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Nemeshazi, E.

Publications and source records attributed to Nemeshazi, E..

8 recordsLinked to original sources

Photo-based individual identification is more reliable than visible implant elastomer tags or toe clipping in young agile frogs

In amphibian capture-recapture studies, commonly used individual-identification methods include toe clipping as well as less invasive alternatives of varying cost. Yet, choosing the best method for a study is challenging, because both the reliability for identification and the severity of adverse effects of a given mark type can greatly vary between species as well as life stages. We compared the reliability of three identification methods in young agile frogs (Rana dalmatina): clipping a single phalanx, injecting visible-implant-elastomer (VIE) tags (one of six colours) under the skin, and photo-based identification using natural colouration. Individuals were regularly photographed from the start of metamorphosis onwards, and were marked by the other two methods soon after all of them finished metamorphosis. Subsequently, we checked mark retention by each method multiple times for more than a year. Photo-based identification was far more reliable than the other two methods: 100% identification success post-metamorphosis in all checking events within small housing groups, and 98% with computer-assisted identification across all housing groups. Post-metamorphic body colouration remained largely stable, and the major patterns were already present at metamorphosis. Based on VIE colour alone, we could correctly identify the animals in 77% of the checks. Green tags were the easiest to recognize. VIE often broke into smaller parts, and those were sometimes found only outside the originally tagged body part (15%) or not found at all (10%). VIE was better retained in the legs than in the arms. Dissection revealed that migrating VIE pieces can accumulate in the internal organs, especially the kidneys. The clipped toe was successfully recognized only in 41% of checks. We conclude that photo-based identification is superior to both VIE-tagging and toe tipping in young agile frogs, and this method should be preferred in future studies seeking a cost-efficient yet reliable identification method in this species.

ecology↗

Put the frog in water: simple methods for improving individual identification as demonstrated with the agile frog

Identification of individuals across time and space is required for investigating numerous evolutionary-ecology and conservation-related questions, and photo-based identification is commonly used for a broad taxonomic range. Systematic comparisons of available photo-matching software have been published for various taxa, and success of such software may greatly depend on image quality as well as the focal body parts. Yet, suitability assessments of images captured with different methods are missing. Here we tested the hypotheses that individual identification by colour patterns can be facilitated by taking into account the natural medium surrounding the animals and the natural body posture they tend to take. We developed new photography methods to enable individual identification by whole-body assessment using the agile frog (Rana dalmatina), a species with common yet so-far neglected melanin-based pattern on its limbs and back. We compared the reliability of different photography methods for computer-assisted identification in the HotSpotter software as well as for observers operating it. We found that photographing either hand-restrained frogs with towel-dried skin, or frogs moving freely in clean water enabled comparison of the dorsal surface of the whole body including the hind legs, and HotSpotter identified matching images at rates similar to the relatively more successful of previously published anuran studies (>92% listed with rank[≤]10). By contrast, submerging hand-restrained frogs in water significantly improved identification: images of re-captured individuals were always ranked as the most likely match. We attribute this outstanding performance to the combination of advantageous effects of in-water light refractions that improve the visibility of melanin patterns, and uniform body postures facilitating comparison across individuals. Observers in general successfully identified matching images and ruled out non-matching ones, but some mistakes were recorded when images featured freely moving frogs. The photography methods developed in this study should be easily adapted to most frog and toad species for reliable individual identification. Our study highlights that taking into account features of the natural environment of the studied species can improve individual identification by photographs. Because such methods are non-invasive and inexpensive, they should be especially beneficial for population monitoring programs of endangered species. Data availabilityData are available from the FigShare Repository [DOI will be assigned upon acceptance for publication]. Further supporting information for methods and results is provided as Supplement to this manuscript.

ecology↗

Interplay of genotypic and thermal sex determination shapes climatic distribution in herpetofauna

Sex is a fundamental trait of all sexually reproducing organisms, and sex-determination systems show a great diversity across the tree of life. A growing body of evidence shows that genotypic and temperature-dependent sex determination (GSD and TSD, respectively) can coexist, which theoretically can have wide-ranging consequences for demography and population persistence, especially under climate change. Temperature-induced sex reversal, resulting from combined effects of sex chromosomes and environmental temperatures on sexual development, can explain the frequent transitions between GSD and TSD, and even between different GSD systems, that happened multiple times in ectothermic vertebrates. However, general lack of empirical data on the prevalence of sex reversal has long constrained the assessment of its evolutionary-ecological significance. Here we analysed an exhaustive compilation of available data to demonstrate that the climatic distribution of extant species is explained by the combination of their sex-chromosome system (GSD) and temperature reaction norm (TSD) across the phylogeny of amphibians and some reptiles. This pattern is in accordance with predictions of the asymmetrical sex reversal theory, underscoring the importance of temperature-induced sex reversal in phylogeography, evolution, and species conservation under the threat of climate change, and highlighting the need for more empirical research on sex reversal in nature.

evolutionary biology↗

"Heat waves" experienced during larval life have species-specific consequences on life-history traits and sexual development in anuran amphibians

Extreme temperatures during heat waves can induce mass-mortality events, but can also exert sublethal negative effects by compromising life-history traits and derailing sexual development. Ectothermic animals may, however, also benefit from increased temperatures via enhanced physiological performance and the suppression of cold-adapted pathogens. Therefore, it is crucial to address how the intensity and timing of naturally occurring or human-induced heat waves affect life-history traits and sexual development in amphibians, to predict future effects of climate change and to minimise risks arising from the application of elevated temperature in disease mitigation. We raised agile frog (Rana dalmatina) and common toad (Bufo bufo) tadpoles at 19 {degrees}C and exposed them to a simulated heat wave of 28 or 30 {degrees}C for six days during one of three ontogenetic periods (early, mid or late larval development). In agile frogs, exposure to 30 {degrees}C during early larval development increased mortality. Regardless of timing, all heat-treatments delayed metamorphosis, and exposure to 30 {degrees}C decreased body mass at metamorphosis. Furthermore, exposure to 30 {degrees}C during any period and to 28 {degrees}C late in development caused female-to-male sex reversal, skewing sex ratios strongly towards males. In common toads, high temperature only slightly decreased survival and did not influence phenotypic sex ratio, while it reduced metamorph mass and length of larval development. Juvenile body mass measured two months after metamorphosis was not adversely affected by temperature treatments in either species. Our results indicate that heat waves may have devastating effects on amphibian populations, and the severity of these negative consequences, and sensitivity can vary greatly between species and with the timing and intensity of heat. Finally, thermal treatments against cold-adapted pathogens have to be executed with caution, taking into account the thermo-sensitivity of the species and the life stage of animals to be treated.

ecology↗

Effects of chlorpyrifos on early development and anti-predator behavior of agile frogs

The widespread application of pesticides makes it important to understand the impacts of these chemicals on wildlife populations. Chlorpyrifos is an organophosphate insecticide which can affect the development and behavior of aquatic organisms and may thereby alter predator-prey interactions. To investigate how environmentally relevant, sublethal concentrations of chlorpyrifos affect anti-predator behavior and larval development of the agile frog (Rana dalmatina), we exposed tadpoles to one of three concentrations (0, 0.5 and 5 g chlorpyrifos / L) either for a brief period of three days (acute exposure) or throughout larval development (chronic exposure). We observed tadpole activity and space use in the presence or absence of chemical cues of predatory fish. We also assessed mortality, time to metamorphosis, mass at metamorphosis, brain morphology and sex ratio. We found that tadpoles chronically exposed to 5 g/L chlorpyrifos swam distances that were longer by more than 20 % and exhibited body masses at metamorphosis that were lower by ca. 7 % than in control individuals, but the other fitness-related traits remained unaffected. The lower concentration of chlorpyrifos applied chronically, and either one of the acute chlorpyrifos treatments did not influence any measured trait. Our results demonstrate that exposure to chlorpyrifos can induce changes in locomotor activity and may result in lowered body mass of agile frog tadpoles, but only if the insecticide is present chronically at concentrations which are rarely reached in natural waterbodies. Thus, agile frog tadpoles appear to be relatively tolerant to chlorpyrifos, but may nonetheless suffer from its presence in situations of repeated high-dose application.

ecology↗

Novel genetic sex markers reveal unexpected lack of, and similar susceptibility to, sex reversal in free-living common toads in both natural and anthropogenic habitats

Anthropogenic environmental changes are affecting biodiversity and microevolution worldwide. Ectothermic vertebrates are especially vulnerable, since their sexual development can be disrupted by environmental changes, which can cause sex reversal, a mismatch between genetic and phenotypic sex, potentially leading to sex-ratio distortion and population decline. Despite these implications, we have scarce empirical knowledge on the incidence of sex reversal in nature. Populations in anthropogenic environments may experience sex reversal more frequently, or alternatively, they may adapt to resist sex reversal. To test these alternative hypotheses, we developed PCR-based genetic sex markers for the common toad (Bufo bufo). We assessed the prevalence of sex reversal in wild populations living in natural, agricultural and urban habitats, and the susceptibility of the same populations to two ubiquitous estrogenic pollutants in a common-garden experiment. We found negligible sex-reversal frequency in free-living adults despite the presence of various endocrine-disrupting pollutants in their breeding ponds. Individuals from different habitat types showed similar susceptibility to sex reversal in the laboratory: all genetic males developed female phenotype when exposed to 1 {micro}g/L 17- ethinylestradiol (EE2) during larval development, whereas no sex reversal occurred in response to 1 ng/L EE2 and a glyphosate-based herbicide with 3 {micro}g/L or 3 mg/L glyphosate. The latter results do not support that populations in anthropogenic habitats would have either increased propensity for or higher tolerance to chemically induced sex reversal. Thus, the surprisingly low sex-reversal frequency in wild toads compared to other ectothermic vertebrates studied before might indicate idiosyncratic, potentially species-specific resistance to sex reversal.

ecology↗

Sex reversal and ontogeny under climate change and chemical pollution: are there interactions between the effects of elevated temperature and a xenoestrogen on early development in agile frogs?

Anthropogenic environmental change poses a special threat to species in which genetic sex determination can be overwritten by the thermal and chemical environment. Endocrine disrupting chemicals as well as extreme temperatures can induce sex reversal in such species, with wide-ranging consequences for fitness, demography, population viability and evolution. Despite accumulating evidence suggesting that chemical and thermal effects may interact in ecological contexts, little is known about their combined effects on sex reversal. Here we assessed the simultaneous effects of high temperature (masculinizing agent) and 17-ethinylestradiol (EE2), a widespread xenoestrogen (feminizing agent), on sexual development and fitness-related traits in agile frogs (Rana dalmatina). We exposed tadpoles to a six-days heat wave (30 {degrees}C) and/or an ecologically relevant concentration of EE2 (30 ng/L) in one of three consecutive larval periods, and diagnosed sex reversals two months after metamorphosis using species-specific markers for genetic sexing. We found that high temperature induced female-to-male sex reversal, decreased survival, delayed metamorphosis, decreased body mass at metamorphosis, and increased the proportion of animals that had no fat bodies, while EE2 had no effect on these traits. Simultaneous exposure to heat and EE2 had non-additive effects on juvenile body mass, which were dependent on treatment timing and further complicated by a negative effect of sex reversal on body mass. These results show that environmentally relevant exposure to EE2 does not diminish the masculinizing effects of high temperature. Instead, our findings on growth suggest that climate change and chemical pollution may have complex consequences for individual fitness and population persistence in species with environment-sensitive sex determination.

pharmacology and toxicology↗

Evolutionary and demographic consequences of temperature-induced masculinization under climate warming: the effects of mate choice

BackgroundOne of the dangers of global climate change to wildlife is distorting sex ratios by temperature-induced sex reversals in populations where sex determination is not exclusively genetic, potentially leading to population collapse and/or sex-determination system transformation. Here we introduce a new concept on how these outcomes may be altered by mate choice if sex-chromosome-linked phenotypic traits allow females to choose between normal and sex-reversed (genetically female) males. ResultsWe developed a theoretical model to investigate if preference for sex-reversed males would spread and affect demographic and evolutionary processes under climate warming. We found that preference for sex-reversed males 1) more likely spread in ZW/ZZ than in XX/XY sex-determination systems, 2) in populations starting with ZW/ZZ system, it significantly hastened the transitions between different sex-determination systems and maintained more balanced adult sex ratio for longer compared to populations where all females preferred normal males; and 3) in ZZ/ZW systems with low but nonzero viability of WW individuals, a widespread preference for sex-reversed males saved the populations from early extinction. ConclusionsOur results suggest that climate change may affect the evolution of mate choice, which in turn may influence the evolution of sex-determination systems, sex ratios, and thereby adaptive potential and population persistence.

evolutionary biology↗