Anatomical Adaptations of Aquatic

Mammals
JOY S. REIDENBERG
*
Center for Anatomy and Functional Morphology, Department of Medical Education,
Mount Sinai School of Medicine, New York, New York
ABSTRACT
This special issue of the Anatomical Record explores many of the an-
atomical adaptations exhibited by aquatic mammals that enable life in
the water. Anatomical observations on a range of fossil and living marine
and freshwater mammals are presented, including sirenians (manatees
and dugongs), cetaceans (both baleen whales and toothed whales, includ-
ing dolphins and porpoises), pinnipeds (seals, sea lions, and walruses),
the sea otter, and the pygmy hippopotamus. A range of anatomical sys-
tems are covered in this issue, including the external form (integument,
tail shape), nervous system (eye, ear, brain), musculoskeletal systems
(cranium, mandible, hyoid, vertebral column, ipper/forelimb), digestive
tract (teeth/tusks/baleen, tongue, stomach), and respiratory tract (larynx).
Emphasis is placed on exploring anatomical function in the context of
aquatic life. The following topics are addressed: evolution, sound produc-
tion, sound reception, feeding, locomotion, buoyancy control, thermoregu-
lation, cognition, and behavior. A variety of approaches and techniques
are used to examine and characterize these adaptations, ranging from
dissection, to histology, to electron microscopy, to two-dimensional (2D)
and 3D computerized tomography, to experimental eld tests of function.
The articles in this issue are a blend of literature review and new, hy-
pothesis-driven anatomical research, which highlight the special nature
of anatomical form and function in aquatic mammals that enables their
exquisite adaptation for life in such a challenging environment. 2007
Wiley-Liss, Inc. Anat Rec, 290:507513, 2007. 2007 Wiley-Liss, Inc.
Key words: aquatic; adaptation; anatomy; marine mammal;
sirenian; cetacean; pinniped; evolution
Aquatic life poses many challenges for mammals that
were originally adapted for life on land. As the evolution-
ary process of natural selection can only apply to modify-
ing present structures, aquatic mammals bring a lot of
terrestrial baggage to their aquatic existence. For one
thing, they do not breathe water as sh do. Therefore, re-
spiratory tract modications are necessary to protect a
system designed to function in air while excluding the
ever-present surrounding water. Many of these adapta-
tions have been previously described, for example, valvu-
lar nostrils that exclude water, and an intranarial larynx
(Reidenberg and Laitman, 1987) that further protects
the respiratory tract from water inundation during swal-
lowing. Diving presents additional challenges, as ambi-
ent pressure rises with increased depth. Lung volumes
collapse under the high pressures of a deep dive (Boyd,
1975; Ridgway and Howard, 1979). A jointed, collapsible
rib cage allows compression of the thorax to accommo-
date the shrinking lungs. Skeletal muscles are adapted
to maintain low levels of aerobic metabolism under the
hypoxic conditions associated with diving (Kanatous
*Correspondence to: Joy S. Reidenberg, Center for Anatomy
and Functional Morphology, Department of Medical Education,
Mail Box 1007, Mount Sinai School of Medicine, 1 Gustave L.
Levy Place, New York, NY 10029-6574.
E-mail: joy.reidenberg@mssm.edu
Received 13 March 2007; Accepted 13 March 2007
DOI 10.1002/ar.20541
Published online in Wiley InterScience (www.interscience.wiley.
com).
2007 WILEY-LISS, INC.
THE ANATOMICAL RECORD 290:507513 (2007)
et al., 2002). Elevated levels of myoglobin in skeletal
muscles also increase oxygen retention, thus enabling
longer dive times between breaths (Noren et al., 2001;
Wright and Davis, 2006). The mass of blood vessels
located in the dorsum of the thorax (retia thoracica) have
been proposed to function during diving to accommodate
for the collapsed lung volume, thereby preventing gross
displacement of abdominal organs (Hui, 1975). Salinity
presents another challenge, as marine mammals must
main water and salt balance, despite the frequent inux
of salt water they consume while swallowing prey. The
kidney structure of cetaceans (whales, including dolphins
and porpoises) and pinnipeds (seals, sea lions, walruses)
is unusual, having a reniculate structure (Abdelbaki
et al., 1984; Henk et al., 1986) not found in any other ter-
restrial mammals except bears, but does not appear to
have a greater ability to concentrate urine (Ortiz, 2001).
Rather, the apparent advantage of numerous independ-
ent renicules in marine mammals is limited tubule
lengths in the necessarily large kidneys of gigantic mam-
mals (Maluf and Gassman, 1998).
Navigation and prey detection systems are also modi-
ed. As many aquatic mammals need to hunt at night
or in turbid or deep water, their sensory systems have
accordingly evolved. Pinnipeds developed longer and
more sensitive vibrissae that can pick up hydrodynamic
trails (vibrations in water) of sh swimming, or relay in-
formation about water current ow and variations in
substrate surfaces (Dehnhardt et al., 2001). Odontocetes
(toothed whales) developed nasal structures that gener-
ate echolocation, enabling them to use sound to locate
prey or navigate past obstacles (Cranford et al., 1996;
Au et al., 2006).
Many marine mammals have modied their external
shape, developing new propulsion mechanisms for loco-
motion in water. Seals use alternating horizontal sweeps
of their hind ippers (Fish et al., 1988). Fur seals and
sea lions y underwater by beating their fore ippers
(English, 1977; Feldkamp, 1987). Walruses sometimes
use their tusks to grip the sea oor or ice and push their
body forward with a downward nod of the head. Sire-
nians (manatees and dugongs) have lost their hind
limbs, but can either propel themselves with their tail
uke(s) or walk along the sea or river oor with their
forelimbs. Cetaceans have excelled in the attainment of
streamlined form, and are thus the fastest swimmers.
As with sirenians, cetaceans have lost appendages that
detract from axial locomotion (hind limbs). Similarly to
pinnipeds, they have modied extremities that assist
with lift and braking (ippers). Cetaceans have also
added new extensions that aid propulsion (ukes) or pre-
vent roll or yaw (dorsal n) while swimming with exag-
gerated pitch (dorsoventral bending).
Although most of the above-mentioned adaptations
have been discussed at length in previous publications,
the articles in this special issue present some new nd-
ings regarding aquatic adaptations. This special issue
focuses on a common hypothesis: the described anatomi-
cal specialization confers a selective advantage to an
aquatic existence. Demonstrating this relationship neces-
sarily involves exploring how the adaptation functions in
an aquatic environment. The studies presented examine
a large array of extant and fossil, marine and fresh
water, aquatic mammals. A variety of anatomical sys-
tems are explored, including digestive tract (teeth, tusks,
baleen, tongue, pharyngeal spaces, stomach), the exter-
nal form (integument and body shape, including ukes
and ippers), musculoskeletal systems (cranial, mandib-
ular, and cervical regions; postcranial axial and appen-
dicular skeleton), nervous system (eye, ear, brain), and
respiratory tract (larynx). Emphasis is placed on explor-
ing anatomical function in the context of aquatic life. A
range of techniques are used, including dissection, histol-
ogy, electron microscopy, computerized tomography and
3D reconstructions, and experimental eld work. The
papers that follow in this issue are a blend of both review
articles and new, hypothesis-driven anatomical research.
These studies highlight the dramatic anatomical changes
seen in the evolution from fossil ancestors to extant
aquatic mammals. This special issue is a tribute to the
unique anatomical forms and functions of aquatic mam-
mals that enables their adaptation to life underwater.
UNDERWATER FORAGING
The rst question that naturally comes to mind is
Why did some mammals become aquatic in the rst
place? Uhen (2007, this issue) discusses the evolution of
aquatic mammals, using both molecular and morphologi-
cal data for Cetacea, Sirenia, Desmostylia, and Pinnipe-
dia. He notes that re-entering the water occurred on at
least seven different occasions. Specic changes occurred
in the axial and appendicular skeleton that improved
locomotion for aquatic foraging. Nostril, eye placement,
rostrum, and dental morphology also changed, depend-
ing upon the need to forage while wading versus sub-
mersion. Although the end product of each of these evo-
lutionary trajectories is vastly different, they all appear
to be the result of natural selection for improved aquatic
foraging. Terrestrial mammals from seven separate line-
ages thus re-invaded the water to ll a vacant niche:
feeding in water.
The foraging mechanisms of fossil ancestors, however,
do not always match present day species. Domning and
Beatty (2007, this issue) compare fossil and modern
dugongs in their tusk shape and cranial anatomy, and
explore whether these specializations indicate tusk use
in feeding. Fossil dugongines exhibit cranial modica-
tions that may have assisted downward and backward
tusk cutting motions. The larger, more blade-like tusks
of fossil dugongines are more effective at harvesting rhi-
zomes. However, examination of microwear patterns in
modern dugong tusks do not support that their use is
necessary in feeding, although it does occasionally occur
in large adult males. Tusk use in modern dugongs has
thus changed radically from the ancestral pattern. As
tusks are not essential for feeding in extant dugongs, the
persistence of erupted tusks in males indicates a possible
role in sexual selection or other social interactions.
Feeding mechanisms are also examined in cetaceans in
this issue. MacLeod et al. (2007, this issue) describe the
relationship between prey size and skull asymmetry.
While most mammals are bilaterally symmetrical, most
odontocetes are characterized by directional asymmetry
of the skull (i.e., the direction of deviation is consistent).
The narial apertures are asymmetrically positioned on
the left side of the head (Yurick and Gaskin, 1988). Above
the skull, this asymmetry is also evident in soft tissue
structures that are used in generating echolocation sig-
nals (Cranford et al., 1996). The different sized nasal
508 REIDENBERG
diverticulae, fat bodies, and valvular aps may enable
generation of two different sounds simultaneously. While
this asymmetry may be useful for echolocation signal gen-
eration, it is suggested that echolocation is an overlay on
asymmetry developed initially in conjunction with feeding
needs. Below the skull, the left-shifted nares correspond
to a left-shifted larynx. A larynx positioned asymmetri-
cally on the left side collapses the left piriform sinus (lat-
eral food channel, but simultaneously provides a larger
piriform sinus on the right side; Reidenberg and Laitman,
1994). This should enable asymmetric odontocetes to
swallow larger prey than their symmetric counterparts.
MacLeod et al. (2007, this issue) test this hypothesis by
examining the relationship between skull asymmetry rel-
ative to skull size and maximum relative prey size con-
sumed. The strong positive correlation indicates that as
odontocete nasal asymmetry increases, so does the size of
the prey they can consume. This is an obvious adaptation
to feeding in general, and to aquatic existence in particu-
lar, as odontocetes swallow their prey whole without proc-
essing. Therefore, more energy is gained by consuming
one large prey item for the same amount of effort as is
expended to catch one small prey item.
Underwater feeding poses an additional challenge:
predators need to engulf prey while sorting it from the
surrounding aquatic milieu. In cetaceans, movements of
the hyoid apparatus play an important role in both
drawing prey into the oral cavity and enlarging the piri-
form sinus (particularly on the right side) for swallowing
prey whole (Reidenberg and Laitman, 1994). In addition,
the tongue plays an important role in squeezing water
out of the mouth. Werths (2007, this issue) study of the
hyolingual apparatus, particularly the tongue, in ceta-
ceans shows aquatic specializations that relate to ther-
moregulation. There are counter current vessels in the
tongue that control heat loss to the water in the oral
cavity. Species-specic differences in musculoskeletal
features of the hyolingual apparatus are related to the
mode of feeding used: suction, raptorial prehension, con-
tinuous ltering, and engulng with straining. Odonto-
cetes have a small, rigid mouth, enlarged hyoid appara-
tus, and hypertrophied tongue muscles. Grasping prey is
much like the game bobbing for applesand old-fash-
ioned New England tradition in which a person dunks
their face into a bucket of water with oating apples
and tries to grasp one with their teeth. In most cases,
the smooth-sided apple eludes capture because it simply
slides out of the grasp of the teeth and forward of the
water pressure generated by the closing mouth. Odonto-
cetes, faced with a similar problem while feeding under-
water, developed a unique mechanism to trap slippery
prey (e.g., sh, squid) in their mouth. They use their
hyoid and tongue as a piston: a sudden retraction gener-
ates negative pressure in the mouth which, in turn,
draws prey into the oral cavity. In some cetaceans, the
large tongue is also used for grasping and manipulating
prey. Mysticetes (baleen whales) use two different modes
of lter feeding. Balaenid mysticetes (right and bowhead
whales) are continuous strainers. They swim forward
with their mouth open, constantly taking in water with
small prey at the front of the mouth while streaming
excess water out of the lateralcaudal edge of the gape.
Their tongue is larger and stiff, and may function to
direct water ow through the mouth. Balaenopterid
mysticetes (rorqual whales, which possess ventral throat
pleats), expand the oor of the oral cavity to engulf
water containing schools of small sh or krill, and then
expel water through their baleen plates. The baleen
serves as a lter, allowing water to pass through while
trapping the small prey. These whales need a highly mo-
bile tongue that can atten and expand to accommodate
the distention of the oral cavity. The tongue may also
aid in wiping prey off of the baleen plates.
Although baleen is an aquatic adaptation that enables
lter feeding, it has an additional use in humpback
whales. Air (technically, gas) from the respiratory tract
may be released into the oral cavity and then pushed out
through the sieve of the baleen plates, resulting in an
underwater visual display called a bubble cloud (Reiden-
berg and Laitman, 2007a, this issue). Gas is released
from the respiratory tract by removing the epiglottis of
the larynx from its normal position behind the soft pal-
ate, and instead inserting it into the oral cavity. Gas can
then ow from the lungs, trachea, or laryngeal sac into
the oral cavity. As the oor of the mouth is contracted,
and the gape of the mouth is held nearly closed, gas is
forced superiorly and laterally against the racks of ba-
leen. The criss-crossing bers on the lingual surface of
the stacked baleen plates serve to break up the gas pass-
ing through it into many small bubbles, which give the
appearance of a ne, white mist underwater. This behav-
ior is surprising, as it risks the protective arrangement of
the intranarial larynx designed to keep water out of the
respiratory tract. It is thus perhaps a unique example of
an aquatic adaptation that compromises another aquatic
adaptation. Despite this risk, there are many potential
advantages to generating such a display. Bubble clouds
may be a signal to conspecics swimming close bypar-
ticularly in water with good visibility such as is found in
the tropical areas where mating usually occurs. The bub-
bles may also help herd prey into a tighter schooling for-
mation, making it easier to engulf larger numbers of
prey during feeding. In addition, bubble clouds may be
used as camouage. In open water, there are no obstacles
to hide behind. A bubble cloud may thus provide a visual
barrier (similar to a bush or a smoke screen), that can
block a predators view of the whale while it takes eva-
sive action. In addition, the bubbles may serve as an
echoic barrier to predatory orcas, causing disruption or
distortion of their echolocation signal (similar to a white
noise generator or a sonar jamming device).
The exploration of digestive tract anatomy continues
in this special issue with an examination of the stomach
in the Ziphiidae, the family of rare beaked whales. Mead
(2007, this issue) describes three morphological appear-
ances of the stomach: generalized ziphiid stomach (1
main stomach, 1 pyloric stomach), derived stomach type
I (2 main stomachs, 1 pyloric stomach), and derived
stomach type II (2 main stomachs, 2 pyloric stomachs).
A multiple chambered stomach is unusual in carnivores.
However, although all cetaceans are carnivores, the
presence of a multichambered stomach should not sur-
prise us. Whales are, afterall, closely related to artiodac-
tyls, which also have multichambered stomachs. While
their multiple chambers may relate to the mechanical
and enzymatic breakdown of an herbivorous diet (e.g.,
separation of food to be regurgitated and re-chewed as
cud), it is unclear what functions multiple chambers
play in the carnivorous ziphiids. Nevertheless, differen-
ces in the appearance of the three stomach morphologies
509 ANATOMICAL ADAPTATIONS OF AQUATIC MAMMALS
appear to be useful for elucidating systematic relation-
ships among the ziphiids.
EXTERNAL ANATOMY: INTEGUMENT AND
BODY SHAPE
One obvious place to discover adaptations to an
aquatic existence is to look at the point of contact
between the aquatic environment and the aquatic mam-
mal. Therefore, the integument and overall body shape
is examined in this special issue. Fur originally func-
tioned as a terrestrial modication to trap an insulating
layer of air, providing camouage, protection from abra-
sion or predatory injury, or shielding from the untravio-
let rays of the sun. Fur in water, while providing all of
the latter features, loses it ability to insulate and also
generates increased drag while swimming. Aquatic
mammals thus have developed oily furs that are rela-
tively waterproof (e.g., polar bears, otters, seals, sea
lions, beavers). Their fur may trap air, thus continuing
to provide insulation even when wet. In some aquatic
mammals, fur was lost in favor of a thicker, waterproof
epidermis (e.g., whales, dolphins, porpoises, manatees,
dugongs, walruses, hippopotomi). This change may be a
response to hydrodynamic needs, such as drag reduction.
The loss of air trapping for insulation necessitated the
development of thickened fat layer called blubber.
Vascular plexuses also developed to enable counter
current exchange, which conserves body heat centrally
while allowing the periphery to remain cold. Cold is not
the only thermal disadvantage to living in the water,
however. Heat can also build up in overly insulated
mammals when the ambient temperature rises at the
waters surface or, in the case of semiaquatic mammals
(e.g., pinnipeds), while on land. Heat dissipation is also
necessary during exertion or during pregnancy. Vascular
adaptations channel excess heat from locomotor muscles
or the reproductive organs to large at surfaces (ukes,
ippers, n) which act as radiators (Rommel et al., 1992,
1993, 1995, 2001). Oral rete allow cetaceans to regulate
heat loss from the oral cavity (Werth, 2007, this issue).
Changes in body shape also contribute to heat conser-
vation/radiation. Terrestrial mammals living in cold envi-
ronments tend to have shortened extremities (e.g., limbs,
ears, muzzles) to restrict heat radiation, while the oppo-
site is true in hot environments. There are several exam-
ples of cold water adapted marine mammals that also dis-
play shortened extremities and rotund body shapes (e.g.,
walrus, bowhead whale, right whale, beluga whale).
Reeb et al. (2007, this issue) examine the integument
of the southern right whale, one of the cold water
adapted marine mammals. Southern right whales have
hairs, but they no longer function to trap air. Rather,
they may have a tactile function and are probably used
as vibrissae to detect changes in prey density. Epidermal
specializations (e.g., callosities) provide barriers against
mechanical injury. There were lipid droplets associated
with the nucleus, which may facilitate the energetics of
nuclear metabolism. This may be an adaptation to sup-
port cellular metabolism during extreme cold exposure
(e.g., deep diving, polar waters) when the arterial supply
of nutrients to the skin is reduced to conserve heat. Not
surprisingly, these whales also have a thick, insulatory
integument, which acts as a thermoregulatory adapta-
tion to a cold environment. There is a highly folded junc-
tion between the epidermis and the dermis, a fat-free
zone of collagen bers in the reticular dermal layer, and
elastic ber networks within the dermal and hypodermal
layers. These features may reduce hydrodynamic fric-
tion, enabling the skin to deform under pressure to
increase hydrodynamic ow of water over the body dur-
ing high speed swimming.
LOCOMOTION
The thicker substrate of water creates resistance to
locomotion compared with air, thus necessitating the
need for a fusiform body shape that decreases drag in
pelagic marine mammals. Aquatic adaptations can also
be seen in the hydrodynamic shapes of the structures
used to generate thrust in cetaceans: tail ukes. Fish
et al. (2007, this issue) uses CT scans to describe the
thickness ratios of cetacean ukes. He found that their
shape was effective at reducing drag while moving at
high speeds. Fluke shapes were also found to be ideal
for reducing the tendency for ow to separate from the
uke surface. This feature, combined with the relatively
large leading edge radius, results in a shape that gener-
ates greater lift and helps to delay stall. Interestingly,
cetacean ukes were better at generating lift than engi-
neered foils, thus showing that we still have a lot to
learn from nature.
Sirenians also use a tail for propulsion which, simi-
larly to cetaceans, consists of a uke (or ukes) that are
supported only by a midline skeleton of caudal verte-
brae. Dugongs have two mirror-image ukes, similar in
shape to the double ukes of cetaceans. Manatees have
a single, paddle-shaped uke. Of interest, the evolution
of tail ukes in sirenians is convergent with the evolu-
tion of tail ukes in cetaceans. Buchholtz et al. (2007,
this issue) indicates that uke evolution developed
before the separation of manatees and dugongs.
Caudal propulsion in manatees is facilitated by
changes in both the shape and number of bones in the
axial skeleton. Buchholtz et al. (2007, this issue)
describe the anatomy of the Florida manatee vertebral
column in comparison to those of African manatees and
dugongs. Manatee vertebral counts and morphology are
unusual compared with both terrestrial mammals and
other sirenians. Aquatic adaptations can be seen in the
compressed cervical and elongate thoracic vertebrae,
short neural spine length, variation and reduction of the
lumbus, low precaudal count, lack of a sacral series, and
discontinuity within the caudal series. These traits all
contribute to aquatic locomotion. The shortened neck
limits head mobility, decreases drag, and effectively
repositions the ippers more anteriorly. Reduction in
precaudal vertebrae count and elongation of dorsal ver-
tebrae lowers the number of intervertebral exion
points, thus stabilizing the column while elongating the
body. Short neural spines and at centrum faces also
decrease vertebral exion and increase stability. Caudal
vertebrae have smaller centra and neural spines, which
increase exibility, and small posteriorly inclined trans-
verse processes, which serve as an anchor for muscles of
locomotion. Rounded centrum faces, absent zygapophy-
ses, and reduction of both neural spines and transverse
processes facilitate exibility in the uke region, a trait
necessary for caudal propulsion. These traits enable
axial locomotion, specically dorsoventral bending.
510 REIDENBERG
Changes in buoyancy are a challenge for aquatic loco-
motion: a shallow-water wading or bottom-feeding ani-
mal needs to be heavier than water to retain traction on
the substrate (e.g., moose) or stay submerged to feed
(e.g., manatee), an animal living at the surface needs to
oat (e.g., sea otter), and an open-water free-swimming
animal needs to be neutrally buoyant to rise and fall
within the water column (e.g., dolphin). Gray et al.
(2007, this issue) discuss the evolution of buoyancy con-
trol mechanisms as evidenced by microstructural
changes in the skeletal system, from analysis of ribs in
ve fossil cetacean families. Paradoxically, this aquatic
specialization predates gross anatomical changes associ-
ated with swimming in archaeocetes. There was a shift
from the typical terrestrial form, to osteopetrosis and
pachyosteosclerosis, and then to osteoporosis in the rst
quarter of cetacean evolutionary history. High bone den-
sity is a static buoyancy mechanism that provides bal-
last and is found in bottom feeders such as sirenians.
Low bone density is associated with dynamic buoyancy
control mechanisms (e.g., amount of gas in the lungs),
and is found in mammals living in deep water.
Appendicular osteology is also highly modied in
aquatic mammals. Unlike caudal ukes, which only
have midline skeletal support, the external form of a
ipper is dependent upon its underlying skeletal struc-
ture. Flipper shape reects functional locomotor require-
ments to increase lift, reduce drag, execute turns, and
enable braking. Narrow, elongate ippers facilitate fast
swimming while broad ippers aid in slow turns. Cooper
et al. (2007, this issue) show that digit loss and digit
positioning appear to underlie these disparate ipper
shapes. The osteology of the cetacean ipper (consisting
of the humerus, radius, ulna, carpals, metacarpals, and
phalanges) also provides many clues regarding their evo-
lution from a terrestrial ancestor with ve digits. Cooper
et al. (2007, this issue) describe differences in the num-
ber of digital rays in the two suborders of mysticetes
and odontocetes. Digital ray I is reduced in most penta-
dactylous cetaceans and is completely lost in tetradacty-
lous mysticetes. Five digits help support a broad ipper
(e.g., right whales), while four digits closely appressed
are seen in narrow, elongated ippers (e.g., humpback
whales). Most odontocetes also reduce the number of
phalangeal elements in digit V, while mysticetes typi-
cally retain the plesiomorphic condition of three pha-
langes. All cetaceans, however, exhibit an increased
number of phalanges (hyperphalangy). Hyperphalangy
and associated multiple interphalangeal joints may
smooth the leading edge contour of the ipper, thereby
helping to distribute leading edge forces.
Flippers are also found in other marine mammals,
including sirenians and pinnipeds. Sirenians may use
them to crawl along the river bed or the sea oor. Unlike
cetaceans and sirenians, the pinnipeds are among the
group of amphibious mammals (i.e., mammals that regu-
larly leave the water for extended periods of time). As
such, these aquatic mammals must adapt to the change
in substrate while entering or exiting water, and thus
retain the ability to locomote both on land and in water.
Sea lions, walruses, and seals all possess both fore and
hind ippers that contain many of the same, although
highly modied, musculoskeletal elements as terrestrial
forelimbs (English, 1976). Sea lions, despite their highly
modied extremities, can still raise themselves on both
their fore and hind ippers to walk and even run on
land. Seals, however, do not usually use their extremities
on land. Rather, they use an unusual rolling motion, pro-
pelling their body forward through the progression of a
dorsoventral body wavesimilar to the alternating side-
ways movements of a snake, but turned 90 degrees into
the vertical plane. Their movement is reminiscent of the
up-and-down body wave many aquatic mammals use to
swim underwater (e.g., dolphins, manatees). Nonip-
pered aquatic mammals that have retained four weight-
bearing limbs (e.g., polar bear, otter, beaver, muskrat)
can walk on land with a quadrupedal gait similar to their
fully terrestrial relatives (Tarasoff et al., 1972). Some
mammals limit their aquatic exposure only to wading in
water (e.g., moose). This allows them to reduce the
effects of friction by keeping their trunk out of the water
(enabled by having long limbs) and reducing the surface
area of the limbs (i.e., skinny legs). Hippos, however,
keep most of their body submerged while in water and
have rather thick extremities.
Fisher et al. (2007, this issue) discuss adaptations in
forelimb of the pygmy hippo that enable them to move
quickly in water despite their rotund habitus. Unlike
most other aquatic mammals, pygmy hippos do not
swim, but rather walk on muddy substrates. Propelling
the trunk through the high frictional resistance of water
thus requires robust musculature, compared with that of
quadrupedal land mammals such as the closely related
artiodactyls. In addition, pygmy hippos bear weight on
all of their toes and can prevent the toes from splaying.
These adaptations enable them to walk on the soft sur-
faces of a muddy substrate, as is found on the bottoms
or edges of lakes or rivers. Hippos retain several primi-
tive muscles, thus indicating their early evolutionary
divergence from Artiodactyla. This divergence may also
be closely allied to the divergence of Cetacea, thus
explaining the molecular data linking hippos and ceta-
ceans as closely related groups.
BRAIN, EYE, AND COMMUNICATION
SYSTEMS
Cetaceans possess among the largest brains, both in
absolute mass and relative to body size. It has been sug-
gested that the large brains are an aquatic adaptation,
particularly in echolocating odontocetes. Marino (2007,
this issue) addresses this relationship in a study compar-
ing brain size (as measured by encephalization quotient,
which accounts for body size) in fossil and modern
aquatic mammals. She concludes that brain size is inde-
pendent of aquatic existence, as large brains developed in
cetaceans well after they became aquatic. Furthermore,
other aquatic mammals (e.g., pinnipeds, sirenians) do not
possess markedly enlarged brains, complex gyrication
patterns, or high encephalization levels compared with
odontocete brains. Echolocation alone cannot account for
all of these changes, as terrestrial echolocators (e.g., bats)
are not highly encephalized. Rather, Marino postulates
that the high encephalization level of odontocetes is more
likely related to their complex social structure.
While brain size may not reect aquaticism, other
nervous tissues do. The eye, which is technically an
extension of the brain, exhibits several specializations in
aquatic mammals. Mass and Supin (2007, this issue)
review eye anatomy in four aquatic groups: cetaceans,
511 ANATOMICAL ADAPTATIONS OF AQUATIC MAMMALS
pinnipeds, sirenians, and sea otters. They found anatom-
ical differences that correspond to species-specic
aquatic adaptations and behaviors. Aquatic mammals
use different mechanisms to achieve aerial versus sub-
merged emmetropia (refraction of light to focus on the
retina). These corrections occur due to species-specic
differences at the cornea or the lens. Pupil shapes corre-
spond with variations in depth-dependent light expo-
sure. Retina composition is similar to nocturnal terres-
trial mammals, which is not surprising because aquatic
mammals are exposed to low light conditions under-
water. Cetaceans exhibit two areas of ganglion-cell con-
centration (the best-vision areas) located in the temporal
and nasal quadrants, while pinnipeds, sirenians, and
sea otters have only one such area.
Aquatic specializations are also apparent in the hear-
ing apparatus of aquatic mammals. The terrestrial ear
depends upon sound waves in air being collected by the
pinna, traveling though the auditory meatus, causing
vibrating of a tympanic membrane. These vibrations are
then transmitted through an ossicular chain to the oval
window, where vibrations set the inner ear membranes
and uid into motion, causing bending of hair cells,
which in turn, transmit an electrical signal that the
brain interprets as sound. Underwater hearing poses
technical challenges, as sound waves are propagated in a
uid medium. Submerged terrestrial mammals primarily
hear through bone conduction. However, as terrestrial
ears are not acoustically isolated from the skull, they
cannot distinguish directionality of sound under water.
Nummela at al. (2007, this issue) describe the evolution
of underwater hearing in cetaceans, particularly the
sound transmission mechanisms in six archaeocete fami-
lies. They show that the pinna and external auditory me-
atus were replaced by the mandible and its associated fat
pad, which transmit sound pressures to the tympanic
plate (lateral wall of the bulla). Other changes include
medial thickening of the tympanic bulla, functional
replacement of the tympanic membrane by a bony plate,
and changes in the orientation and shapes of the ossicles.
In addition, the tympanoperiotic complex becomes acous-
tically isolated from the skull by means of the develop-
ment of air sinuses. This acoustic isolation prevents bony
conduction and, therefore, preserves stereo hearing by
means of mandibular transmission.
Hearing sensitivity is examined in a particularly rare
cetacean, the North Atlantic right whale. As traditional
behavioral or physiological hearing tests are not feasible
with right whales, a functional model was developed
based upon the ear anatomy. Parks et al. (2007, this
issue) examined right whale ears by means of histologic
measurements of the basilar membrane and 2D and 3D
computerized tomography reconstructions of the cochlea.
An estimated hearing range of 10 Hz22 kHz based on
established marine mammal models was obtained. This
knowledge of the sound reception abilities of right
whales is an important beginning to understanding their
acoustic communication system and possible impacts of
anthropogenic noise.
The last article of the special issue addresses the other
end of the communication spectrum: sound generation.
Reidenberg and Laitman (2007b, this issue) describe the
discovery of a mysticete homolog of the vocal folds (the
structures responsible for sound production in terrestrial
mammals). This is a particularly exciting nding, as the
sound source has remained undescribed for mysticetes.
While vocal fold homologs have been identied in odonto-
cetes (Reidenberg and Laitman, 1988), vocal folds were
thought to be absent in baleen whales. Homology was
determined by criteria that dene vocal folds in terres-
trial mammals. The vocal fold homologue is described as
a U-shaped fold that is (1) able to function as a valve to
regulate gas ow, (2) supported by arytenoid cartilages,
(3) controlled by muscles that either directly insert on it
or move the arytenoid cartilages, (4) is connected across
the midline by a ligament, (5) receives motor and sensory
innervation from the recurrent laryngeal nerve for the
controlling musculature and mucosa caudal to the fold,
and sensory innervation from the superior laryngeal
nerve for the mucosa rostral and ventral to the fold, and
(6) is located adjacent to a diverticulum called the laryn-
geal sac (likely derived from the laryngeal ventricles).
Unlike the vocal folds of terrestrial mammals, which are
perpendicular to airow, the mysticete U-fold is oriented
parallel to airow. In this position, it can regulate airow
into/out of the laryngeal sac, and vibration of its edges
may generate sounds. The size and complexity of the
mysticete larynx indicates an organ with multiple func-
tions in addition to sound generation, including protec-
tion during breathing/swallowing, and airow/gas pres-
sure control in the respiratory spaces.
CONCLUSIONS
The articles in this special issue draw from several an-
atomical disciplines to present both the latest discoveries
in aquatic mammal research as well as some thoughtful
and thorough evolutionary and systems-based reviews.
It is hoped that, after reading this collection, one will
have a greater understanding of how much these ani-
mals have changed through the effects of natural selec-
tion from their terrestrial ancestors, through the various
fossil intermediate forms to the diversity of extant
aquatic mammals we have today. Knowledge of their un-
usual specializations will hopefully inspire us to copy na-
ture in the development of new technologies. For exam-
ple, continued investigations on ukes, ippers, axial
movements, feeding mechanics, skin, and body shape
may lead to development of more efcient hydrodynamic
designs for water- and aircraft. Further study of how
aquatic mammals regulate buoyancy, control bone den-
sity, or manage dramatic changes in temperature and
pressure as they rise and fall in the water column may
lead to new treatments for osteoporosis or the invention
of protective gear for exposure to the extreme environ-
mental changes of high and low altitude, space, or ocean
depths. A more complete understanding of neural orga-
nization, underwater vision, or sound generation and
sound reception mechanisms may lead to the creation of
better articial sensory systems. There is so much we
still have to learn about aquatic mammals. This is an
exciting time to be a marine mammal scientist.
A brief note about conservation. Many of the aquatic
mammals discussed in this issue are critically endan-
gered. Unfortunately, people only protect what they
know. Publications such as this, however, enable us to
fulll our duty as scientists to help educate the public
with scientic facts about these splendid animals. After
reading about all the phenomenal adaptations of aquatic
mammals presented here, I hope you will join me not
512 REIDENBERG
only in a new appreciation for how special these animals
truly are, but also in a renewed commitment to help pro-
tect them from extinction.
ACKNOWLEDGMENTS
I thank the contributors to this issue for all their hard
work in producing outstanding pieces. I am in debt to
those reviewers who spent numerous hours reviewing
and providing helpful critiques of the papers, thereby
vastly improving the content of this special issue. A spe-
cial thank you goes to the editor, Kurt Albertine, for
encouraging and promoting publication of high quality,
hypothesis-driven anatomical research. My deepest grat-
itude goes to Jeff Laitman, Associate Editor, for his
invaluable guidance, helpful advice, immeasurable sup-
port, abounding encouragement, and enthusiastic faith
in my ability to pull off this endeavor. He continues to
be a never-failing lighthouse, mentoring my scientic ca-
reer through the turbulent waters of academic life.
LITERATURE CITED
Abdelbaki YZ, Henk WG, Haldiman JT, Albert TF, Henry RW, Duf-
eld DW. 1984. Macroanatomy of the renicule of the bowhead
whale (Balaena mysticetus). Anat Rec 208:481490.
Au WW, Kastelein RA, Benoit-Bird KJ, Cranford TW, McKenna MF.
2006. Acoustic radiation from the head of echolocating harbor por-
poises (Phocoena phocoena). J Exp Biol 209:27262733.
Boyd RB. 1975. A gross and microscopic study of the respiratory
anatomy of the Antarctic Weddell seal, Leptonychotes weddelli. J
Morphol 147:309336.
Buchholtz EA, Booth AC, Webbink KE. 2007. Vertebral anatomy in
the Florida manatee, Trichechus manatus latirostris; a develop-
mental and evolutionary analysis. Anat Rec (this issue).
Cooper L, Berta A, Dawson S, Reidenberg JS. 2007. Evolution of
hyperphalangy and digit reduction in the Cetacean manus. Anat
Rec (this issue).
Cranford TW, Amundin M, Norris KS. 1996. Functional morphology
and homology in the odontocete nasal complex: implications for
sound generation. J Morphol 228:223285.
Dehnhardt G, Mauck B, Hanke W, Bleckmann H. 2001. Hydrody-
namic trail-following in harbor seals (Phoca vitulina). Science
293:102104.
Domning DP, Beatty BL. 2007. The use of tusks in feeding by
dugongid sirenians: observations and tests of hypotheses. Anat
Rec (this issue).
English AM. 1976. Functional anatomy of the hands of fur seals
and sea lions. Am J Anat 147:118.
English AW. 1977. Structural correlates of forelimb function in fur
seals and sea lions. J Morphol 151:325352.
Feldkamp SD. 1987. Swimming in the California sea lion: morpho-
metrics, drag and energetics. J Exp Biol 131:117135.
Fish FE, Innes S, Ronald K. 1988. Kinematics and estimated thrust
production of swimming harp and ringed seals. J Exp Biol 137:
157173.
Fish FE, Beneski JT, Ketten DR. 2007. Examination of the three-
dimensional geometry of Cetacean ukes using CT-scans: hydro-
dynamic implications. Anat Rec (this issue).
Fisher RE, Scott KM, Naples VL. 2007. Fore limb myology of the
pygmy hippopotamus (Choeropsis liberiensis). Anat Rec (this issue).
Gray N-M, Kainec K, Madar S, Tomko L, Wolfe S. 2007. Sink or
swim? Bone density as a mechanism for buoyancy control in early
Cetaceans. Anat Rec (this issue).
Henk WG, Abdelbaki YZ, Haldiman JT, Albert TF. 1986. Microana-
tomy of the renicule of Balaena mysticetus. Anat Rec 214:118129.
Hui CA. 1975. Thoracic collapse as affected by the retia thoracica in
the dolphin. Respir Physiol 25:6370.
Kanatous SB, Davis RW, Watson R, Polasek L, Williams TM,
Mathieu-Costello O. 2002. Aerobic capacities in the skeletal
muscles of Weddell seals: key to longer dive durations? J Exp Biol
205:36013608.
MacLeod CD, Reidenberg JS, Weller M, Santos MB, Herman J,
Goold J, Pierce GJ. 2007. Breaking symmetry: the marine envi-
ronment, prey size and the evolution of asymmetry in Cetacean
skulls. Anat Rec (this issue).
Maluf NS, Gassman JJ. 1998. Kidneys of the killerwhale and signif-
icance of reniculism. Anat Rec 250:3444.
Marino L. 2007. Cetacean brains: how aquatic are they? Anat Rec
(this issue).
Mass AM, Supin AYa. 2007. Adaptive features of the aquatic mam-
mals eye. Anat Rec (this issue).
Mead J. 2007. Stomach anatomy and use in dening systemic rela-
tionships of the cetacean family Ziphiidae (beaked whales). Anat
Rec (this issue).
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 dur-
ing submergence. J Comp Physiol B 171:127134.
Nummela S, Thewissen JGM, Bajpai S, Hussain ST, Kumar K.
2007. Sound transmission in archaic and modern whales: anatom-
ical adaptations for underwater hearing. Anat Rec (this issue).
Ortiz RM. 2001. Osmoregulation in marine mammals. J Exp Biol
204:18311844.
Parks SE, Ketten DR, OMalley JT, Arruda J. 2007. Anatomical pre-
dictions of hearing in the North Atlantic right whale. Anat Rec
(this issue).
Reeb D, Best PB, Angell CM, Kidson SH. 2007. Structure of the
integument of southern right whales, Eubalaena australis. Anat
Rec (this issue).
Reidenberg JS, Laitman JT. 1987. Position of the larynx in Odonto-
ceti (toothed whales). Anat Rec 218:98106.
Reidenberg JS, Laitman JT. 1988. Existence of vocal folds in the
larynx of Odontoceti (toothed whales). Anat Rec 221:892899.
Reidenberg JS, Laitman JT. 1994. Anatomy of the hyoid apparatus
in Odontoceti (toothed whales): specializations of their skeleton
and musculature compared with those of terrestrial mammals.
Anat Rec 240:598624.
Reidenberg JS, Laitman JT. 2007a. Blowing bubbles: an aquatic ad-
aptation that risks protection of the respiratory tract in hump-
back whales (Megaptera novaeangliae). Anat Rec (this issue).
Reidenberg JS, Laitman JT. 2007b. Discovery of a low frequency
sound source in Mysticeti (baleen whales): anatomical establish-
ment of a vocal fold homolog. Anat Rec (this issue).
Ridgway SH, Howard R. 1979. Dolphin lung collapse and intramus-
cular circulation during free diving - evidence from nitrogen
washout. Science 206:11821183.
Rommel SA, Pabst DA, McLellan WA, Mead JG, Potter CW. 1992.
Anatomical evidence for a countercurrent heat exchanger associ-
ated with dolphin testes. Anat Rec 232:150156.
Rommel SA, Pabst DA, McLellan WA. 1993. Functional morphology
of the vascular plexuses associated with the cetacean uterus.
Anat Rec 237:538546.
Rommel SA, Early GA, Matassa KA, Pabst DA, McLellan WA. 1995.
Venous structures associated with thermoregulation of phocid
seal reproductive organs. Anat Rec 243:390402.
Rommel SA, Pabst DA, McLellan WA. 2001. Functional morphology
of venous structures associated with the male and female repro-
ductive systems in Florida manatees (Trichechus manatus latir-
ostris). Anat Rec 264:339347.
Tarasoff FJ, Bisaillon A, Pierard J, Whitt AP. 1972. Locomotory pat-
terns and external morphology of the river otter, sea otter, and
harp seal (Mammalia). Can J Zool 50:915929.
Uhen MD. 2007. Evolution of marine mammals: back to the sea af-
ter 300 million years. Anat Rec (this issue).
Werth AJ. 2007. Adaptations of the cetacean hyolingual apparatus
for aquatic feeding and thermoregulation. Anat Rec (this issue).
Wright TJ, Davis RW. 2006. The effect of myoglobin concentration
on aerobic dive limit in a Weddell seal. J Exp Biol 209:25762585.
Yurick DB, Gaskin DE. 1988. Asymmetry in the skull of the har-
bour porpoise Phocoena phocoena (L.) and its relationship to
sound production and echolocation. Can J Zool 66:399402.
513 ANATOMICAL ADAPTATIONS OF AQUATIC MAMMALS