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Parasitic infection of the hyperiid amphipod Themisto libellula in the Canadian Beaufort Sea (Arctic Ocean), with a description of Ganymedes themistos sp. n. (Apicomplexa, Eugregarinorida)

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Abstract

Two parasites were found in the hyperiid amphipod Themisto libellula sampled with nets and collected by sediment traps over the annual cycle in the Canadian Beaufort Sea. The trophozoites of the newly described gregarine Ganymedes themistos sp. n. infected the digestive tract of 60.2% of the T. libellula analyzed from net collections. An unidentified ciliate infected the body cavity of 4.4% of amphipods. G. themistos possessed the ball-like structure at the anterior end and the cup-like invagination at the posterior end that are typical of the genus Ganymedes. The frequency and severity (number of parasites host−1) of infection by G. themistos increased with the length of T. libellula in the range 8–20 mm, and leveled off at ca. 94% and 186 trophozoites host−1 on average in the range 20–34 mm. Spatially, gregarine infection was less severe (63 ± 100 G. themistos host−1) on the Slope than on the Mackenzie Shelf (110 ± 160) and in the Amundsen Gulf (132 ± 157). No evidence of an impact of trophozoite infection on the feeding and sexual maturation of the host was found. For a given size of T. libellula, infection by both parasites was more frequent in the traps than in the nets (G. themistos: 91.0% vs. 82.7%; ciliates: 16.3% vs. 6%). The 2.7 times higher infection frequency in the traps suggested that the ciliate parasite may kill its host.

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References

  • Åbro A (1996) Gregarine infestation of adult Calopteryx virgo L. (Odonata: Zygoptera). J Nat Hist 30:855–859

    Article  Google Scholar 

  • Arrigo KR, van Dijken GL (2004) Annual cycles of sea ice and phytoplankton in Cape Bathurst polynya, southeastern Beaufort Sea, Canadian Arctic. Geophys Res Lett 31:8. doi:10.1029/2003GL018978

    Article  Google Scholar 

  • Barber DG, Hanesiak JM (2004) Meteorological forcing of sea ice concentration in the southern Beaufort Sea over the period 1979–2000. J Geophys Res 109:C6. doi:10.1029/2003JC002027

    Article  Google Scholar 

  • Bowman TE (1960) The pelagic amphipod genus Parathemisto (Hyperiidea : Hyperiidae) in the North Pacific and adjacent Arctic Ocean. Proc US Natl Mus 112:343–392

    Google Scholar 

  • Clopton RE, Janovy J (1993) Developmental niche structure in the gregarine assemblage parasitizing Tenebrio-Molitor. J Parasitol 79:701–709

    Article  Google Scholar 

  • Dalpadado P (2002) Inter-specific variations in distribution, abundance and possible life-cycle patterns of Themisto spp. (Amphipoda) in the Barents Sea. Polar Biol 25:656–666

    Google Scholar 

  • Darnis G, Barber DG, Fortier L (2008) Sea ice and the onshore–offshore gradient in pre-winter zooplankton assemblages in southeastern Beaufort Sea. J Mar Syst 74:994–1011

    Article  Google Scholar 

  • Dunbar MJ (1946) On Themisto libellula in Baffin Island coastal waters. J Fish Res Board Can 6(6):419–434

    Google Scholar 

  • Dunbar MJ (1957) The determinants of production in northern seas: a study of the biology of Themisto libellula (Mandt). Can J Zool 35:797–819

    Article  Google Scholar 

  • Gómez-Gutiérrez J, Peterson WT, Robertis A, Brodeur RD (2003) Mass mortality of krill caused by parasitoid ciliates. Science 301:339

    Article  PubMed  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Guindon S, Lethiec F, Duroux P, Gascuel O (2005) PHYML online-a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res 1:33

    Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  CAS  PubMed  Google Scholar 

  • Huxley JS (1910) On Ganymedes anaspidis (nov. gen., nov. sp.), a gregarine from the digestive tract of Anaspides tasmaniae (Thompson). Q J Microsc Sci 55:155–175

    Google Scholar 

  • Jiménez R, de Barniol L, Machuca M (2002) Nematopsis marinus n. sp., a new septate gregarine from cultured penaeoid shrimp Litopenaeus vannamei (Boone), in Ecuador. Aquac Res 33(4):231–240

    Article  Google Scholar 

  • Jones I (1968) The life cycle of Ganymedes oaklandi n. sp., an acephaline gregarine of Gammarus fasciatus (Say). J Protozool 15:414–418

    Google Scholar 

  • Koszteyn J, Timoffev S, Węsławski JM, Malinga B (1995) Size structure of Themisto abyssorum (Boeck) and Themisto libellula (Mandt) populations in European Arctic seas. Polar Biol 15:85–92

    Article  Google Scholar 

  • Leander BS (2008) Marine gregarines: evolutionary prelude to the apicomplexan radiation? Trends Parasitol 24:60–67

    Article  PubMed  Google Scholar 

  • Leander BS, Clopton RE, Keeling PJ (2003) Phylogeny of gregarines (Apicomplexa) as inferred from small-subunit rDNA and beta-tubulin. Int J Syst Evol Microbiol 53:345–354

    Article  CAS  PubMed  Google Scholar 

  • Levine ND (1977) Revision and checklist of the species (other than Lecudina) of the aseptate gregarine family Lecudinidae. J Protozool 24:41–52

    CAS  PubMed  Google Scholar 

  • Lightner DV (1993) Diseases of cultured penaeid shrimp. Handbook of mariculture. CRC Press, Boca Raton, pp 393–486

    Google Scholar 

  • Macdonald RW, Paton DW, Carmack EC, Omstead A (1995) The freshwater budget and under-ice spreading of Mackenzie River water in the Canadian Beaufort Sea based on salinity and 18O/16O measurements in water and ice. J Geophys Res 100:895–919

    Article  CAS  Google Scholar 

  • Maddison DR, Maddison WP (2000) MacClade 4. Sinauer Associates, Sunderland

    Google Scholar 

  • Perkins FO, Barta JR, Clopton RE, Pierce MA, Upton SJ (2000) Phylum Apicomplexa. In: Lee JJ, Leedale GF, Bradbury P (eds) The illustrated guide to the protozoa, 2nd edn. Allen Press, Inc., Lawrence, pp 190–304

    Google Scholar 

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  CAS  PubMed  Google Scholar 

  • Sampei M, Sasaki H, Hattori H, Forest A, Fortier L (2009) Significant contribution of passively sinking copepods to downward export flux in Canadian Arctic waters. Limnol Oceanogr 54:1894–1900

    CAS  Google Scholar 

  • Sheridan LAD, Poulin R, Ward DF, Zuk M (2000) Sex differences in parasitic infestation among arthropod hosts: is there a male bias? Oikos 88:327–334

    Article  Google Scholar 

  • Simpson KG, Tremblay J-E, Gratton Y, Price NM (2008) An annual study of nutrient distribution in the southeastern Beaufort Sea, Mackenzie Shelf and Amundsen Gulf. J Geophys Res 113:C07016. doi:10.1029/2007JC004462

    Article  Google Scholar 

  • Siva-Jothy MT, Plaistow SJ (1999) A fitness cost of eugregarine parasitism in damselfly. Ecol Entomol 24:465–470

    Article  Google Scholar 

  • Swofford DL (1999) Phylogenetic analysis using parsimony (and other methods) PAUP* 4.0. Sinauer Associates, Inc., Sunderland

    Google Scholar 

  • Takahashi KT, Kawaguchi S, Kabayashi M, Toda T (2003) Parasitic eugregarines change their spatial distribution within the host digestive tract of Antarctic krill, Euphausia superba. Polar Biol 26:468–473

    Google Scholar 

  • Théodoridès MJ, Desportes I (1972) Mise en évidence de nouveaux représentants de la famille des Ganymedidae Huxley, grégarines parasites de crustacés. CR Acad Sci Paris 274:3251–3253

    Google Scholar 

  • Théodoridès J, Desportes I (1975) Sporozoaires d’invertébrés pélagiques de Villefranche-sur-Mer (ètude descriptive et faunistique). Protistologica 11:205–220

    Google Scholar 

  • Tremblay J-E, Simpson K, Martin J, Miller L, Gratton Y, Barber D, Price NM (2008) Vertical stability and the annual dynamics of nutrients and chlorophyll fluorescence in the coastal, southeast Beaufort Sea. J Geophys Res 113:C07S90. doi:10.1029/2007JC004547

    Article  Google Scholar 

  • Welch HE, Bergmann MA, Siferd TD, Martin KA, Curtis MF, Crawford RE, Conover RJ, Hop H (1992) Energy flow through the marine ecosystem of the Lancaster sound region, arctic Canada. Arctic 45:343–357

    Google Scholar 

  • Zuk M (1987) The effects of Gregarine parasites, body size, and time of day on spermatophore production and sexual selection in field crickets. Behav Ecol 21(1):65–72

    Article  Google Scholar 

  • Zuk M (1990) Reproductive strategies and disease susceptibility: an evolutionary viewpoint. Parasitol Today 6:231–233

    Article  CAS  PubMed  Google Scholar 

  • Zuk M, MacKean KA (1996) Sex differences in parasitic infestations: patterns and processes. Int J Parasitol 26:1009–1024

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the crew of CCGS Pierre Radisson and CCGS Amundsen for their professional work at sea. S. Lebel, L. Michaud, L. Létourneau, and G. Darnis helped in the field and in the laboratory. This study was part of the Canadian Arctic Shelf Exchange Study (CASES) funded by the Natural Sciences and Engineering Research Council of Canada. S. Rueckert and B. S. Leander were funded by the Tula Foundation’s Centre for Microbial Diversity and Evolution. This is a contribution to Québec-Océan at Université Laval and the Canada Research Chair on the response of marine arctic ecosystems to climate warming.

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Authors and Affiliations

  1. Québec-Océan, Département de Biologie, Université Laval, Quebec, QC, G1V 0A6, Canada

    Anna J. Prokopowicz, Josée Michaud & Louis Fortier

  2. Departments of Zoology and Botany, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada

    Sonja Rueckert & Brian S. Leander

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  1. Anna J. Prokopowicz
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  2. Sonja Rueckert
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  3. Brian S. Leander
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  4. Josée Michaud
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  5. Louis Fortier
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Correspondence to Anna J. Prokopowicz.

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Prokopowicz, A.J., Rueckert, S., Leander, B.S. et al. Parasitic infection of the hyperiid amphipod Themisto libellula in the Canadian Beaufort Sea (Arctic Ocean), with a description of Ganymedes themistos sp. n. (Apicomplexa, Eugregarinorida). Polar Biol 33, 1339–1350 (2010). https://doi.org/10.1007/s00300-010-0821-0

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