| More

Population dynamics and predatory impact of the alien jellyfish Aurelia solida (Cnidaria, Scyphozoa) in the Bizerte Lagoon (southwestern Mediterranean Sea)

Views: 647 Downloads: 286
SONIA K.M. GUEROUN, JUAN CARLOS MOLINERO, STEFANO PIRAINO, MOHAMED NEJIB DALY YAHIA
SONIA K.M. GUEROUN, JUAN CARLOS MOLINERO, STEFANO PIRAINO, MOHAMED NEJIB DALY YAHIA

Abstract


Understanding the life cycle strategies and predatory impact of alien jellyfish species is critical to mitigate the impact these organisms may have on local populations, biodiversity, and ultimately on the functioning of food webs. In the Mediterranean Sea, little is known about the dynamics of alien jellyfish, although this area is a biodiversity hotspot and one of the most threatened by an increasing number of alien jellyfish. Here, we investigated the population dynamics and predatory impact of a non-indigenous scyphomedusa, Aurelia solida Browne 1905, in the Bizerte Lagoon, Tunisia. The study was based on a bimonthly survey performed over two consecutive years, from November 2012 to August 2014. Field observations showed that the planktonic phase of A. solida occurs from winter to early summer. Prey composition was investigated by means of gut content and field zooplankton analyses. Calanoid copepods, mollusc larvae and larvaceans represented the main food items of A. solida. To determine the jellyfish feeding rate and their predatory impact on zooplankton populations, the digestion time for zooplankton prey was assessed at three different temperatures: 13, 18 and 23 °C in laboratory conditions, corresponding to the average range of temperatures encountered by A. solida in the Bizerte Lagoon. We found that A. solida consumed 0.5–22.5% and 0.02–37.3% of the daily zooplankton standing stock in 2013 and 2014, respectively. These results indicate a non-negligible but restricted seasonal grazing impact on some mesozooplankton groups, explained by the relatively short lifespan of the medusa stage (5–6 months).


Keywords


Scyphomedusae; abundance; predation; mesozooplankton; SW Mediterranean.

Full Text:

PDF

References


Alsterberg, C., Eklof, J.S., Gamfeldt, L., Havenhand, J.N.,Sundback, K., 2013. Consumers mediate the effects of experimentalocean acidification and warming on primaryproducers. Proceedings of the National Academy of Sciences,110 (21), 8603-8608.

Aoki, K., Yamada, S., Toyokawa, M., Ysuda, A., Kikuchi, T.,2012. Horizontal distribution and growth of jellyfish, Aureliaaurita (Linnaeus 1758) sensu lato, in Mikawa Bay, Japan. Coastal Marine Science, 35, 103-111.

Bailey, K.M., Batty, R.S., 1983. A laboratory study of predationby Aurelia aurita on larval herring (Clupea harengus): Experimentalobservations compared with model predictions.Marine Biology, 72 (3), 295-301.

Balistreri, P., Spiga, A., Deidun, A., Gueroun, S.K.M., Daly-Yahia,M.N., 2017. Further spread of the venomous jellyfishRhopilema nomadica Galil, Spannier & Ferguson, 1990(Rhizostomeae, Rhizostomatidae) in the western Mediterranean.BioInvasions Records, 6, 19-24.

Båmstedt, U., Martinussen, M.B., 2000. Estimating digestionrate and the problem of individual variability, exemplifiedby a scyphozoan jellyfish. Journal of Experimental MarineBiology and Ecology, 251, 2-15.

Barz, K., Hirche, H.J., 2005. Seasonal development of scyphozoanmedusae and the predatory impact of Aurelia aurita onthe zooplankton community in the Bornholm Basin (centralBaltic Sea). Marine Biology, 147 (2), 465-476.

Berstad, V., Båmstedt, U., Martinussen, M.B., 1995. Distributionand swimming of the jellyfishes Aurelia aurita andCyanea capillata. p. 257-271. In: Ecology of Fjords andCoastal Waters. Skjoldal, H.R., Hopkins, C., Erikstad,K.E., Leinaas, H.P. (Eds). Elsevier, Amsterdam.

Boero, F., 2013. Review of jellyfish blooms in the Mediterraneanand Black Sea. Rome, FAO Fisheries Reports, 64 pp.

Bone, Q., Mackie, G.O., 1975. Skin impulses and locomotionin Oikopleura (Tunicata: Larvacea). Biological Bulletin,149 (2), 267-286.

Bonnet, D., Molinero, J.C., Schohn, T., Daly-Yahia, M.N.,2012. Seasonal changes in the population dynamics of Aureliaaurita in Thau lagoon. Cahier de Biologie Marine, 53,343-347.

Boudouresque, C.H., 1999. Introduced species in the Mediterranean:routes, kinetics and consequences. p. 51-72. In:Proceedings of the Workshop on invasive Caulerpa speciesin the Mediterranean, MAP Technical Report Series,UNEP, Athens.

Brotz, L., 2011. Changing jellyfish populations: trends in largeMarine Ecosystems. Fisheries Centre Research Report, 19(5), 1-105.

Brotz, L., Pauly, D. 2012. Jellyfish populations in the MediterraneanSea. Acta Adriatica, 53 (2), 213-232.

Brotz, L., Cheung, W.W.L., Kleisner, K., Pakhomov, E., Pauly,D., 2012. Increasing jellyfish populations: trends in LargeMarine Ecosystems. Hydrobiologia, 690 (1), 3-20.

Brunetti, R., Baiocchi, L., Bressan, M., 1990. Seasonal distributionof Oikopleura (Larvacea) in the Lagoon of Venice.Bolletino di Zoologia, 57 (1), 89-94.

Chakroun, F., Aloui-Bejaouin, N., 1995. Invasion d’Aurelia aurita(Cnidaria, Scyphomédusa) dans le lac de Bizerte (Tunisie)au cours de l’été 1994. Annales de l’Institut Océanographique,71, 67-69.

Daly-Yahia, M.N., Goy, J., Daly Yahia-Kéfi, O., 2003. Distributionet écologie des Méduses (Cnidaria) du golfe de Tunis(Méditerranée sud occidentale). Oceanologica Acta, 26,645-655.

Dawson, M.N., Jacobs, D.K., 2001. Molecular evidence forcryptic species of Aurelia aurita (Cnidaria, Scyphozoa). BiologyBulletin, 200, 92-96.

Dawson, M.N., Martin, L.E., 2001. Geographic variation andecological adaptation in Aurelia (Scyphozoa, Semaeostmeae):some implications from molecular phylogenetics. Hydrobiologia,451, 259-273.

Duarte, C.M., Pitt, K., Lucas, C.H., Purcell, J.E., Uye, S.I. et al., 2013. Is global ocean sprawl a cause of jellyfish blooms?Frontiers in Ecology and the Environment, 11(2), 91-97.

El-Serehy, H.A., Al-Rasheid, K.A., 2011. Reproductive strategyof the jellyfish Aurelia aurita (Cnidaria Scyphomedusae)in the Suez Canal and its migration between the RedSea and Mediterranean. Aquatic Ecosystem Health & Management,14, 269-275.

Fellous, A., Favrel, P., Riviere, G., 2015. Temperature influenceshistone methylation and mRNA expression of the Jmj-Chistone-demethylase orthologues during the early developmentof the oyster Crassostrea gigas. Marine Genomics,19, 23-30.

Fu, Z., Shibata, M., Makabe, R., Ikeda, H., Uye, S.I., 2014.Body size reduction under starvation, and the point of noreturn, in ephyrae of the moon jellyfish Aurelia aurita. MarineEcology Progess Series, 510 (1), 255-263.

Fuchs, B., Wang, W., Graspeuntner, S., Li, Y., Insua, S. et al.,2014. Regulation of polyp-to-jellyfish transition in Aureliaaurita. Current Biology, 24 (3), 263-273.

Gómez Daglio, L.G., Dawson, M.N., 2017. Species richnessof jellyfishes (Scyphozoa: Discomedusae) in the TropicalEastern Pacific: missed taxa, molecules, and morphologymatch in a biodiversity hotspot. Invertebrate Systematics,31 (5), 635-663.

Grace, J.J., Anderson, T.M., Olff, H., Scheiner, S.M., 2010. Onthe specification of structural equation models for ecologicalsystems. Ecological Monographs, 80 (1), 67-87.

Graham, W.M., Kroutil, R.M., 2001. Size-based prey selectivityand dietary shift in the jellyfish, Aurelia aurita. Journalof Plankton Research, 23 (1), 67-74.

Gröndahl, F., 1988. A comparative ecological study on the scyphozoansAurelia aurita, Cyanea capillata and C. lamarckiiin the Gullmar Fjord, western Sweden, 1982 to 1986. MarineBiology, 97, 541-550.

Gueroun, S.K.M., Kéfi-Daly Yahia, O., Deidun, A., Fuentes,V.L., Piraino, S. et al., 2014. First record and potential trophicimpact of Phyllorhiza punctata (Cnidaria: Scyphozoa)along the north Tunisian coast (South Western MediterraneanSea). Italian Journal of Zoology, 82, 95-100.

Heeger, T., Möller, H. 1987. Ultrastructural observations onprey capture and digestion in the scyphomedusa Aureliaaurita. Marine Biology, 96, 391-400.

Hernroth, L., Gröndahl, F. 1985. On the biology of Aurelia aurita.Bulletin of Marine Science, 37 (2), 567-576.Heyland, A., Moroz, L.L., 2006. Signaling mechanisms underlyingmetamorphic transitions in animals. Integrative andComparative Biology, 46 (6), 743-759.

Holst, S., 2012. Effects of climate warming on strobilation andephyra production of North Sea scyphozoan jellyfish. Hydrobiologia,690 (1), 127-140.

Hubot, N., Lucas, C.H., Piraino, S., 2017. Environmental controlof asexual reproduction and somatic growth of Aureliaspp. (Cnidaria, Scyphozoa) polyps from the Adriatic Sea. PLoS ONE, 12 (6), e0178482.

Ishii, H., Tanaka, F., 2001. Food and feeding of Aurelia auritain Tokyo Bay with an analysis of stomach contents and ameasurement of digestion times. Hydrobiologia, 451, 311-320.

Khessiba, A., Hoarau, P., Gnassia-Barelli, M., Aissa, P., Roméo,M., 2001. Biochemical response of the mussel Mytilus galloprovincialisfrom Bizerta (Tunisia) to chemical pollutantexposure. Archives of Environmental Contamination andToxicology, 40 (2), 222-229.

Kinoshita, J., Hiromi, J., Yamada, Y., 2006. Abundance andbiomass of scyphomedusae, Aurelia aurita and Chrysaoramelanaster, and Ctenophora, Bolinopsis mikado, with estimatesof their feeding impact on zooplankton in Tokyo Bay,Japan. Journal of Oceanography, 62, 607-615.

Kogovšek, T., Molinero, J.C., Lučić, D., Onofri, I., Gangai, B.et al., 2012. Interannual size changes of adult Aurelia sp. 5medusae stage in the Marine Protected Area of Mljet IslandSouth Adriatic. Acta Adriatica, 53 (2), 231-240.

Laroche, J.L., 1982. Trophic patterns among larvae of fivespecies of Sculpins (Family: Cottidae) in a Maine estuary.Fishery Bulletin, 80 (4), 827-840.

Lo, W-T., Chen, I.L., 2008. Population succession and feedingof scyphomedusae, Aurelia aurita, in a eutrophic tropicallagoon in Taiwan. Estuarine, Coastal and Shelf Science, 76,227-238.

Lucas, C.H., 1996. Population dynamics of Aurelia aurita(Scyphozoa) from an isolated brackish lake, with particularreference to sexual reproduction. Journal of PhysicalOceanography, 18 (6), 987-1007.

Lucas, C.H., 2001. Reproduction and life history strategies ofthe common jellyfish, Aurelia aurita, in relation to its ambientenvironment. Hydrobiologia, 451, 229-246.

Lucas, C.H., Williams, J.A., 1994. Population dynamics of thescyphomedusa Aurelia aurita in Southampton Water. Journalof Plankton Research, 16 (7), 879-895.

Lucas, C.H., Graham, W.M., Widmer, C., 2012. Jellyfish lifehistories: role of polyps in forming and maintaining Scyphomedusapopulations. Advances in Marine Biology, 63,132-196.

Lynam, C.P., Heath, M.R., Hay, S.J., Brierley, A.S., 2005. Evidencefor impacts by jellyfish on North Sea herring recruitment.Marine Ecology Progress Series, 298, 157-167.

Madin, L.P., 1988. Feeding behaviors of tentaculate predators:in situ observation and a conceptual model. Bulletin of MarineScience, 43 (3), 413-429.

Malej, A., Kogovšek, T., Ramšak, A., Catenacci, L., 2012.Blooms and population dynamics of moon jellyfish in thenorthern Adriatic. Cahiers de Biologie Marine, 53, 337-342.

Marques, R., Albouy-Boyer, S., Delpy, F., Carré, C., Le Floc’H,É. et al., 2015. Pelagic population dynamics of Aurelia sp.in French Mediterranean lagoons. Journal of Plankton Research,37 (5), 1019-1035.

Martinussen, M.B., Båmstedt, U., 1995. Diet, estimated dailyfood ration and predator impact by the scyphozoan jellyfishesAurelia aurita and Cyanea capillata. p 127-145. In:Ecology of Fjords and Coastal Waters. Skjoldal, H., Hopkins,C., Erikstad, K., Leinaas, H. (Eds). Elsevier SciencePublishers, Amsterdam.

Martinussen, M.B., Båmstedt, U., 2001. Digestion rate in relationto temperature of two planktonic predators. Sarsia,86, 21-35.

Matsakis, S., Conover, R.J., 1991. Abundance and feeding ofmedusae and their potential predators on other zooplanktonin Bedford Basin (Nova Scotia, Canada) during spring.Canadian Journal of Fisheries and Aquatic Sciences, 48,1419-1430.

Milisenda, M., Rossi, S., Vizzini, S., Fuentes, V.L., Purcell, J.Eet al., 2018. Seasonal variability of diet and trophic levelof the gelatinous predator Pelagia noctiluca (Scyphozoa).Scientific Reports, 8, 12140.

Miyake, H., Terazaki, M., Kakinuma, Y., 2002. On the polypsof the common jellyfish Aurelia aurita in Kagoshima Bay.Journal of Oceanography, 58, 451-459.

Molinero, J.C., Casini, M., Buecher, E., 2008. The influenceof the Atlantic and regional climate variability on the longtermchanges in gelatinous carnivore populations in thenorthwestern Mediterranean. Limnology and Oceanography,53 (4), 1456-1467.

Möller, H., 1980. Population dynamics of Aurelia aurita in KielBight, Germany (FRG). Marine Biology, 60, 123-128.

Möller, H., 1984. Reduction of a larval herring population byjellyfish predator. Science, 224 (4649), 621-622.

Mutlu, E., 2001. Distribution and abundance of moon jellyfish(Aurelia aurita) and its zooplankton food in the Black Sea.Marine Biology, 138, 329-339.

Olsen, N.J., 1995. Clearance potential of jellyfish Aurelia aurita,and predation impact on zooplankton in a shallow cove.Marine Ecology Progress Series, 124, 63-72.

Olsen, N.J., Frandsen, K., Riisgård, H.U., 1994. Population dynamics,growth and energetics of jellyfish Aurelia aurita ina shallow fjord. Marine Ecology Progess Series, 105, 9-18.

Papathanassiou, E., Panayotidis, P., Anagnostaki, K., 1987.Notes on the biology and ecology of the jellyfish Aureliaaurita LAM. in Elefsis Bay (Saronikos Gulf, Greece).MarineBiology, 8 (1), 49-58.

Pearre, S.Jr., 1982. Estimating prey preference by Predators:Uses of various indices, and a proposal of another based onχ2. Canadian Journal of Fisheries and Aquatic Sciences,39 (6), 914-923.

Pitt, K.A., Budarf, A.C., Browne, J.G., Condon, R.H., 2014.Bloom and bust: why do blooms of jellyfish collapse? p.1-304. In: Jellyfish Blooms. Pitt, K.A., Lucas, C.H. (Eds).Springer, Dordrecht.

Purcell, J.E., 1991. A review of cnidarians and ctenophoresfeeding on competitors in the plankton. Hydrobiologia,216/217, 335-342.

Purcell, J.E., 2003. Predation on zooplankton by large jellyfish,Aurelia labiata, Cyanea capillata and Aequorea aequorea,in Prince William Sound, Alaska. Marine Ecology ProgressSeries, 246, 137-152.

Purcell, J.E., 2005. Climate effects on formation of jellyfish andctenophore blooms: a review. Journal of the Marine BiologicalAssociation of the United Kingdom, 85 (3), 461-476.

Purcell, J.E., 2007. Environmental effects on asexual reproductionrates of the scyphozoan Aurelia labiata. Marine EcologyProgess Series, 348, 183-196.

Purcell, J.E., 2009. Extension of methods for jellyfish andctenophore trophic ecology to large-scale research. Hydrobiologia,616, 23-50.

Purcell, J.E., Sturdevant, M.V., 2001. Prey selection and dietaryoverlap among zooplanktivorous jellyfish and juvenile fishesin Prince William Sound, Alaska. Marine Ecology ProgessSeries, 210, 67-83.

Purcell, J.E., Uye, S., Lo, W.T., 2007. Anthropogenic causes ofjellyfish blooms and their direct consequences for humans :a review. Marine Ecology Progress Series, 350, 153-174.

Purcell, J.E., Cressweli, F.P., Cargo, D.G., Kennedy, V.S., 1991.Differencial ingestion and digestion of bivalve larvae by the Scyphozoan Chrysaora quiquecirrha and the ctenophoreMnemiopsis leidyi. Biology Bulletin, 108, 103-111.

Purcell, J.E., Atienza, D., Fuentes, V.L., Olariaga, A., Tilves, U.et al., 2012. Temperature effects on asexual reproductionrates of scyphozoan species from the northwest MediterraneanSea. Hydrobiologia, 690, 169-180.

Purcell, J.E., Milisenda, G., Rizzo, A., Carrion, S.A., Zampardi,S. et al., 2015. Digestion and predation rates of zooplanktonby the pleustonic hydrozoan Velella velella and widespreadblooms in 2013 and 2014. Journal of Plankton Research,37 (5), 1056-1067.

Riisgård, H.U., Christensen, P.B., Olesen, N.J., Petersen, J.K.,Møller, M.M. et al., 1995. Biological structure in a shallowcove (Kertinge Nor, Denmark)-Control by benthic nutrientfluxes and suspension-feeding ascidians and jellyfish.Ophelia, 41 (1), 329-344.

Sabatés, A., Pagès, F., Atienza, D., Fuentes, V.L., Purcell, J.E.et al., 2010. Planktonic cnidarian distribution and feedingof Pelagia noctiluca in the NW Mediterranean Sea. Hydrobiologia,645 (1), 153-165.

Sakka-Hlaili, A., Grami, B., Niquil, N., Gosselin, M., Hamel,D. et al., 2008. The planktonic food web of the Bizertelagoon (south-western Mediterranean) during summer:I. Spatial distribution under different anthropogenic pressures.Estuarine, Coastal and Shelf Science, 78 (1), 61-77.

Scheinberg, R.D., Landry, M.R., Calbet, A., 2005. Grazingof two common appendicularians on the natural prey assemblageof a tropical coastal ecosystem. Marine EcologyProgress Series, 294, 201-212.

Schroth, W., Jarms, G., Streit, B., Schierwater, B., 2002. Speciationand phylogeography in the cosmopolitan marinemoon jelly, Aurelia sp. BMC Evolutionary Biology, 2, 1-10.

Scorrano, S., Aglieri, G., Boero, F., Dawson, M.N., Piraino, S.,2017. Unmasking Aurelia species in the Mediterranean Sea: An integrative morphometric and molecular approach. ZoologicalJournal of the Linnean Society, 180 (2), 243-267.

Singarajah, K., 1975. Escape reactions of zooplankton: effectsof light and turbulence. Journal of the Marine BiologicalAssociation of the United Kingdom, 55, 627-639.

Suchman, C.L., 2000. Escape behavior of Acartia hudsonicacopepods during interactions with scyphomedusae. Journalof Plankton Research, 22 (12), 2307-2323.

Sullivan, B.K., Garcia, J.R., Klein-MacPhee, G., 1994. Preyselection by the scyphomedusan predator Aurelia aurita.Marine Biology, 121, 335-341.

Tilves U., Fuentes, V., Purcell, J.E., Torrents, A., Pascual, M.et al., 2016. Natural diet and predation impacts of Pelagianoctiluca on fish eggs and larvae in the NW Mediterranean.Journal of Plankton Research, 38 (5), 1243-1254.

Touzri, C., Kéfi-Daly Yahia, O., Hamdi, H., Goy, J., Daly-Yahia,M.N., 2010. Spatio-temporal distribution of Medusae(Cnidaria) in the Bay of Bizerte (South Western MediterraneanSea). Cahier de Biologie Marine, 51, 167-176.

Touzri, C., Hamdi, H., Goy, J., Daly-Yahia, M.N., 2012. Diversityand distribution of gelatinous zooplankton in theSouthwestern Mediterranean Sea. Marine Ecology, 33 (4),393-406.

Toyokawa, M., Furota, T., Terazaki, M., 2000. Life history andseasonal abundance of Aurelia aurita medusae in TokyoBay, Japan. Plankton Biology and Ecology, 47 (I), 48-58.

Verity, P.G., Purcell, J.E., Frischer, M.E., 2011. Seasonal patternsin size and abundance of Phyllorhiza punctata: aninvasive scyphomedusa in coastal Georgia (USA). MarineBiology, 158 (10), 2219-2226.

Wang, N., Li, C., Liang, Y., 2015a. Prey concentration and temperatureeffect on budding and strobilation of Aurelia sp. 1polyps. Hydrobiologia, 754 (1), 125-134.

Wang, Y.T., Zheng, S., Sun, S., Zhang, F., 2015b. Effect of temperatureand food type on asexual reproduction in Aureliasp. 1 polyps. Hydrobiologia, 754 (1), 169-178.


Refbacks

  • There are currently no refbacks.