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Do developmental changes in fitness trade-offs predict how embryos use mechanosensory cues for escape-hatching decisions?

Poster

Do developmental changes in fitness trade-offs predict how embryos use mechanosensory cues for escape-hatching decisions?

Abstract

When defense is more costly, prey should differentiate more strongly between predator cues and benign stimuli and may therefore use more sources of information. Red-eyed treefrog (Agalychnis callidryas) embryos hatch prematurely to escape from egg-eating snakes and wasps, cued by physical disturbance in attacks. Missing predator cues is always costly, but false alarm costs decrease with development. We assessed developmental changes in how embryos use and combine information from two sensory modalities, using a playback system to present motion (shaking), tactile contact (rubbing), or both cue types to eggs in custom-made trays at two ages. Younger embryos showed a stronger hatching response to bimodal over unimodal cues. This synergistic effect disappeared in older embryos, which responded equally strongly to unimodal and bimodal cues and had a shorter latency to hatch. This indicates younger embryos – facing higher predation risk as tadpoles – use more information for their hatching decisions. We also investigated changes in response to tactile cues (simulated wasp attack) manually applied directly to embryos through the capsule (higher threat) or on the capsule away from embryo (lower threat). Younger embryos hatched faster in response to direct tactile contact than capsule-only contact, whereas older embryos responded equally to both. Both within and across sensory modalities, developmental changes in embryos’ cue use are consistent with ontogenetic adaptation, based on improved survival chances outside the egg. Embryo hatching timing can be crucial for survival, and the cognitive processes underlying their behavioral responses have likely been shaped by developmentally changing selection pressures.
Do developmental changes in fitness trade-offs
predict how embryos use mechanosensory cues for
escape-hatching decisions?
FOUILLOUX, C*1; JUNG, J2; OSPINA, AM3; SNYDER, R4; WARKENTIN, KM2
Background
Methods
1MHNM, Université Cadi Ayyad, Morocco, 2Boston University, USA, 3IAVH, Colombia, 4John Carroll University, USA
Q1. Do embryos use motion cues, tactile cues, or both?
Q2. If both, are modalities redundant or non-redundant?
Q3. Does cue use change developmentally?
Red-eyed treefrog (Agalychnis callidryas) embryos use physical
disturbance in egg-predator attacks to cue escape-hatching.
Missing predator cues is always costly, but false alarm
costs decrease with development.
E3. We applied tactile stimuli manually directly on embryos or indirectly
on the membrane away from the body.
Young embryos treat
direct contact as more
risky than indirect
contact, but older
embryos do not.
Younger embryos require more indication of risk before
hatching, accumulated over time or across modalities.
chloe.a.fouilloux@gmail.com @ChloeFouilloux
Results and Conclusions
and / or
E1-2. We used a playback system to present tactile contact
(rubbing), motion (vibration), or both cues, to embryos.
Escape-hatching response to playbacks. Both modalities elicited hatching. Bimodal stimuli
elicited more hatching than either unimodal stimulus at 4 d embryos, but not at 5 d.
Latency to hatch in playbacks. In both experiments, latency to hatching decreased with age.
in E1 (more ‘scary’ stimulus) younger embryos hatched faster to bimodal cues.
Acknowledgements: This research was supported by the US National Science Foundation,
Boston University, and Smithsonian Tropical Research Institute. Thanks to Team Treefrog for
encouragement and friendship, to Bibiana Rojas and Mohammed Znari for support and guidance,
and to A. callidryas for all the eggs.
E1. ‘scary’ stimulus. E2. moderate stimulus.
1100 Hz
0.5 s noise,
1.5 s silence 1250 Hz
1 s noise, 1 s silence
Latency to hatch in response to localized
tactile stimuli.Both direct and indirect
tactile stimuli elicited hatching. Younger
embryos tolerated a longer period of
indirect stimulation before hatching.
H: Embryos use multiple mechanosensory cues and show
adaptive ontogenetic changes in cue use.
2 TEST AGES: 5 days Midway through hatching period
4 days Near onset of predator-induced hatching
E1 E2
ns
ns
Younger embryos treat motion and tactile stimuli as non-
redundant risk cues; for older embryos they are redundant.
E1 E2
Stimulus P = 0.030
Age P = 0.0059 Age P = 0.016
E3
Age P = 2.352 e-16
Stimulus P = 1.96 e-08
ns
b
aAge P = 0.00015
Stimulus P = 0.0031
Interaction P = 0.0047
Age P: 1.151 e-11
Stimulus P: 0.00025
Interaction P: 0.0001
a
c
b
ns
ns
ns
Conclusion: Embryos use both motion and tactile cues
to assess risk and show adaptive ontogenetic changes
in how they combine information.
b
a
... In motion-only playbacks to individual eggs in trays, hatching responses are typically lower than in playbacks presenting the same vibration pattern as a combination of motion and tactile cues (Figs. 4, 6, and 7 vs. 8) (Fouilloux et al. 2019;Jung et al. 2019Jung et al. , 2020Warkentin et al. 2022); thus we do not directly compare data across tray and tine playbacks. Hatching responses varied across stimuli within the trayplayback experiment (χ 2 = 15.02, ...
Article
Full-text available
Stereotyped signals can be a fast, effective means of communicating danger, but animals assessing predation risk must often use more variable incidental cues. Red eyed-treefrog, Agalychnis callidryas, embryos hatch prematurely to escape from egg predators, cued by vibrations in attacks, but benign rain generates vibrations with overlapping properties. Facing high false-alarm costs, embryos use multiple vibration properties to inform hatching, including temporal pattern elements such as pulse durations and inter-pulse intervals. However, measures of snake and rain vibration as simple pulse-interval patterns are a poor match to embryo behavior. We used vibration playbacks to assess if embryos use a second level of temporal pattern, long gaps within a rhythmic pattern, as indicators of risks. Long vibration-free periods are common during snake attacks but absent from hard rain. Long gaps after a few initial vibrations increase the hatching response to a subsequent vibration series. Moreover, vibration patterns as short as three pulses, separated by long periods of silence, can induce as much hatching as rhythmic pulse series with five times more vibration. Embryos can retain information that increases hatching over at least 45 s of silence. This work highlights that embryo behavior is contextually modulated in complex ways. Identical vibration pulses, pulse groups, and periods of silence can be treated as risk cues in some contexts and not in others. Embryos employ a multi-faceted decision-making process to effectively distinguish between risk cues and benign stimuli.
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