Scale effects and morphological diversification in hindlimb segment mass proportions in neognath birds

Abstract

IntroductionIn spite of considerable work on the linear proportions of limbs in amniotes, it remains unknown whether differences in scale effects between proximal and distal limb segments has the potential to influence locomotor costs in amniote lineages and how changes in the mass proportions of limbs have factored into amniote diversification. To broaden our understanding of how the mass proportions of limbs vary within amniote lineages, I collected data on hindlimb segment masses – thigh, shank, pes, tarsometatarsal segment, and digits – from 38 species of neognath birds, one of the most speciose amniote clades. I scaled each of these traits against measures of body size (body mass) and hindlimb size (hindlimb length) to test for departures from isometry. Additionally, I applied two parameters of trait evolution (Pagel’s λ and δ) to understand patterns of diversification in hindlimb segment mass in neognaths.ResultsAll segment masses are positively allometric with body mass. Segment masses are isometric with hindlimb length. When examining scale effects in the neognath subclade Land Birds, segment masses were again positively allometric with body mass; however, shank, pedal, and tarsometatarsal segment masses were also positively allometric with hindlimb length. Methods of branch length scaling to detect phylogenetic signal (i.e., Pagel’s λ) and increasing or decreasing rates of trait change over time (i.e., Pagel’s δ) suffer from wide confidence intervals, likely due to small sample size and deep divergence times.ConclusionsThe scaling of segment masses appears to be more strongly related to the scaling of limb bone mass as opposed to length, and the scaling of hindlimb mass distribution is more a function of scale effects in limb posture than proximo-distal differences in the scaling of limb segment mass. Though negative allometry of segment masses appears to be precluded by the need for mechanically sound limbs, the positive allometry of segment masses relative to body mass may underlie scale effects in stride frequency and length between smaller and larger neognaths. While variation in linear proportions of limbs appear to be governed by developmental mechanisms, variation in mass proportions does not appear to be constrained so.

Morphology and motion: hindlimb proportions and swing phase kinematics in terrestrially locomoting charadriiform birds

“…Muscle fiber area (which serves as a proxy for muscle force) scales isometrically with body mass (Maloiy et al, 1979;Bennett, 1996), resulting in large-bodied birds having muscles that produce less force relative to their body mass than small-bodied birds, as, under isometric scaling, body mass is proportional to length 3 ; in contrast, muscle fiber area is proportional to length 2 under isometric scaling. As limb MOI is known to scale either with isometry (Maloiy et al, 1979) or positive allometry (Kilbourne, 2013), and limb and segment masses are known to scale with positive allometry (Kilbourne, 2013(Kilbourne, , 2014, large-bodied birds in general may be severely hampered in swinging their limbs more rapidly, as these traits all scale with exponents much higher than 1.0. As an allometric exponent of 2/3 characterizes how muscle fiber area scales with increasing body size under isometric scaling, the discrepancies between exponent values of 2/3 and those greater 1.0 indicate that limb MOI and segment masses increase disproportionately in comparison to the force of muscles as birds increase in size.…”

“…Specimens used to measure bone length were Zoologischer Museum Berlin (ZMB) Aves 83/17 ( pied avocet); ZMB Aves 75.116 and ZMB Aves 68.16 (Eurasian oystercatcher); and ZMB Aves 68.181 and ZMB Aves 68.125 (northern lapwing). For methodology of dissecting hindlimb segments, see Kilbourne (2014). N stride denotes the number of strides analyzed.…”

“…Distal limb segments with a high mass result in a longer radius of gyration and, consequently, a greater limb MOI (e.g. Kilbourne, 2014). However, reducing the radius of gyration via kinematic adjustments (e.g.…”

Clade‐specific evolutionary diversification along ontogenetic major axes in avian limb skeleton

“…; Schwenk ; Arthur ; Brakefield ). Nevertheless, explicit treatments of the relationship between the ontogenetic and evolutionary levels of covariation have been scarce (but see Cheverud ; Klingenberg , ). Once popular framework was the study of allometric heterochrony, which focuses on evolutionary modifications of the relationship between organismal size, shape, and developmental time (Gould ; Klingenberg ; Mitteroecker et al.…”

“…; Nudds et al. ; Hinić‐Frlog and Motani ; Kilbourne ). On the other hand, little attention has been paid on potential evolutionary biases in the system, although recent studies have provided interesting insights (Stoessel et al.…”