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Original articles

Under pressure: Cassiopea andromeda jellyfish exposed to increasing water temperature or lead, cadmium and anthropogenic gadolinium contamination

ORCID Icon & ORCID Icon
Pages 48-63 | Received 28 May 2021, Accepted 28 Feb 2022, Published online: 01 Jun 2022

References

  • Aljbour S, Zimmer M, Kunzmann A. 2017. Cellular respiration, oxygen consumption, and trade-offs of the jellyfish Cassiopea sp. in response to temperature change. Journal of Sea Research. 128:92–97. doi:10.1016/j.seares.2017.08.006
  • Amor KOB, Rifi M, Ghanem R, Draief I, Zaouali J, Ben Souissi J. 2016. Update of alien fauna and new records from Tunisian marine waters. Mediterranean Marine Science. 17:124–143. doi:10.12681/mms.1371
  • Arai MN. 1996. A functional biology of Scyphozoa. London: Chapman & Hall.
  • Auernheimer C, Servando C, Jose AP. 1996. Lead pollution in bivalve shells: Mar Menor, Spain. Arch des Sci compte rendu des séances la Société. 49:87–98. doi:10.5169/seals-740414
  • Avian M, Rottini Sandrini L, Stravisi F. 1991. The effect of seawater temperature on the swimming activity of Pelagia noctiluca (Forsskal). Bolletino di Zoologia. 58:135–143. doi:10.1080/11250009109355744
  • Bau M, Dulski P. 1996. Anthropogenic origin of positive gadolinium anomalies in river waters. Earth and Planetary Science Letters. 143:245–255. doi:10.1016/0012-821X(96)00127-6
  • Bau M, Knappe A, Dulski P. 2006. Anthropogenic gadolinium as a micropollutant in river waters in Pennsylvania and in Lake Erie, northeastern United States. Geochemistry. 66:143–152. doi:10.1016/j.chemer.2006.01.002
  • Bhagooli R, Hidaka M. 2003. Comparison of stress susceptibility of in hospite and isolated zooxanthellae among five coral species. Journal of Experimental Marine Biology and Ecology. 291:181–197. doi:10.1016/S0022-0981(03)00121-7
  • Chapman PM, Mcdonald BG, Kickham PE, Mckinnon S. 2006. Global geographic differences in marine metals toxicity. Marine Pollution Bulletin. 52:1081–1084. doi:10.1016/j.marpolbul.2006.05.004
  • Cillari T, Andaloro E, Castriota L. 2018. First documented record of Cassiopea andromeda (Cnidaria: Scyphozoa) in Italian waters. Cahiers de Biologie Marine. 59:193–195. doi:10.21411/CBM.A.1037AA
  • Colin SP, Costello JH. 2003. In situ swimming and feeding behavior of eight co-occurring hydromedusae. Marine Ecology Progress Series. 253:305–309. doi:10.3354/meps253305
  • Díaz-Almeyda EM, Prada C, Ohdera AH, Moran H, Civitello DJ, Iglesias-Prieto R, Carlo TA, Lajeunesse TC, Medina M. 2017. Intraspecific and interspecific variation in thermotolerance and photoacclimation in Symbiodinium dinoflagellates. Proceedings of the Royal Society B: Biological Sciences. 284. doi:10.1098/rspb.2017.1767
  • Dillon TM. 1977. Effects of acute changes in temperature and salinity on pulsation rates in ephyrae of the scyphozoan Aurelia aurita. Marine Biology. 42:31–35. doi:10.1007/BF00392011
  • Epstein HE, Templeman MA, Kingsford MJ. 2016. Fine-scale detection of pollutants by a benthic marine jelly fish. Marine Pollution Bulletin. 107:340–346. doi:10.1016/j.marpolbul.2016.03.027
  • Fitt WK, Warner ME. 1995. Bleaching patterns of four species of Caribbean Reef Corals. The Biological Bulletin. 189:298–307. doi:10.2307/1542147
  • Fowler SW, Danis B, Fowler SW, Teyssié J, Cotret O, Danis B, Rouleau C. 2004. Applied radiotracer techniques for studying pollutant bioaccumulation in selected marine organisms (jellyfish, crabs and sea stars). Nukleonika. 49:97–100.
  • Freeman CJ, Stoner EW, Easson CG, Matterson KO, Baker DM. 2017. Variation in δ13C and δ15N values suggests a coupling of host and symbiont metabolism in the Symbiodinium−Cassiopea mutualism. Marine Ecology Progress Series. 571:245–251. doi:10.3354/meps12138
  • Gatz JA, Kennedy VS, Mihursky JA. 1973. Effects of temperature on activity and mortality of the scyphozoan medusa, Chrysaora quinquecirrha. Chesapeake Science. 14:171–180. doi:10.2307/1350603.
  • Gohar HAF, Eisawy AM. 1960. The biology of Cassiopea andromeda (from the Red Sea). Publications of the Marine Biological Station, Ghardaqa. 11:48–190.
  • Hamed MA, Emara AM. 2006. Marine molluscs as biomonitors for heavy metal levels in the Gulf of Suez, Red Sea. Journal of Marine Systems. 60:220–234. doi:10.1016/j.jmarsys.2005.09.007
  • Hamlet CL, Miller LA. 2012. Feeding currents of the upside down jellyfish in the presence of background flow. Bulletin of Mathematical Biology. 74:2547–2569. doi:10.1007/s11538-012-9765-6
  • Hamlet CL, Santhanakrishnan A, Miller LA. 2011. A numerical study of the effects of bell pulsation dynamics and oral arms on the exchange currents generated by the upside-down jellyfish Cassiopea xamachana. Journal of Experimental Biology. 214:1911–1921. doi:10.1242/jeb.052506
  • Hatje V, Bruland KW, Flegal AR. 2016. Increases in anthropogenic gadolinium anomalies and rare earth element concentrations in San Francisco bay over a 20 year record. Environmental Science & Technology. 50:4159–4168. doi:10.1021/acs.est.5b04322
  • Hoegh-Guldberg O, Jones RJ, Larkum AWD, Schreiber U. 1998. Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant, Cell and Environment. 21:1219–1230. doi:10.1046/j.1365-3040.1998.00345.x
  • Hofmann DK, Kremer BP. 1981. Carbon metabolism and strobilation in Cassiopea andromedea (Cnidaria: Scyphozoa): significance of endosymbiotic dinoflagellates. Marine Biology. 65:25–33. doi:10.1007/BF00397064
  • Holland BS, Dawson MN, Crow GL, Hofmann DK. 2004. Global phylogeography of Cassiopea (Scyphozoa: Rhizostomeae): molecular evidence for cryptic species and multiple invasions of the Hawaiian Islands. Marine Biology. 145:1119–1128. doi:10.1007/s00227-004-1409-4
  • Howe PL, Reichelt-Brushett AJ, Clark MW. 2014. Investigating lethal and sublethal effects of the trace metals cadmium, cobalt, lead, nickel and zinc on the anemone Aiptasia pulchella, a cnidarian representative for ecotoxicology in tropical marine environments. Marine and Freshwater Research. 65:551–561. doi:10.1071/MF13195
  • Iglesias-Prieto R, Matta JL, Robins WA, Trench RK. 1992. Photosynthetic response to elevated temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. Proceedings of the National Academy of Sciences. 89:10302–10305. doi:10.1073/pnas.89.21.10302
  • Jantzen C, Wild C, Rasheed M, El-zibdah M, Richter C. 2010. Enhanced pore-water nutrient fluxes by the upside-down jellyfish Cassiopea sp. in a Red Sea coral reef. Marine Ecology Progress Series. 411:117–125. doi:10.3354/meps08623
  • Karim W, Nakaema S, Hidaka M. 2015. Temperature effects on the growth rates and photosynthetic activities of Symbiodinium cells. Journal of Marine Science and Engineering. 100:368–381. doi:10.3390/jmse3020368.
  • Karunarathne KD, Liyanaarachchi SM, De Croos MDST. 2020. First record of upside-down jellyfish Cassiopea andromeda (Forskål, 1775) (Cnidaria: Scyphozoa: Rhizostomeae: Cassiopeidae) from Sri Lanka. Sri Lanka Journal of Aquatic Sciences. 25:57. doi:10.4038/sljas.v25i2.7577
  • Klein SG, Pitt KA, Carroll AR. 2016. Reduced salinity increases susceptibility of zooxanthellate jellyfish to herbicide toxicity during a simulated rainfall event. Environmental Pollution. 209:79–86. doi:10.1016/j.envpol.2015.11.012
  • Klein SG, Pitt KA, Lucas CH, Hung SH, Schmidt-Roac S, Aranda M, Duarte CM. 2019. Night-time temperature reprieves enhance the thermal tolerance of a symbiotic cnidarian. Frontiers in Marine Science. 6:1–16. doi:10.3389/fmars.2019.00001
  • Krämer WE, Caamaño-Ricken I, Richter C, Bischof K. 2012. Dynamic regulation of photoprotection determines thermal tolerance of two phylotypes of Symbiodinium clade a at two photon fluence rates. Photochemistry and Photobiology. 88:398–413. doi:10.1111/j.1751-1097.2011.01048.x
  • Kremien M, Shavit U, Mass T, Genin A. 2013. Benefit of pulsation in soft corals. Proceedings of the National Academy of Sciences. 110:8978–8983. doi:10.1073/pnas.1301826110
  • Kulaksiz S, Bau M. 2011b. Anthropogenic gadolinium as a microcontaminant in tap water used as drinking water in urban areas and megacities. Applied Geochemistry. 26:1877–1885. doi:10.1016/j.apgeochem.2011.06.011
  • Larson RJ. 1997. Feeding behaviour of Caribbean scyhomedusae: Cassiopea frondosa (Pallas) and Cassiopea xamachana. Studies on the Natural History of the Caribbean Region. 73.
  • Lawrence MG, Ort C, Keller J. 2009. Detection of anthropogenic gadolinium in treated wastewater in South East Queensland, Australia. Water Research. 43:3534–3540. doi:10.1016/j.watres.2009.04.033
  • Lesser MP. 1996. Elevated temperatures and ultraviolet radiation cause oxidative stress and inhibit photosynthesis in symbiotic dinoflagellates. Limnology and Oceanography. 41:271–283. doi:10.4319/lo.1996.41.2.0271
  • Loganathan P, Hedley MJ. 1997. Downward movement of cadmium and phosphorus from phosphatic fertilisers in a pasture soil in New Zealand. Environmental Pollution. 95:319–324. doi:10.1016/S0269-7491(96)00142-X
  • Lyndby NH, Rädecker N, Bessette S, Søgaard Jensen LH, Escrig S, Trampe E, Kühl M, Meibom A. 2020. Amoebocytes facilitate efficient carbon and nitrogen assimilation in the Cassiopea-Symbiodiniaceae symbiosis. Proceedings of the Royal Society B: Biological Sciences. 20202393. doi:10.1098/rspb.2020.2393
  • Maggio T, Allegra A, Bosch-belmar M, Cillari T, Castriota L, Cuttitta A, Falautano M, Milisenda G, Nicosia A. 2019. Molecular identity of the non-indigenous Cassiopea sp. from Palermo Harbour (central Mediterranean Sea).
  • Mammone M, Ferrier-Pages C, Lavorano S, Rizzo L, Piraino S, Rossi S. 2021. High photosynthetic plasticity may reinforce invasiveness of upside-down zooxanthellate jellyfish in Mediterranean coastal waters. PLoS One. 16:1–17. doi:10.1371/journal.pone.0248814
  • Mayer AG. 1914. The effects of temperature on tropical marine animals. Pap Tortugas Lab 3.
  • McGill CJ, Pomory CM. 2008. Effects of bleaching and nutrient supplementation on wet weight in the jellyfish Cassiopea xamachana (Bigelow) (Cnidaria: Scyphozoa). Marine and Freshwater Behaviour and Physiology. 41:179–189. doi:10.1080/10236240802369899
  • McGinty ES, Pieczonka J, Mydlarz LD. 2012. Variations in reactive oxygen release and antioxidant activity in multiple Symbiodinium types in response to elevated temperature. Microbial Ecology. 64:1000–1007. doi:10.1007/s00248-012-0085-z
  • Merschel G, Bau M, Baldewein L, Dantas EL, Walde D, Bühn B. 2015. Tracing and tracking wastewater-derived substances in freshwater lakes and reservoirs: anthropogenic gadolinium and geogenic REEs in Lake Paranoa. Comptes Rendus Geoscience. 347:284–293. doi:10.1016/j.crte.2015.01.004
  • Möller P, Dulski P, Bau M, Knappe A, Pekdeger A, Mo P, Jarmersted CS. 2000. Anthropogenic gadolinium as a conservative tracer in hydrology. Journal of Geochemical Exploration. 69-70:409–414. doi:10.1016/S0375-6742(00)00083-2
  • Morandini AC, Stampar SN, Maronna MM, Da Silveira FL. 2017. All non-indigenous species were introduced recently? The case study of Cassiopea (Cnidaria: Scyphozoa) in Brazilian waters. Journal of the Marine Biological Association of the United Kingdom. 97:321–328. doi:10.1017/S0025315416000400
  • Muñoz-Vera A, García G, García-Sánchez A. 2015. Metal bioaccumulation pattern by Cotylorhiza tuberculata (Cnidaria, Scyphozoa) in the Mar Menor coastal lagoon (SE Spain). Environmental Science and Pollution Research. 22:19157–19169. doi:10.1007/s11356-015-5119-x
  • Negri AP, Flores F, Röthig T, Uthicke S. 2011. Herbicides increase the vulnerability of corals to rising sea surface temperature. Limnology and Oceanography. 56:471–485. doi:10.4319/lo.2011.56.2.0471
  • Negri AP, Hoogenboom MO. 2011. Water contamination reduces the tolerance of coral larvae to thermal stress. PLoS One. 6:e19703. doi:10.1371/journal.pone.0019703
  • Newkirk CR, Frazer TK, Martindale MQ, Schnitzler CE. 2020. Adaptation to bleaching: are Thermotolerant Symbiodiniaceae strains more successful than other strains under elevated temperatures in a model symbiotic cnidarian? Frontiers in Microbiology. 11:1–12. doi:10.3389/fmicb.2020.00822
  • Niggl W, Wild C. 2009. Spatial distribution of the upside-down jellyfish Cassiopea sp. within fringing coral reef environments of the Northern Red Sea: implications for its life cycle. Helgoland Marine Research. 64:281–287. doi:10.1007/s10152-009-0181-8
  • Nozaki Y, Lerche D, Alibo DS, Tsutsumi M. 2000. Dissolved indium and rare earth elements in three Japanese rivers and Tokyo Bay: Evidence for anthropogenic Gd and In. Geochimica et Cosmochimica Acta. 64:3975–3982. doi:10.1016/S0016-7037(00)00472-5
  • Ohdera AH, Abrams MJ, Ames CL, Baker DM, Suescún-Bolívar LP, Collins AG, Freeman CJ, Gamero-Mora E, Goulet TL, Hofmann DK, et al. 2018. Upside-down but headed in the right direction: review of the highly versatile Cassiopea xamachana system. Frontiers in Ecology and Evolution. 6:1–15. doi:10.3389/fevo.2018.00035
  • Özgür E, Öztürk B. 2008. Aa population of the alien jellyfish, Cassiopea andromeda (Forsskål, 1775) (Cnidaria: Scyphozoa: Rhizostomea) in the Ölüdeniz Lagoon, Turkey. Aquatic Invasions. 3:423–428. doi:10.3391/ai.2008.3.4.8
  • Perrat E, Parant M, Py J-S, Rosin C, Cossu-Leguille C. 2017. Bioaccumulation of gadolinium in freshwater bivalves. Environmental Science and Pollution Research. 24:12405–12415. doi:10.1007/s11356-017-8869-9
  • Rädecker N, Pogoreutz C, Wild C, Voolstra CR. 2017. Stimulated respiration and net photosynthesis in Cassiopeia sp. during glucose enrichment suggests in hospite CO2 limitation of algal endosymbionts. Frontiers in Marine Science. 4:2–5. doi:10.3389/fmars.2017.00267
  • Robinson JD, Warner ME. 2006. Differential impacts of photoacclimation and thermal stress on the photobiology of four different phylotopes of Symbiodinium. Journal of Phycology. 42:568–579. doi:10.1111/j.1529-8817.2006.00232.x
  • Roméo M, Gnassia-Barelli M, Carré C. 1992. Importance of gelatinous plankton organisms in storage and transfer of trace metals in the northwestern Mediterranean. Marine Ecology Progress Series. 82:267–274. doi:10.3354/meps082267
  • Rowen DJ, Templeman MA, Kingsford MJ. 2017. Chemosphere herbicide effects on the growth and photosynthetic efficiency of Cassiopea maremetens. Chemosphere. 182:143–148. doi:10.1016/j.chemosphere.2017.05.001
  • Rubio M. 2017. Una medusa tropical, nueva amenaza para la biodiversidad del mar Menor [WWW Document]. [accessed 14 March 2020]. https://elclickverde.com/reportajes/una-medusa-tropical-nueva-amenaza-para-la-biodiversidad-del-mar-menor.
  • Santhanakrishnan A, Dollinger M, Hamlet CL, Colin SP, Miller LA. 2012. Flow structure and transport characteristics of feeding and exchange currents generated by upside-down Cassiopea jellyfish. Journal of Experimental Biology. 215:2369–2381. doi:10.1242/jeb.053744
  • Schembri PJ, Deidun A, Vella PJ. 2010. First record of Cassiopea andromeda (Scyphozoa: Rhizostomeae: Cassiopeidae) from the central Mediterranean Sea. Marine Biodiversity Records. 3:1–2. doi:10.1017/S1755267209990625
  • Smith DJ, Suggett DJ, Baker NR. 2005. Is photoinhibition of zooxanthellae photosynthesis the primary cause of thermal bleaching in corals? Global Change Biology. 11:1–11. doi:10.1111/j.1529-8817.2003.00895.x
  • Stampar SN, Gamero-mora E, Maronna MM, Fritscher JM, Oliveira BSP, Sampaio CLS, Morandini AC. 2020. The puzzling occurrence of the upside-down jellyfish Cassiopea (Cnidaria: Scyphozoa) along the Brazilian coast: a result of several invasion events? Sociedade Brasileira de Zoologia. 4689:1–10.
  • Stoner EW, Layman CA. 2015. Bristle worms attack: benthic jellyfish are not trophic dead ends. Frontiers in Ecology and the Environment. 13:226–227. doi:10.1890/1540-9295-13.4.226
  • Stoner EW, Layman CA, Yeager LA, Hassett HM. 2011. Effects of anthropogenic disturbance on the abundance and size of epibenthic jellyfish Cassiopea spp. Marine Pollution Bulletin. 62:1109–1114. doi:10.1016/j.marpolbul.2011.03.023
  • Tchernov D, Gorbunov MY, de Vargas C, Narayan Yadav S, Milligan AJ, Häggblom M, Falkowski PG. 2004. Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proceedings of the National Academy of Sciences. 101:13531–13535. doi:10.1073/pnas.0402907101
  • Templeman MA, Kingsford M. 2015. Predicting aqueous copper and zinc accumulation in the upside-down jellyfish Cassiopea maremetens through the use of biokinetic models. Environmental Monitoring and Assessment. 187:416. doi:10.1007/s10661-015-4657-5
  • Templeman MA, Kingsford MJ. 2010. Trace element accumulation in Cassiopea sp. (Scyphozoa) from urban marine environments in Australia. Marine Environmental Research. 69:63–72. doi:10.1016/j.marenvres.2009.08.001
  • Templeman MA, Kingsford MJ. 2012. Variation in soft tissue chemistry among scyphozoan and cubozoan jellyfishes from the Great Barrier Reef, Australia. Hydrobiologia. 690:279–290. doi:10.1007/s10750-012-1051-y
  • Thé J, Barroso HS, Mammone M, Viana M, Batista Melo CS, Mies M, Banha TNS, Morandini AC, Rossi S, Soares MO. 2020. Aquaculture facilities promote populational stability throughout seasons and increase medusae size for the invasive jellyfish Cassiopea andromeda. Marine Environmental Research. 105161. doi:10.1016/j.marenvres.2020.105161
  • Thielmann DT. 2011. Novel functionalized rare earth metal clusters and polymers. Göttingen: Karsruhe Institut für Technologie KIT.
  • Titelman J, Riemann L, Sørnes TA, Nilsen T, Griekspoor P, Båmstedt U. 2006. Turnover of dead jellyfish: stimulation and retardation of microbial activity. Marine Ecology Progress Series. 325:43–58. doi:10.3354/meps325043
  • Trapasso G, Chiesa S, Freitas R, Pereira E. 2021. What do we know about the ecotoxicological implications of the rare earth element gadolinium in aquatic ecosystems? Science of The Total Environment. 781:146273. doi:10.1016/j.scitotenv.2021.146273
  • Verde EA, McCloskey LR. 1998. Production, respiration, and photophysiology of the mangrove jellyfish Cassiopea xamachana symbiotic with zooxanthellae: effect of jellyfish size and season. Marine Ecology Progress Series. 168:147–162. doi:10.3354/meps168147
  • Verplanck PL, Taylor HE, Nordstrom DK, Barber LB. 2005. Aqueous stability of gadolinium in surface waters receiving sewage treatment plant effluent Boulder Creek, Colorado. Environmental Science & Technology. 39:6923–6929. doi:10.1021/es048456u
  • Vodenichar JS. 1995. Ecophysiological physiology of the Scyphozoan Cassiopea xamachana. Athens: University of Georgia.
  • Welsh DT, Dunn RJK, Meziane T. 2009. Oxygen and nutrient dynamics of the upside down jellyfish (Cassiopea sp.) and its influence on benthic nutrient exchanges and primary production. Hydrobiologia. 635:351–362. doi:10.1007/s10750-009-9928-0
  • Yamamoto J, Hirose M, Ohtani T, Sugimoto K, Hirase K, Shimamoto N, Shimura T, Honda N, Fujimori Y, Mukai T. 2008. Transportation of organic matter to the sea floor by carrion falls of the giant jellyfish Nemopilema nomurai in the Sea of Japan. Marine Biology. 153:311–317. doi:10.1007/s00227-007-0807-9
  • Zarnoch CB, Hossain N, Fusco E, Alldred M, Hoellein TJ, Perdikaris S. 2020. Size and density of upside-down jellyfish, Cassiopea sp., and their impact on benthic fluxes in a Caribbean lagoon. Marine Environmental Research. 154:104845. doi:10.1016/j.marenvres.2019.104845