Bottom-trawling along submarine canyons impacts deep sedimentary regimes

Many studies highlight that fish trawling activities cause seafloor erosion, but the assessment of the remobilization of surface sediments and its relocation is still not well documented. These impacts were examined along the flanks and axes of three headless submarine canyons incised on the Barcelona continental margin, where trawling fleets have been operating for decades. Trawled grounds along canyon flanks presented eroded and highly reworked surface sediments resulting from the passage of heavy trawling gear. Sedimentation rates on the upper canyon axes tripled and quadrupled its natural (i.e. pre-industrialization) values after a substantial increase in total horsepower of the operating trawling fleets between 1960 s and 1970 s. These impacts affected the upper canyon reaches next to fishing grounds, where sediment resuspended by trawling can be transported towards the canyon axes. This study highlights that bottom trawling has the capacity to alter natural sedimentary environments by promoting sediment-starved canyon flanks, and by enhancing sedimentation rates along the contiguous axes, independently of canyons’ morphology. Considering the global mechanisation and offshore expansion of bottom trawling fisheries since the mid-20th century, these sedimentary alterations may occur in many trawled canyons worldwide, with further ecological impacts on the trophic status of these non-resilient benthic communities.


Results
Results of the parameters analysed for all sediment cores are presented separately for the three studied canyons. Table 1 provides information on the location and sampling depth of all sediment cores and summarizes the main parameters derived from radionuclide analyses, while Figs 2-4 show the concentration profiles of excess 210 Pb and 137 Cs (when applicable). Supported 210 Pb concentrations obtained either from complete decay of excess 210 Pb in depth or from the quantification of 226 Ra through gamma analyses were similar, ranging between 30 and 36 Bq·kg −1 , and comparable to concentrations obtained in other studies from the Catalan margin 30,46 . Grain size and dry bulk density profiles of sediment cores are given in Supplementary Figs S1-S3.
Morràs Canyon. Canyon flank. Sediment cores retrieved along the northern canyon flank of this submarine canyon at ~700 m water-depth, where trawling takes place, have similar grain size (73% and 25% of silt and clay) and very low sand content ( Supplementary Fig. S1). In both cores, slight sediment coarsening is present in the upper layers, caused by an increasing fraction of sand and reduction of clay. Dry bulk densities of both sediment cores were similar in the surface layers (~0.6 g·cm −3 ). In Morràs 1, dry bulk density increased steadily down-core to ~0.8 g·cm −3 at 25 cm, where sediment reached maximum consolidation and remained constant with depth, while in Morràs 2 it rapidly reached ~0.8 g·cm −3 in the upper 5 cm and remained constant below.  The concentrations of excess 210 Pb in the upper 10 cm of Morràs 1 were constant (averaging 196 ± 17 Bq·kg −1 ) and subsequently decreased until reaching the excess horizon at 25 cm, with a total inventory of 19600 ± 600 Bq·m −2 (Table 1; Fig. 2). A mass accumulation rate of 0.150 ± 0.011 g·cm −2 ·y −1 (0.207 ± 0.016 cm·y −1 ) was estimated from the excess 210 Pb concentration profile below the upper mixed layer. In Morràs 2, superficial sediments presented low excess 210 Pb concentrations (55 ± 10 Bq·kg −1 ) that rapidly decreased to a constant 8 ± 2 Bq·kg −1 excess 210 Pb concentration at 3-10 cm, before reaching the excess 210 Pb horizon (Fig. 2). The excess 210 Pb inventory was of 900 ± 100 Bq·m −2 , an order of magnitude lower than in Morràs 1. Sediment accumulation rates could not be calculated for Morràs 2.
Canyon axis. Grain size distributions of sediment cores retrieved from the Morràs canyon axis at ~800 m depth (Morràs 3) and ~1000 m depth (Morràs 4) were similar to those in the canyon flank, with predominant silt (74%) and clay (24%) fractions and minor presence of sand (< 0.5%) ( Supplementary Fig. S1). Dry bulk density profiles of both cores were similar, with low values of ~0.4 g·cm −3 at the surface that increased in the upper 10 cm to ~0.7 g·cm −3 , followed by a steady increase in depth reaching similar maximum consolidation (~0.8 g·cm −3 ) as the sediment cores from the flanks (Supplementary Fig. S1).
The 210 Pb concentration profile of Morràs 3 shows two different decreasing gradients in depth, with an average mass accumulation rate of 0.090 ± 0.005 g·cm −2 ·y −1 (0.128 ± 0.007 cm·y −1 ) in the lower sections overlain by a higher sediment mass accumulation rate of 0.184 ± 0.009 g·cm −2 ·y −1 (0.322 ± 0.016 cm·y −1 ) (Fig. 2). Although the change of 210 Pb concentration in the upper 10 cm could have been confounded by mixing associated to bioturbation and physical reworking of sediments, the 137 Cs time-markers support an almost tripling of the sedimentation rate in the early 1970 s: the 1986 Chernobyl accident at 6-7 cm, and the 1963 maximum fallout at 11-12 cm (Fig. 2). The gradually-decreasing base of the 137 Cs profile imply that this radioisotope has presented a certain downward mobility 46,47 so the 1950 s time-marker could not be identified.
On the other hand, there is no evidence of a change in sedimentation rate in Morràs 4, as shown by the single decreasing excess 210 Pb slope, below a 4 cm surface mixed layer, that corresponds to a sediment accumulation rate of 0.129 ± 0.005 g·cm −2 ·y −1 (0.200 ± 0.007 cm·y −1 ). This core did not present clear 137 Cs maxima, although a relative increase at 8 cm could correspond to the 1986 Chernobyl accident. Nevertheless, the sharp base of the 137 Cs profile, attributable to the early 1950 s, validates the 210 Pb-derived sedimentation rates.
Besòs 2 and 3 also presented different dry bulk density profiles from Besòs 1. In Besòs 2 and 3, bulk density of surface unconsolidated sediment (< 0.4 g·cm −3 ) rapidly increased in the first 10 cm to approximately 0.7 g·cm −3 , from where it then gradually increased with depth to its maximum consolidation (~0.8 g·cm −3 ). In the case of Besòs 1, dry bulk density increased steadily throughout the whole profile from 0.6 g·cm −3 to almost 0.8 g·cm −3 in its bottom-most layer ( Supplementary Fig. S2), which suggests a higher sedimentation in this site in comparison to sediment cores retrieved farther down-canyon.
The horizon of excess 210 Pb profile of Besòs 1 was not reached despite the length of this core (55 cm), thus its inventory is estimated to be greater than 54 000 Bq·m −2 . The concentration profile of excess 210 Pb displays a surface mixed layer in the upper 4 cm, followed by two similarly-decreasing trends of 210 Pb with equivalent sedimentation rates of 0.63 ± 0.06 g·cm −2 ·y −1 (0.98 ± 0.08 cm·y −1 ) and 0.61 ± 0.04 g·cm −2 ·y −1 (0.92 ± 0.06 cm·y −1 ), interrupted by a layer of constant 210 Pb concentrations at 25-28 cm, that is interpreted to be the result of a rapid sedimentation pulse-event during the early 1990 s (Fig. 3). Below 40 cm, a gentler 210 Pb slope reveals a lower sedimentation rate of 0.28 ± 0.03 g·cm −2 ·y −1 (0.39 ± 0.04 cm·y −1 ), indicating that recent sedimentation rates almost tripled over the early 1970 s (Fig. 3). These sediment accumulation rates, along with the pulse-event, were corroborated by the 137 Cs concentration profile, whose base, dated in the early 1950 s, and the overhead concentration maximum, attributed to the 1986 Chernobyl accident, are preserved (Table 1; Fig. 3). The 1963 time-marker is not clearly detected in this core, but based on the shape of the 137 Cs concentration profile it could correspond to 41 cm, which also concurs with the 210 Pb-derived ages.
In Besòs 2, excess 210 Pb concentrations decreased with depth along the core, with an intermediate constant concentration between 12 and 15 cm in depth (Fig. 3). Similar sedimentation rates were obtained below and above this layer, 0.118 ± 0.008 g·cm −2 ·y −1 (0.180 ± 0.012 cm·y −1 ) and 0.110 ± 0.002 g·cm −2 ·y −1 (0.205 ± 0.005 cm·y −1 ), respectively, interrupted by a rapid sedimentation pulse-event dated in the early 1960 s. The concentration profile of 137 Cs clearly preserves the relative maxima corresponding to the Chernobyl accident in 1986, which agrees with the 210 Pb-derived ages (Fig. 3). The 1963 time-marker is not easily identifiable, since it is affected by the presence of the pulse-event, although a concentration maximum at 14 cm may suggest its presence during this episode, which also concurs with 210 Pb-derived ages. In depth, the 1950 s time-marker is not identified since the gradually-decreasing concentration of 137 Cs at the base of this profile indicates some downward mobility of this radioisotope (Table 1; Fig. 3).
Farther down-canyon, the 210 Pb concentration profile of Besòs 3 reveals a 5 cm surface mixed layer, overlaying a sedimentation rate of 0.057 ± 0.002 g·cm −2 ·y −1 (0.078 ± 0.003 cm·y −1 ). This sedimentation rate is corroborated by the 137 Cs relative maximum at 5 cm, which is attributed to the 1963 peak fallout (Fig. 3). Considering the low sedimentation rate of this sediment core, 137 Cs may have been subjected to minor mobility, displacing the base Scientific RepoRts | 7:43332 | DOI: 10.1038/srep43332 of 137 Cs slightly downwards (Fig. 3). The 1986 Chernobyl time-marker is not preserved, as it would have been located in the surface mixed layer.
Arenys Canyon. Sediment cores retrieved along the Arenys Canyon axis at ~1100, ~1400 and ~1650 m depth consist mostly of silt (74%) and clay (25%), with minor sand fraction (< 0.5%). As observed in the other canyons, there is also a gradual coarsening of grain size in the upper layers caused by an increase in the contents of silt ( Supplementary Fig. S3).
Dry bulk density in Arenys 1 steadily increased from ~0.4 g·cm −3 at the surface to ~0.9 g·cm −3 at 15 cm in depth, remaining constant down to the bottom of the core. For both Arenys 2 and 3, dry bulk density increased more rapidly, reaching ~0.8 g·cm −3 at about 10 cm ( Supplementary Fig. S3).
The excess 210 Pb concentration profile of Arenys 1 presents a thin surface mixed layer of 2 cm and, below, two distinct slopes attributable to two different sediment accumulation rates: 0.061 ± 0.004 g·cm −2 ·y −1 (0.078 ± 0.005 cm·y −1 ) that increased to 0.176 ± 0.009 g·cm −2 ·y −1 (0.297 ± 0.015 cm·y −1 ) in the early 1970 s. These sediment accumulation rates are confirmed by the three identified 137 Cs time-markers ( Fig. 4; Table 1). The higher sedimentation rate in the upper layers is also evident in the dry bulk density profiles, where sediment in these layers presented a lower compaction in depth compared to Arenys 2 and 3 ( Supplementary Fig. S3).
Evolution of the fishing fleet. The Barcelona trawling fleet experienced its greatest expansion during the 1950-1970 s, when total number of operating trawlers doubled (from 12 to 24 active trawlers) with the construction of new and more powerful vessels (Fig. 5a), leading to a 5-fold increase in registered total horsepower (from 1050 to 5500 HP). Total horsepower of this fishing fleet peaked during the 1990 s, after which it decreased by 30% (from ~7300 HP to ~5100 HP) along a noteworthy dismantling of 29 trawlers, replaced by 14 new trawlers. Despite this net decrease, the average horsepower still increased by 50% over this period (Fig. 5a).
The growth of the Arenys trawling fleet was delayed by a decade in comparison to Barcelona and it occurred over the 1960-1980 s, also doubling (from 8 to 17) and leading to an almost 6-fold increase in registered total horsepower (from 750 to 4350 HP). These increases were accompanied by a three-fold increase in average horsepower over this period (Fig. 5b). As with the Barcelona fishing fleet, total horsepower peaked over the 1990 s and then almost halved over the following decades (from ~5500 HP to ~3100 HP), with 15 trawlers dismantled and replaced by 9 new ones. Despite this overall decrease, the average horsepower remained constant during this period (Fig. 5b).

Discussion
Several impacts caused by bottom trawling are evident in the sediment cores collected in the Barcelona continental margin (Fig. 1). Regarding the alterations observed on canyon flanks, Morràs 1, retrieved on fishing grounds along the Morràs Canyon flank at ~700 m depth, exhibits concentrations of excess 210 Pb in the upper 10 cm that are constant and lower than expected considering the water depth of this core 46 . This might result from the piling of overworked sediments by the passage of trawling gears, as evidenced on ROV footage of trawled flanks of La Fonera Canyon 20 . Interestingly, the depth of reworked sediments in this core concurs with estimated penetration depths of otter trawls in muddy sediments 10,48 , which upholds this hypothesis. For Morràs 2, also retrieved on fishing grounds at ~700 m depth, the surface excess 210 Pb concentrations were an order of magnitude lower than in the adjacent core Morràs 1, while the horizon of excess 210 Pb and the maximum consolidation of sediment were reached at barely 10 cm (Fig. 2, Supplementary Fig. S1), leading to a substantially lower inventory of 900 ± 100 Bq·m −2 in comparison to 19 600 ± 600 Bq·m −2 calculated for Morràs 1   Table 1). All this suggests that a significant amount of sediment was removed by the passage of heavy trawling gears, which can be estimated as almost a century-worth of sediment deposited in this area. The constant excess 210 Pb concentrations observed between 3 and 10 cm can be related to heavily reworked sediments homogenized by the passage of the trawling gear, further highlighting the capacity of otter trawls to erode and homogenize the seafloor.
Concerning the cores taken within canyon axes, increases in sedimentation rates were observed in all sediment cores retrieved in the upper canyon region (i.e., Morràs 3, Besòs 1 and Arenys 1), starting synchronously in the late 1960 s -early 1970 s (Figs 2,3,4 and 6). These increases are unlikely attributable to the arrival of allochtonous sediments transported by natural processes, since there is no evidence in the study area of an intensification of storms or dense shelf water cascading events during the last decades. Moreover, the sediment yields from rivers discharging in the area have been drastically reduced by 75 to 90% since the early 1960 s, mostly due to river damming 49 , limiting the riverine sediment inputs to the margin. Therefore, such increases of sedimentation rates within submarine canyons have been interpreted here as being associated to the sediment resuspension caused by trawling activities since their industrialization (Fig. 5) and to a greater sediment input carried by the regional Northern current along the upper and mid-slope depths due to this activity. The excess 210 Pb concentration profiles in these cores indicate that this enhanced sedimentation is a continuous process, and cannot be the result of localized sediment mass-transport events. If so, they would have generated non-steady 210 Pb profiles or levels of constant excess 210 Pb concentrations, and possibly a distinct signature in the grain size fraction associated to these events. In this regard, only the shallower cores collected in the Besòs Canyon exhibited sediment layers that could be interpreted as generated by rapid sedimentation events, most likely derived from slope instabilities and mass failures from the canyon flanks (see discussion below).
Within the Morràs canyon, only Morràs 3, collected at ~700 m depth and located within the trawling depths of the Barcelona fleet, presents a significant (threefold) increase of sediment accumulation rate during the early 1970 s. Despite the closeness of Morràs 4 to trawling grounds, it remained unaffected. This sediment core was collected at ~1000 m depth, deeper in relation to the trawlers' 900 m maximum depth extension, thus being out of reach of the advection of the enhanced sediment input that could ultimately alter its sedimentation rates (Figs 2 and 6).
In the narrow Besòs canyon axis, only Besòs 1 located in the upper canyon ~800 m depth and down-current of trawling grounds showed a threefold increase in sedimentation rates during the early 1970 s (Fig. 3). Both this sediment core and Besòs 2, located at ~1200 m depth, presented sediment pulse-events, evidenced by layers of constant 210 Pb concentrations along with constant grain size throughout the cores (Fig. 3 and Supplementary Fig. S2). As previously mentioned, these events may result from submarine canyon slope failures, which are usually triggered by external factors that can destabilize sediment along the canyon flanks 50 . These pulse-events occurred in coincidence with maximum total horsepower in 1990 s for Besòs 1 and the period of greatest modernisation of the fishing fleet in the early 1960 s for Besòs 2 (Figs 3 and 5), suggesting that this rapid accumulation may also have been set off by trawling. After these events, sediment rates returned to those enhanced by trawling in Besòs 1 and to the rates not affected by trawling in Besòs 2, since it is out of reach of the enhanced input of trawled sediment (Figs 3 and 6), as is the case of Besòs 3, located further down-canyon at ~1500 m depth.
Finally, the Arenys canyon axis presented a fourfold increase in sediment accumulation rates in the early 1970 s on the shallower coring site next to trawling grounds, whereas in deeper canyon areas, far away of the trawled flanks, sedimentation rates remained unaffected (Figs 4 and 6).
To our knowledge, the evident capacity of trawling activities to resuspend and erode sediments on the canyon flanks 20,27 , ultimately increasing sediment accumulation rates in submarine canyon environments due to the modernisation of the local trawling fleet, has only been reported in one coring site at La Fonera Canyon axis, around 1700 m depth 30,31 (Fig. 1). A similar upgrade occurred in the Barcelona and Arenys trawling fleets in terms of number of operating vessels and their total and average horsepower (Fig. 5). Over the late 1960 s and early 1970 s, new trawlers became highly technicized, accompanied by the expansion of fishing grounds to deeper depths 16 , which require greater engine power to haul the heavier gears 17 , thus increasing their capacity to resuspend sediment. This resulted in an enhanced input of sediment over the slope region that can be transported by the regional Northern current, increasing sedimentation rates over this period in the upper reaches of the Morràs, Besòs, and Arenys canyons (Fig. 6).
Our observations provide new evidences of the capacity of trawling activities to modify natural sedimentary processes in continental slope environments. Trawling-induced alterations of sedimentation processes within the studied submarine canyons is limited to their upper reaches, where trawling takes place in the contiguous flanks, tripling and quadrupling sedimentation rates on their axes since the period of greatest expansion of the operating trawling fleet (Fig. 5). These results highlight that the effects of trawling in canyon sedimentary regimes are confined to a specific area downslope from trawling grounds, leaving farther and deeper areas in the canyon unaffected (Fig. 6). Our study suggests that submarine canyons impacted by trawling, including those non-incised in the continental shelf, can have altered sedimentary regimes along their flanks and axes, creating anthropogenic sedimentary depocenters.
Indeed, the evolution of the bottom trawling fleets of the ports of Barcelona and Arenys are not only in accordance with those of the port of Palamós 30 , but also with all bottom trawler fisheries operating in the Mediterranean Sea, which have shifted their target species to deep-water crustaceans over this same period 51 .The most relevant bottom trawling European fisheries in the Mediterranean Sea (Italy, Spain, and Greece) augmented substantially between the 1960 s and 1980 s ( Supplementary Fig. S4). This modernization is especially evident for the Italian trawling fleet, which experienced an order of magnitude increase of its fishing fleet and total horsepower, while Spain and Greece tripled the number of operating vessels and total horsepower during this period. Taking this into account and the extension of trawling activities along the canyoned Mediterranean margin 52 , it is likely that they have all experienced perturbations in their sedimentary regime: transformation of canyon flanks into sediment-starved areas and enhancement of sedimentation rates within the proximal canyon axis. Considering the global expansion of bottom trawling fisheries 20 , similar impacts might be occurring in other submarine canyons at a global scale.
Until recently, the awareness of bottom trawling impacts has been mostly restricted to fishing grounds 10-12 , but trawling-derived impacts are not limited to this area. The enhanced sedimentation rates evidenced in La Fonera 30,31 , and now in Arenys, Besòs, and Morràs canyons, which have received three to four times more sediment since the 1970 s, can lead to several ecological implications. On one hand, the arrival of such substantial volume of sediment over several decades to these low resilient environments can smother benthic organisms and alter their communities 31,48,53,54 . Moreover, submarine canyons are important habitats for cold water corals, but only occupy areas where hydrodynamics prevent high sedimentation rates 55 . Recent ROV footage of La Fonera Canyon have identified scarce cold water coral colonies in areas with presumably high sediment input induced by trawling along the contiguous flank, suggesting that sediment concentrations have surpassed these corals' threshold 56 . On the other hand, sediment that is being accumulated come from nutrient-depleted sediment found on trawling grounds 57,58 , which may also affect the trophic status of benthic communities in these deep environments that rely on the arrival of sediment rich in organic matter. These extended impacts of trawling activities within canyon axes should be considered when establishing deep bottom-trawling regulations.

Sampling.
A total of 10 sediment cores were obtained during several oceanographic campaigns aboard the R/V García del Cid: two along the flanks of the Morràs Canyon and two more in its axis, and three sediment cores along the axes of Besòs and Arenys submarine canyons (Table 1; Fig. 1). The sediment cores were all retrieved using a KC Denmark A/X 6-tube (inner diameter 9.4 cm) multicorer that can recover sediment cores of up to 60 cm in length. In every operation, the best-preserved core was chosen for analysis, based on a clear and undisturbed sediment-water interface that indicates minimal sediment disturbance during sampling. Sediment cores were then subsampled at 1 cm intervals and each section was kept frozen in sealed plastic bags until analysis.
Analytical Procedures. Frozen samples were first weighed and then lyophilized for approximately 30 hours using a Laboratory Freeze Dryer at − 50 °C and 0.005 mbar or lower. Dry weights were recorded and dry bulk density was determined by dividing the net dry weight corrected for salt content by the sample volume, the latter estimated assuming a seawater density of 1.025 g·cm −3 and an average grain density of 2.65 g·cm −3 .
Grain size fraction was determined using a Horiba Partica LA-950V2 particle-size analyzer, with an accuracy of 0.6% and 0.1% precision. Prior to this analysis, 1-4 g of each sample were oxidized using 20% H 2 O 2 for a week and then left overnight with a solution of P 2 O 7 to disaggregate the sediment particles. Concentrations of 210 Pb were determined through the analysis of the activity of its granddaughter 210 Po by alpha-spectroscopy 59 , assuming secular equilibrium of both radionuclides at the time of analysis. Samples were traced using 209 Po, followed by an acid digestion using an analytical microwave, and polonium isotopes were subsequently plated on silver discs. Alpha emissions were quantified using Passivated Implanted Planar Silicon (PIPS) detectors (CANBERRA, Mod. PD-450.18 A.M) with a MaestroTM data acquisition software. Supported 210 Pb concentrations were determined by averaging total 210 Pb concentrations at the base of each profile, verified with the 226 Ra concentrations obtained by gamma-spectroscopy. This latter method was employed in cores where the horizon of excess 210 Pb was not reached. Concentrations of 226 Ra were determined through the emission peaks of its two decay products 214 Pb (295 and 352 keV peaks) and 214 Bi (609 keV peak) using a high-purity germanium detector (CANBERRA, mod. GCW3523) in calibrated geometries, sealed for 21 days to reach secular equilibrium with 214 Pb and 214 Bi. In some sediment cores, the concentration profiles of 137 Cs were quantified using gamma-spectroscopy. Sediment accumulation rates were calculated based on accumulated dry mass to correct for sediment compaction in depth, applying the constant flux : constant sedimentation (CF:CS) model 60 . Given that biological and physical reworking of superficial sediments can alter the excess 210 Pb concentration profiles, which can be confounded as being produced by greater sedimentation rates, the congruency of the 210 Pb derived dates was corroborated with the 137 Cs time-markers 61 . These time-markers are: i) the depth at which 137 Cs is detected, dated on the early 1950 s, resulting from the first detonations of thermonuclear weapons and consequent significant emissions of artificial radioactivity to the atmosphere during these years 62 ; ii) a relative concentration maxima corresponding to the time at which maximum deposition occurred prior to the cessation of nuclear atmospheric testing in 1963, and iii) a second relative concentration maxima derived from the emissions of the Chernobyl accident in 1986 47 65 . This database also holds information of the vessel such as its heading, speed, and registered harbor. The spatial distribution of large trawlers (boat length greater than 15 m) on the Barcelona continental margin for the period 2005-2011 is shown in Fig. 1.
Fishing grounds along the Arenys, Besòs, and Morràs canyons are trawled by vessels from the Port of Arenys and the Port of Barcelona, as confirmed from VMS data (Fig. 1). Additional information of trawlers from these ports was obtained from the Community Fishing Fleet Register 64 , an online European Union database that registers the full history of fishing vessels from a Member State along with their characteristics.
Information of bottom trawlers from other European countries with the most relevant bottom trawling fisheries in the Mediterranean Sea 51 was also obtained from the Community Fishing Fleet Register. Full histories of bottom otter trawls of Spain (Mediterranean harbours), Italy and Greece were collected along with their operating ports.