Biology subjects

Warkentin, K. M.

Publications and source records attributed to Warkentin, K. M..

4 recordsLinked to original sources

bioRxiv2024

The role of vibration amplitude in the escape hatching response of red-eyed treefrog embryos

The function and adaptive significance of defensive behaviors depend on the contexts in which they naturally occur. Amplitude properties of predator cues are widely used by prey to assess predation risk, yet rarely studied in the context of the stimuli relevant to defensive decisions in nature. Red-eyed treefrog embryos, Agalychnis callidryas, hatch precociously in response to attacks on their arboreal egg clutches by snakes and wasps. They use vibrations excited during attacks to detect predators, but wind and rainstorms also excite intense vibrations. Past work has demonstrated that to avoid costly decision errors, A. callidryas non-redundantly combine information from the temporal and frequency properties of clutch vibrations. Here we demonstrate that embryos also use absolute amplitude and fine-scale amplitude modulation information to refine their hatching decision. We used vibration recordings to characterize the amplitude properties of the most common predator and benign-source disturbances to A. callidryas egg clutches in nature and tested whether embryos at three ages across the onset of mechanosensory-cued hatching (4-6 days) respond to amplitude variation during playback of synthetic vibrations to eggs. Older embryos responded to much lower-amplitude vibrations, reflecting a >88-fold decrease in response threshold from 4 to 5 days. To assess how embryos combine amplitude with other vibration properties, we played embryos recorded exemplars of snake attack and rain vibrations of varying amplitudes and patterns of amplitude modulation. The amplitude response curve was steeper for snake recordings than for rain. While amplitude information alone is insufficient to discriminate predator attack from benign-source vibrations, A. callidryas employ an impressively complex strategy combining absolute amplitude, amplitude modulation, temporal, and frequency information for their hatching decision.

developmental biology↗

bioRxiv2022

Ontogeny of risk assessment and escape-hatching performance by red-eyed treefrog embryos in two threat contexts

Arboreal embryos of red-eyed treefrogs, Agalychnis callidryas, hatch prematurely in response to hypoxia when flooded and mechanosensory cues (MC) in snake attacks, but hatching later improves tadpole survival. We studied ontogenetic changes in risk assessment and hatching performance of embryos in response to flooding and physical disturbance. We hypothesized that risk assessment decreases as hatchling survival improves and hatching performance increases as embryos develop. Because snakes eat faster than embryos asphyxiate, we hypothesized that embryos decide to hatch sooner and hatch faster in response to MC. We video-recorded individual embryos hatching in response to each cue type, then compared the incidence and timing of a series of events and behaviors from cue onset to complete hatching across ages and stimuli. Latency from cue to hatching decreased developmentally in both contexts and was shorter with MC, but the elements contributing to those changes differed. Hypoxia-assessment involved position changes, which decreased developmentally along with assessment time. MC-assessment was passive, faster, and also decreased with age. The first stages of hatching, membrane rupture and head emergence, were surprisingly age-independent but faster with MC, congruent with greater effort under more immediate risk. In contrast, body emergence and compression showed ontogenetic improvement consistent with morphological constraints but no cue effect. Both appropriate timing and effective performance of hatching are necessary for continued development. Different stages of the process vary with development and environmental context, suggesting combinations of adaptive context- and stage-dependent behavior, cue-related constraints on information acquisition, and ontogenetic constraints on elements of performance. Summary statementDevelopment reduces risk assessment and improves hatching performance by red-eyed treefrog embryos in both flooding and simulated attacks. Predation cues elicit faster decisions and hatching, congruent with more immediate risk.

animal behavior and cognition↗

bioRxiv2020

Multimodal mechanosensing enables treefrog embryos to escape egg-predators

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.

developmental biology↗

bioRxiv2019

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

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

developmental biology↗