Microplastics contamination in pearl-farming lagoons of French Polynesia and their impacts in the pearl oyster Pinctada margaritifera

Plastic pollution of the marine environment is a global environmental, health and socio-economic issue. In French Polynesia, a specific source of plastic waste is associated with pearl-farming of which farming gears have been accumulating in the lagoons for more than 40 years. This plastic deposit is likely to degrade in micro- and nanoplastics (MNP, <5 mm), leading to an ubiquitous contamination at the global scale which is of great concern for risks to marine organisms and ecosystems. The aims of this thesis were to assess microplastics (MP) contamination in pearl-farming lagoons of French Polynesia and to investigate their effects on pearl oyster (Pinctada margaritifera). Results of sampling campaigns carried out in Ahe, Manihi and Takaroa atolls revealed the ubiquity of MP in the surface water, in the water column and the cultured pearl oysters’ tissues. The concentrations recorded in surface waters (0.2 to 8.4 MP.m-3) place these atolls at an unfavorable position compared to the microplastic concentrations measured at sea. Furthermore, the water column was found to be a highly contaminated compartment (14.0 to 716.2 MP.m-3). The pearl oyster, a filter-feeding species reared between 4 and 6 meters deep, is then particularly exposed. Concentrations measured in the tissues of P. margaritifera (~ 0.3-21.5 MP.g-1 wet weight) are among the most contaminated values in marine bivalves. In order to assess the impact of MP in P. margaritifera biology and pearl quality, two in vivo experiments were carried out under controlled laboratory conditions: one involving polystyrene microbeads (standardized micro-PS) and the other involving MNP produced from pearl-farming gears collected in situ including a low level of exposure to consider more realistic scenario. Results indicated a significant impact of micro-PS and pearlfarming MNP on the energy metabolism of exposed individuals. This alteration resulted in decreased of assimilation efficiency resulting in a dose-dependent reduction in energy gain. This energetic disruption has led to gametogenesis alteration and modulation of genes expression involved in defense mechanisms. Furthermore, the pearl quality was impacted at the microstructure level of the pearl nacre deposition. A toxicological approach conducted on pearl-farming plastic gears demonstrated their chemical toxicity potential through a significant hazardous contaminants’ desorption (e.g. phthalates) in seawater (i.e. leachates). P. margaritifera embryos were exposed to these leachates and an alteration of the embryo-larval development was observed in vitro. These results suggest that massive accumulation areas of pearlfarming gears (operational and/or discarded) could represent hotspots of chemical contaminants desorption, potentially harmful for P. margaritifera but also the surrounding biota. Overall, this thesis demonstrates a threat associated with MNP burden on the pearl oyster, the sustainability of pearl-farming industry and more broadly, on the lagoon ecosystem.La pollution plastique du milieu marin est un enjeu mondial sur le plan environnemental, sanitaire et socio-économique. En Polynésie française, une source spécifique de déchets plastiques est associée à la perliculture dont les structures d’élevage s’amoncellent dans les lagons depuis plus de 40 ans. Ce gisement de plastique est susceptible de se dégrader sous la forme de micro- et nanoplastiques (MNP, < 5 mm) dont la contamination ubiquitaire à l’échelle mondiale suscite une grande préoccupation à cause des risques qu’elle représente pour les organismes et les écosystèmes marins. Les objectifs de cette thèse étaient d’évaluer la contamination microplastique (MP) dans les lagons perlicoles de Polynésie française et d’en évaluer les effets sur l’huître perlière (Pinctada margaritifera). Les résultats des campagnes d’échantillonnages réalisées in situ dans les atolls de Ahe, Manihi et Takaroa ont révélé l’omniprésence des MP dans les eaux de surface, la colonne d’eau et les tissus d’huîtres perlières en élevage. Les concentrations enregistrées dans les eaux de surface (0,2 à 8,4 MP.m-3) placent ces trois atolls à une position très défavorable par rapport aux concentrations en MP mesurées dans le monde. De plus, la colonne d’eau s’est révélée être un compartiment hautement contaminé (14,0 à 716,2 MP.m-3). L’huître perlière, organisme filtreur élevé entre 4 et 6 mètres de profondeur, est particulièrement vulnérable à cette contamination. Les concentrations mesurées dans les tissus de P. margaritifera (~ 0,3-21,5 MP.g-1 de chair humide) la positionne d’ailleurs parmi les bivalves marins les plus contaminés. Afin d’évaluer l’impact des MP sur la biologie de P. margaritifera et la qualité de la perle, deux expérimentations in vivo ont été menées en conditions contrôlées de laboratoire : l’une impliquant des microbilles de polystyrène (micro-PS standardisées) et l’autre impliquant des MNP produits à partir de structures perlicoles récoltées in situ dont une dose d’exposition faible proche d’un scenario environnemental. Les résultats de ces travaux ont révélé un impact important des micro-PS et des MNP perlicoles sur le métabolisme énergétique des individus exposés. Cette altération s’est traduite par une diminution de l’efficacité d’assimilation entraînant une réduction dose-dépendante de gain d’énergie. Ce dérèglement énergétique s’est répercuté au niveau cellulaire (i.e. altération de la gamétogénèse) et moléculaire (i.e. modulation de l’expression des gènes impliqués dans des mécanismes de défense face au stress). Par ailleurs, la qualité de la perle s’est avérée impactée au niveau de la microstructure des dépôts nacriers. Une approche toxicologique menée en parallèle sur les plastiques perlicoles a permis de démontrer leur potentiel de toxicité chimique à travers une désorption importante d’additifs (e.g. phtalates) dans l’eau de mer (i.e. lixiviats). Des embryons de P. margaritifera ont été exposés à ces lixiviats et une altération du développement embryolarvaire a été observée in vitro. Ces résultats suggèrent que les zones d’accumulation massive de structures perlicoles en plastique (opérationnelles et/ou abandonnées) pourraient représenter des points chauds de désorption de contaminants chimiques, impactant P. margaritifera, en contact étroit avec ces équipements, mais aussi le biote environnant. Dans l’ensemble, cette thèse démontre une menace associée aux MNP qui pèse sur l’huître perlière, la durabilité de son industrie et plus largement, sur l’écosystème lagonaire

Microplastics Affect Energy Balance and Gametogenesis in the Pearl Oyster Pinctada margaritifera

Plastic pollution in the environment is increasing at global scale. Microplastics (MP) are derived from degradation of larger plastic items or directly produced in microparticles form (<5 mm). Plastics, widely used in structures and equipments of pearl farming, are a source of pollution to the detriment of the lagoon ecosystem. In order to evaluate the impact of MP on the physiology of Pinctada margaritifera, a species of ecological and commercial interests, adult oysters were exposed to polystyrene microbeads (micro-PS of 6 and 10 μm) for 2 months. Three concentrations were tested: 0.25, 2.5, 25 μg L-1 and a control. Ingestion and respiration rate and assimilation efficiency were monitored on a metabolic measurement system to determine the individual energy balance (Scope For Growth, SFG). Effects on reproduction were also assessed. The assimilation efficiency decreased significantly according to micro-PS concentration. The SFG was significantly impacted by a dose-dependent decrease from 0.25 μg L-1 (p < 0.0001). A negative SFG was measured in oysters exposed to 25 μg L-1. Gonads may have provided the missing energy to maintain animals’ metabolism through the production of metabolites derived from germ cells phagocytosis. This study shows that micro-PS significantly impact the assimilation efficiency and more broadly the energy balance of P. margaritifera, with negative repercussions on reproduction

Cryogrinding and sieving techniques as challenges towards producing controlled size range microplastics for relevant ecotoxicological tests

The impact of microplastics (MP) has attracted much attention from the scientific community and many laboratory assessments have been made of their effects on aquatic organisms. To produce MP from real environmental plastic waste, which would enable more realistic experiments, we used plastic pearl farming equipment from French Polynesian lagoons. Here, the pearl oyster Pinctada margaritifera could encounter MP coming from their breakdown in its surrounding environment. We tested an established method based on mechanical cryogenic grinding and liquid sieving. Our desired size range was 20–60 μm, corresponding to the optimal particle size ingested by P. margaritifera. The protocol was effective, generating MP particles of 20–60 μm (∼17,000–28,000 MP μg−1), but also produced too many smaller particles. The peak in the desired size range was thus flattened by the many small particles <3 μm (∼82,000–333,000 MP μg−1; 53–70% of total analysed particles), visible at the limit of Coulter counter analysis (cut-off point: 2 μm). Laser diffraction analysis (cut-off point: 0.4 μm) provided greater detail, showing that ∼80–90% of the total analysed particles were <1 μm. Diverging particle size distributions between those expected based on sieving range and those really observed, highlight the need to perform fine-scaled particle size distribution analyses to avoid underestimating the number of small micro- and nanoplastics (MNP) and to obtain an exact estimation of the fractions produced. Size and microstructure characterization by scanning electron microscopy suggested spontaneous particle self-assembly into crystal superstructures, which is the supposed cause of the divergence we observed. Overall, our results emphasize that particle self-assembly is a technical hurdle requiring further work and highlight the specific need to finely characterize the size distribution of MNP used in ecotoxicological experiments to avoid overestimating effects

Microplastics induce dose-specific transcriptomic disruptions in energy metabolism and immunity of the pearl oyster Pinctada margaritifera

A combined approach integrating bioenergetics and major biological activities is essential to properly understand the impact of microplastics (MP) on marine organisms. Following experimental exposure of polystyrene microbeads (micro-PS of 6 and 10 μm) at 0.25, 2.5, and 25 μg L−1, which demonstrated a dose-dependent decrease of energy balance in the pearl oyster Pinctada margaritifera, a transcriptomic study was conducted on mantle tissue. Transcriptomic data helped us to decipher the molecular mechanisms involved in P. margaritifera responses to micro-PS and search more broadly for effects on energetically expensive maintenance functions. Genes related to the detoxification process were impacted by long-term micro-PS exposure through a decrease in antioxidant response functioning, most likely leading to oxidative stress and damage, especially at higher micro-PS doses. The immune response was also found to be dose-specific, with a stress-related activity stimulated by the lowest dose present after a 2-month exposure period. This stress response was not observed following exposure to higher doses, reflecting an energy-limited capacity of pearl oysters to cope with prolonged stress and a dramatic shift to adjust to pessimum conditions, mostly limited and hampered by a lowered energetic budget. This preliminary experiment lays the foundation for exploring pathways and gene expression in P. margaritifera, and marine mollusks in general, under MP exposure. We also propose a conceptual framework to properly assess realistic MP effects on organisms and population resilience in future investigations

Microplastics Affect Energy Balance and Gametogenesis in the Pearl Oyster <i>Pinctada margaritifera</i>

Plastic pollution in the environment is increasing at global scale. Microplastics (MP) are derived from degradation of larger plastic items or directly produced in microparticles form (< 5 mm). Plastics, widely used in structures and equipment of pearl farming, are a source of pollution to the detriment of the lagoon ecosystem. To evaluate the impact of MP on the physiology of <i>Pinctada margaritifera</i>, a species of ecological and commercial interests, adult oysters were exposed to polystyrene microbeads (micro-PS of 6 and 10 μm) for 2 months. Three concentrations, 0.25, 2.5, and 25 μg L^–1, and a control were tested. Ingestion and respiration rate and assimilation efficiency were monitored on a metabolic measurement system to determine the individual energy balance (Scope For Growth, SFG). Effects on reproduction were also assessed. The assimilation efficiency decreased significantly according to micro-PS concentration. The SFG was significantly impacted by a dose-dependent decrease from 0.25 μg L^–1 (<i>p</i> < 0.0001), and a negative SFG was measured in oysters exposed to 25 μg L^–1. Gonads may have provided the missing energy to maintain animals’ metabolism through the production of metabolites derived from germ cells phagocytosis. This study shows that micro-PS significantly impact the assimilation efficiency and more broadly the energy balance of <i>P. margaritifera</i>, with negative repercussions on reproduction

Pearl Farming Micro-Nanoplastics Affect Oyster Physiology and Pearl Quality

International audiencePearl farming is crucial for the economy of French Polynesia. However, rearing structures contribute significantly to plastic waste, and the widespread contamination of pearl farming lagoons by microplastics has raised concerns about risks to the pearl industry. This study aimed to evaluate the effects of micro-nanoplastics (MNPs, 0.4–200 μm) on the pearl oyster (Pinctada margaritifera) over a 5-month pearl production cycle by closely mimicking ecological scenarios. MNPs were produced from weathered plastic pearl farming gear and tested at environmentally relevant concentrations (0.025 and 1 μg L–1) to decipher biological and functional responses through integrative approaches. The significant findings highlighted the impacts of MNPs on oyster physiology and pearl quality, even at remarkably low concentrations. Exposure to MNPs induced changes in energy metabolism, predominantly driven by reduced assimilation efficiency of microalgae, leading to an alteration in gene expression patterns. A distinct gene expression module exhibited a strong correlation with physiological parameters affected by MNP conditions, identifying key genes as potential environmental indicators of nutritional-MNP stress in cultured oysters. The alteration in pearl biomineralization, evidenced by thinner aragonite crystals and the presence of abnormal biomineral concretions, known as keshi pearls, raises concerns about the potential long-term impact on the Polynesian pearl industry

La perliculture de Polynésie française menacée par les microplastiques

National audienceLa pollution plastique du milieu marin est un enjeu mondial sur le plan environnemental, sanitaire et socio-économique. En Polynésie française, une source spécifique de déchets plastiques est associée à la perliculture dont les structures d’élevage s’accumulent dans les lagons depuis plus de 40 ans. Ce gisement de plastique est susceptible de se dégrader sous la forme de micro- et nanoplastiques (MNP, < 5 mm) dont la contamination ubiquitaire à l’échelle mondiale suscite une grande préoccupation à cause des risques qu’elle représente pour les organismes et les écosystèmes marins. La contamination en MP a été évaluée dans les lagons perlicoles ainsi que leurs impacts sur l’huître perlière (Pinctada margaritifera) en conditions de laboratoire. Cependant, comme la plupart des études d’impact à ce jour, ces phases d’exposition aux MP étaient limitées aux particules standards (microbilles). Afin de mieux appréhender les risques associés aux MNP, des huîtres perlières ont été exposées pendant 5 mois à des MNP produits à partir de structures perlicoles collectées in situ, à des doses prochent d’un scenario environnemental, tout en simulant le cycle de production d’une perle. Un impact sur le métabolisme énergétique de P. margaritifera a pu être observé ainsi qu’une modulation de l’expression des gènes impliqués dans la réponse immunitaire et les mécanismes de détoxification. La qualité de la perle a également été altérée au niveau de la microstructure des dépôts nacriers. Dans l'ensemble, ces résultats démontrent une menace associée aux MNP qui pèse sur l’huître perlière, la durabilité de son industrie et plus largement, sur l’écosystème lagonaire

Validation of the rapid assessment procedure for loiasis (RAPLOA) in the democratic republic of CongoS

Background: A simple method called RAPLOA, to rapidly assess what proportion of people in a community are infected with L. loa and hence which communities are at high risk of severe adverse reactions following ivermectin treatment, was developed in Cameroon and Nigeria. The method needed further validation in other geographical and cultural contexts before its application in all endemic countries. The present study was designed to validate RAPLOA in two regions in the North East and South West of the Democratic Republic of Congo. Methods: In each study region, villages were selected from different bio-ecological zones in order to cover a wide range of loiasis endemicity. In each selected community, 80 people above the age of 15 years were interviewed for a history of eye worm (migration of adult L. loa under the conjunctiva of the eye) and parasitologically examined for the presence and intensity of L. loa infection. In total, 8100 individuals from 99 villages were enrolled into the study. Results: The results confirmed the findings of the original RAPLOA study: i) the eye worm phenomenon was well-known in all endemic areas, ii) there was a clear relationship between the prevalence of eye worm history and the prevalence and intensity of L. loa microfilaraemia, and iii) using a threshold of 40%, the prevalence of eye worm history was a sensitive and specific indicator of high-risk communities. Conclusion: Following this successful validation, RAPLOA was recommended for the assessment of loiasis endemicity in areas targeted for ivermectin treatment by lymphatic filariasis and onchocerciasis control programmes

La perliculture de Polynésie française menacée par les microplastiques

National audienceLa pollution plastique du milieu marin est un enjeu mondial sur le plan environnemental, sanitaire et socio-économique. En Polynésie française, une source spécifique de déchets plastiques est associée à la perliculture dont les structures d’élevage s’accumulent dans les lagons depuis plus de 40 ans. Ce gisement de plastique est susceptible de se dégrader sous la forme de micro- et nanoplastiques (MNP, < 5 mm) dont la contamination ubiquitaire à l’échelle mondiale suscite une grande préoccupation à cause des risques qu’elle représente pour les organismes et les écosystèmes marins. La contamination en MP a été évaluée dans les lagons perlicoles ainsi que leurs impacts sur l’huître perlière (Pinctada margaritifera) en conditions de laboratoire. Cependant, comme la plupart des études d’impact à ce jour, ces phases d’exposition aux MP étaient limitées aux particules standards (microbilles). Afin de mieux appréhender les risques associés aux MNP, des huîtres perlières ont été exposées pendant 5 mois à des MNP produits à partir de structures perlicoles collectées in situ, à des doses prochent d’un scenario environnemental, tout en simulant le cycle de production d’une perle. Un impact sur le métabolisme énergétique de P. margaritifera a pu être observé ainsi qu’une modulation de l’expression des gènes impliqués dans la réponse immunitaire et les mécanismes de détoxification. La qualité de la perle a également été altérée au niveau de la microstructure des dépôts nacriers. Dans l'ensemble, ces résultats démontrent une menace associée aux MNP qui pèse sur l’huître perlière, la durabilité de son industrie et plus largement, sur l’écosystème lagonaire