Abstract
This study presents a light microscopy observation on the life cycle of the prostomatid ciliate, Holophrya teres. We were able to make distinctions between its reproduction and starvation phases. Within these phases, we observed the following stages, namely the trophont, protomont and tomont, as well as reproductive (tomites), temporary and resting cysts. Additionally, we also described two types of active specimens after the excystation process, especially from the reproductive cyst (theront) and from the resting cyst. The main differences between these two specimens were in the shape and size of the cell, the rate of the regeneration, and the speed of the excystation process itself. To date, the life cycle of the genus Holophrya has only been known synonymously with the general model of the life cycle of the genus Prorodon. However, the characteristics of these two cycles are not identical at all. For this reason, we also focused on an overview of currently available data, and we have uncovered several specifics of the life cycle of H. teres for the first time. This study has revealed that the life cycles of limnic ciliates are somewhat more diversified than the life cycles of terrestrial groups of ciliates.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aescht E (2019) The world ciliate catalog. ITIS catalogue of life, 2018 annual checklist. Naturalis, Leiden, the Netherlands. http://www.catalogueoflife.org/col/details/species/id/1ad432f0e8a86b2d7dc30f3c2c82b276. Accessed 12 Feb 2019
Benčaťová S, Tirjaková E (2017) Prvonález druhu Bresslauides terricola (Foissner, 1987) Foissner,1993 (Ciliophora, Colpodea) na Slovensku – cystické štádiá, en- a excystácia. Folia Faun Slov 22:31–40
Cadetti L, Marroni F, Marongoni R, Kuhlmann HW, Gioffré D, Colombetti G (2000) Phototaxis in the ciliated protozoan Ophryoglena flava: dose-effect curves and action spectrum determination. J Photochem Photobiol B Biol 57:41–50. https://doi.org/10.1016/S1011-1344(00)00075-0
Canella MF, Rocchi-Canella I (1977) Biologie des Ophryoglenina (ciliés hyménostomes histophages). Annali dell’Università die Ferrata, Nuova Serie, Sez. III, 3 (Suppl.2), Università die Ferrata, Italy:1–510. https://doi.org/10.1086/410195
Clamp JC, Bradbury PC, Strüder-Kypke MC, Lynn DH (2008) Phylogenetic postition of the apostome ciliates (Phylum Ciliophora, Subclass Apostomatia) tested using small subunit rRNA gene sequences. Denisia 23:395–402
Colorni A (1985) Aspects of the biology of Cryptocaryon irritans, and hyposalinity as control measure in cultured gilt-head sea bream Sparus aurata. Dis Aquat Org 1:19–22. https://doi.org/10.3354/dao001019
Colorni A, Burgess P (1997) Cryptocaryon irritans Brown 1951, the cause of ‘white spot disease’ in marine fish: an update. Aquarium Sci Conserv 4:217–238. https://doi.org/10.1023/A:1018360323287
Colorni A, Diamant A (1993) Ultrastructural features of Cryptocaryon irritans, a ciliate parasite of marine fish. Eur J Protistol 29:425–434. https://doi.org/10.1016/S0932-4739(11)80405-0
Corliss JO, Esser SC (1974) Comments on the role of the resting cyst in the life cycle and survival of the free-living protozoa. Trans Am Microsc Soc 93:578–593. https://doi.org/10.2307/3225158
Diggles BJ (1997) Some information on the morphology of Cryptocaryon irritans from south-East Queensland, Australia. Eur J Protistol 33:200–210. https://doi.org/10.1016/S0932-4739(97)80037-5
Dragesco J (1960) Ciliés mésopsammiques littoraux. Systématique, morphologie, écologie. Des Travaux de la Station Biologique de Roscoff 12:1–356
Esteban GF, Finlay BJ (1996) Morphology and ecology of the cosmopolitan ciliate Prorodon viridis. Arch Protistenkd 147:181–188. https://doi.org/10.1016/S0003-9365(96)80032-7
Foissner W (1993) Colpodea (Ciliophora). Protozoenfauna 4:1–798
Foissner W, Berger H, Kohmann F (1994) Taxonomische und ökologische revision der Ciliaten des Saprobiensystems - band III: Hymenostomata, Prostomatida, Nassulida. Informationsber Bayer Landesamt Wasserwirtsch 1/, vol 94, pp 1–540
Genoveva FE, Finlay BL (1996) Morphology and ecology of the cosmopolitan ciliate Prorodon viridis. Arch Protistenkd 147:181–188. https://doi.org/10.1016/S0003-9365(96)80032-7
Hiller S, Bardelle CHF (1988) Prorodon aklitolophon n. spec. and the “dorsal brush” as a character to identify certain subgroups in the genus Prorodon. Arch Protistenkd 136:213–236. https://doi.org/10.1016/S0003-9365(88)80022-8
Kuhlmann HW (1993) Life cycle dependent phototactic orientation in Ophryoglena catenula. Eur J Protistol 29:344–352. https://doi.org/10.1016/S0932-4739(11)80376-7
Leipe D (1989) Prorodon spirogyrophagus nov. spec. (Ciliophora, Prostomatea): morphology, infraciliature and food-uptake. Eur J Protistol 24:392–401. https://doi.org/10.1016/S0932-4739(89)80009-4
Lom L, Dyková I (1992) Protozoan parasites of fishes. Elsevier, Amsterdam. https://doi.org/10.2307/3283600
Lynn DH (2008) The ciliated protoza: characterization, classification, and guide to the literature. Springer, Guelph. https://doi.org/10.1007/978-1-4020-8239-9
Ma R, Fan X, Yin F, Ni B, Gu F (2017) Ultrastructural features of the tomont of Cryptocaryon irritans (Ciliophora: Protostomatea), a parasitic ciliate of marine fishes. Parasitology 144:720–729. https://doi.org/10.1017/S0031182016002651
Molloy DP, Lynn DH, Giamberini L (2005) Ophryoglena hemophaga n. sp. (Ciliophora: Ophryoglenidae): a parasite of the digestive gland of zebra mussels Dreissena polymorpha. Dis Aquat Org 65:237–243. https://doi.org/10.3354/dao065237
Mugard H (1948) Contribution à l ´études des infusoires hyménostomes histiophages. Ann Sci Nat Zool 11:171–269
Savoie A (1962a) Ophryoglena mugardi n. sp. (Ciliata Hymenostomatida Ophryoglenidae). Cycles de reproduction. J Eukaryot Microbiol 9:296–303. https://doi.org/10.1111/j.15507408.1962.tb02624.x
Savoie A (1962b) Ophryoglena faurei n. sp. (Ciliata Hymenostomatida Ophryoglenidae). Cycles de reproduction. J Eukaryot Microbiol 9:427–434. https://doi.org/10.1111/j.15507408.1962.tb02648.x
Tannreuther GW (1926) Life history of Prorodon griseus. Biol Bull 51:303–320. https://doi.org/10.2307/1537005
Verni F, Rosati G (2011) Resting cysts: a survival strategy in Protozoa Ciliophora. Ital J Zool 78:134–145. https://doi.org/10.1080/11250003.2011.560579
Yambot AV, Song IL, Sung HH (2003) Characterization of Cryptocaryon irritans, a parasite isolated from marine fishes in Taiwan. Dis Aquat Org 54:147–156. https://doi.org/10.3354/dao054147
Yin F, Sun P, Wang J, Gao Q (2016) Transcriptome analysis of dormant tomonts of the marine fish ectoparasitic ciliate Cryptocaryon irritans under low temperature. Parasit Vectors 9:280–291. https://doi.org/10.1186/s13071-016-1550-1
Acknowledgments
We would like to thank Michal Pindura for help with graphic design images and Mike Sabo for English correction. Financial support was provided by the Slovak Scientific Grant Agency (Project No. 1/0114/16).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethical approval
This article does not contain any studies with animals performed by any of the authors.
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Benčaťová, S., Križanová, F. & Tirjaková, E. Current knowledge of the starvation and reproduction stages of the limnic species Holophrya teres (Ciliophora: Prostomatea). Biologia 75, 413–422 (2020). https://doi.org/10.2478/s11756-019-00311-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.2478/s11756-019-00311-1