Abstract
Phenomena such as global warming, rising sea temperatures and extreme weather and climate anomalies such as floods and heat waves have been shown to alter absolute salinity values. While affecting marine and estuarine population dynamics, these scenarios may also favour the invasion and proliferation of opportunistic and potentially harmful species in new geographical areas—such as blooming jellyfish. These organisms are one of the less studied taxa, particularly the proliferative asexual benthic phase, to which effects of in situ and experimental global change scenarios are poorly addressed. Acclimation and plasticity to global change scenarios were individually assessed through life history and physiological responses (survival, settlement time, time until maturity, feeding activity, asexual reproduction and behaviour) of laboratory-reared ciliated buds and polyps (= scyphostomae) of the invasive Phyllorhiza punctata (Cnidaria: Rhizostomeae). The present study evaluated the effects of two temperature levels (21 °C—current thermal scenario, or 25 °C—warming scenario) and six salinity regimes resembling estuarine and marine conditions (15, 20, 25, 30, 35 or 40) during 21 days. Under warming, P. punctata scyphostomae showed faster development and budding rates upon estuarine-like salinities, but higher mortality and reduced development under marine-like conditions—an ecological niche trade-off since at 21 °C such pattern was not found. Overall, our results suggest that global changes might prompt P. punctata proliferation through polyp colonisation mainly in estuarine areas and potentially increase blooming events with further implications at local and regional scales.
Similar content being viewed by others
Availability of data and material
The datasets generated and analysed during the current study are available from the corresponding author on reasonable request.
References
Abed-Navandi D, Kikinger R (2007) First record of the tropical scyphomedusa Phyllorhiza punctata von Lendenfeld, 1884 (Cnidaria: Rhizostomeae) in the Central Mediterranean Sea. Aquat Invasions 2:391–394. https://doi.org/10.3391/ai.2007.2.4.7
Algueró-Muñiz M, Meunier CL, Holst S, Alvarez-Fernandez S, Boersma M (2016) Withstanding multiple stressors: ephyrae of the moon jellyfish (Aurelia aurita, Scyphozoa) in a high-temperature, high-CO2 and low-oxygen environment. Mar Biol. https://doi.org/10.1007/s00227-016-2958-z
Anderson TR, Hawkins E, Jones PD (2016) CO2, the greenhouse effect and global warming: from the pioneering work of Arrhenius and Callendar to today’s Earth System Models. Endeavour. https://doi.org/10.1016/j.endeavour.2016.07.002
Avian M, Motta G, Prodan M, Tordoni E, Macaluso V, Beran A, Goruppi A, Bacaro G, Tirelli V (2021) Asexual reproduction and strobilation of Sanderia malayensis (Scyphozoa, Pelagiidae) in relation to temperature: experimental evidence and implications. Diversity 13:37. https://doi.org/10.3390/d13020037
Boero, F (2014) Review of Jellyfish Blooms in the Mediterranean and Black Sea. Marine Biology Research 10(10):1038–1039. https://doi.org/10.1080/17451000.2014.880790
Boyd PW, Collins S, Dupont S, Fabricius K, Gattuso JP, Havenhand J, Hutchins DA, McGraw CM, Riebesell U, Vichi M, Biswas H, Ciotti A, Dillingham P, Gao K, Gehlen M, Hurd CL, Kurihara H, Navarro J, Nilsson GE, Passow U, Portner H-O (2019) SCOR WG149 handbook to support the SCOR best practice guide for “Multiple Drivers” marine research. University of Tasmania for Scientific Committee on Oceanic Research, Hobart
Ceh J, Gonzalez J, Pacheco AS, Riascos JM (2015) The elusive life cycle of scyphozoan jellyfish—Metagenesis revisited. Sci Rep 5:1–13. https://doi.org/10.1038/srep12037
Chapin FS, Zavaleta ES, Eviner VT, Naylor RL, Vitousek PM, Reynolds HL, Hooper DU, Lavorel S, Sala OE, Hobbie SE, Mack MC, Díaz S (2000) Consequences of changing biodiversity. Nature 405:234–242. https://doi.org/10.1038/35012241
Condon RH, Duarte CM, Pitt KA, Robinson KL, Lucas CH, Sutherland KR, Mianzan HW, Bogeberg M, Purcell JE, Decker MB, Uye S, Madin LP, Brodeur RD, Haddock SHD, Malej A, Parry GD, Eriksen E, Quiñones J, Acha M, Harvey M, Arthur JM, Graham WM (2013) Recurrent jellyfish blooms are a consequence of global oscillations. Proc Natl Acad Sci USA 110:1000–1005. https://doi.org/10.1073/pnas.1210920110
Courtney R, Browning S, Northfield T, Seymour J (2016) Thermal and osmotic tolerance of “Irukandji” Polyps: Cubozoa; Carukia barnesi. PLoS ONE. https://doi.org/10.1371/journal.pone.0159380
Cuthbert RN, Pattison Z, Taylor NG, Verbrugge L, Diagne C, Ahmed DA, Leroy B, Angulo E, Briski E, Capinha C, Catford JA, Dalu T, Essl F, Gozlan RE, Haubrock PJ, Kourantidou M, Kramer AM, Renault D, Wasserman RJ, Courchamp F (2021) Global economic costs of aquatic invasive alien species. Sci Total Environ 775:145238. https://doi.org/10.1016/J.SCITOTENV.2021.145238
Darnell MZ, Nicholson HS, Munguia P (2015) Thermal ecology of the fiddler crab Uca panacea: thermal constraints and organismal responses. J Therm Biol 52:157–165. https://doi.org/10.1016/J.JTHERBIO.2015.06.004
Dong J, Sun M, Purcell JE, Chai Y, Zhao Y, Wang A (2015) Effect of salinity and light intensity on somatic growth and podocyst production in polyps of the giant jellyfish Nemopilema nomurai (Scyphozoa: Rhizostomeae). Hydrobiologia 754:75–83. https://doi.org/10.1007/s10750-014-2087-y
Durack PJ, Wijffels SE, Matear RJ (2012) Ocean salinities reveal strong global water cycle intensification during 1950 to 2000. Science 80(336):455–458. https://doi.org/10.1126/science.1212222
Fabry VJ, Seibel BA, Feely RA, Orr JC (2008) Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J Mar Sci 65:414–432. https://doi.org/10.1093/icesjms/fsn048
Galil BS, Shoval L, Goren M (2009) Phyllorhiza punctata von Lendenfeld, 1884 (Scyphozoa: Rhizostomeae: Mastigiidae) reappeared off the Mediterranean coast of Israel. Aquat Invasions 4:481–483. https://doi.org/10.3391/ai.2009.4.3.6
Gambill M, McNaughton SL, Kreus M (2018) Temperature-dependent settlement of planula larvae of two scyphozoan jellyfish from the North Sea. Estuar Coast Shelf Sci 201:64–71. https://doi.org/10.1016/J.ECSS.2016.08.042
Graham WM, Martin DL, Felder DL, Asper VL, Perry HM (2003) Ecological and economic implications of a tropical jellyfish invader in the Gulf of Mexico. Biol Invasions 5:53–69. https://doi.org/10.1023/A:1024046707234
Gröndahl F (1988) Interactions between polyps of Aurelia aurita and planktonic larvae of scyphozoans: an experimental study. Mar Ecol Prog Ser 45:87–93. https://doi.org/10.3354/meps045087
Gueroun SKM, Yahia OK-D, Deidun A, Fuentes V, Piraino S, Yahia MND, Yahia OK-D (2015) First record and potential trophic impact of Phyllorhiza punctata (Cnidaria: Scyphozoa) along the north Tunisian coast (South Western Mediterranean Sea). Ital J Zool 82:95–100. https://doi.org/10.1080/11250003.2014.981306
Haddad M, Júnior MN (2006) Reappearance and seasonality of Phyllorhiza punctata von Lendenfeld (Cnidaria, Scyphozoa, Rhizostomeae) medusae in southern Brazil. Rev Bras Zool 23:824–831. https://doi.org/10.1590/S0101-81752006000300030
Han C-H, Uye S-I (2010) Combined effects of food supply and temperature on asexual reproduction and somatic growth of polyps of the common jellyfish Aurelia aurita s.l. Plankt Benthos Res 5:98–105
Hernroth B, Sköld HN, Wiklander K, Jutfelt F, Baden S (2012) Simulated climate change causes immune suppression and protein damage in the crustacean Nephrops norvegicus. Fish Shellfish Immunol. https://doi.org/10.1016/j.fsi.2012.08.011
Hunt HL, Scheibling RE (1997) Role of early post-settlement mortality in recruitment of benthic marine invertebrates. Mar Ecol Prog Ser 155:269–301
IPCC (2014) Climate Change 2014. Impacts, adaptation, and vulnerability part A: global and sectoral aspects. IPCC
Kaiser R (2016) Husbandry of jellyfish, from the beginning until today. Der Zool Garten 85:52–63. https://doi.org/10.1016/j.zoolgart.2015.09.009
Kamiyama T (2013) Planktonic ciliates as food for the scyphozoan Aurelia aurita (s.l.): effects on asexual reproduction of the polyp stage. J Exp Mar Biol Ecol 445:21–28. https://doi.org/10.1016/j.jembe.2013.03.018
Kniebusch M, Meier HEM, Radtke H (2019) Changing salinity gradients in the baltic sea as a consequence of altered freshwater budgets. Geophys Res Lett 46:9739–9747. https://doi.org/10.1029/2019GL083902
Kogovšek T, Bogunović B, Malej A (2010) Recurrence of bloom-forming scyphomedusae: wavelet analysis of a 200-year time series. Jellyfish blooms: new problems and solutions. Springer, pp 81–96
Lachkar Z (2014) Effects of upwelling increase on ocean acidification in the California and Canary Current systems. Geophys Res Lett 41:90–95. https://doi.org/10.1002/2013GL058726
Leandro S, Queiroga H, Rodríguez-Graña L, Tiselius P (2006) Temperature-dependent development and somatic growth in two allopatric populations of Acartia clausi (Copepoda: Calanoida). Mar Ecol Prog Ser 322:189–197. https://doi.org/10.3354/meps322189
Little S, Wood PJ, Elliott M (2017) Quantifying salinity-induced changes on estuarine benthic fauna: the potential implications of climate change. Estuar Coast Shelf Sci 198:610–625. https://doi.org/10.1016/J.ECSS.2016.07.020
Liu W-C, Lo W-T, Purcell JE, Chang H-H (2009) Effects of temperature and light intensity on asexual reproduction of the scyphozoan, Aurelia aurita (L.) in Taiwan. Hydrobiologia 616:247–258. https://doi.org/10.1007/s10750-008-9597-4
Lucas CH (2001) Reproduction and life history strategies of the common jellyfish, Aurelia aurita, in relation to its ambient environment. Hydrobiologia 451:229–246. https://doi.org/10.1023/A:1011836326717
Lucas CH, Horton AA (2014) Short-term effects of the heavy metals, Silver and copper, on polyps of the common jellyfish, Aurelia aurita. J Exp Mar Biol Ecol 461:154–161. https://doi.org/10.1016/J.JEMBE.2014.08.003
Madeira D, Narciso L, Diniz MS, Vinagre C (2014) Synergy of environmental variables alters the thermal window and heat shock response: an experimental test with the crab Pachygrapsus marmoratus. Mar Environ Res 98:21–28. https://doi.org/10.1016/j.marenvres.2014.03.011
Marques D, Marques S, Duarte I, Dupont S, Leandro S (2019) Effects of ocean acidification on growth and feeding rates of spotted jellyfish Phyllorhiza punctata early life stage/polyps. Front Mar Sci. https://doi.org/10.3389/CONF.FMARS.2019.08.00131
Miller M-EC, Graham WM (2012) Environmental evidence that seasonal hypoxia enhances survival and success of jellyfish polyps in the northern Gulf of Mexico. J Exp Mar Biol Ecol 432:113–120. https://doi.org/10.1016/j.jembe.2012.07.015
Mills CE (2001) Jellyfish blooms: are populations increasing globally in response to changing ocean conditions? Jellyfish blooms: ecological and societal importance. Springer, Dordrecht, pp 55–68
Miranda FA (2016) Ensaios de reprodução da medusa Phyllorhiza punctata para fins ornamentais. Master Thesis Dissertation, Polytechnic Institute of Leiria
Molinero J-C, Batistić M, Daly-Yahia N, Daly Yahia-Kefi O, Lučić D, Fernadez de Puelles M, Kamburska L, Licandro P, Malej alenka, Prieto L, Sikou-Frangous I, Zervoudaki S (2009) Climate and jellyfish aotburtsts in the Mediterranean Sea: a synthesis through meta-analysis. In: 3rd GLOBEC Open Sci Meet from Ecosyst Funct to Predict, p 137
Ocaña-Luna A, Sánchez-Ramírez M, Aguilar-Durán R (2010) First record of Phyllorhiza punctata von Lendenfeld, 1884 (Cnidaria : Scyphozoa, Mastigiidae ) in Mexico. Aquat Invasions 5:79–84. https://doi.org/10.3391/ai.2010.5.S1.017
Pascual M, Fuentes V, Canepa A, Atienza D, Gili J-M, Purcell JE (2015) Temperature effects on asexual reproduction of the scyphozoan Aurelia aurita s.l.: differences between exotic (Baltic and Red seas) and native (Mediterranean Sea) populations. Mar Ecol 36:994–1002. https://doi.org/10.1111/maec.12196
Pearson RG, Dawson TP (2003) Predicting the impacts of climate change on the distribution of species: are bioclimate envelope models useful? Glob Ecol Biogeogr 12:361–371. https://doi.org/10.1046/j.1466-822X.2003.00042.x
Perry AL (2005) Climate change and distribution shifts in marine fishes. Science 308:1912–1915. https://doi.org/10.1126/science.1111322
Pitt K, Purcell JE (2009) Jellyfish blooms, causes, consequences, and recent advances. Developments in Hydrobioloy 1–289. https://doi.org/10.1007/s10750-008-9599-210.1007/s10750-008-9599-2
Pörtner HO, Peck MA (2010) Climate change effects on fishes and fisheries: towards a cause-and-effect understanding. J Fish Biol 77:1745–1779. https://doi.org/10.1111/j.1095-8649.2010.02783.x
Prandle D, Lane A (2015) Sensitivity of estuaries to sea level rise: vulnerability indices. Estuar Coast Shelf Sci 160:60–68. https://doi.org/10.1016/J.ECSS.2015.04.001
Preisler R, Wasson K, Wolff W, Tyrrell M (2009) Invasions of estuaries vs the adjacent open coast: a global perspective. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems. Springer, Berlin, pp 587–618
Prieto L, Astorga D, Navarro G, Ruiz J (2010a) Environmental control of phase transition and polyp survival of a massive-outbreaker jellyfish. PLoS ONE 5:e13793. https://doi.org/10.1371/journal.pone.0013793
Purcell JE (2012) Jellyfish and ctenophore blooms coincide with human proliferations and environmental perturbations. Annu Rev Mar Sci 4:209–235. https://doi.org/10.1146/annurev-marine-120709-142751
Purcell J, Uye S, Lo W (2007) Anthropogenic causes of jellyfish blooms and their direct consequences for humans: a review. Mar Ecol Prog Ser 350:153–174. https://doi.org/10.3354/meps07093
Purcell JE, Atienza D, Fuentes V, Olariaga A, Tilves U, Colahan C, Gili J-M (2012) Temperature effects on asexual reproduction rates of scyphozoan species from the northwest Mediterranean Sea. Hydrobiologia 690:169–180. https://doi.org/10.1007/s10750-012-1047-7
Rato LD, Novais SC, Lemos MFL, Alves LMF, Leandro SM (2017) Homarus gammarus (Crustacea:Decapoda) larvae under an ocean acidification scenario: responses across different levels of biological organization. Comp Biochem Physiol Part C 203:29–38. https://doi.org/10.1016/j.cbpc.2017.09.002
Raven J, Caldeira K, Elderfield H, Hoegh-Guldberg O, Liss P, Riebesell U, Shepherd J, Turley C, Watson A (2005) Ocean acidification due to increasing atmospheric carbon dioxide. Royal Society, pp 1–68
Richardson AJ, Gibbons MJ (2008) Are jellyfish increasing in response to ocean acidification? Limnol Oceanogr 53:2040–2045. https://doi.org/10.4319/lo.2008.53.5.2040
Riisgård HU, Madsen CV (2011) Clearance rates of ephyrae and small medusae of the common jellyfish Aurelia aurita offered different types of prey. J Sea Res 65:51–57. https://doi.org/10.1016/J.SEARES.2010.07.002
Rippingale RJ, Kelly SJ (1995) Reproduction and survival of Phyllorhiza punctata (Cnidaria: Rhizostomeae) in a seasonally fluctuating salinity regime in Western Australia. Mar Freshw Res 46:1145–1151. https://doi.org/10.1071/MF9951145
R Development Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/. Accessed 10 Aug 2021
Sala OE, Chapin FS, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Oesterheld M, Poff NLR, Sykes MT, Walker BH, Walker M, Wall DH (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774
Schiariti A, Morandini AC, Jarms G, Von Glehn PR, Franke S, Mianzan H (2014) Asexual reproduction strategies and blooming potential in Scyphozoa. Mar Ecol Prog Ser 510:241–253. https://doi.org/10.3354/meps10798
Schiariti A, Melica V, Kogovšek T, Malej A (2015) Density-dependent effects control the reproductive strategy and population growth of Aurelia aurita s.l. scyphistomae. Mar Biol 162:1665–1672. https://doi.org/10.1007/s00227-015-2704-y
Sokołowski A, Brulińska D, Olenycz M, Wołowicz M (2016) Does temperature and salinity limit asexual reproduction of Aurelia aurita polyps (Cnidaria: Scyphozoa) in the Gulf of Gdańsk (southern Baltic Sea)? An experimental study. Hydrobiologia 773:49–62. https://doi.org/10.1007/s10750-016-2678-x
Sondervan PJ (2016) AquaBioSolutions—Europe’s First Jellyfish Breeding Centre AquaBioSolutions—Europas Erstes Quallen-Zucht-Zentrum. Der Zoologische Garten 85:84–90. https://doi.org/10.1016/j.zoolgart.2015.09.012
Stachowicz JJ, Terwin JR, Whitlatch RB, Osman RW (2002) Linking climate change and biological invasions: ocean warming facilitates nonindigenous species invasions. Proc Natl Acad Sci USA 99:15497–15500. https://doi.org/10.1073/pnas.242437499
Stott PA, Sutton RT, Smith DM (2008) Detection and attribution of Atlantic salinity changes. Geophys Res Lett. https://doi.org/10.1029/2008GL035874
Thuesen EV, Rutherford LD, Brommer PL, Garrison K, Gutowska MA, Towanda T (2005) Intragel oxygen promotes hypoxia tolerance of scyphomedusae. J Exp Biol 208:2475–2482. https://doi.org/10.1242/jeb.01655
Turley C, Findlay HS (2009) Chapter 21—ocean acidification as an indicator for climate change. Climate change. IPCC, pp 367–390
Vagelli AA (2007) New observations on the asexual reproduction of Aurelia aurita (Cnidaria, Scyphozoa) with comments on its life cycle and adaptive significance. Invertebr Zool 4:111–127
Van Walraven L, Driessen F, Van Bleijswijk J, Bol A, Pieternella LC, Joop CWP, Bos OG, Adriaan G, Schrieken N, Langenberg VT, Van Der Henk VW (2016) Where are the polyps? Molecular identification, distribution and population differentiation of Aurelia aurita jellyfish polyps in the southern North Sea area. Mar Biol. https://doi.org/10.1007/s00227-016-2945-4
Vargas-Yáñez M, García-Martínez MC, Moya F, Balbín R, López-Jurado JL, Serra M, Zunino P, Pascual J, Salat J (2017) Updating temperature and salinity mean values and trends in the Western Mediterranean: The RADMED project. Prog Oceanogr 157:27–46. https://doi.org/10.1016/J.POCEAN.2017.09.004
Verity PG, Purcell JE, Frischer ME (2011) Seasonal patterns in size and abundance of Phyllorhiza punctata: an invasive scyphomedusa in coastal Georgia (USA). Mar Biol 158:2219–2226. https://doi.org/10.1007/s00227-011-1727-2
Vermeij MJA, Sandin SA (2008) Density-dependent settlement and mortality structure the earliest life phases of a coral population. Ecology 89:1994–2004. https://doi.org/10.1890/07-1296.1
Wake B (2019) Experimenting with multistressors. Nat Clim Change 9:357
Watanabe T, Ishii H (2001) In situ estimation of ephyrae liberated from polyps of Aurelia aurita using settling plates in Tokyo Bay, Japan. Jellyfish blooms: ecological and societal importance. Springer, Dordrecht, pp 247–258
Webster CN, Lucas CH (2012) The effects of food and temperature on settlement of Aurelia aurita planula larvae and subsequent somatic growth. J Exp Mar Biol Ecol 436–437:50–55. https://doi.org/10.1016/J.JEMBE.2012.08.014
Widmer C, Fox C, Brierley A (2016) Effects of temperature and salinity on four species of northeastern Atlantic scyphistomae (Cnidaria: Scyphozoa). Mar Ecol Prog Ser 559:73–88. https://doi.org/10.3354/meps11879
Willcox S, Moltschaniwskyj NA, Crawford C (2007) Asexual reproduction in scyphistomae of Aurelia sp.: effects of temperature and salinity in an experimental study. J Exp Mar Biol Ecol 353:107–114. https://doi.org/10.1016/J.JEMBE.2007.09.006
Zuur AF, Hilbe JM, Ieno EN (2013) A Beginner’s Guide to GLM and GLMM with R: a frequentist and Bayesian perspective for ecologists, Highland Statistics
Funding
Financial support by Fundação para a Ciência e Tecnologia (FCT) through the strategic project UIDB/04292/2020, the project “Jellyfisheries—Towards an integrated approach to enhance predictive accuracy of jellyfish impact on coastal marine ecosystems” (POCI-01-0145-FEDER-016772), the fellowship granted to Lénia D. Rato under the same project (2015–2018 FEDER 16772, FCT, IP—PTDC/MAR-BIO/0440/2014), and the Integrated Programme of SR&TD “Smart Valorisation of Endogenous Marine Biological Resources Under a Changing Climate” (Centro-01-0145-FEDER-000018), co-funded by Centro 2020 program, Portugal 2020, European Union, through the European Regional Development Fund. Oceanário de Lisboa is gratefully acknowledged.
Author information
Authors and Affiliations
Contributions
LDR: conceptualisation, methodology, formal analysis and investigation, writing—original draft preparation and writing—review and editing. CP: methodology, formal analysis and investigation and writing—review. IMD: methodology and writing—review. SML: writing—review, funding acquisition, resources and supervision. SCM: conceptualisation, methodology, writing—review and supervision.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest statement.
Ethics approval
No approval of research ethics committees was required to accomplish the goals of this study because experimental work was conducted with an unregulated invertebrate species.
Additional information
Responsible Editor: E. Briski.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Reviewers: R. N. Cuthbert and undisclosed experts.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Rato, L.D., Pinto, C., Duarte, I.M. et al. Euryhalinity and thermal tolerance of Phyllorhiza punctata (Scyphozoa) scyphostomae: life history and physiological trade-offs. Mar Biol 168, 158 (2021). https://doi.org/10.1007/s00227-021-03969-x
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-021-03969-x