4. DISCUSSION
Two unusual southwest rough sea period, with winter storms Xynthia (February 2010) and Emma (February 2018), preceded the mass mortality events. This situation suggests that SW storms may promote the outbreak of Paramoebiasis episodes in Eastern Atlantic archipelagos, supporting the “killer-storm” hypothesis (Scheibling & Lauzon-Guay 2010). No clear correlation with SST°C was found: the first episode occurred with an average SST of 20.7°C and the second occurred with an average SST of 18.2°C. These kinds of rough SW sea with that lead to a winter storms have also been described by meteorologists as “depressions” or “windstorms” and are often associated with strong wind and local precipitation. In the Canary Islands and Madeira, the Azores anticyclone moves towards the northern Atlantic from the end of autumn through mid-spring and enables the arrival of “normal” northwest storms to the archipelagos. However, when these northwest storms originate at lower latitudes, such as Xynthia and Emma (Liberato et al. 2013), their wet air masses hit the islands from the south or southwest and generate severe windstorms with strong local rain episodes and waves heights above 2 m and storm surge (Figure 3 and 4). These kinds of winter storms develop in the Atlantic, off Madeira, and cross the Canary Islands and then start moving northeast towards the European mainland.
The ”killer storm” hypothesis was described by Scheibling and Hennigar (1997) and modelled by Scheibling and Lauzon-Guay (2010). This hypothesis explains the occurrence of recurrent sea urchin mortality events off the coast of Canada as being due to tropical storms and hurricanes (Scheibling et al. 2013, Feehan & Scheibling 2014). The mechanism involves a tropical storm, a pathogen and sea urchin populations (Scheibling & Hennigar 1997, Feehan et al. 2016). Thanks to long-term coastal monitoring and good baseline data of sea urchin populations, Scheibling and Lauzon-Guay (2010) created a logistic regression model that demonstrated that the probability of mass mortality of sea urchins can be predicted by the intensity and proximity of tropical storms and hurricanes. These tropical storms have been hypothesized to deliver the amoeba Paramoeba invadens to the coast, triggering disease outbreaks. Although questions remain about the source populations of the pathogenic agent and the oceanographic mechanisms affecting its introduction to coastal environments, the model of Scheibling and Lauzon-Guay (2010) has been supported by experiments and field observations (Feehan et al. 2012, Scheibling et al. 2013).
Our results differ from those of our first study (Clemente et al. 2014) because Vibrio was also found in dead urchins at that time. Our hypothesis is that during the first mortality event in 2010, whenVibrio algynoliticus and Parameba braquiphila were isolated, the sea urchins were probably collected in an advanced stage of infection or when they were already dead. This may also be the case of the recent study performed by Gizzi and collaborators (2020) in Madeira, who used late infection stage individuals and do not even look for amoebas. However, this second mortality event suggests that the first pathogen to infect the sea urchins could have been an amoeba. Observations of the moribund sea urchins revealed that the amoeba started to damage the epidermis located on the oral side and over the animals’ ambulacral plates (Figure 2b). This pattern of infection could then accelerate the invasion of amoebae through the ambulacral pores as well as facilitate the entrance of other pathogens such as Vibrioin later infection stages. Therefore, Vibrio and other bacteria could play an opportunistic role while the amoeba may have been the primary cause of sea urchin mortality. These results are also consistent with the findings of studies conducted along western Atlantic coasts that found that paramoebiasis caused sea urchin mass mortality (e.g., Feehan & Scheibling 2014).
We believe that explosive southwest storm events generate pronounced underwater sediment movement and large-scale vertical mixing (Figure 4). Other authors have also suggested that storm events can transport amoebae via horizontal advection from distant source populations or vertically mix amoebae residing locally in deep basins (Scheibling & Hennigar 1997, Scheibling et al. 2013, but see Feehan et al. 2016). Amoebae are benthic organisms that live in sandy stable environments (Dickova et al. 2005, Nowak & Archibald 2018) like the ones found on the southwestern and southeastern sides of the Canary Islands. The massive movement of sediment might increase the number of amoebae in the water column and move them to nearby rocky bottoms where sea urchins reside. Significant sediment deposition over the urchins’ habitat after storms might increase the probability of infection and trigger the mass mortality observed across the archipelagos. Moreover, sediment deposition alone might also cause some damage on the sea urchin epidermis, facilitating the infection. It is important to note that these mass mortalities have been mainly observed in populations living near sandy environments on the southern sides of the islands (Clemente et al. 2014), an observation that supports our hypothesis. Generally, the lee sides of islands are not affected by swell; calm sea weather there favors sediment deposition (Hernández et al. 2008). This situation arises because Atlantic archipelagos are mainly affected by northeastern trade winds, even during winter months, and years with strong southwestern/southern storms are rare (Guijarro et al. 2015) (Figure 3). For instance, in this investigation we only found two large similar episodes over a 10-year period (Figure 3).
The low frequency and variability of southwestern storms can also help to explain why sea urchin barrens have persisted for decades in the Canaries (Hernández 2017). However, this situation might change in the coming years. As climate change accelerates, the magnitude and frequency of extreme events is expected to continue to increase in the North Atlantic. A recent review by Pardowitz (2015) covering the North Atlantic and parts of Europe showed that the intensity and frequency of winter storms will increase in these regions over the 21st century. Changes in storm intensity and frequency are consistently identified among multiple model projections. It has been found that the North-Atlantic Oscillation (NAO) undergoes fundamental changes in its phase and its shape (Pardowitz 2015). Consistent with diagnosed changes in storm frequency, the NAO has been found to be shifting towards a more positive phase with its action center shifting toward the northeast. This change may be related to more favorable growth conditions for periods of storminess over the eastern parts of the North Atlantic. In this sense, the disease outbreak described here can be used to reveal the mechanisms of sea urchin massive die-off and provide predictions about future climate-mediated changes in disease frequency.