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Marine Biodiversity

, Volume 47, Issue 2, pp 539–548 | Cite as

Occurrence of epibionts associated with meiofaunal basibionts from the world’s largest mangrove ecosystem, the Sundarbans

  • K. G. M. T. Ansari
  • P. BhaduryEmail author
Original Paper

Abstract

Epibionts–basibionts interaction is an ecological relationship observed across terrestrial and aquatic environments. Ciliate epibionts associated with meiofaunal organisms are ubiquitous throughout marine ecosystems, but their distribution patterns remain largely unknown in mangrove habitats. We studied the occurrence of ciliate epibionts (peritrichids and suctorians) on meiofaunal organisms in the Sundarbans, the world’s largest mangrove ecosystem, during early monsoon of 2015. The present study revealed that 1.13 % of meiofaunal organisms (18 out of 2744 specimens) were infested by ciliate epibionts. The epibionts were found to be adhered to host organisms belonging to free-living nematodes and harpacticoid copepods. Four different species of ciliate epibionts (Cothurnia nova, Pleurophryodendron sp., Thecacineta cothurnioides and Trematosoma rotunda) were associated with four different host meiofaunal species (Chromaspirina parapontica, Dorylaimposis punctata, Stenhelia sp. and Distioculus sp.) as observed in this study. Among them, the epibionts Cothurnia nova and Thecacineta cothurnioides were found in July 2015, while the other epibiont species were encountered in August 2015. The detailed systematic and host frequency and remarks of each ciliate epibiont have been discussed in this study. To the best of our knowledge, this is the first study which reports ciliate epibionts on meiofaunal basibionts from a mangrove ecosystem in India. Our results indicate that the occurrence of epibionts in a mangrove ecosystem (even a human-disturbed site) could be due to habitat heterogeneity and the nature of anthropogenic disturbance.

Keywords

Ciliates Epibionts Basibionts Mangrove ecosystem Sundarbans 

Notes

Acknowledgments

We are grateful to Dr. Igor Dovgal, Schmalhausen Institute of Zoology, Ukraine, for helping with the identification and confirmation of ciliate epibionts and we are also grateful to Dr. Marleen De Troch, Ghent University, Belgium, for identification of the harpacticoid copepods reported in this study. This work is supported by grants awarded to K.G.M.T. Ansari by the Indian Institute of Science Education Research Kolkata (IISERK) through a Post Doctoral Fellowship, and grants awarded to P. Bhadury from MOES (ITIS of MLRP). We are also grateful to Integrative Taxonomy and Microbial Ecology Research group members for helping us during field work.

References

  1. Allgén CA (1952) Uber zwei neue subantarktische Suctorien aus dem Gracham Land. K Fysiogr Sällsk Lund Forh 21:173–176Google Scholar
  2. Allgén CA (1955) Die Suctorien der schwedischen sudpolar-expedition (1901–1903). Zool Anz 154:36–48Google Scholar
  3. Ansari KGMT, Manokaran S, Raja S, Lyla PS, Ajmal Khan S (2014) Interaction of free-living marine nematodes in the artificial mangrove environment (southeast coast of India). Environ Monit Assess 186:293–305. doi: 10.1007/s10661-013-3374-1 CrossRefPubMedGoogle Scholar
  4. Armenteros M, Perez-Garcıa JA, Perez-Angulo A, Williams JP (2008) Efficiency of extraction of meiofauna from sandy and muddy marine sediments. Rev Invest Mar 29:113–118Google Scholar
  5. Barik J, Chowdhury S (2014) True mangrove species of Sundarbans delta, West Bengal, Eastern India. Check List 10:329–334Google Scholar
  6. Bhattacharjee D (2014) Suctorian epibionts on Chromaspirina sp. (Nematoda: Desmodoridae) from the shallow continental shelf of the Bay of Bengal, northern Indian Ocean. Mar Biodiver Rec 7:e49. doi: 10.1017/S1755267214000451 CrossRefGoogle Scholar
  7. Bhattacharjee D, Samanta B, Danda AA, Bhadury P (2013) Temporal succession of phytoplankton assemblages in a tidal creek system of the sundarbans mangroves: an integrated approach. Int J Biodivers. doi: 10.1155/2013/824543, Article ID 824543Google Scholar
  8. Buchanan JB (1984) Sediment analysis. In: Holme NA, McIntyre AD (eds) Methods for the study of marine benthos. Blackwell, London, pp 41–65Google Scholar
  9. Cabral AF, Dias RJP, Utz LRP, Alves RG, D’Agosto M (2010) Spatial and temporal occurrence of Rhabdostyla cf. chironomi Kahl, 1933 (Ciliophora, Peritrichia) as an epibiont on chironomid larvae in a lotic system in the neotropics. Hydrobiologia 644:351–359. doi: 10.1007/s10750-010-0202-2 CrossRefGoogle Scholar
  10. Chatterjee T, Fernandez-Leborans G, Chan BKK (2011) New record of the ciliate Thecacineta calix (Ciliophora: Suctorea) epibionts on Agauopsis halacarid mite (Acari, Halacaridae) from Taiwan. Scripta Sci Nat 2:121–127Google Scholar
  11. Chatterjee T, Fernandez-Leborans G, Ramteke D, Ingole B (2013) New records of epibionts ciliates (Ciliophora) from Indian coast with descriptions of six new species. Cah Biol Mar 54:143–159Google Scholar
  12. Chatterjee T, Fernandez-Leborans G, Schizas NV (2014) Report of Thecacineta calix (Ciliophora: Suctorea) as an epibionts of harpacticoid from Caribbean mesophotic reefs. Caribb J Sci 48:44–48CrossRefGoogle Scholar
  13. Choudhury AK, Das M, Philip P, Bhadury P (2015) An assessment of the implications of seasonal precipitation and anthropogenic influences on a mangrove ecosystem using phytoplankton as proxies. Est Coast 38:854–872Google Scholar
  14. Collin B (1909) Diagnoses preliminiaries d’Acinetiens nouveaux ou mal connus. C RAcad Sci 149:1094–1095Google Scholar
  15. Curds CR (1985) A revision of Suctoria (Ciliophora, Kinetofragminofora) 1. Acineta and its morphological relatives. Bull Br Mus Nat Hist Zool 48:75–129Google Scholar
  16. Dias RJP, D’avila S, D’agosto M (2006) First record of peritrichs and suctorians (Protozoa, Ciliophora) on Pomacea lineata (Spix, 1827). Braz Arch Biol Technol 49:807–812CrossRefGoogle Scholar
  17. Dovgal IV (1988) Current state of the faunistic knowledge of tentaculous infusoria (Ciliophora, Suctoria) in the Ukrainian SSR. 3135: 1–35. Deposited in VINITI on 22.04.88 (in Russian)Google Scholar
  18. Dovgal IV (1996) Keys for identification of tentaculous infusoria (Ciliophora, Suctoria) of the Ukrainian fauna. Vestnik Zool. Suppl 2: 1–42 (in Russian with English summary)Google Scholar
  19. Dovgal IV (2002) Evolution, phylogeny and classification of Suctorea (Ciliophora). Protistology 2:194–270Google Scholar
  20. Dovgal IV, Pešić V (2012) Suctorian ciliates (Ciliophora, Suctorea) as epibionts of stream-dwelling aquatic beetles (Coleoptera) and water mites (Acari: Hydrachnidia) in the southwestern Palaearctic region. Zootaxa 3166:34–40Google Scholar
  21. Dovgal IV, Chatterjee T, Ingole B (2008a) An overview of suctorian ciliates (Ciliophora: Suctorea) as epibionts of halacarid mites (Acari, Halacaridae). Zootaxa 1810:60–68Google Scholar
  22. Dovgal IV, Chatterjee T, Ingole B, Nanajkar M (2008b) First report of Limnoricus ponticus Dovgal & Lozowskiy (Ciliophora: Suctorea) as epibionts on Pycnophyes (Kinorhyncha) from the Indian Ocean with key to species of the genus Limnoricus. Cah Biol Mar 49:381–385Google Scholar
  23. Dovgal IV, Chatterjee T, Ingole B (2009) New Records of Thecacineta cothurnioides and Trematosoma rotunda (Ciliophora, Suctorea) as epibionts on nematodes from the Indian Ocean. Protistology 6:19–23Google Scholar
  24. Fenchel T (1987) Ecology of protozoa. Science Tech, MadisonGoogle Scholar
  25. Fernandez-Leborans G, Tato-Porto ML (2000a) A review of the species of protozoan epibionts on crustaceans. I. Peritrich ciliates. Crustaceana 73:643–683. doi: 10.1163/156854000504505 CrossRefGoogle Scholar
  26. Fernandez-Leborans G, Tato-Porto ML (2000b) A review of the species of protozoan epibionts on crustaceans. II. Suctorian ciliates. Crustaceana 73:1205–1237. doi: 10.1163/156854000505209 CrossRefGoogle Scholar
  27. 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). Cah Biol Mar 53:53–63Google Scholar
  28. Finch MS, Hydes DJ, Clayson CH, Weigl B, Dakin J, Gwilliam P (1998) A low power ultra violet spectrophotometer for measurement of nitrate in seawater: Introduction, calibration and initial sea trails. Anal Chim Acta 377:167–177CrossRefGoogle Scholar
  29. Fisher R (2003) Ciliate hitch-hikers-nematode ecto-commensals from tropical Australian sea-grass meadows. J Mar Biol Assoc UK 83:445–446. doi: 10.1017/S0025315403007306h CrossRefGoogle Scholar
  30. Foissner W, Berger H, Schaumburg J (1999). Identification and ecology of limnetic plankton ciliates. Informations berichte des Bayer. Landesamtes für Wasserwirtschaft, Heft 3/99. Munich, GermanyGoogle Scholar
  31. Gaudette HE, Flight WR, Lois T, Folger DW (1974) An inexpensive titration method for determination of organic carbon in recent sediments. J Sediment Petrol 44:249–253Google Scholar
  32. Gopal B, Chauhan M (2006) Biodiversity and its conservation in the Sundarban mangrove ecosystem. Aquat Sci 68:338–354Google Scholar
  33. Görtz HD (1996) Symbiosis in ciliates. In: Hausmann K, Bradbury PC (eds) Ciliates: cells as organisms. Gustav Fischer, Stuttgart, pp 441–462Google Scholar
  34. Harrison PJ, Khan N, Yin K, Saleem M, Bano N, Nisa M, Ahmed SI, Rizvi N, Azam F (1997) Nutrient and phytoplankton dynamics in two mangrove tidal creeks of the Indus river delta Pakistan. Mar Ecol Prog Ser 157:13–19CrossRefGoogle Scholar
  35. Huys R, Gee JM, Moore CG, Hamond R (1996) Marine and brackish water harpacticoid copepods. Part 1. (Synopses of the British fauna. New series no 51). Field Studies Council, ShrewsburyGoogle Scholar
  36. Ingole B, Singh R, Sautya S, Dovgal I, Chatterjee T (2010) Report of Epibiont Thecacineta calyx (Ciliophora, Suctorea) on deep sea Desmodora (Nematoda) from the Andaman Sea, Indian Ocean. Mar Biodiver Rec 3:1–3. doi: 10.1017/S1755267209990777 CrossRefGoogle Scholar
  37. Jankowski AV (1978) Phylogeny and divergence of suctorians. Doklady Academii Nauk SSSR 242:493–496 (in Russian)Google Scholar
  38. Jankowski AV (1981) New species, genera and families of tentacled infusoria (class Suctoria). Proc Zool Inst 107:80–115 (in Russian with English summary)Google Scholar
  39. Jankowski AV (2007) Review of taxa Phylum Ciliophora Doflein, 1901. In: Alimov A (ed) Protista: handbook on zoology. Nauka, St Petersburg, pp 415–993Google Scholar
  40. Liao J, Dovgal IV (2015) A new Thecacineta species (Ciliophora, Suctorea) on Desmodora pontica (Nematoda, Desmodorida) from a seagrass bed in Taiwan. Protistology 9:75–78Google Scholar
  41. Liddicoat MI, Tribbitts S, Butler EI (1975) The determination of ammonia in seawater. Limnol Oceanogr 20:131–132CrossRefGoogle Scholar
  42. Lynn DH (2008) The ciliated protozoa. Characterization, classification and guide to the literature, 3rd edn. Springer, BerlinGoogle Scholar
  43. Maria TF, Morgado-Esteves A, Smol N, Vanreusel A, Decraemer W (2009) Chromaspirina guanabarensis sp. n. (Nematoda: Desmodoridae) and a new illustrated dichotomous key to Chromaspirina species. Zootaxa 2092:21–36Google Scholar
  44. Moss AG, Estes AM, Muellner LA, Morgan DD (2001) Protistian epibionts of the ctenophore Mnemiopsis mccradyi Mayer. Hydrobiologia 451:295–304. doi: 10.1023/A:1011846022599 CrossRefGoogle Scholar
  45. Padmakumar KB, Thomas LC, Vijayan A, Sanjeevan VN (2014) Occurrence of epibiontic suctorian protozoansa on marine ostracod Cypridina dentate (Muller, 1906) in the North Eastern Arabian Sea. Indian J Geo-Mar Sci 44:1–5Google Scholar
  46. Pane L, Bonello G, Mariottini GL (2014) Epibiotic ciliates Scyphidia sp. and diatoms on Tigriopus fulvus (Copepoda: Harpacticoida) exoskeleton. J Biol Res 87:4600. doi: 10.4081/jbr.2014.4600 Google Scholar
  47. Pfannkuche O, Thiel H (1988) Sample processing. In: Higgins RP, Thiel H (eds) Introduction to the study of Meiofauna. Smithsonian Institute Press, Washington DC, pp 134–145Google Scholar
  48. Platt HM, Warwick RM (1983) Free living marine nematodes, Part I, British Enoplids, pictorial key to world genera and notes for the identification of British species. In: Kermack DM, Barnes RSK (eds) Synopses of the British Fauna, vol 28. Cambridge University Press, CambridgeGoogle Scholar
  49. Platt HM, Warwick RM (1988) Free living marine nematodes, Part II, British Chromodorids, Pictorial key to world genera and notes for the identification of British species. In: Kermack DM, Barnes RSK (eds) Synopses of the British Fauna (new series), vol 38. Brill/Backhuys, LeidenGoogle Scholar
  50. Rajabunizal K, Ramanibai R (2011) Presence of an epibiont Epistylis niagarae (Protozoa Ciliophora) on Mesocyclops aspericornis in Velachery Lake Chennai India. J Biol Sci 11:189–195CrossRefGoogle Scholar
  51. Roszak DB, Colwell RR (1987) Survival strategies of bacteria in the natural environment. Microbiol Rev 51:365–379PubMedPubMedCentralGoogle Scholar
  52. Samanta B, Bhadury P (2014) Analysis of diversity of chromophytic phytoplankton in a mangrove ecosystem using rbcL gene sequencing. J Phycol 50:328–340. doi: 10.1111/jpy.12163 CrossRefPubMedGoogle Scholar
  53. Samanta B, Bhadury P (2016) A comprehensive framework for functional diversity patterns of marine chromophytic phytoplankton using rbcL phylogeny. Sci Rep. doi: 10.1038/srep20783 Google Scholar
  54. Santhakumari V (1997) Studies on the associates and parasites of zooplankton from southwest and southeast coasts of India Journal of the Marine Biological Association of India. J Mar Biol Assoc India 39:171–174Google Scholar
  55. Seinhorst JW (1959) A rapid method for the transfer of nematodes from fixative to anhydrous glycerine. Nematologica 4:67–69CrossRefGoogle Scholar
  56. Sergeeva N, Dovgal IV (2014) First finding of epibiont peritrich and suctorian ciliates (Ciliophora) on oligochaetes and harpacticoid copepods from the deep-water hypoxic/anoxic conditions of the Black Sea. Ecol Montenegrina 1:49–54Google Scholar
  57. Spalding M, Blasco F, Field C (1997) World Mangrove Atlas. (International Society for Mangrove Ecosystems, OkinawaGoogle Scholar
  58. Strickland JDH, Parsons TR (1984) A practical handbook of seawater analysis, bulletin (vol. 167). Fisheries Research Board of Canada, Queen’s Printer, OttawaGoogle Scholar
  59. Threlkeld ST, Chiavelli DA, Willey RL (1993) The organization of zooplankton epibionts communities. Trends Ecol Evol 8:317–321. doi: 10.1016/0169-5347(93)90238-K CrossRefPubMedGoogle Scholar
  60. Turner RE, Qureshi N, Rabalais NN, Dortch Q, Justic D, Shaw RF, Cope J (1998) Fluctuating silicate: nitrate ratios and coastal plankton food webs. Proc Natl Acad Sci U S A 95:13048–13051. doi: 10.1073/pnas.95.22.13048 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Utz LRP, Coats DW (2005) Spatial and temporal patterns in the occurrence of peritrichs ciliates as epibionts on calanoid copepods in the Chesapeake Bay, USA. J Euk Microbiol 52:236–244. doi: 10.1111/j.1550-7408.2005.00025.x CrossRefPubMedGoogle Scholar
  62. Van Geaver S, Raes M, Pasotti F, Vanreusel A (2010) Spatial scale and habitat-dependent diversity patterns in marine nematode communities in three seepage related sites along the Norwegian Sea margin. Mar Ecol 31:66–77. doi: 10.1111/j.1439-0485.2009.00314.x CrossRefGoogle Scholar
  63. Vanaverbeke J, Bezerra TN, Braeckman U, De Groote A, De Meester N, Deprez T, Derycke S, Gilarte P, Guilini K, Hauquier F, Lins L, Maria T, Moens T, Pape E, Smol N, Taheri M, Van Campenhout J, Vanreusel A, Wu X, Vincx M (2015) NeMys: world database of free-living marine nematodes at http://www.nemys.ugent.be/aphia.php?p=taxadetails&id=2132 added on 02.03.2015
  64. Warwick RM, Platt HM, Somerfield PJD (1998) Free-living marine nematodes, Part III, Monhysterids, pictorial key to world genera and notes for the identification of British species. In: Kermack DM, Barnes RSK (eds) Synopses of the British Fauna (New series), Field Studies Council, ShrewsburyGoogle Scholar
  65. Wells JBJ (1976) Keys to aid in the identification of marine harpacticoid copepods. Aberdeen University Press, AberdeenGoogle Scholar

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© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Integrative Taxonomy and Microbial Ecology Research Group, Department of Biological SciencesIndian Institute of Science Education and Research Kolkata (IISERK)MohanpurIndia

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