Consequences of kelp forest ecosystem shifts and predictors of persistence through multiple stressors.

Ecological communities can be stable over multiple generations, or rapidly shift into structurally and functionally different configurations. In kelp forest ecosystems, overgrazing by sea urchins can abruptly shift forests into alternative states that are void of macroalgae and primarily dominated by actively grazing sea urchins. Beginning in 2014, a sea urchin outbreak along the central coast of California resulted in a patchy mosaic of remnant forests interspersed with sea urchin barrens. In this study, we used a 14-year subtidal monitoring dataset of invertebrates, algae, and fishes to explore changes in community structure associated with the loss of forests. We found that the spatial mosaic of barrens and forests resulted in a region-wide shift in community structure. However, the magnitude of kelp forest loss and taxonomic-level consequences were spatially heterogeneous. Taxonomic diversity declined across the region, but there were no declines in richness for any group, suggesting compositional redistribution. Baseline ecological and environmental conditions, and sea urchin behaviour, explained the persistence of forests through multiple stressors. These results indicate that spatial heterogeneity in preexisting ecological and environmental conditions can explain patterns of community change.

A marine protected area network does not confer community structure resilience to a marine heatwave across coastal ecosystems.

Marine protected areas (MPAs) have gained attention as a conservation tool for enhancing ecosystem resilience to climate change. However, empirical evidence explicitly linking MPAs to enhanced ecological resilience is limited and mixed. To better understand whether MPAs can buffer climate impacts, we tested the resistance and recovery of marine communities to the 2014-2016 Northeast Pacific heatwave in the largest scientifically designed MPA network in the world off the coast of California, United States. The network consists of 124 MPAs (48 no-take state marine reserves, and 76 partial-take or special regulation conservation areas) implemented at different times, with full implementation completed in 2012. We compared fish, benthic invertebrate, and macroalgal community structure inside and outside of 13 no-take MPAs across rocky intertidal, kelp forest, shallow reef, and deep reef nearshore habitats in California's Central Coast region from 2007 to 2020. We also explored whether MPA features, including age, size, depth, proportion rock, historic fishing pressure, habitat diversity and richness, connectivity, and fish biomass response ratios (proxy for ecological performance), conferred climate resilience for kelp forest and rocky intertidal habitats spanning 28 MPAs across the full network. Ecological communities dramatically shifted due to the marine heatwave across all four nearshore habitats, and MPAs did not facilitate habitat-wide resistance or recovery. Only in protected rocky intertidal habitats did community structure significantly resist marine heatwave impacts. Community shifts were associated with a pronounced decline in the relative proportion of cold water species and an increase in warm water species. MPA features did not explain resistance or recovery to the marine heatwave. Collectively, our findings suggest that MPAs have limited ability to mitigate the impacts of marine heatwaves on community structure. Given that mechanisms of resilience to climate perturbations are complex, there is a clear need to expand assessments of ecosystem-wide consequences resulting from acute climate-driven perturbations, and the potential role of regulatory protection in mitigating community structure changes.

Alternations in the foraging behaviour of a primary consumer drive patch transition dynamics in a temperate rocky reef ecosystem.

Understanding the role of animal behaviour in linking individuals to ecosystems is central to advancing knowledge surrounding community structure, stability and transition dynamics. Using 22 years of long-term subtidal monitoring, we show that an abrupt outbreak of purple sea urchins (Strongylocentrotus purpuratus), which occurred in 2014 in southern Monterey Bay, California, USA, was primarily driven by a behavioural shift, not by a demographic response (i.e. survival or recruitment). We then tracked the foraging behaviour of sea urchins for 3 years following the 2014 outbreak and found that behaviour is strongly associated with patch state (forest or barren) transition dynamics. Finally, in 2019, we observed a remarkable recovery of kelp forests at a deep rocky reef. We show that this recovery was associated with sea urchin movement from the deep reef to shallow water. These results demonstrate how changes in grazer behaviour can facilitate patch dynamics and dramatically restructure communities and ecosystems.

Variation in purple sea urchin (Strongylocentrotus purpuratus) morphological traits in relation to resource availability.

Flexible resource investment is a risk sensitive reproductive strategy where individuals trade resources spent on reproduction for basic metabolic maintenance and survival. This study examined morphological variation in herbivorous sea urchin grazers across a mosaic landscape of macroalgae dominated habitats interspersed with patches of sea urchin barrens to determine whether sea urchins shift energy allocation in response to food limitation. Extensive underwater surveys of habitat attributes (e.g., sea urchin density, algae cover) were paired with detailed laboratory assays (e.g., sea urchin dissections) to determine how resource abundance affects energy allocation between reproductive capacity and body structure in the purple sea urchin, Strongylocentrotus purpuratus. We found that: (1) sea urchins had a more elongate jaw structure relative to body size in habitats void of macroalgae (i.e., barrens), (2) sea urchin reproductive capacity (i.e., gonad index) was lower in barrens and the barrens habitat was primarily comprised of encrusting algae, and (3) sea urchin jaw morphology (i.e., lantern index) and reproductive capacity (i.e., gonad index) were inversely related. These results suggest that sea urchins respond to macroalgae limited environments by shifting energy allocation between reproductive capacity and modifications of the foraging apparatus, which may explain the ability of sea urchins to acquire food in resource-limited environments.

Behavioral responses across a mosaic of ecosystem states restructure a sea otter-urchin trophic cascade.

Consumer and predator foraging behavior can impart profound trait-mediated constraints on community regulation that scale up to influence the structure and stability of ecosystems. Here, we demonstrate how the behavioral response of an apex predator to changes in prey behavior and condition can dramatically alter the role and relative contribution of top-down forcing, depending on the spatial organization of ecosystem states. In 2014, a rapid and dramatic decline in the abundance of a mesopredator (Pycnopodia helianthoides) and primary producer (Macrocystis pyrifera) coincided with a fundamental change in purple sea urchin (Strongylocentrotus purpuratus) foraging behavior and condition, resulting in a spatial mosaic of kelp forests interspersed with patches of sea urchin barrens. We show that this mosaic of adjacent alternative ecosystem states led to an increase in the number of sea otters (Enhydra lutris nereis) specializing on urchin prey, a population-level increase in urchin consumption, and an increase in sea otter survivorship. We further show that the spatial distribution of sea otter foraging efforts for urchin prey was not directly linked to high prey density but rather was predicted by the distribution of energetically profitable prey. Therefore, we infer that spatially explicit sea otter foraging enhances the resistance of remnant forests to overgrazing but does not directly contribute to the resilience (recovery) of forests. These results highlight the role of consumer and predator trait-mediated responses to resource mosaics that are common throughout natural ecosystems and enhance understanding of reciprocal feedbacks between top-down and bottom-up forcing on the regional stability of ecosystems.