Precocial development of locomotor performance in a ground-dwelling bird (Alectoris chukar): negotiating a three-dimensional terrestrial environment - PubMed (original) (raw)

Precocial development of locomotor performance in a ground-dwelling bird (Alectoris chukar): negotiating a three-dimensional terrestrial environment

Brandon E Jackson et al. Proc Biol Sci. 2009.

Abstract

Developing animals are particularly vulnerable to predation. Hence, precocial young of many taxa develop predator escape performance that rivals that of adults. Ontogenetically unique among vertebrates, birds transition from hind limb to forelimb dependence for escape behaviours, so developmental investment for immediate gains in running performance may impair flight performance later. Here, in a three-dimensional kinematic study of developing birds performing pre-flight flapping locomotor behaviours, wing-assisted incline running (WAIR) and a newly described behaviour, controlled flapping descent (CFD), we define three stages of locomotor ontogeny in a model gallinaceous bird (Alectoris chukar). In stage I (1-7 days post-hatching (dph)) birds crawl quadrupedally during ascents, and their flapping fails to reduce their acceleration during aerial descents. Stage II (8-19 dph) birds use symmetric wing beats during WAIR, and in CFD significantly reduce acceleration while controlling body pitch to land on their feet. In stage III (20 dph to adults), birds are capable of vertical WAIR and level-powered flight. In contrast to altricial species, which first fly when nearly at adult mass, we show that in a precocial bird the major requirements for flight (i.e. high power output, wing control and wing size) convene by around 8 dph (at ca 5% of adult mass) and yield significant gains in escape performance: immature chukars can fly by 20 dph, at only about 12 per cent of adult mass.

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Figures

Figure 1.

Figure 1.

Birds were filmed while performing WAIR or CFD (a) with four synchronized high speed (250 frames s−1) digital video cameras, which were placed so that all points on the right wing were in view in at least two cameras at all times during the wing beat. (b) Kinematics during WAIR and CFD were calculated based on two frames of reference: the global frame had a fixed origin and orientation of axes and the vertebral frame had an origin fixed to the shoulder of the bird and oriented along the rump–shoulder axis.

Figure 2.

Figure 2.

The ontogeny of locomotor performance during WAIR (closed circles; adapted from Dial et al. 2006) and CFD (open squares; bottom panel). We define three stages of ground-bird locomotor morphology based on behaviour and correlated performance. Stage I (1–7 dph) is marked by quadrupedal crawling and virtual free fall (mean acceleration is not different from a golf ball or a bird with wings bound to its side). In stage II (8–19 dph), birds use WAIR to ascend and significantly slow descent, and in stage III (20 dph to adult), birds are capable of level-powered flight. Maximum angle determined as the steepest ascended by four of five chicks. Descent performance presented as mean ± s.e.m. acceleration of chicks (n = 4) in flapping descent from a 1 m high platform.

Figure 3.

Figure 3.

Dynamic morphometrics during WAIR (closed squares) and CFD (open squares) for 1–58 dph birds. (a) Mass increases slowly so that at the stage I–II transition (7–8 dph) chicks are ca 5 per cent of adult mass and are ca 10 per cent of adult mass when they are first capable of level flight (stage III, 20 dph). (b) Dynamic wing loading and (c) disc loading, calculated from three-dimensional kinematic measurements of wing area and wing-swept area, respectively, demonstrate the positively allometric wing growth relative to body mass from 1 to 20 dph. Data presented as mean ± s.e.m. (n = 3 birds in WAIR, n = 4 in CFD). Asterisk indicates significant difference (p < 0.05) from 58 dph level.

Figure 4.

Figure 4.

Kinematic measurements related to aerodynamic force production. (a) Mean body velocity during WAIR increases until 36 dph. Both stroke amplitude (b) and wing-beat frequency (c) during WAIR reach or surpass 58 dph values by 8 dph. Asterisk indicates significant difference (p < 0.05) from 58 dph level. Open squares, flight/CFD; filled squares, 65° WAIR.

Figure 5.

Figure 5.

Kinematic measurements related to control of the (a–c) wing, averaged across the middle 70 per cent of each downstroke, or the body (d), averaged through an entire run. Global stroke angle (a) and vertebral stroke angle (b) do not differ from 58 dph values after 8 dph for WAIR and are similar during CFD in the global frame of reference, but are higher (more caudally cranially oriented) in the vertebral during CFD. The geometric angle of attack of the hand wing from 3 to 8 dph is among the highest published for birds (see text for details), but it falls to 58 dph values by 10 dph. Wing-control kinematics (a–c) show that chicks gain near-adult levels of control around the stage I–II transition. Body angle (d) is low (more horizontal) only during stage I, as the chicks often maintain contact between the inclined substrate and their chests. Asterisk indicates significant difference (p < 0.05) from 58 dph level. Open square, flight/CFD; filled square, 65° WAIR.

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