2735
The Journal of Experimental Biology 215, 2735-2741
© 2012. Published by The Company of Biologists Ltd
doi:10.1242/jeb.069583
RESEARCH ARTICLE
The dive response redefined: underwater behavior influences cardiac variability in
freely diving dolphins
Shawn R. Noren1,*, Traci Kendall2, Veronica Cuccurullo3 and Terrie M. Williams1
1
Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, Center for Ocean Health, 100 Shaffer Road,
Santa Cruz, CA 95060, USA, 2Long Marine Laboratory, University of California, Santa Cruz, Center for Ocean Health,
100 Shaffer Road, Santa Cruz, CA 95060, USA and 3The Dolphin Experience, PO Box F42433, Freeport, Grand Bahama Island,
The Bahamas
*Author for correspondence (snoren@biology.ucsc.edu)
SUMMARY
A hallmark of the dive response, bradycardia, promotes the conservation of onboard oxygen stores and enables marine mammals
to submerge for prolonged periods. A paradox exists when marine mammals are foraging underwater because activity should
promote an elevation in heart rate (fH) to support increased metabolic demands. To assess the effect of the interaction between
the diving response and underwater activity on fH, we integrated interbeat fH with behavioral observations of adult bottlenose
dolphins diving and swimming along the coast of the Bahamas. As expected for the dive response, fH while resting during
submergence (40±6beatsmin–1) was significantly lower than fH while resting at the water surface (105±8beatsmin–1). The
maximum recorded fH (fH,max) was 128±7beatsmin–1, and occurred during post-dive surface intervals. During submergence, the
level of bradycardia was modified by activity. Behaviors such as simple head bobbing at depth increased fH by 40% from
submerged resting levels. Higher heart rates were observed for horizontal swimming at depth. Indeed, the dolphins operated at
37–58% of their fH,max while active at depth and approached 57–79% of their fH,max during anticipatory tachycardia as the animals
glided to the surface. fH was significantly correlated with stroke frequency (range0–2.5strokess–1, r0.88, N25 dives) and
calculated swim speed (range0–5.4ms–1, r0.88, N25 dives). We find that rather than a static reflex, the dive response is
modulated by behavior and exercise in a predictable manner.
Key words: bradycardia, cetacean, dive response, diving, dolphin, exercise, marine mammal, tachycardia.
Received 19 December 2011; Accepted 16 April 2012
INTRODUCTION
The adaptations that enable marine mammals to prolong breathhold durations while diving have intrigued comparative physiologists
for nearly a century. In their original experiments with forcibly
submerged animals, Scholander and colleagues (Scholander, 1940;
Irving et al., 1941; Scholander et al., 1942) described the suite of
physiological adjustments that occur during breath-hold across
terrestrial and aquatic animals alike. Originally termed the ‘diving
reflex’, the adjustments included a characteristic, pronounced
slowing of the heart (bradycardia) and peripheral vasoconstriction
that accompanied the cessation of breathing upon submergence.
Over the years, the term ‘dive reflex’ has been replaced with ‘dive
response’ to reflect the variability in physiological changes that have
been observed across different types of dives (for a review, see
Ponganis et al., 2003). These original landmark studies remain the
cornerstone in our understanding of the cardiovascular adjustments
required for conserving oxygen and prolonging the duration of
submergence by air-breathing vertebrates. In general, the
physiological response to submersion is qualitatively similar for
aquatically adapted and terrestrial mammals, with diving-induced
bradycardia considered to be the major mechanism to regulate blood
oxygen depletion rate, thereby conserving oxygen for the brain and
heart (Harrison and Tomlinson, 1960; Scholander, 1963; Van
Citters et al., 1965; Ridgway et al., 1975; Davis and Kanatous, 1999;
Alboni et al., 2011).
A complicating factor is that wild marine mammals routinely
engage in a wide variety of behaviors while submerged that can
include high-intensity activities, especially when foraging. When
oxygen is readily available, heart rate is usually graded by exercise
intensity to accommodate increased metabolic demands of working
muscle. Such an exercise response has been demonstrated in both
active terrestrial mammals (Mitchell, 1977) and marine mammals
exercising on the water surface (Williams et al., 1993). However,
when mammals are submerged, the heart rate response to exercise in
general appears to be independent of the level of exertion (as defined
by swim speed) for many species (Fedak et al., 1988; Ponganis et al.,
1997; Hindle et al., 2010). Even humans, with few adaptations for
an aquatic lifestyle, demonstrate a dive response that overrides the
exercise response. For example, Smeland et al. (Smeland et al., 1984)
found that final minimum heart rate levels were nearly identical for
resting and exercising human subjects during face submergence. How
marine-adapted mammals balance the physiological responses needed
to simultaneously support seemingly conflicting diving and exercising
cardiovascular responses is not readily understood (Castellini et al.,
1985; Hochachka, 1986).
To date, it has been difficult to assess the adaptive changes in
heart rate with different levels of underwater activity by marine
mammals. This has been due in part to the difficulty of
simultaneously monitoring behavioral and cardiovascular events
across the natural range of physiological states when an animal dives.
THEJOURNALOFEXPERIMENTALBIOLOGY
2736 The Journal of Experimental Biology 215 (16)
The available studies suggest only modest changes in heart rate with
exercise in marine mammals. For example, Williams et al. (Williams
et al., 1993) reported that the heart rates of dolphins exercising near
the water surface were not statistically different from resting levels
when swim speed was less than or equivalent to 2.1ms–1. Only when
swimming speed was increased above cruising speeds to 2.9ms–1
did the heart rates of the dolphins exhibit a significant exercise effect.
Likewise, seals swimming at low speeds in flumes showed little
change in submerged heart rate from resting levels (Fedak et al.,
1988; Williams et al., 1991) and the bradycardia of sea lions was
not consistently related to diving or swimming effort (Ponganis et
al., 1997; Hindle et al., 2010).
Here we re-examine the relationship between heart rate and
underwater behavior in a diving marine mammal to determine how
diving heart rate may be modified during different levels of physical
exertion as may occur during foraging or social interactions (Herzing,
1996). For the first time, heart rate patterns are linked to observations
of discrete behaviors during open-water diving. The bottlenose
dolphin (Turiops truncatus) served as a model species because of its
trainability for performing a wide variety of activity levels. The results
of this study indicate that the ‘dive response’ is altered by physical
exertion. This is a novel finding for marine mammals. Except during
the initial descent and final ascent portions of the dive, previous studies
of heart rate in naturally diving marine mammals reported relatively
stable heart rates during any one dive and heart rate appeared to be
unaffected by physical exertion (for a review, see Butler and Jones
1997). Rather, we found that numerous factors associated with
underwater behavior, including high levels of physical exertion,
influence the magnitude of cardiac adjustment during periods of
submergence. In contrast to previous studies examining relatively slow
swimming speeds in pinnipeds and cetaceans, we found a significant
correlation between swimming intensity and heart rate response during
submergence, suggesting that the dive response is indeed altered by
the exercise response in a marine mammal.
MATERIALS AND METHODS
Animals
Three adult bottlenose dolphins [Tursiops truncatus (Montagu
1821)] (Table1) housed at The Dolphin Experience (Freeport, Grand
Bahama Island, The Bahamas) were trained over 6months for the
experimental protocols. The animals were maintained in large
(15⫻15⫻5m deep) saltwater enclosures connected to the open
ocean and fed a daily diet of capelin and herring supplemented with
multi-vitamins (Sea Tabs, Pacific Research Laboratories, San Diego,
CA, USA). Total body length and maximum girth (at the anterior
dorsal fin insertion) were measured during the month of study
(February 2009) and were used to estimate body masses using a
dolphin-specific morphometric calculator (Messinger et al., 1999).
This calculator was designed specifically for bottlenose dolphins,
and utilizes gender, total body length, maximum girth and age of
the dolphin to estimate body mass. Data used to parameterize the
equation in the calculator were acquired from dolphins at four
facilities including The Dolphin Experience. The mean estimated
mass of the three study animals was 186±12kg (Table1). All
experimental procedures were conducted in accordance with the
Institutional Animal Use and Care Committees at the University of
California at Santa Cruz, and permitted under National Marine
Fisheries Service Marine Mammal Permit No. 984-1587-00.
Electrocardiograph instrumentation and experimental trials
The dolphins were trained to wear a neoprene vest that carried an
IQmark Advanced Holter electrocardiograph (ECG) monitor
(version 7.2, Midmark Diagnostics Group, Versailles, OH, USA)
housed in a custom-designed waterproof box (18⫻8⫻4.5cm;
Backscatter Underwater and Video, Monterey, CA, USA). ECG
waveform signals were received continuously through shielded wires
connected to two suction cup electrodes (5cm diameter with a 2cm
diameter silver plate electrode) that were attached to the dolphins.
One cup was placed on the sternum along the ventral midline directly
below the pectoral fin insertions, and the other was placed above
the right scapula according to Williams et al. (Williams et al., 1993)
and Noren et al. (Noren et al., 2004). Heart rate was recorded
continuously throughout the experimental sessions once the
electrodes and vest were positioned.
On experimental days, the dolphins followed a boat to the open
ocean where they performed a series of trainer-directed behaviors.
Test behaviors were of variable duration and included: (1) rest while
submerged (Fig.1A), (2) low-intensity activity while submerged
(Fig.1B), (3) horizontal submerged swimming (Fig.1C), (4) vertical
glide to the water surface (Fig.1D) and (5) post-dive surface interval.
Underwater trials took place at 15m depth in the open ocean. After
the animal dove, it stationed near the trainer and was then signaled
to perform a discrete behavior at the ocean floor: rest, low-intensity
activity (i.e. head bob or jaw pop) or horizontal submerged swimming
during which the dolphin chose its speed. Behaviors were performed
in a random order so that the animal could not anticipate the behavior
to be performed. In only a few cases, a second discrete behavior was
performed before the animal was signaled to return to the surface. In
some instances the dolphin returned to the surface to breathe before
the trainer’s signal was given. Dolphins were rewarded with fish
throughout the dive, and the quantity of the fish reward was similar
across all behaviors. In addition to open-water trials, heart rate was
measured during rest on the water surface in the animals’ enclosures.
This enabled us to obtain resting heart rates at the surface exclusive
of the effects of recovery from swimming and diving.
Behavioral and locomotor monitoring
Throughout the underwater trials, behavior and locomotor
movements of the dolphins were monitored visually and recorded
by SCUBA divers with a handheld video recorder (30framess–1;
Sony Handicam, Sony Corporation, Tokyo, Japan) in an
underwater housing (Backscatter Underwater and Video).
Depending on the trial, three to four divers accompanied the
dolphins to direct and monitor specific behaviors. Internal clocks
for the heart rate instrumentation and video recorder were
synchronized to correlate cardiac signals with specific behavioral
events. Simultaneous monitoring allowed for the determination of
the influence of submergence, activity and exercise intensity on
instantaneous changes in heart rate. Stroke frequencies were
analyzed by extracting video clips of the submerged swimming
Table1. Gender and morphology for the adult bottlenose dolphins in this study
ID
Gender
Body length (cm)
Maximum girth (cm)
Estimated body mass (kg)
1M
2M
1F
Male
Male
Female
249
241
241
137
132
147
189
174
196
THEJOURNALOFEXPERIMENTALBIOLOGY
The dive response redefined
A
B
C
D
Fig.1. Adult bottlenose dolphins diving to 15m wearing the neoprene vest
containing the electrocardiogram heart rate monitor. Photographs show (A)
resting at depth, (B) low-intensity activity (ʻhead bobbingʼ), (C) horizontal
swimming at depth and (D) vertical approach to the water surface after
completing a period of submergence at depth.
dolphins using digital video software (Pinnacle Studio 8, Pinnacle
Systems, Mountain View, CA, USA). Videos were examined
frame by frame to determine fluke stroke frequency, defined as
the time it took the fluke to move one cycle from the highest point
of vertical displacement and returning to that same point of
displacement. The time clock for this software was set at 0.01s.
Swimming speed was calculated from stroke frequency using a
previously determined equation for adult, non-reproductive
bottlenose dolphins (Noren, 2008):
U 2.09fS + 0.13,
(1)
–1
where U is dolphin swim speed (ms ) and fS is stroke frequency
(strokess–1).
Heart rate analyses
The ECG waveform (Fig.2) for all sessions was visually inspected
to ensure that the instrumentation accurately determined interbeat
2737
intervals in the absence of signal artifacts associated with muscle
activity. The interbeat interval was then used to calculate instantaneous
heart rate (beatsmin–1). For diving tests, the instantaneous heart rate
was plotted in relation to time into the trial and color coded according
to the recorded behavioral state (Fig.3). Within these trials, a sample
was defined as the mean of all of the instantaneous heart rates
associated with a discrete behavior. Delineations between consecutive
samples were based on the animal changing its behavioral state as
indicated in the video record. For behavioral samples that followed
the descent to depth or preceded the ascent to the surface, instantaneous
heart beat data were visually inspected to determine the inflection
point that defined the beginning and end of the steady-state
physiological period for that behavior. Heart beats prior to or after
this segment represented transitional heart rates associated with
breathing or anticipatory tachycardia, respectively, and were not
included in the mean, following the procedures of Noren et al. (Noren
et al., 2004). For resting trials at the surface in the animal’s enclosure,
the mean of the instantaneous heart rate was inclusive between two
consecutive breaths.
Our primary interest was to quantify differences in heart rate
associated with different behaviors during submergence. Each data
point represents a unique sample (a distinct behavior), and each
sample was of a slightly different duration and exercise intensity;
therefore, measurements were considered to be independent and not
repeated. Although we collected data from three individuals, the
purpose of this study was not to examine individual variation. This
approach enabled us to pool the data and to have a large enough
sample size for statistical analyses. The approach of combining data
across individuals when sample size is low follows the methods
used by previous studies on diving heart rates in marine mammals
and penguins (i.e. Noren et al., 2004; Meir et al., 2008). Nonetheless,
because individual variation may weaken the resulting relationships,
this pooled analytical approach reinforces the robustness of the
conclusions (Meir et al., 2008).
The reported means for heart rate representing each behavioral
state were the average of the samples across all three dolphins.
Differences in heart rate across activity state were determined by
one-way ANOVA in combination with a pairwise Tukey’s test
(multiple comparison procedure). The SegReg (www.waterlog.info)
program was used to determine whether one or more linear
regressions best described the relationship between observed stroke
frequency and heart rate (and calculated swim speed and heart rate).
Briefly, the SegReg program selects the best breakpoint and function
type based on maximizing the statistical coefficient of explanation.
Sigma Stat 2.03 (Systat Software, Chicago, IL, USA) was used for
all other statistical procedures. Data are presented as means ± 1 s.d.
Results were deemed significant at P<0.05.
RESULTS
The three dolphins performed a total of 25 dives to a 15m depth in
the open ocean. The mean duration of the dives was 1.92±0.85min
(range0.27–3.42min), during which the dolphins performed one
to two discrete behaviors of variable duration. We found that
instantaneous heart rate of submerged dolphins varied with behavior.
The minimum and maximum heart rates, which defined the range
of heart rates for each dolphin, occurred during submerged rest at
15m depth and during surface intervals following the dive,
respectively (Figs3, 4). These heart rate extremes for freely diving
dolphins are in agreement with values measured previously for
submerged dolphins resting in an enclosure [50±6beatsmin–1 (Noren
et al., 2004)] and for maximal exertion by trained dolphins pushing
against a load cell at >129kg [139±4beatsmin–1 (Williams et al.,
THEJOURNALOFEXPERIMENTALBIOLOGY
2738 The Journal of Experimental Biology 215 (16)
Fig.2. Representative electrocardiogram (ECG)
traces from an adult bottlenose dolphin. The ECGs
represent three different behaviors: (A) rest at 15m
depth, (B) horizontal swimming at 1.7strokess–1 at
15m depth and (C) post-dive surface interval.
Numbers along the top of the traces denote the
interbeat interval in milliseconds; the row of numbers
below is the calculated heart rate in beats per
minute. Variability in the baseline in B and C is due
to body and respiratory movements. Note that the
specific ECG waveform was dependent on electrode
placement and includes discernible P-wave, QRS
complex and T-wave.
A
B
C
1993)]. In view of this, the present study appeared to elicit the range
of heart rates expected for bottlenose dolphins.
Effect of submergence on heart rate
Variability in heart rate of the dolphins was related in part to location
in the water column, particularly at 15m depth versus the water surface
(Figs3, 4). Mean heart rate for all three subjects during submerged
rest at 15m (40±6beatsmin–1, N15) for a mean duration of 85±51s
(range14–160s) was significantly lower than mean heart rate at the
water surface, which reached 128±7beatsmin–1 (N26) during the
post-dive surface intervals. These surface intervals ranged in duration
from 7 to 118s (mean50±29s). Interestingly, heart rate during rest
at the surface in the enclosures (105±8beatsmin–1, N25), inclusive
between two consecutive breaths, was 1.6 times greater than the
predicted resting heart rate (65±1beatsmin–1) determined from the
allometric regression for heart rate for terrestrial mammals in Stahl
(Stahl, 1967). Submerged resting heart rate was within 62% of this
predicted value. For the purpose of this study, we term heart rate
during submerged rest as baseline heart rate (fH,baseline) and heart rate
at the water surface after diving as maximum heart rate (fH,max).
not deemed statistically different despite the observation that heart
rate was greater in magnitude while swimming.
Indeed, underwater activity modified the level of bradycardia in a
predictable manner. Low-intensity behaviors, such as head bobbing,
jaw popping and various postural adjustments that lasted for a mean
duration of 68±45s (range10–145s), resulted in a 40% increase to
56±7beatsmin–1 (N7) over submerged resting heart rate values
(fH,baseline 40±6beatsmin–1, N15). In comparison, horizontal
submerged swimming that lasted for a shorter duration
(mean37±15s, range17–67s) resulted in a 55% increase to
62±8beatsmin–1 (N10) over fH,baseline (Fig.4). In general, dolphins
approached 37–58% of their fH,max while active at depth. The dolphins
approached 57–79% of their fH,max as they glided to the water surface
after submergence to 15m, demonstrating an anticipatory tachycardia
(Fig.4).
We also found that submerged heart rate during open-water
sessions was correlated with the level of physical exertion during
horizontal swimming (denoted by stroke frequency and speed). Both
of these relationships were best described by one linear regression
(no breakpoint in the data was identified):
fH 12.3fS + 40.6,
Effect of submerged activity on heart rate
As would be expected from an exercise response, heart rate in
submerged dolphins was related to activity type (sedentary behaviors
versus swimming) and intensity level of the behaviors (Figs3–5).
During the open-water sessions, heart rate was significantly different
across the behavioral categories (F5,95346.802, P<0.001). All
results from the subsequent all pairwise multiple comparison were
significant at P<0.05, with the exception that mean heart rate during
submerged swimming and submerged low-intensity activity were
(2)
–1
where fH is mean heart rate (beatsmin ) and fS is in strokess–1
(range0–2.5strokess–1, r0.88, P<0.001, N25). After converting
stroke frequency into swim speed according to Eqn1, this
relationship is described by:
fH 5.7U + 40.5,
–1
(3)
where mean heart rate (fH) is in beatsmin and swim speed (U) is
in ms–1 (range0–5.4ms–1, r0.88, P<0.001, N25; Fig.5).
THEJOURNALOFEXPERIMENTALBIOLOGY
The dive response redefined
Proportion of maximum heart rate (%)
160 1M
140
30 35 40 45 50 55 60 65 70
120
80
60
40
20
0
160 2M
140
5
10
15
20
25
120
Mean heart rate (beats min–1)
140
100
Heart rate (beats min–1)
2739
(26)
120
(25)
100
(18)
80
(10)
60
40
(7)
(15)
100
20
80
60
40
20
0
160 1F
140
2
4
6
8
10
12
14
16
18
20
120
100
80
60
40
Rest
Submerged
Surface
Swim Glide to Post- Rest
surface dive
Low
activity
Fig.4. Mean heart rate of adult bottlenose dolphins while submerged at
15m and while at the water surface. Lower and upper edges of the box
plots indicate the 25th and 75th percentiles, respectively. Error bars below
and above each box show the 10th and 90th percentiles, respectively.
Lines within the boxes denote the median, and circles show outliers. All
behavioral categories were significantly different, with the exception of
submerged low-intensity activity and submerged swim (see Results for
statistics). The colored circles denote the proportion of maximum heart rate
(measured during post-dive surface intervals) utilized for each behavioral
category: submerged rest (blue), submerged low-intensity activity (green),
submerged horizontal swimming (cyan) and vertical glide to the water
surface (gray).
20
0
5
10
15
Time into trial (min)
20
25
Fig.3. Instantaneous heart rate for three adult bottlenose dolphins (1M, 2M
and 1F) during diving bouts to 15m depth. Each point represents an
instantaneous heart beat for submerged rest (blue), submerged lowintensity activity (green), submerged horizontal swimming (cyan), vertical
glide to the water surface (gray) and post-dive surface interval (white)
behaviors plotted in relation to time into the trial.
DISCUSSION
The present study demonstrates the variability in diving bradycardia
that can occur with changes in behavior, particularly physical
exertion, during submergence by a marine mammal. In freely diving
bottlenose dolphins, heart rate cycled systematically as the animals
descended and ascended (Fig.3). Superimposed on this was a
refinement in the level of bradycardia related to specific behaviors
when at depth (Fig.4). In particular, the exercise response was
evident during submergence and appeared to override the dive
response, especially as exercise intensity increased. In the case of
swimming behaviors, heart rate was positively correlated to stroke
frequency (range0–2.5strokess–1) and the corresponding swim
speed (range0–5.4ms–1; Fig.5).
Interestingly, the pattern in heart rate showed elements of the
surface swimming exercise response of dolphins. For bottlenose
dolphins trained to swim next to a boat (Williams et al., 1993), heart
rate was shown to vary little for speeds equal to or slower than the
routine minimum cost of transport (2.1ms–1). Likewise, in the
present study, the heart rate of a submerged dolphin swimming at
approximately 1.2ms–1 did not appear to differ from submerged
resting levels, although the low sample size for slow swimming
during submergence precluded a statistical analysis. However,
when swimming speeds exceeded 3.5ms–1, we observed a marked
increase in heart rate that represented a substantial percentage
(45–58%) of fH,max. These higher swim speeds are faster than the
minimum cost of transport speed (2.1ms–1) for surface-swimming
dolphins (Williams et al., 1993) and exceed the energetically
optimal speeds (averaging 2.0ms–1) observed during dives for a
wide range of marine mammals (Videler and Nolet, 1990).
In view of these results, it may not be surprising that this exercise
response has been overlooked when reviewing heart rate records
retrieved from diving marine mammals. Whether for hydrodynamic
or energetic reasons, deep-diving birds, pinnipeds and cetaceans tend
to move through the water column at predictable, energetically
efficient swim speeds (Costa et al., 1989; Fish and Hui, 1991;
LeBoeuf et al., 1992; Davis et al., 1999; Watanuki et al., 2003;
Watanuki et al., 2005; Miller et al., 2004; Tyack et al., 2006). This
reliance on routine swimming speeds is similar to that observed for
freely moving terrestrial mammals, which utilize a comparatively
narrow range of routine running speeds near the middle of a much
broader range of potential speeds (Wickler et al., 2001).
Consequently, dolphins (Williams et al., 1993) and ponies (Hoyt
and Taylor, 1981) traveling short distances as well as large migrating
ungulates (Pennycuick, 1975) and whales (Mate and Urban-Rámirez,
2003) generally move over a relatively narrow range of preferred
cost-efficient speeds.
This behavioral control over routine exercise levels likely
contributed to the different conclusions for the relationship between
heart rate, speed and stroke frequency reported for diving marine
mammals by the present study and others. Although we found that
heart rate and the level of physical exertion were correlated during
horizontal submerged swimming by dolphins (Fig.5), flume studies
involving gray (Halichoerus grypus) and harbor (Phoca vitulina)
THEJOURNALOFEXPERIMENTALBIOLOGY
2740 The Journal of Experimental Biology 215 (16)
Swim speed (m s–1)
0
0.5
1.0
1.5
2.0
2.5
3.0
3.5
4.0
4.5
5.0
5.5
6.0
6.5
Mean heart rate (beats min–1)
90
80
70
60
50
40
30
20
0
0.5
1.0
1.5
2.0
Fluke stroke frequency (strokes
2.5
3.0
s–1)
Fig.5. Mean heart rate of adult bottlenose dolphins in relation to stroke
frequency and horizontal swimming speed at 15m depth. Mean ± 1 s.d.
heart rates during specific exercise intensities for individual dolphins are
represented by triangles (1M), squares (2M) and circles (1F). Heart rate
data from all three dolphins were combined to construct the least squares
linear regression, denoted by the solid line. Dashed lines show the 95%
confidence intervals for the regression. See Results for equations and
statistics.
seals showed little change in submerged heart rate at relatively slow
swimming speeds (Fedak, 1986; Williams et al., 1991). Studies
measuring the heart rate of freely diving marine mammals also
showed conflicting results, which may be related to the range of
speeds examined. Andrews et al. (Andrews et al., 1997) observed
comparatively high heart rates for northern elephant seals (Mirounga
angustirostris) diving on the continental shelf compared with the
heart rates measured while the seals were off the shelf. Because
elephant seals swim faster when they are on the continental shelf
(Le Boeuf and Crocker, 1996), Andrews et al. (Andrews et al., 1997)
suggested that activity level might have been one of the possible
mechanisms for this alteration in bradycardia. However, this could
not be confirmed because heart rate and swim speed were not
simultaneously measured. In contrast, Hindle et al. (Hindle et al.,
2010) measured stroke frequency, overall dynamic body acceleration
(ODBA) and heart rate in trained, free-ranging Steller sea lions
(Eumetopias jubatus). But the findings in the sea lion study were
inconclusive because the authors demonstrated a correlation between
ODBA and mean heart rate during shallow 10m dives, but reported
that ODBA was not correlated with mean heart rate during deep
40m dives. Based on the tendency of marine mammals to move
over a narrow range of optimal speeds to optimize the use of oxygen
reserves during submergence, Hindle et al. (Hindle et al., 2010) may
have been limited in their ability to detect an exercise response on
heart rate during the deeper dives.
This is not to imply that swimming speed and, by inference, heart
rate never change in the diving animal. Observed sustainable swim
speeds for adult bottlenose dolphins are 3.1ms–1 (Lang, 1975) and
maximum swim speeds of 6.32ms–1 (Noren et al., 2006) and
8.15ms–1 (Rohr et al., 2002) have been routinely observed. These
elevated speeds are undoubtedly important during periods of prey
capture and predator avoidance. Indeed, Weddell seals
(Leptonychotes weddellii) sprint at speeds exceeding two times
routine levels when pursuing Antarctic silverfish 300m below the
sea ice (Davis et al., 1999), and have shown an exercise response
on diving bradycardia (Davis and Williams, 2012). Furthermore, a
recent study on diving short-finned pilot whales (Globicephala
macrorhynchus) named these animals the ‘cheetahs of the seas’
based on remarkable swimming sprint speeds of 3 to 9ms–1 when
actively foraging (Aguilar Soto et al., 2008). Although heart rate
was not measured, if the physiology of this odontocete is similar to
that of bottlenose dolphins, one might expect that diving pilot whales
approach fH,max when pursuing fish at depth, a prediction worth
exploring.
In addition to predictable effects due to behavior and activity
level (Figs4, 5), a closer examination of instantaneous heart rate in
freely diving dolphins (Fig.3) suggests that there may be another
central nervous system (CNS) influence on heart rate (for a review,
see Butler and Jones, 1997). ‘Anticipation’ of events, whether to
prolong submergence or to approach the water surface, may have
modified the magnitude of cardiovascular adjustment during
submergence, particularly during the rest behavior. By videoing the
underwater sessions of the instrumented dolphins, we found that
the animals were capable of adjusting heart rate independent of body
position, behavior or exercise. For example, the level of bradycardia
of quiescent, submerged dolphins sometimes drifted as the duration
of the breath-hold progressed, and these changes in heart rate were
not associated with muscle movements (Fig.3). The drift was in
both directions, both decreasing and increasing heart rate. The
instances of decreasing heart rate while resting at 15m depth may
have been associated with CNS control in ‘anticipation’ of the
animals prolonging breath-hold, as previously described by Elsner
et al. (Elsner et al., 1966). The examples of increasing heart rate
while resting at depth may have corresponded with the ‘anticipation’
of the animals approaching the surface to breathe. Anticipatory
tachycardia, a pronounced elevation in heart rate that occurs as
animals approach the water surface after diving (Fig.3A), has been
attributed to the influence of the CNS (Kooyman, 1989) and it may
actually begin before the animal physically starts the ascent. The
influence of CNS control on heart rate in aquatic animals is not a
novel idea. It has been demonstrated in animals during forced versus
voluntarily submergence (Kooyman, 1989) and it can be conditioned
through training as demonstrated in California sea lions (Zalophus
californianus) (Ridgway et al., 1975). Thus, as found for humans
(De Pascalis et al., 1991), instruction and biofeedback can play an
important role in the voluntary control of heart rate in submerged
marine mammals.
In summary, the cardiovascular profile associated with the dive
response is commonly described as a marked decrease in heart rate
on submergence, followed by a relatively invariant bradycardia at
depth and an anticipatory tachycardia on ascent. Here we find that
this response, in terms of heart rate, is flexible in diving dolphins.
Such a variable dive response raises questions about the management
of blood gases during submergence. Although there is a premium
to conserve oxygen through bradycardia and an associated
redistribution of blood flow (Scholander, 1940; Irving et al., 1941;
Harrison and Tomlinson, 1960; Elsner, 1965; Elsner et al., 1966),
heart rate varies with the intensity of underwater behaviors (Figs4,
5), as does peripheral blood flow, as evident from changes in skin
temperature and heat flow from the extremities of diving dolphins
(Williams et al., 1999; Noren et al., 1999). Rather than a hindrance
to diving, alterations in blood flow (as facilitated by alterations in
heart rate) throughout submergence theoretically facilitate more
effective unloading of endogenous oxygen stores by enabling the
parallel depletion of the blood and muscle oxygen reserves (Davis
and Kanatous, 1999). This may explain the unexpectedly high
muscle oxygen saturation measured during diving in other marine
THEJOURNALOFEXPERIMENTALBIOLOGY
The dive response redefined
mammals (Hill et al., 1995). How these fluctuations in the dive
response will affect the management of other blood gases, including
carbon dioxide and nitrogen, that may impact the susceptibility to
decompression syndromes remains to be answered (Hooker et al.,
2012). Clearly, underwater behavior and activity level have a larger
influence on heart rate during submergence than previously
presumed.
ACKNOWLEDGEMENTS
The authors thank the OʼNeill Company for designing and donating the neoprene
vests for the dolphins. We also are grateful to B. Richter (Long Marine Laboratory,
UCSC) for assistance with testing the vests and calibration of the instrumentation
on dolphins, as well as the trainers at The Dolphin Experience (Freeport,
Bahamas) for assistance in dolphin training and open-water measurements.
FUNDING
This study was funded by grants from the Office of Naval Research (N00014-081-1273 and N00014-05-1-0808) to T.M.W.
REFERENCES
Aguilar Soto, N., Johnson, M. P., Madsen, P. T., Díaz, F., Domínguez, I., Brito, A.
and Tyack, P. (2008). Cheetahs of the deep sea: deep foraging sprints in shortfinned pilot whales off Tenerife (Canary Islands). J. Anim. Ecol. 77, 936-947.
Alboni, P., Alboni, M. and Gianfranchi, L. (2011). Diving bradycardia: a mechanism
of defense against hypoxic damage. J. Cardiovasc. Med. 12, 422-427.
Andrews, R. D., Jones, D. R., Williams, J. D., Thorson, P. H., Oliver, G. W., Costa,
D. P. and Le Boeuf, B. J. (1997). Heart rates of northern elephant seals diving at
sea and resting on the beach. J. Exp. Biol. 200, 2083-2095.
Butler, P. J. and Jones, D. R. (1997). Physiology of diving of birds and mammals.
Physiol. Rev. 77, 837-899.
Castellini, M. A., Murphy, B. J., Fedak, M., Ronald, K., Gofton, N. and Hochachka,
P. W. (1985). Potentially conflicting metabolic demands of diving and exercise in
seals. J. Appl. Physiol. 58, 392-399.
Costa, D. P., Croxall, J. P. and Duck, C. D. (1989). Foraging energetics of Antarctic
fur seals in relation to changes in prey availability. Ecology 70, 596-606.
Davis, R. W. and Kanatous, S. B. (1999). Convective oxygen transport and tissue
oxygen consumption in Weddell seals during aerobic dives. J. Exp. Biol. 202, 10911113.
Davis, R. W. and Williams, T. M. (2012). The marine mammal dive response is
exercise modulated to maximize aerobic dive duration. J. Comp. Physiol. A (in
press).
Davis, R. W., Fuiman, L. A., Williams, T. M., Collier, S. O., Hagey, W. P.,
Kanatous, S. B., Kohin, S. and Horning, M. (1999). Hunting behavior of a marine
mammal beneath the antarctic fast Ice. Science 283, 993-996.
De Pascalis, V., Palumbo, G. and Ronchitelli, V. (1991). Heartbeat perception,
instructions, and biofeedback in the control of heart rate. Int. J. Psychophysiol. 11,
179-193.
Elsner, R. W. (1965). Heart rate response in forced versus trained experimental dives
in pinnipeds. Hvalrad. Skr. 48, 24-29.
Elsner, R. W., Kenney, D. W. and Burgess, K. (1966). Diving bradycardia in the
trained dolphin. Nature 212, 407-408.
Fedak, M. A. (1986). Diving and exercise in seals: a benthic perspective. In Diving in
Animals and Man (ed. A. O. Brubakk, J. W. Kanwisher and G. Sundnes), pp. 11-32.
Trondheim: Tapir.
Fedak, M. A., Pullen, M. R. and Kanwisher, J. (1988). Circulatory responses of seals
to periodic breathing: heart rate and breathing during exercise and diving in the
laboratory and open sea. Can. J. Zool. 66, 53-60.
Fish, F. E. and Hui, C. A. (1991). Dolphin swimming – a review. Mammal Rev. 21,
181-195.
Harrison, R. J. and Tomlinson, J. D. W. (1960). Normal and experimental diving in
the common seal (Phoca vitulina). Mammalia 24, 386-399.
Herzing, D. (1996). Vocalizations and associated underwater behavior of free-ranging
Atlantic spotted dolphins, Stenella frontalis and bottlenose dolphins, Tursiops
truncatus. Aquat. Mamm. 22, 61-79.
Hill, R. D., Schneider, R. C., Liggins, G. C., Schuette, A. H., Elliott, R. L., Guppy,
M., Hochachka, P. W., Qvist, J., Falke, K. J. and Zapol, W. M. (1987). Heart rate
and body temperature during free diving of Weddell seals. Am. J. Physiol. 253,
R344-R351.
Hindle, A. G., Young, B. L., Rosen, D. A. S., Haulena, M. and Trites, A. W. (2010).
Dive response differs between shallow- and deep-diving Steller sea lions
(Eumetopias jubatus). J. Exp. Mar. Biol. Ecol. 394, 141-148.
Hochachka, P. W. (1986). Balancing conflicting metabolic demands of exercise and
diving. Fed. Proc. 45, 2948-2952.
Hooker, S. K., Fahlman, A., Moore, M. J., Aguilar de Soto, N. and Bernaldo de
Quirós, Y., Brubakk, A. O., Costa, D. P., Costidis, A. M., Dennison, S., Falke, K.
J. et al. (2012). Deadly diving? Physiological and behavioural management of
decompression stress in diving mammals. Proc. R. Soc. B 279, 1041-1050.
Hoyt, D. F. and Taylor, C. R. (1981). Gait and the energetics of locomotion in horses.
Nature 292, 239-240.
Irving, L., Scholander, P. F. and Grinnell, S. W. (1941). The respiration of the
porpoise, Tursiops truncatus. J. Cell. Comp. Physiol. 17, 145-168.
2741
Kooyman, G. L. (1989). Diverse Divers: Physiology and Behaviour. Springer-Verlag,
Berlin.
Lang, T. G. (1975). Speed, power, and drag measurements of dolphins and porpoises.
In Swimming and Flying in Nature, Vol. 2 (ed. T. Y. Wu, C. J. Brokaw and C.
Brennen), pp. 553-571. New York: Plenum Press.
Le Boeuf, B. J. and Crocker, D. E. (1996). Diving behavior of elephant seals:
implications for predator avoidance. In Great White Sharks: The Biology of
Carcharodon carcharias (ed. A. P. Klimley and D. G. Ainley), pp. 193-205. San
Diego, CA: Academic Press.
Le Boeuf, B. J., Naito, Y., Asaga, T., Crocker, D. and Costa, D. P. (1992). Swim
speed in a female northern elephant seal: metabolic and foraging implications. Can.
J. Zool. 70, 786-795.
Mate, B.R. and Urban-Rámirez, J. (2003). A note on the route and speed of a gray
whale on its northern migration from Mexico to central California, tracked by satellitemonitored radio tag. J. Cetacean Res. Manage. 5, 155-157.
Meir, J. U., Stockard, T. K., Williams, C. L., Ponganis, K. V. and Ponganis, P. J.
(2008). Heart rate regulation and extreme bradycardia in diving emperor penguins. J.
Exp. Biol. 211, 1169-1179.
Messinger, C., Messinger, D., Dye, G., Berry, P. and Weissensel, R. (1999).
Determining morphometric accuracy in Tursiops truncatus. In Proceedings of the
27th Annual Conference of the International Marine Animal Trainerʼs Association, p.
24.
Miller, P. J. O., Johnson, M. P., Tyack, P. L. and Terray, E. A. (2004). Swimming
gaits, passive drag and buoyancy of diving sperm whales Physeter macrocephalus.
J. Exp. Biol. 207, 1953-1967.
Mitchell, J. W. (1977). Energy exchanges during exercise. In Problems with
Temperature Regulation During Exercise (ed. E. R. Nadel), pp. 11-26. New York:
Academic Press.
Noren, D. P., Williams, T. M., Berry, P. and Butler, E. (1999). Thermoregulation
during swimming and diving in bottlenose dolphins, Tursiops truncatus. J. Comp.
Physiol. B 169, 93-99.
Noren, S. R. (2008). Infant carrying behaviour in dolphins? Costly parental care in an
aquatic environment. Funct. Ecol. 22, 284-288.
Noren, S. R., Cuccurullo, V. and Williams, T. M. (2004). The development of diving
bradycardia in bottlenose dolphins (Tursiops truncatus). J. Comp. Physiol. B 174,
139-147.
Noren, S. R., Biedenbach, G. and Edwards, E. F. (2006). Ontogeny of swim
performance and mechanics in bottlenose dolphins (Tursiops truncatus). J. Exp. Biol.
209, 4724-4731.
Pennycuick, C. J. (1975). On the running of the gnu (Connochaetes taurinus) and
other animals. J. Exp. Biol. 63, 775-799.
Ponganis, P. J., Kooyman, G. L., Winter, L. M. and Starke, L. N. (1997). Heart rate
and plasma lactate responses during submerged swimming and trained diving in
California sea lions, Zalophus californianus. J. Comp. Physiol. B 167, 9-16.
Ponganis, P. J., Kooyman, G. L. and Ridgway, S. H. (2003) Comparative diving
physiology. In Physiology and Medicine of Diving, 5th edn (ed. A. O. Brubakk and T.
S. Neuman), pp. 211-226. New York: Saunders.
Ridgway, S. H., Carder, D. A. and Clark, W. (1975). Conditioned bradycardia in the
sea lion Zalophus californianus. Nature 256, 37-38.
Rohr, J. J., Fish, F. E. and Gilpatrick, J. W., Jr (2002). Maximum swim speeds of
captive and free-ranging delphinids: critical analysis of extraordinary performance.
Mar. Mamm. Sci. 18, 1-19.
Scholander, P. F. (1940). Experimental investigations on the respiratory function in
diving birds and mammals. Hvaldrad. Skr. 22, 1-31.
Scholander, P. F. (1963). Master switch of life. Sci. Am. 209, 92-106.
Scholander, P. F., Irving, L. and Grinnell, S. W. (1942). On the temperature and
metabolism of the seal during diving. J. Cell. Comp. Physiol. 19, 67-78.
Smeland, E. B., Owe, J. O. and Andersen, H. T. (1984). Modification of the ʻdividing
bradycardiaʼ by hypoxia or exercise. Respir. Physiol. 56, 245-251.
Stahl, W. R. (1967). Scaling of respiratory variables in mammals. J. Appl. Physiol. 22,
453-460.
Tyack, P. L., Johnson, M., Aguilar Soto, N. A., Sturlese, A. and Madsen, P. T.
(2006). Extreme diving of beaked whales. J. Exp. Biol. 209, 4238-4253.
Van Citters, R. L., Franklin, D. L., Smith, O. A., Jr, Watson, N. W. and Elsner, R.
W. (1965). Cardiovascular adaptations to diving in the northern elephant seal
Mirounga angustirostris. Comp. Biochem. Physiol. 16, 267-276.
Videler, J. J. and Nolet, B. A. (1990). Costs of swimming measured at optimum
speed: scale effects, differences between swimming styles, taxonomic groups and
submerged and surface swimming. Comp. Biochem. Physiol. 97A, 91-99.
Watanuki, Y., Niizuma, Y., Geir, W. G., Sato, K. and Naito, Y. (2003). Stroke and
glide of wing-propelled divers: deep diving seabirds adjust surge frequency to
buoyancy change with depth. Proc. R. Soc. B 270, 483-488.
Watanuki, Y., Takahashi, A., Daunt, F., Wanless, S., Harris, M., Sato, K. and Naito,
Y. (2005). Regulation of stroke and glide in a foot-propelled avian diver. J. Exp. Biol.
208, 2207-2216.
Wickler, S. J., Hoyt, D. F., Cogger, E. A. and Hall, K. M. (2001). Effect of load on
preferred speed and cost of transport. J. Appl. Physiol. 90, 1548-1551.
Williams, T. M., Kooyman, G. L. and Croll, D. A. (1991). The effect of submergence
on heart rate and oxygen consumption of swimming seals and sea lions. J. Comp.
Physiol. B 160, 637-644.
Williams, T. M., Friedl, W. A. and Haun, J. E. (1993). The physiology of bottlenose
dolphins (Tursiops truncatus): heart rate, metabolic rate and plasma lactate
concentration during exercise. J. Exp. Biol. 179, 31-46.
Williams, T. M., Noren, D., Berry, P., Estes, J. A., Allison, C. and Kirtland, J.
(1999). The diving physiology of bottlenose dolphins (Tursiops truncatus). III.
Thermoregulation at depth. J. Exp. Biol. 202, 2763-2769.
THEJOURNALOFEXPERIMENTALBIOLOGY