Abstract
Epibiosis is a common phenomenon, found in different taxa of aquatic animals. This relationship could occur as hyperepibiosis, when a basibiont being also an epibiont, providing a stable substrate for the hypersymbiont. Here we reported a ciliate-bryozoan-crustacean hyperepibiosis in Mandovi River mouth, Goa, West coast of India. We provided descriptions and characterization of the crab Atergatis sp., serving as basibiont for the bryozoan Triticella pedicellata (Alder, 1857), in turn colonized with (hyperepibionts) the ciliates Paracineta saifulae (Mereschkowsky, 1877) and Cothurnia ceramicola Kahl, 1933. Paracineta saifulae and Cothurnia ceramicola are reported here for first time from the Indian Ocean.
References
Abello, P. & Corbera, J. (1996) Epibiont bryozoans (Bryozoa, Ctenostomatida) of the crab Goneplax rhomboides (Brachyura, Goneplacidae) off Ebro delta (western Mediterranean). Miscellàna Zoològica, 19 (2), 43–52.
Andersen, F.S. (1962) The Norway lobster in Faroe waters. Meddelelser Fra Danmarks Fiskeri-og Havundersogelsr, New Series, 3 (9), 265–326.
Ayres-Peres, L. & Mantelatto, F.L. (2010) Epibiont occurrence on gastropod shells used by the hermit crab Loxopagurus loxochelis (Anomura: Diogenidae) on the northern coast of São Paulo, Brazil. Zoologia, 27 (2), 222–227.
https://doi.org/10.1590/S1984-46702010000200010
Chatterjee, T. (1996) Ciliate infestation on the phytal Halacaridae (Acari) from the Kovalam beach, Kerala. Journal of the Bombay Natural History Society, 93, 107–108.
Chatterjee, T., Kotov, A. & Fernandez-Leborans, G. (2013a) A checklist of epibiotic ciliates (Peritricha, Suctoria) on the cladoceran crustacean. Biologia, 68 (3), 439–447.
https://doi.org/10.2478/s11756-013-0180-8
Chatterjee, T., Fernandez-Leborans, G. & Senna, A.R. (2013b) Ciliate epibionts on Melita petronio Senna et al., 2012 (Crustacea: Amphipoda) from Brazil. Cahiers de Biologie Marine, 54, 393–404.
Chatterjee, T., Fernandez-Leborans, G., Ramteke, D. & Ingole, B. (2013c) New records of epibiont ciliates (Ciliophora) from Indian coast with descriptions of six new species. Cahiers de Biologie Marine, 54, 143–159.
Chatterjee, T., Fernandez-Leborans, G. & Schizas, N. (2014) Report of Thecacineta calix (Ciliophora: Suctorea) as an epibiont of harpacticoid copepods from Caribbean mesophotic reefs. Caribbean Journal of Science, 48, 44–48. https://doi.org/10.18475/cjos.v48i1.a6
Chatterjee, T., Dovgal, I., Pesic, V. & Zawal, A. (2018) A checklist of epibiont suctorian and peritrich ciliates (Ciliophora) on halacarid and hydrachnid mites (Acari: Halacaridae & Hydrachnidia). Zootaxa, 4457 (3), 415–430.
https://doi.org/10.11646/zootaxa.4457.3.4
Chatterjee, T., Dovgal, I. & Fernandez-Leborans, G. (2019a) A checklist of suctorian epibiont ciliates (Ciliophora) found on meiobenthic marine nematodes. Journal of Natural History, 53 (33–34), 2133–2143.
https://doi.org/10.1080/00222933.2019.1692085
Chatterjee, T., Dovgal, I., Nanajkar, M. & Bogati, K. (2019b) Note on the genus Lecanophryella (Ciliophora: Suctorea) with description of a new species from west coast of India. Zootaxa, 4612 (4), 494–500.
https://doi.org/10.11646/zootaxa.4612.4.2
Chatterjee, T., Dovgal, I., Nanajkar, M. & Fernandes, V. (2019c) Report of epibiont ciliates (Cilliophora: Suctorea) on pelagic ostracods (Crustacea: Ostracoda) from the Arabian Sea. Zootaxa, 4695 (4), 378–384.
https://doi.org/10.11646/zootaxa.4695.4.5
Chatterjee, T., Dovgal, I. & Schizas, N.V. (2020a) Report of epibiont ciliates (Ciliophora) on harpacticoid copepods from Caribbean mesophotic reefs. Cahiers De Biologie Marine, 61 (1), 131–136.
https://doi.org/10.21411/CBM.A.E1C0E61
Chatterjee, T., Dovgal, I., Mayen-Estrada, R. & Fernandez-Leborans, G. (2020b) A checklist of ciliates (Ciliophora) inhabiting on ostracods (Crustacea, Ostracoda). Zootaxa, 4763 (1), 17–30.
https://doi.org/10.11646/zootaxa.4763.1.2
Chatterjee, T., Dovgal, I. & Nanajkar, M. (2020c) New records of epibiont ciliates Thecacineta urceolata and Acinetides gruberi (Ciliophora: Suctorea) from the Indian coast. Cahiers De Biologie Marine, 61, 355–360.
https://doi.org/10.21411/CBM.A.B713B863
Chatterjee, T., Dovgal, I. & Nanajkar, M. (2020d) A new species of the genus Corynophrya (Ciliophora: Suctorea) from the west coast of India, Arabian Sea. Cahiers De Biologie Marine, 61, 423–428.
Chatterjee, T., Dovgal, I. & Nanajkar, M. (2020e) Report of Ciliate epibionts (Ciliophora, Suctorea) on meiobenthic invertebrates from the Indian coast near Karwar, Karnataka. Protistology, 14 (2), 84–88.
https://doi.org/10.21685/1680-0826-2020-14-2-5
Clamp, J.C. (1973) Observations on the host-symbiont relationships of Lagenophrys lunatus Imamura. Journal of Protozoology, 20 (5), 558–561.
https://doi.org/10.1111/j.1550-7408.1973.tb03572.x
Clamp, J.C., Chatterjee, T. & Fernandez-Leborans, G. (2016) Occurrence of Epistylis anastatica (Linnaeus, 1767) (Ciliophora: Peritrichia) on Mesocyclopsis abellae 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. Zootaxa, 4168 (3), 525–540.
https://doi.org/10.11646/zootaxa.4168.3.5
Collin, B. (1912) Etudes monographiques sur les Acinetiens. 2. Morphologie, physiologie, systematique. Archives De Zoologie Expérimentale Et Générale, 51, 1–457.
Connell, J.H. & Keough, M.J. (1985) Disturbance and patch dynamics of subtidal marine animals on hard substrata. In: Pickett, S.T.A. & White, P.S. (Eds.), The Ecology of Natural disturbance and patch dynamics. Academic Press, San Diego, pp. 125–151.
https://doi.org/10.1016/B978-0-08-050495-7.50013-2
Corriero, G. & Pronzato, R. (1987) Epibiontic sponges on the bivalve Pinna nobilis. Marine Ecology Progress Series, 35, 75–82.
https://doi.org/10.3354/meps035075
Creen, K., Duffieux, D. & Jeanthon, C. (2018) Bacterial epibiotic communities of ubiquitous and abundant marine diatoms are distinct in short- and long- term associations. Frontiers in Microbiology, 9, 2879.
https://doi.org/10.3389/fmicb.2018.02879
Curds, C.R. (1987) A revision of Suctoria (Ciliophora, Kinetofragminofora). 5. The Paracineta and Corynophrya problem. Bulletin of British Museum (Natural History). Zoology series, 52, 71–106.
Cutress, C.E. & Ross, D.M. (1969) The sea anemone Calliactis tricolor and its association with the Hermit crab Dardanus venosus. Journal of Zoology, 158, 225–241.
https://doi.org/10.1111/j.1469-7998.1969.tb02143.x
Di Camillo, C., Bo, M., Puce, S., Tazioli, S., Froglia, C. & Bavestrello, G. (2008) The epibiontic assemblage of Geryon longipes (Crustacea: Decapoda: Geryonidae) from the Southern Adriatic Sea. Italian Journal of Zoology, 75 (1), 29–35.
https://doi.org/10.1080/11250000701632279
Gordon, D.P. & Wear, R.G. (1999) A new ctenostome bryozoans ectosymbiotic with terminal moult paddle crabs (Portunidae) in New Zealand. New Zealand Journal of Zoology, 26, 373–380.
https://doi.org/10.1080/03014223.1999.9518200
De Smet, W.H. & Verolet, M. (2016) Epibiotic rotifers of Gammarus pulex (L.)(Crustacea, Amphipoda), with descriptions of two new species and notes on the terminology of the trophi. Zootaxa, 4107 (3), 301–320.
https://doi.org/10.11646/zootaxa.4107.3.1
d’Hondt, J.L. (1983) Tabular keys for the identification of the recent Ctenostomatous Bryozoa. Mémoires de l’Institut océanographique, 14, 1–134.
d’Hondt, J.L. & Hayward, P.J. (1981) Nouvelle srécoltes de Bryozoaires Cténostomes bathyaux et abyssaux. Cahiers De Biologie Marine, 22, 267–283.
Dovgal, I.V. (1996) Keys for identification of tentaculous infusoria (Ciliophora, Suctoria) of the Ukrainian fauna. Vestnik Zoologii, Supplement 2, 1–42.
Dovgal, I.V. (2002) Evolution, phylogeny and classification of Suctorea (Ciliophora). Protistology, 24, 194–270.
Dovgal, I.V. (2013) Fauna of Ukraine. Vol. 36. Ciliates—Ciliophora. Issue 1. Class Suctorea. Naukova dumka, Kiev, 267 pp.
Dovgal, I., Chatterjee, T. & Ingole, B. (2008a) An overview of Suctorian ciliates (Ciliophora, Suctorea) as epibionts of halacarid mites (Acari: Halacaridae). Zootaxa, 1810 (1), 60–68.
https://doi.org/10.11646/zootaxa.1810.1.4
Dovgal, I., Chatterjee, T. & Ingole, B. (2009a) New records of Thecacineta cothurnoides and Trematosoma rotunda (Ciliophora, Suctorea) as epibionts on nematodes from Indian Ocean. Protistology, 6, 9–23.
Duval, B. & Margulis, L. (1995) The microbial community of Ophrydium versatile colonies: Endosymbionts, residents, and tenants. Symbiosis, 18, 181–210.
Eggleston, D. (1971) Synchronization between moulting in Calocaris macrandreae (Decapoda) and reproduction in its epibiont Tricella koreni (Polyzoa Ectoprocta). Journal of the Marine Biological Association of the United Kingdom, 51, 409–410.
https://doi.org/10.1017/S0025315400031878
Ejsmont-Karabin, J. & Karpowicz, M. (2019) Epizoic rotifers on Dreissena polymorpha in relation to biotic factors. Hydrobiologia, 828, 137–145.
https://doi.org/10.1007/s10750-018-3808-4
Felinska, M. (1965) Marine ciliata from Plymouth. Peritricha.Vaginincolidae. Journal of the Marine Biological Association of the United Kingdom, 45, 229–239.
https://doi.org/10.1017/S0025315400004094
Fernandez-Leborans, G. (2003a) A review of cnidarian epibionts on marine crustacean. Oceanological and Hydrobiological Studies, 42, 347–354.
https://doi.org/10.2478/s13545-013-0092-9
Fernandez-Leborans, G. (2003b) Protist bryozoans crustacean hyperepibiosis on Goneplax rhomboides (Linnaeus, 1758) (Decapoda, Brachyura) from the NW Medaterannean coast. Crustaceana, 76 (4), 479–497.
https://doi.org/10.1163/156854003322033870
Fernandez-Leborans, G. (2010) Epibiosis in Crustacea: an overview. Crustaceana, 83 (5), 549-640.
https://doi.org/10.1163/001121610X491059
Fernandez-Leborans, G. & Gabilondo, R. (2006) Taxonomy and distribution of the hydrozoan and protozoan epibionts on Pagurus bernhardus (Linnaeus, 1758) (Crustacea, Decapoda) from Scotland. Acta Zoologica, 87, 33–48.
https://doi.org/10.1111/j.1463-6395.2006.00218.x
Fernandez-Leborans, G. & Tato-Porto, M.L. (2000a) A review of the species of protozoan epibionts on crustaceans. I. Peritrich ciliates. Crustaceana, 73, 643–683.
https://doi.org/10.1163/156854000504705
Fernandez-Leborans, G. & Tato-Porto, M.L. (2000b) A review of the species of protozoan epibionts on crustaceans. II. Suctorian ciliates. Crustaceana, 73, 1205–1237.
https://doi.org/10.1163/156854000505209
Fernandez-Leborans, G., Chatterjee, T. & Grego, M. (2012) New records of epibiont ciliates (Ciliophora) on Harpacticoida (Copepoda, Crustacea) from the Bay of Piran (Gulf of Trieste, Northern Adriatic). Cahiers De Biologie Marine, 53, 53–63.
Fernandez-Leborans, G., Dávila, P., Cerezo, E. & Contretas, C. (2013) Epibiosis and hyperepibiosis on Pagurus bernhardus (Crustacea: Decapoda) from the west Coast of Scotland. Journal of the Marine Biological Association of the United Kingdom, 93 (5), 1351–1362.
https://doi.org/10.1017/S0025315412001610
Fraipont, J. (1878) Recherches sur les Acinetiens de la cote d’Ostende. Bulletin de l’Academie (r.) des sciences des lettres et des beaux arte de Belgique, 45, 247–297.
Gili, J., Abello, P. & Villanueva, R. (1993) Epibiont and intermoult duration in the crab Bathynectes piperitus. Marine Ecology Progress Series, 98, 107–113.
https://doi.org/10.3354/meps098107
Gordon, D.P. (1986) The marine fauna of New Zealand: Bryozoa: Gymnolaemata (Ctenostomata and Cheilostomata Anasca) from the western South Island continental shelf and slope. New Zealand Oceanographic Institute Memoir, 95, 1–121.
Gordon, D.P. & Wear, R.G. (1999) A new ctenostome bryozoan ectosymbiotic with terminal-moult paddle crabs (Portunidae) in New Zealand. New Zealand Journal of Zoology, 26, 373–380.
https://doi.org/10.1080/03014223.1999.9518200
Grischenko, A.V. & Chernyshev, A.V. (2015) Triticella minini—a new ctenostome bryozoan from the abyssal plain adjacent to the Kuril-Kamchatka Trench. Deep-Sea Research, Part II, 111, 343-350.
https://doi.org/10.1016/j.dsr2.2014.08.004
Grischenko, A.V. & Chernyshev, A.V. (2017) Deep-water Bryozoa from the Kuril Basin, Sea of Okhotsk. Deep Sea Research, Part II, 154, 59–73.
https://doi.org/10.1016/j.dsr2.2017.09.011
Hadži, J. (1938) Beitrag zur Kenntnis der adriatischen Follikuliniden (Inf. Heterotricha). Subfam. Eufolliculininae. Acta Adriatica, 2, 1–46.
Hadži, J. (1951) Studien uber Follikuliniden. Dela Razredza Prirodoslovnein Medicinske Vede. Slovenska Akademija Znanostiin Umetnosti, 4, 1–390.
Harder, T. (2009) Marine epibiosis: concepts, ecological consequences and host defence. In: Venkatesan, R. Murthy, S.P. & Cooksey, K. (Eds.), Marine and Industrial Biofouling. Vol. 4. Springer, Heidelberg and New York, pp. 219–232.
https://doi.org/10.1007/978-3-540-69796-1_12
Hayward, P.J. (1985) Ctenostome Bryozoans. Keys and notes for the identification of the species. Linnean Society Synopsis of the British Fauna, New Series, 33, 1–169.
Ingle, R.W. (1983) Shallow-water crabs. Synopsis of British fauna, New Series, 25, 1–206.
Jankowski, A.V. (1981) New species, genera and families of the tentacled infusoria (Class Suctoria). Proceedings of the Zoological Institute, 107, 80–115.
Jankowski, A.V. (2007) Review of taxa Phylum Ciliophora Doflein, 1901. In: Alimov, A.F (Ed.), Protista: Handbook on Zoology. Part 2. Nauka, St. Petersburg, pp. 415–993. [in Russian]
Jensen, K. & Bender, K. (1972) Invertebrates associated with snail shells inhabited by Pagurus bernhardus (L.) (Decapoda). Ophelia, 10 (2), 185–192.
https://doi.org/10.1080/00785326.1972.10430113
Kahl, A. (1933) Ciliata libera et ectocommensalia. In: Grimpe, G. & Wagler, E. (Eds.), Die Tierwelt der Nord-und Ostee, Lief. 23 (Teil II, c3), 29–146.
Kahl, A. (1935) Wimpertiere oder Ciliata (lnfusoria), eine Bearbeitung der freilebenden und ectocommensalen Infusorien der Erde, unter Ausschlussder marinen Tintinnidae. 4. Peritricha und Chonotricha. In: Grimpe, G. & Wagler, E. (Eds.), Die Tierwelt der Nord und Ostsee, 30, 651–886.
Key, M.M. Jr., Jeffries, W.B., Voris, H.K. & Yang, C.M. (1996a) Epizoic bryozoans and mobile ephemeral host substrata. In: Gordon, D.P., Smith, A.M. & Grant-Mackie, J.A. (Eds.), Bryozoans in space and time. National Institute of Water & Atmospheric Research, Wellington, pp. 157–165.
Key, M.M. Jr., Jeffries, W.B., Voris, H.K. & Yang, C.M. (1996b) Epizoic bryozoans, horseshoe crabs and other mobile benthic substrates. Bulletin of Marine Science, 58, 368–384.
Key, M.M. Jr. & Barnes, D.K.A. (1999) Bryozoan colonization of the marine isopod Glyptonotus antarcticus at Signy Island, Antarctica. Polar Biology, 21, 48–55.
https://doi.org/10.1007/s003000050331
Key, M.M. Jr., Winston, J.E., Volpe, J.W., Jeffries, W.B. & Voris, H.K. (1999) Bryozoan fouling of the blue crab Callinectes sapidus at Beaufort, North Carolina. Bulletin of Marine Science, 64 (3), 513–533.
Kirkpatrick, R. & Metzellar, J. (1922) On an instance of commensalism between a hermit crab and a polyzoon. Proceedings of the Zoological Society of London, 1923, 938–990.
https://doi.org/10.1111/j.1469-7998.1922.tb07093.x
Littler, M.M. & Littler, D.S. (2013) “The Nature of Macroalgae and their Interactions on reefs”. In: Research and Discoveries: The Revolution of Science through Scuba. Smithsonian Contributions to the Marine Sciences, 2013, pp. 187–198.
Lopez-Ochoterena, E. (1964) Hypophrya fasciculata gen. nov, sp. nov. (Ciliata: Suctorida). Journal of Protozoology, 11 (2), 222–224.
https://doi.org/10.1111/j.1550-7408.1964.tb01744.x
Marcus, E. (1922) Papers from Dr. Th. Mortensen’s Pacific Expedition 1914–16. VI. Bryozoen von den Auckland- und Campbell-Inseln.Videnskabelige Meddelelserfra Dansk naturhistorisk Foreningi Kebenhavn,73, 85–121.
Marcus, E. (1940) Mosdyr (Bryozóaeller Polyzóa). Danmarks Fauna Vol. G.E.C. Gads, København, 401 pp.
Mayén-Estrada, R. & Clamp, J.C. (2016) An annotated checklist of species in the family Lagenophryidae (Ciliophora, Oligohymenophorea, Peritrichia), with a brief review of their taxonomy, morphology, and biogeography. Zootaxa, 4132 (4), 451–492.
https://doi.org/10.11646/zootaxa.4132.4.1
Mayén-Estrada, R. & Utz, L.R.P. (2018) A checklist of species of Vorticellidae (Ciliophora: Peritrichia) epibionts of crustaceans. Zootaxa, 4500 (3), 301–328.
https://doi.org/10.11646/zootaxa.4500.3.1
McGaw, I.J. (2006) Epibionts of sympatric species of Cancer crabs in Barkely sound, British Columbia. Journal of Crustacean Biology, 26, 85–93.
https://doi.org/10.1651/C-2601.1
Menon, N.R. (1972) Species of the sub-order Ctenostomata Busk (Bryozoa) from Indian waters. Internationale Revue der gesamten Hydrobiologie, 57 (4), 599–629.
https://doi.org/10.1002/iroh.19720570410
Mereschkowsky, C. (1877) Studies on the Protozoa of Northern Russia. Travaux de la Société des naturalistes de St.-Petersbourg, 8 (3), 203–385. [in Russian]
Mestre, A., Poulin, R., Holt, R.D., Barfield, M., Clamp, J.C., Fernandez-Leborans, G. & Mesquita-Joanes, F. (2019) The interplay of nested biotic interactions and the abiotic environment regulates populations of a hypersymbiont. Journal of Animal Ecology. [published online]
https://doi.org/10.1111/1365-2656.13091
Nanajkar, M., Fernandes, V., Bogati, K. & Chatterjee, T. (2019) Gregarious true-colonies of ciliate Vorticella oceanica on a chain forming diatom Chaetoceros coarctatus: indicating change in the nature of association. Symbiosis, 79 (3), 221–229.
https://doi.org/10.1007/s13199-019-00640-4
Normant, M., Zawal, A., Chatterjee, T. & Wojcik, D. (2013) Epibiotic mites associated with the invasive Chinese mitten crab Eriocheir sinensis– new records of Halacaridae from Poland. Oceanologia, 55 (4), 901–915.
https://doi.org/10.5697/oc.55-4.901
O’Donoghu, C.H. & O’Donoghue, E. (1926) A second list of Bryozoa from the Vancouver Island region. Contributions to Canadian Biology and Fisheries, New Series, 3, 47–131.
Oresland, V. (2019) The polychaete Histriobdella homari and major groups of epibionts on the European lobster, Homarus gammarus and other decapods. Crustaceana, 92/2, 189–203.
https://doi.org/10.1163/15685403-00003865
Osburn, R.C. (1953) Bryozoa of the Pacific coast of America, part 3, Cyclostomata, Ctenostomata, Entoprocta and Addenda. Report of the Allan Hancock Pacific Expeditions, 14, 613–841.
Overstreet, R.M. (1973) Parasites of some penaeid shrimps with emphasis on reared host. Aquaculture, 2, 105–140.
https://doi.org/10.1016/0044-8486(73)90140-3
Pfaller, J.B., Frick, M.G., Brischoux, F., Sheehy, C.M. & Lillywhite, H.B. (2012) Marine Snake Epibiosis: A Review and first report of decapods associated with Pelamis platurus. Integrative and Comparative Biology, 52 (2), 296–310.
https://doi.org/10.1093/icb/ics038
Precht, H. (1935) Epizoen der Kieler Bucht. Nova Acta Leopoldina, 3, 405–474.
Robinson, N.J., Majewska, R., Lazo-Wasem, E.A., Nel, R., Paladino, F.V., Rojas, L., Zardus, J.D. & Pinou, T. (2016) Epibiotic diatoms are universally present on all Sea Turtle species. PLoS One, 11 (6), e0157011
https://doi.org/10.1371/journal.pone.0157011
Santhakumari, V. (1985) Epizoic and ectoparasitic protozoans from planktonic copepods of the southwest and southeast coasts of India with the description of a new species. Journal of the Marine Biological Association of India, 27 (1–2), 29–38.
Santhakumari, V. (1986a) Epizoic and ectoparasitic protozoans from crab larvae. Mahasagar-Bulletin of the National Institute of Oceanography, 19 (1), 65–67.
Santhakumari, V. (1986b) Two new species of suctorians, Acineta satyanandani sp. nov. and Paracineta karunakarani sp. nov. epizoic on ostracods. Indian Journal of Fisheries, 33 (4), 471–475.
Threlkeld, S.T., Chiavelli, D.A. & Willey, R.L. (1993) The organization of zooplankton epibiont communities. Trends in Ecology and Evolution, 8, 317–321.
https://doi.org/10.1016/0169-5347(93)90238-K
Wahl, M. (1989) Marine epibiosis. I. Fouling and antifouling- some basic aspects. Marine Ecology Progress Series, 58, 175–189.
https://doi.org/10.3354/meps058175
Warren, A. & Paynter, J. (1991) A revision of Cothurnia (Ciliophora, Peritrichida) and its morphological relatives. Bulletin of the British Museum Natural History and Zoology, 57 (1), 17–59.