Jeff S. Wesner

Aquatic predation alters a terrestrial prey subsidy

Organisms with complex life histories (CLH) often cross habitat or ecosystem boundaries as they develop from larvae to adults, coupling energy flow between ecosystems as both prey (bottom-up) and consumers (top-down). Predation effects on one stage of this life cycle can therefore cascade across ecosystems, magnifying the impact of local predation. The majority of predation studies have assessed effects only on a local level, within the habitat of the predator. I used large outdoor stream mesocosms to test the hypothesis that predation in an aquatic habitat alters the magnitude and trophic structure of a prey assemblage in a terrestrial habitat. I also tested how a consumer in the terrestrial habitat (web-weaving spiders) responded to these changes in prey export. Two fish species were the predators (red shiner, Cyprinella lutrensis and orangethroat darter, Etheostoma spectabile) in an experiment with three treatments: both fish species monocultures plus a fishless control. Fish predation reduced aquatic insect emergence biomass by 50% compared to the fishless control and altered the trophic structure of the emergent community, reducing emerging insect predator biomass by 50%, but had no effect on other insect trophic groups. Spiders captured only insects that were unaffected by fish predation (mostly chironomids) and therefore did not respond numerically to overall changes in insect abundance or biomass. Patterns of insect emergence were largely driven by a strong negative relationship between fish and a predatory dragonfly (Pantala flavescens). The results of this experiment show that predation in one habitat can have strong effects on the biomass and trophic structure of subsidies entering adjacent habitats, resulting in contrasting predictions for the role of these subsidies in recipient food webs. In the absence of fish, aquatic habitats produced terrestrial insect communities with higher biomass (bottom-up potential) and a higher proportion of predators (top-down potential) than when fish were present.

Metamorphosis Enhances the Effects of Metal Exposure on the Mayfly, Centroptilum triangulifer

The response of larval aquatic insects to stressors such as metals is used to assess the ecological condition of streams worldwide. However, nearly all larval insects metamorphose from aquatic larvae to winged adults, and recent surveys indicate that adults may be a more sensitive indicator of stream metal toxicity than larvae. One hypothesis to explain this pattern is that insects exposed to elevated metal in their larval stages have a reduced ability to successfully complete metamorphosis. To test this hypothesis we exposed late-instar larvae of the mayfly, Centroptilum triangulifer, to an aqueous Zn gradient (32-476 μg/L) in the laboratory. After 6 days of exposure, when metamorphosis began, larval survival was unaffected by zinc. However, Zn reduced wingpad development at concentrations above 139 μg/L. In contrast, emergence of subimagos and imagos tended to decline with any increase in Zn. At Zn concentrations below 105 μg/L (hardness-adjusted aquatic life criterion), survival between the wingpad and subimago stages declined 5-fold across the Zn gradient. These results support the hypothesis that metamorphosis may be a survival bottleneck, particularly in contaminated streams. Thus, death during metamorphosis may be a key mechanism explaining how stream metal contamination can impact terrestrial communities by reducing aquatic insect emergence.

Metamorphosis alters contaminants and chemical tracers in insects: implications for food webs.

Insects are integral to most freshwater and terrestrial food webs, but due to their accumulation of environmental pollutants they are also contaminant vectors that threaten reproduction, development, and survival of consumers. Metamorphosis from larvae to adult can cause large chemical changes in insects, altering contaminant concentrations and fractionation of chemical tracers used to establish contaminant biomagnification in food webs, but no framework exists for predicting and managing these effects. We analyzed data from 39 studies of 68 analytes (stable isotopes and contaminants), and found that metamorphosis effects varied greatly. δ(15)N, widely used to estimate relative trophic position in biomagnification studies, was enriched by ∼ 1‰ during metamorphosis, while δ(13)C used to estimate diet, was similar in larvae and adults. Metals and polycyclic aromatic hydrocarbons (PAHs) were predominantly lost during metamorphosis leading to ∼ 2 to 125-fold higher larval concentrations and higher exposure risks for predators of larvae compared to predators of adults. In contrast, manufactured organic contaminants (such as polychlorinated biphenyls) were retained and concentrated in adults, causing up to ∼ 3-fold higher adult concentrations and higher exposure risks to predators of adult insects. Both food web studies and contaminant management and mitigation strategies need to consider how metamorphosis affects the movement of materials between habitats and ecosystems, with special regard for aquatic-terrestrial linkages.

Multiple predators indirectly alter community assembly across ecological boundaries

Models of habitat selection often assume that organisms choose habitats based on their intrinsic quality, regardless of the position of these habitats relative to low-quality habitats in the landscape. We created a habitat matrix in which high-quality (predator-free) aquatic habitat patches were positioned adjacent to (predator-associated) or isolated from (control) patches with single or two species of caged predators. After 16 days of colonization, larval insect abundance was reduced by 50% on average in both the predator and predator-associated treatments relative to isolated controls. Effects were largely similar among predator treatments despite variation in number of predator species, predator biomass, and whether predators were native or nonnative. Importantly, the strength of effects did not depend on whether predators were physically present. These results demonstrate that predator cues can cascade with equal strength across ecological boundaries, indirectly altering community assembly via habitat selection in intrinsically high-quality habitats.

Synthesis: comparing effects of resource and consumer fluxes into recipient food webs using meta-analysis.

Here we synthesize empirical research using meta-analysis to compare how consumer and resource fluxes affect recipient food webs. We tested the following hypotheses: (H1) The direct effects of resource fluxes (bottom-up) should be stronger than the direct effects of consumer fluxes (top-down), because resource fluxes are permanent (do not return to the food web in which they were produced) but consumer fluxes may not be (consumers can leave). (H2) Following H1, the indirect effects should attenuate (weaken) more quickly for consumer fluxes than for resource fluxes due to their direct effects being weaker, (H3) The effects of resource fluxes should be stronger when recipient food webs are in different ecosystems than donor food webs due to differences in elevation that accompany cross-ecosystem food web interfaces, often increasing flux quantity due to gravity, while the effects of consumer fluxes should be stronger when donor and recipient food webs are in the same ecosystem as they should more easily assimilate into the recipient food web. We found no differences in the magnitude of bottom-up and top-down direct effects for resource and consumer fluxes, but top-down direct effects were 122% stronger than top-down indirect effects. Indirect effects of prey and predator fluxes quickly attenuated while indirect effects of non-prey resource and herbivore fluxes did not, as the overall direct effects of prey and predator fluxes were 123% and 163% stronger than their indirect effects, respectively. This result suggests that the magnitude of indirect effects decrease as the trophic level of resource and consumer fluxes increases, and also contrasts with results from studies showing in situ top-down indirect effects are stronger than in situ bottom-up indirect effects. We found that resource and consumer flux effect sizes were similar when they occurred between ecosystems, but when they occurred within ecosystems predator flux effects were 107% stronger than nutrient flux effects. Finally, we found that observational studies had higher effect sizes than manipulative studies. Future research should focus on how resource and consumer fluxes might interact and generate feedbacks in empirical studies of natural food webs, and what ecological factors might affect their relative strength.

Contrasting effects of fish predation on benthic versus emerging prey: a meta-analysis

Predator–prey interactions are often studied entirely within the ecosystem of the predator. However, many prey transition between ecosystems during development, expanding the effects of predators across ecosystems. Prey are often vulnerable to predation during this transition, facing a predator gauntlet as they leave their source ecosystem. As a result of predation during this transition, predators may have stronger effects on prey fluxes to the neighboring ecosystem than on prey densities in the predator’s own ecosystem. I used meta-analysis of predator (fish) and prey (invertebrate) interactions in freshwater ecosystems to test the hypothesis that fish have stronger effects on prey flux to the terrestrial ecosystem, by reducing insect emergence biomass, than on prey densities in the aquatic ecosystem, by reducing benthic insect/invertebrate biomass. Fish reduced insect emergence by 39xa0% on average, more than twice as strong as their reductions of benthic prey (16xa0% reduction; averages are variance-weighted). In fact, fish effects on benthic prey were not significantly different from zero, but were significant for emergence. These results indicate that predator effects can not only cascade from one ecosystem to another but also that effects can be stronger outside than within the ecosystem of the predator. Failure to account for this may underestimate the effects of predators on prey.

Fish predation alters benthic, but not emerging, insects across whole pools of an intermittent stream

Abstract.u2003 Predation effects in streams can cascade to terrestrial food webs through the flux of organisms that develop in the stream and emerge as adults to the terrestrial system. This emergence subsidizes some terrestrial predators, an effect that generally varies based on the magnitude of the subsidy. Factors regulating this magnitude are relatively well known, but factors regulating the trophic structure of the subsidy are not. I tested the hypothesis that predatory fish in natural stream pools alter the biomass and trophic structure (proportion of predatory adults) of emerging aquatic insects. I created a 13× gradient of predatory fish biomass (4 species of Lepomis sunfish and the minnow Notropis boops; within the range of natural variation) across 10 pools in Brier Creek, Oklahoma (USA). Pool area and substrate composition varied naturally, so I also measured their effect on insects. At the end of the experiment after the stream became intermittent, fish reduced benthic insect biomass but not emergence to the terrestrial habitat. The proportion of predatory insects emerging from pools was positively associated with pool area, but was unaffected by fish density. The best predictor of emergence biomass among pools on any date was the standing crop of benthic insects before fish manipulation, a result suggesting a time lag between measured benthic standing crop in the stream and subsequent emergence. Fish manipulations occurred during the end of peak summer insect emergence, which may have limited my ability to detect fish effects on emergence. My study demonstrates that variation in the timing of predation may constrain the spatial scale of fish effects in aquatic and terrestrial food webs and suggests that pool size can influence the trophic structure of emerging aquatic insects.

Habitat selection and consumption across a landscape of multiple predators

Predator community composition can alter habitat quality for prey by changing the strength and direction of consumptive effects. Whether predator community composition also alters prey density via nonconsumptive effects during habitat selection is not well known, but is important for understanding how changes to predator communities will alter prey populations. We tested the hypothesis that predator community composition (presence of caged trout, caged dragonflies, or caged trout + dragonflies) alters colonization of aquatic mesocosms by ovipositing aquatic insects. In a previous experiment in this system, we found a spatial contagion effect, in which insects avoided pools with predators, but only when predator-free pools were isolated (∼5 m away from predator pools). Here, we removed the isolated predator-free pools, allowing us to test whether insects would make fine-scale (∼1 m) oviposition decisions in the absence of preferred isolated pools. We also estimated consumptive effects by allowing predators to feed on colonists for 5 days following colonization. All insects collected after 21 days were dipterans, dominated by Chironomidae. Total colonization, measured as the number of developing larvae after 21 days, was not affected by either predator presence or composition. Consumption was significant in the trout only treatment, reducing larval insect density by 46 ± 37% (mean ± SE). No other predator treatment significantly reduced prey density, although the proportion of chironomid larvae in protective cases increased in response to direct predation from dragonflies, indicating an antipredatory behavioral response. Taken together, these results reveal that predator community composition altered larval survival and behavior, but colonizing females either did not or could not assess these risks across small scales during oviposition.

Shoaling species drive fish assemblage response to sequential large floods in a small midwestern U.S.A. stream

I assessed the short-term impact of two sequential scouring floods on the fish assemblage of a small prairie stream. I tested for changes in fish abundance, fish assemblage composition, and fish-habitat associations within individual pools and across a suite of pools following each flood. Before the second flood, 30–90% of fish were removed by seining in five of eight pools. Overall fish abundance was reduced by approximately 50% following the first flood, but effects varied widely among individual pools. Fish abundance was unaffected by the second flood, despite prior removal of a known proportion of fish, suggesting recolonization of defaunated pools during the flood. Fish assemblage similarity across the entire suite of pools was low following each flood, but varied considerably within individual pools. Defaunated pools were more similar to pre-flood assemblages than control pools, though the mechanism behind this pattern was unclear. Changes in abundance and assemblage composition were driven by interpool movement of two minnow species with the shared behavioral trait of shoaling: bigeye shiner Notropis boops and central stoneroller Campostoma anomalum. Shifts in abundance showed no upstream or downstream pattern, suggesting that flooding allowed fish to move actively among pools that are typically isolated by partial barriers (riffles). This study highlights the importance of considering species’ behavioral traits when assessing the impacts of flooding, and suggests that shoaling behavior may be useful trait for predicting fish assemblage change following flooding.

Metamorphosis Affects Metal Concentrations and Isotopic Signatures in a Mayfly (Baetis tricaudatus): Implications for the Aquatic-Terrestrial Transfer of Metals

Insect metamorphosis often results in substantial chemical changes that can alter contaminant concentrations and fractionate isotopes. We exposed larval mayflies (Baetis tricaudatus) and their food (periphyton) to an aqueous zinc gradient (3-340 μg Zn/l) and measured zinc concentrations at different stages of metamorphosis: larval, subimago, and imago. We also measured changes in stable isotopes (δ15N and δ13C) in unexposed mayflies. Larval zinc concentrations were positively related to aqueous zinc, increasing 9-fold across the exposure gradient. Adult zinc concentrations were also positively related to aqueous zinc, but were 7-fold lower than larvae. This relationship varied according to adult substage and sex. Tissue concentrations in female imagoes were not related to exposure concentrations, but the converse was true for all other stage-by-sex combinations. Metamorphosis also increased δ15N by ∼0.8‰, but not δ13C. Thus, the main effects of metamorphosis on insect chemistry were large declines in zinc concentrations coupled with increased δ15N signatures. For zinc, this change was largely consistent across the aqueous exposure gradient. However, differences among sexes and stages suggest that caution is warranted when using nitrogen isotopes or metal concentrations measured in one insect stage (e.g., larvae) to assess risk to wildlife that feed on subsequent life stages (e.g., adults).