Adaptations for Digging & Adaptations for Digging & BurrowingBurrowing

Ch. 17Ch. 17

Digging/BurrowingDigging/Burrowing

Common Common widespread behaviorwidespread behavior For finding food, For finding food,

storing food, hiding storing food, hiding eggs/young, eggs/young, temporary/long-term temporary/long-term sheltershelter

Performed with Performed with hands, feet, head or hands, feet, head or some combination; some combination; occasionally with the occasionally with the mouth or neck mouth or neck ((PituophisPituophis sp.) sp.)

SalamandersSalamanders Least specialized diggers Least specialized diggers

of amphibiansof amphibians Many use pre-existing Many use pre-existing

burrows orburrows or Enlarge natural crevasses Enlarge natural crevasses

w/ shovel-like head motions w/ shovel-like head motions or lateral undulationsor lateral undulations

Tiger salamanders Tiger salamanders apparently best diggersapparently best diggers Survival in arid Survival in arid

environmentsenvironments Dig w/ muscular forelimbs, Dig w/ muscular forelimbs,

alternating every 3-10 alternating every 3-10 strokesstrokes

No apparent morphological No apparent morphological adaptationsadaptations

Feet-First Burrowing FogsFeet-First Burrowing Fogs

Vast majority of frogs burrow hindfeet Vast majority of frogs burrow hindfeet firstfirst

Head raised, 1 leg fully flexed, then soil Head raised, 1 leg fully flexed, then soil immediately beneath & behind feet immediately beneath & behind feet thrown posteriorly or onto frog’s backthrown posteriorly or onto frog’s back

Enlargement of inner metatarsal Enlargement of inner metatarsal tubercle (integumentary projection on tubercle (integumentary projection on ventromedial surface of foot)ventromedial surface of foot)

Increased size & robusticity of Increased size & robusticity of prehallux (skeletal support of inner prehallux (skeletal support of inner metatarsal tubercle)metatarsal tubercle)

Feet-First Burrowing FrogsFeet-First Burrowing Frogs Relatively short hindlimbs Relatively short hindlimbs

where tibiofibula is where tibiofibula is shorter than femurshorter than femur

Mexican burrowing frogs Mexican burrowing frogs ((Rhinophrynus dorsalisRhinophrynus dorsalis)) loses a phalanx from 1loses a phalanx from 1stst

digit & remaining phalanx digit & remaining phalanx morphologically converges morphologically converges on distal prehalluxon distal prehallux

Thickened, rasp-like skin Thickened, rasp-like skin beneath spade-like beneath spade-like elementselements

No apparent burrowing-No apparent burrowing-morphologies of pelvisesmorphologies of pelvises

Head-First Burrowing FrogsHead-First Burrowing Frogs

Most information comes Most information comes from from Hemisus marmoratusHemisus marmoratus & & Arenophryne rotundaArenophryne rotunda

Frog thrust snout into Frog thrust snout into ground, then uses ground, then uses forelimbs to excavate forelimbs to excavate around headaround head Forelimbs may be used Forelimbs may be used

alternately, synchronously, alternately, synchronously, or unilaterallyor unilaterally

Once buried, hindlimbs may Once buried, hindlimbs may be used to propel frog be used to propel frog forwardforward

Head-First Burrowing FrogsHead-First Burrowing Frogs

Humerus, radioulna, & fingers short & Humerus, radioulna, & fingers short & robustrobust

Increased area of attachment for muscles Increased area of attachment for muscles on humerus (ventral humeral crest)on humerus (ventral humeral crest)

Decreased mobility in finger due to Decreased mobility in finger due to changes in shape & number of phalanges changes in shape & number of phalanges & intercalary cartilage (where present)& intercalary cartilage (where present)

Coracoids longer & more robust (provide Coracoids longer & more robust (provide greater surface area for muscle greater surface area for muscle attachment), and are more obliquely attachment), and are more obliquely positioned relative to long axis of bodypositioned relative to long axis of body

Caecilians

Most highly adapted Most highly adapted amphibian burrowers, amphibian burrowers, but are poorly studiedbut are poorly studied

All lack limbs All lack limbs (facilitates burrowing)(facilitates burrowing)

Fossorial taxa burrow Fossorial taxa burrow w/ their headsw/ their heads Rigid, heavily ossified Rigid, heavily ossified

skullsskulls

TurtlesTurtles

Digging is common among turtles Digging is common among turtles especially tortoises, also underwaterespecially tortoises, also underwater Daily shelter, hibernation, nestingDaily shelter, hibernation, nesting

Burrows usually dug w/ forelimbs, egg pits Burrows usually dug w/ forelimbs, egg pits dug w/ alternating scooping w/ hindlimbsdug w/ alternating scooping w/ hindlimbs

Body pits prior to egg pits dug w/ Body pits prior to egg pits dug w/ forelimbs (alternating or synchronous), forelimbs (alternating or synchronous), hindlimbs (alternating), all 4 limbs hindlimbs (alternating), all 4 limbs (diagonally alternating) or some (diagonally alternating) or some sequential combinationsequential combination

TurtlesTurtles

Following based on Following based on GopherusGopherus, an extensive , an extensive tunnelertunneler

Distal phalanges Distal phalanges enlarged to support enlarged to support large, flat nailslarge, flat nails

Forefeet short, broad & Forefeet short, broad & stiffstiff Reduced length & Reduced length &

number of phalanges number of phalanges except distal phalangesexcept distal phalanges

Close-packed, cuboidal Close-packed, cuboidal carpal elementscarpal elements

CrocodiliansCrocodilians

All bury eggs on land & some dig young All bury eggs on land & some dig young out upon hatching, some burrow out upon hatching, some burrow underground during extreme cold or underground during extreme cold or drought, & one (drought, & one (Crocodylus palustrisCrocodylus palustris) ) may bury surplus foodmay bury surplus food

May dig w/ hindlimbs (main method for May dig w/ hindlimbs (main method for egg chambers), forelimbs (main method egg chambers), forelimbs (main method for excavating hatchlings), snout, & jaws for excavating hatchlings), snout, & jaws (in grassy areas)(in grassy areas)

No obvious morphological adaptationsNo obvious morphological adaptations All features seem plesiomorphic or evolved All features seem plesiomorphic or evolved

for other purposesfor other purposes

LepidosauriaLepidosauria

More digging & burrowing taxa than More digging & burrowing taxa than any other major clade of vertebrates, & any other major clade of vertebrates, & almost all at least somewhat capable of almost all at least somewhat capable of diggingdigging

Most quadrupedal species scratch w/ Most quadrupedal species scratch w/ forelimbs alternating after several forelimbs alternating after several strokesstrokes Some may use head (weak forelimbs or Some may use head (weak forelimbs or

burrowing into soft sand)burrowing into soft sand)

LepidosauriaLepidosauria Morphological Morphological

specializations for limb-specializations for limb-digging raredigging rare

Most specialized species: Most specialized species: Palmatogecko rangeiPalmatogecko rangei

Strongly webbed Strongly webbed hand/feethand/feet Likely evolved for Likely evolved for

locomotion over loose sandlocomotion over loose sand Cartilaginous Cartilaginous

paraphalanges strengthen paraphalanges strengthen webbing more proximal webbing more proximal than non-burrowing than non-burrowing speciesspecies

Lepidosauria: Lepidosauria: AmphisbaeniansAmphisbaenians

Head-burrowers; all Head-burrowers; all but 3 species of but 3 species of BipesBipes completely limblesscompletely limbless

Limbed species use Limbed species use large forelimbs (no large forelimbs (no external hindlimbs) to external hindlimbs) to dig when initially dig when initially entering ground; entering ground; afterwards burrow w/ afterwards burrow w/ headhead

Lepidosauria: Lepidosauria: AmphisbaeniansAmphisbaenians

Forelimbs are short, wide, & large relative to bodyForelimbs are short, wide, & large relative to body Zeugopodium short relative to stylopodiumZeugopodium short relative to stylopodium Digits stout & roughly same lengthDigits stout & roughly same length

Loss of phalanges + gain of phalanx in 1Loss of phalanges + gain of phalanx in 1stst digit for some digit for some sp.sp.

Hand is broad w/ large clawsHand is broad w/ large claws Pectoral girdle positioned unusually close to headPectoral girdle positioned unusually close to head Loss of limbs helpful for burrowing, but apparently Loss of limbs helpful for burrowing, but apparently

evolved as a result of body elongationevolved as a result of body elongation

Mammalian Scratch-DiggersMammalian Scratch-Diggers

Most common form of Most common form of digging in mammalsdigging in mammals

Variable degrees of Variable degrees of morphological adaptations morphological adaptations (many have none)(many have none)

Rapid, alternating strokes Rapid, alternating strokes of clawed forelimbs in of clawed forelimbs in predominantly parasagittal predominantly parasagittal planeplane

Many rodents use large Many rodents use large incisors to help loosen soil, incisors to help loosen soil, & some may use head & & some may use head & feet to move loosened soilfeet to move loosened soil

Mammalian Scratch-DiggersMammalian Scratch-Diggers Enlarged sites of attachment for forelimb muscles used in Enlarged sites of attachment for forelimb muscles used in

diggingdigging posteroventral portion of scapula, acromion process long?, deltoid posteroventral portion of scapula, acromion process long?, deltoid

tubercle of humerus, median epicondyle, long olecranon processtubercle of humerus, median epicondyle, long olecranon process Sites of attachment shifted, length of elements changed Sites of attachment shifted, length of elements changed

to increase mechanical advantageto increase mechanical advantage Deltoid tubercle of humerus positioned far from shoulder, long Deltoid tubercle of humerus positioned far from shoulder, long

olecranon process (sometimes accompanied by shortening of olecranon process (sometimes accompanied by shortening of radius), shortened manusradius), shortened manus

Articulations may be altered to stabilize jointsArticulations may be altered to stabilize joints Long acromion may limit lateral rotation of humerus, vertically Long acromion may limit lateral rotation of humerus, vertically

oriented keel-&-groove articulations in digits limit lateral oriented keel-&-groove articulations in digits limit lateral movementsmovements

Some bones shorter/stouter/more robustSome bones shorter/stouter/more robust Short & stout humerus w/ thicker cortical bone around diaphysis, Short & stout humerus w/ thicker cortical bone around diaphysis,

shortened metacarpals & phalanges, large & robust distal shortened metacarpals & phalanges, large & robust distal phalanges/clawsphalanges/claws

Mammalian Scratch-DiggersMammalian Scratch-Diggers Burrowers may brace Burrowers may brace

themselves by pushing themselves by pushing hindlegs out laterally hindlegs out laterally against burrow wallsagainst burrow walls

Pelvis roughly horizontally Pelvis roughly horizontally oriented, nearly parallel w/ oriented, nearly parallel w/ vertebral column, & vertebral column, & acetabula positioned high – acetabula positioned high – prevents torsion when prevents torsion when bracingbracing

Elongated sacrum – Elongated sacrum – increased stability for increased stability for pelvis = greater forces pelvis = greater forces generated by hindlimbs?generated by hindlimbs?

Hook-&-Pull DiggersHook-&-Pull Diggers

Used exclusively by Used exclusively by anteaters to open anteaters to open ant/termite nest ant/termite nest during foragingduring foraging

Large claws on 2Large claws on 2ndnd & & 33rdrd digits hooked into digits hooked into crack/hole, then crack/hole, then fingers are strongly fingers are strongly flexed & the arm is flexed & the arm is pulled towards bodypulled towards body

Hook-&-Pull DiggersHook-&-Pull Diggers

Sites of muscle attachment enlarged to Sites of muscle attachment enlarged to accommodate larger muscles: postscapular accommodate larger muscles: postscapular fossa (limb retractor), median epicondyle (3fossa (limb retractor), median epicondyle (3rdrd digit flexor)digit flexor)

Distal tendon of largest head of the triceps Distal tendon of largest head of the triceps muscle merges w/ tendon of muscle merges w/ tendon of M. flexor digitorum M. flexor digitorum profundusprofundus, changing function to flex the 3, changing function to flex the 3rdrd digit digit

Shape of bones changed to provide mechanical Shape of bones changed to provide mechanical advantage: larger median epicondyle, notch in advantage: larger median epicondyle, notch in median epicondyle acts as a pulley for medial median epicondyle acts as a pulley for medial triceps tendontriceps tendon

Hooking digits large & robustHooking digits large & robust Keel-&-groove articulations in digits limit lateral Keel-&-groove articulations in digits limit lateral

& torsional movement& torsional movement

Possible Theropod AnalogPossible Theropod Analog MononykusMononykus Cretaceous Cretaceous

MongoliaMongolia Single large functional Single large functional

clawclaw Palms face ventrallyPalms face ventrally Joints of manus limit Joints of manus limit

movement to parasagittal movement to parasagittal planeplane

All apparently convergent All apparently convergent w/ mammalian hook-&-w/ mammalian hook-&-pull diggerspull diggers

Senter (2005)Senter (2005)

Humeral Rotation DiggersHumeral Rotation Diggers

Best known in moles & Best known in moles & shrew moles, may also shrew moles, may also be used by monotremesbe used by monotremes

Lateral thrusts of Lateral thrusts of forefeet almost entirely forefeet almost entirely through long-axis through long-axis rotational movements of rotational movements of humerihumeri

Both arms may be used Both arms may be used synchronously (loose synchronously (loose soil) or one at a timesoil) or one at a time

Humeral Rotation DiggersHumeral Rotation Diggers Scapula oriented almost horizontally = anterior Scapula oriented almost horizontally = anterior

displacement of forelimbs, and humerus oriented displacement of forelimbs, and humerus oriented obliquely = forefoot positioned laterallyobliquely = forefoot positioned laterally

Increased area of attachment for enlarged Increased area of attachment for enlarged musclesmuscles Area of origin on scapula for Area of origin on scapula for M. teres majorM. teres major Manubrium long & ventrally keeled for pectoral musclesManubrium long & ventrally keeled for pectoral muscles

Processes & articulations reoriented for Processes & articulations reoriented for mechanical advantage & passive flexion/rotationmechanical advantage & passive flexion/rotation Increased distance between humeral head & teres Increased distance between humeral head & teres

tubercletubercle Deflection of tendon of Deflection of tendon of M. biceps brachiiM. biceps brachii through tunnel through tunnel

= passive rotation of humerus during recovery= passive rotation of humerus during recovery Fossa at distal end of medial epicondyle far lateral to Fossa at distal end of medial epicondyle far lateral to

axis of rotation = passive flexion of manusaxis of rotation = passive flexion of manus

Humeral Rotation DiggersHumeral Rotation Diggers

Glenoid has elliptical articulation w/ Glenoid has elliptical articulation w/ humerus to stabilize jointhumerus to stabilize joint

Radius, ulna, metacarpals, & proximal Radius, ulna, metacarpals, & proximal phalanges shortened (mechanical phalanges shortened (mechanical advantage) & robustadvantage) & robust

Distal phalanges enlarged to support Distal phalanges enlarged to support large broad clawslarge broad claws

Large radial “sesamoid” on inner edge Large radial “sesamoid” on inner edge of forefoot increases width of handof forefoot increases width of hand

Humeral Rotation DiggersHumeral Rotation Diggers

Hindlimbs used for kicking back loose soil Hindlimbs used for kicking back loose soil in deep burrows & for bracing against in deep burrows & for bracing against burrow walls as in scratch-diggersburrow walls as in scratch-diggers

Pelvis elongated & nearly parallel to Pelvis elongated & nearly parallel to vertebral column, acetabula raisedvertebral column, acetabula raised

Pelvis fused to sacrum in up to 3 placesPelvis fused to sacrum in up to 3 places Hindlimbs shorter (shorter tibiofibula & Hindlimbs shorter (shorter tibiofibula &

pes) = increased force generated + pes) = increased force generated + presumed increased efficiency in tunnel presumed increased efficiency in tunnel locomotionlocomotion

Aquatic Adaptations in the Aquatic Adaptations in the Limbs of AmniotesLimbs of Amniotes

Ch. 18Ch. 18

Aquatic/Amphibious Aquatic/Amphibious AmniotesAmniotes

Many different taxa independently Many different taxa independently evolved aquatic or semi-aquatic lifestylesevolved aquatic or semi-aquatic lifestyles

Multiple types of land-to-water transitions Multiple types of land-to-water transitions are easy to make & readily advantageous are easy to make & readily advantageous (as opposed to land-to-air transition)(as opposed to land-to-air transition)

Many animals may be good swimmers Many animals may be good swimmers &/or spend much of their time in the &/or spend much of their time in the water & have little/no aquatic water & have little/no aquatic adaptationsadaptations

MammalsMammals

May primarily wade or May primarily wade or swimswim

May swim w/ forelimbs, May swim w/ forelimbs, hindlimbs/tail, or bothhindlimbs/tail, or both

Limbs/tail may move in Limbs/tail may move in vertical plane or vertical plane or horizontal planehorizontal plane

Limbs may provide Limbs may provide forward thrust through forward thrust through drag-based paddling or drag-based paddling or by generating lift (fin by generating lift (fin shaped like hydrofoil)shaped like hydrofoil)

Mammals: Few Swimming Mammals: Few Swimming AdaptationsAdaptations

Shallow waders: walk in Shallow waders: walk in shallows, generally w/o shallows, generally w/o submergingsubmerging Tapirs, moose, etc.Tapirs, moose, etc. Little or no limb adaptationsLittle or no limb adaptations

Deep waders: walk on Deep waders: walk on substrate beneath surface substrate beneath surface of waterof water HippopotamusHippopotamus May have larger &/or denser May have larger &/or denser

bones to counter buoyancybones to counter buoyancy Quadrupedal paddlersQuadrupedal paddlers

Most terrestrial speciesMost terrestrial species May have webbed feetMay have webbed feet

Mammals: Pelvic Swimming Mammals: Pelvic Swimming II

Alternating pelvic paddling (beaver): alternating Alternating pelvic paddling (beaver): alternating flexion & extension of hindlimbs in vertical planeflexion & extension of hindlimbs in vertical plane

Alternate pelvic rowing (muskrat): alternating Alternate pelvic rowing (muskrat): alternating flexion & extension of hindlimbs in horizontal planeflexion & extension of hindlimbs in horizontal plane

Both may have large feet w/ webbing (or long hairs)Both may have large feet w/ webbing (or long hairs) Muskrat also has feet shifted to be perpendicular to plane Muskrat also has feet shifted to be perpendicular to plane

of motionof motion Lateral pelvic & caudal undulation (giant otter Lateral pelvic & caudal undulation (giant otter

shrew)shrew) propelled mainly by sinuous movements of tail & adjacent propelled mainly by sinuous movements of tail & adjacent

vertebravertebra Hindfeet play secondary roleHindfeet play secondary role Fewer limb specializations than rowers/paddlers; tail may Fewer limb specializations than rowers/paddlers; tail may

be mediolaterally flattenedbe mediolaterally flattened

Mammals: Pelvic Swimming Mammals: Pelvic Swimming IIII

Pelvic oscillation (phocids): Feet move in Pelvic oscillation (phocids): Feet move in horizontal plane w/ plane of feet held vertically, horizontal plane w/ plane of feet held vertically, & most power provided by vertebral column& most power provided by vertebral column

Ilium is short & anterior part is laterally Ilium is short & anterior part is laterally deflected where propulsive muscles in back deflected where propulsive muscles in back attach; ischium & pubis are longattach; ischium & pubis are long

Femur is short, but robust where muscles attachFemur is short, but robust where muscles attach Tibia & fibula are long often w/ a synostosis Tibia & fibula are long often w/ a synostosis

proximallyproximally Feet are symmetrical w/ 1Feet are symmetrical w/ 1stst & 5 & 5thth toes relatively toes relatively

largelarge Forelimb morphology reflect terrestrial Forelimb morphology reflect terrestrial

locomotionlocomotion

Mammals: Pelvic Swimming Mammals: Pelvic Swimming IIIIII

Simultaneous pelvic paddling (otters)Simultaneous pelvic paddling (otters) Synchronous movement of hindlimbs in vertical Synchronous movement of hindlimbs in vertical

planeplane Similar limb morphology to APP: large, webbed feetSimilar limb morphology to APP: large, webbed feet Tail & back muscles also participateTail & back muscles also participate

Dorsoventral pelvic undulation (sea otter)Dorsoventral pelvic undulation (sea otter) Feet are asymmetrical hydrofoils (digit 5 longest) Feet are asymmetrical hydrofoils (digit 5 longest)

thrust provided during upstroke & downstrokethrust provided during upstroke & downstroke Femur, tibia, & fibula shortFemur, tibia, & fibula short

Dorsoventral caudal undulation (giant otter)Dorsoventral caudal undulation (giant otter) Flattened tail + webbed fingers/toesFlattened tail + webbed fingers/toes Limbs generalized since tail is used to swimLimbs generalized since tail is used to swim

Mammals: Pelvic Swimming Mammals: Pelvic Swimming IVIV Caudal oscillation Caudal oscillation

(Cetacea & Sirenia)(Cetacea & Sirenia) All propulsion by All propulsion by

paddle/fluke shaped tails, paddle/fluke shaped tails, no external hindlimbsno external hindlimbs

Forelimbs in cetaceans Forelimbs in cetaceans used for steering & used for steering & stabilizingstabilizing Elbow, wrist, & fingers Elbow, wrist, & fingers

immobileimmobile Fingers asymmetrical w/ Fingers asymmetrical w/

leading edge longest, leading edge longest, displaying hyperphalangydisplaying hyperphalangy

Mammals: Pectoral Mammals: Pectoral Swimming ISwimming I

Alternating pectoral paddling Alternating pectoral paddling (polar bears)(polar bears) Alternating movement of Alternating movement of

forelimbs in vertical planeforelimbs in vertical plane Morphology same as for Morphology same as for

terrestrial bearsterrestrial bears Alternating pectoral rowing Alternating pectoral rowing

(platypus)(platypus) Alternating movement of Alternating movement of

forelimbs in horizontal planeforelimbs in horizontal plane Presumably swim by humeral Presumably swim by humeral

rotation as in walkingrotation as in walking Forelimb of Forelimb of OrnithorhynchusOrnithorhynchus

resembles that of moles resembles that of moles (humeral rotation diggers) w/ (humeral rotation diggers) w/ webbed feetwebbed feet

Mammals: Pectoral Mammals: Pectoral Swimming IISwimming II

Pectoral oscillation (Otariidae)Pectoral oscillation (Otariidae) Forelimbs provide lift during upstroke & Forelimbs provide lift during upstroke &

downstrokedownstroke Forelimbs are powerful & far back on bodyForelimbs are powerful & far back on body Humerus, radius, & ulna shortHumerus, radius, & ulna short Hand long, asymmetrical (thumb longer & more Hand long, asymmetrical (thumb longer & more

robust) flipperrobust) flipper Cartilaginous elements on distal phalanges lengthen Cartilaginous elements on distal phalanges lengthen

fingers beyond nailsfingers beyond nails Hindlimbs used in steering & terrestrial Hindlimbs used in steering & terrestrial

locomotionlocomotion Femurs are shortFemurs are short Feet are long, symmetrical (large 1Feet are long, symmetrical (large 1stst & 5 & 5thth digits) & digits) &

webbedwebbed

BirdsBirds

Many species of birds Many species of birds evolved to live in & evolved to live in & around wateraround water

Three functionally Three functionally distinct regions distinct regions (“locomotor modules”): (“locomotor modules”): pectoral, pelvic, & caudalpectoral, pelvic, & caudal

Aquatic adaptations Aquatic adaptations involve either pelvic or involve either pelvic or pectoral regions w/out pectoral regions w/out significantly affecting the significantly affecting the other regionother region

Bird: Pelvic Swimming IBird: Pelvic Swimming I

WadingWading A large number of birds live in close A large number of birds live in close

association w/ water, but don’t swimassociation w/ water, but don’t swim May have longer, broader toes to distribute May have longer, broader toes to distribute

weight &/or long legs to wade deeperweight &/or long legs to wade deeper Alternating pelvic surface paddling (ducks)Alternating pelvic surface paddling (ducks)

Float on surface & paddle w/ webbed feetFloat on surface & paddle w/ webbed feet Some may do limited diving – short, laterally Some may do limited diving – short, laterally

held femur, tibiotarsus long & parallel to held femur, tibiotarsus long & parallel to vertebra, knee extensions limited, & ankle vertebra, knee extensions limited, & ankle joint at level of tailjoint at level of tail

Birds: Pelvic Swimming IIBirds: Pelvic Swimming II

Alternating pelvic submerged paddling Alternating pelvic submerged paddling (loons, hesperornithiformes)(loons, hesperornithiformes) Paddle backwards underwaterPaddle backwards underwater Webbed feet are reoriented far back on bodyWebbed feet are reoriented far back on body

Lateral pelvic undulation (grebes)Lateral pelvic undulation (grebes) Feet provide lift; toes are asymmetric & each Feet provide lift; toes are asymmetric & each

has a hydrofoil cross-sectionhas a hydrofoil cross-section Quadrupedal surface paddling (flightless Quadrupedal surface paddling (flightless

steamer ducks)steamer ducks) Combine simultaneous beats of wings w/ Combine simultaneous beats of wings w/

alternating beats of hindlimbs on the surfacealternating beats of hindlimbs on the surface

Birds: Pectoral SwimmingBirds: Pectoral Swimming Simultaneous pectoral Simultaneous pectoral

undulation (auks, penguins, etc.)undulation (auks, penguins, etc.) Underwater flying: movement of Underwater flying: movement of

wings similar in air & waterwings similar in air & water Combining aquatic & aerial flight Combining aquatic & aerial flight

reduces efficiency for bothreduces efficiency for both Reduced wing area (shorter) = high Reduced wing area (shorter) = high

wing loadingwing loading Flightless birds maximize Flightless birds maximize

efficiency for swimmingefficiency for swimming Reduced range of motion in joints; Reduced range of motion in joints;

reduced internal wing musculaturereduced internal wing musculature Wing bones are short, stiff, Wing bones are short, stiff,

flattened, & skeleton is denseflattened, & skeleton is dense Wings positioned near midbodyWings positioned near midbody Head, tail, & feet used for steering Head, tail, & feet used for steering

= feet placed more posteriorly= feet placed more posteriorly

ReptilesReptiles

Nonmammalian & Nonmammalian & nonavian amniotesnonavian amniotes

Most obligatorily Most obligatorily aquatic taxa are aquatic taxa are extinct & have extinct & have relatively poorly relatively poorly understood understood evolutionary historiesevolutionary histories

Most extant taxa & Most extant taxa & probably basal probably basal amniotes are/were amniotes are/were facultatively aquaticfacultatively aquatic

Reptiles: Primitive Aquatic Reptiles: Primitive Aquatic LocomotionLocomotion

Wading/bottom walking: many reptiles wade Wading/bottom walking: many reptiles wade into water to feed w/o swimminginto water to feed w/o swimming Some species w/ dense bodies may walk Some species w/ dense bodies may walk

underwater such as some freshwater chelonians & underwater such as some freshwater chelonians & apparently some placodontsapparently some placodonts

Lateral axial undulation & oscillation Lateral axial undulation & oscillation (crocodiles & squamates)(crocodiles & squamates) Propulsion provided by tail & to a lesser extent Propulsion provided by tail & to a lesser extent

bodybody In slow swimming limbs are mainly used for In slow swimming limbs are mainly used for

maneuvering; fast swimming limbs are generally maneuvering; fast swimming limbs are generally held immobile against bodyheld immobile against body

More amphibious forms (crocodilians, phytosaurs) More amphibious forms (crocodilians, phytosaurs) may have shorter, broader limbsmay have shorter, broader limbs

Reptiles: Obligatorily Aquatic Reptiles: Obligatorily Aquatic TaxaTaxa

Lateral axial undulation & oscillationLateral axial undulation & oscillation Mosasaur & ichthyosaur limbs evolved Mosasaur & ichthyosaur limbs evolved

into fins w/ shortened long bones, into fins w/ shortened long bones, reduced flexibility & hyperphalangyreduced flexibility & hyperphalangy

Ichthyosaurs caudal fins convergent w/ Ichthyosaurs caudal fins convergent w/ cetaceans & sharkscetaceans & sharks limbs may show change in number of digits & limbs may show change in number of digits &

loss of digit distinctionloss of digit distinction bones lightweight = buoyancy control or bones lightweight = buoyancy control or

energy conservation (less inertia)energy conservation (less inertia) Sea snakes live entire lives in waterSea snakes live entire lives in water

Limblessness advantageous for streamliningLimblessness advantageous for streamlining Evidence that snakes evolved from aquatic Evidence that snakes evolved from aquatic

taxa: fossils w/ aquatic morphologies taxa: fossils w/ aquatic morphologies (pachyostotic ribs, flattened tail), presumed (pachyostotic ribs, flattened tail), presumed close relatives that are aquatic (mosasaurs)close relatives that are aquatic (mosasaurs)

Reptiles: Limb-Propulsion IReptiles: Limb-Propulsion I

RowingRowing Freshwater turtles row w/ 4 Freshwater turtles row w/ 4

limbs w/ webbed feet in limbs w/ webbed feet in alternating diagonal strokesalternating diagonal strokes

Pachypleurosaurs also Pachypleurosaurs also apparently used this apparently used this method & added tail method & added tail undulationsundulations

Nothosaurs had relatively Nothosaurs had relatively long (hyperphalangy), broad long (hyperphalangy), broad (long bones widened, space (long bones widened, space between radius & ulna), & between radius & ulna), & stiffened forelimbsstiffened forelimbs

Reptiles: Limb-Propulsion IIReptiles: Limb-Propulsion II Quadrupedal undulation (plesiosaurs)Quadrupedal undulation (plesiosaurs)

Lift-based thrust of all limbs w/ comparable Lift-based thrust of all limbs w/ comparable size & structuresize & structure

Laterally projecting hydrofoil limbsLaterally projecting hydrofoil limbs Massive femur/humerus; reduced zeugopod Massive femur/humerus; reduced zeugopod

& wrist/ankle elements, loss of elbow/knee & & wrist/ankle elements, loss of elbow/knee & wrist/ankle joints, & hyperphalangywrist/ankle joints, & hyperphalangy

Pectoral undulation (sea turtles)Pectoral undulation (sea turtles) Lift-based propulsion w/ strong synchronous Lift-based propulsion w/ strong synchronous

beats of long hydrofoil forelimbsbeats of long hydrofoil forelimbs Hindlimbs used for steering & locomotion on Hindlimbs used for steering & locomotion on

landland

Sesamoids & Ossicles in Sesamoids & Ossicles in the Appendicular Skeletonthe Appendicular Skeleton

Ch. 19Ch. 19

Sesamoids & OssiclesSesamoids & Ossicles

Ossicles: any overlooked appendicular skeletal Ossicles: any overlooked appendicular skeletal elementselements

Highly variable size, shape, & position within & Highly variable size, shape, & position within & between taxabetween taxa

Often overlooked by anatomists, but important for Often overlooked by anatomists, but important for pathology & biomechanical issuespathology & biomechanical issues

Intratendinous element: initially develop within a Intratendinous element: initially develop within a tendon or ligament (including sesamoids)tendon or ligament (including sesamoids)

Periarticular element: adjacent to a Periarticular element: adjacent to a joint/articulation but not initially within a tendon or joint/articulation but not initially within a tendon or ligamentligament

SesamoidsSesamoids

‘‘Sesamoid’ often used as a wastebasket Sesamoid’ often used as a wastebasket for any small & unusual skeletal elementsfor any small & unusual skeletal elements

Sesamoid: skeletal elements that develop Sesamoid: skeletal elements that develop within tendon or ligament adjacent to an within tendon or ligament adjacent to an articulation or jointarticulation or joint

Relatively small & ovoid in shapeRelatively small & ovoid in shape Frequently have an inconstant distributionFrequently have an inconstant distribution

Sesamoid Diversity & Sesamoid Diversity & DistributionDistribution

Oldest known example (Permian) next to digit joints on Oldest known example (Permian) next to digit joints on palmar side of manus in captorhinidspalmar side of manus in captorhinids

Oldest example (late Triassic) on a turtle (generally extant Oldest example (late Triassic) on a turtle (generally extant taxa don’t have them) on dorsal side of manus & pestaxa don’t have them) on dorsal side of manus & pes

Similar sesamoids also known in pterosaurs, a dinosaur Similar sesamoids also known in pterosaurs, a dinosaur ((SaichaniaSaichania), lizards, birds, mammals & some anurans), lizards, birds, mammals & some anurans

Ulnar patellas found in some pipid anurans, birds, Ulnar patellas found in some pipid anurans, birds, mammals & most squamatesmammals & most squamates Tends to replace olecranon process in birds & lateral epicondyle in Tends to replace olecranon process in birds & lateral epicondyle in

tree shrews & a bat (tree shrews & a bat (RousettusRousettus)) Oldest knee sesamoid (mid-Triassic) found in Oldest knee sesamoid (mid-Triassic) found in

Macrocnemius bassaniiMacrocnemius bassanii Also found in an anuran, some lizards, mammals & birdsAlso found in an anuran, some lizards, mammals & birds

Tarsal sesamoids found in anurans, birds, lizards & Tarsal sesamoids found in anurans, birds, lizards & primatesprimates

Patella & PatelloidPatella & Patelloid

Patella: relatively large, well-ossified sesamoid Patella: relatively large, well-ossified sesamoid cranially adjacent to distal end of femurcranially adjacent to distal end of femur Predominant sesamoid for study: biomechanical, Predominant sesamoid for study: biomechanical,

orthopedic, pathological & evolutionaryorthopedic, pathological & evolutionary Constant in most lizards, birds, & mammalsConstant in most lizards, birds, & mammals Absent in nonavian archosaurs, turtles & most Absent in nonavian archosaurs, turtles & most

marsupialsmarsupials Patelloid: more proximally positioned sesamoid Patelloid: more proximally positioned sesamoid

of fibrocartilageof fibrocartilage Found in some marsupials, various placental Found in some marsupials, various placental

mammals, a crocodilian & a turtlemammals, a crocodilian & a turtle May co-occur w/ patellaMay co-occur w/ patella

Patella/Patelloid HistologyPatella/Patelloid Histology

Mature patella Mature patella consists of lamellar consists of lamellar cortex and a cortex and a trabeculated core w/ trabeculated core w/ hyaline cartilage hyaline cartilage lined articular lined articular surfacessurfaces

Chondrocyte-like Chondrocyte-like cells of patelloid cells of patelloid more disorderly than more disorderly than in the patellain the patella

Patella DevelopmentPatella Development Most true sesamoids develop through Most true sesamoids develop through

endochondral ossificationendochondral ossification The patella presumably starts as a cluster of cells The patella presumably starts as a cluster of cells

w/in quadriceps-patellar tendon, then undergoes w/in quadriceps-patellar tendon, then undergoes chondrification to form hyaline cartilage masschondrification to form hyaline cartilage mass

Unlike other sesamoids, patellas ossify early in Unlike other sesamoids, patellas ossify early in ontogeny and develop in absence of mechanical ontogeny and develop in absence of mechanical stimulistimuli Though mechanical stimuli necessary for regeneration Though mechanical stimuli necessary for regeneration

(dogs) & to stimulate underdeveloped patellas in (dogs) & to stimulate underdeveloped patellas in humanshumans

Recent research suggest LMXRecent research suggest LMXIIB plays a role in B plays a role in patella development & dorso-ventral limb patella development & dorso-ventral limb patterningpatterning

Hoxa9/Hoxd9Hoxa9/Hoxd9 and and Hoxd9/Hoxd10Hoxd9/Hoxd10 mutants result mutants result in misshapen & displaced patellasin misshapen & displaced patellas

Traction EpiphysesTraction Epiphyses

Bony projections of insertion for a Bony projections of insertion for a tendon/ligament that develop independently of tendon/ligament that develop independently of the limb elementthe limb element

Proposed to be sesamoids incorporated into Proposed to be sesamoids incorporated into long bones, or sesamoids are disarticulated long bones, or sesamoids are disarticulated traction epiphyses, or that both ossicles are traction epiphyses, or that both ossicles are completely separatecompletely separate

Evidence in favor of the 1Evidence in favor of the 1stst hypothesis: hypothesis: In some mammals & birds the tibial tuberosity is In some mammals & birds the tibial tuberosity is

derived from an independent condensation derived from an independent condensation originating from w/in patellar ligamentoriginating from w/in patellar ligament

In some birds the patella is also incorporated into the In some birds the patella is also incorporated into the hypertrophic cnemial cresthypertrophic cnemial crest

Mineralized Tendons & Mineralized Tendons & LigamentsLigaments

Found in various tetrapods, most notably Found in various tetrapods, most notably birdsbirds

Tend to be slender, elongate & terminate Tend to be slender, elongate & terminate in advance of jointsin advance of joints

Development based off of studies of the Development based off of studies of the domestic turkeydomestic turkey

Tenocytes (fibroblasts) of tendons Tenocytes (fibroblasts) of tendons hypertrophy & adopt a stellate hypertrophy & adopt a stellate morphology followed by hypertrophic morphology followed by hypertrophic tenocytes producing vesicles containing tenocytes producing vesicles containing calcium & phosphorus = associated w/ calcium & phosphorus = associated w/ earliest appearance of mineralizationearliest appearance of mineralization

LunulaeLunulae

Periarticular ossicles of the knee & Periarticular ossicles of the knee & other synovial joints, nested within other synovial joints, nested within the meniscithe menisci

They form osseous wedges w/ a They form osseous wedges w/ a crescentic morphologycrescentic morphology

May serve protective & biomechanical May serve protective & biomechanical roles, such as resisting compressive roles, such as resisting compressive forces or acting as a fulcrumforces or acting as a fulcrum

Lunulae Diversity & Lunulae Diversity & DistributionDistribution

Best known in knee, though also found in Best known in knee, though also found in other joints such as the wrist & ankleother joints such as the wrist & ankle

Reported in lissamphibians, squamates, Reported in lissamphibians, squamates, birds, & a variety of mammalsbirds, & a variety of mammals

Very common in nonophidian squamates; Very common in nonophidian squamates; up to 5 elements in an individualup to 5 elements in an individual

Knee lunulae very common in rodentsKnee lunulae very common in rodents

Lunulae Development & Lunulae Development & HistologyHistology

All exists as hyaline cartilaginous precursors & All exists as hyaline cartilaginous precursors & ossify after birth/hatchingossify after birth/hatching

In humans, lunulae most often a result of In humans, lunulae most often a result of injury or pathologyinjury or pathology

Experiments w/ chick embryos suggest that Experiments w/ chick embryos suggest that development of menisci (& therefore lunulae) development of menisci (& therefore lunulae) is dependent on movement of limbs & may is dependent on movement of limbs & may result from biomechanical inductionresult from biomechanical induction

Haines (1942) hypothesized that lunulae form Haines (1942) hypothesized that lunulae form when menisci reach surpass a threshold sizewhen menisci reach surpass a threshold size

Outer layer made of lamellar bone & inner Outer layer made of lamellar bone & inner layer is cancellous bone with or without layer is cancellous bone with or without marrowmarrow

Problematic Sesamoids & Problematic Sesamoids & OssiclesOssicles Definitions of sesamoid & lunulae Definitions of sesamoid & lunulae

require knowledge of where the require knowledge of where the elements form during elements form during skeletogenesis; many ossicles only skeletogenesis; many ossicles only known from mature individualsknown from mature individuals

The panda’s “thumb” may be a The panda’s “thumb” may be a true sesamoid, a remodeled true sesamoid, a remodeled periarticular ossicle, or a periarticular ossicle, or a neomorphic derivitive of the neomorphic derivitive of the carpal seriescarpal series

Other examples include:Other examples include: the “panda’s toe” (enlarged tibial the “panda’s toe” (enlarged tibial

“sesamoid”)“sesamoid”) ““sesamoids” associated w/ digits in sesamoids” associated w/ digits in

human manus (tendons & ligaments human manus (tendons & ligaments attach secondarily)attach secondarily)

Rods & extensions that support Rods & extensions that support wings/membranes of bats, gliding wings/membranes of bats, gliding mammals & pterosaurs (pteroid)mammals & pterosaurs (pteroid)

BiomechanicsBiomechanics Most explanations for sesamoids emphasis Most explanations for sesamoids emphasis

potential current or past biomechanical functionpotential current or past biomechanical function Sesamoids & ossicles are most common in Sesamoids & ossicles are most common in

areas subject to friction, compression or torsionareas subject to friction, compression or torsion Known to sometimes occur in response to injuryKnown to sometimes occur in response to injury Connective tissue known to respond to Connective tissue known to respond to

compression/tension by altering ECM compression/tension by altering ECM composition, fiber orientation, cellular composition, fiber orientation, cellular morphology & cellular orientationmorphology & cellular orientation

Osteogenic index developed to predict the Osteogenic index developed to predict the likelihood & position of sesamoid formation likelihood & position of sesamoid formation under different stress regimesunder different stress regimes