3.1. Physicochemical Parameters and Potential Toxic Metal (PTMs) in Water
The physicochemical parameters measured along the sampling point are presented in Table 1
. DO concentrations are between 0.25 and 3.52 mg/L. The part of the reservoir covered with Water hyacinth plants (RW) presents the lower values mainly because aquatic plants act as a barrier between the atmosphere and the water, preventing the dissolution of oxygen into the surface water. However, the difference is not statistically significant (p
> 0.05). It is reasonable to assume this premise but more data is needed to verify this assumption. Temperature is significantly higher in the rivers than in the rest of the reservoir, however, this may be due to the time of the sampling was not the same, being in the morning in rivers (8:00 a.m.) and in the afternoon for the reservoir. The pH is not significantly different among the different zones studied, probably due to the buffer effect that a high concentration of carbonates coming from natural sources, confers on the reservoir [52
]. Moreover, like pH, the ORP is almost constant along the system. Nevertheless, ORP correlates negatively with temperature (p
< 0.05) mainly because oxygen (the oxidizing agent in the reduction oxide reactions) is reduced at higher temperatures and vice versa.
The most significant results regarding the physicochemical parameters are Turbidity and Electric conductivity, as from the inlet (both rivers) to the outlet of the biofltration system (reservoir covered with Water hyacinth); a decrease of both parameters was registered. In fact, the outlet of the system (RF) presents values of both parameters significantly lower than at the inlet of the biofiltration system (both rivers). Moreover, Turbidity and Electric conductivity have a strong positive correlation (0.953) with p
< 0.05 (Table S1
), revealing that the biofiltration system is efficient in the removal of suspended and dissolved solids.
With respect to the PTMs results, in order to determine the degree of water contamination in the study area, all concentration values were compared with the local regulation reference values for discharges of wastewater into the surface waters (NOM-001-SEMARNAT-1996
, Ley Federal de Derechos Disposiciones Aplicables en Materia de Aguas Nacionales 2015 (LFDMA)
and Finally Declaratoria de clasificación de los ríos Atoyac y Xochiac y sus afluentes (DCRAX)
). Additionally, as with local regulation, the water results were also compared to the Screening Quick Reference Tables (SQuiRTs) from the National Oceanic and Atmospheric administration of the United States Department of Commerce (NOAA). All PTMs levels were shown to be lower than the permissible limits set by local regulations, except for Hg and Ba (Table 2
In Alseseca River, the mean concentration of Hg exceeded the DCRAX limit, probably due to the constant spill of textile and automotive industrial wastes along Alseseca River. On the other hand, mean concentration of Ba exceeded the limit set by LFDMA in all zones studied, possibly related to the natural enrichment in the geology basin [10
]. In regards to the SQuiRTs water values, metal content in the four zones studied were barely above the limits. Moreover, levels of Hg in the rivers are below limits and in the reservoir are close to the limit. Cadmium levels in the two zones of the reservoir (RW and RF) are below the limit, which may pose a threat to the aquatic biota in the reservoir due to the high toxicity of this element.
With respect to the difference in metal concentrations between the parts of the reservoir covered with E. crassipes
(RW) and devoid of E. crassipes
(RF), it was observed that mean values of Zn and Ti are significantly greater in the RW than in RF (p
< 0.05). This is likely because on the shore of the Valsequillo reservoir, particularly close to the sampling point VAL03, there is a human settlement called San Baltazar Tetela
, which discharges their residual waters into the reservoir. This wastewater can contain metals coming from a wide variety of domestic household products, such as toothpaste, cosmetics, batteries, and cleaning materials that contain trace concentrations of these metals [39
] and thus enriching the content of these metals in that specific zone. In addition, Water hyacinth plants that cover the Valsequillo reservoir absorb metals from water during the growing period, but as proved by Jackson [53
], during senescence, the plant is susceptible to release metals along with the Water hyacinth plants tissues into the surrounding water.
Mean concentration values of Ni and V are significantly greater (p
< 0.05) in rivers (Atoyac and Alseseca) than in the zone of reservoir free of Water hyacinth plants (RF). Thus, one may suppose that within the zone covered by Water hyacinths plants, there is a process of metal removal that is performed mainly by these plants. Moreover, the presence of Water hyacinth plants in this zone might promote the sedimentation process driven mainly by the change of the hydraulic regimen. In addition, the plant’s rhizosphere stimulates the growth of the aerobic biofilm which may play an important role in adsorbing PTMs from water [54
]. Furthermore, the plants can secrete exudates that contain carbohydrates, amino acids, polysaccharides and flavonoids [55
], which in turn can act as exogenous chelating agents and thus precipitate PTMs. Consequently, this zone can also be termed as a biofiltration system
The biofiltration system in Valsequillo reservoir proved to be effective in removing PTMs from water as the total PTMs removal efficiency (from the inlet to the outlet) of Co, Zn, As, Ni, Cu, Pb, Ti, Cr, Mo and V was (all values in %) 18, 71, 19, 42, 51, 65, 51, 5, 54 and 65, respectively. (Table 3
). However, for almost all PTMs, the removal efficiency in the first stages of the biofiltration system (i.e., VAL01, VAL02 and VAL03) was low (for some PTMs were zero %). The above may indicate that when dying, the Water hyacinth plants could be adding these elements to the system.
Therefore, one may hypothesize that within the biofiltration system, exists a dynamic equilibrium in which bioaccumulation and release of PTMs by Water hyacinth plants is present at the same time. To test the above hypothesis, PTM content in Water hyacinth plants and sediments were measured and the results are presented below.
3.2. Potential Toxic Metal in Water Hyacinth Plants
Mean concentration values are reported in Table 4
. Levels of Hg in Water hyacinth plants were below the detection limits. Meanwhile, Cd content was 0.4 mg/kg d.w. just in the submerged part. These results agree with the values reported by Odjegba and Fasidi [18
] and Romanova et al. [4
] who also observed that among several metals studied, Hg and Cd were the less absorbed by the Water hyacinth plants (Table S2
). The results also showed that with exception of Ba, most of the PTMs absorbed by Water hyacinth plants were located in the submerged part of the plant (Roots and rhizome.
For Co, Mo and V, the ANOVA analysis showed that the concentration in the submerged part was significantly different with respect to the aerial part of the plant; being as follow: Co (p = 0.034), Mo (p = 0.003) and V (p = 0.029). The Ba showed a different behavior, as the concentration in the aerial part was significantly higher (p = 0.03) than in the submerged part of the plant. This may be due mainly to the great mobility of this element within the Water hyacinth plants. It was also found that the concentrations of Zn, As, Ni, Cu, Pb, Ti and Cr in the submerged part of the plant were higher than in the aerial part. However, the differences were not significant (p > 0.005).
For some PTM, there is a positive correlation in which a decrease was observed from the entrance to the exit of the biofiltration system, revealing a pattern that corresponds to a maximum absorption of metals by the Water hyacinth plants in the sites closest to the mouths of the rivers Atoyac and Alseseca (Table 5
This may imply that Water hyacinth plants have undergone an adaptation process to be able to survive to high PTMs levels. These results are in accordance with Romanova et al. [4
] who observed a decrease in the absorption of metals (particularly Pb and Cd) from water of a gold mine tailing that was passing through Water hyacinths in the River Ur, Siberia. Moreover, Odjegba and Fasidi [18
] reported that concentration of Cd, Cr, Cu, Hg, Ni, Pb and Zn in the Water hyacinth plants increased with an increase in the metal concentration in the external medium, thus witnessing a link between metal content in the ambient water and the content in the Water hyacinth plants. This may imply that, as stated by Baker [41
], Water hyacinth plants act as an indicator more than as a hyperaccumulator in the Valsequillo reservoir.
With exception of some works, the majority of the authors have reported greater concentration of metals in the submerged part of the Water hyacinth plants than in the aerial part (Table S2
). Moreover, the roots act as a first barrier for the metal uptake, and thus they become the main filter for the absorption and retention of the metals, consequently the highest metal concentrations in the plant must be inside the root. Furthermore, according to Tejeda et al. [57
] the content of PTM in Water hyacinth plants decreases in the following order: Roots (>50%), leaves, rhizome (∼10%), petiole, stem and stolon (<10%). This pattern suggest that Water hyacinth plants may adopt a compartmentalization strategy, common in wetland species, which consists in storing the highest levels of PTMs in the submerged part of the Water hyacinth plants (e.g., roots and rhizomes). This is with the aim of protecting the plants against the harmful effects of high levels in leaves, where the photosynthetic processes take place [58
Aquatic plants capable of accumulating up to 5000 mg of metals per kilogram of dry plant biomass or those with BCF > 1000 are considered as hyper-accumulators of PTMs [28
]. In the present work, the total amount of metals accumulated by Water hyacinth plants was below 5000 mg/kg d.w. However, with exception of Cd and Hg, the BFs of all metals were above 1000. Despite being higher than those reported in literature (Table S2
), BF values were in accordance with the range (101
) proposed by Jackson [53
]. In addition, the great variety of metals in water of the Valsequillo reservoir stimulates their absorption by the plant, which confirms that bioaccumulation is more effective when there is a combination of metals compared to only one [24
]. Therefore, with exception of Cd and Hg, we considered the Water hyacinth plants present in Valsequillo reservoir as an indicator but it can also be considered as hyper-accumulator of all metals studied.
From all metals studied, Zn presented the highest translocation from the submerged part to the aerial part of the plant. These results were in accordance with reported by Aurangzed et al. [60
] who registered high TF in young Water hyacinth plants used as removal agent for a steel foundry effluents (Table S2
). This is probably due to the need that the plant has for this metal; although Zn is potentially toxic, it is also an essential element for the plant [5
] which participates in: formation of chlorophyll, conversion of starches to sugars and formation of the auxins (hormones that favor the growth of stems) [2
]. Among all PTMs measured, Co presented the lowest mobility followed by V and Ti. Nevertheless, in spite of the low translocation of Ti, it was greatly accumulated in the submerged part of the plant. These results are similar to the ones obtained by Tejeda et al. [57
], who reported that among Cr, Cu, Ti, Pb, Zn, and Ni, Water hyacinth plants in Lerma River, Mexico absorbed more Ti (325 mg/kg d.w.) (Table S2
From the perspective of the TF, with exception of Ba, all PTMs studied are between 0 and 1 thereby indicating Water hyacinth plants as a tolerant plant for these metals [40
]. In the case of Ba, only 24% of the total content remained in the submerged part of the plant whilst 76% passed to the aeriated part of the plant. The high concentrations of Ba could be attributed to the natural contribution coming from barite (BaSO4
) assemblages of Popocatépetl volcano (active) situated on the western side of the study area, generally hosted in K-feldspars, where Ba substitutes K in many K-bearing minerals [61
]. On the other hand, the anthropogenic contribution of Ba may be related to the automotive industry (widely settled in the basin) [31
]. This is in accordance with the high levels of Ba in the ambient waters, as Ba was the most abundant mineral there (See Section 3.1
). Thus, it is reasonable that the Water hyacinth plants in Valsequillo reservoir are well adapted to this element and, therefore, its ability to accumulate and translocate this particular PTM is well developed.
In terms of the simplified biofiltration system, with exception of Co, As and Ti, in all PTMs, an increase of TF from the sampling point VAL01 to VAL03 was observed, whilst a decrease of BF at the same time was registered (Figure 3
In the present work, a plant damage index was not evaluated, and that’s why the explanation of such phenomenon is presented in terms of BF and TFs results. Water hyacinth plants present exhaustion in metal capture from the inlet to outlet of the reservoir. This may be related to the Water hyacinths at sampling point VAL03 that reached a threshold metal concentration value; therefore, it became toxic and, thus, inhibitory for the growth of the plant. From these results, it can be inferred that in order to avoid toxicity, the Water hyacinth plants adopts two mechanisms: (1) The plant releases metals from the root into the aquatic environment [62
] and consequently BF decreases and; (2) The plant enhances the mobility of metals from the submerged part to the aerial part with the aim of facilitating metal loss during periodical leaf regeneration [59
]. These results are similar to those reported by Odjegba and Fasidi [18
], who observed a decrease of metal absorption by Water hyacinth plants along with an increase of concentration in the ambient water.
Another reason why the bioaccumulation factors (BF) decreased from VAL01 to VAL03 could be related to the low concentrations of oxygen at the VAL03 site (0.31 mg/L). According to Kumari and Tripathi [63
] and with Zimmels et al. [64
], the aeration in wetlands containing Water hyacinth plants generate better conditions for the plant to absorb contaminants. In other words, the lower the oxygenation, the less efficient the absorption of contaminants and vice versa. As mentioned above, the coverage of the Water hyacinth plants could be preventing the exchange of oxygen between the atmosphere and the surface of the water and therefore, that is the reason why the oxygen in this area (very infested with this plant) is lower and, consequently, why the BF decreases. With respect to Pb at the sampling point VAL02, it was not possible to calculate the BF because the concentration of Pb in water were found to be below the detection limit (BDL). The same happened with the As in the sampling site VAL03.
3.3. Potential Toxic Metal in Sediments
Metal concentrations in surface sediments along the study area increased from the Reservoir’s inlet (rivers) to the reservoir’s outlet. PTM levels of Co, Ni, Cu, Ti and Mo in the zone free or E. crassipes
(RF) were greater (p
< 0.05) than in the water of rivers (Table 2
). This tendency is opposite to that of water, where metals content in rivers are higher (p
< 0.05) than in RF, this is particularly true for Hg, V and Ni. These results suggest that an intense process of sedimentation of metals takes place in the reservoir driven by Water hyacinth. However, this process can also occur in different forms such as metals attached to the suspended particles, carbonate bound, occluded in iron and/or manganese oxy-hydroxides, bound to organic matter, sulfide bound or by metal chelation [53
Another important route of metal sedimentation is through the absorption of metals by plants and their subsequent death. This can be corroborated since, there is no significant difference (p
> 0.05) in the content of metals in sediments and in the Water hyacinth plants for Co, Zn, Ni, Cu, Pb, Cr, Ba, Mo and V. Moreover, mean metal content in Water hyacinth plants is significantly higher than in sediments for As (p
< 0.05) (Figure 4
). This could imply, as reported by some authors [54
] that as with Hg and Selenium (Se) [65
], Arsenic (As) in the Water hyacinth plants is undergoing a process of phytovolatilization before it dies.
These results suggest that a major proportion of the surface sediments are composed of dead Water hyacinth. This is in concordance with some studies [53
] that observed a strong positive correlation between content of metals in Water hyacinth plants and sediments. In particular, roots are the organs that normally correlate most with levels of PTMs in the sediment [59
As discussed previously, the sediments can be a source of contamination to the water column, predominantly Cd, Cr, Cu, Pb and Zn, particularly when they are attached to organic sediments [58
]. Furthermore, Wu et al. [67
] reported that finer sediments, as formed by organic matter, tend to have higher metal concentrations and readily wash off into water bodies. This is of particular concern as the Geoaccumulation index (Igeo
) revealed that Zn, Cu, Ti, and V are moderately contaminated in sediments and from the perspective of Pb, sediments are moderately contaminated to contaminated, particularly in the zone of the reservoir free of E. crassipes
. Furthermore, with respect to Hg, in RF, sediments fall under the category of contaminated to strongly contaminated (Figure 5
Similar results were presented for Enrichment Factor (EF), since in both the zone of the reservoir with E. crassipes
(RW) and the one free of E. crassipes
(RF), Cu and Pb present moderately to severe enrichment. In the case of Hg, only in the zone RW an enrichment was observed. Moreover, except for V and Hg, an increase of EF from the inlet (rivers) to the courting of the reservoir (RF) was observed. According to these results, with exception of Hg, the ecological risk in sediments increased in the following order: RF > RW > Alseseca River ~ Atoyac River (Figure 5
The results of EF and Igeo
for Hg are in accordance with the Potential Ecological Risk Index (PERI), as the PERI of RW, RF, Atoyac River and Alseseca River were (all values are dimensionless) 330, 148, 130 and 109, respectively. According to the categories of Hakanson [12
], there is a low risk in the sediments of the rivers and in RF. Nevertheless, in RW there is a considerable risk, mainly due to the elevated values of Hg in that particular zone (Figure 5
c,d). These results pointed out the importance of managing the sediments in the reservoir, as they pose a threat to the water quality due to the constant interchange of matter.