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Marine Biology

, Volume 162, Issue 12, pp 2339–2350 | Cite as

Climate-driven population size fluctuations of jellyfish (Chrysaora plocamia) off Peru

  • Javier Quiñones
  • Hermes Mianzan
  • Sara Purca
  • Kelly L. Robinson
  • Grant D. Adams
  • E. Marcelo Acha
Original Paper

Abstract

There is a general concern that jellyfish populations are increasing throughout marine ecosystems worldwide, mainly due to environmental (e.g., climate drivers) and anthropogenic forces (e.g., overfishing and eutrophication), or interactions among them. To identify drivers of jellyfish populations in the heavily fished northern Humboldt upwelling system (NHUS), we examined linkages between a 43-year-long annual time series (1972–2014) of the biomass of the scyphomedusae Chrysaora plocamia and several forcing factors: the Peruvian Oscillation Index, the Regime Indicator Series and commercial landings of Peruvian anchovy. We found that C. plocamia biomass fluctuated with climate drivers, but not with anchovy landings (a proxy of fishing pressure). Jellyfish biomass was high and variable during the warm El Viejo regime in the 1970s and 1980s, with peaks connected to intra-regime El Niño Southern Oscillation (ENSO) events. By contrast, no peaks occurred during warming events in the cold La Vieja regime in the late 1990s and 2000s when jellyfish biomass was very low or below detection; however, at the end of the study period, biomass rose slightly. The fishing pattern in the NHUS is just the opposite of those that previously have been attributed to removing small pelagic fish. We suggest that environmental factors and prey availability act synergistically to generate observed population size variability of this medusa in the NHUS.

Keywords

Pacific Decadal Oscillation Small Pelagic Fish Jellyfish Bloom Jellyfish Population Jellyfish Abundance 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank the Instituto del Mar del Perú (IMARPE) headquarters at Callao and regional laboratory at Pisco for permission and funding in conducting this investigation. We also thank the reviewers and editors for their assistance, especially to William “Monty” Graham for the earlier version. We thank Hermes Mianzan who was an outstanding person and scientist. This work was supported by the following grants: PIP 112-201101-00892; CRN3070 from the Inter-American Institute for Global Change Research (IAI), which is supported by the US National Science Foundation (Grant GEO-1128040), and EXA 647/14 to H. Mianzan and M. Acha. KL Robinson was supported by a Lenfest Ocean Program Grant (No. 00025535) funded by the Pew Charitable Trusts to WM Graham at The University of Southern Mississippi.

Funding

This study was funded by the following grants: PIP 112–201101–00892; CRN3070 from the Inter-American Institute for Global Change Research (IAI), which was supported by the US National Science Foundation (Grant GEO-1128040), and EXA 647/14 to H. Mianzan and M. Acha.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Human participants and animals consent

No human experimentation was involved in this research. The animals (jellyfish) used in this study were at low taxonomical resolution and were captured as bycatch in the pelagic scientific research cruises.

Supplementary material

227_2015_2751_MOESM1_ESM.pdf (156 kb)
Supplementary material 1 (PDF 156 kb)

References

  1. Alheit J, Niquen M (2004) Regime shifts in the Humboldt Current ecosystem. Prog Oceanogr 60:201–222. doi: 10.1016/j.pocean.2004.02.006 CrossRefGoogle Scholar
  2. Arai MN (2005) Predation on pelagic coelenterates: a review. J Mar Biol Assoc UK 85:523–536. doi: 10.1017/S0025315405011458 CrossRefGoogle Scholar
  3. Ayón P, Swartzman G, Bertrand A, Gutiérrez M, Bertrand S (2008) Zooplankton and forage fish species off Peru: large-scale bottom-up forcing and local-scale depletion. Prog Oceanogr 79:208–214. doi: 10.1016/j.pocean.2008.10.023 CrossRefGoogle Scholar
  4. Ayón P, Swartzman G, Espinoza P, Bertran A (2011) Long-term changes in zooplankton size distribution in the Peruvian Humbodt Current System: conditions favoring sardine or anchovy. Mar Ecol Prog Ser 422:211–222. doi: 10.3354/meps08918 CrossRefGoogle Scholar
  5. Bakun A (1998) Ocean triads and radical interdecadal variation: bane and boon to scientific fisheries management. In: Pitcher T, Haert PJ, Paula D (eds) Reinventing fisheries management. Springer, Dordrecht, pp 331–358. doi: 10.1007/978-94-011-4433-9_25 CrossRefGoogle Scholar
  6. Bakun A, Weeks SJ (2006) Adverse feedback sequences in exploited marine systems: are deliberate interruptive actions warranted? Fish Fish 7:316–333. doi: 10.1111/j.1467-2979.2006.00229.x CrossRefGoogle Scholar
  7. Bayha MK, Graham WM (2014) Nonindigenous marine jellyfish: invasiveness, invasibility and impacts. In: Pitt KA, Lucas CH (eds) Jellyfish blooms. Springer, Dordrecht, pp 45–77. doi: 10.1007/978-94-007-7015-7_1 CrossRefGoogle Scholar
  8. Bertrand A, Segura M, Gutiérrez M, Vásquez L (2004) From small-scale habitat loopholes to decadal cycles: a habitat-based hypothesis explaining fluctuation in pelagic fish populations off Peru. Fish Fish 5:296–316. doi: 10.1111/j.1467-2679.2004.00165.x CrossRefGoogle Scholar
  9. Bigelow KA, Boggs CH, He X (1999) Environmental effects on swordfish and blue shark catch rates in the US North Pacific longline fishery. Fish Oceanogr 8:178–198. doi: 10.1046/j.1365-2419.1999.00105.x CrossRefGoogle Scholar
  10. Boero F, Bouillon J, Gravili C, Miglietta MP, Parsons T, Piraino S (2008) Gelatinous plankton: irregularities rule the world (sometimes). Mar Ecol Prog Ser 356:299–310. doi: 10.3354/meps07368 CrossRefGoogle Scholar
  11. Bonicelli J (2008) Distribución espacial, composición específica y abundancia del zooplancton en la costa peruana durante los años 1996 y 1998. Thesis dissertation, Universidad Nacional Agraria La Molina, Lima. PerúGoogle Scholar
  12. Brander KM (1994) Patterns of distribution, spawning, and growth in north Atlantic cod: the utility of inter-regional comparisons. ICES Mar Sci Symp 198:406–413Google Scholar
  13. Brodeur R, Sugisaki DH, Hunt GL Jr (2002) Increases in jellyfish biomass in the Bering Sea: implications for the ecosystem. Mar Ecol Prog Ser 233:89–103CrossRefGoogle Scholar
  14. Brodeur RD, Decker MB, Ciannelli L, Purcell JE, Bond NA, Stabeno PJ, Acuna E, Hunt GL Jr (2008) The rise and fall of jellyfish in the Bering Sea in relation to climate regime shifts. Prog Oceanogr 77:103–111. doi: 10.1016/j.pocean.2008.03.017 CrossRefGoogle Scholar
  15. Brotz L, Cheung WWL, Kleisner K, Pakhomov E, Pauly D (2012) Increasing jellyfish populations: trends in large marine ecosystems. Hydrobiologia 690:3–20. doi: 10.1007/s10750-012-1039-7 CrossRefGoogle Scholar
  16. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information theoretic approach, 2nd edn. Springer, New YorkGoogle Scholar
  17. Cargo DG, King DR (1990) Forecasting the abundance of the sea nettle, Chrysaora quinquecirrha, in the Chesapeake Bay. Estuaries 13:486–491. doi: 10.2307/1351793 CrossRefGoogle Scholar
  18. Carrasco S, Santander H (1987) The El Niño event and its influence on the zooplankton off Peru. J Geophys Res 92:14405–14410. doi: 10.1029/JC092iC13p14405 CrossRefGoogle Scholar
  19. Ceh J, Gonzalez JE, Pacheco AS, Riascos JM (2015) The elusive life cycle of scyphozoan jellyfish: metagenesis revisited. Sci Rep 5:12037. doi: 10.1038/srep12037 CrossRefGoogle Scholar
  20. Chavez FP, Strutton PG, Friederich GE, Feely RA, Feldman GC, Foley DG, McPhaden MJ (1999) Biological and chemical response of the Equatorial Pacific Ocean to the 1997–98 El Niño. Science 286:2126–2131. doi: 10.1126/science.286.5447.2126 CrossRefGoogle Scholar
  21. Chavez FP, Ryan J, Lluch-Cota SE, Niquen M (2003) From anchovies to sardines and back: multidecadal change in the Pacific Ocean. Science 299:217–221. doi: 10.1126/science.1075880 CrossRefGoogle Scholar
  22. Chavez FP, Bertrand A, Guevara-Carrasco R, Soler P, Csirke J (2008) The northern Humboldt current system: brief history, present status and a view towards the future. Prog Oceanogr 79:95–105. doi: 10.1016/j.pocean.2008.10.012 CrossRefGoogle Scholar
  23. Chiaverano LM, Holland BS, Crow GL, Blair L, Yanagihara AA (2013) Long-term fluctuations in circalunar beach aggregations of the box jellyfish Alatina moseri in Hawaii, with links to environmental variability. PLoS One. doi: 10.1371/journal.pone.0077039 CrossRefGoogle Scholar
  24. Condon RH, Graham WM, Duarte CM, Pitt KA, Lucas CH, Haddock SH, Madin LP (2012) Questioning the rise of gelatinous zooplankton in the world’s oceans. Bioscience 62:160–169. doi: 10.1525/bio.2012.62.2.9 CrossRefGoogle Scholar
  25. Condon RH, Duarte CM, Pitt KA, Robinson KL, Lucas CH, Sutherland KR, Mianzan WM, Bogeberg M, Purcell JE, Decker MB, Uye S, Madin LP, Brodeur RD, Haddock SH, 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. doi: 10.1073/pnas.1210920110 CrossRefGoogle Scholar
  26. Cury P, Bakun A, Crawford RJM, Jarre A, Quiñones RA, Shannon JL, Verheye HM (2000) Small pelagics in upwelling systems: patterns of interaction and structural changes in ‘wasp-waist’ ecosystems. ICES J Mar Sci 57:603–618. doi: 10.1006/jmsc.2000.0712 CrossRefGoogle Scholar
  27. Damalas D, Megalofonou P, Apostolopoulou M (2007) Environmental, spatial, temporal and operational effects on swordfish (Xiphias gladius) catch rates of eastern Mediterranean Sea longline fisheries. Fish Res 84:233–246. doi: 10.1016/j.fishres.2006.11.001 CrossRefGoogle Scholar
  28. Daskalov G, Mamedov E (2007) Integrated fisheries assessment and possible causes for the collapse of anchovy kilka in the Caspian Sea. ICES J Mar Sci 64:503–511. doi: 10.1093/icesjms/fsl047 CrossRefGoogle Scholar
  29. Daskalov G, Grishin AN, Rodionov S, Mihneva V (2007) Trophic cascades triggered by overfishing reveal possible mechanisms of ecosystem regime shifts. Proc Natl Acad Sci USA 104:10518–10523. doi: 10.1073/pnas.0701100104 CrossRefGoogle Scholar
  30. Decker MB, Liu H, Ciannelli L, Ladd C, Cheng W, Chan KS (2013) Linking changes in eastern Bering Sea jellyfish populations to environmental factors via nonlinear time series models. Mar Ecol Prog Ser 494:179–189. doi: 10.3354/meps10545 CrossRefGoogle Scholar
  31. Decker MB, Cieciel K, Zavolokin A, Lauth R, Brodeur RD, Coyle KO (2014) Population fluctuations of jellyfish in the Bering Sea and their ecological role in this productive shelf ecosystem. In: Pitt KA, Lucas CH (eds) Jellyfish blooms. Springer, Dordrecht, pp 153–183. doi: 10.1007/978-94-007-7015-7_1 CrossRefGoogle Scholar
  32. Doney SC, Ruckelshaus M, Duffy JE, Barry JP, Chan F, English CA, Galindo HM, Grebmeier JM, Hollowed AB, Knowlton N, Plovina J, Rabalais NN, Sydeman WJ, Talley LD (2012) Climate change impacts on marine ecosystems. Mar Sci 4:11–37. doi: 10.1146/annurev-marine-041911-111611 CrossRefGoogle Scholar
  33. Dong Z, Liu D, Keesing JK (2010) Jellyfish blooms in China: dominant species, causes and consequences. Mar Pollut Bull 60:954–963. doi: 10.1016/j.marpolbul.2010.04.022 CrossRefGoogle Scholar
  34. Duarte CM, Pitt KA, Lucas CH, Purcell JE, Uye S, Robinson K, Brotz L, Decker MB, Sutherland KR, Malej A, Madin L, Mianzan H, Gili JM, Fuentes V, Atienza D, Pagés F, Breitburg D, Malek J, Graham WM, Condon RH (2012) Is global ocean sprawl a cause of jellyfish blooms? Front Ecol Environ 11:91–97. doi: 10.1890/110246 CrossRefGoogle Scholar
  35. Eriksen E, Prozorkevich D, Trofimov A, Howel D (2012) Biomass of scyphozoan jellyfish, and Its spatial association with 0-group fish in the Barents Sea. PLoS One 7:e33050. doi: 10.1371/journal.pone.0033050 CrossRefGoogle Scholar
  36. Flores A, Wiff R, Diaz E (2015) Using the gonadosomatic index to estimate the maturity ogive: application to Chilean hake (Merluccius gayi gayi). ICES J Mar Sci 72:508–514. doi: 10.1093/icesjms/fsu155 CrossRefGoogle Scholar
  37. Flynn BA, Richardson AJ, Brierley AS, Boyer CD, Axelsen BE, Scott L, Moroff NE, Kainge PI, Tjizoo BM, Gibbons MJ (2012) Temporal and spatial patterns in the abundance of jellyfish in the northern Benguela upwelling ecosystem and their link to thwarted pelagic fishery recovery. Afr J Mar Sci 34:131–146. doi: 10.2989/1814232X.2012.675122 CrossRefGoogle Scholar
  38. Gibbons MJ, Richardson AJ (2009) Patterns of pelagic cnidarian abundance in the North Atlantic. Hydrobiologia 616:51–65. doi: 10.1007/s10750-008-9593-8 CrossRefGoogle Scholar
  39. Goy J, Morand P, Etienne M (1989) Long-term fluctuations of Pelagia noctiluca (Cnidaria, Scyphomedusa) in the western Mediterranean Sea. Prediction by climatic variables. Deep Sea Res 36:269–279. doi: 10.1016/0198-0149(89)90138-6 CrossRefGoogle Scholar
  40. Gutierrez D, Bertrand A, Wosnitza-Mendo C, Dewitte B, Purca S, Peña C, Chaigneau A, Tam J, Graco M, Echevin V, Grados C, Freon P, Guevara-Carrasco R (2011) Sensibilidad del sistema de afloramiento costero del Perú al cambio climático e implicancias ecológicas Climate change sensitivity of the Peruvian upwelling system and ecological implications. Revista Peruana Geoatmosférica 3:124. Available via http://www.crh-eme.ird.fr/team/pfreon/PDF/Gutierrez_et_al_2011_Rev_Peruana_Geo-Atmosferica.pdf. Accessed 22 Jan 2014
  41. Hastie T, Tibshirani R (1986) Generalized additive models. Stat Sci 1:297–318. doi: 10.1214/ss/1177013609 CrossRefGoogle Scholar
  42. Holst S (2012) Effects of climate warming on strobilation and ephyra production of North Sea scyphozoan jellyfish. Hydrobiologia 690:127–140. doi: 10.1007/s10750-012-1043-y CrossRefGoogle Scholar
  43. Jaspers C, Møller LF, Kiørboe T (2011) Salinity gradient of the Baltic Sea limits the reproduction and population expansion of the newly invaded comb jelly Mnemiopsis leidyi. PLoS One 6:e24065. doi: 10.1371/journal.pone.0024065 CrossRefGoogle Scholar
  44. Jensen OP, Branch A, Hilborn R (2012) Marine fisheries as ecological experiments. Theor Ecol 5:3–22. doi: 10.1007/s12080-011-0146-9 CrossRefGoogle Scholar
  45. Kamykowski D (2012) 20th century variability of atlantic meridional overturning circulation: planetary wave influences on world ocean surface phosphate utilization and synchrony of small pelagic fisheries. Deep Sea Res Part I 65:85–99. doi: 10.1016/j.dsr.2012.03.005 CrossRefGoogle Scholar
  46. Kogovšek T, Bogunovic B, Malej A (2010) Recurrence of bloom-forming scyphomedusae: wavelet analysis of a 200-year time series. Hydrobiologia 645:81–96. doi: 10.1007/s10750-010-0217-8 CrossRefGoogle Scholar
  47. Lenarz WH, Ventresca DA, Graham WM, Schwing FB, Chavez F (1995) Explorations of El Niño events and associated biological population dynamics off central California. Calif Coop Oceanic Fish Invest Rep 36:106–119Google Scholar
  48. Lo NC, Jacobson LD, Squire JL (1992) Indices of relative abundance from fish spotter data based on delta-lognormal models. Can J Fish Aquat Sci 49:2515–2526. doi: 10.1139/f92-278 CrossRefGoogle Scholar
  49. Lucas CH, Graham WM, Widmer C (2012) Jellyfish life histories: role of polyps in forming and maintaining scyphomedusa populations. Adv Mar Biol 63:133–196. doi: 10.1016/B978-0-12-394282-1.00003-X CrossRefGoogle Scholar
  50. Lynam CP, Brierley AC, Hay SJ (2005) Jellyfish abundance and climate variation: contrasting responses in oceanographically distinct regions of the North Sea, and possible implications for fisheries. J Mar Biol Assoc UK 85:435–450CrossRefGoogle Scholar
  51. Lynam CP, Gibbons MJ, Axelsen BE, Sparks CA, Cotzee J, Heywood BG, Brierley AS (2006) Jellyfish overtake fish in a heavily fished ecosystem. Curr Biol 16:13R492. doi: 10.1016/j.cub.2006.06.018 CrossRefGoogle Scholar
  52. Lynam CP, Attrill JM, Skogen MD (2010) Climatic and oceanic influences on the abundance of gelatinous zooplankton in the North Sea. J Mar Biol Assoc UK 90:1153–1159CrossRefGoogle Scholar
  53. Lynam CP, Lilley MKS, Bastian T, Doyle TK, Beggs SE, Hays GC (2011) Have jellyfish in the Irish Sea benefited from climate change and overfishing? Global Change Biol 17:767–782. doi: 10.1111/j.1365-2486.2010.02352.x CrossRefGoogle Scholar
  54. McPhaden MJ, Lee T, McClurg D (2011) El Niño and its relationship to changing background conditions in the tropical Pacific Ocean. Geophys Res Lett 38:L15709. doi: 10.1029/2011GL048275 CrossRefGoogle Scholar
  55. Mianzan H, Quiñones J, Palma S, Schiariti A, Acha M, Robinson K, Graham WM (2014) Chrysaora plocamia: a poorly understood jellyfish from South American Waters. In: Pitt KA, Lucas CH (eds) Jellyfish blooms. Springer, Dordrecht, pp 219–236. doi: 10.1007/978-94-007-7015-7_1 CrossRefGoogle Scholar
  56. Miller ME, 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. doi: 10.1016/j.jembe.2012.07.015 CrossRefGoogle Scholar
  57. Mitchell JD, Collins KJ, Miller PI, Suberg LA (2014) Quantifying the impact of environmental variables upon catch per unit effort of the blue shark Prionace glauca in the western English Channel. J Fish Biol 1:657–670. doi: 10.1111/jfb.12448 CrossRefGoogle Scholar
  58. Molinero JC, Buecher E, Lučič D, Malej A, Miloslavič M (2009) Climate and Mediteranean jellyfish: assessing the effect of temperature regimes on jellyfish outbreak dynamics. Ann Ser Hist Nat 19:11–18Google Scholar
  59. Montecinos A, Purca S, Pizarro O (2003) Interannual to interdecadal sea surface temperature variability along the western coast of South America. Geophys Res Lett 30:1570. doi: 10.1029/2003GL017345 CrossRefGoogle Scholar
  60. Ochoa N, Rojas de Mendiola B, Gomez O (1985) Identificación del Fenómeno “El Niño” a través de los Organismos Fitoplanctónicos. In: Arntz W, Landa A, Tarazona J (eds) El Niño: Su impacto en la Fauna Marina. Boletín Instituto del Mar del Perú. Volumen Extraordinario, 23–31. Available via http://biblioimarpe.imarpe.gob.pe:8080/bitstream/handle/123456789/1156/BOL%20EXTR.%20EL%20NI%C3%91O-3.pdf?sequence=1. Accessed 01 March 2014
  61. Ochoa N, Taylor MH, Purca S, Ramos E (2010) Intra and interannual variability of nearshore phytoplankton biovolume and community changes in the northern Humboldt Current system. J Plankton Res 32:843–855. doi: 10.1093/plankt/fbq022 CrossRefGoogle Scholar
  62. Pagés F, Gonzalez HE, Ramon M, Sobarzo M, Gili JM (2001) Gelatinous zooplankton assemblages associated with water masses in the Humboldt Current System, and potential predatory impact by Bassia bassensis (Siphonophora: Calycophorae). Mar Ecol Prog Ser 210:13–24. doi: 10.3354/meps210013 CrossRefGoogle Scholar
  63. Parsons TR, Lalli CM (2002) Jellyfish population explosions: revisiting a hypothesis of possible causes. La Mer 40:111–121Google Scholar
  64. Pauly D, Christensen V, Dalsgaard J, Froese R, Torres F (1998) Fishing down marine food webs. Science 279:860–863. doi: 10.1126/science.279.5352.860 CrossRefGoogle Scholar
  65. Pennington JT, Mahoney KL, Kuwahara VS, Kolber DD, Calienes R, Chavez FP (2006) Primary production in the eastern tropical Pacific: a review. Prog Oceanogr 69:285–317. doi: 10.1016/j.pocean.2006.03.012 CrossRefGoogle Scholar
  66. Photopoulou T, Fedak MA, Thomas L, Matthiopoulos J (2014) Spatial variation in maximum dive depth in gray seals in relation to foraging. Mar Mammal Sci 30:923–938. doi: 10.1111/mms.12092 CrossRefGoogle Scholar
  67. Pointin F, Payne MR (2014) A resolution to the blue whiting (Micromesistius poutassou) population paradox? PLoS One 9:e106237. doi: 10.1371/journal.pone.0106237 CrossRefGoogle Scholar
  68. Prieto L, Astorga D, Navarro G, Ruiz J (2010) Environmental control of phase transition and polyp survival of a massive outbreaker jellyfish. PLoS One 5:e13793. doi: 10.1371/journal.pone.0013793 CrossRefGoogle Scholar
  69. Purcell JE (1991) A review of cnidarians and ctenophores feeding on competitors in the plankton. In Coelenterate Biology: recent research on cnidaria and ctenophora. Hydrobiologia 216(217):335–342. doi: 10.1007/978-94-011-3240-4_48 CrossRefGoogle Scholar
  70. Purcell JE (2003) Predation on zooplankton by large jellyfish, Aurelia labiata, Cyanea capillata and Aequorea aequorea, in Prince William Sound, Alaska. Mar Ecol Prog Ser 246:137–152CrossRefGoogle Scholar
  71. Purcell JE (2005) Climate effects on formation of jellyfish and ctenophore blooms: a review. J Mar Biol Assoc UK 85:461–476. doi: 10.1017/S0025315405011409 CrossRefGoogle Scholar
  72. Purcell JE (2007) Environmental effects on asexual reproduction rates of the scyphozoan Aurelia labiata. Mar Ecol Prog Ser 48:183–196. doi: 10.3354/meps07056 CrossRefGoogle Scholar
  73. Purcell JE (2012) Jellyfish and ctenophore blooms coincide with human proliferations and environmental perturbations. Annu Rev Mar Sci 4:209–235. doi: 10.1146/annurev-marine-120709-142751 CrossRefGoogle Scholar
  74. Purcell JE, Arai MN (2001) Interactions of pelagic cnidarians and ctenophores with fish: a review. Hydrobiologia 451:27–44. doi: 10.1007/978-94-011-3240-4_48 CrossRefGoogle Scholar
  75. Purcell JE, Decker MB (2005) Effects of climate on relative predation by scyphomedusae and ctenophores on copepods in Chesapeake Bay during 1987–2000. Limnol Oceanogr 50:376–387. doi: 10.4319/lo.2005.50.1.0376 CrossRefGoogle Scholar
  76. Purcell JE, Malej A, Benović A (1999a) Potential links of jellyfish to eutrophication and fisheries. In: Ecosystems at the land-sea margin: drainage basin to coastal sea. In: Malone TC, Malej A, Harding Jr. LW, Smodlaka N, Turner RE (eds). Coast Estuar Stud 55:241–263. doi: 10.1029/CE055p0241 CrossRefGoogle Scholar
  77. Purcell JE, White JR, Nemazie DA, Wright DA (1999b) Temperature, salinity and food effects on asexual reproduction and abundance of the scyphozoan Chrysaora quinquecirrha. Mar Ecol Prog Ser 180:187–196CrossRefGoogle Scholar
  78. Purcell JE, Uye S, Lo WT (2007) Anthropogenic causes of jellyfish blooms and direct consequences for humans: a review. Mar Ecol Prog Ser 350:153–174. doi: 10.3354/meps07093 CrossRefGoogle Scholar
  79. Purcell JE, Hoover RA, Schwarck NT (2009) Interannual variation of strobilation by the scyphozoan Aurelia labiata in relation to polyp density, temperature, salinity, and light conditions in situ. Mar Ecol Prog Ser 375:139–149. doi: 10.3354/meps07785 CrossRefGoogle Scholar
  80. Quiñones J (2008) Chrysaora plocamia Lesson, 1830 (Cnidaria, Scyphozoa), frente a Pisco, Perú. Informe Instituto del Mar del Perú, 35:221-230. Available via http://biblioimarpe.imarpe.gob.pe:8080/bitstream/handle/123456789/1972/INF.%2035%283%29-6.pdf?sequence=1. Accessed 17 Jan 2014
  81. Quiñones J, Carman VG, Zeballos J, Purca S, Mianzan H (2010) Effects of El Niño-driven environmental variability on black turtle migration to Peruvian foraging grounds. Hydrobiologia 645:69–79. doi: 10.1007/s10750-010-0225-8 CrossRefGoogle Scholar
  82. R Development Core Team. R (2009) A language and environment for statistical computing. Vienna, Austria. Available via: http://cran.r-project.org. Accessed 02 Feb 2014
  83. Reid PC, Battle EJV, Batten SD, Brander KM (2000) Impacts of fisheries on plankton community structure. ICES J Mar Sci 57:495–502. doi: 10.1006/jmsc.2000.0740 CrossRefGoogle Scholar
  84. Riascos JM, Paredes L, Gonzales K, Caceres I, Pacheco AS (2013) The larval and benthic stages of the scyphozoan medusa Chrysaora plocamia under El Niño–La Niña thermal regimes. J Exp Mar Biol Ecol 446:95–101. doi: 10.1016/j.jembe.2013.05.006 CrossRefGoogle Scholar
  85. Riascos JM, Villegas V, Pacheco AS (2014) Diet composition of the large scyphozoan jellyfish Chrysaora plocamia in a highly productive upwelling centre off northern Chile. Mar Biol Res 10:791–798. doi: 10.1080/17451000.2013.863353 CrossRefGoogle Scholar
  86. Richardson AJ, Bakun A, Hay JC, Gibbons MJ (2009) The jellyfish joyride: causes, consequences and management responses to a more gelatinous future. Trends Ecol Evol 24:312–322. doi: 10.1016/j.tree.2009.01.010 CrossRefGoogle Scholar
  87. Robinson KL, Graham WM (2013) Long-term change in the abundances of northern Gulf of Mexico scyphomedusae Chrysaora sp. and Aurelia sp. with links to climate variability. Limnol Oceanogr 58:235–253. doi: 10.4319/lo.2013.58.1.0235 CrossRefGoogle Scholar
  88. Robinson KL, Graham WM (2014) Warming of subtropical coastal waters accelerates Mnemiopsis leidyi growth and alters timing of spring ctenophore blooms. Mar Ecol Prog Ser 502:105–115. doi: 10.3354/meps10739 CrossRefGoogle Scholar
  89. Robinson KL, Ruzicka JJ, Decker MB, Brodeur RD, Hernandez FJ, Quiñones J, Acha EM, Uye S, Mianzan H, Graham WM (2014) Jellyfish, forage fish, and the world’s major fisheries. Oceanography 27:104–115. doi: 10.5670/oceanog.2014.90 CrossRefGoogle Scholar
  90. Roux JP, Van der Lingen CD, Gibbons MJ, Moroff NE, Shannon LJ, Smith AD, Cury PM (2013) Jellyfication of marine ecosystems as a likely consequence of overfishing small pelagic fishes: lessons from the Benguela. Bull Mar Sci 89:249–284. doi: 10.5343/bms.2011.1145 CrossRefGoogle Scholar
  91. Sánchez S (2000) Variación estacional e interanual de la biomasa fitoplanctónica y concentraciones de clorofila A, frente a la costa peruana durante 1976–2000. Boletín Instituto del Mar del Perú 19:29–44. Available via http://biblioimarpe.imarpe.gob.pe:8080/bitstream/handle/123456789/995/BOL%2019%281-2%29-5.pdf?sequence=1. Accessed 04 February 2014
  92. Santander H, Carrasco S (1985) Cambios en el zooplancton durante El Niño 1982–1983 en el área de Chimbote. In: del Anales I (ed) Aguilar AET. Congreso Nacional de Biología Pesquera, Trujillo, pp 201–206Google Scholar
  93. Segurado P, Araújo MB, Kunin WE (2006) Consequences of spatial autocorrelation for niche-based models. J Appl Ecol 43:433–444. doi: 10.1111/j.1365-2664.2006.01162.x CrossRefGoogle Scholar
  94. Smith TM, Reynolds RW, Peterson CT, Lawrimore J (2008) Improvements to NOAA’s historical merged land-ocean surface temperature analysis (1880–2006). J Clim 21:2283–2296. doi: 10.1175/2007JCLI2100.1 CrossRefGoogle Scholar
  95. Stenseth NC, Mysterud A (2002) Climate, changing phenology, and other life history traits: nonlinearity and match–mismatch to environment. Proc Natl Acad Sci USA 99:13379–13381. doi: 10.1073/pnas.212519399 CrossRefGoogle Scholar
  96. Suchman CL, Daly EA, Keister JE, Peterson WT, Brodeur RD (2008) Feeding patterns and predation potential of scyphomedusae in a highly productive upwelling region. Mar Ecol Prog Ser 358:161–172. doi: 10.3354/meps07313 CrossRefGoogle Scholar
  97. Suchman CL, Brodeur RD, Emmett RL, Daly EA (2012) Large medusae in surface waters of the Northern California current: variability in relation to environmental conditions. Hydrobiologia 690:113–125. doi: 10.1007/s10750-012-1055-7 CrossRefGoogle Scholar
  98. Tarazona J, Arntz W, Canahuire E, Ayala Z, Robles A (1985) Modificaciones producidas durante “El Niño” en la infauna bentónica de áreas someras del ecosistema de afloramiento peruano. In: Arntz W, Landa A, Tarazona J (eds) El Niño: Su impacto en la fauna marina. Boletín Instituto del Mar del Perú. Volumen Extraordinario, 55–63. Available via http://biblioimarpe.imarpe.gob.pe:8080/bitstream/handle/123456789/1166/BOL%20EXTR.%20EL%20NI%C3%91O-7.pdf?sequence=1. Accessed 20 June 2014
  99. Tarazona J, Arntz W, Valle S, Peña T (2001) Los índices de la variabilidad de El Niño y del impacto sobre las comunidades bentónicas. In: Tarazona J, Arntz W, Castillo de Maruenda E (eds) El Niño en América Latina: impactos biológicos y sociales. Consejo Nacional de Ciencia y Tecnología, Editorial Omega, Lima, pp 113–125Google Scholar
  100. Utne-Palm AC, Salvanes AGV, Currie B, Kaartvedt S, Nilsson GE, Braithwaite VA, Stecyk JAW, Hundt M, Van der Bank M, Flynn B et al (2010) Trophic structure and community stability in an overfished ecosystem. Science 329:333–336. doi: 10.1126/science.1190708 CrossRefGoogle Scholar
  101. Uye S (2014) The giant jellyfish Nemopilema nomurai in East Asian marginal seas. In: Pitt KA, Lucas CH (eds) Jellyfish Blooms. Springer, Dordrecht, pp 185–205. doi: 10.1007/978-94-007-7015-7_1 CrossRefGoogle Scholar
  102. Venables WN, Dichmont CM (2004) GLMs, GAMs and GLMMs: an overview of theory for applications in fisheries research. Fish Res 70:319–337. doi: 10.1016/j.fishres.2004.08.011 CrossRefGoogle Scholar
  103. West JW, Pitt KA, Welsh DT, Koop K, Rissik D (2009) Top-down and bottom-up influences of jellyfish on primary productivity and planktonic assemblages. Limnol Oceanogr 54:2058–2071. doi: 10.4319/lo.2009.54.6.2058 CrossRefGoogle Scholar
  104. Wood S (2006) Generalized additive models: an introduction with R. Biometrics 62:392. doi: 10.1111/j.1541-0420.2006.00574.x CrossRefGoogle Scholar
  105. Wood SN, Augustin NH (2002) GAMs with integrated model selection using penalized regression splines and applications to environmental modelling. Ecol Modell 157:157–177. doi: 10.1016/S0304-3800(02)00193-X CrossRefGoogle Scholar
  106. Worm B, Barbier EB, Beaumont N, Duffy JE, Folke C, Halpern BS, Jackson JBC, Lotze HK, Micheli F, Palumbi SR, Sala E, Selkoe KA, Stachowicz JJ, Watson R (2006) Impacts of biodiversity loss on ocean ecosystem services. Science 314:787–790. doi: 10.1126/science.1132294 CrossRefGoogle Scholar
  107. Zuta S, Urquizo W, Rivera T, Maldonado M (1976) Informe de la exploración con bolicheras para el control costero de “El Niño” en Febrero 1976 (EBCCEN 1– 1976), Serie de Informes Especiales, Instituto del Mar del Perú, pp 1–10. Available via: http://biblioimarpe.imarpe.gob.pe:8080/bitstream/handle/123456789/1639/INF%20ESP.%20181.pdf?sequence=1. Accessed 10 Feb 2014

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Javier Quiñones
    • 1
  • Hermes Mianzan
    • 3
    • 4
  • Sara Purca
    • 2
  • Kelly L. Robinson
    • 5
  • Grant D. Adams
    • 6
  • E. Marcelo Acha
    • 3
    • 4
  1. 1.Laboratorio Costero de PiscoInstituto del Mar del Perú IMARPEParacas, IcaPeru
  2. 2.Area de Investigaciones Marino Costeras (AFIMC)Instituto del Mar del Perú IMARPECallaoPeru
  3. 3.Instituto Nacional de Investigación y Desarrollo Pesquero INIDEPMar del PlataArgentina
  4. 4.Instituto de Investigaciones Marinas y Costeras (UNMdP-CONICET)Mar del PlataArgentina
  5. 5.Hatfield Marine Science CenterOregon State UniversityNewportUSA
  6. 6.Gulf Coast Research LaboratoryUniversity of Southern MississippiOcean SpringsUSA

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