Plastic particles and their additives promote plant invasion through physicochemical mechanisms on seed germination

Abstract

1 INTRODUCTION

Terrestrial biodiversity is rapidly decreasing as a consequence of several factors of global change, including soil pollution (IPBES, 2019). Of particular concern is pollution with microplastics (plastic particles <5 mm), which is recognized as an important threat to ecosystems worldwide (Sigmund et al., 2023). Microplastics can contaminate terrestrial systems through soil amendments, plastic mulching, irrigation, flooding, atmospheric input and littering or street run-off (Rochman et al., 2019), with both positive and negative effects on plant–soil systems (Boots et al., 2019; Huang et al., 2019). For instance, in European grasslands, the biomass of the native species Daucus carota can increase in response to the presence of microplastic films in the soil (Huang et al., 2019; Lozano, Lehnert, et al., 2021). This effect is thought to occur because plastic particles could improve soil properties such as porosity and aeration (de Souza Machado et al., 2019; Lozano, Aguilar-Trigueros, et al., 2021). By contrast, the biomass of the native species Lolium perenne may decrease (Boots et al., 2019), presumably due to toxic effects from microplastic leachates. However, not only are native plants affected by microplastics, invasive plants may potentially benefit from microplastic pollution due to traits that enhance their ability to thrive in polluted environments (Lozano & Rillig, 2024). Research shows that microplastic fibres can enhance the growth of species of invasive character such as the range-expanding species Calamagrostis epigejos (Lozano & Rillig, 2020). Microplastic beads can increase fine root biomass and photosynthesis efficiency in invasive plants compared to native species under dry–wet water cycles (Zhang et al., 2024). Also, microplastic fragments may have negligible effects on the growth of the invasive plant Solidago canadensis, while having negative effects on its native counterpart Solidago decurrens (Li et al., 2024). This advantage can be expected, as invasive species could benefit more from the novel environmental conditions created by microplastics, such as changes in soil water content, aeration, microbial activity and aggregation (de Souza Machado et al., 2019; Lozano, Aguilar-Trigueros, et al., 2021). In addition, invasive species can possess advantageous traits that might help them to avoid or better tolerate microplastic pollution (Lozano & Rillig, 2024), enabling them to thrive in human-altered environments (Montesinos, 2021), which are most likely the ones exposed to higher levels of plastic pollution. Nonetheless, microplastics can also inhibit the establishment of invasive plants like Amaranthus palmeri (Meng et al., 2023), and in some cases, they may have stronger negative effects on invasive plant biomass compared to native plants (Fu et al., 2024).

Multiple strategies such as allelopathy, herbivory and propagule pressure—closely linked with seed germination—enable invasive species to outperform native species (Bennett et al., 2011). While seed germination is critical for both native and invasive species, it plays a particular crucial role in the spread and establishment of invasive species (Daneshgar & Jose, 2009; Gioria et al., 2018). Invasive species often germinate faster and in greater proportions than native species (Guido et al., 2017; Lozano et al., 2019), with germination traits providing a key advantage in invasiveness (Moravcova et al., 2010; Palma et al., 2021). For example, species that germinate earlier can benefit from the early access to resources, space and reduced competition at initial stages of establishment (Gioria et al., 2018), which has been observed to be of greater benefit to several invasive plants in comparison to native species (Dickson et al., 2012). Additionally, synchronous germination plays a key role in the successful establishment of invasive species in novel environments (Gioria et al., 2018), as it influences not only the post-germination conditions that native or invasive specs experience, but also key processes like flowering and pollination time, which ultimately affect their growth and survival within the community, and thus their invasion potential (Gioria et al., 2018). The number of seeds that successfully germinate is another critical factor, as it directly influences plant population density and reproductive success, which is closely tied to the persistence of the seed bank in the soil—an important factor in the long-term success of invasive plant species (Gioria et al., 2021). Nonetheless, the relationship between seed germination and plant invasion is complex and can vary across different dimensions such as spread rate, local abundance or environmental range (Palma et al., 2021).

Plant invasion could be exacerbated by the current global change scenarios (Dai et al., 2022), in particular, by the presence of microplastics in the soil (Li et al., 2024). Studies of microplastic effects on seed germination either in native or invasive species are rather scarce and suggest mostly negative effects. For instance, polystyrene particles may decrease germination rate of species such as Lepidium sativum (Bosker et al., 2019; Pflugmacher et al., 2020), while having negligible effects on wheat seeds (Lian et al., 2020). Similarly, microplastics of different shapes may decrease velocity and increase synchrony of seed germination of native species like Daucus carota (Lozano et al., 2022). Whether microplastics could promote the success of invasive plant species through their effects on seed germination parameters (e.g. promoting a faster and/or synchronous germination) remains a gap in our understanding.

Microplastics could potentially alter seed germination through physical and/or chemical mechanisms, highlighting different modes of action (Lozano et al., 2022). On the one hand, there could be a physical mechanism determined by the physical presence of microplastics (i.e. particles) in the soil, which may affect initial and later stages of seed germination through the blockage of seed pores (Bosker et al., 2019), hypocotyl and/or radicle growth. However, plastic particles could improve soil properties such as porosity and aeration (de Souza Machado et al., 2019; Lozano, Aguilar-Trigueros, et al., 2021) with potential positive consequences on seed germination. On the other hand, a chemical mechanism determined by the leaching of additives and chemical substances into the soil could also affect seed germination. Toxic compounds associated with microplastics (Lithner et al., 2011) can interfere with enzyme activity, such as amylase, which is essential for germination (Sethy & Gosh, 2013), ultimately resulting in negative effects. Both physical and chemical effects have been shown to affect the root length of the aquatic plant Lemna minor (Boots et al., 2023) and the growth of Daucus carota (Lozano, Perlenfein et al., 2024). However, we have not yet disentangled physical and chemical effects of microplastics on seed germination, nor has it been determined whether they differentially affect native and invasive plant species, potentially increasing the competitive ability of invasive species.

Thus, we evaluated the individual and combined effects of plastic particles and their additives on seed germination of native and invasive species in European grasslands. We aimed to (i) disentangle the physical (particles) and chemical (additives) effects of microplastics on seed germination and (ii) determine whether microplastics might enhance seed germination of invasive species over natives. Specifically, we hypothesized that the positive physical effects of plastic particles on soil properties would overcome the negative effects of seed pore blockage, thus promoting seed germination. By contrast, we hypothesized that the chemical additives from microplastics could have toxic effects on seeds, negatively affecting seed germination. Additionally, we hypothesized that invasive species, with their unique characteristics, might be better able to exploit the novel conditions created by microplastics compared to native species. To do so, we established a microcosm experiment where plastic particles (physical effect), additives (chemical effect) and their combined effect were evaluated on germination parameters of seven plant species (native and invasive) of grasslands in Germany. We evaluated seed germination parameters such as total germination, germination velocity and germination synchrony. We also determined the chemical additives released by plastics and their potential toxicity, by using different techniques, including untargeted LC-MS and ICP-OES analyses.