Integrative and Comparative Biology Advance Access published online on June 9, 2008
Integrative and Comparative Biology, doi:10.1093/icb/icn055
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Evolution of asynchronous motor activity in paired muscles: effects of ecology, morphology, and phylogeny
*Department of Biological Sciences, University of Rhode Island, Kingston, RI 02881, USA; Department of Ecology and Evolutionary Biology, University of California–Irvine, Irvine, CA 92697, USA
Correspondence: 1E-mail: sgerry{at}mail.uri.edu
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Many studies of feeding behavior have implanted electrodes unilaterally (in muscles on only one side of the head) to determine the basic motor patterns of muscles controlling the jaws. However, bilateral implantation has the potential to achieve a more comprehensive understanding of modification of the motor activity that may be occurring between the left and right sides of the head. In particular, complex processing of prey is often characterized by bilaterally asynchronous and even unilateral activation of the jaw musculature. In this study, we bilaterally implant feeding muscles in species from four orders of elasmobranchs (Squaliformes, Orectolobiformes, Carcharhiniformes, Rajoidea) in order to characterize the effects of type of prey, feeding behavior, and phylogeny on the degree of asynchronous muscle activation. Electrodes were implanted in three of the jaw adductors, two divisions of the quadratomandibularis and the preorbitalis, as well as in a cranial elevator in sharks, the epaxialis. The asynchrony of feeding events (measured as the degree to which activity of members of a muscle pair is out of phase) was compared across species for capture versus processing and simple versus complex prey, then interpreted in the contexts of phylogeny, morphology, and ecology to clarify determinants of asynchronous activity. Whereas capture and processing of prey were characterized by statistically similar degrees of asynchrony for data pooled across species, events involving complex prey were more asynchronous than were those involving simple prey. The two trophic generalists, Squalus acanthias and Leucoraja erinacea, modulated the degree of asynchrony according to type of prey, whereas the two behavioral specialists, Chiloscyllium plagiosum and Mustelus canis, activated the cranial muscles synchronously regardless of type of prey. These differences in jaw muscle activity would not have been detected with unilateral implantation. Therefore, we advocate bilateral implantation in studies of cranial muscle function in fishes, particularly when investigating behaviors associated with processing complex prey. Incorporating this methodology will provide a more detailed understanding of the coordination and evolution of paired-muscle function in the feeding apparatus relative to behavioral and ecological performance.
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Functional morphological studies of vertebrate locomotion often recognize independent motion of the left and right limbs; however, unilateral independence of feeding structures is rarely assessed. This is understandable; limbs are coordinated in motion but uncoupled morphologically, whereas the left and right portions of the visceral arches of the head (i.e., jaws, hyoid, and branchial arches) are often connected medially and therefore constrained to move together. As such, muscular activity on one side of the head may have an effect on the force generated on the other and muscular activity might be constrained to be bilaterally synchronous as well.
Yet, feeding behaviors and activation patterns can be bilaterally asymmetrical. Asynchronous activation of the jaw muscles (i.e., out-of-phase activation of left and right members of a muscle pair) has been shown in many clades of vertebrates: elasmobranchs (Gerry et al. 2006
), ray-finned fishes (Liem 1978, 1979; Lauder and Norton 1980), salamanders (Cundall et al. 1987; Lorenz-Elwood and Cundall 1994), snakes (Cundall 1983), birds (Zweers 1974), and mammals (Hylander et al. 2000; Lieberman and Crompton 2000 and references therein; Dumont and Herrel 2003; Williams et al. 2007 and references therein). This activation is most notably demonstrated in the "pterygoid walk" of colubroid snakes during which the snake alternately advances the opposite sides of the jaws during swallowing (Cundall 1983; Jackson et al. 2004). The above studies have found asynchronous activation of jaw muscles to be prevalent in situations requiring extensive processing and transport of prey. However, the phylogenetic disparity of these groups makes it difficult to draw conclusions about the functional benefits of asynchronous activation of jaw muscles or the selective pressures that led to its expression in some species for some behaviors and types of prey rather than others.
In this study, the feeding behavior of four species of elasmobranch fishes is examined in order to clarify potential functional advantages and morphological correlates relating to the evolution of asynchronous activity in feeding muscles within Elasmobranchii. The species studied represent a range of phylogenetic positions within the clade, but also differ with respect to dietary breadth and to behavior during capture of prey (Fig. 1). Spiny dogfish (Squalea: Squalus acanthias) and little skates (Batoidea: Leucoraja erinacea) are dietary and behavioral generalists that use multiple behaviors (suction or biting) to feed on a variety of prey including small fishes, shrimp, and mollusks (Jones and Geen 1977; Wilga and Motta 1998a; Bowman et al. 2000; Steimle et al. 2000; Link et al. 2002; Wilga et al. 2007), whereas smooth-hounds (Galea: Mustelus canis) are dietary specialists that feed primarily on crabs (Cortes 1999) and use a stereotyped ram behavior independent of prey type (Gerry 2008). Dietary studies of white-spotted bamboo sharks (Galea: Chiloscyllium plagiosum) are lacking; however, the diet of a morphologically similar sister species (Chiloscyllium griseum) is that of a dietary generalist (Devadoss 1986). Furthermore, C. plagiosum feeds on squid, small fishes, shrimp, and crabs in captivity (Ramsay and Wilga 2007); and are specialized suction feeders (Lowry and Motta 2007; Wilga et al. 2007). We chose these species because the diet includes complex prey (i.e., those requiring more manipulation and processing before swallowing), which typically elicits asynchronous behavior. The definitions of simple and complex prey are broad to allow comparison among species that feed on different types of prey. Complex prey may be oversized prey for one species, but hard prey for another.
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The objectives of this study were to examine the effects of behavior (capture versus processing), prey type (simple versus complex), and species on asynchronous activation of the jaw muscles within elasmobranchs. As determined by previous findings, processing of prey and complex prey items are expected to generate the greatest asynchronous activity relative to prey capture and simple prey, respectively (Gerry et al. 2006
). Although smooth-hounds and bamboo sharks feed on complex prey items, stereotyped behavior is expected to correspond to a stereotyped functional response (no modification of neuromuscular control in response to novel prey items; Sanderson 1991). In other words, we expect the timing of activation of pairs of muscles will not differ by behavior or prey type for bamboo sharks or smooth-hounds. Modulation between synchronous and asynchronous activity of jaw muscles by prey type has been demonstrated in spiny dogfish and little skates (Gerry et al. 2006) and as these species are generalist predators, we expect their feeding behaviors to encompass a broader range of asynchrony.
The taxonomic position of Batoidea remains a subject of debate; they are considered either the sister group to sharks or nested within them as derived Squalea (Shirai 1996; Douady et al. 2003; Winchell et al. 2004) (Fig. 1). Asynchronous activation of feeding muscles has only been demonstrated in the batoid and squalean species used in this study. In either hypothesis of elasmobranch phylogeny, if asynchronous activation is present in galean sharks, then the trait may have been gained prior to the squalean–galean split at the base of the elasmobranch clade and thus may be a basal trait of the vertebrates.
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Study animals
Six mature spiny dogfish, S. acanthias, (73–82 cm total length, TL) and three mature smooth-hound sharks, M. canis, (92–95 cm TL) were collected by otter trawl in Narragansett Bay, Rhode Island or off the coast of Woods Hole, Massachusetts, USA. Sharks were housed in a circular tank (3 m in diameter) with a flow-through seawater system at a temperature of 15 ± 1°C. Dogfish were fed to satiation twice weekly on a diet of pieces of herring (Clupea harengus) or pieces of squid (Loligo spp.). Smooth-hounds were fed a diet of green crabs (Carcinus maenas) or pieces of herring (C. harengus) twice weekly. Three sub-adult and adult white-spotted bamboo sharks, C. plagiosum, (68–73 cm TL) were obtained from SeaWorld San Diego and housed in 379–l rectangular aquaria at 26 ± 1°C. Bamboo sharks were fed a combination of green crabs (C. maenas), silversides (Menidia menidia), squid pieces (Loligo spp.), and shrimp pieces (Penaeus spp.) twice weekly to satiation. Three mature little skates, L. erinacea, (25–28 cm disc width, DW) were collected by otter trawl in Narragansett Bay, Rhode Island, USA. Skates were housed in a circular tank (1.2 m in diameter) with a recirculating seawater system at a temperature of 15 ± 1°C. Skates were maintained on a diet of silverside pieces (M. menidia), squid pieces (Loligo spp.), or shrimp pieces (Penaeus spp.) and were fed to satiation three times weekly. Relative prey sizes for all species were kept consistent at one-half mouth width of the predator.
Electromyography
All species of sharks were anesthetized for surgery using 0.175 g l–1 tricaine methanesulfonate (MS-222) and then maintained on a dosage of 0.058 g l–1; similarly, skates were anesthetized for surgery using 0.1 g l–1 MS-222 and maintained on a dosage of 0.05 g l–1 during surgery. A recirculating pump was used to ensure a continuous flow of water over the gills. Electromyograms were recorded using bipolar electrodes constructed from 3 m lengths (sharks) or 2 m lengths (skates) of 0.002 cm diameter insulated alloy wire (California Fine Wire Co., Grover Beach, California, USA). Insulation was stripped 0.05 cm from the end of the wire and the two ends of the wire were bent back into a hook to anchor the electrode into the muscle. A second 5 cm length of insulated wire was also bent into a hook and implanted alongside the electrode to verify placement in case the electrode was pulled out. Electrodes were implanted into cranial muscles that control jaw movements (as determined from previous literature; Wilga and Motta 1998a, 1998b) using 24 gauge hypodermic needles. All muscles were implanted bilaterally (i.e., into both left and right members of a muscle pair) except the coracomandibularis, which acted as the reference muscle.
Seven cranial muscles were implanted in all sharks (Fig. 2): left and right anterior division of the dorsal quadratomandibularis (jaw adductor); left and right preorbitalis (upper jaw protractor and jaw adductor); left and right epaxialis (head elevator); coracomandibularis (unpaired lower jaw depressor). The left and right ventral quadratomandibularis (jaw adductor) were also implanted in dogfish and smooth-hounds. In skates, the left and right anterior quadratomandibularis (jaw adductor); left and right posterior quadratomandibularis (jaw adductor); left and right preorbitalis (upper jaw protractor); and coracomandibularis (unpaired lower jaw depressor) were implanted (Fig. 2). After implantation, the electrode wires were anchored to the skin by a loop of suture anterior to the first dorsal fin (sharks) or at the cranial portion of the tail (skates) and all wires glued together to form a single cable. Surgery lasted 
30 min.
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Following surgery, the fish was returned to the experimental tank and monitored for normal swimming behavior. Electrode wires were inserted into a multi-pin connector joined to 3 m low-noise cables attached to 16-channels AM Systems (model 1700). AC differential amplifiers at a gain of 10 000, bandpass 10–10 000 Hz with 60 Hz notch filter. Muscle activations were recorded simultaneously from all channels using an AD Instruments Powerlab 16SP analog-to-digital converter and Chartview software (AD Instruments, Colorado, USA). Feeding trials were initiated after normal swimming behavior was resumed, at least 30 min post-recovery.
Individuals were fed two functionally different types of prey: "simple" prey items (those requiring less handling/processing) were expected to require less asynchronous activity than "complex" prey items (those requiring greater manipulation and processing). Note that the definitions of simple and complex prey may be taxonomically broad but are intended to elicit similar functional differences among species that feed on different prey. Size and taxonomy may be confounding prey variables; however, these classifications are used because increasing prey size or changing prey taxa is expected to increase the degree of behavioral modulation. Although the specific prey items differed across study species, the general comparison of activation patterns elicited by simple versus complex prey items offered a method of comparing each species’ capacity for asynchronous activation and whether the expression of this ability was modulated according to the feeding situation. Thus, the contrasting of simple and complex feeding events can provide a baseline indication of modulatory ability for the relative activation times of muscle pairs. Dogfish were offered pieces of herring scaled to one-half mouth width (simple) or a half of a herring (complex); smooth-hounds were offered pieces of herring scaled to one-half mouth width (simple) or crabs scaled to mouth width (complex); bamboo sharks were offered pieces of shrimp, squid, or silversides scaled to one-half mouth width (simple) and crabs, whole shrimp, or half of a squid (complex) and skates were offered pieces of shrimp tail with the carapace intact and either scaled to one-half mouth width and lacking the telson and uropods (simple) or larger than mouth width and including the telson and uropods (complex).
At the termination of each experiment, the animal was euthanized by MS-222 overdose according to URI IACUC guidelines. The positions of the electrodes were verified by dissection.
Asynchrony index
Each behavioral event can be described by a series of muscle pair events (pairwise activations; e.g., one activation each of the left and right quadratomandibularis) that are characterized by the onset, offset, and duration of individual muscle bursts. Pairwise muscle-activation events are considered more asynchronous the more the onset or offset of activation differs between left and right members of a muscle pair. The total event length (TE), or the duration of all activity within a muscle pair during a single gape cycle, is calculated as the last burst offset minus the earliest burst onset within a muscle pair. The amount of asynchronous (unilateral) and synchronous (bilateral) activity for a muscle pair can be quantified by comparing the durations of antimere activity relative to the length of the total event:
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where dur1 and dur2 are the durations of the first and second bursts, respectively, within a muscle pair. The Asynchrony Index (AI) has a minimum value of 0.00 when both muscles in a pair have the same onset and offset (complete synchrony), as defined by dur1 = dur2 = TE. The AI has a maximum value of 1.00 when one member of the muscle pair is not active (complete asynchrony or unilateral activation; e.g., muscles on the left side of the head are active with no activation of right side muscles). An intermediate AI value of 0.50 is given when each muscle in the pair is active for the same duration but with no overlap of muscle activation, such that the offset of the first muscle occurs at the onset of the second muscle. This index evaluates the degree of asynchronous activity for muscles within a pair (e.g., left and right quadratomandibularis), the AI does not account for activation differences among muscles (e.g., quadratomandibularis and preorbitalis) within the feeding cycle. The amount of asynchrony for each muscle pair was quantified by calculating the AI using durations calculated from the EMG data; AI values for muscles within a species were pooled (because AI values for muscles did not differ, P > 0.05) and then compared among behaviors and prey types and between species. Note that the purpose of the AI is to compare the differences in activation between members of a muscle pair, rather than among groups of different muscles that are active during the feeding cycle.
Statistics
Assumptions of parametric statistics were tested including normality using Kolmogorov–Smirnov (P < 0.05) and homogeneous variances using Levene's equality of error variances (P < 0.05). All data were square root transformed to achieve normality. A two-way analysis of variance (ANOVA; SPSS, version 12.0) was used to test for differences in AI among species (dogfish, smooth-hounds, bamboos, skates) and between behaviors (capture, processing) with species and behavior as fixed effects. A two-way ANOVA was used to test for differences in AI between species and prey types (simple, complex), with species and prey type as fixed effects. Tukey post hoc tests of species were then used to identify differences detected by the ANOVAs (P < 0.05). Stereotypy of behavior and prey type was evaluated by calculating the coefficient of variation (CV) for each species (Rice and Westneat 2005) based on the square root transformed AI values.
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Behavior
Our statistical design allowed us to compare levels of asynchrony between behaviors (capture versus processing) and prey types (simple versus complex) across species, and to examine differences in behaviors and prey types within species. Across and within species capture and processing of prey were similar (F = 0.889, P = 0.346) (Table 1). This lack of significant difference is likely the result of wide behavioral variation within capture and processing; within each of these behaviors, however, there were significant differences by species (F = 14.73, P < 0.001) (Table 1). In general, bamboo sharks and smooth-hounds exhibit more synchronous behaviors than spiny dogfish, which tend to be more synchronous than little skates (see below).
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Prey capture by bamboo sharks (AI = 0.173) and smooth-hounds (AI = 0.175) is more synchronous than capture by skates (AI = 0.317), with capture by dogfish (AI = 0.187) statistically similar to both groups (F = 3.367, P = 0.020) (Table 1). Capture of prey by bamboo sharks and smooth-hounds was characterized by an activation pattern in which the coracomandibularis was active first, followed by synchronous pairwise activation of the epaxialis and then synchronous pairwise activation of the jaw adductors (Figs. 3 and 4). Spiny dogfish and skates activated the coracomandibularis first (as well as the epaxialis in dogfish), followed by activation of the muscle pairs, but these two species were able to modulate capture of prey between suction and biting. Biting elicited greater asynchronous activation which caused these species to have higher AI values (Figs. 5 and 6) (Gerry 2008
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The degree of asynchronous activation within prey processing also differed by species (F = 29.155, P < 0.001). The processing behavior of smooth-hounds (AI = 0.140) is more synchronous than that of spiny dogfish (AI = 0.257), which is more synchronous than that of skates (AI = 0.468), with that of bamboo sharks (AI = 0.169) being statistically similar to the processing of the other two shark species (Table 1, Fig. 7). Similar to capture of prey, processing of prey by smooth-hounds and bamboo sharks is relatively stereotyped, as shown by the CV (Table 1). These sharks activate the coracomandibularis and epaxialis pairs first followed by relatively synchronous pairwise activation of the jaw adductors (Figs. 3 and 4
). Dogfish often used head-shaking in addition to biting during processing in order to tear larger prey into pieces prior to swallowing. This consisted of a distinct pattern of asynchronous pairwise activation in which dorsal and ventral quadratomandibularis muscles on one side of the head were activated simultaneously with the contralateral epaxialis muscle (Fig. 5). Head-shaking is the most asynchronous processing behavior used by dogfish (AI = 0.501) (Gerry 2008; Gerry et al. 2006). Skates show extremely wide variation in the asynchrony of processing behaviors, ranging from synchronous activation of the jaw adductors (AI < 0.500) to pairwise asynchronous activation (AI = 0.500) to unilateral activation (AI = 1.00), in which only muscles on one side of the head are active (Fig. 6) (Gerry et al. 2006). Unilateral activation was exhibited only by skates and resulted in a greater asynchrony in skates compared to the other three species.
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Type of prey
Feeding on simple and complex prey were characterized by differing degrees of asynchrony across species (F = 27.612, P < 0.001) and within three of four species (P < 0.001; except bamboo sharks, P = 0.860) (Table 2). Simple prey elicited comparatively synchronous pairwise activation patterns (i.e., on average always AI < 0.20) and was often captured and swallowed without further processing. When feeding on simple prey items, dogfish (AI = 0.126) showed more synchronous muscle activation than smooth-hounds (AI = 0.184) with bamboo sharks (AI = 0.167) and skates (AI = 0.191) being statistically indistinct from either of these species (F = 3.764, P = 0.011) (Table 2, Fig. 8).
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Feeding on complex prey showed the most pronounced differences in asynchrony among species, with galean sharks having a response counter to previous findings; that more complex prey elicits a greater degree of asynchrony. Activation patterns in bamboo sharks (AI = 0.173) and smooth-hounds (AI = 0.130) feeding on complex prey items were similar: the coracomandibularis and epaxialis were active prior to relatively synchronous activation of the jaw adductors (Figs. 3 and 4
). Bamboo sharks showed a stereotyped synchronous response to simple and complex prey because they did not modulate the degree of asynchrony by prey type (simple = 0.167, complex = 0.173, F = 0.031, P = 0.860). Smooth-hounds exhibited a distinct biting behavior in which all adductor muscle pairs are activated repeatedly and synchronously prior to another activation of the coracomandibularis (Fig. 4). Contrary to predictions, smooth-hounds exhibited less asynchronous activity when feeding on complex prey as compared to simple prey (simple = 0.184, complex = 0.130, F = 11.249, P < 0.001). Smooth-hounds use relatively synchronous activation for simple and complex prey, however, the mean AI value for complex prey shows increased variability based on differing values of the CV (Table 2). Therefore, this species may vary its response to complex prey while still activating the muscles synchronously.
In contrast to the galean species, feeding on complex prey elicited the greatest amount of asynchrony from dogfish (AI = 0.353) and skates (AI = 0.573), with skates demonstrating a greater degree of asynchrony (F = 53.666, P < 0.001) (Table 2, Fig. 8). Dogfish either bit the prey or used a head-shaking behavior that consisted of swinging the head laterally from side to side to tear prey into smaller pieces (Wilga and Motta 1998a; Gerry 2008). Head-shaking relies on a cyclical alternating pattern of asynchronous activation of muscles on opposite sides of the head (Gerry 2008). That is, in each half of a cycle, the epaxialis on one side of the head is activated, followed by the activation of the jaw adductors on the contralateral side, with little overlap of active muscle bursts (Fig. 5); this pattern is repeated in mirror image to complete a single cycle or shake of the head and then the entire cycle is repeated up to several times.
The high-AI processing behavior of skates is also cyclical, but unlike head shaking is primarily unilateral. To strip complex prey of inedible portions, skates positioned prey in one corner of the jaws and activated only those ipsilateral adductors (unilateral activation, AI = 1.00), an action roughly similar to mammalian unilateral chewing (Fig. 6). This processing behavior resulted in the greatest degree of asynchronous activity shown by any of the species because jaw muscles on one side of the head were active while the contralateral jaw muscles remained inactive.
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The degree of asynchronous activation exhibited by feeding muscles varies according to predator species and prey type (simple or complex), but not between feeding cycle behaviors (capture or processing) (Fig. 8). Based on these differences among species, the ecological, morphological, and phylogenetic advantages to using synchronous versus asynchronous activation are assessed.
Ecological associations
Dogfish, little skates, and likely bamboo sharks are dietary generalists (Bowman et al. 2000; Steimle et al. 2000; Ramsay and Wilga 2007). Behavioral modulation has been associated with a generalist diet such that a variety of prey items should be captured by multiple behaviors (Liem 1978, 1979). Dogfish and skates modulate between suction and bite to feed on a variety of types of prey (Wilga and Motta 1998a; Wilga et al. 2007) as well as modulate between synchronous and asynchronous activation of the jaw muscles. The natural prey items of these species are elusive (small fishes, squid, polychaetes). By activating the jaw muscles asynchronously, the predator can process the prey while maintaining partial contact thus preventing escape. This partial contact is fundamental to unilateral transport in snakes (Kley 2001) and we suggest it to be a major advantage of asynchronous activation in general.
In contrast to the other two generalists, bamboo sharks are stereotyped suction feeders (Lowry and Motta 2007; Ramsay and Wilga 2007); this is reflected in the lack of modulation of asynchronous activation according to prey type. Successful suction capture relies on rapid expansion of the buccal cavity to bring prey into the mouth (Wilga et al. 2007). Also, rapid closure of the jaws during the compressive phase of suction feeding is vital to successful capture of prey (Wainwright and Richard 1995; Van Wassenburgh et al. 2005). If the jaws are closed slowly, or if one side closes faster than the other, the flow into the mouth may be disrupted and result in back-flow of the ingested volume of water from the mouth. Such an action could result in expulsion of any prey contained within that volume (Muller et al. 1982; Muller and Osse 1984). Even though bamboo sharks feed on several kinds of prey, constraints associated with selection for features contributing to the suction-feeding mechanism exhibited by this species may have resulted in the increased level of stereotypy in pairwise activation of muscles regardless of the differences in complexity of the prey. Therefore, for dietary generalists, behavioral modulation by type of prey appears to be more indicative of asynchronous activation than is diet alone.
Unlike the other three species, smooth-hounds can be considered ecological specialists (Sanderson 1990) because the diet is comprised primarily of crustaceans (Bowman et al. 2000). These sharks crush hard-shelled prey using tightly packed low-cusped teeth (Compagno 1984; Frazzetta 1994; Motta 2004), but the activation pattern employed for crushing is stereotyped and employed for softer prey as well (Gerry 2008). Smooth-hounds may activate the jaw muscles synchronously in order to generate enough crushing force, similar to durophagous mammals that recruit balancing-side muscles to increase the force needed to macerate the food (Lieberman and Crompton 2000; Ross et al. 2007a). Synchronous activation of the muscles, as shown by bamboo sharks and smooth-hounds could be characteristic of those sharks that use a stereotyped behavior and have a durophagous diet.
Morphological associations
Asynchronous activation of the muscles is often aided by flexibility of the jaws so that each side of the jaw can be functionally independent (Kardong 1977), thereby permitting fine motor control during feeding and the processing of food. A highly mobile jaw symphysis is characteristic of many other vertebrates that process prey unilaterally (Kardong 1977; Cundall et al. 1987; Lorenz-Elwood et al. 1994; Hylander et al. 1998). Little skates have a dorsoventrally depressed morphology and a euhyostylic jaw suspension by which the mandibular arch is suspended only by the hyomandibula and lacks anterior ligaments or articulations with the cranium (Wilga 2002). In combination with a flexible symphysis, the two sides of the jaws are effectively separated into two working halves. This enables the skate to grasp the prey item in the corner of the jaws and bite repeatedly using only the adductors on that half of the jaw, as in chewing by mammals, which has been shown to be energetically efficient because muscles only fatigue on one side of the head (Ross et al. 2007b).
Although dogfish are able to use a high degree of asynchrony when feeding, this feature is not likely due to an elevated level of symphyseal flexibility in the jaws, as has been suggested for skates. Dogfish have a triangular symphysis that is wider posteriorly than anteriorly. This joint forms a tight connection between the two halves of the jaw anteriorly, but the looser connection at the posterior end provides some flexibility; however, the joint does not have the same degree of movement as in little skates (S. Gerry, personal observation). This joint may require some stability because prey is often positioned at the symphysis prior to head-shaking and held at the center of the jaws while pieces are torn from it.
Smooth-hounds have a rectangular symphysis that expands laterally to widen the distance between the tips of the Meckel's cartilage as the jaw opens (S. Gerry, personal observation). Although this type of symphysis is flexible, low-cusped teeth overlay the symphysis and outer margins of the jaw and provide structural support, stiffening the jaws in response to applied force. Bamboo sharks have a similarly shaped symphysis, but it lacks the potential flexibility of the smooth-hound because the caudal-most ends of the Meckel's cartilage that compose the symphysis compress medially during feeding (Wu 1994, Ramsay and Wilga 2007), such that the medial facing surfaces of the symphyseal portions of the jaw halves contact, possibly reinforcing the articulation. The teeth also overlay the symphysis which compromises flexibility in exchange for support. While these two species have a semi-flexible symphysis, which is typically indicative of the ability to use asynchronous activation, it may be more advantageous to activate the muscles synchronously giving the jaw increased stability for crushing and for suction feeding.
Phylogenetic associations
When the species are mapped on a morphological cladogram, dogfish, and little skates are placed within Squalea, with batoids as derived squalean sharks and Galea as a sister group to Squalea, (Shirai 1996) (Fig. 1). In this scenario, if we consider the types of pairwise muscle activation observed in each of the species we examined to be similar to other members of clade, then asynchronous activation when feeding on complex prey is a basal trait of Squalea and unilateral activation of the jaw muscles in little skates is a derived form of asynchrony. Unilateral activation may have evolved in conjunction with the reduced articulation of the jaws with the cranium. The loss of multiple jaw-suspensory elements increased the mobility of the feeding apparatus in little skates by facilitating more independent movement of the jaw halves and likely resulting in increased processing efficiency within the group. This is a key evolutionary consequence of the reduced jaw suspension that characterizes Batoidea. Galeomorphs either lost the ability to activate the muscles asynchronously, or more likely, synchronous activation is more advantageous for the particular diet, morphology, and feeding mechanisms of the two galean species used in this study. Biting has been shown to elicit asynchronous activation and Galea is composed of many species that feed on complex prey by biting; therefore, the behavior needs to be investigated in several other galean species to gain a better understanding of motor activity patterns within the group. For example, lemon sharks use a stereotyped ram prey capture which would likely use synchronous activation of the jaw muscles, but they manipulate prey using head-shaking which may require asynchronous activation (Motta et al. 1997).
Recent molecular studies reject the Hypnosqualea hypothesis (batoids as derived Squalea) and place batoids as the sister group to sharks (Douady 2003; Winchell et al. 2004) (Fig. 1). Based on our study, asynchronous activation is likely present in the common ancestor to sharks and batoids, but sharks may alternately activate the muscles in conjunction with head-shaking while batoids may activate the muscles unilaterally due to the functional separation of each side of the head. Based on molecular studies, the position of Galea would not change; therefore, those hypotheses discussed above for the morphological cladogram would be supported.
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Asynchronous activation of the jaw muscles is predicted to occur in elasmobranch fishes that possess a flexible symphysis and modulate feeding behavior on the basis of the type of prey. The extreme mobility of the feeding apparatus in little skates suggests that other batoids with this morphology and with the ability to modulate behavior will show unilateral activation as well. Synchronous activation may be more advantageous for durophagous species (sharks or batoids) that need to stiffen the jaws in response to hard prey or for behavioral specialists that show a stereotyped response regardless of type of prey.
Whereas studies using unilateral implantation of electrodes are an important tool in understanding basic jaw-muscle activity associated with a particular behavior, bilateral implantation has the potential to increase our understanding of the function and evolution of musculoskeletal systems. A more comprehensive understanding of the functional differences that may occur on each side of the head during feeding may be gained. Furthermore, bilateral implantation may reveal behavioral or ecological effects on motor activity patterns.
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This article was part of the symposium, Electromyography: Interpretation and Limitations in Functional Analyses of Musculoskeletal Systems. We would like to thank the Journal of Experimental Biology, AD Instruments, SICB Division of Comparative Biomechanics and Grass Technologies for funding this symposium. We thank Corey Eddy, Jocelyne Dolce, Anabela Maia, Andrea Scott, and Dawn Simmons for providing assistance and/or for helpful discussions. This research was funded by the University of Rhode Island Office of the Provost and Department of Biological Sciences, the American Society of Ichthyologists and Herpetologists Raney Fund Award and by Sigma Xi Grants-in-Aid of Research to S.P.G. and by National Science Foundation grants to C.D.W. and S.P.G. (IOS-0542177) and to M.N.D. (IOB-0616322).
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From the symposium "Electromyography: Interpretation and Limitations in Functional Analyses of Musculoskeletal Systems" presented at the annual meeting of the Society for Integrative and Comparative Biology, January 2–6, 2008, at San Antonio, Texas.
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