Vipera Aspis Research Articles

Intraspecific venom variation in the Iberian asp viper (Vipera aspis zinnikeri) across natural and intensive agricultural habitats

Snake venom composition varies at different levels. To date, comparative venom studies have seldom taken into account the role of habitat type in the occurrence of snake venom variation. Here we investigated the presence of venom variation across different populations of the Iberian asp viper (Vipera aspis zinnikeri) inhabiting two contrasting habitats: natural vs. intensive agricultural. We used shotgun proteomics to describe the protein composition of the venoms of six adults from two distinct localities. Furthermore, to test whether local conditions and habitat can alter venom composition in this taxon, we compared the SDS-PAGE profiles of 40 adult venoms from six populations, three in natural habitats and three in intensive agricultural environments. The venoms were composed of 21 toxin families, of which five (CTL, PLA2, VEGF, svSP, and svMP) comprised 69–82 % of each proteome. The relative abundances of toxin families varied considerably at inter- and intra-population levels. Linear regression performed on non-metric multidimensional scaling values showed a significant effect of locality of origin and habitat type on the differences detected between individual SDS-PAGE venom profiles. Our results suggest the presence of regional variation in V. a. zinnikeri venom, potentially reinforcing the role of local pressures in shaping snake venom composition. SignificanceThis work provides the first proteomic characterization of the venom of the Iberian asp viper, Vipera aspis zinnikeri, obtained by means of shotgun proteomics. The statistical analysis of 40 individual SDS-PAGE venom profiles highlights that venom variation in this taxon can be associated with geographical origin and habitat type of the area where each viper was collected. Our results suggest the presence of regional variation in V. a. zinnikeri venom, reinforcing the role that local pressures may play as drivers of snake venom variation.

A review of the Late Miocene herpetofauna of the Keinar locality of Moldova

Small fossil amphibians and reptiles from the Late Miocene of the Keinar locality of Moldova are reviewed for the first time. The following taxa are described: Mioproteus caucasicus, Chelotriton sp., Latonia sp., Pelobates sp., Pelophylax sp., “Colubrinae” indet., Natrix sp., two Vipera spp. (“Vipera aspis complex” and “Oriental vipers complex”), and Squamata indet. Among them, Pelobates sp. exhibits the characters which occur in the Early–Late Miocene (presence of both pit-and-ridge and pustular sculptures of the frontoparietal bone) and in the Pliocene (short frontoparietal–squamosal contact) members of the genus; this combination is not observed in any other Pelobates species. The viperid snake of the “Vipera aspis complex” is recorded from Moldova for the first time.

The tale of the black viper: distribution and bioclimatic niche modelling of melanistic Vipera aspis in Italy

The tale of the black viper: distribution and bioclimatic niche modelling of melanistic Vipera aspis in Italy

Barred, blotched or intermediate? A photographic-based survey on the spatial distribution of <em>Vipera aspis</em> phenotypes from central-southern Italy

Variation in animal colouration, which holds ecological and evolutionary significance, is evident in snakes, including the polytypic and highly polymorphic asp viper Vipera aspis. This species, currently acknowledged with four subspecies, features three of them (V. a. aspis, V. a. francisciredi and V. a. hugyi) within the Italian territory, each displaying distinct dorsal patterns. Analysing 143 georeferenced photos from personal surveys and citizen science, the present study explores transition areas between V. a. francisciredi and V. a. hugyi, revealing the coexistence of three dorsal pattern phenotypes (i.e. francisciredi, hugyi, and intermediate) across central-southern Italy. The outcome of the work reveals occurrences of francisciredi phenotypes considerably beyond the southern limit indicated in recent literature. Remarkably, intermediate phenotypes cover a significant portion of southern Italy, including Apulia (three records), Basilicata (six records) and Campania (three records) regions, and overlapping with both hugyi and francisciredi ranges. These findings suggest asymmetrical gene flow from northern to southern populations, resembling patterns observed in other reptiles. The intricate distribution of colour phenotypes underscores the necessity for molecular investigations to comprehend the genetic context and evolutionary history of V. aspis populations from central-southern Italy.

Diet variations across remote populations of a widely distributed snake species, the Asp viper (Vipera aspis aspis, Linnaeus, 1758)

Abstract Documenting intra-specific diet variations among remote populations, thus across different habitats, is important to address evolutionary (e.g., phenotypic plasticity) and conservation issues (e.g., capacity to adapt to changing prey availability). We compared the diet of different populations of Asp vipers (Vipera aspis aspis; Linnaeus, 1758) living in contrasted habitats of France and Switzerland. We sampled 1680 individuals in five geographical areas, broadly encompassing the distribution range of the species (West to East and North to South): Group 1 = Western Central France; Group 2 = Central France; Group 3 = West France; Group 4 = South France, and Group 5 = Switzerland. We compared mean total body size (TL) of snakes and their diet. We found strong similarities among the groups with a predominance of micromammals in the diet. In mountainous area (Group 5), however, snakes included a substantial number of reptiles and fed occasionally on amphibians and birds. The diet varied ontogenetically (juveniles often consuming lizards, adults heavily feeding on mammals) and sexually (females tending to feed more extensively on mammals). Overall, our results suggest that Asp vipers maintain a diet largely based on micromammals (mostly voles), at least across their continental distribution range.

Isolation and characterization of polymorphic microsatellite loci for the three Iberian vipers, Vipera aspis, V. latastei and V. seoanei by Illumina MiSeq sequencing

BackgroundEuropean vipers (genus Vipera) are a well-studied taxonomic group, but the low resolution of nuclear sanger-sequenced regions has precluded thorough studies at systematic, ecological, evolutionary and conservation levels. In this study, we developed novel microsatellite markers for the three Iberian vipers, Vipera aspis, V. latastei and V. seoanei, and assessed their polymorphism in north-central Iberian populations.Methods and resultsGenomic libraries were developed for each species using an Illumina Miseq sequencing approach. From the 70 primer pairs initially tested, 48 amplified reliably and were polymorphic within species. Cross-species transferability was achieved for 31 microsatellites loci in the three target species and four additional loci that were transferable to one species only. The 48 loci amplified in average seven alleles, and detected average expected and observed heterozygosities of 0.7 and 0.55, in the three genotyped populations/species (26 V. aspis, 20 V. latastei and 10 V. seoanei).ConclusionsOur study provides a selection of 48 polymorphic microsatellite markers that will contribute significantly to current knowledge on genetic diversity, gene flow, population structure, demographic dynamics, systematics, reproduction and heritability in these species, and potentially in other congeneric taxa.

Ecological responses of squamate reptiles to nocturnal warming.

Nocturnal temperatures are increasing at a pace exceeding diurnal temperatures in most parts of the world. The role of warmer nocturnal temperatures in animal ecology has received scant attention and most studies focus on diurnal or daily descriptors of thermal environments' temporal trends. Yet, available evidence from plant and insect studies suggests that organisms can exhibit contrasting physiological responses to diurnal and nocturnal warming. Limiting studies to diurnal trends can thus result in incomplete and misleading interpretations of the ability of species to cope with global warming. Although they are expected to be impacted by warmer nocturnal temperatures, insufficient data are available regarding the night-time ecology of vertebrate ectotherms. Here, we illustrate the complex effects of nocturnal warming on squamate reptiles, a keystone group of vertebrate ectotherms. Our review includes discussion of diurnal and nocturnal ectotherms, but we mainly focus on diurnal species for which nocturnal warming affects a period dedicated to physiological recovery, and thus may perturb activity patterns and energy balance. We first summarise the physical consequences of nocturnal warming on habitats used by squamate reptiles. Second, we describe how such changes can alter the energy balance of diurnal species. We illustrate this with empirical data from the asp viper (Vipera aspis) and common wall lizard (Podarcis muralis), two diurnal species found throughout western Europe. Third, we make use of a mechanistic approach based on an energy-balance model to draw general conclusions about the effects of nocturnal temperatures. Fourth, we examine how warmer nights may affect squamates over their lifetime, with potential consequences on individual fitness and population dynamics. We review quantitative evidence for such lifetime effects using recent data derived from a range of studies on the European common lizard (Zootoca vivipara). Finally, we consider the broader eco-evolutionary ramifications of nocturnal warming and highlight several research questions that require future attention. Our work emphasises the importance of considering the joint influence of diurnal and nocturnal warming on the responses of vertebrate ectotherms to climate warming.

Local niches explain coexistence in environmentally-distinct contact zones between Western Mediterranean vipers

Species’ ecological niches are frequently analysed to gain insights into how anthropogenic changes affect biodiversity. Coping with these changes often involves shifts in niche expression, which can disrupt local biotic interactions. Secondary contact zones, where competition and ecological segregation commonly occur, are ideal for studying the ecological factors influencing species’ niches. In this study, we investigated the effect of climate and landscape factors on the ecological niches of two viper species, Vipera aspis and Vipera latastei, across three contact zones in northern Iberia, characterized by varying levels of landscape alteration. Using niche overlap tests, ecological niche models and spatial analyses we observed local variation in the expression of the species’ niches across the three contact zones, resulting from the different abiotic and biotic conditions of each area. Rather than spatial niche segregation, we observed high niche overlap, suggesting niche convergence. A pattern of asymmetrical niche variation was identified in all contact zones, driven by species' climatic tolerances and the environmental conditions of each area. V. aspis generally exhibited a wider niche, except in the southernmost zone where the pure Mediterranean climate favored V. latastei. Human-induced landscape changes intensified niche asymmetry, by favoring the most generalist V. aspis over the specialist V. latastei, increasing habitat overlap, and likely competition. This study presents a comprehensive analysis of niche expression at range margins, anticipating a heightened impact of landscape changes in V. latastei. The methodological framework implemented here, and our findings, hold significant relevance for biodiversity management and conservation in human-impacted areas.

Meso‐habitat distribution patterns and ecological requirements of two Mediterranean vipers depict weak competition in a contact zone

AbstractDisentangling the multiple factors that shape the ecological niche of a species is often difficult, especially when in contact with other similar and potentially competing species. Ecological niche models (ENMs), albeit originally developed for environmental factors only, can help in assessing competition by comparing the niches of ecologically similar species. Here, we use ENMs and niche overlap tests to compare the ecological niches of the Western Mediterranean vipers, Vipera aspis and V. latastei, in the secondary contact zone of the High Ebro (Northern Spain), partitioning the species occurrences in sympatric and allopatric subsets. We considered nine geomorphological and landcover variables, obtained from remote sensing, and gathered at the meso‐habitat scale (100 × 100 m). Our ENMs showed partial interspecific divergence in habitat requirements between these two closely related species, with V. aspis selecting more canopied areas and V. latastei preferring more open habitats. No intraspecific differences in ecological requirements were found when sympatric and allopatric subsets were compared, that is, the two species are not experiencing ecological shift when in contact, which suggests weak competition in habitat use. Our findings, therefore, suggest that species distributions in this contact zone are mainly determined by the environmental conditions, with almost no contribution of competitive pressure. Still, a localized competition might exist due to minor differences in the ecological niches and a marked and unequal reduction of suitable areas for the sympatric populations, which could be favouring V. aspis in small regions of the contact zone.

Environmental and biological significance of the action of viper poison on the homeostasis of mammals

The article examines the ecological and biological significance of the action of animal poisons as an evolutionary adaptation that maximizes the adaptation of more than 250,000 species to the conditions of their habitat. It was found that animal poisons have a significant impact on the formation and course of various forms of connections in ecosystems, perform several ecological functions and are important biotic factors of the environment. The best-studied venomous animals have been found to be snakes, of over 3,800 different species, only a small number are highly venomous. The Viperidae family includes 101 species of poisonous snakes. In Europe, Vipera ammodytes, Vipera aspis, Vipera berus, Vipera latastei, Vipera seoanei and Vipera ursinii are the most dangerous species, their bites cause severe poisoning. In Ukraine, the genus Vipera is represented by the steppe viper (Vipera renardi (Cristoph, 1861)) and two subspecies of the common viper (Vipera berus (Linnaeus, 1758)) — Vipera berus berus and Nikolsky’s viper (Vipera berus nikolskii, Vedmederja Grubant et Rudaeva, 1986). The factors that affect the diversity of the composition of snake venom are given. It is noted that snake venoms are complex mixtures of proteins, peptides and low molecular weight substances, among which enzymes and non-enzymatic components are distinguished. The biological properties of snake venom depend significantly on the properties of its components, which have a wide range of effects on the general state of homeostasis of a living organism. A generalization of scientific data on the study of the chemical composition of the venom of Vipera renardi, Vipera berus nikolskii and Vipera berus berus and the effects of these venoms on the functioning of the mammalian body has been carried out. It was found that the venom of Vipera berus nikolskii is the most, and Vipera renardi — the least toxic for mammals (mice). The effect of Vipera berus nikolskii and Vipera berus berus venom on the proteolytic balance of individual organs of rats was evaluated. It is emphasized that viper venom toxins have a great, not yet fully developed potential in many scientific fields, therefore they deserve further practical research.

An agonist of CXCR4 induces a rapid recovery from the neurotoxic effects of Vipera ammodytes and Vipera aspis venoms.

People bitten by Alpine vipers are usually treated with antivenom antisera to prevent the noxious consequences caused by the injected venom. However, this treatment suffers from a number of drawbacks and additional therapies are necessary. The venoms of Vipera ammodytes and of Vipera aspis are neurotoxic and cause muscle paralysis by inducing neurodegeneration of motor axon terminals because they contain a presynaptic acting sPLA2 neurotoxin. We have recently found that any type of damage to motor axons is followed by the expression and activation of the intercellular signaling axis consisting of the CXCR4 receptor present on the membrane of the axon stump and of its ligand, the chemokine CXCL12 released by activated terminal Schwann cells. We show here that also V. ammodytes and V. aspis venoms cause the expression of the CXCL12-CXCR4 axis. We also show that a small molecule agonist of CXCR4, dubbed NUCC-390, induces a rapid regeneration of the motor axon terminal with functional recovery of the neuromuscular junction. These findings qualify NUCC-390 as a promising novel therapeutics capable of improving the recovery from the paralysis caused by the snakebite of the two neurotoxic Alpine vipers.

Predation by a smooth snake Coronella austriaca of an aspic viper Vipera aspis in Spain

Predation by a smooth snake Coronella austriaca of an aspic viper Vipera aspis in Spain

Behavioural hydroregulation protects against acute effects of drought in a dry-skinned ectotherm.

During extreme climate events, behavioural thermoregulation may buffer ectotherms from thermal stress and overheating. However, heatwaves are also combined with dry spells and limited water availability, and how much individuals can behaviourally mitigate dehydration risks through microclimate selection remains largely unknown. Herein, we investigated the behavioural and physiological responses to changes in air and microhabitat humidity in a terrestrial ectotherm, the asp viper (Vipera aspis). We exposed individuals to a simulated heatwave together with water deprivation for 3weeks, and manipulated air water vapour density (wet air vs. dry air) and microclimate (wet shelter vs. dry shelter) in a two-by-two factorial design. Dry air conditions led to substantial physiological dehydration and muscle wasting. Vipers exposed to dry air usedmore often a shelter thatoffered a moist microclimate, which reduced dehydration and muscle wasting at the individual level. These results provide the first experimental evidence that active behavioural hydroregulation can mitigate specific physiological stress responses caused by a dry spell in an ectotherm. Future studies investigating organismal responses to climate change should consider moisture gradient in the habitat and integrate both hydroregulation and thermoregulation behaviours.

Impact of invading species on biodiversity: Diet study of the green whip snake’s (Hierophis viridiflavus, L. 1789) in Switzerland

Next-generation sequencing is increasingly used in conservation biology to resolve complex interactions between species, either diet or gut parasites studies. We applied a recent long metabarcoding method to elucidate the green whip snake’s (Hierophis viridiflavus) prey consumption based on DNA extracted from stomach contents. Illegally introduced in Canton of Vaud (Switzerland), three populations of the green whip snake have strongly developed in two regions, East (Chablais) and North. We suspect that this introduced species is threatening part of the local herpetofauna, especially the Asp viper and the Western green lizard in this region. Consequently, an extermination program has been implemented from 2016 to mitigate Hierophis viridiflavus expansion and its impact arising from its generalist diet. Stomach contents of 94 individuals removed from introduction sites were analysed by long metabarcoding. Our study revealed the consumption of 67 prey belonging to 9 species, primarily small mammals and reptiles. The recurrent presence of two parasitic nematodes was also discovered. Although cannibalistic behaviour could not be highlighted with this approach, a scavenging behaviour was suspected based on the presence of an insect used in forensic entomology (Calliphora vicina). These results confirm the opportunistic feeding behaviour of Hierophis viridiflavus and its ability to predate on threatened species. Although 86.6 % of preys were not listed on the Swiss Red List, the impact on the Asp viper population can be important (up to 20 % of consumed preys) and could partially explain its strong decline.

Multiple paternity in the Asp viper

AbstractMany male reptiles maximize their reproductive success by mating with multiple females. This behaviour has often been observed in female reptiles as well, although one mating would usually be sufficient to fertilize the available female eggs. Using 13 microsatellite markers, multiple paternity (MP) was confirmed for the first time in the asp viper (Vipera aspis) in 47% of the tested clutches, with only up to two different fathers. Phenotypic characteristics (length, weight) of the mother did not influence the number of sires, and the number of young did not differ between litters with one or two sires. Males that sired offspring were larger than males that did not successfully reproduce. Excluding an exceptionally long‐distance movement (2464 m), the distance between fathers and mothers was limited (127 m ± 162). Although males exhibit notable combat behaviour during the breeding season, there was no sexual size dimorphism in the study population.

Use of a wireless ultrasound probe as a portable, noninvasive method for studying reproductive biology in the asp viper, Vipera aspis.

In this study, we investigated the use of wireless ultrasonography as an imaging system to study the reproductive ecology of the asp viper (Vipera aspis), a viviparous snake found in southwestern Europe. Female vipers were captured during the summer and immediately scanned to obtain an estimate of the number of embryos. Ultrasound imaging was performed with a pocket‐sized wireless ultrasound probe interfaced with a tablet with a dedicated app. Vipers were then released at the exact capture site after collecting data on body size and weight. We validate wireless ultrasonography as a non‐destructive, effective tool for ultrasonic investigations in the field. Wireless probes are light and compact, which facilitates carriage in rugged terrain. Moreover, the absence of cables simplifies the maneuvers to be made on a small, potentially dangerous snake. Importantly, ultrasound scans can be performed at the capture site, thus minimizing restraint time and handling of gravid females.

Rare genetic admixture and unidirectional gene flow between Vipera aspis and Vipera berus at their contact zone in western France

Abstract Asp vipers (Vipera aspis) and adders (Vipera berus) coexist in the Loire-Atlantique department in France where the two species reach their respective range limits. This contact zone is of special interest since hybridization has been recently discovered there. We carried out extensive sampling to further investigate the hybrid status of morphologically typical individuals and to evaluate the proportion of genetically admixed individuals in this area. Using microsatellite markers, no hybrids with typical morphological traits of either asp vipers or adders were detected. All recently investigated individuals with intermediate morphological traits were shown to be hybrids. A rather low proportion of genetically admixed individuals (1.5-3%) and a very small number of supposed second-generation hybrids suggest reduced fertility of first-generation hybrids or low viability of their progeny. The investigation of mtDNA of newly sampled hybrids support the finding that hybridization only occurs between female V. aspis and male V. berus. Several possible explanations for the unidirectional hybridization are discussed and consequent future studies suggested.

Two stressors are worse than one: combined heatwave and drought affect hydration state and glucocorticoid levels in a temperate ectotherm.

Heatwaves and droughts are becoming more intense and frequent with climate change. These extreme weather events often occur simultaneously and may alter organismal physiology, yet their combined impacts remain largely unknown. Here, we experimentally investigated physiological responses of a temperate ectotherm, the asp viper (Vipera aspis), to a simulated heatwave and drought. We applied a two-by-two factorial design by manipulating the daily temperature cycle (control versus heatwave) and the water availability (water available versus water deprived) over a month followed by exposure to standard thermal conditions with ad libitum access to water. Simulated heatwave and water deprivation additively increased mass loss, while water deprivation led to greater plasma osmolality (dehydration). Mass gain from drinking after the treatment period was higher in vipers from the heatwave and water-deprived group, suggesting that thirst was synergistically influenced by thermal and water constraints. Heatwave conditions and water deprivation also additively increased baseline corticosterone levels but did not influence basal metabolic rate and plasma markers of oxidative stress. Our results demonstrate that a short-term exposure to combined heatwave and drought can exacerbate physiological stress through additive effects, and interactively impact behavioral responses to dehydration. Considering combined effects of temperature and water availability is thus crucial to assess organismal responses to climate change.

Indigenous venomous snakebites in Switzerland: analysis of reports to the National Poisons Information Centre over 22 years.

Two venomous snakes, the asp viper (Vipera aspis) and the common adder (Vipera berus) are native to Switzerland. Bites by both vipers cause mainly local effects, but systemic envenomation is possible. We analysed all calls concerning indigenous venomous snakebites recorded at the Swiss National Poisons Information Centre between 1997 and 2018, including all cases with identification by a herpetologist, and/or with compatible symptoms and circumstances of the exposure. During the study period, 1,364 cases concerned snakebites. One third (466; 34%) were attributed to indigenous vipers. In 243 (52%) patients, medical follow-up information was available, with good causality between exposure and symptoms in 219 (90%) patients. Vipera aspis was identified in 77 of the cases (35%), Vipera berus in 54 (25%), and not further specified vipers in 88 (40%). In over two thirds of the 219 cases (155, 71%) adult patients were affected (male 109, female 46; median age 43 years [range 16-90]). Sixty-four patients were children (male 47, female 16; median age 11 years [range 1.3-15.9]). The highest occurrence of bites was in the summer months. In the majority of patients, the clinical course was mild (94; 43%) or moderate (80; 36%); a lower proportion was either asymptomatic (17; 8%) or exhibited severe symptoms (28; 13%). There were no fatalities reported. The most frequent symptoms were local effects at the bite site with mild (100; 46%) to moderate (56; 25%) swelling, pain (65; 30%) and redness (51; 23%). Gastrointestinal symptoms including nausea (31; 14%), vomiting (47; 22%) and abdominal pain (25; 11%) were also common. Other systemic symptoms included cardiovascular effects (e.g., hypotension (20; 9%) or shock [6; 3%]), neurotoxicity (e.g., visual impairment [5; 2.3%]) and haematotoxicity (e.g., coagulopathy [11; 5%]). Seven (3.2%) patients developed anaphylactic reactions. Antivenom was administered in only 20% (24 with moderate and 19 with severe symptoms) with good resolution of symptoms. The mean duration of hospitalization was 2 days (0-12 days). Snakebites in Switzerland can result in severe symptoms, sometimes necessitating antivenom treatment.

An evidence of asp viper (<em>Vipera aspis</em>) consumption by a western European hedgehog (<em>Erinaceus europaeus</em>) on Elba Island (Italy)

We report a record of consumption of an asp viper by a western European hedgehog. The observation took place in Elba Island, providing the first evidence for Italy and, to our knowledge, only the second ever in support to previous anecdotal accounts.