Biol Invasions DOI 10.1007/s10530-016-1231-1 ORIGINAL PAPER Response of an invasive plant, Flaveria bidentis, to nitrogen addition: a test of form-preference uptake Chaohe Huangfu . Huiyan Li . Xinwei Chen . Hongmei Liu . Hui Wang . Dianlin Yang Received: 29 August 2015 / Accepted: 9 July 2016 Ó Springer International Publishing Switzerland 2016 15 ? Abstract Plants differ in their capacity to use higher N–NH4 recovery across biomass compo- various forms of nitrogen (N). Although previous nents than both co-occurring native plants, Amaran- studies have suggested invasive plants alter N avail- thus retroflexus and Eclipta prostrata. F. bidentis ability, few distinguish their responses to various demonstrated a strong preference for ammonium ? - forms and different concentrations of inorganic N. In (NH4 ) over nitrate (NO3 ) and captured at least 15 ? order to understand how plant preference for N affects twice the N–NH4 as the native plants. By compar- invasions, we tested the growth and physiological ison, the two native species showed no preferences for response of Flaveria bidentis, an invasive plant across the form of N. The greater above-ground biomass of F. north China, to different forms and concentrations of bidentis contributed to its higher 15N recovery. We inorganic N. Seedlings of F. bidentis were cultivated suggest that the ability of F. bidentis to respond in a mothproof screen house to determine if this rapidly to changes in the N pool, especially in invader benefits from increased or altered forms of N. ammonium, may confer a competitive advantage to 15 ? - N-labeled NH4 and NO3 were applied to the soil this species over native species. Our results provide to gain insight into N partitioning in communities insight into how species-specific N preferences influ- invaded by this species. We determined that plant ence the ability of this species to invade a native growth and biomass variables, chlorophyll content, community. and photosynthesis parameters all varied depending on the form of available N. Specifically, N addition Keywords Ammonium Á Biomass allocation Á altered the biomass allocation pattern of plants, with F. Invasive plant Á Nitrate Á N preference Á Stable isotopes bidentis tending to maximize its reproductive output under increased N availability. Also, F. bidentis had Introduction Electronic supplementary material The online version of this article (doi:10.1007/s10530-016-1231-1) contains supple- Plant invasion, serving as a driver of global environ- mentary material, which is available to authorized users. mental change, threatens native biodiversity in many C. Huangfu Á H. Li Á X. Chen Á H. Liu Á areas, leading to profound changes in ecosystem H. Wang Á D. Yang (&) processes and function (Vila` et al. 2011), and Agro-Environmental Protection Institute, Ministry of community structure (Callaway et al. 2005; Hierro Agriculture, 31 Fukang Road, Nankai District, Tianjin 300191, China et al. 2005; Yelenik et al. 2004). Plant species differ in e-mail: [email protected] their ability to take up soil nutrients, and nutrient 123 C. Huangfu et al. mining by invasive plants can affect ecosystem introduced to many countries in Africa, Asia, nutrient cycling (Ehrenfeld 2003). Variations in the Australia, Central and North America and Europe effects of plants on and their responses to nutrient (Gao et al. 2004). In China, F. bidentis was first cycling can result in dynamic feedbacks that influence found in 2001 in the suburbs of Tianjin and a few plant community composition and contributes to cities of Hebei Province (Liu 2005). It invades a invader persistence; however, few studies have wide range of habitats, such as roadsides, abandoned focused on these resource-based feedback mecha- fields or crop fields, outcompeting natural vegetation nisms (Bever et al. 2010). and forming dense, nearly monospecific stands Resource acquisition is one of the main ways that (Huangfu et al. 2011). F. bidentis tolerates environ- invasive species affect invaded communities. Some mental stress from salinity and cold temperature, and invasive plants can increase soil nitrogen (N) pools interferes with the development of sustainable by two orders of magnitude (Corbin and D’Antonio agriculture (Gao et al. 2004). Some evidence shows ? 2004; Vitousek and Walker 1989), thus altering the that elevated levels of N, especially NH4 , are competitive balance in favor of fast-growing inva- associated with F. bidentis invasions in agricultural sive species. Other plants affect N cycling by soils (Zhang et al. 2010). In a recent field study, the altering the ratio of soil N forms through litter presence of F. bidentis resulted in a decreased decomposition and uptake (Aanderud and Bledsoe potential nitrification rate relative to co-occurring 2009). If invasive species use nutrient resources native species in sites in both Jinghai county, Tianjin - more efficiently than native species, this may and Hengshui city, Hebei, where soil NO3 pools change resource flows and create feedbacks affect- were significantly depleted compared with unin- ? ing community biodiversity and ecosystem function vaded sites. In contrast, NH4 pools in invaded soils (Funk and Vitousek 2007; Gross et al. 2005; Pickart were generally stable or elevated (Zhao et al. 2015). et al. 1998). Nutrient acquisition strategies may Because invaded habitats are generally N deficient include details of nutrient uptake, mycorrhizal (Zhao et al. 2015), there is much interest in associations, nutrient requirements, and chemical understanding how the persistence of F. bidentis form preferences, among others. Species’ prefer- alters soil N cycling. It is unknown if F. bidentis ences for specific chemical forms of N can influence responds differently to added N forms, and the the coexistence and distribution of species within degree to which F. bidentis productivity is enhanced some sites (Andersen and Turner 2013). Invasive in the presence of specific N forms relative to co- plants tend to increase nitrification rates (Liao et al. occurring native species is poorly understood. 2008). However, little is known about the role of Soil N is particularly important in sustaining plant changes in N form in driving plant function (e.g., growth and regulating photosynthesis (Vitousek and species-specific N form-preference) or how it affects Farrington 1997). In this study, we first compared the ability of different plants to assimilate nitrate growth and biomass variables along with photosyn- - ? (NO3 ) versus ammonium (NH4 ) (de Graaf et al. thetic parameters of F. bidentis in response to N 1998; Olsson and Falkengren-Grerup 2000). Inva- addition of different forms and concentration (includ- sive species that can monopolize soil nutrient pools ing N deficiency). In the second experiment, using 15N will directly or indirectly suppress native species tracers, two native co-occurring species, Amaranthus (Ehrenfeld 2003). If these invasive species are retroflexus L. (C4 plant, Amaranthaceae) and Eclipta susceptible to increases in total N availability or prostrata (L.) L. (C3 plant, Asteraceae), were added to have different affinities for specific N forms, this experimentally quantify the acquisition of chemical type of positive feedback may further promote their forms of N. We measured recovery of 15N-ammonium 15 ? 15 15 - invasion or accelerate the spread of existing invasive ( NH4 ) and N-nitrate ( NO3 ) by the invader and species. by these two native species. We were specifically A newly introduced non-native invasive weed, interested in determining whether F. bidentis showed a Flaveria bidentis (L.) Kuntze (C4 annual herb, preference for one chemical form of N when compared Asteraceae), commonly called ‘‘yellowtop’’, is with the native plant species and in determining if this increasingly prevalent in northern China. This preference induced shifts in biomass allocation and species originated in South America and has been physiological variables. 123 Response of an invasive plant, Flaveria bidentis, to nitrogen addition Materials and methods australis, Artemisia scoparia and Artemisia annua. After cover vegetation was removed, the top 10 cm of Seedling establishment soil was collected and then passed through a 2 cm sieve to remove stones and coarse woody debris. Forest topsoil Seeds of three species, A. retroflexus, E. prostrata, and was used to provide a substrate with a natural supply of F. bidentis were collected from a site located on the macro- and micro-nutrients, and to increase soil perme- north shore of Tuanbo Lake (38°54.40N, 117°8.460E) ability in the experimental pots. We used field soil rather Jinghai County, Tianjin, China, from September– than sand culture to empirically mimic the conditions October, 2010. Climate at this site is temperate/warm that the test species experienced in the same climatic temperate, with a mean temperature of 11.8 °C. region. Before the treatments, the physical and chemical Annual precipitation is approximately 582 mm, fall- properties of the soil in pots were determined, and were ing primarily from June to August. Bulk seed collec- as follows: pH (7.2), total organic C (28.25 g kg-1), total -1 - -1 ? tions were made from 10 to 30 plants for each species; N (1.85 g kg ), NO3 –N (26.82 mg kg )andNH4 – seeds were cleaned and dry-stored in darkness at room N (4.36 mg kg-1). This potting soil N level falls within temperature (ca. 20 °C) until sowing. F. bidentis the range of N for various habitats previously invaded by produces small, water-dispersed seeds with a thousand F. bidentis (Zhao et al. 2015;Tuetal.2013). grain weight of 204.2 mg, which germinate in the field Next, seeds of the test species were sown at depths from May–October (Zhang et al. 2010). Laboratory of 0–2 cm depending on seed size. Seeds were misted seed germination trials indicated that this species is twice daily to maintain soil humidity at field capacity light-demanding, with a very low germination rate gravimetrically once a day at the germination stage. (0 %) under dark conditions (below 1 cm soil; Afterwards, all pots were watered three times weekly unpublished data).