Many prey species, including amphibian larvae, can adaptively alter coloration and morphology to become more or less conspicuous to predators. Despite abundant research on predator‐induced plasticity in tadpoles, the combination of color and morphological responses to predators remains largely unexplored. We measured predator‐induced morphological and color plasticity in tadpoles. We reared tadpoles of the neotropical treefrog Dendropsophus ebraccatus with dragonfly nymph or fish predators, or in a predator‐free control. After 10 days, we digitally photographed tadpoles and measured eight morphometric variables and five tail color variables. Tadpoles reared with nymphs developed the largest and reddest tails, but incurred a developmental cost, being the smallest overall. Cues from fish induced an opposite tail phenotype in tadpoles, causing shallow achromatic tails. Control tadpoles developed intermediate tail phenotypes. This provides the first experimental evidence that tadpoles can shift both color and morphology in opposite, predator‐specific directions in response to a fish and an odonate predator. Despite mean differences, however, there was substantial variation in the degree of phenotype induction across treatments. Tail redness was correlated with tail spot size, but not perfectly, indicating that color and morphology may be partially decoupled in D. ebraccatus. Balancing selection from multiple conflicting predators may result in genetic variation for developmental plasticity.
Water molds attack aquatic eggs worldwide and have been associated with major mortality events in some cases, but typically only in association with additional stressors. We combined field observations and laboratory experiments to study egg stage defenses against pathogenic water mold in three temperate amphibians. Spotted salamanders (Ambystoma maculatum) wrap their eggs in a protective jelly layer that prevents mold from reaching the embryos. Wood frog (Rana sylvatica) egg masses have less jelly but are laid while ponds are still cold and mold growth is slow. American toad (Bufo americanus) eggs experience the highest infection levels. They are surrounded by thin jelly and are laid when ponds have warmed and mold grows rapidly. Eggs of all three species hatched early when infected, yielding smaller and less developed hatchlings. This response was strongest in B. americanus. Precocious hatching increased vulnerability of wood frog hatchlings to invertebrate predators. Finally, despite being potential toad hatchling predators, R. sylvatica tadpoles can have a positive effect on B. americanus eggs. They eat water mold off infected toad clutches, increasing their hatching success.
Diversification of reproductive mode is a major theme in animal evolution. Vertebrate reproduction began in water, and terrestrial eggs evolved multiple times in fishes and amphibians and in the amniote ancestor. Because oxygen uptake from water conflicts with water retention in air, egg adaptations to one environment typically preclude development in the other. Few animals have variable reproductive modes, and no vertebrates are known to lay eggs both in water and on land. We report phenotypic plasticity of reproduction with aquatic and terrestrial egg deposition by a frog. The treefrog Dendropsophus ebraccatus, known to lay eggs terrestrially, also lays eggs in water, both at the surface and fully submerged, and chooses its reproductive mode based on the shade above a pond. Under unshaded conditions, in a disturbed habitat and in experimental mesocosms, these frogs lay most of their egg masses aquatically. The same pairs also can lay eggs terrestrially, on vegetation over water, even during a single night. Eggs can survive in both aquatic and terrestrial environments, and variable mortality risks in each may make oviposition plasticity adaptive. Phylogenetically, D. ebraccatus branches from the basal node in a clade of terrestrially breeding species, nested within a larger lineage of aquatic-breeding frogs. Reproductive plasticity in D. ebraccatus may represent a retained ancestral state intermediate in the evolution of terrestrial reproduction.aquatic egg-laying ͉ evolution of reproductive mode ͉ Hyla ebraccata ͉ phenotypic plasticity ͉ climate change T he evolution of terrestrially developing eggs from ancestral aquatic eggs is a repeated trend in both invertebrates and vertebrates (1-10). In both groups, aquatic predators and constraints on oxygen uptake are hypothesized to select for terrestrial eggs (2, 7-11). Terrestrial eggs can improve the embryonic respiratory environment, allow oviposition over fast-moving streams where aquatic eggs might be swept away, and allow animals to colonize habitats without permanent water bodies (2, 4, 7-10). However, terrestrial eggs experience new risks from desiccation and terrestrial predators (2, 4, 7-10). Because aquatic and terrestrial environments select for different traits, eggs are usually well adapted to only one environment (2, 4). Adaptations for terrestrial oviposition have evolved independently in several groups [e.g., gastropods (8, 12), insects (9, 13), and fishes and amphibians (1, 2, 4, 10)]. In all of these organisms, the divergence in reproductive mode [oviposition site and type of egg development (1, 2, 10)] occurred long ago, and it is thus difficult to directly assess selective pressures that may have influenced such evolution. Closely related species or populations that vary in their reproductive modes [e.g., between viviparity and oviparity (14-18)] offer the best opportunity to study the selective pressures leading to reproductive mode diversification. Although some foam-nesting frogs are reported to place nests in diverse locations (10,19,20), t...
Citation: Touchon, J. C., and M. W. McCoy. 2016. The mismatch between current statistical practice and doctoral training in ecology. Ecosphere 7(8):e01394. 10.1002/ecs2.1394Abstract. Ecologists are studying increasingly complex and important issues such as climate change and ecosystem services. These topics often involve large data sets and the application of complicated quantitative models. We evaluated changes in statistics used by ecologists by searching nearly 20,000 published articles in ecology from 1990 to 2013. We found that there has been a rise in sophisticated and computationally intensive statistical techniques such as mixed effects models and Bayesian statistics and a decline in reliance on approaches such as ANOVA or t tests. Similarly, ecologists have shifted away from software such as SAS and SPSS to the open source program R. We also searched the published curricula and syllabi of 154 doctoral programs in the United States and found that despite obvious changes in the statistical practices of ecologists, more than one-third of doctoral programs showed no record of required or optional statistics classes. Approximately one-quarter of programs did require a statistics course, but most of those did not cover contemporary statistical philosophy or advanced techniques. Only one-third of doctoral programs surveyed even listed an optional course that teaches some aspect of contemporary statistics. We call for graduate programs to lead the charge in improving training of future ecologists with skills needed to address and understand the ecological challenges facing humanity.
Environmentally cued plasticity in hatching timing is widespread in animals. As with later life‐history switch points, plasticity in hatching timing may have carryover effects that affect subsequent interactions with predators and competitors. Moreover, the strength of such effects of hatching plasticity may be context dependent. We used red‐eyed treefrogs, Agalychnis callidryas, to test for lasting effects of hatching timing (four or six days post‐oviposition) under factorial combinations of resource levels (high or low) and predation risk (none, caged, or lethal Pantala flavescens dragonfly naiads). Tadpoles were raised in 400‐L mesocosms in Gamboa, Panama, from hatching until all animals had metamorphosed or died, allowing assessment of effects across a nearly six‐month period of metamorphosis. Hatching early reduced survival to metamorphosis, increased larval growth, and had context‐dependent effects on metamorph phenotypes. Early during the period of metamorph emergence, early‐hatched animals were larger than late‐hatched ones, but this effect attenuated over time. Early‐hatched animals also left the water with relatively longer tails. Lethal predators dramatically reduced survival to metamorphosis, with most mortality occurring early in the larval period. Predator effects on the timing of metamorphosis and metamorph size and tail length depended upon resources. For example, lethal predators reduced larval periods, and this effect was stronger with low resources. Predators affected metamorph size early in the period of metamorphosis, whereas resource levels were a stronger determinant of phenotype for animals that metamorphosed later. Effects of hatching timing were detectable on top of strong effects of larval predators and resources, across two subsequent life stages, and some were as strong as or stronger than effects of resources. Plasticity in hatching timing is ecologically important and currently underappreciated. Effects on metamorph numbers and phenotypes may impact subsequent interactions with predators, competitors, and mates, with potentially cascading effects on recruitment and fitness.
Most animals metamorphose, changing morphology, physiology, behavior and ecological interactions. Size- and habitat-dependent mortality risk is thought to affect the evolution and plastic expression of metamorphic timing, and high predation during the morphological transition is posited as a critical selective force shaping complex life cycles. Nonetheless, empirical data on how risk changes across metamorphosis and stage-specific habitats, or how that varies with size, are rare. We examined predator-prey interactions of red-eyed treefrogs, Agalychnis callidryas, with an aquatic predator (giant water bug, Belostoma) and a semi-terrestrial predator (fishing spider, Thaumasia) across metamorphosis. We manipulated tadpole density to generate variation in metamorph size and conducted predation trials at multiple developmental stages. We quantified how frog behavior (activity) changes across metamorphic development, habitats, and predator presence or absence. In aquatic trials with water bugs, frog mortality increased with forelimb emergence, as hypothesized. In semi-terrestrial trials, contrary to predictions, predation by spiders increased, not decreased, with tail resorption. In neither case did frog size affect mortality. Frogs reduced activity upon forelimb emergence in the water, and further with emergence into air, then increased activity with tail resorption. Longer-tailed metamorphs were captured more often in spider attacks, but attacked less, as most attacks followed prey movements. Metamorphs behaviorally compensated for poor escape performance more effectively on land than in water, thus emergence timing may critically affect mortality. The developmental timing of the ecological transition between environments that select for different larval and juvenile phenotypes is an important, neglected variable in studies of complex life cycles.
Water molds are widespread in aquatic environments and are important causes of mortality in amphibian and fish eggs. We tested the ability of two species of North American anurans with different breeding phenologies ( Rana sylvatica LeConte, 1825 and Bufo americanus Holbrook, 1836) to alter their hatching timing in response to three indicators of environmental risk: infection with a water mold, exposure to simulated egg predation cues, or exposure to simulated larval predation cues. When infected with water mold (Saprolegniaceae), B. americanus eggs hatched, on average, 44% earlier than the controls and R. sylvatica eggs hatched 19% earlier than the controls. In addition, B. americanus but not R. sylvatica eggs hatched significantly earlier than the controls when exposed to simulated egg and larval predation cues. Bufo americanus embryos hatched before developing muscular response, suggesting that hatching occurs through enzymatic egg capsule degradation combined with ciliary movement, not through behavior. Bufo americanus breeds later than R. sylvatica and responded to infection and simulated predation cues more strongly. This may reflect a history of stronger selection by pathogens and predators that accumulate in ponds as the breeding season progresses. To our knowledge, these are the first examples of induced hatching of amphibians in response to aquatic pathogens.
Summary 1.The importance of rainfall is recognized in arid habitats, but has rarely been explored in ecosystems not viewed as rainfall limited. In addition, most attempts to study how rainfall affects organismal survival have focused on long-term rainfall metrics (e.g. monthly or seasonal patterns) instead of short-term measures. For organisms that are short lived or are sensitive to desiccation, short-term patterns of rainfall may provide insight to understanding what determines survival in particular habitats. 2. We monitored daily rainfall and survival of arboreal eggs of the treefrog Dendropsophus ebraccatus at two ponds during the rainy season in central Panama. Desiccation and predation were the primary sources of egg mortality and their effects were not independent. Rainfall directly reduced desiccation mortality by hydrating and thickening the jelly surrounding eggs. In addition, rainfall reduced predation on egg clutches. 3. To elucidate the mechanism by which rainfall alters predation, we exposed experimentally hydrated and dehydrated egg clutches to the two D. ebraccatus egg predators most common at our site, ants and social wasps. Ants and wasps preferentially preyed on dehydrated clutches and ants consumed dehydrated eggs three times faster than hydrated eggs. 4. Rainfall patterns are expected to change and the responses of organisms that use rainfall as a reliable cue to reproduce may prove maladaptive. If rainfall becomes more sporadic, as is predicted to happen during this century, it may have negative consequences for desiccation-sensitive organisms.
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