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Modeling Tissue and Blood Gas Kinetics in Coastal and Offshore Common Bottlenose Dolphins, Tursiops truncatus


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Bottlenose dolphins (Tursiops truncatus) are highly versatile breath-holding predators that have adapted to a wide range of foraging niches from rivers and coastal ecosystems to deep-water oceanic habitats. Considerable research has been done to understand how bottlenose dolphins manage O 2 during diving, but little information exists on other gases or how pressure affects gas exchange. Here we used a dynamic multi-compartment gas exchange model to estimate blood and tissue O 2 , CO 2 , and N 2 from high-resolution dive records of two different common bottlenose dolphin ecotypes inhabiting shallow (Sarasota Bay) and deep (Bermuda) habitats. The objective was to compare potential physiological strategies used by the two populations to manage shallow and deep diving life styles. We informed the model using species-specific parameters for blood hematocrit, resting metabolic rate, and lung compliance. The model suggested that the known O 2 stores were sufficient for Sarasota Bay dolphins to remain within the calculated aerobic dive limit (cADL), but insufficient for Bermuda dolphins that regularly exceeded their cADL. By adjusting the model to reflect the body composition of deep diving Bermuda dolphins, with elevated muscle mass, muscle myoglobin concentration and blood volume, the cADL increased beyond the longest dive duration, thus reflecting the necessary physiological and morphological changes to maintain their deep-diving lifestyle. The results indicate that cardiac output had to remain elevated during surface intervals for both ecotypes, and suggests that cardiac output has to remain elevated during shallow dives in-between deep dives to allow sufficient restoration of O 2 stores for Bermuda dolphins. Our integrated modeling approach contradicts predictions from simple models, emphasizing the complex nature of physiological interactions between circulation, lung compression, and gas exchange.
Content may be subject to copyright.
published: 17 July 2018
doi: 10.3389/fphys.2018.00838
Frontiers in Physiology | 1July 2018 | Volume 9 | Article 838
Edited by:
Jose Pablo Vazquez-Medina,
University of California, Berkeley,
United States
Reviewed by:
Luis Huckstadt,
University of California, Santa Cruz,
United States
Michael Tift,
University of California, San Diego,
United States
Andreas Fahlman
Frants H. Jensen
Specialty section:
This article was submitted to
Aquatic Physiology,
a section of the journal
Frontiers in Physiology
Received: 16 April 2018
Accepted: 14 June 2018
Published: 17 July 2018
Fahlman A, Jensen FH, Tyack PL and
Wells RS (2018) Modeling Tissue and
Blood Gas Kinetics in Coastal and
Offshore Common Bottlenose
Dolphins, Tursiops truncatus.
Front. Physiol. 9:838.
doi: 10.3389/fphys.2018.00838
Modeling Tissue and Blood Gas
Kinetics in Coastal and Offshore
Common Bottlenose Dolphins,
Tursiops truncatus
Andreas Fahlman 1,2
*, Frants H. Jensen 3†, Peter L. Tyack 4and Randall S. Wells5
1Global Diving Research, Ottawa, ON, Canada, 2Fundación Oceanografic de la Comunidad Valenciana, Valencia, Spain,
3Aarhus Institute of Advanced Studies, Aarhus University, Aarhus, Denmark, 4Sea Mammal Research Unit, Scottish Oceans
Institute, University of St Andrews, St Andrews, United Kingdom, 5Chicago Zoological Society’s Sarasota Dolphin Research
Program, Mote Marine Laboratory, Sarasota, FL, United States
Bottlenose dolphins (Tursiops truncatus) are highly versatile breath-holding predators that
have adapted to a wide range of foraging niches from rivers and coastal ecosystems to
deep-water oceanic habitats. Considerable research has been done to understand how
bottlenose dolphins manage O2during diving, but little information exists on other gases
or how pressure affects gas exchange. Here we used a dynamic multi-compartment gas
exchange model to estimate blood and tissue O2, CO2, and N2from high-resolution
dive records of two different common bottlenose dolphin ecotypes inhabiting shallow
(Sarasota Bay) and deep (Bermuda) habitats. The objective was to compare potential
physiological strategies used by the two populations to manage shallow and deep
diving life styles. We informed the model using species-specific parameters for blood
hematocrit, resting metabolic rate, and lung compliance. The model suggested that
the known O2stores were sufficient for Sarasota Bay dolphins to remain within the
calculated aerobic dive limit (cADL), but insufficient for Bermuda dolphins that regularly
exceeded their cADL. By adjusting the model to reflect the body composition of deep
diving Bermuda dolphins, with elevated muscle mass, muscle myoglobin concentration
and blood volume, the cADL increased beyond the longest dive duration, thus reflecting
the necessary physiological and morphological changes to maintain their deep-diving
life-style. The results indicate that cardiac output had to remain elevated during surface
intervals for both ecotypes, and suggests that cardiac output has to remain elevated
during shallow dives in-between deep dives to allow sufficient restoration of O2stores
for Bermuda dolphins. Our integrated modeling approach contradicts predictions from
simple models, emphasizing the complex nature of physiological interactions between
circulation, lung compression, and gas exchange.
Keywords: diving physiology, modeling and simulations, gas exchange, marine mammals, decompression
sickness, blood gases, hypoxia
Fahlman et al. Estimating Gas Flux in Dolphins
The physiological adaptations that optimize foraging in marine
mammals have long interested researchers. Optimal foraging
theory implies that marine mammals should change dive
behavior and metabolic pathways, and the fraction of aerobic
and anaerobic metabolism based on dive depth and prey
availability (Carbone and Houston, 1996; Cornick and Horning,
2003). Considerable work has been dedicated to understanding
the aerobic limitations of diving air-breathing vertebrates, as
these help with understanding foraging limits and efficiency.
Kooyman et al. (1983) described the maximum dive duration
until increasing blood lactate levels as the aerobic dive limit
(ADL). The calculated ADL (cADL) was later defined as the
total O2stores divided by the rate of O2consumption (Butler
and Jones, 1997), and has been estimated in a number of
species (Kooyman and Ponganis, 1998; Butler, 2006). However,
metabolic rate may change over the course of a dive or foraging
bout, and a few studies have subsequently estimated the cADL
from measured (respirometry: Castellini et al., 1992; Reed et al.,
1994, 2000; Hurley and Costa, 2001; Sparling and Fedak, 2004;
Fahlman et al., 2008a, 2013) or estimated diving metabolic rate
(doubly labeled water, or a proxy of metabolic rate: Boyd et al.,
1995; Froget et al., 2001; Butler et al., 2004; Fahlman et al.,
Most studies agree that the majority of dive durations are
well within the ADL/cADL, as this increases foraging efficiency
and reduces lengthy surface intervals required to remove
accumulated anaerobic by-products such as lactate (Kooyman
et al., 1983). However, some species of otariids that feed on
the benthos appear to exceed their cADL regularly, while those
that feed in shallower water have shorter dive durations and
seldom exceed the cADL (Costa et al., 2001). These differences
may indicate true variation in foraging behavior, but may also be
suggestive of morphological or physiological differences within
or between closely related species that alter cADL (Hückstädt
et al., 2016). For example, the muscle mass in previous studies
was assumed to be similar to that of the Weddell seal (Costa et al.,
2001), and such assumptions are often necessary as available data
do not exist for all variables and species. However, variation in
underwater swimming behavior (Williams, 2001; Fahlman et al.,
2013), or morphological variation in muscle mass and fiber type
(Pabst et al., 2016) may significantly alter the metabolic cost of
Large variations in dive behavior also exist within species. In
the common bottlenose dolphin (Tursiops truncatus), different
ecotypes have evolved to occupy different ecological niches
(Mead and Potter, 1995; Hoelzel et al., 1998). Coastal bottlenose
dolphins inhabit coastal areas and generally perform short
(<60 s), shallow (<10 m) dives (Mate et al., 1995), while offshore
bottlenose dolphins inhabit offshore, deep-water habitats and
regularly dive below 200 m (Klatsky et al., 2007). Interestingly,
neither resting metabolic rate nor lung compliance differed
between the two ecotypes (Fahlman et al., 2018a,b), but blood
hematocrit was significantly higher in the offshore ecotype
(Klatsky et al., 2007; Schwacke et al., 2009; Fahlman et al., 2018a).
In addition, the offshore ecotype is generally larger (Klatsky et al.,
2007), possibly due to larger muscle mass to help increase the
available O2stores and diving capacity. In an attempt to better
understand the physiological limitations of these two ecotypes,
and to explore how variation in morphology and anatomy
may alter gas dynamics during diving, we used a previously
published gas exchange model (Fahlman et al., 2009; Hooker
et al., 2009; Hodanbosi et al., 2016) to estimate blood and tissue
gas tensions for O2(PO2), CO2(PCO2), and N2(PN2) from high
resolution (1 Hz) dive records from coastal bottlenose dolphins
from Sarasota Bay, Florida, and offshore bottlenose dolphins
sampled near the island of Bermuda.
The model described in this paper uses the breath-hold diving gas
dynamics model developed by Fahlman et al. (2009) and Fahlman
et al. (2006), which has been used to estimate lung, blood, and
tissue gas tensions in a number of species (Hooker et al., 2009;
Kvadsheim et al., 2012; Hodanbosi et al., 2016). A brief summary
of the model is included below, with the specific changes made
for the current modeling effort. The model was parameterized for
bottlenose dolphins and was based on published values available
for this species when possible, and otherwise on published values
for beaked whales or phocids (as detailed below).
As in previous work, the body was partitioned into 4
compartments; brain (B), fat (F), muscle (M), and central
circulation (CC), and one blood compartment (BL, arterial and
mixed venous). In the current study, bone was included in the fat
compartment as the bones of deep diving whales are high in fat
content (Higgs et al., 2010). The central circulatory compartment
included heart, kidney, and liver. The muscle compartment
included muscle, skin, connective tissue, and all other tissues
(Fahlman et al., 2009). In previous studies, the alimentary tract
was placed in the central circulation. However, due to its lower
metabolic rate, it was placed in the muscle compartment in
the current study. The size of each compartment as well as the
myoglobin and hemoglobin concentrations were initially taken
from data on coastal dolphins (Mallette et al., 2016). As there is
little or no information about the body composition of offshore
dolphins, changes were made to the body composition of the
offshore ecotype to be more like a beaked whale (Pabst et al.,
Lung Gas Stores and Gas Exchange
Gas exchange occurred between the lungs and blood
compartment and between the blood compartment and
each other compartment (Fahlman et al., 2006). The O2, CO2,
and N2stores in the lung consisted only of a gas phase and were
assumed to be homogenous. We assumed that there was no
diffusion resistance at the lung-surface interface when an animal
was breathing at the water surface (Farhi, 1967). Thus, arterial
blood tension of N2(PaN2), O2(PaO2), and CO2(PaCO2) were
assumed to be equal to the alveolar partial pressures. For an
animal breathing at the surface, we assumed that alveolar partial
pressures of N2(PAN2 ), O2(PAO2), and CO2(PACO2) were,
Frontiers in Physiology | 2July 2018 | Volume 9 | Article 838
Fahlman et al. Estimating Gas Flux in Dolphins
respectively, 0.74 ATA, 0.133 ATA, and 0.065 ATA (Fahlman
et al., 2015), with 0.062 ATA being water vapor.
During diving, hydrostatic pressure compresses the
respiratory system, which causes a pressure-dependent
pulmonary shunt to develop (Fahlman et al., 2009). The
parameters that describe the structural properties for the alveolar
space and conducting airways (Equations 4 and 5 in Bostrom
et al., 2008) were updated based on previously published
compliance values for the bottlenose dolphin (Table 1,Fahlman
et al., 2011, 2015; Moore et al., 2014).
Total lung capacity (TLC) included the volume of the dead
space (trachea and bronchi, VD), and the maximum alveolar
TABLE 1 | Parameters used to describe the structural properties of the respiratory
Parameter Equation
Equation 4 Equation 5
a1.05 ±0.04 (1.1)
b0.90 ±0.06 (1.2)
c2.51 ±0.19 (1.3)
Kp 31.0 ±23 (12.8)
n2.4 ±1.4 (0.91)
The parameters for Equations (4) and (5) in Bostrom et al. (2008) were revised using
previously published compliance data from the bottlenose dolphin (Fahlman et al., 2018b).
Old values are in parentheses.
volume (VA), i.e., TLC =VD+VA. It was assumed that gas
exchange only occurred in the alveoli and when the diving
alveolar volume (DVA) was equal to 0, gas exchange stopped.
We used the equation initially developed by Kooyman (1973),
to estimate TLC (TLCest =0.135 M0.92
b, where Mbis body
mass in kg), and later validated for the dolphin (Fahlman et al.,
2011, 2015). Dead space volume was assumed to be 7% of TLC
(Kooyman, 1973; Fahlman et al., 2011). The relationship between
pulmonary shunt and DVAV1
Awas determined using a power
function (Bostrom et al., 2008) for data from the harbor seals
(Equation 6A in Fahlman et al., 2009).
All pressures were corrected for water vapor pressure,
assuming that the respiratory system was fully saturated at 37C.
Blood and Tissue Gas Stores
As in previous studies, the blood and tissue stores of N2, CO2, and
O2were determined by the solubility coefficients for each gas, as
previously detailed (Fahlman et al., 2006). For O2and CO2, the
average concentration of hemoglobin for each population was
used to estimate the blood O2stores and CO2storage capacity
(Table 2). Tissue gas content was determined as previously
detailed (Fahlman et al., 2006, 2009).
Compartment Size, Cardiac Output, and
Blood Flow Distribution
For the coastal ecotype sampled in Sarasota Bay, the relative
size of each compartment was taken from previous studies in
TABLE 2 | Body compartment composition (% of body mass), estimated compartment metabolic rate (rest), and the value used in the model, cardiac output at
rest/diving and at the surface, male adult dolphins.
Tissue Percent of body mass References
Sarasota Bermuda
Blood 7.1 19.1 Ridgway and Johnston, 1966
Brain 1.0 0.2 Mallette et al., 2016
Fat 31.1 20.7
Central circulation 3.73 3
Muscle 57 (35) 57 (50)
Metabolic rate for a 200 kg animal (l O2min1)
Brain 0.035 0.011 Yazdi et al., 1999; Yeates and Houser, 2008; Noren et al., 2013; Fahlman et al., 2015, 2018a
Fat 0.039 0.024
Central circulation 0.321 0.255
Muscle 0.273 0.245
VO2tot rest 0.67$ 0.54$
Qtot rest (l min1) 6.0¶ 6.0¶ Miedler et al., 2015
Variables for O2storage
[Hb] (g/100 g) 16 16 Ridgway and Johnston, 1966; Noren et al., 2002; Hall et al., 2007; Schwacke et al., 2009
[Mb] (g Mb/100 g muscle) 3 7.3 Noren et al., 2001; Ponganis, 2011; Pabst et al., 2016
Hct (%) 44 57 Ridgway and Johnston, 1966; Hall et al., 2007; Schwacke et al., 2009
O2stores for a 200 kg dolphin (l)
Lung 2.21 2.21 Kooyman, 1989; Kooyman and Ponganis, 1998; Fahlman et al., 2015, 2017b
Tissue 3.82 10.00
Blood 2.68 7.50
For muscle, the value in parenthesis is the actual muscle mass used with myoglobin. Data are for the resting data without the multiplier for exercise. $Values for active animals equal to
2x resting values. ¶Values for active animals equal to 3x resting values (Sarasota dolphins) or 7x resting values (Bermuda dolphins).
Frontiers in Physiology | 3July 2018 | Volume 9 | Article 838
Fahlman et al. Estimating Gas Flux in Dolphins
coastal bottlenose dolphins (Table 2;Ridgway and Johnston,
1966; Mallette et al., 2016). For blood and muscle we used species-
specific values for blood hematocrit (Ridgway and Johnston,
1966; Hall et al., 2007; Schwacke et al., 2009; Fahlman et al.,
2018b), and myoglobin concentration (Noren et al., 2001;
Ponganis, 2011). For the deep-diving offshore dolphins, we
initially assumed that the animals were similar to the coastal
ecotype from Sarasota Bay. However, these assumptions resulted
in a cADL that was too short for all Bermuda dolphins.
We therefore adjusted the body composition of the Bermuda
dolphins, assuming that their body composition was similar to
that of deep diving beaked whales (Pabst et al., 2016), and used
the body composition for Mesoplodon from our previous studies
(Table 2;Hooker et al., 2009).
For the current study, we assumed that the cardiac output
Qtot) at the surface was 3 times higher than the ˙
Qtot measured in
resting bottlenose dolphins (31.5 ml min1kg1,Miedler et al.,
2015). To account for differences in Mb, mass specific ˙
Qtot (s ˙
was adjusted using Equation (5) in Fahlman et al. (2009). During
diving, the ˙
Qtot was reduced to 1/3 of the value at the surface to
account for the dive response, i.e., the diving ˙
Qtot was the same as
that measured in resting animals. Blood flow distributions to each
tissue at the surface and during diving were iteratively tested to
maximize utilization of O2to increase the aerobic dive duration
(Table 2).
Dive Data Used
We used dive data collected from high resolution digital audio
and movement recording tags (DTAG, Johnson and Tyack, 2003)
attached to the dorsal side of each dolphin by means of four
small suction cups, and programmed to release after <24 h.
DTAGs were deployed during 2013–2016 in Sarasota Bay and in
FIGURE 1 | (A) Normalized volume (VA, alveolar volume; VD, dead space/tracheal volume) vs. structural pressure for alveolar and dead space compliances based on
the estimate from Bostrom et al. (2008), or updated estimates from bottlenose dolphins (Fahlman et al., 2011, 2015). (B) Differences in pulmonary shunt with old and
updated compliance values for the respiratory system in dolphins during a representative dive to 150m for an animal with a body composition like the Bermuda
dolphin (Fahlman et al., 2009). The average compliant alveoli and medium compliant trachea were used for the base model, and this model was used as a basis of
comparison with all other simulations. Changes in end-dive mixed venous N2, O2, and CO2levels against (C) dive duration (sec) or (D) maximum dive depth (ATA)
when comparing old and revised lung compliance values. The y-axis is the change in percent for [(old-new)/old * 100]. These changes reflect how the structural
properties alter the shunt and ventilation-perfusion mismatch (Garcia Párraga et al., 2018).
Frontiers in Physiology | 4July 2018 | Volume 9 | Article 838
Fahlman et al. Estimating Gas Flux in Dolphins
August of 2016 off the coast of Bermuda, during capture-release
operations (e.g., Wells et al., 2004; Klatsky et al., 2007). The
dolphins were tagged and data collected under permits issued
by NMFS (Scientific Research Permit Number 15543) and the
Bermuda Government, Department of Environment and Natural
Resources (Research permit number SP160401r).
Data processing was done using the DTAG toolbox
( Tag depth was sampled at
200 Hz and subsequently down-sampled to 25 Hz during
post-processing using a linear phase 10 Hz low-pass FIR filter.
Surfacings were used to estimate the zero-pressure offset and to
characterize and remove the effect of temperature on estimated
A dive was defined as a submergence deeper than 1.5 m (1.15
ATA) and longer than 10 s. The start and end of each dive was
calculated as the first and last point of the dive that exceeded
0.1 m depth, and the surface interval was defined as the time from
current dive to previous dive.
Respiratory Compliance
The updated parameters that defined the structural properties
(compliance) of the respiratory system resulted in a stiffer upper
airway and more compliant alveolar space as compared with the
values used in previous studies (Figure 1A), which affected the
pulmonary shunt (Figure 1B). The parameters for respiratory
compliance were updated and the model output compared with
the results from the previous model (Figures 1C,D). The end-
dive gas tension increased with both dive duration and maximum
dive depth for N2and O2, while for CO2there was a slight
decrease (Figures 1C,D).
Dive Data
There were no significant differences in body mass (Mb,P>0.1,
Welch t-value: 1.8, df =2), body length (P>0.9, t-value: 0.02,
df =5), average number of dives per hour (P<0.1, Welch
t-value: 0.3, df =5), and average surface interval (P>0.1,
Welch t-value: 1.3, df =2, Table 3) between ecotypes. There
were significant differences in the dive behavior between the
two populations, with dive duration (P<0.01, Welch t-value:
4.37, df =2), maximum dive depth (P<0.05, Welch t-value:
3.95, df =2), and mean depth per dive (P<0.05, Welch t-
value: 3.57, df =2) being significantly higher in the Bermuda
dolphins (Table 3,Figures 2,3). For dives <60 s, the Sarasota
dolphins never exceeded a dive depth of 5 m (Figure 3A). As the
dive duration increased >60 s, so did the maximum depth and
also the variation (Figure 3A). For the Bermuda dolphins, there
was a significant increase in the dive duration as the dive depth
increased (Figure 3B). Dives <60 s showed little variation and
few exceeded 10 m (Figure 3B). As the dive duration increased
beyond 100 s, the variation in maximum dive depth increased
and dives exceeding 100 m became more common (Figure 3B).
We found no indication that the surface interval increased with
dive duration of the previous (X2=0.27, df =1, P>0.6) or next
dive X2=0.05, df =1, P>0.8).
TABLE 3 | Descriptive metrics for animals in study.
Animal ID Place Sex MbAge Length
No. dives Dives per
DD (s) Maximum dive
depth (m)
Mean depth
Surf interval (s) No. dives
>100 m
No. dives
>200 m
tt13_127b (FB90) S F 198 43 259 522 23 35 ±20 (10-129) 2 ±0 (1–10) 2 ±0 (1–8) 124 ±743 (1–1,4956) 0 0
tt15_131a (FB123) S F 166 17 241 1032 50 36 ±19 (10–128) 2 ±0 (1–5) 1 ±0 (1–4) 36 ±128 (1–2,015) 0 0
tt15_134a (FB199) S F 142 13 236 684 39 28 ±16 (10–110) 2 ±0 (2–6) 1 ±0 (1–4.1) 65 ±165 (1–3,340) 0 0
tt16_128a (FB33) S F 195 34 258 214 9 46 ±25 (10–125) 2 ±0 (2–6) 1 ±0 (1–5) 363 ±2,165 (1–22,572) 0 0
Average 175 ±26 27 ±14 248 ±12 613 ±341 30 ±18 36 ±7* 2 ±0* 1 ±0* 147 ±149
tt16_243a (Tt0019) B M 294 NA 256 491 28.1 65 ±68 (10–508) 10 ±21 (1–309) 6 ±8 (1–247) 62 ±85(1–706) 6 3
tt16_244a (Tt0021) B F 173 NA 238 805 37 63 ±81 (10–539) 12 ±37 (2–482) 8 ±18(01–280) 34 ±86 (1–1,508) 7 4
tt16_244b (Tt0022) B M 282 NA 251 513 30 82 ±86 (10–487) 20 ±38 (2–328) 12 ±17 (1–176) 37 ±68 (1–1,161) 30 11
Average 250 ±67 248 ±9 603 ±175 32 ±5 70 ±10* 14 ±5* 9 ±3* 44 ±15
Animal dataset (and ID code), dolphin population (Sarasota-S, Bermuda-B), sex (F-female, M-male), body mass (Mb, kg), straight length, average (±SD) number of dives (No. dives), average dives per hour, average dive duration (sec),
average maximum dive depth, average mean depth, and average previous surface interval. *Significant difference between Sarasota and Bermuda animals.
Frontiers in Physiology | 5July 2018 | Volume 9 | Article 838
Fahlman et al. Estimating Gas Flux in Dolphins
FIGURE 2 | Representative dive data from two bottlenose dolphins in
Sarasota Bay, Florida (red line), and Bermuda (black line). Data are plotted on
the same axes range to show the differences in diving capacity/behavior.
Pressure in ATA where 1 ATA is at the surface and 2 ATA is at 10 m depth.
Cardiac Output and Blood Flow
For both populations, we assumed that the diving ˙
Qtot was equal
to resting values measured in the bottlenose dolphins (Table 4;
Miedler et al., 2015). The blood flow distribution for the Sarasota
dolphins was able to vary greatly, due to their shorter and
shallower dive pattern. For the Bermuda dolphins, deviation
from a certain blood flow distribution caused tissues to run out
of O2. The specific variation varied slightly between individual
animals, but one distribution pattern that focused perfusion
to the central circulation, and minimized flow to the muscle,
allowed all dolphins to complete their dives aerobically (Table 4).
The blood flow required at the surface to assure that tissues
received enough blood to restore O2stores at the surface
differed between the two ecotypes. For the Sarasota dolphins,
the minimum ˙
Qtot at the surface was 3 times higher than during
diving. A surface ˙
Qtot at least 7 times higher than during diving
was required for the Bermuda population to ensure that tissues
were saturated with O2; any lower surface ˙
Qtot would result in
tissue PO2continuously decreasing with each dive. In addition,
for the Bermuda dolphins, changes in perfusion associated with
diving, i.e., the dive response, was set to occur only for dives
deeper than 20 m. Consequently, the elevated ˙
Qtot was required
at the surface to help restore blood and tissue O2stores.
Blood and Tissue Gas Tensions
In the Sarasota dolphins, there was considerable variation in end-
dive blood and tissue PO2with dive duration. In Figure 4, the
muscle is used as a representative tissue to show these variations.
In Figure 4A, the large variation in muscle PO2is shown when
the muscle tension is plotted against dive duration. There was
a consistent exponential decrease with dive depth (Figure 4B).
A decrease in the blood and tissue PO2was obvious in the
Bermuda dolphins for both dive duration (Figure 4C) and depth
FIGURE 3 | Dive depth vs. dive duration for (A) coastal Sarasota and (B)
offshore Bermuda dolphins.
TABLE 4 | Blood flow distribution (% of total cardiac output), cardiac output ( ˙
rate of O2consumption, for central circulation (CC), muscle (M), brain (B), and fat
(F) body compartments for a 200 kg dolphin for animals in Sarasota or Bermuda.
Location State Tissue ˙
Qtot ˙
CC M B F (l ·s1) (l O2·min1)
Sarasota Surface 25 65 7 3 0.301 1.34
Sarasota Dive 70 17 7 6 0.100 1.34
Bermuda Surface 60 34 4 2 0.704 1.08
Bermuda Dive 81 9 6 4 0.100 1.08
The ˙
Qtot was assumed to be resting during diving and 3 times resting while at the surface
for the Sarasota dolphins, but 7 times resting for the Bermuda dolphins. The ˙
assumed to be the same at the surface and while diving and estimated to be 2 ×the
resting metabolic rate (Table 1).
(Figure 4D). For the Bermuda dolphins, the decrease in tissue
PO2varied depending on the level of pulmonary shunt, and the
shunt decreased the end dive PO2for dives of the same duration
or maximum depth (Figures 4C,D). The effect of the shunt on
end-dive PO2was most obvious for the muscle compartment, but
was also seen in the other tissues (data not shown).
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Fahlman et al. Estimating Gas Flux in Dolphins
FIGURE 4 | Estimated end-dive muscle PO2(kPa) vs. (A,C) dive duration or (B,D) maximum dive depth (ATA, 1 ATA =98.07 kPa) in (A,B) Sarasota or (B,D)
Bermuda dolphins.
The estimated blood and tissue PO2for a representative dive
for dolphins from Sarasota (Figure 5A) or Bermuda (Figure 5B)
showed similar patterns of a decrease in PO2during a dive.
However, the longer and deeper dive duration resulted in greater
changes in blood and tissue PO2values in the offshore ecotype.
Figures 5C,D show the effect of depth on lung volume and
pulmonary shunt.
In the current study, we modeled tissue and blood PO2,
PCO2, and PN2from fine-scale empirical dive data from
bottlenose dolphins of both the coastal and offshore ecotypes
to assess potential morphological or physiological adaptations
that could help explain the large variation in dive behavior
in these divergent populations. The results shows that the
structural properties of the respiratory system have a significant
effect on pulmonary gas exchange, and these changes are
different for gases with different gas solubilities, agreeing
with past work suggesting that variation in ventilation and
perfusion may be important for managing gases during diving
(West, 1962; Farhi and Yokoyama, 1967; Hodanbosi et al.,
2016; Garcia Párraga et al., 2018). Furthermore, the results
suggest that the deeper and longer dives of the offshore
dolphins most likely reflect a greater O2storage capacity,
potentially combined with foraging of lower energetic cost.
Future tagging studies to assess the energetic requirements of
the different foraging strategies will be crucial to assess how
close to their physiological limits each of these populations are
Theoretical work has suggested that the level of gas exchange,
Qtot and blood flow distribution are important to alter blood
and tissue gas levels (Fahlman et al., 2006, 2009). Previously, we
suggested that the structural properties of the respiratory system
could have a significant effect on the level of gas exchange during
breath-hold diving (Bostrom et al., 2008; Fahlman et al., 2009),
and how man-made disturbances may alter the risk of gas emboli
through changes in the dive profile or physiology (Hooker et al.,
2009; Kvadsheim et al., 2012). However, species-specific estimates
for the structural properties of the respiratory system were not
available and published values from a range of species were used
(Bostrom et al., 2008; Fahlman et al., 2009, 2014; Hooker et al.,
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Fahlman et al. Estimating Gas Flux in Dolphins
FIGURE 5 | (A,B) Estimated central circulation, muscle, brain, fat, arterial, and venous PO2(kPa) or (C,D) estimated shunt fraction, alveolar and tracheal volume for a
long duration dive (depth in ATA, 1 ATA =98.07 kPa) in (A,C) Sarasota and (B,D) Bermuda dolphin.
2009; Kvadsheim et al., 2012), but recent work has suggested
that species-specific estimates may significantly alter the model
estimates (Hodanbosi et al., 2016). We therefore used recently
published data for respiratory compliance (Fahlman et al., 2011,
2015, 2018b), ˙
Qtot (Miedler et al., 2015), and metabolic rate
(Fahlman et al., 2015, 2018a) for coastal and offshore bottlenose
dolphin to update the model parameters. These changes altered
the compression of the alveolar space, which affects the pressure
dependence of the pulmonary shunt (Figure 1).
The updated parameters (Table 1), with stiffer airways and
more compliant alveolar space, increased the level of shunt
and reduced gas exchange throughout dives (Figures 1A,B).
This significantly reduced N2exchange during deeper dives
as the alveolar space began compressing (Figures 1C,D). The
updated parameters also affected O2exchange, but the effect
was less apparent. For CO2there was little effect, and for
longer and deeper dives, CO2exchange was improved. This
implies that variation in gas exchange from changes in the
alveolar ventilation ( ˙
VA) and ˙
Qtot relationship ( ˙
Qtot) differs
for gases with varying gas solubility (West, 1962; Farhi and
Yokoyama, 1967). These results agree with theoretical modeling
in California sea lions that showed that changes in the structural
properties of the respiratory system have a significant effect
on the exchange of O2, CO2, and N2that differs between gas
species (Hodanbosi et al., 2016). Together these studies provide
additional support for a recent hypothesis suggesting that the
lung architecture and varying ˙
Qtot would enable marine
mammals to manipulate which gases are exchanged during
diving (Garcia Párraga et al., 2018). While the current model
does not include the proposed mechanisms that would alter the
Qtot relationship, e.g., the effect of heterogeneous pulmonary
blood flow and alveolar compression (collateral ventilation), it
shows that varying the structural properties, which effectively
reduces the ˙
Qtot, the less soluble (N2) is significantly more
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Fahlman et al. Estimating Gas Flux in Dolphins
affected as compared with the more soluble gases (O2and
CO2) (West, 1962; Farhi and Yokoyama, 1967). Thus, increasing
upper airway stiffness and making the alveolar space more
compliant causes the compression to occur at shallower depth,
as originally hypothesized by Scholander (1940). This increases
the level of shunt and reduces diffusion/ventilation, which has
the greatest effect on gas with low solubility (West, 1962; Farhi
and Yokoyama, 1967). In summary, we propose that the data
in the current study agree with the suggestion that varying the
Qtot ratio may be an efficient way for deep divers to minimize
N2while still accessing pulmonary O2and CO2(Garcia Párraga
et al., 2018).
The dive behaviors for the two dolphin forms were strikingly
different, and demonstrate the large physiological plasticity in
cetacean ecotypes. While these differences in dive behavior are
undoubtedly related to differences in morphology, physiology
and environment, the data presented here provide an interesting
comparison of a species’ capacity to vary physiological traits.
Initially we used the available information for coastal dolphins
to model tissue and blood gas dynamics in both populations
(Table 2). For a 200 kg dolphin, the estimated O2stores were 8.7 l
(43.6 ml O2kg1), resulting in a calculated aerobic dive limit
(cADL) of 6.5 min when assuming a field metabolic rate that
is twice that of resting. This cADL is considerably greater than
the observed maximum dive durations in the Sarasota dolphins
ranging from 2.2 min in the current study (Table 3), or up to
4.5 min in previous work (R. Wells, unpublished observation,
Wells et al., 2013). The diet of bottlenose dolphins in Sarasota
is composed exclusively of fish (>15 different species found in
stomach content of 16 stranded animals; Barros and Wells, 1998).
Thus, their activity may require a variety of high energy activities
from rapid body turns (pinwheel feeding) to tail slaps (fish
whacking, kerpluncking) associated with prey capture (Nowacek,
2002), which would increase the daily metabolic rate and reduce
the cADL. For a cADL of 2.2–4.5 min, the Sarasota ecotype would
have a metabolic scope around 3-6 times their resting metabolic
rate (3 times the estimated field metabolic rate in Table 3). The
metabolic scope is the maximal aerobic metabolic rate divided by
the basal metabolic rate and is typically in the range of 3–10; a
scope >7 cannot be sustained over long periods (Peterson et al.,
1990). Thus, a field metabolic rate that is 6 times higher than
the resting value implies that this ecotype would be working at
or close to the maximal aerobic capacity for a cADL of 2.2 min.
However, another likely explanation is that the coastal dolphins
here operate in an environment where they are seldom limited
by their dive physiology. The bottlenose dolphins from which
dive data were obtained primarily occupy shallow waters in and
around Sarasota and Palma Sola bays, with water depths generally
<10 m, and often less than a few meters. Thus, our results
suggest that they can significantly increase their dive duration if
necessary but that they may not need this to exploit prey in their
shallow-water habitat.
The Bermuda dolphins, on the other hand, had significantly
longer dives than the Sarasota animals. A considerable number
of dives exceeded the cADL, even when calculated from twice
the resting metabolic rate, and the dolphin ran out of O2during
long dives. For this reason, we hypothesized that the offshore
dolphins must have increased O2stores to help increase their dive
duration. We are not aware of any published body composition
data for offshore delphinids, and to increase the O2stores we
therefore modeled the body compartments according to the
proposed body composition for deep-diving beaked whales, with
increased blood and muscle O2storage (Peterson et al., 1990)
that significantly increased the total O2stores (98.6 ml O2kg1),
and the cADL (18.2 min, Table 2). With a maximal dive duration
of 9 min, this provided a considerable scope for the Bermuda
dolphins. The O2storage capacity of the sperm whale (81 ml
O2kg1), hooded seal (90 ml O2kg1), elephant seal (94 ml O2
kg1), and Weddell seal (89 ml O2 kg-1, Ponganis, 2015) are
lower than our estimated value. The calculations made in the
current study are based on assumptions about the blood volume,
and muscle mass of these animals, and it is likely that the O2
storage capacity is lower and the cADL shorter. If we assume that
the longest dive represent the upper limit of the cADL, we would
need an O2storage capacity of approximately 49 ml O2kg1).
Thus, we can predict that the O2storage capacity is somewhere
between these two values for the offshore ecotype.
In addition to a greater O2storage capacity, Bermuda dolphins
may also have a greater capacity to alter diving metabolic rate.
In a previous study, we estimated the field metabolic rate of
coastal ecotype bottlenose dolphins to be around 11.7–23.4 ml
O2min1kg1. As there were no differences in the resting
metabolic rate of the coastal (Fahlman et al., 2018a) or offshore
populations (Fahlman et al., 2018b), this field metabolic rate for
offshore dolphins resulted in a cADL of 4.2–8.4 min, which is
closer to the maximum dive duration seen for these animals.
Studies have indicated that the metabolic cost during longer and
deeper dives is similar to or lower than the resting metabolic rate
at the surface (Hurley and Costa, 2001; Fahlman et al., 2013), and
deeper dives may provide cost savings as the animals may be able
to glide during long portions of the dive (Hurley and Costa, 2001;
Williams, 2001; Fahlman et al., 2013). Thus, offshore dolphins
may also have reduced cost of foraging that increases their
cADL. Assessing field metabolic rate from these two populations
using validated metabolic proxies, such as activity (acceleration,
Fahlman et al., 2008b, 2013), or heart rate (McPhee et al., 2003),
could be used to determine how energy is partitioned in this
population and resolve some of these questions. In fact, the
DTAG data provide such an opportunity and is an objective for
future studies.
The dive data from the Bermuda dolphins are suggestive of
2 different types of dives; one shallow (10–70 m, Figure 3B)
that changes little in depth with duration and another dive
type starting at around 100 m depth with a steep increase in
dive duration with depth (Figure 3B). It is not surprising that
deeper dives are generally longer, as the transit to depth is a
significant portion of the dive duration. During the deeper dives,
the pulmonary shunt alters the blood and tissue gas content, as
shown for the end-dive muscle PO2in Figure 4C. Without access
to pulmonary PO2, the blood O2was reduced and more O2used
from the muscle, pushing down end-dive PO2. This was not seen
in the shallow diving Sarasota dolphins (Figure 4A), which never
dove to depths where the pulmonary shunt began to alter gas
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Fahlman et al. Estimating Gas Flux in Dolphins
The differences in dive behavior had a significant effect on
the gas tension in the blood and tissues (Figure 5). For both
populations there was a continuous decrease in blood gases
during the dive but the decrease was more extreme for the
Bermuda dolphins (Figure 5B), and matching the blood flow
to various tissues was more restrictive. This agrees with the
suggestion made in previous modeling work that an important
aspect of the dive response is to distribute the available perfusion
to central tissues like the heart and brain, while blood flow
to the muscle should be minimal (Davis and Kanatous, 1999).
This allows muscle metabolism to be fueled by endogenous O2
and assures that the matching of utilization of endogenous and
vascular O2increases the duration of the dive that is fueled by
aerobic metabolism (Davis and Kanatous, 1999).
For both ecotypes, the ˙
Qtot while diving was assumed equal
to the resting value measured in bottlenose dolphins (Miedler
et al., 2015). The surface ˙
Qtot in the Sarasota ecotype was set to
3 times higher than resting, which sufficiently restored O2and
removed CO2from the blood and tissues to avoid continuous
changes with repeated dives. In the Bermuda animals, on the
other hand, a surface ˙
Qtot of 3 times resting was not sufficient
to restore the O2or remove the CO2during the longer dives.
Initially, ˙
Qtot was increased to 7 times higher than during diving,
but while this improved restoration of blood and tissue O2and
CO2levels, there were still continuous changes with repeated
dives. By keeping the ˙
Qtot elevated for submersions <20 m,
however, we were able to sufficiently restore O2and remove
enough CO2to prevent accumulating changes across repeated
dives. These results suggest that ˙
Qtot needs to be maintained
during intervening short and shallow dives to allow restoration of
normal blood and tissue gas tensions. Staying submerged during
this time may help increase the PO2and thereby the uptake
of O2. The suggestion that there is little or no cardiovascular
modification during shallow dives may be controversial, as most
studies have reported changes in heart rate during diving. For
example, in the bottlenose dolphin resting at the surface or
while submerged the average heart rate were 105 and 40 beats
min1, respectively (Noren et al., 2012). However, the past
study provides an estimated surface resting heart rate that is
influenced by the respiratory sinus arrhythmia (RSA), which will
significantly elevate the resting values. In a more recent paper the
surface resting heart rate when accounting for the RSA ranged
from 27 to 54 beats min1(Miedler et al., 2015), thus not very
different from the resting diving heart rate reported by Noren
et al. (2012). In addition, in the past study it was also reported
that the diving heart rate increased with underwater activity by
between 40 and 79% (Noren et al., 2012). While our estimated
Qtot at depths shallower than 20 m may be overestimated, there
is experimental evidence that the perfusion is modulated while
submerged and future studies could look at how this changes
during short and shallow dives.
In the Sarasota dolphins, the dive depth caused a reduction
in alveolar volume, but the low pressure did not cause tracheal
compression or induce a pulmonary shunt (Figure 5C). In
the Bermuda dolphins, the arterial PO2increased during the
descent to a maximum value, and then rapidly declined until
the alveoli were reinflated during the ascent at which a second
peak was observed (Figure 5B). We previously suggested that
this pattern of arterial gas tension would support Scholander’s
hypothesis of pressure-induced hyperoxia as the lungs are
compressed, followed by an increasing shunt as the alveoli are
compressed until atelectasis (alveolar collapse), in this case at
126 m (Figure 5D), when the arterial side reflects the mixed
venous (Fahlman et al., 2009; McDonald and Ponganis, 2012).
This is supported by empirically measured arterial and venous
gas tensions in both seals (Falke et al., 1985) and sea lions
(McDonald and Ponganis, 2012). As the dolphin ascends, the
alveoli are recruited at a depth of 126 m and gas exchange
commences again. At this point, there is a second peak as
pulmonary O2again saturates the blood (Figures 5C,D). The
second peak for arterial PO2is lower as compared with the
peak right before atelectasis, despite equivalent pulmonary PO2.
During the dive, the O2in the blood is continuously consumed,
causing both the arterial and venous PO2to decrease. As the
alveoli are recruited at depth, the pulmonary PO2increases.
The high pulmonary and low venous PO2result in an elevated
partial pressure gradient that favors diffusion and gas exchange.
Thus, pulmonary O2diffuses into the pulmonary capillary and
helps saturate the arterial blood. In addition, CO2is removed
from the blood into the lung. Both these processes help prepare
the dolphin to minimize the duration of the surface interval as
CO2is being removed and O2being taken up before reaching
the surface. Elevated gas exchange at depth also increases N2
exchange, increasing the tissue and blood tension and the risk
for gas emboli. However, the elevated pulmonary pressure as the
alveoli open results in an elevated ˙
Qtot ratio, favoring O2
and CO2exchange, while limiting N2exchange (Garcia Párraga
et al., 2018). In addition, it has been hypothesized that marine
mammals are able to separate the lung into two regions; one
region that is ventilated and another atelactic area, with the
latter being perfused (Garcia Párraga et al., 2018). This matching
of pulmonary blood flow to hypoxic/atelactic regions result
in selective gas exchange (Olson et al., 2010; Garcia Párraga
et al., 2018), which during normal dives would help reduce the
risk for gas emboli, and help prepare the dolphin to restore
the O2used and removing the CO2produced (West, 1962;
Farhi and Yokoyama, 1967; Olson et al., 2010). There is also
evidence for an arterio-venous shunt that alters the blood gas
tensions and could help minimize inert gas uptake during the
ascent and help arterialize venous blood (Garcia Párraga et al.,
In a number of marine mammals, there is an anticipatory pre-
surfacing tachycardia, which likely increases ˙
Qtot (Fedak et al.,
1988; Thompson and Fedak, 1993; Andrews et al., 1997; Noren
et al., 2012; Williams et al., 2017). During natural undisturbed
dives, it seems that the change in heart rate begins during the
initial stages of the ascent, but a large increase occurs during the
later stages of the ascent close to the surface. Close to the surface,
the blood and tissue tension would be supersaturated with N2
and the gas would move from the tissues to the lungs (Fahlman
et al., 2009). Elevated ˙
Qtot at this stage of the dive would result in
a decrease in the ˙
Qtot ratio, which would enhance exchange
and removal of N2. It has been hypothesized that disturbance
of normal diving homeostasis, such as exposure to man-made
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Fahlman et al. Estimating Gas Flux in Dolphins
sound, capture in nets, or any stressful situation may alter the
physiology and result in conditions that enhance N2uptake and
the risk for gas emboli (Fernandez et al., 2005; Hooker et al.,
2009; Fahlman et al., 2014; García-Párraga et al., 2014). In turtles,
it has been suggested that the stress associated with incidental
capture in fishing gear result in a sympathetic response, which
opens the arterial pulmonary sphincter, increases pulmonary
blood flow, decreases the ˙
Qtot ratio and increase N2uptake
and risk of gas emboli (García-Párraga et al., 2014, 2017; Fahlman
et al., 2017a). In cetaceans, active management of the pulmonary
perfusion has been hypothesized as a mechanism that allow the
cetaceans to vary the level of the ˙
Qtot match in the lung, and
develop a shunt even at shallow depths that does not depend
on hydrostatic compression (Garcia Párraga et al., 2018). Similar
to the turtles, stress in cetaceans may also alter perfusion and
the ˙
Qtot relationship causing increased pulmonary blood flow,
increased uptake of N2and risk of gas emboli (Fahlman et al.,
2006; Hooker et al., 2009). Theoretical modeling has indicated
that stress related changes in ˙
Qtot may increase the risk for
gas emboli, and empirical data in the narwhal indicate that
the large changes in the diving heart rate occurs deeper under
stressful situations (around 170 m) as compared with natural
dives (Fahlman et al., 2009, 2014; Hooker et al., 2009; Williams
et al., 2017). Thus, this reversal of the diving bradycardia may
result in elevated pulmonary blood flow, changes in blood flow
distribution within the lung and changes in ˙
Qtot, resulting in
elevated N2uptake and risk for gas emboli (Garcia Párraga et al.,
In summary, in the current study we show that the dive
behavior in deep diving bottlenose dolphins likely requires
morphological differences resulting in a greater O2storage
capacity as compared with the coastal ecotype. It is also
possible that the foraging behavior of the offshore population,
with longer periods of gliding, results in lower foraging
metabolic costs. Our results also indicate the importance of
species-specific data when predicting physiological responses
of animals. By updating the compliance estimates for the
respiratory system, we show additional evidence of how
variation in the ventilation/perfusion relationship is able to
alter exchange of gases. This result provides additional support
for our hypothesis of how marine mammals manage gases
during diving and how stress may alter physiology and
cause increased N2uptake and risk of gas emboli from
The theoretical model and data used in this paper are made freely
available at:
AF helped collect the dive data, performed the modeling work,
data analysis, wrote the first draft of the paper. FHJ collected and
extracted the dive data, and helped edit the paper. PT provided
the tools to collect the dive data, and helped edit the paper. RW
helped collect the dive data and edited the paper.
AF (N00014-17-1-2756), PT (N000141512553) and FHJ
(N00014-14-1-0410) were supported by the Office of Naval
Research, and FHJ by an AIASCOFUND fellowship from Aarhus
Institute of Advanced Studies, Aarhus University, under EU’s
FP7 program (Agreement No. 609033). PT received funding
from the MASTS pooling initiative (The Marine Alliance for
Science and Technology for Scotland) and their support is
gratefully acknowledged. MASTS is funded by the Scottish
Funding Council (grant reference HR09011) and contributing
institutions. Funding for the Sarasota Bay and Bermuda field-
work was provided by Dolphin Quest, Inc., and Office of Naval
Research (N00014-14-1-0563).
A special thanks to the many volunteers and staff at Dolphin
Quest and the Sarasota Dolphin Research Project who made
collection of the dive data possible. A special thanks to Nigel
Pollard, the Bermuda Government, the Bermuda Aquarium,
Museum and Zoo (BAMZ), and NOAA.
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Conflict of Interest Statement: The authors declare that the research was
conducted in the absence of any commercial or financial relationships that could
be construed as a potential conflict of interest.
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Frontiers in Physiology | 13 July 2018 | Volume 9 | Article 838
... logM b . The triangles and squares are the estimated end-dive mixed venous N 2 tension for the dolphin (M b = 294 kg; Fahlman et al., 2018b) and Steller sea lion (M b = 210 kg; Hodanbosi et al., 2016), respectively. The blue symbols represent model estimates with structural lung parameters from terrestrial mammals as presented previously (Bostrom et al., 2008), and the red with species-specific parameters (Hodanbosi et al., 2016;Fahlman et al., 2018b). ...
... The triangles and squares are the estimated end-dive mixed venous N 2 tension for the dolphin (M b = 294 kg; Fahlman et al., 2018b) and Steller sea lion (M b = 210 kg; Hodanbosi et al., 2016), respectively. The blue symbols represent model estimates with structural lung parameters from terrestrial mammals as presented previously (Bostrom et al., 2008), and the red with species-specific parameters (Hodanbosi et al., 2016;Fahlman et al., 2018b). The dolphin data represent the end-dive mixed venous N 2 tension following a single dive to 140 m, while sea lion 4 repeated dives to 40 m. ...
... Recent studies in the California sea lion (Zalophus californianus) provided empirical evidence for these theoretical results, and suggested that the alveolar collapse depth occurs at depths exceeding 200 m (McDonald and Ponganis, 2012Ponganis, , 2013. The theoretical modeling (Bostrom et al., 2008;Fahlman et al., 2009Fahlman et al., , 2018bHodanbosi et al., 2016), based on data from studies that defined the structural properties of the respiratory system (Denison et al., 1971;Denison and Kooyman, 1973;Leith, 1976;Piscitelli et al., 2010;Fahlman et al., 2011Fahlman et al., , 2014aFahlman et al., , 2015Fahlman et al., , 2018aFahlman et al., ,c, 2020aMoore C. et al., 2014;Fahlman and Madigan, 2016;Denk et al., 2020), agrees with these empirical estimates for alveolar collapse depths and cessation of gas exchange in the California sea lion, and also the elephant seal (Mirounga angustirostris), and Weddell seal (Leptonychotes weddellii) (Kooyman et al., 1972;Kooyman and Sinnett, 1982;Fahlman et al., 2009;Hodanbosi et al., 2016). ...
Full-text available
Decompression theory has been mainly based on studies on terrestrial mammals, and may not translate well to marine mammals. However, evidence that marine mammals experience gas bubbles during diving is growing, causing concern that these bubbles may cause gas emboli pathology (GEP) under unusual circumstances. Marine mammal management, and usual avoidance, of gas emboli and GEP, or the bends, became a topic of intense scientific interest after sonar-exposed, mass-stranded deep-diving whales were observed with gas bubbles. Theoretical models, based on our current understanding of diving physiology in cetaceans, predict that the tissue and blood N 2 levels in the bottlenose dolphin ( Tursiops truncatus ) are at levels that would result in severe DCS symptoms in similar sized terrestrial mammals. However, the dolphins appear to have physiological or behavioral mechanisms to avoid excessive blood N 2 levels, or may be more resistant to circulating bubbles through immunological/biochemical adaptations. Studies on behavior, anatomy and physiology of marine mammals have enhanced our understanding of the mechanisms that are thought to prevent excessive uptake of N 2 . This has led to the selective gas exchange hypothesis, which provides a mechanism how stress-induced behavioral change may cause failure of the normal physiology, which results in excessive uptake of N 2 , and in extreme cases may cause formation of symptomatic gas emboli. Studies on cardiorespiratory function have been integral to the development of this hypothesis, with work initially being conducted on excised tissues and cadavers, followed by studies on anesthetized animals or trained animals under human care. These studies enabled research on free-ranging common bottlenose dolphins in Sarasota Bay, FL, and off Bermuda, and have included work on the metabolic and cardiorespiratory physiology of both shallow- and deep-diving dolphins and have been integral to better understand how cetaceans can dive to extreme depths, for long durations.
... The gases are then transported via the vascular system throughout the various tissues of the body (Fahlman et al., 2006. The amount of gas that dissolves into the tissues during a dive is, therefore, influenced by the level of gas exchange in the lungs, cardiac output (heart rate and stroke volume), blood flow distribution, and tissue perfusion (Fahlman et al., 2006(Fahlman et al., , 2018. Initially, the rate at which gas diffuses across the lungs increases with depth as higher hydrostatic pressures increase the quantity of gas forced into solution in the blood (Scholander, 1940;Berkson, 1967). ...
... Our goal in this study was to develop a baseline model to estimate the risk of GE formation in sea turtles. To build this model, we built upon a published model for estimating gas tissue N 2 , O 2 , and CO 2 tensions of marine mammals and penguins (Fahlman et al., 2006(Fahlman et al., , 2007(Fahlman et al., , 2018(Fahlman et al., , 2021 and adapted it for use with loggerhead turtles, green turtles (Chelonia mydas), and leatherback turtles (Dermochelys coriacea). While there are many anatomical and physiological differences between marine mammals/ penguins and sea turtles, building off these earlier models provided us with an initial framework for modeling gas dynamics that had been previously validated for use with air-breathing vertebrates. ...
... To estimate gas dynamics in diving sea turtles, we adapted a model that was developed for estimating blood and gas tissue N 2 , O 2 , and CO 2 tensions in marine mammals and penguins (Fahlman et al., 2006(Fahlman et al., , 2007(Fahlman et al., , 2018(Fahlman et al., , 2021). In the model, gas exchange first occurs between the respiratory system and arterial blood, and then between the arterial blood and four compartments: (1) the brain; (2) fat and bone; (3) the central circulatory system, which included the heart, kidney, liver, and digestive tract but not blood; and (4) muscle, which included muscle, skin, connective tissue, and all other tissues and organs that were not included in the other compartments. ...
Full-text available
Sea turtles, like other air-breathing diving vertebrates, commonly experience significant gas embolism (GE) when incidentally caught at depth in fishing gear and brought to the surface. To better understand why sea turtles develop GE, we built a mathematical model to estimate partial pressures of N 2 (PN 2), O 2 (PO 2), and CO 2 (PCO 2) in the major body-compartments of diving loggerheads (Caretta caretta), leatherbacks (Dermochelys coriacea), and green turtles (Chelonia mydas). This model was adapted from a published model for estimating gas dynamics in marine mammals and penguins. To parameterize the sea turtle model, we used values gleaned from previously published literature and 22 necropsies. Next, we applied this model to data collected from free-roaming individuals of the three study species. Finally, we varied body-condition and cardiac output within the model to see how these factors affected the risk of GE. Our model suggests that cardiac output likely plays a significant role in the modulation of GE, especially in the deeper diving leatherback turtles. This baseline model also indicates that even during routine diving behavior, sea turtles are at high risk of GE. This likely means that turtles have additional behavioral, anatomical, and/or physiologic adaptions that serve to reduce the probability of GE but were not incorporated in this model. Identifying these adaptations and incorporating them into future iterations of this model will further reveal the factors driving GE in sea turtles.
... Although the patterns we observed in this study have previously been observed in many marine mammal species, the potential relationship between RSA and apnea has been studied in pinnipeds, but not cetaceans, which are fully aquatic, obligate divers (Castellini et al., 1994b). In contrast to those during diving, circulatory adjustments during surface intervals should increase perfusion to maximize gas exchange and minimize time spent during an otherwise unproductive state (Fahlman et al., 2020b(Fahlman et al., , 2018Fedak et al., 1988). For example, the rapid increase in if H of the RSA may be important in generating an increase in peripheral perfusion to quickly replenish muscle and blood O 2 stores as a clustering of heart beats has been shown to improve O 2 uptake and reduce the physiological dead space to V T ratio in humans (Arieli and Farhi, 1985;Yasuma and Hayano, 2004). ...
... The researchers suggested that for dives shorter than the ADL, bradycardia during diving could be regulated by a similar mechanism of cardiorespiratory control to that which drives RSA and that further reduction in f H only occurs during dives past the ADL. Our data agree with this finding given that the 2 min breath-holds should be well within the calculated ADL of 6.5 min and the measured ADL of approximately 4 min of bottlenose dolphins (Fahlman et al., 2018;Williams et al., 1999). ...
Among the many factors that influence the cardiovascular adjustments of marine mammals is the act of respiration at the surface, which facilitates rapid gas exchange and tissue re-perfusion between dives. We measured heart rate ( f H ) in six, adult male bottlenose dolphins ( Tursiops truncatus ) spontaneously breathing at the surface to quantify the relationship between respiration and f H , and compared this to f H during submerged breath-holds. We found that dolphins exhibit a pronounced respiratory sinus arrhythmia (RSA) during surface breathing resulting in a rapid increase in f H after a breath followed by a gradual decrease over the following 15-20 seconds to a steady f H that is maintained until the following breath. RSA resulted in a maximum instantaneous f H (i f H ) of 87.4±13.6 beats min ⁻¹ , a minimum i f H of 56.8±14.8 beats min ⁻¹ , and the degree of RSA was positively correlated with the inter-breath interval (IBI). The minimum i f H during 2-minute, submerged breath-holds where dolphins exhibited submersion bradycardia (36.4±9.0 beats min ⁻¹ ) was lower than the minimum i f H observed during an average IBI, however during IBIs longer than 30 seconds, the minimum i f H (38.7±10.6 beats min ⁻¹ ) was not significantly different from that during 2-minute breath-holds. These results demonstrate that the f H patterns observed during submerged breath-holds are similar to those resulting from RSA during an extended IBI. Here we highlight the importance of RSA in influencing f H variability and emphasize the need to understand its relationship to submersion bradycardia.
... contrast to those during AQ4 ¶ diving, circulatory adjustments during surface intervals should increase perfusion to maximize gas exchange and minimize time spent during an otherwise unproductive state (Fahlman et al., 2020b(Fahlman et al., , 2018Fedak et al., 1988). For example, the rapid increase in if H of the RSA may be important in generating an increase in peripheral perfusion to quickly replenish muscle and blood O 2 stores as a clustering of heart beats has been shown to improve O 2 uptake and reduce the physiological dead space to V T ratio in humans (Arieli and Farhi, 1985;Yasuma and Hayano, 2004). ...
... The researchers suggested that for dives shorter than the ADL, bradycardia during diving could be regulated by a similar mechanism of cardiorespiratory control to that which drives RSA, and that further reduction in f H only occurs during dives past the ADL. Our data agree with this finding given that the 2 min breath-holds should be well within the calculated ADL of 6.5 min and the measured ADL of approximately 4 min in the animals in this study (Fahlman et al., 2018;Williams et al., 1999). ...
In the present study, we examined lung function in healthy resting adult (born in 2003) Pacific walruses ( Odobenus rosmarus divergens ) by measuring respiratory flow ( V̇ ) using a custom-made pneumotachometer. Three female walruses (670 – 1025 kg) voluntarily participated in spirometry trials while spontaneously breathing on land (sitting and lying down in sternal recumbency) and floating in water. While sitting, two walruses performed active respiratory efforts, and one animal participated in lung compliance measurements. For spontaneous breaths, V̇ was lower when lying down (e.g. expiration: 7.1±1.2 l · s ⁻¹ ) as compared to when in water (9.9±1.4 l · s ⁻¹ ), while tidal volume ( V T , 11.5±4.6 l), breath duration (4.6±1.4 s), and respiratory frequency (7.6±2.2 breaths · min ⁻¹ ) remained the same. The measured V T and specific dynamic lung compliance (0.32±0.07 cmH 2 O ⁻¹ ) for spontaneous breaths, were higher than those estimated for similarly sized terrestrial mammals. The V T increased with body mass (allometric mass-exponent=1.29) and ranged from 3 to 43% of the estimated total lung capacity (TLC est ) for spontaneous breaths. When normalized for TLC est , the maximal expiratory V̇ ( V̇ exp ) was higher than that estimated in phocids, but lower than that reported in cetaceans and the California sea lion. The V̇ exp was maintained over all lung volumes during spontaneous and active respiratory manoeuvres. We conclude that location (water or land) affects lung function in the walrus and should be considered when studying respiratory physiology in semi-aquatic marine mammals.
... Large variations in dive behavior and home range exist within bottlenose dolphins [58][59][60]. Differences in cardiac output between the deep-diving and estuarine/coastal dolphins have been documented and hypothesized to be a result of their different diving behavior [61]. Estuarine/coastal bottlenose dolphins, like those in SB and BB, live close to shore and tend to perform short, shallow dives [58], versus offshore dolphins, living in deeper waters and routinely deep diving [62]. ...
Full-text available
The Deepwater Horizon (DWH) oil spill profoundly impacted the health of bottlenose dolphins ( Tursiops truncatus ) in Barataria Bay, LA (BB). To comprehensively assess the cardiac health of dolphins living within the DWH oil spill footprint, techniques for in-water cardiac evaluation were refined with dolphins cared for by the U.S. Navy Marine Mammal Program in 2018 and applied to free-ranging bottlenose dolphins in BB ( n = 34) and Sarasota Bay, Florida (SB) ( n = 19), a non-oiled reference population. Cardiac auscultation detected systolic murmurs in the majority of dolphins from both sites (88% BB, 89% SB) and echocardiography showed most of the murmurs were innocent flow murmurs attributed to elevated blood flow velocity [1]. Telemetric six-lead electrocardiography detected arrhythmias in BB dolphins (43%) and SB dolphins (31%), all of which were considered low to moderate risk for adverse cardiac events. Echocardiography showed BB dolphins had thinner left ventricular walls, with significant differences in intraventricular septum thickness at the end of diastole ( p = 0.002), and left ventricular posterior wall thickness at the end of diastole ( p = 0.033). BB dolphins also had smaller left atrial size ( p = 0.004), higher prevalence of tricuspid valve prolapse ( p = 0.003), higher prevalence of tricuspid valve thickening ( p = 0.033), and higher prevalence of aortic valve thickening ( p = 0.008). Two dolphins in BB were diagnosed with pulmonary arterial hypertension based on Doppler echocardiography-derived estimates and supporting echocardiographic findings. Histopathology of dolphins who stranded within the DWH oil spill footprint showed a significantly higher prevalence of myocardial fibrosis ( p = 0.003), regardless of age, compared to dolphins outside the oil spill footprint. In conclusion, there were substantial cardiac abnormalities identified in BB dolphins which may be related to DWH oil exposure, however, future work is needed to rule out other hypotheses and further elucidate the connection between oil exposure, pulmonary disease, and the observed cardiac abnormalities.
... We also identified candidate genes and pathways with timedependent changes in expression throughout the breath holds that were validated in functional studies using independently collected samples and assays. These molecular changes occurred within the calculated aerobic dive limit (cADL) of bottlenose dolphins-the duration of a dive that can be sustained without requiring anaerobic respiration at the cellular level, which has been estimated to be approximately 6.5 min [59]. It is also worth considering the possibility that changes in gene expression could occur to support specific physiological responses to diving during a dive, and that this gene expression differs when the animal is at the surface. ...
Background and objectives: Ischemic events, such as ischemic heart disease and stroke, are the number one cause of death globally. Ischemia prevents blood, carrying essential nutrients and oxygen, from reaching tissues, leading to cell and tissue death, and eventual organ failure. While humans are relatively intolerant to ischemic events, other species, such as marine mammals, have evolved a unique tolerance to chronic ischemia/reperfusion during apneic diving. To identify possible molecular features of an increased tolerance for apnea, we examined changes in gene expression in breath-holding dolphins. Methodology: Here, we capitalized on the adaptations possesed by bottlenose dolphins (Tursiops truncatus) for diving as a comparative model of ischemic stress and hypoxia tolerance to identify molecular features associated with breath holding. Given that signals in the blood may influence physiological changes during diving, we used RNA-Seq and enzyme assays to examine time-dependent changes in gene expression in the blood of breath-holding dolphins. Results: We observed time-dependent upregulation of the arachidonate 5-lipoxygenase (ALOX5) gene and increased lipoxygenase activity during breath holding. ALOX5 has been shown to be activated during hypoxia in rodent models, and its metabolites, leukotrienes, induce vasoconstriction. Conclusions and implications: The upregulation of ALOX5 mRNA occurred within the calculated aerobic dive limit of the species, suggesting that ALOX5 may play a role in the dolphin's physiological response to diving, particularly in a pro-inflammatory response to ischemia and in promoting vasoconstriction. These observations pinpoint a potential molecular mechanism by which dolphins, and perhaps other marine mammals, respond to the prolonged breath holds associated with diving.
... Marine mammals also show considerable plasticity in cardiac function during surface intervals. While breathing at the surface marine mammals demonstrate respiratory sinus arrhythmia (RSA), like other terrestrial mammals including humans, where the if H oscillates in synchrony with the respiratory rate ( f R ) [13,[17][18][19][20][21][22]. The mechanism of RSA is understood to be a central phenomenon of respiratory modulation via cardiac vagal stimulation, but its physiological role is less well understood [23][24][25]. ...
Plasticity in the cardiac function of a marine mammal facilitates rapid adjustments to the contrasting metabolic demands of breathing at the surface and diving during an extended apnea. By matching their heart rate ( f H ) to their immediate physiological needs, a marine mammal can improve its metabolic efficiency and maximize the proportion of time spent underwater. Respiratory sinus arrhythmia (RSA) is a known modulation of f H that is driven by respiration and has been suggested to increase cardiorespiratory efficiency. To investigate the presence of RSA in cetaceans and the relationship between f H , breathing rate ( f R ) and body mass ( M b ), we measured simultaneous f H and f R in five cetacean species in human care. We found that a higher f R was associated with a higher mean instantaneous f H (i f H ) and minimum i f H of the RSA. By contrast, f H scaled inversely with M b such that larger animals had lower mean and minimum i f H s of the RSA. There was a significant allometric relationship between maximum i f H of the RSA and M b , but not f R , which may indicate that this parameter is set by physical laws and not adjusted dynamically with physiological needs. RSA was significantly affected by f R and was greatly reduced with small increases in f R . Ultimately, these data show that surface f H s of cetaceans are complex and the f H patterns we observed are controlled by several factors. We suggest the importance of considering RSA when interpreting f H measurements and particularly how f R may drive f H changes that are important for efficient gas exchange. This article is part of the theme issue ‘Measuring physiology in free-living animals (Part I)’.
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Decompression sickness (DCS), clinically diagnosed by reversal of symptoms after recompression treatment, has never been reported in breath hold divers, despite the predictable occurrence in their tissues when nitrogen stresses high enough to lead to bubble formation and lesions based on studies in terrestrial experimental models. In marine mammals, lesions compatible with DCS were described in post mortem studies, in cases where altered diving behavior is assumed because of exposure to high-powered underwater acoustic sources (e.g., active military sonar) and in cases of animals accidentally caught at depth in fisheries. In sea turtles, despite the abundant literature on diving physiology and work on the disruption caused to animals by accidental capture, this is the first report of gas embolism (GE) and DCS in this group. This Thesis is the most comprehensive compilation to date of the disease in any diving vertebrate: it provides evidence of its existence including associated symptoms and lesions, describes diagnostic and therapeutic options, and provides preliminary data on the impact of the disease in the clinical setting of a rehabilitation center as well as under field conditions on board fishing vessels. The study compiles for the first-time information on this new clinic-pathological entity based on more than 300 affected loggerhead turtles (Caretta caretta) as well as isolated specimens of green turtle (Chelonia mydas), olive ridley turtle (Lepidochelys olivacea) and leatherback turtle (Dermochelys coriacea). The work is based on the study of a total of 497 cases recovered from fishing trawls and gillnets in the Valencian Community, as well as in trawlers in Brazil and Italy, studying the presence of the disease and its impact on the animals both on arrival at the rehabilitation center and in its early phase while on board. The severity of the embolism, as well as the characterization of the associated lesions in vital organs have been assessed in the different studies by conventional radiography, computed axial tomography, magnetic resonance imaging, ultrasound, and post mortem examination. In the latter, gas embolism has also been confirmed and characterized in a manner very similar to that described in cetaceans suspected of decompression-associated GE. The incidence of GE was 57% on arrival at the rehabilitation center and 100% immediately after bottom trawl capture. We provide evidence that environmental factors such as water temperature, depth and net setting times correlate with the mortality of turtles caught accidentally. Likewise, the type of fishery (trawl/gillnet), the presence of seawater aspiration, the severity of the embolism, or the level of consciousness in the first neurological examination after recovery from nets on board, also condition survival. On the other hand, the severity of the embolism suffered in animals received at the rehabilitation center was associated with the type of fishery, the depth of the gear, the presence of seawater aspiration and the size of the turtle (CCL and weight). At the rehabilitation center, the overall mortality (including those admitted dead) associated with embolism cases (28.91%) was almost 8 times higher than mortality in the non-embolism group (3.76%). However, the survival rate of affected animals that arrived alive and could be treated by specific hyperbaric oxygen therapy (HBOT) exceeded 90%. In surveys on board fishing vessels, total 30-day mortality ranged from 44% to 63%. Survival of animals in good condition that could be tagged and released back (excluding those that died on board) was 63.88%, which would imply 1 in 3 direct reintroductions. The discovery of DCS in sea turtles opens a new era for research in diving physiology not only in turtles but also in other diving vertebrates, raising new hypotheses or models potentially applicable to other groups of pulmonates including humans and other diving marine vertebrates. In addition, it calls for reviewing and rethinking new strategies to mitigate the mortality associated in the short, medium, and long term with bycatch in order to mitigate the impact of fisheries on turtle populations, favoring their conservation.
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Introduction Physical activity promotes physical, psychological and social health. Despite this, almost half of middle-aged (35–54 years) Australian men are insufficiently active. Exercise adherence is increased with social interaction in a group setting. Team sport can leverage the power of groups and has shown to be more intrinsically motivating than discrete exercise modes. Evaluation of the effect of team sport compared with traditional group exercise on health, particularly psychological and social health, and physical activity levels of middle-aged men is limited. This study aims to compare the effects of team sport participation and group circuit training on physical activity levels and health in insufficiently active middle-aged men. Methods and analysis In this parallel randomised controlled trial, n = 128 men aged 35–54 years will complete a 12-week team sport or group circuit exercise programme. Participants must self-report to not be meeting Australian physical activity guidelines or participating in team sport before recruitment. Health-related quality of life, exercise motivation, psychological needs satisfaction, sleep and physical activity levels (accelerometry), blood lipids, glucose and metabolic syndrome risk score will be assessed at baseline, end of the programme and 12 weeks follow-up. Linear mixed effect models will be used. Ethics and dissemination The study has received ethical approval from the University of South Australia’s Human Research Ethics Committee (Ethics Protocol 203274). Study results will be disseminated via publication in disciplinary-specific journals, conference presentations, and as part of a Doctoral thesis. Trial registration number ANCTRN12621000483853.
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In some fishes, the ability to breathe air has evolved to overcome constraints in hypoxic environments but comes at a cost of increased predation. To reduce this risk, some species perform group air breathing. Temperature may also affect the frequency of air breathing in fishes, but this topic has received relatively little research attention. This study examined how acclimation temperature and acute exposure to hypoxia affected the air-breathing behaviour of a social catfish, the bronze corydoras Corydoras aeneus , and aimed to determine whether individual oxygen demand influenced the behaviour of entire groups. Groups of seven fish were observed in an arena to measure air-breathing frequency of individuals and consequent group air-breathing behaviour, under three oxygen concentrations (100%, 60% and 20% air saturation) and two acclimation temperatures (25 and 30°C). Intermittent flow respirometry was used to estimate oxygen demand of individuals. Increasingly severe hypoxia increased air breathing at the individual and group levels. Although there were minimal differences in air-breathing frequency among individuals in response to an increase in temperature, the effect of temperature that did exist manifested as an increase in group air-breathing frequency at 30°C. Groups that were more socially cohesive during routine activity took more breaths but, in most cases, air breathing among individuals was not temporally clustered. There was no association between an individual's oxygen demand and its air-breathing frequency in a group. For C . aeneus , although air-breathing frequency is influenced by hypoxia, behavioural variation among groups could explain the small overall effect of temperature on group air-breathing frequency.
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Diving mammals have evolved a suite of physiological adaptations to manage respiratory gases during extended breath-hold dives. To test the hypothesis that offshore bottlenose dolphins have evolved physiological adaptations to improve their ability for extended deep dives and as protection for lung barotrauma, we investigated the lung function and respiratory physiology of four wild common bottlenose dolphins (Tursiops truncatus) near the island of Bermuda. We measured blood hematocrit (Hct, %), resting metabolic rate (RMR, l O 2 · min −1), tidal volume (V T , l), respiratory frequency (f R , breaths · min −1), respiratory flow (l · min −1), and dynamic lung compliance (C L , l · cmH 2 O −1) in air and in water, and compared measurements with published results from coastal, shallow-diving dolphins. We found that offshore dolphins had greater Hct (56 ± 2%) compared to shallow-diving bottlenose dolphins (range: 30-49%), thus resulting in a greater O 2 storage capacity and longer aerobic diving duration. Contrary to our hypothesis, the specific C L (sC L , 0.30 ± 0.12 cmH 2 O −1) was not different between populations. Neither the mass-specific RMR (3.0 ± 1.7 ml O 2 · min −1 · kg −1) nor V T (23.0 ± 3.7 ml · kg −1) were different from coastal ecotype bottlenose dolphins, both in the wild and under managed care, suggesting that deep-diving dolphins do not have metabolic or respiratory adaptations that differ from the shallow-diving ecotypes. The lack of respiratory adaptations for deep diving further support the recently developed hypothesis that gas management in cetaceans is not entirely passive but governed by alteration in the ventilation-perfusion matching, which allows for selective gas exchange to protect against diving related problems such as decompression sickness.
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Hydrostatic lung compression in diving marine mammals, with collapsing alveoli blocking gas exchange at depth, has been the main theoretical basis for limiting N2 uptake and avoiding gas emboli (GE) as they ascend. However, studies of beached and bycaught cetaceans and sea turtles imply that air-breathing marine vertebrates may, under unusual circumstances, develop GE that result in decompression sickness (DCS) symptoms. Theoretical modelling of tissue and blood gas dynamics of breath-hold divers suggests that changes in perfusion and blood flow distribution may also play a significant role. The results from the modelling work suggest that our current understanding of diving physiology in many species is poor, as the models predict blood and tissue N2 levels that would result in severe DCS symptoms (chokes, paralysis and death) in a large fraction of natural dive profiles. In this review, we combine published results from marine mammals and turtles to propose alternative mechanisms for how marine vertebrates control gas exchange in the lung, through management of the pulmonary distribution of alveolar ventilation ([Formula: see text]) and cardiac output/lung perfusion ([Formula: see text]), varying the level of [Formula: see text] in different regions of the lung. Man-made disturbances, causing stress, could alter the [Formula: see text] mismatch level in the lung, resulting in an abnormally elevated uptake of N2, increasing the risk for GE. Our hypothesis provides avenues for new areas of research, offers an explanation for how sonar exposure may alter physiology causing GE and provides a new mechanism for how air-breathing marine vertebrates usually avoid the diving-related problems observed in human divers.
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We measured respiratory flow rates, and expired O2 in 32 (2-34 years, body mass [Mb] range: 73-291 kg) common bottlenose dolphins (Tursiops truncatus) during voluntary breaths on land or in water (between 2014 and 2017). The data were used to measure the resting O2 consumption rate (VO2, range: 0.76-9.45 ml O2 min⁻¹ kg⁻¹) and tidal volume (VT, range: 2.2-10.4 l) during rest. For adult dolphins, the resting VT, but not VO2, correlated with body mass (Mb, range: 141-291 kg) with an allometric mass-exponent of 0.41. These data suggest that the mass-specific VT of larger dolphins decreases considerably more than that of terrestrial mammals (mass-exponent: 1.03). The average resting sVO2 was similar to previously published metabolic measurements from the same species. Our data indicate that the resting metabolic rate for a 150 kg dolphin would be 3.9 ml O2 min⁻¹ kg⁻¹, and the metabolic rate for active animals, assuming a multiplier of 3-6, would range from 11.7 to 23.4 ml O2 min⁻¹ kg⁻¹ absbreak Our measurements provide novel data for resting energy use and respiratory physiology in wild cetaceans, which may have significant value for conservation efforts and for understanding the bioenergetic requirements of this species.
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Incidental capture, or ‘bycatch’ in fishing gear is a major global threat to sea turtle populations. A recent study showed that underwater entrapment in fishing gear followed by rapid decompression may cause gas bubble formation within the blood stream (embolism) and tissues leading to organ injury, impairment, and even mortality in some bycaught individuals. We analyzed data from 128 capture events using logistic and ordinal regression to examine risk factors associated with gas embolism in sea turtles captured in trawls and gillnets. Likelihood of fatal decompression increases with increasing depth of gear deployment. A direct relationship was found between depth, risk and severity of embolism, which has not been previously demonstrated in any breath-hold diving species. For the trawl fishery in this study, an average trawl depth of 65 m was estimated to result in 50% mortality in by-caught turtles throughout the year. This finding is critical for a more accurate estimation of sea turtle mortality rates resulting from different fisheries and for devising efforts to avoid or minimize the harmful effects of capture.
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In this Review, we focus on the functional properties of the respiratory system of pinnipeds and cetaceans, and briefly summarize the underlying anatomy; in doing so, we provide an overview of what is currently known about their respiratory physiology and mechanics. While exposure to high pressure is a common challenge among breath-hold divers, there is a large variation in respiratory anatomy, function and capacity between species textendash how are these traits adapted to allow the animals to withstand the physiological challenges faced during dives? The ultra-deep diving feats of some marine mammals defy our current understanding of respiratory physiology and lung mechanics. These animals cope daily with lung compression, alveolar collapse, transient hyperoxia and extreme hypoxia. By improving our understanding of respiratory physiology under these conditions, we will be better able to define the physiological constraints imposed on these animals, and how these limitations may affect the survival of marine mammals in a changing environment. Many of the respiratory traits to survive exposure to an extreme environment may inspire novel treatments for a variety of respiratory problems in humans.
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Theoretical models are used to predict how breath-hold diving vertebrates manage O2, CO2, and N2 while underwater. One recent gas dynamics model used available lung and tracheal compliance data from various species. As variation in respiratory compliance significantly affects alveolar compression and pulmonary shunt, the current study objective was to evaluate changes in model output when using species-specific parameters from California sea lions (Zalophus californianus). We explored the effects of lung and dead space compliance on the uptake of N2, O2, and CO2 in various tissues during a series of hypothetical dives. The updated parameters allowed for increased compliance of the lungs and an increased stiffness in the trachea. When comparing updated model output with a model using previous compliance values, there was a large decrease in N2 uptake but little change in O2 and CO2 levels. Therefore, previous models may overestimate N2 tensions and the risk of gas-related disease, such as decompression sickness (DCS), in marine mammals.
Until recent declines in Arctic sea ice levels, narwhals (Monodon monoceros) have lived in relative isolation from human perturbation and sustained predation pressures. The resulting naïvety has made this cryptic, deep-diving cetacean highly susceptible to disturbance, although quantifiable effects have been lacking. We deployed a submersible, animal-borne electrocardiograph-accelerometer-depth recorder to monitor physiological and behavioral responses of East Greenland narwhals after release from net entanglement and stranding. Escaping narwhals displayed a paradoxical cardiovascular down-regulation (extreme bradycardia with heart rate ≤4 beats per minute) superimposed on exercise up-regulation (stroke frequency >25 strokes per minute and energetic costs three to six times the resting rate of energy expenditure) that rapidly depleted onboard oxygen stores. We attribute this unusual reaction to opposing cardiovascular signals—from diving, exercise, and neurocognitive fear responses—that challenge physiological homeostasis.
This book is not a conventional review of diving physiology. The coverage of the literature has been selective rather than en­ compassing, the emphasis has been on field studies rather than laboratory investigations, and the dive responses described are often discussed from the perspective of some of the flaws or weaknesses in the conclusions. Some of these points are of more historical interest to note how our concepts have evolved as we learn more about behavior and responses to natural diving in contrast to forced submersions in the laboratory. As a result there is a degree of evaluation of some experiments on my part that may seem obvious or controversial to the specialist. I have followed this planat times in order to aid the reader, who I hope is often an untergraduate or graduate stu­ dent, the nonspecialist, and the layman, in appreciating to some degree the level of dissatisfaction or skepticism about certain areas of research in diving physiology. In view of historical boundaries in vertebrate biology, the subject is of broad enough importance to catch the interest of a wide audience of readers if I have done my job well. For ex­ ample, of the major epochal transitions or events there have been in vertebrate history, three come immediately to mind: (1) The transition from aquatic to aerial respiration which ultimately led to a broad occupation of terrestrial habitats. (2) The development of endothermy.
Mesoplodont beaked whales are extreme divers, diving for over 45 mins and to depths of over 800 m. These dives are of similar depth and duration to those of the giant sperm whale (Physeter macrocephalus) whose body mass can be 50 times larger. Velten et al. (2013) provided anatomical data that demonstrated that on-board oxygen stores were sufficient to aerobically support the extreme dives of mesoplodonts if their diving metabolic rates are low. Because no physiological data yet exist, we utilized an anatomical approach—the body composition technique—to examine the relative metabolic rates of mesoplodonts. We utilized a systematic mass dissection protocol to compare the body composition of mesoplodonts with those of two short duration, shallow divers—the harbor porpoise (Phocoena phocoena) and bottlenose dolphin (Tursiops truncatus). We then investigated the body composition of two other extreme divers, the southern elephant seal (Mirounga leonina) and P. macrocephalus using data from the literature. Our results demonstrate that extreme divers invest a smaller percentage of their total body mass (TBM) in metabolically expensive brain and viscera, and a larger percent of their TBM in inexpensive integument, bone, and muscle, than do the shallow divers. Deep divers also share features of their locomotor muscle that contribute to relatively low tissue metabolic rates and high oxygen storage capacity, including large muscle fiber diameters, low mitochondrial volume densities, and high myoglobin concentrations. One feature of the locomotor muscle of mesoplodonts, though, is unique among deep divers investigated to date. Rather than having an endurance athlete’s muscle fiber profile, dominated by slow oxidative fibers, mesoplodonts possess a sprinter’s profile, dominated by fast glycolytic fibers. Velten et al. (2013) hypothesized that these fibers are likely inactive during routine swimming and provide a large, metabolically inexpensive oxygen store for the slow oxidative fibers to aerobically power swimming. We suggest that future anatomical analyses, coupled with performance data transduced through tagging studies, will enhance our understanding of the extreme diving capabilities of marine mammals.