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Climate-associated decline of body condition in a fossorial salamander

Abstract

Temperate ectotherms have responded to recent environmental change, likely due to the direct and indirect effects of temperature on key life cycle events. Yet, a sub- stantial number of ectotherms are fossorial, spending the vast majority of their lives in subterranean microhabitats that are assumed to be buffered against environmen- tal change. Here, we examine whether seasonal climatic conditions influence body condition (a measure of general health and vigor), reproductive output, and breed- ing phenology in a northern population of fossorial salamander (Spotted Salamander, Ambystoma maculatum). We found that breeding body condition declined over a 12- year monitoring period (2008–2019) with warmer summer and autumn temperatures at least partly responsible for the observed decline in body condition. Our findings are consistent with the hypothesis that elevated metabolism drives the negative associa- tion between temperature and condition. Population-level reproduction, assessed via egg mass counts, showed high interannual variation and was weakly influenced by autumn temperatures. Salamander breeding phenology was strongly correlated with lake ice melt but showed no long-term temporal trend (1986–2019). Climatic warm- ing in the region, which has been and is forecasted to be strongest in the summer and autumn, is predicted to lead to a 5%–27% decline in salamander body condition under realistic near-future climate scenarios. Although the subterranean environment offers a thermal buffer, the observed decline in condition and relatively strong ef- fect of summer temperature on body condition suggest that fossorial salamanders are sensitive to the effects of a warming climate. Given the diversity of fossorial taxa, heightened attention to the vulnerability of subterranean microhabitat refugia and their inhabitants is warranted amid global climatic change. https://doi.org/10.1111/gcb.15766
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1 | INTRODUCTION
Global climate change is unequivocal, and rates of observed and
predicted temperature increases are greater at higher latitudes
(Intergovernmental Panel on Climate Change, 2014). High- and
mid- latitude regions have experienced rapid environmental change
over the past half- century, including increases in mean air and sur-
face temperature, extreme high temperature events, decreases in
the number of frost- free days, and decreases in ice cover (Bar tolai
et al., 2015; Cohen et al., 2014). The short post- glacial history of
the Northern hemisphere mid- latitudes, combined with regional
geology, climate, and varied habitat types, makes this region the
Received: 21 March 2021 
|
Accepted: 27 April 2021
DOI: 10.1111/gcb.15766
PRIMARY RESEARCH ARTICLE
Climate- associated decline of body condition in a fossorial
salamander
Patrick D. Moldowan1,2,3 | Glenn J. Tat t ers a ll4| Njal Rollinson1,2
1Depar tment of Ecology a nd Evolutionary
Biolog y, University of Toronto, Toronto,
ON, Canada
2School of the Environment , Univer sity of
Toronto, Toronto, ON, Canad a
3Algonquin Wildlife Research Station,
Whitney, ON, Canada
4Depar tment of B iological Scie nces, Brock
University, St. Catharines, ON , Canada
Correspondence
Patrick D. Moldowa n, Depa rtme nt
of Ecology and Evolut ionar y Biology,
University of Toronto, Toronto, ON M5S
3B2, Canada.
Email: pat rick. moldowan@gmail.com
Funding information
This research was financially supported
by Ontar io Parks; Town of Huntsville
Environmental Research Bursa ry,
graduate student research award from the
Centre fo r Globa l Change Science at t he
University of Toronto, Beatrice and Ar thur
Minden G raduate Research Fellowship at
the Unive rsity of Toronto School of the
Environment, an d a CGS- D award from
the Natural Scie nces and Enginee ring
Research Council of Canada (NSERC) to
PDM; NSERC Discover y Grant (NSERC
RGPIN- 05814) to GJT; Connaught Early
Career Award and N SERC Discovery
Grant (RG PIN- 2016- 06469) to NR; and
the Research Excursion Program f rom the
Faculty of Arts and Science, Universit y of
Tor on to.
Abstract
Temperate ectotherms have responded to recent environmental change, likely due
to the direct and indirect effects of temperature on key life cycle events. Yet, a sub-
stantial number of ectotherms are fossorial, spending the vast majority of their lives
in subterranean microhabitats that are assumed to be buffered against environmen-
tal change. Here, we examine whether seasonal climatic conditions influence body
condition (a measure of general health and vigor), reproductive output, and breed-
ing phenology in a northern population of fossorial salamander (Spotted Salamander,
Ambystoma maculatum). We found that breeding body condition declined over a 12-
year monitoring period (2008– 2019) with warmer summer and autumn temperatures
at least partly responsible for the observed decline in body condition. Our findings are
consistent with the hypothesis that elevated metabolism drives the negative associa-
tion between temperature and condition. Population- level reproduction, assessed via
egg mass counts, showed high interannual variation and was weakly influenced by
autumn temperatures. Salamander breeding phenology was strongly correlated with
lake ice melt but showed no long- term temporal trend (1986– 2019). Climatic warm-
ing in the region, which has been and is forecasted to be strongest in the summer
and autumn, is predicted to lead to a 5%– 27% decline in salamander body condition
under realistic near- future climate scenarios. Although the subterranean environment
offers a thermal buffer, the obser ved decline in condition and relatively strong ef-
fect of summer temperature on body condition suggest that fossorial salamanders
are sensitive to the effects of a warming climate. Given the diversity of fossorial taxa,
heightened attention to the vulnerability of subterranean microhabitat refugia and
their inhabitants is warranted amid global climatic change.
KEYWORDS
Ambystoma maculatum, body condition, climate change, ecophysiology, metabolic rate,
microhabitat, phenolog y, reproduction
1726 
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    MOLDOWAN et AL.
northern range edge of many cold- adapted ectotherms (Lesbarrères
et al., 2014; Seburn & Bishop, 2007; Sunday et al., 2011). Some of
these temperate, cold- adapted species may respond to climate
change with latitudinal and altitudinal range shifts, and indeed,
such shifts are increasingly documented among terrestrial species
(Chen et al., 2011; Hughes, 2000; Walther et al., 2002). However,
not all taxonomic groups are highly mobile and capable of rapid or
long- distance dispersal in response to unfavorable environment al
conditions. For instance, the slow dispersal of many ectothermic
vertebrates, including some amphibians, relative to the accelerating
rate of climate change imposes hard limitations on geographic range
shifts as a response to climate change (Blaustein et al., 2010).
Amphibians— especially high latitude, mid latitude, and northern
range edge populations— are expected to respond strongly to climate
change due to their specific reproduc tive requirements, complex
life histories, and often short breeding period (Daszak et al., 2005;
Fitzpatrick et al., 2020). Climate- induced shifts in reproductive tim-
ing and biology are very well reported for anurans (Beebee, 1995a,
1995b; Gibbs & Breisch, 2001; Klaus & Lougheed, 2013; McCarty,
2001; Sheridan et al., 2018; Terhivuo, 1988; Todd et al., 2011;
Tryjanowski et al., 2006; Walpole et al., 2012). Of broader concern,
however, is that climatic change is negatively impacting amphibian
populations by reducing net resource acquisition rates of individu-
als and/or inducing physiological (temperature and/or water) stress,
leading to lower body condition and curtailed reproductive efforts.
Decreases in anuran body size, body condition, and fecundity, for
example, have been attributed to increases in temperatures or proxy
measures thereof (Benard, 2015; Lannoo & Stiles, 2017; Reading,
2007; Sheridan et al., 2018). Amphibian responses to a changing en-
vironment are complex and have been shown to vary in a number of
ways. For example, warmer winters were correlated with an increase
in body size in two species of European ranid frogs (Tryjanowski
et al., 2006). Annual drought severity, including the interplay of tem-
perature and precipitation, was correlated with decline in Crawfish
Frog (Lithobates areolatus) body condition and fecundity (Lannoo
& Stiles, 2017). Regional changes in frost- free days and precipita-
tion across Nor th America explain sex- specific responses in body
size, including body size increases and decreases, in the Wood Frog
(Lithobates sylvaticus) over the past century (Sheridan et al., 2018).
Climatic warming and drying have been implicated in reducing body
size of plethodontid salamanders in eastern Nor th America (Caruso
et al., 2014; but see Connette et al., 2015). In sum, there is strong
evidence that the breeding biology and life cycles of amphibians,
among other taxa, are responding to rapid climate change.
The cryptic and relatively fossorial nature of many amphibians
has generally impeded research into relationships between climate
change and biology (but see Beebee, 1995a, 1995b; Kirk et al., 2019;
Kusano & Inoue, 2008; Todd et al., 2011). Yet, fossorial lifest yles are
common in amphibians: an estimated 11% of known amphibian spe-
cies (723 spp.) associate with underground environments, including
7% of frogs (397 spp. of Anura), 23% of salamanders (145 spp. of
Caudata), and 97% of caecilians (181 spp. of Gymnophiona; Oliveira
et al., 2017). Although non- fossorial amphibians are likely to bear
the brunt of rapid warming, fossorial species have been largely over-
looked in climate change studies, perhaps owing to the untested
assumption that they are safeguarded by living in a thermally buf f-
ered underground environment. Subterranean- dwelling Ambystoma
salamanders, for instance, demonstrate strong dependence on
temperature and precipitation to signal aboveground migration and
breeding, but bouts of surface activity are shor t (Blanchard, 1930;
Douglas, 1979; Sexton et al., 1990). Thus, subterranean microhab-
itat use may mediate exposure to thermal and moisture extremes,
thereby allowing individuals to persist within their physiological
tolerances in otherwise inhospitable ambient environments (Moore
et al., 2018; Schef fers et al., 2013; Schef fers, Edwards, et al., 2014).
Fossorial lifestyles in amphibians are, in fact, broadly associated with
temperate regions characterized by climatic variabilit y, high tem-
perature variation, and/or low precipitation (Oliveira & Scheffers,
2019), suggesting that below- ground microhabitat use mediates cli-
matic extremes, allowing persistence in challenging above- ground
environments.
If fossorial salamanders demonstrate sensitivity to climatic
change, then there could be broad repercussions, as salamanders
contribute important ecological roles, including trophic structuring,
leaf litter and soil nutrient cycling, and carbon sequestration (Best
& Welsh, 2014; Davic & Welsh, 2004). The goal of this study is to
explore the thermal sensitivity of body condition (i.e., general health,
vigor) and key lifecycle events of a fossorial amphibian, leveraging
a long- term dataset on the Spotted Salamander (Ambystoma macu-
latum; Shaw, 1802). Since 1986, Spotted Salamander reproductive
biology and breeding phenology has been studied non- continuously
in their northern distribution in Algonquin Provincial Park, Ontario,
Canada. Concurrent with global and regional climate change,
changes in seasonal temperature and precipitation have occurred in
Algonquin Provincial Park over the past half- centur y (Lemieux et al.,
2007; Ridgway et al., 2018; Waite & Strickland, 2006). Our first
objective was to estimate the relationship between annual climate
(temperature, precipitation, and ice conditions) and body condition,
population- level reproductive output, and breeding phenology for
the Spotted Salamander. Our second objective was to predict trends
in salamander breeding body condition under realistic near future
(2050– 2100) climate scenarios. Our third objective was to esti-
mate longitudinal trends in the reproductive biology of the Spotted
Salamander.
2 | METHODS
2.1  |  Study species and area
The Spotted Salamander (A. maculatum) is a medium- bodied mem-
ber of the mole salamander group and is widespread in the forests of
eastern North America. The species is a not true burrower (Semlitsch,
1983), instead relying on the burrows created by small mammals (e.g.,
Blanaria, Peromyscus, Tamia s ; Faccio, 2003; Kleeberger & Werner,
1983; Madison, 1997; Montieth & Paton, 2006; Windmiller, 1996).
   
|
  1727
MOLDOWAN et AL.
Brief periods of aboveground activity, limited to late winter/early
spring breeding and autumn movement, are strongly cued by weather,
namely rainfall and spring thaw at northern latitudes (Baldauf, 1952;
Madison, 1997; Sexton et al., 1990). Spotted Salamanders are not
freeze- tolerant and overwinter below the frost line (Madison, 1997).
Breeding occurs in shallow water and females can lay multiple egg
masses during a single spring reproductive period (Petranka, 2010).
Long- term observations suggest that females in our study population
do not breed annually and/or are highly transient at the breeding site
(P.D. Moldowan, unpublished data).
Bat Lake in western Algonquin Provincial Park is a naturally
acidic (pH 4.6) and fishless kettle bog with permanent water (3.4 ha
open- water surface area; mean depth: 4.5 m; maximum depth:
8.3 m; Hoeniger, 1986) in the low latitude boreal wetland region
(Zoltai et al., 1988) of Ontario, Canada. The region is characterized
by a relatively high elevation (300– 600 m above sea level) that is
wetter and cooler than the surrounding landscape (150 m). The ac-
tive season for Spotted Salamanders in the region, defined as the
non- freezing period during which salamanders are post- breeding
and presumed feeding, spans approximately ordinal day 140– 288
(May 20 October 15). This northernly location within the Spotted
Salamander geographic range, local elevation, and prevailing climatic
means that the Bat Lake salamander population effectively lives
near a climatic range edge.
2.2  |  Data collection
The breeding biology of Spotted Salamander was studied non-
continuously from 1986 to 2019 at Bat Lake. Prior to 2008, breed-
ing phenology data (first egg- lay date) were sporadically collected
by various observers (1986, R .G. Tozer and D. Strickland in Oldham
& Weller, 1989; 1992– 1993, D.C. Cunnington, unpublished; 2004–
2007 author G.J. Tattersall). Between 2008 and 2019, the capture–
mark– recapture study and reproductive monitoring were conducted
annually. Each year (N = 12; 2008– 2019) we conducted salamander
trapping using non- baited aquatic funnel traps and egg mass counts,
commencing at lake ice- of f and continuing daily throughout the
duration of the 3- to 4- week spring breeding period. Each year we
distributed traps equidistantly (spaced 8– 10 m apart) around the pe-
rimeter of the lake at fixed locations. Captured salamanders were
measured for snout– vent length (SVL) and body mass. Female repro-
ductive status (gravid or spent) was assessed by visually inspecting
the venter for abdominal distension and visible ova. Individuals were
marked with a single toe clip, digitally photographed, cataloged in
a photo identification database, and recaptures were identified by
their unique spot pattern using Interactive Individual Identification
System Classic software (v. 4.0.2., den Hartog & Reijns, 2020; van
Tienhoven et al., 2007). Trapping ended following three consecutive
days of no salamander captures, coinciding with the mass emigration
of adults out of the lake at the end of the breeding season, or until
water temperature at submerged trap depth reached 10°C (as to not
risk severe hypoxia in submerged salamanders).
We conducted whole lake egg mass counts, a measure of
population- level reproductive output, throughout the annual sam-
pling period by paddling the vegetated perimeter of the lake and
counting egg masses with the aid of polarized sunglasses. Egg mass
counts ceased when egg mass abundance plateaued and/or sal-
amander captures declined sharply in traps, signifying the end of
breeding.
2.3  |  Hypothesis testing and statistics
We were interested in whether climatic conditions prior to breeding
influence female and male breeding body condition, population- level
reproductive output (egg mass abundance), and spring breeding phe-
nology. We therefore identified plausible environmental predictor
variables related to the breeding biology and life history of temper-
ate amphibians (Table S1), including environmental conditions from the
preceding summer, autumn, winter, and the contemporary spring pe-
riod. These predictors included mean temperature (°C) and total pre-
cipitation (mm) of the summer (July and August), autumn (September
and October), pre- winter (November), and spring periods (April and/
or May), as well as the number of days from lake surface freeze to
thaw (ice- on duration, a proxy for the length of winter and hence sala-
mander dormancy), and the ordinal date of majority lake ice- off (i.e.,
first breeding opportunity for pond- breeding salamanders; Table S1).
Climate data were retrieved from the Algonquin Provincial Park East
Gate climate station (45°32′N, 78°16′W; Environment and Climate
Change Canada: www.clima te.weath er.gc.ca) located approximately
30 km east of Bat Lake. Annual ice- off dates were known for Bat Lake,
although annual ice- on dates were not available. We used ice- on date
and ice- on duration from Lake of Two Rivers (2007 2019), a long- term
monitoring site within two kilometers of Bat Lake (R.G. Tozer, unpub-
lished data), as a proxy for Bat Lake. Annual ice- off dates for Bat Lake
and Lake of Two Rivers for the period of data overlap (2008– 2019)
were highly correlated (Pearson correlation: r = 0.93, p < 0.0001).
Statistical analyses were completed in R statistical software
(version 3.6.3, R Development Core Team, 2020). We used an
information- theoretic approach (Burnham & Anderson, 2002;
Burnham et al., 2011; Nakagawa & Schielzeth., 2013) and developed
an ecologically relevant set of candidate models for each response
variable, with each unique candidate set addressing one of the three
major response variables in our study (body condition, reproductive
output, and breeding phenology); below, we broadly describe these
hypotheses for each variable (Tables S2– S4). All models in each can-
didate set were fit with maximum likelihood then ranked according
to the second- order Akaike's information criterion (AICc; Burnham
& Anderson, 2002). The best- ranked models in each set (
wi
0.95;
Burnham & Anderson, 2002) were carried forward for model aver-
aging (using subset or “natural averaging,” as opposed to full- model
averaging; Burnham & Anderson, 2002; Symonds & Moussalli, 2011)
using the R package MuMIn (version 1.43.17; Bartoń, 2020).
We tested all response variables for temporal (i.e., year over
year) autocorrelation because salamanders may skip years and
1728 
|
    MOLDOWAN et AL.
accumulate energ y for reproduc tion over multiple seasons (e.g.,
Bulahova & Berman, 2017; Peacock & Nussbaum, 1973; Yartsev
& Kuranova, 2015). We examined the predictor variables of each
model for multicollinearity by calculating variance inflation factors
(VIF) using the R package car (version 3.0.10, Fox & Weisberg, 2019).
All predictors were retained in the models unless stated otherwise.
2.4  |  Body condition
Salamander body condition at the time of breeding (late April through
mid- May) reflects their state following overwintering, which at the
latitude and elevation of our study site means that salamanders have
presumably not fed for the preceding 5– 6 months, from the onset
of freezing temperatures (November) of the preceding year. Female
and male breeding body condition for the period of 2008– 2019
was calculated as the scaled mass index (SMI; Peig & Green, 2009).
The SMI standardizes the mass of an individual to the mean body
size of all individuals in the population (female and male datasets
were treated independently) while accounting for the SVL– mass al-
lometric relationship (Peig & Green, 2009). The SMI accurately re-
flects the energy stores (fat) of adult newt s and other amphibians
(MacCracken & Stebbings, 2012) and output values are interpretable
in the same unit of measure as input dat a (Peig & Green, 2009). To
calculate SMI, we plotted ln- transformed mass and ln- transformed
SVL, then fitted a line of best fit using standardized major axis re-
gression (Peig & Green, 2009). The slope of this best fit line was
carried forward as the scaling exponent for the SMI calculation. We
used mean SVL (L0, as per Peig & Green, 2009) for females and males
in calculating SMI for each sex.
We reasoned that the summer and/or autumn temperature in the
preceding year may affect fossorial salamander biology by altering
ground temperatures, and thus af fecting metabolic rate and/or the
extent of thermal stress of salamanders while underground. In the
absence of a compensator y response in resource acquisition by sal-
amanders, this would result in a negative relationship between tem-
perature and body condition, and no expected relationship between
precipitation and body condition. We further reasoned that summer
and/or autumn temperature from the preceding year may also affect
forest productivity, thereby altering food availability when salaman-
ders forage aboveground. If productivity and resource acquisition
outweighed a metabolic or stress response, then this would manifest
as a positive relationship between body condition and temperature;
furthermore, under the productivity hypothesis, we also expect a
positive relationship between body condition and precipitation.
Next, we reasoned that the pre- winter environment (November
temperature and precipitation from the preceding year) would be
related to annual variation in the length of the foraging period. We
predicted that November temperature of the previous year would
be positively related to body condition, and that November precip-
itation would be negatively related to condition, as precipitation in
November is overwhelmingly snow (climate data did not differen-
tiate between snow and rain). We predicted that ice- on duration
(i.e., winter duration) would be negatively related to body condition,
reasoning that longer winter periods represent a longer non- feeding
dormancy period and possibly a shorter pre- November foraging pe-
riod. We reasoned that warm temperature and high rainfall during
late winter/early spring of the contemporaneous breeding year
would result in earlier thaw, an earlier onset of salamander breeding,
and shor tened overwinter fasting period. Therefore, we predicted a
positive relationship between body condition and contemporaneous
April temperature and precipitation.
Finally, we included ordinal date (i.e., day of year) of capture as
a covariate in all models, as salamanders do not feed during breed-
ing and are expending energy continuously. We expected that body
condition would decline with ordinal capture date. Reproductive
status was included as a grouping variable (yes, gravid; no, spent)
in all models of female body condition, as some females were cap-
tured before laying and others post- laying. No interactions among
variables were included in any model.
Ultimately, these hypotheses and their combinations resulted in
a set of 17 ecologically plausible models to explain each female and
male body condition from 2009 to 2019 (Tables S1 and S2; body
condition data from 2008 were retained for time series analyses but
excluded from linear mixed- effect models because relevant precip-
itation data were not available); female and male data were fit sep-
arately. Linear mixed- effects models were fit using the R Package
lme4 (version 1.1.23; Bates et al., 2015). Both body condition model
sets included individual ID, unique day (unique date of capture; a
unique day assignment across all years in the dataset that addresses
error unique to a sampling day), and year as random effects to ac-
count for the non- independence of these factors on measures of
condition (Table S2). Data standardizations were used to improve
the biological interpretability of regression coefficients and relative
importance of predictors: The response variable (SMI) was scaled
(centered then divided by the standard deviation), and all predictor
(fixed effect) variables were centered prior to modeling (Schielzeth,
2010).
2.5  |  Body condition: Long- term temporal and
environmental relationships
We investigated whether a temporal change in body condition oc-
curred over the study period (2008– 2019). We used a separate
model for each sex with random effects of year, individual ID, unique
day, and fixed effects of ordinal date, year, and for females, repro-
ductive status; below we refer to this model as the “Base Model”
for each sex, as the model contains the fixed effect of year but no
environmental covariates (Table 1). We inferred a temporal change
in body condition if confidence intervals on the fixed ef fect of year
(βYear ) did not overlap zero.
Next, we explored which environmental covariates, if any, were
responsible for driving temporal changes in body condition. Drawing
from our model selection procedure with the body condition model
set, we sequentially substituted each environmental covariate
   
|
  1729
MOLDOWAN et AL.
identified as important (i.e., where model- averaged confidence in-
tervals did not overlap zero; Figure 1) into the base model, separately
for each sex ( Table 1). For each substitution, we qualitatively exam-
ined how the parameter estimate for the fixed effect of year (βYea r)
changed relative to that of the base model. Large changes in βYear r el-
ative to the base model suggested that an environmental covariate
played a role in driving changes in body condition over time. Because
we were interested only in parameter estimates, all models were fit
with restricted maximum likelihood.
2.6  |  Body condition: Forecasting body condition
under climate change
Our analyses suggested that increased temperature, particularly
summer temperature, was associated with a temporal decline in
salamander body condition, and that this association may be damp-
ened by increases in summer precipitation (see Section 3; Table 1).
Drawing from this result, we used model- averaged parameter esti-
mates to forecast male body condition under three realistic near-
future (2050– 2100) climate scenarios for Algonquin Provincial Park
(Lemieux et al., 2007; Ridgway et al., 2018): up to 24% increase in
mean summer precipitation and up to 3°C increase in each mean
summer temperature, mean autumn temperature, and concurrent
mean summer and autumn temperature. For simplicity, only male
condition was used for forecasting as females had a much lower
sample size coupled with multiple reproductive states.
2.7  |  Egg mass counts
We assumed that the maximum observed egg mass count at the
peak of breeding (2009– 2019) was a suitable estimate of population-
level reproductive output, as egg mass count should be related to
both the number of breeding females and the number of clutches
produced per female. Population- level reproductive output may
be linked to climatic conditions that favor resource acquisition and
body condition, and therefore, the same hypotheses that describe
variation in body condition apply to egg mass counts. We included
one additional fixed effect in our model set, ice- off date, reasoning
that the timing of thaw may be related to how many salamanders ar-
rive to breed (Table S1). Statistic al modeling of egg mass counts was
relatively simple, given that egg mass count was taken as one value
(maximum) per year. Thus, we developed a set of 18 candidate mod-
els (Table S3). We compared models using AICc, as above. We also
used linear regression to test whether maximum egg mass counts
changed during 2008– 2019.
2.8  |  Spring breeding phenology
Our field observations suggested that annual variation in spring
weather patterns is associated with variation in salamander breeding
date. Median breeding date, retrospectively calculated as the ordinal
date at which half of the maximum egg masses were deposited at Bat
Lake, was used as the response variable in the candidate model set.
TAB LE 1 Description of models and results exploring the sensitivity of the parameter βYea r, the slope of Spot ted Salamander ( Ambystoma
maculatum) body condition over year, to environmental covariates. The base model for each sex does not feature an environmental
covariate, whereas subsequent environmental models consider a single environmental covariate; after the addition of the covariate, the
qualitative change in the magnitude and direction of βYea r relative to the base model is described. In all models, random effects are individual
ID, unique day, and year (defined Table S1)
Model description Fixed effects Period βYea r ± SE
% change in βYe ar
relative to base model
Females
Base model F0Reprod status, ordinal date, year 2008– 19 −0.114 ± 0.0470
Env model F1Reprod st atus, ordinal date, year, summer temp 2008– 19 −0.0625 ± 0.0445 −45%
Env model F2Reprod st atus, ordinal date, year, autumn temp 2008– 19 −0.102 ± 0.0552 −11%
Env model F3Reprod st atus, ordinal date, year, ice in
duration
2008– 19 −0.117 ± 0.0519 +3 %
Env model F4Reprod status, ordinal date, year, summer
precip
2009– 19 −0.135 ± 0.0456a+30% a
Males
Base model M0Ordinal date, year 2008– 19 −0.146 ± 0.0482
Env model M1Ordinal date, year, summer temp 2008– 19 −0.106 ± 0.0509 −27 %
Env model M2Ordinal date, year, autumn temp 2008– 19 −0.128 ± 0.0556 −12%
Env model M3Ordinal date, year, ice in dur ation 2008– 19 −0.141 ± 0.0530 −3%
Env model M4Ordinal date, year, april temp 2008– 19 −0.125 ± 0.0654 −14%
Env model M5Ordinal date, year, summer precip 2009– 19 −0.186 ± 0.0473a+22% a
aPrecipitation data were not available in 2007 for pairing with 2008 salamander body condition data. Therefore, Env model F4 and Env model M4
are based on the interval 20 09– 2019. The percent change in βYe ar ± SE estimates is also based on the interval 2009– 2019, where the base model
βYear ± SE estimate for females is −0.103 ± 0.0560 and for males is −0.152 ± 0.0594.
1730 
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    MOLDOWAN et AL.
Median breeding date was selected because it is more robust to out-
liers compared to start date (Carter et al., 2018) and captures the pe-
riod of environmental conditions responsible for the onset of major
breeding activit y. We reasoned that mean temperature and summed
precipitation in March, April, and May, as well as Ice- off Date, could
affect breeding phenology (2008– 2019). We expected tempera-
tures to be negatively associated with breeding date, as high tem-
perature accelerates snow and ice melt. We expected ice- off date
to be positively correlated with breeding date, as breeding cannot
begin until ice is off the breeding pond. Lastly, we expected precipi-
tation in March and April (usually comprising snow) to be positively
associated with breeding date, and precipitation in May (cool rain) to
stimulate activit y and lead to earlier breeding date. Ultimately, these
hypotheses and their combinations resulted in a set of six candidate
models (Table S4).
Linear regression was used to test for temporal trends in repro-
ductive phenology using two dataset s: annual first egg- lay dates
(non- continuous study, 1986– 2019, N = 19 years) and annual first
egg- lay, median egg- lay, and peak egg- lay dates (focal study period,
2008– 2019, N = 12 years). Finally, because ice- off date was a very
strong predictor of salamander breeding (see Section 3), we examined
trends in ice- off phenology at Bat Lake (20 08– 2019, N = 12 years)
and nearby Lake of Two Rivers (1973– 2019, N = 44 years available;
R.G. Tozer, unpublished data).
2.9  |  Salamander metabolic rate estimation
During the period of August 2017 to September 2020, dataloggers
(HOBO TidbiT® v2) recorded temperature every 2 h at three soil
depths (shallow/surface, 0 m; mid- depth, 0.5 m; deep, 1.0 m) in the
forest surrounding Bat Lake. We used soil thermal profiles from Bat
Lake and the Spotted Salamander temperature- metabolic rate re-
lationship repor ted by Whitford and Hutchison (1967) to estimate
metabolic rate for Bat L ake Spotted Salamanders. See the Supporting
Information file for full metabolic rate estimation methods.
3 | RESULTS
Over the period of 2008– 2019, we recorded 1004 capture events
of 956 individual female and 3247 capture events of 2176 individual
male Spotted Salamanders. Male- biased capture rates likely resulted
from sampling methodolog y (aquatic funnel traps disproportionately
FIGURE 1 Parameter estimates from the best- ranked model set (
w
i
≥ 0.95) for (a) female* (black) and male (gray) Spotted Salamander
body condition (scaled mass index, SMI; Peig & Green, 2009); (b) egg mass abundance (population- level reproductive output). Adjusted
standard error (Burnham & Anderson, 2002: section 4.3.3; Bartoń, 2020: 33, 42) was used to construct 95% confidence inter vals of
the parameter estimates. In (a) temperature estimates were multiplied by 0.1 before plotting. Also, April precipitation and mean April
temperature were present in the best- ranked models of the male dataset, but absent from the corresponding female models (Table S5).
*Gravid parameter estimate (0.49 ± 0.11, 95% CI) not plotted among female body condition parameter estimates because of figure scaling
[Colour figure can be viewed at wileyonlinelibrar y.com]
   
|
  1731
MOLDOWAN et AL.
intercept mate searching males), differential breeding turn- out of
the sexes, and/or a male sex bias in the population. Body condition
sample sizes are therefore much larger for males than for females.
3.1  |  Body condition
The best supported model predicting female body condition in-
cluded summer temperature, summer precipitation, ice- on (winter)
duration, and reproductive status (Model FBC13: w = 0.60; Table S5).
Although there was model selection uncertainty, Model FBC13 was
still five to eight times more likely to be the best model compared
to the next- best models in the candidate set (Table S5). As with
females, male body condition was best predicted by a model that
included summer temperature, summer precipitation, and ice- on du-
ration (MBC13: w = 0.39, Table S5). A model that included summer
temperature, autumn temperature, and November temperature was
also competitive in explaining male body condition (MBC8: w = 0.19).
Among model averaged parameter estimates, summer tempera-
ture, autumn temperature, ice- on duration, ordinal date, and repro-
ductive status (for females) were important predictors of female and
male body condition (Figure 1a). Higher mean summer and autumn
temperatures, a longer winter duration, and later spring capture date
negatively affected both female and male body condition (Figure 1a).
We found no significant temporal (i.e., year over year) autocorrela-
tion in mean female body condition when tested with all three data-
sets (gravid, spent, and pooled datasets; Figure S1a– c), but mean
male body condition demonstrated marginally significant temporal
autocorrelation at a 1- year time lag (Figure S1d).
3.2  |  Body condition: Long- term temporal and
environmental relationships
We found that female body condition declined during 2008– 2019
(βYear ± SE = −0.114 ± 0.0470; Figure 2). Substituting summer tem-
perature into the base model resulted in a 45% reduction in the mag-
nitude of the parameter estimate for year (βYea r = −0.0625 ± 0.0445),
whereas little change in βYear was observed when substituting au-
tumn temperature, or ice- in duration (Table 1). Using data from
2009 to 2019 (as no 2007 precipitation data were available to pair
with 2008 condition data), body condition declined across time for
females, albeit marginally (βYear = −0.104 ± 0.0560) and substitut-
ing summer precipitation into the base model slightly increased the
magnitude of βYear ( βYear = −0.135 ± 0.0456, a 30% increase; Table 1).
Results were broadly similar for males. Body condition declined
during 2008– 2019 in males (βYe ar = −0.146 ± 0.0482; Figure 2), and
substitution of summer temperature into the base model resulted in
a 27% reduction in the magnitude of βYe ar (βYea r = −0.106 ± 0.0509).
We observed modest changes in βYear when substituting autumn
temperature, ice- in duration, and April temperature into the base
model ( Table 1). Using data from 2009 to 2019 (again, no 2007 pre-
cipitation data were available to pair with 2008 condition data), body
condition declined across time for males (βYear = −0.152 ± 0.0594)
and substituting summer precipitation increased the magnitude of
βYear in the model (βYear = −0.186 ± 0.0473, a 22% increase; Table 1).
In sum, holding summer temperature constant tended to dampen
the temporal decline in condition in females and males, suggesting
summer temperature played a role in driving the temporal decline in
condition; holding summer precipitation constant tended to exacer-
bate the decline in condition in males and females, suggesting that
annual variation in summer precipitation moderates the temporal
decline in condition.
3.3  |  Body condition: Forecasting body condition
under climate change
Assuming a linear relationship between temperature and body
condition loss (and no compensator y response by salamanders),
warming of Mean Summer Temperature by 1– C is predicted to
reduce male breeding body condition by 5%– 14% (−0.25 to −0.75
SD of body mass; Figure 3a) for an average breeding condition male
(
xSMI
± SD = 9.7 ± 1.8 g, all breeding males 2008– 2019). Warming of
mean autumn temperature by 1– 3°C is predicted to cause a body
condition decline of 5%– 9% for an average condition male (−0.25 to
−0.50 SD of body mass; Figure 3b). Simultaneous increases in both
mean summer and autumn temperature of 1– 3°C are expected to be
additive and expedite body condition loss, with declines of 10%– 27%
FIGURE 2 Body condition, measured as scaled mass index (SMI,
Peig & Green, 2009), for breeding adult female (black) and male
(gray) Spotted Salamanders (Ambystoma maculatum), Bat Lake,
Algonquin Provincial Park, Canada (2008– 2019). Time series body
condition data for females and males with best fit lines and 95%
confidence intervals from base models F0 and M0, respectively
(Table 1) [Colour figure can be viewed at wileyonlinelibrary.com]
1732 
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    MOLDOWAN et AL.
(−0.50 to −1.50 SD of body mass; Figure 3c). Realistic concurrent in-
creases in precipitation are predicted to offer very little to no buffer-
ing of temperature- driven body condition decline (Figure 3).
3.4  |  Reproductive output
Maximum eg g mass abundance (2008– 2019) showed substan-
tial interannual variation across breeding seasons, varying by
approximately 400% (Figure 4). A model containing autumn tem-
perature best explained annual egg mass abundance; however, over-
all support and fit was weak for this model (Model RO5: w = 0.38,
R2
adj
= 0.25) and there was considerable overall model selection un-
certainty (Table S6). Model- averaged parameter estimates suggested
autumn temperature was positively associated with maximum egg
mass abundance, although uncertainty was high (Figure 1b; also see
Figure S2). We detected no temporal autocorrelation in annual egg
mass abundance (Figure S1e).
FIGURE 3 Forecast of male Spotted Salamander (Ambystoma maculatum) body condition under realistic climate scenarios (2050– 2100)
for western Algonquin Provincial Park: (a) increasing summer precipitation (up to 36 mm, or 24% increase in mean summer precipitation) and
increasing mean summer temperatures (increase up to 3°C); (b) increasing summer precipitation and increasing mean autumn temperatures;
and (c) increasing summer precipitation and increasing mean summer and autumn temperatures (synchronous increases up to 3°C in both
seasons). Using 2008– 2019 climate data as a baseline, the SD in mean annual summer and autumn temperature is 1.1°C and the SD in
mean summer precipitation is 50 mm. Therefore, realistic near- future warming of 2– C would be approximately ≥2 SD above current
seasonal temperatures, whereas realistic near- future summer precipitation increases (20%– 24%, equivalent to 30– 36 mm) are <1 SD of
current values. Near- future climate scenarios are based on Lemieux et al. (20 07) and Ridgway et al. (2018) [Colour figure can be viewed at
wileyonlinelibrary.com]
FIGURE 4 Time series of Spotted Salamander (Ambystoma maculatum) egg mass abundance at Bat Lake, Algonquin Provincial Park
(2008– 2019). (a) Daily egg mass counts starting at first egg lay date and extending until maximum (peak) values. During 20 08– 2019, the
earliest breeding star t date was ordinal date 98 (April 7, 2010), latest breeding start date was day 129 (May 9, 2019), and the mean first
breeding date was day 116 (April 26). Egg mass count values that extended post- peak were excluded to improve visual clarity of the plot.
(b) Maximum egg mass count per annum [Colour figure can be viewed at wileyonlinelibrary.com]
(a) (b)
   
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MOLDOWAN et AL.
3.5  |  Spring breeding phenology
During 2008– 2019, the mean first breeding date of Spotted
Salamanders at Bat Lake was ordinal date 116 (April 26). Across this
period, first breeding date varied by 31 days (earliest breeding date:
day 98, April 7, 2010; latest: day 129, May 9, 2018). Salamander first
breeding date (
r2
adj
= 0.29, p = 0.04), median breeding date (
= 0.39,
p = 0.02), and peak breeding date (
r2
adj
= 0.51, p = 0.006) became sig-
nificantly later during 2008– 2019 (Figure 5a); however, the longer
time series (1986– 2019) showed no trend in first breeding date
(
= 0, p = 0.54; Figure 5b).
Model selection showed strong suppor t for Model BP6 in which
ice- off date predicted median breeding date (w = 0.93,
= 0.67;
Table S6). Model averaging was not conducted because Model BP6
was strongly supported. High levels of collinearity (VIF values up
to 6.2) were identified among predictors in models of the breeding
phenology model set (Table S4). The variable(s) with high VIF val-
ues (VIF > 3.0) in a model were removed and model selection was
rerun. The overall outcome of model selection was unaffected, as
strong suppor t remained for Model BP6 as the best- fitting model in
the model set.
In subsequent analysis of ice- off dates, we detec ted a marginally
significant delay in Ice- of f date for Bat Lake (
= 0.27, p = 0.047) at
a rate of 1.3 days per year over the 2008– 2019 monitoring period
(β ± SE = 1.3 ± 0.58 SE). There was no change in ice- off date for the
nearby long- term reference site, Lake of Two Rivers, during 1972
2019 (
r2
adj
= 0, p = 0.90, β ± SE = 0.012 ± 0.099).
3.6  |  Salamander metabolic rate estimation
Ground surface temperature around Bat Lake ranged mostly between
20 and 25°C, occasionally reaching 30°C , in the months of July and
August (Figure 6a). Temperatures were 10– 15°C at depths of 0.5–
1.0 m during summer (Figure 6a). Using soil temperature recorded at
multiple depths and the Spotted Salamander temperature– metabolic
rate relationship reported by Whitford and Hutchison (1967), sala-
manders at shallow depths (14.8°C surface mean temperature) have
an estimated metabolic rate 1.3 times that of individuals at mid-
depths (10.8°C mean temperature at 0.5 m depth) and 1.6 times
that of individuals deep underground (9.1°C mean temperature at
1.0 m depth; Figure 6c) during the active period (May 20– October
15). Metabolic rate estimation highlighted the thermal sensitivity of
these fossorial salamanders. For instance, given the Q10 value re-
ported for the temperature range of 10– 15°C (Q10 = 4.37; Whitford
& Hutchison, 1967), a change of 1, 2, or 3°C results in a 16%, 34%, or
56% change in salamander metabolic rate, respectively.
4 | DISCUSSION
In this study, we explored the association between annual climatic
variation, body condition, population- level reproductive output, and
breeding phenology in a fossorial salamander over a 12- year period.
First, we found that interannual variation in climate is associated
with body condition and breeding phenology of salamanders, but
climatic variation was not strongly associated with our measure of
reproductive output. Second, body condition of females and males
declined during the study period, and a slight increase in summer
temperature during the study period is likely par tly responsible for
the decline. Third, associations between temperature and body con-
dition were predicted to be non- trivial under realistic near- future
climate change, with up to a 27% decline in body condition for a 3°C
seasonal temperature increase and little evidence that precipitation
increases will moderate these temperature effects.
Global amphibian diversity is highly structured across vertical
strata (fossorial, terrestrial, arboreal), with a large propor tion of
temperate and arid species occupying subterranean environment s
(Oliveira et al., 2017; Oliveira & Schef fers, 2019). Microhabitat re-
fugia in combination with behavioral thermoregulation is expected
FIGURE 5 Breeding phenolog y of the Spotted Salamander (Ambystoma maculatum) at Bat Lake, Algonquin Provincial Park. (a) First egg-
laying date (
r2
adj
= 0.29, p = 0.04), median egg- laying date (
r2
adj
= 0.39, p = 0.02), and peak egg- laying date (
= 0.51, p = 0.006) have become
significantly later during the focal study period (2008– 2019). (b) Extended dataset of first breeding date (1986– 2019) shows no temporal
trend (best fit line;
= 0, p = 0.54). Ice- of f dates at Bat Lake (2008– 2019) and nearby reference site, Lake of Two Rivers (1986– 2019 shown)
are highly correlated (r = 0.93, p < 0.0001) during years of data overlap (2008– 2019). Note close synchrony (typically ≤24 h) between Bat
Lake ice- off and first salamander egg- laying
(a) (b)
1734 
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    MOLDOWAN et AL.
to be crucial for individual survival as well as population and spe-
cies persistence under climate change (Fitzpatrick et al., 2020; Huey
& Buckley, 2018; Lara- Reséndiz et al., 2021; Moore et al., 2018;
Scheffers et al., 2013; Scheffers, Edwards, et al., 2014). Amphibians
are susceptible to direct threat s (thermal and hydric stress), indirect
threats (habitat change, food availability, disease risk), and interac-
tions thereof associated with climate change (Blaustein et al., 2010;
Lertzman- Lepofsky et al., 2020; Reading, 2007; Rohr & Palmer,
2013), but fossorial species may be buffered from strong climate
effects, at least in the short term. This is important because sala-
manders, and amphibians more broadly, contribute to numerous
ecological functions (Best & Welsh, 2014; Davic & Welsh, 2004),
particularly in the forest s of eastern Nor th America. Never theless,
given the global distribution, diversity, and ecological roles of fosso-
rial amphibians, heightened attention to the vulnerability of micro-
habitat refugia is warranted amid global climatic change.
Our study shows that fossorial salamanders are sensitive to tem-
perature increases, with temperature from the preceding summer
and autumn negatively affecting breeding body condition. The di-
rection of these relationships is consistent with the interpretation
that reduced body condition may be driven by elevated metabo-
lism and/or thermal stress in the summer. Direct monitoring in the
forest understory around Bat Lake demonstrated that ground sur-
face temperature ranged consistently between 20 and 25°C in July
and August (Figure 6a). Notably, surface temperatures sometimes
reached 30°C, which would greatly elevate metabolism (Whitford
& Hutchinson, 1963, 1967) and likely induce stress, as these tem-
peratures approach the thermal critical maximum of the Spotted
Salamander (Gatz, 1971, 1973; Hutchinson, 1961; Pough & Wilson,
1970). Spotted Salamanders often spend the summer and autumn
periods at shallow depth (2.5– 3 cm below the surface of the leaf
litter; Faccio, 2003) in horizontal burrows and runways of small
mammals, transitioning to use of deeper vertical burrows for over-
wintering (Madison, 1997; Montieth & Paton, 2006; salamanders
at depths of 30– 122 cm are known during summer, Gordon, 1968;
Kleeberger & Werner, 1983). Although temperatures are buffered
in the subterranean environment, thermal profiles at depths of 0.5–
1.0 m at Bat Lake indicated that temperatures still reached 10– 15°C
during summer (Figure 6a). The temperature sensitivity of metabolic
expenditure of Spotted Salamanders at 10– 15°C is high (Q10 = 4.37
at 10– 15°C, based on metabolic rate measured across a temperature
range of 5– 30°C; Whitford & Hutchison, 1967), which could explain
the association between reduced body condition and high active
seasonal temperatures. Using soil temperature data, we estimated
that salamanders at warmer shallow depths have a metabolic rate
1.3– 1.6 times that of individuals at cooler deeper depths (0.5– 1.0 m
depth; Figure 6c). Furthermore, temperature increases of 1– C are
estimated to result in sizable increases in salamander metabolic rate
(16%– 56% change in met abolic rate), suggesting substantive ener-
getic consequences within these commonly encountered spring and
summer temperatures. Spotted Salamander microhabitat selection
during the active season, including use of areas with deeper leaf
litter, high plant and natural object cover, and high small mammal
burrow densities, is consistent with preferences for cool damp con-
ditions that would reduce metabolic rate (Faccio, 2003; Montieth &
Paton, 2006). Soil temperature profiles (Figure 6a) and metabolic rate
FIGURE 6 Thermal environment and estimated metabolic rate
of the Spotted Salamander (Ambystoma maculatum). (a) Averaged
thermal profile at shallow (surface, 0 m), mid- depth (0.5 m), and deep
(1.0 m) soil depths from t wo temperature monitoring s tations at Bat
Lake, Algonquin Provincial Park. (b) Estimated Spotted Salamander
metabolic rate based on soil thermal profiles. Estimates based on
the empirical temperature– metabolic rate relationship reported
by Whitford and Hutchison (1967; see Supporting Information). (c)
Mean estimated metabolic rate of Spotted Salamanders at varying
soil depth across the active and inactive season. For our study
population, the active season spanned from ordinal day 140– 288
(May 20– October 15) and was defined by the non- freezing period
during which salamanders were post- breeding and presumed
feeding (In (a) note that that the underground thermal gradient
flips direction in mid- May and mid- October). The numerical values
presented above each bar are mean soil temperatures at the
respective depth and activit y period. See Supporting Information
for additional information about metabolic rate estimation [Colour
figure can be viewed at wileyonlinelibrary.com]
–15
–10
–5
0
5
10
15
20
25
30
2018 2019 2020
Date
Depth
Shallo w
Mid
Deep
0
25
50
75
100
125
150
2018 2019 2020
Date
Metabolic rate ( l O
2
/g/h)
Depth
Shallow
Mid
Deep
Active Inactive
Shallow MidDeep ShallowMid Deep
0
25
50
75
100
Depth
Metabolic rate ( l O
2
/g/h)
(a)
(b)
(c)
   
|
  1735
MOLDOWAN et AL.
estimates (Figure 6b) suggest that remaining at mid- depths during
the inactive (winter) period offers slight advantage for minimizing
metabolism while also avoiding freezing temperatures (Figure 6b,c).
During the 12- year study period, the breeding body condition of
spent females and males significantly declined (Figure 2). During this
period, our study area experienced a slight increase in mean summer
temperature ( β ± SE = 0.14 ± 0.081°C, p = 0.11, n = 12 years; Table
S8). In our models, holding summer temperature constant dampened
the temporal decline in body condition in both sexes (Table 1) and it
therefore seems likely that increases in summer temperature are at
least partly responsible for the temporal decline in body condition.
Longer term temperature trends for Algonquin Park show significant
temperature increases (1975– 2006, Waite & Strickland, 2006; 1915–
2016, Favot et al., 2019). The parameter estimates for temperature–
condition relationships in our models (Figure 1a), and projec ted
temperature increases for Algonquin Park over the next half- century
(Lemieux et al., 2007; Ridgway et al., 2018), suggest that this trend
in declining body condition is expected to continue (Figure 3). We
did not model female body condition under near- future climate sce-
narios given their multiple reproductive states and a smaller sample
size. However, given the synchronous decline of body condition in
both sexes over the past 12 years (Figure 2) and similar seasonal
temperature sensitivities of body condition in both sexes (Figure 1a),
it is reasonable to expect that female body condition will continue
to decline in a warming climate, as forecasted for males (Figure 3). If
female body condition declines continue, individual- and population-
level consequences may begin to manifest, such as reduced egg size,
clutch size, reproductive frequency, and survival.
The negative relationship between body condition and ice- on
(winter) duration can be reasonably attributed to extended fasting in
years of late ice- off. Similarly, later spring capture dates resulted in
reduced body condition of females and males, a result corroborated
in similar salamander field studies (Homan et al., 2018; Strickland
et al., 2015), and likely related to their non- feeding status and en-
ergy expenditure throughout winter (Figure 6b) and during early
spring migration and breeding. Although we did not forecast how
changes in ice- on duration may affect body condition (largely due to
the lack of any projection available), it seems likely that warmer fall
temperatures will be associated with decreases in winter duration in
future climates, and hence relatively warm temperatures in the over-
wintering environment (Figure 6a), which may partly offset the en-
ergetic benefit of a shortened winter duration. Furthermore, based
on parameter estimates (Figure 1a), a change in ice- on duration of
approximately 20 days is associated with the same change in body
condition as a 1°C change in summer temperature, suggesting that
temperature effects during the active season would overwhelm any
benefit associated with shor ter winter (fasting) duration.
Our forecast of salamander body condition assumed that sala-
manders do not demonstrate a compensator y response to warmer
temperatures, although behavioral thermoregulation in response to
elevated temperatures is a reasonable expectation (Huey & Buckley,
2018; Kearney et al., 2009). Spot ted Salamanders often reside in
shallow horizontal burrows during the active season (Faccio, 2003;
Madison, 1997) but could become more reliant on vertical small
mammal burrows that offer cooler refuge. Although a shift from
horizontal to vertical habitat use during the active season may re-
lieve salamanders from high temperatures and elevated metabolism,
sheltering deeper underground may fur ther complicate energy ac-
quisition and/or retention by stymieing near- surface foraging oppor-
tunities (Gordon, 1968).
Mean autumn temperature was positively correlated with egg
mass abundance (Figure 1; Figure S2). A positive association be-
tween autumn temperature and egg mass count s suggests energetic
gain at the individual level during autumn, but this is contradictory to
our analyses incorporating individual- level information, which sug-
gest that autumn temperature was negatively correlated with female
body condition. We suspect, for several reasons, that the positive as-
sociation between autumn temperature and egg mass counts is spu-
rious. First, the frequency of female reproduction in our population
is likely not annual (as with Homan et al., 2018; Husting, 1965) and
this may confound interpretation of temperature and population-
level reproductive output because individuals are amassing energy
over multiple years. Second, philopatry at the breeding site may be
low, but interpretation of egg mass abundance implies that Bat Lake
is the only breeding site used by salamanders within this population.
Although pond- breeding amphibians are reputed for their philopatry
to breeding sites (e.g., Gamble et al., 2007; Gill, 1978; Semlitsch,
2008; Vasconcelos & Calhoun, 2004), it is also evident that breeding
individuals use alternative sites (e.g., colonization of created ponds;
Denoël et al., 2017; Patrick et al., 2008; Petranka et al., 2003). Also,
temperature may influence reproduction at a finer scale, such as egg
size and clutch size (e.g., Fraser, 1980) or clutch partitioning (female
Spotted Salamanders are reported to lay two to four egg masses per
reproductive bout; Petranka, 2010), rather than at population- level
through breeding turnout. In sum, it seems unlikely that autumn
temperature is positively associated with egg mass counts, and that
more detailed, individual- level data on reproduction may be needed
to estimate associations between climate and reproductive output .
We did not find evidence to suggest that salamander breed-
ing phenology was advancing concurrent with climatic warming.
Although Algonquin Park and surrounding regions have experi-
enced a warming trend of approximately 1°C in the past half- centur y
(Lemieux et al., 2007; Ridgway et al., 2018), much of the warming
has been concentrated in the summer and autumn (Favot et al.,
2019; Waite & Strickland, 2006). Given that salamander breeding
phenology is closely associated with spring conditions, primarily
ice- off, and that there has been little to no significant advancement
of spring thaw conditions in Algonquin Park, salamander breeding
phenology remains unchanged over the past several decades in the
higher elevation uplands of western Algonquin Park. Over our pe-
riod of continuous monitoring (2008– 2019), Spotted Salamanders
demonstrated phenological delay in reproductive timing. Ariet ta
et al. (2020) also reported delayed breeding (2000– 2020) in another
early- spring breeding amphibian, the Wood Frog, in the northeast-
ern United States. These authors cite seasonally heterogeneous
warming temperatures, later snow accumulation, and longer spring
1736 
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snow and ice persistence for delayed breeding, analogous to that
observed in Algonquin Park (Favot et al. 2019). Signals of delayed
breeding in shor ter term datasets of amphibians from northeast-
ern North America (Arietta et al., 2020; this study) are in contrast
to longer datasets, which tend to show mixed responses of am-
phibian breeding phenology to climate change: no change (North
America: Blaustein et al., 2001; Green, 2017; Kirk et al., 2019; Klaus
& Lougheed, 2013; Todd et al., 2011) or advancement (eastern north
America: Gibbs & Breisch, 2001; Todd et al., 2011; Walpole et al.,
2012; Klaus & Lougheed, 2013; northern Europe: Terhivuo, 1988;
Beebee, 1995a, 1995b; Tryjanowski et al., 2006; Japan: Kusano &
Inoue, 2008). Amphibians clearly demonstrate a range of species, re-
gional, and temporal phenological responses to climate change (e.g.,
Muths et al., 2017; Okamiya et al., 2021).
Fossorial species are difficult to study and are underrepre-
sented in research at the interface of organismal biology and climate
change. Our findings show that fossorial species can be susceptible
to rapid warming. Subterranean microhabitats, such as burrows, are
buffered from surface conditions, but these environments are not
completely insulated from aboveground climate. Large numbers of
species live in subterranean microhabitats, especially where already
extreme ambient environmental conditions prevail. Many fossorial
species are ecosystem engineers, creating thermal refugia on the
landscape upon which whole ecological communities are depen-
dent (Doody et al., 2021; Pike & Mitchell, 2013), emphasizing the
importance of protecting burrowing biota. Landscape- scale changes
in species distributions, such as latitudinal and altitudinal shifts,
in response to climate change are increasingly recognized. In con-
trast, comparatively little is known about thermal habitat structure
and species responses to environmental change on the microhab-
itat scale (Scheffers et al., 2013; Scheffers, Edwards, et al., 2014;
Scheffers, Evans, et al., 2014), particularly for subterranean envi-
ronments (Lara- Reséndiz et al., 2021; Moore et al., 2018). Fossorial
ectotherms and amphibians in particular may be at elevated risk as
their thermal microhabitat warms. Our study draws attention to the
vulnerability of subterranean environments and their inhabitants
amid global climatic change.
ACKNOWLEDGMENTS
PDM sincerely thanks DL LeGros for a warm welcome into field bi-
ology and a dozen years of salamander sleuthing; LA Rye and JD
Litzgus for encouragement and suppor t that made several years of
this project possible. We thank RG Tozer for collecting and provid-
ing access to long- term ice data and JA Leivesley for assistance with
troubleshooting R code. We greatly appreciate the help of numerous
research students (and other volunteers) for field data collection, in-
cluding: DL LeGros, SP Boyle, O Butty, JWD Connoy, D Crawford,
EA Francis, G H- Y Gao, N Hrynko, JA Leivesley, DI Mullin, S Paiva, D
Ravenhearst, C Rouleau, M Terebiznik, H Vleck, L Warma, with spe-
cial thanks to SJ Kell and T Wynia for many years of data collection
and frozen fingers. We appreciate the help of R Eckenswiller, TM
Winegard, and the Algonquin Wildlife Research Station for accom-
modation and field support. We thank P Gelok, J Hoare, A Lake, B
Steinberg, L Trute, Algonquin Provincial Park, and Ontario Parks for
permits, funding, and logistical support of this research.
AUTHOR CONTRIBUTIO N
Patrick D. Moldowan, Glenn J. Tattersall, and Njal Rollinson conceived
of the study; Patrick D. Moldowan and Glenn J. Tattersall conducted
field data collection; Patrick D. Moldowan and Glenn J. Tattersall
curated the dat aset; Patrick D. Moldowan, Glenn J. Tattersall, and
Njal Rollinson analyzed the data; Patrick D. Moldowan, Glenn J.
Tattersall, and Njal Rollinson funded the study; Patrick D. Moldowan
and Njal Rollinson wrote the manuscript; Patrick D. Moldowan,
Glenn J. Tattersall, and Njal Rollinson edited and approved the final
version of the manuscript.
DATA AVAILABILITY STATEMENT
The data that suppor t the findings of this study will be openly
available in the Zenodo research data repository at http://doi.
org/10.5281/zenodo.4993600 (reference number 4993600) follow-
ing publication.
ORCID
Patrick D. Moldowan https://orcid.org/000 0-0003-2852-794X
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