Zombies of the nearshore: Metabolic depression in sea urchin barrens associated with food deprivation

Abstract

The proliferation of sea urchins can decimate macroalgal forests in coastal ecosystems, leading to persistent barren seascapes. While kelp forests are among the most productive ecosystems on the planet, productivity in these urchin barrens is dramatically reduced. Moreover, urchins inhabiting these food-depauperate barrens face starvation and many survive in these barrens for years or decades. Urchins in barrens can persist by eating food subsidies from drift algae, pelagic salps, tubeworms, as well as encrusting and filamentous algae, microbial mats, and slow-growing species resistant to herbivory. Despite both food from endogenous production and exogenous subsidies, many urchins in barrens likely experience prolonged food deprivation. This resource limitation may create a trade-off between reproduction and survival; for example, fecundity of purple sea urchins (Strongylocentrotus purpuratus) is 99.9% lower in barrens. Despite food constraints, red sea urchins (Mesocentrotus franciscanus), the dominant urchin species at our study sites, can live in excess of 100 years and barrens in Haida Gwaii, British Columbia (BC), Canada, have persisted for at least 143 years. While these phenomena are widespread and well documented, the bioenergetic adaptations that allow urchins to persist in these food-depauperate barrens remain poorly understood. To quantify habitat-specific differences in metabolic rates and energy reserves (as measured by gonadal mass), we conducted respirometry on and measured gonadal mass in M. franciscanus at three locations in BC inside and outside of adjacent kelp forest and barrens habitat. Here we demonstrate that M. franciscanus in barrens versus kelp forests have substantially lower energy reserves and, importantly, also exhibit dramatic reductions in size-specific resting metabolic rates (RMR), even after standardizing by metabolically active body mass. On average, gonadal mass was 44.6% lower and RMR scaled to metabolically active body mass was 40% lower in barrens urchins than in kelp forest urchins. Such a shift in metabolic rate may provide a mechanism that facilitates barren state stability over long time scales as M. franciscanus can lower energetic demands while they wait for small pulses of food, scrape by on low-productivity resources, and suppress recruitment of macroalgae for months, years, or decades.