When hatchlings outperform adults: locomotor development in Australian brush turkeys (Alectura lathami, Galliformes)

Abstract

Within Galliformes, megapods (brush turkey, malleefowl, scrubfowl) exhibit unique forms of parental care and growth. Hatchlings receive no post-hatching parental care and exhibit the most exaggerated precocial development of all extant birds, hatching with fully developed, flight-capable forelimbs. Rather than flying up to safety, young birds preferentially employ wing-assisted incline running. Newly hatched Australian brush turkeys (Alectura lathami) are extraordinarily proficient at negotiating all textured inclined surfaces and can flap-walk up inclines exceeding the vertical. Yet, as brush turkeys grow, their forelimb-dependent locomotor performance declines. In an attempt to elucidate how hatchlings perform so well, we analysed hindlimb forces and forelimb kinematics. We measured ground reaction forces (GRFs) for animals spanning the entire growth range (110 -2000 g) as they ascended a variably positioned inclined ramp that housed a forceplate. These data are compared with a similar dataset for a chukar partridge (Alectoris chukar) that exhibit a growth strategy typical of most other Galliformes and that demonstrate improved incline performance with increasing age. The brush turkeys' ontogenetic decline in incline running performance is accompanied by loss of traction at steep angles, reduced GRFs and increased wing-loading. We hypothesize that Australian brush turkeys, in contrast to other Galliformes, develop from forelimb-dominated young that exploit a variable terrain (e.g. mound nests, boulders, embankments, cliffs, bushes and trees) into hindlimb-dominated adults dependent on size and running speed to avoid predation.

Evolution of avian flight: muscles and constraints on performance

“…Even if locomotor strategies such as WAIR are ultimately discounted as valid models of the origin of avian flight, they appear to be important components of the development of locomotor capacity during ontogeny in living birds [38,41,43,44] and in the behavioural repertoire of adult birds [26,43]. They may be critical for survival and contribute to the evolution of alternative life-history strategies given the intense predation pressure upon the nestlings of some species [60].…”

“…They may be critical for survival and contribute to the evolution of alternative life-history strategies given the intense predation pressure upon the nestlings of some species [60]. In some circumstances, WAIR may be a readily employed mode of climbing in adults because of adverse scaling of available power for flight [43], or because the species evolved on cliffs [26]. Almost all of our insight about these styles of locomotion comes from laboratory studies, so new field studies in a comparative context are critical for improving understanding of the ecological relevance, testing the ubiquity, of these styles of locomotion that integrate the use of the hindlimb and forelimb modules [61].…”

“…This behaviour has been studied extensively in ontogenetic series up to adults in several species of Galliform birds [32,[38][39][40][41][42][43] and in adult pigeons (C. livia; [26]). Additionally, wing-assisted swimming and branching behaviour are described for developing ducks (Anseriformes) and owls (Strigiformes; [44]).…”

(How) do animals know how much they weigh?

“…juveniles tend to suffer relatively high mechanical stresses in their musculoskeletal designs (Allen et al, 2010;Dial and Jackson, 2011;Main and Biewener, 2006;Smith and Wilson, 2013). Stress similarity or considerations of durability may be less important to a juvenile animal than maximizing burst performance, because of life history and environmental demands (e.g.…”

Kinematics of quadrupedal locomotion in sugar gliders (Petaurus breviceps): effects of age and substrate size

“…This may be particularly true with regard to arboreal habitats, where substrate navigation is complex, locomotor stability is at a premium, and selection pressures on juveniles might be enhanced (Lawler, 2006;. Previous biomechanical studies of locomotor ontogeny have documented heightened, even adult-like, levels of performance in a host of juvenile animals, including crickets (Dangles et al, 2007), fish (Hale, 1996;Gibb et al, 2006), birds (Dial and Jackson, 2011), salamanders (D'Aout and Aerts, 1999;Landberg and Azizi, 2010), lizards (Irschick, 2000;Toro et al, 2003), frogs (Emerson, 1978), guinea pigs (Trillmich et al, 2003), jackrabbits (Carrier, 1995), horses (Grossi and Canals, 2010), gnu (Pennycuick, 1975) and elephants (Hutchinson et al, 2006). Such studies have generally focused on acceleration, sprint speed and jumping distance, aspects of locomotor performance thought to be crucial for escaping predators and promoting juvenile survival.…”