Egg clutch dehydration induces early hatching in red-eyed treefrogs, <i>Agalychnis callidryas</i>

Salica, María José; Vonesh, James R.; Warkentin, Karen M.

doi:10.7717/peerj.3549

Cited by 25 publications

(38 citation statements)

References 36 publications

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“…In general, variation in temperature and humidity can influence the hatching timing of amphibians via effects on development rate (Duellman & Trueb 1986;Seymour & Bradford 1995). In A. callidryas these variables may also directly affect embryos' hatching decisions; both drying and heating can induce hatching (Salica et al 2017). For instance, during the warm El Niño conditions in 2015, embryos in our laboratory developed faster and hatched earlier than in other years (see Warkentin et al 2017).…”

Section: Hatching Timing Experimentsmentioning

confidence: 85%

“…Their hatching is a rapid process, involving enzyme release and exit behavior, that embryos may perform at any point across a broad developmental period; the actual hatching timing of individual embryos depends on their behavioral decision (Cohen et al 2016;Warkentin et al 2017). Embryos exposed to predator attack, flooding, fungal infection, or dehydration can hatch rapidly to escape, starting as early as 3 or 4 days of age (Salica et al 2017;Warkentin 1995;Warkentin 2000b;Warkentin 2007;Warkentin et al 2017;Warkentin et al 2001). In contrast, undisturbed embryos often remain in the egg for 5-7 d (Gomez-Mestre & Warkentin 2007;Hite et al in press;Warkentin 1995;Warkentin 2000b).…”

Section: Introductionmentioning

confidence: 99%

“…In contrast, undisturbed embryos often remain in the egg for 5-7 d (Gomez-Mestre & Warkentin 2007;Hite et al in press;Warkentin 1995;Warkentin 2000b). Undisturbed egg clutches, and those facing the chronic threat of fungus or drying, tend to hatch gradually, often taking over 24 h for all eggs to hatch, while embryos facing immediate threats in attacked clutches may hatch synchronously, within minutes of each other (Salica et al 2017;Warkentin 1995;Warkentin 2000b;Warkentin et al 2001). Aquatic predator communities in A. callidryas breeding ponds vary substantially; however, hatchlings often face visually hunting insects or fishes (Touchon & Vonesh 2016).…”

Section: Introductionmentioning

confidence: 99%

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Peer Review #1 of "When and where to hatch? Red-eyed treefrog embryos use light cues in two contexts (v0.1)"

2018

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Hatching timing is under strong selection and environmentally cued in many species. Embryos use multiple sensory modalities to inform hatching timing and many have spontaneous hatching patterns adaptively synchronized to natural cycles. Embryos can also adaptively shift their hatching timing in response to environmental cues indicating immediate threats or opportunities. Such cued shifts in hatching are widespread among amphibians; however, we know little about what, if anything, regulates their spontaneous hatching. Moreover, in addition to selection on hatching timing, embryos may experience benefits or suffer costs due to the spatial orientation of hatching. Amphibian eggs generally lack internal constraints on hatching direction but embryos might, nonetheless, use external cues to inform hatching orientation. The terrestrial embryos of red-eyed treefrogs, Agalychnis callidryas, hatch rapidly and prematurely in response to vibrational cues in egg-predator attacks and hypoxia if flooded. Here we examined A. callidryas' use of light cues in hatching timing and orientation. To assess patterns of spontaneous hatching and the role of light cues in their diel timing, we recorded hatching times for siblings distributed across three light environments: continuous light, continuous dark, and a 12L:12D photoperiod. Under a natural photoperiod, embryos showed a clear diel pattern of synchronous hatching shortly after nightfall. Hatching was desynchronized in both continuous light and continuous darkness. It was also delayed by continuous light, but not accelerated by continuous dark, suggesting the onset of dark serves as a hatching cue. We examined hatching orientation and light as a potential directional cue for flooded embryos. Embryos flooded in their clutches almost always hatched toward open water, whereas individual eggs flooded in glass cups often failed to do so, suggesting the natural context provides a directional cue. To test if flooded embryos orient hatching toward light, we placed individual eggs in tubes with one end illuminated and the other dark, then flooded them and recorded hatching direction. Most embryos hatched toward the light, suggesting

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Section: Hatching Timing Experimentsmentioning

confidence: 85%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Peer Review #1 of "When and where to hatch? Red-eyed treefrog embryos use light cues in two contexts (v0.1)"

2018

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“…Embryos can hatch within seconds by rapidly releasing hatching enzymes to digest a small hole 78 in the membrane, then squeezing through it (Cohen et al, 2016). Embryos also hatch 79 prematurely in response to flooding, cued by hypoxia (Warkentin, 2002), and drying, based on 80 unknown cues (Salica et al, 2017). 81…”

Section: Introduction 26 27mentioning

confidence: 99%

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

Jung

Kim

Arias

et al. 2019

Preprint

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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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“…It lays eggs on vegetation over ponds; undisturbed eggs hatch after 6 or 7 days, and the tadpoles drop into the water. These embryos can, however, hatch up to 30% early to escape from numerous threats, including pathogenic fungus (Warkentin et al, 2001), flooding (Warkentin, 2002), dehydration (Salica et al, 2012) and predators such as egg-eating snakes and wasps (Warkentin, 1995(Warkentin, , 2000. Hatching early incurs a trade-off; early hatchlings are less developed and more vulnerable to aquatic predators compared with older hatchlings (Touchon et al, 2013;Warkentin, 1995Warkentin, , 1999aWillink et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

How embryos escape from danger: the mechanism of rapid, plastic hatching in red-eyed treefrogs

Cohen

Seid

Warkentin

2016

Journal of Experimental Biology

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Environmentally cued hatching allows embryos to escape dangers and exploit new opportunities. Such adaptive responses require a flexibly regulated hatching mechanism sufficiently fast to meet relevant challenges. Anurans show widespread, diverse cued hatching responses, but their described hatching mechanisms are slow, and regulation of timing is unknown. Arboreal embryos of redeyed treefrogs, Agalychnis callidryas, escape from snake attacks and other threats by very rapid premature hatching. We used videography, manipulation of hatching embryos and electron microscopy to investigate their hatching mechanism. High-speed video revealed three stages of the hatching process: pre-rupture shaking and gaping, vitelline membrane rupture near the snout, and muscular thrashing to exit through the hole. Hatching took 6.5-49 s. We hypothesized membrane rupture to be enzymatic, with hatching enzyme released from the snout during shaking. To test this, we displaced hatching embryos to move their snout from its location during shaking. The membrane ruptured at the original snout position and embryos became trapped in collapsed capsules; they either moved repeatedly to relocate the hole or shook again and made a second hole to exit. Electron microscopy revealed that hatching glands are densely concentrated on the snout and absent elsewhere. They are full of vesicles in embryos and release most of their contents rapidly at hatching. Agalychnis callidryas' hatching mechanism contrasts with the slow process described in anurans to date and exemplifies one way in which embryos can achieve rapid, flexibly timed hatching to escape from acute threats. Other amphibians with cued hatching may also have novel hatching mechanisms.

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Egg clutch dehydration induces early hatching in red-eyed treefrogs, Agalychnis callidryas

Cited by 25 publications

References 36 publications

Peer Review #1 of "When and where to hatch? Red-eyed treefrog embryos use light cues in two contexts (v0.1)"

Peer Review #1 of "When and where to hatch? Red-eyed treefrog embryos use light cues in two contexts (v0.1)"

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

How embryos escape from danger: the mechanism of rapid, plastic hatching in red-eyed treefrogs

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