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 .
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Allen RD (1974) Food vacuole membrane growth with microtubule-associated membrane transport in Paramecium. J Cell Biol 63:904–922
Bradbury PC (1966a) The life cycle and morphology of the apostomatous ciliate, Hyalophysa chattoni n. g., n. sp. J Protozool 13:209–225
Bradbury PC (1966b) The fine structure of the mature tomite of Hyalophysa chattoni. J Protozool 13:591–607
Bradbury PC (1973) The fine structure of the cytostome of the apostomatous ciliate Hyalophysa chattoni. J Protozool 20:405–414
Bradbury PC (1974a) The fine structure of the phoront of the apostomatous ciliates, Hyalophysa chattoni. J Protozool 21:112–120
Bradbury PC (1974b) Stored membranes associated with feeding in apostome trophonts with different diets. Protistologica 10:533–542
Bradbury PC (1989) Evidence for hymenostome affinities in an apostome ciliate. J Protozool 36:95–103
Bradbury PC (1996) Parasitic ciliates. In: Hausmann K, Bradbury PC (eds) Ciliates. Gustav Fisher, Stuttgart, pp 463–477
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
Bradbury PC, Trager W (1967a) Metamorphosis from the phoront to the trophont in Hyalophysa. J Protozool 14:210–213
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
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
Bradbury PC, Deroux G, Campillo A (1987) The feeding apparatus of a chitinivorous ciliate. Tissue Cell 19:351–363
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
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
Bush AO, Fernández JC, Esch GW, Seed JR (2001) Parasitism: the diversity and ecology of animal parasites. Cambridge University Press, Cambridge, 566pp
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
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
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
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
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
Corliss JO (1979) The ciliated protozoa: characterization, classification, and guide to the literature, 2nd edn. Pergamon Press, London/New York
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
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
Gómez-Gutiérrez J, Peterson WT, Robertis AD, Brodeur RD (2003) Mass mortality of krill caused by parasitoid ciliates. Science 301:339
Gómez-Gutiérrez J, Strüder-Kypke MC, Lynn DH, Shaw TC, Aguilar-Méndex MJ, López-Corés A, MartÃnez-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
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
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
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
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
Hausmann K, Peck RK (1979) The mode of function of the cytopharyngeal basket of the ciliate Pseudomicrothorax dubius. Differentiation 14:147–158
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
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
Kimmerer WJ, McKinnon DA (1990) High mortality in a copepod population caused by a parasitic dinoflagellate. Mar Biol 107:449–452
Kudo RR (1966) Protozoology. Thomas, Springfield, 1188pp
Landers SC (1986) Studies of the phoront of Hyalophysa chattoni (Ciliophora, Apostomatida) encysted on grass shrimp. J Protozool 33:546–552
Landers SC (1991a) Trichocyst digestion in Hyalophysa chattoni (Ciliophora: Apostomatida). Trans Am Microsc Soc 110:118–127
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
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
Landers SC (2010) The fine structure of the hypertrophont of the parasitic apostome Synophrya (Ciliophora, Apostomatida). Eur J Protistol 46:171–179
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
Landers SC, Treadaway RA, Johnson JW, Luckie RN (2001) Food plaquette digestion in the ciliated protozoan Hyalophysa chattoni. Invertebr Biol 120:97–103
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
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
Miyashita Y (1933) Studies on a freshwater foettingeriid ciliate, Hyalospira caridinae n g n sp. Jap J Zool 4:439–460
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
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
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
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)
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
Peck RK, Hausmann K (1980) Primary lysosomes of the ciliate Pseudomicrothorax dubius: cytochemical identification and role in phagocytosis. J Protozool 27:401–409
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
Rohdes K (2005) Marine parasitology. CSIRO Publishing, Collingwood, 565pp
Sewell RBS (1951) The epibionts and parasites of the planktonic Copepoda of the Arabian Sea. Sci Rep John Murray Exped 9:255–394
Shields JD (1994) The parasitic dinoflagellates of marine crustaceans. Ann Rew Fish Dis 4:241–271
Skovgaad A (2014) Dirty tricks in the plankton: diversity and role of marine parasitic protists. Acta Protozool 53:51–62
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
Trager W (1957) Excystation of apostomes ciliates in relation to molting of their crustacean hosts. Biol Bull 112:132–136
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
Corresponding author
Editor information
Editors and Affiliations
Rights 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
DOI: https://doi.org/10.1007/978-4-431-55130-0_18
Publisher Name: Springer, Tokyo
Print ISBN: 978-4-431-55129-4
Online ISBN: 978-4-431-55130-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)