Skip to main content

Biology of Symbiotic Apostome Ciliates: Their Diversity and Importance in the Aquatic Ecosystems

  • Chapter
Marine Protists

Abstract

Recently apostome ciliates have been paid more attention in the aquatic ecosystems, since the host population dynamics are more highly influenced by these protists than previously expected. Apostomes are all symbiotic, associated mainly with a wide variety of planktonic and benthic crustaceans and other invertebrates such as cnidarians and chaetognaths . They can also be found within cysts of other apostomes . Some taxa require two distinct hosts.

The life cycles of apostomes are complicated, essentially consisting of four morphologically and functionally different stages: quiescent, encysted phoront s ; feeding trophonts ; divisional, encysted tomont s ; and infective tomite s , with several substages in some taxa. Each metamorphosis accompanies reformation of kineties and organelles. Excystation from phoronts to trophonts is triggered by cues such as molting, injury and predation of hosts. A cell within a phoront is furnished with cilia ready to hatch, and with specialized, membranous organelles related to rapid expansion of food vacuole s. Trophonts with or without a cytostome take nutrients through phagocytosis or pinocytosis, respectively. Some taxa such as Gymnodinoides are exuviotrophic and harmless to the host, while genera such as Vampyrophrya are regarded as parasitoids rather than parasites . Proliferation is mainly due to palintomy to produce numerous tomites within a tomont , whose duration seems to be most greatly influenced by water temperature in the life cycle of apostomes. Tomites actively search for a new host and then transform into phoronts on it.

The present paper briefly reviews previous studies concerning apostomes , and our original data on the histotrophic species Vampyrophrya pelagica infecting copepod s .

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Allen RD (1974) Food vacuole membrane growth with microtubule-associated membrane transport in Paramecium. J Cell Biol 63:904–922

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bradbury PC (1966a) The life cycle and morphology of the apostomatous ciliate, Hyalophysa chattoni n. g., n. sp. J Protozool 13:209–225

    Article  Google Scholar 

  • Bradbury PC (1966b) The fine structure of the mature tomite of Hyalophysa chattoni. J Protozool 13:591–607

    Article  Google Scholar 

  • Bradbury PC (1973) The fine structure of the cytostome of the apostomatous ciliate Hyalophysa chattoni. J Protozool 20:405–414

    Article  Google Scholar 

  • Bradbury PC (1974a) The fine structure of the phoront of the apostomatous ciliates, Hyalophysa chattoni. J Protozool 21:112–120

    Article  Google Scholar 

  • Bradbury PC (1974b) Stored membranes associated with feeding in apostome trophonts with different diets. Protistologica 10:533–542

    Google Scholar 

  • Bradbury PC (1989) Evidence for hymenostome affinities in an apostome ciliate. J Protozool 36:95–103

    Article  Google Scholar 

  • Bradbury PC (1996) Parasitic ciliates. In: Hausmann K, Bradbury PC (eds) Ciliates. Gustav Fisher, Stuttgart, pp 463–477

    Google Scholar 

  • Bradbury PC, Clamp JC (1973) Hyalophysa lwoffi, sp. n. from the fresh-water shrimp Palaemonetes paludosus and revision of the genus Hyalophysa. J Protozool 20:210–213

    Article  Google Scholar 

  • Bradbury PC, Trager W (1967a) Metamorphosis from the phoront to the trophont in Hyalophysa. J Protozool 14:210–213

    Article  Google Scholar 

  • Bradbury PC, Trager W (1967b) Excystation of apostomes ciliates in relation to molting of their crustacean hosts. II. Effects of glycogen. Biol Bull 133:310–316

    Article  CAS  PubMed  Google Scholar 

  • Bradbury PC, Clamp JC, Lyon JT III (1974) Terebrospira chattoni, sp. n., a parasite of the endocuticle of the shrimp Palaemonetes pugio Holthuis. J Protozool 21:678–686

    Article  CAS  PubMed  Google Scholar 

  • Bradbury PC, Deroux G, Campillo A (1987) The feeding apparatus of a chitinivorous ciliate. Tissue Cell 19:351–363

    Article  CAS  PubMed  Google Scholar 

  • Bradbury PC, Zhang L-M, Shi Z-B (1996) A redescription of Gymnodinioides Caridnae (Miyashita, 1933) from Palaemontetes sinensis (Sollaud, 1911) in Songhua river. J Eukaryot Microbiol 43:404–408

    Article  Google Scholar 

  • Bradbury PC, Song W, Zhang L (1997) Stomatogenesis during the formation of the tomite of Hyalophysa chattoni (Hymenostomatida: Ciliophora). Eur J Protistol 33:409–419

    Article  Google Scholar 

  • Bush AO, Fernández JC, Esch GW, Seed JR (2001) Parasitism: the diversity and ecology of animal parasites. Cambridge University Press, Cambridge, 566pp

    Google Scholar 

  • Capriulo GM, Small EB (1986) Discovery of an apostomes ciliate (Collinia beringensis n. sp.) endoparasitic in the Bering Sea euphausiid Thysanoessa inermis. Dis Aquat Org 1:141–146

    Article  Google Scholar 

  • Capriulo GM, Pedone MJ, Small EB (1991) High apostomes ciliate endoparasite infection rates found in the Bering Sea euphausiid Thysanoessa inermis. Mar Ecol Prog Ser 72:203–204

    Article  Google Scholar 

  • Chantangsi C, Lynn DH, Rueckert S, Prokopowicz AJ, Panha S, Leander BS (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

    Article  CAS  PubMed  Google Scholar 

  • Chatton E, Lwoff A (1935) Les ciliés apostomes 1. Aperçu historique et général; etude monographique des genres et des espèces. Arch Zool Exp Gén 77:1–453

    Google Scholar 

  • Clamp JC, Bradbury PC, Strüder-Kypke MC, Lynn DH (2008) Phylogenetic position of the apostome ciliates (Phylum Ciliophora, Subclass Apostomatia) tested using small subunit RNA gene sequences. Denisia 23:395–402

    Google Scholar 

  • Corliss JO (1979) The ciliated protozoa: characterization, classification, and guide to the literature, 2nd edn. Pergamon Press, London/New York

    Google Scholar 

  • Fischer-Defoy D, Hausmann K (1981) Microtubules, microfilaments, and membranes in phagocytosis: structure and function of the oral apparatus of the ciliate Climacostomum virens. Differentiation 20:141–151

    Article  Google Scholar 

  • Gómez-Gutiérrez J, Peterson WT, Morado JF (2006) Discovery of a ciliate parasitoid of euphausiids off Oregon, USA: Collinia oregonensis n. sp. (Apostomatida: Colliniidae). Dis Aquat Org 71:33–49

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Gómez-Gutiérrez J, Strüder-Kypke MC, Lynn DH, Shaw TC, Aguilar-Méndex MJ, López-Corés A, Martínez-Gómez S, Robinson CJ (2012) Pseudocollinia brintoni gen. nov., sp. nov. (Apostomatida: Colliniidae), a parasitoid ciliate infecting the euphausiid Nyctiphanes simplex. Dis Aquat Org 99:57–78

    Article  PubMed  Google Scholar 

  • Grimes BH (1976) Notes on the distribution of Hyalophysa and Gymnodinioides on crustacean hosts in coastal North Carolina and a description of Hyalophysa trageri sp. n. J Protozool 23:246–251

    Article  Google Scholar 

  • Grimes BH, Bradbury PC (1992) The biology of Vampyrophrya pelagica (Chatton & Lwoff, 1930), a histophagous apostomes ciliate associated with marine calanoid copepods. J Protozool 39:65–79

    Article  Google Scholar 

  • Guo Z, Liu S, Hu S, Li T, Huang Y, Liu G, Zhang H, Lin S (2012) Prevalent ciliate symbiosis on copepods; high genetic diversity and wide distribution detected using small subunit ribosomal RNA gene. PloS One 7(9):e44847

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hausmann K, Hausmann M (1981) Structural studies on Trichodina pediculus (Ciliophora, Peritricha). I. The locomotor fringe and the oral apparatus. J Ultrastruct Res 74:131–143

    Article  CAS  PubMed  Google Scholar 

  • Hausmann K, Peck RK (1979) The mode of function of the cytopharyngeal basket of the ciliate Pseudomicrothorax dubius. Differentiation 14:147–158

    Article  Google Scholar 

  • Ianora A, Mazzocchi MG, Carlo BS (1987) Impact of parasitism and intersexuality on Mediterranean populations of Paracalanus parvus (Copepoda: Calanoida). Dis Aquat Org 3:29–36

    Article  Google Scholar 

  • Johnson CA III, Bradbury PC (1976) Observations on the occurrence of the parasitic ciliate Synophrya in decapods in coastal waters off the southeastern United States. J Protozool 23:252–256

    Article  Google Scholar 

  • Kimmerer WJ, McKinnon DA (1990) High mortality in a copepod population caused by a parasitic dinoflagellate. Mar Biol 107:449–452

    Article  Google Scholar 

  • Kudo RR (1966) Protozoology. Thomas, Springfield, 1188pp

    Google Scholar 

  • Landers SC (1986) Studies of the phoront of Hyalophysa chattoni (Ciliophora, Apostomatida) encysted on grass shrimp. J Protozool 33:546–552

    Article  Google Scholar 

  • Landers SC (1991a) Trichocyst digestion in Hyalophysa chattoni (Ciliophora: Apostomatida). Trans Am Microsc Soc 110:118–127

    Article  Google Scholar 

  • Landers SC (1991b) The fine structure of secretion in Hyalophysa chattoni: formation of the attachment peduncle and the chitinous phoretic cyst wall. J Protozool 38:148–157

    Article  CAS  PubMed  Google Scholar 

  • Landers SC (2004) Exuviotrophic apostomes ciliates from crustaceans of St. Andrew Bay, Florida, and a description of Gymnodinioides kozloffi n. sp. J Eukaryot Microbiol 51:644–650

    Article  PubMed  Google Scholar 

  • Landers SC (2010) The fine structure of the hypertrophont of the parasitic apostome Synophrya (Ciliophora, Apostomatida). Eur J Protistol 46:171–179

    Article  PubMed  Google Scholar 

  • Landers SC, Confusione A, Defee D (1996) Hyalophysa bradburyae sp. n., a new species of apostome ciliate from the grass shrimp Palaemonetes kadiakensis. Eur J Protistol 32:372–379

    Article  Google Scholar 

  • Landers SC, Treadaway RA, Johnson JW, Luckie RN (2001) Food plaquette digestion in the ciliated protozoan Hyalophysa chattoni. Invertebr Biol 120:97–103

    Article  Google Scholar 

  • Landers SC, Gómez-Gutiérrez J, Peterson WT (2007) The fine structure of the phoront of Gymnodinioides pacifica, a ciliated protozoan (Ciliophora, Apostomatida) from euphausiids of the Northeastern Pacific. Eur J Protistol 43:239–249

    Article  PubMed  Google Scholar 

  • McKanna JA (1973) Cyclic membrane flow in the ingestive-digestive system of peritrich protozoans. II Cup-shaped coated vesicles. J Cell Sci 13:677–686

    CAS  PubMed  Google Scholar 

  • Miyashita Y (1933) Studies on a freshwater foettingeriid ciliate, Hyalospira caridinae n g n sp. Jap J Zool 4:439–460

    Google Scholar 

  • Ohtsuka S, Boxshall GA (2004) A new species of the deep-sea copepod genus Scutogerulus (Calanoida: Aritetellidae) from the hyperbenthic waters of Okinawa, Japan. Syst Biodivers 2:49–55

    Article  Google Scholar 

  • Ohtsuka S, Boxshall GA, Fosshagen A (2003) A new species of Neoscolecithrix (Crustacea: Copepoda: Calanoida) from off Okinawa, southwestern Japan, with comments on the genetic position in the superfamily Clausocalanoidea. Bull Natn Sci Mus, Tokyo, Ser A 29:53–63

    Google Scholar 

  • Ohtsuka S, Hora M, Suzaki T, Arikawa M, Omura G, Yamada K (2004) Morphology and host-specificity of the apostome ciliate Vampyrophrya pelagica infecting pelagic copepods in the Seto Inland Sea, Japan. Mar Ecol Prog Ser 282:129–142

    Article  Google Scholar 

  • Ohtsuka S, Hanamura Y, Harada S, Shimomura M (2007) Recent advances in studies of parasites on mysid crustaceans. Bull Plankton Soc Jpn 53:37–44 (in Japanese with English abstract)

    Google Scholar 

  • Ohtsuka S, Horiguchi T, Hamamura Y, Yamaguchi A, Shimomura M, Ishiguro K, Hanaoka H, Suzaki T, Ohtani S (2010) Symbiosis of planktonic copepods and mysids with epibionts and parasites in the North Pacific: diversity and interactions. Crustacean Mongr 15:1–14

    Google Scholar 

  • Peck RK, Hausmann K (1980) Primary lysosomes of the ciliate Pseudomicrothorax dubius: cytochemical identification and role in phagocytosis. J Protozool 27:401–409

    Article  Google Scholar 

  • Puytorac PD, Grain J (1975) Etude de la tomitogenèse et l’ultrastructure de Collinia orchestiae, cilié apostome sanguicole, endoparasite du crustacé Orchestia gammarella Pallas. Protistologica 11:61–74

    Google Scholar 

  • Rohdes K (2005) Marine parasitology. CSIRO Publishing, Collingwood, 565pp

    Google Scholar 

  • Sewell RBS (1951) The epibionts and parasites of the planktonic Copepoda of the Arabian Sea. Sci Rep John Murray Exped 9:255–394

    Google Scholar 

  • Shields JD (1994) The parasitic dinoflagellates of marine crustaceans. Ann Rew Fish Dis 4:241–271

    Article  Google Scholar 

  • Skovgaad A (2014) Dirty tricks in the plankton: diversity and role of marine parasitic protists. Acta Protozool 53:51–62

    Google Scholar 

  • Small EB, Lynn DH (1985) Phylum Ciliophora DOFLEIN, 1901. In: Lee JJ, Hunter SH, Bovee EC (eds) An illustrated guide to the protozoa. Society of Protozoologists, Lawrence, pp 393–575

    Google Scholar 

  • Trager W (1957) Excystation of apostomes ciliates in relation to molting of their crustacean hosts. Biol Bull 112:132–136

    Article  Google Scholar 

Download references

Acknowledgments

We wish to express our sincere thanks to Dr. Fabrice Not (Roscoff Biology Station) for critical reading of the early draft. Thanks are due to Miss M. Hora and K. Yamada for their assistance with electron microscopic observations on V. pelagica, and to Mrs. Nicole Guyard (Roscoff Biology Station) for permission for our citation of the figures appearing in Chatton and Lwoff (1935). This study was partially supported by grants-in-aid from the Japan Society for the Promotion of Science (Nos. 20380110, 25304031).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Susumu Ohtsuka .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Japan

About this chapter

Cite this chapter

Ohtsuka, S., Suzaki, T., Kanazawa, A., Ando, M. (2015). Biology of Symbiotic Apostome Ciliates: Their Diversity and Importance in the Aquatic Ecosystems. In: Ohtsuka, S., Suzaki, T., Horiguchi, T., Suzuki, N., Not, F. (eds) Marine Protists. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55130-0_18

Download citation

Publish with us

Policies and ethics