Amphibia-Reptilia 41 (2020): 63-74 brill.com/amre

Body size and life history traits of the fire salamander Salamandra salamandra from Poland

Anna Najbar1,∗, Agnieszka Konowalik1, Konrad Halupka2, Bartłomiej Najbar3, Maria Ogielska1

Abstract. The fire salamander Salamandra salamandra is a widespread taxon in Europe, exhibiting great intraspecific diversity in phenotype and life history traits across its geographical distribution. Here, we studied body size, sexual dimorphism, age, growth rate and condition of fire salamanders from the north-eastern margin of its range. In total, 2,102 individuals from 23 populations representing the Polish parts of the Sudetes and the Carpathian Mountains were sampled between 2004 and 2016. Body traits and age showed significant differences between the western (the Sudetes) and eastern (the Carpathians) groups of populations. Salamanders from the Carpathians tended to be longer, heavier and older. Female-biased sexual size dimorphism was found only in the Carpathians. Body condition at the beginning of the season was poor, then increased to reach a peak in early June, and deteriorated toward the end of the season. Age estimated by skeletochronology on phalangeal bones ranged from 2 to 16 years in both females and males, with the highest share of 7- to 9-year-old individuals. Age of juveniles ranged from 1 to 5 years in the Sudetes and from 1 to 4 years in the Carpathians. Growth curves (fitted using von Bertalanffy’s model) were asymptotic throughout the individual lifespans, but exhibited differences between sexes and mountain ranges. Altitude did not explain differences in characteristics of populations living in the two mountain ranges, but these differences most probably resulted from habitat quality (better in the Carpathians) and adverse human impact (higher in the Sudetes).

Keywords: Amphibia, Caudata, longevity, population structure, Salamandra salamandra, sexual dimorphism, skeletochrono- logy.

Introduction stages, reach sexual maturity later, and have longer lifespan (reviewed in Morrison and Hero, Adaptations to local habitats in ectotherms are 2003). Such trends were documented in Bufo often manifested as differences in phenotypic bufo (Hemelaar, 1988), Salamandra lanzai (Mi- and life history traits (Hastings, 1997; Sin- aud et al., 2001) or Ichthyosaura (former Trit- sch et al., 2007; Merilä and Hendry, 2014; urus) alpestris (Miaud, Guyetant and Faber, Trochet et al., 2014). Such heterogeneity can 2000). A similar variation in morphometric and be observed between populations of the same life history traits is observed within geograph- species within geographical ranges and altitudes (Berven, 1982; Hemelaar, 1988; Olgun, Miaud ical ranges (Hemelaar, 1988; Davenport and and Gautier, 2001; Cogalniceanu˘ and Miaud, Hossack, 2016) or along environmental gradi- 2003; Amat et al., 2015). ents of human disturbance (Cogalniceanu˘ and Amphibians that inhabit higher altitudes dif- Miaud, 2003; Sinsch et al., 2007). On the level fer considerably from those living in lowlands: of proximate mechanisms, differences in body they attain larger body sizes in larval and adult size and life history may be explained by mi- croclimate, trophic conditions, length of the sea- son, or population density, including numbers 1 - Department of Evolutionary Biology and Conservation of larvae (Fraser, 1976; Scott, 1994; Miaud, of Vertebrates, University of Wrocław, Sienkiewicza 21, 50-335 Wrocław, Poland Guyétant and Faber, 2000; Miaud et al., 2001; 2 - Department of Behavioural Ecology, University of Krauze, Steinfartz and Caspers, 2011; Reinhard, Wrocław, Sienkiewicza 21, 50-335 Wrocław, Poland Renner and Kupfer, 2015; Liao et al., 2016). 3 - Faculty of Biological Sciences, University of Zielona The north-eastern margin of range of our Góra, Prof. Z. Szafrana 1, 65-516 Zielona Góra, Poland ∗Corresponding author; study organism, the nominative subspecies S. e-mail: [email protected] salamandra salamandra, covers the Sudetes Downloaded from Brill.com09/29/2021 06:09:10PM via free access © Koninklijke Brill NV, Leiden, 2019. DOI:10.1163/15685381-20191135 64 A. Najbar et al. and the Carpathian Mountains. Both mountain Body size and sex determination ranges are separated by a wide depression, the Total body length was defined as the distance from the tip Moravian Gate, where the fire salamander does of the snout to the posterior tip of the tail. Body mass was not occur. The species was recorded at a wide weighted using 10 g and 60 g PESOLA (populations 2–15) range of altitudes, usually between 300 and and ProScale LCS100 scales (populations 1, 16–23) with an accuracy of up to 0.1 g. Sex of adult individuals was deter- 1,000 m a.s.l. (Zakrzewski, 2007; Głowacinski,´ mined by the shape of the cloaca. In females, cloacal lips Ogrodowczyk-Konowalik and Ogielska, 2018), are poorly developed and flattened, while in males cloaca is rarely up to 1,200 m (Swierad,´ 2003). Fire well developed, large, convex, and cloacal lips form a parted gap (Juszczyk, 1987; Zakrzewski, 2007). Individuals with- salamanders have strict habitat preferences and out developed external sexual characteristics were classified are philopatric to their watersheds (Zakrzewski, as juveniles. 2007), therefore they are particularly vulnera- ble to adverse human impact (e.g. Lorenço et Skeletochronological procedures and age estimation al., 2017). The species is declining due to habi- In total, 1,140 individuals (801 from the Sudetes, and 339 tat loss and fragmentation, pollution of water from the Carpathians) were analysed, and the sample size in and infectious diseases (e.g. Schmidt, Feldmann each population varied from 7 to 76 individuals. We applied standard skeletochronological procedures described by Cas- and Schaub, 2005; Bosch and Martínez-Solano, tanet and Smirina (1990), Smirina (1994) and modified by 2006; Spitzen-van der Sluijs et al., 2016; Na- Rozenblut and Ogielska (2005). For age analysis, the forth jbar, Rusek and Najbar, 2017). In sum, we can digit of the right hind limb was amputated using microsurgi- cal scissors, sterilized every time before use. Wounds were expect that a large diversity of environmental disinfected with 4% aqueous solution of potassium perman- factors combined with natural selection could ganate. Fingers were preserved in 70% or 96% ethanol. create a high variation in morphometry and life Bones were cleaned from soft tissues manually with tweez- history traits of fire salamanders (cf. Miaud et ers and stored in 70% ethanol until use. Depending on size and thickness, bones were decalcified by immersion in 1:1 al., 2001). mixture of 10% formic acid and 4% formaldehyde for 0.5– Here we study geographical variation in body 3.5 hours depending on their size (Rozenblut and Ogiel- size, sexual dimorphism, body condition, age ska, 2005). Next, the bones were washed in distilled water four times for approximately 15 minutes each and stored structure and growth rate of salamanders along in 70% ethanol before further procedures. After air drying the 550-km longitudinal transect across the from ethanol, the bones were embedded in tissue freezing Sudetes and the Carpathians. medium (Leica Biosystems Nussloch GmbH, Germany) and placed in −24°C. The bones were cross-sectioned into 10 or 12 μm thick sections on a freezing microtome Leica CM 1850 UV (Leica Biosystems Nussloch GmbH, Germany), in Materials and methods temperature of approximately −23°C. Cross-sections of bones were stained with aqueous so- Study sites and sampling lution of 0.05% cresyl violet (Sigma) dropped directly on The study area represents the north-eastern margin of the the slide for about 5 minutes and covered with cover glass S. salamandra range and includes two main mountain (Menzel-Gläser, Thermo Scientific). After staining, the so- ranges: the Western, Central and Eastern Sudetes (16 popu- lution was drained on a paper towel. Age was estimated by lations), and the Outer Western and Outer Eastern Carpathi- counting the number of lines of arrested growth (LAGs) re- ans (7 populations). Samples were collected in the years flecting the number of experienced hibernations (1 hiber- = = 2004–2009 (14 populations), 2014–2016 (2 populations) nation 1LAG 1 year of life). LAGs were separated by from the Sudetes, and in 2014–2016 from the Carpathians rings of annual bone growth deposited during active seasons (7 populations). In total, 2,102 individuals were sampled (supplementary fig. S1A–E). For unreadable cross-sections from 23 sites across the entire species distribution in Poland of the periosteal bone, the age was estimated by additional (for details see table 1 and fig. 1). All populations (excluding counting of LAGs in the endosteal bone (total number of population 1) were previously the subject of genetic analy- LAGs minus 1). As we assumed the lack of total resorp- sis based on variation of microsatellite DNA (Najbar et al., tion of the first (the oldest) LAG documented by Alcobendas 2015; Konowalik et al., 2016). In each sampling site, tran- and Castanet (2000) and Miaud et al. (2001), we did not ap- sect was established along a breeding stream and individuals ply the “back calculation” step (Smirina, 1994). LAGs were were collected in the buffer zone of min. 50 m up to 100 m counted under light microscopes Eclipse 80i (Nikon), Ax- wide on both sides. No animal was killed, and all were re- iostar Plus and Axioskop 20 (Carl Zeiss). Photographs of leased to their natural habitats right after the measurement the selected cross-sections were taken using Axio Cam HRc and finger sampling procedures. (Carl Zeiss). Downloaded from Brill.com09/29/2021 06:09:10PM via free access Life history traits of Salamandra salamandra from Poland 65 E E E E E E E E E E E E E E E E E E E E E E E                        46.1 40.2 35.2 24.4 39.8 53.6 20.0 47.3 33.4 48.9 25.9 47.1 11.5 49.4 47.2 54.9 21.5 31.6 06.5 20.8 08.1 58.7 14.3                        N, 14°54 N, 15°33 N, 15°56 N, 15°59 N, 16°02 N, 15°32 N, 16°19 N, 16°40 N, 16°42 N, 16°40 N, 16°43 N, 16°42 N, 16°44 N, 16°45 N, 16°51 N, 17°24 N, 19°05 N, 20°55 N, 21°21 N, 21°50 N, 21°41 N, 21°47 N, 22°34                        05.3 32.7 23.3 24.3 05.8 36.6 49.2 25.1 53.3 41.9 29.9 57.4 11.5 03.3 11.5 33.5 37.9 48.9 15.4 45.2 41.0 10.1 40.5                        ˙ znik Landscape Park Sudetes 496 50°26 ˙ znik Landscape Park Sudetes 372 50°30 ´ Snie ´ Snie ˙ za Landscape Park Sudetes 263 50°52 e ´ Sl˛ in its entire known distribution range in Poland. Coordinates were designated in Google Earth 7.1.5.1557 (Google ˙ zkowice Piedmont, Liwocz Nature Reserve Carpathians 378 49°49 e ˙ zów Piedmont Carpathians 326 49°54 ˙ znik Massif, ˙ za Massif, ˙ znów Piedmont Carpathians 351 49°54 e ´ ´ Sl˛ Snie ´ nska the Ci˛ Salamandra salamandra ´ sna Ro ebowina Bardzkie Mountains Sudetes 418 50°28 Years of samples collection Locality Orographic and conservation units Mountain range Altitude Coordinates Sampling sites of the fire salamander 234 2008–20095 2008–20096 2008–20097 2005–2006, 2008–20098 2008–20099 2008–2009 Lipa Górzyniec 2004–2005 Janowice 2008–2009 Wielkie Katzbach Muchów Mts., Rudawy Janowickie Mts. Izera Mountains Glinica Kaczawskie Piedmont, Chełmy Landscape Park Darnków Kaczawskie Piedmont Sady Cisy Wałbrzyskie Mountains Stołowe Mountains, Stołowe Mountains National Park Sudetes Sudetes Bardzkie Mountains, Cisy and Cisowa Mountain Nature Reserves Sudetes Sudetes 494 394 50°53 50°59 589 407 50°26 50°31 Sudetes Sudetes Sudetes 470 392 50°51 51°00 509 50°51 1 2015–2016 Bogatynia Eastern Upper Lusatia Sudetes 283 50°58 101112 2006–200713 2008–200914 2008–200915 2008–200916 2007–200917 2007–200818 Boguszyn 2014–201519 Opolnica 2015–201620 D˛ 2014, 201621 Bardo 2014–2016 Bardzkie Mountains22 Janowiec 2014–2015 Bardzkie23 Mountains Złoty 2014, Stok 2016 Jarnołtówek 2014–2015 Bielsko-Biała 2016 Bardzkie Mountains Ple Golden Mountains, Opawskie Mountains Góra Bielsko-Biała Kami city, Silesian Piedmont Rakówka Trzciana Czarnorzeki Strzy Lower Beskids Lower Beskids Otryt Sudetes Carpathians Bieszczady Mountains Sudetes 394 356 Sudetes 49°48 Sudetes 279 50°27 50°30 294 401 50°30 50°16 Carpathians Carpathians 440 Carpathians 417 49°45 49°30 615 49°14 Inc., 2005). Table 1. Site number Downloaded from Brill.com09/29/2021 06:09:10PM via free access 66 A. Najbar et al.

Figure 1. Distribution of the fire salamander Salamandra salamandra in Poland (according to Głowacinski,´ Ogrodowczyk- Konowalik and Ogielska, 2018), and sampling sites in the Sudetes (left, populations 1–16) and the Carpathians (right, populations 17–23).

Body condition ver. 3.2.2 (R Development Core Team, 2015), using the library ‘lme4’ (Bates et al., 2014). Body condition was estimated only for sexually mature All variables, except age, were log-transformed, and males (N = 768). Females were excluded from this anal- we applied models with Gaussian errors and an identity ysis, as their body masses during and between reproduc- link function. Considering that salamanders were collected tive periods fluctuate considerably (Najbar A., Konowalik across 12 years (2004–2016), within the whole vegetation A., unpublished). We used the scaled mass index (SMI) seasons (March–September) in 20–23 (depending on the re- method, which was introduced by Peig and Green (2009). sponse variable) local sites, we controlled for random vari- Combining data on body mass of a given individual i (Mi ) ation due to the data acquisition scheme. Thus, to examine and linear body measurements (Li ; we used total body the variation in body length, mass and age, we fitted random lengths), the method calculates scaled mass index (SMIi ), intercepts for the year, season advancement (expressed as that is, body mass of the given individual predicted when its Julian date with the start of the season as 1 March) and site length is standardized to L0 (here the mean body length as (coded as a nominal variable). The fixed explanatory vari- log-transformed data). The algorithm involves three steps: ables included the altitude (in meters a.s.l.), mountain range (i) exclusion of outliers, i.e. individuals with body masses (the Sudetes and the Carpathians, coded as a dummy vari- unusually low or high in comparison to their lengths (we able), sex (female v. male, coded as a dummy variable), and identified on a scatterplot and excluded 6 males), (ii) cal- an interaction between the mountain range and sex. In the culation of the slope (B) of linear regression of log(Mi ) on model for body condition (SMI described above) of male log(Li ), using the reduced major axis method and (iii) cal- salamanders, we fitted random intercepts for the year and culation of SMIi for all individuals (including those ex- site, whereas the season advancement and its quadratic term cluded in the first step) according to the formula: were treated as fixed variables, together with the altitude and mountain range. B SMIi = Mi (L0/Li ) . We visually checked residual plots of the GLMMs to control if the homoscedasticity and normality assumptions In our sample of salamanders, B and L0 equalled, respec- were satisfied. P -values for fixed variables, including in- tively, 2.682 and 2.679 (i.e. log-transformed average body teractions, were calculated using log likelihood-ratio tests length of 14.57 cm). comparing the full model against the model without the tested variable (table 3). Statistical analysis Growth curves were constructed following von Berta- lanffy’s model (1938), which predicts the length (L)ofan Body variables (total body length, body mass and condition individual as a function of its age (t). The equation, refor- expressed as SMI) and age were examined in general linear mulated by Cailliet et al. (2006), has three parameters: A, mixed models (GLMM) developed with the R software, which is the asymptotic length (or, in other words, the mean Downloaded from Brill.com09/29/2021 06:09:10PM via free access Life history traits of Salamandra salamandra from Poland 67 maximal length of individuals); K, which is the growth pa- rameter; and t0, which lacks a straightforward biological interpretation and is regarded as a modelling artefact. The model:    L(t) = A 1 − exp −K(t − t0) was fitted to the data on body length and age of individu- als, using the least squares method and bootstrapped (1,000 iterations) in order to get confidence intervals around pa- rameter estimates (we used a custom-written Python script). Growth curves were considered significantly different at the α = 0.05 level, when 95% confidence intervals around their parameters did not overlap (see Miaud et al., 2001 and ref- erences cited therein).

Results

Body size and condition

Total body length in immature individuals var- ied from 4.0 to 14.5 cm, with an average of 8.96, coefficient of variation of 0.237 (N = 227). Their body mass ranged between 0.5 and 16.5 g (mean 5.67 g, CV = 0.549, N = 225). In fe- males, length ranged from 9.4 to 20.5 cm (mean 14.85 cm, CV = 0.143, N = 786) and mass var- ied from 5.3 to 51.7 g (mean 20.88 g, CV = 0.395, N = 902). Length of males varied from 9.7 to 21.0 cm (mean 14.7 cm, CV = 0.129, N = 774), and their mass ranged from 5.5 to 42.7 g (mean 17.68 g, CV = 0.345, N = 859). Distri- butions of body length and mass in both sexes, populations and mountain ranges are presented in fig. 2, table 2 and supplementary table S1. Body condition of 738 adult males, calculated as SMI (body mass predicted for standardized Figure 2. Medians, quartiles and ranges of distributions body length) varied from 5.06 to 38.44 (CV = of log-transformed body masses, body lengths and age of adult female and male fire salamanders in Sudetes and the 0.187) and the mean value was 17.5 (95% c.l.: Carpathian Mountains. Individuals which deviated more 17.26-17.73). than 1.5 times interquartile range from respective median GLMMs explaining the variation in body values were marked as outliers. The lowest panel demon- strates seasonal changes in body condition, expressed as the length and body mass of adult individuals are scaled mass index, in 738 male fire salamanders. Seasonal summarized in table 3 and in fig. 2. Mod- quadratic trend is shown. els without interactions demonstrated three trends. First, females were on average 0.89 g the Sudetes, although this was statistically sig- heavier (95% c.l.: 0.87-0.92) than males (log nificant only for body length (mean difference likelihood-ratio test: χ 2 = 57.198, df = 1, equalled 1.12 cm, 95% c.l.: 1.05-1.20; χ 2 = P<0.001). Second, salamanders from the 7.0803, df = 1, P = 0.008) and marginally so Carpathians tended to be bigger than those from for body mass (difference of 1.37 g, 95% c.l.: Downloaded from Brill.com09/29/2021 06:09:10PM via free access 68 A. Najbar et al.

Table 2. Total body length, body mass and age of females, males and juvenile fire salamanders from the Polish parts of the Sudetes and the Carpathian Mountains.

Sudetes Carpathians

Females Males Juveniles Females Males Juveniles

Body length (cm) N 639 632 177 147 142 50 Mean 14.34 14.33 8.79 17.03 16.35 9.54 Range 9.4–20.0 9.7–21.0 4.0–12.9 9.8–20.5 10.6–19.5 4.8–14.5 SD 1.861 1.769 2.008 1.820 1.554 2.428 Body mass (g) N 755 717 175 147 142 50 Mean 19.16 16.40 5.29 29.73 24.15 6.97 Range 5.3–48.7 5.5–42.7 0.5–13.3 6.8–51.7 6.8–42.0 0.6–16.5 SD 6.941 5.063 2.704 8.822 6.787 4.009 Age (LAGs) N 329 380 91 146 140 51 Mean 7.12 7.30 2.80 9.06 8.36 1.98 Range 2–12 2–16 1–5 2–16 2–15 1–4 SD 2.041 2.229 1.137 2.549 2.264 0.927

1.15-1.64; χ 2 = 3.598, df = 1, P = 0.058). (0.800

Table 3. Generalized linear mixed models explaining the variation in log-transformed total body length (N = 1,560 observations) and body mass (N = 1,761) of adult fire salamanders. For each dependent variable two models are presented: without (1), and with (2) an interaction between sex and mountain range. Fixed effects are specified as alpha (for intercepts) or beta (for fixed-response variables) coefficients with standard errors. Random effects structure is presented as standard deviations of random intercepts.

Model Coefficients ± SE SD

Body length (1) df = 8 Year 0.0152 Season advancement 0.0329 Site 0.0614 Intercept 2.5570 ± 0.0795 Altitude 0.0000 ± 0.0002 Mountain range 0.1126 ± 0.0336 Sex 0.0006 ± 0.0055 Body length (2) df = 9 Year 0.0147 Season advancement 0.0331 Site 0.0613 Intercept 2.4970 ± 0.0827 Altitude −0.0000 ± 0.0002 Mountain range 0.1671 ± 0.0396 Sex 0.0432 ± 0.0176 Mountain range × Sex 0.0360 ± 0.0141 Body mass (1) df = 8, Year 0.0736 Season advancement 0.1352 Site 0.1429 Intercept 2.7927 ± 0.1876 Figure 3. Growth curves and their parameters for male Altitude −0.0002 ± 0.0004 and female fire salamanders in the Carpathians and the Mountain range 0.3173 ± 0.0917 Sudetian Mountains. On the upper panel, growth curves Sex −0.1117 ± 0.0146 are superimposed on data on age and body lengths of 979 Body mass (2) individuals. The lower panel presents sample sizes, point df = 9 estimates of parameters and, shown as boxes around them, Year 0.0723 their 95% bootstrap percentile confidence intervals. Black Season advancement 0.1351 colour refers to the Carpathian and grey to the Sudetian Site 0.1431 population. Growth curves and boxes around parameter Intercept 2.7492 ± 0.1984 estimates for females are drawn with the solid pattern and Altitude −0.0002 ± 0.0004 for males with the dotted pattern. Mountain range 0.3569 ± 0.1089 Sex −0.0829 ± 0.0482 Mountain range × Sex −0.0248 ± 0.0394 age dimorphism was stronger in populations from the Carpathians than from the Sudetes (fig. 2). Growth curves (fig. 3A) were fitted to four fairly weak. A model, which included an in- subsamples: males and females and both moun- teraction between the mountain range and sex, tain ranges. Exact values of growth curves pa- better fitted to the data (AIC =−3.9; χ 2 = rameters are provided in the supplementary 5.812, df = 1, P = 0.016) and suggested that table S3. The results demonstrated that females Downloaded from Brill.com09/29/2021 06:09:10PM via free access 70 A. Najbar et al. attained significantly higher asymptotic body Carpathians and Sudetes would be the simplest size than males (fig. 3B), but their growth rate explanation of observed variation in biometry of tended to be relatively lower (the difference salamanders. However, even though the altitude was statistically significant only in the Sudetes). of local populations ranged widely (from 283 Growth curves did not differ significantly be- to 615 m a.s.l.), its effect on morphometry was tween the mountain ranges. However, the width negligible in all statistical analyses. Therefore, of confidence intervals suggested that in the the observed variation might be due to other en- Sudetes, relationships between age and body vironmental factors, like microclimate or nutri- length were much looser. This was also reflected tional conditions (Miaud, Guyétant and Faber, by R2 values for fitted growth curves, which in 2000; Miaud et al., 2001; Morrison and Hero, the Sudetes equalled 0.59 and 0.52, whereas in 2003; Sinsch et al., 2007; Reading, 2007; Rein- the Carpathians 0.92 and 0.90 (in females and hard, Renner and Kupfer, 2015). We hypoth- males, respectively). esise that differences in habitat quality result- ing from the anthropogenic impact might play a crucial role. Discussion Between 1860 and 2013 the area covered by forests in the Polish part of the Carpathians in- In the Carpathians, salamanders were longer, creased from 27% to 47%, and in the south- heavier and tended to be older than in the eastern part of this mountain range even from Sudetes. This confirms some results of earlier 35% to 72% (Ostapowicz, 2016). A dynamic studies, based on smaller samples (Juszczyk, increase of the forested areas occurred in 1930– 1987; Paluch and Profus, 2004; Zakrzewski, 1970, and was associated with the abandonment 2007). In amphibians, body size and lifespan of farmlands and depopulation (Ostapowicz, (for salamanders longevity, see table 4) may co- 2016). At present, large parts of the Carpathians vary with altitude (Miaud, Guyétant and Faber, are covered by compact humid forests, includ- 2000). Thus altitudinal differences between the ing old-growth ones, with a large share of fallen

Table 4. Longevity of true salamanders of the genus Salamandra (Salamandridae) studied by skeletochronology. It appears that the duration of life co-varied with the sample size taken in the study (Spearman rank correlation: r = 0.80, N = 15, P<0.001).

Species/subspecies N Maximum age References observed (years)

Salamandra salamandra salamandra 475 ♀, 520 ♂ 16 ♀-17∗ ♂ this study Salamandra algira 17 ♀,42♂ 19 ♀-20 ♂ Reinhard, Renner and Kupfer, 2015 Salamandra algira algira 34 ♀,14♂ 18 ♀-17 ♂ Bouzid et al., 2017 Salamandra atra NA 17 Fachbach, 1988; cited by Smirina, 1994 Salamandra infraimmaculata NA 18 Warburg, 1994; cited by Warburg, 2007 16 ♀,14♂ 12 ♀-11 ♂ Altunı¸sık, 2018 Salamandra lanzai 120 ♀, 135 ♂ 24 ♀-23 ♂ Miaud et al., 2001 Salamandra salamandra almanzoris 25 10 Alcobendas and Castanet, 2000 Salamandra salamandra bejarae 43 13 Alcobendas and Castanet, 2000 Salamandra salamandra bernardezi 29 11 Alcobendas and Castanet, 2000 Salamandra salamandra crespoi 10 9 Alcobendas and Castanet, 2000 Salamandra salamandra fastuosa 28 12 Alcobendas and Castanet, 2000 Salamandra salamandra gallaica 41 15 Alcobendas and Castanet, 2000; 63 ♀,90♂ 15 ♀-19 ♂ Rebelo and Caetano, 1995 Salamandra salamandra longirostris 8 12 Alcobendas and Castanet, 2000 Salamandra salamandra morenica 9 9 Alcobendas and Castanet, 2000 Salamandra salamandra terrestris 22 12 Alcobendas and Castanet, 2000

∗8-year-old male (age estimated by skeletochronology), then collected again after 9 years (capture-mark-recapture method). Downloaded from Brill.com09/29/2021 06:09:10PM via free access Life history traits of Salamandra salamandra from Poland 71 and rotting trees, providing favourable habitats We found significant differences in body size with a high availability of food (see Miaud et al., and mass between females and males, which ap- 2001). This may facilitate undisturbed growth peared to be stronger in the Carpathians. Sexual and high survival rate in fire salamanders. dimorphism in body size has been described in In contrast, in the Sudetes the fragmen- many Salamandra spp. populations (Degani and tation and the loss of suitable habitats are Warburg, 1978; Labus, Cvijanovicˇ and Vukov, observed. Our long-term field data revealed 2013; Balogová and Uhrin, 2015; Altunı¸sık, that about 30% of local populations declined 2017) and explained as a result of stronger cor- (Ogrodowczyk et al., 2010). In some places relation between body size and fecundity in the northern range of the species has shifted females than in males (Shine, 1979; Halliday by 10-20 km to the south (Głowacinski,´ and Tejedo, 1995; Bruce, 2000; Kupfer, 2007; Ogrodowczyk-Konowalik and Ogielska, 2018). Wells, 2007; Liao and Lu, 2011, reviewed in The most important direct cause of population Reinhard, Renner and Kupfer, 2015). We can- decline was a large-scale forest dieback due to not explain a weaker sexual dimorphism in body industrial emissions and acid rainfalls, which in- length observed in the Sudetes. However, some tensified in the 1970–1980s. Only at the Polish- similar exceptions from a general rule that fe- Czech Republic boundary the area of deforesta- male salamanders are larger than males, have tion reached 39,000 ha, and had a destructive already been described. Thus, Kalezicetal.´ effect on invertebrates and selected groups of (2000) reported the reverse trend (with larger vertebrates (Jadczyk, 2009; Mazurski, 2014). It males) in S. salamandra from the Balkans, and should also be noted that mixed forests with pointed to the lack of consistency in sexual size the admixture or predominance of spruce (Picea dimorphism within wider areas. sp.) in the Sudetes, even when undisturbed, In our populations both sexes displayed provide suboptimal habitats for salamanders asymptotic growth, slowing down with age, (Conrady, 2003; Thiesmeier, 2004; Glina et al., typical of Salamandridae (Joly, 1968; Miaud 2016). et al., 2001; Cogalniceanu˘ and Miaud, 2003; In sum, environmental conditions are much Bouzid et al., 2017). Males grew faster in more favourable for fire salamanders in the their first years of life and reached sexual ma- Carpathians compared to the Sudetes and we turity earlier, but at the expense of smaller suggest these differences are most likely respon- size (fig. 3), whereas females grew slower but sible for the differences in the morphometry achieved larger body sizes and became sexu- and mean age (which is a function of survival ally mature later. Such growth patterns are pre- rate) between the two sites. Our previous studies sumably an adaptation to differences in repro- (Najbar et al., 2015; Konowalik et al., 2016) re- ductive efforts (higher in females, cf. Miaud, vealed genetic differences between populations Guyétant and Faber, 2000; Sinsch et al., 2007). from both mountain ranges, thus the phenotypic A weak correlation between body length and variation may also be driven by genetic factors. age in the Sudetes indicates that the sample It should be noted, however, that in the Sudetes was not homogeneous and there were large dif- the composition of gene pools might be affected ferences in growth rates between local popula- by random changes due to the population de- tions, most likely due to different trophic condi- clines (Ogrodowczyk et al., 2010; Konowalik et tions and the extent of habitat deterioration (see al., 2016) and may not necessarily reflect se- above). lective pressures. How much environment and Body condition of males (fig. 2) was poor genes matter might be disentangled in future at the beginning of the active season (March- studies based on a common garden design. April), then reached its peak in early June, Downloaded from Brill.com09/29/2021 06:09:10PM via free access 72 A. Najbar et al. when nutritional conditions are most advanta- References geous, and slightly decreased during summer Alcobendas, M., Castanet, J. (2000): Bone growth plasticity season. A similar pattern was also reported by among populations of Salamandra salamandra: interac- Juszczyk (1987), Thiesmeier (2004) and Za- tions between internal and external factors. Herpetolog- krzewski (2007). Weaker condition of males re- ica 56 (1): 14-26. Altunı¸sık, A. (2017): Sexual size and shape dimorphism corded in later months may be related to their in near eastern fire salamander, Salamandra infraim- higher activity during mating period in late maculata (Caudata: Salamandridae). Anim. Biol. 67 (1): summer and autumn (Ryser, 1989; Zakrzewski, 29-40. Altunı¸sık, A. 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The nales Sciences Naturelles Zoologie, Paris 11: 191-196. project was approved by Polish Ministry of Environ- Cogalniceanu,˘ D., Miaud, C. (2003): Population age struc- ment (permit No. DOPog.-4201-02-74/05kl), General Di- ture and growth in four syntopic amphibian species in- rectorate for Environmental Protection (permit No. DZP- habiting a large river foodplain. Can. J. Zool. Zoology WG.6401.02.7.2014.JRO), Regional Directorate for Envi- 81: 1096-1106. ronmental Protection in Wrocław (permit No. WPN.6401. Conrady, D. (2003): Verbreitung. Lebensraumansprüche, 211.2015.MR.2), and II Local Ethics Commission for Ani- Gefährdung und Erhaltung von Feuersalamander mal Experiments in Wrocław (resolutions No. 63/2008, und Reptilien im “Mittleren Thüringer Wald” und 78/2014 and 68/2015). The study was financed by grants “Thüringer Schiefergebirge”. Artenschutzreport 13: KBN NN 303 4147737, DS 1076/S/IBS/2014´ and 0420/ 5-13. 1409/16. Davenport, J.M., Hossack, B.R. 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