Anthropogenic particles in the stomach contents and liver of the freshwater fish Squalius cephalus

Highlights

• Twenty-five percent of chubs have ingested at least one anthropogenic particle.

• Their mean length was 2.41 mm.

• Microplastic particles translocate into the liver of wild freshwater fish.

• No anthropogenic particle was found in muscle.

• There is no difference between the upstream and the downstream of Paris.

Abstract

Anthropogenic particles (APs) are a very broad category of particles produced directly or indirectly by human activities. Their ingestion by biota is well studied in the marine environment. In contrast, studies on AP ingestion in wild freshwater organisms are scarce despite high contamination levels in some rivers and lakes. In this study, we aimed to evaluate the ingestion of APs and the possible occurrence of APs in the liver and muscle of a freshwater fish, Squalius cephalus, from the Parisian conurbation. After isolation, the particles were analyzed using Raman spectroscopy. In sixty stomachs, eighteen APs were found, half of which were plastics and the other half were dyed particles. Twenty-five percent of sampled individuals had ingested at least one AP. The mean length of the APs was 2.41 mm. No significant difference was found between the sites upstream and downstream of Paris. Additionally, 5% of sampled livers contained one or more APs, which were characterized as microplastics (MPs). No APs were found in the muscle tissue. The majority of APs isolated from stomach contents were fibers, which is similar to the findings of a previous river contamination study. This highlights that fish could be more exposed to fibers than previously thought and that more studies on the impacts of fiber ingestion are required. Despite their low occurrence, MPs are reported, for the first time, in the liver of a wild freshwater fish species. While the pathways and impacts are still unknown, MPs also occur in liver of marine mollusks and fish. Physiological in vitro studies are needed to better evaluate the impacts of such phenomena.

Introduction

Anthropogenic particles (APs) are a very broad category of particles produced directly or indirectly by human activities, thus showing an anthropogenic origin. In this study, APs are defined as small pieces – fragments or fibers – with an anthropogenic origin, such as plastic, dyed particles or textile fibers, regardless of their size. All textile fibers have been handled by humans (e.g., dyed) and thus have an anthropogenic origin, regardless of whether their basic composition is natural. All seas and oceans are contaminated by APs, including plastics (Cózar et al., 2014), and so are a large number of organisms (Kühn et al., 2015). Numerous studies, reviews and books (Bergmann et al., 2015) report the extent of this phenomenon, particularly plastic pollution and its impact on marine environments. However, although marine environments have been well studied regarding APs (mainly plastics), knowledge about freshwater contamination by APs and their ecological impacts remains scarce (Dris et al., 2015b). Yet, rivers continue to be the main source of microplastics (MPs) (<5 mm, (Arthur et al., 2009)) to coastal ecosystems (Lima et al., 2014; Lebreton et al., 2017).

Several studies conducted in freshwater (Dris et al., 2015a; Faure et al., 2015), such as in the Seine River (Gasperi et al., 2014), the River Thames (Morritt et al., 2014), the Danube River (Lechner et al., 2014), the Yangtze and Hanjiang Rivers (Wang et al., 2017), the Laurentian Great Lakes (Eriksen et al., 2013) and in several Chilean rivers (Rech et al., 2014), showed that freshwater is contaminated, sometimes highly contaminated, by APs, especially plastics. Among others, a study by Lechner et al. (2014) calculated that, in the Danube River, the global plastic mass for both MPs and macroplastics was higher than the fish larvae mass. In the U.S.A., over 4 million particles are estimated to be released every day from one Californian wastewater treatment plant (Mason et al., 2016).

High AP concentrations could likely lead to their ingestion by aquatic organisms. Studies focusing on freshwater biota contamination are very scarce. Few studies mention AP or MP ingestion by wild fish species (Faure et al., 2012, Faure et al., 2015; Sanchez et al., 2014; Phillips and Bonner, 2015; Pazos et al., 2017; Silva-Cavalcanti et al., 2017; Vendel et al., 2017) or marine mammal species (Denuncio et al., 2011), and even these have focused only on stomach contents.

Aquatic organisms can suffer mechanical damage from ingestion of APs, e.g., obstruction or starvation, as has been shown in marine mammals and birds (Beck and Barros, 1991; Pierce et al., 2004; Jacobsen et al., 2010). Furthermore, aquatic organisms, including fish, can also be impacted by toxicological issues including pollutant transfer (Cedervall et al., 2012; Rochman et al., 2013; Wright and Kelly, 2017) or translocation of MPs into other organs such as the liver (Avio et al., 2015; Collard et al., 2017a).

In this study, we analyzed the ingestion of APs by the chub Squalius cephalus in two highly anthropized rivers, the Marne and the Seine Rivers, which both cross the Greater Paris Megacity. The chub has not been studied so far in the context of AP pollution despite its omnipresence in European rivers and its abundant population (Freyhof, 2014). Due to its ubiquity, the chub could be a bioindicator for AP pollution in rivers. This species has a minor economic interest, but its consumption by Europeans was at its maximum in 2011 (FAO, 2011). Adults are solitary, and juveniles are gregarious, but both are pelagic. Generally, they feed on insects, plants and crustaceans such as crayfish (Balestrieri et al., 2006; Mann, 1976; Michel and Oberdoff, 1995). However, their diet varies with age and season. In the Babuna River (Republic of Macedonia), they mainly feed on algae (Chrysophyceae) and insect larvae (Ephemeroptera and Plecoptera) in spring, on algae (Chrysophyceae) in summer and autumn and on diatoms and other insect larvae (Chironomidae) in winter (Nastova-Grorgjioska et al., 1997). Young individuals eat primarily insects (Mann, 1976), while adults generally feed on plants or crayfish and on other fish, particularly in winter (Michel and Oberdoff, 1995). Moreover, the chub adapts its diet to its habitat (Piria et al., 2005). For example, in Croatia, depending on the river, the diet -dominant components are Diptera (insects), cladocerans (Djinova, 1976 cited in Piria et al., 2005), detritus (Adamek and Obrdlik, 1977) or zoobenthos (Losos et al., 1980).

AP contamination of the Greater Paris Megacity rivers, e.g., the Seine and Marne Rivers, was studied during a 19-month period between April 2014 and December 2015, excluding January and August 2015, from upstream to downstream suburbs crossing the very dense part of the urban area (Dris et al., 2018). Because of its sprawling population (12 million inhabitants), Greater Paris exerts a high anthropogenic pressure on rivers and, therefore, is a site of great interest for assessing the ingestion of APs by Squalius cephalus. The sampling was done along the continuum of the Seine and Marne Rivers, allowing a comparison between the upstream and the downstream suburbs of Paris. Our objectives were to evaluate the ingestion of APs, including microplastics, by European chubs caught within the Parisian conurbation and to determine whether APs translocate into muscle or liver tissue in this species.