156
Möllmann 2015). Some ecosystems may be able to absorb
stronger disturbances than others depending on their characteristics, but in general, marine ecosystems are known to be
particularly vulnerable to drastic and unexpected shifts,
referred in ecology as regime shifts (deYoung et al. 2008).
Such non-linear dynamics may have positive or negative outcomes for the sustainable use of natural resources and their
management, therefore they should be taken into account
and dealt with great precaution when taking environmental
policy decisions (Holling 1973; Carpenter 2001; Scheffer
2009; Rocha et al. 2014a).
In this chapter, we first present some examples of marine
ecosystems which have exhibited non-linear dynamics in
response to external changes. These examples allow us to
highlight different mechanisms potentially involved in
regime shifts from an empirical point of view, as well as their
potential implications for the sustainable use of marine
resources. Secondly, we review the regime shift theory and
associated concepts to finally consider recent advances and
future challenges of integrating regime shift theory into
holistic marine ecosystem-based management approaches.
Marine Ecosystems Regime Shifts All
Over the World
Although the regime shift concept is still vigorously discussed, an increasing number of studies provide evidence for
the potential of abrupt changes and surprises in marine ecosystems worldwide (Steneck et al. 2002; Beaugrand 2004;
Mumby et al. 2007; Möllmann et al. 2008, 2009; Mumby
2009; Bestelmeyer et al. 2011; Frank et al. 2011, 2016; Llope
et al. 2011; Beaugrand et al. 2015; Gårdmark et al. 2015;
Ling et al. 2015; Vasilakopoulos and Marshall 2015; Auber
et al. 2015). These studies, based on empirical observations,
highlight mechanisms of regime shifts, firstly formulated by
theoretical studies (Holling 1973; May 1977; Scheffer et al.
2001).
The Atlantic Cod Trophic Cascade
Surprises in natural systems are relatively common and can
happen even in well-studied systems, due to different drivers. One driver of non-linear dynamics is the overfishing of
top-predators. Top-predator overfishing may cause the depletion and collapse of their population resulting in unexpected
ecosystem structure reorganizations through trophic cascades (Myers and Worm 2005; Fauchald 2010; Llope et al.
2011; Möllmann and Diekmann 2012; Steneck and Wahle
2013). Atlantic cod (Gadus morhua) is an important toppredator fish species, which can regulate marine ecosystems
through top-down control, and has supported entire human
communities through fisheries for centuries (Haedrich and
Hamilton 2000; Myers and Worm 2005). After the industrial
revolution and the increase of fishing power and capacity
around the 1980s–1890s, many cod stocks collapsed bringing high economic losses (Myers et al. 1997; Frank et al.
2016). Multiple analyses conducted in different basins such
as in the Baltic Sea or in the Eastern Scotian Shelf, showed
that the collapse of cod stocks was caused by a combination
of increased fishing pressure and unfavorable climatic conditions (Frank et al. 2005, 2016; Casini et al. 2008b; Möllmann
et al. 2008, 2009). The high economic loss and social issues
induced, led governments to adopt a range of management
measures, such as drastic quota reductions and, in some
cases, even fishing moratoria. Nevertheless, despite all the
management measures and plans adopted, cod stocks failed
to recover (Hutchings 2000; Frank et al. 2011; Hutchings
and Rangeley 2011).
One of the reasons advanced to explain these management
failures is the undergoing non-linear dynamics known as trophic cascades (Casini et al. 2008a; Star et al. 2011). Indeed,
the collapse of this top-predator resulted in a shift from a
cod-dominated to a forage fishes-dominated system (Frank
et al. 2005; Gårdmark et al. 2015). Before overfishing, adult
cod biomass level was high and cod controlled forage fish
populations through predation. This hindered the forage fish
from negatively impacting younger cod (through predation
and/or competition), thus enhancing its biologically sustainable biomass. However, when cod biomass became depleted,
the consequently increased forage fish abundance caused a
further decline of cod population by increasing their negative
direct (predation) or indirect (competition) impacts on
younger cod. This feedback loop is then very difficult to
reverse (Walters and Kitchell 2001; Möllmann et al. 2009;
Nyström et al. 2012). Based on this example, it is clear how
such systems can show two distinct configurations depending
on their level of top-predator biomass. Of course, changes in
mid-trophic levels will also reflect in lower ones, for instance
high abundance of forage fishes will likely reduce plankton
abundance. Under this new configuration with low cod biomass, a reduction in fishing pressure would likely lead to a
very delayed or even none cod recovery, since new mechanisms would keep its population in the new depleted state. To
summarize, both Baltic Sea and Scotian Shelf regime shifts
were caused by a combination of overfishing and climate
variation, and characterized by a trophic cascade (top-down
mechanism) due to the depletion of Atlantic cod stocks
(Frank et al. 2005; Casini et al. 2008b; Llope et al. 2011;
Möllmann and Diekmann 2012). This led to immediate high
social and economic losses for cod fishery, followed by a
fisheries reorganization in order to adapt to the new ecosystem configuration. Finally, this regime shift led to a considerable increase of fisheries profits due to an outburst of lobster
and crustaceans productivity.
C. Sguotti and X. Cormon
Möllmann 2015). Some ecosystems may be able to absorb
stronger disturbances than others depending on their characteristics, but in general, marine ecosystems are known to be
particularly vulnerable to drastic and unexpected shifts,
referred in ecology as regime shifts (deYoung et al. 2008).
Such non-linear dynamics may have positive or negative outcomes for the sustainable use of natural resources and their
management, therefore they should be taken into account
and dealt with great precaution when taking environmental
policy decisions (Holling 1973; Carpenter 2001; Scheffer
2009; Rocha et al. 2014a).
In this chapter, we first present some examples of marine
ecosystems which have exhibited non-linear dynamics in
response to external changes. These examples allow us to
highlight different mechanisms potentially involved in
regime shifts from an empirical point of view, as well as their
potential implications for the sustainable use of marine
resources. Secondly, we review the regime shift theory and
associated concepts to finally consider recent advances and
future challenges of integrating regime shift theory into
holistic marine ecosystem-based management approaches.
Marine Ecosystems Regime Shifts All
Over the World
Although the regime shift concept is still vigorously discussed, an increasing number of studies provide evidence for
the potential of abrupt changes and surprises in marine ecosystems worldwide (Steneck et al. 2002; Beaugrand 2004;
Mumby et al. 2007; Möllmann et al. 2008, 2009; Mumby
2009; Bestelmeyer et al. 2011; Frank et al. 2011, 2016; Llope
et al. 2011; Beaugrand et al. 2015; Gårdmark et al. 2015;
Ling et al. 2015; Vasilakopoulos and Marshall 2015; Auber
et al. 2015). These studies, based on empirical observations,
highlight mechanisms of regime shifts, firstly formulated by
theoretical studies (Holling 1973; May 1977; Scheffer et al.
2001).
The Atlantic Cod Trophic Cascade
Surprises in natural systems are relatively common and can
happen even in well-studied systems, due to different drivers. One driver of non-linear dynamics is the overfishing of
top-predators. Top-predator overfishing may cause the depletion and collapse of their population resulting in unexpected
ecosystem structure reorganizations through trophic cascades (Myers and Worm 2005; Fauchald 2010; Llope et al.
2011; Möllmann and Diekmann 2012; Steneck and Wahle
2013). Atlantic cod (Gadus morhua) is an important toppredator fish species, which can regulate marine ecosystems
through top-down control, and has supported entire human
communities through fisheries for centuries (Haedrich and
Hamilton 2000; Myers and Worm 2005). After the industrial
revolution and the increase of fishing power and capacity
around the 1980s–1890s, many cod stocks collapsed bringing high economic losses (Myers et al. 1997; Frank et al.
2016). Multiple analyses conducted in different basins such
as in the Baltic Sea or in the Eastern Scotian Shelf, showed
that the collapse of cod stocks was caused by a combination
of increased fishing pressure and unfavorable climatic conditions (Frank et al. 2005, 2016; Casini et al. 2008b; Möllmann
et al. 2008, 2009). The high economic loss and social issues
induced, led governments to adopt a range of management
measures, such as drastic quota reductions and, in some
cases, even fishing moratoria. Nevertheless, despite all the
management measures and plans adopted, cod stocks failed
to recover (Hutchings 2000; Frank et al. 2011; Hutchings
and Rangeley 2011).
One of the reasons advanced to explain these management
failures is the undergoing non-linear dynamics known as trophic cascades (Casini et al. 2008a; Star et al. 2011). Indeed,
the collapse of this top-predator resulted in a shift from a
cod-dominated to a forage fishes-dominated system (Frank
et al. 2005; Gårdmark et al. 2015). Before overfishing, adult
cod biomass level was high and cod controlled forage fish
populations through predation. This hindered the forage fish
from negatively impacting younger cod (through predation
and/or competition), thus enhancing its biologically sustainable biomass. However, when cod biomass became depleted,
the consequently increased forage fish abundance caused a
further decline of cod population by increasing their negative
direct (predation) or indirect (competition) impacts on
younger cod. This feedback loop is then very difficult to
reverse (Walters and Kitchell 2001; Möllmann et al. 2009;
Nyström et al. 2012). Based on this example, it is clear how
such systems can show two distinct configurations depending
on their level of top-predator biomass. Of course, changes in
mid-trophic levels will also reflect in lower ones, for instance
high abundance of forage fishes will likely reduce plankton
abundance. Under this new configuration with low cod biomass, a reduction in fishing pressure would likely lead to a
very delayed or even none cod recovery, since new mechanisms would keep its population in the new depleted state. To
summarize, both Baltic Sea and Scotian Shelf regime shifts
were caused by a combination of overfishing and climate
variation, and characterized by a trophic cascade (top-down
mechanism) due to the depletion of Atlantic cod stocks
(Frank et al. 2005; Casini et al. 2008b; Llope et al. 2011;
Möllmann and Diekmann 2012). This led to immediate high
social and economic losses for cod fishery, followed by a
fisheries reorganization in order to adapt to the new ecosystem configuration. Finally, this regime shift led to a considerable increase of fisheries profits due to an outburst of lobster
and crustaceans productivity.
C. Sguotti and X. Cormon