Echinoderm mass mortality events shape marine ecosystems by altering the dynamics among major benthic groups. The sea urchin Diadema antillarum , virtually extirpated in the Caribbean in the early 1980s by an unknown cause, recently experienced another mass mortality beginning in January 2022. We investigated the cause of this mass mortality event through combined molecular biological and veterinary pathologic approaches comparing grossly normal and abnormal animals collected from 23 sites, representing locations that were either affected or unaffected at the time of sampling. Here, we report that a scuticociliate most similar to Philaster apodigitiformis was consistently associated with abnormal urchins at affected sites but was absent from unaffected sites. Experimentally challenging naïve urchins with a Philaster culture isolated from an abnormal, field-collected specimen resulted in gross signs consistent with those of the mortality event. The same ciliate was recovered from treated specimens postmortem, thus fulfilling Koch’s postulates for this microorganism. We term this condition D. antillarum scuticociliatosis.

The 1983-1984 die-off of the long-spined sea urchin Diadema antillarum stands out as a catastrophic marine event because of its detrimental effects on Caribbean coral reefs. Without the grazing activities of this key herbivore, turf and macroalgae became the dominant benthic group, inhibiting coral recruitment and compromising coral reef recovery from other disturbances. In the decades that followed, recovery of D. antillarum populations was slow to non-existent. In late January 2022, a new mass mortality of D. antillarum was first observed in the U.S. Virgin Islands. We documented the spread and extent of this new die-off using an online survey. Infected individuals were closely monitored in the lab to record signs of illness, while a large population on Saba, Dutch Caribbean, was surveyed weekly before and during mortality to determine the lethality of this event. Within four months the die-off was distributed over 1,300 km from north to south and 2,500 km east to west. Whereas the 1983-1984 die-off advanced mostly with the currents, the 2022 event has appeared far more quickly in geographically distant areas. First die-off observations in each jurisdiction were often close to harbor areas, which, together with their rapid appearance, suggests that anthropogenic factors may have contributed to the spread of the causative agent. The signs of illness in sick D. antillarum were very similar to those recorded during the 1983-1984 die-off: lack of tube feet control, slow spine reaction followed by their loss, and necrosis of the epidermis were observed in both lab and wild urchins. Affected populations succumbed fast; within a month of the first signs of illness, a closely monitored population at Saba, Dutch Caribbean, had decreased from 4.05 individuals per m2 to 0.05 individuals per m2. Lethality can therefore be as high as 99%. The full extent of the 2022 D. antillarum die-off event is not currently known. The slower spread in the summer of 2022 might indicate that the die-off is coming to a (temporary) standstill. If this is the case, some populations will remain unaffected and potentially supply larvae to downstream areas and augment natural recovery processes. In addition, several D. antillarum rehabilitation approaches have been developed in the past decade and some are ready for large scale implementation. However, active conservation and restoration should not distract from the primary goal of identifying a cause and, if possible, implementing actions to decrease the likelihood of future D. antillarum die-off events.