Spadefoot Toad Research Articles

False Spring in the Spawning Migrations of Spadefoot Toads (Pelobates, Anura): Distribution in European Russia and the Phenomenon Scale in 2020

False Spring in the Spawning Migrations of Spadefoot Toads (Pelobates, Anura): Distribution in European Russia and the Phenomenon Scale in 2020

Females alter their mate preferences depending on hybridization risk.

Mating with another species is often maladaptive because it generally results in no or low-fitness offspring. When hybridization is sufficiently costly, individuals should avoid mating with heterospecifics even if it reduces their ability to mate with high-quality conspecifics that resemble heterospecifics. Here, we used spadefoot toads, Spea multiplicata, to evaluate whether females alter their preferences for conspecific male sexual signals (call rate) depending on heterospecific presence. When presented with conspecific signals against a background including both conspecific and heterospecific signals, females preferred male traits that were most dissimilar to heterospecifics-even though these signals are potentially associated with lower-quality mates. However, when these same females were presented with a background that included only conspecific signals, some females switched their preferences, choosing conspecific signals that were exaggerated and indicative of high-quality conspecific mates. Because only some females switched their preferences between these two chorus treatments, there was no population-level preference for exaggerated conspecific male signals in the absence of heterospecifics. These results show that hybridization risk can alter patterns of mate choice and, consequently, sexual selection on male signals. Moreover, they emphasize that the strength and expression of reproductive barriers between species (such as mate choice) can be context-dependent.

Climate Change Alters Sexual Signaling in a Desert-Adapted Frog.

AbstractClimate change is altering species' habitats, phenology, and behavior. Although sexual behaviors impact population persistence and fitness, climate change's effects on sexual signals are understudied. Climate change can directly alter temperature-dependent sexual signals, cause changes in body size or condition that affect signal production, or alter the selective landscape of sexual signals. We tested whether temperature-dependent mating calls of Mexican spadefoot toads (Spea multiplicata) had changed in concert with climate in the southwestern United States across 22 years. We document increasing air temperatures, decreasing rainfall, and changing seasonal patterns of temperature and rainfall in the spadefoots' habitat. Despite increasing air temperatures, spadefoots' ephemeral breeding ponds have been getting colder at most elevations, and male calls have been slowing as a result. However, temperature-standardized call characters have become faster, and male condition has increased, possibly due to changes in the selective environment. Thus, climate change might generate rapid, complex changes in sexual signals with important evolutionary consequences.

Disentangling the developmental origins of a novel phenotype: enhancement versus reversal of environmentally induced gene expression.

Increasing evidence suggests that many novel traits might have originated via plasticity-led evolution (PLE). Yet, little is known of the developmental processes that underpin PLE, especially in its early stages. One such process is 'phenotypic accommodation', which occurs when, in response to a change in the environment, an organism experiences adjustments across variable parts of its phenotype that improve its fitness. Here, we asked if environmentally induced changes in gene expression are enhanced or reversed during phenotypic accommodation of a novel, complex phenotype in spadefoot toad tadpoles (Spea multiplicata). More genes than expected were affected by both the environment and phenotypic accommodation in the liver and brain. However, although phenotypic accommodation primarily reversed environmentally induced changes in gene expression in liver tissue, it enhanced these changes in brain tissue. Thus, depending on the tissue, phenotypic accommodation may either minimize functional disruption via reversal of gene expression patterns or promote novelty via enhancement of existing expression patterns. Our study thereby provides insights into the developmental origins of a novel phenotype and the incipient stages of PLE.

Temperature regulation in the Balkan spadefoot (Pelobates balcanicus Karaman, 1928) at the beginning of nocturnal activity.

On land, the amphibians interact with the environment in a complex way-even small changes in the physiological conditions may significantly impact the behaviour and vice versa. In ectothermic tetrapods, the transition from inactive to active phase may be related to important changes in their thermal status. We studied the thermal ecology of adult Balkan spadefoots (Pelobates balcanicus Karaman, 1928) in northeastern Bulgaria. These toads spend the daytime buried between 10 and 15 cm in sandy substrates, and emerge after sunset. On the substrate, their thermal energy exchange is defined by the absence of heat flow from the sun. Secondary heat sources, like stored heat and infrared radiation from the soil play an important role for the thermal balance of the active spadefoot toads. At the beginning of their daily activity, we measured substrate temperature (at a depth of 11–12 cm), toad’s surface body temperature, and also provided thermal profiles of the animals and the substrate surface in their microhabitats. In animals which recently emerged from the substrate, the temperature was comparatively higher and was closer to that of the subsoil on the spot. After that, body temperature decreased rapidly and continued to change slowly, in correlation with air temperature. We detected a temperature gradient on the dorsal surface of the toads. On the basis of our measurements and additional data, we discuss the eventual role of air humidity and the effects of surface and skin water evaporation on the water balance and activity of the investigated toads.

Morphometric characterstics and body condition of a Common spadefoot toad Pelobates fuscus insubricus population in Lombardy.

Morphometric characterstics and body condition of a Common spadefoot toad Pelobates fuscus insubricus population in Lombardy.

Male toads change their aggregation behaviour when hybridization is favoured

In many species, males form aggregations in which they compete for access to mates. Such aggregations can consist of multiple species, such that hybridization or reproductive interference between species becomes a risk. To enhance mating success with conspecifics, males might preferentially aggregate with conspecifics to minimize the risks of mating or competing with heterospecifics, especially if females are attracted to groups of conspecific males or avoid heterospecific males. Here, we used spadefoot toads (genus Spea ) to evaluate whether males respond to the same environmental cue that females use to facultatively alter their mate choice decisions for conspecific versus heterospecific males. We took advantage of a system in which females facultatively prefer to mate with heterospecifics when doing so is adaptive. We found that males preferentially aggregate with conspecific males when hybridization is disfavoured for females (so that females prefer conspecifics); however, males show no such preference for aggregating with conspecifics when hybridization is favoured (and females are more likely to prefer heterospecifics). We did not find this pattern in a different spadefoot species where females do not adaptively hybridize; males preferentially aggregated with conspecifics in one environment and did not alter their behaviour when the environmental cue was changed. Our results therefore suggest that males track the same environmental cues that females use during mate choice. These findings highlight the potential for males to facultatively adjust their behaviour in response to competitors, as well as the role that male–male interactions might play in the likelihood and consequences of hybridization between species. • Males aggregate with conspecifics when hybridization is disfavoured. • When hybridization is favoured, males spend less time with conspecifics. • This context-dependent behaviour mirrors female mate choice. • We found no such behaviour in a congeneric species lacking adaptive hybridization.

Can stable isotopes assess habitat use in complex coastal wetlands? A case study in an amphibian species

Coastal ecosystems are among the most diverse and productive systems on earth, but they are threatened by various anthropogenic pressures. To understand the magnitude of these constraints on biodiversity, it is essential to assess habitat use of coastal species, which can be challenging in the complex matrix of habitats in coastal environments. The stable isotope method is a powerful tool to assess foraging habitat, as marine influences on the trophic web should decrease with increasing distance from the ocean. In this study, we evaluated whether isotopic values (δ15N, δ13C and δ34S) can be useful to assess habitat use in a coastal amphibian, the western spadefoot toad (Pelobates cultripes). In two coastal wetlands of the French Atlantic coast, we captured individuals from 20 to 1300 m from the seashore in order to assess whether isotopic values were related to the distance to the coastline, and we combined this dataset with data on osmolality that correlate to distance to the ocean in this species. We found divergent site-specific responses, presumably linked to the site-specific extent of a recent marine submersion, highlighting the long-lasting effects of such extreme weather event on trophic webs. In both sites however, we found a larger isotopic niche closer to the seashore suggesting wider diet or prey depending on wider resources near the sea. Overall, our results suggest that isotopic values can provide insights on habitat use depending on site-specific characteristics. Combining isotopic values with other metrics (e.g., osmolality) allows to better understand isoscapes in a site-specific context.

False spring in the spawning migrations of Spadefoot toads (Pelobates, Anura): Distribution in the European Russia and the phenomenon scale in 2020

The 2020 spring processes in the European Russia were developing according to the type of false spring. The absence or weak development of snow cover, as well as its early descent in the last decade of February, determined the rapid warming of the soil profile. A certain complex of meteorological factors led to an abnormally early start of spawning migrations of the common spadefoot toad (Pelobates fuscus (Laurenti, 1768)) and Pallas's spadefoot toad (Pelobates vespertinus (Pallas, 1771)) over a vast territory which included the northwestern, western, central and southeastern parts of the species habitat in the region. Analysis of the snow cover dynamics and the temperature course according to the data of the network of meteorological stations made it possible to assess the phenology of these species of anuran amphibians within this region using the method of reconstructing the reproductive period events of the spadefoot toads. The duration of the period between the start dates of false and true spawning migrations was more than 40 days in the west, in the center and in the south-east of the European Russia. The abnormally early formation of the 2020 false spring phenomenon in the spawning migrations of spadefoot toads is currently registered as a precedent which may have a significant impact on the reproduction success of the species of this genus.

Maintenance of phenotypic plasticity is linked to oxidative stress in spadefoot toad larvae

Maintenance of phenotypic plasticity is linked to oxidative stress in spadefoot toad larvae

Chromosome-level assembly, annotation and phylome of Pelobates cultripes, the western spadefoot toad.

Genomic resources for amphibians are still hugely under-represented in vertebrate genomic research, despite being a group of major interest for ecology, evolution and conservation. Amphibians constitute a highly threatened group of vertebrates, present a vast diversity in reproductive modes, are extremely diverse in morphology, occupy most ecoregions of the world, and present the widest range in genome sizes of any major group of vertebrates. We combined Illumina, Nanopore and Hi-C sequencing technologies to assemble a chromosome-level genome sequence for an anuran with a moderate genome size (assembly span 3.09 Gb); Pelobates cultripes, the western spadefoot toad. The genome has an N50 length of 330 Mb with 98.6% of the total sequence length assembled into 14 super scaffolds, and 87.7% complete BUSCO genes. We use published transcriptomic data to provide annotations, identifying 32,684 protein-coding genes. We also reconstruct the P. cultripes phylome and identify 2,527 gene expansions. We contribute the first draft of the genome of the western spadefoot toad, P. cultripes. This species represents a relatively basal lineage in the anuran tree with an interesting ecology and a high degree of developmental plasticity, and thus is an important resource for amphibian genomic research.

Maintenance of phenotypic plasticity is linked to oxidative stress in spadefoot toad larvae

Phenotypic plasticity allows organisms to improve the match between their phenotype and heterogeneous environments. Theoretical models have argued that costs of maintaining the sensory and response machinery necessary for adaptive phenotypic plasticity are important determinants to the evolution of plasticity. Despite recurrent arguments invoking putative metabolic costs associated with maintenance of cellular machinery, no studies have yet attempted to quantify it from a molecular standpoint. Here we experimentally examine physiological differences across genotypes (sibships) of spadefoot toad larvae with different degrees of plasticity in response to predator cues. We observed marked differences across sibships in developmental, growth and morphological responses to predators, and tested whether increased plasticity was associated with oxidative stress or immune suppression. We observed that more plastic sibships experienced higher antioxidant enzymatic activity when reared in the absence of predator cues, i.e. not expressing their plastic responses. The degree of plasticity was also associated with higher lipid peroxidation and slightly greater granulocyte‐to‐lymphocyte ratio. Higher antioxidant activity in highly plastic sibships suggests that maintenance of phenotypic plasticity may be linked to energy demanding metabolic processes. Our findings suggest that having the potential to produce plastic responses may incur oxidative and immunological costs. In the long term, such maintenance costs may erode individual fitness and even constrain the evolution of plasticity. To our knowledge, this is the first empirical evidence indicating the existence of a physiological cost to the maintenance of phenotypic plasticity.

Distance to coastline modulates morphology and population structure in a coastal amphibian

Abstract Salinization due to sea-level rise and marine submersions is expected to strongly impact coastal ecosystems. Exposure to salinity can negatively impact biodiversity especially in coastal wetlands. To understand comprehensively the consequences of environmental salinization on coastal biodiversity, it is essential to document how coastal species currently respond to exposure to salinity. In this study, we investigated how variations of environmental salinity relative to the distance to the ocean influence population structure (age ratio and sex ratio), and individual hydro-mineral balance (osmolality) and morphology (size, mass, condition) in the western spadefoot toad (Pelobates cultripes) in two populations from the French Atlantic coast. We show that distance to coastline strongly influences exposure to salt on a small spatial scale. Some variables (e.g., abundances, osmolality, morphology) responded similarly in both sites and may be related to salt deposition due to landward sea-spray. Interestingly, other variables (sex ratio and age ratio) displayed site-specific responses and appeared to be linked to the salinity of breeding sites. Distance to the shoreline appears to be a critical population structuring factor in this coastal salt-tolerant species. Future studies should investigate how distance to shoreline—and thus environmental salinity—can ultimately affect individual performances and fitness.

A decharming metamorphosis: The larval and adult morphology of the common spadefoot toad, Pelobates fuscus

Anurans are a highly diverse amphibian order with a biphasic lifestyle. The larva, better known as tadpole, and the adult frog of one species typically occupy different habitats and exploit different resources. Therefore, both are subject of largely independent selection and are able to evolve stage-specific adaptations. Among others, the musculoskeletal features of the larval and adult head of anurans and the description of their specific traits are important to gain a deeper understanding of the evolution and the phylogeny of this highly diverse group. Here we present an overview of the larval and adult cranial morphology of the common spadefoot toad Pelobates fuscus. We provide a detailed description of the cranial musculoskeletal structures based on micro-computed tomography and following 3D reconstruction of two long-term stored specimens of P. fuscus and refer to striking adaptations of this species. P. fuscus inhabits a wide spectrum of habitats including mixed forests, steppes, fields and sandy areas with soft soils in close proximity to permanent water bodies. Adults have a semi-fossorial lifestyle and they are able to dig themselves in using their hindlimbs whereas the tadpoles are the largest of all European anurans. Derived larval features are the presence of an adrostral cartilage within the lower jaw, the presence of three portions of the M. subarcualis rectus I, the presence of the M. diaphragmatopraecordialis and a bipartite suprarostral cartilage. The presence of an enlarged prehallux and the co-ossification of the frontoparietal, as well as a pterygoid that borders the orbit ventrally and rostrally are striking adult features and adaptation to the semi-fossorial lifestyle. With the described morphological features, we want to underline their importance for several adaptations which may have facilitated and stimulated the evolution of anurans and provide baseline data for further investigations.

Commensals of underground mammals: European mole (Talpa europaea, Eulipotyphla, Talpidae) and the greater mole-rat (Spalax microphthalmus, Rodentia, Spalacidae)

Abstract. Stepanova I, Andreychev A, Kulakhmetov R, Lobachev E. 2021. Commensals of underground mammals: European mole (Talpa europaea, Eulipotyphla, Talpidae) and the greater mole-rat (Spalax microphthalmus, Rodentia, Spalacidae). Biodiversitas 22: 4665-4670. The study of lodgers of burrows of underground mammals was carried out using the method of hunting cylinders (cans). In the study, 29 different representatives from the following classes were identified in the courses of the greater mole-rat and European mole: Diplopoda, Chilopoda, Gastropoda, Insecta, Amphibia, and Mammalia. Among the vertebrates captured are Eurasian common shrew (Sorex araneus), Eurasian pygmy shrew (Sorex minutus), bank vole (Clethrionomys glareolus), common spadefoot toad (Pelobates fuscus), moor frog (Rana arvalis), and common toad (Bufo bufo). Twenty-six different species have been identified among invertebrates. Many animals seek shelter in the burrows of underground mammals from enemies and adverse climatic factors for food or conditions for reproduction. In the central part of Russia, more species of commensals were found in European mole burrows (29) than in greater mole-rat burrows (21).

Female mate preferences do not predict male sexual signals across populations

Abstract New species can arise when female preferences and male sexual signals diverge across populations and thereby reduce mating between populations. Under this hypothesized mechanism for speciation, mate preferences and sexual signals should be correlated, but divergent, across populations. We evaluated this prediction using spadefoot toads (Spea multiplicata). We measured a sexually selected male signal (call rate) for which female preferences are known to vary across populations in response to the risk of hybridizing with another species. Contrary to expectation, we found no correlation between male call rate and female preferences across populations. We discuss possible mechanisms of this pattern, including the effect of gene flow from heterospecifics on male call rate. Our results suggest that, even when populations vary in mating traits, the independent evolution of female preferences and male sexual signals might impede reproductive isolation between populations.

A novel larval diet interacts with nutritional stress to modify juvenile behaviors and glucocorticoid responses.

Developmental plasticity can allow the exploitation of alternative diets. While such flexibility during early life is often adaptive, it can leave a legacy in later life that alters the overall health and fitness of an individual. Species of the spadefoot toad genus Spea are uniquely poised to address such carryover effects because their larvae can consume drastically different diets: their ancestral diet of detritus or a derived shrimp diet. Here, we use Spea bombifrons to assess the effects of developmental plasticity in response to larval diet type and nutritional stress on juvenile behaviors and stress axis reactivity. We find that, in an open‐field assay, juveniles fed shrimp as larvae have longer latencies to move, avoid prey items more often, and have poorer prey‐capture abilities. While juveniles fed shrimp as larvae are more exploratory, this effect disappears if they also experienced a temporary nutritional stressor during early life. The larval shrimp diet additionally impairs juvenile jumping performance. Finally, larvae that were fed shrimp under normal nutritional conditions produce juveniles with higher overall glucocorticoid levels, and larvae that were fed shrimp and experienced a temporary nutritional stressor produce juveniles with higher stress‐induced glucocorticoid levels. Thus, while it has been demonstrated that consuming the novel, alternative diet can be adaptive for larvae in nature, doing so has marked effects on juvenile phenotypes that may recalibrate an individual's overall fitness. Given that organisms often utilize diverse diets in nature, our study underscores the importance of considering how diet type interacts with early‐life nutritional adversity to influence subsequent life stages.

Extreme Sensitivity of Hurter's Spadefoot Toad (Scaphiopus hurterii) Tadpoles to Suspended Particulates of Finely Ground and Powdered Rations

Herein we report the high mortality of larval Hurter's spadefoot toad (Scaphiopus hurterii) tadpoles when fed dry powdered feeds. The evidence implies that dry powders remain suspended in the water column where they enter and clog the filtering apparatus of the tadpoles. When the same foods were wetted to a paste and dropped into the aquaria as a moist pellet, the ration fell directly to the substrate and did not become suspended in the water column. Mortalities of tadpoles fed dry powdered rations were severe, whereas mortalities when fed wetted feed were inconsequential. We recommend that that rations made of ground or powdered components not be fed unless first wetted. Further, we speculate that sediment and siltation of natural waters may contribute to amphibian losses via the same mechanism.

Herbivory by spadefoot toad tadpoles and reduced water level affect submerged plants in temporary ponds

ABSTRACT In temporary ponds, submerged plants have adapted to recurrent periods of drought. These ponds often lack the impact of large herbivores but can harbor large numbers of herbivorous tadpoles. Tadpoles of the Iberian spadefoot toad (Pelobates cultripes) may reach large body size and consume large quantities of macrophytes during their long larval period, which is shortened with risk of pond drying. We conducted a mesocosm experiment to analyze the interplay between hydroperiod and impact of herbivorous tadpoles on the abundance and life history of 3 species of submerged plants common to temporary ponds. We observed differences in growth among plant species resulting in lags in timing of maximum cover, probably related to interspecific competitive interactions. Some plants responded to pond drying with a remarkable increase in the production of flowers. Tadpoles greatly reduced the plant cover, although their impact varied across plant species. Differential plant consumption by these large tadpoles can substantially modify the internal structure and complexity of temporary ponds, and tadpoles can also interfere with plant responses to shortened hydroperiod.

Age, size and body condition do not equally reflect population response to habitat change in the common spadefoot toad Pelobates fuscus.

Urbanization impacts biodiversity both directly through physical expansion over land, and indirectly due to land use conversion and human behaviors associated with urban areas. We assessed the response of a common spadefoot toad population (Pelobates fuscus) to habitat loss and fragmentation resulting from urban development by studying changes in size, body condition and age parameters. We compared samples collected in the early 2000s (sample A) and later on during 2012–2014 (sample B). The terrestrial habitats in the study area were severely reduced and fragmented due to the expansion of the human settlement. We found no significant differences in the age parameters between the two sampling periods; the median lifespan shortened from 3.5 (sample A) to 3.0 years (sample B), while the other age parameters were similar in both samples. In contrast, snout-vent length, body mass and body condition experienced a significant decrease over time. Our results suggest that changes in body size and body condition, rather than age parameters, better reflect the response of the common spadefoot toad population to declining habitat quality. Therefore, body measurements can provide reliable estimates of the impact of habitat degradation in amphibian populations.