Grazing halos reveal differential ecosystem vulnerabilities in vegetated habitats

The dynamic balance between primary production and herbivory is key to the resilience of plant-dominated ecosystems across the world. However, many vegetated ecosystems are becoming increasingly susceptible to herbivore-triggered collapses, as this balance is disrupted due to predator declines, increasing nutrients, and other interacting impacts of global change. Yet without accessible, cost-effective tools to evaluate the production-consumption relationship, it is difficult to know how close an ecosystem is to imminent overgrazing collapse. Here, we explore the effectiveness of individually formed sea urchin grazing halos as robust indicators of marine habitat vulnerability to overgrazing. Halos are grazed patches of bare rock on macrophyte-dominated substrates that represent the balance between macrophyte production and per capita herbivore consumption. We measured 1211 halos in 31 locations across the Mediterranean Sea to characterize how plant-herbivore interactions are mediated by endogenous (i.e., species identity, habitat type, and sea urchin size) and exogenous factors (i.e., environmental factors influencing biotic and abiotic contexts: depth, nutrients, temperature, or protection level). Our results show that halo size was effective in detecting differences in the effect of endogenous and exogenous factors on these interactions. Across locations, halo size was sensitive to differences in (i) species identity, with some species being more impactful than others; (ii) the type of habitat, with some habitats being more vulnerable than others; (iii) protection level, with halo size consistently lower inside marine protected areas; (iv) urchin size, with halo size increasing consistently with herbivore size; (v) nutrient conditions, with halo size increasing as nutrient availability decreased; as well as (vi) depth, with halo size increasing consistently with depth. These results indicate that overgrazing vulnerability is highly contingent on local ecological contexts, which strongly mediate plant-herbivore interactions. While drivers of ecosystem collapse may be global, the ability of ecosystems to cope is often inherently local. We need locally responsive measures and contextually meaningful solutions to manage ecological integrity in the face of global change. In this context, individually measured grazing halos can be a powerful tool in assessing and managing the resilience of macrophyte ecosystems.