Marine heatwave-driven mass mortality and microbial community reorganisation in an ecologically important temperate sponge.

Marine heatwaves (MHWs) are increasing in frequency, duration and intensity, disrupting global marine ecosystems. While most reported impacts have been in tropical areas, New Zealand experienced its strongest and longest MHW in 2022, profoundly affecting marine sponges. Sponges are vital to rocky benthic marine communities, with their abundance influencing ecosystem functioning. This study examines the impact of this MHW on the photosynthetic sponge Cymbastella lamellata in Fiordland, New Zealand. We describe the extent, physiological responses, mortality, microbial community changes and ecological impact of this MHW on C. lamellata. The Fiordland MHW reached a maximum temperature of 4.4°C above average, lasting for 259 days. Bleaching occurred in >90% of the C. lamellata Fiordland population. The population size exceeded 66 million from 5 to 25 m, making this the largest bleaching event of its kind ever recorded. We identified the photosynthetic symbiont as a diatom, and bleached sponges had reduced photosynthetic efficiency. Post-MHW surveys in 2023 found that over 50% of sponges at sampling sites had died but that the remaining sponges had mostly recovered from earlier bleaching. Using a simulated MHW experiment, we found that temperature stress was a driver of necrosis rather than bleaching, despite necrosis only rarely being observed in the field (<2% of sponges). This suggests that bleaching may not be the cause of the mortality directly. We also identified a microbial community shift in surviving sponges, which we propose represents a microbial-mediated adaptive response to MHWs. We also found that C. lamellata are key contributors of dissolved organic carbon to the water column, with their loss likely impacting ecosystem function. We demonstrate the potential for MHWs to disrupt key marine phyla in temperate regions, highlighting how susceptible temperate sponges globally might be to MHWs.

Marine heat waves drive bleaching and necrosis of temperate sponges.

Marine heat waves (MHWs) are extended periods of excessively warm water1 that are increasing in frequency, duration, intensity, and impact, and they likely represent a greater threat to marine ecosystems than the more gradual increases in sea surface temperature.2,3,4 Sponges are major and important components of global benthic marine communities,5,6,7 with earlier studies identifying tropical sponges as potential climate change "winners."8,9,10,11 In contrast, cold-water sponges may be less tolerant to predicted ocean warming and concurrent MHWs. Here, we report how a series of unprecedented MHWs in New Zealand have impacted millions of sponges at a spatial scale far greater than previously reported anywhere in the world. We reported sponge tissue necrosis12 and bleaching (symbiont loss/dysfunction),13 which have been previously associated with temperature stress,6,12,14 for three common sponge species across multiple biogeographical regions, with the severity of impact being correlated with MHW intensity. Given the ecological importance of sponges,15 their loss from these rocky temperate reefs will likely have important ecosystem-level consequences.