Biological Conservation 169 (2014) 4453

Contents lists available at ScienceDirect

Biological Conservation
journal homepage: www.elsevier.com/locate/biocon

Perspective

Movement ecology of amphibians: A missing component

for understanding population declines
Shannon E. Pittman, Michael S. Osbourn, Raymond D. Semlitsch
Division of Biological Sciences, University of Missouri, 105 Tucker Hall, Columbia, MO 65211, United States

a r t i c l e

i n f o

Article history:
Received 20 August 2013
Received in revised form 24 October 2013
Accepted 28 October 2013

Keywords:
Amphibian
Connectivity
Dispersal
Individual-based models
Migration
Movement
Settlement

a b s t r a c t
Movement is a fundamental process of all organisms that has strong consequences for individual tness,
gene ow, natural selection, adaptation, population persistence, metapopulation dynamics, and species
distributions. Yet, a lack of understanding about how different organisms move in relation to landscape
structure and resource availability may prevent full understanding of species declines and extinctions. In
this perspective, we introduce the concept of movement ecology for aquatic-breeding amphibians, summarize our knowledge on amphibian movement, identify critical gaps, and provide a context for how
understanding movement will help develop solutions for more effective amphibian conservation. Juvenile amphibian movement is a multi-phase process during which individuals adjust movement speed,
responsiveness to habitat features, and propensity of settling based on internal state and the external
environment. Our review enables future studies to place amphibian movement data into a larger explanatory context and could help guide new avenues of research. Understanding juvenile responses to habitat
features during dispersal will aid in developing realistic, predictive models of amphibian movement that
could be used to further conservation and management efforts such as mitigation and restoration, and
will also add to theory about how movement mechanisms during dispersal impact population persistence in altered landscapes.
2013 Elsevier Ltd. All rights reserved.

Contents
1.
2.

3.
4.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Movement paradigm . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.1.
Pre-departure phase . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.2.
Initial juvenile movement phase . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.3.
Establishment of home range . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.4.
Adult migrations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.5.
Multiple movement modes and juvenile movement success . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Application . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction
Movement is a fundamental aspect of an organisms ecology
(Nathan et al., 2008), dening the spatial and temporal scale of
an organisms interactions with other organisms, resources, and

Corresponding author. Tel.: +1 573 864 2939.

E-mail address: SemlitschR@missouri.edu (R.D. Semlitsch).
0006-3207/$ - see front matter 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.biocon.2013.10.020

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the environment (Clobert et al., 2001, 2009). Movement mechanisms employed by individuals coupled with the structure of the
landscape and the availability and predictability of resources can
inuence the spatio-temporal dynamics of populations (Mueller
et al., 2011). The movement process used by individuals either to
disperse to new sites or settle near natal sites has strong consequences for individual tness, gene ow, natural selection, adaptation, population persistence, metapopulation dynamics, and
species distributions (e.g., Clobert et al., 2001; Knowlton and

S.E. Pittman et al. / Biological Conservation 169 (2014) 4453

Graham, 2010). Despite the importance of movement to the persistence of species, there are signicant gaps in our understanding of
movement processes (e.g., Bonte et al., 2012; Clobert et al., 2009;
Ronce, 2007). Molecular genetic tools have allowed us to describe
patterns of movement based on gene ow and the distribution of
genotypes across the landscape. However, those results merely
present the outcomes of movement and fail to inform an understanding of the underlying mechanisms of movement nor their tness consequences. This lack of understanding is increasingly
problematic as more species and populations face threats of decline and extinction due to global climate change, habitat fragmentation, and increasing human land use (Clobert et al., 2009). This is
especially true among amphibians, where it has been reported that
at least 2468 species or 43.2% of species worldwide are experiencing some form of population decrease (Stuart et al., 2004; Wake
and Vredenburg, 2008).
Historically, amphibian research has been focused on the aquatic larval stage, while the terrestrial juvenile and adult stages have
received less attention until recently. Many amphibians, in all regions of the world, depend on aquatic breeding habitats (e.g.,
seeps, springs, bogs, ponds, streams, lakes) that are clumped in
space (Gill, 1978; Sjogren-Gulve, 1994; Jehle et al., 2005; Grifths
et al., 2010; Heard et al., 2012). Adult populations reside in the terrestrial habitat often within 300 m but up to 1000 m of aquatic
breeding sites (varies by taxa; e.g., Semlitsch and Bodie, 2003;
Schabetsberger et al., 2004; Crawford and Semlitsch, 2007; Sinsch
et al., 2012). These breeding resources are strongly affected by both
deterministic processes of succession and stochastic processes of
weather or sh colonization that cause them to vary in suitability
over time, and occasionally, amphibians using them may be subject to catastrophic reproductive failure and local extinction (e.g.,
Semlitsch et al., 1996; Taylor et al., 2005). As a result of a relatively
high rate of local population extinction that occurs naturally across
the landscape, dispersal ability has a profound impact on aquaticbreeding amphibian persistence (Sjogren-Gulve, 1994; Trenham
et al., 2001; Werner et al., 2009; Grant et al., 2010). Population
dynamics are therefore highly susceptible to the effects of habitat
loss and fragmentation that impede or limit dispersal movement
(Cushman, 2006; Laan and Verboom, 1990; McDonough and Paton,
2007). Juveniles are widely regarded as the primary long-distance
dispersers in pond-breeding amphibian populations (Berven and
Grudzien, 1990; Gamble et al., 2007; Gill, 1978; Grifths et al.,
2010), and population persistence is disproportionately sensitive
to survival at this terrestrial life stage (Harper et al., 2008; Taylor
et al., 2005). Despite the importance of juvenile dispersal, we know
relatively little about the movement and search strategies of juvenile amphibians as they make initial movements into terrestrial
habitat or disperse among populations.
The overall goal of this paper is to introduce the concept of
movement ecology and its application to amphibian conservation.
We summarize the state of knowledge on amphibian movement,
identify critical gaps in our knowledge, illustrate how amphibian
movement data can be used to parameterize predictive models,
and provide a context for how understanding movement will help
understand species declines and susceptibility to extinction. This
paper generally focuses on temperate pond-breeding amphibian
species, and where possible, addresses application to other aquatic
breeding species (e.g., stream breeders), terrestrial species, and
species from tropical regions.

2. Movement paradigm
Nathan et al. (2008) proposed a unifying paradigm of organismal movement that emphasized linking observed movement patterns to specic movement phases, which may be comprised of

45

multiple behavioral states (i.e. movement modes; Fig. 1). This

movement paradigm is highly applicable to aquatic-breeding
amphibians, which exhibit well-dened life stages associated with
distinct movement patterns and movement goals over their lifetime (Fig. 1). For example, an amphibian undergoing a breeding
migration may maximize net displacement during movement to
expend energy the most efciently, and as a result of a cognitive
capacity to locate the breeding pond. Alternatively, an amphibian
that is foraging within a home range may exhibit highly tortuous
movement to exhaustively search an area while minimizing net
displacement. The movement patterns of these two examples are
therefore fundamentally different, and analysis and interpretation
of movement paths should thus be sensitive to the spatio-temporal
scale of movement goals and the sensory and motion capacity of
the animal (Fig. 1).
We hypothesize that movement phases are comprised of multiple movement modes of aquatic-breeding amphibians based on
Nathan et al., 2008 (Table 1). In the following, we review the ways
in which internal and external factors may interact to affect observed amphibian movement patterns and how those movement
patterns may be described in a mechanistic movement-modeling
framework. Specically, we posit and dene behavioral modes
within each movement phase that can be characterized by a pattern of movement (Table 1), and associated features of the organism and landscape that impact the pattern. These phases are
presented with the goal of providing amphibian researchers with
a structure in which to view, collect, and analyze movement data
(Table 1).
The inuence of movement goals on the movement patterns of
aquatic-breeding amphibians during natal dispersal is currently
poorly understood (Semlitsch, 2008). For example, juvenile pondbreeding amphibians emerge from the aquatic environment nave
to the distribution, abundance, and quality of habitat in the terrestrial environment and are greatly affected by external conditions as
a result of their susceptibility to predation and desiccation (Rohr
and Madison, 2003; Rothermel and Luhring, 2005; Shoop, 1974).
Initial movement into terrestrial habitat may constitute a substantial ecological bottleneck for amphibian populations. For example,
as few as 17% of juvenile spotted salamanders (Ambystoma maculatum) survive one year after metamorphosis even in high-quality
forest habitat (Rothermel and Semlitsch, 2002, 2006). Therefore,
the behavioral decisions of juveniles in the dispersal life stage have
profound implications for survival and population persistence,
especially in highly altered and fragmented landscapes. Explicit
investigation of the movement patterns of juveniles will aid in
developing mechanistic movement models that can predict the
ability of amphibians to behaviorally mitigate the effects of environmental perturbations.
2.1. Pre-departure phase
The pre-departure phase primarily describes the timing and initial orientation of juvenile departure from a natal site (Table 1). Because entire cohorts of juveniles emerge from what is ostensibly a
single location within the landscape (e.g. an ephemeral puddle or a
headwater stream), juvenile behavioral responses to external factors such as habitat arrangement in close proximity to the natal
site can affect the survival of large numbers of individuals. However, we know relatively little about what information is used by
juveniles to make initial departure decisions. There is not currently
a strong consensus on the degree to which juveniles acquire and
respond to information about terrestrial habitat while in the predeparture phase, or the role of temporal variation in weather conditions, making this a critical area for future research. We identify
two distinct movement modes within the pre-departure phase:
pre-emergence mode and wait mode (Table 1).

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S.E. Pittman et al. / Biological Conservation 169 (2014) 4453

Fig. 1. Example lifetime movement tract of a pond-breeding salamander that includes different phases of both juvenile and adult. Modied from Nathan et al. (2008).

Table 1
Proposed amphibian movement phases and movement modes.

a
b

Movement phase

Movement mode

Key decisions

Net
displace.

Habitat
response

Movement
rate

Orientation

Pre-departure

Pre-emergence
Waita

When and where to emerge and orient?

When to depart?

None
None

High?
High

Stopped
Stopped

Biased
N/A

Initial juvenile
movement

Away
Directed
Settlement
(temporary)

Where to and how fast to move?

Where to and how fast to move?
When and where to stop?

High
Medium
Low

Low
Medium
High

High
Medium
Low

Random
Biased
Biased

Home range

Settlement (longterm)

When and where to end dispersive movement?

Low

High

Low

Biased

Foragingb

Foraging

Where to forage?

Low

High

Low

Biased

Adult migrations

Immigration
Emigration

When to return and what route to take the breeding site?

When to depart and what route to take back to home range or
over-wintering site?

High
High

Medium
Medium

Medium
Medium

Biased
Biased

Individuals may enter wait mode from any movement phase as they await optimal movement conditions.
Individuals may alternate into a foraging movement phase when energy reserves are low.

Pre-emergence mode is dened as the behavioral stage at which

newly metamorphosed amphibians remain in the natal site, move
to shallower water along the wetland edge, and assess conditions
pertaining to movement into terrestrial habitat. Hayward (2000)
speculated that newt larvae begin orientation towards surrounding
terrestrial habitat prior to metamorphosis. Patrick et al. (2007) observed that wood frog larvae (Lithobates sylvatica) in natural natal
ponds oriented toward terrestrial habitat while within the wetland. When the authors transplanted larvae to experimental pools,
the emerging juveniles maintained their original orientations acquired at their pond of origin. The ability of the juveniles to maintain orientations after translocation suggests that some species are
capable of directional orientation, as has been documented extensively in newts (e.g. Diego-Rasilla et al., 2008). Juveniles are motivated to leave the natal site to nd a terrestrial settlement location
with high quality habitat, low density of conspecics, low predator
densities, and in proximity to a future breeding site. Energy

reserves and body size resulting from the quality of aquatic larval
habitats (Beck and Congdon, 2000; Scott et al., 2007; Lowe, 2009)
and reduced performance due to disease (Cheatsazan et al., 2013;
Parris and Cornelius, 2004) are likely the most signicant internal
factors affecting juvenile decisions during this movement mode.
Important external factors may consist of climatic conditions such
as rainfall, water level or drying rate (e.g., Semlitsch et al., 1996;
Todd and Winne, 2006), and densities of conspecics or predators
(e.g., Scott, 1990; Skelly, 1996).
Wait mode is the behavioral stage at which juveniles delay
departure from the natal site for environmental or internal conditions to improve for movement. Immediately following metamorphosis and emergence, juvenile amphibians often make initial
movements into terrestrial habitats at night during or directly after
rainfall (Mazerolle, 2001; Todd and Winne, 2006). If environmental
conditions for movement are poor, juveniles may remain at the pond
edge. The decision of when to depart involves a trade-off between

S.E. Pittman et al. / Biological Conservation 169 (2014) 4453

the heightened desiccation risk of terrestrial movement in poor conditions (Rittenhouse et al., 2009; Rothermel and Luhring, 2005) or
poor physiological condition as a result of disease (Parris and Cornelius, 2004), and a number of documented risks near the natal pond,
such as depletion of energy reserves (Scott et al., 2007), predation
(Pittman et al., in press; Rittenhouse et al., 2009), and density effects
(Harper and Semlitsch, 2007). Because of these costs, juveniles do
not remain in wait mode indenitely and will move into terrestrial
habitat even under poor environmental conditions, such as droughts
(Rothermel, 2004). Such trade-offs are integral to animal movement
and likely drive the transitions between different movement modes
(Wiens, 2001; Zollner and Lima, 2005). Conditions affecting the initial orientation and timing of departure during the pre-departure
phase contribute to the success of juvenile amphibian movements
in terrestrial habitats.
The sensory capacity of juveniles in the pre-departure stage will
likely determine the degree to which the initial orientations of
juveniles departing their natal site correlates with terrestrial habitat quality. On the whole, research indicates that juveniles have
limited ability to sense terrestrial habitat from their natal site,
and some generalist species may not exit their natal site with afnity for any particular habitat type. Previous research has found that
the overall orientations of departing juveniles are often nonrandom at single ponds (Jenkins et al., 2006; Patrick et al., 2007;
Rittenhouse and Semlitsch, 2006; Rothermel, 2004; Timm et al.,
2007); however, the mean direction of exiting juveniles is not usually correlated with terrestrial habitat quality (but see Patrick et al.,
2007; Walston and Mullin, 2008). Studies have found that although
adult emigration post breeding is highly nonrandom and directed
toward high quality terrestrial habitat, juvenile orientation is generally less concentrated and uncorrelated with terrestrial habitat
quality (Jenkins et al., 2006; Rittenhouse and Semlitsch, 2006).
Therefore, the nonrandom orientations of departing juveniles
may be generated by small-scale climatic or topographic features,
such as shore-line slope or ditches, along the pond edge that dictate juvenile spatial arrangement in the pre-departure phase.
Alternatively, adult orientation is more likely dictated by spatial
memory of terrestrial refugia (Madison, 1997), which likely drives
the differences seen between juvenile and adult patterns of exit
from breeding ponds.
During the pre-departure phase, juveniles may make foray
searches into terrestrial habitat before nal departure, a movement
strategy which has been observed in non-amphibians (Conradt
et al., 2003). Foray loops are fundamentally nonrandom movement
(but see Crone and Schultz, 2008), in which individuals move into
novel landscapes, acquire information, and return to home or safe
locations. Whereas dispersers of numerous other species make
prospecting foray loops into novel habitat, including butteries,
birds, and mammals (Conradt and Roper, 2006; Cox and Kesler,
2012; Schliehe-Diecks et al., 2012), there is little direct evidence
that juvenile amphibians employ this search strategy. Explicitly
testing for the presence of foray searching is an important area
of future research, as this behavior may profoundly inuence dispersal patterns and initial susceptibility to habitat quality and land
use.
2.2. Initial juvenile movement phase
The initial juvenile movement phase consists of three movement modes: away mode, directed mode, and settlement mode
(Table 1). These behavioral states are dened by the extent to
which individuals respond to external factors during movement
and the spatial scale over which they make movement decisions
relative to motion and sensory capacity (Fig. 2). In general, we
hypothesize that juveniles depart from natal sites with low
responsiveness to habitat and high movement rates and gradually

47

Fig. 2. Behavioral modes and characteristics of associated movement parameters

during initial movement of juveniles away from natal sites.

shift into behavioral states with higher responsiveness to habitat

and slower rates of movement. We hypothesize that the primary
goals of amphibians during the initial juvenile movement phase
are to escape the high rates of predation at the pond edge (Pittman
et al., in press; Rittenhouse et al., 2009), to minimize density effects
(Harper and Semlitsch, 2007), and to locate suitable settlement
habitat (Rothermel and Semlitsch, 2002, 2006). Species that do
not encounter high densities of predators or competitors upon
exiting natal sites (such as some tropical species) may not adhere
as strongly to these factors. Such species may depart natal sites
with high responsiveness to habitat and long-distance dispersal
may be driven by longer-term factors such as decreasing kin competition or mitigating environmental stochasticity (Clobert et al.,
2001).
Away mode is dened as movement that is the least responsive
to external cues such as climatic conditions or habitat composition.
We hypothesize that juveniles in away mode are the least responsive to terrestrial habitat quality, and they make movement decisions on a large spatial scale relative to their perceptual range.
They likely do not exhibit boundary behavior and may therefore
be likely to enter inhospitable areas. The benets of this behavioral
state are in maximizing net displacement from a natal site and
expediting escape from areas with the highest densities of predators and competitors. For example, Pittman et al. (in press) found
that approximately 23% of juvenile ringed salamanders (Ambystoma annulatum) making initial movements from ponds into terrestrial habitat were consumed by anuran predators, with the
highest mortality rates occurring within 5 m of the pond edge. Because juveniles are the least responsive to habitat quality during
away mode, movement patterns may be characterized as basic
Brownian motion, or diffusion (Boone et al., 2006), and may be
modeled discretely using random walks (Codling et al., 2008;
Conradt and Roper, 2006; Schwarzkopf and Alford, 2002). Random
walks describe movement as a series of steps and turning angles
drawn from a distribution, where each successive turning angle
is independent of the previous turning angle. At the most basic level, this type of movement is common in animals that are not
responsive to environmental features and which are not employing
spatial memory or navigational mechanisms during movement
(Codling et al., 2008; Haefner and Crist, 1994). However, random
walk models can be modied to incorporate different levels of
behavioral complexity such as changes in step size or directional
persistence (correlation of turning angles) with habitat type or risk
level (e.g., predation or desiccation from land use). Employment of
random walk and diffusion models often involves the analysis of

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S.E. Pittman et al. / Biological Conservation 169 (2014) 4453

ne-scale movement data (Turchin, 1991) or mark-recapture data

(Ovaskainen, 2004; Reeve et al., 2008) to estimate distributions of
path components or diffusion coefcients and to test that observed
movement patterns t random walk expectations. For example, the
movement paths of animals employing systematic searching (such
as foray loops or large-scale orientation) are not well approximated
by random walk models, and goodness of t can be tested explicitly by comparing observed and expected net movement rates
(Benhamou, 2004; Kareiva and Shigesada, 1983; Nams, 2006).
Analysis of ne-scale amphibian movement data within the context of random walk models will help researchers test hypotheses
concerning the spatial memory and navigational abilities of juvenile amphibians (Nams, 2006), estimate the scale at which juveniles make movement decisions (Papastamatiou et al., 2011), and
develop mechanistic models of amphibian movement (McClintock
et al., 2012).
Relevant movement parameters during away mode include
mean step sizes (spatial scale over which individuals make single movement decisions) and the distribution of turning angles,
both of which likely vary with habitat type (Gillies et al.,
2011; Stevens et al., 2005), the perceptual range of the individual (Olden et al., 2004; Peer and Kramer-Schadt, 2008), and
genetically-based behavioral tendency (Cote et al., 2010). Additionally, internal factors such as energetic reserves resulting
from differences in habitat quality, or disease, and species differences in vagility may impact movement parameters during away
mode. Tortuosity of the movement path can be estimated in the
eld using tracking data and may be modeled by parameterizing
the distributions of turning angles and step sizes (Codling et al.,
2008; Haefner and Crist, 1994). Relatively small differences in
turning angle distributions may have large impacts on the efcacy of different search strategies relative to movement goals
(Zollner and Lima, 1999), and risks encountered by individuals
may also heavily affect optimal movement behavior (Fahrig,
2007; Zollner and Lima, 2005; Stevens et al., 2005). Amphibians
with low vagility likely move linearly to decrease the amount of
time spent in close proximity to the wetland edge and to maximize the energy efciency in displacing themselves from the
natal site. For example, Pittman and Semlitsch (2013) found that
juvenile spotted salamander (A. maculatum) movement in forested habitat approximated random walks with high correlation
of turning angles. Alternatively, amphibians with high vagility
may not be limited by energy or time and may move more tortuously during away mode (e.g. some ranid frogs Roznik and
Johnson, 2009; Roznik et al., 2009).
The extent to which juveniles respond to habitat features during
movement away from their natal site likely increases the longer an
animal has been moving, as has been shown explicitly in juvenile
owls and newts (Delgado et al., 2009; Jehle and Arntzen, 2000).
Jenkins et al. (2006) found that salamander orientation differed signicantly at 3 m from the pond edge versus 30 m from the pond
edge. Orientation at 30 m was predicted by habitat quality, while
orientation at 3 m was not, indicating a shift in responsiveness to
habitat. Additionally, Rittenhouse and Semlitsch (2006) found that
while juvenile spotted salamanders oriented non-randomly toward
low-quality habitat during initial emergence from the natal pond,
the majority reversed toward high-quality habitat later, as
individuals likely shifted into a more habitat-responsive behavioral
state.
As juveniles become more responsive to habitat features during
movement, we hypothesize that they shift from away mode into
directed mode. Individuals in directed mode respond to habitat
features at large spatial scales in relation to the species perceptual
range. Directed mode is characterized by higher path sinuosity,
lower movement speed, and higher responsiveness to habitat characteristics than away mode (Fig. 2). Individuals in directed mode

are likely to display edge-mediated movement behavior and may

be less willing to enter poor-quality habitat (DeMaynadier and
Hunter, 1999; Stevens et al., 2006; Popescu and Hunter, 2011). This
movement can be characterized using correlated random walk
models with the inclusion of a bias parameter or advection toward
important habitat features (Barton et al., 2009; Chapman et al.,
2007; Crone and Schultz, 2008; Haddad, 1999); biased movement
toward quality habitat has been documented in both temperate
(Pittman and Semlitsch, 2013; Rittenhouse and Semlitsch, 2006),
and tropical amphibian species (Nowakowski et al., 2013).
The timing of the switch between away mode and directed
mode is likely dependent on external conditions such as habitat
quality and interactions with predators or competitors, and the
internal state of individuals such as energy storage, geneticallybased behavioral tendency, and disease presence (Clobert et al.,
2009; Cote et al., 2010; Rmy et al., 2011; Parris and Cornelius,
2004; Sih et al., 2004). Species with higher vagility may spend
more time in directed mode because they are able to move rapidly through a large amount of habitat, lowering the costs associated with searching previously-visited areas (Zollner and Lima,
1999). Higher vagility and greater responsiveness to habitat may
partially explain the higher movement tortuosity and greater frequency at which green frogs (Lithobates clamitans) cross forest/
non-forest boundaries than spotted salamanders (Osbourn,
2012). Individuals that stay in away mode for the longest time
are more likely to be long-distance dispersers than individuals
that shift to directed mode early during initial dispersal. For an
animal to be a long-distance disperser, the individual likely must
pass over high-quality habitat, which necessitates a lower
responsiveness to habitat and a higher degree of boldness than
individuals that respond to habitat quality and settle (Rehage
and Sih, 2004).
After directed mode, juveniles shift into settlement mode when
searching for a suitable refuge (Table 1). Juveniles in this behavioral mode are highly responsive to habitat features such as moisture gradients, burrows, and cover objects (rocks, coarse woody
debris) at ne spatial scales relative to their perceptual range
(e.g., in wood frogs Patrick et al., 2008). Although this type of
movement is fundamentally non-random because individuals are
responding to habitat features, these movements may be approximated using a pure random walk or a random walk with low correlation of turning angles (Pittman, 2013).
The shifts in behavioral states from away mode to directed
mode to settlement mode may occur in a single night or may
encompass multiple nights, and juveniles may transition among
behavioral states multiple times before nal settlement. For example, juveniles may nd a temporary location for settlement after
the rst night of movement and move again in subsequent nights
when environmental conditions are favorable (Osbourn, 2012).
Multistate random walk models may be used to simulate longterm amphibian movement using a series of biased and correlated
random walks that dene different movement modes (McClintock
et al., 2012).
Transitions between behavioral states occur probabilistically
using various internal and external covariates dictating the risks
and benets to movement. Although the collection of these
ne-scale data are time consuming, once compiled for several
species, the resulting mechanistic models can be used to test a
multitude of habitat quality and conguration questions, not
possible by traditional eld methods (Pittman, 2013). This movement modeling approach will allow a more sophisticated interpretation of amphibian movement paths, generate hypotheses
for the tness consequences of movement behavior, and improve
prediction of the effects of land use, disease, or climate change
on both local population and metapopulation dynamics (e.g.,
Grant et al., 2010).

S.E. Pittman et al. / Biological Conservation 169 (2014) 4453

49

2.3. Establishment of home range

2.5. Multiple movement modes and juvenile movement success

After juveniles have chosen a nal settlement location, the initial juvenile movement phase ends, and they establish home
ranges (Table 1). Although dening an animals home range is complex (Powell and Mitchell, 2012), for our discussion concerning
amphibians, we dene it simply as a refuge area where an individual is protected from desiccation and can nd adequate food resources. Amphibian home ranges are typically small (12 m2),
and consist of small-scale refugia such as logs, rocks, burrows, or
trees (Johnson et al., 2007; Loredo et al., 1996; Pittman et al.,
2008; Vasconcelos and Calhoun, 2004). Species such as toads or
salamanders may remain in terrestrial refugia such as small mammal burrows or under rotting logs at their nal settling location
(e.g., Jehle and Arntzen, 2000; Madison, 1997; Marsh et al.,
2004). In more-aquatic species such as California red-legged frogs
(Lithobates draytonii), the rst home range of juveniles may be in a
small puddle or along a creek. Although there is variation among
species, some pond-breeding species such as wood frogs (82%; Berven and Grudzien, 1990) or marbled salamanders (91%; Gamble
et al., 2007) are highly philopatric, and juveniles establish home
ranges in areas surrounding their natal pond (Semlitsch, 2008).
Some tropical species exhibit long-term territoriality to breeding
sites, and can home to breeding locations after experimental displacement (Pasukonis et al., 2013). Stream salamanders also generally establish home ranges in riparian habitat within a short
distance of stream edges (Crawford and Semlitsch, 2007).
After settlement, an individuals movements consist of short
movements between foraging sites and, after maturity, longer distance seasonal breeding migrations (e.g., Semlitsch, 1981). Movement during foraging bouts is highly biased toward settlement
locations, and individuals likely remain within small home ranges
(Kleeberger and Werner, 1983; Madison, 1997; Semlitsch, 1981).
Mechanistic movement models based on random walks that incorporate spatial memory and/or cognitive maps may approximate
movement within a home range (Moorcroft, 2012; Powell and
Mitchell, 2012; Van Moorter et al., 2009). Habitat alteration and
land use that disrupt the establishment of home ranges or causes
individuals to frequently abandon current locations can inict
added costs such as reduced feeding and growth or reduced survival on individuals during this phase. The reduction of survival
during the juvenile stage, prior to maturation, is the most important factor causing local extinction (Taylor et al., 2005; Harper
et al., 2008).

Juvenile movement decisions have consequences for both

short-term survival and long-term tness. The amount of time that
individuals spend in away, directed, or settlement mode greatly affects the risks that they encounter during dispersal and potential
tness benets. For example, a juvenile whose movement path is
dominated by movement in settlement mode will likely settle
close to the natal pond. This individual may have a smaller chance
of dying from desiccation or loss of energy, but may also encounter
higher rates of predation and may be affected by greater density
(Harper and Semlitsch, 2007) and low juvenile survival (Harper
et al., 2008). However, this individual will not incur great energetic
costs later during adult breeding migrations. An individual that
spends the greatest amount of time in away mode (e.g. a long-distance disperser) will incur signicant energetic and desiccation
costs during movement and will increase the chance of entering
unsuitable habitat and dying. However, this individual will also
have the greatest likelihood of colonizing or locating a new breeding site with high tness benets (McPeek and Holt, 1992; Lowe,
2009).
Habitat alteration changes the risks and benets associated
with different movement modes and associated behavioral decisions (Fahrig, 2007). For example, loss of habitat may increase
the risks associated with away mode, and individuals may have
higher survival by shifting to directed or wait mode quickly during
dispersal. However, movement that is highly responsive to habitat
in clumped or fragmented landscapes may accumulate more juveniles and generate high-density areas that increase time to maturity, and lower growth and survival rates of juveniles (Harper
and Semlitsch, 2007; Patrick et al., 2008). While remaining within
natal populations may increase the chances of survival in altered
landscapes, dispersal to new breeding sites may also yield high tness benets (Grant et al., 2010). For example, theoretical models
have found that evolutionary rescue is possible for buttery species impacted by habitat fragmentation. In simulations, buttery
populations evolved a higher dispersal rate in fragmented landscapes despite the risk of movement because the tness benets
to colonizing newly available habitat outweighed the survival benets of remaining philopatric (Heino and Hanski, 2001). There is
also new evidence in toads that fragmentation can cause inherited
differences in movement propensity of juveniles (Janin et al.,
2012). Understanding the factors that affect amphibian movement
decisions and the costs to those decisions will aid in understanding
amphibians ability to behaviorally or evolutionarily mitigate the
effects of land use, disease, or climate change.

2.4. Adult migrations

In subsequent years following the establishment of a home
range, juveniles continue to grow and eventually join an adult
breeding population that migrate seasonally to and from an aquatic breeding site typically on the scale of 1001000 m (Semlitsch
and Bodie, 2003; Crawford and Semlitsch, 2007; Rittenhouse and
Semlitsch, 2007). Some species or individuals may also migrate between home ranges and overwintering sites (Semlitsch, 2008).
Long-distance migrations to breeding locations are driven by
memory or possibly even external cues such as conspecic trailing
(Malmgren, 2002). Therefore, movement is nonrandom and highly
directed toward breeding sites and to overwintering locations after
breeding (Jenkins et al., 2006; Semlitsch, 1981, 1998; Sinsch, 1990;
Sinsch et al., 2012). The targeted movement of individuals toward
known locations is a fundamental difference between the migration movement phase and initial juvenile movement. Modeling of
movement during migrations should therefore incorporate spatial
memory and potentially large-scale orientation mechanisms toward breeding sites (Mueller et al., 2011).

3. Application
Much of the effort in amphibian conservation research has been
focused on describing patterns of decline. Although this is an
essential starting point, the development of effective management
solutions can only be achieved by understanding why populations
or species decline and reversing those trends. Because movement
of juveniles from natal habitats into terrestrial adult populations
is the fundamental process of local recruitment, and the maintenance of metapopulation dynamics requires dispersal and recolonization across a broader landscape, movement ecology is a
critical component of species persistence. We have introduced
the movement ecology paradigm so that behavioral studies can
be directly linked to tness consequences associated with movement, population growth, and therefore the probability of decline.
Although our introduction of movement ecology for understanding
amphibian declines has focused largely on pond-breeding species
examples, much of what we presented has direct application to

50

S.E. Pittman et al. / Biological Conservation 169 (2014) 4453

other aquatic breeding species (e.g., stream salamanders, many of

which make overland movements; Grant et al., 2010; Heard
et al., 2012; Lowe and McPeek, 2012) and possibly terrestrial
breeding species that exhibit spatial structure (e.g., woodland salamanders Plethodon cinereus; Marsh et al., 2004; Peterman and
Semlitsch, 2013).
Partitioning amphibian movement into phases associated with
particular goals, achieved through multiple behavioral modes, is
a new and potentially useful approach to understanding the persistence of amphibian populations. In recognizing different movement modes, we can begin to place patterns of movement,
especially juveniles, into proper behavioral context and thereby
better understand their role in maintaining local populations and
metapopulations. Continued experimentation and observation is
needed to rene our understanding of each movement mode and
to identify species-specic responses or patterns associated with
species life histories (Grant et al., 2010; Connette and Semlitsch,
2013). This approach should enable us to reinterpret the results
of prior studies and better predict juvenile movement outcomes
and populations dynamics, especially in relation to anthropogenic
habitat changes and land use.
One of the primary goals of juveniles emerging from natal sites
is to nd suitable terrestrial habitat. Studies directed at understanding movement in relation to surrounding terrestrial habitats
of varying quality and at varying distances from the natal site will
help identify the effects of habitat loss and alteration on juvenile
success at this critical stage. The reduction of habitat quality or increased distance between aquatic and terrestrial habitats would
likely decrease juvenile survival and recruitment for local populations, eventually causing declines in adult populations (Harper
et al., 2008). Differences in species vagility and their tolerance of
habitat loss around natal sites would help predict their susceptibility to land use and population decline.
Understanding movement and dispersal behavior is critical to
parameterizing mechanistic movement models with the ability to
predict population processes in dynamic landscapes. Such models
include Individual-Based Modeling (IBM; Peer et al., 2011), diffusion models (Ovaskainen, 2004), or integrodifference equations
(Jongejans et al., 2011; Neubert and Caswell, 2000). These modeling techniques have been widely used across a variety of taxa to
improve the management and conservation of populations in
changing landscapes, including predicting species range expansions or shifts as a result of climate change (e.g., Wasserman
et al., 2012), the progression of species invasions (e.g., Perkins
et al., 2013) or disease (e.g., Green et al., 2006), and the effects of
management regimes on population viability or recolonization
and restoration (e.g., Grant et al., 2010; Connette and Semlitsch,
2013). To make useful predictions about amphibian persistence
in dynamic landscapes, our knowledge of amphibian movement
behavior must progress beyond phenomenological studies (such
as occupancy models) with an additional focus on mechanisms
generating observed patterns of population growth and abundance
and not just presence or absence. Knowledge of movement behavior is necessary to build and implement these models.
Studies that couple landscape genetics with mechanistic
movement models can also increase understanding of species persistence at greater spatial and temporal scales by modeling multidirectional and multi-generational gene ow among natal ponds
(Wang et al., 2009). Studies of individual movement behavior at
smaller scales provide valuable information that can be used for
scaling up from the individual to local population or metapopulation levels. Habitat quality and heterogeneity have been shown to
be important drivers of dispersal (e.g., Bowler and Benton, 2005;
Ferreras et al., 1992; Revilla and Wiegand, 2008). Understanding
factors contributing to species movement and success at a ne
scale can enable us to predict movement patterns over larger scales

and under differing land-use contexts (Lima and Zollner, 1996;

Nathan et al., 2008; Zollner and Lima, 2005). By using mechanistic
movement models, such as IBMs, we can model implications of different movement rules affecting dispersal, thereby expanding the
scale of inference beyond what can realistically be measured in
the eld (e.g., program SEARCH-Pauli et al., 2013). Other studies
have found that small-scale movement properties are a good
mechanistic approximation of dispersal for predicting population-level processes at greater scales using IBMs (Nathan et al.,
2002; Revilla et al., 2004). Ultimately, this approach should help
predict responses to habitat heterogeneity due to land use, determine where to mitigate or restore habitat, enable managers to balance risks of habitat loss, explain why some species are more or
less sensitive to habitat loss, and aid in the conservation of populations and species (Alderman et al., 2005; Gibbs, 1998; Lima and
Zollner, 1996; Stevens et al., 2005; Connette and Semlitsch,
2013). As we continue to determine the relationship between habitat quality and movement behavior, and factors that mediate that
relationship, we will continually improve the accuracy of predictive models to aid in understanding species persistence and in mitigating declines.
4. Conclusions
We introduce the concept of movement ecology to amphibian
conservation to direct research efforts on the dispersal stage of
amphibians. Juvenile movement of aquatic-breeding amphibians
is a multi-stage process during which individuals vary movement
speed, responsiveness to habitat features, and propensity of settling based on internal state and the external environment
(Fig. 2). Although the movement mode approach described in this
paper is a discrete interpretation of what is more likely to be a continuous behavioral spectrum, the use of subdivided behavioral
modes could be a useful rst step in categorizing and interpreting
amphibian movement data. This framework is intended as a starting point to stimulate ideas and be modied as needed to t the
unique characteristics of specic amphibian systems. Currently,
many studies of amphibian movement are large-scale, pattern-oriented approaches that only indirectly address underlying movement mechanisms. Our approach will allow future studies to
place amphibian movement data into a larger explanatory context
and could help guide new avenues of research. Understanding
juvenile responses to habitat features during dispersal will aid in
developing realistic, predictive models of amphibian movement
that can be used to further conservation and management efforts
and will also add to theory about how movement mechanisms during dispersal impact population persistence in altered landscapes.
Acknowledgements
We thank G. Connette, D. Kesler, and P. Zollner for comments on
the manuscript. Manuscript preparation and our cited research
was supported by Grants from NSF DEB 0239943 and DOD SERDP
RC2155.
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