USGS - science for a changing world

Northern Prairie Wildlife Research Center

  Home About NPWRC Our Science Staff Employment Contacts Common Questions About the Site

Environmental Characteristics Associated with the Occurrence of Avian Botulism in Wetlands of a Northern California Refuge

Results


Of the 10 wetlands originally included in the study, only the 4 wetlands flooded year-round were included in our analyses. Outbreaks in seasonally flooded wetlands were inconsistent, and the environmental data collected in these wetlands were insufficient to warrant statistical evaluation.

Botulism outbreaks occurred in sentinel mallards in 2 wetland enclosures (P-2, P-8) in both 1987 and 1989 (Fig. 1); no outbreaks were detected in 1988. During these botulism outbreaks, weekly mortality rates in sentinel mallards ranged from 1.0 to 8.8 deaths/100 birds. Although botulinum toxin was found in 2 carcasses in another enclosure (T-F) in 1988, these cases were widely separated in time (>2 months), and botulism was not detected in wild birds in this or any other wetland in 1988. Because our criteria for classifying outbreak wetlands for this study required the detection of >1 carcass with botulinum toxin, the cases in T-F in 1988 were not considered to constitute an outbreak.

GIF -- bar graph of botulism mortality weekly rates

The range and variability of wetland conditions in our 4 study sites (means, minimums, maximums) fell within expected ranges (Table 1). Water temperatures varied from 13.0 to 26.8°C, with sediment temperatures generally 1–2 degrees higher. The water was very fresh, with specific conductivity values in the range of 88–896 µmhos/cm, and water pH was neutral to moderately alkaline, within a range of 6.0–8.4. Invertebrates included in our statistical analysis (counts and benthic biomass) included gastropods, nematodes, oligochaetes, eubranchipods, lymnaeid snails, cyclopoid copepods, ostracods, unknown dipterans, ceratopogonids, chaoborids, culicids, tipulids, ephydrids, notonectids, muscids, stratiomyids, unknown chironomids, and chironomids of the genera Goeldichironomus, Glyptotendipes, Tanypus, and Procladius. Other invertebrates had very low biomass or counts and were only included in total biomass calculations.

Table 1. Environmental variables measured and averaged (no. of sampling intervals [n], mean [GIF -- mean x], minimum [min] and maximum [max]) in 1.6-ha wetland enclosures where botulism outbreaks occured (outbreak wetlands) and did not occur (nonoutbreak wetlands) in sentinel mallards at the Sacramento National Wildlife Refuge, California, 1987-89. Outbreak wetlands were further separated into outbreak intervals (i.e., when botulism outbreaks occured in sentinel mallards) and nonoutbreak intervals (i.e., when no outbreaks occured). For each sampling interval, environmental measurement averaged from 5 locations distributed throughout the wetland enclosure included redox potential (redox) and standardized redox potential (stand. redox) measured in millivolts, temperature measured in °C, specific conductivity measured in µmhos/cm, pH, numbers of benthic invertebrates (benthic counts; log transformed), mass (g) of benthic invertebrates (benthic biomass; log transformed), mass (g) of total invertebrates (total biomass; log transformed), dissolved oxygen in the water measured in mg/L, percent organic matter in the sediments, water depth measured in centimeters, and water turbidity measured in nepholometer turbidity units.

  Outbreak wetlands (P-2, P-8)  
  Outbreak intervals Nonoutbreak intervals Nonoutbreak wetlands (T-F, T-19)
Variable n Mean X min max n Mean of X min max n Mean of X min max
Redox Wa 15 208 50 338 40 196 -26 467 56 219 8 477
Redox S1b 15 111 -24 303 40 19 -171 254 56 80 -80 337
Redox S2c 15 62 -40 256 39 47 -165 289 56 49 -174 375
Stand. redox W 15 251 86 367 40 227 16 505 56 248 17 485
Stand. redox S1 15 109 -43 252 40 28 -177 274 56 86 -65 317
Stand. redox S2 15 61 -43 252 39 47 -165 289 56 63 -160 359
Temperature W 15 22.4 18.3 26.5 41 20.6 13.0 26.6 57 20.4 12.1 26.8
Temperature S1 15 23.9 19.4 28.3 40 22.1 13.5 28.0 56 21.7 13.7 27.6
Temperature S2 15 23.8 19.5 27.6 39 22.1 13.9 28.0 56 21.8 14.4 27.3
Conductivity W 15 474 285 882 41 428 231 896 57 336 88 864
Conductivity S1 15 793 584 1086 40 733 530 1018 56 670 222 1186
Conductivity S2 15 1028 745 1275 39 1020 688 1510 56 1140 679 1819
pH W 15 7.73 7.09 8.80 41 7.54 7.00 8.77 57 7.51 6.38 8.75
pH S1 13 7.26 7.00 7.47 38 7.26 6.75 8.03 53 7.19 6.50 8.35
pH S2 13 7.14 6.94 7.53 37 7.30 6.73 8.02 53 7.28 5.99 8.87
Benthic counts 15 1.68 1.24 2.15 38 1.53 0.83 2.41 55 1.72 0.87 2.64
Benthic biomass 15 0.010 0.001 0.042 38 0.006 0.000 0.049 55 0.005 0.00 0.02
Total biomass 15 0.012 0.003 0.045 38 0.009 0.002 0.051 55 0.008 0.00 0.08
Dissolved oxygen 15 3.94 1.51 7.05 41 4.20 0.92 10.32 57 4.20 1.00 10.05
% organic matter 15 12.1 4.5 22.5 39 10.8 4.7 18.3 57 6.1 3.8 7.8
Depth 15 52.5 35.8 100.8 41 53.6 22.8 105.7 57 53.8 34.8 85.6
Turbidity 15 11.4 2.4 34.3 40 23.8 2.2 150.0 57 25.6 2.1 78.2
aW refers to water samples collected 7.5 cm above the sediment-water interface.
bS1 refers to interstitial water samples collected 2.5 cm below the sediment-water interface.
cS2 refers to interstitial wtaer samples collected 11.25 cm below the sediment-water interface.

Seven principal components identified by factor analysis accounted for 79% of the variation in the original 22 environmental parameters. Rotated factor loadings showed that environmental parameters in the soil and water were highly correlated (Table 2). The resulting 7 environmental factors had a relatively simple interpretation in relation to the original environmental parameters. Redox potential variables (REDOX) explained the largest portion of the variation (23%) found in the environmental measurements. Temperature variables (TEMP) and a factor consisting of specific conductivity and water pH (SC–pHW) accounted for an additional 26% of the variation. The fourth factor (pHSOIL) represented soil pH, and the fifth factor (INVERT) represented variables related to invertebrates. The sixth factor (DO–DEPTH–POM) was positively associated with dissolved oxygen and water depth but negatively associated with percent organic matter. Water turbidity was the only environmental variable strongly represented by the seventh factor (TURB).

Table 2. Seven principal factor patterns after varimax rotation of environmental variables measured in wetland enclosures at the Sacremento National Wildlife Refuge, California, 1987-89. Standardized regression coefficients indicate sign and relative strength of environmental variables influencing each factor. Only coefficients are included.
Factor Environmental variable Coefficient
REDOX Redox potential Wa 0.858
Redox potential S1b 0.925
Redox potential S2c 0.937
Standardized redox potential W 0.863
Standardized redox potential S1 0.924
Standardized redox potential S2 0.923
TEMP Temperature W 0.962
Temperature S1 0.951
Temperature S2 0.948
SC–pHW Specific conductivity W 0.743
Specific conductivity S1 0.850
Specific conductivity S2 0.760
pHSOIL pH W 0.558
pH S1 0.926
pH S2 0.947
INVERT Benthic invertebrates 0.466
Benthic ivertebrate biomass 0.910
Total invertebrate biomass 0.905
DO–DEPTH–POM Dissolved Oxygen 0.575
Depth 0.556
Percent organic matter -0.647
TURB Turbidity 0.906
aW refers to water samples collected 7.5 cm above the sediment-water interface.
bS1 refers to interstitial water samples collected 2.5 cm below the sediment-water interface.
cS2 refers to interstitial water saples collected 11.25 cm below the sediment-water interface.

Comparisons Between Outbreak and Nonoutbreak Wetlands

Repeated measures ANOVA indicated outbreak wetlands had lower REDOX factor scores (F1,2 = 18.3, P = 0.05) than nonoutbreak wetlands during our study (Fig. 2). None of the remaining environmental factors showed a consistent difference (Ps > 0.20) between the outbreak and nonoutbreak wetlands. Significant changes in environmental factors among sampling intervals were found for REDOX (F19,38 = 12.6, P < 0.01; Fig. 2), TEMP (F19,38 = 24.8, P < 0.01; Fig. 3), pHSOIL (F19,38 = 2.88; P < 0.01; Fig. 4), and SC–pHW (F19,38 = 3.42, P < 0.01; Fig. 5). No sampling interval differences (Ps > 0.20) were found for INVERT, DO–DEPTH–POM, or TURB factors. The only significant interaction between botulism outbreaks and sampling intervals was found for SC–pHW (F19,38 = 2.14; P = 0.02).

GIF -- redox potential and temp scores in wetlands

GIF -- sediment pH and water conductivity in wetlands

Comparisons Within Outbreak Wetlands

In outbreak wetlands (P-2, P-8), logistic regression analyses showed an association between the probability of botulism in sentinel mallards and TEMP (X 21 = 8.95, P < 0.01), INVERT (X 21 = 5.64, P = 0.02), and TURB (X 21 = 12.78, P < 0.01) factors. No differences (Ps > 0.10) were found for other environmental factors or serial correlation among sequential sampling intervals, although REDOX ( X 21 = 2.47, P = 0.12) and pHSOIL (X 21 = 2.61, P = 0.11) approached our significance criteria. Coefficients from the logistic regression model indicated increasing values of TEMP and INVERT were correlated with a higher probability of botulism outbreaks. However, water turbidity appeared to have the opposite relation: decreasing levels of turbidity were correlated with a higher probability of botulism outbreaks. When REDOX and pHSOIL were included in the logistic regression model, they showed opposite effects. Botulism outbreaks were positively related to REDOX and negatively related to pHSOIL.

Preliminary examination of daily mortality rates during outbreaks indicated a larger range of weekly mortality rates in P-8 than in P-2 (Fig. 1). Therefore, correlations between mortality rates and the 7 principal factors were conducted separately for each enclosure. For P-2, daily mortality rates during botulism outbreaks (excluding Jul 1987 due to missing factor data) were negatively correlated with SC–pHW (PPP = -0.87, P = 0.02, n = 6) and INVERT (PPP = -0.90, P = 0.01, n = 6) factors. In contrast, daily botulism mortality rates for P-8 (excluding Jul 1987) were positively correlated with TURB (PPP = 0.83, P = 0.02, n = 7).


Previous Section -- Methods
Return to Contents
Next Section -- Discussion

Accessibility FOIA Privacy Policies and Notices

Take Pride in America logo USA.gov logo U.S. Department of the Interior | U.S. Geological Survey
URL: http://www.npwrc.usgs.gov/resource/birds/botulsm/result.htm
Page Contact Information: Webmaster
Page Last Modified: Friday, 01-Feb-2013 18:14:39 EST
Menlo Park, CA [caww54]