Avoidance behavior of cold-, cool-, and warmwater fish exposed to Zequanox in a two-choice preference chamber
Zebra (Dreissenia polymorpha, Pallas 1771) and quagga (D. bugensis, Andrusov 1897) mussels, collectively referred to as dreissenid mussels, are invasive bivalves native to the Ponto-Caspian region of Eurasia (Stepien et al. 2013; Benson 2018a). High fecundity and a free-swimming planktonic life stage allow for easy and rapid dispersal of dreissenid mussels (Mackie 1991; Marsden et al. 2013). Dreissenids were introduced into the Great Lakes in North America in the mid-1980s via ballast water discharge from oceanic ships (Carlton 2008; Benson 2018b) and they quickly spread to inland waterways aided by anthropogenic mechanisms (Ludyanskiy et al., 1993; Birnbaum 2011). Zebra mussels were found within all of the Laurentian Great Lakes within three years of introduction and within the waterways of 29 U.S. states by 2010 (Benson 2013; Benson 2018a).
The impacts of dreissenid mussel biofouling on industrial and recreational water users has cost billions of dollars for remediation (Pimentel et al. 2005; Lovell et al. 2006). Dreissenids also caused substantial ecosystem harm including transferring energy from the pelagic to the benthic zone (Higgins and Vander Zanden 2010; Mayer et al. 2013), increasing nuisance algal blooms (Bierman et al. 2005; Higgins et al. 2008), altering fish communities (Strayer et al. 2004; Hoyle et al. 2008), and decimating native freshwater mussels (Karatayev et al. 2015; Lucy et al. 2013).
One treatment tool for controlling dreissenid mussels in open water environments is an Environmental Protection Agency (EPA) registered product, Zequanox (Marrone 2017). Zequanox is a formulated biopesticide that contains killed-cells of a soil bacterium, Pseudomonas fluorescensstrain CL145A, as the active ingredient (Luoma and Severson 2016; Marrone 2017). Zequanox has demonstrated safety to many non-target species, including freshwater fish, mussels, and invertebrates (Luoma et al. 2015; Waller and Luoma 2016; Waller et al. 2016). However, a recent study reported latent impacts on the survival and growth of lake trout (Salvelinus namaycush,Walbaum in Artedi 1792) after exposure to the maximum dose allowed by the product label (Luoma et al. In Press).
Characterization of avoidance behaviors in fish exposed to Zequanox is a prudent step in assessing the risk associated with Zequanox applications as exposure-related impacts have the potential be reduced when escapement from treated water is possible. Two-choice preference chambers allow for unimpeded movement of aquatic animals between two interconnected water flumes and they have been used to characterize avoidance behaviors in various aquatic animals (Jutfelt and Hedgärde 2013; Jutfelt et al. 2016; Tix et al. 2017). The goal of this study is to evaluate the potential for reduced risk to non-target animals during Zequanox applications by determining if freshwater fish preferentially avoid Zequanox. The specific objective is to evaluate the avoidance response of two representative species of cold-, cool-, and warmwater fish that are exposed to the maximum label concentration of Zequanox within a two-choice preference chamber.
Objective:
Evaluate the avoidance response of two representative species of cold-, cool-, and warmwater fish that are exposed to maximum label concentration of Zequanox within a two-choice preference chamber.
References:
Benson, A. J. (2013). Chronological history of zebra and quagga mussels (Dreissenidae) in North America, 1988–2010. Quagga and zebra mussels: biology, impacts, and control, 9-31.
Benson, A.J., Raikow, D., Larson, J., Fusaro, A. , and Bogdanoff, A.K. (2018a) Dreissena polymorpha (Pallas, 1771): U.S. Geological Survey, Nonindigenous Aquatic Species Database, Gainesville, FL, https://nas.er.usgs.gov/queries/FactSheet.aspx?speciesID=5, Revision Date: 2/13/2018, Date of access: 3/19/2018
Benson, A.J., Richerson, M.M., Maynard, E., Larson, J., Fusaro, A., Bogdanoff, A.K., and Neilson, M.E., (2018b), Dreissena rostriformis bugensis (Andrusov, 1897): U.S. Geological Survey, Nonindigenous Aquatic Species Database, Gainesville, FL, https://nas.er.usgs.gov/queries/FactSheet.aspx?SpeciesID=95, Revision Date: 6/5/2017, Access Date: 3/19/2018
Bierman, V.J., Kaur, J., DePinto, J.V., Feist, T.J., Dilks, D.W. (2005). Modeling the role of zebra mussels in the proliferation of blue-green algae in Saginaw Bay, Lake Huron. Journal of Great Lakes Research, 31, 32–55.
Birnbaum, Christina (2011). NOBANIS—Invasive alien species fact sheet—Dreissena polymorpha. From: Online Database of the European Network on Invasive Alien Species – NOBANIS www.nobanis.org, at https://www.nobanis.org/globalassets/speciesinfo/d/dreissena-polymorpha/dreissena_polymorpha.pdf, Date of access Date March 20, 2018.
Carlton, J. T. (2008). The zebra mussel Dreissena polymorpha found in North America in 1986 and 1987. Journal of Great Lakes Research, 34(4), 770-773.
Higgins, S. N., Malkin, S. Y., Todd Howell, E., Guildford, S. J., Campbell, L., Hiriart‐Baer, V., & Hecky, R. E. (2008). An ecological review of Cladophora glomerata (Chlorophyta) in the Laurentian Great Lakes. Journal of Phycology, 44(4), 839-854.
Higgins, S.N. and Vander Zanden, M. (2010). What a difference a species makes: a meta-analysis of dreissenid mussel impacts on freshwater ecosystems. Ecological monographs, 80(2), pp.179-196.
Hoyle, J. A., Bowlby, J. N., & Morrison, B. J. (2008). Lake whitefish and walleye population responses to dreissenid mussel invasion in eastern Lake Ontario. Aquatic Ecosystem Health & Management, 11(4), 403-411.
Jutfelt, F., & Hedgärde, M. (2013). Atlantic cod actively avoid CO 2 and predator odour, even after long-term CO 2 exposure. Frontiers in zoology, 10(1), 81.
Jutfelt, F., Sundin, J., Raby, G. D., Krång, A. S., & Clark, T. D. (2016). Two‐current choice flumes for testing avoidance and preference in aquatic animals. Methods in Ecology and Evolution, 8(3), 379-390.
Karatayev, A. Y., Burlakova, L. E., & Padilla, D. K. (2015). Zebra versus quagga mussels: a review of their spread, population dynamics, and ecosystem impacts. Hydrobiologia, 746(1), 97-112.
Lovell, S. J., Stone, S. F., & Fernandez, L. (2006). The economic impacts of aquatic invasive species: a review of the literature. Agricultural and Resource Economics Review, 35(1), 195-208.
Lucy, F. E., Burlakova, L. E., Karatayev, A. Y., Mastitsky, S. E., & Zanatta, D. T. (2013). Zebra mussel impacts on unionids: a synthesis of trends in North America and Europe. Quagga and Zebra Mussels: Biology, Impacts, and Control, 2nd ed. CRC Press, Boca Raton, 623-646.
Ludyanskiy, M. L., McDonald, D., & MacNeill, D. (1993). Impact of the zebra mussel, a bivalve invader. BioScience, 43(8), 533-544.
Luoma, J. A., & Severson, T. J. (2016). Efficacy of Spray-Dried Pseudomonas fluorescens, Strain CL145A (Zequanox®), for Controlling Zebra Mussels (Dreissena polymorpha) within Lake Minnetonka, MN Enclosures. US Geological Survey, La Crosse, WI.
Luoma, J.A., Severson, T.J., Wise, J.K., & Barbour, M.T. (In-Press). Exposure-related effects of Zequanox on juvenile lake sturgeon (Acipenser fulvescens) and lake trout (Salvelinus namaycush). Management of Biological Invasions.
Luoma, J. A., Weber, K. L., Waller, D. L., Wise, J. K., Mayer, D. A., & Aloisi, D. B. (2015). Safety of spray-dried powder formulated Pseudomonas fluorescens strain CL145A exposure to subadult/adult unionid mussels during simulated open-water treatments. US Geological Survey Open-File Report, 1064, 248.
Mackie, G. L. (1991). Biology of the exotic zebra mussel, Dreissena polymorpha, in relation to native bivalves and its potential impact in Lake St. Clair. In Environmental assessment and habitat evaluation of the upper Great Lakes connecting channels (pp. 251-268). Springer, Dordrecht.
Marrone Bio Innovations (2017) Product label. MBI-401SDP. EPA
Reg. No. 84059–15. http://marronebioinnovations.com/wp-content/ uploads/delightful-downloads/2016/12/ZEQUANOX_84059-15_Label_ Container_Insert0914ZQ.pdf (accessed March 26, 2018)
Marsden, J. E., Stangel, P., & Shambaugh, A. D. (2013). Influence of Environmental Factors on Zebra Mussel Population Expansion in Lake Champlain, 1994–2010. Quagga and Zebra Mussels: Biology, Impacts, and Control, 2nd ed. CRC Press, Boca Raton, 33-53.
Mayer, C.M, Burlakova, L.E., Peter E., Fitzgerald, D., Karatayev, A., Ludsin, S.A., Millard, S., Mills, E.L., Ostapenya, A.P., Rudstam, L.G., Zhu, B., & Zhukova, T.V.. (2013). The benthification of freshwater lakes: exotic mussels turning ecosystems upside down. Quagga and Zebra Mussels: Biology, Impacts, and Control. 2nd ed. CRC Press, Boca Raton, 575-585.
Pimentel, D., Zuniga, R., & Morrison, D. (2005). Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecological economics, 52(3), 273-288.
Piper R.G., Mc Elwain I.B., Orrne L.E., McCraren J.P., Fowler L.G., Leonard J.R. (1982). Fish Hatchery Management. Washington, D.C., U.S. Department of the Interior, U.S. Fish & Wildlife Service, 517 pp
Strayer, D. L., Hattala, K. A., & Kahnle, A. W. (2004). Effects of an invasive bivalve (Dreissena polymorpha) on fish in the Hudson River estuary. Canadian Journal of Fisheries and Aquatic Sciences, 61(6), 924-941.
Stepien, C. A., Grigorovich, I. A., Gray, M. A., Sullivan, T. J., Yerga-Woolwine, S., & Kalayci, G. (2013). Evolutionary, biogeographic, and population genetic relationships of dreissenid mussels, with revision of component taxa. Quagga and zebra mussels: biology, impacts, and control, 2nd edn. CRC Press, Boca Raton, 403-444.
SAS (2010) Version 9.3: Cary, N.C., SAS Institute Inc.
Waller, D. L., & Luoma, J. A. (2016). Effects of Spray-Dried Pseudomonas fluorescens, Strain CL145A (Zequanox®) on Reproduction and Early Development of the Fathead Minnow (Pimephales promelas). Legislative-Citizen Commission on Minnesota Resources (LCCMR).
Waller, D. L., Luoma, J. A., & Erickson, R. (2016). Safety of the molluscicide Zequanox® to nontarget macroinvertebrates Gammarus lacustris (Amphipoda: Gammaridae) and Hexagenia spp. (Ephemeroptera: Ephemeridae). Management of Biological Invasions, 7(3), 269-280.
Zebra (Dreissenia polymorpha, Pallas 1771) and quagga (D. bugensis, Andrusov 1897) mussels, collectively referred to as dreissenid mussels, are invasive bivalves native to the Ponto-Caspian region of Eurasia (Stepien et al. 2013; Benson 2018a). High fecundity and a free-swimming planktonic life stage allow for easy and rapid dispersal of dreissenid mussels (Mackie 1991; Marsden et al. 2013). Dreissenids were introduced into the Great Lakes in North America in the mid-1980s via ballast water discharge from oceanic ships (Carlton 2008; Benson 2018b) and they quickly spread to inland waterways aided by anthropogenic mechanisms (Ludyanskiy et al., 1993; Birnbaum 2011). Zebra mussels were found within all of the Laurentian Great Lakes within three years of introduction and within the waterways of 29 U.S. states by 2010 (Benson 2013; Benson 2018a).
The impacts of dreissenid mussel biofouling on industrial and recreational water users has cost billions of dollars for remediation (Pimentel et al. 2005; Lovell et al. 2006). Dreissenids also caused substantial ecosystem harm including transferring energy from the pelagic to the benthic zone (Higgins and Vander Zanden 2010; Mayer et al. 2013), increasing nuisance algal blooms (Bierman et al. 2005; Higgins et al. 2008), altering fish communities (Strayer et al. 2004; Hoyle et al. 2008), and decimating native freshwater mussels (Karatayev et al. 2015; Lucy et al. 2013).
One treatment tool for controlling dreissenid mussels in open water environments is an Environmental Protection Agency (EPA) registered product, Zequanox (Marrone 2017). Zequanox is a formulated biopesticide that contains killed-cells of a soil bacterium, Pseudomonas fluorescensstrain CL145A, as the active ingredient (Luoma and Severson 2016; Marrone 2017). Zequanox has demonstrated safety to many non-target species, including freshwater fish, mussels, and invertebrates (Luoma et al. 2015; Waller and Luoma 2016; Waller et al. 2016). However, a recent study reported latent impacts on the survival and growth of lake trout (Salvelinus namaycush,Walbaum in Artedi 1792) after exposure to the maximum dose allowed by the product label (Luoma et al. In Press).
Characterization of avoidance behaviors in fish exposed to Zequanox is a prudent step in assessing the risk associated with Zequanox applications as exposure-related impacts have the potential be reduced when escapement from treated water is possible. Two-choice preference chambers allow for unimpeded movement of aquatic animals between two interconnected water flumes and they have been used to characterize avoidance behaviors in various aquatic animals (Jutfelt and Hedgärde 2013; Jutfelt et al. 2016; Tix et al. 2017). The goal of this study is to evaluate the potential for reduced risk to non-target animals during Zequanox applications by determining if freshwater fish preferentially avoid Zequanox. The specific objective is to evaluate the avoidance response of two representative species of cold-, cool-, and warmwater fish that are exposed to the maximum label concentration of Zequanox within a two-choice preference chamber.
Objective:
Evaluate the avoidance response of two representative species of cold-, cool-, and warmwater fish that are exposed to maximum label concentration of Zequanox within a two-choice preference chamber.
References:
Benson, A. J. (2013). Chronological history of zebra and quagga mussels (Dreissenidae) in North America, 1988–2010. Quagga and zebra mussels: biology, impacts, and control, 9-31.
Benson, A.J., Raikow, D., Larson, J., Fusaro, A. , and Bogdanoff, A.K. (2018a) Dreissena polymorpha (Pallas, 1771): U.S. Geological Survey, Nonindigenous Aquatic Species Database, Gainesville, FL, https://nas.er.usgs.gov/queries/FactSheet.aspx?speciesID=5, Revision Date: 2/13/2018, Date of access: 3/19/2018
Benson, A.J., Richerson, M.M., Maynard, E., Larson, J., Fusaro, A., Bogdanoff, A.K., and Neilson, M.E., (2018b), Dreissena rostriformis bugensis (Andrusov, 1897): U.S. Geological Survey, Nonindigenous Aquatic Species Database, Gainesville, FL, https://nas.er.usgs.gov/queries/FactSheet.aspx?SpeciesID=95, Revision Date: 6/5/2017, Access Date: 3/19/2018
Bierman, V.J., Kaur, J., DePinto, J.V., Feist, T.J., Dilks, D.W. (2005). Modeling the role of zebra mussels in the proliferation of blue-green algae in Saginaw Bay, Lake Huron. Journal of Great Lakes Research, 31, 32–55.
Birnbaum, Christina (2011). NOBANIS—Invasive alien species fact sheet—Dreissena polymorpha. From: Online Database of the European Network on Invasive Alien Species – NOBANIS www.nobanis.org, at https://www.nobanis.org/globalassets/speciesinfo/d/dreissena-polymorpha/dreissena_polymorpha.pdf, Date of access Date March 20, 2018.
Carlton, J. T. (2008). The zebra mussel Dreissena polymorpha found in North America in 1986 and 1987. Journal of Great Lakes Research, 34(4), 770-773.
Higgins, S. N., Malkin, S. Y., Todd Howell, E., Guildford, S. J., Campbell, L., Hiriart‐Baer, V., & Hecky, R. E. (2008). An ecological review of Cladophora glomerata (Chlorophyta) in the Laurentian Great Lakes. Journal of Phycology, 44(4), 839-854.
Higgins, S.N. and Vander Zanden, M. (2010). What a difference a species makes: a meta-analysis of dreissenid mussel impacts on freshwater ecosystems. Ecological monographs, 80(2), pp.179-196.
Hoyle, J. A., Bowlby, J. N., & Morrison, B. J. (2008). Lake whitefish and walleye population responses to dreissenid mussel invasion in eastern Lake Ontario. Aquatic Ecosystem Health & Management, 11(4), 403-411.
Jutfelt, F., & Hedgärde, M. (2013). Atlantic cod actively avoid CO 2 and predator odour, even after long-term CO 2 exposure. Frontiers in zoology, 10(1), 81.
Jutfelt, F., Sundin, J., Raby, G. D., Krång, A. S., & Clark, T. D. (2016). Two‐current choice flumes for testing avoidance and preference in aquatic animals. Methods in Ecology and Evolution, 8(3), 379-390.
Karatayev, A. Y., Burlakova, L. E., & Padilla, D. K. (2015). Zebra versus quagga mussels: a review of their spread, population dynamics, and ecosystem impacts. Hydrobiologia, 746(1), 97-112.
Lovell, S. J., Stone, S. F., & Fernandez, L. (2006). The economic impacts of aquatic invasive species: a review of the literature. Agricultural and Resource Economics Review, 35(1), 195-208.
Lucy, F. E., Burlakova, L. E., Karatayev, A. Y., Mastitsky, S. E., & Zanatta, D. T. (2013). Zebra mussel impacts on unionids: a synthesis of trends in North America and Europe. Quagga and Zebra Mussels: Biology, Impacts, and Control, 2nd ed. CRC Press, Boca Raton, 623-646.
Ludyanskiy, M. L., McDonald, D., & MacNeill, D. (1993). Impact of the zebra mussel, a bivalve invader. BioScience, 43(8), 533-544.
Luoma, J. A., & Severson, T. J. (2016). Efficacy of Spray-Dried Pseudomonas fluorescens, Strain CL145A (Zequanox®), for Controlling Zebra Mussels (Dreissena polymorpha) within Lake Minnetonka, MN Enclosures. US Geological Survey, La Crosse, WI.
Luoma, J.A., Severson, T.J., Wise, J.K., & Barbour, M.T. (In-Press). Exposure-related effects of Zequanox on juvenile lake sturgeon (Acipenser fulvescens) and lake trout (Salvelinus namaycush). Management of Biological Invasions.
Luoma, J. A., Weber, K. L., Waller, D. L., Wise, J. K., Mayer, D. A., & Aloisi, D. B. (2015). Safety of spray-dried powder formulated Pseudomonas fluorescens strain CL145A exposure to subadult/adult unionid mussels during simulated open-water treatments. US Geological Survey Open-File Report, 1064, 248.
Mackie, G. L. (1991). Biology of the exotic zebra mussel, Dreissena polymorpha, in relation to native bivalves and its potential impact in Lake St. Clair. In Environmental assessment and habitat evaluation of the upper Great Lakes connecting channels (pp. 251-268). Springer, Dordrecht.
Marrone Bio Innovations (2017) Product label. MBI-401SDP. EPA
Reg. No. 84059–15. http://marronebioinnovations.com/wp-content/ uploads/delightful-downloads/2016/12/ZEQUANOX_84059-15_Label_ Container_Insert0914ZQ.pdf (accessed March 26, 2018)
Marsden, J. E., Stangel, P., & Shambaugh, A. D. (2013). Influence of Environmental Factors on Zebra Mussel Population Expansion in Lake Champlain, 1994–2010. Quagga and Zebra Mussels: Biology, Impacts, and Control, 2nd ed. CRC Press, Boca Raton, 33-53.
Mayer, C.M, Burlakova, L.E., Peter E., Fitzgerald, D., Karatayev, A., Ludsin, S.A., Millard, S., Mills, E.L., Ostapenya, A.P., Rudstam, L.G., Zhu, B., & Zhukova, T.V.. (2013). The benthification of freshwater lakes: exotic mussels turning ecosystems upside down. Quagga and Zebra Mussels: Biology, Impacts, and Control. 2nd ed. CRC Press, Boca Raton, 575-585.
Pimentel, D., Zuniga, R., & Morrison, D. (2005). Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecological economics, 52(3), 273-288.
Piper R.G., Mc Elwain I.B., Orrne L.E., McCraren J.P., Fowler L.G., Leonard J.R. (1982). Fish Hatchery Management. Washington, D.C., U.S. Department of the Interior, U.S. Fish & Wildlife Service, 517 pp
Strayer, D. L., Hattala, K. A., & Kahnle, A. W. (2004). Effects of an invasive bivalve (Dreissena polymorpha) on fish in the Hudson River estuary. Canadian Journal of Fisheries and Aquatic Sciences, 61(6), 924-941.
Stepien, C. A., Grigorovich, I. A., Gray, M. A., Sullivan, T. J., Yerga-Woolwine, S., & Kalayci, G. (2013). Evolutionary, biogeographic, and population genetic relationships of dreissenid mussels, with revision of component taxa. Quagga and zebra mussels: biology, impacts, and control, 2nd edn. CRC Press, Boca Raton, 403-444.
SAS (2010) Version 9.3: Cary, N.C., SAS Institute Inc.
Waller, D. L., & Luoma, J. A. (2016). Effects of Spray-Dried Pseudomonas fluorescens, Strain CL145A (Zequanox®) on Reproduction and Early Development of the Fathead Minnow (Pimephales promelas). Legislative-Citizen Commission on Minnesota Resources (LCCMR).
Waller, D. L., Luoma, J. A., & Erickson, R. (2016). Safety of the molluscicide Zequanox® to nontarget macroinvertebrates Gammarus lacustris (Amphipoda: Gammaridae) and Hexagenia spp. (Ephemeroptera: Ephemeridae). Management of Biological Invasions, 7(3), 269-280.