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

ABSTRACT: 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.

SUBMITTER: Smith JG

PROVIDER: S-EPMC7980363 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundIn temperate macroalgal forests, sea urchins are considered as a keystone species due to their grazing ability. Given their potential to shape benthic communities, we monitored the habitat use by three sympatric sea urchin species and compared their behaviors in a vegetated habitat (VH) and an adjacent isoyake habitat (IH).MethodsWe monitored the environmental conditions and sea urchin density along deep and shallow transects of the VH and IH for over a year. The benthic rugosity at both sites were also surveyed. A mark-recapture experiment was conducted on the two most abundant sea urchins, Diadema setosum and Heliocidaris crassispina, to elucidate sea urchin movement patterns and group dynamics.ResultsWe found that exposure to waves was highest at the VH while the IH was sheltered. The deep IH experienced the least amount of light due to high turbidity. Water temperature patterns were similar across sites. The VH benthic topography was more rugose compared to the smoother and silt-covered IH substate. Peak macroalgal bloom occurred three months earlier in IH, but macroalgae persisted longer at the shallow VH. Among the sympatric sea urchins, H. crassispina was most abundant at the shallow VH and was observed in pits and crevices. The most abundant across IH and in the deep VH was D. setosum, preferring either crevices or free-living, depending on hydrodynamic conditions. The least abundant species was D. savignyi, and most often observed in crevices. Small and medium sea urchins were most often observed at the IH site, whereas larger sea urchins were more likely observed at the VH. The mark-recapture study showed that D. setosum was found to displace further at the IH, and H. crassispina was more sedentary. Additionally, D. setosum was always observed in groups, whereas H. crassispina was always solitary.DiscussionThe behaviors of sympatric urchins, Diadema savignyi, D. setosum and H. crassispina, differed in response to changes in the benthic environment and physical conditions. Sea urchin displacement increased when rugosity and wave action were low. Habitat preference shifted to crevices in seasons with high wave action. In general, the mark-recapture experiment showed that sea urchins displaced further at night.

Project description:The arrival of large masses of drifting Sargassum since 2011 has caused changes in the natural dynamics of Caribbean coastal ecosystems. In the summer of 2015, unprecedented and massive mats of S. fluitans and S. natans have been observed throughout the Mexican Caribbean including exceptional accumulations ashore. This study uses stable isotopes to assess the impact of Sargassum blooms on the trophic dynamics of the Diadema antillarum sea urchin, a keystone herbivore on many Caribbean reefs. Bayesian models were used to estimate the variations in the relative proportions of carbon and nitrogen of assimilated algal resources. At three lagoon reef sites, the niche breadth of D. antillarum was analysed and compared under massive influx of drifting Sargassum spp. vs. no influx of Sargassum blooms. The effects of the leachates generated by the decomposition of Sargassum led to hypoxic conditions on these reefs and reduced the taxonomic diversity of macroalgal food sources available to D. antillarum. Our trophic data support the hypothesis that processes of assimilation of carbon and nitrogen were modified under Sargassum effect. Isotopic signatures of macroalgae associated with the reef sites exhibited significantly lower values of δ15N altering the natural herbivory of D. antillarum. The Stable Isotopes Analysis in R (SIAR) indicated that, under the influence of Sargassum blooms, certain algal resources (Dictyota, Halimeda and Udotea) were more assimilated due to a reduction in available algal resources. Despite being an abundant available resource, pelagic Sargassum was a negligible contributor to sea urchin diet. The Stable Isotope Bayesian Ellipses in R (SIBER) analysis displayed differences between sites, and suggests a reduction in trophic niche breadth, particularly in a protected reef lagoon. Our findings reveal that Sargassum blooms caused changes in trophic characteristics of D. antillarum with a negative impact by hypoxic conditions. These dynamics, coupled with the increase in organic matter in an oligotrophic system could lead to reduce coral reef ecosystem function.

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

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