Northeastern Naturalist 88 A.C. Cameron C.-A. M. Hickerson, and C.D. Anthony 22001166 NORTHEASTERN NATURALIST V2o3l.( 12)3:,8 N8–o9. 91 Plethodon cinereus (Eastern Red-backed Salamander) Not Affected by Long-term Exposure to Soil Liming Alexander C. Cameron1,*, Cari-Ann M. Hickerson1, and Carl D. Anthony1 Abstract - The recovery of ecosystems affected by anthropogenic acidification is often a slow process, and one that is not always achievable through natural means. Application of carbonate materials to forest soils is being used more frequently to aid in the recovery of acidified ecosystems. However, few studies have addressed how the application of carbonate materials affects amphibians. We sampled field sites undergoing long-term application of high-calcium lime to investigate the effects of increases in soil pH on body condition and population demography of Plethodon cinereus (Eastern Red-backed Salamander). We found no effect of soil liming on body condition, population demographics, or density of surfaceactive Eastern Red-backed Salamanders. Our results are consistent with previous studies regarding the response of this species to soil liming, but unique in that they arise from an investigation of the long-term effects of liming exposure on density and demography in a wild population of Eastern Red-backed Salamander. Introduction Anthropogenic activities, predominantly the combustion of fossil fuels, have increased the deposition of atmospheric sulfur dioxide and nitrogen oxides (Driscoll et al. 2001, Duarte et al. 2013, Moore et al. 2014) resulting in widespread environmental degradation. Acid deposition has been linked to the acidification of both forested and aquatic ecosystems, the exportation of nutrient cations, and the mobilization of aluminum in soils (Duarte et al. 2013, Reuss and Johnson 1985). The environmental consequences associated with acid deposition have been shown to negatively affect a disparate variety of taxa including: soil biota (Hägvar and Amundsen 1981, Kuperman et al. 2002), herbaceous plants (Chen et al. 2013, Greller et al. 1990), forest-tree species (Battles et al. 2014, Sullivan et al. 2013), birds (Hames et al. 2002; Pabian and Brittingham 2011, 2012), and mammals (Pabian et al. 2012, Scheuhammer 1991). Although various legislative measures have drastically reduced emission levels of sulfur and nitrogen-oxides, acidification of ecosystems via atmospheric nitrogen deposition, primarily NH3, remains an ecological concern (Moore et al. 2014, Templer et al. 2012). Calcium is an essential plant nutrient (Driscoll et al. 2001, Hamburg et al. 2003, Hames et al. 2002, Likens et al. 1996) and its depletion from soils is common in ecosystems affected by anthropogenic acidification. The application of lime to forest soils and aquatic habitats is a mitigation technique commonly used to aid in the recovery of acidified systems (Driscoll et al. 1996). Acidified forest ecosystems have shown positive direct and indirect effects from this mitigation approach, and 1Department of Biology, John Carroll University, University Heights, OH 44118. *Corresponding author - acameron15@jcu.edu. Manuscript Editor: Joseph Milanovich Northeastern Naturalist Vol. 23, No. 1 A.C. Cameron C.-A. M. Hickerson, and C.D. Anthony 2016 89 these effects have been documented in numerous taxa, e.g., Acer saccharum Marsh. (Sugar Maple; Long et al. 1997, 2011; Moore and Ouimet 2010; Moore et al. 2012), gastropods (Hotopp 2002, Skeldon et al. 2007), Seiurus aurocaillus L. (Ovenbird; Pabian and Brittingham 2011), and Oedocoileus virginicus (Zimmermann) (Whitetailed Deer; Pabian et al. 2012). Amphibians are particularly sensitive to acidification of the environment due to several aspects of their life history (Pierce 1985). There are multiple lines of evidence that demonstrate the negative effects of acidic environments on amphibians during the aquatic portion of development (Cummins 1986, Gosner and Black 1957, Pough 1976, Pough and Wilson 1977, Tome and Pough 1982). However, the majority of amphibian species inhabit terrestrial environments for the remainder of the life cycle, and direct-developing species rely solely on terrestrial environments during all stages of life (Petranka 1998). Highly acidic substrates of terrestrial environments have been demonstrated to disrupt the sodium balance and osmoregulation in terrestrial salamanders (Frisbie and Wyman 1991, 1992; Wyman and Jancola 1992), which experience physiological effects comparable to those of amphibians in acidic aquatic environments. However, sensitivity to acidic conditions varies among amphibian species, with some taxa having a higher tolerance to acidity. An example of one such species is Plethodon cinereus (Green) (Eastern Red-backed Salamander), for which there are multiple lines of field-based evidence that suggest this species is able to withstand acidic microhabitats. Eastern Red-backed Salamander abundance was found to be highest at a pH of 3.9 across 17 different field sites in south-central New York, and the species occurred infrequently on soils of a higher pH (Wyman and Jancola 1992). Additionally, a 5-y sampling period within a hardwood forest in Québec revealed that 83% of adult Eastern Red-backed Salamanders captured were found under cover objects on soil with a pH ≤ 3.8 (Moore and Wyman 2010). Furthermore, the salamanders found in that study were among the largest documented for this species in the scientific literature (Moore and Wyman 2010), suggesting these populations were in good health. Wyman and Hawksley-Lescault (1987) reported 50% fewer quadrats containing salamanders when soil pH was high (4.3) compared to those with lower soil pH (3.9). Despite field evidence suggesting that Eastern Red-backed Salamanders are tolerant of or even prefer acidic microhabitats, only 1 previous study has investigated the direct effects of elevating soil pH through the application of lime. Recently, Moore (2014) conducted a 5-month microcosm study in which he found no direct or short-term effect of the application of lime on the mass of Eastern Red-backed Salamanders. However, the long-term and indirect effects of soil liming remain unclear. One long-term effect that has the potential to benefit this species is the increased production of deciduous tree canopies, which ultimately contribute to a thick layer of detritus to the forest floor. Eastern Red-backed Salamanders forage in leaf litter (Burton and Likens 1975, Taub 1961), and an increase in litter thickness may translate to an increase in available foraging time by reducing the risk of desiccation. Conversely, there are some potential long-term effects that may negatively influence Eastern Red-backed Salamanders. There is evidence Northeastern Naturalist 90 A.C. Cameron C.-A. M. Hickerson, and C.D. Anthony 2016 Vol. 23, No. 1 to suggest that soil liming may facilitate earthworm invasion (Bernard et al. 2009, Moore et al. 2013), which has been shown to decrease Eastern Red-backed Salamander abundance (Maerz et al. 2009) and interfere with cover-object use by salamanders (Ziemba et al. 2015). Additionally, changes in soil pH can alter the community composition of soil microinvertebrates (Kuperman 1996, Rusek and Marshall 2000), which may result in changes in prey availability and foraging success for Eastern Red-backed Salamanders. Eastern Red-backed Salamanders are among the most abundant vertebrate species in eastern North America (Burton and Likens 1975, Test and Bingham 1948). It is hypothesized that these salamanders are strong regulators in the detrital food web due to the annual biomass they produce (Hairston 1987, Hickerson et al. 2012, Pough et al. 1987, Walton 2013). Thus, factors that have the potential to affect their distribution and abundance are of concern to ecologists. The objectives of this field study were to investigate whether the increase in soil pH through the long-term application of lime affects body condition, population demographics, and density of Eastern Red-backed Salamanders. Methods Research currently being conducted at the Holden Arboretum, Lake County, OH, offers a unique opportunity to investigate the effect of soil liming on Eastern Red-backed Salamanders in the field. Researchers at Holden Arboretum are investigating how mixed deciduous forests respond to long-term pH manipulation. Lime-treated plots were established in August of 2009, so animals occupying these plots and examined in the current study had been exposed to the treatment application for 5 consecutive years. A shift in pH had occurred within the top 7 cm of the soil (Kluber et al. 2012), which is critical microhabitat for Eastern Red-backed Salamanders and their litter- and soil-dwelling invertebrate prey (Petranka 1998). We conducted our surveys in 2 forest stands (Pierson Creek: 41°36'31.68''N, 81°18'45.67''W; Schoop Forest: 41°36'41.1599''N, 81°19'12.6502''W) at the Holden Arboretum. Within each forest, we surveyed 3 control and 3 limed plots (total = 12 plots). Plots measured 800 m2 and were separated by at least 20 m. The 2 forest stands were separated by 1.14 km and were comprised of ~80-y-old trees dominated by Quercus spp. (oak), Acer spp. (maple), and Fagus grandifolia Ehrh. (American Beech), with small amounts of old growth present in Pierson Creek. High-calcium lime was applied to all plots in fall of 2009, 2010, and 2012. Since 2012, lime has been applied on an as-needed basis, and as of October 2014, all treatment plots were within the pH range of 5.8–6.2. The pH of all control plots ranged from 4.1–4.6. We sampled salamanders from 17 September to 30 October 2014 with 2 visits to each plot. Mean temperature at the plots ranged from 15.3 ºC to 16.2 ºC during sampling round 1, and from 10.9 ºC to 15.4 ºC during the second sampling round. These temperatures are within the range of temperatures at which Eastern Red-backed Salamanders are active at the soil surface (Taub 1961). We avoided sampling on days that were outside the optimal temperature range for this species. Northeastern Naturalist Vol. 23, No. 1 A.C. Cameron C.-A. M. Hickerson, and C.D. Anthony 2016 91 We sampled an equal number of control and experimental plots during each visit between the hours of 8:00 and 16:00. The first sampling round took place from 17 to 25 September, and the search effort was restricted to 50 naturally occurring cover objects (rocks and logs) per plot (600 total). We clipped 2 toes on the right hind foot of each salamander to avoid resampling in subsequent searches. The second round of sampling took place from 2 to 30 October. During the second round, we restricted our search time to 1 h per plot, but we searched a variety of microhabitats including the leaf litter surrounding cover objects. Typically, A.C. Cameron conducted our time-constrained habitat searches. In cases where up to 3 searchers participated, we corrected our abundance estimates by dividing the total number of salamanders found by the number of searchers present. The number of cover objects distributed within plots appeared to be fairly homogenous. We measured and recorded mass (g) and snout–vent length (SVL; mm) of each Eastern Red-backed Salamander encountered to estimate body condition. We also recorded age class to compare demographic patterns between plot types. We categorized individuals that were >32 mm SVL as adults, less than 22 mm SVL as juveniles, and 22–32 mm SVL as sub-adults (Anthony and Pfingsten 2013, Anthony et al. 2008). We calculated the average pH per plot from combined and homogenized 5 cm x 5 cm soil-core sub-samples (n = 6; D. Burke, Holden Arboretum, Kirtland, OH, pers. comm.). We used an independent-samples t-test to compare the soil pH of control plots and plots that had been treated with lime. We employed a 2-way analysis of covariance (ANCOVA) with a normal probability distribution to examine the effects of treatment (control vs. limed) and forest stand (Schoop vs. Pierson Creek) on body condition. We designated mass (g) as our dependent variable while controlling for body size by designating SVL as a covariate. We excluded 41 gravid females and 7 juveniles from our analysis to avoid artificial elevation of body condition (Homyack et al. 201 1). To visualize differences in the body condition of salamanders in control plots compared to plots with elevated pH in each forest stand, we calculated a body-condition index for each salamander using the residuals from an ordinary least-squares regression of SVL and body mass (Anthony et al. 2008, Schulte-Hostedde et al. 2005). Positive residual scores indicate good condition, while individuals with a negative residual value had poor body condition. We conducted a 2-way analysis of variance (ANOVA) to compare the number of surface-active individuals in each age class between plot type and forest stands. Treatment (control vs. limed) and forest stand (Schoop vs. Pierson Creek) were fixed factors in our analysis, and the dependent variables were number of individuals in each age class (adults, sub-adults, and juveniles) per plot. We analyzed each sampling round separately to avoid effects of temporal variation in surface activity (Anthony and Pfingsten 2013). Subsequently, we used a second 2-way ANOVA to explore the effects of treatment and forest stand on total density of surface-active Eastern Red-backed Salamanders (age classes combined). In this analysis, the dependent variable was number of individual salamanders per plot. All statistical analyses were performed in SPSS for Windows v22. Northeastern Naturalist 92 A.C. Cameron C.-A. M. Hickerson, and C.D. Anthony 2016 Vol. 23, No. 1 Results The addition of lime was effective in raising soil pH in treatment plots in both Pierson Creek (t = 11.618, P < 0.0005) and Schoop Forest (t = 11.779, P < 0.0005) (Fig. 1). We recorded a total of 183 Eastern Red-backed Salamanders throughout the sampling period. We estimated body condition for 134 adult individuals. We excluded 1 control plot located within Schoop Forest because we found only 1 individual in the plot throughout the duration of sampling. Although we found no significant effect of soil pH on salamander body condition (F1,176 = 0.854, P = 0.357; Fig. 1), we did find a significant effect of forest stand (F1,176 = 23.73, P < 0.0001; Fig. 1). When controlled for body length, salamanders from Schoop Forest were heavier and had better body condition than those from Pierson Creek. Additionally, we found no interaction between treatment and forest stand (F1,176 = 0.035, P = 0.852; Fig. 1). The demographic profile of the salamander population in control and limetreated plots did not differ for any age class or between forests (Tables 1, 2). We found no effect of liming on the 3 age groups; thus, we opted to combine them to Figure 1. Mean (± SE) residuals from an ordinary least-squares regression of mass and SVL (body condition) for salamanders in each plot and their corresponding pH value. Filled points represent control plots and open points represent lime-treated plots. Letter/ number codes represent plot IDs (PC = Pierson Creek, SF = Schoop Forest). One control plot (SC05) was excluded due to small sample size (1 individual). Positive values indicate better body condition than negative values. We did not detect a significant effect of soil pH on body condition. Northeastern Naturalist Vol. 23, No. 1 A.C. Cameron C.-A. M. Hickerson, and C.D. Anthony 2016 93 examine the effects of liming on overall surface-active salamander density. This analysis revealed no differences in the number of salamanders captured in the first or second round of sampling between control and treatment plots (round 1 = F1,8 = 0.004, P = 0.950; round 2 = F1,7 = 0.285, P = 0.610) or between forest stands (round 1 = F1,8 = 0.103, P = 0.765; round 2 = F1,7 = 0.426, P = 0.535). Discussion We detected no difference in body condition, demography, or total density of Eastern Red-backed Salamanders between plots with acidic soil pH and those with experimentally elevated pH through the application of lime. Given the widespread geographic distribution of Eastern Red-backed Salamanders combined with their generalist nature, relatively small changes in soil pH may not have a strong effect on the fine-scale distribution of this species. For example, in an acidification experiment in Virginia, Pauley et al. (2006) observed no difference in the number of surface-active individuals or in SVL of Eastern Red-backed Salamanders in experimentally acidified watersheds (pH = 4.26) compared to control watersheds (pH = 4.44 and 4.68). In our study, soil pH was increased, rather than decreased, and the magnitude of difference between control and limed plots was greater. Despite this difference, we were unable to detect an effect of pH on salamander condition or surface activity. This result further suggests that Eastern Red-backed Salamanders are tolerant to a wide range of soil pH. Table 2. Results from our ANOVA revealed no significant effect of treatment or forest stand on Plethodon cinereus (Eastern Red-backed salamander) densities from 3 age classes. Mean number of adults, sub-adults, and juveniles (± SD) found within each plot type during the second round of sampling in which surveys were restricted to 1 h of search time. PC = Pierson Creek, SF = Schoop Forest. Forest stand Treatment Adults Subadults Juveniles Fixed factors F3,5 P PC Control 7.00 (6.25) 3.33 (1.53) 0 Lime 6.33 (3.21) 4.33 (4.16) 0.67 (1.15) Treatment 0.231 0.871 Forest Stand 1.113 0.426 SF Control 9.50 (4.95) 0.50 (0.71) 1.00 (1.41) Interaction 1.685 0.284 Lime 6.00 (4.58) 1.00 (1.00) 0 Table 1. Results from our ANOVA revealed no significant effect of treatment or forest stand on Plethodon cinereus (Eastern Red-backed salamander) densities from 3 age classes. Mean number of adults, sub-adults, and juveniles (± SD) found within each plot type during the first round of sampling in which surveys were restricted to 50 cover objects per plot. PC = Pierson Creek, SF = Schoop Forest. Forest stand Treatment Adults Subadults Juveniles Fixed factors F3,5 P PC Control 3.67 (1.53) 4.00 (2.00) 0.33 (0.58) Lime 3.00 (1.00) 2.33 (1.15) 0 Treatment 0.645 0.614 Forest Stand 0.072 0.973 SF Control 1.67 (1.53) 2.67 (1.53) 0.33 (0.58) Interaction 0.238 0.867 Lime 4.33 (5.77) 2.67 (2.52) 0 Northeastern Naturalist 94 A.C. Cameron C.-A. M. Hickerson, and C.D. Anthony 2016 Vol. 23, No. 1 Even though soil liming may not influence the distribution and abundance of Eastern Red-backed Salamanders directly, liming has the potential to affect their invertebrate prey. Eastern Red-backed Salamanders are generalist predators, but numerous studies have shown that mites (Subclass Acari), Collembola sp. (springtails), and ants make up the majority of prey (see citations in Anthony et al. 2008). The salamanders also eat larger prey such as centipedes, spiders, and beetles, but these groups make up a relatively small proportion of the diet (Hickerson et al. 2012). Soil liming has been shown to affect leaf-litter invertebrates. For example, soil liming causes a shift in the vertical distribution of mites within the leaf litter (Hägvar and Amundsen 1981) as well as shifts in the dominance of certain functional groups of springtails (Chagnon et al. 2001). Moreover, Fisk et al. (2006) observed temporal differences in the response of springtail and mite communities to long-term lime application, and the overall result was a decrease in abundance of both groups. Liming of forest floors has also been observed to decrease the abundance of less-common prey items, such as spiders (McCay et al. 2013, Ormerod and Rundle 1998) and millipedes (McCay et al. 2013). Additionally, soil liming may also facilitate the invasion of acid-intolerant species, through the elimination of the habitat required by native acidophilic species (McCay et al. 2013). Thus, increasing soil pH through liming can have direct negative effects on arthropod abundance, distribution, and composition. As a result, we might expect that terrestrial salamanders would experience decreases in body condition and/or density due to shifts in diet associated with shifts in soil pH. Eastern Red-backed Salamanders are most abundant within the soil pH range of 3.7–3.9 (Moore and Wyman 2010), but it is unclear whether they prefer this pH range, are forced to occupy this niche due to competitive interactions with other salamanders, or whether their preferred prey are found in acidic soils. The euryphagic nature of Eastern Red-backed Salamanders, coupled with their ability to incorporate novel prey into their diet, may offer an explanation as to why changes in the abundance of preferred prey items may not significantly affect this salamander. For example, Eastern Red-backed Salamanders incorporate exotic prey into their diets when such prey are available (Ivanov et al. 2011, Maerz et al. 2005), and they exhibit flexibility in a diet based on habitat type and prey availability (Maerz et al. 2005, 2006). These attributes may shield Eastern Red-backed Salamanders from changes in invertebrate communities that are often associated with fluctuating soil pH, and may help to explain why we did not detect effects of liming on body condition or surface activity (Moore 2014). Ours is the first field study to examine the long-term, indirect effects of soil liming on a terrestrial plethodontid salamander. Plethodontid salamanders are widely regarded as important top-down regulators of terrestrial detrital food webs (Best and Welsh 2014, Walton 2013, but see Hocking and Babbitt 2014), and Eastern Red-backed Salamanders are used as indicators of overall forest quality (Moore and Wyman 2010, Moore et al. 2002). Although plethodontids make excellent guages of forest health, Eastern Red-backed Salamanders may not be an ideal indicator of high-quality forest because they appear to be less affected by conditions to Northeastern Naturalist Vol. 23, No. 1 A.C. Cameron C.-A. M. Hickerson, and C.D. Anthony 2016 95 which other plethodontids are sensitive (Anthony and Pfingsten 2013). The results of our study are congruent with previous research regarding soil liming and Eastern Red-backed Salamanders (Moore 2014), and suggest that forest liming may be an effective soil-recovery strategy. However, because less is known about the dietary and pH preferences of other common terrestrial salamander species, we should be cautious in applying these results to other taxa. Acknowledgments We are grateful to scientists at the Holden Arboretum for establishing field plots. We would especially like to thank D. Burke for allowing us access to the field sites. 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