The spatial and temporal patterns of nitrogen fixation and denitrification in aquatic habitats

A problematic, long-held assumption is that nitrogen fixation rates are negligible, and therefore not worth quantifying, in riverine ecosystems. This assumption is in direct contradiction to studies in marine, estuarine and lake ecosystems demonstrating that nitrogen fixation co-occurs with denitrification across a range of reactive nitrogen inputs, and that together these two processes control the N2 fluxes from these aquatic ecosystems. In 2015 I received an NSF CAREER award to test the hypothesis that hot spots and hot moments could allow the co-existence of nitrogen fixation and denitrification in streams and rivers across gradients of reactive nitrogen concentrations. Over the past five years, we have conducted a field study of 30 streams in 13 ecoregions to conduct simultaneous measurements of nitrogen fixation, denitrification, and N2 flux. PhD students Erin Eberhard, Kevin Nevorski, and Michelle Kelly are working in diverse projects characterizing the taxonomic and functional diversity of microbial assemblages across the study streams, quantifying the daily and seasonal variability in N transformation rates in relation to hydrologic variability in a north temperate river, and integrating denitrification into stream carbon and energy budgets through empirical and modeling studies. Over the next five years, I will continue to synthesize understanding of nitrogen fixation across aquatic habitats as a co-leader of the recently NSF funded Aquatic Nitrogen Fixation Research Coordination Network (ANF-RCN) 

Related Publications:

Eberhard EK, Marcarelli AM, Baxter CV. 2018. Co-occurrence of in-stream nitrogen fixation and denitrification across a nitrogen gradient in a western U.S. watershed. Biogeochemistry 139:179-195. 

Dodds WK, Burgin AJ, Marcarelli AM, Strauss EA. 2017. Nitrogen Transformations. Pp 173-196 in: Lamberti GA, Hauer FR (eds) Methods in Stream Ecology Volume 2: Ecosystem Function, 3rd Edition. Elsevier.

Scott JT, and Marcarelli AM. 2012. Cyanobacteria in freshwater benthic environments.  Pp 271-289 in: Whitton BA (ed) Ecology of the Cyanobacteria II: Their Diversity in Time and Space. Springer.

Marcarelli AM, and Wurtsbaugh WA. 2009. Habitat and seasonal variations in nitrogen fixation in linked stream-lake ecosystems. Biogeochemistry 94:95-110. DOI: 10.1007/s10533-009-9311-2

Marcarelli AM, Baker MA, and Wurtsbaugh WA. 2008. Is in-stream nitrogen fixation an important nitrogen source for benthic communities and stream ecosystems? Journal of the North American Benthological Society 27:186-211.

Marcarelli AM, and Wurtsbaugh WA. 2007. Effects of upstream lakes and nutrient limitation on periphytic biomass and nitrogen fixation in oligotrophic, subalpine streams. Freshwater Biology 52:2211-2225.

Marcarelli AM, and Wurtsbaugh WA. 2006. Temperature and nutrient supply interact to control nitrogen fixation in oligotrophic streams: an experimental examination. Limnology and Oceanography 51:2278-2289.

Stream-watershed-lake interactions in the Great Lakes

The Great Lakes have thousands of small to large tributary streams whose contributions and processes are poorly understood and constrained, leading to large uncertainties in the whole-lake nutrient budgets. We have been working to advance understanding of Lake Superior’s 2,800 tributaries through four different lines of inquiry. First, to understand the extent to which in-stream processing may modify nutrient delivery to the nearshore region of Lake Superior and led by Dr. Ashley Coble (PhD 2015), we have been conducting studies of nutrient retention and uptake, dissolved organic matter composition and decomposition, and long-term trends in nutrient and organic matter export from monitored watersheds. Second, PhD student Erin Eberhard is studying how variable environmental conditions control N retention and export at coastal wetland complexes where streams, wetlands and nearshore environments meet as a 2020-2021 Graduate Fellow with Michigan Sea Grant. Third, led by Dr. Chris Adams, we are studying how, when and why migratory salmonids move between tributary and lake habitat as part of their life history strategies. Fourth, we are developing novel methods to quantify the volume and timing of tributary export using autonomous aerial and underwater vehicles to remotely sense tributary water as it forms plumes in the nearshore of Lake Superior. I also worked with the Michigan Tech Forward initiative to establish a partnership to maintain a USGS gauge on the Pilgrim River near Michigan Tech, securing a long-term monitoring site that is essential for this research program and also important for resilient community planning as summer storm and flood frequency increases due to climate change. 

Related Publications:

Meingast KM, Kane ES, Coble AA, Marcarelli AM, Toczydlowski D. Accepted. Climate, snowmelt dynamics and atmospheric deposition interact to control dissolved organic carbon export from a northern forest stream over 26 years. Environmental Research Letters.

Coble AA, Marcarelli AM, Kane ES. 2019. Year-round measurements reveal seasonal drivers of nutrient uptake in a snowmelt-driven headwater stream. Freshwater Science 38:156-169. 

Marcarelli AMCoble AA, Meingast KM, Kane ES, Brooks CN, Buffam I, Green SA, Huckins CJ, Toczydlowski D, Stottlemyer R. 2019. Of small streams and Great Lakes: Integrating tributaries to understand the ecology and biogeochemistry of Lake Superior. Journal of the American Water Resources Association 55:442-458. 

Coble AA, Marcarelli AM, Kane ES, Huckins CJ. 2016. Uptake of ammonium and soluble reactive phosphorus in forested streams: influence of dissolved organic matter composition. Biogeochemistry 131:355-372. DOI: 10.1007/s10533-016-0284-7

Baker MA, Arp CD, Goodman KJ, Marcarelli AM, Wurtsbaugh WA. 2016. Stream-lake interaction: understanding a coupled hydro-ecological system. Pp 321-348 in: Jones JB, Stanley EH (eds) Streams in a Changing Environment. Academic Press.

Coble AA, Marcarelli AM, Kane ES. 2015. Ammonium and glucose amendments stimulate dissolved organic matter mineralization in a Lake Superior tributary. Journal of Great Lakes Research 41:801–807DOI:10.1016/j.jglr.2015.05.015

Consequences of restoration for stream and lake ecosystem processes

Restoration activities are widespread in aquatic habitats and provide opportunities to ask both basic research questions about how ecosystems respond to perturbations as well as applied research about the efficacy of restoration efforts. In the past five years and with funding from two awards through the Great Lakes Restoration Initiative and one through the Michigan Invasive Species Program, our lab has collaborated with many others at Michigan Tech to understand how active management of Eurasian Watermilfoil, an invasive aquatic macrophyte, may alter nutrient cycling and the structure of primary producer communities in lake littoral zones, as well as how to better plan management strategies using novel monitoring and management tools. Led by Dr. Kevyn Juneau (Post-doc 2014-2015), we conducted a series of monitoring experiments to understand whether common treatments for this invasive plant (herbicide application, harvesting, enhancing native herbivores) may have off-target effects on native plants. Dr. Colin Brooks led development of novel tools for identifying and monitoring the spatial coverage of Eurasian Watermilfoil in mixed macrophyte assemblages using unmanned aerial vehicles. We also used these restoration projects as an opportunity to ask basic ecological questions. Undergraduate student Jade Ortiz conducted a mesocosm experiment to ask how Eurasian Watermilfoil and nutrients interact to alter algal assemblages with funding from Michigan Tech’s Summer Undergraduate Research Fellowship program. Ryan Van Goethem started as an undergraduate studying macrophyte assemblages in relation to sediment properties in the Keweenaw Waterway, then studied how presence of Eurasian Watermilfoil alters primary production in littoral zones of north-temperate inland lakes. Prior restoration projects included studies of culvert effects on stream ecosystem processes in Northwood streams, and nutrient mitigation strategies in Colombia River streams.

Related Publications:

Van Goethem RR, Huckins CJ, Marcarelli AM. 2020. Effects of invasive watermilfoil on primary production in littoral zones of north-temperate lakes. Diversity 12:82.

Brooks CN, Grimm AG, Marcarelli AM, Dobson RJ. 2019. Multiscale collection and analysis of submerged aquatic vegetation spectral profiles for Eurasian watermilfoil detection. Journal of Applied Remote Sensing 13:037501.

Ortiz JE, Marcarelli AM, Juneau KJ, Huckins CJ. 2019. Invasive Myriophyllum spicatum and nutrients interact to influence algal assemblages. Aquatic Botany 156:1-9. 

Olson JC, Marcarelli AM, Timm AL, Eggert SL, Kolka RK. 2017. Evaluating the effects of culvert designs on ecosystem processes in northern Wisconsin streams. River Research and Applications 33:777–787 

Collins SF, Baxter CV, Marcarelli AM, Wipfli MS. 2016. Effects of experimentally added salmon subsidies on resident fishes via direct and indirect pathways. Ecosphere 7:e01248DOI:10.1002/ecs2.1248

Marcarelli AM, Huckins CJ, Eggert SL. 2015. Sand aggradation alters biofilm standing crop and metabolism in a low-gradient Lake Superior tributary. Journal of Great Lakes Research 41:1052-1059. DOI:10.1016/j.jglr.2015.09.004

Collins SF, Marcarelli AM, Baxter CV, Wipfli MS. 2015. A critical assessment of the ecological assumptions underpinning compensatory mitigation of salmon-derived nutrients. Environmental Management 56:571-586. DOI: 10.1007/s00267-015-0538-5

Ebel JD, Marcarelli AM, Kohler AE. 2014. Biofilm nutrient limitation, standing crop, and metabolism responses to experimental application of salmon carcass analog in Idaho streams. Canadian Journal of Fisheries and Aquatic Sciences 71:1796-1804. DOI: 10.1139/cjfas-2014-0266

Marcarelli AM, Baxter CV, and Wipfli MS. 2014. Nutrient additions to mitigate for loss of Pacific salmon: consequences for stream biofilm and nutrient dynamics. Ecosphere 5:69. DOI: 10.1890/ES13-00366.1

Mineau MM, Baxter CV, and Marcarelli AM. 2011. A non-native riparian tree (Elaeagnus angustifolia) changes nutrient dynamics in streams. Ecosystems 14:353-365.

Hopkins JH, Marcarelli AM, and Bechtold HA. 2011. Ecosystem structure and function are complementary measures of water quality in a polluted, spring-influenced river. Water, Air and Soil Pollution 214:409-421.  DOI: 10.1007/s11270-010-0432-y

Ecosystem perspectives on community interactions and resource subsidies

I have a continuing interest in combining approaches from ecosystem and community ecology to understand the complicated networks of direct and indirect interactions that characterize biological assemblages and that extend across habitat boundaries. In a recent contribution published in Ecology, I led an ecosystem-level reanalysis of pioneering datasets collected at Horonai Stream, a forested, spring-fed stream in Hokkaido, Japan to demonstrate that the direction of indirect and direct interactions can change depending on the timescale of observation. This international collaboration was partially supported by the Japan Society for the Promotion of Science and included 3 Japanese co-authors, including Shigeru Nakano, who tragically died at sea twenty years ago. We are also continuing to study the role of terrestrial vs. aquatic-derived organic matter for supporting the energetics and carbon budgets of stream ecosystems. Currently, MS student Renn Schipper is studying the contributions of autotrophs to respiration in canopy-covered and black-water rivers in the Upper Peninsula of Michigan.

Related Publications:

Collins SF, Baxter CV, Marcarelli AM, Felicetti L, Florin S, Wipfli MS, Servheen G. 2020. Reverberating effects of resource exchanges in stream-riparian food webs. Oecologia 192:179-189.

Marcarelli AM, Baxter CV, Benjamin JR, Miyake Y, Murakami M, Fausch KD, Nakano S. 2020. Magnitude and direction of stream-forest community interactions change with time scale. Ecology 101:e03064.

Bump JK, Bergman BG, Schrank AJ, Marcarelli AM, Kane ES, Risch AC, Schutz M. 2017. Nutrient release from moose bioturbation in aquatic ecosystems. Oikos 126:389-397.

Mineau MM, Baxter CV, Marcarelli AM, and Minshall GW. 2012. An invasive riparian tree reduces stream ecosystem efficiency via a recalcitrant organic matter subsidy. Ecology 93:1501-1508.

Marcarelli AM, Baxter CV, Mineau MM, Hall RO. 2011. Quantity and quality: unifying food web and ecosystem perspectives on the role of resource subsidies in freshwaters. Ecology 92:1215-1225.

Marcarelli AM, Van Kirk RW, and Baxter CV. 2010. Predicting effects of hydrologic alteration and climate change on ecosystem metabolism in a western U.S. river. Ecological Applications 20:2081-2088. DOI: 10.1890/09-2364.1

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