© 2020. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2020) 225, jeb222109. doi:10.1242/jeb.222109
SHORT COMMUNICATION
Extreme diving in mammals: first estimates of behavioural aerobic
dive limits in Cuvier’s beaked whales
Nicola J. Quick1,*, William R. Cioffi2, Jeanne M. Shearer2, Andreas Fahlman3 and Andrew J. Read1
ABSTRACT
We analysed 3680 dives from 23 satellite-linked tags deployed on
Cuvier’s beaked whales to assess the relationship between long
duration dives and inter-deep dive intervals and to estimate aerobic
dive limit (ADL). The median duration of presumed foraging dives was
59 min and 5% of dives exceeded 77.7 min. We found no relationship
between the longest 5% of dive durations and the following inter-deep
dive interval nor any relationship with the ventilation period
immediately prior to or following a long dive. We suggest that
Cuvier’s beaked whales have low metabolic rates, high oxygen
storage capacities and a high acid-buffering capacity to deal with the
by-products of both aerobic and anaerobic metabolism, which
enables them to extend dive durations and exploit their
bathypelagic foraging habitats.
KEY WORDS: Ziphius cavirostris, ADL, Dive duration, Diving
behaviour, Metabolic rate
INTRODUCTION
Marine mammals rely on a variety of anatomical and physiological
adaptations to perform breath hold dives (Fahlman, 2012; Kooyman
et al., 1980; LeBoeuf et al., 1986, 1988; Ponganis, 2011). The
aerobic dive limit (ADL) is a useful index of the dive duration that
can be supported by aerobic metabolism (Ponganis, 2011, 2015)
and was originally defined as the maximum breath hold period
without a measurable increase in blood lactate in Weddell seals
(Kooyman et al., 1980). In practice, however, measuring ADL
experimentally in wild marine mammals is challenging (Ponganis,
2015). More commonly, ADL is approximated as the calculated
aerobic dive limit (cADL) by dividing total body oxygen stores by
diving metabolic rate and has been estimated in this manner for
numerous species (Ponganis, 2015). However, for some marine
mammals, the cADL is exceeded frequently by dive durations
collected by telemetry. Some species show increased post-dive
surface intervals after very long submergences, whilst others do not
(Arnould and Costa, 2006; Costa et al., 2001; Costa and Gales,
2003; Hassrick et al., 2010; Weise and Costa, 2007), suggesting that
additional physiological and behavioural adaptations may further
reduce the energetic cost of diving (Boyd, 1997), or allow efficient
use of anaerobic pathways.
1
Duke University Marine Laboratory, Marine Science and Conservation, Nicholas
School of the Environment, Beaufort, NC 28516, USA. 2Duke University Marine
Laboratory, University Program in Ecology, Nicholas School of the Environment,
Beaufort, NC 28516, USA. 3Fundació n Oceanogràfic de la Comunitat Valencia,
Valencia, 46005, Spain.
Beaked whales are extreme divers, with deeper and longer
foraging dives than any other mammal species (Schorr et al., 2014;
Shearer et al., 2019; Tyack et al., 2006). Time-depth recorders have
been used to document beaked whale diving behaviour (Schorr
et al., 2014; Shearer et al., 2019; Tyack et al., 2006), but direct
measurements of metabolic rates or blood lactate levels do not exist.
An approximation for the ADL of two beaked whale species was
proposed (Tyack et al., 2006) by extrapolating from the estimated
total O2 stores (93 ml O2 kg−1) and cADL (21 min) for a 330 kg
Weddell seal, but these estimated ADLs of 25 min for Blainville’s
beaked whale (Mesoplodon densirostris) and 33 min for Cuvier’s
beaked whale (Ziphius cavirostris) are exceeded, by a factor of
approximately two, by the average duration of foraging dives
commonly performed by these whales (Tyack et al., 2006). It has
been suggested that these whales use prolonged periods at shallower
depths between foraging dives to recover from the build-up of
anaerobic metabolites (Tyack et al., 2006), akin to other species
(Kooyman et al., 1980). Alternatively, beaked whales may have low
diving metabolic rates like most other diving species (Williams
et al., 2004; Castellini et al., 1992; Maresh et al., 2014), allowing
them to remain within their ADL. Velten et al. (2013) estimated
cADL for Mesoplodon spp. using a range of diving metabolic rates
and body composition data from several species to estimate onboard
oxygen stores. They demonstrated that the average dive durations
reported for Mesoplodon species fall within the cADL, if the diving
metabolic rate is similar or less than the basal metabolic rate (BMR)
predicted by Kleiber’s (1987) equation. Resting metabolic rates
comparable to BMR have been measured in delphinids (Fahlman
et al., 2018a,b; Rosen and Trites, 2013; Worthy et al., 2014), and
pinnipeds can lower their diving metabolic rate below resting values
(Fahlman et al., 2013; Hurley and Costa, 2001; Williams et al.,
2004). In the absence of empirical data on metabolic rates, a
behavioural ADL (bADL) can be estimated by examining the
distribution of dive durations. This approach has been used with
Weddell seals (Burns and Castellini, 1996; Hindle et al., 2011)
based on observations that 92–96% of dives were less than
measured ADLs, and that longer surface intervals followed dives
that exceeded ADL (Kooyman et al., 1980, 1983). Foraging theory
predicts that most foraging dives should be shorter than the ADL
because utilisation of anaerobic pathways requires extended surface
times to manage anaerobic by-products and replenish depleted
oxygen stores, leaving less time for foraging (Houston et al., 2003;
Houston and Carbone, 1992; Kooyman et al., 1980). We analysed
foraging dives of Cuvier’s beaked whales (Shearer et al., 2019) to
estimate a bADL and assess whether whales extend their inter-deep
dive intervals after long duration dives.
*Author for correspondence (njq@duke.edu)
N.J.Q., 0000-0003-3840-6711; W.R.C., 0000-0003-1182-8578; J.M.S., 00000002-7784-870X; A.F., 0000-0002-8675-6479
MATERIALS AND METHODS
Use of animals in research
Received 23 January 2020; Accepted 13 July 2020
All research activities were carried out under NOAA/NMFS
Scientific Research Permits 17086 and 20605 issued to Robin
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Journal of Experimental Biology (2020) 225, jeb222109. doi:10.1242/jeb.222109
Baird; NOAA/NMFS permit 14809-03, issued to Doug Nowacek;
and NOAA General Authorization 16185, issued to Andrew Read,
in accordance with the relevant guidelines and regulations on the
ethical use of animals as experimental subjects. The research
approach was approved by the Institutional Animal Use and Care
Committees (IACUC) of Cascadia Research Collective and Duke
University.
Data collection
Between 2014 and 2018, 26 SPLASH10-292 satellite-linked
location-depth tags ( produced by Wildlife Computers, Redmond,
WA, USA) were deployed on Cuvier’s beaked whales off Cape
Hatteras, USA (Table 1), as part of two separate studies (Shearer
et al., 2019; Quick et al., 2019). Tags were deployed remotely from a
9 m rigid-hulled aluminium boat (Shearer et al., 2019) using a
DAN-INJECT JM 25 pneumatic projector (DanWild LLC, Austin,
TX, USA) in the LIMPET configuration (Andrews et al., 2008).
Tags were programmed to record and transmit dive data using the
behaviour log function in which the beginning and end of each dive
was identified by conductivity sensors on the tags. Tags deployed
between 2014 and 2016 retained dive events longer than 30 s and
deeper than 50 m as well as ventilation periods between dives, and
were initially programmed to transmit for 20 h per day for the first
25–28 days and then only every second or third day to maximise
duration of contact (Shearer et al., 2019). Tags deployed in 2017 and
2018 were programmed to sample only dives that exceeded 33 min
duration and 50 m depth (i.e. likely foraging dives; Shearer et al.,
2019) and the intervals between dives of 33 min, with no duty
cycling (Quick et al., 2019). Photographs of all tagged individuals
were taken to determine sex and age class. Individuals with erupted
teeth and heavy body scarring were classed as adult males (Baird,
2016; Coomber et al., 2016; Falcone et al., 2009; McSweeney et al.,
2007). All other animals were assigned as unknown. We did not tag
dependent calves. Tags from 2017 to 2018 were deployed as part of
a behavioural response study on the effects of US Navy tactical
sonar, so we truncated tag records to include only periods before
experimental sound exposures (Table S1). For three individuals, this
truncation reduced diving records to three or fewer data points, so
these individuals were removed from further analysis (Table S1).
Incidental exposure to sonar is always possible, but Cape Hatteras is
not on a Navy range and is not an area of intensive Navy training
activity, so incidental exposure was not considered further (Shearer
et al., 2019).
Data analysis
We pooled all foraging dives from both studies, defined for this
population as all submergences of 33 min or longer (Shearer et al.,
2019), and assigned them to 5-min time bins based on duration. We
calculated the percent frequency for each time bin, the cumulative
percentage contributed by each bin, and 50th and 95th percentiles of
the presumed foraging dive durations. We recorded the inter-deep
dive interval (IDDI) that followed each dive, defined as the time
between adjacent dives of at least 33 min. This interval was used as
a measure of recovery time between the long, presumed foraging
dives. Although variable, this IDDI typically included several
shorter dives (<33 min, median depth=280 m) interspersed with
ventilation periods near the surface (median duration=2.2 min;
Shearer et al., 2019). If an IDDI record was missing, we excluded
the dive from further analysis. To test for periods of recovery, we
fitted a linear mixed effects model using lme4 (Bates et al., 2015)
in R software (https://www.r-project.org/) to IDDI with dive
duration as a predictor and individual ID as a random effect. We
compared dive depths and IDDIs of each dive within the top 5% of
dive durations using linear regression. For tags from 2014 to 2016,
Table 1. Summary of dives, inter-deep dive intervals (IDDIs) and surface periods in Cuvier’s beaked whales
Individual ID
Age class/sex
Deployment date
ZcTag029
ZcTag030
ZcTag038
ZcTag040
ZcTag041
ZcTag042
ZcTag046
ZcTag048
ZcTag051
ZcTag054
ZcTag055
ZcTag056
ZcTag057
ZcTag058
ZcTag060
ZcTag061
ZcTag062
ZcTag063
ZcTag064
ZcTag065
ZcTag066
ZcTag067
ZcTag068
ZcTag070
ZcTag076
ZcTag078
Unk/Unk
Ad/M
Ad/M
Ad/M
Ad/M
Ad/M
Ad/M
Unk/Unk
Ad/M
Ad/M
Ad/M
Ad/M
Unk/Unk
Unk/Unk
Ad/M
Unk/Unk
Unk/Unk
Ad/M
Unk/Unk
Ad/M
Ad/M
Ad/M
Ad/M
Unk/Unk
Ad/M
Ad/M
13-May-14
16-Sep-14
14-Jun-15
14-Jun-15
15-Oct-15
21-Oct-15
25-May-16
27-May-16
22-Aug-16
10-May-17
10-May-17
10-May-17
16-May-17
16-May-17
17-Aug-17
17-Aug-17
17-Aug-17
20-Aug-17
20-Aug-17
22-Aug-17
04-Sep-17
04-Sep-17
04-Sep-17
25-May-18
06-Aug-18
06-Aug-18
Number of dives >33 min
(median duration, min)
Number of IDDIs
(median duration, min)
Number of dives with before and
following ventilation periods
165 (64.1)
260 (53.8)
327 (60.4)
9 (55.9)
275 (60.8)
97 (59.7)
58 (51.7)
140 (53.4)
66 (59.7)
193 (57.7)
144 (58.9)
524 (57.5)
303 (58.7)
352 (58.4)
45 (69.8)
62 (51.8)
40 (68.0)
20 (51.3)
19 (54.3)
1*
75 (57.4)
2*
78 (52.3)
3*
228 (64.4)
200 (65.2)
3686
92 (83.9)
208 (81.7)
293 (89.4)
8 (58.5)
247 (55.7)
62 (74.0)
38 (38.6)
95 (59.1)
54 (56.1)
193 (74.5)
144 (68.5)
524 (71.9)
303 (102.2)
352 (97.9)
45 (74.4)
62 (49.1)
40 (92.7)
20 (67.7)
19 (93.9)
1*
75 (86.5)
2*
78 (77.6)
3*
228 (65.6)
200 (78.7)
3386
146
235
318
8
261
83
55
128
56
N/A
N/A
N/A
N/A
N/A
N/A
N/A
N/A
N/A
N/A
N/A
N/A
N/A
N/A
N/A
N/A
N/A
1290
Ad, adult; M, male; Unk, unknown. Asterisks indicate tags excluded from analysis owing to low sample size. N/A, data not available.
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Journal of Experimental Biology (2020) 225, jeb222109. doi:10.1242/jeb.222109
we compared all dive durations with periods of ventilation
(Table 1) both before (time actively breathing at the surface
directly before a 33-min dive and after a dive of any length) and
following (time actively breathing at the surface directly after a
33-min dive and before a dive of any length) dives using linear
models.
RESULTS AND DISCUSSION
We analysed 3680 foraging dives from 23 individuals (Table 1).
Dives were not evenly distributed across individuals owing to
variation in deployment durations and data truncation (Table S1). In
total, 3380 dives had IDDIs available for analysis and 1290 dives
had before and after ventilation periods (Table 1, Table S1). Of the
26 tagged individuals, 18 whales were adult males and eight were of
unknown age and sex class (Table 1). The median duration of the
3680 recorded dives was 59.0 min, with a maximum duration of
132 min, and 5% of the dives exceeded 77.7 min (Fig. 1, Table S1).
IDDI following a dive was significantly correlated with dive
duration (P=0.006; Fig. 2A) with an effect size of 0.79 min.
Individual ID explained only a small amount of the variance (537.8,
s.d.=23.19, residual variance=34,002.2, s.d.=184.40; Table S2). In
an analysis of the longest 5% of dives, a linear model showed no
significant relationship between dive duration and subsequent IDDI
(R 2=−0.003, F1,173=1.595, P=0.208; Fig. 2B, Table S2). There was
also no relationship between the duration of these longest dives and
depth (P=0.916; Table S2). Linear regression of dive duration
against ventilation period immediately before a dive showed no
significant relationship (R 2=0.0001, F1,1288=0.179, P=0.673;
Fig. 2C, Table S2), nor did the dive duration against the
ventilation period immediately following the dive (R 2=0.002,
F1,1288=3.126, P=0.077; Fig. 2D, Table S2). Seventeen of the 23
whales exhibited dive durations in the top 5%, including five of the
eight animals that were not adult males (Fig. 2B).
Our study demonstrated a significant relationship between dive
duration and IDDI for presumed foraging dives. For every extra
minute submerged, there was a 0.79 min increase in IDDI,
suggesting that recovery takes more time as dive duration
increases. However, this relationship does not hold for the top 5%
of dive durations, suggesting that there is no apparent requirement
for additional surface rest immediately after long dives that
exceeded 77.7 min. If Cuvier’s beaked whales exceed their ADL
during foraging dives with a frequency (5%) similar to that of
Weddell seals, then the bADL for this species is 77.7 min. However,
the lack of association between the duration of the longest dives and
IDDI and that very short IDDIs occur before and after the 95th
percentile of dive durations suggests that Cuvier’s beaked whales
may dive again before lactate levels have returned to baseline, if they
are surpassing ADL on these very long dives. Such behaviour
would require the ability to buffer disturbances to acid–base balance
from anaerobic metabolism, allowing lactate to accumulate over a
series of deep dives to be metabolised either during later extended
surface periods, or during the sequences of shallow dives that follow
a deep dive (Tyack et al., 2006).
The cADL for Cuvier’s beaked whales of 33 min (Tyack et al.,
2006) corresponds to the minimum duration of foraging dives used
in our study. However, many diving species exceed cADL with
morphological, physiological and behavioural adaptations that
increase the duration of aerobic diving (Arnould and Costa, 2006;
Costa et al., 2001; Halsey et al., 2006; Nakai, 1959; VillegasAmtmann and Costa, 2010; Villegas-Amtmann et al., 2012; Velten,
2012). Pabst et al. (2016) demonstrated that some beaked whales of
the genus Mesoplodon invest a much smaller percentage of their
100%
20
Frequency (%)
15
50%
10
5
128–132
123–127
118–122
113–117
108–112
103–107
98–102
93–97
88–92
83–87
78–82
73–77
68–72
63–67
58–62
53–57
48–52
43–47
38–42
33–37
0
Dive duration (min)
Fig. 1. Binned dive duration (N=3680 dives) against frequency contribution to overall distribution ( primary y-axis) in Cuvier’s beaked whales. Solid line
shows cumulative frequency (5:1 scale), dashed horizontal lines show 50 and 100% of cumulative frequency. Blue vertical line indicates the 95th percentile.
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Journal of Experimental Biology (2020) 225, jeb222109. doi:10.1242/jeb.222109
B
Inter-deep dive interval (min)
400
300
200
100
0
log10 Pre-dive ventilation period
50
75
C
ZcTag029
ZcTag030
ZcTag038
ZcTag040
ZcTag041
ZcTag042
ZcTag046
ZcTag048
ZcTag051
4
3
2
1
0
3.3
3.4
3.5
3.6
ZcTag055
ZcTag056
ZcTag057
ZcTag058
ZcTag060
ZcTag061
ZcTag062
ZcTag066
ZcTag068
ZcTag076
ZcTag078
ZcTag029
ZcTag030
ZcTag038
ZcTag041
ZcTag042
ZcTag051
200
100
0
80
125
Dive duration (min)
100
3.7
log10 Post-dive ventilation period
Inter-deep dive interval (min)
A
500
90
100
110
120
130
D
ZcTag029
ZcTag030
ZcTag038
ZcTag040
ZcTag041
ZcTag042
ZcTag046
ZcTag048
ZcTag051
4
3
2
1
0
3.3
3.4
3.5
3.6
3.7
log10 Dive duration
Fig. 2. Dive duration against inter-deep dive interval and pre- and post-ventilation period. (A) Dive duration against inter-deep dive interval (IDDI)
with regression from linear mixed model (seven outliers with IDDIs over 500 min are not plotted). Black dashed lines show 95% values of duration and IDDI.
(B) Top 5% of durations with IDDIs, by individual. (C) Log of dive duration against log before ventilation period, by individual. (D) Log of dive durations against log
following ventilation period, by individual.
body mass in metabolically expensive tissues such as brain and
viscera, and a much higher proportion in locomotor muscle with low
tissue metabolic rates, high oxygen storage (Velten et al., 2013) and
muscle fibre types that may protect against ischemia/reperfusion
injury (Moore et al., 2014). Beaked whale locomotor muscle
exhibits elevated myoglobin concentrations, low mitochondrial
volume densities, higher lean mass, large fibre diameters and fast
glycolytic fibres. Cuvier’s beaked whales are larger than
Mesoplodon species, and their adaptations may be even more
extreme. Noren (2004) demonstrated that Cuvier’s beaked whale
muscle is capable of prolonged, low-level anaerobic function, as it
has one of the highest acid buffering capacities among cetaceans.
These adaptations, coupled with a dive response that includes
bradycardia and peripheral vasoconstriction (Ponganis, 2011),
reduced kidney and liver function, and delayed digestion
(Sparling et al., 2007; Svärd et al., 2009; Thouzeau et al., 2003),
together with behavioural modifications including swimming
strategies to minimise metabolism (Williams, 2001; Martín López
et al., 2015), have enabled beaked whales to extend dive durations.
Elephant seals (Mirounga spp.) conduct many extended dives
that exceed cADL and are not followed by extended surface periods
(LeBoeuf et al., 1988; Hassrick et al., 2010; Hindell et al., 1992).
The lack of observed recovery time in these species has led to the
conclusion that they modulate their diving metabolic rates,
essentially allowing ADL to vary per dive (LeBoeuf et al., 1988;
Hindell et al., 1992). Diving metabolic rates do not exist for
Cuvier’s beaked whales, but Velten et al. (2013) calculated a diving
metabolic rate for a 1000 kg Mesoplodon using a value for total
body oxygen stores of 86.9 ml O2 kg−1. Scaling this value for a
2000 kg Ziphius, and using our 95% bADL value of 77.7 min, we
estimate a diving metabolic rate of 1.12 ml O2 kg−1 min−1 for
Cuvier’s beaked whales. This value is 25% lower than an estimated
BMR for a generic 2000 kg terrestrial mammal of
1.48 ml O2 kg−1 min−1, calculated using Kleiber’s equation (BMR=
−1
0.00993×M0.75
b , in l O2 min , where Mb is body mass) (Kleiber,
1987). Body oxygen stores may be underestimated as samples from
Velten et al. (2013) were taken some hours after death, and the BMR
for a beaked whale may be lower than that predicted by Kleiber
(1987). Studies have shown differences in metabolic rates among
marine mammals, including reductions in diving metabolic rates
below resting metabolic rate in large phocid seals during long dives
(Williams et al., 2004; Castellini et al., 1992; Maresh et al., 2014) and
the influence of offspring age and environment in fur seals (Trillmich
and Kooyman, 2001). Weddell seals have large oxygen stores per unit
of body mass and are capable of very low diving metabolic rates
(Ponganis, 2015; Velten et al., 2013; Williams et al., 2004). Cuvier’s
beaked whales have a much larger average adult body mass than
Weddell seals, so we assume that the ADLs of beaked whales exceed
that of Weddell seals and also that the adaptations documented in
Mesoplodon (Velten et al., 2013) are present in Cuvier’s beaked
whales. Therefore, we propose that the ADL in Cuvier’s beaked
whales may be much greater than suggested by previous estimates
and more akin to the value of 77.7 min calculated from our data.
The durations of ventilation periods before and after dives in our
study were not correlated with dive duration, possibly because the
time to oxygen load tissues before diving and replenish oxygen
stores after diving is similar regardless of dive duration. This
absence of an increased ventilation period after long duration dives
suggests that the remaining body oxygen stores following shorter
dives may not be substantially higher than following long dives and
could help explain the levelling off of the correlation between IDDI
and dive duration at dive times above our calculated bADL. The
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ventilation period before a foraging dive is consistently longer than
that following a foraging dive (Shearer et al., 2019) and is perhaps
necessary for another function, such as the anticipatory adjustments
for diving observed in seals and penguins (Boutilier et al., 2001;
Fahlman et al., 2008; McKnight et al., 2019; Wilson et al., 2003), or
social coordination before a group dive.
Blood lactate accumulation (Ponganis, 2011) and myoglobin
levels (Noren and Williams, 2000) are known to vary with age
and size in cetaceans. We were not able to quantify the absolute
size of our whales, but five individuals of unknown age and sex
(assumed not to be adult males) recorded dive durations within
the top 5% of all dives observed. We did observe some very long
IDDIs that may reflect processes other than recovery, such as
increased time to digest food from long dives, or periods of social
coordination, but we are unable to explore this fully in our data
owing to differences in tag durations. Nevertheless, we observed
extended IDDIs and long duration dives in the diving records of
most individuals.
Our value of bADL is calculated from a large sample of presumed
foraging dives in our population. It is possible that the 5% value
calculated from our data does not accurately estimate cADL for
beaked whales given their extreme anaerobic capacity, and we
assumed that all long dives (over 33 min) are primarily for foraging,
consistent with previous authors (Tyack et al., 2006). If shorter dives
function to process metabolic by-products from anaerobic
metabolism, then the period during which this metabolism occurs
should increase as the foraging dive duration increases. However, if
all dives are considered equal, we could calculate a bADL using
each dive from a tag record. We explored this approach and
calculated a 95% value of 65.9 min (Fig. S1). This value is lower
than the bADL calculated using only foraging dives, owing to the
large number of shallow non-foraging dives, but is still considerably
higher than the cADL from Tyack et al. (2006).
Finally, in our extended dataset, we recorded two extremely
long dives from one individual (ZcTag066) of 173 and 222 min,
followed by IDDIs of 236 and 268 min, respectively. These
records were censored from our primary data set because they were
recorded 17 and 24 days after a known 1-h exposure to a Navy
mid-frequency active sonar signal. These extreme dive durations
and IDDIs are perhaps more indicative of the true limits of the
diving behaviour of this species. These extreme records
demonstrate that Cuvier’s beaked whales have evolved an
unparalleled ability to deal with the by-products of aerobic and
anaerobic metabolism, which allows them to exploit their
bathypelagic foraging habitats. We hope that our study provides
an impetus to explore these adaptations; further information on
oxygen loading between dives, blood perfusion during diving, and
metabolic rates would greatly help to interpret the remarkable
diving behaviour of this species.
Acknowledgements
We thank all members of the field team responsible for deploying tags: Daniel
Webster from Cascadia Research Collective, Zach Swaim, Heather Foley and
Danielle Waples from Duke University. We also thank the other project PIs: Doug
Nowacek, Brandon Southall and Robin Baird.
Competing interests
The authors declare no competing or financial interests.
Author contributions
Conceptualization: N.J.Q., W.R.C., A.F., A.J.R.; Methodology: N.J.Q., A.F.; Formal
analysis: N.J.Q., W.R.C., J.M.S.; Writing - original draft: N.J.Q.; Writing - review &
editing: W.R.C., J.M.S., A.F., A.J.R.; Project administration: A.J.R.; Funding
acquisition: A.J.R.
Journal of Experimental Biology (2020) 225, jeb222109. doi:10.1242/jeb.222109
Funding
Funding was provided by the US Fleet Forces Command through the Naval Facilities
Engineering Command Atlantic.
Data availability
Data are available at
https://github.com/williamcioffi/quick_zc_adl (doi:10.5281/zenodo.3880177)
Supplementary information
Supplementary information available online at
https://jeb.biologists.org/lookup/doi/10.1242/jeb.222109.supplemental
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Highlighted Article: Long dives in Cuvier’s beaked whales are not followed by prolonged recovery periods, suggesting that diving
metabolism is reduced and/or undescribed mechanisms are used to process products of anaerobic metabolism.
Funding details
S.No.
Funder name
1
US Fleet Forces Command
Funder ID
Grant ID
6