Biological Conservation 170 (2014) 169–176

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Biological Conservation

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Breeding site heterogeneity reduces variability in frog recruitmentand population dynamics

0006-3207/$ - see front matter � 2013 Elsevier Ltd. All rights reserved.http://dx.doi.org/10.1016/j.biocon.2013.12.013

⇑ Corresponding author. Present address: 1116 W Curtiss St., Bozeman, MT59715, USA. Tel.: +1 406 396 0320.

E-mail addresses: amphibecs@gmail.com (R.M. McCaffery), lisa.eby@umontana.edu (L.A. Eby), bmaxell@mt.gov (B.A. Maxell), scorn@usgs.gov (P.S. Corn).

Rebecca M. McCaffery a,⇑, Lisa A. Eby a, Bryce A. Maxell b, Paul Stephen Corn c

a Wildlife Biology Program, College of Forestry and Conservation, University of Montana, Missoula, MT 59812, USAb Montana Natural Heritage Program, 1515 East 6th Ave., Helena, MT 59620, USAc U.S. Geological Survey, Northern Rocky Mountain Science Center, Aldo Leopold Wilderness Research Institute, 790 E. Beckwith Ave., Missoula, MT 59801, USA

a r t i c l e i n f o

Article history:Received 14 June 2013Received in revised form 7 December 2013Accepted 8 December 2013

Keywords:Amphibian conservationEnvironmental stochasticityHabitat heterogeneityMontana, USAPopulation growth rateRana luteiventrisWetland hydroperiod

a b s t r a c t

Environmental stochasticity can have profound effects on the dynamics and viability of wild populations,and habitat heterogeneity provides one mechanism by which populations may be buffered against thenegative effects of environmental fluctuations. Heterogeneity in breeding pond hydroperiod across thelandscape may allow amphibian populations to persist despite variable interannual precipitation. Weexamined recruitment dynamics over 10 yr in a high-elevation Columbia spotted frog (Rana luteiventris)population that breeds in ponds with a variety of hydroperiods. We combined these data with matrixpopulation models to quantify the consequences of heterogeneity in pond hydroperiod on net recruit-ment (i.e. number of metamorphs produced) and population growth rates. We compared our heteroge-neous system to hypothetical homogeneous environments with (1) only ephemeral ponds, (2) only semi-permanent ponds, and (3) only permanent ponds. We also examined the effects of breeding pond habitatloss on population growth rates. Most eggs were laid in permanent ponds each year, but survival to meta-morphosis was highest in the semi-permanent ponds. Recruitment success varied by both year and pondtype. Net recruitment and stochastic population growth rate were highest under a scenario with homo-geneous semi-permanent ponds, but variability in recruitment was lowest in the scenario with theobserved heterogeneity in hydroperiods. Loss of pond habitat decreased population growth rate, withgreater decreases associated with loss of permanent and semi-permanent habitat. The presence of adiversity of pond hydroperiods on the landscape will influence population dynamics, including reducingvariability in recruitment in an uncertain climatic future.

� 2013 Elsevier Ltd. All rights reserved.

1. Introduction

Fluctuations in the environment can affect the populationdynamics of species by increasing the variability of survival, fecun-dity, and other vital rates. Variability in vital rates increases inter-annual changes in population size, and can ultimately lead to de-creased long-term population growth rates and increased risk ofextinction. Indeed, changes in the variability of population growthrate may have a stronger influence on extinction risk than changesin mean population growth rate or population size (Fagan et al.,2001; Inchausti and Halley, 2001). However, environmental vari-ability can also have positive effects, by promoting species coexis-tence in homogeneous or heterogeneous environments (e.g.,Chesson, 2000a,b; Amarasekare, 2003). Recent climate changemodels predict increased variability in climate in addition to

changes in mean values (e.g., Easterling et al., 2000). This variabil-ity could magnify the contrast between wet and dry years and in-crease the frequency of extreme weather events such as drought.Increased stochasticity due to climate change could increase stresson species already sensitive to stochastic changes in environmentalconditions. The consequences of changing climatic variability onplant and animal populations, and our ability to conserve popula-tions in light of this variance, are largely unexamined (but seeBoyce et al., 2006; Morris et al., 2008; Souther and McGraw,2011). However, they are urgent questions in population ecologyand conservation biology.

Habitat heterogeneity may reduce the negative effects ofenvironmental stochasticity on populations and promote popula-tion persistence despite high inter-annual variation in weatherconditions. Effects have included decreased variability in popula-tion size of bush crickets, Metrioptera bicolor, in Sweden (Kindvall,1996), lower extinction risk of the Bay checkerspot, Euphydryaseditha bayensis, in California (McLoughlin et al., 2002), and morestable population dynamics in 35 butterfly species in Great Britain(Oliver et al., 2010). However, the relationship between habitat

Fig. 1. Distribution of lakes and wetlands in the upper basin at Little Rock Creek.This basin contains three non-breeding lakes and one permanent pond with limitedbreeding (lined), three permanent breeding ponds (black) two semi-permanentponds (gray), and four ephemeral breeding ponds (white). Lined water bodies werenot included in the analysis. Three of the ephemeral ponds were analyzed as onepond (E1).

170 R.M. McCaffery et al. / Biological Conservation 170 (2014) 169–176

heterogeneity and stability of population dynamics has rarely beenexamined in other taxa.

Variability in the breeding pond hydroperiod (the number ofdays ephemeral ponds have water) can have strong effects onrecruitment dynamics of amphibians (Daszak et al., 2005;Pechmann et al., 1991; Semlitsch et al., 1996). If ponds dry tooquickly, tadpoles do not have time to complete metamorphosisand recruitment fails. However, permanent ponds can be poorbreeding sites if temperatures are too cold for development orpredators reduce recruitment (e.g., Knapp and Matthews, 2000;Meyer et al., 1998). Several studies have alluded to the potentialbenefits of maintaining diverse pond types or hydroperiods onthe landscape to promote amphibian population persistence(Babbitt et al., 2003; Semlitsch, 2000; Semlitsch and Bodie, 1998;Snodgrass et al., 2000).

Recruitment dynamics in pond-breeding amphibians have beenmonitored in various ways for different species, and each adds toour understanding of factors affecting amphibian recruitment. Atlarger landscape scales, researchers have monitored the presenceor absence of breeding in large networks of ponds, often over longtime periods (Skelly et al., 1999; Trenham et al., 2003; Gould et al.,2012). These studies examine the dynamics of breeding pond use,but do not quantify differential recruitment success at differentponds across years. In other studies, researchers have monitoredegg mass counts in networks of ponds in one or more years(Baldwin et al., 2006; Meyer et al., 1998; Hossack et al., 2013). Thishas allowed us to determine breeding effort in relation to hydrope-riod (e.g., Baldwin et al., 2006), but not to quantify successful netrecruitment. Finally, intensive studies at individual ponds over anumber of years have quantified recruitment success under avariety of environmental conditions (e.g., Semlitsch et al., 1996),but do not examine how the presence of multiple ponds on thelandscape may affect population-level recruitment success overtime, unless the population only uses one breeding site. In a rarestudy to quantify the relative contribution of multiple pond typesto recruitment over time, Karraker and Gibbs (2009) found thatwood frog (Rana sylvatica) reproduction over 3 yr was similar inephemeral and permanent ponds, but that survival to metamor-phosis was higher in permanent ponds, resulting in much higherpredicted production of metamorphs in permanent ponds com-pared to ephemeral ponds. Our study combines the strengths ofthese approaches by quantifying recruitment success in diversebreeding ponds across the landscape over a relatively long timeperiod and by examining the ramifications of variation inrecruitment success to population growth rates.

As climate change alters global precipitation patterns, hydrope-riod dynamics in wetland systems are changing (Winter, 2000),which may have consequences for amphibian recruitment andpopulation dynamics. The presence of heterogeneous pond hyd-roperiods on the landscape could help buffer populations againststochasticity in precipitation by providing suitable breeding habi-tat over a wide range of environmental conditions. We examinedthe recruitment dynamics of Columbia spotted frogs (Rana lutei-ventris) in a heterogeneous high-elevation landscape over 10 yr.R. luteiventris are thought to have high breeding site fidelity, butrecruitment success appears to vary by year as well as pond hydro-period type. We examined how important this diversity in pondhydroperiod was for net recruitment (i.e. number of metamorphsproduced) and population growth rates in the system. First, wecompared recruitment dynamics in ephemeral, semi-permanent,and permanent breeding ponds. Second, we examined how num-ber of recruits would change if all recruitment came solely fromephemeral ponds, semi-permanent ponds, or permanent ponds. Fi-nally, we used stochastic simulations to examine how the source ofrecruitment affected population growth rates in our system. Wealso examined the consequences of climate change-induced

habitat loss on population growth rates. We hypothesized thatnet recruitment and stochastic growth rate from a mixture ofponds would be higher and less variable than recruitment and sto-chastic growth rate from a landscape with a single pond type.

2. Materials and methods

2.1. Site description and field methods

All data were collected in the upper Little Rock Creek basin,located in the Selway-Bitterroot Wilderness in western Montana.Our study area contains nine consistently monitored breedingsites: three permanent ponds, two semi-permanent ponds, andfour ephemeral ponds (Fig. 1). Three of the small, adjacentephemeral ponds were analyzed as one unit because we were un-able to separate recruitment among them (E1; Fig. 1). Permanent,semi-permanent, and ephemeral ponds differed in surface areaand depth (Table 1). Permanent ponds are deeper (>1 m), neverdried over the course of the study, and are fed by streams andlakes. Semi-permanent ponds are only fed by snowpack. Theseponds dried between late August and late September in warmersummers, but retained some water throughout the year in coolersummers. They are unsuitable for overwintering. Ephemeral pondsare all <1-m deep at high water, fed only by snowpack, and driedevery year. During hotter summers, these ponds dried by early Au-gust, but during cooler summers, they held water until lateSeptember.

Although this basin contains many water bodies, genetic analy-ses indicate that the upper basin groups as one population (Funket al., 2005). Neither the ponds nor the lakes support fish popula-tions. R. luteiventris are the primary amphibian species in all ponds,though long-toed salamanders (Ambystoma macrodactylum) breedin small numbers in some of the ponds. The chief predators inthe ponds are gartersnakes (Thamnophis sirtalis and Thamnophiselegans).

In the spring, we searched all standing water bodies for eggmasses one to two times a week for the duration of the breedingseason. We determined number of egg masses deposited at eachpond in each year. From 2000 to 2003, we estimated clutch sizeand variance in a range of egg masses across all breeding pondsusing volumetric displacement (Corn and Livo, 1989; Morris and

Table 1Characteristics of breeding ponds in the Little Rock Creek drainage. Surface area,maximum depth, and emergent vegetation area are approximate values at high water.Emergent vegetation area indicates the approximate area in each pond potentiallyavailable for breeding in the spring. Hydroperiod is either characterized as permanent(P), semi-permanent (S), or ephemeral (E).

PondID

Surfacearea (m2)

Maximumdepth (m)

Emergent vegetationarea (m2)

Hydroperiod

P1 5354 2 18 PP2 1484 1.2 32 PP3 2097 1.5 350 PS1 3693 1 12 SS2 1109 1.2 16 SE1 394 0.7 8 EE1 166 0.4 2 EE1 434 0.6 400 EE2 681 0.3 24 E

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Tanner, 1969; Werner et al., 1999). In the late summer and fall, wecaptured newly metamorphosed frogs (metamorphs) emergingfrom all breeding ponds and marked them with a pond-specificbatch mark. We estimated the number of new metamorphs as theyemerged from the ponds using Chapman’s unbiased version of theLincoln-Peterson estimator (Williams et al., 2002). The batchmarks allowed us to track metamorph recruitment from individualponds each year. Due to forest fires and logistical constraints, wewere unable to estimate metamorph population size in 2000 and2005.

In mid-summer, all water bodies (including non-breeding lakes,which are used for summer foraging and overwintering) were sam-pled for juvenile and adult frogs using a robust sampling design(Pollock, 1982) that is fully described by McCaffery and Maxell(2010). Mark-recapture data from individually marked juvenileand adult frogs were used to parameterize matrix models (seebelow).

2.2. Pond-specific recruitment

To calculate the total number of eggs produced annually in eachpond, we multiplied the number of egg masses for each pond by806, the mean clutch size estimated from our volumetric displace-ment calculations in 2000–2003 across ponds. There was no signif-icant difference in clutch size among ponds during those fouryears. We then calculated the proportion of all eggs laid in eachpond in each year.

We calculated pond-specific egg to metamorph survival ratesfor each year by dividing the number of metamorphs producedin each pond by the number of eggs laid in that pond in that year.To calculate survival from metamorphosis to one year, we dividedthe number of 1-yr-old frogs for each year by the total number ofmetamorphs produced the fall before. One year-olds were definedas animals 34 mm snout-vent length (SVL) or smaller that werecaptured in our mid-summer surveys and individually marked.This maximum length represented a natural break in frog size, withthe next largest frogs typically >40 mm SVL. We estimated theirpopulation size using Huggins closed capture models in ProgramMARK (White and Burnham, 1999). These models allow estimationof population size from initial capture probabilities and recaptureprobabilities of individually marked animals (Huggins, 1989).One yr-olds could not be assigned to their natal pond because ofhigh metamorph dispersal in the basin.

We calculated proportion of egg masses laid, egg to metamorphsurvival, and number of metamorphs produced for each of sevenbreeding ponds annually. Then, we compared these variablesamong the three pond types (permanent, semi-permanent, andephemeral). Proportional and survival rate data were arcsine

square root transformed, and metamorph counts were square roottransformed for normalization prior to statistical analysis. Wecompared the mean of these recruitment parameters using analy-sis of variance (ANOVA) and multiple comparison procedures. Wecompared the variance in these parameters using Levene’s test forequality of variances.

2.3. Effects of pond heterogeneity on net recruitment

Using the proportions of egg masses laid in each pond andpond-specific egg to metamorph survival rates, we determinednet recruitment under hypothetical scenarios where the numberof eggs laid in each year remained constant, but was shifted toeither (1) only permanent, (2) only semi-permanent, or (3) onlyephemeral ponds according to their field distribution. For example,for the permanent pond scenario, the total of the eggs laid acrossthe whole population was shifted to the three permanent pondsin proportion to their observed distribution in each year. Thus,for the first year of this scenario, P1 had 57%, P2 had 10%, and P3had 33% of the total eggs. We multiplied the new number of eggsby the egg to metamorph survival rate for each pond and year todetermine the number of metamorphs produced in each scenario.We calculated the net recruitment in each year for each scenario,and compared the net recruitment from these homogeneous sce-narios to the net recruitment when all ponds contribute to recruit-ment (our observed heterogeneous system). To examine theimportance of pond hydroperiod heterogeneity to recruitmentdynamics, we compared the mean net recruitment using ANOVAand multiple comparison procedures, and compared variance innet recruitment using Levene’s test for equality of variances. Inall analyses, years were the unit of replication (N = 8).

2.4. Effects of pond heterogeneity and habitat loss on populationgrowth rate

We parameterized a female-based, post birth pulse Leftkovichmatrix using vital rate means and variances for the ten years ofour study (Caswell, 2001; Appendix A). Survival and transitionparameters for juvenile, subadult, and adult survival rates wereestimated using capture-mark-recapture (CMR) analysis (seeMcCaffery and Maxell, 2010 for model details and description oflife stages). These models also estimated annual population sizefor each life stage. Breeding probability was estimated by dividingthe number of egg masses deposited by the closed population esti-mate for adult females each year. We estimated recruitment sepa-rately for each individual breeding pond, resulting in sevenfecundity terms and seven egg to metamorph survival terms(Appendix A).

To examine how hydroperiod heterogeneity influences popula-tion growth rates, we simulated population growth rates for thesame scenarios described above: all observed ponds (heteroge-neous hydroperiods), permanent, semi-permanent, and ephemeral.For each scenario, we calculated new breeding proportions to re-flect the shift in breeding proportions to each pond type, as de-scribed above. First, we calculated asymptotic growth rates,which show the expected growth rate if all vital rates were to re-main constant over time. Then, we used stochastic projection ma-trix model simulations to estimate stochastic population growth.Here, each annual vital rate value is drawn from a distributionusing the mean and variance (across years) of that vital rate fromour field estimates. For all simulations, we used code in MATLABmodified from Morris and Doak (2002; Box 8.10). We did not in-clude within year correlations among vital rates because the num-ber of significant correlations among vital rates was close to whatwe would expect by chance, though we stress that these vital raterelationships could change in the future and are important to test

(a)

172 R.M. McCaffery et al. / Biological Conservation 170 (2014) 169–176

in demographic studies. We started our simulations with 100 adultfemales and a stable stage distribution. In addition to comparingthe different scenarios, we examined the percent reduction in sto-chastic population growth rates relative to deterministic growthrates as a metric to quantify the extent to which heterogeneitymay buffer population growth rates in a stochastic environment.

Finally, we examined the consequences of habitat loss onstochastic population growth rate in three scenarios of pond lossdue to warmer and drier future climates. In the first scenario, per-manent and semi-permanent ponds are left unchanged, butephemeral ponds are lost. In the second scenario, permanent pondsare left unchanged, but the semi-permanent ponds becomeephemeral ponds and the ephemeral ponds are lost. In the finalscenario, permanent ponds become semi-permanent, semi-permanent ponds become ephemeral, and ephemeral ponds arelost. For each of these, we adjusted the recruitment vital rates toreflect the shift in pond type and the loss of recruitment due tohabitat loss. We used the same simulation approach and startingvalues as described above.

(b)

Fig. 2. Box plots of (a) egg to metamorph survival across years and (b) number ofmetamorphs produced across years in permanent, semi-permanent, and ephemeralbreeding ponds. Bars indicate median values, boxes show 50th percentiles, anderror bars show 95th percentiles. The dot represents unusually high egg tometamorph survival and recruitment in semi-permanent ponds in 2008.

3. Results

3.1. Pond-specific recruitment

The proportion of egg masses laid differed among the threepond types (ANOVA, F = 270, p < 0.001). The proportion of eggs laidin permanent ponds was over four times higher than in eithersemi-permanent or ephemeral ponds (Tukey’s HSD, p < 0.001),and there was no difference in the proportion of eggs laid inephemeral and semi-permanent ponds (Tukey’s HSD, p = 0.298).

Egg to metamorph survival fluctuated among years for allbreeding ponds. There were weak negative correlations in egg tometamorph survival among all three pond types, suggesting thatdifferent pond types had more successful recruitment in differentyears. Survival to metamorphosis also differed among pond types(ANOVA, F = 4.25, p = 0.028; Fig. 2a). Egg to metamorph survivalaveraged three times higher in semi-permanent ponds thanephemeral (Tukey’s HSD, p = 0.032) and permanent ponds(p = 0.087). This was driven by one year of extremely high survivalin one semi-permanent pond. There was no statistical difference insurvival between ephemeral and permanent ponds (p = 0.877).There was no statistical difference in the variability of egg to meta-morph survival among the three pond types.

Metamorph recruitment differed among the pond types (ANO-VA, F = 3.73, p = 0.041). Successful recruitment in ponds was mostconsistent in semi-permanent ponds (Table 2), where ponds pro-duced metamorphs in all but one year of the study. Successfulrecruitment was much more sporadic in the ephemeral ponds.Two of the permanent ponds produced most of the metamorphsin the early years of the study, but semi-permanent and ephemeralponds produced all of the metamorphs in the last two years. Theselast two years were cool and had shorter growing seasons, so tad-poles in the colder, stream-fed permanent ponds simply did nothave enough days to metamorphose before winter, while warmertemperatures in the semi-permanent and ephemeral ponds facili-tated some recruitment at these sites. Despite the higher survivalrates in semi-permanent ponds, there was no statisticallysignificant difference in the number of metamorphs produced frompermanent ponds and semi-permanent ponds across years(Tukey’s HSD, p = 0.796; Fig. 2b). However, on average there wereover four times more metamorphs produced in permanent pondsthan ephemeral ponds (p = 0.041), and over two times moremetamorphs produced in semi-permanent than ephemeral ponds(p = 0.143). Permanent ponds had eight times higher variance inmetamorph production than ephemeral ponds (Levene’s test for

equality of variance, F = 6.569, p = 0.023) and four times higher var-iance than semi-permanent ponds (F = 4.113, p = 0.062; Fig. 2b).This was driven by the last two years of the study, when perma-nent ponds had no successful recruitment due to cool summerand early onset of winter in contrast to warmer and drier yearswhen several hundred metamorphs emerged from these ponds.

3.2. Effects of pond heterogeneity on net recruitment

Total metamorphs produced differed among scenarios wherewe varied the source pond type but kept total eggs laid constant(ANOVA, F = 3.468, p = 0.029; Fig. 3a). Specifically, the scenariowith all reproduction in semi-permanent ponds resulted in moremetamorphs than the scenarios with only ephemeral (Tukey’sHSD, p = 0.029) or only permanent (p = 0.075) ponds. However, thisscenario did not differ from the scenario where all pondscontribute in their current proportions (p = 0.368). Production of

Table 2Recruitment at different pond types in different years. 1 = Years where each pond had most animals reach metamorphosis, (1) = years where each pond had some animals reachmetamorphosis, but less than ten total metamorphs were captured, and 0 = years where no individuals metamorphosed.

Year Pond

P1 P2 P3 S1 S2 E1 E2

2001 1 1 1 1 1 1 12002 1 0 (1) 1 1 1 12003 1 1 1 1 1 0 (1)2004 1 1 1 1 1 1 (1)2006 1 0 1 1 1 0 02007 1 1 1 1 1 0 02008 0 0 0 1 1 (1) 02009 0 0 0 1 0 1 0Total years with successful recruitment 6 4 5 (6) 8 7 4 (5) 2 (4)

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metamorphs did not differ between any other pairs of scenarios.The scenario with all ponds contributing was less variable thanthe scenarios with only ephemeral (Levene’s test for equality ofvariances, F = 8.149, p = 0.013) or only semi-permanent (F = 0.060,p = 0.060) ponds, but was not different from the scenario with onlypermanent ponds (F = 0.875, p = 0.365).

3.3. Effects of pond heterogeneity and habitat loss on populationgrowth rate

The deterministic growth rate for the population was highest inthe scenario with reproduction in only semi-permanent ponds(k = 0.87), lowest with reproduction in only permanent ponds(k = 0.72), and intermediate with reproduction in all observed

Fig. 3. (a) Box plots of estimated net recruitment across years and (b) meanstochastic population growth rate for four recruitment scenarios: (1) currentmetamorph recruitment in Little Rock Creek basin (Observed), (2) all recruitmentcomes from permanent ponds (Permanent), (3) all recruitment comes from semi-permanent ponds (Semi-Permanent), and (4) all recruitment comes from ephem-eral ponds (Ephemeral). Total number of eggs laid in each scenario is the same.

ponds or only ephemeral ponds (k = 0.75). These values reflectthe higher mean egg to metamorph survival rates found in thetwo semi-permanent ponds compared to other pond types. How-ever, this metric does not incorporate variance in the recruitmentparameters.

When we conducted stochastic simulations, the scenario withonly semi-permanent ponds still had the highest growth rate(k = 0.80), followed by the scenario with all ponds (k = 0.72). Sce-narios with only permanent ponds (k = 0.67) and only ephemeralponds (k = 0.68) had the lowest growth rates (Fig. 3b). Variancein egg to metamorph survival for both semi-permanent andephemeral ponds was higher than that for permanent ponds, andlikely contributed to stochastic k being proportionally lower thandeterministic k in scenarios that only included these ponds (8.1%and 7.9% lower, respectively, versus 5.8% for only permanentponds). The stochastic k for the scenario with all observed pondscontributing to recruitment declined the least from the determin-istic k as compared with other scenarios (4.9%), suggesting thatheterogeneity in pond hydroperiod buffers population growthrates under stochasticity.

In the simulations exploring the effect of pond loss on stochas-tic k, the scenario with the loss of ephemeral ponds resulted in asmall reduction in population growth rate (k = 0.70) compared tothe scenario with all ponds contributing in their current propor-tions (k = 0.72; Fig. 4). The shift in hydroperiod of semi-permanentponds to ephemeral, along with the loss of ephemeral ponds, in thesecond scenario decreased k to 0.67. In the final scenario, wherethe hydroperiod of permanent ponds is shifted to semi-permanent,semi-permanent ponds are shifted to ephemeral, and ephemeralponds are lost, stochastic k was 0.63 (Fig. 4).

4. Discussion

4.1. Pond-specific recruitment dynamics

Our study demonstrates complex recruitment dynamics for R.luteiventris in a heterogeneous breeding landscape. Ephemeral,semi-permanent, and permanent ponds show contrastingdynamics in different years. In particular, recruitment from semi-permanent and ephemeral ponds dominated in two cool wet years(2008–2009), and recruitment from permanent ponds dominatedin years that were hotter or had less snow the preceding winter(2003–2007). As a result, over this dynamic 10 yr, we neverwitnessed complete recruitment failure, even though all but onepond experienced recruitment failure at least once (Table 2). Thus,heterogeneity in hydroperiod stabilized recruitment dynamics,because variability in dynamics across the whole population waslower than what we measured in individual ponds. These resultsare similar to what has been observed for other amphibians(Whiteman and Wissinger, 2005; Hartel et al., 2007; Karraker

Fig. 4. Mean stochastic population growth rates for the current heterogeneouspopulation (Observed) and three pond loss scenarios: (1) permanent and semi-permanent ponds are unchanged and ephemeral ponds are lost; (2) permanentponds are unchanged, semi-permanent ponds shift to ephemeral hydroperiods, andephemeral ponds are lost; and (3) permanent ponds shift to semi-permanenthydroperiods, semi-permanent ponds shift to ephemeral hydroperiods, andephemeral ponds are lost.

174 R.M. McCaffery et al. / Biological Conservation 170 (2014) 169–176

and Gibbs, 2009). For example, Hartel et al. (2007) found that whileyellow-bellied toads (Bombina variegata) primarily bred in perma-nent or semi-permanent ponds, breeding in ephemeral ponds inwet years increased the percent of ponds with successful recruit-ment from 40% to 90%. In dry years, breeding in these ephemeralponds resulted in complete failure to reach metamorphosis. Ourresults also corroborate other researchers’ recommendations toconserve a diversity of pond hydroperiods on the landscape to pro-mote pond-breeding amphibian population persistence (Babbittet al., 2003; Snodgrass et al., 2000).

We found that ponds with long hydroperiods and permanentponds had the highest net recruitment, which is similar to whathas been documented in other studies that have examinedamphibian recruitment dynamics (Baldwin et al., 2006; Semlitsch,1987; Semlitsch et al., 1996; Karraker and Gibbs, 2009; Whitemanand Wissinger, 2005). However, in other high elevation systems,ponds with permanent hydroperiods are often colonized withaquatic predators like fish, which can have strong negative impactson recruitment (Knapp and Matthews, 2000; Pilliod and Peterson,2001; Pope, 2008; but see Pilliod et al., 2010). One feature thatmakes our system unusual compared to many of these systems isthe lack of introduced fish in permanent ponds, which makes themmore generally suitable for recruitment. In our system cool sum-mers limited recruitment from permanent ponds, because tadpolesin these colder environments did not have time to metamorphoseduring the shorter, cooler summers (McCaffery and Maxell, 2010).For R. luteiventris inhabiting mountain systems, the ability of tad-poles to metamorphose within a short growing season is key torecruitment success, and the presence of multiple pond types helpspromote consistent recruitment across years. However, other mon-tane amphibians have multiple year larval stages, making perma-nent, fishless breeding ponds more critical to recruitment success(Lacan et al., 2008; Whiteman and Wissinger, 2005). Life historyelements such as length of the larval period will influence howrecruitment dynamics may be affected by environmental variabil-ity and habitat heterogeneity.

4.2. Effects of pond heterogeneity on net recruitment and populationgrowth rate

Our modeling results for metamorph production show that aheterogeneous system had less variability in net recruitmentacross years than hypothetical systems composed of only

semi-permanent ponds or only ephemeral ponds, and similar var-iability to a system with only permanent ponds. Furthermore, netrecruitment was lower in the hypothetical scenario with onlyephemeral ponds than all other scenarios. This finding agrees withother observations that net recruitment can be extremely variable(Semlitsch et al., 1996) and lower (Karraker and Gibbs, 2009) inephemeral ponds than in semi-permanent or permanent ponds.However, ponds with shorter hydroperiods did play a role in stabi-lizing recruitment in the dynamic, 10-yr period over which thisstudy was conducted, and may be particularly important in highelevation environments where recruitment is often limited byshort growing seasons. Our study system is at the upper ecologicallimit for R. luteiventris, and the importance of hydroperiod diversitymay be different for lower elevation or lower latitude populations.For example, permanent water bodies may be the most criticalhabitats to persistence of R. luteiventris at lower elevation siteswhere drought can severely limit recruitment from ephemeralponds (Hossack et al., 2013).

The effect of pond type on survival to metamorphosis and num-ber of metamorphs produced was also evident when we examinedthe repercussions of pond heterogeneity on population growthrate. The scenario with semi-permanent ponds had the highestpopulation growth rate, followed by the scenario with all ponds.This result was largely due to extremely high egg to metamorphsurvival in the two semi-permanent ponds in 2008. It is possiblethat the occasional conditions that promote exceptionally high sur-vival in these pond types have a true influence on recruitmentdynamics. However, while the survival rate was high, net recruit-ment in these ponds was not necessarily higher than other ponds,because the total number of eggs laid tended to be higher in per-manent ponds. Our results do not qualitatively change if we re-move this data point from our study, because semi-permanentponds had the highest egg to metamorph survival in most years.While we only had two semi-permanent ponds in our study, thissuggests that a landscape rich in semi-permanent breeding ponds,either now or in the future, would have the highest long-termgrowth rate, provided that environmental conditions did not sys-tematically change over time and that complementary permanentoverwintering sites were still available. However, when comparingdeterministic population growth rates to stochastic growth rates,our results also suggest that in a stochastic environment, our ob-served heterogeneous system had growth rates that were morebuffered from this stochasticity than the homogeneous scenarios.Therefore, a landscape of heterogeneous hydroperiods may haveproportionally higher population growth rates than a homoge-neous landscape, which would lead to higher population viabilityin the long-term.

Whereas other studies examining the effect of habitat heteroge-neity on population dynamics examine fluctuations in estimates oftotal population size (Kindvall, 1996; McLoughlin et al., 2002;Oliver et al., 2010), our study only examines the effect of heteroge-neity on egg to metamorph life stages. Other habitat features, suchas foraging and overwintering habitat, may be more important tojuvenile and adult frogs, and be less tied to hydroperiod. Iflandscape heterogeneity were able to promote persistence of adultfrog populations, as suggested by Piha et al. (2007) for the commonfrog (Rana temporaria), population growth rates might be moreimpacted by homogenization of terrestrial habitats. Althoughhabitat heterogeneity has the potential to decrease variability inproduction of metamorphs, it may not be critical to populationviability if other factors are causing declines in post-metamorphiclife stages (McCaffery et al., 2012). For example, fishless lakehabitat provides key foraging and overwintering habitat in oursystem and others (e.g., Pilliod et al., 2002). The presence ofcomplementary resources throughout the system is likely neces-sary for long-term population persistence. Furthermore, other

R.M. McCaffery et al. / Biological Conservation 170 (2014) 169–176 175

elements of amphibian life histories such as breeding frequency,age at first reproduction, and longevity (e.g., Morris et al., 2008)can influence how environmental variability may impact popula-tion growth rates. Finally, the effects of environmental variationon other elements of these montane communities, such as preda-ceous gartersnakes and invertebrate food resources, may alsoimpact the total effects of environmental stochasticity onR. luteiventris population viability and on the dynamics of thecommunity.

Overall, population growth rates were low, and this is likelydriven by changes in juvenile and adult survival rates over thecourse of the study. Both juvenile and adult survival rates declinedfrom 2000 to 2009 (see McCaffery and Maxell, 2010 for discussion),while egg to metamorph survival rates remained relatively con-stant across ponds. Nevertheless, comparisons of these growthrates show that differences in recruitment vital rates due to hydro-period differences can alter population growth rates. In amphibianpopulation ecology, few studies have used matrix population mod-els to examine the contribution of different vital rates to overallpopulation growth (Biek et al., 2002). As such, variation in recruit-ment has rarely been put into a population context (but seeGovindarajulu et al., 2005; Vonesh and De La Cruz, 2002), and thisstudy demonstrates how recruitment variation can alter popula-tion growth rates for a pond-breeding amphibian species.

5. Conclusions

Climate change models around the world predict an increase inclimatic variability (Easterling et al., 2000). Analyses of climatedata for Montana indicate an increase in the number of extremelyhot days (P32.2 �C) per year and an increase in the frequency ofyears with an extreme number of hot days (Pederson et al.,2010). These trends might be positive for recruitment from perma-nent ponds, which is highly correlated with growing degree days(an index of the growing season; R = 0.790, p = 0.035), but couldhave deleterious consequences for recruitment from semi-perma-nent and ephemeral wetlands. Future climate changes will likelyreduce both the number and diversity of ponds on the landscape.For example, an increase in extremely hot years could increasethe frequency of recruitment failure in ephemeral wetlands. Addi-tionally, decreases in snowpack could ultimately lead to the loss ofephemeral ponds, and shortening of other pond hydroperiods.When we explored these scenarios, we found that the loss ofephemeral ponds did not substantially decrease population growthrates. However, population growth rates declined substantially ashydroperiods shortened across the basin, particularly if permanentponds became semi-permanent. Our results suggest that the pop-ulation may be able to sustain some loss of recruitment, particu-larly in the ephemeral ponds, but that permanent loss of certainbreeding pond types will lead to decreases in population viability.It is possible that new habitats may be formed as montane climateschange (e.g., new water bodies form by melting of permanentsnowfields at elevations where the growing season is currentlytoo short to support amphibians). Yet permanent ponds may be-come increasingly important to stabilizing montane amphibianrecruitment dynamics as global warming progresses and semi-per-manent wetlands are lost.

The potential to manage for heterogeneous habitat may helpsustain populations into the future. For example, eradication ofnon-native fishes from permanent lakes and ponds can have posi-tive consequences for amphibian populations across the mountainWest (Knapp et al., 2007; Pope, 2008), especially for species withmultiple-year larval stages. This management action can increasethe diversity and quantity of breeding habitat for many amphibianspecies experiencing variable inter-annual precipitation. The

eradication of fishes from mountain lakes may also be critical tosustaining amphibian populations in the face of climate change ifrecruitment from semi-permanent lakes and wetlands becomesless frequent due to summer drought and snowpack declines(Lacan et al., 2008). Habitat heterogeneity could also be incorpo-rated into the creation of breeding habitat via pond constructionand restoration at different elevations. This management tech-nique may become increasingly important as biologists work toconserve populations in the face of increased drought and variabil-ity in precipitation (Hossack et al., 2013; Shoo et al., 2011).

No other studies have explicitly examined the potential for hab-itat heterogeneity to stabilize recruitment dynamics in amphibianpopulations in stochastic environments. We monitored recruit-ment dynamics in seven breeding ponds over 10-yr with extremelyhigh inter-annual environmental variability, and demonstrated thedynamic contribution of ephemeral, semi-permanent, and perma-nent pond types to annual production of metamorphs. Our studyprovides evidence that heterogeneity in pond hydroperiod can leadto less variability in recruitment over time, and demonstrates thatchanges in egg to metamorph survival rates in relation to pondtype can have a large effect on population growth rate. The impor-tance of breeding pond heterogeneity may increase as climatechange progresses, especially in montane systems where droughtand inter-annual variability in weather conditions are expectedto increase.

Acknowledgements

We are grateful for the many field assistants who have collecteddata during this study. We thank Elizabeth Crone, Winsor Lowe,Scott Mills, Adam Sepulveda, and two anonymous reviewers forconstructive comments on this manuscript. Fieldwork was par-tially supported by funding from the U.S. Geological Survey’sAmphibian Research and Monitoring Initiative (ARMI) and U.S. For-est Service Region 1 Inventory and Monitoring grants. Any use oftrade, firm, or product names is for descriptive purposes onlyand does not imply endorsement by the U.S. Government. This isARMI contribution number 464.

Appendix A. Supplementary material

Supplementary data associated with this article can be found, inthe online version, at http://dx.doi.org/10.1016/j.biocon.2013.12.013.

References

Amarasekare, P., 2003. Competitive coexistence in spatially structuredenvironments: a synthesis. Ecol. Lett. 6, 1109–1122.

Babbitt, K.J., Baber, M.J., Tarr, T.L., 2003. Patterns of larval amphibian distributionalong a wetland hydroperiod gradient. Can. J. Zool. 81, 1539–1552.

Baldwin, R.F., Calhoun, A.J.K., deMaynadier, P.G., 2006. The significance ofhydroperiod and stand maturity for pool-breeding amphibians in forestedlandscapes. Can. J. Zool. 86, 1604–1615.

Biek, R., Funk, W.C., Maxell, B.A., Mills, L.S., 2002. What is missing in amphibiandecline research: insights from ecological sensitivity analysis. Conserv. Biol. 16,728–734.

Boyce, M.S., Haridas, C.V., Lee, C.T., 2006. Demography in an increasingly variableworld. Trends Ecol. Evolut. 21, 141–148.

Caswell, H., 2001. Matrix Population Models–Construction, Analysis, andInterpretation, second ed. Sinauer Associates, Sunderland, Massachusetts.

Chesson, P., 2000a. Mechanisms of maintenance of species diversity. Ann. Rev. Ecol.Syst. 31, 343–366.

Chesson, P., 2000b. General theory of competitive coexistence in spatially-varyingenvironments. Theor. Popul. Biol. 58, 211–237.

Corn, P.S., Livo, L.J., 1989. Leopard frog and wood frog reproduction in Colorado andWyoming. Northwestern Nat. 70, 1–9.

Daszak, P., Scott, D.E., Kilpatrick, A.M., Faggioni, C., Gibbons, J.W., Porter, D., 2005.Amphibian population declines at Savannah River Site are linked to climate, notchytridiomycosis. Ecology 86, 3232–3237.

176 R.M. McCaffery et al. / Biological Conservation 170 (2014) 169–176

Easterling, D.R., Meehl, G.A., Parmesan, C., Changnon, S.A., Karl, T.R., Mearns, L.O.,2000. Climate extremes: observations, modeling, and impacts. Science 289,2068–2074.

Fagan, W.F., Meir, E., Prendergast, J., Folarin, A., Karieva, P., 2001. Characterizingpopulation vulnerability for 758 species. Ecol. Lett. 4, 132–138.

Funk, W.C., Blouin, M.S., Corn, P.S., Maxell, B.A., Pilliod, D.S., Amish, S., Allendorf,F.W., 2005. Population structure of Columbia spotted frogs (Rana luteiventris) isstrongly affected by landscape. Mol. Ecol. 14, 483–496.

Gould, W.R., Patla, D.A., Daley, R., Corn, P.S., Hossack, B.R., Bennetts, R., Peterson,C.R., 2012. Estimating occupancy in large landscapes: evaluation of amphibianmonitoring in the Greater Yellowstone Ecosystem. Wetlands 23, 379–389.

Govindarajulu, P., Altwegg, R., Anholt, B.R., 2005. Matrix model investigation ofinvasive species control: bullfrogs on Vancouver Island. Ecol. Appl. 15, 2161–2170.

Hartel, T., Nemes, S., Mara, G., 2007. Breeding phenology and spatio-temporaldynamics of pond use by the yellow-bellied toad (Bombina variegata)population: the importance of pond availability and duration. Acta Zool. Lit.17, 56–63.

Hossack, B.R., Adams, M.J., Pearl, C.A., Wilson, K.W., Bull, E.L., Lohr, K., Patla, D.,Pilliod, D.S., Jones, J.M., Wheeler, K.K., McKay, S.P., Corn, P.S., 2013. Roles ofpatch characteristics, drought frequency, and restoration in long-term trends ofa widespread amphibian. Conserv. Biol. 27, 1410–1420.

Huggins, R.M., 1989. On the statistical analysis of capture-recapture experiments.Biometrika 76, 133–140.

Inchausti, P., Halley, J., 2001. Investigation long-term ecological variability using theglobal population dynamics database. Science 293, 655–657.

Karraker, N.E., Gibbs, J.P., 2009. Amphibian production in forested landscapes inrelation to wetland hydroperiod: a case study of vernal pools and beaver ponds.Biol. Cons. 142, 2293–2302.

Kindvall, O., 1996. Habitat heterogeneity and survival in a bush cricketmetapopulation. Ecology 77, 207–214.

Knapp, R.A., Matthews, K.R., 2000. Non-native fish introductions and the decline ofthe mountain yellow-legged frog from within protected areas. Conserv. Biol. 14,428–438.

Knapp, R.A., Boiano, D.M., Vredenburg, V.T., 2007. Removal of nonnative fish resultsin population expansion of a declining amphibian (mountain yellow-leggedfrog, Rana muscosa). Biol. Cons. 135, 11–20.

Lacan, I., Matthews, K.R., Feldman, K., 2008. Interaction of an introduced predatorwith future effects of climate change in the recruitment dynamics of theimperiled Sierra Nevada yellow-legged frog (Rana sierrae). Herpetol. Conserv.Biol. 3, 211–223.

McCaffery, R.M., Maxell, B.A., 2010. Decreased winter severity increases viability ofa montane frog population. Proc. Natl. Acad. Sci. USA 107, 8644–8649.

McCaffery, R., Solonen, A., Crone, E.E., 2012. Frog population viability under presentand future climate conditions: a Bayesian state-space approach. J. Anim. Ecol.81, 978–985.

McLoughlin, J.F., Hellmann, J.J., Boggs, C.L., Ehrlich, P.R., 2002. The route toextinction: population dynamics of a threatened butterfly. Oecologia 132,538–548.

Meyer, A.H., Schmidt, B.R., Grossenbacher, K., 1998. Analysis of three amphibianpopulations with quarter-century long time-series. Proc. R. Soc. Lond. [Biol.]265, 523–528.

Morris, W.F., Doak, D.F., 2002. Quantitative Conservation Biology. SinauerAssociates Inc., Sunderland.

Morris, R.L., Tanner, W.W., 1969. The ecology of the western spotted frog, Ranapretiosa pretiosa Baird and Girard: a life history study. Great Basin Nat. 29, 45–81.

Morris, W.F., Pfister, C.A., Tuljapurkar, S., Haridas, C.V., Boggs, C.L., Boyce, M.S.,Bruna, E., Church, D.R., Coulson, T., Doak, D.F., Forsyth, S., Gaillard, J.-M., Horvitz,C.C., Kalisz, S., Kendall, B.E., Knight, T.M., Lee, C.T., Menges, E.S., 2008. Longevitycan buffer plant and animal populations against changing climatic variability.Ecology 89, 19–25.

Oliver, T., Roy, D.B., Hill, J.K., Brereton, T., Thomas, C.D., 2010. Heterogeneouslandscapes promote population stability. Ecol. Lett. 13, 473–484.

Pechmann, J.H.K., Scott, D.E., Semlitsch, R.D., Caldwell, J.P., Vitt, L.J., Gibbons, J.W.,1991. Declining amphibian populations: the problem of separating humanimpacts from natural fluctuations. Science 253, 892–895.

Pederson, G.T., Graumlich, L.J., Fagre, D.B., Kipfer, T., Muhlfield, C.C., 2010. A centuryof climate and ecosystem change in Western Montana: what do temperaturetrends portend? Clim. Change 98, 133–154.

Piha, H., Luoto, M., Piha, M., Merila, J., 2007. Anuran abundance and persistence inagricultural landscapes during a climatic extreme. Global Change Biol. 13, 300–311.

Pilliod, D.S., Peterson, C.R., 2001. Local and landscape effects of introducedtrout on amphibians in historically fishless watersheds. Ecosystems 4,322–333.

Pilliod, D.S., Peterson, C.R., Ritson, P.I., 2002. Seasonal migration of Columbia spottedfrogs (Rana luteiventris) among complementary resources in a high mountainbasin. Can. J. Zool. 80, 1849–1862.

Pilliod, D.S., Hossack, B.R., Bahls, P.F., Bull, E.L., Corn, P.S., Hokit, G., Maxell, B.A.,Munger, J.C., Wyrick, A., 2010. Non-native salmonids affect amphibianoccupancy at multiple spatial scales. Divers. Distrib. 16, 959–974.

Pollock, K.H., 1982. A capture-recapture design robust to unequal probability ofcapture. J. Wildl. Manage. 46, 752–757.

Pope, K.L., 2008. Assessing changes in amphibian population dynamicsfollowing experimental manipulations of introduced fish. Conserv. Biol.22, 1572–1581.

Semlitsch, R.D., 1987. Relationship of pond drying to the reproductive success of thesalamander Ambystoma talpoideum. Copeia 1987, 61–69.

Semlitsch, R.D., 2000. Principles for management of aquatic-breedingamphibians. J. Wildl. Manage. 64, 615–631.

Semlitsch, R.D., Bodie, J.R., 1998. Are small, isolated wetlands expendable? Conserv.Biol. 12, 1129–1133.

Semlitsch, R.D., Scott, D.E., Pechmann, J.H.K., Gibbons, J.W., 1996. Structure anddynamics of an amphibian community. In: Cody, M.L., Smallwood, J.A. (Eds.),Long-term Studies of Vertebrate Communities. Academic Press, San Diego, pp.217–248.

Shoo, L.P., Olson, D.H., McMenamin, S.K., Murray, K.A., Van Sluys, M., Donnelly, M.A.,Stratford, D., Terhivuo, J., Merino-Viteri, A., Herbert, S.M., Bishop, P.J., Corn, P.S.,Dovey, L., Griffiths, R.A., Lowe, K., Mahony, M., McCallum, H., Shuker, J.D.,Simpkins, C., Skerratt, L.F., Williams, S.E., Hero, J.-M., 2011. Engineering a futurefor amphibians under climate change. J. Appl. Ecol. 48, 487–492.

Skelly, D.K., Werner, E.E., Cortwright, S.A., 1999. Long-term distributional dynamicsof a Michigan amphibian assemblage. Ecology 80, 2326–2337.

Snodgrass, J.W., Komoroski, M.J., Bryan Jr., A.L., Burger, J., 2000. Relationships amongisolated wetland size, hydroperiod, and amphibian species richness:implications for wetland regulations. Conserv. Biol. 14, 414–419.

Souther, S., McGraw, J.B., 2011. Evidence of local adaptation in the demographicresponse of American ginseng to interannual temperature variation. Conserv.Biol. 25, 922–931.

Trenham, P.C., Koenig, W.D., Mossman, M.J., Stark, S.L., Jagger, L.A., 2003. Regionaldynamics of wetland-breeding frogs and toads: turnover and synchrony. Ecol.Appl. 13, 1522–1532.

Vonesh, J.R., De La Cruz, O., 2002. Complex life cycles and density dependence:assessing the contribution of egg mortality to amphibian declines. Oecologia133, 325–333.

Werner, J.K., Weaselhead, J., Plummer, T., 1999. The accuracy of estimating eggs inanuran egg masses using weight or volume measurements. Herpetol. Rev. 30,30–31.

White, G.C., Burnham, K.P., 1999. Program MARK: survival estimation frompopulations of marked animals. Bird Study 46 (Supplement), 120–138.

Whiteman, H.H., Wissinger, S.A., 2005. Amphibian population cycles and long-termdata sets. In: Lannoo, M.J. (Ed.), Conservation and Status of North AmericanAmphibians. University of California Press, Berkeley, pp. 177–184.

Williams, B.K., Nichols, J.D., Conroy, M., 2002. Analysis and Management of AnimalPopulations. Academic Press, San Diego.

Winter, T.C., 2000. The vulnerability of wetlands to climate change: a hydrologicallandscape perspective. J. Am. Water Resour. Assn. 36, 305–311.