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Trawling exerts big impacts on small beasts Les Watling1 noa, Honolulu, HI 96822 Department of Biology, University of Hawaii at Ma

Lophelia pertusa, for example, can be up to 8,000 y old and can provide habitat for more than 700 smaller species (2). In contrast, Throughout the world, there is concern about concern has been directed toward deep-sea there has been the sense that trawling on the impact of trawling on deep-sea bottom coral reefs and sponge beds (2, 3). Reef struc- open mud bottoms has little or no impact on the resident species or at least that, because communities (1). For the most part, this tures, formed by the scleractinian coral, the smaller species have higher turnover rates, the recovery from trawling will be rapid (4). In PNAS, however, Pusceddu et al. show that trawling on deep-sea muddy bottoms strongly alters the biochemical nature of the sediment and reduces the species diversity and abundance of meiofaunal organisms (animals ∼40–500 μm in size), and, in particular, the nematodes (5). As the fisheries of the continental shelves have become fully exploited (6), the search for commercially valuable species has moved off the continental shelf and onto the upper slope and offshore seamounts, resulting in depletion of deep-water stocks and also with consequences for benthic habitats (7). Deepsea trawl gear is large and heavy. The paired otter doors, which are metal plates pulled at an angle to the direction of movement of the ship and therefore act to spread the net, can weigh as much as 5 tons each. The bottom leading edge of the net, called the footrope, is armed with stainless steel bobbins or rollers and often rubber disks that are 30 cm or so in diameter, thus allowing the net to traverse rough bottom with minimal damage to the net. Large sediment plumes are generated by the turbulence created as the doors, ropes, and net are pulled across sandy or muddy bottoms at speeds up to 4 kn, and grooves are made in the sediment that can last for a very long time (8) (Fig. 1A). Puig et al. (1) demonstrated that bottom muds resuspended by trawling activity along the upper continental slope could be transported over long distances, often going down canyons to deeper waters, simultaneously drastically reducing the bottom topography and habitat heterogeneity in the area where trawling was frequent. The surficial layer of deep-sea marine sediment is composed of small (most commonly of 2–60 μm diameter) mineral grains loosely bound together by organic polymers Author contributions: L.W. wrote the paper.

Fig. 1. (A) Trawl marks in muddy sediment, Wilkinson Basin, Gulf of Maine. (B) Plastic embedded thin section (method detailed in ref. 9) of muddy sediment from 245-m depth in Wilkinson Basin, Gulf of Maine showing floc structure of the sediment just below the sediment–water interface. The width of the section is 200 μm. Object on the right side of the image is a test of planktonic tintinnid; white areas were originally water-filled spaces. 8704–8705 | PNAS | June 17, 2014 | vol. 111 | no. 24

The author declares no conflict of interest. See companion article on page 8861. 1

E-mail: [email protected]

www.pnas.org/cgi/doi/10.1073/pnas.1407305111

Watling

from water column plankton blooms or by in situ phytobenthos, so the phytopigment concentration can extend several centimeters below the sediment surface. In the deep sea, by contrast, the amount of food arriving at depth is reduced; thus, most deep-sea fauna is concentrated in the upper few centimeters of the sediment, as close to the sediment–water interface as possible. The microbes and metazoans quickly consume most of the deposited organic matter, allowing only a small fraction to be buried.

Trawling resuspends the upper flocculent layer of the sediment, removing the valuable food material. A major consequence of trawling then is that sedimentingesting organisms that resettle on a trawled site will be confronted with a substratum of much lower food quality. It is well known that the abundance and biomass of small benthic animals, who feed on the relatively high quality organic matter, decreases with water depth (17). This pattern is reflected in the data on abundance and biomass of meiofauna in the untrawled areas studied by Pusceddu et al. In contrast, their 500-m trawled site was very depauperate in meiofauna, having abundance and biomass values lower even than the 2,000-m site, suggesting that the repeated passage of bottom trawls created a nutrient-poor environment with conditions analogous to sites in much deeper water. This study demonstrates that the small animals of muddy sediments can be impacted by bottom trawling as much or more than the larger, more charismatic, deep-sea corals and sponges and that very likely no habitat will be immune to the impacts of deep-sea bottom trawling.

1 Puig P, et al. (2012) Ploughing the deep sea floor. Nature 489(7415):286–289. 2 Roberts JM, et al. (2009) Cold-Water Corals: The Biology and Geology of Deep-Sea Coral Habitats (Cambridge Univ Press, Cambridge, UK). 3 Althaus F, et al. (2009) Impacts of bottom trawling on deep-coral ecosystems of seamounts are long-lasting. Mar Ecol Prog Ser 397:279–294. 4 Jennings S, et al. (2002) Effects of chronic trawling disturbance on the production of infaunal communities. Mar Ecol Prog Ser 243:251–260. 5 Pusceddu A, et al. (2014) Chronic and intensive bottom trawling impairs deep-sea biodiversity and ecosystem functioning. Proc Natl Acad Sci USA 111:8861–8866. 6 Pauly D (2007) The Sea Around Us Project: Documenting and communicating global fisheries impacts on marine ecosystems. Ambio 36(4):290–295. 7 Gordon JDM (2003) The Rockall Trough, Northeast Atlantic: The cradle of deep-sea biological oceanography that is now being subjected to unsustainable fishing activity. J Northwest Atl Fish Sci 31:57–83. 8 Roberts JM, et al. (2000) Seabed photography, environmental assessment and evidence for deep-water trawling on the continental margin west of the Hebrides. Hydrobiol 441(1):173–183. 9 Watling L (1988) Small-scale features of marine sediments and their importance to the study of deposit-feeding. Mar Ecol Prog Ser 47:135–144.

10 Graf G (1992) Benthic-pelagic coupling: A benthic view. Oceanogr Mar Biol Annu Rev 30:149–190. 11 Lutz MJ, Caldeira K, Dunbar RB, Behrenfeld MJ (2007) Seasonal rhythms of net primary production and particulate organic carbon flux to depth describe the efficiency of biological pump in the global ocean. J Geophys Res 112:C10011. Available at http://onlinelibrary.wiley.com/doi/10.1029/2006JC003706/ pdf. Accessed May 13, 2014. 12 Mayer LM, et al. (1993) Low-density particles as potential nitrogenous food sources for benthos. J Mar Res 51(2):373–389. 13 Duplisea DE, Jennings S, Malcolm SJ, Parker R, Sivyer DB (2001) Modelling potential impacts of bottom trawl fisheries on soft sediment biogeochemistry in the North Sea. Geochem Trans 2(1):112. 14 Schratzberger M, et al. (2009) The impact of seabed disturbance on nematode communities: Linking field and laboratory observations. Mar Biol 156(4):709–724. 15 Soetaert K, Heip C (1995) Nematode assemblages of deep-sea and shelf break sites in the North Atlantic and Mediterranean Sea. Mar Ecol Prog Ser 125:171–183. 16 Percival P, Frid C, Upstill-Goddard R (2005) The impact of trawling on benthic nutrient dynamics in the North Sea: Implications of laboratory experiments. Am Fish Soc Symp 41:491–501. 17 Rex MA, Etter RJ (2010) Deep-Sea Biodiversity: Pattern and Scale (Harvard Univ Press, Cambridge, MA).

nutritional needs. Trawling resuspends and disperses the flocculent material, so food quality of the sediment after trawling is always lower than before (16). In shallow water, the nutritional quality of the sediment is being constantly replenished by deposition

Pusceddu et al. show that trawling on deep-sea muddy bottoms strongly alters the biochemical nature of the sediment.

PNAS | June 17, 2014 | vol. 111 | no. 24 | 8705

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(9) (Fig. 1B). In shallow water, organic matter input to the sediment surface can be the result of the direct deposition of plankton cells, settling of fecal material from animals feeding on phyto- and bacterio-plankton in the water column, or lateral movement of previously settled material due to slumping or storm wave redistribution (10). Because the sediment surface is frequently shallower than the water column mixing depth, large numbers of organic particles come into contact with and are incorporated into the sediment. As the water depth increases, however, organic matter is more likely to be recycled in the water column, with a concomitant decrease in deposition of phytodetritus to the sediment surface (11). The organic matter at the sediment water interface is in the form organic-mineral flocs (Fig. 1B) that is readily colonized by microbes. The organic matrix and mineral grains support a microbial population in the range of 107–109 cells per g of wet sediment. This “low density” fraction of the sediment has a very high nutritional content (12) and therefore is a valuable food source for the small macrofauna and meiofauna, such as nematodes, living at or near the sediment– water interface. Because of its low density, the floc material is easily resuspended by the turbulence created by a passing trawl. As Pusceddu et al. show, repeated trawling in an area lowers the overall organic content of the surficial layer of the sediment, in effect reducing the food value of the sediment and thus the quality of the habitat. This reduction in habitat quality is reflected in reduced meiofauna abundance, biodiversity, and nematode species richness. Similar results are often seen in shallow water sites subject to frequent trawling (13, 14). The study by Pusceddu et al. demonstrates that deep-sea trawling can have a significant impact on species that are not large or necessarily long-lived but that are quite common and diverse in deep-sea sediments (15). These small species directly depend on the input of phytodetrital flocs for their

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