Monitoring of Salamandrina perspicillata (Savi, 1821) and Rana italica Dubois, 1987, twenty years later (Amphibia: Salamandridae, Ranidae)

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1 RESEARCH ARTICLE 2014 VOLUME 30 PAGES Monitoring of Salamandrina perspicillata (Savi, 1821) and Rana italica Dubois, 1987, twenty years later (Amphibia: Salamandridae, Ranidae) In memory of Francesco Barbieri ( ) who studied with passion the herpetofauna of northern Apennine and discovered most of the localities covered by this note. Roberto Sindaco 1 *, Cristina Grieco 1 1. Istituto per le Piante da Legno e l Ambiente, Corso Casale 476, I Torino, Italy The status of the Italian endemics Salamandrina perspicillata and Rana italica at the northern edge of their ranges is ascertained comparing intensive surveys carried out by F. Barbieri in the nineties and repeated by the authors about twenty years later. Results show that the status of S. perspicillata is stable, while populations of Rana italica have increased in the past decades. INTRODUCTION Salamandrina perspicillata and Rana italica are two Italian endemics distributed along the Apennine Mountains, reaching the Po drainage basin at the northernmost limit of their range (Sindaco et al., 2006). They live in similar habitats, typically in small mountain streams with rocky bottom in forested areas, and often occur in syntopy. Monitoring of these species is of particular interest because both S. perspicillata and R. italica are species of European concern, and chiefly at the range s boundaries, where populations are more sensitive to the extinction risk than those living within the main range, as they tend to have lower densities and show greater population fluctuations (cf. Vucetich & Waite, 2003). No population studies are available for the two species in northern Apennine, but there are reliable data on the reproductive sites occupied about 20 years ago, due to the exhaustive surveys carried out by the late Francesco Barbieri (Barbieri, 1992), who first reported the occurrence of R. italica and S. perspicillata in Piedmont region (Barbieri et al., 1988; Zuffi & Barbieri, 1988). About 20 years later, the authors have conducted in depth surveys to verify all known reproductive localities of the two species in Piedmont, with the aim to evaluate their conservation status at the northern edge of their range. Study area MATERIALS AND METHODS The study area includes three valleys of the Ligurian-Piedmont Apennine (from north to south: Val Curone, Val Borbera and Valle Spinti), all of them located in the Alessandria province (south-eastern Piedmont, NW Italy) (fig. 1). The study area, almost completely mountainous or hilly, is delimited in the north by the Po alluvial plain, in the Received 15 May 2012 *Corresponding author Accepted 06 September 2013 Published Online 31 January 2014 ISSCA and authors 2014 rsindaco@gmail.com

2 ROBERTO SINDACO & CRISTINA GRIECO east by the watershed dividing the Alessandria province from the Pavia and Piacenza provinces, in the south by the watershed dividing the Alessandria and Genoa provinces, and in the west by the Scrivia river. The altitude is between 150 m (Po plain) and 1699 m (Monte Chiappo). Figure 1. The study area, with the localities surveyed by F. Barbieri (all amphibian species; open squares) and during the present study (filled circles). The white line indicate the approximate distribution of Rana italica and Salamandrina perspicillata (the latter north of the dashed line). Survey The knowledge on the distribution of these two species in Piedmont was summarized by Francesco Barbieri (in Andreone & Sindaco, 1999), who surveyed in depth the study area between 1987 and 1992 and discovered almost all the localities currently recorded in the dataset of the herpetological atlas of Piedmont and Aosta Valley (Andreone & Sindaco, 1999). Between 1987 and 1992 the Savi s spectacled salamander was recorded in 11 localities (tab. 1), and the Apennine frog in 8 localities (tab. 2). To plane the monitoring, all known localities have been searched on regional maps (scale 1:10000) and other maps, and geo-referenced to the best accuracy, on the basis of descriptions and altitudes reported in the dataset. Between 2007 and 2009, 11 field trips have been carried out to verify the occurrence of the two species (eggs, larvae and adults) in the known localities. When the search failed, a second and then a third survey have been carried out in different periods. Besides the localities recorded in the past by F. Barbieri, most of suitable habitats encountered in the study area have been visited too. Surveys have been conducted during the day, searching the species during the egg-laying period (April to May) and during the larval development (June to July). Every reproductive site has been georeferenced by a GPS, mapped and filed in order to easily find the sites in the future. Coordinates are not shown in the tables for reasons of conservation; they are available on request for Table 1. Confirmation of past records of S. perspicillata in Piedmont ( ). N Confirmed Locality Altitude Year Reporter 1 + Cabella L., Dova, Rio del Fornetto F. Barbieri 2 + Carrega L., drinking trough of Pra farmhouse F. Barbieri 3 + Carrega L., Cartasegna, Rio Ghiaion F. Barbieri 4a-b + Carrega L., I and II left tributaries of Rio di Berga F. Barbieri 5 + Carrega L., Molino del Chiappellino F. Barbieri 6 + Carrega L., Rio Carreghino F. Barbieri 7 + Grondona, Rio Valbera and tributaries F. Barbieri 8 + Mongiardino L., Canarie, Rio Ferré F. Barbieri 9 + Mongiardino L., Casalbusone, Rio Predabasso F. Barbieri 10 + Mongiardino L., Case Chiare, Rio Riazzo F. Barbieri 11a + Mongiardino L., Gordena, left tributary F. Barbieri 11b + Mongiardino L., Gordena, Rio Campo degli Asini F. Barbieri 11c + Mongiardino L., Gordena, Rio del Ponte F. Barbieri 12 Ovada* MCSNG; Doria et al., 2001 * locality almost certainly wrong 28

3 ALYTES Table 2. Confirmation of past records of Rana italica in Piedmont ( ). N Confirmed Locality Altitude Year Reporter 1 - Albera L., Rio della Lubbia F. Barbieri 2 - Cabella L., Cosola, Rio degli Orti F. Barbieri 3 - Cantalupo L., Torrente Besante F. Barbieri 4 - Carrega L., Torrente Agnellasca F. Barbieri 5 + Fabbrica Curone, Lunassi, Rio dell Olmo F. Barbieri 6 + Fabbrica Curone, bridge Lunassi, Torrente Curone F. Silvano 7 + Fabbrica Curone, Torrente Arisola F. Barbieri 8 + Gremiasco, Castagnola, Torrente Dorbida F. Barbieri scientific purposes. The significance of variation in occupancy of the species has been tested with the Likelihood Ratio Test (Sokal & Rohlf, 1995), comparing the presence of the two species in all localities surveyed by F. Barbieri in the years and by the authors in the years RESULTS All species localities where F. Barbieri recorded one of the species have been found and surveyed. The locality Ovada (tab. 1, loc. 12), where Doria et al. (2001) report an old specimen of S. perspicillata preserved in the Genoa Museum collection, is likely erroneous, because it is far from the known species range and in an area where appropriate habitats are missing. The results of the surveys are shown below: Figure 2. Distribution of Salamandrina perspicillata in the study area (open circles: records by F. Barbieri, filled circles: records by this study). Figure 3. Distribution of Rana italica in the study area (open circles: records by F. Barbieri, filled circles: records by this study). Salamandrina perspicillata The presence of S. perspicillata has been confirmed in all sites where it was previously found (tab. 1); moreover three new sites have been discovered, one of which in a new 10 x 10 UTM national grid (NQ05) (tab. 3). 29

4 ROBERTO SINDACO & CRISTINA GRIECO The small increase of the species presence in the sites surveyed by F. Barbieri in the past is not significant (LR = 1.20, df = 1, P = 0.27). As previously known, the species is only present in the Borbera and Spinti valleys (fig. 2), where it breeds in small bedrock brooks, mostly on slopes where stretches with fast running water alternate with small waterfalls and deep pools with slow flowing water. Almost all sites are in very shady forested areas, at altitudes between 400 and 1170 m a.s.l. The altitudinal limit is represented by the only artificial reproductive site, a stone wash-house close to a small village. Rana italica As for R. italica, the occurrence has been confirmed in just four (50%) known sites (tab. 2); however, it has been found very close by three unconfirmed sites. Table 3. Localities where S. perspicillata has been recorded during this study. N Loc indicates the correspondence with Barbieri s localities (see tab. 1). Localities with a number and a letter refer to small brooks (= Rio, not translated in the text being part of the geographic name) tributaries to the main stream. N Loc Locality Altitude Date Notes Reporters 1 Cabella Ligure, Rio del Fornetto near the confluence in the stream Gordenella VII.2007 a few larvae 2 Carrega Ligure, drinking trough at the Prà farmstead V.2007 egg clumps, R. Scalera, M. Adams 30 3a 3b 4a 4b 5 6 7a Carrega Ligure, second tributary on the right bank of Rio Ghiaion towards the village Cartasegna Carrega Ligure, first tributary on the right bank of Rio Ghiaion towards Cartasegna Carrega Ligure, Berga, first tributary on the left bank of Rio Berga upstream of the bridge Carrega Ligure, Berga, second tributary on the left bank of Rio Berga upstream of the bridge Carrega Ligure, Molino del Pio [= Chiappellino on the regional map] dint. Carrega Ligure, Fontanachiusa, two small tributaries on the right bank of Rio Carreghino along the track to Capanne di Stagnin Roccaforte Ligure, tributary of the stream Valbera along the track from San Martino towards the stream Spinti IV adults in water and on the ground VI adult on the ground V females in water + 2 collective egg clumps V adults on the ground + 2 egg clumps 21.VII.2007 a few larvae RS, A. 609, A. 30.VI larvae V.2007 respectively 4 adults + 1 egg clump and 1 adult + 2 egg clumps, R. Scalera, M. Adams IV adults on the ground 7b Roccaforte Ligure, Grondona, stream Valbera V adult on the ground 8 Mongiardino Ligure, Gordena, tributary of Rio Ferré S of Canarie 9 Mongiardino Ligure, Casalbusone, Rio Predabasso Mongiardino Ligure, Rio Riazzo upstrem of Case Chiare between the ford and the first tributaries on the right bank 11b Mongiardino Ligure, Gordena, Rio Campo degli Asini c Mongiardino Ligure, Gordena, first tributary on the left bank of Rio del Ponte (near the bridge), M. Evangelista IV adult on the ground 15.IV adult 30.VI egg clump, A IV adult on the ground 30.VI IV IV.2007 a few larvae 2 adults on the ground and 2 in water 1 adult on the ground and 1 adult in water, A. Albera Ligure, Centrassi, Rio della Lubbia VII larva, F. Pupin Cabella Ligure, Piuzzo, Rio del Baiardo V egg clumps Mongiardino Ligure, small brook 400 m downstream of the junction to Camisasca VI egg clumps

5 ALYTES Table 4. Localities where R. italica has been recorded during this study. N Loc indicates the correspondence with Barbieri s localities (see tab. 2): the localities 1 to 4 have not been confirmed. N Loc Locality Altitude Date Notes Reporters Fabbrica Curone, Rio dell Olmo [degli Olmi] downstream of Montecapraro Fabbrica Curone, Lunassi, bridge on the Torrente Curone Fabbrica Curone, Torrente Arisola downstream of Frinti Gremiasco, Castagnola, Torrente Dorbida upstream the crossing with the path n VI adult female and 1 juvenile VII.2008 a few larvae, F. Pupin VII.2008 a few larvae, F. Pupin VII adult male + a few larvae, F. Pupin Cabella Ligure, Montaldo di Cosola, Rio Fisina V juvenile Cabella Ligure, Montaldo di Cosola, Rio Gorreio V adult Cabella Ligure, Piuzzo, Rio del Baiardo V adult Cabella Ligure, Rio del Fornetto near the confluence in the Torrente Gordenella Carrega Ligure, Berga, second tributary on the left bank of Rio Berga upstream of the bridge Carrega Ligure, Carrega L., upstream of the bridge on Rio Carreghino Carrega Ligure, second tributary on the right bank of Rio Ghiaion directing towards Cartasegna Carrega Ligure, first tributary on the right bank of Rio Ghiaion directing towards Cartasegna Carrega Ligure, 5 small tributaries on the right bank of Rio Carreghino along the track between Fontanachiusa and Capanne di Stagnin Mongiardino Ligure, Casalbusone, Rio Predabasso 742 Mongiardino Ligure, Gordena, second tributary of Rio Ferré south of Canarie VII juvenile V juveniles VI juveniles + 1 larva, A IV newly metamorphosed VI adult V IV VI.2007 overall 3 adults and 6 juveniles 1 mating pair + 1 female 1 newly metamorphosed, R. Scalera, M. Adams, A IV juvenile Mongiardino Ligure, Gordena, Rio Campo degli Asini VI.2007 a few larvae Mongiardino Ligure, weir on Rio Riazzo near Case Chiare Mongiardino Ligure, small brook 400 m downstream of the junction to Camisasca Mongiardino L., Rovello Superiore, water tank near the village Montacuto, Serbaro, Rio Museglia 795 Roccaforte Ligure, Grondona, Torrente (=stream) Valbera Roccaforte Ligure, Grondona, Torrente Spinti upstream of the village, A IV adult VI.2009 many larvae VI adult V VII larva, F. Pupin 6.VIII.2008 many larvae 2 adults and a few larvae V adults, M. Evangelista, M. Evangelista The species has been observed in 17 additional places identifiable as 14 new sites (tab. 4, fig. 3), included in two new 10 x 10 km UTM national grids. The Likelihood Ratio Test shows a significant increase of the presence of the species in the sites surveyed by F. Barbieri in the past (LR = 3.82, df = 1, P = 0.05). The habitats are very similar to those of S. perspicillata, with which often co-occurs, at altitudes between 500 and 1000 meters. 31

6 ROBERTO SINDACO & CRISTINA GRIECO DISCUSSION Salamandrina perspicillata and Rana italica are two species listed in the annexes of the Habitats and Species Directive 92/43/CEE, for which a monitoring programme is required under the Art. 11 and Art. 17, paragraph 1. Regrettably more than 10 years after the transposition of the Directive into the Italian legislation, no official monitoring programme has been designed or planned yet by the responsible institutions. In 2008 the Societas Herpetologica Italica (SHI), promoted a national monitoring project to assess the status of aquatic breeding sites of Italian amphibians, interrupted to the first phase due to lack of funds (cf. Societas Herpetologica Italica, 2011). In the absence of comprehensive monitoring programmes, the evaluation of the conservation status of a species can be made at the local level verifying regularly the presence in known sites, in order to check for possible local extinctions. The capacity to identify sites quoted in literature (or in datasets), in absence of precise geographical coordinates, depends on the quality of the initial information provided with the first sighting, which in this specific case have proved to be sufficiently informative. Another variable that can affect this type of monitoring is the detectability of the species, as a species difficult to find can be overlooked. During the reproductive season, the detectability of both species has been very high: in the confirmed sites (100% for Salamandrina, 50% for Rana italica), both species have been observed in the first survey, except in two cases, when the presence of S. perspicillata was confirmed during the second inspection. For both species an increase of their presence has been observed in the sites previously surveyed by F. Barbieri, although the increase is significant in R. italica only. As for S. perspicillata, the situation appears stable, since the newfound sites were probably just missed by F. Barbieri and cannot be considered as a real range extension. On the contrary, as regards R. italica, the significant number of new sites along watercourses that at the time were well surveyed by F. Barbieri, shows an extension of the species in this area since ACKNOWLEDGEMENTS The authors wish to thank Gentile Francesco Ficetola and Anna Bonardi for statistical support, and to Alberto, Massimo Evangelista, Riccardo Scalera e Michael Adams for assistance in the field. Antonio Romano provided useful comments on early versions of the article. Thanks to two anonymous referees for their useful comments and suggestions. LITERATURE CITED Andreone, F., Sindaco, R. (eds.) (1999). Erpetologia del Piemonte e della Valle d Aosta: Atlante degli anfibi e dei rettili. Monografie XXVI (1998), Museo Regionale di Scienze Naturali, Torino. Barbieri, F. (1992). Atlante degli Urodeli dell Appennino settentrionale. In: Fasola, M. (ed.). Atti II Seminario Italiano Censimenti Faunistici dei Vertebrati, Brescia, 6-9 Aprile 1989, suppl. Ricerche di Biologia della Selvaggina, XVI: Barbieri, F., Zuffi, M.A.L., Tiso, E. (1988). Salamandrina terdigitata nel versante padano dell Appennino settentrionale. Riassunti 52 Congresso Unione Zoologica Italiana, Camerino, September 1988: 3-3. Doria G., Salvidio S., Tavano M.L. (2001). Catalogo degli Anfibi del Museo Civico di Storia Naturale G. Doria di Genova. Annali del Museo Civico di Storia Naturale G. Doria, Genova, 94: Sindaco R., Doria G., Razzetti E., Bernini F. (2006). Atlante degli Anfibi e dei Rettili d Italia. Societas Herpetologica Italica, Edizioni Polistampa, Firenze. Societas Herpetologica Italica, (2011). Assessing the status of amphibian breeding sites in Italy: a national survey. Acta Herpetologica, 6(1): Sokal, R.R., Rohlf, F.J. (1995). Biometry. W. H. Freeman and Company, York. Vucetich, J.A., Waite, T.A. (2003). Spatial patterns of demography and genetic processes across the species range: null hypoteses for landscape conservation genetics. Conservation Genetics, 4: Zuffi, M.A.L., Barbieri, F. (1988). Proposte per la gestione dell erpetofauna paracquicola appenninica e nuovi dati sulla distribuzione di Salamandrina terdigitata, Triturus alpestris apuanus, Rana graeca, Natrix tessellata. Bollettino del Museo di Storia Naturale della Lunigiana, 6-7: