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Critical review: Grand challenges in assessing the adverse effects of contaminants of emerging concern on aquatic food webs

Much progress has been made in the past few decades in understanding the sources, transport, fate, and biological effects of contaminants of emerging concern (CECs) in aquatic ecosystems. Despite these advancements, significant obstacles still prevent comprehensive assessments of the environmental risks associated with the presence of CECs. Many of these obstacles center around the extrapolation of effects of single chemicals observed in the laboratory or effects found in individual organisms or species in the field to impacts of multiple stressors on aquatic food webs. In the present review, we identify 5 challenges that must be addressed to promote studies of CECs from singular exposure events to multispecies aquatic food web interactions. There needs to be: 1) more detailed information on the complexity of mixtures of CECs in the aquatic environment, 2) a greater understanding of the sublethal effects of CECs on a wide range of aquatic organisms, 3) an ascertaining of the biological consequences of variable duration CEC exposures within and across generations in aquatic species, 4) a linkage of multiple stressors with CEC exposure in aquatic systems, and 5) a documenting of the trophic consequences of CEC exposure across aquatic food webs. We examine the current literature to show how these challenges can be addressed to fill knowledge gaps.

Environmental Toxicology and Chemistry

Year and age effects on residues of dieldrin and heptachlor in dead gray bats, Franklin County, Missouri— 1976, 1977, and 1978

Dead gray bats ( Myotis grisescens ) containing lethal concentrations of dieldrin were found beneath a maternity roost in Bat Cave Nos. 2 and 3, Franklin County, Missouri, in 1976, 1977 and 1978. Whereas residues of dieldrin, DDE [1,1-dichloro-2,2-bis( p -chlorophenyl)ethylene] and PCB polychlorinated biphenyls in bats appeared not to change significantly over the 3 years, residues of heptachlor-related chemicals increased in 1977 to potentially dangerous concentrations and remained elevated in 1978. Lethal brain levels of dieldrin in adult bats (geometric mean = 12.1 μg/g), compared with juvenile bats (geometric mean = 6.5 μg/g), indicated that juveniles are nearly twice as sensitive. The estimated population of gray bats (as maximum number of nonflying young) at Bat Cave Nos. 2 and 3 in 1976 and 1978 was 1,800 bats, but in 1979 no bats were present. Dieldrin, perhaps in conjunction with heptachlor, may have caused the decline and disappearance of this colony. However, dieldrin was banned in 1974 and Missouri's authorization to use heptachlor on corn expired in 1981. Furthermore, three organophosphate insecticides (chlorpyrifos, dyfonate and mocap) are to be substituted. We hope that the gray bats remaining in this area of Missouri survive the residues of dieldrin and heptachlor still in their food chains and prove to be unaffected by the new organophosphates.

Environmental Toxicology and Chemistry

Agricultural sources of contaminants of emerging concern and adverse health effects on freshwater fish

Agricultural contaminants of emerging concern (CECs) are generally thought of as certain classes of chemicals associated with animal feeding and production facilities. Veterinary pharmaceuticals used in animal food production systems represent one of the largest groups of CECs. In our review, we discuss the extensive increase in use of antibiotics in animal feeding operations (AFOs) around the world. AFOs are a major consumer of antibiotics and other veterinary pharmaceuticals and over the past decade there has been growing information on the occurrence, release, and fate of CECs from animal food production operations, including the application of pharmaceutical-containing manure to agricultural fields and releases from waste lagoons. Concentrations of CECs in surface and ground water in proximity to AFOs correspond to their presence in the AFO wastes. In many cases, the environmental concentrations of agriculturally-derived CECs are below toxicity thresholds. Hormones and hormone replacement compounds are a notable exception, where chemical concentrations near AFOs can exceed concentrations known to cause adverse effects on endocrine-related functions in fish. In addition, some agricultural pesticides, once thought to be safe to non-target organisms, have demonstrated endocrine-related effects that may pose threats to fish populations in agricultural regions. That is, we have pesticides with emerging concerns, thus, the concern is emerging and not necessarily the chemical. In this light, one must consider certain agricultural pesticides to be included in the list of CECs. Even though agricultural pesticides are routinely evaluated in regulatory testing schemes which have been used for decades, the potential hazards of some pesticides have only recently been emerging. Emerging concerns of pesticides in fish include interference with hormone signaling pathways; additive (or more than additive) effects from pesticide mixtures; and adverse population-level effects at concentrations below predicted toxicity thresholds. Consequently, there is a need to evaluate the environmental concerns related to pesticide exposures to fish populations based on current biological and toxicological techniques. This presentation reviews some of the agricultural chemicals that have emerged as contaminants of concern and potentially threaten fish populations in agricultural watersheds.

Conference Paper

Application of transcriptomics concentration-response modeling for prioritization of contaminants detected in tributaries of the North American Great Lakes

As part of the Great Lakes Restoration Initiative, chemical monitoring and surveillance efforts have detected approximately 330 chemicals in surface water of Great Lakes tributaries. There were 140 chemicals for which no empirical toxicity data were available. The aim of this study was to generate transcriptomic points of departure (tPODs) for 10 of these compounds and demonstrate how they could be applied in a screening-level prioritization. Organisms representing three trophic levels of the aquatic food web ( Pimephales promelas , Daphnia magna , and Raphidocelis subcapitata ) were exposed for 24 hr to a half-log dilution series of nominal exposure concentrations typically ranging from 66.7–0.021 µM of each chemical. In addition to observations of apical effects (e.g., survival and morphology), whole body transcriptomic responses (tPODs) to each chemical were evaluated with targeted analysis using TempO-seq for P. promelas and D. magna and nontargeted RNA-seq for R. subcapitata . The tPODs ranged from 0.18–10.8 µM for P. promelas and 0.32–29 µM for D. magna , with the most potent of the chemicals tested being fipronil carboxamide for both species. For R. subcapitata , the tPODs ranged from 0.04–1.77 µM, with gabapentin as the most potent chemical tested. Empirically derived tPODs from these data-poor chemicals were compared with concentrations detected in the Great Lakes basin. Environmental concentrations were less than the tPODs except for R. subcapitata and 3,4-dichlorophenyl isocyanate. Similarly, tPODs from previously tested data-rich chemicals were compared with environmental concentrations, in which case tPODs from several chemicals overlapped environmental concentrations. This work demonstrates the potential utility of emerging ecological high-throughput transcriptomics assays to support screening and prioritization of data-poor environmental contaminants.

Environmental Toxicology and Chemistry

Use of riparian spiders as sentinels of persistent and bioavailable chemical contaminants in aquatic ecosystems: A review

Aquatic ecosystems around the world are contaminated with a wide range of anthropogenic chemicals, including metals and organic pollutants, that originate from point and nonpoint sources. Many of these chemical contaminants have complex environmental cycles, are persistent and bioavailable, can be incorporated into aquatic food webs, and pose a threat to the health of wildlife and humans. Identifying appropriate sentinels that reflect bioavailability is critical to assessing and managing aquatic ecosystems impacted by contaminants. The objective of the present study is to review research on riparian spiders as sentinels of persistent and bioavailable chemical contaminants in aquatic ecosystems. Our review of the literature on riparian spiders as sentinels suggests that significant progress has been made during the last two decades of research. We identified 55 published studies conducted around the world in which riparian spiders (primarily of the families Tetragnathidae, Araneidae, Lycosidae, and Pisauridae) were used as sentinels of chemical contamination of lotic, lentic, and estuarine systems. For several contaminants, such as polychlorinated biphenyls (PCBs), Hg, and Se, it is now clear that riparian spiders are appropriate sentinels. However, many contaminants and factors that could impact chemical concentrations in riparian spiders have not been well characterized. Further study of riparian spiders and their potential role as sentinels is critical because it would allow for development of national-scale programs that utilize riparian spiders as sentinels to monitor chemical contaminants in aquatic ecosystems. A riparian spider sentinel program in the United States would be complementary to existing national sentinel programs, including those for fish and immature dragonflies.

Environmental Toxicology and Chemistry

Increased mercury and reduced insect diversity in linked stream-riparian food webs downstream of a historical mercury mine

Historical mining left a legacy of abandoned mines and waste rock in remote headwaters of major river systems in the western United States. Understanding the influence of these legacy mines on culturally and ecological important downstream ecosystems is not always straight-forward because of elevated natural levels of mineralization in mining-impacted watersheds. To test the ecological effects of historic mining in the headwaters of the upper Salmon River watershed (USA), we measured multiple community and chemical endpoints in downstream linked aquatic-terrestrial food webs. Mining inputs impacted downstream food webs through increased mercury accumulation and decreased insect biodiversity. Total mercury (THg) in seston, aquatic insect larvae, adult aquatic insects, riparian spiders, and fish at sites up to 7.6 km downstream of mining was in much higher concentrations (1.3 to 11.3-fold) and isotopically distinct compared with sites immediately upstream of mining inputs. Methylmercury (MeHg) concentrations in bull trout and riparian spiders were sufficiently high (732 – 918 and 347 – 1,140 ng MeHg g -1 dw) to affect humans, birds, and piscivorous fish. Furthermore, the alpha-diversity of benthic insects was locally depressed by 12-20% within 4.3 to 5.7 km downstream of from the mine. However, because total insect biomass was not affected by mine inputs, the mass of mercury in benthic insects at a site (i.e., ng Hg m -2 ) was extremely elevated downstream (10 – 1,778-fold) compared with directly upstream of mining inputs. Downstream adult aquatic insect-mediated fluxes of total mercury were also high (~16 ng THg m -2 d -1 ). Abandoned mines can have ecologically important effects on downstream communities, including reduced biodiversity and increased mercury flux to higher order consumers, including fish, birds, and humans.

Idaho

Ecological harm and economic damages of chemical contamination to linked aquatic-terrestrial food webs: A study-design tool for practitioners

Contamination of aquatic ecosystems can have cascading effects on terrestrial consumers by altering the availability and quality of aquatic insect prey. Comprehensive assessment of these indirect food-web effects of contaminants on natural resources and their associated services necessitates using both ecological and economic tools. In the present study we present an aquatic-terrestrial assessment tool (AT2), including ecological and economic decision trees, to aid practitioners and researchers in designing contaminant effect studies for linked aquatic-terrestrial insect-based food webs. The tool is tailored to address the development of legal claims by the US Department of the Interior's Natural Resource Damage Assessment and Restoration Program, which aims to restore natural resources injured by oil spills and hazardous substance releases into the environment. Such cases require establishing, through scientific inquiry, the existence of natural resource injury as well as the determination of the monetary or in-kind project-based damages required to restore this injury. However, this tool is also useful to researchers interested in questions involving the effects of contaminants on linked aquatic-terrestrial food webs. Stylized cases exemplify how application of AT2 can help practitioners and researchers design studies when the contaminants present at a site are likely to lead to injury of terrestrial aerial insectivores through loss of aquatic insect prey and/or dietary contaminant exposure. Designing such studies with ecological endpoints and economic modeling inputs in mind will increase the relevance and cost-effectiveness of studies, which can in turn improve the outcomes of cases and studies involving the ecological effects of contaminants on food webs.

Environmental Toxicology and Chemistry

Effects of contaminants on reproductive success of aquatic birds nesting at Edwards Air Force Base, California

Contamination by organochlorine pesticides (OCs), polychlorinated biphenyls, metals, and trace elements at Edwards Air Force Base (EAFB), located in the Mojave Desert, could adversely affect nesting aquatic birds, especially at the sewage lagoons that comprise Piute Ponds. Estimates of avian reproduction, in conjunction with analyses of eggs and avian foods for contaminant residues, may indicate the potential for negative effects on avian populations. From 1996 to 1999, we conducted studies at the Piute Ponds area of EAFB to evaluate the impacts of contaminants on nesting birds. Avian reproduction was evaluated in 1999. Eggs were collected for chemical analyses in 1996 and 1999, and African clawed frogs (Xenopus laevis), a likely food source, were collected for chemical analyses in 1998. Avian species occupying the higher trophic levels-black-crowned night-heron (Nycticorax nycticorax), white-faced ibis (Plegadis chihi), and American avocet (Recurvirostra americana)-generally bioaccumulated higher concentrations of contaminants in their eggs. Reproductive success and egg hatchability of night-herons and white-faced ibises in the Piute Ponds were similar to results observed at other western colonies. Deformities were observed in only one embryo in this study, but concentrations of contaminants evaluated in this ibis embryo were considered insufficient to have caused the deformities. Because clawed frogs, a primary prey item for night-herons at Piute Ponds, had no detectable levels of any OCs, it is likely that OCs found in night-heron eggs were acquired from the wintering grounds rather than from EAFB. The presence of isomers of dichlorodiphenyltrichloroethane (DDT) in ibis eggs indicated recent exposure, but invertebrates used for food by ibises were not sampled at Piute Ponds, and conclusions about the source of OCs in ibis eggs could not be made. Concentrations of contaminants in random and failed eggs of individual species were not different, and we concluded that contaminants did not cause the observed egg failures. ?? 2006 Springer Science+Business Media, Inc.

Archives of Environmental Contamination and Toxico

Energetic dose: Beyond fire and flint?

Nutritional and bioenergetic interactions influence exposure to environmental chemicals and may affect the risk realized when wildlife are exposed in the field. Here, food-chain analysis focuses on prairie voles (Microtus ochrogaster) and the evaluation of chemical risks associated with paraquat following 10-d dietary exposures. Reproductive effects were measured in 60-d trials that followed exposures to paraquat-tainted feed: control (untainted feed); 21 mg paraquat/kg feed; 63 mg paraquat/kg feed; and feed-restricted control (untainted feed restricted to 60% baseline consumption). Reproductive success was evaluated in control and treated breeding pairs, and a preliminary bioenergetics analysis was completed in parallel to derive exposure dose. Although reproductive performance differed among groups, feed-restriction appeared to be the dominant treatment effect observed in these 10-d feeding exposure/limited reproductive trials. Exposure dose ranged from 3.70-3.76 to 9.41-11.51 mg parquat/kg BW/day at 21 and 63 mg paraquat/kg feed stock exposures, respectively. Energetic doses as ug paraquat/kcal yielded preliminary estimates of energetic costs associated with paraquat exposure, and were similar within treatments for both sexes, ranging from 4.2-5.5 and 13.1-15.0 ug paraquat/kcal for voles exposed to 21 mg/kg feed stock and 63 mg/kg feed stock, respectively. Given the increasing likelihood that environmental chemicals will be found in wildlife habitat at 'acceptable levels', the critical role that wildlife nutrition plays in evaluating ecological risks should be fully integrated into the assessment process. Tools applied to the analysis of risk must gain higher resolution than the relatively crude methods we currently bring to the process.

Society of Environmental Toxicology and Chemistry,

Cross-ecosystem fluxes of pesticides from prairie wetlands mediated by aquatic insect emergence: Implications for terrestrial insectivores

Contaminants alter the quantity and quality of insect prey available to terrestrial insectivores. In agricultural regions, the quantity of aquatic insects emerging from freshwaters can be impacted by insecticides originating from surrounding croplands. We hypothesized that, in such regions, adult aquatic insects could also act as vectors of pesticide transfer to terrestrial food webs. To estimate insect-mediated pesticide flux from wetlands embedded in an important agricultural landscape, semipermanetly and temporarily ponded wetlands were surveyed in cropland and grassland landscapes across a natural salinity gradient in the Prairie Pothole Region of North Dakota (USA) during the bird breeding season in 2015 and 2016 ( n = 14 and 15 wetlands, respectively). Current-use pesticides, including the herbicide atrazine and the insecticides bifenthrin and imidacloprid, were detected in newly emerged insects. Pesticide detections were similar in insects emerging from agricultural and grassland wetlands. Biomass of emerging aquatic insects decreased 43%, and insect-mediated pesticide flux increased 50% along the observed gradient in concentrations of insecticides in emerging aquatic insects (from 3 to 577 ng total insecticide g –1 insect). Overall, adult aquatic insects were estimated to transfer between 2 and 180 µg total pesticide wetland –1 d –1 to the terrestrial ecosystem. In one of the 2 study years, biomass of emerging adult aquatic insects was also 73% lower from agricultural than grassland wetlands and was dependent on salinity. Our results suggest that accumulated insecticides reduce the availability of adult aquatic insect prey for insectivores and potentially increase insectivore exposure to insect-borne pesticides. Adult aquatic insects retain pesticides across metamorphosis and may expose insectivores living near both agricultural and grassland wetlands to dietary sources of toxic chemicals.

Alberta, Iowa, Manitoba, Minnesota, Montana, North

Field and laboratory evaluation of the influence of copper-diquat on apple snails in southern Florida

The recent decline of apple snail ( Pomacea paludosa ) populations in canals surrounding Loxahatchee National Wildlife Refuge in southern Florida coincided with the use of copper-diquat for the control of the aquatic weed hydrilla ( Hydrilla verticillata ). Field and laboratory studies were designed to assess the effects of copper-diquat on apple snails, which are the primary food of the endangered snail kite Rostrhamus sociabilis (formerly known as the Everglade kite). Acute toxicities (96-h LC 50 values) of Cutrine-Plus and Komeen (chelated formulations of copper) to immature apple snails were 22 and 24 μg/L, respectively. Diquat was toxic at a concentration of 1,800 μg/L and did not increase the toxicity of copper when the chemicals were used in combination. Evaluation of field samples indicated that copper concentrations were higher in detritus than in water, plants and mud, and that there was a gradient of copper concentration from the canal to the interior, the highest residues being in samples from the canal. Copper associated with detritus (up to 150 μg/g) had no effect on growth or survival of apple snails in field cage and tank studies. Also, field applications of copper-diquat to hydrilla had no effect on survival of caged adult and immature snails. Copper from field applications was rapidly taken out of solution by plants and organic material in the water and subsequently incorporated into the bottom detritus. Although the effects of repeated applications of copper-diquat and high body burdens of copper (accumulated during exposure to herbicidal treatment) on survival and reproduction of apple snails are not known, the information available indicates that treatment of hydrilla with copper-diquat was probably not responsible for the decline in the apple snail population. Application at recommended rates should pose no threat to these snails in the organically rich waters of southern Florida.

Environmental Toxicology and Chemistry

Fate and effects to the benthic community of a copper treatment to eradicate invasive mussels in a large western river, USA

Copper-based chemical treatments are commonly used to eradicate invasive mussels in small ponds and lakes, but their use in large rivers has been limited. In 2023, in response to a detection of invasive quagga mussels, a 10-km reach of the Snake River (Idaho, USA), was treated with an unprecedented 19,300 kg of chelated copper molluscicide to a target concentration of 1,000 µg/L for 10 days. We assessed the transport and fate of the copper and its exposure and effects on the nontarget benthic community downstream. Water samples were collected at seven locations throughout the treatment period, and sediment, periphyton, and benthic macroinvertebrates were collected pre- and posttreatment. Nearly half of the original mass of copper was removed from the water column via sedimentation, sorption to algae, or biological uptake within the 10-km treatment reach and the first 15 km downstream. Even so, dissolved copper concentrations exceeded the acute toxicity threshold at least as far as 28 km downstream for more than 2 weeks. Sediment copper increased by up to 8.3-fold, exceeding the consensus-based sediment quality threshold effect concentration at several sites. Effects on benthic macroinvertebrates varied by taxa. From 0–28 km downstream, invertebrate abundances decreased 52%–94%, with gastropods among the most affected. Of the unique taxa present at these sites pretreatment, 52%–64% were not found posttreatment but were replaced by other taxa, indicating a reorganization of the base of the food web. Additionally, from 0–15 km downstream, the percentage of individuals from tolerant taxa increased two to15-fold. Findings from this study can help watershed managers plan future invasive mussel responses while protecting culturally, economically, and ecologically important nontarget species in large rivers.

Idaho