© 2001 by The Society for Integrative and Comparative Biology
Prey Capture in Actinopterygian Fishes: A Review of Suction Feeding Motor Patterns with New Evidence from an Elopomorph Fish, Megalops atlanticus1
1 Department of Evolution and Ecology, University of California at Davis, Davis, California 95616
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SYNOPSIS |
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 SYNOPSIS INTRODUCTIONTAXONOMIC SURVEY OF SUCTION...TESTING THE PHYLOGENETIC SCOPE...NEW EVIDENCE FROM THE...TARPON SUCTION FEEDING...THE ROLE OF LATERAL...References |
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Suction feeding is recognized as the dominant mode of aquatic prey capture in fishes. While much work has been done identifying motor pattern variations of this behavior among diverse groups of actinopterygian fishes, many ray-finned groups are still not represented. Further, the substantial amount of inherent variation in electromyography makes much of the pioneering work of suction feeding motor patterns in several basal groups insufficient for evolutionary comparisons. Robust evolutionary comparisons have identified conserved qualitative traits in the order of muscle activation during suction feeding (jaw opening > buccal cavity expansion > jaw closing). However, quantitative traits of suction motor patterns (i.e., burst durations and relative onset times) have changed over evolutionary time among actinopterygian fishes. Finally, new motor pattern evidence is presented from a previously neglected group, the Elopomorpha. The results suggest that future investigations of the muscles influencing lateral expansion of the mouth cavity and head anatomy may provide valuable new insights into the evolution of suction feeding motor patterns in ray-finned fishes. In addition, the evidence illustrates the value of comprehensive EMG surveys of cranial muscle activities during suction feeding behavior.
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INTRODUCTION |
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SYNOPSISINTRODUCTIONTAXONOMIC SURVEY OF SUCTION...TESTING THE PHYLOGENETIC SCOPE...NEW EVIDENCE FROM THE...TARPON SUCTION FEEDING...THE ROLE OF LATERAL...References |
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Among the range of ray-finned fishes (Actinopterygii), suction feeding has been recognized as the dominant mode of aquatic prey capture (Lauder, 1983, 1985
). The critical movements of the cephalic anatomy during the suction feeding strike can be partitioned primarily among two phases, the expansive and compressive (Elshoud-Oldenhave and Osse, 1976; Lauder, 1985). These phases comprise the main sequences of rapid jaw and head movements that are essential to prey capture. Briefly, the expansive phase constitutes a rapid opening of the jaws and expansion of buccal cavity through cranial elevation, hyoid bar depression, and lateral expansion of the suspensorium. These movements in synergy generate a steep negative pressure gradient within the mouth that causes the water and presumably the prey in front of the head to be sucked into the mouth. The compressive phase begins with jaw closure and progresses posteriorly with hyoid protraction and suspensorium adduction, while the gill slits (opercular cavities) are opened to allow the engulfed water to flow out past the gills.
During the last quarter of the 20th century, advances in technology produced significant insights into the functional morphology, kinematics, and hydrodynamics involved in suction feeding behavior (for a historical review see Ferry-Graham and Lauder, 2001). One technology in particular, electromyography (EMG), has been used extensively to identify and compare the underlying neuromuscular controls (motor patterns) of this dynamic behavior.
The goals of this article are fourfold: 1) to present a taxonomic review of the major groups of ray-finned fishes in which suction feeding motor patterns have been described, 2) to review the evolutionary trends and paradigms of these motor patterns among basal and advanced groups, 3) provide qualitative evidence of suction feeding motor patterns from an unsampled group, the Elopomorpha, and 4) comment on an underappreciated aspect of suction feeding behavior, the role of lateral expansion.
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TAXONOMIC SURVEY OF SUCTION FEEDING MOTOR PATTERNS |
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SYNOPSISINTRODUCTIONTAXONOMIC SURVEY OF SUCTION...TESTING THE PHYLOGENETIC SCOPE...NEW EVIDENCE FROM THE...TARPON SUCTION FEEDING...THE ROLE OF LATERAL...References |
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Following Osse (1969)
, Ballintijn et al. (1972), and Liem (1978), numerous authors have undertaken EMG studies of fish feeding to investigate suction motor patterns among a variety of both primitive and advanced ray-finned fishes (see Table 2). Taxonomic sampling has occurred most frequently among the advanced euteleostean lineages of the Acanthopterygii, particularly in the Order Perciformes. According to this survey, suction feeding motor patterns of at least sixteen species from six families have been documented in this order (Table 2). This bias may be in part due to the overwhelming success of this radiation, the largest of vertebrate orders, which comprises 150 families and at least 6,900 species that inhabit all oceanic realms and many tropical and subtropical freshwater systems (Lauder and Liem, 1983).
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Fewer studies of suction feeding behavior have been conducted among the more basal actinopterygian fishes. Suction motor patterns have been recorded from the sole surviving species of the basal Halecomorpha, Amia calva (Lauder, 1980a
; Wainwright et al., 1989) and representative taxa from other more diverse basal and intermediate teleost groups such as the Osteoglossomorpha, Protacanthopterygii (Salmonidae), and Ostariophysii (see Table 2). However, motor pattern documentation is still lacking for other basal teleost groups. No evidence of feeding motor patterns has been recorded from the Elopomorpha and Clupeomorpha that together contain over 900 species (Lauder and Liem, 1983). Even several other advanced neoteleost groups such as the Stomiiformes, Aulopiformes, Myctophiformes, and the Paracanthopterygii, the sister group to the Acanthopterygii, have yet to be experimentally investigated. The upshot is that there is still a wealth of taxonomic diversity among suction feeding fishes that can further augment our understanding of the patterns of evolution in this dynamic behavior.
While the culmination of these pioneering studies of suction feeding behavior has provided a general mechanistic understanding of its neuromuscular control, many of these early taxonomic surveys were limited in the number of muscles recorded. Although more than ten different cephalic muscles may potentially be active and functionally important during the strike (see Table 1), many of these studies recorded fewer than five muscles simultaneously (Table 2). Some of the early EMG research on Amia calva, Salvelinus fontinalis, characid, and cichlid species (Lauder, 1980, 1981; Lauder and Liem, 1980; Liem, 1978) did extensive surveys of cephalic muscles during suction feeding. Although these experiments were mainly qualitative, they were invaluable in identifying the functional relationships between different muscles' activity patterns and the kinematic phases of the suction strike.
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TESTING THE PHYLOGENETIC SCOPE OF THE "CONSERVATION" PARADIGM |
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SYNOPSISINTRODUCTIONTAXONOMIC SURVEY OF SUCTION...TESTING THE PHYLOGENETIC SCOPE...NEW EVIDENCE FROM THE...TARPON SUCTION FEEDING...THE ROLE OF LATERAL...References |
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Later studies of feeding motor patterns of perciform fishes (Wainwright and Lauder, 1986
; Sanderson, 1988; Wainwright, 1989a) revealed through quantitative analyses that suction feeding and pharyngeal processing motor patterns remained evolutionarily conserved among closely related species in that no interspecific differences of the motor patterns could be detected. Wainwright et al. (1989) was the first study to test this conservation of neuromuscular evolution in suction feeding over a broad phylogenetic spectrum of ray-finned fishes. The authors used an elegant nested ANOVA experimental design that allowed them to partition individual and species variances. They estimated the mean suction motor patterns from three widely divergent groups of ray-finned fishes: the basal halecomorph fish, Amia calva, an osteoglossomorph fish, Notopterus chitala, and two advanced perciform fish, Micropterus salmoides and Lepomis macrochirus, (Fig. 1 and Table 2). The quantitative results indicated that there were significant motor pattern changes among these divergent groups that may have important functional consequences; yet they concluded that qualitative "general features" of the suction feeding motor pattern remained conserved. These general features refer to the sequence of recruitment for the four muscles analyzed. The expansive phase of the strike always began with jaw opening by levator operculi activity followed shortly by buccal cavity expansion through virtually simultaneous firing of the epaxialis and sternohyoideus muscles. Finally, the jaw closing adductor mandibulae was always the last muscle to be recruited and contributed the major activity of the compressive phase. The quantitative changes of suction motor patterns that were identified included differences in the duration and integrated area of activity for the epaxialis and sternohyoideus muscles as well as changes in the relative onset time of the adductor mandibulae (Fig. 1). Wainwright et al. (1989) noted that these were only statistically significant differences and proposed several hypotheses to test whether these motor pattern changes had resulted in functionally important performance changes in the mechanics of the suction strike.
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EP & SH > AM) across all species (see Other studies have analyzed how morphological disparity has affected suction feeding behavior. Westneat and Wainwright (1989)
investigated the evolution of extreme jaw protrusion in the sling jaw wrasse, Epibulus insidiator (Table 2). The authors recorded the suction motor pattern of the same four cephalic muscles as Wainwright et al. (1989) and performed similar ANOVA comparisons to Micropterus salmoides and Lepomis macrochirus. Interestingly, results showed that even with profound morphological and kinematic evolution of the feeding mechanism of the sling jaw wrasse, no changes to the underlying motor pattern could be detected (Fig. 1). The order of muscle firing remained the same as all other ray-finned fishes studied to date; yet, unlike the results of the broad phylogenetic comparison, the quantitative traits of the motor pattern were statistically indistinguishable from the other perciform species with less derived jaw protrusion. |
NEW EVIDENCE FROM THE ELOPOMORPHA |
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The Elopomorpha is a phylogenetically intermediate group of ray-finned fishes positioned between the Osteoglossomorpha and Clupeomorpha (Lauder and Liem, 1983
). This group contains over 600 species of fishes that range widely in their diversity of body forms and habitats. The group includes the silvery herring-like tenpounders (Elops sp.), tarpons (Megalops sp.), and bonefishes (Albula sp.) that inhabit tropical coastal seas, and eel-like forms such as deep water snipe eels (Nemichthyidae), tropical marine snake eels (Ophichthidae), and the famous catadromous freshwater American eel, Anguilla rostrata (Lauder and Liem, 1983). The well known synapomorphy supporting the monophyly of the Elopomorpha is the presence of a leptocephalus larval stage among all taxa. To date, suction feeding motor patterns have not been recorded from this unique group of fishes. The tarpon (Megalops atlanticus) is the largest species of the Elopomorpha growing to over 2 m in length (DeLoach, 1997), and is well known among gamefisherman as a ferocious piscivore making it an ideal elopomorph species to investigate suction feeding behavior.
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TARPON SUCTION FEEDING EXPERIMENTS |
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SYNOPSISINTRODUCTIONTAXONOMIC SURVEY OF SUCTION...TESTING THE PHYLOGENETIC SCOPE...NEW EVIDENCE FROM THE...TARPON SUCTION FEEDING...THE ROLE OF LATERAL...References |
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Due to the small sampling of individuals, the following emg study is presented as a qualitative description of suction motor patterns in the tarpon. Briefly, two tarpon specimens were purchased from local aquarium fish stores in Sacramento, CA. Both individuals (body sizes = 165 and 215 mm SL) were housed in 100 liter laboratory aquaria at 24 ± 2°C and were fed live goldfish (Carassius sp.) during kinematic/EMG experiments (for EMG experimental protocols see Grubich, 2000
). The mean suction feeding motor pattern of the tarpon (Fig. 2) retains the conserved firing order of cephalic muscles that is seen in all other described actinopterygians. The levator operculi (LO) is the first active muscle, on average, resulting in the initial opening of the jaws. The sternohyoideus (SH) is recruited nearly simultaneously with the LO and is shortly followed by the onset of the epaxialis (EP). The onset of the jaw closing muscle, the adductor mandibulae (AM), is delayed 30–40 msec initiating the compressive phase of the strike. In comparing the tarpon to other groups (Fig. 1), closer inspection of the motor pattern reveals qualitative characteristics of both primitive and advanced fishes. The shorter durations in the LO, EP, and SH and the delayed onset of the AM are similar to the advanced perciform taxa (Micropterus salmoides and Epibulus insidiator), but the long duration of activity in the AM (>100 msec) appears similar to the more basal Amia calva and Notopterus chitala.
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There are however, as mentioned earlier, several other cranial muscles that can influence both the expansive and compressive phases of the strike (Table 1). The most notable activity of the tarpon motor pattern was the dilator operculi (DO), an often unsampled muscle in suction EMG studies. It showed almost coincident recruitment of activity with the LO and had an unusually long burst duration lasting 140 msec on average, greater than any other muscle. Interestingly, activity in this muscle was continuous through both the expansive and compressive phases of the strike. It began activity as the buccal cavity expanded and remained active during jaw closure as indicated by activity in the adductor mandibulae (AM). These features of dilator operculi activity have been described in other intermediate actinopterygian fishes, Salvelinus fontinalis and Hoplias malabaricus (Lauder, 1980, 1981
). The question still remains as to whether this strong activity of the DO in the tarpon motor pattern has functional consequences for the suction strike.
A suction feeding sequence (Fig. 3) where EMG's and head movements (filmed at 500 f/sec) were simultaneously recorded, revealed nearly coincident buccal and opercular cavity expansion in the tarpon. As the kinematic trace shows, peak opercular abduction closely follows peak mouth gape and is delayed by merely 12 msec. Further, the onset and duration of activity in the dilator operculi, correlated closely with the kinematic pattern of the operculum (Fig. 3). This close temporal coincidence between peak gape and peak opercular abduction is similar to strike kinematics reported for the intermediate teleosts Salmo gairdneri, Salmo fontinalis (Protacanthopterygii), and Hoplias malabaricus (Ostariophysii) (i.e., 
10–15 msec; Lauder, 1979; Lauder and Liem, 1980) but differs substantially from those patterns reported from the basal Halecomorph, Amia calva (i.e., 25–30 msec; Lauder, 1980a), and an advanced acanthopterygian fish, Lepomis sp (i.e., 35–45 msec; Lauder, 1980b, 1985). A delay in lateral expansion of the operculum until the compressive phase as seen in Amia and Lepomis has been marked as a consistent feature of the suction strike in teleosts (Lauder, 1983, 1985). Although larger sample sizes are needed to verify the generality of this kinematic pattern in tarpon, the suction strike presented here and that reported in other intermediate teleosts actually indicates that among some groups opercular abduction begins much earlier during the expansive phase of the strike.
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THE ROLE OF LATERAL EXPANSION IN SUCTION FEEDING |
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SYNOPSISINTRODUCTIONTAXONOMIC SURVEY OF SUCTION...TESTING THE PHYLOGENETIC SCOPE...NEW EVIDENCE FROM THE...TARPON SUCTION FEEDING...THE ROLE OF LATERAL...References |
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Previous comparative EMG studies of suction feeding in ray-finned fishes have focused on cranial muscles that predominantly affect strike kinematics along the dorso-ventral axis (LO, EP, SH, and AM; Table 1). Future comparative studies should employ a more comprehensive approach when investigating the variation in motor patterns that underlie aquatic prey capture by also recording cranial muscles that influence head expansion and compression along the lateral axis (LAP, AAP, DO, AO, SH, and GH; Table 1). The relationship between motor pattern variation and suction feeding performance in the largemouth bass has raised the potential importance of lateral expansion (Grubich and Wainwright, 1997
). In this study, activity in the LAP, a suspensorium abductor, was always present during varying magnitudes of suction strikes, while activity in the predominantly dorso-ventrally acting muscles, EP and SH were not. Further, hydrodynamic modeling and experimental analysis of prey capture in rainbow trout (Salmo gairdneri) identified the relationship between opercular abduction and mouth opening as critical to the maximization of flow velocity into the buccal cavity during suction feeding (van Leeuwen, 1984). A key component of this relationship in rainbow trout was the timing of body velocity (a.k.a. ram movement) during opercular abduction which prevented backflow of water into the opercular cavity. Tarpon appeared to employ a feeding strategy that was consistent with this relationship. Typically, the tarpon would first slowly approach the prey from below with a closed mouth and operculum, and then would rapidly lunge upward as the mouth and operculum were sequentially expanded during the suction strike. Phylogenetically, suction feeding muscle activities that are indicative of lateral expansion have been consistently documented (though rarely elaborated on) among intermediate and advanced teleosts groups (e.g., Ostariophysii, Protacanthopterygii, and Acanthopterygii). This evidence, taken in conjunction with the new evidence from the basal elopomorph tarpon, suggest that lateral expansion movements and the motor patterns that generate them may be underappreciated mechanisms in the evolution of suction feeding behaviors among actinopterygian fishes and deserve further investigation.
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ACKNOWLEDGMENTS |
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Tom Waltzek was instrumental in obtaining specimens and helping during feeding experiments. Mike Alfaro and Tom Waltzek provided valuable insights during the generation of this manuscript. Special heartfelt thanks and appreciation goes to Kandice McGarvey who was immeasurably supportive and encouraging during this time. I would also like to thank Mike Alfaro and Anthony Herrel for the invitation and organization of such an interesting and thought provoking 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 New address for correspondence: Department of Biological Science, Florida State University, Tallahassee, Florida 32306; E-mail: grubich{at}fsu.edu
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References |
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