A unique feeding method by a teleost fish, the fourhorn poacher Hypsagonus quadricornis (Agonidae).
Teleost fishes employ a wide range of feeding techniques (1), but these rarely involve direct manipulation of objects in order to uncover prey. Some species locate food by using jets of water from the mouth to "blow" at unconsolidated sediments (2) or by using their pectoral fins to fan or move sand aside (3). Moving larger objects is limited to some cichlids that turn over sunken leaves when searching for food (4), triggerfish that move rocks by mouth (5), and labrids that turn gravel using their snout and mouth (6). However, because the mouth is used to grasp and move these larger objects and is thus occupied, such techniques would be of limited use when hunting concealed prey that can quickly move when its shelter is disturbed. Observations of a rarely seen poacher (family Agonidae) have revealed a unique feeding method in which the mechanism for uncovering prey is independent from the mouth, enabling the fish to effectively manipulate objects while leaving the mouth free for prey capture.
Agonids are heavily armored benthic forms, limited in distribution to colder seas. They occur in greatest diversity in the North Pacific. Owing to their often inaccessible habitats and lack of commercial importance, very little is known about the behavior or ecology of this unusual group of fishes. The family encompasses a tremendous variety of body shapes, ranging from long and extremely slender to short and stout. One of the most ornate species is the fourhorn poacher, Hypsagonus quadricornis (Valenciennes 1829), which occurs at depths of 0-452 m in the Sea of Okhotsk and Kuril Islands in the western Pacific and from the Bering Sea to Puget Sound, Washington, in the eastern Pacific (7). This small (to 120 mm total length) slow-moving fish is a very limited swimmer, relying instead on an unusual method of "walking" along the bottom using its pectoral fins and caudal fin. The upper and lower portions of the pectoral fins move separately in a manner analogous to the way anglerfishes use pectoral and pelvic fins during amphipedal progression, or "crutching" (8). As the upper portion of the pectoral fins moves anteriorly, the tail is curled forward; the tail then straightens and pushes against the substrate as the fingerlike lower rays of the pectoral fins pivot anteriorly. The enlarged anal fin is splayed out against the substrate in the opposite direction of the tail, helping to counter the lateral force so that propulsion is directed forward. The fish does not alternate sides when using this "caudal looping" motion, unlike the more forceful terrestrial propulsion described for an intertidal rockskipper (9).
The fingerlike rays used in locomotion are also the primary tools used for dislodging and lifting small rocks, shells, and other materials when foraging for food. The fish positions itself alongside an object and inserts the lowermost pectoral rays under the edge of the object (Fig. 1A), while the opposite pectoral fin provides the primary support (Fig. 1B). When lifting heavier materials, the fish curls its tail forward on the opposite side and straightens it against the substrate to provide additional thrust. As the object is raised, the fish places its head underneath in search of prey (Fig. 1B, C). Lighter objects are often completely overturned (Fig. 1D). Video clips of this behavior can be viewed at <http://www.biolbull.org/supplemental/>.
This appears to be the primary means by which the species forages. Specimens collected from the Pribilof and Aleutian islands, Alaska, and from Washington State have all routinely displayed this behavior within a few days of being placed in an aquarium, and all sizes observed (28-110 mm total length; n = 11) have used this method. Upon the addition of live prey (e.g., gammarid amphipods) to a tank, previously inactive fish will typically initiate shell-lifting behavior. Video analysis of an Aleutian Island specimen (100 mm total length; weight 15 g) presented with six scallop shells (Chlamys hastata, length 42-50 mm) resting on sand revealed the fish systematically lifting and inspecting each shell, and alternating its lifts between its right and left pectoral fins. All six shells were lifted within an 18-min period, and all but one was completely turned over--some more than once. To roughly gauge how much this individual fish was capable of lifting relative to its body mass, single valves of scallop shells were weighted with various amounts of lead shot (total weights 3, 5, 7, 9, 12, and 15 g) and placed flat against the sand. The poacher was able to flip the 7-g shell but was unable to lift the heavier ones, despite making repeated efforts from all sides. Because the scallop shells lay flush with the substrate, only the tips of the lowermost pectoral rays could be placed underneath to start the lift; heavier objects could be turned or shifted if they were already slightly elevated, allowing more rays to be used and providing a better angle for lifting.
An analysis of the stomach contents of wild-caught specimens from the western Pacific revealed a diet consisting almost exclusively of equal amounts of gammarid amphipods and polychaetes (7), food items consistent with this type of search strategy and abundant in the areas where the specimens were collected. Foraging activities may be diurnal or crepuscular since captive specimens are inactive and unresponsive when observed under infrared light at night; however, the means by which uncovered prey are detected is not yet known. In lighted aquaria the fish can be clearly seen tracking moving prey visually, but visual tracking may not be possible at the deeper end of the species' depth range. It is possible that the free rays of the pectoral fins have chemosensory abilities that are similar to those that gurnards (Triglidae) use to probe for prey in sand (10, 11), or that the lateral line or the prominent nasal cirrus (most visible in Fig. 1B and D) plays a role in detecting prey.
Lifting behavior may be rare among the Agonidae and is possibly limited to the genus Hypsagonus, since long-term personal observations of captive agonids in eight other genera (Agonopsis, Ocella, Odontopyxis, Bothragonus, Xeneretmus, Agonus, Pallasina, and Anaplagonus) have not revealed any similar behaviors. Of the five species of Hypsagonus, only two (H. corniger Tarametz 1933 and H. jordani Jordan 1904) have several free pectoral rays similar to those used for lifting by H. quadricornis, suggesting that they may be capable of similar behavior. Kelp poachers, H. mozinoi (Wilimovsky and Wilson, 1979), have only two free rays and have been observed pushing gravel aside with the pectoral fins in an apparent attempt to uncover prey (J. Marliave, Vancouver Aquarium, pers. comm.).
The behavior described here for H. quadricornis gives the species access to food resources that may otherwise be unavailable. It represents a novel use of fins as limbs and allows a more sophisticated manipulation of objects than previously known in fish. In addition to being behaviorally unique, it raises interesting questions about the structural modifications involved. The functional morphology of the pectoral girdle and the other muscular and skeletal elements involved in lifting and locomotion in this species is a rich area for study and may offer phylogenetic insights as well.
Thanks to the National Marine Fisheries Service, Alaska Fisheries Science Center, RACE Division, and Shannon Point Marine Center for assistance in collecting the specimens, and to T.W. Pietsch and two anonymous reviewers for their helpful comments.
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GREGORY C. JENSEN
School of Aquatic and Fishery Sciences, Box 355020, University of Washington, Seattle, Washington 98195
Received 10 August 2005; accepted 13 October 2005.
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|Author:||Jensen, Gregory C.|
|Publication:||The Biological Bulletin|
|Date:||Dec 1, 2005|
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