The Influence of Zooxanthellate and Non-zooxanthellate Jellyfish on Nutrient Cycling and Trophodynamics

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Pitt, Kylie
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Welsh, David
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The appearance and disappearance of large numbers of medusae is a common characteristic of jellyfish populations. Blooms of jellyfish can attain very large biomasses that cover wide areas and can be short-lived, after which time the population may crash rapidly. The sheer biomass of jellyfish during bloom periods and the ‘boom and bust’ population dynamics are likely to have considerable impacts on the surrounding ecosystem. Some species of jellyfish contain symbiotic dinoflagellates called zooxanthellae. Zooxanthellae are able to assimilate nutrients from the surrounding water and transfer photosynthetic products to the host jellyfish. Zooxanthellate jellyfish are likely to acquire and recycle nutrients very differently to non-zooxanthellate species, and are therefore likely to have contrasting influences on nutrient cycling and trophodynamics. However, there are large gaps in our understanding of these processes. This thesis directly compares the role of zooxanthellate and non-zooxanthellate jellyfish on nutrient cycles and trophodynamics, by investigating these processes in zooxanthellate jellyfish, Cassiopea sp. and Phyllorhiza punctata, and the non-zooxanthellate jellyfish, Catostylus mosaicus. An important step in understanding the influence of jellyfish on ecosystem processes is to determine how nutrients are cycled within individual medusae. To do this, the exchanges of nutrients with the surrounding water were compared between zooxanthellate and non-zooxanthellate jellyfish. Experiments were done to compare the net exchanges (uptake and excretion) of organic and inorganic nitrogen and phosphorus with the surrounding water. Changes in nutrient concentrations were measured in tubs housing zooxanthellate Cassiopea sp., non-zooxanthellate C. mosaicus, and water control (no jellyfish). Experiments were repeated during the day, when photosynthesis and respiration could occur, and at night when only respiration could occur. Organic nutrients were found to comprise 25 - 43 % of the total excretion by non-zooxanthellate jellyfish. Organic nutrient excretion by blooms (506 t km-2) of non-zooxanthellate jellyfish were estimated to potentially support 62 – 120 mg C m-2 of bacterial production per day. In addition, excretion of inorganic nutrients by blooms of non-zooxanthellate jellyfish were estimated to potentially support 201- 423 mg C m-2 of primary production per day. In contrast, zooxanthellate jellyfish excreted minimal amounts of inorganic and organic nutrients or took them up from the water column. Therefore, nutrients assimilated by zooxanthellate jellyfish are likely to be retained and temporarily stored in the biomass of the population. The assimilation and retention of nitrogen were compared between zooxanthellate and non-zooxanthellate jellyfish. To do this, firstly, the assimilation and retention of nitrogen were directly compared between Cassiopea sp. and C. mosaicus. Jellyfish were labelled with isotopic nitrogen (15N) from two different sources, 15N-labelled Artemia prey and dissolved ammonium (15NH4+). The incorporation and retention of 15N was measured in the jellyfish tissues over nine days. Secondly, experiments were done to measure the influence of the availability of prey and concentrations of nutrients on the retention of nitrogen by Cassiopea sp. To do this, Cassiopea sp. were labelled with 15NH4+ and then placed in pools that had different combinations of high and low nutrient concentrations and high and low feeding regimes. The retention of 15N was measured in jellyfish over 37 days. Respiration and excretion rates were also measured for animals at the end of the experiment. Cassiopea sp. was found to assimilate nitrogen from both NH4+ and prey, and recycle this nitrogen internally. In contrast, C. mosaicus only assimilated nitrogen from prey and quickly excreted this nitrogen to the external environment, resulting in a short retention time. Cassiopea sp. retained nitrogen more than five times longer than C. mosaicus. Further, the nitrogen retention time of Cassiopea sp. was influenced by the availability of prey and dissolved nutrients, with the availability of prey having the greatest effect. Specifically, medusae exposed to low feeding retained nitrogen twice as long as medusae exposed to high feeding, which suggests that ingestion of prey by the host jellyfish is an important source of nitrogen in Cassiopea sp. Further, daily rates of photosynthesis and respiration suggest that photosynthesis by the zooxanthellae can potentially supply all of the carbon required for respiration and growth of the entire medusa. Jellyfish populations can hold considerable proportions of carbon and nutrients in an ecosystem and when a population crashes, jellyfish may sink to the benthos and decompose. An experiment was done that measured the changes in sediment oxygen demand as well as inorganic and organic nutrients during the decomposition of dead jellyfish, C. mosaicus. Fluxes were measured in tubs housing dead jellyfish over nine days as the jellyfish tissue decomposed. The decomposition of C. mosaicus resulted in a rapid leaching of organic nutrients from the dead tissues. Following this, microbial mineralisation dominated, which consumed oxygen and released dissolved inorganic nutrients. Although this release of nutrients may serve as a trophic link to pelagic primary producers, it may also lead to environmental problems associated with low oxygen concentrations depending on the size of the bloom and the degree of mixing in the system. Lastly, the influence of zooxanthellate and non-zooxanthellate jellyfish on plankton communities was compared. An in situ mesocosm experiment was done to compare the influence of C. mosaicus (non-zooxanthellate) and P. punctata (zooxanthellate). Changes in primary production and plankton assemblages were measured in mesocosms containing C. mosaicus, P. punctata, a combination of these species and compared to controls over six days. Catostylus mosaicus was found to increase chlorophyll a and productivity in the water column due to the large amount of nutrients excreted, causing a bottom-up influence on primary producers. This was in contrast to P. punctata, which were found to have little influence on chlorophyll a and production. This study provided direct experimental evidence that unlike C. mosaicus, P. punctata does not enhance primary production due to the minimal excretion of nutrients. Both P. punctata and C. mosaicus also had a large top-down predation pressure on zooplankton communities, causing significant declines in most species. This was with the exception of bivalve veligers, which were not consumed by either species, and gastropod veligers, which were not consumed by P. punctata. The major findings of this research have been integrated into a conceptual model that compares the influence of zooxanthellate and non-zooxanthellate jellyfish on nutrient cycles and trophodynamics. This model has been discussed in context to existing literature and recommendations have been made for future research. Overall this research found that zooxanthellate and non-zooxanthellate jellyfish assimilate, retain and release nutrients very differently and therefore have contrasting impacts on the nutrient cycling and trophodynamics of their surrounding ecosystem.

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Thesis (PhD Doctorate)
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Doctor of Philosophy (PhD)
Griffith School of Environment
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Aquatic biology
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