Trace element accumulation in Cassiopea sp. (Scyphozoa) from urban marine environments in Australia

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Abstract

Jellyfishes are robust, short-lived animals, tolerant to a wide range of environmental conditions and pollutants. The benthic jellyfish, Cassiopea sp. was collected from five locations along the north and eastern coast of Australia and analysed for trace elements to determine if this species has potential as a marine biomonitor. Both the oral arm and bell tissues readily accumulated aluminium, arsenic, barium, cadmium, chromium, copper, iron, manganese and zinc above ambient seawater levels. In contrast, lithium appeared to be actively regulated within the tissues while calcium, magnesium and strontium reflected the ambient environment. The multi-element signatures showed spatial variation, reflecting the geographical separations between locations, with locations closer together showing more similar elemental patterns. The combination of bioaccumulative capacity, life history traits and biophysical aspects indicate that this species has high potential as a biomonitor in coastal marine systems.

Introduction

Many trace metals have important cellular and tissue functions within organisms. However, excessive concentrations of some elements can have a detrimental effect on the environment and its inhabitants (Sunda and Huntsman, 1998). Heavy metals and organic compounds that have no known biological function can also be taken up and concentrated in biological tissue (Wright, 1977). Although a large body of research exists on the levels, fluxes and cycling of chemicals in marine environments (e.g. Furness and Rainbow, 1990, Sadiq, 1992), concentrations of contaminants in water do not necessarily describe their ecological significance to biota.

The use of organisms as biomonitors for trace metals and environmental contaminants is a well-established practice in both terrestrial and aquatic environments. The extent to which any particular organism can serve as a biomonitor depends on a number of factors including the system under investigation, life history traits of the organism, the specific contaminants being monitored and the extent of uptake and retention of those contaminants (Rainbow and Phillips, 1993).

Gelatinous zooplankton (including jellyfish) can comprise a significant proportion of the total biomass of pelagic marine assemblages (Shenker, 1985, Romeo et al., 1992). Jellyfishes can tolerate a wide range of environmental and water quality conditions (Lucas, 2001, Purcell et al., 2001). They are short-lived generally, capable of rapid population explosions, high growth rates and plasticity of resource allocation. As a consequence, they can have detrimental economic, health and aesthetic effects in coastal systems (Graham et al., 2003, Uye and Shimauchi, 2005), although they are valuable in some regions as a fisheries resource (Kingsford et al., 2000, Pitt and Kingsford, 2003).

Although data is limited on the capacity of jellyfish to take up metals, the available information suggests they are capable of accumulating metals and nutrients above ambient seawater concentrations and potentially transferring these further up the foodchain. (Heymans and Baird, 2000, Kingsford et al., 2000, Fukuda and Naganuma, 2001, Fowler et al., 2004, Hay, 2006). Caurant et al. (1999) linked elevated cadmium levels in tissues of certain turtle species with their jellyfish prey. Romeo et al. (1992) also identified that gelatinous zooplankton may have a role in bioconcentration of metals up the food chain.

Although previously not considered as biomonitors, scyphozoan jellyfish possess many features considered important in biomonitors. Rainbow and Phillips (1993) identified a number of features that were essential for an organism to be considered a suitable biomonitor. These include the capacity to accumulate metals, sedentary behaviour, ease of identification, presence at locations of interest, and tolerance to physico-chemical changes within their environment (Rainbow and Phillips, 1993).

The benthic scyphozoan jellyfish, Cassiopea sp. is euryhaline, tolerant of physio-chemical changes to its environment, is readily identifiable, can be present at high densities, has a wide distribution in tropical coastal environments and due to its benthic nature is relatively sedentary, and as such meets the biomonitoring criteria set out above. Cassiopea sp. are typically found in sheltered locations (e.g. man-made lagoons and lakes, inshore seagrass meadows, mangroves, protected reefs, etc.) and exhibit atypical behaviour of resting upside down on the substrate giving rise to their common name – ‘Upside Down Jellyfish’. They possess an endosymbiotic relationship with Symbodium sp. and thus are capable of photosynthesis, which is associated with demonstrated efficiencies in uptake of inorganic nutrients and elements from the surrounding water column (Estes et al., 2003, Fowler et al., 2004).

The objective of this study was to compare trace element concentrations in bell and oral arm tissues of Cassiopea sp. collected from urban water bodies across eastern and northern Australia. Both essential trace elements and priority pollutants were measured and compared to ambient seawater concentrations from the collection sites to determine if Cassiopea sp. were capable of accumulating trace elements. Trace element signatures in jellyfish and seawater were also compared among locations to determine the potential for jellyfish to provide time-integrated measures of local conditions.

Section snippets

Materials and methods

Cassiopea sp. and water samples were collected from five locations adjacent to urban areas: Myora Drain A & B on the Gold Coast; Lake Magellan A & B on the Sunshine Coast in Queensland; and Lake Alexander in Darwin, Northern Territory, Australia. Locations A & B for Myora Drain & Lake Magellan were separated from each other by approximately 1–1.5 km. Five jellyfish and two water samples were collected at each location (Table 1).

Element concentrations between and within tissues

Trace element concentrations varied among locations and between tissues for most elements (Table 2). Barium and zinc concentrations were significantly higher in oral arm tissues than bell tissue at all locations. Mean concentrations of manganese, arsenic, aluminium and cadmium were also higher in oral arm tissue than bell tissue at all locations but the differences were not always significant (Table 2). Concentrations of copper, iron and strontium were higher in oral arm tissue at some

Trace element uptake and accumulation

Studies have demonstrated that jellyfishes and other gelatinous plankton are capable of absorbing trace elements from the environment in measurable concentrations (Romeo et al., 1992, Hanaoka et al., 2001, Fowler et al., 2004). However, data on bioaccumulation in scyphozoan and other jellyfishes is limited (Table 6).

Investigations into the extent of uptake and/or accumulation of elements from the surrounding water by jellyfish are even more limited. Cimino et al. (1983) found tissue

Conclusions

This study has demonstrated that Cassiopea sp. is capable of accumulating elements above ambient seawater concentrations. It is also possible to discriminate different geographical populations based on chemical signatures in their tissues. While their persistence in polluted systems has been documented, historically jellyfish have not been considered useful biomonitors. We suggest it would be useful to consider them as a future tool in the biomonitoring toolbox, as they meet many of the

Acknowledgements

Thank you to Dr. Yi Hu for reviewing and providing constructive suggestions on the digestion method and for undertaking the ICP-MS analyses. Thank you to Darwin City Council for providing Cassiopea sp. samples. Thank you also to Caloundra City council for providing background information on Lake Magellan. Funding for the project was provided by JCU and the Australian Research Council.

References (34)

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