Ways of Plastic Ingestion
Plastics may be ingested intentionally or accidentally and both pathways deserve further discussion.
Fig. 4.4 Plastic ingestion by northern fulmars (Fulmarus glacialis). Unopened stomach with plastic inside (top), fulmars at sea chewing on a plastic fragment (bottom left), stomach content of a northern fulmar with fragments, foam, sheets and wood (bottom right) (Photos: J.A. van Franeker (1, 3) and S. Kühn (2), IMARES)
Why some animals intentionally ingest plastic debris may depend on a range of factors, and these may vary among different animal groups. Although many of these factors interact, it is useful to review at least some of them separately.
In seabirds, plastic ingestion has been linked to foraging strategy by several authors (e.g. Day et al. 1985; Azzarello and Van Vleet 1987; Ryan 1987; Tourinho et al. 2010.) From their study on many different seabird species, Day et al. (1985) concluded, that pursuit-diving birds have the highest frequency of plastic uptake, followed by surface-seizing and dipping seabirds. Provencher et al. (2010) reported that marine birds, feeding on crustaceans and cephalopods had ingested more plastic than piscivorous seabirds, and those omnivores are most likely to confuse prey and plastic. Seabirds with specialized diets are less likely to misidentify plastic, unless a particular type resembles their prey (Ryan 1987). Many gull species frequent rubbish bins and landfill areas, in addition to foraging in marine habitats and seem prone to ingest debris. However, ingested debris does not often show up in their stomachs during dissections because they clear them daily by regurgitating hard prey remains (Hays and Cormons 1974; Ryan and Fraser 1988; Lindborg et al. 2012). As regurgitation takes place regularly, plastics quantified from boluses reflect the ingestion of the very last period, rather than accumulated debris (Camphuysen et al. 2008; Ceccarelli 2009; Codina-García et al. 2013; Hong et al. 2013). Tubenosed seabirds mostly retain plastic and hard prey items (Mallory 2006) because they possess two stomachs with a constriction (Isthmus gastris) between the glandular proventriculus and the muscular gizzard (Furness 1985; Ryan and Jackson 1986). Even when spitting stomach oil to defend themselves or when feeding their chicks, only plastics from the proventriculus are regurgitated but items from the gizzard are retained (Rothstein 1973). Marine turtles frequently ingest plastic bags as they may mistake them for jellyfish, a common component of their diet (Carr 1987; Lutz 1990; Mrosovsky et al. 2009; Tourinho et al. 2010; Townsend 2011; Campani et al. 2013; Schuyler et al. 2014). While accidental plastic ingestion by filter-feeding baleen whales (Mysticeti) might be assumed to be common, Walker and Coe (1990) expected that toothed whales (Odontoceti) would have a low rate of plastic ingestion because they use echolocation or visual cues to locate their prey. However, Laist (1997), Simmonds (2012) and Baulch and Perry (2014) all made extensive descriptions of toothed whales that had ingested plastic. Indeed, our updated literature search showed that 54 and 62 % of the baleen and toothed whales, respectively, ingest plastics. It has also been suggested, that marine mammals could see plastic as a curiosity and while investigating it, they swallow it or become entrapped (Mattlin and Cawthorn 1986; Laist 1987). Large predatory fishes and birds are known to frequently inspect plastic debris and take bites out of larger plastic items. Cadée (2002) observed that 80 % of foamed plastic debris on the Dutch coast showed peckmarks of birds and suggested that the birds mistake polystyrene foam for cuttlebones or other food. Carson et al. (2013) observed bite marks of sharks or large predatory fishes on 16 % of plastic debris beached on Hawaii indicating 'testing' of materials. Choy and Drazen (2013) showed that among 595 individuals of seven such large predatory fish species, 19 % of individuals (range per species <1–58 %) had actually ingested plastic. Foraging strategies may vary under different conditions of food availability. Duguy et al. (2000) considered that decreased availability of jellyfish during winter could be the reason for the higher incidence of plastic bags during these months in the diet of turtles.
In conclusion it seems that although indiscriminate omnivorous predators or filter feeders appear most prone to plastic ingestion, there are many examples of ingestion among species with specialized foraging techniques and specific prey selection.
One of the factors often considered to influence the consumption of marine debris is color as specific colors might attract predators when resembling the color of their prey. In seabirds, this has been suggested for e.g. greater shearwaters (Puffinus gravis) and red phalaropes (Phalaropus fulicarius) (Moser and Lee 1992). Parakeet auklets (Aethia psittacula) on the Alaskan coast, feeding naturally primarily on light-brown crustaceans, consumed mainly darker plastic granules, suggesting they were mistaken for food items (Day et al. 1985). In studies of marine turtles, the issue of color preference is controversial. Lutz (1990) indicated no preferential ingestion of different plastic colors; neither did Campani et al. (2013) in loggerhead turtles. However, others find light-colored and translucent plastics are most commonly ingested, suggesting similarity to their jellyfish prey (Bugoni et al. 2001; Tourinho et al. 2010). Schuyler et al. (2014) indicated such prey-similarity by the combination of translucency and flexibility of plastic bags and found that blue-colored items were less frequently eaten probably because of lower detection rates in open water. An additional visual factor could be shape as floating plastic bags resemble jellyfish. In fur seal scats, the colors of plastic were white, brown, blue, green and yellow (Eriksson and Burton 2003), however, no clear preference was evident.
White, clear, and blue plastics were primarily ingested by planktivorous fish from the North Pacific central gyre but similar color proportions were recorded from neuston samples (Boerger et al. 2010). By contrast, black particles were most prevalent in stomachs of fish from the English Channel but this study included both pelagic and demersal fish (Lusher et al. 2013). While two mesopelagic fish (Lampris spp.) species did not favour particular colors Alepisaurus ferox seemed to favour white and clear plastic pieces, which may resemble their gelatinous prey (Choy and Drazen 2013). The majority of strands reported from the intestines of Norway lobsters (Nephrops norvegicus) were also transparent (Murray and Cowie 2011).
Studies on the color-specific uptake often do not take into account that color may change in the gastrointestinal tract (e.g. Eriksson and Burton 2003). Also, there are rarely quantitative data on the abundance of various color categories in the foraging ranges of the species studied. In general, light colors seem to be most common in floating marine debris ranging from 94 % of the abundance in the Sargasso Sea (Carpenter et al. 1972) and 82–89 % in the South Atlantic (Ryan 1987) to 72 % in the North Pacific (Day et al. 1985). The frequently observed prevalence of translucent or brightly colored objects in stomachs may thus reflect the availability of such items the ambient environment rather than color selectivity.
Among seabirds, it has been well-established that younger northern fulmars have more plastic in their stomachs than adults (Day et al. 1985; Van Franeker et al. 2011). The same has been shown for flesh-footed and short-tailed shearwater (Puffinus carneipes and P. tenuirostris, respectively, Hutton et al. 2008; Acampora et al. 2014). The chicks of Laysan albatrosses (Phoebastria immutabilis) at colonies (Auman et al. 1997) have a much higher load of plastic than adults at sea (e.g. Gray et al. 2012). In marine turtles, Plotkin and Amos (1990) found a decreasing trend in plastic consumption with age and attributed this to the fact that young turtles linger along drift-lines, where plastic accumulates. However, in the Adriatic Sea no clear age or size-related differences were apparent in loggerhead sea turtles (Caretta caretta) (Lazar and Gracan 2011; Campani et al. 2013). Schuyler et al. (2013) concludes that turtles ingest most debris during their younger oceanic life stages. Significantly higher levels of plastics were recorded in younger franciscana dolphins (Pontoporia blainvillei) off the Argentinian coast (Denuncio et al. 2011). Younger harbour seals (Phoca vitulina) in the Netherlands had significantly more plastic in their stomach than older ones (Bravo Rebolledo et al. 2013) (illustrated by Fig. 4.2). There were no differences in the plastic consumption of different age classes of cat fishes (Ariidae) from a Brazilian estuary (Possatto et al. 2011). Similarly, there was no relationship between ingested litter mass and sex, maturity and body length in deep-water blackmouth catsharks (Galeus melastomus, Anastasopoulou et al. 2013). By contrast, the mean number of plastic items ingested by planktivorous fish from the North Pacific gyre increased as the size of fish increased, reaching a maximum of seven pieces per fish for the 7-cm size class (Boerger et al. 2010). However, this may also be explained by higher plastic uptake of larger individuals during the capture process in the codend (Davison and Asch 2011). Larger individuals of the Norway lobster had fewer plastic threads in their intestines indicating higher ingestion rates of smaller/younger animals (Murray and Cowie 2011) that also have higher incidence of infaunal prey such as polychaetes (Wieczorek et al. 1999).
In summary, it seems that where age differences were shown, younger animals are most affected. The reasons for this are not clear. In seabirds, this could partly be explained by parental delivery of food by regurgitation to chicks at the nest. In such chicks, elevated loads of plastic could be the consequence of being fed by two parents, each transferring much of its own plastic load, which has accumulated in the proventricular stomach over an extended period of time before breeding. In addition, a less developed grinding action in the gizzards of young birds could slow the mechanical break-down of plastic and removal through the intestines. Some species of albatross and shearwater chicks may lose an excess load of plastic by regurgitating proventricular stomach contents prior to fledging (Auman et al. 1997; Hutton et al. 2008). However, in fulmars the high level of plastic persists in immature birds and only gradually disappears after several years (Jensen 2012) and thus cannot be completely explained by parental feeding and stomach functioning. Perhaps, young animals are less efficient at foraging, and therefore
less specific in their prey selection (Day et al. 1985; Baird and Hooker 2000; Denuncio et al. 2011). One important open question therefore is whether higher loads of plastic in younger animals reflect a learning process or mortality of those individuals that ingested too much plastic. Both explanations are speculative, but the latter suggests serious deleterious effects at the population level.
To date, there is no evidence that sex affects plastic ingestion. Studies that specifically evaluated male and female ingestion, found no signifi differences in the plastic load (e.g. Day et al. 1985; Van Franeker and Meijboom 2002; Lazar and Gracan 2011; Murray and Cowie 2011; Anastasopoulou et al. 2013; Bravo Rebolledo et al. 2013). However, species showing strong sexual dimorphy or sex-dependent foraging ranges or winter distributions may show sex-specifi uptake rates.