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.