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J.C. Maerz, R.K. Barrett, K.K. Cecala, and J.L. Devore
22001155 SOUTHEASTERN NATURALIST 1V4o(4l.) :1747,1 N–7o8. 44
Detecting Enigmatic Declines of A Once Common
Salamander in the Coastal Plain of Georgia
John C. Maerz1,*, R. Kyle Barrett1,2, Kristen K. Cecala1,3, and Jayna L. Devore1,4
Abstract - For amphibian species suspected of undergoing enigmatic declines, it is important
to determine the effort required to confidently establish species absence. Desmognathus
auriculatus (Southern Dusky Salamander) has purportedly gone from being quite common
throughout the southeastern US Coastal Plain to now being enigmatically rare. We used
repeated standardized surveys of 5 historically occupied streams and their adjacent riparian
zones between 2007 and 2010 to estimate detection rate of Southern Dusky Salamanders.
We detected Southern Dusky Salamanders at 3 of 5 historic sites. Mean detection rate across
streams known to be occupied at least once during the study was moderately low (mean ±
1 SE = 0.20 ± 0.12 for a double-sampled 50-m survey), improved at 2 sites with increasing
time since drought, and varied among streams. For comparison, we evaluated detection rates
of several other stream salamanders and found those rates to range from 0.37 (± 0.07) for
Eurycea quadridigitata (Dwarf Salamander) to 0.08 (± 0.01) for Siren intermedia (Lesser
Siren). Based on mark–recapture along a 200-m section of stream and the associated riparian
habitat at the site where Southern Dusky Salamanders were most often detected, we
estimated 43 (± 15) and 97 (± 161) individuals to be present February–May 2009 and October
2009–May 2010, respectively. Despite abundant adults, Southern Dusky Salamanders
were the only species that we failed to detect as larvae; however, we observed many newly
metamorphosed Southern Dusky Salamanders—usually under logs with saturated soil and
often near entrances to crayfish burrows. Our results generally support the characterizations
of Southern Dusky Salamanders as having become enigmatically uncommon. Because landcover
change in the study area has been minimal, we suspect habitat damage from Sus scrofa
(Feral Pig) may be responsible for the variation in Southern Dusky Salamander presence
and abundance among sites. Because of the low detectability of Southern Dusky Salamanders,
future work to identify factors driving Southern Dusky Salamander distribution and
abundance will require intensive sampling at sites to provide robust estimates of occupancy
or population size.
Introduction
Amphibian population declines are recognized as a large component of an accelerating
and complex biodiversity conservation crisis (Berger et al. 1998, Collins
2010, Pounds et al. 1999, Wilcove and Master 2005). Multiple and different factors
can contribute to population declines and local extirpation including interactions
1Warnell School of Forestry and Natural Resources, 180 E. Green Street, University of Georgia,
Athens, GA 30602. 2Current address - School of Agricultural, Forest, and Environmental
Sciences, Clemson University, 261 Lehotsky Hall, Clemson, SC 29634. 3Current address
- Department of Biology, 735 University Avenue, Sewanee: The University of the South,
Sewanee, TN 37383. 4Current address - School of Biological Sciences A08, University of
Sydney, New South Wales 2006, Australia. *Corresponding author - jcmaerz@uga.edu.
Manuscript Editor: Joseph Pechmann
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with invasive species, habitat loss and degradation, climate change, over-exploitation,
ultraviolet radiation, contaminants, and emerging infectious pathogens
(reviewed by Blaustein and Kiesecker 2002, Collins 2010, Collins and Storfer
2003, Lannoo 2005, Semlitsch 2003). Ultimately, any specific decline is likely the
result of multiple interacting factors (Blaustein and Kiesecker 2002), and identifying
the etiological agents of a decline is often a challenge.
The apparent decline of Desmognathus auriculatus (Holbrook) (Southern Dusky
Salamander) populations across large portions of the species’ range is an example
of an “enigmatic” amphibian decline (Graham et al. 2010). Southern Dusky Salamanders
are found exclusively within the coastal plain of the southeastern United
States. The southeastern US is a global hotspot for salamander diversity, but declines
of some species such as Ambystoma cingulatum Cope (Frosted Flatwoods
Salamander) and Notophthalmus perstriatus Bishop (Striped Newt) have been documented.
These declines are largely attributed to habitat loss and alteration (Means
2005, Palis and Means 2005). Southern Dusky Salamanders inhabit swamps and
blackwater creeks, and were routinely described as the most common and abundant
salamander in blackwater habitats (Means and Travis 2007). However, the species
has conspicuously declined across its range including at sites within large protected
areas (Beamer 2005, Dodd 1998, Means and Travis 2007). Causes of decline may
include impacts of Sus scrofa L. (Feral Pig), disease (Graham 2006), and habitat
loss and alteration; however, no cause has been conclusively linked to the decreases
in Southern Dusky Salamander detection throughout its range (Means 2005).
For species that are difficult to detect due to rarity or cryptic behavior, monitoring
and conservation planning can be challenging. Even demonstrating that management
is necessary for a species such as Southern Dusky Salamanders is complex. Predecline
reports of species counts do not reliably quantify search effort (Dodd 1998),
and in some cases salamanders of other species may have been counted as sightings
of Southern Dusky Salamanders (Beamer and Lamb 2008, Graham et al. 2010).
Because few historical data exist to quantify the magnitude of declines, future management
of the species must rely on the most reasonable assessments of historical
population estimates, combined with robust monitoring approaches that maximize
efficiency of survey efforts. Short, simple surveys are often insufficient to reliably
determine a species’ absence at a site (Dodd and Dorazio 2004). To address this issue
quantitatively, managers and conservation biologists need tools that will provide reasonable
assurance that failure to find the species is not a false negative.
Our goal was to estimate detection and abundance patterns among historic
Southern Dusky Salamander sites at Ft. Stewart, GA, and to use this information
to further evaluate the steps required to adequately monitor this species throughout
its range. To meet this goal, we determined the level of sampling necessary to
determine confidently that Southern Dusky Salamanders (and other stream salamanders
for comparison) are no longer present at a site, and we provide an estimate
of population size for Southern Dusky Salamanders at one occupied site. Based on
our experience and results, we propose a tiered process for evaluating causative
agents of suspected range-wide population declines in rare and secretive species.
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Field–Site Description
We focused the field-based portion of this study within the boundaries of Ft.
Stewart, GA. Fort Stewart is located approximately 30 miles west of Savannah
and has been in operation since 1940. All of our sampling locations were in the
northwest area of the installation within the Canoochee River system (Fig. 1). The
area is characterized by frequently burned flatwoods and sand hills, and networks
of slow-moving blackwater creeks. Genetic evidence has shown that the only
Desmognathine salamander found in this area is the Southern Dusky Salamander
(Beamer and Lamb 2008).
Site selection on Ft. Stewart began in August 2007 when the creeks that were
dry the previous year from a prolonged drought filled with some late summer rains.
Using information from recent surveys (Graham 2006), and consultations with the
military base’s biologist (Dirk Stevenson), we identified 4 initial sites with historic
records of Southern Dusky Salamanders for this study. We later added a fifth site
where it was suspected and we later confirmed that Southern Dusky Salamanders
might occur. The proximity of these sites allowed us to sample all of them repeatedly
over a 1- to 4-day period, which provided an opportunity to assess detection
probabilities for Southern Dusky Salamanders and other species at those sites. The
majority of sites were characterized by a shallow, braided stream network with
stands of Taxodium distichum L. (Bald Cypress) and Nyssa aquatica L. (Water
Figure 1. Location of the study sites found within Ft Stewart, GA. The imagery shows the
relatively undeveloped watersheds within which the focal streams are located.
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Tupelo). One site (F11/12) was a deeply channeled, quick moving creek that was
atypical of the region. Though F11/12 did not fit the classic description of Southern
Dusky Salamander habitat, it was a listed historical site.
Methods
Sampling methodology
From November 2007 to January 2008, we conducted preliminary sampling at
all sites except F14 to evaluate methods for Southern Dusky Salamander surveys.
In February 2008, we established four 50-m transects along the water line during
each site visit, and we sampled these transects twice (up and back) on 2 consecutive
days. This procedure was followed in February, March, April, and May of 2008,
and twice more in February 2009. In March, April, May, October (1 and 29), and
December 2009 and April and May 2010, we only made a single-day sampling visit
to all sites (Fig. 2). During each sample pass, we dip-netted an area ~1-m wide out
from the water line as well as raked the leaf litter and turned all cover objects >5
cm in diameter in a 1-m swath directly adjacent to the water line. Activities on the
military base made it routinely difficult to travel to site F11/12, so we eliminated
Figure 2. Irregular detection
of Southern Dusky
Salamanders, Dwarf Salamanders,
Mud Salamanders,
and Many-lined Salamanders
at 5 focal study
sites on Ft. Stewart, GA.
Dates range from November
2007 to May 2010.
Months listed twice were
sampled at the beginning
and the end of that month.
Hollow symbols represent
no detection, and shaded
symbols indicate a positive
detection. The amount
of shading (1/2 vs. full)
indicates whether the species
was detected on one
or both consecutive days
of sampling (respectively).
Left-side shading indicates
the species was detected
on Day 1 and right-side
shading indicates detection
on Day 2. Samples from
March 2009–May 2010
were single-day samples
only.
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this site from our regular sampling protocol after May 2008. In April 2008, we
identified a new site (F14) for Southern Dusky Salamanders. From May 2008 to
May 2010, we focused only on 4 sites: F18/19, E6/8, F20B, and F14. At each site
on each sample day, we surveyed 4 consecutive 50-m transects twice each (once
up and once back). Data on water temperature, water depth, soil temperature, pH,
dissolved oxygen, and conductivity were collected at E6/8, F11/12, F18/19, and
F20B on five occasions from November 2007 to January 2008, but do to few detections
of Southern Dusky Salamanders during that period we were not able to model
the influence of those factors on detection rate. In November 2008, we collected
site-level variables at E6/8, F14, F18/19, and F20B, including percentage of area
covered in leaf litter, depth of leaf litter, and percentage of riparian zone with signs
of pig activity (assessed visually in 10% increments).
For all Southern Dusky Salamanders (and occasionally, for other species)
captured, we recorded species, life stage (adult or larva based on the absence
or presence of gills, respectively), sex, snout–vent length, total length, and wet
mass. Data on capture location (water, leaf litter, or cover object) and capture
technique were recorded for most, but not all encounters. All Southern Dusky
Salamanders were uniquely marked using visible implant elastomer (VIE) and
then released at their original capture location (University of Georgia IACUC
#A2007-10190).
Analyses
Data from all sampling occasions were used to describe general patterns of
species richness and capture numbers across sites. We used data from sampling
months during the period February 2008–May 2010 to calculate the detection
probability for each species at each site, and then we calculated a mean detection
probability and standard error among all streams or only those streams where
a species was detected during our study. We report this as the mean probability
and standard error of detecting the species at a site, assuming it is present, during
a double–sampled 50-m survey (up and back) of the water line. We extrapolate
this value to derive the mean cumulative probability of missing a species during
consecutive surveys of a stream, which provides a guideline for the number
of surveys required to ensure sufficient sampling effort. We calculated these
probabilities for Southern Dusky Salamanders and for 4 other sympatric species
(Eurycea quadridigitata [Dwarf Salamander], Pseudotriton montanus [Mud Salamander],
Siren intermedia [Lesser Siren], and Stereochilus marginatus [Many–
lined Salamander]). We included these other members of the stream salamander
assemblage in our analysis to demonstrate the efficacy of these survey methods
for species occupying similar habitats as Southern Dusky Salamanders.
Detection probability was calculated in the manner detailed above, rather
than the more formalized calculations offered by programs such as Presence
(MacKenzie et al. 2006), which would require sampling of a larger number
of sites. A Bayesian approach may have provided a viable alternative (Kéry
2009); however, we did not explore that option. For all species except Southern
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Dusky Salamanders, we only used streams where at least one individual was
detected during the sampling period to estimate detection probability. To assess
general patterns of detection probability for Southern Dusky Salamanders, we
used 2 different approaches. First, we used all study sites (E6/8, F11/12, F14,
F18/19, and F20B) where Southern Dusky Salamanders were historically present.
The second, more conservative approach, involved only using the 3 sites
where Southern Dusky Salamanders were detected during our sampling efforts
beginning in February 2008. We felt the first, more liberal approach, was worth
exploring for 2 reasons. First, while we never detected Southern Dusky Salamanders
at E6/8 or F11/12, the species had been found at both streams within the past
14 years (D. Stevenson, The Orianne Society, Athens, GA, pers. comm.). Second,
we failed to detect the species consecutively from one month to the next at several
of the sites, and on consecutive days in 6 cases at 3 different streams (Fig. 2).
Thus, these 2 analyses bracket detection rates for Southern Dusky Salamanders
at these historic sites.
Site F20B provided a sufficient number of Southern Dusky Salamander recaptures
to estimate population size using a robust design framework in Program
MARK (Williams et al. 2001). Because this species undergoes metamorphosis in
late spring in Georgia (Means 2008), and we only captured individuals post-metamorphosis,
we consider primary sampling periods to be delimited by May sampling
periods—the period after which one might begin to capture individuals from a new
cohort. Specifically, we divided samples into 3 primary sampling periods (February
2008–May 2008, February 2009–May 2009, and October 2009–May 2010),
with 7, 7, and 5 secondary sampling periods in each, respectively. In all models,
immigration and emigration were fixed at zero, and survivorship was assumed to
be equal across primary sampling occasions. We evaluated 3 models; in each, hypothesized
abundance parameters across sample occasions were unique, but models
varied based on assumptions about capture/recapture probabilities (p) across occasions
(Table 1). The number of parameters that could be estimated for models was
limited because the population size of this species was low even at the site where
it was the most abundant. Despite the limited ability to explore a large number of
model structures, we feel that our targeted approach strikes an appropriate balance
between ignoring issues of detection probability altogether and over-stepping the
analytical constraints inherent to small datasets.
Table 1. Hypothesized models of capture/recapture probabilities and associated support for Southern
Dusky Salamanders at stream F20B, Ft. Stewart, GA. The “primary only” model indicates detection
probability was set to vary only across primary sampling occasions (see Methods for details), while
the “all occasions” model represents a scenario in which detection probability varies across each visit
to the site. The p = c(.) model represents a constant capture and recapture probability.
Model AICc ΔAICc AICc weight Model likelihood
p = c(.), N(t) 74.26 0.00 0.52 1.00
p = c(time specific, primary only), N(t) 74.43 0.17 0.48 0.92
p = c(time specific, all occasions), N(t) 143.41 69.15 0.00 0.00
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Results
Physical conditions
Water levels and other conditions showed dramatic variation temporally. Waterquality
variables at E6/8, F11/12, F18/19, and F20B varied temporally. Dissolved
oxygen varied remarkably over the sampling period from a mean across all sites of
40% and 44% (range = 23–63%) in November and December 2007, respectively, to
a mean of 80% (range = 73–86%) in January 2008. Mean water pH across sites was
low (4.92; range = 4.49–5.79) and relatively stable temporally. Average litter depth
showed little variation across sites, with a low mean value of 2.0 cm at E6/8 and a
high mean value of 2.4 cm at F18/19. Similarly, the percentage of plots covered by
leaf litter (as measured in November 2008) varied little, ranging from 86% at F20B
to 94% at F11/12. The percentage of area turned recently by Feral Pigs was 78%
and 67% at E6/8 and F14, respectively. In contrast, we observed no pig activity at
sites F18/19 and F20B.
Species- and assemblage-level summary data
Between November 2007 and May 2010, we spent ~800 person hours sampling
amphibians on Ft. Stewart, including at least 160 person hours each at the 4 localities
believed to be the most likely to yield Southern Dusky Salamanders. We
captured 443 salamanders of 8 different species (Table 2). The Dwarf Salamander
was the most frequently detected salamander species followed by the Many-lined
Salamander, Southern Dusky Salamander, and Plethodon ocmulgee (Ocmulgee
Slimy Salamander). Larvae were the most frequently detected life stage for Southern
Two–Lined Salamanders, Lesser Sirens, and Many-lined Salamanders, while
adults were more commonly found for Mud Salamanders and Dwarf Salamanders.
No larval Southern Dusky Salamanders were captured.
We captured a total of 41 Southern Dusky Salamanders at 3 sites (F18/19,
F20B, and F14) with 1 recapture of the only individual caught at site F14, and 8
Table 2. Captures of salamanders from Ft. Stewart, GA, study sites. Numbers indicate the count of
individuals located at each site.
Sites
Species E6/8 F11/12 F14 F18/19 F20B
Desmognathus auriculatus Holbrook (Southern – – 1 7 33
Dusky Salamander)
Eurycea cirrigera Green (Southern Two-lined – 28 – 1 –
Salamander)
Eurycea quadridigitata Holbrook (Dwarf 41 1 119 55 16
Salamander)
Pseudotriton montanus Baird (Mud Salamander) – 1 – 5 11
Siren intermedia Barnes (Lesser Siren) – – 8 19 –
Siren lacertina L.(Greater Siren) – 1 – – –
Stereochilus marginatus Hallowell (Many-lined – – 55 1 1
Salamander)
Plethodon ocmulgee Highton (Ocmulgee Slimy – – 8 2 30
Salamander)
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individuals recaptured at least once from F20B (yielding 0.06 captures/person-hr).
Ninety-four percent of Southern Dusky Salamander captures were of individuals
found by turning cover along the stream bank or just at the water line. One individual
was located while raking leaf litter, and 1 was dip-netted from the stream. No
Southern Dusky Salamanders were found at site E6/8 or F11/12. Southern Dusky
Salamanders ranged in size from 22 to 68 mm SVL and 42 to 122 mm TL, with
an average mass of 2.5 g (range = 0.3–5.0 g). Of the 34 individuals on which we
attempted to make a sex determination, 11 were female, 7 were male, and 16 were
recently metamorphosed juveniles. Two of the 11 females were gravid upon capture
(found in March 2008 and February 2009). Fourteen of the 16 recently metamorphosed
juveniles were found during or after the fall of 2009.
Detection probability
Assuming all study sites were occupied, we estimate that the mean detection
probability (± 1 SE) for Southern Dusky Salamanders when double-sampling a
50-m transect was 0.15 (± 0.10). The mean detection probability for Southern
Dusky Salamanders among the 3 sites where we found the species during our study
was 0.20 (± 0.12). These detection rates were intermediate to other salamander
species observed among the same streams during our study (Table 3). The mean
detection probability for Dwarf Salamanders (0.37 ± 0.07) was the highest among
all salamander species we encountered.
In terms of sampling effort, to be ≥90% confident that a species that was not
detected at a site was indeed not present, the average minimum number of double
samples of a 50-m transect would be 5, 11, 19, 24, and 27 for Dwarf Salamanders,
Southern Dusky Salamanders, Mud Salamanders, Many-lined Salamanders, and
Lesser Sirens, respectively (Table 3). These estimates do not address variation in
detection among sites. For example, detection is often a function of density, and
at F20B, where we captured the majority of Southern Dusky Salamanders, we
detected individuals on 45% of samples. In contrast, we detected Southern Dusky
Salamanders at F14 and F18/19 during only 6% and 11% of samples, respectively.
Our estimates of mean detection probability assume that detection remained
constant through time for the sample period used; however, detection of some
salamander species appears to have increased at some sites after March 2008 (e.g.,
Southern Dusky Salamanders at F20B), which was approximately 6 months after
the drought broke (Fig. 2).
Population status at F20B
We recorded 40 captures of Southern Dusky Salamanders (of 33 individuals)
within a 200-m length of stream and riparian area at Site F20B, with 7 recaptures
of marked animals. We were able to execute 3 models, which allowed us to assess
the effects of variation in capture/recapture probability on estimates of population
size. The model assuming constant p and the model assuming p varied among
primary sampling occasions had nearly identical support based on comparisons
using Akaike’s Information Criterion (AIC; Table 1). Model averaging (± unconditional
SE) of these 2 models for second and third primary periods yielded abundance
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estimates of 43 (± 15) and 97 (± 161) individuals per 200-m length of riparian forest,
respectively. The model assuming p varied among primary sampling occasions was
responsible for the larger estimate of mean abundance and its associated high unconditional
standard error in the model averaging results for Period 3. The constant
p model for that period provides an estimate of abundance that is more similar to that
in Period 2 (40 ± 16 individuals). Estimates for the first primary period were nonidentifiable
in the period-dependent model, and were estimated to be suspiciously
low in the constant-p model (4.5 ± 3.2 individuals). The estimate for individual capture
probability generated by the constant-p model for site F20B was low (0.07). For
the model where capture/recapture probability was allowed to vary across primary
periods, p was only identifiable for Periods 2 and 3, but each value was similar to
that from the constant-p model (0.09 ± 0.03 and 0.02 ± 0.02, respectively).
Table 3. Mean detection probability and associated probability of missing a species if present across a
range of sampling numbers for select salamander species at Ft. Stewart, GA, between November 2007
and May 2010. A “sample” refers to a double-search (up and back) of a 50-m transect along the water
line including dip-netting all areas within 1 m of water line, and raking all debris and searching all
cover 1 m above the water line. For each species, the minimim number of samplesat which one would
have a ≤0.10 (*) and ≤0.05(**) chance of not detecting the spec ies after a specified number of visits.
Note that only a subset of sample numbers are shown.
Species
Southern Southern
Dusky Dusky Dwarf Mud Many-lined Lesser
SalamanderA SalamanderB SalamanderB SalamanderB SalamanderB SirenB
Mean detection 0.15 (0.10) 0.20 (0.12) 0.37 (0.07) 0.11 (0.03) 0.09 (0.07) 0.08 (0.01)
probability (SE)
No. sites where species - 3 5 3 3 2
was detected
# of samples Probability species was present, but not detected
1 0.85 0.80 0.63 0.89 0.91 0.92
2 0.73 0.64 0.39 0.79 0.83 0.85
3 0.62 0.51 0.24 0.70 0.75 0.78
4 0.53 0.41 0.15 0.62 0.68 0.72
5 0.45 0.33 0.10* 0.55 0.62 0.66
7 0.33 0.21 0.04** 0.44 0.51 0.56
11 0.17 0.09* 0.01 0.27 0.35 0.40
15 0.09* 0.04** 0.00 0.17 0.24 0.28
19 0.05** 0.01 0.00 0.10* 0.16 0.20
24 0.02 0.00 0.00 0.06 0.10* 0.13
25 0.02 0.00 0.00 0.05** 0.09 0.12
27 0.01 0.00 0.00 0.04 0.08 0.10*
31 0.01 0.00 0.00 0.03 0.05** 0.07
35 0.00 0.00 0.00 0.02 0.04 0.05**
AEstimates based on detection rate among 5 streams where the species was historically reported present.
BEstimates based on detection rate among streams where streams where the species was detected during
this study.
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Discussion
Our results generally support other recent characterizations of Southern Dusky
Salamanders as having gone from historically “common” to enigmatically uncommon
in various parts of the species’ range (Graham et al. 2010, Means and Travis
2007). On Ft. Stewart, Southern Dusky Salamanders were difficult to detect at
most sites, except after February 2009 at a single site (F20B). Means and Travis
(2007) report catching 8.65 Southern Dusky Salamanders per person-hour during
the 1970s in the Florida Panhandle, and Graham et al. (2010) found 6 Southern
Dusky Salamanders at F18/19 in 1 hour of searching in 2006. The number of
Southern Dusky Salamanders captured by Graham et al. (2010) in 1 hour in 2006
is comparable to the total number we captured over 31 months at the same site.
There were historic reports of Southern Dusky Salamanders at E6/8 and F11/12
within the past 14 years (D. Stevenson, pers. comm.); however, we estimate the
probability that Southern Dusky Salamanders were present but went undetected at
E6/8 or F11/12 during our study period is less than 0.005. Thus it would be reasonable to
conclude that Southern Dusky Salamanders have declined at Ft. Stewart. However,
by focusing on extensive sampling of 5 focal streams over a 31-month period
rather than single, concurrent samples over broad geographic areas (e.g, Graham
et al. 2010), our results suggest that drought effects on local populations could
limit detection for several years, and make it difficult to distinguish sites where
the species is temporarily undetectable from sites where the species is genuinely
rare or absent.
All of our study streams were dry from August 2006 through October 2007,
and this was the second prolonged drought within a decade. Though occupancy of
some stream-breeding salamanders can remain high during drought years (Price et
al. 2012), extreme droughts are linked to amphibian population declines at other
sites within the region (Daszak et al. 2005). We found that 2 years post drought,
dusky salamanders became relatively common and easy to detect at one historic site
(F20B), while remaining rare or absent at other nearby historic sites. The best evidence
that drought was the major factor initially driving low salamander detection
was the low detection rates of Dwarf Salamanders at all sites from November 2007
through February 2008 (Fig. 2). Dwarf Salamanders are widespread and abundant
in forested blackwater habitats in the region. From November 2007 through April
2009, detection of Dwarf Salamanders increased among all sites, and by October
2009 we found Dwarf Salamanders in large numbers at every site sampled (Fig 2).
We continued to detect Dwarf Salamanders in high numbers on every visit at 3 sites
from October 2009 through May 2010.
Detection of Southern Dusky Salamanders followed a similar pattern at sites
F20B and F18/19, with no detections in November and December 2007, periodic
detections from January through May 2008, and then consistent detections
at F20B from February 2009 through May 2010 (Fig. 2). However, unlike Dwarf
Salamanders, we only saw a consistent increase in Southern Dusky Salamander
detection at F20B, and F20B was the only site where we ever detected multiple
individuals during a visit. Estimates from mark–recapture at F20B indicated that
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2015 Vol. 14, No. 4
individual capture probability was low. Low capture probability may explain why
Southern Dusky Salamanders are difficult to detect at sites where abundance is
also low.
The absence or low abundance of Southern Dusky Salamanders at historic sites
proximate to one site where they remain relatively common suggests that local
factors are important determinants of Southern Dusky Salamander abundance.
Large amounts of habitat have been altered across the range of Southern Dusky
Salamanders; however, it is unlikely that habitat loss is linked to the apparent
rarity of Southern Dusky Salamanders in Georgia and within Ft. Stewart. First,
watersheds across Georgia with historical Southern Dusky Salamander populations
have lost little forested wetland habitat between 1974 and 2005, and forested
wetland remains the second largest land-cover class within historical Southern
Dusky Salamander watersheds in Georgia (Maerz 2010). Second, Southern Dusky
Salamanders appear increasingly rare even in watersheds contained within large
protected areas such as Ft. Stewart, where the watersheds that include our focal
sites have not experienced any significant land-cover change over the past 30 years
(Maerz 2010). We hypothesize that the most likely factor contributing to the rarity
of Southern Dusky Salamanders and potentially other salamanders is the activity of
Feral Pigs. We observed extensive pig damage at sites E6/8 and F14, where Southern
Dusky salamanders were rare or extirpated. In contrast, we did not observe
any comparable hog damage at F20B, where Southern Dusky Salamanders were
regularly detected, or at F18/19, which was our second best site for detecting the
species. Our observations are consistent with those of Means and Travis (2007) for
Southern Dusky Salamanders in Florida where the species appears to have declined
and is now characterized as rare concurrent with extensive damage by Feral Pigs.
We feel it is important to note that despite our finding numerous breeding adult
Southern Dusky Salamanders at F20B, that species was the only one we failed to
detect as larvae at Ft. Stewart. Sampling for larval salamanders is a common approach
for rapid inventory and monitoring because it is often a relatively highly
detectable life stage for many species (Graeter et al. 2013). We successfully detected
larvae of several uncommon salamander species with few if any adult detections,
so the failure to detect larval Southern Dusky Salamanders despite captures
of breeding adults is notable. Moreover, we observed many newly metamorphosed
Southern Dusky Salamanders in 2009 and 2010. One metamorphic Southern Dusky
Salamander was captured in a dip net at the wetted edge of F18/19, but the remainder
of metamorphic Southern Dusky Salamanders were found under logs away
from the main stream channel. In many cases, the soil was saturated with the water
table near the soil surface, and the metamorphic Southern Dusky Salamanders were
often positioned within pooled water and near entrances to crayfish burrows. Little
is known about the larval natural history of Southern Dusky Salamanders, which
hampers our ability to fully understand the factors that regulate the species’ distribution
and abundance and identify causes of local declines. We speculate that larval
Southern Dusky Salamanders may occur in subsurface waters around blackwater
streams, which would limit the effectiveness of stream sampling to detect larvae,
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and could also contribute to the species’ sensitivity to the impacts of Feral Pig damage
to soils along the margins of blackwater streams.
As with any species, evaluating factors potentially affecting Southern Dusky
Salamander distribution and abundance depends on establishing accurate patterns
of occupancy among sites. Because detection rates for the species can be low and
sensitive to recent weather events such as drought, it will be necessary to be strategic
when selecting sites for comparison and to maximize survey effort at those
sites in order to detect a relationship between environmental factors and species
occurrence. Our study lays the groundwork for a more rigorous future assessment
connecting environmental factors such as land-cover change or Feral Pig damage
to the current status of Southern Dusky Salamanders in Georgia. Our study can be
used to inform the amount of sampling that may be required to confidently determine
Southern Dusky Salamander presence or absence. Detection is not an intrinsic
property of a species (Mazzerolle et al. 2007); however, it is reasonable to use estimates
from prior studies and other sites to guide future research.
Collectively, the work we have done suggests a series of steps that will optimize
resources applied to assessment, monitoring, and management of rare or cryptic
wildlife. First, it is important to estimate sampling effort required to detect species
with a desired level of confidence. Once a desired, robust sampling effort is
determined, then a subset of sites selected across an identified gradient (e.g., landcover
change or habitat alteration by invasive species) should be sampled. Further,
more-intense monitoring efforts such as mark–recapture studies can be conducted
within a subset of occupied habitats (Conroy et al. 2008). More-robust data on occupancy
and abundance among sites along an environmental gradient will allow for
rigorous tests of whether specific factors are contributing to the current status of
species within a region. This approach contrasts with the more traditional approach
of sampling all (or most) historical sites to assign presence or abundance and then
correlating variables post hoc to that pattern. In most cases, sampling effort may be
insufficient due to low detection, researchers will have little confidence in assigning
presence or absence, and causal inferences may be weak. We recognize the value
of searching for post hoc correlations when there is no clear mechanism explaining
declines; however, when reasonable hypotheses can be formulated, we believe
that resources diluted in sampling many sites would be better allocated to more focused
sampling of mechanistic gradients established a priori. The effort required to
document the enigmatic decline of a rare species is considerable. A combination of
environmental gradients identified a priori and occupancy-based surveys provides
a framework that will likely yield the most efficient use of lim ited resources.
Acknowledgments
We would like to thank S.P. Graham for initiating this project and for inspiration. We
also thank A. Durso, M.Erickson, A. Ferreira, A. Grosse, T. Pierson, J. Milanovich, L.
Ruyle, and S. Sterrett for field assistance and J. Macey, who facilitated access to Ft. Stewart.
D. Stevenson provided valuable insights and early assistance in locating streams with
Southern Dusky Salamanders. Thanks to A. McKee, B. Crawford, and K. Stohlgren for
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2015 Vol. 14, No. 4
reviewing early drafts of this manuscript. Funding was provided by a Georgia Department
of Natural Resources State Wildlife Grant.
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