Metamorphosis in Aurelia aurita from polyp to medusa: assessing composition and metabolism throughout development

Vanesa Romero-Kutzner , Daniel R. Bondyale-Juez , Ico Martínez , Alicia Herrera , Theodore T. Packard , May Gómez

Marine Life Science & Technology ›› : 1 -15.

PDF
Marine Life Science & Technology ›› :1 -15. DOI: 10.1007/s42995-025-00329-2
Research Paper
research-article

Metamorphosis in Aurelia aurita from polyp to medusa: assessing composition and metabolism throughout development

Author information +
History +
PDF

Abstract

Aurelia aurita exhibits a triphasic life cycle involving metamorphosis, transitioning from sessile polyps to free-swimming ephyrae and eventually maturing into medusae. This metamorphic process is triggered by a reduction in temperature. In this investigation, we delve into the intricate changes in protein, lipid, and carbohydrate content, and examine alterations in respiratory and excretory metabolisms using both physiological and enzymatic methodologies. This study provides the first monitoring of these parameters. Observations at compositional and metabolic levels were conducted over 108 days in triplicate, with three simultaneous cultures maintained under identical conditions throughout the experiment. The findings reveal compositional changes, particularly in lipid content, one of the main sources of biological energy during metamorphosis. Additionally, a 20-day increase in water content from 89 to 99% occurred during the transition from strobila to metaephyra. Respiratory activity reduced by 76% during strobilation, due to the necessary temperature drop. Concurrently, excretory activity showed a more gradual increase in ammonium excretion during the planktonic stages once feeding resumed. These findings highlight the role of temperature-dependent triggers and metabolic shifts in facilitating energy storage among other functions. This knowledge may provide insights into the potential impacts of future environmental change on the entire lifecycle.

Keywords

Excretion / Jellyfish / Lipid / Protein / Respiration / Strobilation

Cite this article

Download citation ▾
Vanesa Romero-Kutzner, Daniel R. Bondyale-Juez, Ico Martínez, Alicia Herrera, Theodore T. Packard, May Gómez. Metamorphosis in Aurelia aurita from polyp to medusa: assessing composition and metabolism throughout development. Marine Life Science & Technology 1-15 DOI:10.1007/s42995-025-00329-2

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Aalto EA, Barry JP, Boch CA, Litvin SY, Micheli F, Woodson CB, De Leo GAD. Abalone populations are most sensitive to environmental stress effects on adult individuals. Mar Ecol Prog Ser, 2020, 643: 75-85

[2]

Abdullah A, Nurjanah N, Hidayat T, Aji DU. Fatty acid profile of jellyfish (Aurelia aurita) as a source raw material of aquatic result rich benefit. Int J Chem Biomol Sci, 2015, 1: 12-16

[3]

Aguiar-González B, Packard TT, Berdalet E, Roy S, Gómez M. Respiration predicted from an enzyme kinetic model and the metabolic theory of ecology in two species of marine bacteria. J Exp Mar Biol Ecol, 2012, 412: 1-12

[4]

Alex D (1971) Isoenzymes in amphibian metamorphosis. Dissertation, California State University East Bay, Hayward

[5]

Algueró-Muñiz M, Meunier CL, Holst S, Alvarez-Fernandez S, Boersma M. Withstanding multiple stressors: ephyrae of the moon jellyfish (Aurelia aurita, Scyphozoa) in a high-temperature, high-CO2 and low-oxygen environment. Mar Biol, 2016, 163: 1-12

[6]

Aljbour SM, Zimmer M, Kunzmann A. Cellular respiration, oxygen consumption, and trade-offs of the jellyfish Cassiopea sp. in response to temperature change. J Sea Res, 2017, 128: 92-97

[7]

Aljbour SM, Zimmer M, Al-Horani FA, Kunzmann A. Metabolic and oxidative stress responses of the jellyfish Cassiopea sp. to changes in seawater temperature. J Sea Res, 2019, 145: 1-7

[8]

Arai MN. A functional biology of Scyphozoa, 1997, London, Chapman & Hall

[9]

Båmstedt U, Martinussen MB, Matsakis S. Trophodynamics of the two scyphozoan jellyfishes, Aurelia aurita and Cyanea capillata, in western Norway. ICES J Mar Sci, 1994, 51: 369-382

[10]

Båmstedt U, Lane J, Martinussen MB. Bioenergetics of ephyra larvae of the scyphozoan jellyfish Aurelia aurita in relation to temperature and salinity. Mar Biol, 1999, 135: 89-98

[11]

Båmstedt U, Wild B, Martinussen MB. Significance of food type for growth of ephyrae Aurelia aurita (Scyphozoa). Mar Biol, 2001, 139: 641-650

[12]

Barnes H, Blackstock J. Estimation of lipids in marine animals and tissues: detailed investigation of the sulphophosphovanilun method for ‘total’ lipids. J Exp Mar Biol Ecol, 1973, 12: 103-118

[13]

Beenakkers AMT, Van der Horst DJ, Van Marrewijk WJA. Role of lipids in energy metabolism. Energy metabolism in insects, 19811New York, Plenum Press53100

[14]

Behrends G, Schneider G. Impact of Aurelia aurita medusae (Cnidaria, Scyphozoa) on the standing stock and community composition of mesozooplankton in the Kiel Bight (western Baltic Sea). Mar Ecol Prog Ser, 1995, 127: 39-45

[15]

Berdalet E, Packard T, Lagacé B, Roy S, St-Amand L, Gagné J-P. CO2 production, O2 consumption and isocitrate dehydrogenase in the marine bacterium Vibrio natriegens. Aquat Microb Ecol, 1995, 9: 211-217

[16]

Bidigare RR, King FD. The measurement of glutamate dehydrogenase activity in Praunus flexuosus and its role in the regulation of ammonium excretion. Comp Biochem and Physiol B-Comp Biochem, 1981, 70: 409-413

[17]

Bidigare R, King FD, Biggs DC. Glutamate dehydrogenase (GDH) and respiratory electron-transport-system (ETS) activities in Gulf of Mexico zooplankton. J Plankton Res, 1982, 4: 895-911

[18]

Biggs DC. Respiration and ammonium excretion by open ocean gelatinous zooplankton. Limnol Oceanogr, 1977, 22: 108-117

[19]

Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol, 1959, 37: 911-917

[20]

Bondyale-Juez DR, Packard TT, Viera-Rodríguez MA, Gómez M. Respiration: comparison of the Winkler technique, O2 electrodes, O2 optodes and the respiratory electron transport system assay. Mar Biol, 2017, 164: 226

[21]

Bondyale-Juez DR, Romero-Kutzner V, Purcell JE, Martínez I, Packard TT, Gómez M. Wind drifting vs. pulsating swimming jellyfish: respiratory metabolism and composition differences in Physalis physalis, Velella velella, Aurelia aurita, and Pelagia noctiluca. Front Mar Sci, 2022, 9 313

[22]

Brekhman V, Malik A, Haas B, Sher N, Lotan T. Transcriptome profiling of the dynamic life cycle of the scypohozoan jellyfish Aurelia aurita. BMC Genom, 2015, 16: 1-14

[23]

Brooks W. The life history of the hydromedusae: a discussion of the medusae and of the significance of metagenesis. Mem Boston Soc Nat Hist, 1886, 3: 359-430

[24]

Cartwright P, Halgedahl SL, Hendricks JR, Jarrard RD, Marques AC, Collins AG, Lieberman BS. Exceptionally preserved jellyfishes from the Middle Cambrian. PLoS ONE, 2007, 2 e1121

[25]

Chamberlin ME. Changes in mitochondrial electron transport chain activity during insect metamorphosis. Am J Physiol Regul Integr Comp Physiol, 2007, 292: 1016-1022

[26]

Chuard PJC, Johnson MD, Guichard F. Ocean acidification causes mortality in the medusa stage of the cubozoan Carybdea xaymacana. Sci Rep, 2019, 9: 1-6

[27]

Chuin TT. Le cycle évolutif du scyphistome de Chrysaora. Étude histophysiologique. Trav Stn Biol Roscoff, 1930, 8: 1-179

[28]

Cloud P, Glaes MF. The ediacarian period and system: metazoa inherit the earth. Science, 1982, 217: 783-792

[29]

Collins AG. Phylogeny of medusozoa and the evolution of cnidarian life cycles. J Evol Biol, 2002, 15: 418-432

[30]

Conover WJ, Iman RL. Rank transformations as a bridge between parametric and nonparametric statistics. Am Stat, 1981, 35: 124-129

[31]

De Coen WM, Janssen CR. The use of biomarkers in Daphnia magna toxicity testing. IV. Cellular energy allocation: a new methodology to assess the energy budget of toxicant-stressed Daphnia populations. J Aquat Ecosyst Stress Recovery, 1997, 6: 43-55

[32]

Dong Z, Sun T. Combined effects of ocean acidification and temperature on planula larvae of the moon jellyfish Aurelia coerulea. Mar Environ Res, 2018, 139: 144-150

[33]

Dubois M, Gilles K, Hamilton JK, Rebers PA, Smith F. A colorimetric method for the determination of sugars. Nature, 1956, 168: 350-356

[34]

Falkenhaug T. Review of jellyfish blooms in the Mediterranean and Black Sea. Mar Biol Res, 2014, 10: 1038-1039

[35]

Fernández-Urruzola I, Packard TT, Gómez M. GDH activity and ammonium excretion in the marine mysid, Leptomysis lingvura: effects of age and starvation. J Exp Mar Biol Ecol, 2011, 409: 21-29

[36]

Fernández-Urruzola I, Osma N, Gómez M, Montesdeoca-Esponda S, Packard TT. Building a model of ammonium excretion in two species of marine zooplankton based on glutamate dehydrogenase kinetics. Mar Ecol Prog Ser, 2016, 550: 83-99

[37]

Fernández-Urruzola I, Osma N, Gómez M, Pollehne F, Postel L, Packard TT. Modelling downward particulate organic nitrogen flux from zooplankton ammonium regeneration in the northern Benguela. Prog Oceanogr, 2016, 149: 121-133

[38]

Fernández-Urruzola I (2015) Understanding the zooplankton ammonium excretion: from biogeochemical implications to intracellular regulatory mechanisms. Universidad de Las Palmas de Gran Canaria

[39]

Foo SA, Byrne M. Acclimatization and adaptive capacity of marine species in a changing ocean. Adv Mar Biol, 2016, 74: 69-116

[40]

Frandsen KT, Riisgård HU. Size-dependent respiration and growth of jellyfish, Aurelia aurita. Sarsia, 1997, 82: 307-312

[41]

Fu Z, Uye S-I. Starvation of the respiratory metabolism and locomotion of Aurelia aurita s.l. ephyrae. Open J Mar Sci, 2021, 11: 1-16

[42]

Fuchs B, Wang W, Graspeuntner S, Li Y, Insua S, Herbst EM, Dirksen P, Böhm AM, Hemmrich G, Sommer F, Domazet-Lošo T, Klostermeier UC, Anton-Erxleben F, Rosenstiel P, Bosch TCG, Khalturin K. Regulation of polyp-to-jellyfish transition in Aurelia aurita. Curr Biol, 2014, 24: 263-273

[43]

Gambill M, Peck MA. Respiration rates of the polyps of four jellyfish species: potential thermal triggers and limits. J Exp Mar Biol Ecol, 2014, 459: 17-22

[44]

Garcıa-Esquivel Z, Bricelj VM, Gonzalez-Gomez MA. Physiological basis for energy demands and early postlarval mortality in the Pacific oyster, Crassostrea gigas. J Exp Mar Biol Ecol, 2001, 263: 77-103

[45]

Gerber U, Huebner R, Rossberg A, Krawczyk-Baersch E, Merroun ML. Metabolism-dependent bioaccumulation of uranium by Rhodosporidium toruloides isolated from the flooding water of a former uranium mine. PLoS ONE, 2018, 13 e0201903

[46]

Gibbin EM, Massamba N’Siala G, Chakravarti LJ, Jarrold MD, Calosi P. The evolution of phenotypic plasticity under global change. Sci Rep, 2017, 7: 17253

[47]

Goldstein J, Steiner UK. Ecological drivers of jellyfish blooms – the complex life history of a ‘well-known’ medusa (Aurelia aurita). J Anim Ecol, 2019, 89: 910-920

[48]

Gómez M, Torres S, Hernzández-León S. Modification of the electron transport system (ETS) method for routine measurements of respiratory rates of zooplankton. S Afr J Mar Sci, 1996, 17: 15-20

[49]

González-Valdovinos M, Ocampo L, Tovar-Ramírez D. Evaluation of digestive capacity in the polyp, ephyrae, and medusae stages of the cannonball jellyfish Stomolophus meleagris. Hydrobiologia, 2019, 828: 259-269

[50]

Hadfield MG. Why and how marine-invertebrate larvae metamorphose so fast. Semin Cell Dev Biol, 2000, 11: 437-443

[51]

Hadži J. An attempt to reconstruct the system of animal classification. Syst Zool, 1953, 2: 145-154

[52]

Haeckel E (1879) Das system der Medusen: Erster Teil einer Monographie der Medusen. Denkschriften der Medicinisch-Naturwissenschaftlichen Gesellschaft zu Jena. 1: XX+1–360, 320 plates.

[53]

Han C, Chae J, Jin J, Yoon W. Estimation of the minimum food requirement using the respiration rate of medusa of Aurelia aurita in Sihwa Lake. Ocean Sci J, 2012, 47: 155-160

[54]

Hassan SM, Rahman RA. Effects of exposure to magnetic field on water properties and hatchability of Artemia salina. J Agr Biol Sci, 2016, 11: 416-423

[55]

Hernández-León S, Gómez M. Factors affecting the respiration/ETS ratio in marine zooplankton. J Plankton Res, 1996, 18: 239-255

[56]

Hernandez-Leon S, Torres S. The relationship between ammonia excretion and GDH activity in marine zooplankton. J Plankton Res, 1997, 19: 587-601

[57]

Hubot ND, Giering SLC, Füssel J, Robidart J, Birchill A, Stinchcombe M, Dumousseaud C, Lucas CH. Evidence of nitrification associated with globally distributed pelagic jellyfish. Limnol Oceanogr, 2021, 66: 2159-2173

[58]

Hubot ND, Giering SLC, Lucas CH. Similarities between the biochemical composition of jellyfish body and mucus. J Plankton Res, 2022, 44: 337-344

[59]

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

[60]

Ishii H, Bamstedt U. Food regulation of growth and maturation in a natural population of Aurelia aurita (L.). J Plankton Res, 1998, 20: 805-816

[61]

Kattner G, Hagen W, Lee RF, Campbell R, Deibel D, Falk-Petersen S, Graeve M, Hansen BW, Hirche HJ, Jónasdóttir SH, Madsen ML, Mayzaud P, Müller-Navarra D, Nichols PD, Paffenhöfer GA, Pond D, Saito H, Stübing D, Virtue P. Perspectives on marine zooplankton lipids. Can J Fish Aquat Sci, 2007, 64: 1628-1639

[62]

Khong NMH, Yusoff FM, Jamilah B, Basri M, Maznah I, Chan KW, Nishikawa J. Nutritional composition and total collagen content of three commercially important edible jellyfish. Food Chem, 2016, 196: 953-960

[63]

King FD, Packard TT. Respiration and the activity of the respiratory electron transport system in marine zooplankton. Limnol Oceanogr, 1975, 20: 849-854

[64]

Kinoshita J, Hiromi J, Kadota S. Do respiratory metabolic rates of the scyphomedusa Aurelia aurita scale isometrically throughout ontogeny in a sexual generation?. Hydrobiologia, 1997, 347: 51-55

[65]

Klein SG, Pitt KA, Rathjen KA, Seymour JE. Irukandji jellyfish polyps exhibit tolerance to interacting climate change stressors. Glob Chang Biol, 2014, 20: 28-37

[66]

Knight JA, Anderson S, Rawle JM. Chemical basis of the sulfo-phospho-vanillin reaction for estimating total serum lipids. Clin Chem, 1972, 18: 199-202

[67]

Korschelt E, Heider K (1890) Lehrbuch der vergleichenden Entwicklungsgeschichte der wirbellosen Tiere.

[68]

Kotova AV, Kovtun OA, Podgornaya OI, Adonin LS. Mesoglein differences between two jellyfish populations of the genus Aurelia. Int Aquat Res, 2015, 7: 123-131

[69]

Kraus JE, Fredman D, Wang W, Khalturin K, Technau U. Adoption of conserved developmental genes in development and origin of the medusa body plan. EvoDevo, 2015, 6: 23

[70]

Kuniyoshi H, Okumura I, Kuroda R, Tsujita N, Arakawa K, Shoji J, Saito T, Osada H. Indomethacin induction of metamorphosis from the asexual stage to sexual stage in the moon jellyfish, Aurelia aurita. Biosci Biotechnol Biochem, 2012, 76: 1397-1400

[71]

Larson RJ. A note on the feeding, growth, and reproduction of the epipelagic scyphomedusa Pelagia noctiluca (Forskal). Biol Oceanogr, 1987, 4: 447-454

[72]

Lee SH, Tseng LC, Yoon YH, Ramirez-Romero E, Hwang JS, Molinero JC. The global spread of jellyfish hazards mirrors the pace of human imprint in the marine environment. Environ Int, 2023, 171 107699

[73]

Lilley MKS, Lombard F. Respiration of fragile planktonic zooplankton: extending the possibilities with a single method. J Exp Mar Biol Ecol, 2015, 471: 226-231

[74]

Locke M. Gilbert LI, Frieden E. Cell structure during insect metamorphosis. Metamorphosis, 1981, Boston, MA, Springer75103

[75]

Loveridge A, Lucas CH. Transgenerational effects influence acclimation to varying temperatures in Aurelia aurita polyps (cnidaria: scyphozoa). Hydrobiologia, 2023, 850: 1955-1967

[76]

Loveridge A, Lucas CH, Pitt KA. Shorter, warmer winters may inhibit production of ephyrae in a population of the moon jellyfish Aurelia aurita. Hydrobiologia, 2021, 848: 739-749

[77]

Loveridge A, Lucas CH, Ford D. Influence of in situ temperature and maternal provisioning on the medusa-to-polyp transition in a year-round population of the scyphozoan Aurelia aurita. J Mar Biol Assoc UK, 2024, 104 e58

[78]

Lowe WH, Martin TE, Skelly DK, Woods HA. Metamorphosis in an era of increasing climate variability. Trends Ecol Evol, 2021, 36: 360-375

[79]

Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the folin phenol reagent. J Biol Chem, 1951, 193: 265-275

[80]

Lu Y, Lucas C, Loveridge A. Transgenerational acclimation influences asexual reproduction in Aurelia aurita jellyfish polyps in response to temperature. Mar Ecol Prog Ser, 2020, 656: 35-50

[81]

Lucas CH. Biochemical composition of Aurelia aurita in relation to age and sexual maturity. J Exp Mar Biol Ecol, 1994, 183: 179-192

[82]

Lucas CH. Reproduction and life history strategies of the common jellyfish, Aurelia aurita, in relation to its ambient environment. Hydrobiologia, 2001, 451: 229-246

[83]

Lucas CH, Graham WM, Widmer C (2012) Jellyfish life histories: Role of polyps in forming and maintaining scyphomedusa populations. In: Lesser M (ed) Advances in marine biology. Vol. 63. Elsevier Ltd., pp 133–196

[84]

Lynam CP, Gibbons MJ, Axelsen BE, Sparks CA, Coetzee J, Heywood BG, Brierley AS. Jellyfish overtake fish in a heavily fished ecosystem. Curr Biol, 2006, 16: R492-R493

[85]

Mangum CP, Oakes MJ, Shick JM. Rate-temperature responses in scyphozoan medusae and polyps. Mar Biol, 1972, 15: 298-303

[86]

Markwell MAK, Haas SM, Bieber LL, Tolbert NE. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal Biochem, 1978, 87: 206-210

[87]

Marques AC, Collins AG. Cladistic analysis of Medusozoa and cnidarian evolution. Invertebr Biol, 2004, 123: 23-42

[88]

Marsh JB, Weinstein DB. Simple charring method for determination of lipids. J Lipid Res, 1966, 7: 574-576

[89]

Martínez I, Gómez M, Packard TT. Potential respiration is a better respiratory predictor than biomass in young Artemia salina. J Exp Mar Biol Ecol, 2010, 390: 78-83

[90]

Martínez I, Herrera A, Tames-espinosa M, Bondyale-juez DR, Romero-Kutzner V, Packard TT, Gómez M. Protein in marine plankton: a comparison of spectrophotometric methods. J Exp Mar Biol Ecol, 2020, 526 151357

[91]

Matsakis S, Conover RJ. Abundance and feeding of medusae and their potential impact as predators on other zooplankton in Bedford Basin (Nova Scotia, Canada) during spring. Can J Fish Aquat Sci, 1991, 48: 1419-1430

[92]

Matveev IV, Adonin LS, Shaposhnikova TG, Podgornaya OI. Aurelia aurita cnidarian with a prominenmedusiod stage. J Exp Zool B Mol Dev Evol, 2012, 318: 1-12

[93]

Møller LF, Riisgård HU. Respiration in the scyphozoan jellyfish Aurelia aurita and two hydromedusae (Sarsia tubulosa and Aequorea vitrina): effect of size, temperature and growth. Mar Ecol Prog Ser, 2007, 330: 149-154

[94]

Muscatine L, Marian RE. Dissolved inorganic nitrogen flux in symbiotic and nonsymbiotic medusae. Limnol Oceanogr, 1982, 27: 910-917

[95]

Nelson DL, Cox MM (2008) Lehninger principles of biochemistry. W. H. Freeman, New York

[96]

Nemazie DA, Purcell JE, Glibert PM. Ammonium excretion by gelatinous zooplankton and their contribution to the ammonium requirements of microplankton in Chesapeake Bay. Mar Biol, 1993, 116: 451-458

[97]

Nestel D, Tolmasky D, Rabossi A, Quesada-allué LA. Lipid, carbohydrates and protein patterns during metamorphosis of the mediterranean fruit fly, Ceratitis capitata (diptera: tephritidae). Ann Entomol Soc Am, 2003, 96: 237-244

[98]

Nordström K, Wallén R, Seymour J, Nilsson D. A simple visual system without neurons in jellyfish larvae. Proc R Soc B-Biol Sci, 2003, 270: 2349-2354

[99]

O’Boyle RN, Beamish FWH. Growth and intermediary metabolism of larval and metamorphosing stages of the landlocked sea lamprey, Petromyzon marinus L. Environ Biol Fishes, 1977, 2: 103-120

[100]

Olesen NJ, Frandsen K, Riisgard HU. Population dynamics, growth and energetics of jellyfish Aurelia aurita in a shallow fjord. Mar Ecol Prog Ser, 1994, 105: 9-18

[101]

Olguín-Jacobson C, Pitt KA, Carroll AR, Melvin SD. Chronic pesticide exposure elicits a subtle carry-over effect on the metabolome of Aurelia coerulea ephyrae. Environ Pollut, 2021, 275 116641

[102]

Osma N, Fernández-Urruzola I, Gómez M, Montesdeoca-Esponda S, Packard TT. Predicting in vivo oxygen consumption rate from ETS activity and bisubstrate enzyme kinetics in cultured marine zooplankton. Mar Biol, 2016, 163: 146

[103]

Östman C. Abundance, feeding behaviour and nematocysts of scyphopolyps (Cnidaria) and nematocysts in their predator, the nudibranch Coryphella verrucosa (Mollusca). Hydrobiologia, 1997, 355: 21-28

[104]

Packard TT. The measurement of respiratory electron-transport activity in marine phytoplankton. J Mar Res, 1971, 29: 235-244

[105]

Packard TT. Williams PJ, Jannasch HW. Measurement of electron transport activity of marine microplankton. Advances in aquatic microbiology, Vol. 3, 1985, New York, Academic Press207261

[106]

Packard TT (1985b) Oxygen consumption in the ocean: measuring and mapping with enzyme analysis. In: Zirino A (ed) Mapping strategies in chemical oceanography. Advances in Chemistry, Vol 209. American Chemical Society: Washington, DC, pp 177–209

[107]

Packard TT, Christensen JP. Respiration and vertical carbon flux in the Gulf of Maine water column. J Mar Res, 2004, 62: 93-115

[108]

Packard TT, Harmon D, Boucher J. Respiratory electron transport activity in plankton from upwelled waters. Tethys, 1974, 6: 213-222

[109]

Pandori LLM, Sorte CJB. The weakest link: sensitivity to climate extremes across life stages of marine invertebrates. Oikos, 2019, 128: 621-629

[110]

Pineda MC, McQuaid CD, Turon X, López-Legentil S, Ordóñez V, Rius M. Tough adults, frail babies: an analysis of stress sensitivity across early life-history stages of widely introduced marine invertebrates. PLoS ONE, 2012, 7 e46672

[111]

Pitt KA, Lucas CH. Jellyfish blooms, 2014, London, Springer

[112]

Pitt KA, Duarte CM, Lucas CH, Sutherland KR, Condon RH, Mianzan H, Purcell JE, Robinson KL, Uye SI. Jellyfish body plans provide allometric advantages beyond low carbon content. PLoS ONE, 2013, 8: 1-10

[113]

Purcell JE, Kremer P. Feeding and metabolism of the siphonophore Sphaeronectes gracilis. J Plankton Res, 1983, 5: 95-106

[114]

Purcell JE, Uye SI, Lo WT. Anthropogenic causes of jellyfish blooms and their direct consequences for humans: a review. Mar Ecol Prog Ser, 2007, 350: 153-174

[115]

Purcell JE, Fuentes V, Atienza D, Tilves U, Astorga D, Kawahara M, Hays GC. Use of respiration rates of scyphozoan jellyfish to estimate their effects on the food web. Hydrobiologia, 2010, 645: 135-152

[116]

Purcell JE, Bondyale-Juez DR, Romero-Kutzner V, Martínez I, Caprioli R, Tames-Espinosa M, Almunia J, Alonso E, Packard TT, Gómez M. Food supply effects on the asexual reproduction and respiratory metabolism of Aurelia aurita polyps. Hydrobiologia, 2019, 846: 135-146

[117]

R Core Team (2017) R: A language and environment for statistical computing.

[118]

Richardson AJ, Bakun A, Hays GC, Gibbons MJ. The jellyfish joyride: causes, consequences and management responses to a more gelatinous future. Trends Ecol Evol, 2009, 24: 312-322

[119]

Riisgård HU, Larsen PS. Bioenergetic model and specific growth rates of jellyfish Aurelia spp. Mar Ecol Prog Ser, 2022, 688: 49-56

[120]

Roberts J. Thermal acclimation of metabolism in the crab Pachygrapsus crassipes Randall. i. The influence of body size, starvation, and molting. Physiol Zool, 1957, 30: 232-242

[121]

Romero-Kutzner V, Packard TT, Berdalet E, Roy SO, Gagné JP, Gómez M. Respiration quotient variability: bacterial evidence. Mar Ecol Prog Ser, 2015, 519: 47-59

[122]

Roy S, Packard T. CO2 production rate predicted from isocitrate dehydrogenase activity, intracellular substrate concentrations and kinetic constants in the marine bacterium Pseudomonas nautica. Mar Biol, 2001, 138: 1251-1258

[123]

Russell FS. The medusae of the British Isles volume II: pelagic scyphozoa, with a supplement to the first volume of hydromedusae, 1970, Cambridge, Cambridge University Press

[124]

Rutter WJ. Wilt FH, Wessels NK. Protein determinations in embryos. Methods in developmental biology, 1967, London, Academic P671683

[125]

Salvini-Plawen LV. Mesopsammic cnidaria from Plymouth (with systematic notes). J Mar Biol Assoc UK, 1987, 67: 623-637

[126]

Sanz-Martín M, Pitt KA, Condon RH, Lucas CH, Novaes de Santana C, Duarte CM. Flawed citation practices facilitate the unsubstantiated perception of a global trend toward increased jellyfish blooms. Glob Ecol Biogeogr, 2016, 25: 1039-1049

[127]

Schneider G. Estimation of food demands of Aurelia aurita medusae populations in the Kiel bight/western Baltic. Ophelia, 1989, 31: 17-27

[128]

Seipp S, Schmich J, Leitz T. Apoptosis – a death-inducing mechanism tightly linked with morphogenesis in Hydractina echinata (Cnidaria, Hydrozoa). Development, 2001, 128: 4891-4898

[129]

Shimauchi H, Uye SI. Excretion and respiration rates of the scyphomedusa Aurelia aurita from the Inland Sea of Japan. J Oceanogr, 2007, 63: 27-34

[130]

Shingala MC, Rajyaguru A. Comparison of post hoc tests for unequal variance. Int J New Technol Sci Eng, 2015, 2: 22-33

[131]

Sizer IW. Effects of temperature on enzyme kinetics. Adv Enzymol Relat Areas Mol Biol, 1943, 3: 35-62

[132]

Solorzano L. Determination of ammonia in natural waters by the phenolhypochlorite method. Limnol Oceanogr, 1969, 14: 799-801

[133]

St-Amand L, Gagnon R, Packard TT, Savenkoff C. Effects of inorganic mercury on the respiration and the swimming activity of shrimp larvae, Pandalus borealis. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol, 1999, 122: 33-43

[134]

Stenvers V, Chi X, Javidpour J. Seasonal variability of the fatty acid composition in Aurelia aurita (Cnidaria: Scyphozoa): implications for gelativore food web studies. J Plankton Res, 2020, 42: 440-452

[135]

Sukhoputova AV, Kraus YA. Environmental factors inducing the transformation of polyp into medusae in Aurelia aurita (scyphozoa). Russ J Dev Biol, 2017, 48: 106-116

[136]

Sweetman AK, Chelsky A, Pitt KA, Andrade H, van Oevelen D, Renaud PE. Jellyfish decomposition at the seafloor rapidly alters biogeochemical cycling and carbon flow through benthic food-webs. Limnol Oceanogr, 2016, 61: 1449-1461

[137]

Takao M, Okawachi H, Uye SI, Okawachi H. Natural predators of polyps of Aurelia aurita s.l. (Cnidaria: Scyphozoa: Semaeostomeae) and their predation rates. Plankton Benthos Res, 2014, 9: 105-113

[138]

Tames-Espinosa M, Martínez I, Romero-Kutzner V, Bondyale-Juez DR, Packard TT, Gomez M. NADP+-dependent isocitrate dehydrogenase activity in marine plankton. Mar Chem, 2018, 204: 86-94

[139]

Thompson WE (1993) Protein expression during Aurelia development. Dissertation, Rutgers, The State University of New Jersey

[140]

Thuesen EV, Childress JJ. Oxygen consumption rates and metabolic enzyme activities of oceanic California medusae in relation to body size and habitat depth. Biol Bull, 1994, 187: 84-98

[141]

Tinta T, Zhao Z, Escobar A, Klun K, Bayer B, Amano C, Bamonti L, Herndl GJ. Microbial processing of jellyfish detritus in the ocean. Front Microbiol, 2020, 11 590995

[142]

Treible LM, Condon RH. Temperature-driven asexual reproduction and strobilation in three scyphozoan jellyfish polyps. J Exp Mar Biol Ecol, 2019, 520 151204

[143]

Treible LM, Pitt KA, Klein SG, Condon RH. Exposure to elevated pCO2 does not exacerbate reproductive suppression of Aurelia aurita jellyfish polyps in low oxygen environments. Mar Ecol Prog Ser, 2018, 591: 129-139

[144]

Uye S, Shimauchi H. Population biomass, feeding, respiration and growth rates, and carbon budget of the scyphomedusa Aurelia aurita in the Inland Sea of Japan. J Plankton Res, 2005, 27: 237-248

[145]

van der Lee GH, Kraak MHS, Verdonschot RCM, Verdonschot PFM. Persist or perish: critical life stages determine the sensitivity of invertebrates to disturbances. Aquat Sci, 2020, 82: 1-11

[146]

von Montfort GM, Costello JH, Colin SP, Morandini AC, Migotto AE, Maronna MM, Reginato M, Miyake H, Nagata RM. Ontogenetic transitions, biomechanical trade-offs and macroevolution of scyphozoan medusae swimming patterns. Sci Rep, 2023, 13: 9760

[147]

Wang W, Wang M, Wang H. Effects of temperature on asexual reproduction and jellyfish booms of Aurelia aurita: insights from mathematical modeling. Ecol Modell, 2025, 499 110915

[148]

Weihrauch D, Allen GJP. Ammonia excretion in aquatic invertebrates: new insights and questions. J Exp Biol, 2018, 221 jeb169219

[149]

Wittig K, Kasper J, Seipp S, Leitz T. Evidence for an instructive role of apoptosis during the metamorphosis of Hydractinia echinata (Hydrozoa). Zoology, 2011, 114: 11-22

[150]

Wright PA. Nitrogen excretion: three end products, many physiological roles. J Exp Biol, 1995, 198: 273-281

[151]

Yuan D, Nakanishi N, Jacobs DK, Hartenstein V. Embryonic development and metamorphosis of the scyphozoan Aurelia. Dev Genes Evol, 2008, 218: 525-539

RIGHTS & PERMISSIONS

The Author(s)

AI Summary AI Mindmap
PDF

13

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/