Received: 11 July 2022 Revised: 12 September 2022 Accepted: 15 September 2022

DOI: 10.1002/ecs2.4345

ARTICLE

Multistate model to estimate sex-specific dispersal rates

and distances for a wetland-breeding amphibian population

Courtney L. Davis 1,2,3 | David J. Muñoz 1,2 | Staci M. Amburgey 4,5 |

Carli R. Dinsmore 1 | Eric W. Teitsworth 6 | David A. W. Miller 1,2

1
Department of Ecosystem Science and
Management, Pennsylvania State
University, University Park,
Pennsylvania, USA
2
Intercollege Graduate Ecology Program,
Pennsylvania State University, University
Park, Pennsylvania, USA
3
Cornell Lab of Ornithology, Cornell
University, Ithaca, New York, USA
4
Washington Cooperative Fish and
Wildlife Research Unit, School of Aquatic
and Fishery Sciences, University of
Washington, Seattle, Washington, USA
5
Washington Department of Fish and
Wildlife, Olympia, Washington, USA
6
Department of Fisheries, Wildlife, and
Conservation Biology, North Carolina
State University, Raleigh,
North Carolina, USA
Correspondence
Courtney L. Davis
Email: cld74@cornell.edu
Handling Editor: George Middendorf
Abstract
How animals move across space and time in heterogeneous landscapes has
important implications for the conservation of imperiled and dispersal-limited
taxa, such as amphibians. Wetland-breeding amphibians are thought to exhibit
strong site fidelity, but there is growing evidence that many species are more
vagile than previously assumed. Few studies have quantified breeding dispersal
probabilities or distances while also accounting for observational uncertainty,
which means that resultant estimates could be biased or confounded with
sampling intensity and other demographic rates (e.g., site- and time-specific
detection and survival probabilities). Here, we analyze data from a 6-year
capture–mark–recapture study on adult spotted salamanders (Ambystoma
maculatum) conducted at 12 wetlands in central Pennsylvania to estimate popu-
lation dynamics and population structure at multiple scales. We used a multi-
state, hidden Markov estimator to quantify sex-specific site fidelity and
breeding dispersal as a function of Euclidean distance between wetlands
while accounting for imperfect detection. We estimated short-timescale
movements (i.e., those that occur within a single breeding season) and
longer timescale movements (i.e., those that occur among breeding seasons) to
determine if dispersal rates and distances differed. We found that interannual site
fidelity of males varied among wetlands and was positively associated with popu-
lation density. Females exhibited higher interannual site fidelity and dispersed
further than males between breeding seasons. Within breeding seasons, we found
that up to 6% of males dispersed to a new wetland each day. Our study is the first
to directly compare amphibian breeding dispersal probabilities and distances at
multiple scales and provides a robust framework for improving inference on the
spatial and temporal patterns of amphibian movement.

KEYWORDS
amphibian movement, hidden Markov model, multistate data, spotted salamanders,
stopover model

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided
the original work is properly cited.
© 2023 The Authors. Ecosphere published by Wiley Periodicals LLC on behalf of The Ecological Society of America.

Ecosphere. 2023;14:e4345. https://onlinelibrary.wiley.com/r/ecs2 1 of 15

https://doi.org/10.1002/ecs2.4345

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INTRODUCTION
Understanding spatial and temporal patterns of animal
movement is critical to predicting how species respond
to environmental change (Gaillard et al., 2010; Morales
et al., 2010; Schneider, 2001). Patterns of animal move-
ment are often complex, acting at multiple spatial and
temporal scales with important ecological and evolution-
ary consequences (Mueller & Fagan, 2008; Nathan et al.,
2008; Ravigné et al., 2009). In spatially structured
populations (i.e., systems of subpopulations occupying
discrete habitat patches that are connected by dispersing
individuals; Thomas & Kunin, 1999), the movement of
individuals between habitat patches contributes to local
colonization–extinction dynamics, buffers against the
effects of genetic drift, and increases gene flow between
subpopulations (Bowler & Benton, 2005). Dispersal rates
and distances can therefore have important implications
for long-term population persistence, particularly in the
face of rapid environmental changes and increased
stochasticity (Beever et al., 2016; Hoffmann & Sgro
, 2011;
Travis et al., 2013).
Dispersal occurs when an individual moves from its
patch of birth to its breeding patch (i.e., natal dispersal)
or among successive breeding patches (i.e., breeding
dispersal), potentially resulting in gene flow (Clobert
et al., 2009; Matthysen, 2012; Ronce, 2007). The process
of dispersal can be broken down into three stages
(Clobert et al., 2009; Matthysen, 2012): emigration
(i.e., departure from the patch), transience (i.e., the
movement within the landscape matrix between
patches), and immigration (i.e., arrival in the new
patch). Each of these stages can be influenced by the
individual’s phenotype (i.e., condition-dependent dis-
persal based on, e.g., sex, body size; Bonte et al., 2012;
Cote et al., 2017; Ronce & Clobert, 2012) and/or
environmental conditions (i.e., context-dependent dis-
persal; Bowler & Benton, 2005; Clobert et al., 2009;
Matthysen, 2012). Individuals may make their choice of
emigration and immigration according to social or
environmental factors that affect their fitness prospect
in a patch (Clobert et al., 2009). Factors such as conspe-
cific density (i.e., density-dependent dispersal), patch
size, and perceived quality of environment for offspring
are important determinates of emigration and immigra-
tion probabilities. Transience, and therefore the
intensity of dispersive flow among patches, can also be
affected by the distance between habitat patches and
the composition of the surrounding landscape matrix
(Baguette et al., 2013).
Dispersal is notoriously difficult to study in natural
systems because of the resource-intensive sampling
required to track individuals across space and time. This is
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DAVIS ET AL.
especially challenging when studying organisms with
complex life histories, such as wetland-breeding amphib-
ians (Cayuela, Valenzuela-S
anchez, et al., 2020). In the
case of amphibians, the movement of individuals between
spatially disjunct wetland habitats can help maintain
genetic diversity, increase local evolutionary potential, and
ensure population persistence through rescue effects
(Joly, 2019; Semlitsch, 2008). However, movement may
also increase extinction risk by facilitating the transmission
of virulent diseases, such as chytridiomycosis (Kolby
et al., 2015; Muths et al., 2018) and ranavirus (Tornabene
et al., 2018), and may erode local adaptation through “gene
swamping” (Lenormand, 2002; Tigano & Friesen, 2016).
Understanding amphibian dispersal is important for deter-
mining the spatial scale at which populations operate and
for designing effective disease and habitat management
strategies to combat recent species declines (Bailey &
Muths, 2019; Converse et al., 2017; Gerber et al., 2018;
Smith & Green, 2005).
Wetland-breeding amphibians are thought to exhibit
strong site fidelity (i.e., tendency to return to the same
breeding wetland year after year) because of the high phys-
iological and ecological costs (e.g., water loss, heat stress,
predation) associated with dispersal (Blaustein et al., 1994;
Sinsch, 1990). However, recent studies have shown that
there is considerable intra- and interspecific variation in
the probabilities, distances, and ecological correlates of dis-
persal events, particularly with regard to breeding dispersal
(i.e., the subsequent, unidirectional movement of individ-
uals between breeding wetland after first reproduction;
reviewed in Cayuela, Valenzuela-S
anchez, et al., 2020).
Breeding dispersal differs from other types of movement,
such as seasonal migration from terrestrial maintenance
habitats (i.e., where feeding, estivation, and overwintering
occur) to breeding wetlands, because these events can
directly contribute to gene flow among populations
(Semlitsch, 2008). Despite the ecological importance of
these movements, adult breeding dispersal remains one of
the least understood components of amphibian life history.
Most of the research conducted on breeding dispersal
in amphibians has focused on understanding the effects of
site-level heterogeneity on movement within a single spa-
tially structured population. Habitat characteristics such as
wetland hydroperiod can strongly influence site fidelity
and/or breeding dispersal (Cayuela, Valenzuela-S
anchez,
et al., 2020; Hamer et al., 2008; Measey, 2016; Tournier
et al., 2017). Conspecific density also plays an important
role for many species, where individuals tend to exhibit
higher site fidelity at wetlands with a high population den-
sity (Boualit et al., 2019; Cayuela et al., 2019; Denoël
et al., 2018; Gamble et al., 2007). Comparatively little
empirical work has been done to understand the effects
of individual-level factors (e.g., age, body size, sex) or

ECOSPHERE
landscape characteristics (e.g., spatial organization of
wetlands and other water bodies) on breeding dispersal
(reviewed in Cayuela, Valenzuela-S
anchez, et al., 2020).
However, several studies have shown that estimated dis-
persal kernels (i.e., the distribution of dispersal distances)
are often leptokurtic and right-skewed, with movement
probabilities decreasing as a function of distance between
breeding sites (Berven & Grudzien, 1990; Breden, 1987;
Cayuela, Besnard, et al., 2020; Gamble et al., 2007; Hendrix
et al., 2017; Peter, 2001; Trenham et al., 2001). The relation-
ship between dispersal probabilities and distance between
sites can have important implications for population con-
nectivity, especially in modified or fragmented landscapes
(Bailey & Muths, 2019).
Few studies have quantified breeding dispersal probabili-
ties or distances while also accounting for observational
uncertainty (Cayuela, Valenzuela-S
anchez, et al., 2020,
though see Cayuela et al., 2018; Denoël et al., 2018; Funk
et al., 2005; Grant et al., 2010). Site fidelity has been tradition-
ally estimated using homing, or displacement, experiments
to track the return of marked individuals to a single breeding
site (e.g., Gill, 1979; Shoop, 1968; Whitford & Vinegar, 1966).
More recently, multiyear sampling efforts have expanded to
track individuals at more than two breeding wetlands,
although inference about movement has been based on the
number of individuals captured at each site. Imperfect detec-
tion is not explicitly accounted for in these studies, meaning
that dispersal is likely confounded with survival and/or
capture probabilities (Bailey & Muths, 2019; Cayuela,
Valenzuela-S
anchez, et al., 2020; Kendall & Nichols, 2002).
Estimated dispersal kernels may also be biased or limited by
the spatial extent of a study area (Bailey & Muths, 2019;
Cayuela, Valenzuela-S
anchez, et al., 2020). A variety of
demographic and genetic methods have been proposed
to overcome these limitations (Cayuela et al., 2018),
including multistate capture–mark–recapture frameworks
that explicitly disentangle movement, survival, and cap-
ture probabilities (Arnason, 1973; Brownie et al., 1993;
Nichols & Kendall, 1995).
Our purpose is threefold: (1) to estimate survival,
abundance, and movement of the spotted salamander
(Ambystoma maculatum Shaw, 1802), while accounting
for observational uncertainty; (2) to estimate breeding
dispersal distances both within and among years, and;
(3) to estimate the effects of sex, habitat characteristics,
and population density on site fidelity. More specifically,
we aim to test the hypotheses that movement is
negatively related to the Euclidean distance between
wetlands, and that conspecific density and wetland
hydroperiod are positively associated with site fidelity
within and among years. To do this, we analyze data
from a 6-year capture–mark–recapture study conducted
at 12 wetlands in central Pennsylvania. We quantify
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3 of 15
inter- and intra-annual site fidelity, breeding dispersal
probabilities as a function of distance between wetlands,
abundance, and annual survival using a multistate,
hidden Markov estimator (modified from Worthington
et al., 2019). Our study improves our understanding of
amphibian population structure and provides a powerful
tool for disentangling multiple population processes that
are necessary for improving inference on the spatial and
temporal aspects of amphibian movement.
METHODS
Study species
The spotted salamander is a common, widespread species
that inhabits lowland deciduous forests throughout east-
ern North America (Petranka, 1998). Adults are rarely
observed outside of their spring breeding season when
they migrate in large numbers from upland habitats to
seasonally inundated wetlands (Sexton et al., 1990;
Shoop, 1968). Annual sex ratios throughout the breeding
season are typically male-biased because females fre-
quently skip years between breeding efforts, arrive later
in the breeding season, and are less abundant (Davis
et al., 2018; Husting, 1965; Patrick et al., 2008; Sexton
et al., 1990; Whitford & Vinegar, 1966). The length of the
breeding season varies by population and depends
heavily on local environmental conditions, although this
species is commonly found in breeding wetlands for only
1–3 weeks following seasonal migration (Husting, 1965;
Semlitsch, 1998). During this short time period, however,
large numbers of adults can be easily observed in wet-
lands and individually identified using their unique dor-
sal spot patterns (Chase et al., 2015). Historical homing
experiments and more recent studies on population
genetic structure (e.g., Zamudio & Wieczorek, 2007) have
suggested that spotted salamander adults tend to exhibit
high site fidelity (Husting, 1965; Whitford & Vinegar,
1966), have limited dispersal abilities (Madison, 1997), and
do not generally move between wetlands during the breed-
ing season (Semlitsch, 1998). Recorded seasonal migration
distances of the spotted salamander have ranged from
0 to 0.430 km (McDonough & Paton, 2007; Semlitsch &
Bodie, 2003), with some evidence that females may
travel nearly twice as far as males (e.g., McDonough &
Paton, 2007; Regosin et al., 2003).
Study site and data collection
We captured, marked, and recaptured adult spotted sala-
manders at 3 temporary wetlands in central Pennsylvania

4 of 15
in 2014 and expanded to include 9 additional wetlands for
a total of 12 from 2015 to 2019 (Figure 1; Appendix S1).
Sites ranged in mean size from 120.2 to 1170.5 m2 and var-
ied in mean hydroperiod (i.e., length of inundation) from
43 to 123 days (from start of spring amphibian breeding
season through larval development and metamorphosis).
These 12 wetlands were spatially organized into three clus-
ters where the mean distance between all sites in a cluster
was approximately 0.078 km (Figure 1). This wetland
network included eight additional sites where we did not
conduct capture–mark–recapture (location and size noted
in Figure 1). Based on egg mass surveys, spotted salaman-
ders have been observed breeding in seven of these eight
sites.
We deployed minnow traps (Grayson et al., 2011;
Piovia-Scott et al., 2011) at our 12 monitored wetlands
from the onset of spring thaw until our capture rates
declined to <5% of the captures achieved at peak migra-
tion (Davis et al., 2018). The number of capture days var-
ied each year for a total number of: 6 days in 2014,
15 days in 2015, 17 days in 2016, 15 days in 2017, 21 days
in 2018, and 10 days in 2019. The number of traps
deployed at each site also varied according to wetland
size and ranged from 4 to 12 traps, with a total of 89 min-
now traps across all 12 sites. We anchored traps at 10-m
F I G U R E 1 Geographic location and mean area (in square
meters) of individual wetlands within the study area in central
Pennsylvania, USA. Circles numbered 1–12 indicate wetlands
surveyed using capture–mark–recapture (CMR), whereas white
triangles indicate the wetlands within this network that were not
surveyed. Surveyed wetlands are broken up into three wetland
clusters: cluster A, cluster B, and cluster C.
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DAVIS ET AL.
intervals along the wetland perimeter and baited the
traps with 15.25-cm green glow sticks to increase capture
probabilities (Antonishak et al., 2017). We checked all
traps daily and subsequently released processed animals
at their location of capture.
We used a combination of visual implant elastomer
(VIE; Northwest Marine Technology, Shaw Island, WA,
USA) and spot pattern recognition software to identify
and track individuals through time and space. Salamanders
were first given a “batch code” using VIE that corresponded
to the site and year of first capture. This allowed us to iden-
tify recaptured individuals in the field and minimize the
probability that animals were misidentified as new individ-
uals by the pattern recognition software (Davis et al., 2018;
Stevick et al., 2001). Mismatches can create “ghost” individ-
uals and movement events leading to substantial bias in
estimates of survival (Tucker et al., 2019) and movement,
respectively. We standardized photographs in the field
using a consistent processing station that maintained the
angle and distance of the camera from the individual (Davis
et al., 2018). We then used the Interactive Individual
Identification Software (I3S; Hartog & Reigns, 2014) to
identify individuals using their unique dorsal spot patterns.
We manually verified all matches; when a recaptured indi-
vidual was not positively matched in the first 100 options
provided by I3S, we manually searched the photograph
database for photos corresponding to the observed VIE
batch mark. If a photograph was not positively matched
manually, then it was recorded as an “unknown” individual
and left out of this analysis (0.4% of all photographs).
We were also interested in testing specific hypotheses
about the influence of conspecific density and wetland
hydroperiod on site fidelity. We used egg mass density
(number of egg masses per unit area) as a proxy for
conspecific density at each site. Following adult emigration
from breeding wetlands, we conducted annual visual
encounter surveys to count the number of spotted salaman-
der egg masses at each of the 12 sites. We averaged egg mass
densities across all years to calculate site-specific estimates
of population density. At the time of these surveys, we also
instrumented wetlands with an iButton Temp Logger
(#DS1921G-F5; Embedded Data Systems, LLC) that we then
used to estimate mean wetland hydroperiod (Earl &
Semlitsch, 2015). We standardized estimates of conspecific
density and wetland hydroperiod to have a mean of 0 and a
standard deviation of 1 across all sites.
Hidden Markov modeling framework
We extended the multistate multiperiod stopover model,
developed by Worthington et al. (2019), to estimate
sex-specific breeding site fidelity, dispersal distances,
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ECOSPHERE 5 of 15

survival, recruitment, abundance, and capture probabil-
ities (Table 1). Because individual salamanders may
only be available for capture (i.e., in a wetland) for a
short period of time during the breeding season, we also
estimated probabilities associated with the arrival and
retention of individuals during the breeding season
(Table 1). We estimated all parameters for each sex sep-
arately by building independent models for males and
females. While the general approach was similar for
both sexes, we considered several modifications to the
overall model structure that allowed us to account for
behavioral differences between males and females. We
first provide an overview of the framework using the
model structure implemented for males and then
describe the modifications made to this structure to esti-
mate female-specific parameters.
Our model consisted of two Markovian multistate
transition processes and followed the convention of robust
design capture–mark–recapture models (Pollock, 1982).
The first was used to estimate movements among wetlands
between primary sampling periods (i.e., from year t to
year t + 1). The second was used to estimate daily move-
ment rates among wetlands between secondary capture
occasions (i.e., from day k to k + 1) within each primary
period. Thus, we were able to simultaneously estimate
short-timescale movements that occur within a single
breeding season and longer timescale movements among
breeding seasons to determine if rates and distances dif-
fered between the two. Unlike the closed robust design
model (Kendall et al., 1995; Pollock, 1982), our framework
assumes an open population both between and within pri-
mary periods. The complete model allowed us to account

TABLE 1 Parameters for the multistate multiperiod stopover model.

Parameter Description
N Total population size: No. observed (n) and unobserved (nm ) individuals that visit the study area for at least one capture
occasion during the study period.
pt Capture: Probability an individual is captured during one of the k occasions in primary period t.
rt Recruitment: Probability an individual is recruited into the population and is first available for capture in primary period
P
t. An individual must visit a study site during at least one primary period, so Tt¼1 r t ¼ 1. The conditional probability
of being recruited in primary period t, given that the individual was not recruited in any of the previous primary
P
periods is calculated as r t ¼ r t = Tj¼t r j for t = 1, …, T.
s Survival: Probability an individual is available for capture in primary period t + 1, given that they were available for
capture in primary period t.
βt,k Arrival: Probability an individual arrives at a study site and is first available for capture on occasion k within primary
period t, given that the individual is in the population and available for capture in primary period t. Within each
P t
primary period, Kk¼1 βt,k ¼ 1. The conditional probability of arriving at a site on occasion k within primary period t,
P t
given that the individual did not arrive on a previous occasion is calculated as βt,k ¼ βt,k = Kj¼k βj,k for k = 2, …, K t and
t = 1, …, T.
ϕt,k Retention: Probability an individual is available for capture on occasion k + 1 in primary period t, given that it was
available for capture on occasion k in primary period t. Within each primary period, ϕt,k must be 1 on occasion 1. The
conditional probability of staying at a site on occasion k within primary period t, given that the individual did not
P t
leave on a previous occasion is calculated as ϕt,k ¼ ϕt,k = Kj¼k ϕt,k for k = 2, …, K t and t = 1, …, T.
aj Initial discrete states: Probability of being at site j on the first occasion an individual is available for capture.
δBj Interannual site fidelity: Probability an individual returned to site j between two consecutive primary periods.

δW
j
Intra-annual site fidelity: Probability an individual remained at site j between two consecutive capture occasions within
primary period t.
σB Interannual dispersal: Scale parameter governing distance moved, given that an individual does not exhibit site fidelity
between consecutive primary periods.
σW Intra-annual dispersal: Scale parameter governing distance moved, given that an individual does not exhibit site fidelity
between consecutive occasions in primary period t.
ω0 Breeding: Probability a female was not available for capture in primary period t + 1, given that the female was not
available for capture in primary period t and survived to period t + 1. Female is assumed to have skipped breeding in
t and t + 1.
ω00 Skipped breeding: Probability a female was not available for capture in primary period t + 1, given that the female was
available for capture in primary period t and survived to period t + 1. Female is assumed to have skipped breeding in
t + 1 after breeding in t.
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6 of 15 DAVIS ET AL.

for the annual breeding dynamics in this population, such the rate of decay in interannual dispersal probability as a
as differences in the arrival and departure of individuals at function of distance. All pairwise dispersal probabilities
wetlands throughout the breeding season, as well as move- for each of the M sites (where j ≠ m) were re-weighted
ment between observable states (i.e., breeding wetlands) at so that:
two different scales. We estimate a superpopulation of
N individuals across all sampling periods that include both   .X
M

observed (n) and unobserved (nm ) individuals (Schwarz & ψBj,m ¼ 1  δBj  dBj,m dBj,m :
m¼1
Arnason, 1996; Worthington et al., 2019).
In the primary level of the model (i.e., each year), we This constrained the sum of the probabilities of dispers-
included a total of 14 hidden states, ht , where: ing to each of the wetlands to equal 1.
We estimated transitions between the 14 hidden
8 states in the primary level as follows:
> 1 not yet recruited into the breeding population
>
>
>
> 2 recruited into the breeding population and at site 1
>
>
>
> 2 3
<3 recruited into the breeding population and at site 2 1  r t r t α1 r t α2 r t α3   0
ht,k ¼ . : 6 0
>
> .. ..
. 6 sψB1,1 sψB1,2 sψB1,3   1  s 7
7
>
> 6 7
>
> 6
>
>
> 13 recruited into the breeding population and at site 12 ΓBt ¼ 6 0 sψB2,1 sψB2,2 sψB2,3   1  s 7
7,
: 6 7
14 departed from population ðdead or emigratedÞ 6 .. .. .. .. .. .. 7
4 . . . . . . 5
The primary level of the model captured three distinct 0 0 0 0   1
processes: (1) recruitment into the breeding population;
(2) survival between primary periods and; (3) interannual where aj represents the probability that an individual
movement among the 12 wetlands. We defined recruit- was at site j on the first occasion it was available for cap-
ment, r t , as the probability an individual was first ture. We assumed these discrete state transition probabil-
recruited into the breeding population and available for ities were constant among primary periods.
P
capture in primary period t, and constrained Tt¼1 r t ¼ 1. In the secondary level of the model (i.e., within each
Thus, every individual in the population must have vis- year), we included a total of 14 hidden states, ht,k , where:
ited a study site during at least one primary period. The 8
hidden Markov model formulation required the use >
> 1 not yet available for capture ðnot arrived at a breeding siteÞ
>2
>
of conditional recruitment probabilities (Worthington >
> available for capture in primary period t and site 1
>
<3 available for capture in primary period t and site 2
et al., 2019), which we defined as the probability an indi- ht, k ¼ . .. :
>
> .. .
vidual was recruited in primary period t, given that the >
>
>
> 13 available for capture in primary period t and site 12
>
:
individual was not recruited in any of the previous pri- 14 departed from breeding site in primary period t
P
mary periods: r t ¼ r t = Tj¼t r j for t = 1, …, T. We defined
survival, s, as the probability an individual was available The secondary level of the model also captured three dis-
for capture in primary period t + 1, given that they were tinct processes: (1) arrival at a breeding site; (2) retention
available in primary period t. For simplicity, we assumed between capture occasions; and (3) movement between
a constant survival probability between primary periods. capture occasions. We defined arrival, βt,k , as the proba-
The transition matrix, ψB , described between-year bility an individual arrived at a study site and was first
movement among the 12 observable states (i.e., wetlands). available for capture on occasion k within primary period
We estimated probabilities within this transition matrix t, given that the individual was in the population and
using a two-step approach. We first estimated interannual available for capture in primary period t. Within each pri-
PKt
site fidelity, δBj , or the probability an individual returned mary period, k¼1 βt,k ¼ 1. The hidden Markov model
to site j between two consecutive primary periods. Second, formulation also required conditional arrival probabilities
we estimated the probability an individual dispersed from (i.e., probability an individual arrives at a site on occasion
site j, conditional on 1  δBj . We used a Gaussian kernel k within primary period t, given that the individual
(Fujiwara et al., 2006) to describe the pairwise probabili- did not arrive on a previous occasion; Worthington
P t
ties of an individual dispersing from site j to site m: et al., 2019), where βt,k ¼ βt,k = Kj¼k βj,k for k = 2, …, K t
  and t = 1, …, T. We defined retention, ϕt,k , as the proba-
2
dBj,m ¼ exp x 2j,m =2σB , bility an individual was available for capture on occasion
k + 1 in primary period t, given that it was available
where x j,m is the Euclidean distance between site j and for capture on occasion k in primary period t. Within
site m, and σB is the scale parameter that determines each primary period, ϕt,k must be 1 on occasion 1. Again,

ECOSPHERE
we calculated conditional retention probabilities as
P t
ϕt,k ¼ ϕt,k = Kj¼k ϕt,k for k = 2, …, K t and t = 1, …, T.
We fitted a logistic regression with capture occasion in
each primary period as the explanatory variable to estimate
arrival and retention probabilities, rather than estimating
probabilities for each occasion separately (Worthington
et al., 2019). We assumed that the intercepts were constant
across years but the slopes varied between years for both
arrival and retention probabilities.
The transition matrix, ψW , described within-year
movement among the 12 observable states (i.e., wet-
lands). Probabilities within this transition matrix were
estimated using the same two-step approach described
above. We first estimated intra-annual site fidelity, δW j , as
the probability an individual stayed at site j between two
consecutive capture occasions. We took the inverse of
this (i.e., 1  δW
j ) to model the daily probability of an indi-
vidual dispersed from site j as a function of distance. We
again used a Gaussian kernel to describe the pairwise
probabilities of dispersing from site j to site m, where σW
is the scale parameter that determines the rate of decay
in intra-annual dispersal probability as a function of dis-
tance. All pairwise dispersal probabilities for each of the
M sites (where j ≠ m) were then re-weighted to sum to 1,
as shown above.
Transitions between the 14 hidden states of the sec-
ondary level were estimated as follows:
2 3
1  βt, k βt, k α1 βt, k α2 βt, k α3  
6 7
6 0 ϕt, k ψ1W, 1 ϕt, k ψ1W, 2 ϕt, k ψ1W, 3   1-ϕt, k 7
6 7
6 ϕt, k ψ2W, 1 ϕt, k ψ2W, 2 ϕt, k ψ2W, 3   1-ϕt, k 7
Γt , k ¼ 6
W
6
0 7:
6 .. .. .. .. ..
6 . . . . .
4 5
0 0 0 0  
We assumed that the proportion of individuals recruited
into each state (aj ) also reflected the proportion of indi-
viduals in the population that migrated to wetland j in
each primary period.
The last component of this model describes the obser-
vation process, which relates the probability of observing
individuals on a given day and location to the unobserved
state of the animal as described above (see Worthington
et al., 2019 for model likelihood and derivation). We esti-
mated daily capture probabilities, pt , that varied by year
but did not vary by occasion or state.
For females, which frequently skip years between
breeding efforts (e.g., Husting, 1965), we incorporated an
unobservable “skipped breeding” state into the primary
level of the model. We defined ω0 as the probability that
females skipped breeding in primary period t + 1 after
not breeding in primary period t, and ω00 as the probabil-
ity that a female skipped breeding in primary period t + 1
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7 of 15
after breeding in t (Table 1). A full description of the
methods for this analysis can be found in Appendix S2.
Due to a low number of female recaptures, we also fixed
site fidelity to be constant among years and simplified the
secondary level of the model structure to have just three
hidden states, where:
8
>
> 1 not yet available for capture ðnot arrived at a breeding siteÞ
>
>
<
ht,k ¼ 2 available for capture in primary period t :
>
>
>
>
:
3 departed from breeding site in primary period t
Therefore, we were not able to estimate intra-annual site
fidelity or dispersal probabilities for females. This simpli-
fied the intra-annual transition matrix, to:
2 3
1  βt,k βt,k 0
6 7
t,k ¼ 4
rW 0 ϕt,k 1  ϕt,k 5:
0 0 1
We estimated all parameters using the nonlinear minimi-
zation function (nlm) in R (version 3.6.0, R Core
Team, 2019). We used a nonparametric bootstrap (n = 50
bootstraps) that resampled individual encounter histories
to estimate standard errors and derived 95% CIs from
those standard error estimates. Finally, we used a regres-
sion approach to test the effects of conspecific density
and wetland hydroperiod on estimated between- and
0 intra-annual site fidelity.
7 RESULTS
.. 7
. 7
From 2014 to 2019, we recorded 15,249 capture occasions
1
of 3,627 unique males and 1132 unique females across
our 12 study sites. Approximately 64% of all captures
occurred at just 2 of the 12 sites (sites 1 and 4 in Figure 1;
Appendix S3). We also observed male-biased recapture
rates, with 72% of males but only 30% of females captured
on more than one occasion (Appendix S3).
The estimated total population of salamanders that vis-
ited any of the 12 sites during the study period was esti-
mated to be N b ½95%CI ¼ 4396 ½4290, 4502 males and
b
N ¼ 2885 ½2559, 3210 females. Estimated daily capture
probabilities were higher for males than females, ranging
among years from b pt ¼ 0:10 ½0:07, 0:13 to 0:29 ½0:27, 0:30
for males and 0.02 [0.01, 0.03] to 0.09 [0.03, 0.15] for
females (Table 2). We also found evidence that females
skip years between consecutive breeding events but are
not likely to skip more than 1 year in a row. That is, the
probability a female was not available for capture in pri-
mary period t + 1, given that it was available for capture
in primary period t and survived to t + 1, ω b 00 ¼
0:47 ½0:32, 0:61. The probability a female was not
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8 of 15 DAVIS ET AL.

T A B L E 2 Estimated means and 95% bootstrap CIs for daily

capture probabilities of male and female spotted salamanders. High-Probability
Daily capture probability

Males Females
Year bt [95% CI]
p bt [95% CI]
p
2014 0.10 [0.07, 0.13] 0.09 [0.03, 0.15]
2015 0.10 [0.09, 0.11] 0.04 [0.03, 0.05]
2016 0.29 [0.27, 0.30] 0.04 [0.03, 0.05]
2017 0.28 [0.26, 0.29] 0.03 [0.02, 0.04]
2018 0.06 [0.05, 0.06] 0.03 [0.02, 0.03]
2019 0.13 [0.12, 0.14] 0.02 [0.01, 0.03]

available for capture in primary period t + 1, given that

the female was not available for capture in primary
period t and survived to primary period (t + 1, ω b0 ¼ Low-Probability

0:01 ½0:00, 0:01). We estimated high survival probabilities

for both sexes (bs ¼ 0:76 ½0:75, 0:77 for males and
bs ¼ 0:81 ½0:74, 0:87 for females).
Recruitment into the breeding population was relatively
consistent throughout the study period (Appendix S4:
Figure S1a). Approximately 62% of males and 71% of females
were initially recruited into the population at either site 1
or site 4 (Appendix S4: Figure S1b). The rest of the popula-
tion was evenly split between the other two clusters
(Appendix S4: Figure S1b). In most years, males migrated to
breeding wetlands before females and continued to arrive
throughout the breeding season (Appendix S4: Figure S2a).
Females generally arrived in synchrony and over a short
period of time (i.e., overnight; Appendix S4: Figure S2a).
Females also stayed in breeding wetlands after males left
and may have remained in wetlands even after our sampling
concluded (Appendix S4: Figure S2b).
F I G U R E 2 Mean estimates for interannual site fidelity and
Interannual site fidelity, the probability an individual did movement of males, broken into (a) high (0.05–0.30) and (b) low
not move to a new wetland between years, ranged among (0.00–0.05) probability movements. High-probability dispersal
wetlands from ψ b i,i ¼ 0:24 ½0:13, 0:34 to 0:93 ½0:92, 0:94 for events were restricted to within-cluster movements, but we did
B
males (δ ¼ 0:69, SD = 0.21; Figure 2). We found that estimate low probabilities of movement between all three clusters.
interannual site fidelity was not strongly associated with Note that we only show patterns in wetland connectivity for
longer wetland hydroperiod (b x ¼ 0:12 ½0:01, 0:22, p low-probability movements; directionality of these movements is
value = 0.07, α-level 0.05), but was positively associated not shown to improve clarity.
(p value = 0.006, α-level 0.05) with conspecific density
x ¼ 0:15 ½0:07, 0:24; Table 3). We estimated high rates of
(b
interannual movement, particularly between wetlands in movements were restricted to wetlands within cluster A.
the same cluster (Figure 2). We also found evidence of However, females had a low probability of moving
directionality in movement patterns (Appendix S5). For within and between all three wetland clusters
example, males in cluster A were more likely to move (Figure 3b). There were no clear patterns in directional-
from site 2, a low-density short hydroperiod wetland, to ity of these breeding dispersal events. Instead, we esti-
site 4, a high-density long hydroperiod wetland, than vice mated reciprocal movement probabilities between
versa. wetlands (Appendix S5).
Female site fidelity was estimated at a constant rate Males exhibited high intra-annual site fidelity, the
B
b
(δ ¼ 0:84 ½0:79, 0:88), with approximately 16% of indi- probability an individual did not move to a new wetland
viduals moving to a different wetland between consecu- between consecutive capture occasions, which ranged
tive breeding seasons (Figure 3). High-probability among wetlands from 0.94 [0.91, 0.97] to 1.00 [0.99, 1.00]
 21508925, 2023, 1, Downloaded from https://esajournals.onlinelibrary.wiley.com/doi/10.1002/ecs2.4345 by CAPES, Wiley Online Library on [06/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
ECOSPHERE 9 of 15

T A B L E 3 Estimated regression coefficients (mean and 95% CI)

for the effects of wetland hydroperiod and conspecific density on High-Probability
interannual and intra-annual site fidelity of male spotted
salamanders.

Wetland Conspecific
Coefficient hydroperiod density
Interannual site fidelity
Intercept 0.69 [0.59, 0.80] 0.69 [0.61, 0.78]
Slope 0.12 [0.01, 0.22] 0.15 [0.07, 0.24]*
Intra-annual site fidelity
Intercept 0.98 [0.97, 0.99] 0.98 [0.98, 0.99]
Slope 0.00 [0.00, 0.01] 0.01 [0.00, 0.02]

Note: We were not able to estimate the effect of wetland hydroperiod and
conspecific density on females because we fixed site fidelity to be constant
across sites. Values in boldface indicate a significant relationship assuming
an α level of 0.05. Low-Probability
*p = 0.006.

(Figure 4). Intra-annual site fidelity was not strongly associ-

ated with wetland hydroperiod (b x ¼ 0:00 ½0:00, 0:01) or
conspecific density (b x ¼ 0:01 ½0:00, 0:02; Table 3).
Estimated movement probabilities were highest in cluster
A, with males preferentially moving to site 1 or site 4
(Appendix S5). Movement between clusters was limited
but occurred at low probabilities between cluster B and
cluster C (Figure 4b).
Finally, we found that females were more likely to
move longer distances than males (b σB ¼ 0:117 km [0.110,
0.124] and 0.150 km [0.134, 0.165] for males and females,
respectively; Figure 5). Approximately 95% of interannual
dispersal events occurred within 0.229 km for males and
0.294 km for females. Intra-annual dispersal of males
occurred over shorter distances than interannual events, F I G U R E 3 Mean estimates for interannual site fidelity and
on average (b σW ¼ 0:088 km [0.057, 0.119]; Figure 5), with movement of females, broken into (a) high (0.05–0.30) and (b) low
95% of intra-annual dispersal events occurring within (less than 0.05) probability movements. High-probability
0.172 km of a particular wetland. movements were restricted to cluster A. However, females had a
low probability of moving within and between all three wetland
clusters. Note that we only show patterns in wetland connectivity
DISC USS I ON for low-probability movements; directionality of these movements
is not shown to improve clarity.

Environmental change will influence species–environment

interactions by altering patterns of animal movement,
such as dispersal (Travis et al., 2013). Understanding a
species’ ability and tendency to move across the
landscape is critical for the development of effective
conservation measures that ensure functional connec-
tivity and maintain or improve population resilience,
particularly for dispersal-limited taxa such as amphib-
ians (Cayuela, Valenzuela-S
anchez, et al., 2020; Joly,
2019; Semlitsch, 2008). Our study provides novel
insights into amphibian population dynamics and struc-
ture, with a specific focus on estimating adult breeding
dispersal at multiple scales. By accounting for observa-
tional uncertainty, we were able to disentangle impor-
tant population processes, including survival, breeding
frequency, and movement.
General insights into spotted salamander
population dynamics and structure
Our study builds on previous knowledge of spotted sala-
mander life history and population dynamics. We found

10 of 15
High-Probability
Low-Probability
F I G U R E 4 Mean estimates for intra-annual site fidelity and
daily movement probabilities of males, broken into (a) high
(0.005–0.025) and (b) low (less than 0.005) probability movements.
High-probability movements were restricted to movement between
wetlands in a cluster. Movement was highest in cluster A, with
males generally moving to site 1 or site 4.
a male-biased sex ratio of 1.5:1 that is consistent with
other studies on spotted salamanders (e.g., Blackwell
et al., 2004; Homan et al., 2018) and is likely due to males
being recruited into the breeding population at a younger
age than females. We estimated higher mean survival
probabilities for females than for males, although the
bootstrap CIs for these estimates did overlap. Our esti-
mates of survival are similar to those reported in other
studies, which range from 0.60 to 1.00 (Blackwell
et al., 2004; Douglas & Monroe, 1981; Homan et al., 2018;
Husting, 1965), but are likely underestimated for both
sexes. In our study system, survival could be confounded
with permanent movement to any of the other,
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DAVIS ET AL.
F I G U R E 5 Estimated mean and 95% bootstrap CIs for
interannual movement of males and females, as well as
intra-annual movement of males. Females were more likely to
move longer distances than males, and intra-annual dispersal of
males occurred over shorter distances than interannual events, on
average.
unmonitored wetlands and emigration from the study
area (e.g., Schmidt et al., 2007). This is particularly true
for females, which are notoriously difficult to capture
because they are only present in breeding wetlands for a
short period of time (Davis et al., 2018; Husting, 1965;
Patrick et al., 2008; Sexton et al., 1990; Whitford &
Vinegar, 1966). By explicitly accounting for annual differ-
ences in arrival and retention of females during the
breeding season, however, we were able to more precisely
estimate female capture probabilities as well as survival,
abundance, movement, and breeding frequency.
Effect of sex on site fidelity and dispersal
distance
We demonstrate that site fidelity and dispersal distances
differ within and among breeding seasons and between
sexes. Females had a higher interannual site fidelity than
males and moved further distances than males between
years. While we were unable to make inference about
the specific factors influencing intra-annual site fidelity
and dispersal distances of females, we found that up to
6% of males disperse to new wetlands each day. We also
found that males moved shorter distances within years
than between years. Most of the movement occurred
within a cluster of wetlands (i.e., among wetlands spaced

ECOSPHERE
0.035–0.143 km from each other), which stands in
stark contrast to the high connectivity between clusters
that we observed between years (i.e., movements of
>0.300 km). Unfortunately, we were unable to estimate
intra-annual breeding dispersal distances of females due
to low recapture rates within breeding seasons. However,
it is likely that the high physiological and ecological
costs associated with breeding (Strickland et al., 2015)
prohibit female movement between wetlands, particu-
larly those located in different clusters, within a breeding
season. Of the 339 females we recaptured over the study
period, we only observed 10 within-year movement
events.
Effect of population density and wetland
hydroperiod on site fidelity of males
We found that interannual site fidelity of males was
positively associated with population density. Higher
population density is likely correlated with higher
breeding success in more stable habitats (e.g., Cayuela
et al., 2019; Gamble et al., 2007; James et al., 2015),
though we did not find a strong relationship between
interannual site fidelity and wetland hydroperiod.
We also did not find a strong relationship between
intra-annual site fidelity and wetland hydroperiod or
population density, which may indicate that males are
leaving wetlands in response to other environmental
variables that reduced reproductive success in the past.
Within-year site fidelity could also depend on local
weather conditions. For example, frequent precipita-
tion events could effectively eliminate the physiological
barriers to movement and facilitate dispersal between
wetlands. Changes in habitat suitability over the course
of the 1- to 3-week breeding season (e.g., pond drying)
could initiate random or informed movement among
wetlands, though we were not able to explicitly capture
those dynamics here.
Conservation implications for
wetland-breeding amphibians
Amphibians are the most imperiled class of vertebrates
on Earth, with approximately 40% of the world’s approxi-
mately 8000 known species threatened with extinction,
and many more experiencing population declines due to
habitat loss, climate change, and disease (Grant et al.,
2016; Hof et al., 2011; Miller et al., 2018). Understanding
amphibian movement is important for determining the
spatial scale at which a population operates, and for
designing effective disease and habitat management
21508925, 2023, 1, Downloaded from https://esajournals.onlinelibrary.wiley.com/doi/10.1002/ecs2.4345 by CAPES, Wiley Online Library on [06/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
11 of 15
strategies to combat species declines (Bailey &
Muths, 2019; Converse et al., 2017; Gerber et al., 2018;
Smith & Green, 2005). Our study adds to the growing
body of literature suggesting that many wetland-breeding
amphibian species are more vagile than previously
assumed (e.g., Denoël et al., 2018; Muths et al., 2018;
Patrick et al., 2008; Petranka & Holbrook, 2006), particu-
larly within breeding seasons. This movement of individ-
uals can maintain genetic diversity, increase local
evolutionary potential (Joly, 2019; Semlitsch, 2008,
though see Lenormand, 2002; Tigano & Friesen, 2016),
but also facilitate disease transmission (Kolby et al., 2015;
Muths et al., 2018; Tornabene et al., 2018).
The emergent fungal pathogen Batrachochytrium
salamandrivorans (Bsal, described in 2013; Martel et al.,
2013) poses a significant conservation risk because of its
high pathogenicity to salamander species (Martel et al.,
2014). Bsal has not yet been detected in North America
but the risk for introduction is high, particularly in the
eastern United States (Richgels et al., 2016; Yap et al.,
2015). Similar to the widespread amphibian pathogen
Batrachochytrium dendrobatidis (Bd, described in 1999;
Longcore et al., 1999), Bsal can be transmitted via direct
contact of individuals (e.g., during amplexus) or contact
with contaminated water (Malagon et al., 2020; Stegen
et al., 2017). Thus, movement to and between high-density
wetlands could be especially problematic in our study
system. Spotted salamanders appear resistant to Bsal
(Barnhart et al., 2020), but it is still unclear if this species
could facilitate community transmission and infection of
sympatric species. By understanding the factors that influ-
ence dispersal and movement of a common and abundant
species, like the spotted salamander, our study takes an
important first step in assessing disease risk. Extensions to
our framework that incorporate information about the dis-
ease state of individuals or sites could further elucidate
potential population- and ecosystem-level impacts of Bsal
and other virulent diseases.
Two of the 12 sites (site 1 and site 4) supported approx-
imately 70% of the breeding population and were preferen-
tially selected by dispersing males, likely because of high
population densities. Our results indicate that these wet-
lands play an important role in population dynamics,
suggesting long-term population persistence is likely to be
enhanced by maintaining wetlands that vary in size,
hydroperiod, and spatial proximity. Given that our wet-
lands were located at the edge of a forested landscape
and in close proximity to one another, we cannot infer
how dispersal probabilities and distances may differ in
highly fragmented landscapes. However, our modeling
framework could be extended to examine the influence of
factors, such as vegetation cover and habitat boundaries,
which can provide insight into the landscape-level features

12 of 15
that impede or facilitate movement in fragmented, or oth-
erwise modified, habitats (e.g., McDonough & Paton, 2007;
Patrick et al., 2008). By disentangling movement, breed-
ing, and other demographic rates at multiple scales, our
integrative approach can further improve inference on
the spatial and temporal aspects of amphibian move-
ment, particularly in the context of environmental
change.
A C K N O WL E D G M E N T S
We thank Christopher Smyth, Jon Kauffman, Robert
Newton, Amber Weiwel, Vishnupriya Sankaraman, Asia
Murphy, Beth Reinke, Matt Toenies, Torey Vayer, and Jerod
Skebo, as well as countless other undergraduate and
graduate students from the Wildlife and Fisheries Science
program and Shaver’s Creek Environmental Center at
Pennsylvania State University, for their help collecting field
data. We thank Jenna Antill, Katherine Reese, Hunter
Kauffman, Rysa Thomas, Lauren Cherry, Anna Lindemuth,
and Alyse Callahan for their help processing salamander
photographs in the lab. We also thank Hugo Cayuela for
insightful comments that helped to improve the manuscript.
We followed ethical handling procedures according to the
Pennsylvania State University’s Institute for Animal Care
and Use Committee protocol, permit #45187. Surveys
were approved by the Pennsylvania Fish and Boat (permit
numbers: 2014-01-0767, 2015-01-0120, 2016-01-0116,
2017-01-0026, 2018-01-0027, and 2019-01-0043) and
Pennsylvania Game Commission (permit numbers: 31460,
34392, 37258, 39887, 42473, and 45392).
CONFLICT OF INTEREST
The authors declare no conflict of interest.
DATA AVAILABILITY STATEMENT
Data and code (Davis, 2022) are available from Zenodo:
https://doi.org/10.5281/zenodo.7271953.
ORCID
Courtney L. Davis https://orcid.org/0000-0002-6467-
4288
David J. Muñoz https://orcid.org/0000-0003-3853-6540
Staci M. Amburgey https://orcid.org/0000-0002-7100-
7811
David A. W. Miller https://orcid.org/0000-0002-3011-
3677
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SU PP O R TI N G I N F O RMA TI O N
Additional supporting information can be found online
in the Supporting Information section at the end of this
article.
How to cite this article: Davis, Courtney L.,
David J. Muñoz, Staci M. Amburgey, Carli
R. Dinsmore, Eric W. Teitsworth, and David
A. W. Miller. 2023. “Multistate Model to Estimate
Sex-Specific Dispersal Rates and Distances for a
Wetland-Breeding Amphibian Population.”
Ecosphere 14(1): e4345. https://doi.org/10.1002/
ecs2.4345