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Food supply effects on the asexual reproduction and respiratory metabolism of Aurelia aurita polyps

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Abstract

Because Aurelia spp. blooms have important regional effects, it is urgent to determine factors that may affect their proliferation and their effects on food webs. The life cycle of most scyphozoans includes an attached stage (polyp or scyphistoma) that reproduces asexually. To test the effects of food availability (unfed, fed 1-, 2-, or 3-times weekly), we measured production rates, mass, and metabolism of Aurelia aurita polyps. Metabolic measurements were physiological respiratory O2 consumption (R), potential O2 consumption (Φ), and potential CO2 production (ψNADP). Φ and ψNADP were calculated from enzymatic activities of the respiratory electron transport system (ETS) and from the CO2-producing enzyme, NADP+-dependent isocitrate dehydrogenase (NADP-IDH), respectively. The production of polyps dramatically increased from ~ 0.1 polyp day−1 (unfed) to ~ 0.65 polyp day−1 (fed 3-times week−1) over 33 days. Mass and metabolism (R, Φ, ψNADP) per polyp were significantly lower in unfed polyps, but indistinguishable among fed polyps. Our results suggested that the polyps maintained low-metabolic rates, putting available energy into asexual reproduction. The polyps were adapted to survive and reproduce when unfed, confirming their contribution to population persistence and potential jellyfish blooms.

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References

  • Amrhein, V., S. Greenland & B. McShane, 2019. Retire statistical significance. Nature 567: 305–307.

    Article  CAS  PubMed  Google Scholar 

  • Arai, M. N., 1997. A Functional Biology of Scyphozoa. Chapman & Hall, London.

    Google Scholar 

  • Ayala, D. J., P. Munk, R. B. C. Lundgreen, S. J. Traving, C. Jaspers, T. S. Jørgensen, L. H. Hansen & L. Riemann, 2018. Gelatinous plankton is important in the diet of European eel (Anguilla anguilla) larvae in the Sargasso Sea. Scientific Reports 8: 6156.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Berdalet, E., T. T. Packard, B. Legacé, S. Roy, L. St Amand & J. P. Gagné, 1995. CO2 production, O2 consumption, isocitrate dehydrogenase in the marine bacteria, Vibrio natriegens. Aquatic Microbial Ecology 9: 211–217.

    Article  Google Scholar 

  • Black, R. E., 1981. Metabolism and ultrastructure of dormant podocysts of Chrysaora quinquecirrha (Scyphozoa). Journal of Experimental Zoology 218: 175–182.

    Article  CAS  Google Scholar 

  • Blanquet, R. S., 1972. Temperature acclimation in the medusa, Chrysaora quinquecirrha. Comparative Biochemistry and Physiology 43B: 717–723.

    Google Scholar 

  • Bondyale-Juez, D. R., T. T. Packard, M. A. Viera-Rodríguez & M. Gómez, 2017. Respiration: comparison of the Winkler technique, O2 electrodes, O2 optodes and the respiratory electron transport system assay. Marine Biology 164: 164–226.

    Article  CAS  Google Scholar 

  • Brodeur, R. D., J. S. Link, B. E. Smith, M. D. Ford, D. Kobayashi & T. T. Jones, 2016. Ecological and economic consequences of ignoring jellyfish: a plea for increased monitoring of ecosystems. Fisheries 41: 622–629.

    Article  Google Scholar 

  • Carlotti, F. & J. C. Poggiale, 2010. Towards methodological approaches to implement the zooplankton component in “end to end” food-web models. Progress in Oceanography 84: 20–38.

    Article  Google Scholar 

  • Ceh, J., J. Gonzalez, A. S. Pacheco & J. M. Riascos, 2015. The elusive life cycle of scyphozoan jellyfish–metagenesis revisited. Scientific Reports 5: 12037.

    Article  PubMed  PubMed Central  Google Scholar 

  • Chapman, D. M., 1968. Structure, histochemistry and formation of the podocyst and cuticle of Aurelia aurita. Journal of the Marine Biological Association of the United Kingdom 48: 187–208.

    Article  Google Scholar 

  • Chiaverano, L. M. & W. M. Graham, 2017. Morphological plasticity in Aurelia polyps, with subsequent effects on asexual fecundity and morphology of young medusae. Marine Ecology Progress Series 582: 79–92.

    Article  CAS  Google Scholar 

  • Coyne, J. A., 1973. An investigation of the dynamics of population growth and control in scyphistomae of the scyphozoan Aurelia aurita. Chesapeake Science 14: 55–58.

    Article  Google Scholar 

  • Dong, Z., 2019. Blooms of the moon jellyfish Aurelia: causes, consequences and controls. In Sheppard, C. (ed.), World Seas: An Environmental Evaluation. Vol. III. Ecological Issues and Environmental Impacts. Elsevier Ltd., London: 163–171.

    Google Scholar 

  • Duarte, C. M., K. A. Pitt, C. H. Lucas, J. E. Purcell, S.-I. Uye, K. Robinson, L. Brotz, M. B. Decker, K. R. Sutherland, A. Malej, L. Madin, H. Mianzan, J.-M. Gili, V. Fuentes, D. Atienza, F. Pagés, D. Breitburg, J. C. Malek, W. M. Graham & R. Condon, 2013. Is global ocean sprawl a cause for jellyfish blooms? Frontiers in Ecology and the Environment 11: 91–97.

    Article  Google Scholar 

  • Feng, S., G. T. Zhang, S. Sun, F. Zhang, S. W. Wang & M. T. Liu, 2015. Effects of temperature regime and food supply on asexual reproduction in Cyanea nozakii and Nemopilema nomurai. Hydrobiologia 754: 201–214.

    Article  Google Scholar 

  • Fu, D., G. Wang, T. Cai, W. Liu, Y. Wang, Y. Zhang, L. Cui, L. Li, H. Yun, Y. Wu, A. Sun, C. Liu, W. Pei, R. R. Gaines & X. Zhang, 2019. The Qingjiang biota – a Burgess Shale–type fossil Lagerstätte from the early Cambrian of South China. Science 363: 133.

    Article  CAS  Google Scholar 

  • Gambill, M. & M. A. Peck, 2014. Respiration rates of the polyps of four jellyfish species: potential thermal triggers and limits. Journal of Experimental Marine Biology and Ecology 459: 17–22.

    Article  Google Scholar 

  • Gibbons, M. J. & A. J. Richardson, 2013. Beyond the jellyfish joyride and global oscillations: advancing jellyfish research. Journal of Plankton Research 35: 929–938.

    Article  Google Scholar 

  • Goldstein, J., C. B. Augustin, S. Bleich & S. Holst, 2017. A matter of tolerance: distribution potential of scyphozoan polyps in a changing environment. Marine Ecology 38: e12457.

    Article  Google Scholar 

  • Goldstein, J., C. Jürgensen, U. K. Steiner & H. U. Riisgård, 2018. Density-driven water exchange controls seasonal declines in jellyfish (Aurelia aurita) abundance in a shallow fjord system. Marine Ecology Progress Series 597: 137–145.

    Article  Google Scholar 

  • Gómez, M., S. Torres & S. Hernández-León, 1996. Modification of the electron transport system (ETS) method for routine measurements of respiratory rates of zooplankton. South African Journal of Marine Science 17: 15–20.

    Article  Google Scholar 

  • Han, C. H. & S. I. Uye, 2010. Combined effects of food supply and temperature on asexual reproduction and somatic growth of polyps of the common jellyfish Aurelia aurita sl. Plankton and Benthos Research 5: 98–105.

    Article  Google Scholar 

  • Heim-Ballew, H. & Z. Olsen, 2019. Salinity and temperature influence on Scyphozoan jellyfish abundance in the Western Gulf of Mexico. Hydrobiologia 827: 247–262.

    Article  CAS  Google Scholar 

  • Hernández-León, S. & M. Gómez, 1996. Factors affecting the respiration/ETS ratio in marine zooplankton. Journal of Plankton Research 18: 239–255.

    Article  Google Scholar 

  • Herrera, A., T. T. Packard, A. Santana & M. Gómez, 2011. Effect of starvation and feeding on respiratory metabolism in Leptomysis lingvura (GO Sars, 1866). Journal of Experimental Marine Biology Ecology 409: 154–159.

    Article  Google Scholar 

  • Holms, W. H., 1986a. The central metabolic pathways of Escherichia coli: relationship between flux and control at a branch point, efficiency of conversion to biomass, excretion of acetate. In Horecker, B. L. & E. R. Stadtman (eds), Current Topics in Cellular Regulation, Vol. 28., Academic Press Orlando, FL: 69–105.

    Google Scholar 

  • Holms, W. H., 1986b. Evolution of the glyoxylate bypass in Escherichia coli—An hypothesis which suggests an alternative to the Krebs cycle. FEMS Microbial Letters 34: 123–127.

    CAS  Google Scholar 

  • Hubot, N., C. H. Lucas & S. Piraino, 2017. Environmental control of asexual reproduction and somatic growth of Aurelia spp. (Cnidaria, Scyphozoa) polyps from the Adriatic Sea. PLoSONE 12: e0178482.

    Article  CAS  Google Scholar 

  • Iguchi, N., H. Iwatani, K. Sugimoto, S. Kitajima, N. Honda & O. Katoh, 2017. Biomass, body elemental composition, carbon requirement of Nemopilema nomurai (Scyphozoa: Rhizostomeae) in the southwestern Japan Sea. Plankton and Benthos Research 12: 104–114.

    Article  Google Scholar 

  • Ikeda, H., C. Mizota & S. I. Uye, 2017. Bioenergetic characterization in Aurelia aurita (Cnidaria: Scyphozoa) polyps and application to natural polyp populations. Marine Ecology Progress Series 568: 87–100.

    Article  CAS  Google Scholar 

  • Ishii, H. & T. Watanabe, 2003. Experimental study of growth and asexual reproduction in Aurelia aurita polyps. Sessile Organisms 20: 69–73.

    Article  Google Scholar 

  • Ishii, H., T. Ohba & T. Kobayashi, 2008. Effects of low dissolved oxygen on planula settlement, polyp growth and asexual reproduction of Aurelia aurita. Plankton and Benthos Research 3: 107–113.

    Article  Google Scholar 

  • Janßen, H., C. B. Augustin, H. H. Hinrichsen & S. Kube, 2013. Impact of secondary hard substrate on the distribution and abundance of Aurelia aurita in the western Baltic Sea. Marine Pollution Bulletin 75: 224–234.

    Article  PubMed  CAS  Google Scholar 

  • Kogovšek, T., M. Vodopivec, F. Raicich, S. I. Uye & A. Malej, 2018. Comparative analysis of the ecosystems in the northern Adriatic Sea and the Inland Sea of Japan: can anthropogenic pressures disclose jellyfish outbreaks? Science of the Total Environment 626: 982–994.

    Article  PubMed  CAS  Google Scholar 

  • Lilley, M. K. S. & F. Lombard, 2015. Respiration of fragile planktonic zooplankton: extending the possibilities with a single method. Journal of Experimental Marine Biology and Ecology 471: 226–231.

    Article  Google Scholar 

  • Liu, W. C., W. T. Lo, J. E. Purcell & H. H. Chang, 2009. Effects of temperature and light intensity on asexual reproduction of the scyphozoan, Aurelia aurita (L.) in Taiwan. Hydrobiologia 616: 247–258.

    Article  Google Scholar 

  • Lowry, O. H., N. J. Rosebrough, A. L. Farr & R. J. Randall, 1951. Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193: 265–275.

    CAS  PubMed  Google Scholar 

  • Lucas, C. H., W. M. Graham & C. Widmer, 2012. Jellyfish life histories: role of polyps in forming and maintaining scyphomedusa populations. Advances in Marine Biology 63: 133–196.

    Article  PubMed  Google Scholar 

  • Mangum, C. P., M. J. Oakes & J. M. Shick, 1972. Rate-temperature responses in scyphozoan medusae and polyps. Marine Biology 15: 298–303.

    Article  Google Scholar 

  • Markwell, M. A. K., S. M. Haas, L. L. Bieber & N. Tolbert, 1978. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Analytical Biochemistry 87: 206–210.

    Article  CAS  PubMed  Google Scholar 

  • Miller, M. E. C. & W. M. Graham, 2012. Environmental evidence that seasonal hypoxia enhances survival and success of jellyfish polyps in the northern Gulf of Mexico. Journal of Experimental Marine Biology and Ecology 432: 113–120.

    Article  Google Scholar 

  • Møller, L. F. & H. U. Riisgård, 2007. Respiration in the scyphozoan jellyfish Aurelia aurita and two hydromedusae (Sarsia tubulosa and Aequorea vitrina): effect of size, temperature and growth. Marine Ecology Progress Series 330: 149–154.

    Article  Google Scholar 

  • Osma, N., M. Aristizabal, I. Fernández-Urruzola, T. T. Packard & M. Gómez, 2016a. Influence of starvation on respiratory metabolism and pyridine nucleotide levels in the marine dinoflagellate Oxyrrhis marina. Protist 167: 136–147.

    Article  CAS  PubMed  Google Scholar 

  • Osma, N., I. Fernández-Urruzola, M. Gómez, S. Montesdeoca-Esponda & T. T. Packard, 2016b. Predicting in vivo oxygen consumption rate from ETS activity and bisubstrate enzyme kinetics in cultured marine zooplankton. Marine Biology 163: 1–14.

    Article  CAS  Google Scholar 

  • Owens, T. G. & F. D. King, 1975. The measurement of respiratory electron-transport-system activity in marine zooplankton. Marine Biology 30: 27–36.

    Article  Google Scholar 

  • Packard, T. T., 1985. Measurement of electron transport activity of microplankton. Advances in Aquatic Microbiology 3: 207–261.

    Google Scholar 

  • Packard, T. T. & J. P. Christensen, 2004. Respiration and vertical carbon flux in the Gulf of Maine water column. Journal of Marine Research 62: 93–115.

    Article  Google Scholar 

  • Packard, T. T., D. Harmon & J. Boucher, 1974. Respiratory electron transport activity in plankton from upwelled waters. Tethys 6: 213–222.

    CAS  Google Scholar 

  • Packard, T. T., E. Berdalet, D. Blasco, S. O. Roy, L. St-Amand, B. Lagacé, K. Lee & J. P. Gagne, 1996. CO2 production predicted from isocitrate dehydrogenase activity and bisubstrate enzyme kinetics in the marine bacterium Pseudomonas nautica. Aquatic Microbial Ecology 11: 11–19.

    Article  Google Scholar 

  • Pascual, M., V. Fuentes, A. Canepa, D. Atienza, J.-M. Gili & J. E. Purcell, 2014. Temperature effects on asexual reproduction of the scyphozoan Aurelia aurita s.l.: differences among exotic (Baltic and Red seas) and native (Mediterranean Sea) populations. Marine Ecology 36: 994–1002.

    Article  Google Scholar 

  • Pauly, D., W. Graham, S. Libralato, L. Morissette & M. D. Palomares, 2009. Jellyfish in ecosystems, online databases, and ecosystem models. Hydrobiologia 616: 67–85.

    Article  Google Scholar 

  • Purcell, J. E., 2007. Environmental effects on asexual reproduction rates of the scyphozoan, Aurelia labiata. Marine Ecology Progress Series 348: 183–196.

    Article  Google Scholar 

  • Purcell, J. E., 2012. Jellyfish and ctenophore blooms coincide with human proliferations and environmental perturbations. Annual Review of Marine Science 4: 209–235.

    Article  PubMed  Google Scholar 

  • Purcell, J. E., S. I. Uye & W. T. Lo, 2007. Anthropogenic causes of jellyfish blooms and their direct consequences for humans: a review. Marine Ecology Progress Series 350: 153–174.

    Article  Google Scholar 

  • Purcell, J. E., V. Fuentes, D. Atienza, U. Tilves, D. Astorga, M. Kawahara & G. C. Hays, 2010. Use of respiration rates of scyphozoan jellyfish to estimate their effects on the food web. Hydrobiologia 645: 135–152.

    Article  CAS  Google Scholar 

  • Purcell, J. E., V. Fuentes, D. Atienza, A. Olariaga, U. Tilves, C. Colahan & J.-M. Gili, 2012. Temperature effects on asexual reproduction rates of scyphozoan polyps from the NW Mediterranean Sea. Hydrobiologia 690: 169–180.

    Article  CAS  Google Scholar 

  • Robinson, K. L., J. J. Ruzicka, M. B. Decker, R. D. Brodeur, F. J. Hernandez, J. Quiñones, E. M. Acha, S. I. Uye, H. Mianzan & W. M. Graham, 2014. Jellyfish, forage fish, and the world’s major fisheries. Oceanography 27: 104–115.

    Article  Google Scholar 

  • Romero-Kutzner, V., T. T. Packard, E. Berdalet, S. O. Roy, J. P. Gagné & M. Gómez, 2015. Respiration quotient variability: bacterial evidence. Marine Ecology Progress Series 519: 47–59.

    Article  CAS  Google Scholar 

  • Roy, S. & T. T. Packard, 2001. CO2 production rate predicted from isocitrate dehydrogenase activity, intracellular substrate concentrations and kinetic constants in the marine bacterium Pseudomonas nautica. Marine Biology 138: 1251–1258.

    Article  CAS  Google Scholar 

  • Rutter, W. J., 1967. Protein determination in embryos. In Wilt, F. H. & N. K. Wessells (eds), Methods in Developmental Biology. Crowell Co, New York: 671–683.

    Google Scholar 

  • Schroth, W., G. Jarms, B. Streit & B. Schierwater, 2002. Speciation and phylogeography in the cosmopolitan marine moon jelly, Aurelia sp. BMC Evolutionary Biology 2: 1–10.

    Article  PubMed  PubMed Central  Google Scholar 

  • Scorrano, S., G. Aglieri, F. Boero, M. N. Dawson & S. Piraino, 2016. Unmasking Aurelia species in the Mediterranean Sea: an integrative morphometric and molecular approach. Zoological Journal of the Linnean Society 180: 243–267.

    Google Scholar 

  • Shick, J. M., 1975. Uptake and utilization of dissolved glycine by Aurelia aurita scyphistomae: temperature effects on the uptake process; nutritional role of dissolved amino acids. The Biological Bulletin 148: 117–140.

    Article  CAS  PubMed  Google Scholar 

  • Tames-Espinosa, M., I. Martínez, V. Romero-Kutzner, D. R. Bondyale-Juez, T. T. Packard & M. Gómez, 2018. NADP + -dependent isocitrate dehydrogenase activity in marine plankton. Marine Chemistry 204: 86–94.

    Article  CAS  Google Scholar 

  • Thuesen, E. V. & J. J. Childress, 1994. Oxygen consumption rates and metabolic enzyme activities of oceanic California medusae in relation to body size and habitat depth. The Biological Bulletin 187: 84–98.

    Article  CAS  PubMed  Google Scholar 

  • Uye, S. & H. Shimauchi, 2005. Population biomass, feeding, respiration and growth rates, and carbon budget of the scyphomedusa Aurelia aurita in the Inland Sea of Japan. Journal of Plankton Research 27: 237–248.

    Article  CAS  Google Scholar 

  • Vodopivec, M., A. Peliz & A. Malej, 2017. Offshore marine constructions as propagators of moon jellyfish dispersal. Environmental Research Letters 12: 084003.

    Article  Google Scholar 

  • Walsh, K. & D. E. Koshland, 1984. Determination of flux through the branch point of two metabolic cycles. The tricarboxylic acid cycle and the glyoxylate shunt. Journal of Biological Chemistry 259: 9646–9654.

    CAS  PubMed  Google Scholar 

  • Wang, N., C. Li, Y. Liang, Y. Shi & J. Lu, 2015. Prey concentration and temperature effect on budding and strobilation of Aurelia sp. 1 polyps. Hydrobiologia 754: 125–134.

    Article  CAS  Google Scholar 

  • Widmer, C. L., C. J. Fox & A. S. Brierley, 2016. Effects of temperature and salinity on four species of northeastern Atlantic scyphistomae (Cnidaria: Scyphozoa). Marine Ecology Progress Series 559: 73–88.

    Article  Google Scholar 

  • Willcox, S., N. A. Moltschaniwskyj & C. Crawford, 2007. Asexual reproduction in scyphistomae of Aurelia sp.: effects of temperature and salinity in an experimental study. Journal of Experimental Marine Biology and Ecology 353: 107–114.

    Article  Google Scholar 

  • Willcox, S., N. A. Moltschaniwskyj & C. Crawford, 2008. Population dynamics of natural colonies of Aurelia sp. scyphistomae in Tasmania, Australia. Marine Biology 154: 661–670.

    Article  Google Scholar 

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Acknowledgements

This work was accomplished thanks to the Fulbright Senior Scholarship to J. E. P., the Spanish Ministry of Economy and Competitiveness, the Spanish Ministry of Education, Culture and Sports at the University of Las Palmas de Gran Canaria. We thank OneMind DataScience for statistical analyses.

Funding

This work was funded by the MERMAC and MEMECAN projects granted by the Canary Islands CEI—Tricontinental Atlantic Campus. Also, funds granted to M. G. came from the PERSEO project (ProID201710051) funded by Canary Island Government and fondos FEDER. J. E. P. was supported by the Commission for Cultural, Educational and Scientific Exchange between the United States of America and Spain as a Fulbright U.S. Senior Researcher in the 2016–2017 Scholar Program. D. R. B.-J. received financial support from the FPU grants from the Spanish Ministry of Education, Culture and Sports. V. R. K. received financial support from the Canary Island Government (Gobierno de Canarias, Agencia Canaria de Investigación, Innovación y Sociedad de la Información). T.T. P. was supported by TIAA-CREF (USA), Social Security (USA), and the Canary Islands CEI—Tricontinental Atlantic Campus.

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  1. Department of Biology, Western Washington University, Bellingham, WA, 98225, USA

    Jennifer E. Purcell

  2. Marine Ecophysiology Group (EOMAR), Universidad de Las Palmas de Gran Canaria, IU-ECOAQUA, 35017, Las Palmas, Spain

    Jennifer E. Purcell, Daniel R. Bondyale-Juez, Vanesa Romero-Kutzner, Ico Martínez, Rosa Caprioli, Mayte Tames-Espinosa, Theodore T. Packard & May Gómez

  3. Loro Parque Foundation, Tenerife, Puerto de la Cruz, Spain

    Javier Almunia & Ester Alonso

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  1. Jennifer E. Purcell
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Purcell, J.E., Bondyale-Juez, D.R., Romero-Kutzner, V. et al. Food supply effects on the asexual reproduction and respiratory metabolism of Aurelia aurita polyps. Hydrobiologia 846, 135–146 (2019). https://doi.org/10.1007/s10750-019-04057-4

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