Review paper Pseudocollinia histophagous ciliates infect krill in the Pacific and Atlantic Oceans and possibly worldwide

Authors

  • Jaime Gómez-Gutiérrez CICIMAR-IPN
  • So Kawaguchi

DOI:

https://doi.org/10.37543/oceanides.v32i2.204

Keywords:

Collinia, Pseudocollinia, Parasitoid, Apostome cilliates, Euphausiacea, distribution, zoogeography

Abstract

The genus Pseudocollinia (Apostomatida, Pseudocolliniidae) currently includes four species (P. beringensis, P. oregonensis, P. brintoni, and P. similis) that infect adults of seven numerically dominant krill species (Order Euphausiacea) in the northeastern Pacific (Bering Sea-to-Gulf of California). In this review, we found four reports in other parts of the world of misidentified or unidentified protists infecting krill. Based on their morphology, cell size and infection of the hemocoel’s host, we infer they are histophagous Pseudocollinia ciliates. We thus conclude that previous reports of protists (identified as microsporidians) infecting Thysanoessa inermis in the northwestern Atlantic Ocean (Bay of Fundy) and unidentified endoparasite ciliates infecting the Euphausia superba in the Southern Ocean (Admiralty Bay, King George Island), Euphausia pacifica in Sanriku, Japan and Euphausia similis var. armata in Tasmania, Australia are actually Pseudocollinia parasitoid ciliates that await to be morphologically and genetically described. This review provides strong evidence that apostome Pseudocollinia ciliates are widespread distributed in the Pacific and Atlantic Oceans, infecting at least nine krill species from Arctic-to-Antarctic zoogeographic regions, having perhaps worldwide distribution as several of their krill hosts. Future studies should focus on discovering parasitoid ciliates in other krill species, as well as in other phytoplankton and zooplankton taxonomic groups.

Downloads

Download data is not yet available.

Author Biography

Jaime Gómez-Gutiérrez, CICIMAR-IPN

Investigador del Departamento de Plancton y Ecologí­a Marina

References

Bradbury, P. C. 1994. Parasitic protozoa of mollusks and crustacea, 2nd edn. In: Kreier, J.P. (ed.) Parasitic protozoa, Academic Press, San Diego, CA, 8, 139-263. https://doi.org/10.1016/B978-0-08-092414-4.50008-9

Brinton, E. 1962. The distribution of Pacific euphausiids. Bull. Scripps Inst. Oceanogr., 8: 51-270.

Brinton, E. 1975. Euphausiids of Southeast Asian waters. Naga Reports. Scripps Institution of Oceanography.

Brinton, E., M. D. Ohman, A. W. Townsend, M. D. Knight & A. L. Bridgeman. 2000. Euphausiids of the world ocean. World Biodiversity Database CD-ROM Series for [Microsoft] Windows version 1.0. Expert Center for Taxonomic Identification, Amsterdam.

Buchholz, F. 1982. Drach's molt staging system adapted for euphausiids. Mar. Biol., 66: 301- 305. https://doi.org/10.1007/BF00397036

Cachon, J. & M. Cachon. 1968. Cytologie et cycle évolutif des Chytriodinium (Chatton). Protistol., 4, 249-262.

Capriulo, G. M. & E. B. Small. 1986. Discovery of an apostome ciliate (Collinia beringensis n. sp.) endoparasitic in the Bering Sea euphausiid Thysanoessa inermis. Dis. Aquat. Org., 1:141-146. https://doi.org/10.3354/dao001141

Capriulo, G. M., M. J. Pedone, & E. B. Small. 1991. High apostome ciliate endoparasite infection rates found in the Bering Sea euphausiid Thysanoessa inermis. Mar. Ecol. Prog. Ser., 72:203-204. https://doi.org/10.3354/meps072203

Chantangsi, C., D. H. Lynn, S. Rueckert, A. J. Prokopowicz, S. Panha & B. S. Leander. 2013. Fusiforma themisticola n. gen., n. sp., a new genus and species of apostome ciliate infecting the hyperiid amphipod Themisto libellula in the Canadian Beaufort Sea (Arctic Ocean), and establishment of the Pseudocolliniidae. (Ciliophora, Apostomatia). Protist, 164: 793-810. https://doi.org/10.1016/j.protis.2013.09.001

Clarke, A. & P. A. Tyler. 2008. Adult Antarctic krill feeding at abyssal depths. Curr. Biol., 18(4): 282-285. https://doi.org/10.1016/j.cub.2008.01.059

Clamp, J. C., P. C. Bradbury, M. Strüder-Kypke & D. H. Lynn. 2008. Phylogenetic position of the apostome ciliates (Phylum Ciliophora, Subclass Apostomatia) tested using small subunit rRNA gene sequences. Denisia, 23: 395-402.

D'Amato, M. E., G. W. Harkins, T. de Oliveira, P. R. Teske & M. J. Gibbons. 2008. Molecular dating and biogeography of the neritic krill Nyctiphanes. Mar. Biol., 155: 243-247. https://doi.org/10.1007/s00227-008-1005-0

Daugbjerg, N., G. Hansen, J. Larsen & Ø. Moestrup. 2000. Phylogeny of some of the major genera of dinoflagellates based on ultrastructure and partial LSU rDNA sequence data, including the erection of three new genera of unarmored dinoflagellates. Phycologia, 39: 302-317. https://doi.org/10.2216/i0031-8884-39-4-302.1

Dogiel, V. 1906. Beitrge zur Kenntnis der Peridineen. Mitt. Zool. Stn. Neapel., 18: 1-45.

Finlay, B. J. 2002. Global dispersal of free-living microbial eukaryotic species. Science, 296: 1061-1063. https://doi.org/10.1126/science.1070710

Foissner, W. 2006. Biogeography and dispersal of micro-organisms: A review emphasizing protists. Acta Protozool., 45: 111-136.

Gómez, F., D. Moreira & P. López-García. 2009. Life cycle and molecular phylogeny of the dinoflagellates Chytriodinium and Dissodinium, ectoparasites of copepod eggs. Eur. J. Protistol., 45: 260-270. https://doi.org/10.1016/j.ejop.2009.05.004

Gómez-Gutiérrez, J. & D. J. Shields. 1998. Range extension for Oculophryxus bicaulis Shields and Gómez (Isopoda, Dajidae) in the South China Sea. Crustaceana, 71: 167-170. https://doi.org/10.1163/156854098X00149

Gómez-Gutiérrez, J. & I. Castellanos-Osorio. 2010. Heterophryxus appendiculatus G.O. Sars, 1885 (Isopoda: Dajidae) extension range in the northeast Pacific and Caribbean Sea (Mexico) that indicates inter-ocean zoogeographic distribution. Crustaceana, 83: 1221-1230. https://doi.org/10.1163/001121610X527004

Gómez-Gutiérrez, J., W. T. Peterson, A. De Robertis & R. Brodeur. 2003. Mass mortality of krill caused by parasitoid ciliates. Science, 301: 339. https://doi.org/10.1126/science.1085164

Gómez-Gutiérrez, J., W. T. Peterson & F. Morado. 2006. Discovery of a ciliate parasitoid of euphausiids off Oregon, USA. Collinia oregonensis n. sp. (Apostomatida: Colliniidae). Dis. Aquat. Org., 71: 33-49. https://doi.org/10.3354/dao071033

Gómez-Gutiérrez, J., S. Kawaguchi & S. Nicol. 2009. Epibiotic suctorians and enigmatic ecto and endoparasitoid dinoflagellates of euphausiid eggs (Euphausiacea) off Oregon, USA. J. Plankt. Res., 31: 777-786. https://doi.org/10.1093/plankt/fbp026

Gómez-Gutiérrez, J., S. Kawaguchi & J. R. Morales-Ávila. 2017. Global diversity and ecological functions of parasites of euphausiids. Springer Nature SBM, UK. http://www.springer.com/us/ book/9783319410531. https://doi.org/10.1007/978-3-319-41055-5

Gómez-Gutiérrez, J., C. J. Robinson, S. Kawaguchi & S. Nicol. 2010. Parasite diversity of Nyctiphanes simplex and Nematoscelis difficilis (Crustacea: Euphausiacea) along the Northwestern coast of Mexico. Dis. Aquat. Org., 88: 249-266. https://doi.org/10.3354/dao02155

Gómez-Gutiérrez, J., M. Strüder-Kypke, D. H. Lynn, T. C. Shaw, M. J. Aguilar-Méndez, A. López-Cortés, S. Martínez-Gómez & C. J. Robinson. 2012. Pseudocollinia brintoni gen. nov. sp. nov. (Apostomatida: Colliniidae), a parasitoid ciliate infecting the euphausiid Nyctiphanes simplex. Dis. Aquat. Org., 99: 57-78. https://doi.org/10.3354/dao02450

Gómez-Gutiérrez, J., A. López-Cortez, M. J. Aguilar-Méndez, J. Del Angel-Rodríguez, N. Tremblay, T. Zenteno-Savín & C. J. Robinson. (2015a) Histophagous ciliate Pseudocollinia brintoni and bacterial assemblage interaction with krill Nyctiphanes simplex: I. Transmission process. Dis. Aquat. Org., 16: 213-226. https://doi.org/10.3354/dao02922

Gómez-Gutiérrez, J., J. Del Angel-Rodríguez, N. Tremblay, T. Zenteno-Savín, M. J. Aguilar-Méndez, A. López-Cortez & C. J. Robinson. 2015b. Histophagous ciliate Pseudocollinia brintoni and bacterial assemblage interaction with krill Nyctiphanes simplex: II. Host responses. Dis. Aquat. Org., 16: 227-336. https://doi.org/10.3354/dao02923

Kawaguchi, S. & T. Toda. 1997. Discovery of ciliates reproducing in the gut of Antarctic krill. Polar Biol., 18: 158-160. https://doi.org/10.1007/s003000050171

Kawaguchi, S., G. Hosie, S. Nicol, H. Marchant, A. McEldowney, G. Nash, M. Naganobu, T. Ichii, T. Toda & M. Kobayashi. 1999. Do gregarines cause damage to midgut gland and intestinal epithelium of Antarctic krill? Paper presented at the Second International Symposium of krill, Santa Barbara, CA, August 22-26. https://doi.org/10.1007/s003000050400

Kulka, D. W. & S. Corey. 1984. Incidence of parasitism and irregular development of gonads in Thysanoessa inermis (Kroyer) in the Bay of Fundy (Euphausiacea). Crustaceana, 46: 87-94. https://doi.org/10.1163/156854084X00081

Lynn, D. H., J. Gómez-Gutiérrez, M. C. Strü-der-Kypke & C. T. Shaw. 2014. Ciliate species diversity and host-parasitoid codiversification in the apostome genus Pseudocollinia (Ciliophora, Apostomatia, Pseudocolliniidae) that infect krill, with description of Pseudocollinia similis n. sp., a parasitoid of the krill Thysanoessa spinifera. Dis. Aquat. Org., 112: 89-102. https://doi.org/10.3354/dao02796

Parmentier, E. & L. Michel. 2013. Boundary lines in symbiosis forms. Symbiosis, 60: 1−5. https://doi.org/10.1007/s13199-013-0236-0

Shimazu, T. 2006. Trematodes and cestodes parasitic in euphausiids. Bull. Plankton Soc. Japan, 53(1): 45-53, (in Japanese, translated to English by So Kawaguchi).

Stankovic, A. & S. Rakusa-Suszczewski. 1996. Parasitic protozoa on appendages and inside the body of Euphausia superba Dana. Polish Polar Res., 17: 169-171.

Sokolova, M. N. 1994. Euphausiid "dead body rain" as a source of food for abyssal benthos. Deep Sea. Res. Part I: Oceanogr. Res. Pap., 41(4): 741-746. https://doi.org/10.1016/0967-0637(94)90052-3

Takahashi, K. T., S. Kawaguchi, M. Kobayashi. & T. Toda. 2003. Parasitic eugregarines change their spatial distribution within the host digestive tract of Antarctic krill, Euphausia superba. Polar Biol., 26: 468-473. https://doi.org/10.1007/s00300-003-0511-2

Takahashi, K. T., S. Kawaguchi, M. Kobayashi & T. Toda. 2011. Eugregarinid infection within the digestive tract of larval Antarctic krill, Euphausia superba. Polar Biol., 34: 1167-1174. https://doi.org/10.1007/s00300-011-0979-0

Van der Spoel, S., A. C. Pierrot-Bults & P. H. Schalk. 1990. Probable mesozoic vicariance in the biogeography of Euphausiacea. Bijdragen tot de Dierkunde, 60: 155-162.

Downloads

Published

2017-11-24

How to Cite

Gómez-Gutiérrez, J., & Kawaguchi, S. (2017). Review paper Pseudocollinia histophagous ciliates infect krill in the Pacific and Atlantic Oceans and possibly worldwide. CICIMAR Oceánides, 32(2), 15–24. https://doi.org/10.37543/oceanides.v32i2.204

Issue

Section

Articles