Multiple anti‐predator mechanisms in the red‐spotted Argentina Frog (Amphibia: Hylidae)

Cajade, Rodrigo; Hermida, Gladys N.; Piñeiro, Jose Miguel; Regueira, Eleonora; Alcalde, Leandro; Fusco, Luciano; Marangoni, Federico

doi:10.1111/jzo.12439

Cited by 6 publications

(18 citation statements)

References 24 publications

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“…4, skulls 20 and 21, and refs. [54][55][56]. The remaining phragmotic species are not known to have this adaptation, but also have not been histologically investigated for similar glands.…”

Section: Discussionmentioning

confidence: 99%

Evolution of hyperossification expands skull diversity in frogs

Paluh

Stanley

Blackburn

2020

Proc. Natl. Acad. Sci. U.S.A.

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Frogs (Anura) are one of the most diverse vertebrate orders, comprising more than 7,000 species with a worldwide distribution and extensive ecological diversity. In contrast to other tetrapods, frogs have a highly derived body plan and simplified skull. In many lineages of anurans, increased mineralization has led to hyperossified skulls, but the function of this trait and its relationship with other aspects of head morphology are largely unexplored. Using three-dimensional morphological data from 158 species representing all frog families, we assessed wide-scale patterns of shape variation across all major lineages, reconstructed the evolutionary history of cranial hyperossification across the anuran phylogeny, and tested for relationships between ecology, skull shape, and hyperossification. Although many frogs share a conserved skull shape, several extreme forms have repeatedly evolved that commonly are associated with hyperossification, which has evolved independently more than 25 times. Variation in cranial shape is not explained by phylogenetic relatedness but is correlated with shifts in body size and ecology. The species with highly divergent, hyperossified skulls often have a specialized diet or a unique predator defense mechanism. Thus, the evolution of hyperossification has repeatedly facilitated the expansion of the head into multiple new shapes and functions.Anura | cranium | dermal ornamentation | geometric morphometrics | microcomputed tomography I dentifying the factors that drive evolutionary changes in the heads of vertebrates has been a long-standing challenge because of the difficulties of sampling taxa broadly, quantifying complex morphologies, and identifying possible mechanisms responsible for generating macroevolutionary patterns. The diverse selective pressures proposed to drive extreme derivations in the skull include specializations in feeding biology (1), habitat use (2), and locomotion (3). Sexual selection also is thought to influence head morphology because the skull often is sexually dimorphic in size and shape (4, 5). The interactions among these selective pressures can result in functional trade-offs (6) that shape the head as an integrated system that must house the sensory organs, capture prey, provide protection, and partake in locomotion and reproduction (7). The nonadaptive mechanisms of architectural constraint (i.e., allometry; ref. 8) and phylogenetic conservatism (9) also have been invoked to explain morphological variation within and across lineages, particularly in cases in which extreme shifts are absent. The diversification of the skull usually results from changes in size or shape of preexisting elements or the loss of bones (10), but the origin of novel structures also may be responsible for shifts in morphology (11).Increased mineralization or hyperossification of the skull is a recurrent feature among vertebrates; it also is known as dermal ornamentation (12,13). In its most rudimentary form, additional membrane bone is deposited on the skeleton to form ridges and...

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“…4, skulls 20 and 21, and refs. [54][55][56]. The remaining phragmotic species are not known to have this adaptation, but also have not been histologically investigated for similar glands.…”

Section: Discussionmentioning

confidence: 99%

Evolution of hyperossification expands skull diversity in frogs

Paluh

Stanley

Blackburn

2020

Proc. Natl. Acad. Sci. U.S.A.

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“…The consolidated group, within the Lophyohylinae subfamily, of the genera Aparasphenodon, Argenteohyla, Corythomantis and Nyctimantis, has been the most studied as to their skin characteristics [16,18]. In this sense, cutaneous secretions of the species Aparasphenodon brunoi and Corythomantis greningii have been implicated in reducing water loss [19,20] and also as a defensive mechanism [21,22] as was Argenteohyla siemersi [23].…”

Section: Introductionmentioning

confidence: 99%

“…As described for C. grenningi and A. brunoi [21,22], A. siemersi is considered a truly venomous frog on account of possessing a specific delivery device for its highly lethal skin secretion. This device is formed by dermal bone spines on the surface of the cranial skin associated with the venom glands and is part of a complex combination of several anti-predator mechanisms [23]. Moreover, the high toxicity of this skin secretion is signalized by prominent aposematic coral-reddish spots on several parts of the body [23].…”

Section: Introductionmentioning

confidence: 99%

“…This device is formed by dermal bone spines on the surface of the cranial skin associated with the venom glands and is part of a complex combination of several anti-predator mechanisms [23]. Moreover, the high toxicity of this skin secretion is signalized by prominent aposematic coral-reddish spots on several parts of the body [23].…”

Section: Introductionmentioning

confidence: 99%

“…Recently, Cajade et al [23] determined the lethal dose of A. siemersi skin secretion (4.75 μg/mouse, BALB/c mice). This secretion was demonstrated to be more lethal in comparison with C. greening (69.75 μg/mouse; Swiss white mice), but less lethal than A. brunoi (3.12 μg/mouse, Swiss white mice) [22].…”

Section: Introductionmentioning

confidence: 99%

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Biochemical characterization and cytotoxic effect of the skin secretion from the red-spotted Argentina frog Argenteohyla siemersi (Anura: Hylidae)

Fusco

Cajade

Piñeiro

et al. 2020

J. Venom. Anim. Toxins incl. Trop. Dis

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Background: Argenteohyla siemersi (red-spotted Argentina frog) is a casque-headed tree frog species belonging to the Hylidae family. This species has a complex combination of anti-predator defense mechanisms that include a highly lethal skin secretion. However, biochemical composition and biological effects of this secretion have not yet been studied. Methods: The A. siemersi skin secretion samples were analyzed by mass spectrometry and chromatographic analysis (MALDI-TOF/MS, RP-HPLC and GC-MS). Proteins were also studied by SDS-PAGE. Among the biological activities evaluated, several enzymatic activities (hemolytic, phospholipase A 2 , clotting, proteolytic and amidolytic) were assessed. Furthermore, the cytotoxic activity (cytolysis and fluorescence staining) was evaluated on myoblasts of the C2C12 cell line. Results: The MALDI-TOF/MS analysis identified polypeptides and proteins in the aqueous solution of A. siemersi skin secretion. SDS-PAGE revealed the presence of proteins with molecular masses from 15 to 55 kDa. Steroids, but no alkaloids or peptides (less than 5 kDa), were detected using mass spectrometry. Skin secretion revealed the presence of lipids in methanolic extract, as analyzed by CG-MS. This secretion showed hemolytic and phospholipase A 2 activities, but was devoid of amidolytic, proteolytic or clotting activities. Moreover, dose-dependent cytotoxicity in cultured C2C12 myoblasts of the skin secretion was demonstrated. Morphological analysis, quantification of lactate dehydrogenase release and fluorescence staining indicated that the cell death triggered by this secretion involved necrosis. Conclusions: Results presented herein evidence the biochemical composition and biological effects of A. siemersi skin secretion and contribute to the knowledge on the defense mechanisms of casque-headed frogs.

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