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Ecological Research

, Volume 33, Issue 1, pp 261–269 | Cite as

Growth responses of Canada goldenrod (Solidago canadensis L.) to increased nitrogen supply correlate with bioavailability of insoluble phosphorus source

  • Ling-Yun Wan
  • Shan-Shan Qi
  • Zhi-Cong Dai
  • Chris B. Zou
  • Yi-Ge Song
  • Zhi-Yuan Hu
  • Bin Zhu
  • Dao-Lin Du
Original Article
  • 240 Downloads

Abstract

Anthropogenic nitrogen (N) inputs lead to the increase of phosphorus (P) demand for plants and plant species competition in a N enriched environment may hinge on its ability to utilize soil P sources. In soils, P mostly exists as insoluble phosphate compounds with three mineral elements: iron (Fe), aluminum (Al) or calcium (Ca), and it remains largely unknown whether invasive plant species are able to access such insoluble P sources and its interaction with N enrichment to gain competitive advantage. We determined the morphological traits, growth and nutrient status of an invasive plant Canada goldenrod (Solidago canadensis L.) cultured in soluble phosphate KH2PO4 (Ortho-P), and insoluble inorganic phosphate AlPO4 (Al–P), FePO4 (Fe–P), Ca5(OH)(PO4)3 (Ca–P) at three N supply levels. Results showed that S. canadensis was able to selectively utilize P from Al–P but not from Fe–P or Ca–P by increasing root number and length under N additions. The increasing growth in S. canadensis was closely correlated with the increasing foliar P. Ability to utilize insoluble P sources under enriched N environment serves as a competitive advantage for S. canadensis in Al rich soils. Effective control of S. canadensis invasion may need to consider soil P management in the context of atmospheric N deposition as well.

Keywords

Canada goldenrod (Solidago canadensis L.) Insoluble phosphorus Nitrogen addition Growth 

Introduction

Nitrogen (N) has been considered an important limiting nutrient for primary productivity in many terrestrial ecosystems, particularly in temperate forest ecosystems with relatively young soils (Vitousek and Howarth 1991). Owing to increasing anthropogenic nutrient inputs, such as the deposition of fossil fuel-associated N (Foley et al. 2005), global cycles of N have been amplified by approximately twice (Falkowski et al. 2000), and it is expected to increase further in the coming decades (Liu et al. 2013). Previous researches suggest that atmospheric N deposition may facilitate the fast growing plant species, such as some invasive plants, to compete successfully against native species that previously tolerate a low N level in plant community. For example, Brooks (2003) has reported that N addition increases the growth of invasive plants in the Mojave Desert. Tomassen et al. (2004) have found that the invasive grass Molinia caerulea is stimulated by enriched N level similar to the level of atmospheric N deposition. Increasing N deposition may, therefore, play a major role in enhancing plant invasion.

However, N may be no longer a restricting factor of primary productivity in previous N-limited ecosystems which continually receive high N input, and increased N availability induces high demand for biotic phosphorus (P) (Mohren et al. 1986; Gress et al. 2007). Previous studies on plant invasion caused by N deposition rarely discussed the side effects of N enrichment on P bioavailability. In fact, enhanced N supply may cause P deficiency (very high N:P ratio) in soils and suppress biomass production (Huang et al. 2012).

P is required as structural components and energy molecules for plant growth (Satyavir et al. 2014), including cell division, photosynthesis and respiration, nutrient transport, genetic expression and metabolic pathways (Zaidi et al. 2009; Elser 2012). In fact, soil total P is usually high in many terrestrial ecosystems. However, P is often sorbed to aluminum (Al) and iron (Fe) exposed at the surfaces of soil constituents in acid soils or to calcium (Ca) in calcareous soils (Holford 1997). These insoluble phosphates are usually considered to be low in bioavailability for plants (Behera et al. 2013). The bioavailability of insoluble phosphate to plants is documented to change under the following two conditions: (1) species special adaptation strategies, including root structural specializations (Williamson et al. 2001; Hu et al. 2010), exudation of compounds (Ryan et al. 2001; Shen et al. 2003), mycorrhizal symbioses (Smith et al. 2011) will result in increase of the bioavailability of insoluble phosphate to plants. Certainly, it is unlikely that a given adaptation can improve access to multiple forms of insoluble P sources for a certain plant species. For example, Canola (Brassica napus L.) is able to access hydroxyapatite almost as readily as it utilizes soluble P, but access AlPO4 and FePO4 less readily (Hoffland et al. 1989; Pearse et al. 2007). The bioavailability of the same insoluble P form is also species specific. For example, AlPO4 is unavailable to field pea (Pisum sativum L.) and chickpea (Cicer arietinum L.) (Pearse et al. 2007), but it is available to wheat (Triticum aestivum L.) (Wang et al. 2011). (2) Soil environmental change such as modification of soil pH may also alter the bioavailability of insoluble phosphate to plants (Hinsinger 2001). Several studies show that N addition leads to soil acidity, causing depletion of base cations, and mobilizing soil Al and Fe, therefore, increasing the levels of Al/Fe phosphate compounds and reducing the P bioavailability in the soil (Zhang et al. 2013).

Many studies have explored the ability of crops to acquire P from various insoluble forms (Pearse et al. 2006, 2007, 2008; Wang et al. 2010, 2011). Currently, minimal effort has been made to understand the adaptive strategies of invasive plants on limiting P sources, especially under the N deposition. Such information is important in improving our mechanistic understanding of invasive species competition with native species and guiding the effective control of invasive species. The objective of this study is to understand the growth responses of an invasive plant Canada goldenrod (Solidago canadensis L.) to increased N supply under insoluble inorganic P from soils of high Al/Fe or Ca contents. Specific questions to be answered through this study include: (1) does growth performance of S. canadensis differ among different insoluble inorganic P sources under N addition? (2) Has the increased growth performance resulted from increased P uptake from inorganic insoluble P sources?

Materials and methods

Study species

Solidago canadensis L. (Asteraceae) was introduced from North America into China as an ornamental plant in 1913 (Li et al. 2001; Jin et al. 2004). Due to its rapid growth and prolific vegetative and generative propagations (Dong et al. 2006a), strong allelopathic effects (Yang et al. 2007; Butcko and Jensen 2009) and closely symbiosis with arbuscular mycorrhizal fungi (Yang et al. 2014), S. canadensis can form near monoculture in its introduced range. Moreover, its seeds are small, numerous and wind dispersed, which facilitates long-distance dispersal (Dong et al. 2006b), S. canadensis has become one of the most aggressive invasive perennial species in China and is widely distributed in several provinces of eastern China, such as Jiangsu, Shanghai, Zhejiang, Jiangxi, and Anhui (Dong et al. 2006b; Lu et al. 2007).

Seeds and preparatory work

Seeds of S. canadensis were collected from the disturbed habitats in the campus of Jiangsu University in Zhenjiang, China (32°20′N, 119°51′E) in November 2014 and stored at 0–4 °C in the fridge. In mid-April 2015, seeds of S. canadensis were put on the surface of the soil in plastic containers (30 × 20 × 8 cm, length × width × height), which were filled with washed and sterilized river sand. During the seed germination, adequate distilled water was supplied to seedlings every 2 days. 0.5× Hoagland solutions were supplied weekly.

Design of nutrient addition experiment

River sand was sieved through a 2-mm mesh sieve and thoroughly washed under running tap water, finally was autoclaved 2 h at 121 °C. The treated sand was packed into plastic plots (15 cm height and 10 cm diameter). We combined four sources of P and three N supply levels in a full factorial design. The resulting twelve treatments were replicated five times. The P treatments comprised the total amount of P was 45.00 mg kg−1 river sand. The three insoluble inorganic P sources: aluminum phosphate (AlPO4, Al–P), iron phosphate (FePO4, Fe–P), hydroxyapatite (Ca5(OH)(PO4)3, Ca–P), and a soluble inorganic P source: potassium dihydrogen phosphate (KH2PO4, Ortho-P), as the control treatment. The four different P sources were added in powder form and then mixed with the sand for each pot before the transplantation of seedling.

The three supply levels of N included no N supply which served as a control level (0.00 mg kg−1; CK), low N level (45.00 mg kg−1; L-N), and high N level (135.00 mg kg−1; H-N). N applied as the mixed solutions of KNO3 and NH4Cl (1:1, M/M), according to the report that the ratio of NO3–N and NH4–N of atmospheric N deposition in recent years in China (Liu et al. 2013). For potassium (K), part of this amount was provided by the compounds used to supply N and P, and the rest by adding KCl to ensure that all treatments received the same amount of K, while all other basal nutrients (i.e. Ca, S, Mg, Fe, B, Mn, Zn, Mo, Cu) were supplied in constant by modified Hoagland solutions (no N and P), non-limiting amounts (Pearse et al. 2007).

When the seedlings produced two cotyledons between 2 and 3 cm in height, they were transplanted into plastic pots in April 2015. The N addition was applied once a week for 3 months beginning when the leaves started to bud (from April 20, 2015 to July 20, 2015). There were 12 treatment combinations in total and each combination contained five pots as replicates. The experiment was performed in a greenhouse at Jiangsu University in Zhenjiang China (temperature: 26 ± 2 °C; relative humidity: 62 ± 2% mean ± SE; photosynthetic photon flux density (PPFD) during the day: approximately 300 µmol m−2 s−1). Each replicate was repositioned randomly every week to avoid the effects of possible environment patchiness within the greenhouse. Enough distilled water was supplied to seedlings every 2 days.

Measurements

After 84 days of nutrition treatments, plant height, stem base diameter and the number of leaves were measured before seedlings harvested. The roots were carefully separated from the soil and rinsed with water for later measurement. Seedlings separated into root, shoot (leaf and stem) fractions. Fresh roots were first gently washed with tap water. Approximately 100 mg of fresh fine root was subsampled for each plant to estimate root length. A digital photo was taken for each subsample. Digital images were analyzed to estimate root length using ImageJ software (National Institutes of Health, USA), after which specific root length (SRL; m g−1 root FW) was calculated. Total root length was calculated by multiplying SRL by total root fresh weight. Leaf area was also taken a digital photo and then calculated with ImageJ software. Sand pH was measured with a Metrohm-744 pH meter with a combined glass electrode after extraction in deionized water for 30 min at sand:water ratio of 1:5 (Li et al. 2010).

Final biomass of all seedling parts was measured after drying at 60 °C for 72 h. Root to shoot ratio (RSR) was calculated as the proportion of root biomass to shoot biomass. Shoot and root fractions of all seedlings were ground and analyzed for N and P concentration. After a digestion procedure (Kjeldahl digestion method; 1 h at 200 °C and 2 h at 340 °C in a mixture of concentrated sulfuric acid and 30% hydrogen peroxide) (Fujita et al. 2010), then they were cooled and diluted with deionized water to 45 ml. N and P concentration were determined colorimetrically using UV-1200 spectrophotometer (MAPADA, Shanghai, China). P uptake was calculated by multiplying concentration by biomass.

Statistical analysis

Two-way analysis of variance (ANOVA) was performed to test the effects of N levels, P sources and their interactions. One-way ANOVA and Tukey–Kramer method’s multiple range tests at P < 0.05 were conducted to find whether significant differences existed among treatments. Before ANOVA, the data were checked for normality and homogeneity of variance. Values for plant height, stem base diameter, shoot biomass, total biomass, P uptake, and N:P ratio was log(x + 1) transformed to satisfy normality and homogeneity of variance. All statistical analyses were performed with SPSS statistics (version 22.0; IBM, Armonk, NY, USA). All figures were drawn with the Origin 9.1 software (Originlab Co., Northampton, MA, USA).

Result

Growth

The growth of S. canadensis was greatly affected by N levels and P sources (Table 1A). Shoot biomass significantly increased in the presence of N addition when plants were grown with Ortho-P or Al–P. However, when P was supplied as Ca–P, N addition had no significant effect on shoot biomass (Fig. 1a). Low N level significantly stimulated an increase of root biomass when plants were grown with Ortho-P or Al–P. However, compared to low N level, root biomass significantly decreased at high N level when plants were grown with Ortho-P or Al–P. Root biomass was the highest in the presence of N addition when P was supplied as Al–P (Fig. 1b). For Fe–P or Ca–P, root biomass decreased in the presence of N addition. At high N level, root biomass was the lowest in Ca–P (Fig. 1b). Effects of N levels and P sources on total biomass were similar with shoot biomass (Fig. 1c). Regardless of P sources, RSR in the presence of N addition significantly decreased compared to the CK level (Fig. 1d).
Table 1

Two-way ANOVA of the effects of nitrogen addition (N) and phosphorus source (P) on the plant growth, morphological trait and P nutrient status of Solidago canadensis

Dependent variable

N level

P source

N × P

(A) Plant growth

  Shoot biomass

< 0.001

< 0.001

< 0.001

  Root biomass

< 0.001

< 0.001

< 0.001

  Total biomass

< 0.001

< 0.001

< 0.001

  RSR

< 0.001

0.378

0.008

(B) Morphological trait

  Plant height

< 0.001

< 0.001

< 0.001

  Number of leaves

< 0.001

< 0.001

< 0.001

  Leaf area

< 0.001

< 0.001

< 0.001

  Stem base diameter

< 0.001

< 0.001

< 0.001

  SRL

< 0.001

< 0.001

0.018

  Total root length

< 0.001

< 0.001

< 0.001

(C) P nutrient status

  Foliar P concentration

0.008

< 0.001

< 0.001

  P uptake

< 0.001

< 0.001

< 0.001

Results were considered statistically significant at P < 0.05

Fig. 1

Shoot biomass (a), root biomass (b), total biomass (c) and root to shoot ratio (d) of Solidago canadensis grown in different phosphorus sources subjected to three nitrogen treatments. CK indicates no nitrogen supply, L-N indicates low nitrogen level, and H-N indicates high nitrogen level. Different letters denote significant differences (P < 0.05) with Tukey–Kramer test. Data shown as the mean ± standard error of the mean (n = 5)

Morphological traits

The morphological traits of S. canadensis were all significantly affected by N levels and P sources (Table 1B). Plant height and number of leaves increased in the presence of N addition when plants were grown with Ortho-P, Al–P or Fe–P. However, when P was supplied as Ca–P, N addition had no significant effect on plant height and number of leaves (Fig. 2a and 2b). Regardless of P sources, leaf area increased in the presence of N addition. At high N level, leaf area was significantly greater in Ortho-P or Al–P compared with Fe–P or Ca–P, rank order of leaf area was Ortho-P ≈ Al–P > Fe–P > Ca–P (Fig. 2c). Stem base diameter significantly increased but SRL decreased in the presence of N addition when plants were grown with Ortho-P or Al–P. However, when P was supplied as Fe–P or Ca–P, N addition had no significant effect on stem base diameter and SRL. At high N level, stem base diameter was the highest but SRL was the lowest in Ortho-P (Fig. 2d and 2e). Low N level significantly stimulated an increase of total root length when plants were grown with Al–P or Fe–P. However, compared to low N level, total root length significantly decreased at high N level when plants were grown with Al–P or Fe–P. Total root length was the highest in the presence of N addition when P was supplied as Al–P (Fig. 2f).
Fig. 2

Plant height (a), number of leaves (b), leaf area (c), stem base diameter (d), SRL (e) and total root length (f) of Solidago canadensis grown in different phosphorus sources subjected to three nitrogen treatments. CK indicates no nitrogen supply, L-N indicates low nitrogen level, and H-N indicates high nitrogen level. Different letters denote significant differences (P < 0.05) with Tukey–Kramer test. Data shown as the mean ± standard error of the mean (n = 5)

Foliar P concentration, P uptake and correlation with total biomass

Foliar P concentration and P uptake varied significantly in response to N levels and P sources (Table 1C). Foliar P concentration was significantly higher in Ortho-P or Al–P than that in Ca–P at CK level. Low N level stimulated an increase of foliar P concentration in Ortho-P or Al–P, but significantly decreased foliar P concentration in Fe–P or Ca–P. Compared with low N level, foliar P concentration decreased at high N level when plants were grown with Ortho-P or Al–P. The rank order of foliar P concentrations in the presence of N addition was: Ortho-P > Al–P > Fe–P ≈ Ca–P (Fig. 3a).
Fig. 3

Foliar P concentration (a) and P uptake (b) of Solidago canadensis grown in different phosphorus sources subjected to three nitrogen treatments. CK indicates no nitrogen supply, L-N indicates low nitrogen level, and H-N indicates high nitrogen level. Different letters denote significant differences (P < 0.05) with Tukey–Kramer test. Data shown as the mean ± standard error of the mean (n = 5)

Compared to the CK level, P uptake significantly increased in the presence of N addition when plants were grown with Ortho-P or Al–P. However, when P was supplied as Fe–P or Ca–P, N addition had no significant effect on P uptake (Fig. 3b).

Positive relationships among foliar P concentration, P uptake and total biomass were observed. Both the increasing foliar P concentration and P uptake were closely correlated with the increasing total biomass (Fig. 4).
Fig. 4

Relationship between foliar P concentration (a) or P uptake (b) and total biomass of Solidago canadensis

N:P ratio

There was no significant effect of N addition on N:P ratio when P was supplied as Ortho-P or Al–P. However, In the presence of N addition, N:P ratio significantly increased when P was supplied as Fe–P or Ca–P, and N:P ratio of Ca–P was significantly higher than that of Fe–P (Fig. 5).
Fig. 5

N:P ratio of Solidago canadensis grown in different phosphorus sources subjected to three nitrogen treatments. CK indicates no nitrogen supply, L-N indicates low nitrogen level, and H-N indicates high nitrogen level. Different letters denote significant differences (P < 0.05) with Tukey–Kramer test. Data shown as the mean ± standard error of the mean (n = 5)

Sand pH

In the presence of N addition, although the pH value significantly decreased when plants were grown with Ortho-P or Al–P, the pH value of Al–P was significantly higher than that of Ortho-P. There was no significant effect of N addition on the pH when P was supplied as Ca–P (Fig. 6).
Fig. 6

Sand pH of Solidago canadensis grown in different phosphorus sources subjected to three nitrogen treatments. CK indicates no nitrogen supply, L-N indicates low nitrogen level, and H-N indicates high nitrogen level. Different letters denote significant differences (P < 0.05) with Tukey–Kramer test. Data shown as the mean ± standard error of the mean (n = 5)

Discussion

In our study, we found that there were significant differences in growth responses of S. canadensis grown under four P sources to N enrichment, and the increasing foliar P concentration and P uptake were closely correlated with increasing total biomass in S. canadensis (Fig. 4). Therefore, we conclude that differences in P bioavailability of inorganic P sources can determine growth responses of S. canadensis to N addition. We found that P uptake significantly increased in the presence of N addition when P source was soluble Ortho-P, which shows that N input increases P uptake and promotes the growth when P availability is high. This is in agreement with Zhao et al. (2010) that N addition increases root P uptake and plant growth due to the increase of biotic P demand.

We also found that in the presence of N addition, the growth of S. canadensis reduced slightly in Fe–P. Compared with that in Ortho-P, N addition almost had no significant effects on P uptake and plant growth of S. canadensis when P was supplied as Ca–P. N:P ratios of plants directly indicate the nutrient demand of plant growth (Koerselman and Meuleman 1996; Güsewell and Koerselman 2002; Tessier and Raynal 2003). N:P ratios of S. canadensis grown in Fe–P or Ca–P were higher than 10 (Fig. 5), indicating S. canadensis had high P biotic demand. However, P in Fe–P or Ca–P is strongly bound by iron (Fe) or calcium (Ca), which makes P availability very low (Bhadoria et al. 2002). Thus, a contrast in high biotic P demand and low P availability may cause no effect of N addition on the growth of S. canadensis. A recent study demonstrated that P availability alters stability of nitrate transporter protein (Medici et al. 2015) and P concentrations in foliar, litter, and fine roots might not change by N fertilization under certain conditions (Weand et al. 2010).

Surprisingly, Al–P was also inorganic insoluble P source, but the growth of S. canadensis was not limited by Al–P (N:P ratios < 10) (Fig. 5). The growth of S. Canadensis in Al–P was not significantly different from that in Ortho-P. Also, P uptake also significantly increased with N addition, suggesting that S. canadensis is able to access P from Al–P. Our results are in agreement with findings that wheat (Triticum aestivum) is capable of accessing Al–P (Pearse et al. 2006; Wang et al. 2011). We propose the following adaptive strategies for increasing P uptake from Al–P to satisfy P biotic demand caused by N addition: (1) a greater number of root and longer roots allow S. canadensis to scavenge a greater volume of soil and increase the surface area of the root system in contact with soil for P uptake (Figs. 1b, 2f); (2) acidification caused by N addition is alleviated by Al (Fig. 6). The excessive anions (nitrate) uptake is balanced by OH or HCO3 extrusion to hamper P bound by Al3+ (Gahoonia et al. 1992), and at a given partial neutral pH, Al–P has a higher solubility than Fe–P or Ca–P (Otani and Ae 1996); (3) Al might be stimulating malate release and in advertently enhancing the P uptake (Pearse et al. 2006); (4) chelation constants of Al by citrate, malate and other organic anions are higher than for Fe (Struthers and Sieling 1950); and (5) iron toxicity may affect plant growth (Perez Corona et al. 1996). S. canadensis is widely distributed in several provinces of southern China, such as Jiangsu, Shanghai, Zhejiang, Jiangxi, and Anhui (Dong et al. 2006b; Lu et al. 2007) where acid soils widely exist (Zhao et al. 2015). In acid soil, majority of soil P fractions was Al–P (Holford 1997), so the area of S. canadensis invasion in China correlates with insoluble Al–P sources. Without effective control measure in place, continuous invasion of S. canadensis in southern China is anticipated with the anthropogenic N inputs.

Future experiments will simulate more biotic and abiotic environmental factors likely to affect growth of invasive plant S. Canadensis in insoluble phosphate conditions. Firstly, N addition exhibits P source specific influences on the growth of the invasive plant S. canadensis. S. Canadensis cannot access insoluble P in Fe–P and Ca–P, but this does not necessarily mean that other species cannot access those forms of insoluble P either. Field pea (Pisum sativum L.) and chickpea (Cicer arietinum L.) were found to be capable of acquiring P from Ca–P (Pearse et al. 2007). Secondly, N:P ratios in some growth conditions (e.g., Ortho-P or Al–P in Fig. 5) in this study were relatively low since continuous increase in N addition will lead to soil acidity, reducing P availability of Al–P, but available N might be not sufficient for plant growth (Zhang et al. 2013). Thirdly, P availability is normally highest at the upper layers and decreases with depth due to relative immobility of P in soils, making P acquisition dependent on root architecture (Lynch 2011). Therefore, comparative analysis of root architectural parameters such as growth angles of axial roots, adventitious rooting, number of axial roots, and dispersion of lateral roots in adaptation to insoluble P forms will be valuable. Finally, our study was conducted in the greenhouse under low light condition for plant growth affecting net photosynthesis rate and this difference may interact with P availability to affect plant growth (Wissuwa et al. 2005).

In summary, this study improves out mechanistic understanding of the growth responses of an invasive species Canada goldenrod to increased N supply under different P conditions and the results will assist control of invasive species through phosphorus management in the context of atmospheric N deposition.

Notes

Acknowledgements

This work was supported by the State Key Research Development Program of China (2017YFC1200103). the National Natural Science Foundation of China (31570414, 31770446), the Natural Science Foundation of Jiangsu (BK20150503, BK20150504), the Research and Innovation Project for College Graduates of Jiangsu Province (KYLX15_1088, 15A316, 15A318), the China Postdoctoral Science Foundation (2016M590416, 2017T100329), and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD). This work was also supported by the USDA National Institute of Food and Agriculture through McIntire-Stennis project to C.B. Zou and the Division of Agricultural Sciences and Natural Resources at Oklahoma State University.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

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Copyright information

© The Ecological Society of Japan 2017

Authors and Affiliations

  • Ling-Yun Wan
    • 1
    • 3
  • Shan-Shan Qi
    • 1
  • Zhi-Cong Dai
    • 1
    • 2
  • Chris B. Zou
    • 3
    • 4
  • Yi-Ge Song
    • 1
  • Zhi-Yuan Hu
    • 1
  • Bin Zhu
    • 5
  • Dao-Lin Du
    • 1
    • 2
  1. 1.Institute of Environment and Ecology, Academy of Environmental Health and Ecological Security, School of the Environment and Safety EngineeringJiangsu UniversityZhenjiangChina
  2. 2.Institute of Agricultural EngineeringJiangsu UniversityZhenjiangChina
  3. 3.Department of Natural Resource Ecology and ManagementOklahoma State UniversityStillwaterUSA
  4. 4.Ecohydrology Research Institute, The University of Tokyo Forests, Graduate School of Agricultural and Life SciencesThe University of TokyoSetoJapan
  5. 5.Department of BiologyUniversity of HartfordWest HartfordUSA

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