Freshwater Bivalve Ecotoxoicology - Chapter 7 ppt

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;Johnsonand Finley 1980; Mayerand Ellersieck1986). These test lengths were adequate to determineshort-termeffects using death as the endpoint.While such relatively simple tests are not an exact measureofchemical toxicity in astream or lake because local factorscan ameliorate or exacerbateeffects,theyservedasthe basisofmostearly waterquality criteria becausethey comprised the best and mostabundant available data.Atthat time,the art and science of toxicity testing was in its infancy and chronic tests require substantially moresophistication relative to equipment, facilities and expertise. Acute tests provide repeatable results, as well as beingsimple, rapid, inexpensive, and provide an easily recognizableendpoint-death. Acute data were and are still used to compare toxicity among species,trophiclevels, differentformulations,and different compounds (Johnsonand Finley 1980; Mayerand Ellersieck 1986). US water quality criteria were originally based upon toxicity data from asuite of aquatic species that represented 95% of those tested (Stephan et al. 1985). For each chemical,aset of testdata that include plant and animal species from several trophic levels,havingdifferent habitat requirements, relyingondifferent food sources, and with different life spans were used. Taken together, responses of several taxa more adequately portray the toxicity of achemical 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 includedwhenavailable.The use of asuite of species also provided the opportunity to include data from species that are important to society because they are food sources, of recreationalvalue, or are species of special concern because they are threatened or endangered.Includedinthe lattercategoryare many speciesofunionidmussels. However, because the life history of unionids makes laboratory culturevery difficult, no acute toxicity data were available for unionids during early criteriadevelopment. Though fewer chronic than acute toxicity tests exposures have been conducted over the years because of the added expenseand difficulty of maintaining aquatic species in the laboratory for extended periods, they are of greatvalue in better estimating the effects of chemicalsinaquatic systems. Results from such tests provide regulators afine-tipped pen with which to establish amore realistic margin of safety than the current approach, which may rely on the use of an arbitraryvalue when morespecific data are lacking.Chronictoxicity tests have been developed for anumber of aquatic species, but test methods for unionid mussels are still beingdeveloped 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 longerthan for many other taxa due to lengthy unionid life spans, theneedtodetermine appropriate endpoints, etc. These issues are being addressedinacollaborative research project nowunderway by the U.S. Geological Survey and the USEPA. 4284X—CHAPTER 7—17/10/2006—13:03—JEBA—XML MODEL C–pp. 151–167 151 © 2007 by the Society of Environmental Toxicology and Chemistry (SETAC) This chapter reviewsthe sensitivityoffreshwatermussels to metals,pesticides, andother contaminants of freshwater systems. Data from thesemollusks, in decline throughout North America and otherparts of the world, were not used to establish water quality criteria for fresh watersbecause such information was virtuallynonexistentinthe early-to-mid-1980swhenthe USEPA begandeveloping itswater quality program (Stephan et al. 1985; Augspurgeretal. 2003). However, in response to theprecipitouslossofspeciesand decreasedabundanceof unionid musselsinrecent years, attention has turned to water pollution as apossiblecause.This spurred interest among anumber of researchers to establish testprotocols and collectmuch needed data. Recently, the USEPA has begun to use thesedata to evaluate the protectiveness of anumber of metal and otherchemical criteria to unionids.Itispossible that criteria for several metals and ammoniawill be modified by inclusion of unionid data into the database.Current water quality criteria are includedinchapter tables for comparison to data for this imperiled fauna. METAL TOXICITY The complicated reproductive strategy of freshwater musselswas probably the major factor limiting the availability of early life stage toxicity data (Chapter 5). UnlikeAsian or fingernail clams, most unionid larvae, called glochidia, must attach to afish 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 cultureofunionids 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 measurethe 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 afraction 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 ametal for a predetermined length of time. Healthy glochidia close when salted,aresponse that mimics their reaction to fishmucus. Thetoxicity 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 Cherry1991;Keller and Zam1991; Lasee 1991; Naimo, Waller, and Holland-Bartels 1992a; McCann 1993), butmanyother metalsalso have been evaluated. Less is known about the toxicity of organic contaminants to mussels. A CUTE T OXICITY OF M ETALS Glochidiatests areperformed by exposingthe larvae to acontaminantand then testingtheir viability after 24–48 h(McCann 1993; Hansten, Heino, and Pynnonen 1996; Keller and Ruessler 1997), determining transformation success after attachment to ahost fish (Jacobson et al. 1997)or measuring activity defined as the number of valveopenings and closingsinagiventime 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 changesinthe “snapping”response (Granmoand Varanka 1979),their closing responseafter exposure to acontaminant(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 achemical (Jacobson et al. 1997). Freshwater BivalveEcotoxicology152 4284X—CHAPTER 7—17/10/2006—13:03—JEBA—XML MODEL C–pp. 151–167 © 2007 by the Society of Environmental Toxicology and Chemistry (SETAC) Granmoand Varanka (1979) conducted astudyofcopper and zinc toxicity to Anodontacygnea (L.) glochidiabasedonhow glochidial “snapping” activity wasmodulated after exposureto 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 usingconcentrations up to 1000 times higher than current US water quality criteria(USEPA 1999a), results are of only limited value in deter- miningthe impact of metals on the likelihoodofattachment to ahost. Since developing glochidia are held in the brood chamber (gill) of the female mussel, isolated from ambientbyonly afew layers of cells prior to their release, the potential impact of contami- nants on glochidiawhile within the brood chambers is also of interest.Cherry, Farris, and Neves (1991) found that the viability of Villosanebulosa developing glochidia was not impacted when the adult was exposedtocopper (12–192 m g/L).These results support conclusions of otherresearch 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 sometimesless viable than unexposed glochidia. So,thisissue remains unresolved. Hansten, Heino, andPynnonen(1996) tested glochidiaof Anodontaanatina, Villosairis , Medionidusconradicus , A. cygnea, Actinonaias pectorosa ,and A. anatina forsensitivity 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). Publishedresults of juvenile unionid mollusk toxicity tests are somewhat more numerous than for glochidia tests, and several testparameters have been evaluated for their effects on toxicity. Juvenile age, testtemperature, andwater hardness are known to impactthe toxicity of metals (Jacobson 1990; Kellerand Zam1991; Lasee 1991; McCann1993).Increased hardness and lowertesttemperaturedecreasedtoxicity, andolder juveniles(14 days)weresomewhatless sensitivetometals thanwere youngerones(0days).These findingsare generallysimilar to those for otheraquatic 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 CaCO 3 )and moderately hard water (80–100mg/L as CaCO 3 ). Zinc was the least toxic metal while cadmium was mosttoxic to thesejuveniles. Zinc toxicity (LC50) rangedfrom 268 to 438 m g/L at 96 h, depending on water hardness. McCann (1993) reported similar values—339–1,185 m g/L at 48 h. The current US criterion recommendation for zinc is 120 m g/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, avital stain. Uptake ceased at 29 m g/L Cu indicating morbidity, while the 24 hLC50 was 83 m g/L for V. iris.These concentrations are similar to the current acuteand chronic criteria recommendationsfor copper in water of 100 mg/L CaCO 3 hard- ness, 13 and 9 m g/L, respectively (USEPA 1999a). Unionidsensitivity has been compared to otheraquatic species in side-by-side tests (Keller 1993; Masnado, Geis, and Sonzongi 1995). Masnado, Geis, and Sonzongi (1995) used different concentrations of metalsinaseries of synthetic effluents(e.g., chromium, copper, zinc, cadmium, andnickel) to determine thethreatamine effluentwould pose to downstream populationsof unionid mussels. Fatheadminnows(Pimephales promelas) and Ceriodaphiadubia were more sensitivetothe effluents than were U. imbecilis mussels. Keller (1993)exposed C. dubia and juvenile U. imbecilis mussels to an effluentcontaining6.4 mg/L chromium. The48-hLC50s were 61 m gCr/L for U. imbecilis and 36 m gCr/L for C. dubia.By96h,the mussel and zooplankton LC50seach had decreasedbyone-third. The current acutecriterion recommendation for chromium in water of 100 mg/L CaCO 3 hardness is 74 m gCr/L (USEPA 1999a). Unionid Mussel Sensitivity to Environmental Contaminants 153 4284X—CHAPTER 7—17/10/2006—13:03—JEBA—XML MODEL C–pp. 151–167 © 2007 by the Society of Environmental Toxicology and Chemistry (SETAC) TABLE 7.1 SummaryofSelected Metal and Inorganic Toxicity Data for Unionid Mussels Chemical or Physical LC50s Cu ( m g/L) Cd ( m g/L) Zn ( m g/L) Hg ( m g/L) Ni ( m g/L) Cr ( m g/L) K ( m g/L) F (mg/L) Ammonia at pH 8.0 (mg/L) Tempera- ture ( 8 C) pH (SU) Reference Species Glochidia Juvenile Adult Exposure (h) Hardness Test (Temp.) 13 a 2.0 b 120 a 1.4 a 470 a 570 a ——8.4 c NA 6.5–9.0 d Granmoand Varanka (1979) A. cygnea x——2010,000 C —————————— Keller and Zam (1991) U. imbecillis x486023171 57 355 216 240 295 ————— Keller and Zam (1991) U. imbecillis x966023869268 147 190 39 ————— Keller and Zam (1991) U. imbecillis x488023388 137 588 233 471 1187 ————— Keller and Zam (1991) U. imbecillis x968023199 107 438 171 252 618 ————— Huebner and Pynnonen (1992) A. cygnea x72— 13 66150 ———————— Hansten, Heino, and Pynnonen (1996) A. anatina x72— 450820 ———————— Imlay (1971) Unknown xmonths —— 25 —————4000– 7000 ———— McCann (1993) Medionidus conradicus x486020— —492 ———————— McCann (1993) A. pectorosa x485020— —274 ———————— McCann (1993) A. pectorosa x48160 20 ——664—739— ——————— McCann (1993) V. iris x4840–50 20 ——577—1155 ———————— McCann (1993) V. iris x48140–160 20 ——836—1230 ———————— McCann (1993) A. pectorosa x484020— —360—370— ——————— McCann (1993) A. pectorosa x48160 20 ——1060—1186 ———————— McCann (1993) V. iris x485020— —339 ———————— McCann (1993) V. iris x48160 20 ——1122 ———————— McCann (1993) A. pectorosa x4840–50 20 52–63 —————————— McCann (1993) A. pectorosa x48140–160 20 76–156 —————————— Freshwater BivalveEcotoxicology154 4284X—CHAPTER 7—17/10/2006—13:03—JEBA—XML MODEL C–pp. 151–167 © 2007 by the Society of Environmental Toxicology and Chemistry (SETAC) Dimock and Wright (1993) Pyganodon cataracta x96— 20 ————————3345 Dimock and Wright (1993) U. imbecillis x—————————————— Jacobson (1990) Vnebulosa x48160 20 56 —————————— Jacobson (1990) A. pectorosa x48170 20 51 —————————— Jacobson (1990) Anodanta grandis x24170 10 347 —————————— Jacobson (1990) A. grandis x24502046— ————————— Jacobson (1990) Lampsillis fasciola x48170 20 40 —————————— Jacobson (1990) M. conradicus x48170 20 16 —————————— Jacobson (1990) V. iris x24190 20 83 —————————— Jacobson (1990) A. grandis x24702044— ————————— Cherry,Farris, and Neves (1991) Ptychobranchus fasciolaris x48170 20 ——212 ———————— Cherry,Farris, and Neves (1991) A. pectorosa x48170 20 ——309 ———————— Cherry,Farris, and Neves (1991) M. conradicus x48170 20 ——570 ———————— Cherry,Farris, and Neves (1991) V. nebulosa x48170 20 ——656 ———————— Klaine, Warren, and Summers (1997) U. imbecillis x96100 25 67 —————————— Klaine, Warren, and Summers (1997) U. imbecillis x96100 25 —47————————— Augspurger et al. (2003) Various xxx24–96, 360 —12–25 ————————0.57–15.5 —— Keller and Augspurger (2005) Alasmidonta raveneliana x243025— ——————288 ——— Keller and Augspurger (2005) U. imbecillis x243425— ——————234 ——— Keller and Augspurger (2005) A. raveneliana x962825— ——————303 ——— Keller and Augspurger (2005) A. pectorosa x963025— ——————178 ——— (continued) Unionid Mussel Sensitivity to Environmental Contaminants 155 4284X—CHAPTER 7—17/10/2006—13:03—JEBA—XML MODEL C–pp. 151–167 © 2007 by the Society of Environmental Toxicology and Chemistry (SETAC) TABLE 7.1 (Continued) Chemical or Physical LC50s Cu ( m g/L) Cd ( m g/L) Zn ( m g/L) Hg ( m g/L) Ni ( m g/L) Cr ( m g/L) K ( m g/L) F (mg/L) Ammonia at pH 8.0 (mg/L) Tempera- ture ( 8 C) pH (SU) Reference Species Glochidia Juvenile Adult Exposure (h) Hardness Test (Temp.) 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) U. imbecillis x963425———————234 ——— Keller and Augspurger (2005) L. fasciola x963225———————172 ——— a USEPA 2002, acute criterion recommendation; listed in the dissolved fractionofthe metalconcentration. b USEPA 1999a, acute criterion recommendation; listed in the dissolved fractionofthe metal concentration. c USEPA 1999b, acute criterion recommendation. d USEPA 1976. Freshwater BivalveEcotoxicology156 4284X—CHAPTER 7—17/10/2006—13:03—JEBA—XML MODEL C–pp. 151–167 © 2007 by the Society of Environmental Toxicology and Chemistry (SETAC) Lasee(1991) conductedahistological andultrastructural study of Lampsilis ventricosa in which she examined the impact of cadmium on tissuesand organs. She ran toxicity tests as part of the studyand calculated 48-h LC50sof141 m gCd/L–345 m gCd/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 LC50sof9m gCd/L–107 m gCd/L at w 40 and 80 mg/L hardness, respectively. The current US criterion recommendation is 4.3 m gCd/L in water with 100mg/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 m gCu/L as “lethal” to mussels (speciesnot identified).Aset of 28-day flow-through copper toxicity tests was performed by Keller et al. (unpublished data) in 1996 using adultmussels in well water. The LC50s for U. imbecilisand Elliptio buckleyi were69and 4.5 m gCu/L, respectively,atahardness of 185 mg/L as CaCO 3 . S UBLETHAL T OXICITY OF M ETALS Exposures of mussels to low concentrations of ametal for along period of time (greater than seven days) permit the measurement of sublethal effects on processessuch 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, andSuresh 1991),amino acid contentoftissues (Gardner,Miller,and Imlay1981),metallothioneinproduction (Couillard, Campbell, and Tessier 1993; Malley et al. 1993), and others. Some of these responses may prove to be useful as indicatorsorbiomarkers of exposure to metals and may improvethe 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. Aseries of paperspublishedbyJenneretal. (1991) and Hemelraad, Holwerda, and Zandee (1986a,1986b, 1990a, 1990b) monitored tissue uptake and responses of A. anatina and A. cygnea to sublethal cadmiumexposure. They found that cadmium accumulated in soft tissueslinearly at low concentrations andinabiphasicmannerathigherconcentrations;thatgills accumulated the greatestamount of cadmium; that exposure to cadmium disturbed energy metabolism; and that ionic balance of the hemolymph and tissueswas disrupted. Reportsfrom anumber of other laboratories amplify these results. Oxygen consumption, ciliary activity, and heartbeat were significantly reduced in Lamellidens marginalis exposedtolethal and sublethal cadmium concentrations (6 and 2mg/L Cd) for one to ten days (Radhakrishnaiah 1988). These physiological impactsresulted from increased mucus production by the gills during cadmium exposure.Inalongerstudy by Naimo,Waller,and Holland-Bartels (1992a) respiration rates decreasedin L. ventricosa exposedtosublethal concentrations of cadmium for 28 days. However, ammoniaexcretion, mussel condition, and food assimilation efficiency were notfound to change significantly, perhaps aresult 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). ATPaseactivityand ciliary activity of gills in A. cygnea was decreased following exposure to cadmium(Pirovarova, Lagerspetz, and Skulskii 1992). Similarly, Raj and Hameed(1991) determinedthat sublethal concentrations of copper and mercuryaccelerated the respiratory rateof L. marginalis ,whilecadmium depressedit. In thislatterstudy,bodyweight decreasedfollowing 30-dayexposures to copper. Finally, the synthesis of porphyrins (part of cyto- chrome, enzyme, vitamin,and myoglobin molecules)was disrupted in Elliptiocomplanata and A. grandis mussels exposed to low concentrations of cadmium(Chamberland et al. 1995). Digestive activityand efficiency can also be impacted by cadmium toxicity. Both Hameedand Raj (1989) and Lasee (1991) found that exposure to copper,cadmium, or mercury resulted in the dissolution of the Unionid Mussel Sensitivity to Environmental Contaminants 157 4284X—CHAPTER 7—17/10/2006—13:03—JEBA—XML MODEL C–pp. 151–167 © 2007 by the Society of Environmental Toxicology and Chemistry (SETAC) crystalline style in Lamellidens marginalis and L. ventricosa,respectively. The style grinds ingested food before it is digested. Exposuretomercury causedthe fastest dissolution of the style of the three metals tested (Hameedand Raj 1989), and resulted in the slowest recovery. Metallothionein production was induced by exposure of several mussel species to cadmium, copper,zinc, andother metals (Couillard,Campbell, andTessier 1993;Malley et al. 1993; Couillard et al. 1995). These proteins serveasprotectors from metal toxicity and have been used as biomarkersofexposure to metals. Perhaps in attempting to relatecause and effect for declining mussel populations, biomarkerssuch as these wouldbeuseful. Thereported impacts of sublethal metal stress on mollusks strongly suggestthat while exposure to metals maynot be immediately apparent, lethality may result from eventual disruptionof metabolic activities,enzymefunctions, respiration, and other important processes. For the long- lived unionid mussels, repeated insults by metal pollution may be partially responsible for their continual decline. Anumber of mussel LC50sare 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 existatthe time. So, even though calculations include abuilt-in uncertainty factor designed to be protective (Stephan et al. 1985), the lack of unionid toxicity data in thosecalculations maymeanthatsomemetal criteria arenot adequately protective of freshwater mussels. ORGANIC CHEMICAL TOXICITY A CUTE T OXICITY OF O RGANIC C ONTAMINANTS The publishedliterature describing the impacts of acute exposure of mussels to various organic compounds is morelimited than for metals. Most of the available information describes responses to pesticides; thesecompounds are often found in aquatic systems as an indirect result of runoffor atmospheric deposition, although spills—both intentional and unintentional—also occur (Mulla and Mian 1981). Some documentshave reviewed the toxic effects of contaminants; an excellent compendium of toxicity data is includedinthe 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 detrimentallyaffect 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 lesssensitive to pesticides, herbicides, and other organic compounds than are the target organisms or other taxa. Toxicity tests usingglochidia have been reported for only afew organic compounds using permanent valveclosure or inability to respond to stimuli as the measureoflethality. In all of the tests exceptone, glochidiawere found to be very insensitive to tested chemicals, including atrazine, cyhalothrin, carbaryl, malathion, and several pesticides used in easternEurope (Varanka 1979; McLeese et al. 1980; Varanka 1987; Johnson, Keller, and Zam1993; Keller and Ruessler 1997) (Table 7.2).Incontrast, Conners and Black (2004) determined that U. imbecillis glochidia were as sensitive or more sensitive to glyphosate and carbaryl than otheraquatic invertebrates. Weinstein and Polk (2001) reportedthat photo-activated anthracene and pyrene were toxic to U. imbecillis glochidia at environmentally relevant concentrations.Anthracene was more toxic with a24-h LC50 of 1.93 m g/L followed by pyreneat2.63 m g/L. Varanka (1977) investigated the effect of several pesticidesontryptamine-induced activity of the adductormuscle of A. cygnea glochidia but found that mosteffects occurred at concentrations far exceedingenvironmental concentrations. However, malathioncaused decreased adductor activityataconcentration of 75 m g/L, which is arealistic 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 deathand genotoxicity. Freshwater BivalveEcotoxicology158 4284X—CHAPTER 7—17/10/2006—13:03—JEBA—XML MODEL C–pp. 151–167 © 2007 by the Society of Environmental Toxicology and Chemistry (SETAC) TABLE 7.2 SummaryofSelected Toxicity Data for Organic Compounds to Unionid Mussels Chemical LC50s Mala- thion ( m g/L) Pyrene (mg/L) Anthr- acene (mg/L) PCP ( m g/L) Toxa- phene ( m g/L) Chlor- dane ( m g/L) Aqua- thol ( m g/L) Hydr- othol ( m g/L) Bayth- roid (Mg/L) 2,4-D (Mg/L) Atra- zine ( m g/L) Cyha- lothrin (mg/L) Carbaryl (mg/L) Reference Species Glochi- dia Juvenile Adult Expos- ure(h) Test (Temp.) TFM a 0.1 b ——19 c 0.73 c 2.4 c ————1.5 d —— Johnson, Keller, and Zam (1993) U. imbecillis x4823 O 60 O 123.7 Waller et al. (1993) Obliquaria reflexa x48171.87 10,000 Chandler and Marking (1975) Elliptio sp./Plectomerus sp. x96—2–9 Keller (1993) U. imbecillis x4823610 740 880 4,850 Keller and Ruessler (1997) U. imbecillis x2425366 Villosa lienosa x242554 Lampsilis teres x242528 L. siliquoidea x24258–54 Megalonaias nervosa x425 22 U. imbecillis x9625215 Elliptio icterina x962532 Loxoconcha claibornensis x962524 L. subangulata x962528 V. lienosa x9625111 Viaa villosa x9625142 Wade, Hudson, and McKinney (1989) U. imbecillis x48244,600 4,600 Weinsteinand Polk (2001) U. imbecillis x24252.63 1.93 a TFM Z 3-trifluoromethyl-4-nitrophenol. b USEPA 2002,chroniccriterion recommendation. c USEPA 2002, acute criterion recommendation. d 2003,acute criterion recommendation. Unionid Mussel Sensitivity to Environmental Contaminants 159 4284X—CHAPTER 7—17/10/2006—13:03—JEBA—XML MODEL C–pp. 151–167 © 2007 by the Society of Environmental Toxicology and Chemistry (SETAC) 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)wereless toxic to U. imbecillis at 48 hthan 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 andMarking 1975), butneitherofthese mollusks was as sensitive as lamprey larvae or other aquatic taxa.Similar results werereported by Walleretal. (1993) and Waller, Bills, and Johnson(1997).Juvenile and adult E. complanata and Anodontacataracta and adult O. reflexa were not impacted by TFM at suggestedapplication 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 exposedtothe herbicide glyphosate (Sonar) at recommended dosagesinfield 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. S UBLETHAL E FFECTS OF O RGANIC C ONTAMINANTS Sublethal responses of adultmusselsfollowing exposure to pesticidesand other organics include decreased enzyme activity,abnormal shellgrowth, changesinmetabolism, heartrate, and siphoning activity, and others. Relativelyfewer studies have evaluated sublethal impacts of pesti- cides and other organic contaminants than have been reportedfor metals. Machado et al. (1990) reported abnormal shellgrowth 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, thougheven this response was elicited at a concentration much higherthan was effective in crustaceans, closer relativestoinsects. Analogous changes in other tissues have been reported for musselsexposedtovarious organic contaminants. Mane, Akarte, andKulkarni(1986) recorded biochemicalchanges in mussels exposedtofenthion, an organophosphate pesticide, including the altered distribution of protein, cholesterol, and particularlyglycogen and lipids, in the mantle tissue, gills,hepatopancreas, gonad, foot, and adductor muscles of Indonaia caeruleus.Ageneral 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 Oikari1992). Toxicity tests and assessmentsofacetylcholinesterase inhibition in E. complanata following exposure to aldicarb and acephate (Moulton,Fleming, and Purnell 1996)indicated that activitywas inhibited after pesticide exposure and was affected by test temperature but recovered after 12 days. Considerable variabilityinenzymeactivitywas reported in control animalsand may have masked the impact of the pesticidesonthe shellclosing response that is mediated by the activityofthe enzyme in the adductor muscle. However, the researchers recommendedfurther evaluationofthe assay as ameasure of fieldexposureofmusselsto 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 causedadecrease in heart rate, but these responses were elicitedonly at concentrations higherthan expected environmental concentrations (EEC). Similar inhibition was notedbySenthilmurugan et al. (1994) in the same species when exposedtophosphamidon at 0.015 m g/L, possibly leading to the disruption of metabolic processes and growth. Freshwater BivalveEcotoxicology160 4284X—CHAPTER 7—17/10/2006—13:03—JEBA—XML MODEL C–pp. 151–167 © 2007 by the Society of Environmental Toxicology and Chemistry (SETAC) [...]... 2002 EPA-822-R-0 2-0 47 U.S Environmental Protection Agency, Notice of Revised Draft Ambient Water Quality Criteria Document for Atrazine and Request for Scientific Reviews, November 2003 EPA-822-F-0 3-0 06 © 20 07 by the Society of Environmental Toxicology and Chemistry (SETAC) 4284X CHAPTER 7 17/ 10/2006—13:03—JEBA—XML MODEL C – pp 151–1 67 Unionid Mussel Sensitivity to Environmental Contaminants 1 67 Varanka,... site-specific copper criteria for the protection of mussel populations [abstract], SETAC, 12th annual meeting, Seattle, WA, pp 3 7, November 1991 Fleming, W J., Augspurger, T P., and Alderman, J A., Freshwater mussel die-off attributed to anticholinesterase poisoning, Environ Toxicol Chem., 14, 877 – 879 , 1995 © 20 07 by the Society of Environmental Toxicology and Chemistry (SETAC) 4284X CHAPTER 7 17/ 10/2006—13:03—JEBA—XML... of Water, Washington, DC, 1 976 , PB-263 U.S Environmental Protection Agency, National Water Quality Criteria Correction, Office of Water, Washington, DC, April 1999a EPA-822-Z-9 9-0 01 U.S Environmental Protection Agency, Update of Ambient Water Quality Criteria for Ammonia, Office of Water, Office of Science and Technology, Washington, DC, p 153, December, 1999b, EPA 822-R-9 9-0 14 U.S Environmental Protection... on three species of freshwater mussels from a metalpolluted watershed in Nova Scotia, Canada, Can J Zool., 70 , 1284–1291, 1992 Moulton, C A., Fleming, W J., and Purnell, C E., Effects of two cholinesterase-inhibiting pesticides on freshwater mussels, Environ Toxicol Chem., 15, 131–1 37, 1996 © 20 07 by the Society of Environmental Toxicology and Chemistry (SETAC) 4284X CHAPTER 7 17/ 10/2006—13:03—JEBA—XML... muscle of fresh-water mussel larvae, Acta Biol Acad Sci Hung., 28, 3 17 332, 1 977 Varanka, I., Effect of some pesticides on rhythmic adductor muscle activity of fresh-water mussel larvae, In Human Impacts on Life in Fresh Waters, Salanki, J and Biro, P., Eds., Symp Biol Hung., Akademiai Kiado, Budapest, Hungary, pp 177 –196, 1 979 Varanka, I., Effect of mosquito killer insecticides on freshwater mussels,... of the freshwater mussel, Parreysia rugosa (G), J Environ Biol., 6, 67 70 , 1985 Richard, P E., Dietz, T H., and Silverman, H., Structure of the gill during reproduction in the unionids Anodonta grandis, Ligumia subrostrata, and Caranculina parva texasensis, Can J Zool., 69, 174 4– 175 4, 1991 Schweinforth, R L and Wade, D C., Effects from subchronic 90-day exposure of in vitro-transformed juvenile freshwater. .. Chandler, J H and Marking, L L., Toxicity of the lampricide 3-trifluoromethyl-4-nitrophenol (TFM) t selected aquatic invertebrates and frog larvae, Invest Fish Contr., 62, 1 7, 1 975 Chandler, J H and Marking, L L., Toxicity of fishery chemicals to the Asiatic clam, Corbicula manilensis Progr Fish-Cult., 41, 148–151, 1 979 Cherry, D S and Farris, J L., Site-Specific Copper Criteria for the Protection of Aquatic... mussels displayed altered lengths of resting and active siphoning (Varanka 19 87) to the extent that inadequate nutrition and slower growth might result when exposed to the mosquito insecticides (Fyfanon–malathion, K-Othrin, Unitox 7 7% dichlorvos-and Unitox 20–20% dichlorvos) These results were generated at exposure levels three-to-five orders of magnitude lower than the acute LC50, and the author maintains... tissues could also limit the abilities of populations to survive in the face of other stressors such as habitat alteration © 20 07 by the Society of Environmental Toxicology and Chemistry (SETAC) 4284X CHAPTER 7 17/ 10/2006—13:03—JEBA—XML MODEL C – pp 151–1 67 162 Freshwater Bivalve Ecotoxicology OTHER POLLUTANTS Even though concentrations and loads of contaminants emanating from wastewater treatment... kinetics in freshwater clams (Unionidae) under field and laboratory conditions, Sci Tot Environ., 108, 205–214, 1991 Johnson, W W and Finley, M T., Handbook of Acute Toxicity of Chemicals to Fish and Aquatic Invertebrates, Resource Publication 1 37, p 98, 1980 © 20 07 by the Society of Environmental Toxicology and Chemistry (SETAC) 4284X CHAPTER 7 17/ 10/2006—13:03—JEBA—XML MODEL C – pp 151–1 67 Unionid Mussel . Scientific Reviews, November 2003. EPA-822-F-0 3-0 06. Freshwater BivalveEcotoxicology166 4284X CHAPTER 7 17/ 10/2006—13:03—JEBA—XML MODEL C–pp. 151–1 67 © 20 07 by the Society of Environmental Toxicology. Fish and Aquatic Invert- ebrates,Resource Publication 1 37, p. 98, 1980. Freshwater BivalveEcotoxicology164 4284X CHAPTER 7 17/ 10/2006—13:03—JEBA—XML MODEL C–pp. 151–1 67 © 20 07 by the Society of. LC50s Mala- thion ( m g/L) Pyrene (mg/L) Anthr- acene (mg/L) PCP ( m g/L) Toxa- phene ( m g/L) Chlor- dane ( m g/L) Aqua- thol ( m g/L) Hydr- othol ( m g/L) Bayth- roid (Mg/L) 2,4-D (Mg/L) Atra- zine (