T. angustifolia Hg content
The increase in [Hg]T between fresh green leaf tissue collected in June and senesced leaf tissue collected in November, as well as the higher translocation factor for senesced leaf tissue, supports the post-hoc hypothesis that there may be translocation of Hg into the leaf tissue over the course of the growing season. However, if translocation occurred then it is reasonable to expect leaf [Hg]T to correlate with the soil [Hg]T. Since fresh green leaf and senesced leaf do not correlate significantly with Hg content in soil, other factors should be considered to explain the increase in [Hg]T over time. Ambient atmosphere concentrations could influence leaf Hg content more than accumulation from the soil. Total Hg content in leaves was more dependent upon air concentrations than soil Hg content in controlled mesocosm experiments with T. latifolia (Fay and Gustin 2007).
Meng et al. (2012) made similar observations in the aboveground tissues of rice (Oryza sativa L.). Therefore, concentrations of Hg in T. angustifolia in this study site may be influenced by a combination of translocation, wet deposition, and ambient concentrations of Hg in air.
The highest [Hg]T among living organ tissues was found in the adventitious roots (p < 0.001, Fig. 3). Elevated Hg content in roots is consistent with other studies that examined Hg bioaccumulation in Typha species (Afrous et al. 2011; Bonanno and Cirelli 2017; Lominchar et al. 2015; Willis et al. 2010) and metal uptake by other plant species (Beauford et al. 1977; Carranza-Alvarez et al. 2008; Patra and Sharma 2000; Taylor et al. 1983; Weis and Weis 2004). Accumulation of Hg in roots may be related to a mechanism for Typha to keep toxicity isolated in roots and away from critical photosynthesis in leaves. Beauvais-Fluck et al. (2018) observed that inorganic mercury (Hginorg) decreased chlorophyll content, whereas MeHg increased antioxidant production in Elodea nuttallii exposed to Hginorg or MeHg in mesocosm experiments. Krupp et al. (2009) identified phytochelatins in rice (Oryza sativa) and common horehound (Marrubium vulgare) that preferentially bound Hginorg (rather than MeHg) within the roots, and this prevented movement of Hg into adjacent tissues, which suggests phytochelatins immobilize Hg in the roots and prevent transport to the leaf. Mercury may behave similarly to other metals, such as lead, upon uptake in plants. Using an electron microscope, Panich-pat et al. (2005) observed the accumulation of lead (Pb) granules near vacuoles in the parenchyma tissue of a T. angustifolia root exposed to Pb-spiked soil. Due to potential growth and photosynthesis impairments, it is reasonable to expect that T. angustifolia in USLR wetlands would preferentially keep bioaccumulated mercury within the roots, away from photosynthetic tissue. Additionally, metal oxides (likely Fe and Mn) were observed on the outer surface of the roots while cleaning. Although the soil and other surficial debris was removed, the oxides were not. Therefore, the [Hg]T may be in part, or in full, due to the oxides on the surface tissue rather than direct uptake. The oxides could have been removed by washing with a reducing agent and a metal complexing ligand solution. For the purposes of estimating the overall Hg budget of the wetland, the roots were cleaned only with deionized water and gentle brushing to remove mineral and organic detritus that were included in the Hg analysis of hydric soils.
The potential use for T. angustifolia as a biomonitor in this environment is low. Root tissue [Hg]T was the only biomass material that correlated significantly with soil [Hg]T (p = 0.045) (Table 1). However, root tissue does not make an ideal biomonitor from a methodological standpoint. Based on the extensive cleaning and processing required for analyzing root tissue [Hg]T in the methodology used here, it may not be the most efficient means to determine if a wetland is Hg contaminated. From an efficiency standpoint, sampling and analyzing the soil itself would be easier than the root tissue.
The role of cattails in Hg stabilization in wetlands
Many species of wetland plants are useful for the remediation of contaminated sites due to their ability to bioaccumulate contaminants (Ashraf et al. 2019; Song et al. 2018, Weis and Weis 2004). Toxic trace metal contamination, including Hg, has the potential to be treated using phytoremediation due to the ability for trace metals to bioaccumulate in plant tissue (Muthusaravanan et al. 2018, Weis and Weis 2004). Many studies discussed here that have examined Hg in Typha were designed to assess the ability for Typha to facilitate phytoremediation. Therefore, our results are discussed in context of phytoremediation-focused Typha studies for the purposes of comparing Hg burden and mechanisms for bioaccumulation.
Although a BCF > 1.0 is commonly accepted as an indication of bioaccumulation, there is not convincing evidence for the widespread application of T. angustifolia in Hg phytoremediation efforts for three main reasons: failure to meet current accepted criteria for hyperaccumulation, overall minimal contribution of roots to the overall wetland total Hg burden, and USLR wetlands exemplify conditions under which Typha performs poorly as a means of phytoremediation relative to other studies.
T. angustifolia did not classify as a hyperaccumulator given the criteria for other metals (Baker and Brooks 1989). Concentrations in plant tissue must be ≥ 1000 µg/g (Co, Cu, Cr, Pb, Ni) or 10,000 µg/g (1%) (Mn, Zn), to be considered a hyperaccumulator. Although Hg is not included in the metals listed in their criteria, the difference in scale of accumulation (ng/g vs. µg/g) is enough to conclude that T. angustifolia from this wetland did not hyperaccumulate Hg. However, higher [Hg]T in the root tissue relative to above-ground organ tissue is characteristic of species used for phytostabilization (Mahar et al. 2016), suggesting the potential for Hg stabilization within USLR riparian wetlands.
The entire root biomass of Typha within the studied wetland made up only 0.12% of the overall Hg burden within the wetland (Table 2). Although the roots had the highest [Hg]T, and a BCF of 1.2, they made up only 0.43% of the total biomass weight. Higher root [Hg]T may fit with the description of a species capable of phytostabilization (Mahar et al. 2016), but in context of the rest of the wetland Hg burden, the living intact roots do not stabilize a significant amount of Hg, at a given time during the growing season.
Studies elsewhere have observed greater phytoremediation potential in Typha, which may be due to environmental differences, such as pollution sources, soil chemistry, and the evolutionary history of the Typha populations in the USLR. Bonanno and Cirrelli (2017) observed a BCF of 5.35 ± 0.28 in T. angustifolia sampled in the spring, and 6.40 ± 0.13 in the fall. Lominchar et al. (2015) observed BCFs in T. domingensis ranging from 121–3168. The difference in BCF here may be due to the Hg in USLR wetlands being deposited from the atmosphere, which created a lower base [Hg]T in the hydric soils of this wetland as compared to studies with point-source contamination from mining or wastewater (Bonanno and Cirrelli 2017; Lominchar et al. 2015). However, findings from Lominchar et al. (2015) indicate that the BCF and amount of Hg bioaccumulated relative to the total Hg in the soil is largely determined by the fraction of total Hg that is soluble. BCF values were highest when Lominchar et al. (2015) compared the relative accumulation to soluble Hg in the soil. Therefore, if much of the Hg in USLR wetland hydric soil is bound to organic particulate, thus not available in a soluble form, a lower BCF would be expected. The high Hg concentrations in the detritus at Coles Creek, relative to soil and root concentrations, support the possibility for most Hg in Coles Creek to be unavailable for bioaccumulation by living Typha as well. The low BCF values may also be attributed to the evolutionary history of the Typha in the USLR. Ye et al. (1997) observed that T. latifolia originating from point source contaminated sites were more efficient at bioaccumulation of metals (Zn, Pb, Cd) than those originating from uncontaminated sites. Although atmospheric deposition of mercury has occurred over the last several decades in the New York region (Risch et al. 2017; Driscoll et al. 2007) most Typha in this region has not experienced point source mercury pollution in the USLR. Therefore, it may be that evolutionary history has not selected for adaptation to mercury pollution in the form of bioaccumulation in USLR T. angustifolia. Moreover, results here indicate T. angustifolia should not be used for phytoremediation or phytostabilization, particularly in regions lacking significant point-source pollution.
The hypotheses and methods of this study provide results that reveal the limited application and potentially adverse outcomes of phytoaccumulation. Bonanno and Cirrelli (2017) suggest that T. angustifolia is effective for phytoremediation due to high uptake ability and high biomass production. Here, the high [Hg]T of detritus in conjunction with other recent work on organic matter increasing Hg exposure risk (Mahar et al. 2016), suggests that high biomass production may instead increase Hg cycling and ecosystem exposure. By focusing on only the living biomass tissue, researchers may be missing a key factor in determining the phytoremediation capabilities of plant species. Although those with higher biomass have the potential to uptake more of the desired contaminant, the dead organic matter resulting from high growth may have unintended consequences, particularly in cases where the contaminant has a complex cycle in the environment, such as Hg. Applications of phytoremediation should be limited to highly controlled and managed situations, such as treatment of wastewater with a hyperaccumulator species that is frequently maintained and disposed of safely. Additionally, in context of the relative contributions of biomass to overall wetland Hg burden (Table 2), criteria determining a specie’s ability to hyperaccumulate or phytostabilize, should be determined on a percent removal basis, considering all major wetland components (soil and different biomass types) on a mass or volume per unit area basis to avoid false positives. For example, here, roots had a BCF > 1.0, but only contributed 0.12% to the overall wetland Hg burden.
Fate of Hg in riparian wetlands
Whereas 83% of total Hg in the Coles Creek wetland resides in the soil, organic detritus makes the next largest contribution (13%), confirming the hypothesis that biomass constitutes a significant fraction (> 5%) of total Hg burden in the wetland. The scale of Hg burden in hydric soil is in part due to the soil volume estimate used in this model, which is dependent on the depth of the soil core. We assume here that the soil most likely to erode is that which was easily cored (Brahmstedt et al. 2019). Based on field observations, the average soil core depth was 20 cm. While the actual volume eroded may vary depending on location in the wetland and erosive conditions, for the purposes of creating a simple model to determine Hg burden within a wetland, 20 cm is functional. In contrast, the contribution made by detritus is not due to its large volume or mass, but rather its high [Hg]T, 110 ± 53 ng/g d.w. (Fig. 3), which is significantly greater than the [Hg]T of the soil (p < 0.001). He et al. (2019) suggest soil organic matter increases risk of Hg exposure, which counters previous work suggesting organic matter acts as more of a Hg sink and lowers bioavailability. Increased Hg methylation may occur in the presence of organic matter due to namely, the characteristics of the organic matter and its ability to stimulate the activity of Hg methylating microbes (He et al. 2019). Considering the overall life cycle of T. angustifolia, as well as the Hg burden in each wetland component present in the Coles Creek wetland, it is evident that T. angustifolia is not good for phytoremediation or phytostabilization. The large amount of detritus biomass resulting from T. angustifolia, may instead increase the risk of Hg exposure to biota within these wetlands by retaining Hg, creating anoxia in hydric soils upon biomass decay, and stimulating Hg-methylation.
From 1958, the year the hydroelectric power dam began production, until 2017, the year a new water level management plan began operating, water levels in the USLR were unnaturally stable and ranged from 73.92–75.68 m elevation above mean sea level, compared to the natural range of 73.88–76.18 m elevation (International Joint Commission 2016). The lack of disturbance to the shoreline allowed for Typha spp. to dominate riparian wetlands and decrease overall wetland vegetation biodiversity (Farrell et al. 2010; Wilcox et al. 2008). The new water level management plan that began in 2017, known as Plan 2014, allows water level fluctuations to simulate natural fluctuations more closely with water levels ranging from 73.72–75.74 m elevation (International Joint Commission 2016). The goal of Plan 2014 is to restore biodiversity within the USLR by increasing disturbance to Typha spp., that will promote an increase in vegetation diversity, and a concomitant increase in the biodiversity of other species, including fish (International Joint Commission 2016).
The water level management plan (Plan 2014) should consider the effects that fluctuating water levels may pose to detritus-bound Hg in this region. The wetland we studied is small (13.2 ha), but it is representative of a protected embayment wetland, of which there are over 6,300 ha in the Upper St. Lawrence River and Lake Ontario, representing 23% of all riparian wetland types present (Wilcox et al., 2005). Although living T. angustifolia biomass did not accumulate Hg extensively, the detritus that originated as T. angustifolia, traps a significant amount of total Hg. Fluctuating water levels are predicted to restore wetland meadows at the terrestrial margin of the wetland and restore submerged aquatic vegetation at the near-channel edge. At the near-channel edge, Typha has recently (July 2019) been observed being uplifted and eroded away in mats by high water levels combined with wave energy during extreme high-water events. Impacts to the terrestrial margin Typha have not yet been observed, although, it is predicted that repeated flooding and drying of Typha at the terrestrial margin will cause marsh dieback, allowing the wetland meadow to reestablish. Once the Typha dies, it will generate detritus, thus creating a region at the terrestrial wetland margin where there is not only periodic wetting and drying of wetland - likely stimulating Hg methylating microbes - but also a thick surface layer of detritus further promoting microbial growth and retention and transformation of Hg.