Developmental onset of escape-hatching responses in red-eyed treefrogs depends on cue type

Warkentin, Karen M.; Diaz, Juliana Cuccaro; Güell, Brandon A.; Jung, Julie; Kim, Su J.; Cohen, Kristina L.

doi:10.1016/j.anbehav.2017.05.008

Cited by 33 publications

(64 citation statements)

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“…Most clutches are laid between 10 pm and 2 am, so we assign embryos to daily 161 age-classes and report developmental timing starting from midnight of their oviposition night 162 (Warkentin, 2002;Warkentin et al, 2005). Across the onset of hatching competence, tested 163 individuals were staged based on morphological markers described in Warkentin et al (2017). University Engineering Products Innovation Center).…”

Section: Egg Clutch Collection and Care 152mentioning

confidence: 99%

“…We measured VOR of 3 276 additional hatchlings that hatched in response to either manual stimulation or hypoxia, but not 277 vibration playback; numbers of manually-stimulated and hypoxia-cued hatchings tested for VOR 278 varied among clutches (total of 3, unless fewer remained after playback). We staged all VOR-279 tested hatchlings (N = 143 hatchlings total) from their frontal photos following a staging system 280 adapted from Warkentin et al (2017) (Fig. 3).…”

Section: Vor and Hatching Response In Vibration Playback To Wholementioning

confidence: 99%

“…When we began this work, we knew that hatching ability does not limit the onset of 417 hatching responses to predator cues, because younger embryos demonstrate hatching competence 418 in response to strong hypoxia (Cohen et al, 2019;Warkentin et al, 2017). Moreover, the rapid 419 developmental increase in hatching response to egg-jiggling -contrasted with the much slower 420 developmental decrease in the costs of early hatching -suggests that some sensory constraint 421 imposes a developmental limit on the onset of the anti-predator response (Warkentin et al, 422 2017).…”

Section: Ontogenetic Congruence Of Vor and Mechanosensory-cued Hatchimentioning

confidence: 99%

“…Specifically, there is a 83 period of development when embryos are competent to hatch, as demonstrated by their 84 consistent hatching response to strong hypoxia and the presence of hatching gland cells, yet still 85 unresponsive to mechanosensory disturbance cues or natural predators (Cohen et al, 2019;86 Warkentin et al, 2017). Up to 10% of eggs laid can be consumed during this period Mestre and Warkentin, 2007;Warkentin, 1995;Warkentin, 2000;Warkentin et al, 2017), 88…”

Section: Introduction 26 27mentioning

confidence: 99%

“…Staging traits are adapted fromWarkentin et al (2017) and all visible in frontal view. 641 (A) Stage 2 -Melanophores extend at least halfway down sides over yolk.…”

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confidence: 99%

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How do red-eyed treefrog embryos sense motion in predator attacks? Assessing the role of vestibular mechanoreception

Jung

Kim

Arias

et al. 2019

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Red-eyed treefrogs' hatching responses to predator attacks, vibration playbacks, and egg-jiggling 1 appear when vestibular function develops. Ear development may be a key limiting factor in the 2 onset of mechanosensory-cued hatching. 3 ABSTRACT 4 5The widespread ability to alter hatching timing in response to environmental cues can 6 serve as a defense against threats to eggs. Arboreal embryos of red-eyed treefrogs, Agalychnis 7 callidryas, hatch up to 30% prematurely to escape predation. This escape-hatching response is 8 cued by physical disturbance of eggs during attacks, including vibrations or motion, and thus 9 depends critically on mechanosensory ability. Predator-induced hatching appears later in 10 development than flooding-induced, hypoxia-cued hatching; thus, its onset is not constrained by 11 the development of hatching ability. It may, instead, reflect the development of mechanosensor 12 function. We hypothesize that vestibular mechanoreception mediates escape-hatching in snake 13 attacks, and that the developmental period when hatching-competent embryos fail to flee from 14 snakes reflects a sensory constraint. We assessed the ontogenetic congruence of escape-hatching 15 responses and an indicator of vestibular function, the vestibulo-ocular reflex (VOR), in three 16ways. First, we measured VOR in two developmental series of embryos 3-7 days old to compare 17 with the published ontogeny of escape success in attacks. Second, during the period of greatest 18 variation in VOR and escape success, we compared hatching responses and VOR across 19 sibships. Finally, in developmental series, we compared the response of individual embryos to a 20 simulated attack cue with their VOR. The onset of VOR and hatching responses were largely 21 concurrent at all three scales. Moreover, latency to hatch in simulated attacks decreased with 22 increasing VOR. These results are consistent with a key role of the vestibular system in the 23 escape-hatching response of A. callidryas embryos to attacks. 24 25

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Section: Egg Clutch Collection and Care 152mentioning

confidence: 99%

Section: Vor and Hatching Response In Vibration Playback To Wholementioning

confidence: 99%

Section: Ontogenetic Congruence Of Vor and Mechanosensory-cued Hatchimentioning

confidence: 99%

Section: Introduction 26 27mentioning

confidence: 99%

“…Staging traits are adapted fromWarkentin et al (2017) and all visible in frontal view. 641 (A) Stage 2 -Melanophores extend at least halfway down sides over yolk.…”

mentioning

confidence: 99%

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How do red-eyed treefrog embryos sense motion in predator attacks? Assessing the role of vestibular mechanoreception

Jung

Kim

Arias

et al. 2019

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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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Elevated ammonia cues hatching in red‐eyed treefrogs: A mechanism for escape from drying eggs

Lisondro‐Arosemena,

Salazar‐Nicholls,

Warkentin

2024

J Exp Zool Pt B

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Egg dehydration can kill terrestrial frog embryos, and this threat is increasing with climate change and deforestation. In several lineages that independently evolved terrestrial eggs, and retained aquatic tadpoles, embryos accelerate hatching to escape from drying eggs, entering the water earlier and less developed. However, the cues that stimulate drying‐induced early hatching are unknown. Ammonia is a toxic, water‐soluble metabolic waste that accumulates within eggs as embryos develop and concentrates as eggs dehydrate. Thus, increasing ammonia concentration may be a direct threat to embryos in drying eggs. We hypothesized that it could serve as a cue, stimulating embryos to hatch and escape. The embryos of red‐eyed treefrogs, Agalychnis callidryas, hatch early to escape from many threats, including dehydration, and are known to use mechanosensory, hypoxia, and light cues. To test if they also use high ammonia as a cue to hatch, we exposed stage‐matched pairs of hatching‐competent, well‐hydrated sibling embryos to ammonia and control solutions in shallow water baths and recorded their behavior. Control embryos remained unhatched while ammonia‐exposed embryos showed a rapid, strong hatching response; 95% hatched, on average in under 15 min. This demonstrates that elevated ammonia can serve as a hatching cue for A. callidryas embryos. This finding is a key step in understanding the mechanisms that enable terrestrial frog embryos to escape from egg drying, opening new possibilities for integrative and comparative studies on this growing threat.

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Developmental onset of escape-hatching responses in red-eyed treefrogs depends on cue type

Cited by 33 publications

References 58 publications

How do red-eyed treefrog embryos sense motion in predator attacks? Assessing the role of vestibular mechanoreception

How do red-eyed treefrog embryos sense motion in predator attacks? Assessing the role of vestibular mechanoreception

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

Elevated ammonia cues hatching in red‐eyed treefrogs: A mechanism for escape from drying eggs

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