Rare colour morphs in the slow worm Anguis fragilis in Norway

Simple SummaryIntraspecific interactions are known to affect habitat use in birds and mammals but their role in spatial ecology of reptiles is far less recognized. Our comparative study shows that species known to exhibit intraspecific predation (smooth snake Coronella austriaca) express clearly different patterns of habitat and shelter occupancy than a species with no such cannibalistic behavior (slow worm Anguis fragilis). Specifically, juvenile smooth snakes prefer sites and shelters not occupied by the adults, even despite suboptimal habitat conditions. We propose that such division indicates an avoidance of predation pressure set by larger individuals on the younger and smaller ones. On the contrary, in slow worms no tendency for intraspecific avoidance are observed, since specimens of different ages commonly share the same area and shelters. This points to higher flexibility in habitat use in slow worms, while the smooth snake population is spatially structured, with juveniles dispersed to the margins of the population range. For endangered smooth snakes, habitat conservation should therefore include a wide buffer zone to maintain the youngest fraction of the population. Future studies on habitat utilization in squamates needs to pay more attention to the social cues, a commonly overlooked aspect in the spatial ecology of reptiles.Reptiles undergo worldwide decline driven mostly by habitat change. Detailed recognition of factors underlying spatial structure and habitat utilization is therefore a prerequisite of effective conservation of this group. While the body of data on spatial ecology of reptiles is rapidly growing, studies on social factors remain still underrepresented. We studied age-specific patterns of shelter use, range size, and habitat preferences in the context of intraspecific interactions in the smooth snake Coronella austriaca—known to exhibit intraspecific predation—and the limbless lizard slow worm Anguis fragilis—with no such behavior observed. Despite smaller availability of preferred microhabitats, juveniles of smooth snakes occupied habitat and shelters located at the edge of the population range that did not overlap with adults. No such pattern was observed in the slow worm. Our study indicates that intraspecific interactions affect the spatial ecology of squamates. Passive and active protection of habitat must include wide buffers to preserve the poorly detectable young fraction of the population.

The bone remains of amphibians, reptiles and small mammals from the loose sediments of the entrance grotto of the Grebnevaya cave (the middle reaches of the Yuryuzan River, Southern Urals) were studied. Amphibians are represented by Bufo sp., Pelophylax ridibundus and Rana cf. temporaria. Reptiles — Anguis fragilis, Lacerta cf. agilis, Zootoca vivipara, Coronella austriaca, Natrix sp., Vipera berus. The identified species composition of amphibians and reptiles from the locality consists of species characteristic of various biotopes of the mountainous part of the Southern Urals from the early Holocene to the present. In the earlier deposits of the cave (layer 3), remains of Microtus (Stenocranius) gregalis, Alexandromys oeconomus, Arvicola amphibius predominate; single remains of Allactaga major and Dicrostonyx torquatus were found. The second layer is dominated by remains of Arvicola amphibius, Microtus arvalis and Alexandromys oeconomus. Ochotona pusilla, Cricetulus migratorius, Lagurus lagurus, Microtus (Stenocranius) gregalis and a few Sorex sp., Apodemus ex gr. uralensis-agrarius, Cricetus cricetus, Myodes ex gr. glareolus–rutilus. The youngest layer 1 is dominated by remains of Microtus arvalis, Sorex sp., Myodes ex gr. glareolus–rutilus and Arvicola amphibius. Pteromys volans, Sciurus vulgaris, Apodemus flavicollis, Ochotona pusilla, Cricetulus migratorius, Allocricetulus eversmanni, Lagurus lagurus and Microtus (Stenocranius) gregalis were identified. A change in the ecological groups of small mammals is observed in the locality. In layer 3, the proportion of forest and meadow species is small, and the proportion of steppe species is significant, which is typical for the middle and early Holocene of the mountainous part of the Southern Urals. In layer 3, remains of lemmings were found, a tundra species characteristic of the early Holocene. The first layer is characterized by a significant proportion of forest and meadow species, but typical steppe species are also present. The accumulation of bone remains of small mammals in the Grebnevaya Cave location probably occurred at the end of the early and middle Holocene. The near-surface deposits of the first layer are enriched with species more characteristic of the late Holocene and modern times. Изучены костные остатки земноводных, пресмыкающихся и мелких млекопитающих из рыхлых отложений привходового грота пещеры Гребневая (среднее течение р. Юрюзань, Южный Урал). Земноводные представлены Bufo sp., Pelophylax ridibundus и Rana cf. temporaria. Пресмыкающиеся — Anguis fragilis, Lacerta cf. agilis, Zootoca vivipara, Coronella austriaca, Natrix sp., Vipera berus. Выявленный видовой состав земноводных и пресмыкающихся из местонахождения состоит из видов, характерных различным биотопам горной части Южного Урала с раннего голоцена и до современности. В более ранних отложениях пещеры (слой 3) преобладают остатки Microtus (Stenocranius) gregalis, Alexandromys oeconomus, Arvicola amphibius, обнаружены единичные остатки Allactaga major и Dicrostonyx torquatus. Во втором слое преобладают остатки Arvicola amphibius, Microtus arvalis и Alexandromys oeconomus. Определены Ochotona pusilla, Cricetulus migratorius, Lagurus lagurus, Microtus (Stenocranius) gregalis и немногочисленные Sorex sp., Apodemus ex gr. uralensis-agrarius, Cricetus cricetus, Myodes ex gr. glareolus-rutilus. В наиболее молодом слое 1 преобладают остатки Microtus arvalis, Sorex sp., Myodes ex gr. glareolus–rutilus и Arvicola amphibius. Определены Pteromys volans, Sciurus vulgaris, Apodemus flavicollis, Ochotona pusilla, Cricetulus migratorius, Allocricetulus eversmanni, Lagurus lagurus и Microtus (Stenocranius) gregalis. В местонахождении наблюдается смена экологических групп мелких млекопитающих. В слое 3 доля лесных и луговых видов невелика, а доля степных видов значительна, что характерно для среднего и раннего голоцена горной части Южного Урала. В слое 3 обнаружены остатки лемминга — тундрового вида, характерного для раннего голоцена. Первый слой характеризуется значительной долей лесных и луговых видов, но присутствуют и типично степные виды. Накопление костных остатков мелких млекопитающих в местонахождении пещера Гребневая происходило, вероятно, в конце раннего и в среднем голоцене. Приповерхностные отложения первого слоя обогащены видами более характерными для позднего голоцена и современности.

Skin structure of the slow worm lizard Anguis fragilis (Anguidae, Sauria, Reptilia) with emphasis on the epidermal micro‐ornamentation in relation to the animal movements (Acta Zoologica, Stockholm). The structure of the skin and superficial micro‐ornamentation in the slow worm Anguis fragilis, a limbless lizard with a fossorial activity, was examined using histology, immunofluorescence, scanning and transmission electron microscopy. The scales, with a triangular to trapezoidal shape, are very overlapped and interlocked to form a smooth surface and are reinforced by osteoderms. The epidermis shows a thin Oberhautchen layer merged with a thicker beta‐layer that contains corneous beta‐proteins. The SEM survey detects a smooth surface made of tile‐like patterned Oberhautchen cells with irregular perimeters that form an interlocking surface. Disk‐like sensory organs of 15–20 μm diameter are observed only on the head scales, the first to sense the environment and contact the ground. Numerous Oberhautchen denticles, namely corneous thorns of about 0.2–0.3 μm, adorn the caudally directed perimeter of Oberhautchen cells in the ventral scales of the trunk and tail. This microstructure may determine gripping and increased friction with the substrate during the lateral undulating and forward movements of the slow worm. TEM observations reveal sparse short serrated protrusions of Oberhautchen cells that are largely merged with the underlying beta‐cells. Altogether, the scale surface of the slow worm efficiently suites this limbless lizard to its environment and lifestyle.

The metal-responsive transcription factor-1 (MTF-1) is a key regulator of heavy metal homeostasis and detoxification. Here we characterize the first MTF-1 from a reptile, the slow worm Anguis fragilis. The slow worm, or blind worm, is a legless lizard also known for its long lifespan of up to several decades. Anguis MTF-1 performs well and matches the strong zinc and cadmium response of its human ortholog, clearly surpassing the activity of rodent MTF-1s. Some amino acid positions critical for metal response are the same in humans and slow worm but not in rodent MTF-1. This points to a divergent evolution of rodent MTF-1, and we speculate that rodents can afford a less sophisticated metal handling than humans and (some) reptiles.

Disease problems caused by viral or bacterial pathogens are common in reptiles kept in captivity. There is no information available on the incidence of viral pathogens or the physiological cloacal bacterial flora of common free-living reptiles in Germany. Therefore, 56 free-living reptiles including 23 European adders (Vipera berus), 12 grass snakes (Natrix natrix) and 21 slow worms (Anguis fragilis) were investigated on the island Hiddensee in northeastern Germany. Pharyngeal and cloacal swabs were taken immediately after capture. Bacteriological examination was performed from the cloacal swabs to study the aerobic cloacal flora. Molecular biological examination included amplification of DNA or RNA from adeno-, rana- and ferlaviruses as well as culturing on Russell's viper heart cells for virus isolation. Salmonella spp. were isolated from European adders but not from the other reptiles examined. The minimal inhibitory concentration was determined from the isolated Salmonella spp. However, some potentially human pathogenic bacteria, such as Proteus vulgaris, Aeromonas hydrophila, Klebsiella pneumoniae and Escherichia coli were isolated. Viruses were not detected in any of the examined reptiles. To the authors' best knowledge, the present study is the first survey of viral pathogens in free-living snakes and slow worms in Germany and the first survey of cloacal aerobic bacterial flora of slow worms.

North Sweden ('Norrland' in Swedish) covers 243000 km2 and lies mainly in the boreal biome. The herpetofauna comprises five amphibian and four reptile species: Lissotriton vulgaris, Triturus cristatus, Bufo bufo, Rana temporaria, Rana arvalis, Zootoca vivipara, Anguis fragilis, Natrix natrix, and Vipera berus. Successful conservation and management of amphibians and reptiles depend on accurate information about distribution, habitat affinities, and abundance. Such knowledge is also essential as a benchmark to assess changes in distribution and abundance that may come about as a result of climate change and human habitat alteration. This paper aims to present accurate distribution maps, describe habitat affinities, and provide abundance estimates for the herpetofauna of North Sweden for the period 1970-2022. Distribution data are presented by traditional faunistic provinces, as well as by biotic regions and alpine life zones. Separate sections address post-glacial colonization and a herpetological perspective on anthropogenic changes in relation to species´ present status. Bufo bufo, Rana temporaria, Rana arvalis, Zootoca vivipara, and Vipera berus are widely distributed throughout the boreal sub-regions. Rana temporaria, Zootoca vivipara, and Vipera berus also extend into the alpine region. Triturus cristatus, Anguis fragilis, and Natrix natrix occur mainly in the coastal parts of the Southern Boreal region. There are no signs of recent changes in distribution range, but Lissotriton vulgaris, Triturus cristatus, and Rana arvalis have been largely overlooked in the past and have a much wider occurrence than previously recognized. Most species are found in habitats usually not described in all-European field guides. Nearly all anurans hibernate in water. Abundance estimates suggest that some species are more common in the boreal than thought, supporting the notion that a large share of their total European population occurs there. Although local extinctions and declines are known, there are no signs of widespread population decline for any species during the study period.

The role of managed coniferous forest in the conservation of reptiles

The results of the research of the current state of reptiles in Western Podillia were presented. Morphometric traits were described; habitat, spread and number of 9 reptile species belonging to 2 lines and 5 families were studied. The regional extinction of Elaphe longissima, which was at the edge of the habitat, was identified. It has been established that the borders of habitats are in the territory of Western Podillia: for Natrix tessellata and Lacerta.viridis – the northern one, for Lacerta vivipara – the southern one.The survey of the found species was made. It was shown that Lacerta agilis appeared to be the most numerous species among reptiles, although its number decreased due to human transformed natural habitats.Such species as Emys orbicularis, Anguis fragilis, Lacerta viridis, Lacerta vivipara, Coronella austriaca and Vipera berus are in a dangerous situation. These species are found sporadically, and there are all reasons to consider them as those which have decreased their number considerably.Natrix natrix and Natrix tessellata are common species. The analysis of reptile occurrence within the region of research has shown that, as to their number, species gravitate to the east and south-east of the region, covering the areas along the left bank of the Dniester River (“Dnistrovskyi canyon”) in Western Podillia Prydnistrovia (administrative territories of Zalishchyky, Bucha, Borshchiv districts of Ternopil region). In Tovtry ridge, they mostly concentrate in the territories of Zbarazh, Pidvolochysk, Husiatyn districts of Ternopil region and Kamianets-Podilsk and Chemerov districts of Khmenlnytskyi region.It is worth mentioning that the area with the highest reptile occurrence coincides with that of reserve “Medobory” and to a lesser degree with the territory of NNP “Podilski Tovtry”. To a great extent the area of reptile concentration coincides with the territory of natural park “Dnistrovskyi canyon”, in particular, closer to the hills of the Dniester River on a tract Beramiany – Ustechko, Zalishchyky – Kasperivtsi (Obizhev and Kasperivskyi reserves) and the outskirts of Dzvenyhorod village, Borshchiv district. In general, the state of reptiles in the region tends to the reduction of the number and diversity of these representatives.

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

Field surveys of rare and elusive reptiles often encounter the problem of low detectability. Therefore, several techniques have been invented to improve detection probability and artificial cover objects (ACOs) are among the most commonly used in reptile studies. However, the methodological effectiveness of ACOs has been rarely evaluated and focused mostly on spatial aspects. The temporal dimension of the ACOs effectiveness remains still understudied, despite well-known seasonal variation in reptile activity patterns. Here, we examined seasonal and between-year variation in the fraction of occupied ACOs, as a proxy for detectability, in two elusive reptile species, the slow worm Anguis fragilis and smooth snake Coronella austriaca. We found that the use of ACOs was species-specific and showed high temporal variation. In the case of smooth snakes, monthly usage varied between years; specifically within-year variation of the proportion in occupied ACOs was most pronounced in 2015, but seems vanishing in consecutive years. This loss of of seasonal pattern occurs only in the last year of survey in the case of slow worm and monthly use of ACOs seem not to vary between years. Considerably low detectability of the studied species by the ACO method in some years may not necessarily indicate their low population density, but rather results from shifts in their diurnal activity and/or microhabitat use dependent on ambient temperatures. Increasing between-year variation in weather conditions may reduce repeatability of seasonal patterns of ACO usage, making we suggest additional detection techniques that could bee incorporated.

During the years 2004-2008 the distribution of the Common Adder and the Slow Worm were studied in Silesia through questionnaire directed to forest inspectorates (n=871); 83.8% of them responded. These data were tested through field work in several randomly selected inspectorates. Both species were found to be widespread in the region, with a few strongholds identified in Sudety Mts. and larger forest complexes. The Common Adder was recorded in 68.5% of forest districts which responded, while the Slow Worm – in 73.6% of those districts. Changes in distribution and population trends could not be derived, since no reliable data were available from previous years.

Reptiles are often overlooked in conservation efforts. Hence, long‐term population data is often unavailable, and evidence for effective conservation actions that improve reptile habitat remains scarce for most species. Here we used a before–after control–intervention (BACI) experiment to investigate the impact of basking bank creation on four co‐occurring reptile species: European adder, barred grass snake, slow worm, and viviparous lizard. Long‐term refuge monitoring at a UK wildlife reserve allowed population assessment before and after habitat modification. Only viviparous lizards were observed at basking banks within 12 months of construction. In subsequent years, barred grass snake observations increased near basking banks and slow worms were observed for the first time, while European adder observations increased away from banks and barred grass snake observations decreased away from banks. Our small‐scale BACI study suggests basking banks attracted barred grass snakes from the surrounding area, which saw a corresponding increase in European adder sightings.

Exploratory behaviour in animals is considered a driver of dispersal propensity, which might result in colonisation of new environments and population range expansion in the long term. To find out whether the patterns of exploratory behaviour and risk-taking in the slow worm, Anguis fragilis (L., 1758) differ from that of the eastern slow worm, A. colchica (Nordmann, 1840), the behaviour of nine A. fragilis and seven A. colchica individuals was tested. Escape latency at capture and response to a novel environment and a new object in captivity were assessed. Slow worms of A. fragilis were more exploratory than A. colchica but no difference in risk-taking between the two species was found. Probably the higher exploratory activity of A. fragilis, compared to A. colchica, could be connected to its wider vertical distribution and greater diversity of habitat occupancy.

The calcium and phosphate metabolism of reproducing reptiles with particular reference to the adder ( vipera berus)

With five currently recognized species that form several secondary contact zones, slow worms (Anguidae: Anguis) offer a valuable model to study the fate of evolutionary lineages in the face of hybridization and genetic introgression. The relationships between the Western Slow Worm Anguis fragilis and the Italian Slow Worm Anguis veronensis are particularly puzzling. Their respective distributions remain poorly known on the edges of their parapatric ranges, as both species lack external differentiation. Contra earlier mitochondrial phylogenies, new phylogenomic inferences have shown that A. fragilis and A. veronensis are sister taxa, thus casting doubts on their specific status. In this study, we analyze the A. fragilis/veronensis transition in southeastern France, based on one mitochondrial (ND2) and two nuclear (PRLR and HA1) genetic markers in 81 specimens from 61 localities. The ranges of A. fragilis and A. veronensis roughly extends northwest and southeast of the Rhône-Durance valleys, respectively, with clear signs of introgressive hybridization in the areas of contact (notably the eastern parts of the lower Rhône valley). Based on the three molecular markers analyzed, gene flow does not seem to reach outside the narrow hybrid zone, which likely indicates (incomplete) intrinsic reproductive isolation. Hence, we provisionally suggest maintaining A. veronensis as a separate species from A. fragilis. More generally, patterns of genetic divergence, external differentiation, and hybridization (both historical and contemporary) in Anguis ssp. supports a speciation continuum spanning from cryptic, genetically compatible alloparapatric lineages to phenotypically distinct, deeply diverged and fully reproductively isolated taxa able to coexist in sympatry.