Transforming Encounters: A review of the drivers and mechanisms of macrofaunal plastic fragmentation in the environment

Abstract

Plastic has infiltrated every ecosystem on the planet, making encounters between this anthropogenic pollutant and fauna inevitable. Abiotic environmental breakdown involving light, oxygen, temperature and mechanical forces is well-characterized, while biotic degradation mechanisms are less well-understood. Reports of the role of macrofauna in the fragmentation of plastic debris are increasing. This review explores the driving factors for macrofaunal fragmentation, as well as the physiological mechanisms by which plastic items are fragmented. The presence, and access to plastic within an organism's habitat are the key determinants of macrofaunal plastic degradation. Foraging strategies, along with burrowing and nesting behaviors increase the likelihood of macrofauna interacting with plastics. Though this type of fragmentation can occur externally, it often follows ingestion, which in itself can be driven by resemblance to food. Four physical mechanisms of macrofaunal plastic fragmentation were identified, namely biting, drilling, grazing and grinding. Biting, restricted to the mouthparts of an organism, was the most common form of macrofaunal fragmentation reported in literature. Similarly, the use of specialized mouthparts for drilling or grazing can produce secondary plastic particles. Lastly, grinding, through manipulation by the gizzard or gastric mill following ingestion can significantly reduce the size of the plastic material. Prolonged and/or repeated interactions with plastics pose the risk of increased wear on the mouthparts and digestive organs involved. Through mechanisms that directly affect the plastic's structural integrity, physical fragmentation by macrofauna can amplify overall plastic degradation rates and the formation of micro-and nanoplastics in the environment, while long internal retention times can contribute to their dispersal, trophic transfer, and the organism's exposure to plastic additives. To more fully understand the extent of macrofaunal plastic fragmentation and allow predictive modeling, we suggest the reporting of evidence in a unified and systematic way. Our findings further highlight the urgency for the implementation of a global plastic waste management system to reduce the burden of micro-and nanoplastics. Impact statementAs 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 c...

Uncoupled: investigating the lack of correlation between the transcription of putative plastic-degrading genes in the global ocean microbiome and marine plastic pollution

“…Using omics, Zettler, et al [31] revealed the widespread presence of microbial communities on plastic fragments dispersed throughout the North Atlantic Ocean, and coined the term "plastisphere" to describe these man-made ecological niches. While the durability of synthetic plastics allows them to persist in marine ecosystems, they can be slowly degraded by abiotic and biotic processes [12], where they can provide a carbon source for microbial growth. Consequently, microorganisms play a pivotal role in the degradation of certain plastics and their abiotic degradation products, across diverse marine habitats [32][33][34].…”

“…They are commonly found in cosmetics, medications, and air-blasting media. Secondary microplastics are formed through the breakdown of larger plastic debris [ 11 ] via the actions of ultraviolet radiation, physical abrasion and other environmental processes [ 12 ]. Thus, environmental plastics are frequently characterised by their size.…”

Exploring the potential of earthworms to reduce microplastic pollution in soils

“…The uptake of PS NPs by edible plants (wheat and lettuce) was also demonstrated recently (Luo et al, 2022), leaving a question about the potential risks of NPs on the food safety. The drilling, rasping, and grinding activities of soil macrofauna could lead to the fragmentation of plastic debris and even certain level of degradation (Adhikari et al, 2023;Meng et al, 2023a;Rambacher et al, 2023), generating more smallsized plastic particles.…”

“…(Huerta Lwanga et al, 2017a;Heinze et al, 2021). And the drilling, rasping, and grinding activities of soil macrofauna could lead to MPs fragmentation and even certain levels of degradation (Wang et al, 2022;Adhikari et al, 2023;Meng et al, 2023a;Rambacher et al, 2023). The byproducts of these biological processes, such as smaller-sized particles and metabolites of biodegradation could be uptaken by edible plants (Luo et al, 2022) or create nutrient hotspot that affect the soil microbial community (Song et al, 2023).…”