Monday, December 26, 2005
evolution of the motor control of feeding in amphibians, The
SYNOPSIS. Based on studies of a few model taxa, amphibians have been considered stereotyped in their feeding movements relative to other vertebrates. However, recent studies on a wide variety of amphibian species have revealed great diversity in feeding mechanics and kinematics, and illustrate that stereotypy is the exception rather than the rule in amphibian feeding. Apparent stereotypy in some taxa may be an artifact of unnatural laboratory conditions. The common ancestor of lissamphibians was probably capable of some modulation of feeding movements, and descendants have evolved along two trajectories with regard to motor control: (1) an increase in modulation via feedback or feed-forward mechanisms, as exemplified by ballistic-tongued plethodontid salamanders and hydrostatic-tongued frogs, and (2) a decrease in variation dictated by biomechanics that require tight coordination between different body parts, such as the tongue and jaws in toads and other frogs with ballistic tongue projection. Multi-joint coordination of rapid movements may hamper accurate tongue placement in ballistic-tongued frogs as compared to both short-tongued frogs and ballistic tongued-salamanders that face simpler motor control tasks. Decoupling of tongue and jaw movements is associated with increased accuracy in both hydrostatic-tongued frogs and ballistic-tongued salamanders.
INTRODUCTION
Until recently, study of the motor control of amphibian feeding was limited to a few model taxa, for example the genera Bufo and Rana representing the Anura, and salamanders of the genus Ambystoma representing the Caudata. Kinematic studies of these taxa gave the impression that amphibian feeding in general is highly stereotyped, that is, it is performed in much the same way every time, with little variation in the timing or extent of movements. However, kinematic studies of a great diversity of salamanders, frogs and caecilians have revealed, in the last 15 yr or so, that these taxa are probably exceptions among amphibians, and were unfortunate models on which to base generalizations about feeding in amphibians. Indeed, Bufo is now known to be among the most stereotyped of frogs in its feeding movements (Nishikawa et al., 1992; Nishikawa and Gans, 1996), and Ambystoma lies at the low end of variation for salamanders (Larsen and Guthrie, 1975; Reilly and Lauder, 1989, 1990, 1992; Beneski et al., 1995). The perspective gained over this time, and the rapid growth of understanding in the field have motivated the current survey of motor control in amphibians. Now is a good time to reassess some early conclusions that were drawn, particularly that of stereotypy of movement, and to highlight some instructive examples and general evolutionary patterns to present a more balanced view of amphibian feeding.
A major conclusion that can be drawn from a survey across living amphibians is that feeding mechanisms are extremely varied, and that kinematics of feeding are accordingly diverse. Part of this diversity stems from the biphasic life cycle that is ancestral for amphibians and which characterizes most living taxa. Most amphibians make a transition from an aquatic larval stage in which suction-based feeding mechanics and lateral line and chemosensory cues dominate (Himstedt et al., 1982; Bartels et al., 1990), to a more terrestrial adult stage in which feeding is accomplished with the tongue and jaws, and visual stimuli become more important in guiding feeding movements (Ewert, 1987; Roth, 1987). There are clear exceptions to this ancestral developmental pattern, such as direct development and viviparity in which the larval stage is skipped, as well as paedomorphosis in which the ancestral larval characteristics are retained in the adult stage. Direct development and viviparity have evolved in all three groups of Lissamphibia: frogs, salamanders and caecilians. Perennibranchiation (a form of paedomorphosis in which external gills persist in adults) has evolved repeatedly only in salamanders, and the perennibranchiate adults use larval biomechanics and sensorimotor control of feeding movements. Feeding movements can be extremely rapid (i.e., five msec for tongue projection in bolitoglossine salamanders; Thexton et al., 1977; Larsen et al., 1989) and controlled by feed-forward mechanisms in which sensory feedback plays no role, or movements can be relatively slow and deliberate (i.e., about 150 msec for tongue protraction in the frog Hemisus, which has a hydrostatic tongue; Ritter and Nishikawa, 1995), relying heavily on feedback to adjust movements as they are performed. Movements can be triggered and guided by visual stimuli alone, as in many frogs and salamanders (Ewert, 1987; Roth, 1987), or by a combination of mechanical and chemical cues as in most caecilians and some frogs (Himstedt and Simon, 1995; Lettvin et al., 1959; Comer and Grobstein, 1981).
Secondarily aquatic adult amphibians provide another source of diversity. Although the common ancestor of amphibians most likely had a terrestrial adult stage, many adult amphibians are now either facultative or obligate aquatic feeders. Adult frogs that feed in water generally use modifications of terrestrial mechanisms, such as tongue protraction and jaw prehension, and only one taxon (Hymenochirus) has reevolved suction feeding (O'Reilly et al., 2002). All caecilians and many salamanders that feed in water as adults use jaw prehension, although the retention of suction feeding in adult salamanders is widespread and probably related to their generalized morphology as compared to frogs and caecilians. Those salamanders that lose all ability to suction feed are specialized for tongue projection.
Biomechanical diversity has been accompanied by diversity of motor control strategies. For example, the fundamentally different biomechanics of ballistic tongue projection in frogs and salamanders call for different characteristics of motor planning. Frogs use a mechanism that requires tight coordination between jaw and tongue movements via feedback, while salamanders have decoupled the tongue from the jaws and project the tongue using feed-forward mechanisms in which feedback is not used to coordinate movements.
Because motor control mechanisms (i.e., feedback vs. feed-forward control) have only been examined directly in a few taxa of frogs and salamanders, we must infer mechanisms for most taxa based on behavioral and kinematic evidence. The lack of direct evidence for many taxa and behavioral data on only a fraction of the extant species makes reconstruction of the evolution of motor control in a phylogenetic context difficult and tenuous. Although a formal phylogenetic analysis of characters should be conducted when more data become available, such an analysis using current data would include many unknown character states. Therefore, instead of a formal phylogenetic analysis, we discuss the trends observed in each of the three groups of extant amphibians with examples of representative taxa, as well as the patterns observed in the Lissamphibia as a whole.
Definitions
For the purposes of this discussion, it is necessary to lay down some operational definitions of terms that appear in the literature that relate to amphibian feeding and the neural control of movement.
Amphibians capture prey using a variety of behaviors that can involve movements of the jaws, hyobranchial apparatus, tongue, limbs, and the entire body. Several modes of prey capture have been discussed in the literature; we describe our understanding of these terms here. Jaw prehension is the grasping of prey between the jaws, and is performed both in water and on land; this is also called biting. Tongue prehension is the grasping of prey with the tongue, and involves tongue protraction or projection followed by tongue retraction. Suction feeding is drawing a single, relatively large prey item into the mouth by a single expansion of the buccal cavity, and is performed only in water. Filter feeding is removing multiple small food particles from the water either by rhythmically repeated buccal expansions that draw water into the mouth, or by moving forward over the particles. Lunging is forward movement of the entire body and can be combined with the other behaviors.
SYNOPSIS. Based on studies of a few model taxa, amphibians have been considered stereotyped in their feeding movements relative to other vertebrates. However, recent studies on a wide variety of amphibian species have revealed great diversity in feeding mechanics and kinematics, and illustrate that stereotypy is the exception rather than the rule in amphibian feeding. Apparent stereotypy in some taxa may be an artifact of unnatural laboratory conditions. The common ancestor of lissamphibians was probably capable of some modulation of feeding movements, and descendants have evolved along two trajectories with regard to motor control: (1) an increase in modulation via feedback or feed-forward mechanisms, as exemplified by ballistic-tongued plethodontid salamanders and hydrostatic-tongued frogs, and (2) a decrease in variation dictated by biomechanics that require tight coordination between different body parts, such as the tongue and jaws in toads and other frogs with ballistic tongue projection. Multi-joint coordination of rapid movements may hamper accurate tongue placement in ballistic-tongued frogs as compared to both short-tongued frogs and ballistic tongued-salamanders that face simpler motor control tasks. Decoupling of tongue and jaw movements is associated with increased accuracy in both hydrostatic-tongued frogs and ballistic-tongued salamanders.
INTRODUCTION
Until recently, study of the motor control of amphibian feeding was limited to a few model taxa, for example the genera Bufo and Rana representing the Anura, and salamanders of the genus Ambystoma representing the Caudata. Kinematic studies of these taxa gave the impression that amphibian feeding in general is highly stereotyped, that is, it is performed in much the same way every time, with little variation in the timing or extent of movements. However, kinematic studies of a great diversity of salamanders, frogs and caecilians have revealed, in the last 15 yr or so, that these taxa are probably exceptions among amphibians, and were unfortunate models on which to base generalizations about feeding in amphibians. Indeed, Bufo is now known to be among the most stereotyped of frogs in its feeding movements (Nishikawa et al., 1992; Nishikawa and Gans, 1996), and Ambystoma lies at the low end of variation for salamanders (Larsen and Guthrie, 1975; Reilly and Lauder, 1989, 1990, 1992; Beneski et al., 1995). The perspective gained over this time, and the rapid growth of understanding in the field have motivated the current survey of motor control in amphibians. Now is a good time to reassess some early conclusions that were drawn, particularly that of stereotypy of movement, and to highlight some instructive examples and general evolutionary patterns to present a more balanced view of amphibian feeding.
A major conclusion that can be drawn from a survey across living amphibians is that feeding mechanisms are extremely varied, and that kinematics of feeding are accordingly diverse. Part of this diversity stems from the biphasic life cycle that is ancestral for amphibians and which characterizes most living taxa. Most amphibians make a transition from an aquatic larval stage in which suction-based feeding mechanics and lateral line and chemosensory cues dominate (Himstedt et al., 1982; Bartels et al., 1990), to a more terrestrial adult stage in which feeding is accomplished with the tongue and jaws, and visual stimuli become more important in guiding feeding movements (Ewert, 1987; Roth, 1987). There are clear exceptions to this ancestral developmental pattern, such as direct development and viviparity in which the larval stage is skipped, as well as paedomorphosis in which the ancestral larval characteristics are retained in the adult stage. Direct development and viviparity have evolved in all three groups of Lissamphibia: frogs, salamanders and caecilians. Perennibranchiation (a form of paedomorphosis in which external gills persist in adults) has evolved repeatedly only in salamanders, and the perennibranchiate adults use larval biomechanics and sensorimotor control of feeding movements. Feeding movements can be extremely rapid (i.e., five msec for tongue projection in bolitoglossine salamanders; Thexton et al., 1977; Larsen et al., 1989) and controlled by feed-forward mechanisms in which sensory feedback plays no role, or movements can be relatively slow and deliberate (i.e., about 150 msec for tongue protraction in the frog Hemisus, which has a hydrostatic tongue; Ritter and Nishikawa, 1995), relying heavily on feedback to adjust movements as they are performed. Movements can be triggered and guided by visual stimuli alone, as in many frogs and salamanders (Ewert, 1987; Roth, 1987), or by a combination of mechanical and chemical cues as in most caecilians and some frogs (Himstedt and Simon, 1995; Lettvin et al., 1959; Comer and Grobstein, 1981).
Secondarily aquatic adult amphibians provide another source of diversity. Although the common ancestor of amphibians most likely had a terrestrial adult stage, many adult amphibians are now either facultative or obligate aquatic feeders. Adult frogs that feed in water generally use modifications of terrestrial mechanisms, such as tongue protraction and jaw prehension, and only one taxon (Hymenochirus) has reevolved suction feeding (O'Reilly et al., 2002). All caecilians and many salamanders that feed in water as adults use jaw prehension, although the retention of suction feeding in adult salamanders is widespread and probably related to their generalized morphology as compared to frogs and caecilians. Those salamanders that lose all ability to suction feed are specialized for tongue projection.
Biomechanical diversity has been accompanied by diversity of motor control strategies. For example, the fundamentally different biomechanics of ballistic tongue projection in frogs and salamanders call for different characteristics of motor planning. Frogs use a mechanism that requires tight coordination between jaw and tongue movements via feedback, while salamanders have decoupled the tongue from the jaws and project the tongue using feed-forward mechanisms in which feedback is not used to coordinate movements.
Because motor control mechanisms (i.e., feedback vs. feed-forward control) have only been examined directly in a few taxa of frogs and salamanders, we must infer mechanisms for most taxa based on behavioral and kinematic evidence. The lack of direct evidence for many taxa and behavioral data on only a fraction of the extant species makes reconstruction of the evolution of motor control in a phylogenetic context difficult and tenuous. Although a formal phylogenetic analysis of characters should be conducted when more data become available, such an analysis using current data would include many unknown character states. Therefore, instead of a formal phylogenetic analysis, we discuss the trends observed in each of the three groups of extant amphibians with examples of representative taxa, as well as the patterns observed in the Lissamphibia as a whole.
Definitions
For the purposes of this discussion, it is necessary to lay down some operational definitions of terms that appear in the literature that relate to amphibian feeding and the neural control of movement.
Amphibians capture prey using a variety of behaviors that can involve movements of the jaws, hyobranchial apparatus, tongue, limbs, and the entire body. Several modes of prey capture have been discussed in the literature; we describe our understanding of these terms here. Jaw prehension is the grasping of prey between the jaws, and is performed both in water and on land; this is also called biting. Tongue prehension is the grasping of prey with the tongue, and involves tongue protraction or projection followed by tongue retraction. Suction feeding is drawing a single, relatively large prey item into the mouth by a single expansion of the buccal cavity, and is performed only in water. Filter feeding is removing multiple small food particles from the water either by rhythmically repeated buccal expansions that draw water into the mouth, or by moving forward over the particles. Lunging is forward movement of the entire body and can be combined with the other behaviors.
# posted by Unknown @ 7:10 PM 
