COMPARING THORACIC MORPHOLOGY AND LUNG SIZE IN SHALLOW
(TURSIOPS TRUNCATUS) AND DEEP (KOGIA SPP.) DIVING CETACEANS
Marina A. Piscitelli
A Thesis Submitted to the
University of North Carolina Wilmington in Partial Fulfillment
of the Requirements for the Degree of
Master of Science
Department of Biology and Marine Biology
University of North Carolina Wilmington
2009
Approved By
Advisory Committee
_____________________________
Dr. Timothy Ballard
____________________________
Dr. Richard Dillaman
_____________________________
Dr. Stephen Kinsey
___________________________
Dr. Sentiel Rommel
___________________________________
Dr. D. A. Pabst
Accepted by
DN: cn=Robert D. Roer, o=UNCW,
ou=Dean of the Graduate School &
Research, email=roer@uncw.edu, c=US
Date: 2009.12.15 16:42:07 -05'00'
___________________________________
Dean, Graduate School
This thesis has been prepared in the style and format
consistent with the journal
Journal of Morphology
ii
TABLE OF CONTENTS
Page
ABSTRACT................................................................................................................. iv
ACKNOWLEDGEMENTS......................................................................................... vi
DEDICATTION ...................................................................................................... ..viii
LIST OF TABLES....................................................................................................... ix
LIST OF FIGURES ..................................................................................................... xi
INTRODUCTION .........................................................................................................1
MATERIALS & METHODS ......................................................................................15
Specimens……………………………………………….…………….….15
Measures of Lung Size: Mass………………… ....……….……….……..16
Measures of Lung Size: Volume.........…………………...……….……...19
Measures of Lung Volume: Whole Body Cross-Sections .......….……….22
Gross Morphology of Skeleton……….......…………………….………..27
Mobility of Isolated Thoraxes........…………………….……….………..28
Thoracic Cavity Volume Models…….......………………….……….......32
RESULTS ....................................................................................................................36
Lung Mass...................………………………………………..……….…37
Excised Lung Volume....………………………..…………………….….44
In situ Lung Volume Calculated from Whole Body Cross-Sections.........48
Mobility of Isolated Thoraxes.......…………………………………….…54
Thoracic Cavity Volume Models.......…………………………………....58
DISCUSSION ..............................................................................................................60
CONCLUSION............................................................................................................80
LITERATURE CITED ................................................................................................82
APPENDIX..................................................................................................................95
iii
ABSTRACT
Coastal bottlenose dolphins (Tursiops truncatus) dive to depths of 1-10m while
pygmy and dwarf sperm whales (Kogia breviceps and K. sima) are estimated to dive
between 400-1,000m. These divers will experience vastly different external pressures at
depth that will, according to Boyle’s and Pascal’s gas laws, influence the volume of air
within their lungs and potentially the amount of thoracic collapse they experience. The
goal of this study was to test the hypotheses that lung size will be reduced and/or thoracic
mobility will be enhanced in deeper diving cetaceans. T. truncatus and Kogia spp. were
compared because relatively large samples of stranded individuals were available.
Thoracic vascular structures were also compared. Lung size was investigated by
comparing lung mass (T. truncatus, n = 111; kogiids, n = 18) and lung volume (T.
truncatus, n = 5; kogiids, n = 4) to total body mass. One T. truncatus and one K. sima
were cross-sectioned whole to calculate lung (as well as thoracic vasculature and other
organ) volumes as a percent of total thoracic cavity volume. Excised thoraxes were
mechanically manipulated into maximally expanded and collapsed postures (T. truncatus,
n = 3; kogiids, n = 5) to compare changes in thoracic cavity shape and volume.
Kogiid lungs were one-half the mass, and between 20-50% of the volume of those
of similarly-sized T. truncatus. The lung occupied only 15% of the total thoracic cavity
volume in K. sima and 37% in T. truncatus, while thoracic arterial retial tissue occupied
8.9% in K. sima and 4.9% in T. truncatus. The kogiid and bottlenose dolphin thoraxes
underwent similar changes in shape and volume. The only significant difference in
thoracic mobility was at the thoracic inlet; the change in width of the inlet was
constrained in kogiids relative to T. truncatus. Thus, the deeper diving kogiids possess
iv
smaller lungs, more voluminous thoracic vasculature, and a similarly mobile thorax as
compared to the shallow diving T. truncatus.
Calculations based upon mass specific metabolic rates and total lung capacities
suggest that the large lung of the shallow diving, “fast” breathing T. truncatus can
provide the oxygen reserves required to meet the metabolic demands of swimming on a
breath-hold. The mobility of the thorax in this species may accommodate the large
changes in air volume routinely experienced during shallow diving, and may function to
permit rapid changes in thoracic volume required during its explosive ventilation. In
contrast, the deep diving, “slow” breathing kogiids possess relatively small lungs, and
will, thus, experience reduced pressure-induced changes in both lung and thoracic
volumes at depth.
A broader phylogenetic comparison demonstrated that the ratio of lung mass to
total body mass in kogiids, physeterids, ziphiids and mysticetes is similar to that of
terrestrial mammals, while delphinids and phocoenids possess relatively large lungs.
Thus, small lung size in deep diving odontocetes may be a plesiomorphic character,
rather than a specialization for diving. The large lung size of delphinids and phocoenids
appears to be a derived condition that may permit the lung to function as a site of
respiratory gas exchange during a dive in these relatively short-duration, shallow divers.
v
ACKNOWLEDGEMENTS
This study on every level required a collaborative effort. There are many people
to thank at multiple institutions. First and foremost, I would like to acknowledge the
tremendous amount of assistance, both mentally and physically, provided by Dr. Ann
Pabst, Bill McLellan, and Dr. Sentiel Rommel. I would first like to especially thank my
wonderfully patient and genuine advisor, Dr. Ann Pabst. Without her guidance,
inspiration, enthusiasm and willingness to go above and beyond what is required, I would
not have been able to complete this project.
I would also like to express my endless appreciation to Bill McLellan for his
masterful ability in meeting every challenge in this study, from excising whole thoraxes
to inflating lungs, and for his creative ideas and thoughtful discussions. I would also like
to express my sincere appreciation to Dr. Sentiel “Butch” Rommel for all the
encouragement along the way, and for his thoughtful critiques and ideas that have led to a
better understanding of the mechanisms at hand.
I would like to acknowledge all of my unbelievably wonderful lab mates, with
special thanks to Brian Balmer, Peter Nilsson, Ryan McAlarney, Sarah Pagentine, and
Laura Bagge, who were always willing to lend a hand at a moment’s notice and provided
endless critiques. I would like to thank Dr. Andrew Westgate for his insights into
pressurized systems and access to his pressure vacuum module, and Dr. James Blum in
the Department of Mathematics and Statistics at UNCW, for his help with analysis of
multiple data sets. I would also like to thank Mark Gay for his patience and repeated
assistance with both histology and image analysis, and Jim Moravansky, computer tech
master, for his fruitful efforts in rescuing data from multiple crashed hard drives.
vi
For sample collection, I would like to thank the Virginia Aquarium Stranding
Response team, especially Sue Barco, for open access to their database and facility, and
for always having such willingness to collect samples. I would especially like to thank
Dr. James Mead at the Smithsonian Institute for the conception of the idea of creating
these databases, and all the employees and volunteers, both at VAQS and UNCW Marine
Mammal Stranding Programs, for their diligence over the past two decades in ensuring
they are kept up to date and accurate. I would also like to extend my gratitude to
Gretchen Lovewell, NIMFS NOAA Beaufort and Dr. Craig Harms, NC State University
for their wonderful support in sample collection. Much appreciation is also expressed to
Dr. Dave Rotstein, NIMFS NOAA, for his wonderful insights into Kogia lungs, and Alex
Costidis for the insightful discussions on Kogia vasculature. I also offer much gratitude to
the Florida Marine Mammal Pathology Laboratory, especially Andy Garrett, for access to
their facility for whole body cross-sectioning.
Finally, I would like to thank those that have willingly served on my committee,
Drs. Timothy Ballard, Richard Dillaman, Stephen Kinsey, and Sentiel “Butch” Rommel.
All of who have provided valuable insights, critiques, and thoughtful questions at every
step in producing this final product.
vii
DEDICATION
I dedicate this thesis to my family, especially my parents Deborah and Eugene
Piscitelli, Jr., who have supported me through myriad opportunities and challenges.
Thank you for always nurturing a curious, creative, and adventurous attitude towards life.
I would also like to acknowledge the strong support of my brothers, Noah Mehrkam and
Eugene “Anthony” Piscitelli, III, who have always enthusiastically encouraged me to
pursue a profession with passion and verve.
viii
LIST OF TABLES
Table
Page
1. Cetacean species utilized in the broader phylogenetic comparison for which
previously published values of lung and total body mass were available ...............7
2. Lung variables compared to total body mass (kg) in terrestrial and marine
mammals ................................................................................................................17
3. Measurements used to calculate total body volume (Vb).......................................26
4. Summary of allometric relationships between organ mass and total body
mass........................................................................................................................38
5. Lung volume measurements for kogiids and T. truncatus.....................................45
6. Mean lung air volume (± S.E.) measures for T. truncatus and Kogia spp.
compared to P. phocoena (n = 4) (*data from Kooyman and Sinnett 1979).........46
7. A comparison of estimated total lung capacity (TLC), based upon
measurements from this study, and those predicted from a variety of existing
allometric relationships based upon total body mass (TBM) ................................49
8. Absolute (L) and relative (%) volumes of organs, vascular tissues and specific
cavities within the entire musculoskeletal thorax calculated from whole body
cross-sections of a single K. sima and T. truncatus ...............................................50
9. The mean (± S.D.) percent difference between the maximal cranially expanded
to caudally collapsed postures (averaged across ribs 1-5) for thoracic dimensions
measured for each species (* denotes significant differeces) ................................55
10. Cranial thoracic cavity volume (L) calculated from whole body cross-sections
and calculated via four geometric models ............................................................59
11. Cranial thoracic cavity volumes (L), calculated using geometric Model 1, for
cranially most expanded and caudally most collapsed postures............................61
12. Common diving capacity measures for a variety of odontocetes for which a
corresponding lung mass and total body mass ratio was available........................63
13. Summary of allometric relationships between lung mass and total body mass
for diving behavior and myoglobin content...........................................................66
14. Myoglobin values for a variety of odontocetes for which a corresponding lung
mass and total body mass were available ..............................................................67
ix
Page
15. The estimated contribution of lung oxygen stores to meeting metabolic costs
of resting and swimming in T. truncatus and kogiids............................................73
16. Heart mass (kg) vs. total body mass (kg) ratios for a variety of cetaceans............75
17. Liver mass (kg) vs. total body mass (kg) ratios for a variety of cetaceans ............78
x
LIST OF FIGURES
Figure
Page
1. The relationship between gas volume within the lung and dive depth,
based on Pascal’s and Boyle’s gas laws ............................................................4
2. The range of thorax mobility in T. truncatus (A-D) ..........................................9
3. Schematic of the custom-built apparatus used to inflate excised lungs
[container used was a 50 or 100 gallon Rubbermaid® water trough
(Newell Rubbermaid Inc., Atlanta, GA, USA)]...............................................20
4. Lung volume-pressure relationships for species used in this study.................23
5. Each excised thorax was (A) suspended from a stable frame and
manipulated into the defined maximum cranially expanded posture ..............30
6. Example of one of four geometric models of the thoracic cavity used to
calculate volumes at the extreme cranially expanded and caudally
collapsed positions ...........................................................................................33
7. Four geometric models of the thoracic cavity used to estimate cavity
volume changes between a maximally cranially expanded and a maximally
caudally collapsed posture ...............................................................................34
8. Log lung mass (kg) vs. log total body mass (kg) for all age classes and
body conditions of T. truncatus and Kogia spp ...............................................39
9. Ratio of lung mass (kg) vs. total body mass (kg) against total body
length (cm) across all age classes and body conditions of T. truncatus
and Kogia spp ..................................................................................................40
10. Log lung mass (kg) vs. log total body mass (kg) for sub-adults and
adults of T. truncatus and Kogia spp. compared to adult terrestrial
mammals ..........................................................................................................42
11. Log lung mass (kg) vs. log total body mass (kg) for Families Delphinidae
and Kogiidae ....................................................................................................43
12. Log lung mass (kg) vs. log total body mass (kg) for species pooled in
Families Delphinidae and Phocoenidae (D-P) and Kogiidae, Physeteridae,
Ziphiidae (K-P-Z) ............................................................................................47
13. Log of calculated total lung capacity (TLC, in liters) vs. log of total
body mass (kg) for T. truncatus and Kogia spp...............................................51
xi
Page
14. Whole body cross-sections at the level of the heart in a (A) T. truncatus
and (B) K. sima ................................................................................................52
15. In (A) T. truncatus the lungs overlap the heart ventro-laterally ......................53
16. Whole body cross-sections at the level of the inlet to the thorax in a (A)
T. truncatus and (B) K. sima............................................................................56
17. The range of thoracic mobility in Kogia spp ...................................................57
18. The ratio of lung mass vs. total body mass is mapped upon a phylogeny
for cetaceans.....................................................................................................64
19. Log lung mass (kg) vs. log total body mass (kg) of species within five
families (Kogiidae, Physeteridae, Ziphiidae, Delphinidae and
Phocoenidae)....................................................................................................68
20. Log lung mass (kg) vs. log total body mass (kg) of species within five
families (Kogiidae, Physeteridae, Ziphiidae, Delphinidae and
Phocoenidae)....................................................................................................69
21. Log heart mass (kg) vs. log total body mass (kg) for T. truncatus and
Kogia spp. compared to adult terrestrial mammals .........................................76
22. Log liver mass (kg) vs. log total body mass (kg) for T. truncatus and
Kogia spp. compared to adult terrestrial mammals .........................................79
xii
INTRODUCTION
All cetaceans are breath-hold divers, but the depths to which species routinely
dive vary immensely. For example, coastal bottlenose dolphins (Tursiops truncatus) dive
to depths of 1-10m while, on average, Cuvier’s beaked whales (Ziphius cavirostris) dive
to over 1000m (Mate et al. 1995, Barros and Wells 1998, Nowacek 1999, Connor et al.
2000, Reeves et al. 2002, Young and Phillips 2002, Torres et al. 2003, Tyack et al.
2006). These two divers will experience vastly different external pressures at depth that
will, according to Boyle’s and Pascal’s gas laws, influence the volume of air within their
lungs and potentially the amount of thoracic collapse they experience (reviewed in
Scholander 1940, Ridgway et al. 1969, Taylor 1994, Skrovan et al. 1999). This study
investigated lung size and thoracic mobility in the shallow diving bottlenose dolphin (T.
truncatus) and the deeper diving pygmy and dwarf sperm whales (Kogia breviceps and
Kogia sima). These species, chosen because relatively large samples of stranded
individuals were available, were used to test the hypotheses that lung size will be reduced
and/or thoracic mobility will be enhanced in deeper divers.
Marine mammals possess a suite of anatomical and physiological specializations
that enhance diving ability, including large body size, increased on-board oxygen stores,
reduced metabolic costs, and energy-saving locomotor strategies (e.g. Scholander 1940,
Kooyman and Andersen 1969, Ridgway 1971, Kooyman 1989, Schreer and Kovacs
1997, Kooyman et al. 1999, Skrovan et al. 1999, Williams et al. 1999, Williams et al.
2000, Nowacek et al. 2001, Miller et al. 2004). Both dive depth and duration can be
extended by increasing on-board oxygen stores (Scholander 1940, Kooyman 1973,
Kooyman 1985, Kooyman et al. 1999, reviewed in Pabst et al. 1999, Noren and Williams
2000, Duffield et al. 2003). It has been demonstrated in pinnipeds, for example, that
deeper diving Weddell seals (Leptonychotes weddellii) (common depth 150-400m, max
depth 500-740m; Kooyman 1966, Kooyman et al. 1971, Castellini et al. 1992, Williams
et al. 2000) possess a relatively larger blood volume, higher hematocrit, and higher
hemoglobin and myoglobin concentrations than does the more shallow diving California
sea lions (Zalophus californianus) (common depth 60-65m; max depth 250-480m; Gentry
et al. 1986, Feldkamp et al. 1989, Melin et al. 1993, Orr and Aurioles-Gamboa 1995)
(Kooyman 1985). The role of the lung as an oxygen store appears to be reduced in both
species, relative to human divers. Alveolar collapse has been demonstrated to occur at
between 30-80m depth in pinnipeds (Scholander 1940, Kooyman et al. 1970, Kooyman
et al. 1971, Kooyman et al. 1973, Denison et al. 1971, Williams et al. 2000, Falke et al.
2008). Thus, deeper divers do not rely upon their lungs as an oxygen store at depth
(Kooyman 1985, Schmidt-Nielsen 1984).
The total on-board oxygen stores in cetaceans have not been less well studied, but
it is known that deeper diving species do have higher myoglobin concentrations in their
locomotor muscles and larger blood volumes than do shallow divers (Ridgway and
Johnston 1966, Ridgway and Harrison 1986, Noren and Williams 2000, Dolar et al.
1999). Cetaceans also experience alveolar collapse during a dive. The depth at which
alveolar collapse occurs was first predicted from intramuscular nitrogen tensions
measured in two trained bottlenose dolphins as they completed a series of repetitive dives
to 100m (Ridgway and Howard 1979). The results suggested alveolar collapse was
complete at approximately 70m (Ridgway and Howard 1979). A free-swimming
bottlenose dolphin, trained to wear a time-depth recorder and video camera, also
2
appeared to experience alveolar collapse at a depth of approximately 80m (Skrovan et al.
1999). At this depth, the dolphin began gliding downwards, rather than actively
swimming. This change in locomotor behavior, which has been measured in other diving
cetaceans, has been ascribed to reduce whole-body buoyancy due to compression of lung
air volume (e.g. Skrovan et al. 1999, Williams et al. 1999, Williams et al. 2000,
Nowacek et al. 2001, Miller et al. 2004, Tyack et al. 2006).
Based on Boyle’s and Pascal’s laws (Resnick and Halliday 1966), as depth
increases air volume within the lung decreases (Figure 1; reviewed in Taylor 1994).
Thus, the relative contribution of the lung as an oxygen storage site is inversely related to
dive depth. Because deeper divers do not rely upon their lungs as an oxygen store at
depth, Scholander (1940) suggested that lungs of deeper diving cetaceans should be
smaller than those of shallow diving species.
Lung size has been investigated in a number of cetacean species. Lung size can be
reported in multiple ways, including total lung mass (Laurie 1933, Crile and Quiring
1940b, Scholander 1940, Crile 1941, Quiring 1943, Omura 1950, Slijper 1958, Kooyman
et al. 1971, Smith and Pace 1971, Bryden 1972, Leith et al. 1972, Perrin and Roberts
1972, Tarasoff and Kooyman 1973, Miyazaki et al. 1981, Lockyer and Waters 1986,
McLellan et al. 2002), total lung volume (Scholander and Irving 1941, Ridgway et al.
1969, Olsen et al. 1969, Denison et al. 1971, Kooyman 1973, Kooyman and Sinnett
1979, Bergey and Baier 1987, Schmidt-Nielson 1997, Falke et al. 2008) and with a
variety of air capacity measurements (Irving et al. 1941, Kenyon 1961, Spencer et al.
1967, Kooyman et al. 1970, Kooyman et al. 1973, Kooyman et al. 1975, Ridgway and
Howard 1979, Kooyman and Cornell 1981, Watson and Gaskin 1983, Ridgway and
3
100
10 L
Surface
Percent volume
gas in lung (%)
Percentof
Volume
90
80
70
60
5L
10 m
50
40
30
20
1L
100 m
1000 m
0.1L
10
0
0
100
200
300
400
500
600
700
800
900
1000
Depth (m)
Depth (m)
Figure 1. The relationship between gas volume within the lung and dive depth, based on Pascal’s and Boyle’s gas laws. The fill in
each box to the right of the curve represents a lung volume of 10L at the surface. Note that air volume decreases by 50% within the
first 10m of descent; below 100m the rate of change in air volume decreases dramatically (reviewed in Taylor 1994). 4
Harrison 1986, Kooyman 1989, Shaffer et al. 1997). Thus, evidence of differences in
relative lung size does exist across clades of cetaceans.
Slijper (1958), for example, reported that the average lung mass of selected
delphinids (Delphinus delphis, Grampus griseus, and Lagenorhynchus acutus) and harbor
porpoises (Phocoena phocoena) were larger than those of similarly-sized terrestrial
mammals. Mysticetes (Megaptera novaeangliae, Balaenoptera borealis, B. physalus, B.
musculus, Eschrichtius robustus, and Eubalaena glacialis) and sperm whales (Physeter
macrocephalus) possess relative lung masses that are smaller than those of similarlysized terrestrial mammals (Slijper 1958). Miyazaki et al. (1981) reported that the lung
mass to total body mass ratios of stenellids (Stenella attenuata, Stenella coeruleoalba)
were larger than those reported for sperm whales and at least some of the mysticetes
reported by Bryden (1972).
Kooyman (1973) reported that lung volumes of a variety of cetaceans were
slightly larger than those of similarly-sized terrestrial mammals. Delphinids (D. delphis,
G. griseus, and L. acutus) and phocoenids (P. phocoena) appear to possess a larger lung
capacity than do similarly-sized terrestrial mammals (Irving et al. 1941, Slijper 1958,
reviewed in Bryden 1972, Kooyman and Sinnett 1979). In contrast, Irving et al. (1941)
reported that lung capacities of rorquals (M. novaeangliae, B. borealis, B. physalus, B.
musculus), sperm whales (P. macrocephalus), and bottlenose whales (Hyperoodon
ampullatus) were smaller than those of similarly-sized terrestrial mammals (reviewed in
Slijper 1958). Thus, existing data suggest that some deep divers, including sperm whales
and bottlenose whales, possess relatively small lungs, but so do a diversity of mysticetes,
which include shallow diving species. In addition, to date, the number of individuals in
5
which lung size has been investigated for any given species is relatively small (Table 1;
but see Miyazaki et al. 1981 and McLellan et al. 2002).
It has also been hypothesized that deep diving cetaceans possess enhanced
thoracic mobility to accommodate pressure-induced reductions in lung volume at depth
(Scholander 1940, Ridgway et al. 1969, Hui 1975, Rommel 1990). That is, during a dive,
as the air volume within the lungs compress and total lung volume is reduced, the thorax
must also simultaneously collapse (Scholander 1940, Kooyman and Andersen 1969,
Ridgway et al. 1969, Ridgway 1972, Ridgway and Harrison 1986). Only two cetacean
studies, both on relatively shallow diving delphinids, have described thoracic collapse
under pressure (Ridgway et al. 1969, Hui 1975). Thoracic shape change was observed to
be a gradual process in a free-diving U.S. Navy bottlenose dolphin named “Tuffy”. At
10m Navy divers observed changes in thoracic shape, and by 60m the collapse of the
thorax was reported to be very apparent, especially in the area behind the pectoral flipper
(Ridgway et al. 1969). The only published photographic evidence of this thoracic
collapse is of “Tuffy” at 300m (Ridgway et al. 1969). These qualitative observations
suggested that the flexible thorax of a bottlenose dolphin continuously changed shape
during a dive (Ridgway et al. 1969).
Hui (1975) investigated the compressibility of the dolphin thorax, by placing a
carcass of a short-beaked common dolphin (D. delphis) in a supine position (i.e. ventral
surface up) in a hyperbaric chamber and subjecting it to two simulated dives to
approximately 70m. Hui (1975) observed a decrease in both thoracic height and width
during the simulated dives. Hui (1975) hypothesized that during thoracic compression the
vertebral rib-sternal rib joints became more acute, and that both the vertebral and sternal
6
Table 1. Cetacean species utilized in the broader phylogenetic comparison for which
previously published values of lung and total body mass were available.
Species
Family
n
Citation
Lockyer and Waters 1986,
Omura 1950, Leith and Lowe
1972*
Balaenoptera borealis
Balaenopteridae
22
Balaenoptera musculus
Balaenopteridae
1
Laurie 1933
Balaenoptera physalus
Balaenopteridae
14
Lockyer and Waters 1986,
Quiring 1943, Leith and Lowe
1972*
Stenella attenuata
Delphinidae
60
Miyazaki et al. 1981, Perrin and
Roberts 1972
Stenella coeruleoalba
Delphinidae
40
Miyazaki et al. 1981
Stenella longirostris
Delphinidae
4
Perrin and Roberts 1972
Phocoena phocoena
Phocoenidae
9
Crile and Quiring 1940b,
Kooyman and Sinnett 1979,
McLellan et al. 2002***
Delphinapterus leucas
Monodontidae
3
Crile and Quiring 1940b,
Ridgway and Harrison 1986
Physeter macrocephalus
Physeteridae
10
Omura 1950
Kogia sp.
Kogiidae
1
Scholander 1940
Berardius bairdii**
Ziphiidae
1
Balcomb 1989**
Hyperoodon ampullatus
Ziphiidae
1
Scholander 1940
Ziphius cavirostris
Ziphiidae
1
Quiring 1943, Kenyon 1961,
reviewed in Bryden 1972
* body mass estimated from published length - weight data
** body mass estimated by Sleptsov 1961 = 8.848 metric tons
*** values used from this source were means from each of four life history categories
(n = 122 total individuals)
7
ribs rotated caudally to decrease thoracic width. Physical manipulations of isolated
bottlenose dolphins thoraxes support these hypotheses (Cotten et al. 2008). Thoracic
cavity volume was observed to decrease by the rotation of the vertebral rib-sternal rib
joints medially (decrease in width) and dorso-caudally (decrease in height) (Figure 2).
These changes in thoracic shape have been attributed to the enhanced flexibility
of the musculoskeletal thorax (Scholander 1940, Ridgway et al. 1969, Hui 1975, Rommel
1990). To date, though, no functional morphological data exist on potential thoracic
shape change in any deep diving cetacean. Interestingly, deep diving cetaceans lack the
specialized thoracic morphologies observed in the flexible bottlenose dolphin thorax (e.g.
bony sternal ribs and associated mobile joints) (Ridgway et al. 1969, Hui 1975, Rommel
1990, Cotten et al. 2008), and instead possess cartilaginous sternal ribs (Benham 1902,
Nagorsen 1985) that may limit thoracic collapse.
Although it has been hypothesized that deeper divers possess enhanced thoracic
mobility to accommodate reductions in lung volume at depth, recent data from freeswimming Weddell seals (Leptonychotes weddellii) suggests such collapse may be
relatively limited (Falke et al. 2008). This study demonstrated that the seal’s thoracic
circumference decreased by less than 2% when measured at 196m. Falke et al. (2008)
hypothesized that thoracic shape may be maintained at depth because as the lungs
collapse, vascular structures within the thorax may become engorged. Phocid seals
possess elaborate venous structures within their thoracic cavity that would accommodate
such a response (Harrison and Tomlinson 1956, Ponganis et al. 2006, Falke et al. 2008).
Two mechanisms that may aid in this process are intrathoracic blood pooling and the
8
A
C
B
D
Figure 2. The range of thorax mobility in T. truncatus (A-D). The body outline in each of
the lateral views (C-D) is fixed between positions. (A) and (C) depict the cranially most
expanded posture, while (B) and (D) depict the caudally most collapsed posture. These
changes in posture occur due to movement at joints between the vertebrae and vertebral
ribs, vertebral and sternal ribs, and sternal ribs and sternum. (Image from Cotten et al.
2008)
9
thoracic (respiratory) pump (Wislocki 1929, Craig 1968, Schaefer et al. 1968, Fanning
and Harrison 1974, Ponganis et al. 2006, Falke et al. 2008).
Intrathoracic blood pooling has been observed in several studies in human breathhold divers (Craig 1968, Schaefer et al. 1968, reviewed in Ferrigno and Lundgren 1999).
As one component of the dive response, systemic vasoconstriction occurs and blood is
redistributed from the periphery into the thorax (Scholander 1940, Craig 1968). This
redistribution of blood volume may help collapse the lungs, and thus contribute to
maintaining pressure equilibrium across the thoracic wall (Craig 1968). Schaefer et al.
(1968) estimated that in a human breath-hold diver, 1.4 to 1.7L of blood was redistributed
into the thorax. This volume represents 25-30% of an average adult human’s total blood
volume (approximately 5.5L; Saladin 2007).
The thoracic (respiratory) pump is a mechanism that aids the flow of venous
blood from the abdominal to the thoracic cavity during ventilation (Saladin 2007,
Ponganis et al. 2006). During inhalation, the thoracic cavity expands and the internal
pressure drops. Simultaneously, the caudal movement of the diaphragm raises pressure in
the abdominal cavity. As a result of this pressure differential, blood is squeezed cranially,
via the caudal vena cava, from the abdominal to the thoracic cavity (Saladin 2007).
Cetaceans are known to inhale prior to a breath-hold dive (Scholander 1940). Thus, the
thoracic pump may bring venous blood into the thorax just prior to diving and
intrathoracic blood pooling may occur as part of the dive response once submerged at
depth.
These two vascular responses, which are well-documented in humans, suggest
that deeper diving cetaceans, which likely have larger blood volumes than do shallow
10
divers (Ridgway and Johnston 1966, Ridgway and Harrison 1986), may redirect a large
amount of blood into the thoracic cavity during a dive. If this hypothesis is true, then one
would expect a deeper diving cetacean to possess more voluminous vascular structures
within its thoracic cavity (Melnikov 1997), as well as mechanisms of blood movement
from the periphery to the thorax.
Scholander (1940) referred to vascular structures that could dynamically change
shape as “swelling” and “displacement” organs. There are a number of vascular
structures within the cetacean thoracic cavity that may function in this manner. These
structures include the thoracic arterial rete, venous plexuses within the trachea and
bronchi of the lung, and the pericardial venous plexus (Scholander 1940, Harrison and
Tomlinson 1956, Ridgway 1972, Hui 1975, Vogl and Fisher 1981, Vogl and Fisher 1982,
Melnikov 1997, Ninomiya et al. 2005, Ponganis et al. 2006).
The thoracic arterial rete lies dorsally between the ribs and extends into the neural
canal to form the epidural rete (reviewed in McFarland et al. 1979,Vogl and Fisher 1981,
Vogl and Fisher 1982, reviewed in Pabst et al. 1999, Melnikov 1997). Hui (1975)
suggested that the thoracic rete may affect the degree and pattern of thoracic collapse in a
diving common dolphin (Delphinus delphis). However, Scholander (1940) hypothesized
that the volume of this vascular structure was too small in Phocoena phocoena to permit
it to function as a significant blood reservoir.
Additionally, extensive plexuses of veins, arteries and arterioles, collectively
referred to as retial tissue, are present within the trachea (between the elastic membrane
enclosing the tracheal hyaline cartilage and the smooth muscle layer) of many marine
mammals (Wislocki 1929, Fanning and Whitting 1969, Fanning and Harrison 1974,
11
Smodlaka et al. 2006). In T. truncatus and Baird’s beaked whale (Berardius bairdii), a
venous plexus in the mucosa that lines the airways of the lung, extending from the extrapulmonary bronchi to the terminal bronchi, has also been described (Wislocki 1929,
Fanning and Harrison 1974, Ninomiya et al. 2005). This periarterial venous plexus is
supplied by pulmonary veins and surrounds the pulmonary arteries up to the terminal
airways. Ninomiya et al. (2005) hypothesized that these veins may become engorged
with large volumes of oxygenated blood, which in turn may be transported to the tissues
to allow for longer aerobic dive duration. Finally, a pericardial venous plexus has been described in the harbor porpoise
(Phocoena phocoena), harbor seal (Phoca vitulina), gray seal (Halichoerus grypus),
elephant seal (Mirounga spp.), and leopard seal (Hydrurga leptonyx) (Burne 1910,
Harrison and Tomlinson 1956, Ponganis et al. 2006). This plexus, a continuous venous
ring surrounding the caudal base of the pericardium, connects the caudal vena cava
dorsally and the phrenic veins ventrally. It can possess leaf-like projections into the
pleural cavity formed by thick-walled veins (0.2-0.3mm) surrounded by lobules of brown
fat (Harrison and Tomlinson 1956). However, Scholander (1940) hypothesized that the
volume of these venous plexuses were also too small to function as a “swelling” organ
within the thoracic cavity of Phocoena phocoena.
Based upon Pascal’s and Boyle’s gas laws, the lungs of deep diving cetaceans will
undergo much larger changes in volume than those of shallow diving species. These
differences likely influence the size of the lung and thoracic vascular structures, as well
as the range of mobility of the thorax. Although lung size has been measured in many
species, few studies have investigated explicitly the relationship between lung size and
12
dive depth. It has been hypothesized that the thorax of a deep diver is capable of
undergoing large shape changes and that shape change may occur due to presence of
highly mobile joints within the thoracic skeleton. However, no data exist that compares
the mobility of the thorax in deep and shallow diving cetaceans. Thoracic vascular
structures may potentially affect thoracic shape change, but to date the relative size of
these thoracic vascular structures in a deep versus shallow diving cetacean has not been
investigated.
Thus, the goals of this study were to compare lung size and thoracic mobility
between the shallow diving coastal bottlenose dolphin (T. truncatus) and the deeper
diving pygmy (K. breviceps) and dwarf (K. sima) sperm whales. An additional goal was
to provide insight into the relative volume of thoracic vascular structures across these
cetaceans. These species were chosen because access to a relatively large sample set was
possible through stranding programs in the mid-Atlantic.
The coastal bottlenose dolphin morphotype is found in relatively shallow
estuarine and near shore waters (within 7.5km of shore), and feeds on shallow water prey
(Mate et al. 1995, Mead and Potter 1995, Barros and Wells 1998, Nowacek 1999, Connor
et al. 2000, Young and Phillips 2002, Torres et al. 2003, Gannon and Waples 2004).
Mean dive durations range from 20 to 40sec, and dive depths range between 1 – 10m
(Würsig 1978, Irvine et al. 1981, Shane et al. 1990, Bassos 1993, Mate et al. 1995,
Barros and Wells 1998, Nowacek 1999, Connor et al. 2000, Reeves et al. 2002, Young
and Phillips 2002).
In contrast, pygmy and dwarf sperm whales are rarely sighted at sea and when
observed are usually seen “logging” (resting) at the surface (Allen 1941, Yamada 1953,
13
Nagorsen 1985, Caldwell and Caldwell 1989, Scott et al. 2001). A radio-tracked juvenile
pygmy sperm whale displayed surface intervals ranging from 4sec (77% of surfacings) to
11min (Scott et al. 2001), and a maximum dive duration of 18min (Scott et al. 2001).
Stomach contents and stable isotope analyses demonstrate that kogiids forage primarily
on deep sea squid (Ross 1979, Martins et al. 1985, Klages et al. 1989, McAlpine et al.
1997, Plön et al. 1999, Barros 2003, Santos et al. 2006, Beatson et al. 2007). Kogiids
have been sighted typically in waters 400-1,000m off the eastern coast of North America
(Scott et al. 2001, Fulling 2003, NOAA Stock Report 2005, Dunphy-Daly et al. 2008).
These species will be used to specifically test three hypotheses. The deeper diving
kogiids are hypothesized to possess smaller lungs and/or enhanced thoracic mobility, and
to possess more voluminous thoracic vascular structures than the shallow diving
bottlenose dolphin. Lung size will be investigated by comparing lung mass and volume
relative to total body size. Thoracic mobility will be investigated by mechanically
manipulating excised thoraxes. The static volumes of thoracic vascular structures will be
compared using whole body cross-sections. To broaden the phylogenetic scope of this
study lung mass relative to total body mass will also be investigated across five families
of odontocete cetaceans. Although sample sizes for individual species in this broader
comparative analysis are relatively small, these data permit comparisons across clades
that display different dive depths and durations.
14
MATERIALS & METHODS
Specimens
Carcasses of Atlantic bottlenose dolphins (Tursiops truncatus) (n = 116), and
pygmy (Kogia breviceps) and dwarf (Kogia sima) sperm whales (n = 21) that stranded or
were incidentally killed in fishing operations were utilized in this study (Appendix A).
For all analyses, K. sima and K. breviceps are combined and reported as Kogia spp.
These specimens were collected by the University of North Carolina Wilmington
(UNCW) Marine Mammal Stranding Program, the Virginia Aquarium Stranding
Response Program (VAQS), and the Cetacean and Sea Turtle Team at the National
Marine Fisheries Service Laboratory in Beaufort, North Carolina. Each specimen was
placed into a life history category as defined by Caldwell and Caldwell (1989), Mead and
Potter (1990), Struntz et al. (2004), and Dunkin et al. (2005). All specimens used in this
study were in fresh to moderate condition (Smithsonian Institute Code 1 through 3;
Geraci and Lounsbury 2005). Carcasses were either freshly dissected or frozen within
hours of death and remained frozen until dissection at a later date.
To examine relative lung size across a broader phylogenetic sample of cetaceans,
the stranding archive databases at UNCW and VAQS were searched. All specimens, for
which both a total lung mass and total body mass were available, were included in this
analysis (Appendix B). Similar data were also obtained from previously published reports
(see Table 1 for species and references). These combined data sets provided at least two
individual records for each genus, with the exception of a single individual record for
Hyperoodon ampullatus, Ziphius cavirostris, and Berardius bairdii. In total, these
15
combined data sets yielded lung mass and total body mass for 352 individuals, from 28
species, representing seven families.
Measures of Lung Size: Mass
To test the hypothesis that deeper divers possess relatively small lungs, lung
masses and total body masses were measured. During dissection, lungs were excised
whole from the carcasses. Each lung was dissected free at the level of the primary
bronchus. Left and right lungs were weighed separately using digital scales and their
masses were added together to obtain total lung mass (n = 111 for T. truncatus and n = 18
for Kogia spp.; Appendix A).
The total data set for each species included a broad range of age classes (neonates
through adults) and individual body conditions (robust to emaciated). To determine
whether body condition influenced the relationships between lung mass and total body
mass for the total data set, a regression analysis was performed both with and without
emaciated specimens included. Because there was no significant difference found in the
resulting allometric relationships for either species (see Results), emaciated individuals
were included in the total dataset. A subset of these individuals, sub-adults and adults
only (n = 84 for T. truncatus and n = 17 for Kogia spp.), were also analyzed separately
and compared to a known allometric equation for adult terrestrial mammals (Table 2).
Using similar methods, total lung mass and total body mass were recorded for a variety of
other cetacean species (Appendix B). This dataset was supplemented with lung masses
and total body masses from previously published reports (Table 1).
16
Table 2. Lung variables compared to total body mass (kg) in terrestrial and marine mammals. y = axb ± 95% C.I., where x = total
body mass (kg), y = organ variable, a = y-intercept, and b = slope. (NR = not reported)
Measurement
n
a
b ± 95% C.I.
Animal
Category
Citation
Actual
Measurement
Brody 1945, Stahl 1965, Stahl 1967,
Lasiewski and Calder 1971, reviewed
in Calder 1984, reviewed in Peters
1993
mass
Lung Mass (kg)
> 100
0.0113
0.986 ± 0.012
adult terrestrial
mammals
Lung Volume
(mL)
333
53.5
1.06 ± 0.02
terrestrial
mammals
Stahl 1967, reviewed in SchmidtNielsen 1984
total lung
capacity
Lung Volume
(L)
17
0.135
0.92
marine
mammals
Kooyman 1973; reviewed in
Kooyman and Sinnett 1979
total lung
capacity
Tenney and Remmers 1963, reviewed
in Schmidt-Nielsen 1984, reviewed in
Peters 1993
inflated lung
tissue volume
Lung Volume
(mL)
26
56.7
1.02
mammals
(shrew to incld.
whale and
porpoise)
Lung Volume
(mL)
27
66.1
0.986 ± 0.017
wild mammals
Gehr et al. 1981; reviewed in Peters
1993
inflated lung
tissue volume
Lung Volume
(mL)
NR
41.92
1.041
mammals
Maina and Settle 1982, reviewed in
Schmidt-Nielsen 1984
NR
Heart Mass (kg)
568
0.006
0.98
mammals
Stahl 1967, reviewed in Calder 1984
mass
Liver Mass (kg)
175
0.033
0.87
mammals
Brody 1945, reviewed in Calder 1984
mass
17
To compare T. truncatus and Kogia spp., relative lung size was investigated in a
number of ways. The allometric relationship between lung mass and total body mass was
computed for (1) all specimens (i.e. the total data set) and (2) a subset of adult and subadult animals, which could be compared with a known allometric relationship for adult
terrestrial mammals (y = 0.0113x0.986; Brody 1945, Stahl 1967, Lasiewski and Calder
1971, reviewed in Calder 1984 and Peters 1993). Total lung masses and body masses
were log-transformed and plotted for each species. An allometric equation was generated
for T. truncatus and Kogia spp. [y = axb, where a = y – intercept, b = slope, x = total body
mass (kg), and y = total lung mass (kg)]. The slopes and y-intercepts of the species lines
were compared using an ANCOVA multiple regression analysis with a pre-determined α
(alpha) set at 0.05. To compare relative lung size across a broader phylogenetic sample of
cetaceans, these analyses were repeated for the entire comparative data set (see Appendix
B). Allometric equations were generated for each family of cetaceans. All statistical
analyses for this study were made using SAS (SAS Institute, Inc., Cary, NC, USA) and
SigmaPlot 11.0 (Systat Software, Inc., San Jose, CA, USA) statistical software.
The percentage of total body mass invested in lung tissue was also investigated
using the total data set for T. truncatus and kogiids. For this analysis, the ratio of lung
mass (kg) to total body mass (kg) was plotted against total body length (cm). The slopes
and y-intercepts of these linear relationships were compared using similar statistical
methods as described above.
18
Measures of Lung Size: Volume
During necropsy, on a subset of individuals (n = 5 for T. truncatus and n = 4 for
Kogia spp.) the intact respiratory tree was dissected free of the carcass at the level of the
trachea, wrapped in plastic to prevent desiccation, and frozen (Appendix A). Before
inflation experiments, lungs were removed from the freezer and thawed to room
temperature. Volumes of both un-inflated and inflated lungs were measured using the
water displacement method (Figure 3). Lungs were inflated using a custom built system.
Each lung was attached to an inflation and pressure monitoring system via rubber tubing
and all connections were wrapped to ensure complete sealing. Each lung was then
submerged and secured loosely below the water’s surface with nylon netting. The initial
un-inflated lung volume was measured and the lung was subsequently inflated using a 1L
super syringe (Hamilton Company, Reno, NV, USA) (Figure 3).
Pressure changes within the lung were measured and recorded using a pressure
vacuum module (PV350, FLUKE®, WA, USA) connected to a multimeter (87 III True
RMS Multimeter, FLUKE®, WA, USA), which was connected in-line with the inflation
system. Air was added in increments of 100mL and an equilibration period of 30sec was
allowed between incremental additions (Denison et al. 1971, Bergey 1986, Bergey and
Baier 1987). The corresponding pressure (psi) at each additional air increment was
recorded. At every 500mL air increment, the total lung volume (mL) was re-measured by
the water displacement method.
While the un-inflated lung volume could be unambiguously defined, a definition
of maximum lung volume had to be developed. Comparative studies on a variety of
terrestrial and marine mammals have defined “inflated” lung volume at + 30cm H2O
19
P
S
Air Outlet
Ruler
V
Figure 3. Schematic of the custom-built apparatus used to inflate excised lungs
[container used was a 50 or 100 gallon Rubbermaid® water trough (Newell Rubbermaid
Inc., Atlanta, GA, USA)]. Each lung was attached to the inflating (S) and pressure
monitoring (P) system via rubber tubing. The lung was then submerged underwater and
loosely secured with nylon netting. The water height was recorded on a metric ruler. The
lung was inflated using a 1L super syringe (S) in 100mL increments of air. The uninflated and inflated lung volumes were recorded using the water displacement method.
Changes in lung volume were measured by removing known volumes of water (via valve,
V), until water height returned to original height on ruler.
20
(0.42psi) of pressure (Denison et al. 1971, Dennison and Kooyman 1973, Weibel 1973,
Kooyman and Sinnett 1979, Bergey 1986, Bergey and Baier 1987). The lungs of T.
truncatus reached this pressure during inflation experiments, but the kogiid lungs did not.
Alternatively, the point at which the volume-pressure curve plateaus has been defined as
the static compliance point of the lung (Denison et al. 1971, Dennison and Kooyman
1973, Kooyman and Sinnett 1979, Bergey 1986, Bergey and Baier 1987). The pressure at
which this point was reached differed between T. truncatus (0.40 - 0.45psi) and kogiids
(0.20 – 0.30psi). Thus, the inflated static compliant volumes reported here are those at
which these species-specific pressures were reached. However, the lungs of both species
reached their static compliance at minimal inflation volumes (usually less that 1.0L),
which did not appear to accurately represent total lung capacity (TLC, maximum amount
of air that the lungs can contain).
Scholander (1940) warned that inflating excised, cannulated lungs could also
result in over-inflated lung volumes. The experimental approach utilized here confirmed
this concern. Kogiid lungs, for example, could be inflated to six times their un-inflated
volume without an appreciable increase in pressure. Visual inspection of the resulting
lung, though, revealed air emboli, suggesting that tissue damage had occurred.
Because neither the volume at a standard inflation pressure nor the static
compliance inflation volume were useful in estimating TLC, and over-inflation of lungs
was of concern, an approach described by Kooyman and Sinnett (1979) in their study of
Phocoena phocoena lungs was used. They recognized that each un-inflated lung
represented a unique start point, because each contained a variable initial volume of
trapped air, termed the minimum air volume (MAV; the amount of air within the lung
21
before the first artificial inflation). To estimate MAV, Kooyman and Sinnett (1979) first
weighed each un-inflated lung, and assuming a tissue density of 1kg/L, calculated lung
tissue volume. These authors then compared this lung tissue volume to that of the whole
un-inflated lung volume, determined via the water displacement method. The difference
in these values represented MAV. In P. phocoena MAV represented 0-17% of the final
TLC measured. A conservative estimate of TLC was thus calculated for each T. truncatus
and kogiid lung by dividing MAV by 0.17. These methods assume that the lungs of both
species are mechanically similar to those of P. phocoena. This assumption likely
introduces error as the pressure-volume curves suggest that kogiid and T. truncatus lungs
reach different maximum pressures (Figure 4).
All lung volumes (L) – un-inflated lung volume, inflated static compliant volume,
MAV, and TLC – for each specimen were reported and each was normalized relative to
total body mass (kg).
Measures of Lung Volume: Whole Body Cross-Sections
To further investigate lung volume, relative to total thoracic cavity volume and
post-cranial body volume, whole body cross-sections were utilized. For T. truncatus,
archived scaled images of cross-sections (approximately 3-5cm thick) through a frozen,
small bottlenose dolphin (“no number”, female, 170.9cm) were used (Pabst 1990). A
small Kogia sima carcass (VAQS 20081002, male, 160.0cm) was frozen and then serially
cross-sectioned whole using a commercial grade Hobart© meat saw (Model #5801;
Hobart Corporation, Troy, Ohio, USA) into approximately 2-3cm thick sections at the
Marine Mammal Pathology Laboratory in St. Petersburg, Florida. Scaled, digital images
22
A
0.6
Lung Pressure (psi)
0.5
0.4
0.3
0.2
0.1
T. truncatus
Kogia spp.
0.0
0
500
1000
1500
2000
2500
Air Volume (mL)
B
0.6
Mean Lung Pressure (psi)
0.5
0.4
0.3
0.2
0.1
T. truncatus
Kogia spp.
0.0
0
200
400
600
800
1000
1200
Air Volume (mL)
Figure 4. Lung volume-pressure relationships for species used in this study. (A) Example
of individual records for T. truncatus, WAM 633 and K. breviceps, VAQS 20071081. (B)
The mean (± S.D.) pressure (psi) of all the specimens used in this part of the study.
23
(TIF format, D100 Nikon camera) were taken of each section on a photo stand. All
images were analyzed using Adobe Photoshop CS3 Extended© (Adobe Systems
Incorporated, San Jose, CA, USA) and Image ProPlus Software (Media Cybernetics,
Baltimore, MD, USA).
The entire musculoskeletal thorax is divided into the thoracic cavity (cavum
thoracis) and intrathoracic abdominal cavity (Nickel et al. 1986, Schaller 1992, Nomina
Anatomica Veterinaria 1994). The thoracic cavity, whose caudal border is defined by the
diaphragm, contains the coelomic pleural (cavum pleurae) and pericardial (cavum
pericardii) cavities (Nickel et al. 1986, Schaller 1992, Nomina Anatomica Veterinaria
1994). The lungs are contained within the pleural cavity, while the heart is located with
the pericardial cavity. The cupula pleurae are the blind cranial ends of the pleural cavity
located at the thoracic inlet (Schaller 1992, Nomina Anatomica Veterinaria 1994). The
intrathoracic abdominal cavity, whose cranial border is defined by the diaphragm,
contains the abdominal organs (i.e. liver) (Nickel et al. 1986, Schaller 1992, Nomina
Anatomica Veterinaria 1994). Thus, both the thoracic and the intrathoracic abdominal
cavities are bounded by the musculoskeletal thorax.
For each species, in situ measurements of the cross-sectional areas of thoracic
viscera, including the lung (with and without surrounding air space), heart, thoracic
arterial rete, and intra-thoracic abdominal viscera, including the liver, were measured for
each cross-section through the thorax. Although this study could not address dynamic
changes in vascular tissues, it could assess the differences in static vascular tissue
volumes. In addition, the entire musculoskeletal thorax, and pleural and intra-thoracic
abdominal cavities were similarly measured. Using Adobe Photoshop CS3 Extended©
24
and Image ProPlus the desired structure to be measured was outlined and its crosssectional area calculated using a calibration value determined from the fixed scale bar
within the image.
For each section, the reported cross-sectional area (cm2) for each structure was the
mean of three repeated measures. To assess measurement error for each structure across
the cross-sections, its mean cross-sectional area and mean standard deviation were
calculated. The percent error for each structure was defined as the mean standard
deviation/mean cross-sectional area*100. The percent error ranged from 0.13% for the
intra-thoracic abdominal cavity, the largest space within the thorax, to 3.5% for the
thoracic arterial rete, the smallest structure measured within the thorax. For each section,
the volume of each visceral organ and cavity measured was then calculated by
multiplying its cross-sectional area (cm2) by the thickness of that cross-section (cm).
These volumes (cm3) were then summed across all cross-sections to get a total organ or
cavity volume.
Volume of the entire musculoskeletal thorax was reported relative to the
specimen’s post-cranial body volume (L). The total post-cranial body volume was
estimated by modeling it as a cylinder (from nuchal crest to anus) in series with a
truncated cone (from the anus to fluke insertion) (Dunkin et al. 2005). Measurements
required for this model, including appropriate lengths and girths were garnered from
standard morphometrics datasheets completed during necropsy (see McLellan et al. 2002;
Table 3). This model of the post-cranial body excludes the area of the head cranial to the
eye and thus is an underestimate of total body volume. Because the volume of the
musculoskeletal thorax en toto represented a similar percentage of total post-cranial body
25
Table 3. Measurements used to calculate total body volume (Vb).
Total
Body
Mass
(kg)
Vb
(L)
Length
(eye to
anus) (cm)
Length
(anus to
fluke
insertion)
(cm)
Average
Girth (eye
to anus, n =
7) (cm)
Anus
Girth
(cm)
Fluke
Insertion
Girth
(cm)
Field ID
Species
Total
Length
(cm)
VAQS 20081002 a
K. sima
160.0
77.0
64.9
87.8
34.6
90.3
74.0
28.4
WAM 637 b
K. sima
198.0
134.0
122.7
124.0
36.5
106.0
82.0
41.0
VAQS 20081003 b
K. sima
218.4
161.5
142.9
122.4
51.4
113.0
94.2
35.2
CLP001 b
K. breviceps
224.0
158.0
150.3
128.5
46.0
115.4
83.5
35.0
WAM 634 b
K. breviceps
237.0
219.0
208.4
149.0
42.0
127.5
88.5
45.5
VAQS 20071081 b
K. breviceps
275.0
234.5
205.0
150.0
56.5
123.9
92.5
45.5
"No ID" a
T. truncatus
170.9
62.5
58.2
95.4
47.6
82.0
58.0
24.4*
BRF 090 b
T. truncatus
182.0
79.0
74.7
99.0
41.0
92.9
61.5
25.5
WAM 633 b
T. truncatus
244.0
180.0
155.2
141.5
52.0
112.2
75.0
34.0
PBN 003 b
T. truncatus
246.0
173.0
159.8
145.0
55.5
113.3
72.5
30.0
* measurement not reported on morphometric datasheet; predicted from linear equation of girth at fluke insertion (cm; y-variable)
and total length (cm; x-variable): y = 0.109 x + 5.747, r2 = 0.804
a
specimen used in Measures of Lung Size: Whole Body Cross-Sections
b
specimen used in Mobility of Isolated Thoraxes
26
volume in both species (see Results), volume measurements for each organ and cavity
were reported relative to the volume of the entire musculoskeletal thorax.
The cross-sectional images from both species were also used to examine the in
situ gross morphology of the organs, diaphragm trajectory, and thoracic shape. This
information was used to help choose the best geometric thoracic cavity volume model in
each species (see “Thoracic Manipulations” below).
Gross Morphology of Skeleton
The thoracic skeleton of the bottlenose dolphin has been well described (Rommel
1990, Cotten et al. 2008), but there exist only fragmented published reports on the kogiid
thoracic skeleton, which are usually focused on rib counts (Haast 1873, Benham 1902,
Allen 1941, Yamada 1953, Omura et al. 1984, Nagorsen 1985). Thus, on a subset of
individual kogiids (n = 5), gross thoracic dissections were conducted to investigate the
morphologies and articulations of skeletal elements, including cervical and thoracic
vertebrae, vertebral ribs, sternal ribs, and sternum. A single K. breviceps thorax (WAM
637) was osteologically prepared (manure and ammonia treatment) and the skeletal
elements re-articulated. The length and width of each cartilaginous sternal rib (these
elements do not survive osteological preparation) were measured before re-articulation.
Two other skeletons (K. breviceps, NMNH 504737 and K. sima, NMNH 504221),
curated at the Smithsonian Institution’s National Museum of Natural History, were also
investigated. Scaled, digital images were taken of the re-articulated and curated skeletons
(Nikon D100, TIFF image files). These images were imported into EasyCAD (Evolution
Computing, Phoenix, Arizona; e.g. Figure 2), scaled, and then used as references to draw
27
scaled illustrations of kogiid osteology (methods similar to Rommel 1990 and Cotten et
al. 2008). These drawings were later used to illustrate the skeletal postures resulting from
the thorax manipulations (see more detail of the thorax drawing under “Mobility of
Isolated Thoraxes”).
Mobility of Isolated Thoraxes
To test the hypothesis that the thorax of deep divers may undergo relatively larger
changes in shape, the mobility of the isolated thorax was investigated on a subset of
individual T. truncatus (n = 3), K. breviceps (n = 4), and K. sima (n = 1). Each isolated
thorax, defined here as consisting of articulated vertebral elements [all cervical (C), all
thoracic (T), and first 1-5 lumbar (L) vertebrae], vertebral ribs, sternal ribs, sternum, and
associated muscle (internal and external intercostals, transverse thoracic, hypaxialis
bisected at L3, and rectus abdominis bisected at sternum), was excised whole during
dissection. Isolated thoraxes were wrapped in plastic to prevent desiccation and frozen
for later mechanical tests. Before tests were conducted, each thorax was removed from
the freezer, and thawed to room temperature. The thorax was kept moist using
physiological saline throughout the physical manipulations.
The goal of the physical manipulations was to document and compare the ranges
of thoracic mobility between T. truncatus and kogiids. For each thorax, forces were
imposed, as described below, to create both a maximally expanded and maximally
collapsed posture (methods similar to those of Cotten et al. 2008). The differences in
metrics of thoracic size between these two extreme postures were used to represent the
range of thoracic mobility.
28
To create the maximally expanded posture, the isolated thorax was suspended
from a metal frame that consisted of a horizontal bar, connected via two uprights, to a
stable base (Figure 5). To secure the thoracic unit, cable ties were wrapped around the
vertebral column at four positions (between C5-6, T6-7, T12-13, and L4-5). Each of these
cable ties was then connected to the metal frame to secure the vertebral column in place.
Before applying a load, white string was placed along the caudal margin of each
vertebral and sternal rib. These strings provided high-contrast markers for the skeletal
elements as they changed positions during the physical manipulations. To manipulate the
thorax into a maximally expanded posture, hi-test nylon fishing line was tied to cranial
skeletal elements at the (1) first vertebral rib-sternal rib joint, (2) manubrium, and (3)
vertebral rib 1, at mid-shaft. These lines were then manually pulled cranially to expand
the thorax. A 5 or 10kg spring scale (Pesola®, Baar, Switzerland), attached in series to the
nylon fishing lines, was used to measure the applied load, so that equivalent forces were
applied across multiple manipulations within the same posture. The maximal cranially
expanded posture was defined at that load at which no further shape change was grossly
observed to occur.
To create the maximally collapsed posture, the thorax was secured in a supine
position (Figure 5). The neural spines were placed between two wooden blocks, which
supported the vertebral column and maintained a stable supine position. In this position,
the thorax naturally collapsed under its own weight, and this posture was defined as the
maximal caudally collapsed posture.
At these two postures, the shape and size of the isolated thorax and the changes in
position of the skeletal elements (vertebral ribs, sternal ribs, and sternum) were recorded.
29
A A
B
Dorsal
Dorsal
Dorsal
Dorsal
Figure 5. Each excised thorax was (A) suspended from a stable frame and manipulated
into the defined maximum cranially expanded posture. The lines attached to the cranial
portion of the thorax represent the lines used to apply the known load to cranially expand
the thorax. Arrows denote the direction of thorax movement during manipulations. (B)
The isolated thorax was secured in a supine position, and allowed to collapse under its
own weight into the defined maximum caudally collapsed position, as denoted by the
arrow. White strings were placed along the caudal margin of each vertebral and sternal
rib, which provided high contrast markers for the skeletal elements as they changed
positions during the physical manipulations. Methods were similar to those used by
Cotten et al. (2008).
30
Circumferences were measured with a flexible measuring tape; heights, depths, widths,
and lengths were measured with anthropometers (Haglof ®, Sweden) (see Appendix C
and Appendix D for detailed descriptions of measurements and datasheet). All reported
measurements were the means of three repeated measures for each measurement. All
values were reported as percent change from the cranially expanded to the caudally
collapsed posture. A parametric two-sample t test (pre-determined α = 0.05) was utilized
to test for differences among measurements between species.
Digital, scaled photographs were taken with a D100 Nikon camera in the dorsal,
ventral, lateral, and frontal views and at a position perpendicular to the joint faces. To
facilitate CAD rendering of the skeletal elements in each posture, the skeleton was
flensed of all muscles except the internal intercostals, which revealed the ribs, while
maintaining the integrity of the thorax (n = 1; VAQS 20081003 K. sima).
Lateral and frontal perspectives of anatomically correct, scaled skeletal figures
were drawn in the cranially expanded and caudally collapsed postures using EasyCAD
software and digital skeletal templates (see “Gross Morphology of Skeleton” above). The
skeletal template for T. truncatus consisted of a vertebral column and skull, and was
provided by Dr. Sentiel Rommel (modified from Rommel 1990; Cotten et al. 2008). For
the kogiid skeletons, digital images taken during the thoracic manipulations were
imported into EasyCAD, along with images of re-articulated and “re-aligned” skeletons
(NMNH 504221 K. sima and WAM 637 K. breviceps; see above). The skeletal template
for the Kogia spp. consists of a vertebral column, thorax and skull, and was the result of a
collaborative drawing effort with Dr. Sentiel Rommel. The re-articulated images were
used as a reference for kogiid anatomy, while the thoracic manipulation images and
31
measurements were used as references for the shape change and range of mobility of the
kogiid thorax.
Thoracic Cavity Volume Models
Measurements of thoracic shape (circumference, length, width, depth, and height)
taken during the manipulations of isolated thoraxes were used to estimate volume
changes between extreme postures. The external circumference and lateral width
measurements were adjusted, by subtracting the thickness of the thoracic wall, and used
to calculate internal thoracic cavity volumes (see model descriptions below). For each
specimen, thoracic cavity volume (L) in each posture and percent change of thoracic
cavity volume between postures were reported with respect to the specimen’s total body
mass (kg) or total post-cranial body volume (L) (Table 3). Thoracic cavity volume
calculated here refers only to the thoracic cavity proper (cavum thoracis) and does not
include the intrathoracic abdominal cavity. The thoracic cavity was further sub-divided in
this study into the (1) cranial thorax, defined as the space bounded by vertebral ribs that
attach directly to the sternum via a sternal rib (vertebral ribs 1-5), and (2) caudal thorax,
defined as that space caudal to rib 5 and bounded by the diaphragm. The shapes of the
cranial and caudal thoraxes differ dramatically and, thus, were modeled with a different
geometric shape (Figure 6).
To calculate thoracic volume, four models were investigated (Figure 7 and
Appendix E). Cranial thoracic volume was modeled using two alternative cross-sectional
shapes, a circle and a cardioid (heart-shape). These geometric shapes were chosen based
upon examination of photographs of cross-sections through the bottlenose dolphin thorax
32
A
B
L
L
L
L
L
L
L
H
H
LL
LL
D
D
Li
Li
S
S
C
Figure 6. Example of one of four geometric models of the thoracic cavity used to
calculate volumes at the extreme cranially expanded and caudally collapsed positions,
where r = radius of circle at the cross-section of rib 1, R = radius of a circle taken at the
cross-section of rib 5, l = length between ribs 1-5, L = length between rib 5 and L3, and θ
= angle of approach of the diaphragm to L3 (Sandifer and Moshos 1996; see Figure X for
explanation of all four models). (B) Cross-sectional photographs of the thoracic cavity of
a T. truncatus corresponding to positions within the cone model at ribs 1, 5, and 8.
(L=lung, H = heart, S = stomach, Li = liver, D = diaphragm) (Pabst 1990) (C) Position of
the diaphragm (thick black line) within the thoracic cavity of a T. truncatus (modified
from Rommel 1990).
33
B
A
C
D
Figure 7. Four geometric models of the thoracic cavity used to estimate cavity volume
changes between a maximally cranially expanded and a maximally caudally collapsed
posture. (A) Model 1 represents a frustum of a right circular cone in series with a
complete slanted cone. (B) Model 2 represents a circular cylinder in series with a
complete slanted cone. (C) Model 3 represents the frustum of a cardioid cone in series
with a complete slanted cone. (D) Model 4 representes a cardioid cylinder in series with a
complete slanted cone. In (A) r = radius of circle at the cross-section of rib 1; in (B) r =
average radius of circle from cross-section of ribs 1-5; in (C) r = the radius of a cardioid
at the cross-section of rib 1 (measured from the ventral aspect of the centrum of V1
laterally to the angle in the rib); in (D) r = average radius of a cardioid at the cross-section
of ribs 1-5 (measured from the ventral aspect of the vertebra centrum laterally to the
angle in the rib). In (A) and (B), R = radius of a circle taken at the cross-section of rib 5,
while in (C) and (D) R = radius of cardioid taken at the cross-section of rib 5. In all
models (A) – (D), l = length between ribs 1-5, L = length between rib 5 and L3, and θ =
angle of approach of the diaphragm to L3 (Sandifer and Moshos1996; see Appendix E for
cardioid proofs of area and volume).
34
and morphology of the diaphragm (Figure 6). Height and width measurements taken on
cross-sectional images of both species in EasyCAD demonstrate that the cranial thorax of
T. truncatus is circular in shape (thorax is as tall as it is wide), while the kogiid thorax is
cardioid in shape (thorax is twice as tall as it is wide). The cross-sectional images also
demonstrate that the thoracic cavity volume between ribs 1-5 increases gradually. Thus,
for each cross-sectional shape the cranial thorax was modeled as either a right cylinder or
a frustum of a right cone.
Cross-sectional images of both species also demonstrated that caudal to rib 5,
thoracic cavity volume decreased rapidly due to the presence of the diaphragm and
concomitant increasing volume of the abdominal cavity (Figure 6). The relaxed
diaphragm of T. truncatus runs virtually horizontally from its dorso-caudal origin at
lumbar vertebrae 2-3 to the level of thoracic vertebra 6 (Dearolf 2003). At thoracic
vertebra 6 the diaphragm changes its trajectory to become vertically oriented. The
diaphragm runs ventro-cranially and inserts on the distal ends of vertebral ribs 7-13, on
the vertebral rib-sternal rib joint of ribs 4-6, and onto the caudal most end of sternabra 3
(Figure 6). In kogiids, the trajectory of the diaphragm was not notably different from that
of T. truncatus, except for the insertion site; the central tendon of the diaphragm attaches
to hypophyses of lumbar vertebrae 2-5 (Appendix A). Thus, in all models, the caudal
thoracic volume (vertebral ribs 5 - lumbar 3 for T. truncatus and lumbar 5 for kogiids)
was modeled as a slanted right cone (Figure 6, Figure 7).
For both T. truncatus and kogiids, the left thoracic wall was removed during
dissection to obtain lateral images of the interior thorax and position of the diaphragm
muscle. Digital, scaled images were taken to note the position of the lungs, diaphragm,
35
and lateral shape of the thorax. These images were uploaded into EasyCAD and used as
references for the geometric models in both T. truncatus and Kogia spp. Each of the
geometric shapes used in the models simplify the true shape of the thoracic cavity, and,
thus, may yield over- or under-estimates of the volume.
The whole cross-sectioned specimens were used to estimate the error of each
thoracic cavity volume model. Images from each cross-sectioned specimen were
imported into EasyCAD and scaled. The appropriate lengths and radiuses were measured
and then used as inputs into each model to calculate thoracic cavity volume. For each
cross-sectioned specimen, the percent difference between the measured thoracic cavity
volume (L) (see “Lung Size: Whole Body Cross-Sections” above) and the modeled
thoracic cavity volume (L) was calculated. The model that most closely estimated the real
measured volume from the cross-sections was considered to be the best model for that
species. This model was then used to estimate the thoracic cavity volume changes that
occurred between the maximal cranially expanded and caudally collapsed postures for
each isolated thorax (n = 3 for T. truncatus and n = 5 for kogiids).
RESULTS
A primary objective of this study was to compare lung size of the shallow diving
coastal T. truncatus with that of the deeper diving kogiids. Lung size was measured using
three different methods. For a large number of individuals, lung mass was recorded, for a
smaller subset of individuals excised lung volume was recorded, and for one individual
each of T. truncatus and K. sima lung volume, derived from whole body cross-sections,
was computed.
36
Lung Mass
The slopes of the lines that describe the allometric relationship between lung mass
and total body mass for T. truncatus and Kogia spp. across all age classes and body
conditions (total data set) were not significantly different from each other and neither was
distinguishable from 1 (Table 4, Figure 8). However, their y-intercepts did differ
significantly (F = 224.15, P < 0.0001, d.f. = 128). Thus, although their lungs grow at a
similar rate, for any given body mass the kogiid lung mass is approximately one-half that
of a T. truncatus. Removing emaciated specimens from the data set did not change these
relationships. The slopes were similar and neither was distinguishable from 1, and the yintercepts were significantly different between species (F = 144.06, P < 0.0001, d.f. =
101; Table 4). Because the inclusion of the emaciated animals did not appear to bias the
relationship between lung mass and total body mass, the total data set was utilized to
investigate how the lung’s contribution to total body mass varied across animals of
different body lengths (Figure 9). The slopes of the lines that describe the relationship
between the lung mass: total body mass ratio and total length for T. truncatus and kogiids
were similar and neither was distinguishable from zero. However, the y-intercepts did
differ significantly between species (T. truncatus = 0.0299, Kogia spp. = 0.0133; F=
117.01, P < 0.0001, d.f. = 128). Thus, across all body lengths kogiid lungs contribute
approximately one-half as much to total body mass as do those of T. truncatus (Figure 9).
A subset of data for each species that included only sub-adults and adults was
used to compare relative lung size of T. truncatus and kogiids to that predicted for adult
terrestrial mammals (y = 0.0113x0.986 ± 0.012, n > 100, r2 = 0.922, b ± 0.012; Brody 1945,
Stahl 1967, Lasiewski and Calder 1971, reviewed in Calder 1984 and Peters 1993). For
37
Table 4. Summary of allometric relationships between organ mass and total body mass. y
= axb, where y = organ mass (kg) and x = total body mass (kg). (n = sample size, a = yintercept, b = slope, C.I. = confidence interval, D-P = Delphinidae-Phocoenidae, and KZ-P = Kogiidae-Ziphiidae-Physeteridae)
n
a
b
95% C.I.
Lung Mass:
Total Data Set
T. truncatus
Kogia spp.
111
18
0.032
0.014
0.973
0.932 - 1.014
Non-emaciated
T. truncatus
Kogia spp.
90
12
0.032
0.014
0.975
0.927 - 1.022
Sub-adults and Adults
T. truncatus
Kogia spp.
84
17
0.028
0.012
1.004
0.921 - 1.087
Family Level Comparisons
256
Delphinidae
19
Kogiidae
0.034
0.017
0.944
0.905 - 0.984
Delphinidae
Phocoenidae
256
15
0.033
0.016
0.949
1.177
0.425 - 1.474
0.916 - 1.438
Kogiidae
Ziphiidae
Physeteridae
19
8
10
0.031
0.041
0.047
0.826
0.732 - 0.919
D-P
K-Z-P
271
37
0.033
0.022
0.951
0.900
0.852 - 1.049
0.858 - 0.941
Heart Mass:
T. truncatus
Kogia spp.
38
19
0.013
0.010
0.857
0.794 – 0.919
Liver Mass:
T. truncatus
Kogia spp.
104
17
0.012
0.002
1.054
1.235
1.004 – 1.104
1.030 – 1.440
38
Log Lung Mass (kg)
Log Total Body Mass (kg)
Figure 8. Log lung mass (kg) vs. log total body mass (kg) for all age classes and body conditions of T. truncatus and Kogia spp. The
slopes of these lines are similar, however, the y-intercepts differ significantly (see Table 4).
39
Lung Mass / Total Body Mass (kg/kg)
Total Body Length (cm)
Figure 9. Ratio of lung mass (kg) vs. total body mass (kg) against total body length (cm) across all age classes and body conditions of
T. truncatus and Kogia spp. The slopes of these lines are similar, however, the y-intercepts differ significantly.
40
this subset of individuals, the slopes of the lines for T. truncatus and Kogia spp. were
similar and neither was distinguishable from 1 (Table 4). As was observed for the total
data set, though, the y-intercepts did differ significantly (F = 213.59, P < 0.0001, d.f. =
100). The allometric equation for kogiids was similar to that of terrestrial mammals, and
both predicted lung masses that were approximately half that of a similarly-sized T.
truncatus (Figure 10).
To broaden the phylogenetic scope of these comparisons, allometric relationships
between lung mass and total body mass were generated for a variety of odontocete
families. Representatives of the Family Delphinidae (n = 256, Table 1, Appendix A,
Appendix B) were first compared to the Family Kogiidae, which included the sample
from this study and one more individual from a previously published report (n = 19). The
slopes of the lines for the Family Delphinidae and Kogiidae were similar and both were
slightly less than 1 (Table 4). The y-intercepts were significantly different between
families (F = 115.56, P < 0.0001, d.f. = 274; Figure 11). Thus, members of the Family
Kogiidae possess lungs that are approximately half the mass of those of a similarly-sized
delphinid.
To further broaden the comparative phylogenetic scope, representatives of the
Families Phocoenidae, Ziphiidae, and Physeteridae (Table 1, Appendix B) were also
included. For the families Phocoenidae and Delphinidae, the slopes were not significantly
different from each other (P = 0.0905) and neither was distinguishable from 1. Given the
relatively low P-value, though, the ANCOVA analysis included the slope interaction
effect and, thus, both slope values were reported in Table 4. The y-intercepts were also
not significantly different (F = 2.32, P = 0.1291, d.f. = 270; Table 4). Because neither
41
1.2
1.1
1.0
T. truncatus
Kogia spp.
Terrestrial Mammals
0.9
0.8
0.7
Log Lung Mass (kg)
0.6
0.5
0.4
0.3
0.2
0.1
0.0
-0.1
-0.2
-0.3
-0.4
1.6
1.7
1.8
1.9
2.0
2.1
2.2
2.3
2.4
2.5
2.6
2.7
Log Total Body Mass (kg)
Figure 10. Log lung mass (kg) vs. log total body mass (kg) for sub-adults and adults of T. truncatus and Kogia spp. compared to adult
terrestrial mammals (y = 0.0113x0.986, b ± 0.012; Brody 1945). The slopes of the lines for T. truncatus and kogiids are not significantly
different, however, the y-intercepts differed significantly.
42
Log Lung Mass (kg)
Log Total Body Mass (kg)
Figure 11. Log lung mass (kg) vs. log total body mass (kg) for Families Delphinidae and Kogiidae. The slopes of these lines were
similar, however, the y-intercepts differed significantly.
43
slope nor y-intercept were significantly different between families, the data were pooled
together to form the group Delphinidae-Phocoenidae (D-P). A similar comparison was
under taken for the Families Kogiidae, Ziphiidae, and Physeteridae. The slopes of the
lines for these three families were similar, and just under 1. The y-intercepts were also
similar (F = 2.92, P = 0.0678, d.f. = 36; Table 4). Thus, data from the three families were
pooled together to form the group Kogiidae-Ziphiidae-Physeteridae (K-Z-P).
The slopes of the lines that describe the relationship between lung mass and total
body mass for the D-P and K-Z-P groups were not significantly different from each other
(P = 0.0817) (Table 4). Given the relatively low P-value, though, the ANCOVA analysis
included the slope interaction effect and, thus, both slope values were reported in Table 4.
The y-intercepts, though, did differ significantly between these two groups (F = 5.05, P =
0.0253, d.f. = 308; Figure 12). Thus, species within the K-P-Z group possess lungs that
are approximately half the mass of those of similarly-sized species within the D-P group.
Excised Lung Volume
The volume of excised lungs in both an un-inflated (n = 5 for T. truncatus and n =
4 for Kogia spp.) and inflated (n = 4 for T. truncatus and n = 3 for Kogia spp.) condition
were measured by the water displacement method. The total lung capacity (TLC) and
minimum air volume (MAV) were calculated using a method modified from Kooyman
and Sinnett (1979) (Table 5, Table 6).
Overall, lung volumes of kogiids were small relative to those of T. truncatus.
When lung volumes were standardized to total body mass (TBM), the un-inflated lung
volume, MAV, and TLC of T. truncatus were approximately five times larger than those
44
Table 5. Lung volume measurements for kogiids and T. truncatus. The un-inflated, and inflated lung with 1.0L of air, lung volumes
were measured during the inflation experiments. The minimum air volume (MAV) and total lung capacity (TLC) were calculated
using methods of Kooyman and Sinnett (1979). MAV was conservatively assumed to be 17% of TLC* (which ranged from 0-17% in
Phocoena phocoena; Kooyman and Sinnett 1979). MAV and TLC for VAQS 20071081 could not be calculated because MAV was
less than zero. (TBM = total body mass)
Field ID
Species
TBM (kg)
Lung
Mass (kg)
Lung Volume
Un-inflated (L)
Lung Vol.
Inflated with
1.0L Air (L)
MAV (L)
TLC (L)*
WAM 637
K. sima
134.0
1.515
2.63
4.94
1.11
6.55
VAQS 20071081
K. breviceps
234.5
2.987
2.67
4.31
0.00
----
MLC 003
K. breviceps
386.2
3.621
4.16
NE
0.54
3.17
WAM 644
K. breviceps
392.0
3.654
5.01
6.98
1.35
7.95
WAM 647
T. truncatus
153.0
5.064
7.61
9.34
2.54
14.95
PBN 003
T. truncatus
173.0
6.065
7.98
10.10
1.91
11.25
WAM 633
T. truncatus
180.0
6.970
11.20
13.01
4.23
24.88
BCB 004
T. truncatus
NE
3.951
5.96
3.92
2.00
11.79
RJM 003
T. truncatus
NE
1.904
3.87
NE
1.96
11.54
45
Table 6. Mean lung air volume (± S.E.) measures for T. truncatus and Kogia spp. compared to P. phocoena (n = 4) (*data from
Kooyman and Sinnett 1979). (TBM = total body mass, MAV = minimum air volume, TLC = total lung capacity)
Species
TBM (kg)
Lung
Volume
Uninflated
(L)
Kogia spp.
286.7 ± 62.6
3.62 ± 0.58
0.01 ± 0.002
1.002 ± 0.241
0.003 ± 0.002
5.892 ± 1.420
0.021 ± 0.012
T. truncatus
168.7 ± 8.1
8.93 ± 1.14
0.05 ± 0.005
2.894 ± 0.692
0.017 ± 0.004
17.025 ± 4.069
0.101 ± 0.021
P. phocoena*
35.0 ± 3.4
---
---
0.383 ± 0.104
0.011 ± 0.003
3.325 ± 0.250
0.095 ± 0.012
Uninflated /
TBM
(L/kg)
MAV (L)
MAV / TBM
(L/kg)
TLC (L)
TLC / TBM
(L/kg)
46
Log Lung Mass (kg)
Log Total Body Mass (kg)
Figure 12. Log lung mass (kg) vs. log total body mass (kg) for species pooled in Families Delphinidae and Phocoenidae (D-P) and
Kogiidae, Physeteridae, Ziphiidae (K-P-Z). The slopes of these lines were similar, however, the y-intercepts differed significantly. The
line for terrestrial mammals was generated using the equation from Brody (1945) (y = 0.0113x0.986, b ± 0.012).
47
volume measures of kogiids (Table 6). The MAV and TLC of T. truncatus were more
similar to, though larger than, those of P. phocoena (reported in Kooyman and Sinnett
1979; Figure 13). The TLC volumes calculated for T. truncatus and Kogia spp. were
compared to those that would be predicted based upon existing allometric relationships
for marine mammals (Kooyman 1973, Kooyman and Sinnett 1979) and terrestrial
mammals (Tenney and Remmers 1963, Stahl 1967) (Table 7). Calculated TLC values for
T. truncatus were similar to those predicted by existing allometric relationships, while all
calculated TLC values for the kogiids were smaller by a factor of at least 20-50%.
In situ Lung Volume Calculated from Whole Body Cross-Sections
The volume of the in situ lung was computed from whole body cross-sections of a
single T. truncatus and K. sima (Table 8). This volume and those of other structures
within the entire musculoskeletal thorax are also reported as a percent of the entire
thoracic volume. The entire thorax comprised 14% of the total post-cranial body volume
in T. truncatus (7.9L absolute) and 15% of the total post-cranial body volume in K. sima
(9.6L absolute).
Both the lungs and pleural cavity of the K. sima were each half the volume of
those structures in the T. truncatus (Table 8). The cross-sections also revealed that the
lungs of K. sima were positioned strictly dorsally throughout the entire thoracic cavity,
while in T. truncatus the lungs extended ventro-laterally and encompassed the heart
(Figure 14, Figure 15). The dorsal position of the lungs had been previously noted in a
fetal K. breviceps (Kernan and Schulte 1918). The tissue along the ventro-lateral margins
48
Table 7. A comparison of estimated total lung capacity (TLC), based upon measurements from this study, and those predicted from a
variety of existing allometric relationships based upon total body mass (TBM). Marine mammal regression line: VL (L) = 0.135 X (kg)
0.92
(Kooyman 1973, Kooyman and Sinnett 1979), terrestrial mammal regression lines: VL (mL) = 56.7 X(kg)1.02 (Tenney and Remmers
1963) and VL (mL) = 53.5 X(kg)1.06 (Stahl 1967).
Marine Mammal
TLC (L)
Tenney and Remmers
Terrestrial TLC (L)
Field ID
Species
TBM (kg)
Calculated
TLC (L)
WAM 637
K. sima
134.0
6.55
12.2
8.4
9.6
MLC 003
K. breviceps
386.2
3.17
32.4
24.7
29.5
WAM 644
K. breviceps
392.0
7.95
32.8
25.0
30.0
WAM 647
T. truncatus
153.0
14.95
13.8
9.6
11.1
PBN 003
T. truncatus
173.0
11.25
15.5
10.9
12.6
WAM 633
T. truncatus
180.0
24.88
16.0
11.3
13.2
49
Stahl Terrestrial
TLC (L)
Table 8. Absolute (L) and relative (%) volumes of organs, vascular tissues and specific cavities within the entire musculoskeletal
thorax calculated from whole body cross-sections of a single K. sima and T. truncatus.
K. sima
9.58
T. truncatus
7.94
% of Thoracic
Region
K. sima
100.0
pleural cavity
2.14
4.27
22.3
53.8
lungs
1.43
2.91
15.0
36.7
thoracic arterial rete
0.86
0.39
8.9
4.9
heart
0.85
0.81
8.9
10.2
intra-thoracic abdominal cavity
5.81
2.01
60.6
25.4
liver
2.38
0.69
24.9
8.7
Structure
Volume (L)
Entire musculoskeletal thorax
50
T. truncatus
100.0
Figure 13. Log of calculated total lung capacity (TLC, in liters) vs. log of total body mass (kg) for T. truncatus and Kogia spp. A
terrestrial (Tenney and Remmers 1963, Stahl 1967) and marine mammal line (Kooyman 1973) has been added for references.
Published values for Phocoena phocoena are from Kooyman and Sinnett (1979). 51
A
B
R
R
L
L
R
R
L
L
H
H
Figure 14. Whole body cross-sections at the level of the heart in a (A) T. truncatus and (B) K. sima. L = lung, H = heart, R = thoracic
arterial rete. The lateral extensions of the thoracic arterial rete is K. sima is denoted by the white outline. (black scale bar = 5cm)
52
A
B
Figure 15. In (A) T. truncatus the lungs overlap the heart ventro-laterally. In (B) Kogia
spp. the lungs are located strictly dorsal to the heart. The blue thick link traversing from
the sternum to the caudal thoracic and lumbar vertebrae represents the dome of the
diaphragm. (Image of T. truncatus from Rommel)
53
of the lungs in this young T. truncatus had not yet fully matured to its inflated condition,
which is a typical characteristic for a juvenile of this species (pers. obs.).
In K. sima, the thoracic arterial rete was also more extensively distributed
throughout the pleural cavity than it was in T. truncatus. In K. sima this rete extends
ventrally, draping over the thoracic inlet, and caudo-laterally along the thoracic wall to
the level of vertebral ribs 3-4. Cranially, this rete completely surrounds both lungs
(Figure 16). The thoracic arterial rete of K. sima was twice the volume of that of T.
truncatus.
Heart volumes were similar between species. The intra-thoracic abdominal cavity
and liver volumes were 2-3 times larger in K. sima than in T. truncatus.
Mobility of Isolated Thoraxes
Results from the manipulations of isolated thoraxes (depicted in lateral and frontal
perspectives in Figure 17) do not support the hypothesis that the thorax of a deeper diving
kogiid is more mobile than that of a shallow diving T. truncatus. There were no
significant differences between the kogiids and T. truncatus in the change in thoracic
height, width, and circumference (measured between ribs 1-5), or inlet height measured
between the maximally expanded and collapsed postures (Table 9, Figure 17, Figure 2).
Note, though, that there was large inter-individual variability in these measurements.
Only the change in inlet width measured between the two postures differed significantly
across species (t = 4.74, d.f. = 5, P = 0.005; Table 9); T. truncatus underwent a larger
change than Kogia spp.
54
Table 9. The mean (± S.D.) percent difference between the maximal cranially expanded
to caudally collapsed postures (averaged across ribs 1-5) for thoracic dimensions
measured for each species (* denotes significant differeces).
Measurement
T. truncatus
Kogia spp.
Avg. Height (%)
25.8 ± 2.9
25.9 ± 8.1
Inlet Height (%)
32.8 ± 4.1
37.2 ± 12.2
Avg. Width* (%)
9.5 ± 2.3
11.8 ± 6.3
Inlet Width (%)
17.8 ± 1.0
9.1 ± 3.0
Avg. Circum. (%)
21.3 ± 11.8
15.6 ± 6.6
Thoracic Vol. (%)
30.5 ± 25.9
20.6 ± 12.5
55
A
B
L
L
L
L
Figure 16. Whole body cross-sections at the level of the inlet to the thorax in a (A) T. truncatus and (B) K. sima. In K. sima the
thoracic arterial rete completely encompasses both left and right lungs. No homologous vascular tissue is observed in T. truncatus. L =
lung, white outline = lung, white arrows = thoracic arterial rete (black scale bar = 5cm)
56
A
C
B
D
Figure 17. The range of thoracic mobility in Kogia spp. The body outline in each of the
lateral views (C-D) is fixed between positions. (A) and (C) depict the cranially most
expanded thoracic posture, while (B) and (D) depict the caudally most collapsed
thoracic posture. Note the lack of a first sternal rib (compare to T. truncatus in Figure
2).
57
The significant difference in the thoracic inlet width measurement is interpretable
given the morphological differences between T. truncatus and Kogia spp. at the first rib.
In T. truncatus, vertebral rib 1 articulates with a relatively long bony sternal rib (74% of
vertebral rib length). These ribs articulate at a highly mobile joint, which flares laterally
as the thorax is manipulated from a caudally collapsed to a cranially expanded position
(Figure 2; Cotten et al. 2008). In contrast, in kogiids, vertebral rib 1 forms an immobile
articulation with a short (11% of vertebral rib length) sternal cartilage. Thus, kogiids lack
a mobile joint between the first vertebral and sternal ribs, which appears to limit lateral
flaring at the inlet in the cranially expanded posture (Figure 17A). In kogiids, sternal ribs
2-5 are also cartilaginous, but unlike sternal rib 1, they form highly mobile joints with
their respective vertebral ribs. Thus, except for sternal rib 1, the cartilaginous sternal ribs
of kogiids form mobile joints with their respective vertebral ribs, in a manner similar to
that of T. truncatus, and unlike that of terrestrial mammals. Kogiids also lack a costal
arch, which is typical in terrestrial mammals.
Thoracic Volume Models
Changes in the volume of the cranial thorax, between the cranially expanded and
caudally collapsed postures, were estimated using geometric models. Each model was
tested for its ability to estimate thoracic volume from known computed values derived
from the whole body cross-sections. Of the four geometric models investigated, Model 1
(frustum of right circular cone in series with a slanted complete cone) appeared to best
estimate the thoracic cavity volume of the cross-sectioned specimens (Table 10). This
model, though, provides only gross estimates of thoracic cavity volume with errors up to
58
Table 10. Cranial thoracic cavity volume (L) calculated from whole body cross-sections
and calculated via four geometric models.
"No ID" Tt
Volume (L)
Measured
VAQS 20081002Ks
%
difference
5.92
Volume (L)
%
difference
3.78
Models
1
6.87
14
4.26
11
2
7.29
19
4.60
18
3
13.19
55
4.54
17
4
13.89
57
4.65
19
59
13.8 and 11.3% for T. truncatus and K. sima, respectively (Table 10). Estimates of kogiid
thoracic volume were relatively insensitive to the geometric shape chosen. In contrast, the
cardioid models poorly predicted the volume of the T. truncatus thorax.
Model 1 was applied to each specimen to estimate changes in thoracic cavity
volume that occurred during manipulation experiments (Table 11). On average, thoracic
cavity volumes decreased, from the maximally expanded to the maximally collapsed
posture, by 30.5% and 20.6% in T. truncatus and Kogia spp., respectively. These values
were not significantly different from each other (t = 0.683, d.f. = 5, P = 0.525).
Gross observations, individual measurements and thoracic cavity volume
estimates all demonstrate that there exists large intra-specific variability in thoracic
mobility. These data also suggest that the thorax of a deep diving kogiid is not more
mobile than that of a shallower diving T. truncatus. In kogiids, the permitted change in
lateral width of the thoracic inlet appears to be constrained, relative to T. truncatus, by
the morphology of the first vertebral-sternal rib pair.
DISCUSSION
This study tested the hypothesis that the deep diving kogiids would possess either
smaller lungs and/or a more flexible thorax than the shallow diving T. truncatus. The
kogiid lungs were one-half the mass, and between 20-50% of the volume of the lungs of a
similarly-sized T. truncatus. There was only one difference in thoracic mobility between
these two groups - the change in width of the kogiid thoracic inlet appears to be
constrained relative to T. truncatus. The kogiid thorax also contained a larger volume of
60
Table 11. Cranial thoracic cavity volumes (L), calculated using geometric Model 1, for
cranially most expanded and caudally most collapsed postures. The percent change
between postures and the mean for each species is also reported.
Field ID
Species
Cranial
(L)
Caudal (L)
%Δ
Mean
%Δ
WAM 633
T. truncatus
27.08
23.33
13.8
30.5
PBN 003
T. truncatus
29.11
24.04
17.4
BRF 090
T. truncatus
13.94
5.53
60.4
WAM 637
K. breviceps
14.66
11.06
24.6
WAM 634
K. breviceps
28.22
26.61
5.7
VAQS 20071081 K. breviceps
40.48
26.20
35.3
VAQS 20081003
25.09
20.88
16.8
K. sima
61
20.6
arterial retial tissue than the dolphin thorax. These observations are discussed within both
a phylogenetic and functional context below.
Interestingly, kogiid lung mass, relative to total body mass, is similar to that
predicted for terrestrial mammals. In a broader phylogenetic comparison, kogiids,
physeterids, and ziphiids all possess relative lung masses similar to those of terrestrial
mammals. When relative lung mass is mapped onto an existing phylogeny for cetaceans
(Messenger and McGuire 1998, Price et al. 2005), and values for mysticetes and
monodonts are included, a phylogenetic pattern in relative lung mass is observed (Figure
18). Mysticetes, physeterids, ziphiids, and kogiids all possess relative lung masses that
are similar to those predicted for terrestrial mammals. That is, lung size in these cetaceans
is a plesiomorphic character. And across these groups relative lung size is not uniformly
associated with deep or prolonged diving – kogiids, physeterids and ziphiids are deep
divers, but mysticetes are not.
To investigate the relationship between lung mass and diving without regard to
phylogenetic relationships, indices of diving ability (e.g. Williams et al. 2008) were
developed based upon information available in the literature (Table 12). Those species
with dive depth and duration data were coded as either a (1) short duration shallow diver,
(2) short duration deep diver (i.e. “deep sprinters” sensu Soto et al. 2008), or (3) long
duration deep diver. A species was defined as a shallow diver if its commonly reported
dive depth was under 100m (see Figure 1, inflection point on the depth-volume curve).
Common, rather than maximum, dive depths were used because all species, even
typically shallow divers, have been recorded or trained to dive to depths greater than
100m. Short dive duration was defined as a common dive duration under 25min. While,
62
Table 12. Common diving capacity measures for a variety of odontocetes for which a corresponding lung mass and total body mass
ratio was available. (* = common depth or duration did not exist for that species and instead maximum record was used)
Family
Dive
Duration
(min.)
Dive Depth (m)
Method
D. delphis
Delphinidae
5*
260*
time depth recorder
Evans 1971, Ridgway and Harrison
1986
S. attenuata
Delphinidae
1.26 1.68
22.1 - 24.0
time depth recorder
Scott and Chivers 2009
T. truncatus
Delphinidae
1
< 20
satellite-linked
recorder
P. phocoena
Phocoenidae
1
14-40
recorder
D. leucas
Monodontidae
12 to 15
400-600
satellite-linked
recorder
Kogia spp.
Kogiidae
12*
> 400
Species
Mate et al. 1995, Ridgway et al. 1986
Westgate et al. 1995
Heide-Jorgensen et al. 1998, Martin
and Smith 1999
recorder transponder Scott et al. 2001
Physeteridae
40-50O
400-600ST
ST=sonar
transponder,
O=observation
H. ampullatus
Ziphiidae
40
800
recorder
M.densitrostris
Ziphiidae
48-68*
1251*D - 1408*T
D=Digital TAG, T=
time depth recorder
P.macrocephalus
Citation
63
Jaquet et al. 2000, Norris and Harvey
1972, Papastavrou et al. 1989, Watkins
et al. 1985, Panigada et al. 1999,
Scholander 1940
Hooker and Baird 1999
Baird et al 2004, Tyack et al. 2006
Family
Lung Mass:TBM (%) Diving Capacity
Delphinidae
2.7%
Shallow, Short & Deep, Short
Phocoenidae
3.0%
Shallow, Short
Monodontidae
Terrestrial 1.0%
Mammals
2.6%
Ziphiidae
1.4%
Kogiidae
1.3%
Physeteridae
0.9%
Mysticetes
0.9%
Deep, Short
Deep, Long
Deep, ?
Deep, Long
Shallow, Short
Figure 18. The ratio of lung mass vs. total body mass is mapped upon a phylogeny for cetaceans (Messenger and McGuire 1998, Price
et al. 2005). The ratio for terrestrial mammals is derived from the allometric equation of Brody (1945). A shallow dive was defined as
a common dive depth < 100m, while a short dive duration was defined as a common dive duration that was < 25min.
64
these definitions are somewhat arbitrary, they do offer broadly comparative bins into
which cetacean species could be placed. The slopes of the lines that describe the
allometric relationship between lung mass and total body mass for these three defined
groups of divers were not significantly different from each other (Table 13). However,
their y-intercepts did differ significantly (F = 62.16, P < 0.0001, d.f. = 176; Table 13).
Deep, prolonged divers possessed significantly smaller lungs than did deep, short divers,
which in turn possessed significantly smaller lungs than did shallow, short divers (Figure
19).
Species were also coded based upon a physiological metric associated with diving
– the myoglobin concentration of locomotor muscle (Table 14). Species were divided
into two bins, dependent upon whether their myoglobin concentrations were below or
above 4g/100g wet weight muscle. In this case, the slopes of the lines that describe the
allometric relationship between lung mass and total body mass for these two defined
groups were significantly different from each other (F = 18.19, P < 0.0001, d.f. = 190;
Table 13). Species with high myoglobin concentrations [Feresa attenuata (a delphinid),
Hyperoodon ampullatus, Kogia spp., and Physeter macrocephalus] possessed smaller
lungs. Most species with relatively large lungs possessed a low myoglobin concentration
(Delphinus delphis, T. truncatus, Stenella attenuata, Delphinapterus leucas). The
exceptions were Stenella coeruleoalba and Phocoena phocoena, which possessed both
high myoglobin concentrations and relatively large lungs (Figure 20). Thus, within the
odontocetes, species with relatively small lungs tend to be long-duration, deep divers
with relatively high myoglobin concentrations. High myoglobin concentrations can,
though, also be found in some large-lunged delphinids and phocoenids.
65
Table 13. Summary of allometric relationships between lung mass and total body mass
for diving behavior and myoglobin content. Shallow dive depth was defined as a common
dive depth under 100m. Short dive duration was defined as a common dive duration
under 25min. Myoglobin content was defined as below or above 4g/100g wet weight
muscle. y = axb, where y = lung mass (kg) and x = total body mass (kg). (n = sample size,
a = y-intercept, b = slope, S.E. = standard error)
n
a
b
S.E.
Shallow, Short Duration
126
0.220
0.986
0.023
Deep, Short Duration
Deep, Long Duration
37
14
0.175
0.136
Myoglobin
Low Myoglobin
126
0.221
0.984
0.035
High Myoglobin
65
0.253
0.833
0.018
Diving Behavior
66
Table 14. Myoglobin values for a variety of odontocetes for which a corresponding lung
mass and total body mass were available.
Family
Myoglobin
(g /100 g
wet
muscle)
Citation
D. delphis
Delphinidae
3.4 - 3.55
Dolar et al. 1999,
Noren et al. 2000
F. attenuata
Delphinidae
5.7
Dolar et al. 1999
S. attenuata
Delphinidae
2.5
Dolar et al. 1999
S. coeruleoalba
Delphinidae
5.78
Noren et al. 2000
T. truncatus
Delphinidae
2.5 to 3.5
P. phocoena
Phocoenidae
4.03 - 4.1
D. leucas
Monodontidae
3.44
Noren et al. 2000
Kogia spp.
Kogiidae
4.33
Noren et al. 2000
Physeteridae
5.7
Dolar et al. 1999
Ziphiidae
6.3
Dolar et al. 1999
Species
P.macrocephalus
H. ampullatus
67
Dolar et al. 1999,
Noren et al. 2000
Dolar et al. 1999,
Noren et al. 2000
3
Log Lung Mass (kg)
2
1
0
-1
Short, Shallow Divers
Short, Deep Divers
Long, Deep Divers
-2
0
1
2
3
4
5
Log Total Body Mass (kg)
Figure 19. Log lung mass (kg) vs. log total body mass (kg) of species within five
families (Kogiidae, Physeteridae, Ziphiidae, Delphinidae and Phocoenidae). Each species
was coded as either a short duration shallow diver, short duration deep diver, or long
duration deep diver (Table 12). The slopes of all three of these lines are similar, however,
the y-intercepts differ significantly (see Table 13).
68
3
Log Lung Mass (kg)
2
1
0
-1
Low Myoglobin (< 4g/100g wet muscle)
High Myoglobin (> 4g/100g wet muscle)
-2
0
1
2
3
Log Total Body Mass (kg)
4
5
Figure 20. Log lung mass (kg) vs. log total body mass (kg) of species within five
families (Kogiidae, Physeteridae, Ziphiidae, Delphinidae and Phocoenidae). Each species
was coded according to its species-specific myoglobin level (Table 14). The slopes of
these lines are significantly different (see Table 13).
69
Although these analyses were undertaken without the explicit use of phylogenetic
information, it is clear that these characters co-occur within the closely related families of
Physeteridae, Ziphiidae, and Kogiidae. Species within these families also achieve large
body sizes, which has been positively correlated to dive depth and duration within the
odontocetes (Schreer and Kovacs 1997).
The mapping of relative lung size onto cetacean phylogeny presented in Figure 18
suggests that the lungs of the deep diving kogiids, physeterids, and ziphiids are not
specialized, relative to the putative ancestral condition. In contrast, it does appear that the
relatively large lung mass observed in delphinids and phocoenids is a shared, derived
character in these families. Most of these species tend to be short-duration shallow divers,
although there are some short-duration deep divers within Delphinidae. In diving
odontocetes, the lungs function as an oxygen store for respiratory gas exchange, a
dynamic buoyancy regulation organ, and as a reservoir for air required for echolocation
(i.e. pneumatic excitation of the phonic lips; Cranford et al. 1996). What are the
functional consequences for a shallow diving species of possessing relatively large lungs?
It is unlikely that a large lung is required to provide air sufficient to support
echolocation at shallow depths. Deep diving ziphiids and physeterids, with their
relatively small lungs, can echolocate at great depths (800-1,000m) (Baird et al. 2004,
Miller et al. 2004, Tyack et al. 2006, Watwood et al. 2006) when the air within the
respiratory system is compressed to only 1-2% of its volume at the surface.
The buoyant function of a large lung in shallow diving marine mammals has been
considered by Taylor (1994). He hypothesized that lung size would vary between species
that control their position within the water column hydrostatically versus
70
hydrodynamically. The shallow diving manatee, for example, has a large lung within a
very dense body (Domning and deBuffrenil 1991). This body composition permits the
manatee to hydrostatically control its position within the water column. Its lungs undergo
large absolute changes in volume (and therefore density) at shallow depths, and coupled
with its dense body, permit the manatee to achieve negative buoyancy at depths of less
than 10m.
Taylor (1994) hypothesized that marine mammals, such as odontocete cetaceans,
which hydrodynamically control their position within the water column, should possess
small lungs and low density bodies. A small lung (and therefore air volume) would
reduce the work required to overcome buoyancy during a dive, and decrease the depth at
which the swimming animal would become neutrally buoyant. This pattern is observed in
the deep diving kogiid, but not in the shallow diving T. truncatus. The dolphin’s
relatively large lung likely increases the mechanical work required to dive (see
Stephenson et al. 1989). It also likely causes the dolphin to experience large changes in
buoyancy at shallow depths, although the functional consequences of this effect in an
animal that controls its position within the water column hydrodynamically are not
known.
It seems likely that the large lung size of the shallow diving T. truncatus permits it
to function as an important oxygen store for respiratory gas exchange during a shallow
dive. Using existing data on mass specific metabolic rates and total lung capacity (TLC)
(Williams et al. 1992, Irving et al. 1941, Ridgway et al. 1969, Kooyman 1973, Kooyman
and Sinnett 1979), one can calculate the relative contributions of lung oxygen stores to
maintaining metabolic function during different activities for an adult bottlenose dolphin
71
(200kg) (Table 15). For a resting bottlenose dolphin, experiencing a prolonged (1min)
apnea, the lungs can provide 169-285% of the oxygen required to maintain its metabolic
rate. For a similarly-sized kogiid, assuming it has a metabolic rate similar to that of a
bottlenose dolphin, the lung can provide only 35-60% of the oxygen required. If a
bottlenose dolphin swam on a 1min breath-hold at a typical swimming speed (2.1m/s,
Williams et al. 1992), the lungs could provide 138-231% of the oxygen required.
Assuming metabolic similarity, the kogiid lung could provide only 29-49% of the oxygen
required during a 1min apneic swim. Thus, the lungs of T. truncatus can provide much of
the oxygen required during rest and routine swimming (even on a prolonged 1min breathhold), whereas kogiid lungs cannot. Bottlenose dolphins do not routinely swim on an
extended breath-hold; their respiratory rate is 2-3breaths/min. Bottlenose dolphins are
therefore replenishing their lung oxygen stores at a much higher rate than the one used in
these “back of the envelope” calculations.
Kooyman (1973) and Scholander (1940) have categorized cetaceans as either
“fast” or “slow” breathers. A “fast breather” usually surfaces on the move and takes a
single breath each time that they pass rapidly through the air-water interface. A “slow
breather” must stay at the surface after a dive and ventilate a number of times to replenish
oxygen stores. By this definition, T. truncatus is a “fast breather” and kogiids are “slow
breathers”. During a ventilation cycle, T. truncatus can routinely exchange 75%, and
maximally up to 90%, of its total lung volume in a third of a second at the surface (Irving
et al. 1941, Ridgway et al. 1969). In contrast, kogiids have been observed to come to the
surface after a dive and log for multiple ventilations (recorded in one individual for up to
11min)(Allen 1941, Yamada 1953, Nagorsen 1985, Caldwell and Caldwell 1989, Scott et
72
Table 15. The estimated contribution of lung oxygen stores to meeting metabolic costs of resting and swimming in T. truncatus and
kogiids. Calculations were based on a 200kg* adult animal with a resting metabolic rate of 6.53mL O2 / kg•min (Williams et al. 2001)
and a swimming (at 2m/s) metabolic rate of 8.07mL O2 / kg•min (Williams et al. 1992). Under both conditions, the animal’s
metabolic costs were calculated for a 1min apnea. The kogiid lung volumes were estimated at 2.1% of the values for T. truncatus (see
Table 6).
TLC (L)*
O2
Available
in Lungs
(L)**
Amount of
Air Required
for Condition
(L)
O2
Provided
by Lungs
(%)
T. truncatus
10-17.7
2.2-3.7
1.3
169-285%
Kogia spp.
2.2-3.7
0.46-0.78
1.3
35-60%
T. truncatus
10-17.7
2.2-3.7
1.6
138-231%
Kogia spp.
2.2-3.7
0.46-0.78
1.6
29-49%
Rest 1min apnea
2.1m/s swim for 1min apnea
* Ridgway et al. (1969) states that a 200kg carcass possessed a 10-11L lung volume. In contrast, from
an allometric equation of lung volume to total body mass in Kooyman (1973) and Kooyman and Sinnett
(1979), a 200kg animal should have a lung volume of 17.7L. Both these values were used to bracket the
calculations.
** accounts for 21% oxygen in air
73
al. 2001, Baird 2004). Their high ventilation rate, short ventilation times and
extraordinarily large tidal volumes suggest that bottlenose dolphins require frequent
replenishment of their lung oxygen stores. Thus, it seems likely that the large lung of the
shallow diving bottlenose dolphin functions primarily to support metabolic demands of a
relatively active lifestyle.
Large heart size has also been observed in animals that are capable of high
endurance activity (Crile and Quiring 1940a, Brody 1945, Tenney and Remmers 1963,
Ridgway and Johnston 1966, Bryden 1972). In the young cross-sectioned specimens, the
ratios of heart volume to total post-cranial body volume were very similar between T.
truncatus and K. sima. However, when heart mass to total body mass was compared
across these two species (n = 38 for T. truncatus and n = 18 for Kogia spp.), T. truncatus
possessed a heart mass significantly larger than that of similarly-sized Kogia spp. (Figure
21). Although the slopes of the lines that describe these allometric relationships were
similar, the y-intercepts did differ significantly (F = 28.51, P < 0.0001, d.f. = 57). When
compared to adult terrestrial mammals T. truncatus possessed a relative heart mass
similar to that of the thoroughbred race horse, Equipoise, while kogiids possessed a
relative heart mass more similar to that of an ox (Table 16; Howell 1930, Crile and
Quiring 1940a, Ridgway and Johnston 1966). Thus, T. truncatus, a shallow diving, “fast”
breathing cetacean possesses significantly larger lungs and heart than a deep diving,
“slow” breathing kogiid.
This study also investigated whether the musculoskeletal thorax of the deep
diving kogiid was more mobile than that of the shallow diving bottlenose dolphin.
Overall, there were no differences in thoracic mobility across species and both species
74
Table 16. Heart mass (kg) vs. total body mass (kg) ratios for a variety of cetaceans. An allometric equation of terrestrial mammals
was used to predict heart mass for each cetacean when total body mass was known (y = 0.006 x0.98, n = 568, r2 = 0.98; Stahl 1967).
(* = data represents the mean value for the sample of that species; NR = not reported)
Megaptera novaeangliae
Balaenoptera borealis
Balaenoptera musculus
Balaenoptera physalus
Eschrichtiidae robustus
3
NR
NR
NR
NR
TBM
(kg)
39311*
NR
NR
NR
NR
Physeter macrocephalus
NR
NR
0.30%
---
Physeter macrocephalus
1
39,000
0.32%
0.49%
Bryden 1972, Quiring 1943, Kenyon 1961
Ziphius cavirostris
1
2952
0.52%
0.51%
Bryden 1972, Quiring 1943, Kenyon 1961
Kogia spp.
Phocoena phocoena
Phocoenoides dalli
Lagenorhynchus obliquidens
Delphinapterus leucas
19
NR
4
5
NR
195*
NR
NR
NR
NR
0.48%*
0.80%
1.31%*
0.85%*
0.60%
0.54%
---------
UNCW database
Slijper 1958
Ridgway and Johnston 1966
Ridgway and Johnston 1966
Omura 1950
Delphinapterus leucas
Tursiops truncatus
Tursiops truncatus
Tursiops truncatus
NR
38
4
NR
521.18
202.3*
NR
NR
0.61%
0.61%*
0.54%*
1.00%
0.53%
0.54%
-----
Crile and Quiring 1940a
UNCW database
Ridgway and Johnston 1966
Slijper 1958
Thoroughbred race horse, "Equipoise"
Ox
1
71
521.5
536*
0.85%
0.35%*
0.53%
0.53%
Crile and Quiring 1940a
Howell 1930, Crile and Quiring 1940a
Species
n
HM /
TBM
1.50%*
0.40%
0.50%
0.70%
0.50%
Stahl
prediction
0.49%
---------
75
Citation
Bryden 1972, Quiring 1943, Kenyon 1961
Omura 1950
Crile and Quiring 1940a, Nishiwaki 1950
Nishiwaki 1950
Omura et al. 1969
Crile and Quiring 1940a, Omura 1950
0.6
Kogia spp.
Terrestrial Mammals
Tursiops truncatus
Log Heart Mass (kg)
0.4
0.2
0.0
-0.2
-0.4
-0.6
-0.8
1.4
1.6
1.8
2.0
2.2
2.4
2.6
2.8
Log Total Body Mass (kg)
Figure 21. Log heart mass (kg) vs. log total body mass (kg) for T. truncatus and Kogia
spp. compared to adult terrestrial mammals (y = 0.006 x0.98, n = 568, r2 = 0.98; Stahl
1967). The slopes of these lines are similar; however, the y-intercepts differ significantly
(see Table 4). Data obtained from UNCW database.
76
could achieve a 20-30% change in thoracic cavity volume. However, due to the
differences in the ecology of these cetaceans, this change in thoracic cavity volume may
be accommodating different features of their lifestyle. T. truncatus is a shallow diver and,
thus, routinely experiences rapid and large changes in thoracic air volume. The
specialized morphological features of the T. truncatus thorax may also function to permit
rapid changes in thoracic volume that may be required during their explosive ventilatory
event (Cotten et al. 2008).
Although the excised kogiid thorax could change shape similar to that of T.
truncatus, on a dive thoracic collapse may be limited. Kogiids possess small lungs that
will undergo absolutely smaller changes in volume during a dive. Within the thorax,
kogiids also possess more extensive vascular structures that may dynamically increase
their volume during a dive. The dorsal arterial rete in K. sima was twice the volume of
that in T. truncatus. Interestingly, there may be another structure, bounded by the
musculoskeletal thorax, which could function as a blood reservoir during a dive. For
example, in adult harbor seals, the hepatic sinus is approximately the size of the liver and
can store at least 1L of blood when completely filled (Harrison and Tomlinson 1956).
The pericardial venous plexus is fed in part by the hepatic sinus of the liver. The liver of
K. sima was 1.5 times the volume of that of T. truncatus (Table 4, Figure 22). When the
relationship between liver mass and total body mass was investigated between these
groups (n = 17 for T. truncatus and n = 104 Kogia spp.) the slope of the line for kogiids
was significantly higher than for T. truncatus (F = 5.35, P = 0.0225, d.f. = 120). When
compared to a variety of other cetaceans, kogiids possessed the largest relative liver mass
(Table 17). The kogiid liver was twice the mass of that predicted for a similarly sized
77
Table 17. Liver mass (kg) vs. total body mass (kg) ratios for a variety of cetaceans. An
allometric equation of terrestrial mammals was used to predict liver mass for each
cetacean when total body mass was known (y = 0.033 x0.87, n = 175, r2 = 0.984; Brody
1945). (* = data represents the mean value for the sample of that species; NR = not
reported)
n
TBM
(kg)
LM /
TBM
Brody
prediction
Balaenoptera borealis
NR
NR
1.30%
---
Bryden 1972
Balenoptera musculus
NR
NR
1.20%
---
Bryden 1972
Balenoptera physalus
NR
NR
1.00%
---
Bryden 1972
Eschrichtius robustus
NR
NR
0.90%
---
Bryden 1972
Megaptera novaeangliae
3
39311*
1.20%*
0.83%
Bryden 1972
Physeter macrocephalus
1
39000
1.07%
0.83%
Bryden 1972
Physeter macrocephalus
NR
NR
1.60%
---
Bryden 1972
Ziphius cavirostris
1
2952
0.88%
1.17%
Bryden 1972
Kogia spp.
17
180*
3.60%*
1.68%
UNCW database
Phocoena phocoena
28
37*
3.19%*
---
Slijper 1958
Phocoena phocoena
NR
NR
3.20%
---
Bryden 1972
Tursiops truncatus
NR
NR
2.20%
---
Bryden 1972
Tursiops truncatus
104
117.7*
2.40%*
1.78%
Delphinapterus leucas
NR
NR
1.50%
---
Species
78
Citation
UNCW database
Bryden 1972
4.5
Kogia spp.
Terrestrial Mammals
T. truncatus
Log Liver Mass (g)
4.0
3.5
3.0
2.5
2.0
1.5
3.8
4.0
4.2
4.4
4.6
4.8
5.0
5.2
5.4
5.6
5.8
Log Total Body Mass (g)
Figure 22. Log liver mass (kg) vs. log total body mass (kg) for T. truncatus and Kogia
spp. compared to adult terrestrial mammals (y = 0.033 x0.87, n = 175, r2 = 0.984; Brody
1945). The slopes of these lines were significantly different (see Table 4). Data obtained
from UNCW database.
79
terrestrial mammal. A larger liver may be able to supply more blood to the pericardial
venous plexus within the thorax at depth.
A future study is needed to examine the thorax and lungs of a shallow and deep
diving cetacean under controlled compression. The morphology and the connections of
multiple vascular structures to other structures has yet to be well-described in a deep
diving cetacean, and how blood is circulated through these structures at depth is
unknown.
CONCLUSION
This study provides evidence to support the hypothesis that the lungs of deep
diving kogiids are significantly smaller, by both mass and volume, than those of the
shallow diving T. truncatus. Calculations based upon mass specific metabolic rates and
total lung capacities suggest that the shallow diving, “fast” breathing T. truncatus may be
using its large lung as an oxygen store to meet its metabolic demands. Similar
calculations for kogiids, assuming metabolic similarity, suggest that their lungs are too
small to provide the oxygen required for even a one minute resting apnea. Overall, the
mobility of the isolated thorax of T. truncatus and kogiids was similar. Thoracic mobility
in T. truncatus may accommodate the routine large changes in thoracic air volume this
species experiences during shallow diving, and may function to permit rapid changes in
thoracic volume required during explosive ventilation. In contrast, the small lung of the
deep diving, “slow” breathing kogiids likely reduces the absolute change in thoracic
volume that occurs during a dive and may contribute to negative buoyancy at shallow
depths. Kogiids also possess extensive thoracic vasculature and a large liver, which may
80
also function to limit thoracic collapse. A phylogenetic analysis suggests that the small
lung size in deep diving odontocetes is a plesiomorphic character rather than a
specialization for diving. The large lung size of delphinids and phocoenids appears to be
a derived condition that likely permits it to function as an oxygen store for respiratory gas
exchange in these active, relatively shallow divers.
81
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94
APPENDIX
Appendix A. Specimens used in this study either stranded or were incidentally killed in
fishing operations. All specimens used in this study were in fresh to moderate condition
(Smithsonian Institute Code 1 through 3; Geraci and Lounsbury 2005). Each specimen
was placed into a life history category as defined by Caldwell and Caldwell (1989), Mead
and Potter (1990), Struntz et al. (2004), and Dunkin et al. (2005). (N/E = not examined,
CBD = could not be determined, NR = not recorded, BC = body condition, NE = not
emaciated, E = emaciated)
Species
Total
Length
(cm)
WAM 635 f,h,i
K. breviceps
116.5
Total
Body
Mass
(kg)
34.6
ASF 029 f,h,i
K. breviceps
124.0
PEM 1516/99 f,h,i
K. sima
VAQS 20081002 d
SAM 35799 f,h,i
Life
History
Category
Code
BC
Neonate
2
NE
N/E
Sub-adult
1
NE
152.5
61.8
Sub-adult
NR
E
K. sima
160.0
77.0
Sub-adult
2
NE
K. sima
178.0
104.5
Sub-adult
NR
E
K. breviceps
198.0
134.0
Sub-adult
1
E
DAP 032 f,h,i
K. sima
207.0
137.0
Sub-adult
1
E
KLC 025 g
K. sima
213.0
N/E
Sub-adult
2
NE
VAQS 20081003 a,c,f
K. sima
218.4
161.5
Sub-adult
1
NE
CLP 001 a,b,c,f,h,i
K. breviceps
225.0
158.0
Adult
1
E
PEM 1516/97 f,h,i
K. sima
235.0
209.1
Adult
NR
NE
K. breviceps
237.0
219.0
Adult
1
E
K. sima
237.0
NR
Adult
NR
NR
a,c,f,g,h,i
K. breviceps
258.0
234.5
Adult
3
E
MLC 003 b,f,g,h
K. breviceps
262.0
386.2
Adult
1
NE
BRF 092 f,h,i
K. breviceps
267.0
316.6
Adult
1
NE
KMS 427 f,h,i
K. breviceps
267.0
363.6
Adult
1
NE
KMS 429 f,h,i
K. breviceps
283.0
371.8
Adult
2
NE
K. breviceps
292.0
400.0
Adult
1
NE
DAP 033 h
K. breviceps
302.0
N/E
Adult
1
E
WAM 644 b,f,h,i
K. breviceps
307.0
392.0
Adult
1
NE
NMNH 504737 e,f
K. breviceps
328.0
465.0
Adult
1
NE
VMSM 971062 h
K. breviceps
133.0
40.0
Neonate
1
NE
Field Identification
Number
WAM 637 a,c,e,f,g,h,i
WAM 634
a,c,f,h,i
NMNH 504221 e
VAQS 20071081
KMS 373
f,h
95
Appendix A. (cont'd)...
Species
Total
Length
(cm)
PEM 1518/85 i
K. sima
189.0
Total
Body
Mass
(kg)
129.5
PEM 1519/59 i
K. sima
189.0
113.2
Sub-adult
NR
NR
PEM 1516/51 h,i
K. sima
136.0
47.3
Sub-adult
NR
NR
No Tag f
T. truncatus
101.5
13.9
Neonate
2
NE
VMSM 951022 f
T. truncatus
104.0
13.8
Neonate
2
E
VMSM 961035 f,i
T. truncatus
105.0
14.4
Neonate
2
NE
T. truncatus
106.0
14.4
Neonate
2
NE
VMSM 20001020 f,i
T. truncatus
106.5
14.4
Neonate
2
NE
CALO 99-19 f,i
T. truncatus
108.0
16.5
Neonate
2
NE
NC 98-079 f,i
T. truncatus
108.0
14.7
Neonate
2
NE
CALO 99-13 f,i
T. truncatus
109.5
14.7
Neonate
2
NE
VMSM 20011080 f,i
T. truncatus
110.0
15.5
Neonate
2
E
VMSM 20021042 f,i
T. truncatus
111.0
19.8
Neonate
2
NE
MMB 003 f,i
T. truncatus
113.0
15.6
Neonate
2
E
VGT 073 f,i
T. truncatus
113.6
16.5
Neonate
2
NE
WAM 550 f,i
T. truncatus
114.5
19.8
Neonate
1
NE
VMSM 19991086 f,i
T. truncatus
115.0
22.7
Neonate
2
NE
VMSM 931046 f,i
T. truncatus
115.0
20.4
Neonate
2
NE
WAM 584 f
T. truncatus
119.0
N/E
Neonate
2
NE
CALO 96-23 f,i
T. truncatus
119.2
17.6
Neonate
2
E
VMSM 20001031 f,i
T. truncatus
127.0
29.2
Neonate
2
NE
VMSM 20011087 f,i
T. truncatus
129.7
30.7
Neonate
2
NE
T. truncatus
131.5
23.8
Neonate
2
NE
VMSM 971049 f,i
T. truncatus
138.0
39.0
Neonate
2
NE
VMSM 20031082 f,i
T. truncatus
142.0
41.8
Neonate
2
NE
VMSM 971045 f,i
T. truncatus
144.0
43.3
Neonate
2
NE
ASF 042 f,i
T. truncatus
146.0
46.4
Neonate
2
NE
VMSM 20021089 f,i
T. truncatus
148.0
49.4
Neonate
2
NE
VMSM 971053 i
VMSM 961028 i
T. truncatus
108.0
18.6
Neonate
2
NE
T. truncatus
110.5
20.5
Sub-adult
2
NE
Field Identification
Number
EMM 010
f,i
NC 98-097
f,i
96
Life
History
Category
Code
BC
Sub-adult
NR
NR
Appendix A. (cont'd)...
Species
Total
Length
(cm)
WAM 569 f,i
T. truncatus
150.0
Total
Body
Mass
(kg)
56.0
VMSM 971060 f,i
T. truncatus
153.3
48.1
Neonate
2
NE
NEFC 00101 571382 f,i
T. truncatus
157.6
53.8
Sub-adult
2
NE
VMSM 921021 f,i
T. truncatus
158.0
61.8
Sub-adult
2
NE
NEFC 00102 571383 f,i
T. truncatus
158.3
58.7
Sub-adult
2
NE
NEFC 00103 571385 f,i
T. truncatus
159.1
55.8
Sub-adult
2
NE
ASF 001 f,i
T. truncatus
160.5
47.4
Sub-adult
2
NE
VMSM 931028 f,i
T. truncatus
163.0
54.4
Sub-adult
2
NE
93-MM-AO-TT-07 f,i
T. truncatus
164.5
63.3
Sub-adult
3
NE
DAP 034 f,i
T. truncatus
169.0
61.3
Sub-adult
2
NE
"No ID" d
T. truncatus
170.9
62.5
Sub-adult
1
NE
KMT 091 f,i
T. truncatus
172.0
70.6
Sub-adult
3
NE
WAM 607 f,i
T. truncatus
173.0
74.5
Sub-adult
2
NE
VAQS 20061008 f,i
T. truncatus
175.1
90.0
Sub-adult
3
NE
VMSM 951037 f,i
T. truncatus
177.0
64.8
Sub-adult
2
NE
T. truncatus
182.0
79.0
Sub-adult
3
NE
T. truncatus
187.0
93.0
Sub-adult
3
NE
RJM 003 g
T. truncatus
188.0
N/E
Sub-adult
2
CBD
PTM 117 f,i
T. truncatus
189.0
73.6
Sub-adult
2
E
VAQS 20051118 f
T. truncatus
189.0
90.2
Sub-adult
1
NE
VMSM 20031043 f,i
T. truncatus
190.5
94.8
Sub-adult
2
NE
VMSM 19961061 f,i
T. truncatus
191.0
107.2
Sub-adult
2
NE
WAM 627 f,h,i
T. truncatus
194.0
93.0
Sub-adult
2
NE
SDZ 001 f,i
T. truncatus
195.0
84.5
Sub-adult
2
NE
VMSM 2004 1079 f,i
T. truncatus
195.0
98.0
Sub-adult
2
NE
VAQS 20051086 f,h,i
T. truncatus
195.4
93.0
Sub-adult
2
NE
VGT 176 f,i
T. truncatus
196.0
84.0
Sub-adult
2
NE
WAM 609 f,h,i
T. truncatus
197.5
110.0
Adult
2
NE
VMSM 20041024 i
WJW 007 i
T. truncatus
190.0
51.2
Sub-adult
2
E
T. truncatus
273.0
294.8
Adult
1
NE
Field Identification
Number
BRF 090 a,c
NCAFFTT 053104
f,i
97
Life
History
Category
Code
BC
Neonate
2
NE
Appendix A. (cont'd)...
Species
Total
Length
(cm)
DAP 031 f,i
T. truncatus
201.0
Total
Body
Mass
(kg)
92.0
MMSC 92-11571496f,o,i
T. truncatus
202.2
75.2
Sub-adult
3
E
NEFSC 03976 f
T. truncatus
203.0
128.6
Sub-adult
2
NE
VMSM 2004 1042 f,i
T. truncatus
203.6
95.7
Sub-adult
3
NE
KMT 013 f,i
T. truncatus
204.0
98.2
Sub-adult
2
NE
VMSM 20031104 f,i
T. truncatus
204.0
114.0
Sub-adult
2
NE
VMSM 20001049 f,i
T. truncatus
207.0
114.0
Sub-adult
1
NE
NEFC 016 571381 f,i
T. truncatus
208.5
114.3
Sub-adult
2
NE
VGT 087 f,i
T. truncatus
209.8
122.7
Sub-adult
2
NE
KMT 099 f,i
T. truncatus
212.0
114.0
Sub-adult
2
NE
PTM 047 f,i
T. truncatus
212.0
124.6
Sub-adult
2
NE
VMSM 941001 f,i
T. truncatus
212.0
83.0
Sub-adult
2
E
VGT 155 f,i
T. truncatus
216.0
181.8
Sub-adult
2
NE
NEFSC 5451 f,i
T. truncatus
218.0
158.0
Sub-adult
2
NE
KMT 100 f
T. truncatus
219.0
153.6
Sub-adult
2
E
T. truncatus
221.0
N/E
Sub-adult
3
NE
T. truncatus
222.8
114.0
Sub-adult
2
E
KR 001 (571521) f,i
T. truncatus
223.0
149.0
Sub-adult
2
NE
KMT 023 f,i
T. truncatus
223.5
150.4
Sub-adult
2
NE
PTM 007 f,i
T. truncatus
225.0
162.6
Adult
2
E
VMSM 2004 1027 f,i
T. truncatus
225.0
141.4
Sub-adult
2
NE
WAM 647 f,g
T. truncatus
225.0
153
Sub-adult
2
NE
BCB 004 g
T. truncatus
228.0
N/E
Sub-adult
2
NE
NEFSC 5332 f,i
T. truncatus
228.0
163.0
Sub-adult
1
NE
KMT 051 f,o,i
T. truncatus
229.0
96.0
Sub-adult
2
E
VAQS 20071081 h
T. truncatus
275.0
234.5
Adult
3
E
CJH 003 f,i
WAM 553 f,i
T. truncatus
229.5
138.0
Adult
2
NE
T. truncatus
232.0
160.0
Sub-adult
2
NE
Field Identification
Number
RJM 004 g
WAM 591
f,i
98
Life
History
Category
Code
BC
Sub-adult
2
NE
Appendix A. (cont'd)...
Species
Total
Length
(cm)
VMSM 2004 1040 f,i
T. truncatus
234.5
Total
Body
Mass
(kg)
139.0
MMB 002 f
T. truncatus
235.0
167.0
Sub-adult
2
NE
PTM 074 f,h,i
T. truncatus
237.0
197.2
Adult
2
NE
WAM 579 f,h,i
T. truncatus
237.0
184.0
Adult
2
E
MML 0412 (FB119) f,h,i
T. truncatus
238.0
168.0
Adult
2
CBD
HOF 007 f,h,i
T. truncatus
238.8
184.0
Adult
1
NE
T. truncatus
239.0
126.4
Adult
2
E
WAM 559 f,h,i
T. truncatus
239.0
166.0
Adult
1
NE
VMSM 951023 f,h,i
T. truncatus
240.0
232.8
Adult
2
NE
WAM 573 f,h,i
T. truncatus
241.5
200.0
Adult
2
NE
WAM 633 a,c,f,g,h,i
T. truncatus
244.0
180.0
Adult
1
NE
WAM 560 f,h,i
T. truncatus
245.0
193.0
Adult
1
NE
PBN 003 a,c,f,g,h,i
T. truncatus
246.0
173.0
Adult
2
E
WAM 545 f,h,i
T. truncatus
246.0
238.0
Adult
2
NE
T. truncatus
246.0
213.0
Adult
2
NE
VGT 168 f,h,i
T. truncatus
247.0
164.6
Adult
2
E
VMSM 951039 f,h,i
T. truncatus
249.0
190.0
Adult
2
NE
WAM 642 f,h,i
T. truncatus
250.0
226.0
Adult
2
NE
NEFSC 01408 f,o,h,i
T. truncatus
252.0
236.0
Adult
2
NE
VGT 049 f
T. truncatus
253.0
254.0
Adult
2
NE
WAM 533 f,o,h
T. truncatus
261.0
170.0
Adult
2
E
BRF 164 f,o,h,i
T. truncatus
262.0
216.5
Adult
1
NE
f,h,i
T. truncatus
264.0
297.0
Adult
2
NE
REL 014 f,h,i
T. truncatus
265.0
260.4
Adult
2
NE
VMSM 921006 f,h,i
VMSM 941101 f,o,h,i
T. truncatus
265.0
210.0
Adult
2
NE
T. truncatus
265.0
263.1
Adult
2
NE
Field Identification
Number
VMSM 951045
WAM 628
WAM 535
f,h,i
f,h,i
99
Life
History
Category
Code
BC
Sub-adult
2
NE
Appendix A. (cont'd)...
Species
Total
Length
(cm)
VMSM 951035 f,h,i
T. truncatus
267.0
Total
Body
Mass
(kg)
199.0
AJW 001 f,o,h,i
T. truncatus
274.0
BRF 061 f,h,i
T. truncatus
WAM 631 f,o,h,i
Life
History
Category
Code
BC
Adult
2
NE
231.0
Adult
1
NE
275.0
257.0
Adult
2
NE
T. truncatus
275.0
209.0
Adult
2
NE
WAM 639 f,h,i
T. truncatus
276.0
290.0
Adult
3
NE
MML 0111 f,h,i
T. truncatus
277.0
170.2
Adult
NR
E
VMSM 951051 f,h,i
T. truncatus
277.0
196.0
Adult
2
E
KLC 020 f,o,i
T. truncatus
282.0
228.0
Adult
3
E
DAP 027 f,o,h
T. truncatus
283.0
233.0
Adult
2
E
571687 f,i
T. truncatus
300.5
312.0
Adult
2
E
Field Identification
Number
a
Gross description of thorax
Gross description of mycology in Kogia
c
Thorax manipulations
d
Cross-section anatomy and volume
e
Skeleton drawing
f
Lung mass: Total Body Mass
g
Lung volume
h
Heart mass
i
Liver mass
o
Offshore morphotype based on morphological characteristics
b
100
Appendix B. Cetacean species, investigated by VAQS or UNCW, used to compare lung mass to total body mass across a broader
phylogenetic sample. All specimens used in this study were in fresh to moderate condition (Smithsonian Institute Code 1 through 3;
Geraci and Lounsbury 2005). Each specimen was placed into a life history category as defined by stranding records. (NE = not
examined, NR = not recorded, CBD = could not be determined)
Field
Identification
Number
EgNEFL 0704
Species
Family
Total Length
(cm)
Total Body
Mass (kg)
Life History
Category
Code
Body Condition
Eubalaena glacialis
Balaenida
401.0
749.0
Sub-adult
3
CBD
KLC 022
Eubalaena glacialis
Balaenida
495.0
1586.0
Neonate
1
not emaciated
CTH 001
VMSM 20031051
VMSM 20041024
VAQS 20081012
VAQS 20081009
Balaenoptera acutorostrata
Delphinus delphis
Delphinus delphis
Delphinus delphis
Delphinus delphis
Balaenopteridae
Delphinidae
Delphinidae
Delphinidae
Delphinidae
284.0
183.0
190.0
199.0
200.0
211.4
66.8
51.2
70.0
88.0
Sub-adult
Sub-adult
Sub-adult
Sub-adult
Adult
1
1
2
1
1
emaciated
not emaciated
emaciated
emaciated
not emaciated
VAQS 20081013
Delphinus delphis
Delphinidae
200.5
86.0
Adult
1
not emaciated
VMSM 20031099
Delphinus delphis
Delphinidae
202.0
86.0
Adult
1
not emaciated
VMSM 20031090
Delphinus delphis
Delphinidae
207.0
74.4
Adult
2
emaciated
VMSM 19981025
VAQS 20051007
VMSM 20011030
Delphinus delphis
Delphinus delphis
Delphinus delphis
Delphinidae
Delphinidae
Delphinidae
215.0
222.0
223.0
100.8
130.0
112.7
Adult
Adult
Adult
1
2
1
not emaciated
not emaciated
not emaciated
VMSM 20011045
Delphinus delphis
Delphinidae
232.0
114.4
Adult
2
not emaciated
VMSM 20041020
Delphinus delphis
Delphinidae
232.0
132.0
Adult
1
not emaciated
GNL 080
Feresa attenuata
Delphinidae
205.0
122.4
Adult
1
not emaciated
SC 0735
Feresa attenuata
Delphinidae
207.0
128.0
Adult
1
not emaciated
VMSM 20031052
Globicephala melas
Delphinidae
201.0
103.0
Sub-adult
1
not emaciated
VMSM 951002
Grampus griseus
Delphinidae
173.0
57.2
Neonate
2
emaciated
VMSM 19981045
Grampus griseus
Delphinidae
277.0
197.6
Adult
1
NR
VAQS 20051082
Grampus griseus
Delphinidae
277.2
301.4
Adult
1
NR
101
Appendix B. (cont'd)...
Field Identification
Number
Species
Family
Total
Length
(cm)
Total Body
Mass (kg)
Life History
Category
Code
Body Condition
DMB 008
LRD 003
VAQS 20081066
VAQS 20081069
Lagenorhynchus acutus
Lagenorhynchus acutus
Peponocephala electra
Peponocephala electra
Delphinidae
Delphinidae
Delphinidae
Delphinidae
164.0
165.0
247.8
249.4
55.0
46.4
157.0
166.5
Sub-adult
Neonate
Adult
Adult
1
1
2
1
not emaciated
NR
NR
not emaciated
VMSM 941095
Stenella attenuata
Delphinidae
174.4
64.7
Sub-adult
2
NR
WAM 602
Stenella clymene
Delphinidae
202.0
92.0
Adult
1
not emaciated
VMSM 971064
SGB 127
Stenella coeruleoalba
Stenella coeruleoalba
Delphinidae
Delphinidae
135.5
152.8
28.8
41.0
Sub-adult
Sub-adult
2
2
NR
not emaciated
SGB 126
Stenella coeruleoalba
Delphinidae
172.5
63.0
Sub-adult
1
not emaciated
VAQS 20051117
VMSM 20031005
WAM 622
WAM 619
WAM 615
WAM 612
WAM 614
WAM 618
WAM 623
WAM 621
Stenella coeruleoalba
Stenella coeruleoalba
Stenella coeruleoalba
Stenella coeruleoalba
Stenella coeruleoalba
Stenella coeruleoalba
Stenella coeruleoalba
Stenella coeruleoalba
Stenella coeruleoalba
Stenella coeruleoalba
Delphinidae
Delphinidae
Delphinidae
Delphinidae
Delphinidae
Delphinidae
Delphinidae
Delphinidae
Delphinidae
Delphinidae
181.8
184.5
219.0
222.0
223.0
225.0
225.5
226.0
229.5
230.0
64.0
76.0
116.0
120.0
120.0
120.5
118.0
129.5
128.5
134.0
Sub-adult
Sub-adult
Adult
Adult
Adult
Adult
Adult
Adult
Adult
Adult
2
1
2
2
2
2
2
2
2
2
NR
not emaciated
not emaciated
not emaciated
not emaciated
not emaciated
not emaciated
not emaciated
not emaciated
not emaciated
WAM 620
Stenella coeruleoalba
Delphinidae
233.5
146.0
Adult
2
not emaciated
WAM 613
Stenella coeruleoalba
Delphinidae
235.0
123.0
Adult
2
not emaciated
WAM 645
Stenella frontalis
Delphinidae
177.0
59.0
Adult
2
not emaciated
SGB 114
Stenella sp.
Delphinidae
NR
47.8
NR
2
NR
102
Appendix B. (cont'd)...
Field Identification
Number
Species
Family
Total
Length
(cm)
Total Body
Mass (kg)
Life History
Category
Code
Body Condition
VMSM 971002
MLC 001
VMSM 20011013
VMSM 971010
DMB 001
Phocoena phocoena
Phocoena phocoena
Phocoena phocoena
Phocoena phocoena
Phocoena phocoena
Phocoenidae
Phocoenidae
Phocoenidae
Phocoenidae
Phocoenidae
109.5
113.0
113.0
119.0
133.0
20.4
20.0
22.8
22.3
28.2
Sub-adult
Sub-adult
Sub-adult
Sub-adult
Adult
2
1
2
2
1
NR
not emaciated
not emaciated
NR
emaciated
VMSM 977013
Phocoena phocoena
Phocoenidae
170.5
21.6
Adult
2
NR
WAM 593
VMSM 20021056
VMSM 931036
NMNH 571568
VMSM 20031098
Mesoplodon densitrostris
Mesoplodon europeus
Mesoplodon europeus
Mesoplodon europeus
Mesoplodon mirus
Ziphiidae
Ziphiidae
Ziphiidae
Ziphiidae
Ziphiidae
423.0
204.0
214.6
422.0
391.0
940.3
75.5
86.2
760.0
618.2
Adult
Sub-adult
Neonate
no sperm
Sub-adult
2
1
1
2
3
not emaciated
not emaciated
NR
NR
emaciated
103
Appendix C. Description of measurements taken during thoracic mobility manipulations.
In the maximally expanded and collapsed postures the following measurements were
taken:
(1) length of the thorax from the cranial margin of vertebral rib 1 to the caudal margin of
the last vertebral rib, at mid-shaft (“1” on datasheet);
(2) length of cranial vertebral ribs only, from the cranial margin of vertebral rib 1 to the
caudal margin of last sternally connected vertebral rib (for T. truncatus vertebral rib 6
and for kogiids vertebral rib 4), at mid-shaft (“2” on datasheet);
(3) length of the sternal ribs from the cranial margin of sternal rib 1, at its articulation
with the sternum, to the caudal margin of the terminal sternal rib (for T. truncatus
vertebral rib 8 and for kogiids vertebral rib 11 or 12), at mid-shaft (“3” on datasheet);
(4) length of the thorax from the cranial margin of sternal rib 1, at its articulation
with the sternum, to the caudal margin of the last vertebral rib, at mid-shaft (“4” on
datasheet);
(5) length of the distance between the cranial margin of the manubrium, at the midline,
to the ventro-cranial margin of cervical vertebra 1, at the midline (“5” on datasheet);
(6) two measures of thoracic inlet height:
(a) perpendicular distance between the ventral surface of the vertebral body and
the dorsal surface of the sternal midline (“a” on datasheet);
(b) straight-line measurement between the ventral surface of the angle of
vertebral rib 1 and dorsal surface of the manubrium wing (“b” on datasheet);
(7) external thoracic height, taken at the level of each rib, as the perpendicular distance
from the dorsal most aspect of the rib (either dorsal rib angle or articulation of the
104
vertebral rib with the transverse process, whichever is highest) to the ventral
articulation with the sternum (ventral most aspect of the sternum or for the caudal ribs
their ventral most tip) (“Lat. Height” on datasheet);
(8) thoracic inlet width as the perpendicular distance between the medial surfaces of the
first vertebral-sternal rib joints in T. truncatus (“c” on datasheet) and between the
medial surfaces of the first vertebral rib, at mid-shaft, in kogiids (“d” on datasheet);
(9) external thoracic width, taken at the level of each rib as the perpendicular distance
between the widest position between vertebral ribs (usually mid-shaft) (“Ext. Width”
on datasheet);
(10) thoracic vertebral width as the distance from right to left transverse processes at
each vertebra, which is added to the circumference measurements (“Vert. Width” on
datasheet).
(11) thoracic circumference was measured at the level of each sternal rib between the
left and right vertebra-vertebral rib joints; the circumferences were measured for
the cranial vertebral ribs only, i.e. those that have associated sternal ribs
(“Circumference” on datasheet).
(12) thoracic wall thicknesses was measured at the level of vertebral rib 1 and the
last sternally connected vertebral rib (for T. truncatus vertebral rib 6 and for kogiids
vertebral rib 4), at three circumferential positions: (a) angle of rib, (b) mid-shaft and
(c) just lateral to adjacent sternabra.
105
Appendix D. Datasheet used to define measurements of the thorax in a cranially
expanded and caudally collapsed position. Each dimension was measured (cm) three
times and then the mean was calculated. Measurements include, lateral lengths (1), (2),
(3), (4), (5); widths at each vertebral rib; lateral height at each vertebral rib; lateral
vertebra width at each vertebra; circumference at each vertebral rib that has an associated
sternal rib (i.e. for T. truncatus at each vertebral rib for vertebral ribs 1-6); inlet
dimensions (a), (b), (c), (d); and thoracic wall thicknesses at six different locations (not
shown here).
THORAX MOBILITY
Field ID: ___________
Species: _____________
Position: suspended OR supine
cranial OR caudal
TL: _____
TBM: ______
Muscle Present: _____________
Spring Load (kg): _____________
Fishing Line Position: ___________________________________________
106
Appendix E. The equations of all four models used to estimate thoracic cavity volume
are listed here.
The first model to estimate thoracic cavity volume used a frustum of a right
circular cone in series with a slanted right circular cone (see Figure 6A; Sandifer and
Moshos 1996):
(1) frustum of a right circular cone,
V ⅓ π l r2 Rr R2 , where l = length between vertebral ribs 1-5, r = radius of a circle at the cross-section
between vertebral ribs 1-2 (derived from the circumference measurement taken between
ribs 1-2), and R = radius of a circle at the cross-section between vertebral ribs 5-6
(derived from the circumference measurement taken between ribs 5-6).
(2) slanted right circular cone,
V ⅓ π cos θ L R2,
where L = length between vertebral rib 5 and lumbar vertebra 3, R= radius of circle at the
cross-section between ribs 5-6 (derived from the circumference measurement taken
between vertebral ribs 5-6) and θ = the angle of approach of the diaphragm to lumbar
vertebra 3 (Sandifer and Moshos 1996).
The second model included a right circular cylinder for the cranial thorax in
series with the same slanted right circular cone used above for the caudal thorax (see
above for slanted cone equation; Figure 6B; Sandifer and Moshos 1996):
(1) right circular cylinder,
107
V π r2 l ,
where r = average radius of circle at the cross-section between ribs 1-2 (derived from the
circumference measurements taken between vertebral ribs 1-6), and l = length between
vertebral ribs 1-5.
A third model to estimate thoracic cavity volume included a frustum of a right
cardioid cone in series with a slanted right cardioid cone (Figure 6C):
(1) frustum of a right cardioid cone,
V 1/2 l π r2 rR R2 , where a = radius of cardioid at the cross-section between vertebral ribs 1-2 (derived from
the lateral width measurements taken between vertebral ribs 1-2), A = radius of cardioid
at the cross-section between vertebral ribs 5-6 (derived from lateral width measurements
taken at vertebral ribs 5-6), and l = length between vertebral ribs 1-5.
(2) slanted right cardioid cone,
V 1/2 π cos θ L R2, where L = length between vertebral rib 5 and lumbar vertebra 3, A= radius of cardioid at
the cross-section between ribs 5-6 (derived from the lateral width measurement taken
between vertebral ribs 5-6) and θ = the angle of approach of the diaphragm to lumbar
vertebra 3 (Sandifer and Moshos 1996).
The fourth and final model used to estimate thoracic cavity volume utilized a
right cardioid cylinder, for the cranial thorax, in series with the slanted right cardioid
108
cone for the caudal thorax. The following equation was used for the cardioid shaped
cylinder (see equation in model 3 for slanted cone) (Figure 6D):
(1) right cardioid cylinder,
V 3/2 π r2 l, where a = average radius of cardioid at the cross-section between vertebral ribs 1-6
(derived from the average of lateral width measurements taken between vertebral ribs 16), and l = length between vertebral ribs 1-5.
109