Abstract
Unraveling planktonic community patterns and their linkage with the surrounding ecology is essential for aquatic resource management. Studies on the tintinnid microzooplankton in most of the marine waters of Malaysian South China Sea (SCS) are scarce though the trophic role of this community is well established. Thus, we aimed to investigate on spatiotemporal pattern of composition, abundance, and biomass of tintinnid, and how this community patterns are regulated with the basic ecological parameters. A total of 46 species were recorded, mostly in southwest monsoon (33 species) during the study period from May 2016 to April 2017. Tintinnopsis was counted as major genera with 19 species, and Tintinnopsis radix, a species that reported as neritic-estuarine origin calculated as the most abundant (11%) in our study. Both the space and time were equally responsible for differences in species richness, diversity, abundance, and biomass. However, species richness variation was not influenced by space–time interaction, whereas we observed season (time) and species size worked as a strong factor in terms of biomass variations. Accordingly, the higher mean abundance (Station 3; 132,116 ind m−3 in southwest monsoon) did not scale up to the bigger mean biomass (Station 4; 1.317 µgC L−1 in Inter-monsoon April). Among the ecological variables, the strongest influence was observed in the tintinnid community by pH, dissolved oxygen and salinity mostly during southwest monsoon around Bintulu-Mukah areas. Similarly, species-specific affinity to pH was also observed by most of the species. In addition, Favella campanula showed affinity to salinity, turbidity, and conductivity, while T. cylindrica and T. gracilis were driven by the temperature and dissolved oxygen. The findings of this research may help to explore comprehensive food web dynamics in future ecosystem studies in SCS region.
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Abdullah Al, M., Alam, M. D., Akhtar, A., Xu, H., Islam, M. S., Abu Hena, M. K., Uddin, M. M., & Alam, M. W. (2018). Annual pattern of zooplankton communities and their environmental response in a subtropical maritime channel system in the northern Bay of Bengal, Bangladesh. Acta Oceanologica Sinica, 37, 1–9.
Aberle, N., Bauer, B., Lewandowska, A., Gaedke, U., & Sommer, U. (2012). Warming induces shifts in microzooplankton phenology and reduces time-lags between phytoplankton and protozoan production. Marine Biology. https://doi.org/10.1007/s00227-012-1947-0
Abu Hena, M. K., Idris, M. H., Hafizuddin, M., Bhuiyan, K. A., Aiman, W. M., Nesarul, M. H., & Kumar, U. (2016b). Diversity and composition of fish from Kuala Nyalau River estuary, Bintulu, Sarawak, Malaysia. Malaysia: Fundamental Science Congress 2016, Universiti Putra Malaysia.
Abu Hena, M. K., Idris, M. H., Khairul, R. M. Y., Bhuiyan, K. A., Nesarul, M. H., & Kumar, U. (2016a). Diversity of macro-benthos in the mangrove forest of Kuala Sibuti, Miri, Sarawak. Malaysia: Malaysia International Biology Symposium 2016, Putrajaya.
Bachy, C., Moreira, D., Dolan, J. R., & López-García, P. (2013). Seasonal dynamics of free-living tintinnid ciliate communities revealed by environmental sequences from the North-West Mediterranean Sea. FEMS Microbiology Ecology, 87, 330–342.
Billah, M. M., Abu Hena, M. K., Idris, M. H., & Ismail, J. (2017). Mangrove macroalgae as biomonitors of heavy metal contamination in a tropical estuary, Malaysia. Water, Air, Soil Pollution, 228, 347. https://doi.org/10.1007/s11270-017-3500-8
Biswas, S. N., Godhantaraman, N., Rakshit, D., & Sarkar, S. K. (2013). Community composition, abundance, biomass and production rates of Tintinnids (Ciliata: Protozoa) in the coastal region of Sundarban Mangrove wetland, India. Indian J Geo Mar Sci, 42, 163–173.
Boero, F. (1994). Fluctuations and variations in coastal marine environments. Marine Ecology, 15, 3–25.
Cao, M. S. B., Beigt, D., & Piccolo, C. (2005). Temporal variability of diversity and biomass of tintinnids (Ciliophora) in a southwestern Atlantic temperate estuary. Journal of Plankton Research, 27, 1103–1111.
Caron, D. A., & Hutchins, D. A. (2013). The effect of changing climate on microzooplankton grazing and community structure: Drivers, predictions and knowledge gaps. Journal of Plankton Research, 35(2), 235–252.
Casas-Monroy, O., Linley, R. D., Adams, J. K., Chan, F. T., Drake, D. A. R., & Bailey, S. A. (2015). Relative invasion risk for plankton across marine and freshwater systems: Examining efficacy of proposed international ballast water discharge standards. PLoS ONE, 10(3), e0118267. https://doi.org/10.1371/journal.pone.0118267
Chen, B., Liu, H., Landry, M. R., Dai, M., Huang, B., & Sun, J. (2009). Close coupling between phytoplankton growth and microzooplankton grazing in the western South China Sea. Limnology and Oceanography, 54, 1084–1097.
Chen, C. T. A. (2008). Distributions of nutrients in the East China Sea and the South China Sea connection. Journal of Oceanography, 64, 737–751.
Dash, S., Behera, R. K., Mohapatra, P. K., Sarangi, R. K., Raut, D., Pati, A., & Patanik, L. (2017). Species composition of microzooplankton Tintinnid from the coastal waters of Digha, Bay of Bengal. Environmental Monitoring and Assessment, 189(6), 258. https://doi.org/10.1007/s10661-017-5961-z
DiBacco, C., Humphrey, D. B., Nasmith, L. E., & Levings, C. D. (2012). Ballast water transport of non-indigenous zooplankton to Canadian ports. ICES Journal of Marine Science, 69(3), 483–491.
Dolan, J. R. (2012). Introduction to tintinnids. In J. R. Dolan, D. J. S. Montagnes, S. Agatha, D. W. Coats, & D. K. Stoecker (Eds.), The biology and ecology of Tintinnid ciliates: models for marine plankton (pp. 1–16). Chichester: Wiley.
Dolan, J. R., Gimenez, A., Cornet-Barthaux, V., & de Verneil, A. (2016). Community structure of tintinnid ciliates of the microzooplankton in the South West Pacific Ocean: Comparison of a high primary productivity with a typical oligotrophic site. Journal of Eukaryotic Microbiology, 63, 813–822.
Dolan, J. R., Ritchie, M. E., & Ras, J. (2007). The “neutral” community structure of planktonic herbivores, tintinnid ciliates of the microzooplankton, across the SE tropical Pacific Ocean. Biogeosciences, 4, 297–310.
Dolan, J. R., Yang, E. J., Lee, S. H., & Kim, S. Y. (2013). Tintinnids ciliates of Amundsen Sea (Antarctica) plankton communities. Polar Research. https://doi.org/10.3402/polar.v32i0.19784
Dunthorn, M., Lipps, J. H., Dolan, J. R., Saab, M. A., Aescht, E., Bachy, C., de Cao, M. S. B., Berger, H., et al. (2015). Ciliates-Protist with complex morphologies and ambiguous early fossil record. Marine Micropaleontology, 119, 1–6.
Elangovan, S. S., Kumar, M. A., Karthik, R., Sankar, R. S., Jayabarathi, R., & Padmavati, G. (2012). Abundance, species composition of microzooplankton from the coastal waters of Port Blair, South Andaman Island. Aquatic Biosystems, 8, 20. https://doi.org/10.1186/2046-9063-8-20
Feng, M., Zhang, W., Zhang, C., Xiao, T., & Li, C. (2010). Horizontal distribution of large tintinnids in the northern South China Sea. Journal of Tropical Oceanography, 29, 141–150.
Garces, L. R., Alias, M., Abu Talib, A., Mohamad-Norizam, M., & Silvestre, G. T. (2003). A trophic model of the coastal fisheries ecosystem off the West Coast of Sabah and Sarawak, Malaysia. In: G. Silvestre, L. Garces, I. Stobutzki, M. Ahmed, R. A. Valmonte-Santos, C. Luna, L. Lachica-Alino, & P. Munro (Eds.), Assessment, management and future directions for coastal fisheries in Asian Countries (vol. 67, pp. 333–335). WorldFish center conference proceedings.
Gavrilova, N., & Dolan, J. R. (2007). A note on species list and ecosystem shifts: Black Sea tintinnids, ciliates of the microzooplankton. Acta Protozoologica, 46, 279–288.
Godhantaraman, N., & Uye, S. (2003). Geographical and seasonal variations in taxonomic composition, abundance and biomass of microzooplankton across a brackish-water lagoonal system of Japan. Journal of Plankton Research, 25, 465–482.
Gomez, F. (2007). Trends on the distribution of ciliates in the open Pacific Ocean. Acta Oecologica, 32, 188–202.
Hada, Y. (1938). Studies on the tintinnoinea from the Western Pacific. Journal of the Faculty of Science, Hokkaido University Series, 6(6), 87–190.
Heneash, A. M. M., Abdel-Rahman, N. S., & Gharib, S. M. (2015). Community composition abundance and biomass of tintinnids (Ciliata: Protozoa) in the Western Harbour, south-eastern Mediterranean Sea, Egypt. Environmental Monitoring and Assessment, 187, 517.
Hillebrand, H., Dürselen, C., Kirschtel, D., Pollingher, U., & Zohary, T. (1999). Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology, 35, 403–424.
Hoque, M. M., Abu Hena, M. K., Idris, M. H., Ahmed, O. H., Saifullah, A. S. M., & Billah, M. M. (2015). Status of some fishery resources in a tropical mangrove estuary of Sarawak, Malaysia. Marine Biology Research, 11, 834–846.
James, M. R. (1991). Sampling and preservation methods for the quantitative enumeration of microzooplankton. New Zealand Journal of Marine and Freshwater Research, 25, 305–310.
Jiang, Y., Yang, E. J., Min, J. O., Kang, S. H., & Lee, S. (2013). Using pelagic ciliated microzooplankton communities as an indicator for monitoring environmental condition under impact of summer sea-ice reduction in Western Arctic ocean. Ecological Indicators, 34, 380–390.
Johan, I., Abu Hena, M. K., Idris, M. H., & Arshad, A. (2013). Taxonomic composition and abundance of zooplankton copepoda in the coastal waters of Bintulu, Sarawak, Malaysia. Journal of Fisheries and Aquatic Science, 8, 472–479.
Kofoid, C. A., & Campbell, A. S. (1939). The tintinnoinea of the Eastern Tropical Pcific. Bulletin of the Museum of Comparative Zoology at Harvard College, 84, 1–473.
Kogan, M. (2005). Estudio de la composición específica, abundancia y distribución espacial del microzooplancton (Protozoos y micrometazoos) en el estuario del Río de La Plata (Argentina-Uruguay). Ph.D. thesis, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Buenos Aires, Argentina.
Krsinic, F., Grbec, B. (2006). Horizontal distribution of tintinnids in the open waters of the South Adriatic (Eastern Mediterraean). Scientia Marina, 70, 77–88.
Horton. et al. (2020). World register of marine species (WoRMS). http://www.marinespecies.org/. Retrieved July 25, 2020.
Li, H., Wang, C., Liang, C., Zhao, Y., Zhang, W., Gregori, G., & Xiao, T. (2019). Diversity and distribution of tintinnid ciliates along salinity gradient in the Pearl River estuary in Southern China. Estuarine, Coastal and Shelf Science, 226, 106268. https://doi.org/10.1016/j.ecss.2019.106268
Li, H., Zhang, W., Zhao, Y., Zhao, L., Dong, Y., Wang, C., Liang, C., & Xiao, T. (2018). Tintinnid diversity in the tropical West Pacific Ocean. Acta Oceanologica Sinica, 37, 218–228.
Liang, Z., Xing, T., Wang, Y., & Zeng, L. (2019). Mixed layer heat variations in the South China Sea observed by Argo Float and reanalysis data during 2012–2015. Sustainability, 11, 5429. https://doi.org/10.3390/su11195429
Lopez-Abbate, M. C. (2021). Microzooplankton communities in a changing ocean: A risk assessment. Diversity, 13, 82. https://doi.org/10.3390/d13020082
Lynn, D. H. (Ed.). (2008). The ciliated protozoa: Characterization, classification, and guide to the literature (3rd ed., p. 605). Springer.
Molina, A., Duque, G., & Cogua, P. (2020). Influence of environmental conditions in the fish assemblage structure of a tropical estuary. Marine Biodiversity, 50, 5. https://doi.org/10.1007/s12526-019-01023-0
Morgan, J. R., & Valencia, M. J. (1983). The natural environment setting. In J. R. Morgan & M. J. Valencia (Eds.), Atlas for Marine Policy in Southeast Asian Seas (pp. 56–86). University of California Press.
Muhamad, N., & Rahim, S. A. K. (2014). Preliminary study on fish larvae at selected coastal waters of Sarawak. Born Journal of Research in Science Teaching, 4(2), 1–8.
Njire, J., Batistic, M., Kovacevic, V., Garic, R., & Bensi, M. (2019). Tintinnid ciliates communities in pre-and post-winter conditions in the Southern Adriatic Sea (NE Mediterranean). Water, 11, 2329.
Omori, M., & Ikeda, T. (1984). Methods in marine zooplankton ecology (p. 332). Wiley.
Pielou, E. C. (1966). The measurement of diversity in different types of biological collections. Journal of Theoretical Biology, 13, 131–144.
R Core Team. (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.
Sabri, W. M., Manaf, O. A., & Minhat, F. I. (2019). Distribution and diversity of foraminifera in the north-west of Sarawak offshore waters, Malaysia. Journal of Undergraduate Research Universiti Malaysia Terengganu, 1, 19–25.
Sacca, A., & Giuffre, G. (2013). Biogeography and ecology of Rhizodomus tagatzi, a presumptive invasive tintinnid ciliate. Journal of Plankton Research, 35, 894–906.
Saifullah, A. S. M., Abu Hena, M. K., Idris, M. H., & Rajaee, A. H. (2019). Community composition and diversity of phytoplankton in relation to environmental variables and seasonality in a tropical mangrove estuary. Regional Studies in Marine Science, 32, 100826. https://doi.org/10.1016/j.rsma.2019.100826
Saifullah, A. S. M., Abu Hena, M. K., Idris, M. H., Rajaee, A. H., & Bhuiyan, M. K. A. (2015). Phytoplankton in tropical mangrove estuaries: Role and interdependency. Forest Science and Technology, 12, 104–113.
Saifullah, A. S. M., Abu Hena, M. K., Idris, M. H., Rajaee, A. H., & Johan, I. (2014). Composition and diversity of phytoplankton from mangrove estuaries in Sarawak, Malaysia. Journal of Biological Sciences, 14, 361–369.
Shamsudin, L., Yasin, A. H., Razak, S. A., & Yusoff, M. S. (1999). Microplankton on distribution in the South China Sea. Area II: Sarawak, Sabah and Brunei Darussalam waters. In: Proc. 2nd Tech. Sem. Mar. Fish. Resour. Surv. South China Sea. Area II: west coast of Sabah, Sarawak and Brunei Darussalam, 14–15 Dec 1998. SEAFDEC, Kuala Lampur, Malaysia (pp. 197–223).
Shannon, C. E., & Weaver, W. (1963). The mathematical theory of communication. University of Illinois Press.
Stoecker, D. K., & Capuzzo, J. M. (1990). Predation on protozoa: Its importance to zooplankton. Journal of Plankton Research, 12, 891–908.
Su, Q., Huang, L., Tan, Y., Xu, R., Li, T., Xu, Z., Zhang, J., & Qiu, D. (2007). Preliminary study of microzooplankton grazing and community composition in the north of South China Sea in Autumn. Marine Science Bulletin, 9, 43–53.
Sun, J., & Liu, D. (2003). Geometric models for calculating cell biovolume and surface area for phytoplankton. Journal of Plankton Research, 25, 1331–1346.
Urrutxurtu, I. (2004). Seasonal succession of tintinnids in the Nervión river estuary, Basque Country, Spain. Journal of Plankton Research, 26, 307–314.
Van der Putten, W. H., Macel, M., & Visser, M. E. (2010). Predicting species distribution and abundance responses to climate change: Why it is essential to include biotic interactions across trophic levels. Philosophical Transactions of the Royal Society of London Series B, 365, 2025–2034.
Vaque, D., Blough, H. A., & Duarte, C. M. (1997). Dynamics of ciliate abundance, biomass and community composition in an oligotrophic coastal environment (NW Mediterranean). Aquatic Microbial Ecology, 12, 71–83.
Verity, P. G., & Lagdon, C. (1984). Relationships between lorica volume, carbon, nitrogen, and ATP content of tintinids in Narragansett Bay. Journal of Plankton Research, 6, 859–868.
Wang CF, Zhao L, Zhao Y, Li HB, Chen X, Zhang S, Zhang WC, Xiao T (2018) Vertical distribution of planktonic ciliates in tropical Western Pacific. Deep-Sea Res. Pt. II.
Wang, Y., Zhang, W., Lin, Y., Cao, W., Zheng, L., & Yang, J. (2014a). Phosphorus, nitrogen and chlorophyll-a are significant factors controlling ciliate communities in summer in the northern Beibu Gulf, South China Sea. PLoS ONE, 9(7), e101121.
Wang, Y., Zhang, W., Lin, Y., Zheng, L., Cao, W., & Yang, J. (2014b). Spatial and seasonal variations of large tintinnid ciliates in Shenhu Bay of China. Oceanological and Hydrobiological Studies, 43, 292–302.
Wang, Z., Qi, Y., Chen, J., Xu, N., & Yang, Y. (2006). Phytoplankton abundance, community structure, and nutrients in cultural areas of Daya Bay, South China Sea. Journal of Marine Systems, 62, 85–94.
Wang, Z., Zhao, J., Zhang, Y., & Cao, Y. (2009). Phytoplankton community structure and environmental parameters in aquaculture areas of Daya Bay, South China Sea. Journal of Environmental Sciences, 21, 1268–1275.
Wu, M. L., Wang, Y. S., Wang, Y. T., Sun, F. L., Sun, C. C., Jiang, Z. Y., & Cheng, H. (2014). Influence of environmental changes on phytoplankton pattern in Daya Bay, South China Sea. Revista De Biología Marina y Oceanografía, 49, 323–337.
Yong, Y. L., Chew, L. L., Lee, C. W., & Chong, V. C. (2016). Monsoonal and lunar variability in microzooplankton abundance and community structure in the Terusan mangrove creek (Malaysia). Marine Biology Research, 12, 278–293.
Yu, Y., Ma, Y., Chen, W., Wang, Q., & Zhang, W. (2016). Community structure of large tintinnids (Ciliophora, Tintinnida) in Bohai Bay during spring and summer. Marine Sciences, 40, 57–61.
Yu, Y., Zhang, W., Zhao, N., Sun, X., Zhang, C., Feng, M., & Xiao, T. (2011). Annual variations in the abundance and biomass of planktonic ciliate in the Jiaozhou Bay. Oceanology and Limnology Sin, 42, 690–701.
Zeng, X., Peng, S., Li, Z., Qi, Y., & Chen, R. (2014). A reanalysis dataset of the South China Sea. Science Data, 1, 140052. https://doi.org/10.1038/sdata.2014.52
Zhang, H., Liu, C., Jin, X., Shi, J., Zhao, S., & Jian, Z. (2016). Dynamics of primary productivity in the northern South China Sea over the past 24,000 years. Geochemistry, Geophysics, Geosystems, 17, 4878–4891.
Zhang, Y., Wang, X., & Yin, K. (2018). Spatial contrast in phytoplankton, bacteria and microzooplankton grazing between the eutrophic Yellow Sea and the oligotrophic South China Sea. Chinese Journal of Oceanology and Limnology, 36, 92–104.
Zhou, L., Tan, Y., Huang, L., Huang, J., Liu, H., & Lian, X. (2011). Phytoplankton growth and microzooplankton grazing in the continental shelf area of northeastern South China Sea after typhoon Fengshen. Continental Shelf Research, 31, 1663–1671.
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The authors would like to thanks to Water Quality & Ecology lab, Universiti Putra Malaysia, campus Bintulu for technical support and facilities provided.
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This work was supported by the Malaysian Government under E-Science grant (04-01-04-SF1422) and Universiti Malaysia Terengganu, ref. UMT/CRIM/2-2/2/20 (79), project number 55211.
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Kumar, U., Abu Hena, M.K. contributed to concept; sampling was done by Kumar, U., Abu Hena, M.K., Johan, I.; microscopy analysis was done by Kumar, U., data analysis was done by Kumar, U., Muyassar, H.A., Das, J.; resources were gathered by Idris, M.H., Abu Hena, M.K.; writing original of the draft was done by Kumar, U.; writing—review and editing were done by Abu Hena, M.K., Karim, N.U., Rasdi, W.N., Das, J., Muyassar, H.A.; visualization of the study was done by Kumar, U., Muyassar, H.A.; supervision was carried out by Abu Hena, M.K.; project administration was done by Abu Hena, M.K.; funding acquisition was done by Abu Hena, M.K. All authors have read and agreed to the research contribution.
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Kumar, U., Kamal, A.M., Karim, N.U. et al. Spatiotemporal variation of tintinnid microzooplankton (Ciliophora: tintinnina) from Sarawak inshore water, South China Sea. COMMUNITY ECOLOGY 22, 351–365 (2021). https://doi.org/10.1007/s42974-021-00059-2
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DOI: https://doi.org/10.1007/s42974-021-00059-2