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Symbiotic associations between crustaceans and gelatinous zooplankton in deep and surface waters off California

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Abstract

Using a remotely operated submersible (ROV) in the sea off Monterey, California, we collected deep-living zooplankton and observed their associations with crustacean symbionts. Little is known about the nature of these symbioses. Among the most interesting findings was the description of a previously unknown modality of symbiosis of the deep-living copepod Pseudolubbockia dilatata Sars. It was recorded within the subumbrellar cavity of three specimens of the bathypelagic hydromedusa Aegina citrea Eschscholtz at depths of 606–1,098 m. One of these medusae hosted a mating pair of adult copepods along with the remains of their molts corresponding to copepodid stages CV of the female and CII, CIII, CIV, and CV of the male; another medusa had an adult female, and molts of a female CV and of male CIII, CIV and CV copepodids. Our data indicate that the medusae were occupied first by an early male copepodid, and then the female joined as a CV. The presence of an adult female alone with its CV molt in a third medusa suggests that females invade the host regardless of the presence of the male in it. The medusa represents a protected environment for these copepods during vulnerable stages or processes (molting and mating). We also observed 13 new associations between hyperiid amphipods and gelatinous zooplankton at different depths. These involve four new records among members of the Infraorder Physosomata, for which only six other associations were known, and five species of amphipods and six hosts among the gelatinous zooplankton not previously recorded as symbionts. Data are provided on three families of Hyperiidea for which symbiotic associations were hitherto unknown. The ROV represents a valuable tool for the observation and sampling of these associations, whose existence has been known for a long time, but which are still poorly understood.

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References

  • Boxshall GA (1990) Precopulatory mate guarding in copepods. Bijdr Dierkd 60:209–213

    Google Scholar 

  • Boxshall GA, Halsey SH (2004) An introduction to copepod diversity, vol. 166. The Ray Society, London

    Google Scholar 

  • 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

    Article  Google Scholar 

  • De Lima M, Valentin JL (2001) New records of Amphipoda Hyperiidea in associations with gelatinous zooplankton. Hydrobiologia 448:229–235

    Article  Google Scholar 

  • Gasca R, Haddock SHD (2004) Associations between gelatinous zooplankton and hyperiid amphipods (Crustacea: Peracarida) in the Gulf of California. Hydrobiologia 530/531:529–535

    Article  Google Scholar 

  • Gardner GA, Szabo I (1982) British Columbia pelagic marine Copepoda: an identification manual and annotated bibliography. Can Spec Publ Fish Aquat Sci 62:1–536

    Google Scholar 

  • Go YB, Oh B-C, Terazaki M (1998) Feeding behavior of the poecilostomatoid copepods Oncaea spp. on chaetognaths. J Mar Syst 15:475–482

    Article  Google Scholar 

  • Haddock, SHD, Heine, JN (2005) Scientific blue-water diving. California Sea Grant, La Jolla, CA

  • Harbison GR, Bigs DC, Madin LP (1977) The associations of Amphipoda Hyperiidea with gelatinous zooplankton-II. Associations with Cnidaria, Ctenophora and Radiolaria. Deep Sea Res 24:465–468

    Article  Google Scholar 

  • Hay ME, Parker JD, Burkepile DE, Caudill CC, Wilson AE, Hallinan ZP, Chequer AD (2004) Mutualisms and aquatic community structure: the enemy of my enemy is my friend. Annu Rev Ecol Syst 35:175–197

    Article  Google Scholar 

  • Heron GA, Damkaer DM (1969) Five species of deep-water cyclopoid copepods from the plankton of the Gulf of Alaska. Smithson Contrib Zool 20:1–24

    Article  Google Scholar 

  • Heron GA, Damkaer DM (1978) Seven Lubbockia species (Copepoda: Cyclopoida) from the plankton of the Northeast Pacific, with a Review of the Genus. Smithson Contrib Zool 267:1–36

    Article  Google Scholar 

  • Heron GA, Bradford-Grieve JM (1995) The marine fauna of New Zealand: pelagic Copepoda: Poecilostomatoida: Oncaeidae. NZOI Mem 104:5–57

    Google Scholar 

  • Humes AG (1953) Two new semiparasitic harpacticoid copepods from the coast of New Hampshire. J Wash Acad Sci 37(5):170–178

    Google Scholar 

  • Humes AG (1969) A cyclopoid copepod, Sewellochiron fidens n. gen., n. sp. associated with a medusa in Puerto Rico. Beaufortia 16(219):171–183

    Google Scholar 

  • Humes AG (1985) Cnidarians and copepods: a success story. Trans Am Microsc Soc 104:313–320

    Article  Google Scholar 

  • Huys R, Böttger-Schnack R (1997) On the diphyletic origin of the Oncaeidae Giesbrecht, 1892 (Copepoda: Poecilostomatoida) with a phylogenetic analysis of the Lubbockiidae fam. nov. Zool Anz 235:243–261

    Google Scholar 

  • Izawa K (1991) Evolutionary reduction of body segments in the poecilostome Cyclopoida (Crustacea: Copepoda). Bull Plankton Soc Jpn (Spec Vol):71–86

  • Kramp PL (1965) The Hydromedusae of the Pacific and Indian Oceans. Dana Rep 63:1–162

    Google Scholar 

  • Laval P (1980) Hyperiid amphipods as crustacean parasitoids associated with gelatinous zooplankton. Oceanogr Mar Biol Annu Rev 18:11–56

    Google Scholar 

  • Lonsdale DJ, Frey MA, Snell TW (1997) The role of chemical signals in copepod reproduction. J Mar Syst 15:1–12

    Article  Google Scholar 

  • Madin LP, Harbison GR (1977) The associations of Amphipoda Hyperiidea with gelatinous zooplankton-I. Associations with Salpidae. Deep Sea Res 24:449–463

    Article  Google Scholar 

  • Mayer AG (1910) Medusae of the World, Vol I. The Hydromedusae. Carnegie Institution of Washington, Washington

  • Razouls C (1996) Diversité et répartition géographique chez les copépodes pélagiques. 2-Platycopioida, Misophrioida, Mormonilloida, Cyclopoida, Poecilostomatoida, Siphonostomatoida, Harpacticoida, Monstrilloida. Ann Inst Oceanogr Paris Nouv Ser 72:1–149

    Google Scholar 

  • Reddiah K (1968) Three new species of Paramacrochiron (Lichomolgidae) associated with medusae. Crustaceana (Suppl 1):193–209

  • Reddiah K (1969) Pseudomacrochiron stocki n.g., n.sp., a cyclopoid copepod associated with a medusa. Crustaceana 16:43–50

    Article  Google Scholar 

  • Robison BH (2004) Deep pelagic biology. J Exp Mar Biol Ecol 300:253–272

    Article  Google Scholar 

  • Sars GO (1909) Note préliminaire sur trois formes remarquables de Copépodes, provenant des Campaignes de S.A.S. le Prince Albert de Monaco. Bull Inst Oceanogr 147:1–8

    Google Scholar 

  • Shih C-t, Chen Q-c (1995) Zooplankton of China Seas (2). The Hyperiidea (Crustacea: Amphipoda). China Ocean Press, Beijing

    Google Scholar 

  • Thurston MH (1977) Depth distribution of Hyperia spinigera Bovallius, 1889 (Crustacea: Amphipoda) and medusae in the North Atlantic Ocean, with notes on the association between Hyperia and coelenterates. In: Angel M (ed) A voyage of discovery. Pergamon, Oxford, pp 499–536

    Google Scholar 

  • Van Duren LA, Videler JJ (1996) The trade-off between feeding, mate seeking and predator avoidance in copepods: behavioural responses to chemical cues. J Plankton Res 18:805–818

    Article  Google Scholar 

  • Vinogradov G (1999) Amphipoda. In: Boltovskoy D (ed) South Atlantic zooplankton. Backhuys Publishers, Leiden, pp 1141–1240

    Google Scholar 

  • Vinogradov ME, Volkov AF, Semenova TN (1996) Hyperiid amphipods (Amphipoda, Hyperiidea) of the world oceans. Science Publ Inc., Lebanon

    Google Scholar 

  • Wrobel D, Mills C (1998) Pacific coast pelagic invertebrates. A guide to the common gelatinous animals. Sea Challengers, Monterey

    Google Scholar 

Download references

Acknowledgments

We thank the crews of the ROV “Tiburon” and “Western Flyer” and also Bruce Robison (MBARI) for assistance in obtaining specimens. Rosa María Hernández-Flores deposited the specimens in the collection of zooplankton of El Colegio de la Frontera Sur, Mexico. Claudia Mills, Friday Harbor Laboratories, University of Washington, kindly provided information about the specimens of the medusa Neoturris. Edgar Tovar helped in the identification of L. zacae.

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Correspondence to Rebeca Gasca.

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Communicated by P.W. Sammarco, Chauvin.

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Gasca, R., Suárez-Morales, E. & Haddock, S.H.D. Symbiotic associations between crustaceans and gelatinous zooplankton in deep and surface waters off California. Mar Biol 151, 233–242 (2007). https://doi.org/10.1007/s00227-006-0478-y

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