Skip to main content

Advertisement

SpringerLink
Log in

Hydrological regulation of Vibrio dynamics in a tropical monsoonal estuary: a classification and regression tree approach

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Dynamics of Vibrio populations in aquatic environments are of concern, as they encompass members pathogenic to humans as well as marine flora and fauna. Spatiotemporal distribution of its culturable abundance for a range of physicochemical and biological parameters in the Cochin estuary (CE), one of the largest tropical monsoonal estuary along the southwest coast of India, witnessed a proliferation of this bacterial group (707 ± 196 CFU ml−1) in downstream stations during a relative dry period. The study for the first time employed classification and regression tree (CART) along with multiple linear regression (MLR) based approaches to explore the nonlinear and linear interactions, respectively, among environmental variables regulating Vibrio abundance in CE. Both the techniques were on consensus to ascertain salinity as the primary determinant of Vibrio dynamics, during the entire sampling period regardless of the seasons, viz., dry and wet. Nevertheless, CART outperformed MLR in performance index, suggesting that in a dynamic system like estuaries, usage of the latter is limited by complex nonlinear relationships among environmental variables. According to CART, Vibrio proliferation observed in downstream stations of the estuary (salinity ≥ 13.4 psu) during a relative dry period was driven by eutrophication (dissolved inorganic phosphate ≥ 1.48 μM L−1) associated with reduced flushing resulting in an oxygen-limited environment (dissolved oxygen < 4.56 ml L−1), wherein phytoplankton production diverts to support microbes. Our results imply that anthropogenic activities and sea level rise in future may prompt Vibrio proliferation, to be a concern for public health and impinge on fisheries yield from tropical estuaries.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Akanda AS, Jutla AS, Islam S (2009) Dual peak cholera transmission in Bengal Delta: a hydroclimatological explanation. Geophys Res Lett 36

  • Akanda AS et al (2013) Population vulnerability to biannual cholera outbreaks and associated macro-scale drivers in the Bengal Delta. Am J Trop Med Hyg 89:950–959. https://doi.org/10.4269/ajtmh.12-0492

    Article  Google Scholar 

  • Ashok K, Guan Z, Yamagata T (2001) Impact of the Indian Ocean dipole on the relationship between the Indian monsoon rainfall and ENSO. Geophys Res Lett 28:4499–4502. https://doi.org/10.1029/2001GL013294

    Article  Google Scholar 

  • Ashok K, Guan Z, Saji N, Yamagata T (2004) Individual and combined influences of ENSO and the Indian Ocean dipole on the Indian summer monsoon. J Clim 17:3141–3155. https://doi.org/10.1175/1520-0442(2004)017<3141:IACIOE>2.0.CO;2

    Article  Google Scholar 

  • Asplund ME, Rehnstam-Holm AS, Atnur V, Raghunath P, Saravanan V, Härnström K, Collin B, Karunasagar I, Godhe A (2011) Water column dynamics of Vibrio in relation to phytoplankton community composition and environmental conditions in a tropical coastal area. Environ Microbiol 13:2738–2751

    Google Scholar 

  • Baird D, Christian RR, Peterson CH, Johnson GA (2004) Consequences of hypoxia on estuarine ecosystem function: energy diversion from consumers to microbes. Ecol Appl 14:805–822. https://doi.org/10.1890/02-5094

    Article  Google Scholar 

  • Bertone S, Giacomini M, Ruggiero C, Piccarolo C, Calegari L (1996) Automated systems for identification of heterotrophic marine bacteria on the basis of their fatty acid composition. Appl Environ Microbiol 62:2122–2132

    CAS  Google Scholar 

  • Blake PA (1994) Historical perspectives on pandemic cholera. In: Vibrio cholerae and Cholera. American Society of Microbiology, pp 293–295

  • Caburlotto G, Bianchi F, Gennari M, Ghidini V, Socal G, Aubry FB, Bastianini M, Tafi MC, Lleo MM (2012) Integrated evaluation of environmental parameters influencing Vibrio occurrence in the coastal Northern Adriatic Sea (Italy) facing the Venetian lagoon. Microb Ecol 63:20–31. https://doi.org/10.1007/s00248-011-9920-x

    Article  Google Scholar 

  • Clarke K, Gorley R (2006) PRIMER v6: user manual/tutorial (Plymouth routines in multivariate ecological research). Primer-E Ltd, Plymouth

    Google Scholar 

  • Colwell RR (1996) Global climate and infectious disease: the cholera paradigm*. Science 274:2025–2031

    CAS  Google Scholar 

  • Crump BC, Hopkinson CS, Sogin ML, Hobbie JE (2004) Microbial biogeography along an estuarine salinity gradient: combined influences of bacterial growth and residence time. Appl Environ Microbiol 70:1494–1505

    CAS  Google Scholar 

  • Deepanjali A, Kumar HS, Karunasagar I, Karunasagar I (2005) Seasonal variation in abundance of total and pathogenic Vibrio parahaemolyticus bacteria in oysters along the Southwest Coast of India. Appl Environ Microbiol 71:3575–3580

    CAS  Google Scholar 

  • Ferdous J, Sultana R, Rashid RB, Tasnimuzzaman M, Nordland A, Begum A, Jensen PK (2018) A comparative analysis of Vibrio cholerae contamination in point-of-drinking and source water in a low-income urban community, Bangladesh. Front Microbiol 9:489. https://doi.org/10.3389/fmicb.2018.00489

    Article  Google Scholar 

  • Gadgil S (2007) The Indian Monsoon. Resonance 12:4–20

    Google Scholar 

  • Gilbert JA, Steele JA, Caporaso JG, Steinbrück L, Reeder J, Temperton B, Huse S, McHardy AC, Knight R, Joint I, Somerfield P, Fuhrman JA, Field D (2012) Defining seasonal marine microbial community dynamics. ISME J 6:298–308. https://doi.org/10.1038/ismej.2011.107

    Article  CAS  Google Scholar 

  • Grasshoff K, Kremling K, Ehrhardt M (2009) Methods of seawater analysis. John Wiley & Sons

  • Hashizume M, Faruque A, Terao T, Yunus M, Streatfield K, Yamamoto T, Moji K (2011) The Indian Ocean dipole and cholera incidence in Bangladesh: a time-series analysis. Environ Health Perspect 119:239–244. https://doi.org/10.1289/ehp.1002302

    Article  Google Scholar 

  • Howarth RW, Swaney DP, Butler TJ, Marino R (2000) Rapid communication: climatic control on eutrophication of the Hudson River Estuary. Ecosystems 3:210–215

    Google Scholar 

  • Howarth R, Chan F, Conley DJ, Garnier J, Doney SC, Marino R, Billen G (2011) Coupled biogeochemical cycles: eutrophication and hypoxia in temperate estuaries and coastal marine ecosystems. Front Ecol Environ 9:18–26

    Google Scholar 

  • Hsieh JL, Fries JS, Noble RT (2008) Dynamics and predictive modelling of Vibrio spp. in the Neuse River Estuary, North Carolina, USA. Environ Microbiol 10:57–64

    Google Scholar 

  • Hunt DE, Gevers D, Vahora NM, Polz MF (2008) Conservation of the chitin utilization pathway in the Vibrionaceae. Appl Environ Microbiol 74:44–51

    CAS  Google Scholar 

  • Inc S Released (2007) SPSS for Windows, version 16.0. SPSS Inc., Chicago

    Google Scholar 

  • Jahid IK, Silva AJ, Benitez JA (2006) Polyphosphate stores enhance the ability of Vibrio cholerae to overcome environmental stresses in a low-phosphate environment. Appl Environ Microbiol 72:7043–7049

    CAS  Google Scholar 

  • Kumar KK, Rajagopalan B, Hoerling M, Bates G, Cane M (2006) Unraveling the mystery of Indian monsoon failure during El Niño. Science 314:115–119

    CAS  Google Scholar 

  • Labreuche Y, Lambert C, Soudant P, Boulo V, Huvet A, Nicolas JL (2006) Cellular and molecular hemocyte responses of the Pacific oyster, Crassostrea gigas, following bacterial infection with Vibrio aestuarianus strain 01/32. Microbes Infect 8:2715–2724

    CAS  Google Scholar 

  • Lallu K, Fausia K, Vinita J, Balachandran K, Kumar KN, Rehitha T (2014) Transport of dissolved nutrients and chlorophyll a in a tropical estuary, southwest coast of India. Environ Monit Assess 186:4829–4839

    CAS  Google Scholar 

  • Lambert MA, Hickman-Brenner F, Farmer J III, Moss CW (1983) Differentiation of Vibrionaceae species by their cellular fatty acid composition. Int J Syst Evol Microbiol 33:777–792

    CAS  Google Scholar 

  • Lara RJ, Neogi SB, Islam MS, Mahmud ZH, Yamasaki S, Nair GB (2009) Influence of catastrophic climatic events and human waste on Vibrio distribution in the Karnaphuli Estuary, Bangladesh. EcoHealth 6:279–286

    Google Scholar 

  • Loder TC, Reichard RP (1981) The dynamics of conservative mixing in estuaries. Estuaries 4:64–69

    Google Scholar 

  • Louis VR et al (2003) Predictability of Vibrio cholerae in Chesapeake Bay. Appl Environ Microbiol 69:2773–2785

    CAS  Google Scholar 

  • Maiti B, Shekar M, Khushiramani R, Karunasagar I, Karunasagar I (2009) Evaluation of RAPD-PCR and protein profile analysis to differentiate Vibrio harveyi strains prevalent along the southwest coast of India. J Genet 88:273–279

    CAS  Google Scholar 

  • Mansergh S, Zehr JP (2014) Vibrio diversity and dynamics in the Monterey Bay upwelling region. Front Microbiol 5. https://doi.org/10.3389/fmicb.2014.00048

  • Martin G et al (2011) Eutrophication induced changes in benthic community structure of a flow-restricted tropical estuary (Cochin backwaters), India. Environ Monit Assess 176:427–438

    CAS  Google Scholar 

  • Martinez-Urtaza J, Huapaya B, Gavilan RG, Blanco-Abad V, Ansede-Bermejo J, Cadarso-Suarez C, Figueiras A, Trinanes J (2008) Emergence of asiatic Vibrio diseases in South America in phase with El Niño. Epidemiology 19:829–837

    Google Scholar 

  • Murali RM, Kumar PD (2015) Implications of sea level rise scenarios on land use/land cover classes of the coastal zones of Cochin, India. J Environ Manag 148:124–133

    Google Scholar 

  • Oberbeckmann S, Fuchs BM, Meiners M, Wichels A, Wiltshire KH, Gerdts G (2012) Seasonal dynamics and modeling of a Vibrio community in coastal waters of the North Sea. Microb Ecol 63:543–551

    Google Scholar 

  • Paerl HW, Valdes LM, Peierls BL, Adolf JE, Harding LJW (2006) Anthropogenic and climatic influences on the eutrophication of large estuarine ecosystems. Limnol Oceanogr 51:448–462

    CAS  Google Scholar 

  • Parvathi A, Kumar HS, Karunasagar I, Karunasagar I (2004) Detection and Enumeration of Vibrio vulnificus in Oysters from Two Estuaries along the Southwest Coast of India, Using Molecular Methods. Appl Environ Microbiol 70:6909–6913

    CAS  Google Scholar 

  • Pascual M, Rodó X, Ellner SP, Colwell R, Bouma MJ (2000) Cholera dynamics and El Nino-southern oscillation. Science 289:1766–1769

    CAS  Google Scholar 

  • Pfeffer C, Oliver J (2003) A comparison of thiosulphate-citrate-bile salts-sucrose (TCBS) agar and thiosulphate-chloride-iodide (TCI) agar for the isolation of Vibrio species from estuarine environments. Lett Appl Microbiol 36:150–151

    CAS  Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • Racault M-F et al (2019) Environmental Reservoirs of Vibrio cholerae: challenges and Opportunities for Ocean-Color Remote Sensing. Remote Sens 11:2763

    Google Scholar 

  • Richardson CJ, King RS, Qian SS, Vaithiyanathan P, Qualls RG, Stow CA (2007) Estimating ecological thresholds for phosphorus in the Everglades. Environ Sci Technol 41:8084–8091

    CAS  Google Scholar 

  • Ruby EG, Urbanowski M, Campbell J, Dunn A, Faini M, Gunsalus R, Lostroh P, Lupp C, McCann J, Millikan D, Schaefer A, Stabb E, Stevens A, Visick K, Whistler C, Greenberg EP (2005) Complete genome sequence of Vibrio fischeri: a symbiotic bacterium with pathogenic congeners. Proc Natl Acad Sci 102:3004–3009

    CAS  Google Scholar 

  • Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. MIDI technical note 101. MIDI Inc., Newark, DE

    Google Scholar 

  • Shivaprasad A, Vinita J, Revichandran C, Reny P, Deepak M, Muraleedharan K, NaveenKumar K (2013) Seasonal stratification and property distributions in a tropical estuary (Cochin estuary, west coast, India). Hydrol Earth Syst Sci 17:187–199

    Google Scholar 

  • Siboni N, Balaraju V, Carney R, Labbate M, Seymour JR (2016) Spatiotemporal dynamics of Vibrio spp. within the Sydney Harbour Estuary. Front Microbiol:7. https://doi.org/10.3389/fmicb.2016.00460

  • Snedden GA, Cable JE, Kjerfve B (2013) Estuarine geomorphology and coastal hidrology. Estuarine Ecol:19–38

  • Sneha K et al (2016) Distribution of multiple antibiotic resistant Vibrio spp across Palk Bay. Reg Stud Mar Sci 3:242–250

    Google Scholar 

  • Strickland JD, Parsons TR (1972) A practical handbook of seawater analysis

  • Takemura AF, Chien DM, Polz MF (2014) Associations and dynamics of Vibrionaceae in the environment, from the genus to the population level Vibrio ecology, pathogenesis and evolution. Front Microbiol 5. https://doi.org/10.3389/fmicb.2014.00038

  • Tantillo G, Fontanarosa M, Di Pinto A, Musti M (2004) Updated perspectives on emerging vibrios associated with human infections. Lett Appl Microbiol 39:117–126

    CAS  Google Scholar 

  • Thompson JR, Polz MF (2006) Dynamics of Vibrio populations and their role in environmental nutrient cycling. The biology of vibrios. American Society of Microbiology, In, pp 190–203

    Google Scholar 

  • Thompson FL, Iida T, Swings J (2004) Biodiversity of vibrios. Microbiol Mol Biol Rev 68:403–431

    CAS  Google Scholar 

  • Turner JW, Good B, Cole D, Lipp EK (2009) Plankton composition and environmental factors contribute to Vibrio seasonality. ISME J 3:1082–1092

    CAS  Google Scholar 

  • Unnikrishnan A, Nidheesh A, Lengaigne M (2015) Sea-level-rise trends off the Indian coasts during the last two decades. Curr Sci 108:966–971

    Google Scholar 

  • Urdaci M, Marchand M, Grimont P (1990) Characterization of 22 Vibrio species by gas chromatography analysis of their cellular fatty acids. Res Microbiol 141:437–452

    CAS  Google Scholar 

  • Verschuere L, Hanglamong H, Godelieve C (2000) Selected bacterial strains protect Artemia spp. from the pathogenic effects of Vibrio proteolyticus CW8T2. Appl Environ Microbiol 66:1139–1146

    CAS  Google Scholar 

  • Vezzulli L, Grande C, Reid PC, Hélaouët P, Edwards M, Höfle MG, Brettar I, Colwell RR, Pruzzo C (2016) Climate influence on Vibrio and associated human diseases during the past half-century in the coastal North Atlantic. Proc Natl Acad Sci 113:E5062–E5071. https://doi.org/10.1073/pnas.1609157113

    Article  CAS  Google Scholar 

  • Vijith V, Sundar D, Shetye S (2009) Time-dependence of salinity in monsoonal estuaries. Estuar Coast Shelf Sci 85:601–608

    CAS  Google Scholar 

  • Wong H-C, Liu S-H (2008) Characterization of the low-salinity stress in Vibrio vulnificus. J Food Prot 71:416–419

    Google Scholar 

  • Yang X-E, Wu X, Hao H-L, He Z-L (2008) Mechanisms and assessment of water eutrophication. J Zhejiang Univ Sci B 9:197–209

    CAS  Google Scholar 

  • Yoo K, Yoo H, Lee JM, Shukla SK, Park J (2018) Classification and regression tree approach for prediction of potential hazards of urban airborne bacteria during Asian dust events. Sci Rep 8:1–11. https://doi.org/10.1038/s41598-018-29796-7

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank the Director of CSIR-National Institute of Oceanography (NIO) and Scientist in Charge, Regional Centre, CSIR-NIO, Cochin, Kerala, for the facilities provided. The study was jointly supported by projects “Ecosystem modelling of Cochin estuary” and “Microbial reference facility” funded by ICMAM-PD. The authors also thank two anonymous reviewers for their constructive comments on the manuscript.

Funding

This study received funding from the Director of Integrated Coastal and Marine Area Management Project Directorate (ICMAM-PD), Ministry of Earth Sciences (MoES), Chennai, through the project GAP 2743.

Author information

Authors and Affiliations

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

    Kiran Krishna, Vipindas Puthiya Veettil & Abdulaziz Anas

  2. National Centre for Polar and Ocean Research, Headland Sada, Vasco-da-Gama, Goa, 403804, India

    Vipindas Puthiya Veettil

  3. CSIR - National Institute of Oceanography, Dona Paula, Goa, 403004, India

    Shanta Nair

Authors
  1. Kiran Krishna
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vipindas Puthiya Veettil
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Abdulaziz Anas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shanta Nair
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kiran Krishna.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible Editor: Diane Purchase

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOC 693 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Krishna, K., Veettil, V.P., Anas, A. et al. Hydrological regulation of Vibrio dynamics in a tropical monsoonal estuary: a classification and regression tree approach. Environ Sci Pollut Res 28, 724–737 (2021). https://doi.org/10.1007/s11356-020-10486-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-020-10486-9

Keywords

Search

Navigation