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Arbuscular mycorrhizal (AM) status in urban wetland plants and its impact factors
Aquatic Botany 150 (2018) 33–45
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Aquatic Botany journal homepage: www.elsevier.com/locate/aquabot
Arbuscular mycorrhizal (AM) status in urban wetland plants and its impact factors ⁎
T
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Shuguang Wanga, , Dongwei Daia, Shuang Songa, Xiaojun Diaob, , Leimeng Maa a b
Department of Environmental Science and Engineering, Beijing University of Chemical Technology, Beijing, China Appraisal Center for Environment and Engineering, Ministry of Environmental Protection, Beijing, China
A R T I C LE I N FO
A B S T R A C T
Keywords: Arbuscular mycorrhizal symbiosis Urban wetland Mycorrhizal colonization rate Water Property Sediment Property
Urban wetlands play an important role in improving urban environment and microclimate, while they are suffering degradation and destruction during urbanization process. Arbuscular mycorrhizae may enhance plant tolerance to environmental stresses and increase vegetation restoration in wetlands. However, presently little is known how about arbuscular mycorrhizal (AM) symbiosis in urban wetland plants and the factors affecting AM formation. Here, a survey for AM status in urban wetland plants was done in Beijing area, and the factors affecting AM formation were also discussed, such as water and sediment characteristics. Results showed that 87.5% of plants (49 of 56 species) were colonized by AM fungi. Mycorrhizal colonization rates (MCRs) ranged from 2% to 72%, while most of them were low level (< 25%). The highest mycorrhizal colonization rate (MCR) was observed in Tephroseris palustris. Relationships between MCRs and water properties as well as sediment properties were analyzed by Pearson’s correlation analysis. MCRs in Phragmites australi were negatively correlated with water ammonium nitrogen and a total dissolved phosphorus, while were positively correlated with nitrate nitrogen, nitrite nitrogen and total organic carbon (TOC) in sediment. MCRs in Typha orientalis were negatively correlated with water oxidation-reduction potential while were positively correlated with sediment TOC. MCRs in Glyceria maxima were positively correlated with sediment nitrate nitrogen. MCRs showed seasonal and temporal shift, while the variation was related to plant species. This study indicates that AM symbiosis widely exists in urban wetland plants, while AM formation in various plants is affected by different water and sediment properties.
1. Introduction Wetlands are unique habitats at the interface between terrestrial and aquatic ecosystems, which have ecological significance in natural waste purification and nutrient cycling, preventing floods and erosion, recharging groundwater aquifers (Mitsch and Gosselink, 1993; Turner and Daily, 2008). Urban wetland can provided valuable ecological services such as improving water quality, adjusting local microclimate and providing recreation for nearby residents (Hettiarachchi et al., 2014). However, urban wetland is suffering degradation and destruction during urbanization (Ehrenfeld, 2000; Faulkner, 2004; Wentzell et al., 2016). In China, rapid urbanization has been attracting the attention in recent years, and the urbanization level has reached to 56.1% with the urban population of 771.16 million in 2015 (NBSC, 2016). Area, function and structure of urban wetlands are negatively affected by the rapid urbanization (Peng et al., 2016; Li et al., 2017a; Du and Huang, 2017). For example, forest land, grassland and agricultural land
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are excessively transformed into construction land due to housing demands (Liu et al., 2011; Li et al., 2017b), which cause area reduction, functional decline and acute eutrophication of urban wetlands (Yin and Yang, 2013; Sun et al., 2016). Urban wetland restoration and protection has become an increasingly important issue with the development of urbanization. In order to restore and protect urban wetland functions, it is necessary to alleviate the negative effects of urbanization on urban wetland ecosystem (Doherty and Zedler, 2014). Arbuscular mycorrhizae (AM) are the most common and widespread mycorrhizal associations, which occur in over two-thirds of terrestrial vascular plant species (Smith and Read, 2008). In recent two decades, more and more studies confirm that AM symbioses also widely exist in wetland plants (see review by Xu et al., 2016). Although AM fungal colonization is generally regarded as lower in wetlands than in upland (Jayachandran and Shetty, 2003; Lumini et al., 2011), the presence of AM symbiosis produces a wide range of benefits to their plant partners (Miller and Sharitz, 2000; Wang et al., 2010). This implies that
Corresponding author at: P.O. 107, No. 15, Beisanhuan East Road, Chaoyang District, Beijing, 100029, China. Corresponding author. E-mail addresses: [email protected] (S. Wang), [email protected] (X. Diao).
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https://doi.org/10.1016/j.aquabot.2018.07.002 Received 24 November 2017; Received in revised form 20 June 2018; Accepted 4 July 2018 Available online 05 July 2018 0304-3770/ © 2018 Elsevier B.V. All rights reserved.
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Fig. 1. Study area and sampling sites locations. Red dots indicate sampling sites. R-BY: Beiyun River, R-WY: Wenyu River, R-YD: Yongding River, R-GS: Guishui River, R-LS: Liangshui River, R-FH: Fenghe River; P-HSQ: Hanshiqiao Wetland Park, P-NHZ: Nanhaizi Wetland Park, P-OLF: Olympic Forest Wetland Park; RE-GT: Guanting Reservoir, RE-SH: Shahe Reservoir, RE-MY: Miyun Reservoir (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article).
natural wetlands. However, the results are not consistent. For example, Beck-Nielsen and Madsen (2001) reported that 20% of lake plants (5 of 25 species) and 16.67% of stream plants (4 of 24 species) formed AM symbiosis in Denmark; Wang and Zhao (2006) found that 4.0% of lake plants (1 of 25 species) and 35.3% of stream plants (6 of 17 species) were colonized by AM fungi in Yunnan province, southwest China. In contrast, Radhika and Rodrigues (2007) found that 71.4% of aquatic plants (10 of 14 species) and 83.3% of marshy plants (5 of 6 species) were colonized by AM fungi in Goa, India. Weishampel and Bedford (2006) found that 74.6% of wetland plants (50 of 67 species) formed fully developed AM symbiosis in three calcareous fens located near Ithaca, New York. These inconsistent results indicate further study is needed. Beijing is the capital of China and is one of the most populated and developed cities, with total dimension of 16,410.54 km2, a huge population of 21.7 million and a gross domestic product of 2800 billion RMB in 2017 (BMBS, 2018). It is reported that large quantities of domestic sewage (about 3.3 million tons per day) are produced from residential areas. However, only 83% of wastewater is treated in the wastewater treatment plants, and the rest is directly discharged into the waterbody (Dai et al., 2015). This may affect AM formation in urban wetland plants. Our objectives are to (1) investigate AM status vegetation in different types of wetlands in Beijing area; (2) analyze the relationships between the degree of colonization of three plant species (reed, reed mannagrass and cattail) with many physicochemical properties of water and sediments; and (3) study the seasonal (Autumn and Spring) and temporal (2013 and 2014 year) variability on AM colonization. We hypothesized that AM formation would be partly affected by water and sediment properties, and seasonal and annual shift. We believed that this study may promote application of AM fungi in constructed wetlands and urban wetlands.
Table 1 Information on sampling sites in urban wetlands in Beijing area. Wetland types
Wetland names
Number of sampling site
Plant species richness (Mean ± SD)/ plant species m−2
River
Beiyun (R-BY) Wenyu (R-WY) Yongding (R-YD) Guishui (R-GS) Liangshui (R-LS) Fenghe (R-FH) Hanshiqiao (PHSQ) Nanhaizi (PNHZ) Oplympic Forest (P-OLF) Guanting (REGT) Miyun (RE-MY) Shahe (RE-SH)
5 3 10 2 2 3 2
5.60 9.00 4.20 5.50 9.50 2.00 6.00
12
10.25 ± 4.27
12
4.08 ± 1.79
4
4.50 ± 1.29
4 6
1.50 ± 0.58 10.0 ± 3.90
Wetland park
Reservoir
± ± ± ± ± ± ±
2.97 1.00 2.78 4.95 4.95 1.00 2.83
arbuscular mycorrhizae may be important for wetland ecosystems. Up to know, however, little is known regarding AM symbiosis in urban wetland plants and the factors affecting AM formation. Urban wetlands differ from natural wetlands, which generally receive massive industrial and domestic wastewater disposal and thus AM formation may be negatively affected in urban wetlands. Wang et al. (2014) found that the colonization intensity of AM fungi was inhibited by municipal sewage discharge in mangrove plant, especially vesicles and arbuscules were more sensitive to wastewater discharge than the hyphal structure. Twanabasu et al. (2013) found that 0.4 μg L−1 triclosan significantly reduced AM and hyphal colonization levels in North American wetlands. These results indicate that factors affecting AM formation in urban wetlands may be different from these in natural wetlands. In addition, if we plan to use AM fungi to improve plant growth in urban wetlands, it is necessary to clarify what factors affect AM formation. Some studies have surveyed species of AM fungi and their host plants, and have investigated the factors affecting AM formation in
2. Materials and methods 2.1. Site description The study area is located in the suburb of Beijing city (Fig. 1). 34
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Sampling sites distributed in rivers, wetland parks and reservoirs. Sampling sites were determined according to the geographical feature, hydrological regime, river channel hardening (some rivers were hardening by bricks or cement, and thus few plants grew, such as Kunyu River, Nanchang River) and government permission (some wetlands were controlled by government and not allowed to enter, such as Cuihu Wetland Park, Daoxianghu Wetland Park, Shisanling Reservoir, etc.). In our study, the rivers include Beiyun (R-BY), Wenyu (R-WY), Yongding (R-YD), Guishui (R-GS), Liangshui (R-LS) and Fenghe (R-FH); the wetland parks include Hanshiqiao (P-HSQ), Nanhaizi (P-NHZ) and Olympic Forest (P-OLF); the reservoirs include Guanting (RE-GT), Shahe (RE-SH) and Miyun (RE-MY) (Table 1). Sample number in each wetland depended on river length, area of park and reservoir as well as vegetation distribution.
Table 2 Occurrence of arbuscular mycorrhiza (AM) symbiosis in urban wetland plants in Beijing area. Wetland types Plant species
Phragmites australi Typha orientalis Glyceria maxima Salix babylonica Ulmus pumila Polygonum hydropiper Scirpus validus Actinostemma tenerum Sagittaria trifolia Rorippa globosa Artemisia argyi Bidens pilosa Cyperus rotundus Echinochloa caudata Scirpus planiculmis Typha minima Rhoeo spathacea Fimbristylis dichotoma Alisma plantagoaquatica Humulus scandens Hemarthria altissima Ceratophyllum demersum Inula japonica Triarrherca sacchariflora Echinochloa crusgalli Arthraxon hispidus Potamogeton franchetii Myriophyllum verticillatum Arundo donax Oenanthe javanica Nasturtium officinale Ranunculus japonicus Acorus calamus Juncus effuses Veronica undulata Equisetum arvense Equisetum ramosissimum Lysimachia barystachys Lythrum salicaria Sparganium stoloniferum Vallisneria natans Chenopodium album Stellaria radians Malachium aquaticum Costus speciosus Nymphaea tetragona Carex tristachya Polypogon fugax Senecio scandens Adenophora trachelioides Scirpus triangulatus Potamogeton crispus Eriachne pallescens Utricularia bifida Spartina alterniflora Achnatherum splendens
Reservoirs
Rivers
1
2
3
4
5
+ + + +
+ +
+
+ + +
+ +
+ + +
+ —
Parks 6
7
+ + + + +
+ +
+
+ + +
+ + + +
+ + + + — +
+ +
+ + + + + +
+
+
+
+
2.2. Sample collection — + +
+ +
In each quadrat (1 m × 1 m), 2 superficial water samples (0–20 cm) were firstly taken by 1 L polypropylene bottles, then 1–3 individuals of each plant species was collected, and finally 2 sediment samples (0–20 cm) were randomly taken by a stainless steel sampler. No quadrat replicates was designed. Both water and sediment samples had two replicates. Some plants species had 2–3 individuals in each quadrat while other plants species only had one individual. A total of 130 superficial water samples, 130 sediment samples and 315 plant samples were obtained. All samples were taken in September 2013. In the study on the changes of MCRs with seasonal and annual shift, we only selected two plants species (reed Phragmites australi and cattail Typha orientalis) in two wetland parks (P-NHZ and P-OLF). This is because reed and cattail are the most common wetland plants and are frequently used in constructed wetland and ecological floating bed; moreover, they are potential feedstock for sustainable bioenergy production. Although other plants such as reed mannagrass (Glyceria maxima) plant also exist in some sites, they are seldom used by human. The reasons for selecting P-NHZ and P-OLF are that (1) their areas are large (800 and 680 hm2), and (2) they locate the North and South region of Beijing city respectively and are very representative. Sampling method was similar to the survey study. Among 12 sampling sites, 5 sampling sites were designed in each wetland park. Sampling was conducted in May 2013 (average air temperature at night and day: 1628℃), September 2013 (16-26℃), May 2014 (16-28℃) and September 2014 (16-25℃), respectively.
+ + + +
+ +
+
+ +
+
+
+ + +
+ +
+ + —
+
+
+ + +
+
+
— +
+
+
— +
+ + + + + + + + — + + + + +
+
+
+ +—
+ —
12
+
+
— +
11
+ +
+
10
+ — +
+ + + + + + + + +
9
+
+
+ +
8
—
+ +
+ + + + +
+ + +
+ + + + +
+ — + + +
+
+ + —
—
+
+
2.3. Sample analysis
+ + + +
+ +
2.3.1. Water sample Samples from each site were analyzed in the field for temperature, pH, dissolved oxygen (DO), water conductivity (EC) and oxidation-reduction potential (ORP) using a portable water quality analyzer (YSI Pro Plus, America). In lab, water samples were filtered through a 0.45 μm membrane filter for the analysis of nitrogen and phosphorus. NH4+-N was determined by the indophenol-blue method described by Aminot et al. (1997), NO3−-N, NO2−-N, total dissolved phosphorus (TDP) and PO43- -P were determined by a flow injection analyzer (SEALAA3,German).
+ — + + + — + + +
— + +
+
+ + + + +
+ +
+
+
+
+
+ +
2.3.2. Sediment sample The ammonia (NH4+-N) was measured by the Nesslerization method; Nitrite (NO2−-N) was measured by N-1 naphthyl ethylenediamine spectrophotometric method at 540 nm; Nitrate (NO3−-N) was determined using an ultraviolet spectrophotometric screening method at 220 and 275 nm (UV-2450, Shimadzu, Kyoto, Japan) (AMWW, 2002). Total organic carbon (TOC) was analyzed with an automatic TOC analyzer (Vario TOC, Elementar, Germany) according to the user manual provided by the manufacturer.
Reservoir: 1- Shahe Reservoir, 2- Miyun Reservoir, 3. Guanting Reservoir; River: 4- Beiyun River, 5- Wenyu River, 6- Yongding River, 7- Guishui River, 8Fenghe River, 9- Liangshui River; Park 10- Olympic Forest Wetland Park, 11Nanhaizi Wetland Park, 12- Hanshiqiao Wetland Park. + indicates the presence of AM symbiosis; — indicates the absence of AM symbiosis; Blanks indicate that no plant is sampled in this urban wetland.
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Table 3 Information on aquatic plants with or without AM symbiosis in urban wetlands in Beijing area. Family
Species
Plant type
MCR (%)
nM/nNM
nTotal
Poaceae
Echinochloa caudata Echinochloa crusgalli Phragmites australi Glyceria maxima Hemarthria altissima Triarrherca sacchariflora Arthraxon hispidus Arundo donax Polypogon fugax Eriachne pallescens Spartina alterniflora Achnatherum splendens Typha orientalis Typha minima Sparganium stoloniferum Salix babylonica Ulmus pumila Polygonum hydropiper Actinostemma tenerum Sagittaria trifolia Alisma plantago-aquatica Rorippa globosa Nasturtium officinale Artemisia argyi Bidens pilosa Inula japonica Senecio scandens Scirpus validus Scirpus planiculmis Scirpus triangulatus Cyperus rotundus Fimbristylis dichotoma Carex tristachya Humulus scandens Rhoeo spathacea Ceratophyllum demersum Potamogeton franchetii Potamogeton crispus Myriophyllum verticillatum Oenanthe javanica Ranunculus japonicus Acorus calamus Juncus effuses Veronica undulata Equisetum arvense Equisetum ramosissimum Lysimachia barystachys Lythrum salicaria Vallisneria natans Chenopodium album Stellaria radians Malachium aquaticum Costus speciosus Nymphaea tetragona Adenophora trachelioides Utricularia bifida
Weed Weed Herb Grass Grass Herb Herb Herb Weed Grass Weed Herb Grass Grass Herb Tree Tree Herb Herb Weed Herb Herb Herb Herb Herb Herb Herb Grass Herb Herb Herb Herb Grass Herb Herb Herb Herb Grass Grass Herb Herb Grass Herb Weed Herb Herb Herb Grass Herb Herb Herb Herb Herb Grass Herb Herb
10.7 ± 4.80 22.0 ± 6.07 23.1 ± 12.3 14.2 ± 10.5 2.66 ± 1.15 9.60 ± 6.07 7.00 ± 7.75 19.1 ± 12.4 52.0 ± 12.0 16.0 ± 9.17 41.3 ± 16.3 4.8 ± 2.68 13.4 ± 7.37 17.7 ± 3.73 0 14.4 ± 6.23 22.5 ± 9.98 16.4 ± 14.7 0 11.3 ± 9.27 14.7 ± 3.06 4.00 ± 2.00 29.3 ± 3.03 3.60 ± 2.61 0 2.67 ± 3.06 41.0 ± 20.9 0 4.00 ± 3.16 3.33 ± 3.06 15.5 ± 4.12 3.60 ± 2.61 0 8.40 ± 3.85 5.11 ± 4.26 19.5 ± 5.51 11.2 ± 3.03 19.6 ± 21.3 0 0 6.67 ± 3.06 4.67 ± 3.01 41.5 ± 7.00 34.0 ± 6.00 25.5 ± 15.9 11.7 ± 7.09 10.5 ± 3.42 5.50 ± 3.42 24.3 ± 15.5 12.9 ± 6.82 21.2 ± 12.7 40.0 ± 25.5 40.7 ± 1.15 8.00 ± 8.49 53.0 ± 15.6 6.00 ± 2.00
9/0 6/0 23/0 10/2 3/0 5/0 3/1 6/1 4/0 3/0 4/0 5/0 17/0 7/0 0/4 5/0 4/0 8/1 0/1 6/0 3/0 3/0 4/0 4/1 0/1 2/1 4/0 0/1 4/1 2/1 4/0 4/1 0/2 5/0 7/2 4/0 5/0 5/0 0/2 0/2 4/0 6/0 4/0 3/0 4/0 5/1 4/0 4/0 6/0 7/0 5/0 2/0 3/0 2/0 2/0 3/0
9 6 23 12 3 5 4 7 4 3 4 5 17 7 4 5 4 9 1 6 3 3 4 5 1 3 4 1 5 3 4 5 2 5 9 4 5 5 2 2 4 6 4 3 4 6 4 4 6 7 5 2 3 2 2 3
Typhaceae
Salicaceae Ulmaceae Polygonaceae Cucurbitaceae Alismataceae Brassicaceae Asteraceae
Cyperaceae
Cannabaceae Commelinaceae Ceratophyllaceae Potamogetonaceae Haloragaceae Apiaceae Ranunculaceae Acoraceae Juncaceae Plantaginaceae Equisetaceae Primulaceae Lythraceae Hydrocharitaceae Amaranthaceae Caryophyllaceae Costaceae Nymphaeaceae Campanulaceae Lentibulariaceae
MCRs are average ± deviation, and nTotal =nM+nNM; nM indicates the number of plant species colonized by AM fungi, and nNM indicates the number of plant species not colonized by AM fungi.
2.3.3. Plant sample 2.3.3.1. Plant species identification. Plant species was identified according to the handbooks: Botanical Illustrations of Aquatic Plant (Zhao and Liu, 2009) and Wetland Plants: Colorful Illustrations of 365 Kinds of Hygrophyte, Aquatic and Marsh Plants (Li and Xu, 2010).
magnification (Giovannetti and Sbrana, 1998). To verify colonization, selected colonized root pieces were mounted on slides and viewed with a compound microscope at 400× magnification.
2.3.3.2. Mycorrhizal colonization rate (MCR). Roots (3 g fresh weight) were cut into 1 cm segments and rinsed and cleared with 10% KOH for 90 min at 90℃. The KOH was rinsed off and the segments acidified with 5% lactic acid for 20 min. Thereafter the roots were then stained with 0.05% (w/v) Trypan blue for 30 min at 90℃. Root segments were determined according to the gridline-intersect method at 25×
All measurements of MCRs were carried out by the same person in the same condition. Relationships between MCR and water characteristics as well as MCR and sediment characteristics were tested using Pearson’s correlation. One-way ANOVA (Duncan’s HSD test) was conducted to test if seasonal or annual shift had effects on MCRs at the significance level α < 0.05. Statistical analyses were conducted using
2.4. Statistical analysis
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Table 4 Mycorrhizal colonization rates in reed, cattail and reed mannagrass in urban wetlands. Sample sites
RE-SH RE-MY RE-GT R-BY R-WY R-YD R-GS R-FH R-LS P-OLF P-NHZ P-HSQ
Reed
Cattail
Reed mannagrass
Range
Mean ± SD
Range
Mean ± SD
Range
Mean ± SD
12–22% 12–14% 12–20% 10–44%
17.3 ± 5.03% 13 ± 1.41% 16.0 ± 4.00% 22.5 ± 14.9%
6% 2%
6% 2%
10%
10%
28–46% 24–38%
37.0 ± 12.7% 31.0 ± 9.90%
10–14% 18–24% 18–24% 26–32%
12.0 ± 2.83% 17.3 ± 7.02% 20.7 ± 3.05% 29 ± 4.24%
12% 12–26% 10% 10–16%
12% 19.0 ± 9.90% 10% 14.0 ± 2.00%
4–10% 8–40% 14–46% 18%
7.0 ± 4.20% 23.8 ± 11.9% 31.0 ± 10.2% 18%
8–24% 10–26%
19.0 ± 4.76% 17.3 ± 9.45%
8–38%
19.3 ± 16.3%
RE-SH: Shahe Reservoir; RE-MY: Miyun Reservoir; RE-GT: Guanting Reservoir; R-BY: Beiyun River; R-WY: Wenyu River; R-YD: Yongding River; R-GS: Guishui River; R-FH: Fenghe River; R-LS: Liangshui River; P-OLF: Olympic Forest Wetland Park; P-NHZ: Nanhaizi Wetland Park; P-HSQ: Hanshiqiao Wetland Park. Blanks indicate that no these plants were sampled in this urban wetland.
NO2−-N (r = 0.888, p < 0.05) (Fig. 7). Although MCRs in cattail and reed mannagrass plants did not show significant correlation with NO3−-N (p > 0.05), the evident change trends were observed.
SPSS 17.0 software package. 3. Results 3.1. AM fungal colonization in urban wetland plants
3.4. Effects of MCRs dynamic with seasonal and annual shift in urban wetland
In total, 315 specimens of 56 hydrophyte species were investigated. Typical AM structures (arbuscule, hyphae and vesicle) were observed in 49 hydrophyte species, and the proportion was up to 87.5% (Tables 2 and 3). MCRs ranged from 2% to 72%, while most of them were relative low (< 25%). Tephroseris palustris had the highest MCR as 72%. Even the same plant species, MCRs varied with different sampling sites. For example, MCR was 40% in Phragmites austral collected from R-YD, while it was only 20% in Phragmites austral collected from RE-GT. This can also be seen from Table 4, which showed MCRs in reed, cattail and reed mannagrass in various urban wetlands.
In both NHZ and OLF wetland parks, MCRs in reed plant in Spring (May) were higher than in Autumn (September) but the difference was not significant in P-NHZ (Fig. 8a). However, MCRs in cattail showed contrary trends between two seasons, and the difference was also not significant in P-OLF (Fig. 8b). This indicated that AM formation was affected by seasonal shift, while positive or negative effects depended on plant species. Fig. 9 showed MCRs dynamic with annual shift in reed and cattail plants. It can be seen that MCRs in reed plant showed upward trends from May 2013 to May 2014, but the difference was not significant (Fig. 9a). In cattail, however, MCRs in May 2013 were significantly lower than in May 2014 (Fig. 9b). This indicated that AM formation was affected by annual shift, while positive or negative effects depended on plant species.
3.2. Correlation of MCRs and water properties in urban wetlands In reed plant, Pearson’s correlation analysis indicated that MCRs did not exhibit significant correlation to water properties except for NH4+N and TDP (Fig. 2). MCRs were significantly and negatively correlated to water NH4+-N and TDP concentrations (rNH4-N = 0.636, pNH4N < 0.01; rTDP = 0.562, pTDP < 0.05). In cattail plant, Pearson’s correlation analysis indicated that MCRs also did not exhibit significant correlation to water properties except for ORP (Fig. 3). MCRs were significantly and negatively correlated to water ORP (r = 0.724, p < 0.05). In reed mannagrass plant, no significant correlation between MCRs and water properties was found (Fig. 4). Generally, MCRs presented change trends with most water properties, but the correlation was not significant (p > 0.05). For example, MCRs in three wetland plants showed upwards trend with increasing EC, and showed downward trends with increasing water PO43−-P concentrations (Figs. 2–4).
4. Discussion 4.1. Plants with AM symbiosis in urban wetlands In this study, the proportion of wetland plant species (87.5%) which were colonized by AM fungi was higher than that in most previous studies (Radhika and Rodrigues, 2007; Weishampel and Bedford, 2006; Seerangan et al., 2010; Zhao et al., 2016). The possible reasons include that (1) dispersal of AM fungi is changed by hydraulic engineering, such as wetland eco-restoring project and municipal engineering, and (2) plants are collected from big area, and thus plants have high probability to be colonized by AM fungi. This may be confirmed by present study. Plants species without AM symbiosis were collected from a few sampling sites (< 3), such as Scirpus validus, Actinostemma tenerum and Bidens pilosa from one sampling site, and Myriophyllum verticillatum, Oenanthe javanica and Carex tristachya from two sampling sites. It cannot be denied that there are contrary results. For example, Scirpus validus (Liberta et al., 1983; Bauer et al., 2003) and Bidens pilosa (Zhao et al., 2016) were reported to establish AM symbiosis. The detailed reasons need further study. MCRs were relative low in most wetland plants (< 25%), indicating that most plants may be difficult to be colonized by AM fungi in wetland habitat. This result is consistent with some previous studies (Wang
3.3. Correlation of MCR and sediment properties in urban wetlands In reed plant, Pearson’s correlation analysis indicated that MCR was significantly and positively correlated to sediment NO3−-N, NO2−-N and TOC (rNO3-N = 0.631, pNO3-N < 0.05; rNO2-N = 0.661, pNO2N < 0.05; rTOC = 0.694, pTOC < 0.01) (Fig. 5). In cattail plant, MCR was significantly and positively correlated to sediment TOC (r = 0.855, p < 0.05) (Fig. 6). In reed mannagrass plant, MCRs were significantly and positively correlated to only sediment 37
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Fig. 2. Correlation between MCR in reed and water properties. “r” indicates Pearson’s correlation coefficient, “p” indicates test of significance by two-tailed, “n” indicates sample number. DO: dissolved oxygen; EC: water conductivity; ORP: oxidation-reduction potential; TDP, total dissolved phosphorus.
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Fig. 3. Correlation between MCR in cattail and water properties. “r” indicates Pearson’s correlation coefficient, “p” indicates test of significance by two-tailed, “n” indicates sample number. DO: dissolved oxygen; EC: water conductivity; ORP: oxidation-reduction potential; TDP, total dissolved phosphorus.
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Fig. 4. Correlation between MCR in reed mannagrass and water properties. “r” indicates Pearson’s correlation coefficient, “p” indicates test of significance by twotailed, “n” indicates sample number. DO: dissolved oxygen; EC: water conductivity; ORP: oxidation-reduction potential; TDP, total dissolved phosphorus.
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Fig. 5. Correlation between MCR in reed and sediment properties. “r” indicates Pearson’s correlation coefficient, “p” indicates test of significance by two-tailed, “n” indicates sample number. TDP, total dissolved phosphorus; TOC: total organic carbon.
characteristics due to difference in geographical position. AM fungi species also varies with different wetlands. For example, Glomus mosseae and Glomus claroideum were the dominant AM fungi in the studies of Wang and Zhao (2006) and Radhika and Rodrigues (2007) respectively, while in the study of Wilde et al. (2009), the dominant AM fungi was Glomus intraradices.
and Zhao, 2006; Zhao et al., 2016). However, high MCRs in some wetland plants were found (> 40%), such as Costus speciosus, Polypogon fugax, Adenophora trachelioide and Senecio scandens. Similar phenomena are also reported in previous studies. Seerangan et al. (2010) found that MCRs ranged from 49.19% (Oryza sativa) to 86.05% (Lindernia parviflora) in 8 hydrophytes and 50 wetland plants species from four sites in south India. MCRs in same plant also showed great variation. For example, MCR was 72% in Senecio scandens collected from P-NHZ while it was only 30% in same plant species collected from RE-SH, R-WY and R-YD. Similar phenomena are reported in previous studies. Beck-Nielsen and Madsen (2001) found no mycorrhizal colonization in submerged specimens while very low colonization levels were found in the same emerged species. It has been reported that, depending on the habitats, cattail was colonized or not by AM fungi (Stenlund and Charvat, 1994; Thormann et al., 1999). This difference may be related to wetland habitat and AM fungi species. Different wetland habitats often have various water levels, water temperatures, and water and sediment
4.2. Effects of water and sediment properties on AM formation in urban wetlands It has been confirmed that AM formation is affected by many factors in terrestrial environment, such as soil nutrients, pH, compaction, moisture stress, pollutants (Soka and Ritchie, 2014; Lenoir et al., 2016). In wetland habits, AM formation may be also affected by a variety of environmental factors, such as hydrological conditions (Miller and Bever, 1999; Wang et al., 2011), nutrients (Wang et al., 2010), pH and electric-conductivity levels (D’Souza and Rodrigues, 2013). Although many studies have concerned this subject, up to now no agreement has 41
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Fig. 6. Correlation between MCR in cattail and sediment properties. “r” indicates Pearson’s correlation coefficient, “p” indicates test of significance by two-tailed, “n” indicates sample number. TDP, total dissolved phosphorus; TOC: total organic carbon.
Wang et al., 2010). In this study, however, AM fungal colonization in three plants was not affected by PO43−-P and TDP concentrations in water and sediment except for the fact that water TDP and AM colonization in reed showed negative correlation. This result almost supports the finding of Miller et al. (1999) in a comprehensive study, in which soil P availability and AM fungal colonization in the genus Carex did not show significant correlation. Van Hoewyk et al. (2001) also found that the extent of AM fungal colonization of Dasiphora floribunda did not vary among calcareous wetlands of different soil P concentrations. This suggests that P availability may not be the key factor for AM formation in wetland. Certainly, the difference may be related to plant species, AM fungal species, P level and other coexisted factors (such as pH, ORP). For example, Stevens et al. (2002) found that AM colonization levels in Lythrum salicaria were significantly reduced at P concentrations of 5 mg L-1 and higher, while Xie et al. (2014) found that the optimal P level for AM fungal colonization in mangrove species Kandelia obovata was 30 mg kg-1. AM fungal species also differ in the extent to which phosphate decreases mycorrhiza formation (Thomson et al., 1986).
been reached in most cases. In the present study, MCRs in reed were negatively correlated to water NH4+-N, TDP and MCRs in cattle were negatively correlated to ORP. MCR decreases with increasing water NH4+-N, possibly because high concentrations of NH4+-N inhibits the germination of AM fungal spores and is toxic to AM fungal colonization (Cornejo et al., 2007). ORP plays a role in AM formation in wetland plant. Beck-Nielsen and Madsen (2001) found that the redox potential in sediments with noninfected specimen ranged from 54 to 280 mV and in sediments with infected species from 250 to 530 mV. ORP in the rhizosphere of wetland plants generally ranges from 130 mV to 350 mV (Li et al., 2014), so this means AM formation in wetland plant is inhibited in most cases. This may explain why MCRs were low in most wetland plants in this study. Presently, however, it is difficult to provide reasonable explanation on that MCRs were negatively correlated with ORP in cattail. We will continue to concern this subject in further study. It has been confirmed that AM formation is sensitive to available P, since many previous studies confirm that both low and high P can inhibit AM fungal colonization (Koide and Li, 1990; Chen et al., 2008; 42
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Fig. 7. Correlation between MCR in reed mannagrass and sediment properties. “r” indicates Pearson’s correlation coefficient, “p” indicates test of significance by twotailed, “n” indicates sample number. TDP, total dissolved phosphorus; TOC: total organic carbon.
Fig. 8. Effect of seasonal shift on MCRs dynamic in reed and cattail plant in urban wetlands. Different lowercase letters indicate a significant difference between two seasons at p = 0.05 in each wetland park. P-NHZ: Nanhaizi Wetland Park; P-OLF: Olympic Forest Wetland Park.
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Fig. 9. Effect of temporal shift on MCRs dynamic in reed and cattail plant in urban wetlands. Different lowercase letters indicate a significant difference between two years at p = 0.05 in each wetland park. P-NHZ: Nanhaizi Wetland Park; P-OLF: Olympic Forest Wetland Park.
MCRs in reed showed positive correlation to sediment NO3−-N, NO2−-N or TOC, showed positive correlation to sediment TOC in cattail, and showed positive correlation to sediment NO2−-N in reed mannagrass. This is possibly because the concentrations of sediment NO3−-N, NO2−-N and TOC are low relative to plant requirement in most sampling sites, and they are the inhibitive factors for plant growth. In higher concentrations of NO3−-N, NO2−-N and TOC, plant growth is better and in turn facilitates AM fungal propagation and colonization. Fraser and Feinstein (2005) found that growth of the wetland plants was limited more by nitrogen than by phosphorus. Certainly, if sediment nutrients are high enough, AM fungal propagation and colonization might be inhibited. There is a solid evidence showing that an appropriate application of organic matter could promote AM fungal colonization in host species (Hodge and Fitter, 2010), while excess organic matter can be harmful to this symbiotic relationship (Sáinz et al., 1998). Due to few studies on the relationship between AM formation and N in wetland (Miller, 2000), it is difficult to further discuss effect of N on AM formation. In the present study, MCRs in three plants didn’t show significant correlation with water DO. This is different from previous studies (Miller and Bever, 1999; Beck-Nielsen and Madsen, 2001; Wang et al., 2014). This is possibly because (1) three plants are rooted emergent plants and thus MCRs are slightly affected by water DO; (2) AM fungi can obtain oxygen directly from root through aerenchyma and slightly depend on water DO; and (3) water DO little varies in all sampling sites (0–40 mg L−1) and thus it is difficult to show significant correlation between them.
revealed that season and host coaffected AM spore density and species richness with the former having greater influence than the latter. Seasonal variation of water regimes in wetlands likely provides the soil with opportunities to aerate, thus providing the AM fungi with periods of increased oxygenation for survival. For example, Ipsilantis and Sylvia (2007) found that AM root colonization was least during the dry winter and spring seasons and greatest in the flooded summer and fall seasons in several plant communities (i.e., Panicum, Cladium, and Typha). In both two wetland parks, MCRs in reed were higher in 2013 than in 2014, while contrary result was found in cattail. This is possibly related to AM fungal species and plant species that are different in cold tolerance. The lowest temperature is -14℃ in January 2013 in Beijing, which can threaten wetland plant survival. Cattail generally has greater cold tolerance than reed, and this may make cattail has good growing in next year. Different AM fungal species also have different cold tolerance (Varga et al., 2015), so they have different colonization ability after low temperature stress. Berch and Kendrick (1982) found that plant physiology and turnover of plant roots are among the drivers of AM fungal seasonality. This may be another reason that resulted in MCR variation with annual shift. 5. Conclusions Urban wetland functions may be improved by AM fungi, such as providing recreational and landscape space, natural scenic beauty, and buffering against noise and pollution. For this reason, it is necessary to deeper investigate the role of AM symbiosis in urban wetland. In our study, we found that 87.0% of urban wetland plants (49 of 56 species) were colonized by AM fungi, and MCRs ranged from 2% to 72%. In the investigation on three plants (Phragmites australi, Typha orientalis and Glyceria maxima), AM formation was affected by water and sediment properties, and the latter had greater effects than the former. Moreover, MCRs showed seasonal and temporal variation. As a whole, although most MCRs were lower than 25% in urban wetland plants, it is promising to use AM fungi to improve urban wetland functions. AM formation in urban wetland plants can be increased by regulating some properties of water and sediment.
4.3. MCRs dynamics with seasonal and temporal shift in urban wetlands Few studies have concerned the MCRs dynamic with seasonal and temporal shift in wetlands (Turner and Friese, 1998; Miller, 2000; Oliveira and Dodd, 2001; Bohrer et al., 2004). In this study, MCR in reed was higher in May than in September, showing significant seasonal variation exists. This is consistent to the result of Bohrer et al. (2004) in wetlands, in which AM fungal colonization was the highest in Spring and was the lowest in Summer. This is possibly because AM fungal colonization coordinates with plant growth stages, and reed root activity is vigorous in May (Engloner, 2009). Bohrer et al. (2004) concluded that abiotic factors had minimal influence on AM fungal colonization variation, so AM seasonal dynamics was in response to plant phenology. However, MCR in cattail was lower in May than in September, which is contrary to MCR in reed. This is possibly because cattail growth is later than reed (about mid-April) and keeps long time (till to end of October), so cattail growth is vigorous in September. Certainly, we should not neglect the effects of seasonal shift and water table level on AM fungal activity. D’Souza and Rodrigues (2013)
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Arbuscular mycorrhizal (AM) status in urban wetland plants and its impact factors ⁎
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Shuguang Wanga, , Dongwei Daia, Shuang Songa, Xiaojun Diaob, , Leimeng Maa a b
Department of Environmental Science and Engineering, Beijing University of Chemical Technology, Beijing, China Appraisal Center for Environment and Engineering, Ministry of Environmental Protection, Beijing, China
A R T I C LE I N FO
A B S T R A C T
Keywords: Arbuscular mycorrhizal symbiosis Urban wetland Mycorrhizal colonization rate Water Property Sediment Property
Urban wetlands play an important role in improving urban environment and microclimate, while they are suffering degradation and destruction during urbanization process. Arbuscular mycorrhizae may enhance plant tolerance to environmental stresses and increase vegetation restoration in wetlands. However, presently little is known how about arbuscular mycorrhizal (AM) symbiosis in urban wetland plants and the factors affecting AM formation. Here, a survey for AM status in urban wetland plants was done in Beijing area, and the factors affecting AM formation were also discussed, such as water and sediment characteristics. Results showed that 87.5% of plants (49 of 56 species) were colonized by AM fungi. Mycorrhizal colonization rates (MCRs) ranged from 2% to 72%, while most of them were low level (< 25%). The highest mycorrhizal colonization rate (MCR) was observed in Tephroseris palustris. Relationships between MCRs and water properties as well as sediment properties were analyzed by Pearson’s correlation analysis. MCRs in Phragmites australi were negatively correlated with water ammonium nitrogen and a total dissolved phosphorus, while were positively correlated with nitrate nitrogen, nitrite nitrogen and total organic carbon (TOC) in sediment. MCRs in Typha orientalis were negatively correlated with water oxidation-reduction potential while were positively correlated with sediment TOC. MCRs in Glyceria maxima were positively correlated with sediment nitrate nitrogen. MCRs showed seasonal and temporal shift, while the variation was related to plant species. This study indicates that AM symbiosis widely exists in urban wetland plants, while AM formation in various plants is affected by different water and sediment properties.
1. Introduction Wetlands are unique habitats at the interface between terrestrial and aquatic ecosystems, which have ecological significance in natural waste purification and nutrient cycling, preventing floods and erosion, recharging groundwater aquifers (Mitsch and Gosselink, 1993; Turner and Daily, 2008). Urban wetland can provided valuable ecological services such as improving water quality, adjusting local microclimate and providing recreation for nearby residents (Hettiarachchi et al., 2014). However, urban wetland is suffering degradation and destruction during urbanization (Ehrenfeld, 2000; Faulkner, 2004; Wentzell et al., 2016). In China, rapid urbanization has been attracting the attention in recent years, and the urbanization level has reached to 56.1% with the urban population of 771.16 million in 2015 (NBSC, 2016). Area, function and structure of urban wetlands are negatively affected by the rapid urbanization (Peng et al., 2016; Li et al., 2017a; Du and Huang, 2017). For example, forest land, grassland and agricultural land
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are excessively transformed into construction land due to housing demands (Liu et al., 2011; Li et al., 2017b), which cause area reduction, functional decline and acute eutrophication of urban wetlands (Yin and Yang, 2013; Sun et al., 2016). Urban wetland restoration and protection has become an increasingly important issue with the development of urbanization. In order to restore and protect urban wetland functions, it is necessary to alleviate the negative effects of urbanization on urban wetland ecosystem (Doherty and Zedler, 2014). Arbuscular mycorrhizae (AM) are the most common and widespread mycorrhizal associations, which occur in over two-thirds of terrestrial vascular plant species (Smith and Read, 2008). In recent two decades, more and more studies confirm that AM symbioses also widely exist in wetland plants (see review by Xu et al., 2016). Although AM fungal colonization is generally regarded as lower in wetlands than in upland (Jayachandran and Shetty, 2003; Lumini et al., 2011), the presence of AM symbiosis produces a wide range of benefits to their plant partners (Miller and Sharitz, 2000; Wang et al., 2010). This implies that
Corresponding author at: P.O. 107, No. 15, Beisanhuan East Road, Chaoyang District, Beijing, 100029, China. Corresponding author. E-mail addresses: [email protected] (S. Wang), [email protected] (X. Diao).
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https://doi.org/10.1016/j.aquabot.2018.07.002 Received 24 November 2017; Received in revised form 20 June 2018; Accepted 4 July 2018 Available online 05 July 2018 0304-3770/ © 2018 Elsevier B.V. All rights reserved.
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Fig. 1. Study area and sampling sites locations. Red dots indicate sampling sites. R-BY: Beiyun River, R-WY: Wenyu River, R-YD: Yongding River, R-GS: Guishui River, R-LS: Liangshui River, R-FH: Fenghe River; P-HSQ: Hanshiqiao Wetland Park, P-NHZ: Nanhaizi Wetland Park, P-OLF: Olympic Forest Wetland Park; RE-GT: Guanting Reservoir, RE-SH: Shahe Reservoir, RE-MY: Miyun Reservoir (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article).
natural wetlands. However, the results are not consistent. For example, Beck-Nielsen and Madsen (2001) reported that 20% of lake plants (5 of 25 species) and 16.67% of stream plants (4 of 24 species) formed AM symbiosis in Denmark; Wang and Zhao (2006) found that 4.0% of lake plants (1 of 25 species) and 35.3% of stream plants (6 of 17 species) were colonized by AM fungi in Yunnan province, southwest China. In contrast, Radhika and Rodrigues (2007) found that 71.4% of aquatic plants (10 of 14 species) and 83.3% of marshy plants (5 of 6 species) were colonized by AM fungi in Goa, India. Weishampel and Bedford (2006) found that 74.6% of wetland plants (50 of 67 species) formed fully developed AM symbiosis in three calcareous fens located near Ithaca, New York. These inconsistent results indicate further study is needed. Beijing is the capital of China and is one of the most populated and developed cities, with total dimension of 16,410.54 km2, a huge population of 21.7 million and a gross domestic product of 2800 billion RMB in 2017 (BMBS, 2018). It is reported that large quantities of domestic sewage (about 3.3 million tons per day) are produced from residential areas. However, only 83% of wastewater is treated in the wastewater treatment plants, and the rest is directly discharged into the waterbody (Dai et al., 2015). This may affect AM formation in urban wetland plants. Our objectives are to (1) investigate AM status vegetation in different types of wetlands in Beijing area; (2) analyze the relationships between the degree of colonization of three plant species (reed, reed mannagrass and cattail) with many physicochemical properties of water and sediments; and (3) study the seasonal (Autumn and Spring) and temporal (2013 and 2014 year) variability on AM colonization. We hypothesized that AM formation would be partly affected by water and sediment properties, and seasonal and annual shift. We believed that this study may promote application of AM fungi in constructed wetlands and urban wetlands.
Table 1 Information on sampling sites in urban wetlands in Beijing area. Wetland types
Wetland names
Number of sampling site
Plant species richness (Mean ± SD)/ plant species m−2
River
Beiyun (R-BY) Wenyu (R-WY) Yongding (R-YD) Guishui (R-GS) Liangshui (R-LS) Fenghe (R-FH) Hanshiqiao (PHSQ) Nanhaizi (PNHZ) Oplympic Forest (P-OLF) Guanting (REGT) Miyun (RE-MY) Shahe (RE-SH)
5 3 10 2 2 3 2
5.60 9.00 4.20 5.50 9.50 2.00 6.00
12
10.25 ± 4.27
12
4.08 ± 1.79
4
4.50 ± 1.29
4 6
1.50 ± 0.58 10.0 ± 3.90
Wetland park
Reservoir
± ± ± ± ± ± ±
2.97 1.00 2.78 4.95 4.95 1.00 2.83
arbuscular mycorrhizae may be important for wetland ecosystems. Up to know, however, little is known regarding AM symbiosis in urban wetland plants and the factors affecting AM formation. Urban wetlands differ from natural wetlands, which generally receive massive industrial and domestic wastewater disposal and thus AM formation may be negatively affected in urban wetlands. Wang et al. (2014) found that the colonization intensity of AM fungi was inhibited by municipal sewage discharge in mangrove plant, especially vesicles and arbuscules were more sensitive to wastewater discharge than the hyphal structure. Twanabasu et al. (2013) found that 0.4 μg L−1 triclosan significantly reduced AM and hyphal colonization levels in North American wetlands. These results indicate that factors affecting AM formation in urban wetlands may be different from these in natural wetlands. In addition, if we plan to use AM fungi to improve plant growth in urban wetlands, it is necessary to clarify what factors affect AM formation. Some studies have surveyed species of AM fungi and their host plants, and have investigated the factors affecting AM formation in
2. Materials and methods 2.1. Site description The study area is located in the suburb of Beijing city (Fig. 1). 34
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Sampling sites distributed in rivers, wetland parks and reservoirs. Sampling sites were determined according to the geographical feature, hydrological regime, river channel hardening (some rivers were hardening by bricks or cement, and thus few plants grew, such as Kunyu River, Nanchang River) and government permission (some wetlands were controlled by government and not allowed to enter, such as Cuihu Wetland Park, Daoxianghu Wetland Park, Shisanling Reservoir, etc.). In our study, the rivers include Beiyun (R-BY), Wenyu (R-WY), Yongding (R-YD), Guishui (R-GS), Liangshui (R-LS) and Fenghe (R-FH); the wetland parks include Hanshiqiao (P-HSQ), Nanhaizi (P-NHZ) and Olympic Forest (P-OLF); the reservoirs include Guanting (RE-GT), Shahe (RE-SH) and Miyun (RE-MY) (Table 1). Sample number in each wetland depended on river length, area of park and reservoir as well as vegetation distribution.
Table 2 Occurrence of arbuscular mycorrhiza (AM) symbiosis in urban wetland plants in Beijing area. Wetland types Plant species
Phragmites australi Typha orientalis Glyceria maxima Salix babylonica Ulmus pumila Polygonum hydropiper Scirpus validus Actinostemma tenerum Sagittaria trifolia Rorippa globosa Artemisia argyi Bidens pilosa Cyperus rotundus Echinochloa caudata Scirpus planiculmis Typha minima Rhoeo spathacea Fimbristylis dichotoma Alisma plantagoaquatica Humulus scandens Hemarthria altissima Ceratophyllum demersum Inula japonica Triarrherca sacchariflora Echinochloa crusgalli Arthraxon hispidus Potamogeton franchetii Myriophyllum verticillatum Arundo donax Oenanthe javanica Nasturtium officinale Ranunculus japonicus Acorus calamus Juncus effuses Veronica undulata Equisetum arvense Equisetum ramosissimum Lysimachia barystachys Lythrum salicaria Sparganium stoloniferum Vallisneria natans Chenopodium album Stellaria radians Malachium aquaticum Costus speciosus Nymphaea tetragona Carex tristachya Polypogon fugax Senecio scandens Adenophora trachelioides Scirpus triangulatus Potamogeton crispus Eriachne pallescens Utricularia bifida Spartina alterniflora Achnatherum splendens
Reservoirs
Rivers
1
2
3
4
5
+ + + +
+ +
+
+ + +
+ +
+ + +
+ —
Parks 6
7
+ + + + +
+ +
+
+ + +
+ + + +
+ + + + — +
+ +
+ + + + + +
+
+
+
+
2.2. Sample collection — + +
+ +
In each quadrat (1 m × 1 m), 2 superficial water samples (0–20 cm) were firstly taken by 1 L polypropylene bottles, then 1–3 individuals of each plant species was collected, and finally 2 sediment samples (0–20 cm) were randomly taken by a stainless steel sampler. No quadrat replicates was designed. Both water and sediment samples had two replicates. Some plants species had 2–3 individuals in each quadrat while other plants species only had one individual. A total of 130 superficial water samples, 130 sediment samples and 315 plant samples were obtained. All samples were taken in September 2013. In the study on the changes of MCRs with seasonal and annual shift, we only selected two plants species (reed Phragmites australi and cattail Typha orientalis) in two wetland parks (P-NHZ and P-OLF). This is because reed and cattail are the most common wetland plants and are frequently used in constructed wetland and ecological floating bed; moreover, they are potential feedstock for sustainable bioenergy production. Although other plants such as reed mannagrass (Glyceria maxima) plant also exist in some sites, they are seldom used by human. The reasons for selecting P-NHZ and P-OLF are that (1) their areas are large (800 and 680 hm2), and (2) they locate the North and South region of Beijing city respectively and are very representative. Sampling method was similar to the survey study. Among 12 sampling sites, 5 sampling sites were designed in each wetland park. Sampling was conducted in May 2013 (average air temperature at night and day: 1628℃), September 2013 (16-26℃), May 2014 (16-28℃) and September 2014 (16-25℃), respectively.
+ + + +
+ +
+
+ +
+
+
+ + +
+ +
+ + —
+
+
+ + +
+
+
— +
+
+
— +
+ + + + + + + + — + + + + +
+
+
+ +—
+ —
12
+
+
— +
11
+ +
+
10
+ — +
+ + + + + + + + +
9
+
+
+ +
8
—
+ +
+ + + + +
+ + +
+ + + + +
+ — + + +
+
+ + —
—
+
+
2.3. Sample analysis
+ + + +
+ +
2.3.1. Water sample Samples from each site were analyzed in the field for temperature, pH, dissolved oxygen (DO), water conductivity (EC) and oxidation-reduction potential (ORP) using a portable water quality analyzer (YSI Pro Plus, America). In lab, water samples were filtered through a 0.45 μm membrane filter for the analysis of nitrogen and phosphorus. NH4+-N was determined by the indophenol-blue method described by Aminot et al. (1997), NO3−-N, NO2−-N, total dissolved phosphorus (TDP) and PO43- -P were determined by a flow injection analyzer (SEALAA3,German).
+ — + + + — + + +
— + +
+
+ + + + +
+ +
+
+
+
+
+ +
2.3.2. Sediment sample The ammonia (NH4+-N) was measured by the Nesslerization method; Nitrite (NO2−-N) was measured by N-1 naphthyl ethylenediamine spectrophotometric method at 540 nm; Nitrate (NO3−-N) was determined using an ultraviolet spectrophotometric screening method at 220 and 275 nm (UV-2450, Shimadzu, Kyoto, Japan) (AMWW, 2002). Total organic carbon (TOC) was analyzed with an automatic TOC analyzer (Vario TOC, Elementar, Germany) according to the user manual provided by the manufacturer.
Reservoir: 1- Shahe Reservoir, 2- Miyun Reservoir, 3. Guanting Reservoir; River: 4- Beiyun River, 5- Wenyu River, 6- Yongding River, 7- Guishui River, 8Fenghe River, 9- Liangshui River; Park 10- Olympic Forest Wetland Park, 11Nanhaizi Wetland Park, 12- Hanshiqiao Wetland Park. + indicates the presence of AM symbiosis; — indicates the absence of AM symbiosis; Blanks indicate that no plant is sampled in this urban wetland.
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Table 3 Information on aquatic plants with or without AM symbiosis in urban wetlands in Beijing area. Family
Species
Plant type
MCR (%)
nM/nNM
nTotal
Poaceae
Echinochloa caudata Echinochloa crusgalli Phragmites australi Glyceria maxima Hemarthria altissima Triarrherca sacchariflora Arthraxon hispidus Arundo donax Polypogon fugax Eriachne pallescens Spartina alterniflora Achnatherum splendens Typha orientalis Typha minima Sparganium stoloniferum Salix babylonica Ulmus pumila Polygonum hydropiper Actinostemma tenerum Sagittaria trifolia Alisma plantago-aquatica Rorippa globosa Nasturtium officinale Artemisia argyi Bidens pilosa Inula japonica Senecio scandens Scirpus validus Scirpus planiculmis Scirpus triangulatus Cyperus rotundus Fimbristylis dichotoma Carex tristachya Humulus scandens Rhoeo spathacea Ceratophyllum demersum Potamogeton franchetii Potamogeton crispus Myriophyllum verticillatum Oenanthe javanica Ranunculus japonicus Acorus calamus Juncus effuses Veronica undulata Equisetum arvense Equisetum ramosissimum Lysimachia barystachys Lythrum salicaria Vallisneria natans Chenopodium album Stellaria radians Malachium aquaticum Costus speciosus Nymphaea tetragona Adenophora trachelioides Utricularia bifida
Weed Weed Herb Grass Grass Herb Herb Herb Weed Grass Weed Herb Grass Grass Herb Tree Tree Herb Herb Weed Herb Herb Herb Herb Herb Herb Herb Grass Herb Herb Herb Herb Grass Herb Herb Herb Herb Grass Grass Herb Herb Grass Herb Weed Herb Herb Herb Grass Herb Herb Herb Herb Herb Grass Herb Herb
10.7 ± 4.80 22.0 ± 6.07 23.1 ± 12.3 14.2 ± 10.5 2.66 ± 1.15 9.60 ± 6.07 7.00 ± 7.75 19.1 ± 12.4 52.0 ± 12.0 16.0 ± 9.17 41.3 ± 16.3 4.8 ± 2.68 13.4 ± 7.37 17.7 ± 3.73 0 14.4 ± 6.23 22.5 ± 9.98 16.4 ± 14.7 0 11.3 ± 9.27 14.7 ± 3.06 4.00 ± 2.00 29.3 ± 3.03 3.60 ± 2.61 0 2.67 ± 3.06 41.0 ± 20.9 0 4.00 ± 3.16 3.33 ± 3.06 15.5 ± 4.12 3.60 ± 2.61 0 8.40 ± 3.85 5.11 ± 4.26 19.5 ± 5.51 11.2 ± 3.03 19.6 ± 21.3 0 0 6.67 ± 3.06 4.67 ± 3.01 41.5 ± 7.00 34.0 ± 6.00 25.5 ± 15.9 11.7 ± 7.09 10.5 ± 3.42 5.50 ± 3.42 24.3 ± 15.5 12.9 ± 6.82 21.2 ± 12.7 40.0 ± 25.5 40.7 ± 1.15 8.00 ± 8.49 53.0 ± 15.6 6.00 ± 2.00
9/0 6/0 23/0 10/2 3/0 5/0 3/1 6/1 4/0 3/0 4/0 5/0 17/0 7/0 0/4 5/0 4/0 8/1 0/1 6/0 3/0 3/0 4/0 4/1 0/1 2/1 4/0 0/1 4/1 2/1 4/0 4/1 0/2 5/0 7/2 4/0 5/0 5/0 0/2 0/2 4/0 6/0 4/0 3/0 4/0 5/1 4/0 4/0 6/0 7/0 5/0 2/0 3/0 2/0 2/0 3/0
9 6 23 12 3 5 4 7 4 3 4 5 17 7 4 5 4 9 1 6 3 3 4 5 1 3 4 1 5 3 4 5 2 5 9 4 5 5 2 2 4 6 4 3 4 6 4 4 6 7 5 2 3 2 2 3
Typhaceae
Salicaceae Ulmaceae Polygonaceae Cucurbitaceae Alismataceae Brassicaceae Asteraceae
Cyperaceae
Cannabaceae Commelinaceae Ceratophyllaceae Potamogetonaceae Haloragaceae Apiaceae Ranunculaceae Acoraceae Juncaceae Plantaginaceae Equisetaceae Primulaceae Lythraceae Hydrocharitaceae Amaranthaceae Caryophyllaceae Costaceae Nymphaeaceae Campanulaceae Lentibulariaceae
MCRs are average ± deviation, and nTotal =nM+nNM; nM indicates the number of plant species colonized by AM fungi, and nNM indicates the number of plant species not colonized by AM fungi.
2.3.3. Plant sample 2.3.3.1. Plant species identification. Plant species was identified according to the handbooks: Botanical Illustrations of Aquatic Plant (Zhao and Liu, 2009) and Wetland Plants: Colorful Illustrations of 365 Kinds of Hygrophyte, Aquatic and Marsh Plants (Li and Xu, 2010).
magnification (Giovannetti and Sbrana, 1998). To verify colonization, selected colonized root pieces were mounted on slides and viewed with a compound microscope at 400× magnification.
2.3.3.2. Mycorrhizal colonization rate (MCR). Roots (3 g fresh weight) were cut into 1 cm segments and rinsed and cleared with 10% KOH for 90 min at 90℃. The KOH was rinsed off and the segments acidified with 5% lactic acid for 20 min. Thereafter the roots were then stained with 0.05% (w/v) Trypan blue for 30 min at 90℃. Root segments were determined according to the gridline-intersect method at 25×
All measurements of MCRs were carried out by the same person in the same condition. Relationships between MCR and water characteristics as well as MCR and sediment characteristics were tested using Pearson’s correlation. One-way ANOVA (Duncan’s HSD test) was conducted to test if seasonal or annual shift had effects on MCRs at the significance level α < 0.05. Statistical analyses were conducted using
2.4. Statistical analysis
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Table 4 Mycorrhizal colonization rates in reed, cattail and reed mannagrass in urban wetlands. Sample sites
RE-SH RE-MY RE-GT R-BY R-WY R-YD R-GS R-FH R-LS P-OLF P-NHZ P-HSQ
Reed
Cattail
Reed mannagrass
Range
Mean ± SD
Range
Mean ± SD
Range
Mean ± SD
12–22% 12–14% 12–20% 10–44%
17.3 ± 5.03% 13 ± 1.41% 16.0 ± 4.00% 22.5 ± 14.9%
6% 2%
6% 2%
10%
10%
28–46% 24–38%
37.0 ± 12.7% 31.0 ± 9.90%
10–14% 18–24% 18–24% 26–32%
12.0 ± 2.83% 17.3 ± 7.02% 20.7 ± 3.05% 29 ± 4.24%
12% 12–26% 10% 10–16%
12% 19.0 ± 9.90% 10% 14.0 ± 2.00%
4–10% 8–40% 14–46% 18%
7.0 ± 4.20% 23.8 ± 11.9% 31.0 ± 10.2% 18%
8–24% 10–26%
19.0 ± 4.76% 17.3 ± 9.45%
8–38%
19.3 ± 16.3%
RE-SH: Shahe Reservoir; RE-MY: Miyun Reservoir; RE-GT: Guanting Reservoir; R-BY: Beiyun River; R-WY: Wenyu River; R-YD: Yongding River; R-GS: Guishui River; R-FH: Fenghe River; R-LS: Liangshui River; P-OLF: Olympic Forest Wetland Park; P-NHZ: Nanhaizi Wetland Park; P-HSQ: Hanshiqiao Wetland Park. Blanks indicate that no these plants were sampled in this urban wetland.
NO2−-N (r = 0.888, p < 0.05) (Fig. 7). Although MCRs in cattail and reed mannagrass plants did not show significant correlation with NO3−-N (p > 0.05), the evident change trends were observed.
SPSS 17.0 software package. 3. Results 3.1. AM fungal colonization in urban wetland plants
3.4. Effects of MCRs dynamic with seasonal and annual shift in urban wetland
In total, 315 specimens of 56 hydrophyte species were investigated. Typical AM structures (arbuscule, hyphae and vesicle) were observed in 49 hydrophyte species, and the proportion was up to 87.5% (Tables 2 and 3). MCRs ranged from 2% to 72%, while most of them were relative low (< 25%). Tephroseris palustris had the highest MCR as 72%. Even the same plant species, MCRs varied with different sampling sites. For example, MCR was 40% in Phragmites austral collected from R-YD, while it was only 20% in Phragmites austral collected from RE-GT. This can also be seen from Table 4, which showed MCRs in reed, cattail and reed mannagrass in various urban wetlands.
In both NHZ and OLF wetland parks, MCRs in reed plant in Spring (May) were higher than in Autumn (September) but the difference was not significant in P-NHZ (Fig. 8a). However, MCRs in cattail showed contrary trends between two seasons, and the difference was also not significant in P-OLF (Fig. 8b). This indicated that AM formation was affected by seasonal shift, while positive or negative effects depended on plant species. Fig. 9 showed MCRs dynamic with annual shift in reed and cattail plants. It can be seen that MCRs in reed plant showed upward trends from May 2013 to May 2014, but the difference was not significant (Fig. 9a). In cattail, however, MCRs in May 2013 were significantly lower than in May 2014 (Fig. 9b). This indicated that AM formation was affected by annual shift, while positive or negative effects depended on plant species.
3.2. Correlation of MCRs and water properties in urban wetlands In reed plant, Pearson’s correlation analysis indicated that MCRs did not exhibit significant correlation to water properties except for NH4+N and TDP (Fig. 2). MCRs were significantly and negatively correlated to water NH4+-N and TDP concentrations (rNH4-N = 0.636, pNH4N < 0.01; rTDP = 0.562, pTDP < 0.05). In cattail plant, Pearson’s correlation analysis indicated that MCRs also did not exhibit significant correlation to water properties except for ORP (Fig. 3). MCRs were significantly and negatively correlated to water ORP (r = 0.724, p < 0.05). In reed mannagrass plant, no significant correlation between MCRs and water properties was found (Fig. 4). Generally, MCRs presented change trends with most water properties, but the correlation was not significant (p > 0.05). For example, MCRs in three wetland plants showed upwards trend with increasing EC, and showed downward trends with increasing water PO43−-P concentrations (Figs. 2–4).
4. Discussion 4.1. Plants with AM symbiosis in urban wetlands In this study, the proportion of wetland plant species (87.5%) which were colonized by AM fungi was higher than that in most previous studies (Radhika and Rodrigues, 2007; Weishampel and Bedford, 2006; Seerangan et al., 2010; Zhao et al., 2016). The possible reasons include that (1) dispersal of AM fungi is changed by hydraulic engineering, such as wetland eco-restoring project and municipal engineering, and (2) plants are collected from big area, and thus plants have high probability to be colonized by AM fungi. This may be confirmed by present study. Plants species without AM symbiosis were collected from a few sampling sites (< 3), such as Scirpus validus, Actinostemma tenerum and Bidens pilosa from one sampling site, and Myriophyllum verticillatum, Oenanthe javanica and Carex tristachya from two sampling sites. It cannot be denied that there are contrary results. For example, Scirpus validus (Liberta et al., 1983; Bauer et al., 2003) and Bidens pilosa (Zhao et al., 2016) were reported to establish AM symbiosis. The detailed reasons need further study. MCRs were relative low in most wetland plants (< 25%), indicating that most plants may be difficult to be colonized by AM fungi in wetland habitat. This result is consistent with some previous studies (Wang
3.3. Correlation of MCR and sediment properties in urban wetlands In reed plant, Pearson’s correlation analysis indicated that MCR was significantly and positively correlated to sediment NO3−-N, NO2−-N and TOC (rNO3-N = 0.631, pNO3-N < 0.05; rNO2-N = 0.661, pNO2N < 0.05; rTOC = 0.694, pTOC < 0.01) (Fig. 5). In cattail plant, MCR was significantly and positively correlated to sediment TOC (r = 0.855, p < 0.05) (Fig. 6). In reed mannagrass plant, MCRs were significantly and positively correlated to only sediment 37
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Fig. 2. Correlation between MCR in reed and water properties. “r” indicates Pearson’s correlation coefficient, “p” indicates test of significance by two-tailed, “n” indicates sample number. DO: dissolved oxygen; EC: water conductivity; ORP: oxidation-reduction potential; TDP, total dissolved phosphorus.
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Fig. 3. Correlation between MCR in cattail and water properties. “r” indicates Pearson’s correlation coefficient, “p” indicates test of significance by two-tailed, “n” indicates sample number. DO: dissolved oxygen; EC: water conductivity; ORP: oxidation-reduction potential; TDP, total dissolved phosphorus.
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Fig. 4. Correlation between MCR in reed mannagrass and water properties. “r” indicates Pearson’s correlation coefficient, “p” indicates test of significance by twotailed, “n” indicates sample number. DO: dissolved oxygen; EC: water conductivity; ORP: oxidation-reduction potential; TDP, total dissolved phosphorus.
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Fig. 5. Correlation between MCR in reed and sediment properties. “r” indicates Pearson’s correlation coefficient, “p” indicates test of significance by two-tailed, “n” indicates sample number. TDP, total dissolved phosphorus; TOC: total organic carbon.
characteristics due to difference in geographical position. AM fungi species also varies with different wetlands. For example, Glomus mosseae and Glomus claroideum were the dominant AM fungi in the studies of Wang and Zhao (2006) and Radhika and Rodrigues (2007) respectively, while in the study of Wilde et al. (2009), the dominant AM fungi was Glomus intraradices.
and Zhao, 2006; Zhao et al., 2016). However, high MCRs in some wetland plants were found (> 40%), such as Costus speciosus, Polypogon fugax, Adenophora trachelioide and Senecio scandens. Similar phenomena are also reported in previous studies. Seerangan et al. (2010) found that MCRs ranged from 49.19% (Oryza sativa) to 86.05% (Lindernia parviflora) in 8 hydrophytes and 50 wetland plants species from four sites in south India. MCRs in same plant also showed great variation. For example, MCR was 72% in Senecio scandens collected from P-NHZ while it was only 30% in same plant species collected from RE-SH, R-WY and R-YD. Similar phenomena are reported in previous studies. Beck-Nielsen and Madsen (2001) found no mycorrhizal colonization in submerged specimens while very low colonization levels were found in the same emerged species. It has been reported that, depending on the habitats, cattail was colonized or not by AM fungi (Stenlund and Charvat, 1994; Thormann et al., 1999). This difference may be related to wetland habitat and AM fungi species. Different wetland habitats often have various water levels, water temperatures, and water and sediment
4.2. Effects of water and sediment properties on AM formation in urban wetlands It has been confirmed that AM formation is affected by many factors in terrestrial environment, such as soil nutrients, pH, compaction, moisture stress, pollutants (Soka and Ritchie, 2014; Lenoir et al., 2016). In wetland habits, AM formation may be also affected by a variety of environmental factors, such as hydrological conditions (Miller and Bever, 1999; Wang et al., 2011), nutrients (Wang et al., 2010), pH and electric-conductivity levels (D’Souza and Rodrigues, 2013). Although many studies have concerned this subject, up to now no agreement has 41
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Fig. 6. Correlation between MCR in cattail and sediment properties. “r” indicates Pearson’s correlation coefficient, “p” indicates test of significance by two-tailed, “n” indicates sample number. TDP, total dissolved phosphorus; TOC: total organic carbon.
Wang et al., 2010). In this study, however, AM fungal colonization in three plants was not affected by PO43−-P and TDP concentrations in water and sediment except for the fact that water TDP and AM colonization in reed showed negative correlation. This result almost supports the finding of Miller et al. (1999) in a comprehensive study, in which soil P availability and AM fungal colonization in the genus Carex did not show significant correlation. Van Hoewyk et al. (2001) also found that the extent of AM fungal colonization of Dasiphora floribunda did not vary among calcareous wetlands of different soil P concentrations. This suggests that P availability may not be the key factor for AM formation in wetland. Certainly, the difference may be related to plant species, AM fungal species, P level and other coexisted factors (such as pH, ORP). For example, Stevens et al. (2002) found that AM colonization levels in Lythrum salicaria were significantly reduced at P concentrations of 5 mg L-1 and higher, while Xie et al. (2014) found that the optimal P level for AM fungal colonization in mangrove species Kandelia obovata was 30 mg kg-1. AM fungal species also differ in the extent to which phosphate decreases mycorrhiza formation (Thomson et al., 1986).
been reached in most cases. In the present study, MCRs in reed were negatively correlated to water NH4+-N, TDP and MCRs in cattle were negatively correlated to ORP. MCR decreases with increasing water NH4+-N, possibly because high concentrations of NH4+-N inhibits the germination of AM fungal spores and is toxic to AM fungal colonization (Cornejo et al., 2007). ORP plays a role in AM formation in wetland plant. Beck-Nielsen and Madsen (2001) found that the redox potential in sediments with noninfected specimen ranged from 54 to 280 mV and in sediments with infected species from 250 to 530 mV. ORP in the rhizosphere of wetland plants generally ranges from 130 mV to 350 mV (Li et al., 2014), so this means AM formation in wetland plant is inhibited in most cases. This may explain why MCRs were low in most wetland plants in this study. Presently, however, it is difficult to provide reasonable explanation on that MCRs were negatively correlated with ORP in cattail. We will continue to concern this subject in further study. It has been confirmed that AM formation is sensitive to available P, since many previous studies confirm that both low and high P can inhibit AM fungal colonization (Koide and Li, 1990; Chen et al., 2008; 42
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Fig. 7. Correlation between MCR in reed mannagrass and sediment properties. “r” indicates Pearson’s correlation coefficient, “p” indicates test of significance by twotailed, “n” indicates sample number. TDP, total dissolved phosphorus; TOC: total organic carbon.
Fig. 8. Effect of seasonal shift on MCRs dynamic in reed and cattail plant in urban wetlands. Different lowercase letters indicate a significant difference between two seasons at p = 0.05 in each wetland park. P-NHZ: Nanhaizi Wetland Park; P-OLF: Olympic Forest Wetland Park.
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Fig. 9. Effect of temporal shift on MCRs dynamic in reed and cattail plant in urban wetlands. Different lowercase letters indicate a significant difference between two years at p = 0.05 in each wetland park. P-NHZ: Nanhaizi Wetland Park; P-OLF: Olympic Forest Wetland Park.
MCRs in reed showed positive correlation to sediment NO3−-N, NO2−-N or TOC, showed positive correlation to sediment TOC in cattail, and showed positive correlation to sediment NO2−-N in reed mannagrass. This is possibly because the concentrations of sediment NO3−-N, NO2−-N and TOC are low relative to plant requirement in most sampling sites, and they are the inhibitive factors for plant growth. In higher concentrations of NO3−-N, NO2−-N and TOC, plant growth is better and in turn facilitates AM fungal propagation and colonization. Fraser and Feinstein (2005) found that growth of the wetland plants was limited more by nitrogen than by phosphorus. Certainly, if sediment nutrients are high enough, AM fungal propagation and colonization might be inhibited. There is a solid evidence showing that an appropriate application of organic matter could promote AM fungal colonization in host species (Hodge and Fitter, 2010), while excess organic matter can be harmful to this symbiotic relationship (Sáinz et al., 1998). Due to few studies on the relationship between AM formation and N in wetland (Miller, 2000), it is difficult to further discuss effect of N on AM formation. In the present study, MCRs in three plants didn’t show significant correlation with water DO. This is different from previous studies (Miller and Bever, 1999; Beck-Nielsen and Madsen, 2001; Wang et al., 2014). This is possibly because (1) three plants are rooted emergent plants and thus MCRs are slightly affected by water DO; (2) AM fungi can obtain oxygen directly from root through aerenchyma and slightly depend on water DO; and (3) water DO little varies in all sampling sites (0–40 mg L−1) and thus it is difficult to show significant correlation between them.
revealed that season and host coaffected AM spore density and species richness with the former having greater influence than the latter. Seasonal variation of water regimes in wetlands likely provides the soil with opportunities to aerate, thus providing the AM fungi with periods of increased oxygenation for survival. For example, Ipsilantis and Sylvia (2007) found that AM root colonization was least during the dry winter and spring seasons and greatest in the flooded summer and fall seasons in several plant communities (i.e., Panicum, Cladium, and Typha). In both two wetland parks, MCRs in reed were higher in 2013 than in 2014, while contrary result was found in cattail. This is possibly related to AM fungal species and plant species that are different in cold tolerance. The lowest temperature is -14℃ in January 2013 in Beijing, which can threaten wetland plant survival. Cattail generally has greater cold tolerance than reed, and this may make cattail has good growing in next year. Different AM fungal species also have different cold tolerance (Varga et al., 2015), so they have different colonization ability after low temperature stress. Berch and Kendrick (1982) found that plant physiology and turnover of plant roots are among the drivers of AM fungal seasonality. This may be another reason that resulted in MCR variation with annual shift. 5. Conclusions Urban wetland functions may be improved by AM fungi, such as providing recreational and landscape space, natural scenic beauty, and buffering against noise and pollution. For this reason, it is necessary to deeper investigate the role of AM symbiosis in urban wetland. In our study, we found that 87.0% of urban wetland plants (49 of 56 species) were colonized by AM fungi, and MCRs ranged from 2% to 72%. In the investigation on three plants (Phragmites australi, Typha orientalis and Glyceria maxima), AM formation was affected by water and sediment properties, and the latter had greater effects than the former. Moreover, MCRs showed seasonal and temporal variation. As a whole, although most MCRs were lower than 25% in urban wetland plants, it is promising to use AM fungi to improve urban wetland functions. AM formation in urban wetland plants can be increased by regulating some properties of water and sediment.
4.3. MCRs dynamics with seasonal and temporal shift in urban wetlands Few studies have concerned the MCRs dynamic with seasonal and temporal shift in wetlands (Turner and Friese, 1998; Miller, 2000; Oliveira and Dodd, 2001; Bohrer et al., 2004). In this study, MCR in reed was higher in May than in September, showing significant seasonal variation exists. This is consistent to the result of Bohrer et al. (2004) in wetlands, in which AM fungal colonization was the highest in Spring and was the lowest in Summer. This is possibly because AM fungal colonization coordinates with plant growth stages, and reed root activity is vigorous in May (Engloner, 2009). Bohrer et al. (2004) concluded that abiotic factors had minimal influence on AM fungal colonization variation, so AM seasonal dynamics was in response to plant phenology. However, MCR in cattail was lower in May than in September, which is contrary to MCR in reed. This is possibly because cattail growth is later than reed (about mid-April) and keeps long time (till to end of October), so cattail growth is vigorous in September. Certainly, we should not neglect the effects of seasonal shift and water table level on AM fungal activity. D’Souza and Rodrigues (2013)
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