ReviewThe use of Hediste diversicolor in the study of emerging contaminants
Graphical abstract
Introduction
The contamination of aquatic environments has, for many years, been the focus of intense research to understand the deleterious impacts in the ecosystems (Borgwardt et al., 2019; Halpern et al., 2015). The available data points to sediments as particular targets for accumulation of contaminants and as a source of contamination throughout the food web (Herrero et al., 2018; Wilkinson et al., 2018). In this perspective, species inhabiting the sediments of reservoirs and estuaries, like polychaetes, can be valuable tools to assess the impact of contaminants including emerging contaminants of concern like pharmaceuticals, nanoparticles and small plastic particles (Lewis and Watson, 2012; Silva et al., 2020a, Silva et al., 2020b; Wilkinson et al., 2016). Recent studies have been using Hediste diversicolor as a biological model in ecotoxicity studies addressing the impact of contaminants like pharmaceuticals (Nunes et al., 2016; Pires et al., 2016a), metals, polycyclic aromatic hydrocarbons (PAHs), polychlorinated biphenyls (PCBs), pesticides (Dean, 2008; Gomiero et al., 2018) and micro(nano)plastics (Gomiero et al., 2018; Muller-Karanassos et al., 2019; Silva et al., 2020a, Silva et al., 2020b) due to their sensitivity and quick response to contamination. Oxidative stress parameters have been shown to be responsive in H. diversicolor exposed to pharmaceutical drugs, such as caffeine (Pires et al., 2016a), nanoparticles, like copper oxide nanoparticles (Buffet et al., 2012a), and microplastics, such as polyvinyl chloride (PVC) (Gomiero et al., 2018). Studies addressing the effects of silver nanoparticles (Cong et al., 2014) and nanoplastics of polystyrene (PS) (Silva et al., 2020a) demonstrated a systematic impairment in behavior, a very relevant endpoint, considering that behavioral changes may reflect alterations at lower levels of biological organization, with potential considerable impact on animal fitness and survival.
Studies have also demonstrated the effects of pharmaceutical drugs, nanoparticles and plastics on other polychaete species, such as Diopatra neapolitana and Arenicola marina. Pires et al. (2016b) reported that exposure to caffeine led to alterations in oxidative stress related enzymes, decreased glycogen content and increased cell membrane damage in D. neapolitana, whereas in A. marina only increased cell membrane damage was found. D. neapolitana exposed to carbamazepine presented a decreased regenerative capacity, as well as an increase in the number of days necessary to fully regenerate the lost segments, which was exacerbated when it was exposed to caffeine (Pires et al., 2016c).
Regarding nanoparticles, borrowing time decreased in the polychaete A. marina exposed to single walled carbon nanotubes but increased in this species when organisms were exposed to titanium dioxide nanoparticles (Galloway et al., 2010). In the polychaete Perinereis aibuhitensis exposed to polystyrene microplastics (8–12 μm and 32–38 μm), regardless of concentration (100 and 1000 beads/mL) and size tested, the regenerative capacity was reduced to half of its normal percentage (Leung and Chan, 2018).
The easy capture and maintenance in laboratory conditions and the high degree of responsivity make H. diversicolor particularly suitable for ecotoxicological studies. The present review aims to present information on laboratorial and field studies addressing the problem of environmental contamination, in terms of emerging contaminants, using H. diversicolor as the model species, emphasizing the importance of this model, relevant endpoints that may be addressed, and future applications.
Hediste diversicolor (O.F. Müller, 1776), commonly called ragworm, is a polychaete species belonging to the phylum Annelida, family Nereididae. This species lives in shallow marine and brackish water ecosystems, in muddy sands, but can also be found in gravel, clay and even turf (Scaps, 2002). H. diversicolor has a wide distribution along the North temperate zones of the Atlantic Ocean, in Europe (from Norway to Morocco, including also the Baltic, Mediterranean, Black and Caspian Seas (Fauvel, 1923; Clay, 1967; Smith, 1977; Read and Fauchald, 2020)) and the eastern North American coast (Fauvel, 1923; Clay, 1967; Smith, 1977), being also reported in the Pacific Ocean (Caribbean sea (Miloslavich et al., 2010)).
H. diversicolor reproduces only once in their lifetime and presents sexes separated throughout their life cycle (Dales, 1950; Scaps, 2002). The immature organisms have a reddish-brown color that changes to green upon maturation. Females become dark green and males have a lighter grass-green due to the production of sperm (among others Andries, 2001; Durou and Mouneyrac, 2007). These organisms reach maturity after one to two years, although in the natural environment it has been shown that individuals can live up to three years before spawning (among others Möller, 1985; Nithart, 1998). This species presents a high tolerance to salinity variations. However, at salinities lower than 10% of normal seawater salinity, osmoregulation and viability of offspring is compromised due to larval sensibility (Scaps, 2002; Smith, 1955, 1956).
H. diversicolor plays a key role in the ecosystems where it inhabits, influencing the biogeochemical cycle of nutrients, sediment oxygenation and (endo-)benthic fauna (among others Banta and Andersen, 2003; Davey, 1994; Gillet, 2012). They create U- or Y-shaped burrows, in which they live, only leaving it to search for food (Dales, 1950; Esselink and Zwarts, 1989; Kristensen and Mikkelsen, 2003). The body size and seasonal variance of water temperature influence the depth of the burrow (Esselink and Zwarts, 1989; Scaps, 2002). The ragworms are highly territorial concerning their burrows, carefully constructing them to avoid contact with others.
H. diversicolor is omnivorous and may act as a predator, actively searching for food, or as a deposit-feeder, by capturing food within the mucous secretions it produces (Fauchald and Jumars, 1979; Reise, 1979; Riisgård and Larsen, 2010). This species is highly predated by small fishes, birds, shrimps and larger crabs (Evans et al., 1979; Scaps, 2002). Predators may take only part of this animal and H. diversicolor has the ability to regenerate the posterior part of its body, as do other polychaete species (Bely, 2006). However, few studies have focused on the repercussions of environmental contamination on this capacity.
In addition to their ecological importance, H. diversicolor is also one of the polychaete species used as fish bait in recreational fishing and in aquaculture, in an integrated multitrophic approach (e.g. Pombo et al., 2018; Wang et al., 2019).
Section snippets
Ecotoxicological studies
The easy laboratorial maintenance, broad tolerance to temperature, salinity and oxygen levels, and quick response to environmental stressors, like metals, make H. diversicolor a good potential biological model for toxicological studies (e.g. Banta and Andersen, 2003; Dhainaut and Scaps, 2001; Gomes et al., 2013; Kristensen, 1983). However, so far, little is known about their response to emerging contaminants. In this context, emerging contaminants are defined as new natural or synthetic
Conclusion
In this review studies with H. diversicolor referring to nine pharmaceutical drugs, five types of nanoparticles, and five plastic polymers were analyzed. A review of the literature from 2010 to 2019 was performed using the database Scopus and using the following combination of terms: Hediste diversicolor AND drugs; Hediste diversicolor AND nanoparticles; Hediste diversicolor AND plastics. The available data does not allow comparison of the role of exposure pathways on the magnitude of effects
Declaration of competing interest
The authors declare no conflict of interest.
Acknowledgments
Thanks are due to FCT/MCTES for the financial support to CESAM (UIDP/50017/2020+UIDB/50017/2020), through national funds. AP was contracted under Decree-Law 57/2016 Art.23rd - Transitional Rule, by national funds (OE), through FCT – Fundação para a Ciência e a Tecnologia, I.P. MO had financial support of the program Investigator FCT, co-funded by the Human Potential Operational Programme and European Social Fund (IF/00335–2015). This work was also financially supported by the project BIOGEOCLIM
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