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.