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Determining the Appropraite Duration of Toxicity Tests with Glochidia of Native Freshwater Mussels

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Determining the Appropraite Duration of Toxicity Tests with Glochidia of Native Freshwater Mussels Determining the Appropriate Duration of Toxicity Tests with Glochidia of Native Freshwater Mussels Final Completion Report for the period August 1, 2010 – July 31, 2012 Submitted to Edward Hammer U.S. Environmental Protection Agency 77 West Jackson Blvd. Chicago, IL 60604-3590 by Robert B. Bringolf, Ph.D. The University of Georgia Warnell School of Forestry & Natural Resources 180 East Green St., Athens, GA 30602-2152 Telephone: 706-542-1477 E-mail: [email protected] M. Christopher Barnhart, Ph.D. Biology Department Missouri State University 901 South National Ave. Springfield, MO 65897 Telephone: 417-836-5166 Email: [email protected] and W. Gregory Cope, Ph.D. North Carolina State University Department of Environmental & Molecular Toxicology Box 7633, Raleigh, NC 27695-7633 Telephone: 919-515-5296 E-mail: [email protected] Submitted May 8, 2013 1 Executive Summary The overall goal of this project was to provide information for determining the appropriate duration of toxicity tests with the larval stage (glochidia) of freshwater mussels belonging to the family Unionidae. The project was developed to provide insight into the ecological relevance of using the glochidia closing response to salt as an endpoint for toxicity tests and as a measure of condition in determining the appropriate duration of standardized toxicity tests with glochidia. Specific objectives were to determine: 1) if the duration of glochidia viability, defined as the ability to close in response to salt (NaCl) solution, is equivalent to the duration of infectivity- the ability to attach to a host fish and metamorphose successfully into the juvenile stage; 2) if the duration of infectivity of glochidia deposited in natural stream sediment is similar to the duration observed in water-only exposures; and 3) the probability that glochidia deposited onto the sediment surface will infect host fish, using representative mussel-host species pairs. During the first phase of the project, we tested glochidia viability and infectivity of six mussel species that differ in their host-infection strategies. Three of these species use mantle lures and host extraction (Lampsilis siliquoidea, Lampsilis cardium, Villosa lienosa), two species broadcast glochidia into the water column (Utterbackia imbecillis and Amblema plicata), and one species releases glochidia in conglutinates (Ptychobranchus occidentalis). Our results indicate that within the first 24 h after release from the female mussel, glochidia viability was indicative of infectivity, as long as viability was >90%. After 24 h, viability remained relatively high (>60%) in many species tested, but infectivity of glochidia free in water sometimes declined rapidly after 24 h. Infectivity was high at all times when viability was >90%. The current American Society for Testing and Materials (ASTM) guideline for conducting toxicity tests with 2 glochidia of freshwater mussels requires >90% viability for control groups at test termination (commonly 24 h). Our results indicated that viability is an adequate proxy for infectivity of glochidia free in water when viability is >90%, and that infectivity decreased markedly in some species when viability dropped below 90%. Our results also indicated that glochidia released in conglutinates remained viable and infective for longer periods than glochidia released free into the water. We also noted for species that brood for several months (long term brooders), glochidia collected from females toward the end of the brooding season were viable for a shorter duration than those collected earlier in the brooding season. Based on these data, we recommend that the current ASTM guideline for conducting toxicity tests with glochidia be retained with a maximum test duration of 24 h for all mussel species. Additionally, we recommend that glochidia from long term brooders be collected before the end of the brooding season. For species with previously defined duration of viability of ≥ 24 h, we recommend a 24 h toxicity test; however, for species with little or no data on duration of viability, we recommend that viability be assessed at an intermediate time point(s) (e.g., 6, 12, 18, 24 h) during toxicity tests in the event that control viability is <90% by 24 h (e.g. at test termination). In the second phase of the project, we compared the duration of glochidia viability and infectivity 1) in natural water and sediment versus reconstituted water, and 2) in free glochidia versus glochidia within conglutinates. These experiments were performed with Ptychobranchus occidentalis glochidia and rainbow darters (Etheostoma caeruleum). Infectivity of free glochidia of Ptychobranchus declined to near zero within 24 h, more rapidly than the other species tested. Viability declined more rapidly in natural water and sediment than in reconstituted water, perhaps because of microorganisms that attack the glochidia. In contrast to free glochidia, glochidia in conglutinates remained viable and infective for the duration of the study (96 h). The 3 apparent protective effects of the conglutinate suggest that 24-h toxicity test duration with intact conglutinates would be conservative. In a third phase of the project, we evaluated infectivity for glochidia that had been exposed to NaCl or copper (Cu) for 24 hr. We used glochidia of two mussel species, Lampsilis cardium and Lampsilis dolabraeformis, and largemouth bass for this study. Two experiments were performed with glochidia of L. cardium, one with glochidia collected early in the brooding season (January) and a second with glochidia collected near the end of the brooding season (June) to determine if maternal brooding time influenced sensitivity to the toxicant, viability, or infectivity. Following the 24-h exposure to a range of concentrations of NaCl or Cu, we observed predictable results that viability decreased with increasing toxicant concentration. The remaining viable glochidia in each treatment were placed on largemouth bass to determine if they were also able to attach and metamorphose on the fish. In each of the 5 trials, we observed that the viable glochidia were indeed able to metamorphose at a rate similar to those in the control. These results suggest that the glochidia viability endpoint is a proxy for metamorphosis success and is therefore ecologically relevant for 24 h toxicity tests. The data also demonstrated that glochidia collected early in the brooding season were significantly less sensitive to the toxicant, had higher metamorphosis success, and remained viable (>90%) longer than those collected late in the brooding season. These results have important implications for timing of glochidia collection for toxicity test with long-term brooding mussel species (e.g., members of the tribe Lampsilini). In summary, the results of this study provided data that support retaining the current ASTM guideline for toxicity testing with glochidia using viability as the endpoint, but with recommended maximum test duration of 24 h. We recommend that glochidia be collected before 4 the end of the brooding season for toxicity tests to ensure health and viability of glochidia. We recommend that glochidia viability be assessed in toxicity tests at a time point between 0 and 24 h (e.g., 6, 12, 18 h) for species for which duration of viability has not been defined in the event that viability of control mussels of a given species decreases to <90% by the 24 h time point. Formatted for submission to: Environmental Toxicology and Chemistry 5 Determining the appropriate duration of toxicity tests with glochidia of native freshwater mussels Andrea K. Fritts1, M. Christopher Barnhart2, Megan Bradley2, Na Liu2, W. Gregory Cope3, and Robert B. Bringolf1,4 1 University of Georgia, Warnell School of Forestry & Natural Resources, Athens, Georgia 30602 2 Missouri State University, Department of Biology, Springfield, Missouri 65897 3 North Carolina State University, Department of Environmental and Molecular Toxicology, Raleigh, North Carolina 27695 4 Corresponding author: [email protected] 6 Abstract Freshwater mussels (Unionidae) have a remarkable life cycle in which larvae (glochidia) are brooded by the female parent and then released into the water where they must attach to a fish host to metamorphose into a juvenile mussel. Glochidia attach by closing the shell valves on the host. Glochidia also close in response to salt solution, and this closing response to salt is widely used as a measure of viability to determine if glochidia are suitable for host fish suitability trials, as an endpoint for standard toxicity tests, and for a variety of other applications. The lifespan of glochidia in water is limited. We tested the assumption that glochidia viability, measured by the closing response to salt, is indicative of infectivity, the ability of glochidia to attach to a host fish and successfully metamorphose to the juvenile stage. We compared the durations of glochidia viability and infectivity in water for seven mussel species (Lampsilis siliquoidea, Lampsilis cardium, Lampsilis dolabraeformis, Villosa lienosa, Ptychobranchus occidentalis, Amblema plicata, and Utterbackia imbecillis). Viability was indicative of infectivity between 0 and 24 hours. However, often infectivity of glochidia in water decreased after 24 h even when viability remained relatively high, especially for glochidia collected near the end of the brooding season. The duration of viability and infectivity for glochidia of P. occidentalis was shorter in river water with sediment compared to
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