Explosive breeding and its consequences for critical adult and embryo behaviors in gliding treefrogs
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Abstract
Anurans exhibit remarkable variation in reproduction, even among closely related species, with consequences for behavior across multiple life stages. Phyllomedusid treefrogs include explosive-breeders and better studied prolonged-breeding species. As adults, the explosive breeders gather rarely, in huge numbers, for intensely concentrated reproductive activity. As embryos, they have faster development, less gelatinous egg clutches, and tougher egg capsules than prolonged breeders, but much lower escape-hatching success in snake attacks. I studied adult and embryo behavior in the explosive-breeding gliding treefrog, Agalychnis spurrelli. First, in Chapter 2 I combined long-term natural history observations and automated acoustic recordings with machine-learning analysis to describe the phenology and environmental predictors of explosive breeding. I found that breeding occurs up to 11 times per year during 1–2-day long reproductive events, from late May to mid-September. Reproductive activity is strongly associated with rainfall over the previous 48 hours, especially afternoon and evening rain. This analysis advances our understanding of explosive-breeding phenology in anurans and highlights the importance of fine-scale changes in environmental conditions for frog reproduction and conservation. In Chapter 3, I tested the long-standing and widely accepted hypothesis that an unusual “egg-kicking” behavior by non-amplexed male A. spurrelli functions as an antagonistic strategy to dislodge and kill competitors’ eggs. I recorded and analyzed videos from breeding aggregations to demonstrate that egg-kicking does not dislodge eggs, rejecting this hypothesis. Instead, I propose this behavior functions as part of an alternative reproductive tactic under highly male-skewed operational sex ratios. In Chapters 4 and 5, I tested two hypotheses about why A. spurrelli embryos have strikingly lower escape-hatching success in snake attacks, compared to the prolonged breeding A. callidryas. In Chapter 4, I assessed a hypothesized sensory constraint, testing if later development of vestibular mechanosensing could constrain the ability of A. spurrelli embryos to sense risk cues. I found that vestibular mechanosensory ability, measured by strength of the vestibulo-occular reflex, strongly predicts hatching responses to physical disturbance in A. spurrelli, as in A. callidryas, and that its developmental timing is similar in both species. This rejects the hypothesized constraint and indicates that some other aspect of their biology causes species differences in escape success. In Chapter 5, I compared the egg-clutch biomechanics of A. spurrelli and A. callidryas and used egg-transplant snake-predation experiments and simulated attacks on de-jellied and control A. spurrelli eggs to test the role of egg and clutch structure in mechanosensory-cued hatching. I found that species differences in clutch structure affect vibration biomechanics and thus the cues available to embryos, and transplantation into A. callidryas clutches improved A. spurrelli’s escape success. Moreover, removing their tough jelly capsule increased hatching attempts and eliminated hatching complications. Together, these experiments show how parentally-produced egg and clutch structures contribute to species differences in embryo behavior and the effectiveness of antipredator defenses. Overall, this research enhances our understanding of how mating systems can influence behavior at multiple life stages and demonstrates the value of integrative and comparative research in elucidating mechanisms that underly functionally important interspecific differences in behavior.