Integrating adult occurrence and reproduction data to identify conservation measures for amphibians.

Monitoring programs are pivotal to establishing sound management. Due to economic, logistic, and time limitations, monitoring programs often overlook differences among life-history stages. However, species occurrence does not necessarily mean population viability, and it is unclear to what extent monitoring programs that do not consider separately adult presence and reproduction provide effective management indications. Unfortunately, collecting data on certain life stages requires high sampling effort, leading to a trade-off between model reliability and resources needed for monitoring. We collected data on presence and reproduction of amphibians by monitoring 207 waterbodies in Lombardy (northern Italy) in 2017-2022. We then used multistate occupancy models to test whether certain environmental features, namely, pond area, hydroperiod, forest cover, shade, aquatic vegetation, and predators' presence, differentially affected adult occurrence and breeding probabilities of multiple amphibian species. To assess optimal sampling efforts, we modeled the detection probabilities of adults and reproduction across multiple species. Finally, we identified the optimal monitoring strategy under different scenarios of resource availability, comparing adult-only monitoring versus joint assessment of the occurrence of adults and reproduction. In many cases, the main drivers of adult occurrence and reproduction did not coincide because most investigated ecological variables affected one life stage or the other. Forest area, for instance, increased occurrence probabilities of adults of the endemic Rana latastei but showed no effect on their reproduction probabilities. Quantitative estimates of the sampling effort showed that occurrence of adults was easier to spot in 4 out of 7 species. Multicriteria decision analyses showed that when resources were scarce, monitoring adults was the optimal strategy for those 4 species. Conversely, with more resources, monitoring both adults and reproduction emerged as the best strategy for all the considered species. Integrated monitoring of adults and reproduction is essential to comprehensively identify effective conservation measures for amphibians.

Integración de datos de presencia adulta y de reproducción para identificar medidas de conservación para los anfibios Resumen Los programas de monitoreo son fundamentales para establecer una gestión adecuada. Debido a limitaciones económicas, logísticas y de tiempo, los programas de seguimiento suelen pasar por alto las diferencias entre las distintas fases del ciclo de vida. Sin embargo, la presencia de especies no significa necesariamente la viabilidad de la población, y no está claro hasta qué punto los programas de seguimiento que no consideran por separado la presencia de adultos y la reproducción proporcionan indicaciones eficaces para la gestión. Desgraciadamente, la recolección de datos sobre etapas determinadas del ciclo de vida requiere un gran esfuerzo de muestreo, lo que lleva a un compromiso entre la fiabilidad del modelo y los recursos necesarios para el seguimiento. Recopilamos datos sobre la presencia y reproducción de anfibios mediante el monitoreo de 207 cuerpos de agua en Lombardía (norte de Italia) entre 2017 y 2022. Después utilizamos modelos de ocupación multiestado para comprobar si determinadas características ambientales (superficie de los estanques, hidroperiodo, cubierta forestal, sombra, vegetación acuática y presencia de depredadores) afectaban de forma diferencial la presencia de adultos y a las probabilidades de reproducción de múltiples especies de anfibios. Para evaluar los esfuerzos de muestreo óptimos, modelamos las probabilidades de detección de adultos y reproducción de múltiples especies. Por último, identificamos la estrategia de seguimiento óptima en diferentes escenarios de disponibilidad de recursos y comparamos el seguimiento exclusivo de adultos frente a la evaluación conjunta de la presencia de adultos y reproducción. En muchos casos, los principales factores en la presencia de adultos y en la reproducción no coincidían, ya que la mayoría de las variables ecológicas investigadas afectaban a una u otra etapa del ciclo. La cubierta forestal, por ejemplo, aumentó la probabilidad de presencia de adultos de la especie endémica Rana latastei pero no mostraron un efecto sobre su probabilidad de reproducción. Las estimaciones cuantitativas del esfuerzo de muestreo mostraron que la presencia de adultos era más fácil de detectar en cuatro de las siete especies. Los análisis de decisión multicriterio mostraron que, cuando los recursos eran escasos, el seguimiento de los adultos era la estrategia óptima para esas cuatro especies. Por el contrario, con más recursos, el seguimiento tanto de los adultos como de la reproducción resultó ser la mejor estrategia para todas las especies consideradas. El seguimiento integrado de los adultos y la reproducción es esencial para identificar de forma exhaustiva medidas de conservación eficaces para los anfibios.

Spatial ecology of crested porcupine in a metropolitan landscape.

Human settlements, including cities, may provide wildlife with new ecological niches, in terms of habitat types and food availability, thus requiring plasticity for adaptation. The crested porcupine Hystrix cristata is a habitat-generalist, large-sized rodent, also recorded in some suburban areas, but no information is available on its habitat use in metropolitan landscapes. Here, we assessed the land-use factors influencing the presence of crested porcupines in a metropolitan area of Central Italy. We collected data on the occurrence of crested porcupines from the metropolitan area of Rome, following an observer-oriented approach to record occurrences and retreive pseudo-absences. We then related the presence/absence of H. cristata to landscape composition. Occupancy models showed that cultivations and scrubland were positively related to porcupine presence, most likely as they provide food resources and shelter sites, respectively. Although the crested porcupine has been confirmed as a "generalist" species in terms of habitat selection, a strong preference for areas limiting the risk of being killed and providing enough food and shelter was observed. We therefore suggest that the crested porcupine may adapt to deeply modified landscapes such as large cities by selecting specific favourable land-use types.

Long-term drivers of persistence and colonization dynamics in spatially structured amphibian populations.

Many organisms live in networks of local populations connected by dispersing individuals, called spatially structured populations (SSPs), where the long-term persistence of the entire network is determined by the balance between 2 processes acting at the scale of local populations: extinction and colonization. When multiple threats act on an SSP, a comparison of the different factors determining local extinctions and colonizations is essential to plan sound conservation actions. We assessed the drivers of long-term population dynamics of multiple amphibian species at the regional scale. We used dynamic occupancy models within a Bayesian framework to identify the factors determining persistence and colonization of local populations. Because connectivity among patches is fundamental to SSPs dynamics, we considered 2 measures of connectivity acting on each focal patch: incidence of the focal species and incidence of invasive crayfish. We used meta-analysis to summarize the effect of different drivers at the community level. Persistence and colonization of local populations were jointly determined by factors acting at different scales. Persistence probability was positively related to the area and the permanence of wetlands, whereas it was negatively related to occurrence of fish. Colonization probability was highest in semipermanent wetlands and in sites with a high incidence of the focal species in nearby sites, whereas it showed a negative relationship with the incidence of invasive crayfish in the landscape. By analyzing long-term data on amphibian population dynamics, we found a strong effect of some classic features commonly used in SSP studies, such as patch area and focal species incidence. The presence of an invasive non-native species at the landscape scale emerged as one of the strongest drivers of colonization dynamics, suggesting that studies on SSPs should consider different connectivity measures more frequently, such as the incidence of predators, especially when dealing with biological invasions.

Factores a Largo Plazo de la Persistencia y las Dinámicas Colonizadoras en una Población Anfibia Estructurada Espacialmente Resumen Muchos organismos viven en redes formadas por poblaciones locales conectadas por individuos dispersos, llamadas poblaciones estructuradas espacialmente (PEE), en donde la persistencia a largo plazo de la red completa está determinada por dos procesos que actúan a escala local en las poblaciones: extinción y colonización. Cuando múltiples amenazas actúan sobre una PEE, es esencial una comparación entre los diferentes factores que determinan las extinciones y colonizaciones locales para planear acciones de conservación prudentes. Analizamos los factores a largo plazo de las dinámicas poblaciones de varias especies anfibias a escala regional. Usamos modelos de ocupación dinámica dentro de un marco de trabajo bayesiano para identificar los factores que determinan la persistencia y colonización de las poblaciones locales. Ya que la conectividad entre los fragmentos es fundamental para las dinámicas de las PEE, consideramos dos medidas de conectividad que actúan sobre cada fragmento focal: la incidencia de las especies focales y la incidencia de cangrejos de río invasores. Usamos un meta análisis para resumir el efecto de los diferentes factores a nivel de comunidad. La persistencia y la colonización de las poblaciones locales estuvieron determinadas en conjunto por los factores que actúan a diferentes escalas. La probabilidad de persistencia estuvo relacionada positivamente con el área y la permanencia de los humedales; mientras que estuvo relacionada negativamente con la presencia de peces. La probabilidad de colonización fue más alta en los humedales semipermanentes y en sitios con una alta incidencia de especies focales en sitios cercanos; mientras que mostró una relación negativa con la incidencia de los cangrejos de río invasores en el paisaje. Cuando analizamos los datos a largo plazo de las dinámicas de las poblaciones anfibias, encontramos un efecto firme de algunos rasgos clásicos de uso común en los estudios de las PEE, como el área del fragmento y la incidencia de la especie focal. La presencia de una especie invasora no nativa a escala de paisaje surgió como uno de los factores más fuertes para las dinámicas de colonización, lo que sugiere que los estudios sobre las PEE deberían considerar diferentes medidas de conectividad con mayor frecuencia, como lo es la incidencia de depredadores, especialmente cuando se está trabajando con invasiones biológicas.

Close encounters of the three morphs: Does color affect aggression in a polymorphic lizard?

Color polymorphism is genetically controlled, and the process generating and maintaining morphs can affect speciation/extinction rates. Color badges are useful signals in intraspecific communication because they convey information about alternative strategies and can potentially decrease unnecessary conflicts among different color morphs. Competition and aggressive interactions among color morphs can contribute to polymorphism maintenance. This could lead to an uneven spatial distribution of morphs in a population because the local frequency of each morph establishes the intensity of the competition and the fitness of each male. We used a polymorphic lizard, Podarcis muralis, to assess if aggression varies among morphs under two contrasting hypotheses: a heteromorphic versus homomorphic aggression. We used laboratory mirror tests after lizard color manipulation, and we verified the consistency of results with an analysis of the spatial distribution of morphs in a wild population. Both the experiments confirmed that aggression is more common during homomorphic than heteromorphic contests. The adoption of alternative behavioral strategies that minimize risks and costs could facilitate the stable coexistence of the phenotypes and reduce competition. A bias in aggression would advantage rarer morph, which would suffer less harassment by common morphs obtaining a fitness advantage. This process would be negatively-frequency-dependent and would stabilize polymorphism, possibly contributing to sympatric speciation.

Continental-scale determinants of population trends in European amphibians and reptiles.

The continuous decline of biodiversity is determined by the complex and joint effects of multiple environmental drivers. Still, a large part of past global change studies reporting and explaining biodiversity trends have focused on a single driver. Therefore, we are often unable to attribute biodiversity changes to different drivers, since a multivariable design is required to disentangle joint effects and interactions. In this work, we used a meta-regression within a Bayesian framework to analyze 843 time series of population abundance from 17 European amphibian and reptile species over the last 45 years. We investigated the relative effects of climate change, alien species, habitat availability, and habitat change in driving trends of population abundance over time, and evaluated how the importance of these factors differs across species. A large number of populations (54%) declined, but differences between species were strong, with some species showing positive trends. Populations declined more often in areas with a high number of alien species, and in areas where climate change has caused loss of suitability. Habitat features showed small variation over the last 25 years, with an average loss of suitable habitat of 0.1%/year per population. Still, a strong interaction between habitat availability and the richness of alien species indicated that the negative impact of alien species was particularly strong for populations living in landscapes with less suitable habitat. Furthermore, when excluding the two commonest species, habitat loss was the main correlate of negative population trends for the remaining species. By analyzing trends for multiple species across a broad spatial scale, we identify alien species, climate change, and habitat changes as the major drivers of European amphibian and reptile decline.

Biodiversity communication in the digital era through the Emoji tree of life.

Emojis enable direct expressions of ideas and emotions in digital communication, also contributing to discussions on biodiversity conservation. Nevertheless, the ability of emojis to represent the Earth's tree of life remains unexplored. Here, we quantified the taxonomic comprehensiveness of currently available nature-related emojis and tested whether the expanding availability of emojis enables a better coverage of extant biodiversity. Currently available emojis encompass a broad range of animal species, while plants, fungi, and microorganisms are underrepresented. Within animals, vertebrates are significantly overrepresented compared to their actual richness, while arthropods are underrepresented. Notwithstanding these taxonomic disparities, animal taxa represented by emojis more than doubled from 2015 to 2022, allowing an improved representation of both taxonomic and phylogenetic diversity, driven by the recent addition of cnidarians and annelids. Creating an inclusive emoji set is essential to ensure a fair representation of biodiversity in digital communication and showcase its importance for biosphere functioning.

Spatial ecology of the invasive Asian common toad in Madagascar and its implications for invasion dynamics.

Invasion dynamics are determined, among other aspects, by the spatial behaviour of invasive populations. The invasive toad Duttaphrynus melanostictus is spreading inland from the eastern coast of Madagascar, causing considerable ecological impacts. Understanding the basic factors determining the spread dynamics can inform management strategies and provide insights into spatial evolutionary processes. We radio-tracked 91 adult toads in three localities along the invasion gradient to determine whether spatial sorting of dispersive phenotypes is occurring, and investigate intrinsic and extrinsic determinants of spatial behaviour. Overall, toads in our study appeared as habitat generalists, and their sheltering behaviour was tied to water proximity, with toads changing shelter more frequently closer to waterbodies. Toads showed low displacement rates (mean = 4.12 m/day) and quite a philopatric behaviour but were able to perform daily movements of over 50 m. We did not detect any spatial sorting of dispersal-relevant traits nor sex- or size-biased dispersal. Our results suggest that toads are more likely to expand their range during the wet season, and that the range expansion is probably dominated by short-distance dispersal at this stage of the invasion, although a future increase in invasion speed is expected, due to the capacity for long-distance movements of this species.

Effects of temperature and precipitation changes on shifts in breeding phenology of an endangered toad.

In the last century, a plethora of species have shown rapid phenological changes in response to climate change. Among animals, amphibians exhibit some of the greatest responses since their activity strongly depends on temperature and rainfall regimes. These shifts in phenology can have negative consequences for amphibian fitness. Thus, understanding phenological changes in amphibians is pivotal to design conservation actions to mitigate climate change effects. We used data on Common Spadefoot Toad (Pelobates fuscus) reproductive migration to wetlands over a period of 8 years in Italy to (i) identify the factors related to breeding migrations, (ii) assess potential phenological shifts in the breeding period, and (iii) determine which climatic factors are related to the observed phenological shifts. Our results showed that toads migrate to spawning sites preferably in early spring, on rainy days with temperatures of 9-14 °C, and with high humidity. Furthermore, despite an increase in average temperature across the study period, we observed a delay in the start of breeding migrations of 12.4 days over 8 years. This counterintuitive pattern was the result of a succession of hot and dry years that occurred in the study area, highlighting that for ephemeral pond breeders, precipitation could have a larger impact than temperature on phenology. Our results belie the strong presumption that climate change will shift amphibian phenology toward an earlier breeding migration and underline the importance of closely investigating the environmental factors related to species phenology.

Decline and Extinction of the Italian Agile Frog Rana latastei from Core Areas of Its Range.

Detecting the trends of species and populations is fundamental to identifying taxa with high conservation priority. Unfortunately, long-term monitoring programs are challenging and often lacking. The Italian agile frog Rana latastei is endemic to Northern Italy and adjacent countries, is considered vulnerable by the IUCN, and is protected at the European level. However, quantitative estimates of its decline are extremely scarce. In this study, we document the trends in abundance and distribution of Rana latastei within Monza Park, which currently represents the area closer to the type locality of the species and holds unique genetic features. Wetlands within the park were monitored from 2000 to 2023; counts of egg clutches were taken as a measure of reproductive output and the abundance of breeding females. In 2000, the species occurred over a significant proportion of the park. Total abundance showed strong yearly variation but remained rather constant from 2000 to 2019. However, Rana latastei disappeared from the park around 2021 and was never detected in 2022-2023. The decline is probably related to the joint effect of multiple factors, including the conversion of breeding sites for farming, inappropriate water management, invasive alien species, and severe drought. The local extinction of Rana latastei occurred despite legal protection, highlighting the need for more effective and stringent tools for the conservation of European biodiversity.

Assessing Population Trends of Species with Imperfect Detection: Double Count Analyses and Simulations Confirm Reliable Estimates in Brown Frogs.

Most animal species are detected imperfectly and overlooking individuals can result in a biased inference of the abundance patterns and underlying processes. Several techniques can incorporate the imperfect detection process for a more accurate estimation of abundance, but most of them require repeated surveys, i.e., more sampling effort compared to single counts. In this study, we used the dependent double-observer approach to estimate the detection probability of the egg clutches of two brown frog species, Rana dalmatina and R. latastei. We then simulated the data of a declining population at different levels of detection probability in order to assess under which conditions the double counts provided better estimates of population trends compared to naïve egg counts, given the detectability of frog clutches. Both species showed a very high detection probability, with average values of 93% for Rana dalmatina and 97% for R. latastei. Simulations showed that not considering imperfect detection reduces the power of detecting population trends if detection probability is low. However, at high detection probability (>80%), ignoring the imperfect detection does not bias the estimates of population trends. This suggests that, for species laying large and easily identifiable egg clutches, a single count can provide useful estimates if surveys are correctly timed.

The Early Season Community of Flower-Visiting Arthropods in a High-Altitude Alpine Environment.

In mountain ecosystems, climate change can cause spatiotemporal shifts, impacting the composition of communities and altering fundamental biotic interactions, such as those involving flower-visiting arthropods. On of the main problems in assessing the effects of climate change on arthropods in these environments is the lack of baseline data. In particular, the arthropod communities on early flowering high-altitude plants are poorly investigated, although the early season is a critical moment for possible mismatches. In this study, we characterised the flower-visiting arthropod community on the early flowering high-altitude Alpine plant, Androsace brevis (Primulaceae). In addition, we tested the effect of abiotic factors (temperature and wind speed) and other variables (time, i.e., hour of the day, and number of flowers per plant) on the occurrence, abundance, and diversity of this community. A. brevis is a vulnerable endemic species growing in the Central Alps above 2000 m asl and flowering for a very short period immediately after snowmelt, thus representing a possible focal plant for arthropods in this particular moment of the season. Diptera and Hymenoptera were the main flower visitors, and three major features of the community emerged: an evident predominance of anthomyiid flies among Diptera, a rare presence of bees, and a relevant share of parasitoid wasps. Temperature and time (hour of the day), but not wind speed and number of flowers per plant, affected the flower visitors' activity. Our study contributes to (1) defining the composition of high-altitude Alpine flower-visiting arthropod communities in the early season, (2) establishing how these communities are affected by environmental variables, and (3) setting the stage for future evaluation of climate change effects on flower-visiting arthropods in high-altitude environments in the early season.

Condition- and context-dependent variation of sexual dimorphism across lizard populations at different spatial scales.

The evolution of sexual dimorphism (SD) is driven by intricate interplays between sexual and natural selection. When it comes to SD variation within populations, however, environmental factors play a major role. Sexually selected traits are expected to be strongly dependent on individual body condition, which is influenced by the local environment that individuals experience. As a consequence, the degree of SD may also depend on resource availability. Here, we investigated the potential drivers of SD expression at two sexually dimorphic morphometric traits, body size (snout vent length) and head shape (head geometric morphometrics), in the Italian wall lizard (Podarcis siculus). We assessed the existence of condition- and context-dependent SD across ten islands of the Aeolian archipelago (southern Italy), at within- and among-population scales. We observed strong geographical variation of SD among islands, and tested three potential SD predictors related to resource availability (individual body condition, ecosystem productivity, temperature). Body condition and ecosystem productivity were the main drivers of body size SD variation, and body condition was also the main driver for head shape SD. Our results highlight that the expression of SD in the Italian wall lizard is both condition- and context-dependent. These results are congruent at within- and among-populations scales highlighting that spatial multi-scale analysis represents a useful approach to understand patterns of SD expression.

Statistical methodology for the evaluation of leukocyte data in wild reptile populations: A case study with the common wall lizard (Podarcis muralis).

The leukocyte profile has the potential to be a reliable method to measure health conditions and stress in wild animals, but limitations occur because current knowledge on reference intervals is largely incomplete, especially because data come from studies on captive animals involving few individuals from single populations. Here we propose a general framework for achieving reliable leukocyte reference intervals, encompassing a set of internal and external factors, potentially affecting the leukogram. To do so, we present a systematic survey of the hematology of the common wall lizard, Podarcis muralis, involving 794 lizards from 54 populations over the whole geographic range of the species in Italy. Reference intervals for white blood cell (WBC) and leukocyte differential count were obtained by using linear mixed models in a Bayesian framework. The application of the procedure clearly showed that both internal (sex and size) and external (latitude and season) factors are a source of variation of leukocyte profile. Furthermore, the leukogram of common wall lizard has a strong variability among populations, which accounts for more than 50% of the whole variation. Consequently, some common assumptions used in studies on captive individuals are no longer supported in wild populations, namely, i) any group of individuals is a representative sample, ii) any population is representative of all others, iii) geographic clines do not occur over the species range, and iv) seasonal variation has limited effects. We encourage researchers aimed at the definition of leukocyte reference intervals for wild populations of reptiles to involve a large number of populations over a wide geographic range in ad hoc statistical models to disentangle local and geographic effects on leukocyte profile variation.