Atmospheric indices allow anticipating the incidence of jellyfish coastal swarms


Published: Jul 1, 2020
Keywords:
Alboran Sea Arctic Oscillation climatic fluctuations gelatinous zooplankton Mediterranean Sea North Atlantic Oscillation Pelagia noctiluca Sea Surface Temperature
JUAN J. BELLIDO
https://orcid.org/0000-0002-4262-3551
JOSÉ C. BÁEZ
LUCRECIA SOUVIRON-PRIEGO
FRANCISCO FERRI-YAÑEZ
CARMEN SALAS
JUAN ANTONIO LÓPEZ
RAIMUNDO REAL
Abstract

Jellyfish swarms affect littoral ecosystems, are unpleasant for bathers and jeopardize coastal socio-economic sectors. Anticipating the incidence of jellyfish swarms could be useful for implementing preventive management measures. Macroclimatic indices are good candidates for this type of anticipation since they are macro-ecologically related to oceanographic characteristics that affect marine species after a certain time lag. An increase of jellyfish swarms has been recently reported in the Mediterranean Sea. From 2005 to 2018, jellyfish swarms in the littoral of the province of Malaga (Spain, northwest coast of the Alboran Sea), mainly formed by the mauve stinger (Pelagia noctiluca), were frequent during summer. We recorded data on jellyfish swarm incidence in the province of Malaga from 2005 to 2018 using the reports in local newspapers, searches in Google Search Engine, and a citizen science application for mobile phones as information sources. With this information, we classified the period in years of low, medium and high incidence of jellyfish swarms. Then, we tested if the known effects of the Arctic Oscillation (AO) and North Atlantic Oscillation (NAO) in winter on the sea surface temperature (SST) during the year, which in turn affects the proliferation of jellyfish, could explain the inter-annual variation in this incidence. Our hypothesis significantly explained the variation in the medium versus low incidence of jellyfish swarms, with medium incidence in the summers of higher SST. This suggests that medium incidence of jellyfish swarms was caused by the proliferation of jellyfish. This also suggests that years of medium incidence of jellyfish in the beach during summer could be anticipated by computing the average AO and NAO values of the previous winter. Years of high incidence of swarms could not be explained by this process. We speculate that they may be caused by a change in the distribution of the swarms rather than by proliferation. Jellyfish may be pushed from the pelagic western anticyclonic gyre of the Alboran Sea to the northern coast by eddies that are formed when, as recent literature has shown, this gyre is weakened by westerly winds and the Atlantic jet. Citizen science has contributed useful data to build macroecological models that may result in better management plans based on scientific data.

Article Details
  • Section
  • Research Article
Downloads
Download data is not yet available.
Author Biography
JUAN J. BELLIDO, Aula del Mar de Málaga. Calle Pacífico 80, E-29004, Málaga Departamento de Biología Animal, Cátedra de Ciencias del Litoral de la Costa del Sol, Facultad de Ciencias, 29071, Campus de Teatinos, Universidad de Málaga, Málaga
Researcher and project manager
References
Acevedo, P., Real, R., 2012. Favourability: concept, distinctive characteristics and potential usefulness. Naturwissenschaften, 99 (7), 515-522.
Akaike, H., 1973. Information Theory and an Extension of the Maximum Likelihood Principle. p. 199–213. In: Proceedings of the second international symposium on information theory. Akademiai Kiado, Petrov, B.N., Csaki, F. (Eds). Budapest, Hungary.
Ansell, A., 1972. Distribution, growth and seasonal changes in biochemical composition for the bivalve Donax vittatus (da Costa) from Kames Bay, Millport. Journal of Experimental Marine Biology and Ecology, 10 (2), 137-150.
Aouititen, M., Bekkali, R., Nachit, D., Luan, X., Mrhraoui, M., 2019. Predicting Jellyfish Strandings in the Moroccan North-West Mediterranean Coastline. European Scientific Journal, 15 (2), 72-84.
Avian, M., Rottini Sandrini, L., Stravisi, F., 1991. The effect of seawater temperature on the swimming activity of Pelagia noctiluca (Forsskål). Italian Journal of Zoology, 58 (2), 135-143.
Báez, J.C., Gimeno, L., Gómez-Gesteira, M., Ferri-Yáñez, F., Real, R., 2013. Combined Effects of the North Atlantic Oscillation and the Arctic Oscillation on Sea Surface Temperature in the Alboran Sea. PLoS ONE, 8 (4), e62201.
Berline, L., Siokou-Frangou, I., Marasović, I., Vidjak, O., Fernández de Puelles, M.L. et al., 2012. Intercomparison of six Mediterranean zooplankton time series. Progress in Oceanography, 97–100, 76-91.
Boero, F., Bouillon, J., Gravili, C., Miglietta, M.P., Parsons, T. et al., 2008. Gelatinous plankton: Irregularities rule the world (sometimes). Marine Ecology Progress Series, 356, 299-310.
Boero, F., 2013. Review of Jellyfish Blooms in the Mediterranean and Black Sea. Studies and Reviews. General Fisheries Commission for the Mediterranean, 93.
Burnham, K.P., Anderson, D.R., 2004. Multimodel Inference: Understanding AIC and BIC in Model Selection. Sociological Methods & Research, 33 (2), 261-304.
Canepa, A.J., 2014. Jellyfish of the Spanish Mediterranean coast: effects of environmental factors on their spatio-temporal dynamics and economic impacts. PhD Thesis. University of Barcelona, Spain, 252 pp.
Carrasco, C., Navarro, J., Leiva, G., 2006. Biochemical composition and tissue weight of Chorus giganteus (Gastropoda: Muricidae) exposed to different diets and temperatures during reproductive conditioning. Interciencia, 31 (5), 376-381.
Condon, R.H., Graham, W.M., Duarte, C.M., Pitt, K.A., Lucas, C.H. et al., 2012. Questioning the rise of gelatinous zooplankton in the world's oceans. BioScience, 62 (2), 160-169.
Condon, R.H., Duarte, C.M., Pitt, K.A., Robinson, K.L., Lucas, C.H. et al., 2013. Recurrent jellyfish blooms are a consequence of global oscillations. Proceedings of the National Academy of Sciences, 110 (3), 1000-1005.
Conrad, C.C., Hilchey, K.G., 2011. A review of citizen science and community-based environmental monitoring: issues and opportunities. Environmental Monitoring and Assessment, 176 (1-4), 273-291.
Daly Yahia, M.N., Batistic, W., Lucic, D., Fernández de Puelles, M.L., Licandro, P. et al., 2010. Are outbreaks of Pelagia noctiluca (Forskäl, 1771) more frequent in the Mediterranean basin? In: Gislason, A., Gorsky, G. (Eds.), Proceedings of the Joint ICES/CIESM Workshop to Compare Zooplankton Ecology and Methodologies between the Mediterranean and the North Atlantic (WKZEM): ICES Cooperative Research Report, 300, pp. 8-14. Copenhagen.
Delap, M., Delap, C., 1906. Notes on the plankton of Valencia Harbour, 1902-1905. Fisheries, Ireland, Scientific Investigations 1905, 7, 3-21.
Fiala, M., Sournia, A., Claustre, H., Marty, J.C., Prieur, L. et al., 1994. Gradients of phytoplankton abundance, composition and photosynthetic pigments across the Almeria-Oran front (SW Mediterranean Sea). Journal of Marine Systems, 5 (3-5), 223-233.
Fielding, A., Bell, J., 1997. A review of methods for the assessment of prediction errors in conservation presence/absence models. Environmental Conservation, 24 (1), 38-49.
Fielding, S., Crisp, N., Allen, J., Hartman, M., Rabe, B. et al., 2001. Mesoscale subduction at the Almeria–Oran front: Part 2. Biophysical interactions. Journal of Marine Systems, 30 (3-4), 287-304.
Fossette, S., Gleiss, A.C., Chalumeau, J., Bastian, T., Armstrong, C.D. et al., 2015. Current-Oriented Swimming by Jellyfish and Its Role in Bloom Maintenance. Current Biology, 25 (3), 342-347.
Goy, J., Morand, P., Etienne, M., 1988. Long-term fluctuations of Pelagia noctiluca (Cnidaria, Scyphomedusa) in the western Mediterranean Sea. Prediction by climatic variables. Deep Sea Research, 36 (2), 269-279.
Graham, W.M., Pagès, F., Hamner, W.M., 2001. A physical context for gelatinous zooplankton aggregations: a review. Hydrobiologia, 451, 199-212.
Graham, W.M., Gelcich, S., Robinson, K.L., Duarte, C. M., Brotz, L. et al., 2014. Linking human wellbeing and jellyfish: ecosystem services, impacts and social responses. Frontiers in Ecology and the Environment, 12 (9), 515-523.
Guerrero, E., Gili, J.M., Grinyó, J., Raya, V., Sabatés, A., 2018. Long-term changes in the planktonic cnidarian community in a mesoscale area of the NW Mediterranean. PLOS ONE, 13 (5), e0196431.
Hamner, W.M., Hauri, I.R., 1981. Long-distance horizontal migrations of zooplankton (Scyphomedusae: Mastigias). Limnology and Oceanography, 26 (3), 414-423.
Hamner, W.M., Hamner, P.P., Strand, S.W., 1994. Sun-compass migration by Aurelia aurita (Scyphozoa): population retention and reproduction in Saanich Inlet, British Columbia. Marine Biology, 119 (3), 347-356.
Hamner, W.M., Dawson, M.N., 2009. A review and synthesis on the systematics and evolution of jellyfish blooms: advantageous aggregations and adaptive assemblages. Hydrobiologia 616 (1), 161-191.
Hosmer, D.W., Lemeshow, S., 2000. Applied Logistic Regression. Wiley Series in Probability and Statistics. Wiley, New York, 375 pp.
Hurrell, J.W., 1995. Decadal Trends in the North Atlantic Oscillation: Regional Temperatures and Precipitation. Science, 269 (5224), 676-679.
Hurrell, J.W., Kushnir, Y., Visbeck, M.H., 2001. CLIMATE: The North Atlantic Oscillation. Science, 291 (5504), 603-605.
Kogovšek, T., Bogunovic, B, Malej, A., 2010. Recurrence of bloom-forming scyphomedusae: wavelet analysis of a 200-year time series. Hydrobiologia, 645, 81-96.
La Spada, G., Marino, A., Sorrenti, G., 2002. Pelagia noctiluca “Blooming” in the Strait of Messina: preliminary studies on the applicability of two methods for isolating nematocytes. Marine Ecology, 23 (1), 220-227.
Lee, T., Quinn, M., Duke D., 2006. Citizen, Science, Highways, and Wildlife: Using a Web-based GIS to Engage Citizens in Collecting Wildlife Information. Ecology and Society, 11 (1), 11.
Legendre, P., Legendre, L., 1998. Numerical ecology. Second English Edition. Elsevier, 853 pp.
León, P., Blanco, J., Flexas, M., Gomis, D., Reul, A., et al., 2015. Surface mesoscale pico–nanoplankton patterns at the main fronts of the Alboran Sea. Journal of Marine Systems, 143, 7-23.
Licandro, P., Conway, D.V.P., Daly Yahia, M.N., Fernandez de Puelles, M.L., Gasparini, S. et al., 2010. A blooming jellyfish in the northeast Atlantic and Mediterranean. Biology letters, 6 (5), 688-691.
Lobo, J., Jiménez-Valverde, A., Real, R. 2008. AUC: a misleading measure of the performance of predictive distribution models. Global Ecology and Biogeography, 17 (2), 145-151.
MacAli, A., Semenov, A., Venuti, V., Crupi, V., D’Amico, F. et al., 2018. Episodic records of jellyfish ingestion of plastic items reveal a novel pathway for trophic transference of marine litter. Scientific Reports, 8 (1), 6105.
Malej, A., 1989. Behaviour and trophic ecology of the jellyfish Pelagia noctiluca (Forsskål, 1775). Journal of Experimental Marine Biology and Ecology, 126 (3), 259-270.
Mills, C.E., 2001. Jellyfish blooms: are populations increasing globally in response to changing ocean conditions? Hydrobiologia, 451 (1-3), 55-68.
Muñoz, A.R., Márquez, A.L. Real, R. 2013. Updating known distribution models for forecasting climate change impact on endangered species. PLoS ONE, 8(6): e65462.
Mutlu, E., 2001. Distribution and abundance of moon jellyfish (Aurelia aurita) and its zooplankton food in the Black Sea. Marine Biology, 138 (2), 329-339.
Oguz, T., Macias, D., Garcia-Lafuente, J., Pascual, A., Tintore, J., 2014. Fueling plankton production by a meandering frontal jet: a case study for the Alboran Sea (Western Mediterranean). PLoS ONE, 9 (11), e111482.
Palmer, J.R.B., Oltra, A., Collantes, F., Delgado, J.A., Lucientes, J. et al., 2017. Citizen science provides a reliable and scalable tool to track disease-carrying mosquitoes. Nature Communications, 8 (1), 916.
Peng, C.Y.J., Lee, K.L., Ingersoll, G.M., 2002. An Introduction to Logistic Regression Analysis and Reporting. The Journal of Educational Research, 96 (1), 3-14.
Pérez-Portela, R., Wangensteen, O.S., Garcia-Cisneros, A. et al. 2019. Spatio-temporal patterns of genetic variation in Arbacia lixula, a thermophilous sea urchin in expansion in the Mediterranean. Heredity 122, 244-259.
Piccineti-Manfrin, C., Piccinetti, C., Fiorentini, C., 1986. Distribuzione di Pelagia noctiluca in Adriatico negli anni 1983 e 1984. Nova Thalassia, 8, 99-102.
Pourjomeh, F., Shokri, M.R., Rezai, H., Rajabi-Maham, H., Maghsoudlou, E., 2017. The relationship among environmental variables, jellyfish and non-gelatinous zooplankton: A case study in the north of the Gulf of Oman. Marine Ecology, 38 (6), e12476.
Purcell, J.E., 2005. Climate effects on formation of jellyfish and ctenophore blooms: a review. Journal of the Marine Biological Association of the United Kingdom, 85 (3), 461-476.
Real, R., Barbosa, A. M., Vargas, J. M., 2006. Obtaining environmental favourability functions from logistic regression. Environmental and Ecological Statistics, 13 (2), 237-245.
Real, R., Barbosa, A. M., Bull, J. W., 2017. Species distributions, quantum theory, and the enhancement of biodiversity measures. Systematic Biology, 66 (3), 453-462.
Rottini Sandrini, L., Avian, M., 1991. Reproduction of Pelagia noctiluca in the central and northern Adriatic Sea. Hydrobiologia, 216-217, 197-202.
Sánchez-Garrido, J.C., García Lafuente, J., Álvarez Fanjul, E., Sotillo, M.G., de los Santos, F.J., 2013. What does cause the collapse of the Western Alboran Gyre? results of an operational ocean model. Progress in Oceanography, 116, 142-153.
Science Communication Unit, University of the West of England, Bristol 2013. Science for Environment Policy In- depth Report: Environmental Citizen Science. Report produced for the European Commission DG Environment, December 2013 (Accessed 25 March 2020).
Shenker, J.M., 1984. Scyphomedusae in surface waters near the Oregon coast, May-August 1981. Estuarine, Coastal and Shelf Science, 19 (6), 619-632.
Sillero, N., Martínez-Freiría, F., Real, R., Barbosa, A.M., 2010. Los modelos de nicho ecológico en la herpetología ibérica: pasado, presente y futuro. Boletín de la Asociación Herpetológica Española, 21, 2-24.
Silvertown, J., 2009. A new dawn for citizen science. Trends in Ecology and Evolution, 24 (9), 467-471.
Thompson, D.W.J., Wallace, J.M., 1998. The Arctic oscillation signature in the wintertime geopotential height and temperature fields. Geophysical Research Letters, 25 (9), 1297-1300.
Tintore, J., La Violette, P.E., Blade, I., Cruzado, A., 1988. A Study of an Intense Density Front in the Eastern Alboran Sea: The Almeria–Oran Front. Journal of Physical Oceanography, 18 (10), 1384-1397.
Tomlinson, B., Maynou, F., Sabatés, A., Fuentes, V., Canepa, A. et al., 2018. Systems approach modelling of the interactive effects of fisheries, jellyfish and tourism in the Catalan coast. Estuarine, Coastal and Shelf Science, 201, 198-207.
Zavodnik, D., 1987. Spatial aggregations of the swarming jellyfish Pelagia noctiluca (Scyphozoa). Marine Biology, 94 (2), 265-269.
Most read articles by the same author(s)