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Review and Synthesis of Estimated Vital Rates for Terrestrial Salamanders in
the Family Plethodontidae
Jillian S. Howard
1
and John C. Maerz
2
Population models depend on reliable estimates of vital rates, yet for many taxa, such estimates and how they vary in
response to spatial or temporal environmental gradients are lacking. The goal of this review was to determine whether
existing estimates of vital rates for temperate, direct-developing plethodontid salamanders (subfamily Plethodonti-
nae) could be used to reasonably project values for populations or species where such estimates are lacking, or whether
current estimates are biased in a manner that limits their utility. We synthesized current knowledge of stage-specific
survival rates, age- and size-at-maturity at first clutch, and clutch frequency. We tested for expected correlations
among published vital rates (e.g., age at maturity and survival) and between vital rates and factors such as body size or
latitude. We used matrix projection models to judge whether published estimates were reasonably possible for stable
salamander populations. The largest number of published vital rates were for clutch size, clutch frequency (proportion
of females with clutches), size at maturity or first clutch, and age at maturity or first clutch, though the latter vital rate
is primarily inferred from size distribution and growth rate data. Among these vital rates, we found expected
correlations with body size and latitude suggesting these rates were reasonable and somewhat predictable among
species or populations. In contrast, there were few estimates of egg hatch rate or juvenile or adult survival. Hatch and
survival rate estimates were widely variable; estimates seldom included measures of uncertainty, but when uncertainty
measurements were included, they were generally high. Based on projection models, few survival estimates were likely
unbiased or realistic for stable populations given other salamander vital rates. Additionally, few studies quantified how
vital rates vary with spatial or temporal environmental gradients. We outline the key knowledge gaps that limit basic
demographic modeling of these remarkably common, influential, and otherwise well-studied salamanders, and make
recommendations for future research efforts.
POPULATION models are valuable tools for under-
standing animal ecology, diagnosing anthropogenic
causes of decline, and developing effective manage-
ment strategies (Caswell, 2000; Heppell et al., 2000; Morris
and Doak, 2002; Conroy and Carroll, 2009). Rigorous
population models depend on reliable estimates of vital
rates, yet for many taxa, such estimates and how they vary in
response to spatial or temporal environmental gradients are
lacking (Heppell, 1998; Heppell et al., 2000). For amphibians,
missing vital rates is a chronic problem which likely stems
from their highly latent life histories (Bailey et al., 2004a,
2004b; Wells, 2007). Even for the most well-studied and
abundant amphibian species, we lack essential vital rates that
can populate even basic demographic models. This funda-
mental knowledge gap can hinder our ability to forecast how
populations may fluctuate in space and time in response to
global change or to develop models to inform management.
Salamanders in the family Plethodontidae are among the
most widely studied amphibians, particularly in temperate
North America. A Web of Science (Clarivate Analytics, 2018)
search using the keyword ‘Plethodontidae’ returned 5,572
published studies between 1864 and 2018; however, among
all 468 species combined, there are only a small number of
estimates for the most basic vital rates, and few attempts to
model population dynamics have been made for any species.
Temperate North American plethodontids are often the most
abundant vertebrates in forest ecosystems (Burton and
Likens, 1975; Hairston, 1987; Ovaska and Gregory, 1989;
Welsh and Lind, 1992), where they are important prey for
other taxa such as snakes, small mammals, and birds
(Petranka, 1998; Jobe et al., 2019) and can influence key
ecosystem processes including the abundance of soil inver-
tebrates, leaf litter decomposition, and nutrient dynamics
(Davic and Welsh, 2004; Best and Welsh, 2014). Our lack of
understanding of population dynamics for this important
group of organisms limits our understanding of how
salamander effects on ecosystems may vary spatially or
temporally and may impede effective conservation in the
face of multiple threats to salamander populations and
species persistence (Maerz et al., 2009; Milanovich et al.,
2010; Martel et al., 2013; Barrett and Price, 2014; Bean, 2015;
Mallakpour and Villarini, 2017; Cecala et al., 2018).
In this review, we summarized and synthesized published
vital rate estimates for temperate, direct-developing species
within the family Plethodontidae, subfamily Plethodontinae
(Wake, 2012). We chose to focus only on direct-developing
species because life history is directly related to vital rates, and
addressing differences in rates among species with and
without larval phases was beyond our focus. Specific vital
rates included: stage- or age-specific survival from egg to adult,
1
Swaim Biological Inc., 4556 Contractors Pl., Livermore, California 94551; Email: jillianhoward163@gmail.com. Send reprint requests to this
address.
2
Warnell School of Forestry and Natural Resources, University of Georgia, 180 E Green St., Athens, Georgia 30602; Email: jcmaerz@uga.edu.
Submitted: 20 May 2020. Accepted: 3 July 2021. Associate Editor: C. Bevier.
Ó2021 by the American Society of Ichthyologists and Herpetologists DOI: 10.1643/h2020079 Published online: 22 October 2021
Ichthyology & Herpetology 109, No. 4, 2021, 929–939
size and age at first reproduction (defined as age when first
clutch is deposited), the annual proportion of females that
breed (clutch frequency), and clutch size. We examined
whether vital rate estimates were correlated or varied based
on methodology, study duration, body size, or geography. We
used a Leslie projection matrix to evaluate whether published
or putative vital rate estimates were reasonable (limited bias).
Ultimately, the goal of this paper was to scrutinize the limited
nature and numbers of vital rates available for these species,
thereby illustrating the need for more and better efforts to
estimate demographic and vital rates over temporal and spatial
gradients. We also suggest elements of study design that would
yield more rigorous and less biased estimates going forward.
MATERIALS AND METHODS
Literature review.—We reviewed published estimates of vital
rates of direct-developing North American, European, and
Asian species of the subfamily Plethodontinae within the
family Plethodontidae, which included the genera Aneides,
Ensatina,Hydromantes,Karsenia,Plethodon,Speleomantes, and
the desmognathine species Desmognathus aeneus,D. wrighti,
and Phaeognathus hubrichti (Wiens et al., 2006; Wake, 2012).
We elected not to broaden our review to include estimates for
the genus Batrachoseps within the subfamily Hemidactylinae.
Batrachoseps do occur in temperate North America and have
direct development, but they represent a distinct clade. We
used several approaches to identify primary sources for vital
rate estimates. References were initially collected from species
accounts found in Lannoo (2005). In addition, between
January 1, 2015 and April 1, 2020, we conducted searches in
the Google Scholar (Google Inc., 2018) and Web of Science
databases (Clarivate Analytics, 2018) spanning the years
1900 to 2020 using the terms Plethodontidae, Aneides,
Ensatina,Hydromantes,Karsenia,Plethodon,Speleomantes,
Desmognathus aeneus,D. wrighti,orPhaeognathus paired with
the words ‘life history’, ‘demography’, ‘natural history’,
‘survival’, ‘survival rate’, ‘fecundity’, ‘reproduction’, ‘repro-
ductive rates’, ‘maturation’, ‘sexual maturity’, ‘hatch rate’,
‘eggs’, or ‘clutch size’. We identified additional sources from
references within papers collected through the prior two
methods. We excluded sources, or some data contained
within a source, when clearly inaccurate or when the rate was
not explicitly substantiated by data. All collected data with
citations are provided in a single table in the supplementary
materials (Supplementary Table 1; see Data Accessibility).
Modeling vital rate relationships.—We selected relationships
between published vital rate estimates and other commonly
available factors based on theorized and observed plethodon-
tid life history patterns. A pillar of life-history theory is the
idea that relationships exist among some life-history traits
such as age at maturity and adult survival, and body size and
fecundity (Gadgil and Bossert, 1970; Stearns, 1989; Wine-
miller and Rose, 1992). Generally, plethodontid life histories
are characterized by delayed maturity to a large adult body
size relative to size at hatching, intermediate frequency of
reproduction among females with high adult survival, and
large eggs with small clutch sizes relative to other salamanders
and for a given body size (Sayler, 1966; Salthe, 1969);
however, there is variation in size and—presumably—age at
maturity that creates exceptions to this general pattern.
We used regression analysis to model the following
relationships among published vital rates: (1) clutch size
and snout–vent length at first reproduction; (2) annual
clutch frequency and latitude of studied population; (3) age
at first reproduction, snout–vent length at first reproduction,
and latitude of studied population; and (4) apparent annual
adult or non-size-specific survival and study duration. For
some vital rates where there was insufficient data to model,
we used visual examination of plotted data to determine
whether relationships might exist. We did this to compare (1)
adult survival and snout–vent length at first reproduction;
and (2) adult survival and age at first reproduction. We
assigned population latitude from published location data or
we used Google Earth Pro (Google Inc., 2017) to determine
the latitude of the approximate center of the study area as
described in the publication.
Matrix projection model analysis.—We used a females-only,
age-based projection matrix to construct isoclines where
combinations of vital rates would yield stable populations (k
¼1). This is a post-birth model in which individuals survive
before reproducing. We parameterized the model with mean
annual age-specific survival rates across species and reports,
mean age at first clutch across species and reports, mean
clutch size across species and reports, mean hatch rate across
species and reports, and mean annual clutch frequency
across species and reports (Table 1). The literature is
somewhat confusing on the topic of age at first clutch, most
often ‘age at maturity’ is reported, but the amount of time
between maturity and first reproduction can be variable
across individuals, cohorts, locations, etc. We added six
months to each estimate of age at maturity based on the
assumption that most females would deposit a first clutch six
months after reaching maturity and mating. Because we
calculated mean age at first clutch as 3.88 years, the fecundity
term was first applied in the base model to age 4 animals.
The projection matrix used was:
000fu4fu5fu6þ
u100 0 0 0
0u200 0 0
00u300 0
000 u400
000 0 u5u6þ
2
6
6
6
6
6
6
4
3
7
7
7
7
7
7
5
We assumed fwas equal to zero for animals age 3 or younger,
and we varied ffor animals greater than age 3 to examine the
effects of first clutch produced at different ages. We
superimposed published estimates of juvenile and adult
survival on isocline plots to assess whether published
estimates were likely biased. This approach was premised
on the assumption that published vital rates were estimated
from data collected on stable salamander populations, that
stability is achieved through intrinsic rates of survival and
recruitment and not dependent on immigration, and that
vital rates are not density dependent. The validity of these
assumptions in relation to our inferences is discussed later.
RESULTS
While estimates of body-size-dependent clutch size were
relatively consistent within and among species, and size at
maturity was generally consistent within species, estimates of
survival, clutch frequency, and egg hatch rates were highly
930 Ichthyology & Herpetology 109, No. 4, 2021
variable within and among species (Supplementary Table 1;
see Data Accessibility).
Adult survival.—We found 15 published studies with esti-
mates of survival or apparent survival (does not distinguish
between permanent emigration and mortality [Lebreton et
al., 1992; Sandercock, 2006; Supplementary Table 1; see Data
Accessibility]). One published study generated survival rates
with no explicit time unit (such as annual or monthly) and
was not included in our summary estimates (Kniowski and
Reichenbach, 2009). A second study was excluded because
the confidence limits around the survival estimate included
both 0 and 1 (Welsh and Lind, 1992). The 13 remaining
studies estimated juvenile and/or adult apparent survival
rates for Aneides (Lee et al., 2012), Desmognathus (Organ,
1961; Bruce, 2013), Plethodon (Hairston, 1983; Marvin, 1996;
Welsh et al., 2008; Otto et al., 2014; Connette and Semlitsch,
2015; Taylor et al., 2015; Peele et al., 2017; Caruso and
Rissler, 2018), Speleomantes (Lindstr¨
om et al., 2010), or a
single composite apparent survival rate for two species of
Plethodon and one species of Ensatina (Olson and Kluber,
2012; Table 1; Supplementary Table 1; see Data Accessibility).
No study reported survival rates for Phaeognathus hubrichti or
for the genus Karsenia.
Six studies generated separate apparent survival estimates
for juvenile and adult life stages (Organ, 1961; Hairston,
1983; Marvin, 1996; Lindstr¨
om et al., 2010; Lee et al., 2012;
Caruso and Rissler, 2018), while all others estimated only
adult survival, or a single, non-age-specific survival rate.
Lindstr¨
om et al. (2010) and Lee et al. (2012) were the only
studies to evaluate the plausibility of their survival estimates.
Using matrix models, Lindstr¨
om et al. (2010) estimated the
median growth rate (k) for a population of Speleomantes
strinatii to be 0.95 (95% confidence interval: 0.91–0.99),
while Lee et al. (2012) estimated the growth rate (k) for a
population of Aneides lugubris to be between 0.928 and 1.093.
Among the 13 studies considered here, the estimates of
apparent annual adult or non-age-specific survival probabil-
ity ranged from 0.215 to 0.882, and when provided, the
standard error ranged from 0.03 to 0.23 (Supplementary
Table 1; see Data Accessibility). Estimated survival probability
was only weakly positively correlated with study duration
(survival ¼0.586þ0.0202*study duration;R
2
¼0.0313; where
duration is measured in years; Fig. 1A). Whether the author
identified the study site as disturbed or not disturbed did not
have any apparent effect on the variation among the limited
number of estimated survival rates (Fig. 1A).
Only five studies estimated both survival probability and
snout–vent length (SVL) at maturity, and only five of these
estimated both survival probability and age at maturity.
Among this limited number of studies, there was a strong
positive relationship (R
2
¼0.730) between survival probabil-
ity and length at maturity (Fig. 1B):
survival ¼0:630 þ0:0284 SVL
and a moderate positive relationship (R
2
¼0.412) between
survival probability and age at maturity (Fig. 1C):
survival ¼0:645 þ0:0386 age
Whether the estimate was generated using repeated counts or
capture–mark–recapture did not have an apparent effect on
the relationship between study design and estimated survival
though we caution that there were limited data to quanti-
tatively evaluate this potential relationship (Fig. 1B, C).
Egg survival (hatch rate).—Because plethodontines lay eggs in
locations that are difficult to access without disturbing the nest
site such as underground burrows, beneath rocks and logs, or
Table 1. Mean published demographic rates used in the age-based projection matrix.
Annual survival by age (year)
Species 0 1 2 3 4 5þ
Aneides lugubris 0.363 0.45 0.552 0.625 0.668 0.783
Desmognathus aeneus 0.215 0.215 0.215 0.215 0.215 0.215
Desmognathus wrighti 0.593 0.593 0.593 0.233 0.593 0.252
Ensatina eschscholtzii þPlethodon dunni þP. vehiculum 0.64 0.64 0.64 0.64 0.64 0.64
Plethodon albagula 0.69 0.69 0.69 0.69 0.69 0.69
Plethodon cinereus 0.707 0.707 0.707 0.707 0.707 0.707
Plethodon elongatus — — — 0.47 0.47 0.47
Plethodon kentucki — 0.48 0.68 0.72 0.72 0.72
Plethodon metcalfi 0.837 0.364 0.484 0.81 0.81 0.81
Plethodon montanus 0.294 0.384 0.592 0.715 0.882 0.882
Plethodon shermani — — — 0.66 0.66 0.66
Speleomantes strinatii 0.2 0.2 0.2 0.42 0.42 0.72
Mean 0.504 0.472 0.535 0.575 0.623 0.629
Standard deviation 0.238 0.184 0.186 0.196 0.181 0.21
First age to apply fecundity rate 4
Mean Standard deviation
Age at first clutch 3.88 1.09
Average hatch rate 0.66 0.24
Average clutch size 11.4 6
Average clutch frequency 0.56 0.25
Howard and Maerz—Vital rates of Plethodontidae 931
in natural caves and abandoned mines (Wells, 2007), it makes
repeated observations of nests in situ challenging. We found 24
published reports of egg-hatch rates and used one unpublished
dataset from coauthor Maerz for P. cinereus. We excluded ten of
the published reports because the estimates were methodo-
logically unreliable (Supplementary Table 1; see Data Accessi-
bility). The remaining reported hatch rates ranged from 0.216
to 1 with standard deviations from 0.062 to 0.53 where
provided (Supplementary Table 1; see Data Accessibility).
Age and size at maturity.—Age and SVL at maturity, and
population latitude were available for Aneides lugubris and A.
hardii,Desmognathus aeneus,Ensatina eschscholtzii, 21 species
of Plethodon,Speleomantes ambrosii, and S. sarrabusensis. For
species with all three values reported by multiple studies, we
treated each study as an independent data point (Supple-
mentary Table 1; see Data Accessibility).
Among all studies, mean reported age at maturity was
positively correlated with both length at maturity and
population latitude (Fig. 2A, B):
age ¼3:259 þ0:531 SVL þ0:345 latitude
and the adjusted R
2
value was 0.427 (Fig. 2A, B).
Fig. 1. Across all three plots, genera are coded symbolically: Aneides ¼triangle, Desmognathus ¼square, Plethodon ¼circle, Speleomantes ¼‘3,’
and the one combined estimate for Plethodon and Ensatina ¼diamond. The fitted regression lines are black, while the upper and lower 95%
confidence limit lines are gray. Plot A shows the relationship between estimated annual adult or non-age-specific survival probability and study
duration for temperate, direct-developing salamanders in the subfamily Plethodontinae. In this plot, open symbols denote estimates from studies in
‘undisturbed’ habitats, and black symbols denote estimates from studies in ‘disturbed’ habitats. Plot B shows the relationship between estimated
adult or non-age-specific survival probability and snout–vent length. Gray points indicate estimates from count data, white points indicate estimates
from capture–mark–recapture studies, and error bars indicate standard errors if reported by the study. Plot C shows the relationship between
estimated adult or non-age-specific survival probability and age at maturity (in years). Point colors indicate study type, and error bars are standard
errors, as in plot B.
932 Ichthyology & Herpetology 109, No. 4, 2021
Clutch frequency.—Across most, if not all, plethodontid
species, males are assumed to have an annual reproduction
probability of 1.0, while the probability of reproduction
among females is expected to be less than one and variable
among environments (examples in Highton, 1956; Fraser,
1974; Salthe and Mecham, 1974; Bull and Shine, 1979;
Semlitsch and West, 1983; Lynch, 1984; Herrington, 1985;
Ovaska, 1987; Takahashi and Pauley, 2010).
We found 68 estimates of clutch frequency for 37 species
within 45 published studies, of which 59 estimates (repre-
senting 31 species and 43 studies) could be associated with a
population latitude and had been obtained using reliable
methods (Supplementary Table 1; see Data Accessibility).
Across studies, clutch frequency declined with increasing
population latitude (Fig. 2C):
clutch frequency ¼1:655 0:0278 latitude
and the adjusted R
2
value was 0.213.
Clutch size.—We collected 227 clutch size reports from 144
sources. However, 17 reports were excluded due to meth-
odological concerns, and only 52 of the remaining reports
also had an estimate of mean SVL at maturity (Supplemen-
tary Table 1; see Data Accessibility) that could be used in
our regression analysis. Overall, clutch size increased with
SVL (Fig. 2D). Phaeognathus hubrichti was a clear outlier,
having the largest SVL at maturity but among the smallest
reported clutch size of all species in this review. When
Phaeognathus was included in the analysis, the regression
equation was
clutch size ¼1:032 þ0:204 SVL
and the adjusted R
2
value was 0.264. With Phaeognathus
excluded, the regression equation was
clutch size ¼3:817 þ0:317 SVL
Fig. 2. Regression relationships between vital rates for temperate, direct-developing salamanders in the family Plethodontidae. Across plots, genera
are coded by shapes: Aneides by triangles, Desmognathus by squares, Ensatina by diamonds, Phaeognathus by a ‘þ’ symbol, Speleomantes by a ‘3’
symbol, and Plethodon by circles. Gray lines represent 95% confidence intervals; the black line is the fitted regression line. Plots A and B show the
two sub-relationships included in the multivariate regression analysis for age at maturity, respectively: age at maturity and snout–vent length, and age
at maturity and latitude of the studied population. Plot C shows the relationship between frequency of reproductive females, which is interpreted as
the annual probability of female reproduction, and latitude of the studied population. Plot D shows the relationship between clutch size and body
size.The solid lines represent the fitted regression line and 95% confidence limits when all points are included in the analysis, while the dashed lines
represent the fitted regression line and 95% confidence limits when the outlying point, a single estimate for Phaeognathus hubrichti, is excluded.
Phaeognathus hubrichti is the longest species but has one of the smallest reported clutch sizes. When Phaeognathus hubrichti was removed, the
slope increased from 0.204 to 0.317, and the adjusted R
2
increased from 0.264 to 0.447.
Howard and Maerz—Vital rates of Plethodontidae 933
and the adjusted R
2
value was 0.447, indicating that both
the slope and the fit of the regression line increased (Fig.
2D).
Matrix projection model analysis.—We param e teriz e d the
matrix model with mean annual age-specific survival rates
across species and reports, mean age at first clutch across
species and reports (we added six months to reports of age at
maturity), mean clutch size across species and reports, mean
hatch rate across species and reports, and mean annual
clutch frequency across species and reports (Table 1). For
nearly all combinations of egg hatch rate (0.3, 0.5, or 0.75),
probability of laying a clutch (0.20, 0.33, 0.50, 0.75, and
1.00), and ages at first clutch (ages 4, 5, or 6), the majority of
published estimates of adult and juvenile survival were not
likely to result in stable population growth (k¼1; Fig. 3). In
fact, most estimates of adult survival were far too low for any
realistic combination of other vital rates to yield stable
population growth, and most estimates of adult survival
would result in projections of catastrophically rapid popula-
tion decline. Only under the most optimistic egg hatch rates
(0.75), earlier ages at first reproduction (4–5 years), and high
annual probability of producing a clutch (0.75–1.00) were a
majority of published estimates of adult and juvenile survival
likely to result in stable population growth (Fig. 3).
Fig. 3. Stable population growth (k¼1) isoclines for a generic, temperate, direct-developing salamander in the subfamily Plethodontinae. Each
isocline represents different combinations of female age at first reproduction, adult (age 5þ) and juvenile (age 1) annual survival, annual probability
(or proportion) a female lays a clutch, and probability an egg hatches. Egg hatch rates are organized by columns increasing from left to right, and age
at maturity is arranged as rows increasing from top to bottom. Probability of laying a clutch is represented by the different isoclines within each plot.
Each point represents a pair of published survival estimates for a given species (Supplementary Table 1; see Data Accessibility), with the genus
Aneides represented by triangles, Desmognathus by squares, Plethodon by circles, and the single study that produced a combined survival estimate
for Plethodon and Ensatina by diamonds. Dark gray points are those that fall to the left/below all isoclines indicating that those survival rate estimates
would result in a declining population (k,1) under all estimates of probability of laying a clutch at that age at maturity and egg hatch rate, and are
likely unrealistically biased estimates assuming the population was stable.
934 Ichthyology & Herpetology 109, No. 4, 2021
DISCUSSION
The information summarized in this review represents the
current, relatively limited knowledge of the vital rates of
temperate, direct-developing plethodontines—arguably
among the most widely studied amphibian clades. Most
species lack any published vital rate for even a single
population, and very few species have estimates of most of
the vital rates needed to parametrize a matrix projection
model. Only one study of one species had estimates from
multiple populations or locations that allowed for estimating
environmental effects on vital rates (Caruso and Rissler,
2018). Data limitation is a pervasive problem for modeling
population dynamics for many animal species, and one way
to address this limitation is to evaluate the transferability or
predictability of vital rate estimates across species, popula-
tions, and environments (e.g., Heppell, 1998; Heppell et al.,
2000). We found evidence for moderate predictive relation-
ships with body length and age at maturity and clutch size,
and age at maturity and probability of female reproduction
and latitude. Therefore, in the absence of direct estimates,
reasonable rates could be projected from these relationships
for use in population models.
In contrast with estimates of clutch size or age at maturity,
estimates of adult and juvenile survival and largely latent
vital rates such as egg hatch rate were very limited and
evidence of bias among survival and hatch rate estimates
currently limits robust prediction of those rates. Estimates of
adult survival were highly variable and most were likely
biased low and not plausible for a stable population in
conjunction with a wide range of other vital rates, based on
the outcome of the matrix population model simulations we
conducted. However, we did observe a moderate positive
relationship (R
2
¼0.412; Fig. 1B) between the seven
published estimates (from five studies) of adult survival and
age at maturity, and a strong positive relationship (R
2
¼
0.730; Fig. 1C) between those adult survival estimates and
SVL at maturity. A positive relationship between age at
maturity and adult survival is a robust relationship among
wide ranging taxa which may support, contrary to the model
simulation results, the accuracy of available survival esti-
mates. Nevertheless, we caution that any inferences about
these relationships are inherently weak because of limited
data.
One reason for bias among published survival rates is the
methodology used to estimate survival. The lowest and least
plausible published survival rate estimates were for Desmog-
nathus aeneus and D. wrighti. The low estimates for these
species are likely a result of using count data with no
correction for imperfect detection or temporary emigration,
and life tables to estimate instantaneous mortality rates
(Bruce, 2013). This approach assumes capture probabilities
are constant among individuals and through time (Conroy
and Carroll, 2009); these are unreasonable assumptions for
terrestrial salamanders. Terrestrial salamander surface activity
varies with weather and body size, and individuals spend
substantial portions of their time in inaccessible microhab-
itats (e.g., underground; Feder, 1983). As a result, both
capture probability and temporary emigration of terrestrial
salamanders is highly variable spatially and temporally with
variation in ambient moisture levels and certain character-
istics of habitat type (Bailey et al., 2004b; O’Donnell et al.,
2015). A model that does not account for capture probability
or temporary emigration assumes the observer has perfect or
near-perfect detection and that animals only emigrate
permanently. Thus, counts are interpreted as directly pro-
portional to the number of animals present at the sampling
location. When detection is low and temporary emigration
occurs frequently and at a rate unequal to the rate of return
to the sampling area from the temporarily emigrated state,
estimates of survival and abundance will be biased low.
Count data can be more rigorously analyzed using N-mixture
models (Royle, 2004; Zipkin et al., 2014), especially if counts
are repeated and employ a robust design (Pollock, 1982).
O’Donnell et al. (2015) developed a N-mixture model
specifically with terrestrial salamander populations in mind,
which expands on those versions previously cited by adding
estimation of temporary emigration probabilities in addition
to detection probabilities in the estimation of abundance.
Though considered the ‘‘gold standard’’ for estimating
survival rates, only a subset of published studies used
capture–recapture methods to estimate survival, and only a
few of these used a robust design (Pollock, 1982) to estimate
capture probability and temporary emigration. Thus, it is
imperative that future studies incorporate methods to
account for imperfect capture and estimate temporary
emigration to reduce bias in salamander survival estimates.
While accounting for temporary emigration is critical in
studies of terrestrial salamanders, the need to account for
permanent emigration may be negligible. Most methods for
modeling capture–recapture data, including those used in the
studies we encountered for this paper, cannot readily
separate true survival from site fidelity, and therefore the
methods generate estimates of apparent survival (Lebreton et
al., 1992; Sandercock, 2006) that can be biased low if site
fidelity is low. Traditional models of capture–recapture data
from migratory or otherwise highly mobile animal popula-
tions, for example, are inherently susceptible to this problem
(Rowat et al., 2008; V¨
ogeli et al., 2008; Stracey and Robinson,
2012). Over the last decade, models have been developed
that use the spatial data associated with mark–recapture
studies and the power of hierarchical Bayesian approaches to
make estimation of true survival possible (Gilroy et al., 2012;
Schaub and Royle, 2014). While these models are a big step
forward for the field in general, we suspect that estimates of
apparent survival are likely good approximations of true
survival for terrestrial salamanders as they are well known to
exhibit high site fidelity, the factor which can bias survival
estimates low if present and not accounted for.
Another likely reason for the large proportion of likely low-
biased published survival estimates was study duration.
Regular temporary emigration from the surface results in
low capture probabilities for salamanders (Bailey et al.,
2004a, 2004b). This increases the likelihood that animals
can go for extended periods without detection. Our analysis
found a positive relationship between study duration and
adult survival estimates. Most published survival estimates
were from studies of three years or less, and all but one
(Lindstr¨
om et al., 2010) were less than the generation time
for the focal species. We note that the relationship we
observed between study duration and estimated survival was
weak (Fig. 1A) and had a high degree of uncertainty,
potentially because some studies were reported from dis-
turbed sites or differed in methodology. Also, we assumed
that published survival rates were estimated from stable
populations and are not density dependent. If these
Howard and Maerz—Vital rates of Plethodontidae 935
assumptions are false, then it is possible that some published
rates that appear biased low may be reasonable. Additionally,
lower survival rates could be possible for a stable population
provided the immigration rate is sufficiently high. Very little
is known about dispersal or immigration rates among
plethodontines (e.g., Marsh et al., 2004), which is a key gap
in understanding local population dynamics and larger scale
source–sink or metapopulation dynamics for these species.
Further limiting the utility of the published survival rates
for projecting population growth was that only six studies
provided stage- or age-specific survival rates, while the
remaining nine studies estimated a single, population-wide
rate. Given the large size differences between hatchling,
juvenile, and adult salamanders within the Plethodontinae,
the assumption of constant survival across life stages seems
unrealistic. Smaller salamanders should be more sensitive to
weather-related mortality, predation, and competition (Feder,
1978, 1983; Hairston, 1987). Indeed, the few studies that
have used capture–recapture to estimate age-specific survival
all estimate increasing survival with age/body size (Marvin,
1996; Lee et al., 2012; Caruso and Rissler, 2018). We believe
that all future studies should be designed to estimate age,
stage, or size-specific vital rates in relation to weather and
other habitat covariates.
Our analysis examined the sensitivity of projected popu-
lation growth rate and the plausibility of survival estimates to
estimates of the annual probability of laying a clutch, the
probability of an egg hatching, and age at first reproduction
(Fig. 3). These rates are all challenging to estimate for
salamanders, yet any population projection will depend
strongly on these estimates. Estimating egg-hatch rate is
challenging because eggs are laid in locations that are
difficult if not impossible to observe naturally. Natural
clutches of eggs have not been observed for most species of
plethodontines. For studies that have observed clutches,
observations required high frequency intrusion on nesting
females in situ or the use of ex situ environments, both of
which may have altered hatch rates. Our analyses demon-
strate that a wide range of egg-hatching rates are plausible
across a reasonable range of adult and juvenile survival rates,
clutch frequencies, and ages at maturity (Fig. 3). Given the
latent nature of the egg stage for most species, using
alternative ways to estimate reproductive rates such as using
post-hatch estimates of adult to hatchling ratios may be
appropriate provided estimates of adult and hatchling
abundance are rigorous (Conroy and Carroll, 2009). Repro-
ductive rate estimates should not rely only on direct ratios of
observed counts but could be modeled from abundance
estimates using repeated counts (N-mixture models, Royle,
2004; Fiske and Chandler, 2011; Zipkin et al., 2014) or
capture–recapture data.
Though we found many estimates of age at maturity and
the annual probability that a female will lay a clutch (clutch
frequency), we caution that these two rates are seldom
directly estimated. We found no longitudinal study that
estimated the probability a female would lay a clutch in a
given year. This is likely a result of the low likelihood of
observing females in all years and the short duration of most
studies. Instead, most studies derive the probability of
reproduction by estimating the proportion of gravid and
non-gravid females in the population. This assumes that
gravid and non-gravid females have equal probabilities of
capture—something that is not estimated or evaluated in
most studies—and that the annual probability of laying a
clutch does not vary with age or size. Whether the
probability of reproduction varies with age or size could be
estimated, but it has not been in any published studies.
Similarly, age at maturity is not directly estimated, but it is
rather inferred from relationships between size at maturity
and estimated growth rates. Maturity in salamanders is size,
not age, dependent, and therefore, environmental factors
that affect growth are likely to drive variation in age at
maturity within and among populations. Converting size at
maturity to age at maturity depends on the rigor of growth
estimates from known-age animals, and few published
studies are of sufficient length for such estimates. Instead,
most estimates rely on inferring age from temporal size
distributions, which are inherently uncertain for salaman-
ders beyond age two. Because of the strong potential for
temporal and spatial variation in growth, we believe it is
likely that age at maturity and age at first clutch is highly
variable within and among populations and estimating that
variation will be important for more robust population
projection models.
A lesson illustrated by our analysis is the importance of
evaluating the plausibility of vital rate estimates and
thoroughly considering factors that may bias estimates. This
is a pervasive problem for many wildlife species that
transcends the terrestrial salamander literature (Heppell et
al., 2000). Incredible published estimates can muddy the
literature and lead to erroneous conclusions when applied to
models or other analyses. It is often beyond the scope of
subsequent studies to evaluate the reliability of all published
vital rates, especially when synthesizing large numbers of
studies and diverse suites of taxa (Heppell et al., 2000).
Therefore, there is greater responsibility for individuals to
assess the potential for bias in their vital rate estimates before
publishing. We found that only two studies of species in the
Plethodontinae had used a projection matrix to examine
whether their survival estimates were plausible for a stable
population, which their study population appeared to be
(Lindstr¨
om et al., 2010; Lee et al., 2012). Our analysis also
suggests that survival rate estimates may be more likely to be
biased low with shorter study duration. Currently, only one
published survival estimate for direct-developing plethodon-
tines comes from a study of longer than five years (Lindstr ¨
om
et al., 2010), which is around the female age of first
reproduction for many species and less than species’
generation times. Long-term studies are critical for under-
standing drivers of temporal variation in vital rates and
population dynamics. Recent reviews and syntheses have
emphasized the critical value of long-term population studies
(Reinke et al., 2019) and a need for more studies of
hierarchical landscape-scale patterns of demography to better
understand natural and anthropogenic effects on population
dynamics (Gurevitch et al., 2016). These papers also
acknowledge the obstacles to long-term studies including
short funding cycles and a priority placed on short-term
results and novelty over long-term understanding. Some
published survival estimates show adult salamander survival
may be reduced by 20–62% in disturbed habitats, usually
logging or forest clearing (Ash et al., 2003; Welsh et al., 2008;
Connette and Semlitsch, 2012). Other studies indicate that,
compared to juveniles, adult salamanders may be more
resilient to habitat disturbance (Ash et al., 2003) and drought
(Peterman and Semlitsch, 2014; Caruso and Rissler, 2018).
936 Ichthyology & Herpetology 109, No. 4, 2021
Aside from these few examples, it should be alarming that
even among an extensively studied group of animals, we lack
a most basic understanding of demography for nearly all
species. If confronted with an urgent need for conservation
action, we would struggle to develop rigorous population
models for any plethodontine to inform our actions.
In this review, we have shown that most existing survival
estimates seem implausible across a wide range of egg-hatch
rates, age at first reproduction, and annual probability of
female reproduction. Many survival estimates are likely
biased low due to less rigorous methodologies that do not
account for imperfect capture or temporary emigration, and
due to short study durations relative to age at first
reproduction that are exacerbated by low capture rates. In
the absence of direct estimates for population modeling
purposes, some vital rates such as age and size at maturity,
clutch size, and the annual probability of female reproduc-
tion may be reasonably predictable within and among
species based on size at maturity and/or latitude. Given the
multiple pressures facing terrestrial salamanders and other
wildlife, there is an obvious and eminent need for population
models to inform conservation, and the need for long-term
studies across a range of sites and species to generate
estimates of vital rates and how they vary in space and time.
DATA ACCESSIBILITY
Supplemental material is available at https://www.
ichthyologyandherpetology.org/h2020079. Unless an alter-
native copyright or statement noting that a figure is
reprinted from a previous source is noted in a figure caption,
the published images and illustrations in this article are
licensed by the American Society of Ichthyologists and
Herpetologists for use if the use includes a citation to the
original source (American Society of Ichthyologists and
Herpetologists, the DOI of the Ichthyology & Herpetology
article, and any individual image credits listed in the figure
caption) in accordance with the Creative Commons Attribu-
tion CC BY License.
LITERATURE CITED
Ash, A. N., R. C. Bruce, J. Castanet, and H. Francillon-
Vieillot. 2003. Population parameters of Plethodon metcalfi
on a 10-year-old clearcut and in nearby forest in the
southern Blue Ridge Mountains. Journal of Herpetology
37:445–452.
Bailey, L. L., T. R. Simons, and K. H. Pollock. 2004a.
Estimating detection probability parameters for Plethodon
salamanders using the robust capture–recapture design.
Journal of Wildlife Management 68:1–13.
Bailey, L. L., T. R. Simons, and K. H. Pollock. 2004b. Spatial
and temporal variation in detection probability of Pletho-
don salamanders using the robust capture–recapture de-
sign. Journal of Wildlife Management 68:14–24.
Barrett, K., and S. J. Price. 2014. Urbanization and stream
salamanders: a review, conservation options, and research
needs. Freshwater Science 33:927–940.
Bean, M. J. 2015. Injurious Wildlife Species: Listing Sala-
manders Due to Risk of Salamander Chytrid Fungus. Vol.
50 CFR Part 16. United States Fish and Wildlife Service.
Best, M. L., and H. H. Welsh. 2014. The trophic role of a
forest salamander: impacts on invertebrates, leaf litter
retention, and the humification process. Ecosphere 5:1–19.
Bruce, R. C. 2013. Size-mediated tradeoffs in life-history
traits in dusky salamanders. Copeia 2013:262–267.
Bull, J., and R. Shine. 1979. Iteroparous animals that skip
opportunities for reproduction. The American Naturalist
114:296–303.
Burton,T.M.,andG.E.Likens.1975. Salamander
populations and biomass in the Hubbard Brook Experi-
mental Forest, New Hampshire. Copeia 1975:541–546.
Caruso, N. M., and L. J. Rissler. 2018. Demographic
consequences of climate variation along an elevational
gradient for a montane terrestrial salamander. Population
Ecology 61:171–182.
Caswell, H. 2000. Prospective and retrospective perturbation
analyses: their roles in conservation biology. Ecology 81:
619–627.
Cecala, K. K., J. C. Maerz, J. Chamblee, J. F. Frisch, T. L.
Gragson, J. A. Hepinstall-Cymerman, D. S. Leigh, C. R.
Jackson, J. T. Peterson, and C. M. Pringle. 2018. Multiple
drivers, scales, and interactions influence southern Appa-
lachian stream salamander occupancy. Ecosphere 9:
e02150.
Clarivate Analytics. 2018. Web of Science: all databases.
https://apps.webofknowledge.com (accessed 1 March
2018).
Connette, G. M., and R. D. Semlitsch. 2012. Successful use
of a passive integrated transponder (PIT) system for below-
ground detection of plethodontid salamanders. Wildlife
Research 39:1–6.
Connette, G. M., and R. D. Semlitsch. 2015. A multistate
mark–recapture approach to estimating survival of PIT-
tagged salamanders following timber harvest. Journal of
Applied Ecology 52:1316–1324.
Conroy,M.J.,andJ.P.Carroll.2009. Quantitative
Conservation of Vertebrates. Wiley-Blackwell, Chichester,
U.K.
Davic, R. D., and H. H. Welsh. 2004. On the ecological roles
of salamanders. Annual Review of Ecology, Evolution, and
Systematics 35:405–434.
Feder, M. E. 1978. Environmental variability and thermal
acclimation in neotropical and temperate zone salaman-
ders. Physiological Zoology 51:7–16.
Feder, M. E. 1983. Integrating the ecology and physiology of
plethodontid salamanders. Herpetologica 39:291–310.
Fiske, I. J., and R. B. Chandler. 2011. unmarked: an R
package for fitting hierarchical models of wildlife occur-
rence and abundance. Journal of Statistical Software 43:1–
23.
Fraser, D. F. 1974. Interactions between salamanders of the
genus Plethodon in the central Appalachians. Unpubl.
Ph.D. diss., University of Maryland, College Park, Mary-
land.
Gadgil, M., and W. H. Bossert. 1970. Life historical
consequences of natural selection. The American Naturalist
104:1–24.
Gilroy, J. J., T. Virzi, R. L. Boulton, and J. L. Lockwood.
2012. A new approach to the ‘‘apparent survival’’ problem:
estimating true survival rates from mark–recapture studies.
Ecology 93:1509–1516.
Google Inc. 2017. Google Earth Pro, Google Inc., Mountain
View, California. https://www.google.com/earth/desktop/
Google Inc. 2018. Google Scholar. https://scholar.google.
com/ (accessed 1 March 2018).
Howard and Maerz—Vital rates of Plethodontidae 937
Gurevitch, J., G. A. Fox, N. L. Fowler, and C. H. Graham.
2016. Landscape demography: population change and its
drivers across spatial scales. The Quarterly Review of
Biology 91:460–485.
Hairston, N. G. 1983. Growth, survival and reproduction of
Plethodon jordani: trade-offs between selective pressures
Copeia 1983:1024–1035.
Hairston, N. G., Sr. 1987. Community Ecology and Sala-
mander Guilds. Cambridge University Press, Cambridge.
Heppell, S. S. 1998. Application of life-history theory and
population model analysis to turtle conservation. Copeia
1998:367–375.
Heppell, S. S., H. Caswell, and L. B. Crowder. 2000. Life
histories and elasticity patterns: perturbation analysis for
species with minimal demographic data. Ecology 81:654–
665.
Herrington, R. E. 1985. The ecology, reproductive biology
and management of the Larch Mountain salamander
(Plethodon larselli Burns) with comparisons to two other
sympatric Plethodons. Unpubl. Ph.D. diss., Washington
State University, Pullman, Washington.
Highton, R. 1956. The life history of the slimy salamander,
Plethodon glutinosus, in Florida. Copeia 1956:75–93.
Jobe, K. L., C. G. Monta˜
na, and C. M. Schalk. 2019.
Emergent patterns between salamander prey and their
predators. Food Webs 21:e001028.
Kniowski, A., and N. Reichenbach. 2009. The ecology of
the Peaks of Otter salamander (Plethodon hubrichti)in
sympatry with the eastern red-backed salamander (Pletho-
don cinereus). Herpetological Conservation and Biology 4:
285–294.
Lannoo, M. (Ed.). 2005. Amphibian Declines: The Conser-
vation Status of United States Species. University of
California Press, Berkeley and Los Angeles, California.
Lebreton, J. D., K. P. Burnham, J. Clobert, and D. R.
Anderson. 1992. Modeling survival and testing biological
hypotheses using marked animals: a unified approach with
case studies. Ecological Monographs 62:67–118.
Lee, D. E., J. B. Bettaso, M. L. Bond, R. W. Bradley, J. R.
Tietz, and P. M. Warzybok. 2012. Growth, age at maturity,
and age-specific survival of the arboreal salamander
(Aneides lugubris) on Southeast Farallon Island, California.
Journal of Herpetology 46:64–71.
Lindstr¨
om, J., R. Reeve, and S. Salvidio. 2010. Bayesian
salamanders: analysing the demography of an under-
ground population of the European plethodontid Speleo-
mantes strinatii with state-space modelling. BioMed Central
Ecology 10:4.
Lynch, J. E. 1984. Reproductive ecology of Plethodon idaho-
ensis. Unpubl. M.S. thesis, University of Idaho, Moscow,
Idaho.
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.
Mallakpour, I., and G. Villarini. 2017. Analysis of changes
in the magnitude, frequency, and seasonality of heavy
precipitation over the contiguous USA. Theoretical and
Applied Climatology 130:345–363.
Marsh, D. M., K. A. Thakur, K. C. Bulka, and L. B. Clarke.
2004. Dispersal and colonization through open fields by a
terrestrial, woodland salamander. Ecology 85:3396–3405.
Martel, A., A. Spitzen-van der Sluijs, M. Blooi, W. Bert, R.
Ducatelle, M. C. Fisher, A. Woeltjes, W. Bosman, K.
Chiers, F. Bossuyt, and F. Pasmans. 2013. Batrachochy-
trium salamandrivorans sp. nov. causes lethal chytridiomy-
cosis in amphibians. Proceedings of the National Academy
of Sciences of the United States of America 110:15325–
15329.
Marvin, G. A. 1996. Life history and population character-
istics of the salamander Plethodon kentucki with a review of
Plethodon life histories. American Midland Naturalist 136:
385–400.
Milanovich, J. R., W. E. Peterman, N. P. Nibbelink, and J.
C. Maerz. 2010. Projected loss of a salamander diversity
hotspot as a consequence of projected global climate
change. PLoS ONE 5:e12189.
Morris, W. F., and D. F. Doak. 2002. Quantitative Conser-
vation Biology: Theory and Practice of Population Viability
Analysis. Oxford University Press.
O’Donnell, K. M., F. R. Thompson, III, and R. D. Semlitsch.
2015. Partitioning detectability components in popula-
tions subject to within-season temporary emigration using
binomial mixture models. PLoS ONE 10:e0117216.
Olson, D. H., and M. R. Kluber. 2012. Plethodontid
salamander distributions in managed forest headwaters in
western Oregon, USA. Herpetological Conservation and
Biology 9:76–96.
Organ, J. A. 1961. Studies of the local distribution, life
history, and population dynamics of the salamander genus
Desmognathus in Virginia. Ecological Monographs 31:189–
220.
Otto, C. R. V., G. J. Roloff, and R. E. Thames. 2014.
Comparing population patterns to processes: abundance
and survival of a forest salamander following habitat
degradation. PLoS ONE 9:e93859.
Ovaska, K. 1987. Social behavior of the western red-backed
salamander, Plethodon vehiculum.Unpubl.Ph.D.diss.,
University of Victoria, Victoria, British Columbia.
Ovaska, K., and P. T. Gregory. 1989. Population structure,
growth, and reproduction in a Vancouver Island popula-
tion of the salamander Plethodon vehiculum. Herpetologica
45:133–143.
Peele, J., C. Nix, P. Ruhl, R. Chapman, P. Zollner, and M. R.
Saunders. 2017. Effects of woody biomass harvests on a
population of plethodontid salamanders in southeast
Indiana. American Midland Naturalist 178:132–143.
Peterman, W., and R. D. Semlitsch. 2014. Spatial variation
in water loss predicts terrestrial salamander distribution
and population dynamics. Oecologia 176:257–269.
Petranka, J. W. 1998. Salamanders of the United States and
Canada. Smithsonian Institution Press, Washington, D.C.
Pollock, K. H. 1982. A capture–recapture design robust to
unequal probability of capture. Journal of Wildlife Man-
agement 46:752–757.
Reinke, B. A., D. A. W. Miller, and F. J. Janzen. 2019. What
have long-term field studies taught us about population
dynamics? Annual Review of Ecology, Evolution, and
Systematics 50:261–278.
Rowat, D., C. W. Speed, M. G. Meekan, M. A. Gore, and C.
J. A. Bradshaw. 2008. Population abundance and apparent
survival of the vulnerable whale shark Rhincodon typus in
the Seychelles aggregation. Oryx 43:591–598.
938 Ichthyology & Herpetology 109, No. 4, 2021
Royle, J. A. 2004. N-mixture models for estimating popula-
tion size from spatially replicated counts. Biometrics 60:
108–115.
Salthe, S. N. 1969. Reproductive modes and the number and
sizes of ova in the Urodeles. American Midland Naturalist
81:467–490.
Salthe, S. N., and J. S. Mecham. 1974. Reproductive and
courtship patterns, p. 309–521. In: Physiology of the
Amphibia. Vol. II. B. Lofts (ed.). Academic Press, New York
and London.
Sandercock, B. K. 2006. Estimation of demographic param-
eters from live-encounter data: a summary review. Journal
of Wildlife Management 70:1504–1520.
Sayler, A. 1966. The reproductive ecology of the red-backed
salamander, Plethodon cinereus, in Maryland. Copeia 1966:
183–193.
Schaub, M., and J. A. Royle. 2014. Estimating true instead of
apparent survival using spatial Cormack-Jolly-Seber mod-
els. Methods in Ecology and Evolution 5:1316–1326.
Semlitsch, R. D., and C. A. West. 1983. Aspects of the life
history and ecology of Webster’s salamander, Plethodon
websteri. Copeia 1983:339–346.
Stearns, S. C. 1989. Trade-offs in life-history evolution.
Functional Ecology 3:259–268.
Stracey, C. M., and S. K. Robinson. 2012. Are urban habitats
ecological traps for a native songbird? Season-long pro-
ductivity, apparent survival, and site fidelity in urban and
rural habitats. Journal of Avian Biology 43:50–60.
Takahashi, M. K., and T. K. Pauley. 2010. Resource
allocation and life history traits of Plethodon cinereus at
different elevations. American Midland Naturalist 163:87–
94.
Taylor, S. J., J. K. Krejca, M. L. Niemiller, M. J. Dreslik, and
C. A. Phillips. 2015. Life history and demographic
differences between cave and surface populations of the
western slimy salamander, Plethodon albagula (Caudata:
Plethodontidae), in central Texas. Herpetological Conser-
vation and Biology 10:740–752.
V¨
ogeli, M., P. Laiolo, D. Serrano, and J. L. Tella. 2008. Who
are we sampling? Apparent survival differs between
methods in a secretive species. Oikos 117:1816–1823.
Wake, D. B. 2012. Taxonomy of salamanders of the family
Plethodontidae (Amphibia: Caudata). Zootaxa 3484:75–82.
Wells, K. D. 2007. The Ecology and Behavior of Amphibians.
The University of Chicago Press, Chicago and London.
Welsh, H. H., and A. J. Lind. 1992. Population ecology of
two relictual salamanders from the Klamath Mountains of
northwestern California, p. 419–437. In: Wildlife 2001:
Populations. D. R. McCullough and R. H. Barrett (eds.).
Elsevier Science Publishers Ltd., London.
Welsh, H. H., K. L. Pope, and C. A. Wheeler. 2008. Using
multiple metrics to assess the effects of forest succession on
population status: a comparative study of two terrestrial
salamanders in the US Pacific Northwest. Biological
Conservation 141:1149–1160.
Wiens, J. J., T. N. Engstrom, and P. T. Chippindale. 2006.
Rapid diversification, incomplete isolation, and the ‘‘spe-
ciation clock’’ in North American salamanders (genus
Plethodon): testing the hybrid swarm hypothesis of rapid
radiation. Evolution 60:2585–2603.
Winemiller, K. O., and K. A. Rose. 1992. Patterns of life-
history diversification in North American fishes: implica-
tions for population regulation. Canadian Journal of
Fisheries and Aquatic Sciences 49:2196–2218.
Zipkin, E. F., J. T. Thorson, K. See, H. J. Lynch, E. H. C.
Grant, Y. Kanno, R. B. Chandler, B. H. Letcher, and J. A.
Royle. 2014. Modeling structured population dynamics
using data from unmarked individuals. Ecology 95:22–29.
Howard and Maerz—Vital rates of Plethodontidae 939
