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Activities of several vital antioxidant enzymes were determined after exposure to CECs

The continued observation of the formation of N4-acetylsulfamethoxazole, an acetyl conjugate, in the environment is of considerable interest because conjugates have the potential to maintain the biological activity of the parent compound . Further, because researchers traditionally only quantify parent compounds during environmental assessments, the formation and accumulation of conjugates implies that there may be an underestimation of environmental exposure to CECs such as pharmaceuticals and further incomplete environmental risk assessment of CECs . This is of particular concern for antibiotics, because of the rise of antimicrobial resistance . The major metabolite of methyl paraben, p-hydroxybenzoic acid, was observed in all soil samples, including the non-treated controls . This was likely due to the endogenous p-hydroxybenzoic acid in sphagnum peat . However, the concentration of p-hydroxybenzoic acid was higher in the spiked earthworm treatments than in the blank controls or non-earthworms chemical controls indicating that E. fetida was also capable of taking up and metabolizing methyl paraben and excreting of p-hydroxybenzoic acid into the soil. This was consistent with previous contact tests in which 70% of the initial methyl paraben was found to be metabolized to p-hydroxybenzoic acid and phenol within 48 h in E. fetida . The transformation products o-desmethylnaproxen and nordiazepam were not detected in earthworm tissues, but o-desmethylnaproxen was quantifiable in earthworm-CEC treated soils during the 21 d incubation , indicating active uptake, metabolism, and excretion. The quantification of the major metabolites for naproxen, sulfamethoxazole and methyl paraben, o-desmethylnaproxen, N4- acetylsulfamethoxazole, and p-hydroxybenzoic acid suggested a trend in the capabilities of E. fetida to take up, metabolize and excrete then transformation products of some CECs in the soil environment. Previous studies used radiolabeling and LC-FTMS analysis to assess potential metabolism of carbamazepine,blueberry plant pot diclofenac and fluoxetine in E. fetida but were unable to verify the presence of metabolites in earthworm tissues . Results from this and other studies indicated that metabolism may be chemical-specific.

To the best of knowledge, this was the first study to identify and quantify metabolites of these CECs in E. fetida dwelling in a soil. A significant increase in the activity of glutathione-S-transferase in the treatment samples over the controls was observed starting after 3 d into the incubation , and the GST activity continued to increase until the end of the 21 d incubation . This observation suggested that increased exposure time resulted in increased oxidative stress because glutathione is considered a critical antioxidant that acts to maintain redox homeostasis and signaling in cells . Further, GST is a crucial enzyme family for the detoxification of xenobiotics during Phase II metabolism . Thus, the observed increase in GST activity may indicate that there was a formation of additional Phase II metabolites. However, the detection of these potential metabolites was not attempted due to a lack of authentic standards. High GST activity was also observed at 0 h for both the controls and treated samples. However, this increase in activity is likely due to the initial stress of the earthworm being transferred into the test media, and the effect dissipated within the first day of exposure. No significant difference in catalase activity was observed between the treatment and controls until the end of the exposure period . At the 21 d time point a significant increase was seen in the treatment samples , indicating that extended exposure to CECs likely resulted in increased production of hydrogen peroxide in earthworm tissue . However, an increase in the CAT activity was also found in the control at 0 h. The increase in CAT activity was, again, likely due to the initial stress of the earthworms being transferred to different environmental conditions and the difference dissipated within 24 h. A significant increase in superoxide dismutase was observed at 1 d and 3 d . However, no significant differences were observed between the treatment and controls after 3 d . This trend was in accordance with SOD has the first line of defense against reactive oxygen species . SOD acts to catalyze the superoxide radical into oxygen molecules or hydrogen peroxide . As an increase in CAT was observed at the later time point it was likely that SOD activity increased initially, resulting in an increased production of hydrogen peroxide, which was then detoxified by CAT. Previous studies examining the biochemical effects of CEC exposure in earthworms showed somewhat similar trends.

For example, a study exploring the biochemical and genetic toxicity of triclosan in E. fetida showed a dose-dependent hormesis effect over time for both CAT and GST activity, with increasing activity being observed after a 2 d exposure at low doses and an inhibition of enzyme activity being observed after 14 d at high doses. Further, similar studies considering oxidative stress in E. fetida exposed to herbicides showed an increase in enzyme activities at lower concentrations and a suppression of enzyme activities at high concentrations . Thus, it is likely that the lower, environmentally relevant, concentrations of CECs used in this study resulted in the observed increase in enzyme activities while these concentrations were not high enough to cause an inhibition in enzyme activity. Currently we are experiencing a series of global trends that are creating unique challenges for the future of sustainable development. These trends include shifting precipitations patterns, rising temperatures, growing human populations, and rapid urbanization. In order to meet these challenges, traditionally under-utilized resources, such as treated wastewater and bio-solids, will have to be harnessed. These resources are derived from wastewater treatment plants and contain biologically active, pseudo-persistent, trace chemicals referred to as contaminants of emerging concern . Land application of TWW and bio-solids for agriculture and landscaping has the potential to introduce CECs into terrestrial ecosystems, from where they could accumulate, be metabolized and/or cause adverse effects in terrestrial organisms. This dissertation has described the ability of terrestrial plants and invertebrates to take up and metabolize CECs and highlighted the potential for these trace contaminants to induce biochemical changes in non-target terrestrial organisms. The findings of this project, overall conclusions, and recommendations for future work are summarized below. In arid and semi-arid areas, TWW reuse is becoming increasingly prevalent for agricultural irrigation. However, irrigation with TWW has the potential to introduce CECs including antibiotics into agroecosystems. One of the most commonly prescribed and environmentally relevant antibiotics is sulfamethoxazole. However, little is known about the fate of sulfamethoxazole in terrestrial plants. In this study, sulfamethoxazole was observed to be taken up and actively metabolized by Arabidopsis thaliana cells into six transformation products. The transformation products included oxidation of the amine group, producing Phase I metabolites, which was followed by conjugations with glutathione, glucuronic acid and leucine, producing Phase II metabolites.

Phase III metabolism was assessed by determining the mass balance of 14C-sulfamethoxazole in A. thaliana cells and cucumber seedlings. Non-extractable 14C-sulfamethoxazole increased over time in both A. thaliana cells and cucumber seedlings, indicating that Phase III metabolism significantly contributed to the fate of sulfamethoxazole in A. thaliana cells and cucumbers. Further, in A. thaliana cells and cucumber seedlings, the mass balances were calculated to range from 80-120% and 80-94%, suggesting a minor role of mineralization. The results from this study highlighted the potential of terrestrial plants to transform pharmaceuticals, forming both bioactive Phase I metabolites and Phase II conjugates, and store them as in the form of bound residues as Phase III metabolism. Plant uptake of CECs from TWW reuse and bio-solid application has been documented in agroecosystems. Previous studies suggested that plants were capable of metabolizing CECs after uptake. However, these studies often reported different results even with the same CECs,plastic gardening pots likely due to the use of different plant species and/or different laboratory conditions. In this study, the metabolism of the benzodiazepine diazepam was explored in three different plant species, A. thaliana, cucumber , and radish . The plants were exposed to diazepam in laboratory under three different laboratory exposure conditions that included a 6 d cell culture, an acute /high concentration hydroponic cultivation, and a chronic /low concentration hydroponic cultivation. 14C-Diazepam was incubated concurrently with non-labeled diazepam to determine the fractions of extractable and non-extractable radioactivity to quantify Phase III metabolism. Diazepam was taken up and metabolized in all plant species under the different exposure conditions. A. thaliana cells actively transformed diazepam into temazepam and nordiazepam via Phase I metabolism. This metabolism mimicked human metabolism, as temazepam and nordiazepam are the minor and major metabolites, respectively, formed during human metabolism of diazepam. Intriguingly, both of these metabolites are bioactive and prescribed pharmaceuticals in their own right, alluding to a potential for increased risk from consumption not considered in previous studies. The fraction of non-extractable residue increased over the 6 d incubation, indicating extensive Phase III metabolism over time in A. thaliana cells. In cucumber and radish seedlings, a similar Phase I metabolism pattern was observed, with nordiazepam being the most prevalent metabolite at the end of the 7 d and 28 d cultivations. However, significant differences in phase III metabolism were observed between the radish and cucumber plants. For example, after the acute exposure, diazepam mass balance was 99.3% for cucumber seedlings but only 58.1% for radish seedlings, indicating increased mineralization in the radish system. Diazepam induced changes in the regulation of glycosyltransferase activity in both cucumber and radish seedlings, indicating the formation of Phase II metabolites. The results from this study showed that exposure conditions and plant species can influence the metabolism of diazepam, and formation of bio-active transformation intermediates and different phases of metabolism should be considered in order to achieve a comprehensive understanding of risks of CECs in agroecosystems.

Exposure of terrestrial invertebrates to CECs will likely increase with increasing TWW reuse and bio-solid application. However, currently there is limited information on the fate and effects of CECs in terrestrial organisms. In this study, the earthworm E. fetida was exposed to three pharmaceuticals, i.e., sulfamethoxazole, diazepam, and naproxen, and one preservative, i.e., methyl paraben, for 21 d in an artificial soil. Methyl paraben did not accumulate in the earthworm tissue, likely due to its rapid degradation in the soil. The other CECs showed an accumulation in earthworm tissues from the soil/soil porewater. The presence of E. fetida did not significantly affect the adsorption of these CECs to the soil. The presence of primary metabolites in the treated soil suggested that E. fetida were capable of actively metabolizing the three pharmaceuticals and excreting the metabolites. However, the metabolism was chemical-specific, and only N4- acetylsulfamethoxazole was detected in earthworm tissues. Exposure to the four CECs also resulted in the up-regulation of several antioxidant enzymes, including glutathione-S-transferase, superoxide dismutase, and catalase, and an increase in malondialdehyde, indicating oxidative stress in the exposed E. fetida. Results from this study highlighted the need to consider the role of, and effects on terrestrial invertebrates when understanding risks of CECs in agroecosystems. Our findings illuminate the complexity of the interactions between contaminants of emerging concern and terrestrial organisms. The dissertation highlights the ability of terrestrial organisms to take up and transform CECs through metabolism, which results in both bio-activation and detoxification of the target contaminants. This project also demonstrates the ability of CECs to alter the biochemistry of the studied terrestrial organisms by changing the regulation of enzymes associated with oxidative stress and metabolism. The use of cell cultivations, hydroponic studies, and artificial soil allowed us to examine the metabolism and effects of CECs in terrestrial organisms with limited confounding factors. However, it is highly likely that similar studies conducted in soils may show low rates of uptake and different patterns in metabolism. Our research suggests that scientifically sound understanding of fate of, and risks from, CECs in the environment cannot solely rely on the assessment of the parent compound and/or only consider the potential for human exposure to CECs. One must also consider the potential for the formation of metabolites and the consequences of exposure to all non-target organisms in order to better understand the fate and risks of CECs in terrestrial environments. The results have potential implications for policy makers and other stakeholders attempting to assess the risks for the land application of treated wastewater and bio-solids.

All ag-MAR field sites were chosen based on SAGBI suitability prior to flooding

Glyphosate-resistant horseweed, or mare’s tail , was reported in 2005 and is one of the dominant weeds in and around raisin and tree fruit production areas of the San Joaquin Valley, as well as on roadsides and canal banks in the region . The level of glyphosate resistance in horse weed is relatively low, and resistant plants are usually injured to some degree following glyphosate applications, which suggests that resistance is not due to an altered target enzyme. Genetic comparisons of horseweed accessions from around the state suggest that there have been multiple, independent origins of resistance in this species, rather than the spread of resistance from a single-source population . Hairy fleabane populations resistant to glyphosate were reported in 2007 . Glyphosate resistance in hairy fleabane appears to be similar to resistance in horse weed in that selection has occurred in response to similar management strategies in perennial crops and surrounding areas ; multiple origins of resistance are suspected ; and growth stage and environmental conditions affect the level of resistance . The discovery by Moretti, Hanson et al. of hairy fleabane resistant to both glyphosate and paraquat raises questions about whether a common physiological mechanism is helping to confer resistance to these dissimilar herbicides, and research is ongoing to elucidate these factors. Junglerice resistant to glyphosate was first identified in 2008 in a Roundup Ready corn field in the Sacramento Valley ; since then, glyphosate-resistant junglerice has become widespread in orchards and field crops throughout California . Resistance appears to be due to mutations in the EPSPS target site , although some populations also appear to have enhanced EPSPS activity . Target-site mutations appear to be the most frequent mechanism among the accessions so far collected in California; however,blueberry pot size additional research is ongoing to determine whether the same is true with populations selected in orchards and in other regions of the Central Valley.

Several other common weeds in orchards and vineyards, including Palmer amaranth , three spike goose grass and witch grass , are suspected to have evolved resistance to glyphosate; preliminary research trials by UC researchers and California State University, Fresno, collaborators have been initiated to verify and characterize the putative resistant populations. Since the discovery of herbicide resistant weed bio-types in California, UC research and Cooperative Extension personnel, as well as university and non-university cooperators and students, have conducted locally relevant weed management research in the state. Research and extension efforts have included alternative chemical management techniques using various post emergence and pre-emergence herbicides along with mechanical control measures in an integrated approach. Applied research integrating agronomy, weed control, spray application technology and water management have been useful to regulatory agencies and have had positive impacts on water and air quality, wildlife habitat and water use . Information on the underlying mechanisms and genetic basis of resistance provides useful information to California weed managers in the longer term. This information is broadly applicable to the biology, physiology, evolution and control of weeds in other crops and regions at the local, national and international level. Although this paper has focused on the efforts of UC weed scientists and collaborators, the basic and applied scientific information developed in California supports similar research being conducted in other regions of the country and world. Like many other areas encompassed by the Endemic and Invasive Pests and Diseases Strategic Initiative, solutions to herbicide resistance are not simple and are affected by many biological, economic, regulatory and social factors. The diverse network of weed scientists and collaborators in a land-grant university system is well positioned to address these complex issues and respond to stakeholder concerns through applied and basic research, extension and outreach to affected agricultural industries, and education of future scientists and leaders. Ultimately, the goal of weed science research is to help growers maintain agricultural productivity and economic stability while increasing environmental sustainability.

Increasing groundwater use for agriculture and public utilities in the last century have put pressure on and diminished groundwater storage in California’s aquifers. The severe droughts that occurred over the last decade were exceptionally warm and dry, including some of the driest years since the late nineteenth century, further exacerbating the adverse effects of decreased ground water water resources . Years of decreased precipitation and increased groundwater extraction have rendered many of California’s groundwater basins and sub-basins to be in a state of groundwater overdraft, where out fluxes of groundwater through pumping or other natural processes greatly exceed influxes to groundwater storage. State agencies recently tasked with achieving groundwater sustainability by 2040, known as Groundwater Sustainability Agencies , have taken action to correct how we can locally manage groundwater resources in California in order to combat groundwater overdraft through the Sustainable Groundwater Management Act . Given how crucial groundwater is to California’s growing population and massive agricultural industry, it is imperative to practice sustainable management of this vital resource. The consequences of mismanagement of California’s groundwater resources are the driving force behind the implementation of methods that can help restore and increase groundwater storage in aquifer systems across the Central Valley. Rising in prevalence as a way of both maintaining and improving groundwater levels is managed aquifer recharge , a process that intentionally places more water into groundwater aquifers than would naturally occur using surface spreading or injection methods . The method of MAR used in this project, agricultural-managed aquifer recharge , spreads diverted surface water onto fallow agricultural fields to recharge groundwater supplies and store water for future use. The feasibility of MAR in agricultural settings depends on water availability, infrastructure, crop tolerance, and the suitability of soil to allow for deep percolation .

The suitability of soil in agricultural fields can be assessed using the Soil and Agricultural Groundwater Banking Index to determine if ag-MAR would be a viable and successful method of replenishing groundwater in a certain area, depending on the rate of deep percolation through the material, residence time of water in the root zone, soil chemistry, as well as topographic and other surface conditions . As long as conditions are viable, ag-MAR can be implemented annually, providing a reliable and sustainable source of stored groundwater to be used in times of drought when other water sources are deficient. In the coming years, GSAs may look towards ag-MAR as a powerful tool in sustainable groundwater management. However, ag-MAR is not only a tool to replenish our groundwater resources, as this application has multiple benefits to an environmental system,raspberry container size including nearby communities and wildlife. There are a limited number of studies that assess the multiple benefits of ag-MAR projects in addition to the apparent hydrologic response in a field’s underlying water table. Although ecological benefits may be harder to measure than hydrologic benefits, considering benefits to wildlife and the environment as design outcomes may have a positive influence on gaining stakeholders to implement more ag-MAR projects. MAR projects undoubtedly have the potential to bridge the gap between two distinct but connected fields of science. Ag-MAR projects are important, especially in California’s Central Valley, because they provide a sustainable way to manage and store groundwater while also being an ecological asset to migratory birds and other organisms that depend on wetland habitats . Across California, groundwater extraction accounts for 40% of the water supply for farms and cities . Colusa County, like many counties in the Central Valley, is highly dependent on pumping groundwater to support their agricultural production. Increased groundwater pumping has resulted in groundwater level declines of >20 ft over the last decade, which highlights the necessity of practicing sustainable groundwater management at the local level. Implementing ag-MAR in Colusa County gives support to farmers while recharging groundwater resources for local communities’ future water usage. The Nature Conservancy , in partnership with Colusa Groundwater Authority, has developed a multi-benefit recharge program to compensate farmers that volunteer their fields to be flooded during the fall season when water resources are limited but migratory bird and waterfowl habitat are in high demand during the fall migratory season . Desirable conditions in the fields that are conducive to both recharge and bird stopovers are those that best mimic a natural wetland habitat. The idea of the TNC project is to convert agricultural fields to temporary wetland habitats that have enough standing water and are free of orchards and other trees that would limit space in the fields and inhibit the bird’s eye view of the fields from above, as migrating birds are more inclined to stop in open flooded fields . Incentive programs like TNC’s on-farm multi-benefit recharge program or BirdReturns, are known to produce a large proportion of open water habitats in post-harvest rice fields during times of drought . BirdReturns and other incentive programs were responsible for providing, on average, 35% of the wetland habitat on the landscape during the 2013-2015 drought, with a few days even reaching up to 100% of the wetland habitat . Previous results of TNC’s incentive program have shown some of the largest average densities in shorebird presence in this agricultural region when wetland habitat was provided for migratory birds that are usually unable to stop in fallow rice fields . The timing of flooding during the fall also makes these ag-MAR sites valuable habitats for birds during migration season when habitats are in deficit, especially during drought .

Just as incentive programs provide a means of sustaining migratory bird populations during dry years, they also provide a way of restoring groundwater resources for use during drought, which further highlights the importance of multi-benefit recharge programs.The goal for this study was to develop two groundwater models using MODFLOW in order to simulate and understand the effects of conducting ag-MAR on selected field sites in Colusa County during the fall season. The first model developed was a large-scale regional model, called the parent model, which was built to derive a more refined, and local child model, which mainly focused on selected recharge sites. The development of the parent and child models allowed us to quantitatively and qualitatively assess the benefits of ag-MAR on the study area’s groundwater resources, the water supply of nearby communities, and as a wetland habitat for migratory birds. In addition to quantifying the effects to these beneficial users, with the results of our models we aimed to answer the following key research questions:1. Through the process of groundwater model development and analysis of results, what guidelines can we provide for optimizing the design of multi-benefit groundwater recharge projects like this in the future? 2. How does the timing, frequency, and amount of recharge affect the results of our model, and what are the benefits of changing each factor? Also, what would we need to monitor to measure these benefits? 3. In what ways can we use groundwater models in the context of understanding hydrologic and environmental impacts in multi-benefit recharge projects, and what answers can we derive from such models?The project area is located in Colusa County, California, in the northern Sacramento Valley region . Located in the Colusa groundwater subbasin of the Sacramento Valley groundwater basin, the project area is bounded by the foothills of the Coast Ranges in the west, and the Sacramento River and other surface water features in the east near the Sutter Buttes. The topography of the project area is mostly flat agricultural land, with higher topography in the southwestern area near the foothills of the Coast Ranges and in the east near the Sutter Buttes. With the exception of a few major urban centers and wildlife refuges, the land use in the area is predominantly agricultural. Agriculture in the area is supported with irrigation water supplied to growers via surface water features like canals and supply systems .Major surface water features in the study area include the Sacramento River, Butte Creek, Butte Slough, the West Borrow Ditch, the Colusa Trough, and the Glenn-Colusa Canal. The Sacramento River flows north to south along the eastern border of the parent model domain and serves as the principal stream in the Colusa Subbasin, significantly contributing to California’s water supply . Regionally, streams that drain the Coast Ranges and Sierra Nevada serve as tributaries to the Sacramento River .