Freshwater Bivalve Ecotoxoicology - Chapter 7 ppt

Chronic toxicity tests have been developed for a number of aquatic species, but test methods for unionid mussels are still being developed or reﬁned.. The toxicity of cadmium and copper

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7 Unionid Mussel Sensitivity to

Environmental Contaminants

Anne Keller, Mike Lydy, and D Shane Ruessler

INTRODUCTION

In the 1960s and 1970s, chemical impacts on aquatic toxicity tests that lasted 2–4 days (NAS/NAE 1973; Johnson and Finley 1980; Mayer and Ellersieck 1986) These test lengths were adequate to determine short-term effects using death as the endpoint While such relatively simple tests are not

an exact measure of chemical toxicity in a stream or lake because local factors can ameliorate or exacerbate effects, they served as the basis of most early water quality criteria because they comprised the best and most abundant available data At that time, the art and science of toxicity testing was in its infancy and chronic tests require substantially more sophistication relative to equipment, facilities and expertise Acute tests provide repeatable results, as well as being simple, rapid, inexpensive, and provide an easily recognizable endpoint-death Acute data were and are still used to compare toxicity among species, trophic levels, different formulations, and different compounds (Johnson and Finley 1980; Mayer and Ellersieck 1986)

US water quality criteria were originally based upon toxicity data from a suite of aquatic species that represented 95% of those tested (Stephan et al 1985) For each chemical, a set of test data that include plant and animal species from several trophic levels, having different habitat requirements, relying on different food sources, and with different life spans were used Taken together, responses

of several taxa more adequately portray the toxicity of a chemical to the ecosystem than do toxicity data from just one or two species Data from bioaccumulation studies, ﬁeld exposures and any available chronic data were also included when available The use of a suite of species also provided the opportunity to include data from species that are important to society because they are food sources, of recreational value, or are species of special concern because they are threatened or endangered Included in the latter category are many species of unionid mussels However, because the life history of unionids makes laboratory culture very difﬁcult, no acute toxicity data were available for unionids during early criteria development

Though fewer chronic than acute toxicity tests exposures have been conducted over the years because of the added expense and difficulty of maintaining aquatic species in the laboratory for extended periods, they are of great value in better estimating the effects of chemicals in aquatic systems Results from such tests provide regulators a fine-tipped pen with which to establish a more realistic margin of safety than the current approach, which may rely on the use of an arbitrary value when more specific data are lacking Chronic toxicity tests have been developed for a number of aquatic species, but test methods for unionid mussels are still being developed or refined Road-blocks to the development of chronic tests include the difficulty of maintaining unionids in the laboratory, the fact that tests would have to be longer than for many other taxa due to lengthy unionid life spans, the need to determine appropriate endpoints, etc These issues are being addressed in a collaborative research project now underway by the U.S Geological Survey and the USEPA

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This chapter reviews the sensitivity of freshwater mussels to metals, pesticides, and other contaminants of freshwater systems Data from these mollusks, in decline throughout North America and other parts of the world, were not used to establish water quality criteria for fresh waters because such information was virtually nonexistent in the early-to-mid-1980s when the USEPA began developing its water quality program (Stephan et al 1985; Augspurger et al 2003) However, in response to the precipitous loss of species and decreased abundance of unionid mussels in recent years, attention has turned to water pollution as a possible cause This spurred interest among a number of researchers to establish test protocols and collect much needed data Recently, the USEPA has begun to use these data to evaluate the protectiveness of a number of metal and other chemical criteria to unionids It is possible that criteria for several metals and ammonia will be modiﬁed by inclusion of unionid data into the database Current water quality criteria are included in chapter tables for comparison to data for this imperiled fauna

METAL TOXICITY

The complicated reproductive strategy of freshwater mussels was probably the major factor limiting the availability of early life stage toxicity data(Chapter 5).Unlike Asian or fingernail clams, most unionid larvae, called glochidia, must attach to a fish host for 7–30 days or more, during which they transform and grow into juveniles, are transported to new areas, and drop off This larval transfor-mation process made laboratory culture of unionids difficult until new methods were developed (Isom and Hudson 1982; Keller and Zam 1990) Beginning in the late 1980s and early 1990s, several laboratories began to measure the sensitivity of unionid glochidia, juveniles and adults (Schweinforth and Wade 1990; Keller and Zam 1991; Jacobson et al 1993) Even so, toxicity data for unionids are available for only a fraction of the contaminants that enter the aquatic systems of North America

Several researchers have evaluated the toxicity of mining-related contaminants to unionids that inhabit nearby streams (Cherry and Farris 1991; Cherry, Farris, and Neves 1991; McCann 1993; Hansten, Heino, and Pynnonen 1996) These tests were based on the change in glochidial closing response when salt is added to water in their test chamber following exposure to a metal for a predetermined length of time Healthy glochidia close when salted, a response that mimics their reaction to ﬁsh mucus

The toxicity of cadmium and copper have been tested frequently, probably because they are common contaminants in industrialized areas and are very toxic to aquatic organisms (Holwerda and Herwig 1986; Hemelraad, Holwerda, and Zandee 1986a; Jacobson 1990; Farris, Van Hassel, and Cherry 1991; Keller and Zam 1991; Lasee 1991; Naimo, Waller, and Holland-Bartels 1992a; McCann 1993), but many other metals also have been evaluated Less is known about the toxicity of organic contaminants to mussels

ACUTETOXICITY OFMETALS

Glochidia tests are performed by exposing the larvae to a contaminant and then testing their viability after 24–48 h (McCann 1993; Hansten, Heino, and Pynnonen 1996; Keller and Ruessler 1997), determining transformation success after attachment to a host ﬁsh (Jacobson et al 1997) or measuring activity deﬁned as the number of valve openings and closings in a given time period (Varanka 1977) Fewer than two dozen papers evaluating the toxicity of metals to glochidia have been published (Chapter 5)

Several approaches to glochidia tests have been used These include measuring changes in the

“snapping” response (Granmo and Varanka 1979), their closing response after exposure to

a contaminant (Jacobson et al 1997; Keller and Ruessler 1997), their uptake of vital stain (Jacobson

et al 1997), and transformation success after exposure of glochidia to a chemical (Jacobson et al 1997)

Freshwater Bivalve Ecotoxicology 152

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Granmo and Varanka (1979) conducted a study of copper and zinc toxicity to Anodonta cygnea (L.) glochidia based on how glochidial “snapping” activity was modulated after exposure to contaminants The opening and closing of glochidia valves is an important part of their attracting host ﬁsh and in attaching to them They determined that copper and zinc exposure reduced the snapping signiﬁcantly Since the tests were performed using concentrations up to 1000 times higher than current US water quality criteria (USEPA 1999a), results are of only limited value in deter-mining the impact of metals on the likelihood of attachment to a host

Since developing glochidia are held in the brood chamber (gill) of the female mussel, isolated from ambient by only a few layers of cells prior to their release, the potential impact of contami-nants on glochidia while within the brood chambers is also of interest Cherry, Farris, and Neves (1991) found that the viability of Villosa nebulosa developing glochidia was not impacted when the adult was exposed to copper (12–192 mg/L) These results support conclusions of other research that glochidia are isolated from the outside environment during residence in the female’s gills (Silverman, McNeil, and Dietz 1987; Lasee 1991; Richard, Dietz, and Silverman 1991) In contrast, Huebner and Pynnonen (1992) and Jacobson et al (1997), found that glochidia from gravid females exposed to metals were sometimes less viable than unexposed glochidia So, this issue remains unresolved

Hansten, Heino, and Pynnonen (1996) tested glochidia of Anodonta anatina, Villosa iris, Medionidus conradicus, A cygnea, Actinonaias pectorosa, and A anatina for sensitivity to cadmium, zinc, and copper Toxicity was apparent at metal concentrations similar to US acute water quality criteria recommendations(Table 7.1) Not unexpectedly, humic acids, EDTA, iron, and manganese, all chelators of metals, ameliorated toxicity (Hansten, Heino, and Pynnonen 1996) Published results of juvenile unionid mollusk toxicity tests are somewhat more numerous than for glochidia tests, and several test parameters have been evaluated for their effects on toxicity Juvenile age, test temperature, and water hardness are known to impact the toxicity of metals (Jacobson 1990; Keller and Zam 1991; Lasee 1991; McCann 1993) Increased hardness and lower test temperature decreased toxicity, and older juveniles (14 days) were somewhat less sensitive to metals than were younger ones (0 days) These ﬁndings are generally similar to those for other aquatic species

Keller and Zam (1991) evaluated the 48- and 96-h toxicity of zinc, copper, cadmium, mercury, chromium, and nickel to juvenile Utterbackia imbecilis mussels in soft (40–48 mg/L as CaCO3) and moderately hard water (80–100 mg/L as CaCO3) Zinc was the least toxic metal while cadmium was most toxic to these juveniles Zinc toxicity (LC50) ranged from 268 to 438 mg/L at 96 h, depending on water hardness McCann (1993) reported similar values—339–1,185 mg/L at 48 h The current US criterion recommendation for zinc is 120 mg/L in water with 100 mg/L hardness (USEPA 1999a)

Jacobson et al (1993) measured sublethal copper toxicity in exposed juvenile V iris and Villosa grandis based on their uptake of neutral red, a vital stain Uptake ceased at 29 mg/L Cu indicating morbidity, while the 24 h LC50 was 83 mg/L for V iris These concentrations are similar to the current acute and chronic criteria recommendations for copper in water of 100 mg/L CaCO3 hard-ness, 13 and 9 mg/L, respectively (USEPA 1999a)

Unionid sensitivity has been compared to other aquatic species in side-by-side tests (Keller 1993; Masnado, Geis, and Sonzongi 1995) Masnado, Geis, and Sonzongi (1995) used different concentrations of metals in a series of synthetic effluents (e.g., chromium, copper, zinc, cadmium, and nickel) to determine the threat a mine effluent would pose to downstream populations of unionid mussels Fathead minnows (Pimephales promelas) and Ceriodaphia dubia were more sensitive to the effluents than were U imbecilis mussels Keller (1993) exposed C dubia and juvenile U imbecilis mussels to an effluent containing 6.4 mg/L chromium The 48-h LC50s were 61 mg Cr/L for U imbecilis and 36 mg Cr/L for C dubia By 96 h, the mussel and zooplankton LC50s each had decreased by one-third The current acute criterion recommendation for chromium

in water of 100 mg/L CaCO3hardness is 74 mg Cr/L (USEPA 1999a)

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TABLE 7.1

Summary of Selected Metal and Inorganic Toxicity Data for Unionid Mussels

Chemical or Physical LC50s

Cu (mg/L) (mg/L)Cd (mg/L)Zn (mg/L)Hg (mg/L)Ni (mg/L)Cr (mg/L)K (mg/L)F

Ammonia at

pH 8.0 (mg/L)

Tempera-ture (8C) (SU)pH Reference Species Glochidia Juvenile Adult Exposure(h) Hardness (Temp.)Test 13 a 2.0 b 120 a 1.4 a 470 a 570 a — — 8.4 c NA 6.5–9.0 d

Granmo and

Varanka

(1979)

Keller and Zam

Huebner

and

Pynnonen

(1992)

Hansten, Heino,

and

Pynnonen

(1996)

McCann (1993) Medionidus

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Dimock and

Wright

(1993)

Pyganodon

Dimock and

Wright

(1993)

Jacobson (1990) Anodanta

Jacobson (1990) Lampsillis

Cherry, Farris,

and Neves

(1991)

Ptychobranchus

Cherry, Farris,

and Neves

(1991)

Cherry, Farris,

and Neves

(1991)

Cherry, Farris,

and Neves

(1991)

Klaine, Warren,

and Summers

(1997)

Klaine, Warren,

and Summers

(1997)

Augspurger et al.

Keller and

Augspurger

(2005)

Alasmidonta

Keller and

Augspurger

(2005)

Keller and

Augspurger

(2005)

Keller and

Augspurger

(2005)

(continued)

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TABLE 7.1 (Continued)

Chemical or Physical LC50s

Cu (mg/L) (mg/L)Cd (mg/L)Zn (mg/L)Hg (mg/L)Ni (mg/L)Cr (mg/L)K (mg/L)F

Ammonia at

pH 8.0 (mg/L)

Tempera-ture (8C) (SU)pH Reference Species Glochidia Juvenile Adult Exposure(h) Hardness (Temp.)Test 13 a 2.0 b 120 a 1.4 a 470 a 570 a — — 8.4 c NA 6.5–9.0 d

Keller and

Augspurger

(2005)

Keller and

Augspurger

(2005)

a USEPA 2002, acute criterion recommendation; listed in the dissolved fraction of the metal concentration.

b USEPA 1999a, acute criterion recommendation; listed in the dissolved fraction of the metal concentration.

c USEPA 1999b, acute criterion recommendation.

d USEPA 1976.

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Lasee (1991) conducted a histological and ultrastructural study of Lampsilis ventricosa in which she examined the impact of cadmium on tissues and organs She ran toxicity tests as part

of the study and calculated 48-h LC50s of 141 mg Cd/L–345 mg Cd/L at 150 mg/L hardness for juveniles at 0–14-days posttransformation These values are similar to those seen by Keller and Zam (1991), who reported 48-h LC50s of 9 mg Cd/L–107 mg Cd/L at w40 and 80 mg/L hardness, respectively The current US criterion recommendation is 4.3 mg Cd/L in water with 100 mg/L hardness (USEPA 1999a)

Few adult unionid mussel toxicity tests have been reported, probably because their maintenance requirements in the laboratory have not been well characterized Imlay (1971) described 25 mg Cu/L

as “lethal” to mussels (species not identiﬁed) A set of 28-day ﬂow-through copper toxicity tests was performed by Keller et al (unpublished data) in 1996 using adult mussels in well water The LC50s for U imbecilis and Elliptio buckleyi were 69 and 4.5 mg Cu/L, respectively, at a hardness of

185 mg/L as CaCO3

SUBLETHALTOXICITY OFMETALS

Exposures of mussels to low concentrations of a metal for a long period of time (greater than seven days) permit the measurement of sublethal effects on processes such as growth (Hinch and Green 1989; Schweinforth and Wade 1990; Lasee 1991; Metcalfe-Smith and Green 1992), enzyme pro-duction (Reddy and Chari 1985), ionic balance (Malley, Huebner, and Donkersloot 1988; Pynnonen 1991; Sivaramakrishna, Radhakrishnaiah, and Suresh 1991), amino acid content of tissues (Gardner, Miller, and Imlay 1981), metallothionein production (Couillard, Campbell, and Tessier 1993; Malley et al 1993), and others Some of these responses may prove to be useful

as indicators or biomarkers of exposure to metals and may improve the use of mussels as sentinels

of ecosystem health Virtually no information is available on the sublethal impact of metal pollution

on glochidia or juvenile mussels

A series of papers published by Jenner et al (1991) and Hemelraad, Holwerda, and Zandee (1986a, 1986b, 1990a, 1990b) monitored tissue uptake and responses of A anatina and A cygnea to sublethal cadmium exposure They found that cadmium accumulated in soft tissues linearly at low concentrations and in a biphasic manner at higher concentrations; that gills accumulated the greatest amount of cadmium; that exposure to cadmium disturbed energy metabolism; and that ionic balance of the hemolymph and tissues was disrupted

Reports from a number of other laboratories amplify these results Oxygen consumption, ciliary activity, and heartbeat were significantly reduced in Lamellidens marginalis exposed to lethal and sublethal cadmium concentrations (6 and 2 mg/L Cd) for one to ten days (Radhakrishnaiah 1988) These physiological impacts resulted from increased mucus production by the gills during cadmium exposure In a longer study by Naimo, Waller, and Holland-Bartels (1992a) respiration rates decreased in L ventricosa exposed to sublethal concentrations of cadmium for 28 days However, ammonia excretion, mussel condition, and food assimilation efficiency were not found to change significantly, perhaps a result of the high variability among individual animals (Naimo, Waller, and Holland-Bartels 1992a) Mucus production also increased in the animals tested by Naimo, Waller, and Holland-Bartels (1992b) ATPase activity and ciliary activity of gills in A cygnea was decreased following exposure to cadmium (Pirovarova, Lagerspetz, and Skulskii 1992) Similarly, Raj and Hameed (1991) determined that sublethal concentrations of copper and mercury accelerated the respiratory rate of L marginalis, while cadmium depressed it In this latter study, body weight decreased following 30-day exposures to copper Finally, the synthesis of porphyrins (part of cyto-chrome, enzyme, vitamin, and myoglobin molecules) was disrupted in Elliptio complanata and

A grandis mussels exposed to low concentrations of cadmium (Chamberland et al 1995) Digestive activity and efﬁciency can also be impacted by cadmium toxicity Both Hameed and Raj (1989) and Lasee (1991) found that exposure to copper, cadmium, or mercury resulted in the dissolution of the

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crystalline style in Lamellidens marginalis and L ventricosa, respectively The style grinds ingested food before it is digested Exposure to mercury caused the fastest dissolution of the style of the three metals tested (Hameed and Raj 1989), and resulted in the slowest recovery

Metallothionein production was induced by exposure of several mussel species to cadmium, copper, zinc, and other metals (Couillard, Campbell, and Tessier 1993; Malley et al 1993; Couillard et al 1995) These proteins serve as protectors from metal toxicity and have been used

as biomarkers of exposure to metals Perhaps in attempting to relate cause and effect for declining mussel populations, biomarkers such as these would be useful

The reported impacts of sublethal metal stress on mollusks strongly suggest that while exposure

to metals may not be immediately apparent, lethality may result from eventual disruption of metabolic activities, enzyme functions, respiration, and other important processes For the long-lived unionid mussels, repeated insults by metal pollution may be partially responsible for their continual decline A number of mussel LC50s are similar to water quality criteria used to establish efﬂuent concentration limits (e.g., copper and zinc) Most criteria were established based on data that lacked unionid toxicity test results because such data did not exist at the time So, even though calculations include a built-in uncertainty factor designed to be protective (Stephan et al 1985), the lack of unionid toxicity data in those calculations may mean that some metal criteria are not adequately protective of freshwater mussels

ORGANIC CHEMICAL TOXICITY

ACUTETOXICITY OFORGANICCONTAMINANTS

The published literature describing the impacts of acute exposure of mussels to various organic compounds is more limited than for metals Most of the available information describes responses

to pesticides; these compounds are often found in aquatic systems as an indirect result of runoff or atmospheric deposition, although spills—both intentional and unintentional—also occur (Mulla and Mian 1981) Some documents have reviewed the toxic effects of contaminants; an excellent compendium of toxicity data is included in the work of Havlik and Marking (1987) and will not

be duplicated here Acute toxicity data are vital to develop adequately protective restrictions on pesticide use in areas where they may detrimentally affect sensitive or endangered species of unionid mussels and other mollusks (Keller 1993) and to assess the risk posed by chemical spills Most toxicity tests have found freshwater mollusks to be less sensitive to pesticides, herbicides, and other organic compounds than are the target organisms or other taxa

Toxicity tests using glochidia have been reported for only a few organic compounds using permanent valve closure or inability to respond to stimuli as the measure of lethality In all of the tests except one, glochidia were found to be very insensitive to tested chemicals, including atrazine, cyhalothrin, carbaryl, malathion, and several pesticides used in eastern Europe (Varanka 1979; McLeese et al 1980; Varanka 1987; Johnson, Keller, and Zam 1993; Keller and Ruessler 1997) (Table 7.2) In contrast, Conners and Black (2004) determined that U imbecillis glochidia were as sensitive or more sensitive to glyphosate and carbaryl than other aquatic invertebrates Weinstein and Polk (2001) reported that photo-activated anthracene and pyrene were toxic to U imbecillis glochidia at environmentally relevant concentrations Anthracene was more toxic with a 24-h LC50

of 1.93 mg/L followed by pyrene at 2.63 mg/L

Varanka (1977) investigated the effect of several pesticides on tryptamine-induced activity of the adductor muscle of A cygnea glochidia but found that most effects occurred at concentrations far exceeding environmental concentrations However, malathion caused decreased adductor activity at a concentration of 75 mg/L, which is a realistic environmental concentration In 24-h toxicity tests, Conners and Black (2004) found that U imbecillis glochidia were sensitive to copper, atrazine, glyphosate, and carbaryl, as measured by death and genotoxicity

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TABLE 7.2

Summary of Selected Toxicity Data for Organic Compounds to Unionid Mussels

Chemical LC50s

Mala-thion (mg/L) Pyrene(mg/L)

Anthr-acene (mg/L) (mg/L)PCP

Toxa-phene (mg/L)

Chlor-dane (mg/L)

Aqua-thol (mg/L)

Hydr-othol (mg/L)

Bayth-roid (Mg/L) (Mg/L)2,4-D

Atra-zine (mg/L)

Cyha-lothrin (mg/L) Carbaryl(mg/L)

Johnson, Keller,

Chandler and

Marking (1975) Elliptiosp./Plectomerus

sp.

Keller and Ruessler

Megalonaias

Loxoconcha

Wade, Hudson, and

McKinney

(1989)

Weinstein and Polk

a TFMZ3-triﬂuoromethyl-4-nitrophenol.

b USEPA 2002, chronic criterion recommendation.

c USEPA 2002, acute criterion recommendation.

d 2003, acute criterion recommendation.

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Neither 2,4-D, the mosquito larvicide BTI, nor the herbicide aquathol-K was toxic to juvenile

U imbecillis after 9-day exposures at concentrations up to twice the accepted application rate (Wade, Hudson, and McKinney 1989) Keller (1993) determined that seven of eight organic compounds (including hydrothol, toxaphene, and pentachlorophenol) were less toxic to U imbecillis at 48 h than

to zooplankton or fish PCP was equally toxic to U imbecillis, zooplankton, and fish (Keller 1993) Moderate sensitivity to the lampricide TFM (3-trifluoromethyl-4-nitrophenol) was measured in adult Elliptio spp and Plectomerus spp (Chandler and Marking 1975), but neither of these mollusks was as sensitive as lamprey larvae or other aquatic taxa Similar results were reported

by Waller et al (1993) and Waller, Bills, and Johnson (1997) Juvenile and adult E complanata and Anodonta cataracta and adult O reﬂexa were not impacted by TFM at suggested application rates

In fact, Waller et al (1993) determined that mussels were among the least sensitive taxa to 15 organic chemicals being considered as zebra mussel control agents Similar results were noted in tests performed by Chandler and Marking (1979) in tests with 20 ﬁshery chemicals and Keller and Ruessler (1997) in tests with malathion and various juvenile unionids

Warren (1992) saw no signiﬁcant difference in survival between adult E buckleyi controls and animals exposed to the herbicide glyphosate (Sonar) at recommended dosages in ﬁeld exposures monitored for six months, and after exposure to Sonar in the laboratory for seven days at concen-trations up to 100 times the recommended application rate

SUBLETHALEFFECTS OFORGANICCONTAMINANTS

Sublethal responses of adult mussels following exposure to pesticides and other organics include decreased enzyme activity, abnormal shell growth, changes in metabolism, heart rate, and siphoning activity, and others Relatively fewer studies have evaluated sublethal impacts of pesti-cides and other organic contaminants than have been reported for metals

Machado et al (1990) reported abnormal shell growth in A cygnea exposed to the insecti-cide diﬂubenzuron, designed to retard juvenile metamorphosis The effective concentration was

200 mg/L, far higher than the expected environmental concentration This could increase the mussels’ vulnerability to predation or shell erosion, though even this response was elicited at a concentration much higher than was effective in crustaceans, closer relatives to insects Analogous changes in other tissues have been reported for mussels exposed to various organic contaminants Mane, Akarte, and Kulkarni (1986) recorded biochemical changes in mussels exposed to fenthion, an organophosphate pesticide, including the altered distribution of protein, cholesterol, and particularly glycogen and lipids, in the mantle tissue, gills, hepatopancreas, gonad, foot, and adductor muscles of Indonaia caeruleus A general decrease in glycogen content, the main energy reserve in mussels, was also observed for I caeruleus (Mane, Akarte, and Kulkarni 1986; Makela, Lindstrom-Seppa, and Oikari 1992) Toxicity tests and assessments of acetylcholinesterase inhibition in E complanata following exposure to aldicarb and acephate (Moulton, Fleming, and Purnell 1996) indicated that activity was inhibited after pesticide exposure and was affected by test temperature but recovered after 12 days Considerable variability in enzyme activity was reported

in control animals and may have masked the impact of the pesticides on the shell closing response that is mediated by the activity of the enzyme in the adductor muscle However, the researchers recommended further evaluation of the assay as a measure of ﬁeld exposure of mussels to agricultural chemicals

Rao, Rao, and Rao (1983) measured the effects of malathion (40 mg/L) and methyl parathion (10 mg/L) on L marginalis heart rates Both pesticides caused a decrease in heart rate, but these responses were elicited only at concentrations higher than expected environmental concentrations (EEC) Similar inhibition was noted by Senthilmurugan et al (1994) in the same species when exposed to phosphamidon at 0.015 mg/L, possibly leading to the disruption of metabolic processes and growth

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