Abstract
Excessive nutrient loading of water bodies is a leading cause of water pollution worldwide1,2, and controlling nutrient levels in watersheds is a primary objective of most environmental policy3. Over the past two decades, much research has shown that ecosystems with more species are more efficient at removing nutrients from soil and water than are ecosystems with fewer species4,5,6,7. This has led some to suggest that conservation of biodiversity might be a useful tool for managing nutrient uptake and storage7,8,9,10, but this suggestion has been controversial, in part because the specific biological mechanisms by which species diversity influences nutrient uptake have not been identified10,11,12. Here I use a model system of stream biofilms to show that niche partitioning among species of algae can increase the uptake and storage of nitrate, a nutrient pollutant of global concern. I manipulated the number of species of algae growing in the biofilms of 150 stream mesocosms that had been set up to mimic the variety of flow habitats and disturbance regimes that are typical of natural streams. Nitrogen uptake rates, as measured by using 15N-labelled nitrate, increased linearly with species richness and were driven by niche differences among species. As different forms of algae came to dominate each unique habitat in a stream, the more diverse communities achieved a higher biomass and greater 15N uptake. When these niche opportunities were experimentally removed by making all of the habitats in a stream uniform, diversity did not influence nitrogen uptake, and biofilms collapsed to a single dominant species. These results provide direct evidence that communities with more species take greater advantage of the niche opportunities in an environment, and this allows diverse systems to capture a greater proportion of biologically available resources such as nitrogen. One implication is that biodiversity may help to buffer natural ecosystems against the ecological impacts of nutrient pollution.
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Acknowledgements
We thank J. Byrnes, W. Dodds, J. Levine and A. Steinman for comments that improved the manuscript. D. Bennett, K. Matulich, L. Power and J. Weis helped to set up and run the experiment. M. Potapova provided images of the algae in Fig. 2. This work was funded by grants from the US National Science Foundation (DEB 0614428 and DEB 1046121).
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B.J.C. designed the study, collected data with the assistance of those mentioned in the Acknowledgements, analysed the data and wrote the paper.
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Cardinale, B. Biodiversity improves water quality through niche partitioning. Nature 472, 86–89 (2011). https://doi.org/10.1038/nature09904
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DOI: https://doi.org/10.1038/nature09904
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Martin Doyle
Cardinale (2011) uses a series of microcosm experiments and shows that algal biodiversity may play an important role in improving water quality because of observed increases in nitrate retention with increasing number of algal species. The work represents a painstakingly thorough study that helps identify mechanisms of niche partitioning at the experimental scale in streams, and represents exciting ground for stream scientists. However, the lessons from this study for water quality must be considered very carefully based on what we now understand about watershed hydrology and biogeochemistry.
Many nutrient loads are primarily transported in streams during high flows. The nitrate retention observed by Cardinale was for baseflow conditions. While the effect of disturbance was simulated via physically scouring algal patches, the nitrate retention simulated was solely for uniform (per microcosm), steady flow, very low depth, uniform high light conditions. Such conditions occur during baseflow, when nutrient loads are often minimal. High nitrate loads tend to occur during floods, when algal nutrient retention is reduced either because of erosion, low light-high turbidity conditions, low temperature (spring/snow runoff), or simply high depth that dramatically reduces the potential for water-algae contact (1). Moreover, research from urban watersheds (2) and agricultural watersheds including the Mississippi River basin (3) show that increased watershed development is associated with increasing shifts in nitrate export toward higher discharge.
Thus, baseflow nitrate retention, as simulated by Cardinale, plays a more limited role than floods in affecting downstream water quality, particularly in developed areas. The results of Cardinale are likely most relevant for streams and rivers immediately downstream of point sources of pollution, such as wastewater treatment plants, which produce very steady and high nitrate loads under all flows, including baseflow. It is now important to understand if, and how, some of these mechanisms identified by Cardinale may influence nitrate dynamics under varying flow conditions, or if altogether different mechanisms may need to be understood.
(1) Doyle 2005. Journal of Geophysical Research, 110, G01003, doi:101.1029/2005JG00015.
(2) Shields et al., 2008. Water Resources Research, 44, W09416, doi:10.1029/2007WR006360.
(3) Royer et al., 2006. Environmental Science and Technology. 40(13), 4126-4131.
Martin W Doyle and Lawrence E Band
Department of Geography, University of North Carolina ? Chapel Hill
Correspondence to mwdoyle@email.unc.edu; 919-962-3876
Bradley Cardinale
My colleague Martin Doyle raises several good points in his comment that are well-worth attention in future research efforts. There has long been a debate in ecology about whether the properties of communities and ecosystems, as well as the processes performed by communities within ecosystems, are more influenced by large periodic events, or by biological interactions that are presumed to be strongest in the interval between events [1, 2]. In the broader field, this topic has manifest itself as a debate over the importance of equilibrium verses non-equilibrium dynamics in ecosystems <sup class="footnote">3</sup>, the role of harsh vs. benign conditions in establishing the structure and function of communities <sup class="footnote">4</sup>, and others. Within the field of stream ecology, the debate has primarily focused on the relative importance of periodic floods in controlling stream biodiversity and nutrient dynamics, verses the role of biological interactions in controlling diversity and nutrient dynamics between floods [5, 6].
Doyle?s comment revisits this debate within the context of factors that control nitrogen dynamics within streams. He has proposed that long-term nutrient retention in streams is more influenced by hydrologic forces like floods, than it is by biological dynamics like niche partitioning than influence assimilation. After citing references that emphasize the role of hydrology in nutrient dynamics, he goes on to summarize by saying ?Thus, baseflow nitrate retention, as simulated by Cardinale, plays a more limited role than floods in affecting downstream water quality, particularly in developed areas.?
I tend to disagree with Doyle?s summary sentence because he makes it sound as if we already have quantified, and know for sure that hydrology is more important than biology in driving N-dynamics. I do not believe this is a statement that can be backed by solid evidence at this point in time. To the best of my knowledge, we do not yet have any direct quantitative comparisons of the relative importance of abiotic factors like floods vs. biotic factors like niche partitioning to the long-term nitrogen budget of streams. On the other hand, I think Doyle has raised a valuable and testable hypothesis that the impacts of biodiversity on N-assimilation contribute significantly less to the long-term retention of nitrogen in a stream than do periodic floods.
Doyle?s hypothesis is a potentially valuable new direction for researchers working in streams, as well as for those working on biodiversity in general. We now have more than 400 experiments that have manipulated the diversity of plants, animals, fungi and bacteria in ecosystems around the globe. Of the 59 experiments that have examined how biodiversity impacts NO3-, 51 have shown that diverse communities reduce nitrate concentrations in soil or water by a mean 48%. We have unequivocal evidence that diversity effects on NO3- are significant. The question now is ? are those effects large or trivial compared to other controls on nutrient dynamics?
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Adriano Caliman
Cardinale?s paper gives a large contribution to the accumulating body of knowledge about how species diversity affects ecosystem processes. Although I completely agree with most of the interpretations provided by the author, I am somewhat skeptical to the Cardinale?s conclusion regarding the improvement of water quality by algae species diversity. Specifically, my concerns are related to the fact that Cardinale?s study was based only on a specific response variable (NO3-removal). It is well established that phosphorus and other forms of inorganic nitrogen (e.g. ammonium NH4+) contribute largely to the eutrophication processes of freshwater systems1. In fact, phosphorus is credited to be the primary precursor of eutrophication of freshwater systems and because NH4+ is the primary metabolic by-product of most metazoans and the main substrate to NO3- production via microbial-mediated nitrification, its concentration in aquatic systems is on average much larger than NO3- itself. Finally, because NH4+ absorption is biochemistrily cheaper than NO3-, which needs to be primarily processed by enzymes (nitrate reductase) before it is ready to be used in cell growth, NH4+ is the preferential and readily absorbed form of inorganic nitrogen by most of freshwater primary producers including benthic algae.
From the above, one can conclude that while the results of Cardinale?s study add lots to our knowledge about the specific mechanisms through which species rich communities are more efficient in sequester available resources, it is supposedly to have less impact on questions regarding water quality, because the conclusions of the study are based only on NO3- removal, a process which is of lesser importance to the eutrophication processes than phosphorus and/or NH4 removal. It also raises question if Cardinale?s conclusions are biased to a specific ecosystem variable or are consistent over several nutrient forms which both represent a variety of important resources in fueling primary production and in promote the degradation of aquatic ecosystems worldwide. The multifunctional effects of algae biodiversity2 on the removal of multiple nutrients that are directly linked to eutrophication should be the preferred method to test the significance of biodiversity to water quality.
1	Elser, J. J. et al. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecology Letters 10, 1135-1142 (2007).
2	Hector, A. & Bagchi, R. Biodiversity and ecosystem multifunctionality. Nature 448, 188-191 (2007).
Bradley Cardinale
My colleague Adriano Caliman makes a good point that multiple nutrients (nitrate, ammonium, phosphate) have been implicated as drivers of eutrophication, and the decline water quality worldwide. He them outlines skepticism of the conclusions of my paper (that biodiversity enhances water quality) because my experiment focused on only one of the nutrients responsible for water quality (nitrate).
It is correct that my study focused on just one aspect of water quality, and I agree with Caliman that it would be worthwhile to extend the research to examine other nutrient pollutants as well. But I would argue that the biological principles that influenced nitrate assimilation in my study are likely to hold for other forms of nutrient pollution as well. The key mechanism that enhanced nitrate uptake and assimilation in my experiment was niche partitioning whereby different species dominated different habitats of the stream environment. While some species dominated low flow environments others dominated high flow environments. While some species were specialized for colonizing recently disturbed habitats, others dominated undisturbed habitats. These forms of niche partitioning allowed a diverse community to achieve greater total biomass in a stream than any single species could alone.
When assimilation is proportional to biomass (as it was in my study), then I would hypothesize that algal diversity should enhance uptake of any biologically essential nutrient. I do not doubt that the dynamics of uptake and assimilation are likely to differ among nutrient forms (see Caliman's distinction about the efficiency of uptake of NO3- vs. NH4+). But I do not agree with the statement that my study has "? less impact on questions regarding water quality, because the conclusions of the study are based only on NO3- removal." This statement ignores the general ecological mechanisms that influence nutrient uptake by a community.