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NORTH-WESTERN JOURNAL OF ZOOLOGY
International scientific research journal of zoology and animal ecology
of the Herpetological Club - Oradea
Univeristy of Oradea, Faculty of Sciences, Department of Biology
Univeristatii str. No.1, Oradea – 410087, Romania
Publisher: University of Oradea Publishing House
Contact e-mail: [email protected], [email protected]
NORTH – WESTERN JOURNAL OF ZOOLOGY
(International journal of zoology and animal ecology)
ACCEPTED PAPER
- Online until proofing -
Authors: Enrico LUNGHI; Rosalba MURGIA; Gianni DE FALCO; Salvatore
BUSCHETTU; Cinzia MULAS; Manuela MULARGIA; Claudia CANEDOLI; Raoul
MANENTI; Gentile Francesco FICETOLA
Title: First data on nesting ecology and behaviour in the Imperial cave salamander
Hydromantes imperialis
Journal: North-Western Journal of Zoology
Article number: 151505
Status: awaiting English spelling editing
awaiting proofing
How to cite:
Lunghi E., Murgia R., De Falco G., Buschettu S., Mulas C., Mulargia M., Canedoli
C., Manenti R., Ficetola G.F. (2015): First data on nesting ecology and behaviour in
the Imperial cave salamander Hydromantes imperialis. North-Western Journal of
Zoology 11: art.151505
Date published: <2015-05-03>
Citation as online first paper: North-western Journal of Zoology 11: art.151505
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First data on nesting ecology and behaviour in the Imperial cave salamander
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Hydromantes imperialis
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Enrico LUNGHI1, Rosalba MURGIA2,3, Gianni DE FALCO2, Salvatore BUSCHETTU2,
Cinzia MULAS4, Manuela MULARGIA5, Claudia CANEDOLI6, Raoul MANENTI7, Gentile
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Francesco FICETOLA6,8,9
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Natural Oasis, Via di Galceti 141, 59100 Prato, Italy
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Speleo Club Oristanese, Via Canepa 8, 09170 Oristano, Italy
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IMC-International Marine Centre, Torregrande, 09170 Oristano, Italy
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Gruppo Grotte Ogliastra, Via Pascoli snc, 08046 Perdasdefogu, Italy
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Speleo Club Nuoro, Via Tunisi 3, 08100 Nuoro, Italy
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Dipartimento di Scienze dell’Ambiente e del Territorio e di Scienze della Terra, Università degli
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Studi di Milano-Bicocca, Piazza della Scienza 1, 20126 Milano, Italy
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Dipartimento di Bioscienze, Università degli Studi di Milano, Via Celoria 26, 20133 Milano, Italy
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Laboratoire d’Ecologie Alpine (LECA), Université Grenoble-Alpes, F-38000 Grenoble, France
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CNRS, LECA, F-38000 Grenoble, France
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Corresponding author: Enrico Lunghi, [email protected]
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Abstract
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During the dry season, the European Plethodontid salamanders (genus Hydromantes) usually
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occupy underground environments (i.e. caves), where they can find cold temperatures and
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high moisture. Hydromantes breed in hypogean environments, where they usually lay eggs in
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hidden shelters. Mothers perform a long-lasting parental care of the eggs, which continue also
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after hatching. Due to the cryptic habitat and behaviour, their breeding biology is poorly
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known. Most of available data refer to observations in captivity, while data from wild
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populations are scarce and deal with the findings of single nests. Here we report the first study
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on the Imperial cave salamander H. imperialis nesting ecology and behaviour, by performing
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quantitative observations on multiple nests. We found four nests in a cave located in Central
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Sardinia. We monitored them through five months, recording environmental features. Nests
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were associated to cold, humid and dark sectors of the cave, but sectors with nests did not
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show more climatic stability than the superficial ones. Nests were continuously attended by
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females; females left more frequently the nests unattended when temperatures are high and
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later in the season. Newborns were attended by the mothers up to 52 days after hatch. The
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comparison of breeding biology across multiple Hydromantes species suggests earlier hatch in
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population/species living in warmer areas, with similar post-hatch brood attendance among
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species.
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Key-words: Microclimate, temperature, humidity, parental cares, brood attendance, cave
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fauna, amphibians
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Running title: Multiple nesting of Hydromantes imperialis
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Introduction
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Cave salamanders of the genus Hydromantes Gistel, 1848 are fully terrestrial and lay eggs in
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sub-aerial environments (Lanza et al. 2006). Such features force these salamanders to live and
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reproduce in environments with specific microclimate, such as cold temperature and high
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moisture (Ficetola et al. 2012, Lunghi et al. 2014a). In Europe there are eight species of
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Hydromantes, five of which are endemic to Sardinia (Sillero et al. 2014). Seven of these
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species belong to the sub-genus Speleomantes, while one species belongs to the sub-genus
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Atylodes (Wake 2013). In Mediterranean areas, cave salamanders can exploit both epigean
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and hypogean environments; however outdoor environments are avoided during hottest and
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driest seasons (Cimmaruta et al. 1999, Lanza et al. 2006). On the other hand, hypogean
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environments represent a shelter in which Hydromantes can find suitable microclimatic
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conditions even during unfavourable periods (e.g. hot and dry summers) (Salvidio et al. 1994,
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Vignoli et al. 2008, Ficetola et al. 2012, Lunghi et al. 2014a). In these habitats, Hydromantes
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select the most appropriate zone to breed and to perform their long-lasting eggs care (Stefani
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& Serra 1966, Papinuto 2005, Lunghi et al. 2014b). Until few years ago the knowledge on the
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reproduction of these salamanders was quite scarce (Lanza et al. 2006). Recent studies
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performed both in natural and semi-natural conditions improved our understanding of their
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reproductive biology, and showed the complexity of parental cares in these salamanders
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(Stefani & Serra 1966, Papinuto 2005, Lanza et al. 2006, Oneto et al. 2010, Oneto et al. 2013,
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Lunghi et al. 2014b, Oneto et al. 2014). Observations in both natural and controlled
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environments can be useful to understand the breeding behaviour of these salamanders. Oneto
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et al. (2010, 2014) recently studied the parental cares of H. strinatii, by performing
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observations on individuals under semi-natural conditions. H. strinatii females attended nest
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constantly, keeping their body in touch with eggs (Oneto et al. 2010). During eggs care,
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mother moved rarely from the nest; however temporary desertion of the nest became more
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frequent after all eggs were hatched (Oneto et al. 2010). Posthatching parental care lasted six
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weeks, during which newborns tried to keep their body in touch with the mother as much as
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they could. During this time, only mothers moved occasionally away from the nest, and
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females actively defended the broods against conspecific intruders (Oneto et al. 2014).
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However, observations performed in wild conditions, and on a wider range of species, are
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needed to assess the generality of results obtained under controlled conditions. Until now,
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information on the breeding behaviour of Hydromantes in nature was extremely limited and
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available for three species only. Papinuto (2005) observed a clutch of H. genei in an
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abandoned mine, and observed that mother stayed constantly close to eggs, moving away
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from the nest rarely and only for a short time. Newborns left definitively the nest after two
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weeks. Lunghi et al. (2014b) reported two observations: a clutch of H. flavus in a deep zone
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of a cave system and a clutch of H. italicus in an abandoned mine. In these species, the
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mothers were never observed far from the nest, and post-hatch parental cares lasted from one
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week to one month, in H. flavus and H. italicus, respectively. However, due to the difficulty
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of accessibility and finding cave salamander nests, all the studies from natural environments
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reported observations on single nests, without possibilities to compare the nesting behaviour
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of different females of the same population, and only recorded quantitative data.
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Here we report the first study on the Imperial cave salamander H. imperialis nesting
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ecology and behaviour, by performing quantitative observations on multiple nests. First, we
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assessed whether the selection of nesting areas is related to cave environmental features.
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Specifically, we tested two non-exclusive hypotheses: i) cave sectors with eggs are
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characterized by high humidity, low light and temperature (as observed for the adults of other
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Hydromantes species (Ficetola et al. 2013)); ii) sectors with eggs have particularly stable
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microclimatic conditions(Lunghi et al. 2014b). Second, we quantitatively recorded the
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brooding behaviour of females, and evaluated whether it is related to specific microhabitat
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features (Oneto et al. 2010). In particular we assessed whether the periods in which females
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leave the nest unattended (Oneto et al. 2010) are related to specific environmental conditions.
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Methods
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Surveys were conducted during an herpetological field activity performed in a Cave located in
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Oristano District in Central Sardinia (39° 53'N, 8° 58' E). The presence of H. imperialis was
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assessed using visual encounter surveys in June 2014, following the same procedure described
by Ficetola et al. (2013). After the first observation of clutches, the site was repeatedly
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surveyed until the complete abandonment of all nests by mothers and newborns: from 15 June
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to 25 October 2014 the cave was surveyed 20 times. Eggs or brooding females were never
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touched or directly disturbed. Using a metric wheel we measured the maximum depth of the
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cave (from the entrance to the deepest point) and determined the position of each nest
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(distance from entrance and height from the ground). We also measured the height and width
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of nest’s entrance. Starting from the entrance, we divided the cave environment in 3-meters
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sectors. This size approximately corresponds to the size of Hydromantes home-ranges during
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their underground activity (Salvidio et al. 1994). In each sectors we recorded microclimatic
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parameters [air temperature, relative humidity and max/min incident light (illuminance)]
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using a EM882 multi-function Environmental Meter (PCE Instruments; minimum illuminance
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0.01 lux). Data on temperature and relative humidity was recorded 17 times through the
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whole period. As previous studies suggest that Hydromantes select cold, humid and dark
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sectors of caves (Ficetola et al. 2012, Lunghi et al. 2014a), we used one-tailed t-test to
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evaluate whether nest sites are associated to these microhabitat conditions. We used Levene’s
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test to assess whether eggs are associated to areas with particularly stable microclimate (as
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hypothesized by Lunghi et al. 2014b), by testing whether sectors in which nest were present
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have significantly variance for temperature and humidity, compared to the first sector of the
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cave (parameters recorded within the cave, 3 m from the cave entrance).
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Moreover, we used Generalized linear mixed models (GLMM) assuming binomial error
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distribution to test if mothers move away from their nest under specific microclimatic features
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or in particular periods. To analyse mother’s choice to move away from nest, we considered
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as dependent variable female attendance to the nest during each survey. As independent
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variables, we considered microclimatic conditions (temperature, relative humidity), day of
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survey, and presence of hatched eggs. Nest identity was considered as random factor. We
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used the Aikake’s Information Criterion corrected for small sample size (AICc) to identify the
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combination of variables that explains attendance/nonattendance of females to the nest
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(Stephens et al. 2007). If a model showed AICc higher than a simpler nested model, it was not
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included among the candidate models (Richards et al. 2011). We tested significance of each
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variables included into the best model (i.e. the model with lowest AICc) using a likelihood
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ratio test. Prior to perform analyses, humidity was transformed using square-root arcsine,
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while illuminance was log-transformed to better meet the assumptions of parametric analyses.
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All statistical analysis were performed in R 3.1.1 (R Development Core Team 2014).
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Results
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We found four clutches of Hydromantes imperialis during the first survey performed on 15
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June 2014. The maximum cave depth was 30 m. Nests were located in different points
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through the development of the cave, into small holes present on cave walls (Table 1). Sectors
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with nests showed significantly higher humidity (t7.03 = -2.26, P = 0.029) and lower
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illuminance (t7 = 2.05, P = 0.04) compared to sectors without nests. Furthermore, sectors with
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nests tended to have lower temperature, although this test was marginally non-significant (t8.68
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= 1.66; P = 0.067). Considering temperature, no one of the nests was located in cave sectors
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showing lower variability than the first sector of the cave (Levene’s test: all P ≥ 0.29).
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Similarly, sectors with nests did not show low variability than first sector also for humidity
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(all P ≥ 0.10).
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Clutches were composed by 7-11 eggs each, all provided with a peduncle (Figure 1).
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During the first surveys (June) eggs were transparent and the embryos inside were perfectly
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observable (Figure 2 and Figure 3a). In early July almost half yolk were absorbed and
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embryos started to have a defined shape, allowing us to recognize various morphology of this
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animals. In late July-early August embryos were filled up all the available space inside the
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eggs, making their aspect more dark and opaque (Figure 3b-c). The first newborns were
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observed on 16 August in the nest furthest from the entrance, while in the other nests the first
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newborns appeared on 25 and 28 August (Table 1; Figure 4d). Eggs from the same nest did
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not hatch contemporarily, but required up to 10 days for hatch completion (Table 1).
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During surveys mothers constantly took care of their broods, moving away from them
rarely (Table 1). The best-AIC model suggested that nests were more frequently unattended
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by mothers when temperature was higher (χ21 = 4.52, P = 0.03) and later in the season (χ21 =
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3.40, P = 0.06) (Table 2). A significant positive interaction between temperature and day of
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survey indicated that the effect of temperature was particularly important later in the season
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(χ21 = 5.10, P = 0.024).
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When nests were unattended, females changed eggs position, by moving them to the
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deepest and most hidden part of the nest-holes. After hatch, newborns followed their mother
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into and outside nests for 6-52 days (mean: 27). Some newborns sometimes explored areas
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just outside the nest, while mother remained inside nest with other part of her brood. This
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behaviour was observed 6 times, and was observed most frequently for the deepest nest: we
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found 4 times newborns salamanders outside from the fourth nest and only one time outside
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from the first and the second. On the 25 October all nests were abandoned.
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Discussion
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This study describes the first finding of multiple nests for the genus Hydromantes
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(Speleomantes) under natural conditions, by analysing the first collection of quantitative
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parameters on environmental features potentially related to nest site choice and parental care
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behaviour for the genus. Before this study, Hydromantes clutches in natural environments
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have been observed only few times (Stefani & Serra 1966, Papinuto 2005, Lunghi et al.
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2014b), while clutches of H. imperialis were only observed in captivity (Lanza et al. 2006).
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Clutches of H. imperialis were inside small holes located on cave walls, as observed by
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studies on the other species (Stefani & Serra 1966, Papinuto 2005, Lunghi et al. 2014b).
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Females look for hidden places in order to protect as much as possible their eggs (Lanza et al.
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2006, Pastorelli & Laghi 2006, Oneto et al. 2010). Normally, observed females laid their eggs
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not too close to the entrance, in areas that present suitable microclimatic features (cool
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temperature, high moisture and darkness), with a pattern of microhabitat selection similar to
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the one observed by individuals of other Hydromantes species (Ficetola et al. 2013, Lunghi et
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al. 2014a). During previous observations, females with eggs were always relatively far from
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entrance, and previous work suggested that these areas might be characterized by high
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microclimatic stability (Lunghi et al. 2014b). Females selected nest-holes relatively far from
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the entrance also in H. imperialis, and the recording of microclimatic parameters in multiple
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occasions allowed to test this hypotheses. Actually, the cave sectors selected for nesting did
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not show particularly high microclimatic stability, compared to the areas of the cave closest to
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the surface, i.e. where the highest microclimatic variability is expected (Romero 2009). This
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suggests that the microclimatic stability, that is characteristic of the whole cave environment
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(Romero 2009), is sufficient to maintain suitable microhabitat conditions during the several
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months required for eggs development (Lanza et al. 2006). To lay their eggs, females
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probably select the first suitable area of the cave (enough fresh and humid) which is at the
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same time not too far from food resources (Ficetola et al. 2013). This choice might help
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females to obtain food without distancing too much from their clutches. Females choice might
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therefore result from the trade-off between environmental features, clutch security and food
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supply.
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Clutches size was similar to the one previously reported for other species (Lanza et al.
2006). For all the nests, hatch was relatively synchronous, toward the end of Summer, like
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what was observed in all the other Hydromantes species (Papinuto 2005, Lanza et al. 2006,
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Lunghi et al. 2014b) (Table 3). End of Summer may be an extremely suitable period for
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juveniles, as it generally corresponds to the end of the dry season, and thus juveniles may
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move outside from caves, where food availability is higher. Nevertheless, across the different
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Hydromantes species, average hatch date was significantly related to the mean annual
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temperature: eggs hatched significantly earlier in populations living in warmest areas (Table
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3; linear regression, weighted for the number of clutches, between mean hatch date and mean
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annual temperature: F1,3 = 52.2, P = 0.005, R2 = 0.93). Cave temperature is strongly related to
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the mean annual outdoor temperature (Romero 2009), and in amphibians high temperature
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increases metabolism, accelerating embryo development (Morrison & Hero 2003). Overall,
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the good synchrony of hatches, with earlier hatch in the warmer localities, suggests that the
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whole breeding cycle may follow a similar seasonal pattern across the whole Hydromantes
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genus.
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Within a nest eggs hatched over a relatively long period (Table 1). Like what was
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observed for H. strinatii (Oneto et al. 2010), eggs from all 4 nests of H. imperialis never
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hatched in the same day: a single clutch require up to 10 days for let all newborns come out
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from their eggs (Figure 4d).
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Mothers take care carefully on their broods, attending and protecting them against
predators and infections (Lanza et al. 2006, Oneto et al. 2014). However, is already known
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that sometimes mothers left unattended their nest (Oneto et al. 2010). With our observation
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we could see that the mothers choice to distance for a while from their nest is related to some
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environmental features. Mothers left nest mostly when air temperature is relatively high and
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during later periods. However, before moving away from the nests, mothers replace the eggs
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in a concealed part of the nest. During our observation we always saw mothers curled on their
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eggs inside holes; however, in two circumstance, before leaving the nest, mothers hidden the
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bunch of eggs on the backside of nest walls, making extremely difficult (or impossible) their
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detection. For all species, after hatching, mothers continued to occupy the nest with newborns
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in average for one month, with strong differences among females (min 6 days, max 52 days).
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The post-hatch nest attendance overlaps what has been observed in other species (Table 3),
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suggesting a lack of interspecific divergence in post-hatching behaviour, but rather some
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variation among females, which could depend from both environmental features and physical
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status. As observed by Oneto et al. (2010) newborns never fed before leave definitively the
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nest. Time of permanence inside the nest after hatching might thus also depend from how
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long last yolk absorption of newborns (Lunghi et al. 2014b). However, differently from the
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observations performed on H. strinatii (Oneto et al. 2010), in our study newborns were more
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inclined to explore areas around the nest, even without their mother, as also reported by
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Papinuto (2005). This difference in behaviour might be due to the different environmental
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conditions (natural vs. semi-natural) which may influence the behaviour of both mother and
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newborns.
Our study adds new insights on the brooding behaviour of European cave
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salamanders; however information remains limited to a handful of species (Table 3), and for
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each species no more than one population has been investigated. Further researches,
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comparing the results of multiple nests and multiple populations will be necessary to better
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understand the complex breeding behaviour of these cryptic salamanders.
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Acknowledgments
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We are grateful to many friends that took part to this long survey: Valentina Mirimin, Sandro
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Corona, Francesca Fais, Sandro Murru, Silvestro Papinuto, Francesco Papinuto, Denise Atzei,
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Luca Buschettu, Giancarlo Cadeddu, Rita Cadeddu, Alfredo Camedda, Franca Contu,
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Gabriele Espis, Salvatore Manca, Carla Meli, Gianfranco Muzzetto, Simona Putzolu, Cristina
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Santona, Loredana Tegas. This study was allowed by the Italian Ministry of the Environment,
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out withstanding of the DPR 357/97 , Prot. 0040002.
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Sillero, N., Campos, J., Bonardi, A., Corti, C., Creemers, R., Crochet, P.-A., Isailović, J.C., Denoël, M.,
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Vignoli, L., Caldera, F. Bologna, M.A. (2008): Spatial niche of the Italian cave salamander,
Speleomantes italicus (Dunn, 1923) (Plethodontidae, Amphibia), in a subterranean system of
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Table and Figure captions
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Table 1: Position and morphology of nests and data on their occupancy: Distance (distance from
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entrance); Height (height from the ground); Size of the nest-hole (height and width of the entrance of
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nests); First born (date of first eggs hatched); All born (date when all eggs were hatched); Empty (date
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when the nest was completely uninhabited); Nest unattended (date when mother left unattended the
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nest). * The fourth nest were not checked between 14 and 26 September due to the high risk to step on
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salamanders that were covering the ground floor.
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Table 2: Candidate AIC models created using following dependent factors: Day (day of
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survey); Eggs hatch (presence of eggs hatched); Temp (air temperature); Hum (relative
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humidity); Day*T (interaction between day of survey and air temperature).
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Table 3: Mean hatch date and length of post-hatch parental cares, in different studies on
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Hydromantes nests, from natural and semi-natural environments. Mean annual temperature is
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the mean annual temperature of the outdoor environment, obtained from the world climate
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(Hijmans et al. 2005).
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Figure 1: Seven eggs provided with peduncle that drawn them close (third nest; 15 June).
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Figure 2: First nest during survey on 15 June: eggs show high transparency and embryos and
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yolk are clearly recognisable.
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Figure 3: Third nest observed in different times. A) On 23 June eggs were transparent and
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embryos in early developmental stage are detectable; B) On 9 August embryos were grow up
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and showed an advanced body-shape; C) On 17 August yolks were continuously less visible
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due to embryos development; D) First salamander born on 28 August.
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Tables
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Table 1
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1st nest
2nd nest
3rd nest
4th nest
Distance
from
Height
entrance
14.8 m 100 cm
17.6 m
50 cm
20 m
20 cm
21.7 m 150 cm
Size of the
nest-hole
First born
All
Born
Empty
Nest
unattended
2 x 2 cm
5 x 2 cm
3 x 2 cm
4 x 3 cm
28/08
25/08
28/08
16/08
3/09
3/09
7/09
25/08
25/10
20/09
13/09
27/09*
17/08
7/09
7/09
9/08
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Table 2
Day
-1.612
-0.04962
Eggs hatch
Temp
-4.615
1.0960
Hum
Day*T
0.08958
df
5
4
2
AICc
31.0
33.8
34.7
delta
0.00
2.77
3.70
weight
0.71
0.18
0.11
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Table 3
Species
Study
Mean
hatch date
Number
of clutches
Mean outdoor
temperature
H. genei
H. imperialis
H. italicus
H. flavus
H. strinatii
(Papinuto 2005)
this study
(Lunghi et al. 2014b)
(Lunghi et al. 2014b)
(Oneto et al. 2010, 2014)
31 August
24 August
11 September
26 August
6 October
1
4
1
1
3
13.7
15.0
12.0
15.9
10.2
Post-hatch
parental
cares (days)
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6-52
30
7
42
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Figures
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Figure 1
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Figure 2
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Figure 3
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