© 2001 by The Society for Integrative and Comparative Biology
Control of the Cranio-Cervical System During Feeding in Birds1
1 Department of Evolutionary Morphology, Institute of Evolutionary and Ecological Sciences, Leiden University, Kaiserstraat 63, 2311 GP Leiden, The Netherlands
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The avian neck is a complex, kinematically redundant system, which plays a role during inter alia food prehension and manipulation. Kinematical analysis shows that chickens (Gallus domesticus) move their vertebrae according to a geometric principle that maximizes angular rotation efficiency. The movement pattern shows simultaneous rotations in some joints, while not in the others. Anseriformes show a pattern of successive, rather than simultaneous rotations in the rostral part of the neck. A kinematical model indicates that the geometric principle produces an anseriform-like pattern only if a constraint on the movement of the caudal vertebrae is introduced. The strength of this constraint, required for a realistic simulation, is related to the amount of stretch in the long dorsal neck muscles (M. biventer and M. longus colli dorsalis), which have a different configuration in Anseriformes compared to the chicken. To investigate whether the difference in movement pattern is a result of differences in anatomy only, or also of differences in neuromotor patterns, the EMG-patterns of the neck muscles of the mallard and chicken during drinking and pecking were studied. Considerable overlap in the activity of antagonists is found in mallards, but not in chickens. Muscles in the rostral part of the neck are activated successively in mallards, but simultaneously in chickens. We conclude that the difference in movement patterning between chickens and Anseriformes, results from both a difference in the control system of the neck, and a difference in the anatomy. The anseriform pattern is found in water as well as on land, which suggests that neck movement in both environments is controlled by the same neuromotor patterns. The modifications in motor control system and anatomy of the Anseriformes may have evolved as an adaptation to aquatic feeding, since the anseriform pattern is energetically more beneficial in an aquatic environment than on land.
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INTRODUCTION |
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A key question in the study of evolution is how complex organismal systems change, while maintaining the integration of the various components. Changes in one part of the system may have consequences for the performance of other parts and may affect the performance of the system as a whole. Neuromotor patterns are believed by some to be conserved in evolution (Lauder, 1991
; but see Goslow et al., 2000), while diversification occurs at the level of musculo-skeletal design (Roth and Wake, 1989). The similarities in neuromotor patterns and kinematics during feeding in vertebrates led to the postulation of a "Generalized Feeding Cycle" by Bramble and Wake (1985).
The great diversity of the trophic system in birds has been the subject of many studies (reviewed by Zweers et al., 1994a). However, descriptions of the anatomy, kinematics, feeding mechanisms, performance, and sensory and motor control are available only for a few species (e.g., Anas platyrhynchos, Columba livia, Gallus domesticus) and the available data on the evolution of motor patterns during feeding in these species is limited (Zweers, 1982; Dubbeldam, 1984; Berkhoudt, 1985; Klein et al., 1985; Kooloos and Zweers, 1991; Van den Heuvel, 1992; Heidweiller et al., 1992a; Bout, 1994; Bout and Zeigler, 1994; Van Gennip and Berkhoudt, 1994). The results show that the Generalized Feeding Cycle is not found often in birds (Smith, 1994; Bout, 1998). Even when the kinematics of food intake, such as the tongue assisted intra-oral transport of seeds in Pigeons ("slide and glue"), resembles the Generalized Feeding Cycle quite well, the underlying EMG motor pattern is totally different.
Motor patterns are variable and modifiable by peripheral sensory input, as well as by descending central control mechanisms. Therefore, it is difficult to discriminate between differences in motor patterns that are due to perhaps small differences in functional demands, or to fundamental differences in the control of the trophic system.
In contrast to the jaw apparatus of birds, in which functional demands mainly comprise opening and closing, the neck system has to meet a wide variety of functional demands in terms of different head trajectories during many different behaviors (Zweers et al., 1994b): food acquisition, head balancing during locomotion, orientation, preening, display, etc. The neck system in birds is kinematically redundant and comprises many more degrees of freedom, than are required to move the head, due to the large number of articulating elements (Bout, 1997). Therefore, a large number of different movement patterns may move the head from one position to another, relative to the body. The kinematical redundancy of the neck makes it an interesting subject for studying the evolution of motor patterns, since the number of possible solutions for a similar functional demand (head trajectory) is much larger than in the jaw apparatus of birds.
Most studies have connected anatomical features of the avian neck to feeding habits or foraging methods (Palmgren, 1949; Zusi, 1962; Zusi and Storer, 1969; Burton, 1974; Zusi and Bentz, 1984; Fritsch and Schuchmann, 1988), but without including an analysis of the neck movement pattern. The selection of head trajectories for the analysis of neck movement patterns is difficult since only a few bird species show extreme functional demands in terms of velocity or force on the neck system, like the darting stroke in the heron (Kral, 1965) or pounding in woodpeckers (Spring, 1965; Kirby, 1980). In most bird species no extreme functional demands on the neck are found, which leaves open the possibility that in many species the neck is adapted to the economics of continuous and varied movement, rather than extreme functional demands.
Here, we focus on the general characteristics of neck movement patterning, by comparing a variety of head trajectories. The head trajectories are considered as the functional demands on the neck system, instead of selecting a specific behavior as the functional demand. If species show fundamental differences in neck movement patterning, the motor patterns can be compared for similar head trajectories as a first step to study evolutionary change in motor control. In this paper a number of studies (Van der Leeuw, 1992; unpublished data, A.V.D.L.) are reviewed to compare the characteristic neck movement and motor patterns between chicken and Anseriformes during goal directed head movements.
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THE AVIAN NECK SYSTEM |
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The avian neck comprises 12 to 24 cervical vertebrae. The vertebrae articulate around a saddle-shaped joint (articulatio intercorporalis) at the base of the vertebral body and two sliding joints at the top (articulatio zygapophysialis). As a result, relatively large dorsoventral and small lateral rotations are possible. Boas (1929)
divided the avian cervical column into three major flexion regions: the most rostral region 1 allows mainly ventral flexion, region 2 allows mainly dorsal flexion and region 3 allows both ventral and dorsal flexions but only to a limited extent (Fig. 1).
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Variables of the cervical column are the total number of vertebrae, the number of vertebrae in each of the three flexion regions, and vertebral dimensions (Boas, 1929
; Van der Leeuw, 1992; Van der Leeuw et al., 2001). For example, the number of vertebrae in Anseriformes ranges from 16 in ducks to 24 in swans; the 8 additional vertebrae in swans are all situated in region 1. The cervical musculature (Fig. 2) consists of a large number of muscle slips, assembled in a complex configuration, usually crossing more than one joint (Vanden Berge and Zweers, 1993). Four muscle subsystems may be recognized: a cranio-cervical (between the head and rostral part of the neck), a dorsal, a ventral and a lateral subsystem.
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Differences in cervical anatomy are in part due to scaling effects (Van der Leeuw, 1992
), and the basic design of the neck musculature is very similar across a wide range of species. For example, the neck anatomy of similarly sized mallards and chickens differs only slightly (Landolt and Zweers, 1985; Zweers et al., 1987; Van der Leeuw et al., 2001). The mallard, in contrast to the chicken, has one additional vertebra in the rostral region, two slips in the M. splenius accessorius instead of one, and up to four slips in each unit of the M. cervicalis ascendens instead of two. Another difference concerns the characteristics of the fascia around the long dorsal neck muscles (M. biventer and M. Longus colli dorsalis) that cross over the caudal loop in Anseriformes instead of remaining close to the cervical vertebrae as in chickens (Fig. 3). As a result, the length of the long dorsal neck muscles in Anseriformes increases up to 25% (unpublished data, A.V.D.L.) of total neck length from an upright posture (–20° between the line through processus occipitalis and notarium, and the horizon) to an extended downward posture (+50° between the line through processus occipitalis and notarium, and the horizon).
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NECK MOVEMENT IN THE CHICKEN AND ANSERIFORMES |
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In order to ascertain general characteristics of neck movement patterns in the mallard, approach and return movements of the head to goals at various distances and heights were studied during drinking and pecking. Despite variation in the extent and direction of the head trajectories, all movement patterns have two waves of vertebral rotations in common. For descriptive purposes, we use the terms "rostral loop" and "caudal loop" of the S-shaped neck to describe neck movements. These loops are determined by the neck posture, not by the anatomical regions as described earlier. In the neck movement pattern that is characteristic of Anseriformes, the two waves occur in the rostral loop of the S-shaped neck, which comprises region 1 and the rostral half of region 2 in the mallard (see the shaded area in Fig. 4A). Within the rostral loop, the two waves start only a few joints apart, and then run from rostral to caudal during down strokes (Fig. 4B) and vice versa during upstrokes. The two waves show considerable overlap, which means that a number of joints in the rostral loop first show rotations of one wave and then the rotations of the other wave (Fig. 5B actual neck movement). The direction of the rotations in these waves depends on whether the head is protracted (vertebrae in first wave move dorsad, in the second wave ventrad, Fig. 4B) or is retracted (rotations reversed). These two waves of rotations are also found in seven other anseriform species during upstrokes and down strokes in large and small vertical and horizontal head trajectories (Van der Leeuw, 1992
). These two waves of rotations result in a rolling pattern in the rostral loop of the neck, in which the outline of the loop remains more or less the same, but the vertebrae move through the outline of the loop from rostral to caudal or vice versa, leading to a change in the length of the segments that form the rostral loop (Fig. 4).
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The neck movement pattern of the chicken is characterized by simultaneous, rather than successive rotations in the caudal loop of the S-shaped neck, as well as a large contribution of the body, both in a rotation and translation, to the neck movement (Heidweiller et al., 1992b
). The caudal loop is composed of anatomical regions 2 and 3 (see the shaded area in Fig. 4A). Instead of a change in length of the ‘bars' as in the rolling pattern, the angle between the bars of the caudal loop changes during neck movement in the chicken (Fig. 4). This lever pattern is found in all kinds of neck movements of chickens (unpublished data, A.V.D.L.). The caudal loop widens during a head protraction, because the vertebrae in the middle of the caudal loop rotate to ventral and vice versa during a head retraction.
To summarize, mallards and chickens differ in the general characteristics of neck movement during various kinds of head trajectories, such as a rolling pattern in the rostral loop in the mallard, versus a lever pattern in the caudal loop of the chicken. Differences in head trajectories follow from differences in amplitudes of the characteristic rotations, the number of joints involved, and additional rotations to move the neck relative to the body, or the head relative to the neck. An example of these additional rotations is the short wave of rotations to dorsal in the rostral part of the neck in Anseriformes during the drinking upstroke, to elevate the head to a vertical position (Van der Leeuw, 1992). Another example is the wave of rotations that runs from rostral to caudal in the caudal part of the neck, to assist in the elevation of the whole neck during large vertical head trajectories like the drinking upstroke, which is found in both the mallard and the chicken. The occurrence of these additional waves varies, with one important exception: during a down stroke, the caudal loop in Anseriformes is not lowered any further than in the resting posture, in contrast to the chicken. In aquatic feeding, the caudal loop is even elevated during immersion of the head and neck, which is completely opposite to the pattern of chickens (see below).
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THE KINEMATICAL MODEL |
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Since the general characteristics of neck movement patterns are fundamentally different in the mallard and the chicken, neck movement patterns should also differ when the functional demands (starting posture, head trajectory, body movement) are the same. Because starting postures and head trajectories are difficult to manipulate experimentally, a kinematical model is used.
Heidweiller et al. (1992b) suggested that the lever pattern in the chicken may be explained as the result of a simple rule for the movement of individual vertebrae: the amount of rotation for each vertebra is proportional to its contribution to the decrease in distance of the head towards the target. In other words, the largest rotations occur for those vertebrae that move the head over the largest distance towards the target, while vertebrae that do not contribute to a decrease in distance should not move. This rotation rule minimizes the amount of rotation of the chain required for a given distance along the head trajectory and maximizes rotation efficiency over the whole cervical chain. For any given head trajectory and starting posture, a kinematical model that optimises this movement principle can resolve kinematical redundancy by distributing rotations over the vertebrae proportional to their angle and distance with the desired head trajectory. Bout (1997) showed that optimising rotations between successive postures does predict a large variety of static neck postures. A model that implements the minimal rotation rule and generates successive postures along a head trajectory was used to simulate neck movement patterns from observed starting postures and head trajectories. Such a model simulates neck movement during drinking and pecking down strokes and upstrokes for the chicken quite well. However, the same model did not produce an anseriform neck movement pattern, when the head trajectory and starting posture of the mallard were used as input (Fig. 5). The model is able to produce waves of rotation as was found for rolling patterns in the caudal loop of Rhea (unpublished data, A.V.D.L.). Comparison of simulated and observed postures suggests that the difference in overall posture is caused by the absence of movement of the most caudal vertebrae. The anseriform pattern is correctly simulated when the movement of the caudal vertebrae is constrained in the model, suggesting that the geometric principle only applies to the rostral part of the neck in Anseriformes.
The observed trajectories of chicken and mallard differ, but the kinematical model suggests that this difference in trajectories does not explain the difference in vertebral rotation patterns. When a chicken neck is used to simulate a mallard head trajectory, it still produces a lever pattern. Moreover, when a mallard neck is used to simulate a chicken head trajectory (including a constraint on movement of the caudal vertebrae), it still produces a rolling pattern in the rostral loop.
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MOTOR PATTERNS DURING FEEDING |
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The results of the kinematical model suggest that a constraint on the movement of the caudal vertebrae in the mallard may cause the difference in neck movement patterns. The strength of this constraint, required for a realistic simulation, is related to the amount of stretch in the long dorsal neck muscles (M. biventer and M. longus colli dorsalis), which have a different configuration in Anseriformes compared to the chicken (see Fig. 3). From a biomechanical point of view, it is theoretically possible that a change in passive forces related to the stretching of the long dorsal neck muscles results in a different movement of the whole neck. However, the motor control of the neck system might also be fundamentally different between the chicken and the mallard. Muscle activity patterns were recorded for seven cervical muscle slips (see Fig. 2) in five mallards and four chickens during various head trajectories of pecking and drinking. Since the focus is on general characteristics of neck movement patterning, EMG signals were averaged over all feeding bouts and individuals per species, and are summarized in Figures 6 and 7. The M. longus colli ventralis pars cranialis (VCR) is ventral to the rostral loop, and the pars caudalis (VCA) is located ventrally to the caudal loop. The activity of two slips of the M. longus colli dorsalis pars cranialis (DCR1, DCR2) were recorded. These muscles and the M. splenius accessorii 5 (SPL) are located dorsal to the rostral loop. The activity of two slips of the M. longus colli dorsalis pars cranialis (DCA1, DCA2) and of the M. cervicalis ascendentes (CA1, CA2) were recorded, and these muscles are located dorsal to the caudal loop.
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Filterfeeding/pecking (Fig. 6)
Filterfeeding in the mallard is characterized by an approach towards the water, a filterfeeding phase with the bills immersed, a return phase and a swallowing phase. The approach, return and swallowing phases are comparable to those in pecking chickens. The filterfeeding phase is highly variable and cannot be compared to the short grasp of a chicken. Neck movement during the approach and return of filterfeeding comprises only the characteristic rolling pattern in the rostral loop, additional rotations to manipulate the head relative to the neck or the head relative to the neck are not required. The neck movements during pecking are small and during the return, the head shows less upward rotation than during drinking.
Muscle activity patterns during both the approach and the return are characterized by co-activation of the ventral (VCR, VCA) and dorsal (DCR, SPL, DCA, CA) muscles, although EMG amplitude of the ventral muscles is much larger than of the dorsal muscles during the approach phase and vice versa during the return. The slips of the DCR are not active during the approach. The successive activity of the DCR slips during the upstroke parallels the successive rotations from caudal to rostral of the kinematical rolling pattern in this area. Although the rolling pattern is also present during the approach, the EMG pattern of filterfeeding does not show successive activity in the VCR and VCA as clearly as during drinking (see next section). It is possible that the successive activity during pecking is limited to the VCR slips on the ventral side of the rostral loop. Unfortunately, the activity of only one slip of the VCR was recorded.
In the chicken, the ventral muscles show synchronous activity at the start of the approach, which is followed by activity in the dorsal muscles, including the DCR slips. During the return movement, activity in the dorsal muscles is followed by activity in the ventral muscles.
Drinking (Fig. 7)
Drinking in the mallard is characterized by an approach towards the water, immersion of the bills, upstroke of the head, and swallowing with the head tipped up. A rolling pattern is found in the rostral loop during the approach and the upstroke, but at the end of the upstroke, an additional wave of rotations in opposite direction (rostral to caudal) is found in the caudal part of the neck, to elevate the neck relative to the body. The muscle activity patterns are quite similar to the approach and upstroke of filterfeeding. Ventral and dorsal muscles are co-activated and DCR slips are not active during the approach. During the down stroke, the ventral muscles (VCR and VCA) show successive activity peaks that coincide with the direction of the rotations in the rostral loop, while subsequent activity of the DCR slips are found during the upstroke. A difference with filterfeeding is that the dorsal muscles (DCA and CA) in the caudal part of the neck show subsequent activity during the drinking upstroke, that parallels the rotations running from rostral to caudal in this part of the neck.
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The chicken has similar drinking phases, but approach and upstroke often occur in discrete steps. The drinking approach is much slower than the pecking approach and shows low-level activity of the ventral muscles at the start of each step in the approach phase and very small activity of the dorsal muscles. The upstroke is similar to the pecking return for the middle part of the neck, where the simultaneous activity in the dorsal muscles (DCR, SPL) is followed by activity in the VCR. The activity pattern in the caudal muscles resembles the pattern in the mallard: the caudal VCA is coactive with the dorsal muscles (DCA and CA) that show successive activity from rostral to caudal. This activity parallels the wave of rotations of vertebrae in the caudal neck region that are used to elevate the neck at the end of the upstroke.
To summarize, the mallard shows successive activity of dorsal muscles (DCR) during an upstroke and ventral muscles (VCR, VCA) during a down stroke in the rostral loop, in contrast to synchronous activity of these muscles in the chicken. Further, the mallard shows considerable co-activation of antagonists, in contrast to the chicken where activation of the agonist muscles is followed by activity of the antagonist muscles. Similar EMG patterns are found for the caudal part of the neck during the drinking upstroke, where the mallard and the chicken both show an additional wave of rotations to elevate the whole neck relative to the body: successive activity in the caudal dorsal neck muscles, and co-activation with the ventral muscles in that part of the neck.
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ADAPTATIONS TO THE AQUATIC ENVIRONMENT IN WATERFOWL |
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Although cervical anatomy differs only slightly between the mallard and the chicken, relatively large differences are found in neck movement patterning. The results from the kinematical model suggest that these differences are not the result of differences in head trajectory, but fundamental differences in movement patterns. Movement patterns are the expression of all actively generated muscle forces, passive forces in the musculo-skeletal system, and external forces. As there are no large external forces during the movements studied, this raises the question whether the differences result from passive forces (an anatomical constraint) or active forces, or both. The strength of the constraint on the movement of the caudal vertebrae that is required for anseriform neck movement in the model, is related to the amount of stretch in the long dorsal neck muscles, which have a different configuration in Anseriformes, compared to the chicken. However, a biomechanical model is required to assess the contribution of passive forces to differences in neck movement patterning.
The EMG analysis shows large differences in muscle activity patterns for the mallard and the chicken. The characteristic rolling pattern in the rostral loop of Anseriformes is clearly related to successive activity of the muscles in that area, in contrast to simultaneous activity of these muscles in the chicken. The differences in co-activation and overlap of the activity of antagonist muscles are probably related to differences in the velocity of the movement (Ghez and Gordon, 1987). Velocity itself may be considered a characteristic feature of the movement pattern but is not directly related to the different patterns of vertebral rotations (rolling pattern vs. lever pattern). On the other hand, the two waves of the rolling pattern are characterized by their overlapping activity in the joints of the rostral loop. Joints in this area first rotate in one direction (the first wave), shortly followed by rotation in the opposite direction (the second wave; Fig. 5, actual neck movement). Therefore in the rostral loop, ventral and dorsal rotations occur very near to each other, which may explain the co-activation of dorsal and ventral muscles. It is necessary to study the relationship between kinematics and EMG patterns in more detail to determine whether the difference in co-activation of antagonists between mallard and chicken are related to differences in velocity or in neck movement pattern.
The difference between rolling and lever patterns is not the result of the inability of chickens to generate successive activity in muscle slips. This is illustrated by two observations. First, the caudal muscles ((D)CA) show a shift in peak activity during the additional wave of rotations in the drinking upstroke to elevate the neck relative to the body. Second, in a study into the ontogeny of motor patterns during drinking in the chicken, Heidweiller et al. (1992c) found rolling patterns in the caudal loop of the neck during the upstroke (‘bike chain pattern’) in chicks up to 4 wk of age. The characteristic lever pattern in this region was found in 8 wk old and adult chickens. The rolling pattern in chicks results from activity of only the long dorsal neck muscles. As the force to lift the head and neck increases with body size, the activity of other short dorsal neck muscles is required as well. EMG amplitude of the short dorsal neck muscles increases with the allometric growth of head and neck. However, this increase in amplitude of the short dorsal neck muscles does not explain the transition from a bike chain pattern to a lever pattern during the ontogeny of chickens. This type of rolling pattern is also found in adult chickens when their body is experimentally fixed to prevent movement and results from differences in timing of activity in the dorsal muscle slips. Interestingly, these observations suggest that body movements determine the type of movement pattern used. However, despite the ability of chickens to generate patterns of successive activity in muscle slips, a rolling pattern does not occur in the rostral loop. Therefore, we conclude that the motor control strategy of neck movements is actually different in chicken and mallard.
From an evolutionary point of view, a fundamental difference in motor control strategy should be parallel to a difference in performance (fitness). Most hypotheses on avian phylogeny (Livezey and Zusi, 2001) consider Galliformes and Anseriformes as sister taxa that are the first offshoot in the Neognathae. Assuming that the ancestor of Galliformes and Anseriformes is a terrestrial bird, the functional demands on the neck system must have changed during the transition from a terrestrial to an aquatic environment. Our analysis of the general characteristics of neck movement suggests that neck movement patterns are largely determined by the economics of movement in general (minimizing rotation), rather than by extreme functional demands on force or velocity. However, in an aquatic environment, the displacement of water by the neck and especially the body requires large forces compared to movements on land. The rolling pattern in Anseriformes seems to be energetically beneficial in an aquatic environment (Fig. 8) for two reasons: first, during a down stroke, the caudal loop is not lowered into the water, as would happen in a terrestrial pattern; second, the head and the rostral part of the neck are kept vertical when they are lowered into the water during aquatic feeding, reducing the amount of drag. Within Anseriformes, the characteristic movement pattern is also found during movements on land, and in more terrestrially feeding species such as geese, which suggests that neck movement in water and on land are controlled by the same motor patterns. Despite a relatively large variation in anatomy and food acquisition methods (secondary feeding on land, surface feeding, upending and diving), there are no basic differences in neck movement patterning within waterfowl. Apparently, only significant changes in functional demands on the neck system, such as large external forces that act on the neck in an aquatic environment, result in a selective regime that changes movement and motor control pattern.
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ACKNOWLEDGMENTS |
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We like to thank Peter Snelderwaard for all the help during the experiments and operations, Peter Mulken for the photographic work, and the members of the Evolutionary Morphology group at Leiden University for their useful comments and discussions. Michael Alfaro and Anthony Herrel are thanked for the invitation to write this review. The SICB and Leids Universiteits Fonds, Leiden, The Netherlands, provided funding for the contribution to the SICB symposium.
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FOOTNOTES |
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1 From the Symposium Motor Control of Vertebrate Feeding: Function and Evolution presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 3–7 January 2001, at Chicago, Illinois.
2 E-mail: vdleeuw{at}rulsfb.leidenuniv.nl
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