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Elegantcrested Tinamous Eudromia Elegans Do Not Synchronize Head

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Elegantcrested Tinamous Eudromia Elegans Do Not Synchronize Head Ibis (2014), 156, 198–208 Elegant-crested Tinamous Eudromia elegans do not synchronize head and leg movements during head-bobbing JENNIFER A. HANCOCK,1* NANCY J. STEVENS2 & AUDRONE R. BIKNEVICIUS2 1Department of Biology and Environmental Science, Marietta College, Marietta, OH, USA 2Department of Biomedical Sciences, Ohio University Heritage College of Osteopathic Medicine, Athens, OH, USA Head-bobbing is the fore–aft movement of the head relative to the body during terres- trial locomotion in birds. It is considered to be a behaviour that helps to stabilize images on the retina during locomotion, yet some studies have suggested biomechanical links between the movements of the head and legs. This study analysed terrestrial locomotion and head-bobbing in the Elegant-crested Tinamou Eudromia elegans at a range of speeds by synchronously recording high-speed video and ground reaction forces in a laboratory setting. The results indicate that the timing of head and leg movements are dissociated from one another. Nonetheless, head and neck movements do affect stance duration, ground reaction forces and body pitch and, as a result, the movement of the centre of mass in head-bobbing birds. This study does not support the hypothesis that head-bob- bing is itself constrained by terrestrial locomotion. Instead, it suggests that visual cues are the primary trigger for head-bobbing in birds, and locomotion is, in turn, constrained by a need for image stabilization and depth perception. Keywords: biomechanics, bird, locomotion, pitch. Head-bobbing, the fore–aft movement of the head suggested that head movements during walking during terrestrial locomotion in some birds, is an may reflect patterns observed during jumping and optomotor response (Friedman 1975). However, hopping in birds. When jumping or hopping, a some researchers have suggested that head- bird flexes its neck prior to the hop and extends bobbing may also be linked mechanically with the neck during the hop. If head-bobbing during aspects of locomotor biodynamics. Head-bobbing walking is simply part of the same locomotor has two distinct phases: a hold phase and a thrust behavioural complex as head movements during phase (Dunlap & Mowrer 1930). During the hold jumping and hopping, then any visual function of phase, the head is immobile (remains fixed in head-bobbing is likely to be secondarily derived. space) as the body travels forward, creating an Dagg (1977) further suggested that head move- illusion of backward movement of the head. The ment during thrust phase of the head-bob assists flexibility of the neck in birds (Van Der Leeuw with shifting the bird’s centre of mass (COM) et al. 2001) allows the head to remain stable as forward as each leg begins to swing forward. the body moves forward. During the thrust phase, Importantly, head-bobbing frequency appears to the speed of the head is greater than the speed of be speed-dependent, such that as the forward the body, such that the head is translated to a speed of the bird increases, the proportion of the point in front of the body. Daanje (1951) noted stride spent in the hold phase decreases linearly that the beginning of the thrust phase often occurs (Davies & Green 1988). At relatively high speeds, with the leg touchdown, whereas the beginning of flexion and extension of the neck occur without a the hold phase often occurs with leg liftoff, and ‘hold phase’ to stabilize the head relative to the environment. At the fastest speeds, head move- *Corresponding author. ment is absent and the neck is extended in a Email: [email protected] constant thrust phase. © 2013 British Ornithologists’ Union Head-bobbing and terrestrial locomotion 199 Evidence suggesting that head-bobbing affects americana (Cronin et al. 2005). Although the locomotor mechanics was found in a study of mechanics of terrestrial locomotion have been Black-headed Gulls Chroicocephalus ridibundus evaluated in a variety of birds (Clark & Alexander (Fujita 2006). Differences in stride characteristics 1975, Gatesy 1999, Abourachid & Renous 2000, were revealed in a comparison of head-bobbing Reilly 2000, Verstappen & Aerts 2000, Aboura- and non-head-bobbing strides, with an increase in chid 2001, Hancock et al. 2007), only four studies stride length and decrease in stride frequency integrate locomotor mechanics with data on head- when Black-headed Gulls bobbed their heads bobbing. Data on both leg and head kinematics during walking. are reported for pigeons (Fujita 2002), gulls (Fujita Yet other evidence suggests that head move- 2006), and egrets, stilts and herons (Fujita 2003, ments are not always mechanically linked to loco- Fujita & Kawakami 2003). Only two studies motor movements. Neither birds walking on (Fujita 2002, 2003) have analysed the coordina- treadmills nor blindfolded birds exhibit head-bob- tion of leg and head movements, and concluded bing behaviours (Frost 1978, Necker et al. 2000), that the beginning of the hold phase began slightly presumably because a streaming visual signal is after the liftoff of a leg and the beginning of the suppressed. Also, head-bobbing has been observed thrust phase occurred slightly before the touch- during landing when the legs are held against the down of a leg (Fig. 1). However, this conclusion body (Green et al. 1994). Hence, head-bobbing was drawn from the mean values of the difference birds can and do have leg movements without in timing of head and leg movements. In reality, head-bobs, as well as head-bobs without leg move- when considering the ranges and standard devia- ments. Indeed, head-bobbing may be induced by tions of kinematic variables, both studies found the need to process particular types of visual considerable variability in the coordination of signals. The hold phase is believed to function in head and leg movements, suggesting that they stabilizing an image on the retina and detecting lacked the precise coordination that might be the motion of objects in the environment (Dunlap expected were they part of a synchronized loco- & Mowrer 1930, Davies & Green 1988). In con- motor complex. trast, the thrust phase is thought to facilitate Although coordination of head and leg move- motion parallax to generate depth perception: the ments during head-bobbing behaviours has been movement of the head during thrust causes objects suggested, all studies that have directly measured closer to the bird to appear to move faster than head-bobbing and leg events have found consider- objects farther away (Frost 1978). Moreover, the able variation in their timing. Fujita (2002) thrust phase may allow for differentiation of sta- measured the duration between head-bobbing and tionary items against a background (Davies & footfall events in pigeons, but reported the Green 1988), an important factor for foraging birds. For example, Black-headed Gulls head-bob while foraging, but do no head-bob when they engage in non-foraging walking (Fujita 2006). Sim- ilarly, Pacific Reef Herons Egretta sacra and Grey Head Herons Ardea cinerea cease head-bobbing when Left foot they are not foraging (Fujita & Kawakami 2003). The kinematics of head-bobbing have been studied most extensively in domestic pigeons Right foot Columba livia (Dunlap & Mowrer 1930, Frost Sagittal coordinates Left foot 1978, Davies & Green 1988, Wohlschl€ager et al. 1993, Troje & Frost 2000, Fujita 2002). Docu- mentation of head-bobbing kinematics in other Time species has been limited to domestic chickens Gallus gallus (Dunlap & Mowrer 1930, Bangert Figure 1. Fujita’s (2002) proposed coordination of head = 1960, Pratt 1982), starlings (Sturnidae; Dunlap & (dashed line sagittal movements (i.e. movements in the x- axis) of the head) and leg movements (white and grey Mowrer 1930), African Collared Doves Streptopelia boxes = stance phases – the beginning of each box is the risoria (Friedman 1975), Little Egrets Egretta time of foot touchdown and the end of each box is the time of garzetta (Fujita 2003) and Whooping Cranes Grus liftoff) in a walking pigeon (modified from Fujita 2002). © 2013 British Ornithologists’ Union 200 J. A. Hancock, N. J. Stevens & A. R. Biknevicius durations as frames and did not calculate values force platform (plate type 9281B; Amherst, NY, relative to stance duration. Using reported values USA) built into a 4.9-m trackway. As the birds for mean, maximum and minimum durations, moved naturally along the trackway, a range of together with mean stance duration, an estimate of speeds was recorded. Force platform dimensions the variation in the pigeon dataset can be made: were adequate in length (0.6 m) to capture two to the relative duration from the beginning of hold five steps during each trial, depending on the to liftoff would range from À36 to 29% stride lengths of a given sequence. The force plat- (mean = À8% Æ sd = 13%) and the relative dura- form recorded vertical, fore–aft (longitudinal) and tion from the beginning of thrust to touchdown mediolateral (transverse) ground reaction forces would range from À22 to 29% (17 Æ 9%). Using (GRFs) at 1000 Hz. Video and force data were reported values for Little Egrets (Fujita 2003), the synchronized using MOTUS motion analysis software relative intervals from the beginning of hold to (version 7.2.6; Peak Performance Technologies, liftoff would range from À5 to 37% of stride Centennial, CO, USA). durations (8 Æ 9%) and the relative intervals from the beginning of thrust to touchdown would range Locomotor kinematics from À25 to 17% (À0.3 Æ 9%). Although defini- tive assessment can only be obtained from the raw Reflective markers were attached to the base of data, it appears that much variation in timing of the claw of the third digit, synsacrum (between head-bobs was documented for both pigeons and the femoral heads, approximating the acetabulum) Little Egrets. and breast (between the furcula and keel). Each The first aim of this study was to evaluate the marker, in addition to the left eye, was digitized in relationship between head-bobbing and footfall every frame within a trial using MOTUS software pattern over a range of speeds.
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