Body Size and Life History Traits of the Fire Salamander Salamandra

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, skeletochronology. 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 season, 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 Table 1. Sampling sites of the fire salamander Salamandra salamandra in its entire known distribution range in Poland. Coordinates were designated in Google Earth 7.1.5.1557 (Google Inc., 2005). Salamandra salamandra Site Years of samples collection Locality Orographic and conservation units Mountain range Altitude Coordinates number 1 2015–2016 Bogatynia Eastern Upper Lusatia Sudetes 283 50°5805.3N, 14°5446.1E 2 2008–2009 Górzyniec Izera Mountains Sudetes 470 50°5132.7N, 15°3340.2E 3 2008–2009 Janowice Wielkie Katzbach Mts., Rudawy Janowickie Mts.

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