THE ECOLOGY OF SCYPHOZOAN JELLYFISH IN LAKE ILLAWARRA
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1 THE ECOLOGY OF SCYPHOZOAN JELLYFISH IN LAKE ILLAWARRA Kylie A. Pitt 1, Klaus Koop 2, David Rissik 3 and M.J. Kingsford 4 1 Centre for Aquatic Processes and Pollution School of Environmental and Applied Sciences Griffith University, PMB 50, Gold Coast Mail Centre, QLD New South Wales Department of Environment and Conservation PO Box A290, Sydney South, NSW Ecosystems Branch, Natural Resources Products Division Department of Infrastructure, Planning and Natural Resources GPO Box 39, Sydney NSW School of Marine Biology and Aquaculture, James Cook University, QLD 4811 ABSTRACT The scyphozoan jellyfish of Lake Illawarra are well known to most people who use Lake Illwarra for research, commercial fishing or recreation. Here we review the biology and ecology of the two most well-studied species, Catostylus mosaicus and Phyllorhiza punctata, and present preliminary results of studies that investigated their role in the trophic and nutrient dynamics of coastal lagoons. Specifically we show that C. mosaicus is a voracious predator of zooplankton and that the presence of medusae may promote production of phytoplankton either via excretion of inorganic nutrients or because grazing by C. mosaicus on zooplankton, in turn, reduces grazing by zooplankton on phytoplankton. Comparisons of rates of excretion by C. mosaicus and P. punctata show that C. mosaicus excretes substantial amounts of NH 3 which, during times of their peak biomass, may account for 8% of the NH 3 required by phytoplankton. In contrast P. punctata exhibits no net excretion of NH 3, probably because its excretory products are predominantly translocated to symbiotic zooxanthellae within its tissues. Hence these species have contrasting roles in nutrient regeneration. Current gaps in our knowledge of the ecology of these species are identified. INTRODUCTION Scyphozoan jellyfish are probably the most conspicuous animals in Lake Illawarra and anyone who has spent time working on the Lake has probably encountered dense aggregations of them. The three species seen most commonly are the rhizostomes Catostylus mosaicus (the jelly blubber ) and Phyllorhiza punctata (a dark brown medusa that has white spots on its bell) and the semaeostome Aurelia aurita (a smaller transparent species known commonly as the moon jellyfish ). Of the three, C. mosaicus is usually the most common and research has focused mostly on this species. Although A. aurita is probably the most intensively studied species of jellyfish world-wide, minimal research on this species has been undertaken in Australia. Hence this review will focus predominantly 118
2 on the ecology of C. mosaicus and P. punctata as these species have been studied the most thoroughly in Lake Illawarra. LIFE HISTORY OF JELLYFISH Jellyfish have complex life histories that incorporate both benthic and pelagic stages and sexual and asexual modes of reproduction (Fig. 1) (Pitt 2000). All three species found in the Lake have similar life histories (Kakinuma 1975; Rippingale and Kelly 1995). The stage of the life history that most people are familiar with is the medusa, which is the large, free-swimming, pelagic stage of the life history. Medusae are gonochoristic, meaning there are separate male and female animals. The gonads occur as a thin band of tissue ~5mm wide that lay above the gastric cirri (digestive tissue) on the undersides of the bell (Pitt and Kingsford 2000b). Planula larvae are produced by sexual reproduction and since the larvae are brooded by the females, the eggs are probably fertilised internally. After leaving the medusa, planulae settle onto the substratum and metamorphose into tiny, 4-tentacled polyps that are typically less than 1mm tall. We do not yet know where the polyps occur in the Lake but a laboratory study suggested that planulae can settle on a variety of surfaces (Pitt 2000), so they may occur in a variety of habitats. Figure 1. The life history of C. mosaicus (Pitt 2000) Polyps may reproduce asexually by budding or undergoing fission to form new polyps. They may also form podocysts an encysting stage thought 119
3 to be resistant to adverse environmental conditions. Under favourable conditions, one or more ephyrae (juvenile medusae) bud asexually from the polyps in a process known as strobilation. Ephyrae of C. mosaicus typically recruit between December and June but the timing of recruitment within this period is variable (Pitt and Kingsford 2003a). PATTERNS OF ABUNDANCE AND BIOMASS Abundances of jellyfish fluctuate enormously in Lake Illawarra. Counts of C. mosaicus in Lake Illawarra over a period of more than four years indicate that abundances of this species follow a seasonal pattern, with numbers being greatest between about February and July (Fig. 2). This seasonal pattern of abundance contrasts to observations made at other estuaries in NSW (such as Botany Bay) where jellyfish populations do not appear to follow a consistent seasonal pattern (Pitt and Kingsford 2000a). On rare occasions population blooms of C. mosaicus may occur. For example, during 1998, the abundance of medusae increased more than 30-fold over a period of just 6 weeks. During the bloom, the biomass of jellyfish in the lake was estimated conservatively to be 18,000 t compared to non-bloom periods where biomass was recorded to vary between approximately 2,000 and 4,000 t (Pitt and Kingsford 2003b). Although numbers of P. punctata have not been counted in Lake Illawarra, their presence or absence from the lake has been recorded. Whereas C. mosaicus may occur throughout the year, P. punctata has only been recorded occurring between uary and April (Fig. 2). Hence the population dynamics of these two species are fundamentally different. The reasons behind the contrasting population dynamics are not clear but may relate to the differences in the physiology of the two species. Fig. 2. Temporal patterns of abundance of C. mosaicus in Lake Illawarra. indicates times when P. punctata was observed Number 1500m RATES OF GROWTH The growth rates of jellyfish are difficult to measure because they have 120
4 no hard structures (such as the otoliths found in fish) that can be used to age individuals. One method that has been used to estimate growth has been to track the increase in the size (measured as bell diameter (BD)) of cohorts of medusae through time (Pitt and Kingsford 2003a). Cohort analysis of populations of C. mosaicus at Lake Illawarra indicated that it takes about 3 months for medusae to grow from approximately 20mm to 150mm BD (Pitt and Kingsford 2003a). Although growth rates have not been estimated for P. punctata, given that the medusae appear as juveniles in late spring or summer and disappear by late autumn, their growth rates are likely to be as fast, if not faster, than those observed for C. mosaicus. The complex and flexible nature of the life history, coupled with the rapid growth rate of medusae is likely to be a major factor causing numbers of jellyfish to fluctuate enormously over periods of just weeks to months. SYMBIOSES Like other cnidarians (such as corals and anemones) some species of jellyfish house microscopic, symbiotic algae (known as zooxanthellae) within their tissues. The zooxanthellae photosynthesise and the products of photosynthesis are translocated to the host jellyfish, which use them for nutrition. Indeed, some jellyfish contain such dense concentrations of zooxanthellae that they may be almost entirely autotrophic, although in reality most symbiotic species appear to still capture some zooplankton. Recently, a molecular study has indicated that both C. mosaicus and P. punctata have symbiotic zooxanthellae (R. Moore, unpubl. data). Although densities of zooxanthellae have yet to be measured, anecdotal observations suggest that P. punctata contain much greater densities of zooxanthellae than C. mosaicus and P. punctata may derive a large proportion of its nutrition from photosynthesis. This differing reliance on photosynthesis as a source of nutrition may be one reason for the contrasting population dynamics of the two species. The cold temperature of the lake during winter (~11 C) coupled with the shorter day-length may reduce the rate of photosynthesis to such an extent that the animal cannot be sustained and dies. Clearly studies of the photophysiology and feeding ecology of P. punctata are required to determine whether this hypothesis is supported. ROLE OF JELLYFISH IN THE ECOLOGY OF LAKE ILLAWARRA The role of jellyfish in the ecology of marine and estuarine systems is increasingly becoming the focus of research, both in Australia and elsewhere. Jellyfish are known to be voracious predators of zooplankton and are thus thought to influence the trophodynamics of estuaries. Less is known, however, about the role of jellyfish as a source of prey in the marine environment but recent studies indicate that gelatinous zooplankton may be a major source of food for fish (Mianzan et al. 1996). Given their sometimes-enormous biomass, excretion of inorganic nutrients by jellyfish may also have an important role in nutrient regeneration. Finally, large numbers of juvenile fish may surround the oral arms and tentacles of medusae suggesting that jellyfish may provide a type of nursery habitat for some species. Recently the roles of jellyfish in the trophic and nutrient dynamics of estuaries have been studied. 121
5 EFFECTS OF C. MOSAICUS ON THE TROPHIC ECOLOGY OF LAKE ILLAWARRA Since jellyfish prey on zooplankton and, in turn, zooplankton prey on phytoplankton, predation by jellyfish may influence abundances of multiple trophic groups. An experiment that investigated the influence of jellyfish on the trophic ecology of Lake Illawarra was conducted in Twelve mesocosms that contained approximately 3m 3 of water were deployed in the Lake and a pump was used to fill each mesocosm with water that contained natural assemblages of zooplankton and phytoplankton. Inorganic nutrients (NH 3, NO X and PO 4 ) were added to half of the mesocosms to examine whether results were similar under eutrophic conditions. Two C. mosaicus were then added to each of three mesocosms that contained nutrients and to three to which no nutrients had been added. The experiment ran for five days and each day water samples were extracted to measure concentrations of chlorophyll a (an index of the abundance of phytoplankton). At the end of the experiment a plankton net (100µm mesh) was used to sample the zooplankton in the mesocosms. Larval polychaetes were the most abundant mesozooplankton present at the end of the 5-day experiment. Regardless of whether nutrients had been added, larval polychaetes were approximately twice as abundant in the mesocosms that did not contain jellyfish compared to those that did (Fig. 3). Hence, predation by jellyfish on larval polychaetes was substantial, suggesting that jellyfish may have a major influence on abundances of zooplankton. Fig. 3. Variation in concentrations of larval polychaetes at the end of the 5-day mesocosm experiment. L = Lagoon water, N = nutrients, J = jellyfish Number m LW N J LW N LW J LW Concentrations of chlorophyll a increased rapidly in all mesocosms treated with nutrients (Fig. 4). Concentrations increased slightly in mesocosms that contained jellyfish but no nutrients and decreased in the mesocosms that contained only lagoon water. At the end of the experiment, concentrations of chlorophyll a were similar between the mesocosms treated with nutrients, regardless of the presence of jellyfish, although there was a trend for chlorophyll a to be more concentrated in the mesocosms that had been treated with nutrients and jellyfish than with nutrients only. Chlorophyll a was more concentrated in mesocosms that contained jellyfish but no nutrients than in those that contained only lagoon water. Hence concentrations of phytoplankton may increase in the presence of C. mosaicus. There are two possible processes that may have generated the observed increase in chlorophyll a. First, intensive predation on zooplankton by jellyfish may have reduced the grazing pressure of zooplankton on Fig. 4. Mean daily concentrations of chlorophyll a among treatments of the mesocosm experiment. 122
6 Concentration (ug L -1 ) Lagoon water Nutrients Jellyfish Lagoon water Nutrients Lagoon water Jellyfish Lagoon water Date sampled ( 2001) phytoplankton. Second, given that medusae did not appear to take up nutrients, excretion of waste nutrients may have stimulated phytoplankton production. It is likely that a combination of the two processes may have been responsible. CONTRIBUTIONS OF MEDUSAE TO NUTRIENT RECYCLING Excretion of inorganic nutrients by medusae is thought to provide a valuable source of regenerated nutrients for primary producers (Biggs 1977). Although any one medusa may excrete only small amounts, their large overall biomass means that the contribution of jellyfish to nutrient regeneration may be substantial. The presence of symbiotic zooxanthellae in the tissues of some species, however, may greatly reduce the amount of nutrients released by the host medusae because zooxanthellae may utilise the excretory products of their host. Hence jellyfish that contain dense concentrations of zooxanthellae may regenerate fewer nutrients than azooxanthellate forms (or those with few zooxanthellae). Although both C. mosaicus and P. punctata have symbiotic zooxanthellae, the apparent difference in the density of zooxanthellae in their tissues suggests that they may excrete different amounts of inorganic nutrients. Specifically we predicted that C. mosaicus would excrete inorganic nutrients but P. punctata may demonstrate no net excretion or even take up inorganic nutrients from the surrounding water. To test our hypothesis rates of uptake or excretion of NH 3, PO 4 and NO X (nitrate and nitrite) were measured for C. mosaicus and P. punctata. Due to the paucity of P. punctata in Lake Illawarra at the time (Feb 2003), experiments were conducted at Smiths Lake on the central coast of New South Wales. Rates of uptake or excretion were measured as changes in the nutrient concentration of the water in the containers housing the animals over a period of six hours. Measurements were made for each species and two control treatments: a water only treatment that controlled for changes in the water in the absence of jellyfish and a mucus treatment that controlled for possible changes in nutrient concentration due to the production of strings of mucus by C. mosaicus (C. mosaicus appears to 123
7 produce strings of mucus whereas P. punctata does not). Experiments were repeated twice during the day (when photosynthesis occurred) and twice at night (in the absence of photosynthesis) and were conducted under both ambient and enriched nutrient conditions. Catostylus mosaicus was found to excrete large quantities of NH 3 (Fig. 5). Medusae excreted NH 3 at a rate of µg g -1 (wet weight) hr -1 during the day and µg g -1 hr -1 during the night, under ambient nutrient conditions. In contrast, P. punctata made no net contribution of NH 3, with the flux of NH 3 being no different to the controls. Rates of excretion by C. mosaicus were similar under enriched nutrient conditions but P. punctata showed a trend where it took up small quantities of NH 3 during the day (0.123 µg g -1 hr -1 ) and excreted them during the night (0.049 µg g -1 hr -1 ). The flux of nutrients overall, however, was substantially smaller than that of C. mosaicus and not very different from that of the controls which suggests that the nutrients being excreted by P. punctata are being taken up by their symbionts (or else the rate of excretion by the medusa is similar to the rate at which the symbionts take up nutrients from the water column). Hence C. mosaicus and P. punctata appear to have contrasting contributions to the recycling of inorganic nutrients. Although the contribution of P. punctata to the regeneration of NH 3 is negligible, excretion by C. mosaicus may have a significant influence on primary production. Although care must be taken when extrapolating results to other places and times, during times of peak abundance (18,000t - Pitt and Kingsford 2003b) we estimate that excretion of NH 3 by C. mosaicus may provide 8% of the phytoplankton requirements in Lake Illawarra. The rates of excretion also equates to 11% of DIN released by sediments. Fig. 5. Mean difference between the initial and final concentration of NH 3 among treatments during the day and night under ambient and enriched nutrient conditions. C = Catostylus mosaicus, P = Phyllorhiza punctata, M = mucus control, W = water control. NH 3 µg L µg g -1 hr Ambient 4 73 Day Night Enriched C P M W Hence excretion by C. mosaicus is C P M W Treatment likely to be ecologically significant and 124
8 the presence of dense aggregations of jellyfish is likely to stimulate primary production in the water column. In contrast, although excretion by P. punctata may stimulate primary production by its symbionts, it will have negligible influence on primary production in the water column. AREAS FOR FUTURE RESEARCH Recently, our understanding of the basic biology and ecology of medusae has increased rapidly and we now recognise the importance that jellyfish have to the trophodynamics and nutrient cycling of Lake Illawarra. Despite this there are several key areas that require investigation. What eats jellyfish? A comprehensive understanding of the role of a species in the trophodynamics of a system requires knowledge of both what the animal eats and what eats it. Although we know that jellyfish are voracious predators of zooplankton we know very little about what eats jellyfish in estuaries in NSW. In other places jellyfish are preyed on by numerous organisms including fish (Ates 1988), turtles (den Hartog and van Nierop 1984; Purcell and Arai 2001) and birds (Ates 1991). Although the caloric content of medusae may be less than that of other sources of prey (Arai 1988), jellyfish are generally abundant and slow moving and so the reduced energy required to find and capture them, relative to other types of food, may result in a net energetic gain for the predator. Identification of the predators of jellyfish and their rates of predation are required to further our understanding of the role of jellyfish in the ecology of Lake Illawarra. Factors influencing abundances of medusae Extreme and rapid fluctuations in numbers are a common characteristic of jellyfish populations and population blooms occur relatively frequently. The number of medusae produced is likely to be a function of the number and fecundity of the polyps and rates of survivorship of the ephyrae. As yet we have almost no information about the ecology of the benthic and ephyral stages of the life history. This is true, not only of Australian species, but also of jellyfish generally. A combination of manipulative lab-based studies that examine the processes governing the timing and magnitude of strobilation and field-based studies that examine recruitment of polyps and their survivorship and fecundity are required. CONCLUSIONS Jellyfish are an integral part of the ecology of Lake Illawarra and, at times, they probably represent the greatest biomass of any animal occurring in the Lake. As a likely consequence of their different rates of photosynthesis, their contribution to nutrient regeneration appears to differ, with P. punctata excreting negligible quantities of NH 3 whereas excretion by C. mosaiucs is substantial. Excretion, coupled with voracious predation on zooplankton suggests that C. mosaicus in particular, has a substantial influence on the nutrient and trophodynamics of Lake Illawarra. ACKNOWLEDGEMENTS We would like to thank J Browne, J Grayson, D Annese and B Clynick for assistance with fieldwork and J Browne, J Grayson and S Wellman for undertaking laboratory analyses. Our research has been supported by an Australian Research Council Strategic 125
9 Partnership - Industry Training and Research grant awarded to M Kingsford, K Pitt, K Koop and D Rissik. REFERENCES Arai MN (1988) Interactions of fish and pelagic coelenterates. Canadian Journal of Zoology 66: Ates RML (1988) Medusivorous fishes, a review. Zoologische Mededelingen 62: Ates RML (1991) Predation on Cnidaria by vertebrates other than fishes. Hydrobiologia 216/217: Biggs D (1977) Respiration and ammonium excretion by open ocean gelatinous zooplankton. Limnology and Oceanography 22: den Hartog JC, van Nierop MM (1984) A study on the gut contents of six leathery turtles Dermochelys coriacea (Linnaeus) (Reptilia: Testudines: Dermochelyidae) from British waters and from the Netherlands. Zoologische Verhandelingen 209: 3-36 Kakinuma Y (1975) An experimental study of the life history and organ differentiation of "Aurelia aurita" Lamarck. Bulletin of the Marine Biological Station of Asamushi 15: Mianzan H, Mari N, Prenski B, Sanchez F (1996) Fish predation on neritic ctenophores from the Argentine continental shelf: A neglected food resource? Fisheries Research 27: Pitt KA (2000) Life history and settlement preferences of the edible jellyfish "Catostylus mosaicus" (Scyphozoa: Rhizostomeae). Marine Biology 136: Pitt KA, Kingsford MJ (2000a) Geographic separation of stocks of the edible jellyfish "Catostylus mosaicus" (Rhizostomeae) in New South Wales, Australia. Marine Ecology Progress Series 136: Pitt KA, Kingsford MJ (2000b) Reproductive biology of the edible jellyfish "Catostylus mosaicus" (Rhizostomeae). Marine Biology 137: Pitt KA, Kingsford MJ (2003a) Temporal and spatial variation in recruitment and growth of medusae of the jellyfish, Catostylus mosaicus (Scyphozoa: Rhizostomeae). Marine and Freshwater Research 54: Pitt KA, Kingsford MJ (2003b) Temporal variation in the virgin biomass of the edible jellyfish, Catostylus mosaicus (Scyphozoa, Rhizostomeae). Fisheries Research 63: Purcell JE, Arai MN (2001) Interactions of pelagic cnidarians and ctenophores with fish: a review. Hydrobiologia 451: Rippingale RJ, Kelly SJ (1995) Reproduction and Survival of "Phyllorhiza punctata" (Cnidaria: Rhizostomeae) in a Seasonally Fluctuating Salinity Regime in Western Australia. Marine and Freshwater Research 46:
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