Functional morphology of the forelimb musculature reflects flight and foraging styles in aquatic birds

Abstract

Aquatic birds show a great diversity of locomotion styles and wing morphologies, from penguins that are fully specialized for an aquatic life to species of aerial flyers that also use their wings for underwater propulsion (e.g. auks and shearwaters). Moving between the air–water interface exerts conflicting pressures on the body and wing anatomy of diving birds. In this work, we investigated the functional morphology of the forelimb musculature of 18 species of aquatic birds that display a variety of flight and foraging styles. Muscle architecture was related to function, with special emphasis on muscle mass. Dissections of one of the forelimbs of 20 specimens of waterbirds were performed to obtain numerical data of muscle architecture. Total wing muscle mass scaled isometrically to body mass1.0, whereas fascicle length scaled to muscle mass0.284, which is consistent with previous results of scaling in wings of raptors. A principal component analysis (PCA) of normalised muscle masses resulted in a biplot where three main morphological groups can be distinguished. Anatids (ducks and geese) occupy a space represented by muscles that are activated during downstroke. Auks and penguins clustered together in a region dominated by muscles that assist in wing elevation and showed a degree of hypertrophy. The rest of the species grouped together in the lower limits of both PCs where muscles that facilitate wing flexion–extension and stabilisation are loaded. The distribution of mass in the wing muscles of the aquatic birds seemed to be related to flight and foraging style and showed non-significant influence of shared phylogenetic history (Kmult: 0.71, p value: 0.083, 10,000 permutations).

Trends of avian locomotion in water – an overview of swimming styles

“…On the water surface, both groups apply alternate paddling (Ancel et al 2000) and during the descent and horizontal underwater swimming, much of the propulsion is provided by the strong hind feet (Johnsgard 1987). Usually, both the lesser and highly diving taxa hold their wings close to the body, and strike with them only rarely, for example during sudden turns , Owre 1967, or the phase of submergence from the surface (Kelso 1922), or in the case of some anatids, the wings are held partly extended and used as a diving plane , Brooks 1945).…”

“…Besides simultaneous symmetrical strokes, Canvasbacks (Aythya valisineria) occasionally dive with alternate (asymmetrical) strokes (Tome & Wrubleski 1988), and their wings are always folded such as in Mergus spp. , Brooks 1945, and in the case of all the above mentioned ducks (Tome & Wrubleski 1988). Steamer Ducks (Tachyeres spp.)…”

“…Several anatids -such as the White-winged Scoter (Melanitta deglandi) and Surf Scoter (Melanitta perspicillata) -extend the wings partially during and following the submergence but do not use them for propulsion (Brooks 1945). In contrast, some authors mentioned that Long-tailed Ducks (or Oldsquaw) (Clangula hyemalis) apply wing-propulsion for diving and horizontal progression , Snell 1985, however, understanding this phenomenon probably needs further observations.…”

“…However, besides the highly specialised swimmers, many examples of 'amphibious flyers' (e.g. alcids) with the ability to swim and dive, fly, and sometimes also to walk effectively are known (Storer 1945, Raikow et al 1988, Bribiesca-Contreras et al 2021. Because air and water represent highly different physical characteristics (density, viscosity, etc.…”

“…Because air and water represent highly different physical characteristics (density, viscosity, etc. ) and because of the presence of distinct mechanical loads during movements in different environments, the musculoskeletal system of birds with aquatic habits must deal with various constraints, which required tradeoffs and novel solutions in their morpho-functional adaptations (Raikow et al 1988, Habib 2010, Fish 2016, Bribiesca-Contreras et al 2021.…”