Unprecedented Warming and Increased Herbivory Drive Collapse of Japan's Kelp Forests

Kelp forests underpin entire ecosystems and provide key services for human society, yet are threatened by anthropogenic stressors, most notably ocean warming and overgrazing. While Japanese kelp forests have substantial historical and cultural value, responses to recent environmental change remain poorly resolved. Here, we assessed how recent Kuroshio-associated warming and increased herbivory were linked to kelp forest collapse across approximately 200 km of the Izu Peninsula (central-eastern Japan). We combined 40 years of in situ kelp biomass (1980-2024) and 12-14 years of canopy-cover records (2009-2025) with satellite-derived sea-surface temperature and marine heatwave metrics. Herbivorous fish assemblages and bite rates were surveyed monthly (2021-2022) across reefs spanning healthy, mosaic, and barren states. Laboratory experiments quantified lethal and sub-lethal thermal thresholds of juvenile Ecklonia cava using temperature-ramping (20°C-33°C) and growth trials (22°C vs. 28°C). Spatial analyses compared thermal-threshold exceedance and seasonal grazing-window expansion with observed canopy loss, evaluating whether warming and herbivory were consistent with the spatial extent of decline. Warming along the Izu coast intensified during the recent Kuroshio Large Meander, increasing from 0.15°C decade-1 (1982-2016) to 2.98°C decade^-1 (2017-2024), with cumulative marine heatwave intensity rising from 2.34°C to 63.22°C·day decade^-1. Over the same period, canopy-forming E. cava cover fell from ~75% to zero, and peak biomass declined from 2.37 kg DW m^-2 to zero, indicating local extirpation and likely regional functional loss. Laboratory assays showed rapid physiological decline above 29.5°C and mortality at 32°C-33°C; temperatures exceeded during summer 2023/2024. The grazing season by warm-adapted herbivorous fishes expanded by up to 86 days, amplifying kelp loss across heat-stressed reefs. Together, extreme thermal stress and expanded herbivory were strongly associated with a shift from kelp forests to barren reefs, highlighting how physiological stress and trophic processes can contribute to rapid kelp loss in warming boundary-current systems.