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Chemoreception in an arctic amphipod crustacean: A field study
J. Exp. Mar. Biol. Ecol., 1982, Vol. 62, pp. 261-269 Elsevier Biomedical Press
261
CHEMORECEPTION IN AN ARCTIC AMPHIPOD CRUSTACEAN: A FIELD STUDY
M. BUSDOSH Woodward-Clyde Consultants. EnvironmentalSystems Division, 3489 Kurtz Street, San Diego, CA 92110. U.S.A. G.
A. ROBILLIARD
Woodward-Clyde Consultants, San Fran&co. CA 94111, U.S.A. K. TARBOX’ Woodward-Clyde Consultants,Anchorage, AK 99503, U.S.A.
C.
L. BEEHLER’
Woodward-Clyde Consultants, San Diego, CA 92110, U.S.A Abstract: Traps baited with meat or fish were set through the ice in 5 m of water near Prudhoe Bay, Alaska. They were monitored by divers and surface observers. Over 99% of the animals attracted to the bait were the lysianassid amphipod Boeckosimus (= Onirimus) a&is (Hansen). Up to 20000 individuals were collected during each 24-h trapping period. Animals moved to the trap only from a downcurrent direction, and from a distance of up to at least 30 m away. It is suggested that chemoreception is the method used to find bait: animals swam into the current after receiving the stimulus and required a constant presence of stimulus at some threshold level to continue moving to the bait.
Use of baited traps to catch marine invertebrates is not a recent innovation. Crabs and lobsters, invertebrates edible to man, have been taken in this manner for centuries. One of the first published uses of baited traps in the Arctic was by Greely (1886), as his crew tried desperately, with minimal success, to ward off starvation after being shipwrecked in the Canadian Arctic. Walker (1907) used baited traps to capture large numbers of amphipods in the Antarctic, and in the 195Os, MacGinitie (1955) and Barnard (1959) used baited traps to sample invertebrates in the Alaskan Arctic. The ability of invertebrates to fmd bait, often in dark and turbid waters, is ascribed to chemoreception. Mackie & Shelton (1972) have listed five separate studies noting ’ Present address: Alaska Department of Fish and Game, Soldotna, AK 99669, U.S.A. 2 Present address: Department of Physics, University of California, Santa Barbara, Goleta, CA 93106, U.S.A. 0022-O981/82/OOOO-0000/$02.750 1982 Elsevier Biomedical Press
267
M. BUSDOSN
ETAL.
such characteristics as long ago as 1897. Much laboratory study has been accomplished on types and concentrations of compounds necessary to stimulate chemoreceptors, and the location of chemoreceptors on crustacean bodies (see Lindstedt’s reviews, 197 1, in press). The capacity of chemoreceptors to work over distance has been examined in the laboratory, but distances have been restricted to a few meters. Barnard (1959) speculating on distances from which arctic ~phipods were attracted in the ocean, suggested attraction “on the order of yards and not fractions of a mile’“.There has been little work accomplished in situ, however, to actually measure these distances. This study was designed to evaluate how and from what distances animals respond to baited traps during winter (under-ice) conditions. MATERKALS AND METHQDS
Traps were set on a silty, low relief bottom in 5 m of water, 3000 m offshore in the Beaufort Sea near Prudhoe Bay, Alaska. Standard minnow traps (6-mm mesh) and shrimp baskets (13-mm mesh) were baited with 1 to 5 lb of either medium-rare beef, fish (Mugil cephalus), or fish and canned sardines with mustard. Traps were set in the morning and retrieved the following morning. On 30 April and 2 May, 1979, two baited traps were moni~r~ periodically by divers. Noted were areas and distances from which animals moved to the bait, behavior of amphipods affeeted and not affected by the presence of bait, numbers of animals attracted, and the water current direction. Along with the divers’ observations, each trap was visually monitored from the surface. RESULTS
More than 99% of the individuals taken were the amphipod Boecku,~&rus( = Onisimw) &his (Hansen). Over each 24-h sampling period up to 20000 individuals of this species were attracted to the bait in each trap. Three different behavior patterns were exhibited by B. ajhis during this study. In the areas designated A (Fig. 1) the animals swam slowly and intermitte#Iy along the bottom with a back-and-forth “sweeping*’ pattern, frequently changing direction. This behavior was commonly observed by divers during many underwater hours in the vicinity on related studies. Wiihin the talI, narrow triangle of area B, amphipods swam directly upeurrent toward the bait. In contrast to the normal sweeping movements of animals in area A, the path of those within B varied -C 15” on either side of a direct line to the trap, with the animals quickly coming back “on line”. This triangle was % 1 m wide at a distance of 5 m from the trap, widening to = 5 m at a distance of 25 m, the limit of the divers’ safety lines. Excellent visibility aIlowed the divers to extend the length of area B another
CHEMORECEPTION
IN AN ARCTIC AMPHIPOD
263 3
5 Meters
5
. 5
Normal Direct,
0
5 Meters
movement rapid movement
Swarming
to bait
movement
f Fig. 1. Areas delineating behavioral differences of Boeckosimus ujinis.
264
M. BUSDOSH ETAL.
5 m, where B. affinis were observed swimming directly toward the trap from the limits of visibility. The animals swam more quickly in area B than in area A, and swam steadily, without the ch~~t~sti~ inte~tt~t movement of those in area A. The animals swam within 5 cm of the bottom along the path. A line drawn perpendicular to the current anywhere along area B was crossed by 75 to 100 animals/min for the first several hours of the study. Stationary current meters near the study site showed no measurable current (threshold 2.57 cm/s) at the time ofthe experiment. The maximum bottom current at the site at any time, measured with a remote meter, in February, March, and April, was 1.68 cm/s (Mangarella et al., 1979). A heightened state of activity occurred in the area designated C, an area extending z 1 m from the trap in directions perpendicular to the current, and for 2 m downcurrent of the trap. After a few hours of bait exposure, area C was occupied by a seething mass of amphipods sing quickly and randomly into and around the trap, up to a meter off the bottom. Animals began moving to the ban within 10 min of its placement. Within 1 h all bait pieces were totally covered by feeding amphipods, and within 6 h a mass of several thousand scavengers was moving about the trap. At this point fewer animals were being attracted, and from not as great distances as occurred initially. After apparent satiation, animals lay on their sides on the bottom, curled into a C-shape. Twenty-four h after the removal or consumption of bait most animals had dispersed. Divers observed more B. afinis in the general area for 48 to 72 h after the bait had been offered than were noted in dives prior to a trapping period.
DISCUSSION
Boeckosimris affmus is common in the North American Arctic, and has been taken with baited traps extensively in both Alaska (Busdosh & Atlas, 1975; Busdosh et al.,
1978) and Canada (Percy, 1975). The behavior of amphipods in the areas designated A in Fig. 1 was the normal, searching pattern exhibit&d by the species. As the behavior in area A is not affected by the baited traps, it will not be considered further. Crustaceans may detect food at a distance by vibration receptors, sight, or chemoreception (Iiindley, 1975). With a non-living ban it is unlikely that vibration is me~in~ul. Form vision is rudimentary, and visual cues play a minor role in feeding behavior (Bullock & Porridge, 1965; Fuzessery & Childress, 1975; Hindley, 1975). Dahl(l979) concluded chemosensory stimulation was the most likely agency by which amphipods were led to carrion on the deep sea bottom. Amphipods studied by Dahl belong to the family Lysianassidae, which contains many species that are scavengers. B. a~~j~ also belongs to this family, which is rno~ho~o~~y adapted for e&ient chemoreception of stimuli carried by water currents (Dahl 1977, 1979). Lindstedt (197 1, in press) has thoroughly reviewed a chemoreception literature that
CHEMORECEPTION
IN AN ARCTIC AMPHIPOD
265
“is extremely scattered and has little unity of terminology or method.. .“. Investigators have generally agreed that amino acids are a stimulus to crustacean chemoreceptors, and that combinations are more successful than individual chemicals (Mackie & Shelton, 1972; Shelton & Mackie, 1972; Bardach, 1975; Fuzessery & Childress, 1975; McLeese, 1970). B: @innis has been attracted to traps baited with fish, roast beef, and canned sardines (in the present study), and with rotting whale meat, seal blubber, and fish (Busdosh & Atlas, 1975; Busdosh et al., 1978). Based on this field study and on evidence from the investigations cited, the following scenario seems to best explain the amphipods behavioral reaction to the bait. The animals in the long, thin triangle of area B (Fig. 1) received chemical stimuli from the bait. These stimuli were carried in the water passing over the animals, by the slow but constant current. These animals moved to the bait, and as these first arrivals fed the bait became shredded, which allowed more bait solution and created more food particles sufficiently small to be carried by the current. This activity of the first arrivals allowed a more concentrated signal to be sent out, a signal strong enough to attract animals in area B at increasing distances from the bait. Reference to Fig. 1 leaves little doubt the chemical stimuli were current-borne. No animals reacted to the bait in any area except downcurrent of the bait. These animals, those of area B, for B delineates the area of sufficient stimulus, then moved to the bait. One of two mechanisms would seem likely to account for this movement: (1) amphipods swim up a gradient of everincreasing strength; (2) amphipods orient and swim into the current after reception of stimulus. Hamner & Hamner (1977) demonstrated that a planktonic shrimp (Acetes sibogae austrulis) followed scent trails of sinking food. Upon encountering a scent, the animals descended along the food’s trail. However, when food was raised up through the water column, rather than allowed to sink, the shrimp still descended upon contact with the scent, moving along a decreasing gradient. They concluded that the shrimp do not follow a chemical gradient, but have evolved a pattern for feeding on falling material. Hindley’s work (1975) with a prawn (Penaeus merguiensis) led him to conclude that while the animals could locate food in still water, the mechanism was not very efficient. He concluded the prawn reacted to current after recognizing food, and that the chemical gradient was important only when near food. Castilla & Crisp (1973) reported a starfish was able to respond to a gradient between two streams of water, and followed the stream whose water contained the attractant. They pointed out that still water is necessary for a true gradient, and still water is an impossibility in the natural habitat of starfish. They conclude, “ . . .the only effective response of an animal to chemical stimulus in nature is to follow the scent upstream”. The preceding implies that B. afinis received a chemical stimulus, interpreted the signal as food, and swam upcurrent to the source. A slight but sudden change in current direction during the experiment proved fortuitous. Had amphipods continued to move into the current, now from a slightly different direction, they would not have found the bait. However, movement into the
266
M. BUSDOSH
ET AL.
current did not continue: animals quickly went into a back-and-forth searching pattern until they again were in the scent plume. These observations indicate amphipods do not simply sense food one time and then swim upcurrent until they fmd it. The adjustments made by animals out of the scent plume do not establish that a chemical gradient is being followed, but do establish that loss of the attractant scent stops the movement into the current. It would seem that an exposure above some threshold level of the attractant is required to stimulate constant undirectional movement, and when this threshold is not attained, the searching behavior dominates. The apparent confusion in area C near the trap may be the result of, or the combination of, different factors. In the close proximity of the bait, an arrestant may be present. Lindstedt (197 1) defined such a substance as “a stimulus that causes an animal to cease locomotion when in close contact with an apparent source”. If so, the arrestant may be the source itself in this case. Thousands offeeding amphipods caused the water surrounding the trap to be a slurry of dissolved food and food particles. The density of this slurry may have been sufficient to be recognized as the source itself. Another possible cause for the movement was the lack of available surface area on the bait. Animals arriving after the first few hours found the surface of the bait completely covered by a tightly-packed mass of amphipods. Along with the demonstration that constant sensing of attractant is coupled with orientation into current, the present study points out that chemoreception works over long distances in real-world situations - animals 15 mm in length were drawn to a bait from a minimum of 30 m. Correlated with this long-ranging effect are the numbers of animals drawn, with an estimated 20000 amphipods attracted by 5 kg of bait. The question of where 20000 amphipods originated prior to moving to the bait can be speculated on only very tenuously. No thorough definition of the density of B. affl& in this area has been accomplished. Chin et al.‘s (1979) data indicated 15 animaIs/m2, based on five samples at each of only three stations. If such a density is valid, then triangle B would need to project a distance of 115 m from the bait to attract 20 000 animals. Several factors indicate that such a distance, in a real-world situation, is unnecessarily large. Consideration must be made that these animals are motile. Busdosh (1981) has shown, in laboratory experiments, that members of this species move on the average of 100 cm/mm, and spend more than half of the time moving during their active period. Busdosh et al. (1978) and Percy (1977) have both noted that this species divides its time between swimming and remaining burrowed, an alternation of activity that Percy (pers. comm.) suggests may be related to the tidal cycle. For our purposes we can assume that a specimen moves 100 cm/n& for one-half of its active time. If tide-related, whether ebb or flow, this active period would approximate 12 h. Manipulation of these estimates gives a potential movement of 360 m per day per animal. Such a figure, if within even an order of magnitude, underscores the importance of motility. A large number of animals in the normal activity of area A could move into area B,
CHEMORECEPTIONINANARCTICAMPHIPOD
267
sense the bait, and move to it. There is essentially no return of animals to area A, as any individual entering area B will remain within its confmes, and move to the bait. This motility would allow a large number of animals near the trap, but initially not within area B, to become captured. Compoundiig this factor’s effect would be current shifts, which would bring stimulus to a different group of animals along a different axis to the trap, yet not lose all of the animals along the former axis, who, once stimulated, searched for the stimulus again. Although the shallow Beaufort Sea has several motile species, response to baited traps has been almost exclusively by B. ufjinis in water z 5 m depth, and by two other lyssianassid amphipods, Onisimus ( = Pseudalibrotus) gIacialis and 0. litoralis, in shallower waters. ~~~kos~~ a&i% is largely a d~tivore. Many hours of field observation by divers show the animals moving about the bottom, picking among sediment particles and debris. Detritus is perhaps the primary food source. Sufficient vertebrate carcasses may not be available to sustain large populations of amphipods, as whales and seals do not occur in the area during most of the year, and marine fish populations do not seem abundantly widespread throughout the zone. Working in the deep sea, Dayton & Hessler (1972) and Isaacs (1969) noted the presence of several species of large, motile scavengers that quickly find bait (s~ula~g carcasses), apparently by current-borne clues. Dayton & Hessler (1972) suggested these animals quickly break down large food parcels (carcasses) which fall to the ocean floor, resulting in greater availability of food (as small pieces or as feces) to other bottom dwellers. The Beaufort Sea off the coast of Alaska does not seem to have several species of large, highly motile scavengers; it does not seem to have any. This role has apparently been assumed by small ( w 15 mm) ~phipods, and then by only two or three species. The apparent lack of large, highly motile scavengers may indicate there are not sufficient carcasses to support a population. The amphipod Boeckosimus aflnis is a detritalfeeding, small, motile scavenger, with chemoreceptive capabilities to allow it to find and utilize the occasional rich protein source of a carcass. ACKNOWLEDGEMENTS
This study was performed under the sponsorship of the owner companies of the Prudhoe Bay Unit, and with the assistance of personnel from ARC0 Oil and Gas Company. Our thanks to ARCO’s Dr. .I. Lindstedt Siva who shared her experience and library on the subject, and who graciously reviewed the manuscript. We would like to thank Dr. R. W. Firth, Jr., for his help in the coordination of the project. Literature research was sponsored by the Professional Development Fund of Woodward-Clyde Consultants.
268
M. BUSDOSH ET AL. REFERENCES
BARDACH,J. E., 1975. Chemoreception of aquatic animals. In, Olfaction and taste. Part V, edited by D.A. Denton & J.P. Coghlan, Pergamon Press, New York, pp, 121-132. BARNARD,J. L., 1959. Epipelagic and under ice amphipoda of the central Arctic Basin. In, Scientific studies at Fletcher’s Ice Island, T-3 (1952-1955), edited by V. Bushnell, U.S. Air Force Cambridge Research Center. Geophysical Research Paper, Vol. 63, pp. 115-152. BULLOCK,T. H. & G. A. HORRIDGE,1965. Structure andfunction in the nervous systems ojinvertebrates, Vol. 2, W. H. Freeman & Co., San Francisco, 1719 pp. BUSDOSH,M., 1981. Long-term effects of the water soluble fraction of Prudhoe Bay crude oil on survival, movement, and food search success in the arctic amphipod Eoeckarimus (= Onlsimus) aflnis. Mar. Environ. Res., Vol. 5, pp. 167-180. BUSDOSH, M. & R.M. ATLAS, 1975. Response of two arctic amphipods, Gammarus zaddachi and Boeckostmus ( = Onistmus) a&is, to variations in temperature and salinity. J. Ftsh Res. Board Can., Vol. 32, pp. 2564-2568. B~JSDOSH,M., K.W. DOBRA, A. HOROWITZ,S.E. NEFF L R.M. ATLAS, 1978.Potential long-term effects ojPrudhoe Bay crude oil in arctic sediments on indigenous benthic invertebrate communities. Am. Institute of Biol. Sci. Proceedings of the conference on assessment of ecological impacts of oil spills; June 14--t7 1978; Keystone, Colorado, pp. 856-869. CASTILLA,J.C. & D. 3. CRISP, 1973. Responses of&ret&s rubens to water currents and their modifications by certain environmental factors. Neth. J. Sea Res., Vol. 7, pp. 171-190. CHIN, H., A. NIEDORODA,G.A. ROBILLIARD& M. BUSDOSH,1979. Related studies: biological effects of impingement and entrainment from operation of the proposed intake. in. Prudehoe Bay waterflood project. Woodward-Clyde Consultants, Dec. 1979, pp. 3-1 to 3-136. DAHL, E., 1977. The amphipod functional model and its bearing upon systematics and phylogeny. Zoof. Scripta, Vol. 6, pp. 221-228. DAHL, E., 1979. Deep-sea carrion feeding amphipods: evolutionary patterns in niche adaptation. O&OS, Vol. 33, pp. 167-175. DAYTON,P. K. & R. R. HESSLER,1972. Role of biological disturbance in maintaining diversity in the deep sea. Deep-Sea Res., Vol. 19, pp. 199-210. FUZESSERY,Z.M. & J.J. CHILDRESS,1975. Comparative chemosensitivity to amino acids and their role in the feeding activity of bathypelagic and littoral crustaceans. Biol. Bull. (Woods Hole. Mass.), Vol. 149, pp. 522-538. GREELY,A. W., 1886. Three years ojarctic service, Vol. 2. An account of the Lady Franklin Bay Expedition of 1881-1884, and the attainment of farthest north. Charles Scribner’s Sons, New York. HAMNER,P. & W.M. HAMNER, 1977. Chemosensory tracking of scent trails by the planktonic shrimp Acetes sibogae australis. Science, Vol. 195, pp. 886-888. HINDLEY,J. P. R., 1975.The detection, location and recognition of food by juvenile banana prawns, Penaeus merguiensis de Man. Mar. Behav. Physiol., Vol. 3, pp. 193-210. ISAACS, J. D., 1969. The nature of oceanic life. Sci. Am., Vol. 221, pp. 146162. LINDSTEDT, K.J., 1971. Chemical control of feeding behavior. Camp. Biochem. Physiol., Vol. 39A, pp. 553-581. LINDSTEDT,K. J., in press. Chemical control offeeding behavior in some aquatic organisms. CRC Handbook on nutrition and food. CRC Press, West Palm Beach, Florida. MACGINITIE,G.E., 1955. Distribution and ecology of the marine invertebrates of Pt. Barrow, Alaska. Smtthson. Misc. Collect., Vol. 128, pp. l-201. MACKIE, A.M. & R.G.J. SHELTON,1972. A whole-animal bioassay for the determination of the food attractants of the lobster Homarus gammarus. Mar. Biol., Vol. 14, pp. 217-22 1. MANGARELLA,P., H. CHIN & A. NIEDORODA,1979. Under-ice water conditions in the Beaufort Sea relative to the proposed watefflood discharge. In, Environmental studies ojihe Beaufort Sea, winter 1979. Woodward-Clyde Consultants, Dec. 1979, pp. l-252. MCLEESE, D. W., 1970. Detection of dissolved substances by the American lobster (Homarus americanus) and olfactory attraction between lobsters. J. Fish Res. Board Can., Vol. 27, pp. 1371-1378. PERCY,J. A., 1975. Ecological physiology of arctic marine invertebrates. Temperature and salinity relationships of the amphipod Onisimus a@&, H. J. Hansen. J. Exp. Mar. Biol. Ecol.. Vol. 20, pp. 99-117.
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IN AN ARCTIC AMPHIPOD
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PERCY,J. A., 1977. Responses of arctic marine benthic crustaceans to sediments contaminated with crude oil. Environ. Pollut., Vol. 13, pp. 155-162. SHELTON,R. G.J. & A.M. MACKIE, 1972. Studies on the chemical preferences of the shore crab, Curcinus maena~ (L.). J. Ex;p. Mar. Biol. Ecol., Vol. 7, pp. 4149. WALKER, A.O., 1907. Crustacea 3: Amphipoda. Natn. Antarct. Exped. 1901-1904, Vol. 3, 39 pp.
261
CHEMORECEPTION IN AN ARCTIC AMPHIPOD CRUSTACEAN: A FIELD STUDY
M. BUSDOSH Woodward-Clyde Consultants. EnvironmentalSystems Division, 3489 Kurtz Street, San Diego, CA 92110. U.S.A. G.
A. ROBILLIARD
Woodward-Clyde Consultants, San Fran&co. CA 94111, U.S.A. K. TARBOX’ Woodward-Clyde Consultants,Anchorage, AK 99503, U.S.A.
C.
L. BEEHLER’
Woodward-Clyde Consultants, San Diego, CA 92110, U.S.A Abstract: Traps baited with meat or fish were set through the ice in 5 m of water near Prudhoe Bay, Alaska. They were monitored by divers and surface observers. Over 99% of the animals attracted to the bait were the lysianassid amphipod Boeckosimus (= Onirimus) a&is (Hansen). Up to 20000 individuals were collected during each 24-h trapping period. Animals moved to the trap only from a downcurrent direction, and from a distance of up to at least 30 m away. It is suggested that chemoreception is the method used to find bait: animals swam into the current after receiving the stimulus and required a constant presence of stimulus at some threshold level to continue moving to the bait.
Use of baited traps to catch marine invertebrates is not a recent innovation. Crabs and lobsters, invertebrates edible to man, have been taken in this manner for centuries. One of the first published uses of baited traps in the Arctic was by Greely (1886), as his crew tried desperately, with minimal success, to ward off starvation after being shipwrecked in the Canadian Arctic. Walker (1907) used baited traps to capture large numbers of amphipods in the Antarctic, and in the 195Os, MacGinitie (1955) and Barnard (1959) used baited traps to sample invertebrates in the Alaskan Arctic. The ability of invertebrates to fmd bait, often in dark and turbid waters, is ascribed to chemoreception. Mackie & Shelton (1972) have listed five separate studies noting ’ Present address: Alaska Department of Fish and Game, Soldotna, AK 99669, U.S.A. 2 Present address: Department of Physics, University of California, Santa Barbara, Goleta, CA 93106, U.S.A. 0022-O981/82/OOOO-0000/$02.750 1982 Elsevier Biomedical Press
267
M. BUSDOSN
ETAL.
such characteristics as long ago as 1897. Much laboratory study has been accomplished on types and concentrations of compounds necessary to stimulate chemoreceptors, and the location of chemoreceptors on crustacean bodies (see Lindstedt’s reviews, 197 1, in press). The capacity of chemoreceptors to work over distance has been examined in the laboratory, but distances have been restricted to a few meters. Barnard (1959) speculating on distances from which arctic ~phipods were attracted in the ocean, suggested attraction “on the order of yards and not fractions of a mile’“.There has been little work accomplished in situ, however, to actually measure these distances. This study was designed to evaluate how and from what distances animals respond to baited traps during winter (under-ice) conditions. MATERKALS AND METHQDS
Traps were set on a silty, low relief bottom in 5 m of water, 3000 m offshore in the Beaufort Sea near Prudhoe Bay, Alaska. Standard minnow traps (6-mm mesh) and shrimp baskets (13-mm mesh) were baited with 1 to 5 lb of either medium-rare beef, fish (Mugil cephalus), or fish and canned sardines with mustard. Traps were set in the morning and retrieved the following morning. On 30 April and 2 May, 1979, two baited traps were moni~r~ periodically by divers. Noted were areas and distances from which animals moved to the bait, behavior of amphipods affeeted and not affected by the presence of bait, numbers of animals attracted, and the water current direction. Along with the divers’ observations, each trap was visually monitored from the surface. RESULTS
More than 99% of the individuals taken were the amphipod Boecku,~&rus( = Onisimw) &his (Hansen). Over each 24-h sampling period up to 20000 individuals of this species were attracted to the bait in each trap. Three different behavior patterns were exhibited by B. ajhis during this study. In the areas designated A (Fig. 1) the animals swam slowly and intermitte#Iy along the bottom with a back-and-forth “sweeping*’ pattern, frequently changing direction. This behavior was commonly observed by divers during many underwater hours in the vicinity on related studies. Wiihin the talI, narrow triangle of area B, amphipods swam directly upeurrent toward the bait. In contrast to the normal sweeping movements of animals in area A, the path of those within B varied -C 15” on either side of a direct line to the trap, with the animals quickly coming back “on line”. This triangle was % 1 m wide at a distance of 5 m from the trap, widening to = 5 m at a distance of 25 m, the limit of the divers’ safety lines. Excellent visibility aIlowed the divers to extend the length of area B another
CHEMORECEPTION
IN AN ARCTIC AMPHIPOD
263 3
5 Meters
5
. 5
Normal Direct,
0
5 Meters
movement rapid movement
Swarming
to bait
movement
f Fig. 1. Areas delineating behavioral differences of Boeckosimus ujinis.
264
M. BUSDOSH ETAL.
5 m, where B. affinis were observed swimming directly toward the trap from the limits of visibility. The animals swam more quickly in area B than in area A, and swam steadily, without the ch~~t~sti~ inte~tt~t movement of those in area A. The animals swam within 5 cm of the bottom along the path. A line drawn perpendicular to the current anywhere along area B was crossed by 75 to 100 animals/min for the first several hours of the study. Stationary current meters near the study site showed no measurable current (threshold 2.57 cm/s) at the time ofthe experiment. The maximum bottom current at the site at any time, measured with a remote meter, in February, March, and April, was 1.68 cm/s (Mangarella et al., 1979). A heightened state of activity occurred in the area designated C, an area extending z 1 m from the trap in directions perpendicular to the current, and for 2 m downcurrent of the trap. After a few hours of bait exposure, area C was occupied by a seething mass of amphipods sing quickly and randomly into and around the trap, up to a meter off the bottom. Animals began moving to the ban within 10 min of its placement. Within 1 h all bait pieces were totally covered by feeding amphipods, and within 6 h a mass of several thousand scavengers was moving about the trap. At this point fewer animals were being attracted, and from not as great distances as occurred initially. After apparent satiation, animals lay on their sides on the bottom, curled into a C-shape. Twenty-four h after the removal or consumption of bait most animals had dispersed. Divers observed more B. afinis in the general area for 48 to 72 h after the bait had been offered than were noted in dives prior to a trapping period.
DISCUSSION
Boeckosimris affmus is common in the North American Arctic, and has been taken with baited traps extensively in both Alaska (Busdosh & Atlas, 1975; Busdosh et al.,
1978) and Canada (Percy, 1975). The behavior of amphipods in the areas designated A in Fig. 1 was the normal, searching pattern exhibit&d by the species. As the behavior in area A is not affected by the baited traps, it will not be considered further. Crustaceans may detect food at a distance by vibration receptors, sight, or chemoreception (Iiindley, 1975). With a non-living ban it is unlikely that vibration is me~in~ul. Form vision is rudimentary, and visual cues play a minor role in feeding behavior (Bullock & Porridge, 1965; Fuzessery & Childress, 1975; Hindley, 1975). Dahl(l979) concluded chemosensory stimulation was the most likely agency by which amphipods were led to carrion on the deep sea bottom. Amphipods studied by Dahl belong to the family Lysianassidae, which contains many species that are scavengers. B. a~~j~ also belongs to this family, which is rno~ho~o~~y adapted for e&ient chemoreception of stimuli carried by water currents (Dahl 1977, 1979). Lindstedt (197 1, in press) has thoroughly reviewed a chemoreception literature that
CHEMORECEPTION
IN AN ARCTIC AMPHIPOD
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“is extremely scattered and has little unity of terminology or method.. .“. Investigators have generally agreed that amino acids are a stimulus to crustacean chemoreceptors, and that combinations are more successful than individual chemicals (Mackie & Shelton, 1972; Shelton & Mackie, 1972; Bardach, 1975; Fuzessery & Childress, 1975; McLeese, 1970). B: @innis has been attracted to traps baited with fish, roast beef, and canned sardines (in the present study), and with rotting whale meat, seal blubber, and fish (Busdosh & Atlas, 1975; Busdosh et al., 1978). Based on this field study and on evidence from the investigations cited, the following scenario seems to best explain the amphipods behavioral reaction to the bait. The animals in the long, thin triangle of area B (Fig. 1) received chemical stimuli from the bait. These stimuli were carried in the water passing over the animals, by the slow but constant current. These animals moved to the bait, and as these first arrivals fed the bait became shredded, which allowed more bait solution and created more food particles sufficiently small to be carried by the current. This activity of the first arrivals allowed a more concentrated signal to be sent out, a signal strong enough to attract animals in area B at increasing distances from the bait. Reference to Fig. 1 leaves little doubt the chemical stimuli were current-borne. No animals reacted to the bait in any area except downcurrent of the bait. These animals, those of area B, for B delineates the area of sufficient stimulus, then moved to the bait. One of two mechanisms would seem likely to account for this movement: (1) amphipods swim up a gradient of everincreasing strength; (2) amphipods orient and swim into the current after reception of stimulus. Hamner & Hamner (1977) demonstrated that a planktonic shrimp (Acetes sibogae austrulis) followed scent trails of sinking food. Upon encountering a scent, the animals descended along the food’s trail. However, when food was raised up through the water column, rather than allowed to sink, the shrimp still descended upon contact with the scent, moving along a decreasing gradient. They concluded that the shrimp do not follow a chemical gradient, but have evolved a pattern for feeding on falling material. Hindley’s work (1975) with a prawn (Penaeus merguiensis) led him to conclude that while the animals could locate food in still water, the mechanism was not very efficient. He concluded the prawn reacted to current after recognizing food, and that the chemical gradient was important only when near food. Castilla & Crisp (1973) reported a starfish was able to respond to a gradient between two streams of water, and followed the stream whose water contained the attractant. They pointed out that still water is necessary for a true gradient, and still water is an impossibility in the natural habitat of starfish. They conclude, “ . . .the only effective response of an animal to chemical stimulus in nature is to follow the scent upstream”. The preceding implies that B. afinis received a chemical stimulus, interpreted the signal as food, and swam upcurrent to the source. A slight but sudden change in current direction during the experiment proved fortuitous. Had amphipods continued to move into the current, now from a slightly different direction, they would not have found the bait. However, movement into the
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current did not continue: animals quickly went into a back-and-forth searching pattern until they again were in the scent plume. These observations indicate amphipods do not simply sense food one time and then swim upcurrent until they fmd it. The adjustments made by animals out of the scent plume do not establish that a chemical gradient is being followed, but do establish that loss of the attractant scent stops the movement into the current. It would seem that an exposure above some threshold level of the attractant is required to stimulate constant undirectional movement, and when this threshold is not attained, the searching behavior dominates. The apparent confusion in area C near the trap may be the result of, or the combination of, different factors. In the close proximity of the bait, an arrestant may be present. Lindstedt (197 1) defined such a substance as “a stimulus that causes an animal to cease locomotion when in close contact with an apparent source”. If so, the arrestant may be the source itself in this case. Thousands offeeding amphipods caused the water surrounding the trap to be a slurry of dissolved food and food particles. The density of this slurry may have been sufficient to be recognized as the source itself. Another possible cause for the movement was the lack of available surface area on the bait. Animals arriving after the first few hours found the surface of the bait completely covered by a tightly-packed mass of amphipods. Along with the demonstration that constant sensing of attractant is coupled with orientation into current, the present study points out that chemoreception works over long distances in real-world situations - animals 15 mm in length were drawn to a bait from a minimum of 30 m. Correlated with this long-ranging effect are the numbers of animals drawn, with an estimated 20000 amphipods attracted by 5 kg of bait. The question of where 20000 amphipods originated prior to moving to the bait can be speculated on only very tenuously. No thorough definition of the density of B. affl& in this area has been accomplished. Chin et al.‘s (1979) data indicated 15 animaIs/m2, based on five samples at each of only three stations. If such a density is valid, then triangle B would need to project a distance of 115 m from the bait to attract 20 000 animals. Several factors indicate that such a distance, in a real-world situation, is unnecessarily large. Consideration must be made that these animals are motile. Busdosh (1981) has shown, in laboratory experiments, that members of this species move on the average of 100 cm/mm, and spend more than half of the time moving during their active period. Busdosh et al. (1978) and Percy (1977) have both noted that this species divides its time between swimming and remaining burrowed, an alternation of activity that Percy (pers. comm.) suggests may be related to the tidal cycle. For our purposes we can assume that a specimen moves 100 cm/n& for one-half of its active time. If tide-related, whether ebb or flow, this active period would approximate 12 h. Manipulation of these estimates gives a potential movement of 360 m per day per animal. Such a figure, if within even an order of magnitude, underscores the importance of motility. A large number of animals in the normal activity of area A could move into area B,
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sense the bait, and move to it. There is essentially no return of animals to area A, as any individual entering area B will remain within its confmes, and move to the bait. This motility would allow a large number of animals near the trap, but initially not within area B, to become captured. Compoundiig this factor’s effect would be current shifts, which would bring stimulus to a different group of animals along a different axis to the trap, yet not lose all of the animals along the former axis, who, once stimulated, searched for the stimulus again. Although the shallow Beaufort Sea has several motile species, response to baited traps has been almost exclusively by B. ufjinis in water z 5 m depth, and by two other lyssianassid amphipods, Onisimus ( = Pseudalibrotus) gIacialis and 0. litoralis, in shallower waters. ~~~kos~~ a&i% is largely a d~tivore. Many hours of field observation by divers show the animals moving about the bottom, picking among sediment particles and debris. Detritus is perhaps the primary food source. Sufficient vertebrate carcasses may not be available to sustain large populations of amphipods, as whales and seals do not occur in the area during most of the year, and marine fish populations do not seem abundantly widespread throughout the zone. Working in the deep sea, Dayton & Hessler (1972) and Isaacs (1969) noted the presence of several species of large, motile scavengers that quickly find bait (s~ula~g carcasses), apparently by current-borne clues. Dayton & Hessler (1972) suggested these animals quickly break down large food parcels (carcasses) which fall to the ocean floor, resulting in greater availability of food (as small pieces or as feces) to other bottom dwellers. The Beaufort Sea off the coast of Alaska does not seem to have several species of large, highly motile scavengers; it does not seem to have any. This role has apparently been assumed by small ( w 15 mm) ~phipods, and then by only two or three species. The apparent lack of large, highly motile scavengers may indicate there are not sufficient carcasses to support a population. The amphipod Boeckosimus aflnis is a detritalfeeding, small, motile scavenger, with chemoreceptive capabilities to allow it to find and utilize the occasional rich protein source of a carcass. ACKNOWLEDGEMENTS
This study was performed under the sponsorship of the owner companies of the Prudhoe Bay Unit, and with the assistance of personnel from ARC0 Oil and Gas Company. Our thanks to ARCO’s Dr. .I. Lindstedt Siva who shared her experience and library on the subject, and who graciously reviewed the manuscript. We would like to thank Dr. R. W. Firth, Jr., for his help in the coordination of the project. Literature research was sponsored by the Professional Development Fund of Woodward-Clyde Consultants.
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