With rapid marine economic development, the pollution of coastal water environments has become severe. Common environmental pollutants include heavy metals, persistent organic compounds such as polycyclic aromatic hydrocarbons (PAHs) and polychlorinated biphenyls (PCBs), and microplastics, which have recently attracted significant attention (Storelli, 2008). Heavy metals are highly toxic substances that can continuously accumulate in the bodies of living organisms, thereby causing both acute and chronic toxic effects. Many studies have reported that different degrees of heavy metal pollution have been detected within seafood in the coastal areas of China (Liu et al., 2018; Milenkovic et al., 2019; Hossain, 2020; Liu et al., 2020a; Ngoc et al., 2020; Pandion et al., 2022). Benzo[a]pyrene (B[a]P) is a common persistent organic pollutant (POP) that is widely found in aquaculture environments and has stable properties, strong toxicity, and carcinogenic effects (Quintanilla-Mena et al., 2021; Ju et al., 2022). Other studies have revealed that shellfish biomagnifies B[a]P; and high B[a]P content has been detected in various shellfish samples (Qu et al., 2019). Microplastics are a new type of environmental pollutant, and they are widely prevalent in the marine environment. Their potential to cause harm to organisms has been identified, including physical damage and the release of certain biological and chemical toxicants that result in further toxic effects, which explains why they have been extensively studied. Moreover, microplastics have a strong adsorption capacity for heavy metals, B[a]P, and other environmental pollutants, and as the particle size of microplastics is similar that of many types of fish food, it is easy to be mistakenly consumed by the aquatic animals (Chen et al., 2022). Honryo et al. (2021) reported that tuna accidentally ingested polystyrene flakes, which would accumulate in the body and affect the swimming speed and feeding of tuna. Consequently, microplastics may pose a greater safety risk than metals and organic pollutants (Sun et al., 2019). Once these environmental pollutants enter the food chain and accumulate in aquatic organisms, they will cause adverse effects on organisms and damage human health (Gao et al., 2022). Therefore, there is an urgent need for contaminant analysis of Chinese coastal marine organisms.

The seahorse is an important environmental indicator organism (Alves et al., 2013; Delunardo et al., 2015; Chipari-Gomes et al., 2017), and has an important place in ornamental aquarium (Vincent et al., 2011; Foster et al., 2016; Koning and Hoeksema, 2021). Seahorses primarily inhabit shallow coastal areas and are often found in seagrass beds, benthic algae, coral reefs, and mangroves (Barboza et al., 2020). Foster and Vincent (2004) reported that the unique life history of seahorses, such as male-pregnancy reproduction and limited moving range, increase their vulnerability to environmental change, including habitat destruction, overfishing, and marine pollution. In particular, the shallow coastal areas inhabited by seahorses are usually more susceptible to different marine contaminants (Pojana et al., 2007). Until now, little research has been reported on the presence of environmental contaminants in wild seahorses along the Chinese coast. The aim of this study was to investigate the presence and accumulation of heavy metals, B[a]P and microplastics in wild seahorse populations at different locations along the Chinese coast, and the overall results will help to improve our understanding of the accumulation of contaminants in wild seahorses along the Chinese coast.

Recent studies have shown that heavy metals, persistent organic pollutants, and microplastic pollution produce increasingly severe impacts on the marine environment. These pollutants also migrate upwards through the food chain, bioaccumulating in organisms and ultimately posing threats to human health and safety (Tang et al., 2021; Du et al., 2022). Seahorses have been labeled as a flagship species for marine conservation. However, their sensitivity to marine pollution and ability to bioaccumulate heavy metals at low levels, inhibiting growth and causing death, are of growing concern (Sun et al., 2019). Previous studies have determined that heavy metal pollution is common in most coastal areas around China (Han et al., 2021; Wang et al., 2022). Interestingly, in this study, we found that the heavy metal bioaccumulation in seahorses collected from different locations along the coastal waters of China was lower than that in majority of other marine species previously reported. We infer that this is because the smaller seahorse feeds primarily on plankton, which occupy a lower trophic niche than most carnivorous fish (Tipton and Bell, 1988), contributing to a lower cumulative efficiency. As adults, seahorses feed mainly on small crustaceans, including mysids shrimp, amphibians and other benthic crustaceans. The different seahorse populations were contaminated with Cu and Cr, which corresponds with previous studies on zooplankton (El-Metwally et al., 2022) and phytoplankton (Szymańska-Walkiewicz et al., 2022). Consistent with the experiments of Sun et al. (2019) in which the seahorse ingested heavy metals and MPs adsorbed by mysid shrimp, resulting in the accumulation of heavy metals and MPs in the seahorse and inhibition of growth. Implying that the heavy metals accumulated in the seahorses were most likely derived from food chain transmission. In addition, seahorses collected from different locations varied remarkably in their heavy metal bioaccumulation. Our results suggest that different seahorse species, which represented different life histories and micro-habitats, could contribute towards these regional variations. For example, the H. mohnikei populations prefer to live with seagrass or seaweed in shallower water, where more heavy metal pollution was observed (Khoei, 2022). The maximum differences between heavy metals (Cu and Cr) were identified between the QHD and WH populations for H. mohnikei, suggesting that regional variations in marine pollution, in addition to species, might also play a critical role in seahorse heavy metal bioaccumulation.

Our results demonstrate that microplastics accumulated in all wild seahorse populations along China’s coast; however, there were variations among different locations. Further, the significant variation of microplastic contents among three seahorse species suggests that different seahorse species are impacted differently by microplastic pollution. The surface color of MPs was mainly blue and green in seahorse intestines collected in nine cities. The reason may be that the seahorse feeds mainly on plankton and small arthropods. MPs suspended in water cause seahorses to ingest. In a recent study, the color of MPs in shrimp was determined to be predominantly blue (Yan et al., 2021). This indicates that MPs float with water and are similar in color and shape to prey. Aquatic animals may confuse blue debris or particles with prey, Ory et al. (2017) also confirmed this view. According to Bermúdez and Swarzenski (2021) micro-size plastics’ size range between 20–200μm, thus size equivalent to diatoms, dinoflagellates, ciliates, and daphnids and meso-size plastics 200–2000μm, equivalent to Amphipods, appendicularians, chetognatos, copepods, and thaliaceans. The seahorse mainly feeds on small arthropods and plankton, and MPs can accumulate in the form of food chains. This makes smaller MPs accumulate in the seahorse. In this study, the highest proportion of MPs smaller than 200μm was found in the seahorse, followed by 200-500μm and 500-1000μm. This suggests that MPs accumulate in organisms more through ingestion and food chain accumulation. In this study, there were few MPs with a size of more than 1000μm in the intestinal tract of seahorse, and no MPs with a size of more than 2000μm were found, indicating that MPs with larger particle size were not easily ingested by seahorse. We speculate that the remarkable variation in body size and depth preference might contribute towards the final differentiation among species (Choo and Liew, 2003). For example, H. mohnikei and H. trimaculatus are relatively small and prefer benthic habitats in Shallow water (Lourie et al., 2005), yet relatively high levels of MPs pollution in offshore waters greatly increase their risk of ingesting microplastics (Vroom et al., 2017). In contrast, H. kelloggi prefers to live in deeper offshore water (depths exceeding 65 m) (Choo and Liew, 2003), where fewer microplastics occur, and this species has the largest body size in the Hippocampus genus and prefers to feed on larger shrimps (Botterell et al., 2019). This suggests that aquatic organisms may directly or indirectly increase the accumulation of microplastics in organisms through food chains or food webs (Tang et al., 2021). In this study, the main polymer types detected in all seahorse intestines were PE and PA. PE is one of the main polymers in the ocean and is widely used in everyday products such as plastic packaging bags, plastic bottles and films. High strength polyethylene is widely used in the production of fishing nets and ropes (Hung et al., 2022). PA mainly used in industrial manufacturing and textiles, and is also a difficult contaminant to remove in sewage treatment (Liu and Nowack, 2022). In this experiment, the wild seahorse came from nine coastal cities, and the bay received sewage discharge from inland rivers and coastal cities. The pollution level of MPs was relatively high, and the results confirmed this finding.

B[a]P content is one of the important environmental monitoring parameters (Cirillo et al., 2006; Gaspare et al., 2009). The toxic effects of B[a]P include tissue and organ damage and reduction of immune function in fish (Banaei et al., 2008). In the present study, the B[a]P content of the three seahorse species differed considerably. The B[a]P concentrations ranged from 1.6 to 8.7 μg/kg in all samples. In general, B[a]P contamination remains at relatively low levels among the wild seahorse species inhabiting the coast of China. The results were in accordance with the findings of studies on mussels originating from the Italian Adriatic and Campania coasts (Serpe et al., 2010), while the average B[a]P levels of farmed and wild mussels inhabiting the Gulf of Naples were found much higher at 15.4 ± 2.75 μg/kg and 29.5 ± 5.83 μg/kg, respectively (Mercogliano et al., 2016). B[a]P may be released to the aquatic environment through river runoff and industrial wastewater, and the aquaculture sites in the Bay of Naples are mainly located near local commercial and industrial activities, increasing the B[a]P content in mussels. The investigation of this experiment found that the B[a]P content in the seahorse collected in LS was much higher than that in other cities. It may be speculated that the junction of LS Port and the outer sea has a narrow diameter, insufficient seawater exchange, and the pollutants have a relatively large impact on the breeding environment, which increases the accumulation of B[a]P in the seahorse. In addition, we found a highly significant positive correlation between the B[α]P content in the seahorse population and the amount of MPs in the intestinal tract in this study. This may be related to the stronger adsorption of microplastics to heavy metals and organic pollutants (Fu et al., 2019). The adsorption of microplastics to pollutants in the environment and their re-release through the food chain into the organism may produce stronger toxicological effects (Liu et al., 2020b).

Microplastics are small in volume, with a large specific surface area and a porous and rough surface, easing their co-transport with other pollutants, such as polycyclic aromatic hydrocarbons (PAHs) and heavy metals (Wright et al., 2013; Fu et al., 2019). Thus, microplastics might disturb the bioaccumulation processes of other pollutants by altering their environmental behavior, toxicity, and bioavailability (Yang et al., 2020). Interestingly, we identified a strong correlation between microplastics and B[a]P, suggesting that the accumulation of microplastics might be associated with the accumulation of B[a]P in seahorses. A previous ex situ study proved that microplastics could carry B[a]P into the digestive system of zebrafish during a 24 h feeding experiment (Batel et al., 2018). In addition, we also found significant correlations between heavy metals (Pb, Cd, Cr) and microplastics, implying that microplastics might also increase the bioaccumulation of heavy metals, which corresponds with prior seahorse feeding studies (Sun et al., 2019). In addition, the correlation between microplastics and B[a]P may be due to the fact that the seahorse living environment is influenced by multiple pollutants and there may be a synergistic accumulation effect between pollutants. Therefore, the potential effect of microplastics on wild seahorse populations might be magnified, especially when multiple contaminant types co-exist in their habitat and environment.

Our study determined that wild seahorse populations in China commonly experience environmental pollutant exposure. Species and environmental pollution concentration are critical factors affecting the bioaccumulation in seahorses from different regions. Further, the remarkable correlation between microplastics and other pollutant types suggests that the synergistic effects of these toxic substances might threaten wild seahorse populations more than previously expected.

The original contributions presented in the study are included in the article/supplementary material. Further inquiries can be directed to the corresponding author.

The animal study was reviewed and approved by Ethics Committee of Tianjin Agricultural University.

JS: conceptualization, supervision, writing - review and editing, funding acquisition. YL: formal analysis, visualization, conceptualization, software, data curation, writing - original draft. DS: investigation, methodology, writing - review and editing. YY and PC: resources, visualization. All authors contributed to the article and approved the submitted version.

This work was supported by the National Key Research and Development Program of China (Grant No. 2018YFD0900206) and the Tianjin Science and Technology Program Project (21YDTPJC00340).

Author DS was employed by Tanjin Nongken Bohai Agricultural Group Co. Ltd.

The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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