Impact statement

As plastic is found in every ecosystem of the planet, encounters between organisms and this anthropogenic pollutant are inevitable. The breakdown of plastic through exposure to environmental elements and microbes is well understood, however, the role of larger organisms in this breakdown is unclear. By systematically categorizing both drivers and aspects of encounters with plastic debris, and internal and external mechanisms directly causing plastic to fragment, this work highlights the extent of the contribution of macrofauna to the environmental fate of plastic debris. Beyond expected mechanical wear on the mouthparts and digestive tract of the animals, the resulting smaller size makes the plastic particles availability to a wider range of organisms and contribute substantially to the cycling of micro- and nanoplastics through global food webs. This work establishes the presence of plastic waste in the environment as the root cause of this form of breakdown and therefore calls for the implementation of adequate plastic waste management systems. Clearly and consistently documented findings from both laboratory studies and field observations will aid deeper understanding of the implications of this form of widespread, rapid environmental breakdown of plastic debris. Understanding the global plastic cycling processes constitutes the foundation for effective legislative measures to mitigate the risks posed by this anthropogenic pollutant.

Presence and access to plastic debris

The presence and abundance of plastic within the habitat of any organism is a key predictor of encounters and potential subsequent interactions. The accumulation of anthropogenic plastic waste initially occurs in proximity to its original source and is hence often found in and around urban centers (Barnes et al., Reference Barnes, Galgani, Thompson and Barlaz2009; Andrady, Reference Andrady2017). In a study of plastic ingestion by toads (Rhinella diptycha), lizards (Tropidurus torquatus) and geckos (Hemidactylus mabouia) in urban Paraguay where there is a lack of recycling facilities, 81 of 311 individuals contained microplastics, with clear fibers being the most abundant morphotype (Mackenzie and Vladimirova, Reference Mackenzie and Vladimirova2021). Those vulture species (Coragyps atratus, Cathartes aura) resilient to anthropogenic presence and routinely visiting garbage dumps in Patagonia had high levels of plastic contamination in their pellets (Ballejo et al., Reference Ballejo, Plaza, Speziale, Lambertucci and Lambertucci2021). Likewise, the visitation of garbage dumps has been suggested as the cause for the high number of plastic items found in the gizzards of juvenile and adult white storks (Ciconia Ciconia) in Spain (Peris, Reference Peris2003).

Within the aquatic environment, a similar pattern is observed. For example, in a study of two species of sunfish (Lepomis macrochirus; Lepomis megalotis) from a river basin in Texas, Southern US, individuals from sampling sites categorized as “urban” had the highest microplastic stomach load (Peters and Bratton, Reference Peters and Bratton2016). An analysis of preserved freshwater fish from 1900 to 2017 demonstrated microplastic ingestion began in 1950, when mass production of plastic materials started, and rose with increased societal plastic use. Interestingly, all microplastics recovered were fibers, indicative of wastewater treatment plants as the probable source of microplastics to rivers and streams (Hou et al., Reference Hou, McMahan, McNeish, Munno, Rochman and Hoellein2021). The same trend was observed in feces of the Eurasian otter (Lutra lutra), which contained microplastic of mainly fibrous-shape. As otters are a top predator in freshwater ecosystems, this observation may indicate trophic transfer of the plastic fibers (O’Connor et al., Reference O’Connor, Lally, Mahon, O’Connor, Nash, O’Sullivan, Bruen, Heerey, Koelmans, Marnell and Murphy2022).

Marine hotspots of high plastic debris abundance, like the South Pacific Gyre, can be the result of specific transport paths of anthropogenic plastic waste within the oceans, and provide conditions that lead to a high incidence of encounters of marine life with plastic (Markic et al., Reference Markic, Niemand, Bridson, Mazouni-Gaertner, Gaertner, Eriksen and Bowen2018). Remote locations such as Henderson Island in the South Pacific, where high amounts of plastic pieces accumulated in beach sediments, can act as a sink for plastic debris (Lavers and Bond, Reference Lavers and Bond2017). A study of four genera of reef-inhabiting fish (Myripristis spp., Siganus spp., Epinephelus merra, Cheilopogon simus) from around Moorea Island in French Polynesia demonstrated the ingestion of microplastic of various shapes through the presence in their digestive tracts (Garnier et al., Reference Garnier, Jacob, Guerra, Bertucci and Lecchini2019). Additionally, certain plastic products are particularly prone to improper disposal, which can then make them more likely to be encountered by wildlife, such as cigarette filters (Novotny et al., Reference Novotny, Hardin, Hovda, Novotny, McLean and Khan2011) and synthetic face masks widely used as part of the response to global Covid-19 pandemic (Patrício Silva et al., Reference Patrício Silva, Prata, Mouneyrac, Barcelò, Duarte and Rocha-Santos2021).

Behaviors driving interactions with plastic debris

Interactions of macrofauna with plastic debris are often motivated by behaviors such as burrowing and nesting, courtship, or as part of foraging activities for food and water. In a controlled laboratory experiment, earthworms (Lumbricus terrestris) were observed transporting polyethylene beads through the soil by the processes of ingestion, egestion and incorporation into their burrows (Rillig et al., Reference Rillig, Ziersch and Hempel2017). This downward transport of microplastic particles through the soil profile and deposition on the walls of the earthworms’ burrows was further observed in a mesocosm experiment (Lwanga et al., Reference Lwanga, Gertsen, Gooren, Peters, Salánki, van der Ploeg, Besseling, Koelmans and Geissen2017). Additionally, microplastics can be transported through the soil profile by adhering to the body of soil- dwelling fauna such as collembola (Folsomia candida, Proisotoma minuta) (Maaß et al., Reference Maaß, Daphi, Lehmann and Rillig2017). Damage to buried irrigation pipes by the whitefringed weevil (Naupactus leucoloma) was suggested to be driven by the animals seeking moisture (Nicholas, Reference Nicholas2010).

A range of organisms have been documented to use plastic debris as nesting materials, with an example depicted in Figure 2. This is evidenced by the elevated amounts of plastic in seabird nesting areas (Hidalgo-Ruz et al., Reference Hidalgo-Ruz, Luna-Jorquera, Eriksen, Frick, Miranda-Urbina, Portflitt-Toro, Rivadeneira, Robertson, Scofield, Serratosa, Suazo and Thiel2021) and direct incorporation of plastic into the nests of herring gulls (Larus argentatus) and great black-backed gulls (Larus marinus) (Lato et al., Reference Lato, Thorne, Fuirst and Brownawell2021), as well as Northern Gannets (Morus bassanus) (O’Hanlon et al., Reference O’Hanlon, Bond, Lavers, Masden and James2019). Incorporation of plastic debris into nesting areas is not limited to vertebrates. A nest of the solitary leafcutter bee Megachile sp., constructed solely from agricultural plastic waste, was found by Allasino et al. (Reference Allasino, Marrero, Dorado and Torretta2019). Caddisfly larvae (Lepidostoma basale) have been observed to incorporate high-density plastic particles alongside sand into their cases, resulting the cases to be less stable and presumably providing less protection against predation (Ehlers et al., Reference Ehlers, Al Najjar, Taupp and Koop2020). Hermit crabs (Diogenidae, unknown species) have been reported to use plastic items instead of natural materials for shelter (Barreiros and Luiz, Reference Barreiros and Luiz2009). Male satin bower birds (Ptilonorhynchus violaceus) decorate their bowers with blue plastic items to attract mates, and have been observed stealing these items from each other (Wojcieszek et al., Reference Wojcieszek, Nicholls, Marshall and Goldizen2006).

Figure 2. Photos of a bird’s nest containing strands of synthetic material, identified as PE and PP. Credit: Olga Pantos.

Certain feeding strategies and foraging behaviors make encounters of macrofauna with plastic more likely. Both aquatic and terrestrial scavengers have been reported to ingest small particles, for example, the Norway lobster (Nephrops norvegicus) (Cau et al., Reference Cau, Avio, Dessì, Moccia, Pusceddu, Regoli, Cannas and Follesa2020) and spotted hyaena (Crocuta crocuta) (Belton et al., Reference Belton, Cameron and Dalerum2018). Stomach contents and regurgitated materials of 34 species of seabirds evidenced that nonselective omnivorous feeders had the highest amounts of ingested plastic particles. Foraging methods in seabird species further affect the plastic load, with those species employing surface dipping and pattering having a higher rate of plastic ingestion compared to those that plunge dive to capture their prey (Ryan, Reference Ryan1987). Prey selection was also identified as a key factor driving the higher plastic ingestion rate in the surface-feeding Eastern Hooded Plovers (Thinornis cucullatus) when compared to the Australian Pied Oystercatcher (Haematopus longirostris) (Mylius et al., Reference Mylius, Lavers, Woehler, Rodemann, Keys and Rivers-Auty2023). A similar pattern was observed for feces of ducks in African freshwater systems, where filter-feeding Cape Shovelers (Spatula smithii) ingested plastics at a higher rate than species that graze on vegetation (Reynolds and Ryan, Reference Reynolds and Ryan2018).

Factors driving likelihood of plastic debris ingestion

The most common and widely used size definition for microplastics is that they are <5 mm (Arthur et al., Reference Arthur, Baker and Bamford2009), a concept based on the likelihood for ingestion by higher organisms (GESAMP, 2015). A number of factors determine the degree of attractiveness of anthropogenic plastic litter to macrofauna, and therefore the likelihood of ingestion. A field study on stranded posthatchling sea turtles suggested that ingested plastic particles in the micrometer range would resemble fish eggs in both size and diameter, and could therefore have been deliberately sought out by the animals (White et al., Reference White, Clark, Manire, Crawford, Wang, Locklin and Ritchie2018). Color and overall appearance have also previously been linked to ingestion preference in sea turtles, indicating that soft, transparent items are mistaken for jellyfish (Schuyler et al., Reference Schuyler, Hardesty, Wilcox and Townsend2012). Distinct bite marks on washed-up marine plastic debris on Hawai’i are indicative of “attacks” by various fish species, wherein blue and yellow items were most frequently affected, pointing at a color preference (Carson, Reference Carson2013). This finding is in part supported by a recent experimental study on freshwater and marine fish, where the fish had a preference for yellow, green and red color, whereas blue plastic particles ingested less frequently (Okamoto et al., Reference Okamoto, Nomura, Horie and Okamura2022). Attractiveness of plastic items can further be determined by shape, as suggested in a study by Carson, who observed bite marks on stranded debris most frequently occurring on bottle-shaped plastic objects (Carson, Reference Carson2013). Chemical cues are likewise demonstrated to illicit ingestion, such as airborne olfactory cues from in situ biofouled plastic, which had the same effect on the behavior of loggerhead sea turtles (C. caretta) as food, suggesting it is of equal attractiveness (Pfaller et al., Reference Pfaller, Goforth, Gil, Savoca and Lohmann2020). The aging of microplastics and resulting biofilm also increases the likelihood of uptake of microplastic particles by marine zooplankton. Chemical cues from the biofilm were detected by copepods (spp.) and led to a preference for ingestion of biofouled over unaged plastic particles (Vroom et al., Reference Vroom, Koelmans, Besseling and Halsband2017). In contrast, sea urchins (Paracentrotus lividus) made no distinction between biofouled plastic and a natural food source (Porter et al., Reference Porter, Smith and Lewis2019).

Mechanisms of macrofaunal plastic fragmentation

Physical mechanisms by which macrofauna fragment and degrade plastic can be divided into four major groups, as outlined in Table 1. The following paragraphs explore these mechanism groups in detail.

Table 1. Recognized evidence of macrofaunal fragmentation.

Note: Evidence derived from field observations is marked with *.

Drilling and boring

Burrowing behavior by a range of invertebrate taxa can perforate plastic items, producing microplastics and potentially weakening the structural integrity of the item. For example, holes in a Malaysian power plant’s acrylonitrile-butadiene-styrene (ABS) pipe system were caused by woodboring clams (Martesia striata) (Jenner et al., Reference Jenner, Rajagopal, Van der Velde and Daud2003). Small invertebrates including Isopoda, polychaetes and clam worms burrowing into expanded polystyrene (EPS) floats, commonly used in aquaculture, are potentially a significant source of secondary microplastics (Davidson, Reference Davidson2012; Jang et al., Reference Jang, Shim, Han, Song and Hong2018; Zheng et al., Reference Zheng, Zhu, Li, Li and Shi2023) Similarly, crabs living in EPS floats produce millions of small plastic particles by tearing the material (Zheng et al., Reference Zheng, Zhu, Li, Li and Shi2023). A terrestrial example of perforation of plastic materials by macrofauna comes from a study on the prevention of damage to polyethylene (PE) irrigation systems by the Syrian woodpecker (Dendrocopos syriacus), who has been regularly observed perforating the plastic and thereby causing economic losses (Moran et al., Reference Moran, Keidar and Wolf1980).

Biting, pecking and gnawing

There is an increasing evidence for macrofaunal interaction with plastic debris through biting, pecking and gnawing. Investigations into the source of “trimmed triangular fragments,” washed up in South China led to the hypothesis that they were caused by marine macrofauna such as pufferfish (Tetraodontida spp.) (Po et al., Reference Po, Lo, Cheung and Lai2020). Similarly, bite marks on washed-up plastic bottles in Bermuda matched with the jaws of triggerfish (Canthidermis sufflamen, Balistes capricus) and indicated that the phenomenon of fish causing physical alteration through attacking them with their teeth, is widespread (Eriksen et al., Reference Eriksen, Thiel, Lebreton, Takada and Karapanagioti2019). It is plausible that other species of corallivores are capable of causing a similar type of plastic fragmentation using their teeth. The gastrointestinal tract of wild caught parrotfish (Scaridae spp.) for example contained plastic particles, proving ingestion of plastic debris occurs within this family (Markic et al., Reference Markic, Niemand, Bridson, Mazouni-Gaertner, Gaertner, Eriksen and Bowen2018). Bite marks on marine plastic debris has further been linked to marine turtles (C. caretta, Chelonia mydas, Eretmochelys imbricata) (Eriksen et al., Reference Eriksen, Thiel, Lebreton, Takada and Karapanagioti2019). Observational studies of sea turtles, such as the loggerhead turtle (C. caretta) in the Indian Ocean have documented the ingestion and egestion of plastic items in high numbers, with more than half of the 74 individuals being affected (Hoarau et al., Reference Hoarau, Ainley, Jean and Ciccione2014). An ex vivo incubation of conventional, degradable and biodegradable plastic in gastrointestinal fluids of two sea turtle species (C. mydas, C. caretta) ruled out degradational processes within the animals’ digestive tract as a major contributor to the breakdown to any of these tested plastic materials (Müller et al., Reference Müller, Townsend and Matschullat2012). Amphipods (Orchestia gammarellus) as an example of small semi-terrestrial crustacea created bite marks on biofouled PE sheets as they were feeding on the biofilm (Hodgson et al., Reference Hodgson, Bréchon and Thompson2018).

Birds interact with plastics using their beaks. Plastic items washed up on the Dutch coast, such as EPS, had identical peck marks to those present on cuttlebones originating from the Northern Fulmar’s (Fulmarus glacialis) natural prey, sepia (Cadée, Reference Cadée2002). In insects, the ability to actively fragment polylactic acid (PLA) films has recently been observed in Caddisfly larvae (Agrypnia sp.) under laboratory conditions. Previously biofouled plastic sheets were offered with either a finite or infinite amount of leaf material, and in both cases, plastic was used alongside natural materials by the larvae to build their cases. Evidence of chewing, using their mandibles, was apparent on the plastic films, as well as the formation and release of microplastic particles >1 mm in size resulting from the larvae’s building activities (Valentine et al., Reference Valentine, Cross, Cox, Woodmancy and Boxall2022). Indeed, insects chewing through rearing containers has been documented as early as 1976: Housefly larvae (Musca domestica) and brown apple moth larvae (Epiphyas postvittana) chew through plastic bags, likely polyethylene, without apparent ingestion of any plastic material (Singh and Jerram, Reference Singh and Jerram2012). Damage to plastic items by chewing is a common phenomenon, observed, for example, in termites (Isoptera spp.), that are reported to readily chew through polyvinyl chloride (PVC), cellulose and PE (Gay and Wetherly, Reference Gay and Wetherly1969). Termites share traits of their mouthparts with other insect species such as cockroaches, grasshoppers, beetles and caterpillars, who can therefore be presumed to possess similar plastic-altering capabilities. Jaws of whitefringed weevils (Naupactus leucoloma) match puncture marks on irrigation pipes (Nicholas, Reference Nicholas2010), which have also been reported to be chewed on by a vast array of vertebrate taxa, including mice (Mus musculus), rats (Rattus rattus alexandrines, Nesokia indica, Spalax ehrenbergi), foxes (Vulpes vulpes), badgers (Meles meles), dogs (Canis familiaris) and wild boars (Sus scrofa) (Moran, Reference Moran1981).

Rasping

Feeding structures used for the scraping of algal turf off hard benthic surfaces, such as echinoderm Aristotle’s lanterns and molluscan radula, can produce miniscule plastic particles during grazing on plastics. Sea urchins (P. lividus) grazing on plastic-associated turf have been found to ingest plastic particles which they generate as they feed (Porter et al., Reference Porter, Smith and Lewis2019). They further have been observed to accumulate waterborne PS microspheres via the madreporite, followed by a translocation into organs including the gonads (Murano et al., Reference Murano, Agnisola, Caramiello, Castellano, Casotti, Corsi and Palumbo2020). Consequently, sea urchins could simultaneously be externally producing, and taking up plastic particles via two distinct routes.

Similarly, radula scraping can mechanically alter the surface structure of plastic substrates. Indentations of up to 4 mm depth have been observed on expanded polystyrene following the grazing activities of terrestrial snails (Achatina fulica) (Song et al., Reference Song, Qiu, Hu, Li, Zhang, Chen, Wu and He2020). While it may not be surprising that soft plastic materials like polystyrene (PS) foam can be physically damaged by mechanical scraping, similar grazing marks have also been seen formed by marine gastropods on hard, nonfoamed plastics such as PE and polypropylene (PP)(Weinstein et al., Reference Weinstein, Crocker and Gray2016). Grazing copepod crustacea have specially adapted mandibular gnathobase which have been found to leave characteristic indentation on the surface of plastic substrate, a process presumed to lead to the formation of small plastic particles (Reisser et al., Reference Reisser, Proietti, Shaw and Pattiaratchi2014).

Grinding and milling

Upon ingestion of plastic debris, the presence of a gizzard, or gastric mill, is often associated with reported physical alteration of the material. This specialized organ, found across different phyla, is capable of grinding or “milling” hard and indigestible food items.

In aquatic crustaceans, the gastric mill contains chitinous teeth, and can lead to the fragmentation of ingested plastic particles. Initially observed in a feeding trial involving shore crabs (Carcinus maenas), passage through the digestive tract of these animals results in a size reduction and amalgamation of PP fibers (Watts et al., Reference Watts, Urbina, Corr, Lewis and Galloway2015). In Antarctic krill (Euphausia superba), the ingestion of polyethylene (PE) microspheres under controlled conditions led to their fragmentation (Dawson et al., Reference Dawson, Kawaguchi, King, Townsend, King, Huston and Nash2018). This occurrence has been confirmed by field observations in the Norway lobster (N. norvegicus). Within the animals, particle numbers significantly increased, while particles size decreased with progression through the gastrointestinal tract. Polymer type did not influence their fragmentation (Cau et al., Reference Cau, Avio, Dessì, Moccia, Pusceddu, Regoli, Cannas and Follesa2020). In freshwater amphipods (Gammarus duebeni) the same mechanism is suggested to be, at least in part, behind their observed ability to fragment PE microspheres into nano-sized particles of various shapes (Mateos-Cárdenas et al., Reference Mateos-Cárdenas, O’Halloran, van Pelt and Jansen2020), and the gizzard in dragonfly larvae (Anax imperator) has a similar effect on ingested polyester fibers, as demonstrated in a feeding experiment (Immerschitt and Martens, Reference Immerschitt and Martens2020). Through presenting earthworms with three types of polymers mixed into soil, sand naturally occurring in soil was identified to facilitate the fragmentation of PE, whereas polyester appeared to be degraded solely by the mechanical action of the gizzard (Meng et al., Reference Meng, Lwanga, van der Zee, Munhoz and Geissen2023). In a similar experiment, surface changes such as cracks and pitting on tire rubber particles were observed after ingestion by earthworms (Sheng et al., Reference Sheng, Liu, Wang, Cizdziel, Wu and Zhou2021).

Gizzards in birds are similarly capable of physically altering ingested plastic debris: In an early study investigating the residence time of PE fed to Petrels fledgelings (Procellaria aequinoctialis), Ryan (Reference Ryan1987) measured a plastic mass loss of 1% during 12 days, although no surface changes were detected in this feeding trial. Upon ingestion by Japanese quails (Coturnix coturnix japonica), the size of aged PS fragments reduced in diameter as they transitioned from the gizzard to the intestines and feces. Furthermore, some fragments translocated into the liver of the animals had become more spheroidal, indicating both size reduction and shape alteration by an avian gizzard (de Souza et al., Reference de Souza, Freitas, Gonçalves, Marinho da Luz, da Costa Araújo, Rajagopal, Balasubramani, Rahman and Malafaia2022). In fact, one study on the digestive tract of birds has likened their gizzards to mammalian molars, as turkey gizzards enable them to crush or “pulverize” walnut shells and surgical scalpels (Feduccia, Reference Feduccia2011). Herring gulls drop larger prey items from a certain height, whereas smaller bivalve shells are swallowed whole and crushed internally (Cadée, Reference Cadée1995).

Conclusion and outlook

As outlined in this review, the mere presence of plastic debris in the environment can initiate a cascade of biologically mediated fragmentation processes, with far-reaching implications for global ecosystems. This work explored the drivers behind this presently under-studied and potentially underreported aspect of environmental material breakdown, the mechanisms by which macrofaunal fragmentation occurs, and the nature of anticipated negative effects for the individuum involved. As the rate of this form of biological fragmentation is predicted to be higher than through other degradational pathways, it can substantially contribute to the bioavailability of micro- and nanosized plastic particles to lower trophic levels, and hence facilitate their trophic transfer. Finally, macrofauna can act as spreaders of the plastic material, enhancing its dispersal and ultimately affecting the cycling of plastic debris in the environment. Encounters of macrofauna with plastic debris have therefore the potential to alter the risk profile of this class of anthropogenic pollutants significantly.

Based on these findings, our recommendations are twofold: Firstly, to better understand global patterns and allow the use of predictive models estimating size and mass reductions in plastics, we recommend that work reporting on macrofaunal fragmentation should state the resulting particle size. Documenting the physical state of plastic particles found within field-collected biota aids the understanding of the preceding interactions. To facilitate discoverability of literature, we additionally propose a unified use of the term macrofaunal fragmentation when reporting observations of plastic fragmentation through macrofauna. Finally, there is urgency in implementing adequate plastic waste management practices globally as an effective measure to prevent or at least limit macrofaunal plastic fragmentation.