Rana Berlandieri Research Articles

Traffic Noise Impacts Glucocorticoid Response, Activity, and Growth in Two Species of Tadpoles.

There is a large body of evidence linking increased noise to negative health effects for animals. Anthropogenic noise induces behavioral and physiological reactions across a range of taxa and increased traffic noise affects glucocorticoid (GC) hormones associated with the stress response in amphibians. GCs help to maintain homeostasis while balancing energetic trade-offs between reproduction, growth, and activity. Stressors during early development can impact fitness at later life stages. We measured growth, activity, and GCs in response to high levels of traffic noise in two tadpole species that differ in life history: Acris crepitans and Rana berlandieri. We predicted that earlier exposures to traffic noise will slow down the development and alter the behavior and GC concentrations differently than later exposures. Subjects were initially either exposed to natural levels of traffic noise for 8 days (early exposure) or a white noise control (later exposure), then the treatment was switched. Activity was measured via focal sampling and tadpoles were categorized as active if movement was detected. Tadpoles exposed to white noise initially maintained mass and activity throughout the experiment and early exposure to traffic noise had a greater impact on mass, activity, and GCs. Tadpoles exposed to traffic noise initially lost mass, with A. crepitans regaining mass but not R. berlandieri. When exposed earlier to traffic noise, R. berlandieri increased movement when shifted to the white noise treatment while A. crepitans did not significantly change activity. Acris creptians had higher corticosterone release rates compared to R. berlandieri, and in both species, release rates were higher for tadpoles exposed to noise earlier. The longer-lived R. berlandieri allocated more of their energetic resources into activity, while the shorter-lived A. crepitans allocated energy toward growth. Rana berlandieri and A. crepitans utilized different coping strategies to contend with early exposure to traffic noise, potentially due to differences in life histories. Our findings suggest that these tadpoles employ different coping mechanisms to modulate stress responses in noise-polluted environments, and these mechanisms could influence their fitness later in life. Further study is needed to understand the impact in more sensitive tadpole species.

Exposure to Roundup and Antibiotics Alters Gut Microbial Communities, Growth, and Behavior in Rana berlandieri Tadpoles.

The gut microbiome is important for digestion, host fitness, and defense against pathogens, which provides a tool for host health assessment. Amphibians and their microbiomes are highly susceptible to pollutants including antibiotics. We explored the role of an unmanipulated gut microbiome on tadpole fitness and phenotype by comparing tadpoles of Rana berlandieri in a control group (1) with tadpoles exposed to: (2) Roundup® (glyphosate active ingredient), (3) antibiotic cocktail (enrofloxacin, sulfamethazine, trimethoprim, streptomycin, and penicillin), and (4) a combination of Roundup and antibiotics. Tadpoles in the antibiotic and combination treatments had the smallest dorsal body area and were the least active compared to control and Roundup-exposed tadpoles, which were less active than control tadpoles. The gut microbial community significantly changed across treatments at the alpha, beta, and core bacterial levels. However, we did not find significant differences between the antibiotic- and combination-exposed tadpoles, suggesting that antibiotic alone was enough to suppress growth, change behavior, and alter the gut microbiome composition. Here, we demonstrate that the gut microbial communities of tadpoles are sensitive to environmental pollutants, namely Roundup and antibiotics, which may have consequences for host phenotype and fitness via altered behavior and growth.

Molecular link between the metacercariae and adults of four species Haematoloechus (Digenea: Plagiorchioidea), including scanning electron microscopy characterization.

Haematoloechus comprises a species-rich genus of trematodes commonly found in the lungs of amphibians across the globe. Of the approximately 70 species reported worldwide, Mexico stands out as a biodiversity hot spot for the genus, with 16 species described. In Los Tuxtlas tropical rainforest, in south-eastern Mexico, three species have been reported, two of them endemic of the frog species occurring in the area. Here, we added the record of a fourth species in the area, and partially elucidated the life cycle of these species using DNA sequence data from the 28S rRNA and the COI genes. Frogs, and a diverse array of species of aquatic insects were sampled in two lakes within the tropical rain forest. Adults and metacercariae of Haematoloechus were obtained. Both developmental stages were linked molecularly contributing to our understanding of their transmission pathways, and probable host-specificity patterns. Each of the four species of Haematoloechus were sampled in a particular species of anisopteran odonate, and therefore were considered as specialists towards their second intermediate host. We validated the presence of H. complexus in the region of Los Tuxtlas because their metacercariae, sampled in the anisopteran dragongly Agriogomphus tumens, matched with sequences of H. complexus from Nebraska and Illinois in USA. We further described the ultrastructure of the tegument of three of the four species of Haematoloechus, sampled from their definitive host (Rana vaillanti, Rana berlandieri), to contribute with characters that can be reliable for species delimitation of the genus.

Rana berlandieri

This datasheet on Rana berlandieri covers Identity, Distribution.

A new species of Gorgoderina (Digenea: Gorgoderidae) from Rana berlandieri in Los Tuxtlas tropical rainforest, Mexico, with the elucidation of its life cycle.

Species in the genus Gorgoderina Looss, 1902 are parasites of the urinary bladder of amphibians and include around 50 species described globally. Molecular data on species of the genus are scarce, as is the information of their life-cycle patterns. During a survey on the genetic characterization of the frog trematodes in the tropical rain forest of Los Tuxtlas, in the Gulf of Mexico slope of Mexico, specimens of two morphotypes of Gorgoderina were sampled from the Rio Grande leopard frog, Rana berlandieri. One of them represented an undescribed species which is described herein as Gorgoderina rosamondae n. sp., whereas the other one was morphologically very similar to an apparently widely distributed North American species, G. attenuata, which has been previously reported in the same geographical area. Specimens of both morphotypes were sequenced for two nuclear and one mitochondrial genes. Phylogenetic trees corroborated the distinction of the new species, and data on the internal transcribed spacer 2 revealed genetic differences between G. attenuata sequenced from frogs in USA and specimens of Gorgoderina sp. from Los Tuxtlas, indicating the possibility that they also represent an undescribed species. COI sequences showed high genetic divergence values between the new species and Gorgoderina sp. from Los Tuxtlas (8.63-9.99%). Additionally, COI sequences of the larval forms (sporocyst, cercariae and metacercariae) sampled in the same locality from their first and second intermediate hosts (Pisidium sp. and Agriogomphus tumens, respectively) showed conspecificity, and the 3 host life-cycle of the new species was elucidated.

Artificial light at night (ALAN) affects the stress physiology but not the behavior or growth of Rana berlandieri and Bufo valliceps.

Artificial light at night (ALAN) alters the natural light dark patterns in ecosystems. ALAN can have a suite of effects on community structure and is a driver of evolutionary processes that influences a range of behavioral and physiological traits. Our understanding of possible effects of ALAN across species amphibians is lacking and research is warranted as ALAN could contribute to stress and declines of amphibian populations, particularly in urban areas. We tested the hypothesis that exposure to constant light or pulsed ALAN would physiologically stress Rio Grande leopard frog (Rana berlandieri) and Gulf Coast toad (Bufo valliceps) tadpoles. We reared tadpoles under constant or pulsed (on and off again) ALAN for 14 days and measured corticosterone release rates over time using a non-invasive water-borne hormone protocol. ALAN treatments did not affect behavior or growth. Tadpoles of both species had higher corticosterone (cort) release rates after 14 days of constant light exposure. Leopard frog tadpoles had lower cort release rates after exposure to pulsed ALAN while toad tadpoles had higher cort release rates. These results suggest that short-term exposure to constant or pulsed light at night may contribute to stress in tadpoles but that each species differentially modulated their cort response to ALAN exposure and a subsequent stressor. This flexibility in the upregulation and downregulation of hypothalamic-pituitary-interrenal axis response may indicate an alternative mechanism for diminishing the deleterious effects of chronic stress. Nonetheless, ALAN should be considered in management and conservation plans for amphibians.

Standardized ethograms and a device for assessing amphibian thermal responses in a warming world.

Most predictions of how populations and species of ectotherms will respond to global warming are based on estimates of the temperature at which organisms lose motor control (i.e., CTmax - the Critical Thermal Maximum). Here, we describe a non-lethal protocol and ethograms to estimate the relative tolerance of amphibians to increasing temperatures. These methods-suitable for field or laboratory conditions-are replicable, inexpensive and applicable to both post-metamorphic stages and organisms with direct development. We illustrate the use of this standardized protocol for four amphibians from a tropical cloud forest in Veracruz, Mexico with contrasting life histories: a lungless salamander (Aquiloeurycea cafetalera: Plethodontidae), a leaf-litter frog (Craugastor rhodopis: Craugastoridae), a semiaquatic frog (Lithobates berlandieri: Ranidae), and a tree frog (Rheohyla miotympanum: Hylidae). We identified four behavioral responses preceding CTmax for all amphibians included in this study: 1) Optimal Activity Range, 2) Supra-optimal Activity Range, 3) Heat Stress Range, and 4) Involuntary Movements Range. Additionally, we identified a fifth parameter associated with resilience to heat shock: 5) Recovery Stage after reaching CTmax. We conclude that the behavioral responses preceding the Critical Thermal Maximum are as informative as CTmax. Using behavioral responses to estimate thermal tolerance has the additional advantage of reducing the risk of injury or death of amphibians during physiological experiments.

Variation in Feeding Habits between Two Syntopic Frog Species (Genus Lithobates) of a Tropical Habitat in the Atlantic Versant of Mexico

Abstract Lithobates johni and Lithobates berlandieri have, respectively, a restricted and a wide geographic distribution, and cohabit in the center of the Atlantic versant of Mexico. We analyze and...

Validation of water-borne cortisol and corticosterone in tadpoles: Recovery rate from an acute stressor, repeatability, and evaluating rearing methods

Amphibian populations are declining globally, so understanding how individuals respond to anthropogenic and environmental stressors may aid conservation efforts. Using a non-invasive water-borne hormone assay, we measured the release rates of two glucocorticoid hormones, corticosterone and cortisol, in Rio Grande Leopard frog, Rana berlandieri, tadpoles. We validated this method pharmacologically and biologically using an adrenocorticotropic hormone (ACTH) challenge, exposure to exogenous corticosterone, and an agitation test. We calculated the repeatability of hormone release rates, the recovery time from an acute stressor, and explored rearing methods for tadpoles. Tadpole corticosterone release rates increased following an ACTH challenge, exposure to exogenous corticosterone, and agitation, validating the use of water-borne hormone methods in this species. After exposure to an acute stressor via agitation, corticosterone release rates began to decline after 2 h and were lowest after 6 h, suggesting a relatively rapid recovery from an acute stressor. Tadpoles reared in groups had higher corticosterone release rates than tadpoles reared individually, and lost mass by Day 7, while tadpoles reared individually did not show a stress response, therefore either rearing method is viable, but have differing physiological costs for tadpoles. Repeatability of corticosterone release rates was moderate to high in R. berlandieri tadpoles, indicating that this species can show a response to selection and potentially respond to rapid environmental change. Our results show that the water-borne hormone assay is a viable way to measure glucocorticoids in this species and is useful in the field of conservation physiology for rare and endangered species.

The Rio Grande leopard frog (Lithobates berlandieri) and other introduced and native riparian herpetofauna of the Coachella Valley, Riverside County, California

The Rio Grande leopard frog (Lithobates berlandieri) and other introduced and native riparian herpetofauna of the Coachella Valley, Riverside County, California

Life history of the Rio Grande leopard frog (Lithobates berlandieri) in Texas

ABSTRACTWe ascertained various life-history traits from an examination of 310 museum specimens of the Rio Grande leopard frog (Lithobates berlandieri) collected during 1907–2016 from Texas, USA. Lithobates berlandieri was captured during every month of the year except November, and adults were most frequently encountered during January–September, with a distinct peak in May. Mean body size of adult males (69.5 mm) was smaller than that of adult females (77.5 mm), and adult body sizes tended to be smaller at higher latitudes, a trend that was more pronounced in males. Females were gravid during January–September, and most gravid females were captured from late winter to early summer. Gonadal enlargement in males was generally high throughout January–September with no detectable seasonal increase. Feeding became widespread in both sexes during May–June shortly after a spring breeding bout. Spent females (ovarian stage 1) were common in July and lipid deposition increased in June/July, signalling oogenesis for breeding in the fall. From 15 gravid females, we estimated a mean clutch size of 3107 eggs which was correlated with female body size, yet egg diameter was not related to clutch or body size. Age to metamorphosis was likely 2–4 months depending upon whether eggs were laid in the winter/spring or late fall. If metamorphosis occurred in May/June, the minimum size at sexual maturity could have been reached in 7–8 months for adult males (50.1 mm) and in 9–10 months for adult females (57.2 mm). Mean adult body sizes, however, may have taken 14 to 17 months to reach. A synthesis across Texas populations suggests that the breeding season extends almost continuously from the fall through the winter and spring until mid-summer and is interrupted by extreme temperatures in the winter and summer.

Preliminary Report: Exotic armored catfish may reduce survival and growth of native amphibians

Invasive species threaten biodiversity worldwide. Armored catfish, which are benthic grazers, have been introduced globally and damage ecosystems in numerous ways. However, their competitive interactions with native benthic grazers have not been tested. This study tested for the effects of an invasive armored catfish (Hypostomus plecostomus) on performance in native Rio Grande leopard frog (Rana berlandieri) tadpoles. Aquarium tests showed that armored catfish can negatively affect native amphibian survival and growth even when food is abundant. However, mesocosm tests showed no effects or competition. While the mechanisms of effect remain unclear this is the first study to demonstrate exotic armored catfish as a potential threat to native amphibians, which are declining globally.

<p><strong>New records of amphibians parasitized by chiggers in Los Tuxtlas Biosphere Reserve, Mexico, and taxonomic notes on <em>Hannemania mexicana</em> (Acariformes: Prostigmata: Leeuwenhoekiidae) </strong></p>

We conducted a survey on chigger mites infesting amphibians at Los Tuxtlas Biosphere Reserve in Southeast Mexico, where we collected 25 frogs of three species: Lithobates berlandieri (n = 5), L. brownorum (n = 3) and L. vaillanti (n = 17). A total of 916 mites belonging to Hannemania mexicana Hoffmann, 1965 were collected. It is the first record of H. mexicana in the state of Veracruz and in L. brownorum and L. vaillanti. The frog species with the highest level of infestation was L. berlandieri with a prevalence of 80%, a mean abundance of 56 mites per host, and a mean intensity of 70 mites per infested host. Additionally, to corroborate identification we compared specimens from the type series of H. mexicana and we found variation in some characters of taxonomic importance such as the number of setae on leg genu and the shape of the palpal claw.

Experimental Exposure of Adult San Marcos Salamanders and Larval Leopard Frogs to the Cercariae ofCentrocestus formosanus

The gill parasite Centrocestus formosanus (Trematoda: Heterophyidae) is an exotic parasite of concern in Texas because it has been shown to infect multiple threatened and endangered fish species. The purpose of this study was to determine if C. formosanus could present a threat to larval anurans, as well as threatened neotenic salamanders endemic to the spring-fed systems of Texas. We exposed adults of the San Marcos salamander Eurycea nana (Caudata: Plethodontidae) and tadpoles of the Rio Grande leopard frog Lithobates berlandieri (Anura: Ranidae) to the cercariae of C. formosanus . The San Marcos salamander showed no signs of metacercarial infection, suggesting that E. nana may be refractory to C. formosanus cercariae. Centrocestus formosanus readily infects the gills of leopard frog tadpoles, but the metacercariae apparently died prior to reaching maturity in our tadpoles.

Lethal and Sublethal Effects of Salinity on Three Common Texas Amphibians

Amphibian populations worldwide are experiencing declines and contaminants are hypothesized to be one of the leading contributors to these declines. In particular, the salinization of amphibian habitats is a global issue that has received relatively little attention. Of the recent studies that have emerged, the majority focus on single-species responses, and because these studies often vary in methodology, assessing tolerances across species can be challenging. Thus, one step toward a broader understanding of salt loading is to assess tolerances across multiple species using similar methodologies. Additionally, in nature, amphibians can face low, sublethal concentrations of increased salinity. Though not lethal, these low concentrations can have long-term impacts on amphibian traits such as mass or their responses to future stressors. To address these issues, we first compared relative salinity tolerances of three common frogs in central Texas (Incilius nebulifer, Gulf Coast Toad; Lithobates berlandieri, Rio Grande Leopard Frog; and Acris crepitans, Blanchard's Cricket Frogs). Next, we explored the effect of sublethal salinities on the mass of I. nebulifer. Finally, we investigated the potential for sublethal salinities to increase tolerance of I. nebulifer to a later exposure of lethal salinity concentrations (acclimation). We found that across the three amphibian species, A. crepitans tadpoles were the most tolerant, followed by L. berlandieri tadpoles, and then I. nebulifer tadpoles. Sublethal concentrations of salinity did not affect mass of I. nebulifer tadpoles. Finally, exposure to sublethal levels of salinity did not increase tolerance of I. nebulifer tadpoles to a later exposure of higher salinity concentrations. Instead, tadpoles exposed to sublethal concentrations of salinity died at a faster rate when exposed later to a higher salinity concentration. With the increasing potential for salt loading to amphibian habitats due to anthropogenic influences and global climate change, understanding the consequences of salinity across multiple species as well as the effects of sublethal concentrations has important implications for amphibian conservation.

Class II ADP-ribosylation Factors Are Required for Efficient Secretion of Dengue Viruses

Identification and characterization of virus-host interactions are very important steps toward a better understanding of the molecular mechanisms responsible for disease progression and pathogenesis. To date, very few cellular factors involved in the life cycle of flaviviruses, which are important human pathogens, have been described. In this study, we demonstrate a crucial role for class II Arf proteins (Arf4 and Arf5) in the dengue flavivirus life cycle. We show that simultaneous depletion of Arf4 and Arf5 blocks recombinant subviral particle secretion for all four dengue serotypes. Immunostaining analysis suggests that class II Arf proteins are required at an early pre-Golgi step for dengue virus secretion. Using a horseradish peroxidase protein fused to a signal peptide, we show that class II Arfs act specifically on dengue virus secretion without altering the secretion of proteins through the constitutive secretory pathway. Co-immunoprecipitation data demonstrate that the dengue prM glycoprotein interacts with class II Arf proteins but not through its C-terminal VXPX motif. Finally, experiments performed with replication-competent dengue and yellow fever viruses demonstrate that the depletion of class II Arfs inhibits virus secretion, thus confirming their implication in the virus life cycle, although data obtained with West Nile virus pointed out the differences in virus-host interactions among flaviviruses. Our findings shed new light on a molecular mechanism used by dengue viruses during the late stages of the life cycle and demonstrate a novel function for class II Arf proteins.

Phylogenetic relationships of leopard frogs ( Rana pipiens complex) from an isolated coastal mountain range in southern Sonora, Mexico

Mitochondrial DNA sequence data from the control region and 12S rRNA in leopard frogs from the Sierra El Aguaje of southern Sonora, Mexico, together with GenBank sequences, were used to infer taxonomic identity and provide phylogenetic hypotheses for relationships with other members of the Rana pipiens complex. We show that frogs from the Sierra El Aguaje belong to the Rana berlandieri subgroup, or Scurrilirana clade, of the R. pipiens group, and are most closely related to Rana magnaocularis from Nayarit, Mexico. We also provide further evidence that Rana magnaocularis and R. yavapaiensis are close relatives.

The Chinese bamboo leaf odorous frog ( Rana ( Odorrana) versabilis) and North American Rana frogs share the same families of skin antimicrobial peptides

The Chinese bamboo leaf odorous frog ( Rana ( Odorrana) versabilis) and the North American pickerel frog ( Rana palustris) occupy different ecological niches on two different continents with no overlap in geographical distribution. R. palustris skin secretions contain a formidable array of antimicrobial peptides including homologs of brevinin-1, esculentin-1, esculentin-2, ranatuerin-2, a temporin and a family of peptides considered of unique structural attributes when isolated, palustrins 1–3. Here we describe the structures of mature peptides and precursors of eight putative antimicrobial peptides from the skin secretion of the Chinese bamboo leaf odorous frog ( Rana ( Odorrana) versabilis). Each peptide represents a structural homolog of respective peptide families isolated from R. palustris, including two peptides identical in primary structure to palustrin 1c and palustrin 3b. Additionally, two peptides were found to be structural homologs of ranatuerin 2B and ranatuerin 2P from the closely-related North American species, Rana berlandieri (the Rio Grande leopard frog) and Rana pipiens (the Northern leopard frog), respectively. Both palustrins and ranatuerins have hitherto been considered unique to North American ranid frogs. The use of primary structures of amphibian skin antimicrobial peptides is thus questionable as a taxonomic device or alternatively, the micro-evolution and/or ancestry of ranid frogs is more highly complex than previously thought.

Phylogeny of the Mexican coastal leopard frogs of the Rana berlandieri group based on mtDNA sequences

Phylogenetic relationships among specimens from 25 different locations for the six Mexican coastal leopard frog species of the Rana berlandieri species group were investigated using 797 bp of the mitochondrial 12S rDNA gene. Relationships among the haplotypes obtained were recovered using maximum parsimony and Bayesian analyses. Most of the clades recovered by both tree building methods are strongly supported, but conflicting clades recovered by each analysis are generally poorly supported. Both analyses reject the previously proposed subgroupings of the R. berlandieri species group. Based on the strongly supported relationships, genetic differentiation, and geographic distribution of the haplotypes examined, nine independent lineages appear to comprise the group of study. However, confirmation of the new proposed lineages will require further analyses based on other genetic markers and additional samples that cover their entire geographic distribution. Concordance was noted between Miocene–Pliocene geological and climatic events in Mexico and the relationships recovered among the lineages proposed and their geographic distribution.

Neotropical tadpoles: spatial and temporal distribution and habitat use in a seasonal lake in Veracruz, México

We studied a tadpole assemblage in a seasonal neotropical lake where 14 species of anurans reproduce. Tadpoles were collected monthly at nine sampling stations at depth intervals of 1 m from the surface to the bottom (13 m). Sufficient numbers of tadpoles of three species were collected to compare habitat use. This three species assemblage breed in the following order (first to last): Smilisca baudinii, Gastrophryne usta, and Rana berlandieri. R. berlandieri had the greatest microhabitat breadth followed by S. baudinii. S. baudinii and G. usta had high microhabitat overlap, but significant differences in microhabitat use were found. S. baudinii tended to occur near the bottom, while G. usta was near the surface. This study shows that temporal and habitat partitioning both occur and depend on the species of tadpole. Dynamic interactions occur between habitat and temporal dimensions. Phenology and habitat selection depend both on the species and on abiotic and biotic factors.