Local extinction of Bombina pachypus Bonaparte, 1838 in three

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Introduction Apennine yellow-bellied toad (Bombina pachypus) has been recently recognized as a distinct species from B. variegata (Lanza and Corti, 1993; Fromhage, Vences and Veith, 2004), on the basis of morphological and genetic evidences (Vaccaneo, 1931; Lanza and Vanni, 1991; Sarrocco and Bologna 2000, Canestrelli et al., 2006), and is recognized as a species also by IUCN (Andreone et al., 2008), although for long it has been perceived as a subspecies of B. variegata (Barbieri et al., 2004; Hofman et al., 2007; Zheng et al., 2009). This taxon is an endemism of the Italian peninsula although restricted to the Appenine mountain chain; while from Lombardy to Friuli, a similar species occurs: B. variegata. Bombina pachypus spend the daylight hours in the water, while nocturnal feeding activity is recorded on terrestrial invertebrates around the ponds (Barbieri et al., 2004). The species is active between March and October, although the maximum activity is recorded between May and June (Barbieri et al., 2004). It breeds in ephemeral freshwater pools (Lanza, 1983; Guarino et al., 1998; Mirabile et al., 2009), in areas of variable altitudes of the Apennine Mountains (200-800 m a.s.l., up to 1600 m a.s.l.: Barbieri et al., 2004). From the end of April to the beginning of September, each individual of Apennine yellow-bellied toad can breed several times (Barbieri et al., 2004). The highly fragmented distribution range allowed the formation of distinct genetic pools, with a high diversity in Calabria, that acted as a biogeographic refuge during the last glaciation period (Canestrelli et al., 2006). Fragmentation of population poses higher risk of local extinction (Sarrocco and Bologna, 2000; Barbieri et al., 2004; Arillo et al., 2009), because of small population sizes (Ellstrand and Elam, 1993; Allendorf and Luikart, 2007). Apennine yellow- bellied toad is protected by the EU (Berne Convention, Annex II; Habitats Directive, Annex IIB and IVD), and by national (DPR 357/1997 and DPR 120/2003) and regional (LR 56/2000) legislation for Biological Conservation, this species is still declining in its entire distribution range (Di Martino and Ferri, 2002; Angelini et al., 2004; Barbieri et al., 2004; Colliva et al., 2006; Mattoccia et al., 2006; Fiacchini, 2007; Romano et al., 2010), and its IUCN status has recently been changed from “Least Concern” to “Endangered” (Andreone et al., 2008). This progressive decline can be provoked by many contributing causes, including habitat loss and fragmentation, desiccation of ponds, disappearing of suitable microhabitats for reproduction (e.g. by cleaning of the pools of livestock watering), increase of the maximum temperature in summer, that could be responsible for the drying up of reproductive sites Herpetology Notes, volume 5: 407-412 (2012) (published online on 10 September 2012) Local extinction of Bombina pachypus Bonaparte, 1838 in three stations: a 17 years survey in pSCI “Poggi di Prata” (Southern Tuscany, Italy). Emiliano Mori 1 * and Alice Giovani 2 1 University of Siena, Department of Environmental Science “G. Sarfatti”, Via T. Pendola, 62 – 53100 Siena, Italy; e-mail: [email protected] 2 Haras de Couvains “L’Hotel Pohier”- 50680 Couvains (Man- che), France; e-mail: [email protected] Abstract. Apennine yellow-bellied toad (Amphibia, Bombinatoridae) is an Italian endemism distributed along the Apennine from the Po River to Southern Calabria. The species is declining throughout its range due to habitat loss, small population sizes and diseases. This species has been recorded at three localities in Grosseto (Southern Tuscany), where the last documented reproduction attempt dated back to 1998, but the species became probably extinct at these sites after 2004. The natural habitat of this species at these localities remained more or less the same in the 17 years of survey (1994-2011) and average year rainfall amount didn’t substantially change. Few animals were found during the study period and this limited number of individual was probably not enough to warrant the sufficient survival of a viable population. Moreover, the great distances between the detected reproductive sites somehow might have limited dispersal. Keywords. Apennine yellow-bellied toad, Grosseto, small population sizes, long-term survey.

Transcript of Local extinction of Bombina pachypus Bonaparte, 1838 in three

Page 1: Local extinction of Bombina pachypus Bonaparte, 1838 in three

IntroductionApennine yellow-bellied toad (Bombina pachypus)

has been recently recognized as a distinct species from B. variegata (Lanza and Corti, 1993; Fromhage, Vences and Veith, 2004), on the basis of morphological and genetic evidences (Vaccaneo, 1931; Lanza and Vanni, 1991; Sarrocco and Bologna 2000, Canestrelli et al., 2006), and is recognized as a species also by IUCN (Andreone et al., 2008), although for long it has been perceived as a subspecies of B. variegata (Barbieri et al., 2004; Hofman et al., 2007; Zheng et al., 2009). This taxon is an endemism of the Italian peninsula although restricted to the Appenine mountain chain; while from Lombardy to Friuli, a similar species occurs: B. variegata. Bombina pachypus spend the daylight hours in the water, while nocturnal feeding activity is recorded on terrestrial invertebrates around the ponds (Barbieri et al., 2004). The species is active between March and October, although the maximum activity is recorded between May and June (Barbieri et al., 2004). It breeds in ephemeral freshwater pools (Lanza, 1983; Guarino et al., 1998; Mirabile et al., 2009), in areas of variable altitudes of the Apennine Mountains (200-800 m a.s.l.,

up to 1600 m a.s.l.: Barbieri et al., 2004). From the end of April to the beginning of September, each individual of Apennine yellow-bellied toad can breed several times (Barbieri et al., 2004). The highly fragmented distribution range allowed the formation of distinct genetic pools, with a high diversity in Calabria, that acted as a biogeographic refuge during the last glaciation period (Canestrelli et al., 2006). Fragmentation of population poses higher risk of local extinction (Sarrocco and Bologna, 2000; Barbieri et al., 2004; Arillo et al., 2009), because of small population sizes (Ellstrand and Elam, 1993; Allendorf and Luikart, 2007). Apennine yellow-bellied toad is protected by the EU (Berne Convention, Annex II; Habitats Directive, Annex IIB and IVD), and by national (DPR 357/1997 and DPR 120/2003) and regional (LR 56/2000) legislation for Biological Conservation, this species is still declining in its entire distribution range (Di Martino and Ferri, 2002; Angelini et al., 2004; Barbieri et al., 2004; Colliva et al., 2006; Mattoccia et al., 2006; Fiacchini, 2007; Romano et al., 2010), and its IUCN status has recently been changed from “Least Concern” to “Endangered” (Andreone et al., 2008).

This progressive decline can be provoked by many contributing causes, including habitat loss and fragmentation, desiccation of ponds, disappearing of suitable microhabitats for reproduction (e.g. by cleaning of the pools of livestock watering), increase of the maximum temperature in summer, that could be responsible for the drying up of reproductive sites

Herpetology Notes, volume 5: 407-412 (2012) (published online on 10 September 2012)

Local extinction of Bombina pachypus Bonaparte, 1838 in three stations: a 17 years survey in pSCI “Poggi di Prata”

(Southern Tuscany, Italy).

Emiliano Mori1* and Alice Giovani2

1 University of Siena, Department of Environmental Science “G. Sarfatti”, Via T. Pendola, 62 – 53100 Siena, Italy; e-mail: [email protected]

2 Haras de Couvains “L’Hotel Pohier”- 50680 Couvains (Man-che), France; e-mail: [email protected]

Abstract. Apennine yellow-bellied toad (Amphibia, Bombinatoridae) is an Italian endemism distributed along the Apennine from the Po River to Southern Calabria. The species is declining throughout its range due to habitat loss, small population sizes and diseases. This species has been recorded at three localities in Grosseto (Southern Tuscany), where the last documented reproduction attempt dated back to 1998, but the species became probably extinct at these sites after 2004. The natural habitat of this species at these localities remained more or less the same in the 17 years of survey (1994-2011) and average year rainfall amount didn’t substantially change. Few animals were found during the study period and this limited number of individual was probably not enough to warrant the sufficient survival of a viable population. Moreover, the great distances between the detected reproductive sites somehow might have limited dispersal.

Keywords. Apennine yellow-bellied toad, Grosseto, small population sizes, long-term survey.

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Emiliano Mori & Alice Giovani408

(Girardello et al., 2010), and predation by dragonfly larvae, mostly on tadpoles (Barbieri et al., 2004; Arillo et al., 2009). And in the Northern Apennines, infection

by chytridiomycosis has been reported as a cause of extinction of this species (Stagni et al., 2004). Sun exposure, water temperature and level of vegetation cover seem to be less influential variables for the survival of the Apennine yellow-bellied toad (Arillo et al., 2009), but the drying of reproductive sites is currently inducing populations isolation, and that might trigger a local extinction process. Ecological researches and conservative actions, as for example surveillance of reproductive sites and long term studies, are essential for this species (Scoccianti, 2004; Arillo et al., 2011). In this work, we present the results of a survey on the Apennine yellow-bellied toad, performed for 17 years. Two individuals (one male and one female) have been recorded near Boccheggiano (43.090075° N, 11.033477° E, 582 m a.s.l.), in an artificial cement pond (1.70×0.80×0.8m), in 1995 and in 1997, but breeding never occurred. They disappeared after the introduction of Carassius auratus in the pond. Analysis and comparison of ventral pattern revealed that migration between these stations never occurred.

Figure 1. Location of the study area. The miniature of Tuscany localizes the village of Prata.

Figure 2. Drawing of the individual ventral pattern of one of the studied B. pachypus (M1FC1).

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Local extinction of Bombina pachypus 409

Materials and Methods

Study areaThe study area is included in a proposed site of community im-portance (pSCI) of about 1062 hectares around the village of Prata (Grosseto), between 618 and 1060 m a.s.l (Fig. 1), in the Metalliferous Hills.

The average annual temperature is around 12° C, with an average excursion of about 18° C. The average annual rainfall is around 1000 mm, with a small proportion of snow. The species of Am-phibians found in the pSCI are listed below: Italian crested newt (Triturus carnifex), Smooth newt (Lissotriton vulgaris), Apen-nine yellow-bellied toad (Bombina pachypus), Italian pool frog

(Pelophylax bergeri), Italian edible frog (Pelophylax kl. hispani-cus), Italian stream frog (Rana italica), agile frog (Rana dalmati-na) and European toad (Bufo bufo). The three areas inhabited by Apennine yellow-bellied toad are (i) Fonte Canali, (ii) Fonte dei Poveri, (iii) La Pilina, while B. pachypus has never been detected in other ponds inside the pSCI. Fonte Canali (43.116049° N, 10.982529° E, 810 m a.s.l.) is an old livestock watering consis-ting of six cement pools (1.20×0.40×0.4m each), located immedi-ately below the summit of Poggione, in a grassy (Brachipodium sp., Cynodon dactylon, Viola odorata…) surrounded by a mixed deciduous wood (Quercus cerris, Ostrya carpinifolia, Carpinus betulus and Fraxinus ornus). The batrachofauna of this locality consists of T. carnifex, L. vulgaris, R. dalmatina, P. bergeri and B. pachypus. Fonte dei Poveri (43.097933° N,10.990253° E, 688

1

Fonte Canali Fonte dei Poveri La Pilina YearIndividual MFC1 MFC2 MFC3 FFC1 Breeding

(y/n) MFP1 FMP1 Breeding

(y/n) MLP1 MLP2 FLP1 Breeding

(y/n) 1994 2/6 4/6 1/6 6/6 0/6 0/6 0/6 0/61995 4/5 0/5 0/5 5/5 0/5 3/5 0/5 0/51996 7/7 3/7 0/5 4/7 1/7 6/7 7/7 2/7 2/6 1/6 4/6 0/61997 6/6 2/6 4/6 5/6 2/6 4/6 3/6 1/6 8/8 8/8 8/8 0/81998 6/6 0/6 0/6 6/6 3/6 0/6 0/6 0/6 8/8 8/8 6/8 0/81999 4/7 0/7 0/7 0/7 0/7 0/7 0/7 0/7 0/9 0/9 0/9 0/92000 4/6 5/6 0/6 1/6 0/6 0/6 0/6 0/6 2/7 0/7 0/7 0/72001 5/7 0/7 0/7 0/7 0/7 5/7 0/7 0/7 0/8 0/8 0/8 0/82002 0/6 0/6 0/6 0/6 0/6 0/6 0/6 0/6 0/8 0/8 0/8 0/82003 0/6 0/6 0/6 0/6 0/6 0/6 0/6 0/6 0/7 0/7 0/7 0/72004 6/7 0/7 0/7 0/7 0/7 0/7 0/7 0/7 0/7 0/7 0/7 0/72005 0/6 0/6 0/6 0/6 0/6 0/6 0/6 0/6 0/9 0/9 0/9 0/92006 0/8 0/8 0/8 0/8 0/8 0/8 0/8 0/8 0/8 0/8 0/8 0/82007 0/5 0/5 0/5 0/5 0/5 0/5 0/5 0/5 0/8 0/8 0/8 0/82008 0/6 0/6 0/6 0/6 0/6 0/6 0/6 0/6 0/7 0/7 0/7 0/72009 0/7 0/7 0/7 0/7 0/7 0/7 0/7 0/7 0/7 0/7 0/7 0/72010 0/7 0/7 0/7 0/7 0/7 0/7 0/7 0/7 0/8 0/8 0/8 0/82011 0/6 0/6 0/6 0/6 0/6 0/6 0/6 0/6 0/7 0/7 0/7 0/7

Table 1. Data set indicate presence of individuals in the three stations during period 1994-2011. Each specimen is represented by an alpha-numerical code (for example MFC1) where: the first letter indicate sex (M = male, F = female); seconds two letters indicate station (FC = Fonte Canali; FP = Fonte dei Poveri; LP = La Pilina); at the end there is a consecutive number. For example, MFC1 indicate the first specimen recorded at Fonte Canali, a male. Fractions indicate, for each year and for each specimen, total number of presences versus total number of visits. For example, in 1994, the value 2/6 for specimen MFC1 mean that this individual was encountered twice over five six visits. Breeding activity is also indicated.

Figure 3. Bombina pachypus population trends. On y-axis total number of individuals recorded in the stations during each monitoring year is reported.

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m a.s.l.) is represented by two cement pools (2×1.2×1m) each), exactly in front of Podere “Casa Rosa”, in the dirt road that cross the chestnut woodland. The presence of T. carnifex, B. bufo, P. bergeri and B. pachypus was recorded on this locality. At La Pili-na (43.087485° N, 10.982529° E, 569 m a.s.l.), are two temporary pools of natural origin (2.4×1.9×0.8m and 1.8×1.6×0.6m) and a cement tank (0.8×0.8×1m). The mentioned water-bodies collect rainwater and are used for irrigation and are tipically inhabited by T. carnifex, L. vulgaris, B. pachypus, P. bergeri, B. bufo and R. dalmatina. Pools in La Pilina are located inside a private vegetab-le garden, surrounded by shrubberies (Rubus sp., Erica scoparia, Genista sp., Crataegus monogyna) and Robinia pseudacacia. Si-milar environments are inhabited by B. pachypus even in other Italian areas during the spring and the summer, while the species overwinters outside the water but not far from the reproductive sites (Mattoccia et al., 2006; Arillo et al., 2009; Basile, 2011).

Survey methodsThe three study areas were visited at least once a month between April and September every year from 1994 to 2011. The num-ber of sighted individuals has been reported. We used a common fishing-net to capture Apennine yellow-bellied toads and we detected individuals by recognizing them through their ventral pattern. Sexes were easily distinguished as reported in Lanza (1983). Ventral patterns were drawn on a paper with a pencil, to allow individual recognition (Di Cerbo and Biancardi, 2010) year by year (Fig. 2).

Results

In table 1 we summarize the number of B. pachypus detected between 1994 and 2011 in the three sites and figure 3 illustrates the trends of the three subpopulations.

Sex-ratio, where individuals were more than two, turned out to be slightly unbalanced in favor of males, as already reported by Colliva et al. (2006). An adult male in Fonte dei Poveri disappeared for 4 years (1998-2001), for re-appearing (alone) in 2002; another male did the same in Fonte Canali, but just for two years. The letter has now been observed for ten years (1994-2004) in the same pond. Every year we observed breeding, both eggs and tadpoles were found in all the locations, while neo-metamorphosed individuals were detected just in Fonte Canali, in 1997 (n = 3) and 1998 (n = 4, and another one dead in the road, 50 m South to the ponds).

Discussion

Though recorded mainly in hilly area for Tuscany, B. pachypus is not reported for the pSCI “Poggi di Prata” (Corti et al., 1991; Vanni and Nistri 2006), and just one few occurrencies are recorded for this species after 1985 in the province of Grosseto (Favilli, 2001; Vanni and Nistri, 2006). No published works report this species

to be present in the pSCI “Poggi di Prata” (Grosseto, Southern Tuscany: Regione Toscana, 1995; Melini, 2005), where the species was detected at least until 2004, maybe because of the small number of individuals or because of the location of the ponds, surrounded by thick shrubwoods (Rubus sp., Crataegus monogyna). Long-term survey and detailed knowledge of the study area lead us to exclude the possibility that there are not surveyed sites in the same pSCI, so that all the areas of occurrency for this species has been detected for sure. The same adult individuals have been observed for long periods. A similar situation has been observed in the province of Bologna where small populations were driven to extinction by B. dendrobatidis infections and drying up of the pools (Stagni et al., 2004). In Fonte Canali, one adult male has been seen from 1994 to 2004: the major longevity reported in literature for this species is 16 years (Guarino et al., 1995). The species disappeared almost simultaneously from all the three analyzed stations, for unknown reasons.

Bombina pachypus is locally vanishing from many areas in Central Italy (Bulgarini et al., 1998; Andreone and Luiselli, 2000; Sarrocco and Bologna, 2000; Angelini et al., 2004; Piazzini, Favilli and Manganelli, 2005; Stagni et al., 2004; Vanni and Nistri, 2006), due to different causes, including habitat loss and fragmentation, small population sizes, competition with introduced fishes and diseases. Macroscopic environmental features (vegetal cover, summer mean temperatures, average year rainfall, water levels in the ponds, etc) in the whole study area remained almost the same in these 17 years; even in 2003, when we detected the hottest summer temperatures (with peaks up to 37°C), and ponds did not dry. Periods of particular drought are in facts hypothesed to be responsible for the extinction of B. pachypus populations in the Northern Apennine (Stagni et al., 2004). However, ponds in La Pilina were systematically cleaned every year, even when the species was present, and so we exclude that such operations could have cause this dramatic disappearance.

The small number of individuals detected suggests that this population might not have been viable since 1994. Usually, yellow-bellied toads tend to remain near their breeding sites (Venchi et al., 2002), although a dispersal distance of 190 m and 150 m for males and females has been recorded in individuals of B. variegata in Austria (Gollman et al., 2000): however, the three detected reproductive sites in pSCI “Poggi di Prata” are too distant from each other to allow toads to

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migrate. Hartel (2008) documented many continuous movements of B. variegata between ponds, also favored by the rains: these movements would not be possible in the study area, because of the isolation and remoteness of drinking troughs where the species was found. In addition, newly-metamorphosed individuals could turn back in breeding sites after 4-5 years on the mainland (Hartel, 2008). Anyway, their absence in the study area since 2003 seems to militate in favor of the high juvenile mortality observed in this species (Hartel, 2008).

Endemic status and vulnerability of B. pachypus deserve peculiar attention throughout the entire Italian peninsula, in particular for what concerns the conservation of breeding sites and the connectivity between ponds characterized by the presence of this species. Data collected during this survey will be useful for comparison with future data in a research applied to the conservation of the species. An inter-regional coordination would be desirable to develop an action plan to indicate both the health status of each population and the conservation strategies to be prepared on a national scale.

References

Allendorf, F.W., Luikart, G. (2007): Conservation and the Gene-tics of Populations. Blackwell Publishing, Malden, Massachu-setts, USA.

Andreone, F., Corti, C., Sindaco, R., Romano, A., Giachi, F., Van-ni, S., Delfino, G. (2008): Bombina pachypus. In: IUCN 2009. IUCN Red List of Threatened Species. Version 2009.2. www.iucnredlist.org.

Andreone, F., Luiselli, L. (2000): The Italian batrachofauna and its conservation status: a statistical assessment. Biol. Cons. 96: 197-208.

Angelini, C., Cari, B., Mattoccia, M., Romano, A. (2004): Dis-tribuzione di Bombina variegata pachypus (Bonaparte, 1838) sui Monti Lepini (Lazio) (Amphibia: Anura). Atti Soc. It. Sci.

Nat. Museo Civ. Stor. Nat. Milano 145: 321-328.Arillo, A., Braida, L., Canessa, S., Oneto, F., Ottonello, D., Rai-

neri, A. (2009): Problematiche di conservazione delle popo-lazioni di Bombina pachypus (Bonaparte, 1838) in Liguria. Bollettino dei Musei e Istituti Biologici, Genova, 71:89.

Arillo, A., Braida, L., Stefano Caness a1, Ferravante, C., Oneto, F., Ottonello, D., Salvidio, S. (2011): Azioni di salvaguardia di Bombina pachypus (Bonaparte, 1838) in Liguria,. In: “Atti 4. Convegno nazionale Salvaguardia Anfibi (Idro, 2011)”, Pia-nura, 27: 171-173.

Barbieri , F., Bernini, F., Guarino, F.M., Venchi, A. (2004). Dis-tribution and conservation status of Bombina variegata in Italy (Amphibia, Bombinatoridae). It. J. Zool. 71(1): 83-90.

Basile, M. (2011): Compilazione della Red List dei Vertebrati in Campania. Metodi e applicazioni, Tesi di Laurea in Scienze della Natura, Università degli Studi di Napoli Federico II, Fa-coltà di Scienze MM.FF.NN.

Bulgarini F., Calvario E., Fraticelli F., Petretti F., Sarrocco S. (1998): Libro rosso degli animali d’Italia- Vertebrati. WWF Italia, Roma.

Canestrelli, D., Cimmaruta, R., Costantini, V., Nascetti, G. (2006): Genetic diversity and phylogeography of the Apennine yellow bellied toad Bombina pachypus, with implications for conservation. Mol. Ecol. 15: 3741-3754.

Colliva, C., Stagni, G., Mazzotti, S., Zaccanti, F., Falconi, R. (2006): Struttura e dinamica di popolazioni di Bombina pachy-pus nell’Appennino romagnolo. Atti del 6° Congresso Nazio-nale della Societas Herpetologica Italica.

Corti, C., Nistri, A., Poggesi, M. Vanni, S. (1991): Biogeographi-cal analysis of the Tuscan herpetofauna (Central Italy). Rev. Esp. Herpet. 5: 51-75.

Di Cerbo, A.R., Biancardi, C.M. (2010): Quantitative pattern ana-lysis methodology in amphibians In: Atti VIII Congresso Nazi-onale Societas Herpetologica Italica (Chieti, 22-26 Settembre 2010). Edited by: Di Tizio L., Di Cerbo A.R., Di Francesco N. & Cameli A., Ianieri Edizioni, Pescara: 383-390.

Di Martino, V., Ferri, V. (2002): Distribuzione ed iniziative di conservazione di Bombina pachypus nel Parco Nazionale del Gran Sasso e dei Monti della Laga. Atti III Conv “Salvagu-ardia Anfibi”, Lugano 23-24 giugno 2000- Cogecstre (Eds.), Penne: 41-45.

Ellstrand, N.C., Elam D.R. (1993): Population genetic conse-quences of small population size: implication for plants con-servation. Annu. Rev. Ecol. Syst. 24: 217-242.

Favilli, L., Piazzini, S., Manganelli, G. (2001): Nuovi dati sul-la distribuzione in Toscana Meridionale di Anfibi e Rettili di interesse conservazionistico. Atti Soc. Tosc. Sci. Nat., Mem., Serie B, 108: 59-69.

Fiacchini, D. (2007). Bombina pachypus (Amphibia, Bombinato-ridae) nelle Marche: aspetti corologici, ecologici e conservazi-onistici. Biogeographia, 28.

Fromhage, L., Vences, M. & Veith, M. 2004. Testing alternative vicariance scenarios in Western Mediterranean Discoglossid frogs. Mol. Phyl. Evol. 31: 308-322.

Girardello, M., Griggio, M., Whittingham, M.J., Rushton, S.P. (2010): Models of climate associations and distributions of amphibians in Italy. Biol. Cons. 111 (3): 331-343.

Gollmann, B., Gollmann, G., Miesler, M. (2000): Habitatnutzung und Wanderungen in einer Gelbbauchunken-Population (Bom-bina v. variegata). Zeitschrift Feldherpet., 7: 1-16.

Guarino F. M., Angelini F., Cammarota M. (1995): A skeletochro-nological analysis in three syntopic species of southern Italy. Amphibia-Reptilia, 16: 197-203.

Guarino, F.M., Bellini, L., Mazzarella, G., Angelini, F. (1998): Reproductive activity of Bombina pachypus from Southern Italy. It. J. Zool., 65: 335-342.

Hartel, T. (2008): Movement activity in a Bombina variegata population from a deciduous forested landscape. NW J. Zool., 4(1): 79-90.

Hofman, S., Spolsky, C., Uzzell, T., Cogalniceanu, D., Babik, W., Szymura, J.M. (2007): Phylogeography of the fire-bellied toads Bombina: independent Pleistocene histories inferred from mitochondrial genomes. Mol. Ecol, 16(11): 2301-2316.

Local extinction of Bombina pachypus 411

Page 6: Local extinction of Bombina pachypus Bonaparte, 1838 in three

Lanza, B. (1983): Anfibi e Rettili. In: Guide Per Il Riconoscimen-to Delle Specie Animali Delle Acque Interne Italiane. CNR, Italy.

Lanza, B., Vanni, S. (1991): Notes on the biogeography of the Mediterranean islands amphibians. In: Accademia Nazionale dei Lincei (eds): International Symposium on: Biogeographi-cal Aspects of Insularity, Roma 18-22th May 1987. Atti Conv. Lincei, 85: 335-344.

Lanza, B., Corti, C. (1993): Erpetofauna italiana: acquisizioni ed estinzioni nel corso del novecento. Suppl. Ric. Biol. Selv. 21: 5-49.

Mattoccia, M., Cari, B., Romano, A., Angelini, C. (2006): Os-servazioni sull’ecologia di alcune popolazioni di Bombina pa-chypus (Amphibia: Bombinatoridae) nei Monti Lepini, Lazio. Proceedings V Congresso Nazionale della Societas Herpetolo-gica Italica: 161-166.

Melini, D. (2005): La gestione forestale nei Siti di Importanza Comunitaria. Il sito “Poggi di Prata” (Gr). L’Italia Forestale e Montana, Rivista di Politica, Economia e Tecnica, 3: 249-267.

Mirabile, M., Melleti, M., Venchi, A., Bologna, M.A. (2009): The reproduction of the Apennine yellow-bellied toad (Bombina pachypus) in central Italy. Amphibia-Reptilia 30: 303-312. Piazzini, S., Favilli, L., Manganelli, G. (2005): Atlante degli Anfibi della Provincia di Siena (1999-2004). Sistema delle Ri-serve Naturali della Provincia di Siena, Quaderni Naturalistici 1: 112.

Regione Toscana (1995): Scheda d’Identificazione sito “Poggi di Prata”. Regione Toscana, Firenze.

Romano, A., Ventre, N., De Riso, L., Pignataro, C., Spilinga, C. (2010): Amphibians of the “Cilento e Vallo di Diano” National Park (Campania, Southern Italy): updated check list, distributi-on and conservation notes. Acta Herpetol., 5(2): 233-244.

Sarrocco, S., Bologna, M.A. (2000): Bombina variegata. In: An-fibi e Rettili del Lazio (eds Bologna M.A., Capula M., Carpa-neto G.M.), Palombi editore, Italy: 38-39.

Scoccianti, C. (2004): Amphibians: threats and conservation. Ital. J. Zool., 71(1): 9-15.

Stagni, G., Dall’Olio, R., Fusini, U., Mazzotti, S., Scoccianti, C., Serra, A. (2004): Declining populations of the Apennine yel-low bellied toad Bombina pachypus in the northern Apennine (Italy): is Batrachochytrium dendrobatidis the main cause? It. J. Zool 71(2): 151-154.

Vanni, S., Nistri, A. (2006): Atlante degli Anfibi e dei Rettili della Toscana. Museo di storia naturale “La Specola”, Sezione di Zoologia. Direzione generale politiche territoriali e ambientali: 173-176.

Venchi, A., Bombi, P., Bologna, M. (2002). Dinamica metapo-polazionale di ululone appenninico nel Parco Nazionale della Majella. Abstract del IV Congr. Naz. Soc. Herpetol. Ital., Er-colano: 44.

Vaccaneo, R. (1931): Ricerche sui caratteri morfologici dei Bom-binator italiani. Boll. Museo Zool. Anat. Comp. Univ. 41(5): 1-48.

Zheng, Y.C., Fu, J.Z., Li, S.Q. (2009): Toward understanding the distribution of Laurasian frogs: A test of Savage’s biogeogra-phical hypothesis using the genus Bombina. Mol. Phyl. Evol. 52(1): 70-83.

Emiliano Mori & Alice Giovani412

Accepted by Angelica Crottini