Egg clutch dehydration induces early hatching in red-eyed treefrogs, Agalychnis callidryas

Terrestrial eggs have evolved repeatedly in tropical anurans exposing embryos to the new threat of dehydration. Red-eyed treefrogs, Agalychnis callidryas, lay eggs on plants over water. Maternally provided water allows shaded eggs in humid sites to develop to hatching without rainfall, but unshaded eggs and those in less humid sites can die from dehydration. Hatching responses of amphibian eggs to dry conditions are known from two lineages with independent origins of terrestrial eggs. Here, we experimentally tested for dehydration-induced early hatching in another lineage (Agalychnis callidryas, Phyllomedusidae), representing a third independent origin of terrestrial eggs. We also investigated how dehydration affected egg and clutch structure, and egg mortality. We collected clutches from a pond in Gamboa, Panama, and randomly allocated them to wet or dry treatments at age 1 day. Embryos hatched earlier from dry clutches than from wet clutches, accelerating hatching by ∼11%. Clutch thickness and egg diameter were affected by dehydration, diverging between treatments over time. Meanwhile, mortality in dry clutches was six-fold higher than in control clutches. With this study, early hatching responses to escape mortality from egg dehydration are now known from three anuran lineages with independent origins of terrestrial eggs, suggesting they may be widespread. Further studies are needed to understand how terrestrial amphibian eggs can respond to, or will be affected by, rapid changes in climate over the next decades.Fil: Salica, María José. Universidad Nacional de Jujuy. Facultad de Ciencias Agrarias. Instituto de Ecorregiones Andinas. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico CONICET - Salta. San Salvador de Jujuy; ArgentinaFil: Vonesh, James R.. Virginia Commonwealth University; Estados UnidosFil: Warkentin, Karen M.. Smithsonian Tropical Research Institute; Panamá. Boston University; Estados Unido

Prey Responses to Predator Chemical Cues: Disentangling the Importance of the Number and Biomass of Prey Consumed

To effectively balance investment in predator defenses versus other traits, organisms must accurately assess predation risk. Chemical cues caused by predation events are indicators of risk for prey in a wide variety of systems, but the relationship between how prey perceive risk in relation to the amount of prey consumed by predators is poorly understood. While per capita predation rate is often used as the metric of relative risk, studies aimed at quantifying predator-induced defenses commonly control biomass of prey consumed as the metric of risk. However, biomass consumed can change by altering either the number or size of prey consumed. In this study we determine whether phenotypic plasticity to predator chemical cues depends upon prey biomass consumed, prey number consumed, or both. We examine the growth response of red-eyed treefrog tadpoles (Agalychnis callidryas) to cues from a larval dragonfly (Anax amazili). Biomass consumed was manipulated by either increasing the number of prey while holding individual prey size constant, or by holding the number of prey constant and varying individual prey size. We address two questions. (i) Do prey reduce growth rate in response to chemical cues in a dose dependent manner? (ii) Does the magnitude of the response depend on whether prey consumption increases via number or size of prey? We find that the phenotypic response of prey is an asymptotic function of prey biomass consumed. However, the asymptotic response is higher when more prey are consumed. Our findings have important implications for evaluating past studies and how future experiments should be designed. A stronger response to predation cues generated by more individual prey deaths is consistent with models that predict prey sensitivity to per capita risk, providing a more direct link between empirical and theoretical studies which are often focused on changes in population sizes not individual biomass

Risk assessment based on indirect predation cues: revisiting fine-grained variation

To adaptively express inducible defenses, prey must gauge risk based on indirect cues of predation. However, the information contained in indirect cues that enable prey to fine-tune their phenotypes to variation in risk is still unclear. In aquatic systems, research has focused on cue concentration as the key variable driving threat-sensitive responses to risk. However, while risk is measured as individuals killed per time, cue concentration may vary with either the number or biomass killed. Alternatively, fine-grained variation in cue, that is, frequency of cue pulses irrespective of concentration, may provide a more reliable signal of risk. Here, we present results from laboratory experiments that examine the relationship between red-eyed treefrog tadpole growth and total cue, cue per pulse, and cue pulse frequency. We also reanalyze an earlier study that examined the effect of fine-grained variation in predator cues on wood frog tadpole growth. Both studies show growth declines with increasing cue pulse frequency, even though individual pulses in high-frequency treatments contained very little cue. This result suggests that counter to earlier conclusions, tadpoles are using fine-grained variation in cue arising from the number of predation events to assess and respond to predation risk, as predicted by consumer–resource theory.ECU Open Access Publishing Support Fund; National Science Foundation Grant Numbers: 0716923, 071722

Cross-ecosystem effects of terrestrial predators link treefrogs, zooplankton, and aquatic primary production

Predators can directly or indirectly shape food webs through a combination of consumptive and non-consumptive effects. Yet, how these effects vary across natural populations and their consequences for adjacent ecosystems remains poorly resolved. We examined links between terrestrial predators and aquatic ecosystems through their effects on a locally abundant amphibian, the red-eyed treefrog (Agalychnis callidryas), which has arboreal eggs (heavily predated by snakes and wasps) and aquatic larvae; embryos can escape terrestrial threats by hatching at an earlier age and smaller size. Our multi-site field survey indicates that in natural populations, the relative contributions of these consumptive and non-consumptive effects of predators can be substantial and remarkably similar. However, in mesocosms where we experimentally mimicked these predator effects, changes in the density and initial hatching age of tadpoles carried distinct consequences for aquatic food webs. Density-dependent growth resulted in peak tadpole biomass at intermediate densities (reflecting intermediate predation), and early-hatched tadpoles grew 16% faster and produced 26% more biomass than their late-hatched counterparts. These changes in tadpole growth and size differentially affected zooplankton communities, and the production and stability of phytoplankton. Together, these results illustrate multiple pathways through which predators in one ecosystem can modulate the structure of adjacent food webs

Data from: Patterns of parental care in Neotropical glassfrogs: fieldwork alters hypotheses of sex-role evolution

Many animals provide parental care to offspring. Parental sex-roles vary extensively across taxa, and such patterns are considered well documented. However, information on amphibians is lacking relative to other vertebrate groups. We combine natural history observations with functional and historical analyses to examine the evolution of egg care in glassfrogs (Centrolenidae). Parental care was considered rare and predominately provided by males. Our field observations of 40 species revealed that care occurs throughout the family, and the caregiving sex changes across lineages. We discovered that a brief period of maternal care is widespread and occurs in species previously thought to lack care. Using a combination of female-removal experiments, prey-choice tests with egg-eating katydids, and parental disturbance-tolerance assays, we confirm the adaptive benefits of short-term maternal care in wild Cochranella granulosa and Teratohyla pulverata. To examine historical transitions between caregiving sexes, we assembled a molecular phylogeny and estimated ancestral care states using our data and the literature. We assessed patterns indicative of sex-specific constraints by testing whether transitions between the sexes are associated with changes in care levels. Our analyses support that male-only care evolved 2-3 times from female-only care, and this change is associated with substantial increases in care levels-a pattern supporting the hypothesis that male-only care evolved via constraints on maternal expenditure. Many groups of amphibians remain poorly studied, with emerging evidence indicating that care patterns are more diverse than currently appreciated. Natural history remains fundamental to uncovering this diversity and generating testable hypotheses of sex-role evolution

Data from: How embryos escape from danger: the mechanism of rapid, plastic hatching in red-eyed treefrogs

Environmentally cued hatching allows embryos to escape dangers and exploit new opportunities. Such adaptive responses require a flexibly regulated hatching mechanism sufficiently fast to meet relevant challenges. Anurans show widespread, diverse cued hatching responses, but their described hatching mechanisms are slow, and regulation of timing is unknown. Arboreal embryos of red-eyed treefrogs, Agalychnis callidryas, escape from snake attacks and other threats by very rapid premature hatching. We used videography, manipulation of hatching embryos, and electron microscopy to investigate their hatching mechanism. High-speed video revealed three stages of the hatching process: pre-rupture shaking and gaping, vitelline membrane rupture near the snout, and muscular thrashing to exit through the hole. Hatching took 6.5-49 s. We hypothesized membrane rupture to be enzymatic, with hatching enzyme released from the snout during shaking. To test this, we displaced hatching embryos to move their snout from its location during shaking. The membrane ruptured at the original snout position and embryos became trapped in collapsed capsules; they either moved repeatedly to relocate the hole or shook again and made a second hole to exit. Electron microscopy revealed that hatching glands are densely concentrated on the snout and absent elsewhere. They are full of vesicles in embryos and release most of their contents rapidly at hatching. Agalychnis callidryas' hatching mechanism contrasts with the slow process described in anurans to date and exemplifies one way embryos can achieve rapid, flexibly timed hatching to escape from acute threats. Other amphibians with cued hatching may also have novel hatching mechanisms

High speed video data

These are the data from high speed video of Agalychnis callidryas embryos hatching

Data from: Predicting predation through prey ontogeny using size-dependent functional response models

The functional response is a critical link between consumer and resource dynamics, describing how a consumer's feeding rate varies with prey density. Functional response models often assume homogenous prey size and size-independent feeding rates. However, variation in prey size due to ontogeny and competition is ubiquitous, and predation rates are often size dependent. Thus, functional responses that ignore prey size may not effectively predict predation rates through ontogeny or in heterogeneous populations. Here, we use short-term response surface experiments and statistical modeling to develop and test prey size-dependent functional responses for water bugs and dragonfly larvae feeding on red-eyed treefrog tadpoles. We then extend these models through simulations to predict mortality through time for growing prey. Predation rates of both predators were more sensitive to changes in prey size than density. Both conventional and size-dependent functional response models predicted average overall mortality in short-term mixed cohort experiments, but only the size-dependent models accurately captured how mortality was spread across sizes. As a result, simulations that extrapolated these results through prey ontogeny, showed that differences in size-specific mortality are compounded as prey grow, causing predictions from conventional and size-dependent functional response models to diverge dramatically through time. Our results highlight the importance of incorporating prey size when modeling consumer-prey dynamics in size-structured, growing prey populations