Site by Bennett Web & Design Co.
2013 SOUTHEASTERN NATURALIST 12(2):339–352
Quantifiable Long-term Monitoring on Parks and Natur e
Sharon Becker1,*, Christopher Moorman1, Christopher DePerno1,
and Theodore Simons2
Abstract - Herpetofauna have declined globally, and monitoring is a useful approach to
document local and long-term changes. However, monitoring efforts often fail to account
for detectability or follow standardized protocols. We performed a case study at Hemlock
Bluffs Nature Preserve in Cary, NC to model occupancy of focal species and demonstrate
a replicable long-term protocol useful to parks and nature preserves. From March 2010 to
2011, we documented occupancy of Ambystoma opacum (Marbled Salamander), Plethodon
cinereus (Red-backed Salamander), Carphophis amoenus (Eastern Worm Snake),
and Diadophis punctatus (Ringneck Snake) at coverboard sites and estimated breeding
female Ambystoma maculatum (Spotted Salamander) abundance via dependent doubleobserver
egg-mass counts in ephemeral pools. Temperature influenced detection of both
Marbled and Red-backed Salamanders. Based on egg-mass data, we estimated Spotted
Salamander abundance to be between 21 and 44 breeding females. We detected 43 of 53
previously documented herpetofauna species. Our approach demonstrates a monitoring
protocol that accounts for factors that influence species detection and is replicable by
parks or nature preserves with limited resources.
Reptile and amphibian species have declined globally, with more species declining
than either birds or mammals (Gibbons et. al 2000, Gardner et al. 2007,
Heyer et al. 1994, Pechman et al. 1991, Wake 1991). Climate change, disease,
invasive species, and habitat loss and degradation contribute to declines (Alford
and Richards 1999, Gamble et al. 2009, Stuart et al. 2004). Additionally, reptiles
and amphibians are important bio-indicators of ecosystem health, so understanding
the drivers of population change is critical (Bury and Corn 1988, Dunson et
al. 1992, Gibbons et al. 2000, Hanlin et al. 2000, Wake 1991).
Documenting species distribution and abundance is essential to comprehending
changes in global biodiversity. Some reptiles and amphibians are wide
ranging and could serve as global indicators of biodiversity change; other species
are endemic to smaller areas and could indicate local conservation threats (Heyer
et al. 1994). However, knowledge of the distribution and status of most herpetofauna
species is lacking, even on public lands (Smith et al. 2006). Therefore,
long-term monitoring of local sites is particularly critical to describing largerscale
changes in biodiversity (Gooch et al. 2006).
Park and nature preserves need repeatable and affordable methods for monitoring
herpetofaunal populations to document long-term population trends and
1 Fisheries, Wildlife, and Conservation Biology Program, Turner House, Box 7646, North
Carolina State University, Raleigh, NC 27695. 2US Geological Survey, NC Cooperative
Fish and Wildlife Research Unit, David Clark Labs, Box 7617, North Carolina State
University, Raleigh, NC 27695. *Corresponding author - email@example.com.
340 Southeastern Naturalist Vol. 12, No. 2
make well-informed management decisions. Standardized monitoring is necessary
to assess changes in local species diversity and species-specific responses
to management (Yoccoz et. al 2001). Data from monitoring programs are critical
for making inferences about species occurrence, conservation status, and metapopulation
dynamics (Heyer et al. 1994, Nichols et al. 2007, Williams and Berkson
2004). Standardized sampling protocols that account for variations in detection
probability reduce biases associated with nondetection, and allow managers to
compare estimates of species distribution, abundance, and occurrence across space
and time (Heyer et al. 1994, Feest 2006). Nevertheless, inferences about system
dynamics often are derived from monitoring data that represent spatial and temporal
snapshots of species distribution. Additionally, perfect detection of species on
surveys is rare, so practitioners often are faced with the challenge of determining
whether the absence of a species represents a true absence or simply a case where
an observer failed to detect a species that actually occurred on a site. Occupancy
modeling accounts for the probability of imperfectly detecting a species during a
survey (MacKenzie 2005, MacKenzie et al. 2002). Multi-season occupancy modeling
is a modern technique that provides direct estimates of detection probability
through replicated presence-absence surveys at a series of sites, is often less labor
intensive than methods used to estimate abundance, and can provide useful information
on species distribution and abundance to parks and natural preserves with
limited resources (MacKenzie et al. 2006).
We used a 1-year monitoring study at Hemlock Bluffs Nature Preserve (HBNP),
Cary, NC to demonstrate this approach for other nature preserves, parks, and land
trusts that are interested in developing long-term monitoring programs. We monitored
the presence of herpetofauna within the preserve to develop a preliminary
inventory and standardized and replicable survey methods. Our study determined
baseline occupancy and detection probability estimates of Ambystoma opacum
Gravenhorst (Marbled Salamander), Plethodon cinereus Green (Red-backed
Salamander), Carphophis amoenus Say (Eastern Worm Snake), and Diadophis
punctatus L. (Ringneck Snake), which will provide the opportunity to model
long-term changes in species distribution on the property. Also, we estimated the
abundance of breeding female Ambystoma maculatum Shaw (Spotted Salamander)
using egg-mass counts, which can be used with other pool-breeding amphibians to
provide a useful index for modeling long-term changes in reproductive effort.
Hemlock Bluffs is a 64-ha nature preserve located in southwestern Cary,
NC. The property is co-owned by the State of North Carolina and the Town of
Cary and has high patron visitation (annual visitation estimate for 2010 was
100,000 patrons [J. Logan, Hemlock Bluffs Nature Preserve Customer Service
Representative, Cary, NC, pers. comm.]). Several boardwalks, overlooks, and
approximately 4.8 km of trails occur within the preserve. A natural area owned
by the State of North Carolina includes a system of north-facing bluffs featuring
a disjunct population of Tsuga canadensis Carr (Eastern Hemlock). This bluff
system is adjacent to Swift Creek, which runs through the preserve and along a
portion of the property boundary. Also, several small tributaries of Swift Creek
2013 S. Becker, C. Moorman, C. DePerno, and T. Simons 341
intersect the property. The bluffs create a division between upland ridges and flats
and the floodplain forest habitat, which is primarily at the east end of the preserve.
Upland areas are mainly a pine-hardwood mix. The floodplain forest lies in
the northeastern part of the property and contains several ephemeral pools, which
provide essential breeding areas for many amphibian species such as Marbled
Salamander, Spotted Salamander, Pseudacris feriarum Baird (Upland Chorus
Frog), and Pseudacris crucifer Wied-Neuwied (Spring Peeper).
Areas of urban development encompass 3 sides of the preserve, with a 4-lane
road on the southeastern boundary. The loss of forest cover adjacent to the preserve
has increased water discharge of Swift Creek (Fig. 1; USGS 2011), which
is a primary variable affecting transport of sediment and channel morphology in
alluvial streams (Doyle et al. 2005). The increase of water discharge could lead
to increased flooding, bank erosion, stream sedimentation, and overall changes
in hydrology of the floodplain forest, af fecting key amphibian breeding sites.
Historically, HBNP has not conducted standardized and quantifiable herpetofauna
monitoring, which has limited the ability of park staff to directly compare
results from species inventories conducted in the preserve. Preserve managers
recognized the need for a standardized monitoring program to track the response
of the herpetofaunal community to urban development and other long-term conservation
During fall 2009, we established coverboards (0.6-m x 0.6-m x 0.0127-m
untreated plywood boards) at 35 sites throughout HBNP, each site containing
one coverboard. Coverboard locations effectively sampled each major habitat
type, surrounded ephemeral pools, and avoided visibility from walking trails.
We were unable to establish coverboards randomly at HBNP because we were
concerned that patrons would venture off trails and disturb boards at visible
Figure 1. Annual water
discharge for Swift
Creek near Apex, NC
from 2004–2010. Water
volume in Swift
Creek has increased
342 Southeastern Naturalist Vol. 12, No. 2
locations (Fig. 2). We located coverboards at least 30 m apart, numbered each,
and recorded locations with a GPS. We checked all 35 coverboards during each
survey from March 2010 through March 2011. We checked coverboards every 2
weeks and recorded each species detected. We conducted 28 coverboard surveys
from 2010 through 2011 with 7 surveys in each of 4 sampling seasons. We designated
samplings seasons as spring (March–May 2010), summer (June–August
2010), fall (September–December 2010), and winter (January–March 2011).
We recorded the covariates ambient temperature, precipitation, and sampling
season that could influence herpetofauna detection and habitat type (upland or
bottomland habitat) which could influence occupancy. We recorded precipitation
as a categorical variable, denoting if a rain event occurred during each survey.
We measured ambient temperature at the beginning of each survey.
We conducted Spotted Salamander egg-mass surveys in 3 ephemeral pools
within HBNP. We used a dependent double-observer approach, where observer
1 pointed out and counted egg masses to observer 2, who then recorded the observations
and noted any egg masses missed by observer 1 (Grant et al. 2005).
Halfway through each survey at individual pools, observer 1 and 2 switched
responsibilities (Grant et al. 2005). We counted egg masses by viewing from the
shore, and the same observers conducted surveys on 2 occasions in each pool to
ensure the maximum number of egg masses was counted. We conducted surveys
during March, which is prime oviposition time for Spotted Salamanders (Egan
and Paton 2004). Spotted Salamander breeding females lay between 2 and 4 egg
Figure 2. Coverboard sites monitored at Hemlock Bluffs Nature Preserve, Cary, NC from
March 2010–March 2011.
2013 S. Becker, C. Moorman, C. DePerno, and T. Simons 343
masses each year (Petranka 1998); we used this range in egg masses per female
to estimate the number of breeding female salamanders in the 3 pools.
We used the program PRESENCE to estimate detection probabilities and site
occupancy for Marbled Salamanders, Red-backed Salamanders, Eastern Worm
Snakes, and Ringneck Snakes through multiple sampling seasons (Hines and
MacKenzie 2002). These 4 species were selected as focal species because they
were the only species detected >5 times over the entire year. By conducting
multiple surveys within each sampling season, we were able to model changes
in occupancy and detection probabilities across the seasons (MacKenzie et al.
2002, 2003, 2006). We developed multi-season models with every combination
of covariates (precipitation, temperature, and habitat type) for each focal species.
We reported only models with ΔAICc scores of less than 2. We used program
DOBSERVE to estimate detection probabilities and abundance of egg masses
(Hines 1996). We used egg-mass abundance estimates to calculate the abundance
of breeding Spotted Salamander females (Nichols et al. 2000). We used 2 models,
the first held variation of detection due to observer effect constant and the second
allowed for variation of detection based on observer.
We recorded opportunistic encounters by HBNP staff to supplement the species
inventory. This species list was compared with historical records of species
within HBNP from personal field notes of A. Braswell (North Carolina Museum
of Natural Sciences [NCMNS], Raleigh, NC, 2010 unpubl. data) and a species
list developed by M. Johns (Hemlock Bluffs Nature Preserve [HBNP], Cary, NC,
2010 unpubl. data).
Sampling season influenced detection for all focal species (Table 1). Detection
of Ringneck Snake was highest in summer, and we did not detect individuals
during spring or winter (Table 2). Ringneck Snake had the lowest number of detections
of the 4 focal species. We detected Eastern Worm Snake the most during
spring and did not detect this species during summer or fall (Table 2). We most
commonly detected Marbled Salamander during fall and Red-backed Salamander
during winter but did not detect either species during the spring or summer
Table 1. Multi-season occupancy models for each focal species from program PRESENCE. ΔAICc
scores of less than 2 designate appropriate top models for each species. Habitat type influenced
site occupancy (Ψ), whereas ambient temperature and precipitation events influenced detection
Species Top occupancy models AICc Δ AICc
Worm Snake Ψγεp(seasons)(precip) 91.77 0.00
Marbled Salamander Ψγεp(seasons)(temp) 128.24 0.00
Red-backed Salamander Ψγεp(seasons)(temp) 109.82 0.00
Ringneck Snake Ψγεp(seasons) 61.23 0.00
Ψγεp(seasons)(precip) 61.46 0.23
Ψ(habitat)γεp(seasons) 63.03 1.80
344 Southeastern Naturalist Vol. 12, No. 2
(Table 2). Temperature was an important predictor of detection for the 2 salamander
species, with higher detection probabilities during the cooler months of the
year (Table 1, 3). Precipitation was present in top models for both snake species;
however, 95% confidence intervals of parameter estimates overlapped zero.
Site-occupancy estimates for Eastern Worm Snake and Ringneck Snake were
constant across seasons (Table 2). Occupancy estimates were highest in winter for
Marbled Salamander and in fall for Red-backed Salamander. Increased site-occupancy
parameter estimates during fall and winter corresponded with the timing of
breeding-season migrations for both salamander species. Habitat type was not an
influential predictor of occupancy for any of the four focal species (Table 1).
Egg-mass detection and salamander abundance
The first survey produced a higher count of egg masses, so we used it for
analysis in the DOBSERV software. Detection of egg masses differed only by
an AICc weight of 0.0002 between the 2 models, and the top model did not
include the observer covariate (Table 4). The estimated range of egg-mass
abundance was 84.7 to 88.6. Therefore, estimates of breeding female Spotted
Salamander abundance, considering egg masses could range from 2 to 4 per female,
were between 21.2 and 44.3 across the 3 pools surveyed.
Table 3. Parameter estimates, standard error (SE), and 95% confidence intervals for temperature
from multi-season occupancy models.
Species Estimate SE 95%CI
Marbled Salamander 1.105887 0.448135 0.2324–1.9842
Red-backed Salamander -1.308516 0.674132 -2.6298–0.0128
Table 2. Occupancy (Ψ), standard error (SE), and detection probability (P) estimates from the top
model for each focal species across the seasons. Seasons were designated as spring = March–May,
summer = June–August, fall = September–December, winter = January–March. * = species not
Species Season Ψ 95%CI SE P
Worm Snake Spring 0.34 0.08–0.75 0.20 0.13
Winter 0.34 0.08–0.75 0.20 0.02
Marbled Salamander Spring*
Fall 0.47 0.03–0.91 0.23 0.09
Winter 0.62 0.13–1.10 0.25 0.02
Red-backed Salamander Spring*
Fall 0.23 0.05–0.41 0.09 0.09
Winter 0.11 -0.02–0.24 0.07 0.14
Ringneck Snake Spring*
Summer 0.18 -0.13–0.49 0.16 0.07
Fall 0.18 -0.13–0.49 0.16 0.02
2013 S. Becker, C. Moorman, C. DePerno, and T. Simons 345
Species richness inventory
We documented 22 of the 25 amphibian species previously known to occur
within HBNP (Table 5). Two caudate and 2 anuran species were recorded in historical
surveys but not detected in recent surveys. Three anuran species detected
in recent surveys (Historic 2 and Present surveys) went undetected in Historic
1 (Table 5). In addition, we documented 21 of the 28 reptilian species reported
in historical accounts (Table 6). Six squamate species and 1 testudinate species
not detected in present surveys had been previously detected (Table 6). Thirteen
reptilian species detected in recent surveys (Historic 2 and Present surveys) had
not been detected in Historic survey 1. Overall, we documented 43 of the 53 reptile
and amphibian species previously known to occur within HBNP.
Table 4. Models for Spotted Salamander egg-mass abundance estimates from program DOBSERV.
Model AICc ΔAICc P n (egg masses) 95% CI n (adult females)
p (.,.) 8.178 0.000 0.9921 86.68 84.7–88.6 21.2–44.3
p (.,observer) 10.230 2.052 0.9923 86.67 84.7–88.6 21.2–44.3
Table 5. Comprehensive list of amphibian species detected within Hemlock Bluffs Nature Preserve,
Cary, NC. Species from current survey (March 2010 through March 2011) were compared against
historical inventory data collected from March 1973 through February 1984 (Historic 1) and inventory
data collected from 1990 through 2009 (Historic 2).
Species Historic 1 Historic 2 Present
Acris crepitans (Northern Cricket Frog) X X X
Anaxyrus americanus (American Toad) X X X
Anaxyrus fowleri (Fowler’s Toad ) X X
Gastrophryne carolinensis (Eastern Narrowmouth Toad) X X X
Hyla chrysoscelis (Cope’s Gray Treefrog) X X X
Hyla cinerea (Green Treefrog) X X
Hyla squirella (Squirrel Treefrog) X
Lithobates catesbeianus (American Bullfrog) X X X
Lithobates clamitans (Green Frog) X X X
Lithobates sphenocephalus (Southern Leopard Frog) X X
Pseudacris crucifer (Spring Peeper) X X X
Pseudacris feriarum (Upland Chorus Frog) X X X
Scaphiopus holbrookii (Eastern Spadefoot) X
Ambystoma maculatum (Spotted Salamander) X X X
Ambystoma opacum (Marbled Salamander) X X X
Desmognathus fuscus (Northern Dusky Salamander) X X X
Eurycea cirrigera (Southern Two-lined Salamander) X X X
Eurycea guttolineata (Three-lined Salamander) X X X
Eurycea quadridigitata (Dwarf Salamander) X X X
Hemidactylium scutatum (Four-toed Salamander) X X X
Notophthalmus viridescens viridescens (Red-spotted Newt) X X X
Plethodon cinereus (Red-backed Salamander) X X X
Plethodon cylindraceus (White-spotted slimy Salamander) X X X
Pseudotriton montanus (Mud Salamander) X X
Pseudotriton ruber (Red Salamander) X
346 Southeastern Naturalist Vol. 12, No. 2
Occupancy modeling is an efficient method for parks and nature preserves
to monitor the presence of species. Common approaches to monitoring herpetofauna
based on ad-hoc inventories are subject to biases from a variety of
factors affecting species detection probabilities. We detected several species not
previously recorded at HBNP, possibly due to site colonization or our sampling
design, which provided more spatially complete sampling. Anaxyrus fowleri
Hinckley (Fowler’s Toad), Lithobates sphenocephalus Cope (Southern Leopard
Frog), and 13 historically undetected reptilian species have wide ranges across
North Carolina and were likely present but not detected during surveys prior to
1990 (Historic 1) (Beane et al. 2010). Conversely, the Hyla cinerea Schneider
(Green Treefrog) range in North Carolina has expanded westward from the
Table 6. Comprehensive list of reptilian species detected within Hemlock Bluffs Nature Preserve,
Cary, NC. Species from current survey (March 2010 through March 2011) were compared against
historical inventory data collected from March 1973 through February 1984 (Historic 1) and inventory
data collected from 1990 through 2009 (Historic 2).
Species Historic 1 Historic 2 Present
Agkistrodon contortrix (Copperhead) X X
Anolis carolinensis (Green Anole) X X
Carphophis amoenus (Eastern Worm Snake) X X
Coluber constrictor (Black Racer) X X
Diadophis punctatus (Ringneck Snake) X X X
Elaphe guttata guttata (Corn Snake) X
Elaphe obsolete obsoleta (Black Rat Snake) X X X
Eumeces fasciatus (Five-lined Skink) X X X
Eumeces laticeps (Broadhead Skink) X X
Heterodon platirhinos (Eastern Hog-nosed Snake) X X
Lampropeltis calligaster rhombommaculata (Mole Kingsnake) X
Lampropeltis getula getula (Eastern Kingsnake) X
Nerodia erythrogaster erythrogaster (Redbelly Water Snake) X
Nerodia sipedon (Northern Water Snake) X X X
Opheodrys aestivus (Rough Green Snake) X X
Sceloporus undulatus (Eastern Fence Lizard) X X
Scincella lateralis (Ground Skink) X X
Storeria dekayi (Brown Snake) X X X
Tantilla coronata (Southeastern Crowned Snake) X
Thamnophis sauritus (Eastern Ribbon Snake) X X
Thamnophis sirtalis (Common Garter Snake) X X
Virginia striatula (Rough Earth Snake) X
Chelydra serpentine (Common Snapping Turtle) X X
Clemmys guttata (Spotted Turtle) X X X
Kinosternon subrubrum (Eastern Mud Turtle) X X X
Sternotherus odoratus (Common Musk Turtle) X X X
Terrapene carolina (Eastern Box Turtle) X X
Tracemys scripta scripta (Yellow-bellied Slider) X
2013 S. Becker, C. Moorman, C. DePerno, and T. Simons 347
Coastal Plain indicating it may have been absent from HBNP during Historic 1
(Beane et al. 2010).
Site extinction and the short time frame of our study may explain why we
did not detect 7 reptilian and 2 anuran species historically recorded at HBNP.
Generally, herpetofauna have low detection probabilities and detection can be
highly variable depending on changes in environmental covariates (Dodd 2010).
Most of the species we did not detect are nocturnal, secretive, or rare (Beane et
al. 2010). These characteristics and our short sampling time frame reduced the
probability of detection. In addition to our short sampling time frame, changing
habitat conditions leading to site extinctions may explain why 2 caudate (Pseudotriton
montanus Baird [Mud Salamander] and Pseudotriton ruber Sonni de
Manoncourt and Latreille [Red Salamander]) and 2 squamate (Thamnophis sauritus
L. [Eastern Ribbon Snake] and Nerodia erythrogaster erythrogaster Forster
[Red-bellied Water Snake]) species were not detected. Forest succession and increased
water discharge enabled vegetation to encroach into the spring-fed seeps
within the lowlands of HBNP, which altered the Swift Creek stream morphology
and made habitat conditions less suitable for these 4 species (Beane et al. 2010;
M. Johns, pers. comm.).
Although our comparisons across inventories imply site extinction or colonization,
there is no quantifiable data from historical methods to help explain
non-detections. Conversely, estimating occupancy and detection probabilities
allowed park staff to account for external influences and design a replicable protocol
for future long-term monitoring. Although Hemlock Bluffs Nature Preserve
had historical records of several species of special concern to North Carolina,
including Tantilla coronata Baird and Girard (Southeastern Crowned Snake)
and Hemidactylium scutatum Temminck and Schlegel (Four-toed Salamander)
(Alvin Braswell, North Carolina Museum of Natural Sciences, Raleigh, NC, and
M. Johns, pers. comm.), we are not able to use these historical records to assess
changes in species occurrence because prior surveys lacked any measure of detection
In the future, occupancy modeling will allow preserve staff to work more
efficiently by accounting for environmental covariates that influence detection.
Because sampling season influenced detection probability for all 4 focal
species, sampling could occur only during seasons with the highest detection
probabilities. Ambient temperature influenced detection of both salamander species,
indicating monitoring programs could account for the influence of annual
climatic variation on salamander detection. Detection of both salamander species
was low from April to October, when temperatures were above monthly averages
Although modeling occupancy and detection probability provides a preferable
alternative to compiling simple species inventories, there are limitations
to this approach. Rare species that are often the focus of monitoring programs
occur with very low and highly variable detection probabilities (Royle and
Nichols 2003). However, including covariates influential to detection (e.g.,
weather conditions, seasonal behavior patterns, and differences between
348 Southeastern Naturalist Vol. 12, No. 2
observers) improves occupancy estimates for rare species (MacKenzie et al.
2006). Additionally, occupancy modeling estimates only species occurrence
and not population abundance. Therefore, tracking changes in population size is
not possible with this approach alone.
We used two sampling methods to monitor herpetofauna on HBNP, but there
are other methods not implemented in this survey that may increase detection
probabilities of focal species (Heyer et al. 1994, Hutchens and DePerno 2009).
Repeated visual encounter surveys in selected plots would provide more sampling
events and improve estimate accuracy (MacKenzie et al. 2006). Drift-fence
arrays provide a passive capture method that is especially effective at detecting
nocturnal and secretive species; however, effort required to install, maintain,
and monitor drift-fence arrays is often more expensive and time consuming than
small preserves can afford (Heyer et al. 1994). Calling amphibian surveys can account
for anuran species that otherwise have low detection probabilities, require
no equipment, and can cover large sampling areas (Dodd 2010).
Available statistical software such as PRESENCE and DOBSERV may present
an additional challenge for park staff not trained in statistical analysis. We
recommend parks and nature preserves work with local universities or hire
system-wide personnel that are trained to use statistical software. Some training
of HBNP staff is needed to collect and compile data using occupancy-based
methods, but the cost of this training is minimal.
Randomization of site locations helps reduce estimate bias (Heyer et al.
1994), but randomization may be difficult to accomplish at small parks and
nature preserves. We were unable to establish site locations randomly at
HBNP because we were concerned that patrons would disturb our plots and
reduce our detection probabilities. Parks with high visitation such as HBNP
prioritize preservation of wildlife habitat and patron safety. Sampling locations
often represent a balance between effectively sampling each habitat type
and reducing the visibility of site locations.
We believe long-term multi-season occupancy modeling provides a useful
approach for long-term species monitoring in parks and nature preserves with
limited resources. Traditional approaches based on simple inventories are subject
to multiple sources of bias due to variations in detection probability. Integrating
occupancy modeling into a park or nature preserve monitoring protocol generates
quantifiable results that can be compared across long time frames and provide
reliable insight to guide management decisions.
We thank M. Johns, L. White, and the staff of Hemlock Bluffs State Nature Preserve
for assistance in the field and for granting access to preserve property. A. Braswell
granted access to historical NC Museum of Natural Sciences records and personal field
notes. K. Burge assisted with conducting egg-mass surveys. M. Johns, A. Braswell, J.
Hall, J. Beane, E. Corey, and J. Humphries offered insightful discussions on site-specific
herpetofauna natural history.
2013 S. Becker, C. Moorman, C. DePerno, and T. Simons 349
Alford, R.A., and S.J. Richards. 1999. Global amphibian declines: A problem in applied
ecology. Annual Review of Ecology and Systematics 30:133–165.
Beane, J.C., A.L. Braswell, J.C. Mitchell, W.M. Palmer, and J. Dermid. 2010. Amphibians
and Reptiles of the Carolinas and Virginia, 2nd Edition. The University of North
Carolina Press, Chapel Hill, NC. 274 pp.
Bury, R.B., and P.S. Corn. 1988. Douglas-fir forests in the Oregon and Washington Cascades.
Relation of the herpetofauna to stand age and moisture. Management of Amphibians,
Reptiles, and Small Mammals in North America. General Technical Report
RM - 166. Rocky Mountain Forest and Range Experiment Station, US Department of
Agriculture, Forest Service. Pp. 11–22.
Dodd, C.K., Jr. 2010. Amphibian Ecology and Conservation: A Handbook of Techniques.
Oxford University Press, Inc., New York, NY. 556 pp.
Doyle, M.W., E.H. Stanley, D.L. Strayer, R.B. Jacobson, and J.C. Schmidt. 2005. Effective
discharge analysis of ecological processes in streams. Water Resources Research
Dunson, W.A., R.L. Wyman, and E.S. Corbett. 1992. A symposium on amphibian declines
and habitat acidification. Journal of Herpetology 26:349– 352.
Egan, R.S., and P.W.C. Paton. 2004. Within-pond parameters affecting oviposition by
Wood Frogs and Spotted Salamanders. Wetlands 24:1–13.
Feest, A. 2006. Establishing baseline indices for the quality of biodiversity of restored
habitats using a standardized sampling process. Restoration Ecology 14(1):112–122.
Gamble, L.R., K. McGarigal, D.B. Sigourney, and B.C. Timm. 2009. Survival and breeding
frequency in Marbled Salamanders (Ambystoma opacum): Implications for spatiotemporal
population dynamics. Copeia 2:394–407.
Gardner, T.A., J. Barlow, and C.A. Peres. 2007. Paradox, presumption, and pitfalls in
conservation biology: The importance of habitat change for amphibians and reptiles.
Biological Conservation 138:167–179.
Gibbons, J.W., D.E. Scott, T.J. Ryan, K.A. Buhlmann, T.D. Tuberville, B.S. Metts, J.L.
Greene, T. Mills, Y. Leiden, S. Poppy, and C.T. Winne. 2000. The global decline of
reptiles, déjà vu amphibians. BioScience 50:655–666.
Gooch, M.M., A.M. Heupel, S.J. Price, and M.E. Dorcas. 2006. The effects of survey
protocol on detection probabilities and site occupancy estimates of summer breeding
anurans. Applied Herpetology 3:129–142.
Grant, E.H.C., R.E. Jung, J.D. Nichols, and J.E. Hines. 2005. Double-observer approach
to estimating egg-mass abundance of pool-breeding amphibians. Wetlands Ecology
and Management 13:305–320.
Hanlin, H.G., F.D. Martin, L.D. Wike, and S.H. Bennett. 2000. Terrestrial activity,
abundance, and species richness of amphibians in managed forests in South Carolina.
American Midland Naturalist 143:70–83.
Heyer, W.R., M.A. Donnelly, R.W. McDiarmid, L.C. Hayek, and M.S. Foster. 1994.
Measuring and Monitoring Biological Diversity: Standard Methods for Amphibians.
Smithsonian Institution Press, Washington, DC. 364 pp.
Hines, J.E. 1996. DOBSERV Software to estimate detection probability and abundance
from double-observer approach. USGS-PWRC. Available online at http://www.mbrpwrc.
usgs.gov/software/dobserv.shtml. Accessed 6 May 2011.
Hines, J.E., and D.L. MacKenzie. 2002. PRESENCE Software to estimate patch occupancy
rates and related parameters. USGS-PWRC. Available online at http://www.
mbr-pwrc.usgs.gov/software/presence.shtml. Accessed 29 August 2010.
350 Southeastern Naturalist Vol. 12, No. 2
Hutchens, S., and C. DePerno. 2009. Measuring species diversity to determine land-use
effects on reptile and amphibian assemblages. Amphibia-Reptilia 30(1):81–88.
Integrated Taxonomic Information System (ITIS). 2011. Available online at http://www.
itis.gov. Accessed 8 July 2011.
MacKenzie, D.L. 2005. What are the issues with presence-absence data for wildlife managers?
Journal of Wildlife Management 69(3):849–860.
MacKenzie, D.L., J.D. Nichols, G.B. Lachman, S. Droege, J.A. Royle, and C.A.
Langtimm. 2002. Estimating site-occupancy rates when detection probabilities are
less than one. Ecology 83(8):2248–2255.
MacKenzie, D.L., J.D. Nichols, J.E. Hines, M.G. Knutson, and A.B. Franklin. 2003. Estimating
site occupancy, colonization, and local extinction when a species is detected
imperfectly. Ecology 84(8):2200–2207.
MacKenzie, D.L., J.D. Nichols, J.A. Royle, K.H. Pollock, L.L. Bailey, and J.E. Hines.
2006. Occupancy Estimation and Modeling: Inferring Patterns and Dynamics of Species
Occurrence. Academic Press, New York, NY. 324 pp.
Nichols, J.D., J.E. Hines, J.R. Sauer, F.W. Fallon, and P.J. Geglund. 2000. A Doubleobserver
approach for estimating detection probability and abundance from point
counts. The Auk 117(2):393–408.
Nichols, J.D., J.E. Hines, D.L. MacKenzie, M.E. Seamans, and R.J. Gutierrez. 2007. Occupancy
estimation and modeling with multiple states and state uncertainty. Ecology
Pechman, J.H.K., D.E. Scott, R.D. Semlitsch, J.P. Caldwell, L.J. Vitt, and J.W. Gibbons.
1991. Declining amphibian populations: The problem of separating human
impacts from natural fluctuations. Science 253:892–895.
Petranka, J.W. 1998. Salamanders of the United States and Canada. Smithsonian Institution
Press, Washington, DC. 587 pp.
Royle, J.A., and J.D. Nichols. 2003. Estimating abundance from repeated presenceabsence
data or point counts. Ecology 84:777–790.
Smith, L.L., W.J. Barichivich, J.S. Staiger, K.G. Smith, and C.K. Dodd, Jr. 2006. Detection
probabilities and site-occupancy estimates for amphibians at Okefenokee National
Wildlife Refuge. American Midland Naturalist 155:149–161.
Southeast Regional Climate Center (SERCC). 2011. Period of record monthly climate
summary. NC State University, Raleigh, NC. Available online at http://www. sercc.
com/cgi-bin/sercc/cliMAIN.pl?nc7079. Accessed 18 September 2011.
Stuart, S.N., J.S. Chanson, N.A. Cox, B.E. Young, A.S.L. Rodrigues, D.L. Fischman, and
R.W. Walker. 2004. Status and trends of amphibian declines and extinctions worldwide.
United States Geological Survey (USGS). 2011. USGS surface-water annual statistics
for the nation. Available online at http://waterdata.usgs.gov/usa/nwis/uv?02087580.
Accessed 8 July 2011.
Wake, D.B. 1991. Declining amphibian populations. Science 253:860.
Williams, A.K, and J. Berkson. 2004. Reducing false absences in survey data: Detection
probabilities of Red-backed Salamanders. Journal of Wildlife Management
Yoccoz, N.G., J.D. Nichols, and T. Boulinier. 2001. Monitoring of biological diversity in
space and time. Trends in Ecology and Evolution 16:446–453.
2013 S. Becker, C. Moorman, C. DePerno, and T. Simons 351
Appendix 1. Taxonomic classification of all reptilian and amphibian species referenced
in the study with corresponding authority names (ITIS 201 1).
Anaxyrus americanus Holbrook (American Toad)
Anaxyrus fowleri Hinckley (Fowler’s Toad)
Acris crepitans Baird (Northern Cricket Frog)
Hyla chrysoscelis Cope (Cope’s Gray Treefrog)
Hyla cinerea Schneider (Green Treefrog)
Hyla squirella Bosc (Squirrel Treefrog)
Pseudacris crucifer Wied-Neuwied (Spring Peeper)
Pseudacris feriarum Baird (Upland Chorus Frog)
Lithobates catesbeianus Shaw (American Bullfrog)
Lithobates clamitans Latreille (Green Frog)
Lithobates sphenocephalus Cope (Southern Leopard Frog)
Gastrophryne carolinensis Holbrook (Eastern Narrowmouth Toad)
Scaphiopus holbrookii Harlan (Eastern Spadefoot)
Ambystoma maculatum Shaw (Spotted Salamander)
Ambystoma opacum Gravenhorst (Marbled Salamander)
Desmognathus fuscus Rafinesque (Northern Dusky Salamander)
Eurycea cirrigera Green (Southern Two-lined Salamander)
Eurycea guttolineata Holbrook (Three-lined Salamander)
Eurycea quadridigitata Holbrook (Dwarf Salamander)
Hemidactylium scutatum Temminck & Schlegel (Four-toed Salamander)
Plethodon cinereus Green (Red-backed Salamander)
Plethodon cylindraceus Harlan (White-spotted slimy Salamander)
Pseudotriton montanus Baird (Mud Salamander)
Pseudotriton ruber Sonnini de Manoncourt and Latreille (Red Salamander)
Notophthalmus viridescens viridescens Rafinesque (Red-spotted Newt)
Sceloporus undulatus Bosc & Daudin (Eastern Fence Lizard)
Anolis carolinensis Voigt (Green Anole)
Eumeces fasciatus L. (Five-lined Skink)
Eumeces laticeps Schneider (Broadhead Skink)
Scincella lateralis Say (Ground Skink)
352 Southeastern Naturalist Vol. 12, No. 2
Carphophis amoenus Say (Eastern Worm Snake)
Coluber constrictor L. (Black Racer)
Diadophis punctatus L. (Ringneck Snake)
Elaphe guttata guttata L. (Corn Snake)
Elaphe obsolete obsoleta Say (Black Rat Snake)
Heterodon platirhinos Latreille (Eastern Hog-nosed Snake)
Lampropeltis calligaster rhombommaculata Holbrook (Mole Kingsnake)
Lampropeltis getula getula L. (Eastern Kingsnake)
Nerodia erythrogaster erythrogaster Forster (Redbelly Water Snake)
Nerodia sipedon L. (Northern Water Snake)
Opheodrys aestivus L. (Rough Green Snake)
Storeria dekayi Holbrook (Brown Snake)
Tantilla coronata Baird & Girard (Southeastern Crowned Snake)
Thamnophis sauritus L. (Eastern Ribbon Snake)
Thamnophis sirtalis L. (Common Garter Snake)
Virginia striatula L. (Rough Earth Snake)
Agkistrodon contortrix L. (Copperhead)
Chelydra serpentina L. (Common Snapping Turtle)
Clemmys guttata Schneider (Spotted Turtle)
Terrapene carolina L. (Eastern Box Turtle)
Tracemys scripta scripta Schoepff (Yellow-bellied Slider)
Kinosternon subrubrum Lacepede (Eastern Mud Turtle)
Sternotherus odoratus Latreille (Common Musk Turtle)