Cross‐ecosystem effects of terrestrial predators link treefrogs, zooplankton, and aquatic primary production

Hite, Jessica L.; Hughey, Myra C.; Warkentin, Karen M.; Vonesh, James R.

doi:10.1002/ecs2.2377

Cited by 11 publications

(16 citation statements)

References 61 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…Across successively finer levels of developmental precision, our results reveal a 456 substantial increase in mechanosensory-cued hatching responses with the development of 457 vestibular function, consistent with a role for this sensory system in mediating the response. In 458 general, the timing of onset of vestibular function is consistent with the onset of escape success 459 in predator attacks (Almanzar and Warkentin, 2018;Hite et al, 2018;Warkentin, 2000;460 Warkentin et al, 2006a). In our vibration playbacks to clutches, no embryos lacking VOR 461 hatched.…”

Section: Ontogenetic Congruence Of Vor and Mechanosensory-cued Hatchimentioning

confidence: 75%

“…In attacks by egg-predatory snakes and wasps, we 121 have never observed hatching before about 2.5 days prematurely. In our Panamanian study 122 population, escape-hatching success is zero at age 3 d, present but relatively low and variable at 123 4 d, and consistently high thereafter, with spontaneous hatching in the evening at 6 d (Almanzar 124 and Warkentin, 2018;Hite et al, 2018;Warkentin, 2000;Warkentin et al, 2006a). In 125…”

Section: Introduction 26 27mentioning

confidence: 76%

“…We performed four experiments to examine the role of vestibular mechanoreception in 423 embryos' risk assessment by comparing the ontogeny of responses at a population level, at a 424 clutch level, and at an individual level. 425 First, at a population level, we found that the developmental onset of the vestibulo-ocular 426 reflex in red-eyed treefrog embryos (individually in series Ia and across clutches in series Ib) is 427 congruent with the documented onset of escape-hatching responses to predator attacks in the 428 Gamboa population of A. callidryas (Almanzar and Warkentin, 2018;Hite et al, 2018;429 Warkentin, 2000;Warkentin et al, 2006a). If the onset of VOR were clearly before or after the 430 developmental period when predator-induced hatching begins in this population of A. callidryas, 431 it would have rejected the hypothesized key role of vestibular system development in enabling 432 the antipredator response.…”

Section: Ontogenetic Congruence Of Vor and Mechanosensory-cued Hatchimentioning

confidence: 82%

See 2 more Smart Citations

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

Jung

Kim

Arias

et al. 2019

Preprint

Self Cite

View full text Add to dashboard Cite

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

show abstract

Section: Ontogenetic Congruence Of Vor and Mechanosensory-cued Hatchimentioning

confidence: 75%

Section: Introduction 26 27mentioning

confidence: 76%

Section: Ontogenetic Congruence Of Vor and Mechanosensory-cued Hatchimentioning

confidence: 82%

See 1 more Smart Citation

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

Jung

Kim

Arias

et al. 2019

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…We tested the effect of gentamicin on jiggling-induced hatching in two later periods to determine if the dependence of MCH on lateral line function changes developmentally. In A. callidryas, embryos hatch spontaneously from 5-7 d, while younger embryos almost never hatch if undisturbed (Güell and Warkentin, 2018;Hite et al, 2018;Warkentin, 2000;Warkentin et al, 2001). From age 4 to 5 d, embryos become more likely to escape during snake and wasp attacks (Gomez-Mestre and Warkentin, 2007;Warkentin, 1995;Warkentin, 2000) and to hatch in vibration playbacks (Jung et al, 2019;Warkentin et al, In press;Warkentin et al, 2019).…”

Section: Hatching-response Test: Manual Egg Jigglingmentioning

confidence: 99%

Multimodal mechanosensing enables treefrog embryos to escape egg-predators

Jung

Rojas

Warkentin

2020

Preprint

Self Cite

View full text Add to dashboard Cite

Mechanosensory-cued hatching (MCH) is widespread, diverse, and improves survival in many animals. From flatworms and insects to frogs and turtles, embryos use mechanosensory cues and signals to inform hatching timing, yet mechanisms mediating mechanosensing in ovo are largely unknown. The arboreal embryos of red-eyed treefrogs, Agalychnis callidryas, hatch prematurely to escape predation, cued by physical disturbance in snake attacks. When otoconial organs in the developing vestibular system become functional, this response strengthens, but its earlier occurrence indicates another sensor must contribute. Post-hatching, tadpoles use lateral line neuromasts to detect water motion. We ablated neuromast function with gentamicin to assess their role in A. callidryas’ hatching response to disturbance. Prior to vestibular function, this nearly eliminated the hatching response to a complex simulated attack cue, egg-jiggling, revealing that neuromasts mediate early MCH. Vestibular function onset increased hatching, independent of neuromast function, indicating young embryos use multiple mechanosensory systems. MCH increased developmentally. All older embryos hatched in response to egg-jiggling, but neuromast function reduced response latency. In contrast, neuromast ablation had no effect on timing or level of hatching in motion-only vibration playbacks. It appears only a subset of egg-disturbance cues stimulate neuromasts; thus embryos in attacked clutches may receive uni- or multimodal stimuli. A. callidryas embryos have more neuromasts than described for any other species at hatching, suggesting precocious sensory development may facilitate MCH. Our findings provide insight into the behavioral roles of two mechanosensory systems in ovo and open possibilities for exploring sensory perception across taxa in early life stages.SUMMARYRed-eyed treefrog embryos use both their lateral line and vestibular systems to sense the disturbance cues in egg-predator attacks that inform escape-hatching decisions.

show abstract

“…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, Vonesh & Warkentin, 2017 ; Warkentin, 1995 ; Warkentin, 2000b ; Warkentin, 2007 ; Warkentin et al, 2017 ; Warkentin, Currie & Rehner, 2001 ). In contrast, undisturbed embryos often remain in the egg for 5–7 d ( Gomez-Mestre & Warkentin, 2007 ; Hite et al, 2018 ; 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, Vonesh & Warkentin, 2017 ; Warkentin, 1995 ; Warkentin, 2000b ; Warkentin, Currie & Rehner, 2001 ).…”

Section: Introductionmentioning

confidence: 99%

When and where to hatch? Red-eyed treefrog embryos use light cues in two contexts

Güell

Warkentin

2018

PeerJ

Self Cite

View full text Add to dashboard Cite

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 they use light as a directional cue. Our results support that A. callidryas embryos use light cues to inform both when and where to hatch. Both the spatial orientation of hatching and the timing of spontaneous hatching may affect fitness and be informed by cues in a broader range of species than is currently appreciated.

show abstract

Cross‐ecosystem effects of terrestrial predators link treefrogs, zooplankton, and aquatic primary production

Cited by 11 publications

References 61 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

Multimodal mechanosensing enables treefrog embryos to escape egg-predators

When and where to hatch? Red-eyed treefrog embryos use light cues in two contexts

Contact Info

Product

Resources

About