Title: How to waddle with a paddle: A study of duck hindlimb anatomy, kinematics, and muscle function across behaviors and species
Committee: Andrew Biewener (Advisor), George Lauder, Stephanie Pierce, Thomas Roberts (Brown University)
Abstract: The most impressive animal movements often arise from animals that have specialized their anatomy, muscle function, and kinematics (the way they move) for a specific behavior or environment. However, specialization may come at a cost, as most animals require their structures and muscles to perform multiple behaviors. Despite the specialization of their hindlimb (pelvic limb) for swimming, ducks are able to use their hindlimbs to move on land and to takeoff, in addition to swimming at the surface and diving. How are they able to use the same structures (the hindlimb, pelvis, and foot) and muscles that drive them to perform so many behaviors? What structures and traits are associated with their specialization for aquatic locomotion, and are there tradeoffs in locomotor ability that come with this specialization? In my dissertation, I begin to explore the answers to these questions by studying the kinematics (Ch. 1, 3), muscle function (Ch. 1, 2), and anatomy of ducks (Ch. 3) across behaviors and across the duck phylogeny.
In Chapter 1, I examined kinematics and function of a bi-articular hindlimb muscle, the lateral gastrocnemius (LG), during aquatic and terrestrial takeoffs in mallard ducks. Unlike many waterbirds, mallards are capable of vertical takeoffs from both land and water, regimes where force production and demands on the animal differ. Mallards change their kinematics and LG function with takeoff medium. Importantly, the knee moves in the opposite direction, extending during terrestrial takeoff to launch the body into the air but flexing during aquatic takeoff to contribute to caudal motion of the foot. The LG powers both ankle extension and knee flexion, so it undergoes larger excursions and higher shortening velocities during aquatic takeoffs than terrestrial, making tuning of the muscle’s force-length and force-velocity properties across takeoff media challenging.
The function of the mallard LG was explored in greater depth in Chapter 2 by focusing on how it operates during cyclical behaviors like walking and swimming. Post-activation potentiation (PAP) is a less well-studied physiological property of muscle that represents an increase in force and rate of force development in muscle after recent activation. PAP could therefore impact LG function during behaviors that require repeated muscle activation. Using an in situ muscle preparation, I controlled mallard LG cycle frequency, length change, and activation parameters to mimic surface swimming. As hypothesized, PAP affected LG function, resulting in a gradual increase in muscle force, rate of force development, and work production over several cycles despite no change in activation. The degree of PAP depended on cycle frequency. This work was novel because our knowledge of mallard LG function during cyclical behaviors in vivo allowed me to make a strong connection between these behaviors and PAP of the muscle observed in situ.
Ducks exhibit a wide range of swimming abilities, including highly terrestrial species, ducks that swim well but only at the surface, foot-propelled divers, and wing-and-foot-propelled divers. In Chapter 3, I explored how anatomy and movement relate to specialization for swimming in ducks. Some hindlimb structures differed among behavioral groups, including the proportional length of the femur and tarsometatarsus, the shape of the femur and tibiotarsus, and the lateral cnemial crest size. However, only the increased size of the cnemial crest is consistent with the anatomical features seen in other avian swimming specialists and is thought to contribute to increased knee stabilization (by increasing the moment arm of knee extensors) and to powering distal limb movement (by increasing attachment surface for the digital flexors). I examined how kinematics varied among surface swimmers (mallards), foot-propelled divers (scaup), and wing-propelled divers (eiders) during walking, surface swimming, and diving. All three species increased speed by increasing stride length for all behaviors. Cycle frequency was increased with speed only during walking, remaining constant during surface swimming and diving. Eiders increased stride length with diving speed more rapidly than the others, perhaps enabled by their simultaneous use of wings and feet. During walking, eiders used higher cycle frequencies and both eiders and scaup exhibited higher body angles, perhaps an indication of lower terrestrial stability than the surface swimming mallards.