{"title":"Egg-clutch Biomechanics Affect Escape-Hatching Behavior And Performance","authors":"B. A. Güell, J. G. McDaniel, K. Warkentin","doi":"10.1093/iob/obae006","DOIUrl":null,"url":null,"abstract":"\n Arboreal embryos of phyllomedusine treefrogs hatch prematurely to escape snake predation, cued by vibrations in their egg clutches during attacks. However, escape success varies between species, from ∼77% in Agalychnis callidryas to just ∼9% in A. spurrelli at 1 day premature. Both species begin responding to snake attacks at similar developmental stages, when vestibular mechanosensory function begins, suggesting that sensory ability does not limit the hatching response in A. spurrelli. Agalychnis callidryas clutches are thick and gelatinous, while A. spurrelli clutches are thinner and stiffer. We hypothesized that this structural difference alters the egg motion excited by attacks. Since vibrations excited by snakes must propagate through clutches to reach embryos, we hypothesized that the species difference in attack-induced hatching may reflect effects of clutch biomechanics on the cues available to embryos. Mechanics predicts that thinner, stiffer structures have higher free vibration frequencies, greater spatial attenuation, and faster vibration damping than thicker, more flexible structures. We assessed clutch biomechanics by embedding small accelerometers in clutches of both species and recording vibrations during standardized excitation tests at two distances from the accelerometer. Analyses of recorded vibrations showed that A. spurrelli clutches have higher free vibration frequencies and greater vibration damping than A. callidryas clutches. Higher frequencies elicit less hatching in A. callidryas, and greater damping could reduce the amount of vibration embryos can perceive. To directly test if clutch structure affects escape success in snake attacks, we transplanted A. spurrelli eggs into A. callidryas clutches and compared their escape rates with untransplanted, age-matched conspecific controls. We also performed reciprocal transplantation of eggs between pairs of A. callidryas clutches as a method control. Transplanting A. spurrelli embryos into A. callidryas clutches nearly tripled their escape success (44%) compared to conspecific controls (15%), whereas transplanting A. callidryas embryos into different A. callidryas clutches only increased escape success by 10%. At hatching competence, A. callidryas eggs are no longer jelly-encapsulated, while A. spurrelli eggs retain their jelly coat. Therefore, we compared the hatching response and latency of A. spurrelli in de-jellied eggs and their control, jelly-encapsulated siblings using manual egg-jiggling to simulate predation cues. Embryos in de-jellied eggs were more likely to hatch and hatched faster than control siblings. Together, our results suggest that the properties of parentally produced egg-clutch structures, including their vibration biomechanics, constrain the information available to A. spurrelli embryos and contribute to interspecific differences in hatching responses to predator attacks.","PeriodicalId":13666,"journal":{"name":"Integrative Organismal Biology","volume":null,"pages":null},"PeriodicalIF":2.2000,"publicationDate":"2024-03-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Integrative Organismal Biology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1093/iob/obae006","RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"BIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Arboreal embryos of phyllomedusine treefrogs hatch prematurely to escape snake predation, cued by vibrations in their egg clutches during attacks. However, escape success varies between species, from ∼77% in Agalychnis callidryas to just ∼9% in A. spurrelli at 1 day premature. Both species begin responding to snake attacks at similar developmental stages, when vestibular mechanosensory function begins, suggesting that sensory ability does not limit the hatching response in A. spurrelli. Agalychnis callidryas clutches are thick and gelatinous, while A. spurrelli clutches are thinner and stiffer. We hypothesized that this structural difference alters the egg motion excited by attacks. Since vibrations excited by snakes must propagate through clutches to reach embryos, we hypothesized that the species difference in attack-induced hatching may reflect effects of clutch biomechanics on the cues available to embryos. Mechanics predicts that thinner, stiffer structures have higher free vibration frequencies, greater spatial attenuation, and faster vibration damping than thicker, more flexible structures. We assessed clutch biomechanics by embedding small accelerometers in clutches of both species and recording vibrations during standardized excitation tests at two distances from the accelerometer. Analyses of recorded vibrations showed that A. spurrelli clutches have higher free vibration frequencies and greater vibration damping than A. callidryas clutches. Higher frequencies elicit less hatching in A. callidryas, and greater damping could reduce the amount of vibration embryos can perceive. To directly test if clutch structure affects escape success in snake attacks, we transplanted A. spurrelli eggs into A. callidryas clutches and compared their escape rates with untransplanted, age-matched conspecific controls. We also performed reciprocal transplantation of eggs between pairs of A. callidryas clutches as a method control. Transplanting A. spurrelli embryos into A. callidryas clutches nearly tripled their escape success (44%) compared to conspecific controls (15%), whereas transplanting A. callidryas embryos into different A. callidryas clutches only increased escape success by 10%. At hatching competence, A. callidryas eggs are no longer jelly-encapsulated, while A. spurrelli eggs retain their jelly coat. Therefore, we compared the hatching response and latency of A. spurrelli in de-jellied eggs and their control, jelly-encapsulated siblings using manual egg-jiggling to simulate predation cues. Embryos in de-jellied eggs were more likely to hatch and hatched faster than control siblings. Together, our results suggest that the properties of parentally produced egg-clutch structures, including their vibration biomechanics, constrain the information available to A. spurrelli embryos and contribute to interspecific differences in hatching responses to predator attacks.
树蛙的树栖胚胎会过早孵化,以躲避蛇的捕食。然而,不同物种的逃生成功率不同,早产1天的Agalychnis callidryas的成功率为77%,而A. spurrelli的成功率仅为9%。这两个物种在相似的发育阶段就开始对蛇的攻击做出反应,此时前庭机械感觉功能开始起作用,这表明感觉能力并不限制马刺鱼的孵化反应。Agalychnis callidryas的胎衣厚而呈胶状,而A. spurrelli的胎衣薄而坚硬。我们推测,这种结构上的差异会改变攻击所激发的卵的运动。由于蛇激发的振动必须通过卵巢传播才能到达胚胎,我们假设攻击诱导孵化的物种差异可能反映了卵巢生物力学对胚胎可用线索的影响。根据力学预测,与更厚、更灵活的结构相比,更薄、更硬的结构具有更高的自由振动频率、更大的空间衰减和更快的振动阻尼。我们将小型加速度计嵌入两个物种的卵巢中,在离加速度计两个距离处进行标准化激励测试时记录振动,以此评估卵巢的生物力学。对记录到的振动进行分析表明,马刺秧鸡卵巢的自由振动频率比马刺秧鸡卵巢高,振动阻尼也比马刺秧鸡卵巢大。较高的频率会减少马氏杓鹬的孵化率,而较大的阻尼会减少胚胎可感知的振动量。为了直接检验蛇攻击中的卵窝结构是否会影响逃生成功率,我们将马刺蓟马卵移植到马刺蓟马卵窝中,并将它们的逃生率与未移植的、年龄匹配的同种对照组进行比较。作为对照方法,我们还在一对 A. callidryas 卵之间进行了卵的相互移植。与同种对照组(15%)相比,将 A. spurrelli 胚胎移植到 A. callidryas 卵中的逃逸成功率(44%)提高了近三倍,而将 A. callidryas 胚胎移植到不同的 A. callidryas 卵中的逃逸成功率仅提高了 10%。在孵化能力方面,A. callidryas卵不再被胶冻包裹,而A. spurrelli卵则保留了胶冻外衣。因此,我们使用人工抖动卵子来模拟捕食线索,比较了去胶冻卵中的马氏刺蓟马和对照组胶冻包裹卵中的马氏刺蓟马的孵化反应和潜伏期。去胶冻卵中的胚胎比对照卵中的胚胎更容易孵化,孵化速度也更快。总之,我们的研究结果表明,亲本生产的卵离合器结构的特性(包括其振动生物力学)限制了马刺秧鸡胚胎可获得的信息,并导致了对捕食者攻击的孵化反应的种间差异。