Marine Biology

, Volume 162, Issue 9, pp 1841–1848 | Cite as

Trophic relationships between the large scyphomedusa Chrysaora plocamia and the parasitic amphipod Hyperia curticephala

  • José M. RiascosEmail author
  • Felipe Docmac
  • Carl Reddin
  • Chris Harrod
Original Paper


Scyphozoan jellyfish develop dramatic population blooms, which may significantly alter marine food webs. In turn, hyperiid amphipods parasitising jellyfish can occur in such great numbers that they represent an important trophic link to diverse species of fish, and may contribute to the decline of their host populations. Therefore, there is an urgent need to assess the trophic function and energy transfer through jellyfish and their parasites. We studied the isotopic composition (i.e. δ13C and δ15N) of Chrysaora plocamia, the largest and most abundant scyphozoan jellyfish in the Humboldt Current System of Chile and Peru, and of its associated hyperiid parasite Hyperia curticephala. The isotopic composition of C. plocamia changed with body size, suggesting that that the diet of this species may include both pelagic and benthic prey as a consequence of the vertical distribution patterns observed. Although the density and intensity of infection of the parasite H. curticephala changed with the size of the host, their isotopic composition showed little variation, suggesting no shifts in the use of resources by the parasite. In contrast to other hyperiid parasites, reported to shift to a benthic mode of life when their hosts are lacking or in low abundance, the isotopic composition of H. curticephala revealed that their food source is mainly pelagic.


Isotopic Composition Macroalgae Particulate Organic Matter Infection Intensity Gonad Tissue 
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.



JMR was funded through the CONICYT Grant 11100256; CH, FD and CR were funded through CONICYT Grant PAI MEL 81105006.

Supplementary material

227_2015_2716_MOESM1_ESM.docx (177 kb)
Supplementary material 1 (DOCX 176 kb)


  1. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  2. Carabel S, Godínez-Domínguez E, Verísimo P, Fernández L, Freire J (2006) An assessment of sample processing methods for stable isotope analyses of marine food webs. J Exp Mar Biol Ecol 336:254–261CrossRefGoogle Scholar
  3. 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
  4. 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 79:95–105CrossRefGoogle Scholar
  5. Condon RH, Steinberg DK, del Giorgio PA, Bouvier TC, Bronk DA, Graham WM, Ducklow HW (2011) Jellyfish blooms result in a major microbial respiratory sink of carbon in marine systems. Proc Nat Acad Sci 108:10225–10230CrossRefGoogle Scholar
  6. Condon RH, Duarte CM, Pitt KA, Robinson KL, Lucas CH, Sutherland KR, Mianzan HW, Bogeberg M, Purcell JE, Decker MB, S-i Uye, Madin LP, Brodeur RD, Haddock SHD, 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 Nat Acad Sci 110:1000–1005CrossRefGoogle Scholar
  7. D’Ambra I, Graham WM, Carmichael RH, Hernandez FJ Jr (2015) Fish rely on scyphozoan hosts as a primary food source: evidence from stable isotope analysis. Mar Biol 162:247–252CrossRefGoogle Scholar
  8. Dittrich B (1988) Studies on the life cycle and reproduction of the parasitic amphipod Hyperia galba in the North Sea. Helgol Mar Res 42:79–98Google Scholar
  9. Doyle TK, Hays GC, Harrod C, Houghton JDR (2014) Ecological and societal benefits of jellyfish. In: Lucas CH, Pitt KA (eds) Jellyfish blooms. Springer, GermanyGoogle Scholar
  10. Fleming N, Houghton J, Magill C, Harrod C (2011) Preservation methods alter stable isotope values in gelatinous zooplankton: implications for interpreting trophic ecology. Mar Biol 158:2141–2146CrossRefGoogle Scholar
  11. Fleming NEC, Harrod C, Griffin DC, Newton J, Houghton JDR (2014) Jellyfish provide short-term reproductive habitat for hyperiid amphipods in a temperate near-shore environments. Mar Ecol Prog Ser 510:229–240CrossRefGoogle Scholar
  12. France R (1995) Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications. Mar Ecol Prog Ser 124:307–312CrossRefGoogle Scholar
  13. Hamner WM, Dawson MN (2009) A review and synthesis on the systematics and evolution of jellyfish blooms: advantageous aggregations and adaptive assemblages. In: Pitt KA, Purcell JE (eds) Jellyfish blooms: causes, consequences, and recent advances. Springer, Netherlands, pp 161–191Google Scholar
  14. Hays GC, Bastian T, Doyle TK, Fossette S, Gleiss AC, Gravenor MB, Hobson VJ, Humphries NE, Lilley MKS, Pade NG, Sims DW (2012) High activity and Levy searches: jellyfish can search the water column like fish. Proc R Soc Ser B Lon 279:465–473CrossRefGoogle Scholar
  15. Iyengar EV (2008) Kleptoparasitic interactions throughout the animal kingdom and a re-evaluation, based on participant mobility, of the conditions promoting the evolution of kleptoparasitism. Biol J Linnean Soc 93:745–762CrossRefGoogle Scholar
  16. Laval P (1980) Hyperiid amphipods as crustacean parasitoids associated with gelatinous zooplankton. Oceanogr Mar Biol Ann Rev 18:11–56Google Scholar
  17. Lynam CP, Gibbons MJ, Axelsen BE, Sparks CA, Coetzee J, Heywood BG, Brierley AS (2006) Jellyfish overtake fish in a heavily fished ecosystem. Curr Biol 16:R492–R493CrossRefGoogle Scholar
  18. Mallela J, Harrod C (2008) δ13C and δ15N reveal significant differences in the coastal foodwebs of the seas surrounding Trinidad and Tobago. Mar Ecol Progr Ser 368:41–51CrossRefGoogle Scholar
  19. McCutchan JH, Lewis WM, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–390CrossRefGoogle Scholar
  20. Mianzan H, Quiñones J, Palma S, Schiariti A, Acha EM, Robinson KL, Graham WM (2014) Chrysaora plocamia: a poorly understood jellyfish from South American waters. In: Pitt KA, Lucas CH (eds) Jellyfish blooms. Springer, Netherlands, pp. 219–236CrossRefGoogle Scholar
  21. Milisenda G, Rosa S, Fuentes VL, Boero F, Guglielmo L, Purcell JE, Piraino S (2014) Jellyfish as prey: frequency of predation and selective foraging of Boops boops (Vertebrata, Actinopterygii) on the mauve stinger Pelagia noctiluca (Cnidaria, Scyphozoa). PLoS ONE 9:e94600CrossRefGoogle Scholar
  22. Mills CE (1993) Natural mortality in NE Pacific coastal hydromedusae: grazing predation, wound healing and senescence. Bull Mar Sci 53:194–203Google Scholar
  23. Montecino V, Lange CB (2009) The Humboldt Current System: ecosystem components and processes, fisheries, and sediment studies. Progr Oceanogr 83:65–79CrossRefGoogle Scholar
  24. Morandini AC, Da Silveira FL, Jarms G (2004) The life cycle of Chrysaora lactea Eschscholtz, 1829 (Cnidaria, Scyphozoa) with notes on the scyphistoma stage of three other species. Hydrobiologia 530:347–354CrossRefGoogle Scholar
  25. Ng JSS, Wai T-C, Williams GA (2007) The effects of acidification on the stable isotope signatures of marine algae and molluscs. Mar Chem 103:97–102CrossRefGoogle Scholar
  26. Ohtsuka S, Koike K, Lindsay D, Nishikawa J, Miyake H, Kawahara M, Mujiono N, Hiromi J, Komatsu H (2009) Symbionts of marine medusae and ctenophores. Plankton Benthos Res 4:1–13CrossRefGoogle Scholar
  27. Oliva ME, Maffet A, Laudien J (2010) Asociación entre Chrysaora plocamia (Cnidaria, Scyphozoa) e Hyperia curticephala (Peracarida: Amphipoda) en Bahía de Mejillones, norte de Chile. Rev Biol Mar Oceanogr 45:127–130CrossRefGoogle Scholar
  28. Pagès F, González HE, Ramón 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 210:13–24CrossRefGoogle Scholar
  29. Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS ONE 5:e9672CrossRefGoogle Scholar
  30. Pauly D, Graham W, Libralato S, Morissette L, Palomares MLD (2009) Jellyfish in ecosystems, online databases and ecosystem models. Hydrobiologia 616:67–85CrossRefGoogle Scholar
  31. Pitt KA, Clement AL, Connolly RM, Thibault-Botha D (2008) Predation by jellyfish on large and emergent zooplankton: implications for benthic–pelagic coupling. Estuar Coast Shelf Sci 76:827–833CrossRefGoogle Scholar
  32. Pitt KA, Budarf AC, Browne JG, Condon RH (2014) Bloom and bust: why do blooms of jellyfish collapse? In: Pitt KA, Lucas CH (eds) Jellyfish blooms. Springer, Netherlands, pp. 79–103CrossRefGoogle Scholar
  33. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718CrossRefGoogle Scholar
  34. R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  35. Reddin CJ, Docmac FM, O’Connor NE, Bothwell JH, Harrod C (2015) Coastal upwelling drives intertidal community composition and trophic ecology. PloS ONE 10(7):e0130789. doi: 10.1371/journal.pone.0130789 CrossRefGoogle Scholar
  36. Riascos JM, Vergara M, Fajardo J, Villegas V, Pacheco AS (2012) The role of hyperiid parasites as a trophic link between jellyfish and fishes. J Fish Biol 81:1686–1695CrossRefGoogle Scholar
  37. Riascos JM, Villegas V, Cáceres I, Gonzalez JE, Pacheco AS (2013) Patterns of a novel association between the scyphomedusa Chrysaora plocamia and the parasitic anemone Peachia chilensis. J Mar Biol Assoc UK 93:919–923CrossRefGoogle Scholar
  38. 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 10:791–798CrossRefGoogle Scholar
  39. Richardson AJ, Bakun A, Hays GC, Gibbons MJ (2009) The jellyfish joyride: causes, consequences and management responses to a more gelatinous future. Trends Ecol Evol 24:312–322CrossRefGoogle Scholar
  40. Thiel M, Macaya E, Acuña E, Arntz W, Bastias H, Brokordt K, Camus P, Castilla J, Castro L, Cortés M, Dumont C, Escribano R, Fernández M, Gajardo J, Gaymer C, Gomez I, González A, González H, Haye P, Illanes J, Iriarte J, Lancellotti D, Luna-Jorquera G, Luxoro C, Manríquez P, Marín V, Muñoz P, Navarrete S, Perez E, Poulin E, Sellanes J, Sepúlveda H, Stotz W, Tala F, Thomas A, Vargas C, Vasquez J, Alonso-Vega J (2007) The Humboldt Current System of Northern and Central Chile—oceanographic processes, ecological interactions and socioeconomic feedback. Oceanogr Mar Biol Ann Rev 45:195–344Google Scholar
  41. Towanda T, Thuesen EV (2006) Ectosymbiotic behavior of Cancer gracilis and its trophic relationships with its host Phacellophora camtschatica and the parasitoid Hyperia medusarum. Mar Ecol Progr Ser 315:221–236CrossRefGoogle Scholar
  42. Trexler JC, Travis J (1993) Nontraditional regression analyses. Ecology 74:1629–1637CrossRefGoogle Scholar
  43. Verity PG, Smetacek V (1996) Organism life cycles, predation, and the structure of marine pelagic ecosystems. Mar Ecol Progr Ser 130:277–293CrossRefGoogle Scholar
  44. Vinogradov ME, Volkov AF, Semenova TN (1996) Hyperiid amphipods (Amphipoda, Hyperiidea) of the World Oceans. Science Publishers Inc, EnfieldCrossRefGoogle Scholar
  45. Weimerskirch H, Bertrand S, Silva J, Bost C, Peraltilla S (2012) Foraging in Guanay cormorant and Peruvian booby, the major guano-producing seabirds in the Humboldt Current System. Mar Ecol Progr Ser 458:231–245CrossRefGoogle Scholar
  46. West JB, Bowen GJ, Cerling TE, Ehleringer JR (2006) Stable isotopes as one of nature’s ecological recorders. Trends Ecol Evol 21:408–414CrossRefGoogle Scholar
  47. Zeballos J, Arones I, Cabrera A, Galindo O, Lorenzo A, Quiñones J, Zavala J, Flores D, Carbajo L (2008) Informe de las actividades desarrolladas durante el año 2007. Instituto del Mar del Perú, Laboratorio Costero de Pisco, PerúGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • José M. Riascos
    • 1
    Email author
  • Felipe Docmac
    • 2
  • Carl Reddin
    • 3
  • Chris Harrod
    • 2
  1. 1.Climate Change Ecology Group, CENSOR Laboratory, Instituto de Ciencias Naturales Alexander von HumboldtUniversidad de AntofagastaAntofagastaChile
  2. 2.Fish and Stable Isotope Ecology Laboratory, Instituto de Ciencias Naturales Alexander von HumboldtUniversidad de AntofagastaAntofagastaChile
  3. 3.School of Biological SciencesQueen’s UniversityBelfastUK

Personalised recommendations