The Role of Temperature in Survival of the Polyp Stage of the Tropical Rhizostome Jelly®Sh Cassiopea Xamachana
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Journal of Experimental Marine Biology and Ecology, L 222 (1998) 79±91 The role of temperature in survival of the polyp stage of the tropical rhizostome jelly®sh Cassiopea 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 Cassiopea xamachana 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 species 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: Scyphozoa; 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 mangroves or soft bottom bay habitats, giving rise to the common names ``mangrove jelly®sh'' or ``upside-down jelly®sh''. Medusae obtain a portion of their carbon requirements from symbiotic algae of the genus Symbiodinium, also known by the generic term ``zooxanthellae'' (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 corals, 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 animals 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.