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Research Article

Linking fecal bacteria in rivers to landscape, geochemical, and hydrologic factors and sources at the basin scale

View ORCID ProfileMarc P. Verhougstraete, Sherry L. Martin, Anthony D. Kendall, David W. Hyndman, and Joan B. Rose
  1. aDepartment of Fisheries and Wildlife, Michigan State University, East Lansing, MI 48824;
  2. bDepartment of Geological Sciences, Michigan State University, East Lansing, MI 48824

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PNAS August 18, 2015 112 (33) 10419-10424; first published August 3, 2015; https://doi.org/10.1073/pnas.1415836112
Marc P. Verhougstraete
aDepartment of Fisheries and Wildlife, Michigan State University, East Lansing, MI 48824;
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  • ORCID record for Marc P. Verhougstraete
  • For correspondence: mverhougstraete@email.arizona.edu
Sherry L. Martin
bDepartment of Geological Sciences, Michigan State University, East Lansing, MI 48824
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Anthony D. Kendall
bDepartment of Geological Sciences, Michigan State University, East Lansing, MI 48824
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David W. Hyndman
bDepartment of Geological Sciences, Michigan State University, East Lansing, MI 48824
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Joan B. Rose
aDepartment of Fisheries and Wildlife, Michigan State University, East Lansing, MI 48824;
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  1. Edited* by Rita R. Colwell, University of Maryland, College Park, MD, and approved June 29, 2015 (received for review August 15, 2014)

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    Fig. 1.

    (A) E. coli (log10 MPN⋅100 mL−1) and (B) B. theta (log10 CE⋅100 mL−1) concentrations measured in 64 rivers under baseflow conditions. Areas in black were not represented with samples.

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    Fig. 2.

    CART analyses for (A) E. coli and (B) B. theta concentrations as dependent variables and land use, nutrient, chemical, hydrologic, and environmental parameters as independent variables in watersheds. PRE, proportion of reduction in error.

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    Fig. S1.

    CART analyses for log-transformed (A) E. coli and (B) B. theta concentrations as dependent variables and land use, nutrient, chemical, hydrologic, and environmental parameters as independent variables in reduced watersheds (n = 52).

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    Fig. 3.

    B. theta versus septic systems illustrating the CART output from the first split of Fig. 2B.

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    Fig. 4.

    CART of E. coli and B. theta Z-scores illustrating conditions associated with different concentrations between these two microbes. PRE, proportion of reduction in error.

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    Fig. S2.

    Scatter plots of B. theta versus E. coli (A) concentrations (n = 64) and (B) loads (n = 63).

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    Fig. S3.

    Watersheds of sampled river systems that drain Michigan's Lower Peninsula and states to the south, colored by 2006 NLCD land use classes.

Tables

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    Table S1.

    Description of land, discharge, and E. coli and B. theta concentrations at 64 Michigan rivers under baseflow

    River systemE. coli, MPN⋅100 mL−1B. theta, CE⋅100 mL−1Discharge, m3⋅s−1Area, km2Urban, %Agriculture, %Rangeland, %Forest, %Water, %Wetland, %Barren, %No. of septic systemsAverage annual WWTP discharge, MGD
    St. Joseph River1.05.357.311,06114.359.51.110.42.412.20.293,64324.2
    Paw Paw River1.85.78.01,02711.547.52.621.11.415.60.318,1062.3
    Kalamazoo River1.65.943.65,00214.147.81.821.52.112.40.4102,94849.2
    Grand River1.55.550.712,85412.755.31.016.61.512.70.3246,03388.1
    Muskegon River1.85.437.86,4187.619.69.640.53.918.60.147,1156.7
    White River2.15.87.71,0495.220.39.749.70.714.30.16,2240.0
    Pere Marquette River2.25.812.21,7905.09.38.361.61.214.50.16,0940.0
    Big Sable River0.75.32.94765.311.58.052.45.017.00.81,9750.0
    Little Manistee River1.45.44.55264.73.912.568.60.79.60.11,2280.0
    Manistee River0.24.742.83,5595.79.615.956.41.410.90.111,9510.0
    Bear Creek2.15.93.03506.313.820.137.62.319.70.11,6560.0
    Betsie River2.05.822.86188.17.613.146.29.915.00.16,1400.0
    Platte River0.25.24.84716.69.913.456.27.56.10.24,6970.0
    Boardman River1.15.36.771610.810.418.846.72.110.90.29,8244.0
    Elk-Torch River0.24.512.81,3087.614.413.645.411.37.40.29,5950.0
    Cheboygan River0.24.926.12,3176.48.211.651.08.114.50.211,6600.0
    Black River1.24.811.61,5095.54.412.147.13.927.00.12,7470.3
    Thunder Bay River0.54.912.62,2416.311.08.840.22.731.00.17,2831.6
    Au Sable River1.25.632.55,2878.43.214.558.92.012.80.123,1560.6
    Au Gres River2.15.31.19876.423.37.637.72.222.00.74,5730.4
    Rifle River1.65.55.08589.316.58.944.21.619.40.16,3221.6
    Black River1.15.40.661,2506.274.21.210.60.17.50.16,5494.1
    Pine River2.65.40.054409.046.53.233.30.37.50.16,4300.0
    Belle River2.05.61.45129.559.71.719.00.39.70.26,4163.2
    Clinton River2.05.5n/a1,88051.520.21.314.92.88.60.795,581152.9
    River Rouge2.75.50.321,03382.95.40.57.20.72.90.341,34510.9
    Huron River1.95.87.72,29832.524.51.221.84.215.10.6117,12243.9
    Raisin River1.45.44.72,68310.867.40.811.11.48.30.241,99914.0
    South Branch Black River2.35.91.13139.145.84.422.81.216.50.24,0991.7
    North Branch Black River2.25.61.53987.043.65.624.81.717.10.24,0730.6
    Macatawa River1.35.60.1629223.567.80.74.00.23.10.95,9601.1
    Pine Creek2.14.90.274848.430.91.112.10.36.11.15,4870.0
    Pigeon River2.75.00.0810211.066.02.015.30.15.10.51,7610.0
    Rush Creek2.35.40.1215256.431.50.47.61.12.30.612,6070.0
    Buck Creek2.24.60.64391.30.00.61.40.95.80.000.0
    Sand Creek2.34.90.3114219.160.80.811.30.27.60.33,7800.0
    Bass River2.15.10.2012711.163.62.116.00.26.60.52,5940.0
    Little Pigeon Creek2.54.90.031418.916.46.241.90.016.30.31670.0
    Black Creek3.04.80.6613614.934.85.329.94.810.10.24,1970.0
    Silver Creek1.74.40.374111.70.615.263.74.24.40.26430.0
    Flower Creek2.54.60.347910.245.610.727.70.63.41.85800.0
    Stony Lake Outlet0.55.21.316010.137.711.735.11.04.10.31,6350.0
    Swan Creek2.54.90.34545.557.98.215.51.311.50.02480.0
    Lincoln River2.25.00.662155.633.211.830.62.116.50.21,0870.0
    Crystal River0.74.61.61104.73.48.753.723.73.32.45180.0
    Belangers Creek1.34.70.08256.738.412.730.81.59.90.01880.0
    Mitchell Creek2.24.80.293828.322.816.319.40.213.00.11,6080.0
    Jordan River0.94.44.11743.27.86.570.70.011.80.13670.0
    Monroe Creek1.24.50.08274.222.38.844.52.218.10.01130.0
    Boyne River1.25.41.71998.316.110.854.50.69.40.21,6470.0
    Bear River1.54.81.62936.413.37.048.56.618.10.22,2760.0
    Carp River1.05.01.81196.28.67.722.07.048.30.13750.0
    Ocqueoc River0.94.72.43694.76.511.543.42.231.40.35760.0
    Trout River1.34.80.41824.613.59.528.80.143.10.32910.0
    Little Trout River2.44.90.06285.427.87.514.30.144.60.3950.0
    Long Lake Creek1.84.20.031625.711.77.120.715.739.10.11,1420.0
    Tawas River1.24.51.64038.47.16.951.62.024.00.01,5970.9
    Harrington Drain2.04.50.015399.70.00.00.20.00.10.01,7140.0
    Marsh Creek2.45.30.137872.04.71.715.40.05.90.21,8380.0
    Sandy Creek2.24.90.028226.258.71.310.60.02.70.41,5060.5
    Cass River1.25.42.02,1746.957.42.219.70.213.50.115,9992.8
    Flint River1.95.76.33,20621.040.62.024.11.610.40.3141,16875.6
    Shiawassee River2.04.74.41,51715.752.50.717.02.211.40.437,04313.5
    Tittabawassee River1.95.617.56,2118.632.87.330.61.519.10.255,63516.3
    • n/a, not applicable.

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    Table S2.

    Descriptive statistics of physical, chemical, and hydrologic variables measured during baseflow conditions at 64 rivers

    ParameterCountMinimumMeanMaximumSD5th percentile95th percentile
    Ammonia, µg⋅L−1630.023.6280.045.60.098.5
    Calcium, mg⋅L−16330.062.4160.621.633.898.2
    Chlorine (Cl−), mg⋅L−1633.442.3291.854.45.9174.8
    Dissolved oxygen, mg⋅L−1645.99.813.31.77.212.2
    Dissolved organic carbon (NPOC), mg⋅L−1631.66.126.84.22.115.6
    Magnesium, mg⋅L−1637.018.434.26.310.329.1
    Nitrate/nitrite (NOx), µg⋅L−1640.0858.35,638.91,310.30.04,095.6
    Pheophytin corrected chlorophyll a, µg⋅L−1590.00.84.41.00.13.4
    pH637.98.28.40.18.08.4
    Potassium, mg⋅L−1630.42.29.81.90.56.0
    Sodium, mg⋅L−1633.027.0199.336.93.4113.0
    Soil hydraulic conductivity (Ksat), m⋅d−1640.52.24.71.10.64.2
    Specific conductance, μS⋅cm−163257.0527.01,589.0264.2265.21,039.8
    Soluble reactive P, µg⋅L−1640.923.3266.045.02.187.0
    Sulfate, µg⋅L−1632.432.1169.830.55.689.6
    Total dissolved N, µg⋅L−1640.01,423.36,033.71,346.5337.65,414.1
    Total dissolved P, µg⋅L−1643.125.2292.338.63.958.0
    Total N, µg⋅L−16481.81,082.15,583.11,129.3110.83,610.6
    Total P, µg⋅L−1647.737.8395.552.48.9102.5
    Total chlorophyll a, µg⋅L−1590.11.67.81.90.27.4
    Precipitation,† mm
     6 h640.00.19.21.2——
     12 h640.01.977.910.20.07.9
     18 h640.03.478.611.60.030.8
     24 h640.04.478.611.90.031.0
     2 d640.06.078.611.90.031.0
     3 d640.07.780.113.70.034.2
     4 d640.08.380.513.50.034.2
     6 d640.09.087.314.10.034.2
     8 d640.011.692.616.50.057.2
    Discharge, m3⋅s−1630.06.757.312.50.043.4
    Water temperature, °C647.013.117.52.68.216.6
    • ↵† Precipitation measured at hourly averages from 16-km2 NEXRAD cells and reported in cumulative millimeters per time.

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    Table S3.

    Summary of chemical and nutrient methods

    AssayMethod descriptionRefs.
    Ammonia, µg⋅L−1Phenate methodStandard methods 4500-NH3-G (68)
    Calcium, mg⋅L−1Flame atomic absorption spectrophotometry65
    Chlorine (Cl−), mg⋅L−1Dionex membrane-suppression ion chromatography65, 66
    Magnesium, mg⋅L−1Flame atomic absorption spectrophotometry65
    Nitrate/nitrite, µg⋅L−1Cadmium reductionStandard methods 4500-NO3-E (68)
    Pheophytin corrected chlorophyll a, µg⋅L−1Fluorometry with pheophytin correction following ethanol extractionStandard methods 10200.H (68)
    pHHydrolab multisonde66
    Potassium, mg⋅L−1Flame atomic absorption spectrophotometry (0.5% HNO3 preservative)66
    Sodium, mg⋅L−1Flame atomic absorption spectrophotometry (0.5% HNO3 preservative)66
    Soluble reactive phosphorus, µg⋅L−1Ascorbic acid methodStandard methods 4500-P.E. (68)
    Sulfate (SO4), µg⋅L−1Dionex membrane- suppression ion chromatography66
    Total dissolved nitrogen, µg⋅L−1Second derivative spectroscopy following persulfate digestion67
    Total dissolved phosphorus, µg⋅L−1Ascorbic acid method following persulfate digestionStandard methods 4500-P.E and 4500-N.C (68)
    Total nitrogen, µg⋅L−1Second derivative spectroscopy following persulfate digestion67
    Total phosphorus, µg⋅L−1Ascorbic acid method following persulfate digestionStandard methods 4500-P.E and 4500-N.C (68)
    Total chlorophyll a, µg⋅L−1Fluorometry following ethanol extractionStandard methods 10200.H (68)
    • View popup
    Table S4.

    Land use summary for full watersheds, reduced watersheds, and 60-m buffers

    Scale parameterMinimumMeanMaximumSD
    Full watershed†
     Area, km22.881,37712,8542,431
     Estimated septic systems0.019,579246,03341,902
     Septic density, no. per km20.015.7113.719.5
     Population density, persons per km271311,597281
     Population density on WWTP0981,589279
     Population density on septic71141,567236
     Impervious surface, km20.415.1356.99.8
     Urban, %3.1616.799.70.21
     Agriculture, %0.02874.20.22
     Open, %0.06.9720.10.05
     Forest, %0.1931.470.70.18
     Water, %0.02.6823.70.04
     Wetland, %0.071448.30.1
     Barren, %0.00.312.450.0
    Reduced watershed‡
     Area, km20.153664,065630
     Estimated septic systems0.022,299246,03345,592
     Septic density, no. per km20.016.111418.8
     Population density, persons per km271471,597306
     Population density on WWTP01151,589307
     Population density on septic71241,567259
     Impervious surface, km20.47.555.913.6
     Urban, %3.121.399.726.2
     Agriculture, %0.027.277.424
     Open, %0.06.1618.85.27
     Forest, %0.02971.219.5
     Water, %0.01.6115.43.32
     Wetland, %0.013.947.912.1
     Barren, %0.00.7731.13.87
    60-m riparian buffer‡
     Area, km20.064649778.3
     Estimated septic systems0.02,67228,2565,596
     Septic density, no. per km20.01510421
     Population density, persons per km271241,567259
     Population density on WWTP0000
     Population density on septic03210524
     Impervious surface, km20.05.542.79.64
     Urban, %0.018.998.323
     Agriculture, %0.021.472.121.7
     Open, %0.03.6419.43.8
     Forest, %0.022.162.614.9
     Water, %0.06.0963.212
     Wetland, %0.027.376.317.9
     Barren, %0.00.5924.93.12
    • ↵† Entire upstream drainage area including lakes (n = 64).

    • ↵‡ Watersheds were defined as the total upstream area to the nearest lake draining to each respective river sampling point (n = 52).

    • View popup
    Table S5.

    Anderson level 1 land use classifications and descriptions

    ClassificationDescriptionExamplesAssociated NLCD classifications (code)
    UrbanIntensive use with structures covering the majority of landCities, shopping, industrial, and commercial centersDeveloped open space (21)
    Developed low intensity (22)
    Developed medium intensity (23)
    Developed high intensity (24)
    AgriculturalLand used for food productionPasture, row crop, orchards, confined feeding operationsPasture and hay (81)
    Cultivated crops (82)
    OpenPredominant natural vegetation is grass or shrubsHerbaceous, shrub, brushShrub and scrub (52)
    Grassland and herbaceous (71)
    ForestClosed canopy at least 10% from timber quality treesDeciduous, coniferous, and mixed forestedDeciduous forest (41)
    Evergreen forest (42)
    Mixed forest (43)
    WaterArea predominantly covered by water throughout yearStreams, lakes, bays, and reservoirsWater (11)
    WetlandLand with water table near land surface for significant portion of yearMarshes, swamps, perched bogsWoody wetland (90)
    Emergent herbaceous wetland (95)
    BarrenLand that has less than one-third vegetative coverBeaches, exposed rock, gravel pitsBarren (31)

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Bacteria in rivers linked to land and geochemistry
Marc P. Verhougstraete, Sherry L. Martin, Anthony D. Kendall, David W. Hyndman, Joan B. Rose
Proceedings of the National Academy of Sciences Aug 2015, 112 (33) 10419-10424; DOI: 10.1073/pnas.1415836112

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Bacteria in rivers linked to land and geochemistry
Marc P. Verhougstraete, Sherry L. Martin, Anthony D. Kendall, David W. Hyndman, Joan B. Rose
Proceedings of the National Academy of Sciences Aug 2015, 112 (33) 10419-10424; DOI: 10.1073/pnas.1415836112
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