Teresa J. Newton

Differential exposure, duration, and sensitivity of unionoidean bivalve life stages to environmental contaminants

Abstract Freshwater mussels (superfamily Unionoidea) are in serious global decline and in urgent need of protection and conservation. The declines have been attributed to a wide array of human activities resulting in pollution and water-quality degradation, and habitat destruction and alteration. Linkages among poor water quality, pollutant sources, and mussel decline in rivers and streams have been associated with results of laboratory-based tests of specific pollutants. However, uncertainties remain about the relationship of laboratory data to actual contaminant exposure routes for various mussel species, life stages, and in the habitats occupied during these exposures. We evaluated the pathways of exposure to environmental pollutants for all 4 life stages (free glochidia, encysted glochidia, juveniles, adults) of unionoidean mussels and found that each life stage has both common and unique characteristics that contribute to observed differences in exposure and sensitivity. Free glochidia typically are exposed only briefly (e.g., seconds to days) through surface water, whereas adults sustain exposure over years to decades through surface water, pore water, sediment, and diet. Juveniles live largely burrowed in the sediment for the first 0 to 4 y of life. Thus, sediment, pore water, and diet are the predominant exposure routes for this life stage, but surface water also might contribute to exposure during certain periods and environmental conditions. The obligate parasitic stage (encysted glochidia stage) on a host fish might be exposed from surface water while partially encysted or from toxicants in host-fish tissue while fully encysted. Laboratory methods for testing for acute and chronic exposures in water have advanced, and toxicant-specific information has increased in recent years. However, additional research is needed to understand interactions of life history, habitat, and long-term exposure to contaminants through water, pore water, sediment, and diet so that the risks of environmental exposures can be properly assessed and managed.

Environmental occurrence and reproductive effects of the pharmaceutical fluoxetine in native freshwater mussels

The present study measured the occurrence, distribution, and bioaccumulation of fluoxetine in samples of water, polar organic chemical integrative sampler (POCIS), sediment, and caged freshwater mussels at stream sites near a municipal wastewater treatment facility effluent discharge. We assessed the relation of the environmental concentrations to reproductive endpoints in mussels in acute laboratory tests. Concentrations of fluoxetine in water and POCIS samples were similar (<20% difference) within each site and were greatest in the effluent channel (104-119 ng/L), and decreased at 50 m and 100 m downstream. Likewise, concentrations of fluoxetine in sediment and mussel (Elliptio complanata) tissue were greatest in the effluent channel (17.4 ng/g wet wt for sediment and 79.1 ng/g wet wt for mussels). In 96-h lab tests, fluoxetine significantly induced parturition of nonviable larvae from female E. complanata exposed to 300 microg/L (p = 0.0118) and 3,000 microg/L (p < 0.0001) compared to controls. Fluoxetine exposure at 300 microg/L (p = 0.0075) and 3,000 microg/L (p = 0.0001) also resulted in stimulation of lure display behavior in female Lampsilis fasciola and Lampsilis cardium, respectively. In male E. complanata, 3,000 microg fluoxetine/L significantly induced release of spermatozeugmata during a 48-h exposure. These results suggest that fluoxetine accumulates in mussel tissue and has the potential to disrupt several aspects of reproduction in freshwater mussels, a faunal group recognized as one of the most imperiled in the world. Despite the disparity between measured environmental concentrations of fluoxetine and effects concentrations in our short-term tests with these long-lived animals, additional tests are warranted to evaluate the effects of long-term exposure to environmentally relevant concentrations and critical lifestages (e.g., juveniles).

Effects of substrate and hydrodynamic conditions on the formation of mussel beds in a large river

Abstract A numerical model for simulation of freshwater mussel dynamics was used to investigate the effects of substrate and hydrodynamic conditions on the formation of mussel beds in a 10-km reach of the Upper Mississippi River (UMR). Suitable habitats for mussel survival were identified by creating a dimensionless parameter (shear stress ratio) combining shear force and substrate type. This parameter is a measure of substrate stability that could be used in many different applications. Dispersal of juvenile mussels with flow as they detach from their fish hosts was simulated by a particle-tracking mechanism that identified suitable areas for colonization with the potential to evolve into mussel beds. Simulated areas of mussel accumulation coincided with reported locations of mussel beds, and simulated densities were in the range of abundant mussel beds in other reaches of the UMR. These results, although more qualitative than quantitative, provide insight into factors influencing the formation of mussel beds in a large river.

Using landscape ecology to understand and manage freshwater mussel populations

Abstract Mussel populations and the environments they inhabit are heterogeneous and fragmented. We review 3 areas in which principles of landscape ecology might be applied to the scientific understanding and management of freshwater mussels. First, recent studies show that hydraulics can be used successfully to delineate patches of mussel habitat, but additional variables such as host fish, food, or predators are probably important under certain conditions. However, research on patch dynamics in freshwater mussels is in its infancy, and we do not know if existing methods to delineate patches are adequate. Second, mussel ecologists are starting to think about the importance of connectivity among habitat patches. Major challenges will be to determine whether connectivity can be estimated in the field and whether human activities that reduce connectivity (e.g., dams) have produced large extinction debts in mussel populations. Third, we need to better understand the links between events on the watershed (e.g., timing and amounts of water, nutrient, and sediment inputs) and the quality, extent, location, and connections among patches of mussel habitats. Because of its focus on patterns and processes, landscape ecology has the potential to improve scientific understanding and management of mussel populations and, in particular, to help define the best spatial scales for scientific studies and management activities.

EFFECTS OF AMMONIA ON JUVENILE UNIONID MUSSELS ( LAMPSILIS CARDIUM ) IN LABORATORY SEDIMENT TOXICITY TESTS

Ammonia is a relatively toxic compound generated in water and sediments by heterotrophic bacteria and accumulates in sediments and pore water. Recent data suggest that unionid mussels are sensitive to un-ionized ammonia (NH3) relative to other organisms. Existing sediment exposure systems are not suitable for ammonia toxicity studies with juvenile unionids; thus, we modified a system to expose juveniles to ammonia that was continuously infused into sediments. This system maintained consistent concentrations of ammonia in pore water up to 10 d. Juvenile Lampsilis cardium mussels were exposed to NH3 in pore water in replicate 96-h and 10-d sediment toxicity tests. The 96-h median lethal concentrations (LC50s) were 127 and 165 microg NH3-N/L, and the 10-d LC50s were 93 and 140 microg NH3-N/L. The median effective concentrations (EC50s) (based on the proportion affected, including dead and inactive mussels) were 73 and 119 microg NH3-N/L in the 96-h tests and 71 and 99 microg NH3-N/L in the 10-d tests. Growth rate was substantially reduced at concentrations between 31 and 76 microg NH3-N/L. The lethality results (when expressed as total ammonia) are about one-half the acute national water quality criteria for total ammonia, suggesting that existing criteria may not protect juvenile unionids.

Use of complex hydraulic variables to predict the distribution and density of unionids in a side channel of the Upper Mississippi River

Previous attempts to predict the importance of abiotic and biotic factors to unionids in large rivers have been largely unsuccessful. Many simple physical habitat descriptors (e.g., current velocity, substrate particle size, and water depth) have limited ability to predict unionid density. However, more recent studies have found that complex hydraulic variables (e.g., shear velocity, boundary shear stress, and Reynolds number) may be more useful predictors of unionid density. We performed a retrospective analysis with unionid density, current velocity, and substrate particle size data from 1987 to 1988 in a 6-km reach of the Upper Mississippi River near Prairie du Chien, Wisconsin. We used these data to model simple and complex hydraulic variables under low and high flow conditions. We then used classification and regression tree analysis to examine the relationships between hydraulic variables and unionid density. We found that boundary Reynolds number, Froude number, boundary shear stress, and grain size were the best predictors of density. Models with complex hydraulic variables were a substantial improvement over previously published discriminant models and correctly classified 65–88% of the observations for the total mussel fauna and six species. These data suggest that unionid beds may be constrained by threshold limits at both ends of the flow regime. Under low flow, mussels may require a minimum hydraulic variable (Re*, Fr) to transport nutrients, oxygen, and waste products. Under high flow, areas with relatively low boundary shear stress may provide a hydraulic refuge for mussels. Data on hydraulic preferences and identification of other conditions that constitute unionid habitat are needed to help restore and enhance habitats for unionids in rivers.

Lethal and sublethal effects of ammonia to juvenile Lampsilis mussels (unionidae) in sediment and water‐only exposures

We compared the sensitivity of two juvenile unionid mussels (Lampsilis cardium and Lampsilis higginsii) to ammonia in 96-h water-only and sediment tests by use of mortality and growth measurements. Twenty mussels were placed in chambers buried 2.5 cm into reference sediments to approximate pore-water exposure (sediment tests) or elevated above the bottom of the experimental units (water-only tests). In the sediment tests, a pH gradient existed between the overlying water (mean 8.0), sediment- water interface (mean 7.7), and 2.5 cm depth (mean 7.4). We assumed that mussels were exposed to ammonia in pore water and report effect concentrations in pore water, but if they were exposed to the higher pH water, more of the ammonia would be in the toxic un-ionized (NH(3)) form. The only differences in toxicity and growth between mussel species occurred in some of the water-only tests. In sediment tests, median lethal concentrations (LC50s) ranged from 124 to 125 microg NH(3)-N/L. In water-only tests, LC50s ranged from 157 to 372 microg NH(3)-N/L. In sediment tests, median effective concentrations (EC50s based on growth) ranged from 30 to 32 microg NH(3)-N/L. Juvenile mussels in the water-only tests grew poorly and did not exhibit a dose-response relation. These data demonstrate that growth is a sensitive and valuable endpoint for studies on ammonia toxicity with juvenile freshwater mussels and that growth should be measured via sediment tests.

Evaluation of relocation of unionid mussels into artificial ponds

Relocation of unionid mussels into refuges (e.g., hatchery ponds) has been suggested as a management tool to protect these animals from the threat of zebra mussel (Dreissena polymorpha) invasion. To evaluate the efficacy of relocation, we experimentally relocated 768 mussels, representing 5 species (Leptodea fragilis, Obliquaria reflexa, Fusconaia flava, Amblema plicata, and Quadrula quadrula) into an earthen pond at a National Fish Hatchery or back into the river. In both locations, mussels were placed into 1 of 4 treatments (mesh bags, corrals, and buried or suspended substrate-filled trays). Mussels were examined annually for survival, growth (shell length and wet mass), and physiological condition (glycogen concentration in foot and mantle and tissue condition index) for 36 mo in the pond or 40 mo in the river. We observed significant differences in mortality rates between locations (mortality was 4 times greater in the pond than in the river), among treatments (lowest mortality in the suspended trays), and among species (lower mortality in the amblemines than lampsilines). Overall survival in both locations averaged 80% the 1st year; survival in the pond decreased dramatically after that. Although length and weight varied between locations and over time, these changes were small, suggesting that their utility as short-term measures of well being in long-lived unionids is questionable. Mussels relocated to the pond were in poor physiological condition relative to those in the river, but the magnitude of these differences was small compared to the inherent variability in physiological condition of reference mussels. These data suggest that relocation of unionids into artificial ponds is a high-risk conservation strategy; alternatives such as introduction of infected host fish, identification of mussel beds at greatest risk from zebra mussels, and a critical, large-scale assessment of the factors contributing to their decline should be explored.

Intra‐ and interlaboratory variability in acute toxicity tests with glochidia and juveniles of freshwater mussels (unionidae)

The present study evaluated the performance and variability in acute toxicity tests with glochidia and newly transformed juvenile mussels using the standard methods outlined in American Society for Testing and Materials (ASTM). Multiple 48-h toxicity tests with glochidia and 96-h tests with juvenile mussels were conducted within a single laboratory and among five laboratories. All tests met the test acceptability requirements (e.g., >or=90% control survival). Intralaboratory tests were conducted over two consecutive mussel-spawning seasons with mucket (Actinonaias ligamentina) or fatmucket (Lampsilis siliquoidea) using copper, ammonia, or chlorine as a toxicant. For the glochidia of both species, the variability of intralaboratory median effective concentrations (EC50s) for the three toxicants, expressed as the coefficient of variation (CV), ranged from 14 to 27% in 24-h exposures and from 13 to 36% in 48-h exposures. The intralaboratory CV of copper EC50s for juvenile fatmucket was 24% in 48-h exposures and 13% in 96-h exposures. Interlaboratory tests were conducted with fatmucket glochidia and juveniles by five laboratories using copper as a toxicant. The interlaboratory CV of copper EC50s for glochidia was 13% in 24-h exposures and 24% in 48-h exposures, and the interlaboratory CV for juveniles was 22% in 48-h exposures and 42% in 96-h exposures. The high completion success and the overall low variability in test results indicate that the test methods have acceptable precision and can be performed routinely.

Long-term monitoring of growth in the Eastern Elliptio, Elliptio complanata (Bivalvia: Unionidae), in Rhode Island: a transplant experiment

Abstract The lengths of marked specimens of the freshwater mussel, Eastern Elliptio (Elliptio complanata [Lightfoot 1786]), were monitored annually in 3 lakes in Rhode Island, USA, from 1991 to 2005. Mussels growing in Worden Pond showed a change in mean shell length of only 4.3 mm over 14 y, whereas mussel growth in 2 nearby lakes was 3 to 8× greater than growth in Worden Pond over the same time period. L∞, the length at which shell growth stops, was significantly different (p < 0.001) among lakes and ranged from 60.5 to 87.4 mm. Transplant experiments revealed that mussels moved to Worden Pond stopped growing, whereas mussels moved from Worden Pond to the 2 other lakes grew at rates similar to the rates observed for resident mussels in the 2 lakes. Standard water-quality measures did not explain the observed growth cessation and lower condition indices of mussels in Worden Pond. Our growth data are consistent with food limitation. The consistent slow growth of E. complanata in Worden Pond, without high mortality, and its ability to increase growth when placed in environments more favorable than Worden Pond, suggests both growth plasticity and longevity in these animals.