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Ecology of a Speleomantes ambrosii population inhabiting an artificial tunnel

Authors:
  • Museo Civico di Storia Naturale

Abstract

A Speleomantes ambrosii population living in an artificial tunnel in NW Italy was studied for two consecutive years. Activity on the walls varied cyclically in relation to seasonal temperatures and food abundance. The main food item was the trogloxenic dipteran Limonia nubeculosa, which accounted for more than 80% of the total ingested prey by volume. Juvenile cave salamanders had a broader trophic nich than adults. Oviposition and juvenile recruitment appeared to be seasonal. The spatial distribution inside the tunnel was related to microhabitat heterogeneity and particularly to the distance from the entrance. Juveniles were observed outside or close to the entrance more often than adults. Movement of adult salamanders were generally low and averaged 7 cm/day; some repeatedly recaptured individuals had a mean home range of 6 m2.
... Our aim was to assess whether the salamander population dynamics were in some way showing a significant change over the study period, or whether the underground environment was efficiently buffering the effects of the local external climate. This salamander population has been monitored continuously since 1990 by using a relative index of activity and since 1996 by estimating its total abundance and demographic structure (Salvidio et al. 1994(Salvidio et al. , 2016(Salvidio et al. , 2020. ...
... The study site is an artificial cave situated at 369 m a.s.l. in the municipality of Savignone (Province of Genova, Liguria, northwestern Italy). Salamanders were sampled inside the Biospeleological Station ''Arturo Issel,'' previously known as Biospeleological Station of San Bartolomeo di Besolagno (Salvidio et al. 1994). This site is situated at an air distance of approximately 17 km from the Ligurian Sea and 4 km from the border between the regions of Liguria and Piedmont ( Fig. 1a,b). ...
... Issel'' and was equipped to become an underground laboratory dedicated to the ecological study of cave salamanders. The remaining entrance was closed by an iron gate, and the tunnel's walls were equipped with air thermometers, a psychrometer, and a permanent grid from the entrance up to 21 m inside the cave, with 1 3 1 m mesh to allow the analysis of the spatial distribution of the resident population (Salvidio et al. 1994;Salvidio and Pastorino 2002). The presence of a cave salamander population colonizing this underground environment was recorded at least since summer 1972 (Pastorino and Pedemonte 1974). ...
Article
Long-term effects of current climate on animal populations living in subterranean habitats are still poorly understood. In this study, we analyzed the variability of the demographic structure and abundance of a population of terrestrial plethodontid Strinati's Cave Salamanders (Speleomantes strinatii) (Aellen, 1958) living inside a northwestern Italian artificial cave over 27 yr from 1996 to 2022. The study site is situated in the Northern Apennines, where average air temperatures measured at two local weather stations were steadily increasing, whereas precipitation was relatively constant over the past 60 yr. Our objective was to evaluate whether the demographic traits of the population of Strinati's Cave Salamanders were showing detectable signs of directional shift during the 27 yr. Each year in July, the population abundance was estimated by a three-occasion removal experiment, salamanders' snout-vent length (SVL) was measured, and the population polymodal body-size distribution was decomposed into estimated age classes. The annual population abundance, adult sex ratio, recruitment, SVL, and growth increments of first-and second-year immature salamanders were analyzed. The Strinati's Cave Salamander time series was modeled by autoregressive moving average (ARMA) analysis, and demographic parameters were tested for temporal trends. There were no directional trends observed in any of the demographic parameters of the focal cave salamander population over the study period. The best autoregressive model describing the population variation was an ARMA (2,1). Results indicated that the salamander population had a complex fluctuating pattern in which the interaction of lagged density dependence and an external autocorrelated factor were influencing the population long-term dynamics. Our findings suggest that the population of this long-lived salamander species was probably buffered from external conditions by the thermal inertia of its subterranean habitat that is known to delay and reduce the amplitude of aboveground climatic signals.
... Our aim was to assess whether the salamander population dynamics were in some way showing a significant change over the study period, or whether the underground environment was efficiently buffering the effects of the local external climate. This salamander population has been monitored continuously since 1990 by using a relative index of activity and since 1996 by estimating its total abundance and demographic structure (Salvidio et al. 1994(Salvidio et al. , 2016(Salvidio et al. , 2020. ...
... The study site is an artificial cave situated at 369 m a.s.l. in the municipality of Savignone (Province of Genova, Liguria, northwestern Italy). Salamanders were sampled inside the Biospeleological Station ''Arturo Issel,'' previously known as Biospeleological Station of San Bartolomeo di Besolagno (Salvidio et al. 1994). This site is situated at an air distance of approximately 17 km from the Ligurian Sea and 4 km from the border between the regions of Liguria and Piedmont ( Fig. 1a,b). ...
... Issel'' and was equipped to become an underground laboratory dedicated to the ecological study of cave salamanders. The remaining entrance was closed by an iron gate, and the tunnel's walls were equipped with air thermometers, a psychrometer, and a permanent grid from the entrance up to 21 m inside the cave, with 1 3 1 m mesh to allow the analysis of the spatial distribution of the resident population (Salvidio et al. 1994;Salvidio and Pastorino 2002). The presence of a cave salamander population colonizing this underground environment was recorded at least since summer 1972 (Pastorino and Pedemonte 1974). ...
... Secondly, as facultative cave-dwellers (so-called troglophiles; Howarth and Moldovan 2018), Speleomantes often forage on the surface, where prey is more abundant Culver and Pipan 2019). Climate change may reduce prey availability in both surface and subterranean habitats, confining salamanders to deep, resource-poor spaces (Salvidio et al. 1994;. ...
... A few artificial springs may serve as subterranean refugia for a specific population; nonetheless, a decline in the abundance of this population has been already detected over the past few years (Cogoni et al. 2023). Given the lacking access to caves due to the surrounding granitic terrain, any climate change-induced reduction in surface suitability will have a direct impact on this species, as it cannot retreat to subterranean habitats hosting more stable conditions (Salvidio et al. 1994;). ...
Article
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Aim: Amphibians are particularly sensitive to rapid climatic shifts, due to their eco-physiology, life history traits and high frequency of narrowly distributed species. The genus Speleomantes encompasses the only extant Western Palearctic plethodontids, with three species occurring in peninsular Italy and the remaining five endemic to Sardinia Island. Given the restricted ranges of Speleomantes species and their vulnerability to environmental change, we implemented Ecological Niche Models (ENMs) to estimate the likely impacts of various global warming scenarios on the extent and geographical location of climatically suitable areas. Time Period: Current, with ENMs projected to 2030, 2050 and 2070 under alternative Shared Socioeconomic Pathways. Location: Italian Peninsula and Sardinia Island. Major Taxa Studied: Speleomantes Dubois 1984 (Caudata: Plethodontidae). Methods: Ensembles of ENMs were fitted for each Speleomantes species, using the 'biomod2' modelling platform in R environment. Then, post-modelling analyses were applied in GIS environment to highlight: (i) the primary geographic direction of predicted suitability shifts for each species and (ii) the proportion of stable, gained and lost suitable areas for each genetic lineage of the single species. Results: We found a noticeable shrinking of suitable areas for all Speleomantes species, being particularly extensive under 'business-as-usual' scenarios for the Sardinian ones. Moreover, core suitable areas were predicted to shift for most species and suitability losses emerged to differently affect distinct genetic lineages, posing additional challenges for designing effective conservation measures. Main Conclusions: The predicted shrinkage and shifting of climatically suitable areas for most Speleomantes species point to the urgency of evaluating in due time alternative conservation strategies for these endemic urodeles, to prevent losses of taxonomic and genetic diversity. Our modelling framework may be applied to other species with similar traits (e.g., low dispersal ability and narrow environmental niche breadth) to predict climate-induced range contractions or shifts, using the gained information to optimise conservation outcomes.
... The life history of this species together with all the other species in the genus Speleomantes was described by Lanza et al. (2006), while its behavioural ecology has been recently reviewed by Costa et al. (2023). The study took place inside the Biospeleological Station "Arturo Issel" a subterranean tunnel in the municipality of Savignone (province of Genova), used as an air shelter during WWII (Salvidio et al., 1994). This subterranean site has been colonized by cave salamanders since at least 1972 (Pastorino and Pedemonte, 1974), and has been equipped with a permanent 1 × 1 m square grid to study the spatial distribution of the resident salamander population (Salvidio et al., 2020). ...
... The grid has a total of 210 squares, placed on the walls of the cave, which is 42 meters long. In this site, the salamander abundance and population demographic structure has been continuously monitored from 1996 until today (Salvidio et al., 1994;Costa et al., in press). In July 2021, salamander boldness was assessed by measuring the time of emergence from a shelter located in an unfamiliar environment. ...
Article
Boldness is a personality trait defined as the propensity of an animal to engage in risk-taking behaviours. Boldness is often associated with social ranking, dispersal, movement, and home range in many animal species. In this study we tested if boldness was correlated with individual spatial behaviour, in a population of the Cave Salamander Speleomantes strinatii living in a subterranean habitat. Boldness was measured in a controlled environment by means of an emerging from a shelter trial, while home ranges and distances moved over two years were obtained in the wild from a spatially explicit capture-mark-recapture study. We obtained data from 13 salamanders that were captured at least 5 times (mean 7.23; range 5-11). As expected, there was a highly significant and negative correlation between individual risk taking behaviour and home range overlap with conspecifics (r s = 0.84; p = 0.005). This pattern could be explained by differences in habitat physical quality or in its available resources, but more research is needed to better understand this behavioural pattern.
... All individuals were sexually mature adults with a SVL > 52 mm to reduce possible effects of ontology on the outcomes of the experiment. Salamanders were housed singularly for 72 hr before the experiments, in 50 mL tubes with a perforated cap and lined with humid paper in complete darkness, at constant temperature (9 and 11 °C in autumn and spring, respectively) and constant air humidity (~ 100%), inside the Biospelological Station "Arturo Issel", an artificial tunnel naturally colonized by cave salamanders and used as a subterranean laboratory (Salvidio et al. 1994(Salvidio et al. , 2021. In this way, we ensured that salamanders' stomachs were empty before the experiment. ...
Article
Behavioral adaptation is one of the first responses put in play by individuals to buffer environmental variations and to maintain homeostatic equilibrium with their environment. Microhabitat selection is pivotal for maximizing fitness, survival and reproduction, but how individuals process and exploit information acquired from the environment to make future microhabitat choice is yet understudied. In this study, we used outdoor mesocosms in which we introduced Strinati's cave salamanders (Speleomantes strinatii), to assess their behavioral patterns of shelter site fidelity. In each mesocosm three microhabitats were available to the salamanders: the leaf litter, a log and a rock. A total of 22 salamanders were tested over an 8-day period, 11 in autumn and 11 in spring. Salamanders shelter site fidelity was driven by both micro-habitat humidity and previous experience obtained in the mesocosm. In our experiment , the time spent in the mesocosm was the main factor influencing shelter site fidelity, suggesting that previous experience and familiarity are important in salaman-ders' behavioral adaptation. Therefore, cave salamanders are capable of learning from experience when selecting their shelters, a behavior that could also be relevant during migration, colonization of new environments and adaptation to climate change.
... Plethodontids could display behavioral thermoregulation within the range of ambient temperatures, in order to control their body temperatures in response to internal and environmental cues (Spotila, 1972;Feder, 1982). Contrary to our findings, in underground environments S. strinatii shows a clear age-class segregation (Salvidio et al., 1994;Ficetola et al., 2013;Salvidio et al., 2020). Juvenile salamanders concentrate near the entrance of the cave and occupy the twilight zone, displaying an aggregate distribution (Salvidio and Pastorino, 2002), while subadults and adults disperse in the inner cave, where absence of light is permanent and climatic conditions are more stable, daily and seasonally (Ficetola et al., 2013;Salvidio et al., 2020). ...
Article
Full-text available
Spatial distribution of animals is affected by environmental and social factors, acting both at inter- and intraspecific levels, and generating patterns of segregation or aggregation. Several studies investigated age-class segregation of the European Cave Salamander Speleomantes strinatii, in underground environments, showing a clear spatial segregation. We investigated the spatial distribution of S. strinatii on the forest floor, on 111 plots surveyed three times/season for two consecutive seasons, in northern Italy during autumn 2017 and spring 2018. We analyzed count data to model co-abundance of adults and juveniles, using a conditional two-species N-mixture model, incorporating environmental covariates. In contrast with what was observed in underground environments, we recorded no spatial segregation between juvenile and adult of S. strinatii on the forest floor. Instead, we found that adults and juveniles showed different responses to environmental features.
... All experiments were performed inside the Biospeleological Station of S. Bartolomeo di Besolagno, an artificial underground tunnel excavated in the municipality of Savignone (province of Genova) and used as an air shelter during WWII (Salvidio et al., 1994). This artificial cave has been naturally colonized by cave salamanders at least since 1972 (Pastorino and Pedemonte, 1974), and the abundance and demographic structure of the resident population has been annually analysed by temporary removal sampling since 1996 (Salvidio and Pastorino, 2002;Salvidio et al., 2020). ...
Article
Full-text available
Animal personality is a relatively neglected field in amphibian research. In this study we assessed the influence of stomach flushing, a non-lethal technique used in amphibian dietary studies, on the boldness behaviour of the cave salamander Speleomantes strinatii. The time of emergence from a shelter located in an unfamiliar environment (a proxy for individual boldness) was measured in 26 cave salamanders before and after stomach flushing, while 14 non-flushed salamanders were tested as controls. Boldness was a repeatable behaviour for salamanders and larger individuals emerged from their shelter more rapidly than smaller ones. Linear mixed model analysis showed that flushing, sex and body condition had no effect on this behaviour. These findings are promising in the framework of the study of salamander personality. In particular, our results will be useful when exploring the relationship between individual trophic strategy and boldness, aggression or exploration behaviours in terrestrial salamanders.
... Strinati's cave salamander is a fully terrestrial, long-lived, plethodontid found in southern France and northwestern Italy (Lanza 2007). It usually inhabits forest litter and humid rockfaces along stream banks, but it also establishes stable populations in underground habitats (Salvidio et al. 1994). The Northern spectacled salamander is a biphasic salamander, endemic to central and northern Italy (Romano et al. 2009). ...
Article
Ecological networks, usually depicting interactions among species, have been recently down‐scaled to the individual level, permitting description of patterns of inter‐individual resource variation, that are usually hindered at the species level. Optimal diet theory (ODT) models, applied to prey‐predator systems, predict different patterns of nestedness and modularity in the network, depending on the available resources and intra‐specific competition. The effect of resource availability on the emergence of networks structures, and ODT framework, has not yet fully been clarified. Here we analyzed the structural patterns of individual‐resource networks in three species of Mediterranean salamanders, in relation to changes in prey availability. We used weighted individual‐resource network metrics to interpret the observed patterns, according to three ODT models. We found significant nestedness recurring in our study system, indicating that both selective and opportunistic individuals occur in the same population. Prey diversity, rather than abundance, was apparently related to inter‐individual resource variation and promoted the emergence of significant modularity within all networks. The observed patterns of nestedness and modularity, together with the variation in resource diversity and intra‐specific competition, is in agreement with the distinct preferences model of ODT. These findings suggest that in the focal prey‐predator systems, individuals were able to perceive changes in prey diversity and to exploit in different ways the variations in composition of available resources, shifting their diet assembly rules accordingly. Our findings also confirm that the use of weighted individual‐resource networks, in prey‐predator systems, allows to disclose dynamics that are masked at the species or population level. https://onlinelibrary.wiley.com/share/author/IQBWGVIRVX5PIPUIRYTF?target=10.1111/1749-4877.12520
... The first cave (Cave 1) is the experimental Biospeleological Station of S. Bartolomeo (Municipality of Savignone, Province of Genova, Liguria). In this site a permanent square grid (with a 1-m mesh) of nylon wires is present on cave walls, and is set up from the entrance to 21 m deep (Salvidio et al. 1994). The second cave (Cave 2) is located at about 10 km from the first one, in the municipality of Isola del Cantone (Province of Genova, Liguria). ...
Article
Full-text available
Information on population abundance is important to correctly plan conservation and management of animal populations. In general, capture-mark-recapture (CMR) is considered the most robust technique to estimate population abundance, but it is costly in terms of time and effort. Recently, binomial N-mixture models, based on counts of unmarked individuals, have been widely employed to estimate abundance. These models have limits and their reliability has been criticized. In the majority of cases, multinomial N-mixture models based on multiple observer protocols, that are hierarchical extensions of simple CMR, are applied in estimating abundance of animals with large body size, conspicuous behavior or high detection probabilities. We applied and evaluated the reliability of a multinomial N-mixture modelling approach with multiple observer data to a small and cryptic terrestrial salamander, found in different habitats where populations possess different level of detectability. Estimates obtained with multinomial N-mixture models were compared to estimates obtained with classical methods, such as removal sampling, and their reliability has also been evaluated by simulations scenarios. Our results show that multinomial N-mixture models, applied within a multiple observer framework, give reliable and robust estimates of population abundance even when detection and density are relatively low. Therefore, multinomial N-mixture models appear efficient and cost-effective when planning and identifying management actions and conservation programs of small terrestrial animals such as amphibians and reptiles.
Article
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We here present the first study on the consumed prey by an epigean population of the Italian cave salamander (Speleomantes italicus) from the Republic of San Marino. Using the harmless technique of stomach flushing, we aimed to provide the first data on the diet and on the degree of individual specialization that characterizes the studied population. We performed two-night surveys (one in autumn 2022 and one in spring 2023) in which we opportunistically searched for salamanders in forested areas and dry walls. Captured salamanders were sexed, weighed, photographed, measured and stomach flushed. Overall, we inspected the stomach contents of 67 individuals, recognizing 1,018 prey items belonging to 28 different prey categories. The examined population was mainly composed by generalist individuals, and no differences in number and diversity of prey consumed were observed among salamanders. Contrarily to what has been observed in other Speleomantes species, flying prey provided a minor contribution to the diet of the investigated population. Our study produced the first information on the diet of Speleomantes italicus from the Republic of San Marino, representing the starting point for future assessments on the dietary habits of this specific population.
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