# Impact of microplastic white tide on the light and dark metabolism of the macroalgae Fucus serratus: petroleum-based vs biosourced polymers

Solène Cazalis-Henry, Seuront Laurent, Camille Delaeter, Camille Hennion, Ombeline Deplechin, Nicolas Spilmont

► To cite this version:

Solène Cazalis-Henry, Seuront Laurent, Camille Delaeter, Camille Hennion, Ombeline Deplechin, et al. Impact of microplastic white tide on the light and dark metabolism of the macroalgae Fucus serratus: petroleum-based vs biosourced polymers. Jean-Yves Reynaud; Eric Armynot du Châtelet. Short Papers from the 19th French Congress of Sedimentology, Lille, 84, Association des Sédimentologistes Français, pp.21-26, 2025, 2-907205-83-8. 10.70665/GVNU5485. hal-05005313

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# IMPACT OF MICROPLASTIC WHITE TIDE ON THE LIGHT AND DARK METABOLISM OF THE MACROALGAE *FUCUS SERRATUS*: PETROLEUM-BASED VS BIOSOURCED POLYMERS

Solène CAZALIS-HENRY<fnref n="1" />, Laurent SEURONT<fnref n="1" />,<fnref n="2" />,<fnref n="3" />, Camille DELAETER<fnref n="1" />, Camille HENNION<fnref n="1" />, Ombeline DEPLECHIN<fnref n="1" /> and Nicolas SPILMONT<fnref n="1" />

Corresponding author: solene.henry@univ-lille.fr

**Abstract:** In a context of global change, the rising intensity of extreme climatic and pollution events, particularly plastic pollution and accumulation of plastic pellets, threaten intertidal organisms' living conditions and physiology. In response to the need for reduced fossil fuel reliance and the use of potentially toxic chemical compounds, the plastics industry is developing bioplastics marketed as "biosourced" or "biodegradable." However, bioplastics often share the same environmental issues as conventional plastics. To address gaps in understanding how conventional and bioplastics affect brown algae, we studied the impact of four virgin plastic polymers —polypropylene (PP), a biosourced polypropylene with a scallop shell matrix (PPSS), a biodegradable polylactic acid (PLA), and a biodegradable biopolyester (BioP)— on CO₂ fluxes in *Fucus serratus* under massive microbead exposure. Results showed limited effects of PP, PPSS, and BioP on the algae's photosynthesis and respiration, indicating resilience to short-term plastic exposure. In contrast, PLA exposure significantly increased dark respiration rates, suggesting a metabolic stress. However, prolonged high energy demand could be detrimental to algal health and resilience. Our future research will explore the effects of these polymers in a wider ecological context, both under natural seasonal variations and/or combined with an exceptional thermal stress.

**Keywords:** Photosynthesis, respiration, pollution, bioplastic, extreme event

## 1 INTRODUCTION

Brown algae have a global distribution (Coyer et al., 2006; Raffaelli and Hawkins, 1999) and are recognized as ecosystem engineer species that drive significant ecological changes, influencing both habitats and resources available to other organisms (Bertness et al., 1999; Wernberg et al., 2010). These engineer species play a crucial role in enhancing biodiversity, primarily by creating new habitats, offering shelter from predators (Raffaelli and Hawkins, 1999) and enriching the ecosystem with organic matter (Duggins et al., 1989) through their high productivity (Mann, 1973; Birkett et al., 1998; Vadas et al., 2004). Brown algae serve as excellent models for studying how environmental factors influence photosynthesis, particularly in response to light intensity variations (Huppertz et al., 1990; Gevaert et al., 2002; Delebecq et al., 2011) and temperature changes (Davison et al., 1991; Major and Davison, 1998). Macroalgae are highly susceptible to the impacts of climate change and human activities (Pereira et al., 2015); in particular, brown algal communities have experienced significant declines, with notable shifts in their assemblages in recent years (Wernberg et al., 2011; Raybaud et al., 2013; Christie et al., 2019; de la Hoz et al., 2019).

In an era of global change, plastic contamination of the oceans is an increasingly alarming and potentially growing threat to a wide range of marine organisms (Avio et al., 2017). Coastal ecosystems are particularly impacted, ranking among the most plastic-polluted environments (Serra Gonçalves et al., 2019; Wu et al., 2022). This pollution includes macroplastic (> 5 mm), microplastics (< 5 mm) and nanoplastics (< 100 nm) items, either produced directly by industry (primary plastic) or resulting from the fragmentation of larger plastic items (secondary plastic; Cole et al., 2011; Paul-Pont et al., 2018; Delaeter et al., 2022). Nowadays, bioplastics are increasingly considered as sustainable alternatives to conventional petroleum-based plastics (European Bioplastics, 2023). These materials can be classified into three primary categories based on their origin and end-of-life characteristics: (i) petroleum-based biodegradable plastics, e.g. biopolyester (BioP); (ii) bio-based non-biodegradable plastics, e.g. biosourced polypropylene enhanced with a biological matrix, such as scallop shell (PPSS) and (iii) bio-based and biodegradable plastics, e.g. polylactic acid (PLA). While bioplastics are often presented as environmentally-friendly solutions, recent research indicates they may generate more microplastics, i.e. almost 3 times greater to what is generated by fossil fuel plastic (Yang et al., 2022) and pose adverse effects on the physiology of intertidal organisms, sometimes exceeding the impacts caused by conventional plastics (Green et al., 2016; Yokota and Mehlrose, 2020).

<footnote n="1">¹Univ. Lille, CNRS, Univ. Littoral Côte d'Opale, IRD, UMR 8187 LOG, Station Marine de Wimereux, F-59000 Lille, France</footnote>

<footnote n="2">²Department of Marine Resources and Energy, Tokyo University of Marine Science and Technology, Tokyo, Japan</footnote>

<footnote n="3">³Department of Zoology and Entomology, Rhodes University, Grahamstown 6140, South Africa</footnote>
Although there is a growing awareness of the harmful physical and chemical effects of plastics on primary photosynthetic microorganisms (e.g. Larue et al., 2021; Sánchez-Fortún et al., 2021), a significant knowledge gaps remain regarding their impact on macroalgae, especially brown algae. To the best of our knowledge, only six studies have investigated the effects of conventional micro- and nanoplastics on macroalgae (Web of Science, accessed on 4 December, 2024). Notably, only one of these studies (Zardi et al., 2024) has opportunistically focused on brown alga, despite their critical ecological role in primary production. In this context, the present study investigates the effect of an intense plastic stress corresponding to a white tide (i.e., massive concentrations of pellet spills; Galgani and Rangel-Buitrago, 2024) of four virgin plastic polymers, including a conventional non-biodegradable petrosourced polymer, polypropylene (PP), and a polymer from each category of bioplastics (i.e. PPSS, PLA and BioP) on the physiology of brown algae *Fucus serratus*.

# 2 MATERIALS AND METHODS

## 2.1 Sampling design

Individuals of *F. serratus* were collected during low tide on an intertidal rocky reef (the Fort de Croy, 50°45'47"N 1°35'59"E) located along the French shores of the eastern English Channel. The algae were subsequently acclimatized 48 hours at the laboratory in a flow-through natural seawater aquarium representative of *in situ* conditions (T = 10°C; S = 33). The organisms collected had an average exchange surface area of 48.63 ± 17.94 cm² (mean ± standard deviation), and were selected based on the absence of both reproductive cells and predation marks.

## 2.2 Experimental design

The experiment was designed to simulate intense plastic stress corresponding to a white tide of plastic pellets experienced by *Fucus serratus* during a typical half tidal cycle at the sampling site (i.e. 6h immersion with a water temperature of 10°C). Organisms were exposed to a high concentration of plastic particles equivalent to an exchange surface —to promote the standardization of the concentrations used (see Delaeter et al., 2022 for a review)— of 17,800 mm² of plastic, realistically corresponding to the white tide event that occurred along the French shores of the eastern English Channel following the accidental spillage of 8-tonne of pellets from a tanker-truck in 2016 (i.e. 20 ml L⁻¹ of polypropylene (PP); Seuront, 2018; Gravier and Haut, 2020; Seuront et al., 2021; Uguen et al., 2022). Accordingly, the concentrations used were 10 g L⁻¹ PP, 11.1 g L⁻¹ PPSS, 7.1 g L⁻¹ PLA and 14.9 g L⁻¹ BioP. For each experimental treatment (control and plastic treatments), 5 algae were used (N = 25). The algae were incubated in a 1.5 L glass jar containing 1 L of continuously oxygenated control seawater, and PP, PPSS, PLA and BIOP solutions, incubated in temperature-controlled cabinets (MIR-154, Panasonic, Japan; temperature resolution ± 0.3°C) at 10°C for 6h.

## 2.3 Fluxes measurements

The metabolism (net photosynthesis, gross photosynthesis and respiration) of *Fucus serratus* was assessed by measuring inorganic carbon fluxes under emersion in a 2-L benthic chamber connected to a closed circuit for CO₂ analysis following Migné et al. (2002). Variations in CO₂ concentration in air were measured in the chamber using a non-dispersive infrared gas analyzer (µmolC mol air⁻¹ min⁻¹; model LI-COR IRGA LI-830) and recorded at 1 s intervals during incubations lasting 5 min. Measurements were carried out at a light intensity of 850 µmol photons m⁻² s⁻¹ using two lamps (NANLITE FS-300)—representing the light intensity conditions of the study site at solar noon (9-year average; Halawi Ghosn et al., 2023)— and in darkness in order to estimate net photosynthesis (NP) and respiration (R), respectively. Between two consecutive measurements, the benthic chamber was opened to renew the ambient air. At the end of the series of experiments, the algae were dried for 48 h at 70°C to assess their dry weight (DW). CO₂ flux (µmol C gDW⁻¹ h⁻¹) was calculated by regression analysis of CO₂ concentration versus time during light and dark incubations. Gross photosynthesis (GP) was determined by using measurements of respiration and net photosynthesis (Eq. [1]).

$$GP=NP + CR \quad [1]$$

## 2.4 Statistical analyses

Graphical representation and data analyses were performed using the R 4.3.1 programming language (R Core Team, 2019). The Kruskal-Wallis (KW) test has been shown to be more robust to use than the F-test (ANOVA), particularly when the distribution assumptions of the datasets are questionable (Nwobi and Akanno, 2021). Insofar as the overall residuals of the comparisons did not follow a Normal distribution (Shapiro-Wilkson test < 0.05), the KW test was used to compare the effect of different plastic polymers on respiration, net and gross photosynthesis in *F. serratus* in multiple comparisons. A post-hoc Dunn test (Dunn, 1961) was performed where appropriate to identify treatments that differed significantly from the control.
## 3 RESULTS AND DISCUSSION

Net and gross photosynthesis (Fig. 1A and 1C) showed no significant differences between the control and various plastic treatments (p > 0.05). This result contrasts with previous studies showing that microplastics can impair the photosynthetic processes of cyanobacteria (Tetu et al., 2019) and the freshwater green microalgae *Chlamydomonas reinhardtii* (Dong et al., 2021). Similarly, prolonged exposure to 1 g L⁻¹ of polypropylene reduced the maximum net photosynthesis rates in the bare leaves of seagrass *Zostera marina* (Molin et al., 2023). Our results may hence suggest that brown intertidal algae exhibit greater resilience to plastic pollution. However, prolonged exposure may nevertheless have adverse effects on their physiological parameters and growth, which warrants the need for further investigation.

Respiration of *F. serratus* was unaffected by exposure to a massive pollution tide containing polypropylene microplastics, polypropene composed of a scallop shell matrix, and biopolyester (p > 0.05) compared to control (Fig. 1B). However, respiration increased significantly following an exposure to 7.1 g L⁻¹ of PLA (p < 0.05) compared to the control (Fig. 1B). This also contrasts with previous studies reporting that microplastic inhibit respiration in microalgae (Dong et al., 2021) and seagrass beds (Malte Molin et al., 2023). Respiration-stimulating effects have also been recorded following heavy metal exposure and were attributed to an increased demand for ATP to promote detoxification and repair processes (Meharg, 1993; Scheidegger et al., 2011; Dao and Beardall, 2016) or to compensate for a reduced supply of ATP from photophosphorylation (Ernst, 1980). Poskuta et al. (1996) also suggested that, when CO₂ fixation is inhibited, the redox equivalents generated during photosynthesis are transferred to the mitochondria where they are oxidized, intensifying respiratory electron transport. Although the mechanisms underlying the observed increase in respiration remain speculative and need to be studied in more detail, the response to exposure to the biosourced and biodegradable polymer (i.e. PLA) indicates the activation of a stress-related mechanism in *Fucus serratus*.

<figure><img src="image_2.png" /><figcaption>Figure 1. Carbon fluxes (mean ± se) measured in the benthic chamber of *Fucus serratus* (in µmol C gDW⁻¹ h⁻¹) in light (A) or in dark (B) and corresponding gross photosynthesis (C) under emersion. Letters (a or b) denote significant differences at α = 0.05.</figcaption></figure>

We observed that polylactic acid (PLA), a polymer notably commonly used in medical applications such as sutures, bone fixation materials and drug delivery devices, exhibited a more pronounced deleterious effect than conventional plastics. Similar results have been reported in studies examining the impacts of plastics on marine organisms, such as altered respiration rates in oysters and disruption of phytoplankton assemblages (Green, 2016; Yokota & Mehlrose, 2020). These results could be explained by the presumed fragility of this polymer (Casalini et al., 2019) and by the ability of bioplastics to leach their additives more easily than conventional ones (Quade et al., 2022). Although further work is needed to identify plastic pellet additives before and after lixiviation (Seuront et al., 2022) and allow us to validate this hypothesis.

## 4 CONCLUSION

Taken together, our results show that conventional microplastic particles (PP) and bioplastics (PPSS and BioP) have limited effects on both photosynthetic and respiratory performances of *Fucus serratus*, demonstrating that their ability to act as a CO₂ source or sink is unaffected and indicating relatively high resilience in the face of massive short-term plastic exposure. However, exposure to PLA significantly affected respiration rates, suggesting an increase of metabolic stress. If the increase of respiration persists over the long term, these high energy requirements can have more serious consequences for the health and resilience of these organisms. Aware of the limitations of studying exposure to a single stress, future research is needed to assess the effects of these four plastic polymers in a broader ecological context, e.g. following a heat stress event and during seasonal monitoring.

Given that PLA is considered as an alternative to one of the most widely used conventional polymers, polyethylene (PE; Ali et al., 2023), and that it is both biosourced and biodegradable, and among the most
produced biopolymers in 2021 (European Bioplastics, 2023), we propose that future plastic pollution management strategies should take into account the environmental challenges it shares with conventional petroleum-based plastics. Despite its sustainable origins, PLA's environmental behavior —in particular its degradation process and impact on ecosystems— highlights the need for further research before promoting more “environmentally-friendly solutions”.

## 5 ACKNOWLEDGMENT

The authors would like to thank Kevin Robache for his help in processing the MAREL Carnot data, and Mathilde Schapira for reviewing the manuscript. This work was financially supported by the 'Agence Nationale de la Recherche' (ANR) through the project ECUME [Project Number = ANR-22-CE06-0029]. S. Cazalis-Henry is financially supported by a PhD scholarship from the ANR ECUME and the University of Lille, France. This paper has been reviewed by Mathilde Schapira.

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