Variation in Response of Laboratory-Cultured Freshwater Macroinvertebrates to Sediment from Streams with Differential Exposure to Agriculture

Abstract

Agricultural land use is widely accepted to elicit changes on surrounding environment and neighboring ecosystems. Meanwhile, the impact of different types of agricultural land use likely cause a variety of impacts on nearby ecosystems and the organisms that inhabit them. Freshwater systems support a wide range of organisms—from infaunal or epifaunal invertebrates to mobile pelagic and littoral fish species. The focus of this study was to determine how agricultural activity in the upstream catchment influences sediment properties and the resulting ability of three distinct invertebrate species to survive and reproduce in these different sediments. This will be the first study that evaluates the utility of the sediment quality triad when assessing the impact of agricultural activity on invertebrate growth, reproduction, and survival. In analyzing sediment and water chemistry, as well as metal and pesticide levels, none of the predictor variables were able to adequately explain the variation seen in any of the biological endpoints (reproduction, mortality, growth, or biomass). Although none of the factors measured in this experiment could explain the variation seen in biological endpoints, the experimental approach was informative in delineating biological trends between sediments subject to varying levels of agricultural activity. Although an experiment of this nature was not able to identify a causal mechanism to explain the variation in invertebrate biological endpoint, it is still extremely useful as an exploratory approach to assess relative sediment toxicity.

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References

  1. Allan, J. D. (2004). Influence of land use and landscape setting on the ecological status of rivers. Limnetica, 23, 187–198. https://doi.org/10.1146/annurev.ecolsys.35.120202.110122.

    Article  Google Scholar 

  2. Allan, J. D., Erickson, D. L., & Fay, J. (1997). The influence of catchment land use on stream integrity across multiple spatial scales. Freshwater Biolology, 37, 149–161. https://doi.org/10.1046/j.1365-2427.1997.d01-546.x.

    Article  Google Scholar 

  3. Barbour, M. T., Gerritsen, J., Snyder, B. D., Stribling, J. B. (1999). USEPA rapid bioassessment protocols for use in streams and wadeable rivers: periphyton, benthic macroinvertebrates and fish, Second edition. EPA 841-B-99-002. U.S. Environmental Protection Agency; Office of Water; Washington, D.C.

  4. Beketov, M. (2004). Different sensitivity of mayflies (Insecta, Ephemeroptera) to ammonia, nitrite and nitrate: linkage between experimental and observational data. Hydrobiologia, 528, 209–216.

    CAS  Article  Google Scholar 

  5. Borgmann, U., Ralph, K. M., & Norwood, W. P. (1989). Toxicity test procedures for Hyalella azteca, and chronic toxicity of cadmium and pentachlorophenol to H-azteca, Gammarus-fasciatus, and Daphnia magna. Archives of Environmental Contamination and Toxicology, 18, 756–764. https://doi.org/10.1007/BF01225013.

    CAS  Article  Google Scholar 

  6. Burt, A. J., McKee, P. M., Hart, D. R., & Kauss, P. B. (1991). Effects of pollution on benthic invertebrate communities of the St. Marys River, 1985. Hydrobiologia, 219, 63–81. https://doi.org/10.1007/BF00024747.

    CAS  Article  Google Scholar 

  7. Carpenter, S. R., Cole, J. J., Pace, M. L., Van de Bogert, M., Bade, D. L., Bastviken, D., Gille, C. M., Hodgson, J. R., Kitchell, J. F., & Kritzberg, E. S. (2005). Ecosystems subsidies: terrestrial support of aquatic food webs from 13C addition to contrasting lakes. Ecology, 86, 2737–2750.

    Article  Google Scholar 

  8. Casellato, S. (1996). Oligochaetes in the southern basin of the Venetian Lagoon: community composition, species abundance and biomass. Hydrobiologia, 334, 103–114. https://doi.org/10.1007/BF00017359.

    Article  Google Scholar 

  9. CCME. (2001). CCME protocol for the derivation of Canadian sediment quality guidelines for the protection of aquatic life. Transport, 1–4.

  10. Chapman, P. M. (1990). The sediment quality triad approach to determining pollution-induced degradation. Science of the Total Environment, 97(98), 815–825. https://doi.org/10.1016/0048-9697(90)90277-2.

    Article  Google Scholar 

  11. Compin, A., & Céréghino, R. (2003). Sensitivity of aquatic insect species richness to disturbance in the Adour-Garonne stream system (France). Ecological Indicators, 3, 135–142.

    Article  Google Scholar 

  12. Cooper, C. M. (1993). Biological effects of agriculturally derived surface water pollutants on aquatic systems—a review. Journal of Environmental Quality, 22, 402. https://doi.org/10.2134/jeq1993.00472425002200030003x.

    CAS  Article  Google Scholar 

  13. Courtney, L. A., & Clements, W. H. (1998). Effects of acidic pH on benthic macroinvertebrate communities in stream microcosms. Hydrobiologia, 379(1–3), 135–145.

    Article  Google Scholar 

  14. Cuffney, T. F., Meador, M. R., Porter, S. D., & Gurtz, M. E. (2000). Responses of physical, chemical, and biological indicators of water quality to a gradient of agricultural land use in the Yakima river basin, Washington. Environmental Monitoring and Assessment, 64, 259–270. https://doi.org/10.1023/A:1006473106407.

    CAS  Article  Google Scholar 

  15. Egler, M., Buss, D., Moreira, J., & Baptista, D. (2012). Influence of agricultural land-use and pesticides on benthic macroinvertebrate assemblages in an agricultural river basin in Southeast Brazil. Brazilian Journal of Biology, 72, 437–443. https://doi.org/10.1590/S1519-69842012000300004.

    CAS  Article  Google Scholar 

  16. Fils Mamert, O., Serge Hubert, Z. T., Ernest, K., Nectaire Lie, N. T., & Simenon, T. (2016). Influence of municipal and industrial pollution on the diversity and the structure of benthic macro-invertebrates community of an urban stream in Douala, Cameroon. Journal of Biodiversity and Environmental Sciences, 8, 120–133.

    Google Scholar 

  17. Gan, J., Lee, S. J., Liu, W. P., Haver, D. L., & Kabashima, J. N. (2005). Distribution and persistence of pyrethroids in runoff sediments. Journal of Environmental Quality, 34, 836–841.

    CAS  Article  Google Scholar 

  18. Giller, P. S. (2005). River restoration: seeking ecological standards. Editor’s introduction. Journal of Applied Ecology, 42, 201–207. https://doi.org/10.1111/j.1365-2664.2005.01020.x.

    Article  Google Scholar 

  19. Gillis, P. L., Diener, L. C., Reynoldson, T. F., & Dixon, D. G. (2002). Cadmium-induced production of a metallothionein-like protein in Tubifex tubifex (Oligochaeta) and Chironomus riparius (Diptera): correlation with reproduction and growth. Environmental Toxicology and Chemistry, 21, 1836–1844.

    CAS  Article  Google Scholar 

  20. Glass, G. V., Peckham, P. D., & Sanders, J. R. (1972). Consequences of failure to meet assumptions underlying fixed effects analyses of variance and covariance. Review of Educational Research, 42, 237–288.

    Article  Google Scholar 

  21. Harwell, M. R., Rubinstein, E. N., Hayes, W. S., & Olds, C. C. (1992). Summarizing Monte Carlo results in methodological research: the one- and two-factor fixed effects ANOVA cases. Journal of Statistics Education, 17, 315–339.

    Article  Google Scholar 

  22. Herman, M. R., & Najadhashemi, A. P. (2015). A review of macroinvertebrates- and fish-based stream health indices. Ecohydrology and Hydrobiology, 15, 53–67.

    Article  Google Scholar 

  23. Herringshaw, C. J., Stewart, T. W., Thompson, J. R., & Anderson, P. F. (2011). Land use, stream habitat and benthic invertebrate assemblages in a highly altered Iowa watershed. The American Midland Naturalist, 165, 274–293. https://doi.org/10.1674/0003-0031-165.2.274.

    Article  Google Scholar 

  24. Hurlbert, S. H. (1984). Pseudoreplication and the design of ecological field experiments. Ecological Monographs, 54(2), 187–211.

  25. Hung, C., Gong, G., Chen, H., Hsieh, H., Santschi, P. H., Wade, T. L., & Sericano, J. S. (2007). Relationship between pesticide and organic carbon fractions in sediments of the Danshui River estruary and adjacent coastal areas of Taiwan. Environmental Pollution, 148, 546–554.

    CAS  Article  Google Scholar 

  26. Jaagumagi, R., & Persaud, D. (1993). Sediment assessment: a guide to study design, sampling, and laboratory analysis. Toronto: Queen’s Printer for Ontario.

    Google Scholar 

  27. Johnston, J. M., Barber, M. C., Wolfe, K., Galvin, M., Cyterski, M., & Parmar, R. (2017). An integrated ecological modeling system for assessing impacts of multiple stressors on stream and riverine ecosystem services within river basin. Ecological Modelling, 354, 104–114.

    CAS  Article  Google Scholar 

  28. Jones, C., Somers, K. M., Craig, B., & Reynoldson, T. B. (2007). Ontario Benthos Biomonitoring Network: protocol manual. Toronto: Queens Printer for Ontario.

    Google Scholar 

  29. Koop, J. H. E., Winkelmann, C., Becker, J., Hellmann, C., & Ortmann, C. (2011). Physiological indicators of fitness in benthic invertebrates; a useful measure for ecological health assessment and experimental biology. Aquatic Ecology, 45, 547–559.

    Article  Google Scholar 

  30. Lantz, B. (2013). The impact of sample non-normality on ANOVA and alternative methods. The British Journal of Mathematical and Statistical Psychology, 66(2), 224–244.

    Article  Google Scholar 

  31. Lenat, D. R., & Crawford, J. K. (1994). Effects of land use on water quality and aquatic biota of three North Carolina Piedmont streams. Hydrobiologia, 294, 185–199.

    Article  Google Scholar 

  32. Lix, L. M., Keselman, J. C., & Keselman, H. J. (1996). Consequences of assumption violations revisited: a quantitative review of alternatives to the one-way analysis of variance F test. Review of Educational Research, 66, 579–619.

    Google Scholar 

  33. López-Doval, J. C., Großschartner, M., Höss, S., Orendt, C., Traunspurger, W., Wolfram, G., & Muñoz, I. (2010). Invertebrate communities in soft sediments along a pollution gradient in a Mediterranean river (Llobregat, NE Spain). Limnetica, 29, 311–322. https://doi.org/10.1111/1467-9906.00002.

    Article  Google Scholar 

  34. MacDonald, D. D., Ingersoll, C. G., & Berger, T. A. (2000). Development and evaluation of consensus-based sediment quality guidelines for freshwater ecosystems. Archives of Environmental Contamination and Toxicology, 39, 20–31. https://doi.org/10.1007/s002440010075.

    CAS  Article  Google Scholar 

  35. Matlou, K., Addo-Bediako, A., & Jooste, A. (2017). Benthic macroinvertebrate assemblage along a pollution gradient in the Steelpoort River, Olifants River system. African Entomology, 25, 445–453. https://doi.org/10.4001/003.025.0445.

    Article  Google Scholar 

  36. Matthaei, C. D., Weller, F., Kelly, D. W., & Townsend, C. R. (2006). Impacts of fine sediment addition to tussock, pasture, dairy and deer farming streams in New Zealand. Freshwater Biology, 51, 2154–2172. https://doi.org/10.1111/j.1365-2427.2006.01643.x.

    Article  Google Scholar 

  37. McTammany, M. E., Benfield, E. F., & Webster, J. R. (2007). Recovery of stream ecosystem metabolism from historical agriculture. Journal of the North American Benthological Society, 26, 532–545. https://doi.org/10.1899/06-092.1.

    Article  Google Scholar 

  38. Meyer, J. L., Sale, M. J., Mulholland, P. J., & Poff, N. L. (1999). Impacts of climate change on aquatic ecosystem functioning and health. Journal of the American Water Resources Association, 35, 1373–1386. https://doi.org/10.1111/j.1752-1688.1999.tb04222.x.

    Article  Google Scholar 

  39. Milani, D., Reynoldson, T. B., Borgmann, U., & Kolasa, J. (2003). The relative sensitivity of four benthic invertebrates to metals in spiked-sediment exposures and application to contaminated field sediment. Environmental Toxicology and Chemistry, 22, 845–854. https://doi.org/10.1002/etc.5620220424.

    CAS  Article  Google Scholar 

  40. MOECC. (2012). Standard operating procedure: Hexagenia spp. culturing. SOP HX1.v5. Ontario Ministry of the Environment; Laboratory Services Branch; Aquatic Toxicology Unit; Toronto, Ontario, Canada.

  41. Moore, A. A., & Palmer, M. A. (2005). Invertebrate biodiversity in agricultural and urban headwater streams: implications for conservation and management. Ecological Applications, 15, 1169–1177. https://doi.org/10.1890/04-1484.

    Article  Google Scholar 

  42. Nakano, S., & Murakami, M. (2001). Reciprocal subsidies: dynamic interdependence between terrestrial and aquatic food webs. Proceedings of the National Academy of Sciences of the United States of America, 98, 166–170.

    CAS  Article  Google Scholar 

  43. Nilsson, C., & Berggren, K. (2000). Alterations of riparian ecosystems caused by river regulation. Bioscience, 50, 783–792. https://doi.org/10.1641/0006-3568(2000)050[0783:AORECB]2.0.CO;2.

    Article  Google Scholar 

  44. OMAFRA. 2016. Area of census farm (acres) by county, Ontario: 2016. http://www.omafra.gov.on.ca/english/stats/census/cty30a.htm

  45. Ometo, J. P. H. B., Martinelli, L. A., Ballester, M. V., Gessner, A., Krusche, A. V., Victoria, R. L., & Williams, M. (2000). Effects of land use on water chemistry and macroinvertebrates in two streams of the Piracicaba river basin, south-east Brazil. Freshwater Biology, 44, 327–337. https://doi.org/10.1046/j.1365-2427.2000.00557.x.

    CAS  Article  Google Scholar 

  46. OMNRF (Ontario Ministry of Natural Resources and Forestry). (2017). User guide for Ontario Flow Assessment Tool (OFAT). Provincial Mapping Unit, Mapping and Information Resources Branch.

  47. Pace, M. L., Cole, J. J., Carpenter, S. R., Kitchell, J. F., Hodgson, J. R., Van de Bogert, M. C., Bade, D. L., Kritzberg, E. S., & Bastviken, D. (2004). Whole-lake carbon-13 additions reveal terrestrial support of aquatic food webs. Nature, 427, 240–243.

    CAS  Article  Google Scholar 

  48. Pavlin, M., Birk, S., Hering, D., & Urbanič, G. (2011). The role of land use, nutrients, and other stressors in shaping benthic invertebrate assemblages in Slovenian rivers. Hydrobiologia, 678, 137–153. https://doi.org/10.1007/s10750-011-0836-8.

    CAS  Article  Google Scholar 

  49. Prosser, R. S., Bartlett, A. J., Milani, D., Holman, E. A. M., Ikert, H., Schissler, D., Toito, J., Parrott, J. L., Gillis, P. L., & Balakrishnan, V. K. (2017a). Variation in the toxicity of sediment-associated substituted phenylamine antioxidants to an epibenthic (Hyalella azteca) and endobenthic (Tubifex tubifex) invertebrate. Chemosphere, 181, 250–258. https://doi.org/10.1016/j.chemosphere.2017.04.066.

    CAS  Article  Google Scholar 

  50. Prosser, R. S., Parrott, J. L., Galicia, M., Shires, K., Sullivan, C., Toito, J., Bartlett, A. J., Milani, D., Gillis, P. L., & Balakrishnan, V. K. (2017b). Toxicity of sediment-associated substituted phenylamine antioxidants on the early life stages of Pimephales promelas and a characterization of effects on freshwater organisms. Environmental Toxicology and Chemistry, 36, 2730–2738.

    CAS  Article  Google Scholar 

  51. Reynoldson, T. B. (1994). A field test of a sediment bioassay with the oligochaete worm Tubifex tubifex (Müller, 1774). Hydrobiologia, 278, 223–230.

  52. Reynoldson, T. B., & Metcalfe-Smith, J. L. (1992). An overview of the assessment of aquatic ecosystem health using benthic invertebrates. Aquatic Ecosystem Health, 1, 295–308.

    Article  Google Scholar 

  53. Reynoldson, T. B., Thompson, S. P., & Bamsey, J. L. (1991). A sediment bioassay using the tubificid oligochaete worm Tubifex tubifex. Environmental Toxicology and Chemistry, 10, 1061–1072.

    CAS  Article  Google Scholar 

  54. Richards, C., Host, G. E., & Arthur, J. W. (1993). Identification of predominant environmental factors structuring stream macroinvertebrate communities within a large agricultural catchment. Freshwater Biology, 29, 285–294. https://doi.org/10.1111/j.1365-2427.1993.tb00764.x.

    Article  Google Scholar 

  55. Rubach, M. N., Ashauer, R., Buchwalter, D. B., De Lange, H. J., Hamer, M., Preuss, T. G., Töpke, K., & Maund, S. J. (2011). Framework for traits-based assessment in ecotoxicology. Integrated Environmental Assessment and Management, 7, 172–186. https://doi.org/10.1002/ieam.105.

    Article  Google Scholar 

  56. Scott, M. C., & Helfman, G. S. (2001). Native invasions, homogenization, and the mismeasure of integrity of fish assemblages. Fisheries, 26, 6–15. https://doi.org/10.1577/1548-8446(2001)026<0006:NIHATM>2.0.CO;2.

    Article  Google Scholar 

  57. Smith, S. L., MacDonald, D. D., Keenleyside, K. A., Ingersoll, C. G., & Field, L. J. (1996). A preliminary evaluation of sediment quality assessment values for freshwater ecosystems. Journal of Great Lakes Research, 22, 624–638. https://doi.org/10.1016/S0380-1330(96)70985-1.

    CAS  Article  Google Scholar 

  58. Søndergaard, M., & Jeppesen, E. (2007). Anthropogenic impacts on lake and stream ecosystems, and approaches to restoration. Journal of Applied Ecology, 44, 1089–1094. https://doi.org/10.1111/j.1365-2664.2007.01426.x.

    Article  Google Scholar 

  59. Stepenuck, K. F., Crunkilton, R. L., & Wang, Z. (2002). Impacts of urban landuse on macroinvertebrate communities in southeastern Wisconsin streams. Journal of American Water Resources Association, 38, 1041–1051.

    Article  Google Scholar 

  60. Storey, R. G., & Cowley, D. R. (1997). Recovery of three New Zealand rural streams as they pass through native forest remnants. Hydrobiologia, 353, 63–76. https://doi.org/10.1023/A:1003042425431.

    CAS  Article  Google Scholar 

  61. Strayer, D. L., Beighley, R. E., Thompson, L. C., Brooks, S., Nilsson, C., Pinay, G., & Naiman, R. J. (2003). Effects of land cover on stream ecosystems: roles of empirical models and scaling issues. Ecosystems, 6, 407–423. https://doi.org/10.1007/s10021-002-0170-0.

    Article  Google Scholar 

  62. Suedel, C. B., & Rodgers Jr., J. J. (1994). Responses of Hyalella Azteca and Chironomus Tentans to particle-size distribution and organic matter content of formulated and natural freshwater sediments. Environmental Toxicology and Chemistry, 13, 1639–1648. https://doi.org/10.1002/etc.5620131013.

    CAS  Article  Google Scholar 

  63. Tang, H., Song, M.-Y., Cho, W.-S., Park, Y.-S., & Chon, T.-S. (2010). Species abundance distribution of benthic chironomids and other macroinvertebrates across different levels of pollution in streams. Annales de Limnologie—Internal Journal of Limnology, 46, 53–66. https://doi.org/10.1051/limn/2009031.

    Article  Google Scholar 

  64. Townsend, C. R., Dolédec, S., Norris, R., Peacock, K., & Arbuckle, C. (2003). The influence of scale and geography on relationships between stream community composition and landscape variables: description and prediction. Freshwater Biology, 48, 768–785. https://doi.org/10.1046/j.1365-2427.2003.01043.x.

    Article  Google Scholar 

  65. Virbickas, T., Pliuraite, V., & Kesminas, V. (2011). Impact of agricultural land use on macroinvertebrate fauna in Lithuania. Polish Journal of Environmental Studies, 20, 1327–1334.

    Google Scholar 

  66. Wang, L., Lyons, J., Kanehl, P., & Gatti, R. (1997). Influences of watershed land use on habitat quality and biotic integrity in Wisconsin streams. Fisheries Magazine, 22, 6–12.

    Article  Google Scholar 

  67. Wood, P. J., & Armitage, P. D. (1997). Biological effects of fine sediment in the lotic environment. Environmental Management, 21, 203–217. https://doi.org/10.1002/hyp.7604.

    CAS  Article  Google Scholar 

  68. Wright, L. L., & Mattice, J. S. (1981). Substrate selection as a factor in Hexagenia distribution. Aquatic Insects, 3, 13–24. https://doi.org/10.1080/01650428109361039.

    Article  Google Scholar 

  69. Wright, I. A., & Ryan, M. M. (2016). Impact of mining and industrial pollution on stream macroinvertebrates: importance of taxonomic resolution, water geochemistry and EPT indices for impact detection. Hydrobiologia, 772, 103–115. https://doi.org/10.1007/s10750-016-2644-7.

    CAS  Article  Google Scholar 

  70. Yuan, L. (2010). Estimating the effects of excess nutrients on invertebrates from observational data. Ecological Applications, 20(1), 110–125.

    Article  Google Scholar 

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Acknowledgments

The authors would like to thank the Long Point Region Conservation Authority, the Kettle Creek Conservation Authority, the farmers who allowed us access to their land, and Emelia Myles-Gonzalez, Laura Johnson, Kathleen Lo, and Eric Johnson for their time and contributions to the study.

Funding

This work was supported by the Canada First Research Excellence Fund – Food For Thought Grant to K.S. McCann and Natural Science and Engineering Research Council Discovery Grant to R.S. Prosser. The funding source had no such involvement in the study design, collection, analysis, or interpretation of the data. There was also no involvement in the writing of the report or the decision to submit the article for publication.

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Wolf, J.F., Prosser, R.S., Champagne, E.J. et al. Variation in Response of Laboratory-Cultured Freshwater Macroinvertebrates to Sediment from Streams with Differential Exposure to Agriculture. Water Air Soil Pollut 231, 13 (2020). https://doi.org/10.1007/s11270-019-4376-6

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Keywords

  • Ephemeroptera
  • Agricultural land use
  • Sediment
  • Oligochaete
  • Amphipod