Inconsistent Relationships of Primary Consumer N Stable Isotope Values to Gradients of Sheep/Beef Farming Intensity and Flow Reduction in Streams
Abstract
:1. Introduction
- δ15N values of common primary consumers (grazers) will show similar patterns along the gradients of catchment land-use intensity because they all feed on one resource (periphyton) and are therefore ingesting food with the same isotopic composition;
- δ15N values are positively related to catchment land-use intensities because higher farming intensity and greater flow reduction increase the input of heavy isotopes from fertilisation and increase the intensity of nitrogen transformation processes [17]; and
- δ15N values follow antagonistic response patterns along the gradients of land-use intensity and flow reduction because both stressors have strong individual effects and their joint effects cannot exceed 100% [3].
2. Methods
2.1. Study Sites
2.2. Field Sampling and Sample Processing
2.3. Data Analysis
3. Results
4. Discussion
4.1. Do Primary Consumers Show Similar Relationships along Stressor Gradients
4.2. Multiple-Stressor Patterns of Primary Consumer Stable Isotope Values
4.3. Differences in Consumers’ Relationships with Sheep/Beef Farming Intensity
4.4. Positive Consumer Relationships with Flow Reduction Intensity
4.5. Antagonistic Stressor Interaction
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Vinebrooke, R.D.; Cottingham, K.L.; Norberg, M.S.J.; Dodson, S.I.; Maberly, S.C.; Sommer, U.; Norberg, M.S. Impacts of multiple stressors on biodiversity and ecosystem functioning: The role of species co-tolerance. Oikos 2004, 104, 451–457. [Google Scholar] [CrossRef]
- Ormerod, S.J.; Dobson, M.; Hildrew, A.G.; Townsend, C.R. Multiple stressors in freshwater ecosystems. Freshw. Boil. 2010, 55, 1–4. [Google Scholar] [CrossRef]
- Folt, C.L.; Chen, C.Y.; Moore, M.V.; Burnaford, J. Synergism and antagonism among multiple stressors. Limnol. Oceanogr. 1999, 44, 864–877. [Google Scholar] [CrossRef] [Green Version]
- Vivian, C. Tracers of sewage sludge in the marine environment: A review. Sci. Total Environ. 1986, 53, 5–40. [Google Scholar] [CrossRef]
- Peterson, B.J.; Fry, B. Stable Isotopes in Ecosystem Studies. Annu. Rev. Ecol. Syst. 1987, 18, 293–320. [Google Scholar] [CrossRef]
- Anderson, C.; Cabana, G. Does δ15N in river food webs reflect the intensity and origin of N loads from the watershed? Sci. Total Environ. 2006, 367, 968–978. [Google Scholar] [CrossRef]
- Clapcott, J.E.; Young, R.G.; Goodwin, E.O.; Leathwick, J.R. APPLIED ISSUES: Exploring the response of functional indicators of stream health to land-use gradients. Freshw. Boil. 2010, 55, 2181–2199. [Google Scholar] [CrossRef]
- Larson, J.H.; Richardson, W.B.; Vallazza, J.M.; Nelson, J.C. Rivermouth Alteration of Agricultural Impacts on Consumer Tissue δ15N. PLoS ONE 2013, 8, e69313. [Google Scholar] [CrossRef]
- Lake, J.L.; McKinney, R.A.; Osterman, F.A.; Pruell, R.J.; Kiddon, J.; Ryba, S.A.; Libby, A.D. Stable nitrogen isotopes as indicators of anthropogenic activities in small freshwater systems. Can. J. Fish. Aquat. Sci. 2001, 58, 870–878. [Google Scholar] [CrossRef]
- Cabana, G.; Rasmussen, J.B. Comparison of aquatic food chains using nitrogen isotopes. Proc. Natl. Acad. Sci. USA 1996, 93, 10844–10847. [Google Scholar] [CrossRef]
- McClelland, J.W.; Valiela, I. Linking nitrogen in estuarine producers to land-derived sources. Limnol. Oceanogr. 1998, 43, 577–585. [Google Scholar] [CrossRef] [Green Version]
- Vermeulen, S.; Sturaro, N.; Gobert, S.; Bouquegneau, J.; Lepoint, G. Potential early indicators of anthropogenically derived nutrients: A multiscale stable isotope analysis. Mar. Ecol. Prog. Ser. 2011, 422, 9–22. [Google Scholar] [CrossRef]
- Barr, N.G.; Dudley, B.D.; Rogers, K.M.; Cornelisen, C.D. Broad-scale patterns of tissue-δ15N and tissue-N indices in frondose Ulva spp.; developing a national baseline indicator of nitrogen-loading for coastal New Zealand. Mar. Pollut. Bull. 2013, 67, 203–216. [Google Scholar] [CrossRef] [PubMed]
- Allan, J.D. Landscapes and Riverscapes: The Influence of Land Use on Stream Ecosystems. Annu. Rev. Ecol. Evol. Syst. 2004, 35, 257–284. [Google Scholar] [CrossRef] [Green Version]
- Davies-Colley, R.J.; Meleason, M.A.; Hall, R.M.; Rutherford, J.C. Modelling the time course of shade, temperature, and wood recovery in streams with riparian forest restoration. N. Z. J. Mar. Freshw. Res. 2009, 43, 673–688. [Google Scholar] [CrossRef] [Green Version]
- Dewson, Z.S.; James, A.B.W.; Death, R.G. A review of the consequences of decreased flow for instream habitat and macroinvertebrates. J. N. Am. Benthol. Soc. 2007, 26, 401–415. [Google Scholar] [CrossRef]
- Seitzinger, S.; Harrison, J.A.; Bohlke, J.K.; Bouwman, A.F.; Lowrance, R.; Peterson, B.; Tobias, C.; Van Drecht, G. Denitrification across landscapes and waterscapes: A synthesis. Ecol. Appl. 2006, 16, 2064–2090. [Google Scholar] [CrossRef]
- Anderson, C.; Cabana, G. δ15N in riverine food webs: Effects of N inputs from agricultural watersheds. Can. J. Fish. Aquat. Sci. 2005, 62, 333–340. [Google Scholar] [CrossRef]
- Mayer, B.; Boyer, E.W.; Goodale, C.; Jaworski, N.A.; Van Breemen, N.; Howarth, R.W.; Seitzinger, S.; Billen, G.; Lajtha, K.; Nadelhoffer, K.; et al. Sources of nitrate in rivers draining sixteen watersheds in the northeastern U.S.: Isotopic constraints. Biogeochemistry 2002, 57, 171–197. [Google Scholar] [CrossRef]
- Sébilo, M.; Billen, G.; Grably, M.; Mariotti, A. Isotopic composition of nitrate-nitrogen as a marker of riparian and benthic denitrification at the scale of the whole Seine River system. Biogeochemistry 2003, 63, 35–51. [Google Scholar] [CrossRef]
- Kellman, L.; Hillaire-Marcel, C. Nitrate cycling in streams: Using natural abundances of -δ15N to measure in-situ denitrification. Biogeochemistry 1998, 43, 273–292. [Google Scholar] [CrossRef]
- Diebel, M.W.; Zanden, M.J.V. Nitrogen stable isotopes in streams: Effects of agricultural sources and transformations. Ecol. Appl. 2009, 19, 1127–1134. [Google Scholar] [CrossRef] [PubMed]
- Kendall, C. Tracing Nitrogen Sources and Cycling in Catchments. In Isotope Tracers in Catchment Hydrology; Kendall, C., McDonnell, J.J., Eds.; Elsevier: Amsterdam, The Netherlands, 1998; pp. 519–576. [Google Scholar]
- Voss, M.; Deutsch, B.; Elmgren, R.; Humborg, C.; Kuuppo, P.; Pastuszak, M.; Rolff, C.; Schulte, U. Source identification of nitrate by means of isotopic tracers in the Baltic Sea catchments. Biogeosciences 2006, 3, 663–676. [Google Scholar] [CrossRef] [Green Version]
- Barnes, R.T.; Raymond, P.A. Land-use controls on sources and processing of nitrate in small watersheds: Insights from dual isotopic analysis. Ecol. Appl. 2010, 20, 1961–1978. [Google Scholar] [CrossRef]
- Udy, J.W.; Fellows, C.S.; Bartkow, M.E.; Bunn, S.E.; Clapcott, J.E.; Harch, B.D. Measures of Nutrient Processes as Indicators of Stream Ecosystem Health. Hydrobiologia 2006, 572, 89–102. [Google Scholar] [CrossRef]
- Udy, J.W.; Bunn, S.E. Elevated delta N-15 values in aquatic plants from cleared catchments: Why? Mar. Freshw. Res. 2001, 52, 347–351. [Google Scholar] [CrossRef]
- Atkinson, C.L.; Christian, A.D.; Spooner, D.E.; Vaughn, C.C. Long-lived organisms provide an integrative footprint of agricultural land use. Ecol. Appl. 2014, 24, 375–384. [Google Scholar] [CrossRef]
- Anderson, C.; Cabana, G. Estimating the trophic position of aquatic consumers in river food webs using stable nitrogen isotopes. J. N. Am. Benthol. Soc. 2007, 26, 273–285. [Google Scholar] [CrossRef]
- Finlay, J.C. Patterns and controls of lotic algal stable carbon isotope ratios. Limnol. Oceanogr. 2004, 49, 850–861. [Google Scholar] [CrossRef] [Green Version]
- Jardine, T.D.; Kidd, K.A.; Fisk, A.T. Applications, Considerations, and Sources of Uncertainty When Using Stable Isotope Analysis in Ecotoxicology. Environ. Sci. Technol. 2006, 40, 7501–7511. [Google Scholar] [CrossRef]
- Jardine, T.D.; Hadwen, W.L.; Hamilton, S.K.; Hladyz, S.; Mitrovic, S.M.; Kidd, K.A.; Tsoi, W.Y.; Spears, M.; Westhorpe, D.P.; Fry, V.M.; et al. Understanding and covercoming baseline isotopic variability in running waters. River Res. Appl. 2014, 30, 155–165. [Google Scholar] [CrossRef]
- Jackson, M.C.; Loewen, C.J.G.; Vinebrooke, R.D.; Chimimba, C.T. Net effects of multiple stressors in freshwater ecosystems: A meta-analysis. Glob. Chang. Biol. 2016, 22, 180–189. [Google Scholar] [CrossRef] [PubMed]
- Lange, K.; Townsend, C.R.; Matthaei, C.D. Can biological traits of stream invertebrates help disentangle the effects of multiple stressors in an agricultural catchment? Freshw. Boil. 2014, 59, 2431–2446. [Google Scholar] [CrossRef]
- Lange, K.; Townsend, C.R.; Gabrielsson, R.; Chanut, P.C.M.; Matthaei, C.D. Responses of stream fish populations to farming intensity and water abstraction in an agricultural catchment. Freshwat. Biol. 2014, 59, 286–299. [Google Scholar] [CrossRef]
- Ministry for the Environment. Land Cover Database II (LCDB2); Ministry for the Environment: Wellington, New Zealand, 2008.
- Ministry for the Environment. River Environmental Classification (REC); Ministry for the Environment: Wellington, New Zealand, 2010.
- Harding, J.S.; Benfield, E.F.; Bolstad, P.V.; Helfman, G.S.; Jones, E.B.D. Stream biodiversity: The ghost of land use past. Proc. Natl. Acad. Sci. USA 1998, 95, 14843–14847. [Google Scholar] [CrossRef] [Green Version]
- Kienzle, S.W.; Schmidt, J. Hydrological impacts of irrigated agriculture in the Manuherikia catchment, Otago, New Zealand. J. Hydrol. N. Z. 2008, 47, 67–84. [Google Scholar]
- Stark, J.D.; Boothroyd, I.K.G.; Harding, J.S.; Maxted, J.R.; Scarsbrook, M.R. Protocols for Sampling Macroinvertebrates in Wadeable Streams; Ministry for the Environment: Wellington, New Zealand, 2001; p. 48.
- Syväranta, J.; Vesala, S.; Rask, M.; Ruuhijärvi, J.; Jones, R. Evaluating the utility of stable isotope analyses of archived freshwater sample materials. Hydrobiologia 2008, 600, 121–130. [Google Scholar] [CrossRef]
- Lau, D.C.P.; Leung, K.M.Y.; Dudgeon, D. Preservation effects on C/N ratios and stable isotope signatures of freshwater fishes and benthic macroinvertebrates. Limnol. Oceanogr. Methods 2012, 10, 75–89. [Google Scholar] [CrossRef]
- Jardine, T.D.; Curry, R.A.; Heard, K.S.; Cunjak, R.A. High fidelity: Isotopic relationship between stream invertebrates and their gut contents. J. N. Am. Benthol. Soc. 2005, 24, 290–299. [Google Scholar] [CrossRef]
- Johnson, J.B.; Omland, K.S. Model selection in ecology and evolution. Trends Ecol. Evol. 2004, 19, 101–108. [Google Scholar] [CrossRef]
- Wagenhoff, A.; Townsend, C.R.; Phillips, N.; Matthaei, C.D. Subsidy-stress and multiple-stressor effects along gradients of deposited fine sediment and dissolved nutrients in a regional set of streams and rivers. Freshw. Boil. 2011, 56, 1916–1936. [Google Scholar] [CrossRef]
- Finlay, J.C.; Power, M.E.; Cabana, G. Effects of water velocity on algal carbon isotope ratios: Implications for river food web studies. Limnol. Oceanogr. 1999, 44, 1198–1203. [Google Scholar] [CrossRef] [Green Version]
- Schielzeth, H. Simple means to improve the interpretability of regression coefficients. Methods Ecol. Evol. 2010, 1, 103–113. [Google Scholar] [CrossRef]
- Burnham, K.P.; Anderson, D.R. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach; Springer: New York, NY, USA, 2002; Volume 2, p. 488. [Google Scholar]
- R Development Core Team. R: A Language and Environment for Statistical Computing, 3.0.2; R Development Core Team: Vienna, Austria, 2014. [Google Scholar]
- Bates, D.; Maechler, M.; Bolker, B.; Walker, S. Lme4: Mixed-Effects Modeling with R, 1.1-7. 2015. Available online: https://mran.microsoft.com/snapshot/2016-03-04/web/packages/lme4/README.html (accessed on 26 October 2019).
- Bartoń, K. MuMIn: Multi-Model Inference, 1.9.0. 2013. Available online: http://www2.uaem.mx/r-mirror/web/packages/MuMIn/MuMIn.pdf (accessed on 26 October 2019).
- Nakagawa, S.; Cuthill, I.C. Effect size, confidence interval and statistical significance: A practical guide for biologists. Boil. Rev. 2007, 82, 591–605. [Google Scholar] [CrossRef] [PubMed]
- Post, D.M. Using stable isotopes to estimate trophic position: Models, methods, and assumptions. Ecology 2002, 83, 703–718. [Google Scholar] [CrossRef]
- Broekhuizen, N.; Parkyn, S.; Miller, D. Fine sediment effects on feeding and growth in the invertebrate grazers Potamopyrgus antipodarum (Gastropoda, Hydrobiidae) and Deleatidium sp. (Ephemeroptera, Leptophlebiidae). Hydrobiologia 2001, 457, 125–132. [Google Scholar] [CrossRef]
- Finlay, J.C. Stable-Carbon-Isotope Ratios of River Biota: Implications for Energy Flow in Lotic Food Webs. Ecology 2001, 82, 1052. [Google Scholar] [CrossRef]
- Hicks, B.J. Food webs in forest and pasture streams in the Waikato region, New Zealand: A study based on analyses of stable isotopes of carbon and nitrogen, and fish gut contents. N. Z. J. Mar. Freshw. Res. 1997, 31, 651–664. [Google Scholar] [CrossRef] [Green Version]
- Holomuzki, J.R.; Biggs, B.J.F. Food Limitation Affects Algivory and Grazer Performance for New Zealand Stream Macroinvertebrates. Hydrobiologia 2006, 561, 83–94. [Google Scholar] [CrossRef]
- Rounick, J.S.; Winterbourn, M.J. The formation, structure and utilization of stone surface organic layers in two New Zealand streams. Freshw. Boil. 1983, 13, 57–72. [Google Scholar] [CrossRef]
- Parkyn, S.M.; Quinn, J.M.; Cox, T.J.; Broekhuizen, N. Pathways of N and C uptake and transfer in stream food webs: An isotope enrichment experiment. J. N. Am. Benthol. Soc. 2005, 24, 955–975. [Google Scholar] [CrossRef]
- Townsend, C.R.; Uhlmann, S.S.; Matthaei, C.D. Individual and combined responses of stream ecosystems to multiple stressors. J. Appl. Ecol. 2008, 45, 1810–1819. [Google Scholar] [CrossRef]
- Finlay, J.C.; Kendall, C. Stable isotope tracing of temporal and spatial variability in organic matter sources to freshwater ecosystems. In Stable Isotopes in Ecology and Environmental Science; Michener, R.H., Lajtha, K., Eds.; Blackwell Publishing: Singapore, 2007; pp. 283–333. [Google Scholar]
- Crain, C.M.; Kroeker, K.; Halpern, B.S. Interactive and cumulative effects of multiple human stressors in marine systems. Ecol. Lett. 2008, 11, 1304–1315. [Google Scholar] [CrossRef] [PubMed]
- Huryn, A.D. Temperature-dependent growth and life cycle of Deleatidium (Ephemeroptera: Leptophlebiidae) in two high-country streams in New Zealand. Freshwat. Biol. 1996, 36, 351–361. [Google Scholar] [CrossRef]
- Dybdahl, M.F.; Kane, S.L. Adaptation vs. phenotypic plasticity in the success of a clonal invader. Ecology 2005, 86, 1592–1601. [Google Scholar] [CrossRef]
- Broekhuizen, N.; Parkyn, S.; Miller, D.; Rose, R. The relationship between food density and short term assimilation rates in Potamopyrgus antipodarum and Deleatidium sp. Hydrobiologia 2002, 477, 181–188. [Google Scholar] [CrossRef]
- Piggott, J.J.; Niyogi, D.K.; Townsend, C.R.; Matthaei, C.D. Multiple stressors and stream ecosystem functioning: Climate warming and agricultural stressors interact to affect processing of organic matter. J. Appl. Ecol. 2015, 52, 1126–1134. [Google Scholar] [CrossRef]
- Aebi, A.; Neumann, P. Endosymbionts and honey bee colony losses? Trends Ecol. Evol. 2011, 26, 494. [Google Scholar] [CrossRef] [Green Version]
- Potts, S.G.; Biesmeijer, J.C.; Kremen, C.; Neumann, P.; Schweiger, O.; Kunin, W.E. Global pollinator declines: Trends, impacts and drivers. Trends Ecol. Evol. 2010, 25, 345–353. [Google Scholar] [CrossRef]
- McLeod, E.; Anthony, K.R.; Andersson, A.; Beeden, R.; Golbuu, Y.; Kleypas, J.; Kroeker, K.; Manzello, D.; Salm, R.V.; Schuttenberg, H.; et al. Preparing to manage coral reefs for ocean acidification: Lessons from coral bleaching. Front. Ecol. Environ. 2013, 11, 20–27. [Google Scholar] [CrossRef]
Response Variable | Intercept | FI | FI × FI | FR | FI × FR | ΔAICc | Weight | Marginal R2 | |||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
95% CIs | ES | 95% CIs | ES | 95% CIs | ES | 95% CIs | ES | 95% CIs | |||||
δ15N Deleatidium | 0.12 | (−0.02, 0.26) | 1.23 | (0.86, 1.60) | −0.48 | (−0.83, −0.12) | 0.00 | 0.51 | 0.75 | ||||
0.14 | (0.01, 0.29) | 0.94 | (0.59, 1.29) | 0.15 | (−0.14, 0.44) | −0.92 | (−1.70, −0.14) | 1.48 | 0.25 | 0.76 | |||
0.01 | (−0.12, 0.15) | 0.84 | (0.56, 1.13) | 1.53 | 0.24 | 0.66 | |||||||
δ15N Potamopyrgus | −0.01 | (−0.19, 0.16) | 0.00 | 0.73 | 0.00 | ||||||||
−0.01 | (−0.19, 0.16) | 0.24 | (−0.09, 0.57) | 1.95 | 0.27 | 0.06 | |||||||
δ15N Physella | −0.02 | (−0.19, 0.15) | 0.00 | 0.52 | 0.00 | ||||||||
−0.02 | (−0.18, 0.14) | 0.26 | (−0.06, 0.57) | 1.57 | 0.24 | 0.06 | |||||||
−0.03 | (−0.19, 0.14) | −0.26 | (−0.58, 0.06) | 1.58 | 0.24 | 0.06 |
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Lange, K.; Townsend, C.R.; Matthaei, C.D. Inconsistent Relationships of Primary Consumer N Stable Isotope Values to Gradients of Sheep/Beef Farming Intensity and Flow Reduction in Streams. Water 2019, 11, 2239. https://doi.org/10.3390/w11112239
Lange K, Townsend CR, Matthaei CD. Inconsistent Relationships of Primary Consumer N Stable Isotope Values to Gradients of Sheep/Beef Farming Intensity and Flow Reduction in Streams. Water. 2019; 11(11):2239. https://doi.org/10.3390/w11112239
Chicago/Turabian StyleLange, Katharina, Colin R. Townsend, and Christoph D. Matthaei. 2019. "Inconsistent Relationships of Primary Consumer N Stable Isotope Values to Gradients of Sheep/Beef Farming Intensity and Flow Reduction in Streams" Water 11, no. 11: 2239. https://doi.org/10.3390/w11112239