The Neglected Role of Intraspecific Variation in Plastic Pollution Research

The predominant focus of initial research endeavours investigating the impacts of ongoing climate change on biodiversity has been on studying the effects on species as the primary unit of measurement. However, over the last decade, numerous studies have taught us that neglecting intraspecific (genetic and/or phenotypic) diversity limits our understanding of the impacts that human activities have on life on Earth. Intraspecific biodiversity is a critical component of ecological systems, providing the foundation for adaptation, stability, productivity, and the long-term persistence of species and ecosystems. Evidence has demonstrated that consideration of variation below the species level is an absolute prerequisite for a comprehensive understanding of the impacts of anthropogenic pressure, the likely consequences for wider ecosystems and efficient management strategies. Plastic litter has rapidly emerged as a worldwide threat to global biodiversity. Critically, to date, akin to the initial phases of climate change research, the main emphasis of studies has primarily been on examining the effects of plastics on species as the principal metric of assessment. Studies investigating how, or to what extent, plastic pollution affects diversity below the species level are lagging. In this perspective piece, we argue that, by overlooking the role of intraspecific variation in plastic pollution research, the consequences of this new, and ever growing, ecological threat may be oversimplified and underestimated.

Since the beginning of the recent COVID-19 (SARS-CoV-2) pandemic, plastic-based personal protective equipment (PPE) and packaging have rapidly emerged as determinant safety measures to prevent the spread of the virus (e.g. Ankit et al. 2021). Concurrently, the increased use of such items and their mismanagement as waste has led to a significant increase in related plastic debris in the environment globally (de Sousa 2021; Patrício Silva et al. 2020). This recent and timely example of the conflicting advantages and drawbacks of plastics illustrates the contradictory relationship that humans have developed with this material over the last 70 years. Plastic is now used in virtually all commercial and industrial sectors and its production has grown faster than any other type of manufactured material (Geyer et al. 2017), from about 2 million metric tonnes in 1950 to ~ 368 million metric tonnes in 2019 (PlasticsEurope 2020). Of the 8.3 billion metric tonnes of plastic produced thus far, roughly 9% has been recycled, 12% incinerated and the remaining resides in dumps, landfills and the environment (PlasticsEurope 2020). The immense reservoir of plastic waste is a growing cause of concern. Inherent durability, lightweight and buoyancy allow plastic debris to persist in the environment and to disperse over long distances carried by winds and ocean currents (Alimi et al. 2018). Plastic debris has been found in atmospheric fallout (Brahney et al. 2020) and in every ecosystem that has been studied, including the most remote, uninhabited and thus presumably pristine areas of the world, such as the Arctic Ocean (Bergmann et al. 2019), Henderson Island (Lavers and Bond 2017), deep ocean trenches (Jamieson et al. 2019) and at the summit of Mount Everest .
There is now overwhelming evidence that plastic contamination of the natural environment is an increasingly common threat to terrestrial and aquatic wildlife, further contributing to the impacts of other forms of global anthropogenic disturbance, such as rising temperatures, ocean acidification and habitat loss and fragmentation (Beaumont et al. 2019;Haward 2018;Law and Thompson 2014). The issue of plastic pollution is a pressing and global environmental concern that transcends borders. The detrimental impact of plastic pollution extends to various dimensions of sustainable development, including the environment, society and economy. Plastic pollution poses a significant barrier to achieving the UN-Sustainable Development Goals (UNEA 2022) within the expected timeframe. Therefore, it is imperative to employ innovative strategies at the local, national, regional, and global levels in order to effectively combat and overcome plastic pollution (Bundela and Pandey 2022). Plastic debris can be physically and chemically harmful and can cause a variety of sub-lethal and lethal effects (e.g. see reviews in Puskic et al. 2020;Rochman 2016). The ingestion or entanglement of plastic debris may result in the suffocation, damage to locomotory, respiratory or digestive organs of organisms. More recently, other less obvious adverse effects of plastics have been highlighted. For instance, our limited but growing understanding of the insidious causes of the toxicity of leachates from plastic waste has drawn attention to several deleterious impacts, including carcinogenesis, endocrine disruption, anomalous embryonic development and behavioural impairment (eg, Seuront 2018;Wright et al. 2013).

Intraspecific variation in the context of plastic pollution is still dramatically neglected
Importantly, the effects of plastic debris can be species specific. Distinct species may respond differently to the same form of plastic pollution. Interspecific differences in response to plastic pollutions have been highlighted in recent studies even when comparing closely related and functionally equivalent species. For example, plastic leachates have distinct effects on the motion and aggregation behaviours and strength of attachment among Mytilidae mussel species (Seuront et al. 2021) and species co-existing in the same habitat display different plastic ingestion rates with potentially different accumulation and fate of plastics at different trophic levels (Cozzolino et al. 2020(Cozzolino et al. , 2021. When species with different responses to plastic pollution have key roles as ecosystem engineers, such distinctive effects can permeate beyond the individual organism, affecting the functioning of ecosystems and, potentially, the goods and services they provide to humanity (e.g. Green et al. 2016;Law 2017). Based on the standard implicit assumption that plastic pollution applies equally to all individuals across all the diversity nested within a single species, intraspecific variation (i.e. within-species variation) has been largely neglected. A limited number of recent studies have highlighted consistent inter-individual differences in plastic ingestion. For example, more active behavioural phenotypes within populations of juvenile anemonefish ingest more microplastic particles than less active individuals with potential implications at the community level (Nanninga et al. 2020). Through emerging evidence utilizing manipulative field transplant experiments and laboratory-controlled hydrodynamic simulations, the assessment of intraspecific and interspecific diversity's relative impacts on microplastic trapping in coastal biogenic habitats revealed that genetically based intraspecific phenotypic variation not only influences the extent of plastic entrapment between morphotypes of the same species but can also exert more substantial effects than interspecific differences (Cozzolino et al. 2022). In this context, a recent set of laboratory and field experiments have examined the impacts of symbiont-induced intraspecific phenotypic variation in a habitat forming species (the Mediterranean mussel Mytilus galloprovincialis) on the trapping and ingestion of microplastics ). This study unambiguously demonstrates that mussels displaying phenotypic alterations induced by symbionts displayed higher rates of microplastic ingestion and trapping in comparison to conspecifics lacking symbionts.
In the light of these recent findings and building upon the lessons learned from extensive climate change research, we stress here that it is imperative to underscore the critical role of within-species diversity in advancing the current understanding of plastic pollution. Indeed, the plethora of research conducted on climate change has informed us that considering conspecifics as ecologically equivalents, hence neglecting phenotypic and genetic variations within and among populations, is ill-advised (see, e.g. Carvalho et al. 2019;Des Roches et al. 2018, 2021. The number N Inter(climate) of studies on the effects of contemporary climate change on species distribution and abundance which considered species as homogeneous units increased exponentially from 1990 to 2022 (i.e. N Inter(climate) ∝ e 0.215t , r 2 = 0.97, p < 0.01), though a slight decrease (3%) occurred between 2021 and 2022 (Fig. 1A). In sharp contrast, comparable studies targeting intraspecific diversity lagged decades behind and, as per 2022, they are nearly two orders of magnitude less numerous (Fig. 1B). Only later research has taught us that consideration of variation below the species level is a prerequisite for a comprehensive understanding of the impacts of anthropogenic pressure. The number N Intra(climate) of these studies has demonstrated exponential growth since 2005 (i.e. N Intra(climate) ∝ e 0.25t , r 2 = 0.93, p < 0.01; Fig. 1B), noticeably at a relatively faster rate that N Inter(climate) , which may be an indication of a growing awareness of the importance of this issue in the climate change community. The state of the literature is, however, noticeably drastically different when one considers plastic pollution (Fig. 1). Specifically, the body of literature assessing the interspecific effect of plastic pollution increased at a relatively slow pace of ca. 1.2 paper per year from 1990 to 2010, before skyrocketing as a power law (N Inter(plastic) ∝ t 3.5 , r 2 = 0.98) over the last decade. Although the resolution of the rationale behind the distinct temporal patterns observed between N Inter(climate) and N Inter(plastic) lies beyond the scope of the present paper, the virtual absence of literature on the intraspecific consequences of plastic pollution-as per 2022 only 7 papers dealt with this topic (Fig. 1B)-further stresses that this field of study is only in its early infancy.

Lesson from climate change research
Variation below the species level is one of the most fundamental components of biodiversity. Traditionally, it has been addressed from an evolutionary perspective (Lewontin 1974;Skoptsov 1968). This type of variation can now be explained through a variety of evolutionary and plastic mechanisms, such as phenotypic plasticity, local adaptation and parental condition (Des Roches et al. 2018). Triggered by the relentless advance of climate change, intraspecific variation has been increasingly acquiring renewed ecological (and evolutionary) relevance. Early research investigating the effects of contemporary climate change on species distribution and abundance considered that a species typically responds to

Below species level
Species level the change as an undifferentiated entity along their entire distribution. Yet, diversity from the same species has then been shown to respond in different ways to environmental change. For instance, Northern hemisphere's most widespread conifers, Pinus spp., and other widely distributed species show differences in intraspecific response to precipitations and temperature regimes which are crucial to predict distributional changes under various climate change scenarios (e.g. Brabec et al. 2017;Kahl et al. 2021;Rehfeldt et al. 2002;Zhang et al. 2004). Differences in the response to ocean acidification among different local populations have also been reported in cold and warm-water coral species as well as in other many other calcifying organisms (Kurman et al. 2017;Parker et al. 2011;Shaw et al. 2016). Over the last decade, research-based evidence has shown how climate-induced changes observed at the species level are preceded by changes in phenotypic and genotypic composition below the species level (Baruah et al. 2019;Clements et al. 2017;Clements and Ozgul 2016). We are now becoming increasingly aware that intraspecific variation in responses can have far-reaching impacts and may influence ecosystem functions as much as variation among species and, in turn, shape the benefits provided to society (e.g. Raffard et al. 2019). Noticeably, the ecological effects of biodiversity changes can be particularly strong when occurring at high trophic levels or for ecological key species. For example, losses in genotypic and functional richness in a fish consumer can, through trophic cascades, lead to substantial top-down effects on entire food chains (Raffard et al. 2021). Intraspecific diversity in an ecological engineer mussel species has also been shown to functionally supersede interspecific diversity in shaping community structure Figs. 2, 3).
Most recently, the importance of diversity below the species level has also been tentatively addressed in biodiversity conservation procedures. For instance, freshwater priority areas identified using intraspecific genetic data from multiple species have been shown to provide more effective conservation solutions than those relying on species-level diversity (Paz-Vinas et al. 2018). Crucially, despite the lack of an explicit mention of wild species in the zero-draft released one year earlier Laikre et al. 2020), the safeguarding of the genetic diversity of all species is also now one of the milestones to be reached by 2030 listed in the Draft 1 of the Post-2020 Global Biodiversity Framework.

Conclusions
Based on the lesson learned from decades of climate change research, we stress that acknowledging the role of withinspecies diversity is fundamental to advance the state-ofthe-art of plastic pollution research. Undoubtedly, the exponentially growing number of studies addressing the issue of plastic pollution-particularly over the last decade (Fig. 1A)-has generated sufficient knowledge to justify long-term solutions and mitigations to reduce the dispersal of plastic into the environment (e.g., Prata et al. 2019). The rapidly increasing mass and number of plastic debris entering the environment, combined with the longevity of the waste already present, emphasizes how crucial it is that research efforts continue to assess the impact of plastic pollution on ecosystem functioning. This is especially timely as several significant uncertainties about the ongoing and potential future harm of plastic contamination remain (Loy et al. 2023). The recently adopted draft resolution by UNEA The UNEA draft resolution addresses two key themes: responsible consumption and production (SDG-12), and circular economy principles. It is crucial to transition towards sustainable and environmentally friendly plastic production, ensuring responsible and controlled usage that avoids littering and polluting our ecosystems and natural resources. Embracing circularity principles is also vital to prevent the accumulation of plastics in our biosphere and promote recycling, reuse and sustainable product design. The aim of the UNEA draft resolution is to promote sustainable production and consumption of plastics through measures, such as product design and environmentally sound waste management, utilizing resource efficiency and circular economy approaches (www. un. org/ pga/ 73/ plast ics/). Member states can seize this opportunity to update their policy frameworks and effectively address global plastic pollution within the proposed provisions of the resolution. Critically, this aligns with their targets for the UN-SDGs (2015-2030, the UN Decade on Ecosystem Restoration (2021-2030) and the UN Decade of Ocean Science for Sustainable Development (2021)(2022)(2023)(2024)(2025)(2026)(2027)(2028)(2029)(2030).
In this context, we stress that the critical significance of intraspecific diversity, which represents the most fundamental level of biodiversity, should be given careful consideration within international initiatives aiming to comprehensively limit the detrimental impacts of plastic pollution. Given the knowledge that we gathered over the recent decade on the relative important role of intraspecific variation in a climate change context, shifting from a species-centred focus to one that identifies intraspecific vulnerabilities to plastic pollution is pivotal to promote a realistic understanding of how this unfolding threat will affect biodiversity and to prioritize management and conservation actions. The current state of knowledge of plastic pollution impacts on a species could be either under-or over-estimated depending on which population is chosen to represent the physiological and behavioural spectra of the species in question. Mapping the tolerance over the full geographical ranges of single species is also essential to address interspecific patterns. As for interspecific biodiversity, to gain a comprehensive understanding of the effects of plastics at levels below the species, a transdisciplinary approach is essential (Seuront . This approach should consider the physicochemical properties of plastics, such as polymer composition and particle size and shape (e.g. Seuront et al. 2021Seuront et al. , 2022Zimmermann et al. 2020), their abundance in the environment (e.g. Napper and Thompson 2020) and the potential toxicity of associated leachates (i.e. the desorption of molecules that are adsorbed onto the surface of a polymer and/ or absorbed into the polymer matrix ). Finally, understanding whether the impact of plastic pollution on intraspecific diversity could affect the functioning of ecosystems and, in turn, the ecosystem services valued by society is also crucial in achieving the targets of the 2030 Agenda for Sustainable Development.