Native Frogs Research Articles

Characterization of the microbiome of the invasive Asian toad in Madagascar across the expansion range and comparison with a native co-occurring species

Biological invasions are on the rise, with each invader carrying a plethora of associated microbes. These microbes play important, yet poorly understood, ecological roles that can include assisting the hosts in colonization and adaptation processes or as possible pathogens. Understanding how these communities differ in an invasion scenario may help to understand the host’s resilience and adaptability. The Asian common toad, Duttaphrynus melanostictus is an invasive amphibian, which has recently established in Madagascar and is expected to pose numerous threats to the native ecosystems. We characterized the skin and gut bacterial communities of D. melanostictus in Toamasina (Eastern Madagascar), and compared them to those of a co-occurring native frog species, Ptychadena mascareniensis, at three sites where the toad arrived in different years. Microbial composition did not vary among sites, showing that D. melanostictus keeps a stable community across its expansion but significant differences were observed between these two amphibians. Moreover, D. melanostictus had richer and more diverse communities and also harboured a high percentage of total unique taxa (skin: 80%; gut: 52%). These differences may reflect the combination of multiple host-associated factors including microhabitat selection, skin features and dietary preferences.

Diet of a community of frogs in an agroecosystem in western Cuba

The study of frog diets in agricultural areas enables us to recognize their role in terrestrial food webs as predators of invertebrates, which can become crop pests or disease transmission vectors for humans. The present study examines the diet composition of three syntopic frog species occurring in one agroecosystem in Cuba, and their interspecific trophic interactions. The fieldwork was in Zea mays and Colocasia esculenta crops in Pinar del Río province, Cuba, in August, 2020. The frogs were measured and stomach-flushed in situ, and released at the site of capture. Niche overlap between species was calculated. Fifty-two frogs were captured and 43 (82.7%) had prey in their stomachs. Eleutherodactylus goini had the highest rate of prey/stomach and the broadest diet diversity while Osteopilus septentrionalis had the lowest rate and the narrowest diet diversity. High diet overlap was detected between Eleutherodactylus species. The most consumed prey were Lepidoptera, Hymenoptera, and Blattodea. The diet data suggests that these species could be important biological controls of the invertebrate community in the studied agroecosystems. This indicates a positive impact of these native frogs to the crops by controlling noxious and damaging invertebrates.

Invasive Cuban Treefrogs (Osteopilus septentrionalis) Have More Robust Locomotor Performance Than Two Native Treefrogs (Hyla spp.) in Florida, USA, in Response to Temperature and Parasitic Infections

Introduced species pose a threat to biodiversity, and ecological and physiological factors are important in determining whether an introduced species becomes successfully established in a new region. Locomotor performance is one such factor that can influence the abundance and distribution of an introduced species. We investigated the effects of temperature and parasitism by the intestinal nematode Aplectana hamatospicula on the maximum jump distance and endurance in one invasive and two native treefrogs in Florida, USA. We collected frogs from the wild, estimated their parasite loads, and tested their locomotor performance at three temperatures. Contrary to expectations, invasive Cuban treefrogs (Osteopilus septentrionalis), which are adapted to a warmer climate in the Caribbean, outperformed pinewoods treefrogs (Hyla femoralis) and squirrel treefrogs (H. squirella) at each temperature, even when controlling for body size differences. In all three species, maximum jump distance was positively related to temperature, and this relationship was stronger for larger frogs. Parasites influenced both the maximum jump distance and endurance of frogs. In all three species, larger frogs jumped farther maximum distances than smaller frogs, but this relationship was stronger when frogs had lower, rather than higher, parasite loads. Parasitism had little effect on endurance in invasive frogs, but it tended to decrease the endurance of native frogs at high temperatures. Furthermore, at low temperatures, the lengths of consecutive jumps of infected native frogs tended to increase, suggesting that parasites limited the distances of initial jumps. Effects of temperature and parasites on the locomotor performance of frogs could influence their abilities to forage, escape predators, and disperse. The tremendous locomotor performance of O. septentrionalis, which is maintained across temperatures and parasite loads, likely contributes to the invasion success of this species.

When introduced prey violates trophic hierarchy: Conservation of an endangered predator

Introduced species often disrupt established food webs, but some native predators can come to rely on introduced prey. Understanding the net effects of the non-natives on imperiled predators is crucial for planning conservation measures. The invasive American bullfrog (Lithobates catesbeianus) can be prey, predator, and competitor for the critically endangered San Francisco garter snake (Thamnophis sirtalis tetrataenia). We examined the seasonal prey use of a San Francisco garter snake population that co-occurs with American bullfrogs to examine intraguild predation between these species. Juvenile and adult snakes mainly consumed native anurans instead of American bullfrogs, and this diet pattern peaked in spring, a critical foraging period for the snakes. In spring, large adult American bullfrogs also foraged heavily on native anurans and displayed a high degree of diet overlap with San Francisco garter snakes. Invasive American bullfrogs are detrimental to San Francisco garter snakes mainly through seasonal competition rather than reciprocal predation. Removal of invasive species provided further evidence that eliminating American bullfrogs can benefit San Francisco garter snakes by reducing predation pressure on their shared amphibian prey. Better understanding the interactions of invasive species with native species of conservation concern informs management practices and improves conservation outcomes.

The Japanese Common Toad, Bufo japonicus formosus, Contains Toxin in the Egg Stage

Abstract: Bufonid toads generally possess cardiotoxic steroids called bufadienolides as defensive chemicals. Although knowledge of the life stages at which the toad species possess the poison is important for our understanding of diversity of toxicity among bufonid toads, this knowledge is limited. In the present study, we revealed that the Japanese common toad, Bufo japonicus formosus, possesses toxins at the unfertilized egg stage by conducting a bioassay experiment. Recent studies documented that hatchlings of B. j. formosus have lethal toxic effects on native frog tadpoles (Rana pirica) in the invasive area of the toad (Hokkaido). In our bioassay experiment using R. pirica tadpole as a predator, no tadpoles died when they did not consume any prey item during two-days experimental period. However, approximately 90% of R. pirica tadpoles immediately died when they consumed an unfertilized egg of B. j. formosus. These results suggest that the toxin at the early life stages of B. j. formosus is, at least partly, provided from female parent.

Rapid responses in morphology and performance of native frogs induced by predation pressure from invasive mongooses

Invasive predators often decrease the abundance and distribution of native prey, but only a few studies have reported rapid predator-induced morphological and performance changes. An effective prey performance response may actually depend whether the predator uses a sit-and-wait or an active foraging strategy; the former would require prey to obtain the ability to move quickly in bursts, while the latter would require prey to increase their endurance to survive. The performance of native prey should therefore change according to the predation type of an invasive predator when it differs from that of native predators. As such, it is critical to evaluate prey performance to understand the effects of different predation types. We examined rapid morphological (hind limb length) and performance (burst movement ability, endurance) changes in a native prey frog induced by an invasive predator mongoose on Amami Island, Japan, where the only native predators of the frog are snakes. The hind limb length of the frog increased under the strong predation effect of the mongoose, which may have acted as a selective agent to induce rapid morphological responses. The endurance, but not the burst movement ability, of the frog was higher under the strong effect of predation by the mongoose. This suggests that endurance was a specific target of natural selection and that the performance of the native prey changed in response to the new predation type. Examining not only morphological but also performance changes will allow us to understand in detail the impact of invasive predators.

Correction to: The enemy within: consequences of the invasive bullfrog on native anuran populations

In the original publication of the article, the last name of the first author was published incorrectly and the correct name is given in this correction.

The enemy within: consequences of the invasive bullfrog on native anuran populations

The bullfrog, Lithobates catesbeianus, is one of the most important invasive anurans, affecting especially native anurans due to their similar habits. Here we used a hierarchical co-occurrence model fit in a Bayesian framework to investigate the effects of the bullfrog on two native frog species from southern Brazil, testing the hypothesis that bullfrog presence changes the activity of native species and their relationship with habitat. We found that both occupancy and detection probabilities of native species were similar with bullfrog presence or absence at a site. However, we observed changes in activity and microhabitat use preferences of both native species when the bullfrog was present, suggesting that the presence of the invasive species altered the behavior of the native species. Changes induced by invasive species can result in severe long-term consequences for native species since niche differentiation may not mediate the ability of species to persist together indefinitely.

Tissues injury and pathological changes in Hyla intermedia juveniles after chronic larval exposure to tebuconazole

Tebuconazole (TBZ), an azole pesticide, is one of the most frequently detected fungicides in surface water. Despite its harmful effects, mainly related to endocrine disturbance, the consequences of TBZ exposure in amphibians remain poorly understood. Here, we investigated the adverse and delayed effects of TBZ chronic exposure on a native anuran species, often inhabiting cultivated areas, the Italian tree frog (Hyla intermedia). To disclose the multiple mechanisms of action through which TBZ exerts its toxicity we exposed tadpoles over the whole larval period to two sublethal TBZ concentrations (5 and 50 μg/L), and we evaluated histological alterations in three target organs highly susceptible to xenobiotics: liver, kidney, and gonads. We also assessed morphometric and gravimetric parameters: snout-vent length (SVL), body mass (BM), liver somatic index (LSI), and gonad-mesonephros complex index (GMCI) and determined sex ratio, gonadal development, and differentiation. Our results show that TBZ induces irreversible effects on multiple target organs in H. intermedia, exerting its harmful effects through several pathological pathways, including a massive inflammatory response. Moreover, TBZ markedly affects sexual differentiation also by inducing the appearance of sexually undetermined individuals and a general delay of germ cell maturation. Given the paucity of data on the effects of TBZ in amphibians, our results will contribute to a better understanding of the environmental risk posed by this fungicide to the most endangered group of vertebrates.

Giant Gartersnakes (Thamnophis gigas) Exploit Abundant Nonnative Prey While Maintaining Their Appetite for Native Anurans

The introductions of nonnative species can cause great change in the trophic dynamics of native species. Giant Gartersnakes, endemic predators in the Central Valley of California, are listed as threatened because of the conversion of their once vast wetland habitat to agriculture. Further contributing to this snake's changing ecology is the introduction of many nonnative prey species, resulting in a diet that is almost completely composed of nonnative species. In order to determine whether these snakes actively select their prey or simply consume what is abundant, we examined prey selection by adult Giant Gartersnakes in the context of what prey was available to each individual. Giant Gartersnakes selected a native anuran over nonnative anuran and fish species despite these nonnatives dominating the available species composition. These results contribute to understanding the mechanisms underlying Giant Gartersnake diets in the contemporary landscape and can lead to improved management of prey communities for Giant Gartersnakes and other native predators.

Apparent lack of spill-over of parasites from an invasive anuran: PCR detects Entamoeba in cane toads (Rhinella marina) but not in sympatric Australian native frogs.

The recent detection of a novel amoebozoan parasite (Entamoeba sp. CT1) killing invasive cane toads (Rhinella marina) in tropical Australia raises concerns of potential spill-over into native anuran populations. Considering the vulnerability of anuran communities globally, Entamoeba sp. CT1 may pose a serious threat to anuran biodiversity. Through PCR-based detection and molecular identification, we investigated the prevalence of Entamoeba spp. in the faeces and colon tissue of cane toads (Rhinella marina) and eleven native Australian frog species from a single locality in the Northern Territory. No Entamoeba DNA was detected in samples of native frog faeces (N = 57) or colons (N = 17). Entamoeba DNA was detected in 24% of 45 cane toads (95%CI 14.08–38.82). Both E. ranarum and Entamoeba sp. CT1 were present in cane toads. The failure of faecal samples to indicate Entamoeba spp. in infected cane toads may be due to cysts in faeces being shed intermittently, degraded before analysis, or impervious to lysis prior to DNA isolation. Our results suggest that native frogs do not carry the pathogen in an area where 20–30% of cane toads are infected with Entamoeba sp. CT1. We demonstrate the importance of recognising PCR inhibition prior to molecular diagnostics, and the apparent inadequacy of faecal samples for the detection of Entamoeba spp. in anurans.

Monitoring of the last stronghold of native pool frogs (Pelophylax lessonae) in Western Europe, with implications for their conservation

The original diversity of Pelophylax water frogs has been compromised by multiple biological invasions all over Western Europe. For the European pool frog (P. lessonae), the Joux Valley—a 30 km highland depression in northwestern Switzerland—stands as the last stronghold spared by exotic lineages. In order to manage P. lessonae in the valley, we combined traditional field surveys with environmental DNA metabarcoding and mapped the regional distribution of amphibian species. Both approaches concurred that P. lessonae persists at a single isolated site (Pontet). Continuous monitoring of this population throughout the spring and summer 2019 informed on their wintering quarters (most likely the forest litter immediately surrounding the breeding pond), as well as the timing of migration (end of April), breeding (June), and larval development (June–August). In parallel, we experimented the first use of drone technology for amphibian surveillance: 30 adults were individually counted during an aerial survey at the peak of the breeding season, confirming the small size of the population. Finally, we compared some biotic and abiotic properties among water bodies throughout the valley and flagged a few sites that were ecologically similar to Pontet. In a landscape dominated by pastoral activities where Pelophylax dispersal is virtually impossible, these could be candidates for future translocation efforts. Our study illustrates the application of next-generation monitoring techniques for the urgent management of threatened species and stresses the need for reevaluating the conservation status of P. lessonae in Western Europe, where it appears to subsist in low numbers at one last locality.

Morphological Change during Rapid Population Expansion Confounds Leopard Frog Identifications in the Southwestern United States

Lowland Leopard Frogs (Rana yavapaiensis) have experienced extensive population declines over the last century. In California, this species was historically known to occur in scattered localities in the extreme southeastern portion of the state, but it has not been positively documented since 1965. Subsequent to this decline in California, nonnative Rio Grande Leopard Frogs (R. berlandieri) have expanded into localities previously occupied by R. yavapaiensis. The lack of extensive formal surveys and the difficulty distinguishing between these species using morphological characters have caused uncertainty about whether Lowland Leopard Frogs persist within their historical range in California. Recently, leopard frogs that could not be confidently identified to species have been observed at historical localities of R. yavapaiensis . Thus, we undertook a formal study of these populations to characterize their morphological and genetic variation, and conclusively determine to which species they belong. Our genetic analyses demonstrate that these frogs are R. berlandieri, but the morphological characters typically used to diagnose these species are largely overlapping. Further complicating field identifications, for some morphological characters, the California R. berlandieri are more similar to R. yavapaiensis than to native-range R. berlandieri. Additionally, invasive R. berlandieri show greater variation in a key character—the condition of the inset dorsolateral folds—than that found across much of the species' native range. These results demonstrate the potential for morphological change during rapid population expansions to confound species identifications. Our findings have implications for future efforts to resolve the status of R. yavapaiensis in California and to identify other native leopard frogs found within the expanding range of R. berlandieri. Our results also highlight the utility of genetic approaches for reliably identifying morphologically similar leopard frogs.

Elucidating mechanisms of invasion success: effects of parasite removal on growth and survival rates of invasive and native frogs.

Identifying the mechanisms underlying biological invasions can inform the management of invasive species. The enemy release hypothesis (ERH) suggests that invasive species have a competitive advantage in their introduced range because they leave behind many of their predators and parasites from their native range, allowing them to shift resources from defenses to growth, reproduction, and dispersal. Many studies have demonstrated that invasive species have fewer parasites than their native counterparts, but few studies have tested whether the loss of these natural enemies appears to be a primary driver of the invasion process.To test the ERH, we conducted a mark-recapture study in which we used an anthelmintic drug to successfully reduce parasitic worms in invasive Cuban treefrogs (Osteopilus septentrionalis) and native treefrogs (Hyla spp.) at half of 12 wetlands, marking nearly 4,200 frogs. If the ERH is supported, we would expect that treating for parasitic worms would have a greater benefit to native than invasive hosts.Growth and survival rates of invasive and native treefrogs responded similarly to the anthelmintic treatment, suggesting that the Cuban treefrog's release from parasitic worms does not appear to significantly contribute to its invasiveness in established areas. Instead, it appears that the overall faster rates of growth and maturation, higher survival rates, and larger body sizes of Cuban treefrogs that we observed may contribute to their expansion and proliferation.Synthesis and applications. Although Cuban treefrogs have a lower diversity of parasitic worms in their invasive than native range, this does not appear to significantly contribute to their invasion success in areas where they have been established for more than 20 years. This suggests that any manipulation of parasites in invasive or native hosts would not be an effective method of controlling Cuban treefrogs or reducing their impacts. Further research into other hypotheses is needed to explain the Cuban treefrog's success and help guide management actions to reduce their spread and negative impacts. Our study demonstrates that enemy release may not be a primary driver of invasiveness, highlighting the need for more experimental tests of the enemy release hypothesis to examine its generality.

Native and invasive alien anuran species in urbanized areas in Davao City, Philippines, with preliminary study of feeding biology

This article presents the anuran species in urbanized areas, diet overlaps between native and invasive alien anuran species, and its implications on conservation and ecological health in urban environment. Visual encounter technique following the road as a transect was done to determine the diversity of anurans, and stomach content extraction was employed to analyze its diet composition. Results revealed a very low anuran diversity (Shannon-Weiner; 1.165), which is dominated by invasive alien anuran species. Jackknife 1 species richness estimator indicated that 77-100% of the anuran species in the area were already detected which includes three invasive; Rhinella marina (Linnaeus, 1758), Kaloula pulchra Gray, 1831, Hoplobatrachus rugulosus (Wiegmann, 1834), and two natives; Polypedates leucomystax (Gravenhorst, 1829), Limnonectes leytensis (Boettger, 1893). Additionally, assessing the diet of 33 randomly selected anuran samples revealed that Formicidae dominated their food item. Invasive anurans also showed more diverse diet composition compared to native frogs, in which diet overlaps were observed. In conclusion, the study supports the idea that urbanization decreases anuran diversity and supports the dominance of invasive anurans which compete for food with their native and endemic counterparts. Additionally, it is important to manage invasive anurans that dominates urban ecosystem which might affect the native and endemic species in the area and possibly in nearby pristine environment.

Aliens in the backyard: Did the American bullfrog conquer the habitat of native frogs in the semi-deciduous Atlantic Forest?

The American bullfrog Lithobates catesbeianus has a natural distribution in North America, but was spread by human activities in different regions around the world. It is listed as the most invasive amphibian species, affecting terrestrial and aquatic ecosystems and the community of native species. In addition, the American bullfrog is extensively associated with lethal pathogens, with high correlation of the presence of this species with population declines and extinctions. Here we test if this alien species has spread through the landscape, establishing populations at new locations. We used diverse methods including georeferencing of satellite images, ethnobiological interviews and field data to evaluate the dispersion and effects of L. catesbeianus introduction on amphibian composition, species number, and density of individuals in forest fragments in an Atlantic Forest landscape. We did not find any relationship between density of individuals, number of species or composition of the native anuran assemblages in forest fragments in relation to the presence or proximity of American bullfrog introduction points. Additionally, we found that the dispersion potential of this species in the studied landscape is zero, as it was only found in those fragments where it was specifically introduced 15 years ago. The species has not established new populations in the landscape. Although exotic, L. catesbeianus thrives in lentic habitats and has no apparent effect on the structural metrics of the native anuran assemblage. Despite this alien species exhibiting a capacity to adapt and survive at the point of introduction, its potential for propagation is limited probably by the fragmented terrestrial landscape and regional stream network.

Exposure to metals (Ca, K, Mn) and road salt (NaCl) differentially affect development and survival in two model amphibians

ABSTRACTHuman activity has led to widespread chemical alteration of natural environments. Aquatic ecosystems are especially susceptible to chemical changes, including those caused by runoff and invasive species. Here, we examined the effects of water chemistry, specifically sodium chloride as well as three metals (Ca, K, and Mn) known to differ between native and invasive wetland plant species’ leaf tissues, on the development of two model amphibians: the native Northern leopard frog, Lithobates pipiens, and the non-native African clawed frog, Xenopus laevis. We exposed frog eggs to metal treatment solutions and measured time to hatching (TTH), and following hatching, we exposed tadpoles to a lethal concentration of sodium chloride and recorded time to death (TTD). We found that increasing metal concentrations generally resulted in acceleration of TTH for Xenopus tadpoles, but had no effect on leopard frogs. However, increasing metal concentrations (Ca, Mn) increased leopard frog tadpole susceptibility to NaCl (decreased TTD), while increasing metal concentrations (Ca, K) generally resulted in decreased Xenopus tadpole susceptibility to NaCl. Overall, our data suggest that invasive amphibians may be more tolerant to chemical changes than native amphibians, including those driven by the introduction of invasive plant species.

Current approaches to rehoming unwanted, escaped and seized native animal pets in New South Wales and recent trends

Native mammals, birds, reptiles and frogs kept as pets become displaced after they are unwanted, escaped or seized. The Office of Environment and Heritage manages the rehoming of displaced native animal pets, which are regulated under the Biodiversity Conservation Act 2016 in New South Wales. Primarily, animals are balloted to licensed animal keepers and exhibitors. Otherwise, rehoming may be delegated to third party organisations, and pet shops licensed to sell reptiles are obligated to accept back returned reptiles for resale. From 2014 to 2017, at least 1,000 native animal pets were rehomed in New South Wales, the majority of which were reptiles. During this period, there was a significant increase in annual numbers of displaced native animal pets related to a recent increase in displaced reptiles. The majority of cases occurred within the Greater Sydney region. The trends presented in this paper had important implications for a review of the current management framework in light of the increasing volumes. Initial stakeholder consultations have supported the notion of a community education program with an emphasis on responsible pet ownership.

Predation by introduced cats Felis catus on Australian frogs: compilation of species records and estimation of numbers killed

Abstract ContextWe recently estimated the numbers of reptiles, birds and mammals killed by cats (Felis catus) in Australia, with these assessments providing further evidence that cats have significant impacts on Australian wildlife. No previous studies have estimated the numbers of frogs killed by cats in Australia and there is limited comparable information from elsewhere in the world. AimsWe sought to (1) estimate the numbers of frogs killed by cats in Australia and (2) compile a list of Australian frog species known to be killed by cats. MethodsFor feral cats, we estimated the number of frogs killed from information on their frequency of occurrence in 53 cat dietary studies (that examined stomach contents), the mean number of frogs in dietary samples that contained frogs, and the numbers of cats in Australia. We collated comparable information for take of frogs by pet cats, but the information base was far sparser. Key resultsFrogs were far more likely to be reported in studies that sampled cat stomachs than cat scats. The mean frequency of occurrence of frogs in cat stomachs was 1.5%. The estimated annual per capita consumption by feral cats in Australia’s natural environments is 44 frogs, and, hence, the annual total take is estimated at 92 million frogs. The estimated annual per capita consumption by pet cats is 0.26 frogs, for a total annual kill of one million frogs by pet cats. Thirty native frog species (13% of the Australian frog fauna) are known to be killed by cats: this tally does not include any of the 51 threatened frog species, but this may simply be because no cat dietary studies have occurred within the small ranges typical of threatened frog species. ConclusionsThe present study indicated that cats in Australia kill nearly 100 million frogs annually, but further research is required to understand the conservation significance of such predation rates. ImplicationsThe present study completed a set of reviews of the impacts of cats on Australian terrestrial vertebrates. Cat predation on Australian frogs is substantial, but is likely to be markedly less than that on Australian reptiles, birds and mammals.

Native and non-native frogs responded differently to modernization at Japanese paddy fields

Rice farming modernizations, especially changes in the irrigation system, have been accused as one of the reasons of frog population decline in Japan. Here, we examined responses of native frog, Daruma pond frog (Pelophylax porosus porosus) and non-native frog, Rice frog (Fejervarya kawamurai) population to the modernization in Japanese paddy field. We tested the following two hypotheses: 1) native frog’s density will be lower in the modernized paddy field, and 2) non-native frog density will not be affected by modernization. After two periods of field studies (2017 and 2018), we found that native frog’s density is indeed lower in modernized paddy fields, and the non-native frog’s density is lower in the non-modernized sites. Presumably, changes of shallow soil ditches to concrete ditches in modernized paddy fields act as a death trap for Daruma pond frog. Ditch depth and the distance from forest also significantly affecting the density of Daruma pond frog. On the other hand, the population of Rice frog did not show any negative response to the modernizations. The non-native frog population remained stable because they may have high fecundity.