Respiratory function and mechanics in pinnipeds and cetaceans

Abstract

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.

Full text

REVIEW
Respiratory function and mechanics in pinnipeds and cetaceans
Andreas Fahlman
1,2,
*, Michael J. Moore
3
and Daniel Garcia-Parraga
1,4
ABSTRACT
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 –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.
KEY WORDS: Compliance, Marine mammal, Lung function,
Respiratory flow, Tidal volume, Residual volume, Total lung capacity,
Respiratory frequency, Alveolar collapse
Introduction
In 1940, Per Scholander published his 131-page-long monograph
on cardiorespiratory function in marine mammals and birds. In his
treatise, he summarized the respiratory and cardiovascular traits
required by marine mammals to manage life in an extreme
environment and cope daily with challenges such as alveolar
collapse (atelectasis; see Glossary), alveolar recruitment (see
Glossary), transient hyperoxia, extreme hypoxia and
decompression sickness (DCS; see Glossary). In this Review, we
focus on the link between form and function in the respiratory
systems of diving marine mammals, but emphasize studies that have
attempted to understand lung function and mechanics in pinnipeds
and cetaceans (the species where the majority of work has been
done). Scholander’s model of lung/alveolar collapse (see below) is
of particular interest to this Review; this model provides a
mechanism for how marine mammals avoid lung squeeze (see
Glossary), limit their uptake of N
2
, avoid inert gas narcosis (see
Glossary) and DCS, and are able to generate high respiratory flows
that are sustained over the entire vital capacity (VC; see Glossary).
There are several reviews that describe anatomical features of
diving marine mammals (e.g. Piscitelli et al., 2013), but these
reviews focus on the structural properties of excised tissues, which
may not always reflect the functional properties of live animals
(Kooyman, 1973; Ponganis, 2015). For example, compliance
estimates of excised tissues do not account for the influence of
surrounding structures that encase the respiratory system (Cozzi
et al., 2005; Fahlman et al., 2011, 2014; Moore et al., 2014).
Likewise, pulmonary volume changes during compression of entire
dead specimens (Moore et al., 2011) cannot account for the
potential effects of blood engorgement of the tracheal mucosa in
cetaceans (Leith, 1976; Cozzi et al., 2005; Davenport et al., 2013).
Thus, the functional properties of the whole living animal cannot be
determined from deceased specimens. Here, we discuss recent
advances in our understanding of pulmonary mechanics and lung
function that we believe provide a theoretical framework that can
merge past and future studies to enhance our knowledge of the traits
that allow deep diving.
Scholander’s legacy, the model of lung/alveolar collapse
Scholander (1940) argued that the compliances of the respiratory
system, with a flexible thorax, would allow the elastic and highly
compliant alveoli to compress and push the air into the more rigid
(far less compliant) conducting airways. As the alveoli compress
and collapse, the gas diffusion rate would decrease and cause a
pulmonary shunt that increases with depth until the alveoli fully
collapse and gas exchange ceases (Fig. 1A,D). Pulmonary shunt
represents the amount of blood bypassing the lung and not
participating in gas exchange, and it varies between 0% and
100%, where 0% represents a fully inflated lung with perfect gas
exchange, and 100% represents termination of gas exchange.
Scholander assumed that the trachea behaved like an idealized non-
compressible pipe connected to a very compliant lung/alveolar
space (balloon-pipe model; Fig. 1A; Bostrom et al., 2008), allowing
the alveolar collapse depth to be estimated from Boyle’slaw
(Scholander, 1940; Bostrom et al., 2008). This has been an
important assumption used to understand diving physiology and
how marine mammals avoid diving-related problems, such as DCS
and N
2
narcosis, by reducing N
2
uptake and blood and tissue N
2
tension. However, many aspects of marine mammal respiratory
physiology are still not well understood; therefore, in this Review,
we summarize past and recent studies with the aim of providing
some generalizations about the different traits that have evolved to
allow marine mammals to manage a life in the ocean.
Static respiratory variables
Static indices of respiratory capacity are those that do not change
between breaths. Data on these variables exist for a limited
number of marine mammal species and include information on the
total lung capacity (TLC) and minimum air volume (MAV; see
Glossary) of the relaxed lung, as discussed below (Kooyman,
1973; Kooyman and Sinnett, 1979; Piscitelli et al., 2010; Fahlman
et al., 2011).
1
Fundación Oceanográfic de la Comunidad Valenciana, Gran Vı
́
a Marques del
Turia 19, Valencia 46005, Spain.
2
Department of Life Sciences, Texas A&M
University-Corpus Christi, 6300 Ocean Drive, Corpus Christi, TX 78412, USA.
3
Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA
02543, USA.
4
Oceanográfic-Avanqua, Ciudad de las Artes y las Ciencias, Valencia
46013, Spain.
*Author for correspondence (afahlman@oceanografic.org)
A.F., 0000-0002-8675-6479
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© 2017. Published by The Company of Biologists Ltd
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TLC or lung size
Overall, maximal lung volumes, or TLC ( generally defined as the
volume of air in the lung when the transpulmonary pressure is
30 cmH
2
O, where 1 cmH
2
O≈98 Pa), of diving mammals are in the
general range of those of terrestrial mammals (Kooyman, 1973;
Fahlman et al., 2011; Piscitelli et al., 2013; Ponganis, 2015).
Exceptions are the smaller lungs of deep-diving cetaceans and the
enlarged lungs of shallow-diving species, e.g. sea otters
(Scholander, 1940; Kooyman, 1973; Leith, 1989; Piscitelli et al.,
2013; Ponganis, 2015). While the classification of deep and shallow
divers is not well defined, and changes as we find out more about the
life history of different species, one study defined a shallow diver to
be a species where most dives are shallower than 100 m, e.g.
bottlenose dolphin (Tursiops truncatus) and harbor porpoise
(Phocoena phocoena) (Piscitelli et al., 2010).
Kooyman (1973) compiled the available values for TLC in
pinnipeds and cetaceans of different body mass (M
b
), from harbor
seal (Phoca vitulina,M
b
≈15 kg) to fin whale (Balaenoptera
physalus,M
b
≈44 tonne), allowing him to derive an equation to
estimate TLC (TLC
est
, in liters) from a known value of M
b
(kg):
TLC
est
=0.135M
b0.92
. However, a later study suggested that the
relationship between M
b
, lung size (and possibly TLC) and muscle
myoglobin concentration differed between a number of deep- (e.g.
pygmy Kogia breviceps, and dwarf sperm whales Kogia sima) and
Glossary
Alveolar recruitment
The point when collapsed alveoli open up and gas exchange resumes.
Atelectasis
Alveolar collapse, resulting in cessation of gas exchange.
Collateral ventilation
Ventilatory flow through the lung parenchyma through alternative flow
pathways, such as pores of Kohn.
Dead space
The volume of air in the respiratory system not participating in gas
exchange, e.g. air in the trachea.
Decompression sickness
Also called the ‘bends’or caisson disease; a collection of symptoms
observed following a reduction in ambient pressure, which causes
bubbles to form in the blood and tissues. In humans, symptoms include
dizziness, numbness, fatigue and, in more severe cases, paralysis,
problems breathing and death.
Inert gas narcosis
Caused by the anesthetic effect of lipid-soluble gases at high pressure.
In air-breathing divers the symptoms may ultimately lead to loss of
consciousness as pressure increases.
Lung squeeze
Pulmonary edema caused by intrathoracic pressures that are lower than
environmental pressures during breath-hold diving.
Maximal/forced breath
Often used in human lung-function testing to assess the maximal
capacity of lung function such as VC, PEF, PIF and airway obstruction.
The individual is asked to expire maximally, followed by an inspiration.
Minimum air volume
The volume of air left in the relaxed lung.
Respiratory frequency
The number of breaths per unit time.
Rete
A network of arteries or veins
Tidal volume
The volume of air exhaled or inhaled during a normal breath.
Vital capacity
The maximal volume of air that can be exchanged in one breath. In
marine mammals, VC is close to TLC.
Balloon–pipe model
Rigid but compressible
trachea
Increasing pressure
Trach ea
Alveoli
A
BC
D
1 cm
4
3
2
1
Volume (I)
0
0123456789101112
Pressure (ATA)
Alveolar
collapse
Compliant trachea
Rigid trachea
10
20
30
40
50
Relative diffusion rate (P⫻A)
020
Depth (m)
40 60 80 100
AI 252 m VA=0 ml, VDS=420 ml
120
VA
VDS
VA
VDS
Fig. 1. The effect of pressure on lung volume and diffusion rate. (A) Graph
showing how the compression of the respiratory system is affected when the
compliance of the upper and lower airways are accounted for. The figure
assumes a Weddell seal with a diving lung volume of 11 liters, an alveolar
volume (V
A
, solid lines) of 10 liters and a dead space volume (V
DS
,broken
lines) of 1 liter. The black lines represent the volume of the respiratory system in
relation to depth for Scholander’s original balloon-pipe model, with a stiff dead
space that does not compress, and the red lines represent the volume of the
lung based on the lung compression model presented in Bostrom et al. (2008).
The schematic below panel A provides a qualitative explanation of the two
models. The balloon-pipe model, where the conducting airways do not
compress, is shown in black, and the model where the airways begin to
compress at a depth determined by the specific compliances of the upper and
lower airways (in this case 30 m) is shown in red. (B,C) Radiographs of the
trachea of a Weddell seal submerged at 1 ATA (atmospheres absolute), the
surface (B) and during a dive to 31.6 ATA (C). The arrowheads show the
tracheal margins. The circular object is an electrocardiogram (ECG) electrode.
Reproduced with permission from Bostrom et al. (2008). (D) A graph showing
the effect of alveolar compression on the diffusion rate [pressure (P)×surface
area (A), assuming that the alveolar membrane thickness is not affected],
assuming Scholander’s original balloon-pipe model (black line) or the lung
compression model presented in A (red line).
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shallow-diving (bottlenose dolphin and harbor porpoise) cetaceans
investigated (Piscitelli et al., 2010). The deep-diving species with
smaller lungs also had a higher myoglobin concentration whereas
species that were assumed to be shallow divers had larger lungs. It
was suggested that the larger lungs in shallow-diving species would
help to increase the amount of available O
2
during short shallow
dives. In the deep-diving species, the available O
2
is instead
increased through higher muscle myoglobin concentration, as a
greater diving lung volume would increase the amount of N
2
taken
up during dives, thus increasing the risk of DCS (Piscitelli et al.,
2010).
Whether these differences are evolutionary adaptations or traits
derived from anatomical and physiological plasticity is unclear.
There is evidence that muscle myoglobin concentration changes as
juveniles increase their diving capacity throughout ontogeny (Noren
and Williams, 2000; Noren et al., 2001), and that diving capacity
alters hematology (Duffield et al., 1983; Ridgway and Harrison,
1986). In addition, studies have indicated that lung conditioning,
through repeated chest compressions, alters the mechanical
properties of the lung (Johansson and Schagatay, 2012; Fahlman
et al., 2014). Consequently, there may be considerable physiological
plasticity to alter the O
2
stores so that animals may vary muscle
myoglobin concentration, pulmonary size and mechanical
properties of the lungs, depending on their life history. This may
explain the large intra-species differences in diving capability
between inshore and pelagic bottlenose dolphins (Mate et al., 1995;
Klatsky et al., 2007). Comparing intraspecific differences in
respiratory function and myoglobin concentrations in these
populations would help to clarify this issue.
Functional residual capacity, residual volume and MAV
The functional residual capacity (FRC) and residual volumes (RV)
are, respectively, the amounts of air that remain in the lung
following a passive and maximal exhalation. In the human lung,
FRC and RV are approximately 40% and 22% of TLC, respectively
(Berend et al., 1980; Crapo et al., 1981). At relaxed FRC, the inward
recoil of the lung equals the outward recoil of the chest so that the
forces balance, and at RV, the inward recoil of the lung is lower than
the outward recoil of the chest. This outward recoil helps to retain a
volume of air in the lung, thereby preventing alveolar closure and
atelectasis. In the marine mammals tested, mainly pinnipeds, the
chest does not resist compression, i.e. it has very high compliance
(Fig. 2) (Leith, 1976; Fahlman et al., 2014). In these species, relaxed
FRC is close to or equal to RV. The excised lung of a terrestrial
mammal retains a certain amount of air whereas the pulmonary
architecture in marine mammals allows for near-complete alveolar
emptying (Denison et al., 1971; Kooyman and Sinnett, 1979;
Piscitelli et al., 2010; Fahlman et al., 2011). Consequently, the MAV
that remains in the relaxed excised lung is similar to FRC or RV in
the pinnipeds (Kooyman and Sinnett, 1979) (see the ‘Chest
compliance’section). In excised lungs from a number of species
of cetaceans and pinnipeds, the mean MAV is 7% (range 0–17%) of
TLC (Kooyman and Sinnett, 1979; Fahlman et al., 2011), which is
close to the measured FRC in a live pilot whale (Globicephala
scammoni) and California sea lion (Zalophus californianus,
12–19% of TLC) (Olsen et al., 1969; Kerem et al., 1975).
Consequently, residual air in the lungs of marine mammals
following a maximal exhalation is minimal, and the maximal
volume that can be exchanged during a breath, the VC, would be
close to TLC. This allows marine mammals to exchange almost the
entire lung volume in a single breath, which minimizes dead space
ventilation (see Glossary) and is an efficient ventilatory strategy. In
addition, the small volume of air that remains at MAV reduces the
risk of barotrauma during breath-hold diving.
Dynamic respiratory variables
Dynamic respiratory variables are those that may change between
breaths and, at least in some sense, are under voluntary control. This
includes variables such as respiratory frequency ( f
R
; see Glossary),
tidal volume (V
T
; see Glossary) and VC. There are limited data on
dynamic respiratory variables for pinnipeds and cetaceans, and there
is considerable variability among marine mammal species
(Ponganis, 2011, 2015). However, there are some general trends
that can be described. For example, compared with similarly sized
terrestrial mammals on land (see table 1 in Stahl, 1967), f
R
is
significantly lower and V
T
is higher in resting cetaceans and
pinnipeds when in water or breathing at the water surface, and for
pinnipeds on land (Table 1).
Respiratory frequency
Data from 29 species of semi- and fully aquatic marine mammals
have allowed f
R
to be determined as: f
R
=33M
b
−0.42
(Mortola and
Limoges, 2006). The allometric mass-exponent is significantly
different from that calculated for terrestrial mammals (−0.26, Stahl,
1967); thus, for similarly sized animals, f
R
is significantly lower in
an aquatic mammal as compared with a terrestrial one. In addition,
the terrestrial breathing strategy in adult land mammals involves a
brief expiratory pause whereas the aquatic breathing strategy in
marine mammals involves an inspiratory pause, which often lasts
for seconds to minutes (Scholander, 1940; Spencer et al., 1967;
Olsen et al., 1969; Kooyman et al., 1971; Kooyman, 1973; Kerem
et al., 1975; Mortola and Lanthier, 1989; Reed et al., 1994; Mortola
and Limoges, 2006; Fahlman et al., 2015b; Fahlman and Madigan,
2016). In pinnipeds, this breathing strategy persists on land (Mortola
and Lanthier, 1989; Mortola and Limoges, 2006; Fahlman and
Madigan, 2016). Interestingly, humans change their ventilation
pattern to the aquatic form, with a respiratory pause on inspiration,
when in water (Kooyman, 1973). It was hypothesized that the
120
100
80
Volume (% TLCest)
60
40
20
0
01020
CSL10244
CSL10638
CSL10650
CSL10244
CSL10638
CSL10650
30 40
Pressure (cmH2O)
Fig. 2. The pressure–volume relationship (compliance) for the lung and
chest for three individual California sea lions (Zalophus californianus).
Values for the lung are represented byclosed symbols, and those for the chest
are represented by open symbols. Each of the different shapes represents a
different individual sea lion. Figure modified from Fahlman et al. (2014), with
permission. TLC
est
is estimated lung capacity (Kooyman, 1973). The much
higher compliance of the chest indicates that the chest does not resist
compression, which minimizes the risk of lung squeeze.
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aquatic breathing strategy evolved to aid buoyancy (Mortola and
Limoges, 2006). An alternative hypothesis was presented in a later
paper, where Mortola and Sequin (2009) suggested that the aquatic
respiration pattern in marine mammals may help maintain the arterial
partial pressure of CO
2
(Pa
CO
2
) at levels similar to that of land
mammals despite a much lower f
R
, not entirely matched by a higher
V
T
. Results in the walrus (Odobenus rosmarus) and California sea
lion, bottlenose dolphin, killer whale (Orcinus orca) or beluga whale
(Delphinapterus leucas)suggestthatPa
CO
2
during calm breathing is
within a range similar to that of humans (32–42 mmHg, Mortola and
Sequin, 2009). Others have reported that the normal Pa
CO
2
may be
slightly higher, around 46–68 mmHg in bottlenose dolphins
(McCormick, 1969; Fahlman et al., 2015b).
Respiratory duration
There is considerable variability in the duration of the expiratoryand
inspiratory phases of breathing in marine mammals (Table 1). One
reason could be that the measurements have been performed in
animals under different conditions, such as during rest or following
exercise or diving. In the resting beluga whale (Epple, 2016), and in
both the Atlantic and Pacific bottlenose dolphin (Kooyman and
Cornell, 1981; Fahlman et al., 2015b), the duration of the expiratory
phase is shorter than the inspiratory phase for normal and forced
(maximal) breaths (see Glossary; Table 1). In California sea lions
following recovery from diving, the expiratory phase is shorter than
the inspiratory phase (Table 1) (see fig. 2 in Kerem et al., 1975).
With increasing V
T
, the duration of the expiratory phase decreases
while that of the inspiratory phase increases (Kerem et al., 1975). In
Patagonia sea lions (southern sea lion, Otaria flavescens), resting
while laying down, the expiratory duration is significantly longer
than the inspiratory duration (Fahlman and Madigan, 2016). In the
gray whale (Eschrichtius robustus), expiratory durations range
greatly (Table 1) (Wahrenbrock et al., 1974; Kooyman et al., 1975;
Sumich, 2001). Thus, there appears to be considerable variability in
breath durations, and animals appear to alter these depending on
respiratory efforts, possibly as flow rates reach the upper
physiological limit (Kerem et al., 1975; Epple, 2016).
VC and V
T
Marine mammals, and in particular cetaceans, are able to generate
high expiratory flow (Table 1), and have VCs that are close to TLC.
However, V
T
for most normal breaths, even following diving or
exercise, is well below VC (Fig. 3) (Irving et al., 1941; Olsen et al.,
1969; Kooyman and Cornell, 1981; Reed et al., 2000; Fahlman
et al., 2015b, 2016). It is reasonable to assume that animals may
increase both V
T
and f
R
when they return from a long dive, or during
intense swimming efforts at the surface, as this would maximize gas
exchange and reduce time to recovery. Several studies have shown
that there is a correlation between dive duration, dive depth and the
f
R
following a dive (Würsig et al., 1984, 1986; Dolphin, 1987b).
Thus, the respiratory effort, or minute ventilation (the volume of air
inhaled/exhaled per minute estimated as the product of V
T
and f
R
), is
likely to vary with activity as in terrestrial mammals (Williams and
Noren, 2009; Fahlman et al., 2016).
Some studies have used f
R
to estimate field metabolic rate in free-
ranging large whales where standard methods, like respirometry, are
not logistically feasible (Sumich, 1983; Dolphin, 1987a; Armstrong
and Siegfried, 1991; Folkow and Blix, 1992; Blix and Folkow,
Table 1. Tidal volume (V
T
), breathing frequency (f
R
), minute ventilation ( _
V
E
) and maximum expiratory and inspiratory flowsduring rest in a number
of marine mammal species
Rest
Species
Body mass
(kg) V
T
(l)
f
R
(breaths
min
−1
)
_
VE(l min
−1
)
Respiratory duration (s)
Maximum respiratory
flow (l s
−1
)
ReferencesExpiration Inspiration Expiration Inspiration
Grey seal* 160–250 6.3 19.4 123 9.7 8.4 Reed et al., 1994
Weddell seal 280–430 4.0–10.0 4.0–10.0 32.4 5.8–7.0 4.6–6.3 Kooyman et al., 1971; Falke
et al., 2008
Harbor porpoise* 28 1.0–1.1 4.7–5.3 4.6–5.8 4.9–6.0 4.0–5.3 Reed et al., 2000
Pacific bottlenose
dolphin
285 26.4 115–162 45–56 Kooyman and Cornell, 1981
Atlantic
bottlenose
dolphin
140–250 5–10 3.4 0.26–0.31 0.43–0.66 20–140 15–33 Irving et al., 1941; Ridgway
et al., 1969; Fahlman et al.,
2015b
California sea lion 32–46 1.2–2 16.4–18.1 21.3–22.9 0.8 1.0 8.6–14 5 Kerem et al., 1975; Matthews,
1977
Gray whale 1500
‡
–6000 38–212 1–223–303 0.3–1.2 101–202 116–176 Wahrenbrock et al., 1974;
Kooyman et al., 1975
Killer whale 1090
§
–3700 46–218 1 180 61 Spencer et al., 1967; Kasting
et al., 1989
Beluga whale 324–640 14.0–12.6 0.52 0.89–0.98 58.5±23.6 28.2±10.0 Kasting et al., 1989; Epple,
2016
Pilot whale 450 9–39.5 1–2 Olsen et al., 1969
Fin whale ∼40,000 0.5–1 0.73±0.15 0.91±0.23 Lafortuna et al., 2003
Minke whale 1840–5740 0.48–1.35 Blix and Folkow, 1995
Walrus 640–841 8–15 1.30±0.33 1.96±0.56 >45 11 Fahlman et al., 2015a
Patagonia sea lion 94–286 2.4–7.6 2.43±0.62 1.89±0.23 3.6–9.1 3.1–7.0 Fahlman and Madigan, 2016
Human 70 0.6 18 11.3 7–10 5 Stahl, 1967; Jordanoglou and
Pride, 1968; Knudson et al.,
1976
The range of maximal flows between different individuals is given when available.
*Data collected during surface periods between breath holds/apneas.
‡
Body mass of wild animals was estimated from length [4.8–5.8 m estimated to be approximately 1500–2300 kg (Krogh, 1929)].
§
Beached female.
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1995; Rodríguez de la Gala-Hernández et al., 2008; Christiansen
et al., 2014). The volume of O
2
taken up per breath is the product of
the V
T
and the difference in inhaled and exhaled O
2
concentration,
i.e. the O
2
exchange ratio. These models assume that the O
2
exchange ratio and V
T
remain constant during the surface interval.
However, both change during recovery from exercise and diving,
and accounting for these dynamic changes in physiology improves
the estimated metabolic rate (Ridgway et al., 1969; Reed et al., 1994,
2000; Miedler et al., 2015; Fahlman et al., 2016). Thus, an improved
knowledge of respiratory physiology may be useful to improve
estimates of field metabolic rate using this method.
Diving lung volume
The diving lung volume is the volume of air that an animal brings
with it during submersion; it can be adjusted behaviorally at the
beginning of the dive or by exhaling while submerged. The
structural properties of the respiratory system and the ratio between
alveolar and dead space volume, and therefore the diving lung
volume, affect the alveolar collapse depth (Scholander, 1940;
Bostrom et al., 2008). Thus, behavioral adjustment of the diving
lung volume may be important to adjust the O
2
stores or to minimize
N
2
uptake and the risk of gas emboli (Hooker et al., 2005; Fahlman
et al., 2009; McDonald and Ponganis, 2012). The fact that each
animal has the ability to behaviorally alter the alveolar collapse
depth makes this a complicated variable to predict.
There appears to be considerable variability in the diving lung
volume within and between species or even within different dives of
the same individual. Our current assumption is that most seals
exhale before diving whereas sea lions and cetaceans dive on
inhalation (Snyder, 1983; Ridgway, 1986; Ridgway and Harrison,
1986; Kooyman, 1989). Scholander (1940) reported that gray seals
(Halichoerus grypus) exhale before diving and inhale when they
return from a dive. In the Weddell seal (Leptonychotes weddelli)
dives begin and end with an expiration, which indicates that they do
not dive on RV (Kooyman et al., 1972). In a forced diving
experiment on seals in a pressure chamber, the measured diving
lung volume varied between 20% and 60% of TLC and increased
for longer, but not necessarily deeper, dives (Kooyman et al., 1972).
Similarly, California sea lions diving in a water-filled chamber
exhaled upon surfacing (Kerem et al., 1975). Freely diving
Antarctic fur seals exhale during the ascent. This is possibly a
behavioral method to prevent recruitment of collapsed alveoli,
thereby preventing shallow water black-out (Hooker et al., 2005),
which is caused by expansion of the alveolar volume, causing a
significant drop in lung O
2
partial pressure and a reversal of O
2
diffusion from the pulmonary capillary into the lung. This rapidly
reduces the arterial O
2
tension and results in cerebral hypoxia and
unconsciousness. Hooker and colleagues argued that by reducing
the diving lung volume, the alveolar collapse and recruitment depth
would become shallower, thereby preventing the O
2
reversal. In the
California sea lion, the estimated alveolar collapse depth increases
with dive depth, suggesting that the diving lung volume increases
with depth (McDonald and Ponganis, 2012).
In cetaceans, breath-by-breath analysis and observations in
dolphins (Ridgway, 1986; Fahlman et al., 2015b), beluga whale
(Epple et al., 2015), harbor porpoise (Reed et al., 2000), gray whale
(Sumich, 2001) and pilot whale (Olsen et al., 1969) suggest that the
majority of breaths begin with exhalation, followed by inspiration
and a respiratory pause (see the ‘Respiratory frequency’section).
This is also consistent before and after a bout of exercise or a breath-
hold (Fahlman et al., 2016). These studies are often performed on
restrained animals or those under human care, and thus may not
entirely reflect the behavior in free-ranging whales. However,
measuring the diving lung volume in free-ranging animals is
logistically challenging, and few studies have been attempted to do
this. Technological advances may help us to understand the
behavioral strategies of various species. For example, one study
used a digital acoustic recording tag (Dtag) to estimate the diving
lung volume based on the acceleration and gliding patterns in the
sperm whale (Miller et al., 2004). Other studies have recorded the
respiratory pattern using data recorders and microphones, and these
may shed some light on both respiratory patterns and effort in wild
animals (Blix and Folkow, 1995; Sumich and May, 2009; van der
Hoop et al., 2014).
Respiratory mechanics: flow and compliance
In addition to anatomical descriptions of the thorax of some marine
mammal species (Piscitelli et al., 2010), limited work has
investigated the functional and mechanical properties of the
respiratory system in live animals (Scholander, 1940; Olsen et al.,
1969; Kooyman et al., 1971, 1973, 1975; Kerem et al., 1975; Leith,
1976; Kooyman and Cornell, 1981; Kooyman and Sinnett, 1982;
Kasting et al., 1989; Leith, 1989; Reed et al., 1994, 2000; Fahlman
et al., 2014, 2015b; Fahlman and Madigan, 2016). For example, it
has been suggested that the diaphragm and intercostal muscles are
important to generate high respiratory flow and rapid f
R
(Ridgway,
1972; Dearolf, 2003; Cotten et al., 2008). However, few studies
have compared the functional properties within and between
species. The available studies have detailed the functional
properties of the different parts of the respiratory system from
excised tissues, estimated the effect of pressure on lung volume or
whole cadavers, or estimated lung and chest compliance in
anesthetized and awake voluntarily participating animals (Denison
0
50
1000 2000 3000
Beluga whale
Walrus
Dolphin
Gray seal
Weddell seal
Killer whale
California sea lion
Harbor porpoise
Pilot whale
False killer whale
Patagonia sea lion
TLCest (l)
VT,e s t (l)
Mb (kg)
100
VT (l)
150
200
Fig. 3. The relationship between measured resting tidal volume (V
T
)and
body mass (M
b
) in a number of marine mammal species. Different marine
mammals are represented by colored symbols. For comparison, the
relationship between estimated V
T
(V
T,est
) and M
b
is shown for terrestrial
animals (solid line, Stahl, 1967). The relationship between estimated total lung
capacity (TLC
est
; broken line, Kooyman, 1973) and M
b
for marine mammals
reveals that the volume of most breaths of marine mammals is not close to the
vital capacity of the animal. References: bottlenose dolphin (Fahlman et al.,
2015b), gray seal (Reed et al., 1994), Weddell seal (Kooyman et al., 1971),
harbor porpoise (Reed et al., 2000), California sea lion (Kerem et al., 1975;
Matthews, 1977), pilot whale (Olsen et al., 1969), killer whale (Spencer et al.,
1967; Kasting et al., 1989), beluga whale (Kasting et al., 1989; Epple et al.,
2015), walrus (Fahlman et al., 2015a), Patagonia sea lion (Fahlman and
Madigan, 2016) and false killer whale (M. Piscitelli, Y. Molgat, P. Dominelli,
M. Haulena and A.F., unpublished observation).
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et al., 1971; Denison and Kooyman, 1973; Kooyman, 1973;
Tarasoff and Kooyman, 1973; Leith, 1976; Kooyman and Sinnett,
1979; Kooyman and Cornell, 1981; Fahlman et al., 2011, 2014,
2015b; Moore et al., 2011, 2014). Studies using trained marine
mammals that voluntarily participate have been used to define flow–
volume characteristics (Olsen et al., 1969; Kooyman and Cornell,
1981; Fahlman et al., 2015b; Fahlman and Madigan, 2016). These
data provide mechanistic information about flow limitations, and
similar methods are used in human medicine to diagnose a variety of
pulmonary disorders (Clausen, 1982). Thus, assessment of lung
function may be a useful way to diagnose respiratory health in
marine mammals. If successful, lung function studies on wild
marine mammals may be a useful method to assess respiratory
health in different populations.
Flow–volume limitations
In humans, the flow during forced exhalation is effort independent,
and maximal flow occurs at high lung volume and then rapidly
declines as lung volume decreases (Hyatt et al., 1958). This flow
limitation is caused by increasing flow resistance as the distal airways
compress and close during maximal respiratory efforts (Mead, 1961).
Consequently, in the human lung, greater expiratory effort does not
increase the expiratory flow as the lung volume decreases below
∼80% of VC (Fig. 4) (Kooyman and Cornell, 1981; Fahlman et al.,
2015b). By contrast, flow–volume curves from the excised lungs of
fin whale, sei whale (Balaenoptera borealis), harbor porpoise and
California sea lion, and from maximal respiratory efforts in
voluntarily participating Atlantic and Pacific bottlenose dolphins
and California sea lions have shown that expiratory flow is effort
dependent, and maximal flow persists at all lung volumes (Fig. 4)
(Leith et al., 1972; Kerem et al., 1975; Matthews, 1977; Kooyman
and Sinnett, 1979; Kooyman and Cornell, 1981; Fahlman et al.,
2015b). Consequently, in cetaceans and pinnipeds, it appears that the
expiratory flow is not limited by the conducting airways and lung
volume as in terrestrial mammals (Fig. 4).
It has been suggested that short, rapid breaths are useful to
minimize the time spent breathing at the surface, especially in
species that breathe while traveling (e.g. porpoising) or during a
surface interval in a dive bout. Thus, it appears that the respiratory
anatomy in cetaceans and sea lions allows very high, and almost
constant, flow over most of the VC (Olsen et al., 1969; Kerem et al.,
1975; Kooyman et al., 1975; Kooyman and Sinnett, 1979; Fahlman
et al., 2015b). In addition, this anatomy allows the lungs to almost
completely empty during maximal respiratory efforts or during
compression (Denison et al., 1971). Currently, we are not aware of
any data in the seal, but given the divergent anatomy and lifestyle
between seals, sea lions and cetaceans, one may hypothesize that the
exhalations of a seal are more effort independent, and that they are
not able to generate similarly high respiratory flow rates as
compared with sea lions and cetaceans.
The peak/maximal respiratory flow is seen during expiration, and
both cetaceans and pinnipeds (Table 1) have expiratory flows that
exceed those of terrestrial mammals (see table 1 in Stahl, 1967).
When expressed as a proportion of TLC
est
per second (TLC
est
s
−1
),
only the cetaceans (gray whale, bottlenose dolphins, harbor
porpoise, beluga whale and killer whale) and the California sea
lion have respiratory flow exceeding that seen in humans of about
2 TLC
est
s
−1
(Table 1) (Kerem et al., 1975; Kooyman et al., 1975;
Kooyman and Sinnett, 1979; Kooyman and Cornell, 1981; Fahlman
et al., 2015b; Epple, 2016). In both odontocetes and otariids,
expiratory flow is effort dependent over most of the VC, and is not
limited by lung volume as is seen in terrestrial mammals (Kerem
et al., 1975; Matthews, 1977; Kooyman and Sinnett, 1979;
Kooyman and Cornell, 1981; Fahlman et al., 2015b). At least in
cetaceans, normal exhalations appear to be mainly passive and
driven by the elastic recoil of the chest (Fig. 5A) (Olsen et al., 1969;
Fahlman et al., 2015b), typically generating flow rates of
20–40 l s
−1
. It has been suggested that the lack of a central tendon
in the cetacean diaphragm facilitates emptying (Olsen et al., 1969).
By contrast, inspiration and maximal expiratory efforts are active,
and exhalations exceeding 160 l s
−1
have been reported in resting
bottlenose dolphins (Fig. 5C) (Kooyman and Cornell, 1981;
Fahlman et al., 2015b). During maximal efforts, the diaphragm
and intercostal muscles provide active muscle force to increase the
flow generated by the passive recoil of the chest (Ridgway, 1972;
Dearolf, 2003; Cotten et al., 2008). It is likely that these flow rates
are higher in actively swimming dolphins as the respiratory and
locomotor muscles seem to be coupled (Cotten et al., 2008). Thus,
evolutionary forces may have engineered a respiratory system with
reinforced airways that allow sustained flow rates over most of
the VC.
In humans, the ratio between peak expiratory flow (PEF) and
peak inspiratory flow (PIF) typically is between 1.2 and 1.4 in
healthy subjects (Jordanoglou and Pride, 1968). In the bottlenose
dolphin (Kooyman and Cornell, 1981; Fahlman et al., 2015b) and
beluga whale (Epple, 2016) the ratio is between 2 and 3 during
maximal efforts. These results may indicate physiological
limitations during active inspiration that restrict the maximal
inspiratory flow rates. Alternatively, these results may be an
artefact of working with trained animals, where training
maximizes expiration but not inspiration. During normal
respiration, the PEF/PIF ratio is between 1 and 1.5 (Fahlman
et al., 2015b; Epple, 2016).
Chest compliance
Terrestrial mammals have stiff chest walls, resulting in a relatively
large FRC, which prevents atelectasis when the airway is open and
the respiratory muscles are relaxed (West, 2012). When terrestrial
mammals breath-hold dive, the terrestrial thoracic phenotype resists
compression as external hydrostatic pressure increases, which
causes negative pressures to develop inside the chest (i.e. lung
squeeze) (Lundgren and Miller, 1999). In humans, these negative
Forced breath 1
140
120
100
80
60
40
20
0
–20
–40
Forced breath 2
05
Volume (l)
Flow rate (l s–1)
10 15 20
Expiration
Fig. 4. Flow–volume curves for two forced breaths from a bottlenose
dolphin. The marked absence of changes in flow with variation in lung volume
indicatesthat flow is effort dependent. Expiratory flow is positive and exhalations
have positive volume (modified from Fahlman et al., 2015b, with permission).
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pressures cause blood to be drawn into the thoracic cavity (thoracic
blood pooling) –this reduces the gas space volume and helps to
reduce the pressure difference (Craig, 1968; Schaefer et al., 1968;
Leith, 1989). In human breath-hold divers, pulmonary edema and
hemorrhage are common; in the case of extreme negative
intrathoracic pressures, cardiac arrhythmias and rupture of the
vena cava have been reported (Scholander et al., 1962; Leith, 1989;
Hansel et al., 2008; Lindholm et al., 2008; Linér and Andersson,
2008; Lindholm and Lundgren, 2009).
In anesthetized pinnipeds, it seems that the chest is highly
compliant (Fig. 2) (Leith, 1976; Fahlman et al., 2014). As discussed
above, in species with high chest compliance, FRC and RV are
almost equal, which supports Scholander’s hypothesis that the
structural properties of the respiratory system allow the alveoli to
compress to the limit of collapse without the risk of lung squeeze
(Scholander, 1940; Kooyman, 1973; Kooyman and Sinnett, 1979;
Leith, 1989; Fahlman et al., 2014).
To our knowledge, no data exist on the mechanical properties
of the cetacean chest wall in live animals. In intact carcasses, the
odontocete thorax appears to be stiffer than that of the pinnipeds
(A.F. and M.J. M., unpublished observation), and it recoils inward
to low volumes and is able to compress when exposed to pressure
(Ridgway et al., 1969; Moore et al., 2011; Fahlman et al., 2015b). In
the seminal work by Ridgway et al. (1969), it was shown that the
chest of the dolphin compresses and changes shape during diving.
Compression of the chest was observed at depths as shallow as
10 m, and the classic photograph of the trained bottlenose dolphin
Tuffy at 300 m shows extensive thoracic compression behind the
pectoral flippers (Ridgway et al., 1969). These results were
confirmed in deceased cetacean specimens compressed in a
hyperbaric chamber and imaged using computed tomography at
varying pressures (see fig. 2 in Moore et al., 2011). Thus, the
structural properties of the cetacean thorax may allow pressure to
compress the chest and lung to very low volumes, thereby
preventing pulmonary barotrauma (lung squeeze). We propose
that this greater inward recoil in the cetacean might help to produce
the high passive expiratory flow reported in odontocetes (Fig. 5A,B)
(Olsen et al., 1969; Kooyman and Cornell, 1981; Fahlman et al.,
2015b). Future studies are needed to confirm these observations of
chest compliance.
Several species of cetaceans have complex thoracic arterial and
venous retes (see Glossary). An arterial rete has limited ability to
expand, and its tortuosity and interconnections may trap bubbles or
emboli and guarantee alternative flow pathways (collateral
circulation) to prevent neural emboli and possible trauma (Vogl
and Fisher, 1982; Blix et al., 2013). By contrast, the venous rete,
being far more distensible, can engorge with blood and reduce the
volume of gas-filled spaces, thereby protecting against lung squeeze
[similar to the thoracic blood pooling reported in human breath-hold
divers (Harrison and Tomlinson, 1956; Murdaugh et al., 1962;
Craig, 1968; Hui, 1975; Ridgway et al., 1984)]. It has also been
suggested that venous retes may help regulate pressure, flow or
pulse, and affect blood composition (Hui, 1975). The phocid seal
has an unusually large vena cava, which may fill with blood and
expand and serve to protect against pressure-related injuries.
A highly compliant chest under elastic recoil, with a FRC with
minimal volume may result in atelectasis if the airway remains open
and the respiratory muscles are relaxed. Closing the upper airway
(blow-hole or nares) is a simple solution that helps to prevent
alveolar collapse in marine mammals when they are not holding
their breath underwater. Thus, the aquatic breathing strategy –with
an inspiratory pause between breaths, a f
R
that is lower than that of
their terrestrial relatives and a mass-specific V
T
that is up to three
times greater than that of terrestrial mammals (Spencer et al., 1967;
Olsen et al., 1969; Kooyman et al., 1971; Kooyman, 1973; Mortola
and Lanthier, 1989; Reed et al., 2000; Mortola and Limoges, 2006;
Mortola and Sequin, 2009; Epple et al., 2015; Fahlman et al.,
2015b) –may be a compromise to prevent alveolar atelectasis while
maintaining an alveolar minute ventilation rate that is similar to that
8A
B
C
40
30
20
10
0
–10
–20
6
4
2
0
–2
Expiration
–4
–6
–8
0 0.5 1.0 1.5 2.0 2.5 3.0
30 40
30
20
10
0
–10
–30
–20
20
10
0
–10
–20
–30
–40
–50
0 0.5 1.0 1.5
Flow (l s–1)
Esophageal pressure (cmH2O)
2.0
40
20
0
–20
–40
–60
–80
–100
–120
–140
–160
60
40
20
0
–40
–20
0.4 0.6 0.8 1.0 1.2 1.4 1.6 1.8 2.0
Time (s)
Fig. 5. Respiratory flow and esophageal pressure during normal and
forced breaths in a bottlenose dolphin (Tursiops truncatus). The graphs
show normal (A,B) and forced (C) breaths, where expiratory flow is negative.
Esophageal pressure is shown in red and respiratory flow is in black. During
passive exhalation (A), the elasticrecoil of the thorax provides the driving force
for the emptying of the lungs and the esophageal pressure decreases slightly.
In B, the exhalation is in part active, and the esophageal pressures increase
slightly before the exhalation and remains more or less constant until the end of
the exhalation phase. (C) Maximal exhalations are marked by a large increase
in esophageal pressure during the exhalation, indicating an active component
to help generate the extreme flow rates seen in cetaceans. Figure modified
from Fahlman et al. (2015b), with permission.
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of land mammals. In newborn human infants, with a highly
compliant chest wall, the aquatic respiratory pattern is sometimes
present for a few hours following birth (Fisher et al., 1982). Thus,
the flexible chest wall may be useful to prevent pulmonary
barotrauma but also reflects the need for an aquatic breathing
strategy with an inspiratory apnea that helps to prevent atelectasis
and improve gas exchange during the respiratory pause between
breaths (Leith, 1989; Mortola and Lanthier, 1989).
Airway compliance
While physiological function is at least limited by structural
properties, it is not always easy to ascertain function from form. The
reinforced conducting airway of marine mammals is a good
example. Marine mammals are reported to have reinforced
airways (Kooyman and Sinnett, 1982), and there appears to be
significant variability between orders and species (Wislocki, 1929,
1942; Bélanger, 1940; Wislocki and Belanger, 1940; Goudappel
and Slijper, 1958; Denison and Kooyman, 1973; Henk and
Haldiman, 1990; Wessels and Chase, 1998; Ninomiya et al.,
2005; Bagnoli et al., 2011). In the sea lion and cetaceans, the
cartilaginous reinforcement extends down to the entrance of the
alveoli or alveolar sac –there are no respiratory bronchioles –
whereas in the seal the last few millimeters of the conducting airway
are reinforced with muscle and appear to be much more compliant
(Tarasoff and Kooyman, 1973; Cozzi et al., 2005; Bagnoli et al.,
2011; Moore et al., 2014). As discussed above, Scholander (1940)
proposed that the cartilaginous reinforcement prevents the
compression of the airway, facilitating alveolar collapse and
cessation of gas exchange, and preventing excessive N
2
uptake
(Fig. 1A,D).
It was hypothesized that if reinforced airways are crucial for
alveolar collapse, the anatomical differences between the harbor
seal and California sea lion would result in differences in alveolar
collapse depth. However, these differences in the terminal airways
did not result in a marked difference in the pressure-related
pulmonary shunt during forced dives in a pressure chamber
(Kooyman and Sinnett, 1982). One explanation may be the
significant variation in compliance estimates of the upper airways
between species (Bagnoli et al., 2011; Davenport et al., 2013;
Moore et al., 2014). A comparative study showed that deep-diving
pinnipeds have a more compliant trachea as compared with more
shallow-diving species whereas deep-diving cetaceans have a stiffer
trachea than shallow-diving cetaceans (Moore et al., 2014).
Theoretical work suggests that the structural properties of the
various components of the respiratory system may significantly alter
the response to pressure (Fig. 1A,D) (Bostrom et al., 2008; Fahlman
et al., 2009). Studies on forced diving seals have shown that the
trachea does compress during diving (Fig. 1B,C) (Kooyman et al.,
1970). In addition, both theoretical work and studies on cadavers
and live animals agree that the alveolar collapse depth when gas
exchange ceases is probably significantly deeper (Kooyman and
Sinnett, 1982; Bostrom et al., 2008; Fahlman et al., 2009; Moore
et al., 2011; McDonald and Ponganis, 2012) than suggested from
studies that estimate the alveolar collapse depth based on blood N
2
tension (Kooyman et al., 1972; Falke et al., 1985) or muscle N
2
tension (Ridgway and Howard, 1979), even when the animals
exhale prior to the dive (Kooyman and Sinnett, 1982). The effect of
pressure on the respiratory system is complex and there is currently
limited information available.
While tracheal stiffness may be important for diving ability,
submucosal vascular structures in the conducting airways have been
reported in both cetaceans (striped dolphin, Stenella coeruleoalba;
bottlenose dolphin; Baird’s beaked whale, Berardius bairdii;
pygmy sperm whale; sperm whale, Physeter macrocephalus) and
phocids (ringed seal, Phoca hispida; Weddell seal; crabeater seal,
Lobodon carcinophagus) (Welsch and Drescher, 1982; Cozzi et al.,
2005; Ninomiya et al., 2005; Smodlaka et al., 2006; Bagnoli et al.,
2011; Costidis and Rommel, 2012; Davenport et al., 2013; Moore
et al., 2014). This plexus consists primarily of large veins and some
arterioles, which may engorge and fill the tracheal lumen with
blood, thus reducing the internal volume of the airway, preventing
extreme intraluminal negative pressures and minimizing deformity
of the tracheal wall. With increasing pressure, tracheal compression
may eventually result in negative pressures, which fills the veins and
alters the effective tracheal compliance. This will affect the
observed relationship between pressure and volume, and will alter
the results based on measured structural properties on excised
tracheal sections (Moore et al., 2014). Consequently, the effects of
pressure on the respiratory system are complex and may also be
affected by blood-flow regulation to areas that experience
intrathoracic pressures that are below the environmental pressures.
In addition, rigid air spaces like cranial sinuses (which do not exist
in pinnipeds) and middle ear cavities are also lined with venous
plexuses, which would engorge at depth to prevent barotrauma
(Odend’hal and Poulter, 1966; Leith, 1989; Costidis and Rommel,
2012; Ponganis, 2015).
These results indicate that different species may have alternative
traits or behaviors that minimize diving-related issues. However,
they are based on post-mortem specimens and only account for the
functional properties of the tissues. Live animals may have
alternative strategies to alter compliance through engorgement of
blood vessels. In addition, rigid airways may also have other
benefits. For example, the increased airway stiffness in sea lions and
cetaceans helps to explain how maximal flow can be maintained
over the entire lung capacity (see the ‘Flow–volume limitations’
section), which allows the surface interval to be short while
porpoising (Kooyman and Sinnett, 1979; Kooyman and Cornell,
1981; Fahlman et al., 2015b). In cetaceans, a functional air volume
is required for sound production, and for an adult Cuvier’s beaked
(Ziphius cavirostris) whale diving to 3000 m this air volume would
be approximately 240 ml (Scholander, 1940; Kooyman, 1973;
Schorr et al., 2014). Future studies using medical imaging of live
diving specimens may allow us to clarify the importance of the
structural properties of the upper airways for diving ability (Leith,
1989).
Lung compliance and collateral ventilation
In excised lungs, the pressure–volume relationship during inflation
was similar between otariids, phocids and odontocetes (Fahlman
et al., 2011). By contrast, during expiration, the pressure–volume
curves diverge: for recoil pressures from 30 cmH
2
O to 10 cmH
2
O,
the reduction in volume was lower in the phocid than the odontocete
(Denison et al., 1971; Kooyman and Sinnett, 1979; Fahlman et al.,
2011). At lower volumes, the odontocete lung appears to be less
compliant; these results suggest that the alveolar collapse depth is
greater in odontocetes than in phocids (see fig. 4 in Fahlman et al.,
2011). This is in agreement with results on cadavers imaged at
pressure, for which the alveolar collapse depth was greater for
cetaceans than for pinnipeds when the diving lung volume was
maximal (Moore et al., 2011).
In studies on live anesthetized animals, inflation volumes
are generally much lower to prevent alveolar rupture from
overexpansion. As the pulmonary pressure–volume relationship is
not linear, and as the method of analysis differs, comparisons
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between studies on excised tissues and those on live animals are
difficult. The previously published data have been reanalysed below
to allow a direct comparison. Because lung compliance (C
L
) varies
with M
b
(Stahl, 1967), we computed ‘specific compliance’(sC
L
,
cmH
2
O, measured C
L
was divided by the estimated MAV)
(Fahlman et al., 2014), in order to provide an index that is
independent of animal size (Table 2).
The sC
L
of excised lungs estimated using the equation by
Venegas et al. (1998) was greater in the phocid than the odontocete.
Using the same equation to reanalyse curves of the excised lungs
from the California sea lion (see table 2 in Fahlman et al., 2011)
suggests that the functional properties of the sea lion lung may be
similar to those of phocid lungs during inflation and odontocete
lungs during deflation. However, this conclusion should be viewed
with caution given the large variation in these estimates owing to the
limited numbers of samples.
The sC
L
from live anesthetized seals and sea lions, and awake
bottlenose dolphin, Patagonia sea lion, walrus and pilot whale are
similar to the results from excised lungs (Table 2). The sC
L
estimates from marine mammals collected so far, with the exception
of the pilot whale, are greater than the mean value in humans.
Interestingly, the sC
L
in anesthetized pinnipeds is significantly
higher in animals from the wild that were confirmed to be free of
respiratory disease (Table 2, California sea lion, harbor seal,
northern fur seal) compared with those managed under human care
(Steller sea lion) (Fahlman et al., 2014). These results may have
been caused by the difference in age between the two groups, but
may also indicate that lung conditioning and repeated diving alters
lung function. Interestingly, humans undergoing divers lung
training have been shown to increase VC (Johansson and
Schagatay, 2012), possibly suggesting that there is considerable
plasticity in mammalian lung function (Butler et al., 2012).
Consequently, differences in life history, rather than evolutionary
divergence, may explain the results presented by Piscitelli et al.
(2010) on differences in lung size between deep- and shallow-
diving species.
Taken together, these differences are interesting and may indicate
biochemical differences in the lung surfactants between species
(Spragg et al., 2004; Miller et al., 2005, 2006a,b; Gutierrez et al.,
2015), an active role of bronchial myoelastic sphincters (Kooyman,
1973; Kooyman and Sinnett, 1979; Ninomiya et al., 2005; Piscitelli
et al., 2013) and/or variation in lung architecture such as collateral
ventilation (see Glossary; Fahlman et al., 2011). During preliminary
experiments in the excised lungs of a harbor seal, a white-sided
dolphin and a pilot whale, we noted the possibility of collateral
ventilation in the cetaceans but not in the seal (A.F and M.J.M.,
unpublished observation). We used the Chartis system (https://
pulmonx.com/ous/products/chartis-system/) to quantify collateral
ventilation in an anesthetized bottlenose dolphin (A.F., D.G.-P. and
E. Cases, unpublished observation), but the level of collateral
ventilation was above anything measured in humans, and the system
was unable to make an accurate estimate. We propose that indirect
secondary pathways (e.g. pores of Kohn) open as the
transpulmonary pressure increases to allow air to be shunted
through connections between the alveoli or bronchi (Macklem,
1978; Cetti et al., 2006), and this may help prevent elevated
transpulmonary pressures and facilitate the recruitment of collapsed
alveoli (Namati et al., 2008).
Gas exchange during diving
In the lung, gas diffusion occurs between the gas-filled alveolar
space and the pulmonary capillaries through the alveolar membrane.
Fick’s law of diffusion states that the rate of diffusion increases with
increasing alveolar partial pressure, increasing alveolar surface area
and decreasing diffusion distance. Scholander proposed that as an
animal descends, the diffusion rate would increase, reach a
maximum and then decrease to zero upon alveolar collapse
(Fig. 1D, rigid trachea; Scholander, 1940). The initial rise in
diffusion rate is caused by an increasing alveolar–venous partial
pressure gradient as the ambient pressure increases. However,
alveolar compression both reduces the surface area available for
diffusion and increases the diffusion distance (the alveolar
membrane thickness), thereby decreasing the diffusion rate.
The pulmonary shunt was measured in harbor seals and
California sea lions submerged in a pressure chamber up to
10 ATA (atmospheres absolute) (90 m; Kooyman and Sinnett,
1982). The results showed that the shunt increased with pressure but
decreased with the diving lung volume, and Kooyman and Sinnett
(1982) estimated that full shunt would have occurred at a depth
>150 m. Recent work on free-diving California sea lions agrees, and
predicts that the alveolar collapse depth is significantly deeper than
100 m, which disagrees with the much shallower alveolar collapse
depth from studies in the Weddell seal (Falke et al., 1985) and
bottlenose dolphin (Ridgway and Howard, 1979). Bostrom et al.
(2008) suggested that a number of varying assumptions between the
different studies could explain the difference in estimated alveolar
collapse depth. Bostrom and colleagues combined the model of
lung compression (Bostrom et al., 2008) with a model that allows
the prediction of lung, blood and tissue gas contents (Fahlman et al.,
2006) to provide a theoretical framework explaining how pressure
affects the lungs and gas exchange (Fahlman et al., 2009). The
results from this model agree with Scholander’s predictions, and
suggest that the initial increase in diffusion rate followed by a
decrease indicates an increasing pulmonary shunt that develops with
depth (Fig. 1A,D) (Bostrom et al., 2008). Following alveolar
collapse and cessation of gas exchange, the model indicates that
there should be a sudden drop in arterial P
N
2
as venous blood
bypasses the lung without exchanging gases. Thus, upon alveolar
collapse, the arterial gas tensions should reflect mixed venous gas
tensions. This model provides a unified theory that extends
Scholander’s alveolar collapse theory and provides an explanation
for the differences between estimated alveolar collapse depths
between different studies and species (Fitz-Clarke, 2007; Bostrom
et al., 2008; Fahlman et al., 2009).
These studies have shown how theoretical models may provide
useful insights into complex physiological systems, where a number
Table 2. Values of specific lung compliance (sC
L
) for a range of marine
mammal species
Species
sC
L
(cmH
2
O) Reference
Harbor seal 1.48±0.03 Fahlman et al., 2011, 2014
Elephant seal 0.68±0.20 Fahlman et al., 2014
Steller sea lion 0.25±0.05 Fahlman et al., 2014
California sea lion 0.92±0.16 Fahlman et al., 2014
Northern fur seal 1.58 Fahlman et al., 2014
Patagonia sea lion 0.41±0.10 Fahlman and Madigan, 2016
Walrus 0.61 Fahlman et al., 2015a
Bottlenose dolphin 0.31±0.04 Fahlman et al., 2015b
Pilot whale 0.13 Olsen et al., 1969
Human 0.08–0.12 Stahl, 1967; Stocks and Quanjer, 1995;
Galetke et al., 2007; West, 2012
sC
L
is computed as the measured lung compliance divided by the minimum air
volume (see the ‘Lung compliance and collateral ventilation’section).
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Journal of Experimental Biology

of studies with seemingly varying results can be explained on the
basis of a unifying theory (Scholander, 1940; Ridgway et al., 1969;
Kooyman et al., 1972; Ridgway and Howard, 1979; Falke et al.,
1985; McDonald and Ponganis, 2012; Hooker and Fahlman, 2015;
Hodanbosi et al., 2016). However, it is important to realize that
model outputs from these theoretical constructs, such as estimating
blood and tissue gas distribution during diving, are limited by
available information about basic respiratory physiology (e.g.
minute ventilation, V
T
,f
R
, PEF, PIF, diving lung volume), the
structural properties of the various portions of the respiratorysystem
(e.g. compliance), and the link between cardiac and respiratory
function in live animals (Bostrom et al., 2008; Fahlman et al., 2009).
However, an improved understanding of respiratory function in
pinnipeds and cetaceans will help us to improve the accuracy of
these models, which in turn will allow us to generate new
hypotheses and further develop our understanding of the
mechanism of the physiological limitations to diving imposed by
the respiratory system in these species. For example, the theoretical
lung compression model only assumes passive compression of the
respiratory system to alter the pulmonary shunt. In sea lions, unlike
terrestrial mammals, hypoxia causes vasodilatation of pulmonary
vessels (Olson et al., 2010). This may shunt blood away from
ventilated areas to collapsed hypoxic areas, increasing the
functional shunt. In other words, the animals may re-route blood
flow to avoid gas exchange and create an intrapulmonary shunt.
Furthermore, in the zoological community it is known that
cetaceans are able to control buoyancy without exhaling, possibly
by modulating intrathoracic pressures. This may be a method to
actively collapse some lung areas and adjust the shunt by active
compression of the chest or lung, not relying solely on hydrostatic
pressure. However, these potential mechanisms available to
minimize complications during diving require further study.
Conclusions
In 1929, August Krogh, the Nobel laureate and grandfather of
comparative physiology, first mentioned how some animals appear
to have been purposefully created for certain physiological
problems (Krogh, 1929). This later became known as the Krogh
principle, and it states that ‘For every defined physiological
problem, there is an optimally suited animal that would most
efficiently yield an answer’. The respiratory physiology of marine
mammals is a perfect example of that principle. For example, the
highly compliant chest of seals and sea lions provide a great
example of how these species prevent lung squeeze. Understanding
the respiratory traitsthat allow marine mammals to manage life in an
extreme environment and cope daily with alveolar collapse and
recruitment, extreme respiratory flow, transient hyperoxia, extreme
hypoxia, hyper- and hypotension, intravascular gas bubbles, lung
squeeze and inert gas narcosis is vital in understanding the
physiological constraints imposed on these animals, and how
these limitations may affect survival.
Few studies have investigated respiratory physiology in live or
awake marine mammals (Olsen et al., 1969; Ridgway et al., 1969;
Kerem et al., 1975; Kooyman and Cornell, 1981; Fahlman et al.,
2015b; Fahlman and Madigan, 2016). Whereas useful information
can be derived from comparative studies from the molecular level to
cellular, organ, systemic and whole-animal levels, probably the most
valuable tool for an integrated understanding of how respiratory
physiology affects diving capability is the ability to work with live
trained animals voluntarily participating in research trials. Under
these conditions, the ontogenyand phylogenyof respiratory function
or mechanics can be investigated, and this may allow usto assess the
traits required to allow deep and prolonged diving without ensuing
barotrauma or problems associated with decompression.
Consequently, knowledge of the combination of structural and
functional responses may be crucial to our understanding of the
physiological and mechanical mechanisms that allow marine
mammals to prevent potential complications associated with diving.
A better understanding of the respiratory physiology of marine
mammals may explain the convergent evolution of traits to prevent
barotrauma, and enable alveolar collapse and recruitment. Improved
understanding of respiratory physiology will also increase our
understanding of how marine mammals manage gases during
diving and how this improves aerobic dive durations while
minimizing the risk of gas emboli and N
2
narcosis. In addition,
many of the physiological solutions allowing marine mammals to
avoid trauma during prolonged deep diving may be of clinical
importance to humans and have potential medical applications. For
example, understanding how marine mammals are able to fully
collapse and recruit the alveoli without apparent trauma may have
implications for people undergoing surgery where atelectasis is
likely or for prematurely born children where the lung surfactants
are not fully developed.
Acknowledgements
We are grateful to the many excellent colleagues, animal care specialists and
students that have enabled us to complete a small portion of the studies in this
review. We are also grateful for the past studies that have given us the background
information, and for the many researchers and colleagues that have inspired and
provided comments. Four referees provided constructive criticism, which we believe
significantly improved this paper. A special thank you to Stephen Loring and James
Butler for always answering an endless stream of questions, and to Gerry Kooyman
for providing a copy of the original radiographs from his 1970 study to be reproduced
here. We are grateful for the patience and continuous help from Charlotte Rutledge
during the revisions of this review.
Competing interests
The authors declare no competing or financial interests.
Author contributions
A.F. wrote the paper, prepared the figures and completed the analysis of previous
data; M.J.M. and D.G.-P. participated in discussions on the content, provided advice
and references and helped edit the paper.
Funding
Funding for this project was provided by the Office of Naval Research (ONR YIP
Award no. N000141410563).
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