Terrestrial Frog Research Articles

Diet of terrestrial anurans in an ephemeral and simplified habitat during the dry season in the Brazilian Cerrado

Amphibians often use ephemeral and simplified habitats during dry seasons in tropical biomes. These simplified habitats can have less prey available, but only a few studies focus on how their use affects frogs’ diet. Here we studied the diet of three terrestrial frogs (Adenomera sp., Ameerega berohoka, and Rhinella ocellata) at a riverbank exposed only during the dry season in the Brazilian Cerrado biome. Diets overlapped more than expected by chance and were composed mainly of social insects (ants and termites). Prey volumes were not related to the size of frogs or their head measurements. Frogs at the riverbank ingested less prey categories and fewer prey items in comparison to studies conducted in more stable and complex environments. We suggest that frogs were attracted to riverbanks by the humidity and availability of reproductive sites, opportunistically ingesting prey available in the habitat. The abundance of social insects allowed the presence of frogs specialized in ants, such as the bufonid Rhinella ocellata and the dendrobatid Ameerega berohoka.

Defining corridors for movement of multiple species in a forest-plantation landscape

Forestry plantations of Pinus radiata, managed through clearcutting method, would offer resistance to the movement of native fauna among remnants of native forest. In this study, we evaluate the possibilities of establishing connectivity corridors for native fauna in a forest landscape dominated by P. radiata, focusing on seven species with some level of specialisation in the use of different land covers and that exhibit different movement strategies. We sampled presences and abundances using several types of sampling to determine the abundance and crossing edge probabilities for the ground-dwelling beetle Ceroglossus chilensis; the mesocarnivores Conepatus chinga, Lycalopex culpaeus and Leopardus guigna; the terrestrial frogs Eupsophus septentrionalis and Pleuroderma thaul, and the understory bird Pteroptochos castaneus. We use species distribution modelling and circuit theory to calculate connectivity for each species. Finally, a spatial priorization approach was applied to obtain two scenarios of least-cost corridors. The results show that species with more specific requirements such as L. guigna, P. castaneus, P. thaul and E. septentrionalis, are unlikely to move through clear cuttings and young plantations, but their movement is possible through adult pine plantations with understory. For species that are habitat generalists such as C. chinga and L. culpaeus plantations were suitable for movement. The management of forest plantations should use multi-taxa assessments in the design of biological corridors that allow the connection of forest fragments.

Synergistic effects of warming and disease linked to high mortality in cool-adapted terrestrial frogs

Cool-adapted species inhabiting montane tropical forests are vulnerable to heat stress associated with climate warming. According to the thermal mismatch hypothesis, pathogens are predicted to have broader thermal tolerances than their hosts, which can lead to increased pathogen loads and host mortality when temperatures are outside hosts' thermal optima. We tested the thermal mismatch hypothesis in two habitat generalist species expected to have wide thermal tolerance ranges: Dendropsophus minutus captured at a high elevation and D. elegans captured at a warmer low elevation. We also tested high-elevation individuals of the Brazilian direct-developing species Ischnocnema parva, which are expected to have a narrow thermal tolerance range based on life history. We exposed all frogs to the pathogenic fungus Batrachochytrium dendrobatidis (Bd) under three temperatures ranging from the average nighttime temperature where frogs were collected (16 and 21 °C for high and low elevations, respectively) to a simulated warming event (26 °C). Bd loads across all three host species were negatively associated with temperature. However, the interaction between Bd infection and warming led to increased mortality in cool-adapted I. parva at higher temperatures, despite lower infection loads. Our results indicate that Bd may lead to declines of cool-adapted montane frogs under the combined pressures of pathogen infection and warming, even at temperatures approaching the pathogen's upper thermal limit. Thus, climatic warming at a level that lowers fitness of heat-sensitive pathogens may not uniformly reduce host disease risk.

Two New Frog Species of the Genus <i>Copiula</i> Mehely, 1901 (Anura, Microhylidae, Asterophryinae) from Southern Papua New Guinea

We describe two new species in the microhylid frog genus Copiula from Western Province, Southern Highlands Province, and Gulf Province in southern Papua New Guinea based on morphological and acoustic data. Both species are medium-sized (between 27 – 30 mm SVL), terrestrial frogs with a predominantly beige-colored dorsum and a yellow ventrum. They can be distinguished from each other and from all congeners by their distinct advertisement calls. In the first species calls are short bursts of 3 – 7 rapidly repeated yapping notes lasting 30 – 44 msec at a repetition rate of 11.6 – 16.5 notes/sec, and in the second species calls consist almost exclusively of two notes (occasionally one or three notes) lasting 50 – 91 msec and produced at a repetition rate of 7.1 – 11.3 notes/sec. Calls of the second species are usually uttered in long call series that may start with one or more, one-note calls before increasing to two notes, and occasionally to three notes/call late in the series. Descriptions of these two species brings the number of Copiula known from the New Guinea region to at least 12.

Earth Stewardship Science—Transdisciplinary Contributions to Quantifying Natural and Cultural Heritage of Southernmost Africa

Evaluating anthropogenic changes to natural systems demand greater quantification through innovative transdisciplinary research focused on adaptation and mitigation across a wide range of thematic sciences. Southernmost Africa is a unique field laboratory to conduct such research linked to earth stewardship, with ‘earth’ as in our Commons. One main focus of the AEON’s Earth Stewardship Science Research Institute (ESSRI) is to quantify the region’s natural and cultural heritage at various scales across land and its flanking oceans, as well as its time-scales ranging from the early Phanerozoic (some 540 million years) to the evolution of the Anthropocene (changes) following the emergence of the first human-culture on the planet some 200 thousand years ago. Here we illustrate the value of this linked research through a number of examples, including: (i) geological field mapping with the aid of drone, satellite and geophysical methods, and geochemical fingerprinting; (ii) regional ground and surface water interaction studies; (iii) monitoring soil erosion, mine tailing dam stability and farming practices linked to food security and development; (iv) ecosystem services through specific biodiversity changes based on spatial logging of marine (oysters and whales) and terrestrial (termites, frogs and monkeys) animals. We find that the history of this margin is highly episodic and complex by, for example, the successful application of ambient noise and groundwater monitoring to assess human-impacted ecosystems. This is also being explored with local Khoisan representatives and rural communities through Citizen Science. Our goal is to publicly share and disseminate the scientific and cultural data, through initiatives like the Africa Alive Corridor 10: ‘Homo Sapiens’ that embraces storytelling along the entire southern coast. It is envisioned that this approach will begin to develop the requisite integrated technological and societal practices that can contribute toward the needs of an ever-evolving and changing global ‘village’.

Una fantástica nueva especie del grupo Pristimantis orcesi de los Andes sur de Ecuador

ABSTRACT We describe a new glandular terrestrial frog of the Pristimantis (Anura: Craugastoridae) genus. The new species inhabits the high montane forests of the Cañar province in southern Ecuador. It differs from other terrestrial frogs by having a striking dark gray and red dorsal coloration, dorsal skin with a corrugated texture, a small tubercle on the eyelid and heel, absence of vomerine odontophores, and large glandular patches on the supratympanic area, arms and limbs. Our molecular analyses show that the new species is in a clade with P. orcesi and P. erythros. Based on our results, we redefine the orcesi group and suggest that it contains only three species (P. orcesi, P. erythros, and the new species); the group is diagnosed mainly by exhibiting conspicuous dermal macroglands on the head, body and legs.

Climbing behavior of Rhinella icterica (Spix, 1824) (Anura, Bufonidae): A typically terrestrial toad being scansorial

Toads of the Family Bufonidae do present diversified life histories, most of them are terrestrial, but there are aquatic and arboreal species. Rhinella icterica (Spix, 1824) (Anura, Bufonidae) is a ground dweller bufonid that use the habitat mainly horizontally. Here, we report the occurrence of climbing behavior in R. icterica, adding knowledge with respect to its types of locomotion. The individual was found on the ground and when perceived the presence of the observer it jumped to a wall, hit it, fell back to the ground, and then started to climb the wall. The toad climbed slowly, but apparently without difficulty, since it went up without slipping until the top of the ravine. Performing a given locomotor behavior even rarely confer additional ability to evade from threats and to access otherwise inaccessible food and spatial resources. Whether this behavior is common or rare in the genus is still obscure, nevertheless, at least some typically terrestrial species of Rhinella are capable of climbing and, as R. icterica, use the habitat vertically.

Anthropogenic substrate-borne vibrations impact anuran calling

Anthropogenic disturbance is a major cause of the biodiversity crisis. Nevertheless, the role of anthropogenic substrate vibrations in disrupting animal behavior is poorly understood. Amphibians comprise the terrestrial vertebrates most sensitive to vibrations, and since communication is crucial to their survival and reproduction, they are a suitable model for investigating this timely subject. Playback tests were used to assess the effects of substrate vibrations produced by two sources of anthropogenic activity– road traffic and wind turbines– on the calling activity of a naïve population of terrestrial toads. In their natural habitat, a buried tactile sound transducer was used to emit simulated traffic and wind turbine vibrations, and changes in the toads’ acoustic responses were analyzed by measuring parameters important for reproductive success: call rate, call duration and dominant frequency. Our results showed a significant call rate reduction by males of Alytes obstetricans in response to both seismic sources, whereas other parameters remained stable. Since females of several species prefer males with higher call rates, our results suggest that anthropogenically derived substrate-borne vibrations could reduce individual reproductive success. Our study demonstrates a clear negative effect of anthropogenic vibrations on anuran communication, and the urgent need for further investigation in this area.

The Mating Call of the Terrestrial Toad, Rhinella arenarum, as a Cue for Spatial Orientation and Its Associated Brain Activity

Acoustic communication is essential for reproduction and predator avoidance in many anuran species. For example, mating calls are generally produced by males and represent a conspicuous communication signal employed during the breeding season. Although anuran mating calls have been largely studied to analyze content and phonotaxis toward choruses, they are rarely discussed as sources of information guiding spatial behavior in broader contexts. This is striking if we consider that previous studies have shown anurans to be impressive navigators. In the current study, we investigated whether terrestrial toad (Rhinella arenarum) males can use a mating call as a spatial cue to locate a water reward in a laboratory maze. Male toads could indeed learn the location of a reward guided by a mating call. This navigational ability, as indicated by c-Fos, was associated with greater neuronal activity in the telencephalic hippocampal formation (HF; also referred to in amphibians as medial pallium), the medial septum (MS), and the central amygdala (CeA). HF and MS are telencephalic structures associated with spatial navigation in mammals and other vertebrates. The CeA, by contrast, has been studied in the context of acoustic processing and communication in other amphibian species. The results are discussed in the framework of an evolutionary conserved, HF-septal spatial-cognitive network shared by amphibians and mammals.

Geographic body size variation of a tropical anuran: effects of water deficit and precipitation seasonality on Asian common toad from southern Asia

BackgroundTwo previous studies on interspecific body size variation of anurans found that the key drivers of variation are the species’ lifestyles and the environments that they live in. To examine whether those findings apply at the intraspecific level, we conducted a study of the Asian common toad (Duttaphrynus melanostictus), a terrestrial anuran distributed in tropical regions. The body size of toads from 15 locations, covering the majority of their geographic range, and local environmental data were summarized from published literature. We used a model selection process based on an information-theoretic approach to examine the relationship between toad body size and those environmental parameters.ResultsWe found a positive correlation between the body size of the Asian common toad and the water deficit gradient, but no linkage between body size and temperature-related parameters. Furthermore, there was a positive correlation between the seasonality of precipitation and body size of females from different sampled populations.ConclusionsAs a terrestrial anuran, the Asian common toad should experience greater pressure from environmental fluctuations than aquatic species. It is mainly distributed in tropical regions where temperatures are generally warm and stable, but water availability fluctuates. Therefore, while thermal gradients are not strong enough to generate selection pressure on body size, the moisture gradient is strong enough to select for larger size in both males and females in dryer regions. Larger body size supports more efficient water conservation, a pattern in accordance with the prediction that lifestyles of different species and their local habitats determine the relationship between body size and environment. In addition, larger females occur in regions with greater seasonality in precipitation, which may happen because larger females can afford greater reproductive output in a limited reproductive season.

Novel method for detection probability and estimating population size of mountain frog, Rana macrocnemis (Boulenger, 1885) at the end of its distribution range

Local amphibian populations at the edge of a species range are possibly of greater conservation concern than any other amphibians group. They experience greater demographic fluctuation than populations at the core of the range. We detected the most suitable distribution range of R. macrocnemis by maximum entropy (MaxEnt) method at the end of the southeastern edge of natural distribution range to find out which environmental variables have a significant role in determining the distribution pattern of this species in marginal populations. According to the map constructed, three important variables had a high contribution to species presence as land cover (63.4%), annual precipitation (27%), and precipitation of coldest quarter of the year (5.4%) variables. Then, we described new methods for estimating detection probability for terrestrial frogs, specifically R. macrocnemis. Finally, we estimated the population size of mountain frogs by calculated detection probability. Our repeated capture–re-capture (RCR) results suggest that the estimated detection probability for R. macrocnemis is: $$\widehat{p} = 0.052$$. Thus, the total average number of R. macrocnemis obtained from the 17 habitat sites is 982.5 adults (range: 708–1211 adults). In conclusion, the population estimates by detection probability index are generally much higher than densities reported for the Mountain frog populations than visual encounter estimation about 50.5 adults (range: 37–63 adults).

On the transfer of spatial learning between geometrically different shaped environments in the terrestrial toad, Rhinella arenarum.

When trained in a rectangular arena, some research has suggested that rats are guided by local features rather than overall boundary geometry. We explored this hypothesis using the terrestrial toad, Rhinella arenarum, as a comparative contrast. In two experiments, toads were trained to find a water-reward goal location in either a featureless rectangular arena (Experiment 1) or in a rectangular arena with a removable colored feature panel covering one short wall (Experiment 2). After learning to successfully locate the water reward, probe trials were carried out by changing the shape of the arena into a kite form with two 90°-angled corners, and in the case of Experiment 2, also shifting the location of the color panel. The results of Experiment 1 indicated that the toads, in contrast to rats, relied primarily on overall shape or boundary geometry to encode the location of a goal. Under the probe conditions of the altered environmental geometry in Experiment 2, the toads seemed to preferentially choose a corner that was generally correct relative to the feature panel experienced during training. Together, the data of the current study suggest that toads and rats differ in the strategies they employ to represent spatial information available in a rectangular arena. Further, the results support the hypothesis that amphibians and mammals engage different neural mechanisms, perhaps related to different evolutionary selective pressures, for the representation of environmental geometry used for navigation.

Pristimantis tinguichaca Brito, Ojala-Barbour, Batallas & Almendariz, 2016 (Anura, Strabomantidae): range extension and notes on variation in color pattern

In this paper we extend the known distribution of the endemic and recently described Pristimantis tinguichaca Brito et al. 2016, a terrestrial robber frog characterized by its beige and brown to dark-brown dorsal coloration, flanks with longitudinal or diagonal cream-coloured bands which are separated by brown, and reddish iris. The new records, based on two specimens collected from the Cerro Candelaria and Cerro Mayordomo reserves of Fundación Ecominga in the upper Pastaza River watershed, Tungurahua province, east-central Ecuador, represent the northern limit of the species and extend this species to the Llanganates–Sangay ecological corridor.

Feeding Ecology of a Tropical Litter-Dwelling Frog, Chaperina fusca (Microhylidae) from Borneo

We analyzed the diet of a litter-dwelling microhylid frog, Chaperina fusca, from the lowland rainforest of Borneo. We flushed the stomachs of 194 frogs: 94.8% had contents and 5.2% were empty. Although the diet composition of C. fusca was diverse, with 27 prey categories, we found that ants, mites, beetles, and springtails, in that order, dominated its diet both numerically and volumetrically. Among these four categories, however, ants were by far the most frequently consumed in both number (63.5%) and volume (82.6%) and in higher proportion than in the leaf litter. A novel aspect of our study, conducted in only a limited number of studies of anuran diets, was to determine the ant genera consumed. We identified 41 ant genera consumed by C. fusca whereby the genera Lophomyrmex, Pheidole, and Tetramorium were the most prominent. We also recorded a significant relationship of prey volume and number with both body size and mouth width of frogs. Our data provide circumstantial evidence that C. fusca is an ant-specialist feeder and active forager. These results are in line with the dietary characteristics of many terrestrial microhylid frogs in subtropical and tropical Asia, the Neotropics, and the Afrotropics.

A new species of terrestrial frog of the genus Noblella Barbour, 1930 (Amphibia: Strabomantidae) from the Llanganates-Sangay Ecological Corridor, Tungurahua, Ecuador.

We describe a new species of terrestrial frog of the genus Noblella from the eastern versants of the Ecuadorian Andes in the upper Pastaza watershed. Noblella naturetrekii sp. n. differs from its Ecuadorian congeners by the presence of a differentiated tympanic membrane and a weakly defined tympanic annulus, and eyelids with rounded tubercles. In addition, the new species is characterized by its blackish–dark brown ventral coloration scattered with little white dots and the absence of papillae at the tip of the fingers and toes. We provide a detailed description of the call and osteology of the new species. Finally, we present the most complete phylogeny of the genus, which confirms that Noblella is a non-monophyletic group.

Digital dissection of the pelvis and hindlimb of the red-legged running frog,Phlyctimantis maculatus, using Diffusible Iodine Contrast Enhanced computed microtomography (DICEμCT)

BackgroundThe current study applies both traditional and Diffusible Iodine Contrast Enhanced computed microtomography (DICE µCT) techniques to reveal the musculoskeletal anatomy of Phlyctimantis maculatus. DICE µCT has emerged as a powerful tool to visualise intricate musculoskeletal anatomy. By generating 3D digital models, anatomical analyses can be conducted non-destructively, preserving the in situ 3D topography of the system, therefore eliminating some of the drawbacks associated with traditional methods. We aim to describe the musculature of the spine, pelvis, and hindlimb, compare the musculoskeletal anatomy and pelvic morphology of P. maculatus with functionally diverse frogs, and produce 3D digital anatomy reference data.MethodAn adult frog was stained using an aqueous Lugol’s solution and scanned in a SkyScan1176 in vivo µCT scanner. Scan images were reconstructed, resampled, and digitally segmented to produce a 3D model. A further adult female frog was dissected traditionally for visualisation of tendinous insertions.ResultsOur work revealed three main findings: (1) P. maculatus has similar gross muscular anatomy to Rana catesbeiana (bullfrog) but is distinct from those species that exhibit ancestral traits (leopelmids) and those that are highly specialised (pipids), (2) P. maculatus’s pelvic anatomy best fits the description of Emerson’s walking/hopping pelvic morphotype IIA, and (3) a split in the semimembranosus and gracilis major muscles is consistent with the reported myology in other anuran species.DiscussionWhile DICE µCT methods were instrumental in characterising the 3D anatomy, traditional dissection was still required to visualise important structures such as the knee aponeurosis, tendinous insertions, and fasciae. Nonetheless, the anatomical data presented here marks the first detailed digital description of an arboreal and terrestrial frog. Further, our digital model presents P. maculatus as a good frog model system and as such has formed a crucial platform for further functional analysis within the anuran pelvis and hindlimb.

Composition of Terrestrial Anurans in Areas with Different Degrees of Alteration in San Rafael National Park (Paraguay)

We examined the effects of landscape changes in an environmental gradient of forest, a Vernicia fordii plantation, and crops on the distribution patterns of amphibians in San Rafael National Park. We conducted eight periods of fieldwork between June 2012–April 2013 and used pit fall traps with drift fences to capture amphibians. We recorded eight species of the families Bufonidae, Leptodactylidae, and Odontophrynidae. The environmental variables correlated with the abundance of amphibians were relative humidity, litter depth, herbaceous cover, and air temperature, and significant differences were found in species composition. Generalist species like Leptodactylus mystacinus and Physalaemus cuvieri were found in the most altered areas such as crops and the plantation. Rhinella ornata and Proceratophrys avelinoi were primarily restricted to primary forests, and their abundance was sensitive to forest lost and degradation. Our results support the idea that modified habitats influence distribution patterns of amphibians, and the protection of the remnants of pristine Atlantic Forest is a critical step in the conservation of anuran biodiversity in Paraguay.

Integrating the role of antifungal bacteria into skin symbiotic communities of three Neotropical frog species.

Chytridiomycosis, caused by the pathogen Batrachochytrium dendrobatidis (Bd), has led to population declines and extinctions of frog species around the world. While it is known that symbiotic skin bacteria can play a protective role against pathogens, it is not known how these defensive bacteria are integrated into the bacterial community on amphibian skin. In this study, we used 16S rRNA gene amplicon sequencing, culturing and Bd inhibition bioassays to characterize the communities of skin bacteria on three Neotropical frog species that persist in a Bd-infected area in Panama and determined the abundance and integration of anti-Bd bacteria into the community. We found that the two treefrog species had a similar bacterial community structure, which differed from the more diverse community found on the terrestrial frog. Co-occurrence networks also revealed differences between frog species such that the treefrogs had a significantly higher number of culturable Bd-inhibitory OTUs with high centrality scores compared with the terrestrial frog. We found that culture-dependent OTUs captured between 21 and 39% of the total relative abundance revealed in culture-independent communities. Our results suggest different ecological strategies occurring within skin antifungal communities on host species that have not succumbed to Bd infections in the wild.

The influence of land cover and within-pool characteristics on larval, froglet, and adult wood frogs along a rural to suburban gradient

Urbanization is known to extirpate many species, but far less is known about how suburbanization may affect amphibian populations. We studied wood frogs (Lithobates sylvaticus) to test the effects of site characteristics (within-pool conditions and land cover indicative of suburbanization within 1000 m) and larval morphology on newly emerged froglets and post-breeding males across a suburbanization gradient in 15 pools in greater Bangor, Maine, USA. We raised field-captured larvae in microcosms and examined froglet morphology and locomotor performance at emergence and one month post-emergence. Larval mass was positively correlated with 50% of froglet responses (survival, size, and locomotor performance) but was negatively associated with adult size. Among site characteristics, egg density had the most salient influence with negative effects on larval survival and morphology as well as on 11 of 14 froglet responses. Vegetation, hydrology, and suburban-associated cover near pools also influenced froglet performance, and hydrology and suburban-associated cover was associated with larger and smaller adult morphology. However the influence of suburban-associated cover on froglet performance and adult morphology was small compared to that of within-pool characteristics. Specifically, our findings support the idea that within-pool conditions experienced by larvae can influence terrestrial stages with potentially life-long consequences. Nevertheless, in suburban landscapes where there is evidence of population declines, it is likely that suburbanization has the greatest impact on populations via direct effects on terrestrial stages. We encourage planners to maintain high-quality habitat for aquatic and terrestrial stage wood frogs in suburbanizing landscapes to avoid extirpation.

Effects of skin region and relative lipophilicity on percutaneous absorption in the toad Rhinella marina.

Owing to the dynamic interaction between frog skin and the environment, xenobiotics in frog habitats are of particular concern, and knowledge of percutaneous absorption in frog skin is necessary for risk-mitigation purposes. Baseline transdermal kinetics in adult aquatic and arboreal frog species have recently been reported; however, there is little information regarding absorption kinetics in adult terrestrial species. The present study investigated the in vitro absorption kinetics of 3 model chemicals-caffeine, benzoic acid, and ibuprofen-through different skin regions in the terrestrial toad Rhinella marina. Caffeine flux was consistently higher than that of the other 2 chemicals (p < 0.001), whereas the fluxes of the moderately and highly lipophilic chemicals (benzoic acid and ibuprofen) were similar, regardless of skin region. When considering individual chemicals, caffeine demonstrated increased flux through the ventral pelvic skin compared with the ventral thoracic or dorsal skin regions. Flux did not differ between skin regions for either benzoic acid or ibuprofen. These findings have implications for management of environmental contamination in frog habitats, as many environmental xenobiotics are of moderate to high lipophilicity and would be expected to be equally absorbed from all skin surfaces in terrestrial toads. Environ Toxicol Chem 2019;38:361-367. © 2018 SETAC.