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PLOS ONE 2014

Jellyfish as Prey: Frequency of Predation and Selective Foraging of Boops boops (Vertebrata, Actinopterygii) on the Mauve Stinger Pelagia noctiluca (Cnidaria, Scyphozoa)

DOI: 10.1371/journal.pone.0094600

Giacomo Milisenda, Sara Rosa, Veronica L. Fuentes, Ferdinando Boero, Letterio Guglielmo, Jennifer E. Purcell, Stefano Piraino

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Abstract:

In recent years, jellyfish blooms have attracted considerable scientific interest for their potential impacts on human activities and ecosystem functioning, with much attention paid to jellyfish as predators and to gelatinous biomass as a carbon sink. Other than qualitative data and observations, few studies have quantified direct predation of fish on jellyfish to clarify whether they may represent a seasonally abundant food source. Here we estimate predation frequency by the commercially valuable Mediterranean bogue, Boops boops on the mauve stinger jellyfish, Pelagia noctiluca, in the Strait of Messina (NE Sicily). A total of 1054 jellyfish were sampled throughout one year to quantify predation by B. boops from bite marks on partially eaten jellyfish and energy density of the jellyfish. Predation by B. boops in summer was almost twice that in winter, and they selectively fed according to medusa gender and body part. Calorimetric analysis and biochemical composition showed that female jellyfish gonads had significantly higher energy content than male gonads due to more lipids and that gonads had six-fold higher energy content than the somatic tissues due to higher lipid and protein concentrations. Energetically, jellyfish gonads represent a highly rewarding food source, largely available to B. boops throughout spring and summer. During the remainder of the year, when gonads were not very evident, fish predation switched towards less-selective foraging on the somatic gelatinous biomass. P. noctiluca, the most abundant jellyfish species in the Mediterranean Sea and a key planktonic predator, may represent not only a nuisance for human leisure activities and a source of mortality for fish eggs and larvae, but also an important resource for fish species of commercial value, such as B. boops.

References

[1]	Arai MN (1988) Interactions of fish and pelagic coelenterates. Can J Zool 66: 1913–1927. doi: 10.1139/z88-280
[2]	Arai MN (1997) A functional biology of Scyphozoa. Chapman, Hall, editors London.
[3]	Purcell JE (1991) A review of cnidarians and ctenophores feeding on competitors in the plankton. Hydrobiologia 216–217: 335–342. doi: 10.1007/bf00026483
[4]	Purcell JE (1997) Pelagic cnidarians and ctenophores as predators: selective predation, feeding rates, and effects on prey populations. Ann l'Institut Océanogr Paris 73: 125–137.
[5]	Brodeur RD, Suchman CL, Reese DC, Miller TW, Daly EA (2008) Spatial overlap and trophic interactions between pelagic fish and large jellyfish in the northern California Current. Mar Biol 154: 649–659. doi: 10.1007/s00227-008-0958-3
[6]	Lynam CP, Heath MR, Hay SJ, Brierley AS (2005) Evidence for impacts by jellyfish on North Sea herring recruitment. Mar Ecol Prog Ser 298: 157–167. doi: 10.3354/meps298157
[7]	Lynam CP, Gibbons MJ, Axelsen BE, Sparks CAJ, Coetzee J, et al. (2006) Jellyfish overtake fish in a heavily fished ecosystem. Curr Biol 16: R492–3. doi: 10.1016/j.cub.2006.06.018
[8]	Boero F, Bouillon J, Gravili C, Miglietta M, Parsons T, et al. (2008) Gelatinous plankton: irregularities rule the world (sometimes). Mar Ecol Prog Ser 356: 299–310. doi: 10.3354/meps07368
[9]	Boero F (2013) Review of jellyfish blooms in the Mediterranean and Black Sea. Rome. FAO Fisheries Reports, 92, pp 64. Available: http://www.vliz.be/imis/imis.php?module=？ref&refid=226251. Accessed 2014 January 11.
[10]	Boero F, Belmonte G, Bracale R, Fraschetti S, Piraino S, et al. (2013) A salp bloom (Tunicata, Thaliacea) along the Apulian coast and in the Otranto Channel between March-May 2013. F1000Research 181: 1–7. Available: http://f1000research.com/articles/2-181/？v1. Accessed 2014 March 8.
[11]	Sommer U, Stibor H, Katechakis A, Sommer F, Hansen T (2002) Pelagic food web configurations at different levels of nutrient richness and their implications for the ratio fish production: primary production. Hydrobiologia 484: 11–20. Available: http://link.springer.com/chapter/10.1007？/978-94-017-3190-4_2. Accessed 2014 March 8.
[12]	Condon RH, Steinberg DK, del Giorgio PA, Bouvier TC, Bronk DA, et al. (2011) Jellyfish blooms result in a major microbial respiratory sink of carbon in marine systems. Proc Natl Acad Sci U S A 108: 10225–10230. Available: http://www.pubmedcentral.nih.gov/article？render.fcgi?artid=3121804&tool=pmcentrez？&rendertype=abstract. Accessed 2013 September 21.
[13]	Arai MN (2005) Predation on pelagic coelenterates: a review. J Mar Biol Assoc UK 85: 523–536. doi: 10.1017/s0025315405011458
[14]	Arai MN, Welch DW, Dunsmuir AL, Jacobs MC, Ladouceur AR (2003) Digestion of pelagic Ctenophora and Cnidaria by fish. Can J Fish Aquat Sci 60: 825–829. doi: 10.1139/f03-071
[15]	Miyajima Y, Masuda R, Yamashita Y (2011) Feeding preference of threadsail filefish Stephanolepis cirrhifer on moon jellyfish and lobworm in the laboratory. Plankt Benthos Res 6: : 12–17. Available: http://japanlinkcenter.org/JST.JSTAGE/pb？r/6.12?from=Google. Accessed 2013 December 4.
[16]	Yamamoto J, Hirose M, Ohtani T, Sugimoto K, Hirase K, et al. (2007) Transportation of organic matter to the sea floor by carrion falls of the giant jellyfish Nemopilema nomurai in the Sea of Japan. Mar Biol 153: : 311–317. Available: http://link.springer.com/10.1007/s00227-？007-0807-9. Accessed 2014 March 4.
[17]	Arkhipkin A, Laptikhovsky V (2013) From gelatinous to muscle food chain: rock cod Patagonotothen ramsayi recycles coelenterate and tunicate resources on the Patagonian Shelf. J Fish Biol 83: 1210–1220. Available: http://doi.wiley.com/10.1111/jfb.12217. Accessed 2014 February 3.
[18]	Cardona L, álvarez de Quevedo I, Borrell A, Aguilar A (2012) Massive consumption of gelatinous plankton by Mediterranean apex predators. PLoS One 7: e31329. Available: http://www.pubmedcentral.nih.gov/article？render.fcgi?artid=3310041&tool=pmcentrez？&rendertype=abstract. Accessed 2013 December 4.
[19]	González Carman V, Botto F, Gaitán E, Albareda D, Campagna C, et al. (2013) A jellyfish diet for the herbivorous green turtle Chelonia mydas in the temperate SW Atlantic. Mar Biol 161: 339–349. Available: http://link.springer.com/10.1007/s00227-？013-2339-9. Accessed 2014 January 29.
[20]	Mianzan HW, Mari N, Prenski B, Sanchez F (1996) Fish predation on neritic ctenophores from the Argentine continental shelf: A neglected food resource? Fish Res 27: 69–79. doi: 10.1016/0165-7836(95)00459-9
[21]	Mianzan H, Pájaro M (2001) Feeding on survival-food: gelatinous plankton as a source of food for anchovies. Hydrobiologia 451: 45–53. Available: http://link.springer.com/chapter/10.1007？/978-94-010-0722-1_5. Accessed 2013 October 14.
[22]	James M, Herman T (2001) Feeding of Dermochelys coriacea on medusae in the northwest Atlantic. Chelonian Conserv Biol 4: 202–205. Available: http://scholar.google.com/scholar?hl=en&？btnG=Search&q=intitle:Feeding+of+Dermoch？elys+coriacea+on+Medusae+in+the+Northwes？t+Atlantic#0. Accessed 2014 March 8.
[23]	Pauly D, Graham W, Libralato S, Morissette L, Deng Palomares ML (2008) Jellyfish in ecosystems, online databases, and ecosystem models. Hydrobiologia 616: 67–85. Available: http://link.springer.com/10.1007/s10750-？008-9583-x. Accessed 2014 January 13.
[24]	Heaslip SG, Iverson SJ, Bowen WD, James MC (2012) Jellyfish support high energy intake of leatherback sea turtles (Dermochelys coriacea): video evidence from animal-borne cameras. PLoS One 7: e33259. Available: http://www.pubmedcentral.nih.gov/article？render.fcgi?artid=3306388&tool=pmcentrez？&rendertype=abstract. Accessed 2014 February 10.
[25]	Galil B, Gevili R (2013) A moveable feast: Beroe cucumis sensu Mayer, 1912 (Ctenophora; Beroida; Beroidae) preying on Mnemiopsis leidyi A. Agassiz, 1865 (Ctenophora; Lobata; Bolinopsidae) off the Mediterranean coast of Israel. BioInv Rec 2: 191–194. doi: 10.3391/bir.2013.2.3.03
[26]	Polis GA, Myers CA, Holt RD (1989) The ecology and evolution of intraguild predation: potential competitors that eat each ether. Annu Rev Ecol Syst 20: 297–330. doi: 10.1146/annurev.es.20.110189.001501
[27]	Titelman J, Gandon L, Goarant A, Nilsen T (2007) Intraguild predatory interactions between the jellyfish Cyanea capillata and Aurelia aurita. Mar Biol 152: : 745–756. Available: http://link.springer.com/10.1007/s00227-？007-0721-1. Accessed 2014 March 8.
[28]	Tilves U, Purcell JE, Marambio M, Canepa A, Olariaga A, et al. (2012) Predation by the scyphozoan Pelagia noctiluca on Mnemiopsis leidyi ctenophores in the NW Mediterranean Sea. J Plankton Res 35: 218-224. Available: http://www.plankt.oxfordjournals.org/cgi？/doi/10.1093/plankt/fbs082. Accessed 2012 January 12.
[29]	Bayha KM, Graham WM, Higgins III JE, Fletcher H (2012) Predation potential of the jellyfish Drymonema larsoni Bayha & Dawson (Scyphozoa: Drymonematidae) on the moon jellyfish Aurelia sp. in the northern Gulf of Mexico. Hydrobiologia 690: 189–197. Available: http://link.springer.com/10.1007/s10750-？012-1038-8. Accessed 2013 October 30.
[30]	Schneider G (1992) A comparison of carbon-specific respiration rates in gelatinous and non-gelatinous zooplankton - a search for general rules in zooplankton metabolism. Helgol Meeresunters 46: 377–388. doi: 10.1007/bf02367205
[31]	Lucas CH, Pitt KA, Purcell JE, Lebrato M, Condon RH (2011) What's in a jellyfish? Proximate and elemental composition and biometric relationships for use in biogeochemical studies. Ecology 92: 1704. doi: 10.1890/11-0302.1
[32]	B？mstedt U, Ishii H, Martinussen M (1997) Is the scyphomedusa Cyanea capillata (l.) dependent on gelatinous prey for its early development? Sarsia 82: 269–273.
[33]	Purcell JE, Arai MN (2001) Interactions of pelagic cnidarians and ctenophores with fish: a review. Hydrobiologia 451: 27–44. doi: 10.1007/978-94-010-0722-1_4
[34]	Utne-Palm AC, Salvanes AGV, Currie B, Kaartvedt S, Nilsson GE, et al. (2010) Trophic Structure and community stability in an overfished ecosystem. Science 329: 333–336. doi: 10.1126/science.1190708
[35]	Canepa A, Fuentes V, Sabatés A, Piraino S, Boero F, et al. (2014) Pelagia noctiluca in the Mediterranean Sea. In: Pitt KA, Lucas CH, editors. Jellyfish blooms. Springer Netherlands. pp. 237–266.
[36]	Bjorndahl K (1997) Foraging ecology and nutrition of sea turtles. In: Lutz P, Musick J, editors. The biology of sea turtles. New York, NY. pp. 199–231.
[37]	Houghton JDR, Doyle TK, Wilson MW, Davenport J, Hays GC (2006) Jellyfish aggregations and leatherback turtle foraging patterns in a temperate coastal environment. Ecology 87: 1967–1972. doi: 10.1890/0012-9658(2006)87[1967:jaaltf]2.0.co;2
[38]	Bauchot M, Hureau J (1986) Sparidae. In: Whitehead P, Bauchot M, Hureau J, Nielsen J, Tortonese E, editors. Fishes of the north-eastern Atlantic and Mediterranean. Vol. II. U.K.: UNESCO. pp. 883–907.
[39]	Sanches JG (1992) Guia para identifica？？o do pescado de Portugal submetido a tamanho mínimo de captura. Lisboa: Instituto Nacional de Investiga？？o das Pescas [Divis？o de Informa？？o e Documenta？？o Científica e Técnica].
[40]	Riede K (2004) Global register of migratory species - from global to regional scales. Final Report of the R&D-Projekt 808 05 081. Bonn. Available: http://d-nb.info/970973322/04. Accessed 2013 November 14.
[41]	Dobroslavi？ T, Zlatovi？ A, Bartulovi？ D, Lu？i？ D, Glamuzina B (2013) Diet overlap of juvenile salema (Sarpa salpa), bogue (Boops boops) and common two-banded sea bream (Diplodus vulgaris) in the south-eastern Adriatic. J Appl Ochthyol 29: 181–185. doi: 10.1111/j.1439-0426.2012.02046.x
[42]	Derbal F, Kara MH (2008) Composition du régime alimentaire du bogue Boops boops des c？tes de l'Est Algérien. Cybium 2: 325–333.
[43]	Malej A, Vukovi？ A (1986) Some data on the metabolism of Pelagia noctiluca in the Gulf of trieste. Nov Thalass 8: 107–111.
[44]	Vucetic T, Alegria-Hernandez V (1988) Trends of annual catches or stock densities of some pelagic fishes in recent “Pelagia years” in the Adriatic. FAO Fisheries Reports, 133–136 No.394.
[45]	Spallanzani L (1799) Méduses phosphoriques observées dans le détroit de Messine. Voyages dans les deux Siciles et dans quelques uarties des Apennins. Paris. pp. Vol. 1, pp. 1–37, Vol. 4, pp. 137–171.
[46]	Rosa S, Pansera M, Granata A, Guglielmo L (2013) Interannual variability, growth, reproduction and feeding of Pelagia noctiluca (Cnidaria: Scyphozoa) in the Straits of Messina (Central Mediterranean Sea): Linkages with temperature and diet. J Mar Syst 111–112: 97–107. Available: http://linkinghub.elsevier.com/retrieve/？pii/S0924796312001972. Accessed 2013 September 21.
[47]	Azzaro F, Decembrini F (2007) Seasonal variability of phytoplankton fluorescence in relation to the Straits of Messina (Sicily) tidal upwelling. Ocean Sci Discuss 4: 415–440. Available: http://hal.archives-ouvertes.fr/hal-0029？8476/. Accessed 2013 November 15.
[48]	De Domenico M, Cortese G, Pulicano G, De Domenico E (1988) Variazione spazio-temporale di nutrienti, clorofilla e carica microbica nelle acque dello Stretto di Messina. Atti AIOL 8: 337–355.
[49]	Azzaro F, Decembrini F, Crisafi E (1995) Continuos survey of upwelling in the Straits of Messina. Rapp Comm Int Mer Medit 34: 167.
[50]	Magazzu G, Decembrini F (1995) Primary production, biomass and abundance of phototrophic picoplankton in the Mediterranean Sea: a review. Aquat Microb Ecol 9: : 97–104. Available: http://cat.inist.fr/?aModele=afficheN&cp？sidt=3555288. Accessed 2013 December 23.
[51]	Kinder T, Bryden H (1990) Aspiration of deep waters through straits. In: Pratt LJ, editor. The physical oceanography of sea straits. Springer Netherlands, Vol. 318. pp. 295–319.
[52]	Anderson MJ (2001) Permutation tests for univariate or multivariate analysis of variance and regression. Can J Fish Aquat Sci 58: 626-639. Available: http://www.nrc.ca/cgi-bin/cisti/journals？/rp/rp2_abst_e?cjfas_f01-004_58_ns_nf_cj？fas58-01. Accessed 2013 October 19.
[53]	Doyle TK, Houghton JDR, McDevitt R, Davenport J, Hays GC (2007) The energy density of jellyfish: Estimates from bomb-calorimetry and proximate-composition. J Exp Mar Bio Ecol 343: 239–252. Available: http://linkinghub.elsevier.com/retrieve/？pii/S0022098107000172. Accessed 2013 September 21.
[54]	Malej A, Faganelli J, Pezdi？ J (1993) Stable isotopes and biochemical fractionation in the marine pelagic food chain: the jellyfish Pelagia noctiluca and net zooplankton. Mar Biol 116: 565–570. doi: 10.1007/bf00355475
[55]	Dubois M, Gilles K, Hamilton J, Reber P, Smith F (1956) Colorimetric method for determination of sugar and related substances. Anal Chem 28: 350–356. doi: 10.1021/ac60111a017
[56]	Lowry O (1951) Protein measurement with Folin phenol reagent. J Biol Chem 193: 265.
[57]	Barnes H, Blackstock J (1973) Estimation of lipids in marine animals tissues: detailed investigation of the sulphophosphovanill in method for “total” lipids. J Exp Mar Biol Ecol 12: 103–118. doi: 10.1016/0022-0981(73)90040-3
[58]	Reina-Hervás JA, Serrano P (1987) Structural and seasonal variations of inshore fish populations in Málaga Bay, southeastern Spain. Mar Biol 95: 501–508. doi: 10.1007/bf00393093
[59]	Sabatés A, Olivar M (1996) Variation of larval fish distributions associated with variability in the location of a shelf-slope front. Mar Ecol Prog Ser 1: 1–20. Available: http://www.int-res.com/abstracts/meps/v1？35/p11-20/. Accessed 2014 March 8.
[60]	Avian M, Sandrini LR (1991) Oocyte development in four species of scyphomedusa in the northern Adriatic Sea. Hydrobiologia 216/217: 189–195. doi: 10.1007/bf00026461
[61]	Epigenetics I, Sunderland DE, Sin MA (2009) Ecological developmental biology: integrating epigenetics, medicine, and evolution. By. Yale J Biol Med 82: 231–236.
[62]	Adams M, Johnsen P (1986) Chemical control of feeding in herbivorous and carnivorous fish. In: Duvall D, Müller-Schwarze D, Silverstein R, editors. Chemical signals in vertebrates. Springer US. pp. 45–61.
[63]	Guidetti P (2004) Fish assemblages associated with coastal defence structures in south-western Italy (Mediterranean Sea). J Mar Biol Assoc UK 84: 669–670. doi: 10.1017/s0025315404009725h
[64]	Sibly R, Calow P (1986) Physiological ecology of animals: an evolutionary approach. Oxford: Blackwell Science Inc.
[65]	Ates RML (1991) Predation on Cnidaria by vertebrates other than fishes. Hydrobiologia 216–217: 305–307. doi: 10.1007/bf00026479
[66]	Buecher E, Sparks C, Brierley A, Boyer H, Gibbons M (2001) Biometry and size distribution of Chrysaora hysoscella (Cnidaria, Scyphozoa) and Aequorea aequorea (Cnidaria, Hydrozoa) off Namibia with some notes on their parasite Hyperia medusarum. J Plankton Res 23: 1073–1080. doi: 10.1093/plankt/23.10.1073
[67]	Gende SM, Quinn TP, Willson MF (2001) Consumption choice by bears feeding on salmon. Oecologia 127: 372–382. Available: http://link.springer.com/10.1007/s004420？000590. Accessed 2014 January 21.
[68]	Ford J, Ellis G (2006) Selective foraging by fish-eating killer whales Orcinus orca in British Columbia. Mar Ecol Prog Ser 316: 185–199. doi: 10.3354/meps316185
[69]	Svensson J-E (1997) Fish predation on Eudiaptomus gracilis in relation to clutch size, body size, and sex: a field experiment. Hydrobiologia 344: 155–161.
[70]	Dittrich B (1988) Studies on the life cycle and reproduction of the parasitic amphipod Hyperia galba in the North Sea. Helgol？nd Meeresunters 42: 79–98. doi: 10.1007/bf02364205
[71]	Laval P (1980) Hyperiid amphipods as crustacean parasitoids associated with gelatinous zooplankton. Oceanogr Mar Biol Ann Rev 18: 11–56.
[72]	Ates RML (1988) Medusivorous fishes, a review. Zool Meded 62: 29–42.

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