Skip to main content Skip to main navigation menu Skip to site footer
Responsive image
Issue: Vol. 4168 No. 3: 16 Sept. 2016
Type: Article
Published: 2016-09-16
DOI: 10.11646/zootaxa.4168.3.5
Page range: 525–540
Abstract views: 117
PDF downloaded: 92

Occurrence of Epistylis anastatica (Linnaeus, 1767) (Ciliophora: Peritrichia) on Mesocyclops isabellae Dussart & Fernando (Crustacea: Copepoda: Cyclopoida) in India, with an annotated checklist of species of Epistylis reported as Epibionts of Cyclopoid Copepods and resources for their identification

Department of Biology, North Carolina Central University, Durham 27707 U.S.A.
Department of Biology, Indian School of Learning, I.S.M. Annexe, P.O. – I. S. M., Dhanbad 826004, Jharkhand, India.
Department of Zoology, Faculty of Biology, Pnta 9, Complutense University, 28040 Madrid, Spain.
Crustacea peritrich ciliate freshwater plankton biogeography taxonomy predator-prey relationship

Abstract

The colonial peritrich ciliate Epistylis anastatica (Linnaeus, 1767) was discovered living as an epibiont on Mesocyclops isabellae Dussart & Fernando, 1988 collected from a pond in Andhra Pradesh state, India. This is the first report of Epistylis on this host, and a description of its morphological characteristics is provided. The biomass of colonies of E. anastatica relative to that of their hosts was relatively high, being greater than that of the host in some cases (8.11 mm3 vs. 1.14 mm3 or less), and this epibiotic burden has the potential to have an impact on the host’s activities. Relationships between epibiotic peritrichs and microcrustaceans like cyclopoid copepods may be much more complex than previously supposed and merit more thorough investigation. Species of Epistylis are commonly found on cyclopoid copepods, but resources for taxonomic identification are limited and scattered; therefore, an annotated checklist of all species reported from cyclopoid copepods and a summary of the diagnostic characteristics of each one is provided as an aid to investigators. Some records of Epistylis spp. from cyclopoid copepods that are accompanied by documentary evidence are misidentifications, raising the suspicion that many other undocumented records also may be erroneous; therefore, it is suggested that authors provide supplementary descriptions and figures.

 

References

  1. Anderson, R.S. (1970) Predator–prey relationships and predation rates for crustacean zooplankters from some lakes in western Canada. Canadian Journal of Zoology, 48, 1229–1240.
    http://dx.doi.org/10.1139/z70-212

    Andrade, A. & López, C. (2005) Predatory interactions between Thermocyclops decipiens Kiefer (Cyclopoida: Copepoda) and two small cladocerans: behavior and prey post-encounter vulnerability. Annales de Limnologie - International Journal of Limnology, 41 (3), 153–159.

    http://dx.doi.org/10.1051/limn:20054130153

    Andr, E. (1912) Infusoires. Catalogue de Invertébrés de la Suisse, 6, 1–227.

    Barea-Arco, J., Pérez-Martínez, C. & Morales-Baquero, R. (2001) Evidence of a mutualistic relationship between an algal epibiont and its host, Daphnia pulicaria. Limnology and Oceanography, 46 (4), 871–881.

    http://dx.doi.org/10.4319/lo.2001.46.4.0871

    Bickel, S.L., Tang, K.W. & Grossart, H.P. (2012) Ciliate epibionts associated with crustacean zooplankton in German lakes: distribution, motility, and bacterivory. Frontiers in Microbiology, 3, 243.

    http://dx.doi.org/10.3389/fmicb.2012.00243

    Bozkurt, A. & Genc, E. (2009) First record of the epibiont protozoan Epistylis sp. on zooplankton (Copepoda, Cladocera, and Rotifera) from the Asi River, Turkey. Crustaceana, 82 (5), 515–530.

    http://dx.doi.org/10.1163/156854009x407687

    Burris, Z.P. & Dam, H.G. (2014) Deleterious effects of the ciliate epibiont Zoothamnium sp. on fitness of the copepod Acartia tonsa. Journal of Plankton Research, 36 (3), 788–799.

    http://dx.doi.org/10.1093/plankt/fbt137

    Canella, M.F. (1954) Ricerche sulla microfauna delle acque interne Ferraresi. Introduzione allo studio dei ciliati e dei rotiferi. Pubblicazioni civico Museo di Storia Naturale di Ferrara, 4, 1–154.

    http://dx.doi.org/10.1086/402007

    Clamp, J.C. (1973) Observations on the host-symbiont relationships of Lagenophrys lunatus Imamura. Journal of Protozoology, 20 (5), 558–561.
    http://dx.doi.org/10.1111/j.1550-7408.1973.tb03572.x

    Claparède, E. & Lachmann, J. (1858) Études sur les infusoires et les rhizopodes. Mémoires de l’Institut National Genevois, 5, 1–260.
    http://dx.doi.org/10.5962/bhl.title.29753

    Daday, E. (1905) Untersuchungen über die Süßwassermikrofauna Paraguays. Mit einem Anhang von W.Michaelsen. Zoologica, 44, 1–374.
    http://dx.doi.org/10.5962/bhl.title.11316

    Daday, E. (1910) Untersuchungen über die Süsswasser-Mikrofauna Deutsch-Ost-Afrikas. Zoologica, 59, 1–314.

    http://dx.doi.org/10.5962/bhl.title.11655

    Ehrenberg, C. (1838) Die Infusionsthiere als vollkommene Organismen. L. Voss, Leipzig, 548 pp.

    Engelmann, T.W. (1862) Zur Naturgeschichte der Infusionsthiere. Zeitschrift für wissenschaftliche Zoologie, 11 (4), 347–393.

    Fauré-Frémiet, E. (1906) Note sur quelques formes nouvelles de Vorticellidae. Zoologischer Anzeiger, 29 (13), 430–432.

    Fernandez-Leborans, G. & Tato-Porto, M.L. (2000) A review of the species of protozoan epibionts on crustaceans. I. Peritrich ciliates. Crustaceana, 73 (6), 643–683.

    http://dx.doi.org/10.1163/156854000504705

    Foissner, W. (1992a) Protargol Methods. In: Lee, J.J. & Soldo, A.T. (Eds.), Protocols in Protozoology. Society of Protozoologists, Lawrence, KS, pp. C-6.1–6.7.

    Foissner, W. (1992b) The “Dry” Silver Nitrate Method. In: Lee, J.J. & Soldo, A.T. (Eds.), Protocols in Protozoology. Society of Protozoologists, Lawrence, KS, pp. C-11.1–11.3.

    Foissner W. & Schiffman, J. (1975) Biometrische und morphologische Untersuchungen über die Variabilität von argyrophilen Strukturen bei peritrichen Ciliaten. Protistologica, 11, 415–428.

    Foissner, W., Berger, H. & Kohmann, F. (1992) Taxonomische und ökologische Revision der Ciliaten des Saprobiensystems–Band II: Peritrichia, Heterotrichida, Odontostomatida. Bayerisches Landesamt für Wasserwirtschaft, Heft 5/92, 1–502.

    Foissner, W., Berger, H. & Schaumburg, J. (1999) Identification and Ecology of Limnetic Plankton Ciliates. Bayerisches Landesamt für Wasserwirtschaft, Heft 3/99, 1–793.

    Franc, F. (1897) 1. Section. Protozoen. Resultate der wissenschaftlichen Erforschung des Balatonsees, 2, 1–64.

    Fryer, G. (1957) The food of some freshwater cyclopoid copepods and its ecological significance. Journal of Animal Ecology, 26 (2), 263–286.

    http://dx.doi.org/10.2307/1747

    Gilbert J.J. & Schröder T. (2003) The ciliate epibiont Epistylis pygmaeum: selection for zooplankton hosts, reproduction and effect on two rotifers. Freshwater Biology, 48 (5), 878–893.

    http://dx.doi.org/10.1046/j.1365-2427.2003.01059.x

    Green, J. (1960) Crustacea in Lake Ohrid, with special reference to their parasites and epibionts. Zbornik na Rabotite Hidrobioloski Zavod Ohrid, 8, 1–11.

    Green, J. (1974) Parasites and epibionts of Cladocera. Transactions of the Zoological Society of London, 32 (6), 417–515.

    http://dx.doi.org/10.1111/j.1096-3642.1974.tb00031.x

    Haempel, O. (1918) Zur Kenntniss einiger Alpenseen, mit besonderer Berücksichtigung ihrer biologischen und Fischerei–Verhältnisse. International Revue der gesamten Hydrobiologie und Hydrographie, 8 (3), 225–306.

    http://dx.doi.org/10.1002/iroh.19180080302

    Haney, J.F. (2013) An-Image-based Key to the Zooplankton of North America, version 5.0 released 2013. University of New Hampshire Center for Freshwater Biology. Available from: http://cfb.unh.edu/cfbkey/html/index.html (accessed 13 August 2016)

    Henebry, M.S. & Ridgeway, B.T. (1979) Epizoic ciliated protozoa of planktonic copepods and cladocerans and their possible use as indicators of organic water pollution. Transactions of the American Microscopical Society, 98 (4), 495–508.

    http://dx.doi.org/10.2307/3225899

    Herman, S.S. & Mihursky, J.A. (1964) Infestation of the copepod Acartia tonsa with the stalked ciliate Zoothamnium. Science, 146 (3643), 543–544.

    http://dx.doi.org/10.1126/science.146.3643.543

    Heuscher, H. (1917) Das Zooplankton des Zürichsees. Archiv für Hydrobiologie und Planktonkunde, 11, 1–81.

    Hofer, B. (1899) Die Verbreitung der Tierwelt un Bodensee nebst vergleichenden Untersuchungen im einigen andern Süsswasserbecken: Der Bodensee-Forschungen zehnter Abschnitt. Joh. Thom. Stettner, Lindau, 64 pp.

    Hołyńska, M., Reid, J.W. & Ueda, H. (2003) Genus Mesocyclops Sars, 1914. In: Ueda, H. & Reid, J.W. (Eds.), Copepoda: Cyclopoida. Genera Mesocyclops and Thermocyclops. Guides to the identification of the Microinvertebrates of the Continental Waters of the World 20. Backhuys Publishers, Leiden, pp.12–213.

    Hudson, P.L. & Lesko, L.T. (2003) Free-living and Parasitic Copepods of the Laurentian Great Lakes: Keys and Details on Individual Species. Ann Arbor, MI: Great Lakes Science Center Home Page. Accessed from: http://www.glsc.usgs.gov/greatlakescopepods/MainMenu.php (accessed14 July 2014)

    Imhof, O.E. (1884) Resultate meiner Studien über die Pelagische Fauna kleinerer und grösserer Süsswasserbecken der Schweiz. Zeitschrift für wissenschaftliche Zoologie, 40 (1), 154–178.

    Kahl A. (1935) Urtiere oder Protozoa I: Wimpertiere oder Ciliata (Infusoria), 4. Peritricha und Chonotricha. In: Dahl, F. (Ed.), Die Tierwelt Deutschlands. 30 Teil. G. Fischer, Jena, pp. 651–805.

    Kankaala, P. & Eloranta, P. (1987) Epizoic ciliates (Vorticella sp.) compete for food with their host Daphnia longispina in a small polyhumic lake. Oecologia, 73 (2), 203–206.

    http://dx.doi.org/10.1007/bf00377508

    Keiser A. (1921) Die sessilen peritrichen Infusorien und Suctorien von Basel und Umgebung. Revue Suisse de Zoologie, 28 (12), 221–341.

    Kellicott, D.S. (1883) On some Infusoria found on the cray fish. Proceedings of the American Society of Microscopists, 5, 105–111.

    http://dx.doi.org/10.2307/3220341

    Kent, W.S. (1881) A Manual of the Infusoria. Volume II. David Bogue, London, 298 pp.

    Kerfoot, W.C. (1978) Combat between predatory copepods and their prey: Cyclops, Epischura, and Bosmina. Limnology and Oceanography, 23 (6), 1089–1102.

    http://dx.doi.org/10.4319/lo.1978.23.6.1089

    Laird, M. (1960) Malayan Protozoa 4. Epistylis caldwelli n. sp. (Ciliata: Peritricha), from freshwater neuston. Journal of Protozoology, 7 (4), 303–306.

    http://dx.doi.org/10.1111/j.1550-7408.1960.tb05973.x

    Li, J. & Li, H. (1979) Species specific factors affecting predator-prey interactions of the copepod Acanthocyclops vernalis with its natural prey. Limnology and Oceanography, 24 (4), 613–626.

    http://dx.doi.org/10.4319/lo.1979.24.4.0613

    Lom, J. (1964) The morphology and morphogenesis of the buccal ciliary organelles in some peritrichous ciliates. Archiv für Protistenkunde, 107, 131–162.

    López, C., Ochoa, E., Páez, R. & Theis, S. (1998) Epizoans on a tropical freshwater crustacean assemblage. Marine and Freshwater Research, 49 (3), 271–276.
    http://dx.doi.org/10.1071/mf96037

    Marten, G.G. & Reid, J.W. (2007) Cyclopoid Copepods. In: Floore, T.G. (Ed.), Biorational Control of Mosquitoes. Bulletin No.7, American Mosquito Control Association, Mount Laurel, NJ, pp. 65–92.

    Matthes, D. (1950) Beitrag zur Peritrichenfauna der Umgebung Erlangens. Zoologische Jahrbücher. Abteilung für Systematik, Geographie und Biologie der Tiere, 79, 437–448.

    Matthes, D. (1974) Die Wimpertierwelt unserer Flusskrebse. I. Epistylis niagarae und ihre Parasiten. Mikrokosmos, 63, 13–17.

    Matthes, D. & Guhl, W. (1973) Sessile Ciliaten der Flusskrebse. Protistologica, 9 (4), 459–470.

    Matthes, D. & Scheubel, J. (1970) Epistylis galea, Ehrenberg, ein polyrnorphes Peritrich. Archiv für Protistenkunde, 112, 30–64.

    Mermod. (1914) Recherches sur la faune infusorienne des tourbières et des eaux voisines de Sainte-Croix (Jura vaudois). Revue Suisse de Zoologie, 22 (3), 31–114.

    Miao, W., Yu, Y.-H. & Shen, Y.-F. (2001) Phylogenetic relationships of the subclass Peritrichia (Oligohymenophorea, Ciliophora) with emphasis on the genus Epistylis, inferred from small subunit rRNA gene sequences. Journal of Eukaryotic Microbiology, 48 (5), 583–587.

    http://dx.doi.org/10.1111/j.1550-7408.2001.tb00194.x

    Miao, W., Fen, W.-S., Yu, Y.-H., Zhang, X.-Y. & Shen, Y.-F. (2004) Phylogenetic relationships of the subclass Peritrichia (Oligohymenophorea, Ciliophora) inferred from small subunit rRNA gene sequences. Journal of Eukaryotic Microbiology, 51 (2), 180–186.
    http://dx.doi.org/10.1111/j.1550-7408.2004.tb00543.x

    Monard, A. (1919) La faune profonde du lac de Neuchâtel. Bulletin de la Société Neuchâteloise des Sciences Naturelles, 44, 65–235.

    Nenninger, U. (1948) Die Peritrichen der Umgebung von Erlangen mit besonderer Berücksichtigung ihrer Wirtsspezifität. Zoologische Jahrbücher Abteilung für Systematik Oekologie und Geographie der Tiere, 77, 169–266.

    Perty, M. (1852) Zur Kenntniss kleinster Lebensformen nach Bau, Funktionen, Systematik, mit Specialverzeichniss der in der Schweiz beobachteten. Jent & Reinert, Bern, 228 pp.

    Pritchard, A. (1852) A History of Infusorial Animacules, Living and Fossil. Whitaker and Co., London, 704 pp.

    Rajabunizal, K. & Ramanibai, R. (2011) Presence of an epibiont Epistylis niagarae (Protozoa, Ciliophora) on Mesocyclops aspericornis in Velachery Lake, Chennai, India. Journal of Biological Science, 11 (2), 189–195.

    http://dx.doi.org/10.3923/jbs.2011.189.195

    Regali-Seleghim, M.H. & Godinho, M.J.L. (2004) Peritrich epibiont protozoans in the zooplankton of a subtropical shallow aquatic ecosystem (Monjolinho Reservoir, Sao Carlos, Brazil). Journal of Plankton Research, 26 (5), 501–508.
    http://dx.doi.org/10.1093/plankt/fbh055

    Roberts, D. (2014) Ciliophora. Accessed from: http://ciliateguide.myspecies.info (accessed 11 July 2014)

    Roux, J. (1901) Faune infusorienne des eaux stagnantes des environs de Genève. Mémoires de l'Institut National Genevois, 19, 1–149.

    Saler, S. & Dörücü, M. (2008) The first observation of Epistylis niagarae on Cyclops vicinus Uljanin, 1875 living in Hazar Lake (Elazığ -Turkey). International Journal of Science & Technology, 3 (2), 161–163.

    Schneider, G. (1909) Der Obersee bei Reval. Archiv für Biontologie, 2, 1–192.

    Sommer, G. (1949) Die Peritrichen eines astatischen Gartenbeckens. Schweizerische Zeitschrift für Hydrologie, 11 (3), 608–617.

    http://dx.doi.org/10.1007/bf02503371

    Sommer, G. (1951) Die peritrichen Ciliaten des Grossen Plöner Sees. Archiv für Hydrobiologie, 44, 349–440.

    Sprague, V. & Couch, J. (1971) An annotated list of protozoan parasites, hyperparasites, and commensals of decapod crustacea. Journal of Protozoology, 18 (3), 526–537.

    http://dx.doi.org/10.1111/j.1550-7408.1971.tb03367.x

    Šrámek-Hušek, R. (1948) Ciliata–Peritricha našich řek (příspěvky k poznání československých nálevníků III). Časopis Národního Musea, 117, 167–183.

    Stein, F. (1854) Die Infusionsthiere auf ihre Entwickelungsgeschichte untersucht. W, Engelmann, Leipzig, 206 pp.

    http://dx.doi.org/10.5962/bhl.title.14880

    Stiller, J. (1931) Über Kolonienbildung bei Rhabdostyla ovum Kent. Acta Littererum ac. Scientiarum Regiae Universitatas Hungaricae Francisco-Josephina, Acta Biologica, Szeged, Sectio A. Biologica, 2, 37–40.

    Stiller, J. (1942) Einige Gewässer der Umgebung von Szeged und ihre Peritrichenfauna. Archiv für Hydrobiologie, 38, 313–435.

    Stloukal, E. (1999) Nlezy epibiontných nálevníkov z čeľade Epistylididae (Ciliophora: Peritrichia) na západnom Slovensku. Folia Faunistica Slovaca, 4, 15–24.

    Thorp, J.H. & Covich, A.P. (Eds.) (2010) Ecology and Classification of North American Freshwater Invertebrates. 3rd Edition. Academic Press, London, 1021 pp.

    Utz, L.R.P., Simão, T.L.L., Safi, L.S.L. &. Eizirik, E. (2010) Expanded phylogenetic representation of genera Opercularia and Epistylis sheds light on the evolution and higher-level taxonomy of peritrich ciliates (Ciliophora: Peritrichia). Journal of Eukaryotic Microbiology, 57 (5), 2010, 415–420.

    http://dx.doi.org/10.1111/j.1550-7408.2010.00497.x

    Van As, J.G. & Viljoen, S. (1984) A taxonomic study of sessile peritrichs (Ciliophora: Peritricha) associated with crustacean fish ectoparasites in South Africa. South African Journal of Zoology, 19 (4), 275–279.
    http://dx.doi.org/10.1080/02541858.1984.11447893

    Walter, T.C. & Boxshall, G. (2014) World of Copepods database. Abailable from: http://www.marinespecies.org/copepoda (accessed 8 July 2014)

    Wang C.C. & Nie D. (1933) Report on the rare and new species of fresh-water infusoria, part I. Contributions of the Biological Laboratory of the Scientific Society of China, Zoological Series, 10, 1–99.

    Willey, R.L. & Threlkeld, S.T. (1993) Organization of crustacean epizoan communities in a chain of subalpine ponds. Limnology and Oceanography, 38 (3), 623–627.

    http://dx.doi.org/10.4319/lo.1993.38.3.0623

    Willey, R.L., Cantrell, P.A. & Threlkeld, S.T. (1990) Epibiotic euglenoid flagellates increase the susceptibility of some zooplankton to fish predation. Limnology and Oceanography, 35 (4), 952–959.
    http://dx.doi.org/10.4319/lo.1990.35.4.0952

    Xie, P., Sanderson, B., Frost, T. & Magnuson, J.J. (2001) Manipulation of host density affects infestation of a peritrich ciliate (Epistylis lacustris) on a calanoid copepod (Leptodiaptomus minutus) in Crystal Lake, Wisconsin, USA. Journal of Freshwater Ecology, 16 (4), 557–564.
    http://dx.doi.org/10.1080/02705060.2001.9663847

    Xu, Z. (1993) The infection of Moina macrocopa by a colonial peritrich, Epistylis daphniae, and its effects on the host. Freshwater Biology, 30 (1), 181–186.
    http://dx.doi.org/10.1111/j.1365-2427.1993.tb00798.x

    Xu, Z. & Burns, C.W. (1991) Effects of the epizoic ciliate, Epistylis daphniae, on growth, reproduction and mortality of Boeckella triarticulata (Thomson) (Copepoda: Calanoida). Hydrobiologia, 209 (3), 183–189.
    http://dx.doi.org/10.1007/bf00015341