Population structure in Salamandra atra aurorae and ...

ATTI XI CONGRESSO NAZIONALE SOCIETAS HERPETOLOGICA ITALICA Trento 22 - 25 Settembre 2016

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Michele Menegon Ana Rodriguez-Prieto Maria Chiara Deflorian

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Population structure in Salamandra atra aurorae and S. atra pasubiensis: a preliminary evaluation of spatial and temporal variation Lucio BONATO1, Enrico ROMANAZZI1ᅤ, Sara LEFOSSE1, Wouter BEUKEMA2, Kurt GROSSENBACHER3 1

Università di Padova, Dipartimento di Biologia, via Bassi 58B, I-35131 Padova, Italy. E-mails: [email protected];[email protected] 2 Department of Pathology, Bacteriology and Avian Diseases, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium. E-mail [email protected] 3 Eichholzstrasse 18F, CH-3027 Bern, Switzerland. E-mail: [email protected]

Abstract

The unusually yellow-patched populations of Salamandra atra isolated on the Altopiano dei Sette Comuni (S. atra aurorae) and on the Pasubio massif (S. atra pasubiensis) are recognized to have great scientific and conservation value. Despite the absence of extended surveys and long-term monitoring, irregular visits and short-term researches during the period 1995-2015 provide some insights on the structure and juvenile recruitment of four populations during three subsequent periods. We found a significantly lower proportion of juveniles and a higher proportion of adult males when sampling salamanders in epigean activity, compared to sampling inactive salamanders in refuges. After controlling for methodological biases and sampling errors, we found generally a lower proportion of juveniles in the period 2006-2008 compared to an earlier (1995-1998) and a later (2012-2015) period. A higher proportion of juveniles was usually found in the population of S. atra aurorae in Val d’Anime-Bosco del Dosso than in another two populations of the same subspecies. Instead, an adult sex ratio distinctly biased towards males was found in the population of S. atra pasubiensis, also among the individuals sampled while inactive in refuges, whereas an average males/ females ratio of 0.9 was found in the same period in the populations of S. atra aurorae.

Riassunto

Struttura di popolazione in Salamandra atra aurorae e S. atra pasubiensis: una valutazione preliminare di variazioni spaziali e temporali. Le popolazioni di salamandre alpine che si trovano isolate sull’Altopiano dei Sette Comuni (Salamandra atra aurorae) e sul massiccio del Pasubio (S. atra pasubiensis) sono riconosciute di notevole interesse scientifico e conservazionistico. No-

Atti XI Congresso Nazionale della Societas Herpetologica Italica, Trento 2016 153

,  nostante ciò, non sono ancora state attivate ricerche estese e monitoraggi a lungo termine. Tuttavia, i dati ottenuti finora da visite occasionali e indagini standardizzate condotte per brevi periodi permettono alcune valutazioni sulla struttura di tre popolazioni di S. atra aurorae e della sola popolazione conosciuta di S. atra pasubiensis. Per evitare bias dovuti ai diversi metodi di ricerca, sono stati considerati solo gli individui trovati inattivi nei rifugi, mentre sono stati esclusi quelli osservati in attività spontanea in superficie. In generale, la proporzione di giovani stimata nel periodo 2006-2008 è risultata inferiore sia rispetto a un periodo precedente (1995-1998) sia a uno successivo (2012-2015). Tale proporzione, inoltre, è risultata di solito maggiore nella popolazione di S. atra aurorae di Val d’Anime-Bosco del Dosso che in altre due popolazioni della stessa sottospecie. Invece, tra gli adulti, la proporzione tra maschi e femmine è risultata sbilanciata per i maschi nella popolazione di S. atra pasubiensis, diversamete da quella stimata nello stesso periodo nelle popolazioni di S. atra aurorae. Keywords

Salamandra atra aurorae, Salamandra atra pasubiensis, sex ratio, recruitment.

Introduction Unique yellow-patched populations of Salamandra atra are present in narrow areas on the Italian Eastern Prealps. They are distinguished as S. atra aurorae (about a dozen sites on the Altopiano dei Sette Comuni) and S. atra pasubiensis (a single known population on the Pasubio massif; Romanazzi & Bonato, 2014). Despite the fact that these populations have been recognized to have major scientific and conservation value (e.g., Andreone et al., 2009; Rondinini et al., 2013), basic information on their structure and dynamics is still missing. These populations have been investigated so far mainly by irregular volunteer surveys, while standardized surveys have focused on single populations for short periods of time. Nevertheless, occasional visits and short-term researches during the last two decades allowed accumulating data on different populations of S. atra aurorae and the single known population of S. atra pasubiensis in different years. Even though these data are inadequate to accurately estimate population composition (age classes, sexes) and rate of recruitment while controlling for detectability variation (Schmidt, 2004; Mazerolle et al., 2007), they nevertheless allow to test for major differences between populations and between time periods. Materials and Methods Between 1995 and 2015, we visited repeatedly three distinct sites on the Altopiano dei Sette Comuni and another single area on the Pasubio massif (Tab. 1), searching for individuals of S. atra aurorae and S. atra pasubiensis respectively. Searches were carried on during daylight, following two alternative methods: (a) searching for inactive individuals while resting in their diurnal refuges, by inspecting


,  holes, crevices and shelters on the ground; (b) searching for active individuals on the ground surface, by walking and exploring visually the surface. The latter method was applied only when raining or in the first hours after intense rains. All effective visits were between May and October, but they were carried out at regular intervals only in single sites and in some years. In particular, the population of S. atra aurorae from Val d’Anime-Bosco del Dosso was surveyed more intensely and at regular intervals during the years 1996-1997 and 2014-2015. Overall, we performed 156 daily visits and spent more than 300 hours searching for salamanders. Almost all individuals found were measured (total length, from the snout to the tail tip, to the nearest mm), by gently aligning the individual along a ruler, and photos were taken of the dorsal side. By comparing the pattern of yellow patches between photos, it was possible to confidently distinguish all individuals of S. atra aurorae and most individuals of S. atra pasubiensis (except a few uniformly black individuals; Bonato et al., 2007). Following conventional thresholds for S. atra (e.g.: Klewen, 1988; Luiselli et al., 2001; Bonato & Fracasso, 2003), an individual was considered “adult” if ≥ 90 mm long, “juvenile” if < 90 mm long, “new-born” (i.e., most probably born in the year) if < 65 mm long. The sex was evaluated only in adults: males were distinguished from females for a more distinct ventral protrusion of the cloacal region (Klewen, 1988; Bonato et al., 2007). Females were considered “obviously pregnant” when the posterior part of their trunk was distinctly swollen laterally (Klewen, 1988; Kalezić et al., 2000). Results When comparing the samples of salamanders found inactive in refuges with the sample of salamanders found active on the ground surface, within a single population in a single year, we found significant differences in the age and sex composition of the samples obtained with the two alternative searching methods. At least in the most intensely surveyed population of S. atra aurorae from Val d’Anime-Bosco del Dosso, we found a significantly lower proportion of juveniles and a higher proportion of adult males among the individuals found active on the surface (Tab. 2). Additionally, in all populations we found new-borns almost only among the individuals found inactive in refuges and a higher proportion of obviously pregnant females among these individuals, but the differences were not statistically significant (Tab. 2). As the estimates of the population parameters were affected by the sampling method, we limited our comparisons to the individuals found resting in refuges, for which we obtained usually larger samples. Within any single population, we found evidence for some changes in the population structure through the years, assuming negligible temporal variation in detectability. In particular, in the population of S. atra aurorae from Val d’Anime-Bosco del Dosso, variable proportions were found in different years for the new-borns (between 3% in 2015, n = 29, and 22% in 1996, n = 65) and the juveniles (between 10% in 2007, n = 10, and 38% in 1996, n = 65), but the differences between years were not statistically significant (Ȳ2: P > 0.05 for both parameters). However, after pooling the samples obtained in


,  contiguous years (Fig. 1), we found in all populations that the proportion of juveniles in the period 2006-2008 was generally lower than in an earlier and a more recent period. The differences were statistically significant not only in the single population from Val d’Anime-Bosco del Dosso but also when considering all populations of S. atra aurorae together, both with respect to an earlier period (1995-1998; Fisher exact test: P = 0.0047) and with respect to a later period (2012-2015; P = 0.0226). We recovered a similar, significant difference also in S. atra pasubiensis, when comparing the two periods 20062008 and 2012-2015 (P = 0.0159). Conversely, similar sex ratios and proportions of pregnant females were found in different years, also when pooling years or populations (Fig. 1; Fisher exact test and Ȳ2: P > 0.05 in all cases). Comparing the three surveyed populations of S. atra aurorae, we found generally higher proportions of juveniles in Val d’Anime-Bosco del Dosso than in the other sites, but with marginal statistical significance only when pooling the samples from the entire period 1995-2015: 33% in Val d’Anime-Bosco del Dosso vs. 11% in Costa di Sopra-Valle Sparavieri (Fisher exact test: P = 0.0655) and 13% in Val di Nos (P = 0.0596). Instead, no evidence emerged for differences between the three populations in the proportion of new-borns, adult sex ratio and proportion of pregnant females, even when pooling the samples from the entire period (Ȳ2: P > 0.05 in all cases). Considering the adult sex ratio in our samples, we found a distinct bias towards males in the population of S. atra pasubiensis, both in the period 2006-2008 and 2012-2015, but not in the populations of S. atra aurorae (Fig. 1). Taking the two periods together, the overall sex ratio in S. atra pasubiensis (75% males and 25% females, n = 20) was significantly different from that found in S. atra aurorae both when considering the single population from Val d’Anime-Bosco del Dosso (48% males and 52% females, n = 48; Fischer exact test: P = 0.0317) and when uniting all populations of the latter subspecies (47% males and 53% females, n = 74; P = 0.0421). Instead, differences between S. atra pasubiensis and the populations of S. atra aurorae in the proportion of new-borns, juveniles and pregnant females were not significant, also after pooling the samples from different years (P > 0.05 in all cases). Discussion Population structure evaluation of S. atra aurorae and S. atra pasubiensis is difficult because of their behaviour: they are usually subterranean and hard to detect. Published estimates of population parameters in other populations of S. atra are very variable (summarized in Bonato et al., 2007; also Helfer et al., 2012): the sex ratio is most often male-biased, with males comprising from 50% to almost 70% of the adults, and the proportion of juveniles varies from almost none to more than 40%. However, these are hardly comparable with our estimates, because different authors employed different sampling methods, looking for active salamanders or searching for salamanders concealed in the soil or even mixing the two approaches. Moreover, estimating and comparing basic parameters of population structure is complicated by the fact that very different estimates are obtained depending on the sampling strategy. Smaller and younger individuals are remarkably more frequent Atti XI Congresso Nazionale della Societas Herpetologica Italica, Trento 2016 156

,  among the salamanders found concealed in the soil, whereas the apparent sex ratio is distinctly biased towards males among the salamanders sampled in epigean activity. These differences agree with the results obtained when different methods were directly tested (on a single population of S. atra aurorae in a single year; Lefosse et al., 2016) and may be explained by differences in mobility, depth of refuges and/or visual detectability between individuals of different age, body size and sex. As a consequence, in order to test for differences between populations and between periods, we preliminarily filtered our records to reduce these expected methodological biases. Assuming negligible variation in detectability between period of years and between sites, significant evidence emerged for some temporal variation in the population recruitment through the two decades, at least in some sites, and for different proportions of males and females between the populations of S. atra pasubiensis and those of S. atra aurorae. The latter difference, however, could be partially affected by different habitat features between the sites, determining different microclimate and availability of shelters on the ground, and eventually different detectability of individuals of different age, size and sex. While all three populations of S. atra aurorae inhabit stable forest soils on moderate slopes, the population of S. atra pasubiensis occupies much more rocky and unstable terrains with shrubby vegetation (Bonato & Steinfartz, 2005; Romanazzi & Bonato, 2014). More generally, our results should be considered with caution also because most searching sessions have been performed under variable meteorological conditions and at irregular intervals during the season, and the salamander behaviour could be variably affected by the contingent conditions depending on age and sex.

Fig. 1. Proportions of juveniles (histograms) and adults of different sex (pie-charts), estimated in different periods among the individuals found resting in refuges, in S. atra aurorae and S. atra pasubiensis. Atti XI Congresso Nazionale della Societas Herpetologica Italica, Trento 2016 157

, 

CODE

ALTITUDE

SURVEYED AREA

PERIOD

SUBSPECIES

Costa di Sopra-Valle Sparavieri

2

1360-1450 m

~ 10 ha

2007

aurorae

Val d’Anime-Bosco del Dosso

3

1340-1550 m

~ 50 ha

1995-2015

aurorae

Val di Nos: Giaron-KaprustEsenplatz

9

1280-1530 m

~ 30 ha

1995-2014

aurorae

Vajo del Ponte-Val Fontana d’Oro

13

1450-1800 m

~ 5 ha

1999-2012

pasubiensis

NAME

Tab. 1. Populations of S. atra aurorae and S. atra pasubiensis investigated in the period 1995-2015. Populations are named and coded following Romanazzi & Bonato (2014).

YEAR

2014

2015

SAMPLED INDIVIDUALS

ALL INDIVIDUALS

ᄛᄛADULTS

ADULTS

n % new-borns % juveniles

n

%ᄝᄝ

n

% pregnant

inactive

36

11%

28%

24

54%

11

45%

active

62

0%

8%

54

72%

16

31%

P

-

0.1179

0.0174

-

0.1289

-

0.6868

inactive

31

3%

26%

21

43%

12

33%

active

47

0%

4%

43

67%

17

6%

P

-

0.4915

0.0008

-

0.0026

-

0.1296

Tab. 2. Proportions of new-borns, juveniles, adult males and females, and obviously pregnant females, found with different sampling methods (searching for individuals in refuges vs. searching for active individuals on the ground surface), in two years, in the population of S. atra aurorae from Val d’Anime-Bosco del Dosso. p-values refer to the Fisher exact test.

Acknowledgements We are grateful to many people who collaborated during field research, including P. Brakels, I. Mosele, V. Pedron, V. Pigato, A. Riga, and to an anonymous reviewer who helped us to improve the paper. Permits for searching and manipulation of salamanders were obtained by Italian M.A.T.T.M. (prot.: 14198 13/07/2012, 1758 29/01/2014, 3128 18/02/2014) and Comune di Asiago. Field researches were partly supported by Regione Veneto (Sezione Parchi, Biodiversità, Programmazione Silvopastorale e Tutela del Consu-


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