According to regional assessments following IUCN criteria, S. atra aurorae has been categorized as Vulnerable (VU) under criterion D2, because the “extent of occurrence” was estimated <20 km2 (Bonato et al. 2007; Comitato Italiano IUCN 2013; Rondinini et al. 2013). Instead, within the global assessment of the species S. atra, evaluators proposed to rank the subspecies S. atra aurorae as CR (critically endangered), under criterion B1ab (iii), because it was considered comprising a single local population and the habitat quality was judged as declining (Andreone et al. 2009).
Salamandra atra pasubiensis differs from all other subspecies of S. atra in the individual variability of the body colour. The body surface is mainly uniformly black, with a variable number and extent of yellow and brown patches on the dorsal surface of the head, the trunk, the limbs and the tail. The patches are very similar to those found in S. atra aurorae, however much smaller and covering only a minor part of the dorsal surface. Extent and arrangement of the patches are highly variable between individuals, some of which are even entirely black, like in S. atra atra and S. a. prenjensis (Bonato et al. 2007). The colour pattern is established at birth and it is assumed to change only slightly with growth, like in S. atra aurorae.
The sexual dimorphism is very slight. Like in other subspecies of S. atra, the cloacal region is usually swollen in the adult males.
S. atra pasubiensis lives only on the Pasubio massif, in the Venetian Prealps, NE Italy. All documented and reliable records are from two adjacent small valleys on the southern slope of the massif, and refer most probably to a single population. The known area of occupancy is less than 2 km2 and the altitudinal range is 1450-1800 m (Romanazzi & Bonato 2014).
There are a few other reports of alpine salamanders from other parts on the Pasubio massif and from the nearby Carega massif, but all these records are unconfirmed (Romanazzi & Bonato 2014).
The rocky, steep valleys inhabited by S. atra pasubiensis are only marginally exploited for wood harvesting and cattle pasture, and are visited almost only by hikers and hunters. Therefore, S. atra pasubiensis is not threatened directly by human activities, but the narrow extent and the isolation of the suitable habitat increases vulnerability in the face of the general climatic trend (Comitato Italiano IUCN 2013).
According to regional assessments following IUCN criteria, S. atra pasubiensis has been considered as Endangered (EN), under criterion D1, because it seems to be present in a single site, the population size could be less than 250 individuals and it is threatened by the general climatic trend (Bonato et al. 2007; Comitato Italiano IUCN 2013; Rondinini et al. 2013).
S. atra aurorae had remained unknown to scientists up to 1978 and its discovery was published for the first time in 1981 (Trevisan et al. 1981). The taxonomic description and denomination appeared in the following year, first within an abstract for a congress and then in a detailed article (Trevisan 1982). For nomenclatural purposes, the type locality was designated as the “Bosco del Dosso, near Vaio di Pian del Morto, between val Remaloch and Val Rotta” and the holotype has been deposited in the Zoological Museum La Specola in Florence (Trevisan 1982). Since the original description, S. atra aurorae has been almost universally distinguished at the subspecies rank, but it has been sometimes raised to the species rank (Joger 1986; Dubois & Raffaëlli 2009).
The taxonomic distinction of S. atra aurorae is corroborated by both phenotypic and genetic differences from all other populations of the S. atra: all specimens of S. atra aurorae have yellow blotches covering more than half of the dorsal surface, whereas the specimens of all other subspecies are either uniformly black or at most only sparsely spotted (Bonato et al. 2007); additionally, genetic data suggests that S. atra aurorae represent a distinct lineage within S. atra (Ribéron et al. 2004, Steinfartz et al. 2000). Mating between S. atra aurorae and S. atra atra has been observed under captive conditions, producing viable and fertile juveniles with narrower yellow patches (Raffaëlli 2014).
The range of distribution of S. atra aurorae is mainly in the Veneto Region, specifically in the Province of Vicenza, but a part is in the Province of Trento.
S. atra aurorae is listed in the Annex II (originally under the name 'Salamandra salamandra aurorae') and Annex IV (under the name 'Salamandra aurorae') of the EU Habitats Directive 92/43/EEC. Most of the known range is included in the Natura 2000 site IT3220036 “Altopiano dei Sette Comuni”.
The single known population of S. atra pasubiensis is in the Veneto Region, specifically in the Province of Vicenza. It is entirely in the Natura 2000 site IT3210040 “Monti Lessini - Pasubio - Piccole Dolomiti Vicentine”.
S. atra pasubiensis is not considered in the EU Habitats Directive 92/43/EEC because it was unknown at the time.
All forests inhabited by S. atra aurorae are exploited for wood since centuries. However, modern practices commonly employed in wood harvesting include the use of heavy machines moving on the ground during the season of activity of the animals, compacting the soil and removing the ground vegetation along broad stripes. As a consequence, the microhabitat conditions become locally unsuitable for S. atra aurorae (AA.VV. 2012; Comitato Italiano IUCN 2013).
Concerns have also been raised, especially in the past, for the negative impacts of the illegal and uncontrolled collection of specimens, primarily for pet trade, and for the alteration of the local microclimate as a consequence of the capture of water springs for human use (Andreone et al. 2009).
Individuals overwinter underground, most probably at some depth in the soil, where they remain inactive for at least 6 months (Bonato & Fracasso 1998). Since late April to late September, instead, they still spend most part of the time resting in the soil, however often in the most upper level, sometimes concealed under occasional shelters (e.g., stones emerging from the ground, dead wood or pieces of barks on the surface). During this period, they exit and move on the surface only when the surface is wet and the air is very humid, especially after intense rains following dry periods, independently from the daily cycle of light. At difference from other S. atra, S. atra aurorae does not exit regularly every day around dawn (Lefosse et al 2016). Adult males are apparently more prone to epigean activity than females and juveniles (Lefosse et al 2016).
While juveniles disperse during the yearly season, adults are sedentary and remain within their home range also between years (Bonato & Fracasso 2003). Different shelters are used by a single individual within its home range, which is a few tens of square metres on average, without any obvious differences between males and females. Individual home ranges are partially overlapping, also between individuals of the same sex. The population density has been estimated up to hundreds of individuals per hectare (Bonato & Fracasso 2003).
The life cycle of S. atra aurorae has been investigated only in part, but is probably similar to that documented for S. atra atra.
The embryonic and larval development are completed in the uteri of the mother and the juvenile is born after completing metamorphosis, even though it may retain small residuals of gills for a period (Bonato & Fracasso 1998). Usually two juveniles are given born together by a pregnant female (Trevisan 1982).
Salamandra atra aurorae is very similar in body shape to all other subspecies of S. atra, also in all major characters that often distinguish different species of Salamandra: outline of the head, position of the vomerine teeth, proportions of body parts and limbs, arrangement glandular bulges and pores on the skin, and shape and length of the tail (Bonato et al. 2007).
However, the body surface is not entirely and uniformly black as in most other populations of S. atra. Conversely, the dorsal side of S. atra aurorae is broadly covered with yellow-brown blotches, which are broader and often coalescent on the head and the trunk, they are usually present also on the arms, the thighs and the tail, whereas they are rare on the flanks and the ventral sides (Bonato et al. 2007). Blotches are invariantly present in all individuals, but highly variable in extent (covering from slightly more than half of the dorsal surface to almost the entire dorsal surface) and in dominant hue (from pale yellow to marbled brown) (Bonato & Fracasso 1998). The colour pattern is highly variable between individuals, without any obvious difference neither between sexes nor between sites. It is established at birth and it usually changes only slightly with growth (Trevisan et al. 1982; Bonato et al. 2007). However, relatively rapid and extended changes from yellow to brown have been occasionally observed in captive individuals (Steinfartz 1998).
Newly born individuals are about 50 mm long and less than 1 g, whereas adults may reach 134 mm in males and 139 mm in females, and 14 g in pregnant females (Bonato & Fracasso 1998).
The sexual dimorphism is very slight, but it has not been investigated adequately. Like in other subspecies of S. atra, the cloacal region is usually swollen in the adult males.
S. atra aurorae lives only in the northern part of the Sette Comuni plateau, in the Venetian Prealps, NE Italy. The actual distribution is known only incompletely, because the animals are very elusive and therefore hard to detect, and adequate investigations have not been carried out (Lefosse et al. 2016). As to 2016, all documented or reliable records cluster in 12 areas, more than 0.7 km far from each other and approximately aligned West to East from Val Postesina to Monte Fossetta (Romanazzi & Bonato 2014). However, it is unknown whether the populations detected in these areas are actually separated or instead connected through suitable intermediate areas (Andreone et al. 2009). The estimated area of occupancy of S. atra aurorae is 26 km2 (Romanazzi & Bonato 2014).
Areas inhabited by S. atra aurorae are in the range 1200-1800 m and include both moderately inclined slopes and narrow valleys facing south. The substrate is rocky, calcareous and karstic. Most sites are covered with old-growth forest stands with Beech, Silver Fir and Norway Spruce. The soil is rocky, with variable abundance of leaf litter, dead wood on the ground, and patches of grass and moss. Only a few records are from shrubby meadows (Romanazzi & Bonato 2014).
In the area of the Bosco del Dosso, S. atra aurorae inhabits only the inner parts of the forest, where old-growth stands of Silver Fir with Beech are apparently more suitable than thicker stands dominated by Norway Spruce (Bonato & Fracasso 2015). Among adults, habitat requirements are similar between males and females (Bonato & Fracasso 2015).
After a few uncertain or undocumented reports, the presence of a differentiated population of S. atra on the Pasubio massif was eventually confirmed in 1999 (Bonato 2000). This population has been named as a distinct subspecies in 2005, because it is chromatically and genetically differentiated from both S. atra atra and S. atra aurorae, and geographically separated from the remaining species range (Bonato & Steinfartz, 2005). The type locality is “Val Fontana d'Oro” and the holotype has been deposited in the Zoological Museum La Specola in Florence (Bonato & Steinfartz, 2005).
The alpine salamander (Salamandra atra) is a black salamander that can be found in the French Alps, and through the mountainous range in Europe.[2] It is a member of the genus salamandra. Their species name, atra, may be derived from the Latin ater, meaning dull black.[3] The salamanders' coloration has evolved over time, as some species are completely monochrome black and others have yellow spotting and marks.[4][5][6][7] Their life expectancy is at least 10 years. There are four subspecies of the alpine salamander, with varied distribution and physical coloration.[8] Unlike other salamanders, whose larvae are developed in water, the alpine salamander and its subspecies are a fully terrestrial species in life and gestation.[8] They give birth to live young.[9]
Alpine salamanders produce toxic compounds from their skin.[8] These compounds may protect them from both predator and microbial threats.[10][11][12][13]
Alpine salamanders are often small in size, and dark brown or black.[8] Members of the subspecies are not wholly black or brown monochrome, but rather have mosaic or spotted patterns.[8] Members of the subspecies Salamandra atra aurorae have bright splotches on its dorsal side and head. The color is often bright yellow, but can range to shades of white or even gray.[8] Distribution of the pigment is dependent on the distribution of certain cells, so may be smooth and even or patchy.[8]
Female S. atra tend to be larger than the males, and can grow up to 151 millimeters, or around 5.9 inches.[8] Males will grow to around 144 millimeters, or 5.6 inches: both measurements include the tail.[8] Males have swollen, visible cloacae, and are more slender than females.[8][14] The salamanders have parotid glands posterior and lateral to their eyes, giving them an elongated head shape.[8] They tend to have between 11 and 13 costal grooves along the sides of their bodies, and a double row of dorsal glands runs down their backs on either side of their spines, down to the tips of their tails.[8]
Most alpine salamanders that are either completely black (melanistic) or predominantly black have the dark pigment as a baseline, but the evolution behind this dark coloring has a winding history.[4] Scientists have studied the hypothesis of if the salamanders start completely black, or if they evolved like that over time.[5] DNA-evidence traced through maternal lineages suggest the latter: that salamanders evolved their black coloration over time.[5]
Biological pigmentation is determined by presentation of specific color-producing cells, called chromatophores, which absorb and/or reflect light in a particular way to then appear as a color.[7][15] In S. atra, there are different cells present or activated, which yield different colors: melanophores contribute to the dark coloration by producing the dark pigment melanin,[7] while xanthophores produce a yellow pigment,[4] and iridophores are simply light-reflecting.[4] The fully-black phenotype seen in S. a. atra results from the salamanders' melanophores in the dermis and epidermis, producing melanin alone.[5][7] Xanthophore-iridophore complexes are responsible for production of yellow spotting, which appears bright.[5] In species without yellow patches, it appears that they do not ever develop these cells.[5] In S. a. aurorae or other salamanders with different coloration on different parts of their body, two distinct skin types are present: one that only contains melanophores (black), and one that has melanophores, xanthophores, and iridophores in combination.[7]
The yellow coloring on some alpine salamanders is thought to be an aposematic strategy to fend off predation.[11] The pure black coloring is also hypothesized to be a form of thermoregulation,[11] though it may also be considered a warning to some predators.[11]
Genetic analysis suggests that the Corsican fire salamander (Salamandra corsica) is the closest related species, and the black-yellow coloration is an ancestral feature of alpine salamanders. Proposed colonization from south (Prealps) to Alps was carried out by the fully melanistic (derived feature) S. a. atra after the last retreat of the ice sheets.[18]
As terrestrial salamanders, these organisms live on land.[8][19] S. atra tend to live underneath stones or logs, or in rocky crevices in their mountainous habitat.[8] They also are diurnal, and most active in the day with periods of inactivity, rest, or sleep at night.[16] They will engage in nocturnal activity on a weather-dependent basis.[20] Ideal weather for alpine salamanders is rainy or post-rain, at temperatures between 3 and 18C (around 37-64 F).[16]
The alpine salamander is found from the France–Switzerland border at the western end of its range, all the way through Austria to the Dinaric Alps at the eastern edge of its territory. This salamander typically lives at altitudes above 700 metres (2,300 ft) above sea level, even reaching 2,000 metres (6,600 ft) of elevation.[8] The western Alps (in France and Italy) are inhabited by a similar species, Lanza's alpine salamander (Salamandra lanzai), in only one small area. S. atra generally live in forested biomes, particularly deciduous-coniferous mixes.[8] They also can inhabit meadows or grasslands in the mountains,[8] and tend to do well with a mix of tree types.[21][16]
Their range spans several nations, including: Slovenia, Croatia, Bosnia, Hersegovina, Montenegro, Kosovo, France, Italy, Austria.
They thrive in forest environments that have silver fir and beech trees.[21][22] Coniferous forests that have high proportions of Norway spruce and European larch trees also provide adequate habitats, even though the salamanders live on the ground floor.[21] Because alpine salamanders are completely terrestrial, they have on-land territories that they tend to return to throughout the day and for refuge. They often return to the same sites for much of their lives.[21] Any time that they leave their sites, they expose themselves to predation and also to the chance of losing their site.[21] Alpine salamanders are ectothermic, so losing a refuge or shelter could leave them exposed to the elements and be extremely costly, if not fatal,[21] due their lack of an internal thermoregulation mechanism.
This high dependency on a quality nest site supports the theory that many terrestrial salamanders, including S. atra, engage in territorial behaviors.[21] Capture-recapture methods suggest that the species is very stationary;[23] 12 metres (39 ft) was the maximum observed distance traveled by one individual during the summer season. About 120 individuals per hectare were counted in most suitable areas with over 2000 individuals per hectare also observed, suggesting that this rather cryptic species is quite abundant.[17]
They employ scent-marking techniques for territorial behaviors, and to mark their territories using fecal pellets so they can identify their own shelters.[21] Scent-marking is an intra-species communication, where chemical signals convey specific messages to other S. atra individuals.[21][24] Alpine salamanders can determine if a found fecal pellet has been left by a member of their same sex and/or species.[21] Thus, this technique serves a double purpose to warn other salamanders that that particular location has already been claimed.[21]
Females are more likely to return to their home site, while males are more emboldened to enter another male's territory.[21] Their fecal pellets allow them to both participate in homing behavior, or returning to their own site, and territoriality, and determine intruders on their territory or invade the spaces of others.[21]
Alpine salamanders are not resilient to habitat changes— few terrestrial salamanders are— so risks of climate change altering their living spaces is severe.[23] Although alpine salamanders are listed as Least Concern on IUCN Red List, their numbers are decreasing.[25] Additionally, some subspecies of S. atra are in greater danger.[26] Population numbers are declining in S. a. aurorae, for example.
One of the greatest dangers to alpine salamanders overall is commercial deforestation in their habitats.[26] Machinery like tractors or other forestry tools can compress the soil, eliminating some of the small insects that S. atra eat or eliminating potential nooks and burrows for them to use as shelters.[26] Many scientists propose changes in the lumber industry as an attempt to heal these habitats.[26] These salamanders may also change their morphology as global temperatures rise.[27] Amphibians and other organisms that do not internally regulate their body temperature may need adaption mechanisms to remain at ideal physiological temperatures in the face of changing climates.[27] Other issues like acid rain or precipitation changes could prompt many animals, including alpine salamanders, to be forced into new habitats.[27] Alpine salamanders play a crucial role in their ecosystems.[28] There are already animal and ecosystem conservation laws in Europe, but many scholars recommend additional ones to protect the flora and fauna.[12]
Due to their toxicity,[10][11] as well as decreased concentration of animals at high altitudes,[29] researchers are unsure of consistent predators for alpine salamanders with limited observation.[8] These salamanders do move slowly, which could increase their risk of being caught.[29] Generally, predators of the broad category of toxic Salamandra species can include birds, rats and snakes, as well as other, larger carnivorous mammals like raccoons, minks, wild boars and foxes.[10]
One notable predator of S. atra is young snakes.[29] In particular, juvenile European adders (Vipera berus) pose a risk because they live at similarly high altitudes to alpine salamanders.[29] S. atra have been suggested to make up just under half of these snakes' diets in some locations.[29] They may hunt for alpine salamanders during early morning hours, when S. atra is most active.[29] There also has been recorded evidence of these snakes swallowing alpine salamanders.[29] V. berus, alongside the grass snake (Natrix natrix), are noted predators of alpine salamanders in the Italian Alps.[8]
Male and female alpine salamanders have relatively similar diets.[30] Some specific organisms they prey on include species such as beetles, snails, millipedes, and spiders,[31] but alpine salamanders display preferences among prey.[30] S. atra typically consume organisms from the Coleoptera and mollusca taxa.[30] These taxa are the most crucial component of their diet. They also tend to eat larger prey since they themselves are larger salamanders.[30] Such preference indicates a dimensional selectivity, in which the energy intake of prey consumption is maximized.[30] Though alpine salamanders have definite dietary preferences, they have a substantial amount of variation in their diet[30] that corresponds to their own optimized physical needs and prey-catching abilities.
The alpine salamander engages in a promiscuous mating pattern,[20] meaning that they engage in multiple partner pairings. Males immigrate and travel farther than females do, potentially to find mates and following a scent emitted by females.[20] Typically, males migrated when they were in the juvenile stage of life.[20] Female S. atra find and defend their shelters, which is a potential reason that they may stay more local than males.[20]
Males are more likely to engage in chasing other males, as well as actually fighting with each other.[32] Oftentimes, one male will mount the other, loosely grasp it with his forearms, and start rubbing his head on the other male.[32] The two males will switch roles, and in one studied interaction, continued like this for seven minutes before parting ways.[32] In a second documented fight, the behavior was more intense. When one member tried to leave, the other male chased it to re-engage.[32] This encounter lasted eight minutes. There is both photographic and video evidence of these behaviors.[32] Researchers are unsure if it is caused by territoriality, confusion on sexual identification and mistaken mating, or true combat.[32]
Alpine salamanders live in a sex ratio of 1:1.[33] Mating occurs on land. The male clasps the female at the forelegs, and fertilization is internal. S. atra are categorized as viviparous, meaning that their young are born alive and unlike many other amphibians, do not go through metamorphosis[8][9] They give birth to 2 young, sometimes 3 or 4. New young alpine salamanders may measure as long as 50 millimetres (2 in) at birth, with the mother measuring only 120 millimetres (4.7 in).
Female alpine salamanders have uteruses that are composed of a single luminal epithelial cell layer, connective tissue, and smooth muscle.[9] The uterine eggs are large and numerous, but, as a rule, only one fully develops in each uterus. The embryo is nourished on the yolk of the other eggs, which more or less dissolve to form a large mass of nutrient matter. The egg mass can be as long as between 25 mm and 40 mm long.[9] The embryo passes through three stages:[34]
Generally, at altitudes of 650–1,000 metres (2,130–3,280 ft) above sea level, a pregnancy lasts two years, and at altitudes of 1,400-1,700 m above sea level, the pregnancy lasts around three years, though anything within a 2-4 year range is considered standard.[9] Alpine salamander embryos are unique in how they are able to take in these nutrients through a long gestation.[9] A portion of the mother's uterine wall becomes nourishment after the salamanders have already eaten the unfertilized eggs,[9] (called oophagy or stage 1 and 2).[9] They then partake in epitheliophagy, or stage 3, where they ingest these zona trophica cells until birth, and have special tooth-like developments that allow it to do so without detriment to the mother.[9]
As mentioned above, alpine salamanders have poison glands.[8] They are known to produce some alkaloid molecules and peptide products, and thus have a mustard-like scent associated with them.[10] Salamandra bioproduction is still a developing research area. Salamandarines are a chemical secretion produced by the skin of alpine salamanders, as well as some fire salamanders.[8][35] They are neurotoxins, and are synthesized via a biochemical pathway, completely independent of dietary intake.[8] This means that they make these chemicals within their bodies, not as a result of ingesting poisonous substances.The starting material for this nerve-block is most likely cholesterol, and it is about twice as potent as cyanide.[8] This pales in comparison to other toxins produced by salamanders, but S. atra do not only use this powerful substance to paralyze prey: they may have antimicrobial properties that protect them against bacterial and fungal infections.[8][36] Salamandorone is another biochemical compound produced by S. atra, and though it is less potent against prey it is the strongest antimicrobial weapon these salamanders have.[8][13][36]
There are two main categories of toxin studied, samandarine and samandarone.[8][11] There also exist many other compounds, as well as miscellaneous alkaloid secretions.[8] Both samandarine and samandarone are produced by S. atra species.[11] It is hypothesized that salamandarine is more commonly produced in alpine salamanders as a predator defense mechanism, and salamandorones are produced where there is greater infection risk.[8] There is also noted geographic variation in toxin production by alpine salamanders.[8]
Samandarone, a toxin they produce via skin secretion, has noted antimicrobial activity.[8] In one study, this toxin was present where there was infection risk, but at low concentration.[8] There is a wide arsenal of toxins produced by S. atra , many of which are antimicrobial or could be precursors to other protective molecules.[8] Nonetheless, the alpine salamander has been relatively lucky in avoiding infection with amphian chytrid fungus[36] compared to other amphibian species.[36][37] This dangerous fungal infection, caused by Batrachochytrium dendrobatidis (Bd) has decimated amphibian populations on every continent.[36] Bd is present in the Alps where alpine salamanders live, but in a study performed in 2012, there were no salamanders who tested positive when swabbed.[36] This may be because Bd infections are more common in species who spend more of their time in water, and since the alpine salamanders are terrestrial, they are less susceptible.[36] An alternate hypothesis proposes that S. atra are resistant via their skin microbiome or a produced molecule, thus granting them immunity.[36][38] This theory is untested, but considering how many salamanders excrete biological toxins, plausible.[36][38]
The alpine salamander (Salamandra atra) is a black salamander that can be found in the French Alps, and through the mountainous range in Europe. It is a member of the genus salamandra. Their species name, atra, may be derived from the Latin ater, meaning dull black. The salamanders' coloration has evolved over time, as some species are completely monochrome black and others have yellow spotting and marks. Their life expectancy is at least 10 years. There are four subspecies of the alpine salamander, with varied distribution and physical coloration. Unlike other salamanders, whose larvae are developed in water, the alpine salamander and its subspecies are a fully terrestrial species in life and gestation. They give birth to live young.
Alpine salamanders produce toxic compounds from their skin. These compounds may protect them from both predator and microbial threats.
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