Context Dependency of Species Interactions

The sign and strength of species interactions can vary with biotic and abiotic context. For example, under an environmentally stressful condition, two species that normally compete for resources may work together to reduce the impact of stress. Although much research has demonstrated how two species may interact differently across a single environmental gradient, much remains to be done. For instance, there is still uncertainty associated with how interactions among three or more species (e.g., trophic cascades) vary across environmental gradients. Furthermore, groups of species likely interact in environments with multiple biotic and abiotic factors that change asynchronously across the landscape and over time. Given the anthropogenic changes to climate and biodiversity, the study of species interactions across multiple environmental contexts is needed in order for community ecology to become a more predictive discipline.

The biogeography of trophic cascades

Predators can indirectly benefit prey populations by suppressing mid-trophic level consumers, and these indirect effects can influence the biodiversity and functioning of coastal ecosystems. However, the strength and outcome of these predator effects may vary across physical and biological biogeographic gradients, and thus extrapolating results from one region to another is often problematic. Moreover, this mismatch between the scale of ecological studies and the biogeographic range at which species interactions occur fundamentally inhibits our understanding of linkages between community ecology and ecosystem processes, as well as our ability to manage these systems.

With collaborators from the University of North Carolina, the University of Georgia, and Northeastern University, we surveyed oyster reef communities across a 1000-km coastal region from North Carolina to northern Florida (the Southeast Atlantic Bight). We then conducted simultaneous manipulative field experiments across this region to ask:

How do predators on oyster reefs alter ecosystem function through consumptive and non-consumptive effects?

Are the effects of these predators on ecosystem function consistent across the biogeographic region?

We found that densities of oyster consumers were weakly influenced by predators at all sites. However, consumer foraging behavior varied considerably across sites in the presence of predators, and these behavioral effects altered the trophic cascade across space. Variability in consumer behavior was linked to regional gradients in oyster recruitment to and sediment accumulation on reefs. Specifically, asynchronous gradients in these factors influenced whether the benefits of suppressed consumer foraging on oyster recruits exceeded costs of sediment accumulation resulting from decreased consumer activity. Thus, although predation on consumers remains consistent, predator influences on behavior do not; rather, they interact with environmental gradients to cause biogeographic variability in the net strength of trophic cascades.

Mudcrab and oyster drill – the consumers on the mid-trophic level used in the field experiment.

Kimbro, D. L., J. E. Byers, J. H. Grabowski, A. R. Hughes, M. F. Piehler. 2014. The biogeography of trophic cascades on US oyster reefs. Ecology Letters 17 (7): 845-854

Tidal regime dictates the cascading effects of multiple predators on a marsh plant in the NW Gulf of Mexico

When prey detect a predator, the prey must behaviorally balance the need to avoid being eaten with the need to consume resources. Differences in the environment, which may influence the way that prey perceive predators, may result in differences in this behavioral response. In this study, I was interested in how physical processes influenced prey perception of predators, the subsequent behavior of prey, and consequent effects of this behavior on a basal resource.

In Spartina alterniflora systems in the Southeast, snails feed on dead plant material (detritus) on the ground, as well as on fungus growing on Spartina leaves. The snails farm the fungus by slicing open the leaves, which are then colonized by a fungal infection. If this “fungal farming” becomes too intense, the plants may become stressed and die.

The snails will climb up Spartina plants at high tide in order to avoid predators such as blue crabs and crown conchs. Given that tides dictate how often and how long predators are present in the marshes, I wondered whether geographic differences in tidal regime (diurnal vs. semidiurnal) could result in differences in snail climbing behavior, the intensity of fungal farming, and plant damage.

Snails climbing Spartina alterniflora

On the panhandle of Florida, coastlines to the west experience diurnal tides (12 hours flood and 12 hours ebb each day), whereas coastlines to the east experience semidiurnal mixed tides (2 low tides and 2 high tides that are each 6 hours). In the field, I found that Spartina was less productive and had more snail-farming scars along shorelines with diurnal tides than along shorelines with semidiurnal tides. This pattern occurred despite there being equal numbers of snails and predators along both shorelines, so it was clear that densities or consumptive effects were not driving this pattern.

I next conducted a lab experiment crossing tidal regime with several predator treatments. These treatments allowed me to distunguish between the consumptive and non-lethal effects of two different predators on snails. I found that:

(1) Predators caused snails to ascend Spartina regardless of tidal regime and predator identity.

(2) Regardless of tidal regime, blue crabs consumed more snails than crown conchs, and the highest snail consumption was seen when both predators were present. In other words, consumptive effects were consistent across tidal schedules.

(3) In the presence of predators, snail grazing on Spartina was greater under the diurnal tidal schedule than under the semidiurnal tidal schedule. In fact, the snails subject to semidurnal tides had no net effect on Spartina.

The tidal schedule therefore dictated the strength of non-lethal predator effects, and whether predator cues indirectly benefitted or harmed Spartina through their effects on snail predator-avoidance and farming behavior. These results match the patterns observed in nature. We can see how the same assemblage of predator and prey can function differently in slightly different environments due to effects on prey behavior.

Kimbro, D. L. 2012. Tidal regime dictates the cascading consumptive and nonconsumptive effects of multiple predators on a marsh plant. Ecology 93(2): 334-344.

The benefit of a trait-mediated trophic cascade on oysters dampens but then rebounds over time

A quarter century of research has demonstrated that predators can alter prey traits such as behavior, morphology, and growth and that such nonconsumptive effects (NCEs) can cascade across multiple trophic levels in food webs to alter community composition and ecosystem function. Indeed, experimental evidence from a range of study systems suggests that predator NCEs may equal or sometimes exceed the consumptive effect (CE) of predators. Consequently, a primary focus of ecology over the last decade has been the use of controlled experiments to understand how the relative importance of CEs and NCEs depends on resource supply, predator diversity, habitat complexity, and more recently, climate change. Clearly, another experimental test about the importance of NCEs under a variety of contexts is not novel.

However, the growing number of NCE experiments has been met with several key critiques about their design: most experiments are conducted in laboratory settings, are concluded too soon to allow for changes in prey state, and utilize treatments (predator cue versus no-cue treatments) that do not represent how predators function in nature. Thus, it is reasonable to consider whether the collection of experimental results merely describes the potential importance of NCEs, rather than their actual importance in natural systems.

In light of these critiques, we re-evaluated a toadfish (predator), crab (prey), and oyster (resource) system that had been shown by our previous, short-term experiments to display a strong NCE-mediated trophic cascade. In a four-month field experiment, we varied toadfish cue (NCE) and crab density (approximating variation in predator consumptive effect, CE) on 1.25 m² replicate oyster reefs. Our results supported two key theoretical predictions: that NCEs weaken when measured over longer time scales, but may reemerge and oscillate because of variation in prey state; and that CEs rather than NCEs are the primary driver of long-term, population and ecosystem-level consequences of predation. These results can help inform a vigorous debate within the broader field of ecology about the proper scale at which to estimate the relative strength of NCEs, and the degree to which common experimental approaches successfully isolate and reveal NCEs versus introducing artifacts that inflate their perceived influence.

Figure 1. Diagram of direct (solid lines) and indirect (dashed lines) interactions by which a toadfish predator can influence the community structure and ecosystem functioning of intertidal oyster reefs. Black solid line illustrates the direct consumptive effect (CE) of toadfish predation on the density of mud crabs, which can indirectly (black dashed line) influence oyster survival and consequently alter ecosystem properties, because suspension feeding by oysters leads to benthic-pelagic coupling and augmentation of sediment organic matter (SOM). Gray solid line illustrates the direct nonconsumptive effect (NCE) of toadfish cue on the foraging behavior of mud crabs, which can also indirectly (gray dashed line) influence the survivorship of oysters and SOM production. Drawing by T. Rogers.

Figure 2. Proportional survivorship of juvenile oysters (vertical axis) as a function of mud crab density (axis) over a series of 19-day trials spanning the 163-day experiment. Dates of each trial are given in the panel. Mud crabs consume juvenile oysters, and were either exposed (open triangles, dotted curve) or not (closed circles, solid curve) to cues from an enclosed toadfish (a mud crab predator). The gradient in mud crab density approximates the consumptive effect of a predator on mud crab density (high density = weak CE, and vice versa). Lines indicate the fit of a generalized linear model (binomial error; logit link); shading indicates 95% confidence interval on the regression line.

Kimbro, D.L., J.H. Grabowski, A.R. Hughes, M.F. Piehler, J.W. White. 2017. Nonconsumptive effects of a predator weaken then rebound over time. Ecology 98(3), 656-667.

Quantifying the influence of nonconsumptive predator effects on prey population dynamics

Currently, the Kimbro Lab is working on a new project in Florida in collaboration with Dr. Will White at Oregon State University. Working closely with the Guana Tolomato Matanzas National Estuarine Research Reserve, we are quantifying the importance of nonconsumptive effects of predators on Crassostrea virginica (Eastern oyster) throughout the estuary. Through large scale surveys, field caging experiments, and monitoring the growth and survival of outplanted oysters, a model will be created to help to aid future restoration efforts.

As other work within the lab has shown, predators affect their prey in ways other than by eating them. They can also affect prey behavior, which can have cascading effects to other trophic levels. However, the importance of these effects, especially in comparison to consumptive effects, is unclear. By looking at the response of oysters to their prey, mudcrabs and crown conch, we will first determine what the effects are of the oysters’ exposure to their predators. Then, we will create two models: one that includes these effects, and one that does not. We will then test both of these models, to see which more accurately describes the system. In this way, we can determine the importance of nonconsumptive effects on prey population dynamics.

This work was featured in the GTMNERR’s blog.