Natrix Helvetica Research Articles

Crabs as snake predators? An observation from southern Italy leading to a comprehensive review

The recent elevation of the Western Grass Snake, Natrix helvetica, from subspecies status prompted an assessment of its natural history and ecological traits compared to closely related species. We report an unusual predation attempt by the freshwater crab Potamon fluviatile on N. helvetica sicula from Sicily, indicating an ecological interaction previously overlooked in this species. The observation suggests that this crab may utilise snakes’ muscle tissue as an additional nutrient source. This predator-prey interaction, although probably rare, adds to the understanding of the dynamics between crabs and snakes, shedding light on their interaction in freshwater habitats. To provide context for our observation and highlight its rarity, we searched through scientific literature and online sources to generate a comprehensive review of the phenomenon that examines the predatory behaviour of crabs on snakes.

Patterns of spatial and temporal association between Zootoca vivipara, Anguis fragilis, Vipera berus and Natrix helvetica at artificial refuges

A 15-year data set of reptile observations at corrugated iron refuges was analysed to describe the spatial and temporal associations between species pairs of viviparous lizards Zootoca vivipara, slow worms Anguis fragilis, northern vipers Vipera berus and grass snakes Natrix helvetica. Of the two snake species, only the viper is known as a routine lizard predator. We analysed two variables expressing pairwise reptile associations at refuges. The first analysis was of monthly spatial overlap assessed as the proportion of unique refuge positions used in common, but not necessarily used simultaneously. The second analysis was of a more precise spatial and temporal assessment based on counts of reptile pairs cohabitating at the refuges (i.e. using the same refuges simultaneously). Apart from viviparous lizards paired with either of the two snake species, the frequencies for both variables were either as expected or significantly greater than expected by chance; in particular grass snakes cohabited much more frequently than expected with both vipers (+327%) and slow worms (+218%). In contrast, for the viviparous lizard/viper pair both variables were statistically significantly less frequent than expected by chance - monthly overlap (-35%) and cohabitation (-87%). As viviparous lizards are predated by vipers, cohabiting would be much reduced but the significantly lowered monthly spatial overlap may indicate active avoidance. For the viviparous lizard/grass snake pair the spatial overlap was as expected by chance but, as with vipers, the frequency of cohabiting was significantly less than expected by chance (-75%). These observations are discussed in relation to the known kairomonal responses of this lizard to viper and grass snake deposits. Viper deposits are also believed to act as a kairomone for slow worms, but we found no evidence that they avoided vipers, supporting existing literature showing that V. berus is unlikely to be an important slow worm predator. Keywords: species associations, cohabitation, corrugated iron refuges, viper kairomone, chalk grassland

Melanin-based color variation in response to changing climates in snakes.

Melanism, the process of heavier melanin deposition, can interact with climate variation at both micro and macro scales, ultimately influencing color evolution in organisms. While the ecological processes regulating melanin production in relation to climate have been extensively studied, intraspecific variations of melanism are seldom considered. Such scientific gap hampers our understanding of how species adapt to rapidly changing climates. For example, dark coloration may lead to higher heat absorption and be advantageous in cool climates, but also in hot environments as a UV or antimicrobial protection mechanism. To disentangle such opposing predictions, here we examined the effect of climate on shaping melanism variation in 150 barred grass snakes (Natrix helvetica) and 383 green whip snakes (Hierophis viridiflavus) across Italy. By utilizing melanistic morphs (charcoal and picturata in N. helvetica, charcoal and abundistic in H. viridiflavus) and compiling observations from 2002 to 2021, we predicted that charcoal morphs in H. viridiflavus would optimize heat absorption in cold environments, while offering protection from excessive UV radiation in N. helvetica within warm habitats; whereas picturata and abundistic morphs would thrive in humid environments, which naturally have a denser vegetation and wetter substrates producing darker ambient light, thus providing concealment advantages. While picturata and abundistic morphs did not align with our initial humidity expectations, the charcoal morph in N. helvetica is associated with UV environments, suggesting protection mechanisms against damaging solar radiation. H. viridiflavus is associated with high precipitations, which might offer antimicrobial protection. Overall, our results provide insights into the correlations between melanin-based color morphs and climate variables in snake populations. While suggestive of potential adaptive responses, future research should delve deeper into the underlying mechanisms regulating this relationship.

Detection of Ophidiomyces ophidiicola in wild barred grass snakes (Natrix helvetica) in the Netherlands

Ophidiomyces ophidiicola is the causative agent of ophidiomycosis (also called snake fungal disease) and has been associated with mycosis in individual snakes and population declines in several North American snake species. While cases of ophidiomycosis from North America have been numerous in the past two decades, reports from Europe remain sparse and are lacking from the Benelux. Between 2017 and 2023, sloughed skins, carcasses and swabs from 284 freeranging, captive and introduced snakes belonging to 22 species were screened for the presence of O. ophidiicola in the Netherlands. Two free-ranging barred grass snakes’ (Natrix helvetica) shed skin sloughs tested positive despite a lack of gross cutaneous signs of disease. These findings are presented in this article. To the authors’ knowledge, this is the first report of the presence of O. ophidiicola in the Netherlands.

Characterisation, prevalence and severity of skin lesions caused by ophidiomycosis in a population of wild snakes

Ophidiomycosis is an emerging infectious disease affecting wild snakes in the Northern Hemisphere. Recently confirmed in Great Britain, the prevalence, severity and significance of ophidiomycosis has yet to be characterised in free-living snakes at a population level in Europe. Therefore, a population of barred grass snakes (Natrix helvetica) in eastern England was monitored for three seasons (May 2019 to October 2021), to investigate the prevalence (25.5%; 191/750 snakes) and severity of skin lesions and their aetiology. The most frequently observed skin lesion characteristics were changes in scale colour, crusting, and scale margin erosion. The majority of such lesions (96.9%; 185/191 snakes) was observed on the ventral surface along the length of the body. The severity of skin lesions was considered mild in more than half of the cases (53.1%; 98/191 snakes). Predominantly, skin lesions were observed in adult snakes (72.8%; 139/191 snakes). Combined histological examinations and qPCR tests of skin lesions from N. helvetica sloughs and/or carcasses confirmed a diagnosis of ophidiomycosis. Further targeted surveillance, supported by molecular and histological examinations to confirm skin lesion aetiology, is required to determine the extent to which our findings reflect the occurrence of ophidiomycosis in populations within wider landscapes.

The Endangered Sardinian Grass Snake: Distribution Update, Bioclimatic Niche Modelling, Dorsal Pattern Characterisation, and Literature Review.

The Sardinian grass snake, Natrix helvetica cetti, is an endangered endemic snake subspecies with a restricted and highly fragmented geographic distribution. Information on its ecology and detailed geographic distribution are scarce and may negatively impact on its conservation status. Therefore, a literature review on its taxonomy, morphology, ecology, and conservation is presented here. Moreover, field records from the authors, citizen science and the existing literature provide an updated geographic distribution highlighting its presence within 13 new and 7 historic 10 × 10 km cells. Bioclimatic niche modelling was then applied to explore patterns of habitat suitability and phenotypic variation within N. h. cetti. The geographic distribution of the species was found to be positively correlated with altitude and precipitation values, whereas temperature showed a negative correlation. Taken together, these outcomes may explain the snake's presence, particularly in eastern Sardinia. In addition, analysis of distribution overlap with the competing viperine snake (N. maura) and the urodeles as possible overlooked trophic resources (Speleomantes spp. and Euproctus platycephalus) showed overlaps of 66% and 79%, respectively. Finally, geographical or bioclimatic correlations did not explain phenotypic variation patterns observed in this highly polymorphic taxon. Perspectives on future research to investigate N. h. cetti's decline and support effective conservation measures are discussed.

Screening of Ophidiomyces ophidiicola in the free-ranging snake community annually harvested for the popular ritual of San Domenico e dei Serpari (Cocullo, AQ, Italy)

In the Abruzzi village of Cocullo (Italy), each year, on May 1st, local snake hunters (known as Serpari) display colubrids, captured in the wild, to commemorate the ancient ritual of San Domenico. The ascomycete Ophidiomyces ophidiicola (Oo) is the causative agent of ophidiomycosis, an emerging disease with sublethal effects. Skin lesions, such as dysecdysis, edematous, crusty or necrotic scales, swellings, nodules, and ulcers, are the most common clinical manifestation of the disease. The pathogen and its associated disease are well characterized in wild snakes in North America, whereas broad screenings of free ranging wild ophidians in Europe are rare. In 2019, as part of a multi-year snake health monitoring project, all the Cocullo ophidians were carefully examined for integumentary affections and those showing signs consistent with ophidiomycosis were dry swabbed on the skin and on any visible cutaneous lesions with a single applicator. The extracted DNA underwent a broad-range panfungal PCR targeting the D1-D2 region, as well as two conventional PCRs specific to the ITS2 and IGS regions of Oo DNA. Twenty-three out of 129 snakes (13/82 Elaphe quatuorlineata; 7/31 Hierophis viridiflavus; 3/15 Zamenis longissumus; 0/1 Natrix helvetica) resulted clinically affected, but no specific Oo genomic DNA was detected by PCR. The Cocullo ritual celebration provided a unique opportunity for the first systematic testing of a large sample size of a local snake community for the monitoring of this pathogen in Italy.

High-Density Geometric Morphometric Analysis of Intraspecific Cranial Integration in the Barred Grass Snake (Natrix helvetica) and Green Anole (Anolis carolinensis).

How do phenotypic associations intrinsic to an organism, such as developmental and mechanical processes, direct morphological evolution? Comparisons of intraspecific and clade-wide patterns of phenotypic covariation could inform how population-level trends ultimately dictate macroevolutionary changes. However, most studies have focused on analyzing integration and modularity either at macroevolutionary or intraspecific levels, without a shared analytical framework unifying these temporal scales. In this study, we investigate the intraspecific patterns of cranial integration in two squamate species: Natrix helvetica and Anolis carolinensis. We analyze their cranial integration patterns using the same high-density three-dimensional geometric morphometric approach used in a prior squamate-wide evolutionary study. Our results indicate that Natrix and Anolis exhibit shared intraspecific cranial integration patterns, with some differences, including a more integrated rostrum in the latter. Notably, these differences in intraspecific patterns correspond to their respective interspecific patterns in snakes and lizards, with few exceptions. These results suggest that interspecific patterns of cranial integration reflect intraspecific patterns. Hence, our study suggests that the phenotypic associations that direct morphological variation within species extend across micro- and macroevolutionary levels, bridging these two scales.

Assessing habitat connectivity in environmental impact assessment: a case-study in the UK context

ABSTRACT Ecological connectivity across landscapes is vital for the maintenance of biodiversity and the processes that enable life on earth. Despite this, environmental planning decisions are usually made at the scale of individual projects, failing to account for landscape-scale impacts. Incorporating habitat connectivity analysis in Environmental Impact Assessments (EIAs) could provide an opportunity to address this gap. We present a novel approach to model habitat connectivity in an EIA undertaken for the Heathrow Third Runway Expansion Project, a proposed development in south-east England. Drawing on field data, remote sensing, and species-specific literature reviews, a circuit theory approach was used to assess functional connectivity across the project landscape for grass snakes Natrix helvetica and soprano pipistrelles Pipistrellus pygmaeus. Results indicated key areas for species movement and potential ‘pinch-points’ vulnerable to development impacts. We discuss lessons learnt, potential applications to inform impact assessment, mitigation design, and biodiversity net gain approaches, and further work required to mainstream connectivity analyses in EIA and decision-making.

How landscape and biotic interactions shape a Mediterranean reptile community

ContextDisentangling the effect of environment and biological interaction on community composition with observational data, within the environmental filtering framework, is challenging because the two processes produce non independent results.ObjectivesAdopting community N-mixture models with symmetric interactions, we aimed at estimating differential effects of landscape structure and biotic interactions on the local abundance of a Mediterranean reptile community including four lizards (Lacerta bilineata; Podarcis siculus; P. muralis; Chalcides chalcides) and two snakes (Hierophis viridiflavus; Natrix Helvetica).MethodsWe sampled reptiles for three consecutive years (2019–2021; 4 surveys/year) on 52 linear transects on a Mediterranean coastal landscape. We analyzed count data by means of a multi-species N-mixture model with symmetric interactions. Interactions within pair of species were estimated from the residual correlation of their realized abundances, after accounting for four landscape features: landscape heterogeneity calculated from land cover data, edge density of woody vegetation patches, tree cover density, net primary productivity.ResultsMost species displayed very low detection probability (p ~ 0.10). All species responded with different intensity and sensitivity to landscape predictors. Two biological interactions resulted significant: L. bilineata and P. siculus showed a positive interaction, while P. muralis and C. chalcides displayed a negative interaction.ConclusionsUsing community N-mixture models we demonstrated that, also with observational data obtained from a realized community, partitioning the filtering process of the landscape from the one of biotic interactions is possible.

An updated check-list of Italian amphibians and reptiles

This paper represents an update of the list of Italian amphibians and reptiles published 15 years ago by Razzetti et al. (2006) and of the checklist published in 1993 by the late Benedetto Lanza. At present, the Italian herpetofauna includes 101 species (41 amphibians and 60 reptiles) and an amphibian taxon of hybrid origin. Seven species and one subspecies are allochthonous and became naturalized within the last century. Since the last published list, a new species has been described (Vipera walser), five taxa have been raised to species rank (Salamandrina perspicillata, Speleomantes sarrabusensis, Zootoca carniolica, Malpolon insignitus and Natrix helvetica) while three taxa have been downgraded to subspecies. All the relevant taxonomic changes based upon new research have been discussed, including tentative revisions and controversial taxa. Nine species reported or listed dubitatively in Lanza’s 1993 list are excluded here.

Predation and ingestion of a barred grass snake Natrix helvetica by a rainbow trout Oncorhynchus mykiss in Lot, France

Predation and ingestion of a barred grass snake Natrix helvetica by a rainbow trout Oncorhynchus mykiss in Lot, France

Transalpine dispersal: Italian barred grass snakes in southernmost Bavaria—This far but no further!

Based on 1031 samples of grass snakes from Central Europe, we examine the recently reported occurrence of the southern subspecies of the barred grass snake (Natrix helvetica sicula) in southern Bavaria, Germany. Using 13 microsatellite loci and mtDNA coding for the cytb gene and the partial ND4 gene plus adjacent tRNAs, we show that N. h. sicula is restricted to a few river valleys (Inn, Isar, Loisach) in southernmost Bavaria and adjacent Tyrol, Austria. At the widening of the river valleys into the pre-Alpine plains, N. h. sicula hybridizes locally with the common grass snake (Natrix natrix) in a bimodal hybrid zone. Our study provides evidence that Central Europe was colonized by Natrix helvetica over two distinct immigration routes. In addition to the previously known western route of the nominotypical subspecies, leading to the colonization of the Rhine region, N. h. sicula crossed the Alps, most likely using the Brenner Pass and/or the Reschen Pass. Our study underlines that the Alps are not an impermeable biogeographic barrier, as often assumed. North of the Alps, the combination of geographic setting (occurrence of N. h. sicula in sheltered Alpine valleys) and population-density-dependent blocking of immigrants by the resident species (N. natrix), acting in concert with intrinsic genetic factors, prevented the formation of a geographically more extended hybrid zone. Unlike N. helvetica, the two subspecies of N. natrix hybridize north of the Alps broadly, in accordance with their better genetic compatibility. Many populations of the resident Central European subspecies (Natrix natrix natrix) have been “genetically swamped” by Natrix natrix vulgaris immigrating from the Balkans. This led to the complete replacement of N. n. natrix by N. n. vulgaris in some regions, where today only the mtDNA of the nominotypical subspecies persists.

Behavioural interactions between barred grass snake Natrix helvetica and northern viper Vipera berus

Behavioural interactions between barred grass snake Natrix helvetica and northern viper Vipera berus

How often do they do it? An in-depth analysis of the hybrid zone of two grass snake species (Natrix astreptophoraandNatrix helvetica)

AbstractWe examined the contact zone of two parapatric species of grass snake (Natrix astreptophora and Natrix helvetica) in southern France. To this end, we used comprehensive sampling, analysed mtDNA sequences and microsatellite loci, and built Species Distribution Models for current and past climatic conditions. The contact zone had established by the mid-Holocene during range expansions from glacial refuges in the Iberian Peninsula (N. astreptophora) and southern or western France (N. helvetica). The contact zone represents a narrow bimodal hybrid zone, with steep genetic transition from one taxon to the other and rare hybridization, supporting species status for N. astreptophora and N. helvetica. Our results suggest that the steepness of the clines is a more robust tool for species delimitation than cline width. In addition, we discovered in western France, beyond the hybrid zone, a remote population of N. helvetica with genetic signatures of hybridization with N. astreptophora, most likely the result of human-mediated long-distance dispersal. For N. helvetica, we identified a southern and a northern population cluster, connected by broad-scale gene flow in a unimodal hybrid zone running across France. This pattern either reflects genetic divergence caused by allopatry in two microrefuges and subsequent secondary contact or introgression of foreign alleles into the southern cluster.

The valid scientific names of the barred grass snake and its subspecies from mainland Italy and Sicily

Abstract To stabilize current nomenclature, Coluber helveticus Lacepède, 1789 and Coluber siculus Cuvier, 1829 are qualified as nomina protecta to ensure the usage of the established names Natrix helvetica (Lacepède, 1789) and Natrix helvetica sicula (Cuvier, 1829) for the barred grass snake. For the same reason, Coluber bipes Gmelin, 1789, Coluber tyrolensis Gmelin, 1789 and Coluber scopolianus Daudin, 1803, all with type locality Dolomiti di Fiemme (Italy), are declared as nomina oblita according to Article 23.9 of the International Code of Zoological Nomenclature (1999). Coluber helveticus Lacepède, 1789 was originally introduced as a replacement name for Coluber vulgaris Razoumowsky, 1789 (type locality: Jorat, Switzerland). However, the latter name becomes a junior secondary homonym of Natrix vulgaris Laurenti, 1768 when transferred to the genus Natrix and thus, according to Articles 57 and 59 of the Code, invalid and does not threaten the usage of Natrix helvetica for the barred grass snake.

Mitochondrial ghost lineages blur phylogeography and taxonomy of Natrix helvetica and N. natrix in Italy and Corsica

AbstractGrass snakes are widely distributed across the Western Palearctic. Recent phylogeographic studies provided evidence that three distinct parapatric species exist. Two of these occur in Italy, Natrix helvetica and N. natrix, and a contact zone between both taxa has been suggested for north‐eastern Italy. Moreover, previous investigations revealed for the Italian Peninsula a complex phylogeographic structure. Using mtDNA sequences and microsatellite loci, we examined the situation for mainland Italy, Sicily, Sardinia, and Corsica. Our study confirmed the occurrence of N. natrix in north‐eastern Italy. Cline analyses revealed limited gene flow between N. helvetica and N. natrix across a narrow hybrid zone. Within N. helvetica, conflicting patterns of mitochondrial and nuclear genomic differentiation were revealed. Three nuclear genomic clusters were found; one of them corresponded to no fewer than five distinct and, in part, deeply divergent and ancient mitochondrial lineages from mainland Italy and Sicily. This cluster was paraphyletic with respect to the two remaining mitochondrial lineages, each of which matched with another nuclear genomic cluster (one from Corsica plus Sardinia and another one from western Europe north of the Alps). This unexpected pattern most likely results from mainly male‐mediated gene flow and female philopatry combined with population‐density‐dependent processes such as ‘high‐density blocking’. With respect to taxonomy, we propose to synonymize N. h. lanzai Kramer, 1970 with N. h. sicula (Cuvier, 1829), acknowledging their lacking nuclear genomic differentiation. The studied hybrid zone of N. h. helvetica and N. h. sicula in Italy is wide, with a smooth cline for nuclear markers, supporting their subspecies status. We found no evidence for the distinctiveness of the two subspecies from Corsica (N. h. corsa) and Sardinia (N. h. cetti), suggesting their synonymy, but refrain from taxonomic conclusions because of small sample sizes and the endangered status of the Sardinian taxon.

Snakes and the Eternal City: variation in community metrics, body size and population density of snakes in contrasted landscapes of suburban Rome (Italy)

Reports of global declines in animal populations are now numerous and also include snakes, a group of animals now widely regarded as bio indicators. A prerequisite for any conservation management plan to protect or restore snake populations requires a data base that provides insight into population composition and changes. However, snakes are well known to be particularly difficult to quantitatively sample due to their secretive and elusive nature, and hence accumulating an adequate database for analysis requires long-term field studies that involve intensive searches. Populations of four snake species, Zamensis longissimus, Natrix helvetica, Vipera aspis and Hierophis viridiflavus living in two suburban areas of Rome with different extents of habitat alteration (deforestation), Vejo, a less altered site, and Tor Bella Monaca, a high altered site, have been monitored, but with interruptions since 1995. The results indicated that H. viridiflavus was the commonest species at both sites. Male bias was found in all four species but especially in Z. longissimus and V. aspis with detection of juveniles greatest in H. viridiflavus and N. helvetica. Snout to vent lengths (SVL) of H. viridiflavus and Z. longissimus, which were present at both sites, were greater at the less degraded habitat of the two study localities. Community metrics indicated that the degraded habitat had lower species richness, evenness, Shannon and Simpson diversity indices, but a higher dominance index. Recapture frequencies of snakes recaptured either once or multiple times were in general greater at Vejo. The highest population densities were found in H. viridiflavus, followed by V. aspis and N. helvetica, which were similar. However, long term trends in densities show declines in V. aspis and N. helvetica between 1995 and 2019. Population densities were in good agreement with density estimates found in previous studies of snakes in more natural habitats.

A reference DNA barcode library for Austrian amphibians and reptiles.

In the last few years, DNA barcoding became an established method for species identification in biodiversity inventories and monitoring studies. Such studies depend on the access to a comprehensive reference data base, covering all relevant taxa. Here we present a comprehensive DNA barcode inventory of all amphibian and reptile species native to Austria, except for the putatively extinct Vipera ursinii rakosiensis and Lissotriton helveticus, which has been only recently reported for the very western edge of Austria. A total of 194 DNA barcodes were generated in the framework of the Austrian Barcode of Life (ABOL) initiative. Species identification via DNA barcodes was successful for most species, except for the hybridogenetic species complex of water frogs (Pelophylax spp.) and the crested newts (Triturus spp.), in areas of sympatry. However, DNA barcoding also proved powerful in detecting deep conspecific lineages, e.g. within Natrix natrix or the wall lizard (Podarcis muralis), resulting in more than one Barcode Index Number (BIN) per species. Moreover, DNA barcodes revealed the presence of Natrix helvetica, which has been elevated to species level only recently, and genetic signatures of the Italian water frog Pelophylax bergeri in Western Austria for the first time. Comparison to previously published DNA barcoding data of European amphibians and reptiles corroborated the results of the Austrian data but also revealed certain peculiarities, underlining the particular strengths and in the case of the genus Pelophylax also the limitations of DNA barcoding. Consequently, DNA barcoding is not only powerful for species identification of all life stages of most Austrian amphibian and reptile species, but also for the detection of new species, the monitoring of gene flow or the presence of alien populations and/or species. Thus, DNA barcoding and the data generated in this study may serve both scientific and national or even transnational conservation purposes.

Distribution and hybridisation of barred and common grass snakes (Natrix helvetica, N. natrix) in Baden-Württemberg, South-western Germany

The distribution and hybridisation zone of the two grass snake species occurring in the German state of Baden-Württemberg are described, based on genetic data from maternally inherited mitochondrial DNA (mtDNA, up to 1983 bp) and biparentally inherited microsatellite DNA (13 loci). In agreement with previously published morphological evidence, the barred grass snake (Natrix helvetica) occurs in the Upper Rhine Valley and the Black Forest, while the common grass snake (N. natrix, ‘yellow lineage’) is distributed across the remaining, more eastern parts of Baden-Württemberg. Cline analyses across two transects running through the region of Karlsruhe and the Black Forest indicate that the hybrid zone is similarly narrow here as in the previously characterised stretch near Lake Constance. With respect to nuclear DNA, the Black Forest constitutes no impediment to gene flow in comparison with lowland regions (Karlsruhe, Lake Constance). However, on the eastern slope of the Black Forest, the abrupt replacement of mtDNA ofN. helveticaby that ofN. natrixindicates male-mediated gene flow and that the Black Forest represents a dispersal barrier for female grass snakes.