Plastic contamination in the decapod crustacean Nephrops norvegicus (Linnaeus, 1758)

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Abstract

The aim of this study was to determine the extent Nephrops consumes plastics in the Clyde Sea and if this intake occurs through their diet. Plastic contamination was found to be high in Nephrops, 83% of the animals sampled contained plastics (predominately filaments) in their stomachs. Tightly tangled balls of plastic strands were found in 62% of the animals studied but were least prevalent in animals which had recently moulted. No significant difference in plastic load was observed between males and females. Raman spectroscopy indicated that some of the microfilaments identified from gut contents could be sourced to fishing waste. Nephrops fed fish seeded with strands of polypropylene rope were found to ingest but not to excrete the strands. The fishery for Norway lobster, Nephrops norvegicus, is the most valuable in Scotland and the high prevalence of plastics in Nephrops may have implications for the health of the stock.

Highlights

► Clyde Sea Nephrops norvegicus were examined for the presence of plastics. ► Eighty three percent of the animals sampled contained plastic filaments. ► Tangled balls of filaments were found in 62% of the animals studied. ► Plastic filaments could be sourced to fishing waste. ► Nephrops in the laboratory ingested filaments in their diet.

Introduction

Plastic pollution is one of the most enduring threats faced by wildlife. Plastics are produced in huge quantities and are highly resistant to degradation. Although the problems associated with large plastic items, such as carrier bags, on large marine animals are well documented, it is only recently that the impacts of smaller plastic fragments, in particular on invertebrates have been considered. Plastics are incredibly persistent in the world’s oceans (Rios et al., 2007, Moore, 2008) and are among the primary pollutants of surface waters, pelagic waters and the marine benthos (Graham and Thompson, 2009). Plastics found in the marine environment originate from a variety of different sources with ships now estimated to discard 6.5 million tons of plastics every year (Derraik, 2002).

The impacts of larger plastics are well documented. Altogether 267 marine species are known to be affected by plastic debris through ingestion or entanglement (Teuten et al., 2007). These include 86% of all turtle species, 44% of all seabird species and 43% of all marine mammal species as well as numerous fish and crustaceans (Laist, 1987, Hartwig et al., 2007, Teuten et al., 2007). Seabirds are some of the most visibly affected oceanic animals, and by consequence some of the best studied (Laist, 1987, Ryan et al., 1988, Hartwig et al., 2007). Around 46% of plastics are buoyant (Barnes and Milner, 2005) and remain so until they accumulate too much epifauna and sink. Floating plastics disperse widely and degradation of plastic materials occurs slower in the sea than on the land due to the cool waters (Rios et al., 2007). As a large proportion of plastics are buoyant, contamination of marine sediments has, until recently, been widely ignored, although it is now recognised that small fragments in particular habitually enter the benthos. Plastics were shown to make up 80–85% of seabed debris in Tokyo Bay (Kanehiro et al., 1995) and 70% of seabed trawls carried out in the Mediterranean contained plastic (Galil et al., 1995). All plastics progressively fragment in the marine environment through mechanical action (Klemchuck, 2000), and the resulting fragments and microparticulates have a high potential for ingestion by animals (Browne et al., 2008). The impacts of these smaller fragments are not well studied, partly because quantifying plastics in tissues is challenging (Browne et al., 2008).

Small plastic fragments are available to invertebrates at the base of the food chain because they are in the same size range as sand and plankton (Browne et al., 2008). Many of these small fragments originate from fishing debris, which accumulates in areas used by commercially important marine life (Laist, 1987). Laboratory trials have shown that amphipods (detritivores), barnacles (filter feeders) and lugworms (deposit feeders) can ingest microplastics (Thompson et al., 2004). A study on particle collection showed that filter feeding polychaetes, bivalves, echinoderms and bryozoans will ingest 10 μm polystyrene microspheres (Ward and Shumway, 2004). Most recently sea cucumbers have been shown to selectively ingest plastics over sand particles, suggesting that holothurians could be voluntarily ingesting plastics (Graham and Thompson, 2009). It is now clear that certain species of marine invertebrates can, and do, ingest plastics. It is still unknown whether plastics of any size can be transferred up the food chain (Browne et al., 2008) and any ecological consequences remain unclear (Thompson et al., 2004). Harmful effects of plastics on invertebrates once ingested are still largely speculative (Ng and Obbard, 2006).

In addition to the potential physical impacts of plastic fragments, concern has recently been expressed about the potential for plastics to adsorb persistent organic pollutants. Oceanic plastics have been found to adsorb and transport chemicals including high concentrations of polychlorinated biphenols (PCBs), dichlorodiphenyl trichloroethane (DDT) and nonylphenol polyaromatic and aliphatic hydrocarbons (PAHs) (Carpenter et al., 1972, Mato et al., 2001, Rios et al., 2007, Teuten et al., 2007), many of which are banned substances. Once inside an organism, the presence of digestive surfactants is known to increase the bioavailability of PAHs sorbed to plastics (Voparil and Mayer, 2000) by increasing the desorption rate of plastics by up to 20 times compared to in sea water (Teuten et al., 2007). Recent studies have highlighted those phthalate-based plasticisers, which are widely added to plastic products, may leach from plastics. Although there have been few studies into their effects, they have been shown to affect development and reproduction in a range of species, including crustaceans (Oehlmann et al., 2009), to be endocrine disrupters in humans (Koch and Calafat, 2009) and are potentially carcinogenic (Talsness et al., 2009).

Studies on plastic ingestion in crustaceans have, so far, been limited. Thompson et al. (2004) conducted preliminary experiments using the amphipod Orchestia gammarellus. Amphipods, like all other invertebrate species studied so far, are primary consumers of plastics, directly mistaking the plastics for food. Little work has been done to investigate whether plastics can be transferred up a food web once they have been ingested. The proven ability of particulate debris to accumulate in sediments (Thompson et al., 2004) indicates that larger benthic crustaceans are exposed to this debris. The crustacean Nephrops norvegicus lives in muddy sediments and has a varied, non-selective diet as both an active predator and a scavenger (Cristo and Cartes, 1998). It has the potential to ingest plastics from its food and burrowing activities. Throughout its range, it is trawled commercially in deep water at depths of 40 m down to over 800 m (Phillips et al., 1980). The Nephrops fishery is the most valuable in Scotland, with the 2006 landings estimated to be worth £89.3 million according to the Fisheries Research Services Scotland (Milligan et al., 2009). In the Clyde there are around 40 Nephrops trawlers operating from Clyde Sea ports and an additional 30–40 seasonally from other Scottish and Irish ports. Trawling is permitted throughout the year except on weekends to vessels of a maximum length of 21 m (Wieczorek et al., 1999). Knowledge of threats to this species is vital in maintaining the sustainability and profitability of this fishery.

Nylon, most likely from fishing debris, has been incidentally recorded in the stomachs of Nephrops captured in the Adriatic as part of a study on diet (Wieczorek et al., 1999) but so far no study has been carried out to determine the prevalence of plastics in Nephrops from British waters. This novel, preliminary study aimed to assess whether this commercially important crustacean is capable of consuming small plastic fragments and to what extent this behaviour is prevalent in situ in the Clyde Sea area. A twofold approach was used: the analysis of stomach contents from animals caught from a range of locations within the Clyde Sea study area and a laboratory-based manipulation study.

Section snippets

Collection of samples

In May and June 2009, trawls were carried out in the north Clyde Sea area around the Isles of Cumbrae by the RV Aplysia from the University Marine Biological Station, Millport (UMBSM) (Fig. 1). Six trawl locations were selected, which had been previously identified as being heavily trawled areas (Marrs et al., 2002); these areas were chosen as the animals caught are representative of those caught for the commercial market. A beam trawl with a standard 70 mm mesh net was used. Short 15 min trawls

Stomach contents analysis

Hundred out of the 120 animals examined contained plastic in their stomachs (a prevalence of 83%). This plastic ranged in volume and size but was mainly composed of strands of monofilament plastics of different colours and thickness. The number of strands present varied with different animals and were categorised: none, if there was no plastic present; strands, if there were up to five strands present in the stomach; strands and ball, where there were some loose strands but others were tangled

Discussion

This preliminary study is the first to show that in the Clyde Sea, a high proportion of the decapod crustacean N. norvegicus contain plastic within their stomachs and that this plastic has the potential to accumulate within these crustaceans. No previous study has specifically studied the amounts of plastic found in Nephrops stomachs, but several studies have incidentally noted the presence of synthetic materials in the foreguts of Nephrops as a result of gut contents analyses. Bailey et al.

Acknowledgements

This research was completed in partial fulfilment of the requirements for the degree of MSc in Marine Ecology & Environmental Management studied by Fiona Murray and jointly run by Queen Mary, University of London and UMBSM. Thanks to Dr. Helen Keenan and Sornnarin Bangkedphol from the University of Strathclyde for their advice and analysis of the plastic filaments. Thanks also to the crews of R.Vs. Aora and Actinia for their help in obtaining the Nephrops used in this study and Howard McCrindle

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