Accidental and Secondary Ingestion
Filter-feeding marine organisms, ranging in size from small crustaceans, to shellfish, fish, some seabirds (prions, Pachyptila spp.) and ultimately large baleen whales may be prone to plastic ingestion. These species obtain their nutrition by filtering large volumes of water, which may contain debris in addition to the targeted food source. Although non-food items can be ejected before passage into the digestive system, this is not always the case. In their natural habitat, ingested plastics have been found in filter-feeding crustaceans such as goose barnacles (Lepas spp.; Goldstein and Goodwin 2013) and mussels (Mytilus edulis, Van Cauwenberghe et al. 2012; Leslie et al. 2013; Van Cauwenberghe and Janssen 2014). Large baleen whales have been long known to occasionally ingest debris (Laist 1997; Baulch and Perry 2014). In France, a young minke whale (Balaenoptera acutorostrata) beached with various plastic bags completely filling its stomachs (De Pierrepont et al. 2005). Curiously, we have found no record of plastic ingestion by obligate filter-feeding large fish such as basking shark (Cetorhinus maximus) or manta ray (Manta birostris). Some bony fish species partially use filter-feeding, but also directional feeding making it difficult to assign the pathway of debris ingestion. Uptake of plastic by filter-feeding fish has been reported for herring (Clupea harengus) and horse mackerel (Trachurus trachurus) from the North Sea and English Channel (Foekema et al. 2013; Lusher et al. 2013). Accidental ingestion of a mixture of food and debris is not restricted to filter feeders. In the Clyde Sea, 83 % of Norway lobsters (Nephrops norvegicus) had plastic in their stomach, which was attributed either to passive ingestion of sediment while feeding or to secondary ingestion (Murray and Cowie 2011), although it could be argued that the fibres ingested may resemble benthic polychaete prey. Plastics and other non-food items found in stomachs of harbour seals in the Netherlands were considered to have been accidentally ingested when catching prey fishes (Bravo Rebolledo et al. 2013). A similar route for plastic ingestion was proposed by Di Beneditto and Ramos (2014), who showed that plastic in franciscana dolphins was related to benthic feeding habits, in which disturbance of sediment probably induced accidental intake of plastic debris. Florida manatees (Trichechus manatus latirostris) may take up plastic accidentally during foraging on plants (Beck and Barros 1991). Pelagic loggerhead sea turtles may ingest plastic because they feed indiscriminately or graze on organisms settled on floating plastic (McCauley and Bjorndal 1999; Tomas et al. 2002). A special case of such accidental ingestion is known for the Laysan albatross who take up plastic particles in combination with eggs strings of flying fish. The fishes attach their eggs to floating items: previously seaweed, bits of wood or pumice, but nowadays often plastic objects (Pettit et al. 1981). This phenomenon has also been observed in loggerhead turtles. The plastic in their stomachs was sometimes covered by the eggs of the insect Halobates micans (Frick et al. 2009).
A final case of unintentional plastic ingestion is that of secondary ingestion, which occurs when animals feed on prey, which had already ingested debris. This may concern both prey swallowed as a whole or scavenging. In seabirds, skuas are known to forage on smaller seabirds that consume plastic (Ryan 1987). Great skuas (Stercorarius skua) from the South Atlantic Ocean predate several seabird species, and their regurgitated boluses showed a link with the amount of secondarily ingested plastic and their main prey species (Bourne and Imber 1982; Ryan and Fraser 1988). In the monitoring study on northern fulmars (Fulmarus glacialis) in the North Sea intact stomachs from scavenged fulmars or black-legged kittiwakes (Rissa tridactyla) were occasionally found, which contained plastic (Van Franeker et al. 2011). A spectacular example of secondary ingestions was provided by Perry et al. (2013) who reported a ball of nylon fishing line in the stomach of a little auk (Alle alle), that was found in the stomach of a goose fish (Lophius americanus). The presence of small plastic particles in the faeces of fur seals on Macquarie Island was attributed to secondary ingestion through the consumption of myctophid fishes (Eriksson and Burton 2003). High abundance of small plastics in myctophid fishes (Boerger et al. 2010; Davison and Asch 2011), in combination with the fact that this type of fish is a common prey for many larger marine predators, suggest that secondary ingestion may be more common than reported.