MARINE ECOLOGY PROGRESS SERIES Vol. 180: 187-196,1999 Published May 3 Mar Ecol Prog Ser

Temperature, salinity and food effects on and abundance of the scyphozoan quinquecirrha

Jennifer E. ~urcell'**,Jacques R. white1,**,David A. Nemaziel, David A. wright2

'University of Maryland Center for Environmental Science (UMCES). Horn Point Laboratory. PO Box 775, Cambridge, Maryland 21613, USA 2UMCES, Chesapeake Biological Laboratory. PO Box 38. Solomons, Maryland 20688-0038, USA

ABSTRACT: Outbreaks of are reported worldwide, yet the environmental factors that control the sizes of jellyfish populations are not well understood. The scyphomedusan Chrysaora quinquecir- rha occurs in the mesohaline portion of Chesapeake Bay each summer. Population sizes of the medusae show dramatic annual variations that are correlated with salinity and temperature. We measured the total numbers of ephyrae and polyps produced by benthic polyps of C. quinquecirrha in laboratory experiments lasting 42 d, and found that temperature (15. 20, 25°C) was not a statistically significant factor at low salinities (5 to 20P:m); however, ephyra production increased significantly with increasing temperature at high salinities (20 to 35%). Conversely, each 5°C decrease in temperature delayed stro- bilation (ephyra production) by about 1 wk. Salinity significantly affected the numbers of ephyrae and polyps produced in all experiments. Ephyra and polyp production was lower at both low (

KEY WORDS: . . Medusa . Scyphistoma . Temperature . Salinity . Zooplankton . Production . Strobllation . Environmental factors . Asexual reproduction

INTRODUCTION economic losses due to reduction of recreational activ- ities and fisheries. High biomasses of large jellyfish are noticed period- When jellyfish occur in large numbers, their preda- ically in estuaries and partly enclosed marine waters tion can have substantial effects on the zooplankton worldwide (e.g. Yasuda 1970, Moller 1979, Cargo & and ichthyoplankton populations. Because the pre- King 1990, Purcell et al. 1999). There has been consid- dominant summertime scyphomedusae in Chesapeake erable interest as to the causes and effects of conspicu- Bay, , are voracious con- ous jellyfish outbreaks, because coastal areas are sumers of zooplankton and ichthyoplankton (e.g. Pur- heavily used for human activities, and jellyfish cause cell 1992, Cowan & Houde 1993, Purcell et al. 1994a, concerns about potential human health hazards and b), they may be detrimental to estuarine fish popula- tions. Food web analyses suggest that, due to their high trophic positions and high abundance, this gelati- 'E-mail: [email protected] nous species is extremely important to plankton "Present address: People for Puget Sound, 1402 3rd Avenue, dynamics during the summer in Chesapeake Bay Suite 1200, Seattle, Washington 98101, USA (Baird & Ulanowicz 1989).

O Inter-Research 1999 Resale of full article not permitted 188 Mar Ecol Prog Ser

The life cycles of coastal scyphomedusae include a Salinity decreases throughout the spring in Che- benthic stage (scyphistoma) that lives attached to hard sapeake Bay (Calder 1974, Cargo & King 1990), but surfaces and a scvimmlng stage, the medusa. Scyphis- the effect of salinity on strobilation in Chrysaora tomae of Chrysaora quinquecirrha reproduce asexu- quinquecir-rha is unknown. Salinity has not been ally in 2 ways; polyps can be formed by budding, and 1 identified as a likely trigger for strobilation in other to 2 mm medusae (ephyrae) are released by segmenta- scyphomedusae (Spangenberg 1968, Hernroth & tion called strobilation (Cargo & Rabenold 1980). The Grondahl 1985); however, salinity and iodide concen- scyphistomae spend the cold winter months in a dor- trations are linearly correlated (Luther & Cole 1988), mant state (cyst) and then excyst to form polyps, which and iodide is required for strobilation by scyphis- produce ephyrae when spring water temperatures tomae, which synthesize thyroxine and related reach 17°C (Cargo & Schultz 1967). Ephyrae are bud- compounds (Spangenberg 1967, 1968, 197 l, Black & ded from scyphistomae mostly in June, but continue Webb 1973, Silverstone et al. 1978). Both Aurelia through September (Calder 1974). The medusa stage aurita and C. quinquecirrha showed increased strobi- becomes sexually reproductive at about 2 cnl diameter 1ati.on with increasing iodide concentrations (1 to (Purcell unpubl. data). Planula larvae from fertilized 100 mM, Spangenberg 1967, and 300 to 600 nM, eggs settle to become the benthic scyphistomae. The Black & Webb 1973). Threshold concentrations of medusae die in the autumn, probably in response to iodide necessary to stimulate strobilation were not falling water temperatures (Gatz et al. 1973), but the determined. Iodine concentrations in Chesapeake scyphistomae may survive for more than 1 yr (Cargo & Bay ranged from 470 nM at 35% to 70 nM at 5'Xo Schultz 1967). (Luther & Cole 1988). Iodide concentration was Population size of the swimming medusa stage in 200 nM in a tributary of Chesapeake Bay where a.ny given year is determined by the abundance of salinity was 19 to 21% (Black & Webb 1973). There- scyphistomae, the production of ephyrae, and survival fore, nanomolar levels of iodide sufficient to stimulate of the ephyrae. Only the studies of Hernroth & Gron- strobilation in C. quinquecirrha are present in meso- dahl (1983, 1985) and Grondahl & Hernroth (1987) haline tributary waters of Chesapeake Bay. examine environmental factors in situ (temperature, There has been speculation that eutrophication of light, and a nudibranch predator of the polyps) that coastal waters has lead to increased populations of jel- may affect ephyra abundance. Numerous factors (tem- lyfish (Parsons et al. 1977). The abundance of food is perature, light, iodide and thyroxine, bacterial exu- undoubtedly an important factor in determining the dates, and the presence of zooxanthellae) have been population sizes of medusae. Thiel (1962) first showed found in laboratory experiments to initiate strobilation the effects of food concentration on strobilation in in several species of scyphomedusae (Spangenberg Aurelia aurita. The number of segments on scyphis- 1967, 1968, Loeb 1972, Hofmann et al. 1978, 1996). For tomae increased with increased food (Spangenberg Chrysaora quinquecirrha in Chesapeake Bay, strobila- 1967, 1968). The greatest numbers of segments in A. tion occurs in spring when 3 environmental factors aurita strobilae in situ occurred in autumn after the (light, temperature, and food) are increasing, and peak zooplankton biomass (Hernroth & Grondahl salinity is decreasing, so it is difficult to distinguish 1983). Chen et al. (1985) showed increased strobilation which factors are most important in sjtu. Loeb (1972) with increased food in Rhopilema esculenta in the lab- concluded that several weeks of chilling ('pre-condi- oratory. tioning') and subsequent warming of the polyps by Here we report laboratory experiments to test the about 6°C was necessary for strobilation. effects of temperature, salinity, and food levels on the Some cnidarians occur in low salinity waters, but production of Chrysaora quinquecirrha ephyrae and species diversity decreases sharply with decreased polyps Dramatic differences in the numbers and distri- salin~ty (Dumont 1994). Chrysaora quinquecirrha is butions of medusae in Chesapeake Bay in July 1995 unusual among cnidarians because it tolerates salinl- and 1996 are discussed relative to differences in tem- ties as low as 5% and thrives at salinities of 10 to 12%. perature, salinity, and zooplankton densities. The scyphistomae are not found in Chesapeake Bay where salinities are less than 7%0,and thrive at salini- ties of 10 to 25'::n1; surprisingly, the polyps are not found METHODS AND MATERIALS in bay waters above 25% (Cargo & Schultz 1966, 1967). Thus, the populations of C. quinquecirrha in the Laboratory experiments. Oyster shells with polyps mesohaline portion of Chesapeake Bay may be limited of Chrysaora quinquecirrha were collected with a by both low (<5','&7)and high (>257;w) sal.inities, which dredge during April 1991 and 1992, from a tributary is intriguing in terms of their ecology and their physio- of the Choptank River, where water temperature was logy (see Wright & Purcell 1997). 13°C and salinity was 11?&, and transported to the Purcell et al. Effects on scyphomedusa asexual reproduction and abundance 189

Horn Point Laboratory on the Choptank River, a tribu- The polyps were fed 3 or 4 times per week in all tary of Chesapeake Bay in Maryland. At the time of experiments; however, the foods offered to polyps dif- collection, polyps had experienced the natural sea- fered among experiments. Expt 1 was the low food sonal environmental conditions, which included sev- treatment, in which polyps were fed only cultured eral weeks of chilling, which is required before strobi- copepod nauplii (Acartia tonsa). Prey densities were lation will occur (Loeb 1972). The oyster shells with estimated by counting subsamples using a dissecting polyps were maintained in 20 1 buckets of aerated microscope. In Expt 2, polyps were fed a combination estuary water in an environmental chamber at 12OC of Artemia salina nauplii and copepod nauplii. Expt 3 and 20%h before the experiments. Polyps were fed was the high food treatment, in which polyps were fed Artemia salina nauplii and water was replaced every mixed natural zooplankton that passed through a 3 to 4 d. No strobilation occurred under those con- 200 p111 Nitex mesh. The concentration of zooplankton ditions. in the petri dishes was measured with a Coulter parti- Treatment water used in the experiments was col- cle counter. lected from Indian River inlet, Delaware (320/0,)),and The raw data (total ephyrae and total polyps pro- the salinity increased by adding Instant Ocean sea salt, duced) from each experiment were tested for devia- or decreased by mixing with deionized water. All tions from normal distributions before statistical analy- water was filtered before use in experiments with a sis. All data sets required logarithmic transformation. combination of glass fiber pre-filters and 0.22 pm The log transformed data were analyzed in a com- Nucleopore brand MF filters. pletely factorial design analysis of variance (ANOVA) Three separate experiments were conducted to procedure. The hypothesis that treatments within an examine the combined effects of temperature and experiment were significantly different (p < 0.05) was salinity on ephgra and polyp production. Each expen- satisfied in all experiments except for polyp production ment comprised a matrix of different temperature and in Expt 3. salinity combinations, with each condition having Field sampling. Sampling was conducted as part of 4 replicate dishes. Expt 1 (June to July 1991) was the NSF sponsored LMER (Land Margin Ecosystem designed to examine the combined effects of tempera- Research) project in Chesapeake Bay called TIES tures typical of spring and summer (15, 20, 25"C), and (Trophic Interactions in Estuarine Systems). Bay wide salinities characteristic of oligo- to mesohaline regions sampling occurred during 19 to 29 July 1995 and 16 to of Chesapeake Bay (5, 10, 15, 20%").Expt 2 (September 26 July 1996. Temperature and salinity were measured to October 1991) was run at 1 temperature (25°C) to with a CTD at 30 to 40 stations during each cruise. At specifically determine the minimum salinity (5, 7, 9, each station, zooplankton and jellyfish samples were 11%o) necessary for ephyra production. Expt 3 (July to collected with a 1 m2 Tucker Trawl fitted with 280 pm August 1992) tested the combined effects of tempera- mesh nets and a General Oceanics flowmeter. Samples ture (15, 20, 25°C) and moderate to high salinities (20, from oblique hauls from the pycnocline to the surface 25, 30, 35%0) characteristic of lower-bay and ocean were poured through a collander that retained waters. Chrysaora quinquecirrha medusae, which were rinsed Polyps were prepared for experimental treatments and counted. Zooplankton from those samples were by cutting the oyster shells into sections bearing 3 to preserved in ethanol. In 1996, no medusae were 16 polyps each. This method subjected the polyps to caught in the Tucker Trawl, so we counted medusae less stress than removal from the shell. The shell from a midwater trawl, with a nominal mo.uth area of pieces were cleaned of other attached organisms, 8 m2 and a cod end mesh size of 6 mm, which was affixed to the bottonl of plastic 375 m1 petri dishes towed obliquely from bottom to surface for 20 min. with either natural bees wax or non-toxic modeling Densities of medusae were estimated using the calcu- clay, and covered with 200 m1 of treatment solution. lated voluine of water filtered during these trawls, The polyps were acclimated to experimental salinities which was approximately 38000 m3, based on net and temperatures by changing both parameters mouth size, ship speed, and tow duration. In 1995, zoo- simultaneously over increments of 5°C and 5%" daily plankton were counted (by use of a dissecting micro- until experimental conditions were attained The scope) from 3 subsamples taken with a 5 m1 Hensen treatments were maintained at experimental tempera- stempel pipette from each of the Tucker Trawl sam- tures in walk-in incubators with dim fluorescent lights ples, which were brought to 2 l volume and agitated on a 12 h light : 12 h dark cycle. The numbers of liv- before subsampling. In 1996, zooplankton were ing polyps and ephyrae were counted daily, and counted in the same manner from samples taken at 1 m water in the dishes replaced and uneaten zooplankton depth with a diaphragm pump, which ran for 5 min at removed every other day. All experiments were run 20 1 min-l, filtered through a 200 pm sieve, and pre- for 42 d. served. 190 Mar Ecol Prog Ser 180: 187-196, 1999

Fig. 1, Chrysaora quinquecirrha. Total numbers of ephyrae produced per polyp (initial num- bers) in Expt 1 (5 to 20%) and in Expt 3 (20 to 35%~)at 3 temperatures (15, 20, and 25'C) dur- ing 42 d. Initial numbers of polyps are given above each bar

at the high temperature (25OC), about 1 wk later at 20°C and another week later at 15OC in both Expts 1 and 3 (Fig. 3). There Experiment 1 , Ex eriment 3 >.Q' was no apparent effect of temperature on - 0.9 20° ¤ 12 production of new polyps (Figs. 4 & 5), and 0.8 temperature effects were not significant 0.7 1 23 aye (Table 1).

Effects of salinity

Ephyra production was maximum at 20%0 in Expts 1 and 3, showing reduced strobilation at both lower and higher salin- ities (Figs. 1 & 2). No ephyrae were pro- duced at 5%0in any experiment (Figs. 1, 2 & 6). The lowest salinities in which sub- stantial strobilation occurred were 10 to 11 %o in Expts 1 and 2, respectively (Figs. 1, 2 & 6). Similarly, new polyp production was low at salinities below 10 %o and above

5 10 15 20 25 30 20%o(Figs. 4, 5 & 6), Effects of salinity on Salinity Salinity ephyra and polyp production were signifi- cant in all experiments (Table 1).

Experiment 1 RESULTS Q. o,5 I

Laboratory experiments

Effects of temperature

There were fewer ephyrae produced per polyp at 15OC in both Expts 1 and 3 - (Figs. 1 & 2), although temperature was a 5 10 15 20 20 25 30 35 significant factor only in Expt 3 (Table 1). Salinity Salinity The main effect of temperature was in the onset of strobilation, which occurred first

Fig. 2. Chrysaora quinquecirrha. Same data as in Fig. 1 (total numbers of ephyrae pro- duced per polyp), but with all temperatures combined (15, 20, 25OC), and all salinities combined, in Expt 1 (5 to 20%) and in Expt 3 - (20 to 35%). Initial numbers of polyps are 15 20 25 15 20 25 given above each bar Temperature Temperature Purcell et a1 Effects on scyphomedusa asexual reproduction and abundance 191

Table 1. List of experiment conditions, variables, effects, F-ratios and p resulted in markedly lower salinities (about values from Factorial ANOVA. Experiment = overall effects; SAL = 2% baywide) in July 1996 than in 1995, and effects of salinity; TEMP = effects of temperature; and SAL'TEMP = water temperatures also were lower (about interaction between sallnity and temperature 2°C baywide) in July 1996 than in 1995. Zooplankton densities also were lower in Experiment/ Varlable Effect conditions July 1996 than in 1995. At stations where Chrysaora quinquecirrha medusae were 1. 5-20%. Ephyrae Experiment found in the Tucker Trawl samples, medusa 15-25°C SAL densities ranged from 1 to 9 per 100 m3 TEMP in 1995; however, no specimens were col- SAL'TEMP Polyps Experiment lected in identical sampling in July 1996. SAL Medusa densities estimated from midwater TEMP trawl sampling in 1996 were 2 orders of SAL'TEMP magnitude lower (0.01 to 0.04 per 100 m3) 2.5-1 l "/, Ephyrae Experiment than in 1995. Also, the distributions of 25°C SAL medusae were different in the 2 years, with Polyps Experiment medusae being mainly north of the Poto- SAL moc River in 1995, but mainly south of the 3. 20-35% Ephyrae Experiment Potomoc River in 1996 (Fig. 7). The stations 15-25°C SAL TEMP where medusae were collected differed in SAL'TEMP temperature (about 3.5"C) and zooplankton Polyps Experiment densities (about 2-fold) between years, but SAL did not differ in salinity (Table 2), because TEMP the medusa population was shifted south SAL'TEMP towards the bay mouth where salinities were higher.

Effects of food Experiment 1 2 0.8 - The effects of food were tested by comparing ephyra - 2001m -m- 15C --~--zoc-25~1 and polyp production at 20%0 in Expts 1 and 3. In Expt 1, the polyps were given only cultured copepod nauplii (0.2 prey ml-'), which yielded a low rate of ephyra production (0.3 to 0.9 ephyrae polyp-') (Figs. 1 3 0.4 & 2). In Expt 3, the polyps were fed with natural zoo- plankton S200 pm (4.3 to 4.4 prey ml-'), and ephyra a, 02- production was high (1 to 13 ephyrae polyp-') (Figs. 1 I & 2). In contrast, similar numbers of new polyps were produced in both experiments (0.7 to 1.7 polyps 123456 polyp-' in Expt 1, and 0.5 to 0.9 in Expt 3) (Figs. 4 & 5) , P!ment 3 >. 8 20 O/, Statistical comparisions between Expts 1 and 3 showed that ephyra production differed significantly between Lg 51 a, food treatments (ANOVA, p < 0.001), but that new U 4- polyp production did not differ significantly with food 0a, I level. U3 3. i m Field sampling

Sahnity, temperature, and zooplankton and medusa 123456 densities were measured in the surface layer of Week Chesapeake Bay in July 1995 and 1996 (Table 2). Fig. 3. Chrysaora quinquecirrha. Weekly totals of the num- Freshwater inputs to the bay were about 25 % bers of ephyrae produced per polyp (initial numbers) in Expt 1 the average in lgg51 but about 25% and in Expt 3 at 20% salinity for 3 different temperatures the average in 1996 (Boynton et al. 1997). This (15, 20, ;nd 25°C) 192 Mar Ecol Prog Ser 180. 1.87-196, 1999

Flg 4 Chrysaora qu~nqucnrrhaTotal numbers of polyps produced per polyp (init~alnumbers) In Expt 1 (5 to 20°.,) and in Expt 3 (20 to 35"r~o) at 3 temperatures (15. 20, and 25°C) durlng 42 d Initial numbers of polyps are given above each bar

15"C, which is below the initiation tem- perature reported previously by Cargo & Schultz (1967), Cones & Haven (1969), Expenrnenfl a,1.8 - and Calder (1974). Temperature did affect 2 1.6. 'Ooc the timing of strobilation in our experi- ments; each 5°C reduction in temperature delayed peak production by about 1 wk. Cool environmental temperatures also delay the appearance of C. quinquecirrha medusae in Chesapeake Bay (Cargo & King 1990). Changing temperatures may be the stimulus that initiates strobilation for

Experiment3 - - most scyphomedusan species, including Chrysaora quinquecirrha, Cyanea capil- lata, and Cotylorhlza tuberculata (Cargo 1.4 & Schultz 1967, Calder 1974, Grondahl & l Hernroth 1987, Brewer & Feingold 1991, 18 70 kkinger 1992). However, for Aurelia au- rita, Hernroth & Grondahl (1985) believed that temperature change did not trigger strobilation because spring warming only occurred in the surface layer above the 5 10 15 20 20 25 30 35 Salinity Salinity

DISCUSSION

Laboratory experiments

Effects of temperature

In the low salinity (5 to 20%) experi- ments, temperature did not significantly 5 10 15 20 20 25 30 35 affect the total numbers of Chrysaora Salinity Salinity quinquecirrha ephyrae or polyps pro- duced. Strobilatlon occurred even at

Fig. 5. Chrysaora quinquecirrha. Same data as in Fig. 4 (total numbers of polyps produced per polyp), but with all temperatures com- bined (1.5, 20, 25"C), and all, sal~nitlescom- bined, in. Expt 1 (5 to 20°L) and in Expt 3 (20 U" to 35"m). Initial numbers of polyps are given 15 20 25 15 20 25 above each bar Temperature Temperature Purcell et al.: Effects on scyphomedusa asexual reproduction and abundance 193

Whether the higher strobilation at salinities >10Y6, relative to that at salinities ~10%~is directly related to salinity or corresponding iodide levels is not known. Luther & Cole (1988)showed that iodide concentration was directly related to salinity; in our experiments, iodide would have ranged from 67 nM at 5";" salinity to 470 nM at 35'1.k salinity. Scyphistomae of Chrysaora quinquecirrha accumulated iodide against a concen- tration gradient (Black & Webb 1973),and the rate of accumulation increased with increasing temperatures (Olmon & Webb 1974). Our results on ephyra produc- Experiment2 tion at low salinities (Expts 1 and 2) are consistent with 2.a ia -8 16 250C the idea that increasing iodide availability and accu- mulation by the scyphistomae would increase strobila- tion, with a threshold occurring at about 10%~salinity (200 nM iodide). The fact that production of both polyps and ephyrae of C, quinquecirrha was low at low salinities suggests that ionic regulation may be com- promised at low salinities (Wright & Purcell 1997).Low

5 7 9 11 salinities might be expected to be stressful to C. quin- Salinity quecirrha because few cnidarian species inhabit oligo- haline waters (Dumont 1994). Fig. 6. Chrysaora quinquecirrha. Total numbers of ephyrae More surprising is the low production of Chrysaora and polyps produced per polyp num- qUlnquecjrrha ephyrae and polyps at high sallnities bers) in Expt 2 (5 to 11%) during 42 d. Initial numbers of polyps are given above each bar (25 to 35%"),to which most cnidarian species are adapted. Cones & Haven (1969)stated that ephyrae were not produced at 35 and 40%0and that the polyps polyps, and strobilating polyps occurred in autumn encysted above 35.5%0. Polyps were absent from through spring. Seasonal salinity changes were ~2%" areas where salinities were 19 to 25x0, and they and were thought unlikely to be the trigger. Therefore, encysted or died in experiments run at 25, 30, and they concluded that changing light conditions must be 35%~(Cargo & Schultz 1966). Our results (Expt 3) the stimulus triggering strobilation. The effects of light showed that few ephyrae and polyps were produced on strobilation have been studied only for A. aurita, at salinities above 20Y~.Because high iodide concen- and those experimental results are not definitive trations would occur at these high salinities, which (reviewed in Spangenberg 1968). Light conditions should have stimulated higher strobilation (Black & were consistent throughout all of our experiments and Webb 1973),iodide probably was not responsible for could not be responsible for any of the observed, the reduced asexual reproduction of C. quinquecirrha differences. at high salinities. The observed low asexual reproduction at high salinities by Chr}~saoraquinquecirrha polyps from Effects of salinity Chesapeake Bay is puzzling because this species also occurs in high salinity coastal waters along the U.S. The results of the production experi- Atlantic and Gulf Coasts (Mayer 1910, Kramp 1961). ments were consistent with field observa- tions that medusae and polyps are found Table 2. Environmental parameters at stations where Chrysaora quinque- in waters of >?Yw and 125%0salinities cirrha medusae were collected in July 1995 and 1996. TT = Tucker Trawl (Cargo & Schultz 1966, 1967). Specifi- samples; MT = midwater trawl samples. Numbers are means + 1 SD cally, our experiments showed that both ephyra and polyp production were low at 1995 1996 salinities of 5, 30, and 35%0.Salinity, or a - CO-varying factor such as iodine, can No. of stations with medusae 18 of 46 TT 0 of 30 TT, l7 of 30 MT affect medusa population size by affect- Range (ON latitude) 37.5 to 39.00 37.33 to 38.67 Temperature ("C) 29.1 t 0.4 25.5 t 1 14 ing the numbers of ephyrae and polyps Salinity 14.1 + 1.7 14.4 +53 produced. Asexual reproduction abruptly ~~~~l~~k~~~(no, 2251.8 + 2027.4 875.7 + 626.4 declined at salinities < 10 %o. 194 Mar Ecol Prog Ser 180: 187-196, 1999

are milky white without dark pigmentation. Thus, we conclude that there is a local population adapted to the mid-salinity range found in the mesohaline portion of Chesapeake Bay. Whether this 'mid-salinity' (white) form is genetically distinct from the 'high-salinity' (red) form has not been determined; however, both red and white medusae were found in 10 of 17 trawl samples in July 1996. Presumably, the red medusae are carried up the bay in high salinity bottom waters, and the white medusae are carried down the bay in the low salinity surface layer, which is the typical summertime circula- tion pattern in Chesapeake Bay.

Effects of food

In our experiments, ephyra production was greatly increased when polyps were provided with more food. Increased prey abundance in situ could cause a rapid increase in the population size of medusae. Numbers Hin 0.01lm3 $ of ephyrae similar to those in the high food treatment Max 0.09lm3 (1 to 13) were produced per polyp in situ (Calder 1974). By contrast, we saw no increase in polyp numbers with increased food availability. Polyp production would not be as rapid a response to trophic conditions as ephyra production. Therefore, asexual production of polyps may be a long-term strategy to maintain populations, and ephyra production may be more flexible, enabling the population to respond quickly to changing trophic conditions. Recent outbreaks of gelatinous zooplankton around the world have led to speculation that human activities may have changed the trophic structure of coastal waters, causing jellyfish populations to increase (Legovik 1987).For example, Newel1 (1988) documents the dramatic decline of oysters Crassostrea virginica in Chesapeake Bay since about 1880, and he argues that the phytoplankton they would have consumed may now go instead to zooplankton grazers, thus providing additional food to zooplanktivores such as medusae, and consequently enlarging their populations. A .- model by Ulanowicz & Tuttle (1992) predicts an 89% Min 0.011100m3 reduction in gelatinous zooplankton if oysters were Max 0.04/100m3 1 restored to their former abundance in Chesapeake Ray. Reductions of zooplanktivorous fish populations due to commercial harvesting also could result in enhanced zooplankton foods for jellyfish (Mills 1995, Fig. 7. Chrysaora qulnquecirrha. Densities of medusae Purcell et al. 1999). Increased nutrients from sewage in Chesapeake Bay in July 1995 (numbers m-3) and 1996 effluents or fertilizers in estuarine or coastal waters (numbers 100 m-3). (0) Stations sampled may change plankton food webs in ways such that jellyfish populations increase (Parsons et al. 1977); C. quinquecirrha medusae from those waters are however, direct evidence connecting human effects on marked with reddish brown stripes on the swimming estuarine systems with changes in jellyfish populations bell and down the oral arms (Mayer 1910), unlike is lacking. For example, no data on the abundances of medusae from the mesohaline Chesapeake Bay, which Chrysaora quinquecirrha medusae exist before 1960, a Purcell et al.. Effects on scyphomedus a asexual reproduction and abundance 195

time by which Chesapeake Bay was already badly scyphistomae by a nudibranch in 1 year. In the north- impacted, and medusa numbers have not generally ern Adriatic Sea, outbreaks of are increased since then (Cargo & King 1990). The lack of initiated by enhaced water advection from the south, historical data on environmental variables, nutrients, bringing the medusae into the northern region, where and plankton populations prevents adequate evalua- warmer than normal winters and water temperatures tion of possible effects of fisheries and eutrophication sustain a continuous population of the medusae, which on jellyfish population sizes. ususally cannot overwinter there (Purcell et al. 1999). Cargo & King (1990) found that flow from the Susque- hanna River (January through June), and water tem- Field sampling perature (May) correlated best with July to August medusa numbers at Solomons, Maryland. Lu et al. The dramatic differences in the numbers of (1989) showed a similar pattern for the edible scypho- Chrysaora quinquecirrha medusae during July 1995 zoan Rhopilema esculenta, for which strobilation and and 1996 in Chesapeake Bay are consistent with our survival decreased below 14%0 and above 20% sal- experimental results. Medusae were 2 orders of mag- inity, and dramatic reductions of medusae in situ were nitude more abundant in 1995, when all 3 factors that linked to high river flow. Here, we have shown that we found to increase ephyra production (salinity, tem- environmental variables (temperature, salinity, and perature, and food) were greater than in 1996. The fact food) affect the production of ephyrae in laboratory that medusae occurred at the same salinities in 1995 experiments and population size in situ. Therefore, and 1996, but at temperatures that differed by 3.5"C, evidence is accumulating that a combination of hydro- suggests that salinity constrained medusa distribution graphic and environmental factors often are responsi- but that temperature did not. ble for medusa population outbreaks. It is more difficult to evaluate the relative importance of zooplankton abundance on population size of Chrysaora quinquecirrha in situ because of trophic Acknowledgements. This research was funded by grants interactions throughout the food web. Production in from NSF (OCE-9019404 and OCE- 9633607) and from the University of Maryland Sea Grant College (UMSGC)(R/P-98- the Chesapeake system is strongly linked to nutrient P/D) to J.E.P. We thank Dr D. Meritt for use of the oyster inputs brought by springtime freshwater flow from the dredge, Dr D. Jacobs for statistical advice, and REU student B. Susquehanna River, which supplies 60% of the fresh- Byrne (funded by NSF grant OCE-930001 to the UMSGC) for water and 80 % of the nitrogen to the upper bay (Mal- her valuable assistance. Logistical support and environmental data were supplied by the TIES Group at UMCES (NSF grant one et al. 1988, Harding & Perry 1997). In years of high DEB-9412113). We especially thank Dr E. D. Houde's group river flow, like 1996, allochthanous nutrient input is for assistance in the field. Dr M. R. Roman's group for use of high, leading to high phytoplankton and zooplankton 1996 zooplankton data, and C. Pacey and M. Kiladis for field biomasses, as seen in April 1996 (Boynton et al. 1997). data analysis and figure preparation. UMCES Contribution By summer, the system is strongly stratified, and No. 3121. phytoplankton production depends on nutrient recy- cling above the pycnocline. 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Editonal responsib~llty:Otto Kinne (Editor), Submitted: July 3, 1998; Accepted: November 3, 1998 Oldendorf/Luhe, Germany Proofs received from author(s): Apnl6, 1999