Introduction
A shift in focus from species to ecological networks of interactions has
recently been proposed as a necessary step in the adaptation of
conservation goals to the maintenance of ecosystem integrity and the
services ecosystems underpin (Scotti & Jordán 2010; Harvey et
al. 2017; Pecl et al. 2017). Ecological network enables to
evaluate the vulnerability of ecosystems to a perturbation through the
study of the changes in the structure of the network (Tylianakiset al. 2007; Stouffer & Bascompte 2011; Hattab et al.2016; Robinson & Strauss 2020). Its use to assess ecosystem state has
increased in the recent years as it allows considering in a single
framework the effects of fluctuation in species’ abundance and their
preys and predators, but also on indirectly linked species and the whole
network itself (Jordán et al. 2006; Wallach et al. 2017).
The risk of network collapse can be characterized by its robustness to
species extinction, namely its capacity to withstand the cascading
perturbation generated by the removal of species (Dunne et al.2004; Dunne & Williams 2009; Jonsson et al. 2015). Human impact
on ecosystems is intensifying and has already caused numerous collapses
of species (Duarte et al. 2020). As ecosystems are being degraded
at an unprecedented rate, the need to understand which perturbation
sequences are expected to be more devastating than others has become
pressing (Jonsson et al. 2015). The collapse of some
well-connected species is expected to have a disproportionate impact on
their ecosystems relatively to their biomass, and these species have to
be identified (Jordán 2009; Klemm et al. 2012; Worm & Paine
2016). Central species with a large number of interactions, are likely
to influence numerous species and thus have been defined as network hubs
that should be prioritized for conservation (Curtsdotter et al.2011). To identify these central species, mesoscale measures (i.e.
intermediate level between the species (local) and the entire network
(global)), such as eigenvector centrality, betweenness centrality or
closeness centrality have proven to be particularly suited for the
assessment of species importance in the spread of a perturbation across
the network (Estrada 2007; Jordán 2009).
Sensitivity and vulnerability assessment of species (defined as
sensitivity added to exposure (IPCC 2001)) have largely been conducted
based on species traits (Tillin et al. 2010; Le Quesne &
Jennings 2012; van Treeck et al. 2020). However, to evaluate
properly the potential of a species to spread perturbation across the
network, its centrality should be assessed alongside its sensitivity and
exposure to a given pressure. Indeed, a species can be sensitive and
vulnerable but not central, or it may be central but not sensitive nor
vulnerable. In both cases, the species would not spread a perturbation
across the network. In that sense, one can ask whether the robustness of
the trophic network to the spread of a perturbation can be inferred from
the sensitivity of its components.
To answer this question and shift the sensitivity assessment focus from
species to ecological network, we propose a framework that examines
network robustness to a given perturbation at the local (species),
mesoscale and global (network) level, based on species traits and on the
topology of the network. Specifically, we investigated the impact on the
robustness of the network of the loss of the sensitive species, the
exposed species and the central species.
We applied this framework to fishing pressure robustness of a trophic
network from a historically exploited fishing ground, the Celtic Sea.
Fishing impacts on the ecosystems are numerous, from decreased species
abundance and depletion of higher trophic levels (Pauly & Palomares
2005) to altered trophic networks as fishing pressure increases
(Gilarranz et al. 2016). At the species level, life history
traits (e.g. maximum length, longevity or age at maturity) are good
proxies of species’ demographic characteristics and enable to
characterize their sensitivity to fishing by ranking them along a
“slow-fast” continuum of life history strategies (Le Quesne &
Jennings 2012). Fishing tends to favour small-sized, short-lived species
that mature early and have a better capacity to recover after a fishing
perturbation (Jennings et al. 1998; Le Quesne & Jennings 2012;
Wiedmann et al. 2014). In the Celtic Sea, the intense development
of fishing in the area during the second half of the 20th century until
its climax in the late 1980’s, deeply altered the ecosystem structure
through the depletion of large demersal predators, i.e. cod, whiting,
hake and sole (Guénette & Gascuel 2012; Hernvann & Gascuel 2020).
Based on literature and isotopic measurements for 69 taxa (including
fishes, elasmobranches, cephalopods, bivalves, and crustaceans), we
assessed the vulnerability to fishing of both taxa and the trophic
network structure. Specifically, we investigate whether (i) the most
sensitive and the most exposed taxa to fishing are the most central; and
whether (ii) the loss of sensitive, exposed or central taxa is the most
detrimental for the network robustness. For a better understanding of
the processes at play, we tested the robustness of the network against
different species ‘removal sequences, and notably assessed the
importance of the number of predators and preys.