Past selection impacts the strength of an aquatic trophic cascade

Abstract

In complex food webs, interactions among species in different trophic levels can generate cascading indirect effects that couple top predators with primary producers, thereby affecting ecosystem functioning. Natural selection imposed by top predators on intermediate predators may play a role in shaping the strength of these trophic cascades, but this conjecture remains largely untested. To determine the effects of natural selection on the strength of trophic cascades, we conducted a two‐part experiment in a four‐level aquatic trophic system involving a top predator (fish), an intermediate predator (damselflies), herbivores (zooplankton) and primary producers (algae). We first quantified how predation by fish generated selection on damselfly activity levels after controlling for phenotypic plasticity. We then measured the indirect effects of this selection on primary production (phytoplankton biomass). In both experiments, we varied the density of predators, allowing us to elucidate both trait‐mediated and density‐mediated indirect effects. We found that as fish density increased, damselfly survivorship declined, which generated natural selection favouring less active damselflies. These results are robust after taking into account latent effects of plasticity in response to fish predator cues. The surviving damselflies likely foraged less, freeing herbivores from predation, which in turn reduced primary production. This selection‐driven trait‐mediated indirect effect was only apparent at low damselfly densities, because the consumptive effect of damselflies at high densities overwhelmed the effects of past selection. These results demonstrate how the past action of natural selection imposed by predators affects the phenotypes of prey that consume herbivores, which ultimately influences primary productivity—a selective trophic cascade. Natural selection can therefore act as a mechanism coupling ecological dynamics across trophic levels, which ultimately influences ecosystem functioning. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13102/suppinfo is available for this article.

Feedbacks link ecosystem ecology and evolution across spatial and temporal scales: Empirical evidence and future directions

“…Eco‐evolutionary feedbacks in aquatic ecosystems have been studied primarily through the perspectives of trophic interactions and nutrient recycling (Matthews, Narwani et al, ; Post & Palkovacs, ; Schoener, ). The presence of eco‐evo feedbacks in aquatic microcosms is now incontrovertible with evidence for eco‐evo effects outside of laboratory experiments for a wide variety of aquatic taxa, including zooplankton (Matthews, Hausch, Winter, Suttle, & Shurin, ; Miner, Meester, Pfrender, Lampert, & Hairston, ), aquatic macroinvertebrates (Ousterhout, Graham, Hasik, Serrano, & Siepielski, ), amphibians (Reinhardt, Steinfartz, Paetzold, & Weitere, ; Urban, ) and fishes (Auer et al, ; Carlson, Quinn, & Hendry, ; Fryxell & Palkovacs, ; Tuckett, Simon, & Kinnison, ). Here, we detail evidence for feedbacks in three fish study systems—alewife, guppies and threespine stickleback in the context of Figure .…”

Predators weaken prey intraspecific competition through phenotypic selection

“…We focused on predator‐prey interactions between centrarchid fish and larvae of the orange bluet ( Enallagma signatum ), a common damselfly found in our Northwestern Arkansas study region. Enallagma are mid‐trophic level ambush predators found in many lakes, where the larvae inhabit macrophytes, feed on smaller invertebrates, and are fed upon by themselves and larger predators, especially fish (McPeek 1990; McPeek 1998; McPeek & Brown 2000; Ousterhout et al 2018). Fish predation has repeatedly been shown to select for reduced activity levels in damselflies (Strobbe et al 2011; Swaegers et al 2017; Ousterhout et al 2018).…”

“…Enallagma are mid‐trophic level ambush predators found in many lakes, where the larvae inhabit macrophytes, feed on smaller invertebrates, and are fed upon by themselves and larger predators, especially fish (McPeek 1990; McPeek 1998; McPeek & Brown 2000; Ousterhout et al 2018). Fish predation has repeatedly been shown to select for reduced activity levels in damselflies (Strobbe et al 2011; Swaegers et al 2017; Ousterhout et al 2018). Selection operates in this stereotypical way because damselflies attract fish when swimming (Baker et al 1999) and cannot swim away fast enough to evade fish (McPeek 2000; Stoks & De Block 2000); therefore reducing activity helps damselflies avoid detection (Strobbe et al 2011).…”

“…We then manipulated damselfly densities in these activity level distributions to understand how intraspecific competition may be affected by selection on activity. Our previous work found that the strength of selection on damselfly activity varies with fish densities (Ousterhout et al 2018), as the strength of selection on prey is expected to increase with prey mortality (Benkman 2013). It follows then, that as fish densities increase, stronger selection for reduced activity should weaken the strength of intraspecific competition in the wild.…”

Predation risk and habitat complexity modify intermediate predator feeding rates and energetic efficiencies in a tri‐trophic system

“…Species are embedded within communities and the strengths of predator-prey interactions depend on direct interactions between the predator and its prey but also on indirect interactions mediated through one or more species (Schmitz, Krivan, & Ovadia, 2004;Sentis, Gémard, Jaugeon, & Boukal, 2017;Werner & Peacor, 2003). While food-web studies traditionally focus on trophic interactions in single predator-prey systems, multiple studies have highlighted the importance of indirect density-and trait-mediated effects for the strengths of species interactions in ecological communities (Davenport & Chalcraft, 2013;McCoy, Stier, & Osenberg, 2012;Okuyama & Bolker, 2007;Ousterhout, Graham, Hasik, Serrano, & Siepielski, 2018;Werner & Peacor, 2003). For instance, prey are typically less active and feed less in the presence of a predator or its cues (Hawlena & Schmitz, 2010b;Stoks & McPeek, 2003;Trussell, Ewanchuk, & Bertness, 2003), which may indirectly alter species interaction strengths between the prey and their resources.…”