Foot shape in arboreal birds: two morphological patterns for the same pincer‐like tool

Abstract

The feet are the only contact between the body and the substrate in limbed animals and as such they provide a crucial interface between the animal and its environment. This is especially true for bipedal and arboreal species living in a complex three-dimensional environment that likely induces strong selection on foot morphology. In birds, foot morphology is highly variable, with different orientations of the toes, making it a good model for the study of the role of functional, developmental, and phylogenetic constraints in the evolution of phenotypic diversity. Our data on the proportions of the phalanges analyzed in a phylogenetic context show that two different morphological patterns exist that depend mainly on habitat and toe orientation. In the anisodactyl foot, the hallux is the only backward-oriented toe and is enlarged in climbing species and reduced in terrestrial ones. Moreover, a proximo-distal gradient in phalanx size is observed depending on the degree of terrestriality. In the two other cases (heterodactyl and zygodactyl) that have two toes that point backward, the hallux is rather small in contrast to the other backward-pointing toe, which is enlarged. The first pattern is convergent and common among tetrapods and follows rules of skeletal development. The second pattern is unique for the clade and under muscle-morphogenetic control. In all cases, the functional result is the same tool, a pincer-like foot.

The skin of birds' feet: Morphological adaptations of the plantar surface

“…Most often, it connects the first phalanges on two forward toes. However, Abourachid et al (2017) showed that the proportions of the phalanges change in arboreal birds. In zygodactyl birds, the part of the toes linked by the skin, that is, the proximal phalanx of the toe II, is rather narrow compared to anisodactyl birds.…”

“…However, recent papers suggested the anisodactyly of the Passeriformes is derived from a zygodactyl foot (Botelho, Smith-Paredes, Soto-Acuña, et al, 2015;Botelho, Smith-Paredes, Nuñes-Leon, Soto-Acuña, & Vargas, 2014;Vargas et al, 2017). Abourachid, Fabre, Cornette, and Höfling (2017) analyzed the anisodactyl, zygodactyl, and heterodactyl forms of bird feet. They pointed out that two distinct functional patterns permit the adaptation of the foot to an arboreal life, depending on toe orientation: in the anisodactyl foot, the hallux is the only backward-oriented toe and it is enlarged in perching species and reduced in terrestrial ones; in the zygodactyl and heterodactyl birds, where two toes point backward, the hallux is small and the other toe is enlarged.…”

“…There is vast knowledge about different aspects of the bird foot, mainly with regard to toe orientation and development (e.g., Abourachid et al, 2017; Bock & Miller, 1959; Botelho et al, 2014; Botelho, Smith‐Paredes, Soto‐Acuña, et al, 2015; Botelho, Smith‐Paredes, & Vargas, 2015; de Bakker et al, 2013; Raikow, 1985; Tokita, Matsushita, & Asakura, 2020). Nevertheless, association between the keratinous plantar surface, of ectoderm origin, and skeletal structure of toes, of mesoderm origin, has been little explored with regard to functional foot use by birds.…”

Scaling of avian bipedal locomotion reveals independent effects of body mass and leg posture on gait

“…Foot morphology and function is one particularly under-explored aspect of avian gait dynamics. Bird foot morphology is diverse, and control of foot-substrate interactions is likely to be crucial in effective movement and balance (Abourachid et al, 2017;Backus et al, 2015). Yet, the relationship between foot form and function remains poorly understood.…”

“…Yet, the relationship between foot form and function remains poorly understood. Foot shapes range from the relatively basal and common anisodactyl foot (with digit 1 backward, digits 2-4 forward) to the next most frequent arrangements of heterodactyl and zygodactyl feet, which both have two toes facing forwards and two toes backwards (Bock and Miller, 1959), and the more derived pamprodactyl foot (Collins, 1983), with two inner toes forward and two outer toes that can rotate forward and backwards (Abourachid et al, 2017;Botelho et al, 2014;Livesey and Zusi, 2006). Foot morphology appears to be a relatively plastic developmental structure across the avian lineage, which may have facilitated the observed diversity in foot anatomy (Botelho et al, 2015a,b).…”