Loss of foundation species: disturbance frequency outweighs severity in structuring kelp forest communities

Abstract

Disturbances often cause the disproportionate loss of foundation species but understanding how the frequency and severity of disturbance to such organisms influence biological communities remains unresolved. This gap in knowledge exists in part because of the rarity of ecologically meaningful studies capable of disentangling different elements of disturbance. Hence, we carried out a long‐term (9 yr), large‐scale (2,000 m2 plots), spatially replicated (4 sites) field experiment in which we manipulated disturbance to a globally distributed marine foundation species, the giant kelp Macrocystis pyrifera, and tracked community responses over time. To distinguish the effects of disturbance frequency and severity on the biodiversity and composition of temperate rocky reef communities, we simulated the repeated loss of giant kelp from destructive winter waves across a background of natural variation in disturbance. By following the response of over 200 taxa from the surrounding community, we discovered that the frequency of disturbance to giant kelp changed the biomass, diversity, and composition of community guilds in a manner commensurate with their dependence on the physical (i.e., benthic light and space), trophic (i.e., living and detrital biomass), and habitat (i.e., biogenic structure) resources mediated by this foundation species. Annual winter disturbance to giant kelp reduced living and detrital giant kelp biomass by 57% and 40%, respectively, enhanced bottom light by 22%, and halved the seafloor area covered by giant kelp holdfasts. Concomitantly, the biomass of understory algae and epilithic sessile invertebrates more than doubled, while the biomass of rock‐boring clams, mobile invertebrates, and fishes decreased 30–61%. Frequent loss of giant kelp boosted understory algal richness by 82% and lowered sessile invertebrate richness by 13% but did not affect the biodiversity of mobile fauna. In contrast to changes driven by disturbance frequency, interannual variation in the severity of disturbance to giant kelp had weaker, less consistent effects, causing only modest changes in assemblages of sessile invertebrates, mobile invertebrate herbivores, and fishes. Our results broaden the foundation species concept by demonstrating that repeated disturbance to a dominant habitat‐forming species can outweigh the influence of less frequent but severe disturbances for the surrounding community.

Species insurance trumps spatial insurance in stabilizing biomass of a marine macroalgal metacommunity

“…The stronger stabilizing effect of asynchronous species dynamics could stem from several factors, including lifehistory trade-offs that lead to niche differentiation among species. For instance, the algae in this study have different levels of tolerance to shading (Harrer et al 2013), causing some species to be favored over others as the giant kelp canopy waxes and wanes (Miller et al 2011, Castorani et al 2018. Algal species also differ in their susceptibility to removal by grazing and wave disturbance, leading to community shifts as sea urchin populations and wave events fluctuate (Ebeling et al 1985, Harrold andReed 1985).…”

“…, Castorani et al. ). Algal species also differ in their susceptibility to removal by grazing and wave disturbance, leading to community shifts as sea urchin populations and wave events fluctuate (Ebeling et al.…”

Foundation species promote community stability by increasing diversity in a giant kelp forest

“…The stabilizing path involving species richness is supported in part by observations of increased diversity in the presence of foundation species (Kikvidze et al , Miller et al ). Other lines of evidence show that foundation species reduce abiotic stress (Kikvidze et al ), alter resources (Castorani et al ), provide refuge from predators and competitors (Dayton , Stachowicz , Canion and Heck ), and provide nursery habitat (Heck et al ) for many species. Thus, foundation species have the capacity to promote community stability by directly enhancing the stability of individual species and the degree of asynchronous fluctuations among them.…”

“…In this study, we used the Thibaut and Connolly framework to explore the bounds of DSRs in nature and the role of foundation species in underpinning them. We focused on a taxonomically and phylogenetically diverse assemblage of primary space holders (understory algae and sessile suspension‐feeding invertebrates) on temperate rocky reefs that thrive beneath the canopy of the giant kelp ( Macrocystis pyrifera ), an iconic foundation species (Graham , Castorani et al , Miller et al ). We hypothesized that aggregate community biomass should be more stable on reefs where giant kelp biomass is also more stable.…”

Alternative responses to rare selection events are differentially vulnerable to changes in the frequency, scope, and intensity of environmental extremes

“…The ideas discussed here may also be useful for predicting the potential interactive effects of different aspects of climate change and anthropogenic action (Castorani, Reed, & Miller, 2018;Miller, Roxburgh, & Shea, 2011). For example, fire suppression practices have not only decreased the frequency of wildfires in large areas of the world, but have also intensified the fires that actually occur due to the increased buildup of fuel (Miller, Safford, Crimmins, & Thode, 2009;Scott, Bowman, Bond, Pyne, & Alexander, 2014;Steel, Safford, & Viers, 2015).…”