Articles | Volume 17, issue 22
https://doi.org/10.5194/bg-17-5489-2020
© Author(s) 2020. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
https://doi.org/10.5194/bg-17-5489-2020
© Author(s) 2020. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
The effects of decomposing invasive jellyfish on biogeochemical fluxes and microbial dynamics in an ultra-oligotrophic sea
Tamar Guy-Haim
CORRESPONDING AUTHOR
Israel Oceanographic and Limnological Research, National Oceanography
Institute, Haifa, 3108000, Israel
Maxim Rubin-Blum
Israel Oceanographic and Limnological Research, National Oceanography
Institute, Haifa, 3108000, Israel
Eyal Rahav
Israel Oceanographic and Limnological Research, National Oceanography
Institute, Haifa, 3108000, Israel
Natalia Belkin
Israel Oceanographic and Limnological Research, National Oceanography
Institute, Haifa, 3108000, Israel
Jacob Silverman
Israel Oceanographic and Limnological Research, National Oceanography
Institute, Haifa, 3108000, Israel
Guy Sisma-Ventura
Israel Oceanographic and Limnological Research, National Oceanography
Institute, Haifa, 3108000, Israel
Related authors
Natalia Belkin, Tamar Guy-Haim, Maxim Rubin-Blum, Ayah Lazar, Guy Sisma-Ventura, Rainer Kiko, Arseniy R. Morov, Tal Ozer, Isaac Gertman, Barak Herut, and Eyal Rahav
Ocean Sci., 18, 693–715, https://doi.org/10.5194/os-18-693-2022, https://doi.org/10.5194/os-18-693-2022, 2022
Short summary
Short summary
We studied how distinct water circulations that elevate (cyclone) or descend (anticyclone) water from the upper ocean affect the biomass, activity and diversity of planktonic microorganisms in the impoverished eastern Mediterranean. We show that cyclonic and anticyclonic eddies differ in their community composition and production. Moreover, the anticyclone may be a potential bio-invasion and dispersal vector, while the cyclone may serve as a thermal refugee for native species.
Tom Reich, Natalia Belkin, Guy Sisma-Ventura, Hagar Hauzer, Maxim Rubin-Blum, Ilana Berman-Frank, and Eyal Rahav
EGUsphere, https://doi.org/10.5194/egusphere-2025-1445, https://doi.org/10.5194/egusphere-2025-1445, 2025
Short summary
Short summary
Dark carbon fixation by chemoautotrophs take a vital part in marine primary productivity. Measured rates can be seen all the way down to the dark layers of the ocean and integrated in our study site come close to the magnitude of photosynthesis. It can also explain about ~35 % of the missing organic carbon supply needed by deep microbial communities. By using oceanographic observations and analysis this paper highlights the significant of this overlooked parameter.
Maxim Rubin-Blum, Eyal Rahav, Guy Sisma-Ventura, Yana Yudkovski, Zoya Harbuzov, Or M. Bialik, Oded Ezra, Anneleen Foubert, Barak Herut, and Yizhaq Makovsky
Biogeosciences, 22, 1321–1340, https://doi.org/10.5194/bg-22-1321-2025, https://doi.org/10.5194/bg-22-1321-2025, 2025
Short summary
Short summary
Chemotones, transition zones in chemosynthetic ecosystems, alter geochemical cycles and biodiversity. We studied seep chemotones, which are heavily burrowed by ghost shrimp. To investigate if burrowing affects habitat functionality, we surveyed the seafloor with deep-sea vehicles, analyzed sediment, and explored microbial communities in burrows. We found chemosynthetic biofilms, linking them to macromolecule turnover and nutrient cycling. This process may play a crucial role in deep-sea cycles.
Zhibo Shao, Yangchun Xu, Hua Wang, Weicheng Luo, Lice Wang, Yuhong Huang, Nona Sheila R. Agawin, Ayaz Ahmed, Mar Benavides, Mikkel Bentzon-Tilia, Ilana Berman-Frank, Hugo Berthelot, Isabelle C. Biegala, Mariana B. Bif, Antonio Bode, Sophie Bonnet, Deborah A. Bronk, Mark V. Brown, Lisa Campbell, Douglas G. Capone, Edward J. Carpenter, Nicolas Cassar, Bonnie X. Chang, Dreux Chappell, Yuh-ling Lee Chen, Matthew J. Church, Francisco M. Cornejo-Castillo, Amália Maria Sacilotto Detoni, Scott C. Doney, Cecile Dupouy, Marta Estrada, Camila Fernandez, Bieito Fernández-Castro, Debany Fonseca-Batista, Rachel A. Foster, Ken Furuya, Nicole Garcia, Kanji Goto, Jesús Gago, Mary R. Gradoville, M. Robert Hamersley, Britt A. Henke, Cora Hörstmann, Amal Jayakumar, Zhibing Jiang, Shuh-Ji Kao, David M. Karl, Leila R. Kittu, Angela N. Knapp, Sanjeev Kumar, Julie LaRoche, Hongbin Liu, Jiaxing Liu, Caroline Lory, Carolin R. Löscher, Emilio Marañón, Lauren F. Messer, Matthew M. Mills, Wiebke Mohr, Pia H. Moisander, Claire Mahaffey, Robert Moore, Beatriz Mouriño-Carballido, Margaret R. Mulholland, Shin-ichiro Nakaoka, Joseph A. Needoba, Eric J. Raes, Eyal Rahav, Teodoro Ramírez-Cárdenas, Christian Furbo Reeder, Lasse Riemann, Virginie Riou, Julie C. Robidart, Vedula V. S. S. Sarma, Takuya Sato, Himanshu Saxena, Corday Selden, Justin R. Seymour, Dalin Shi, Takuhei Shiozaki, Arvind Singh, Rachel E. Sipler, Jun Sun, Koji Suzuki, Kazutaka Takahashi, Yehui Tan, Weiyi Tang, Jean-Éric Tremblay, Kendra Turk-Kubo, Zuozhu Wen, Angelicque E. White, Samuel T. Wilson, Takashi Yoshida, Jonathan P. Zehr, Run Zhang, Yao Zhang, and Ya-Wei Luo
Earth Syst. Sci. Data, 15, 3673–3709, https://doi.org/10.5194/essd-15-3673-2023, https://doi.org/10.5194/essd-15-3673-2023, 2023
Short summary
Short summary
N2 fixation by marine diazotrophs is an important bioavailable N source to the global ocean. This updated global oceanic diazotroph database increases the number of in situ measurements of N2 fixation rates, diazotrophic cell abundances, and nifH gene copy abundances by 184 %, 86 %, and 809 %, respectively. Using the updated database, the global marine N2 fixation rate is estimated at 223 ± 30 Tg N yr−1, which triplicates that using the original database.
Natalia Belkin, Tamar Guy-Haim, Maxim Rubin-Blum, Ayah Lazar, Guy Sisma-Ventura, Rainer Kiko, Arseniy R. Morov, Tal Ozer, Isaac Gertman, Barak Herut, and Eyal Rahav
Ocean Sci., 18, 693–715, https://doi.org/10.5194/os-18-693-2022, https://doi.org/10.5194/os-18-693-2022, 2022
Short summary
Short summary
We studied how distinct water circulations that elevate (cyclone) or descend (anticyclone) water from the upper ocean affect the biomass, activity and diversity of planktonic microorganisms in the impoverished eastern Mediterranean. We show that cyclonic and anticyclonic eddies differ in their community composition and production. Moreover, the anticyclone may be a potential bio-invasion and dispersal vector, while the cyclone may serve as a thermal refugee for native species.
Hanni Vigderovich, Werner Eckert, Michal Elul, Maxim Rubin-Blum, Marcus Elvert, and Orit Sivan
Biogeosciences, 19, 2313–2331, https://doi.org/10.5194/bg-19-2313-2022, https://doi.org/10.5194/bg-19-2313-2022, 2022
Short summary
Short summary
Anaerobic oxidation of methane (AOM) is one of the major processes limiting the release of the greenhouse gas methane from natural environments. Here we show that significant AOM exists in the methane zone of lake sediments in natural conditions and even after long-term (ca. 18 months) anaerobic slurry incubations with two stages. Methanogens were most likely responsible for oxidizing the methane, and humic substances and iron oxides are likely electron acceptors to support this oxidation.
Cited articles
Amaral-Zettler, L. A., McCliment, E. A., Ducklow, H. W., and Huse, S. M.: A
method for studying protistan diversity using massively parallel sequencing
of V9 hypervariable regions of small-subunit ribosomal RNA genes, PloS one,
4, e6372,
https://doi.org/10.1371/journal.pone.0006372, 2009.
Andersen, K. S., Kirkegaard, R. H., Karst, S. M., and Albertsen, M.:
ampvis2: an R package to analyse and visualise 16S rRNA amplicon data,
bioRxiv 299537, https://doi.org/10.1101/299537, 2018.
Angel, D. L., Edelist, D., and Freeman, S.: Local perspectives on regional
challenges: jellyfish proliferation and fish stock management along the
Israeli Mediterranean coast, Reg. Environ. Change, 16, 315–323,
2016.
Apprill, A., McNally, S., Parsons, R., and Weber, L.: Minor revision to V4
region SSU rRNA 806R gene primer greatly increases detection of SAR11
bacterioplankton, Aquat. Microbial Ecol., 75, 129–137, 2015.
Attrill, M. J., Wright, J., and Edwards, M.: Climate-related increases in
jellyfish frequency suggest a more gelatinous future for the North Sea,
Limnol. Oceanogr., 52, 480–485, 2007.
Bagby, S. C. and Chisholm, S. W.: Response of Prochlorococcus to varying
CO2:O2 ratios, ISME J., 9, 2232–2245, 2015.
Balistreri, P., Spiga, A., Deidun, A., Gueroun, S. K., and Yahia, M. N. D.:
Further spread of the venomous jellyfish Rhopilema nomadica Galil, Spannier & Ferguson, 1990
(Rhizostomeae, Rhizostomatidae) in the western Mediterranean, BioInvasions
Records, 6, 19–24, 2017.
Bar-Zeev, E. and Rahav, E.: Microbial metabolism of transparent exopolymer
particles during the summer months along a eutrophic estuary system,
Front. Microbiol., 6, p. 403, 2015.
Basso, L., Rizzo, L., Marzano, M., Intranuovo, M., Fosso, B., Pesole, G.,
Piraino, S., and Stabili, L.: Jellyfish summer outbreaks as bacterial
vectors and potential hazards for marine animals and humans health? The case
of Rhizostoma pulmo (Scyphozoa, Cnidaria), Sci. Total Environ.,
692, 305–318, 2019.
Bižić-Ionescu, M., Zeder, M., Ionescu, D., Orlić, S., Fuchs, B.
M., Grossart, H. P., and Amann, R.: Comparison of bacterial communities on
limnic versus coastal marine particles reveals profound differences in
colonization, Environ. Microbiol., 17, 3500–3514, 2015.
Blanchet, M., Pringault, O., Bouvy, M., Catala, P., Oriol, L., Caparros, J.,
Ortega-Retuerta, E., Intertaglia, L., West, N., and Agis, M.: Changes in
bacterial community metabolism and composition during the degradation of
dissolved organic matter from the jellyfish Aurelia aurita in a Mediterranean coastal
lagoon, Environ. Sci. Pollut. Res., 22, 13638–13653, 2015.
Bolyen, E., Rideout, J. R., Dillon, M. R., Bokulich, N. A., Abnet, C.,
Al-Ghalith, G. A., Alexander, H., Alm, E. J., Arumugam, M., and Asnicar, F.:
QIIME 2: Reproducible, interactive, scalable, and extensible microbiome data
science, PeerJ Preprints, 6, 2167–9843, 2018.
Brotz, L., Cheung, W. W., Kleisner, K., Pakhomov, E., and Pauly, D.:
Increasing jellyfish populations: trends in large marine ecosystems,
Jellyfish Blooms IV, Springer, 2012.
Brun, F. G., Hernández, I., Vergara, J. J., Peralta, G., and
Pérez-Lloréns, J. L.: Assessing the toxicity of ammonium pulses to
the survival and growth of Zostera noltii, Mar. Ecol. Prog. Ser., 225, 177–187,
2002.
Callahan, B. J., McMurdie, P. J., Rosen, M. J., Han, A. W., Johnson, A. J.
A., and Holmes, S. P.: DADA2: high-resolution sample inference from Illumina
amplicon data, Nature Methods, 13, 581–583, 2016.
Chelsky, A., Pitt, K. A., and Welsh, D. T.: Biogeochemical implications of
decomposing jellyfish blooms in a changing climate, Estuarine,
Coast. Shelf Sci., 154, 77–83, 2015.
Chelsky, A., Pitt, K. A., Ferguson, A. J., Bennett, W. W., Teasdale, P. R.,
and Welsh, D. T.: Decomposition of jellyfish carrion in situ: Short-term
impacts on infauna, benthic nutrient fluxes and sediment redox conditions,
Sci. Total Environ., 566, 929–937, 2016.
Condon, R. H., Steinberg, D. K., Del Giorgio, P. A., Bouvier, T. C., Bronk,
D. A., Graham, W. M., and Ducklow, H. W.: Jellyfish blooms result in a major
microbial respiratory sink of carbon in marine systems, P. Natl. Acad. Sci., 108, 10225–10230, 2011.
Condon, R. H., Duarte, C. M., Pitt, K. A., Robinson, K. L., Lucas, C. H.,
Sutherland, K. R., Mianzan, H. W., Bogeberg, M., Purcell, J. E., and Decker,
M. B.: Recurrent jellyfish blooms are a consequence of global oscillations,
P. Natl. Acad. Sci., 110, 1000–1005, 2013.
R Core Team: A language and environment for statistical computing version 4.0.2, R Foundation for Statistical Computing, Vienna, Austria, ISBN 3-900051-07-0, available at: http://www.R-project.org/ (last access: 15 June 2020), 2020.
Cottrell, M. T. and Kirchman, D. L.: Natural assemblages of marine
proteobacteria and members of the Cytophaga-Flavobacter cluster consuming
low-and high-molecular-weight dissolved organic matter, Appl. Environ.
Microbiol., 66, 1692–1697, 2000.
Denis, L., Grenz, C., Alliot, E., and Rodier, M.: Temporal variability in
dissolved inorganic nitrogen fluxes at the sediment–water interface and
related annual budget on a continental shelf (NW Mediterranean),
Oceanologica Acta, 24, 85–97, 2001.
Dinasquet, J., Granhag, L. M., and Riemann, L.: Stimulated bacterioplankton
growth and selection for certain bacterial taxa in the vicinity of the
ctenophore Mnemiopsis leidyi, Front. Microbiol., 3, p. 302, 2012.
Duarte, C. M., Pitt, K. A., Lucas, C. H., Purcell, J. E., Uye, S.-i.,
Robinson, K., Brotz, L., Decker, M. B., Sutherland, K. R., and Malej, A.: Is
global ocean sprawl a cause of jellyfish blooms?,
Front. Ecol. Environ., 11, 91–97, 2013.
Dupont, C. L., Rusch, D. B., Yooseph, S., Lombardo, M.-J., Richter, R. A.,
Valas, R., Novotny, M., Yee-Greenbaum, J., Selengut, J. D., and Haft, D. H.:
Genomic insights to SAR86, an abundant and uncultivated marine bacterial
lineage, ISME J., 6, 1186–1199, 2012.
Durham, B. P., Grote, J., Whittaker, K. A., Bender, S. J., Luo, H., Grim, S.
L., Brown, J. M., Casey, J. R., Dron, A., and Florez-Leiva, L.: Draft genome
sequence of marine alphaproteobacterial strain HIMB11, the first cultivated
representative of a unique lineage within the Roseobacter clade possessing
an unusually small genome, Stand. Genomic Sci., 9, 632–645, 2014.
Eddy, F.: Ammonia in estuaries and effects on fish, J. Fish Biol.,
67, 1495–1513, 2005.
Edelist, D., Guy-Haim, T., Kuplik, Z., Zuckerman, N., Nemoy, P., and Angel,
D. L.: Phenological shift in swarming patterns of Rhopilema nomadica in the Eastern
Mediterranean Sea, J. Plankton Res., 42, 211–219, 2020.
Epstein, S. S., Burkovsky, I. V., and Shiaris, M. P.: Ciliate grazing on
bacteria, flagellates, and microalgae in a temperate zone sandy tidal flat:
ingestion rates and food niche partitioning, Journal of experimental marine
Biol. Ecol., 165, 103–123, 1992.
Feely, R. A., Alin, S. R., Newton, J., Sabine, C. L., Warner, M., Devol, A.,
Krembs, C., and Maloy, C.: The combined effects of ocean acidification,
mixing, and respiration on pH and carbonate saturation in an urbanized
estuary, Estuar. Coast. Shelf Sci., 88, 442–449, 2010.
Ferretti, J. A. and Calesso, D. F.: Toxicity of ammonia to surf clam
(Spisula solidissima) larvae in saltwater and sediment elutriates, Mar. Environ.
Res., 71, 189–194, 2011.
Frost, J. R., Jacoby, C. A., Frazer, T. K., and Zimmerman, A. R.: Pulse
perturbations from bacterial decomposition of Chrysaora quinquecirrha (Scyphozoa: Pelagiidae), in:
Jellyfish Blooms IV, ISBN 978-94-007-5315-0,
Springer, Dordrecht, 2012.
Galil, B.: Poisonous and venomous: marine alien species in the
Mediterranean Sea and human health, in: Invasive Species and Human
Health, edited by: Mazza, G., 1–15,
ISBN 9781786390981,
CABI, Oxfordshire, UK, 2018.
Galil, B., Spanier, E., and Ferguson, W.: The Scyphomedusae of the
Mediterranean coast of Israel, including two Lessepsian migrants new to the
Mediterranean, Zoologische Mededelingen, 64, 95–105, 1990.
Galil, B. S.: Truth and consequences: the bioinvasion of the Mediterranean
Sea, Integrative Zoology, 7, 299–311, 2012.
Gasol, J. M. and Kirchman, D. L.: Microbial ecology of the oceans, ISBN 9781119107187, USA John
Wiley & Sons, Hoboken, 2018.
Ghermandi, A., Galil, B., Gowdy, J., and Nunes, P. A.: Jellyfish outbreak
impacts on recreation in the Mediterranean Sea: welfare estimates from a
socioeconomic pilot survey in Israel, Ecosystem Services, 11, 140–147, 2015.
Giovannoni, S. J.: SAR11 bacteria: the most abundant plankton in the oceans,
Annu. Rev. Mar. Sci., 9, 231–255, 2017.
Glud, R. N.: Oxygen dynamics of marine sediments, Mar. Biol. Res.,
4, 243–289, 2008.
Gobler, C. J. and Baumann, H.: Hypoxia and acidification in ocean
ecosystems: coupled dynamics and effects on marine life, Biol. Lett.,
12, 20150976, https://doi.org/10.1098/rsbl.2015.0976, 2016.
Gobler, C. J., DePasquale, E. L., Griffith, A. W., and Baumann, H.: Hypoxia
and acidification have additive and synergistic negative effects on the
growth, survival, and metamorphosis of early life stage bivalves, PloS one,
9, e83648, https://doi.org/10.1371/journal.pone.0083648, 2014.
Guy-Haim, T., Rubin-Blum, M., Rahav, E., Belkin, N., Silverman, J., and Sisma-Ventura, G.: Experiment on biogeochemical changes following Rhopilema nomadica decomposition, PANGAEA, https://doi.org/10.1594/PANGAEA.915464, 2020.
Hammer, Ø., Harper, D. A., and Ryan, P. D.: PAST: Paleontological
statistics software package for education and data analysis, Palaeontologia
Electronica, 4, 1–9, 2001.
Hammond, D. E., Cummins, K. M., McManus, J., Berelson, W. M., Smith, G., and
Spagnoli, F.: Methods for measuring benthic nutrient flux on the California
Margin: Comparing shipboard core incubations to in situ lander results,
Limnol. Oceanogr.-Methods, 2, 146–159, 2004.
Hamner, W. M. and Dawson, M. N.: A review and synthesis on the systematics
and evolution of jellyfish blooms: advantageous aggregations and adaptive
assemblages, Hydrobiologia, 616, 161–191, 2009.
Harrell, F.: Hmisc: Harrell Miscellaneous library for R statistical
software, R package, 2, 2–3, 2004.
Hays, G. C., Doyle, T. K., and Houghton, J. D.: A paradigm shift in the
trophic importance of jellyfish?, Trends Ecol. Evol., 33,
874–884, 2018.
Hubot, N., Giering, S. L. C., Lucas, C., Robidart, J., and Fuessel, J.:
Evidence of nitrification associated with jellyfish, Ocean Sciences Meeting Proceedings, available at: https://agu.confex.com/agu/osm20/meetingapp.cgi/Paper/639039 (last access: 18 February 2020), 2020.
Hyams-Kaphzan, O., Almogi-Labin, A., Benjamini, C., and Herut, B.: Natural
oligotrophy vs. pollution-induced eutrophy on the SE Mediterranean shallow
shelf (Israel): Environmental parameters and benthic foraminifera, Mar.
Pollut. Bull., 58, 1888–1902, 2009.
Ignatiades, L., Gotsis-Skretas, O., Pagou, K., and Krasakopoulou, E.:
Diversification of phytoplankton community structure and related parameters
along a large-scale longitudinal east–west transect of the Mediterranean
Sea, J. Plankton Res., 31, 411–428, 2009.
Kamiyama, T.: Planktonic ciliates as food for the scyphozoan Aurelia
coerulea: feeding and growth responses of ephyra and metephyra stages,
J. Oceanogr., 74, 53–63, 2018.
Katsanevakis, S., Wallentinus, I., Zenetos, A., Leppäkoski, E.,
Çinar, M. E., Oztürk, B., Grabowski, M., Golani, D., and Cardoso, A.
C.: Impacts of invasive alien marine species on ecosystem services and
biodiversity: a pan-European review, Aquatic Invasions, 9, 391–423, 2014.
Kramar, M. K., Tinta, T., Lučić, D., Malej, A., and Turk, V.:
Bacteria associated with moon jellyfish during bloom and post-bloom periods
in the Gulf of Trieste (northern Adriatic), PloS one, 14, e0198056, https://doi.org/10.1371/journal.pone.0198056, 2019.
Kress, N., Thingstad, T. F., Pitta, P., Psarra, S., Tanaka, T., Zohary, T.,
Groom, S., Herut, B., Mantoura, R. F. C., and Polychronaki, T.: Effect of P
and N addition to oligotrophic Eastern Mediterranean waters influenced by
near-shore waters: a microcosm experiment, Deep Sea Res. Pt. II, 52, 3054–3073, 2005.
Kress, N., Gertman, I., and Herut, B.: Temporal evolution of physical and
chemical characteristics of the water column in the Easternmost Levantine
basin (Eastern Mediterranean Sea) from 2002 to 2010, J. Mar.
Syst., 135, 6–13, 2014.
Kroeker, K. J., Kordas, R. L., Crim, R. N., and Singh, G. G.: Meta-analysis
reveals negative yet variable effects of ocean acidification on marine
organisms, Ecol. Lett., 13, 1419–1434, 2010.
Lakkis, S. and Zeidane, R.: Jellyfish swarm along the Lebanese coast
(Abstract) Lebanese Association for the Advancement of Science 11th Science
Meeting American University of Beirut, 1991.
Lebrato, M. and Jones, D.: Jellyfish biomass in the biological pump:
Expanding the oceanic carbon cycle, Biochem. Soc. J., 33,
35–39, 2011.
Lebrato, M., Pitt, K. A., Sweetman, A. K., Jones, D. O., Cartes, J. E.,
Oschlies, A., Condon, R. H., Molinero, J. C., Adler, L., and Gaillard, C.:
Jelly-falls historic and recent observations: a review to drive future
research directions, Hydrobiologia, 690, 227–245, 2012.
Licandro, P., Conway, D., Daly Yahia, M., Fernandez de Puelles, M. L.,
Gasparini, S., Hecq, J.-H., Tranter, P., and Kirby, R.: A blooming jellyfish
in the northeast Atlantic and Mediterranean, Biol. Lett., 6, 688–691,
2010.
Lotan, A., Ben-Hillel, R., and Loya, Y.: Life cycle of Rhopilema nomadica: a new immigrant
scyphomedusan in the Mediterranean, Mar. Biol., 112, 237–242, 1992.
Lotan, A., Fine, M., and Ben-Hillel, R.: Synchronization of the life cycle
and dispersal pattern of the tropical invader scyphomedusan Rhopilema nomadica is temperature
dependent, Mar. Ecol. Prog. Ser., 109, 59–59, 1994.
Love, M. I., Huber, W., and Anders, S.: Moderated estimation of fold change
and dispersion for RNA-seq data with DESeq2, Genome Biol., 15, p. 550, 2014.
Lucas, C. H., Pitt, K. A., Purcell, J. E., Lebrato, M., and Condon, R. H.:
What's in a jellyfish? Proximate and elemental composition and biometric
relationships for use in biogeochemical studies, Ecology, 92, 1704, https://doi.org/10.1890/11-0302.1, 2011.
Lynam, C. P., Gibbons, M. J., Axelsen, B. E., Sparks, C. A., Coetzee, J.,
Heywood, B. G., and Brierley, A. S.: Jellyfish overtake fish in a heavily
fished ecosystem, Current Biol., 16, R492–R493, 2006.
MacKenzie, K. M., Trueman, C. N., Lucas, C. H., and Bortoluzzi, J.: The
preparation of jellyfish for stable isotope analysis, Mar. Biol., 164,
p. 219, 2017.
Madkour, F. F., Safwat, W., and Hanafy, M. H.: Record of Aggregation of
Alien Tropical Schyphozoan Rhopilema nomadica Galil, 1990 in the Mediterranean Coast of Egypt,
Int. Mar. Sci. J., 1, p. 1, 2019.
McMurdie, P. J. and Holmes, S.: phyloseq: an R package for reproducible
interactive analysis and graphics of microbiome census data, PloS one, 8, e61217, https://doi.org/10.1371/journal.pone.0061217,
2013.
Melzner, F., Thomsen, J., Koeve, W., Oschlies, A., Gutowska, M. A., Bange,
H. W., Hansen, H. P., and Körtzinger, A.: Future ocean acidification
will be amplified by hypoxia in coastal habitats, Mar. Biol., 160,
1875–1888, 2013.
Møller, L. F. and Riisgård, H. U.: Impact of jellyfish and mussels on
algal blooms caused by seasonal oxygen depletion and nutrient release from
the sediment in a Danish fjord, J. Exp. Mar. Biol. Ecol., 351, 92–105, 2007.
Müller, T., Walter, B., Wirtz, A., and Burkovski, A.: Ammonium toxicity
in bacteria, Current Microbiol., 52, 400–406, 2006.
Nakar, N., Disegni, D., and Angel, D.: Economic evaluation of jellyfish
effects on the fishery sector – Case study from the eastern Mediterranean, in: Proceedings of the Thirteenth Annual BIOECON Conference, 10 May 2011, 11–13,
2011.
Niepceron, M., Martin-Laurent, F., Crampon, M., Portet-Koltalo, F.,
Akpa-Vinceslas, M., Legras, M., Bru, D., Bureau, F., and Bodilis, J.:
GammaProteobacteria as a potential bioindicator of a multiple contamination
by polycyclic aromatic hydrocarbons (PAHs) in agricultural soils,
Environ. Pollut., 180, 199–205, 2013.
Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., O'hara, R., Simpson,
G. L., Solymos, P., Stevens, M. H. H., and Wagner, H.: Vegan: community
ecology package, R package version 1.17-4, available at: http://CRAN.R-project.org/package=vegan (last access: March 2016), 2010.
Parada, A. E., Needham, D. M., and Fuhrman, J. A.: Every base matters:
assessing small subunit rRNA primers for marine microbiomes with mock
communities, time series and global field samples, Environ. Microbiol., 18, 1403–1414, 2016.
Pitt, K. A., Welsh, D. T., and Condon, R. H.: Influence of jellyfish blooms
on carbon, nitrogen and phosphorus cycling and plankton production,
Hydrobiologia, 616, 133–149, 2009.
Pratihary, A. K., Naqvi, S. W. A., Narvenkar, G., Kurian, S., Naik, H., Naik, R., and Manjunatha, B. R.: Benthic mineralization and nutrient exchange over the inner continental shelf of western India, Biogeosciences, 11, 2771–2791, https://doi.org/10.5194/bg-11-2771-2014, 2014.
Purcell, J. E.: Jellyfish and ctenophore blooms coincide with human
proliferations and environmental perturbations, Annu. Rev. Mar.
Sci., 4, 209–235, 2012.
Purcell, J. E., Uye, S.-I., and Lo, W.-T.: Anthropogenic causes of jellyfish
blooms and their direct consequences for humans: a review, Mar. Ecol.
Prog. Ser., 350, 153–174, 2007.
Qu, C.-F., Song, J.-M., Li, N., Li, X.-G., Yuan, H.-M., Duan, L.-Q., and Ma,
Q.-X.: Jellyfish (Cyanea nozakii) decomposition and its potential influence on marine
environments studied via simulation experiments, Mar. Pollut. Bull.,
97, 199–208, 2015.
Quiñones, J., Mianzan, H., Purca, S., Robinson, K. L., Adams, G. D., and
Acha, E. M.: Climate-driven population size fluctuations of jellyfish
(Chrysaora plocamia) off Peru, Mar. Biol., 162, 2339–2350, 2015.
Rahav, E., Belkin, N., Paytan, A., and Herut, B.: Phytoplankton and
Bacterial Response to Desert Dust Deposition in the Coastal Waters of the
Southeastern Mediterranean Sea: A Four-Year In Situ Survey, Atmosphere, 9,
p. 305, 2018a.
Rahav, E., Raveh, O., Hazan, O., Gordon, N., Kress, N., Silverman, J., and
Herut, B.: Impact of nutrient enrichment on productivity of coastal water
along the SE Mediterranean shore of Israel-A bioassay approach, Mar. Pollut. Bull., 127, 559–567, 2018b.
Raveh, O., David, N., Rilov, G., and Rahav, E.: The temporal dynamics of
coastal phytoplankton and bacterioplankton in the Eastern Mediterranean Sea,
PLoS One, 10, e0140690, https://doi.org/10.1371/journal.pone.0140690, 2015.
Reichenbach, H.: The order cytophagales, in: The prokaryotes,
Springer, New York, NY, ISBN 978-1-4757-2193-5,
1992.
Richardson, A. J., Bakun, A., Hays, G. C., and Gibbons, M. J.: The jellyfish
joyride: causes, consequences and management responses to a more gelatinous
future, Trends Ecol. Evol., 24, 312–322, 2009.
Sanz-Martín, M., Pitt, K. A., Condon, R. H., Lucas, C. H., Novaes de
Santana, C., and Duarte, C. M.: Flawed citation practices facilitate the
unsubstantiated perception of a global trend toward increased jellyfish
blooms, Global Ecol. Biogeogr., 25, 1039–1049, 2016.
Schnedler-Meyer, N. A., Kiørboe, T., and Mariani, P.: Boom and Bust: Life
History, Environmental Noise, and the (un) Predictability of Jellyfish
Blooms, Front. Mar. Sci., 5, p. 257, 2018.
Shiganova, T., Mirzoyan, Z., Studenikina, E., Volovik, S., Siokou-Frangou,
I., Zervoudaki, S., Christou, E., Skirta, A., and Dumont, H.: Population
development of the invader ctenophore Mnemiopsis leidyi, in the Black Sea
and in other seas of the Mediterranean basin, Mar. Biol., 139, 431–445,
2001.
Simon, M.: Improved assessment of bacterial production: combined
measurements of protein synthesis via leucine and cell multiplication via
thymidine incorporation, Ergebnisse der Limnologie ERLIA, 6, 151–155, 1990.
Simon, M. and Azam, F.: Protein content and protein synthesis rates of
planktonic marine bacteria, Marine ecology progress series, Oldendorf, 51,
201–213, 1989.
Simon, M., Grossart, H.-P., Schweitzer, B., and Ploug, H.: Microbial ecology
of organic aggregates in aquatic ecosystems, Aquat. Microbial Ecol., 28,
175–211, 2002.
Sisma-Ventura, G. and Rahav, E.: DOP stimulates heterotrophic bacterial
production in the oligotrophic southeastern Mediterranean coastal waters,
Front. Microbiol., 10, 1913, https://doi.org/10.3389/fmicb.2019.01913, 2019.
Skoog, A. C. and Arias-Esquivel, V. A.: The effect of induced anoxia and
reoxygenation on benthic fluxes of organic carbon, phosphate, iron, and
manganese, Sci. Total Environ., 407, 6085–6092, 2009.
Stief, P.: Stimulation of microbial nitrogen cycling in aquatic ecosystems by benthic macrofauna: mechanisms and environmental implications, Biogeosciences, 10, 7829–7846, https://doi.org/10.5194/bg-10-7829-2013, 2013.
Stoeck, T., Bass, D., Nebel, M., Christen, R., Jones, M. D., Breiner, H. W.,
and Richards, T. A.: Multiple marker parallel tag environmental DNA
sequencing reveals a highly complex eukaryotic community in marine anoxic
water, Molecular Ecol., 19, 21–31, 2010.
Stoecker, D. K., Michaels, A. E., and Davis, L. H.: Grazing by the
jellyfish, Aurelia aurita, on microzooplankton, J. Plankton Res., 9, 901–915,
1987.
Streftaris, N. and Zenetos, A.: Alien marine species in the
Mediterranean-the 100 `Worst Invasives' and their impact, Mediterranean
Mar. Sci., 7, 87–118, 2006.
Sun, S., Jones, R. B., and Fodor, A. A.: Inference-based accuracy of
metagenome prediction tools varies across sample types and functional
categories, Microbiome, 8, 1–9, 2020.
Sweetman, A. K. and Chapman, A.: First observations of jelly-falls at the
seafloor in a deep-sea fjord, Deep Sea Res. Pt. I, 58, 1206–1211, 2011.
Sweetman, A. K., Smith, C. R., Dale, T., and Jones, D. O.: Rapid scavenging
of jellyfish carcasses reveals the importance of gelatinous material to
deep-sea food webs, Proc. Roy. Soc. B,
281, 20142210, https://doi.org/10.1098/rspb.2014.2210, 2014.
Sweetman, A. K., Chelsky, A., Pitt, K. A., Andrade, H., van Oevelen, D., and
Renaud, P. E.: Jellyfish decomposition at the seafloor rapidly alters
biogeochemical cycling and carbon flow through benthic food-webs, Limnol. Oceanogr., 61, 1449–1461, 2016.
Tadir, R., Benjamini, C., Almogi-Labin, A., and Hyams-Kaphzan, O.: Temporal
trends in live foraminiferal assemblages near a pollution outfall on the
Levant shelf, Mar. Pollut. Bull., 117, 50–60, 2017.
Thingstad, T. F., Krom, M., Mantoura, R., Flaten, G. F., Groom, S., Herut,
B., Kress, N., Law, C., Pasternak, A., and Pitta, P.: Nature of phosphorus
limitation in the ultraoligotrophic eastern Mediterranean, Science, 309,
1068–1071, 2005.
Tinta, T., Malej, A., Kos, M., and Turk, V.: Degradation of the Adriatic
medusa Aurelia sp. by ambient bacteria, in: Jellyfish Blooms: New Problems and
Solutions, ISBN 978-90-481-9540-4,
Springer, Dordrecht, 2010.
Tinta, T., Kogovšek, T., Malej, A., and Turk, V.: Jellyfish modulate
bacterial dynamic and community structure, PloS one, 7, e39274, https://doi.org/10.1371/journal.pone.0039274, 2012.
Tinta, T., Kogovšek, T., Turk, V., Shiganova, T. A., Mikaelyan, A. S.,
and Malej, A.: Microbial transformation of jellyfish organic matter affects
the nitrogen cycle in the marine water column—A Black Sea case study,
J. Exp. Mar. Biol. Ecol., 475, 19–30, 2016.
Titelman, J., Riemann, L., Sørnes, T. A., Nilsen, T., Griekspoor, P., and
Båmstedt, U.: Turnover of dead jellyfish: stimulation and retardation of
microbial activity, Mar. Ecol. Prog. Ser., 325, 43–58, 2006.
Welsh, D. T.: It's a dirty job but someone has to do it: the role of marine
benthic macrofauna in organic matter turnover and nutrient recycling to the
water column, Chem. Ecol., 19, 321–342, 2003.
Welsh, D. T., Dunn, R. J., and Meziane, T.: 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, 2009.
Wemheuer, F., Taylor, J. A., Daniel, R., Johnston, E., Meinicke, P., Thomas,
T., and Wemheuer, B.: Tax4Fun2: a R-based tool for the rapid prediction of
habitat-specific functional profiles and functional redundancy based on 16S
rRNA gene marker gene sequences, BioRxiv 490037, 2018.
West, E. J., Welsh, D. T., and Pitt, K. A.: Influence of decomposing
jellyfish on the sediment oxygen demand and nutrient dynamics, in: Jellyfish
Blooms: Causes, Consequences, and Recent Advances, Springer, ISBN 978-1-4020-9748-5, 2008.
West, E. J., Pitt, K. A., Welsh, D. T., Koop, K., and Rissik, D.: Top-down
and bottom-up influences of jellyfish on primary productivity and planktonic
assemblages, Limnol. Oceanogr., 54, 2058–2071, 2009.
Wickham, H.: ggplot2: elegant graphics for data analysis, Springer, New York, ISBN 9783319242750, 2016.
Woyke, T., Xie, G., Copeland, A., Gonzalez, J. M., Han, C., Kiss, H., Saw,
J. H., Senin, P., Yang, C., and Chatterji, S.: Assembling the marine
metagenome, one cell at a time, PloS one, 4, e5299, https://doi.org/10.1371/journal.pone.0005299, 2009.
Xiao, W., Zeng, Y., Liu, X., Huang, X., Chiang, K.-P., Mi, T., Zhang, F.,
Li, C., Wei, H., and Yao, Q.: The impact of giant jellyfish Nemopilema
nomurai blooms on plankton communities in a temperate marginal sea, Mar.
Pollut. Bull., 149, 110507, https://doi.org/10.1016/j.marpolbul.2019.110507, 2019.
Yahia, M. N. D., Yahia, O. K.-D., Gueroun, S. K. M., Aissi, M., Deidun, A.,
Fuentes, V., and Piraino, S.: The invasive tropical scyphozoan Rhopilema nomadica Galil, 1990
reaches the Tunisian coast of the Mediterranean Sea, BioInvasions Records,
2, 319–323, 2013.
Yakimov, M. M., Timmis, K. N., and Golyshin, P. N.: Obligate oil-degrading
marine bacteria, Current Opinion in Biotechnology, 18, 257–266, 2007.
Zenetos, A., Gofas, S., Verlaque, M., Çinar, M. E., Raso, J. G.,
Bianchi, C., Morri, C., Azzurro, E., Bilecenoglu, M., and Froglia, C.: Alien
species in the Mediterranean Sea by 2010. A contribution to the application
of European Union's Marine Strategy Framework Directive (MSFD). Part I.
Spatial distribution, Mediterranean Mar. Sci., 11, 381–493, 2010.
Zunino, S., Canu, D. M., Bandelj, V., and Solidoro, C.: Effects of ocean
acidification on benthic organisms in the Mediterranean Sea under realistic
climatic scenarios: a meta-analysis, Reg. Stud. Mar. Sci., 10,
86–96, 2017.
Short summary
The availability of nutrients in oligotrophic marine ecosystems is limited. Following jellyfish blooms, large die-off events result in the release of high amounts of nutrients to the water column and sediment. Our study assessed the decomposition effects of an infamous invasive jellyfish in the ultra-oligotrophic Eastern Mediterranean Sea. We found that jellyfish decomposition favored heterotrophic bacteria and altered biogeochemical fluxes, further impoverishing this nutrient-poor ecosystem.
The availability of nutrients in oligotrophic marine ecosystems is limited. Following jellyfish...
Altmetrics
Final-revised paper
Preprint