Impacts of Bottom Fishing on Sediment Biogeochemical and Biological Parameters in Cohesive and Non-cohesive Sediments

Bottom-trawl fisheries are wide-spread and have large effects on benthic ecosystems.We investigate the effect of scallop dredging on sand and otter trawling on mud by measuring changes in the infaunal community and the biogeochemical processes which they mediate. We hypothesize that changes in biogeochemistry due to fishing will be larger in mud where macrofauna-mediated processes are expected to play a greater role, than in sand where hydrodynamics mediate the redox system. We sampled benthic infauna, sediment porewater nutrients, oxygen, chlorophyll a (Chl a), apparent redox potential discontinuity layer, organic carbon and nitrogen content over a gradient of fishing intensity in sand and mud. The effects of fishing on biogeochemistry were stronger on mud than on sand, where biogeochemistry appeared to be more strongly influenced by tidal currents and waves. On mud, trawling increased sediment-surface Chl a and ammonium concentration beyond 5 cm depth, but decreased ammonium and silicate concentration in the upper sediment layers. The effects of fauna and bioturbation potential on biogeochemistry were very limited in both mud and sand habitats. Our results suggests that otter trawling may be affecting organic-matter remineralization and nutrient cycling through sediment resuspension and burial of organic matter to depth rather than through the loss of bioturbation potential of the benthic community. In conclusion, our hypothesis that the effects of trawling on biogeochemistry are larger in mud is supported, but the hypothesis that these effects are mediated by changes in the infauna is not supported. These results imply that management of trawling on muddy sediments should have higher priority. Fishing with bottom towed fishing gear is a major source of physical disturbance for marine benthic ecosystems. Large parts of most shelf and deep seas have been intensively exploited by bottom fishing for decades (Halpern et al. 2008; Puig et al. 2012). As nets, beams, trawl doors, chains and dredges pass over the seabed, the sediment surface is disturbed and 20–50% of the resident biota (e.g., bivalves, burrowing crustaceans, tube-building polychaetes, and echinoderms) is damaged or removed (Jennings and Kaiser 1998; Kaiser et al. 2006). Previous studies have shown that bottom fishing results in a decrease in benthic secondary production, as well as changes in the community structure and size composition of benthic invertebrate communities (Hiddink et al. 2006; Hinz et al. 2009; Bolam et al. 2014a). Shifts toward higher abundances of scavenging and deposit feeding organisms and smallbodied infaunal species have also been reported due to trawling (Kaiser et al. 2000; Tillin et al. 2006). In addition to changes to benthic faunal communities, bottom fishing can alter the biogeochemical characteristics of the sediment and that of the overlying water column through a combination of the removal of surficial sediments and the burial or mixing of organic matter (Duplisea et al. 2001; Warnken et al. 2003; O’Neill and Summerbell 2011). The resuspended sediment created by groundropes, chains and nets as bottom trawls are dragged along the seabed increases the water turbidity and the concentration of particulate organic matter in the overlying water and may enhance phytoplankton primary production due to higher nutrient loads (Riemann and Hoffman 1991; Pilskaln et al. 1998; Palanques et al. 2001). Changes within the sediment matrix, such as an increase in sediment sorting and porosity (Trimmer et al. 2005) can result in changes to the oxygen *Correspondence: m.sciberras@bangor.ac.uk Additional Supporting Information may be found in the online version of this article. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. 1 LIMNOLOGY and OCEANOGRAPHY Limnol. Oceanogr. 00, 2016, 00–00 VC 2016 The Authors Limnology and Oceanography published by Wiley Periodicals, Inc. on behalf of Association for the Sciences of Limnology and Oceanography doi: 10.1002/lno.10354 regime (Warnken et al. 2003), which may influence key steps in the nitrogen cycle, as oxygen regulates both nitrification and denitrification in benthic sediments (Rysgaard et al. 1994). Because of their weight, otter trawl boards and dredges create large furrows in the sea floor that range between 5 cm and 35 cm deep depending on the type of sediment (Eigaard et al. 2015). The redistribution of organic matter that results from this ploughing action may shift the balance between aerobic and anaerobic mineralization, as the organic matter is buried beneath the narrow oxic zone before mineralization is complete (Mayer et al. 1991; Pilskaln et al. 1998). Duplisea et al. (2001) and Trimmer et al. (2005) found higher rates of organic matter remineralization via sulphate reduction at high trawling disturbance areas. Indirectly, bottom fishing may affect the oxygen regime and biogeochemical processing of carbon by altering the composition of the benthic fauna, which itself regulates oxygen and redox structure through bioturbation and bioirrigation (Kristensen 2000; Duplisea et al. 2001; Waldbusser et al. 2004). Mesocosm experiments by Olsgard et al. (2008) showed that the reduction of large-bodied bioturbators such as the surficial modifiers Brissopsis lyrifera and Nuculana minuta, resulted in a lower efflux of silicate (SiO4 ) and nitrate/ nitrite (NOx) from the sediment to the overlying water. Declines in the density of burrowand tube-building organisms may result in changes to benthic respiration and denitrification due to a reduction in oxygen penetration and microbial metabolism (Aller and Aller 1998; Braeckman et al. 2010). It may therefore be expected that trawling will affect sediment chemistry through a reduction in community bioturbation potential, burrow density and functional diversity. Habitat characteristics may be strong determinants of the relative impact of bottom fishing activity on both the infauna and sediment biogeochemical processes. For example, the effects of bottom fishing on benthic carbon mineralization and sediment characteristics (e.g., particle size distribution, porosity) have been demonstrated to be smaller in highly natural disturbed areas where wave and tidal actions lead to bulk sediment disturbance and transport (Osinga et al. 1996; Trimmer et al. 2005). Similarly, several studies have shown that the effects of fishing on fauna are smaller in coarse than fine sediment (Collie et al. 2000; Kaiser et al. 2006; references therein), as the former are characterized by a higher fraction of small-sized, fast growing and highly productive species that are more adapted to continual natural disturbance by tides and waves (Kaiser and Spencer 1996). Experiments have shown that the influence of bioturbation on nutrient regeneration and oxygen consumption is greater in diffusion dominated (low disturbance, fine sediments and low rates of sediment pore water exchange) than in advection dominated (high disturbance, coarse sediments and consequently high rates of sediment pore water exchange) systems, as sediment processes in the former are more strongly influenced by bioturbation (reviewed by Mermillod-Blondin and Rosenberg 2006). It may therefore be expected that trawling disturbance will have stronger effects on the fauna and biogeochemical processes in mud than on sand by altering diffusion of dissolved oxygen from the sediment-overlying seawater into the pore water and oxygenation of the sediment pore water by sediment resuspension. Few empirical studies to date have investigated the combined effects of bottom fishing on both the infaunal community and the biogeochemical processes which they mediate (Pilskaln et al. 1998; Duplisea et al. 2001; Waldbusser et al. 2004; Hiddink et al. 2006), and this is important for understanding the impacts of fishing on ecosystem functioning. This study fills this knowledge gap by assessing the large-scale impact of chronic bottom fishing on benthic community structure and sediment biogeochemistry across different fishing pressure gradients and habitat types (muddy vs. sandy habitats). The following hypotheses are tested; (i) fishing will negatively affect benthic invertebrate abundance and reduce the bioturbation potential of the community as large bioturbatory macrofaunal species are removed by trawling; (ii) fishing will result in changes in the sediment redox and associated biogeochemistry as a result of sediment resuspension (e.g., lower concentration of NH4 in upper sediment layers) and sediment/carbon mixing to depth (e.g., higher concentration of NH4 in pore-water); (iii) changes in sediment biogeochemistry due to fishing will be larger in mud where macrofauna-mediated processes are expected to play a more significant role, than in sand where physical processes such as tides and currents generally mediate the redox system.


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Fishing with bottom towed fishing gear is a major source of physical disturbance for marine   highly productive species that are more adapted to continual natural disturbance by tides and 99 waves (Kaiser and Spencer 1996). Experiments have shown that the influence of bioturbation on 100 nutrient regeneration and oxygen consumption is greater in diffusion dominated (low 101 disturbance, fine sediments and low rates of sediment pore water exchange) than in advection 102 dominated (high disturbance, coarse sediments and consequently high rates of sediment pore 103 water exchange) systems, as sediment processes in the former are more strongly influenced by   The effects of chronic bottom fishing on benthic infauna and sediment biogeochemistry were 129 investigated over gradients of commercial bottom fishing intensity on muddy and sandy fishing 130 grounds in the north Irish Sea between the 28 th June and 6 th July 2014 (Fig.1) Within each of the two areas, sixteen 1 x 2 km sites were selected along a gradient of fishing   techniques were used to produce a complete particle size distribution for sediment particles 205 larger and smaller than 1 mm, respectively. Porosity was calculated following methods described 206 by Holme and McIntyre (1984). Sediment chlorophyll-a was extracted from the thawed sub-207 cores using acetone and analysed using a fluorometer as described by Tett (1987). Samples for 208 the analysis of sediment organic carbon and nitrogen were thawed, freeze dried and acidified as Samples for pore-water nutrients were extracted using a sipping system from intact NIOZ cores 215 at the following sediment depths; 0, 1, 2, 3, 4, 5, 7.5, 10, 14, 17, 20 cm (D. B. Sivyer unpubl.).

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The extracted water samples were filtered using 0.2 µm filters and analysed for nitrate, nitrite, 217 ammonium, silicate and phosphate using a scalar auto-analyser (Kirkwood et al. 1996). At the 218 sandy sites, the deepest pore-water sample was taken at 14 cm as the NIOZ corer generally 219 penetrated to about 15 cm in sand. The sediment within the sub-core used for oxygen measurements (ca. 0.16 m 3 , equivalent to ca. The muddy sites were composed of more than 60% mud (< 63 µm) and the sediment was poorly 340 sorted, whereas the sandy sites were composed of more than 95% sand (> 63 µm and < 2000 341 µm) and the sediment was moderately well sorted (SM 1). The fishing frequencies between the 342 two study areas did not overlap; the fishing frequency ranged from 2.95 to 8.51 yr -1 at the muddy 343 sites and from 0 to 1.63 yr -1 at the sandy sites (SM 1).  (Fig.2a, b). The infaunal community in mud was dominated by fewer species but larger 351 individuals, whereas the sand community was characterized by a more diverse assemblage of 352 smaller individuals. The average total infaunal density and biomass in sand were 198.14 ± 27.14 353 individuals m -2 and 1.54 ± 0.29 g WW m -2 , respectively (Fig.2a, b). In mud, the average infaunal 354 density and biomass were 34.69 ± 2.46 individuals m -2 and 5.29 ± 0.99 g WW m -2 , respectively 355 ( Fig.2a, b). The community bioturbation potential index (BP C ) was similar between the two 356 sediment types and did not change significantly with fishing frequency in mud (t = 0.12, df = 9, p 357 = 0.90, r 2 = 0.01) and sand (t = 0.88, df = 6, p = 0.41, r 2 = 0.11) (Fig.2c). However, different   Table 1a, b). However, none of the motility, feeding or 372 bioturbation modalities examined at the muddy sites showed a significant relationship with 373 fishing frequency (non-significant 'fishing term' in Table 1). In contrast, fishing resulted in a 374 significant increase in the biomass of surface deposit feeders and suspension feeders relative to 375 predators and scavengers at the sandy sites ( Fig.2g; significant 'interaction term' in Table 2a).

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There was no significant effect of fishing on species with different mobilities or bioturbation 377 modes in sand (Table 2b, c). The sediment at the muddy sites had significantly higher organic carbon and nitrogen content 382 than the sandy sites (organic carbon: 0.87 ± 0.04 %m/m in mud vs. 0.06 ± 0.01 %m/m in sand; 383 organic nitrogen: 0.1 ± 0.004 %m/m in mud vs. 0.02 ± 0.001 %m/m in sand) (Fig.3b, c). The 384 average chlorophyll-a content of the muddy substratum was 1.8 ± 0.18 µg/g (Fig.3a), whereas 385 Sciberras et al.
Trawling impacts on ecosystem processes 18 that in sand was < 1 µg/g, which was lower than the minimum detection limit of the fluorometer 386 hence why no data is plotted for sand in Fig. 3a. At the muddy sites, sediment chlorophyll-a 387 content and porosity increased significantly with fishing frequency indicating that the sediment 388 matrix contained more water and phytodetritus at sites exposed to higher fishing disturbance 389 (Fig.3a, d; Table 3a). There was a slight but significant increase in organic nitrogen content with 390 fishing frequency at the sandy sites, but no significant effects of fishing on organic carbon 391 content (Table 3b).

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The oxygen penetration depth (OPD) and the depth of the apparent redox discontinuity layer 394 (aRPD) were shallower than 2 cm across the sites sampled in the muddy substratum. The OPD 395 ranged between 0.30 and 1.20 cm and the aRPD between 0.85 and 1.90 cm in mud (Fig.3e, f).

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Most of the oxygen profiles showed a smooth decreasing trend in the concentration of free 397 oxygen with sediment depth, indicating that the oxygen distribution in mud was governed by 398 molecular diffusion between the oxic seawater and the oxygen-consuming sediment (SM 5A).

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Neither the OPD nor the aRPD showed a significant relationship with fishing frequency in mud 400 (Table 3a). The coarse sand mixed with shell fragments at the sandy sites only allowed oxygen 401 profiling of the top 2 cm of the sediment core. High concentrations of oxygen were still present 402 at 2 cm (SM 5B), thus suggesting that the OPD in sand was deeper than 2 cm. In sand, the SPI- SPI-images obtained from the muddy sites indicate that the sediment is highly disturbed at these 408 sites (SM 6).

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The concentrations of ammonium (NH 4 + ) and silicate (SiO 4 -) in pore-water were an order of 411 magnitude higher in mud than in sand (Fig.4, SM 5), reflecting the higher organic carbon and 412 chlorophyll-a (and associated diatom) levels in mud, which are the source of these inorganic 413 nutrients. The integrated-depth profiles for NH 4 + in mud (Fig.4a)  cms of the muddy sediment, but increased significantly with fishing between 5 and 20 cm 418 (Fig.4a, c; significant interaction term in Table 4a Trawling impacts on ecosystem processes 21 significant pore-water relocation caused by trawling, which is the only process which could act 453 to these depths at the sites. The injection of carbon to depth is also likely to stimulate localized 454 Fe reduction which mediates increased phosphate release at depth. Future analysis of total 455 organic carbon and C:N ratios in profiles would enable age determination and source of carbon, 456 hence allowing the mechanism of impact to be identified better. Trans. 14: 1-6.