Foraging under extreme events: Contrasting adaptations by benthic macrofauna to drastic biogeochemical disturbance

Abstract

Abstract Hydrothermal vent systems are important biodiversity hotspots that host a vast array of unique species and provide information on life's evolutionary adaptations to extreme environments. However, these habitats are threatened by both human exploitation and extreme natural events, both of which can rapidly disrupt the delicate balance of the food webs found in these systems. This is particularly true for shallow vent endemic animals due to their limited dietary niche and specialized adaptations to specific biogeochemical conditions. In this study, we used the shallow hydrothermal vents of Kueishantao off the coast of Taiwan as a natural laboratory to examine the response of a benthic food web to a M5.8 earthquake and a C5 typhoon that led to a two‐year “near shutdown” of the vents. These perturbations drastically altered the local biogeochemical cycle and the dietary availability of chemosynthetic versus photosynthetic food resources. Our analysis of multiple stable isotopes, including those of sulphur, carbon, and nitrogen (δ34S, δ13C, and δ15N), from different benthic macrofauna reveals that endemic and non‐endemic consumers exhibited different responses to sudden disruption in habitat and biogeochemical cycling. The endemic vent crab, Xenograpsus testudinatus, continued to partially rely on chemosynthetic sulphur bacteria despite photosynthetic sources being the most dominant food source after the disruption. We posit that X. testudinatus has an obligate nutritional dependence on chemoautotrophic sources because the decrease in chemoautotrophic production was accompanied by a dramatic decrease in the abundance of X. testudinatus. The population decline rate was ~19 individuals per m2 per year before the perturbation, but the decline rate increased to 40 individuals per m2 per year after the perturbation. In contrast, the non‐endemic gastropods exhibited much greater dietary plasticity that tracked the overall abundance of photo‐ and chemo‐synthetic dietary sources. The catastrophic events in shallow hydrothermal vent ecosystem presented a novel opportunity to examine dietary adaptations among endemic and non‐endemic benthic macrofauna in response to altered biogeochemical cycling. Our findings highlight the vulnerability of benthic specialists to the growing environmental pressures exerted by human activities worldwide. Read the free Plain Language Summary for this article on the Journal blog.