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Ozone-induced Leaf Symptoms on Vegetation in the Mingo National Wildlife Refuge, Missouri
Donald D. Davis

Northeastern Naturalist, Volume 18, Issue 1 (2011): 115–122

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2011 NORTHEASTERN NATURALIST 18(1):115–122 Ozone-induced Leaf Symptoms on Vegetation in the Mingo National Wildlife Refuge, Missouri Donald D. Davis* Abstract - Field surveys were conducted during 1998, 2000, 2003, and 2004 within the Mingo National Wildlife Refuge in southeastern Missouri to determine if ambient ground-level ozone was impacting ozone-sensitive refuge vegetation. Ozone-induced leaf symptoms (stipple) were observed within the refuge during each survey year. Percentage of bioindicator plants exhibiting stipple were wild grape (16.1%) > Common Milkweed (16.0%) > ash (7.5%) > Black Cherry (6.7%) > Flowering Dogwood (4.9%) > Sassafras (2.3%) > Sweetgum (1.2%). By year, the incidence of symptomatic plants were 1998 (22.8%) > 2003 (3.9%) > 2000 (3.4%) > 2004 (2.5%). Cumulative ambient ozone levels (SUM60, ppb.hrs) monitored at the closest EPA monitor (Bonne Terre, MO) at time of survey were 1998 (44,886) > 2000 (39,611) > 2003 (38,465) > 2004 (15,147). The cumulative SUM60 threshold value of ozone needed to cause foliar symptoms on ozone-sensitive plants within the refuge appears to be ca. 10,000 ppb.hrs. Ozone injury is likely to occur on ozone-sensitive plant species within the refuge during most years. Introduction The Mingo National Wildlife Refuge (Mingo NWR), located in southeastern Missouri, was established in 1945 as a resting and wintering area for migratory waterfowl. The Mingo NWR contains 8772 ha within a former Mississippi River channel. The refuge is predominantly a bottomland-hardwood swamp, bordered on the west by the Ozark Uplift foothills and on the east by Crowley’s Ridge. Ridgetops are 123 m above mean sea level (MSL) and the basin floor is 103 m above MSL (unpublished US Fish and Wildlife Service brochures). In 1978, approximately 3000 ha of the refuge was designated the Mingo Wilderness Area, which included a Class I air quality area, giving the refuge stringent protection under the Clean Air Act as amended in 1977 (US Congress 1977). The amended act gave federal land managers of Class I areas the responsibility to protect air quality related values (AQRVs), including vegetation, wildlife, water, soils, visibility, and cultural resources. Despite protection, wilderness areas have been adversely impacted by ground-level ozone (Chappelka et al. 2003; Davis 2007a, b; Lefohn and Manning 1995; Manning et al. 1996, Neufeld et. al. 1992) and may be at risk from ambient ozone (Kohut 2007). In addition, AQRVs in Class I areas are to be protected by federal law from deterioration over time. However, in order to assess temporal deterioration, baseline values of AQRVs, such as vegetation health, must be determined to detect future changes (Shaver et al. 1995). The objectives of this survey were to: 1) determine if vegetation within the refuge was exhibiting foliar stipple induced by ambient ozone and 2) determine *Department of Plant Pathology and Penn State Institutes of Energy and the Environment, Pennsylvania State University, University Park, PA 16802; ddd2@psu.edu. 116 Northeastern Naturalist Vol. 18, No. 1 the incidence (percentage) of ozone-sensitive bioindicator plants exhibiting stipple. This paper is the fifth in a series dealing with ozone injury to vegetation within US National Wildlife Refuges (Davis 2007a, 2007b, 2009; Davis and Orendovici 2006). Methods Thompson (1980) published a list of woody flora assumed to occur within the Mingo NWR, based on plant distributions in Missouri compiled by Steyermark (1963). The author was furnished the list of potential refuge flora prior to the initial 1998 field survey. From this list, the author identified the following potential ozone-sensitive bioindicator plants (later summarized in USDOI 2003): Asclepias syriaca L. (Common Milkweed), Cercis canadensis L. (Redbud), Cornus florida L. (Flowering Dogwood), Fraxinus sp. (ash), Liquidambar styraciflua L. (Sweetgum), Prunus serotina Ehrh. (Black Cherry), Rhus aromatica Ait. (Fragrant Sumac), Rhus copallina L. var. latifolia Engl. (Winged Sumac), Sambucus canadensis L. (Black Elderberry), Sassafras albidum (Nutt.) Nees. (Sassafras), and Vitis sp. (wild grape). Ozone bioindicators are broadleaved, ozone-sensitive plants that respond to ambient ozone by producing characteristic, diagnostic adaxial “stipple” as first described by Richards et al. (1958) and later illustrated by Skelly (2000). More bioindicator species were listed as occuring within the Mingo NWR than were found at other National Wildlife Refuges surveyed by the author (Davis 2007a, 2007b, 2009; Davis and Orendovici 2006). The high number of plant species in general, as well as bioindicator species, is likely related to the refuge being located on the boundaries of several floristic provinces (Steyermark 1963, Thompson 1980). The closest EPA ozone-monitoring site to the Mingo NWR was located at Bonne Terre, MO (EPA AIRS Site #29-186-0005), approximately 130 km north (downwind) of the refuge. Ambient ground-level concentrations of ozone have been monitored at this EPA site since 1996. Prior to the first survey, the author examined ozone datasets for 1996 and 1997, and considered ozone concentrations to be great enough to induce foliar symptoms. This information, along with the presence of many species of ozone-sensitive plants within the refuge, provided impetus for these surveys. Vegetation within the refuge was surveyed during late summer 1998, 2000, 2003, and 2004 on dates listed in Table 1. Survey methods were similar to those used in other wildlife refuges (Davis 2007a, 2007b, 2009; Davis and Orendovici 2006). The author conducted preliminary field visits to locate survey sites that contained at least 10 individuals of each potential bioindicator species growing in open areas with unrestricted air movement and sunlight (Anderson et al. 1989). These criteria resulted in 10 potential survey sites being selected (Fig. 1), although all bioindicator species were not present at all sites. In addition, some ozone-sensitive species occurred only as scattered individuals, or were present in very few numbers. Bioindicator species present in sufficient numbers were ash (Green and White Ash were not distinguished), Black Cherry, Common Milkweed, Flowering Dogwood, Sassafras, Sweetgum, and wild grape. At each survey area, the author counted the total 2011 D.D. Davis 117 number of individual plants of each bioindicator species and tallied the number of plants exhibiting adaxial stipple. Stipple was noted as present or absent and percentage (incidence) of plants exhibiting stipple was calculated for each bioindicator species. Severity (percent symptomatic leaf tissue) was not evaluated. A total of 1241 plants were evaluated during the 4 years of survey. Occasionally, foliage on individual plants could not be evaluated due to severe insect injury, defoliation, or discoloration. Plant species, ozone concentration, and drought stress all influence amount of ozone-induced stipple (Showman 1991, US DOI 2003, Yuska et al. 2003). The author attempted to determine the relationship between these factors and incidence of stipple using a binary logistic model, as had been utilized in previous surveys (Davis 2007a, 2007b, 2009; Davis and Orendovici 2006). However, the Pearson’s (chi-square) goodness-of-fit statistic was not significant (Minitab Figure 1. Location of 10 survey sites (circles with site numbers) in the Mingo NWR in southeastern Missouri (Base map courtesy US Fish and Wildlife Service). 118 Northeastern Naturalist Vol. 18, No. 1 2003), and the model could not be utilized. Therefore, incidence of plants exhibiting foliar stipple is simply presented in tabular format (Table 1), and SUM60 ozone levels for April through September of each survey year are graphed to illustrate temporal ozone patterns during the growing season (Fig. 2). Results and Discussion Bioindicators Symptomatic ash, Black Cherry, Common Milkweed, Flowering Dogwood, Sassafras, Sweetgum, and wild grape exhibited classic, adaxial, ozone-induced stipple (Richards et al. 1958, Skelly 2000). These seven species had the most complete datasets, which were used in data summarization (Table 1). Across all 4 survey years and the seven species, 102 individuals out of 1241 (8.22%) exhibited stipple. Incidence was greatest on wild grape (16.1%) and Common Milkweed (16.0%), with percentage affected considerably greater than for the other species. Across all species, the greatest incidence of symptomatic plants within a year occurred in 1998 (23.0%), followed by 2003 (4.6%), 2004 (3.0%), and 2000 (2.7%). However, incidence values for Black Cherry (n = 30) and Flowering Dogwood (n = 41) were based on small samples and must be interpreted with caution. The author has utilized some of these bioindicator species during similar surveys within other national wildlife refuges. Wild grape was used to evaluate ozone-induced leaf stipple in the Edwin B. Forsythe NWR in New Jersey (Davis and Orendovici 2006) and the Cape Romain NWR in South Carolina (Davis Table 1. Summary of observations made during 1998, 2000, 2003, and 2004 surveys at the Mingo NWR. Numbers in table refer to number of plants exhibiting ozone-induced leaf stipple as compared to total number of plants evaluated for each bioindicator species; data also expressed as percentages. A = ash sp., Ch = Cherry, CM = Common Milkweed, FD = Flowering Dogwood, WS = Wild Sassafras, Sw = Sweetgum, Gr = wild grape sp. Weighted Survey date A Ch CM FD WS Sw Gr Mean 1998 (Sept. 4–7) Number plants examined 137 7 51 10 39 22 30 Number plants injured 25 2 30 1 3 1 6 Percentage 18.2 28.6 58.8 10.0 7.7 4.5 20.0 23.0 2000 (Sept. 9–11) Number plants examined 114 10 10 10 28 90 31 Number plants injured 3 0 0 0 0 1 4 Percentage 2.6 0.0 0.0 0.0 0.0 1.1 12.9 2.7 2003 (Sept. 12–14) Number plants examined 180 7 100 11 35 34 22 Number plants injured 13 0 0 1 0 0 4 Percentage 7.2 0.0 0.0 9.1 0.0 0.0 18.2 4.6 2004 (Sept 3–5) Number plants examined 113 6 39 10 30 24 41 Number plants injured 0 0 2 0 0 0 6 Percentage 0.0 0.0 5.1 0.0 0.0 0.0 14.6 3.0 Weighted mean (%) 7.5 6.7 16.0 4.9 2.3 1.2 16.1 8.2 2011 D.D. Davis 119 2009). Because of their widespread range, wild grapes are valuable bioindicators to detect ozone-induced symptoms over wide geographic areas. However, grape leaves may suffer from late-summer insect infestations that mask stipple and complicate symptom evaluation. Common Milkweed is also very sensitive to ambient ozone (Duchelle and Skelly 1981) and was used successfully as a bioindicator within the Edwin B. Forsythe NWR in New Jersey (Davis and Orendovici 2006) and in the Seney NWR in Michigan (Davis 2007b). The author considers Common Milkweed and wild grape among the most valuable ozone-sensitive bioindicators for use in such refuge surveys. Ambient ozone Ambient ozone concentrations impinging on vegetation within the Mingo NWR were approximated from the closest EPA monitoring site, located at Bonne Terre, MO, approximately 130 km north (directly downwind during the ozone season) of the refuge. It is unknown if ambient ozone levels monitored at Bonne Terre accurately reflect ambient ozone levels within the refuge, and caution must be exercised when relating ambient ozone data from Bonne Terre with ozoneinduced vegetation symptoms within the Mingo NWR. Nevertheless, SUM60 (ppb.hrs) ozone levels at Bonne Terre as of the first day of survey in each year were 44,886 ppb.hrs (1998), 39,611 ppb.hrs (2000), 38,465 ppb.hrs (2003), and 15,147 ppb.hrs (2004). The relatively high ambient ozone levels monitored during 1998, 2000, and 2003 were comparable to levels monitored at the Edwin B. Figure 2. Cumulative sum of hourly ozone concentrations ≥60 ppb (SUM60, ppb.hrs) at EPA AIRS Site # 29-186-0005, Bonne Terre, MO. The Bonne Terre monitoring site is located approximately 130 km north of the Mingo NWR, directly downwind during the ozone season. 120 Northeastern Naturalist Vol. 18, No. 1 Forsythe NWR in New Jersey, a refuge having high ambient ozone and signifi- cant ozone-induced plant symptoms (Davis and Orendovici 2006). Ozone levels at Bonne Terre were slightly greater than those monitored at the Moosehorn NWR in Maine (Davis 2007a) and Cape Romain in South Carolina (Davis 2009), but much greater than that monitored in the remote Seney NWR in the Upper Peninsula of northern Michigan (Davis 2007b); plant injury due to ambient ozone has been found in all of these refuges. As expected, seasonal ozone concentrations at Bonne Terre gradually increased from April to the end of summer (Fig. 2). However, ozone concentrations continued to rise throughout the fall (data not shown) and did not level off as had occurred in other refuges (Davis 2007a, 2007b, 2009; Davis and Orendovici 2006). In fact, during the non-survey year of 1999, the SUM60 ozone levels at Bonne Terre ultimately reached approximately 80,000 ppb.hrs in November (data not shown), an extremely high level of ozone. The possible impact of this high, late-season ozone on refuge vegetation, or other refuge biota, is unknown. Conclusions If the ambient ozone concentrations monitored at the EPA site at Bonne Terre reflect those at the Mingo NWR, the threshold value of SUM60 ozone needed to cause foliar symptoms on ozone-sensitive plants within the Mingo NWR was likely ca. ≤10,000 ppb.hrs (Fig. 1, Table 1), similar to the value estimated for the Moosehorn NWR in Maine (Davis 2007a). In addition, phytotoxic concentrations of ozone may occur by early June within the Mingo NWR (Fig. 2), revealing that ozone stress may occur on late-spring or early-summer ephemeral plants (Barbo et al. 1998, Davis and Orendovici 2006). Ozone injury that occurs on these early season plants would not be detected during routine annual ozone injury surveys, which are normally conducted in late summer (i.e., August). By August, new growth might obscure ozone-induced symptoms formed during the spring, and/or injured leaves may have excised by late summer. Manning (2003) cautioned that use of cumulative ozone data as threshold values for predicting ozone injury to plants should take into account biological and environmental factors that affect ozone uptake via stomata. For example, soil moisture stress can induce stomatal closure, which limits ozone uptake, thereby reducing or eliminating subsequent ozone injury even in years of high ambient ozone concentrations (Showman 1991, Yuska et al. 2003). In summary, foliar symptoms induced by ambient ground-level ozone were observed on ozone-sensitive bioindicator plants within the Mingo NWR, which includes a Class I air quality area. Ozone-induced stipple was observed during each survey year, and likely occurs annually within the refuge. The highest incidence of stipple was recorded during 1998, a year of relatively high ozone concentrations. It is likely that environmental conditions for gas (ozone) uptake and expression of foliar symptoms were also ideal during this year. Future surveys to evaluate ozone-induced symptoms in the Mingo NWR should be conducted in August, and should emphasize use of Common Milkweed and wild grape as bioindicators. The US Fish and Wildlife Service should consider results of this and similar surveys when making air quality management decisions, including 2011 D.D. Davis 121 review of Prevention of Significant Deterioration permits, regarding the Mingo NWR. In addition, an ozone monitor should be located within the refuge, in or near the Class I Wilderness Area. Acknowledgments The author gratefully acknowledges receiving financial support from the US Fish and Wildlife Service, Air Quality Branch, Denver and The Pennsylvania Department of Environmental Protection, Bureau of Air Quality, Harrisburg. The author also thanks David Joseph, National Park Service, Air Resources Division, Lakewood, CO, for supplying the EPA ozone data sets. Literature Cited Anderson, R.L., C.M. Huber, R.P. Belanger, J. Knighten, T. McCartney, and B. 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