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Notice: © 1989 Marine Biological Association of the United Kingdom. This manuscript is an author version with the final publication available and may be cited as: Larson, R. J., Mills, C. E., & Harbison, G. R. (1989). In situ foraging and feeding behavior of narcomedusae (Cnidaria: Hydrozoa). Journal of the Marine Biological Association of the United Kingdom 69(4), 785-794. doi: 10.1017/S002531540003215X {yjO J. mar. bioI. Ass. U.K. (1989), 69, 785-794 785 Printed in Great Britain

IN SITU FORAGING AND FEEDING BEHAVIOUR OF NARCOMEDUSAE (CNIDARIA: HYDROZOA)

RONALD J. LARSON*, CLAUDIA E. MILLSt AND G. RICHARD HARBISON* 'Harbor Branch Oceanographic Institution, 5600 Old Dixie Highway, Fort Pierce, Florida 34946 USA tFriday Harbor Laboratories, University of Washington, 620 University Road, Friday Harbor, Washington 98250, USA

(Figure 1)

Narcomedusae are a small and mostly oceanic group of hydromedusae whose tentacle morphology and comportment sets them off behaviourally and perhaps ecologically from most other medusae. Their tentacles are relatively few in number (2-40), stiff, and non­ contractile, with points of insertion located well above the bell margin. Eleven species representing eight narcomedusan genera (Aegina, Aeginura,an undescribed aeginid, Cunina, Pegantha, Solmaris, Solmissus, and Solmundello) were observed and collected in situ in the NW Atlantic, Arctic and Antarctic, using scuba and manned submersibles. In life, the tentacles of narcomedusae are nearly always held upwards over the bell or projected laterally. The major prey were other gelatinous zooplankton, especially salps and doliolids. In the laboratory, these relatively large prey were caught on the tentacles which bend inward and coil at the tips to bring food to the mouth. By extending the tentacles perpendicular to the swimming path, these medusae achieve a relatively large encounter area, thus increasing the probability of contact with prey, for the amount of protein invested in tentacles.

INTRODUCTION

Narcomedusae are common oceanic hydromedusae that have been little studied because of their inaccessibility. Although there are only about 50 species, some of these are widely distributed (e.g. Aegina citrea Eschscholtz, Aeginura grimaldii Maas, Pegantha clara R.P. Bigelow, Cunina octonaria McCrady, Solmtssus incisa (Fewkes), Solmissus marshalli Agassiz & Mayer and Solmundeila biientaculaia (Quoy & Gaimard) (Kramp, 1961). For example,S. biteniaculata occurs in the Antarctic, tropics and boreal regions of the world oceans, and at shallow and great depths. Although most species are found above 1000 m, some species (e.g. Solmissus spp.) occur at greater depths [Hartman & Emery, 1956; Peres, 1958, 1959 (as 501maris)J. Narcomedusae are holoplanktonic medusae. In some species (e.g. Cunina peregrina, Pegantha triloba) the larvae are known to parasitize other medusae (Bouillon, 1987), whereas other species develop non-parasitically in the plankton. The morphology and histology of narcomedusae have been described by Vanhoffen (1908), Bigelow (1909), Russell (953), and others. They typically have a fragile lens- or dome-shaped umbrella a

786 RJ. LARSON, C.E. MILLSAND G.R. HARBISON

1-10em in diameter that is generally transparent, but may be pigmented in mesopelagic species (e.g. Aeginuragrimaldii). Narcomedusae have from 2 to 40 solid tentacles project­ ing from the bell margin. The non-extensile tentacles are equally spaced around the bell and may be equal in length to the bell radius or up to about twice as long as the bell diameter. Grooves extending downward from the tentacles allow each tentacle to bend inward across the lower portion of the bell, bringing attached prey into contact with the circular mouth. The stomach is flat and broad, covering most of the subumbrella surface and can accommodate large prey. The cnidome of narcomedusae has been described for only a few species. Where known, it consists exclusively of apotrichous isorhizas, which are sometimes most abundant on the upper (abaxial) side of the tentacles and can have an extremely long (9 mm) thread (Mackie & Mackie, 1963; Mills & Miller, 1984; Mills & Goy, 1988; Purcell & Mills, 1988). Because most of these medusae are oceanic, fragile, and transparent, they have rarely been observed alive in an undamaged state. Bigelow (909) noted that freshly netted specimens had tentacles that extended stiffly outwards. He also remarked that some species were powerful and active swimmers, while others were inactive owing to reduced swimming muscles. Gladfelter (973), who studied the locomotion of Solmissus marshalli, noted that the bell was divided into two zones, a rigid central disc and a flexible lateral wall. Upon contraction of the circular swimming muscle, the lateral wall bends inward and upward, providing propulsive thrust. Madin (988) described ten­ tacle postures of three narcomedusan genera observed by scuba diving or from sub­ mersibles. Mills & Goy (988) described very active swimming and extensive vertical migration of Solmissus albescens (Cegenbaur), as seen from a submersible. Narcomedusae can be abundant at mesopelagic depths. In fact, they were among the first mid water animals to be photographed in situ. Emery (952) and Hartman & Emery (956) photographed many Solmissus incisa off California using a remote 'benthograph' camera. One of their photographs shows five specimens swimming in various direc­ tions with the tentacles arched outwards (Hartman & Emery, 1956, plate 1, incorrectly identified as a trachyline medusa). Other photographs of narcomedusae have been taken by manned submersibles. Bernard (958), Peres 0958, 1959), Tregouboff (1959), Houot (960), and Laban et al. (963) observed and photographed several narcomedu­ san species in the Mediterranean and off Japan, as deep as 2000 rn, from the French bathyscaphe FNRS III. Most of their observations concerned vertical distributions but they did note that the tentacles of Solmissus albescens and Aegina citrea (incorrectly identified as Aeginopsis Iaureniii Brandy) are usually held stiffly outward or upward from the bell. Benovic (1973) and Mills & Goy (1988) have described the 300-600 m (50­ 144 m h') diel vertical migration of S. albescens in the southern Adriatic and Ligurian Sea in the Mediterranean. Mackie & Mackie (1963), at Friday Harbor, Washington, observed Solmissus marshalli, a weak swimmer that holds its tentacles either up over the bell or laterally from the sides. One specimen that was maintained in an aquarium, ingested a hydromedusa (Euphysa sp.). Mills observed a S. marshalli in situ at the same location feeding on Euphysa sp. FEEDING AND FORAGING IN NARCOMEDUSAE 787

Mills & Miller (1984) have described predation on Aegina citrea by the ctenophore Haeckelia rubra (Kolliker), In the same paper they report feeding by the narcomedusa Cunina sp. on H. rubra in the laboratory. Mills & Goy (988) reported in situ observations from the submersible Cyana of several Solmissus albescens in the Ligurian Sea with the pteropod Cavolinia sp. in their guts, and of one S. albescens capturing, but subsequently dropping, the ctenophore Bathocyroe sp. In this paper, we describe swimming and tentacle posture, feeding, and diet for representatives of eight genera of narcomedusae that have been observed, photo­ graphed, and collected using scuba and manned submersibles in the western North Atlantic Ocean and elsewhere. .. METHODS Some of the medusae were observed in situ and were collected with the aid of scuba equipment, using 'blue water' diving techniques (Madin et a1., 1986) during a series of scuba transects made on a trans-Atlantic cruise of the RV 'Alantis' I [cruise no. 101, June-July 1978: see Bidigare & Biggs (980) for cruise track]. Other medusae, were observed in the Antarctic (McMurdo Sound) in December 1987 and in the Arctic (between Iceland and Spitsbergen) during August 1988. For observations of feeding behaviour, medusae were collected individually in jars and were maintained in ship­ board aquaria at near sea-surface temperatures (see Table 1). Mesopelagic narcomedusae were observed, photographed, video recorded, and col­ lected using the manned submersibles 'Johnson-Sea-Link' I and II [equipment fully described by Youngbluth (1984)] during cruises off the Bahamas in October 1984 and October 1988, off New England in September 1986 and August 1987, and off the Dry Tortugas in August September 1987.

RESULTS In situ observations Representatives of eight narcomedusan genera (Aegina, Aeginura, an undescribed aeginid, Cunina, Pegantha, Solmaris, Solmissus, and Solmundella) were observed in situ and collected (Table 1). Narcomedusae in the sea were oriented in apparently random directions, but were usually swimming. Bell pulsation rates for epipelagic medusae were generally an inverse function of size, ranging from 0·08-0·17 Hz (pulsations per second) in relatively large (>30 mm bell diameter) sluggish species (Cunina duplicata and Cunina proboscidea), to 0·75-1·67 Hz in small medusae 00-20 mm bell diameter) (Aegina citrea and Solmaris corona). However, the small· epipelagic species, Cunina globosa, was relatively inactive, with pulsation rates of about 0·33-0·50 Hz. Pulsation rates of mesopelagic species ranged from 0·31-0·79 Hz for Solmissus spp. (bell diameter 30-60 mm) to 0·50-1·00 Hz for Aeginuragrimaldii (bell diameter 20-30mm) to 1·25 Hz for an undescribed aeginid (bell diameter 30 mm).

FEEDING ANO FORAGING IN NARCOMEOUSAE 789

tentacles. For example, in Aeginura grimaldii (Figure 1C), which has a small, dome­ shaped bell and eight short tentacles, swimming propelled the medusa about 1-2 bell diameters per pulsation; our observations yielded 45-85 em travelled in 30 seconds (1·5­ 2.8 em S1) by a 3 em diameterA. grimaldii. In Solmissus spp. (Figures 10, E), which have a broad, flat umbrella and more numerous (up to 40) and longer tentacles, swimming was much slower, with each pulsation propelling the medusa only a fraction of the bell diameter; our observations yielded 30-80 em travelled in 30 sec 0-2·7 em s') by a 7 em diameter S. marshallior S. incisa. Narcomedusae are able to change the intensity of the bell contractions, and thereby vary their swimming speed. Swimming narcomedusae held their tentacles in various positions (Figure 1); stiffly upwards over the bell at an angle of about 60-90° 'Solmariscorona, Solmundella bitentacu­ lata, large mesopelagic Aegina citrea,new aeginid); at 180° outwards (Aeginura grimaldii, small epipelagic Aegina citreat; laterally to the side and slightly arched tCunina globosa, Pegantha mariagon); of arched upwards and downwads (Cunina duplicata, Cunina proboscidea, Solmissus spp.). Solmissus albescensalso frequently swam with its tentacles held straight down (Mills & Goy, 1988). Escape behaviour was observed in Aeginura grimaldii that were apparently disturbed by the submersible, whereby the tentacles were held straight down during swimming, probably to reduce drag and to hasten escape. Tentacle postures do change, many of these narcomedusan species were capable of switching between one or more of these tentacle postures, although most seemed to maintain a single characteristic posture most of the time. Some narcomedusae were seen in situ containing ingested prey (Table 1). Epipelagic specimens of Aegina citrea, Pegantha ?laevis, and Cunina proboscidea, from the western Atlantic, contained partially-digested saIps, mostly Ihlea punctata (Forskal) and Thalia democratica (Forskal). One C. proboscidea medusa was collected with about 40 ingested T. democratica zooids in various stages of digestion. Doliolids were observed in the guts of Solmaris corolla and C. duplicata. One very large C. duplicata medusa 02 em bell diame­ ter) was observed with its stomach crammed with hundreds of doliolid zooids. Aegina citrea from the Arctic were observed with ingested ctenophores tBolinopsi« infundibulum and Mertensia ouumi. One s. corolla contained a single chaetognath. Unidentifed mate­ rial was noted in the stomachs of a number of species. In the Antarctic, several Solmundella bitentaculat« were seen feeding on the pteropod Limacina helicina (Phipps). Although many narcomedusae were seen from the submersible, those with visible prey in their gut were rare. Only one Solmissus incisa medusa collected at 670 m in the Bahamas contained pieces of comb rows from a partially digested ctenophore.

Shipboa I'd observations Even though the medusae were carefully collected, most specimens showed abnor­ mal behaviour in aquaria. A few medusae, primarily small ones, did extend their tentacles in their normal in situ postures; but others kept their tentacles curled below the umbrella or only partially extended. Laboratory feeding studies were conducted on the most normal-looking specimens. Because salps appeared to be the major prey of 790 R.J. LARSON, C.E. MILLS AND G.R. HARBISON

Table 1. Gut contents of narcomedusae collected in situ

Narcomedusa Gut contents Location Reference"

Aegina citrea salps N.W. Atlantic 4 Aegina citrea ctenophores Arctic 4 Aegina citrea hydromedusa N.E. Pacific 3 Clmina duplicata doliolids N.W. Atlantic 4 Cunina proboscidea salps & doliolids N.W. Atlantic 4

Pegantha ? laevis salps N.W. Atlantic 4 Solmaris corona doliolids & chaetognath N.W. Atlantic 4 Solmissus albescens pteropods Mediterranean 2 Solmissus incisa ctenophore Bahamas 4 Solmissus marshaIii hydrornedusa N.E. Pacific 1,2 Solmundella bitentaeulata pteropods Antarctic 4

"References: 1= Mackie & Mackie, 1963; 2= Mills & Goy, 1988; 3= Purcell & Mills, 1988; 4= this paper epipelagic narcomedusae, feeding experiments were done using the salps Ihlea punctaia, Pegea bicaudata (Quoy & Cairnard), and Thalia democratica as prey. The following medusae captured and ingested salps in the laboratory: Cunina duplicaia, C. globosa, C. proboscidea, and Pegantha clara. Prey capture and feeding behaviour were similar in all species. Prey contacting the tentacles were caught by discharge of cnidae. Although the salps attempted to escape, and some successfully did so, most were caught. The tentacle with captured prey then bent toward the' mouth, along the peronial groove. The distal one third of the tentacle became coiled, bringing the prey near the mouth. The umbrella margin adjacent to the tentacle also bent inward, causing the prey to contact the mouth. The normally flat mouth and inconspicuous lips then bulged and folded outward and after contacting the prey, began to creep over it, pulling it into the stomach presumably by means of cilia lining the lips and stomach. Ingestion of prey took 5-15 min depending on the relative sizes of predator and prey. During transfer of the prey from tentacle to mouth, swimming was inhibited. The thin­ walled stomach of narcomedusae is very elastic and can hold many relatively large prey, causing bulging of the stomach far below the bell margin. Once ingested, prey were moved to the perimeter of the stomach where digestion occurred. Digestion of small salps 00-20 mm long) took from 1-3 h.

DISCUSSION Narcomedusae appear to feed primarily on soft-bodied prey such as pelagic coelen­ terates, tunicates, and pteropods. Although epipelagic narcomedusae may feed exten­ sively on salps and doliolids. mesopelagic forms appear to eat mostly medusae, cteno­ phores, and pteropods; with few exceptions, pelagic tunicates are not abundant at mesopelagic depths. Net-collected specimens are very unlikely to contain prey because the stomach is easily voided during handling. In fact, often all that remained of net- FEEDING AND FORAGING IN NARCOMEDUSAE 791 caught midwater hydromedusae was a mesogleal disc - the tentacles, stomach and other structures having been abraded away. Purcell & Mills (1988) suggest that hydrozoans that have isorhiza cnidae and lack rhopalonemes are adapted for feeding on soft bodied prey. Narcomedusae possess only one type of cnida, apotrichous isorhizas (Purcell & Mills, 1988; Carre et al., in press). These cnidae have an extremely long thread that appears to be specialized for piercing and holding on to saIps, ctenophores, medusae and other thick, soft-bodied prey. Cnidae in hydrozoans that feed on crustaceans are often concentrated in batteries, but in narcomedusae the cnidae are more or less scattered over the abaxial surface of the tentacle (Purcell & Mills, 1988). Perhaps high concentrations of cnidae (i.e. battery structures) are not needed by narcomedusae because of the large area of contact between tentacle and the gelatinous prey. Narcomedusae forage by slowly swimming with tentacles held rigidly outstretched. Bigelow (1909) noted that some freshly netted medusae had their tentacles bent inward towards the mouth. This is not a normal posture, but was due to being captured; narcomedusae generally bend their tentacles inward towards the mouth when handled, even if gently collected by hand. The normal tentacle posture of narcomedusae is very similar to that described for another primarily oceanic group of medusae, the coronate scyphomedusae (Larson, 1979). Medusae in both of these groups have solid tentacles with a core of large, vacuolated, endodermal cells (the chordate cells of Bigelow, 1909) that are covered by a more or less developed muscular epidermis containing cnidocytes. Also, the tentacles in both groups have endodermaI, root-like extensions into the umbrellar mesoglea that may provide structural support. However, the tentacles of narcomedusae are neither as large, nor as muscular as those of some coronates such as Periphylla, which is in the same bell size range. Furthermore, the tentacles of narcomedusae have a core com­ posed of only a single row of disc-shaped cells (see Russell, 1953, text-fig. 314), whereas in coronates the endodermal core cells are more numerous and irregularly arranged. In another primarily mesopelagic group of hydromedusae, the trachymedusae, the solid and apparently non-contractile tentacles of some species are also held rigidly outwards. During '[ohnson-Sea-Link' dives we have observed Halitrephes raldioiac Vanhoffen with arched tentacles similar in posture to Solmissus spp.; Agiantlza digita!« (O.F. Muller) and Amphogona apicata Kramp hold their tentacles outwards at about 90= from the bell when they are not swimming. The tentacles of trachymedusae differ from those in narcomedusae in that they often are very numerous (up to 500 or more) and, in the Halicreatidae, they are divided into two distinct morphological zones (proximal and distal) (Russell, 1953; Hesthagen, 1971; unpublished observations). In narcomedusae, the posture of the tentacles appears to be at least partially a function of tentacle length. Genera that have short tentacles (e.g. Aeginura and Solmaris) c usually hold them over the bell or outwards at 90 , whereas taxa with longer tentacles (e.g. Cunina spp. and Solmissus spp.) tend to have an arched tentacle posture (Figure 1). In Aegina citrea, the tentacles are at first relatively short then become longer. In juve­ niles, the short tentacles are held out laterally (Figure 1), but later when the tentacles lengthen, they are held up over the bell. •

792 R.]. LARSON, C.E. MILLS AND G.R. HARBISON

The tentacles of narcomedusae are very different in posture and structure from the long and sometimes exceedingly thin, hollow, contractile, primary tentacles of antho­ medusae and leptomedusae. Mills (1981) stated that morphology and behaviour of medusae affect their feeding efficiency as well as influencing the size and kinds of prey captured. Many neritic anthomedusae and leptomedusae having numerous filiform tentacles feed on small copepods and otherrnicrocrustaceans, and on various invertebrate eggs and larvae (Larson, 1987; Purcell & Mills, 1988; Mills, 1988). Numerous filiform tentacles may be adaptive for feeding on small prey. On the other hand, narcomedusae and coronate scyphomedusae have shorter, non-contractile, relatively thick tentacles that seem to be specialized for capturing relatively large prey. Most non-narcomedusae have cnidae equally dispersed around the tentacle, but in narcornedusae the cnidae are mainly on the abaxial portion of the tentacle. This suggests that narcomedusae capture prey on the aboral surface of the tentacles as they slowly swim. Differences in tentacle morphology, however, do not fully explain the specialized feeding by narcornedusae because other medusae with different tentacle morphologies also feed on large soft-bodied prey. For example, some semaeostome scyphomedusae (e.g. Chrusaora, Cyanea, Pelagia, and Drvmonema) that feed extensively on gelatinous prey, have long, relatively thick, contractile tentacles (Larson, 1978). Additionally, some coastal and epipelagic pandeid anthornedusae and aequorid leptomedusae, hav­ ing very long and fine tentacles, also primarily eat gelatinous prey (Purcell & Mills, 1988). The laterally extended tentacles of narcomedusae may offer some trophic advantage to narcomedusae in the relatively depauperate oceanic environment. Gerritsen & Strick­ ler (1977), using encounter theory, predisted that encounter area was the most impor­ tant factor affecting the probability of predator/prey contact. Tentaculate predators can increase their encounter area by increasing the number and / or length of their tentacles. Yet, this would mean diverting carbon and nitrogen from reproduction to the growth and maintenance of muscular tentacles. Such a strategy might be disadvan­ tagous in oligotrophic oceanic waters. Perhaps narcomedusae tentacles have evolved as a compromise between the need to provide a maximum prey catching area and a low energy expenditure. If the encounter area (At) is equal to the projected area of the medusa, perpendicular to the direction of swimming, a medusa \...·ith trailing tentacles l would have an A[=JrRR (RR=bell radius), whereas the encounter area for a narcome­ dusa with laterally extended tentacles would be A/= mRR+Lr)l (Lr=tentacle length). Thus by having laterally extended tentacles only as long as the bell radius, the encoun­ ter area is increased fourfold. Because prey density in the open ocean is relatively low, narcomedusae increase the rate of encounter with prey by swimming. rather than pas­ sively drifting as many neritic medusae do. Also by swimming, they increase their rates of encounter with inactive prey. The short, stiff, laterally positioned tentacles of narcomedusae may represent a means of minimizing carbon cost while still maintaining a relatively large encounter radius, a strategy that would be advantageous in the open ocean where prey may be larger but less numerous than in neritic waters. FEEDING AND FORAGING IN NARCOMEDUSAE 793

We wish to thank all of our scientific colleagues and the JSL submersible pilots who helped collect narcomedusae. Research and ship support came from; 1) National Science Foundation (Biological Oceanography) grant nos. OCE-8400243, OCE-8516083 and OCE-8746136; 2) NOAA NURP (University of Connecticut); and 3) inhouse grants from Harbor Branch Oceanographic Institution. This paper is contribution no. 19 of the Direct Study of Mesopelagic Communities project and contribution no. 730 of the Harbor Branch Oceanographic Institution.

REFERENCES

Benovic, A., 1973. Diurnal vertical migration of Solmissus albescens (Hydromedusae) in the southern Adriatic. Marine Biology,18, 298-301. Bernard, F., 1958. Plancton et benthos observes durant trois plongees en bathyscaphe au large de Toulon. Annates de l'lnstitut Oceanographique, 35, 287-326. Bidigare, RR. & Biggs, nc, 1980. The role of sulfate exclusion in buoyancy maintenance by siphonophores and other oceanic gelatinous zooplankton. Comparative Biochemistry and Physiology, 66A, 467-471. Bigelow, H.B., 1909. Reports on the scientific results of the expedition to the eastern tropical Pacific, in charge of Alexander Agassiz, by the US Fish Commission Steamer "Albatross", from October 1904 to March 1905. Lt. Commander L.M. Garrett, USN., commanding. XVI. The Medusae. Memoirs of the Museum of ComparativeZoology of Haniard College, 37,1-243. Bouillon, J., 1987. Considerations sur Ie developpernent des Narcorneduses et sur leur position phylogenetique. Indo-Malayan Zoology, 4, 189-298. Carre, D., Carre, C & Mills, CE., in press. An ultrastructural study of the cnidocysts of narcorne­ dusae and a medusivorous ctenophore: distinctive new features and confirmation of kleptocnidism. Tissue and Cell. Emery, K.O., 1952. Submarine photography with the benthograph. Scientific Monthly, New York, 75,3-11. Gerritsen, J. & Strickler, J.R, 1977. Encounter probabilities and community structure in-zooplank­ ton: a mathematical model. [ournal of the Fisheries Research Board of Canada, 34, 73-82'­ Gladfelter, W.B., 1973. A comparative analysis of the locomotory systems of medusoid Cnidaria. Helgoliinder Wissenschaftliche Meeresuntersuchungfll, 25, 228-272. Hartman, O. & Emery, K.O., 1956. Bathypelagic coelenterates. Limnology and Oceanography, 1, 304-312. Hesthagen, I.H., 1971. On the biology of the bottom-dwelling trachymedusa Tesserogastria museu­ losa Beyer. Norioegian Journal of Zoology, 19,1-19. Houot. GS, 1960. Deep diving off Japan. National Geographic Magazine, 17, 138-150. Kramp, P.L., 1961. Synopsis of the medusae of the world. Journal of the Marine Biological Associa­ tion of the United Kingdom, 40, 1-469. Laban, A., Peres, J.-M. & Picard, J., ]963. La photographie sous-marine profonde et son exploita­ tion scientifique. Bulletin de l'Institut Oceanographique, no 1258, 32 pp. Larson, R.J., ] 978. Aspects of the Feeding and Functional Morphology of Scyphomedllsae. MS thesis, University of Puerto Rico. Larson, K}., ]979. Feeding in coronate medusae (Class Scyphozoa, Order Coronatae). Marine Behnuiour and PhYSiology, 6, 123-129. Larson, KJ., 1987. Trophic ecology of planktonic gelatinous predators in Saanich Inlet, British Columbia: diets and prey selection. Journalof Plankton Research, 9, 811-820. Mackie, G.O. & Mackie, G.V., 1963. Systematic and biological notes on living hydromedusae from Puget Sound. Bulletin. National Museulll of Canada, no. 199,63-84. Madin. L.P., 1988. Feeding behavior of tentaculate predators: in situ observations and a concep­ tual model. Bulletin of Marine Science, 43, 413-429. \tadin, L.P., Harbison, G.K & Rioux, T. 1986. Blue water diving equipment and procedures used at Woods Hole Oceanographic Institution. In Bille Water Dilling Guidelines (ed. J.N. Heine), ..,p.43-46. La Jolla: California Sea Grant Program, .,

794 RJ. LARSON, C.E. MILLS AND G.R HARBISON

Mills, CE., ]981. Diversity of swimming behaviors in hydromedusae as related to feeding and utilization of space. Marine Biology, 64, 185-189. Mills, CE., 1988. Species differences in diet and prey selection by hydromedusae. American Zoologist, 28, 192A. Mills, CE. & Goy, J., 1988.In situ observations of the behavior of mesopelagic Solmissus narcome­ dusae (Cnidaria. Hydrozoa). Bulletin of Marine Science, 43, 739-751. Mills, CE. & Miller, RL., 19841ngestion of a medusa (Aegina citrea) by the nematocyst-contain­ ing ctenophore Haeckelia rubra (formerly Euchlora rubra): phylogenetic implications. Marine Biology, 78,2]5-22]. Peres, J.-M., 1958. Remarques generales sur un ensemble de quinze plonges effectues avec Ie bathyscaphe F.N.RS. III. Annales de l'lnstitut Oceanographique, 35, 259-285. Peres, J.-M., 1959. Deux plongees au large du [apon avec Ie bathyscaphe francais F.N.RS. III. Bulletin de l'lnstiiui de Oceanographique, no. 1134,28 pp. Purcell, J.E., & Mills, CE., I988. The correlation between nematocyst types and diets in pelagic hydrozoa. In The Biology of Nematocysts (ed. D.A. Hessinger and H. Lenhoff), pp. 463-485. San Diego: Academic Press. Russell, FS., 1953. Medusae of the British Isles. Anihomedusae, Lepiomedusae, Limnomedusae, Tra­ chipnedusae, and Narcomedusae. London: Cambridge University Press. Tregouboff, G., I959.Prospection biologique sous-marine dans la region de Villefranche-sur-Mer en mars 1959. Bulletin de l'Institut Oceanographique, no. ] ]56, 18 pp. Vanhoffen. E., ]908. Die Narcomedusen. Deutsche Tieisee-Expedition 1898-1899, 19,42-74. Youngbluth, M.J., I984. Manned submersibles and sophisticated instrumentation: tools for oceano­ graphic research. In Proceedings of SUBTECH 1983 Symposium, pp. 335-344. London: Society of Underwater Technology.