Discussion
Since the ecological role of taxa heavily depends on their position in
the trophic network, we were interested in identifying whether the
sensitivity and exposure of taxa to fishing pressure (i.e.
vulnerability), completed by taxa’s centrality, could have consequences
on the robustness of the trophic network.
The secondary extinction analysis conducted here highlighted that the
robustness of the Celtic Sea to fishing is not closely related to the
sensitivity of its taxa to this pressure. This behaviour of the network
results from the respective characteristics and feeding ecology of the
taxa. Indeed, in the Celtic Sea, the most sensitive taxa are medium size
elasmobranchs which are not top predators and have medium trophic levels
(circa TL=3). Medium trophic levels taxa often have a high structural
importance, with usually the largest values of centrality (Scotti &
Jordán 2010). However, we showed that this is not the case in the Celtic
Sea were the most sensitive taxa are not the most central and are thus,
if targeted, unlikely to spread a perturbation to the whole network.
Considering both the sensitivity and the exposure to fishing pressure,
we showed that none of the taxa considered in this study is highly
vulnerable to fishing, which could be linked to the long history of
exploitation of the area (Guénette & Gascuel 2012). The most vulnerable
taxa include smooth hound, a sensitive and moderately exposed taxon, as
well as large piscivorous taxa (cod, hake, anglerfishes, plaice, conger,
ling) that are not very sensitive but are highly fished. Amongst these
large piscivorous taxa, cod, anglerfish and hake are central taxa and
are likely to propagate a perturbation to the whole network through
top-down control. These species are important commercial stocks under
quotas in the area, whose decrease should lead to significant cascading
impacts in the trophic network.
The robustness of the Celtic Sea network to the removal of taxa with
many preys and highly connected taxa was relatively high. The removal of
taxa with many preys leads to the fastest collapse of the network, but
only happens after removing 60% of the taxa, which is far from
realistic conditions. Connectance decreases before the network
collapses, making in a first instance the propagation of a perturbation
less likely and the network more robust. Likewise, the network seems
relatively robust to the removal of the most central taxa (decrease in
connectance and a number of secondary extinctions similar to the one
expected by chance). This finding contradicts the expected low
robustness of a network facing the removal of its most connected taxa
(Dunne & Williams 2009; Staniczenko et al. 2010; Curtsdotteret al. 2011; De Visser et al. 2011) but see (Allesina &
Pascual 2009). Nevertheless, the robustness of the network facing these
two removal sequences is in line with the observed increase in
modularity and decrease in nestedness (Fig. S2). Indeed, the increased
modularity indicates an increased compartmentalization, which is known
to promote stability by restricting the spread of the perturbation
outside the module (Thébault & Fontaine 2010). On the other hand, a
decrease in nestedness implies the removal of the redundant trophic
interactions first (Nordstrom et al. 2015), which translates here
into the removal of whiting Merlangus merlangius , megrim and
squid loligo sp. that are preyed upon by generalist taxa.
The removal of taxa with many predators leads to the lowest robustness
of the trophic network. Taxa with the largest number of predators here
belong to intermediate trophic levels (between 3 and 3.5) namely herringClupea harengus , sprat Sprattus sprattus , sardine
Sardina pilchardus , dragonet Callionymus lyra , poutsTrisopterus esmarkii and Trisopterus minutus and horse
mackerel Trachurus trachurus (Table S1). These forage species
account for a large proportion of the biomass of the taxa considered in
this study but also a large proportion in the catches (ICES 2018b;
Hernvann & Gascuel 2020). These species are crucial for the network
stability as their predators display medium to high trophic levels and
are both benthic and pelagic. Hence, forage species allow the coupling
between these two pathways, which has been shown to participate to
trophic network stability and resilience (Blanchard et al. 2011).
In addition, if affected by a perturbation, these taxa heavily
destabilize the network of the Celtic Sea (Moullec et al. 2017).
The food-web topology reconstructed here integrates data from trophic
studies covering a long time-span. Thus, the restructuration of the
network due to changes in diets could not be investigated. Nonetheless,
this makes the response of the network to removal-scenarios
interpretable regarding the long-term history of the ecosystem. The
relatively high robustness of the network to the removal of taxa with
many preys could be one of the stability factors (with predation control
of benthopelagic predator larvae by pelagic fish, Baum & Worm, 2009) of
the more pelagic-dominated state of the ecosystem after the depletion of
high trophic levels before 1980 (Hernvann & Gascuel 2020).
Finally, the network has low robustness to the removal of the most
exposed taxa at early stage of perturbation (i.e. when removing the 7%
of the most exposed taxa). These highly exploited taxa are queen scallopAequipecten opercularis , king scallop Pecten maximus ,
edible crab, European spider crab Maja brachydactyla , cod, sprat
and hake. This increase in connectance originates from a faster decrease
in the number of potential interactions than in the realized ones and is
due to these removed taxa having in general fewer feeding links than the
averaged species in the network. This raised one of the limitations of
network reconstruction, since the taxa considered were sampled with a
bottom trawl that is not adapted to sample the basal components of the
network (phyto and zooplankton are missing while benthos is
underrepresented), as well as the top predators. Nevertheless, taxa
included here are megafauna with the highest occurrence and account for
most part of the network, enabling notably the survival of commercial
taxa. These taxa are thus considered to provide a representative picture
of the Celtic Sea ecosystems. Trophic levels were computed from local
isotopic data collected in the Celtic Sea whereas the trophic links were
taken from the literature. Thus, there might be a mismatch between the
trophic position and the trophic links of some taxa with taxon feeding
on taxon at slightly higher trophic level. However, because the
computation the centrality score of one taxon is not based on data
specific to our study area, it could be applied to other North-East
Atlantic studies. In addition, we did not consider the fluxes of biomass
between taxa, which could modulate our findings. Indeed, it might
influence the spread of a perturbation, with a larger spread between
taxa linked by a large flux of biomass.
Network theory has been identified as a helpful tool to support
ecosystem-based fisheries management (Gaichas & Francis 2008; Deeet al. 2017). Exposure and trait-based sensitivity metrics
relative to fishing brought here a complementary information to the
network analysis. Indeed, our study suggests that widely used mesoscale
metrics such as centrality were not always adapted to prioritize species
conservation to maintain the structure and the functioning of the
network. On the contrary, our exposure metric highlighted that in some
cases, the current fishing exploitation pressure should prevail on
topology-based metrics, while sensitivity must be considered as it
implies different abilities of species to tolerate various exposure
levels. Such metrics are particularly promising in the context of
exploring potential new fishing management strategies. In particular,
integrating the sensitivity to fishing, they could be used to
investigate the risk of exploiting new species regarding to their own
productivity potential (Zhou et al. 2019).
Studying fishing perturbation, we showed that the trophic network of the
Celtic Sea was the least robust to the simulated loss of taxa with many
predators (i.e. forage taxa) and of the 7% taxa the most exposed to
fishing pressure. Estimating the sensitivity to fishing of the 69 taxa
of the network was insufficient to predict its robustness since the
simulated removal of the taxa most sensitive led to a robustness level
similar as that of a random removal sequence. This study focused on
fishing since this variable has a documented impact on taxa’s biomass in
the Celtic Sea, due to the long history of exploitation of this
ecosystem (Hernvann & Gascuel 2020). However, climate change will
likely become the main driver of this ecosystem in the coming years. The
framework proposed in this work could easily be adapted to assess
species sensitivity to temperature or pH tolerance by selecting traits
known to respond to these pressures. Ultimately, such a framework could
be used in complement of management tools to indicate which taxon could
impair ecological network structure and ecosystem functioning under
increasing global change. It could also unravel early warnings about the
loss of certain taxa that could jeopardize a trophic network more than
their sensitivity at the taxon’s level could suggest.