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INTRODUCTION
Metals are natural components of the envi ronment, frequently present as trace elements of continental rocks, water column, in soil, or available through food chains (Elberling et al., 2003). Some metals are essential elements in liv ing organisms, acting as cofactors for many en zymes and for stabilizing structures of proteins. Nevertheless, metal concentrations and their potential toxic effects may be anthropogenically enriched, mainly if industrial and urban wastes are discharged directly on the seabed (Loring & Asmund, 1989; Amin, 1995; Elberling et al., 2003; Prashanth et al., 2015). Metal mining ac tivities generate serious environmental prob lems due to the generally low solubility of con taminants in sea water and their accumulation, mainly in sediments with negative effects over benthic organisms living there (Elberling et al., 2003; Danis et al., 2004; Benedicto et al., 2008). Increased non-essential metals concentrations seem to reduce reproduction, behavior (Furness & Rainbow, 1990; Rhora, 2005), and have effects in skeletal morphogenesis (Temara et al., 1997) in some marine species. Consequently, marine fauna accumulate trace metals in soft body tis sues reaching higher concentrations than en vironmental levels (De Moreno et al., 1997; Vázquez et al., 2007; Idaszkin et al., 2017), while toxicity could occur when the rate of metal up take exceeds the combined rates of detoxification and excretion (Rainbow, 2007). Coastal species are more vulnerable to anthropogenic distur bances than those from offshore (Thompson et al., 2002). This is because intertidal ecosystems are more prone to direct interaction with physi cal and chemical alterations of the habitat, such as city waste discharges.
Sea stars are widely distributed around the world with ca. 1900 species grouped into 36 families (Pawson, 2007; Mah & Blake, 2012). Sea stars occupy meaningful ecological roles, such as the North Pacific Pisaster, whose influence in the structure of benthic communities on rocky shores is well known (Paine et al., 1985; Mah & Blake, 2012). In the last two decades, sea stars have been used as bioindicators in the evaluation of anthropogenic waste fluxes, such as heavy met als (Temara et al., 1998; Den Besten et al., 2001; Danis et al., 2004, 2006). High contaminant lev els by industries emissions, such as persistent or ganic pollutants, nutrients, oils and heavy metals (Islam & Tanaka, 2004), can lead to DNA damage, abnormal embryonic development, reproductive inhibition, and impaired offspring quality (Den Besten et al., 1989; Trieff et al., 1995; Au et al., 2001a, b; Yang & Xiong, 2015), which can, in turn, affect sea stars populations (Temara et al., 1998; Danis et al., 2006). Abnormalities in sea stars populations, such as deviations from pentamer ism, suggest environmental perturbations on the metamorphosis of larvae or abnormal regenera tion of arms (Hotchkiss, 2000; Kolandhasamy & Subramanian, 2012; Maheswaran et al., 2015; Arribas et al., 2017).
The oral brooding sea star Anasterias minu ta Perrier, 1875 is one of the most conspicuous macro-invertebrate top-predator species in the Atlantic Patagonian rocky shores, which preys upon a wide range of organisms (Gil & Zaixso, 2008; Brogger et al., 2013; Arribas et al., 2017). In the last fifty years, Patagonian coasts suf fered an increase in anthropogenic population, tourism, industries, and maritime traffic (Yorio et al., 2001; Commendatore & Esteves, 2007; Chomnalez, 2011; Márquez et al., 2017; Primost et al., 2017). Playas Doradas is a recreational area in Río Negro Province (Atlantic Patagonia, Argentina) located in the San Matías Gulf. The area has a mineral port, located south to the town, which used to distribute iron by ships and throw away metal wastes, as iron pellets to the marine environment (pers. obs.). Although the iron mine “Hierro Patagónico Rionegrino S.A.” (HIPARSA) is inactive since November 2016, an open-pit iron ore deposit of ca. 5 thousand tons remains near the pier of Punta Colorada (Zanettini, 2008). Therefore, the volatility of the continental dust (Paparazzo et al., 2018), such as iron deposit, added to the strong winds in the area (Genchi, 2012) could affect coast populations and ecosystem, representing a serious risk to the flo ra and fauna (Gurzau et al., 2003). Puerto Lobos was declared Natural Protected Area in 1998. It used to be an old wool jetty now used as touris tic and recreational activities related to whale, bird and sea lion watching, and artisanal fishing (Zanettini, 2008; Morsán & Ciocco, 2011).
The aim of this exploratory study was to de termine for the first time the essential and non-essential metals concentrations in gonads of the rocky intertidal sea star A. minuta from two pop ulations of different anthropogenic impact, near the iron-ore loading wharf Punta Colorada (PC) and in the Natural Protected Area Puerto Lobos (PL), located 35 km south to PC.
MATERIAL AND METHODS
Study site and sampling populations
The survey was conducted in two rocky inter tidal shores ca. 35 km separated from each other in the south of the San Matías Gulf, Atlantic Patagonia: Punta Colorada (41°42’ S - 65°1’ W, hereafter PC, Fig. 1A) near Playas Doradas town, and the Natural Protected Area Puerto Lobos (41°57’ S - 65°4’ W, hereafter PL; Fig. 1B). Both rocky outcrops belong to a group of volca nic and marine sediments with large pyroclastic contribution (Kokot et al., 2004). At PC shore, there is a 1,000 meters length ore wharf that was used to distribute iron from Sierra Grande Mine (MCC S.A.) to the dock (Zanettini, 2008), where a 1,500 meters conveyor belt can load ships with a maximum of 2,000 tons per hour. This pier was active until a few months before our survey.
Fig. 1 Sampling sites (A) Punta Colorada iron-ore loading wharf (PC) and (B) the Natural Protected Area Puerto Lobos (PL) on the SW Atlantic coast (Argentina).
Sea stars of similar size were collected from low intertidal level at PC (ca. 400 m south of pier, n = 21) and PL (ca. 35 km south of pier, n = 18) in the austral summer of 2017, when gonads reach maturity in both sexes before the brooding season (Gil et al., 2011; Pérez et al., 2015). Sea stars size (as the longest arm length R) was measured with Vernier calipers (± 0.01 mm) and weighted to calculate wet biomass (± 0.1, g m−2). Individuals were stored in refrigerated plastic containers and transported to the laboratory. Metals concentra tions were measured in Anasterias minuta dry gonads at both localities. Gonads of A. minuta were dissected and lyophilized to be digested in a Novawave microwave Digestor to quantify metal levels (μg g-1 ± SD). The measurements were made on an inductively coupled plasma optical emission spectrometer (ICP-OES) Agilent 720 (Marinho et al., 2018). To achieve the minimum recommended sample in the microwave digestor (dry weight ca. 0.5 g), a random pooled of among two and four individuals were carried out (eight and six replicates were analyzed at PC and PL, respectively).
RESULTS
Sea stars mean R size (± SD) and wet bio mass (± SD) from the population at PC was 26.1 ± 3.1 mm and 5.7 ± 1.4 g, respectively. At PL, sea stars population presented a mean R size of 24.8 ± 1.9 mm and a wet biomass of 5.3 ± 1.4 g. Sea stars collected did not show significant differences between R sizes (t-test, t= 1.89, p = 0.065) or wet biomass (t-test t = 0.76, p = 0.45) between populations at both localities.
Similar metals were found in gonads of popu lations of the sea star Anasterias minuta at both localities (Table 1). However, the essential metal Co and the non-essential metal Pb were only de tected in the gonads of the A. minuta population of the Natural Protected Area PL, and were below to the quantification limit in all gonads sampled at the iron-ore loading wharf PC. Otherwise, the essential metals Fe, Mn, Zn, Cu, Cr and Ni, and the non-essential metal Cd and As were present in gonads of both sea star populations (Table 1).
Table 1 Metal concentrations (μg g-1 ± SD) in gonads of the sea star Anasterias minuta from two populations, the pier area Punta Colorada (PC, n = 21) and the marine natural protected area Puerto Lobos (PL, n = 18). NA not available, ND below the quantification limit. * Value detected in only one simple
DISCUSSION
In our study, essential and non-essential met als were quantified in gonads of both sea star populations separated ca. 35 km away from each other. While similar metal types were found in gonads of the brooding sea star Anasterias minu ta in both populations, some metals as Co and Pb were only detected in the Natural Protected Area PL, being under the quantification limit in the iron-ore loading wharf PC. Previous studies have shown similar metal compositions with variable values of essential and non-essential metals in tissues of sea stars and their effects over echino derm populations (Den Besten et al., 1989, 2001; Flammang et al., 1997; Temara et al., 1997, 1998, 2002; Danis et al., 2004, 2006). Negative effects derived from high metal concentrations have been found in marine populations at contami nated areas, such as decrease in abundance and biomass (Menge et al., 2016), retarded embryo development (Trieff et al., 1995; Kobayashi & Okamura, 2004, 2005), and effects in DNA and enzymatic processes (Jakimska et al., 2011a). Experimental studies in the sea star Asterias rubens have shown that exposures to high con centrations of essential metals reduced righting time (Sköld et al., 2015), increased numbers of coelomocytes and proliferation of epithelial cells (Oweson et al., 2010), while increased levels of HSC70 in immune cells (Matranga et al., 2012). On the other hand, the increase of non-essential metal concentrations seem to reduce reproduc tion, behavior (Furness & Rainbow, 1990; Rhora, 2005), and have effects in skeletal morphogenesis (Temara et al., 1997) in some marine species. For example, skeletal material stiffness and tough ness of Asterina rubens decreased in Pb contami nated areas (Temara et al., 1997; Moureaux et al., 2011). Arribas et al. (2017) registered sea stars with abnormal characteristics at the PC locality, whereby deeper experimental and field studies in A. minuta are necessary to elucidate the effect of differentially increased environmental met als alongshore in sea star populations using the baseline data obtained at this work, as well as the potential use of this species as bioindicator of contamination.
Mollusks, crustaceans, and echinoderms can act as bioindicators to evaluate the availability of environmental metals. The accumulation degree in tissues depends on the properties of the species, the environmental conditions, and the level in the trophic position (Temara et al., 2002; Jakimska et al., 2011b). The accumulation of metals in the animal body is highly dependent on diet, where animals at the top of the trophic pyramid present higher metal levels in their tissues (Jakimska et al., 2011b). For example, ecotoxicologists often use mussels as bioindicator, although they do not always indicate the relationship between tissue and environmental conditions, as is the case of the asteroid Asterias rubens in Norway (Temara et al., 2002). In species such as A. minuta, which preys upon a wide range of species and the main preys depend on the environmental availability (Gil & Zaixso, 2008; Arribas et al., 2017), future research on metals accumulation should con template concentrations focus on several spe cies from the trophic chains, as recommended by Temara et al. (2002) and Jakimska et al. (2011b), and assess the availability of the metals in the environment where individuals develop (seawa ter and benthos).
Although environmental data is not available and only gonads were analyzed in the present work, this baseline information of metals in A. minuta from two localities (an anthropically im pact area and a Natural Protected Area) showed the importance of metals quantification and monitoring of different populations alongshore in a generalist or opportunistic predator species, such as A. minuta. In populations that present a brood protection reproductive strategy with low dispersal ability, as A. minuta (Salvat, 1985; Gil et al., 2011), marine contamination such as un controlled industries waste (Pearse et al., 2009) can generate aberrations during the embryonic and larval development (Den Besten et al., 1989; Trieff et al., 1995; Kobayashi & Okamura, 2004, 2005; Glynn & Colley, 2008; Pearse et al., 2009) leading to a decrease in local sea star populations, and a cascade effect in the benthic communities. More studies may strengthen the biological im plications of metal contamination on A. minuta and their ecological impact on rocky intertidal assemblages in Atlantic Patagonia.
CONCLUSIONS
Even though sea stars could be used as biomonitors of early warning signals of met al pollution and the quality of coastal waters (Temara et al., 1998, 2002), an exhaustive eco logical impact and monitoring program should be implemented in the urbanized and natural ar eas of Patagonian coasts to evaluate the health of marine organisms and their populations, which provide ecosystem services. In addition, it should be evaluated other A. minuta organs, such as pyloric caeca (detoxified storage) or the whole sea star, as well as the anatomy of the brooders, seawater and local sediments to explore relation ships between concentration detect in the biota and those in the environment.
