Abstract
Phyllomedusid treefrogs hatch prematurely to escape egg predation, but escape success varies among species. Snake attacks elicited 55% less escape hatching in spontaneously hatching Agalychnis spurrelli than in less developed A. callidryas. Agalychnis callidryas use their vestibular system and, secondarily, their lateral line to sense physical disturbances that cue hatching. Since A. spurrelli develop faster, we hypothesized that heterochronic shifts in the onset timing of vestibular mechanosensory function, relative to hatching ability, might explain their lower escape response to mechanosensory cues. To test this, we compared onset timings of hypoxia- and mechanosensory-cued hatching (MCH) and vestibular mechanosensory function in developmental series of both species. Across species, most sibships began responding to each cue at the same developmental stage and vestibular function development, measured by the vestibulo-ocular reflex (VOR), was similar. These results demonstrate that low escape-hatching success in A. spurrelli is not caused by a delay in the onset of vestibular mechanosensory function. MCH onset in A. spurrelli was associated with VOR, but with a higher threshold than in A. callidryas. The absence of MCH before strong vestibular function suggests multimodal mechanosensing may not contribute to antipredator responses of A. spurrelli embryos. Our observations of higher escape success of larger clutches in snake attacks and hatching complications in flooded A. spurrelli suggest that differences in clutch and egg capsule structure may contribute directly to species differences in escape-hatching success. Moreover, hatching complications in A. spurrelli may select against false alarms, increasing the stringency of hatching decision rules.
Significance statement
Hatching is an essential life-stage transition during development. For some species, it also functions as an effective defense against egg-stage risks. However, the causes for variation in environmentally cued hatching responses are poorly understood. We assessed why two closely related treefrogs exhibit different escape-hatching responses to snake attacks. Comparing the onset of induced-hatching responses and vestibular function in Agalychnis callidryas and A. spurrelli revealed that the primary mechanism for mechanosensing and its developmental timing are conserved within this group, but the sensory function threshold for behavioral response differs. It also revealed that egg-clutch properties, including egg-clutch size and individual egg structure, affect the escape-hatching response. This motivates further research assessing the role of egg-clutch properties and their biomechanics in embryo escape-hatching responses.
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Data availability
The data collected for and analyzed in this paper is available on Dryad at https://doi.org/https://doi.org/10.5061/dryad.cnp5hqc8x.
References
Alberch P, Gould SJ, Oster GF, Wake DB (1979) Size and shape in ontogeny and phylogeny. Paleobiology 5:296–317. https://doi.org/10.1017/S0094837300006588
Almanazar A, Warkentin KM (2018) How development changes escape-hatching success in snake attacks: a video analysis of red-eyed treefrog embryo behavior and performance. Integr Comp Biol 58:E267. https://doi.org/10.1093/icb/icy002
Barrio-Amorós CL (2019) On the taxonomy of snakes in the genus Leptodeira, with an emphasis on Costa Rican species. Reptil Amphib 26:1–15. https://doi.org/10.17161/randa.v26i1.14321
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using {lme4}. J Stat Softw 67:1–48. https://doi.org/10.48550/arXiv.1406.5823
Bland A (2013) The husbandry and captive reproduction of the gliding leaf frog Agalychnis spurrelli (Boulenger 1913). Herpetol Bull 124:9–12
Caldwell MS, McDaniel JG, Warkentin KM (2009) Frequency information in the vibration-cued escape hatching of red-eyed treefrogs. J Exp Biol 212:566–575. https://doi.org/10.1242/jeb.026518
Caldwell MS, McDaniel JG, Warkentin KM (2010) Is it safe? Red-eyed treefrog embryos assessing predation risk use two features of rain vibrations to avoid false alarms. Anim Behav 79:255–260. https://doi.org/10.1016/j.anbehav.2009.11.005
Dall SR, Giraldeau L-A, Olsson O, McNamara JM, Stephens DW (2005) Information and its use by animals in evolutionary ecology. Trends Ecol Evol 20:187–193. https://doi.org/10.1016/j.tree.2005.01.010
Delia JR, Ramirez-Bautista A, Summers K (2014) Glassfrog embryos hatch early after parental desertion. Proc R Soc B 281:20133237. https://doi.org/10.1098/rspb.2013.3237
Doughty P (1996) Statistical analysis of natural experiments in evolutionary biology: comments on recent criticisms of the use of comparative methods to study adaptation. Am Nat 148:943–956. https://doi.org/10.1086/285965
Du WG, Shine R (2022) The behavioural and physiological ecology of embryos: responding to the challenges of life inside an egg. Biol Rev 97:1272–1286. https://doi.org/10.1111/brv.12841
Duellman WE (1968) The genera of phyllomedusine frogs (Anura: Hylidae). Univ Kans Publ Mus Nat Hist 18:1–10
Duellman WE (2001) The hylid frogs of Middle America. Copeia 2002:545–552
Duellman WE (1970) The hylid frogs of Middle America, 1–2. Monographs of the Museum of Natural History. University of Kansas, Lawrence
Fox J, Weisberg S (2019) An R companion to applied regression, 3rd edn. Sage Publishing, Thousand Oaks
Garland TJ, Adolph SC (1994) Why not to do two-species comparative studies: limitations on inferring adaptation. Physiol Zool 67:797–828. https://doi.org/10.1086/physzool.67.4.30163866
Gomez EK, Chaiyasarikul A, Güell BA, Warkentin KM (2023) Developmental changes in red-eyed treefrog embryo behavior increase escape-hatching success in wasp attacks. Behav Ecol Sociobiol 77:52. https://doi.org/10.1007/s00265-023-03324-8
Gomez-Mestre I, Warkentin KM (2007) To hatch and hatch not: similar selective trade-offs but different responses to egg predators in two closely related, syntopic treefrogs. Oecologia 153:197–206. https://doi.org/10.1007/s00442-007-0708-0
Gomez-Mestre I, Wiens JJ, Warkentin KM (2008) Evolution of adaptive plasticity: risk sensitive hatching in Neotropical leaf-breeding treefrogs. Ecol Monogr 78:205–224. https://doi.org/10.1890/07-0529.1
González K, Warkentin KM, Güell BA (2021) Dehydration-induced mortality and premature hatching in gliding treefrogs with even small reductions in humidity. Ichthyol Herpetol 109:21–30. https://doi.org/10.1643/h2020085
Gould S (1977) Ontogeny and phylogeny. Harvard University Press, Cambridge, MA
Güell BA, González K (2019) Mating mayhem. Front Ecol Environ 17:128–128. https://doi.org/10.1002/fee.2011
Güell BA, Warkentin KM (2018a) Does accelerated development impair predator-detection and escape-hatching of phyllomedusid treefrog embryos? Integr Comp Biol 58:e321. https://doi.org/10.1093/icb/icy002
Güell BA, Warkentin KM (2018b) When and where to hatch? Red-eyed treefrog embryos use light cues in two contexts. PeerJ 6:e6018. https://doi.org/10.7717/peerj.6018
Güell BA, Warkentin KM (2023) Phenology and environmental determinants of explosive breeding in gliding treefrogs: diel timing of rainfall matters. Behav Ecol 34:1023–1035. https://doi.org/10.1093/beheco/arad072
Güell BA, Jung J, Almanzar A, Cuccaro-Díaz J, Warkentin KM (2022) Ontogeny of risk assessment and escape-hatching performance by red-eyed treefrog embryos in two threat contexts. J Exp Biol 225:jeb244533. https://doi.org/10.1242/jeb.244533
Güell BA, González K, Pedroso-Santos F (2019) Opportunistic predation by two aquatic-feeding predators on an explosive-breeding aggregation of arboreal gliding treefrogs (Agalychnis spurrelli Boulenger, 1913; Anura: Phyllomedusidae) on the Osa Peninsula of Costa Rica. Herpetol Notes 12:795–798. https://www.biotaxa.org/hn/article/view/50621
Güell BA (2023) Explosive breeding and its consequences for critical adult and embryo behaviors in gliding treefrogs. PhD dissertation. Boston University, Boston
Ims RA (1990) On the adaptive value of reproductive synchrony as a pretador-swamping strategy. Am Nat 136:485–498. https://doi.org/10.1086/285109
Jung J, Kim SJ, Perez Arias SM, McDaniel JG, Warkentin KM (2019) How do red-eyed treefrog embryos sense motion in predator attacks? Assessing the role of vestibular mechanoreception. J Exp Biol 222:jeb206052. https://doi.org/10.1242/jeb.206052
Jung J, Serrano-Rojas SJ, Warkentin KM (2020) Multimodal mechanosensing enables treefrog embryos to escape egg-predators. J Exp Biol 223:jeb236141. https://doi.org/10.1242/jeb.236141
Jung J, Guo M, Crovella M, McDaniel JG, Warkentin KM (2022) Frog embryos use multiple levels of temporal pattern in risk assessment for vibration-cued hatching. Anim Cogn 25:1527–1544. https://doi.org/10.1007/s10071-022-01634-4
Lenth RV (2023) emmeans: Estimated marginal means, aka least-squares means, https://CRAN.R-project.org/package=emmeans
Nannini M, Belk MC (2006) Antipredator responses of two native stream fishes to an introduced predator: does similarity in morphology predict similarity in behavioural response? Ecol Freshw Fish 15:453–463. https://doi.org/10.1111/j.1600-0633.2006.00177.x
NOAA National Centers for Environmental Information (2022) Climate at a Glance: Global Time Series, https://www.ncei.noaa.gov/access/monitoring/climate-at-a-glance/global/time-series
Pyburn WF (1963) Observations on the life history of the treefrog, Phyllomedusa callidryas (Cope). Tex J Sci 15:155–170
Pyburn WF (1970) Breeding behavior of the leaf-frogs Phyllomedusa callidryas and Phyllomedusa dacnicolor in Mexico. Copeia 1970:209–218. https://doi.org/10.2307/1441643
R Core Development Team (2021) R: a language and environment for statistical computing, version 3.4.1. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org
Raff RA, Wray GA (1989) Heterochrony: developmental mechanisms and evolutionary results. J Evol Biol 2:409–434. https://doi.org/10.1046/j.1420-9101.1989.2060409.x
Reilly SM, Wiley E, Meinhardt DJ (1997) An integrative approach to heterochrony: the distinction between interspecific and intraspecific phenomena. Biol J Linn Soc 60:119–143. https://doi.org/10.1006/bijl.1996.0092
Roberts WE (1994) Explosive breeding aggregations and parachuting in a Neotropical frog, Agalychnis saltator (Hylidae). J Herpetol 28:193–199
Rosenthal GG (2017) Mate choice: the evolution of sexual decision making from microbes to humans. Princeton University Press, Princeton
Salica MJ, Vonesh JR, Warkentin KM (2017) Egg clutch dehydration induces early hatching in red-eyed treefrogs. Agalychnis callidryas Peerj 5:e3549. https://doi.org/10.7717/peerj.3549
Santos RG, Pinheiro HT, Martins AS, Riul P, Bruno SC, Janzen FJ, Ioannou CC (2016) The anti-predator role of within-nest emergence synchrony in sea turtle hatchlings. Proc R Soc B 283:20160697. https://doi.org/10.1098/rspb.2016.0697
Schmidt B, Van Buskirk J (2005) A comparative analysis of predator-induced plasticity in larval Triturus newts. J Evol Biol 18:415–425. https://doi.org/10.1111/j.1420-9101.2004.00822.x
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. https://doi.org/10.1038/nmeth.2089
Torres-Carvajal O, Sanchez-Nivicela JC, Posse V, Celi E, Koch C (2020) A new species of cat-eyed snake (Serpentes: Dipsadinae: Leptodeirini) from the Andes of southern Ecuador. Zootaxa 4895:357–380. https://doi.org/10.11646/zootaxa.4895.3.3
Vamosi SM (2005) On the role of enemies in divergence and diversification of prey: a review and synthesis. Can J Zool 83:894–910. https://doi.org/10.1139/z05-063
Warkentin KM (1995) Adaptive plasticity in hatching age: a response to predation risk trade-offs. P Natl Acad Sci USA 92:3507–3510. https://doi.org/10.1073/pnas.92.8.350
Warkentin KM (1999) The development of behavioral defenses: a mechanistic analysis of vulnerability in red-eyed tree frog hatchlings. Behav Ecol 10:251–262. https://doi.org/10.1093/beheco/10.3.251
Warkentin KM (2000) Wasp predation and wasp-induced hatching of red-eyed treefrog eggs. Anim Behav 60:503–510. https://doi.org/10.1006/anbe.2000.1508
Warkentin KM (2002) Hatching timing, oxygen availability, and external gill regression in the tree frog, Agalychnis callidryas. Physiol Biochem Zool 2:155–164. https://doi.org/10.1086/339214
Warkentin KM (2005) How do embryos assess risk? Vibrational cues in predator-induced hatching of red-eyed treefrogs. Anim Behav 70:59–71. https://doi.org/10.1016/j.anbehav.2004.09.019
Warkentin KM (2011a) Environmentally cued hatching across taxa: embryos respond to risk and opportunity. Integr Comp Biol 51:14–25. https://doi.org/10.1093/icb/icr017
Warkentin KM (2011b) Plasticity of hatching in amphibians: evolution, trade-offs, cues and mechanisms. Integr Comp Biol 51:111–127. https://doi.org/10.1093/icb/icr046
Warkentin KM (2017) Development of red-eyed treefrog embryos: a staging table for integrative research on environmentally cued hatching. Integr Comp Biol 57:e175. https://doi.org/10.6084/m9.figshare.10070558.v1
Warkentin KM, Caldwell MS (2009) Assessing risk: embryos, information, and escape hatching. In: Dukas R, Ratcliffe JM (eds) Cognitive ecology II. University of Chicago Press, Chicago, pp 177–200
Warkentin KM, Gomez-Mestre I, McDaniel JG (2005) Development, surface exposure, and embryo behavior affect oxygen levels in eggs of the red-eyed treefrog, Agalychnis callidryas. Physiol Biochem Zool 78:956–966. https://doi.org/10.1086/432849
Warkentin KM, Buckley CR, Metcalf KA (2006a) Development of red-eyed treefrog eggs affects efficiency and choices of egg-foraging wasps. Anim Behav 71:417–425. https://doi.org/10.1016/j.anbehav.2005.06.007
Warkentin KM, Caldwell MS, McDaniel JG (2006b) Temporal pattern cues in vibrational risk assessment by embryos of the red-eyed treefrog, Agalychnis callidryas. J Exp Biol 209:1376–1384. https://doi.org/10.1242/jeb.02150
Warkentin KM, Caldwell MS, Siok TD, D’Amato AT, McDaniel JG (2007) Flexible information sampling in vibrational assessment of predation risk by red-eyed treefrog embryos. J Exp Biol 210:614–619. https://doi.org/10.1242/jeb.001362
Warkentin KM, Cuccaro Diaz J, Güell BA, Jung J, Kim SJ, Cohen KL (2017) Developmental onset of escape-hatching responses in red-eyed treefrogs depends on cue type. Anim Behav 129:103–112. https://doi.org/10.1016/j.anbehav.2017.05.008
Warkentin KM, Jung J, McDaniel JG (2022) Research approaches in mechanosensory-cued hatching. In: Hill PSM, Mazzoni V, Stritih-Peljhan N, Virant-Doberlet M, Wessel A (eds) Biotremology: physiology, ecology, and evolution. Springer International Publishing, Cham, pp 157–201
Watanabe JM (1983) Anti-predator defenses of three kelp forest gastropods: contrasting adaptations of closely-related prey species. J Exp Mar Biol Ecol 71:257–270. https://doi.org/10.1016/0022-0981(83)90119-3
Windig JJ, de Kovel CG, de Jong G (2004) Genetics and mechanics of plasticity. In: DeWitt TJ, Scheiner SM (eds) Phenotypic plasticity: functional and conceptual approaches. Oxford University Press, Oxford, pp 31–49
Acknowledgements
We thank Adrian Tanner and J. Gregory McDaniel for helping design and build the tadpole rotator, Sonia M. Pérez Arias for developing the Python code to construct VOR curves, Katherine González for field assistance, Elena K. Gomez for measuring images to calculate VOR, and Osa Conservation for laboratory space and logistical support. We also thank members of the BU Egg Science Research Group for feedback that improved this work at many stages of its development and three anonymous reviewers for their comments on the manuscript.
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This work was supported by the National Science Foundation (DGE-1247312 to BAG and IOS-1354072 to KMW), Sigma Xi (G2018031596022314 to BAG), and Boston University.
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BAG: conceptualization, data curation, formal analysis, funding acquisition, investigation, methodology, project administration, resources, software, validation, visualization, writing – original draft, writing – review and editing. KMW: conceptualization, funding acquisition, methodology, project administration, resources, validation, writing – review and editing.
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All applicable international, national, and institutional guidelines for the use of animals were followed. This research was conducted under BU IACUC protocol 18–003 and permits from the Costa Rican Ministerio de Ambiente y Energía (MINAE) and the Sistema Nacional de Áreas de Conservación (SINAC) (ACOSA-INV-048–18, INV-ACOSA-055–18, ACOSA-DASP-OI-R-019–2021).
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Güell, B.A., Warkentin, K.M. To hatch and hatch not: does heterochrony in onset of vestibular mechanosensing explain species differences in escape-hatching success of Agalychnis embryos in snake attacks?. Behav Ecol Sociobiol 77, 141 (2023). https://doi.org/10.1007/s00265-023-03417-4
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DOI: https://doi.org/10.1007/s00265-023-03417-4