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

Abstract

Because natural ecosystems are complex, it is difficult to predict how their variability scales across space and levels of organization. The species‐insurance hypothesis predicts that asynchronous dynamics among species should reduce variability when biomass is aggregated either from local species populations to local multispecies communities, or from metapopulations to metacommunities. Similarly, the spatial‐insurance hypothesis predicts that asynchronous spatial dynamics among either local populations or local communities should stabilize metapopulation biomass and metacommunity biomass, respectively. In combination, both species and spatial insurance reduce variation in metacommunity biomass over time, yet these insurances are rarely considered together in natural systems. We partitioned the extent that species insurance and spatial insurance reduced the annual variation in macroalgal biomass in a southern California kelp forest. We quantified variability and synchrony at two levels of organization (population and community) and two spatial scales (local plots and region) and quantified the strength of species and spatial insurance by comparing observed variability and synchrony in aggregate biomass to null models of independent species or spatial dynamics based on cyclic‐shift permutation. Spatial insurance was weak, presumably because large‐scale oceanographic processes in the study region led to high spatial synchrony at both population‐ and community‐level biomass. Species insurance was stronger due to asynchronous dynamics among the metapopulations of a few common species. In particular, a regional decline in the dominant understory kelp species Pterygophora californica was compensated for by the rise of three subdominant species. These compensatory dynamics were associated with positive values of the Pacific Decadal Oscillation, indicating that differential species tolerances to warmer temperature and nutrient‐poor conditions may underlie species insurance in this system. Our results illustrate how species insurance can stabilize aggregate community properties in natural ecosystems where environmental conditions vary over broad spatial scales.

Scaling‐up biodiversity‐ecosystem functioning research

“…For example, the change in IAR with spatial extent is explained by the distance‐dependent decay in synchrony in growth dynamics (Wang et al ; Delsol et al ) that is altered by local and regional environmental variability, and turnover in diversity among assemblages (Thibaut and Connolly 2013; Wang et al ). Ultimately, the magnitude and stability of ecosystem functioning at different scales depends upon whether environmental conditions, movement and trophic interactions synchronise or desynchronise species or functional groups (Ives et al ; Gonzalez & Loreau ; Gouhier et al ; Wang et al ; Lamy et al ).…”

The dual nature of metacommunity variability

“…Second, we found relatively high degree of compositional spatial synchrony. This result shows that most local communities underwent similar compositional trajectories, in particular, major declines of the dominant species that were partially compensated for by the increase of the three sub-dominant species (Lamy et al 2019). Our empirical case study is therefore akin to the spatial synchrony scenario displayed in Figure 4.…”

“…As a result, compositional variability of the metacommunity mirrored that of local communities, which exhibited large compositional shifts that would have been undetected from aggregate properties alone (Figure 2B). Indeed, this higher compositional spatial synchrony captures the fact that most local communities underwent similar trajectories, in particular, major declines of the dominant species that were partly compensated for by the rise of the three sub-dominant species (Lamy et al 2019). Consequently, the metacommunity underwent a similarly large shift in composition as the dominant species was replaced by the sub-dominant species (Figure 2B).…”

“…For example, if changes in local environmental conditions are similar across patches, local community composition might follow similar trajectories, leading to high compositional metacommunity variability (Figure 3A). This is probably the mechanism driving the metacommunity change observed in the case study of understory algae as the consistent replacement of the dominant species by a few sub-dominant species was linked to large-scale variations in sea surface temperature and nutrient concentration along the coast of California (Lamy et al 2019). However, if environmental change is not strongly correlated in space, if dispersal is limited, or if community dynamics are largely stochastic, spatial compositional synchrony may be low, resulting in reduced compositional metacommunity variability (Figure 3B; Micheli et al 1999, Gonzalez andLoreau 2009).…”

“…For example, if changes in local environmental conditions are similar across patches, local community composition might follow similar trajectories if community assembly is influenced more by environmental drivers than biotic interactions, leading to high compositional metacommunity variability. This is probably the mechanism driving the metacommunity change observed in the case study of understory algae, as the consistent replacement of the dominant species by a few sub-dominant species was linked to broad-scale variations in temperature and nutrients along the California coast (Lamy et al 2019). Spatial synchrony can also result from the regional synchronizing effect of highly mobile consumers, although this mechanism has been less well-described than dispersal and synchronizing environmental fluctuations (Ims and Steen 1990;de Roos et al 1998).…”