Assessment of Heavy Metal Pollution of the Peter the Great Bay (North-West Pacific Region) Using Brown Algae

According to the content of heavy metals Fe, Mn, Cu, Zn, Pb, Cd and Ni in brown algae Sargassum miyabei from the Peter the Great Bay of the Sea of Japan, geochemical factors were calculated. The algae geochemical anomaly index (I GA ) characterizes the degree of excess of the background concentrations of metals. The heavy metal pollution factor (F p ) is used to estimate the degree of pollution of the marine environment with heavy metals. The Peter the Great Bay has a low level of heavy metal pollution, but some parts of second-order bays, such as Amurskii Bay, Ussuriiskii Bay and Vostok Bay, have a moderate degree of pollution. The high pollution level was registed on the western coast of the Ussuriiskii Bay near the Vladivostok city landfill. Thirty percent of sampling stations were noted to have higher threshold levels of metals in the algae. These areas need to be monitored to assess their environmental status and measures should be applied to reduce the impact on the environment.


Introduction
The heavy-metals pollution of the marine environment is the pressing problem.
The basis line in the solution of this problem is a decrease in income of contaminants from the main sources of pollution as well as a getting the positive balance between assimilatory capacity of the coastal ecosystem and intensity of the pollution supply (Israel, 1989). Monitoring of the environment is a basis for base Nakhodka Bays are situated further east.
The Tumen River flows into the Sea of Japan on the south boundary of the Peter the Great Bay. Predominance of the southward Primorski Current causes a transportation of the river discharge to the shores of the Korean Peninsula and reigns in the influence of the Tumen River flow on the Russian coastal waters (Shulkin & Semykina, 2012). The Razdolnaya, Partizanskaya Rivers and a great number of small rivers flow into the PGB.
The total area of the Peter the Great Bay catchment basin is 23,800 km 2 . About a half of this territory is occupied by forests (10,095 km 2 ) and protected natural areas (1157 km 2 ).
Within the PGB catchment basin reside, 1.3 million people. Here, the cities of Power, machinery production, woodworking, chemical, textile, food industries, construction and agriculture are basic industries on the territory of the PGB catchment basin. The amount of wastewaters produced within the catchment basin has reduced from 620 million tons in 1990 to 290 million tons in (Brief…, 2016. The main reason of the wastewater amount reduction is a decline in the industrial production since 1990s. Figure 1. Formulas of the geochemical coefficients: I GA -algae geochemical anomaly index, and F p -heavy metal pollution factor. Notations: C i is concentration of i-metal in S. miyabei, С med is the background concentration of metal which is equal to median of metal concentrations in the shared dataset for S. miyabei from the north-western Sea of Japan (Kozhenkova & Chernova, 2018), N is the number of elements used for index, С UT is the threshold concentration of metal for this type of algae calculated earlier (Chernova & Kozhenkova, 2016) as a median plus double median of absolute deviations from median (Ме + 2МАD); а i is the danger coefficient of i-element depending on danger class of element: а = 2.5 in case of I danger class, а = 1.5 in case of II danger class (Cd, Pb), а = 1.0 in case of III danger class (Cu), а = 0.5 in case of IV danger class (Fe, Mn).

Materials and Methods
(2012), south-western part of the Peter the Great Bay and around Russki Island (2016) were used (Kobzar & Kristoforova, 2015;Khristoforova, Gamayunova, & Afanasyev, 2015;Khristoforova & Kobzar, 2017;Khristoforova, Emelyanov, & Efimov, 2018). The stations of macrophyte sampling by the authors of this paper and our colleagues have intersected and, thereby, a total number of points of macrophyte sampling in the Peter the Great Bay reaches 84 stations. if F p = 0.81 -3.5, or as high if F p = 3.51 -7.5, or as heavy pollution if F p > 7.5 (Kozhenkova & Chernova, 2018).

Results
In total I GA varied in a range of 0.3 -7.5, and 50% of values (percentile 0.25 - Mn contribution the source of which is the Vladivostok landfill. In Strelok, Vostok and Nakhodka Bays, the stations with I GA > 2 were also revealed. At the same time, the values of I GA at stations in Kievka Bight and south-western Peter the Great Bay were not increased. Heavy metal pollution factor (F p ) at different stations in PGB coast has varied in a range of 0.2 -4.7, a percentile Р 85 was equal to 1.0, thus the mean value of F p = 0.55. This characterizes the degree of pollution as low.
The water pollution in different parts of the Bay varies from light (south-western part) to moderate one (Amurskii Bay and Ussuriiskii Bay) (Table 1).

Discussion
The determination of the space structure of pollution differentiating the territory with respect to level of ecological hazard is the crucial task of the geochemical surveys of environment.
The main routes of metals to the marine environment are river runoff and atmospheric deposition (Shulkin, 2012).  (Cantillo, 1998;Reinmann, Filzmoser, & Garrett, 2005;Lukashev, 2007;Zalewska & Danowska, 2017). In many countries, the health-based exposure limits were approved for determining the safety in use of bioresources but they are not in line with goals of maintaining the stability of ecosystems.
The degree of environmental hazard of territory and water area can be determined using the different kinds of combined and/or integrated pollution indices.
The international Metal Pollution Index (MPI) proposed by J. Usero with coauthors (1996), in its current form, only allows to compare the global trace metal pollution between the different monitored sites of a specific survey, for a given species (Richir & Gobert, 2014). Hereafter, two new adapted indices-TESVI (Trace Element Spatial Variation Index) and TEPI (Trace Element Pollution Index)-which were based on account of the statistically average values-mean standard deviation, maximum and minimum values of metal concentrations in a dataset were proposed (Richir & Gobert, 2014).

S. Kozhenkova, E. Chernova Journal of Geoscience and Environment Protection
Based on the study of C. Reinmann with coauthors (2005), we have calculated the background and threshold heave metal concentrations in algae of the coastal part of the Sea of Japan (Chernova, 2012;Chernova & Kozhenkova, 2016), as well as for Okhotsk Sea, White Sea and South China Sea (Chernova & Khristoforova, 2012).
Brown algae are the integral indicators of heavy metal pollution in the coastal waters (Rainbow & Phillips, 1993;Vasquez & Guerra, 1996;Shulkin, Chernova, Khristoforova, & Kozhenkova, 2015;Chernova & Kozhenkova, 2016;Pan, Wernberg, de Bettignies, Holmer, Li, Wu et al., 2018). Biogeochemical coefficients reflect the features of the microelement composition of the brown alga S. miyabei in the different localities or within a "separate" water area (Table 1, Table 2). A value of I GA (algae geochemical anomaly index) assesses the features of the content of the metal complex in algae with respect to the background conditions. As the background concentration, the median of the dataset with the excluded statistical outliers was used. Therefore, I GA =1 corresponds to the background level of metals in the alga. If a value of I GA < 2, the algae grow in the environment with natural level of metal content (Chernova & Kozhenkova, 2020).
However, at I GA > 2, the anthropogenic effect on the entry of metals to the marine environment becomes deciding. In the Peter the Great Bay, the stations with I GA > 2 are located on the eastern coast of the Amurskii Bay and western coast of the Ussuriiskii Bay and related to heavy metal pollution from the industrial and municipal sewage waters of Vladivostok, washout of pollutants on the town landfill territory and effect of the port. In the Strelok, Vostok and Nakhodka Bays, the stations with I GA > 2 are located near ports and outlets of polluted wastewaters from populated areas. Different metals are characterized by different toxicities for the marine organisms (Chu & Chow, 2002;Golovanova, 2008;Mebane, Hennessy, & Dillon, 2008). Heavy metal pollution factor (F p ) characterizes the enrichment of algae with heavy metals with respect to the threshold levels and with consideration for the hazard class for marine organisms. All the chemical substances in the fishery water bodies were separated into 4 hazard classes (Fe, Mn-4;Cu, Zn, Ni-3;Cd, Pb-2;Order…, 2016). The stations with the largest values of Fp are rated as most dangerous from the toxicological standpoint for the marine biota. Therefore, the measures related to reducing the volumes of metal entry to the coastal seawaters in such areas should be carried out in the first place.
According to F p value for S. miyabei the pollution degree of PGB water areas is rated as low. Different parts of the second-order bays, such as Amurskii, Ussuriiskii and Vostok Bays, have a moderate degree of pollution ( Figure 2, Table   2). The high pollution level was determined on the western coast of the Ussuriiskii Bay near the Vladivostok city landfill ( copper in the BSs of these water areas exceed 10 and more times the background level (Shulkin, 2004). The brown algae S. miyabei were not found within the Port of Vladivostok, so we have not data on heavy metal concentration in the ma-