Stanisław Bury’s research while affiliated with Jagiellonian University and other places

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Publications (59)


Table 3 (continued)
Diversity of A. fragilis and A. colchica ND2 haplotypes from Poland and summary of genetic polymorphism for both species.
Contact zone of slow worms Anguis fragilis Linnaeus, 1758 and Anguis colchica (Nordmann, 1840) in Poland
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January 2025

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Stanisław Bury

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Background Legless lizards, the slow worms of the genus Anguis, are forming secondary contact zones within their Europe-wide distribution. Methods We examined 35 populations of A. fragilis and A. colchica to identify the level of morphological and genetic divergence in Poland. We applied a conventional study approach using metric, meristic, and categorial (coloration) features for a phenotype analysis, and two standard molecular markers, a mitochondrial (NADH-ubiquinone oxidoreductase chain 2; ND2 ) and a nuclear (V(D)J recombination-activating protein 1; RAG1 ) one. Results We found clear differences between A. fragilis and A. colchica in molecular markers and phenotype—in meristic features, e.g., ear opening, number of scales rows around the body, and higher than so far known diversity in ND2 and RAG1 haplotypes. The presence of five hybrids was detected in three populations in the Polish part of the European contact zone. In all hybrids, homozygous alleles of RAG1 were detected, which suggests a back-crossing within the genus. Conclusions The ability to produce fertile offspring by A. fragilis x A. colchica hybrids shows inefficient mechanisms of reproductive isolation of the two legless lizards. The hybrids were indistinguishable from parental species in head proportions (principal components and discriminant analyses) but more resembling A. colchica in meristic traits.

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Ocena stanu populacji gniewosza plamistego Coronella austriaca (Laurenti, 1768) w Krakowie w latach 2010-2024

November 2024

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29 Reads

Gniewosz plamisty (Coronella austriaca) jest jednym z najrzadszych gatunków gadów występujących w Polsce. Stan rozpoznania jego populacji w kraju uległ znacznej poprawie w ostatnich latach, jednak wciąż wymaga dalszych badań. Jednym z lepiej zbadanych i regularnie monitorowanych stanowisk gniewosza jest krakowski Zakrzówek. W okresie 2010-2024 sześciokrotnie prowadzono badania monitoringowe populacji gniewosza plamistego na Zakrzówku, które miały na celu ocenę liczebności oraz struktury płci populacji, w kontekście perspektyw jej zachowania i ochrony. Liczba osobników stwierdzanych w każdym z sześciu lat badań waha się pomiędzy 10 a 18 (średnio 14), bez wyraźnych trendów spadkowych lub wzrostowych. Struktura płci w żadnym z sześciu lat badań nie odbiegała istotnie od stosunku 1:1. Obserwacje osobników juwenilnych były sporadyczne i nie przekraczały dwóch osobników rocznie, co może wynikać z niskiej wykrywalności lub wysokiej śmiertelności młodych. Należy mieć na uwadze, że pomimo względnie stabilnego statusu populacji liczebność gniewosza na Zakrzówku może zacząć spadać w kolejnych latach w wyniku niedawnych niekorzystnych zmian w siedlisku związanych z przekształceniem kolejnych fragmentów Zakrzówka. Monitoring gniewosza na Zakrzówku powinien być kontynuowany, a także rozszerzony o wybrane stanowiska w Tyńcu, dla których regularne badania nie są prowadzone.


Retrospective Detection of Ophidiomyces ophidiicola from Snake Moults Collected in Bieszczady Mountains, Poland

July 2024

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163 Reads

Microorganisms

Ophidiomyces ophidiicola, the causative agent of ophidiomycosis, poses a potential threat to wild snakes worldwide. This study aimed to retrospectively investigate the prevalence of O. ophidiicola in archived snake moults collected from the San River Valley in the Bieszczady Mountains, Poland, from 2010 to 2012. Using qPCR for O. ophidiicola detection and conventional PCR for clade characterisation, we analysed 58 moults and one road-killed specimen of Zamenis longissimus and Natrix natrix. A novel combination of primers (ITS2L) was used to simultaneously confirm SYBR Green-based qPCR results and perform genotyping. O. ophidiicola has been detected from two Z. longissimus and one N. natrix specimens. The identified clade (I-B) is consistent with those found in wild snakes of eastern Europe and San River Valley, indicating that O. ophidiicola has been present in this region for at least a decade. This study underscores the value of historical samples in understanding the long-term presence of pathogens and highlights the potential role of environmental reservoirs in the persistence of O. ophidiicola. Our findings are crucial for informing conservation strategies for the endangered Aesculapian snake populations in Poland, emphasising the need for ongoing monitoring and habitat management to mitigate the potential impact of ophidiomycosis.


The classification of Salmonella isolates into different subspecies based on the detection of specific genes for each subspecies (according to Lee et al., 2009). In blue boxes we highlighted Salmonella spp. isolates identified as Salmonella enterica subsp. houtenae (4.1S, II4.1S, IINN.6.1 and NN12.2); M—DNA molecular weight marker.
The determination of genetic correlation of Salmonella spp. strains isolated from reptiles based on ERIC‐PCR. (A) Agarose gel as in Figure 1 indicating strictly conserved fragments of the genome of studied Salmonella spp. isolates enabling the determination of the genetic similarities between them. (B) Cluster analysis of ERIC‐PCR profiles of Salmonella spp. with their corresponding origin. The phylogenetic tree was generated by the average linkage agglomeration method (unweighted pair group method with arithmetic mean) using BioNumerics 7.6.2 (Applied Maths).
Virulence factors of Salmonella spp. isolated from free‐living grass snakes Natrix natrix

July 2024

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54 Reads

Salmonellosis associated with reptiles is a well‐researched topic, particularly in China and the United States, but it occurs less frequently in Europe. The growth of the human population and changes in the environment could potentially increase the interaction between humans and free‐living reptiles, which are an unidentified source of Salmonella species. In this study, we sought to explore this issue by comparing the microbiota of free‐living European grass snakes, scientifically known as Natrix natrix, with that of captive banded water snakes, or Nerodia fasciata. We were able to isolate 27 strains of Salmonella species from cloacal swabs of 59 N. natrix and 3 strains from 10 N. fasciata. Our findings revealed that free‐living snakes can carry strains of Salmonella species that are resistant to normal human serum (NHS). In contrast, all the Salmonella species strains isolated from N. fasciata were sensitive to the action of the NHS, further supporting our findings. We identified two serovars from N. natrix: Salmonella enterica subspecies diarizonae and S. enterica subspecies houtenae. Additionally, we identified three different virulotypes (VT) with invA, sipB, prgH, orgA, tolC, iroN, sitC, sifA, sopB, spiA, cdtB and msgA genes, and β‐galactosidase synthesised by 23 serovars. The identification of Salmonella species in terms of their VT is a relatively unknown aspect of their pathology. This can be specific to the serovar and pathovar and could be a result of adaptation to a new host or environment.



Spatial distribution of snake captures and detections of O. ophidiicola across Europe
a Each circle represents an individual snake capture and overlapping points were jittered for visualization. Different colors are used to distinguish countries, filled points indicate snakes that were qPCR positive (n = 109), and outlined points are qPCR negative snakes (n = 1145). Underlying density heatmap shows spatial distribution of O. ophidiicola infection risk based on qPCR positive detections using a kernel density estimation algorithm. We used a 100-km radius around each positive point and the scale bar indicates point density (i.e. relative disease risk) across each region. b Estimated O. ophidiicola prevalence across sites (n = 33) sampled in 10 countries. Each transparent black circle represents a single snake as being either negative (0) or positive (1). Larger circles and whiskers show the model predicted posterior mean ± standard deviation (thick lines), and 95% credible intervals (thin lines). Color of the circles represent the different countries; red line shows threshold for elevated prevalence defined as the estimated mean prevalence across all sites.
Predicted prevalence of O. ophidiicola in different species of snakes across Europe
Each transparent black circle represents a single snake as being either negative (0) or positive (1). Larger circles and whiskers show the model predicted posterior mean ± standard deviation (thick lines), and 95% credible intervals (thin lines) for each species across all countries. Colors indicate different species (n = 16).
Lesion prevalence and disease severity in O. ophidiicola-positive snakes across different species
Color circles and whiskers show the model predicted posterior mean, ±standard deviation (thick lines), and 95% credible intervals (thin lines) for different species across all countries. a Each transparent black circle represents a single snake as being either negative (0) or positive (1) for presence of lesions, which was used to calculate the proportion of the population that tested positive (prevalence). b Each transparent black circle represents the percentage of the body of a single snake covered in lesions and the size of the circle is proportional to the total surface area of the snake (scale ranges 250–1000 cm²).
Distribution of O. ophidiicola clades and genotypes across Europe
aO. ophidiicola clades and genotypes from positive detections (n = 93) across the landscape in Europe. Points are slightly jittered for visual representation of the sampling range. Color of the point indicates the clades and genotypes, samples that were qPCR negative are represented as gray points (n = 1145), and samples that failed to amplify with the genotyping PCR are represented as black points (n = 16). Pink and medium blue points represent simultaneous detections of genotypes I-A and II-D/E and genotypes I-A and I-B, respectively, from the same swab sample (i.e., snakes infected with multiple genotypes). The enlarged map (inset) shows better resolution of detections in Switzerland. b The proportion of each O. ophidiicola clade (clade I or clade I & II) detected by species. Small color points are predicted mean prevalence at a site for a given species and clade, point size indicates sample size at each site. Large color points and whiskers show the model predicted posterior mean, ±standard deviation (thick lines), and 95% credible intervals (thin lines) across different species. c Photo of a N. tessellata from Hungary infected with O. ophidiicola from clade I-B. d Photo of a N. tessellata from Switzerland infected with O. ophidiicola from clade II-F showing facial infection.
Contribution of host species and pathogen clade to snake fungal disease hotspots in Europe

April 2024

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336 Reads

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6 Citations

Communications Biology

Infectious diseases are influenced by interactions between host and pathogen, and the number of infected hosts is rarely homogenous across the landscape. Areas with elevated pathogen prevalence can maintain a high force of infection and may indicate areas with disease impacts on host populations. However, isolating the ecological processes that result in increases in infection prevalence and intensity remains a challenge. Here we elucidate the contribution of pathogen clade and host species in disease hotspots caused by Ophidiomyces ophidiicola, the pathogen responsible for snake fungal disease, in 21 species of snakes infected with multiple pathogen strains across 10 countries in Europe. We found isolated areas of disease hotspots in a landscape where infections were otherwise low. O. ophidiicola clade had important effects on transmission, and areas with multiple pathogen clades had higher host infection prevalence. Snake species further influenced infection, with most positive detections coming from species within the Natrix genus. Our results suggest that both host and pathogen identity are essential components contributing to increased pathogen prevalence.


Sexual dimorphism and allometry in the head and body size of two viperid snakes (genus Vipera)

February 2024

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115 Reads

Belgian Journal of Zoology

Sexual dimorphism in the size and shape of the body and head is the result of manifold selective pressures acting on organisms. In snakes, sexual size dimorphism is common and has been well-studied. However, intersexual differences in relative head size and shape have attracted far less attention. Similarly, the allometric properties of head shape and size in snakes are poorly known. Here, we analyse sexual dimorphism in two viperid species: European adder Vipera berus (Linnaeus, 1758) and Steppe viper Vipera renardi (Christoph, 1861). We measured body length, tail length and several head characteristics: head length, head width, head height, pileus length, interorbital distance and internarial distance. Our findings were that males and females of both species did not differ in body length (SVL), but that males tended to have significantly longer tails; there were also significant differences in head characteristics-males tended to have higher heads, and larger internarial and interorbital distances. The head dimensions displayed negative allometry when compared against SVL but when scaled against head length, dimensions like head height and head width exhibited positive allometry. We argue that these differences may be related to sexual selection and that the wider heads may also serve as antipredatory signal.


Relationships between morphological variables of erythrocytes. (a) N : C ratio (nucleus size/cell size) and (c) elongation ratio (cell length/width) are negatively correlated to cell size expressed as area. However, the relationship that built up these ratio traits is well approximated by a linear function indicating proportional changes of nucleus size with changes in cell size (b), and proportional changes in cell length with changes in cell width (d). Regression lines indicate a significant relationship corrected for the phylogeny.
Schematic depiction of potential relationships between variables (nucleus and cell area, or cell length and width) used for the construction of N : C (nucleus size/cell size) and elongation (cell length/width) ratios. Linear relationships between numerator and denominator with a zero intercept (graph (a), black line—proportionality) result in a constant ratio (graph (b)), while linear function with exactly the same slope but a positive intercept results in a negative nonlinear scaling of ratios (graphs (a) and (b), dark grey lines) statistically indistinguishable from the ratio scaling derived from a nonlinear relationship between numerator and denominator (graphs (a) and (b), light grey lines; power function is shown here as an example of a nonlinear function).
Scaling of erythrocyte shape and nucleus size among squamate reptiles: reanalysis points to constrained, proportional rather than adaptive changes

April 2023

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60 Reads

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1 Citation

Small erythrocytes might be beneficial for blood rheology, as they contribute less to blood viscosity than large erythrocytes. We predicted that rheological disadvantages of larger erythrocytes could be alleviated by relatively smaller nucleus size in larger cells allowing higher flexibility and by more elongated shape. Across squamate reptiles, we found that species with larger erythrocytes tend to have smaller ratio of nucleus size to cell size (N : C ratio), but that larger erythrocytes tend to be rounder, not more elongated. Nevertheless, we document that in fact nucleus area changes with erythrocyte area more or less linearly, which is also true for the relationship between cell length and cell width. These linear relationships suggest that nucleus size and cell size, and cell width and cell length, might be constrained to largely proportional mutual changes. The shifts in widely used N : C ratio and elongation ratio (cell length/cell width) with cell size might be misleading, as they do not reflect adaptive or maladaptive changes of erythrocytes, but rather mathematically trivial scaling of the ratios of two variables with a linear relationship with non-zero intercepts. We warn that ratio scaling without analyses of underlying patterns of evolutionary changes can lead to misinterpretation of evolutionary processes.


Fig. 2. Map of the localities of the populations sampled in this study. Anguis colchica populations: 1 -Beskid Żywiecki, 2 -Kłaj, 3 -Bóbrka, 4 -Myczkowce, 5 -Ustrzyki Górne, 6 -Czudec, 10 -Štramberk, 17 -Lutcza, 20 -Kuźnia Raciborska, 24 -Baligród, 25 -Leżajsk, 29 -Lutoryż, 30 -San River Valley; Anguis fragilis populations: 7 -Wrocław, 8 -Šumava, 9 -Sulistrowiczki, 11 -Pszczew, 12 -Prague, 13 -Podkowa Leśna, 14 -Piotrków Trybunalski, 15 -Niemojów, 16 -Milicz, 18 -Lubliniec, 19 -Ligota, 21 -Iława, 22 -Byków, 23 -Bartniki, 26 -Leśniczówka, 27 -Dzioły, 28 -Susły, 31 -Górażdże.
Is the blue-spotted phenotype more widespread in the eastern slow worm Anguis colchica (Nordmann, 1840) than the western slow worm Anguis fragilis Linnaeus, 1758 and does it correlate with the male body size? A case study from Central Europe

April 2023

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269 Reads

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1 Citation

Folia Biologica

The blue-spotted phenotype in a slow worm can be considered as an alternative colour morph or a secondary sexual characteristic. This phenotype is known to entail an elevated predation risk; thus, its continuous presence in a population must be balanced by additional and positive fitness consequences. In this study, we show that blue-spotted males are characterised by a greater snout-vent length (SVL) than typical specimens. Importantly, the SVL of blue-spotted males reaches the magnitude of the average female size. This indicates that the presence of blue spots may involve a correlated positive effect on growth and body size. The greater body size of the blue-spotted males could enhance their survival and mating success, and thus facilitate the continued presence of a high fraction of this morph within the population. In addition, we found that the blue-spotted phenotype is more common in the eastern than the western slow worm, and the proposed fitness consequences of the blue-spotted phenotype might enhance its tendency to spread in the eastern Anguis lineage.


Fig. 1. Map of sampling plots (A) in the northeastern corner of Niepołomice Forest in south-central Poland (inset). The plots are split into three groups indicated by color coding: group N in managed forest north of a main road (solid line), group E in managed forest southeast of the main road, and group L in Lipówka reserve (green rectangle) in old growth, unmanaged forest. Blue stippling shows area in which five historical plots were located (Głowaci´nskiGłowaci´nski and Witkowski 1970). Photographs of fragments of sampling plots in managed forest (B, plot N1) and old growth forest (C, plot L8). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
Amphibian decline in a Central European forest and the importance of woody debris for population persistence

February 2023

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413 Reads

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6 Citations

Ecological Indicators

Despite amphibian decline is one of the best studied symptom of biodiversity reduction, quantitative data on the phenomenon are scarce, which applies mostly to terrestrial habitats. Herein we present data on an abundance and a biomass of amphibians i Niepołomice Forest (Southern Poland) over 50 years. The study showed clear decline in both abundance and a biomass and changes in species composition as well. Moreover, we found that the amount of deadwood debris has a positive effect on frogs, and should be concerned as important element of amphibian conservation i woodlands. Other factors including ground water drainage, pollution and habitat fragmentation presumably affecting local populations, are discussed.


Citations (27)


... In contrast, high canopy cover is associated with poor thermal quality and reduced snake abundance (Blouin-Demers & Weatherhead, 2001). Areas of low elevation in Tennessee are often associated with aquatic habitats, and previous work suggests that either O. ophidiicola is reliant on aquatic habitats (Lorch et al., 2016) or that semiaquatic snakes are more susceptible to O. ophidiicola (Blanvillain et al., 2024;McKenzie et al., 2019). We were unable to detect a relationship between habitat suitability for O. ophidiicola and the dysbiosis index. ...

Reference:

Effects of snake fungal disease (ophidiomycosis) on the skin microbiome across two major experimental scales
Contribution of host species and pathogen clade to snake fungal disease hotspots in Europe

Communications Biology

... fig-1 authors to outline a reliable evolutionary scenario of differentiation in some morphological characters, concluding that A. fragilis bears more plesiomorphic traits, and hybrids resemble A. fragilis more. It seems especially important as some morphological traits, taken as species-diagnostic like blue spots in the dorsal part of the body, differ between the two species by frequency of occurrence (Bury et al., 2023). ...

Is the blue-spotted phenotype more widespread in the eastern slow worm Anguis colchica (Nordmann, 1840) than the western slow worm Anguis fragilis Linnaeus, 1758 and does it correlate with the male body size? A case study from Central Europe

Folia Biologica

... Worldwide amphibian populations are experiencing significant declines and many species are on the brink of extinction. While disease and habitat loss are the primary drivers of amphibian loss (Rachowicz et al., 2005;Pabijan et al., 2023), this phenomenon may also be influenced by complex and often not entirely understood factors (Green et al., 2020). Among these there is climate change (Stuart et al., 2004;Corn, 2005;Luedtke et al., 2023), alteration ultraviolet radiation (Kiesecker et al., 2001), pollution (Mirabile et al., 2009) and interference from introduced species due to predation, competition and spillover of parasites (Beebee and Griffiths, 2005). ...

Amphibian decline in a Central European forest and the importance of woody debris for population persistence

Ecological Indicators

... While a growing number of studies have investigated the occurrence and impact of ophidiomycosis in freeliving populations of snakes in North America 22,23 , research in Europe is relatively limited. To date, small numbers of snakes in the Czech Republic, Germany, Italy, Poland, and the Slovak Republic have tested qPCR positive for Oo DNA 16,24,25 . However, there is a paucity of information on disease progression and recovery in free-living snakes through serial recaptures 26 . ...

Hotspots for snake fungal disease across Europe are maintained by host and pathogen identity

... The adult digenean Leptophallus nigrovenosus (Bellingham, 1844) is an esophageal parasite of ophidians in Europe and northern Africa and is mainly found in water snakes of the genus Natrix (Laurenti, 1768) [1,2]. The infective stage for snakes (metacercaria) is found in amphibians (adults and tadpoles) that comprise some of the main prey species in the diet of Natrix snakes [3]. ...

Frequent infection of urban grass snakes (Natrix natrix) oral cavity with Leptophallus nigrovenosus trematode
  • Citing Article
  • April 2022

Parasitology Research

... Increased rainfall can enhance their activity and positively impact their breeding [6]. Additionally, research has shown that snakes in various regions often become more active following rainfall due to the availability of food and suitable microhabitats [7]. This increased activity leads to more frequent encounters between humans and snakes, resulting in a higher incidence of snakebites [7]. ...

Climatic conditions and prevalence of melanistic snakes—contrasting effects of warm springs and mild winters
  • Citing Article
  • April 2022

International Journal of Biometeorology

... During extended periods of digestive quiescence, gut downregulation reduces maintenance costs, allowing greater energy investment in activity, growth, and reproduction, and offsetting any costs incurred by occasional gut upregulation (Secor and Diamond 1998;Secor 2001Secor , 2005. Many snake species (Serpentes) that naturally experience long bouts of fasting and widely regulate gut performance are considered model organisms for examination of the energetic economics of vertebrate regulatory responses to feeding (Secor and Diamond 1998;Wang and Rindom, 2021;Bury 2022). ...

Intestinal upregulation and specific dynamic action in snakes – Implications for the ‘pay before pumping’ hypothesis
  • Citing Article
  • September 2021

Comparative Biochemistry and Physiology Part A Physiology

... Still, the proper use of morphological characters depends on the knowledge of the nature of their variation. Considering skull morphology, previous studies have shown some sources of intraspecific variation, such as ontogenetic variation (Murta-Fonseca and Fernandes 2016; Patterson et al. 2022), static allometry (Hampton 2014;Hampton and Kalmus 2014), and sexual dimorphism (Borczyk 2019;Murta-Fonseca et al. 2019;Borczyk et al. 2021), although such data are still unknown for most taxa. ...

Sexual dimorphism and skull size and shape in the highly specialized snake species, Aipysurus eydouxii (Elapidae: Hydrophiinae)

... It may also be the way to reduce the risk of predation by larger lizards, as sand lizards are known to prey on the same species of hatchlings (e.g., Bury and Kolanek 2020). The air temperature also influences the number of observed lizards (Kolanek and Bury 2021). When it is too hot or cold, reptiles limit their activity or exposure to the sun. ...

Detectability of Elusive Reptiles under Artificial Cover Objects is Species- and Year-Specific

Polish Journal of Ecology

... Interestingly all three victims were sloughing, as was the constricted neonate grass snake reported here. Also, Kolanek & Bury (2020) observed that a juvenile smooth snake attempted cannibalism of a sibling just after their first shed and suggested that the shed may have triggered this behaviour. A Norwegian Lundehund (small dog) trained for finding smooth snakes in eastern Norway finds clutches of newborn smooth snakes during their first slough that are not visible to us and detect sloughs that are hidden under vegetation (Rune Botnermyr, pers comm). ...

CORONELLA AUSTRIACA (Smooth Snake). DIET/CANNIBALISM.
  • Citing Article
  • September 2020

Herpetological Review