Brandon T. Barton

Climate warming strengthens indirect interactions in an old‐field food web

Climate change is expected to alter trophic interactions within food chains, but predicting the fate of particular species is difficult because the predictions hinge on knowing exactly how climate influences direct and indirect interactions. We used two complementary approaches to examine how climate change may alter trophic interactions within an old-field food web composed of herbaceous plants, grasshopper herbivores, and spider predators. We synthesized data spanning 15 years of experimentation during which interannual mean growing season temperature varied by 2 degrees C and precipitation by 2.5 cm. We also manipulated temperature within mesocosms to test the affect of temperature on primary production and strength of direct and indirect trophic interactions. Both approaches produced similar results: plant production was not directly affected by temperature or precipitation, but the strength of top-down indirect effects on grasses and forbs increased by 30-40% per 1 degrees C. Hence, the net effect of climate change was to strengthen top-down control of this terrestrial system.

Experimental warming transforms multiple predator effects in a grassland food web

This experimental study tests new theory for multiple predator effects on communities by using warming to alter predator habitat use and hence direct and indirect interactions in a grassland food web containing two dominant spider predator species, a dominant grasshopper herbivore and grass and herb plants. Experimental warming further offers insight into how climate change might alter direct and indirect effects. Under ambient environmental conditions, spiders used habitat in spatially complementary locations. Consistent with predictions, the multiple predator effect on grasshoppers and on plants was the average of the individual predator effects. Warming strengthened the single predator effects. It also caused the spider species to overlap lower in the vegetation canopy. Consistent with predictions, the system was transformed into an intraguild predation system with the consequent extinction of one spider species. The results portend climate caused loss of predator diversity with important consequences for food web structure and function.

A bioenergetic framework for the temperature dependence of trophic interactions

Changing temperature can substantially shift ecological communities by altering the strength and stability of trophic interactions. Because many ecological rates are constrained by temperature, new approaches are required to understand how simultaneous changes in multiple rates alter the relative performance of species and their trophic interactions. We develop an energetic approach to identify the relationship between biomass fluxes and standing biomass across trophic levels. Our approach links ecological rates and trophic dynamics to measure temperature-dependent changes to the strength of trophic interactions and determine how these changes alter food web stability. It accomplishes this by using biomass as a common energetic currency and isolating three temperature-dependent processes that are common to all consumer-resource interactions: biomass accumulation of the resource, resource consumption and consumer mortality. Using this framework, we clarify when and how temperature alters consumer to resource biomass ratios, equilibrium resilience, consumer variability, extinction risk and transient vs. equilibrium dynamics. Finally, we characterise key asymmetries in species responses to temperature that produce these distinct dynamic behaviours and identify when they are likely to emerge. Overall, our framework provides a mechanistic and more unified understanding of the temperature dependence of trophic dynamics in terms of ecological rates, biomass ratios and stability.

Climate warming and predation risk during herbivore ontogeny.

Phenological effects of climate change are expected to differ among species, altering interactions within ecological communities. However, the nature and strength of these effects can vary during ontogeny, so the net community-level effects will be the result of integration over an individuals lifetime. I resolved the mechanism driving the effects of warming and spider predation risk on a generalist grasshopper herbivore at each ontogenetic stage and quantified the treatment effects on a measure of reproductive fitness. Spiders caused nymphal grasshoppers to increase the proportion of herbs in their diet, thus having a positive indirect effect on grasses and a negative indirect effect on herbs. Warming strengthened the top-down effect by affecting spiders and grasshoppers differently. In cooler, ambient conditions, grasshoppers and spiders had a high degree of spatial overlap within the plant canopy. Grasshopper position was unaffected by temperature, but spiders moved lower in the canopy in response to warming. This decreased the spatial overlap between predator and prey, allowing nymphal grasshoppers to increase daily feeding time. While spiders decreased grasshopper growth and reproductive fitness in ambient conditions, spiders had no effect on grasshopper fitness in warmed treatments. The study demonstrates the importance of considering the ontogeny of behavior when examining the effects of climate change on trophic interactions.

Local adaptation to temperature conserves top-down control in a grassland food web

A fundamental limitation in many climate change experiments is that tests represent relatively short-term ‘shock’ experiments and so do not incorporate the phenotypic plasticity or evolutionary change that may occur during the gradual process of climate change. However, capturing this aspect of climate change effects in an experimental design is a difficult challenge that few studies have accomplished. I examined the effect of temperature and predator climate history in food webs composed of herbaceous plants, generalist grasshopper herbivores and spider predators across a natural 4.8°C temperature gradient spanning 500 km in northeastern USA. In these grasslands, the effects of rising temperatures on the plant community are indirect and arise via altered predator–herbivore interactions. Experimental warming had no direct effect on grasshoppers, but reduced predation risk effects by causing spiders from all study sites to seek thermal refuge lower in the plant canopy. However, spider thermal tolerance corresponded to spider origin such that spiders from warmer study sites tolerated higher temperatures than spiders from cooler study sites. As a consequence, the magnitude of the indirect effect of spiders on plants did not differ along the temperature gradient, although a reciprocal transplant experiment revealed significantly different effects of spider origin on the magnitude of top-down control. These results suggest that variation in predator response to warming may maintain species interactions and associated food web processes when faced with long term, chronic climate warming.

The Body Size Dependence of Trophic Cascades

Trophic cascades are indirect positive effects of predators on resources via control of intermediate consumers. Larger-bodied predators appear to induce stronger trophic cascades (a greater rebound of resource density toward carrying capacity), but how this happens is unknown because we lack a clear depiction of how the strength of trophic cascades is determined. Using consumer resource models, we first show that the strength of a trophic cascade has an upper limit set by the interaction strength between the basal trophic group and its consumer and that this limit is approached as the interaction strength between the consumer and its predator increases. We then express the strength of a trophic cascade explicitly in terms of predator body size and use two independent parameter sets to calculate how the strength of a trophic cascade depends on predator size. Both parameter sets predict a positive effect of predator size on the strength of a trophic cascade, driven mostly by the body size dependence of the interaction strength between the first two trophic levels. Our results support previous empirical findings and suggest that the loss of larger predators will have greater consequences on trophic control and biomass structure in food webs than the loss of smaller predators.

Species interactions and a chain of indirect effects driven by reduced precipitation

Climate change can affect species directly and indirectly by altering interactions between species within communities. These indirect effects can ramify through a community and affect many species, including some that may not have been directly affected by the perturbation. Identifying these chains of indirect effects is difficult, and most studies only follow indirect effects across two or three species. Here, we use a factorial field experiment to demonstrate that precipitation affects spotted aphids through a complex chain of indirect interactions that are mediated by other herbivores and a generalist predator. We experimentally simulated drought, which reduced water content in alfalfa plants. While water stress in alfalfa had no direct effect on spotted aphids, it lowered the population growth rate of pea aphids, another common alfalfa pest. Because ladybeetle predators were attracted to high pea aphid densities, predator densities were lower in drought treatments. Consequently, spotted aphid densities were released from top-down control (apparent competition) in drought treatments and reached densities three times higher than spotted aphids in ambient treatments with high pea aphid densities. Thus, drought affected spotted aphids in the interaction chain: drought --> alfalfa --> pea aphids --> predators --> spotted aphids. This result illustrates the lengthy path that indirect effects of climate change may take through a community, as well as the importance of community-level experiments in determining the net effect of climate change.

Direct and indirect effects of warming on aphids, their predators, and ant mutualists.

Species exist within communities of other interacting species, so an exogenous force that directly affects one species can indirectly affect all other members of the community. In the case of climate change, many species may be affected directly and subsequently initiate numerous indirect effects that propagate throughout the community. Therefore, the net effect of climate change on any one species is a function of the direct and indirect effects. We investigated the direct and indirect effects of climate warming on corn leaf aphids, a pest of corn and other grasses, by performing an experimental manipulation of temperature, predators, and two common aphid-tending ants. Although warming had a positive direct effect on aphid population growth rate, warming reduced aphid abundance when ants and predators were present. This occurred because winter ants, which aggressively defend aphids from predators under control temperatures, were less aggressive toward predators and less abundant when temperatures were increased. In contrast, warming increased the abundance of cornfield ants, but they did not protect aphids from predators with the same vigor as winter ants. Thus, warming broke down the ant-aphid mutualism and counterintuitively reduced the abundance of this agricultural pest.

Reduced wind strengthens top-down control of an insect herbivore

Global wind speeds have decreased 5–15% over the last 30 years and are expected to continue decreasing in the future. However, little is known about how wind affects species and their interactions within communities. I experimentally tested the effects of wind on predator–prey interactions using soybean aphids and predatory multicolored Asian ladybeetles. First, I examined the direct effect of wind on aphids in a greenhouse without predators under three treatments: no wind, wind (oscillating fan), or simulated wind movement. Aphid abundances did not differ among treatments. Next, I conducted a field experiment in soybean plots assigned to either control or wind-block treatments. Predators were more abundant in wind-block treatments and reduced aphid abundance by 40% compared to control plots. To elucidate why wind indirectly increased aphid density in open plots, I conducted a feeding trial with ladybeetles foraging for aphids on plants that were assigned to either control or simulated wind movement treat...

On their best behavior: how animal behavior can help determine the combined effects of species interactions and climate change

The increasingly appreciated link between climate change and species interactions has the potential to help us understand and predict how organisms respond to a changing environment. As this connection grows, it becomes even more important to appreciate the mechanisms that create and control the combined effect of these factors. However, we believe one such important set of mechanisms comes from species’ behavior and the subsequent trait‐mediated interactions, as opposed to the more often studied density‐mediated effects. Behavioral mechanisms are already well appreciated for mitigating the separate effects of the environment and species interactions. Thus, they could be at the forefront for understanding the combined effects. In this review, we (1) show some of the known behaviors that influence the individual and combined effects of climate change and species interactions; (2) conceptualize general ways behavior may mediate these combined effects; and (3) illustrate the potential importance of including behavior in our current tools for predicting climate change effects. In doing so, we hope to promote more research on behavior and other mechanistic factors that may increase our ability to accurately predict climate change effects.