Keystone predation: trait‐based or driven by extrinsic processes? Assessment using a comparative‐experimental approach

Abstract

Keystone predation can be a determinant of community structure, including species diversity, but factors underlying “keystoneness” have been minimally explored. Using the system in which the original keystone, the sea star Pisaster ochraceus, was discovered, we focused on two potential (but overlapping) determinants of keystoneness: intrinsic traits or state variables of the species (e.g., size, density), and extrinsic environmental parameters (e.g., prey productivity) that may provide conditions favorable for keystone predator evolution. Using a comparative‐experimental approach, with repeated field experiments at multiple sites across a variable coastal environment, we tested predation rates, or how quickly predators consumed prey, and predation effects, or community response to predator presence or absence. We tested five hypotheses: (H1) predation rates and effects will vary in space but not time; (H2) per population predation rates will vary primarily with individual traits and population variables; (HJHH3) per capita predation rates will vary only with individual traits; (H4) predation effects will vary with traits, variables, and external drivers; and (H5) as predicted by the keystone predation hypothesis, diversity will vary unimodally with predation pressure. As hypothesized, predation rates differed among sites but not over time (H1), and in caging exclusion experiments, predation effect varied with both intrinsic and extrinsic factors (H4). Unexpectedly, predation rates varied with both intrinsic and extrinsic (H2, per population), or only with extrinsic (H3, per capita) factors. Further, in large‐plot exclusion experiments, predation effect was most closely associated with individual traits (contra H4). Finally, taxon diversity varied unimodally with proxies of predation pressure (sessile prey abundance) and was sensitive to extrinsic factors (mussel growth, temperature, and upwelling, H5). Hence, keystoneness depended on predator individual traits, predator population variables, and environmental parameters. However, temporal differences in caging experiments suggested that environmental characteristics underlying prey dynamics may be preeminent. Compared to prior experiments, predation was weaker with low prey input compared to periods with high prey input. Collectively, our results suggest that keystone predator evolution depends on the coalescence of species‐specific characteristics, and environmental parameters favoring high prey productivity. Our approach may be a model for future studies exploring the generality of keystoneness.

Quantitative biogeography: Decreasing and more variable dynamics of critical species in an iconic meta‐ecosystem

“…Sea star reproduction was severely affected by SSW and is still low but showed some signs of recovery from 2014 to 2019. As expected from growth rate differences (sea stars grow fastest in Region 3; Menge, Foley, et al, 2021), reproductive output was higher in Region 3 than in Regions 2 or 5. Predation rate was also sharply reduced due to SSW-caused losses of large sea stars, and has shown only modest recovery since 2015, but the rank order of predation rate in space continues to be as documented prior to 2014.…”

“…Besides often severe, mostly winter‐time wave action, the dominant oceanic feature of the Oregon coast is intermittent upwelling from April through September, and predominance of downwelling conditions from October through March (Checkley & Barth, 2009; Hickey & Banas, 2003; Huyer, 1983). All study sites have been described in recent publications (e.g., Close et al, 2020; Hacker et al, 2019; Menge et al, 2015; Menge, Foley, et al, 2021). Briefly, all were wave‐exposed rocky intertidal benches with mussel‐dominated mid intertidal zones, and fucoid‐ and barnacle‐dominated high intertidal zones.…”

Predatory Bacteria Select for Sustained Prey Diversity

“…By imposing predatory selection on prey, predators can increase diversity within prey communities and populations by diverse mechanisms. For example, keystone predators can promote diversity by targeting the most dominant prey species and thereby increasing resources available for other prey species [27][28][29]41,42]. Predation can ameliorate competitive exclusion among competing prey species by promoting prey that are less competitive at low predation pressure but less susceptible to predation by a dominant predator [10,43].…”

Mistletoe infection changes arthropod community on its cactus host through indirect effects

“…Although it has been emphasised the role of predators as initiators of indirect effects and their key roles in structuring communities (top‐down trophic pathways) (Hairston et al ., 1960; Paine, 1966; Schmitz, 2003; Menge et al ., 2021), theoretically any organism at any taxonomic level can act as initiator, transmitter or receiver species (Wootton, 1994; Pearson, 2010). In the context of trait‐mediated indirect interactions (TMIIs; Ohgushi et al ., 2012), here we show the role of a parasitic plant (mistletoe) as the initiator of a phenotypic change that cascades into the arthropod community associated with its host (cactus), as follows: (i) induction of cactus susceptibility to stem‐borers by way of decreasing tissue toughness; (ii) generation of structural changes in cacti by stem‐borers (construction of brood chambers) that result in new habitats, which are quantitative and qualitatively superior to those built on non‐parasitised cacti; and (iii) enhanced colonisation of those new habitats by arthropods, thereby modifying community composition and diversity (Fig.…”