Plethodon cinereus (Eastern Red-backed Salamander) Not
Affected by Long-term Exposure to Soil Liming
Alexander C. Cameron, Cari-Ann M. Hickerson, and Carl D. Anthony
Northeastern Naturalist, Volume 23, Issue 1 (2016): 88–99
Full-text pdf (Accessible only to subscribers. To subscribe click here.)
Access Journal Content
Open access browsing of table of contents and abstract pages. Full text pdfs available for download for subscribers.
Current Issue: Vol. 30 (3)
Check out NENA's latest Monograph:
Monograph 22
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. Two anonymous
reviewers provided helpful comments on an earlier version of this manuscript. We
appreciate N. Spies, A. Murray, and I. Reider for their help in the field. Finally, we thank
the John Carroll Biology Department for the use of equipment. Field-work was approved
by JCU IACUC protocol #1302.
Literature Cited
Anthony C.D., and R.A. Pfingsten. 2013. Eastern Red-Backed Salamander, Plethodon cinereus.
Pp. 335–360, In R.A. Pfingsten, J.G. Davis, T.O. Matson, G. Lipps Jr., D. Wynn,
and B.J. Armitage (Eds.). Amphibians of Ohio. Vol. 17. No 1. Ohio Biological Survey
Bulletin New Series, Columbus, OH. 899 pp.
Anthony, C.D., M.D. Venesky, and C.M. Hickerson. 2008. Ecological separation in a polymorphic
terrestrial salamander. Journal of Animal Ecology 77:646–653.
Battles, J.J., T.J. Fahey, C.T. Driscoll Jr., J.D. Blum, and C.E. Johnson. 2014. Restoring
soil calcium reverses forest decline. Environmental Science and Technology Letters
1:15–19.
Bernard, M.J., M.A. Neatrour, and T.S. McCay. 2009. Influence of soil buffering-capacity
on earthworm growth, survival, and community composition in the Western Adirondacks
and Central New York. Northeastern Naturalist 16:269–284.
Best, M.L., and H.H. Welsh Jr. 2014. The trophic role of a forest salamander: Impacts on
invertebrates, leaf-litter retention, and the humification process. Ecosphere 5:art16 doi.
org/10.1890/ES13-00302.1.
Burton, T.M., and G.E. Likens. 1975. Salamander populations and biomass in the Hubbard
Brook Experimental Forest, New Hampshire. Copeia 1075:541–546.
Chagnon, M., D. Paré, C. Hébert, and C. Camiré. 2001. Effects of experimental liming on
collembolan communities and soil microbial biomass in a southern Quebec Sugar Maple
(Acer saccharum Marsh.) stand. Applied Soil Ecology 17:81–90.
Chen, D., L. Zhichun, X. Bai, J.B. Grace, and Y. Bai. 2013. Evidence that acidificationinduced
declines in plant diversity and productivity are mediated by changes in belowground
communities and soil properties in a semi-arid steppe. Journal of Ecology
101:1322–1334.
Cummins, C.P. 1986. Effects of aluminum and low pH on growth and development in Rana
temporaria tadpoles. Oecologia 69:248–252.
Driscoll, C.T., C.P. Cirmo, T.J. Fahey, V.L. Blette, P.A. Bukaveckas, D.A. Burns, C.P.
Gubala, D.J. Leopold, R.M. Newton, D.J. Raynal, C.L. Schofield, J.B. Yavitt, and D.B.
Porcella. 1996. The experimental watershed-liming study: Comparison of lake and watershed
neutralization strategies. Biogeochemistry 32:143–174.
Northeastern Naturalist
96
A.C. Cameron C.-A. M. Hickerson, and C.D. Anthony
2016 Vol. 23, No. 1
Driscoll, C.T., G.B. Lawerence, A.J. Bulger, T.J. Butler, C.S. Cronan, C. Eager, K.F. Lambert,
G.E. Likens, J.L. Stoddard, and K.C. Weathers. 2001. Acidic deposition in the
Northeastern United States: Sources and inputs, ecosystem effects, and management
strategies. BioScience 51:180–198.
Duarte, N., L.H. Pardo, and M.J. Robin-Abbott. 2013. Susceptibility of forests in the
northeastern USA to nitrogen and sulfur deposition: Critical-load exceedance and forest
health. Water, Air, and Soil Pollution 224:1–21.
Fisk, M.C., W.R. Kessler, A. Goodale, T.J. Fahey, P.M. Groffman, and C.T. Driscoll. 2006.
Landscape variation in microarthropod response to calcium addition in a northern hardwood
forest ecosystem. Pedobiologica 50:69–78.
Frisbie, M.P., and R.L. Wyman. 1991. The effects of soil pH on sodium balance in the Redbacked
Salamander, Plethodon cinereus, and three other terrestrial salamanders. Physiological
Zoology 64:1050–1068.
Frisbie, M.P., and R.L. Wyman. 1992. The effect of soil chemistry on sodium balance in
the Red-backed Salamander: A comparison of two forest types. Journal of Herpetology
26:434–442.
Gosner, K.L., and I.H. Black. 1957. The effects of acidity on the development and hatching
of New Jersey Frogs. Ecology 38:256–262.
Greller, A.M., D.C. Locke, V. Kilanowski, and G.E. Lotowycz. 1990. Changes in vegetation
composition and soil acidity between 1922 and 1985 at a site on the North Shore of Long
Island, New York. Bulletin of the Torrey Botanical Club 117:450–458.
Hägvar, S., and T. Amundsen. 1981. Effects of liming and artificial acid rain on the mite
(Acari) fauna in coniferous forest. Oikos 37:7–20.
Hairston, N.G. 1987. Community Ecology and Salamander Guilds. Cambridge University
Press, Cambridge, MA. 240 pp.
Hamburg, S.P., R.D. Yanai, M.A. Arthur, J.D. Blum, and T.G. Siccama. 2003. Biotic control
of calcium cycling in northern hardwood forests: Acid rain and aging forests. Ecosystems
6:399–406.
Hames, R.S., K.V. Rosenburg, J.D. Lowe, S.E. Barker, and A.A. Dhondt. 2002. Adverse effects
of acid rain on the distribution of the Wood Thrush Hylocichla mustelina in North
America. Proceedings of the National Academy of Sciences 99:11,235–11,240.
Hickerson, C.M., C.D. Anthony, and B.M. Walton. 2012. Interactions among forest-floor
guild members in structurally simple microhabitats. American Midland Naturalist
168:30–42.
Hocking, D.J., and K.J. Babbitt. 2014. Effects of Red-backed Salamanders on ecosystem
functions. PloS ONE 9: e86854.
Homyack, J.A., C.A. Haas, and W.A. Hopkins. 2011. Energetics of surface-activity terrestrial
salamanders in experimentally harvested forest. Journal of Wildlife Management
75:1267–1278.
Hotopp, K.P. 2002. Land snails and soil calcium in central Appalachian Mountain Forest.
Southeastern Naturalist 1:27–44.
Ivanov, K., O.M. Lockhart, J. Keiper, and B.M. Walton. 2011. Status of the exotic ant, Nylanderia
flavipes (Hymenoptera: Formicidae), in northeastern Ohio. Biological Invasions
13:1945–1950.
Kluber, A.L., S. Carrino-Kyker, K. Coyle, J. DeForest, C. Hewins, A. Shaw, K. Smemo, and
D. Burke. 2012. Mycorrhizal response to experimental pH and P manipulation in acidic
hardwood forests. PLoS ONE 11: e48946.
Northeastern Naturalist Vol. 23, No. 1
A.C. Cameron C.-A. M. Hickerson, and C.D. Anthony
2016
97
Kuperman, R.G. 1996. Relationships between soil properties and community structure of
soil macroinvertebrates in oak–hickory forests along an acidic deposition gradient. Applied
Soil Ecology 4:125–137.
Kuperman, R.G., M.B. Potapov, and E.A. Sinitzina. 2002. Precipitation and pollution interaction
effect on the abundance of collembola in hardwood forests in the lower midwestern
United States. European Journal of Soil Biology 38:277–280.
Likens, G E., C.T. Driscoll, and D.C. Buso. 1996. Long-term effects of acid rain: Response
and recovery of a forest ecosystem. Science 272:244–246.
Long, R.P., S.B. Horsley, and P.R. Lilja. 1997. Impact of forest liming on growth and crown
vigor of Sugar Maple and associated hardwoods. Canadian Journal of Forest Research
27:1560–1573.
Long, R.P., S.B. Horsley, and T.J. Hall. 2011. Long-term impact of liming on growth and
vigor of northern hardwoods. Canadian Journal of Forest Research 41:1295–1307.
Maerz, J.C., J.M. Karuzas, D.M. Madison, and B. Blossey. 2005. Introduced invertebrates
are important prey for a generalist predator. Diversity and Distributions 11:83–90.
Maerz, J.C., E.M. Myers, and D.C. Adams. 2006. Trophic polymorphism in a terrestrial
salamander. Evolutionary Ecology Research 8:23–25.
Maerz, J.C., V.A. Nuzzo, and B. Blossey. 2009. Declines in woodland-salamander abundance
associated with non-native earthworm and plant invasions. Conservation Biology
23:975–981.
McCay, T.S., C.L. Cardelús, and M.A. Neatour. 2013. Rate of litter decay and litter macroinvertebrates
in limed and unlimed forests of the Adirondack Mountains, USA. Forest
Ecology and Management 304:254–260.
Moore, J-D. 2014. Short-term effect of forest liming on Eastern Red-backed Salamander
(Plethodon cinereus). Forest Ecology Management 318:270–273.
Moore, J-D., and R. Ouimet. 2010. Effects of two Ca-fertilizer types on Sugar Maple vitality.
Canadian Journal of Forest Research 40:1985–1992.
Moore, J-D., and R.L. Wyman. 2010. Eastern Red-backed Salamander (Plethodon cinereus)
in a highly acid forest soil. American Midland Naturalist 163:95–105.
Moore, J.D., R. Ouimet, C. Camiré, and D. Houle. 2002. Effects of two silvicultural practices
on soil fauna abundance in a northern hardwood forest, Québec, Canada. Canadian
Journal of Soil Science 82:105–113.
Moore, J-D., R. Ouimet, and L. Duchesne. 2012. Soil and Sugar Maple response 15 years
after dolomitic lime application. Forest Ecology and Management 281:130–139.
Moore, J-D., R. Ouimet, and P. Bohlen. 2013. Effects of liming on survival and reproduction
of two potentially invasive earthworm species in a northern forest podzol. Soil
Biology and Biochemistry 64:174–180.
Moore, J-D., R. Ouimet, R.P. Long, and P.A. Bukaveckas. 2014. Ecological benefits and
risks arising from liming Sugar Maple-dominated forests in northeastern North America.
Environmental Reviews 23:66–77.
Ormerod, S.J., and S.D. Rundle. 1998. Effects of experimental acidification and liming on
terrestrial invertebrates: Implications for calcium availability to vertebrates. Environmental
Pollution 103:183–191.
Pabian, S.E., and M.C. Brittingham. 2011. Soil-calcium availability limits forest songbird
productivity and density. The Auk 128:441–447.
Pabian, S.E., and M.C. Brittingham. 2012. Soil calcium and forest birds: Indirect links between
nutrient availability and community composition. Ecosystems 15:748–760.
Northeastern Naturalist
98
A.C. Cameron C.-A. M. Hickerson, and C.D. Anthony
2016 Vol. 23, No. 1
Pabian, S.E., N.M. Ermer, W.M. Tzilkowski, and M.C. Brittingham. 2012. Effects of liming
on forage availability and nutrient content in a forest impacted by acid rain. PLoS ONE
7: e39755. doi:10.1371/journal.pone.0039755.
Pauley, T.K., M.B. Watson, J.N. Kochenderfer, and M. Little. 2006. Response of salamanders
to experimental acidification treatments. Pp. 189–206, In M.B. Adams, D.R.
DeWalle, and J.L. Horn (Eds). Fernow Watershed Acidification Study. Vol 11. Environmental
Pollution Series, 279 pp.
Petranka, J.W. 1998. Salamanders of the United States and Canada. Smithsonian Institute
Press, Washington, DC. 592 pp.
Pierce, A.B. 1985. Acid tolerance in amphibians. Bioscience 35:239–243.
Pough, F.H. 1976. Acid precipitation and embryonic mortality of Spotted Salamander, Ambystoma
maculatum. Science 192:68–72.
Pough, F.H., and R.E. Wilson. 1977. Acid precipitation and reproductive success of Ambystoma
salamanders. Water Air and Soil Pollution 7:531–544.
Pough, F.H., M.E. Smith, H.D. Rhodes, and A. Collazo. 1987. The abundance of salamanders
in forest stands with different histories of disturbance. Journal of Forest Ecology
and Management 20:1–9.
Reuss, J.O., and D.W. Johnson. 1985. Implications of Ca–Al exchange system for the effect
of acid precipitation on soils. Journal of Environmental Quality 12:591–595.
Rusek, J., and V.G. Marshall. 2000. Impacts of airborne pollutants on soil fauna. Annual
Review of Ecology and Systematics 31:395–423.
Scheuhammer, A.M. 1991. Effects of acidification on the availability of toxic metals and
calcium to wild birds and mammals. Environmental Pollution 7:329–375.
Schulte-Hostedde, A.I., B. Zinner, J.S. Millar, and G.J. Hickling. 2005. Restitution of masssize
residuals: Validating body-condition indices. Ecology 86:155–163.
Skeldon, M.A., M.A. Vadeboncoeur, S.P. Hamburg, and J.D. Blum. 2007. Terrestrial gastropod
responses to an ecosystem-level calcium manipulation in a northern hardwood
forest. Canadian Journal of Zoology 85:994–1007.
Sullivan, T.J., G.B. Lawrence, S.W. Bailey, T.C. McDonnell, C.M. Beirer, K.C. Weathers,
G.T. McPherson, and D.A. Bishop. 2013. Effects of acidic deposition and soil acidification
on Sugar Maple trees in the Adirondack Mountains, New York. Environmental
Science and Technology 47:12,687–12,694.
Taub, F.B. 1961. The distribution of Red-backed Salamanders, Plethodon cinereus, within
the soil. Ecology 42:681–698.
Templer, P.H., R.W. Pinder, and C.L. Goodale. 2012. Effects of nitrogen deposition on
greenhouse-gas fluxes for forests and grasslands of North America. Frontiers in Ecology
and the Environment 10:547–553.
Test, F.H., and B.A. Bingham.1948. Census of a population of the Red-backed Salamander
(Plethodon cinereus). American Midland Naturalist 39:362–372.
Tome, M.A., and F.H. Pough. 1982. Responses of amphibians to acid precipitation. Pp.
245–254, In T.A. Haines, and R.E. Johnson (Eds.). Acid Rain/Fisheries. American Fisheries
Society, Bethesda, MD. 357 pp.
Walton, B.M. 2013. Top-down regulation of litter invertebrates by a terrestrial salamander.
Herpetologica 69:127–146.
Wyman, R.L., and D.S. Hawksley-Lescault. 1987. Soil acidity affects distribution, behavior,
and physiology of the salamander Plethodon cinereus. Ecology 68:1819–1827.
Northeastern Naturalist Vol. 23, No. 1
A.C. Cameron C.-A. M. Hickerson, and C.D. Anthony
2016
99
Wyman, R.L., and J. Jancola. 1992. Degree and scale of terrestrial acidification and amphibian-
community structure. Journal of Herpetology 26:392–401.
Ziemba, J.L., A.C. Cameron, K. Peterson, C.M. Hickerson, and C.D. Anthony. 2015. The
presence of an invasive Asian earthworm (Amynthas spp.) alters terrestrial salamander
(Plethodon cinereus) microhabitat use in laboratory microcosms. Journal of Canadian
Zoology 10.1139/cjz-2015-0056.