Prey capture in actinopterygian fishes: A review of suction feeding motor patterns with new evidence from an elopomorph fish, Megalops atlanticus

American Zoologist, Dec 2001 by Grubich, Justin R

Prey Capture in Actinopterygian Fishes: A Review of Suction Feeding Motor Patterns with New Evidence from an Elopomorph Fish, Megalops atlanticus1

SYNOPSIS. 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 (ie., 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.

Among the range of ray-tinned 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.

TAXONOMIC SURVEY OF SUCTION FEEDING MOTOR PATTERNS

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).

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.