In Situ Observations of the Behavior of Mesopelagic <I>Solmissus</I> Narcomedusae (Cnidaria, Hydrozoa)

BULLETINOF MARINESCIENCE,43(3): 739-751, 1988

IN SITU OBSERVATIONS OF THE BEHAVIOR OF MESOPELAGIC SOLMISSUS NARCOMEDUSAE (CNIDARIA, HYDROZOA)

Claudia E. Mills and Jacqueline Goy

ABSTRACT Solmissus albescens is the most numerous medusa in the mesopelagie western Mediter- ranean, This endemic species undergoes a nocturnal vertical migration from a depth of 400- 700 m to the upper 100 m. In situ observations of S. albescens reported here were made during 10 dives using the French submersible CYANAin 1985-1986 in conjunction with simultaneous conventional plankton sampling, and are combined here with published observations by earlier French submersible users for completeness. The hundreds of 2-5 cm diameter S. albescens seen from the CYANAwere almost always actively swimming regardless of time of day, with pulsation frequencies between 1.3 and 2.0 Hz. Swimming becomes directional at dawn and at dusk and the speed of upward and downward migrations appears

to be the same, approximately 100 m· h -1 as estimated from in situ point observations and from population depth distributions at different times onate afternoon, evening, and morning. Vertical migration appears to be conducted solely by swimming without need for changes in buoyancy. S. albescens can hold its non-extensible tentacles directly above its bell, curved laterally outward, or directed downward. Unlike many other hydro medusae, S. albescens swims and feeds simultaneously. Although all net-collected Solmissus had empty guts both during the day and at night, from the submersible we saw S. albescens feeding on non- migratory epipelagic Cavolinia pteropods at night. One S. albescens during the day was seen capturing a lobate ctenophore, but all other daytime observations indicated empty guts. Solmissus and other narcomedusae may be limited to feeding on soft-bodied prey by the type of nematocysts on their tentacles (apotrichous isorhizas). S. marshalli has also been observed in situ, from the SEALINK II and PISCESIV submersibles. In comparison to S. albescens, this cosmopolitan mesopelagic species has slower swimming speed (0.6-0.7 Hz), frequent periods of quiescence, and no long-range diel migrations.

The activities of medusae in plankton communities received little attention before the advent of submersibles and deep water cameras. In situ submersible observations have revealed the numbers and omnipresence of gelatinous organisms in deep water plankton (Peres 1958a, 1959; Tregouboff, 1961; Mackie and Mills, 1983; Mackie, 1985). The large size of most gelatinous zooplankton makes them prime objects for study using these techniques. In pioneering bathypelagic camera studies of the early 1950's, Hartman and Emery (1956) found medusae to be among the most abundant and recognizable deep water forms. We discuss some meso- and bathypelagic narcomedusae, similar to those figured by Hartman and Emery (1956; plates 1, 2, misidentified as trachyline Trachymedusae). In December 1985 and April 1986, we participated in a series of 10 dives using the French submersible CYANA to observe distribution and behavior of macroplankton in the Ligurian Sea area of the Mediterranean Sea. During these dives the narcomedusa Solmissus albeseens was among the most abundant midwater invertebrate species observable from the submersible. We saw over 500 of these narcomedusae in the 10dives, with local abundances as great as l·m-3• S. albeseens was described as having an extensive (over 300 m) diel vertical migration in the Adriatic Sea by Benovic (1973), who was able to determine this while taking vertical plankton hauls with an open net. Little more is known about the biology of this long distance migrator, so we present here our in situ observations of S.

739 740 BULLETINOFMARINESCIENCE,VOL.43, NO.3,1988

albescens, which, combined with those of earlier Mediterranean submersible div- ers (1954-1961), provide a fairly detailed picture of the behavioral biology of this medusa. The findings about S. albescens are compared with our less extensive in situ observations of its congener, S. marshalli, in subtropical Atlantic and temperate Pacific waters, as well as with some other mesopelagic medusae. Narcomedusae have been assumed to be a group of relatively inactive hydromedusae (the name of this Order is derived from the Greek narke meaning numbness, stupor, torpor). In situ observations from the submersibles CYANA, JOHNSONSEALINKII and PISCESIV indicate that the Narcomedusae are no less active as a group than other hydromedusae, and that, in fact, the Mediterranean narcomedusa S. albescens demonstrates nearly continuous swimming activity, making it among the more active of over 100 species of hydro medusae that have been observed in situ (Mills, unpub1.).

MATERIALSANDMETHODS

New data on the medusa S. albeseens reported here come from the French "Premigragel" and "Migragel I" campaigns, whose purpose was to study distribution and migration of gelatinous zooplankton in the Ligurean Sea region of the Mediterranean Sea using the submersible CYANA.All submersible dives occurred off the southeastern coast of France on a transect from the mouth of the Bay of Villefranche (east of Nice) toward Calvi, Corsica, Approximately 500 S. albeseens were seen during 10 dives totalling about 50 h of underwater observation. The "Premigragel" campaign consisted of two daytime dives on 17 and 18 December 1985, at 8 and 12 miles off the mouth of the Bay of Villefranche. On both dives, the submersible descended all the way to the bottom, to 1,590 and 2,080 m, respectively. The "Migragel I" dive series consisted of eight more dives between 22 and 27 April 1986 including four day dives and four night dives made at 3, 6, 13, and 23 miles offshore on the transect (moving toward Calvi) to depths of 420-1,300 m over bottom depths of 900-2,200 m, All of the water column examined in each dive was given approximately equal viewing time. Whereas this paper deals primarily with the behavior of S. albeseens, a quantitative report of the distribution of all major macroplankters including S. albescens will be presented elsewhere [PoLaval et al. (Station Zoologique), submitted']. Although full moon occurred during the week of diving (April 26), it was overcast every night. The CYANAcarried two pilots and one scientist on each dive, A metal quadrat marked at 5-cm intervals for scale was mounted outside of the observer's port. An immovable exterior video camera continuously recorded objects passing through this quadrat, although the depth of field and general resolution was insufficient for many purposes. The audio track of this videotape recorded comments by the observer and pilots inside the submersible and was often of more value in later reassembling the plankton community than was the videotape. Comparisons of the behavior of S. albeseens with that of S. marshalli and the coronate seypho- medusae Periphylla periphylla and Atalla spp. rely on in situ and videotaped observations made during 63 dives in the submersible JOHNSONSEALINKII to 720 m in the Bahamas, 16 October to 4 November 1984 and to 900 m off the Dry Tortugas, 26 August to 4 September 1987. In an additional 50 dives (1980-1983) in the submersible PISCESIV in fjords and inlets in British Columbia, Canada (Mackie and Mills, 1983 and unpubI.) the narcomedusa Aegina citrea was common and one S. marshalli was seen. Additional observations of upwelled but apparently healthy S. marshalli medusae were made from the docks of the Friday Harbor Laboratories. The JOHNSONSEALINKII and PISCESIV both carried two scientists and one pilot per dive: this duplication of scientific observers was invaluable in increasing the area searched and in allowing for discussion of observations as they occurred.

RESULTS Distribution. - The narcomedusa S. albescens is a common mesopelagic carnivore endemic to the Mediterranean Sea (Kramp, 1959). It is most abundant in the western portion of the Mediterranean and in the Adriatic Sea; it has also been collected in the eastern Mediterranean off Lebanon (Lakkis and Zeidane, 1985), but was not found off Egypt (Dowidar, 1981) or Israel (Schmidt, 1973). It occurs

] Laval, P., J. C. Braconnot, C. Carre, J. Goy, C. E. Mills and P. Morand. Small-scale distribution of macroplankton in the Ligurean Sea (Mediterranean) as observed from the manned submersible CY ANA. Submitted. MILLS AND GOY: BEHAVIOR OF MESOPELAGIC SOLMISSUS NARCOMEDUSAE 741

abc d e 9 h k I m n 0 p q r s t u v w x 0

~ QI 500 Cii 1 E + l: • J:. a. 1000 QI 0

1500 Figure 1. Summary of year-round daytime distribution (plotted in order left to right by day of the year) of Solmissus alhescens in the Mediterranean Sea based on 24 dives (a-x) using the submersibles FNRS III (1955-1961) and CYANA (1985-1986); dives in which fewerthan two S. albescens were seen have been omitted. Vertical lines indicate continuous observations from the submersible windows. Each line terminates at the lowest depth searched on that dive; arrowheads indicate that observations continued below 1,500 m. Solitary circles represent sightings of single individuals, overlapping circles indicate multiple individuals seen at that depth and are not strictly quantitative. Medusae in dives 0, r. s, t, u, and v were variously identified by observers as "Solmaris," "meduses," or "Solmissus or So/maris," but are all considered by us to have been S. albeseens. Dive date (bottom depth), time of dive, nearest town, and references are as follow: a, 1.18.61 (1,930 m), 1015-1530 Villefranche, Tre- gouboff(1962); b, 3.3.59 (1,180 m), 1040-1345, Villefranche, Tregouboff(1959); c, 3.6.59 (1,400 m), 0944-1355, Villefranche, Tregouboff(1959); d, 4.22.86 (1,000 m), 1100-1700, Villefranche, MI- GRAGEL I (unpubl.); e, 4.23.86 (2,350 m), 1045-1600, Villefranche, MIGRAGEL I (unpubl.); f, 4.24.86 (2,220 m), 0930-1445, Villefranche, MIGRAGEL I (unpubl.); g, 4.27.86 (1,300 m), 0930- 1330, Villefranche, MIGRAGEL I (unpub.); h, 5.3.57 (2,180 m), 0925-1620, Villefranche, Tregouboff (1958); i, 5.17.55 (550 m), daytime, Toulon, Peres and Picard (1955), Peres (1958a); j, 5.31.55 (2,120 m), 0900-1500, Toulon, Bernard (1955, 1957); k, 6.14.56 (800 m), 0955-1325, Villefranche, Tre- gouboff (I 956); t, 6.17.56 (1,280 m), 0940-1343, Villefranche, Tregouboff(1956); m, 6.17.55 (1,040 m 1000-1400, Toulon, Peres and Picard (1956), Peres (l958a); n, 6.23.55 (1,300 m), 1000-1400, Toulon, Peres and Picard (1956), Peres (I 958a); 0,7.7.55 (1,300 m), 0830-1515, Toulon, Furnestin (1955); p, 7.18.55 (1,350 m), 1000-1400, Toulon, peres and Picard (1956), peres (I 958a); q, 7.28.60 (2,200 m), 1018-1540, Villefranche, Tregouboff(l961); r, 8.21.57 (1,390 m), 0917-1305, Toulon, Peres (l958b); s, 9.10.57 (2,150 m), 0803-?, Toulon, Bernard (1957); t, 9.18.57 (2,290 m), 0637-?, Toulon, Bernard (1957); u, 10.18.57 (1,250 m), 0745-1400, Toulon, peres (I 958b); v, 10.24.57 (1,350 m), 0737-?, Toulon, Peres (l958b); w, 12.17.85 (1,590 m), 1015-1730, Villefranche, PREMIGRAGEL (unpub.) and x, 12.18.85 (2,080 m), 1113-1750, Villefranche, PREMIGRAGEL (unpub.).

year-round in the Ligurian Sea (Goy, 1971; 1972; 1974), where the present study was conducted. Its daytime distribution closely corresponds with the intermediate water layer (temperature about l3.5°C), although when the water column is well mixed in late autumn through spring, a few S. albeseens can also be found both in the upper strata (Goy, 1971) and in the deep Mediterranean bottom layers (Fig. 1). In general, S. albeseens may be replaced by the coronate scyphomedusa Peri- phylla periphylla in deep water (J. Goy and P. Laval observations in "Premigragel" dives, 1985). S. albeseens (up to 5 cm in diameter) is mesopelagic by day throughout the year, forming a more or less continuous layer that is usually about 100-200 m thick, occurring somewhere between 400 and 700 m (Fig. 1), regardless of the degree of stratification of the water column (see Goy, 1987). It migrates as a population into the upper water layers at night; its daytime depth distribution is probably light-dependent. S. albeseens may be found at the surface in the daytime from December through April, especially after strong winds, and it is occasionally 742 BULLETIN OF MARINE SCIENCE, VOL 43, NO.3, 1988

carried to the surface by upwelling as late as June. The consistent mesopelagic distribution observed from submersibles (Fig. 1) may indicate that the population is readily able to resume its deep habitat after mixing ofthe water column, perhaps on the next evening's downward migration. The unusually shallow population distribution on April 27, 1986 (Fig. Ig) is thought to be due to a decrease in light penetration caused by the occurrence of a heavy phytoplankton bloom in surface waters at that time [PoNival (Station Zoologique), in prep.]. In contrast to S. albeseens, S. marshalli is widely distributed in warm and temperate waters of the Atlantic, Pacific, and Indian Oceans (Kramp, 1968). Although it has most frequently been collected in open nets, S. marshalli appears to be eurybathic in distribution, occurring from surface to abyssal depths (Kramp, 1968). Population densities of this species are generally low, and there is no evidence to suggest whether or not it vertically migrates. Up to 40 S. marshalli were seen during 63 night dives in the Bahamas and off the Dry Tortugas in the JOHNSONSEALINKII; these specimens were all between 600 and 720 m deep, but other depths were not explored. Only one S. marshalli was seen during 50 PISCES IV dives in protected British Columbia waters; this specimen was 105 m deep, just above a bottom layer of virtually anoxic water. S. marshalli has also been observed from the floating docks of the Friday Harbor Laboratories from mid-February through mid-November, but it is regularly seen only from May through July (Mills, 1981a). At its most numerous, about 20-30 S. marshalli may be seen in an hour by a stationary observer at the nightlight (specimens are seen less frequently during the day). Most specimens are less than 8 cm in bell diameter. The water column in Friday Harbor is strongly mixed by tidal currents, so presence of this species at the surface is not indicative of its vertical distribution in less turbulent waters. In a series of over 600 stratified vertical plankton samples taken monthly or bimonthly 1978-1980 in nearby Saanich Inlet (Mills, 1982), only one S. marshalli was collected (in a 75-130 m sample just above poorly oxygenated bottom waters). S. marshalli in protected northeast Pacific waters may in fact be oceanic immigrants rather than a repro- ducing population. Vertical Migration and Swimming Behavior. -As first reported by Benovic (1973) based on open-net plankton hauls in the Adriatic Sea, we confirm the extensive upward die1vertical migration by S. albescens into the upper layers at night. The CYANAdives indicate that in April the migration seems to begin in the mid- afternoon, the population front having moved upward 100-150 m between 1400 and 1615 h on 22 April 1986 (Fig. 2e, f). The upward migration seems to be complete at about 2200 h, 8 hours later (Fig. 2j, k). Figures I and 2 are not meant to be strictly quantitative, but to indicate location of the Solmissus populations in the water column. Nearly all of the S. albeseens seen from submersibles, either during the day or at night, were actively swimming. Of 123 medusae whose activities were specif- ically mentioned by CYANAobservers, 98% were swimming. In situ observations and videotapes from the CYANAdives provided us with measurements of swimming rates of 49 medusae. The pulsation rates varied between 1.3 and 2.0 Hz (pulsations per second). Most species of hydromedusae show strong correlation between pulsation rate and size. The variability in pulsation rate of S. albeseens may also have been size-related, but diameter could not be measured from the submersible or in videotaped animals because distance from the observer or camera could not be determined (medusae were more or less in focus for almost a meter in depth over which their apparent diameter would vary). Estimations of the swimming speed of S. albescens were difficult to make either MILLS AND GOY: BEHAVIOR OF MESOPELAGIC SOLMISSUS NARCOMEDUSAE 743

a b c d e 9 h k 0

~ 2! Gl 200 E l:: .c ii 400 Gl C

600

Figure 2. Changes in depth distribution related to vertical migration of S. albeseens observed during vertical transects (a-k) from the submersible CvANA in April 1986. Vertical lines indicate continuous observations from the submersible windows. Each line terminates at the lowest depth searched on that dive; the arrowhead indicates that observations continued to 1300 m on that transect. Solitary circles represent sightings of single individuals, overlapping circles indicate multiple individuals seen at that depth and are not strictly quantitative. Dive date, mean time of transect, distance from shore, and dive number are as follows: a, 4.27.86, 1015,6 miles, D8; b, 4.24.86, 1230, 13 miles, D4; c, 4.24.86,1330, 13 miles, D4; d, 4.23.86,1400,23 miles, D2; e, 4.22.86,1400,3 miles, DI; f, 4.22.86, 1600,3 miles, DI; g, 4.24.86, 2030,13 miles, D5; h, 4.25.86, 2100,3 miles, D6; i, 4.23.86, 2130, 23 miles, D3; j, 4.26.86, 2200, 6 miles, D7; and k, 4.23.86, 0000, 23 miles, D3. in situ or from videotapes. In seven cases when the submersible was not moving, it was possible to measure distance travelled against the metal quadrat in front ofthe observer's porthole. This varied from 2.0-4.0 cm· sec-I, which converts to l 1.2-2.4 m·min-I or 72-144 m·h- , yielding an estimated time to migrate 500 m of between 3.5 and 6.9 h. There was no evidence of day/night differences in swimming rate. Estimates of the speed of migration can also be calculated from changes in the population distribution of S. albescens as illustrated in Figure 2. Transects eand foccurred on the ascent and descent, respectively, of CYAN A Dive 1, and were 2 h apart, at about 1400 and 1600. The upper boundary of the population moved up from 380 to 285 m during this period, or about 50 m· h-I. The lower population boundary was not established during Transect e. Transects i and k of Figure 2 occurred on the descent and ascent, respectively, of CYAN A Dive 3, 2.5 hours apart at about 2130 and midnight. The upper boundary of the population moved from 175 to 25 m and the lower front moved from 355 to 105 m, indicating swimming speeds of75 to 125 m·h-I. These values values of 50-125 m .h -I determined by the population distribution as observed intermittently from the submersible are similar to the 72-144 m·h-I estimated above by watching individual swimming medusae in situ. Differences between the two sets of values may be at least partially accounted for by size differences in medusae (small medusae pulsating faster and moving shorter distances per pulsation). Also, apparently migrating S. albescens were seen swimming in any orientation and direction, suggesting that the swimming path for any given animal in migration may be circuitous rather than straight, favoring the lower speed estimates taken from the population distribution. Even using a submersible, observations of vertical migration are usually indirect. It is not possible or practical to stay with the animals in question for long periods of time and still get believable results because the light will affect the behavior of most animals, and the inevitable turbulence caused by moving the sub will also affect the immediate environment of the animals under observation. 744 BULLETIN OF MARINE SCIENCE, VOL. 43, NO.3, 1988

a b

c d

Figure 3. (a, b, c) Sketches of Solmissus albescens showing the three postures commonly exhibited in situ. Swimming medusae may assume any of these tentacle postures, but it is assumed that feeding can be accomplished only in postures (a) and (c); posture (b) appears to be only locomotory. (d) In situ photograph of Solmissus marshalli (700 m, Bahamas) showing typical tentacle posture.

S. albeseens assumes three principal postures. It may hold its tentacles up above the bell at an angle of 900 or greater from the plane of the bell margin (the distal ends of the tentacles in this case are usually somewhat recurved outwards) (Fig. 3a), it may hold the tentacles out in approximately the body plane with each tentacle arching upwards in its midsection (Fig. 3c), or it may hold its tentacles downward at an angle of 900 from the bell margin, in which case the tentacles are usually perfectly straight (Fig. 3b). Although the significance of these 3 different postures is not understood, it appeared that the medusae moved more rapidly when their tentacles were held either up or down (the tentacles-down posture seemed to be the fastest), and that less distance was covered when they were swimming with their tentacles held outward. Speed of travel is not necessarily proportional to pulsation rate in hydromedusae; many species seem able to "shift gears" and cover varying distances without changing pulsation rate (Mills, unpub!.). The S. marshalli observed in the Atlantic and Pacific pulsated more slowly (0.6-0.7 Hz) and a lower percentage of the time observed than S. albeseens. S. marshalli may typically be either quiescent or slowly pulsating with tentacles arched outward slightly above the plane of the bell margin (Fig. 3d); the rapid swimming typical of S. albeseens, with tentacles held overhead, has not been seen in S. marshalli either in the Atlantic or during over ten years of dock observations at Friday Harbor (Mills, 1976-1987, unpub!.). Solmissus medusae are colorless and extremely transparent. They appear whit- ish from the submersible only because the lights are reflected from body surfaces. Both S. albeseens and S. marshalli bioluminesce when agitated. S. marshalli also has green-fluorescent patches on its umbrella, but no fluorescence is detectable in S. albeseens at about 500 nm using a compound microscope (Mills, unpub!.). Actual use of bioluminescence was never observed for either species of Solmissus and whether it is of value for feeding or defense is not known. MILLS AND GOY: BEHAVIOR OF MESOPELAGIC SOLMISSUS NARCOMEDUSAE 745

Feeding. -Feeding by S. albescens is assumed to take place during swimming since the S. albescens that we observed were swimming nearly all of the time. Observations of prey capture or ingestion by this species during the CYANAdives were limited to one medusa seen capturing a lobate ctenophore Bathocyroe? fosteri (which it subsequently dropped) at 510 m by day and about 10-20 Solmissus medusae that were observed with Cavolinia sp. pteropods or unidentified material in their guts during the night dives (2200-0030) between 25 and 50 m (night) or at 300 m (1030). All other S. albescens appeared to have empty stomachs. Observations of S. marshalli at the Friday Harbor Laboratories indicate that narcomedusae have only a tenuous grasp on ingested prey and that in most cases, handling a narcomedusa with prey in its gut will cause the prey to be dropped. The stomach muscle only weakly encloses prey, but deep water medusae presum- ably rarely meet turbulence during their lifetimes and the need for tightly sealing mouths may not occur. Such a process undoubtedly explains the fact that all of the several thousand S. albescens examined from net collections taken both during the day and at night the same month as the CYANAdives had empty guts (or their stomachs had been damaged by the net). One S. marshalli was seen in situ from the Friday Harbor docks with a Euphysa sp. hydromedusa in its stomach. Mackie and Mackie (1963) successfully fed S. marshalli pieces of crab muscle in the laboratory and they found that one S. marshalli ate a hydromedusa Euphysa flammea that had been placed in the same tank with it. Other known examples of narcomedusae feeding include the following: Mills (unpubl.) collected one S. incisa from the JOHNSONSEALINKII at 600 m off the Dry Tortugas that had a ctenophore in its gut, but most of the ctenophore was wafted out of the medusa's stomach by the sub's turbulence before the animal was collected. Mills and Miller (1984) inadvertently fed a ctenophore (Haeckelia rubra) to the narcomedusa Cunina sp. that had been placed in the same container. R. Larson (pers. comm.) reports five species ofnarcomedusae in the Atlantic Ocean feeding on salps and doliolids and one chaetognath. Nearly all of the nematocysts (stinging cells) on the tentacles of Solmissus spp. occur on the upper side of the tentacles (Fig. 4a), indicating that the prey are captured on this side of the tentacles. The tentacles are then swept downward and into the mouth where the prey is removed. Solmissus medusae have three sizes of nematocysts, all of the type called apotrichous isorhizas, which are found only in Narcomedusae. These nematocysts are nearly spherical, with an exceedingly long, spined tubule (Fig. 4c). Since the tubules are so long, it has been hypothesized that these nematocysts are especially adapted for penetrating and maintaining hold ofthick-jellied prey (Purcell and Mills, in press) and may, therefore, provide the selection device limiting these medusae to large gelatinous food. In S. albescens, the nematocysts on the tentacles are of two sizes (capsule diameters given here are of undischarged nematocysts): 22.5-25.5 .urnand 8.4- 9.6.um in diameter. Nematocysts are also found on the peripheral portions of the exumbrella, although whether these are used for feeding or defense is not known. The exumbrellar nematocysts are also spherical apotrichous isorhizas, with diameters of 14.4-15.6 .urn; they occur in patches of about 10-15. The two size classes of undischarged nematocysts in the tentacles of Friday Harbor specimens of S. marshalli measured 21.0-26.4 .urn and 7.0-9.6 .urn in diameter, with everted tubules measuring respectively 7,000-8,550 and 425-500 .urnlong (Mackie and Mackie, 1963; Mills, unpubl.). The large-sized nematocysts were also found in the subumbrella ectoderm overlying the stomach pouches, and the small-sized nematocysts occurred in the rim of the mouth, edge ofthe velum, and subumbrellar areas covering the stomach pouches, as well as in the tentacles. 746 BULLETIN OF MARINE SCIENCE, VOL. 43, NO.3, 1988

Figure 4. Nematocysts of Solmissus albeseem. (a) Light micrograph showing distribution of apotrichous isorhiza nematocysts on a tentacle. Nearly all of the nematocysts occur on the upper side of the tentacles, indicating that the prey are captured on this side of the tentacles, which are then swept downward and into the mouth. Scale bar = 100 /-Lm. (b) Light micrograph of nematocyst patches on the peripheral area of the exumbrella. Scale bar = 25 /-Lm. (c) Transmission electron micrograph of a portion of the tubules of a discharged apotrichous isorhiza nematocysts of S. albeseens. Scale bar = l.5 i'm.

A third size class of spherical nematocyst, measuring 16.0-18.4 .urnin diameter before discharge, with a 900 .urnlong everted tubule, occurred in patches of 15- 60 capsules (Fig. 4b) in the peripheral areas of the exumbrella (Mackie and Mackie, 1963; Mills, unpubl.).

DISCUSSION Hydromedusae have been reported to undergo diel vertical migrations ranging from about 20 m (Russell, 1928; Thurston, 1977) to the extensive 400-600 m dieI migration of S. abescens examined here. Because species-specific buoyancies in hydro medusae are apparently achieved by exclusion of relatively heavy sulphate ions by an active cross-membrane pump (Mackay, 1969), the possibility that medusae might be able to regulate this buoyancy on a diel basis in order to facilitate long-range vertical migrations has been raised by Mackie (1974). Mills and Vogt (1984) found no variations in day/night ion concentrations in eight species of hydromedusae and a ctenophore and concluded that vertical migration was probably achieved solely by swimming. Our in situ observations reported here of S. albescens, the hydromedusan species with the longest documented diel migration, support the swimming hypothesis: S. albescens is able to swim long distances continuously without stopping. Nearly all of the S. albescens observed were actively swimming during both day and night dives. The long-distance vertical migration of S. albescens appears to occur throughout its range in the western Mediterranean Sea and probably occurs year-round. Con- firming studies have been made in April (the present paper), July, August, and September (Benovic, 1973), and March, May, June and October (Goy and Thiriot, 1976 and Goy, unpubl.). MILLS AND GOY: HEHAVrOR OF MESOPELAGIC SOLMISSUS NARCOMEDUSAE 747

As suggested by Benovic (1973), S. albeseens appears to migrate following an isolume. It did not rise above 100 m during samples taken by Benovic at full moon, yet was observed all the way to the surface during an overcast full moon dive in CYANA (26 April 1986). S. albeseens falls into the group of hydro medusae lacking ocelli that nevertheless show a marked vertical migration in response to light, but in which the light detecting cells have so far not been identified (Mills, 1983). The S. albeseens population migrates to the surface at night. Assuming that its spawning is light synchronized and that spawning occurs at night as in many species of hydromedusae (Miller, 1979; Mills, 1983), vertical migration could increase the chance of fertilization of the freely spawned gametes by doubling the population abundance at night as the animals move into a narrower band near the surface (Fig. 2). The time of spawning is not known for any species of Solmissus. S. albeseens were 1-2 m apart at their most dense. The population density of S. albeseens is much greater than that of most mesopelagic species of medusae. Such high numbers might be supported by trophic advantages gained by the daily migrations to the upper layers to feed on larger or more available prey. In fact, the exact feeding advantages gained from the dieI migration of S. albeseens are not clear from our observations. We know that the medusae feed on Cavolinia pteropods at night in the upper layers (Cavolinia remains above 200 m; unpublished CYANA observations) and that these pteropods do not co-occur with S. albeseens during the day. Whether or not the medusae also feed substantially on the numerous lobate ctenophores Bathoeyroe? fosteri with which it coexists by day (the ratio is up to 20 ctenophores per Solmissus) cannot be established from the one interaction we observed. Although S. albeseens always appeared to have empty guts during the daytime, it is very possible that ingested transparent ctenophores would be effectively invisible to observers in the submersible. As mentioned earlier, gut content studies on net-collected specimens are not feasible since narcomedusae easily void their guts when disturbed. Benovic (1973) surmised that S. albeseens migrated upward following copepods, "its basic food source." It now appears that Narcomedusae do not eat copepods, but feed primarily on gelatinous zooplankton, and that one ofthe selective agents in determining this diet may be their specialized nematocysts with very long (to 8.5 cm), spined tubules. Prey selection by hydromedusae is probably determined in general by a com- bination of swimming pattern and tentacle posture (Mills, 1981b) and nematocyst type (Purcell and Mills, 1987). Feeding while swimming, as occurs with S. albeseens, is done by species of medusae that eat large (usually gelatinous) prey and is seen as the appropriate strategy for taking relatively rare prey which requires searching a large area. In contrast, medusae that feed on small prey usually swim with contracted tentacles, stop, and then spread their tentacles to fish (Mills, 1981b and unpubl.). Observations of animal behavior from a submersible may be biased by the fact that animals living in dimly lit or virtually dark waters are assaulted by the bright lights of the submersible. The fact that the migration speeds calculated from watching individual (well-lit) medusae correspond well to speeds derived from submersible transects giving locations of the whole population is encouraging. Also we observed no clear directional response of S. albeseens to the lights [e.g., swimming downward, as has been seen for some species in laboratory studies of vertical migration in a 1,500 I tank (Mills, 1983)]-S. albeseens seen from CYANA were routinely swimming in all directions and orientations. We are also encouraged by the fact that individual S. marshalli behaved very differently (qui- 748 BULLETINOFMARINESCIENCE,VOL.43,NO.3, 1988

escence or slow pulsations) from S. albescens under similar lighting conditions. It is possible that light-receptive cells in these mesopelagic organisms are over- loaded and rendered non-functional in bright light and that therefore (ironically) behavior may not be seriously affected. Narcomedusae (or at least species of Salmissus, Salmaris and Aegina citrea for which we have in situ observations) seem behaviorally very similar to meso- and bathypelagic coronate scyphomedusae of the genera Periphylla and Atalla. Both groups are strong swimmers, and usually swim with tentacles held above the bell (see photo of Periphylla in Child and Harbison, 1986). Prey capture has been described in two epipelagic coronate species, Nausithae punctata and Linuche unguiculata, by Larson (1979). These species, swimming with their tentacles held up over their bell, capture prey with a rapid downward flexure of the tentacles that pushes the prey down and into the bell. In situ still photographs and an analysis of tentacle morphology led Larson to predict that larger deep water coronates probably feed in the same manner. The apparent convergence of feeding and swimming behaviors between Nar- comedusae and coronate Scyphomedusae are interesting; both of these groups have non-extensile, but bendable tentacles that are different from other Hydro- medusae (except Obelia) and non-coronate Scyphomedusae (which have strongly contractile tentacles also capable of contortions in most dimensions). The limited gut analysis for these two groups suggest that whereas Narcomedusae feed on gelatinous prey, coronates eat at least some crustaceans in their diet (Larson, 1979). The types of nematocysts present in the tentacles and exumbrellas of coronates are completely different than narcomedusan nematocysts and it may be the ability of the various nematocyst types to hang onto potential prey that separates the niches of these two groups of medusae.

ACKNOWLEDGMENTS

We thank P. Laval, J.-c. Bracconnot, C. Carre, and P. Morand for sharing the Solrnissus data from their dives in the "Premigragel" and "Migragel I" campaigns using the submersible CYANAin 1985- 1986. Thanks also to P. Nival for hosting C.E.M.'s visit to France. R. Harbison, L. Madin, and N. Swanberg shared their videotapes from the JOHNSONSEALINK II including footage of Solrnissus rnarshalli. Special thanks are extended to the crews of the CYANA,NOROIS,JOHNSONSEALINKII, SEA DIVER,ED LINK,CAPEFLORIDA,PISCESIV and PANDORAwho made the dives possible and enjoyable, C.E.M. was supported by the International Exchange of Scientists Program between the National Science Foundation (USA) and thc Centre National de la Recherche Scientifique (CNRS) of France during her stay in France. Observations from the JOHNSONSEALINKII were made possible by NSF (Biological Oceanography) Grants #OCE-8400243 to G. R. Harbison and L. P. Madin, #OCE-8701388 to G. R. Harbison, and an "inhouse" Harbor Branch Oceanographic Institution grant to G. R. Har- bison. Observations from the PiSCESIV were made at the invitation of G. O. Mackie. Skidaway Institute of Oceanography funded the Zooplankton Behavior Symposium in which this paper was presented. Most of the research was conducted at the Station Zoologique in Villefranche-sur-Mer, France. This paper is contribution number 12 from the Direct Study of Mesopelagic Plankton Project.

LITERATURE CITED

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Furnestin, J. 1955. Une plongee en bathyscaphe. Rev. Trav. Inst. Peches Marit. 19: 435-442. Goy, J. 1971. Sur la repartition bathymctrique des hydromcduses en mer de Ligurie. Rapp. Comm. Int. Mer. Mcdit. 20: 397-400. ---. 1972. Les hydromcduses de la mer Ligure. Bull. Mus. Hist. nat., Paris, 3"ser. 83, Zoologie 62: 965-1009. ---. 1974. Calendrier des hydrom6duses en mer Ligure. Comm. Int. Mer. Medit. 22: 125-127. ---. 1987. Summer subvergence of Persa incalarata McCrady, 1857 (Cnidaria, Hydromedusa) in the Mediterranean. Ann. Inst. Oceanogr. (Paris) 63: 47-56. --- and A. Thiriot. 1976. Conditions estivales dans la divergence de Mcditerance nord-occidcn- tale. II. Macroplancton et micronecton. Etude qualitative et estimation quantitative des cnidaires et des euphausiaccs. Ann. Inst. Oceanogr. (Paris) 52: 33-44. Hartman, O. and K. O. Emery. 1956. Bathypelagic coelenterates. Limnol. Oceanogr. I: 304-310. Kramp, P. L. 1959. The Hydromedusae of the Atlantic Ocean and adjacent waters. Dana Rep. 46: 1-283. ---. 1968. The Hydromedusae of the Pacific and Indian Oceans: Sections II and III. Dana Rep. 72: 1-200. Lakkis, S. and R. Zeidane. 1985. Les hydrom6duses des eaux neritiques libanaises: composition et distribution. Rapp. Comm. Int. Mer. Mcdit. 29: 179-180. Larson, R. J. 1979. Feeding in coronate medusae (Class Scyphozoa, Order Coronatae). Mar. Behav. Physiol. 6: 123-129. Mackay, W. C. 1969. Sulphate regulation in jellyfish. Compo Biochem. Physiol. 30: 481-488. Mackie, G. O. 1974. Locomotion, flotation and dispersal. Pages 313-357 in L. Muscatine and H. Lenhoff, eds. Coelenterate biology: reviews and new perspectives. Academic Press, New York. ---. 1985. Midwater macroplankton of British Columbia studied by submersible PISCES IV J. Plankton Res. 7: 753-777. --- and G. V. Mackie. 1963. Systematic and biological notes on living hydromedusae from Puget Sound. Natl. Mus. Canada (Contrib. Zool.) Bull. 199: 63-84. --- and C. E. Mills. 1983. Use of the Pisces IV submersible for zooplankton studies in coastal waters of British Columbia. Can. J. Fish. Aquat. Sci. 40: 763-776. Miller, R. L. 1979. Sperm chemotaxis in the hydromedusae. I. Species-specificityand sperm behavior. Mar. BioI. 53: 93-114. Mills, C. E. 1981a. Seasonal occurrence of planktonic medusae and ctenophores in the San Juan Archipelago (NE Pacific). Wasmann J. BioI. 39: 6-29. ---. 1981b. Diversity of swimming behaviors in hydromedusae as related to feeding and utili- zation of space. Mar. BioI. 64: 185-189. ---. 1982. Patterns and mechanisms of vertical distribution of medusae and ctenophores. Ph.D. Dissertation, University of Victoria, Victoria, Canada. 384 pp. ---. 1983. Vertical migration and diel activity patterns of hydromedusae: studies in a large tank. J. Plankton Res. 5: 619-635. --- and R. L. Miller. 1984. Ingestion of a mcdusa (Aegina citrea) by the nematocyst-containing ctenophore Haeckelia rubra (formerly Euchlara rubra): phylogenetic implications. Mar. BioI. 78: 215-221. --- and R. G. Vogt. 1984. Evidence that ion regulation in hydromedusae and ctenophores does not facilitate vertical migration. BioI. Bull. 166: 2 J 6-227. Peres, J. M. 1958a. Resultats scientifiques des campagnes du Bathyscaphe F.N.R.S. III 1954-1957. V. Remarques generales sur un ensemble de quinze plong6es effectuees avec Ie bathyscaphe F.N.R.S. III. Ann. Inst. Oceanogr. (Monaco) 35: 259-285. ---. 1958b. Trois plong6es dans Ie canyon du Cap Sicie, effectuees avec Ie bathyscaphe F.N.R.S. III de la Marine Nationale. Bull. Inst. Oceanogr. (Monaco) 1115: 1-21. ---. 1959. Deux plongees au large du Japon avec Ie bathyscaphe franyais F.N.R.S. III. Bull. Inst. Oc6anogr. (Monaco) 1134: 1-28. --- and J. Picard. 1955. Observations biologiques effectuees au large de Toulon avec Ie bathy- scaphc F.N.R.S. III de la Marine Nationale. Bull. Inst. Oceanogr. (Monaco) 1061: 1-8. --- and ---. 1956. Nouvelles observations biologiques effectu6esavec Iebathyscaphe F.N.R.S. III et considerations sur Ie systeme aphotique de la Mediterranee. Bull. Inst. Oceanogr. (Monaco), 1075: 1-10. Purcell, J. E. and C. E. Mills. In press. The correlation between nematocyst types and diets in pelagic Hydrozoa. In D. A. Hessinger and H. Lenhoff, eds. The biology of nematocysts. Academic Press, New York. Russell, F. S. 1928. The vertical distribution of marine macroplankton. VI. Further observations on diurnal changes. J. Mar. BioI. Assoc. U.K. 15: 81-103. Schmidt, H.-E. ]973. Hyromedusae from the eastern Mediterranean Sea. Israel J. Zool. 22: 151- 167. 750 BULLETINOFMARINESCIENCE,VOL.43, NO.3,1988

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DATEACCEPTED:April II, 1988.

ADDRESSES:(C.E.M.) Friday Harbor Laboratories, University of Washington, 620 University Road, Friday Harbor, Washington 98250. (J.G.) Laboratoire d'/chtyologie generale et applique, Museum national d'Hisloire naturelle, 43 rue Cuvier, 7523/ Paris Cedex 05, France.

ApPENDIX: DISCUSSION AFTER MILLS AND GOY W. De.i\.1ott:What predators might be causing medusae to migrate down during the day? C. Mills: Other medusae are probably the major predators on hydromedusae, There is also some anecdotal evidence of feeding by birds, turtles and some fishes. J. Runge: I participated in a study of feeding behavior of Atlantic mackerel on the medusae Aglantha digitale. We found that mackerel in a large tank fed readily on Aglantha. The fish would show distinct biting behaviors when Aglantha were added, usually approaching the medusae from underneath, Fish predation on medusae may be more important than we now think. N. Marcus: Pennington and Emlet (J,E.M.B.E., 1986) have recently demonstrated that echinoid larvae behaviorally avoid high UV surface waters. Is it possible that downward migrations of these very transparent animals are an attempt to escape damage from UV light? C. .i\.1ills:Unfortunately there are not any data on that. M. Omori: In the case of pelagic crustaceans and fishes, diel vertical migrations are well observed among epi- and mesopelagic species (living above 800- 1,000 m depth), but bathy- and abyssopelagic species do not migrate. Is this also true with medusae? L. .i\.1adin:Narcomedusae and coronate scyphomedusae are generally non-migrating mesopelagic forms. C. Mills: Michael Thurston has presented net data showing small-scale diel vertical migrations of several North Atlantic mesopelagic species of medusae. On the other hand, George Mackie has shown that deeper living individuals of migratory species that occur over broad depth distributions do not show the same diel patterns as epipelagic individuals, apparently for lack ofIight cues. I am not aware of any good bathy- or abyssopelagic data sets for migration of medusae, M. Gliwicz: Is there enough data to estimate the costs of escaping predation for medusae? C. Mills: Besidesproduction ofnematocysts and vertical migration, there is another cost which is so far unexamined. Medusae have a distinctive smell that may MILLS AND GOY: BEHAVIOR OF MESOPELAGIC SOLMISSUS NARCOMEDUSAE 751

be a compound that they produce for protective or offensive purposes. Other than anecdotal observations on the occurrence of this substance, its purpose and cost of production are unexamined. It also should be noted that with the exception of 1 or 2 species, we do not know the daily feeding ration of most medusae. Much basic information is lacking. D. Checkley: Do these animals feed continuously? C. Mills: We do not know.