Biogeosciences, 16, 4307–4320, 2019 https://doi.org/10.5194/bg-16-4307-2019 © Author(s) 2019. This work is distributed under the Creative Commons Attribution 4.0 License. Organic matter contents and degradation in a highly trawled area during fresh particle inputs (Gulf of Castellammare, southwestern Mediterranean) Sarah Paradis1 , Antonio Pusceddu2 , Pere Masqué1,3,4,5 , Pere Puig6 , Davide Moccia2 , Tommaso Russo7 , and Claudio Lo Iacono6,8 1 Institut de Ciència i Tecnologia Ambientals, Universitat Autònoma de Barcelona, Bellaterra, 08193, Spain 2 Dipartimento di Scienze della Vita e dell’Ambiente, Università degli Studi di Cagliari, Cagliari, 09126, Italy 3 Departament de Física, Universitat Autònoma de Barcelona, Bellaterra, 08193, Spain 4 School of Natural Sciences, Centre for Marine Ecosystems Research, Edith Cowan University, Joondalup, WA 6027, Australia 5 School of Physics and Oceans Institute, University of Western Australia, Crawley, WA 6009, Australia 6 Marine Sciences Institute, Consejo Superior de Investigaciones Científicas, Barcelona, 08003, Spain 7 Laboratory of Experimental Ecology and Aquaculture, Department of Biology, University of Rome Tor Vergata, Rome, 00133, Italy 8 National Oceanography Centre, University of Southampton Waterfront Campus, Southampton, SO14 3ZH, UK Correspondence: Sarah Paradis (sarah.paradis@uab.cat) Received: 19 June 2019 – Discussion started: 28 June 2019 Revised: 4 October 2019 – Accepted: 11 October 2019 – Published: 12 November 2019 Abstract. Bottom trawling in the deep sea is one of the main which were between 20 % and 60 % lower than those in the drivers of sediment resuspension, eroding the seafloor and untrawled site. However, the upper 2 cm of the trawled site altering the content and composition of sedimentary organic consisted of recently accumulated sediments enriched in ex- matter (OM). The physical and biogeochemical impacts of cess 234 Th, excess 210 Pb, and phytopigments, while OM con- bottom trawling were studied on the continental slope of tents were similar to those from the untrawled core. This the Gulf of Castellammare, Sicily (southwestern Mediter- fresh sediment supported protein turnover rates of 0.025 d−1 , ranean), through the analysis of two triplicate sediment cores which doubled those quantified in surface sediments of the collected at trawled and untrawled sites ( ∼ 550 m water untrawled site. The enhancement of remineralization rates depth) during the summer of 2016. Geochemical and sedi- in surface sediment of the trawled site was associated with mentological parameters (excess 210 Pb, excess 234 Th, 137 Cs, the arrival of fresh particles on a chronically trawled deep- dry bulk density, and grain size), elemental (organic carbon sea region that is generally deprived of OM. We conclude and nitrogen) and biochemical composition of sedimentary that the detrimental effects of bottom trawling can be tem- OM (proteins, carbohydrates, lipids), as well as its freshness porarily and partially abated by the arrival of fresh and nu- (phytopigments) and degradation rates were determined in tritionally rich OM, which stimulate the response of benthic both coring locations. The untrawled site had a sedimenta- communities. However, these ephemeral deposits are likely tion rate of 0.15 cm yr−1 and presented a 6 cm thick surface to be swiftly eroded due to the high trawling frequency over mixed layer that contained siltier sediment with low excess fishing grounds, highlighting the importance of establishing 210 Pb concentrations, possibly resulting from the resuspen- science-based management strategies to mitigate the impacts sion, posterior advection, and eventual deposition of coarser of bottom trawling. and older sediment from adjacent trawling grounds. In con- trast, the trawled site was eroded and presented compacted century-old sediment highly depleted in OM components, Published by Copernicus Publications on behalf of the European Geosciences Union. 4308 S. Paradis et al.: Organic matter contents and degradation in a highly trawled area during fresh particle inputs 1 Introduction anthropogenic sedimentary depocenters (Puig et al., 2015; Paradis et al., 2017, 2018). Contrary to the observed increases in total organic carbon Bottom trawling is among the most extensive forms on muddy continental shelf trawling grounds (Palanques et of anthropogenic activities affecting marine ecosystems al., 2014; Polymenakou et al., 2005; Pusceddu et al., 2005a), (Amoroso et al., 2018; Eigaard et al., 2017), and it is one the continuous removal of sediment by trawlers on continen- of the most harmful in terms of fish stock overexploitation tal slopes has significantly impoverished bulk organic carbon (Pauly et al., 2002), destruction of habitats (Kaiser et al., as well as its labile and fresh pools (Martín et al., 2014b; 2002; Simpson and Watling, 2006), and the physical impact Pusceddu et al., 2014; Sañé et al., 2013). The loss of or- it exerts on the sediments (Martín et al., 2014a; Oberle et al., ganic matter has also reduced organic carbon turnover rates 2018; Puig et al., 2012). Since bottom trawling targets ben- on slope trawling grounds, severely impacting the meiofauna thic and demersal fisheries, its gear is designed to be in con- and, at the same time, promoting the abundance of taxa with tinuous contact with the seafloor, scraping the bottom, resus- opportunistic life strategies (Pusceddu et al., 2014). How- pending large volumes of sediment (O’Neill and Ivanović, ever, the combined effect of bottom trawling erosion along 2016; Palanques et al., 2014), and causing significant ero- with the alteration of sedimentary organic matter, which usu- sion (Martín et al., 2014b; Oberle et al., 2016). The resus- ally represents the fundamental energy source for commer- pension of sediment releases nutrients and organic matter cial deep-sea benthic species, is not fully understood. (OM) to the overlying water column, and degradation of OM The Gulf of Castellammare holds one of the most impor- can be accelerated through enhanced microbial activity (Dur- tant bottom trawling grounds in the northern Sicilian shore rieu de Madron et al., 2005; Pusceddu et al., 2005b, 2015). (southwestern Mediterranean Sea). Bottom trawlers in this The effects that these perturbations generate on sedimentary gulf operate using otter trawl gear, a trawling technique OM can vary in cohesive (i.e., muddy sediment with high which consists of dragging a wide net that is held open and clay content) and non-cohesive (i.e., sandy seafloor) sedi- in contact with the seafloor by two otter doors (Martín et al., ment. For instance, trawling on cohesive sediments can in- 2014a). The first data of bottom trawlers in the area go back crease superficial concentrations of sedimentary OM (Palan- to the 1960s, but this fishing technique has became more ques et al., 2014; Pusceddu et al., 2005a; Sciberras et al., active since the 1980s (European Commission Fisheries & 2016; Polymenakou et al., 2005), whereas trawling on coarse Maritime Affairs, 2014), as a result of the modernization of non-cohesive sediments can exert null or minimal effects on the Sicilian trawling fleet (L.R. 1/1980, 1980; L.R. 26/1987, OM contents and benthic community metabolism (Hale et 1987). Fishing stocks within this gulf were declining alarm- al., 2017; Tiano et al., 2019; Trimmer et al., 2005). ingly until the Sicilian government established a trawling ban Most of these impacts have been documented in shallow area in the inner shelf in 1990 (L.R. 25/1990, 1990), delim- environments, where sediment and OM fluxes are generally ited by the junction between Capo Rama and Torre dell’Uzzo high and sediment resuspension and OM remineralization in- (Fig. 1). Since the establishment of this closure, both dem- duced by bottom trawling can be comparable to those in- ersal biomass and catch per unit effort (CPUE) of artisanal duced by natural high-energy events such as storms (Bus- fisheries (non-towed bottom gear and pelagic gear) have in- cail et al., 1990; Dellapenna et al., 2006; Ferré et al., 2008; creased in that area (Pipitone et al., 2000; Whitmarsh et al., Pusceddu et al., 2005b). Since these natural physical distur- 2002). However, bottom trawlers have been concentrating bances are persistent, shallow benthic communities generally their efforts beyond the restricted area in the mid-continental present higher resilience to the impacts of bottom trawling slope (> 500 m depth), leading to a decrease in CPUE since than communities that live in less disturbed areas, such as the trawl ban as a result of the continuous overexploitation the deep sea (Kaiser, 1998). of fishing stocks (Arculeo et al., 2014; Whitmarsh, 2002). A However, bottom trawling has been progressively expand- more recent management strategy aimed to prevent the col- ing to deeper environments (> 200 m depth) since the 1950s lapse of Sicilian fisheries established a 30 d bottom trawling (Morato et al., 2006; Roberts, 2002), driven by technological closure per year, which can occur from 1 August to 31 Octo- advances in parallel with an ongoing depletion of shallow- ber (Decreto 1339/2001, 2001). water fisheries (Koslow et al., 2000; Martín et al., 2014a). Despite the numerous studies that address the effects of the At such depths, natural sediment fluxes to the seafloor and trawl ban in the Gulf of Castellammare (Fanelli et al., 2008; resuspension processes tend to be low. Hence, bottom trawl- Romano et al., 2016; Pipitone et al., 2000; Whitmarsh et al., ing has become a major mechanism of sediment resuspen- 2002), no studies have yet assessed the impacts of bottom sion on continental slopes, leading to eroded fishing grounds trawling on the gulf’s sedimentary environment. This study (Martín et al., 2014b, c; Puig et al., 2012). Resuspended par- aims to reveal whether erosion prevails in bottom trawling ticles can then be exported by ambient currents across- and grounds and what the consequent alterations on sedimentary along-margin as enhanced nepheloid layers (Arjona-Camas organic matter are, by comparing sediment cores collected et al., 2019; Wilson et al., 2015), or as sediment gravity flows at a trawled and untrawled site in the Gulf of Castellam- (Martín et al., 2014c; Puig et al., 2012) ultimately generating mare. The degree of erosion will be estimated based on sed- Biogeosciences, 16, 4307–4320, 2019 www.biogeosciences.net/16/4307/2019/ S. Paradis et al.: Organic matter contents and degradation in a highly trawled area during fresh particle inputs 4309 Figure 1. Bathymetric map of the Gulf of Castellammare. Location of the sediment cores sampled at the trawled (red circles) and untrawled (blue squares) sites. Unfilled sampling points indicate unsuccessful sediment core deployments. Seafloor images obtained from ROV dives are shown with triangles (see Fig. S1). The distribution of trawling grounds as trawling frequency (number of total hauls per grid area) in 2016 (1 January to 10 August) was calculated for a 200 m × 200 m grid. The limit of the trawl banned area between Torre dell’Uzzo and Cape Rama is indicated by a dashed line. The main trawling harbors (Castellammare del Golfo and Terrasini) and the most relevant ephemeral rivers (San Bartolomeo, Nocella, and Jato) are also annotated. The yellow arrow illustrates the direction of the regional surface current. imentological parameters and radioactive tracers with differ- narrow submarine canyons cut the slope, breaching the shelf ent half-lives (210 Pb, t1/2 = 22.3 years; 234 Th, t1/2 = 24.1 d), break at 120 to 140 m depth (Lo Iacono et al., 2014). Small whereas the alterations on sedimentary organic matter will seasonal torrents discharge into the gulf, namely the Nocella, be determined based on its quantity, composition, and nu- Jato, and San Bartolomeo rivers, with annual average dis- tritional quality. The coupled analyses of radioactive tracers charges between 0.24 and 0.32 m3 s−1 (Regione Siciliana, and biomarkers will also provide insights into the effects of 2007). Storm-induced flash floods can cause short flushing the arrival of fresh sediment on impacted trawling grounds. events of up to 1.2 m3 s−1 that transport significant amounts of nutrients into the sea (Calvo and Genchi, 1989). 2 Methods 2.2 Sediment core sampling 2.1 Study area In the framework of the FP7 EU-Eurofleets 2 ISLAND (Ex- plorIng SiciLian CAnyoN Dynamics) cruise on board the The Gulf of Castellammare is one of the widest bays of the R/V Angeles Alvariño, sediment cores were collected in northern coast of Sicily, with over 70 km of coastline, en- August 2016 from trawled and untrawled sites in the Gulf closed by Cape Rama to the east and Cape San Vito to the of Castellammare. Sampling locations were selected based west (Fig. 1). A cyclonic along-slope current dominates the on the distribution of operating trawlers using data from gulf’s circulation at an average speed of 0.1–0.2 m s−1 on the a vessel monitoring system (VMS) (see Sect. 2.8). Sam- upper continental shelf, which can sometimes reach maxi- pling took place prior to the temporal fishing closure in the mum speeds of 0.4 m s−1 (Sarà et al., 2006). The seafloor Gulf of Castellammare, which took place that year between morphology consists of a subhorizontal gently sloping conti- 17 September and 16 October. This ensured that sediment nental shelf that extends approximately 5 km offshore. The cores reflect the alterations caused by bottom trawling per- continental slope is around 11◦ steep down to 500 m wa- sisting in this deep environment. ter depth, and it then gradually decreases to around 1.5◦ at A total of five multicore deployments were conducted us- 1300 m water depth (Lo Iacono et al., 2014). Several small, ing a K/C Denmark A/X six-tube multicorer (inner diame- www.biogeosciences.net/16/4307/2019/ Biogeosciences, 16, 4307–4320, 2019 4310 S. Paradis et al.: Organic matter contents and degradation in a highly trawled area during fresh particle inputs ter 9.4 cm) at trawled and untrawled sites along the 550 m trawled core and from 27 to 49 cm for the untrawled core, contour line. However, only one trawled and one untrawled assuming complete decay of excess 210 Pb at these depths. site could be sampled (Fig. 1), possibly due to high sediment Supported 210 Pb concentrations were corroborated by mea- compaction at the trawled sites, as experienced by Martín et suring 226 Ra concentrations through its decay product 214 Pb al. (2014b), and/or due to the swell during the coring oper- (295 and 352 keV) in several samples along each core using ation that could hamper a successful triggering of the multi- gamma spectroscopy, using calibrated geometries in a well- corer. type high-purity germanium detector (CANBERRA, model Triplicate sediment cores were retrieved at each site from GCW3523). three independent multicore deployments to account for spa- Concentrations of 234 Th were also measured with gamma tial variability of organic matter analyses. The sediment cores spectroscopy through the 63 keV emission line. Given its were sliced on deck (0–1, 1–3, 3–5, 5–7, and 7–9 cm) and short half-life (24.1 d), samples were measured within two stored in calcinated aluminum foil at −20 ◦ C until analysis of half-lives (∼ 6 weeks) since sampling, which only allowed organic matter content. At each site, a single sediment core the measurement of the upper 5 cm of the trawled and un- from one of the three deployments was reserved for sedimen- trawled cores. Samples were remeasured at least 6 months tary, radiochemical, and elemental analyses. This sediment later, after excess 234 Th had decayed, to obtain supported core was sliced on deck at 1 cm intervals and kept in sealed 234 Th concentrations, equivalent to 238 U concentrations. Ex- plastic bags at −20 ◦ C until being freeze-dried in the labora- cess 234 Th was calculated by subtracting supported 234 Th tory for analyses. from total 234 Th, accounting for 234 Th decay and in-growth Prior to sediment recovery, the remotely operated vehi- from 238 U since sampling. cle (ROV) Seaeye Falcon, from the University of Plymouth Concentrations of 137 Cs were also quantified using gamma (UK), collected visual evidence of trawling impact at the spectroscopy through the emission line at 662 keV. Gamma trawled sampling site and of no impact at the control site measurements of the untrawled sediment core were extended to corroborate the sampling strategy (Fig. S1 in the Supple- in depth to 20 cm, whereas in the trawled core measurements ment). were limited to the upper 5 cm since no 137 Cs was detected in that core. 2.3 Sedimentary characteristics 2.5 Elemental analyses Dry bulk densities of sediment cores were calculated by di- viding the net dry weight corrected for salt content by the Analyses of total carbon, organic carbon (OC), and total ni- sample volume. Grain size fractions of sand (> 63 µm), silt trogen (TN) were carried out with an elemental analyzer (4–63 µm), and clay (< 4 µm) were obtained using a Horiba (Costech ECS analyzer 4010), according to the procedure Partica LA-950V2 particle-size analyzer, with an accuracy described in Nieuwenhuize et al. (1994). Samples for OC of 0.6 % and a precision of 0.1 %. Prior to analysis, 1–4 g of analysis were first decarbonated by acid-fuming the samples sample was oxidized using 20 % H2 O2 and sediment parti- in the presence of 12 N HCl for 24 h and repeatedly adding cles were disaggregated with P2 O−7. 100 µL of 2 N HCl to the sample until effervescence ceased. Inorganic carbon (IC), quantified as the difference between 2.4 Radiochemical analyses total carbon and organic carbon, was converted to calcium carbonate (CaCO3 ) concentrations using the molecular mass Concentrations of 210 Pb were determined through the analy- ratio of CaCO3 : IC (100 / 12), assuming all inorganic carbon sis of its decay product 210 Po by alpha spectrometry follow- present is in the form of CaCO3 . To account for analytical ing the method described by Sanchez-Cabeza et al. (1998), error, replicate analyses were performed for samples every assuming secular equilibrium of both radionuclides at the 5 cm throughout the cores. An average percentage error of time of analysis. Between 150 and 300 mg of homoge- 1.2 % was obtained for carbon whereas nitrogen presented a nized ground sample was spiked with 209 Po as a chemi- slightly higher average percentage error of 1.9 %. cal yield and microwave-digested using concentrated HNO3 , HF, and HBO3 . The resulting solutions were evaporated and 2.6 Biochemical composition of sedimentary organic reconditioned with 1 M HCl. Polonium isotopes were spon- matter taneously deposited onto silver disks while stirring at 70 ◦ C for at least 8 h. Alpha emissions of 209 Po (4883 keV) and Total proteins, carbohydrates, and lipids were quantified 210 Po (5304 keV) were quantified using passivated implanted spectrophotometrically (Varian Cary® 50 UV-Vis) accord- planar silicon (PIPS) detectors (CANBERRA, model PD- ing to the methods described in Hartree (1972) and modified 450.18 A.M.) and the Genie™ data acquisition software. by Rice (1982), Gerchakov and Hatcher (1972), Bligh and Supported concentrations of 210 Pb in the sediment cores Dryer (1959), and Marsh and Weinstein (1966). The analy- were obtained by averaging constant concentrations of total ses of proteins and lipids were carried out on 0.1–0.6 g of 210 Pb from the bottom of the core, from 2 to 37 cm for the frozen sediment, whereas carbohydrate analyses were per- Biogeosciences, 16, 4307–4320, 2019 www.biogeosciences.net/16/4307/2019/ S. Paradis et al.: Organic matter contents and degradation in a highly trawled area during fresh particle inputs 4311 formed on previously dried sediment. Protein, carbohydrate was represented as the number of times trawled per grid and lipid contents were transformed into carbon equivalents cell (200 m × 200 m) during each year. The native VMS data using 0.49, 0.4, and 0.75 mgC mg−1 as conversion factors, were processed using the R package VMSbase (Russo et al., respectively, and their sum reported as biopolymeric C (Fabi- 2014). The size of the grid was defined considering the er- ano et al., 1995). Chlorophyll a and phaeopigments, after ror associated with the reconstruction of the trawling hauls extraction with 90 % acetone, were quantified fluorometri- as described by Russo et al. (2011). cally (Shimadzu RF-6000) according to Lorenzen and Jef- frey (1980) and modified by Danovaro (2010) for sediments. 2.9 Statistical analyses Total phytopigment concentrations were defined as the sum of chlorophyll a and phaeopigment concentrations and con- Statistical analyses were used to test whether OM quan- verted into carbon equivalents using a conversion factor of tity and biochemical composition (protein, carbohydrate, 40 (Pusceddu et al., 2010). lipid, and phytopigment concentrations), freshness (the phytopigment-to-biopolymeric C ratio), and degradation 2.7 Sedimentary OM freshness and degradation rates rates (sedimentary protein turnover rates) were statistically different between trawled and untrawled sites in the upper The contribution of phytopigment to biopolymeric C was 9 cm of sediment cores. The analysis consisted of two or- used as a proxy to estimate OM freshness: since in the deep thogonal factors: site (trawled vs. untrawled) and depth in sea there is no in situ primary production, higher values of the sediment (five levels: 0–1, 1–3, 3–5, 5–7, 7–9 cm). Per- this ratio are associated with recently deposited material of mutational analyses of variance (PERMANOVA), in either algal origin (Pusceddu et al., 2010). the univariate (variable by variable) or multivariate contexts, Since N is the most limiting factor for heterotrophic nu- were based on Euclidean distances of previously normalized trition and proteins are N-rich products, sedimentary OM data using 999 permutations of residuals with unrestricted degradation was estimated using the degradation rate of pro- permutation of raw data (univariate tests) or under a reduced teins, obtained from the analysis of extracellular aminopepti- model (multivariate tests) (Anderson, 2001). Since for al- dase activities. Aminopeptidase activity was estimated fluo- most all tests the interaction between factors was significant, rometrically after incubation of approximately 0.1 g of sedi- we conducted post hoc permutational pairwise comparison ment with 100 µM L-leucine-4-methylcumarinyl-7-amide for tests between trawled and untrawled sites for each sediment 1 h in the dark. This substrate, when exposed to extracellular layer and among sediment layers for trawled and untrawled aminopeptidase, produces fluorescence with an intensity pro- sites, separately. Given the restricted number of unique per- portional to the enzyme activity. Fluorometric analyses were mutations, p values were obtained from Monte Carlo sim- carried out before and after incubation, and the difference ulations (Anderson and Robinson, 2003). Bi-plots produced was used to calculate protease activities (Danovaro, 2010). after canonical analysis of principal components (CAP) were The results were converted to carbon equivalents using the used to visualize the differences between trawled and un- conversion factor of 72 ngC nmol protease−1 (Fabiano and trawled samples in terms of organic matter biochemical com- Danovaro, 1998). Turnover rates were then calculated by di- position (Anderson and Willis, 2003). All statistical analyses viding protein-C degradation rates by protein-C sedimentary were performed using the routines included in the PRIMER contents. 6+ software. 2.8 Trawling effort from VMS data 3 Results Fishing intensity of the Italian bottom trawling fleet was ob- Bottom trawling in the Gulf of Castellammare is limited to tained using data provided by the vessel monitoring system the mid-slope (> 500 m), beyond the trawling-ban area. In (VMS), the main tracking device used for monitoring fish- the main bottom trawling ground, where the trawled core was ing activities. According to the Common Fisheries Policy of retrieved, hauls generally follow the contour lines in a W– the European Union (European Commission, 2003), fishing E direction (Fig. 1). Fishing effort has generally increased vessels with overall length equal to or larger than 15 m must since 2007, with a predominating trawling frequency of 1 to be equipped with a VMS transmitter, called “Blue Box”. It 40 hauls per grid cell during that year, which then increased estimates the position of the vessel using the Global Posi- to around 60 to 100 hauls per grid cell since 2013 (Fig. S2). A tioning System and sends this information, along with the smaller trawling ground has opened since 2012 towards the speed and heading of the vessel, to the network of the coastal eastern side of the gulf, close to Cape Rama (Figs. 1, S2). Al- guard by Inmarsat C to the Fishing Monitoring Centre in less though trawling frequency for 2016 was only computed from than 10 min at 2 h time intervals. Fishing intensity was cal- January to August, this year presented the highest fishing ef- culated using yearly VMS data from 2007 to 2015, whereas fort in comparison to the previous years. for 2016, only VMS data from 1 January to 10 August were taken into account, prior to sampling. Trawling frequency www.biogeosciences.net/16/4307/2019/ Biogeosciences, 16, 4307–4320, 2019 4312 S. Paradis et al.: Organic matter contents and degradation in a highly trawled area during fresh particle inputs Table 1. Summary of the main parameters of the trawled and untrawled cores. Data for grain size, CaCO3 , OC, TN, and OC/TN correspond to average values ±1 standard deviation of that layer. MAR: mass accumulation rate; SAR: sediment accumulation rate. Core Layer Excess 234 Th Excess 210 Pb Sedimentation rates Grain size (%) CaCO3 OC TN OC/TN (cm) inventory inventory (%) (%) (%) MAR SAR Sand Silt Clay (Bq m−2 ) (Bq m−2 ) (g cm−2 yr−1 ) (cm yr−1 ) (> 63 µm) (4–63 µm) (< 4 µm) Untrawled 0–6 > 1080 ± 70 7310 ± 160 Surface mixed layer <1 77 ± 8 22 ± 8 18.4 ± 0.3 0.96 ± 0.02 0.133±0.002 7.2 ± 0.2 6–25 – 10 480 ± 490 0.090±0.003 0.151±0.005 1.5 ± 0.4 44 ± 5 54 ± 4 17 ± 2 0.93 ± 0.03 0.132±0.004 7.1 ± 0.2 25–50 – – ∗ 3±2 42 ± 2 55 ± 2 20 ± 2 0.79 ± 0.06 0.110±0.010 7.2 ± 0.4 Trawled 0–2 1000 ± 50 340 ± 30 Fresh sediment <1 52 ± 8 48 ± 8 27.1 ± 0.5 0.79 ± 0.02 0.101±0.002 7.8 ± 0.4 2–37 – – ∗ 1.4 ± 1.5 41.4 ± 1.1 57.3 ± 1.3 26.1 ± 1.3 0.73 ± 0.03 0.103±0.007 7.1 ± 0.4 ∗ Section depleted of excess 210 Pb, corresponding to sediment deposited before ∼ 1900. 3.1 Physical characteristics and then slightly increased with depth until ∼ 20 % at 30 cm (Fig. 4d). In the sediment core collected from the trawled site, both The untrawled sediment core presented an excess 210 Pb excess 210 Pb and excess 234 Th were only present in the up- concentration profile that extended to 25 cm in depth, with per 2 cm, with inventories of 340±30 and 1000±50 Bq m−2 , a total inventory of 17 900 ± 900 Bq m−2 (Fig. 2a; Ta- respectively (Table 1, Fig. 3a, b). 137 Cs was not detected in ble 1). In the upper 6 cm, excess 210 Pb concentrations the upper 5 cm analyzed. Dry bulk density rapidly increased slightly decreased towards the surface from 372±22 Bq kg−1 from 0.4 to 0.7 g cm−3 in the upper 3 cm and kept increas- to 272 ± 15 Bq kg−1 (Fig. 2a). Below, excess 210 Pb con- ing to ∼ 0.8 g cm−3 at 13 cm, from where it remained rela- centrations presented a continuous decrease between 6 tively constant with depth (Fig. 3c). Despite the slight coars- and 25 cm, from which an average sediment accumulation ening of grain size in the upper 2 cm, this core presented con- rate of 0.090 ± 0.003 g cm−2 yr−1 , equivalent to 0.151 ± stant grain size along the upper 37 cm, consisting of higher 0.005 cm yr−1 (R 2 = 0.995) (Table 1), was calculated ap- clay (57 %) and lower silt (41 %) fractions (Fig. 3c, Table 1), plying the Constant Flux : Constant Sedimentation model similar to grain sizes below 6 cm of the untrawled site. Con- (CF : CS; Krishnaswamy et al., 1971). This sedimentation centrations of CaCO3 averaged at 26.9 ± 0.7 % in the upper rate was independently validated by 137 Cs. Detectable con- 10 cm, whereas the deeper layers had lower concentrations centrations of 137 Cs appeared at 17 cm depth, which was of ∼ 24 % (Fig. 3d). ascribed to the first detonations of thermonuclear weapons in the early 1950s. Above, 137 Cs concentrations depicted a 3.2 Sedimentary organic matter broad concentration maximum at 8–13 cm, centered at 10– 11 cm. This maximum was attributed to the combined accu- Trawled and untrawled sediment cores presented different mulation of the maximum fallout prior to the cessation of OC and TN concentration profiles (Fig. 4). The untrawled nuclear atmospheric testing in 1963 as well as the deposi- core had OC concentrations of ∼ 0.9 % in the upper 20 cm, tion of 137 Cs emitted from the Chernobyl accident in 1986 which then decreased to ∼ 0.8 % at 35 cm. In contrast, the (Fig. 2a). The deposition of 137 Cs from each of these events trawled core presented OC concentrations that fluctuated be- could not be distinguished due to the low sedimentation rate tween ∼ 0.8 % and ∼ 0.7 % with depth. Similarly, concentra- and the sampling resolution of this core. Concentrations of tions of TN in the untrawled core were ∼ 0.13 % in the upper excess 234 Th ranged between 71 and 97 Bq kg−1 between 2 20 cm, which then decreased to ∼ 0.10 % at 35 cm, whereas and 5 cm, decreased to 37±7 Bq kg−1 at 1–2 cm and was not the trawled core presented TN concentrations varying be- detected on surface sediments (0–1 cm) of the core (Fig. 2b). tween ∼ 0.11 % and ∼ 0.09 % with depth. For both OC and The penetration depth of excess 234 Th could be greater than TN, concentrations in the upper 20 cm were ∼ 20 % lower at the upper 5 cm analyzed, leading to an inventory of at least the trawled site in comparison to the untrawled site, reaching 1080 Bq m−2 (Table 1). Dry bulk density of the untrawled similar concentrations at 30 cm in depth (Fig. 4). Profiles of site remained constant in the upper 7 cm at ∼ 0.5 g cm−3 , the OC/TN ratio presented similar values at both sites, vary- gradually increased to ∼ 0.7 g cm−3 at 15 cm, and then re- ing between 6.5 and 7.5 throughout the core (Fig. 4c). mained relatively constant with depth (Fig. 2c). The upper In general, organic matter quantity was higher at the un- 6 cm presented coarser grain size consisting of higher silt trawled site than at the trawled site, with the exception of (77 %) and lower clay (22 %) fractions, in comparison to the surface layers, which presented similar concentrations at rest of the core, which had lower silt (44 %) and higher clay both sites (Fig. 5). Protein concentrations at the untrawled (54 %) fractions (Fig. 2c, Table 1). CaCO3 concentrations site were 1.5 mgC g−1 in the upper 3 cm, increased to max- were constant in the upper 10 cm, with an average concen- imum concentrations of ∼ 3 mgC g−1 at 3–7 cm, and de- tration of 18.4 ± 0.4 %, decreased to ∼ 15 % at 15–20 cm, creased to 2.4 mgC g−1 at 7–9 cm. The trawled site had sim- Biogeosciences, 16, 4307–4320, 2019 www.biogeosciences.net/16/4307/2019/ S. Paradis et al.: Organic matter contents and degradation in a highly trawled area during fresh particle inputs 4313 Figure 2. Sedimentological and geochemical characteristics of the untrawled sediment core. (a) Concentration profiles of excess 210 Pb (circles), indicating the average sedimentation rate below the upper 6 cm, and 137 Cs (triangles). (b) Concentration profile of excess 234 Th in the upper 5 cm. (c) Dry bulk density and grain size. (d) CaCO3 concentration profile. The analytical error is given in horizontal error bars. Vertical scales indicate the process that has occurred in the depth range given. SML: surface mixed layer; SR: sedimentation rate. Figure 3. Sedimentological and geochemical characteristics of the trawled sediment core. (a) Concentration profiles of excess 210 Pb. (b) Con- centration profile of excess 234 Th in the upper 5 cm. (c) Dry bulk density and grain size profile. (d) CaCO3 concentration profile. The ana- lytical error is given in horizontal error bars. Vertical scales indicate the process that has occurred in the depth range given. SML: Surface Mixed Layer; SR: Sedimentation Rate. ilar ∼ 1.5 mgC g−1 protein concentrations in surface sed- were constant (2.5 ± 0.1 mgC g−1 ) along the upper 9 cm of iment that increased to almost 2.5 mgC g−1 in the deep- the trawled core, whereas concentrations increased in the un- est layer analyzed (Fig. 5a). Carbohydrate concentrations trawled core from 2.9 ± 0.2 mgC g−1 in the topmost layer to at the untrawled site presented decreasing concentrations ∼ 4 mgC g−1 in the 3–7 cm layer, before returning to sim- from between 0.7 and 0.9 mgC g−1 in the upper 3 cm to ilar values observed in the surface layer (Fig. 5d). At both 0.44 mgC g−1 in the deepest layer, whereas the trawled site sites, phytopigment profiles showed decreasing trends, with had constant concentrations of 0.42 mgC g−1 in the upper a sharper decrease at the trawled site from 126±7 µgC g−1 in 9 cm of the trawled site (Fig. 5b). Untrawled and trawled the top layer to relatively constant values of 39 ± 5 µgC g−1 sites had similar lipid concentrations of ∼ 0.6 mgC g−1 in below 3 cm, whereas the untrawled site showed a grad- the topmost sediment layer, decreasing to 0.34 ± 0.03 and ual decrease from 161 ± 18 µgC g−1 in the topmost layer to 0.17 ± 0.01 mgC g−1 at 7–9 cm of the untrawled and trawled 77 ± 12 µgC g−1 in the deepest one (Fig. 5e). cores, respectively (Fig. 5c). Biopolymeric C concentrations www.biogeosciences.net/16/4307/2019/ Biogeosciences, 16, 4307–4320, 2019 4314 S. Paradis et al.: Organic matter contents and degradation in a highly trawled area during fresh particle inputs Figure 4. Profiles from elemental analyses of untrawled (blue) and trawled (red) cores. Organic carbon (a), total nitrogen (b), and the OC/TN ratio (c). The analytical error is represented by error bars. Vertical scales indicate the process that has occurred in the depth range given for both untrawled (blue) and trawled (red) sediment cores. SML: surface mixed layer; SR: sedimentation rate. Figure 5. Organic matter quantity of untrawled (blue) and trawled (red) sites. Proteins (a), carbohydrates (b), lipids (c), biopolymeric carbon (d), and phytopigments (e). Bar graphs and error bars illustrate the mean values and standard errors at each site and depth of the triplicate sediment cores collected. Asterisks next to bars denote significant difference of post hoc permutational pairwise tests between trawled and untrawled sites: ∗ p < 0.05; ∗∗ p < 0.01; ∗∗∗ p < 0.001; n.s. denotes not significant. Vertical scales indicate the process that has occurred in the depth range given for both untrawled (blue) and trawled (red) sediment cores. SML: surface mixed layer; SR: sedimentation rate. Statistical analyses of the data indicated that both sampling 3.3 Organic matter biochemical composition, site and core depth had significant effects on the quantity of freshness, and turnover rates sedimentary OM (Table S1). The post hoc comparison tests (Table S2) demonstrated that OM contents between trawled Variations in the biochemical composition of sedimentary and untrawled sites were generally statistically different only OM in terms of protein, carbohydrate, lipid, and phytopig- below the topmost sediment layer (0–1 cm), with the excep- ment contents were assessed through PERMANOVA testing tion of carbohydrates. (Table S3). The results revealed that the biochemical compo- sition of sedimentary OM not only differed between trawled and untrawled sites, but that these differences varied depend- ing on the depth in the core. The consequent post hoc pair- wise tests between the trawled and untrawled sites at all sed- Biogeosciences, 16, 4307–4320, 2019 www.biogeosciences.net/16/4307/2019/ S. Paradis et al.: Organic matter contents and degradation in a highly trawled area during fresh particle inputs 4315 superficial sediments of trawled and untrawled sites, with relatively high values (∼ 5 %) that decreased with depth at both sites, although more pronouncedly at the trawled site, reaching ∼ 1.4 % at 5–7 cm, than at the untrawled site, reach- ing 2.5 % at 7–9 cm (Fig. 7a). Turnover rates were signifi- cantly higher in the upper 3 cm of the trawled site (0.017– 0.025 d−1 ) in comparison to ∼ 0.015 d−1 of the superficial sediment of the untrawled site (Table S5b, Fig. 7b). Below, turnover rates decreased to ∼ 0.005 d−1 for both sites. Figure 6. Variations in the biochemical composition of the sedi- 4 Discussion mentary organic matter. Bi-plot after canonical analysis of the prin- cipal coordinates. Note that symbols represent the same core depth 4.1 Long-term impacts of intense bottom trawling for both trawled (red) and untrawled (blue) sites and that increasing depth is also illustrated by a fading filling. Evidence of the long-term impacts of intense bottom trawl- ing are clear at a trawled site of the Gulf of Castellammare. ROV images from the trawled area present a barren seafloor, with several deep linear furrows hundreds of meters long and up to 70 cm deep, presumably caused by the trawling gear’s heavy otter doors (Fig. S1a). The shallow penetration depth of excess 210 Pb in the trawled core suggests that only the up- per 2 cm of sediment had been recently deposited on top of highly compacted sediments (0.7–0.8 g cm−3 ) that had accu- mulated more than 100 years ago, considering the absence of excess 210 Pb (Fig. 3a, c). These sedimentological patterns are characteristic of a seafloor eroded by trawling activities, Figure 7. Organic matter freshness and degradation rates of trawled as observed in other trawled regions with shallow horizons (red) and untrawled (blue) cores. Relative contribution of phytopig- of excess 210 Pb and exposed over-consolidated, century-old ments to biopolymeric C (a) and protein turnover rates (b). Bar sediments (Martín et al., 2014b; Oberle et al., 2016; Paradis graphs and error bars illustrate the mean values and standard er- rors at each site and depth of the triplicate sediment cores col- et al., 2017, 2018). The uprooting of old sediment at this lected. Asterisks next to bars denote significance of post hoc permu- trawled site, with only a thin accumulation of recent sedi- tational pairwise tests between trawled and untrawled sites: ∗ p < ment in superficial layers, reveals that the rate of sediment 0.05; ∗∗ p < 0.01; ∗∗∗ p < 0.001; n.s. denotes not significant. Verti- erosion induced by the high trawling frequency is greater cal scales indicate the process that has occurred in the depth range than sediment accumulation rates in the Gulf of Castellam- given for both untrawled (blue) and trawled (red) sediment cores. mare. Furthermore, the coincident penetration depth of both SML: surface mixed layer; SR: sedimentation rate. excess 210 Pb and excess 234 Th at the trawled site (Fig. 3a, b) indicates that the accumulation of fresh sediment would have occurred after the passage of the last trawler over the iment layers indicated that the biochemical composition of sampling area and thus reveals that trawling frequency con- sedimentary OM, similar to the OM content, varied signifi- trols the residence time of fresh sediment in these trawling cantly between trawled and untrawled sites at all depths, ex- grounds. cluding surface sediments (Table S4). The bi-plot produced In contrast, excess 210 Pb inventories were 2 orders of after the canonical analysis of principal components (Fig. 6) magnitude higher in the untrawled core. This core had a revealed that the vertical variations in the biochemical com- sedimentation rate of 0.151 ± 0.005 cm yr−1 , comparable to position of sedimentary OM in the untrawled sediment core those quantified at similar depths in the Mediterranean Sea are greater than those observed at the trawled site, as ob- (DeGeest et al., 2008; Miralles et al., 2005; Sanchez-Cabeza served from the greater spatial distribution of these samples. et al., 1999). The upper 6 cm of this core had excess 210 Pb However, the proximity of superficial samples of trawled concentrations that slightly decreased towards the surface, a cores to most of the untrawled samples in the bi-plot illus- deep penetration depth of excess 234 Th, and low dry bulk trates a resemblance in their biochemical composition. densities (Fig. 2a, b), altogether signs of biological mixing The contributions of phytopigment to biopolymeric C and (Arias-Ortiz, et al., 2018; Pope et al., 1996; van Weering et the protein turnover rates at trawled and untrawled sites are al., 1998). The influence of bioturbation at this site is corrob- given in Table S5 and illustrated in Fig. 7. The relative con- orated by the presence of several burrows directly observed tribution of phytopigments to biopolymeric C was similar in during ROV dives prior to sampling (Fig. S1b). Sediment www.biogeosciences.net/16/4307/2019/ Biogeosciences, 16, 4307–4320, 2019 4316 S. Paradis et al.: Organic matter contents and degradation in a highly trawled area during fresh particle inputs mixing caused by bioturbation could explain the broad 137 Cs different organic matter composition and significantly lower concentration maximum observed at 8–13 cm, attributed to nutritional quality in comparison to its untrawled counterpart the combined accumulation of 137 Cs from the 1986 Cher- (Figs. 6, 7a). This suggests that, aside from the ephemeral nobyl accident and from the 1963 global fallout, as well as deposition of fresh OM that will be swiftly eroded by bot- diluting the 1954 signal with depth (Fig. 2a). However, bio- tom trawlers’ gear, deep-sea trawling grounds are gener- turbation alone cannot account for the coarsening of sedi- ally characterized by nutritionally poor organic matter con- ment observed in the upper 6 cm (Fig. 2c; Table 1). Provided tents (Pusceddu et al., 2014; Sañé et al., 2013), which in- the high capacity of bottom trawling gear to resuspend sed- creases the dependence on the supply of fresh OM in or- iments (Martin et al., 2014a, c; Oberle et al., 2018; Puig et der to sustain benthic communities. This hypothesis is cor- al., 2012), the siltation of superficial sediments on the un- roborated by the higher OM turnover rates in surface sedi- trawled site could be explained by the preferential deposi- ment of the trawled site in comparison to the untrawled site tion of siltier particles resuspended from an adjacent trawl- (Fig. 7b), which reveal a prompt stimulation of microbial ac- ing ground located ∼ 1 km up-current from this sampled site tivities resulting from the recent accumulation of fresh and (Fig. 1). Finer clay particles resuspended by bottom trawlers nutritionally enriched OM on the trawled site. In fact, ben- can be advected to farther distances along the margin (Lin- thic communities in areas that have severe nutrient limita- ders et al., 2017). This siltier sediment would have been pos- tions, such as in eroded sediment of this trawled site or in teriorly redistributed and preserved within the surface mixed oligotrophic deep-sea regions, react instantaneously to food layer of the untrawled site (Fig. 1). pulses (Bett et al., 2001; Fabiano et al., 2001; Witte et al., Excluding the fresh superficial layers of the trawled site, 2003). In contrast, the untrawled site is characterized by rel- the chronic erosion induced by bottom trawling resuspension atively higher total organic matter contents as well as fresh considerably depleted the trawled site of both OC and TN by and bioavailable compounds throughout the core, possibly ∼ 20 % in comparison to the untrawled site (Fig. 4; Table 1). due to a deeper penetration of labile material through bi- Concentrations of OC and TN were similar in the deeper ological mixing (Fig. 5). However, these sections also pre- layers of both sites, where sediments would have accumu- sented slowly decreasing concentrations of phytopigment to lated more than a century ago, revealing that bottom trawl- biopolymeric C with depth as well as lower protein turnover ing re-exposes old sediment impoverished in OM (Fig. 4; Ta- rates, revealing that this unstressed environment has a lower ble 1). Similarly, the trawled site had lower proteins (−5 % to consumption of labile OM and a relatively reduced depen- −38 %), carbohydrates (−13 % to −58 %), lipids (−36 % to dence on the arrival of fresh OM (Fig. 7a). −52 %), biopolymeric carbon (−12 % to −37 %), and phy- The higher OM turnover rates observed in the freshly topigments (−53 % to −67 %) than the untrawled site, with deposited surface layers of the trawled site also indicate a the exception of superficial layers (Fig. 5). These results are greater efficiency of OM consumption and remineralization in accordance with previous studies that showed compara- in the trawling ground in comparison to the untrawled site. ble losses of organic matter in slope trawling grounds, rein- This enhanced mineralization through self-priming can oc- forcing the concept that chronic and intensive bottom trawl- cur when fresh and degradable organic matter, such as fresh ing depletes these deep-sea sedimentary habitats of organic phytoplankton, arrives to areas with more refractory com- matter, promoting their degradation over time (Martín et al., pounds (Canfield, 1994; van Nugteren et al., 2009), as was 2014b; Pusceddu et al., 2014; Sañé et al., 2013). observed in a shallow trawling-disturbed area in the south- ern North Sea, off the Belgian coast (van de Velde et al., 4.2 Effects of the arrival of fresh sediment 2018). Similarly, bottom trawling in the shallow Thermaikos Gulf (Aegean Sea) intensified microbial activities, which en- During the ISLAND cruise, ROV dives showed high settling hanced nutrient cycling and organic carbon mineralization fluxes of large particulate matter aggregates to the seafloor (Polymenakou et al., 2005; Pusceddu et al., 2005a). This (Fig. S1). At both sampled sites, evidence of recent accu- could have been attributed to the combined effect of trawling- mulation of surface sediments was provided by the presence induced mixing of superficial labile OM with more degraded of excess 234 Th and high concentrations of phytopigments subsurface OM, along with the continuous arrival of fresh (Fig. 5e), a compound that usually represents the most im- OM to these shallow continental shelves (Buscail et al., 1990; portant food source for deep-sea heterotrophic consumption Tselepides et al., 2000). (Pusceddu et al., 2010; Stephens et al., 1997). This indicates In contrast, surface sediments collected in a deeper that the Gulf of Castellammare was receiving highly nutri- and intensely trawled flank of La Fonera Canyon, in the tious organic matter inputs during the sampling period. In- NW Mediterranean margin, presented significantly lower deed, both the composition of sedimentary organic matter turnover rates than the nearby untrawled grounds (Pusceddu and the relative contribution of phytopigment to biopoly- et al., 2014). However, those sediment cores did not present meric C were similar in the fresh superficial sediments at signs of recently accumulated sediment as observed at our both trawled and untrawled sites. However, the subsurface, sampling sites, further proving the dependence on the arrival century-old sediments of the trawled site have distinctively of fresh and nutritionally rich sediment in intensely trawled Biogeosciences, 16, 4307–4320, 2019 www.biogeosciences.net/16/4307/2019/ S. Paradis et al.: Organic matter contents and degradation in a highly trawled area during fresh particle inputs 4317 grounds to support benthic organisms living in these im- Acknowledgements. The results presented in this study were ob- pacted deep-sea environments. tained within the Exploring SiciLian CAnyoN Dynamics (IS- The high nutritional quality and OM turnover rates in re- LAND) project and the Assessment of Bottom-trawling Impacts cently accumulated sediments from the trawled site suggest in DEep-sea Sediments (ABIDES) Spanish Research Project. We that high OM fluxes could help deep bottom trawling grounds would like to thank the crew of the R/V Ángeles Alvariño and the ISLAND cruise team that helped collect the samples. This work recover the nutritional characteristics of sedimentary OM. is contributing to the Institut de Ciència i Tencologia Ambientals These results confirm that actions aimed at mitigating the “Unit of Excellence”. Sarah Paradis is supported by a predoctoral impacts of bottom trawling include the implementation of FPU grant from the Spanish government. temporary fishing closures, allowing for a longer-lived de- position of fresh OM on the seafloor. However, such tem- porary trawling closures would most probably not allow the Financial support. This research has been supported by the full restoration of fresh sediment from trawl-induced erosion, European Commission, Seventh Framework Programme (EU- given the low sedimentation rates found in these deep envi- ROFLEETS2 (grant no. 312762)), the Ministerio de Economía ronments. Further management strategies would need to be y Competitividad (grant no. CTM2015-65142-R), the Generali- implemented to mitigate the impacts of bottom trawling ero- tat de Catalunya (2017 SGR-863 and 1588), the Australian Re- sion (Depestele et al., 2018), which would magnify the effect search Council (LIEF project (grant no. LE170100219)), the Minis- of temporary closures on the restoration of sedimentary OM terio de Economía y Competitividad (grant no. MDM2015-0552), in nutrient-deprived trawling grounds. and the Ministerio de Educación, Cultura y Deporte (grant no. FPU14/07039). 5 Conclusion Review statement. This paper was edited by Jack Middelburg Chronic and intense deep bottom trawling in the Gulf of and reviewed by Sebastiaan van de Velde and Xavier Dur- Castellammare erodes large volumes of sediment, exposing rieu de Madron. century-old, compacted sediment that is depleted in OM. This continuous erosion limits the accumulation of fresh sediment since any recently deposited particulate matter is promptly removed due to the high trawling frequency. Nev- References ertheless, we present evidence that the short-lived deposi- tion of recent and nutritionally rich organic matter leads to Amoroso, R. O., Pitcher, C. R., Rijnsdorp, A. D., McConnaughey, high turnover rates of labile OM. Our results emphasize that R. A., Parma, A. M., Suuronen, P., Eigaard, O. R., Bastardie, nutrient-deprived and eroded deep bottom trawling grounds F., Hintzen N. T., Althaus, F., Baird, S. J., Black, J., Buhl- Mortensen, L., Campbell, A. B., Catarino, R., Collie, J. S., are highly dependent on the arrival of fresh and nourishing Cowan, J. H., Durholtz, D., Engstrom, N., Fairweather, T. P., particulate organic matter to sustain benthic communities, Fock, H. O., Ford, R., Gálvez, P. A., Gerritsen, H. D., Gón- which can temporarily and partially abate the detrimental ef- gora, M. E., González, J., Hiddink, J. G., Hughes, K. M., In- fects of bottom trawling in superficial sediment. telmann, S. S., Jenkins, C., Jonsson, P., Kainge, P., Kangas, M., Kathena, J. N., Kavadas, S., Leslie, R. W., Lewis, S. G., Lundy, M., Makin, D., Martin, J., Mazor, T., Mirelis, G. G., Newman, S. Data availability. All data included in this study are available upon J., Papadopoulou, K. N., Posen, P. E., Rochester, W., Russo, T., request by contact with the corresponding author. Sala, A., Semmens, J. M., Silva, C., Tsolos, A., Vanelsander, B., Wakefield, C. B., Wood, B. A., Hilborn, R., Kaiser, M. J., and Jennings, S.: Bottom trawl-fishing footprints on the world’s con- Supplement. The supplement related to this article is available on- tinental shelves, P. Natl. Acad. Sci. USA, 115, E10275–E10282, line at: https://doi.org/10.5194/bg-16-4307-2019-supplement. https://doi.org/10.1073/pnas.1802379115, 2018. Anderson, M. J.: A new method for non-parametric mul- tivariate analysis of variance, Austral Ecol., 26, 32–46, Author contributions. SP, AP, PP, and CLI designed the scientific https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x, 2001. study. SP and CLI retrieved the samples. SP and DM performed Anderson, M. J. and Robinson, J.: Generalized discriminant anal- the analyses and TR processed the fishing effort data. SP wrote the ysis based on distances, Aust. N.Z. J. Stat., 45, 301–318, paper. All authors contributed to the interpretation and discussion https://doi.org/10.1111/1467-842X.00285, 2003. of the results, as well as the revision of the paper. Anderson, M. J. and Willis, T. J.: Canonical analysis of prin- cipal coordinates: A useful method of constrained ordination for ecology, Ecology, 84, 511–525, https://doi.org/10.1890/0012- 9658(2003)084[0511:CAOPCA]2.0.CO;2, 2003. Competing interests. The authors declare that they have no conflict Arculeo, M., Lo Brutto, S., Cannizzaro, L., and Vitale, S.: of interest. Growth and reproduction of the deep-water rose shrimp, Parapenaeus longirostris (Lucas, 1846) (Decapoda, Penaei- www.biogeosciences.net/16/4307/2019/ Biogeosciences, 16, 4307–4320, 2019 4318 S. Paradis et al.: Organic matter contents and degradation in a highly trawled area during fresh particle inputs dae), in the Southern Tyrrhenian Sea, Crust., 87, 1168–1184, Res., 25, 2387–2409, https://doi.org/10.1016/j.csr.2005.08.002, https://doi.org/10.1163/15685403-00003334, 2014. 2005. Arias-Ortiz, A., Masqué, P., Garcia-Orellana, J., Serrano, O., Eigaard, O. R., Bastardie, F., Niels, T., Hintzen, T., Buhl-Mortensen, Mazarrasa, I., Marbà, N., Lovelock, C. E., Lavery, P. S., and L., Buhl-Mortensen, M., Catarino, R., Dinesen, G. E., Egekvist, Duarte, C. M.: Reviews and syntheses: 210 Pb-derived sediment J., Fock, H., Geitner, K., Gerritsen, H., Marín González, M., Jon- and carbon accumulation rates in vegetated coastal ecosystems sson, P., Kavadas, S., Laffargue, P., Lundy, M., Mirelis, G. G., – setting the record straight, Biogeosciences, 15, 6791–6818, Rasmus Nielsen, J., Papadopoulou, N., Posen, P. E., Pulcinella, https://doi.org/10.5194/bg-15-6791-2018, 2018. J., Russo, T., Sala, A., Silva, C., Smith, C. J., Vanelslander, B., Arjona-Camas, M., Puig, P., Palanques, A., Emelianov, M., and and Rijnsdorp, A. D.: The footprint of bottom trawling in Euro- Durán, R.: Evidence of trawling-induced resuspension events pean waters: distribution, intensity, and seabed integrity, ICES J. in the generation of nepheloid layers in the Foix submarine Mar. Sci., 74, 847–865, https://doi.org/10.1093/icesjms/fsw194, canyon (NW Mediterranean), J. Marine Syst., 196, 86–96, 2017. https://doi.org/10.1016/j.jmarsys.2019.05.003, 2019. European Commission: Commission Regulation (EC) No. Bett, B. J., Malzone, M. G., Narayanaswamy, B., and Wigham, B. 2244/2003 of 18 December 2003 laying gown detailed provi- D.: Temporal variability in phytodetritus and megabenthic activ- sions regarding satellite-based Vessel Monitoring Systems, Off. ity at the seabed in the deep Northeast Atlantic, Prog. Oceanogr., J. Eur. Union, L333, 17–27, 2003. 50, 349–368, https://doi.org/10.1016/S0079-6611(01)00066-0, European Comission Fisheries & Maritime Affairs: Fleet Register 2001. on the Net, available at: http://ec.europa.eu/fisheries/fleet/index. Bligh, E. G. and Dyer, W. J.: A rapid method of total lipid ex- cfm and https://ec.europa.eu/fisheries/cfp/fishing_rules/fishing_ traction and purification, Can. J. Biochem Phys., 37, 911–917, fleet_en (last access: 31 January 2018), 2014. https://doi.org/10.1139/o59-099, 1959. Fabiano, M. and Danovaro, R.: Enzymatic activity, bacterial distri- Buscail, R., Pocklington, R., Daumas, R., and Guidi, L.: Fluxes and bution, and organic matter composition in sediments of the ross budget of organic matter in the benthic boundary layer over the sea (Antarctica), Appl. Environ. Microb., 64, 3838–3845, 1998. northwestern Mediterranean margin, Cont. Shelf Res., 10, 1089– Fabiano, M., Danovaro, R., and Fraschetti, S.: A three-year time se- 1122, https://doi.org/10.1016/0278-4343(90)90076-X, 1990. ries of elemental and biochemical composition of organic matter Calvo, S. and Genchi, G.: Carico organico ed effete eutrofici nel in subtidal sandy sediments of the Ligurian Sea (north western Golfo di Castellammare (Sicilia nord-occidentale), OEbalia, 15, Mediterranean), Cont. Shelf Res., 15, 1453–1469, 1995. 397–408, 1989. Fabiano, M., Pusceddu, A., Dell’Anno, A., Armeni, M., Vanucci, Canfield, D. E.: Factors influencing organic carbon preser- S., Lampitt, R. S., Wolff, G. A., and Danovaro, R.: Fluxes of vation in marine sediments, Chem. Geol., 114, 315–329, phytopigments and labile organic matter to the deep ocean in the https://doi.org/10.1016/0009-2541(94)90061-2, 1994. NE Atlantic Ocean, Prog. Oceanogr., 50, 89–104, 2001. Danovaro, R.: Methods for the study of deep-sea sediments, their Fanelli, E., Cartes, J. E., Badalamenti, F., Rumolo, P., and functioning and biodiversity, edited by: Danovaro, R., CRC Sprovieri, M.: Trophodynamics of suprabenthic fauna Press, Boca Raton, 2010. on coastal muddy bottoms of the southern Tyrrhenian Decreto 1339/2001: DECRETO 11 luglio 2001 – Disposizioni rel- Sea (western Mediterranean), J. Sea Res., 61, 174–187, ative all’interruzione tecnica delle attività di pesca nei comparti- https://doi.org/10.1016/j.seares.2008.10.005, 2008. menti marittimi siciliani per il triennio 2001/2003, Gazzetta Uf- Ferré, B., Durrieu de Madron, X., Estournel, C., Ulses, C., and Le ficiale della Regione Siciliana, Palermo, Italy, 2001. Corre, G.: Impact of natural and anthropogenic (trawl) resuspen- DeGeest, A. L., Mullenbach, B. L., Puig, P., Nittrouer, C. A., sion on the export of particulate matter to the open ocean. Appli- Drexler, T. M., Durrieu de Madron, X., and Orange, D. L.: cation to the Gulf of Lion (NW Mediterranean), Cont. Shelf Res., Sediment accumulation in the western Gulf of Lions, France: 28, 2071–2091, https://doi.org/10.1016/j.csr.2008.02.002, 2008. the role of Cap de Creus Canyon in linking shelf and slope Gerchakov, S. M. and Hatcher, P. G.: Improved technique for anal- sediment dispersal systems, Cont. Shelf Res., 28, 2031–2047, ysis of carbohydrates in sediments, Limnol. Oceanogr., 17, 938– https://doi.org/10.1016/j.csr.2008.02.008, 2008. 943, https://doi.org/10.4319/lo.1972.17.6.0938, 1972. Dellapenna, T. M., Allison, M. A., Gill, G. A., Lehman, R. Hale, R., Godbold, J. A., Sciberras, M., Dwight, J., Wood, C., D., and Warnken, K. W.: The impact of shrimp trawl- Hiddink, J. G., and Solan, M.: Mediation of macronutrients ing and associated sediment resuspension in mud dominated, and carbon by post-disturbance shelf sea sediment communities, shallow estuaries, Estuar. Coast. Shelf Sc., 69, 519–530, Biogeochemistry, 135, 121–133, https://doi.org/10.1007/s10533- https://doi.org/10.1016/j.ecss.2006.04.024, 2006. 017-0350-9, 2017. Depestele, J., Degrendele, K., Esmaeili, M., Ivanović, A., Kröger, Hartree, E. F.: Determination of protein: A modification of S., O’Neill, F. G., Parker, R., Polet, H., Roche, M., Teal, L. R., the lowry method that gives a linear photometric response, Vanelslander, B., and Rijnsdorp, A. D.: Comparison of mechan- Anal. Biochem., 48, 422–427, https://doi.org/10.1016/0003- ical disturbance in soft sediments due to tickler-chain SumWing 2697(72)90094-2, 1972. trawl vs. electro-fitted PulseWing trawl, ICES J Mar. Sci., 76, Kaiser, M. J.: Significance of Bottom-Fishing Disturbance, 312–329, https://doi.org/10.1093/icesjms/fsy124, 2018. Conserv. Biol., 12, 1230–1235, https://doi.org/10.1046/j.1523- Durrieu de Madron, X., Ferré, B., Le Corre, G., Grenz, C., Conan, 1739.1998.0120061230.x, 1998. P., Pujo-Pay, M., Buscail, R., and Bodiot, O.: Trawling-induced Kaiser, M. J., Collie, J. S., Hall, S. J., Jennings, S., and resuspension and dispersal of muddy sediments and dissolved Poiner, I. R.: Modification of marine habitats by trawling elements in the Gulf of Lion (NW Mediterranean), Cont. Shelf Biogeosciences, 16, 4307–4320, 2019 www.biogeosciences.net/16/4307/2019/ S. Paradis et al.: Organic matter contents and degradation in a highly trawled area during fresh particle inputs 4319 activities: prognosis and solutions, Fish Fish., 3, 114–136, Oberle, F. K. J., Puig, P., and Martín, J.: Fishing Activities, 503– https://doi.org/10.1046/j.1467-2979.2002.00079.x, 2002. 534, Springer, Cham., 2018. Koslow, J., Boehlert, G. W., Gordon, J. D. M., Haedrich, R. L., Lo- O’Neill, F. G. and Ivanović, A.: The physical impact of towed dem- rance, P., and Parin, N.: Continental slope and deep-sea fisheries: ersal fishing gears on soft sediments, ICES J. Mar. Sci. J. Cons., implications for a fragile ecosystem, ICES J. Mar. Sci., 57, 548– 73, i5–i14, https://doi.org/10.1093/icesjms/fsv125, 2016. 557, https://doi.org/10.1006/jmsc.2000.0722, 2000. Palanques, A., Puig, P., Guillén, J., Demestre, M., and Martín, J.: Ef- Krishnaswamy, S., Lal, D., Martin, J. M., and Meybeck, M.: fects of bottom trawling on the Ebro continental shelf sedimen- Geochronology of lake sediments, Earth Planet. Sc. Lett., 11, tary system (NW Mediterranean), Cont. Shelf Res., 72, 83–98, 407–414, https://doi.org/10.1016/0012-821X(71)90202-0, 1971. https://doi.org/10.1016/j.csr.2013.10.008, 2014. Linders, T., Nilsson, P., Wikström, A., and Sköld, M.: Distri- Paradis, S., Puig, P., Masqué, P., Juan-Díaz, X., Martín, J., bution and fate of trawling-induced suspension of sediments and Palanques, A.: Bottom-trawling along submarine canyons in a marine protected area, ICES J. Mar. Sci., 75, 785–795, impacts deep sedimentary regimes, Sci. Rep.-UK, 7, 43332, https://doi.org/10.1093/icesjms/fsx196, 2017. https://doi.org/10.1038/srep43332, 2017. Lo Iacono, C., Sulli, A., and Agate, M.: Submarine canyons of Paradis, S., Sanchez-Vidal, A., Masqué, P., Garcia-Orellana, north-western Sicily (Southern Tyrrhenian Sea): Variability in J., Calafat, A., and Canals, M.: Spatial distribution of morphology, sedimentary processes and evolution on a tec- sedimentation-rate increases in Blanes Canyon caused by techni- tonically active margin, Deep-Sea Res. Pt. II, 104, 93–105, fication of bottom trawling fleet, Prog. Oceanogr., 169, 241–252, https://doi.org/10.1016/J.DSR2.2013.06.018, 2014. https://doi.org/10.1016/J.POCEAN.2018.07.001, 2018. Lorenzen, C. and Jeffrey, J.: Determination of chlorophyll in sea- Pauly, D., Christensen, V., Guénette, S., Pitcher, T. J., Sumaila, water, Technical Paper in Marine Science (UNESCO), Technical U. R., Walters, C. J., Watson, R., and Zeller, D.: To- Papers in Marine Science, UNESCO, Paris, France, 35, 1–20, wards sustainability in world fisheries, Nature, 418, 689–695, 1980. https://doi.org/10.1038/nature01017, 2002. L. R. 1/1980: Provvedimenti per la razionalizzazione della pesca in Pipitone, C., Badalamenti, F., D’Anna, G., and Patti, B.: Fish Sicilia, Gazzetta Ufficiale della Regione Siciliana, Palermo, Italy, biomass increase after a four-year trawl ban in the Gulf of Castel- 1980. lammare (NW Sicily, Mediterranean Sea), Fish. Res., 48, 23–30, L. R. 25/1990: Modificazioni e integrazioni della legislazione re- https://doi.org/10.1016/S0165-7836(00)00114-4, 2000. gionale in materia di pesca, Gazzetta Ufficiale della Regione Si- Polymenakou, P. N., Pusceddu, A., Tselepides, A., Polychron- ciliana, Palermo, Italy, 1990. aki, T., Giannakourou, A., Fiordelmondo, C., Hatziyanni, L. R. 26/1987: Interventi nel settore della pesca, Gazzetta Ufficiale E., and Danovaro, R.: Benthic microbial abundance and della Regione Siciliana, Palermo, Italy, 1987. activities in an intensively trawled ecosystem (Thermaikos Marsh, J. B. and Weinstein, D. B.: Simple charring method for de- Gulf, Aegean Sea), Cont. Shelf Res., 25, 2570–2584, termination of lipids, J. Lipid Res., 7, 574–576, 1966. https://doi.org/10.1016/J.CSR.2005.08.018, 2005. Martín, J., Puig, P., Palanques, A., and Giamportone, A.: Commer- Pope, R. H., Demaster, D. J., Smith, C. R., and Seltmann, H.: Rapid cial bottom trawling as a driver of sediment dynamics and deep bioturbation in equatorial Pacific sediments: evidence from ex- seascape evolution in the Anthropocene, Anthropocene, 7, 1–15, cess 234 Th measurements, Deep-Sea Res. Pt. II, 43, 1339–1364, https://doi.org/10.1016/j.ancene.2015.01.002, 2014a. https://doi.org/10.1016/0967-0645(96)00009-4, 1996. Martín, J., Puig, P., Masqué, P., Palanques, A., and Sánchez-Gómez, Puig, P., Canals, M., Company, J. B., Martín, J., Amblas, D., Las- A.: Impact of bottom trawling on deep-sea sediment properties tras, G., and Palanques, A.: Ploughing the deep sea floor, Nature, along the flanks of a submarine canyon, PLoS One, 9, e104536, 489, 286–289, https://doi.org/10.1038/nature11410, 2012. https://doi.org/10.1371/journal.pone.0104536, 2014b. Puig, P., Martín, J., Masqué, P., and Palanques, A.: Increas- Martín, J., Puig, P., Palanques, A., and Ribó, M.: Trawling- ing sediment accumulation rates in La Fonera (Palamós) induced daily sediment resuspension in the flank of a Mediter- submarine canyon axis and their relationship with bot- ranean submarine canyon, Deep-Sea Res. Pt. II, 104, 174–183, tom trawling activities, Geophys. Res. Lett., 42, 8106–8113, https://doi.org/10.1016/j.dsr2.2013.05.036, 2014c. https://doi.org/10.1002/2015GL065052, 2015. Miralles, J., Radakovitch, O., and Aloisi, J. C.: 210 Pb sedimentation Pusceddu, A., Fiordelmondo, C., Polymenakou, P., Polychron- rates from the Northwestern Mediterranean margin, Mar. Geol., aki, T., Tselepides, A., and Danovaro, R.: Effects of bottom 216, 155–167, https://doi.org/10.1016/j.margeo.2005.02.020, trawling on the quantity and biochemical composition of or- 2005. ganic matter in coastal marine sediments (Thermaikos Gulf, Morato, T., Watson, R., Pitcher, T. J., and Pauly, D.: Fishing down northwestern Aegean Sea), Cont. Shelf Res., 25, 2491–2505, the deep, Fish Fish., 7, 24–34, 2006. https://doi.org/10.1016/j.csr.2005.08.013, 2005a. Nieuwenhuize, J., Maas, Y. E. M., and Middelburg, J. J.: Rapid anal- Pusceddu, A., Grémare, A., Escoubeyrou, K., Amouroux, J. M., ysis of organic carbon and nitrogen in particulate materials, Mar. Fiordelmondo, C., and Danovaro, R.: Impact of natural (storm) Chem., 45, 217–224, 1994. and anthropogenic (trawling) sediment resuspension on particu- Oberle, F. K. J., Swarzenski, P. W., Reddy, C. M., Nelson, late organic matter in coastal environments, Cont. Shelf Res., 25, R. K., Baasch, B., and Hanebuth, T. J. J.: Deciphering the 2506–2520, https://doi.org/10.1016/j.csr.2005.08.012, 2005b. lithological consequences of bottom trawling to sedimen- Pusceddu, A., Bianchelli, S., Canals, M., Sanchez-Vidal, A., Dur- tary habitats on the shelf, J. Marine Syst., 159, 120–131, rieu de Madron, X., Heussner, S., Lykousis, V., deStigter, H., https://doi.org/10.1016/j.jmarsys.2015.12.008, 2016. Trincardi, F., and Danovaro, R.: Organic matter in sediments of canyons and open slopes of the Portuguese, Catalan, Southern www.biogeosciences.net/16/4307/2019/ Biogeosciences, 16, 4307–4320, 2019 4320 S. Paradis et al.: Organic matter contents and degradation in a highly trawled area during fresh particle inputs Adriatic and Cretan Sea margins, Deep-Sea Res. Pt. I, 57, 441– and non-cohesive sediments, Limnol. Oceanogr., 61, 2076–2089, 457, https://doi.org/10.1016/j.dsr.2009.11.008, 2010. https://doi.org/10.1002/lno.10354, 2016. Pusceddu, A., Bianchelli, S., Martín, J., Puig, P., Palanques, Simpson, A. and Watling, A.: An investigation of the cumu- A., Masqué, P., and Danovaro, R.: Chronic and intensive lative impacts of shrimp trawling on mud-bottom fishing bottom trawling impairs deep-sea biodiversity and ecosys- grounds in the Gulf of Maine: effects on habitat and macro- tem functioning, P. Natl. Acad. Sci. USA, 111, 8861–8866, faunal community structure, ICES J. Mar. Sci., 63, 1616–1630, https://doi.org/10.1073/pnas.1405454111, 2014. https://doi.org/10.1016/j.icesjms.2006.07.008, 2006. Pusceddu, A., Bianchelli, S., and Danovaro, R.: Quantity Stephens, M. P., Kadko, D. C., Smith, C. R., and Latasa, M.: and biochemical composition of particulate organic mat- Chlorophyll-a and pheopigments as tracers of labile organic car- ter in a highly trawled area (Thermaikos Gulf, Eastern bon at the central equatorial Pacific seafloor, Geochim. Cos- Mediterranean Sea), Adv. Oceanogr. Limnol., 6, 21–32, mochim. Ac., 61, 4605–4619, https://doi.org/10.1016/S0016- https://doi.org/10.4081/aiol.2015.5448, 2015. 7037(97)00358-X, 1997 Regione Siciliana: Piano di tutela delle acque della Sicilia, SO- Tiano, J. C., Witbaard, R., Bergman, M. J. N., van Rijswijk, P., GESID, Palermo, Sicilia, 243 pp., 2007. Tramper, A., van Oevelen, D., and Soetaert, K.: Acute impacts of Rice, D. L.: The Detritus Nitrogen Problem: New Observations and bottom trawl gears on benthic metabolism and nutrient cycling, Perspectives from Organic Geochemistry, Mar. Ecol.-Prog. Ser., ICES J. Mar. Sci., https://doi.org/10.1093/icesjms/fsz060, online 9, 153–162, 1982. first, 2019. Roberts, C. M.: Deep impact: The rising toll of fishing in the deep Trimmer, M., Petersen, J., Sivyer, D. B., Mills, C., Young, sea, Trends Ecol. Evol., 17, 242–245, 2002. E., and Parker, E. R.: Impact of long-term benthic trawl Romano, C., Fanelli, E., D’Anna, G., Pipitone, C., Vizzini, disturbance on sediment sorting and biogeochemistry in the S., Mazzola, A., and Badalamenti, F.: Spatial variabil- southern North Sea, Mar. Ecol.-Prog. Ser., 298, 79–94, ity of soft-bottom macrobenthic communities in north- https://doi.org/10.3354/meps298079, 2005. ern Sicily (Western Mediterranean): Contrasting trawled Tselepides, A., Polychronaki, T., Marrale, D., Akoumianaki, I., vs. untrawled areas, Mar. Environ. Res., 122, 113–125, Dell’Anno, A., Pusceddu, A., and Danovaro, R.: Organic matter https://doi.org/10.1016/j.marenvres.2016.10.002, 2016. composition of the continental shelf and bathyal sediments of the Russo, T., Parisi, A., and Cataudella, S.: New in- Cretan Sea (NE Mediterranean), Prog. Oceanogr., 46, 311–344, sights in interpolating fishing tracks from VMS https://doi.org/10.1016/S0079-6611(00)00024-0, 2000. data for different métiers, Fish. Res., 108, 184–194, van de Velde, S., Van Lancker, V., Hidalgo-Martinez, S., Berelson, https://doi.org/10.1016/j.fishres.2010.12.020, 2011. W. M., and Meysman, F. J. R.: Anthropogenic disturbance keeps Russo, T., Parisi, A., Garofalo, G., Gristina, M., Cataudella, the coastal seafloor biogeochemistry in a transient state, Sci. S., and Fiorentino, F.: SMART: A Spatially Explicit Bio- Rep.-UK, 8, 5582, https://doi.org/10.1038/s41598-018-23925-y, Economic Model for Assessing and Managing Demersal Fish- 2018. eries, with an Application to Italian Trawlers in the Strait of van Nugteren, P., Moodley, L., Brummer, G.-J., Heip, C. H. R., Her- Sicily, edited by: MacKenzie, B. R., PLoS One, 9, e86222, man, P. M. J., and Middelburg, J. J.: Seafloor ecosystem function- https://doi.org/10.1371/journal.pone.0086222, 2014. ing: the importance of organic matter priming, Mar. Biol., 156, Sanchez-Cabeza, J. A., Masqué, P., and Ani-Ragolta, I.: Pb- 2277–2287, https://doi.org/10.1007/s00227-009-1255-5, 2009. 210 and Po-210 analysis in sediments and soils by mi- van Weering, T. C. E., Hall, I. R., de Stigter, H. C., McCave, crowave acid digestion, J. Radioanal. Nucl. Ch., 227, 19–22, I. N., and Thomsen, L.: Recent sediments, sediment accu- https://doi.org/10.1007/BF02386425, 1998. mulation and carbon burial at Goban Spur, N.W. European Sanchez-Cabeza, J. A., Masqué, P., Ani-Ragolta, I., Merino, Continental Margin (47–50◦ N), Prog. Oceanogr., 42, 5–35, J., Frignani, M., Alvisi, F., Palanques, A., and Puig, P.: https://doi.org/10.1016/S0079-6611(98)00026-3, 1998. Sediment accumulation rates in the southern Barcelona Whitmarsh, D., Carl, J., Pickering, H., Pipitone, C., Badalamenti, continental margin (NW Mediterranean Sea) derived from F., and D’Anna, G.: Economic Effects of Fisheries Exclusion 210 Pb and 137 Cs chronology, Prog. Oceanogr., 44, 313–332, Zones: A Sicilian Case Study, Mar. Resour. Econ., 17, 239–250, https://doi.org/10.1016/S0079-6611(99)00031-2, 1999. https://doi.org/10.1086/mre.17.3.42629366, 2002. Sañé, E., Martín, J., Puig, P., and Palanques, A.: Organic biomark- Wilson, A. M., Kiriakoulakis, K., Raine, R., Gerritsen, H. ers in deep-sea regions affected by bottom trawling: pigments, D., Blackbird, S., Allcocke, A. L., and White, M.: An- fatty acids, amino acids and carbohydrates in surface sediments thropogenic influence on sediment transport in the Whit- from the La Fonera (Palamós) Canyon, NW Mediterranean Sea, tard Canyon, NE Atlantic, Mar. Pollut. Bull., 101, 320–329, Biogeosciences, 10, 8093–8108, https://doi.org/10.5194/bg-10- https://doi.org/10.1016/j.marpolbul.2015.10.067, 2015. 8093-2013, 2013. Witte, U., Aberle, N., Sand, M., and Wenzhöfer, F.: Rapid re- Sarà, G., Scilipoti, D., Milazzo, M., and Modica, A.: Use of stable sponse of a deep-sea benthic community to POM enrichment: isotopes to investigate dispersal of waste from fish farms as a an in situ experimental study, Mar. Ecol.-Prog. Ser., 251, 27–36, function of hydrodynamics, Mar. Ecol.-Prog. Ser., 313, 261–270, https://doi.org/10.3354/meps251027, 2003. https://doi.org/10.3354/meps313261, 2006. Sciberras, M., Parker, R., Powell, C., Robertson, C., Kröger, S., Bo- lam, S., and Hiddink, J. G.: Impacts of bottom fishing on the sediment infaunal community and biogeochemistry of cohesive Biogeosciences, 16, 4307–4320, 2019 www.biogeosciences.net/16/4307/2019/