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

Discussion


For most botulism outbreaks in wild waterfowl, the site of botulinum toxin ingestion and the population of birds that is actually at risk for contracting botulism are unknown, which makes comparisons to local environmental conditions difficult. In contrast, the use of sentinel mallards in our study provided a known and consistent population at risk, assured knowledge of the site of toxin ingestion, and permitted the calculation of botulism mortality rates. Botulism outbreaks in sentinel mallards occurred 4 times during our study, with weekly losses ranging from 1.0 to 8.8 birds/100 at risk. For a typical fall (Sept–Oct) mallard population of ≥25,000 at SNWR (J. G. Mensik, SNWR, personal communication), mortality rates of 1–9% could result in the death of 250–2,200 mallards/week, assuming the entire population was at equal risk of contracting botulism.

Comparisons Between Outbreak and Nonoutbreak Wetlands

Factor scores for REDOX were generally lower in outbreak wetlands than nonoutbreak wetlands. In biological systems, redox potential of the surrounding environment influences the direction of biochemical reactions, the operation of enzyme systems and electron acceptors, and thus the metabolic processes that yield energy for growth (Hewitt 1950). In soils or sediments, measured values of redox potential reflect the intensity of reduction (Gambrell and Patrick 1978) and the type of microbial activity that prevails (Watanabe and Furusaka 1980), but measurements of redox potential are often difficult to interpret. Because Clostridium botulinum is a strict anaerobe, one might expect more growth to occur at lower redox potential. However, laboratory studies suggest, in the absence of oxygen, redox potential alone does not appear to be a limiting factor in the growth of Clostridium botulinum (Smoot and Pierson 1979) and may interact with other factors such as salinity and pH. The association between botulism outbreaks and redox potential may possibly be indirect and due to the competitive or even synergistic effects of other wetland microbes.

No other consistent differences were found between factor scores in outbreak and nonoutbreak wetlands, although significant temporal changes were detected for REDOX, TEMP, and pHSOIL factors (Figs. 2–4). The strong seasonal pattern for TEMP was expected, as soil and water temperature steadily declined from July to October. For REDOX and pHSOIL, however, yearly differences, as well as seasonal patterns, were evident. In 1988, pHSOIL and REDOX patterns appear different than patterns observed in 1987 and 1989. Interestingly, in 1988, no botulism outbreaks were detected in sentinel or free-ranging wild birds anywhere on the refuge, which was fairly unusual for SNWR. We also found a significant interaction for SC–pHW between wetland classification and time (Fig. 5). In 1987 and 1989, when botulism outbreaks occurred, seasonal trends in SC–pHW were similar in values and ranges in outbreak wetlands. For nonoutbreak wetlands, however, the seasonal trends differed: SC–pHW decreased during 1987 but increased during 1989. In 1988, when no botulism occurred, values of SC–pHW in both outbreak and nonoutbreak wetlands were lower than 1987 and 1989 and were without apparent seasonal trends.

Comparison Within Outbreak Wetlands

For outbreak wetlands, logistic regression analysis revealed that the probability of botulism in sentinel mallards increased with higher TEMP and INVERT factor scores and lower TURB factor scores. Botulism outbreaks occurred in the wetlands we studied only during sampling intervals with water temperatures ≥18.3°C (Table 1). Water temperature ranged from 13.0 to 26.6°C during nonoutbreak intervals and ranged from 9.6 to 26.8°C in nonoutbreak wetlands. The seasonal occurrence of botulism in waterbirds has long been recognized (Kalmbach and Gunderson 1934). Thus, an association between wetland temperature and the probability of botulism outbreaks was not very surprising. However, elevated temperature alone does not appear to initiate outbreaks.

Invertebrates are thought to be the primary source of toxin for birds, acting as either a substrate for toxin production or a means of transfer from the substrate to the birds. Previous investigators (Jensen and Allen 1960) presented empirical evidence suggesting botulism outbreaks at the Bear River Migratory Bird Refuge in Utah coincided with a sharp decline of the predominant benthic invertebrates following a population peak, presumably in response to decreasing oxygen. The authors postulated that dead invertebrates provided substrate that facilitated bacterial growth and production of botulinum toxin. In our study, the average biomass of invertebrates was higher in outbreak intervals (total: 0.010 g; benthic: 0.012 g) than either nonoutbreak intervals (total: 0.006 g; benthic: 0.009 g) or nonoutbreak wetlands (total: 0.005 g; benthic: 0.008 g; Table 1). Hence, our results suggested invertebrates may play a role in initiating botulism outbreaks by providing a means of toxin transfer.

Average turbidity during outbreak intervals (11.4 units) was less than half the values during nonoutbreak intervals (23.8 units) and in nonoutbreak wetlands (25.6 units; Table 1). Lower turbidity in a wetland would allow more light penetration, thereby increasing primary productivity, and we would not expect this factor to directly affect the growth of C. botulinum. More likely, the association between decreasing turbidity and botulism outbreaks is indirect and due to the influence of turbidity on invertebrates or other microbial populations, and hence their interactions with C. botulinum.

Botulism mortality rates were associated with different environmental factors in P-2 and P-8 (the 2 enclosures where outbreaks occurred), and these relations appeared to contradict the results of our previous analyses. In P-2, a higher botulism mortality rate was positively associated with lower INVERT and SC–pHW factor scores, but the range of weekly botulism mortality rates was limited in this enclosure (0.013–0.029). Perhaps the changes in invertebrate and SC–pHW factor scores were related to other wetland characteristics and were simply coincident to changes in the botulism mortality rate. In P-8, which experienced a wider range of botulism mortality (0.010–0.088), the daily rates were associated with higher turbidity, seemingly in contrast to our logistic regression analysis which indicated that higher turbidity decreased the probability of an outbreak. We suspect increased investigator activity within the enclosure upon discovery of a botulism outbreak may have inadvertently elevated the turbidity of the water and resulted in an artificial association.

Interestingly, dissolved oxygen, percent organic matter, and water depth (the DO–DEPTH–POM factor), variables previously believed to play a major role in the initiation of botulism outbreaks (Kalmbach and Gunderson 1934, Quortrup and Holt 1941, Rosen 1971), were not important in our study. We found no association between DO–DEPTH–POM factor scores and the probability of botulism outbreaks within an enclosure, nor were any differences in this factor detected between outbreak and nonoutbreak wetlands. Botulism outbreaks occurred in sentinel mallards in wetlands with low to moderate levels of dissolved oxygen in the water column (1.5–7.0 mg/L), a wide range of organic matter in the sediments (4.5–22.5%), and moderate water depth (36–101 cm; Table 1). Our study showed that shallow water is not a prerequisite to, nor is dissolved oxygen predictive of, a botulism outbreak in waterbirds.


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