Adaptations for Digging &
Burrowing
Ch. 17
Digging/Burrowing

Common widespread
behavior


For finding food, storing
food, hiding
eggs/young,
temporary/long-term
shelter
Performed with hands,
feet, head or some
combination;
occasionally with the
mouth or neck
(Pituophis sp.)
Salamanders

Least specialized diggers of
amphibians



Many use pre-existing
burrows or
Enlarge natural crevasses w/
shovel-like head motions or
lateral undulations
Tiger salamanders
apparently best diggers



Survival in arid environments
Dig w/ muscular forelimbs,
alternating every 3-10 strokes
No apparent morphological
adaptations
Feet-First Burrowing Fogs




Vast majority of frogs burrow hindfeet first
Head raised, 1 leg fully flexed, then soil
immediately beneath & behind feet thrown
posteriorly or onto frog’s back
Enlargement of inner metatarsal tubercle
(integumentary projection on ventromedial
surface of foot)
Increased size & robusticity of prehallux
(skeletal support of inner metatarsal
tubercle)
Feet-First Burrowing Frogs


Relatively short hindlimbs
where tibiofibula is shorter
than femur
Mexican burrowing frogs
(Rhinophrynus dorsalis)



loses a phalanx from 1st digit
& remaining phalanx
morphologically converges on
distal prehallux
Thickened, rasp-like skin
beneath spade-like elements
No apparent burrowingmorphologies of pelvises
Head-First Burrowing Frogs

Most information comes from
Hemisus marmoratus &
Arenophryne rotunda

Frog thrust snout into ground,
then uses forelimbs to
excavate around head


Forelimbs may be used
alternately, synchronously, or
unilaterally
Once buried, hindlimbs may be
used to propel frog forward
Head-First Burrowing Frogs




Humerus, radioulna, & fingers short & robust
Increased area of attachment for muscles on
humerus (ventral humeral crest)
Decreased mobility in finger due to changes
in shape & number of phalanges & intercalary
cartilage (where present)
Coracoids longer & more robust (provide
greater surface area for muscle attachment),
and are more obliquely positioned relative to
long axis of body
Caecilians



Most highly adapted
amphibian burrowers,
but are poorly studied
All lack limbs (facilitates
burrowing)
Fossorial taxa burrow w/
their heads

Rigid, heavily ossified
skulls
Turtles

Digging is common among turtles especially
tortoises, also underwater



Daily shelter, hibernation, nesting
Burrows usually dug w/ forelimbs, egg pits
dug w/ alternating scooping w/ hindlimbs
Body pits prior to egg pits dug w/ forelimbs
(alternating or synchronous), hindlimbs
(alternating), all 4 limbs (diagonally
alternating) or some sequential combination
Turtles



Following based on
Gopherus, an extensive
tunneler
Distal phalanges enlarged
to support large, flat nails
Forefeet short, broad &
stiff


Reduced length & number of
phalanges except distal
phalanges
Close-packed, cuboidal
carpal elements
Crocodilians



All bury eggs on land & some dig young out
upon hatching, some burrow underground
during extreme cold or drought, & one
(Crocodylus palustris) may bury surplus food
May dig w/ hindlimbs (main method for egg
chambers), forelimbs (main method for
excavating hatchlings), snout, & jaws (in
grassy areas)
No obvious morphological adaptations

All features seem plesiomorphic or evolved for
other purposes
Lepidosauria


More digging & burrowing taxa than any
other major clade of vertebrates, & almost all
at least somewhat capable of digging
Most quadrupedal species scratch w/
forelimbs alternating after several strokes

Some may use head (weak forelimbs or
burrowing into soft sand)
Lepidosauria

Morphological
specializations for limbdigging rare
Most specialized species:

Strongly webbed hand/feet

Palmatogecko rangei


Likely evolved for locomotion
over loose sand
Cartilaginous paraphalanges
strengthen webbing more
proximal than nonburrowing species
Lepidosauria: Amphisbaenians


Head-burrowers; all but
3 species of Bipes
completely limbless
Limbed species use
large forelimbs (no
external hindlimbs) to
dig when initially
entering ground;
afterwards burrow w/
head
Lepidosauria: Amphisbaenians



Forelimbs are short, wide, & large relative to body
Zeugopodium short relative to stylopodium
Digits stout & roughly same length




Loss of phalanges + gain of phalanx in 1st digit for some
sp.
Hand is broad w/ large claws
Pectoral girdle positioned unusually close to head
Loss of limbs helpful for burrowing, but apparently
evolved as a result of body elongation
Mammalian Scratch-Diggers




Most common form of digging
in mammals
Variable degrees of
morphological adaptations
(many have none)
Rapid, alternating strokes of
clawed forelimbs in
predominantly parasagittal
plane
Many rodents use large incisors
to help loosen soil, & some
may use head & feet to move
loosened soil
Mammalian Scratch-Diggers

Enlarged sites of attachment for forelimb muscles used in
digging


Sites of attachment shifted, length of elements changed to
increase mechanical advantage


Deltoid tubercle of humerus positioned far from shoulder, long
olecranon process (sometimes accompanied by shortening of radius),
shortened manus
Articulations may be altered to stabilize joints


posteroventral portion of scapula, acromion process long?, deltoid
tubercle of humerus, median epicondyle, long olecranon process
Long acromion may limit lateral rotation of humerus, vertically oriented
keel-&-groove articulations in digits limit lateral movements
Some bones shorter/stouter/more robust

Short & stout humerus w/ thicker cortical bone around diaphysis,
shortened metacarpals & phalanges, large & robust distal
phalanges/claws
Mammalian Scratch-Diggers



Burrowers may brace
themselves by pushing
hindlegs out laterally against
burrow walls
Pelvis roughly horizontally
oriented, nearly parallel w/
vertebral column, & acetabula
positioned high – prevents
torsion when bracing
Elongated sacrum – increased
stability for pelvis = greater
forces generated by
hindlimbs?
Hook-&-Pull Diggers


Used exclusively by
anteaters to open
ant/termite nest during
foraging
Large claws on 2nd &
3rd digits hooked into
crack/hole, then
fingers are strongly
flexed & the arm is
pulled towards body
Hook-&-Pull Diggers





Sites of muscle attachment enlarged to accommodate
larger muscles: postscapular fossa (limb retractor),
median epicondyle (3rd digit flexor)
Distal tendon of largest head of the triceps muscle
merges w/ tendon of M. flexor digitorum profundus,
changing function to flex the 3rd digit
Shape of bones changed to provide mechanical
advantage: larger median epicondyle, notch in
median epicondyle acts as a pulley for medial triceps
tendon
Hooking digits large & robust
Keel-&-groove articulations in digits limit lateral &
torsional movement
Possible Theropod Analog






Mononykus Cretaceous
Mongolia
Single large functional claw
Palms face ventrally
Joints of manus limit
movement to parasagittal
plane
All apparently convergent
w/ mammalian hook-&-pull
diggers
Senter (2005)
Humeral Rotation Diggers



Best known in moles &
shrew moles, may also be
used by monotremes
Lateral thrusts of forefeet
almost entirely through
long-axis rotational
movements of humeri
Both arms may be used
synchronously (loose soil)
or one at a time
Humeral Rotation Diggers


Scapula oriented almost horizontally = anterior
displacement of forelimbs, and humerus oriented
obliquely = forefoot positioned laterally
Increased area of attachment for enlarged muscles



Area of origin on scapula for M. teres major
Manubrium long & ventrally keeled for pectoral muscles
Processes & articulations reoriented for mechanical
advantage & passive flexion/rotation



Increased distance between humeral head & teres tubercle
Deflection of tendon of M. biceps brachii through tunnel =
passive rotation of humerus during recovery
Fossa at distal end of medial epicondyle far lateral to axis
of rotation = passive flexion of manus
Humeral Rotation Diggers




Glenoid has elliptical articulation w/
humerus to stabilize joint
Radius, ulna, metacarpals, & proximal
phalanges shortened (mechanical
advantage) & robust
Distal phalanges enlarged to support large
broad claws
Large radial “sesamoid” on inner edge of
forefoot increases width of hand
Humeral Rotation Diggers




Hindlimbs used for kicking back loose soil in
deep burrows & for bracing against burrow
walls as in scratch-diggers
Pelvis elongated & nearly parallel to vertebral
column, acetabula raised
Pelvis fused to sacrum in up to 3 places
Hindlimbs shorter (shorter tibiofibula & pes) =
increased force generated + presumed
increased efficiency in tunnel locomotion
Aquatic Adaptations in the
Limbs of Amniotes
Ch. 18
Aquatic/Amphibious Amniotes



Many different taxa independently evolved
aquatic or semi-aquatic lifestyles
Multiple types of land-to-water transitions
are easy to make & readily advantageous
(as opposed to land-to-air transition)
Many animals may be good swimmers
&/or spend much of their time in the
water & have little/no aquatic adaptations
Mammals




May primarily wade or
swim
May swim w/ forelimbs,
hindlimbs/tail, or both
Limbs/tail may move in
vertical plane or horizontal
plane
Limbs may provide forward
thrust through drag-based
paddling or by generating
lift (fin shaped like
hydrofoil)
Mammals: Few Swimming
Adaptations

Shallow waders: walk in
shallows, generally w/o
submerging



Deep waders: walk on substrate
beneath surface of water



Tapirs, moose, etc.
Little or no limb adaptations
Hippopotamus
May have larger &/or denser bones
to counter buoyancy
Quadrupedal paddlers


Most terrestrial species
May have webbed feet
Mammals: Pelvic Swimming I



Alternating pelvic paddling (beaver): alternating
flexion & extension of hindlimbs in vertical plane
Alternate pelvic rowing (muskrat): alternating flexion
& extension of hindlimbs in horizontal plane
Both may have large feet w/ webbing (or long hairs)


Muskrat also has feet shifted to be perpendicular to plane
of motion
Lateral pelvic & caudal undulation (giant otter shrew)



propelled mainly by sinuous movements of tail & adjacent
vertebra
Hindfeet play secondary role
Fewer limb specializations than rowers/paddlers; tail may
be mediolaterally flattened
Mammals: Pelvic Swimming II






Pelvic oscillation (phocids): Feet move in horizontal
plane w/ plane of feet held vertically, & most power
provided by vertebral column
Ilium is short & anterior part is laterally deflected
where propulsive muscles in back attach; ischium &
pubis are long
Femur is short, but robust where muscles attach
Tibia & fibula are long often w/ a synostosis
proximally
Feet are symmetrical w/ 1st & 5th toes relatively large
Forelimb morphology reflect terrestrial locomotion
Mammals: Pelvic Swimming III

Simultaneous pelvic paddling (otters)




Dorsoventral pelvic undulation (sea otter)



Synchronous movement of hindlimbs in vertical plane
Similar limb morphology to APP: large, webbed feet
Tail & back muscles also participate
Feet are asymmetrical hydrofoils (digit 5 longest) thrust
provided during upstroke & downstroke
Femur, tibia, & fibula short
Dorsoventral caudal undulation (giant otter)


Flattened tail + webbed fingers/toes
Limbs generalized since tail is used to swim
Mammals: Pelvic Swimming IV



Caudal oscillation (Cetacea
& Sirenia)
All propulsion by
paddle/fluke shaped tails,
no external hindlimbs
Forelimbs in cetaceans used
for steering & stabilizing


Elbow, wrist, & fingers
immobile
Fingers asymmetrical w/
leading edge longest,
displaying hyperphalangy
Mammals: Pectoral Swimming I

Alternating pectoral paddling
(polar bears)



Alternating movement of forelimbs in
vertical plane
Morphology same as for terrestrial
bears
Alternating pectoral rowing
(platypus)



Alternating movement of forelimbs in
horizontal plane
Presumably swim by humeral
rotation as in walking
Forelimb of Ornithorhynchus
resembles that of moles (humeral
rotation diggers) w/ webbed feet
Mammals: Pectoral Swimming II





Pectoral oscillation (Otariidae)
Forelimbs provide lift during upstroke & downstroke
Forelimbs are powerful & far back on body
Humerus, radius, & ulna short
Hand long, asymmetrical (thumb longer & more
robust) flipper


Cartilaginous elements on distal phalanges lengthen
fingers beyond nails
Hindlimbs used in steering & terrestrial locomotion


Femurs are short
Feet are long, symmetrical (large 1st & 5th digits) & webbed
Birds



Many species of birds
evolved to live in & around
water
Three functionally distinct
regions (“locomotor
modules”): pectoral, pelvic,
& caudal
Aquatic adaptations involve
either pelvic or pectoral
regions w/out significantly
affecting the other region
Bird: Pelvic Swimming I

Wading



A large number of birds live in close association w/
water, but don’t swim
May have longer, broader toes to distribute weight
&/or long legs to wade deeper
Alternating pelvic surface paddling (ducks)


Float on surface & paddle w/ webbed feet
Some may do limited diving – short, laterally held
femur, tibiotarsus long & parallel to vertebra, knee
extensions limited, & ankle joint at level of tail
Birds: Pelvic Swimming II

Alternating pelvic submerged paddling (loons,
hesperornithiformes)



Lateral pelvic undulation (grebes)


Paddle backwards underwater
Webbed feet are reoriented far back on body
Feet provide lift; toes are asymmetric & each has
a hydrofoil cross-section
Quadrupedal surface paddling (flightless
steamer ducks)

Combine simultaneous beats of wings w/
alternating beats of hindlimbs on the surface
Birds: Pectoral Swimming



Simultaneous pectoral undulation
(auks, penguins, etc.)
Underwater flying: movement of
wings similar in air & water
Combining aquatic & aerial flight
reduces efficiency for both


Reduced wing area (shorter) = high
wing loading
Flightless birds maximize
efficiency for swimming




Reduced range of motion in joints;
reduced internal wing musculature
Wing bones are short, stiff, flattened,
& skeleton is dense
Wings positioned near midbody
Head, tail, & feet used for steering =
feet placed more posteriorly
Reptiles



Nonmammalian &
nonavian amniotes
Most obligatorily aquatic
taxa are extinct & have
relatively poorly
understood evolutionary
histories
Most extant taxa &
probably basal amniotes
are/were facultatively
aquatic
Reptiles: Primitive Aquatic
Locomotion

Wading/bottom walking: many reptiles wade into
water to feed w/o swimming


Some species w/ dense bodies may walk underwater such
as some freshwater chelonians & apparently some
placodonts
Lateral axial undulation & oscillation (crocodiles &
squamates)



Propulsion provided by tail & to a lesser extent body
In slow swimming limbs are mainly used for maneuvering;
fast swimming limbs are generally held immobile against
body
More amphibious forms (crocodilians, phytosaurs) may
have shorter, broader limbs
Reptiles: Obligatorily Aquatic Taxa



Lateral axial undulation & oscillation
Mosasaur & ichthyosaur limbs evolved into fins
w/ shortened long bones, reduced flexibility &
hyperphalangy
Ichthyosaurs caudal fins convergent w/
cetaceans & sharks



limbs may show change in number of digits & loss of
digit distinction
bones lightweight = buoyancy control or energy
conservation (less inertia)
Sea snakes live entire lives in water


Limblessness advantageous for streamlining
Evidence that snakes evolved from aquatic taxa:
fossils w/ aquatic morphologies (pachyostotic ribs,
flattened tail), presumed close relatives that are
aquatic (mosasaurs)
Reptiles: Limb-Propulsion I




Rowing
Freshwater turtles row w/ 4
limbs w/ webbed feet in
alternating diagonal strokes
Pachypleurosaurs also
apparently used this method
& added tail undulations
Nothosaurs had relatively
long (hyperphalangy), broad
(long bones widened, space
between radius & ulna), &
stiffened forelimbs
Reptiles: Limb-Propulsion II

Quadrupedal undulation (plesiosaurs)




Lift-based thrust of all limbs w/ comparable size &
structure
Laterally projecting hydrofoil limbs
Massive femur/humerus; reduced zeugopod &
wrist/ankle elements, loss of elbow/knee &
wrist/ankle joints, & hyperphalangy
Pectoral undulation (sea turtles)


Lift-based propulsion w/ strong synchronous beats
of long hydrofoil forelimbs
Hindlimbs used for steering & locomotion on land
Sesamoids & Ossicles in the
Appendicular Skeleton
Ch. 19
Sesamoids & Ossicles





Ossicles: any overlooked appendicular skeletal
elements
Highly variable size, shape, & position within &
between taxa
Often overlooked by anatomists, but important for
pathology & biomechanical issues
Intratendinous element: initially develop within a
tendon or ligament (including sesamoids)
Periarticular element: adjacent to a joint/articulation
but not initially within a tendon or ligament
Sesamoids




‘Sesamoid’ often used as a wastebasket
for any small & unusual skeletal elements
Sesamoid: skeletal elements that develop
within tendon or ligament adjacent to an
articulation or joint
Relatively small & ovoid in shape
Frequently have an inconstant distribution
Sesamoid Diversity & Distribution




Oldest known example (Permian) next to digit joints on
palmar side of manus in captorhinids
Oldest example (late Triassic) on a turtle (generally extant
taxa don’t have them) on dorsal side of manus & pes
Similar sesamoids also known in pterosaurs, a dinosaur
(Saichania), lizards, birds, mammals & some anurans
Ulnar patellas found in some pipid anurans, birds, mammals &
most squamates


Oldest knee sesamoid (mid-Triassic) found in Macrocnemius
bassanii


Tends to replace olecranon process in birds & lateral epicondyle in tree
shrews & a bat (Rousettus)
Also found in an anuran, some lizards, mammals & birds
Tarsal sesamoids found in anurans, birds, lizards & primates
Patella & Patelloid

Patella: relatively large, well-ossified sesamoid
cranially adjacent to distal end of femur




Predominant sesamoid for study: biomechanical,
orthopedic, pathological & evolutionary
Constant in most lizards, birds, & mammals
Absent in nonavian archosaurs, turtles & most marsupials
Patelloid: more proximally positioned sesamoid of
fibrocartilage


Found in some marsupials, various placental mammals, a
crocodilian & a turtle
May co-occur w/ patella
Patella/Patelloid Histology


Mature patella consists
of lamellar cortex and
a trabeculated core w/
hyaline cartilage lined
articular surfaces
Chondrocyte-like cells
of patelloid more
disorderly than in the
patella
Patella Development



Most true sesamoids develop through endochondral
ossification
The patella presumably starts as a cluster of cells w/in
quadriceps-patellar tendon, then undergoes
chondrification to form hyaline cartilage mass
Unlike other sesamoids, patellas ossify early in
ontogeny and develop in absence of mechanical
stimuli



Though mechanical stimuli necessary for regeneration
(dogs) & to stimulate underdeveloped patellas in humans
Recent research suggest LMXIB plays a role in patella
development & dorso-ventral limb patterning
Hoxa9/Hoxd9 and Hoxd9/Hoxd10 mutants result in
misshapen & displaced patellas
Traction Epiphyses



Bony projections of insertion for a tendon/ligament
that develop independently of the limb element
Proposed to be sesamoids incorporated into long
bones, or sesamoids are disarticulated traction
epiphyses, or that both ossicles are completely
separate
Evidence in favor of the 1st hypothesis:


In some mammals & birds the tibial tuberosity is derived
from an independent condensation originating from w/in
patellar ligament
In some birds the patella is also incorporated into the
hypertrophic cnemial crest
Mineralized Tendons & Ligaments




Found in various tetrapods, most notably birds
Tend to be slender, elongate & terminate in
advance of joints
Development based off of studies of the
domestic turkey
Tenocytes (fibroblasts) of tendons
hypertrophy & adopt a stellate morphology
followed by hypertrophic tenocytes producing
vesicles containing calcium & phosphorus =
associated w/ earliest appearance of
mineralization
Lunulae



Periarticular ossicles of the knee & other
synovial joints, nested within the menisci
They form osseous wedges w/ a
crescentic morphology
May serve protective & biomechanical
roles, such as resisting compressive forces
or acting as a fulcrum
Lunulae Diversity & Distribution




Best known in knee, though also found in
other joints such as the wrist & ankle
Reported in lissamphibians, squamates,
birds, & a variety of mammals
Very common in nonophidian squamates;
up to 5 elements in an individual
Knee lunulae very common in rodents
Lunulae Development & Histology





All exists as hyaline cartilaginous precursors & ossify
after birth/hatching
In humans, lunulae most often a result of injury or
pathology
Experiments w/ chick embryos suggest that
development of menisci (& therefore lunulae) is
dependent on movement of limbs & may result from
biomechanical induction
Haines (1942) hypothesized that lunulae form when
menisci reach surpass a threshold size
Outer layer made of lamellar bone & inner layer is
cancellous bone with or without marrow
Problematic Sesamoids & Ossicles



Definitions of sesamoid & lunulae
require knowledge of where the
elements form during skeletogenesis;
many ossicles only known from
mature individuals
The panda’s “thumb” may be a true
sesamoid, a remodeled periarticular
ossicle, or a neomorphic derivitive of
the carpal series
Other examples include:



the “panda’s toe” (enlarged tibial
“sesamoid”)
“sesamoids” associated w/ digits in
human manus (tendons & ligaments
attach secondarily)
Rods & extensions that support
wings/membranes of bats, gliding
mammals & pterosaurs (pteroid)
Biomechanics





Most explanations for sesamoids emphasis potential
current or past biomechanical function
Sesamoids & ossicles are most common in areas
subject to friction, compression or torsion
Known to sometimes occur in response to injury
Connective tissue known to respond to
compression/tension by altering ECM composition,
fiber orientation, cellular morphology & cellular
orientation
Osteogenic index developed to predict the likelihood
& position of sesamoid formation under different
stress regimes