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The Pace-of-Life syndrome proposes that behavioural, physiological and immune characteristics vary along a slow-fast gradient. Urbanization poses several physiological challenges to organisms. However, little is known about how the health status of frogs is affected by urbanization in the Tropics, which have a faster and more recent urbanization than the northern hemisphere. Here, we analysed a suite of physiological variables that reflect whole organism health, reproduction, metabolic and circulatory physiology and leukocyte responses in Leptodactylus podicipinus. Specifically, we tested how leukocyte profile, erythrocyte morphometrics and germ cell density, as well as somatic indices and erythrocyte nuclear abnormalities differ throughout the adult life span between urban and rural populations. We used Phenotypic Trajectory Analysis to test the effect of age and site on each of the multivariate data sets; and a Generalised Linear Model to test the effect of site and age on nuclear abnormalities. Somatic indices, erythrocyte nuclear abnormalities, erythrocyte morphometrics and leukocyte profile differed between populations, but less so for germ cell density. We found a large effect of site on nuclear abnormalities, with urban frogs having twice as many abnormalities as rural frogs. Our results suggest that urban frogs have a faster pace of life, but the response of phenotypic compartments is not fully concerted.

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This study evaluated the genetic damage, oxidative stress, neurotoxicity, and energy metabolism in bullfrog tadpoles (Lithobates catesbeianus) exposed to water from two sites of the Sorocaba River, Ibiúna (PI), and Itupararanga reservoir (PIR), in summer and winter. After 96-h exposure, the erythrocyte number decreased in PI and increase in PIR in summer. Bullfrogs show oxidative unbalance (liver, kidney, and muscle), with alterations in the nitric oxide synthase and glucose 6-phosphate dehydrogenase. Cholinesterase increased in the brain in PI and PIR in the summer and decreased in PI in the winter. It also increased in the muscle in both PI and PIR in the winter. Tadpoles show alterations in the activity of the metabolic enzymes (liver, kidney, and muscle), such as phosphofructokinase, pyruvatokinase, malate dehydrogenase, and lactate dehydrogenase; and in the amount of glucose and triglycerides metabolites. Exposure to the Sorocaba River reflected a stressful situation for L. catesbeianus as the changes caused to their metabolism associated with oxidative stress and neurotoxicity may have effects on the development of tadpoles.

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Hematological parameters can provide key information to an animal health status. However, this information is usually hard to obtain. Here, we described the hematological parameters of Leptodactylus podicipinus in the Brazilian Pantanal. We measured red blood cell morphometrics, erythrogram, and leukogram. We also tested for phylogenetic signal in the erythrogram and leukogram of 48 frog species from 15 families, testing if body size explains their variation. Lymphocytes were the most abundant leukocytes (>60%) in L. podicipinus, followed by neutrophils (∼10%). Given that L. podicipinus is an abundant and widely distributed species in central Brazil, knowing its hematological pattern can help establish a baseline and improve its use as a bioindicator of environmental degradation. Mean corpuscular hemoglobin and value contributed more to the phylomorphospace of erythrogram, in which Leptodactylus spp. and Hypsiboas raniceps had lower values of these variables, whereas Bufotes viridis and Hyla arborea had high values. The phylogenetic signal was spread throughout the dimensions of the leukogram phylomorphospace. The variables that most contributed to it were total leukocytes counts, lymphocytes, and neutrophils. We also found a moderate phylogenetic signal for both the erythrogram and leukogram. Accordingly, body size accounted for a low proportion of variation in both the leukogram (4.7%) and erythrogram (0.57%). By applying phylogenetic comparative methods to hematological parameters, our results add a new perspective on the evolution of blood cell physiology in frogs.

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For over 40 years, anurans have been used as a study model to assess the adverse effects of benzo(α)pyrene (BαP), which include genotoxic, hepatotoxic, and immunotoxic effects. In these studies, BαP is administered cutaneously or by injection, with no comparison between two or more routes. The purpose of this study is to assess whether the effect of BαP is influenced by its route of administration, using the response of hepatic biomarkers of Physalaemus nattereri. Specimens (n = 108) were collected and divided into three experimental treatments (cutaneous, injection, and oral) and three experimental times (one, three, and seven days). Specimens received 0.02 ml of pure mineral oil (control) or mineral oil containing 2 mg/kg of BαP. The BαP causes changes in morphological (melanin, hemosiderin, lipofuscin, and mast cells) and biochemical (superoxide dismutase and glutathione S-transferase) hepatic biomarkers. Compared to biochemical, morphological biomarkers underwent a greater number of significant changes due to the treatment with BαP. The route of exposure alters the effects of BαP, mainly seen in morphological biomarkers, especially the pigments melanin, hemosiderin, and lipofuscin. In these pigments, the effect of the exposure pathway changes according to the analyzed biomarker, and the exposure time modulates the exposure pathway effect. These results are unprecedented for anurans and contribute to the field of herpetology and ecotoxicology.

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Environmental pollution plays an important role in amphibian population decline. Contamination with endocrine disrupting chemicals (EDCs) is particularly worrying due to their capacity to adversely affect organisms at low doses. We hypothesized that exposure to EDCs such as 4-nonylphenol (NP) and cyproterone acetate (CPA) could trigger responses in the liver and gonads, due to toxic and endocrine disrupting effects. Growth rate may also be impaired by contamination. We investigated sublethal effects of a 28-day exposure to three different concentrations of NP and CPA on liver pigmentation, gonadal morphology, body mass, and length of tadpoles and juveniles Lithobates catesbeianus. Liver pigmentation and the gonadal morphologies of treated tadpoles did not differ from control, but growth rate was impaired by both pollutants. Juveniles treated with 10 µg/L NP and 0.025 and 0.25 ng/L CPA displayed increased liver melanin pigmentation, but gonadal morphologies, sex ratios, and body mass were not affected after treatments. The increase in liver pigmentation may be related to defensive, cytoprotective role of melanomacrophages. The decreased growth rate in tadpoles indicates toxic effects of NP and CPA. Thus, contamination with NP and CPA remains a concern and sublethal effects of different dosages of the compounds on native species should be determined.

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The sensitivity of anuran to the effects of habitat destruction and contamination has led to a preoccupying global decline in their populations. Morphological biomarkers such as micronuclei and other erythrocyte nuclear abnormalities (ENAs), as well as the occurrence of hepatic melanin, can be used to evaluate the effects of habitat impacts. In the present study, these two parameters were combined for the in situ assessment of the effects of soybean cultivation on the grassfrog, Leptodactylus fuscus. Specimens were also collected from a protected area to provide a reference site (non-agricultural environment). The frequency of some of the nuclear abnormalities in the animals from the soybean plantation was much higher than that recorded at the reference site, in particular micronuclei, which were 3.6 times more frequent in the plantation, lobulated nuclei (3.4 times more frequent), and reniform nuclei, which were four times more common than at the reference site. The combined analysis of all the ENAs together also revealed a frequency approximately 1.4 times higher in the animals from the soybean plantation, in comparison with the protected area. Smaller areas of hepatic melanin were observed in the specimens from the soybean plantation. These results provide further evidence of the sensitivity of anurans to habitat impacts and indicate that animals found in soybean plantations are susceptible to systematic alterations of their cells.

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Fish have defense systems that are capable of repairing damages caused by xenobiotics like benzo[a]pyrene (BaP), so the aims of this study were to identify BaP toxicity in melanomacrophages (MMs) cytoskeleton, evaluate the melanin area in MMs, and analyze genotoxicity. Rainbow trout juveniles (n = 24) were split in 48h and 7d treatments that received 2 mg/kg of BaP. After the experiment, blood samples were collected and liver was removed, to proceed with the analysis: EROD activity, MMs melanin area quantification, melanosomes movements, and a genotoxicity test. The results revealed increased in EROD activity after 48-h and 7-day BaP exposure. The group 7d displayed a reduction in MMs pigmented area, melanosomes aggregation, in addition to an increased frequency of micronucleus. By means of the EROD assay, it was possible to confirm the activation of BaP biotransformation system. The impairment of the melanosomes' movements possibly by an inactivation of the protein responsible for the pigment dispersion consequently affects the melanin area and thus might negatively impact the MMs detoxification capacity. In addition to this cytotoxicity, the increased frequency of micronucleus might also indicate the genotoxicity of BaP in this important fish species.

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The aim of this study was to evaluate the genotoxic and morphological systemic effects of both an acute and a chronic exposure of bullfrog tadpoles to fipronil. Lithobates catesbeianus tadpoles had morphological biomarkers (skin, liver, and blood) analyzed at Gosner stages 36-38, when exposed to four different concentrations of Regent® 800 WG (80% fipronil): 0.00 (control), 0.04, 0.08, 0.4 mg/L, and four experimental times: 4, 8, 12, and 16 days. Body darkness responded directly to the treatment and exposure time. There was a treatment-dependent decrease in darkness of heads and tails. In relation to the biometric analysis, fipronil induced a decrease in the individual weight and liver mass at the end of the experiments, whereas the hepatosomatic index did not vary according to the treatment. For the exposed animals and for the control group, the area of hepatic melanin increased as exposure time increased. Fipronil has genotoxic effects on L. catesbeianus tadpoles even after short exposure times (e.g., 4 and 8 days), and the main nuclear abnormality is in the anucleate cells. A relevant correlation was observed between genotoxic biomarkers and cutaneous and internal melanin. The frequency of nuclear abnormalities is inversely correlated both with the hepatic melanin area and with the cutaneous melanin of animals. Fipronil has distinct systemic effects on tadpoles based on its concentration, as well as on its exposure time. Such alterations (pigmentation level and rate of erythrocyte abnormality) result in morphological and physiological effects, which may compromise the behavior and survival of the anurans.

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The liver is an important metabolic organ in vertebrates. In anurans, the hepatosomatic index (HSI) reflects differences in energy storage and reproductive activities between males and females. The objective of this study was to describe the histological and histometric parameters of the livers of five species of Neotropical anurans, taking sex-related differences into account. We also tested how the relationship between quantitative histometric variables and HSI varied between males and females in different species. Five males and five females of Elachistocleis matogrosso, Leptodactylus podicipinus, Lysapsus limellum, Pseudis platensis, and Trachycephalus typhonius were captured in central Brazil during the rainy season. HSI did not vary according to sex, but it varied among species. Elachistocleis matogrosso had the highest HSI due to the large hepatocyte size. The percentage of melanomacrophage centers (MMCs) was higher in P. platensis and L. limellum. In T. thyphonius, hepatocyte area was negatively associated with HSI, while the MMC percentages were positively associated with HSI. The liver plays a key role in reproductive activities, especially for species with explosive reproduction. Additionally, histometric patterns and volumetric structural density varied between males and females due to energy utilization for reproduction. Not only are these results important for future studies on hepatic morphophysiology but they also provide tools for evolutionary and phylogenetic studies.

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The liver of anurans play an important role in metabolism, including detoxification, the biotransformation of molecules, and the storage of metabolites. Surfactants are part of domestic and industrial effluents. The effects of linear alkylbenzene sulfonate (LAS) on anuran liver remain unknown, however, some studies have evaluated the effects of LAS on the skin, gills, heart, testes, and liver of fishes. Here, we tested the hypothesis that LAS is hepatotoxic, promoting morphometric alterations in hepatocytes along with inflammation in the tissue, altering hepatic catabolism. We evaluated the effects of a LAS concentration that is considered environmentally safe in Brazilian inland waters on the liver of Lithobates catesbeianus tadpoles, including studies on morphology, morphometry, immunology, and metabolism. LAS exposure promoted enlargement of liver sinusoids and vacuolization of hepatocytes. Exposure to LAS also increased the area of mast cells and melanomacrophages (MMs). Additionally, LAS exposure increased hemosiderin inside MMs, suggesting alterations in the catabolism and storage of iron. Hepatocyte size increased after exposure to LAS, suggesting cytotoxic effects. Integrative analyses (i.e., morphometric, metabolic, and immunological) demonstrated hepatotoxic effects of LAS. These types of studies are key to understanding the negative effects of these substances on tadpole health, as these liver alterations impair anuran homeostasis.

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BACKGROUND: Changes in land use trigger environmental changes that can lead to decreased biodiversity and species loss. The liver is an essential detoxification organ that reflects systemic physiological responses to environmental changes. Here, we tested whether contrasting land use patterns influence the amount of substances from the hepatic cellular catabolism and melanomacrophages (MMs) of five anuran species in the Brazilian Cerrado. METHODS: We collected the same five species of pond-dwelling frogs in one protected area and in an area with intense agricultural activity. We used routine histological and histochemical techniques to quantify the area occupied by lipofuscin, melanin, and hemosiderin in the liver of two frogs Leptodactylus fuscus, Physalaemus cuvieri, and three tree-frogs Dendropsophus minutus, Scinax fuscomarginatus, and Boana albopunctata. We classified land use types in a buffer around each pond based on satellite images. We then used a double-constrained Correspondence Analysis, a recently developed ecological method to relate functional traits to environmental variables, to test the effect of each land use type on the area of each liver pigment. RESULTS: There was an increase in the amount of melanin in environments with high proportion of agriculture, as well as variation in the amount of lipofuscin and hemosiderin. Liver pigments of P. cuvieri and B. albopunctata varied more strongly in response to land use types, suggesting they could be good indicator species. Therefore, the area of MMs in the liver and the metabolic products in their cytoplasm can be used as biomarkers of environmental changes in regions with intense agricultural activities. Our results add a new perspective to the influence of land use patterns on environmental health by highlighting the effect of environmental changes on internal morphological aspects of animals.

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Endocrine disrupting chemicals are one of the most important factors contributing to worldwide amphibian decline. The 4-nonylphenol (NP) is a degradation product of several compounds, such as detergents and pesticides, affecting the aquatic environment. Here, we test whether treatment with NP has an effect on developing ovarian tissue, nuclear abnormalities in erythrocytes, and body darkness in pre-metamorphic tadpoles of the bullfrog Lithobates catesbeianus. Tadpoles were exposed for 14 days to three different concentrations of NP (1, 10, and 100 µg/L) besides the control group, which was maintained only with water. After determining body coloration, animals were euthanized and gonads and blood were collected and processed for histology and genotoxic analysis. Even though most animals were females, intersex tadpoles were observed in control and treated groups and there were no males in any group. The highest concentration of NP showed an increase in atretic oocytes, but the area corresponding to somatic compartment and early and late germ cells were not affected. Furthermore, all treated groups presented higher amount of nuclear abnormalities in erythrocytes and body darkening when compared with the control group. These results suggest that NP causes genetic damage and morphological alterations in L. catesbeianus tadpoles by disrupting oogenesis, inducing genotoxicity and increasing body coloration. Its effects on gonadal development could cause future impairments in reproduction, while its deleterious effects on genotoxicity and body pigmentation could be used as a biomarker of effect to this compound.

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Many agricultural practices cause environmental degradation that affects the cellular integrity of anurans. In the present study, we provided in situ data of Dendropsophus minutus, Physalaemus cuvieri, and Scinax fuscovarius collected in soybean/corn and conservation units in the Brazilian Cerrado. The in situ data showed no significant variation in the micronucleus frequency between the sites, only the reniform cells had a higher rate for the agricultural environment. A combined analysis of all nuclear erythrocyte abnormalities (ENAs = nuclear buds, reniform nuclei, apoptotic cell, binucleated, and anucleated cells) was recorded higher frequencies in farmland. Overall, Scinax fuscovarius was considered the best potential bioindicator for soybean/corn plantations. Finally, we recommend expanding the micronucleus test for in situ studies to expand our understanding of the sensitivity of native anuran species and provide a more systematic assessment of the adverse effects of environmental pollutants on wildlife.

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Amphibians are considered to be excellent bioindicators to their morphophysiological characteristics and life cycle. In this context, the present study investigated the morphological integrity of anuran larvae collected in preserved environments in the Emas National Park, in the municipality of Mineiros (Goiás state, Brazil), and in environments representative of the agricultural matrix of the Rio Verde region, also in Goiás, where there is a long history of the use of agricultural pesticides. Samples of water from temporary ponds, permanent dams, and veredas were analyzed for the presence of pesticides and, especially atrazine (5350 µg/L), found at significantly higher concentrations in the agricultural matrix. We observed a high percentage (approximately 10%) of morphological malformations including alterations of the fins in Boana albopunctatus and Scinax fuscovarius; alteration in oral structures in B. albopunctatus, Dematonotus muelleri, Physalaemus centralis, Physalaemus cuvieri, and Leptodactylus fuscus mainly in the tadpoles collected in the agricultural environment in comparison with those from the protected area (3.5%; P < 0.0001, χ2 31.75). However, changes in the eyes, mouth, intestines, and nostrils, as well as amelia were observed only in the agricultural environment. The vast majority of the observed malformations were associated with the tail and oral disc, which suggests that these anatomical parameters may be used as sensitive morphological biomarkers. Given these findings, we reinforce that areas of agricultural land may have a deleterious effect on the morphological integrity of the tadpoles and consequently, on their development, and that these features may be used as indicators of environmental quality and health.

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Brazil is an important consumer of herbicides. In sugarcane cultivation-the country's most extensive agricultural crop-atrazine-based formulations are the principal form of weed control. Several studies have investigated adverse effects of atrazine or their formulations on anurans, but not specifically on Brazilian species. Our aim was therefore to investigate the lethal and sublethal effects of an atrazine-based herbicide in Rhinella schneideri tadpoles and, in particular, effects on the pigmentation system as a new endpoint in ecotoxicological studies. Rhinella schneideri tadpoles at the Gosner-30 stage were exposed to the atrazine-based herbicide formulation, SIPTRAN 500 SC®, in acute bioassays at concentrations of 1.5-25 mg/L. The lethal and sublethal effects induced were analysed at different ecotoxicological levels: organismal level (alterations in behaviour, growth, development, and body mass; morphologic abnormalities), histological level (liver histopathology), the pigmentation system (melanomacrophages and dermal-melanophores), and cellular level (erythrocyte micronucleus formation and other nuclear-abnormalities). This herbicide induced sublethal effects at the organismal level with alterations in swimming and growth and morphologic abnormalities. These results demonstrated that, in anuran tadpoles, the atrazine-based agrochemical increased the frequency of micronucleus formation and other nuclear-abnormalities in erythrocytes and caused liver damage. In addition, we demonstrated for the first time effects of an atrazine-based formulation on the pigmentation system of anuran tadpoles, specifically an increase in the number of melanomacrophages and dermal melanophores. This study is the first to use several widely differing endpoints at different ecotoxicological levels in a comprehensive manner for assessment of the effects of environmental stressors in order to determine the health status of Neotropical anuran species. In doing so, this study establishes a foundation for future ecological assessments.

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The processes of follicular development, ovulation, egg capture, and egg transport vary among vertebrates. Therefore, analysis of the reproductive tract of several lineages is needed for understanding the evolutionary changes of the reproductive system. In turtles, the ovulated eggs are released into the coelomic cavity and taken up by one of the two oviducts, a phenomenon called extrauterine migration of eggs. However, the process of egg uptake in lizards is different. The egg is ovulated directly into the infundibulum, and oocyte uptake by the contralateral oviduct rarely occurs. The same pattern has been hypothesized to occur in snakes. To test this hypothesis, we analyzed the reproductive tract of female Micrurus corallinus preserved in zoological collections. We examined the anatomical characteristics of the infundibulum and ovary and compared the reproductive output between the ovaries to verify the mechanism of egg capture and the anatomical viability of extrauterine migration of eggs. The reproductive output of the right ovary was higher than that of the left ovary, and the higher number of eggs in the right oviduct is due exclusively to the production of the ipsilateral ovary. Several anatomical features prevent extrauterine migration of eggs, including the asymmetry of the reproductive system, the arrangement of the ovarian follicles in a single row, and the formation of a wrapping around the ovary and infundibulum by the visceral pleuroperitoneum membrane (preventing against ectopic eggs). Therefore, the hypothesis of egg capture by the contralateral oviduct is anatomically infeasible in M. corallinus and possibly in other snakes. Anat Rec, 301:1936-1943, 2018. © 2018 Wiley Periodicals, Inc.

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Glyphosate (GLY) is the most used herbicide worldwide and its effects on anurans are well known. Pollutants can cause physiological and morphological effects. Therefore, this study evaluated the effects of GLY on hepatic melanomacrophages as a response to environmental stressors. Three treatments were exposed to different concentrations of pure GLY (100, 1000, and 10,000 µg g(-1), respectively), and there was also a control group. After the experimental time, liver and blood were analyzed. Melanomacrophages (MMCs) were located between the hepatocyte cordons, close to sinusoids. GLY increased the melanin area in MMCs of Leptodactylus latinasus exposed since lowest concentration until highest concentration. GLY also changed the occurrence of hepatic catabolism pigments into melanomacrophages and erythrocyte nuclear abnormalities; therefore, it can interfere with the hepatic metabolism. In conclusion, GLY promotes alterations in the hepatic tissue and erythrocyte nuclear abnormalities. Furthermore, MMCs may be useful as morphological responses of GLY effects.

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Melanomacrophages are the pigmented cells present in the hematopoietic organs. Besides melanin, hemosiderin and lipofuscin are also observed in the melanomacrophages. For the liver, however, numerous studies relate these cells to immunological and metabolic functions. Therefore, the aim of this study is to evaluate the hepatic metabolism by quantifying melanin, hemosiderin and lipofuscin in the anuran Eupemphix nattereri submitted to varying thermal conditions. E. nattereri adult males were separated into three groups, as follows: (i) five animals in the control group were kept at room temperature (27°C); (ii) 30 animals were submitted to hyperthermic (35.1°C); and (iii) 30 to hypothermic (18.9°) conditions. In each experiment, the animals were analyzed and separated into two different treatments: (1) immediately after undergoing the stress; and, (2) after recovering from the stress caused by the stimulus, at three distinct times (12 hr, 24 hr, and 48 hr). Both hyperthermia and hypothermia decreased hepatic pigmentation after thermal stress. The recovered animals of both experimental treatments showed as much pigmentation as the control animals. Thermal stress alters hemosiderin and lipofuscin as well, which may be related to liver function catabolism. In conclusion, liver pigmentation decreased due to temperature variation and duration of thermal stimulation to which the animals were exposed. The increase in temperature rather than hypothermia led to more drastic physiological disorders. In this study, we observed that thermal stress for a short period compromises the morphology and liver function, as observed by the changing pigmentation of melanomacrophages. These analyses can be used as biomarkers of environmental effects.

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The greatest diversity of anurans in the world is in Brazil and one of the major challenges is to reconcile the accelerated economic development with strategies that aim to maintain this diversity in forest fragments, often representing ESUs of some biomes. This study aimed to obtain data that will support conservation projects through the pioneering use of ISSR analysis in Neotropical anurans, estimating the intra- and interpopulation genetic diversity of four populations of P. cuvieri (Paraná and São Paulo regions). Of the 65 loci scored 58 were polymorphic, with 0.797 intrapopulation variation and 0.203 interpopulation variation. The index of interpopulation genetic differentiation (Fst) proved to be high among the population of Marmeleiro-PR and the three populations of SP (Fst > 0.288); genetic dissimilarity was related to the geographical distance. The ISSR proved to be efficient and useful molecular markers in comparison with other markers most widely used for preliminary diagnosis of genetic diversity in populations of amphibians, and could be applied as a tool for future conservation projects, since they could identify potential ESUs and influence decisions on the preservation of fragments.

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The arrangement of the hepatic tissue is directly related to physiological characteristics of animals, such as ectothermy, diet, and reproductive status. Here, we describe the anatomy, histology, and ultrastructure of the liver in adult males of Eupemphix nattereri during the breeding season. The liver is an organ with an irregular shape, red in color, and occupies a large portion of the body cavity. Anatomically, it is divided into three lobes: right, mid, and left. Further subdivision into lobules is not observed. A thin capsule of connective tissue covers externally the organ, which is responsible for its support and protection. The hepatic parenchyma is formed by two layers of polyhedralshaped hepatocytes arranged in a double cordon. These cordons are filled with hepatic sinusoids that greatly vary in size and are closely associated with hepatocytes. There are also bile canaliculi and immune cells between hepatic cordons-the melanomacrophages. These canaliculi are covered with short microvilli, which protrude into the lumen. Melanomacrophages have several cytoplasmic substances, such as melanin, lipofuscin, and hemosiderin, which form due to liver metabolism and contribute to the typical coloration of the organ. A large amount of mitochondria and other organelles, such as a well-developed Golgi apparatus, smooth endoplasmic reticulum, and abundant glycogen are found in the cytoplasm of hepatocytes.

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