Abstract
Fecal pollution of estuaries and adjacent creeks and streams is of significant concern along the Gulf of Mexico. The prospective threat to human life and water quality impairment via fecal pollution is a substantial danger to the strength and resistance of coastline areas. Pensacola, FL, has a prosperous coastal tourism industry that is utilized for numerous other uses, such as recreational watersports and boating, seafood, and shellfish harvesting. However, the frequency and severity of fecal contamination present possible socio-economic issues, specifically financial hardships. Therefore, understanding the source, abundance, and fate of fecal microbial pollutants in aquatic systems signifies an imperative initial stage for detecting the host sources and techniques to lessen their transport from the landscape. This research aimed to quantify the fecal indicator bacteria (FIB), Escherichia coli, and perform microbiological fecal source tracking to verify if the fecal inputs are of either animal or human host origin. Surface water samples were taken from urban and peri-urban creeks for two sampling periods (February 2021 and January 2022), and IDEXX Colilert-18 (USEPA Standard Method 9223) was used for E. coli enumeration. DNA extractions were obtained from each sample, and quantitative PCR was utilized for fecal microbial source tracking (MST) to detect human, dog, ruminant, and bird host-specific Bacteroides DNA. The result indicates elevated quantities of FIB, E. coli, that surpass the threshold considered safe regarding human health. E. coli at six sites over the two sampling periods exceeded the impairment threshold, reaching as high as 866.4 MPN/100 ml. Fecal source tracking identified human host fecal contamination at four of nine sites, dogs at three of nine, and birds at one site. However, those sites with sources identified via MST all had E. coli levels below impairment thresholds. No sites were determined to be positive for ruminant as a source or for the pathogen Helicobacter pylori. No canine host fecal inputs were found in January 2022, and only one site with human sewage. Our results highlight the utility of MST in assessing bacterial inputs to water bodies and the challenges.
Similar content being viewed by others
Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request and are included in this published article.
References
Adams, C. M., Hernandez, E., & Cato, J. C. (2004). The economic significance of the Gulf of Mexico related to population, income, employment, minerals, fisheries, and shipping. Ocean & Coastal Management, 47(11–12), 565–580.
Ahmed, W., Sawant, S., Huygens, F., Goonetilleke, A., & Gardner, T. (2009). Prevalence and occurrence of zoonotic bacterial pathogens in surface waters determined by quantitative PCR. Water Research, 43(19), 4918–4928.
Ashbolt, N. J. (2004). Microbial contamination of drinking water and disease outcomes in developing regions. Toxicology, 198(1–3), 229–238.
Bachoon, D. S., Markand, S., Otero, E., Perry, G., & Ramsubaugh, A. (2010). Assessment of non-point sources of fecal pollution in coastal waters of Puerto Rico and Trinidad. Marine Pollution Bulletin, 60(7), 1117–1121.
Bernhard, A. E., & Field, K. G. (2000). Identification of non-point sources of fecal pollution in coastal waters using host-specific 16S ribosomal DNA genetic markers from fecal anaerobes. Applied and Environmental Microbiology, 66(4), 1587–1594.
Blaustein, R. A., Pachepsky, Y., Hill, R. L., Shelton, D. R., & Whelan, G. (2013). Escherichia coli survival in waters: Temperature dependence. Water Research, 47(2), 569–578.
Board, O. S., & National Research Council. (2013). An ecosystem services approach to assessing the impacts of the Deepwater Horizon oil spill in the Gulf of Mexico. Washington, DC: The National Academies Press.
Bradshaw, J. K., Snyder, B. J., Oladeinde, A., Spidle, D., Berrang, M. E., Meinersmann, R. J., & Molina, M. (2016). Characterizing relationships among fecal indicator bacteria, microbial source tracking markers, and associated water-borne pathogen occurrence in stream water and sediments in a mixed land use watershed. Water Research, 101, 498–509.
Bridgemohan, R. S., Bachoon, D. S., Wang, Y., Bridgemohan, P., Mutiti, C., & Ramsubhag, A. (2020). Identifying the primary sources of fecal contamination along the beaches and rivers of Trinidad. Journal of Water and Health, 18(2), 229–238.
Bustin, S. A., Benes, V., Garson, J. A., Hellemans, J., Huggett, J., Kubista, M., & Wittwer, C. T. (2009). The MIQE Guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry, 55(4), 611–622.
Caffrey, J. M., & Murrell, M. C. (2016). A historical perspective on eutrophication in the Pensacola Bay estuary, FL, USA. Aquatic microbial ecology and biogeochemistry: a dual perspective (pp. 199–213). Cham: Springer.
Cinotto, P. J. (2005). Occurrence of fecal-indicator bacteria and protocols for Identification of fecal-contamination sources in selected reaches of the West Branch Brandywine Creek, Chester County, Pennsylvania. Reston: US Department of the Interior, US Geological Survey.
Colford, J. M., Jr., Wade, T. J., Schiff, K. C., Wright, C. C., Griffith, J. F., Sandhu, S. K., & Weisberg, S. B. (2007). Water quality indicators and the risk of illness at beaches with non-point sources of fecal contamination. Epidemiology, 18, 27–35.
DeFlorio-Barker, S., Wing, C., Jones, R. M., & Dorevitch, S. (2018). Estimate of incidence and cost of recreational water-borne illness on United States surface waters. Environmental Health, 17(1), 1–10.
Devereux, R., Wan, Y., Rackley, J. L., Fasselt, V., & Vivian, D. N. (2021). Comparative analysis of nitrogen concentrations and sources within a coastal urban bayou watershed: A multi-tracer approach. Science of the Total Environment, 776, 145862.
Dick, L. K., Simonich, M. T., & Field, K. G. (2005). Microplate subtractive hybridization to enrich for Bacteroidales genetic markers for fecal source identification. Applied and Environmental Microbiology, 71(6), 3179–3183.
Field, K. G., & Samadpour, M. (2007). Fecal source tracking, the indicator paradigm, and managing water quality. Water Research, 41(16), 3517–3538.
Florida Department of Environmental Protection (FDEP). (2021). Statewide comprehensive verified list of impaired waters.
Garzio-Hadzick, A., Shelton, D. R., Hill, R. L., Pachepsky, Y. A., Guber, A. K., & Rowland, R. (2010). Survival of manure-borne E. coli in streambed sediment: effects of temperature and sediment properties. Water Research, 44(9), 2753–2762.
Genthner, F. J., James, J. B., Yates, D. F., & Friedman, S. D. (2005). Use of composite data sets for source-tracking enterococci in the water column and shoreline interstitial waters on Pensacola Beach. Florida. Marine Pollution Bulletin, 50(7), 724–732.
Graves, A. K., Hagedorn, C., Teetor, A., Mahal, M., Booth, A. M., & Reneau, R. B. (2002). Antibiotic resistance profiles to determine sources of fecal contamination in a rural Virginia watershed. Journal of Environmental Quality, 31(4), 1300–1308.
Green, H. C., Haugland, R. A., Varma, M., Millen, H. T., Borchardt, M. A., Field, K. G., & Shanks, O. C. (2014). Improved HF183 quantitative real-time PCR assay for characterization of human fecal pollution in ambient surface water samples. Applied and environmental microbiology, 80(10), 3086–3094.
Hager, M.C. 2001. Detecting bacteria in coastal waters. In Stormwater. Parts 1 & 2. Buyers Guide 2002:22–27, and May/June 2001:16–25.
Harwood, V. J., Brownell, M., Wang, S., Lepo, J., Ellender, R. D., Ajidahun, A., & Flood, C. (2009). Validation and field testing of library-independent microbial source tracking methods in the Gulf of Mexico. Water Research, 43(19), 4812–4819.
Harwood, V. J., Staley, C., Badgley, B. D., Borges, K., & Korajkic, A. (2014). Microbial source tracking markers for detection of fecal contamination in environmental waters: Relationships between pathogens and human health outcomes. FEMS Microbiology Reviews, 38(1), 1–40.
Haugland, R. A., Varma, M., Sivaganesan, M., Kelty, C., Peed, L., & Shanks, O. C. (2010). Evaluation of genetic markers from the 16S rRNA gene V2 region for use in quantitative detection of selected Bacteroidales species and human fecal waste by qPCR. Systematic and Applied Microbiology, 33(6), 348–357.
Hegarty, J. P., Dowd, M. T., & Baker, K. H. (1999). Occurrence of Helicobacter pylori in surface water in the United States. Journal of Applied Microbiology, 87(5), 697–701.
Hellein, K. N., Battie, C., Tauchman, E., Lund, D., Oyarzabal, O. A., & Lepo, J. E. (2011). Culture-based indicators of fecal contamination and molecular microbial indicators rarely correlate with Campylobacter spp. in recreational waters. Journal of water and health, 9(4), 695–707.
Herrig, I., Fleischmann, S., Regnery, J., Wesp, J., Reifferscheid, G., & Manz, W. (2020). Prevalence and seasonal dynamics of bla CTX-M antibiotic resistance genes and fecal indicator organisms in the lower Lahn River. Germany. Plos One, 15(4), e0232289.
Holman, C. B., Bachoon, D. S., Otero, E., & Ramsubhag, A. (2014). Detection of Helicobacter pylori in the coastal waters of Georgia, Puerto Rico and Trinidad. Marine Pollution Bulletin, 79(1–2), 354–358.
Ishii, S., & Sadowsky, M. J. (2008). Escherichia coli in the environment: Implications for water quality and human health. Microbes and Environments, 23(2), 101–108.
Kern, J., Petrauskas, B., McClellan, P., Shanholtz, V., & Hagedorn, C. (2002). Bacterial source tracking: a tool for total maximum daily load development. In T. Younos (Ed.), Advances in water. Water Resource Publications LLC.
Kim, S. S., Ruiz, V. E., Carroll, J. D., & Moss, S. F. (2011). Helicobacter pylori in the pathogenesis of gastric cancer and gastric lymphoma. Cancer Letters, 305(2), 228–238.
Kobayashi, D., Eishi, Y., Ohkusa, T., Ishige, I., Suzuki, T., Minami, J., & Koike, M. (2002). Gastric mucosal density of Helicobacter pylori estimated by real-time PCR compared with results of urea breath test and histological grading. Journal of Medical Microbiology, 51(4), 305–311.
Kongprajug, A., Chyerochana, N., Rattanakul, S., Denpetkul, T., Sangkaew, W., Somnark, P., & Sirikanchana, K. (2021). Integrated analyses of fecal indicator bacteria, microbial source tracking markers, and pathogens for Southeast Asian beach water quality assessment. Water Research, 203, 117479.
Leclerc, H., Schwartzbrod, L., & Dei-Cas, E. (2002). Microbial agents associated with water-borne diseases. Critical Reviews in Microbiology, 28(4), 371–409.
Liu, Y., Engel, B. A., Flanagan, D. C., Gitau, M. W., McMillan, S. K., & Chaubey, I. (2017). A review on effectiveness of best management practices in improving hydrology and water quality: Needs and opportunities. Science of the Total Environment, 601, 580–593.
Lu, J., Santo Domingo, J., & Shanks, O. C. (2007). Identification of chicken-specific fecal microbial sequences using a metagenomic approach. Water Research, 41(16), 3561–3574.
Mandaville, S. M. (2002). Bacterial source tracking (BST)- A review. Project H-2, Soil & Water Conservation Society of Metro Halifax. X, 46p. Appendices A to T.
Meybeck, M. (2003). Global analysis of river systems: from Earth system controls to Anthropocene syndromes. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 358(1440), 1935–1955.
Mississippi Department of Environmental Quality (MDEQ). (2020). List of impaired water bodies.
Mohrherr, C. J., Liebens, J., Lepo, J. E., & Rao, K. R. (2005). Profiles of selected pollutants in Bayou Texar, Pensacola, FL. University of West Florida.
Morrison, C. R., Bachoon, D. S., & Gates, K. W. (2008). Quantification of enterococci and bifidobacteria in Georgia estuaries using conventional and molecular methods. Water Research, 42(14), 4001–4009.
Moss, J. A., & Snyder, R. A. (2019). Surveillance of Microsporidia and protozoan pathogens in Pensacola Florida: A one-year study. Journal of Eukaryotic Microbiology, 66(4), 617–624.
Nag, R., Nolan, S., O’Flaherty, V., Fenton, O., Richards, K. G., Markey, B. K., & Cummins, E. (2021). Quantitative microbial human exposure model for faecal indicator bacteria and risk assessment of pathogenic Escherichia coli in surface runoff following application of dairy cattle slurry and co-digestate to grassland. Journal of Environmental Management, 299, 113627.
Nguyen, K. H., Senay, C., Young, S., Nayak, B., Lobos, A., Conrad, J., & Harwood, V. J. (2018). Determination of wild animal sources of fecal indicator bacteria by microbial source tracking (MST) influences regulatory decisions. Water Research, 144, 424–434.
Ouyang, W., Skidmore, A. K., Toxopeus, A. G., & Hao, F. (2010). Long-term vegetation landscape pattern with non-point source nutrient pollution in upper stream of Yellow River basin. Journal of Hydrology, 389(3–4), 373–380.
Pachepsky, Y. A., & Shelton, D. R. (2011). Escherichia coli and fecal coliforms in freshwater and estuarine sediments. Critical Reviews in Environmental Science and Technology, 41(12), 1067–1110.
Paul, M. J., & Meyer, J. L. (2008). Streams in the urban landscape. Urban ecology (pp. 207–231). Boston, MA: Springer.
Petkova, E. P., Ebi, K. L., Culp, D., & Redlener, I. (2015). Climate change and health on the US Gulf Coast: public health adaptation is needed to address future risks. International Journal of Environmental Research and Public Health, 12(8), 9342–9356.
Pratt, T. R., Richards, C. J., Milla, K. A., Wagner, J. R., Johnson, J. L., & Curry, R. J. (1996). Northwest Florida water management district.
Propst, C. W., Harwood, V. J., & Morrison, G. (2011). Case studies of urban and suburban watersheds. Microbial source tracking: methods, applications, and case studies (pp. 433–450). New York: Springer.
Quigg, A., Broach, L., Denton, W., & Miranda, R. (2009). Water quality in the Dickinson Bayou watershed (Texas, Gulf of Mexico) and health issues. Marine Pollution Bulletin, 58(6), 896–904.
Ram, J. L., et al. (2007). Identification of pets and raccoons as sources of bacterial contamination of urban storm sewers using a sequence-based bacterial source tracking method. Water Research, 41(16), 3605–3614.
Schriewer, A., Goodwin, K. D., Sinigalliano, C. D., Cox, A. M., Wanless, D., Bartkowiak, J., & Wuertz, S. (2013). Performance evaluation of canine-associated Bacteroidales assays in a multi-laboratory comparison study. Water Research, 47(18), 6909–6920.
Stewart, J. R., Gast, R. J., Fujioka, R. S., Solo-Gabriele, H. M., Meschke, J. S., Amaral-Zettler, L. A., & Holland, A. F. (2008). The coastal environment and human health: microbial indicators, pathogens, sentinels and reservoirs. Environmental Health, 7(2), 1–14.
Stocker, M. D., Smith, J. E., Hernandez, C., Macarisin, D., & Pachepsky, Y. (2019). Seasonality of E. coli and enterococci concentrations in creek water, sediment, and periphyton. Water, Air, & Soil Pollution, 230(9), 1–12.
Texas Commission on Environmental Quality (TCEQ). (2020). Texas integrated report index of water quality impairments.
Thevenon, F., Regier, N., Benagli, C., Tonolla, M., Adatte, T., Wildi, W., & Poté, J. (2012). Characterization of fecal indicator bacteria in sediments cores from the largest freshwater lake of Western Europe (Lake Geneva, Switzerland). Ecotoxicology and Environmental Safety, 78, 50–56.
Tyrrel, S. F., & Quinton, J. N. (2003). Overland flow transport of pathogens from agricultural land receiving faecal wastes. Journal of Applied Microbiology, 94, 87–93.
USEPA, U. (2000). Risk-based concentration table. Philadelphia, PA: United States Environmental Protection Agency.
USEPA. (2007). Carson river: Total maximum daily loads for TSS and turbidity. Retrieved from website: http://www.epa.gov/waters/tmdldocs/Carson%20TSS%20NTU%20TMDL%20Aug%2006.pdf
USEPA. (December 2012). 2012 recreational water quality criteria. Retrieved from: http://water.epa.gov/scitech/swguidance/standards/criteria/health/recreation/upload/factsheet2012.pdf
U.S. EPA Method 300.1 (1997) Determination of inorganic anions in drinking water by ion chromatography. Revision 1.0, USEPA. EPA/600/R-98/118.
Wade, T. J., Calderon, R. L., Brenner, K. P., Sams, E., Beach, M., Haugland, R., & Dufour, A. P. (2008). High sensitivity of children to swimming-associated gastrointestinal illness: Results using a rapid assay of recreational water quality. Epidemiology, 19(3), 375–383.
Wenninger, J., Uhlenbrook, S., Tilch, N., & Leibundgut, C. (2003). Proving pressure wave effects at a hillslope/floodplain/channel system using hydrochemisty and groundwater levels (p. 362). EGS-AGU-EUG Joint Assembly.
Wheeler, A. P., Angermeier, P. L., & Rosenberger, A. E. (2005). Impacts of new highways and subsequent landscape urbanization on stream habitat and biota. Reviews in Fisheries Science, 13(3), 141–164.
Whitman, R. L., Shively, D. A., Pawlik, H., Nevers, M. B., & Byappanahalli, M. N. (2003). Occurrence of Escherichia coli and enterococci in Cladophora (Chlorophyta) in nearshore water and beach sand of Lake Michigan. Applied and Environmental Microbiology, 69(8), 4714–4719.
WHO (World Health Organization). (2003). Chlorite and chlorate in drinking water. Background document for preparation of WHO Guidelines for drinking water quality. Geneva: World Health Organization. WHO/SDE/WSH/0.3.04/86.
WHO, G. (2011). Guidelines for drinking-water quality. World Health Organization, 216, 303–304.
Wright, M. E., Solo-Gabriele, H. M., Elmir, S., & Fleming, L. E. (2009). Microbial load from animal feces at a recreational beach. Marine Pollution Bulletin, 58(11), 1649–1656.
Yáñez-Arancibia, A., & Day, J. W. (2004). Environmental sub-regions in the Gulf of Mexico coastal zone: The ecosystem approach as an integrated management tool. Ocean & Coastal Management, 47(11–12), 727–757.
Zhu, X. F., Wang, J. D., Solo-Gabriele, H. M., & Fleming, L. E. (2011). A water quality modeling study of non-point sources at recreational marine beaches. Water Research, 45, 2985–2995.
Acknowledgements
We thank the facilities of the UF IFAS West Florida Research and Education Center and the Microbiology Laboratory at Georgia College. Finally, to the watershed management laboratory team, Savannah Cain, Emily Harmon, and Caitlyn Turnbull, at UF IFAS WFREC, for their field and laboratory assistance.
Funding
Support of this research was funded by the United States Environmental Protection Agency Grant number MX—00D86419 and the United States Department of Agriculture Hatch Grant number FLA-WFC-005577.
Author information
Authors and Affiliations
Contributions
Every one of the writers and scientists added to the research concept, writing up, and design. Material preparation, sampling, data collection, and analysis were performed by Ronell Bridgemohan, Matthew Deitch, Tesfay Gebremicael, Matt Whiles, P. Christopher Wilson, Dave Bachoon, and Israel Tharpe. Ronell Shamir Hemsley Bridgemohan, Matthew Jaeger Deitch, and Tesfay Gebremicael performed sampling, water quality testing, FIB enumeration, membrane filtration, and nutrient testing. Dave Bachoon and Israel Tharpe extracted DNA and performed MST via PCR. Matt Whiles and Patrick Christopher Wilson aided in data analysis, manuscript write-up, and statistics. The original version of the research manuscript was written by Ronell Bridgemohan, and each researcher/author was critiqued on prior editions of the document. Everyone read and granted approval on the final version. The data collected during and/or analyzed throughout the research are accessible from the corresponding author upon request.
Corresponding author
Ethics declarations
Ethics approval
All authors have read, understood, and have complied as applicable with the statement on “Ethical responsibilities of Authors” as found in the Instructions for Authors and are aware that with minor exceptions, no changes can be made to authorship once the paper is submitted. This is an observational study. The Research Ethics Committee has confirmed that no ethical approval is required.
Competing interests
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Bridgemohan, R.S.H., Deitch, M.J., Gebremicael, T. et al. Environmental risk assessment for fecal contamination sources in urban and peri-urban estuaries, in Escambia and Santa Rosa counties, FL, USA. Environ Monit Assess 195, 867 (2023). https://doi.org/10.1007/s10661-023-11478-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10661-023-11478-1