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Several species of amphibians are known to inhabit
subterranean habitats. While some species are obligatory
cave-dwelling (e.g., Proteus anguinus Laurenti, 1768),
others tend to use caves only for limited periods of their
lives (Peck, 1974; Romero, 2009). At least 17 species of
amphibians that belong to the Italian herpetofauna have
on occasion been found in caves or other underground
spaces and several of them occasionally breed in
subterranean sites. Here we provide the first evidence
of a population of yellow-bellied toads (Bombina
variegata) exploiting a subterranean habitat (Fig. 1).
The range of Bombina variegata (Linnaeus, 1758)
includes most of eastern, central, and southern Europe.
It extends from the Carpathian Mountains in the east
to France in the west and southern Italy in the south
(Gollmann et al., 1997). The species inhabits different
kinds of freshwater environments, including ephemeral
ponds, slow-moving streams, artificial basins and
troughs, and it is usually considered a heliophile species
(Bauer, 1987; Guarino et al., 1996). It is found from
sea level up to elevation 2200 m (Petrov, 2007), and
it is generally active from April–October (Bressi and
Barbieri, 2006).
During a study between April and November 2017
we monitored a population of B. variegata pachypus3
(Bonaparte, 1838), the Apennine yellow-bellied toad,
and discovered that it was exploiting subterranean
spaces in addition to its usual habitat. The study site
(Fig. 2) is located in the southern Apennine Mountains,
about 20 km NW of Salerno, at an elevation of 600
m, in an area characterized by vegetation primarily
composed of maqui and several species of oaks (e.g.,
Quercus cerris, Q. ilex). The study site is located inside
the “Lauro Mountains” Site of Community Importance.
In the monitored area there are (i) three concrete-made
artificial basins used as troughs, (ii) a large cave, and (iii)
a system of smaller caves. The largest cave measures
about 15 m at its longest point, 7 m at its widest, with
maximum ceiling height of 5 m. The cave’s floor is to
90% of its surface covered in water throughout the year.
The maximum water depth is ca. 30 cm. The cave is of
natural origin but was artificially modified in the past
for use as a water reservoir.
During our surveys, we ascertained the presence of
several specimens of B. v. pachypus inside the main
cave. We monitored the site for a total of seven times
(always during the daytime) and located individuals
of B. v. pachypus in the main cave during each visit.
Individuals observed in the smaller caves were always
impossible to be captured due to the difficulties of the
terrain. We also recorded the presence and reproductive
activity of Bufo bufo (Linnaeus, 1758) and Salamandra
salamandra (Linnaeus, 1758). Whereas there have been
reports for the presence and reproduction in hypogeous
habitat (Bonini et al., 1999; Manenti et al., 2011), this
is the first time that B. v. pachypus is reported for such
an environment.
We used a mark & recapture method in order to
understand whether individuals occurring in the main
cave were always the same individuals. Given that the
genus Bombina is characterized by an individualised
belly pattern (Delarze et al., 2000), photographing the
Herpetology Notes, volume 11: 967-969 (2018) (published online on 19 November 2018)
First record of Bombina variegata (Linnaeus, 1758)
in a cave environment
Valerio Giovanni Russo1,*, Luca Francesco Russo1, Luca Coppari2, and Tommaso Notomista1
1 Associazione Ardea, via Ventilabro 6, 80126 Naples, Italy.
2 Amphibian Evolution Lab, Vrije Universiteit Brussel, Plainlaan
2, 1050 Brussels, Belgium.
* Corresponding author. E-mail: valerio.giovanni.russo@gmail.
3 7he taxonomic position of B. v. pachypus is still subject to some
debate, with some authors considering it a full species (e.g.,
Nascetti et al., 1982; Lanza and Corti, 1993; Szymura and
Gollmann, 1996) and with others just recognising its validity
as a subspecies (Speybroeck et al., 2010).
Valerio Giovanni Russo et al.
ventral side of animals found inside and outside the
cavern allowed us to reliably identify every individual.
Individual pattern recognition is known as the least
invasive method for marking amphibians (Loafman,
1991). For photo identification we used the I3S Pattern
software (Van Tienhoven et al., 2007).
Results demonstrated that individuals found inside
the cave would subsequently be found outside and
vice versa, confirming that the cave was not working
as a trap and that specimens were able to freely move
in and out. Moreover, individual recognition allowed
us to recognize how healthy animals were. Specimens
always found in the cave showed, at least at a first sight,
good health conditions, suggesting that during their
stay in the hypogeous habitat toads are not suffering
of starvation or other issue related to the conditions
of a cave environment. We found between four and
nine specimens in the main cave. Of the 44 specimens
marked in the entire area, 17 were found at least once in
the main cave.
We do not know why this population uses the
subterranean habitat. It has been shown in other species
(e.g., Prather and Briggler, 2001) that the use of cave
spaces could be due to a need for lower temperatures and
higher levels of humidity, but it would be speculative to
Figure 1. An individual of Bombina variegata pachypus found inside one of the caves of the study site.
Figure 2. Map of Italy (A) and specific location of the Site of
Community Importance “Lauro Mountains” (dark grey area
in B). (C) The exterior of the study site where some of the
smaller caves and one of the artificial troughs are visible.
assert this here. Studies to analyse how this population
copes with the hypogeous habitat, if feeding occurs
in the cave and what prey items may be consumed, at
which stage of their life these frogs begin to use the cave
environment, if they reproduce inside it, or whether the
cave is mainly used as a refuge during colder periods,
are currently ongoing.
Our findings refute any evidence that B. v. pachypus
could be a strictly heliophilic species. Furthermore,
it is becoming clear that even for well-studied taxa,
there is still work to be done in order to more fully
understand their biology and ecology. Considering that
this subspecies may be suffering a population decline
throughout its range and is protected by national and
international legislation, improving the knowledge about
its ecology is critical for building better conservation
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First record of Bombina variegata in a cave environment 969
Accepted by Hinrich Kaiser
... Apart from the obligate cavernicole species belonging to the Proteidae and Plethodontidae families (Romero, 2009), the occurrence of amphibians in caves and other underground habitats was often documented, especially for salamanders (Sequeira et al., 2001;Manenti et al., 2009;Ianc et al., 2012) but also for some anurans (Rosa et Penado, 2013;Koller, 2017;Russo et al., 2018). Although their presence in the subterranean environment can be accidental (Niemiller and Miller, 2009), there are studies indicating the preferences of some amphibian species for specific environmental features and active selection of the cave (Lunghi et al., 2014;Lunghi et al., 2018). ...
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The common toad ( Bufo bufo ) is a widespread species in Europe, with accidental occurrence in caves. This study reports the first case of breeding of B. bufo in a natural cave in the Carpathian Mountains. The breeding activity was observed at the end of May and the beginning of June. We identified pairs of common toads in axillary amplexus, egg strings and tadpoles up to a distance of 97 m inside the cave. We hypothesized that there is an active selection of some cave sites as breeding habitat and that the egg deposition is not randomly distributed inside the cave. In 25 sample points, we recorded ten cave environmental features and we assessed the relationship between egg strings presence and environmental features by performing a bias reduction in binomial-response generalized linear model. The results revealed that the strongest ecological factor determining the selection of breeding areas inside the cave was water flow velocity. The presence of light, although an important environmental feature, was not the most determining factor in breeding site selection, as toads successfully entered in completely dark environments to lay eggs in hydrologically favourable places. This study provides new information about the cave breeding of Bufo bufo and highlights the environmental features determining the common toad’s breeding site selection.
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Research on the taxonomy of European amphibians and reptiles has increased noticeably over the last few decades, indicating the need for recognition of new species and the cancellation of others. This paper provides a critical review of recent changes and draws up a tentative species list.
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Several studies documented the presence of amphibians in caves, yet investigations on the factorsdetermining amphibian distribution and reproduction in underground environments remain scarce. In this study we analyze the environmental features allowing the reproduction of the fire salamander Salamandra salamandra in natural caves, and we compare the features of natural and artificial hypogeous springs. We performed surveys to assess salamander distribution and measured environmental variables in 61 natural caves. We recorded larval occurrence in 18% of caves, in waterbodies distant up to 50 m from the entrance. Larvae were associated to the most accessible caves, with gentle slope below the entrance, with waterbodies nearby the entrance and hosting rich macrobenthos communities. Occupied natural and artificial caves had similar environmental features. Larvae metamorphosing in caves attained larger body size than those grown under outdoor conditions. This result shows the key importance of the cave accessibility also for natural caves and confirms the S. salamandra ability to breed in underground damp biotopes if placed in a suitable environmental context. However, frequent water catchments for human use prevent the access of animals and threaten these populations.
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The ability to identify individual animals is a critical aid in wildlife and conservation studies requiring information on behaviour, distribution, habitat use, population and life‐history parameters. We present a computer‐aided photo‐identification technique that relies on natural marks to identify individuals of Carcharias taurus , a shark species that is critically endangered off the eastern Australian coast and considered globally vulnerable. The technique could potentially be applied to a range of species of similar form and bearing natural marks. The use of natural marks for photo‐identification is a non‐invasive technique for identifying individual animals. As photo‐identification databases grow larger, and their implementation spans several years, the historically used visual‐matching processes lose accuracy and speed. A computerized pattern‐matching system that requires initial user interaction to select the key features aids researchers by considerably reducing the time needed for identification of individuals. Our method uses a two‐dimensional affine transformation to compare two individuals in a commonly defined reference space. The methodology was developed using a database of 221 individually identifiable sharks that were photographically marked and rephotographed over 9 years, demonstrating both the efficacy of the technique and that the natural pigment marks of C. taurus are a reliable means of tracking individuals over several years. Synthesis and applications. The identification of individual animals that are naturally marked with spots or similar patterns is achieved with an interactive pattern‐matching system that uses an affine transformation to compare selected points in a single‐user computer‐aided interface. Our technique has been used successfully on C. taurus and we believe the methodology can be applied to other species of a similar form that have natural marks or patterns. The identification of individuals allows accurate tracking of their movements and distribution, and contributes to better population estimates for improved wildlife management and conservation planning.
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The geographical position, mild climate, mountainous landscape, and habitat heterogeneity determine Bulgaria’s rich diversity of herpetofauna. Currently, 17 species of amphibians (20 subspecies) and 36 species of reptiles (45 subspecies) are known from Bulgaria. Due to its transitional position, Bulgaria lies at the southern or northern distribution limits of many species of amphibians and reptiles. Vertical distribution is presented for all species found in Bulgaria. The richest in terms of diversity and abundance are the areas below 400 m, where nearly 95% of taxa occur. The geographical ranges of almost all amphibians and reptiles in Bulgaria are well-known, although on a local scale the information is often limited. Zoogeographical analysis demonstrates that amphibian species belong to nine chorotypes, of which the Eastern Mediterranean and the European chorotypes are represented with three species each. Out of the ten chorotypes recognized for the reptiles, 51.4% of the species belong to the Eastern Mediterranean (25.7%) and Turanian–Mediterranean (25.7%) chorotypes. Only two subspecies are Bulgarian endemics (Salamandra salamandra beschkovi and Mediodactylus kotschyi rumelicus). Due to the high diversity and mosaic distribution of habitats in Bulgaria, the herpetofauna has a rather continuous occurrence and high relative abundance. Although 80% of the Bulgarian herpetofauna is legally protected by the Biodiversity Protection Act (2002) and other conventions, some species are threatened through collection for trade or habitat changes due to construction. Several sites in the southern part of Bulgaria are very rich in herpetofauna (nine to ten species of amphibians and 19 to 21 species of reptiles)
Identification individuelle de crapauds sonneurs (Bombina variegata, Anura)
  • R Delarze
  • J Pellet
  • F Ciardo
Delarze, R., Pellet, J., Ciardo, F. (2000): Identification individuelle de crapauds sonneurs (Bombina variegata, Anura). Bulletin de la Murithienne 118: 83-86.
Erpetofauna: acquisizioni ed estinzione nel corso del Novecento. Supplemento alle ricerche di
  • B Lanza
  • C Corti
Lanza, B., Corti, C. (1993): Erpetofauna: acquisizioni ed estinzione nel corso del Novecento. Supplemento alle ricerche di Biologia della Selvaggina 21: 5-49.
Identifying individual spotted salamanders by spot pattern
  • P Loafman
Loafman, P. (1991): Identifying individual spotted salamanders by spot pattern. Herpetological Review 22: 91-92.
Variabilità e divergenza genetica in popolazioni italiane del genere Bombina (Amphibia, Discoglossidae)
  • G Nascetti
  • S Vanni
  • L Bullini
  • B Lanza
Nascetti, G., Vanni, S., Bullini, L., Lanza, B. (1982): Variabilità e divergenza genetica in popolazioni italiane del genere Bombina (Amphibia, Discoglossidae). Bollettino Zoologico (Padova) 49: 134-135.