Triturus Marmoratus 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.

Hybridization and introgression in deeply differentiated salamander species – molecular genetics and a reappraisal of Dr. Louis Vallée’s osteological data

Abstract Two morphologically and genetically distinct salamander species (the crested newt, Triturus cristatus and the marbled newt, T. marmoratus) engage over a large area in the west of France where they hybridize at ca. 4%. The species interaction is characterized by ecological differentiation and limited gene flow beyond the F1 hybrid generation. Incompletely isolated species like these allow to investigate the genetic mechanisms and evolutionary forces that maintain their identity in the face of ongoing gene flow, to which a large mosaic hybrid zone provides excellent opportunities. A reanalysis of published morphological data supports the partial breakdown of the species barrier whereas extensive genetic data show that introgression is low yet asymmetric, in line with the dynamics of species replacement inferred earlier. The current work, with seven diagnostic nuclear markers studied for a large sample, revises the estimates of introgression in both T. cristatus (to 0.24%) and T. marmoratus (to 0.11%). Difficulties remain in the recognition of potential triploid hybrids versus backcross hybrids. Haldane’s rule is partially supported, but deeper analyses require the use of a molecular marker for sex that is not yet available.

Using the dead to infer about the living: Amphibian roadkill spatiotemporal dynamics suggest local populations' reduction

Roads represent one of the main sources of wildlife mortality, population decline, and isolation, especially for low-vagility animal groups. It is still not clearly understood how wildlife populations respond to these negative effects over space and time. Most studies on wildlife road mortality do not consider the spatial and temporal components simultaneously, or the imperfect roadkill detection, both of which could lead to inaccurate assumptions and unreliable mitigation actions. In this study, we applied a multi-season occupancy model to a 14-year amphibian mortality dataset collected along 120 km of roads, combined with freely available landscape and remote sensing metrics, to identify the spatiotemporal patterns of amphibian roadkill in a Mediterranean landscape in Southern Portugal. Our models showed an explicit general decrease in amphibian roadkill. The Iberian painted frog (Discoglossus galganoi) experienced roadkill declines over time of ∼70 %, while the spiny common toad (Bufo spinosus) and the fire salamander (Salamandra salamandra) had a loss of nearly 50 %, and the Southern marbled newt (Triturus pygmaeus) had 40 %. Despite the decreasing trend in roadkill, spatial patterns seem to be rather stable from year to year.Multi-season occupancy models, when combined with relevant landscape and remote sensing predictors, as well as long-term monitoring data, can describe dynamic changes in roadkill over space and time. These patterns are valuable tools for understanding roadkill patterns and drivers in Mediterranean landscapes, enabling the differentiation of road sections with varying roadkill over time. Ultimately, this information may contribute to the development of effective conservation measures.

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.

Morphological and genetic diversification of pygmy and marbled newts, with the description of a new species from the wider Lisbon Peninsula (Triturus, Salamandridae)

Abstract Iberian populations of large-bodied newts, with Triturus marmoratus in the north and T. pygmaeus in the south of the peninsula, were studied for external morphology, mitochondrial dna and for a panel of single nucleotide polymorphisms. This confirmed the species’ low level of interspecific hybridization and their parapatric, mosaic-like mutual range border across the peninsula. The genetic data also revealed substantial variation within T. pygmaeus, with narrow (0.43–35.2 km) clinal transitions in the very centre of Portugal. Similar clines were observed for body size and colouration pattern. Pygmy newts in the west of Portugal are larger, with a more striped (less reticulated) green dorso-lateral colouration pattern than those in the east and south of the country. The western group of populations is described as a new species, Triturus rudolfi sp. nov., on account of a long, ca. 2.5 Ma, independent evolutionary history and limited hybridization with its sister-species T. pygmaeus, suggesting selection against hybrid offspring. The range of the newly described species may be restricted to the wider Lisbon Peninsula, stretching northwards along the Atlantic coast to the river Vouga estuary. Inland, the range border may be set by the lower Tejo River, or by the currently wide area of agricultural land at either side of that river, that may accommodate a residual hybrid zone. The close contact between both pygmy newt species is effectively limited to a ca. 20 × 40 km area directly north of the town Entroncamento, where T. rudolfi sp. nov. is sandwiched in between T. marmoratus and the river Tejo.

Spatial genetic structure in European marbled newts revealed with target enrichment by sequence capture

European marbled newts come in two species that have abutting ranges. The northern species, Triturus marmoratus, is found in France and the northern part of the Iberian Peninsula, whereas the southern species, T. pygmaeus, is found in the southwestern corner of the Iberian Peninsula. We study the intraspecific genetic differentiation of the group because morphological data show geographical variation and because the Iberian Peninsula is a recognized center of speciation and intraspecific genetic diversity for all kinds of organisms, amphibians included. We use target enrichment by sequence capture to generate c. 7 k nuclear DNA markers. We observe limited genetic exchange between the species, which confirms their distinctiveness. Both species show substantial genetic structuring that is only in part mirrored by morphological variation. Genetically differentiated groups are found in the south (T. marmoratus) and west (T. pygmaeus) of the species ranges. Our observations highlight the position of the Iberian Peninsula as a hotspot for genetic differentiation.

Morphological and genetic diversification of Old-World marbled newts, with the description of a new and ‘not-at-all-cryptic’ subspecies from the Iberian Peninsula (Triturus, Salamandridae)

Abstract Morphological and genetic variation of organisms is generally lower in northern than in southern regions of the Palearctic. This ubiquitous geographical pattern has been associated with extinction and recolonization processes in the north versus persistence in the Mediterranean area, as governed by climate change in the Pleistocene. One area of differentiation and complexity is the Iberian Peninsula where two distinct sister-species of marbled newts possess adjoining and geographically sharply delimited ranges over the north (Triturus marmoratus) and the south of the peninsula (T. pygmaeus). Within the latter species two forms are here documented, with different colouration patterns and non-overlapping ranges. The southern form is striped, much as in T. marmoratus, and occurs to the south of the Guadalquivir River. The northern form, here described as a new subspecies, has a reticulated dorsal colouration. It occurs only north of the Guadalquivir and is thus sandwiched in between two striped marbled newt taxa. Both T. pygmaeus subspecies engage inside the Doñana National Park in a ca. 2,500 m narrow contact zone. Although an inferred substantial selection against hybrids goes a long way to support species status, a reanalysis of published genetic data is required to solve this issue, along with the wider investigation of the same type of (microsatelite) data for the southern, nominotypical subspecies.

Agricultural intensification alters marbled newt genetic diversity and gene flow through density and dispersal reduction.

Recent agricultural intensification threatens global biodiversity with amphibians being one of the most impacted groups. Because of their biphasic life cycle, amphibians are particularly vulnerable to habitat loss and fragmentation that often result in small, isolated populations and loss of genetic diversity. Here, we studied how landscape heterogeneity affects genetic diversity, gene flow and demographic parameters in the marbled newt, Triturus marmoratus, over a hedgerow network landscape in Western France. While the northern part of the study area consists of preserved hedged farmland, the southern part was more profoundly converted for intensive arable crops production after WWII. Based on 67sampled ponds and 10microsatellite loci, we characterized regional population genetic structure and evaluated the correlation between landscape variables and (i) local genetic diversity using mixed models and (ii) genetic distance using multiple regression methods and commonality analysis. We identified a single genetic population characterized by a spatially heterogeneous isolation-by-distance pattern. Pond density in the surrounding landscape positively affected local genetic diversity while arable crop land cover negatively affected gene flow and connectivity. We used demographic inferences to quantitatively assess differences in effective population density and dispersal between the contrasted landscapes characterizing the northern and southern parts of the study area. Altogether, results suggest recent land conversion affected T. marmoratus through reduction in both effective population density and dispersal due to habitat loss and reduced connectivity.

Climate change would prevail over land use change in shaping the future distribution of Triturus marmoratus in France

AbstractClimate and land use/land cover (LULC) change are two major global change factors driving shifts in the location of suitable areas for many species. Here, we assessed if a low‐vagility newt, Triturus marmoratus, can track displacement of suitable areas by 2100, and tested whether climate or LULC changes are primary drivers of the species’ future distribution. We combined niche modelling with the process‐based model simRShift to improve biological relevance and simulate species dispersal by 2100 under scenarios of climate and LULC changes at high spatial resolution. Our results show that T. marmoratus could lose a significant part of its current French range in the coming decades, and that the range loss will primarily be driven by climate change, with LULC change playing a secondary role. The species seems unlikely to be able to track the northern shift of its suitable habitat as rapidly as required given the rate of climate warming during the 21st century. This is due to insufficient dispersal ability, which is compounded by the magnitude of habitat fragmentation in the human‐dominated landscape. We highlight the need to assess vulnerability and anticipate threats arising from global change even for species that are not currently considered endangered. We identified areas where the species is most likely to occur and be extinct in the future, which can serve as a guide for population monitoring. Our framework can support conservation strategy development by defining ecological corridors that would assist species to track their required habitats in the face of global change.

Population trends of four species of amphibians in western France; results from a 15 year time series derived from road mortality counts

Reports of declining amphibians are a major concern for conservation given their role as indicators of environmental change. This includes potentially impacting on the ecology other species and highlights the importance of monitoring long-term changes in amphibian populations. The core difficulty is gathering long term data sets that as well as being time consuming, may be costly and impractical for logistical reasons. Road mortalities have value in this respect since they are highly visible and have been frequently used as a metric to monitor changes in a variety of animal populations. In this paper they have been employed as proxies to estimate long-term population changes in four European species of amphibians. From January 2005 to December 2019 a total of 747 amphibian mortalities were recorded, the majority of which were urodeles. Most individuals were adults that entered roads during the annual migration period. Long term annual counts fluctuated widely in all species and peaked during the 4-year period from 2009 to 2012 with second period of high numbers in Triturus marmoratus and Hyla arborea during 2018 and 2019. Long-term population trends were evaluated using regression analysis of the logarithmic (loge) transforms of annual counts against year as independent variables, which were then tested against a hypothetical 0 regression coefficient, indicative of population stability. The results indicated long-term stability in T. marmoratus and H. arborea but potential declines in Lissotriton helveticus and Pelophylax lessonae, the latter showing metapopulation extinctions followed by recolonisation. Stepwise regression of potential climate drivers in amphibian numbers suggested a 2-year lag of rainfall during October and December were potential factors involved in population change.

Tracing species replacement in Iberian marbled newts.

Secondary contact between closely related species can lead to the formation of hybrid zones, allowing for interspecific gene flow. Hybrid zone movement can take place if one of the species possesses a competitive advantage over the other, ultimately resulting in species replacement. Such hybrid zone displacement is predicted to leave a genomic footprint across the landscape in the form of asymmetric gene flow (or introgression) of selectively neutral alleles from the displaced to the advancing species. Hybrid zone movement has been suggested for marbled newts in the Iberian Peninsula, supported by asymmetric gene flow and a distribution relict (i.e., an enclave) of Triturus marmoratus in the range of T. pygmaeus. We developed a panel of nuclear and mitochondrial SNP markers to test for the presence of a T. marmoratus genomic footprint in the Lisbon peninsula, south of the enclave. We found no additional populations of T. marmoratus. Analysis with the software Structure showed no genetic traces of T. marmoratus in T. pygmaeus. A principal component analysis showed some variation within the local T. pygmaeus, but it is unclear if this represents introgression from T. marmoratus. The results may be explained by (a) species replacement without introgressive hybridization and (b) displacement with hybridization followed by the near‐complete erosion of the footprint by purifying selection. We predict that testing for a genomic footprint north of the reported enclave would confirm that species replacement in these marbled newts occurred with hybridization.

A genomic footprint of a moving hybrid zone in marbled newts

We developed a panel of 44 nuclear genetic markers and applied this to two species of marbled newts in the north (Triturus marmoratus) and the south (T. pygmaeus) of the Iberian Peninsula, to document pattern and process of interspecific gene flow. The northernmost occurrence of T. pygmaeus genetic material was in a T. marmoratus population north of the Vouga river estuary. This suggested the past presence of a hybrid zone, possibly coinciding with a natural river outlet at ca. 1200 A.D. Since 1808, the species contact has moved back south to a by then completed, man-made Vouga channel. We also found evidence for a T. marmoratus genomic footprint in T. pygmaeus from the Serra de Sintra, near Lisbon. In combination with a previously reported southern, relic occurrence of T. marmoratus in between both areas, the data point to the superseding with hybridization of T. marmoratus by T. pygmaeus. We estimate that the species hybrid zone has moved over a distance of ca. 215 km.

Presence of low virulence chytrid fungi could protect European amphibians from more deadly strains

Wildlife diseases are contributing to the current Earth’s sixth mass extinction; one disease, chytridiomycosis, has caused mass amphibian die-offs. While global spread of a hypervirulent lineage of the fungus Batrachochytrium dendrobatidis (BdGPL) causes unprecedented loss of vertebrate diversity by decimating amphibian populations, its impact on amphibian communities is highly variable across regions. Here, we combine field data with in vitro and in vivo trials that demonstrate the presence of a markedly diverse variety of low virulence isolates of BdGPL in northern European amphibian communities. Pre-exposure to some of these low virulence isolates protects against disease following subsequent exposure to highly virulent BdGPL in midwife toads (Alytes obstetricans) and alters infection dynamics of its sister species B. salamandrivorans in newts (Triturus marmoratus), but not in salamanders (Salamandra salamandra). The key role of pathogen virulence in the complex host-pathogen-environment interaction supports efforts to limit pathogen pollution in a globalized world.

Acoustic enrichment in wildlife passages under railways improves their use by amphibians

Linear transport infrastructure can impact wildlife directly or indirectly, and amphibians are particularly affected. In some cases, mitigation measures – such as tunnels below the linear transport infrastructure – are implemented, but an evaluation of their effectiveness is often lacking, especially for small animals such as amphibians. Few studies have focused on crossing behaviour in underpasses, yet this information may be crucial to improve mitigation measures. In this study, we conducted experiments in three tunnels below a high-speed railway with individually marked amphibians (great crested newt Triturus cristatus, marbled newt Triturus marmoratus, alpine newt Ichthyosaura alpestris, fire salamander Salamandra salamandra, spined toad Bufo spinosus, agile frog Rana dalmatina and edible/pool frog Pelophylax kl. esculentus/lessonae) which were released at the entrance of tunnels varying in length. Behaviours (e.g. completed crossing, U-turn, not moving, and stay) and crossing speed were recorded. R. dalmatina, S. salamandra and T. cristatus (but not B. spinosus) exhibited crossing rate differences between tunnels 21 m and 40 m in length. More individuals performed “complete crossing” through the shorter tunnel. The crossing speed of the S. salamandra and T. cristatus did not differ between the tunnels of different lengths. In a second experiment, we evaluated the effect of acoustic enrichment on the crossing behaviour of one frog and three newt species by broadcasting a soundtrack of mating calls of syntopic anuran species in the tunnels. Pelophylax kl exhibited a large increase in complete crossings and in speed. T. cristatus showed an increase in tunnel complete crossings (but not speed) in one of the acoustically enhanced tunnels. These results indicate that acoustic enrichment can improve the crossing of underpasses. This low cost and easily implementable method could help to inform the design of wildlife passages as mitigation measures for impacted amphibian populations, though more experiments on the effect of tunnel characteristics on amphibian behaviour would be valuable.

High pathogen prevalence in an amphibian and reptile assemblage at a site with risk factors for dispersal in Galicia, Spain.

Ranaviruses are agents of disease, mortality and population declines in ectothermic vertebrates and emergences have been repeatedly linked to human activities. Ranaviruses in the common midwife toad ranavirus lineage are emerging in Europe. They are known to be severe multi-host pathogens of amphibians and can also cause disease in reptiles. Recurrent outbreaks of ranavirus disease and mortality affecting three species have occurred at a small reservoir in north-west Spain but no data were available on occurrence of the pathogen in the other amphibian and reptile species present or at adjacent sites. We sampled nine species of amphibians and reptiles at the reservoir and nearby sites and screened for ranavirus presence using molecular methods. Our results show infection with ranavirus in all nine species, including first reports for Hyla molleri, Pelophylax perezi, Rana iberica, and Podarcis bocagei. We detected ranavirus in all four local sites and confirmed mass mortality incidents involving Lissotriton boscai and Triturus marmoratus were ongoing. The reservoir regularly hosts water sports tournaments and the risks of ranavirus dispersal through the translocation of contaminated equipment are discussed.

Habitat patches for newts in the face of climate change: local scale assessment combining niche modelling and graph theory

Triturus cristatus and Triturus marmoratus are two protected and declining newts occurring in the administrative department of Vienne, in France. They have limited dispersal abilities and rely on the connectivity between habitats and their suitability. In a warming climate, the locations of suitable habitats are expected to change, as is the connectivity. Here, we wondered how climate change might affect shifts in habitat suitability and connectivity of habitat patches, as connectivity is a key element enabling species to realize a potential range shift. We used ecological niche modelling (ENM), combining large-scale climate suitability with local scale, high-resolution habitat features, to identify suitable areas for the two species, under low and high warming scenarios (RCP 2.6 and RCP 8.5). We associated it with connectivity assessment through graph theory. The variable ‘small ponds’ contributed most to land cover-only ENMs for both species. Projections with climate change scenarios revealed a potential impact of warming on suitable habitat patches for newts, especially for T. cristatus. We observed a decrease in connectivity following a decrease in patch suitability. Our results highlight the important areas for newt habitat connectivity within the study area, and define those potentially threatened by climate warming. We provide information for prioritizing sites for acquisition, protection or restoration, and to advise landscape policies. Our framework is a useful and easily reproducible way to combine global climate requirements of the species with detailed information on species habitats and occurrence when available.

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.

Triturus newts

Ben Wielstra introduces Eurasian newts of the genus Triturus.

Influence of substrate types and morphological traits on movement behavior in a toad and newt species.

BackgroundInter-patch movements may lead to genetic mixing, decreasing both inbreeding and population extinction risks, and is hence a crucial aspect of amphibian meta-population dynamics. Traveling through heterogeneous landscapes might be particularly risky for amphibians. Understanding how these species perceive their environment and how they move in heterogeneous habitats is an essential step in explaining metapopulation dynamics and can be important for predicting species’ responses to climate change and for conservation policy and management.MethodsUsing an experimental approach, the present study focused on the movement behavior (crossing speed and number of stops) on different substrates mimicking landscape components (human-made and natural substrates) in two amphibian species contrasting in locomotion mode: the common toad (Bufo bufo), a hopping and burrowing anuran and the marbled newt (Triturus marmoratus), a walking salamander. We tested the hypothesis that species reaction to substrate is dependent on specific ecological requirements or locomotion modes because of morphological and behavioral differences.ResultsIn both species, substrate type influenced individual crossing speed, with individuals moving faster on soil than on concrete substrate. We also demonstrated that long-legged individuals moved faster than individuals with short legs. In both species, the number of stops was higher in females than in males. In common toads, the number of stops did not vary between substrates tested, whereas in marbled newts the number of stops was higher on concrete than on soil substrate.DiscussionWe highlighted that concrete substrate (mimicking roads) negatively affect the crossing speed of both studied species, with an effect potentially higher in marbled newts. Our findings corroborate negative effects of such heterogeneous landscapes on movement behavior of two amphibian species, which may have implications for the dynamics of metapopulations.

Variable effects of an invasive species on the reproduction and distribution of native species in pond networks

Abstract The arrival of non‐native species in a community can be deleterious for native species. The joint investigation of several descriptors of native populations susceptible to invaders, under different invasion contexts, may help in predicting the outcome of their co‐occurrence with invasive species. Moreover, empirical studies seldom document the relative importance of the effects of invasive species on native species compared with other factors. Using survey data, we evaluated whether reproduction (larval density) and distribution of breeding sites of three amphibian species (Rana dalmatina, Lissotriton helveticus, and Triturus marmoratus) were related to the presence of invasive red swamp crayfish Procambarus clarkii, compared to other native predators, habitat, and landscape features, in two pond networks that differed in invasion intensity. The red swamp crayfish was only negatively associated with the larval density of one amphibian species studied. Its effect size was similar to that of some native predators, and much smaller than that of the canopy cover of ponds. Amphibians were widespread in the two pond networks. The occupancy of only one species in each network was negatively related to crayfish presence, while the occupancy of all species was negatively related to fish presence. The distribution of amphibian breeding sites was positively associated with aquatic vegetation cover. Negative associations between amphibians and red swamp crayfish were detected only in a few cases, even in the most invaded area, and thus results were less alarming than in previous studies. Differences in ecological traits of native amphibians and interactions with other environmental factors may explain the variable effects of red swamp crayfish on native amphibian populations.