Investigating the potential of jellyfishes as marine biomonitors and bioindicators of metal pollution

Metal pollution has long been recognised as having a significant impact on the biodiversity and health of marine coastal systems. The use of biomonitor and bioindicator species is widely accepted for protecting ecosystem integrity and remediation of impacted systems. Species used as biomonitors in marine systems are typically benthic sessile species with a tolerance to the pollutant under investigation. In contrast, bioindicator species need to be sensitive to the pollutant. Historically, jellyfishes have not been regarded as useful bioindicators as they have been considered very tolerant of polluted environments and thus not evaluated in the suite of indicator species. Their pelagic behaviour and seasonality also mean they have not previously been considered useful biomonitor species despite their potentially high seasonal abundance in coastal systems. Notwithstanding these factors, current concerns about increased jellyfish blooms and their ability to cycle large quantities of inorganic elements suggest jellyfishes could fulfil a useful role in assessing ecosystem health. The objective of this project was to assess the potential jellyfishes have as biomonitors or bioindicators to the effects of dissolved metals. The research focused on the response of scyphozoan and cubozoan jellyfishes to metal exposure and assessed bioaccumulative capacity and retention as well as sensitivity to metals. To assess the biomonitoring capacity, elemental concentrations in tissues of jellyfishes were measured at multiple locations on the Great Barrier Reef over a three year period. Scyphozoan jellyfishes accumulated higher concentrations of elements at coastal and inshore locations compared with off-shore locations, which likely reflected the gradient of terrestrially derived elements into the marine system. Symbiotic scyphozoan jellyfishes typically had higher body concentrations of elements than their asymbiotic relatives collected from the same location and time. Further, variations in elemental tissue concentrations among cubozoan jellyfishes were species dependent. Laboratory assessment of the bioconcentration of aqueous copper or zinc in the symbiotic rhizostome jellyfish Cassiopea sp. showed that both metals readily accumulated in tissues at levels that were orders of magnitude above ambient water concentrations. However, the accumulative capacity and retention time varied between the metals. Copper was accumulated more rapidly and excreted more rapidly post-exposure (biological half-life 1.7 days), while zinc was accumulated more slowly and did not reach saturation during the study but was retained for much longer (biological half-life 9.1 days). Although the exact mechanisms of uptake and retention were not identified, it was apparent that accumulation and retention strategies in Cassiopea sp. were strongly metal dependent. To assess the bioindicator potential of jellyfishes, a series of laboratory studies measured the acute effects of copper and zinc at multiple lifestages in three species of jellyfish. From the outcomes of the acute toxicity, additional studies were conducted using the most sensitive species to determine sub-lethal responses of the jellyfish to copper or zinc exposure. The acute toxicity of aqueous copper and zinc was assessed in three species of jellyfish representing symbiotic (Cassiopea sp.) and asymbiotic Scyphozoa (Aurelia sp.), and a cubozoan jellyfish (Alatina mordens). Copper was an order of magnitude more toxic to all species and lifestages than zinc. Cassiopea sp. was more sensitive to both copper and zinc exposure than Alatina mordens. Aurelia sp. was the least sensitive of the three species to both metals. Sensitivity to copper and zinc varied among lifestage also, with the newly metamorphosed / strobilated stages being more sensitive than the benthic polyps in the three species. Cassiopea sp. was the most sensitive species from the acute toxicity studies. Sub-lethal toxicity to copper and zinc was assessed for both the jellyfish and its endosymbiont zooxanthellae. The response of the zooxanthellae was tested using photosynthetic yield as the end point and the host jellyfish response was assessed using change in bell diameter. There was a decrease in photosynthetic yield in the zooxanthellae exposed to increasing concentrations of copper or zinc although this was only significant at the higher concentrations (24 μg.L⁻¹ Cu, 0.88 mg.L⁻¹ Zn). Post-experiment counts of zooxanthellae abundances showed that the jellyfish did not expel the symbionts as a stress response to metal exposure, so that the change in photosynthetic yield resulted from decreased zooxanthellae activity rather than decreased abundance in the host tissues. Change in bell diameter of the Cassiopea sp. was significant at all concentrations of copper and zinc tested. This demonstrated that the host response was the more sensitive measure of exposure to copper or zinc than symbiont activity. In conclusion, the project demonstrated that jellyfishes were sensitive to metal pollution and have potential as bioindicators. The responses were variable among species and lifestages but demonstrated high sensitivity comparable to other marine bioindicators (e.g. hermatypic corals and molluscs). When exposed to low concentrations of metals, jellyfishes were capable of concentrating metals in their tissues and retaining them for days to weeks suggesting they are of high utility as marine biomonitors. These outcomes challenge historical views that jellyfish are more tolerant to pollutants than most marine taxa and are more likely to persist under poor environmental conditions. It also demonstrates that jellyfishes have strong potential for monitoring and assessing ecosystem health