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Benthic metabolism responses to environmental attributes at multiple scales and its linkage to algal community structure in streams

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Abstract

Human activities have increasingly impacted rivers globally and influence environmental factors at multiple scales: proximal factors (e.g., light and nutrients) and distal controls (e.g., riparian cover and forest area in the basin) that affect benthic metabolism or algal assemblage structure. Function and structure have been studied separately and thus the linkage between them is not well understood. Furthermore, how much of the variability of benthic metabolism can be explained by changes in the environmental variables is inconclusive. We measured the structural and metabolism of epilithic algae in streams across gradients of catchment forest cover (3.5 to 88.6%) and riparian zone canopy cover (0 to 91.0%) in South East Queensland, Australia. Overall net daily metabolism (NDM) on cobbles was positive (gross primary production, GPP exceeded respiration, R) for all but three of the 34 sites. Chl a biomass of benthic algae on cobbles ranged from 1.37 to 178.05 mg m−2. Shaded streams had the highest percentage of diatoms (95.4%), while the least shaded streams were dominated by cyanobacteria (82.2%). Partial least squares (PLS) regression modeling showed that most of the variation in GPP, R, and NDM was explained by light intensity (photosynthetic photon flux density, PPFD), phosphorus concentration in water, water temperature, and the percentage of mid-dense forest upstream of the site. Path analysis (structural equation modeling, SEM) indicated that, as a surrogate for metabolism, diatom (Bacillariophyta) density was the best predictor of GPP and NDM when we assessed the environmental process in the streams. In comparison, Chl a, which has been traditionally used as a surrogate for measurements of GPP or NDM, performed well only when the percentage of diatoms in the epilithic algal community exceeded 75%. Our results also indicated that both the structure and function of benthic algal communities were sensitive to anthropogenic modifications, including riparian vegetation and forest cover in the catchment in river ecosystems.

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References

  • Abal, E. G., S. E. Bunn & W. C. Dennison, 2005. Healthy waterways healthy catchments: making the connection in South East Queensland, Australia. Moreton Bay Waterways and Catchments Partnership Brisbane: 240.

  • APHA, 1998. Standard methods for the examination of water and wastewater, 20th edition. American Public Health Association, Washington, DC.

  • Armston, J. D., R. J. Denham, T. J. Danaher, P. F. Scarth & T. N. Moffiet, 2009. Prediction and validation of foliage projective cover from Landsat-5 TM and Landsat-7 ETM+ imagery. Journal of Applied Remote Sensing 3: 33540–33528.

    Article  Google Scholar 

  • Bernot, M. J., D. J. Sobota, J. R. O. Hall, P. J. Mulholland, W. K. Dodds & J. R. Webster, 2010. Inter-regional comparison of land-use effects on stream metabolism. Freshwater Biology 55: 1874–1890.

    Article  Google Scholar 

  • Biggs, B.J.F., 1995. The contribution of flood disturbance, catchment geology and land-use to the habitat template of periphyton in stream ecosystems. Freshwater Biology 33(3): 419–438.

    Article  Google Scholar 

  • Biggs, B. J. F. & C. Kilroy, 2000. Periphyton Monitoring Manual: The New Zealand Ministry for the Environment. NIWA, Christchurch.

    Google Scholar 

  • Borchardt, M. A., 1996. Nutrients. In Stevenson, R. J., M. L. Bothwell & R. X. Lowe (eds) Algal Ecology Freshwater Benthic Ecosystem. Academic Press, Cambridge, 206–218.

    Google Scholar 

  • Bott, T. L., J. T. Brock, C. S. Dunn, R. J. Naiman, R. W. Ovink & R. C. Petersen, 1985. Benthic community metabolism in 4 temperate stream systems: an inter-biome comparison and evaluation of the River Continuum Concept. Hydrobiologia 123: 3–45.

    Article  Google Scholar 

  • Brett, M. T., S. E. Bunn & S. Chandra, 2017. How important are terrestrial organic carbon inputs for secondary production in freshwater ecosystems? Freshwater Biology 62: 833–853.

    Article  CAS  Google Scholar 

  • Bunn, S. E., P. M. Davies & T. D. Mosisch, 1999. Ecosystem measures of river health and their response to riparian and catchment degradation. Freshwater Biology 41: 333–345.

    Article  Google Scholar 

  • Bunn, S. E., E. G. Abal, M. J. Smith, S. C. Choy, C. S. Fellows, B. D. Harch, M. J. Kennard & F. Sheldon, 2010. Integration of science and monitoring of river ecosystem health to guide investments in catchment protection and rehabilitation. Freshwater Biology 55: 223–240.

    Article  Google Scholar 

  • Catterall, C. P. & M. Kingston, 1993. Remnant Bushland of South East Queensland in the 1990’s: Its Distribution, Loss, Ecological Consequences and Future Prospects. Institute of Applied Environmental Research, Griffith University and Brisbane City Council, Brisbane.

    Google Scholar 

  • Clapcott, J. E., R. G. Young, E. O. Goodwin & J. R. Leathwick, 2010. Exploring the response of functional indicators of stream health to land-use gradients. Freshwater Biology 55: 2181–2199.

    Article  Google Scholar 

  • Cross, W. F., J. M. Hood, J. P. Benstead, A. D. Huryn & D. Nelson, 2015. Interactions between temperature and nutrients across levels of ecological organization. Global Change Biology 21: 1025–1040.

    Article  PubMed  Google Scholar 

  • Davies, P. M., S. E. Bunn & S. K. Hamilton, 2008. Primary production in tropical streams and rivers. In: D. Dudgeon (ed) Tropical Stream Ecology. Academic Press, San Diego, 23.

    Chapter  Google Scholar 

  • DNRM. 2008. Monitoring Standard for Freshwater Blue Green Alage (Cyanobacteria). Department of Natural Resources and Mines, Queensland Government: 22.

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

    Article  Google Scholar 

  • Dodds, W. K. & B. J. F. Biggs, 2002. Water velocity attenuation by stream periphyton and macrophytes in relation to growth form and architecture. Journal of the North American Benthological Society 21: 2–15.

    Article  Google Scholar 

  • Dodds, W. K. & J. Brock, 2010. A portable flow chamber for in situ determination of benthic metabolism. Freshwater Biology 39: 49–59.

    Article  Google Scholar 

  • Englund, G., B. Malmqvist & Y. Zhang. 1997. Using predictive models to estimate effects of flow regulation on net-spinning caddis larve in North Swedish rivers. Freshwater Biology 37: 687–697.

    Article  Google Scholar 

  • Entwisle, T. J., J. A. Sonneman & S. H. Lewis, 1997. Freshwater Algae in Australia: A Guide to Conspicuous Genera. Sainty and Associates, Sydney.

    Google Scholar 

  • Fellows, C. S., J. E. Clapcott, J. W. Udy, S. E. Bunn, B. D. Harch, M. J. Smith & P. M Davies, 2006. Benthic metabolism as an indicator of stream ecosystem health. Hydrobiologia 572: 71–87.

    Article  Google Scholar 

  • Foged, N., 1978. Diatoms in Eastern Australia. Bibliotheca Phycologica, 41. J. Cramer, Vaduz: 1–243.

  • Garcia, E. A., N. E. Pettit, D. M. Warfe, P. M. Davies, P. M. Kyne, P. Novak & M. M. Douglas, 2015. Temporal variation in benthic primary production in streams of the Australian wet-dry tropics. Hydrobiologia 760: 43–55.

    Article  Google Scholar 

  • Gell, P., J. Sonneman, M. Reid, M. Illman & A. Sincock, 1999. An illustrated key to common diatom genera from southern Australia. The Murray-Darling Freshwater Research Centre Identification Guide. No. 26.

  • Grace, J. B., 2006. Structural Equation Modeling and Natural Systems, Cambridge Univ. Press, New York.

    Book  Google Scholar 

  • Hosomi, M. & R. Sudo, 1986. Simultaneous determination of total nitrogen and total phosphorus in freshwater samples using persulfate digestion. International Journal of Environmental Studies 27: 167–275.

    Article  Google Scholar 

  • Hötzel, G. & R.Croome, 1999. A Phytoplankton Methods Manual for Australian Freshwaters. LWRRDC Occasional Paper 22/99, Canberra.

  • Hou, E., C. Chen, Y. Kuang, Y. Zhang, M. Heenan & D. Wen, 2016. A structural equation model analysis of phosphorus transformations in global unfertilized and uncultivated soils. Global Biogeochemical Cycles 30:1300–1309.

    Article  CAS  Google Scholar 

  • Houser, J. N., L. A. Bartsch, W. B. Richardson , J. T. Rogala & J. F. Sullivan, 2015. Ecosystem metabolism and nutrient dynamics in the main channel and backwaters of the Upper Mississippi River. Freshwater Biology 60: 1863–1879.

    Article  CAS  Google Scholar 

  • Hudon, C. & E. Bourget, 1983. The effect of light on the vertical structure of epibenthic diatom communities. Botanica Marina 26: 317–330.

    Article  Google Scholar 

  • Hunt, R. J., T. D. Jardine, S. K. Hamilton & S. E. Bunn, 2012. Temporal and spatial variation in ecosystem metabolism and food web carbon transfer in a wet-dry tropical river. Freshwater Biology 57: 435–450.

    Article  CAS  Google Scholar 

  • Jeffrey, S. W. & N. A. Welshmeyer, 1997. Spectrophotometric and fluorometric equations in common use in oceanography. In Jeffrey, S.W., R. F. C. Mantoura & S. W. Wright (eds) Phytoplankton Pigments in Oceanography, Monographs on Oceanographic Methodology. vol. 10, UNESCO Publishing, Paris, 597–615.

    Google Scholar 

  • John, J., 1983. The diatom flora of the Swan River Estuary Western Australia. J. Cramer in der A.-R.-Gantner-Verlag-Kommanditgesellschaft.

  • Kendrick, M.R. & A. D. Huryn, 2015. Discharge, legacy effects and nutrient availability as determinants of temporal patterns in biofilm metabolism and accrual in an arctic river. Freshwater Biology 60: 2323–2336.

    Article  CAS  Google Scholar 

  • Kennard, M. J., B. J. Pusey, A. H. Arthington, B. D. Harch & S. J. Mackay, 2006. Development and application of a predictive model of freshwater fish assemblage composition to evaluate river health in eastern Australia. Hydrobiologia 572: 33–57.

    Article  Google Scholar 

  • Kennard, M. J., B. J. Pusey, J. D. Olden, S. J. Mackay, J. L. Stein & N. Marsh, 2010. Classification of natural flow regimes in Australia to support environmental flow management. Freshwater Biology 55: 171–193.

    Article  Google Scholar 

  • Kerr, J. G., M. Burford, J. Olley & J. Udy, 2011. Phosphorus sorption in soils and sediments: implications for phosphate supply to a subtropical river in southeast Queensland, Australia. Biogeochemistry 102: 73–85.

    Article  CAS  Google Scholar 

  • Krammer, K. 2002. Cymbella. In H. Lange-Bertalot (Ed.), Diatoms of Europe. Ruggell, Germany: Gantner.

  • Krammer, K., H. Lange-Bertalot, 1986. Bacillariophyceae 1. Teil, Naviculaceae. In Ettl H., J. Gerloff, H. Heynig & D. Mollenhauer (eds) ´Süßwass erflora von Mitteleuropa´. Gustav Fischer Verlag, Stuttgart.

    Google Scholar 

  • Krammer, K. & H.Lange-Bertalot, 1991b. Bacillariophyceae 4. Teil, Achnanthaceae, Kritische Ergänzungen zu Navicula (Lineolatae) und Gomphonema, Gesamtliteraturverzeichnis Teil 1-4. In Ettl H., G. Gärtner, J. Gerloff, H. Heynig & D. Mollenhauer (eds) ´Süßwasserflora von Mitteleuropa.´ Gustav Fischer Verlag, Stuttgart.

    Google Scholar 

  • Krammer, K. & H.Lange-Bertalot, 1991a. Bacillariophyceae 3. Teil, Centrales, Fragilariaceae, Eunotiaceae. In Ettl H., G. Gärtner, J. Gerloff, H. Heynig & D. Mollenhauer (eds) ´Süßwasserflora von Mitteleuropa´. Gustav Fischer Verlag: Stuttgart.

    Google Scholar 

  • Langdon, C., 1988. On the causes of interspecific differences in the growth-irradiance relationship for phytoplankton. II: a general review. Journal of Plankton Research 10: 1291–1312.

    Article  Google Scholar 

  • Leland, H. V., 1995. Distribution of phytobenthos in the Yakima River basin, Washington, in relation to geology, land use, and other environmental factors. Canadian Journal of Fisheries and Aquatic Sciences 52: 1108–1129.

    Article  Google Scholar 

  • Leland, H. V. & S. D. Porter, 2000. Distribution of benthic algae in the upper Illinois River basin in relation to geology and land use. Freshwater Biology 44: 279–301.

    Article  Google Scholar 

  • Lewis, A. S., B. S. Kim, H. L. Edwards, H. L Wander, C. M. Garfield, & H. E. Murphy, 2020. Prevalence of phytoplankton limitation by both nitrogen and phosphorus related to nutrient stoichiometry, land use, and primary producer biomass across the northeastern United States. Inland Waters 10: 42–50.

    Article  CAS  Google Scholar 

  • Lovett, G. M., J. J. Cole & M. L. Pace, 2006. Is net ecosystem production equal to ecosystem carbon accumulation? Ecosystems 9: 1–4.

    Article  CAS  Google Scholar 

  • Reference Manual for the ETo Calculator (Evapotranspiration from a reference surface), 2009. Food and Agriculture Organization of the United Nations Land and Water Division; FAO, Via delle Terme di Caracalla, 00153 Rome, Italy (Version 3.1, January 2009).

  • Mosisch, T. D., S. E. Bunn & P. M, Davies, 2001. The relative importance of shading and nutrients on algal production in subtropical streams. Freshwater Biology 46: 1269−1278.

    Article  Google Scholar 

  • Muhid, P., T. W. Davis, S. E. Bunn & M. A. Burford, 2013. Effects of inorganic nutrients in recycled water on freshwater phytoplankton biomass and composition. Water Research 47: 384–394.

    Article  CAS  PubMed  Google Scholar 

  • Nelson, C. E. , D. M. Bennett & B. J. Cardinale, 2013. Consistency and sensitivity of stream periphyton community structural and functional responses to nutrient enrichment. Ecological Applications 23(1): 159–173.

    Article  PubMed  Google Scholar 

  • Palmer, M. A., E. S. Bernhardt, J. D. Allan, P. S. Lake, G. Alexander, S. Brooks, J. Carr, S. Clayton, C. N. Dahm, J. Follstad Shah, D. L. Galat, S. G. Loss, P. Goodwin, D. D. Hart , B. Hassett, R. Jenkinson, G. M. Kondolf, R. Lave, J. L. Meyer, T. K. O’donnell, L. Pagano & E. Sudduth, 2005. Standards for ecologically successful river restoration. Journal of Applied Ecology 42(2): 208–217.

    Article  Google Scholar 

  • Peterson, E. E., F. Sheldon, & R. Darnell, 2011. A comparison of spatially explicit landscape representation methods and their relationship to stream condition. Freshwater Biology 56(3): 590–610.

    Article  Google Scholar 

  • Pielou, E. C., 1966. The measurement of diversity in different types of biological collections. Journal of Theoretical Biology 13: 131–144.

    Article  Google Scholar 

  • Potapova, M. G. & F. D. Charles, 2003. Distribution of benthic diatoms in U. S. rivers in relation to conductivity and ionic composition. Freshwater Biology 48: 1311–1328.

    Article  CAS  Google Scholar 

  • Prygiel, J. & M. Coste, 2000. Guide méthodologique pour la mise en oeuvre de l’Indice Biologique Diatomées NF T 90-354. Agences de l’Eau-Cemagref-Groupement de Bordeaux. Agences de l’Eau, Mars.

  • Rapport, D. J., R. Costanza & A. J. McMichael, 1998. Assessing ecosystem health. Trends in Ecology and Evolution 13: 397–402.

    Article  CAS  PubMed  Google Scholar 

  • Romero-Martínez, L., M. Morales-Pineda, B. Úbeda, S. A. Loiselle, A. Cózar & J. A. Gálvez, 2013. Planktonic community metabolism in two stratified Mediterranean reservoirs with different trophic status. Aquatic Ecosystem Health and Management 16(2): 183–189.

    Article  Google Scholar 

  • Rovelli, L., K. M. Attard, A. Binley, C. M. Heppell, H. Stahl, M. Trimmer& Glud R. N., 2017. Reach-scale river metabolism acroos contrasting sub-catchment geologies: effect of light and hydrology. Limnology and Oceanography 62 (Suppl Suppl 1):S381–399.

    Article  PubMed  PubMed Central  Google Scholar 

  • Shannon, C. E., W. Weaver, 1949. The Mathematical Theory of Communication. University of Illinois Press, Urbana, Illinois.

    Google Scholar 

  • Siders, A.C., D. M. Larson, J. Rüegg & W. Dodds, 2017. Probing whole-stream metabolism: influence of spatial heterogeneity on rate estimates. Freshwater Biology 62: 711–723.

    Article  Google Scholar 

  • Silva, C., M. Mattioli, E. Fabbri, E. Yáñez, T. A. DelValls & M. L.Martín- Díaz, 2012. Benthic community structure and biomarker responses of the clam Scrobicularia plana in a shallow tidal creek affected by fish farm effluents (Rio San Pedra, SW Spain). Environment International 47: 86–98.

    Article  CAS  PubMed  Google Scholar 

  • Sonneman, J., A. Sincock, J. Fluin, M. Reid, P. Newal, J. Tibby & P. Gell. 2000. An illustrated guide to common stream diatom species from temperate Australia. The Murray-Darling Freshwater Research Centre Identification Guide No. 33.

  • Stevenson, R. J., 1996. An Introduction to algal ecology in freshwater benthic habitats. In Stevenson, R. J., M. L. Bothwell & R. X. Lowe (eds) Algal Ecology Freshwater Benthic Ecosystem. Academic press, Cambridge.

    Google Scholar 

  • Stevenson, R.J. 2014. Ecological assessments with algae: a review and synthesis. Journal of Phycology 50: 437–461.

    Article  PubMed  Google Scholar 

  • Tan, X., F. Sheldon, S. E. Bunn & Q. Zhang, 2013. Using diatom indices for water quality assessment in a subtropical river, China. Environment Science and Pollution Research 20(6), 4164–4175.

    Article  CAS  Google Scholar 

  • Tan, X., P. Ma, X. Xia & Q. Zhang, 2014a. Spatial pattern of benthic diatoms and water quality assessment using diatom indices in a subtropical river, China. Clean-Soil, Air, Water 42: 20–28.

    Article  CAS  Google Scholar 

  • Tan, X., X. Xia, Q. Zhao & Q. Zhang, 2014b. Temporal variations of benthic diatom community and its main influencing factors in a subtropical river, China. Environmental Science and Pollution Research 21: 434–444.

    Article  PubMed  Google Scholar 

  • Tan, X., P. Ma , S.E. Bunn & Q. Zhang, 2015. Development of a benthic diatom index of biotic integrity (BD-IBI) for ecosystem health assessment of human dominant subtropical rivers, China. Journal of Environmental Management 151: 286–294.

    Article  PubMed  Google Scholar 

  • Tan, X., 2015. Environmental influences on benthic algal communities and their application for biomonitoring of Australian and Chinese Rivers. Ph D Dissertation. Griffith University.

  • Turunen, J., J. Markkula, M, Rajakallio & J. Aroviita, 2019. Riparian forests mitigate harmful ecological effects of agriculture diffuse pollution in medium-sized streams. Science of the Total Environment 649: 495–503.

    Article  CAS  PubMed  Google Scholar 

  • Wang, Y., R. J. Stevenson & L. Metzmeier, 2005. Development and evaluation of a diatom-based Index of Biotic Integrity for the Interior Plateau Ecoregion, USA. Journal of North American Benthological Society 24(4): 990–1008.

    Article  Google Scholar 

  • Weilhoefer, C. L. & Y. D. Pan, 2006. Diatom assemblages and their associations with environmental variables in Oregon Coast Range streams, USA. Hydrobiologia 561: 207–219.

    Article  CAS  Google Scholar 

  • Winter, J. G. & H. C. Duthie, 2000. Epilithic diatoms as indicators of stream total N and total P concentration. Journal of North American Benthological Society. 19(1), 32–49.

    Article  Google Scholar 

  • Yates, A. G., R. B. Brua, J. M. Culp & P. A. Chambers, 2013. Multi-scaled drivers of rural prairie stream metabolism along human activity gradients. Freshwater Biology 58: 675–689.

    Article  CAS  Google Scholar 

  • Yates, A. G., R. B. Brua, J. M. Culp, R. G. Young & P. A. Chambers, 2017. Variation in stream metabolism and benthic invertebrate composition along longitudinal profiles of two contrasting river systems. Canadian Journal of Fisheries and Aquatic Sciences 75: 549–559.

    Article  Google Scholar 

  • Ye, L., Q. Cai, M. Zhang, L. Tan & H. Shen, 2016. Ecosystem metabolism and the driving factors in Xiangxi Bay of Three Gorges Reservoir, China. Freshwater Science 35: 826–833.

    Article  Google Scholar 

  • Young, R. G. & K. J. Collier, 2009. Contrasting responses to catchment modification among a range of functional and structural indicators of river ecosystem health. Freshwater Biology 54: 2155–2170.

    Article  CAS  Google Scholar 

  • Young, R. G., A. D. Huryn, 1999. Effects of land use on stream metabolism and organic matter turnover. Ecological Applications 9(4): 1359–1376.

    Article  Google Scholar 

  • Zhang, J., X. Shu, Y. Zhang, X. Tan, Q. Zhang, 2020. The responses of epilithic algal community structure and function to light and nutrients and their lingkages in subtropical rivers. Hydrobiologia 847: 841–855.

    Article  CAS  Google Scholar 

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Acknowledgements

We thank Dr. Douglas Ward and Mr. Kenn Tews at Australian Rivers Institute, Griffith University and Dr. Dezhi Wang at Wuhan Botanical Garden, CAS for their assistance with land-use analysis and plotting. We appreciate the help from Mr. Dominic Valdez, Ms. Ann Chuang, Ms. Carolyn Polson, and Dr. Wingying Tsoi at the Australian Rivers Institute, Griffith University, with water quality analysis and sampling in the field. We thank Dr. Yulong Zhang at the University of North Carolina at Chapel Hill for the potential radiation analysis and Dr. Xingzhong Wang at the Huzhou University, P.R. China for help with data analysis. We also thank Mr. Russell Doughty at the California Institute of Technology (Caltech) for editing the manuscript.

Funding

The research was supported by the National Natural Science Foundation of China (No. 31720103905) and a postgraduate scholarship from Griffith University, Griffith School of Environment, ARI 1011-AXTSB.

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XT and SB conceived and designed the experiment. XT and EH did the data analysis and XT drafted the original manuscript. QZ revised the manuscript and provided very constructive comments.

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Tan, X., Hou, E., Zhang, Q. et al. Benthic metabolism responses to environmental attributes at multiple scales and its linkage to algal community structure in streams. Hydrobiologia 848, 5067–5085 (2021). https://doi.org/10.1007/s10750-021-04693-9

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