Consumer resilience suppresses the recovery of overgrazed ecosystems

Abstract

O_LIMany heterotroph species perish when faced with severe food limitation, others can persist, adapt, and thrive. Sea urchins are emblematic of this paradox: they can overgraze kelp forests to form barren habitats, but can then survive for decades in these nutritionally depauperate seascapes. Understanding the mechanisms enabling persistence under starvation, and rapid recovery when food returns, provides insight into how consumer resilience shapes ecosystem dynamics. C_LIO_LIWe quantified how food abundance, quality, deprivation, and reintroduction influence bioenergetic performance in the red sea urchin (Mesocentrotus franciscanus), integrating field observations of kelp forest and barren populations with a controlled feeding experiment. We measured respiration, feeding rates, gonadal growth, and fatty acid biomarkers to test how habitat history and diet jointly govern metabolic plasticity and nutrient assimilation. C_LIO_LIResting metabolic rates (RMR) were nearly twofold higher in kelp forest urchins than barrens conspecifics, yet feeding rates were equivalent across habitats, indicating that metabolic depression does not constrain food intake. Reciprocal shifts emerged in the experiment: starvation reduced RMR and lipid reserves in kelp forest urchins, while feeding elevated both traits in barrens urchins to levels comparable with kelp forest conspecifics. These results demonstrate rapid physiological compensation in response to both food deprivation and reintroduction. C_LIO_LIDiet quality strongly modulated performance. Urchins fed nutritionally poor monospecific diets consumed more biomass and calories than those on diverse, polyunsaturated fatty acid (PUFA)-rich diets, but did so with markedly lower efficiency of conversion to gonadal tissue. Fatty acid assimilation revealed that starvation elevated bacterial and biofilm biomarkers in tissues, whereas algal diets enriched essential PUFA profiles, particularly when diets were diverse. These results highlight that both quantity and quality of food influence consumer recovery trajectories, with nutritional geometry shaping efficiency of energy and nutrient use. C_LIO_LITogether, our findings show that M. franciscanus exhibits pronounced metabolic resilience, allowing persistence in barren habitats and rapid reactivation of grazing and reproduction when food becomes available. This work links nutritional ecology to ecosystem feedbacks by showing how compensatory feeding and metabolic flexibility enable consumers to maintain pressure on primary producers, thereby influencing the stability, hysteresis, and recovery of degraded ecosystems. C_LI