Skip to main content

Advertisement

SpringerLink
Log in

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

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • 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

    Article  Google Scholar 

  • Arai MN (2005) Predation on pelagic coelenterates: a review. J Mar Biol Assoc UK 85:523–536. doi:10.1017/S0025315405011458

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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. Perú

  • Brander KM (1994) Patterns of distribution, spawning, and growth in north Atlantic cod: the utility of inter-regional comparisons. ICES Mar Sci Symp 198:406–413

    Google Scholar 

  • Brodeur R, Sugisaki DH, Hunt GL Jr (2002) Increases in jellyfish biomass in the Bering Sea: implications for the ecosystem. Mar Ecol Prog Ser 233:89–103

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

  • Hastie T, Tibshirani R (1986) Generalized additive models. Stat Sci 1:297–318. doi:10.1214/ss/1177013609

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Jensen OP, Branch A, Hilborn R (2012) Marine fisheries as ecological experiments. Theor Ecol 5:3–22. doi:10.1007/s12080-011-0146-9

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 36:106–119

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 85:435–450

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 90:1153–1159

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 19:11–18

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Parsons TR, Lalli CM (2002) Jellyfish population explosions: revisiting a hypothesis of possible causes. La Mer 40:111–121

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 246:137–152

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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 180:187–196

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

  • 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

    Article  Google Scholar 

  • 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

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

  • 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 201–206

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

  • 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 113–125

  • 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

    Article  CAS  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Wood S (2006) Generalized additive models: an introduction with R. Biometrics 62:392. doi:10.1111/j.1541-0420.2006.00574.x

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

Download references

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.

Author information

Authors and Affiliations

  1. Laboratorio Costero de Pisco, Instituto del Mar del Perú IMARPE, Av. Los Libertadores A-12, Urb. El Golf, Paracas, Ica, Peru

    Javier Quiñones

  2. Area de Investigaciones Marino Costeras (AFIMC), Instituto del Mar del Perú IMARPE, Esquina Gamarra y General Valle S/N Chucuito, Callao, Peru

    Sara Purca

  3. Instituto Nacional de Investigación y Desarrollo Pesquero INIDEP, Paseo Victoria Ocampo N°1, B7602HSA, Mar del Plata, Argentina

    Hermes Mianzan & E. Marcelo Acha

  4. Instituto de Investigaciones Marinas y Costeras (UNMdP-CONICET), Mar del Plata, Argentina

    Hermes Mianzan & E. Marcelo Acha

  5. Hatfield Marine Science Center, Oregon State University, Newport, OR, USA

    Kelly L. Robinson

  6. Gulf Coast Research Laboratory, University of Southern Mississippi, Ocean Springs, MS, USA

    Grant D. Adams

Authors
  1. Javier Quiñones
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hermes Mianzan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sara Purca
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kelly L. Robinson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Grant D. Adams
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. E. Marcelo Acha
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Javier Quiñones.

Ethics declarations

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.

Additional information

Responsible Editor: J. Purcell.

Hermes Mianzan: Deceased.

Reviewed by undisclosed experts.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 156 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Quiñones, J., Mianzan, H., Purca, S. et al. Climate-driven population size fluctuations of jellyfish (Chrysaora plocamia) off Peru. Mar Biol 162, 2339–2350 (2015). https://doi.org/10.1007/s00227-015-2751-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-015-2751-4

Keywords

Search

Navigation