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Inter-annual variability of phytoplankton assemblage and Tetraspora gelatinosa bloom from anthropogenically affected harbour, Veraval, India

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Abstract

Veraval, one of Asia’s largest fishing harbours, situated on the south-west coast of Gujarat, India, has transformed into an industrial hub dominated by fish processing units, rayon manufacturing industry, and transportation facilities. The study investigated the high abundance of Tetraspora gelatinosa along with the augmented level of ammonia in the harbour. The high concentration of ammonia was associated with the accumulation of sewage, industrial, and fishery wastes in the harbour. Low-energy expenditure associated with assimilation of ammonia made it a principal nitrogen source for Tetraspora gelatinosa growth. Even though ammonia is the preferred nitrogen source by phytoplankton, elevated concentration causes toxicity to the cells. Augmented level of ammonia and high TSS hampered the efficiency of PS II, thereby impeding the chlorophyll a degradation and oxygen evolution. Built of the organic load from fish processing industries as well as domestic waste along with a reduction in photosynthetic oxygen evolution has made the harbour hypoxic (DO < 1.6 mg L−1)/anoxic (DO = 0.0 mg L−1). Shannon-Wiener diversity index as a pollution index suggested that the inner harbour area was highly polluted as the diversity ranged from 0.01 to 1.57. Whereas, the outer harbour (Near-shore and off-shore) with less anthropogenic effect recorded high diversity (av. 2.17) suggesting a healthy environment.

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References

  • Achary, M. S., Panigrahi, S., Satpathy, K. K., Sahu, G., Mohanty, A. K., Selvanayagam, M., & Panigrahy, R. C. (2014). Nutrient dynamics and seasonal variation of phytoplankton assemblages in the coastal waters of southwest Bay of Bengal. Environmental Monitoring and Assessment, 186, 5681–5695.

    Article  CAS  Google Scholar 

  • APHA (American Public Health Association). (2005). Standard methods for examination of water and waste water. Washington.

  • Baliarsingh, S. K., Sahu, B. K., Srichandan, S., & Sahu, K. C. (2012). Seasonal variation of phytoplankton community in navigable channel of Gopalpur Port, East Coast of India: a taxonomic study. International Journal of Modern Botany, 2, 40–46.

    Article  Google Scholar 

  • Balloch, D., Davies, C. E., Jones, F. H. (1976). Biological assessment of water quality in three British rivers: the North Esk (Scotland), the Ivel (England) and the Taf (Wales). Water Poll Cont (UK).

  • Bhadja, P., Poriya, P., Kundu, R. (2014). Community structure and distribution pattern of intertidal invertebrate macrofauna at some anthropogenically influenced coasts of Kathiawar peninsula (India). Advances in Ecology, 2014.

  • Bistricki, T., & Munawar, M. (1978). A rapid preparation method for scanning electron microscopy of Lugol preserved algae. Journal of Microscopy, 114, 215–218.

    Article  Google Scholar 

  • Borade, S., Dhawde, R., Maloo, A., Gajbhiye, S. N., Ram, A., & Dastager, S. G. (2015). Assessment of enteric bacterial indicators and correlation with physico-chemical parameters in Veraval coast, India. Indian Journal of Geo-Marine Sciences, 44, 501–507.

    Google Scholar 

  • Chalar, G. (2009). The use of phytoplankton patterns of diversity for algal bloom management. Limnologica-Ecology and Management of Inland Waters, 39, 200–208.

    Article  CAS  Google Scholar 

  • Clarke, K. R., Warwick, R. M., (1994). Change in marine communities. Plymouth Marine Laboratory.

  • CPCB (2009–2010). Status of water supply, waste water generation and treatment in class I cities and class II towns of India in control of urban pollution series. CUPS/70/2009–10.

  • Dayala, V. T., Salas, P. M., & Sujatha, C. H. (2014). Spatial and seasonal variations of phytoplankton species and their relationship to physico-chemical variables in the Cochin estuarine waters, Southwest coast of India. Indian Journal of Geo-Marine Sciences, 43, 943–953.

    Google Scholar 

  • Dean, V. A. (2017). Water and wastewater examination manual (p. 264). Routledge publisher, ISBN 1351405071.

  • Desikachary, T. V. (1959). Cyanophyta. New Delhi: Indian Council of Agricultural Research.

    Google Scholar 

  • Diaz, R. J. (2001). Overview of hypoxia around the world. Journal of Environmental Quality, 30, 275–281.

    Article  CAS  Google Scholar 

  • Dortch, Q. (1990). The interaction between ammonium and nitrate uptake in phytoplankton. Marine Ecology Progress Series, 61, 183–201.

    Article  CAS  Google Scholar 

  • Drath, M., Kloft, N., Batschauer, A., Marin, K., Novak, J., & Forchhammer, K. (2008). Ammonia triggers photodamage of photosystem II in the cyanobacterium Synechocystis sp. strain PCC 6803. Plant Physiology, 147, 206–215.

    Article  CAS  Google Scholar 

  • Eby, L. A., & Crowder, L. B. (2002). Hypoxia-based habitat compression in the Neuse River Estuary: context-dependent shifts in behavioral avoidance thresholds. Canadian Journal of Fisheries and Aquatic Sciences, 59, 952–965.

    Article  Google Scholar 

  • Eppley, R. W., Coatsworth, J. L., & Solórzano, L. (1969). Studies of nitrate reductase in marine phytoplankton. Limnology and Oceanography, 14, 194–205.

    Article  CAS  Google Scholar 

  • Falkowski, P. G., & Owens, T. G. (1978). Effects of light intensity on photosynthesis and dark respiration in six species of marine phytoplankton. Marine Biology, 45, 289–295.

    Article  CAS  Google Scholar 

  • Feely, R. A., Alin, S. R., Newton, J., Sabine, C. L., Warner, M., Devol, A., & Maloy, C. (2010). The combined effects of ocean acidification, mixing, and respiration on pH and carbonate saturation in an urbanized estuary. Estuarine, Coastal and Shelf Science, 88, 442–449.

    Article  CAS  Google Scholar 

  • Field, J. G., Clarke, K. R., & Warwick, R. M. (1982). A practical strategy for analysing multispecies distribution patterns. Marine Ecology Progress Series, 8, 37–52.

    Article  Google Scholar 

  • Gao, X., & Song, J. (2005). Phytoplankton distributions and their relationship with the environment in the Changjiang estuary, China. Marine Pollution Bulletin, 50, 327–335.

    Article  CAS  Google Scholar 

  • Ghazala, B., Shameel, M., Choudhary, M. I., Shahzad, S., & Leghari, S. M. (2004). Phycochemistry and bioactivity of Tetraspora (Volvocophyta) from Sindh. Pakistan Journal of Botany, 36, 531–548.

    Google Scholar 

  • Giani, M., Djakovac, T., Degobbis, D., Cozzi, S., Solidoro, C., & Umani, S. F. (2012). Recent changes in the marine ecosystems of the northern Adriatic Sea. Estuarine, Coastal and Shelf Science, 115, 1–13.

    Article  Google Scholar 

  • Gilbert, D., Rabalais, N. N., Diaz, R. J., & Zhang, J. (2009). Evidence for greater oxygen decline rates in the coastal ocean than in the open ocean. Biogeosciences Discussions, 6, 9127–9160.

    Article  Google Scholar 

  • Glibert, P. M., & Goldman, J. C. (1981). Rapid ammonium uptake by marine phytoplankton. Mar. Ecol. Berlin, 2, 25–31.

    CAS  Google Scholar 

  • Glibert, P. M., Wilkerson, F. P., Dugdale, R. C., Raven, J. A., Dupont, C. L., Leavitt, P. R., Parker, A. E., Burkholder, J. M., & Kana, T. M. (2016). Pluses and minuses of ammonium and nitrate uptake and assimilation by phytoplankton and implications for productivity and community composition, with emphasis on nitrogen-enriched conditions. Limnology and Oceanography, 61, 165–197.

    Article  CAS  Google Scholar 

  • Gomes, H., Goes, J. I., Matondkar, S. P., Buskey, E. J., Basu, S., Parab, S., & Thoppil, P. (2014). Massive outbreaks of Noctiluca scintillans blooms in the Arabian Sea due to spread of hypoxia. Nature Communications, 5, 4862.

    Article  CAS  Google Scholar 

  • Graneli, E., Weberg, M., & Salomon, P. S. (2008). Harmful algal blooms of allelopathic microalgal species: the role of eutrophication. Harmful Algae, 8, 94–102.

    Article  CAS  Google Scholar 

  • Grasshoff, K. (1983). Methods of sea water analysis (2nd ed.). Veinheim: Verlag Chemie.

    Google Scholar 

  • Gutowski, A. N. T. J. E., Foerster, J. U. L. I. A., & Schaumburg, J. O. C. H. E. N. (2004). The use of benthic algae, excluding diatoms and Charales, for the asessment of the ecological status of running fresh waters: a case history from Germany. Oceanological and Hydrobiological Studies, 33(2), 3–15.

    CAS  Google Scholar 

  • Hagy, J. D., Boynton, W. R., Keefe, C. W., & Wood, K. V. (2004). Hypoxia in Chesapeake Bay, 1950–2001: longterm change in relation to nutrient loading and river flow. Estuaries, 27, 634–658.

    Article  CAS  Google Scholar 

  • Hardikar, R., Haridevi, C. K., Chowdhury, M., Shinde, N., Ram, A., Rokade, M. A., & Rakesh, P. S. (2017). Seasonal distribution of phytoplankton and its association with physico-chemical parameters in coastal waters of Malvan, west coast of India. Environmental Monitoring and Assessment, 189(4), 151.

    Article  Google Scholar 

  • Harnstrom, K., Karunasagar, I., & Godhe, A. (2009). Phytoplankton species assemblages and their relationship to hydrographic factors — a study at the old port in Mangalore, coastal Arabian Sea. Indian Journal of Marine Science, 38, 234–234.

    Google Scholar 

  • Howarth, R., Chan, F., Conley, D. J., Garnier, J., Doney, S. C., Marino, R., & Billen, G. (2011). Coupled biogeochemical cycles: eutrophication and hypoxia in temperate estuaries and coastal marine ecosystems. Frontiers in Ecology and the Environment, 9, 18–26.

    Article  Google Scholar 

  • Ismael, A. A. (2003). Succession of heterotrophic and mixotrophic dinoflagellates as well as autotrophic microplankton in the Harbour of Alexandria, Egypt. Journal of Plankton Research, 25, 193–202.

    Article  Google Scholar 

  • Jugnu, R. (2006). Studies on the prevalence of algal blooms along Kerala coast, India.

  • Kaparapu, J., Rao, G. N. (2013). Phytoplankton assemblages associated with water quality parameters in Meghadrigedda Reservoir of Visakhapatnam, Andhra Pradesh, India.

  • Kemp, W. M., Testa, J. M., Conley, D. J., Gilbert, D., & Hagy, J. D. (2009). Temporal responses of coastal hypoxia to nutrient loading and physical controls. Biogeosciences, 6, 2985–3008.

    Article  CAS  Google Scholar 

  • Labib, W. (2002). Phytoplankton variability in the Eastern Harbour (alexandria, Egypt). Egyptian Journal of Aquatic Biology and Fisheries, 6, 75–102.

    Article  Google Scholar 

  • Lohar, D. N., Korekar, S. L. (2015). Diversity of Chlorophyta in Freshwater Lakes of Sangli (MS) India. In National Conference on Advances in Bioscience & Environmental Science: Present & Future (ABES) (p. 127).

  • Majithiya, D., Yadav, A., & Ram, A. (2017). Behaviour of trace metals in the anoxic environment of Veraval Harbour, India. Marine Pollution Bulletin, 129, 645–654.

    Article  Google Scholar 

  • Malik, D. S., & Bharti, U. (2012). Status of plankton diversity and biological productivity of Sahastradhara stream at Uttarakhand, India. Journal of Applied and Natural Science, 4, 96–103.

    Article  Google Scholar 

  • Mandal, S. K., Patel, V. R., Temkar, G., George, B. M., & Raman, M. (2015). Bio-optic characterization of Discosphaera tubifer bloom occurs in an overcrowded fishing Harbour at Veraval, India. Environmental Monitoring and Assessment, 187, 597.

    Article  Google Scholar 

  • Maneeruttanarungroj, C., Lindblad, P., & Incharoensakdi, A. (2010). A newly isolated green alga, Tetraspora CU2551, from Thailand with efficient hydrogen production. International Journal of Hydrogen Energy, 35, 13193–13199.

    Article  CAS  Google Scholar 

  • Markou, G., Vandamme, D., & Muylaert, K. (2014). Ammonia inhibition on Arthrospira platensis in relation to the initial biomass density and pH. Bioresource Technology, 166, 259–265.

    Article  CAS  Google Scholar 

  • Markou, G., Depraetere, O., & Muylaert, K. (2016). Effect of ammonia on the photosynthetic activity of Arthrospira and Chlorella: a study on chlorophyll fluorescence and electron transport. Algal Research, 16, 449–457.

    Article  Google Scholar 

  • McCarthy, J. J., Taylor, W. R., & Taft, J. L. (1977). Nitrogenous nutrition of the plankton in the Chesapeake Bay, nutrient availability and phytoplankton preferences. Limnology and Oceanography, 22, 996–1011.

    Article  CAS  Google Scholar 

  • Middelburg, J. J., & Levin, L. A. (2009). Coastal hypoxia and sediment biogeochemistry. Biogeosciences, 6, 1273–1293.

    Article  CAS  Google Scholar 

  • Nagengast, B., kueznskakippen, T. N. (2014). Relation between chlorophyll and phaeophytin as indicator of disturbances in environment of flood plains ponds of the Warta River (Poland). Internation conference Wetland, “Wetland biodiversity and services: Tool for socio-ecological development” IX European wetland congress and 6 European pond conservation network, Spain, Volume: Book Abstract-169.

  • NIO. (2014). Report of Monitoring of Environmental Quality off Veraval.

  • NIO. (2015). Report of Monitoring of Environmental Quality off Veraval.

  • Olsen, P. S., & Mahoney, J. B. (2001). Phytoplankton in the Barnegat Bay—Little Egg Harbour estuarine system: species composition and picoplankton bloom development. Journal of Coastal Research, 115–143.

  • Paasche, E. (1971). Effect of ammonia and nitrate on growth, photosynthesis, and ribulose diphosphate carboxylase content of Dunaliella tertiolecta. Physiologia Plantarum, 25, 294–299.

    Article  CAS  Google Scholar 

  • Patil, J. S., & Anil, A. C. (2015). Effect of monsoonal perturbations on the occurrence of phytoplankton blooms in a tropical bay. Marine Ecology Progress Series, 530, 77–92.

    Article  Google Scholar 

  • Paerl, H. W., Pinckney, J. L., Fear, J. M., & Peierls, B. L. (1998). Ecosystem responses to internal and watershed organic matter loading: consequences for hypoxia in the eutrophying Neuse River Estuary, North Carolina, USA. Marine Ecology Progress Series, 166, 17–25.

  • Ram, A., Jaiswar, J. R., Rokade, M. A., Bharti, S., Vishwasrao, C., & Majithiya, D. (2014). Nutrients, hypoxia and Mass Fishkill events in Tapi Estuary, India. Estuarine, Coastal and Shelf Science, 148, 48–58.

    Article  CAS  Google Scholar 

  • Ramaiah, N., Ramaiah, N., & Nair, V. R. (1998). Phytoplankton characteristics in a polluted Bombay Harbour-Thana-Bassein creek estuarine complex. Indian Journal of Geo-Marine Sciences, 27, 281–285.

    CAS  Google Scholar 

  • Ranjan, G., Singh, N. P., & Singh, R. B. (2007). Physico-chemical characteristics of Ghariyarwa pond of Birganj, Nepal in relation to growth of phytoplankton. Nature, Environment and Pollution Technology, 6(4), 629.

    CAS  Google Scholar 

  • Reynolds, C. S. (1998). What factors influence the species composition of phytoplankton in lakes of different trophic status? In Phytoplankton and trophic gradients (pp. 11–26). Springer Netherlands.

  • Richter, D., Matuła, J., & Pietryka, M. (2014). The northernmost populations of T. gelatinosa (Chlorophyta) from Spitsbergen. Polish Polar Research, 35, 521–538.

    Article  Google Scholar 

  • Satoh, F., Hamasaki, K., Toda, T., & Taguchi, S. (2000). Summer phytoplankton bloom in Manazuru Harbour, Sagami Bay, central Japan. Plankton Biology and Ecology, 47, 73–79.

    Google Scholar 

  • Scavia, D., Rabalais, N. N., Turner, R. E., Justić, D., & Wiseman, W. J. (2003). Predicting the response of Gulf of Mexico hypoxia to variations in Mississippi River nitrogen load. Limnology and Oceanography, 48, 951–956.

    Article  CAS  Google Scholar 

  • Schnetzer, A., Miller, P. E., Schaffner, R. A., Stauffer, B. A., Jones, B. H., Weisberg, S. B., & Caron, D. A. (2007). Blooms of Pseudo-nitzschia and domoic acid in the San Pedro Channel and Los Angeles Harbour areas of the Southern California Bight, 2003–2004. Harmful Algae, 6, 372–387.

    Article  CAS  Google Scholar 

  • Seitzinger, S. P., Mayorga, E., Bouwman, A. F., Kroeze, C., Beusen, A. H. W., Billen, G., & Harrison, J. A. (2010). Global river nutrient export: a scenario analysis of past and future trends. Global Biogeochem Cycles, 24.

  • Shanthala, M., Hosmani, S. P., & Hosetti, B. B. (2009). Diversity of phytoplanktons in a waste stabilization pond at Shimoga Town, Karnataka State, India. Environmental Monitoring and Assessment, 151, 437–443.

    Article  CAS  Google Scholar 

  • Smith, V. H. (2003). Eutrophication of freshwater and coastal marine ecosystems a global problem. Environmental Science and Pollution Research, 10(2), 126–139.

    Article  CAS  Google Scholar 

  • Smith, V. H., Joye, S. B., & Howarth, R. W. (2006). Eutrophication of freshwater and marine ecosystems. Limnology and Oceanography, 51, 351–355.

    Article  CAS  Google Scholar 

  • Strickland, J. D. H., Parsons, T. R. (1972). In: A practical handbook of sea water analysis. Fish Res Board Canadian Bull (2nd ed.) Ottawa.

  • Subha Rao, D. V. (1969). Asterionella japonica bloom and discoloration off Waltair, Bay of Bengal. Limnology and Oceanography, 14, 632–634.

    Article  Google Scholar 

  • Subrahmanyan, R. (1946). A systematic account of the madras coast. Proceedings of the Indiana Academy of Sciences, 24, 85–197.

    Google Scholar 

  • Sundararajan, S., Khadanga, M. K., Kumar, J. P. P. J., Raghumaran, S., Vijaya, R., & Jena, B. K. (2017). Ecological risk assessment of trace metal accumulation in sediments of Veraval Harbor, Gujarat, Arabian Sea. Marine Pollution Bulletin, 114(1), 592–601.

    Article  CAS  Google Scholar 

  • Syrett, P. J., & Morris, I. (1963). The inhibition of nitrate assimilation by ammonium in Chlorella. Biochimica et Biophysica Acta (BBA)-Specialized Section on Enzymological Subjects, 67, 566–575.

    Article  CAS  Google Scholar 

  • Tam, N. F. Y., & Wong, Y. S. (1996). Retention and distribution of heavy metals in mangrove soils receiving wastewater. Environmental Pollution, 94, 283–291.

    Article  CAS  Google Scholar 

  • Testa, J. M., & Kemp, W. M. (2012). Hypoxia induced shifts in nitrogen and phosphorus cycling in Chesapeake Bay. Limnology and Oceanography, 57, 835–850.

    Article  CAS  Google Scholar 

  • Tomas, C. R. (Ed.). (1997). Identifying marine phytoplankton. California: Academic Press.

    Google Scholar 

  • Toppo, K., & Suseela, M. R. (2013). Enumeration of fresh water algal flora of Ranchi, Jharkhand, India. Journal of the Indian Botanical Society, 92, 89–96.

    Google Scholar 

  • UNESCO. (1994). Protocols for joint global ocean flux study. UNESCO.

  • Vinocur, A., & Pizarro, H. (2000). Microbial mats of twenty-six lakes from Potter Peninsula, King George island, Antarctica. Hydrobiologia, 437(1–3), 171–185.

    Article  Google Scholar 

  • Wang, X. C., Chen, R. F., & Gardner, G. B. (2004). Sources and transport of dissolved and particulate organic carbon in the Mississippi River estuary and adjacent coastal waters of the northern Gulf of Mexico. Marine Chemistry, 89(1–4), 241–256.

    Article  CAS  Google Scholar 

  • Wang, B., Chen, J., Jin, H., Li, H., Huang, D., & Cai, W. J. (2017). Diatom bloom derived bottom water hypoxia off the Changjiang estuary, with and without typhoon influence. Limnology and Oceanography, 62, 1552–1569.

    Article  CAS  Google Scholar 

  • Wright, J. J., Konwar, K. M., & Hallam, S. J. (2012). Microbial ecology of expanding oxygen minimum zones. Nature Reviews. Microbiology, 10, 381–394.

    Article  CAS  Google Scholar 

  • Yin, K., & Harrison, P. J. (2007). Influence of the Pearl River estuary and vertical mixing in Victoria Harbour on water quality in relation to eutrophication impacts in Hong Kong waters. Marine Pollution Bulletin, 54, 646–656.

    Article  CAS  Google Scholar 

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Acknowledgements

We are grateful to the director, CSIR-NIO, for facilitating the study. The authors would like to thank, former Scientist in Charge Dr. S. N. Gajbhiye and present Scientist in Charge Dr. A. K. Chaubey of regional centre Mumbai for their immense support in carrying out the research. We also express our sincere gratitude to three anonymous reviewers for their valuable comments and suggestions. Financial support from Coastal Ocean Monitoring and Predicting System (COMAPS), MoES, and OLP1708 are gratefully acknowledged. NIO contribution number is 6341.

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Hardikar, R., Haridevi, C.K., Ram, A. et al. Inter-annual variability of phytoplankton assemblage and Tetraspora gelatinosa bloom from anthropogenically affected harbour, Veraval, India. Environ Monit Assess 191, 87 (2019). https://doi.org/10.1007/s10661-019-7192-y

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