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Relationship between habitat type, fire frequency, and Amblyomma americanum populations in east-central Alabama

2012; Wiley; Volume: 37; Issue: 2 Linguagem: Inglês

10.1111/j.1948-7134.2012.00241.x

1948-7134

D.C. Willis, Robert Carter, Chris Murdock, Benjie G. Blair,

Viral Infections and Vectors

Ticks were collected from 20 sites in the Calhoun, Cherokee, and Cleburne Counties in east-central Alabama areas to determine the relationship between plant physiognomy, environmental variables, and tick populations. Sites investigated included various burning regimes, wildland-urban–interface (WUI), a college campus, and an unmanaged area. Amblyomma americanum (L.) (Acari: Ixodidae) dominated the tick population while Ixodes scapularis Say was not encountered. There were complex differences in tick populations among site conditions. After prescribed burning, the tick population size was small but was larger in subsequent 2- and 5-year post-burn sites. An increase in Odocoileus virginianus foraging in recently burned sites is likely responsible for this phenomenon. WUI areas had the largest tick populations likely due to Odocoileus virginianus activity in an area that provides cover, forage, and a connection to a wildlife refuge. It is possible that the likelihood of humans coming in contact with ticks and tick-borne diseases is greater in WUI areas than in unbroken contiguous forest. A. americanum showed a positive correlation with percent cover of grass and leaf litter mass and a negative relationship with pine sapling density. Variables expected to be strongly correlated with A. americanum populations such as soil moisture, canopy closure, and tree density were found to have weak correlations. Ticks are capable of vectoring a wide range of pathogenic viruses, bacteria, and protozoans (Adelson et al. 2004) including Rocky Mountain spotted fever (Rickettsia rickettsii), Lyme disease (Borrelia burgdorferi), babesiosis (Babesia sp.), tularemia (Francisella tularensis), human monocytotrophic ehrlichiosis (Ehrlichia chaffeensis), Q fever (Coxiella burnetii), and Powassan viral encephalitis (Flavivirus). The genus Borrelia includes several pathogenic strains of motile spirochetes that are vectored by ticks. Lyme disease (Borrelia burgdorferi) is the most common vector-borne disease in the U.S. (Burkot et al. 2001, CDC 2005) and has been found in the lone star tick (Amblyomma americanum). However, A. americanum has not been proven capable of transmitting B. burgdorferi to humans (Schulze et al. 1984, Levine et al. 1989, Luckhart et al. 1991, Clark 2004). Amblyomma americanum has a more aggressive and indiscriminant questing behavior than most other tick species in the U.S. (Bishopp and Trembley 1945, Hair and Howell 1970) and is the dominant hard tick species in much of the southern U.S. (Stegall-Faulk et al. 2003). In Georgia and South Carolina, 83% of ticks collected by Felz et al. (1996) were A. americanum, while in North Carolina 95% collected were A. americanum (Kennamer et al. 1992). Hair (1979) reported that 57% of white-tailed deer (Odocoileus virginianus) fawns die from A. americanum infestations in portions of the Ozarks. Amblyomma americanum population size is strongly influenced by suitable host and host habitat. Although most mammals are potential hosts for at least one life stage, O. virginicus is the most important host for A. americanum providing a blood meal for all life stages (Mount et al. 1993, Childs and Paddock 2003) and providing a means of transport to new habitats (Paddock and Yabsley 2007). Vegetation manipulation such as mowing (Mount 1981), canopy removal (Davidson et al. 1994), and prescribed fire (Allan 2009) have been reported to influence Amblyomma americanum populations. Removal of understory plants reduces questing habitat and lowers the amount of leaf litter on the forest floor, which lowers survival of the ticks. Canopy reduction reduces humidity while increasing ground-level temperatures and light penetration. Increased temperature and decreased humidity can decrease reproductive efficiency and molting success (Davidson et al. 1994). At humidity levels below 85%, ticks (A. americanum and I. scapularis) are restricted to microhabitats where humidity is higher (Adler et al. 1992, Koch and Burg 2006), although A. americanum is less sensitive than Ixodes species (Adler et al. 1992, Schulze et al. 2002). Following a prescribed fire, Davidson et al. (1994) found a population decline the year after a burn likely due to reduced leaf litter, which alters the microhabitats used by all life stages of ticks. However, Allan (2009) found a peak in Amblyomma americanum populations the second year after prescribed burns. The objective of this study was to investigate the relationship between tick populations and habitat conditions in urbanized and forested habitats in three counties in east-central Alabama. It was expected that Ixodes scapularis would be present in small numbers while Amblyomma americanum would be the primary tick captured. It was hypothesized that there would be a positive correlation between tick populations and soil moisture, tree density, tree basal area, and canopy closure. Increased tree density and basal area will increase crown closure and decrease evaporation from the litter layer. The resulting increase in humidity could increase tick activity and population size. It also was hypothesized that tick populations would be small immediately after a fire. The study area consisted of 20 sites in Calhoun, Cleburne, and Cherokee counties in east-central Alabama. Sites were chosen to include a wide range of vegetation cover types, geophysical properties, burn regimes, and land usage histories. Twelve sites were in the Shoal Creek District of the Talladega National Forest in Cleburne County. Three wildland-urban-interface (WUI) sites were located in the McClellan community near Anniston in Calhoun County. Two sites were in forested patches located on the campus of Jacksonville State University in Calhoun County. The remaining three unmanaged sites were located on private lands in Cherokee County. The study area is located within the Ridge and Valley physiographic province near the southern terminus of the Appalachian Mountains. Elevation varies from approximately 200 to over 700 m above mean sea level (msl). Rainfall accounts for the majority of recorded yearly precipitation with an average of 1.45 m per year. Precipitation is distributed throughout the year, with summer months typically drier than winter/spring. Temperatures range from a January average of 3.6° C to a July average of 25.4° C (USDA Soil Conservation Service 1961). Six sites on the Talladega National Forest were burned biennially to restore Pinus palustris forests and manage for Picoides borealis and Colinus virginianus, while the remaining six sites were not burned on a regular basis. All sites on the Talladega National Forest were along a 4 km portion of Forest Service Road 500 (Table 1). Sites varied from 0.33 to 1.5 km apart with each treatment having one plot in close proximity to a stream while the other two sites were upland pine or hardwood dominated. Three biennially burned sites were last treated in 2008 and three in 2007. Three sites were burned in 2003 (5-year burn), while the remaining three were burned in 1993 (15-year burn). The three WUI sites in the McClellan community were approximately 0.8 km apart and consisted of small patches of forest and fields mingled with commercial and residential development. Most forested areas were narrow corridors and small patches divided by buildings, houses, and roads. One site was adjacent to a stream while the remaining sites were hardwood or pine dominated. All sites were less than 1.2 km from contiguous forest of the Mountain Longleaf Wildlife Refuge. Two sites were located on the campus of Jacksonville State University in small forested patches surrounded by roads or buildings. Between the campus sites and a contiguous forest were over 1.6 km of densely populated neighborhoods, thus reducing large mammal access to the sites. Three sites located in Cherokee County were unmanaged and provided control sites. One site was adjacent to a stream while the remaining two were in hardwood dominated upland sites. (Table 1). The vegetative structure at each site was measured including the tree, sapling, seedling, and herb strata. The methodology used was a modified Carolina Vegetation Survey with 20 × 20 m plots divided into 10 × 10 m subplots (Peet et al. 1998). The diameter of the trees and saplings was measured at breast-height (1.4 m) throughout the plot. Woody stems > 11.4 cm at breast height were considered trees, while stems < 11.4 cm were saplings. Woody stems < 1.4 m were considered seedlings. Cover calls for seedlings, shrubs, vines, grasses, ferns, and herbs were conducted in each of the 10 × 10 m subplots at each site. Forest canopy crown closure was determined with a concave spherical densiometer (Lemmon 1956, 1957). In the Talladega National Forest sites, leaf litter was collected in the winter of 2009 in four 1 m2 subplots in each plot. The collection did not include partially decomposed leaves. The leaf litter was dried and mass determined. Soil moisture was measured at each site monthly (at the time of tick collection) with a soil moisture probe (Soilmoisture Equipment Corporation model 2900F1 Quick Draw). The probe was inserted 20–40 cm deep (variation due to rocks) and left for the duration of the 20-min tick sampling period. The moisture value was then read and the probe removed. Ticks were collected using a modified flag method (Goddard 1997) in the 20 × 20 m plots from June, 2008 to May, 2009. The cloth was 1 m2 white flannel material attached to a 5/8"× 40" wooden dowel forming a "flag" structure. The cloth was dragged through vegetation and across the forest floor at each site for 20 min once monthly. All collections were completed before 11:00 within a period of approximately three days with similar meteorological conditions. The cloths were inspected approximately each 5–10 m during the sampling. Any ticks found on the cloths were immediately removed and preserved in 70% ethanol or isopropanol. Preserved ticks were identified by species, sex, and life stage (adult or nymph) using a tick key for Alabama (Cooney and Hays 1972). The tick population size and tree and sapling variables by treatment were compared using pairwise multiresponse permutation procedures (MRPP-Sorenson's distance) and permutational multivariate analysis of variance (PERMANOVA; Anderson 2001, McArdle and Anderson 2001) with PC-ORD (McCune and Mefford 2006). PERMANOVA does not assume normally distributed data. MRPP (Mielke and Berry 2001) is a nonparametric procedure for testing the hypothesis of no difference between two or more groups based on a measure of distance (in this case, Sorensen's distance) between groups. Statistic A indicates the within group agreement compared to random expectation. An A of 1 indicates all samples within a group are the same, 0 indicates the expected heterogeneity, and negative values indicate greater heterogeneity than expected (McCune and Grace 2002). A significant p value indicates that the hypothesis of no difference is rejected. A significance level of p < 0.05 was used due to the highly variable nature of ecological data. The Shapiro-Wilk test for normality was performed before regression and correlation analysis was performed. The data was then log-transformed before Pearson's correlation analysis and least squares regression (SYSTAT 2004) was used to determine the relationships between tick populations and soil moisture, canopy closure, vegetation density, vegetation basal area, leaf litter mass, and understory cover. A total of 475 ticks was collected, with Dermacentor variabilis accounting for 3.7% (n=20). Amblyomma americanum accounted for 96.3% of ticks with 69 (14.8%) adult females, 57 (12.4%) adult males, and the remaining 328 (72.8%) nymphs. A. americanum collection totals per site ranged from 0–95 (Table 2). The highest number collected from a single site/month was 55 (June, 2008). No Ixodes species were encountered. Abundance was extremely low from October through March for both nymphs and adults and was not included in Table 2. There was considerable variation in tick populations between treatment types. WUI sites accounted for 44.49% of all collections. Five-year and 2-year post-burn treatments accounted for 24.23% and 13.22%, respectively. All other treatments accounted for less than 10% each (Table 2). In the Talladega National Forest sites, the greatest number of ticks was in the 5-year post-burn sites and the least in the 15-year post-burn sites. The number of ticks more than doubled from year 1 to year 2 post-burn (Table 2). Shapiro-Wilk test statistic for normality indicated that Amblyomma americanum numbers and environmental variables were not normally distributed except hardwood tree basal area, hardwood sapling density, leaf litter mass, and soil moisture. Analysis of the A. americanum population size with PERMANOVA indicated that treatments were significantly different (p = 0.001), however pairwise site comparisons (p<0.05) were not significantly different (Table 3) despite the large differences in the number of A. americanum collected (Table 2). MRPP (p<0.05) revealed numerous statistical differences between treatments (Table 3). Tick populations were significantly different between WUI sites and 15-year post-burn sites, while the difference between WUI and five-year sites was not found to be statistically different (Table 3) although WUI had nearly twice as many ticks (Table 2). WUI tick populations differed significantly from unmanaged sites (Table 3) due to the very low populations in unmanaged sites (Table 2). Although the WUI and campus sites were both small forest patches, the urban sites had a greater and significantly different number of A. americanum (Table 2 and 3). A. americanum populations in the 5-year site were much higher than the 1-year sites (Table 2) and statistically different (Table 3). Campus and 15-year sites were not significantly different despite being in located in very different environments. Percent cover of grass was greatest in 1- and 2-year sites (Table 4) reflecting the abundant sunlight available (crown closure of 82% and 69%, respectively). Percent grass was nearly equal in 5-year and urban sites (16%) but nearly absent from 15-year and campus sites. Forb percent cover was greatest in 1- and 2-year sites, respectively, but low in remaining sites. Five- and 15-year post-burn sites had the greatest leaf litter mass (Table 4), and leaf litter had the strongest correlation (Table 5) with tick populations on the Talladega National Forest sites. Sapling and tree strata were significantly different (p<0.05) depending on the comparison (Table 6 and 7). When comparing sapling variables, WUI sites were statistically different from unmanaged sites, while the burned treatments on the Talladega National Forest were not different from each other (Table 6). Tree density was high in WUI areas, but hardwood basal area was greater in unmanaged areas (Table 8). Sapling density, especially hardwood, and basal area was much higher in WUI areas likely due to greater light availability in small forested patches surrounded by open areas (Table 9). The tick population, environmental, and vegetation variables failed to have a normal distribution (Shapiro-Wilks test) and were log-transformed. Pearson's correlation analysis indicated positive relationships between Amblyomma americanum and percent cover of grass and leaf litter mass and a negative relationship with pine sapling density. Soil moisture and canopy did not show a strong relationship to A. americanum. For least means squares regressions, pine sapling density, leaf litter mass, and percent cover of grass had the strongest relationships with A. americanum (Table 5). The poor relationship between hardwood sapling variables and seedling cover combined with the negative correlation with pine sapling density indicates the sites more suitable for A. americanum have an open understory with abundant grass. Amblyomma americanum dominated collections at all sites, likely reflecting the aggressive nature of the species and the population structure of the area. A. americanum collections peaked in early summer (Table 2) as expected for the southeastern U.S. (Jackson et al. 1996). The WUI sites accounted for 44.5% of the ticks collected. The WUI sites were characterized by small forested patches interspersed with residential or commercial development and open fields in close proximity to the Mountain Longleaf National Wildlife Refuge. Small patch sizes have been shown to contain higher populations of small and medium-sized mammals, which are hosts for many tick species (Debinski and Holt 2000). Concentrated host populations could be a possible explanation for the high tick population in WUI sites. The increased edge habitat and small patches interspersed with grassy open sites in WUI areas may increase host populations (Allan et al. 2003, Jackson et al. 2006). The risk for acquisition of any form of tick-borne disease may increase in WUI areas because human interaction with large tick populations can be more likely. Campus sites were in an urban setting but were not connected directly to large forested areas and were surrounded by pavement and buildings. It is likely that populations of medium-to-large mammals are less common in the small campus forested patches due to human disturbance and a lack of nearby grazing areas. Prescribed burning played a role in modulating tick populations. The number of ticks collected following a prescribed burn was relatively low but quickly increased (within 2–5 years) to levels exceeding unburned sites (Table 2). This trend of low numbers after a fire followed by a larger numbers was also found in Georgia (Davidson et al. 1994). Jacobson and Hurst (1979) found that Eastern wild turkey poults foraging in sites 3 months post-burn in Mississippi had a lower number of Amblyomma americanum than those foraging in an area burned three years prior. Allan (2009) found that Amblyomma americanum populations in the Missouri Ozark Mountains were significantly higher in sites 2 years after a burn than in sites immediately after a burn. The number of ticks was approximately six times higher than those of unburned control sites 2 years after a fire. Prescribed fire tends to alter microhabitat characteristics such as leaf litter depth and humidity, thus making a site less suitable for ticks (Davidson et al. 1994, Iverson and Hutchinson 2002). Fire does reduce the number of ticks initially (Hoch et al. 1972, Davidson et al. 1994, Cully 1999) due to direct killing and reductions in leaf litter and herbaceous cover (Hoch et al. 1972). The leaf litter hypothesis is supported by this study with a positive correlation between the mass of leaf litter and A. americanum populations. Semtner et al. (1971) found that populations of adult and nypmhal A. americanum were greatest near ecotones with nymphal populations higher in deeper leaf litter presumably because it provides better overwintering habitats. A larger A. americanum population in years 2 and 5 post-burn is likely due to an increase in litter mass and O. virginianus grazing after prescribed burning (Leslie et al. 1996, Main and Richardson 2002, Allan 2009). On the Talladega National Forest, fire increased cover of grasses and forbs (Table 4), and fire has been shown to increase the nutritional content and palatability of forage (Masters et al. 1996, Schindler et al. 2004). Thus, annual burns may reduce tick populations, while biennial burns permit tick populations to increase to levels exceeding preburned areas (Davidson et al. 1994) due to increases in leaf litter, percent cover of grass, and O. virginianus grazing. Increased levels of deer activity could reintroduce of ticks to the burned areas (Allan 2009). Prescribed fire, although useful in many aspects of ecosystem management, may increase localized populations of A. americanum. In this study, sites with high tick populations had an understory (grass) that provided food for mammals and an overstory that provided cover. In the Talladega National Forest, 5 year sites had a grass component in the understory along with the highest percent cover of vines and seedlings (Table 4), thus it provides the food needed by Odocoileus virginianus leading to high Amblyomma americanum populations (Table 2). In WUI sites, O. virginianus likely uses forested patches for cover during the day, feeds in grassy areas and lawns, and receives protection from predators due to the presence of humans (Swihart et al. 1995). The result can be a high tick population within close proximity to human habitations. The lower A. americanum populations in 15-year sites could be a function of lower percent cover of grass and forbs (Table 4), thus reducing food available for O. virginianus and other hosts. Unmanaged sites were in an unbroken forest with few open grassy areas, thus O. virginianus populations are likely low (Swihart et al. 1995). The open physiognomy of campus sites offers little cover for O. virginianus and the sites were not adjacent to open grassy areas for browsing. Thus, campus sites do not provide optimum habitat requirements for O. virginianus. Canopy closure percentage and soil moisture were not shown to be strongly correlated to Amblyomma americanum populations (Table 5). Canopy closure is likely to increase relative humidity and soil moisture in forested areas, thus creating a more favorable tick habitat. However, A. americanum is less sensitive to low humidity and moisture levels (Adler et al. 1992, Schulze et al. 2002). Adult A. americanum have been found to be more common in thinner leaf litter (Semtner et al. 1971, Schulze et al. 2002) and appear to be tolerant of lower humidity (Semtner et al. 1971). Schulze and Jordan (2005) found that A. americanum could thrive in numerous habitats and in warmer conditions than I. scapularis. The strong positive correlation with leaf litter mass and percent cover of grass and negative correlation with pine sapling density indicates that an open midstory with a high cover of grass and litter mass is a more suitable habitat for A. americanum. The litter likely provides a site for egg laying and development while the grass provides a site for questing. Tick larvae populations are impacted more by soil moisture than adult and nymphal populations because available moisture is a major factor in egg development (Lancaster 1957, Sonenshine and Tigner 1969, Sauer and Hair 1971). Only adult and nymphal tick populations were studied during this experiment, which may (at least partially) explain the lack of significance found between soil moisture and tick populations. This research suggests that some logical assumptions concerning Amblyomma americanum populations could be misleading. Prescribed fire may not reduce tick populations and may lead to an increase, while soil moisture and canopy closure do not strongly influence populations due to A. americanum's tolerance of harsher environments. The amount of leaf litter and percent grass cover are better predictors of A. americanum populations. The large A. americanum populations found at the WUI indicates that people building homes in suburban areas, especially when the area is adjacent or connected to areas of contiguous forests, may have a greater chance of encountering ticks and tick-borne diseases. Further research into the relationship between landscape scale habitat structure needs to be conducted in WUI areas to quantify the influence of fragmented habitats on tick populations. This research was supported by Gary Mullen, Auburn University, Talladega National Forest, and Jacksonville State University.