Journal of Experimental Marine Biology and Ecology, L 222 (1998) 79±91

The role of temperature in survival of the stage of the tropical rhizostome jelly®sh xamachana

William K. Fitt* , Kristin Costley Institute of Ecology, Bioscience 711, University of Georgia, Athens, GA 30602, USA Received 27 September 1996; received in revised form 21 April 1997; accepted 27 May 1997

Abstract

The life cycle of the tropical jelly®sh involves alternation between a polyp ( 5 scyphistoma) and a medusa, the latter usually resting bell-down on a sand or mud substratum. The scyphistoma and newly strobilated medusa (5 ephyra) are found only during the summer and early fall in South Florida and not during the winter, while the medusae are found year around. New medusae originate as ephyrae, strobilated by the polyp, in late summer and fall. Laboratory experiments showed that nematocyst function, and the ability of larvae to settle and metamorphose change little during exposure to temperatures between 158C and up to 338C. However, tentacle length decreased and ability to transfer captured food to the mouth was disrupted at temperatures # 188C. Unlike temperate-zone of scyphozoans, which usually over-winter in the polyp or podocyst form when medusae disappear, this tropical species has cold-sensitive scyphistomae and more temperature-tolerant medusae.  1998 Elsevier Science B.V.

Keywords: ; Jelly®sh; Cassiopea; Temperature; Life history

1. Introduction

The rhizostome medusae of Cassiopea xamachana are found throughout the Carib- bean Sea, with their northern limit of distribution on the southern tip of Florida. Unlike most scyphozoans these jelly®sh are seldom seen swimming, and instead lie pulsating bell-down on sandy or muddy substrata in or soft bottom bay habitats, giving rise to the common names `` jelly®sh'' or ``upside-down jelly®sh''. Medusae obtain a portion of their carbon requirements from symbiotic algae of the Symbiodinium, also known by the generic term ``'' (see Hofmann and

*Corresponding author.

0022-0981/98/$19.00  1998 Elsevier Science B.V. All rights reserved. PII S0022-0981(97)00139-1 80 W.K. Fitt, K. Costley / J. Exp. Mar. Biol. Ecol. 222 (1998) 79 ±91

Kremer, 1981; Trench, 1993). Unlike zooxanthellate , however, only the largest Cassiopea xamachana are able to theoretically obtain all of the carbon necessary to fuel their respiratory metabolism from their zooxanthellae (Vodenichar, 1995), and most medusae must obtain a portion of their nutrients from external feeding and possibly absorption of dissolved nutrients (Schlichter, 1982). The life cycle of Cassiopea involves alternation between a medusoid stage and a polyp (5 scyphistoma) and has been widely studied (Bigelow, 1900; Smith, 1936; Hofmann et al., 1996). The medusae are dioecious; the eggs in the female presumably fertilized by sperm released by nearby males. The fertilized eggs are transported to specialized knob-shaped tentacles near the center of the female, where they develop into larvae which hatch out shortly after acquiring competence to metamorphose. The planulae attach permanently to hard substrata during settlement and then metamorphose into a polyp with tentacles. These scyphistomae can reproduce asexually by budding when food is plentiful, and the buds settle and form scyphistomae. Scyphistomae strobilate, producing medusae, only after they acquire certain species of Symbiodinium and when temperatures are higher than 208C (Hofmann et al., 1978, cf. Rahat and Adar, 1980). Whereas the medusae are always found with zooxanthellae, larvae and newly- settled scyphistomae are aposymbiotic. Each new scyphistomae must acquire zoox- anthellae in order to complete the life cycle. They apparently acquire zooxanthellae from the surrounding seawater or in conjunction with feeding (Fitt, 1992). While there has been little monitoring of populations of Cassiopea spp. over time, there are many anecdotal accounts of large numbers of these medusae appearing in areas near centers of human population. For instance, many canals and near-shore areas in the Florida Keys have become ®lled with adult medusae during the past ten years where apparently few if any existed before. These observations, coupled with the ®nding that carbon from zooxanthellae in most medusae of Cassiopea xamachana cannot provide all of the energy necessary for basic respiratory metabolic needs (Vodenichar, 1995), suggest that high dissolved and/or particulate nutrients may be augmenting growth and successful recruitment in high-nutrient habitats (LaPointe et al., 1990; Mackey and Smail, 1996). Similarly, large populations of medusae of Cotylorgiza tuberculata and Pelagia noctiluca become a nuisance in bays and areas near coastal cities in the Mediterranean off Greece during the summer months, but disappear during the winter months (Goy et al., 1989; Kikinger, 1992). The scyphistomae of Cotylorgiza tuberculata are thought to survive the wintertime conditions, strobilating medusae when the temperatures rise in the spring. Such is also the case with Aurelia aurita, Cyanea capillata, and Chrysaora quinquecirrha, where exposure to low temperatures for a critical amount of time is thought to be required for scyphistomae to strobilate (see Spangenberg, 1967; Loeb, 1972; Calder, 1974). The cannonball jelly®sh, Stomolophus meleagris, a temperate-zone rhizostome common during the spring and summer months on the East Coast of the United States, also has scyphistomae that survive the winter (Calder, 1982). Thus, most temperate scyphozoan species appear to tolerate seasonal low temperatures in the polyp morphology, or sometimes as podocysts during the coldest part of the winter (i.e., Calder, 1982), while thriving during the spring, summer and fall as either medusae or scyphistomae. In this study we investigate physiological factors important in controlling the life W.K. Fitt, K. Costley / J. Exp. Mar. Biol. Ecol. 222 (1998) 79 ±91 81 cycle of Cassiopea spp., while correlating the seasonal occurrence of scyphistomae to the seasonal changes in size structure of a population of medusae of Cassiopea xamachana in the Florida Keys.

2. Materials and methods

2.1. Maintenance of

Stock cultures of scyphistomae of Cassiopea xamachana were maintained at room temperature (26628C) in Instant Ocean seawater (30 ppt). The scyphistomae were fed at 3-day intervals during both maintenance and experiments, and their water was changed after each feeding on the day of feeding. Unless otherwise noted, all animals were moved directly from maintenance conditions into glass Petri dishes which were placed inside the temperature-controlled water baths at the beginning of the experimental period. Measurements of seawater temperatures in the glass Petri dishes showed that transition to experimental temperatures occurred in the form of slow heat transfer through the glass Petri dishes. It took approximately 1 h for seawater in the Petri dishes to change 58C.

2.2. Seasonal presence of scyphistomae and changes in size of medusae

The presence or absence of the scyphistomae polyps was monitored from a mangrove site on Grassy Key and in a man-made swimming lagoon at the Ocean Reef Resort on Key Largo in the Florida Keys over a 5-year period between 1989 and 1994. The substratum on which the scyphistomae were found was noted. Medusa size (diameter) was measured approximately every 2 months during 1992±1993 from 50±100 in- dividuals sampled from approximately the same 1 m2 location near a mangrove island on Grassy Key. The presence or absence of developing eggs on large females was assessed seasonally, by manually checking for eggs in all females encountered in conjunction with the seasonal size measurements.

2.3. Settlement experiments

Dark red mangrove leaves (n 5 10), a natural substratum for scyphistomae, were collected during different seasons and placed into sterile cell culture dishes with 10±20 larvae of Cassiopea xamachana for 1 wk. Previous research has shown that a peptide found in degrading mangrove leaves induces larvae to settle on the leaves (Hofmann et al., 1996). Settlement of larvae on mangrove leaf, as well as the plastic culture dish, was noted. All leaf experiments were performed at room temperature, 26628C. In order to quantify the effects of seawater temperature on settlement, larvae of Cassiopea xamachana were placed in Petri dishes of seawater containing known amounts of arti®cial inducer at temperatures of 158C, 208C, 268C, and 338C for 72 h. Metamorphosis was induced by addition of 5, 10, or 25 mM of the arti®cial peptide inducer Z-Gly-Pro-Gly-Gly-Pro-Ala (Sigma) to 20±30 larvae in 1 ml of seawater 82 W.K. Fitt, K. Costley / J. Exp. Mar. Biol. Ecol. 222 (1998) 79 ±91 containing antibiotics (Fitt et al., 1992). After 24 h the percentage of larvae attached at each temperature was recorded. Control larvae were maintained at each experimental temperature without the addition of the peptide.

2.4. Feeding experiments

The effect of temperature on tentacle extension and general polyp appearance was investigated in another experiment. Mean tentacle length per polyp was determined from the average length of four tentacles from each of six scyphistomae at the beginning of the experiment and at 6-day intervals. Measurements were made with an ocular micrometer. After the initial measurements at 268C, six scyphistomae were placed in each Petri dish in water baths set at 188C, 208C, 308C, 338C, and 368C. Water temperatures took about1htostabilize at the new temperatures. Four tentacles from each polyp were measured after 6 days. The 188C and 208C baths were then decreased to 15 and 178C respectively, and the 338C bath was increased to 358C, and then to 388C. After another 6 days, or 24 h for animals in 388C seawater, the lengths of four tentacles from each polyp were measured again and change in mean length was calculated. In order to control for the change in tentacle length in response to the multiple temperatures tested above, sets of six replicate scyphistomae were maintained for 6 days at constant experimental temperature (18, 20, 30, and 338C), in addition to the control temperature of 268C. Four tentacles from each were measured at the beginning and after 6 days. Nematocyst function was assayed using tentacles of scyphistomae that were main- tained at temperatures ranging from 68Cto388C. After 24, 48, and 72 h at temperature three polyps from each experimental temperature were macerated on microscope slides. Acetic acid (5%) was added to the slides, and ability of nematocysts to discharge was monitored microscopically. Another assay of nematocyst function was ability of scyphistomae to capture newly-hatched nauplii of Artemia. Tentacular capture and ingestion of Artemia by scyphistomae was observed in animals maintained for 72 h at temperatures ranging from 10±368C. Prey capture and ingestion were recorded.

2.5. Measurement of metabolic rate

The respiration rate of twenty scyphistomae was determined from measurements using a Yellow Springs Instrument (YSI) oxygen electrode at 268C, and following a 30-min acclimation interval between temperatures, also at 228C, 208C, 188C, 158C, and 128C. Rates were also determined from a second set of twenty scyphistomae maintained at room temperature, with measurements made successively at 268C, 308C, 328C, 348C, and 368C after 30 min acclimation periods.

3. Results

3.1. Field observations

Scyphistomae were found on the undersides of mangrove leaves, sometimes on leaves W.K. Fitt, K. Costley / J. Exp. Mar. Biol. Ecol. 222 (1998) 79 ±91 83 of other trees, and rarely on dead blades of turtle grass Thalassia during the mid and late summers of 1990±1996. However, no scyphistomae were observed at these sites between late November and early June. Large numbers of the benthic-dwelling ephyra and strobilating scyphistomae were present from late June and into the fall. There were no ephyra seen during the winter or spring. The average size of medusae in 1992±1993 from the Grassy Key site increased between August and January, at which time it leveled off at 5±7 cm diameter (Fig. 1). The average diameter decreased again with the strobilation of new medusae late the next summer. Though medusae were always seen at Grassy Key throughout the year, there were three instances when some individuals looked stressed and abnormal. In December 1991, following the passage of a severe cold front through Florida, numerous medusae had distended tentacles and asymmetric bells. The water temperature in the shallow seagrass beds surrounding adjacent to mangrove islands at Grassy Key was 12±148C. Though the population density of medusae was obviously less than the previous fall, it was not clear if temperature or other environmental factors were responsible for the decrease. An example of the rapid decreases in temperature that occur on the shallow seagrass± mangrove ¯ats where the jelly®sh live during the passage of a cold front is given in Fig. 2. In August of 1992, 1993 and 1996 many medusae on a shallow seagrass±mangrove ¯at at Grassy Key appeared bleached with clear gelatinous bells and tentacles containing less than 20% of the normal density of zooxanthellae. Afternoon water temperatures of 36±378C on the bottom were recorded on September 5, 1993 and in late summer 1996 (Fig. 2), and many individuals had holes through their bells or bells separated from the tentacles. All female medusae ( . 5 cm diameter) carried developing eggs during the summer

Fig. 1. Size±frequency distribution of medusae of Cassiopea xamachana from Grassy Key over the course of a year. 84 W.K. Fitt, K. Costley / J. Exp. Mar. Biol. Ecol. 222 (1998) 79 ±91

Fig. 2. Temperature records from shallow (ca. 0.2 m) seagrass±mangrove ¯ats in Florida Bay near Grassy Key, 1996. Note daily temperature variation, with rates of change sometimes reaching 28C per hour. (A) Late summer. (B) Late fall. and fall, while less than half had eggs during the winter months (Table 1). The only times eggs were dif®cult to ®nd on female medusae were a week to two weeks following cold fronts that pass through South Florida during the winter and early spring, and a W.K. Fitt, K. Costley / J. Exp. Mar. Biol. Ecol. 222 (1998) 79 ±91 85

Table 1 Presence of developing larvae of Cassiopea xamachana on mature female medusae ( . ca. 7 cm diameter) and ability of larvae to metamorphose on mangrove leaves found in the same environment as the adult medusae Date Percent of Settlement and female medusae metamorphosis on with developing mangrove leaves larvae Summer 100 1 Fall 100 1 Winter , 50a 1 Spring 100a 1 a One to two weeks following the passage of severe cold fronts through South Florida the percentage of mature females with developing larvae decreased, sometimes to 0. week to two weeks following the close passage of a hurricane with westerly winds that brought masses of rotting seagrasses onshore during August 1996.

3.2. Settlement and metamorphosis

Larvae settled and metamorphosed on natural and arti®cial substrata during all seasons (Table 1). Most larvae introduced to seawater containing mangrove leaf settled within 2 days on the mangrove leaf or sometimes on the sides of the culture plate wells containing mangrove leaves. Settled animals typically developed a mouth and tentacles and completed metamorphosis within a few days of settlement. The percentage of larvae that settled and metamorphosed in response to peptide inducer generally increased with increasing concentration of peptide inducer at all temperatures tested (Fig. 3). However, lower percentages of larvae tested at 15 and 208C metamorphosed over a 72 h period compared to larvae tested at higher temperatures. Control animals with no inducer added did not settle at any temperature.

3.3. Feeding ability of scyphistomae

Nematocysts discharged normally at every experimental temperature and time tested between 6 and 388C when subjected to 5% acetic acid (Table 2). Tentacles from polyps held at 36 and 388C were withdrawn, and though the animal tissue began to disintegrate the nematocysts present discharged. Scyphistomae captured and ingested Artemia at all temperatures between 208Cto348C. However, at temperatures # 158C Artemia were captured but not ingested (Table 2). At temperatures higher than 368C, tentacles began to fall apart and Artemia were not captured. The effect of temperature on tentacle extension was documented. Tentacles of scyphistomae were extended and ®liform in appearance when exposed to temperatures between 20 to 348C for up to 72 h (Table 3, Fig. 4). Tentacle length of scyphistomae was generally . 1 mm at all temperatures between 20 and 348C, above which the length 86 W.K. Fitt, K. Costley / J. Exp. Mar. Biol. Ecol. 222 (1998) 79 ±91

Fig. 3. Percentage of larvae of Cassiopea xamachana settling and metamorphosing in response to the standard peptide inducer z-GPGGPA (see Section 2). (A) Colder temperatures: 268C (open circles), 208C (closed circles), 158C (triangles). (B) Warmer temperatures: 268C (open circles), 338C (triangles). decreased markedly (Fig. 4). At 368C all tentacles appeared withdrawn, shorter and broader in comparison to controls, and at 388C the tentacles began to disintegrate within 24 h. When moved to 15±208C temperatures the polyps retained their shape except that tentacles became noticeably shorter and thicker (Fig. 4). Scyphistomae died within 5 days at temperatures below 158C.

3.4. Respiration rates

The effect of temperature on respiration rate was investigated on two groups of twenty W.K. Fitt, K. Costley / J. Exp. Mar. Biol. Ecol. 222 (1998) 79 ±91 87

Table 2 Nematocyst ®ring, prey capture and ingestion of nauplii of Artermia by scyphistomae of Cassiopea xamachana Temperature (8C) Nematocysts ®ring Prey capture Ingestion 6 1 n.d. n.d. 8 1 n.d. n.d. 10 112 15 112 20 111 26 111 30 111 36 111 38 1 n.d. n.d. Nematocyst ®ring: 15nematocyst discharge; 25no discharge. Prey capture: 15Artemia captured on tentacle. Ingestion: 15Artemia captured and transferred to mouth and engulfed by scyphistomae; 25Artemia captured, no transfer or engulfment observed within 15 min; n.d. 5 no data available due to disintegration of tentacle. polyps (Fig. 5). When temperature was decreased from 26 to 128C in one group, the respiration rate decreased (Q10 5 2.48). Conversely, as temperature increased between 26 and 368C, the change in respiration rate increased (Q10 5 2.43).

4. Discussion

Medusae of Cassiopea spp. are formed from polyps by the process known as strobilation, whereby the oral disc of the scyphistomae pinches off from the stalk to form the juvenile jelly®sh known as an ephyra. Strobilation occurs only at temperatures higher than 208C and in the presence of zooxanthellae (Hofmann et al., 1978, cf. Rahat and Adar, 1980). The fact that scyphistomae and ephyra were found only during the summer and early fall when water temperatures were highest, but not in the late fall or winter or spring when cold fronts from the north lowered water temperatures, suggests that the polyp portion of the life cycle may have different physiological limits than either the larvae or medusae. Our data show that the scyphistomae did not effectively ingest food at temperatures # 158C. Tentacle length decreased, nematocysts ®red, and prey was Table 3 Tentacle length (mm) of scyphistomae of Cassiopea xamachana at the beginning and end of a 6-day experiment where temperature was held constant Temperature (8C) Beginning length (s.d.) End length (s.d.) Percent change 18 1.1260.16 0.1860.10 2 83 20 1.2960.36 1.7460.63 1 35 26 1.0460.22 1.4460.58 1 38 30 1.3160.28 1.8060.40 1 38 33 1.1360.67 2.0960.66 1 84 Data are means6s.d. from tentacles of six scyphistomae for each temperature. 88 W.K. Fitt, K. Costley / J. Exp. Mar. Biol. Ecol. 222 (1998) 79 ±91

Fig. 4. Mean tentacle lengths of Cassiopea xamachana (four tentacles measured and averaged from each of six scyphistomae for each data point): (A) tentacle length in relation to time for control animals maintained at 268C; (B) tentacle length of animals at the control temperature of 268C, and then 72 h after being moved to a temperature either above or below 268C as indicated by arrows. Each line represents one separate experiment. In some experiments animals were moved again to another temperature, in the same direction (arrows) after another 72 h.

captured on tentacles, but polyps were unable to transfer captured food to the mouth. Reduced tentacle length and ciliary function may be responsible for the latter observation. The data suggest that scyphistomae may starve to death during periods of cold water, in spite of the fact they may be able to catch food. This observation, coupled with ®ndings of signi®cantly less larval settlement at temperatures , 208C compared to . 208C, could explain the absence of the scyphistomae portion of the life cycle from late W.K. Fitt, K. Costley / J. Exp. Mar. Biol. Ecol. 222 (1998) 79 ±91 89

Fig. 5. Respiration rates (oxygen consumption) of two sets of twenty scyphistomae of Cassiopea xamachana held at 268C and then moved to either successively higher (®lled symbols, y 520.459 1 0.026, R2 5 0.958) or successively lower (open symbols y 520.034 1 0.006, R2 5 0.718) temperatures.

fall to the early summer when seawater temperatures rise in south Florida and other locations in the Caribbean Sea. The possibility that female medusae produce no larvae during the winter months was rejected since female medusae carried developing eggs the entire year, except for brief periods following severe cold fronts passing through South Florida during the winter and early spring. Virtually every mature ( . ca. 10 cm diameter) female contained developing egg during the summer months. The proportion of females carrying eggs decreased to , 50% during the winter and early spring. Another hypothesis explaining the lack of scyphistomae during the winter holds that natural cues for settlement and metamorphosis are not present during the winter and spring. This hypothesis was also rejected since laboratory experiments showed that numerous substrata, including rock, sand, shell and rotting vegetation can serve as substrata for polyps, even during the winter and spring. However, in controlled experiments with an arti®cial peptide inducer, larvae exhibited reduced settlement and metamorphosis at 158C, compared to settlement at 208C and higher, as well as disintegration of larvae at temperatures between 10 and 158C. Metabolic rate of scyphistomae increased with increasing temperature and decreased with decreasing temperature at rates typical of marine invertebrates, with a Q10 5 ca. 2.4. There was no evidence that changes in metabolic rates were responsible for the disappearance of scyphistomae. Unlike medusae which contain high densities of zooxanthellae (Hofmann and Kremer, 1981; Vodenichar, 1995), scyphistomae start out life aposymbiotic and acquire low numbers of zooxanthellae before strobilation, thus requiring an external source of nutrients. The hypothesis that zooplankton food, present predominantly in tropical reef 90 W.K. Fitt, K. Costley / J. Exp. Mar. Biol. Ecol. 222 (1998) 79 ±91 habitats as demersal plankton (Alldredge and King, 1977), is not available for scyphistomae to feed on during the winter and spring was not investigated in this study. However, McWilliam et al. (1981) showed that there are less demersal plankton in the water column on reefs at night during the winter than during the summer. Lack of adequate planktonic food during part of the year might help explain the absence of scyphistomae, except that density of food makes little difference when scyphistomae in colder water are unable to eat. There is evidence that scyphozoans living in more tropical habitats (i.e., lower latitudes) may experience less seasonal variation resulting in various size classes throughout the year. For instance, all sizes of medusae of the rhizostome Mastigias papua live in lakes in Palau Western Caroline Islands, ca. 78 latitude (Hamner and Hauri, 1981; Muscatine et al., 1986), and scyphistomae are apparently common throughout the year (Hamner and Hauri, 1981; Fitt, unpubl. obs.). By contrast, it appears that the life cycle of species of scyphozoans living in more temperate-zone climates may be broken during the colder winter months. The medusa stage of most temperate scyphozoan species disappear during colder seasons, including the sea nettle Chrysaora quinquecirrha (Calder, 1974), the rhizostome ``cannonball jelly®sh'' Stomolophus meleagris (Calder, 1982), Cyanea capillata (in Spangenberg, 1967), and the ubiquitous ``moon jelly'' Aurelia aurita (Moller, 1980). In addition, medusae of the most common rhizostome in the Mediterranean, Cotylorgiza tuberculata, vanish from coastal pelagic habitats during the colder months while the polyp presumably remains to repopulate the next spring (Kikinger, 1992). In the present study, the scyphistoma stage of the life cycle of Cassiopea xamachana, but not the medusae, disappear during the winter months in south Florida. The physiological tolerance of the polyp stage to cold stress appears to surpass that of the medusa stage in the former more temperate species, while the opposite holds true for the more tropical species of Cassiopea spp., perhaps de®ning a physiological basis limiting its latitudinal distribution.

Acknowledgements

We thank the Florida Department of Natural Resources for permits to collect jelly®sh in the Florida Keys, R. Post and the residents of Ocean Reef Club on Key Largo for permission to collect specimens from their lagoon on northern Key Largo, and Dr. S. Kempf for introducing us to the Grassy Key site many years ago. G. Chilcoat, Dr. Dieter and Dora Hofmann, B. Fitt, Dr. J. Fleck, N. Jess, S. Quinlan, M. Warner, J. Vodenichar, and many others assisted over the years on various aspects of this study. We thank Dr. A. Alldredge for information on demersal plankton. This research was partially supported by NSF (9108074). Contribution No. 005 of the Key Largo Marine Research Labora- tory.

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