Raoul Manenti

Water, stream morphology and landscape: complex habitat determinants for the fire salamander Salamandra salamandra

Understanding the relationship between environmental features and species distribution is a key step for successful habitat conservation. In semiaquatic amphibians, the features of both breeding sites and the surrounding upland habitat can play important roles. We evaluated the relative role of (1) stream morphology, (2) biotic features of water, and (3) composition of landscape surrounding wetlands, for the distribution of the fire salamander, Salamandra salamandra. We determined the presence of larvae in 132 localities, and we used an information-theoretic approach to build species distribution models. We then used variance partitioning to evaluate the relative importance of environmental variables. A model including both stream and landscape features explained a large proportion of variation. Larvae were associated to heterogeneous and shallow streams, with scarce periphyton, rich macrobenthos communities characteristic of oligotrophic water, and surrounded by woodlands. Variance partitioning showed that stream morphology was the parameter with the largest independent effect, but most of variation was explained by the combined effect of multiple variables, suggesting a strong interplay among biotic and abiotic features in determining species distribution. The complementation between multiple elements, such as wetlands and landscape features, can be the key of a correct understanding of distribution of semi-aquatic amphibians.

Spatial segregation among age classes in cave salamanders: habitat selection or social interactions?

Within species, individuals with different sexes, morphs and age classes often show spatial segregation. Both habitat selection and social processes have been proposed to explain intraspecific spatial segregation, but their relative importance is difficult to assess. We investigated spatial segregation between age classes in the cave salamander Hydromantes (Speleomantes) strinatii, and used a hypothetico-deductive approach to evaluate whether social or ecological processes explain segregation pattern. We recorded the location and age class of salamanders along multiple caves; we measured multiple microhabitat features of different sectors of caves that may determine salamander distribution. We assessed age-class segregation, and used generalized mixed models and an information-theoretic framework, to test if segregation is explained by social processes or by differences in habitat selection. We found significant age-class segregation, juveniles living in more external cave sectors than adults. Multiple environmental features varied along caves. Juveniles and adults showed contrasting habitat selection patterns: juveniles were associated with sectors having high invertebrate abundance, while adults were associated with scarce invertebrates and low temperature. When the effect of environmental features was taken into account, the relationship between juveniles and adults was non negative. This suggests that different habitat preferences, related to distinct risk-taking strategies of age classes, can explain the spatial segregation. Juveniles require more food and select more external sectors, even if they may be risky. Conversely, adults may trade off food availability in favour of safe areas with stable micro-climate.

Foraging plasticity favours adaptation to new habitats in fire salamanders

Predators often show strong plasticity of optimal foraging strategies. A major difference in foraging strategies occurs between sit-and-wait and active predators. Models predict that the efficiency of these strategies is affected by environmental conditions, active predators being favoured when prey are scarce and their detection difficult. The shift between the two strategies may occur through both phenotypic plasticity and local adaptations. Larvae of the fire salamander, Salamandra salamandra, are typically stream-dwelling sit-and-wait predators, but some populations breed in caves. We evaluated whether local adaptations or phenotypic plasticity determine shifts in foraging strategy between stream and cave populations. The foraging behaviour of salamander larvae was evaluated under all combinations of three test conditions during trials: light versus darkness, prey presence versus absence and food deprived versus fed; larvae originated from caves and streams and were reared in epigeous photoperiod or in darkness. Observations and video tracking showed that salamander larvae modified their behaviour in response to environmental conditions. In the darkness, larvae showed higher average velocity and moved longer distances. Movements were higher in food-deprived larvae and in the presence of prey compared to fed larvae and prey absent conditions. Furthermore, larvae from cave populations showed higher behavioural plasticity than stream larvae, and better exploited the available space in test environments. Variation in foraging behaviour was strong, and involved complex interactions between plasticity and local adaptations. Larvae from cave populations showed higher behavioural plasticity, supporting the hypothesis that this trait may be important for the exploitation of novel environments, such as caves.

Antagonizing Retinoic Acid and FGF/MAPK Pathways Control Posterior Body Patterning in the Invertebrate Chordate Ciona intestinalis

Vertebrate embryos exploit the mutual inhibition between the RA and FGF signalling pathways to coordinate the proliferative elongation of the main body axis with the progressive patterning and differentiation of its neuroectodermal and paraxial mesodermal structures. The evolutionary history of this patterning system is still poorly understood. Here, we investigate the role played by the RA and FGF/MAPK signals during the development of the tail structures in the tunicate Ciona intestinalis, an invertebrate chordate belonging to the sister clade of vertebrates, in which the prototypical chordate body plan is established through very derived morphogenetic processes. Ciona embryos are constituted of few cells and develop according to a fixed lineage; elongation of the tail occurs largely by rearrangement of postmitotic cells; mesoderm segmentation and somitogenesis are absent. We show that in the Ciona embryo, the antagonism of the RA and FGF/MAPK signals is required to control the anteroposterior patterning of the tail epidermis. We also demonstrate that the RA, FGF/MAPK and canonical Wnt pathways control the anteroposterior patterning of the tail peripheral nervous system, and reveal the existence of distinct subpopulations of caudal epidermal neurons with different responsiveness to the RA, FGF/MAPK and canonical Wnt signals. Our data provide the first demonstration that the use of the antagonism between the RA and FGF signals to pattern the main body axis predates the emergence of vertebrates and highlight the evolutionary plasticity of this patterning strategy, showing that in different chordates it can be used to pattern different tissues within the same homologous body region.

Seasonal variation in microhabitat of salamanders: environmental variation or shift of habitat selection?

Relationships between species and their habitats are not always constant. Different processes may determine changes in species-habitat association: individuals may prefer different habitat typologies in different periods, or they may be forced to occupy a different habitat in order to follow the changing environment. The aim of our study was to assess whether cave salamanders change their habitat association pattern through the year, and to test whether such changes are determined by environmental changes or by changes in preferences. We monitored multiple caves in Central Italy through one year, and monthly measured biotic and abiotic features of microhabitat and recorded Italian cave salamanders distribution. We used mixed models and niche similarity tests to assess whether species-habitat relationships remain constant through the year. Microhabitat showed strong seasonal variation, with the highest variability in the superficial sectors. Salamanders were associated to relatively cold and humid sectors in summer, but not during winter. Such apparent shift in habitat preferences mostly occurred because the environmental gradient changed through the year, while individuals generally selected similar conditions. Nevertheless, juveniles were more tolerant to dry sectors during late winter, when food demand was highest. This suggests that tolerance for suboptimal abiotic conditions may change through time, depending on the required resources. Differences in habitat use are jointly determined by environmental variation through time, and by changes in the preferred habitat. The trade-offs between tolerance and resources requirement are major determinant of such variation.

Odonata occurrence in caves: Active or accidentals? A new case study

Caves are environments that host unique faunas and may be important for organisms not exclusively dependent on caves. The occurrence of epigean taxa in caves is often considered accidental, but their study can provide useful information on cave colonization. Records of Odonata underground are extremely scarce. We have identified larvae of Cordulegaster bidentata in two caves, one natural and one artificial, from Lombardy in northwestern Italy. They occurred in pools near the cave entrance that have 84 lux of maximum illuminance, reached in early spring. In both caves we found a high density of larvae, and some of them were at very advanced instars. They had an important role in the cave’s trophic web, exerting a high predation pressure on larvae of the salamander Salamandra salamandra. The plasticity of some Odonata species may allow them to take advantage of underground springs.

Dry stone walls favour biodiversity: a case-study from the Appennines

One of the classical and traditional wall typology built in agricultural or pastoral landscapes are dry stone walls (walls built only of stones without concrete). These vertical surfaces are expected to increase habitat heterogeneity and to play an important role for biodiversity. This study focused on two groups of organisms: amphibians, represented by the rock-dwelling salamander Hydromantes strinatii, that are expected to use walls mainly as shelters, and molluscs, which use of walls may be affected mainly by the trophic resources available. A mountain area of the northern Appennines (NW-Italy) was surveyed to assess the differences between dry stone walls and the wall typologies in terms of morphology, surrounding landscape and salamander and mollusc occurrence; the relationships between wall typology features and salamander and mollusc distribution were assessed. Dry stone walls were more heterogeneous than concrete walls and hosted more lichens than natural rocky walls. They were more used by H. strinatii juveniles than the other walls and played an important role for their distribution. They were positively related to the occurrence of several molluscan species, including species with high ecological plasticity and rock-dwelling species. Among wall features, the most important for molluscs species distribution was vegetation cover, followed by lichen cover and heterogeneity, confirming the importance of trophic content for mollusc exploitation, while vegetated without concrete walls hosted higher number of species. The results suggest that dry stone walls can be important for fauna biodiversity and should be maintained and preserved as a part of landscape management.

Cave features, seasonality and subterranean distribution of non-obligate cave dwellers

Seasonality impacts species distributions through changes of the environmental conditions that affect the presence of individuals at a given place. Although the dynamics of cave microclimates are well known, only a few studies have evaluated the effects of such dynamics on non-strictly cave species. Here we assessed if species exploiting subterranean environments show changes in habitat occupation related to seasonal variation of cave microclimates. We surveyed 16 caves in central Italy every month for one year. Caves were subdivided into longitudinal sectors of three meters. In each sector we measured cave morphology and microclimatic features, assessed the occurrence of eight non-troglobitic taxa (orthopterans, spiders, gastropods and amphibians), and related species distribution to environmental features and sampling periods. The occurrence of most species was related to both cave morphology and microclimatic features. The survey month was the major factor determining the presence of species in cave sectors, indicating that cave-dwelling taxa show strong seasonality in activity and distribution. For multiple species, we detected interactions between sampling period and microclimatic features, suggesting that species may associate with different microhabitats throughout the year. The richest communities were found in sites with specific microclimates (i.e., high humidity, warm temperature and low light) but seasonality for species richness was strong as well, stressing the complexity of interactions between outdoor and subterranean environments.

Thermal equilibrium and temperature differences among body regions in European plethodontid salamanders.

Information on species thermal physiology is extremely important to understand species responses to environmental heterogeneity and changes. Thermography is an emerging technology that allows high resolution and accurate measurement of body temperature, but until now it has not been used to study thermal physiology of amphibians in the wild. Hydromantes terrestrial salamanders are strongly depending on ambient temperature for their activity and gas exchanges, but information on their body temperature is extremely limited. In this study we tested if Hydromantes salamanders are thermoconform, we assessed whether there are temperature differences among body regions, and evaluated the time required to reach the thermal equilibrium. During summers of 2014 and 2015 we analysed 56 salamanders (Hydromantes ambrosii and Hydromantes italicus) using infrared thermocamera. We photographed salamanders at the moment in which we found them and 1, 2, 3, 4, 5 and 15min after having kept them in the hands. Body temperature was equal to air temperature; salamanders attained the equilibrium with air temperature in about 8min, the time required to reach equilibrium was longer in individuals with large body size. We detected small temperature differences between body parts, the head being slightly warmer than the body and the tail (mean difference: 0.05°C). These salamanders quickly reach the equilibrium with the environment, thus microhabitat measurement allows obtaining accurate information on their tolerance limits.

Field-recorded data on the diet of six species of European Hydromantes cave salamanders

The availability of data on the feeding habits of species of conservation value may be of great importance to develop analyses for both scientific and management purposes. Stomach flushing is a harmless technique that allowed us to collect extensive data on the feeding habits of six Hydromantes species. Here, we present two datasets originating from a three-year study performed in multiple seasons (spring and autumn) on 19 different populations of cave salamanders. The first dataset contains data of the stomach content of 1,250 salamanders, where 6,010 items were recognized; the second one reports the size of the intact prey items found in the stomachs. These datasets integrate considerably data already available on the diet of the European plethodontid salamanders, being also of potential use for large scale meta-analyses on amphibian diet.