlenose dolphins are water temperature and prey redistribution. However,
the distribution of dolphins is likely to be due to both biotic and abiotic
factors and not to one factor alone. In addition to water temperature and prey
redistribution, alternative factors include bathymetry, social structure and
predator avoidance, each of which may itself be influenced by one of the other
factors. On both the Pacific and Atlantic coasts, coastal bottlenose dolphins
typically reside in areas where water depth is 25 m or less
(Kenney, 1990;
Torres et al., 2005). However,
minimum population estimates of coastal bottlenose dolphins in the Atlantic
exceed 10,000 individuals (Waring et al.,
2007), which is substantially higher than the 323 animals
estimated for the Pacific coastal stock. In contrast to the east coast, the
bathymetry along the west coast of the US lacks a wide shallow continental
shelf potentially limiting the habitat suitable to support large populations
of coastal bottlenose dolphins. Whether or not this is a factor in determining
coastal bottlenose dolphin distributions, and to what extent it affects
distributions, requires further investigation. Additional factors, such as
prey preference and predator avoidance, also exert some influence over coastal
bottlenose dolphin distribution and are themselves likely to be related to
coastal bathymetry and temperature (Hastie
et al., 2004). For example, Heithaus and Dill demonstrated that
water temperature indirectly affected dolphin habitat use by influencing the
presence and absence of a predator
(Heithaus and Dill, 2002).
During cooler months when tiger shark presence was low, dolphins exploited
areas of high prey biomass. During the warmer months, when tiger shark
presence was high, dolphins avoided the area even though prey availability
remained the same. The relationship of prey distribution to dolphin
distribution is also not as clearly determined
(Barco et al., 1999;
Wells et al., 1990); although
prey distribution must to some extent affect habitat selection (e.g.
Barros and Wells, 1998), the
observed plasticity in prey selection
(Young and Phillips, 2002;
Gannon and Waples, 2004) may
minimize the impact resulting from temporal and spatial variations in specific
prey availability in the bottlenose dolphin.
As in any wild population of mammals, the distribution and habitat
utilization of the coastal bottlenose dolphin will be influenced by the
movement of prey, water temperature, the minimization of predation pressure
and the need for social interactions. With respect to water temperature, the
LCTw of bottlenose dolphins acclimated to the waters of coastal
southern California seems sufficient to support the utilization of higher
latitudes for larger animals (i.e. >187 kg). Cold air temperature common to
the higher latitudes would appear to have a minor impact on thermoregulation
in bottlenose dolphins and probably does not limit the range of these animals.
However, the observed northward limits on coastal bottlenose dolphin ranges
may result, in part, because of a need for neonates, adolescents and attending
(presumably reproductive) females to remain in the warmer waters of the
coastal USA. Similar propositions have been made with regard to the increase
in abundance of animals in the inmost waters of the Moray Firth during the
summer months when the water temperature is relatively high
(Wilson et al., 1997). Future
research into coastal bottlenose dolphin distribution should focus on whether
habitats with seasonally cold water and with both resident and migratory
individuals favor utilization by larger, male dolphins during the coldest
months of the year.
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Acknowledgments |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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