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The ground beetle Parallelomorphus laevigatus is a potential indicator of trace metal contamination on the eastern coast of Sicily
Ecotoxicology and Environmental Safety 135 (2017) 183–190
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The ground beetle Parallelomorphus laevigatus is a potential indicator of trace metal contamination on the eastern coast of Sicily ⁎
Erminia Contia, , Sandro Dattilob, Giovanni Costaa, Concetto Puglisib a b
Dipartimento di Scienze Biologiche, Geologiche e Ambientali, Catania University, Via Androne 81, 95124 Catania, Italy Institute for Polymers, Composites and Biomaterials, Section of Catania, National Research Council of Italy, Via Gaifami 18, 95126 Catania, Italy
A R T I C L E I N F O
A BS T RAC T
Keywords: Carabidae Sicilian sandy shores Trace elements Industrial settlements Environmental assessment
Carabids are generally considered to be non-specialized predators, and they have been considered useful ecological indicators. They can play a key role in clarifying the route of contaminants in food webs because they are predators of small invertebrates and, in turn, part of the diet of several vertebrates. The Mediterranean species Parallelomorphus laevigatus, which so far has not been studied from an ecotoxicological point of view, is an excellent ecological indicator in sandy coastal environments. We investigated the accumulation of trace elements in Ionian populations of P. laevigatus and evaluated the transfer of metal through the food chain of the coastal ecosystem. We analyzed 15 metals, including 11 essential metals (Co, Cr, Cu, Fe, Mn, Mo, Ni, Se, Sn, V and Zn) and four toxic metals (As, Cd, Hg and Pb). Significant differences were found in metal concentration in animal tissues among sites. Our results support the existence of defense mechanisms for the studied species. High values of As, Cd, Cr, Pb, Ni, and Hg detected in the beetles from the control site can be explained by both the emission sources from the nearby industrial plants and the intense agricultural activity. The present paper shows increasing Hg concentrations in the simplified trophic web of sandy beaches and confirms the capability of this pollutant to biomagnify. Moreover, the high value of biomagnification factor (BMF) points to the severe pollution level in this protected area.
1. Introduction The trophic transfer of toxins through the food chain has increasingly become the focus of ecotoxicologists. One of the reasons for this special interest is that our species actively participates in food webs, and like any consumer, man must depend on food intake to survive. Many studies have been primarily carried out in aquatic environments, where potentially harmful substances, such as pesticides and heavy metals (i.e., mercury and hydrocarbons), are often released (e.g., Metcalf et al., 1971; Gerlach, 1981; Nriagu, 1979). Later investigations in terrestrial systems have clarified the fundamental role of soil as a sink for metals and other chemicals. Some groups of invertebrates belonging to the meso- and macrofauna have been proposed as bioindicators (Hopkin, 1989, 1990). Saprophagous animals, such as woodlice, springtails, millipedes and earthworms, are appropriate organisms to evaluate the effects of toxic substance accumulation in the soil (Hopkin et al., 1985; Gräff et al., 1997; Kale, 1988). Moreover, these invertebrates are situated at the lowest levels of terrestrial food webs, thus, they are food for several animals and a transference route for the biomagnification of contaminants in ⁎
food webs (Andréa, 2010). Among the predators that live and feed on the soil surface or within the first few centimeters of soil, the carabid beetles are considered useful ecological indicators (den Boer, 1977; Brandmayr et al., 2005; Butovsky, 1997; Butovsky et al., 1999; Lagisz and Laskowski, 2008; Schirmel et al., 2015; Simon et al., 2016). In fact, they play a key role in clarifying the route of contaminants in food webs, as they are predators of small invertebrates and, in turn, part of the diet of amphibians, reptiles, birds and small mammals (Butovsky, 2011). These animals have been studied in forest, grassland, agro-ecosystems, and even roadside habitats, to evaluate the impacts of man on terrestrial ecosystems (e.g., Andrews and Cooke, 1984; Beyer et al., 1985; Butovsky, 1994, 1995a, 1995b; Emetz and Kulmatov, 1983; Emetz and Zhulidov, 1983; Jelaska et al., 2007; Novak, 1989; Purchart and Kula, 2007; Roth, 1993; van Straalen and van Wensem, 1986). The distribution of this group of insects in all types of terrestrial habitats makes it excellent for ecotoxicological analysis. Generally, carabids are characterized as poor accumulators of heavy metals (Kramarz, 1999; Heikins et al., 2001), probably because they have a series of detoxification enzymes (Kramarz, 1999; Stone et al., 2002). In
Corresponding author. E-mail address: [email protected] (E. Conti).
http://dx.doi.org/10.1016/j.ecoenv.2016.09.029 Received 22 June 2016; Received in revised form 21 September 2016; Accepted 29 September 2016 0147-6513/ © 2016 Elsevier Inc. All rights reserved.
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coastline of Sicily, during May, July and September 2013. Ten specimens per site and per sampling day were collected by hand within 10 m of the beach, close to the shoreline. Collections took place during 20:30 to 23:30, when the animals began their surface activity. The specimens were placed individually in Falcon tubes containing sand from the collection sites and transported to the laboratory. Each individual was cleaned of sand and weighed 20 times, consecutively, using a Sartorius balance (model CPA225D), which allows the weighing of moving objects. Then, animal samples were stored at −18 °C.
addition, it was found that carnivorous ground beetles incorporate higher concentrations of non-essential metals, such as Cd and Pb (van Straalen et al., 2001), and that non-specialized predatory ground beetles accumulate less Cu and Zn than specialized predators or parasitoids (Butovsky and van Straalen, 1995). The Mediterranean species Parallelomorphus laevigatus (Fabricius) (homotypic synonym of Scarites (Parallelomorphus) laevigatus Fabricius, 1792) is a ground beetle that has not been studied from an ecotoxicological point of view. An excellent ecological indicator for sandy coastal environments (Zanella et al., 2009), it lives on sandy beaches and spends the daylight hours in an individual burrow in the sand near the shoreline. The beetle goes outside after dark and spends the night hunting mainly Talitrus saltator (Alicata et al., 1982; Caltabiano et al., 1984). P. laevigatus is widespread on the Atlantic coasts of the Mediterranean and Morocco, and along the Mediterranean basin and the western coast of the Black Sea (Magistretti, 1963). It has been the subject of several eco-ethological investigations, in different coastal sites of eastern and southern Sicily, since 1981(Caltabiano et al., 1981, 1984; Conti, 1994; Conti et al., 2004; Costa et al., 1982a, b, c; Costa et al., 1986). Thus, it was possible to identify all the details of this beetle's extraordinary ability to orient itself (Costa et al., 1986). The shoreline can be a rather hazardous habitat because often animals are in danger of falling into the water, dragged by the surf or wind, but effective behavioral adaptations allow P. laevigatus to overcome this danger. Indeed, it is able to float and quickly land thanks to a specialized swimming technique (Caltabiano et al., 1981); in addition, it reaches the shore with the shortest path, which is perpendicular to the coast line (Ferguson, 1967). During daytime, the beetle uses the solar azimuth as an orientation cue to maintain the correct direction to land according to a y-axis path (Costa et al., 1982a). It is also able to compensate for the apparent motion of the sun (Costa et al., 1982b). Nocturnal tests have also demonstrated the ability of P. laevigatus for lunar orientation (Costa et al., 1982c) and a sensitivity to the magnetic field (Conti, 1994). Frequent monitoring activity in the different sandy beaches of eastern Sicily has shown a progressive depletion of the population size of this species, in part due to human impacts (Conti et al., 2004). Moreover, it should be emphasized that the southern part of the Ionian coast of Sicily includes one of largest refining and petrochemicals industries in western Europe. Many studies have shown that this type of industrial activity (i.e., crude-oil production, transportations, and refining operations) releases several pollutants into the environment, both organic and inorganic (e.g., Mahajan, 1985; Cholakov, 2010). However, determinations of environmental pollution sources cannot exclude natural causes. Indeed, some of these sandy beaches are also influenced by the presence of Mount Etna, the tallest active volcano in Europe. It is well known that both volcanic eruptions and volcanic ash contain a large amount of toxic substances, including many trace elements, which are transported through the waterways to the sea. The primary aim of this study was to evaluate the accumulation of trace elements in Ionian populations of P. laevigatus, as yet uninvestigated. Moreover, we sought to evaluate the metal transfer through the food chain of the coastal ecosystem. Since sandhoppers are the main food of P. laevigatus, and they have been thoroughly studied from an ecotoxicological point of view (Moore and Rainbow, 1987; Rainbow et al., 1989, 1998; Rainbow and Moore, 1990; Weeks and Rainbow, 1991, 1993; Fialkowski et al., 2000, 2003, 2009; Marsden and Rainbow, 2004; Ugolini et al., 2004, 2005, 2008; Rainbow, 2006; Ungherese et al., 2010a, 2010b; Conti et al., 2016), this study will generate useful contributions on this topic.
2.2. Sampling areas For this study we selected the sites A, B, C, and D along the sandy beaches of eastern Sicily (Fig. 1). Site A was the Simeto Nature Reserve Oasis (37°24′28.605″ N, 15°5′30.046″ E), located south of the mouth of the Simeto, a major river in Sicily that runs through the volcanic territory of Mount Etna and reaches the sea a few kilometers south of the town of Catania. This reserve is very important ecologically because it is a wintering area for migratory birds. Unfortunately, the presence of many illegal houses and the proximity of a large industrial plant in Catania pose considerable risks to the natural conditions of this area, adding their negative effects to those caused by volcanic materials produced from Etna and transported to sea in the Simeto river. Site B was the Agnone Bagni (37°19′55.353″ N, 15°5′41.247″ E), a seaside resort near the small town of Agnone Bagni, approximately 20 km south of Catania and 40 km north of Syracuse. The inshore waters of this area are frequently subject to the proliferation of the green algae Ulva lactuca due to a purification problem in the San Leonardo River. Because of this, bulldozers and mechanical shovels are often used to remove the algal mass deposited onshore by the tide. Site C was the Marina di Priolo (37°8′54.473″ N, 15°13′20.581″ E), a sandy beach approximately 15 km north of Syracuse and just south of the Peninsula Magnisi, on a narrow strip of land located in the heart of the Augusta Bay known for the famous archaeological site Thapsos. This site lies only a few kilometers away from the small Priolo Bay, where the impressive industrial and petrochemical center of Priolo Gargallo (Syracuse) is located. Site D was the Vendicari Nature Reserve (36°46′45.032″ N, 15°5′39.635″ E), located approximately 40 km south of Syracuse, which has been recognized as a wetland of international importance under the Ramsar Convention of 1971 because it includes a mixture of lagoons, sand dunes, rocky coastlines and sandy beaches. The Vendicari Reserve covers roughly 1512 ha, 575 of which constitute the zone A of integral reserve and 937 zone B (the so-called prereserve), which is dedicated to agriculture, tourism and sport. We selected it as a control area because it is located approximately 100 km from Mount Etna and considered by many researchers (e.g., Fasulo et al., 2012; Cappello et al., 2015) to be unaffected by the petrochemical contamination. 2.3. Metal analysis Frozen samples were dried in an oven at 105 °C until they reached a constant weight. After being homogenized, they were mineralized with an Anton-Paar Multiwave 3000 Microwave digestion system and PTFE vessels. Then, according to EPA Method 3052 (with a different amount of acid due to the best performance of the Anton-Paar system), we added 3.5 ml of HNO3 and 1.5 ml of H2O2 to the digestion mixture. At the end of this procedure, the content of individual vessels was diluted with 2 ml of ultrapure water and filtered using Whatman 40 filters. An aliquot of 500 μl, previously taken from the filtrate and diluted to 10 ml, was further diluted to 10 ml and then subjected to the experimental analysis. After suitable calibration through the internal standard method, analyses were conducted using a Perkin Elmer ICPMS, model Nexion 300X (Perkin Elmer Inc. Waltham, Massachusetts,
2. Materials and methods 2.1. Sampling method Adult beetles were collected at four sites along the sandy, Ionian 184
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using the Pearson r coefficient. In significant cases, a subsequent analysis with linear regression was performed. All the data were log transformed (natural logarithms) to achieve a normal distribution necessary for the parametric statistical analysis. The normality was tested with a Shapiro-Wilk test and the homogeneity of variance with a Levene's test. A one-way ANOVA was used to test for differences in metal concentrations in the animal tissues from the study sites. Post-hoc comparisons were conducted using the Tukey HSD method (Sokal and Rohlf, 2012). Finally, to assess the possible transfer of each metal through the food chain, we carried out a two-way ANOVA with the metal concentration as the dependent variable and the site and trophic level (prey, predator) as factors. In regards to the prey, as above specified, we used the data reported for Talitrus saltator by Conti et al. (2016). Statistical analyses were performed using SPSS for Windows (version 18.0). We considered p < 0.05 for the assessment of statistical significance. Finally, we calculated the transfer trophic coefficient (TTC), as the ratio of the metal concentration in the beetles to that in its prey, and considered it indicative of the biomagnification factor (BMF) when it was greater than 1 for the four toxic metals investigated.
U.S.A.), according to EPA Method 6020. For this investigation, we selected 16 target metals, 11 of which are essential elements for living organisms (Co, Cr, Cu, Fe, Mn, Mo, Ni, Se, Sn, V and Zn) and four of which are toxic (As, Cd, Hg and Pb). The results were normalized with blanks of mineralization and measurement, so the values are reported in mg/kg, taking into account the amount of sample and the multiple dilutions made prior to the analysis. Each determination was performed three times. The accuracy of the analytical procedure was confirmed by measuring a standard reference material, Nist 1566B oyster tissue in three replicates with a range of recovery between 96% and 102%, without observing any appreciable difference. 2.4. Statistical analysis At each site, the mean concentration and standard deviation of each metal in the beetle tissues was calculated. In addition, we also took into account the data relating to samples of the amphipod Talitrus saltator, the favorite prey of P. laevigatus, and the sand collected from the sites at the same time (Conti et al., 2016). The bioaccumulation of each metal in the animals was compared to the metal concentrations in the sand and beetles, and in the beetles and amphipods, using a Wilcoxon signed-rank test. We also tested the correlations between the metal concentration in the sand and carabids, as well as in the carabids and sandhoppers,
3. Results The mean and standard deviation of metal concentrations in the
Fig. 1. Map of the sampling sites; the Simeto Nature Reserve Oasis (A), the Agnone Bagni (B), the Marina di Priolo (C), and the Vendicari Nature Reserve (D).
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content in the prey and y the metal content in the predator:
Table 1 Mean trace metal concentrations (mg/kg) ± SD in Parallelomorphus laevigatus for the sampling sites A, B, C, and D.. Metal
A
B
C
D
As Cd Co Cr Cu Fe Hg Mn Mo Ni Pb Se Sn V Zn
1.03 ± 0.13 0.33 ± 0.05 0.35 ± 0.02 0.62 ± 0.06 20.67 ± 1.09 104.11 ± 38.80 0.38 ± 0.01 17.37 ± 0.43 0.57 ± 0.02 0.35 ± 0.05 0.27 ± 0.003 0.75 ± 0.69 0.16 ± 0.02 0.27 ± 0.06 107.06 ± 6.24
1.06 ± 0.10 0.09 ± 0.002 0.59 ± 0.05 0.23 ± 0.02 15.39 ± 0.65 129.56 ± 43.54 0.16 ± 0.01 12.48 ± 0.55 0.40 ± 0.03 0.46 ± 0.06 0.53 ± 0.01 0.76 ± 0.67 0.05 ± 0.02 0.16 ± 0.02 78.45 ± 4.27
0.98 ± 0.08 0.30 ± 0.02 0.16 ± 0.005 0.48 ± 0.02 15.73 ± 0.21 95.09 ± 61.90 0.53 ± 0.02 18.55 ± 0.40 0.66 ± 0.01 0.34 ± 0.03 0.17 ± 0.004 0.53 ± 0.41 0.05 ± 0.03 0.24 ± 0.02 116.21 ± 1.05
1.89 ± 0.17 1.04 ± 0.06 0.17 ± 0.008 0.69 ± 0.02 16.26 ± 0.39 57.87 ± 19.61 1.10 ± 0.04 6.83 ± 0.18 0.32 ± 0.02 0.84 ± 0.06 0.63 ± 0.003 1.24 ± 0.61 0.27 ± 0.02 0.15 ± 0.03 92.40 ± 1.58
y = 1 . 004x + 1. 541 Moreover, the TTC was 5.01 for Hg, and less than 1 for As, Cd and Pb. 4. Discussion As predators, ground beetles are a potential bioaccumulator of high metal concentrations in the tissues of their prey. However, Hopkin (1989) highlighted that carabids have suitable mechanisms for detoxification, such as the removal of whole degenerated cells, exocytosis, and extrusion of metal-containing vesicles into the lumen of the digestive tract. Moreover, Janssen et al. (1991) and Kramarz (1999) found rapid metal excretion in this group. Both of these mechanisms
tissues of P. laevigatus (mg/kg dry weight) are given in Table 1. At site D, numerous elements (e.g., As, Cd, Cr, Hg, Ni, Pb, Se and Sn) were present at the highest values, while Fe and Mn were at the lowest values. It should also be noted that Cu and V are more abundant in the specimens from site A, Co and Fe from site B, and Mn, Mo and Zn from site C. The mean metal content decreased in the following sequence, Zn (98.53 mg/kg), Fe (96.66 mg/kg), Cu (17.01 mg/kg), Mn (13.81 mg/ kg), As (1.24 mg/kg), Se (0.82 mg/kg), Hg (0.54 mg/kg), Cr (0.51 mg/ kg), Ni (0,50 mg/kg), Mo (0.49 mg/kg), Cd (0.44 mg/kg), Pb (0.40 mg/ kg), Co (0.32 mg/kg), V (0.21 mg/kg), Sn (0.13 mg/kg). The concentration of these metals in the tissues of P. laevigatus differed among the four sites. Nevertheless, a one-way ANOVA showed significant differences among the metal concentrations in the beetles only for Hg (F =7.585, p < 0.01), Cd (F=6.190, p < 0.05) and Se (F=6.004, p < 0.05). The post-hoc comparisons clarified that these differences were due to the Hg (p < 0.01) and Cd (p < 0.05) concentrations at sites B and D, and the Se (p < 0.05) concentrations at sites C and D sites (Fig. 2). The Wilcoxon signed-rank test showed significantly higher concentration of Cd (p=0.003), Cu (p=0.003), Hg (p=0.003), Mo (p=0.005), and Zn (p=0.003) in the beetles than in the sand. Conversely, the metal concentration was greater in the sand than in the animal tissues for As (p=0.003), Co (p=0.008), Cr (p=0.003), Fe (p=0.003), Mn (p=0.003), Ni (p=0.01), Pb (p=0.004), Se (p=0.003), and V (p=0.003). By applying the Wilcoxon signed-rank test to the data presented in Conti et al. (2016) for the amphipod Talitrus saltator, we were able to determine that only mercury has a concentration greater in the beetle than in its prey (p=0.003). The two-way ANOVA proved that the different metal concentrations were dependent on the trophic niche of animals for As (F=37.001; p < 0.001), Cr (F=8.547; p < 0.01), Cu (F=20.415; p < 0.001), Ni (F=14.188; p < 0.01) and Se (F=31.414; p < 0.001). The differences were due to the main effects (e.g., the trophic niche and the site) for Cd (F=8.722; p < 0.01 and F=8.572; p < 0.01), Co (F=14.440; p < 0.01 and F=5.279; p < 0.01), Fe (F=22.936; p < 0.001 and F=4.870; p < 0.05), Hg (F=50.270; p < 0.001 and F=14.951; p < 0.001) and V (F=18.919; p < 0.001 and F=3.897; p < 0.05). For Mn, the differences were dependent not only on the trophic niche of the animals (F=10.551; p < 0.01) and the site (F=7.722; p < 0.01) but also on their interactions (F=3.760; p < 0.05) (i.e., the concentration of this metal differed among sites in a different way for the prey and predator) (Fig. 3). No correlation was found between the concentration of metals in the animal tissues and sand. The correlation analysis of the metal concentrations in P. laevigatus and its favorite prey (Table 2) was significant only for Hg (r=0.80, p < 0.01). The linear regression of this metal (Fig. 4) has the following equation, with x being the metal
Fig. 2. Mean concentrations of trace metal expressed as ln(mg/kg) in the animal tissues at the sampling sites (A–D). The letter (a–c) indicates a difference at the p < 0.05 level according to post-hoc comparisons. Only metals that contribute to the statistical differences are shown.
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Fig. 3. Two-way ANOVA plots of the predator (continuous line) and prey (dashed lines) at each sampling site, A, B, C, and D. The toxic metals underlying the statistical differences and Mn are shown. Table 2 Correlation between the metal concentration in Parallelomorphus laevigatus (predator) and Talitrus saltator (prey) collected at the four Sicilian sites; r is the Pearson coefficient value and P is the statistical significance. Metal
r
P
As Cd Co Cr Cu Fe Hg Mn Mo Ni Pb Se Sn V Zn
−0.06 0.52 0.24 −0.13 0.43 0.40 0.80 0.40 0.24 0.002 −0.31 0.01 −0.02 0.32 0.39
0.86 0.10 0.47 0.70 0.19 0.23 0.03 0.22 0.48 1.00 0.36 0.98 0.96 0.34 0.23
allow these ground beetles to avoid significant metal poisoning (Butovsky and van Straalen, 1995; Hunter et al., 1987; Janssen et al., 1991; Kramarz and Laskowski, 1997; Lagisz et al., 2005; Lindquist et al., 1995). Our data on P. laevigatus supports the existence of defense mechanisms in this never before investigated species. Indeed, the two-way ANOVA showed that the metal content in animal tissues was always higher in the prey than in the predators, except for mercury. Few ecotoxicological investigations, however, have been conducted on species of ground beetles inhabiting coastal systems. To our knowledge, P. laevigatus is the first psammo-halophilous species used for this purpose. Moreover, unlike most Carabidae which are generally
Fig. 4. Linear regression for Hg in predator and prey.
considered non-specialized predators, P. laevigatus is a specialized predator on sandhoppers (Alicata et al., 1982; Caltabiano et al., 1984; Audisio and Vigna Taglianti, 2010). Furthermore, the environment where this insect lives is very special. The strip of beach next to the shoreline is a transitional habitat between two very different systems, the sea and the land, which affect each other. This mutual influence doubles the chances of habitat pollution, as toxicants from the sea (e.g., chemicals of industrial origin, and oil spills) end up on the beach and chemicals from land (e.g., pesticides and fertilizers) end up in the sea. 187
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allowed living organisms to adequately adapt. The situation in the southern area is very different. The industrial plant of Priolo dates back to the early 1950s. The main contamination of Augusta Bay, due to overboard discharge of various metals, including mercury, occurred in the 1970s (Ausili et al., 2008). Anthropogenic pollution makes it difficult for animals to adapt to such quick, massive changes in their habitat. Therefore, we are currently unable to predict what the long-term consequences of mercury accumulation means for the future of this species and the entire food web. However, it has been hypothesized that the mercury pollution generated in Augusta basin is spreading through the Mediterranean Sea (Sprovieri et al., 2011) and may cause serious problems for living organisms and marine ecological balances, even at great distances from the place of the original pollution. In addition, pollutants such as mercury biomagnify in the food web. For example, the presence of large amounts of Hg in fish in the basin of Augusta has been detected (Bonsignore et al., 2013) and the implications of this threat to human health are easily predictable. In conclusion, this paper confirms that ground beetles are potential indicators of anthropogenic stress, which has been suggested for different ecosystems by various authors (e.g., Butovsky, 2011; Ribera et al., 2001; Schirmel et al., 2015; Simon et al., 2016).
The concentrations of Cd, Cu, Mo, Hg and Zn were higher in the carabids that in the sand, which leads us to hypothesize a possible dermal absorption of these elements from the soil. Brunsting and Heessen (1984) asserted that in beetles the dermal absorption of soil pollutants is restricted to the larval phase, while in adults metal transfer only comes from the prey to the predator. Similarly, we believe that the intake of metals in adult P. laevigatus takes place only through the food chain. Indeed, Conti et al. (2016) showed that in the same habitats studied here, the trace metals were bioaccumulated in adults of T. saltator and transferred to their predators. The high values of As, Cd, Cr, Pb, Ni and Hg detected in beetles from site D, are likely from the emissions sources of the nearby industrial plants, such as the Priolo settlement, which is located 30 miles away from Vendicari (Mudu et al., 2014). In regards to cadmium, there is also intense agricultural activity in the pre-reserve part of site D that explains the high concentration of that metal both in the prey (Conti et al., 2016) and the predators. Indeed, many sources of phosphate in fertilizers contain cadmium, which can lead to an increased concentration of this metal both in the soil and water (Jensen and Bro-Rasmussen, 1992, Van Assche and Ciarletta, 1992). Furthermore, data on the high concentration of Hg in insect tissues from site D are not surprising. In fact, Ausili et al. (2008), when analyzing the sediments, the mussel Mytilus galloprovincialis and the red mullet Mullus barbatus, collected from various locations in the petrochemical area between Augusta and Priolo, detected such elevated concentrations of mercury that this site was identified as the most polluted in the Mediterranean. Subsequently, various authors (e.g., Sprovieri et al., 2011, Di Leonardo et al., 2014) have considered this area to be a mercury point-source for the entire Mediterranean Sea. Longo et al. (2013) found a high presence of this metal in the tissues of Ligia italica, a woodlouse present at the Vendicari Reserve. These authors interpreted this anomalous presence to be the result of pollution from the industrial plant of Priolo, transported south by sea currents. The present paper shows increasing Hg concentrations throughout the simplified trophic web of sandy beaches and confirms the capability of this pollutant to biomagnificate, as evident from both the two-way ANOVA and the correlation analyses. Moreover, the high value of BMF (approximately 5) confirms the severe pollution level even in this protected area. It is noteworthy that site C, which was closest to the industrial area of Priolo, was less influenced by the metal pollution coming from the petrochemical plant. This is due to the protective barrier of the Peninsula Magnisi. Some elements, such as Mn, Mo and Zn, can reach that site only by being carried with ash particles, rather than from the sea. Iron, cobalt, cuprum and vanadium are some of the most significant metals present in volcanic emissions (Cimino and Ziino, 1983; Cimino et al., 1984; Toscano et al., 2008). Their massive presence at sites A and C is probably from the outflow of the Simeto river and its tributaries, which transports a mixture of volcanic materials and materials resulting from the river’s erosive action to the sea. The Ionian sandy coast of Sicily can be divided into a northern region (sites A and B), where there is the influence of Mount Etna, and a southern region (sites C and D), where there is the anthropogenic influence. Both conditions can cause metal pollution, however, of these two, the most dangerous seems to be the man-made one. The Etnean volcanic activity began approximately 570,000 years ago and has continued rather steadily with degassing and ash emissions from summit craters. Many of trace metals measured (i.e., Fe, Mn, V, Zn and Cr) are present in lava soil and volcanic ash, causing sand contamination (Taylor and Lichte, 1980; Okamoto et al., 1997; Cimino and Toscano, 1998; Toscano et al., 2008; Ochota et al., 2012; Baturin et al., 2013; Orecchio et al., 2016). With its long-term contribution of heavy metals to the environment, the volcano has
Declaration and contribution All authors declare that this work described has not been published previously neither it is under consideration for publication elsewhere. All authors approve the publication of MS on Ecotoxicology and Environmental Safety and that, if accepted, it will not be published elsewhere in the same form, in English or in any other language, including electronically without the written consent of the copyrightholder. Authors participated in the present study as follows: Erminia Conti and Giovanni Costa performed the field sampling, prepared the samples and conducted the statistical analysis; Concetto Puglisi and Sandro Dattilo carried out analytical analysis for detecting metal concentration in animal tissues All the authors contributed in drafting the manuscript. All authors read and approved the final manuscript. Acknowledgments We would like to thank the Ministry of University and Scientific Research (MIUR) of Italy and the National Council of Research (CNR) of Italy for financial support. We especially thank the associate editor and the anonymous reviewers for providing constructive critiques of the manuscript. References Alicata, P., Caruso, D., Costa, G., Marcellino, I., Motta, S. and Petralia, A. 1982. Studi eco-etologici su artropodi delle dune costiere di Portopalo (Siracusa, Sicilia). Quaderni sulla struttura delle zoocenosi terrestri. C.N.R. Roma. 3. Ambienti mediterranei. I. Le coste sabbiose, 159–183. Andréa, M.M., 2010. O uso de minhocas como bioindicadores de contaminação de solos. Acta Zool. Mex. 2, 95–107, (n.s.). Andrews, S.M. and Cooke, J.A. 1984. Cadmium within a contaminated grassland ecosystem established on a metalliferous mine waste. In: Osborn D. (Ed) Metals in animals. Symposium N 12, Institute of Terrestrial Ecology. Abbots Ripton, pp. 11– 15. Audisio, P. and Vigna Taglianti, A. 2010. Insecta Coleoptera. Biol. Mar. Medit. 17 (Suppl. 1), 547–571. Ausili, A., Gabellini, M., Cammarata, G., Fattorini, D., Debenedetti, M., Pisanelli, B., Gorbi, S., Regoli, F., 2008. Ecotoxicological and human health risk in a petrochemical district of southern Italy. Mar. Environ. Res. 66, 215–217. Baturin, G.N., Dubinchuk, V.T., Manewich, T.M., 2013. Species of graphite, phosphorus, and some heavy metals in volcanic ashes. Dokl. Earth Sci. 451 (I), 770–774. Beyer, W.N., Pattee, O.,H., Sileo, L., Hoffman, D.J., Mulhern, B.M., 1985. Metal contamination in wildlife living near two zinc smelters. Environ. Pollut. 38A, 63–86. den Boer, P.J., 1977. Dispersal power and survival. Misc. Pap. Landbouw. Wagen.. 14,
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The ground beetle Parallelomorphus laevigatus is a potential indicator of trace metal contamination on the eastern coast of Sicily ⁎
Erminia Contia, , Sandro Dattilob, Giovanni Costaa, Concetto Puglisib a b
Dipartimento di Scienze Biologiche, Geologiche e Ambientali, Catania University, Via Androne 81, 95124 Catania, Italy Institute for Polymers, Composites and Biomaterials, Section of Catania, National Research Council of Italy, Via Gaifami 18, 95126 Catania, Italy
A R T I C L E I N F O
A BS T RAC T
Keywords: Carabidae Sicilian sandy shores Trace elements Industrial settlements Environmental assessment
Carabids are generally considered to be non-specialized predators, and they have been considered useful ecological indicators. They can play a key role in clarifying the route of contaminants in food webs because they are predators of small invertebrates and, in turn, part of the diet of several vertebrates. The Mediterranean species Parallelomorphus laevigatus, which so far has not been studied from an ecotoxicological point of view, is an excellent ecological indicator in sandy coastal environments. We investigated the accumulation of trace elements in Ionian populations of P. laevigatus and evaluated the transfer of metal through the food chain of the coastal ecosystem. We analyzed 15 metals, including 11 essential metals (Co, Cr, Cu, Fe, Mn, Mo, Ni, Se, Sn, V and Zn) and four toxic metals (As, Cd, Hg and Pb). Significant differences were found in metal concentration in animal tissues among sites. Our results support the existence of defense mechanisms for the studied species. High values of As, Cd, Cr, Pb, Ni, and Hg detected in the beetles from the control site can be explained by both the emission sources from the nearby industrial plants and the intense agricultural activity. The present paper shows increasing Hg concentrations in the simplified trophic web of sandy beaches and confirms the capability of this pollutant to biomagnify. Moreover, the high value of biomagnification factor (BMF) points to the severe pollution level in this protected area.
1. Introduction The trophic transfer of toxins through the food chain has increasingly become the focus of ecotoxicologists. One of the reasons for this special interest is that our species actively participates in food webs, and like any consumer, man must depend on food intake to survive. Many studies have been primarily carried out in aquatic environments, where potentially harmful substances, such as pesticides and heavy metals (i.e., mercury and hydrocarbons), are often released (e.g., Metcalf et al., 1971; Gerlach, 1981; Nriagu, 1979). Later investigations in terrestrial systems have clarified the fundamental role of soil as a sink for metals and other chemicals. Some groups of invertebrates belonging to the meso- and macrofauna have been proposed as bioindicators (Hopkin, 1989, 1990). Saprophagous animals, such as woodlice, springtails, millipedes and earthworms, are appropriate organisms to evaluate the effects of toxic substance accumulation in the soil (Hopkin et al., 1985; Gräff et al., 1997; Kale, 1988). Moreover, these invertebrates are situated at the lowest levels of terrestrial food webs, thus, they are food for several animals and a transference route for the biomagnification of contaminants in ⁎
food webs (Andréa, 2010). Among the predators that live and feed on the soil surface or within the first few centimeters of soil, the carabid beetles are considered useful ecological indicators (den Boer, 1977; Brandmayr et al., 2005; Butovsky, 1997; Butovsky et al., 1999; Lagisz and Laskowski, 2008; Schirmel et al., 2015; Simon et al., 2016). In fact, they play a key role in clarifying the route of contaminants in food webs, as they are predators of small invertebrates and, in turn, part of the diet of amphibians, reptiles, birds and small mammals (Butovsky, 2011). These animals have been studied in forest, grassland, agro-ecosystems, and even roadside habitats, to evaluate the impacts of man on terrestrial ecosystems (e.g., Andrews and Cooke, 1984; Beyer et al., 1985; Butovsky, 1994, 1995a, 1995b; Emetz and Kulmatov, 1983; Emetz and Zhulidov, 1983; Jelaska et al., 2007; Novak, 1989; Purchart and Kula, 2007; Roth, 1993; van Straalen and van Wensem, 1986). The distribution of this group of insects in all types of terrestrial habitats makes it excellent for ecotoxicological analysis. Generally, carabids are characterized as poor accumulators of heavy metals (Kramarz, 1999; Heikins et al., 2001), probably because they have a series of detoxification enzymes (Kramarz, 1999; Stone et al., 2002). In
Corresponding author. E-mail address: [email protected] (E. Conti).
http://dx.doi.org/10.1016/j.ecoenv.2016.09.029 Received 22 June 2016; Received in revised form 21 September 2016; Accepted 29 September 2016 0147-6513/ © 2016 Elsevier Inc. All rights reserved.
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coastline of Sicily, during May, July and September 2013. Ten specimens per site and per sampling day were collected by hand within 10 m of the beach, close to the shoreline. Collections took place during 20:30 to 23:30, when the animals began their surface activity. The specimens were placed individually in Falcon tubes containing sand from the collection sites and transported to the laboratory. Each individual was cleaned of sand and weighed 20 times, consecutively, using a Sartorius balance (model CPA225D), which allows the weighing of moving objects. Then, animal samples were stored at −18 °C.
addition, it was found that carnivorous ground beetles incorporate higher concentrations of non-essential metals, such as Cd and Pb (van Straalen et al., 2001), and that non-specialized predatory ground beetles accumulate less Cu and Zn than specialized predators or parasitoids (Butovsky and van Straalen, 1995). The Mediterranean species Parallelomorphus laevigatus (Fabricius) (homotypic synonym of Scarites (Parallelomorphus) laevigatus Fabricius, 1792) is a ground beetle that has not been studied from an ecotoxicological point of view. An excellent ecological indicator for sandy coastal environments (Zanella et al., 2009), it lives on sandy beaches and spends the daylight hours in an individual burrow in the sand near the shoreline. The beetle goes outside after dark and spends the night hunting mainly Talitrus saltator (Alicata et al., 1982; Caltabiano et al., 1984). P. laevigatus is widespread on the Atlantic coasts of the Mediterranean and Morocco, and along the Mediterranean basin and the western coast of the Black Sea (Magistretti, 1963). It has been the subject of several eco-ethological investigations, in different coastal sites of eastern and southern Sicily, since 1981(Caltabiano et al., 1981, 1984; Conti, 1994; Conti et al., 2004; Costa et al., 1982a, b, c; Costa et al., 1986). Thus, it was possible to identify all the details of this beetle's extraordinary ability to orient itself (Costa et al., 1986). The shoreline can be a rather hazardous habitat because often animals are in danger of falling into the water, dragged by the surf or wind, but effective behavioral adaptations allow P. laevigatus to overcome this danger. Indeed, it is able to float and quickly land thanks to a specialized swimming technique (Caltabiano et al., 1981); in addition, it reaches the shore with the shortest path, which is perpendicular to the coast line (Ferguson, 1967). During daytime, the beetle uses the solar azimuth as an orientation cue to maintain the correct direction to land according to a y-axis path (Costa et al., 1982a). It is also able to compensate for the apparent motion of the sun (Costa et al., 1982b). Nocturnal tests have also demonstrated the ability of P. laevigatus for lunar orientation (Costa et al., 1982c) and a sensitivity to the magnetic field (Conti, 1994). Frequent monitoring activity in the different sandy beaches of eastern Sicily has shown a progressive depletion of the population size of this species, in part due to human impacts (Conti et al., 2004). Moreover, it should be emphasized that the southern part of the Ionian coast of Sicily includes one of largest refining and petrochemicals industries in western Europe. Many studies have shown that this type of industrial activity (i.e., crude-oil production, transportations, and refining operations) releases several pollutants into the environment, both organic and inorganic (e.g., Mahajan, 1985; Cholakov, 2010). However, determinations of environmental pollution sources cannot exclude natural causes. Indeed, some of these sandy beaches are also influenced by the presence of Mount Etna, the tallest active volcano in Europe. It is well known that both volcanic eruptions and volcanic ash contain a large amount of toxic substances, including many trace elements, which are transported through the waterways to the sea. The primary aim of this study was to evaluate the accumulation of trace elements in Ionian populations of P. laevigatus, as yet uninvestigated. Moreover, we sought to evaluate the metal transfer through the food chain of the coastal ecosystem. Since sandhoppers are the main food of P. laevigatus, and they have been thoroughly studied from an ecotoxicological point of view (Moore and Rainbow, 1987; Rainbow et al., 1989, 1998; Rainbow and Moore, 1990; Weeks and Rainbow, 1991, 1993; Fialkowski et al., 2000, 2003, 2009; Marsden and Rainbow, 2004; Ugolini et al., 2004, 2005, 2008; Rainbow, 2006; Ungherese et al., 2010a, 2010b; Conti et al., 2016), this study will generate useful contributions on this topic.
2.2. Sampling areas For this study we selected the sites A, B, C, and D along the sandy beaches of eastern Sicily (Fig. 1). Site A was the Simeto Nature Reserve Oasis (37°24′28.605″ N, 15°5′30.046″ E), located south of the mouth of the Simeto, a major river in Sicily that runs through the volcanic territory of Mount Etna and reaches the sea a few kilometers south of the town of Catania. This reserve is very important ecologically because it is a wintering area for migratory birds. Unfortunately, the presence of many illegal houses and the proximity of a large industrial plant in Catania pose considerable risks to the natural conditions of this area, adding their negative effects to those caused by volcanic materials produced from Etna and transported to sea in the Simeto river. Site B was the Agnone Bagni (37°19′55.353″ N, 15°5′41.247″ E), a seaside resort near the small town of Agnone Bagni, approximately 20 km south of Catania and 40 km north of Syracuse. The inshore waters of this area are frequently subject to the proliferation of the green algae Ulva lactuca due to a purification problem in the San Leonardo River. Because of this, bulldozers and mechanical shovels are often used to remove the algal mass deposited onshore by the tide. Site C was the Marina di Priolo (37°8′54.473″ N, 15°13′20.581″ E), a sandy beach approximately 15 km north of Syracuse and just south of the Peninsula Magnisi, on a narrow strip of land located in the heart of the Augusta Bay known for the famous archaeological site Thapsos. This site lies only a few kilometers away from the small Priolo Bay, where the impressive industrial and petrochemical center of Priolo Gargallo (Syracuse) is located. Site D was the Vendicari Nature Reserve (36°46′45.032″ N, 15°5′39.635″ E), located approximately 40 km south of Syracuse, which has been recognized as a wetland of international importance under the Ramsar Convention of 1971 because it includes a mixture of lagoons, sand dunes, rocky coastlines and sandy beaches. The Vendicari Reserve covers roughly 1512 ha, 575 of which constitute the zone A of integral reserve and 937 zone B (the so-called prereserve), which is dedicated to agriculture, tourism and sport. We selected it as a control area because it is located approximately 100 km from Mount Etna and considered by many researchers (e.g., Fasulo et al., 2012; Cappello et al., 2015) to be unaffected by the petrochemical contamination. 2.3. Metal analysis Frozen samples were dried in an oven at 105 °C until they reached a constant weight. After being homogenized, they were mineralized with an Anton-Paar Multiwave 3000 Microwave digestion system and PTFE vessels. Then, according to EPA Method 3052 (with a different amount of acid due to the best performance of the Anton-Paar system), we added 3.5 ml of HNO3 and 1.5 ml of H2O2 to the digestion mixture. At the end of this procedure, the content of individual vessels was diluted with 2 ml of ultrapure water and filtered using Whatman 40 filters. An aliquot of 500 μl, previously taken from the filtrate and diluted to 10 ml, was further diluted to 10 ml and then subjected to the experimental analysis. After suitable calibration through the internal standard method, analyses were conducted using a Perkin Elmer ICPMS, model Nexion 300X (Perkin Elmer Inc. Waltham, Massachusetts,
2. Materials and methods 2.1. Sampling method Adult beetles were collected at four sites along the sandy, Ionian 184
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using the Pearson r coefficient. In significant cases, a subsequent analysis with linear regression was performed. All the data were log transformed (natural logarithms) to achieve a normal distribution necessary for the parametric statistical analysis. The normality was tested with a Shapiro-Wilk test and the homogeneity of variance with a Levene's test. A one-way ANOVA was used to test for differences in metal concentrations in the animal tissues from the study sites. Post-hoc comparisons were conducted using the Tukey HSD method (Sokal and Rohlf, 2012). Finally, to assess the possible transfer of each metal through the food chain, we carried out a two-way ANOVA with the metal concentration as the dependent variable and the site and trophic level (prey, predator) as factors. In regards to the prey, as above specified, we used the data reported for Talitrus saltator by Conti et al. (2016). Statistical analyses were performed using SPSS for Windows (version 18.0). We considered p < 0.05 for the assessment of statistical significance. Finally, we calculated the transfer trophic coefficient (TTC), as the ratio of the metal concentration in the beetles to that in its prey, and considered it indicative of the biomagnification factor (BMF) when it was greater than 1 for the four toxic metals investigated.
U.S.A.), according to EPA Method 6020. For this investigation, we selected 16 target metals, 11 of which are essential elements for living organisms (Co, Cr, Cu, Fe, Mn, Mo, Ni, Se, Sn, V and Zn) and four of which are toxic (As, Cd, Hg and Pb). The results were normalized with blanks of mineralization and measurement, so the values are reported in mg/kg, taking into account the amount of sample and the multiple dilutions made prior to the analysis. Each determination was performed three times. The accuracy of the analytical procedure was confirmed by measuring a standard reference material, Nist 1566B oyster tissue in three replicates with a range of recovery between 96% and 102%, without observing any appreciable difference. 2.4. Statistical analysis At each site, the mean concentration and standard deviation of each metal in the beetle tissues was calculated. In addition, we also took into account the data relating to samples of the amphipod Talitrus saltator, the favorite prey of P. laevigatus, and the sand collected from the sites at the same time (Conti et al., 2016). The bioaccumulation of each metal in the animals was compared to the metal concentrations in the sand and beetles, and in the beetles and amphipods, using a Wilcoxon signed-rank test. We also tested the correlations between the metal concentration in the sand and carabids, as well as in the carabids and sandhoppers,
3. Results The mean and standard deviation of metal concentrations in the
Fig. 1. Map of the sampling sites; the Simeto Nature Reserve Oasis (A), the Agnone Bagni (B), the Marina di Priolo (C), and the Vendicari Nature Reserve (D).
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content in the prey and y the metal content in the predator:
Table 1 Mean trace metal concentrations (mg/kg) ± SD in Parallelomorphus laevigatus for the sampling sites A, B, C, and D.. Metal
A
B
C
D
As Cd Co Cr Cu Fe Hg Mn Mo Ni Pb Se Sn V Zn
1.03 ± 0.13 0.33 ± 0.05 0.35 ± 0.02 0.62 ± 0.06 20.67 ± 1.09 104.11 ± 38.80 0.38 ± 0.01 17.37 ± 0.43 0.57 ± 0.02 0.35 ± 0.05 0.27 ± 0.003 0.75 ± 0.69 0.16 ± 0.02 0.27 ± 0.06 107.06 ± 6.24
1.06 ± 0.10 0.09 ± 0.002 0.59 ± 0.05 0.23 ± 0.02 15.39 ± 0.65 129.56 ± 43.54 0.16 ± 0.01 12.48 ± 0.55 0.40 ± 0.03 0.46 ± 0.06 0.53 ± 0.01 0.76 ± 0.67 0.05 ± 0.02 0.16 ± 0.02 78.45 ± 4.27
0.98 ± 0.08 0.30 ± 0.02 0.16 ± 0.005 0.48 ± 0.02 15.73 ± 0.21 95.09 ± 61.90 0.53 ± 0.02 18.55 ± 0.40 0.66 ± 0.01 0.34 ± 0.03 0.17 ± 0.004 0.53 ± 0.41 0.05 ± 0.03 0.24 ± 0.02 116.21 ± 1.05
1.89 ± 0.17 1.04 ± 0.06 0.17 ± 0.008 0.69 ± 0.02 16.26 ± 0.39 57.87 ± 19.61 1.10 ± 0.04 6.83 ± 0.18 0.32 ± 0.02 0.84 ± 0.06 0.63 ± 0.003 1.24 ± 0.61 0.27 ± 0.02 0.15 ± 0.03 92.40 ± 1.58
y = 1 . 004x + 1. 541 Moreover, the TTC was 5.01 for Hg, and less than 1 for As, Cd and Pb. 4. Discussion As predators, ground beetles are a potential bioaccumulator of high metal concentrations in the tissues of their prey. However, Hopkin (1989) highlighted that carabids have suitable mechanisms for detoxification, such as the removal of whole degenerated cells, exocytosis, and extrusion of metal-containing vesicles into the lumen of the digestive tract. Moreover, Janssen et al. (1991) and Kramarz (1999) found rapid metal excretion in this group. Both of these mechanisms
tissues of P. laevigatus (mg/kg dry weight) are given in Table 1. At site D, numerous elements (e.g., As, Cd, Cr, Hg, Ni, Pb, Se and Sn) were present at the highest values, while Fe and Mn were at the lowest values. It should also be noted that Cu and V are more abundant in the specimens from site A, Co and Fe from site B, and Mn, Mo and Zn from site C. The mean metal content decreased in the following sequence, Zn (98.53 mg/kg), Fe (96.66 mg/kg), Cu (17.01 mg/kg), Mn (13.81 mg/ kg), As (1.24 mg/kg), Se (0.82 mg/kg), Hg (0.54 mg/kg), Cr (0.51 mg/ kg), Ni (0,50 mg/kg), Mo (0.49 mg/kg), Cd (0.44 mg/kg), Pb (0.40 mg/ kg), Co (0.32 mg/kg), V (0.21 mg/kg), Sn (0.13 mg/kg). The concentration of these metals in the tissues of P. laevigatus differed among the four sites. Nevertheless, a one-way ANOVA showed significant differences among the metal concentrations in the beetles only for Hg (F =7.585, p < 0.01), Cd (F=6.190, p < 0.05) and Se (F=6.004, p < 0.05). The post-hoc comparisons clarified that these differences were due to the Hg (p < 0.01) and Cd (p < 0.05) concentrations at sites B and D, and the Se (p < 0.05) concentrations at sites C and D sites (Fig. 2). The Wilcoxon signed-rank test showed significantly higher concentration of Cd (p=0.003), Cu (p=0.003), Hg (p=0.003), Mo (p=0.005), and Zn (p=0.003) in the beetles than in the sand. Conversely, the metal concentration was greater in the sand than in the animal tissues for As (p=0.003), Co (p=0.008), Cr (p=0.003), Fe (p=0.003), Mn (p=0.003), Ni (p=0.01), Pb (p=0.004), Se (p=0.003), and V (p=0.003). By applying the Wilcoxon signed-rank test to the data presented in Conti et al. (2016) for the amphipod Talitrus saltator, we were able to determine that only mercury has a concentration greater in the beetle than in its prey (p=0.003). The two-way ANOVA proved that the different metal concentrations were dependent on the trophic niche of animals for As (F=37.001; p < 0.001), Cr (F=8.547; p < 0.01), Cu (F=20.415; p < 0.001), Ni (F=14.188; p < 0.01) and Se (F=31.414; p < 0.001). The differences were due to the main effects (e.g., the trophic niche and the site) for Cd (F=8.722; p < 0.01 and F=8.572; p < 0.01), Co (F=14.440; p < 0.01 and F=5.279; p < 0.01), Fe (F=22.936; p < 0.001 and F=4.870; p < 0.05), Hg (F=50.270; p < 0.001 and F=14.951; p < 0.001) and V (F=18.919; p < 0.001 and F=3.897; p < 0.05). For Mn, the differences were dependent not only on the trophic niche of the animals (F=10.551; p < 0.01) and the site (F=7.722; p < 0.01) but also on their interactions (F=3.760; p < 0.05) (i.e., the concentration of this metal differed among sites in a different way for the prey and predator) (Fig. 3). No correlation was found between the concentration of metals in the animal tissues and sand. The correlation analysis of the metal concentrations in P. laevigatus and its favorite prey (Table 2) was significant only for Hg (r=0.80, p < 0.01). The linear regression of this metal (Fig. 4) has the following equation, with x being the metal
Fig. 2. Mean concentrations of trace metal expressed as ln(mg/kg) in the animal tissues at the sampling sites (A–D). The letter (a–c) indicates a difference at the p < 0.05 level according to post-hoc comparisons. Only metals that contribute to the statistical differences are shown.
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Fig. 3. Two-way ANOVA plots of the predator (continuous line) and prey (dashed lines) at each sampling site, A, B, C, and D. The toxic metals underlying the statistical differences and Mn are shown. Table 2 Correlation between the metal concentration in Parallelomorphus laevigatus (predator) and Talitrus saltator (prey) collected at the four Sicilian sites; r is the Pearson coefficient value and P is the statistical significance. Metal
r
P
As Cd Co Cr Cu Fe Hg Mn Mo Ni Pb Se Sn V Zn
−0.06 0.52 0.24 −0.13 0.43 0.40 0.80 0.40 0.24 0.002 −0.31 0.01 −0.02 0.32 0.39
0.86 0.10 0.47 0.70 0.19 0.23 0.03 0.22 0.48 1.00 0.36 0.98 0.96 0.34 0.23
allow these ground beetles to avoid significant metal poisoning (Butovsky and van Straalen, 1995; Hunter et al., 1987; Janssen et al., 1991; Kramarz and Laskowski, 1997; Lagisz et al., 2005; Lindquist et al., 1995). Our data on P. laevigatus supports the existence of defense mechanisms in this never before investigated species. Indeed, the two-way ANOVA showed that the metal content in animal tissues was always higher in the prey than in the predators, except for mercury. Few ecotoxicological investigations, however, have been conducted on species of ground beetles inhabiting coastal systems. To our knowledge, P. laevigatus is the first psammo-halophilous species used for this purpose. Moreover, unlike most Carabidae which are generally
Fig. 4. Linear regression for Hg in predator and prey.
considered non-specialized predators, P. laevigatus is a specialized predator on sandhoppers (Alicata et al., 1982; Caltabiano et al., 1984; Audisio and Vigna Taglianti, 2010). Furthermore, the environment where this insect lives is very special. The strip of beach next to the shoreline is a transitional habitat between two very different systems, the sea and the land, which affect each other. This mutual influence doubles the chances of habitat pollution, as toxicants from the sea (e.g., chemicals of industrial origin, and oil spills) end up on the beach and chemicals from land (e.g., pesticides and fertilizers) end up in the sea. 187
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allowed living organisms to adequately adapt. The situation in the southern area is very different. The industrial plant of Priolo dates back to the early 1950s. The main contamination of Augusta Bay, due to overboard discharge of various metals, including mercury, occurred in the 1970s (Ausili et al., 2008). Anthropogenic pollution makes it difficult for animals to adapt to such quick, massive changes in their habitat. Therefore, we are currently unable to predict what the long-term consequences of mercury accumulation means for the future of this species and the entire food web. However, it has been hypothesized that the mercury pollution generated in Augusta basin is spreading through the Mediterranean Sea (Sprovieri et al., 2011) and may cause serious problems for living organisms and marine ecological balances, even at great distances from the place of the original pollution. In addition, pollutants such as mercury biomagnify in the food web. For example, the presence of large amounts of Hg in fish in the basin of Augusta has been detected (Bonsignore et al., 2013) and the implications of this threat to human health are easily predictable. In conclusion, this paper confirms that ground beetles are potential indicators of anthropogenic stress, which has been suggested for different ecosystems by various authors (e.g., Butovsky, 2011; Ribera et al., 2001; Schirmel et al., 2015; Simon et al., 2016).
The concentrations of Cd, Cu, Mo, Hg and Zn were higher in the carabids that in the sand, which leads us to hypothesize a possible dermal absorption of these elements from the soil. Brunsting and Heessen (1984) asserted that in beetles the dermal absorption of soil pollutants is restricted to the larval phase, while in adults metal transfer only comes from the prey to the predator. Similarly, we believe that the intake of metals in adult P. laevigatus takes place only through the food chain. Indeed, Conti et al. (2016) showed that in the same habitats studied here, the trace metals were bioaccumulated in adults of T. saltator and transferred to their predators. The high values of As, Cd, Cr, Pb, Ni and Hg detected in beetles from site D, are likely from the emissions sources of the nearby industrial plants, such as the Priolo settlement, which is located 30 miles away from Vendicari (Mudu et al., 2014). In regards to cadmium, there is also intense agricultural activity in the pre-reserve part of site D that explains the high concentration of that metal both in the prey (Conti et al., 2016) and the predators. Indeed, many sources of phosphate in fertilizers contain cadmium, which can lead to an increased concentration of this metal both in the soil and water (Jensen and Bro-Rasmussen, 1992, Van Assche and Ciarletta, 1992). Furthermore, data on the high concentration of Hg in insect tissues from site D are not surprising. In fact, Ausili et al. (2008), when analyzing the sediments, the mussel Mytilus galloprovincialis and the red mullet Mullus barbatus, collected from various locations in the petrochemical area between Augusta and Priolo, detected such elevated concentrations of mercury that this site was identified as the most polluted in the Mediterranean. Subsequently, various authors (e.g., Sprovieri et al., 2011, Di Leonardo et al., 2014) have considered this area to be a mercury point-source for the entire Mediterranean Sea. Longo et al. (2013) found a high presence of this metal in the tissues of Ligia italica, a woodlouse present at the Vendicari Reserve. These authors interpreted this anomalous presence to be the result of pollution from the industrial plant of Priolo, transported south by sea currents. The present paper shows increasing Hg concentrations throughout the simplified trophic web of sandy beaches and confirms the capability of this pollutant to biomagnificate, as evident from both the two-way ANOVA and the correlation analyses. Moreover, the high value of BMF (approximately 5) confirms the severe pollution level even in this protected area. It is noteworthy that site C, which was closest to the industrial area of Priolo, was less influenced by the metal pollution coming from the petrochemical plant. This is due to the protective barrier of the Peninsula Magnisi. Some elements, such as Mn, Mo and Zn, can reach that site only by being carried with ash particles, rather than from the sea. Iron, cobalt, cuprum and vanadium are some of the most significant metals present in volcanic emissions (Cimino and Ziino, 1983; Cimino et al., 1984; Toscano et al., 2008). Their massive presence at sites A and C is probably from the outflow of the Simeto river and its tributaries, which transports a mixture of volcanic materials and materials resulting from the river’s erosive action to the sea. The Ionian sandy coast of Sicily can be divided into a northern region (sites A and B), where there is the influence of Mount Etna, and a southern region (sites C and D), where there is the anthropogenic influence. Both conditions can cause metal pollution, however, of these two, the most dangerous seems to be the man-made one. The Etnean volcanic activity began approximately 570,000 years ago and has continued rather steadily with degassing and ash emissions from summit craters. Many of trace metals measured (i.e., Fe, Mn, V, Zn and Cr) are present in lava soil and volcanic ash, causing sand contamination (Taylor and Lichte, 1980; Okamoto et al., 1997; Cimino and Toscano, 1998; Toscano et al., 2008; Ochota et al., 2012; Baturin et al., 2013; Orecchio et al., 2016). With its long-term contribution of heavy metals to the environment, the volcano has
Declaration and contribution All authors declare that this work described has not been published previously neither it is under consideration for publication elsewhere. All authors approve the publication of MS on Ecotoxicology and Environmental Safety and that, if accepted, it will not be published elsewhere in the same form, in English or in any other language, including electronically without the written consent of the copyrightholder. Authors participated in the present study as follows: Erminia Conti and Giovanni Costa performed the field sampling, prepared the samples and conducted the statistical analysis; Concetto Puglisi and Sandro Dattilo carried out analytical analysis for detecting metal concentration in animal tissues All the authors contributed in drafting the manuscript. All authors read and approved the final manuscript. Acknowledgments We would like to thank the Ministry of University and Scientific Research (MIUR) of Italy and the National Council of Research (CNR) of Italy for financial support. We especially thank the associate editor and the anonymous reviewers for providing constructive critiques of the manuscript. References Alicata, P., Caruso, D., Costa, G., Marcellino, I., Motta, S. and Petralia, A. 1982. Studi eco-etologici su artropodi delle dune costiere di Portopalo (Siracusa, Sicilia). Quaderni sulla struttura delle zoocenosi terrestri. C.N.R. Roma. 3. Ambienti mediterranei. I. Le coste sabbiose, 159–183. Andréa, M.M., 2010. O uso de minhocas como bioindicadores de contaminação de solos. Acta Zool. Mex. 2, 95–107, (n.s.). Andrews, S.M. and Cooke, J.A. 1984. Cadmium within a contaminated grassland ecosystem established on a metalliferous mine waste. In: Osborn D. (Ed) Metals in animals. Symposium N 12, Institute of Terrestrial Ecology. Abbots Ripton, pp. 11– 15. Audisio, P. and Vigna Taglianti, A. 2010. Insecta Coleoptera. Biol. Mar. Medit. 17 (Suppl. 1), 547–571. Ausili, A., Gabellini, M., Cammarata, G., Fattorini, D., Debenedetti, M., Pisanelli, B., Gorbi, S., Regoli, F., 2008. Ecotoxicological and human health risk in a petrochemical district of southern Italy. Mar. Environ. Res. 66, 215–217. Baturin, G.N., Dubinchuk, V.T., Manewich, T.M., 2013. Species of graphite, phosphorus, and some heavy metals in volcanic ashes. Dokl. Earth Sci. 451 (I), 770–774. Beyer, W.N., Pattee, O.,H., Sileo, L., Hoffman, D.J., Mulhern, B.M., 1985. Metal contamination in wildlife living near two zinc smelters. Environ. Pollut. 38A, 63–86. den Boer, P.J., 1977. Dispersal power and survival. Misc. Pap. Landbouw. Wagen.. 14,
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