Michael W. McCoy

Trophic cascades across ecosystems

Predation can be intense, creating strong direct and indirect effects throughout food webs. In addition, ecologists increasingly recognize that fluxes of organisms across ecosystem boundaries can have major consequences for community dynamics. Species with complex life histories often shift habitats during their life cycles and provide potent conduits coupling ecosystems. Thus, local interactions that affect predator abundance in one ecosystem (for example a larval habitat) may have reverberating effects in another (for example an adult habitat). Here we show that fish indirectly facilitate terrestrial plant reproduction through cascading trophic interactions across ecosystem boundaries. Fish reduce larval dragonfly abundances in ponds, leading to fewer adult dragonflies nearby. Adult dragonflies consume insect pollinators and alter their foraging behaviour. As a result, plants near ponds with fish receive more pollinator visits and are less pollen limited than plants near fish-free ponds. Our results confirm that strong species interactions can reverberate across ecosystems, and emphasize the importance of landscape-level processes in driving local species interactions.

Degradation and resilience in Louisiana salt marshes after the BP–Deepwater Horizon oil spill

More than 2 y have passed since the BP–Deepwater Horizon oil spill in the Gulf of Mexico, yet we still have little understanding of its ecological impacts. Examining effects of this oil spill will generate much-needed insight into how shoreline habitats and the valuable ecological services they provide (e.g., shoreline protection) are affected by and recover from large-scale disturbance. Here we report on not only rapid salt-marsh recovery (high resilience) but also permanent marsh area loss after the BP–Deepwater Horizon oil spill. Field observations, experimental manipulations, and wave-propagation modeling reveal that (i) oil coverage was primarily concentrated on the seaward edge of marshes; (ii) there were thresholds of oil coverage that were associated with severity of salt-marsh damage, with heavy oiling leading to plant mortality; (iii) oil-driven plant death on the edges of these marshes more than doubled rates of shoreline erosion, further driving marsh platform loss that is likely to be permanent; and (iv) after 18 mo, marsh grasses have largely recovered into previously oiled, noneroded areas, and the elevated shoreline retreat rates observed at oiled sites have decreased to levels at reference marsh sites. This paper highlights that heavy oil coverage on the shorelines of Louisiana marshes, already experiencing elevated retreat because of intense human activities, induced a geomorphic feedback that amplified this erosion and thereby set limits to the recovery of otherwise resilient vegetation. It thus warns of the enhanced vulnerability of already degraded marshes to heavy oil coverage and provides a clear example of how multiple human-induced stressors can interact to hasten ecosystem decline.

Size correction: comparing morphological traits among populations and environments

Morphological relationships change with overall body size and body size often varies among populations. Therefore, quantitative analyses of individual traits from organisms in different populations or environments (e.g., in studies of phenotypic plasticity) often adjust for differences in body size to isolate changes in allometry. Most studies of among population variation in morphology either (1) use analysis of covariance (ANCOVA) with a univariate measure of body size as the covariate, or (2) compare residuals from ordinary least squares regression of each trait against body size or the first principal component of the pooled data (shearing). However, both approaches are problematic. ANCOVA depends on assumptions (small variance in the covariate) that are frequently violated in this context. Residuals analysis assumes that scaling relationships within groups are equal, but this assumption is rarely tested. Furthermore, scaling relationships obtained from pooled data typically mischaracterize within-group scaling relationships. We discuss potential biases imposed by the application of ANCOVA and residuals analysis for quantifying morphological differences, and elaborate and demonstrate a more effective alternative: common principal components analysis combined with Burnaby’s back-projection method.

Integrator Networks: Illuminating the Black Box Linking Genotype and Phenotype

Emerging concepts in developmental biology, such as facilitated variation and dynamical patterning modules, address a major shortcoming of the Modern Synthesis in Biology: how genotypic variation is transduced into functional yet diverse phenotypic variation. Still, we lack a theory to explain how variation at the cellular and tissue level is coordinated into variation at the whole-organism level, especially as priority of cellular and tissue functions change over an individuals lifetime and are influenced by environmental variation. Here, we propose that interactions among a limited subset of physiological factors that we call, integrators, regulate most phenotypic variation at the organismal level. Integrators are unique among physiological factors in that they have the propensity to coordinate the expression of conserved gene modules of most types of tissues because they participate as nodes in a hierarchical network. In other words, integrator networks impose physiological epistasis, meaning that whole-organism phenotypic responses will be influenced by previous experiences, current environmental conditions, and fitness priorities as encoded by individual integrators. Below, we provide examples of how integrator networks are responsible for both profound and irreversible phenotypic changes (i.e., metamorphosis, sexual differentiation) as well as subtler, transient (e.g., pelage color, seasonal fluctuations in lymphoid and reproductive tissues) variation. The goal of this article is not to describe completely how integrator networks function, but to stimulate discussion about the role of physiology in linking genetic to phenotypic variation. To generate useful data sets for understanding integrator networks and to inform whole-organism physiology generally, we describe several useful tools including vector-field editing, response-surface regression, and experiments of life-table responses. We then close by highlighting some implications of integrator networks for conservation and biomedicine.

Effects of metabolic rate on protein evolution

Since the modern evolutionary synthesis was first proposed early in the twentieth century, attention has focused on assessing the relative contribution of mutation versus natural selection on protein evolution. Here we test a model that yields general quantitative predictions on rates of protein evolution by combining principles of individual energetics with Kimuras neutral theory. The model successfully predicts much of the heterogeneity in rates of protein evolution for diverse eukaryotes (i.e. fishes, amphibians, reptiles, birds, mammals) from different thermal environments. Data also show that the ratio of non-synonymous to synonymous nucleotide substitution is independent of body size, and thus presumably of effective population size. These findings indicate that rates of protein evolution are largely controlled by mutation rates, which in turn are strongly influenced by individual metabolic rate.

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. 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.

Carry-over effects of the larval environment on post-metamorphic performance in two hylid frogs

Life history theory and empirical studies suggest that large size or earlier metamorphosis are suitable proxies for increased lifetime fitness. Thus, across a gradient of larval habitat quality, individuals with similar phenotypes for these traits should exhibit similar post-metamorphic performance. Here we examine this paradigm by testing for differences in post-metamorphic growth and survival independent of metamorphic size in a temperate (spring peeper, Pseudacris crucifer) and tropical (red-eyed treefrog, Agalychnis callidryas) anuran reared under differing larval conditions. For spring peepers, increased food in the larval environment increased post-metamorphic growth efficiency more than predicted by metamorphic phenotype and led to increased mass. Similarly, red-eyed treefrogs reared at low larval density ended the experiment at a higher mass than predicted by metamorphic phenotype. These results show that larval environments can have delayed effects not captured by examining only metamorphic phenotype. These delayed effects for the larval environment link larval and juvenile life history stages and could be important in the population dynamics of organisms with complex life cycles.

Conspecific density determines the magnitude and character of predator-induced phenotype

The benefits in survival gained from predator-induced phenotypes often come at a cost to other components of fitness. Therefore, the level of expression of an induced phenotype should mirror the level of risk in the environment. When a predator exhibits a saturating functional response the risk of mortality to a given prey decreases as prey density increases. Therefore, for a given predator threat, investment in defense should be lower in prey at high density relative to those at low density. In this study, I test whether the magnitude of predator-induced morphological plasticity decreases with increasing conspecific density by exposing pine woods tree frog (Hyla femoralis) tadpoles at three different densities to predators (present or absent) in a factorial experiment. Tadpole morphology was not affected by changes in density in the absence of predators. However, predators had a significant, density-dependent effect on tadpole morphology. Specifically, the magnitude of morphological response was graded and larger for animals in the low density (high risk) environment. This study demonstrates that tadpoles can modulate phenotypic plasticity in response to mortality risk as a function of both the density of conspecifics and chemical cues from predators, which suggests that they are able to detect and respond to fine-scale changes in the threat environment. In addition, this study highlights the need for analytical approaches that allow morphological plasticity studies to elucidate allometric relationships in addition to simply quantifying size-corrected traits.

Effects of plastic hatching timing carry over through metamorphosis in red‐eyed treefrogs

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 la...

Endocrine Activity of Extraembryonic Membranes Extends beyond Placental Amniotes

Background During development, all amniotes (mammals, reptiles, and birds) form extraembryonic membranes, which regulate gas and water exchange, remove metabolic wastes, provide shock absorption, and transfer maternally derived nutrients. In viviparous (live-bearing) amniotes, both extraembryonic membranes and maternal uterine tissues contribute to the placenta, an endocrine organ that synthesizes, transports, and metabolizes hormones essential for development. Historically, endocrine properties of the placenta have been viewed as an innovation of placental amniotes. However, an endocrine role of extraembryonic membranes has not been investigated in oviparous (egg-laying) amniotes despite similarities in their basic structure, function, and shared evolutionary ancestry. In this study, we ask whether the oviparous chorioallantoic membrane (CAM) of chicken (Gallus gallus) has the capability to synthesize and receive signaling of progesterone, a major placental steroid hormone. Methodology/Principal Findings We quantified mRNA expression of key steroidogenic enzymes involved in progesterone synthesis and found that 3β-hydroxysteroid dehydrogenase, which converts pregnenolone to progesterone exhibited a 464 fold increase in the CAM from day 8 to day 18 of embryonic development (F5, 68 = 89.282, p<0.0001). To further investigate progesterone synthesis, we performed explant culture and found that the CAM synthesizes progesterone in vitro in the presence of a steroid precursor. Finally, we quantified mRNA expression and performed protein immunolocalization of the progesterone receptor in the CAM. Conclusions/Significance Collectively, our data indicate that the chick CAM is steroidogenic and has the capability to both synthesize progesterone and receive progesterone signaling. These findings represent a paradigm shift in evolutionary reproductive biology by suggesting that endocrine activity of extraembryonic membranes is not a novel characteristic of placental amniotes. Rather, we hypothesize that these membranes may share an additional unifying characteristic, steroidogenesis, across amniotes at large.