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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.

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Digging burrowing l.jpg
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.)


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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


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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)


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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 burrowing-morphologies of pelvises


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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


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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


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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


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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


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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


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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


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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)


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Lepidosauria

  • Morphological specializations for limb-digging rare

  • Most specialized species: Palmatogecko rangei

  • Strongly webbed hand/feet

    • Likely evolved for locomotion over loose sand

  • Cartilaginous paraphalanges strengthen webbing more proximal than non-burrowing species


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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


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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


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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


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Mammalian Scratch-Diggers

  • Enlarged sites of attachment for forelimb muscles used in digging

    • posteroventral portion of scapula, acromion process long?, deltoid tubercle of humerus, median epicondyle, long olecranon process

  • 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

    • 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


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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?


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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


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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


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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)


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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


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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


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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


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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



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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


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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)


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Mammals: Few Swimming Adaptations

  • Shallow waders: walk in shallows, generally w/o submerging

    • Tapirs, moose, etc.

    • Little or no limb adaptations

  • Deep waders: walk on substrate beneath surface of water

    • Hippopotamus

    • May have larger &/or denser bones to counter buoyancy

  • Quadrupedal paddlers

    • Most terrestrial species

    • May have webbed feet


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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


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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


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Mammals: Pelvic Swimming III

  • Simultaneous pelvic paddling (otters)

    • Synchronous movement of hindlimbs in vertical plane

    • Similar limb morphology to APP: large, webbed feet

    • Tail & back muscles also participate

  • Dorsoventral pelvic undulation (sea otter)

    • 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


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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


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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


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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


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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


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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


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Birds: Pelvic Swimming II

  • Alternating pelvic submerged paddling (loons, hesperornithiformes)

    • Paddle backwards underwater

    • Webbed feet are reoriented far back on body

  • Lateral pelvic undulation (grebes)

    • 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


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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


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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


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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


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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)


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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


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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



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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


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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


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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

    • Tends to replace olecranon process in birds & lateral epicondyle in tree shrews & a bat (Rousettus)

  • Oldest knee sesamoid (mid-Triassic) found in Macrocnemius bassanii

    • Also found in an anuran, some lizards, mammals & birds

  • Tarsal sesamoids found in anurans, birds, lizards & primates


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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


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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


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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


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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


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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


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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


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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


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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


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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)


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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


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