Welcome to

Given our unique location in Socorro, NM, and our network of collaborators and projects in the Southwest, the Duval Lab is thriving as a hub for arid land ecosystem research and teaching. Please contact us about potential collaboration, existing projects, and if you have interest in joining us as a student or visiting researcher.



Congratulations to Marina Hein and Katie McLain for receiving a grant award from the Native Plant Society of New Mexico! This will help further their MS theses projects on our middle Rio Grande work on evapotranspiration, greenhouse gas flux and native/invasive riparian plant communities.


Happy New Year. We are busy at work with the Rio Grande hydro-biogeochemistry project, finishing up instrumentation at D-DIRT Sevilleta, and moving forward with our soil bacterio-phage/N-cycle project. Good things to come in 2021!


We are excited to announce new funding from BLM! We are looking for a motivated student to work on a Master’s level project related to creosote encroachment, grassland restoration, and all of the biogeochemical consequences therein. Please contact for more information.


We are happy to invite Marina Hein into the lab as our newest graduate student. Welcome, Marina!


Sergio de Tomas Marin successfully defended his Master’s thesis! Congratulations Sergio!


Biology 112 students please follow this link for updated class information given our current distance education situation.


The Duval Lab is actively recruiting Master’s students to begin in August of 2020 to work on projects related to invasive plant impacts on N biogeochemistry and desert soil C cycling. Please contact with a letter (or email) of interest and a brief resume/CV with contact information from a former mentor and a former employer. Review will start immediately and final decisions will be made by early-mid April 2020.


Walter Whitford and I’s book (Ecology of Desert Systems, 2nd edition) has been printed! I’m incredibly excited to have helped Walt update his seminal work, and am looking forward to feedback from our colleagues working in desert systems.


Please consider submitting an abstract to our session at the American Geophysical Union Fall 2019 meeting! I will be co-convening a session with Dr. Jennie McLaren (UTEP Biology) and Dr. Dan Cadol (NM Tech Hydrology) on the biogeochemical effects of invasive and encroaching plants. We are super excited to solicit research presentations using any methodology (field measurements, lab experiments, modeling) that address soil-microbial-atmosphere interactions leading to a better understanding of how invasive/encroaching plants change local and regional biogeochemistry.


Update on the book Ecology of Desert Systems 2nd Edition, Walt and I are expecting a September 1 release date.


Benjamin Duval

​Assistant Professor
Department of Biology,
​New Mexico Institute of Mining and Technology

Current Position Aug. 2016-present

…lot’s of stuff in between (thanks to Evan DeLucia and Pete Vadas and Rob Anex…)

PhD, Northern Arizona University 2010
MS, New Mexico State University 2005
BA, The College of Wooster, 2001

Gustav Falcon Coleman-Duval

Youngest lab member & aspiring New Mexican plant ecologist. ​Shown here skeptically surveying a grassland ecotone at the Sevilleta NWR.

Marina Hein (Master’s student, Biology)

Marina earned her B.S. at Wisconsin’s Northland College in 2017. She received the Natural Resource Faculty Award for her work using linear mixed models to determine drivers of algae abundance in Great Lakes wetlands as part of EPA’s Great Lakes Coastal Wetland Monitoring Program. After moving to Washington state, Marina developed the Reed Canarygrass Monitoring Program for the 10,000 Years Institute to study how invasive reed canarygrass (Phalaris arundinacea) is changing the morphology, chemistry, and biology of streams earmarked by scientists as resilient to the effects of climate change, and valuable spawning and rearing habitat for coldwater species, particularly salmonids :

Currently, she is a collaborator on our project to study the effect of invasive plants in Rio Grande riparian areas on evapotranspiration and nitrogen biogeochemistry.

Evangelina Carabotta (Undergraduate Researcher)

Resident bug catcher and burgeoning entomologist. Eva is working on cataloging the aquatic insects from the Gold King Mine project as well as starting a new endeavor to monitor terrestrial arthropod communities in response to Russian olive removal along the Rio Grande.

Samuel Hoffman (Undergraduate Researcher)

Sara Watson (Undergraduate Researcher)

Sara is a Senior in the NMT Biology department interested in environmental science, including ecology, evolution, Eco-morphology, and conservation. Sara is working with Eleanor House on a native plant germination project funded by the Institute of Applied Ecology in Santa Fe. This involves the treatment of seeds to find the methods for optimal germination success.

Eleanor House (Undergraduate Researcher)

Lab alums

Jamie Martin

Former Laboratory Manager/Plant Ecologist

So sorry to see Jamie leave for Alaska, but we know her amazing field abilities, lab skills and plant ID acumen will serve her well in whatever the next chapter will be. We miss you Jamie!

Sergio de Tomas Marin (Master’s graduate; Biology)

Sergio’s thesis work focused on the biogeochemical response (nutrient dynamics and GHG flux) of soils following invasive riparian plant removal. He is currently pursuing his PhD in Germany at the University of Zurich (UZH).

Faith Simitz

​Undergraduate Researcher, Duval Lab & NMT Biology Alum

I finished my bachelors in Biology with Environmental Science option. I am interested in Ecology and am working as a natural resource specialist since graduation. I worked with Dr. Duval as a research assistant, and conducted research project using Opuntia ficus-indica mucus as a soil amendment to improve C storage in desert and agricultural soils in New Mexico.

Cody Champion

Post-doctoral Scientist (ORISE Fellow)

Cody earned his 5-year B.S./M.S. at NMT in 2014 in Biology. He then attended NMSU from 2014 to 2018 for his Ph.D. program. During this time he received the National Science Foundation Graduate Research Fellowship for his work in mosquito physiology and associated microbial communities. Currently, he is working through the IC fellowship program sponsored by ORISE on the development of autonomous drone sensing of plant stress."


I study ecosystem ecology, and am specifically interested in atmosphere-soil interactions that are controlled by plants and the microbes they associate with. I am especially interested in how plants and microbes respond to climate variation, invasive plants and how changing agricultural inputs alter the nitrogen cycle.

My research answers questions via measurements in the field and lab. Our lab takes advantage of the range of ecosystems, both natural and managed, that are within close proximity to Socorro. Below are our recent and soon to be underway projects.

Ecology courses at NM Tech

The following is general information about courses I teach. If you are a New Mexico Tech student enrolled in the courses below, course-related material is housed on Canvas. If you are a New Mexico Tech student interested in the courses below, please contact me

Ecotoxicology (BIOL 489/589, Spring 2020)

This is a new course and will focus on how anthropogenic environmental pollution impacts ecological systems and potentially changes biotic communities. More to come…

Ecosystem Biology (BIOL 402/502 next offering, Spring 2021)

Ecosystem Biology builds off of topics covered in General Ecology, with more emphasis on climate systems and biotic interactions with the physical environment. We cover basic climate physics, soil formation, physical ecosystem structure and function, water and energy budgets, nutrient cycling, disturbance regimes and species mediated feedbacks to all of the above. Particular attention is paid to plant-microbe-soil interactions and effects of climate change on terrestrial ecosystems. New Mexico Tech is unique for its close proximity to desert grassland, several montane systems, the Rio Grande Valley and two wildlife refuges (Bosque Del Apache and Sevilleta). We take full advantage of those ecosystems via field trips and data collection!

Evolution, BIOL 345 (next offering Fall 2020)

Evolution isn’t a sub-discipline of biology. It IS Biology. For that reason, I successfully lobbied to make Evolution at NM Tech a 300-level course that will expose students to these critical concepts early in their upper division coursework. We cover early Earth evolution and the origins of life, geologic and molecular evidence for evolution, basic molecular genetics, population genetics, phylogenetics, sexual selection and macroevolution. Biology 112, Chemistry 121 and 122 are prerequisites for this course; Earth and Environmental Science majors who have taken ERTH 201 will be considered for waivers of the BIOL 112 prerequisite.

General Ecology, BIOL 344 & 344 Lab (next offering, Fall 2020)

What is “ecology”? The boring, textbook definition is something about organisms, their environment, interactions, etc., etc. But organisms are incredibly complicated, hence entire disciplines of Microbiology, Zoology, Physiology, Molecular Biology and Botany. And the “Environment” could be anything from a micropore on a soil aggregate to the entire globe! So scale matters, and what you want to know about an organism, or its environment, or how each shape each other, also matters. Keeping all that firmly in the front of our minds, we will get into generalities and details about how species interact with each other (via competition, predation, pollination, mutualisms, parasitism), how populations form and move, community structure, causes and effects of diversity and the ecosystem concept. An optional lab component will be modified this year given uncertainty about SARS-Cov-2, but we will likely delve into Bayesian statistics with ecological data sets. Biology 112, Chemistry 121 and 122 are prerequisites for this course.

Introductory Biology (2nd Semester for Majors, every Spring), BIOL 112 & 112 Lab

This is the second semester of our Introductory Biology sequence at Tech. Building from knowledge gained in BIO 111 (chemistry of biology & workings of the cell), we introduce the diversity of organisms in an evolutionary and ecological context. Heavy emphasis early in the semester is placed on presenting a more sophisticated view of evolution than students may have previously encountered. We expect our Biology majors to have a firm understanding how genetic drift, natural selection, sexual selection and mutation shape our living world, and Biology 112 is our way of introducing students to these concepts.



Duval B.D. (2020) Abiotic pulses and microbial activity lags in greenhouse gas emissions due to tillage. Agrosyst Geosci Environ.

Duval, B.D., Cadol, D., Martin, J., Frey, B. & Timmons, S. (2020). Effects of the Gold King Mine spill on metal cycling through river and riparian biota. Wetlands

Duval, B.D., Curtsinger, H., Hands, A., Martin, J., McLaren, J. & Cadol, D. (2020) Greenhouse gas emissions and extracellular enzyme activity variability during decomposition of native versus invasive riparian tree litter. Plant Ecology doi:10.1007/s11258-020-01003-6duval_etal2020_ghg_emissions_and_enzyme_activity_decomposing_litter.pdf


Whitford, W.G. & Duval, B.D. (2019) Ecology of Desert Systems, 2nd edition. Elsevier Press.

Aguerre, M.A., Duval, B.D., Vadas, P., Powell, J.A. & Wattiaux, M. (2019) Effects of feeding a quebracho-chestnut tannin extract on lactating cow performance and nitrogen utilization efficiency. Journal of Dairy Science

Thapa, V.R. Ghimire, R., Duval, B.D., & Marsalis, M.A. (2019) Tillage and Cover Cropping Affect Soil Organic Carbon Dynamics and Net Ecosystem Carbon Balance in Semiarid Drylands. Agrosystems, Geosciences and Environment doi:10.2134/age2019.03.0022


Duval, B.D., Cadol, D., Martin, J. & Timmons, S. (2018) Persistent effects of the Gold King Mine Spill on Biota: Animas and San Juan Rivers, Northern New Mexico. NM Bureau of Geology and Mineral Resources, Open File Report 601.

Duval, B. D., Ghimire, R., Hartman, M. & Marsalis, M.A. (2018). Water and nitrogen management effects on semi-arid sorghum production and trace gas flux under future climate. PLoS ONE 13(4): e0195782.


Veltman, K., Jones, C.D., Gaillard, R., Cela, S., Chase, L., Duval, B.D., et al. (2017). Comparison of process-based models to quantify nutrient flows and greenhouse gas emissisons associated with milk production. Agriculture, Ecosystems and Environment 237, 31-44.


Duval, B. D., Aguerre, M., Wattiaux, M., Vadas, P. A., & Powell, J. M. (2016). Potential for Reducing On-Farm Greenhouse Gas and Ammonia Emissions from Dairy Cows with Prolonged Dietary Tannin Additions. Water, Air, & Soil Pollution, 227(9), 329. doi:10.1007/s11270-016-2997-6
Gaillard, R., Duval, B.D., Osterholz, W.R. & Kucharik, C.J. (2016). Simulated effects of soil texture on nitrous oxide emissions factors from corn and soybean agroecosystems in Wisconsin. Journal of Environmental Quality 45:1540-1548. ​doi:10.2134/jeq2016.03.0112
Li, A., Duval, B. D., Anex, R., Scharf, P., Ashtekar, J. M., Owens, P. R., & Ellis, C. (2016). A Case Study of Environmental Benefits of Sensor-Based Nitrogen Application in Corn. Journal of Environmental Quality, 45(2), 675-683. doi:10.2134/jeq2015.07.0404


Duval, B. D., Hartman, M., Marx, E., Parton, W. J., Long, S. P., & DeLucia, E. H. (2015). Biogeochemical consequences of regional land use change to a biofuel crop in the southeastern United States. Ecosphere, 6(12), 1-14. doi:10.1890/ES15-00546.1
Duval, B.D., Natali, S.A. & B.A. Hungate. (2015). What constitutes plant available molybdenum in sandy, acidic soils? Comm. Soil Sci. Plant Analysis 46:318-326. doi:10.1080/00103624.2014.969405
Hungate, B. A., Duval, B. D., Dijkstra, P., Johnson, D. W., Ketterer, M. E., Stiling, P., Cheng, W., Millman, J., Hartley, A. & Stover, D. B. (2014). Nitrogen inputs and losses in response to chronic CO 2 exposure in a subtropical oak woodland. Biogeosciences, 11(12), 3323-3337. doi:10.5194/bg-11-3323-2014


Anderson‐Teixeira, K. J., Miller, A. D., Mohan, J. E., Hudiburg, T. W., Duval, B. D., & DeLucia, E. H. (2013). Altered dynamics of forest recovery under a changing climate. Global Change Biology, 19(7), 2001-2021. doi: 10.1111/gcb.12194

Duval, B. D., Anderson-Teixeira, K. J., Davis, S. C., Keogh, C., Long, S. P., Parton, W. J., & DeLucia, E. H. (2013). Predicting greenhouse gas emissions and soil carbon from changing pasture to an energy crop. PloS ONE, 8(8), e72019.

Duval, B. D., Dijkstra, P., Drake, B. G., Johnson, D. W., Ketterer, M. E., Megonigal, J. P., & Hungate, B. A. (2013). Element Pool Changes within a Scrub-Oak Ecosystem after 11 Years of Exposure to Elevated CO 2. PloS ONE, 8(5), e64386.

Day, F. P., Schroeder, R. E., Stover, D. B., Brown, A. L., Butnor, J. R., Dilustro, J., Hungate, B.A., Dijkstra, P., Duval, B.D., Siler, T., Drake, B. G. & Hinkle, C.R. (2013). The effects of 11 yr of CO2 enrichment on roots in a Florida scrub‐oak ecosystem. New Phytologist, 200(3), 778-787. doi: 10.1111/nph.1224

Hungate, B. A., Dijkstra, P., Wu, Z., Duval, B. D., Day, F. P., Johnson, D. W., Megonigal, J.P., Brown, A.L.P… & Garland, J. L. (2013). Cumulative response of ecosystem carbon and nitrogen stocks to chronic CO2 exposure in a subtropical oak woodland. New Phytologist, 200(3), 753-766. doi: 10.1111/nph.12333

Hungate, B. A., Day, F. P., Dijkstra, P., Duval, B. D., Hinkle, C. R., Langley, J. A., Megonigal, J.P., Stiling, P., Johnson, D.W. & Drake, B. G. (2013). Fire, hurricane and carbon dioxide: effects on net primary production of a subtropical woodland. New Phytologist, 200(3), 767-777. doi: 10.1111/nph.12409


Anderson-Teixeira, K. J., Duval, B. D., Long, S. P., & DeLucia, E. H. (2012). Biofuels on the landscape: Is “land sharing” preferable to “land sparing”?. Ecological Applications, 22(8), 2035-2048. doi: 10.1890/12-0711.1

​Duval, B. D., & Whitford, W. G. (2012). Reintroduced prairie dog colonies change arthropod communities and enhance burrowing owl foraging resources. Immediate Science Ecology, 1. article link

Duval, B. D., Blankinship, J. C., Dijkstra, P., & Hungate, B. A. (2012). RETRACTED ARTICLE: CO2 effects on plant nutrient concentration depend on plant functional group and available nitrogen: a meta-analysis. Plant Ecology, 213(3), 505-521. doi: 10.1007/s11258-015-0541-1


Duval, B. D., Dijkstra, P., Natali, S. M., Megonigal, J. P., Ketterer, M. E., Drake, B. G., Lerdau, M.T., Gordon, G., Anbar, A.D. & Hungate, B. A. (2011). Plant− soil distribution of potentially toxic elements in response to elevated atmospheric CO2. Environmental Science & Technology, 45(7), 2570-2574. doi: 10.1021/es102250u

Eldridge, D. J., Whitford, W. G., & Duval, B. D. (2009). Animal disturbances promote shrub maintenance in a desertified grassland. Journal of Ecology, 97(6), 1302-1310. doi: 10.1111/j.1365-2745.2009.01558.x

​Duval, B. D., & Whitford, W. G. (2009). Camel spider (Solifugae) use of prairie dog colonies. Western North American Naturalist, 69(2), 272-276. doi: 10.3398/064.069.0220

Duval, B. D., & Whitford, W. G. (2008). Resource regulation by a twig‐girdling beetle has implications for desertification. Ecological Entomology, 33(2), 161-166. doi:10.1111/j.1365-2311.2007.00928.x

Duval, B. D., Jackson, E., & Whitford, W. G. (2005). Mesquite (Prosopis glandulosa) germination and survival in black-grama (Bouteloua eriopoda) grassland: relations between microsite and heteromyid rodent (Dipodomys spp.) impact. Journal of Arid Environments, 62(4), 541-554. doi:10.1016/j.jaridenv.2005.01.012

Extended Team

Ecological research is inherently collaborative and the Duval Lab owes a major debt to many groups. And thankfully, that list keeps getting longer! For this space, we’ll try to keep a current list of collaborators.

Sevilleta LTER:

Sorghum/ROOTS/Dryland Agriculture project(s):

Arid woodland seed production and C-cycling:

Animas River Contaminant Cycling:


Biology at New Mexico Tech

The New Mexico Institute of Mining and Technology was founded in 1899 as the New Mexico School of Mines. Excellence in geology and engineering are a hallmark of our university, but the Department of Biology is home to a small group of dedicated scholar/teachers with research interests in drug discovery, extremeophile & environmental microbiology, microbial genetics, functional evolution, and ecosystem science. We work closely with other Departments such as Chemistry, Chemical Engineering, Earth & Environmental Sciences and we tolerate the Physics and Math Departments…There is a lot of interdisciplinary work going on at NMT and we are in the middle of it.

The NMT official website is significantly better than it was not too long ago…go check it out…

Student Positions

We are actively recruiting students to the Duval Lab. Specific degrees are not as important as your sincere interest in plants and soil, and self-motivation. Funding is limited, and TA positions fill quickly. We do not require GRE scores for admission to the Biology Master’s program. Tech is in the process of migrating to a new online application system for all grad applications, so contact me directly for updates, and we will work together to make sure you are in the cue for a fully considered application.

Many, many words have been written about what your motivation should be for grad school, advice for how to succeed in grad school and probably an equal or greater number of words complaining about grad school. I’m hoping you’ve already read some of those words on your way to this page. What I guarantee are clear expectations. Here are some:

What we want: motivated, accountable, self-reliant people that are willing to learn and share in both the reward and occasional tedium of doing ecosystem science. You will be working with a group of supportive people that come from diverse backgrounds and have equally diverse ideas about how the world works. We collaborate with Geologists, Chemists, modelers and quantitative geneticists. We also work with farmers, ranchers and people that dig wells for a living. We respect hard work no matter how many or how few letters you have after your name. I will never expect you to do something that I am not willing to do myself, or show you how to do.

What we do not want: People that are applying to grad school as a “back up plan”. People that have a hard time, being on time. Anyone that thinks success comes before work. Working in science is incredibly rewarding, and the process is educational in ways that you do not often anticipate. There will be broken glassware. There will be flat tires in the desert. You might run over an irrigation pipe (it happens…). You will get papers rejected and funding denied. We do not want people that balk at these challenges, because we know from experience that all these events will happen.

If you are still reading, and have decided that you would like to be a part of the work going on in my lab, let’s start a conversation.

-Please, first email me with brief information about yourself, what about my work is interesting to you and why, a brief (1 to 2 page) CV or resume that includes the names and contact info for at least 2 references (preferably at least 1 academic reference and someone you worked with/for in any capacity).

I will make a preliminary decision, and if we seem like a good fit for each other, we will schedule a phone conversation, and hopefully you can make an in-person visit to Socorro. Please check this out for my “biased with an attempt to be realistic” views about living in central NM and Socorro specifically.

Living in Socorro

New Mexico hosts a diversity of landscapes that offer endless opportunities for natural areas research. While outsiders may think New Mexico is primarily desert, the Rio Grande runs the length of the this state which has more named peaks than Colorado. The area around Socorro boasts the confluence of the Colorado Plateau, Great Plains, Conifer systems at higher elevation and the northern limit of the Chihuahuan Desert (image to left from Sevilleta LTER).

Within 30 minutes of Socorro, you can be in ponderosa pine forest, desert grassland, Rio Grande-irrigated farmland or pinon-juniper woodland. This diversity of ecosytems, coupled with extremely low population density, makes this part of New Mexico incredible for outdoor recreation and field research.

Watershed nutrient cycling field site with Sierra Ladrones in background.

Socorro is perhaps the least pretentious town in the mountain west. But the benefits of living in a remote place constitute drawbacks for other people. The population of Socorro is ~8000. ​There is one, small grocery other than Wal-Mart. The town does offer several good Mexican restaurants, one brewery, one coffee shop, and a legit cowboy bar on the plaza. The farmer’s market on Tuesday’s is a favorite meeting spot and your go-to destination for duck eggs. For touring music acts, museums and fine arts, Albuquerque is an hour away…

For potential graduate students, I assume that if you have more than a casual interest (or hope to cultivate one) in rock climbing, mountain biking, hiking and camping, you will find your time in Socorro to be thoroughly enjoyable. We have beautiful and remote field sites in mountain and grassland areas, in addition to the agricultural work which has its own beauty. Also, the cost of living is incredibly reasonable.

Rock spire in the Monzano Mountains ~1.5hrs east of Socorro

Greenhouse gas emissions and extracellular enzyme activityvariability during decomposition of native versus invasiveriparian tree litter

Benjamin D. Duval . Heather D. Curtsinger . Aubrey Hands .Jamie Martin . Jennie R. McLaren . Daniel D. Cadol


Invasive plants alter riparian vegetationcommunities and shift biogeochemical processes bychanging decomposition rates and the soil chemicalenvironment created by leaf litter. It is unclear if thismechanism shifts nutrient dynamics favoring invasivedominance; riparian areas in the Southwestern USAinvaded by salt cedar and Russian olive often still hostmixed stands of native plants. To test the hypothesisthat invasive plant success is related to altered litterinputs, microbial activity and nutrient cycling, weperformed laboratory incubations examining green-house gas emissions and microbial extracellularenzyme activity (EEA). The responses of GHG fluxand EAA were measured from decomposing translo-cated litter from native and invasive woody perennialsbetween soils where they were growing. Litter decomposition from two invasive species (salt cedarand Russian olive) and two native trees (coyote willowand Fremont cottonwood) were tracked for 3 months.Soil respiration, carbon content and EEA were allmore closely related to soil origin than leaf litterspecies. The highest decomposition rate was fromwillow soil. Soil nitrate at the end of the experimentwas highest for soils collected under cottonwood.Nitrous oxide (N2O) emissions were significantlygreater from Russian olive litter than other species, onall soil types. Patterns observed here suggest that (1)plant influences on local soil properties over thelifetime of a plant have a greater control on decom-position processes than short-term litter input source,(2) EEA is strongly related to available C resources,and (3) the invasive shrub Russian olive may beresponsible for previously undocumented large N2Oemissions in riparian systems in the USA.Keywords Litter decomposition Б Greenhousegases Б Invasive species Б Extracellular enzymes БNitrogen cycling Б Riparian

Communicated by Shayne Martin Jacobs.B. D. Duval (&) Б H. D. Curtsinger Б A. Hands БJ. MartinBiology Department, New Mexico Institute of Mining andTechnology, Socorro, NM 87801, USAe-mail: benjamin.duval@nmt.eduJ. R. McLarenThe Department of Biological Sciences, University ofTexas-El Paso, El Paso, TX 79968, USAD. D. CadolEarth and Environmental Sciences Department, NewMexico Institute of Mining and Technology, Socorro,NM 87801, USA


Alien-invasive plant species are globally ubiquitousdue to humans’ purposeful and inadvertent altering ofplant distributions to meet our nutritional, fiber, andornamental whims. Once plant colonizers have been introduced, they may persist despite competition withnative species evolved in those environments. AsElton (1958) articulated, this is often because alienspecies exhibit functional traits relevant to a signifi-cant ecosystem process; symbiotic N2-fixers increaseN import in N-limiting soils, early-senescing grassesaccelerate fire return that reduces interspecific com-petition, and unique root morphology can allow forexploitation of novel soil resources (D’Antonio andVitousek 1992; Humphrey and Schupp 2004; Nsikaniet al. 2018).When invasive plants successfully establish andecosystem processes change, efforts to restore nativeplant species and communities are often rooted in theassumption that what came first must be best. It isnearly axiomatic among conservationists of the west-ern United States’ riparian areas that salt cedar(Tamarix ramosissima and hybrids; Gaskin and Schaal2002) is a scourge due to its water profligacy(Audubon Society 2018), despite abundant evidenceto the contrary, especially compared to native vege-tation (van Hylckama 1970; Nagler et al. 2009;McDonald et al. 2015). For example, using a suite of30 ecosystem traits including soil, geomorphology andvegetation physiology characters, Stromberg (1998)concluded that salt cedar is functionally equivalent toFremont cottonwood (Populus fremontii) in the SanPedro riparian areas in southern Arizona.Irrespective of water use, the expansion of saltcedar is still of concern as salt cedar leaves concentrateand excrete salts as a means to survive in high-salinitysoils, which has implications for decomposition pro-cesses and nutrient cycling. Kennedy and Hobbie(2004) report that salt cedar leaf decomposition instreams was lower than ash (Fraxinus velutina) leaves,but faster than bulrush (Scirpus americanus). Otherwork reports that salt cedar decomposed faster withinstreams compared to Fremont cottonwood; however,salt cedar litter packs hosted lower species richnessand abundance of stream macroinvertebrates com-pared to Fremont cottonwood at Wet Beaver Creek,Arizona (Bailey et al. 2001).Russian olive (Elaeagnus angustifolia) is anotherEurasian invader of western US riparian systems, andits establishment success is likely due to its hosting ofsymbiotic N2-fixing microbes in its rhizome (DeCant2008) and ability to establish in shade while utilizingsoil moisture instead of groundwater (Reynolds andCooper 2010). The presence of a symbiotic N2-fixer ina community can enhance N resources for plantspecies (Khamzina et al. 2009). However, excess Ncan be a hindrance to native species restoration asmany woody riparian species evolved in N-poorenvironments (Rice et al. 2004), and N deposition inexcess of vegetation requirements is understood toreduce plant community diversity (Bobbink et al.2010). If a given plant’s litter modifies local soilmicrobial communities, feedbacks may exist to indi-vidual plant N nutrition via microbial activity thatchanges local pH or nitrification rates (Kourtev et al.2003).The question remains as to how easily salt cedarand Russian olive invade stands of native woodyvegetation. A related question is how much invasivespecies change the soil microbial community, and canthat knowledge be used in restoration efforts? In theabsence of shading out competitors, competitionbetween plants for water and other resources occursbelowground and can be mediated by the microbialcommunity (Ludwig et al. 2004; Van Der Heijdenet al. 2008). Microbial extracellular enzymes areimportant for organic matter depolymerization andcycling N and P within soils (Sinsabaugh et al. 2003).If invasive plants change local soil biogeochemistryand nutrient cycles, those changes are likely driven bydifferences in decomposing leaf chemistry and may beevidenced by altered enzyme activity.We hypothesized that invasive shrub species alterthe biogeochemical (i.e., C and N processing) role ofsoil microbial communities compared to native ripar-ian plants via leaf litter inputs. We tested thishypothesis using a reciprocal transplant experimentthat incubated invasive and native litters on soils fromwhich the parent plants were collected. We assessedthe interactions between plant material and soil withthree different metrics of litter decomposition: massloss, systematic measurements of greenhouse gasproduction from litter/soil combinations, and micro-bial extracellular enzyme activity (EEA) at the end ofthe experiment. We specifically predicted that inva-sive plant litter on soil conditioned by native plantswould decompose faster than native plant litter onsoils home to native plants, and accelerate N cycling,evidenced by higher gaseous N losses and higherpotential rates of N-processing EAA, thus providing amicrobial feedback to facilitate invasion.

Materials and methods

Study species

We sampled plant tissue and soil along the San JuanRiver near Bloomfield, New Mexico, USA (36.702 N,107.978 W). We collected live leaves and petiolesfrom the ‘‘natives’’ coyote willow (Salix exigua;hereafter ‘‘willow’’) and broadleaf cottonwood (Pop-ulus fremontii; hereafter ‘‘cottonwood’’), and ‘‘inva-sive/aliens’’ salt cedar (Tamarix spp.) and Russianolive (Elaeagnus angustifolia). All of these species areearly successional woody perennial shrubs/trees withdistributions in the western USA typically limited toriparian areas. The study area was chosen for plantsampling because it had (by visual estimation) roughlysimilar landscape distribution/land cover across allfour species and thus represents an opportunity toexamine decomposition dynamics in a mixed nativevs. invasive community. We chose to use fresh leavesas a decomposition substrate as we aimed to testdifferences in plant species litter typ#### e compared to thesoil microenvironment, and mimic a realistic decom-position environment in the laboratory. Individualplants within a species selected for leaf collectionswere similar in size and approximate age. Wecollected fully expanded leaves from ten individualsof each species by hand, by defoliating the terminal 1m of five individual branches per plant. We used ahand trowel to collect soil to a depth of 10 cm underthe canopy (within 30 cm of the trunk) of each plantsampled.

Experimental design

We air-dried leaves for 72 h in paper sacks in adesiccating cabinet. We separated leaves and petiolesfrom stems, then we ground all plant leaves with acoffee grinder so that microbial decomposition rateswere dependent primarily on the chemical composi-tion of the different species rather than their inherentlydifferent surface areas. To construct litter decompo-sition bags, we placed * 2 g of ground plant materialinto empty tea bags (Nuiby Co, China). We dried bagswith litter at 40 °C for 24 h and included the mass oflitter bags as a record of pre-incubation mass. Bagswere made of unbleached biodegradable hemp; how-ever, we assume any bag mass loss to be uniformacross litter/soil treatments as preliminary labevaluations showed no mass loss in the empty bagspre and post drying. We chose these specific bags toreduce the possibility of chemical interference withdecomposition that could confound our results.Soils at the site are Green River sandy loams(Oxyaquic Torrifluvents). Soil texture, pH or initialSOC content did not appreciably vary within the studyarea between soils under invasive and native plants.We homogenized air-dried soil by passing through a2-mm sieve and then a 250-lm screen (Andruschke-witsch et al. 2014). We assembled incubation cham-bers by placing * 20 g of sieved soil into 120 mlsterile sample cups, and allowing to pre-incubate insample cups for 24 h. Next, we placed a litter bag inthe cup, and covered with another * 20 g of soil,setting up replicate cups (n = 3) for each of the 16combinations of litter and soil (factorial combinationsof 4 plant species and their soil).We added water to incubation soil and litter cups torestore samples to the water content in each soil at timeof collection using a micro-pipette to ensure evendistribution across the soil surface. We determinedthat value from the mass of water lost during airdrying, so each sample differed slightly in the amountadded. We then incubated sample cups in 900 ml glassjars with sealed lids and a small amount of water in thejar (* 40 ml separate from the sample cup) to preventdesiccation of the samples. We measured gas concen-tration immediately after set-up was completed to givea time 0 measurement.

Decomposition measurements

We measured decomposition with three metrics: littermass loss over the course of the experiment, green-house gas emissions [Carbon dioxide (CO2) andnitrous oxide (N2O)], and EEA. At the end of theexperiment, litter bags were removed from soil cups,and excess soil sticking to bags was carefully removedby brushing soil away with a small clean paintbrush.Bags were dried for 24 h at 40 °C to replicate the pre-incubation procedure before taking the final mass.Mass loss was determined by the difference in mass ofthe litter bags ? litter at the end of the incubationcompared to the initial conditions.Incubation jars were sealed with lids and incubatedin the dark at 25 °C. Gas analysis was performed byventing jars for * 5 min prior to measurements, thenaffixing a modified lid with quick-connect fitting attached to sample tubing connected to the gasanalyzer. Trace gas measurements were made with aGasmet DX-4040 Fourier-transform infrared (FTIR)gas analyzer (Oy, Finland). The instrument wascalibrated before measurements by zeroing the detec-tor with ultra-high purity N2. Gas measurements beganimmediately after adding water to the samples (dried,sieved soil ? litter) (Time 0). During measurements,gas concentration was determined automatically viaCalcmet software every 20 s over a 3–5 min interval.Jars were re-sealed following gas analysis. Fluxeswere calculated with a linear model after correctinggas concentration for molar mass and evaluating thechange in mass in the incubation chambers overmeasurement time. Measurements were taken dailybetween Time 0 and day 7, then weekly between day 7and day 91. Carbon dioxide (CO2) emissions fromsamples came from litter ? soil, and are hereaftertermed soil respiration (Rs). All gas fluxes werecalculated from the molar mass changes in gases in theincubation jars over the length of measurement time,corrected by the volume of incubation chamber.EEA was determined from soils at the end of theincubation. Following litter bag removal, 1 g of soilwas removed and frozen at -20˚C until the time ofenzyme assays. We assayed soils for a group ofhydrolytic and oxidative enzymes involved in C, N,and P acquisition from the later stages of organicmatter decomposition. Enzymes surveyed were asfollows: cellulose-degrading b-glucosidase, chitin-degrading N-acetyl-glucosaminidase (NAG), the pro-tease Leucine aminopeptidase (LAP), and acidphosphatase.EEA methodology was modified from Saiya-Corket al (2002) and McLaren et al. (2017). Soil wasblended with a tissue tearor (Biospec Products, Inc,Bartlesville, Oklahoma) in pH 5 sodium acetate bufferand pipetted into 96-well plates, with eight analyticalreplicates per sample. Fluorescing, 4-methylumbellif-erone (MUB) (b-D-glucoside, N-acetyl-a-D-glu-cosaminide and phosphate) or methylcoumarin (MC)(7-amino-4-methylcoumarin) tagged substrate wereadded. Assays were incubated at 20 °C for 3.5 h, withhalf-hourly measurements ensuring activity was mea-sured in the linear range of the reaction. Samplefluorescence (i.e., cleaved substrate) was read with aBioTek Synergy HT microplate reader (BioTekInstruments Inc., Winooski, VT, USA) at 360 nmexcitation and 460 nm emission. For each substrate,we measured the background fluorescence of soils andsubstrate and the quenching of MUB by soils, and usedstandard curves of MUB to calculate the rate ofsubstrate hydrolyzed, hereafter EEA.

Mineral N and 13C analysis

Ammonium (NH4?) and nitrate (NO3-) were deter-mined from post-incubation soils extracted with 2 MKCl. Ammonium analysis follows Weatherburn(1967), whereas NO3- analysis follows Doane andHorwath (2003). After the assays were completed,absorbance spectra were determined with a FisherScientific accuSkan Go plate reader (Vantaa, Finland)and calculations to establish N concentration wereperformed via linear regression analysis based onstandard concentrations added to plates.Carbon stable isotopes (13C and 12C) are a usefulindicator of C substrate quality. Fractionation of Cduring decomposition favors 12CO2 production andenriches the microbial biomass and remaining Cresources (i.e., higher 13C content). We thereforeconducted pre-incubation soil and leaf 13C and 15Nanalysis (Center for Stable Isotopes at the Universityof New Mexico; Table 1). Isotope results are presentedin delta (d) notation, which represents per milldeviations from standards:daX ¼ aRsample/aRstandard А 1()В 1000where X is 13C or 15N and R is the ratio of 13C:12C or15N:14N. Standards for isotope analysis were Califor-nia Buckeye and peach leaf for plant tissue. Regres-sion coefficients for accepted NIST values vsmeasured 13C and 15N were [ 0.99 for both sets ofstandards.At the end of the experiment, total organic carbon(TOC) and C stable isotopes were determined from 4 to 12 mg samples of post-incubation soils using aThermoFisher Delta V Plus isotope ratio mass spec-trometer (Vantaa, Finland). Solid samples were com-busted to produce CO2 in a Costech ECS 4010CHNSO Elemental Analyzer which was then intro-duced to the mass spectrometer. Instrument standardsused were IAEA-C7 and Mexican calcite (A. Camp-bell, New Mexico Tech).

Statistical analysis

Mineral N content (NO3- and NH4?), soil C (mass and13C), and enzyme activity were tested for homogeneityof variance via the Fligner-Killeen test. Two-wayANOVA models (testing the effects of litter type andsoil origin) were employed when variances werestatistically equal. In instances of heteroskedastic data,Kruskal–Wallis tests were employed to evaluatedifferences between groups, independently for litterand for soil origin. Analyses were conducted in the Rstatistical software package (R Core Team 2018).Time series data for CO2 and N2O flux measured inthe decomposition experiment were evaluated with arepeated measures, 2-factor ANOVA model consid-ering soil origin and species of plant litter as maineffects, an interaction term, and sample day as therepeated measure. Those analyses were also con-ducted in R (R Core Team 2018).


Litter types differed in their C and N initial chemistryand stable isotope composition (Table 1). There weresignificant differences in the mass loss over theduration of the experiment between litter species(two-factor ANOVA; F3,32 = 170.2, P \ 0.001), soilorigin (F3,32 = 10.70, P \ 0.001), and a significantinteraction between soil and leaf type (F3,32 = 3.19,P \ 0.01). Mass loss between the beginning and endof the laboratory incubations showed that irrespectiveof plant species, litter decomposed most completely onsoils collected under willow (24–32% of original massremained; Table 2). The greatest mass loss from asoil–litter combination was for Russian olive leavesdecomposing on willow soil (Table 2). The least massloss was also from willow litter, but decomposed oncottonwood soil (Table 2). The range in values forlitter mass remaining after 90 days was greater whencomparing a single litter type over the range of soils(15–19%) versus the range of values for a single soiltype over the diversity of plant litters (4–8%).Soil CCarbon content of soils at the end of the experimentnegatively correlated with d13C (Fig. 1). Willow soilswere most enriched in 13C relative to other soils. Allsoil types grouped similarly when %C was plottedagainst 13C, again showing a dominant effect of soilover plant litter (Fig. 1).

Mineral N

Soil NH4? concentration was significantly affected bysoil origin, with the greatest concentrations observedfor willow soils and the lowest values for Russianolive soil (Fig. 2; Kruskal–Wallis, v2 = 17.19, df = 3,P \ 0.01). No significant differences were found insoil NH4? concentration when litter type was tested asa main effect (Kruskal–Wallis, v2 = 3.31, df = 3,P = 0.35).There was a significant effect of both litter and soilorigin as main effects on soil NO3- concentration atthe end of the incubation experiment (Fig. 3). Thehighest concentration of NO3- was measured fromsoils on which we incubated cottonwood litter forthree of the four soil types, but the highest overallmean NO3- value came from cottonwood soils withRussian olive litter (litter, F3,32 = 6.50, P \ 0.01; soil,F3,32 = 161.99, P \ 0.001). There was a significantinteraction between soil type and litter type for NO3-concentration (F9,32 = 14.62, P \ 0.001).

Gas flux

There was a significant effect of litter species(F3,785 = 37.34,P \ 0.001),soilorigin(F3,785 = 4.66, P \ 0.01), the interaction betweenlitter and soil (F9,785 = 3.01, P \ 0.001), and asignificant effect of time (F18,785 = 5.36, P \ 0.001)on soil respiration. Multiple comparisons via Tukey’sHSD of Rs as a function of soil type revealed twosignificant pair-wise comparisons whereby salt cedarsoil had greater Rs over the course of the incubationscompared to soils collected under Russian olive andcottonwood, respectively (both P \ 0.001; Fig. 4).Russian olive litter resulted in greater Rs over the course of the incubations than any other litter species,across soil type. Soil respiration measurements did notsupport the hypothesis that litter decomposes fasterwhen incubated in soils collected from under the sameplant species (Fig. 4).Nitrous oxide emissions were significantly affectedby litter species (F3,803 = 37.34, P \ 0.001), soilorigin (F3,803 = 4.66, P \ 0.01), and the interactionbetween litter and soil (F9,803 = 3.01, P \ 0.001). Ingeneral, the N2O emissions, by rank were as follows:cottonwood [ Russian olive [ salt cedar [ willow.Among plant litters, Russian olive decomposition onany of the soil types resulted in a striking temporalpattern whereby emissions peaked after approximately10 days for three of the soil types and after 30 days onwillow soil (Fig. 5).

Soil enzyme activity

Exo-enzyme activity (EEA) was more strongly con-trolled by soil origin than litter additions (Fig. 6).Leucine aminopeptidase (LAP) activity was greater oncottonwood and salt cedar soils compared to willowand Russian olive soils (Kruskal–Wallis, v2 = 17.19,df = 3, P \ 0.001), but there was no difference in LAPactivity among litter types (P = 0.35). Beta-1,4-glucosidase and phosphatase followed a similar pat-tern as we measured significantly higher activity ofthose enzymes on cottonwood and salt cedar soilscompared to willow and Russian olive soils (Я-1,4-glucosidase, Kruskal–Wallis, v2 = 37.16, df = 3,P \ 0.001;phosphatase,v2 = 39.40,df = 3,P \ 0.001), but there was no effect of litter type foreither enzyme (Я-1,4-glucosidase, P = 0.18; phos-phatase, P = 0.57). N-acetyl-glucosaminidase (NAG)was the only enzyme assayed that significantlydiffered in activity due to both soil and litter species(2-way ANOVA, soil F = 161.99, P \ 0.001; litterF = 6.50, P = 0.001).EEAs generally showed a positive relationship withsoil C content and a negative relationship with d13C(Fig. 6). Carbon dynamics clustered around soil originrather than litter species in a similar manner as littermass loss: we measured the lowest enzyme activityfrom samples containing willow litter, which also hadthe lowest C content by percent (0.24%), and theisotopically heaviest C (- 24.98%; Fig. 1). Forspecific EEAs, NAG and acid phosphatase activity displayed the most dramatic grouping of soil type byd13C, and the highest activity rates were on soils thathad been collected under tamarisk, irrespective of leaflitter type (Fig. 6).


Concern about invasive alien plant species is welljustified, especially in ecologically sensitive areas likeriparian zones. Potential impacts of these plantcommunity changes are alterations to the localhydrology, allochthonous nutrient inputs, and fireregimes (Brooks et al. 2004; Predick and Turner2008). These impacts, either observed or predicted, arethe drivers of efforts in many areas to restore ripariansystems to native vegetation. However, efforts toreplace plant communities at the landscape or regionalscale at which invasive plants have taken hold arenecessarily intense, and can be economically costly.Mechanical thinning is laborious, and treatments withchemical herbicides are costly and potentially harmfulto non-target organisms (Shepard et al. 2004). There-fore, determining the value of the ecosystem servicesthat are most meaningful for successful restorationsuch as decomposition and nutrient cycling shouldenter into discussions about habitat alteration.Discussions of invasive plant removal often solelyfocus on plants, and our results argue for more targeteddata acquisition and monitoring on soils in invadedsystems. Contrary to our expectations, soil source,rather than plant litter, had a greater effect ondecomposition, soil respiration, and microbial EEA.Previous workers have shown that mixing litters of different species and functional groups has non-additive effects, i.e., ecosystem consequences ofdecomposition are not easily predicted from thenumber of species represented in a consortium oflitter (Wardle et al. 1997; McLaren and Turkington2011). In a companion study in this same ripariansystem, we did not observe significant differencesalong transects of overbank soils for physiochemicalmetrics like pH, electrical conductivity or moisturecontents (Duval unpublished data). Soil properties arenecessarily a function of the plants growing on themand dependent of leaf litter inputs over the life span ofthe plants (Rhoades 1996). However, trees affect thesoil system through their uptake of soil nutrients andmicrobial symbionts associated with the root system.Recent work in a semi-arid system suggested thatvegetation plays a more important role than soil instructuring extracellular enzymatic stoichiometry (Cuiet al. 2018); however, given the latent physiochemicalsimilarity of soils in this study, the short-term effect ofour direct litter additions may not be as strong as thelonger-term influence of plants shifting soil conditionsthrough litter build-up and rhizosphere processes. Inother words, plants likely dictate the soil effectsobserved here.The differences in Rs observed across soils seemsomewhat paradoxical given that willow litter decom-posed most fully on willow soils, yet Rs from salt cedarsoils was higher than other soils on most sample dates.C-hydrolyzing EEA (Я-1,4-glucosidase and NAG)were also lowest on willow soils, which appear to berelated to the low concentration of organic C at thetime of assays (Fig. 6). However, 13C enrichment inthose willow soil samples could be inferred to be aresult of high respiration losses in this experimentalsystem since we did not have to contend with isotopic vagaries introduced by active plant roots and mycor-rhizal fungi (Bhupinderpal-Singh 2003). When didthose respiration losses occur? There is not a strongtrend of high Rs at the beginning of the incubations andquickly dropping, but the loss of over 75% of the littermass by the end of the experiment implies that the Rssignature is more strongly dominated by the soil ratherthan the litter. We posit that this result argues forstudies of this nature to include multiple lines ofevidence that point to different time scales duringdecomposition. Mass loss is cumulative, gas flux is amore immediate metric of microbial activity, andenzyme activity data are better thought of as apotential measurement of decomposition but one thatis dependent on soil and litter properties (McLarenet al. 2017).Even though it is well established that Russian olivehosts symbiotic N2-fixing microbes, our end-of-incu-bation measurements showed that soil NH4? was thelowest on Russian olive soil, likely as a result of highnitrification/denitrification rates, and concomitantN2O from both of those pathways during the exper-iment. While N import may be a crucial factor inRussian olive invasiveness on N-poor soils, largegaseous N losses may preclude other species fromtaking advantage of those N inputs (DeCant 2008).Our data suggest that Russian olive may be accelarat-ing riparian N cycling instead of changing N pools in agiven area. Given that willow and cottonwood havelikely evolved under low N conditions, physicallyremoving Russian olive may be a viable restorationstrategy if N-rich litter is not increasing soil N pools given the high rates of N2O production we observerelative to other plant species litters. While we did nottrack changes in soil N through time, the finalchemical analysis showed that no litter type decom-posing on its native soil (i.e., cottonwood leaves oncottonwood-derived soil) exhibited the highestamount of soil NH4? (Fig. 2). However, cottonwoodsoil hosted the highest concentration of NO3- fromdecomposing cottonwood leaves (Fig. 3). The rela-tively high NO3- content of soils under cottonwood isworth further investigation as this property is related toN2O emissions as well, and has been correlated withcottonwood stand age in other parts of the southwest-ern USA (Stromberg 1998).While greater gaseous N losses would removelabile N from riparian soils and potentially create amore favorable environment for native tree reintro-ductions, it also suggests that areas invaded by Russianolive are potentially underappreciated sources of N2Oemissions to the atmosphere. Further work at thelandscape and regional scale needs to address thisinteraction between invasive shrub ecology andgreenhouse gas emissions via litter decomposition.


Andruschkewitsch R, Geisseler D, Dultz S, Joergensen RG,Ludwig B (2014) Rate of soil aggregate formation underdifferent organic matter amendments—a short-term incu-bation experiment. J Plant Nutr Soil Sc 177:297–306Audubon Society (2018) Accessed 1 Apr 2019Bailey JK, Schweitzer JA, Whitham TG (2001) Salt cedarnegatively affects biodiversity of aquatic macroinverte-brates. Wetlands 21:442–447Bhupinderpal-Singh NA, Ottosson Lцfvenius M, Hцgberg MN,Mellander PE, Hцgberg P (2003) Tree root and soil het-erotrophic respiration as revealed by girdling of borealScots pine forest: extending observations beyond the firstyear. Plant Cell Environ 26:1287–1296Bobbink R, Hicks K, Galloway J, Spranger T, Alkemade R,Ashmore M, Bustamante M, Cinderby S, Davidson E,Dentener F, Emmett B (2010) Global assessment ofnitrogen deposition effects on terrestrial plant diversity: asynthesis. Ecol Appl 20:30–59Brooks ML, D’antonio CM, Richardson DM, Grace JB, KeeleyJE, DiTomaso JM, Hobbs RJ, Pellant M, Pyke D (2004)Effects of invasive alien plants on fire regimes. Bioscience54:677–688Cui Y, Fang L, Guo X, Wang X, Zhang Y, Li P, Zhang X (2018)Ecoenzymatic stoichiometry and microbial nutrient limi-tation in rhizosphere soil in the arid area of the northernLoess Plateau, China. Soil Biol Biochem 116:11–21D’Antonio CM, Vitousek PM (1992) Biological invasions byexotic grasses, the grass/fire cycle, and global change.Annu Rev Ecol S 23:63–87DeCant JP (2008) Russian olive, Elaeagnus angustifolia, alterspatterns in soil nitrogen pools along the Rio Grande River,New Mexico, USA. Wetlands 28:896Doane TA, Horwбth WR (2003) Spectrophotometric determi-nation of nitrate with a single reagent. Anal Lett36:2713–2722Elton CS (1958) The ecology of invasions by animals and plants.University of Chicago Press, ChicagoGaskin JF, Schaal BA (2002) Hybrid Tamarix widespread in USinvasion and undetected in native Asian range. Proc NatAcad Sci 99(17):11256–11259Humphrey LD, Schupp EW (2004) Competition as a barrier toestablishment of a native perennial grass (Elymus ely-moides) in alien annual grass (Bromus tectorum) commu-nities. J Arid Environ 58:405–422Kennedy TA, Hobbie SE (2004) Saltcedar (Tamarix ramosis-sima) invasion alters organic matter dynamics in a desertstream. Freshwater Biol 49:65–76Khamzina A, Lamers JP, Vlek PL (2009) Nitrogen fixation byElaeagnus angustifolia in the reclamation of degradedcroplands of Central Asia. Tree Physiol 29(6):799–808Kourtev PS, Ehrenfeld JG, Hдggblom M (2003) Experimentalanalysis of the effect of exotic and native plant species onthe structure and function of soil microbial communities.Soil Biol Biochem 35:895–905Ludwig F, Dawson TE, Prins HH, Berendse F, De Kroon H(2004) Below-ground competition between trees andgrasses may overwhelm the facilitative effects of hydrauliclift. Ecol Lett 7:623–631McDonald AK, Wilcox BP, Moore GW, Hart CR, Sheng Z,Owens MK (2015) Tamarix transpiration along a semiaridriver has negligible impact on water resources. WaterResour Res 51:5117–5127McLaren JR, Turkington R (2011) Plant identity influencesdecomposition through more than one mechanism. PLoSONE 6:e23702McLaren JR, Buckeridge KM, van de Weg MJ, Shaver GR,Schimel JP, Gough L (2017) Shrub encroachment in Arctictundra: Betula nana effects on above-and belowgroundlitter decomposition. Ecology 98:1361–1376Nagler PL, Morino K, Didan K, Erker J, Osterberg J, HultineKR, Glenn EP (2009) Wide-area estimates of salt cedar(Tamarix spp.) evapotranspiration on the lower ColoradoRiver measured by heat balance and remote sensingmethods. Ecohydrology 2:18–33Nsikani MM, van Wilgen BW, Gaertner M (2018) Barriers toecosystem restoration presented by soil legacy effects ofinvasive alien N2-fixing woody species: implications forecological restoration. Restor Ecol 26:235–244Predick KI, Turner MG (2008) Landscape configuration andflood frequency influence invasive shrubs in floodplainforests of the Wisconsin River (USA). J Ecol 96:91–102bFig. 6 Microbial exo-enzyme activity rates in response to soilorganic C (%) and d13C values following a 90-day laboratoryincubations of invasive and native leaf litter decomposing underidentical abiotic conditions on soils collected under each of thefour plant species in a fully reciprocal design, i.e., all litter typeswere decomposed on all soil types. Soil origin is denoted bysymbols, and leaf litter decomposed during the experiment ishighlighted by symbol color. d13C is given as %. Error barsare ± 1 standard deviation from the mean123Plant Ecol
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R Core Team (2018) R: A Language and Environment forStatistical Computing. R Foundation for Statistical Com-puting, AustriaReynolds LV, Cooper DJ (2010) Environmental tolerance of aninvasive riparian tree and its potential for continued spreadin the southwestern US. J Veg Sci 21:733–743Rhoades CC (1996) Single-tree influences on soil properties inagroforestry: lessons from natural forest and savannaecosystems. Agrofor Syst 35:71–94Rice SK, Westerman B, Federici R (2004) Impacts of the exotic,nitrogen-fixing black locust (Robinia pseudoacacia) onnitrogen-cycling in a pine–oak ecosystem. Plant Ecol174:97–107Saiya-Cork KR, Sinsabaugh RL, Zak DR (2002) The effects oflong term nitrogen deposition on extracellular enzymeactivity in an Acer saccharum forest soil. Soil Biol Bio-chem 34:309–1315Shepard JP, Creighton J, Duzan H (2004) Forestry herbicides inthe United States: an overview. Wildlife Soc B32:1020–1027Sinsabaugh RL, Saiya-Cork K, Long T, Osgood MP, Neher DA,Zak DR, Norby RJ (2003) Soil microbial activity in aLiquidambar plantation unresponsive to CO2-drivenincreases in primary production. Appl Soil Ecol24:263–271Stromberg JC (1998) Functional equivalency of saltcedar (Ta-marix chinensis) and Fremont cottonwood (Populus fre-montii) along a free-flowing river. Wetlands 18:675–686Van Der Heijden MG, Bardgett RD, Van Straalen NM (2008)The unseen majority: soil microbes as drivers of plantdiversity and productivity in terrestrial ecosystems. EcolLett 11:296–310van Hylckama TEA (1970) Water use by salt cedar. WaterResour Res 6:728–735Wardle DA, Bonner KI, Nicholson KS (1997) Biodiversity andplant litter: experimental evidence which does not supportthe view that enhanced species richness improves ecosys-tem function. Oikos 79:247–258Weatherburn MW (1967) Phenol-hypochlorite reaction fordetermination of ammonia. Anal Chem 39:971–974