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Factors regulating proliferation and co-occurrence of loricate ciliates in the microzooplankton community from the eastern Arabian Sea

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Abstract

Ciliates are highly developed and diverse eukaryotes belonging to the microzooplankton community; they exhibit a wide distributional range and are a crucial component of the microbial food web. The current study addresses the species aggregation of ciliates, which is rare and underreported, from the Indian waters. The aggregation was dominated by coexisting species such as Amphorides quadrilineata and Salpingella faurei during 2018 (45–95%), whereas Dadayiella ganymedes and Helicostomella subulata predominated in 2003 (40%), with both aggregations occurring during late summer monsoon (September) in the region. The species environmental correlation revealed that salinity and chlorophyll a, especially the nanoplankton fraction, were significant factors responsible for the exceptional abundance and community structure. The pattern of association with the distinct lorica oral diameter (LOD) of the coexisting species exhibits an upper range of 28–32 µm (A. quadrilineata and D. ganymedes) and a lower LOD range of 15–17 µm (S. faurei and H. subulata), delineating a niche based on resource spectrum and revealing why certain species successfully predominate in utilizing the available resources. Although such events have received sporadic attention, the recurrence of aggregation comprising strategic coexistence of species indicates the status of the ecosystem and argues for future monitoring to better understand the dynamics of the region.

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The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  • Adl SM, Bass D, Lane CE, Lukeš J, Schoch CL, Smirnov A, Agatha S, Berney C, Brown MW, Burki F, Cárdenas P (2019) Revisions to the classification, nomenclature, and diversity of eukaryotes. J Eukaryot Microbiol 66(1):4–119

    Article  PubMed  PubMed Central  Google Scholar 

  • Albin KJ, Jyothibabu R, Alok KT, Santhikrishnan S, Sarath S, Sudheesh V, Sherin CK, Balachandran KK, Asha Devi CR, Gupta GVM (2022) Distinctive phytoplankton size responses to the nutrient enrichment of coastal upwelling and winter convection in the eastern Arabian Sea. Prog Oceanogr. https://doi.org/10.1016/j.pocean.2022.102779

    Article  Google Scholar 

  • Amol P (2018) Impact of Rossby waves on chlorophyll variability in the southeastern Arabian Sea. Remote Sens Lett 9(12):1214–1223

    Article  Google Scholar 

  • Anjusha A, Jyothibabu R, Jagadeesan L, Arunpandi N (2018) Role of rotifers in microzooplankton community in a large monsoonal estuary (Cochin back waters) along the west coast of India. Environ Monit Assess 190(5):295

    Article  CAS  PubMed  Google Scholar 

  • Asha Devi CR, Jyothibabu R, Sabu P, Jacob J, Habeebrehman H, Prabhakaran MP, Jayalakshmi KJ, Achuthankutty CT (2010) Seasonal variations and trophic ecology of microzooplankton in the southeastern Arabian Sea. Cont Shelf Res 30:1070–1084

    Article  Google Scholar 

  • Asha Devi CR, Kumar KV, Gupta GVM, Vijayan A, Sudhakar M (2018) Implications of stratification on the heterotrophic plankton community (micro- & meso zooplankton) in the South Eastern Arabian Sea. Reg Stud Mar Sci 24:66–81

    Google Scholar 

  • Beers J, Stewart GL (1967) Micro-zooplankton in the euphotic zone at five locations across the California Current. J Fish Board Can 24(10):2053–2068

    Article  Google Scholar 

  • Calbet A (2008) The trophic roles of microzooplankton in marine systems. ICES J Mar Sci 65(3):325–331. https://doi.org/10.1093/icesjms/fsn013

    Article  Google Scholar 

  • Carritt DE, Carpenter JH (1966) Comparison and evaluation of currently employed modifications of the Winkler method for determining dissolved oxygen in seawater: a NASCO report. J Mar Res 24:286–318

    CAS  Google Scholar 

  • Chowdhury M, Biswas H (2023) A coherent status of summer monsoon phytoplankton communities (2017–2018) along the Western Indian continental shelf: implications for fisheries. Sci Total Environ 878:162963. https://doi.org/10.1016/j.scitotenv.2023.162963

    Article  CAS  PubMed  Google Scholar 

  • Claessens M, Wickham SA, Post AF, Reuter M (2010) A paradox of the ciliates? High ciliate diversity in a resource-poor environment. Mar Biol 157:483–494

    Article  Google Scholar 

  • D’Alelio D, Libralato S, Wyatt T, Ribera d’Alcalà M (2016) Ecological-network models link diversity, structure and function in the plankton food-web. Sci Rep 6(1):21806

    Article  PubMed  PubMed Central  Google Scholar 

  • Dale T, Dahl E (1987) Mass occurrence of planktonic oligotrichous ciliates in a bay in southern Norway. J Plankton Res 9:871–879

    Article  Google Scholar 

  • Dolan JR (2010) Morphology and ecology in tintinnid ciliates of the marine plankton: correlates of lorica dimensions. Acta Protozoologica 49:235–344

    Google Scholar 

  • Dolan JR (2013) Introduction to tintinnids. Biol Ecol Tintinnid Ciliates: Models Mar Plankton 1:1–16

    Google Scholar 

  • Dolan JR, Landry MR, Ritchie ME (2013) The species-rich assemblages of tintinnids (marine planktonic protists) are structured by mouth size. ISME J 7(6):1237–1243

    Article  PubMed  PubMed Central  Google Scholar 

  • Dolan JR, Raybaud V (2020) Zooplankton I. Micro- and Mesozooplankton. In: Migon C, Nival P, Sciandra A (eds) The Mediterranean Sea in the era of global change 2: 30 years of multidisciplinary study of the Ligurian Sea. pp 67–107

  • Fileman ES, Leakey RJG (2005) Microzooplankton dynamics during the development of the spring bloom in the north-east Atlantic. J Mar Biol Assoc UK 85(4):741–753

    Article  CAS  Google Scholar 

  • García-Robledo E, Corzo A, Papaspyrou S (2014) A fast and direct spectrophotometric method for the sequential determination of nitrate and nitrite at low concentrations in small volumes. Mar Chem 162:30–36

    Article  Google Scholar 

  • Gauns M (2000) Role of microzooplankton in the food chain dynamics of some tropicalmarine environments. Ph D Thesis University of Goa India, p 210

  • Grasshoff K, Ehrhardt M, Kremling K (1999) Methods of sea water analysis, 3rd edn. Wiley-VCH, Weinheim, New York, pp 75–89 (159–196)

    Book  Google Scholar 

  • Grattepanche JD, Santoferrara LF, McManus GB, Katz LA (2016) Unexpected biodiversity of ciliates in marine samples from below the photic zone. Mol Ecol 25(16):3987–4000

    Article  PubMed  Google Scholar 

  • Gupta GVM, Jyothibabu R, Ramu CV, Reddy AY, Balachandran KK, Sudheesh V, Kumar S, Chari NVHK, Bepari KF, Marathe PH, Reddy BB (2021) The world’s largest coastal deoxygenation zone is not anthropogenically driven. Environ Res Lett 16(5):054009

    Article  CAS  Google Scholar 

  • Habeebrehman H, Prabhakaran MP, Jacob J, Sabu P, Jayalakshmi KJ, Achuthankutty CT, Revichandran C (2008) Variability in biological responses influenced by upwelling events in the Eastern Arabian Sea. J Mar Syst 74:545–560

    Article  Google Scholar 

  • Hareesh Kumar PV, Anand P (2016) Coastal upwelling off the southwest coast of India: observations and simulations. Int J Dig Earth 9(12):1256–1274

    Article  Google Scholar 

  • Haury LR, McGowan JA, Wiebe PH (1978) Patterns and processes in the time-space scales of plankton distributions. In: Steele JH (ed) Spatial pattern in plankton communities. Plenum, New York, pp 277–327

    Chapter  Google Scholar 

  • Heinbokel JF (1978) Studies on the functional role of tintinnids in the southern California Bight. I. Grazing and growth rates in laboratory cultures. Mar Biol 47:177–189

    Article  Google Scholar 

  • Heinbokel JF (1988) Reproductive rates and periodicities of oceanic tintinnine ciliates. Mar Ecol Progress Ser 47:239–248

    Article  Google Scholar 

  • Jagadeesan L, Jyothibabu R, Arunpandi N, Karnan C, Balachandran KK (2017) Dominance of coastal upwelling over Mud Bank in shaping the mesozooplankton along the southwest coast of India during the Southwest Monsoon. Prog Oceanogr 156:252–275

    Article  Google Scholar 

  • Jayaram C, Chacko N, Joseph KA, Balchand AN (2010) Interannual variability of upwelling indices in the Southeastern Arabian Sea: a satellite-based study. Ocean Sci J 45(1):27–40

    Article  Google Scholar 

  • Jyothibabu R, Asha Devi CR, Madhu NV, Sabu P, Jayalakshmy KV, Jacob J, Habeebrehman H, Prabhakaran MP, Balasubramanian T, Nair KKC (2008) The response of microzooplankton (20–200 μm) to coastal upwelling and summer stratification in the southeastern Arabian Sea. Cont Shelf Res 28:653–671

    Article  Google Scholar 

  • Jyothibabu R, Madhu NV, Habeebrehman H, Jayalakshmy KV, Nair KKC, Achuthankutty CT (2010) Re-evaluation of “paradox of mesozooplankton” in the eastern Arabian Sea based on ship and satellite observations. J Mar Syst 81:235–251

    Article  Google Scholar 

  • Jyothibabu R, Jagadeesan L, Karnan C, Arunpandi N, Pandiyarajan RS, Balachandran KK (2018) Ecological indications of copepods to oxygen-deficient near-shore waters. Ecol Indic 93:76–90. https://doi.org/10.1016/j.ecolind.2018.04.069

    Article  CAS  Google Scholar 

  • Kamiyama T (2015) Planktonic ciliates: diverse ecological function in seawater. 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_11

    Chapter  Google Scholar 

  • Karnan C, Jyothibabu R, Arunpandi N, Albin KJ, Parthasarathi S, Krishnan SS (2020) Response of microplankton size structure to summer stratification, freshwater influx and coastal upwelling in the Southeastern Arabian Sea. Cont Shelf Res 193:104038

    Article  Google Scholar 

  • Kofoid CA, Campbell AS (1929) A conspectus of the marine and fresh-water ciliata belonging to the suborder tintinnoinea, with descriptions of new species principally from the Agassiz expedition to the eastern tropical Pacific 1904–1905. Univ Calif Publ Zool 34:1–403

    Google Scholar 

  • Kofoid CA, Campbell AS (1939) The Tintinnoinea of the eastern tropical Pacific. Bull Mus Compar Zool Harvard Coll 84:1–473

    Google Scholar 

  • Krishnamurthy K, Naidu DW (1977) Swarming of tintinnids in the Vellar estuary. Curr Sci 46(11):384

    Google Scholar 

  • Lepš J, Šmilauer P (2003) Multivariate analysis of ecological data using CANOCO. Cambridge University Press

    Book  Google Scholar 

  • Li H, Wang C, Zhao L, Dong Y, Zhao Y, Zhang W (2023) Variability of tintinnid ciliate communities with water masses in the western Pacific Ocean. J Plankton Res 45(3):509–522. https://doi.org/10.1093/plankt/fbad011

    Article  CAS  Google Scholar 

  • Longhurst AR (1981) Analysis of marine ecosystems. Academic Press, London, p 741

    Google Scholar 

  • López-Abbate MC (2021) Microzooplankton communities in a changing ocean: a risk assessment. Diversity 13(2):82

    Article  Google Scholar 

  • McManus GB, Santoferrara LF (2013) Tintinnids in microzooplankton communities. The biology and ecology of tintinnid ciliates: models for marine plankton, 198–213

  • Middlebrook K, Emerson CW, Roff JC, Lynn DH (1987) Distribution and abundance of tintinnids in the Quoddy Region of the Bay of Fundy. Can J Zool 65(3):594–601

    Article  Google Scholar 

  • Naidu DW (1986) Tintinnid swarms of Portonovo waters. Mahasagar Bull Natl Inst Oceanogr 19(1):23–27

    Google Scholar 

  • Omori M, Hamner WM (1982) Patchy distribution of zooplankton: behavior, population assessment and sampling problems. Mar Biol 72:193–200

    Article  Google Scholar 

  • Pierce RW, Turner JT (1992) Ecology of planktonic ciliates in marine food webs. Rev Aquat Sci 6(2):139–181

    Google Scholar 

  • Pond S, Pickard GL (1983) Introductory Dynamic Oceanography. Pergamon Press, New York, p 240

  • Resplandy L, Lévy M, Madec G, Pous S, Aumont O, Kumar V (2011) Contribution of mesoscale processes to nutrient budgets in the Arabian Sea. J Geophys Res 116:C11007. https://doi.org/10.1029/2011JC007006

    Article  Google Scholar 

  • Rodriguez F, Varela M, Fernandez E, Zapata M (2003) Phytoplankton and pigment distributions in an anticyclonic slope water oceanic eddy (SWODDY) in the southern Bay of Biscay. Mar Biol 143(5):995–1011. https://doi.org/10.1007/s00227-003-1129-1

    Article  CAS  Google Scholar 

  • Shafeeque M, Balchand AN, Shah P, George G, Smitha BR, Eldho V, Joseph, AK, Sathyendranath S, Platt T (2021) Spatio-temporal variability of chlorophyll-a in response to coastal upwelling and mesoscale eddies in the South Eastern Arabian Sea. Int J Remote Sens 42(13):4840–4867

    Article  Google Scholar 

  • Shankar D, Shetye SR (1997) On the dynamics of the Lakshadweep high and low in the southeastern Arabian Sea. J Geophys Res: Oceans 102(C6):12551–12562

    Article  Google Scholar 

  • Shankar D, Remya R, Anil AC, Vijith V (2019) Role of physical processes in determining the nature of fisheries in the eastern Arabian Sea. Prog Oceanogr 172:124–158

    Article  Google Scholar 

  • Shetye SR, Gouveia AD, Shenoi SSC, Sundar D, Michael GS, Almeida AM, Santanam K (1990) Hydrography and circulation off the west coast of India during the southwest monsoon 1987. J Mar Res 48:359–378

    Article  Google Scholar 

  • Shyni TN, Hareesh Kumar PV (2014) The influence of meso-scale eddies on the current field and thermal structure of the southeastern Arabian Sea. Int J Remote Sens 35(14):5479–5496

    Article  Google Scholar 

  • Sivasankar R, Kumar PS, Ezhilarasan P, Naidu SA, Rao GD, Kanuri VV, Rao VR, Ramu K (2017) Swarm of Tintinnopsis uruguayensis in the estuarine waters of Kochi, Southwest coast of India. Food Webs 13:30–32

    Article  Google Scholar 

  • Smitha BR, Sanjeevan VN, Vimal Kumar KG, Revichandran C (2008) On the upwelling off the southern tip and along the west coast of India. J Coastal Res 24(4C):95–102

    Article  Google Scholar 

  • Spilling K, San Martín MA, Granlund M, Schulz KG, Vanharanta M, Goldenberg S, Riebesell U (2023) Microzooplankton communities and their grazing of phytoplankton under artificial upwelling in the oligotrophic ocean. Front Mar Sci 10:1286899

    Article  Google Scholar 

  • Stelfox-Widdicombe CE, Archer SD, Burkill PH, Stefels J (2004) Microzooplankton grazing in Phaeocystis and diatom-dominated waters in the southern North Sea in spring. J Sea Res 51:37–51

    Article  Google Scholar 

  • Sudheesh V, Gupta GVM, Sudharma KV, Naik H, Shenoy DM, Sudhakar M, Naqvi SWA (2016) Upwelling intensity modulates N2O concentrations over the western Indian shelf. J Geophys Res (oceans) 121(12):8551–8565

    Article  CAS  Google Scholar 

  • ter Braak CJF, Šmilauer P (2002) CANOCO 4.5. Reference Manual and CanoDraw for Windows User’s Guide: Software for Canonical Community Ordination. Version 4.5. Microcomputer Power, Ithaca, New York, USA

  • Thomas LC, Padmakumar KB, Smitha BR, Devi CA, Nandan SB, Sanjeevan VN (2013) Spatio-temporal variation of microphytoplankton in the upwelling system of the south-eastern Arabian Sea during the summer monsoon of 2009. Oceanologia 55(1):185–204

    Article  Google Scholar 

  • Thushara V, Vinayachandran PN (2020) Unprecedented surface chlorophyll blooms in the southeastern Arabian Sea during an extreme negative Indian Ocean Dipole. Geophys Res Lett 47(13):e2019GL085026

    Article  Google Scholar 

  • UNESCO (1994) Protocols for the joint global ocean flux study (JGOFS). Core Measurements. UNESCO, Paris 29: 170

  • Verity PG (1987) Abundance, community composition, size distribution, and production rates of tintinnids in Narragansett Bay, Rhode Island. Estuarine Coast Shelf Sci 24:671–690

    Article  CAS  Google Scholar 

  • Vishnu NNS, Sachin TS, Rasheed K (2020) Dynamics and forcing mechanisms of upwelling along the south eastern Arabian sea during south west monsoon. Reg Stud Mar Sci 40:101519. https://doi.org/10.1016/j.rsma.2020.101519,1-11

    Article  Google Scholar 

  • Vishnu NNS, Sarma YVB, Rasheed K, Gupta GVM (2022) Influence of dynamic stability on chlorophyll distribution along the eastern Arabian Sea. Cont Shelf Res 236:104678

    Article  Google Scholar 

  • Wickham SA, Steinmair U, Kamennaya N (2011) Ciliate distributions and forcing factors in the Amundsen and Bellingshausen Seas (Antarctic). Aquat Microb Ecol 62(3):215–230

    Article  Google Scholar 

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Acknowledgements

Authors acknowledge the Secretary, Ministry of Earth Sciences for providing the facilities and support. We thank Dr. M. Sudhakar, former Director, Centre for Marine Living Resources and Ecology whose support greatly helped in the implementation of the project Marine Ecosystem Dynamics of Eastern Arabian Sea (MEDAS) under the Marine Living Resources Programme. All the participants of MEDAS cruises who rendered help in sampling are acknowledged. Satellite-derived SST and Chlorophyll data are taken from Aqua-MODIS, SLA and Geostrophy currents retrieved from AVISO/Miller are duly acknowledged. Authors acknowledge the anonymous reviewers for constructive comments that improved the manuscript. This is CMLRE contribution number 173.

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Ministry of Earth Sciences (MoES), India.

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Authors and Affiliations

  1. Centre for Marine Living Resources and Ecology, Ministry of Earth Sciences, Kochi, 682508, India

    C. R. Asha Devi, Jhimli Mondal, N. N. S. Vishnu, C. K. Sherin, I. Anandavelu & G. V. M. Gupta

  2. CSIR-National Institute of Oceanography, Regional Centre, Kochi, 682018, India

    N. N. S. Vishnu & K. J. Albin

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  1. C. R. Asha Devi
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  2. Jhimli Mondal
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  3. N. N. S. Vishnu
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Contributions

CRAD: conceptualization, data analysis, validation and interpretation, writing. JM: sample and data analysis, writing. NNSV: physical oceanography data analysis, plotting and writing. CKS: nutrient analysis, plotting and writing. KJA: chlorophyll data analysis, plotting and writing. IA: statistical analysis and writing. GVMG: editorial corrections.

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Correspondence to C. R. Asha Devi.

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Asha Devi, C.R., Mondal, J., Vishnu, N.N.S. et al. Factors regulating proliferation and co-occurrence of loricate ciliates in the microzooplankton community from the eastern Arabian Sea. Aquat Sci 86, 31 (2024). https://doi.org/10.1007/s00027-024-01047-0

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