Integrative and Comparative Biology

Integrative and Comparative Biology, volume 56, number 6, pp. 1285–1297

doi:10.1093/icb/icw123 Society for Integrative and Comparative Biology

SYMPOSIUM

Secondary Evolution of Aquatic Propulsion in Higher Vertebrates:

Validation and Prospect
Frank E. Fish1
Department of Biology, West Chester University, 750 S. Church St., West Chester, PA 19383, USA

Downloaded from https://academic.oup.com/icb/article/56/6/1285/2647100 by guest on 10 February 2024

From the symposium ‘‘Functional (Secondary) Adaptation to an Aquatic Life in Vertebrates’’ presented at the
International Congress of Vertebrate Morphology (ICVM11), June 29–July 3, 2016 at Washington D.C.
1
E-mail: ffish@wcupa.edu

Synopsis Re-invasion of the aquatic environment by terrestrial vertebrates resulted in the evolution of species expressing
a suite of adaptations for high-performance swimming. Examination of swimming by secondarily aquatic vertebrates
provides opportunities to understand potential selection pressures and mechanical constraints, which may have directed
the evolution of these aquatic species. Mammals and birds realigned the body and limbs for cursorial movements and
flight, respectively, from the primitive tetrapod configuration. This realignment produced multiple solutions for aquatic
specializations and swimming modes. Initially, in the evolution of aquatic mammals and birds, swimming was accom-
plished by using paired appendages in a low-efficiency, drag-based paddling mode. This mode of swimming arose from
the modification of neuromotor patterns associated with gaits characteristic of terrestrial and aerial locomotion. The
evolution of advanced swimming modes occurred in concert with changes in buoyancy control for submerged swimming,
and a need for increased aquatic performance. Aquatic mammals evolved three specialized lift-based modes of swimming
that included caudal oscillation, pectoral oscillation, and pelvic oscillation. Based on modern analogs, a biomechanical
model was developed to explain the evolution of specialized aquatic mammals and their transitional forms. Subsequently,
fossil aquatic mammals were described that validated much of the model. However, for birds, which were adapted for
aerial flight, fossil evidence has been less forthcoming to explain the transition to aquatic capabilities. A biomechanical
model is proposed for birds to describe the evolution of specialized lift-based foot and wing swimming. For both birds
and mammals, convergence in morphology and propulsive mechanics is dictated by the need to increase speed, reduce
drag, improve thrust output, enhance efficiency, and control maneuverability in the aquatic environment.

Introduction replaced the sprawling stance and rapid, low-endur-

With approximately 70% of the planet’s surface cov-
ered by water, it is not surprising that a wide variety
of vertebrate lineages have secondarily invaded the
aquatic environment. The re-invasion of the aquatic
environment by terrestrial vertebrates has been one
of the great evolutionary transformations. This trans-
formation occurred in all the groups of tetrapod ver-
tebrates at different times in the evolutionary history
of the earth. These seminal events have been parti-
cularly notable for aquatic mammals and birds,
whose evolution occurred at least 300 million years
after the first steps by vertebrates moving from water
onto land. Terrestrial locomotion by mammals and
birds departed from the typical reptilian design for
walking and running on land. Mammals and birds
ance locomotion with an erect stance and high-
endurance physiology. In addition, birds modified
their forelimbs as wings and took to the air.
For mammals and birds, movement into water
and the evolution of efficient swimming mechanisms
from terrestrial and aerial habits has meant large-
scale morphological and physiological changes to op-
erate in a radically different environmental medium.
Compared with the physical environments experi-
enced on land and in the air, aquatic animals
move through a higher-density and more viscous
medium, where drag effects are increased. In water,
the density ratio (density of animal/density of envi-
ronment) is near unity (Daniel and Webb 1987).
Therefore, the effects of gravity are diminished as

Advanced Access publication October 3, 2016

ß The Author 2016. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology.
All rights reserved. For permissions please email: journals.permissions@oup.com.
1286
mammals and birds are buoyed up by the water and
weight is no longer a concern. On land, weight and
static friction of the limb with the ground limit speed
(Daniel and Webb 1987). The gravity-dominated ter-
restrial environment has presented biomechanical
and energetic hurdles to the transition of organisms
from walking to swimming (Fish 1992, 1996;
Williams 1999). In flight, weight and the large dif-
ferential between the densities of air and water have
dictated the morphology and locomotor perfor-
mance of birds (Daniel and Webb 1987). The lack
of continuous contact with the ground or the lack
of persistent negative buoyancy (lift) in the air has
provided challenges to maintaining stability. Such
challenges are largely absent in water, where the
density ratio fosters neutral buoyancy without dire
consequences to stability (due to loss of lift or
thrust) or to body orientation.
Both aquatic mammals and birds have undergone
large morphological, physiological, and behavioral
adjustments to operate in water. The body has
been streamlined with a fusiform shape to reduce
the drag and energy to move through a dense aquatic
medium (Webb 1975, 1988; Aleyev 1977; Fish 1993a,
1996). Thrust production has been enhanced with
elongated, webbed feet that act as paddles, and
even more effective oscillating hydrofoils in the
form of wing-like flippers and caudal flukes.
Paddles are drag-based propulsors that operate well
for surface swimming, but have low efficiency and
produce large thrust only at slow speeds; whereas
oscillating hydrofoils are highly efficient when the
animal is fully submerged and function at high
swimming speeds (Webb 1975, 1988; Vogel 1994;
Fish 1996). Increasing size in aquatic mammals and
birds is associated with lift-based propulsion that
provides high thrust, and body shapes that minimize
drag (Webb and de Buffrénil 1990). Physiological
adjustments for thermoregulation (e.g., blubber,
counter-current exchange, thermal windows), deep
diving (e.g., collapsible lungs, enlarged spleen), and
endurance swimming (e.g., migrations, high aerobic
scope) are necessary for obligate air-breathing ho-
meothermic endotherms to perform in water
(Kooyman 1973, 1989; Noren et al. 2001; Castellini
and Mellish 2016). Enhanced efficiency, endurance,
and speed are facilitated by behavioral strategies.
Bow riding, submerged swimming, drafting, hydro-
planing, and burst-and-coast swimming are examples
of mechanisms used by aquatic mammals and birds
to reduce the energy cost of swimming (Hertel 1966;
Williams 1989; Fish and Hui 1991; Williams et al.
1992; Fish 1994, 1995; Williams 1999; Fish et al.
2013).
F. E. Fish
The evolutionary changes in aquatic mammals and
birds have occurred through transitional forms that
were simultaneously semiaquatic and semiterrestrial
(Fish and Baudinette 1999). These intermediate,
semiaquatic species were in an energetically precari-
ous position (Williams 1999) as they were not spe-
cialized for either aquatic or terrestrial habitats. The
energetic performance by intermediate species was
limited in each environment by both anatomy and
physiology that were compromises amid the dispa-
rate forces experienced on land and in water. The
evolution of increasingly aquatic habits in mammals
Downloaded from https://academic.oup.com/icb/article/56/6/1285/2647100 by guest on 10 February 2024
and birds necessitated adaptations that allowed them
to optimize energy use by reduction of resistive
forces, improvement in propulsive force production
and efficiency, thermoregulation, and control of
buoyancy (Fish 1996; Williams 1999).
The early evolution of aquatic mammals and birds
can be traced through the fossil record and modern
analogs of marine lineages (Barnes et al. 1985; Fish
1996, 2000; Thewissen and Fish 1997; Thewissen and
Bajpai 2001; Berta 2012; Gingerich 2015). Because
modern semiaquatic species are the best representa-
tions of the transitional aquatic forms (Fish 1996;
Thewissen and Fish 1997), direct examination of
morphologies and physiologies of extant species can
point to the potential selective factors and mechan-
ical constraints that directed the evolution of more
derived aquatic forms. While the fossil record pro-
vides exceptionally strong evidence for the evolution-
ary changes within lineages, the record is incomplete.
It has only been in the last 33 years that numerous
fossil transitional forms of marine mammals have
been unearthed to provide a more complete picture
of the evolution of cetaceans, pinnipeds, and sire-
nians (Domning 2001a; Berta 2012; Thewissen
2014; Gingerich 2015). However, the fossil record
for aquatic birds is poor. While molecular techniques
have delivered evidence relating penguins with a sea-
bird clade including Procellariiformes, Gaviiformes,
Pelecaniformes, and Ciconiiformes (Simpson 1946;
Ho et al. 1976; Ksepka and Ando 2011), the transi-
tional forms and their swimming mechanics have
been less forthcoming.
Twenty years ago (Fish 1996), I proposed a bio-
mechanical model (Fig. 1) to explain the routes from
terrestrial mammals to the highly derived marine
mammals (e.g., cetaceans, pinnipeds), which was
later refined (Fish 2000). As new fossils have been
unearthed, it is appropriate to reevaluate the model
and its predictions and determine what questions
still remain unresolved. As much of the model ap-
pears to address the evolutionary changes that oc-
curred in the various lineages of aquatic mammals,
Swimming evolution
Fig. 1 Model for sequence of swimming mode transitions from
terrestrial quadruped and drag-based propulsion to advanced
high-performance modes using lift-based propulsion. Surface-
swimming mammals use alternate paddling modes and possess
non-wettable fur (gray), which provides positive buoyancy. With a
shift to submerged swimming, semiaquatic mammals adopted
swimming modes that increased performance and countered the
buoyancy of the fur. Increased time in the water coincided with
the evolution of highly efficient lift-based swimming modes using
oscillating hydrofoils and replacement of fur with blubber (black)
as a means of thermal protection and control of buoyancy with
deeper diving.
a corresponding biomechanical model can be hy-
pothesized for the evolution of aquatic birds based
on the modern analogs.
Aquatic mammal functional model
The phylogenetic relationships of all aquatic mam-
mals indicate that there was a fully terrestrial ances-
tor. Therefore, within any clade, it is assumed that an
ancestral terrestrial mammal would first have swum
by paddling quadrupedally with alternating strokes
(Fig. 1; Rayner 1985; Fish 1993a). Modern terrestrial
mammals swim with this quadrupedal mode (Davis
1942; Dagg and Windsor 1972; Fish 1993c).
Quadrupedal swimming is considered to result
from conservative neuromotor patterns (Jenkins
and Goslow 1983; Goslow et al. 1989; Smith 1994;
Fish 1996) that are independent of changes in mor-
phology and functional role (Smith 1994). Neural
patterns, such as central pattern generators, would
control the repetitive motions of the legs by
1287
Downloaded from https://academic.oup.com/icb/article/56/6/1285/2647100 by guest on 10 February 2024
Fig. 2 Diagram illustrating the drag-based and lift-based propul-
sive modes and the associated major forces. The drag-based
mode is illustrated by the paddling muskrat (Ondatra zibethicus).
Lift-based propulsion is indicated by the sea lion (Zalophus cali-
fornianus): pectoral oscillation; the harp seal (Pagophilus groenlan-
dica): pelvic oscillation; bottlenose dolphin (Tursiops truncatus):
caudal oscillation. The forces indicated are the body drag (D),
thrust (T), lift (L), and drag on the propulsive appendage (d). The
actions and relationships of the forces are described in the text.
providing the correct timing for muscular contrac-
tion (Grillner 1975, 1985, 1996; Stein et al. 1995).
Changing from quadrupedal terrestrial locomotion
to quadrupedal swimming would therefore utilize
the same neuromotor patterns as would further
modification associated with more derived swim-
ming modes.
Paddling is a drag-based propulsive mode with the
limbs oriented and stroking fore and aft in parasa-
gittal planes (Fish 1996). The stroke cycle is divided
into power and recovery phases. During the power
phase, the posterior sweep of the foot generates drag,
which is used to generate an anteriorly-directed
thrust to propel the animal (Fig. 2). To maximize
the thrust, the digits of the feet are abducted
(spread) to increase the planar area, and the limb
is extended to increase the lever length while rapidly
accelerated. The recovery phase repositions the limb
for another power stroke. As the limb is moving
anteriorly, it incurs a non-thrust-generating drag
1288
that adds to the total drag on the body. To minimize
the additional drag, the digits of the feet are ad-
ducted and positioned close to the body to reduce
the planar area.
As mammals became semiaquatic, the need for
greater swimming performance (i.e., speed, effi-
ciency) is proposed to have led to a shift from qua-
drupedal paddling to bipedal paddling when
swimming at the water surface. This bipedal paddling
used alternating motions of either the pectoral or
pelvic limbs (Fig. 1). Bipedal paddling avoids me-
chanical and hydrodynamic interference between
the limbs and frees one set for stabilization, maneu-
vering, tactile reception, or food capture and pro-
cessing (Dagg and Windsor 1972; Fish 1993c).
With the development of pectoral or pelvic paddling,
specialization of the limbs would have been favored
wherever a greater commitment to life in water
proved advantages to increase thrust and improve
stability. These specializations associated with modi-
fications of the propulsive limbs included (1) devel-
opment of a short, robust humerus and femur, (2)
elongation of digits, (3) increase in propulsive sur-
face (planar) area by addition of interdigital webbing
or fringe hairs, and (4) increase in bone density for
stability (Tarasoff et al. 1972; Stein 1981, 1989; Wyss
1988; Berta and Ray 1990; Fish and Stein 1991;
Thewissen et al. 1994; Fish 1996).
Semiaquatic habits led to the acquisition of non-
wettable fur by some species. This fur provided
greater thermal insulation against the high thermal
conductivity of water and enhanced buoyancy for
swimming on the water surface (Fish 1992, 1996;
Fish et al. 2002). The dense pelage traps air, also
reducing the density of the animal and thus provid-
ing hydrostatic buoyancy (Davis 1942; Dagg and
Windsor 1972; Williams 1983; Fish 1993c). Control
of buoyancy by hydrostatic equilibrium uncouples
maintenance of posture from swimming motions to
ensure continuous breathing, while a more horizon-
tal posture would have enhanced streamlining in
swimming (Fish 1993c). Without the need to gener-
ate lift for flotation, a more effective bipedal pad-
dling mode, using either forelimbs or hind limbs,
can be employed in swimming (Fish 2000).
From alternate paddling, it is postulated that
rowing would develop as some lineages transitioned
from surface swimming to foraging underwater
(Fig. 1). Rowing requires reorientation of the limbs
by abduction of the humerus or femur from the
vertical to the horizontal plane for pectoral rowing
or pelvic rowing, respectively. The reorientation of
the limbs was needed to counter positive buoyancy
when submerged (Fish 2000). With the limbs in the
F. E. Fish
horizontal plane, the feet could be twisted to gener-
ate both thrust and a downward force on the body to
oppose positive buoyancy. This mechanism is em-
ployed by the platypus, Ornithorhynchus anatinus,
and muskrat, Ondatra zibethicus (Mizelle 1935;
Howell 1937; Fish et al. 1997).
An alternative mode of submerged swimming
from alternate pelvic paddling involved simultaneous
pelvic paddling (Fig. 1). This mode is based on the
terrestrial bounding gait and is used by the sea otter,
Enhydra lutris, and the river otter, Lontra canadensis,
to swim rapidly underwater (Tarasoff et al. 1972;
Downloaded from https://academic.oup.com/icb/article/56/6/1285/2647100 by guest on 10 February 2024
Williams 1989; Fish 2000). However, the simulta-
neous strokes have a severe disadvantage in that
thrust will be produced only in half the stroke
cycle, leading to periodic accelerations and increased
drag during the recovery phase of the hind feet.
Oscillations in velocity would be reduced by dorso-
ventral flexion of the body and tail, which produces
a propulsive traveling wave for undulatory swimming
(Fish 1994). The traveling wave moves faster poste-
riorly than the animal moves forward, and its am-
plitude increases to a maximum toward the tip of the
tail. Use of undulatory motions would maintain
thrust production through the entire propulsive
cycle and increase the efficiency of locomotion
(Fig. 2). With abandonment of limbs for inefficient
paddle propulsion and distal expansion of the tail,
swimming performance (i.e., reduced energy cost,
increased speed) would be improved (Fish 1994,
1996, 2000). The increased surface area and large
amplitude of oscillation at the tip of the tail work
against a greater mass of water, increasing total mo-
mentum, as traveling waves move along the body
(Webb 1975).
The final phase in the evolution of the most de-
rived aquatic mammals (e.g., otariids, phocids, odo-
benids, cetaceans, sirenians) involved the transition
to a lift-based mechanism by oscillatory movements
of the propulsive appendages (Figs. 1 and 2; pelvic
oscillation, caudal oscillation, pectoral oscillation).
For these animals, the propulsive appendages were
modified as wing-like hydrofoils, such as the flippers
for pinnipeds and caudal flukes of cetaceans and si-
renians (Fish 2004). A forward-canted lift due to
oscillation of the hydrofoil could be resolved into a
thrust component acting continuously through the
stroke cycle (Feldkamp 1987a, 1987b; Fish et al.
1988; Fish 1993b, 1998a, 1998b). This propulsive
mechanism would further increase swimming speed
and efficiency.
The shift to high-efficiency lift-based propulsive
modes is considered to have coincided with the re-
placement of non-wettable fur with blubber as
Swimming evolution
aquatic mammals spent greater amounts of time in
the water and descended to greater depths when for-
aging (Fish 2000). This shift from fur to blubber
reduces the high maintenance cost of grooming
and prevents loss of buoyancy and thermal insulation
due to fouling (Wolfe and Esher 1981; Williams
1989; Williams and Davis 1995). Also, blubber is
not compressed as water pressure increases with
depth, consistently affording the animal near-neutral
buoyancy (body density ¼ water density). The differ-
ence in density of marine mammals (cetaceans, pin-
nipeds) is 3–11% lower than seawater (Aleyev 1977).
At neutral buoyancy, control surfaces and propulsors
are liberated from buoyancy control for use in ma-
neuvering and high-efficiency lift-based swimming.
Evidence for model validation
Fossils of extinct aquatic mammals and the genetic
relationships among the various lineages of both
aquatic and non-aquatic mammals have aided in de-
veloping a more complete picture of the evolutionary
transition from land to sea (Berta 2012; Gingerich
2015). Previous attempts at articulating the interme-
diate stages have been based on little hard evidence
and instead formulated from mere speculation
(Flower 1883; Gutmann 1994). Gutmann (1994) pro-
vided pictorial schemes of the evolution of cetaceans
from a cursorial mammal, sirenians from a terrestrial
grazer, and pinnipeds from a swimming bear, but
without supporting documentation. It has only
been in the past 33 years that enough fossils of tran-
sitional forms and their respective postcranial skeletal
materials have been unearthed to make reasonable
assertions regarding the evolution of swimming
modes. The skeleton of the archaeocete Basilosaurus
was discovered in the 19th century and reconstruc-
tions of Basilosaurus pictured this whale swimming
with lateral undulations of the body and small hor-
izontal flukes, or passing multiple waves down the
body in the vertical plane (Gingerich et al. 1990; Fish
2001). In another case, the Eocene protocetacid
Pakicetus was reconstructed prematurely with an
otter-like body and swimming mode, in the absence
of postcranial material (Gingerich et al. 1983).
Recently a number of cetacean fossils were discov-
ered with sufficient postcranial material to determine
their ability to walk on land. Eocene protocetaceans
included Indohyus (Fig. 3; Thewissen et al. 2007),
Pakicetus (Fig. 4; Thewissen et al. 2001; Madar
2007), Ambulocetus (Fig. 4; Thewissen et al. 1994),
Kutchicetus (Bajpai and Thewissen 2000), Rodhocetus
(Gingerich et al. 1994, 2001), and Maiacetus
(Gingerich et al. 2009). Later species that reflect a
1289
Fig. 3 Skeletal reconstruction of Indohyus, an Eocene artiodactyl
of the family Raoellidae that is closely related to whales.
(Courtesy of J.G.M. Thewissen).
Downloaded from https://academic.oup.com/icb/article/56/6/1285/2647100 by guest on 10 February 2024
more fully aquatic lifestyle, including Basilosaurus
and Dorudon, displayed hind limbs with a remnant
pelvis, femur, tibia and digits, demonstrating a link
with terrestrial quadrupeds (Gingerich et al. 1990;
Thewissen and Bajpai 2001). Modern cetaceans still
possess a small innominate bone that is imbedded in
the ventral musculature. Similarly, sirenians had an
intermediate species, Pezosiren, with four well-devel-
oped legs and the ability to walk quadrupedally on
land (Domning 2001a). Pezosiren and Ambulocetus
had limited undulatory swimming ability as the
caudal vertebrae of both species lacked broad tra-
verse processes for attachment of large tail muscles.
Swimming would have utilized simultaneous pelvic
paddling in concert with spinal undulations similar
to otters (Fish 1994; Thewissen and Fish 1997;
Domning 2001a).
The structure of the vertebral column, legs, and
size of the feet indicate a progressive change from
terrestrial to aquatic existence for both cetaceans and
sirenians. Both groups showed a similar trajectory
(Thewissen and Fish 1997; Domning 2001a).
Paddling with limbs in a drag-based swimming
mode is associated with slow swimming and is inef-
ficient compared with lift-based swimming (Fish
1996, 2000). By eliminating use of inefficient pad-
dling appendages, the undulatory mode is expected
to dominate, improving performance. The use of si-
multaneous paddling to initiate spinal undulation
and a propulsive traveling wave in the tail would
maintain thrust throughout the stroke cycle (Fish
1994). A large mass of water accelerated by dorso-
ventral movements of the undulating tail could pro-
duce large propulsive forces, independent of paddling
motions of the feet. The river otter, L. canadensis,
dorso-ventrally undulates the body and tail in con-
junction with simultaneous paddling efforts of the
hind feet (Fig. 2; Tarasoff et al. 1972; Fish 1994).
Thrust produced by undulation in Lontra would
be low, because the tail tapers to a narrow tip.
The tail tip has the largest amplitude of motion
1290
Fig. 4 Skeletons and reconstructions of the quadrupedal Eocene whales, Pakicetus (A, C) and Ambulocetus (B, D). (Images courtesy of
J.G.M. Thewissen).
and potentially could affect the greatest volume of
water, but the tapered tip reduces momentum ex-
change (Fish 2000). The beaver, Castor canadensis,
the giant otter, Pteronura brasiliensis, and the ex-
tinct Mesozoic mammal Castorocauda lutrasimilis,
have broad tails that when undulated can produce
large amounts of thrust (Rue 1964; Fish 1994;
Qiang et al. 2006).
The addition of caudal flukes further enhances
performance in the final transition to lift-based
swimming. The fossil gradient shows enlarged hind
feet for paddling (e.g., Ambulocetus; Thewissen and
Fish 1997), lengthening, and strengthening of the
vertebral column for undulation (e.g., Kutchicetus,
Rodhocetus), and eventually caudal oscillation (i.e.,
Dorudon, modern cetaceans). The presence of a
long, robust tail is a precondition for development
of caudal oscillatory swimming. The sequence of ce-
tacean fossils is summarized in Fig. 5 with their os-
teology, locomotor swimming modes, associated
performance and morphology.
The important transitional pinnipeds are repre-
sented by Puijila (Rybczynski et al. 2009) and
Enaliarctos (Berta et al. 1989; Berta and Ray 1990).
Puijila had an otter-like body with a long tail and
large, probably webbed feet (Rybczynski et al. 2009;
Berta 2012). Puijila and another, earlier-described
otter-like carnivore, Potamotherium (Savage 1957)
have been hypothesized to be semiaquatic, inhabiting
F. E. Fish
Downloaded from https://academic.oup.com/icb/article/56/6/1285/2647100 by guest on 10 February 2024
freshwater (Rybczynski et al. 2009). The elongate tail
in these otter-like mammals contradicts the model
proposed above, which predicts a short tail in ances-
tral pinnipeds and thus precludes caudal oscillation
as a possible endpoint for a high-efficiency propul-
sive mode. Without a long tail, pinnipeds would
have been restricted to limbed propulsion. Whether
Puijila is an early pinnipedimorph or early arctoid
carnivore is still unclear (Berta 2012). In addition,
sea otters (Enhydra) have short tails compared with
related freshwater lutrines. The short tail of the sea
otter precludes its use in generating thrust, necessi-
tating the enlargement and use of the hind feet as
propulsors (Kenyon 1969; Williams 1989). The pin-
niped Enaliarctos had a short tail (Berta and Ray
1990). In the one to seven million years between
the appearances of Puijila and Enaliarctos, transi-
tional species may have developed a shorter tail
with movement into cold seawater. Both Puijila
and Enaliarctos had well-developed limbs, adapted
for terrestrial locomotion. The limbs of later pinni-
peds increased in size and became differently special-
ized for lift-based swimming depending on the clade
(e.g., otariid, phocid) and particular mode (e.g.,
pelvic oscillation, pectoral oscillation) of limbed
swimming (Wyss 1989; Berta and Ray 1990; Fish
2000).
A possible explanation for the possession of long
or short tails may lie in an association with
Swimming evolution
Fig. 5 Summary of associated osteological features, swimming modes, locomotor performance, and morphological changes in the
evolution of the Cetacea. (Courtesy of W. Bemis).
thermoregulation in different climates. On account
of their high surface-to-volume ratios and vasculari-
zation, mammal tails can act as effective thermoreg-
ulatory devices, adjusting body temperature by
regional heterothermia (Fish 1979; Hickman 1979).
In warm climates, a long tail could be used to coun-
teract overheating by dumping excess metabolic heat
to the environment. In cold climates where insula-
tion may be essential, a short tail would limit heat
loss. This thermoregulatory hypothesis is supported
by paleoclimatic evidence and fossil distributions
(Fish 2001). The long-tailed ancestors of cetaceans
and sirenians originated in tropical and subtropical
climates (Domning 1976; Barnes et al. 1985;
Gingerich et al. 1994; Thewissen et al. 1994).
Reviewing the distributions of fossil cetaceans,
Fordyce (1992) likewise inferred a warm-water
origin for cetaceans. However, the short-tailed pin-
nipeds originated in temperate or subarctic climates
(Repenning 1976; Barnes et al. 1985).
Other evidence supporting the biomechanical
model comes from the physiology of modern analogs
(Fish 1996, 2000; Williams 1999). Whereas limbed
swimming by semiaquatic mammals is associated
with inefficiencies and high energetic costs (Fish
1992; Williams 1999), the converse is considered
true for some fully aquatic mammals. These species
1291
Downloaded from https://academic.oup.com/icb/article/56/6/1285/2647100 by guest on 10 February 2024
are far removed from their terrestrial ancestors and
as such are specialized to live and forage primarily in
water. In this regard, evolution of the propulsive ap-
pendages has shaped the limbs into high-efficiency
hydrofoils, which affect locomotion by transferring
momentum to the fluid surroundings. This change
in limb structure, although negatively impacting an
aquatic mammal’s performance on land, enhances
performance in the water.
Aquatic bird functional model
How did birds that perfected winged aerial flight give
rise to the varied assemblage of aquatic birds that
swim today? Unlike mammals that have an expand-
ing fossil record for intermediate aquatic forms, the
fossil record for birds has been less forthcoming.
Although flying in air and swimming in water re-
quire the transfer of momentum in fluid media, dif-
ferences between the physical characteristics of the
two media (i.e., density, viscosity) require changes
in the propulsive systems for movement from air
to water. Long wingspans provide high lift produc-
tion in air, but in water wingspans need to be
shorter. Penguins have shorter and narrower wings
than flying birds of equivalent size, with a more
robust skeleton. Although having a wing structure
that permits aerial flight, various other seabirds
1292
partially fold the wing, modifying the configuration
with a reduced wingspan for underwater flight. This
shortening of the wingspan underwater reduces the
torque at the shoulder and loading on the bones in
the wing from pushing against the dense aquatic
medium. Alternatively, foot propulsion arose inde-
pendently in various lineages of diving birds
(Feduccia 1996).
The construction of a biomechanical model for
the evolution of swimming modes of aquatic birds
may permit the formulation of testable hypotheses
similar to the model proposed for aquatic mammals
(above). As with the evolution of aquatic mammals,
Gutmann (1994) proposed a pictorial sequence for
the evolution of swimming by penguins from a flying
bird, but gave no mechanism for the transitional
stage. Other authors have investigated the evolution
of flightlessness in penguins from fossils, morphol-
ogy, and genetics (Simpson 1946; Raikow et al. 1988;
Slack et al. 2006; Jadwiszczak 2009; Elliott et al.
2013), but have not developed a comprehensive
model for the evolution of swimming in birds.
The proposed model shows possible pathways to
the two most derived mechanisms of subsurface
swimming by birds (Fig. 6). These mechanisms in-
clude symmetrical subaqueous flight and hind feet
rowing. Symmetrical subaqueous flight is exemplified
by modern and ancient penguins (Sphenisciformes).
These aquatic birds are capable of swimming at
speeds of 1.7–3.2 m/s underwater (Clark and Bemis
1979; Bannasch 1994). This speed is high enough to
leap from the water and porpoise (i.e., make rapid
rhythmic serial leaps; Hui 1987). The motion of the
wings of penguins resembles that of flying birds with
lift generated throughout the stroke, but thrust is
produced over both the up- and downstrokes in pen-
guins (Clark and Bemis 1979). Thrust is derived
therefore through the generation of lift. Hind
feet rowing is the specialized swimming mode of
foot-propelled birds, including cormorants
(Phalacrocoracidae), grebes (Podicipedidae), loons
(Gaviidae), and the extinct Hesperornis. Without
use of the wings, the hind feet act as paddles and
are positioned lateral to the body as they are simul-
taneously swept rearward and forward in power and
recovery strokes, respectively (Lovvron 1991;
Feduccia 1996; Johansson and Norberg 2001, 2003;
Ribak et al. 2005). This resembles the drag-based
propulsive system that is typical of the asymmetrical
paddling of ducks (Anseriformes). However, in the
more specialized hind-feet rowers, lift-based symmet-
rical rowing can be used to produce higher levels of
thrust more efficiently than drag-based asymmetrical
paddling (Johansson and Norberg 2001). In the
F. E. Fish
Downloaded from https://academic.oup.com/icb/article/56/6/1285/2647100 by guest on 10 February 2024
Fig. 6 Model for sequence of swimming mode transitions from
flying to swimming birds. Winged swimming using symmetrical
subaqueous flight, as exemplified by penguins, had possible in-
termediate stages from winged paddling and/or plunge diving
through asymmetrical subaqueous flight, as exemplified by alcids.
Subsurface hind foot rowing, used by loons and grebes, is pre-
dicted to have gone through a hind foot paddling stage at the air-
water interface.
grebe (Podiceps cristatus), the asymmetrical design
of the foot and its kinematics produce lift-based pad-
dling (Johansson and Norberg 2000, 2001).
The ancestors of modern diving birds would ini-
tially have had winged aerial capabilities (Simpson
1946; Jadwiszczak 2009). The transition to aquatic
habits from volant birds would have had three pos-
sible routes: wing paddling, plunge diving, and hind
feet paddling (Fig. 6). Both wing paddling and
plunge diving are proposed to have developed into
asymmetrical subaqueous flight as a transitional stage
before the highly derived symmetrical subaqueous
flight of penguins, whereas hind feet paddling
would have led to hind feet rowing.
Wing paddling may have developed from birds
entering the water from flight or from the shoreline.
Bald eagles (Haliaeetus leucocephalus) are shown to
land in the water when trying to catch fish, and swim
by paddling the wings (e.g., https://www.youtube.
com/watch?v¼QCDJo4_WOAg; https://www.you-
tube.com/watch?v¼0gB6j1Csqxw). In this mode, the
bird swims with a power stroke as the wings are
adducted ventrally and caudally at the shoulder.
The area of the wing is reduced as it is slightly
flexed. The wings appear to contact the water parallel
to the surface. In the recovery stroke, the wings are
abducted and pulled out of the water. Alternatively,
wing paddling may have developed once the ances-
tral bird was already capable of swimming on the
water surface by hind feet paddling. Hind feet
Swimming evolution
paddling is augmented by wing paddling in eider
ducks (Somateria mollissima) and steamer ducks
(Tachyeres spp.) during rapid swimming (Livezey
and Humphrey 1983; Gough et al. 2015). The wing
paddling is referred to as ‘‘steaming’’ that mimics a
steamboat’s circular paddlewheel. Eider ducks and
steamer ducks are able to swim at speeds of 3.99
and 6.67 m/s, respectively, when steaming, which is
faster than swimming by hind feet paddling alone
(Livezey and Humphrey 1983; Gough et al. 2015).
From wing paddling, foraging underwater would
require a mechanism of winged propulsion in which
the wings are used for submerged swimming, but in
this transitional state also function for aerial flight
(Gill 2007). This dual-purpose wing is found in var-
ious pursuit diving birds that dive under the surface
of the water to prey on fish and invertebrates. Such
birds include the Alcidae (murres, auks, auklets, puf-
fins, guillemots) and Pelecanoididae (diving petrel;
Pennycuick 1987; Feduccia 1996; Watanuki et al.
2003) and represent the intermediate stage in the
evolution of flightless wing-propelled diving birds
(Raikow et al. 1988). The diving petrel
(Pelecanoides sp.) will actually swim through waves,
although some species can dive routinely to 25–40 m
and to a maximum depth of 83.1 m (Prince and
Jones 1992; Huin 1994; Zavalaga and Jahncke
1997). This subaqueous flight uses an up- and down-
stroke of partially folded wings to provide thrust
(Johansson and Aldrin 2002; Johansson 2003).
Thrust is generated mainly in the downstroke,
whereas the upstroke produces some thrust and a
downward-directed force on the body, opposed to
the positive buoyancy of the bird (Spring 1971;
Rayner 1985; Johansson and Aldrin 2002;
Johansson 2003; Watanuki et al. 2003, 2006). As
thrust production is not equivalent between the
up- and downstrokes in asymmetrical subaqueous
flight and the wings must be able to function in
both air and water, there are energetic consequences.
For example, flight costs in murres are 33% higher
than expected and dive costs are 30% higher than
expected for penguins of equivalent size (Elliott et al.
2013).
An alternate pathway to the asymmetrical sub-
aqueous flight mode is through plunge diving
(Fig. 6). Seabirds such as gannets and boobies
(Sulidae), pelicans (Pelecanidae), and some terns
(Sternidae) dive into the water after fish from a
height as high as 30 m above the surface of the
water (Lee and Reddish 1981). The momentum of
the dive drives the bird underwater to a depth of
0.3–12.6 m as it enters the water at up to 24 m/s
(Lee and Reddish 1981; Adams and Walter 1993;
1293
Ropert-Coudert et al. 2004). From the initial descent,
deeper dives down to 30 m and underwater pursuit
of fish are accomplished by active swimming (Adams
and Walter 1993; Garthe et al. 2000). The wings are
employed for active swimming in an asymmetrical
subaqueous flight (Adams and Walter 1993; Le
Corre 1997).
For foot-based swimmers, the transitional swim-
ming mode is envisioned to have started with hind
feet paddling. This drag-based swimming mode, al-
though effective for highly buoyant birds (i.e., most
Anseriformes), presents limitations to speed and ef-
Downloaded from https://academic.oup.com/icb/article/56/6/1285/2647100 by guest on 10 February 2024
ficiency when swimming at the air-water interface
(Aigeldinger and Fish 1995; Fish 2000; Gough et al.
2015). This method of swimming relies on alternate
strokes of the hind feet, which have interdigital web-
bing or fringes that increase the propulsive surface
area to affect a larger mass of water. However, the
efficiency of the paddling stroke remains low due to
the increased drag and lack of thrust on the recovery
stroke. As birds moved to underwater swimming,
surface effects were negated (i.e., wave drag, hull
speed). Once underwater, swimming shifted from al-
ternate paddling to simultaneous hind feet rowing
(Fig. 6). Cormorants swim on the surface using al-
ternate paddling strokes of the feet but swim under-
water by stroking with both feet simultaneously
(Lovvron 1991; Schmid et al. 1995; Ancel et al.
2000; Ribak et al. 2005). Simultaneous rowing per-
mits rapid bouts of thrust production interspersed
with gliding phases in the stroke cycle (Johansson
and Norberg 2001; Ribak et al. 2005). This burst-
and-glide gait is associated with energy savings in
swimming over a given distance, thereby increasing
propulsive efficiency (Ribak et al. 2005).
Furthermore, in specialized foot-propelling aquatic
birds, the feet can produce lift-based thrust
(Johansson and Norberg 2001).
Regardless of the final swimming mode in aquatic
birds, whether wing-based or foot-based, the selec-
tion forces were probably centered on increasing
swimming performance. Increasing speed and effi-
ciency would dominate the transition toward the de-
rived lift-based swimming modes. Intermediate
forms were energetically most precarious with high
locomotor costs for both flight and swimming
(Williams 1999; Fish 2000; Elliott et al. 2013).
Transition from aerial flight to the high-performance
propulsive modes for submerged swimming was
allied with morphological and physiological adapta-
tions (Kooyman 1989; Ksepka and Ando; Elliott et
al. 2013; Ponganis 2015). Movement into water
would have necessitated increased insulation against
the high thermal conductivity of the aquatic medium
1294
by waterproof and densely-packed feathers (Ksepka
and Ando 2011). This increased insulation would
have provided enhanced positive buoyancy at the
water surface, but would have been a disadvantage
in submerged swimming. As birds swam underwater,
propulsion by wings or feet would have produced
thrust as well as a downward force to counter the
increased buoyancy. Greater subsurface swimming
specialization would have included reduction of
wingspan or loss of wings, stiffening of wing joints,
increasing density of the bones and body mass, en-
hanced diving capabilities, and a streamlined body
(Raikow et al. 1988; Bannasch 1995; Ksepka and
Ando; Elliott et al. 2013; Ponganis 2015). With
these adaptations and the possible pathways hypoth-
esized in the model, aquatic birds evolved various
solutions for efficient high-speed swimming that
could function at depth.
Unanswered questions
Despite the evidence that supports these models for
aquatic mammals and birds, problems still exist that
have not been fully resolved. The models do not
address the ultimate causalities for why these animals
moved to the water in the first place. Initial swim-
ming would have been slow and inefficient compared
with walking or flying. Escape from predators would
be a possible reason for the first forays into water.
New resources such as food would also have had a
major impact on why these animals moved into
water (Domning 2001b; Berta 2012; Haidr and
Acosta Hospitaleche 2012). High-performance swim-
ming would have been strongly selected for to pursue
elusive prey and reduce transit time to foraging
areas. More efficient swimming allows foraging
trips to be energetically more productive (Hui 1988).
The fossil record for aquatic mammals is still in-
complete. Although there are a number of cetacean
fossils indicating the use of oscillations of the tail for
propulsion, there are no fossilized imprints of the
caudal flukes to correlate with skeletal changes
toward high-performance swimming. Such imprints
are preserved for some fish and ichthyosaurs
(McGowan 1991; Long 1995), but are not known
for cetaceans as the matrix surrounding the skeletal
remains is typically too coarse to preserve an imprint
(J.G.M. Thewissen, personal communication). A
number of questions are unresolved for the pinni-
peds due to a lack of transitional forms. For phocids
and odobenids, there are no distinct fossil interme-
diate forms or modern analogs for a laterally-undu-
lating hind-flipper-propelled swimmer. However,
Berta et al. (1989) noted that the lumbar vertebrae
F. E. Fish
in the early fossil pinniped Enaliarctos allowed swim-
ming by lateral movements of the trunk along with
propulsion by the limbs. The only modern semi-
aquatic mammalian swimmers that laterally undulate
are the African otter shrew (Potamogale) and the
muskrat (Ondatra), but these semiaquatic mammals
only undulate the tail (Fish 1996). Similarly, the
otariids have a gap in their evolutionary history be-
tween paddling and foreflipper oscillation. Although
Enaliarctos may have filled this gap, the structure of
its flippers suggests a morphology that is more ad-
vanced than a paddle-propelling translational pinni-
Downloaded from https://academic.oup.com/icb/article/56/6/1285/2647100 by guest on 10 February 2024
ped. For modern analogs, the platypus
(Ornithorhynchus) swims by forelimb paddling, but
the animal uses alternating motion of the contralat-
eral paddles and the limbs are rotated so that the
plantar surface of the foot is facing dorsally (Fish
2000). Furthermore, there is little information on
the swimming modes of the extinct aquatic sloth
(Thalassocnus) and desmostylians (de Muizon and
McDonald 1995; Berta 2012), though at least the
latter have been regarded as alternate pectoral pad-
dlers such as polar bears (Domning 2002).
Until more fossil material becomes available, the
evolution of swimming modes in birds may remain
as controversial as the origin of flight (Feduccia
1996; Dial 2003). Early aquatic and fish-eating
birds from the Cretaceous were represented by the
Hesperornithiformes (Hesperornis) and
Ornithuromorpha (Ichthyornis). Hesperornis was
flightless and aquatic, using hind foot propulsion,
but it was not related to other birds using a similar
mode of swimming (Feduccia 1996). Ichthyornis was
tern-like, but although able to fly, it gives no indi-
cation of swimming capabilities (Feduccia 1996). For
now, further analysis of the mechanics and energetics
of modern aquatic birds may provide evidence to
support the model (Lovvron 1991; Elliott et al. 2013)
Acknowledgments
I would like to thank Alexandra Houssaye for per-
suading me to co-sponsor this symposium. I am also
grateful to Danielle Adams and William Gough for
reviewing an earlier version of this article.
Funding
None.
References
Adams NJ, Walter CB. 1993. Diving depths of Cape gannets.
Condor 95:734–6.
Swimming evolution
Aigeldinger TL, Fish FE. 1995. Hydroplaning by ducklings:
overcoming limitations to swimming at the water surface.
J Exp Biol 198:1567–74.
Aleyev YG. 1977. Nekton. The Hague: Junk.
Ancel A, Starke LN, Ponganis PJ, Van Dam R, Kooyman GL.
2000. Energetics of surface swimming in Brandt’s cormo-
rants (Phalacrocorax penicillatus Brandt). J Exp Biol 203:
3727–31.
Bajpai S, Thewissen JGM. 2000. A new, diminutive Eocene
whale from Kachchh (Gujarat, India) and its implications
for locomotor evolution of cetaceans. Curr Sci 79:1478–82.
Bannasch R. 1994. Functional anatomy of the ‘‘flight’’
apparatus in penguins. In: Maddock L, Bone Q, Rayner
JMV, editors. Mechanics and physiology of animal
swimming. Cambridge: Cambridge University Press.
p. 163–92.
Bannasch R. 1995. Hydrodynamics of penguins – an experi-
mental approach. In: Dann P, Norman I, Reilly P, editors.
The penguins: ecology and management. Chipping Norton,
NSW: Surrey Beatty. p. 140–76.
Barnes LG, Domning DP, Ray CE. 1985. Status of studies on
fossil marine mammals. Mar Mamm Sci 1:15–53.
Berta A. 2012. Return to the sea. Berkeley: University of
California Press.
Berta A, Ray CE, Wyss AR. 1989. Skeleton of the oldest
known pinniped Enaliarctos mealsi. Science 244:60–2.
Berta A, Ray CE. 1990. Skeletal morphology and locomotor
capabilities of the archaic pinniped Enaliarctos mealsi.
J Vert Paleont 10:141–57.
Castellini MA, Mellish J-A. 2016. Marine mammal physiology.
Boca Raton, FL: CRC Press.
Clark BD, Bemis W. 1979. Kinematics of swimming of pen-
guins at the Detroit Zoo. J Zool 188:411–28.
Dagg AI, Windsor DE. 1972. Swimming in northern terres-
trial mammals. Can J Zool 50:117–30.
Daniel TL, Webb PW. 1987. Physical determinants of loco-
motion. In: Dejours P, Bolis L, Taylor CR, Weibel ER,
editors. Comparative physiology: life in water and on
land. Berlin: Liviana. p. 343–69.
Davis WB. 1942. Swimming ability of two small mammals.
J Mamm 23:99.
de Muizon C, McDonald HG. 1995. An aquatic sloth m the
Pliocene of Peru. Nature 375:224–7.
Dial KP. 2003. Wing-assisted incline running and the evolu-
tion of flight. Science 299:402–4.
Domning DP. 1976. An ecological model for late Tertiary
sirenian evolution in the North Pacific Ocean. Syst Zool
25:352–62.
Domning DP. 2001a. The earliest known fully quadrupedal
sirenian. Nature 413:625–7.
Domning DP. 2001b. Sirenians, seagrasses, and Cenozoic eco-
logical change in the Caribbean. Palaeogeogr Palaeocl
Palaeoecol 122:27–50.
Domning DP. 2002. The terrestrial posture of desmostylians.
In: Emry RJ, editor. Cenozoic mammals of land and sea:
tributes to the career of Clayton E. Ray. Smithson Contr
Paleobiol 93:99–111.
Elliott KH, Ricklefs RE, Gaston AJ, Hatch SA, Speakman JR,
Davoren GK. 2013. High flight costs, but low dive costs, in
auks support the biomechanical hypothesis for flightlessness
in penguins. Proc Nat Acad Sci 110:9380–4.
1295
Feduccia A. 1996. The origin and evolution of birds. New
Haven: Yale University Press.
Feldkamp SD. 1987a. Swimming in the California sea
lion: morphometrics, drag and energetics. J Exp Biol
131:117–35.
Feldkamp SD. 1987b. Foreflipper propulsion in the
California sea lion, Zalophus californianus. J Zool Lond
212:43–57.
Fish FE. 1979. Thermoregulation in the muskrat (Ondatra
zibethicus): the use of regional heterothermia. Comp
Biochem Physiol A 64:391–7.
Fish FE. 1992. Aquatic locomotion. In: Tomasi T, Horton T,
editors. Mammalian energetics: interdisciplinary views of
metabolism and reproduction. Ithaca: Cornell University
Downloaded from https://academic.oup.com/icb/article/56/6/1285/2647100 by guest on 10 February 2024
Press. p. 34–63.
Fish FE. 1993a. Influence of hydrodynamic design and pro-
pulsive mode on mammalian swimming energetics. Aust J
Zool 42:79–101.
Fish FE. 1993b. Power output and propulsive efficiency of
swimming bottlenose dolphins (Tursiops truncatus). J Exp
Biol 185:179–93.
Fish FE. 1993c. Comparison of swimming kinematics between
terrestrial and semiaquatic opossums. J Mamm 74:275–84.
Fish FE. 1994. Association of propulsive swimming mode
with behavior in river otters (Lutra canadensis). J Mamm
75:989–97.
Fish FE. 1995. Kinematics of ducklings swimming in
formation: energetic consequences of position. J Exp Zool
272:1–11.
Fish FE. 1996. Transitions from drag-based to lift-based pro-
pulsion in mammalian swimming. Amer Zool 36:628–41.
Fish FE. 1998a. Comparative kinematics and hydrodynamics
of odontocete cetaceans: morphological and ecological
correlates with swimming performance. J Exp Biol
201:2867–77.
Fish FE. 1998b. Biomechanical perspectives on the origin of
cetacean flukes. In: Thewissen JGM, editor. The emergence
of whales. New York: Plenum. p. 303–24.
Fish FE. 2000. Biomechanics and energetics in aquatic and
semiaquatic mammals: platypus to whale. Physiol
Biochem Zool 73:683–98.
Fish FE. 2001. Mechanism for evolutionary transition in
swimming mode by mammals. In: Mazin J-M, Vignaud
P, de Buffrénil V, editors. Secondary adaptation of tetra-
pods to life in water. München: Verlag Dr. Friedrich Pfeil.
p. 26187.
Fish FE. 2004. Structure and mechanics of nonpiscine control
surfaces. IEEE J Ocean Eng 29:605–21.
Fish FE, Innes S, Ronald K. 1988. Kinematics and estimated
thrust production of swimming harp and ringed seals.
J Exp Biol 137:157–73.
Fish FE, Stein BR. 1991. Functional correlates of differences in
bone density among terrestrial and aquatic genera in the
family Mustelidae (Mammalia). Zoomorphology
110:339–45.
Fish FE, Hui CA. 1991. Dolphin swimming - a review. Mamm
Rev 21:181–95.
Fish FE, Baudinette RV, Frappell P, Sarre M. 1997. Energetics
of swimming by the platypus (Ornithorhynchus anatinus):
metabolic effort associated with rowing. J Exp Biol
200:2647–52.
1296
Fish FE, Baudinette RV. 1999. Energetics of locomotion by
the Australian water rat (Hydromys chrysogaster): compari-
son of swimming and running in a semiaquatic mammal.
J Exp Biol 202:353–63.
Fish FE, Smelstoys J, Baudinette RV, Reynolds PS. 2002. Fur
doesn’t fly, it floats: buoyancy of hair in semi-aquatic
mammals. Aqu Mamm 28.2:103–12.
Fish FE, Goetz KT, Rugh DJ, Brattström LV. 2013.
Hydrodynamic patterns associated with echelon formation
swimming by feeding bowhead whales (Balaena mysticetus).
Mar Mamm Sci 29:E498–507.
Flower WH. 1883. On whales, present and past and their
probable origin. Nature 28:226–30.
Fordyce RE. 1992. Cetacean evolution and Eocene/Oligocene
environments. In: Prothero DR, Berggren WA, editors.
Eocene-Oligocene climatic and biotic evolution.
Princeton: Princeton University Press. p. 368–81.
Garthe S, Benvenuti S, Montevecchi WA. 2000. Pursuit
plunging by northern gannets (Sula bassana) feeding on
capelin (Mallotus villosus). Proc Roy Soc Lond B
267:1717–22.
Gill FB. 2007. Ornithology. New York: Freeman.
Gingerich PD. 2015. Evolution of whales from land to sea. In:
Dial KP, Shubin N, Brainerd EL, Editors. Great transfor-
mation in vertebrate evolution. Chicago: Chicago
University Press. p. 239–56.
Gingerich PD, Wells NA, Russell DE, Shah SI. 1983. Origin of
whales in epicontinental remnant seas: new evidence from
the early Eocene of Pakistan. Science 220:403–6.
Gingerich PD, Smith BH, Simons EL. 1990. Hind limbs of
Eocene Basilosaurus: evidence of feet in whales. Science
249:154–7.
Gingerich PD, Raza SM, Arif M, Anwar M, Zhou XY. 1994.
New whale from the Eocene of Pakistan and the origin of
cetacean swimming. Nature 368:844–7.
Gingerich PD, ul Haq M, Zalmout IS, Khan IH, Malkani MS.
2001. Origin of whales from early artiodactyls: hands and
feet of Eocene Protocetidae from Pakistan. Science 293:
2239–42.
Gingerich PD, von Koenigswald W, Sanders WJ, Smith BH,
Zalmout IS. 2009. New protocetid whale from the middle
Eocene of Pakistan: birth on land, precocial development,
and sexual dimorphism. PLoS ONE 4:e4366.
Goslow GE, Dial KP, Jenkins FA. 1989. The avian shoulder:
an experimental approach. Am Zool 29:287–301.
Gough WT, Farina SC, Fish FE. 2015. Aquatic burst locomo-
tion by hydroplaning and running in common eiders
(Somateria mollissima). J Exp Biol 218:1632–8.
Grillner S. 1975. Locomotion in vertebrates: central mecha-
nisms and reflex interactions. Physiol Rev 55:247–304.
Grillner S. 1985. Neurobiological bases of rhythmic motor
acts in vertebrates. Science 228:143–9.
Grillner S. 1996. Neural networks for vertebrate locomotion.
Sci Am 274:64–9.
Gutmann WF. 1994. Konstruktionszwänge in der Evolution:
schwimmende Vierfüsser. Natur Mus 124:165–88.
Haidr N, Acosta Hospitaleche C. 2012. Feeding habits of
Antarctic Eocene penguins from a morpho-functional per-
spective. N Jb Geol Paläont Abh 263:125–31.
Hertel H. 1966. Structure, form, movement. New York:
Reinhold.
F. E. Fish
Hickman GC. 1979. The mammalian tail: a review of func-
tions. Mamm Rev 9:143–57.
Ho CY-K, Prager EM, Wilson AC, Osuga DT, Feeney RE.
1976. Penguin evolution: protein comparisons demonstrate
phylogenetic relationship to flying aquatic birds. J Mol Evol
8:271–82.
Howell AB. 1937. The swimming mechanism of the platypus.
J Mamm 18:217–22.
Hui CA. 1987. The porpoising of penguins: an energy-con-
serving behavior for respiratory ventilation? Can J Zool
65:209–11.
Hui CA. 1988. Penguin swimming. II. Energetics and behav-
ior. Physiol Zool 61:344–50.
Huin N. 1994. Diving depths of white-chinned petrels.
Downloaded from https://academic.oup.com/icb/article/56/6/1285/2647100 by guest on 10 February 2024
Condor 96:111–13.
Jadwiszczak P. 2009. Penguin past: the current state of knowl-
edge. Pol Polar Res 30:3–28.
Jenkins FA, Goslow GE. 1983. The functional anatomy of the
shoulder of the savannah monitor lizard (Varanus exanthe-
maticus). J Morph 175:195–216.
Johansson LC. 2003. Indirect estimates of wing-propulsion
forces in horizontally diving Atlantic puffins (Fratercula
arctica L.). Can J Zool 81:816–22.
Johansson LC, Norberg UML. 2000. Asymmetric toes aid un-
derwater swimming. Nature 407:582–3.
Johansson LC, Norberg UML. 2001. Lift-based paddling in
diving grebe. J Exp Biol 204:1687–96.
Johansson LC, Aldrin BS. 2002. Kinematics of diving Atlantic
puffins (Fratercula arctica L.): evidence for an active up-
stroke. J Exp Biol 205:371–8.
Johansson LC, Norberg RÅ. 2003. Delta-wing function of
webbed feet gives hydrodynamic lift for swimming propul-
sion in birds. Nature 424:65–8.
Kenyon KW. 1969. The sea otter in the eastern Pacific Ocean.
Am Fauna 68:1–352.
Kooyman GL. 1973. Respiratory adaptations in marine mam-
mals. Am Zool 13:457–68.
Kooyman GL. 1989. Diverse divers: physiology and behavior.
Berlin: Springer.
Ksepka DL, Ando T. 2011. Penguins past, present, and future:
trends in the evolution of the Sphenisciformes. In: Dyke G,
Kaiser G, editors. The evolutionary history of modern
birds. West Sussex: Wiley. p. 156–86.
Le Corre M. 1997. Diving depths of two tropical
Pelecaniformes: the red-tailed tropicbird and the red-
footed booby. Condor 99:1004–7.
Lee DN, Reddish PE. 1981. Plummeting gannets: a paradigm
of ecological optics. Nature 293:293–4.
Livezey BC, Humphrey PS. 1983. Mechanics of steaming in
steamer-ducks. Auk 100:485–8.
Long JA. 1995. The rise of fishes. Baltimore: Johns Hopkins
University Press.
Lovvron JR. 1991. Mechanics of underwater swimming in
foot propelled diving birds. Proc Int Ornithol Congr
20:1868–74.
Madar SI. 2007. The postcranial skeleton of early Eocene
pakicetid cetaceans. J Paleont 8:176–200.
McGowan C. 1991. Dinosaurs, spitfires, & sea dragons.
Cambridge: Harvard University Press.
Mizelle JD. 1935. Swimming of the muskrat. J Mamm
16:22–5.
Swimming evolution
Noren SR, Williams TM, Pabst DA, McLellan WA, Dearolf JL.
2001. The development of diving in marine endotherms:
preparing the skeletal muscles of dolphins, penguins, and
seals for activity during submergence. J Comp Physiol B
171:127–34.
Pennycuick CJ. 1987. Flight of auks (Alcidae) and other north-
ern seabirds compared with southern Procellariiformes:
Ornithodolite observations. J Exp Biol 128:335–47.
Ponganis PJ. 2015. Diving physiology of marine mammals
and seabirds. Cambridge: Cambridge University Press.
Prince PA, Jones M. 1992. Maximum dive depths attained by
South Georgia diving petrel Pelecanoides georgicus at Bird
Island, South Georgia. Antarct Sci 4:433–4.
Qiang J, Luo Z-X, Yuan C-X, Tabrum AR. 2006. A swimming
mammaliaform from the Middle Jurassic and ecomorpholo-
gical diversification of early mammals. Science 311: 1123–7.
Raikow RJ, Bicanovsky L, Bledsoe AH. 1988. Forelimb joint
mobility and the evolution of wing-propelled diving in
birds. Auk 100:446–51.
Rayner JMV. 1985. Vorticity and propulsion mechanics in
swimming and flying animals. In: Riess J, Frey E,
editors. Konstruktionsprinzipen lebender und ausgestorbener
Reptilien. Tubingen, FRG: University of Tubingen. p. 89–118.
Repenning CA. 1976. Advances in systematics of marine
mammals. Syst Zool 25:301–436.
Ribak G, Weihs D, Arad Z. 2005. Submerged swimming of
the great cormorant Phalacrocorax carbo sinensis is a variant
of the burst-and-glide gait. J Exp Biol 208:3835–49.
Ropert-Coudert Y, Grémillet D, Ryan P, Kato A, Naito Y, Le
Maho Y. 2004. Between air and water: the plunge dive of
the Cape Gannet Morus capensis. Ibis 146:281–90.
Rue LL. III. 1964. The world of the beaver. Philadelphia: J. B.
Lippincott Co.
Rybczynski N, Dawson MR, Tedford RH. 2009. A semi-aqua-
tic Arctic mammalian carnivore from the Miocene epoch
and origin of Pinnipedia. Nature 458:1021–4.
Savage RJG. 1957. The anatomy of Potamotherium, an
Oligocene lutrine. Proc Zool Soc Lond 129:151–244.
Schmid D, Grémillet DJ, Culik BM. 1995. Energetics of un-
derwater swimming in the great cormorant (Phalacrocorax
carbo sinensis). Mar Biol 123:875–81.
Simpson GG. 1946. Fossil penguins. Bull Amer Mus Nat Hist
87:1–99.
Slack KE, Jones CM, Ando T, Harrison GA, Fordyce RE,
Arnason U, Penny D. 2006. Early penguin fossils, plus mi-
tochondrial genomes, calibrate avian evolution. Mol Biol
Evol 23:1144–55.
Smith KK. 1994. Are neuromotor systems conserved in evo-
lution? Brain Behav Evol 43:293–305.
Spring L. 1971. A comparison of functional and morpholog-
ical adaptations in the common murre (Uria aalge) and
thick-billed murre (Uria lomvia). Condor 73:1–27.
Stein BR. 1981. Comparative limb myology of two opossums,
Didelphis and Chironectes. J Morph 169:113–40.
Stein BR. 1989. Bone density and adaptation in semiaquatic
mammals. J Mamm 70:467–76.
Stein PSG, Victor JC, Field EC, Currie SN. 1995. Bilateral
control of hindlimb scratching in the spinal turtle: contra-
lateral spinal circuitry contributes to normal ipsilateral
motor pattern of fictive rostral scratching. J Neurosci
15:4343–55.
1297
Tarasoff FJ, Bisaillon A, Pierard J, Whitt AP. 1972.
Locomotory patterns and external morphology of the
river otter, sea otter, and harp seal (Mammalia). Can J
Zool 50:915–29.
Thewissen JGM. 2014. The walking whales. Berkeley:
University of California Press.
Thewissen JGM, Hussain ST, Arif M. 1994. Fossil evidence for
the origin of aquatic locomotion in archaeocete whales.
Science 263:210–1.
Thewissen JGM, Fish FE. 1997. Locomotor evolution in the
earliest cetaceans: functional model, modern analogues, and
paleontological evidence. Paleobiology 23:482–90.
Thewissen JGM, Bajpai S. 2001. Whale origins as a poster
child for macroevolution. BioScience 51:1037–49.
Downloaded from https://academic.oup.com/icb/article/56/6/1285/2647100 by guest on 10 February 2024
Thewissen JGM, Williams EM, Roe LJ, Hussain ST. 2001.
Skeletons of terrestrial cetaceans and the relationship of
whales to artiodactyls. Nature 413:277–81.
Thewissen JGM, Cooper LN, Clementz MT, Bajpai S, Tiwari
BN. 2007. Whales originated from aquatic artiodactyls in
the Eocene epoch of India. Nature 450:1190–4.
Vogel S. 1994. Life in moving fluids. Princeton: Princeton
University Press.
Watanuki Y, Niizuma Y, Geir WG, Sato K, Naito Y. 2003.
Stroke and glide of wing–propelled divers: deep diving sea-
birds adjust surge frequency to buoyancy change with
depth. Proc Roy Soc Lond B 270:483–8.
Watanuki Y, Wanless S, Harris M, Lovvorn JR, Miyazaki M,
Tanaka H, Sato K. 2006. Swim speeds and stroke patterns
in wing-propelled divers: a comparison among alcids and a
penguin. J Exp Biol 209:1217–30.
Webb PW. 1975. Hydrodynamics and energetics of fish pro-
pulsion. Bull Fish Res Bd Can 190:1–158.
Webb PW. 1988. Simple physical principles and vertebrate
aquatic locomotion. Am Zool 28:709–25.
Webb PW, de Buffrénil V. 1990. Locomotion in the biology
of large aquatic vertebrates. Trans Am Fish Soc 119:629–41.
Williams TM. 1983. Locomotion in the North American
mink, a semi-aquatic mammal. I. Swimming energetics
and body drag. J Exp Biol 103:155–68.
Williams TM. 1989. Swimming by sea otters: adaptations for
low energetic cost locomotion. J Comp Physiol A 164:
815–24.
Williams TM. 1999. The evolution of cost efficient swimming
in marine mammals: limits to energetic optimization.
Philos Trans Roy Soc Lond B 353:1–9.
Williams TM, Friedl WA, Fong ML, Yamada RM, Sedivy P,
Haun JE. 1992. Travel at low energetic cost by swimming
and wave-riding bottlenose dolphins. Nature 355:821–3.
Williams TM, Davis RW. 1995. Emergency care and rehabil-
itation of oiled sea otters: a guide for oil spills involving
fur-bearing marine mammals. Fairbanks: University of
Alaska Press.
Wolfe JL, Esher RJ. 1981. Effects of crude oil on swimming
behavior and survival in the rice rat. Environ Res 26:486–9.
Wyss AR. 1988. Evidence from flipper structure for a single
origin of pinnipeds. Nature 334:427–8.
Wyss AR. 1989. Flippers and pinniped phylogeny: has the
problem of convergence been overrated? Mar Mamm Sci
5:343–60.
Zavalaga CB, Jahncke J. 1997. Maximum dive depths of the
Peruvian diving-petrel. Condor 99:1002–4.