Polycyclic Aromatic Hydrocarbons in Soil and Vegetation of Niger Delta, Nigeria: Ecological Risk Assessment

The Niger Delta, Nigeria, is noted for crude oil exploration. Whereas there seems to be a handful of data on soil polycyclic aromatic hydrocarbon (PAH) levels in this area, there is a paucity of studies that have evaluated soil and vegetation PAHs simultaneously. The present study has addressed this information gap. Fresh Panicum maximum (Jacq) (guinea grass), Pennisetum purpureum Schumach (elephant grass), Zea mays (L.) (maize), and soil samples were collected in triplicate from Choba, Khana, Trans-Amadi, Eleme, Uyo, and Yenagoa. PAHs determination was carried out using GC-MS. The percentage composition of the molecular weight distribution of PAHs, the molecular ratio of selected PAHs for identification of possible sources, and the isomeric ratio and total index of soil were evaluated. Pennisetum purpureum Schumach (elephant grass) from Uyo has the highest (10.0 mg·kg−1) PAH while Panicum maximum (Jacq) (guinea grass) has the highest PAH (32.5 mg·kg−1 from Khana. Zea mays (L.) (maize) from Uyo (46.04%), Pennisetum purpureum Schumach (elephant grass) from Trans-Amadi (47.7%), guinea grass from Eleme (49.2%), and elephant grass from Choba (39.9%) contained the highest percentage of high molecular weight (HMW) PAHs. Soil samples from Yenagoa (53.5%) and Khana (55.3%) showed the highest percentage of HMW PAHs. The total index ranged 0.27–12.4 in Uyo, 0.29–8.69 in Choba, 0.02–10.1 in Khana, 0.01–5.53 in Yenagoa, 0.21–9.52 in Eleme, and 0.13–8.96 in Trans-Amadi. The presence of HMW PAHs and molecular diagnostic ratios suggest PAH pollution from pyrogenic and petrogenic sources. Some soils in the Niger Delta show RQ(NCs) values higher than 800 and require remediation to forestall ecohealth consequences.

Te environmental persistence and public health importance of PAHs in recent years have attracted global attention [14][15][16]. Te principal sources of PAHs in diferent environmental matrices (soil, water, atmosphere, and food) are natural sources and anthropogenic processes including diverse industrial activities, especially those involving incomplete combustion of coal. Similarly, crude oil and petroleum manufacturing process also produce signifcant amounts of PAHs [17][18][19].
Although the uptake of PAH by leaves is mainly by gaseous deposition [20], some reports have demonstrated that leaves can accumulate PAHs from contaminated soils through their roots [21][22][23]. Nevertheless, Su and Zhu [24] suggested that the PAHs transported from roots to shoots may be negligible, with other researchers afrming that atmospheric PAHs are dominant contributors to the total PAHs in leaves [25,26].
Long periods of crude oil exploitation in many countries have led to complex contamination by petroleum hydrocarbons and PAHs in many cities. For instance, some studies from China have reported an average content of 16 PAHs ( 16 PAHs) of 1840 μg/kg in Daqing street dust [27]. All in all, it is known that the pollution efects of PAHs on ecological land in oilproducing cities and surrounding communities have great signifcance on urban ecological security and environmental health [28,29]. Te Niger Delta area of Nigeria is one of the major crude oil-exploring regions in the world with inundated cases of oil spills, aerial deposition of organic by-products originating from fared gases and massive environmental degradation by both inorganic and organic pollutants like PAHs [10]. Some researchers have reported concentrations and compositional patterns of PAHs that can be employed in understanding the efects, sources, fate, and transport of PAHs in soils, as well as environmental quality management in the Niger Delta, Nigeria [30,31]. PAHs strongly accumulate in the food chain and are subsequently transferred to humans, thereby posing a threat to human health [32,33]. Some skeletal surveys of PAHs in agricultural soils have been carried out in Niger Delta [34][35][36]. Some of these surveys suggest that some agricultural soils in the Niger Delta, Nigeria, sufer from PAH pollution due mainly to point source pollution. Surface and underground water are polluted with PAHs in Nigeria [37,38]. PAHs can transfer from soil to borehole water [39]. Although some studies have reported soil and vegetation PAH contamination, information remains sparse on PAH contamination of both soils and vegetation from the same location [40]. Understanding of the spatial distribution of PAHs in agricultural topsoil is critical for environmental management and the safety of agricultural produce.
As recently discussed [41], the One Health strategy, including environmental health and food safety, can help risk assessors and risk managers in prioritising actions for the prevention and mitigation of PAH pollution and its spread and accumulation. In the present study, we evaluated the whole ecological risk of PAHs in soil and vegetation samples from farmlands in six major cities of Niger Delta, Nigeria.

Study Area.
Te Niger Delta, Nigeria, is the third largest mangrove forest and the second largest delta in the world. It falls within the central coastlands of southern Nigeria [10]. Te Niger Delta area is well known for crude oil exploration and environmental pollution. According to Okoye et al. [10], the black to greyish brown and dark grey soils are acidic with slight to moderate electrical conductivity and high organic carbon content.  Figure 1 shows the sampling sites. Te sampling, done in triplicate, was carried out during the period of mass fowering of plants, specifcally in January 2018. Soil samples were sampled from 0 to 5 cm depth as the most rootinhabited soil layer according to the US EPA Method 610 (U.S. EPA, 1977). Te sampled soil was cleaned of plant residues and other inclusions, ground in a porcelain mortar, and passed through a sieve with a hole diameter of 1 mm. Plants were dried and ground up to a hole diameter of 1 mm for analytical analysis.

Information on LOD, LOQ, and Calibration (QA/QC).
Analyses of PAHs were done using gas chromatography (6890 series and 6890 plus) equipped with a dual detector (FID-ECD), dual column, TriPlus AS autosampler with helium carrier gas, and a quadrupole mass spectrometer (Agilent 5975 MSD) based on the US EPA method 8100. Tis analytical procedure has been described previously [42][43][44][45]. Briefy, the extraction of PAHs from the samples was done with a sonicator (ultrasonic bath, Elmsonic S40H) in accordance with US SW-846 Method 3550. Two grams of either soil or plant samples were extracted with a 50 : 50 mixture of acetone and methylene chloride (analytical grade), spiked with 1 ml of PAH internal standard, and shaken thoroughly for proper mixing before being placed in an ultrasonic bath. Tereafter, 2.00 μl of each sample extracts were injected into the GC port set at column conditions: HP-5cross-linked PH-ME siloxane, length of 30 m, I.D: 0.25 mm, thickness of 1 μm with helium carrier gas set in the spitless, constant fow mode with a 1.2 ml/min fow rate. Other GC and MS operating setups were done according to the instrument's method of development as specifed in the operating instruction manual. Identifcation and quantifcation of individual PAHs were based on an internal calibration standard containing known concentrations of the 16 PAHs [43][44][45]. Te specifcity of the 16 PAHs sought in the samples was confrmed by the presence of transition ions (quantifer and qualifer) as shown by their retention times which corresponded to those of their respective standards. Te measured peak area ratios of precursor to quantifer ions were in close agreement with those of the standards. Te detection limit (LOD) is estimated as three times the background noise (IUPAC criterion). Te blank samples remained always below the quantifcation limit (LOQ). Table  S1 shows the reproducibility relative standard deviation (RSDr; n � 6), repeatability relative standard deviation (RSDr; n � 6), recoveries, linear range, LOQ, LOD, and coefcient of estimation (r 2 ).

Data
Analysis. SPSS version 17.0 software (SPSS Inc., USA) was used to perform all statistical analyses. Te data were analyzed to test for the signifcance of observed differences in the PAH content by using analysis of variance (ANOVA), while the Tukey test was used to establish if the observed diferences in the mean content of PAHs from the diferent cities were signifcant.
Te sources of the soil PAHs from diferent cities were evaluated by using PAH isomeric ratios.
Te risk quotient in ecological risk assessment is defned as the level of risk produced by a particular PAH and is estimated from the risk quotient (RQ), as shown in the following equation: where C PAHs is the concentration of certain PAHs in the soil and C QV is the corresponding quality value concentration for these PAHs in the soil. Cao et al. [46] model was adopted in order to obtain the quality value concentrations in the present study. Te negligible concentrations (NCs) and the maximum permissible concentrations (MPCs) of PAHs are two quality values employed here with corresponding risk quotients, RQ NCs and RQ MPCs , respectively, computed from where C QV(NCs) is the quality value of the NCs and C QV(MPCs) is the quality value of the MPCs of the PAHs in the soil. Te risk caused by a combination of all 16 PAHs can be appraised by calculating RQ PAHs (NCs) and RQ PAHs (MPCs) in which the values of RQ NCs and RQ MPCs of the individual PAHs that are not less than one are summed, as shown as follows: where RQ i(NCs) ≥ 1.

RQ PAHs
where RQ i(MPCs) ≥ 1. Te RQ denotes as follows: RQ NCs <1.0 indicates that the individual PAH compounds are probably of negligible concern, while RQ MPCs ≥ 1 suggests severe contamination by the individual PAH compound that requires remediation. RQ NCs ≥ 1.0 and RQ MPCs <1 indicate moderate risk posed by a single PAH compound that might require some control and remediation. However, RQ PAHs (NCs) ≥ 800 and RQ PAHs (MPCs) � 0 imply moderate risk 1. RQ PAHs (NCs) < 800 and RQ PAHs (MPCs) ≥ 1 indicate that the PAHs constitute a moderate risk 2; RQ PAHs (NCs) ≥ 800 and RQ PAHs (MPCs) ≥ 1 show a high risk of the 16 PAHs in the ecosystem. Table 1 shows the levels of PAHs in soil and elephant grass, maize, and guinea grass samples from Uyo, Choba, Khana, Yenagoa, Eleme, and Trans-Amadi. Guinea grass from Khana had the highest level of total PAH 32.5, whereas elephant grass from Uyo had the highest level of PAH 10.0. Maize samples from Yenagoa showed the highest level of PAH (9.73). Soil samples from Uyo had the highest soil total PAH (8.80). Figures 2 and 3 show the PAHs content in elephant grass 2(a), maize 2(b), and guinea grass 2(c) from diferent locations in the Niger Delta and the abundance of individual PAHs in elephant grass 3(a), maize 3(b), and guinea grass 3(c) from Choba, Eleme, Khana, Trans-Amadi, Uyo, and Yenagoa in the Niger Delta, respectively.

Source Apportionment.
Te levels of diferent PAH content in elephant grass, maize, guinea grass, and soil samples, respectively, from Choba, Eleme, Khana, Trans-Amadi, Uyo, and Yenagoa in the Niger Delta, Nigeria, are provided in Figures 2-5. Figure 2(a) shows that elephant grass from Uyo had the highest number and content of PAHs whereas Khana had the least number of PAHs and the highest content of BaA (4.22 mg·kg −1 ). Te highest content of benzo[a]anthracene (BaA) in elephant grass and dibenzo[ah]anthracene (DahA) content in guinea grass seen in Khana may be an indication of the severity of PAH pollution, and its impact on ecohealth should be further investigated. Figure 2(b) shows that the maize from Yenagoa and Eleme had a higher content of diferent PAHs than Khana which contained a fewer number of PAHs with BaA being the highest. Te lowest levels of PAHs were seen in guinea grass 2C from Yenagoa, Eleme, Choba, Trans-Amadi, and Uyo. Guinea grass from Khana, Niger Delta, contain all the PAHs and highest levels of Acy (11.9 mg·kg −1 ) and BaP (11.1 mg·kg −1 ) in comparison to other locations in this study (Figure 2 A comparison of the total soil PAH levels (mean and ranges) from diferent countries and present study is shown in Table 2.
Te PAH concentrations of agricultural soils from Choba, Eleme, Khana, Trans-Amadi, Uyo, and Yenagoa, Niger Delta, were 7417, 6787, 6325, 7972, 8799, and 7394 μg·kg −1 , respectively. Tese PAH levels were higher than most of the soil PAH levels from other countries [61,69,70]. Figure 6 shows the total PAHs for the diferent samples from diferent locations in the Niger Delta of which Uyo has the highest (10.016 mg·kg −1 ) in elephant grass and Khana has the highest PAH (32.508 mg·kg −1 ) in guinea grass and the least in all the other samples. Vegetal levels (2.698 maize-32.508 mg·kg −1 elephant grass) of PAHs were higher than soil sample levels (6.325-8.799 mg·kg −1 ).
Based on the number of rings or molecular structure, the priority PAHs are classifed as follows: low molecular weight (LMW) PAHs, i.e., Naph, Acy, Acen, Flu, Phen, and Anth (containing two and three rings), medium molecular weight (MMW) PAHs, i.e., Flan, Pyr, Chry, and BaA (with four rings), and high molecular weight (HMW) PAHs, i.e., BbF, BkF, BaP, IP, DBahA, and BghiP (with fve and six rings) [71]. Te percentage composition and molecular weight distribution of PAHs in vegetation, i.e., elephant grass, maize, and guinea grass and soils from Uyo, Choba, Khana, Yenagoa, Eleme, and Trans-Amadi in the Niger Delta, Nigeria, are shown in Table 3 Figure 7 shows the diferent distribution of PAHs according to their molecular weight: for Uyo, maize has more HMW while in guinea grass, elephant grass, and soil samples, LMW was more abundant. For Choba, samples of elephant grass and maize contain more HMW while guinea grass and soil samples have more LMW. For Khana, elephant grass and maize have more MMW PAH and HMW PAH in soil samples. Te same trend follows in Yenagoa, Eleme, and Trans-Amadi with HMW in soil samples, guinea grass, and elephant grass, respectively.
Although there were higher levels of HMW PAHs in plant/vegetation samples in some cities in the present study, the fairly appreciable presence of 4-ring PAHs and 3-ring PAHs (Table 3 and Figure 7) is indicative of mixed pyrogenic sources. Te LMW and MMW PAHs are known to exist both in the vapor and particulate phases [77] and usually reside within the locality of the origin or source. Te observation from an additive standpoint that 3-4-rings PAHs predominated in this study suggests localized mixed sources coupled with atmospheric transport [40,70].
PAHs with less than 4 aromatic rings (LMW PAHs) are typifed by grass and industrial oil, wood combustion, and petroleum products (Liu et al. 2017), whereas PAHs with more than 4 aromatic rings (HMW PAHs) signify pyrogenic activities at high temperature including coal combustion and vehicular emissions [78]. Te higher levels of HMW PAHs in  Since HMW PAHs tend to reside in closer proximity to emission sources and LMW PAHs are carried to areas far from the emission sources [40,70], the homolog pattern of PAHs in this study with diferent molecular weights may be characterized by local combustion sources in addition to atmospheric transported depositions [77,79].
Usually, PAHs associated with combustion or hightemperature processes possess a total index that is greater than 4, whereas PAHs originating from petroleum products or low-temperature processes have a total index that is less than 4. In the present study, the total index ranged 0. 27-12.4 in Uyo, 0. 29-8.67 in Choba, 0.00-10.1 in Khana, 0.01-5.53 in Yenagoa, 0.21-9.52 in Eleme, and 0. 13-8.96 in Trans-Amadi. All the sampling locations had total index values greater than 4. It can therefore be inferred from the total index values that PAHs emanated from low-and high-temperature combustion processes. Tese observations seem to be in agreement with previous results from Warri [46]. Table 6 shows the RQ (NCs) and RQ PAHs (NCs) and RQ (MPCs) and RQ PAHs (MPCs) for the 16 priority PAHs in soils from Uyo, Choba, Khana, Yenagoa, Eleme, and Trans-Amadi, Niger Delta, Nigeria.

Ecological Risk Assessment.
RQ PAHs (NCs) values less than 800 are indicative of low ecological risk of PAHs while RQ PAHs (NCs) higher than 800 connote higher ecological risk of PAHs. Although some soil samples from the various sampling locations had RQ (NCs) values greater than 800 in the present study, preponderance of the samples showed RQ (NCs) values less than 800 which is suggestive of a low ecological risk of PAHs in these soils. Some previous studies in Nigeria have reported similar RQ (NCs) values less than 800 [88]. Te RQ PAHs (MPCs) values were greater than 1 except for soil samples from Khana. In this study, Nap, Acy, Ace, Flu, Ant, Flt, and Pyr were the major causes of the ecological risk of PAHs in soils from Uyo, Choba, Yenagoa, Eleme, and Trans-Amadi, Niger Delta, Nigeria. Te ecosystem risk of PAHs in soils from Khana was majorly, whereas due to Flt, Phe contributed less to the ecosystem risk of PAHs in soils from Uyo. Similarly, Ant contributed less to the ecosystem risk of PAHs in soils from Choba, Yenagoa, Eleme, and Trans-Amadi, Niger Delta, Nigeria.

Conclusion
Nap, Acy, Ace, Flu, Ant, Flt, and Pyr were the major causes of the ecological risk due to PAHs in soils from Uyo, Choba, Yenagoa, Eleme, and Trans-Amadi in the Niger Delta, Nigeria. Te ecological risk assessment of PAHs derived from isomeric ratios suggested that the PAHs in soils and vegetation samples from Choba, Yenagoa, Eleme, and Trans-Amadi emanated from pyrogenic processes including trafc emissions, fossil fuels, and biomass combustion as well as petrogenic sources such as occasional spills of liquid petroleum fuels and discharges from automobile workshops. From the risk quotient standpoint, some soil samples from the Niger Delta had RQ (NCs) values greater than 800, thus indicating that soil may require remediation to forestall ecohealth consequences.

Data Availability
Te data used to support the fndings of this study are included within the article.

Additional Points
Highlights. (i) Tere is a widespread PAH pollution in the Niger Delta, Nigeria, (ii) Nap, Acy, Ace, Flu, Ant, Flt, and Pyr pose major ecological risk of PAHs in soils, (iii) PAHs from the Niger Delta emanated from pyrogenic processes and petrogenic sources, and (iv) some soil in the Niger Delta may require remediation.

Conflicts of Interest
Te authors declare that there are no conficts of interest.