Adaptations for Digging & Burrowing

1. Adaptations for Digging & Burrowing Ch. 17

2. 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.)

3. 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

4. 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)

5. 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

6. 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

7. 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

8. 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

9. 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

10. 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

11. 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

12. 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)

13. 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

14. 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

15. 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

16. 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

17. 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

18. 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?

19. 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

20. 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

21. 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)

22. 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

23. 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

24. 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

25. 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

26. Aquatic Adaptations in the Limbs of Amniotes Ch. 18

27. 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

28. 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)

29. 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

30. 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

31. 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

32. 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

33. 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

34. 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

35. 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

36. 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

37. 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

38. 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

39. 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

40. 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

41. 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

42. 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)

43. 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

44. 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

46. Sesamoids & Ossicles in the Appendicular Skeleton Ch. 19

47. 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

48. 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

49. 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

50. 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