Advertisement

A survival pack for escaping predation in the open ocean: amphipod – pteropod associations in the Southern Ocean

  • Charlotte Havermans
  • Wilhelm Hagen
  • Wolfgang Zeidler
  • Christoph Held
  • Holger Auel
Original Paper

Abstract

Hyperiidean amphipods are a major prey for fish and seabirds. In the Southern Ocean, they are particularly abundant, with distributions ranging from the Polar Frontal Zone to Antarctic shelf waters. The species Hyperiella dilatata has previously been reported to show a peculiar anti-predatory behaviour: It captures chemically protected, gymnosome pteropods in the water column and carries them on its dorsum, like a backpack. We report this association at four oceanic sampling sites between latitudes 45° and 71° S. Molecular barcodes of both hosts and pteropods are provided and compared with those of other hyperiidean and pteropod specimens. Morphological identifications as well as molecular analyses show a so far undocumented association of Hyperiella antarctica with the pteropod Spongiobranchaea australis in the Polar Frontal Zone (Lazarev Sea). H. dilatata carried Clione limacina antarctica specimens in the Weddell Sea, as recorded previously for the Ross Sea. Lengths of the abducted pteropods varied between 1 and 5 mm, with the biggest pteropod measuring more than half the host’s size. One of the abducting amphipods was a female carrying eggs. The formation of such tandem is known to be very efficient as protection from visually hunting icefish in the crystal-clear coastal waters around the Antarctic continent; however, in the open ocean, this behaviour was so far undocumented. Here, we develop hypotheses on its origin and function.

Keywords

Hyperiidea Hyperiella Clione Spongiobranchaea Gymnosomata COI barcodes 

Notes

Acknowledgements

We greatly acknowledge Dr. Olaf Boebel as chief scientist during the expedition PS103, for the numerous sampling opportunities, as well as the captain and crew of R/V Polarstern for their skilful support. Samples were also obtained during the R/V Polarstern expedition PS82 (ANT-XXIX/9) to the Filchner area of the Weddell Sea, for which we are grateful to the chief scientist Dr. Rainer Knust, captain and crew as well as fellow scientists of the pelagic sampling team for providing amphipods. This publication is a result of the Polarstern Grant No. AWI_PS103_03 of the project “InterPelagic” and Grant No. AWI_PS82_03 of the Filchner expedition. A permit for sampling south of 60° S under the Antarctic Treaty was obtained from the German Environmental Agency (UBA) with the number II 2.8–94003-3/382. Special thanks go to Franz Schröter and Simon Schöbinger for their valuable support in sorting samples during PS103.

Funding

This work was supported by the German Science Foundation/Deutsche Forschungsgemeinschaft (DFG) in the framework of the Priority Programme 1158 on “Antarctic Research with comparative investigations in Arctic ice areas” by the grant HA 7627/1-1 to the first author.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national and/or institutional guidelines for the care and use of animals (invertebrates) were followed.

Sampling and field studies

The necessary permit for sampling and observational field studies have been obtained by the authors from the competent authorities and are mentioned in the acknowledgements.

References

  1. Asao H, Nakamura Y, Furuya Y, Kuwahara S, Baker BJ, Kiyota H (2010) Synthesis of pteroenone and its stereoisomers, a defensive metabolite of the abducted Antarctic pteropod Clione antarctica. Helv Chim Acta 93(10):1933–1944CrossRefGoogle Scholar
  2. Barnard KH (1930) Crustacea. Part XI - Amphipoda. British Antarctic (“Terra Nova”) Expedition, 1910. Natural history Rep, Zoolog 8(4):307–454Google Scholar
  3. Barrera-Oro E (2003) Analysis of dietary overlap in Antarctic fish (Notothenioidei) from the South Shetland Islands: no evidence of food competition. Polar Biol 26:631–637CrossRefGoogle Scholar
  4. Böer M, Graeve M, Kattner G (2006) Impact of feeding and starvation on the lipid metabolism of the Arctic pteropod Clione limacina. J Exp Mar Biol Ecol 328:98–112CrossRefGoogle Scholar
  5. Boulenger GA (1902) Pisces. Report on the collections of natural history made in the Antarctic regions during the voyage of the ‘Southern Cross’. Brit Mus (natural history), London, pp 174-189Google Scholar
  6. Bovallius C (1887) Systematical list of the Amphipoda Hyperiidea. Kungliga Svenska Vetenskapsakademiens Handlingar 11:16, 50 ppGoogle Scholar
  7. Bowman TE (1973) Pelagic amphipods of the genus Hyperia and closely related genera. Smithson Contrib Zool 136:1–76Google Scholar
  8. Browne WE, Haddock SHD, Martindale MQ (2007) Phylogenetic analysis of lineage relationships among hyperiid amphipods as revealed by examination of the mitochondrial gene, cytochrome oxidase 1 (CO1). Integr Comp Biol 47(6):815–830CrossRefGoogle Scholar
  9. Bryan PJ, Yoshida WY, McClintock JB, Baker BJ (1995) Ecological role for pteroenone, a novel antifeedant from the conspicuous Antarctic pteropod Clione antarctica (Gymnosomata: Gastropoda). Mar Biol 122:271–277Google Scholar
  10. Casaux RJ, Mazzotta AS, Barrera-Oro ER (1990) Seasonal aspects of the biology and diet of nearshore nototheniid fish at Potter Cove, South Shetland Islands, Antarctica. Polar Biol 11:63–72Google Scholar
  11. Cheng F, Wang M, Sun S, Li C, Zhang Y (2013) DNA barcoding of Antarctic marine zooplankton for species identification and recognition. Adv Polar Sci 24(2):119–127CrossRefGoogle Scholar
  12. Claus C (1879) Die Gattungen und Arten der Platysceliden in systematischer Übersicht. Arbeiten aus dem Zoologischen Institut der Universität zu Wien 2:147–198Google Scholar
  13. Conover RJ, Lalli CM (1974) Feeding and growth in Clione limacina (Phipps), a pteropod mollusc. II. Assimilation, metabolism, and growth efficiency. J Exp Mar Biol Ecol 16(2):131–154CrossRefGoogle Scholar
  14. Costa FO, deWaard JR, Boutillier J, Ratnasingjam S, Dooh RT, Hajibabaei M, Hebert PDN (2007) Biological identifications through DNA barcodes: the case of the Crustacea. Can J Fish Aquat Sci 64(2):272–295CrossRefGoogle Scholar
  15. Dall WH (1871) Descriptions of sixty new forms of molluscs and brachiopods of the southeastern coast of North America and the North Pacific Ocean, with notes on others already described. Am J Conch 7(2):93–180Google Scholar
  16. Dana JD (1853) On the classification and geographical distribution of Crustacea. The report on Crustacea of the U. S. exploring expedition during the years 1838-42 under the command of Charles Wilkes, U.S.N. 13(2):689–1618. PhiladelphiaGoogle Scholar
  17. Duhamel G, Hulley PA, Causse R, Koubbi P, Vacchi M, Pruvost P, Vigetta S, Irisson JO, Mormède S, Belchier M, Dettai A, Detrich W, Gutt J, Jones CD, Kock KH, Abellan LJL, Van de Putte A (2014) Biogeographic patterns of fish. In: De Broyer C, Koubbi P, Griffiths HJ, Raymond B, Udekem d’Acoz C d’ et al. (eds) Biogeographic Atlas of the Southern Ocean. Scientific Committee on Antarctic Research, Cambridge, pp 323–362Google Scholar
  18. Fanta E, Donatti L, Freiberger S (1999) Visual sufficiency in food detection and initiation of feeding behaviour in the Antarctic fish Trematomus newnesi Boulanger. Antarct Rec 43(2):221–236Google Scholar
  19. Filin AA, Gorchinsky KV, Kiseleva VM (1991) Biomass of myctophids in the Atlantic sector of the Southern Ocean as estimated by acoustic surveys. Selected scientific papers (SC-CAMLR-SSP/7). CCAMLR, Hobart, Australia, pp 417–431Google Scholar
  20. Flores H, van Franeker JA, Cisewski B, Leach H, Van de Putte AP, Meesters E, Bathmann U, Wolff WJ (2011) Macrofauna under sea ice and in open surface layer of the Lazarev Sea, Southern Ocean. Deep-Sea Res II 58:1948–1961Google Scholar
  21. Folmer O, Black M, Hoeh R, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechn 3(5):294–299Google Scholar
  22. Foster BA (1987) Composition and abundance of zooplankton under the spring sea-ice of McMurdo Sound, Antarctica. Polar Biol 8(1):41–48CrossRefGoogle Scholar
  23. Foster BA (1989) Time and depth comparisons of sub-ice zooplankton in McMurdo Sound, Antarctica. Polar Biol 9(7):431–435CrossRefGoogle Scholar
  24. Foster BA, Montgomery JC (1993) Planktivory in benthic nototheniid fish in McMurdo Sound, Antarctica. Environ Biol Fish 36(3):313–318CrossRefGoogle Scholar
  25. Foster BA, Cargill JM, Montgomery JC (1987) Planktivory in Pagothenia borchgrevinki (Pisces: Nototheniidae) in McMurdo Sound, Antarctica. Polar Biol 8(1):49–54CrossRefGoogle Scholar
  26. Gasca R, Haddock SHD (2004) Associations between gelatinous zooplankton and hyperiid amphipods (Crustacea: Peracarida) in the Gulf of Mexico. Hydrobiologia 530(531):529–535CrossRefGoogle Scholar
  27. Guérin FE (1825) Encyclopédie Méthodique Histoire Naturelle. Entomologie, ou histoire naturelle des Crustacés, des Arachnides et des Insectes par M. Latreille. Tome 10. Paris Google Scholar
  28. Harbison GR, Biggs DC, Madin LP (1977) The associations of Amphipoda Hyperiidea with gelatinous zooplankton—II. Associations with Cnidaria, Ctenophora and Radiolaria. Deep-Sea Res 24:465–488CrossRefGoogle Scholar
  29. Hunt BPV, Pakhomov EA, Hosie GW, Siegel V, Ward P, Bernard K (2008) Pteropods in Southern Ocean ecosystems. Progr Oceanogr 78(3):193–221CrossRefGoogle Scholar
  30. Hunt B, Strugnell J, Bednarsek N, Linse K, Nelson RJ, Pakhomov E, Seibel B, Steinke D, Würzberg L (2010) Poles apart: the “bipolar” pteropod species Limacina helicina is genetically distinct between the Arctic and Antarctic oceans. PLoS One 5(3):e9835CrossRefGoogle Scholar
  31. Kattner G, Hagen W, Graeve M, Albers C (1998) Exceptional lipids and fatty acids in the pteropod Clione limacina from both polar oceans. Mar Chem 61:219–228CrossRefGoogle Scholar
  32. Klussmann-Kolb A, Dinapoli A (2006) Systematic position of the pelagic Thecosomata and Gymnosomata within Opisthobranchia (Mollusca, Gastropoda)—revival of the Pteropoda. J Zool Syst Evol Res 44:118–129CrossRefGoogle Scholar
  33. Laval P (1980) Hyperiid amphipods as crustacean parasitoids associated with gelatinous plankton. Oceanogr Mar Biol Ann Rev 18:11–56Google Scholar
  34. Lesueur BHMD (1821) Hyale, Hyalaea (Malacoz). In: Cuvier F (ed) Dictionnaire des Sciences Naturelles Levrault, Strasbourg & Le Normant, Paris, vol 22, pp 65–83Google Scholar
  35. Loeb VJ, Santora JA (2013) Pteropods and climate off the Antarctic Peninsula. Prog Ocean 116:31–48CrossRefGoogle Scholar
  36. Loeb V, Outram D, Puglise K, Armstrong WA, Hobday A, Nelson MM, Phleger CF, Sterling J, Watters G, Yender R (1998) Direct krill and zooplankton sampling. CAMLR 1996/97 Field season reports LJ-97. Southwest Fisheries Science Center, Antarctic Ecosystem Research GroupGoogle Scholar
  37. McClintock JB, Baker BJ (1998) Chemical ecology in Antarctic seas. Am Sci 86:254–263CrossRefGoogle Scholar
  38. McClintock JB, Janssen J (1990) Pteropod abduction as a chemical defence in a pelagic Antarctic amphipod. Nature 346:424–426CrossRefGoogle Scholar
  39. Minichev YS (1976) Subclass back-gilled molluscs. In: Animals and plants of Peter-the-Great Bay. Leningrad, Nauka, pp 92–95 (in Russian)Google Scholar
  40. Montagu G (1815) Descriptions of several new or rare animals, principally marine, discovered on the south coast of Devonshire. Trans Linn Soc London 11(1):1–26Google Scholar
  41. Müller F (1864) Für Darwin. Wilhelm Engelmann, Leipzig, 91 ppGoogle Scholar
  42. Niebuhr C (1776) Icones rerum naturalium, quas in itinere orientali depingi curavit Petrus Forskål, prof. Haun., post mortem auctoris... edidit Carsten Niebuhr. Hauniae [Copenhagen], 43 pp.Google Scholar
  43. Orbigny AD d' (1836) Voyage dans l’Amérique méridionale exécuté pendant les années 1826, 1827, 1828, 1829, 1830, 1831, 1832 et 1833, Tome 5, Partie 3. Mol Ther:758 ppGoogle Scholar
  44. Pakhomov EA, Perissinotto R, Froneman PW (1999) Predation impact of carnivorous macrozooplankton and micronekton in the Atlantic sector of the Southern Ocean. J Mar Sys 19:47–64CrossRefGoogle Scholar
  45. Phleger CF, Nelson MM, Mooney B, Nichols PD (1999) Lipids of abducted Antarctic pteropods, Spongiobranchaea australis, and their hyperiid amphipod host. Comp Biochem Physiol B 124:295–307CrossRefGoogle Scholar
  46. Ratnasingham S, Hebert PD (2007) BOLD: The Barcode of Life Data System (http://www. barcodinglife. org). Mol Ecol Notes 7(3):355–364.
  47. Roberts D, Hopcroft RR, Hosie GW (2014) Southern Ocean pteropods. In: De Broyer C, Koubbi P, Griffiths HJ, Raymond B, Udekem d’Acoz C d’ et al (eds) Biogeographic Atlas of the Southern Ocean. Scientific Committee on Antarctic Research, Cambridge, pp 276–283Google Scholar
  48. Rodhouse G, White MG (1995) Cephalopods occupy the ecological niche of epipelagic fish in the Antarctic polar frontal zone. Biol Bull 189(2):77–80CrossRefGoogle Scholar
  49. Schlitzer R (2018) Ocean Data View, https://odv.awi.de
  50. Sheader M, Batten SD (1995) Comparative study of sympatric populations of two hyperiid amphipods, Primno johnsoni and P. evansi, from the eastern North Atlantic Ocean. Mar Biol 124:43–50CrossRefGoogle Scholar
  51. Smith EA (1902) VII. Mollusca. Report on the collections of natural history made in the Antarctic regions during the voyage of the “Southern Cross” 201-213, pls 24-25Google Scholar
  52. Sromek L, Lasota R, Szymelfenig M, Wolowicz M (2015) Genetic evidence for the existence of two species of the “bipolar” pelagic mollusc Clione limacina. Am Malacol Bull 33(1):118–120CrossRefGoogle Scholar
  53. Stebbing TRR (1888) Report on the Amphipoda collected by H.M.S. Challenger during the years 1873-1876. Report on the scientific results of the voyage of H.M.S. challenger during the years 1873-76. Zoology 29:1–1737Google Scholar
  54. Stephensen K (1925) Hyperiidea-Amphipoda (part 3: Lycaeopsidae, Pronoidae, Lycaeidae, Brachyscelidae, Oxycephalidae, Parascelidae, Platyscelidae). Report on the Danish oceanographical expeditions 1908-1910 to the Mediterranean and adjacent seas 2:151–252Google Scholar
  55. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729CrossRefGoogle Scholar
  56. Vacchi M, La Mesa M (1995) The diet of the Antarctic fish Trematomus newnesi Boulenger, 1902 (Nototheniidae) from Terra Nova Bay, Ross Sea. Ant Sci 7(1):37–38CrossRefGoogle Scholar
  57. Vinogradov GM (1999) Amphipoda. In: Boltovskoy D (ed) South Atlantic zooplankton. Backhuys Publishers, Leiden, pp 1141–1240Google Scholar
  58. Weigmann-Haass R (1989) Zur Taxonomie und Verbreitung der Gattung Hyperiella Bovallius 1887 im antarktischen Teil des Atlantik (Crustacea: Amphipoda: Hyperiidae). Senckenberg Biol 69:177–191Google Scholar
  59. Zeidler W (2015) A review of the hyperiidean amphipod genus Hyperoche Bovallius, 1887 (Crustacea: Amphipoda: Hyperiidea: Hyperiidae), with the description of a new genus to accommodate H. shihi Gasca, 2005. Zootaxa 3905(2):151–192CrossRefGoogle Scholar
  60. Zeidler W, De Broyer C (2009) Catalogue of the Hyperiidean Amphipoda (Crustacea) of the Southern Ocean with distribution and ecological data. In: De Broyer C (ed) Census of Antarctic marine life: synopsis of the Amphipoda of the Southern Ocean. vol. 3. Bull l’Institut R Sci Nat Belgique, Biol 79:1–96Google Scholar
  61. Zeidler W, De Broyer C (2014) Amphipoda: Hyperiidea. In: De Broyer C, Koubbi P, Griffiths HJ, Raymond B, Udekem d’Acoz C d’ et al (eds) Biogeographic Atlas of the Southern Ocean. Scientific Committee on Antarctic Research, Cambridge, pp 303–308Google Scholar

Copyright information

© Senckenberg Gesellschaft für Naturforschung 2018

Authors and Affiliations

  1. 1.BreMarE - Bremen Marine Ecology, Marine ZoologyUniversität BremenBremenGermany
  2. 2.Alfred-Wegener-Institut Helmholtz-Zentrum für Polar- und MeeresforschungBremerhavenGermany
  3. 3.South Australian MuseumAdelaideAustralia

Personalised recommendations