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Many proximate causes of global amphibian declines have been well documented, but the role that climate change has played and will play in this crisis remains ambiguous for many species. Breeding phenology and disease outbreaks have been associated with warming temperatures, but, to date, few studies have evaluated effects of climate change on individual vital rates and subsequent population dynamics of amphibians. We evaluated relationships among local climate variables, annual survival and fecundity, and population growth rates from a 9-year demographic study of Columbia spotted frogs (Rana luteiventris) in the Bitterroot Mountains of Montana. We documented an increase in survival and breeding probability as severity of winter decreased. Therefore, a warming climate with less severe winters is likely to promote population viability in this montane frog population. More generally, amphibians and other ectotherms inhabiting alpine or boreal habitats at or near their thermal ecological limits may benefit from the milder winters provided by a warming climate as long as suitable habitats remain intact. A more thorough understanding of how climate change is expected to benefit or harm amphibian populations at different latitudes and elevations is essential for determining the best strategies to conserve viable populations and allow for gene flow and shifts in geographic range.
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Decreased winter severity increases viability of
a montane frog population
Rebecca M. McCaffery
and Bryce A. Maxell
Wildlife Biology Program, College of Forestry and Conservation, University of Montana, Missoula, MT 59812; and
Montana Natural Heritage Program,
University of Montana, Helena, MT 59620
Edited by David B. Wake, University of California, Berkeley, CA, and approved April 6, 2010 (received for review November 9, 2009)
Many proximate causes of global amphibian declines have been
well documented, but the role that climate change has played and
will play in this crisis remains ambiguous for many species. Breeding
phenology and disease outbreaks have been associated with
warming temperatures, but, to date, few studies have evaluated
effects of climate change on individual vital rates and subsequent
population dynamics of amphibians. We evaluated relationships
among local climate variables, annual survival and fecundity, and
population growth rates from a 9-year demographic study of
Columbia spotted frogs (Rana luteiventris) in the Bitterroot Moun-
tains of Montana. We documented an increase in survival and
breeding probability as severity of winter decreased. Therefore,
a warming climate with less severe winters is likely to promote
population viability in this montane frog population. More gener-
ally, amphibians and other ectotherms inhabiting alpine or boreal
habitats at or near their thermal ecological limits may benet from
the milder winters provided by a warming climate as long as suit-
able habitats remain intact. A more thorough understanding of how
climate change is expected to benet or harm amphibian popula-
tions at different latitudes and elevations is essential for determin-
ing the best strategies to conserve viable populations and allow
for gene ow and shifts in geographic range.
climate change
Rana luteiventris
Amphibian populations are declining around the globe at an
alarming rate (13), and climate change now gures promi-
nently as a potential interactive driver of some of these declines
(46). A shift to earlier breeding phenology has been documented
in a number of species (711), but this shift is not universal across
species and has not been tied to population-level consequences.
Other work has associated climatic conditions with disease-related
declines in the Neotropics (4, 5), yet no mechanisms have been
denitively linked to these correlations (12, 13). Reading et al. (14)
showed a decrease in adult female body condition and survival in
a population of common toads (Bufo bufo) that corresponded
with an increase in average annual temperatures. However, these
demographic changes were not explicitly linked to changes in
population size over time. Kiesecker et al. (15) showed that dis-
ease, UV-B, and climate change could interact to increase embryo
mortality in western toad (Bufo boreas) populations, yet these
populations have not declined. This increased premetamorphic
mortality may not be sufcient to cause otherwise increasing
populations to decline in the long term. Alternatively, it may be
that conditions in short-term or laboratory-based studies are not
always representative of long-term patterns in natural pop-
ulations. To determine mechanisms of population change, we rst
need to know which vital rates are affected by changes in climate,
and then how these changes affect population dynamics.
The effects of climate change on growth and survival are par-
ticularly relevantfor amphibian species in high elevation temperate
ecosystems, where individuals are exposed to extreme and variable
temperatures (e.g., ref. 16). In these environments, amphibians are
active at a wider range of temperatures than closely related species
inhabiting lower elevations (17). In general, juveniles and adults in
high elevation temperate environments must reproduce and ac-
quire resources over much shorter growing seasons than low ele-
vation individuals. Similarly, tadpoles must be able to develop and
metamorphose over a short season or survive long cold winters. In
these environments, longer growing seasons due to climate
warming may allow more time for adults, juveniles, and tadpoles to
grow and acquire resources. Winter severity may decrease, re-
ducing winterkill due to freezing or hypoxia, which can be a major
cause of mortality in these systems (18, 19). However, reduced
precipitation and a warm environment could result in less water in
these high-elevation landscapes, which may negatively impact
amphibian species that rely on ephemeral pools for reproduction
and foraging. Additionally, amphibian populations and speciesthat
are adapted to a colder thermal regime in alpine systems may have
physiological constraints that prevent adaptation to an increase in
temperature (20). With climate change models for the western
United States predicting a reduction in snowpack, as well as in-
creased variability in precipitation levels (21, 22), understanding
the role of these climate variables in the growth and survival of
high-elevation populations of amphibians is critical to predicting
future impacts of climate change on amphibians.
We evaluated relationships between annual vital rate estimates,
estimates of asymptotic population growth rate, and local climate
variables in a high elevation population of a temperate pond-
breeding frog species, the Columbia spotted frog (Rana lutei-
ventris). To evaluate these relationships, we used both mark-re-
capture and demographic analyses. A longstanding principle of
demography is that not all vital rates are equally important for
population dynamics. For example, large changes in annual re-
cruitment, which are commonly documented in amphibians, tend
to have less impact on population growth rates than relatively
small changes in postmetamorphic survival rates (23). We exam-
ined variation in survival, growth, and recruitment in relation to
summer and winter climate variables. We then used matrix models
to calculate asymptotic growth rate (λ) for each set of annual vital
rates (2426) and related λto these climate variables by using
linear regression. Our results advance our understanding of how
climate change may affect amphibian populations, and have
implications for the conservation of other temperate amphibian
species occupying alpine and boreal habitats.
We conducted our study in the Little Rock Creek Basin, found
in the Selway-Bitterroot Wilderness 16 km south of Hamilton,
MT. This drainage is composed of two glacial cirques. Our
analyses were focused on the upper basin (2,200 m), which is
delineated by glacial headwalls (Fig. 1). Although this upper
basin contains multiple breeding and foraging sites, they function
as one population (27). The basin contains requisite habitats for
R. luteiventris overwintering, breeding, and summer foraging, and
Author contribution s: R.M.M. and B.A.M. designed resea rch; R.M.M. and B.A.M. per-
formed research; R.M.M. analyzed data; and R.M.M. and B.A.M. wrote the paper.
The authors declare no conict of interest.
This article is a PNAS Direct Submission.
To whom correspondence should be addressed. E-mail:
This article contains supporting information online at
May 11, 2010
vol. 107
no. 19
is shless (Fig. 1). We have not tested for the presence of the
amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd) in
this population, but Bd is widespread in Montana and has been
detected in amphibians within a few miles of this watershed (28).
However, no mortality events were noted in this watershed, no
local or broad-scale declines have been detected for R. lutei-
ventris in western Montana during the course of this study (28),
and R. luteiventris is known to have skin peptides that are highly
resistant to Bd (29). Therefore, we believe that common culprits
for amphibian declines at high elevation sites (i.e., introduced
sh and disease; refs. 30 and 31) do not complicate our analyses.
We monitored all life stages of R. luteiventris from 2000 to 2008
and related these demographic data to climate data collected at
a nearby weather station. Climate variables included (i) peak
snow-water equivalency (hereafter SWE, a common measure
of snowpack), (ii) winter length, (iii) end of winter Julian date
(hereafter last day of winter), (iv) summer length, and (v)
growing degree days (see Methods for complete description of
climate variables).
Climate Variables. During the 9 years of our study, SWE ranged
from 67 to 135 cm, winter lengths varied by 41 days, last day of
winter varied by 33 days, summer length ranged from 84 to 120
days, and growing degree days ranged from 431 to 648 days.
There were no trends in any of the climate variables over the
study period. The range of SWE falls within the historical range
of peak SWE at this station (46171 cm), and average peak SWE
for the length of our study is identical to the historical average
(101 cm). Therefore, the range and magnitude of variability in
climate variables seen in our study captures what has been
recorded historically. Winter variables were correlated with each
other (R
>0.62), as were summer variables (R
= 0.66), but
winter variables were not correlated with summer variables.
Relationships Between Climate and Vital Rates. Breeding probability
was inversely related to the length of the previous winter (P=
0.002; Fig. 2). There was no relationship between breeding
probability and either of the summer climate variables. There
was no relationship between survival to 1 yr of age and any of the
winter or summer climate variables.
Survival and transition probabilities depended on winter severity.
Capture-recapture data for 4,279 individual frogs captured over
9 years were analyzed by using program MARK (32), with climate
variables included as group covariates in various combinations.
Model selection results for the capture probability models in-
dicated that probability of initial capture (p) and probability of
recapture (c) varied both across years and among life stages.
Therefore, we used this capture probability structure in all sub-
sequent transition and survival models. Capture probabilities
ranged from 4 to 50%, depending on the year and the life stage.
Models with SWE and last day of winter were far better supported
than any other candidate models (AIC weight = 0.999, model
likelihood = 1.0, 93 parameters). In these models, an increase in
SWE was associated with a decrease in survival for juvenile and
adult stage classes (Fig. 3). Juvenile frogs showed the strongest
relationship with variation in SWE (β=0.042 ±0.005 SE), but
the effect was also signicant in adult females (β=0.037 ±0.011
SE) and adult males (β=0.051 ±0.012 SE). There was no
relationship between SWE and survival for subadult females
(β=0.023 ±0.018 SE).
SWE was inversely related to transition from juvenile to sub-
adult female or male (β=0.029 ±0.007 SE) and transition
from juvenile to adult female (β=0.081 ±0.024 SE). There
was no relationship with transition from subadult to adult female
(β= 0.015 ±0.015 SE).
Demographic Analysis. We used survival and transition parameter
estimates from a time-varyingcapture-recapture model to calculate
annual vital rates (Table S1) to parameterize female-based, post-
birth pulse Leftkovich matrix models for each year of the study
(Fig. 4). Across these matrices, estimates of λwere higher in years
with lower SWE (P= 0.023; Fig. 5A), tended to be lower in years
with a later last day of winter (P= 0.185; Fig. 5B), and were not
related to winter length (P= 0.611).
Lower Basin
Upper Basin
Fig. 1. The Little Rock Creek drainage, Bitterroot Mountains, Montana. All
analyses were based on data collected in the upper basin. Habitat used by R.
luteiventris includes the following: (i) permanent water bodies with no
emergent vegetation used for summer foraging and overwintering (hatch
marks); (ii) permanent ponds and lakes with emergent vegetation used for
breeding, foraging, and overwintering (solid); and (iii) ephemeral ponds
with emergent vegetation used for breeding and foraging (open).
2005 2006
2007 2008
Fig. 2. Linear regression of female breeding probability with length of
previous winter. Longer winters were associated with lower breeding
probabilities in the following spring (P= 0.002).
Survival probability
Peak SWE (cm)
Juvenile Survival Subadult Survival Female Survival Male Survival
Fig. 3. Relationship between stage-specic survival rates in R. luteiventris
and SWE for four age/sex classes: juvenile, subadult female, adult male, and
adult female. The lines are the predicted survival curves for different values
of SWE from the top model.
McCaffery and Maxell PNAS
May 11, 2010
vol. 107
no. 19
Parameters that describe winter severity were negatively corre-
lated with survival, transition, and breeding probabilities in this
high elevation R. luteiventris population. These relationships
resulted in higher estimated λin years with earlier ending winters
and lower snowpack. Climate change predictions for the Rocky
Mountains suggest that snowpack will continue to decrease and
snowmelt will occur at an increasingly earlier date (33). Because
effects of decreased winter severity were uniformly positive, our
results indicate that this climate trend will increase population
viability of R. luteiventris in this mountain system. Researchers
have typically assumed that if climate change affects amphibian
species, the outcome will be negative. Rarely do we allow our-
selves to consider that global warming may confer benets to
some species. Contrary to much of what has been discussed in
the literature (e.g., refs. 6 and 34, but see ref. 35), these results
suggest that under certain circumstances, a warming climate may
be helpful to some amphibian populations, particularly those
that live in harsh conditions at the edge of their thermal toler-
ances. A reduced winter severity could benet high and low el-
evation populations of R. luteiventris alike, although failures in
recruitment due to drying of breeding habitat may overwhelm
positive effects of warmer winters in some populations, especially
at lower elevations and latitudes.
There are several reasons that we might expect R. luteiventris
juvenile and adult survival in these systems to increase with de-
creased snowpack. At high elevations, this species spends up to 8
or 9 months overwintering in lakes and permanent ponds, where
its metabolism slows considerably. Hypoxic conditions have been
shown to be an important source of mortality for overwintering
amphibian populations in high elevation systems (18). Winters
with above-average precipitation had thicker ice covering on lakes
used by mountain yellow-legged frogs (R. muscosa) for over-
wintering, resulting in an increase in the rate of oxygen depletion
(18). Radio-tagged R. luteiventris overwintering in low elevation
ponds in eastern Oregon all remained in shallow water within 1 m
of shore, but they moved to microhabitats with higher water
temperatures or dissolved oxygen concentrations (36). Juvenile
frogs in our system may be more likely to overwinter in shallow
lakes than adult frogs, because we nd them in higher concen-
trations at these water bodies during summer surveys and they
may not be able to locate larger water bodies. Overwintering
in shallow waters may expose juveniles to more hypoxic conditions
in the winter than adult frogs and likely explains the strong
negative associations among SWE and juvenile survival and
transition rates.
Years with higher snowpack tended to have snow on the ground
for a longer time periodand later into the spring. As a result, it is also
possible that high winter severity depletes the fat reserves of frogs
and leads to greater mortality rates. The later the last day of winter,
the longer frogs remain in overwintering sites, and the later insect
prey emerge. This delay in foraging and depletion of fatreserves may
contribute to the negative relationship between SWE and transition
probability to larger age classes, which we observed for juveniles.
The depletion of fat reserves may be less important for subadult and
adult frogs and may explain why we do not see a relationship be-
tween their transition rates and winter severity variables.
In all years of our study, asymptotic estimates of λwere less than
one, suggesting a declining population. This agrees with our ob-
servation that this population has generally declined over the
9 years of the study, from 997 frogs in 2000 to 700 frogs in 2008. A
decreasing population growth rate during most years is consistent
with population growth patterns measured in other amphibian
populations (37, 38). However, in contrast to our asymptotic
estimates of λ, population size uctuated considerably among
years, with some large increases in population size between years.
Therefore, our asymptotic analyses do not capture the range of
stochastic uctuations observed in the eld. For example, it may
be that population dynamics are partly driven by intermittent
pulses of recruitment that were not captured in our 9-year study.
As such, we cannot discern whether a warming climate will actu-
ally lead to a viable population in the long term. However, this
caveat does not change the result that we observed uniformly
positive effects of climate warming.
The results of this study highlight the need for amphibian de-
cline research to focus on environmental variables affecting post-
metamorphic survival parameters and those affecting recruitment
and larval survival (23). Although repeated failures in recruitment
due to drought may critically affect the persistence of some pop-
ulations, changes in juvenile and adult survival could have a greater
effect on population growth and viability in many amphibian
species. Although we saw high annual uctuations in the number
of egg masses laid and successful metamorphs produced in this
system (Table S1), differences in juvenile and adult survival rates,
particularly survival of juvenile frogs, drove the differences we
observed in λacross years. In our population, juveniles and adults
have greater variance in vital rates among years, as well as higher
elasticities in those rates (Table S2). Vital rates for R. luteiventris
juveniles and adults are therefore disproportionately important to
the dynamics of this population. Long-term monitoring of am-
phibian populations has typically focused on variation in re-
Fig. 4. Female-based, postbirth pulse matrix model for R. luteiventris. Each
year, average values for survival, growth, and fecundity were used to cal-
culate the asymptotic population growth rate. Average clutch size was 406
female eggs for all years based on measurements of clutch size.
y = -0.006x + 1.384
R = 0.589
60 70 80 90 100 110 120 130 140
Peak SWE (cm)
y = -0.010x + 2.300
R = 0.290
145 150 155 160 165 170 175 180 185
End of winter (days)
Fig. 5. Linear regression of annual asymptotic λvalues and winter variables,
including SWE (P= 0.021) (A) and end of winter Julian date (P= 0.185) (B).
| McCaffery and Maxell
cruitment or breeding population size (e.g., ref. 37). Past research
has focused on the effect of weather variability on production
of juveniles, which can depend heavily on rainfall in some regions
(39). However, it is less clear to what extent this measured varia-
tion in annual recruitment affects long-term population dynamics
in these systems, because recruitment dynamics are rarely placed
in a population-level context (but see refs. 23 and 40).
Although there was variation in annual recruitment, we never
witnessed complete failures in recruitment, even in the driest years.
Every year, individuals breed in both ephemeral and permanent
water bodies. On cool and wet years, most successful recruitment
comes from ephemeral ponds, which persist throughout the grow-
ing season, whereas tadpoles from colder permanent ponds do not
have enough time to reach metamorphosis. However, in hot, dry
years the majority of recruitment comes from permanent ponds,
because ephemeral ponds dry up before animals are able to suc-
cessfully metamorphose. Therefore, it may be that frogs in our
study system have the ability to compensate recruitment in dry years
through the diversity of breeding sites available across this glacial
basin. The presence of a diversity of unimpacted breeding sites in
these types of systems may be important for amphibian populations
to persist in the face of climate change. In high-elevation systems
where amphibians are negatively impacted by introduced sh (e.g.,
ref. 31), reduction of hydroperiod in ephemeral, shless breeding
sites may be much more important to species persistence. Because
this system is shless, amphibians are able to breed and forage in
a greater diversity of habitats than in areas where sh and other
predators restrict populations to ephemeral ponds and wetlands.
Our analyses suggest that for amphibians and other ectotherms
living at temperatures below their physiological optima, such as
those found at high elevations or latitudes, global warming may
have neutral or positive impacts, at least under some climate
change scenarios (41). However, outcomes will surely depend on
how quickly and to what extent the climate changes. It is possible
that changes in temperature and precipitation may only have
benets to a certain point, after which habitat will be negatively
affected, possibly by changing community structure or reducing
heterogeneity of breeding sites. At the extreme, if ongoing climate
change eventually makes high elevation and latitude sites unsuit-
able, species may have no other refugia to move to (42). Both the
positive and negative impacts of climate change on species will
need to be reassessed as climate change progresses to determine
whether such a tipping point will be reached.
We have shown how individual amphibian vital rates and as-
ymptotic population growth rates vary with summer and winter
climate variables in a high elevation population of the Columbia
spotted frog. These results unambiguously demonstrate that
earlier ending winters with lower snowpack in this system lead to
higher survival rates, higher probabilities of breeding, and higher
population viability. Most research on amphibian declines
assumes that climate change will have negative impacts on al-
ready vulnerable species, yet we show that this may not be the
case for alpine and boreal amphibian populations currently
persisting in harsh environments. This provides a unique per-
spective to the role of climate change in amphibian declines in
temperate ecosystems. Previous shifts in climate have had dra-
matic effects on the distribution, genetics, and ecology of nu-
merous temperate amphibian species (4345). The impacts of
ongoing climate change will vary across the globe, and this is
likely to increase the viability of some species while being det-
rimental to others. To best conserve viable populations, promote
gene ow, and allow for shifts in geographic range in the face of
climate change, developing a more comprehensive un-
derstanding of how climate change is expected to benet or harm
amphibian populations at different latitudes and elevations is
imperative. Ultimately, research that simultaneously evaluates
the effects of climate change on multiple vital rates is key to
disentangling which population processes may be affected by
a warming climate.
Materials and Methods
Population Surveys. We collected demographic data from 2000 to 2008. We
conducted systematic searches for egg masses in late spring. We searched all
shallow water environments for egg masses over several weeks and recorded
countsof egg masses at eachwater body. We calculatedmultiyearestimates and
variancesin clutch size for R. luteiven tris at mostof the breeding ponds by using
volumetric displacement (4648). During the egg mass surveys, we also mea-
suredthe snout-vent lengthof females presentat the breeding siteto determine
the range of size of breeding females. These data were used to distinguish
breeding adult females from subadult females in our demographic analyses.
We useda robust designcapture-mark-recapture methodto monitor juvenile
and adult frogs (49). For this method, we captured animals for multiple con-
secutive secondary sessions (days) within the primary sampling period (year).
Across the secondary sessions, we assumed that the population was closed to
immigration, emigration, births, and deaths. This closure allowed population
size, corrected for capture probability, to be estimated. Between primary ses-
sions,the populationwas open to gains and losses,and survivalwas estimatedby
using the Cormack-Jolly-Seber model (5052). We monitored three female life
stages: juveniles were frogs that were too young to be sexed, subadults were
frogs that were larger than the size at which secondary sex characteristics of
males were pre sent but smaller than the s mallest documente db reeding female,
and adults were frogs large enough to breed. During each primary sampling
period, we systematically surveyed all of the ponds and lakeshores in the basin
each yearand captured animals by handor net. We individually marked animals
by clipping unique combinations of toes by using an alphanumeric coding sys-
tem (53) and weighed and measured snout-vent length. We also recorded the
general location of all new and recaptured animals at each session.
Table 1. Model structures for assessing how climate variables relate to survival and growth
Winter variables Summer variables
Stage + (SWE) Stage + (summer length)
Stage + (end of winter) Stage + (growing degree days)
Stage + (winter length) Stage + (summer length + growing degree days)
Stage + (SWE + winter length) Stage ×(summer length)
Stage + (SWE + end of winter) Stage ×(growing degree days)
Stage ×(SWE) Stage ×(summer length + growing degree days)
Stage ×(end of winter)
Stage ×(winter length)
Stage ×(SWE + winter length)
Stage ×(SWE + end of winter)
For all models, we let pand cvary by both age class and time. We rst estimated survival probabilities,
keeping growth probabilities constant, and then estimated growth probabilities by using the best model from
the survival analysis. For transition models, we examined scenarios where all transitions were different and
where probability of juvenile to male transition was equal to juvenile to subadult transition.
McCaffery and Maxell PNAS
May 11, 2010
vol. 107
no. 19
Climate Data. Climate data were from the Twin Lakes SNOTEL site (www.wcc., located 18 km northwest of the upper Little Rock Creek
basin at 1,950 m elevation. This SNOTEL site is located within the same
mountain range and has similar aspect and elevation to our study area. We
used data on SWE and temperature as annual covariates. SWE is the depth of
water that would theoretically result if one were to melt the entire snowpack
instantaneously and is commonly used as a measure of snowpack (e.g., ref.
21). We used the peak SWE value recorded for each year in our analyses. We
calculated the end of winter Julian date as the last day that SWE was recorded
in the spring. Then we calculated the number of consecutive days with snow
on the ground (winter length) and the number of consecutive days without
snow on the ground (summer length). Finally, we calculated the cumulative
number of days throughout the summer that the temperature was >10 °C
(, which represented
growing degree days. The value of 10 °C was used as a relative physiological
zero for the species, temperatures below which we would not expect to see
growth. Although it is unlikely that this temperature is the true physiological
zero, which is unknown, this cutoff allows for comparison of relative growing
season length across years. We used winter length, last day of winter, and
SWE data as indices of local winter severity, and we used growin g degree days
and summer length as indices of summer intensity.
Wetested for relationshipsamong all climatevariables overthe 9 yearsof the
study by using principal components analysis. The rst two axes explained 89%
of the variance. Axis 1 (56% of variance) was correlated with winter severity (r>
0.85 for all winter variables; r<0.53 for all summer variables). Axis 2 (33% of
variance) was correlated with summer variables (r>0.75 for all summer vari-
ables; r<0.40 for all winter variables). Therefore, we can clearly distinguish
winter from summer variables but cannot statistically separate individual
winter or summer variables. However, we chose to analyze all variables in-
dividually to discuss hypothetical mechanisms associated with each variable.
Breeding Probability and Prejuvenile Analysis. We estimated breeding prob-
ability as the number of egg masses deposited each year divided by the
number of adult females that year (closed population estimate from the
mark-recapture data). We estimated survival from eggs to 1 year for each year
by dividing the number of 1-year-old frogs by the number of eggs laid the
previous spring (average number of eggs per mass multiplied by the number
of egg masses deposited). We used an average of 812 eggs per mass (assumed
to be equivalent to 406 female embryos given a 1:1 sex ratio) from our clutch
size estimates for all years of the analysis. To estimate the number of 1-year-
old frogs, we isolated the capture histories for all animals 34 mm snout-vent
length and smaller each year and then calculated the abundance of those
animals by using Huggins closed population models in program MARK (32).
We used weighted linear regressions to examine the dependence of
breeding probability and rst-year survival on the ve climate variables
described above. Additionally, we examined relationships between number
of egg masses deposited and climate variables.
Post-Metamorph Analysis. We analyzed capture data of juveniles, subadults,
and adults in program MARK by using closed robust design, multistate mark-
recapture models (54, 55). The statesin our models were frog life stages:
juvenile, subadult female, adult female, and adult male frogs. These models
provided parameter estimates and variances for age- and sex-specic survival,
transition rates between life stages, and population size for each year (56, 57).
Survival, transitions, and the covariates were our primary parameters of in-
terest, but we rst evaluated models of capture probability (p) and recapture
probability given initial capture (c) to avoid bias and imprecision in the sur-
vival estimates (58). We evaluated the following capture probability models:
(i)pand cwere constant across years but varied among age classes, (ii )pand c
varied across years but did not vary among age classes, (iii )pand cvaried
across years and differed between juvenile and adult age classes, but not
within adult age classes, and (iv)pand cvaried across years and among all age
classes. For these models, survival and transition rates were held constant.
We modeled age-specic survival and transition probabilities to examine
their variation in relation to snowpack, winter length, end of winter, summer
length, and growing degree-days. First, we examined how each of these
variables related to survival in each age class individually. Then, we examined
whether additive models containing multiple climate variables improved the
t. For each model structure, we estimated models where (i) the effect of
covariates was the same for each age class and (ii ) the effect of covariates
was different for each age class, resulting in a total of 16 basic models (Table
1). Once we tested these models, we also examined two additional models
where (i) male survival was equal to female survival and (ii) all adult age
classes had the same survival. For these models, we kept transition proba-
bilities constant. Once we had modeled survival, we examined how climate
variables affected growth by using the structure from the best survival
model. We examined the same suite of variables for growth as we did for
survival. In addition to the 16 models described above, we estimated models
where probability of transitioning from juvenile to subadult was equal to
transitioning to male (Table 1). We evaluated all models for relative support
and ranked them by using Akaikes Information Criterion (AICc) (59, 60).
Demographic Analysis. We determined the demographic consequences of
changes in climate variables on the population growth rate using matrix
models (19). We constructed female-based postbirth pulse stage-structured
matrix models by using the average vital rates estimated for each year (Table
S1 and Fig. 4). Survival and transition parameters came from the best time-
dependent model ranked by using AICc. We tested four time-dependent
models where survival varied by both year and life stage: (i) survival varies in
the same way for each life stage in each year; (ii ) juvenile survival varies dif-
ferently from subadult, male, and female survival, which vary in the same way
each year; (iii) male and female survival vary in the same way, but both ju-
venile and subadult survival vary differently in each year; and (iv) all life stages
varied differently from each other in each year. The best model varied tran-
sitions for each life stage and year, but transition probability from juvenile to
subadult was equal to that for juvenile to male. Capture and recapture
probabilities varied by year and life stage for all models. Other vital rates were
calculated as described above. For each year, we calculated asymptotic λ,the
rate at which a population would increase if vital rates remained constant
over time. This metric represents an integrative measure of population per-
formance. We then used linear regression of the asymptotic lambda values
for each year against values of climate variables for each year to see whether
this integrative metric showed similar patterns to individual vital rates.
ACKNOWLEDGMENTS. We thank the many eld assistants who helped
collect the demographic data used in this study and K. Grifn for assistance
with the mark-recapture analyses. We thank E. E. Crone, L. Eby, P. S. Corn,
L. S. Mills, W. H. Lowe, and two anonymous reviewers for helpful comments
and insights on analyses and drafts of the manuscript. Fieldwork was partly
supported with funding from the US Geological Surveys Amphibian Re-
search and Monitoring Initiative through cooperative agreements among
the US Geological Survey, the University of Montana, and the Montana
Natural Heritage Program. Research was also partly supported by US Forest
Service Region 1 Inventory and Monitoring grants (to B.A.M.).
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McCaffery and Maxell PNAS
May 11, 2010
vol. 107
no. 19
... In colder climates, anurans survive the winter by seeking shelter underwater or underground to avoid freezing temperatures (Swanson & Burdick, 2010 Many amphibians use temperature and precipitation cues to guide reproduction onset (Blaustein et al., 2001(Blaustein et al., , 2010, which affects the timing of breeding and subsequently, the time available for development and metamorphosis. Shorter winters may allow for earlier breeding, providing additional time for growth and development, which can increase survival and reproductive fitness (Corn, 2005;McCaffery & Maxell, 2010;Sinsch & Schäfer, 2016). This effect may be especially important for juveniles, as smaller individuals may be more susceptible to winter mortality (Sinsch & Schäfer, 2016) and winter conditions may have carryover effects on survival and fitness (Newman, 1992). ...
... For example, in some systems, snowmelt runoff determines the habitat suitability for wood frog (Lithobates sylvaticus) breeding and development (Donald et al., 2011). Substantial reductions in winter precipitation may reduce the amount of water available for feeding and reproduction during warmer months, as groundwater levels may not raise high enough to support wetlands or ephemeral pools during spring and summer amphibian breeding seasons (Greenberg et al., 2017;McCaffery & Maxell, 2010). ...
... Short winters with low snowpack have been associated with higher survival rates, higher breeding probabilities, and higher population viabilities in montane frogs (McCaffery & Maxell, 2010). These warm winters reduce the risk that hibernating individuals will be exposed to killing cold (McCaffery & Maxell, 2010). ...
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Aim Climate change is an increasingly important driver of biodiversity loss. The ectothermic nature of amphibians may make them particularly sensitive to changes in temperature and precipitation regimes, adding to declines from other threats. While active season environmental conditions can influence growth and survival, effects of variation in winter conditions on population dynamics are less well‐studied. Given that extreme winter temperatures can influence amphibian survival and fitness, we expected that increased winter severity—as measured by variability in winter temperatures and snow cover—would be associated with decreased occupancy, and that populations that experience more severe winters would have the largest sensitivities and show the greatest declines. Location Eastern United States. Time period 2001–2015. Major taxa studied Anurans. Methods We used large‐scale citizen science data from the eastern half of the United States, a diverse biogeographic and climatic region, to assess how variation in winter severity influenced occupancy dynamics (i.e. presence or absence of species across sites and years) of 11 spring and summer breeding anuran species. Results Most species had increased occupancy in years with greater than average snow cover and warmer than average mean winter temperatures. Surprisingly, climatic conditions in winter affected occupancy dynamics of species with varying life history characteristics, including both spring and summer breeding species, those that overwinter under the soil, and those that overwinter in ponds and stream beds. For two wide‐ranging species (Lithobates catesbeianus and Lithobates clamitans), colder winter temperatures reduced occupancy more at northern latitudes, while the association between days of snow cover and latitude was equivocal. Main conclusions As the climate continues to change, expected reductions in snowpack may reduce occupancy of already declining anuran populations, while milder winters may improve overwinter survival for some species. The contradictory impacts of temperature and snow cover illustrate the importance of considering multi‐dimensional impacts of climate change on anuran populations.
... In a study by Ref. [109] on Bufo bufo under laboratory conditions, it was found that shorter winters and more moderate temperatures during hibernation had a positive effect on the survival of toads and body mass changes. The positive effect of mild and shorter winters has also been reported in other studies [110,111]. Great seasonal variations in immunity of ectotherms usually occur with maximal immune responses during the summer season [112]. Studies on amphibians showed that in cold seasons, the possibility of spreading diseases increases [113,114]. ...
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Persistence and coexistence of many pond-breeding amphibians depend on seasonality. Temperature , as a seasonal climate component, affects numerous physical and biological processes of pond-breeding amphibians. Satellite-derived land surface temperature (LST) is the radiative skin temperature of the land surface, which has received less attention in spatiotemporal seasonal habitat monitoring. The present study aims to evaluate the increasing and decreasing effects of LST trends at two levels: (1) habitat suitability and connectivity; (2) individual population sites and their longitudinal distribution (with increasing longitude). Habitat suitability modeling was conducted based on an ensemble species distribution model (eSDM). Using electrical circuit theory, the connectivity of interior and intact habitat cores was investigated. An average seasonal LST was prepared separately for each season from 2003 to 2021 and entered into Mann-Kendall (MK) analysis to determine the spatiotemporal effects of LST changes using the Z-Score (ZMK) at two confidence levels of 95 and 99%. Based on the results, in winter, 28.12% and 70.70% of the suitable habitat were affected by an increasing trend of LST at 95% and 99% confidence levels, respectively. The highest spatial overlap of the decreasing trend of LST with the suitable habitat occurred in summer and was 6.4% at the 95% confidence level and 4.2% at the 99% confidence level. Considering population site at 95% confidence interval, the increasing trend of LST was calculated to be 20.2%, 9.5%, 4.2%, and 6.3% of localities in winter, spring, summer, and autumn, respectively. At the 99% confidence level, these percentages reduced to 8.5%, 3.1%, 1%, and 1%, respectively. During winter and summer, based on the results of the longitudinal trend, an increasing trend of LST was observed in sites. Localities of Hatay and Iica village in Turkey experienced seasonally asynchronous climate change regimes. The approach used in this study allowed us to create a link between the life cycle and seasonal changes on a micro-scale (breeding sites) and macro-scale (distribution and connectivity). Findings of this paper can be effectively used by conservation managers to preserve S. infraimmaculata's metapopulation.
... One of the research areas pertaining to the effects of climate change on species entails measuring the expected shift in the ranges they will experience in the future. Changes in geographic distribution can occur because climate change affects population growth and their survival or the ability to colonise new areas (McCaffery & Maxell, 2010), mediated by the species' physiological adaptation to a range of environmental conditions (Greenberg & Palen, 2021). Modelling habitat suitability across time using current data is commonly used to predict how amphibian ranges will change, an event shaped by the effect of climate change (see for example García & Ortega-Huerta, 2013;Duan et al., 2016;Agudelo, Urbina-Cardona & Armenteras-Pascual, 2019;Kim et al., 2021). ...
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The Montseny massif shelters the southernmost western populations of common frogs (Rana temporaria) that live in a Mediterranean climate, one which poses a challenge for the species' persistence in a scenario of rising temperatures. We evaluated the effect of climate change at three levels. First, we analysed if there has been an advancement in the onset of spawning period due to the increase in temperatures. Second, we analysed the impact of climatic variables on the onset of the spawning period and, third, how the distribution of this species could vary according to the predictions with regard to rising temperatures for the end of this century. From 2009 to 2021, we found there had been an increase in temperatures of 0.439 C/decade, more than the 0.1 C indicated by estimates for the second half of the previous century. We found an advancement in the onset of the reproduction process of 26 days/decade for the period 2009-2022, a change that has been even more marked during the last eight years, when data were annually recorded. Minimum temperatures and the absence of frost days in the week prior to the onset of the spawning period determine the start of reproduction. Predictions on habitat availability for spawning provided by climatic niche analysis for the period 2021-2100 show a potential contraction of the species range in the Montseny and, remarkably, much isolation from the neighbouring populations.
... Intriguingly, it appears as if earlylife losses are discounted for in birth rates (Honeycutt et al. 2019). For example, the survival rates of adult tailed frogs are similar to those of other long-lived, pond-breeding anurans in the region that are much more fecund than tailed frogs (McCaffery & Maxell 2010;Muths et al. 2010;Honeycutt et al. 2019). The similar survival rates among adults of these species suggest that ontogenescence in the highly fecund species is likely much stronger than for species such as tailed frogs that lay comparably few eggs. ...
... The cool temperatures at high altitudes may exacerbate the negative effects of UVR on the physiological function of individuals [23,25]. However, a moderately warming climate may have positive effects on amphibians, accelerating the metamorphosis of tadpoles and thus improving the survival rate of the population [2,26]. However, empirical evidence for the interaction of a warming climate and UVR on amphibians living at high altitudes, and the relevant mechanisms involved, is still limited. ...
Full-text available
Both the warming climate and ultraviolet-B radiation (UVBR) are considered to be notable environmental factors affecting amphibian population decline, with particular effects on tadpole development. However, the phenotypes of tadpoles living at high altitudes may be improved by moderately warming temperatures, reducing or eliminating the negative effects of oxidative damage caused by cool temperatures or strong UVBR at high altitudes. To verify this hypothesis, Rana kukunoris tadpoles, which live at high altitudes, were used to test the effect of the interaction of temperature and UVBR on their development and antioxidant systems in a fully factorial design. The tadpoles were exposed to UVBR and UVBR-free environments at 14 (cool temperature) and 22 °C (warm temperature), respectively. UVBR and a warm temperature had opposite influences on several traits of the tadpoles, including their survival, developmental rate, individual size, preferred body temperature, thermal tolerance temperature, oxidative damage, and enzymatic and nonenzymatic antioxidant systems. The moderate temperature could compensate for or override the negative effects of UVBR by increasing the tadpoles’ preferred body temperature and critical tolerance temperature, thus enhancing the locomotion ability and thermal sensitivity of their antioxidant systems. Furthermore, the dark skin coloration and aggregation behavior of R. kukunoris tadpoles may also be effective strategies for allowing them to resist UVBR and helping them to better adapt to a warming environment with stronger UVBR. Thus, it is possible that a moderate degree of warming may increase the capacity of living organisms to adapt to environmental changes and thus have positive effects on the development of tadpoles living at high altitudes.
... Bd infects the keratinized epidermis of metamorphosed and adult amphibians as well as the tooth rows and jaw sheaths of larvae (Berger et al., 1998;Longcore et al., 1999;Vredenburg and Summers, 2001). While Bd is present across the CSF range, widespread population declines have not been observed (McCaffery and Maxell, 2010;Hossack et al., 2013) potentially because CSF are known to have skin peptides that are highly resistant to chytrid fungus (Rollins-Smith et al., 2002). Even if CSF populations demonstrate some resistance to chytrid fungus, other amphibians are susceptible. ...
Full-text available
The Columbia Spotted Frog (Rana luteiventris; CSF) is widely distributed across northwestern North America; however, declines in the southernmost populations, including those in Utah, have resulted in the consideration of this species for protection under the Endangered Species Act. In 1998, a conservation agreement and strategy for Utah's populations of CSF was developed and identified needed conservation actions, including range expansion. We repatriated CSF larvae during 2008-2010 from an extant population in the Provo River into Beaver Creek, a beaver-dominated stream, in the Weber River, a watershed where contemporary surveys indicate CSF have likely been extirpated. In 2011, CSF breeding was first observed in the repatriated population when 11 egg masses were documented in four depositional areas. After ten years of monitoring egg mass numbers, we consider the repatriation a success as this population continues to grow and expand with a high of 54 egg masses (2019) within ten depositional areas (2020). High quality habitat and the large number of CSF larvae transplanted likely attributed to the success of this repatriation. We used 1-2 day old CSF larvae (Gosner life stage 20-21) as the repatriation life stage that we believed would be the most likely to prevent the spread of amphibian chytrid fungus (Batrachochytrium dendrobatidis, Bd) from the known chytrid fungus positive donor site in the Provo River. Genetic testing of a robust sample (n ¼ 59) of CSF tadpoles across the repatriation site in 2020 did not detect the presence of Bd, potentially indicating that we did not move Bd through the repatriation. Additional replicates would be required beyond this single experiment, however, to better determine if our transplant techniques are effective at preventing the spread of Bd.
Full-text available
Context Climate change and anthropogenic stressors have contributed to rapid declines in biodiversity worldwide, particularly for amphibians. Amphibians play important ecological roles, yet little is known about how distribution hotspots may change or the factors in uencing distribution patterns in the North American Great Plains. Objectives Ecological niche models improve understanding of biotic and abiotic factors associated with species' distributions and can highlight potential threats to species conservation. Here, we identify important predictors of amphibian distributions and predict how land use and climate change may alter distributions in the Upper Missouri River Basin. Methods We used publicly available occurrence data, 16 environmental and climatic predictors, and the machine-learning algorithm, Random Forests, to create spatially-explicit distribution models for eight amphibian species. Models were scored to current conditions (2005) and two future climate-change/land-use scenarios to predict changes in amphibian distributions for 2060. Results Models were highly accurate and revealed more pronounced distributional changes under the intensive RCP8.5/CONUS A2 scenario compared to the moderate RCP6.0/CONUS B2 scenario. Both scenarios predicted gains for most southeastern species (i.e., Blanchard's cricket frogs, Plains leopard frogs, Woodhouse's toads, and Great Plains toads) and declines for all western montane species. Overall, distribution changes were most in uenced by climatic and geographic predictors, (e.g., summer temperature, precipitation, and elevation), and geography, versus anthropogenic land-use variables. Conclusions Changes in occurrence area varied by species and geography, however, high-elevation western species were more negatively impacted. Our distribution models provide a framework for future conservation efforts aiding the persistence of amphibian species across a warming, agriculturally dominated landscape.
Amphibians naturally occur in metapopulations characterized by spatially separated breeding habitats connected by dispersing individuals. The rate at which individuals grow to maturity, size of the metapopulation, and movement behavior varies widely across amphibian species, and their compounding interactions play a large role in population dynamics and viability. When populations in a connected network exhibit cyclic behavior the level of synchrony between populations is important for assessing extinction risk. In addition, the qualitative behavior of fluctuations provides insight into the patterns of the population cycles and can be used to predict forward trajectories in time. Chaotic oscillations, characterized by aperiodic cycles and sensitivity to initial conditions, are known to amplify noise, thus lowering population synchrony; however, other oscillation types (invariant cycles, k-cycles) have not been explicitly explored in relation to synchrony. In this paper, we investigate the relationship between synchrony and oscillation type for a two-patch system of a species with 1, 2, and 3 life-history stages. Using dynamical systems analysis, we determine the mechanisms that induce the different oscillation types and relate them with dispersal rates and synchrony. We find that dispersal has a greater effect on population dynamics of a species with 1 life-history stage compared to the subtle changes in dynamics found for species with 2 and 3 life-history stages. For low levels of dispersal, oscillating populations are driven to equilibrium as synchrony increases. Under medium to high levels of dispersal, oscillations may be created from equilibrium with low levels of synchrony. In general, chaos does not have noticeably lower synchrony than other oscillation types but has synchrony levels comparable to the oscillation types surrounding chaos. In this study, we cover a broad range of dispersal probabilities and life histories intended for general amphibian systems. The variety of results found in our analysis emphasizes the importance of determining model parameters and life history assumptions when studying specific amphibian species to ensure that the resulting dynamics accurately reflect the system.
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Animals that reproduce in temporary aquatic systems expose their offspring to a heightened risk of desiccation, as they must race to complete development and escape before water levels recede. Adults must therefore synchronise reproduction with the changing availability of water, yet the conditions they experience to trigger such an event may not relate to those offspring face throughout development, potentially leading to clutch failure. The sandpaper frog (Lechriodus fletcheri) breeds in ephemeral pools that dry within days to weeks after rainfall has ceased. We examined whether spawning frequency and offspring survival differed across two consecutive breeding seasons based on (1) rainfall at the moment of oviposition and throughout offspring development, and (2) pool volume, given their combined effect on hydroperiod. Reproduction was triggered by rainfall, with more spawn laid during periods of greater rainfall and in larger pools. While pool size was a predictor of offspring survival, rainfall during oviposition was not. Rather, follow-up rain events were required to prevent pools drying prior to metamorphosis, with rainfall evenness during development the strongest predictor of reproductive success. High clutch failure rates recorded in both seasons suggest that adults do not have the capability to predict rainfall frequency post-oviposition. We thus conclude that unpredictable rainfall leading to premature desiccation of spawning sites is the primary source of pre-metamorphic mortality for this species. Understanding the influence of rainfall predictability on offspring survival could be critical in predicting the effects of altered hydroperiod regimes due to climate change for species that exploit temporary waters.
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This chapter describes a 16-year study, in which it has been found that pond hydroperiod is a primary source of variation in community structure for a natural community of pond-breeding amphibians. Larval competition and predation form other axes that are positioned along a continuum of hydroperiod, and the strength of their influence on the success of species is mediated by pond hydroperiod. Although hydroperiod, competition, and predation had a detectable influence on the amphibian community at Rainbow Bay, the effects of these factors were often difficult to separate. Correlative analyses are less powerful for sorting out confounding factors than manipulative experiments in replicated artificial ponds. The predictor variables used are often themselves correlated. Nevertheless, in many cases, a good year for a species is also a good year for its competitors and predators. Juvenile recruitment of all species is limited by a short hydroperiod in the driest years. In years with longer hydroperiods, the density of competitors affected the number of metamorphosing juveniles per breeding females for some species. The density of salamander larvae is also a significant predictor of per-capita juvenile recruitment for anurans. A significant negative relationship is detected for two of four anuran species analyzed, most likely due to predation by the salamander larvae on the anuran tadpoles. These results indicate that community structure, at least in terms of relative abundances, varied continuously. However, regulation of community structure within a pond occurs through the predictable interaction of rainfall, hydroperiod, competition, and predation.
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The impact of anthropogenic climate change on terrestrial organisms is often predicted to increase with latitude, in parallel with the rate of warming. Yet the biological impact of rising temperatures also depends on the physiological sensitivity of organisms to temperature change. We integrate empirical fitness curves describing the thermal tolerance of terrestrial insects from around the world with the projected geographic distribution of climate change for the next century to estimate the direct impact of warming on insect fitness across latitude. The results show that warming in the tropics, although relatively small in magnitude, is likely to have the most deleterious consequences because tropical insects are relatively sensitive to temperature change and are currently living very close to their optimal temperature. In contrast, species at higher latitudes have broader thermal tolerance and are living in climates that are currently cooler than their physiological optima, so that warming may even enhance their fitness. Available thermal tolerance data for several vertebrate taxa exhibit similar patterns, suggesting that these results are general for terrestrial ectotherms. Our analyses imply that, in the absence of ameliorating factors such as migration and adaptation, the greatest extinction risks from global warming may be in the tropics, where biological diversity is also greatest. • biodiversity • fitness • global warming • physiology • tropical
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We studied behavior and locations of ovewintering Columbia spotted frogs in northeastern Oregon. We monitored 66 radio-tagged frogs as they moved to overwinterirg sites during 1997-2000. Frogs used a diversity of overwintering sites, but alI sites had an aquatic component including ice-covered ponds (44%). partially frozen ponds (29%), lotic habilats (23%), and temporary backwaters and seeps (4%). The distance between the original point of frog capture in August-September and the overwintering site varied from 15 to 1200 m. lndividuals in ponds were active all winter and remained in shallow rater within I m of the shore. Frogs overwintering in ponds selected microhabitats wilh significantly higher water temperalures and djssolved oxygen concentrations compared to other locations in the ponds. Movements during the overwintering period appeared to be linked to water temperatures and dissolved oxygen concentrations.
Between 1978 and 1988, we recorded reproductive information from populations of ranid frogs in Colorado and Wyoming. Egg masses from five plains and montane populations of northern leopard frogs (Rana pipiens) contained 645-6272 eggs (x̄ = 3045, N = 68 egg masses). In two montane populations of wood frogs (Rana sylvatica) numbers of eggs per egg mass varied from 711-1248 (x̄ = 876, N = 15) and probably were equal to total clutch size. Mean hatching success was 90% in egg masses from one R. sylvatica population and ranged from 70% to 99% in R. pipiens egg masses. Rana pipiens egg masses from one location were assigned to three overlapping size distributions, which we believe reflects the underlying age structure of female frogs.
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Both larval and metamorphosed mountain yellow-legged frog over-winter for 6-9 mo in ice-covered lakes and streams at high elevation in California and Nevada. In some winters almost all the frogs in shallow lakes (<4 m deep) die. This mortality is associated with oxygen depletion, which occurs most rapidly in shallow lakes. However, tadpoles survive for months in nearly anoxic conditions when shallow lakes are frozen to the bottom. Quantification of parameters from laboratory studies is discussed. -from Author