Environmentally cued hatching
Since the initial discoveries of predator effects on hatching timing (Sih & Moore 1993, Warkentin 1995) we have learned that embryos of many species change when they hatch in response to environmental conditions. Some hatch early to escape from predators, pathogens, or abiotic threats. Some delay hatching in response to larval predators, abiotic threats, or lack of larval food. Parents also cue and manipulate offspring hatching.
The symposium on “Environmentally Cued Hatching Across Taxa” (ICB 2011 • co-organized with Karen Martin, Richard Strathmann) showed that cued hatching responses are diverse and widespread across the animal phylogeny. They may be more the norm than the exception. Current research addresses the nature and magnitude of cued hatching responses, their evolutionary history, their developmental, physiological and behavioral mechanisms, and their developmental and ecological consequences.
Most of our research focuses on amphibians, where cued hatching is relatively well studied, and we have accumulated a strong foundation. Our central study species is the red-eyed treefrog and we also work with other neotropical and temperate frogs. However, we are broadly interested in cued hatching studies in other taxa and happy to help facilitate such research where possible.
Mechanisms of hatching and hatching plasticity
Amphibian hatching has been described as a gradual developmental process involving release of proteolytic enzymes from unicellular hatching glands on the head, with enzymes released as they are synthesized. However, hatching mechanisms are clearly more diverse. For instance, red-eyed treefrogs can hatch in seconds in predator attacks at any point during the last third of their typical undisturbed embryonic period, with no prior degradation of the egg capsule. We want to understand how embryos hatch, how they are able to change their hatching timing in response to cues, and how this varies among species and across development. Current research focuses on red-eyed treefrogs, hourglass treefrogs, and American toads – three species with very different eggs, and embryos, that appear to hatch, and to accelerate hatching, in different ways. The evolution and development of hatching mechanisms is the focus of Kristina Cohen‘s PhD research. Hatching mechanisms may enable and/or constrain the evolution of responses to particular environmental threats. • Collaborators Marc Seid, Sean Mullen.
How do embryos assess risk using vibrational cues?
Red-eyed treefrog embryos use the physical disturbance of egg clutches by predators as a cue to hatch prematurely; however, they are also subject to frequent benign disturbances, such as by torrential tropical rainstorms. We use vibration recordings and playback experiments to study the cues available to embryos in different disturbance types and probe their responses to disturbance patterns. We know that they use many different properties of vibrations to modulate their hatching response, including frequency and temporal properties, and that these are non-redundant, but we are far from having a full understanding of their behavioral decision rules. Many prey use such incidental cues from predators to cue defensive behavior, and must distinguish predator cues from benign background stimuli. We know that they do this, but understand relatively little about how they do it, for any predator–prey system. Vibration-cued escape hatching thus offers a tractable case in which to examine some general questions about the cognitive ecology of prey. • Collaborators mechanical engineer Greg McDaniel, computer scientist Mark Crovella, students Michael Caldwell (PhD 2010) and Ming Guo (MA in progress).
Development of adaptive embryo behavior – changing senses, abilities, trade-offs and choices
Escape hatching responses of embryos to threats depend critically both on cue reception and hatching ability, which in turn depend on the development of sensory systems and hatching mechanisms. In addition, as traits affecting the ability to survive within and outside the egg capsule change, so do the costs of accelerating or delaying hatching, and of potential decision errors. In red-eyed treefrogs, older embryos hatch more readily but even 30%-premature embryos sometimes hatch within seconds of a cue. We want to understand how changes in perceptual abilities, behavioral competencies, and optimal decisions combine to shape the development and expression of escape hatching behavior. Embryos use cues in multiple sensory modalities. We are focusing on physical disturbance of clutches and hypoxia, both of which are important for red-eyed treefrogs and common as hatching cues across taxa. These cues also differ in important ways. Hypoxia kills embryos, so the cue and the threat are identical, and clear. Also, embryos sense and respond behaviorally to oxygen cues long before hatching competence. Physical disturbance (and the resulting vibration) is fundamentally ambiguous – sometimes caused by predators but often by rain or wind – creating the possibility of missed cues and false alarms. We do not know (yet) how embryos receive vibrational cues, but a likely candidate sensor – the inner ear – changes substantially during the period of hatching competence. This is a multifacted research project that will offer many opportunities for graduate and undergraduate student involvement.
Parent–embryo co-evolution in glassfrogs: plasticity, parental care, and sexual selection
Glassfrogs represent an independent origin of terrestrial eggs and show a diversity of parental care strategies, with multiple origins of male care of embryos. Embryos hatch prematurely in response to dehydration or attacks by predators. Parental care can protect embryos from both types of risk, but caring behavior varies widely among species, across contexts and, probably, among individuals. Moreover, females are extremely choosy about mates but apparently not on the basis of male calls or physical or territory traits. Might they be selecting for good fathers, judging by prior eggs? Might multiple matings affect subsequent caring behavior? And might this alter embryo behavior and hatchling phenotypes? How interactions between males, females, and embryos play out on behavioral and evolutionary time scales is the focus of Jesse Delia’s PhD research. • Collaborator Laura Bravo Valencia, STRI fellow/ MA student at Universidad de los Andes.
Metamorphic ontogeny of risk, performance, and behavior across the water to land transition
Anuran metamorphs are awkward – morphologically transitional between aquatic tadpoles and terrestrial frogs they seem poorly suited for any habitat and have long been considered a highly vulnerable stage. Plasticity in larval period and size at metamorphosis is well known in anurans, and the duration of metamorphosis (from forelimb emergence to tail resorption) can also be plastic in apparently adaptive ways but, surprisingly, we know little about plasticity in the developmental timing of the critical ecological transition – when animals climb out of the water. We are studying how risk in alternative aquatic/ terrestrial environments changes with size and developmental stage through metamorphosis, how behavior changes developmentally and with environmental context, and the role of behavior in modulating risk. Like hatching, the transition from water to land occurs during a period of very rapid development when small changes in timing can make a large difference to phenotype, performance, and survival. Also like embryos, we know relatively little about how metamorph behavior develops and is expressed during this critical period in important natural contexts. • Behavior and development during metamorphosis – Greene, Noss, Landberg, Vonesh & Warkentin, SICB 2011 poster • Development of climbing performance and behavior – Landberg, Willink, Greene, Noss, Vonesh & Warkentin, SICB 2012 talk • Behavioral plasticity mitigates risk across environments and predators – Touchon, Jímenez, Abinette, Vonesh & Warkentin, Oecologia 2013.
Fear, death, and life history switch points: cumulative effects of plasticity and predation across three life stages
Predator-prey relationships are a fundamental part of ecology. Predators kill prey and prey alter behavior and development in response to predators. We assessed the relative importance and context-dependence of these two mechanisms for population processes and natural selection. Most species have complex life cycles, and the timing of stage-transitions (e.g., hatching, metamorphosis) is both plastic and important for survival. In red-eyed treefrogs arboreal embryos hatch early to escape from egg predators and tadpoles accelerate metamorphosis in response to aquatic predators. They also delay metamorphosis in response to semiterrestrial predators of froglets. We manipulated both direct effects of predators (prey density and mortality) and their indirect effects (cues that elicit prey responses) across egg, tadpole, and froglet stages to assess their individual and interacting, cumulative effects in combination with other ecologically relevant variables. We developed mathematical models, based on the results of short-term experiments that measured simple combinations of size- and density-dependent processes, then used these models in simulations to predict the outcomes of longer, more complex experiments. The simulations and experimental results show that egg stage effects – including both direct effects of and embryo responses to egg predators – can alter growth and survival in the aquatic larval stage and continue to affect animals at metamorphosis. This enhances our understanding of development by quantifying how effects of early environments can persist to affect the characteristics of animals and their responses in later life stages, and to what extent this varies across ecological contexts. The modeling framework we developed for assessing the magnitude of effects of direct predation and plastic, predator-induced changes in prey development and behavior across key axes of environmental variation (e.g., resource availability and risk in particular stages) has broad relevance for understanding the relative importance of trait and density-mediated effects for population processes and provides broadly applicable quantitative methods for predicting predator effects on growing prey. • Collaborators James Vonesh and Michael McCoy are building on this research. I encourage prospective students focused more on predator–prey ecology than on integrative biology of early life stages to contact James or Mike.