Environmental Toxicology and Chemistry, Vol. 34, No. 3, pp. 626–639, 2015 # 2014 SETAC Printed in the USA
TOXICITY OF SEDIMENTS FROM LEAD–ZINC MINING AREAS TO JUVENILE FRESHWATER MUSSELS (LAMPSILIS SILIQUOIDEA) COMPARED TO STANDARD TEST ORGANISMS JOHN M. BESSER,*y CHRISTOPHER G. INGERSOLL,y WILLIAM G. BRUMBAUGH,y NILE E. KEMBLE,y THOMAS W. MAY,y NING WANG,y DONALD D. MACDONALD,z and ANDREW D. ROBERTSx yUnited States Geological Survey, Columbia, Missouri zMacDonald Environmental Sciences, Nanaimo, British Columbia, Canada xUnited States Fish and Wildlife Service, Columbia, Missouri
(Submitted 12 September 2014; Returned for Revision 3 December 2014; Accepted 7 December 2014) Abstract: Sediment toxicity tests compared chronic effects on survival, growth, and biomass of juvenile freshwater mussels (28-d exposures with Lampsilis siliquoidea) to the responses of standard test organisms—amphipods (28-d exposures with Hyalella azteca) and midges (10-d exposures with Chironomus dilutus)—in sediments from 2 lead–zinc mining areas: the Tri-State Mining District and Southeast Missouri Mining District. Mussel tests were conducted in sediments sieved to 1800 km2), located in southwest Missouri, southeast Kansas, and northeast Oklahoma (Supplemental Data, Figure S1). More than 100 yr of intensive mining ended in 1967 in Tri-State and in 1972 in southeast Missouri [9], leaving large deposits of metal-contaminated mine wastes that remain All Supplemental Data may be found in the online version of this article. * Address correspondence to [email protected] Published online 26 December 2014 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/etc.2849 626
Toxicity of lead–zinc mining sediments to freshwater mussels
Zn mining areas on freshwater mussel populations, it is difficult to establish cause and effect relationships based on population data alone. A common complicating factor is the co-occurrence of metal contamination with alterations to physical habitats that may also adversely affect freshwater mussels. Although recent mussel surveys in both the Big River and Spring River drainages did not find strong associations between habitat quality and observed impacts on mussel populations [13,14], there remains a need to determine the toxicity of metal-contaminated sediments of mining-impacted streams to freshwater mussels. Metal contamination and toxicity of sediments have been the primary focus of recent investigations in the Tri-State and southeast Missouri mining areas [10,11,15–18], most of which have been conducted under the federal Superfund and Natural Resource Damage Assessment and Restoration programs. These investigations have the common goals of assessing, remediating, and restoring ecological impacts of historic mining activities. These studies have relied primarily on wholesediment toxicity tests with standard test organisms, including 28-d exposures with the amphipod, Hyalella azteca, and 10-d exposures with the midge, Chironomus dilutus [19,20]. However, there has been little data to demonstrate that tests with these species adequately reflect toxicity risks to freshwater mussels. Until recently, the reliability of data from laboratory toxicity tests with freshwater mussels was uncertain. The complex life history of mussels necessitates specialized methods for laboratory culture [21,22] and toxicity testing [23]. The development of a standard guide for conducting water-only toxicity tests with larval and juvenile stages of freshwater mussels [24] has led to tests that have documented the high sensitivity of early life stages of mussels to several contaminants in water, including ammonia and some metals [5–7,25]. The results of these studies indicate that tests with laboratorycultured juvenile mussels may adequately represent the sensitivity of threatened and endangered mussel species. A recent study adapted water-only test methods to successfully conduct laboratory sediment toxicity tests with 2 species of juvenile mussels in sediments from streams affected by coal mining in Virginia and Tennessee [26]. The objectives of the present study were: 1) to demonstrate the feasibility of conducting chronic, whole-sediment toxicity tests with the juvenile life stage of the fatmucket mussel, L. siliquoidea; 2) to compare the sensitivity of L. siliquoidea and standard test organisms (H. azteca and C. dilutus) to metalcontaminated sediments from the Tri-State and southeast Missouri study areas; and 3) to compare the responses of mussels in laboratory toxicity tests to the results of recent field surveys of mussel communities in both study areas.
METHODS
Study areas and site selection
The Tri-State study area included parts of Missouri, Kansas, and Oklahoma in the Spring River and Neosho River watersheds (Supplemental Data, Figure S1) in Cherokee County, KS; Jasper County, MO; Newton County, MO; and Ottawa County, OK. Seventy primary sites in the Tri-State area were sampled in 2007 (Supplemental Data, Table S1) based on preliminary sediment chemistry data collected for 241 sites in 2006 [15]. These sites were selected to represent sediments across 8 geographic areas and across a wide range of metal contamination [16]. Sediments from these sites were collected during July 2007 (group 1) and
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August 2007 (group 2), processed 1 wk after collection, and tested 2 wk after collection. Six additional Tri-State sediments sampled in August 2006 and tested in November 2006 using similar methods were also included in this analysis (group 3; Supplemental Data, Table S1). The southeast Missouri study area consisted of portions of the Meramec River watershed in St. Francois, Washington, Jefferson, and Franklin Counties, MO (Supplemental Data, Figure S1). Sediments from 21 southeast Missouri sites were collected in September 2008 [17]. Seventeen of these sites were located on the Big River, which drains the primary mining area in St. Francois County. Additional sites were located on Mineral Fork, a tributary of the Big River that drains a smaller mining area in Washington County; the Meramec River, upstream and downstream of the mouth of Big River; and the Bourbeuse River, a tributary to the Meramec River that has no known mining in its watershed. Many of these sites were located close to mussel beds that were sampled in a concurrent 2008 mussel population study [13]. Candidate reference sites were selected to characterize biological responses in uncontaminated sediments from each study area. Sediments from reference sites were expected to have low metal concentrations and to have physical and chemical characteristics (e.g., particle size distribution, organic carbon content) similar to sediments from nonreference sites (subsequently referred to as “test sites”) in each study area. Eleven of the Tri-State sites sampled in 2006 and 2007 were designated as reference sites (6 sites in group 1; 3 in group 2; and 2 in group 3). Most of the Tri-State reference sites were located in the upper Spring River, which had no mining activity, and the remaining reference sites were located in upstream reaches of streams with mining activity, including Center Creek, Shoal Creek, and Neosho River [18]. Four sites in the southeast Missouri study area were selected as candidate reference sites, including 1 site in the Big River upstream of mining (Site 1), 2 sites in the Meramec River (Sites 19 and 20), and 1 site in the Bourbeuse River (Site 21). The suitability of candidate reference sites was verified based on chemical criteria to ensure that the toxic effects of metals did not adversely affect the performance of test organisms in reference samples. Chemical criteria for reference sites were based on measured sediment metal concentrations in sediment and porewater expressed as metal hazard indexes (described below in Metal hazard indices). Sediment collection and sample processing
About 20 liters of bulk sediment (wet sieved to
TOXICITY OF SEDIMENTS FROM LEAD–ZINC MINING AREAS TO JUVENILE FRESHWATER MUSSELS (LAMPSILIS SILIQUOIDEA) COMPARED TO STANDARD TEST ORGANISMS JOHN M. BESSER,*y CHRISTOPHER G. INGERSOLL,y WILLIAM G. BRUMBAUGH,y NILE E. KEMBLE,y THOMAS W. MAY,y NING WANG,y DONALD D. MACDONALD,z and ANDREW D. ROBERTSx yUnited States Geological Survey, Columbia, Missouri zMacDonald Environmental Sciences, Nanaimo, British Columbia, Canada xUnited States Fish and Wildlife Service, Columbia, Missouri
(Submitted 12 September 2014; Returned for Revision 3 December 2014; Accepted 7 December 2014) Abstract: Sediment toxicity tests compared chronic effects on survival, growth, and biomass of juvenile freshwater mussels (28-d exposures with Lampsilis siliquoidea) to the responses of standard test organisms—amphipods (28-d exposures with Hyalella azteca) and midges (10-d exposures with Chironomus dilutus)—in sediments from 2 lead–zinc mining areas: the Tri-State Mining District and Southeast Missouri Mining District. Mussel tests were conducted in sediments sieved to 1800 km2), located in southwest Missouri, southeast Kansas, and northeast Oklahoma (Supplemental Data, Figure S1). More than 100 yr of intensive mining ended in 1967 in Tri-State and in 1972 in southeast Missouri [9], leaving large deposits of metal-contaminated mine wastes that remain All Supplemental Data may be found in the online version of this article. * Address correspondence to [email protected] Published online 26 December 2014 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/etc.2849 626
Toxicity of lead–zinc mining sediments to freshwater mussels
Zn mining areas on freshwater mussel populations, it is difficult to establish cause and effect relationships based on population data alone. A common complicating factor is the co-occurrence of metal contamination with alterations to physical habitats that may also adversely affect freshwater mussels. Although recent mussel surveys in both the Big River and Spring River drainages did not find strong associations between habitat quality and observed impacts on mussel populations [13,14], there remains a need to determine the toxicity of metal-contaminated sediments of mining-impacted streams to freshwater mussels. Metal contamination and toxicity of sediments have been the primary focus of recent investigations in the Tri-State and southeast Missouri mining areas [10,11,15–18], most of which have been conducted under the federal Superfund and Natural Resource Damage Assessment and Restoration programs. These investigations have the common goals of assessing, remediating, and restoring ecological impacts of historic mining activities. These studies have relied primarily on wholesediment toxicity tests with standard test organisms, including 28-d exposures with the amphipod, Hyalella azteca, and 10-d exposures with the midge, Chironomus dilutus [19,20]. However, there has been little data to demonstrate that tests with these species adequately reflect toxicity risks to freshwater mussels. Until recently, the reliability of data from laboratory toxicity tests with freshwater mussels was uncertain. The complex life history of mussels necessitates specialized methods for laboratory culture [21,22] and toxicity testing [23]. The development of a standard guide for conducting water-only toxicity tests with larval and juvenile stages of freshwater mussels [24] has led to tests that have documented the high sensitivity of early life stages of mussels to several contaminants in water, including ammonia and some metals [5–7,25]. The results of these studies indicate that tests with laboratorycultured juvenile mussels may adequately represent the sensitivity of threatened and endangered mussel species. A recent study adapted water-only test methods to successfully conduct laboratory sediment toxicity tests with 2 species of juvenile mussels in sediments from streams affected by coal mining in Virginia and Tennessee [26]. The objectives of the present study were: 1) to demonstrate the feasibility of conducting chronic, whole-sediment toxicity tests with the juvenile life stage of the fatmucket mussel, L. siliquoidea; 2) to compare the sensitivity of L. siliquoidea and standard test organisms (H. azteca and C. dilutus) to metalcontaminated sediments from the Tri-State and southeast Missouri study areas; and 3) to compare the responses of mussels in laboratory toxicity tests to the results of recent field surveys of mussel communities in both study areas.
METHODS
Study areas and site selection
The Tri-State study area included parts of Missouri, Kansas, and Oklahoma in the Spring River and Neosho River watersheds (Supplemental Data, Figure S1) in Cherokee County, KS; Jasper County, MO; Newton County, MO; and Ottawa County, OK. Seventy primary sites in the Tri-State area were sampled in 2007 (Supplemental Data, Table S1) based on preliminary sediment chemistry data collected for 241 sites in 2006 [15]. These sites were selected to represent sediments across 8 geographic areas and across a wide range of metal contamination [16]. Sediments from these sites were collected during July 2007 (group 1) and
Environ Toxicol Chem 34, 2015
627
August 2007 (group 2), processed 1 wk after collection, and tested 2 wk after collection. Six additional Tri-State sediments sampled in August 2006 and tested in November 2006 using similar methods were also included in this analysis (group 3; Supplemental Data, Table S1). The southeast Missouri study area consisted of portions of the Meramec River watershed in St. Francois, Washington, Jefferson, and Franklin Counties, MO (Supplemental Data, Figure S1). Sediments from 21 southeast Missouri sites were collected in September 2008 [17]. Seventeen of these sites were located on the Big River, which drains the primary mining area in St. Francois County. Additional sites were located on Mineral Fork, a tributary of the Big River that drains a smaller mining area in Washington County; the Meramec River, upstream and downstream of the mouth of Big River; and the Bourbeuse River, a tributary to the Meramec River that has no known mining in its watershed. Many of these sites were located close to mussel beds that were sampled in a concurrent 2008 mussel population study [13]. Candidate reference sites were selected to characterize biological responses in uncontaminated sediments from each study area. Sediments from reference sites were expected to have low metal concentrations and to have physical and chemical characteristics (e.g., particle size distribution, organic carbon content) similar to sediments from nonreference sites (subsequently referred to as “test sites”) in each study area. Eleven of the Tri-State sites sampled in 2006 and 2007 were designated as reference sites (6 sites in group 1; 3 in group 2; and 2 in group 3). Most of the Tri-State reference sites were located in the upper Spring River, which had no mining activity, and the remaining reference sites were located in upstream reaches of streams with mining activity, including Center Creek, Shoal Creek, and Neosho River [18]. Four sites in the southeast Missouri study area were selected as candidate reference sites, including 1 site in the Big River upstream of mining (Site 1), 2 sites in the Meramec River (Sites 19 and 20), and 1 site in the Bourbeuse River (Site 21). The suitability of candidate reference sites was verified based on chemical criteria to ensure that the toxic effects of metals did not adversely affect the performance of test organisms in reference samples. Chemical criteria for reference sites were based on measured sediment metal concentrations in sediment and porewater expressed as metal hazard indexes (described below in Metal hazard indices). Sediment collection and sample processing
About 20 liters of bulk sediment (wet sieved to
