Introduction

1Currently, coastal lagoons in Mexico face serious problems caused by pollution, which produces considerable damage to the organisms that inhabit them (Botello & Páez-Osuna, 1986). These ecosystems are extremely fragile and have been suffering very important transformations along the entire country’s coast. These are caused by river damming, closing of the communication between the lagoons and the ocean, and municipal and industrial waste water discharge from the surrounding populations, which contain various contaminants, including an important number of metals (Villanueva & Botello, 1992). Mendoza-Carranza et al. (2016) reported that in southeastern Mexico metal pollution has been associated with agrochemical use, urban expansion, and particularly petroleum extraction. Most of these pollutants are transported by runoffs to rivers and are finally deposited in water bodies with low hydrological dynamics such as coastal lagoons where accumulation occurs primarily in sediments (Lester, 2014; Melgar et al. 2008).

2Metals and metalloids are highly reactive elements which are accumulated in minerals and organisms within the aquatic environment. These contaminants are present in the form of trace elements, being in water, and in the sediment or the marine biota, and thus can become toxic if found in high concentrations. The occurrence and bioaccumulation of many pollutants through the food-chain could present a risk to human health (Comby et al. 2014). There are other elements that do not belong to the transition group but, through mobilization by human activity, their levels have exceeded the concentrations found naturally, such is the case of lead. The impact that these increases have on terrestrial and aquatic ecosystems is very high, since they can affect organisms at both, somatic and genetic levels (Song et al. 2014). There are many metals such as: copper, cobalt, chromium, zinc, fluorine, and vanadium that are a natural part of biologic systems, but when their levels are increased or they change their chemical form they can become toxic.

3Metallic elements are found in all living organisms and play several roles. They may be structural elements, stabilizers of biological structures, components of control mechanisms (e.g., in nerves and muscles), and in particular, are activators or components of redox systems. Thus, some metals are essential elements, and their deficiency results in biological functions impairment. Essential metals, when present in excess, may even be toxic; it should be recognized that metals might also have deleterious effects on other animal species and plants; such effects may lead to modification of an entire population or species assembly in an ecosystem and also may be of great significance to human life so theyshould be considered in the total evaluation of environmental pollution by metals and their compounds (Nordberg et al. 2007).

4The effects of pollutants on human health have led to the evaluation of trace metals presence in the last decades of research, since they have characteristics such as persistence and bioaccumulation capacity and are considered as dangerous substances, they are also a part of complex mixtures in the coastal zone from non-point sources, especially in developing countries such as Mexico (Diop et al. 2015; Lei et al. 2016). Sontecomapan Lagoon is a region with no intense industrial influence, with fishing, tourism and local agricultural activities, for self-consumption, so it is likely that the potentially toxic metals found in this lagoon ecosystem come from industrial areas such as Coatzacoalcos and Minatitlán located in the southern region of the state of Veracruz, and these anthropic emissions are transported to the study area mainly by winds and rains compared to the specific contributions of temporary runoff around the lagoon.

General characteristics of metals

5Lead (Pb) and Cadmium (Cd) are non-essential metal for organisms. However, Pb exists in every tissue and organ in mammals and it presents two different oxidation states, Pb⁺² and Pb⁺⁴, the first being predominant in an aquatic environment; in sea water, it is found as PbCl₂ (43 %), PbCO₃ (42 %) and Pb (OH)₂ (9 %), additionally there are some sulfurous compounds formed with this metal under anaerobic conditions in marine sediment. Pb quantities increase in places where there is mud discharge from treatment plants, port dredging and waterways, or where there is discharge from industrial waste into rivers, estuaries and coastal lagoons (Nordberg et al. 2007; Jacob et al. 2018). Cd in freshwater environments is closely associated with colloidal matter as CdCl₂ and CdSO₄; in the ocean, 66 % is present as Cd⁺² ion along with CdCO₃ (26 %), Cd (OH)₂ (5 %), CdCl₂ (1 %), and CdSO₄ (1 %); in coastal waters and estuaries, a high proportion of this metal is found associated with particles, forming complexes. The main sources of Cd in aquatic environments come from drainage water from agricultural soil and discharge from mining and industry in addition to municipal wastewater discharge and the sludge from treatment plants (UNEP, 1985; Nordberg et al. 2007); its presence in marine environments reduces the survival of fish larvae and juveniles, mollusks and crustaceans (Fukunaga & Anderson, 2011).

6Chromium (Cr), Copper (Cu), Nickel (Ni), Cobalt (Co) and Zinc (Zn) are considered to be essential metals for living organisms when found at low concentrations and under certain chemical forms. For example, Cr III is insoluble and difficult to transport into the cells whereas Cr VI is very toxic because of its solubility and easy penetration into the cells. In rivers and oceans, Cr is found mainly in hydroxide complexes such as CrO^-2 ion, becoming part of the manganese nodules in marine waters. In coastal environments, it is intimately associated to wastewater discharge from industry: mining, tannery, galvanoplasty and fertilizer industry (Nordberg et al. 2007; Jacob et al. 2018). Cu acts in metabolism at enzymatic levels and the effects of its toxicity or deficiency on animals depends on its interactions with other elements, such as molybdenum and zinc. Ni, although it is an essential metal, in high concentrations it can cause cancer in lungs and nose, as well as severe dermatitis; it is intimately related with vanadium because it is also employed as a catalyst in the petroleum refining process; its high concentrations are caused directly by activities related to the oil industry (Nordberg et al. 2007; Jacob et al. 2018). Co acts as a coenzyme, depending on the chemical form; variations in its concentration can represent a risk and cause of dermatitis (Ponce-Vélez, 1988; Ponce-Vélez & Botello, 1991; Nordberg et al. 2007). Zn is found abundantly in the human body; it generally shows low toxicity to aquatic life, although some species are sensitive to low concentrations; however, the emission of zinc into the atmosphere can cause lung damage (Jacob et al. 2018).

Metals in water

7In water, metals can be found dissolved, in a colloidal state, or in suspension, adhered to materials such as organic matter (Goldberg, 1976). The state of metals speciation in the aquatic media is difficult to establish, since these elements form complexes with inorganic ligands and organic compounds present in water, thus forming a reservoir of metals in solution. The study of metallic complexes formation in an aquatic environment is of great importance if you consider the toxicity that some of these metals have on the organisms present in the environment, and aids to determine their final destination (Mandelli, 1979). Heavy metals can be considered as other aspect of the human fingerprint as well, although all of them are present in the earth crust, their wide presence in waters, soils and atmosphere is mainly due to human activities; their sources in the environment are difficult to identify, as they could be a combination of natural and anthropogenic sources, both diffuse and point (Bayen, 2012).

Metals in sediment

8In marine sediments, the concentrations of these elements are more easily measured than those found in water columns, mainly due to the fact that metals tend to sediment or be adsorbed because of their high chemical reactivity. Thus, it is important to carry out a geochemical study to determine the degree of contamination for the water body. There are several advantages in using sediments for this type: they are relatively stable deposits of real and potential contaminants; they can provide a historic record of the contamintants contribution from anthropogenic activities; they allow the procurement of more adequate samples, reproducible and easier to analyze compared to water and organisms, and they facilitate data collection in a wide range of environmental conditions (GEMSI, 1983). For geochemical studies, it is important to carry out analyses to quantify organic carbon concentrations, the presence of calcium carbonates and the granulometric composition of the sediment, since the affinity of certain metals can depend on some of these parameters. Organic material, for example, is a source of energy for the sedimentary system, and biological agents are the main factors for diagenetic changes, which allow for materials transformation in both, their composition and their physicochemical properties; it is here where trace elements are retained. This organic material can be found in aquatic systems in two forms: particulate and colloidal (Libes, 1992).

9Precise information on metal interactions is derived from local and regional studies, like the one carried out by Ponce-Vélez (1988) which shows that some toxic metals, like lead and cadmium, have a certain tendency to be deposited in sediments with high concentrations of calcium carbonate. Conversely, clays adsorb metallic ions on their surface and carry them into estuaries, where they are deposited thanks to their cohesive properties and prevailing environmental conditions; therefore, the metallic elements are trapped into the sediments and are thus available to organisms (Förstner & Wittman, 1979). Metals in seawater and marine sediments can incorporate into the aquatic food webs through sediment water exchanges and then are biomagnified at higher levels of food webs (Hosono et al. 2011). This process may cause potential damage to mammals, vertebrates and human health as well (Chen et al. 2010) (Fig. 1).

Figure 1. Metal cycle between the different compartments of an estuarine environment (de Souza et al. 2016).

Metals in organisms

10Some biological processes in the environment can become mechanisms for mobilizing metals, which would otherwise be lost in the sediments. In this regard, bacterial action plays an important role in the mobilization of toxic metals within the aquatic environment. Microorganisms are capable of interacting with metals and change their oxidation state or organic complex thereby affecting the speciation and mobility of the metal elements (Olaniran et al. 2013; Jacob et al. 2018). However, due to the capability of metals to form complexes with organic matter, they tend to be fixed in the tissue of exposed organisms. This is one of the greatest problems that metals present as contaminants in the aquatic environment, since organisms commonly suffer from a phenomenon of bioconcentration, which is the ability of organisms in the same trophic level to absorb a contaminant into their tissues from the environment that surrounds them. Conversely, a process of bioaccumulation can occur; this refers, not only to the capacity to concentrate it but also to incorporate it into their tissues through metabolic processes. Therefore, at some point in time, the contaminant concentration in tissues is greater than that of the surrounding environment. Another phenomenon is biomagnification, which refers to a contaminant increase within successive trophic levels, that is, a concentration of a certain contaminant in organisms greater than that in the organisms they fed upon, which causes a greater concentration in the higher levels of the trophic web; this event has been proven for metals like mercury (Cabrita et al. 2017; Cipro et al. 2017), cadmium (Majer et al. 2014), and potential biomagnification for Zinc (Cheung & Wang, 2008; Cardwell et al. 2013) (Fig. 2).

Figure 2. Routes and metal interactions in the coastal zone. Mercury as an example of toxic metal (Mandelli, 1979).

11Some organisms are indicators of contaminants, either through fixation of these in their tissues, because of their abundance, or through their unexpected absence. In order for a species to be used as an indicator of particular characteristics of a biotype in environment, it must:

1. Be easily identified, even by those who are not experts.

2. Be abundant in its preferred habitats, throughout an extensive geographical region.

3. Exhibit approximately the same degree of tolerance to a particular parameter.

4. Possess a moderately long life cycle.

5. Be relatively sessile or at least not able to temporarily escape from the environmental changes by rapid migration (Farrington et al. 2016).

12The levels of metals in mollusks and other invertebrates are often considerably higher than in other constituents of marine environment due to their habitat and feeding habits (Sun et al. 2011). Compared to sediments, mollusks exhibit greater spatial sensitivity and therefore, are the most reliable tool for identifying sources of available metal contamination (Hamed & Emara, 2006). Under certain environmental conditions, metals might accumulate up to toxic concentrations and cause ecological damage (Bai et al. 2011). Metals such as iron, copper, zinc and manganese, are essential since they play important roles in biological systems (Hogstrand & Haux, 2001), whereas non-essential metals such as Pb, Cd and Hg are usually potent toxins and their bioaccumulation in tissues leads to intoxication, decreased fertility, cellular and tissue damage, cell death and organ malfunction (Oliveira Ribeiro et al. 2002).

13This set of characteristics is met by certain types of algae, marine phanerogams and some mollusks, such as oysters and mussels. Thus, these have been used as bioindicators to quantify levels of inorganic contaminants that may threaten the ecosystem balance.

Justification

14This work was carried out in order to have a reference point for a pristine area, since the situation faced by the coastal systems of the Gulf of Mexico is extremely serious (González-Fierro, 1995). Thus, we searched for a lagoon that was distant from the highly impacted zones and also, that was of ecological and economic importance. Therefore, the Sontecomapan Lagoon, in the State of Veracruz, was chosen because in this area there is no industry that can discharge waste directly into the system and no petrochemical complexes that could originate high levels of contamination.

Region of study

15The Sontecomapan Lagoon (18° 0’ and 18° 34’ N; 95° 00’ and 95° 04’ W) belongs to the basin region formed by San Martín Tuxtla and Sierra de Santa Martha volcanos, in the State of Veracruz (Mexico). It is located in the mountain range of Los Tuxtlas, which separates the tertiary basins of Veracruz and the Salina del Istmo. The ground is made up of clastic volcanic rock, where breccia lavas, and basaltic and andesitic tuffs are predominant. The bottom of the lagoon is covered with ash from volcanic activity, fluvial bed load from nearby areas, or Eolic processes from preexisting volcanic ash (Carranza-Edwards, 1975).

16It is a small lagoon of irregular shape that measures about 12 km in length and 1.5 km in width. At the northeastern side it has a mouth that permanently connects with the ocean by a narrow canal. At one side there is a sediment deposit, and on the other end of the mouth there is a basalt flow named “Roca Morro”, and further down there is a valley that allows the accumulation of organic matter, thus generating a fertile area with agricultural importance. The area presents a climate type Am (f) that corresponds to warm-humid with rains all the year and an average annual temperature greater than 22 °C (García, 1988, 1990). The presence of volcanic ash has been reported at the lagoon bottom; the sediments are mainly sandy clay and belong to the morphometric unit II (Carranza-Edwards, 1975). The fresh water contribution comes from various tributaries at different points of the system, mainly from the southern and southeastern zones, and it is closely related with the climatic conditions and variations in the region. The rivers that feed it are: La Palma, Coscoapan, Viejo Coscoapan, Sábalo, and Haltajapan, and the streams are: Sumidero, Basura, Sontecomapan, Chuniapan, El Fraile, Los Pollos, and La Boya (Fig. 3).

Figure 3. Location of sampling sites in the lagoon Sontecomapan, Veracruz. (CONANP, 2004).

17The lagoon system is divided into several zones: the sandbar, which extends from the beach to Roca Morro, and the canal “El Real”, which encompasses the zone of the Palma River and extends to a canal that opens up and makes up for the majority of the lagoon, with an average depth of 1.50 m. Total annual precipitation is between 3000 and 4000 mm. February and March are the driest months and September is the wettest with over 6000 mm. The temperature of the region is considered to be isothermal, with a maximum of 26 °C in January. The salinity data show a decreasing gradient from the sandbar to the southern side, at the mouth of the Coscoapan River (Contreras, 1993). The major body of the lagoon is completely surrounded by a belt of mangrove, Rhizophora mangle and Avicennia sp., strongly impacted; there is submerged vegetation like Ruppia maritima, which is present in a patchy distribution. The aquatic plankton is characterized by the presence of filamentous algae, diatoms, protozoa, dinoflagellates, rotifers, crustaceans and fish larvae. Among the commercially important species are white shrimp, oyster, prawn, snapper, sea bass, mullet, red snapper, big-eye thresher, croaker, and white mullet; this book includes recent information on the flora and fauna of the lagoon. Since 2004, the site RAMSAR 1342 has been rich in biodiversity and is an important ecosystem in the migratory route of various bird species (CONANP, 2004).

Materials and Methods

Sampling

18Ten stations at the lagoon were sampled for collection of organisms, water and sediments during two annual cycles (1991-1992), taking into consideration the different climatic seasons of the region: “dry season” (March-June), “rainy season” (July-October), and “Nortes season” (November-February) (González-Fierro et al., 1994; González-Fierro, 1995); it should be mentioned that in sites 1 and 3 only organisms were obtained. The physicochemical parameters measured in water column were: temperature, salinity, pH, depth, and transparency.

19In sediments, organic matter, calcium carbonates and texture percentages were determined. To record temperature we used a Taylor thermometer (-10 to 200 °C); salinity was measured using a refractometer; pH values were registered using a Piccolo field pH meter; depth and transparency were measured with a Secchi disc.

Sediments

20In order to obtain sediment samples, we used a Van Veen dredge. In order to avoid sample contamination by metals, only the sediments from the central part of the dredge were taken, without coming into contact with its walls. The sediments were then placed into plastic bags into a cooler to be sent to the laboratory for processing.

Water

21Water samples were collected in one-liter plastic bottles in surface water, 5 ml of concentrated sulfuric acid were added and the samples were then kept frozen until they were processed in the laboratory.

Organisms

22All organisms were collected manually, placed in plastic bags and stored in a cooler (González-Fierro, 1995).

Laboratory processing of samples

Sediment conditioning

23Samples were thawed at room temperature, then dried at 50 °C in an oven for 48 h, except for the portion that was used for granulometry analysis.

Organic Matter (determined as Organic Carbon OC)

24Between 0.2 and 0.5 g of dry sediment (using the fraction that was retained in a 0.2 mm mesh) was placed in a 500 ml Erlenmeyer flask, 10 ml of 1N potassium dichromate were added and mixed. 20 ml of concentrated sulfuric acid were added and mixed for one minute, gently swirling the flask in order to ensure a complete mixture of the reagents with the sediment, and taking care that the sample did not remain adhered to the walls so that it remained in contact with the reagents. The mixture was allowed to sit for an additional 30 minutes and then diluted to 200 ml with distilled water, then, 10 ml of 85 % phosphoric acid, 0.2 g of sodium fluoride and 15 drops of diphenylamine indicator were added. The mixture was titrated with a solution of ferrous sulfate 0.5 N. The color changed from brownish green to brilliant green. As control, a blank was run in the same manner without sediment (Gaudette et al. 1974)

Carbonates

25The samples were dried in porcelain capsules at 110 °C for 8 h, then put into porcelain mortars to pulverize and homogenize them, and stored in polyethylene bags for posterior analyses. The determination was carried out using a Bernard calcimeter, which consists of a graduated glass column joined, using a latex hose, to a glass bubble that serves to level the column. At one end, we placed a reaction flask with two entries, one to the Bernard column and the other to a burette containing 50 % HCl. The calcimeter measures the displacement in a graduated column after the addition of HCl to the sediment. Since this is a manometric analysis, it is necessary to consider the pressure and temperature in the system when equilibrating the column with the atmospheric pressure. Thus, in the calculations we included a factor determined by the Berthelot equation (real gases) (Hesse, 1971).

Granulometry

26For the determination of the percentage of gravel, sands, silt, and clays, we followed the techniques proposed by Folk (1974), known as sieves and pipettes, based on the rate of sedimentation in a ratio inversely proportional to the size of the particle.

Metals in Water

27Water samples were thawed at room temperature and a 50 ml aliquot was digested with HClO₄ at 100 °C until approximately 10 ml of residue was left. This was diluted to 50 ml, 3 ml of HBF₄ were added, and the sample was read in an atomic absorption spectrophotometer (Villanueva, 1987).

Metals in Sediments

28For determination of total concentration, the material used for the analysis was washed for three days in HCl 2N, then for three days in HNO₃ 2N, and finally rinsed in distilled water and stored in plastic bags for later use. The sediment was dried at 60 °C, pulverized and sifted through a plastic screen, 5cm in diameter. 0.25 g were placed in a PTFE vessel with 10 ml of inverted aqua regia (HNO₃:HCl, 3: 1). The digesters were maintained at 100 °C ± 10 °C for approximately 18 h and the residue washed in bidestilled water. The supernatants were read in a flame atomic absorption/emission spectrophotometer (Shimadzu), using blank controls="true" for every group of eight samples, and standards of known concentrations (Loring & Rantala, 1977; modified by Páez-Osuna & Osuna-López, 1990). For determining the bioavailable fraction, 2 g of sediment were washed for 24 hours in 25 ml of 25 % CH₃-COOH, and then rinsed in bidistilled water. Supernatants were collected and read by atomic absorption in the same manner (Agemian & Chau, 1976).

Metals in Organisms

29The collected organisms were dried at 60 °C for 48 h and tissue was pulverized in a porcelain mortar. A sample was taken for metal extraction by acid digestion with concentrated HNO₃. Once the acid was added, the samples were dried at 350 °C for two hours and then, the operation was repeated. The ashes obtained were resuspended in 2N HNO₃, centrifuged and if necessary, and filtered. Samples were read in an atomic absorption spectrophotometer (Goldberg et al. 1983).

Results and Discussion

30The data reported in this paper correspond to the original research developed by González-Fierro in 1995 at the Grupo de Contaminación Marina del Instituto de Ciencias del Mar y Limnología de la Universidad Nacional Autónoma de México, as part of an integral project to carry out the environmental diagnosis of the Sontecomapan Lagoon and to record the first data on various environmental pollutants such as metals; a general description of the metals concentrations in sediments and organisms of this lagoon has already been published in Spanish by the authors of this chapter (González-Fierro et al. 1994).

Water

Physical and chemical parameters

31Table 1 shows the physical and chemical parameters data recorded in situ during annual cycle, in the dry season in March, 1991 greatest depth, transparency and salinity were recorded, the latter variable behaved as expected because of high evaporation leading to maximum values of 24.9 ups; however, high depth may be justified due to unusual rains input prior to sampling, which increased the strap depth of the lagoon up to 6 m.

32It notes that, from the 1991 drought, subsequent sampling showed a freshwater to brackish (oligohaline) behavior in the lagoon system studied, as the salinity ranged from 0.25 ups in rains from August, 1992 and 4.0 ups in rainy July, 1991, a scenario that directly influences metal solubility in the water column (Owsianiak et al. 2015). The pH, another important factor for the solubility of metals evaluated in this work, stayed about 7, being more basic in dry seasons of 1991 and 1992, with 7.94 and 7.71, respectively; the lowest value was 6.8 recorded in rainy September, 1991. It is known that when the pH is neutral or close to 7, metals are in solution in water and have a longer residence before reaching the sediments (Mendoza-Carranza et al. 2016).

Metals

33It was not possible to reliably determine the concentrations of metals in water, because they were below the detection limit of the instrument used (<1 µg/l), an atomic absorption spectrophotometer, even in the case of high aqueous solubility metals such as cadmium.

Sediments

Organic Carbon

34Table 2 shows the results of Organic Carbon (OC) which are presented in percentage values as an indicator of organic matter presence in the lagoon sediments; there is a noticeable homogeneity in the mean along the six sampling periods. The overall range of OC was 0.11 (August, 1992 rainy season) to 4.16 % (September, 1991 rainy season), which shows that the transport of organic matter occurs through the important runoff draining into the lagoon. The duration and intensity of the rains, that can vary from year to year, influence the organic material deposited in sediments and is reflected in these different values from one year to another during the rainy season, so it is important to have data periods longer than an annual cycle to evaluate the oscillations in large temporary records.

Table 1. Physicochemical parameters in water column of Sontecomapan Lagoon, Veracruz. 1991-1992

Table 2. Organic Carbon as an indicator of organic matter content in the sediments of Sontecomapan Lagoon, Veracruz. Values in %. 1991-1992

Granulometry

35Figure 4 shows sedimentary texture considering only the four particle categories most reported in the literature on coastal and marine sediments pollution. The sand content was dominant in the sampling sites 2-7 with values between 59.74 (Station 6) and 99.4 % (Station 2) which does not represent a separate depositional environment for the retention and storage of metals; in contrast, the sites 8 to 10 had clay dominance, except at site 8 wherein the sediment was silty clay type with a ratio of 44: 43 % and the remainder was made up of sand and gravel; in general, a higher metal content would be expected at these three sampling points (Burdige, 2006; Szava-Kovats, 2008; Belabed et al. 2013).

Figure 4. Type of sediment in the Sontecomapan Lagoon, Veracruz. 1991-1992.

36Correlations were made with all the registered data and were significant between silts or clays and organic carbon were obtained as shown in Figure 5, which point out towards the existence of a depositional environment enabling for the accumulation of metals at specific sites (6, 8, 9 and 10); it should be noted that the sands and OC show a significant inverse correlation (r=-0.9376, p=0.0006) agreeing with what is reported in literature; with gravel, no relationship was found probably due to the small amount found.

Figure 5. Correlations between silts and OC (a), and clay and OC (b) in sediments of Sontecomapan Lagoon, Veracruz. 1991-1992.

Calcium Carbonate

37The values of this sedimentary component were low in the lagoon because at Sontecomapan it can be in the form of colloids which prevented its detection in this study, since in all samples it was < 0.30 %. It has been reported that low carbonate content in sediments may indicate a terrestrial origin or a siliciclastic type (Vallejo-Toro et al. 2016).

Total Metals

38The criteria for evaluating sediment quality assessed in a wide study from the mid-90s by a group of Canadian and American researchers (Long et al. 1995), have become the benchmarks to assess potential or actual risk that the content of various elements and compounds represent to the benthic community. International government entities as the US Agency of the Atmosphere and Ocean (NOAA), established a reference guide to assess possible biological damage from toxic substances accumulated in the sediments of aquatic ecosystems (Buchman, 2008). Thus, there are two critical values, the ERL (effects range low values) whose value indicates a low probability of causing alterations on biotic benthic species and ERM (effects-range median values) concentration from which the deleterious effect on these organisms occurs; this means that a value with magnitude between ERL and ERM has a chance of benthic damage.

39Figures 6, 7 and 8 show the variability between periods and stations for the total concentration of the seven metals on Sontecomapan sediments. Copper (Cu) showed the highest level at site 9 with 131 μgg^-1 during the rains of August, 1992 while the minimum was 1.1 µgg^-1 at site 2 during “Nortes” season in November, 1991; most of sedimentary total Cu was < 80 μgg^-1. Overall, 43.5 % of the sites had Cu concentrations > ERL (34 μgg^-1) (Fig. 6) where point 9 already mentioned the most likely alteration to the benthos.

40For cobalt (Co) no sediment quality criteria is yet established. However, its records in this study showed concentrations around 35-45 μgg^-1 with the exception of the rainy season and “Nortes” 1991 where values decreased below the analytical detection limit (Fig. 6).

41Chromium (Cr) showed its highest level at site 10 with 150.6 μgg^-1 during the rainy season (July, 1991), and the minimum of 14.7 μgg^-1 towards the end of this climatic period in September of the same year. When compared to the criteria for sediment quality, 41.3 % of Cr concentrations exceeded the guideline value of ERL of 34 μgg^-1, mainly in stations 6 8, 9 and 10 but without exceeding the upper ERM of 370 μgg^-1 (Fig. 6).

42Total nickel (Ni) concentrations are in the range of 3.07 to 269.6 μgg^-1 at 4 sites during the dry season of 1992 and 2 sites in the rainy season of July, 1991, respectively. The levels found in this study show a worrying situation regarding the biological risk posed by Ni stored, since 13 % (6 sites) of the records were in the range ERL<concentration<ERM, while 50 % of the data were > ERM (51.6 μgg^-1) which means a real biological risk and inherent ecological impact to the benthos; the magnitude of total Ni concentrations decreased by 1992, mainly in the rainy season (August), as even non-detectable data were obtained from 17.4 % of sediment sampling sites (Fig. 7). Total concentrations of zinc (Zn) did not exceed the lowest quality criteria for sediment ERL (150 μgg^-1) and

Figure 6. Total concentrations of Cu, Co and Cr in surface sediments of Sontecomapan Lagoon, Veracruz. 1991-1992.

Figure 7. Total concentrations of Ni and Zn in surface sediments of Sontecomapan Lagoon, Veracruz. 1991-1992.

43Total cadmium (Cd) concentration showed quite uniform values, with a minimum of 0.3 μgg^-1 at site 7 in September, 1991 and a maximum of 2.7 μgg^-1 in sampling point 10 during “Nortes” (November, 1991) (Fig. 8). Cd was undetected in 40 % of samples, six of the sites evaluated had levels <ERL (1.2 μgg^-1) while 50 % was ERL<concentration<ERM with a probability of actual benthic damage in most cases.

44The lead (Pb) concentration ranged between 2.77 (site 5; August, 1992) and 48.2 μgg^-1 (site 6; July, 1991). Most data were <ERL (46.7 μgg^-1), only point 6 mentioned above surpassed this guide level, and close to it were the concentrations found in sites 8 and 10 in the rainy season of 1991 and at three sites values were under the detection limit (Fig. 8).

45The mean values for the concentrations of the seven metals determined in the sediments of the Sontecomapan Lagoon, Veracruz, are summarized in Figure 9; Cr, Ni and Zn had the highest levels in decreasing order, followed by Cu, Co and Pb, being Cd the one that recorded the lowest average value of the whole study. The three dominant metals are likely to be derived from human activities in areas surrounding the lagoon system such as the use of agrochemicals that have metals in their molecules and manufacturing processes, chronic supply of crude oil that contributes to the presence of nickel as well as emissions by the engines of the fishing and tourist boats in the study area.

Figure 8. Total concentrations of Cd and Pb in surface sediments of Sontecomapan Lagoon, Veracruz. 1991-1992.

Figure 9. Total concentrations of metals in surface sediments of Sontecomapan Lagoon, Veracruz. Mean values. 1991-1992.

46In order to estimate the intrinsic toxicity of sediments in a global way due to the metal assembly contained in this environmental matrix, it is recommended to use the mean Sediment Quality Guideline Quotients (mSQGQ) which is calculated using the individual concentrations quotients of the elements determined in relation to the concentration established in the sediment quality guides already mentioned, particularly ERL of each metal (Long et al. 2006); the result is a single, unitless, effect-based index of the relative degree of contamination that can provide a basis for determining the likelihood that a sediment sample would be toxic to sediment-dwelling organisms. Accordingly, mSQGQs provide several advantages for the interpretation of complex mixtures of potentially toxic substances in sediments significance (Wang et al., 2016).

47To estimate this indicator of environmental quality for the Sontecomapan sediments, only six metals over the seven recorded have been considered since the Co does not have its quality criterion of ERL sediments (Long et al., 1995). The mSQGQ overall valueof the integrated metal assembly was 1.05 and compared with the reported experimental and statistical data for the incidence of significant toxicity for test organisms of estuarine and marine environments (Ampelisca abdita and Rhepoxynius abronius), was between 55-60 % and classified as ecological risk from medium to high (Wang et al., 2016); this ecotoxicological tool can be used to establish a concentration/response relation for a specific site and to be able to identify the toxicological risk that exists that can be acceptable or not, since as the magnitude of the mSQGQ increases the incidence of toxicity and mortality (Long et al. 2006).

48However, it is important to note that at the individual level, Ni had the highest total concentration/ERL sediment quality guideline (C_T/ERL) ratio with 2.90 classified as high ecological risk, followed by Cu (C_T/ERL=1.12 medium/high risk), Cr (C_T/ ERL=0.93 medium risk), Cd (C_T/ERL=0.75 medium risk) and for Zn and Pb was 0.29 classified as medium/low risk (Wang et al., 2016) this pattern is very important to establish the metals of greatest risk for the ecosystem under study and to be able to define the required mitigation actions required to reduce the environmental impact of these substances.

49Statistical analysis of the various sedimentological parameters and total concentrations of metals can provide important information about the origin of these substances and their accumulation patterns in a specific ecosystem. Table 3 shows the linear correlation coefficient between sedimentological parameters and the total concentration of the seven metals determined in this study.

50It can be observed that Cu had good relationship with organic carbon (r=0.9380) and Zn (r=0.9554), both essential metals for various metabolic pathways. Co showed a significant correlation coefficient with Cr (r=0.9310) and Zn (r=0.9588). Cr had also a significant relationship with organic carbon (r=0.9131) and Zn (r=0.9415). We must highlight the fact that Ni and Cd showed no significant correlation with any metals or sedimentological parameters. Zn and OC had a significant direct relationship (r=0.9289). Pb correlations were recorded with a lower degree of significance with OC, Co and Cr (coefficients of 0.8055, 0.8360 and 0.8528, respectively).

Table 3. Linear correlation coefficients between the sedimentological parameters and the total concentration of metals in the Sontecomapan Lagoon, Veracruz. 1991-1992. Bold values mean significant correlations (p<0.05).

51Sediments are the final recipient of whatever reaches coastal ecosystems and store it for a long time; both beneficial materials like nutrients and risk pollutants such as Cd, Pb, Hg and pesticides, play a significant role in sustainability of food supply for the biological communities that inhabit them as well as to become a secondary source of dangerous substances (Bodin et al. 2013). Because of this, the analysis of coastal sediments continues to be a very useful tool to evaluate contamination by metals in these ecosystems since the recording of these elements high concentrations indicates anthropogenic impact rather than natural contributions due to phenomena of geological weathering (Memet, 2011).

Bioavailable Metals

52Recent environmental sciences research have aimed to study the chemical speciation of metals in order to better explain distribution, mobility and especially the bioavailability of these elements to ascertain whether the concentrations are determined by these processes and existing factors in the ecosystem (Zemberyová et al., 2007). Metal solution is one of the environmental processes that directly affect metals immediate bioavailability and therefore their absorption and uptake by the biota and their deposition in the sediments after sedimentation or death (Owsianiak et al., 2013, 2015; Chiappetta et al., 2016). The evaluation of the bioavailability of metals in coastal sediments is a very important aspect since it provides information to predict the environmental and toxicological impact of these substances because this chemical fraction is the one that can be solubilized during the process of digestion in organisms and metals can be absorbed by different metabolic pathways and accumulate in various tissues such as liver, kidney, muscle and skeletal, among others, causing different sublethal effects of reproductive or growth type as well as acute effects including death (Tumer and Olsen, 2000).

53In this regard, the content of the sedimentary bioavailable metal fraction of the Sontecomapan Lagoon, was evaluated holistically, i.e., without obtaining specific phases as the aforementioned. Figure 10 shows the distribution of bioavailable Cu, Co and Zn concentrations. Cu had the highest concentrations (>20 μgg^-1) in sites 4, 5 and 6 of the samples corresponding to rains (August, 1992) and the lowest (<1.0 μgg^-1) in the dry and rainy seasons of 1991.

54Comparatively, Co was more uniform, with values around 1 to 6 μgg^-1 with the exception of the sampling sites 9 and 10 in March, 1992 with concentrations >10 μgg^-1. For bioavailable Zn, considered an essential element, the pattern was similar to that shown for cobalt, the substantial difference was the very high concentration found at site 2 in March, 1992, which had high levels (11.87 μgg^-1), that did not occur for Co (3.29 μgg^-1) (Fig. 10).

55The detected pattern for Cr and Ni (Fig. 11), may represent a biohazard due to both its chemical form and the magnitude of their concentrations. Overall, Cr had uniform values, with an increasing trend in 1992 and levels <5.0 μgg^-1, with the exception of sediments from sites 8, 9 and 10 collected in March, 1992 (dry season). Nickel presented a heterogeneous pattern, as its concentrations decreased to be less than the detection limit in 1992 when data could be recorded only in sites 9 and 10, whereas the maximum was obtained, with 12 μgg^-1, at site 9 in August, 1992. The bioavailable concentrations of Cd and Pb (Fig. 12) showed a similar distribution. They were undetectable in 1991 and could only be detected in 1992, but at concentrations higher than those of cadmium. This situation is to be highlighted because, naturally, this metal comes in smaller levels than those of Pb for total concentration (<3.0 μgg^-1), a scenario that was reversed for the bioavailable fraction.

56Correlation coefficients between bioavailable metals and sedimentological parameters are presented in Table 4. For organic carbon the highest correlation was with Cr (r=0.9383) and second with Zn (r=0.8504). Co and Ni were also highly correlated (r=.9440), followed by the Co-Zn relationship (r=0.8653); it should be noted that an unexpected relationship was detected for Pb-Ni since it was of inverse type (r=-0.8588), which is not commonly found in these metals behavior. It can be said that desorption mechanisms of Co, Ni and Zn at low pH condition caused by a weak acid environment are similar in comparison with what may occur to Pb evidenced by the inverse correlation obtained with Ni.

Figure 10. Bioavailable concentrations of Cu, Co and Zn in surface sediments of Sontecomapan Lagoon, Veracruz. 1991-1992.

Figure 11. Bioavailable concentrations of Cr and Ni in surface sediments of Sontecomapan Lagoon, Veracruz. 1991-1992.

Figure 12. Bioavailable concentrations of Cd and Pb in surface sediments of Sontecomapan Lagoon, Veracruz. Cycle 1991-1992.

57The adsorbed metals at sediments in their labile form represent the chemical fraction of greatest risk for biota because they can cause sub-lethal effects at population level in the majority of the species that come in contact with these chemical forms, mainly toxic elements like As Cd, Pb, As, Hg, V and Cr. Examples of these effects are the inhibition of the enzymatic activity of acetylcholinesterase in clams and mussels, oxidative DNA damage on bivalve gills, and vertebral deformities in various species of fish (Zaaboub et al. 2015).

58Coastal ecosystems are large receivers of harmful substances, including metals, which come from several sources of industry and that acquire environmental relevance due to their accumulation in the sediments of these natural areas where they can be enriched and become a secondary source of contaminants. Most of the metals accumulated in the sediments form complexes with the fine particles, with the existing organic matter, with the Fe and Mn oxides and may be bioavailable for benthic biota or for detritivorous organisms, thus representing a toxicological risk to cause biological damage from sub-lethal to deadly in the food web (Nethaji et al., 2017).

Table 4. Linear correlation coefficients between the sedimentological parameters and bioavailable metal concentrations in the Sontecomapan Lagoon, Veracruz. 1991-1992. Bold values mean significant correlations (p<0.05)

Metals in Organisms

59Four species of organisms present in the Sontecomapan Lagoon, Veracruz, were assessed during this study. The Cladophoropsis membranacea algae was obtained from sites 1, 4, 5 and 6 in March, 1991 and site 9 in August, 1991. Seagrass Ruppia maritima was collected at the sampling stations 6 and 7 during dry and Nortes, 1991. The oyster Crassostrea rhizophorae was collected from site 3 of the two 1992 collections and the mussel Brachidontes exustus was sampled at sites 7 and 9 in March, 1991 and at sites 6 and 7 in rain and Nortes, 1991 and August, 1992. The bioconcentration factors (BCF) were calculated for the submerged vegetation and the bivalves due to their close relation with the sediments from the following relation:

60BCF = Corganism / Csediment. It has been established that the BCF value represents the sessile species efficiency to absorb a certain element of the sediments and to accumulate it in their tissues, reason why high values of BCF mean a greater capacity of bioaccumulation (EPA, 2007).

61In Figure 13 the results of the seven metals on the two species of submerged vegetation are analyzed; it can be seen that the Zn found in C. membranacea algae had the highest level with 66.7 μgg^-1 for organisms collected at site 5 during March, 1991, which contrasts with the 18 μgg^-1 value recorded for the seagrass at a nearby site (station 6) in the same sampling time. The content of potentially toxic metals, Cd and Pb were comparable for both species.

Figure 13. Content of total metals in submerged vegetation of Sontecomapan Lagoon, Veracruz. 1991-1992.

62In recent years the need to have more organisms that function as biomonitors has been recognized, in order to know if the concentrations of certain substances such as metals mean an toxicological risk for ecosystems. Aquatic vegetation provides information on current conditions of the metals bioavailability and also provides historical data on the past environmental characteristics at a lower cost than water and sediment analyses which require study of complete sedimentary cores. When determining the concentration of metals in the vegetation, bioavailability of toxicological relevance and actual signs of environmental disturbance can be known (Bonano & Di Martino, 2016).

63Seagrass provide comprehensive data on the ecosystem physicochemical and biological parameters where marine phanerogams inhabit and are recognized as suitable organisms for biomonitoring of trace elements (Lewis & Devereux, 2009). Similarly, seagrass has been used to trace metal contamination and, as this process of coastal disturbance has increased in developing countries, it is necessary to continue with bioindicators of this type of submerged vegetation as these plant species are able to provide information on alteration by metals of specific sites by point sources as well as integrate periods where metal discharges have occurred at local and global scale. Govers et al. (2014) conducted a meta analysis to compile this benchmark of global trace metal concentrations in seagrass leaves; the values of metals that they found for the majority of the seagrass species that were included in their compilation, were, for Cd 0.1-10 μgg^-1, for Cu and Pb 5-80 μgg^-1, for Cr 0.5-50 μgg^-1, for Ni 1-100 μgg^-1 and for Zn 5-500 μgg^-1; comparatively, the levels of these metals recorded in this study for R. maritima were low, close to the lower limit reported by these authors. Brito et al. (2016) reported concentrations of several metals on the Halodule wrightii seagrass in Brazil; the average values of Cd, Cr and Cu for R. maritima from Sontecomapan lagoon were higher while those of Ni, Pb and Zn were lower than those of the Brazilian species.

64Another important aspect of including aquatic vegetation in metal contamination assessments is the fact that these species, as primary producers, contribute to nutrients and energy and can transfer their stored metal content by initiating the biomagnification process (Govers et al., 2014). In photosynthetic organisms, toxic metals such as Cd, Cr, Pb, V, As, Hg and others, cause alteration on the photosynthetic mechanism as they decrease the pigments responsible for photosynthesis and damage the process reactions occurring in the presence of light and in obscurity, the membrane structure of chloroplasts and above all, alter the electron transport, lipid metabolism and energy decrease in plants (Navarro-Aviño et al., 2007; Kumar et al., 2014).

65Figure 14 shows the results of metal concentrations in the two bivalve species. The highest contents of Zn and Cu were recorded in the oyster C. rhizophorae with maxim of 265 and 29.3 μgg^-1 respectively at site 3 in March, 1992, while for the mussel B. exustus recorded the highest contents were 46.62 and 15.1 μgg^-1 respectively. Co, Cr and Ni showed a reverse pattern, as B. exustus had the highest (31, 40.2 and 6.28 μgg^-1, respectively); Cd and Pb concentrations were similar. Differences in concentrations of Cu and Ni among similar bivalves species have already been reported in other studies, indicating that they could be significant and surprising; the best-known examples are the differences of metal concentrations in mussels and oysters collected simultaneously at the same locations by the National Status and Trends Programs and the concentrations of Ag, Cd, Cu, Ni, Zn, which tend to bind with the S-containing ligands (e.g., proteins), are typically much higher in American oysters (Crassostrea virginica) than in mussels (Mytilus sp.), whereas the concentrations of Se, Pb, Hg, Cr, and As in mussels are higher than those found in oysters collected from the same sites (Wang, 2009; De Souza et al. 2016).

Figure 14. Content of total metals in bivalve mollusks at Sontecomapan Lagoon, Veracruz. Average values. 1991-1992.

66High Cu content in bivalve species (Mussels 12-698 µg g^-1; Scallops 3.3-9 µg g^-1) is normal since Cu is an essential element and is present in hemocyanin, the blood pigment of these invertebrates, vital for respiration and oxygen transport (Lino et al., 2016). Thus the high concentrations found in this study (4.21 µg g^-1 for B. exustus and 25.72 µg g^-1 for C. rizophorae) can be considered as normal due to the essentiality of this element. The case of Zn, another essential metal for bivalves, is similar to that of Cu, since the content of this element is high in mollusks and plays an important role in the composition of approximately 90 different enzymes of mussels, which justifies significant Zn levels in mollusks from pristine areas (Lino et al., 2016); and in this work, there also were differences between the content of Zn recorded in the oysters and the mussels of Sontecomapan Lagoon, being higher in C. rizophorae (172.9 µg g^-1) than in B. exustus (15.1 µg g^-1).

67For several decades, bivalve mollusks and other invertebrates have been included in long-term environmental monitoring programs as they accumulate different hazardous substances to a greater extent than other constituents of coastal ecosystems, mainly due to their filtering behavior. Since they are sessile or sedentary organisms, bivalves can provide greater spatial integration than sediment and provide information to identify sources of bioavailable metals. In addition, the metals that these organisms accumulate can reach toxic concentrations and cause biological and ecological damage (Bai et al., 2011). Toxic metals such as Cd, Pb, As accumulated in the tissues of these species can cause from poisoning to decreased fertility, damage and cell death, alteration of various organs and death (El Nemr et al., 2012).

68With the full concentrations of metals in organisms, Figure 15 was constructed for global comparison purposes, using the average values for each of the vegetation and bivalves species tested. This allows comparative evaluation of accumulated metal contents since these biota are sessile, permanently exposed to environmental conditions where they live, including exogenous materials of anthropogenic origin, although some metals may be essential, changing their chemical state and attaining potentially harmful concentrations. Zn present in C. rhizophorae oyster tissue ranked with 173 ± 129.7 μgg^-1 while others metals were <25 μgg^-1 Co and Ni had their highest average concentrations in widgeon grass with 13.51 ± 8.7 and 3.7 ± 1.5 μgg^-1, respectively, while the average Cu peaked in the C. rhizophorae oyster with 25.7 ± 5.05 μgg^-1 and Cr recorded its highest average value in the B. exustus mussel with 13.7 ± 9.93 μgg^-1, followed closely by widgeon grass with 8.21 ± 2.27 μgg^-1 (Fig. 15).

Figure 15. Content of total metals in organisms Sontecomapan lagoon, Veracruz. Average values. 1991-1992.

69Table 5 compares the bioconcentration factors (BCF) obtained for the four species of organisms. The C. membranacea algae showed lower BCF values than seagrass for Co, Cr, Ni and Cd whereas for Cu, Zn and Pb BCF was higher in chlorophyte than in marine phanerogama; we must highlight the Co BCF value close to 1 in R. maritime, which means that there is practically the same proportion of metal in the sedimentary matrix than in this plant tissue whereas for nickel the low BCF value revealed a very low accumulation. In the case of bivalve mollusks, C. rizophorae had high BCF values for Cu (1.17) and Zn (17.57), the latter being of a very high magnitude recorded in the dry season of 1992, probably because this metal is highly used for the formation of its shell. B. exustus mussel concentrated higher amounts of toxic metal Cd (2.21) than the oyster which represents a risk to the ecosystem and consumers of this species, since cadmium is currently considered carcinogenic to humans (IARC, 2011).

Table 5. Bioconcentration factors (BCF) of metals estimated for the organisms analyzed in the Sontecomapan Lagoon, Veracruz. 1991-1992

70When organisms absorb heavy metals from the surrounding environment, metabolic mechanisms are initiated to excrete and detoxify them in the case of toxic metals or if the essential elements are in high concentrations in order to avoid harmful effects. Indeed, metals that exceed the amount for the metabolic requirements as well as the accumulation capacity of the species become dangerous, the risk is low or does not exist when the biota stores metals in non-toxic chemical forms. Therefore, the bioaccumulation of metals is a complex process, since there are multiple factors involved such as life stage, biochemical pathways, sediment physicochemistry, type of exposure and biological mechanisms to detoxify and regulate them. However, the tissue content of metals in species is a good measure of these elements bioavailability towards organisms and has long been proposed as a good predictor of metals toxicity in the environment (Fukunaga & Anderson, 2011; Wang et al., 2016).

71The bioavailability and potential for bioaccumulation and biomagnification of metals in ecosystem compartments are high. For many species such as bivalve mollusks, ingestion is the main route for acquiring these substances from their environment and at the same time, transferring the metals load through the food chain, making clear the importance of understanding the contaminants dynamics in aquatic environments (Mendoza-Carranza et al., 2016).

Conclusions

72The highest total concentrations of metals found in the surface sediments of the Sontecomapan Lagoon were for Cr, Ni and Zn, the first two considered as toxic metals and the latter being an essential element for various biochemical pathways. A large number of total concentrations recorded were higher than the sedimentary quality criteria with a low probability of causing benthic damage, except for Ni since most of the results were higher than the established high probability concentration that cause biological alteration to benthos. The Pb had levels higher than those recorded for Cd in their total concentration, both at the threshold limit to disturb the benthic species. The bioavailable fraction evaluated in the lagoon sediments had an expected pattern since the essential metals were recorded throughout the study cycle while the potentially toxic ones such as Cd and Pb were only detected in the final collections at low concentrations. The content of the metals studied in the various species analyzed showed that marine phanerogams bioaccumulated more than algae and oysters and had a higher content of the essential metals Cu and Zn, while mussels stored at higher levels potentially toxic elements such as Cr and Ni, while the concentrations of Cd and Pb were low in both vegetation and bivalves. The obtained bioconcentration factors showed that sediments are an important source of metals for the oysters, mainly Zn, Cu and Cd and to a lesser degree for mussels and marine phanerogama, for which the monitoring of metals must be maintained through bioindicators analysis and recent sediments in this Mexican lagoon ecosystem.