Skip to main content
Log in

Benthic Invertebrate Indices Show No Response to High Nitrate-Nitrogen in Lowland Agricultural Streams

  • Published:
Water, Air, & Soil Pollution Aims and scope Submit manuscript

Abstract

Globally benthic invertebrate biotic indices are widely used to assess stream health. In New Zealand, the response of biotic indices to high nitrate-nitrogen (hereafter nitrate) concentrations has not been rigorously tested. We conducted a field survey of benthic invertebrates in 41 lowland intensively farmed Canterbury streams representing a wide nitrate gradient (0.4–11.3 mg/l) to determine if biotic indices respond in a predictable manner to increasing nitrate (e.g. show a subsidy stress response). Our results show commonly used biotic indices were not able to detect any effects of high nitrate. We found homogenous and tolerant benthic invertebrate communities dominated and suggest the lack of any detected effects may be because taxa sensitive to nutrients have already been lost from these systems. Therefore, we recommend caution is needed when using biotic indices in lowland agricultural streams where nutrients may be high.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adler, P. B., Seabloom, E. W., Borer, E. T., Hillebrand, H., Hautier, Y., Hector, A., Harpole, W. S., O’Halloran, L. R., Grace, J. B., & Anderson, T. M. (2011). Productivity is a poor predictor of plant species richness. Science, 333, 1750–1753.

    Article  CAS  Google Scholar 

  • APHA. (1995). Standard methods for the examination of water and wastewater. American Public Health Associatoin.

    Google Scholar 

  • APHA. (2005). Part 2000 Physical and aggregate properties. In A. D. Eaton, L. S. Clesceri, E. W. Rice, & A. H. Greenberg (Eds.), Standard methods for the examination of water and wastewater (21st ed.). . American Public Health Association.

    Google Scholar 

  • Artigas, J., García-Berthou, E., Bauer, D. E., Castro, M. I., Cochero, J., Colautti, D. C., Cortelezzi, A., Donato, J. C., Elosegi, A., & Feijoó, C. (2013). Global pressures, specific responses: Effects of nutrient enrichment in streams from different biomes. Environmental Research Letters, 8, 014002.

    Article  Google Scholar 

  • Balvanera, P., Pfisterer, A. B., Buchmann, N., He, J. S., Nakashizuka, T., Raffaelli, D., & Schmid, B. J. (2006). Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecology Letters, 9, 1146–1156.

    Article  Google Scholar 

  • Berger, E., Haase, P., Schafer, R. B., & Sundermann, A. (2018). Towards stressor-specific macroinvertebrate indices: Which traits and taxonomic groups are associated with vulnerable and tolerant taxa? Science of the Total Environment, 619–620, 144–154.

    Article  CAS  Google Scholar 

  • Biggs, B. J. F. (2000). Eutrophication of streams and rivers: Dissolved nutrient-chlorophyll relationships for benthic algae. Journal of the North American Benthological Society, 19, 17–31.

    Article  Google Scholar 

  • Bini, L. M., Landeiro, V. L., Padial, A. A., Siqueira, T., & Heino, J. (2014). Nutrient enrichment is related to two facets of beta diversity for stream invertebrates across the United States. Ecology, 95, 1569–1578.

    Article  Google Scholar 

  • Borcard D., Gillet F., & Legendre, P. (2011). Unconstrained ordination. In Numerical ecology with R. Use R. New York: Springer. https://doi.org/10.1007/978-1-4419-7976-6_5.

  • Bovee K. (1982). A guide to stream habitat analysis using the instream flow incremental methodology. Instream Flow Information Paper 12. US Fish and Wildlife Service Biological Services Program FWS/OBS-82/26. USDI Fish and Wildlife Services

  • Burdon, F. J., McIntosh, A. R., & Harding, J. S. (2013). Habitat loss drives threshold response of benthic invertebrate communities to deposited sediment in agricultural streams. Ecological Applications, 23, 1036–1047.

    Article  Google Scholar 

  • Burnham, K. P., & Anderson, D. R. (2002). Model selection and multimodel inference: A practical information theoretic approach. Springer-Verlag.

    Google Scholar 

  • Burrell, T. K., O’Brien, J. M., Graham, S. E., Simon, K. S., Harding, J. S., & McIntosh, A. R. (2013). Riparian shading mitigates stream eutrophication in agricultural catchments. Freshwater Science, 33, 73–84.

    Article  Google Scholar 

  • Camargo, J. A., Alonso, A., & Salamanca, A. (2005). Nitrate toxicity to aquatic animals: A review with new data for freshwater invertebrates. Chemosphere, 58, 1255–1267.

    Article  CAS  Google Scholar 

  • Chapman, M. A., Lewis, M. H., & Winterbourn, M. J. (2011). Guide to the freshwater Crustacea of New Zealand. New Zealand Freshwater Sciences Society.

    Google Scholar 

  • Clapcott, J. E., Collier, K. J., Death, R. G., Goodwin, E. O., Harding, J. S., Kelly, D., Leathwick, J. R., & Young, R. G. (2012). Quantifying relationships between land-use gradients and structural and functional indicators of stream ecological integrity. Freshwater Biology, 57, 74–90.

    Article  Google Scholar 

  • Cortelezzi, A., Ocón, C., Oosterom, M. V. L. V., Cepeda, R., & Capítulo, A. R. (2015). Nutrient enrichment effect on macroinvertebrates in a lowland stream of Argentina. Iheringia Série Zoologia, 105, 228–234.

    Article  Google Scholar 

  • D’Amario, S. C., Rearick, D. C., Fasching, C., Kembel, S. W., Porter-Goff, E., Spooner, D. E., Williams, C. J., Wilson, H. F., & Xenopoulos, M. A. (2019). The prevalence of nonlinearity and detection of ecological breakpoints across a land use gradient in streams. Scientific Reports, 9, 3878.

    Article  CAS  Google Scholar 

  • Dodds, W. K. (2007). Trophic state, eutrophication and nutrient criteria in streams. Trends in Ecology and Evolution, 22, 669–676.

    Article  Google Scholar 

  • Dodds, W. K., Bouska, W. W., Eitzmann, J. L., Pilger, T. J., Pitts, K. L., Riley, A. J., Schloesser, J. T., & Thornbrugh, D. J. (2009). Eutrophication of US freshwaters: Analysis of potential economic damages. Environmental Science and Technology, 43, 12–19.

    Article  CAS  Google Scholar 

  • Dodson, S. I., Arnott, S. E., & Cottingham, K. L. (2000). The relationship in lake communities between primary productivity and species richness. Ecology, 81, 2662–2679.

    Article  Google Scholar 

  • Donohue, I., Jackson, A. L., Pusch, M. T., & Irvine, K. (2009). Nutrient enrichment homogenizes lake benthic assemblages at local and regional scales. Ecology, 90, 3470–3477.

    Article  Google Scholar 

  • Duggan, C. D., Collier, K. J., & Lambert, P. W. (2002). Evaluation of invertebrate biometrics and the influence of subsample size using data from some Westland, New Zealand, lowland streams. New Zealand Journal of Marine and Freshwater Research, 36, 117–128.

    Article  Google Scholar 

  • Erisman, J. W., Galloway, J. N., Seitzinger, S., Bleeker, A., Dise, N. B., Petrescu, A. R., Leach, A. M., & de Vries, W. (2013). Consequences of human modification of the global nitrogen cycle. Philosophical Transactions of the Royal Society B, 368, 20130116.

    Article  CAS  Google Scholar 

  • Evans-White, M. A., Dodds, W. K., Huggins, D. G., & Baker, D. S. (2009). Thresholds in macroinvertebrate biodiversity and stoichiometry across water-quality gradients in Central Plains (USA) streams. Journal of the North American Benthological Society, 28, 855–868.

    Article  Google Scholar 

  • Foote, K. J., Joy, M. K., & Death, R. G. (2015). New Zealand dairy farming: Milking our environment for all its worth. Environmental Mangement, 56, 709–720.

    Google Scholar 

  • Friberg, N., Skriver, J., Larsen, S. E., Pedersen, M. L., & Buffagni, A. (2010). Stream macroinvertebrate occurrence along gradients in organic pollution and eutrophication. Freshwater Biology, 55, 1405–1419.

    Article  CAS  Google Scholar 

  • Galloway, J. N., Townsend, A. R., Erisman, J. W., Bekunda, M., Cai, Z., Freney, J. R., Martinelli, L. A., Seitzinger, S. P., & Sutton, M. A. (2008). Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science, 320, 889–892.

    Article  CAS  Google Scholar 

  • Gleason, J. E., & Rooney, R. C. (2017). Aquatic macroinvertebrates are poor indicators of agricultural activity in northern prairie pothole wetlands. Ecological Indicators, 81, 333–339.

    Article  Google Scholar 

  • Goeller, B. C., Burbery, L. F., Febria, C. M., Collins, K. E., Burrows, N. J., Simon, K. S., Harding, J. S., & McIntosh, A. R. (2019). Capacity for bioreactors and riparian rehabilitation to enhance nitrate attenuation in agricultural streams. Ecological Engineering, 134, 65–77.

    Article  Google Scholar 

  • Good, A. G., & Beatty, P. H. (2011). Fertilizing nature: A tragedy of excess in the commons. PLoS Biology, 9, e1001124.

    Article  CAS  Google Scholar 

  • Gray, D. P., & Harding, J. S. (2012). Acid Mine Drainage Index (AMDI): A benthic invertebrate biotic index for assessing coal mining impacts in New Zealand Streams. New Zealand Journal of Marine and Freshwater Research, 46, 335–352.

    Article  CAS  Google Scholar 

  • Greenwood, M. J., Harding, J. S., Niyogi, D. K., & McIntosh, A. R. (2012). Improving the effectiveness of riparian management for aquatic invertebrates in a degraded agricultural landscape: Stream size and land-use legacies. Journal of Applied Ecology, 49, 213–222.

    Article  Google Scholar 

  • Groffman, P. M., Baron, J. S., Blett, T., Gold, A. J., Goodman, I., Gunderson, L. H., Levinson, B. M., Palmer, M. A., Paerl, H. W., & Peterson, G. D. (2006). Ecological thresholds: the key to successful environmental management or an important concept with no practical application? Ecosystems, 9, 1–13.

    Article  Google Scholar 

  • Hanson CR. 2002. Nitrate concentrations in Canterbury groundwater. Canterbury Regional Council report R02/17

  • Harding, J. S., Clapcott, J. E., Quinn, J. M., Hayes, J. W., Joy, M. K., Storey, R. G., Greig, H. S., Hay, J., James, T., Beech, M. A., et al. (2009). Stream habitat assessment protocols for wadeable rivers and streams of New Zealand. University of Canterbury.

    Google Scholar 

  • Hickey, C. W., & Vickers, M. L. (1992). Comparison of the sensitivity to heavy metals and pentachlorophenol of the mayflies Deleatidium spp. and the cladoceran Daphnia magna. New Zealand Journal of Marine and Freshwater Research, 26, 87–93.

    Article  CAS  Google Scholar 

  • Hillebrand, H., & Cardinale, B. J. (2010). A critique for meta-analyses and the productivity–diversity relationship. Ecology, 91, 2545–2549.

    Article  Google Scholar 

  • Joy, M. K., Foote, K. J., McNie, P., & Piria, M. (2018). Decline in New Zealand’s freshwater fish fauna: Effect of land use. Marine and Freshwater Research, 70, 114–124.

    Article  Google Scholar 

  • Jowett, I. G., & Richardson, J. (1990). Microhabitat preferences of benthic invertebrates in a New Zealand river and the development of in-stream flow-habitat models for Deleatidium spp. New Zealand Journal of Marine and Freshwater Research, 24, 19–30.

    Article  Google Scholar 

  • Kronvang, B., Jensen, J. P., Hoffmann, C. C., & Boers, P. (2008). Chapter 9 - Nitrogen transport and fate in European streams, rivers, lakes, and wetlands. In J. L. Hatfield, R. F. Follett (Eds.), Nitrogen in the environment (Second Edition) (pp. 241–270). Academic Press. https://doi.org/10.1016/B978-0-12-374347-3.00009-3.

  • Kruskal, J. B. (1964). Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika, 29, 1–27.

    Article  Google Scholar 

  • Kuzmanovic, M., Doledec, S., de Castro-Catala, N., Ginebreda, A., Sabater, S., Munoz, I., & Barcelo, D. (2017). Environmental stressors as a driver of the trait composition of benthic macroinvertebrate assemblages in polluted Iberian rivers. Environmental Research, 156, 485–493.

    Article  CAS  Google Scholar 

  • Lake, P. S. (2000). Disturbance, patchiness, and diversity in streams. Journal of the North American Benthological Society, 19, 573–592.

    Article  Google Scholar 

  • MacLeod, C. J., & Moller, H. (2006). Intensification and diversification of New Zealand agriculture since 1960: An evaluation of current indicators of land use change. Agriculture, Ecosystems & Environment, 115, 201–218.

    Article  Google Scholar 

  • Martin M, Thompson K. (2012). Chronic sensitivity of two native New Zealand species (freshwater fish-Inanga Galaxias maculatus and mayfly-Deleatidium spp.) to nitrate. HBR12230

  • Meybeck, M. (1982). Carbon, nitrogen, and phosphorus transport by world rivers. American Journal of Science, 282, 401–450.

    Article  CAS  Google Scholar 

  • Mittelbach, G. G., Steiner, C. F., Scheiner, S. M., Gross, K. L., Reynolds, H. L., Waide, R. B., Willig, M. R., Dodson, S. I., & Gough, L. (2001). What is the observed relationship between species richness and productivity? Ecology, 82, 2381–2396.

    Article  Google Scholar 

  • Niyogi, D. K., Koren, M., Arbuckle, C. J., & Townsend, C. R. (2007). Stream communities along a catchment land-use gradient: Subsidy-stress responses to pastoral development. Environmental Management, 39, 213–225.

    Article  Google Scholar 

  • Nguyen, T. H. T., Boets, P., Lock, K., Forio, M. A. E., Van Echelpoel, W., Van Butsel, J., Utreras, J. A. D., Everaert, G., Granda, L. E. D., Hoang, T. H. T., et al. (2017). Water quality related macroinvertebrate community responses to environmental gradients in the Portoviejo River (Ecuador). Annales De Limnologie - International Journal of Limnology, 53, 203–219.

    Article  Google Scholar 

  • Odum, E. P., Finn, J. T., & Franz, E. H. (1979). Perturbation theory and the subsidy-stress gradient. BioScience, 29, 349–352.

    Article  Google Scholar 

  • O’Halloran, K., Cavanagh, J. A., & Harding, J. S. (2008). Response of a New Zealand mayfly (Deleatidium spp.) to acid mine drainage: Implications for mine remediation. Environmental Toxicology and Chemistry: an International Journal, 27, 1135–1140.

    Article  Google Scholar 

  • Oksanen J. (2015). Multivariate analysis of ecological communities in R: Vegan tutorial. R package version 2.5–4

  • Ouyang, Z., Qian, S. S., Becker, R., & Chen, J. (2018). The effects of nutrients on stream invertebrates: A regional estimation by generalized propensity score. Ecological Processes, 7, 21.

    Article  Google Scholar 

  • Pangborn MC, Woodford KB. 2011. Canterbury dairying - a study in land use change and increasing production. Proceedings of the 18th International Farm Management Congress, Methven, Canterbury, New Zealand. International Farm Management Association, Cambridge, UK

  • Pangborn, M. C., Woodford, K. B., & Nuthall, P. L. (2015). Development of a dairy industry in a new area-land use change in Canterbury, New Zealand. International Journal of Agricultural Management, 5, 20–24.

    Google Scholar 

  • Pfankuch DJ. (1975). Stream reach inventory and channel stability evaluation, Missoula, Montana: USDA Forest Service, Region 1

  • R Core Team (2018). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. URLhttps://www.R-project.org/.

  • Reid, A. J., Carlson, A. K., Creed, I. F., Eliason, E. J., Gell, P. A., Johnson, P. T. J., Kidd, K. A., MacCormack, T. J., Olden, J. D., Ormerod, S. J., et al. (2019). Emerging threats and persistent conservation challenges for freshwater biodiversity. Biological Reviews, 94, 849–873.

    Article  Google Scholar 

  • Resh, V. H., & Rosenberg, D. M. (1993). Freshwater biomonitoring and benthic macroinvertebrates. Chapman and Hall.

    Google Scholar 

  • Robinson, P. W., & Scott, R. R. (1995). The toxicity of cyromazine to Chironomus zealandicus (Chironomidae) and Deleatidium spp. (Leptophlebiidae). Pesticide Science, 44, 283–292.

    Article  CAS  Google Scholar 

  • Sala, O. E., Chapin, F. S., Armesto, J. J., Berlow, E., Bloomfield, J., Dirzo, R., Huber-Sanwald, E., Huenneke, L. F., Jackson, R. B., & Kinzig, A. (2000). Global biodiversity scenarios for the year 2100. Science, 287, 1770–1774.

    Article  CAS  Google Scholar 

  • Scheffer, M., Carpenter, S. R., Lenton, T. M., Bascompte, J., Brock, W., Dakos, V., Van de Koppel, J., Van de Leemput, I. A., Levin, S. A., & Van Nes, E. H. (2012). Anticipating critical transitions. Science, 338, 344–348.

    Article  CAS  Google Scholar 

  • Smith, V. H., Tilman, G. D., & Nekola, J. C. (1999). Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environmental Pollution, 100, 179–196.

    Article  CAS  Google Scholar 

  • Smith, A. J., Bode, R. W., & Kleppel, G. S. (2007). A nutrient biotic index (NBI) for use with benthic macroinvertebrate communities. Ecological Indicators, 7, 371–386.

    Article  Google Scholar 

  • Stark JD. (1985). A macroinvertebrate community index of water quality for stoney streams. Water and Soil Miscellaneous Publication 87. National Water and Soil Conservation Authority

  • Stark, J. D. (1993). Performance of the Macroinvertebrate Community Index: Effects of sampling method, sample replication, water depth, current velocity, and substratum on index values. New Zealand Journal of Marine and Freshwater Research, 27, 463–478.

    Article  Google Scholar 

  • Stark JD, Boothroyd IKG, Harding JS, Maxted JR, Scarsbrook MR. (2001). Protocols for sampling macroinvertebrates in wadeable streams, New Zealand Macroinvertebrate Working Group report no. 1 Wellington: Ministry for the Environment

  • Sultana, J., Recknagel, F., Tibby, J., & Maxwell, S. (2019). Comparison of water quality thresholds for macroinvertebrates in two Mediterranean catchments quantified by the inferential techniques TITAN and HEA. Ecological Indicators, 101, 867–877.

    Article  CAS  Google Scholar 

  • Sundermann, A., Leps, M., Leisner, S., & Haase, P. (2015). Taxon-specific physico-chemical change points for stream benthic invertebrates. Ecological Indicators, 57, 314–323.

    Article  CAS  Google Scholar 

  • Thompson, R., & Townsend, C. R. (2005). Energy availability, spatial heterogeneity and ecosystem size predict food-web structure in streams. Oikos, 108, 137–148.

    Article  Google Scholar 

  • Tilman, D., Balzer, C., Hill, J., & Befort, B. L. (2011). Global food demand and the sustainable intensification of agriculture. Proceedings of the National Academy of Sciences, 108, 20260–20264.

    Article  CAS  Google Scholar 

  • Townsend, C. R., Scarsbrook, M. R., & Dolédec, S. J. (1997). Quantifying disturbance in streams: Alternative measures of disturbance in relation to macroinvertebrate species traits and species richness. Journal of the North American Benthological Society, 16, 531–544.

    Article  Google Scholar 

  • Townsend, C. R., Thompson, R. M., McIntosh, A. R., Kilroy, C., Edwards, E., & Scarsbrook, M. R. (1998). Disturbance, resource supply, and food-web architecture in streams. Ecology Letters, 1, 200–209.

    Article  Google Scholar 

  • Turunen, J., Muotka, T., Vuori, K. M., Karjalainen, S. M., Raapysjarvi, J., Sutela, T., & Aroviita, J. (2016). Disentangling the responses of boreal stream assemblages to low stressor levels of diffuse pollution and altered channel morphology. Science of the Total Environment, 544, 954–962.

    Article  CAS  Google Scholar 

  • Ver Hoef, J. M., & Boveng, P. L. (2007). Quasi-Poisson vs. negative binomial regression: How should we model overdispersed count data? Ecology, 88, 2766–2772.

    Article  Google Scholar 

  • Wagenhoff, A., Clapcott, J. E., Lau, K. E., Lewis, G. D., & Young, R. G. (2017). Identifying congruence in stream assemblage thresholds in response to nutrient and sediment gradients for limit setting. Ecological Applications, 27, 469–484.

    Article  Google Scholar 

  • Wagenhoff, A., Townsend, C. R., & Matthaei, C. D. (2012). Macroinvertebrate responses along broad stressor gradients of deposited fine sediment and dissolved nutrients: A stream mesocosm experiment. Journal of Applied Ecology, 49, 892–902.

    Article  CAS  Google Scholar 

  • Wagenhoff, A., Townsend, C. R., Phillips, N., & Matthaei, C. D. (2011). Subsidy-stress and multiple-stressor effects along gradients of deposited fine sediment and dissolved nutrients in a regional set of streams and rivers. Freshwater Biology, 56, 1916–1936.

    Article  Google Scholar 

  • Wentworth, C. K. (1922). A scale of grade and class terms for clastic sediments. The Journal of Geology, 30, 377–392.

    Article  Google Scholar 

  • Winterbourn, M. J. (1973). A guide to the freshwater Mollusca of New Zealand. Tuatara, 20, 141–159.

    Google Scholar 

  • Winterbourn MJ, Gregson KLD, Dolphin CH. (2006). Guide to the aquatic insects of New Zealand. 3rd ed. Bulletin of the Entomological Society of New Zealand 14

  • Wright-Stow, A. E., & Winterbourn, M. J. (2003). How well do New Zealand’s stream-monitoring indicators, the macroinvertebrate community index and its quantitative variant, correspond? New Zealand Journal of Freshwater and Marine Research, 37, 461–470.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Zhang, Y., Cheng, L., Li, K., Zhang, L., Cai, Y., Wang, X., & Heino, J. (2018). Nutrient enrichment homogenizes taxonomic and functional diversity of benthic macroinvertebrate assemblages in shallow lakes. Limnology and Oceanography, 64, 1047–1058.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Elizabeth Graham and anonymous reviewers for valuable feedback to improve the quality of the manuscript, along with Hayley Devlin and Nixie Boddy for field work assistance, and Linda Morris, Kim Roberts and Jon O’Brien for laboratory assistance.

Funding

This project was funded by a grant from the Mackenzie Charitable Foundation as part of the Canterbury Waterways Rehabilitation Experiment. TM was supported by an Environment Canterbury Postgraduate Scholarship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Thomas P. Moore.

Ethics declarations

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 204 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Moore, T.P., Febria, C.M., McIntosh, A.R. et al. Benthic Invertebrate Indices Show No Response to High Nitrate-Nitrogen in Lowland Agricultural Streams. Water Air Soil Pollut 232, 263 (2021). https://doi.org/10.1007/s11270-021-05169-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11270-021-05169-1

Keywords

Navigation