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

Marc P. Verhougstraete; Sherry L. Martin; Anthony D. Kendall; David W. Hyndman; Joan B. Rose

doi:10.1073/pnas.1415836112

New Research In

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.

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Table S1.

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

River system	E. coli, MPN⋅100 mL⁻¹	B. theta, CE⋅100 mL⁻¹	Discharge, m³⋅s⁻¹	Area, km²	Urban, %	Agriculture, %	Rangeland, %	Forest, %	Water, %	Wetland, %	Barren, %	No. of septic systems	Average annual WWTP discharge, MGD
St. Joseph River	1.0	5.3	57.3	11,061	14.3	59.5	1.1	10.4	2.4	12.2	0.2	93,643	24.2
Paw Paw River	1.8	5.7	8.0	1,027	11.5	47.5	2.6	21.1	1.4	15.6	0.3	18,106	2.3
Kalamazoo River	1.6	5.9	43.6	5,002	14.1	47.8	1.8	21.5	2.1	12.4	0.4	102,948	49.2
Grand River	1.5	5.5	50.7	12,854	12.7	55.3	1.0	16.6	1.5	12.7	0.3	246,033	88.1
Muskegon River	1.8	5.4	37.8	6,418	7.6	19.6	9.6	40.5	3.9	18.6	0.1	47,115	6.7
White River	2.1	5.8	7.7	1,049	5.2	20.3	9.7	49.7	0.7	14.3	0.1	6,224	0.0
Pere Marquette River	2.2	5.8	12.2	1,790	5.0	9.3	8.3	61.6	1.2	14.5	0.1	6,094	0.0
Big Sable River	0.7	5.3	2.9	476	5.3	11.5	8.0	52.4	5.0	17.0	0.8	1,975	0.0
Little Manistee River	1.4	5.4	4.5	526	4.7	3.9	12.5	68.6	0.7	9.6	0.1	1,228	0.0
Manistee River	0.2	4.7	42.8	3,559	5.7	9.6	15.9	56.4	1.4	10.9	0.1	11,951	0.0
Bear Creek	2.1	5.9	3.0	350	6.3	13.8	20.1	37.6	2.3	19.7	0.1	1,656	0.0
Betsie River	2.0	5.8	22.8	618	8.1	7.6	13.1	46.2	9.9	15.0	0.1	6,140	0.0
Platte River	0.2	5.2	4.8	471	6.6	9.9	13.4	56.2	7.5	6.1	0.2	4,697	0.0
Boardman River	1.1	5.3	6.7	716	10.8	10.4	18.8	46.7	2.1	10.9	0.2	9,824	4.0
Elk-Torch River	0.2	4.5	12.8	1,308	7.6	14.4	13.6	45.4	11.3	7.4	0.2	9,595	0.0
Cheboygan River	0.2	4.9	26.1	2,317	6.4	8.2	11.6	51.0	8.1	14.5	0.2	11,660	0.0
Black River	1.2	4.8	11.6	1,509	5.5	4.4	12.1	47.1	3.9	27.0	0.1	2,747	0.3
Thunder Bay River	0.5	4.9	12.6	2,241	6.3	11.0	8.8	40.2	2.7	31.0	0.1	7,283	1.6
Au Sable River	1.2	5.6	32.5	5,287	8.4	3.2	14.5	58.9	2.0	12.8	0.1	23,156	0.6
Au Gres River	2.1	5.3	1.1	987	6.4	23.3	7.6	37.7	2.2	22.0	0.7	4,573	0.4
Rifle River	1.6	5.5	5.0	858	9.3	16.5	8.9	44.2	1.6	19.4	0.1	6,322	1.6
Black River	1.1	5.4	0.66	1,250	6.2	74.2	1.2	10.6	0.1	7.5	0.1	6,549	4.1
Pine River	2.6	5.4	0.05	440	9.0	46.5	3.2	33.3	0.3	7.5	0.1	6,430	0.0
Belle River	2.0	5.6	1.4	512	9.5	59.7	1.7	19.0	0.3	9.7	0.2	6,416	3.2
Clinton River	2.0	5.5	n/a	1,880	51.5	20.2	1.3	14.9	2.8	8.6	0.7	95,581	152.9
River Rouge	2.7	5.5	0.32	1,033	82.9	5.4	0.5	7.2	0.7	2.9	0.3	41,345	10.9
Huron River	1.9	5.8	7.7	2,298	32.5	24.5	1.2	21.8	4.2	15.1	0.6	117,122	43.9
Raisin River	1.4	5.4	4.7	2,683	10.8	67.4	0.8	11.1	1.4	8.3	0.2	41,999	14.0
South Branch Black River	2.3	5.9	1.1	313	9.1	45.8	4.4	22.8	1.2	16.5	0.2	4,099	1.7
North Branch Black River	2.2	5.6	1.5	398	7.0	43.6	5.6	24.8	1.7	17.1	0.2	4,073	0.6
Macatawa River	1.3	5.6	0.16	292	23.5	67.8	0.7	4.0	0.2	3.1	0.9	5,960	1.1
Pine Creek	2.1	4.9	0.27	48	48.4	30.9	1.1	12.1	0.3	6.1	1.1	5,487	0.0
Pigeon River	2.7	5.0	0.08	102	11.0	66.0	2.0	15.3	0.1	5.1	0.5	1,761	0.0
Rush Creek	2.3	5.4	0.12	152	56.4	31.5	0.4	7.6	1.1	2.3	0.6	12,607	0.0
Buck Creek	2.2	4.6	0.64	3	91.3	0.0	0.6	1.4	0.9	5.8	0.0	0	0.0
Sand Creek	2.3	4.9	0.31	142	19.1	60.8	0.8	11.3	0.2	7.6	0.3	3,780	0.0
Bass River	2.1	5.1	0.20	127	11.1	63.6	2.1	16.0	0.2	6.6	0.5	2,594	0.0
Little Pigeon Creek	2.5	4.9	0.03	14	18.9	16.4	6.2	41.9	0.0	16.3	0.3	167	0.0
Black Creek	3.0	4.8	0.66	136	14.9	34.8	5.3	29.9	4.8	10.1	0.2	4,197	0.0
Silver Creek	1.7	4.4	0.37	41	11.7	0.6	15.2	63.7	4.2	4.4	0.2	643	0.0
Flower Creek	2.5	4.6	0.34	79	10.2	45.6	10.7	27.7	0.6	3.4	1.8	580	0.0
Stony Lake Outlet	0.5	5.2	1.3	160	10.1	37.7	11.7	35.1	1.0	4.1	0.3	1,635	0.0
Swan Creek	2.5	4.9	0.34	54	5.5	57.9	8.2	15.5	1.3	11.5	0.0	248	0.0
Lincoln River	2.2	5.0	0.66	215	5.6	33.2	11.8	30.6	2.1	16.5	0.2	1,087	0.0
Crystal River	0.7	4.6	1.6	110	4.7	3.4	8.7	53.7	23.7	3.3	2.4	518	0.0
Belangers Creek	1.3	4.7	0.08	25	6.7	38.4	12.7	30.8	1.5	9.9	0.0	188	0.0
Mitchell Creek	2.2	4.8	0.29	38	28.3	22.8	16.3	19.4	0.2	13.0	0.1	1,608	0.0
Jordan River	0.9	4.4	4.1	174	3.2	7.8	6.5	70.7	0.0	11.8	0.1	367	0.0
Monroe Creek	1.2	4.5	0.08	27	4.2	22.3	8.8	44.5	2.2	18.1	0.0	113	0.0
Boyne River	1.2	5.4	1.7	199	8.3	16.1	10.8	54.5	0.6	9.4	0.2	1,647	0.0
Bear River	1.5	4.8	1.6	293	6.4	13.3	7.0	48.5	6.6	18.1	0.2	2,276	0.0
Carp River	1.0	5.0	1.8	119	6.2	8.6	7.7	22.0	7.0	48.3	0.1	375	0.0
Ocqueoc River	0.9	4.7	2.4	369	4.7	6.5	11.5	43.4	2.2	31.4	0.3	576	0.0
Trout River	1.3	4.8	0.41	82	4.6	13.5	9.5	28.8	0.1	43.1	0.3	291	0.0
Little Trout River	2.4	4.9	0.06	28	5.4	27.8	7.5	14.3	0.1	44.6	0.3	95	0.0
Long Lake Creek	1.8	4.2	0.03	162	5.7	11.7	7.1	20.7	15.7	39.1	0.1	1,142	0.0
Tawas River	1.2	4.5	1.6	403	8.4	7.1	6.9	51.6	2.0	24.0	0.0	1,597	0.9
Harrington Drain	2.0	4.5	0.01	53	99.7	0.0	0.0	0.2	0.0	0.1	0.0	1,714	0.0
Marsh Creek	2.4	5.3	0.13	78	72.0	4.7	1.7	15.4	0.0	5.9	0.2	1,838	0.0
Sandy Creek	2.2	4.9	0.02	82	26.2	58.7	1.3	10.6	0.0	2.7	0.4	1,506	0.5
Cass River	1.2	5.4	2.0	2,174	6.9	57.4	2.2	19.7	0.2	13.5	0.1	15,999	2.8
Flint River	1.9	5.7	6.3	3,206	21.0	40.6	2.0	24.1	1.6	10.4	0.3	141,168	75.6
Shiawassee River	2.0	4.7	4.4	1,517	15.7	52.5	0.7	17.0	2.2	11.4	0.4	37,043	13.5
Tittabawassee River	1.9	5.6	17.5	6,211	8.6	32.8	7.3	30.6	1.5	19.1	0.2	55,635	16.3

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

Parameter	Count	Minimum	Mean	Maximum	SD	5th percentile	95th percentile
Ammonia, µg⋅L⁻¹	63	0.0	23.6	280.0	45.6	0.0	98.5
Calcium, mg⋅L⁻¹	63	30.0	62.4	160.6	21.6	33.8	98.2
Chlorine (Cl⁻), mg⋅L⁻¹	63	3.4	42.3	291.8	54.4	5.9	174.8
Dissolved oxygen, mg⋅L⁻¹	64	5.9	9.8	13.3	1.7	7.2	12.2
Dissolved organic carbon (NPOC), mg⋅L⁻¹	63	1.6	6.1	26.8	4.2	2.1	15.6
Magnesium, mg⋅L⁻¹	63	7.0	18.4	34.2	6.3	10.3	29.1
Nitrate/nitrite (NO_x), µg⋅L⁻¹	64	0.0	858.3	5,638.9	1,310.3	0.0	4,095.6
Pheophytin corrected chlorophyll a, µg⋅L⁻¹	59	0.0	0.8	4.4	1.0	0.1	3.4
pH	63	7.9	8.2	8.4	0.1	8.0	8.4
Potassium, mg⋅L⁻¹	63	0.4	2.2	9.8	1.9	0.5	6.0
Sodium, mg⋅L⁻¹	63	3.0	27.0	199.3	36.9	3.4	113.0
Soil hydraulic conductivity (K_sat), m⋅d⁻¹	64	0.5	2.2	4.7	1.1	0.6	4.2
Specific conductance, μS⋅cm⁻¹	63	257.0	527.0	1,589.0	264.2	265.2	1,039.8
Soluble reactive P, µg⋅L⁻¹	64	0.9	23.3	266.0	45.0	2.1	87.0
Sulfate, µg⋅L⁻¹	63	2.4	32.1	169.8	30.5	5.6	89.6
Total dissolved N, µg⋅L⁻¹	64	0.0	1,423.3	6,033.7	1,346.5	337.6	5,414.1
Total dissolved P, µg⋅L⁻¹	64	3.1	25.2	292.3	38.6	3.9	58.0
Total N, µg⋅L⁻¹	64	81.8	1,082.1	5,583.1	1,129.3	110.8	3,610.6
Total P, µg⋅L⁻¹	64	7.7	37.8	395.5	52.4	8.9	102.5
Total chlorophyll a, µg⋅L⁻¹	59	0.1	1.6	7.8	1.9	0.2	7.4
Precipitation,^† mm
6 h	64	0.0	0.1	9.2	1.2	—	—
12 h	64	0.0	1.9	77.9	10.2	0.0	7.9
18 h	64	0.0	3.4	78.6	11.6	0.0	30.8
24 h	64	0.0	4.4	78.6	11.9	0.0	31.0
2 d	64	0.0	6.0	78.6	11.9	0.0	31.0
3 d	64	0.0	7.7	80.1	13.7	0.0	34.2
4 d	64	0.0	8.3	80.5	13.5	0.0	34.2
6 d	64	0.0	9.0	87.3	14.1	0.0	34.2
8 d	64	0.0	11.6	92.6	16.5	0.0	57.2
Discharge, m³⋅s⁻¹	63	0.0	6.7	57.3	12.5	0.0	43.4
Water temperature, °C	64	7.0	13.1	17.5	2.6	8.2	16.6

↵^† 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

Assay	Method description	Refs.
Ammonia, µg⋅L⁻¹	Phenate method	Standard methods 4500-NH₃-G (68)
Calcium, mg⋅L⁻¹	Flame atomic absorption spectrophotometry	65
Chlorine (Cl⁻), mg⋅L⁻¹	Dionex membrane-suppression ion chromatography	65, 66
Magnesium, mg⋅L⁻¹	Flame atomic absorption spectrophotometry	65
Nitrate/nitrite, µg⋅L⁻¹	Cadmium reduction	Standard methods 4500-NO₃-E (68)
Pheophytin corrected chlorophyll a, µg⋅L⁻¹	Fluorometry with pheophytin correction following ethanol extraction	Standard methods 10200.H (68)
pH	Hydrolab multisonde	66
Potassium, mg⋅L⁻¹	Flame atomic absorption spectrophotometry (0.5% HNO₃ preservative)	66
Sodium, mg⋅L⁻¹	Flame atomic absorption spectrophotometry (0.5% HNO₃ preservative)	66
Soluble reactive phosphorus, µg⋅L⁻¹	Ascorbic acid method	Standard methods 4500-P.E. (68)
Sulfate (SO₄), µg⋅L⁻¹	Dionex membrane- suppression ion chromatography	66
Total dissolved nitrogen, µg⋅L⁻¹	Second derivative spectroscopy following persulfate digestion	67
Total dissolved phosphorus, µg⋅L⁻¹	Ascorbic acid method following persulfate digestion	Standard methods 4500-P.E and 4500-N.C (68)
Total nitrogen, µg⋅L⁻¹	Second derivative spectroscopy following persulfate digestion	67
Total phosphorus, µg⋅L⁻¹	Ascorbic acid method following persulfate digestion	Standard methods 4500-P.E and 4500-N.C (68)
Total chlorophyll a, µg⋅L⁻¹	Fluorometry following ethanol extraction	Standard methods 10200.H (68)

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Table S4.

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

Scale parameter	Minimum	Mean	Maximum	SD
Full watershed^{^†}
Area, km²	2.88	1,377	12,854	2,431
Estimated septic systems	0.0	19,579	246,033	41,902
Septic density, no. per km²	0.0	15.7	113.7	19.5
Population density, persons per km²	7	131	1,597	281
Population density on WWTP	0	98	1,589	279
Population density on septic	7	114	1,567	236
Impervious surface, km²	0.41	5.13	56.9	9.8
Urban, %	3.16	16.7	99.7	0.21
Agriculture, %	0.0	28	74.2	0.22
Open, %	0.0	6.97	20.1	0.05
Forest, %	0.19	31.4	70.7	0.18
Water, %	0.0	2.68	23.7	0.04
Wetland, %	0.07	14	48.3	0.1
Barren, %	0.0	0.31	2.45	0.0
Reduced watershed^‡
Area, km²	0.15	366	4,065	630
Estimated septic systems	0.0	22,299	246,033	45,592
Septic density, no. per km²	0.0	16.1	114	18.8
Population density, persons per km²	7	147	1,597	306
Population density on WWTP	0	115	1,589	307
Population density on septic	7	124	1,567	259
Impervious surface, km²	0.4	7.5	55.9	13.6
Urban, %	3.1	21.3	99.7	26.2
Agriculture, %	0.0	27.2	77.4	24
Open, %	0.0	6.16	18.8	5.27
Forest, %	0.0	29	71.2	19.5
Water, %	0.0	1.61	15.4	3.32
Wetland, %	0.0	13.9	47.9	12.1
Barren, %	0.0	0.77	31.1	3.87
60-m riparian buffer^‡
Area, km²	0.06	46	497	78.3
Estimated septic systems	0.0	2,672	28,256	5,596
Septic density, no. per km²	0.0	15	104	21
Population density, persons per km²	7	124	1,567	259
Population density on WWTP	0	0	0	0
Population density on septic	0	32	105	24
Impervious surface, km²	0.0	5.5	42.7	9.64
Urban, %	0.0	18.9	98.3	23
Agriculture, %	0.0	21.4	72.1	21.7
Open, %	0.0	3.64	19.4	3.8
Forest, %	0.0	22.1	62.6	14.9
Water, %	0.0	6.09	63.2	12
Wetland, %	0.0	27.3	76.3	17.9
Barren, %	0.0	0.59	24.9	3.12

↵^† 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).

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Table S5.

Anderson level 1 land use classifications and descriptions

Classification	Description	Examples	Associated NLCD classifications (code)
Urban	Intensive use with structures covering the majority of land	Cities, shopping, industrial, and commercial centers	Developed open space (21)
			Developed low intensity (22)
			Developed medium intensity (23)
			Developed high intensity (24)
Agricultural	Land used for food production	Pasture, row crop, orchards, confined feeding operations	Pasture and hay (81)
Agricultural	Land used for food production	Pasture, row crop, orchards, confined feeding operations	Cultivated crops (82)
Open	Predominant natural vegetation is grass or shrubs	Herbaceous, shrub, brush	Shrub and scrub (52)
Open	Predominant natural vegetation is grass or shrubs	Herbaceous, shrub, brush	Grassland and herbaceous (71)
Forest	Closed canopy at least 10% from timber quality trees	Deciduous, coniferous, and mixed forested	Deciduous forest (41)
			Evergreen forest (42)
			Mixed forest (43)
Water	Area predominantly covered by water throughout year	Streams, lakes, bays, and reservoirs	Water (11)
Wetland	Land with water table near land surface for significant portion of year	Marshes, swamps, perched bogs	Woody wetland (90)
Wetland		Marshes, swamps, perched bogs	Emergent herbaceous wetland (95)
Barren	Land that has less than one-third vegetative cover	Beaches, exposed rock, gravel pits	Barren (31)