Ureotelism as the prevailing mode of nitrogen excretion in larvae of the marsupial frog Gastrotheca riobambae (Fowler) (Anura, Hylidae)

Alcocer, Iliana; Santacruz, Ximena; Steinbeißer, Herbert; Thierauch, Karl‐Heinz; Pino, Eugenia M. del

doi:10.1016/0300-9629(92)90527-w

Cited by 17 publications

(7 citation statements)

References 16 publications

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“…This is relevant for at least some studies that reported urea in PVF and foam nests during terrestrial development (Alcocer et al, 1992; del Pino et al, 1994; Shoemaker & McClanahan, 1973). Other studies reported an early capacity for urea excretion based on indirect measurements, after initially terrestrial individuals were moved to water (Grafe et al, 2005; Martin & Cooper, 1972; Shoemaker & McClanahan, 1982), or arginase activity was detected in embryonic tissues (Alcocer et al, 1992; Shoemaker & McClanahan, 1982). Nonetheless, arginase can be involved in other biochemical pathways during early development, so activity of rate‐limiting enzymes such as CPS1 is necessary to confirm urea cycle activity (Srivastava & Ratha, 2010).…”

Section: Discussionmentioning

confidence: 84%

“…In frogs, embryonic and larval adaptations, including plastic responses during early development, have been described in response to biotic and abiotic environmental challenges on land (Alcocer et al, 1992 ; Bradford & Seymour, 1985 ; Delia et al, 2014 ; Downie, 1984 ; Seymour & Bradford, 1995 ; Warkentin, 1995 , 2007 ). Plastic responses to common environmental threats during development may help explain repeated evolution of traits among distantly related taxa, via changes in shared underlying mechanisms (Gomez‐Mestre & Buchholz, 2006 ; Ledón‐Rettig et al, 2010 ; Warkentin, 2011 ).…”

Section: Introductionmentioning

confidence: 99%

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Reproductive colonization of land by frogs: Embryos and larvae excrete urea to avoid ammonia toxicity

Narvaez

Warkentin

2022

Ecology and Evolution

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Vertebrate colonization of land has occurred multiple times, including over 50 origins of terrestrial eggs in frogs. Some environmental factors and phenotypic responses that facilitated these transitions are known, but responses to water constraints and risk of ammonia toxicity during early development are poorly understood. We tested if ammonia accumulation and dehydration risk induce a shift from ammonia to urea excretion during early stages of four anurans, from three origins of terrestrial development. We quantified ammonia and urea concentrations during early development on land, under well‐hydrated and dry conditions. Where we found urea excretion, we tested for a plastic increase under dry conditions and with ammonia accumulation in developmental environments. We assessed the potential adaptive role of urea excretion by comparing ammonia tolerance measured in 96h‐LC50 tests with ammonia levels in developmental environments. Ammonia accumulated in foam nests and perivitelline fluid, increasing over development and reaching higher concentrations under dry conditions. All four species showed high ammonia tolerance, compared to fishes and aquatic‐breeding frogs. Both nest‐dwelling larvae of Leptodactylus fragilis and late embryos of Hyalinobatrachium fleischmanni excreted urea, showing a plastic increase under dry conditions. These two species can develop the longest on land and urea excretion appears adaptive, preventing their exposure to potentially lethal levels of ammonia. Neither late embryos of Agalychnis callidryas nor nest‐dwelling larvae of Engystomops pustulosus experienced toxic ammonia levels under dry conditions, and neither excreted urea. Our results suggest that an early onset of urea excretion, its increase under dry conditions, and elevated ammonia tolerance can all help prevent ammonia toxicity during terrestrial development. High ammonia represents a general risk for development which may be exacerbated as climate change increases dehydration risk for terrestrial‐breeding frogs. It may also be a cue that elicits adaptive physiological responses during early development.

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Section: Discussionmentioning

confidence: 84%

Section: Introductionmentioning

confidence: 99%

Reproductive colonization of land by frogs: Embryos and larvae excrete urea to avoid ammonia toxicity

Narvaez

Warkentin

2022

Ecology and Evolution

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“…Another component of fetal adaptation in G. riobambae , and presumably all members of the genus, is that embryos in the pouch excrete urea, as do free‐living tadpoles following birth (Alcocer et al, ). Typically, embryos and aquatic tadpoles excrete mostly ammonia, but acquire full ureotely at metamorphosis (Balinsky, ).…”

Section: Back‐brooding In Frogsmentioning

confidence: 99%

“…In G. riobambae , fluid surrounding embryos in the pouch had very high concentrations of urea, and that in the blood of pregnant and nonpregnant females and males lower concentrations, but present in all samples. Further, activity of arginase, a key enzyme in the ureotelic cycle, increased as embryos advanced in development (see Alcocer et al, ). Ureotely is maintained during both the 3‐month pouch period, the 2–12 months tadpole phase in water before metamorphosis, and in adulthood.…”

Section: Back‐brooding In Frogsmentioning

confidence: 99%

Fetal adaptations for viviparity in amphibians

Wake

2014

Journal of Morphology

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Live-bearing has evolved in all three orders of amphibians-frogs, salamanders, and caecilians. Developing young may be either yolk dependent, or maternal nutrients may be supplied after yolk is resorbed, depending on the species. Among frogs, embryos in two distantly related lineages develop in the skin of the maternal parents' backs; they are born either as advanced larvae or fully metamorphosed froglets, depending on the species. In other frogs, and in salamanders and caecilians, viviparity is intraoviductal; one lineage of salamanders includes species that are yolk dependent and born either as larvae or metamorphs, or that practice cannibalism and are born as metamorphs. Live-bearing caecilians all, so far as is known, exhaust yolk before hatching and mothers provide nutrients during the rest of the relatively long gestation period. The developing young that have maternal nutrition have a number of heterochronic changes, such as precocious development of the feeding apparatus and the gut. Furthermore, several of the fetal adaptations, such as a specialized dentition and a prolonged metamorphosis, are homoplasious and present in members of two or all three of the amphibian orders. At the same time, we know little about the developmental and functional bases for fetal adaptations, and less about the factors that drive their evolution and facilitate their maintenance. J.

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“…Nitrogen waste excretion was changed to ureotelic in G. riobambae embryos and tadpoles 105. Ureotelism is an adaptation for prolonged incubation in the maternal pouch of G. riobambae and favors development with limited water 105. Embryos can be cultured in vitro in a physiological saline solution that contains urea 106.…”

Section: Developmental Adaptations In Frogsmentioning

confidence: 99%

Developmental diversity of amphibians

Elinson

Pino

2011

WIREs Developmental Biology

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The current model amphibian, Xenopus laevis, develops rapidly in water to a tadpole which metamorphoses into a frog. Many amphibians deviate from the X. laevis developmental pattern. Among other adaptations, their embryos develop in foam nests on land or in pouches on their mother’s back or on a leaf guarded by a parent. The diversity of developmental patterns includes multinucleated oogenesis, lack of RNA localization, huge non-pigmented eggs, and asynchronous, irregular early cleavages. Variations in patterns of gastrulation highlight the modularity of this critical developmental period. Many species have eliminated the larva or tadpole and directly develop to the adult. The wealth of developmental diversity among amphibians coupled with the wealth of mechanistic information from X. laevis permit comparisons that provide deeper insights into developmental processes.

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Ureotelism as the prevailing mode of nitrogen excretion in larvae of the marsupial frog Gastrotheca riobambae (Fowler) (Anura, Hylidae)

Cited by 17 publications

References 16 publications

Reproductive colonization of land by frogs: Embryos and larvae excrete urea to avoid ammonia toxicity

Reproductive colonization of land by frogs: Embryos and larvae excrete urea to avoid ammonia toxicity

Fetal adaptations for viviparity in amphibians

Developmental diversity of amphibians

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