Triturus Research Articles

On the aquatic phenology of sympatric crested and marbled newts (genus Triturus)

Abstract The large-bodied newts Triturus cristatus and T. marmoratus possess ranges that overlap in western France where they frequently share breeding ponds. I test the hypothesis that the aquatic phenology differs between them, as associated with a more aquatic and terrestrial life style respectively. Total adult population sizes were determined in spring in 13 experiments by the capture-mark-recapture methodology, followed by equivalent experiments in summer. Population sizes dropped by an order of magnitude on average whereas species frequencies changed in favour of T. cristatus, suggesting that T. marmoratus leaves the breeding site earlier than T. cristatus. Interspecies hybrids behaved like T. marmoratus. Descriptions are provided of other features (in ecology, morphology, demography, and colouration pattern) that support the different, aquatic versus terrestrial life styles of T. cristatus and T. marmoratus.

A staging table of Balkan crested newt embryonic development to serve as a baseline in evolutionary developmental studies.

There is an increased interest in the evolution and development of newts from the genus Triturus because: (1) morphological differentiation among the nine constituent species largely corresponds to different ecological preferences, (2) hybridization between different species pairs has various evolutionary outcomes in terms of life history traits and morphology, and (3) the genus expresses a balanced lethal system that causes arrested growth and death of half of the embryos. These features provide natural experimental settings for molecular, morphological, and life-history studies. Therefore, we produce a staging table for the Balkan crested newt (T. ivanbureschi). We provide detailed descriptions of 34 embryonic stages based on easily observable and interpretable external morphological characters, to ensure reproducibility. Compared with previous staging tables for Triturus, we include a vastly increased sample size and provide high-resolution photographs in lateral, ventral, and dorsal view, complemented by videos of specific developmental periods, and accompanied by detailed explanations on how to delineate the specific stages. Our staging table will serve as a baseline in comparative studies on Triturus newts: an emerging model system in evolutionary and developmental studies.

A subspecies of marbled newt (Triturus marmoratus) in the Iberian Peninsula newly resolved from congruent nuclear and mitochondrial dna data

Abstract The herpetofauna of the Iberian Peninsula is relatively well-researched, yet detailed studies, at least in part relying on molecular genetic data, continue to reveal taxa new to science, mostly species and subspecies. Newts of the genus Triturus are one such group with undiscovered yet taxonomically relevant variation, as shown by the recent description of new (sub)species of pygmy newts (T. pygmaeus, T. rudolfi). The marbled newt, Triturus marmoratus, shows an equally deep and geographically coherent spatial-genetic diversification. It is here shown that a northern and a southern group are characterized by different mitochondrial dna profiles and are also differentiated in morphometry and colouration pattern. With no firm evidence for selection against intermediate genotypes, the southern group is described at the subspecies level, as T. marmoratus harmannis ssp. nov. The subspecies’ contact zone is situated at ca. 41.5 northern latitude and stretches from the Atlantic coast near Porto, Portugal to the northeast of Madrid, Spain.

Molecular data confirm the presence of the Southern Crested Newt Triturus karelinii (Strauch, 1870) in Anatolia

Two species of newts of the genus Triturus are known to occur in Türkiye: Triturus ivanbureschi Wielstra & Arntzen, 2013 and T. anatolicus Wielstra & Arntzen, 2016. Here, we used the mitochondrial ND4 gene as a genetic marker to determine the taxonomic position of a new population found in Posof, Ardahan, northeastern Anatolia. It was shown the population belongs to T. karelinii (Strauch, 1870), which is thus the third species of Triturus present in Türkiye.

Environmental and training factors affect canine detection probabilities for terrestrial newt surveys

Amphibians are of great interest to scientific research, but many populations are highly threatened and declining worldwide. Although varieties of aquatic survey methods exist, traditional methods for terrestrial surveys are very time-consuming but often not very effective. A novel method to detect terrestrial amphibians is the use of wildlife detection dogs. While their use for and factors affecting detection rates of mammals and reptiles are well documented, scientific literature on amphibian detection dogs is just emerging. The purpose of this study was to investigate the effects of environmental (habitat, weather) and training factors on detection probabilities for a newt detection dog. An experienced wildlife detection dog was trained and tested on smooth (Lissotriton vulgaris) and great crested newts (Triturus cristatus). Environmental and training parameters were recorded for 101 test trials and used as explanatory parameters in a binomial GLM. I found that detection probability strongly depended on temperature, whereby optimal temperatures varied by habitat. Detection probabilities were lowest in short grass, but there was no strong difference among forest habitats. They were higher for males than females and for great crested than smooth newts. For this dog, detection probabilities were also higher if the dog was working off the leash than on it, and when the dog was cooperative than fatigued. Dog performance increased over time with a strong increase at the beginning and a plateau at 92% detection probability. However, detection rates of this specific dog slightly decreased when the dog was working for more than two hours. The findings of this study provide a valuable basis for future deployments of this and other amphibian detection dogs. Dogs can certainly work in a variety of different habitats, although directed off-leash searching with enough time in complex habitats and specific training for small species with low detection distances may enhance their performance. The study design might also consider the temperature and humidity at which the dog will be deployed. A regular assessment of the detection dog using blind tests will give an indication of its reliability. Assessments similar to this study may further be used to estimate detection probability for a particular dog under given field conditions. Regular blind tests will show when the detection rates reached a plateau, which may then give an indication of on its reliability. Altogether, results suggest that newt detection dogs may provide a highly promising survey method, which can certainly be transferred for detecting other amphibians in terrestrial habitats.

Explaining declines of newt abundance in northern Italy

Abstract Amphibians are an exemplary case of the current biodiversity crisis, being among the vertebrates suffering the fastest decline. Population dynamics of amphibians can result from processes acting at different scales. Both the local characteristics of breeding wetlands and the features of the surrounding landscape can strongly affect the temporal dynamics of amphibian populations. European newts are particularly threatened by land‐use change and invasive alien species. While it is known that newts are declining across Europe, few studies have performed broad‐scale assessments of their decline, either because abundance dynamics are more complex to analyse than presence/absence data or because they require a high sampling effort and long‐term monitoring. In this study, we show that long‐term distribution data can be combined with demographic models to quantify the decline in abundance of newt species at the regional scale, and to assess the importance of multiple factors in determining abundance dynamics. We performed multiple surveys between 1996 and 2020 and used N‐mixture models in a Bayesian framework. We then calculated abundance changes between the first and the last sampling season, which were performed with an average timespan of 13 years across all wetlands. Both Italian crested newts and smooth newts showed large declines, with an average estimated abundance loss between the first and last sampling season of 57% and 63%, respectively. Local characteristics of the wetlands were the main determinants of abundance dynamics: the abundance of both species showed a positive relationship with the area and the permanence of the wetland and a negative relationship with the presence of fish. Additionally, the abundance of Italian crested newts was negatively related to the presence of invasive crayfish. No relationship was detected between abundance and terrestrial habitat availability or connectivity measures. Despite uncertainties in the absolute values of estimated abundance, the striking regional‐scale decline of newts is evident. Among the major determinants of population dynamics, fish and crayfish presence increased their prevalence in the study area, while other factors remained more stable. Management actions aimed at eradicating or controlling invasive fish and crayfish might halt abundance loss and even revert this declining trend. The application of N‐mixture models to long‐term data from representative sites permits the analysis of temporal trends of species at the regional scale even when data come from complex monitoring schemes. We found large declines in abundance of two newt species, suggesting that European newts may be more threatened than previously thought.

Anadolu Yarımadası’ndan İki Semender Türünün (Ommatotriton ophryticus & Triturus ivanbureschi) Olağandışı Kış Aktivitesi Gözlemleri

Interactions between the internal regulation and the environment drive the biophysiological patterns of amphibians. It is well known phenomenon that newts in the northern hemisphere are tend to have hibernation strategies in winter seasons. However, the winter activity record for newts is quite rare. Therefore, we would like to report two winter activity cases from Anatolia, Turkey via two newt species: The northern banded newt (Ommatotriton ophryticus) from Ordu and Balkan crested newt (Triturus ivanbureschi) from Çanakkale. The striking outcomes of this study are that the Northern Banded Newt demonstrates winter activity from another locality apart from Trabzon, and the Balkan Crested Newt has been observed in winter for the first time in its natural habitat. However, it is more important that to document these winter activities are remarkable to provide valuable preliminary data for interpreting the global climate change dynamics in local cases.

Phylotranscriptomic evidence for pervasive ancient hybridization among Old World salamanders

Hybridization can leave genealogical signatures in an organism's genome, originating from the parental lineages and persisting over time. This potentially confounds phylogenetic inference methods that aim to represent evolution as a strictly bifurcating tree. We apply a phylotranscriptomic approach to study the evolutionary history of, and test for inter-lineage introgression in the Salamandridae, a Holarctic salamanders group of interest in studies of toxicity and aposematism, courtship behavior, and molecular evolution. Although the relationships between the 21 currently recognized salamandrid genera have been the subject of numerous molecular phylogenetic studies, some branches have remained controversial and sometimes affected by discordances between mitochondrial vs. nuclear trees. To resolve the phylogeny of this family, and understand the source of mito-nuclear discordance, we generated new transcriptomic (RNAseq) data for 20 salamandrids and used these along with published data, including 28 mitochondrial genomes, to obtain a comprehensive nuclear and mitochondrial perspective on salamandrid evolution. Our final phylotranscriptomic data set included 5455 gene alignments for 40 species representing 17 of the 21 salamandrid genera. Using concatenation and species-tree phylogenetic methods, we find (1) Salamandrina sister to the clade of the “True Salamanders” (consisting of Chioglossa, Mertensiella, Lyciasalamandra, and Salamandra), (2) Ichthyosaura sister to the Near Eastern genera Neurergus and Ommatotriton, (3) Triturus sister to Lissotriton, and (4) Cynops paraphyletic with respect to Paramesotriton and Pachytriton. Combining introgression tests and phylogenetic networks, we find evidence for introgression among taxa within the clades of “Modern Asian Newts” and “Modern European Newts”. However, we could not unambiguously identify the number, position, and direction of introgressive events. Combining evidence from nuclear gene analysis with the observed mito-nuclear phylogenetic discordances, we hypothesize a scenario with hybridization and mitochondrial capture among ancestral lineages of (1) Lissotriton into Ichthyosaura and (2) Triturus into Calotriton, plus introgression of nuclear genes from Triturus into Lissotriton. Furthermore, both mitochondrial capture and nuclear introgression may have occurred among lineages assigned to Cynops. More comprehensive genomic data will, in the future, allow testing this against alternative scenarios involving hybridization with other, extinct lineages of newts.

Landscape genetics of northern crested newt Triturus cristatus populations in a contrasting natural and human-impacted boreal forest

Among vertebrates, amphibians currently have the highest proportion of threatened species worldwide, mainly through loss of habitat, leading to increased population isolation. Smaller amphibian populations may lose more genetic diversity, and become more dependent on immigration for survival. Investigations of landscape factors and patterns mediating migration and population genetic differentiation are fundamental for knowledge-based conservation. The pond-breeding northern crested newt (Triturus cristatus) populations are decreasing throughout Europe, and are a conservation concern. Using microsatellites, we studied the genetic structure of the northern crested newt in a boreal forest ecosystem containing two contrasting landscapes, one subject to recent change and habitat loss by clear-cutting and roadbuilding, and one with little anthropogenic disturbance. Newts from 12 breeding ponds were analyzed for 13 microsatellites and 7 landscape and spatial variables. With a Maximum-likelihood population-effects model we investigated important landscape factors potentially explaining genetic patterns. Results indicate that intervening landscape factors between breeding ponds, explain the genetic differentiation in addition to an isolation-by-distance effect. Geographic distance, gravel roads, and south/south-west facing slopes reduced landscape permeability and increased genetic differentiation for these newts. The effect was opposite for streams, presumably being more favorable for newt dispersal. Populations within or bordering on old growth forest had a higher allelic richness than populations in managed forest outside these areas. Old growth forest areas may be important source habitats in the conservation of northern crested newt populations.

Integral chain management of wildlife diseases

AbstractThe chytrid fungus Batrachochytrium dendrobatidis has caused the most prominent loss of vertebrate diversity ever recorded, which peaked in the 1980s. Recent incursion by its sister species B. salamandrivorans in Europe raised the alarm for a new wave of declines and extinctions in western Palearctic urodeles. The European Commission has responded by restricting amphibian trade. However, private amphibian collections, the main end consumers, were exempted from the European legislation. Here, we report how invasion by a released, exotic newt coincided with B. salamandrivorans invasion at over 1000 km from the nearest natural outbreak site, causing mass mortality in indigenous marbled newts (Triturus marmoratus), and posing an acute threat to the survival of nearby populations of the most critically endangered European newt species (Montseny brook newt, Calotriton arnoldi). Disease management was initiated shortly after detection in a close collaboration between policy and science and included drastic on site measures and intensive disease surveillance. Despite these efforts, the disease is considered temporarily contained but not eradicated and continued efforts will be necessary to minimize the probability of further pathogen dispersal. This precedent demonstrates the importance of tackling wildlife diseases at an early stage using an integrated approach, involving all stakeholders and closing loopholes in existing regulations.

Changes in prey importance and prey niche overlap of sexes during the alpine newt breeding season

Urodeles, including European newts, are usually sexually dimorphic predators. Among newts, the alpine newt has the most pronounced sexual size dimorphism (in favour of females). Gender is a factor that is often associated with intra-specific diet differences. Despite the significant number of dietary studies on the alpine newt, some topics such as the breadth of the trophic niche and its overlap between sexes, or inter-sexual differences in qualitative and quantitative composition of prey remain unresolved. The present study dealing with these questions was conducted at two localities (ponds at an elevation of about 450 m) in the Czech Republic. Newts were captured from the banks during the entire breeding season using a dip net, and the stomach contents were extracted using a stomach flushing technique. Altogether 190 individuals were sampled, and a total of 1,417 prey items were obtained. The available food sources differed over the course of the breeding season, as newts changed the taxa they preyed on. This reflects the ability of newts to switch between several hunting strategies. The overall food niche overlap between the sexes was relatively large (C = 0.761, resp. C = 0.797). Inter-sexual differences were detected at both localities, mainly in the number of prey items consumed from the most important prey categories such as Rana eggs or Isopoda, which were consumed in higher numbers by females. The findings of this study suggest that females are more sensitive to the trade-off between energy intake and expenditure during the breeding season.

Distribucija velikih mrmoljaka u Srbiji - pregled i dopuna

Four, morphologically similar species of crested newts (genus Triturus) meet and hybridize in Serbia, making a complex system with several hybrid zones. The puzzling and rapidly changing taxonomic status of crested newts has been a major issue in getting hold of their distribution. We provide an overview of the current knowledge on Triturus taxonomy and compile available faunistic data into a distribution map, highlighting the species contact and hybrid zones. At the present state of faunistic and genetic research, the northwestern , northeastern , Eastern and southeastern parts of Serbia transpire as areas that are exceptionally important for the diversity of crested newts.

Massive introgression of major histocompatibility complex (MHC) genes in newt hybrid zones.

Variation in the vertebrate major histocompatibility complex (MHC) genes is crucial for fighting pathogen assault. Because new alleles confer a selective advantage, MHC should readily introgress between species, even under limited hybridization. Using replicated transects through two hybrid zones between strongly reproductively isolated European newts, Lissotriton montandoni and L.vulgaris, we demonstrated recent and ongoing MHC class I and II introgression in the Carpathian region. The extent of introgression correlated with the age of contact. In the older zone, MHC similarity between species within transects exceeded similarity between transects within species, implying pervasive introgression - a massive exchange of MHC genes, not limited to specific variants. In simulations, the observed pattern emerged under the combined action of balancing selection and hybridization, but not when these processes acted separately. Thus, massive introgression at advanced stages of divergence can introduce novel and restore previously lost MHC variation, boosting the adaptive potential of hybridizing taxa. In consequence, MHC genes may be the last to stop introgressing between incipient species.

Differential introgression across newt hybrid zones: Evidence from replicated transects.

Genomic heterogeneity of divergence between hybridizing species may reflect heterogeneity of introgression, but also processes unrelated to hybridization. Heterogeneous introgression and its repeatability can be directly tested in natural hybrid zones by examining multiple transects. Here, we studied hybrid zones between the European newts Lissotriton montandoni and two lineages of Lissotriton vulgaris, with replicate transects within each zone. Over 1,000 nuclear genes located on a linkage map and mitochondrial DNA were investigated using geographical and genomic clines. Overall, the five transects were all similar, showing hallmarks of strong reproductive isolation: bimodal distribution of genotypes in central populations and narrow allele frequency clines. However, the extent of introgression differed between the zones, possibly as a consequence of their different ages, as suggested by the analysis of heterozygosity runs in diagnostic markers. In three transects genomic signatures of small-scale (~2km) zone movements were detected. We found limited overlap of cline outliers between transects, and only weak evidence of stronger differentiation of introgression between zones than between transects within zones. Introgression was heterogeneous across linkage groups, with patterns of heterogeneity similar between transects and zones. Predefined candidates for increased or reduced introgression exhibited only a subtle tendency in the expected direction, suggesting that interspecific differentiation is not a reliable indicator for the strength of introgression. These hierarchically sampled hybrid zones of apparently different ages show how introgression unfolds with time and offer an excellent opportunity to dissect the dynamics of hybridization and architecture of reproductive isolation at advanced stages of speciation.

Captivity and Infection by the Fungal Pathogen Batrachochytrium salamandrivorans Perturb the Amphibian Skin Microbiome.

The emerging fungal pathogen, Batrachochytrium salamandrivorans (Bsal) is responsible for the catastrophic decline of European salamanders and poses a threat to amphibians globally. The amphibian skin microbiome can influence disease outcome for several host-pathogen systems, yet little is known of its role in Bsal infection. In addition, many experimental in-vivo amphibian disease studies to date have relied on specimens that have been kept in captivity for long periods without considering the influence of environment on the microbiome and how this may impact the host response to pathogen exposure. We characterized the impact of captivity and exposure to Bsal on the skin bacterial and fungal communities of two co-occurring European newt species, the smooth newt, Lissotriton vulgaris and the great-crested newt, Triturus cristatus. We show that captivity led to significant losses in bacterial and fungal diversity of amphibian skin, which may be indicative of a decline in microbe-mediated protection. We further demonstrate that in both L. vulgaris and T. cristatus, Bsal infection was associated with changes in the composition of skin bacterial communities with possible negative consequences to host health. Our findings advance current understanding of the role of host-associated microbiota in Bsal infection and highlight important considerations for ex-situ amphibian conservation programmes.

Relationships between seasonal (spring, summer, autumnal) thermal variations and cell proliferation in heterothermic vertebrates, as revealed by PCNA expression in the brain of adult Triturus carnifex

Inspired both by the literature reports and our previous findings on the question if a seasonal cycle alone, consisting of temperature and photoperiod variations, might impact on or activate natural proliferative fluctuations or unmask a latent spontaneous proliferative power in adult brain of poikilothermal Anamnia (fresh water, earth-dwelling) and Amniota (terrestrial), consequently allowing for encephalic reparative and even regenerative potentialities, an investigation has been carried on in normal adult brain of Triturus carnifex caught in nature in spring, summer, autumn. Cells immunostained for PCNA, i.e. cycling cells, were found scattered (“matrix cells”) in the olfactory territories, where they appeared scarce in spring, more frequent in summer, noticeable in autumn; also, immunostained cells were found clustered in “matrix areas”, also named zonae germinativae dorsales and ventrales, in the telencephalic hemispheres: few clusters in spring, an intermediate condition in summer, frequent cell groups in autumn. These results reveal an increasing trend in proliferation from spring, through summer, to autumn. This scenario was appreciable in the forebrain, mainly in the olfactory and telencephalic districts, which is the typical site of stem cells. Signs of potential proliferative activity are well appreciable in the urodele Amphibians, which are the best provided among vertebrates with reparative and regenerative power and possess the richest endowment of dormant cells susceptible to be recruited to proliferation.

Translocation of a large population of great crested newts

The great crested newt, Triturus cristatus, is a European Protected Species. Its legal protection requires appropriate mitigation and compensation measures to be developed for populations threatened by built development in order to demonstrate no likely detriment to the maintenance of the favourable conservation status of the species in its natural range. A major regeneration project at a site near Neath Port Talbot in South Wales, United Kingdom, resulted in the destruction of the breeding sites and associated terrestrial habitats of a population of great crested newts. Capture and translocation of 9,500 newts of all life stages was undertaken between 2009 and 2016 to an adjacent receptor site with waterbodies and extensive terrestrial habitats. Eggs and larvae have been observed in waterbodies in the receptor site throughout the monitoring period from 2013 to 2017, and great crested newts are colonising new waterbodies. The translocated population was much larger than the population size predicted from the baseline surveys of waterbodies on the development site. The design, planning and licensing of mitigation and compensation schemes for great crested newts threatened by built development projects need to give full weight to the limitations of survey methods when estimating the size of a population.

Phylogenomics of the adaptive radiation of Triturus newts supports gradual ecological niche expansion towards an incrementally aquatic lifestyle

Newts of the genus Triturus (marbled and crested newts) exhibit substantial variation in the number of trunk vertebrae (NTV) and a higher NTV corresponds to a longer annual aquatic period. Because the Triturus phylogeny has thwarted resolution to date, the evolutionary history of NTV, annual aquatic period, and their potential coevolution has remained unclear. To resolve the phylogeny of Triturus, we generated a c. 6000 transcriptome-derived marker data set using a custom target enrichment probe set, and conducted phylogenetic analyses using: (1) data concatenation with RAxML, (2) gene-tree summary with ASTRAL, and (3) species-tree estimation with SNAPP. All analyses produce the same, highly supported topology, despite cladogenesis having occurred over a short timeframe, resulting in short internal branch lengths. Our new phylogenetic hypothesis is consistent with the minimal number of inferred changes in NTV count necessary to explain the diversity in NTV observed today. Although a causal relationship between NTV, body form, and aquatic ecology has yet to be experimentally established, our phylogeny indicates that these features have evolved together, and suggest that they may underlie the adaptive radiation that characterizes Triturus.

Body size, age and population structure of Triturus carnifex (Urodela: Salamandridae) in the context of facultative paedomorphosis

Facultative paedomorphosis occurs rarely in the genus Triturus compared to other European newts such as Ichthyosaura alpestris and Lissotriton spp., with most of observation related to single or few individuals per site. In this paper we report about body size, age and population size of two populations of Triturus carnifex with paedomorphs. Since one of the populations consisted of approximately 25% of paedomorphs, this is the first study about a population of large-bodied newts with a conspicuous number of paedomorphic individuals. We found evidences for an ecological causation of paedomorphosis, as well as further support for two recent findings about paedomorphosis: the reduction of sexual size dimorphism and the female-biased sex-ratio within paedomorphs.

Climate change produces winners and losers: Differential responses of amphibians in mountain forests of the Near East

Climate change is now considered as a serious threat to the viability of many species and consequently as one of the major drivers of global biodiversity loss. Amphibians serve critical roles in forest ecosystems and are one of the most sensitive groups to environmental change. Despite the importance of amphibians in forest ecosystems and their sensitivity to environmental changes, little is known about potential impacts of future climate change on forest-dwelling amphibians. We projected the impact of climate change on the geographic distribution of three typical species of forest-dwelling amphibians, the Balkan Crested Newt (Triturus ivanbureschi), the Anatolian Crested Newt (T. anatolicus) and the Southern Crested Newt (T. karelinii). We also evaluated the representation of suitable habitats of the three crested newts in protected areas under the current and future climatic condition. We found that the Balkan Crested Newt and the Anatolian Crested Newt are likely to lose considerable proportions of their currently suitable habitats in the future as climate changes, while the Southern Crested Newt is likely to gain new habitats. Results showed that the future coverage of the most suitable habitats inside protected areas would drop by 22% and 49.2% for the Balkan Crested Newt and for the Anatolian Crested Newt, respectively. However, results showed a 15.7% increase in the suitable habitats of the Southern Crested Newt inside protected areas. Our study suggests that forest biodiversity will be negatively affected by future climatic change. Our findings also highlight the importance of integrating the impacts of climate change into designation of new protected areas in mountain forests of the Near East.