PREDATOR-PREY RELATIONSHIP BETWEEN PACIFIC HERRING, CLUPEA HARENGUS PALLASI, LARVAE AND A PREDATORY HYPERIID AMPHIPOD, HYPEROCHE MEDUSARUM1

HEIN VON WESTERNHAGEN AND HARALD ROSENTHAL2

ABSTRACT

Predatory efficiency of Hyperoche medusarum (Hyperiida, Amphipoda) on yolk-sac larvae of Pacific herring, Clupea harengus pal/asi, was studied in the laboratory under continuous light conditions: 1,5, 10, and 50 herring larvae were exposed to 1,2,4,8, and 16 hyperiids in 500-ml beakers. It was found that the number of attacked larvae per unit time increased with rising predatory and/or prey density. Individual mean predation rate was found to decline with increasing predator as well as prey densities, prolonged exposure times, and the presence of alternative prey.

Aside from starvation (Sette 1943; Schnack 1972), medusarum and marine fish larvae, this study was one major cause of mortality in marine fish larvae initiated to shed some light on the predatory is assumed to be predation (Stevenson 1962), the efficiency of this amphipod. predators frequently being crustaceans, as de­ scribed by Garstang (1900), Lebour (1925), Davis MATERIAL AND METHODS (1959), Lillelund (1967), Rosenthal (1967), Kabata (1970), Lillelund and Lasker (1971), Theilacker and For prey, yolk-sac larvae (8.0-9.5 mm TL (total Lasker (1974), and others. The pelagic hyperiid length» of the Pacific herring incubated in the amphipod Hyperoche medusarum occurs com­ laboratory were used. Immature H. medusarum monly off the Oregon coast (Lorz and Pearcy 1975), (1.48-1.80 mm TL) which had aggregated beneath in Californian waters (Hurley 1956), in the North a light at night were caught with a pail and Atlantic (Shoemaker 1930; Bowman et al. 1963; separated from other plankton organisms with a Dunbar 1963), in the North Sea (Sars 1895; Evans large bore pipette. and Sheader 1972), and in New Zealand waters Experiments were performed in filtered (Hurley 1955). In British Columbia waters it occurs seawater in 500-ml beakers (salinity 28%0; tem­ commonly in the upper layers «30 m) of the water perature 9°C; constant light). The water surface of column (Bowman 1953), and in Departure Bay the beakers was covered with 300-p,m mesh size (Vancouver Island) its juveniles are frequently nylon gauze in order to keep the amphipods from found clinging to the exumbrellae of hydromedu­ breaking through the surface. Because Hyperoche sae (Westernhagen 1976). specimens in their natural habitat were occasion­ The cooccurrence of large numbers of juvenile ally found resting on the exumbrellae of medusae, H. medusarum with newly hatched larvae of the a strip of nylon gauze (50 x 20 mm) hanging from Pacific herring, Clupea harengus pallasi, was the surface cover provided attachment for the incidentally discovered in 1974 at the pier of the amphipods when needed. Pacific Biological Station, Departure Bay. Field Different numbers of herring larvae 1,5, 10, and observations indicated that Hyperoche juveniles 50 were exposed to 1, 2, 4, 8, and 16 hyperiids for preyed on herring larvae and occasionally on other three exposure periods (2, 4, and 8 h). The number fish larvae. Since this was the first record on a of replicates for all predator/prey ratios were 4, 6, possible predator-prey relationship between H. and 5 for the 2-, 4-, and S-h exposure periods. Some additional experiments with 6- and 10-h exposure periods were used for the computation of a mean lThis study was sponsored by the international bureau of the Gesellschaft fUr Kernenergieverwertung in Schiffbau and attack rate on the basis of 111 h of observation. Schiffahrt in connection with the German-Canadian agreement Eleven trials using 25 herring and 25 flatfish on scientific and technical cooperation. larvae with 16 amphipods were also conducted. 2Biologische Anstalt Helgoland (~entrale, 2 Hamburg 50, Palmaille 9, Germany (Federal Republic of Germany)). One additional control vessel (50 herring larvae, no

Manuscript accepted February 1976. FISHERY BULLETIN: VOL. 74, NO.3, 1976. 669 FISHERY BULLETIN: VOL. 74. NO.3 amphipods) was used for each exposure period. Predatory Efficiency of Mortality of larvae was measured every 2, 4, and 8 Hyperoche medusarum h by means of direct counts. All remaining larvae were removed, and healthy, wounded, and dead The results of all experiments were summarized larvae were counted. The original number of and presented as the number of larvae attacked herring larvae then was restored before a new per hour at different predator and prey densities experiment was started. Between experiments, (Figure 1). The number of wounded and killed the hyperiids were provided with food in order to larvae was dependent on two factors, the density reduce cannibalism. of the herring larvae and the density of hyperiids. With increasing numbers (predator or prey) larval RESULTS mortality per hour increased, reaching a value. of more than two larvae killed or wounded per hour at Swimming and Feeding Behavior of the 16 Hyperoche and 50 herring larvae Hyperoche medusarum combination. The number of larvae attacked per unit time (1 Two modes of swimming were observed: 1) h) depended to a great extend on the duration of quick darting movements with the body kept in a the experiment (Figure 2). Experiments with horizontal position; and 2) slow hovering, in which short exposure times (2 h) yielded for all larvae the body was held in a vertical position, and the and hyperiid combinations higher attack rates per pleopods beat continuously. The latter mode of hour than experiments lasting 4 or 8 h. The mean swimming was maintained for periods longer than predatory efficiency of the hyperiids was affected 20 min, but the speed of swimming was slow also by their density in each beaker. The number (about 10 em/min). It was only during swimming of larvae attacked per unit time decreased as the that Hyperoche would, by chance encounter, cap­ density of the predators increased (Figure 3). It is ture a herring larva. The amphipod usually for this reason that there are different values for grasped the tail but attacks at the head and the the number of herring larvae attacked per hour by midportion of the larva also occurred. An attacked one hyperiid (Figure 4), (A) for the observation of larva did not survive long. The larva attempted to one single hyperiid, and (B) for the calculated shake the amphipod off for a few minutes, then mean predation rate of a hyperiid from exper­ sank to the bottom where it was eaten by the iments with 1, 2, 4, 8, and 16 Hyperoche. Yet both Hyperoche. Larvae were not always consumed. curves show that an increase of a potential prey in Frequently, amphipods clung to a larva for only a a constant environment beyond a certain density few seconds but the wound inflicted during this process inevitably lead to the death of the larva. " Wounded larvae which were removed after ter­ -r----'------.-.--.--,----:o.-.-'- . 2.0 mination of the experiment never survived for more than 4-5 h when kept in separate beakers. .- ",,~ . 1.5 Between swimming activities, the amphipods 2.0 .- either remained on the bottom (probably an ar­ ",;' tifact due to the small size of the beakers-in large - 1.0 enough containers Hyperoche juveniles swam 1.5 continuously (Westernhagen 1976», or attached 0.5 themselves with the posterior pereiopods to the nylon gauze provided in the beakers for this 0.1 purpose and assumed a resting posture. This '16 posture has been described for Hyperia galba by Bowman et al. (1963) and for Hyperoche medusar­ um by Evans and Sheader (1972). The latter 0.1 authors defined the posture as an "inactive curled 01 5 10 position head and urus directed away from the substrate it (the animal) sits on:' Larvae that FIGURE I.-Predatory efficiency of Hyperoche medusarum on yolk-sac larvae of Clupea harengus pallasi at different predator bumped into resting amphipods were not pursued and prey densities. Water temperature: 9°C; total observation or captured. time: 111 h; observation periods: 20.

670 WESTERN HAGEN and ROSENTHAL: PREDATOR-PREY RELATIONSHIP

.r------r 5.0 llarva /500 ml ["4.0 51ar vae / 500 ml 4.0 3.0 3.0 .c "­ "0 ~ 5.0 2.0 5.0 2.0 E c 4.0 1.0 4.0 !?'" .2 3.0 ~~~o --~~------~ 30 g' 2 t j 2.0 2.0 ~ 1> I ~ 1.0 ~ E :J Z '7' /' a 8 a 1 2 4 8 16 8 16

,.,,------,5.0 ,-1------,5.0

10 Iarvae/500ml 4.n 50 larvae / 500 ml 4.0 ~ 3.0 t3.0 ~ 5.0 2.0 5.0 2.0 g ~ ~ 4.0 0_ ---"",0_0 . ~/ 1.0 4.0 1.0

L 3.0 ! 30 lL17 ---;iL------!-- 2.0 !::ff;:?7't-'~':L-o, ,#" 1.0 :J z a -t<-1=t'--j<----/'------1"8 a 1 2 4 8 16 2 4 8 16 Number of Hyperache/500ml Number of Hyperache/500ml

FIGURE 2.-Mean number of yolk-sac larvae of Clupea harengus pal/asi attacked by Hyperoche medusarum after different exposure times. Water temperature goe.

does not necessarily lead to a corresponding in­ larval and hyperiid density. Increase in larval as crease in predation. At herring larvae densities of well as predator density lead to increasing attack 5/500 ml and 10/500 ml, one individual hyperiid rates per hour. Because searching and contacting attacked 0.1 larvae/h and 0.16 larvae/h, respec­ are random, this response was expected and has tively. At 50 larvae/500 ml the attack rate was 0.45 been described by Murdoch (1971) for predator­ larvae/h. Assuming a linear increase in attack prey interaction. That relatively more larvae are rate, we would have expected rates of 1.0 and 0.8 attacked per hour during short exposure periods larvae/h. than during long ones (Figure 2) can be partially Alterations in predation rates of Hyperoche explained by a rapid thinning out effect on prey in were obtained when heterogenous prey was confined containers, a problem discussed by Mur­ offered (25 herring larvae + 25 flatfish larvae), and doch (1969) for the predation of Thais and Figure 3 shows that predation on larvae was Acanthina on Mytilus and Balanus. These data remarkably reduced. Of the 0.07 larvae attacked suggest that short observation periods are prefer­ per hour by one hyperiid, 0.055 (78%) were herring able in experiments of this type, a point larvae and 0.015 (22%) flatfish larvae, thereby frequently neglected in experiments with expo­ showing a pronounced preference for herring. sure times of 20 and more hours (Lillelund 1967; Lillelund and Lasker 1971; Theilacker and Lasker DISCUSSION 1974; Ambler and Frost 1974), leading to an under­ estimate of the actual possible predation rate. Figure 1 shows a clear, direct relationship An additional factor may be the degree of satia­ between number of attacked larvae and both tion, which could be shown for invertebrates to

671 FISHERY BULLETIN: VOL. 74, NO.3

0.5

A 0.4 .-. 1 larva 1500ml 0-0 5 larvael 500ml 10 larvael 500ml .c A-A 50 larvael 500ml " 0.3 Q! 50 larvae (mixed) ~ • g 'tJ Q! .Y. Uc 15 0.2 '0 @ .D E ::> .\\.. A __A _ z 01 10 50 Number of herring larvae I 500 ml 0.1 0\ .

FIGURE 4.-Mean number of yolk-sac larvae of Clupea harenguH /':~._---: pallasi attacked per hour by one Hyperoche at different larval \i 0 _ densities: A. data of actual experiments with single hyperiids; ~~.~/_r"--...-=~.~====~.======-!~­ B. data obtained from mean values for experiments with 1,2,4,8, o -! and 16 hyperiids/500 m!. o 1 2 I. 8 16 Number of Hyperoche/500ml The number of herring larvae attacked did not FIGURE 3. - Mean number of yolk-sac larvae of Clupea harenguH increase proportionally with an increase of her­ pallasi attacked by Hyperoche medusarum during I-h exposure time in an experimental volume of 500 ml at different larval ring larvae available for the predators (Figure 4). concentrations. Water temperature goe. the "mixed" trial was This phenomenon has been termed "functional provided with 25 herring and 25 flatfish larvae (II replicates, 64 h total observation time). response" (type 2 response) by Holling (1966), and is believed to occur commonly in preying inverte­ reduce the rate of predation (Holling 1966; Brandl brates. Similar responses are displayed by the and Fernando 1974). house cricket, Acheta domesticus (Pimentel and Itbecame evident through the experiments that Cranston 1960); Podiscus maculiventris (Morris predation rate was also influenced by the number 1963); Acanthina sp. (Murdock 1969); Tortanus of predators present in an experimental beaker discaudatus (Ambler and Frost 1974); and Eu­ (Figure 3). Calculated mean individual predation phausia pacifica (Theilacker and Lasker 1974). In rates in experiments using 50, 10, and 5 larvae a typical functional response curve, the number of decreased as the number of hyperiids in one prey eaten or attacked per predator increases to container increased. Lillelund (1967) observed the reach or approach a maximum at an asymptote same phenomenon in his experiment using cy­ (Murdoch 1971). Although the curves in Figure 4 do clopids preying on larvae of Osmerus eperlanus, not yet approach an asymptote due to insufficient and Salt (1967) noted the same trend in exper­ prey density, the trend towards a maximum at­ iments using the predatory protozoan Woodruffia tacking rate at a given prey density is noticeable. metabolica preying on Paramecium. We con­ Hyperoche medusarurn exposed to two species sider this phenomenon an artifact caused by more of fish larvae clearly discriminated disproportion­ than one predator feeding on the same prey, an ately between these two. In Figure 3, the total event frequently observed at higher predator number of larvae attacked in trials providing densities. This is unlikely to occur in the natural alternate prey at equal densities is given as 0.7 habitat, because a herring larva once killed by its individuals/h. Of these, 0.055 were herring larvae predator which is still attached to it would sink and 0.015 flatfish larvae. Discrimination between down to the bottom out of the reach of the other two prey species, which is likely to occur only in Hyperoche. predators with searching and food selection

672 WESTERNHAGEN and ROSENTHAL: PREDATOR-PREY RELATIONSHIP behavior (Murdoch and Marks 1973), might be copepod, Tortanlls disculldatlls. Limnol. Oceanogr. either caused by different distribution of prey 19:446-451. BOWMAN, T. E. species (Oaten and Murdoch 1975), differences in 1953. The systematics and distribution of pelagic am­ palatibility (Holling 1965), avoidance behavior of phipods of the families Vibiliidae, Paraphronimidae, the prey, or conditioning and/or training of the Hyperiidae, Dairellidae, and Pbrosinnidae from tbe predator (Murdoch 1969; Oaten and Murdoch 1975) northeastern Pacific. Ph.D. Thesis, Univ. California, Los in cases of weak preferences. Ang., 430 p. BOWMAN, T. E., C. D. MEYERS, AND S. D. HICKS. Although generally H. medusarum was con­ 1963. Notes on associations between hyperiid amphipods sidered to lead a parasitic life on medusae (Sars and medusae in Chesapeake and Narragansett Bays and 1895) such as Cyanea capillata (Bowman et al. the Niantic River. Chesapeake Sci. 4:141-146. 1963) or Pleurobrachia pileus (Evans and Sheader BRANDL, Z., AND C. H. F~;RNANDO. 1974. Feeding of the copepod Acantlwcyc!ops 1Iernalis on 1972), the results of our experiments show that the cladoceren Ceriodaphnia reticlliata under laboratory even in the presence of alternate prey this am­ conditions. Can. J. Zool. 52:99-105.

phipod displays considerable predation on herring DAVIS, C. C. larvae. 1959. Damage to fish fry by cyclopoid copepods. Ohio J. Sci. Unlike another carnivorous hyperiid, Para­ 59:101-102. themisto gaudichaudi, which hunts moving plank­ DUNBAR, M. J. 1963. Amphipoda. Sub-order: Hyperiidea Family: Hyper­ ton visually (Sheader and Evans 1975), H. medu­ iidae. Cons. Perm. Int. Explor. Mer, Fiches Identification sarum depends on random encounters with its Zooplankton 103:2-4. prey. Many carnivorous copepods display the same DZIUBAN, N. A. behavior (Dziuban 1937; Fryer 1957; Lillelund 1937. On the nutrition of some Cyc!opidae (Crustacea). C.R. 1967; Rosenthal 1972; Brandl and Fernando 1974; (DokJ.) Akad. Sci. URSS, Nour. Ser. 17:319-322. Ambler and Frost 1974). This mode of hunting EVANS, F., AND M. SHEADER. requires a relatively high density of prey in­ 1972. Host species of the hyperiid amphipod Hyperoche medusarum (Kr~yer) in the North Sea. Crustaceana dividuals which at times is provided by the enor­ (Suppl.) 3:275-276. mous numbers of newly hatched herring larvae. FRYER,G. During this investigation, herring larvae density 1957. The feeding mechanism of some freshwater cyclopoid during the day at the water surface was copepods. Proc. Zoo!. Soc. Lond. 129:1-25. 2 GARSTANG, W. frequently above 2 larvae/lOO cm (direct obser­ 1900. Preliminary experiments on the rearing of sea-fish vations). Simultaneous mass occurrences of H. larvae. J. Mar. Bio!. Assoc. U.K. 6:70-93. medusarum suggest that the amphipods could HOLLING, C. S. possibly contribute considerably to herring larvae 1965. The functional response of predators to prey density mortality, especially since conditioning to abun­ and its role in mimicry and population regulation. Mem. dant prey organisms is comprehensible as could be Entomol. Soc. Can. 45:1-60. 1966. The functional response of invertebrate predators to shown by Sheader and Evans (1975) for P. gaudi­ prey density. Mem. Entomol. Soc. Can. 48:1-86. chaudi and its feeding on fish larvae. In fact HURLEY, D. E. stomach-content analyses of H. medusarum cap­ 1955. Pelagic amphipods of the sub-order Hyperiidae in tured during this study period revealed that the New Zealand waters. I.-Systematics. Trans. R. Soc. N.Z. 83:119-194. amphipods had eaten considerable amounts of fish 1956. Bathypelagic and other Hyperiidae from Californian larvae (Westernhagen 1976). waters. Allan Hancock Found., Occas. Pap. 18,25 p.

KABATA, Z. ACKNOWLEDGMENTS 1970. Crustacea as enemies of fishes. In S. F. Snieszko and H. A. Axelrod (editors), Diseases of fishes. Vol. I, p. We are indebted to D. F. Alderdice for providing 128-133. T.F.H. Publ. Inc., Jersey City, N.J. LEBOUR, M. V. laboratory space, to J. Klinckmann and G. Fiir­ 1925. Young anglers in captivity and some of their en­ stenberg for expert technical assistance and to M. emies. A study in a plunger jar. J. Mar. BioI. Assoc. U.K. Blake for advice on the preparation of the 13:721-734. manuscript. LILLELUND, K. 1967. Experimentelle Untersuchungen tiber den Einfluss carnivorer Cyclopiden auf die Sterblichkeit der Fisch­ LITERATURE CITED brut. Z. Fisch. Hilfswiss. 15:29-43. LILLELUND, K., AND R. LASKER. AMBLER, J. W., AND B. W. FROST. 1971. Laboratory studies of predation by marine copepods 1974. The feeding behavior of a predatory planktonic on fish larvae. Fish. Bull., U.S. 69:655-667.

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LoRZ, H. V., AND W. G. PEARCY. SARS, G. O. 1975. Distribution of hyperiid amphipods off the Oregon 1895. An account of the crustacea of Norway. Vol. 1. coast. J. Fish. Res. Board Can. 32:1442-1447. Amphipoda. Alb. Cammermeyers Forlag, Copenh., MORRIS, R. F. 711 p. 1963. The effect of predator age and prey defense on the SCHNACK,D. functional response of Podisus maculiventris Say to the 1972. Nahrungsokologische Untersuchungen an Herings­ density of Hyphantria cunea Drury. Can. Entomol. larven. Ber. Dtsch. wiss. Komm. Meeresforsch. 22:273­ 95:1009-1020. 343. MURDOCH, W. W. SETTE, O. E. 1969. Switching in general predators: experiments on 1943. Biology of the Atlantic mackerel (Scomber scombrus) predator specificity and stability of prey populations. of North America. Part I: Early life history, including the Ecol. Monogr. 39:335-354. growth, drift, and mortality of the egg and larval popula­ 1971. The developmental response of predators to changes tions. U.S. Fish Wildl. Serv., Fish. Bull. 50:149-237. in prey density. Ecology 52:132-137. SHEADER, M., AND F. EVANS. MURDOCH, W. W.,ANDJ. R. MARKS. 1975. Feeding and gut structure of Parathemisto gaudi­ 1973. Predation by coccinellid beetles: Experiments on chaudi (Guerin) (Amphipoda, Hyperiidea). J. Mar. BioI. switching. Ecology 54:160-167. Assoc. U.K. 55:641-656. OATEN, A., AND W. W. MURDOCH. SHOEMAKER, C. R. 1975. Switching, functional response, and stability in 1930. The amphipoda of the Cheticamp expedition of predator-prey systems. Am. Nat. 109:299-318. 1971. Contrib. Can. BioI. Fish. 5:221-359. PIMENTEL, D., AND F. CRANSTON. STEVENSON, J. C. 1960. The house cricket, ACheta dmnesticus, and the house 1962. Distribution and survival of herring larvae (Clupea fly, Musca domestica, as a model predator-prey system. J. pal/asi Valenciennes) in British Columbia waters. J. Fish. Econ. Entomol. 53:171-172. Res. Board Can. 19:735-810. ROSENTHAL, H. THEILACKER, G. H., AND R. LASKER. 1967. Parasites in larvae of the herring (Clupea harengus 1974. Laboratory studies of predation by euphausiid L.) fed with wild plankton. Mar. BioI. (Berl.) 1:10-15. shrimps on fish larvae. In J. H. S. Blaxter (editor), The 1972. Uber die Geschwindigkeit der Sprungbewegungen bei early life history of fish, p. 287-299. Springer-Verlag, Cyclops strenuus (Copepoda). Int. Rev. Gesamten Hy­ Berl. drobiol. 57:157-167. WESTERNHAGEN, H. VON. SALT,G. W. 1976. Some aspects of the biology of the hyperiid amphipod 1967. Predation in an experimental protozoan population Hyperoche medasarum. HelgoUinder wiss. Meeresunters. (Woodruffia-Paramecium). Ecol. Monogr. 37:113-144. 28:43-50.

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