ORIGINAL PAPER

Climatic influences on the breeding biology of the agile frog(Rana dalmatina)

Magali Combes1 & David Pinaud1& Christophe Barbraud1

& Jacques Trotignon2& François Brischoux1

Received: 27 July 2017 /Revised: 7 December 2017 /Accepted: 8 December 2017# Springer-Verlag GmbH Germany, part of Springer Nature 2017

AbstractSevere population declines of amphibians have been shown to be attributed to climate change. Nevertheless, the various mechanismsthrough which climate can influence population dynamics of amphibians remain to be assessed, notably to disentangle the relativesynergetic or antagonistic influences of temperature and precipitations on specific life history stages. We investigated the impact ofrainfall and temperature on the egg-clutch abundance in a population of agile frog (Rana dalmatina) during 29 years (1987–2016) on14 breeding sites located in Brenne Natural Park, France. Specifically, we examined the influence of environmental conditionsoccurring during five temporal windows of the year cycle corresponding to specific life history stages. Overall, our results suggestthat the year-to-year fluctuations of egg-clutch abundances in Brenne Natural Park were partly dependent on local climatic conditions(rainfall and temperature). Climate seemed to influence breeding frogs during the autumn-winter period preceding reproduction. Springand summer conditions did not influence reproduction. Additionally, we failed to detect effects of climatic conditions on newlymetamorphosed individuals. Other factors such as density dependence and inter-specific interactions with introduced predators arelikely to play a significant role in reproduction dynamics of the studied frog populations.

Keywords Rainfall . Temperature . Climatic conditions . Population dynamics . Amphibian . Rana dalmatina

Introduction

Amphibians are one of the most threatened vertebrate taxa, suf-fering severe population declines (Houlahan et al. 2000; Stuartet al. 2004; Beebee and Griffiths 2005). Indeed, these taxa aresensitive to a wide array of anthropogenic factors, such as habitatloss and fragmentation, environmental contamination, direct ex-ploitation, and alien species introduction (Collins and Storfer2003; Beebee and Griffiths 2005).

In addition, amphibians are among the most sensitive speciesto climate change (Blaustein et al. 2010). Amphibians are ecto-thermic vertebrates with permeable skin, which requires specificmicroclimatic conditions to fulfil its role in respiration and os-moregulation (Hillman 2009) and as such, most of their lifehistory traits are tightly dependant on environmental temperatureand hydric conditions (Jørgensen 1986; Köhler et al. 2011; Gaoet al. 2015a). Through their effect on metabolism, climatic con-ditions (i.e., moisture and temperature) strongly influence theenergy use (Reading and Clarke 1995; Reading 2007; Dillonet al. 2010), activity patterns (e.g., mobility of feeding,Jørgensen 1986; Chan-McLeod 2003; Köhler et al. 2011), andthe initiation of critical life history phases such as hibernation orbreeding (Gao et al. 2015a, b). Most species have a complex lifecycle that relies on both aquatic (egg laying, tadpole develop-ment) and terrestrial environments (other life history traits). Suchreliance on diverse habitats induces a strong sensitivity to terres-trial and aquatic conditions (Collins and Storfer 2003; Beebeeand Griffiths 2005). Finally, even though amphibian dispersalabilities are often underestimated, they remain limited (e.g., upto 11–13 km for anurans, Smith and Green 2005), thereby reduc-ing amphibians’ capacity to escape locally adverse conditions(Araújo et al. 2006; Lawler et al. 2009).

Communicated by: Oliver Hawlitschek

Electronic supplementary material The online version of this article(https://doi.org/10.1007/s00114-017-1530-0) contains supplementarymaterial, which is available to authorized users.

* François Brischouxfrancois.brischoux@gmail.com

1 Centre d’Etudes Biologiques de Chizé, CEBC UMR 7372CNRS-ULR, 79360 Villiers en Bois, France

2 Réserve Naturelle Nationale de Chérine, Maison de la Nature et de laRéserve, 36290 Saint-Michel-en-Brenne, France

The Science of Nature (2018) 105:5 https://doi.org/10.1007/s00114-017-1530-0

Accordingly, multiple studies have demonstrated fastand strong responses of amphibians to changing climaticconditions (Blaustein et al. 2010). For instance, risingtemperatures have caused modifications in the breedingphenology of several species (Beebee 1995; Gibbs andBreisch 2001; Tryjanowski et al. 2003; Carroll et al.2009; Benard 2015), and droughts have caused severepopulation decreases (Daszak et al. 2005; Rittenhouseet al. 2009; Cayuela et al. 2016a). Modifications ofthe thermal and hydric conditions are also expected toinduce significant shifts in species distribution (Araújoet al. 2006; Lawler et al. 2009). Climate can also syn-ergistically interact with other factors that may impactamphibian populations (Blaustein et al. 2010; Veneskyet al. 2014; Davis et al. 2017; Crump and Houlahan2017).

Nevertheless, the various mechanisms through whichclimate influences amphibians population dynamics, asfor other organisms, are complex and remain to beassessed (Collins and Storfer 2003; Blaustein et al. 2010;Knape and de Valpine 2011; Selwood et al. 2015).Moreover, rainfall and temperature effects on amphibiandynamics can be complex to assess as these climatic pa-rameters may interact synergistically or antagonistically(Amburgey et al. 2017). In Europe, it has been shown thatwarmer temperatures before the breeding period could re-duce adult survival and fecundity, or lower recruitment,because of an increased consumption of nutrient reservesduring overwintering (Bufo bufo: Reading 2007; Trituruscristatus: Griffiths et al. 2010; Bombina variegata: Cayuelaet al. 2017). Conversely, mild winters could enhance therecruitment probability of newly-metamorphosed amphib-ians, because these climatic conditions are associated withincreased food availability and faster growth (Speleomantesstrinatii: Salvidio et al. 2016; Triturus cristatus: Cayuelaet al. 2017). In parallel, pre-reproductive rainfall has beenrelated to increased survival or breeding probability forBombina variegata (Cayuela et al. 2014), and to enhancedcolonization rates (and lowered extinction rates) at breed-ing ponds for several species (Cayuela et al. 2012).Besides the important consequences of extreme events(droughts, floods) that can cause high mortalities or repro-duction failing in several species (Triturus cristatus:Griffiths et al. 2010; Bombina variegata: Cayuela et al.2015a, 2016a), the persistence of climate-induced changesin demographic parameters through years can affect popu-lation growth rates and induce severe population declines,as shown in Europe for Bufo bufo (Reading 2007), orTriturus cristatus (Griffiths et al. 2010; Cayuela et al.2017). Additionally, other factors such as density depen-dence have been shown to strongly influence populationgrowth rates (Hyla arborea, Pellet et al. 2006; Ranadalmatina, Băncilă et al. 2016). Finally, climate effects

on amphibian can be context-dependent, as the organismalresponse may vary according to the species and its lifehistory traits (Cayuela et al. 2017), the population studied(latitudinal, topographical, hydrometric, and climatic con-text (Cayuela et al. 2016b, 2017; Amburgey et al. 2017),and the age of individuals (Cayuela et al. 2016b). In thiscontext, it seems crucial to multiply long-term studies todetect climate-induced changes in populations.

In this study, we analyzed the effects of climate on an agilefrog (Rana dalmatina) population through its influence onreproduction. The European agile frog is a species character-ized by an explosive-breeding behavior, with numerous egg-deposition events condensed during a short period in late win-ter (mid-February to early March, Duguet et al. 2003; Hartelet al. 2007; Hartel 2008). In this species, inter-annual varia-tions in the egg-clutch abundance could be influenced notonly by the survival rate of reproductive frogs, but also bythe probability of breeding. Indeed, when unfavorable condi-tions occur, female frogs can decide to skip reproduction inorder to maximize survival (rainfall deficit or extremedrought: Cayuela et al. 2014, 2016a; warm conditions:Cayuela et al. 2017; food restriction: Gao et al. 2015a). Inaddition, juvenile survival can be a major driver of animalpopulation dynamics (Gaillard et al. 1998), particularly inBfast^ life history species, i.e., species with a short life spanand high fecundity rate (Sæther 1997). This is particularly truein amphibians where juvenile survival can equal or even out-pace the direct influences of fecundity and adult survival(Vonesh and De la Cruz 2002; Conroy and Brook 2003). Inthe studied population of agile frog, which life history wouldbe between the Bmidway^ and the Bfast^ species characteris-tics, reduced breeding could be the consequence of a climate-induced poor recruitment (Cayuela et al. 2017).

We investigated the impact of climate conditions (i.e., rain-fall and temperature) on the abundance of egg-clutches (aproxy of female breeding population size, Meyer et al. 1998;Hartel 2008; Băncilă et al. 2016) for a population of agile frog,over a 29-year monitoring period on 14 breeding sites locatedin the Brenne Natural Park, France. Basing our hypotheses onthe thermal and hydric preference of brown frogs (Köhleret al. 2011) and the geographical and climatic context of ourstudy (woods and wetlands in a temperate climate with oce-anic and continental influences), we predicted that

1. Moist conditions occurring over all periods of the yearpreceding reproduction would positively influence theegg-clutch abundance because of high survival and breed-ing probabilities resulting from lower hydric stress andenhanced activity levels (foraging, migration to ponds)(Chan-McLeod 2003; Rittenhouse et al. 2008; Köhleret al. 2011; Cayuela et al. 2012, 2014);

2. Effects of temperatures on egg-clutch abundance wouldvary in function of the period considered during the year

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preceding reproduction. In this context, we predicted thatmild autumn-winter conditions would positively influ-ence the egg-clutch abundance of the following reproduc-tion event, because of an increased breeding probabilitydue to a longer foraging period allowing to store nutrientreserves (Gao et al. 2015b), and a minimized risk of mor-tality due to freezing (McCaffery and Maxell 2010;Köhler et al. 2011). We also predicted that hot and drysummer conditions would negatively influence the egg-clutch abundance of the following year because of anincreased mortality if lethal or sub-lethal temperature af-fected frogs (i.e., ~ 30 °C, Köhler et al. 2011). Hot condi-tions would also result in increased patterns of energy use(metabolic rates, Dillon et al. 2010) and foraging limita-tion (estivation or hiding) that would lower the probabilityof breeding (i.e., lack of reserves to fuel the oogenesis thatoccurs in summer, Elmberg 1991; Miaud et al. 1999).

3. Delayed effects of climate, particularly of the summerconditions 3 years before a reproduction event, wouldalso influence egg-clutch abundance (at year Y) throughpost-metamorphosed juvenile survival (at year Y-3) andthus recruitment, which is largely affected by the condi-tions of the first summer of froglets (Cayuela et al. 2016a,b). Because of the same biological mechanisms enouncedabove, we predicted that rainfall would positively influ-ence recruitment, and hot and dry summer conditionswould negatively influence recruitment.

We examined the effects of the two main climatic variableson breeding focusing on five temporal windows of the yearcycle. Each of these temporal windows was selected accord-ing to specific influences of climate on biological parametersof the species that should ultimately bear consequences onreproductive biology and thus abundance of egg-clutches, de-posited in February–March in a given year:

1. Overall yearly conditions [April–January]: large-scale in-fluence of climatic conditions on reproductive adults’body condition and thus breeding probability

2. Autumn-winter period [November to January]: specificclimate effects on physiological patterns (energy use, hy-dration) and activity (overwintering, foraging) of repro-ductive adults

3. Month preceding reproduction [January]: specific climateeffects on physiological patterns (energy use, hydration),activity (foraging) and behavioral stimulation (migrationto ponds, breeding behaviors) of reproductive adults

4. Active period [April–October]: specific climate effects onphysiological patterns (lethal thresholds of thermal andhydric conditions) and activity (foraging versus estivat-ing) of reproductive adults

5. First summer of newly metamorphosed frogs [April–October with a 3-year lag]: specific climate effects on

the recruitment rate of reproductive adults, resulting fromclimate influence on physiological patterns (high dehy-dration risk and increased metabolism) and activity (for-aging to complete growth) of newly metamorphosedfrogs, whose first breeding generally occurs at age three(Duguet et al. 2003)

Materials and methods

Study species

The agile frog belongs to the brown frog group (Bartoń andRafiński 2006), which consists of species that are tightlylinked to woodlands, particularly deciduous forests (Duguetet al. 2003). During the late winter, adults migrate towardsaquatic breeding areas where females lay one clutch with ca500–2000 eggs attached to submerged wood or vegetation(Kyriakopoulou-Sklavounou and Sofianidou 1983; Duguetet al. 2003; Bartoń and Rafiński 2006). After breeding, adultsreturn to their terrestrial habitat (Duguet et al. 2003), wherethey perform all their other activities, including foraging andthus reserve storage (liver and fat bodies) for the winter andcompletion of the next breeding cycle (Elmberg 1991; Miaudet al. 1999). Metamorphosis occurs after 3 to 4 months oflarval development (Duguet et al. 2003; Sarasola-Puenteet al. 2011). Newly metamorphosed froglets leave the aquatichabitat and establish in woodlands where they grow and ma-ture. Their first breeding event usually occurs during theirthird winter (Duguet et al. 2003; Sarasola-Puente et al. 2011).

Study area

Study sites are situated in the Réserve Naturelle Nationale deChérine protected area (46° 47′ 17″ N, 1° 11′ 12″ E, 93 m asl,370 ha) within the Brenne Natural Park, one of the largestFrench wetlands, constituted by a network of ponds andmarshes, surrounded by reed-beds, woods, and grasslands(see Online appendix 1). Thirty-two breeding sitesrepresenting the majority of the reserve’s water bodies wereregularly surveyed during the agile frog reproductive seasonbetween 1987 and 2016. Sampling duration of each site variedbetween 4 and 27 years, as several sites were successivelyadded to the monitoring program over the time. Egg-clutchabundances (defined as the number of clutches counted perbreeding site) were monitored once a year, in mid-March aftermost of the adults have left the breeding sites, but beforetadpoles hatched in order to comprehensively assess egg-clutch abundance. Agile frogs lay their conspicuous clutchof eggs in shallow water (< 80 cm deep) and surveys (countsof egg-clutches observed along systematic transects) occurredin such accessible and shallow water areas, thereby

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maximizing the detection probability. In order to further de-crease any influences of detection probability on egg-clutchcounts, monitoring was performed by the same individuals oneach study site throughout the study period. The duration ofsurveys for each site varied according to its surface area ofshallow water, and to the cover of macrophytes (visual inspec-tion of the vegetation).

In order to study long-term trends in the frogs breedingdynamic, only sites surveyed at least for 10 years were select-ed for the analysis. Two very specific sites (lowland woodswith varying winter-flooded areas), as well as six small tem-porary ponds considered as marginal breeding sites (maxi-mum amount of egg-clutches inferior to 20 over the surveyperiod) were excluded from the analysis. This selection pro-cess resulted in an analysis of 14 breeding sites, characterizedin Online appendix 2. Themedian distance between these siteswas 960 m (minimum 46 m; maximum 9890 m, Online ap-pendix 1).

Climatic variables

Meteorological records were obtained from two local stations.The stations were located 3.5 km (at Mézières-en-Brenne fordaily cumulated rainfall, mm) and 11.3 km (at Martizay fordaily minimum and maximum temperatures, °C) from thenatural reserve.We investigated the effects of cumulative rain-fall and means of minimum and maximum temperatures oc-curring during the year before one event of reproduction. Weextracted these parameters for the four time frames concerningthe effects on adult frogs breeding as described in theBIntroduction^ section: annual effect excluding reproductionmonths (April to January), autumn-winter period (Novemberto January), month of January, active period (April toOctober). We also investigated putative delayed effects onegg-clutch abundances by examining the influence of climateon the survival of newly metamorphosed juveniles (June toOctober with a 3-year lag corresponding to the maturity of thisspecies, Duguet et al. 2003; Sarasola-Puente et al. 2011).

Statistical analyses

We made the hypothesis that variations in clutch abundanceobserved at one site were the combination of local influencesspecific to this site (for example micro-changes in habitatsaround the pond) and a shared effect of large (regional) scaledrivers like climatic conditions.

For each of the 14 sites, we modeled the local breedingdynamic by analyzing the abundance of egg-clutches as afunction of year (see Online appendix 3 for examples). Wemade no a priori assumptions about the form of the rela-tionships between egg-clutch abundance and year. We usedgeneralized additive models (GAM {mgcv} R package, seeWood 2006; Zuur et al. 2009) to explore the shape of the

relationships (see Online appendix 3). After a visual exam-ination of the site-specific patterns, we fixed an identicalsmoothing parameter (k = 5) for all the sites. This allowedthe smoothing to be homogeneous between the sites, andthe residuals to have the same range of variation (Onlineappendix 3).

The standardized residuals of the 14 breeding siteswere clustered to analyze the breeding dynamics at aregional scale. Because some sites displayed very highnumbers of clutches (up to ~ 600, see Online appendices2 and 3) while others had lower abundances (less than50, see Online appendices 2 and 3), the standardizationof residuals allowed to control for the site-specific clutchnumber by homogenizing abundances and their varianceacross all studied sites. These standardized residuals rep-resent the positive or negative deviations of egg-clutchabundance to the GAM models predicted dynamics.Years with a positive residual average were defined asfavorable for breeding, whereas years with a negativeresidual average were defined as unfavorable for breed-ing, independently from the site-specific absolute abun-dances. An analysis of variance (ANOVA) using the yearas a factor was used to test if inter-annual fluctuations ofthe residuals of egg-clutch abundance occurred. The ex-istence of a trend in the residuals of clutch abundanceover time was tested using a linear model (with the yearas a continuous variable).

In order to analyze climatic influences, Pearson correla-tion tests were used to check for correlations between cli-matic variables within each of the five time frames. Wefound a strong correlation between precipitations, maxi-mum temperatures, and minimum temperatures for mostof the time frame we studied (average correlation factor[absolute value] between minimum temperatures and rain-fall, 0.50; maximum temperatures and rainfall, 0.29; min-imum temperatures and maximum temperatures, 0.54; de-tailed results in Online appendix 4). Therefore, we testedthe influences of these climatic variables independently.Then, the standardized yearly residuals from all sites (onevalue of standardized residual per site and per year) weremodeled against the climatic variables. A total of 15 linearmodels were produced (three climatic variables tested onfive temporal windows).

To take into account the multiple testing issue, we chose touse a Bonferroni correction (Zuur et al. 2007) that brought thesignificance threshold down to p = 0.0033. Additionally, weinspected for presence of residual outliers, independence, andhomogenized variance conditions following the recommenda-tions of Zuur et al. (2007). Specifically, we examined thedistribution of residuals. If an outlier was detected, we testedits influence by removing it from the model. Since no signif-icance change was observed during this procedure, only thefull models are presented.

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All data analyses were conducted with the R 3.3.0 software(R Core Team 2014).

Results

The number of sites under survey per year varied between 0and 14 (Fig. 1). Over the 29 years of monitoring, 240 events ofcounts on the studied sites resulted on a total of 14,318 egg-clutches counted. Counts of egg-clutches varied between 0and 658 according to sites and years, with an average yearlynumber of clutches per site of 60. The GAM analysishighlighted strongly fluctuating breeding dynamics, with acoefficient of variation of egg-clutches abundance rangingfrom 51 to 142% according to the site (Online appendix 3).For example, the abundance of egg-clutches could show eitherstable, decreasing or increasing phases or a combination there-of (Online appendix 3).

We found a significant effect of the year on the residuals ofabundance of egg-clutches for the 14 study sites (ANOVAwith year as factor, F28,211 = 3.18, p < 0.001, Fig. 1).However, no clear negative or positive trend was detectedacross the study period (linear model df = 238, t = 0.068,p = 0.946, Fig. 1).

Among the 15 tested models, 7 showed a significant influ-ence of climatic conditions on egg-clutch abundances after theBonferroni correction (Table 1). Annual, autumn-winter, andJanuary cumulative rainfall influenced positively the abun-dance residuals (Table 1, Fig. 2). Similar effects were foundfor these three periods for minimum temperatures (Table 1,Fig. 3). Maximum temperatures during the autumn-winter pe-riod positively influenced the relative number of clutches(Table 1, Fig. 3).

Discussion

From site-specific to regional fluctuationsof egg-clutch abundance

Our study is characterized by a remarkably long survey period(29 years) and a relatively high number of sites monitored(14). This allowed to robustly identifying various site-specific breeding dynamics (Online appendix 3). Most of thesites showed highly fluctuating patterns typical of explosive-breeders, as observed in other brown frog species (Meyer et al.1998; Duguet et al. 2003; Green 2003; Hartel et al. 2007;Hartel 2008). We do not believe that strong biases in egg-clutch detection were responsible for these very strong varia-tions as the method we use relied on a systematic count ofconspicuous egg-clutches in the shallow water area of eachsite (i.e., < 80 cm deep) by the same individuals, which shouldallow for a high probability of egg-clutch detection (> 90%,Grant et al. 2005). However, future prospection methodsshould valuably implement multiple counts per sites in orderto quantify a putative detection bias (Mazerolle et al. 2007). Inaddition, performing multiple count sessions distributed overthe breeding season would usefully reduce the count bias andallow including variation of phenology in future studies.

Some study sites were situated in close proximity: 11% ofthe inter-pond distances were inferior to 300 m, which hasbeen measured as the adult agile frog’s dispersion capacity(Ponsero and Joly, 1998). As highlighted by Petranka et al.(2004), the geographical context could influence the site-specific dynamics via the behavioral switching of reproduc-tive adults from one pond to another. Although we acknowl-edge this potential bias, we do not believe that such processcould be responsible for the remarkably wide demographicvariations we observed in the studied sites (Online appendix3), especially since most of the dispersion in amphibians oc-curs during the juvenile life stage (Smith and Green 2005;Pittman et al. 2014). Finally, site-specific dynamics could alsoresult from topographical (water levels variations, digging op-erations) or biotic changes (vegetation variations, presence ofpredator) at a local scale (Van Buskirk 2005; Hartel et al.2011; Cayuela et al. 2012). Because of the lack of detailedinformation on such changes across the time-scale of ourstudy, we remained cautious with the interpretation of thesesite-specific fluctuations.

Our analysis of standardized abundance residuals allowedto identify deviations from site-specific predicted dynamicsand to determine the presence of inter-annual fluctuations atthe regional scale. Although, we did not detect any long-termlinear trend (either decline or increase) in the abundance ofegg-clutches, the overall climatic conditions during the yearpreceding reproduction influenced clutch abundance. Thepositive effects of yearly rainfall and minimum temperatureon egg-clutch abundance support the fact that generally moist

Year1990 1995 2000 2005 2010 2015

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Fig. 1 Yearly fluctuations of egg-clutch abundance (standardized resid-uals) on the 14 sites across the 29 years of monitoring. Standardizedresiduals are presented as mean ± SD. Numbers above the error bars in-dicate number of site monitored per year

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and mild conditions would be favorable to agile frogs (Köhleret al. 2011), maximizing their survival and breeding probabil-ity. Moreover, climatic conditions influenced clutch abun-dance during specific critical periods of the life cyclediscussed below.

Effect of autumn-winter conditions on breeding

We detected significant effects of climatic conditions on egg-clutch abundance during the autumn-winter period for whichthe three climatic variables analyzed (precipitation, minimumand maximum temperature) positively influenced egg-clutchabundances. Other studies have demonstrated the positive im-pact of autumn-winter rainfall on egg-clutches (Jensen et al.2003; Hartel 2008) or adult (Salvidio et al. 2016) abundances,frogs’ fecundity and survival (Cayuela et al. 2014; Benard2015), or colonization rate of ponds for breeding (Cayuelaet al. 2012). It is well admitted that high level of humiditywould decrease desiccation risks during overwintering andmigration, and would also positively influence mobility forthe breeding migration (Chan-McLeod 2003; Rittenhouseet al. 2008; Köhler et al. 2011).

Although some studies, as the present study, found evi-dence for positive autumn-winter temperature effect on egg-clutch abundance (Amburgey et al. 2017) or adult abundance(Salvidio et al. 2016), others showed opposite results(Reading 2007; Griffiths et al. 2010; Benard 2015). Severalstudies in temperate environment have emphasized that ele-vated temperature during winter would increase the pattern ofenergy use (metabolic rates, Dillon et al. 2010) of adult fe-males, thereby negatively influencing their survival and

breeding probability (Reading and Clarke 1995; Reading2007; Griffiths et al. 2010; Benard 2015). However, ovariancycle completion (vitellogenic growth) in a sister species(Rana temporaria) occurs during the preceding summer(Elmberg 1991; Miaud et al. 1999), and thus, it should berelatively independent of winter conditions. It is noteworthythat in harsh conditions, females may also be able to modulatetheir annual breeding investment through egg resorption dur-ing the overwintering period (Jørgensen 1984), which couldinfluence egg-clutch abundances.

According to our results, we suggest that in temperate envi-ronments, mild autumn-winter conditions could allow frogs toforage and accumulate nutrient reserves (i.e., reducedoverwintering period, Gao et al. 2015b). In a mesocosm envi-ronment where temperature and food availability werecontrolled, Gao et al. (2015a) showed that the feeding ratewas the major predictor of reproductive status and body sizeof pond frogs (Pelophylax nigromaculatus), which were notimpacted by warmer temperatures. Other studies found thatbody condition of adult toads mainly depended on density,probably through food resource competition, and was not (oronlymarginally) influenced by temperature variations (Readingand Clarke 1995; Green and Middleton 2013). In addition, wesuggest that, in temperate environments, mild autumn-winterconditions could positively influence the activity and the abun-dance of the prey of agile frogs (small invertebrates, Cameron1970; Honek 1997). As a consequence, we can then expect thatmild autumn-winter conditions would appear as opportunitiesfor frogs to forage and store more reserves, leading to enhancedbody condition of reproductive individuals after overwinteringand thus to an increased probability of breeding.

Table 1 Results of the linear models of the standardized abundance residuals explained by the climate variables during the studied periods. Italicindicates significant models at p = 0.05; *Significant models using the Bonferroni correction (p = 0.0033). BJuvenile growth^ corresponds to delayedeffects with a 3-year lag. See text for details

Variable Period df β t p R2

Rainfall Active period 238 0.002 2.706 0.0073 0.03

Juvenile growth 238 0.001 0.675 0.500 < 0.01

January 224 0.012 5.783 < 0.0001* 0.13

Autumn-winter 224 0.004 3.71 0.0003* 0.06

Annual 224 0.002 3.598 0.0004* 0.05

Minimum temperature Active period 238 0.215 2.037 0.0427 0.02

Juvenile growth 238 − 0.103 − 1.33 0.185 0.01

January 224 0.109 3.432 0.0007* 0.05

Autumn-winter 224 0.276 5.238 < 0.0001* 0.11

Annual 224 0.417 4.13 < 0.0001* 0.07

Maximum temperature Active period 238 − 0.114 − 1.681 0.0940 0.01

Juvenile growth 238 − 0.142 − 2.32 0.0212 0.02

January 224 0.086 2.716 0.0071 0.03

Autumn-winter 224 0.199 3.955 0.0001* 0.07

Annual 224 0.121 1.369 0.173 0.01

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Our results suggest that abundant rainfall associated withmild temperatures in autumn and winter would induce highsurvival and breeding probabilities among reproductive frogs,leading to an increase of egg-clutch abundance. Together withthe general impact of climatic conditions on frogs during theautumn-winter period, the positive effects of rainfall and min-imum temperatures in January on egg-clutch abundance thatwe detected highlight the importance of climatic conditionsduring the weeks preceding breeding (Reading and Clarke1995). The seasonal start of temperature rising at the end ofthe winter (end of January–early February) as well as theincreasing photoperiod (Canavero and Arim 2009) could in-duce a behavioral stimulation such as the end of overwintering(Gao et al. 2015b), the migration to ponds, and the start ofbreeding behaviors (e.g., calls, Gibbs and Breisch 2001).

Effect of active period conditions on breeding

We did not detect any influence of precipitation and tempera-ture of the active period preceding reproduction on the egg-clutch abundance, after Bonferroni correction. While onestudy has reported evidence for impacts of climate duringfrogs’ active season (temperature and precipitation) on theamount of clutches deposited the next year (Amburgey et al.2017), others have not (Meyer et al. 1998; Hartel 2008). Webelieve that several hypotheses can explain this lack ofclearcut influences of the active period conditions on the sub-sequent reproduction of agile frogs. First, the terrestrial habitatof the frog (forested areas), as well as the micro-habitats with-in, may retain significant moisture and coolness and signifi-cantly buffer deleterious hot and dry summer conditions(Chen et al. 1993; Rittenhouse et al. 2008). Second, somespecies of frog can estivate to evade unfavorable conditions(Storey 2002), although this behavior has yet to be reportedfor Rana dalmatina. Finally, environmental conditions in ourstudy area may not reach the physiological tolerance thresholdof agile frogs (23–30 °C, Köhler et al. 2011).

Delayed effects on breeding

We did not detect any delayed influence of climate on egg-clutch abundances as expected from the importance of envi-ronmental conditions on metamorphic froglets that are highlysensitive to dehydration (Rittenhouse et al. 2008; Cayuelaet al. 2016a).

Previous studies found contradictory results concerning de-layed effects of rainfall on population growth rate (Pellet et al.2006; Amburgey et al. 2017), or failed to detect influence ofclimatic conditions on the following reproduction events (2-,3-, and 4-year lag on Rana temporaria, Meyer et al. 1998),and this may be due to several reasons. First, juvenile strate-gies, including movements and micro-habitat selection couldallow froglets to maximize their survival through dispersalwhen harsh conditions occur (Cushman 2006, Cayuela et al.2016c). Second, local recruitment may be influenced not onlyby juvenile survival but also by juvenile dispersal as this is theperiod during which amphibians colonize new habitats (Smithand Green 2005; Cushman 2006; Pittman et al. 2014).Recruitment could also be impacted by a density-dependentmechanism, such as competition for food in the larval or ter-restrial stages of immature frogs (Vonesh and De la Cruz2002; Altwegg 2003; Harper and Semlitsch 2007). For in-stance, delayed density-dependence (2-year lag) effects onpopulation growth rate were lower than direct density depen-dence for agile frogs (Băncilă et al. 2016). Third, the age offirst reproduction may vary among individuals and popula-tions (Augert and Joly 1993; Miaud et al. 1999; Sarasola-Puente et al. 2011), and such variability would obscure anyinfluence of the survival of juveniles during their first summer

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Fig. 2 Linear models of abundance residuals according to rainfall dataduring the activity period (a), the autumn-winter period (b), and themonth of January (c). Each symbol corresponds to one count, i.e., tothe abundance residual of one site and one rainfall value (summed upfor the time frame under focus) for each year. The total number of counts(n) is 240

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on egg-clutch abundances. Similarly, reproductive adults mayconsist of a combination of numerous cohorts as the life spanofRana dalmatina can reach up to 6 years (Duguet et al. 2003;Sarasola-Puente et al. 2011). This would inevitably dilute theinfluence of juvenile survival during a specific season. Finally,some individuals can skip reproduction if poor conditionshave negatively influenced their body conditions (Cayuelaet al. 2014, 2016a, 2017; Gao et al. 2015a), and such phenom-enon may contribute to the variability of the number of breed-ing adults each year.

Other factors affecting breeding

In our study, climatic variables explained a modest proportionof the variation of the abundance residuals (from 5 to 13%,Table 1). Climate effects on animal time series are generallydifficult to detect, and often show aweak explained proportionof time series variation because of the complexity of the bio-logical mechanisms they affect (Knape and de Valpine 2011).

Hence, we emphasize that even a low effect of climate asfound in our time series is important to consider. Clearly, otherfactors known to affect amphibian population dynamics couldhave influenced the studied population of agile frog and theseare discussed below.

In pond-breeding amphibians, wide population fluctuationsare common and are thought to result from metapopulationdynamics and stochasticity (Green 2003; Griffiths et al. 2010;Cayuela et al. 2012, 2015b). Amphibian spatially structuredpopulations usually display higher turn-over rates of breedingpatches (Green 2003; Petranka et al. 2004). Frequent extinc-tions in breeding patches occur due to a high environmentalstochasticity (Green 2003; Cayuela et al. 2012, 2015b) andfrequent re-colonization events occur through dispersal(Smith and Green 2005; Cayuela et al. 2016c). Indeed, someauthors emphasize that these meta-population dynamics arehighly sensitive to habitat fragmentation which creates dis-persal barriers (Green 2003; Cushman 2006). Moreover, thelife strategy adopted by an amphibian population (dispersal

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Fig. 3 Linear models ofabundance residuals according tominimum temperature dataduring the activity period (a), theautumn-winter period (b), and themonth of January (c), and tomaximum temperature data dur-ing the activity period (d), theautumn-winter period (e), and themonth of January (f). Each sym-bol corresponds to one count, i.e.,to the abundance residual of onesite and one temperature value(averaged for the time frame un-der focus) for each year. The totalnumber of counts (n) is 240

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rate, fecundity and survival probability), and thus the subse-quent demographic dynamics, has been shown to vary accord-ing to the environmental stochasticity level that the populationexperiences (Cayuela et al. 2015b, 2016c). As a consequence,higher levels of environmental stochasticity associated to in-creased habitat loss could be an important driver of amphibianpopulations’ declines in the near future.

Biotic interaction factors are also likely to contribute toamphibian demographic fluctuations, acting on the terrestrialor on the aquatic stages of the complex life cycle of agilefrogs. For instance, density dependence is known to influenceamphibian population dynamics (Meyer et al. 1998; Pelletet al. 2006; Hartel 2008; Băncilă et al. 2016), especiallythrough parameters such as competition for resources andmicro-habitats affecting juvenile and/or adult body conditionor survival (Reading and Clarke 1995; Vonesh and De la Cruz2002; Altwegg 2003; Harper and Semlitsch 2007; Green andMiddleton 2013). Actually, the influence of density depen-dence may even exceed effects driven by climatic conditions(Pellet et al. 2006; Green and Middleton 2013; Băncilă et al.2016). In addition, interactions with other species (disease,predation, competition) can also strongly influence frog spe-cies population fluctuations (Meyer et al. 1998; Kieseckeret al. 2001; Cruz et al. 2008; Venesky et al. 2014, seereviewed examples in Collins and Storfer 2003; Beebee andGriffiths 2005). Moreover, these interactions are likely to bemediated by climate, such as predator-prey interactions (Daviset al. 2017; Crump and Houlahan 2017), or Chytridomycosiswhich seems to be dependent, at least in part, on climaticconditions (Venesky et al. 2014). There is currently no infor-mation on the status of Chytridomycosis in Brenne NaturalPark, and this factor will require specific attention in the nearfuture. Finally, the Natural Reserve of Chérine undergoes analien crayfish (Red Swamp crayfish, Procambarus clarkii)colonization, which started in 2010 and is progressing fast.This species is known to impact the amphibian larval stages(Cruz et al. 2008) and could lead to negative consequences onthe studied population of agile frog.

Conclusion

Overall, our result suggests that the year-to-year fluctua-tions of egg-clutch abundances in the Brenne Natural Parkare partly dependent on local climatic conditions (rainfalland temperature). Climate seems to influence breedingfrogs especially during the autumn and winter precedingbreeding. It is noteworthy that an important part of thesefluctuations remains unexplained, and several factors thatcan influence the reproduction of temperate frogs remain tobe identified in order to comprehensively understand thepopulation dynamics of amphibians.

Acknowledgments We warmly thank the staff from the RéserveNaturelle Nationale de Chérine, and especially Laura Beau, CécileDanel, Joël Deberge, Christian Laverdan Godin, Julien Vèque, andRémy Vioux for their crucial help during counts of egg-clutches.Alexandre Boissinot provided information on the natural history of agilefrogs. Three anonymous reviewers provided constructive and insightfulcomments during the revision process.

Funding information Funding was provided by the CNRS and theMinistère en charge de l’environnement.

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