Many ecosystems are experiencing unprecedented environmental changes, underscoring theimportance of understanding ecological processes that impart ecosystem resistance and resilience.Many kelp forests around the world have experienced dramatic declines, including forests of giant kelp(Macrocystis pyrifera) along the coast of central California. We investigated the causes andconsequences of these declines and the ecological mechanisms of ecosystem resistance and resilience.

Loss of giant kelp forests along the Monterey Peninsula in central California coincided with (i) the localecological extinction of the sunflower star (Pycnopodia helianthoides), a significant predator of seaurchins, in 2013 and (ii) a marine heatwave that persisted from 2014 to 2016. Loss of Pycnopodia wasassociated with the sea star wasting disease (SSWD) epidemic. During and since these events, weobserved outbreaks of the purple sea urchin (Strongylocentrotus purpuratus), which created a spatialmosaic of ?urchin barrens? devoid of macroalgae, and remaining kelp forests.

We combined community surveys with field and laboratory (mesocosm) experiments to test alternativeexplanations for these urchin outbreaks. Surveys of community structure before, during and after theSSWD and MHW revealed a decline and persistent loss of Pycnopodia, increase in counts of purple seaurchins, and the coincident decline in densities of kelps and other algae. Many sites that exhibited thistransition from forested to ?urchin barens? have persisted through 2021.

Surveys of purple urchin size structure (i.e. relative abundance of urchin sizes) and size-baseddemographic modelling indicate that rapid increases in counts of large (4-5 cm diameter) purple urchinswas initiated by a foraging response, with subsequent larval recruitment contributing to the persistenceof barrens. With the loss of a predator and declining abundance of kelp, purple urchins emerged fromcracks and crevices and possibly migrated from deeper depths to overgraze algae. Field and labexperiments substantiate that the lack of predators and drift kelp precipitate the emergence of purpleurchins and overgrazing of kelps.

We evaluated the role of alternative predators, sea otters (Enhydra lutris nereis) and the red rock crab(Cancer productus), in reducing grazing by urchins in barrens and facilitating forest recovery. Weexplored direct numerical responses and indirect behavioral responses of predators and their urchinprey. The number of sea otters specializing on urchin prey caused an increase in urchin consumption,increase in sea otter survivorship, and local population size. However, sea otter foraging was confined toenergetically profitable urchins with high gonad volumes within remaining forests and not linked to highdensities of urchins with poor gonad condition in barrens. Therefore, while sea otter foraging enhancedthe resistance of remaining forests to overgrazing, it did not contribute to the decline of urchins inbarrens. Nonetheless, the remaining forests are the sources of kelp spores required to reforest barrensand thereby enhance forest resilience.

To evaluate the role of rock crabs, we conducted experiments in lab mesocosms (1.1 m 3 cattle troughs),and on small (0.5 m 3 ) and large (6 m 3 ) caged rocky reefs in the field. These experiments differ in theircontrol, accuracy, and frequency of observations (mesocosms>small cages>large cages) and how wellthey represent the natural environment (large cages>small cages> mesocosms). Results across theseexperiments demonstrated that rock crab, unlike sea otters, kill gonad-poor sea urchins from barrensand reduce grazing rates and kelp loss by at least 50%. Moreover, the direct mortality of urchins and the
behavioral response of urchins to seek shelter from predators contribute equally to the increasedsurvival of kelp. Efforts to quantify the abundance of rock crabs in urchin barrens are ongoing.

We observed forest recovery in one of the monitored urchin barrens. Purple sea urchins migrated fromthe deeper barrens to shallow reefs that supported beds of red algae. A forest eventually reestablishedon the deeper reef vacated by the sea urchins, demonstrating the important role of foraging migrationsin the process of forest recovery.

Together, our results demonstrate the importance of diversity of alternative predators for the resilienceof communities to disturbance, the crucial role of behavior, both of predators and prey, in determiningthe state (forested vs. deforested) of an ecosystem, and how the pattern of disturbances (thejuxtaposition of forest and barrens) influences the behavior and interactions between predators andprey and ecosystem resilience.

Broader impacts of this project include the training of eight high school and over 30 undergraduateunderrepresented minority students, many of whom produced independent studies, theses, andpresentations. Many of these students graduated and are now in graduate programs or working forresource management agencies. The project demonstrates the productive collaboration betweenacademic (UCSC), federal (USGS) and non-profit (Monterey Bay Aquarium) organizations. Results havebeen presented at multiple scientific and public venues, informing the public and state and federalresource managers of the importance of predator diversity in the persistence and resilience of kelpforest ecosystems.

Last Modified: 01/21/2022
Modified by: Mark H Carr