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Effect of Jellyfish Size and Season

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Effect of Jellyfish Size and Season MARINE ECOLOGY PROGRESS SERIES Vol. 168: 147-162,1998 Published July 9 Mar Ecol Prog Ser Production, respiration, and photophysiology of the mangrove jellyfish Cassiopea xamachana symbiotic with zooxanthellae: effect of jellyfish size and season E. Alan verde1r', L. R. McCloskey2 'Oregon State University. Department of Zoology. 3029 Cordley Hall, Corvallis, Oregon 97331. USA *~aSierra University, Department of Biology, 4700 Pierce Street, Riverside, California 92515, USA ABSTRACT: The association between the symbiont Symbiodinium microadriaticum (zooxanthellae) and its host jellyfish, Cassiopea xamachana, was investigated as a function of jellyfish size and season. Symbiont cell diameter and volume were higher dunng January than September. Although zooxan- thella-specific chlorophyll was independent of jellyfish size, both chlorophyll a and c were higher dur- ing January. Regardless of season, algal density and jellyfish size were inversely related. The die1 mitotic index (MI) of zooxanthellae was phased, with a peak of 0.25 y: occurring between 09:OO and 12:OO h. September photosynthetic rates were always higher than January rates and reflected the sea- sonal light and temperature regimes at the latitude of the Florida Keys (USA). Photosynthesis, when normalized to either zooxanthella density or protein, displayed an inverse relationship with jellyfish slie ?v?~ii~l~dliIB~~II~LIUII 1die3 dlbu biluwed iuve~be~eidii~llsilip w~ii~ jeiiyiisil size, w~iilSepielll'uer metabolism being higher than that of January. The carbon budgets calculated for these rnedusae indi- cate that the carbon photosynthetically fixed by the zooxanthellae, and subsequently translocated to the host, is capable of satisfying about 169% of the host's metabolic demand (CZAR) and is indepen- dent of both jellyfish size and season. These seasonally influenced physiological effects underscore the necessity for seasonal examinations of algal-cnidarian syrnbioses in order to understand the photo- physiology of the association on an annual basis KEY WORDS: Cassiopea xamachana - Zooxanthellae . Jellyfish . Photosynthesis . Respiration . Photo- physiology. Carbon budgets. CZAR INTRODUCTION of zooxanthellae. Differences in the excretion rates of ammonia between aposymbiotic and symbiotic Cassio- The relationship between marine unialgal symbionts pea sp. suggest that the zooxanthellae remove host- (zooxanthellae) and cnidarian hosts has been more produced ammonia and aid in the recycling of nitrogen widely studied for benthic cnidarians (reviews by Mus- (Cates & McLaughlin 1976).Hofmann & Kremer (1981) catine 1990, Battey 1992, Davles 1992, Trench 1993) and Hofmann et al. (1996) investigated the importance than for motile ones. Early studies on the scyphozoan of zooxanthellae to strobilation in Cassiopea androm- Cassiopea sp. showed that endosymbiotic zooxanthel- eda and reported that the presence of algae was indis- lae (Symbiodinium)are capable of CO2uptake and fix- pensable although algal photosynthesis or photosyn- ation (Balderston & Claus 1969, Drew 1972) and subse- thate release was not essential for this process. quent carbon translocation to host tissues (Balderston Apparently, the symbiotic zooxanthellae produce and & Claus 1969). Cates (1975) suggested that these pho- supply a 'factor' which promotes the elevated metabo- tosynthesis-respiration interactions enhance the eco- lism required for proceeding through developmental logical efficiency of Cassiopea sp. due to the presence stages (Rahat & Hofmann 1987). The photosynthetic carbon budget of the epipelagic coronate medusa Linuche unguiculata has been inves- 0 Inter-Research 1998 Resale of full article not permitted 148 Mar Ecol Prog Ser 168: 147-162. 1998 tigated by Kremer et al. (1990); zooxanthellae from Algal parameters. Chlorophylls: After homogeniza- these medusae are capable of contributing carbon tion of each jellyfish, the algae were obtained by 3 cen- products towards host respiratory requirements trifugation~,each at 3 to 4 min at top speed in a clinical (CZAR) of approximately 160%. A similar study on the centrifuge, with the algal pellet resuspended each time swimming rhizostomid medusa Mastigias sp. was con- in filtered seawater. Three replicate aliquots (3.0 m1 ducted by McCloskey et al. (1994); CZAR estimates each) of resuspended algae were processed as averaged 97 and 176% for lake and lagoon ecotypes, described by Verde & McCloskey (1996). Between 15 respectively. In contrast to both L. unguiculata and and 20 hemacytometer grids were counted to obtain Mastigias sp., Cassiopea xamachana is more seden- algal density (cells ml-l) of the suspension which was tary, spending most of its time with the bell's exum- used for chlorophyll assays. The chlorophyll content brella in direct contact with the substrate and its tenta- was calculated using the equations of Jeffrey & cles elevated towards the surface (Blanquet & Phelan Humphrey (1975) as moMied by Parsons et al. (1984). 1987).Therefore, we wanted to investigate whether or Density, size, and biomass: Algal numbers from not these semi-sedentary medusae rely as much on 20 replicate samples from each homogenate were symbiont-derived organic products for metabolism as counted with a hemacytometer and converted to total do L. unguiculata and Mastigias sp. standing stock of algae per jellyfish. Concurrently, the To our knowledge, no study estimating the photo- diameters of 20 randomly chosen zooxanthellae were synthetic capabhties and resultant carbon budgets of measured from each jellyfish homogenate. For biomass scyphozoans has investigated these parameters as a studies, freshly collected, jellyfish (n = 4, January and function of seasonal environmental changes. Most September) were individually homogenized in filtered photosynthesis-respiration estimates are based on a seawater. Aliquots of the algal suspension were cen- single-case time period, as is the case for Linuche trifuged for 3 to 4 min in a clinical centrifuge and the jel- unguiculata (Kremer et al. 1990), Mastigias sp. lyfish tissue layer above the algal pellet was discarded. (McCloskey et al. 1994), and Cassiopea xamachana Jellyfish contam~nati.on,of the algal suspension was pe- (Vodenichar 1995).The few seasonal-based studies on riodically checked by hernacytometer counts; after the scyphozoans have only dealt with jellyfish population alga1:nematocyst ratio exceeded 95 %, 20 hemacytome- dynamics or distributions (Brewer & Feingold 1991, ter grids were counted to obtain algal density (cetlsml-l). Olesen et al. 1994) or growth (Olesen et al. 1994). With Samples for C:N analysis were prepared for isolated respect to medusan size, 2 studies on Mastigias sp. are algae as follows. Either 2.0 m1 or 3.0 m1 of the jellyfish- the only investigations that have documented the free algal cell suspension was filtered, under gentle influence of jellyfish size on photosynthesis, respira- vacuum, through a precombusted (450°C for 12 h) tion, and carbon budgets (McCloskey et al. 1994) and GF/C filter (25 mm Whatman). Each filter was subse- algal symbiont population density and regulation quently rinsed with 0.5 m1 of hstdled water, to remove (Muscatine et al. 1986). Consequently, we also wanted salts, and frozen. Four seawater-filter blanks were to determine if medusan size or seasonal environmen- included in all sample sets as controls. Prior to C:N tal change affects the carbon budgets of C. xamachana analysis, the filters were dried (45°C for 12 h) and the symbiotic with Sym biodinium microadriaticum (Freud- carbon and nitrogen masses quantified using a Control enthal 1962, Trench & Blank 1987). Equipment Corporation Elemental Analyzer (Model 240X). After accounting for seawater blanks, the algal carbon and nitrogen masses (pg cell-') were calcu- MATERIALS AND METHODS lated. The nitrogen mass was multiplied by 6.25 to obtain protein per algal cell (Muscatine et al. 1986). Collection and processing of jellyfish. Different-sized Mitotic index and growth: Tentacle snips chosen specimens of Cassiopea xamachana were collected ddy at random from freshly collected and individually from a shallow, mangrove-lined lagoon at Little Conch marked medusae (January and September) were col- Key (mile marker 62.3) in the Florida Keys (USA).All lected every hour for 24 h and frozen. Each sample was production and respiration experiments were conducted homogenized and the dividing algal cells counted in a during September 1992 and January 1993. After each hemacytometer. The mitotic index (MI) was calculated experiment, bell diameter, wet weight (ww),and dis- as described by Wilkerson et al. (1983). The phased- placement volume of each jellyfish were measured. The division formulae of Vaulot (1992) was used to calcu- jellyfish were individually homogenized in filtered sea- late the algal-specific growth (p) water (Whatman no. 5 filter), the homogenate volume determined, and sub-samples taken for various assays. Each jellyfish was assigned to 1 of 3 size classes based on where f,,, and E,,,, are the maximum and minimum bell diameters: small, medium, or large. daily fraction of dividing cells, respectively. Verde & McCloskey: Photobiology of the mangrove jellyfish 149 Jellyfish and algal biomass. Frozen aliquots of the RESULTS jellyfish homogenate were thawed and the protein content of the medusan fraction estimated by the BCA Environmental parameters Protein Assay (Pierce Chemical) using bovine serum albumen (fraction V) as the standard. Total jellyfish Average (k SD) daylength during January (11.2 * biomass
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