Discussion
The present study identifies regime shifts in a long-term metric of
biological productivity in relation to regime shifts in potential causal
drivers, using a Bayesian online change point detection (BOCPD)
algorithm. Juvenile Atlantic cod in Norwegian coastal Skagerrak
experienced two stepwise reductions in mean abundance, beginning in 1975
and 1999, ultimately attaining a level ~30% of what it
was in the first half of the 20th Century. Regime
shifts in indices for the NAO and zooplankton abundance since 1960 were
directionally the same, the opposite, or independent of directional
shifts in cod catch rates. The degree of temporal overlap between
regimes shifts in cod abundance and water temperature depended on
season. Single regime shifts of increased mean temperature (by 1 to
20C) during the winter and spring months either
preceded the 1999 cod regime shift by more than a decade or occurred
several years thereafter. However, summer-autumn temperature regime
shifts (1 to 20C increase) were either concomitant
with, or occurred slightly in advance of, the cod regime shift
(decrease) in 1999. The earlier cod regime shift (1975) was not
associated with a regime shift in water temperature for any month of the
year.
The relative importance of hypothesized drivers can be ascertained by
the temporal proximity of their regime shifts with regime shifts in cod.
It is clear that shifts in some factors, such as the NAO index and
abundance of C. finmarchicus , do not always have obvious
biological consequences for Atlantic cod. Against the background of
temporal changes in fishing mortality and spawning stock biomass of
North Sea cod, the earliest regime shifts in NAO (1961; a decline from
0.2 to -2.0) and C. finmarchicus (1982; a ~75%
decline) were not linked with regime shifts in cod (Fig. 3a). The same
was true of the 1-20 C regime-shift increase in water
temperature during the winter-spring months in 1988.
One interpretation of this lack of influence is that drivers of cod
productivity are less likely to manifest biological change when (i) they
act singly, (ii) human-induced mortality is relatively low, and (iii)
cod population size is relatively high. When the NAO shifted in 1961,
fishing mortality on North Sea cod was less thanFlim and SSB was 1.36Blim ; when zooplankton abundance shifted
downwards in 1982, fishing mortality was increasing but population
biomass remained high (1.53 Blim ). Regarding the
winter-spring increase during the regime shift in water temperature that
began in 1988, it is notable that, despite these increases, temperatures
remained well within the range thought to be optimal for cod eggs and
larvae (Nissling 2004; Righton et al. 2010). Indeed, these January-June
regime shifts might have had a beneficial influence on cod productivity,
mitigating to some extent any steadily increasing effects of
persistently high fishing mortality and declining SSB.
Our analyses reveal two occasions when regime shifts in potential
drivers of cod productivity preceded regime shifts in cod catch rate by
a time period sufficiently brief (< 5 yr) that they
could plausibly have influenced the subsequent abundance of cod aged 0+
to 2+ years (Fig. 6). Even though a decline in NAO in 1961 had no
discernable effect on cod, the increase in 1972 might well have, insofar
as the first cod regime shift followed two years later. This supposition
is supported by studies (e.g., Stige et al. 2006) that have concluded
that an increased NAO index has a negative influence on cod productivity
in the northeast Atlantic. One possible reason for why the NAO
apparently affected cod (beginning in 1974) is that the magnitude of the
NAO regime shift (−2.0 to 1.5) was the greatest of the three shifts that
occurred between 1864 and 2018. It is also notable, however, that the
1974 cod regime shift occurred during a period of steadily increasing
and unsustainably high fishing mortality (1.5Flim ), potentially affecting the ability of cod
to resist environmental changes caused by the NAO, changes to which an
unfished population might have been resilient. This underscores the
challenge in disentangling the effects of fishing and climate-related
indices on biological productivity.
The cod regime shift that began in 1999 was preceded by a ‘perfect
storm’ of multiple concomitant changes in the environment. Summer-autumn
temperatures jumped 1-20 C; the NAO index declined
from 1.5 to 0.5; C. finmarchicus had plunged to its lowest level
in the time series; fishing mortality was at its highest level since
1963 (2.0 Flim ); and spawning stock biomass was
at its lowest level in the time series (0.8 Blim )
en route to a minimum of 0.41 Blim in 2006. The
effects of the NAO, C. finmarchicus , and temperature on cod
productivity were undoubtedly accentuated by the directionality of their
regime shifts in 1999. As the NAO index declines, so does primary and
secondary productivity in Skagerrak (Tiselius et al. 2016), and
increased water temperatures are associated with increasingly
unfavourable conditions for C. finmarchicus (Fromentin et al.
1998).
Among the putative drivers of cod productivity, the 1996 regime shift in
NAO may have been the most benign, given that (i) a reduction in the
index did not have its anticipated positive effect on cod and that (ii)
the index had returned to levels characteristic of the 1868 to 1960
period. The very considerable reduction in C. finmarchicus(beginning in 1997; Fig. 3) was likely a much more prominent factor,
given the exceedingly low levels to which this key prey species of
juvenile cod had declined.
There is, however, reason to believe that the summer-autumn increase in
water temperature was of considerably greater importance than either the
NAO or zooplankton abundance. Successive regime shifts from 1994 to 1999
during July through October raised temperatures to their highest
recorded levels in coastal Skagerrak since 1925, when the time series
began. In some years, mean August temperatures exceeded
200C, approaching the critical thermal maximum for
Atlantic cod (Righton et al. 2010; Norin et al. 2019).
We hypothesize that cod did not respond positively to the presumed
increased in food supply in 2008 because of the physiological stress
associated with increased summer-autumn water temperatures. Based on
tagging studies at sea of almost 400 cod from 8 northeast Atlantic cod
stocks, Righton et al. (2010) found that although the total thermal
niche of adult cod ranged between −1.5 and 19.00 C,
the temperature range was considerably narrower during the spawning
period when larval and juvenile cod are developing (1 to
80 C). Nissling (2004) reported that survival of
larval cod in the laboratory declined considerably when water
temperatures exceeded 100 C.
One fundamentally important element to consider when evaluating the
consequences of climate-related and environmental regime shifts on
population productivity is the size of the population relative to a
metric of long-term sustainability, such as carrying capacity or
population size in an unfished state. This is because small populations
are more vulnerable to environmental stochasticity than comparatively
large populations (Lande 1993). This link between population size and
susceptibility to environmental change has been repeatedly considered
when assessing the recovery capacity of depleted cod populations
(Hutchings and Myers 1994; Hutchings and Kuparinen 2017). But it has
also been made with respect to potential drivers of cod regime shifts.
Based on an analysis of cod populations on the European Shelf south of
62oN, including North Sea cod, Brander (2005)
concluded that environmental variability, as represented by the NAO
index, only affects cod when the spawning stock biomass is low.
Brander’s (2005) argument is both theoretically compelling and
empirically supported by the present study.
There are several attributes to the methodology we have applied here.
Firstly, the same algorithm is used to identify regime shifts in a
metric of biological productivity and putative causal drivers of that
metric. Secondly, our approach greatly reduces the subjectivity inherent
in deciding the magnitude of data change which constitutes a regime
shift (the ‘effect’ size) and when it is that a regime shift occurs; we
did not presume the existence of a regime shift in any given year for
any given variable. A third improvement is that the BOCPD algorithm
accounts for changes in the variance in the data, not simply the mean.
One limitation in our interpretation of the relative importance of
fishing and the environment on regime shifts in cod productivity is our
use of estimates of fishing mortality and spawning stock biomass for
North Sea cod as metrics of fishing pressure and population size for
Skagerrak cod. But if we were to account for fishing mortality in our
analyses, we needed to avail ourselves of the best available data in
this regard, and these data were available for North Sea cod. There are
empirically defensible reasons for our application of North Sea cod
estimates of F and SSB to Skagerrak cod. Firstly, North Sea cod
genotypes exist along the Norwegian Skagerrak coast (Knutsen et al.
2018). Secondly, Skagerrak has long been considered part of the North
Sea cod stock unit (ICES 2019). Thirdly, limited estimates of fishing
mortality available for Skagerrak cod confirm that fishing mortality can
be exceedingly high. Kleiven et al. (2016) reported that recreational
and commercial fisheries for cod in Skagerrak fjords resulted in a
mortality rate of 55.6% for the years 2005 to 2013, equivalent toF =0.81. For comparison, the average F for North Sea cod
over the same time period was 0.61 (ICES 2019), suggesting that the
fishing mortality experienced by North Sea cod may be comparable to, and
possibly less than, that experienced by Norwegian Skagerrak coastal cod
in some years.
The concept of regime shifts permeates the marine ecological and
fisheries literature. Definitions vary considerably. The ecological
literature tends to interpret regime shifts as community-level changes
between alternative stable states with the implication that such shifts
are difficult to reverse (Conversi et al. 2015; Ling et al. 2015). In
contrast, regime-shift analyses of meteorological factors tend not to
focus on alternative stable states, being much more accepting of
regime-shift ‘reversibility’ (e.g., Dippner et al. 2014; Jaagus et al.
2017). The fisheries literature is perhaps intermediate with respect to
the question of regime-shift reversibility. Some work draws attention to
long-term, slow-to-reverse discontinuities in ecosystem properties
(Möllmann et al. 2009), whereas neither reversibility nor regime-shift
time period have been integral to a lack of temporal stationarity in
fish-stock productivity (e.g., Vert-pre et al. 2013; Perälä and
Kuparinen 2015).
Our analyses emphasize the utility in examining multiple regime shifts
when trying to understand the causal mechanisms responsible for regime
shifts in metrics of biological productivity. Doing so allows one to
formulate hypotheses and to draw conclusions concerning the conditional
probabilities that an environmentally related regime shift will affect
biological productivity. One hypothesis that emerges here is that the
strength of the effect of an environmental or climate-related regime
shift is accentuated when it coincides with other regime shifts. A
second hypothesis, underscoring the findings of previous work (Brander
2005; Hutchings and Kuparinen 2017), is that climate-related regime
shifts are more likely to affect populations when they are relatively
small. The present study affirms the dominant role that fishing has on
the probability that populations will respond to regime shifts in
environmental variables, underscoring the fundamental necessity of
accounting for fishing mortality in any analysis of regime shifts in
commercially exploited marine fishes (de Young et al. 2004; Möllmann et
al. 2009).
For our case study of Norwegian Skagerrak cod, our work suggests that
steadily increasing fishing mortality from commercial and recreational
fisheries has increasingly sensitized the cod to regime shifts in NAO,
zooplankton abundance, and water temperature. Fishing mortality remains
unsustainably high in the region (Kleiven et al. 2016). This, coupled
with small population size and increased summer and autumn water
temperatures that broach the thermal limit for the species, are likely
major factors limiting the recovery capacity for cod in southern coastal
Norway.