Differences in responsiveness and sensitivity to exogenous disruptors of the thyroid gland in three anuran species

Abstract

Anuran larval development comprises tissues/organs/systems that are: exclusively of larvae, able to be remodelled, and those of postmetamorphic stages. Also, the anuran larval development is characterized by inter‐related parameters: time, size and shape forming part of growth and differentiation. The anuran metamorphosis starts when growth and differentiation achieve a threshold that differs among species since it is regulated by a number of external (environmental) and internal (hormonal) processes. Here we explore the consequences of exogenous disruptors on the thyroid gland (e.g., methimazole and thyroxine as T4) of three species by immersing premetamorphic tadpoles in predetermined concentrations of the disruptors for short periods (10 or 16 days). The species were Pleurodema borellii, Leptodactylus chaquensis, and Dermatonotus muelleri, which all breed in small temporary ponds during the summer, but differ in their ecomorphology. The experiments were conducted to evaluate the effects of these substances on larval development (based in Gosner larval stages), morphometric variation in body parameters (snout‐vent and total length by larval stages), and thyroid gland histopathology at the end of the assays. In P. borelli and L. chaquensis, methimazole produces significant increment of size measurements (nonparametric Kruskal–Wallis, p < .05) during stages of digit differentiation and induced thyroid gland hypertrophy. In the three species, T4 exposure accelerated limb development and caused atrophy of thyroid gland. Prolonged T4 exposure in L. chaquensis and D. muelleri triggered metamorphic transformation in the gut and skull cartilages. Discussion about interspecific differences in responsiveness and sensitivity elucidates the importance of hormonal signals to morphological evolution.

Evolutionary and developmental considerations of the diet and gut morphology in ceratophryid tadpoles (Anura)

“…In Lepidobatrachus, the early loss of the vent tube indicates that remaining metamorphoric changes may promptly follow. This is consistent with that vent tube disappearing as the first sign of metamorphosis when it is experimentally induced with exogenous thyroxine [20].…”

Phenotypic Variation Through Ontogeny: Thyroid Axis Disruption During Larval Development in the Frog Pleurodema borellii

“…Tadpoles were immersed in predetermined concentrations at the beginning of larval development (early exposure, Gosner Stage 25), and after 18 days of hatching (late exposure). Larval exposure to disruptors began at an earlier development stage than in previous studies and finished later (Degitz et al, 2005;Fabrezi et al, 2019; Tables 1, 2).…”

“…Mesocosm experiments provide realistic data about environmental conditions and timing; thus, those experiments are useful to describe anuran larval development and are suitable to analyze developmental rates (Skelly and Kiesecker, 2001). Recently, mesocosm experiments of three anuran species (Pleurodema borellii, Leptodactylus chaquensis, and Dermatonotus muelleri) reported differential responsiveness and sensitivity to endocrine disruptors in tadpoles exposed from premetamorphic stages (Fabrezi et al, 2019). At similar concentrations of T4, developmental rates were modified, as evidenced in body size, histomorphology of the thyroid gland, limb development, and metamorphic transformations were triggered in gut and skull cartilage remodeling in two species (e.g., Leptodactylus chaquensis and Dermatonotus muelleri), whereas methimazole increased growth rates in Pleurodema borellii (Fabrezi et al, 2019).…”

“…Pleurodema borellii (Peracca, 1895) is a common frog present in the northwest of Argentina; reproduction and breeding occur during the wet season, eggs are laid in foam nests, tadpoles are typical of ephemeral ponds, with developmental stages identified by standard anuran staging table (Gosner, 1960;Cruz, 2020). Larval development in P. borellii shows intraspecific heterochronic variations, since tadpoles belonging to a single clutch complete the embryonic stages at the same time (6 days after fertilization), but larvae develop at different rates; then, after 20 days, tadpoles may reach stages of digit differentiation or remain at limb bud stages, suggesting different individual development under similar environmental variables (Fabrezi et al, 2019;this study).…”

Evaluation of the Acute Toxicity of an Ammonium Sulfate Fertilizer in Two Species of Anuran Tadpoles: Bufo mauritanicus (Schlegel 1841) and Rana ridibunda (Boulanger 1913)

“…This high sensitivity is due to incomplete differentiation of tissues and organs in tadpoles in the early stages of development (Herkovits et al 1978). Since the development of anurans is characterized by the appearance of new phenotypic characters over time (Fabrezi et al, 2019). In addition, in the anurans tadpoles belonging to the advanced stage of development, the gills are internal but for the first stages of development, the gills are external and in direct contact with water (Gosner, 1969); therefore, during this stage of development, a negative effect of ammonium sulfates on osmoregulation could be significant.…”