1. INTRODUCTION
Sea urchins play a key role in structuring benthic rocky ecosystems in temperate and subtropical regions of the oceans (Lawrence 1975, Harrold & Pearse 1987). Their population density often undergoes marked fluctuations that promote a state shift in the ecosystem they inhabit (Ling et al. 2015, Hernández 2017). Population increases of some sea urchin species can result in catastrophic environmental changes because the animals decimate erect macroalgae cover by grazing. This less-productive ecosystem state is known as “urchin barren.” Urchin barren is considered to be an undesirable ecosystem state that has clear negative impacts on commercial reef-based fisheries and local biodiversity (Hernández 2017). Therefore, there is a need to understand the dynamics of sea urchin fluctuations and the resilience of macroalgae beds. However, the general dynamics of collapse and recovery of these underwater forests remain poorly defined in many regions of the word (Ling et al. 2015). In some regions, sea urchin barrens can be highly persistent and persist for many decades (Watanuki et al. 2010, Hernández 2017). In other regions, there is a cyclical alternation between ecosystem states in which recurrent sea urchin mass mortality helps kelp beds recover every 10–20 years (Scheibling et al. 2013).
Several mass mortality causative agents have been detected in sea urchins, including high temperatures during extreme low tides and different epizootic pathogens and toxicity resulting from harmful algae blooms (Feehan & Scheibling 2014, Jurgens et al. 2015). Among the epizootic pathogens, amoebas have been identified as a major actor in widespread die-off events along Northwest Atlantic shores (Feehan & Scheibling 2014) and recently in Eastern Atlantic archipelagos (Clemente et al. 2014). In the Northwest Atlantic, storm activity and high temperatures have been also well correlated with amoeba blooms (Paramoebiasis) that resulted in sea urchin die-off (Scheibling et al. 2013). In other regions where pronounced sea urchin mass mortality has been observed, such as the Caribbean, the pathogens were not properly identified (Lessios 1988). This situation stems from the inherent complication of isolating pathogens and establishing cause-effect relationships. Therefore, every large mortality events offers a unique opportunity to understand these natural phenomena.
In 2014, we reported for the first time a widespread mass mortality event of Diadema africanum sea urchin populations in the Eastern Atlantic archipelagos off Madeira and the Canary Islands that took place from October 2009 through April 2010 (Clemente et al. 2014). Despite the disease’s spatial heterogeneity, there was an overall 65% reduction in the population compared with the pre-mortality density. The disease mainly affected the southeastern and southwestern coasts of the islands and extended more than 400 km straight into the Eastern Atlantic. Initial laboratory results strongly suggested that Vibrio alginolyticus was involved in the disease. However, we could not rule out the possibility of a synergy between isolated species of bacteria and other pathogens. For instance, a study conducted with D. africanum specimens collected during the same mortality event revealed the presence of free-living amoebae in the coelomic fluid of diseased individuals. This amoeba species was identified as Neoparamoeba branchiphila (now Paramoeba branchiphila ) (Dyková et al. 2011). Confirmed later using small subunits of nuclear rDNA, this species of amoeba was found to be closely related to Paramoeba invadens from the western Atlantic region (Feehan et al. 2013).
A second sea urchin mass mortality event was recently detected in Eastern Atlantic archipelagos off Madeira and the Canary Islands. This recurrent episode of urchin population die-off provides evidence for a link with large-scale meteorological and oceanographic events. We believe that this event can help generalize a natural process to explain sea urchin mass mortality occurring in subtropical and temperate north Atlantic coastal regions. The primary objectives of this study included (1) comparing sea urchin densities before and after the recent mass mortality, using well-monitored sites; (2) identifying the pathogen with molecular techniques; and (3) performing a long-term meteorological-oceanographic exploration to determine links between sea urchin population die-offs and large-scale oceanographic phenomena, such as storms. Although the idea proposed here is not new and other authors have linked large-scale meteorological and oceanographic events with sea urchin mortalities (see the review by Feehan & Scheibling 2014), this new mortality episode, in a different region and affecting a different species, provides evidence to support a general explanation for sea urchin mass die-offs. In this sense, the findings described here are central to better understanding the dynamics of sea urchin disease outbreaks and the alternation between sea urchin barrens and macroalgae forests. Determining the general mechanisms of this natural event in the East Atlantic Archipelagos will help scientists make accurate predictions of climate-mediated changes in disease frequency and determine the impacts of this disease on the future of coastal marine ecosystems in the Atlantic.