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Outdoor mesocosm study evaluating how mass, NaCl tolerance, and pesticide tolerance affect oxidative stress biomarkers (CAT, SOD, GR, GPx, TBARS) in larval wood frogs (Rana sylvatica) exposed to baseline and NaCl-contaminated conditions, 2019
Biomarkers of oxidative stress can aid in wildlife monitoring by allowing conservationists to detect sublethal environmental shifts. However, interpretation of stress responses can be complicated by multiple interacting factors (e.g., individual development, evolved physiological tolerance to stressors) which alter biomarker expression. Here, we investigated how individual ontogenetic traits and population-level tolerance traits influence oxidative stress responses under baseline and contaminated environmental conditions. For our model contaminant, we used NaCl (common freshwater contaminant due to factors such as coastal flooding, irrigation, airborne salt circulation, drought, runoff from road deicing salts). For our model wildlife populations, we used larval wood frogs (Rana sylvatica) from six noninteracting populations known to vary in two population-level tolerance traits: NaCl tolerance (calculated as average time to death from lethal NaCl exposure) and pesticide tolerance (determined by proxy of distance to agriculture - a consistent and highly repeatable relationship). At an outdoor research facility, R. sylvatica tadpoles were exposed to either baseline conditions (0 g/L NaCl added) or NaCl-contaminated conditions (1 g/L NaCl added for 21 days, then reduced to 0.5 g/L NaCl). Exposures were conducted in individual units with 40 replicates per population for each treatment. The experiment was terminated per individual to capture the full term of larval development (Developmental stage: Gosner stage 36), lasting between 33-48 days. For each individual, we measured mass, Snout-Vent-Length, and developmental stage before processing for biomarker expression. Individual homogenates were assayed for oxidative stress biomarkers superoxide dismutase (SOD; responsible for Reactive Oxygen Species capture and peroxide production), glutathione peroxidase (GPx; responsible for high-affinity peroxide reduction), catalase (CAT; responsible for low-affinity peroxide reducti
Fig. 5 in Captive management, reproduction, and comparative larval development of Klappenbach's Red-bellied Frog, Melanophryniscus klappenbachi Prigioni and Langone, 2000
Fig. 5. Body size of different test groups. (A) Single tadpole, O‒1, and (B) five tadpoles per box, O‒5, in osmosis water. (C) Single tadpole, P‒1, and (D) five tadpoles per box, P‒5, in pond water.
Fig. 2. Keeping and rearing M in Captive management, reproduction, and comparative larval development of Klappenbach's Red-bellied Frog, Melanophryniscus klappenbachi Prigioni and Langone, 2000
Fig. 2. Keeping and rearing M. klappenbachi. (A) Terrarium of the adult group housing eight specimens. (B) Rearing of the tadpole test groups in a climate chamber.(C) Rearing containers for the young toadlets.
Fig. 1 in Captive management, reproduction, and comparative larval development of Klappenbach's Red-bellied Frog, Melanophryniscus klappenbachi Prigioni and Langone, 2000
Fig. 1. Melanophryniscus klappenbachi. (A) Dorsal and (B) ventral view of an adult female. (C) Amplexus.(D) Egg clump attached to moss. (E) Contrasting photo of a tadpole, used for evaluating the growth.
Fig. 4 in Captive management, reproduction, and comparative larval development of Klappenbach's Red-bellied Frog, Melanophryniscus klappenbachi Prigioni and Langone, 2000
Fig. 4. (A) Mortality rate of different test groups until metamorphosis. (B) Average growth rate of the different test groups. (C) Number of tadpoles metamorphosed per day after hatching (O = osmosis water, P = pond water, number indicates individuals per container).
Fig. 3 in Captive management, reproduction, and comparative larval development of Klappenbach's Red-bellied Frog, Melanophryniscus klappenbachi Prigioni and Langone, 2000
Fig. 3. Developing coloration in young toadlets of different ages. (A) Recently metamorphosed toadlet. (B) Ten days after metamorphosis. (C) Twenty-three days after metamorphosis. (D) Two months after metamorphosis.
Fig. 63. Character 109, dorsal larval transport. State 1 in PHYLOGENETIC SYSTEMATICS OF DART-POISON FROGS AND THEIR RELATIVES (AMPHIBIA: ATHESPHATANURA: DENDROBATIDAE)
Fig. 63. Character 109, dorsal larval transport. State 1, present (fraterdanieli, specimens at UVC). This male nurse frog was transporting 12 tadpoles.
Fig. 61. Character 88, larval oral disc. A, B in PHYLOGENETIC SYSTEMATICS OF DART-POISON FROGS AND THEIR RELATIVES (AMPHIBIA: ATHESPHATANURA: DENDROBATIDAE)
Fig. 61. Character 88, larval oral disc. A, B: Ventral (A) and lateral (B) views of State 0, ''normal'' (''Neblina species'', AMNH 118673). C, D: Ventral (C) and lateral (D) views of State 1, umbelliform disc (nubicola, AMNH 94849). Note also the submarginal papillae scattered over the surface of the oral disc (character 91).
Fig. 1 in Patterns of larval development in Cretaceous pipid frogs
Fig. 1. Larval development in the Early Cretaceous pipid Thoraciliacus rostriceps from Makhtesh Ramon, Israel. A. The earliest recorded larva, with rudimentary ribs and not−yet fused neural arches; stage NF 59, dorsal aspect (HUJZ−Th01). B. Same developmental stage (HUJZ−FL3b). C. Stage NF 60, ventral view (HUJZ−Th03); note the anterior tip of the parasphenoid exceeding beyond the both frontoparietals. The photo taken by Zeiss Stemi 2000C stereomicroscope (C1). The photo taken by means of the image analysing software "Image Pro Plus" (C2). D. Stage NF 60, dorsal view (HUJZ−Th02). The photo taken by Zeiss Stemi 2000C stereomicroscope (D1). The photo taken by means of the image analysing software "Image Pro Plus" (D2). E. Stage NF 61, ventral view (HUJZ−Th04). Rudiments of ilia and femora are marked by arrows. F. Estimated stage NF 63, according to ossified tips of toes, probably ventral aspect (HUJZ−Th11). G. Postmetamorphic stage with the ilio−sacral articulation, ventral aspect (HUJZ−F301). H. Postmetamorphic stage, ventral aspect (HUJZF235); note fusion of sacral and praesacral diapophyses. I. Adult, ventral aspect (HUJZ−F93; holotype, cf. also Trueb 1999). Scale bars 5 mm.
Fig. 5 in Patterns of larval development in Cretaceous pipid frogs
Fig. 5. Comparison of the relative sequence of some developmental events of the skull in the Cretaceous Shomronella, Oligocene Palaeobatrachus, and Recent Xenopus, with the Paleozoic Apateon (Temnospondyli: Branchiosauridae), primitive recent caudates Ranodon and Salamandrella (Cryptobranchoidea: Hynobiidae), and neotenic caudate Ambystoma (Ambystomatidae). Bones that are retained in the anurans are in bold. Because of differences in definition of metamorphosis among various authors, and because of different definition of developmental stages in the Paleozoic amphibians, caudates and anurans, comparison in terms of exactly corresponding anatomical stages is not possible. The most objective for staging in the amphibians is formation of the mouth, beginning of metamorphosis (associated with reduction of gills in caudates, development of the limbs in anurans), and the end of metamorphosis (loss of tail in the anurans). Data on Apateon from Schoch (1998), on the caudates from Lebedkina (2004), and on Palaeobatrachus from Roček (2003b).
Fig. 2 in Patterns of larval development in Cretaceous pipid frogs
Fig. 2. Larval development of the Early Cretaceous pipid Shomronella jordanica from the Shomron region, Israel. A. The earliest recorded larva, stage approximately NF 47–50, probably dorsal aspect (HUJZ−13150). Displaced eyeball marked by arrow. Note complete parasphenoid. The photo taken by Zeiss Stemi 2000C stereomicroscope (A1). The photo taken by means of the image analysing software "Image Pro Plus" (A2). B. Moderately older stage, approximately NF 51–54, dorsal view (HUJZ−13062). Displaced eyeball marked by arrow. C. Approximately same stage as the previous, dorsal view (HUJZ−13190). Rudimentary frontoparietals. D. Approximately same stage as the previous, dorsal view (HUJZ−13132). Scale bars 5 mm.
Figure 5 in Husbandry, captive breeding, larval development and stages of the Malayan horned frog Megophrys nasuta (Schlegel, 1858) (Amphibia: Anura: Megophryidae)
Figure 5. Megophrys nasuta larvae in stages 18 to 22; blue color is caused by the blue cellular material at the aquarium ground / background while taking photographs. Photos: R. Bach, T. Ziegler, D. Karbe.
Figure 2 in Husbandry, captive breeding, larval development and stages of the Malayan horned frog Megophrys nasuta (Schlegel, 1858) (Amphibia: Anura: Megophryidae)
Figure 2. Megophrys nasuta at the amphibian breeding unit at the Cologne Zoo a) calling male, b) couple in ampleXus during egg deposition, c) embryos, and d) hatched larvae with yolk sacs. Photos: D. Karbe, A. Heidrich, T. Ziegler.
Figure 1 in Husbandry, captive breeding, larval development and stages of the Malayan horned frog Megophrys nasuta (Schlegel, 1858) (Amphibia: Anura: Megophryidae)
Figure 1. Megophrys nasuta enclosures in the amphibian breeding unit at the Cologne Zoo: a) terrarium of the adults, b) rearing tank for larvae at early developmental stages, c) aquaria for advanced larval stages, and d) rearing terraria for juveniles. Photos: D. Karbe.
Figure 15 in Morphological evolution in Ceratophryinae frogs (Anura, Neobatrachia): the effects of heterochronic changes during larval development and metamorphosis
Figure 15. Comparison of the changes between the larval and adult body plans during larval development. The horizontal axis represents developmental stages (Gosner, 1960). The curves plotted depict structural modifications, and the grey area represents metamorphic events that take place during the metamorphic climax (stages 42–46) for most anurans. The early occurrence of metamorphic events (predisplacement) is observed in the ceratophryine frogs, especially in Lepidobatrachus spp., that have precocious metamorphosis. Delayed metamorphic events take place in the development of Pseudis platensis, a species in which some morphological changes that imply the end of metamorphosis for most anurans have yet to finish.
Figure 13 in Morphological evolution in Ceratophryinae frogs (Anura, Neobatrachia): the effects of heterochronic changes during larval development and metamorphosis
Figure 13. Variation in structural changes in some external features. A, dorsal view of Lepidobatrachus llanensis at the end of metamorphosis. A small tail stub is present. B, lateral view of the same specimen in (A) showing the angle of the mouth far beyond the posterior margin of the eye. C, dorsal view of Chacophrys pierottii during metamorphosis. The tail has started to reduce. D, lateral view of the same specimen in (C). The disappearance of the caudal fin is advanced, and the angle of the mouth reaches the posterior margin of the eye. E and F, ventral and lateral views of a Pseudis platensis tadpole at the beginning of metamorphosis. The oral disc and keratinized buccal structures are still present, and the forelimbs have emerged, but the anal tube remains well developed. G and H, ventral and lateral views of a P. platensis tadpole during metamorphosis. Larval mouthparts have disappeared; tail regression has started with the reduction of the fins, whereas the disappearance of the anal tube is delayed. I, dorsal view of P. platensis at an advanced metamorphic stage. The tail is conserved and has reduced caudal fins. J, ventral view of the same specimen showing the absence of the anal tube, and features of the mouth that are similar to those present in most anurans at the end of metamorphosis. K, detail in lateral view of the position of the angle of the mouth posterior to the eye.
Figure 12 in Morphological evolution in Ceratophryinae frogs (Anura, Neobatrachia): the effects of heterochronic changes during larval development and metamorphosis
Figure 12. Hematoxylin–eosin cross sections (6-Mm thick) at the diaphyseal level of metatarsal IV in postmetamorphic specimens. Black arrowheads indicate lines of arrested growth (LAGs). A, Lepidobatrachus llanensis, five LAGs male [data for two adult males; 5 ± 1 (SVL 74.5 mm) and 6 ± 1 (SVL 74.1 mm)]. B, Lepidobatrachus laevis, six LAGs female [data for two adult females; 6 ± 1 (SVL 144 mm) and 7 ± 1 (SVL 111 mm)]. C, Chacophrys pierottii, four LAGs male [data for two adult males; 6 ± 1 (SVL 49.9 mm) and 4 ± 1 (SVL 45.2 mm)]. D, Ceratophrys cranwelli, 11 LAGs male [data for three adult males; 14 ± 1 (SVL 84.6 mm), 11 ± 1 (SVL 81 mm), and 13 ± 1 (SVL 74.3 mm)]. E, Pseudis platensis, two LAGs female [data for two adults (female and male); 2 ± 1 (SVL 46 mm) and 3 ± 1 (SVL 44.6 mm)]. F, Telmatobius atacamensis, juvenile specimen, two LAGs [data for an adult male; 5 ± 1 (SVL 45.4 mm) and for the juvenile 2 ± 1 (SVL 45 mm)]. Abbreviations: mc; marrow cavity. Scale bars: 0.05 mm.
Figure 11 in Morphological evolution in Ceratophryinae frogs (Anura, Neobatrachia): the effects of heterochronic changes during larval development and metamorphosis
Figure 11. Mean, maximum, and minimum values of snout–vent lengths (SVLs) in advanced tadpoles (stages 38–41), during metamorphosis (stages 42–46), and in adults. Values of SVL are given in mm. Light-grey areas approximately represent the extension of larval development (LD) in months, and dark-grey areas refer to postmetamorphic growth (PG) in lines of arrested growth (LAGs). Lepidobatrachus llanensis: SVL in tadpoles (N = 15, SVL = 36.7 ± 3.4 mm); SVL of metamorphic specimens (N = 26, SVL = 36.3 ± 5.8 mm); SVL of adults (N = 16, SVL = 76.5 ± 7.5 mm). Larval development takes place over a period of 2 weeks. Postmetamorphic growth estimated in LAGs = 6 years. Lepidobatrachus laevis: SVL in tadpoles (N = 12, SVL = 46.6 ± 2.8 mm); SVL of metamorphic specimens (N = 26, SVL = 49.9 ± 7.8 mm); SVL of adults (N = 13, SVL = 99.2 ± 22.1 mm). Larval development takes over a period of 2 weeks. Postmetamorphic growth estimated in LAGs = 7 years. Chacophrys pierottii: SVL in tadpoles (N = 10, SVL = 46.3 ± 3.9 mm); SVL of metamorphic specimens (N = 28, SVL = 36.3 ± 2.6 mm); SVL of adults (N = 15, SVL = 47.8 ± 2.7 mm). Larval development takes place over a period of 2 weeks. Postmetamorphic growth estimated in LAGs = 6 years. Ceratophrys cranwelli: SVL in tadpoles (N = 8, SVL = 26.3 ± 3.8 mm); SVL of metamorphic specimens (N = 18, SVL = 27.5 ± 4.4 mm); SVL of adults (N = 10, SVL = 91.9 ± 12.7 mm). Larval development takes place over a period of 3 weeks. Postmetamorphic growth estimated in LAGs = 14 years. Pseudis platensis: SVL in tadpoles (N = 9, SVL = 46.3 ± 3.6 mm); SVL of metamorphic specimens (N = 8, SVL = 37.4 ± 2.7 mm); SVL of adults (N = 7, SVL = 45.3 ± 5.0 mm). Larval development takes place over a period of 6 months. Postmetamorphic growth estimated in LAGs = 3 years. Telmatobius atacamensis: SVL in tadpoles (N = 11, SVL = 32.9 ± 3.4 mm); SVL of metamorphic specimens (N = 30, SVL = 31.0 ± 1.8 mm); SVL of adults (N = 2, SVL = 45.2 ± 1.0 mm). Larval development takes place over a period of 8 months. Postmetamorphic growth estimated in LAGs = 5 years.
Figure 14 in Morphological evolution in Ceratophryinae frogs (Anura, Neobatrachia): the effects of heterochronic changes during larval development and metamorphosis
Figure 14. Presence and absence of m. suspensoriohyoideus among selected anuran tadpoles, following the criteria proposed by Haas (2003) at larval stage 37. A, Pseudis platensis. The muscle is absent. B–F, the muscle is present. B, Telmatobius atacamensis. C, Lepidobatrachus laevis. D, Lepidobatrachus llanensis. E, Ceratophrys cranwelli. F, Chacophrys pierottii. The absence of m. suspensoriohyoideus was reported for Ceratophrys ornata, L. laevis (Ruibal & Thomas, 1988; Haas, 2003), and C. cranwelli (Vera Candioti, 2005), but Palavecino (1999) described it in C. ornata and C. cranwelli. Haas (2003) proposed that the absence of m. suspensoriohyoideus is a synapomorphy for the Ceratophrys and Lepidobatrachus clade, and Frost et al. (2006) extended the synapomorphy for Ceratophryini. Our data demonstrate the presence of the m. suspensoriohyoideous in tadpoles of the three genera of Ceratophryinae. Abbreviations: oh, m. orbitohyoideus; sh, m. suspensoriohyoideus. Scale bars: 1 mm.
Figure 9 in Morphological evolution in Ceratophryinae frogs (Anura, Neobatrachia): the effects of heterochronic changes during larval development and metamorphosis
Figure 9. Palmar and plantar views of the autopodia in anurans at the end of metamorphosis, where subarticular turbercles are already well defined. A, Bombina variegata (foot): subarticular tubercles are absent and metatarsal tubercles are poorly developed. B, Bombina variegata (hand): subarticular tubercles are absent. C, Odontophrynus americanus (foot): subarticular tubercles are evident, and the inner metatarsal is not yet keratinized. D, Odontophrynus americanus (hand): subarticular tubercles are strongly developed. E, Pseudis platensis (foot): tubercles are absent and the inner metatarsal tubercle is defined. F, Pseudis platensis (hand): small subarticular tubercles are evident. G, Telmatobius atacamensis (foot): small subarticular tubercles and the inner metatarsal tubercle are present. H, Telmatobius atacamensis (hand): subarticular tubercles are better defined than in the foot. I, Lepidobatrachus llanensis (foot): subarticular tubercles are absent. The well-developed inner metatarsal tubercle and toe tips are keratinized. J, Lepidobatrachus llanensis (hand): subarticular tubercles are absent. K, Lepidobatrachus laevis (foot): subarticular tubercles are absent, and the inner metatarsal tubercle presents incipient keratinization. L, Lepidobatrachus laevis (hand): subarticular tubercles are absent. M, Ceratophrys cranwellii (foot): small subarticular tubercles are defined, and the inner metatarsal tubercles are poorly keratinized. N, Ceratophrys cranwelli (hand): small subarticular tubercles are present. O, Chacophrys pierottii (foot): subarticular tubercles are not prominent. Inner metatarsal tubercle has keratinization. P, Chacophrys pierottii (hand): subarticular tubercles are well developed. The pattern of distribution of subarticular tubercles is considered as diagnostic in most species, and development of these structures takes place at larval stages 38–40 (Gosner, 1960). Subarticular tubercles in manus and pes are also absent or poorly developed in Xenopus, Hymenochirus, Pipa, Ascaphus, Leiopelma, Alytes, Discoglossus, Madecassophryne, Stumpffia, Rhinoderma, Brachycephalus, Truebella, and Ansonia (Guibé, 1978; Graybeal & Cannatella, 1995; Matsui, Nabhitabhata & Panha, 1998; Pombal & Gasparini, 2006, among others). Scale bar: 0.2 mm.
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