Ecotoxicology (2014) 23:11–20 DOI 10.1007/s10646-013-1146-x

Interactive effects of elevated ozone and UV-B radiation on soil nematode diversity Xuelian Bao • Qi Li • Jianfeng Hua Tianhong Zhao • Wenju Liang



Accepted: 14 October 2013 / Published online: 25 October 2013 Ó Springer Science+Business Media New York 2013

Abstract Ultraviolet-B (UV-B) radiation and elevated tropospheric ozone may cause reductions in the productivity and quality of important agricultural crops. However, research regarding their interactive effect is still scarce, especially on the belowground processes. Using the open top chambers experimental setup, we monitored the response of soil nematodes to the elevated O3 and UV-B radiation individually as well as in combination. Our results indicated that elevated O3 and UV-B radiation have impact not only on the belowground biomass of plants, but also on the community structure and functional diversity of soil nematodes. The canonical correspondence analysis suggested that soil pH, shoot biomass and microbial biomass C and N were relevant parameters that influencing soil nematode distribution. The interactive effects of elevated O3 and UV-B radiation was only observed on the abundance of bacterivores. UV-B radiation significantly increased the abundance of total nematodes and bacterivores in comparison with the control at pod-filling stage of

X. Bao  Q. Li (&)  W. Liang State Key Laboratory of Forest and Soil Ecology, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang 110164, China e-mail: [email protected] X. Bao University of Chinese Academy of Sciences, Beijing 100049, China J. Hua Institute of Botany, Jiangsu Province and Chinese Academy of Sciences, Nanjing 210014, China T. Zhao College of Agronomy, Shenyang Agricultural University, Shenyang 110161, China

soybean. Following elevated O3, nematode diversity index decreased and dominance index increased relative to the control at pod-filling stage of soybean. Nematode functional diversity showed response to the effects of elevated O3 and UV-B radiation at pod-bearing stage. Higher enrichment index and lower structure index in the treatment with both elevated O3 and UV-B radiation indicated a stressed soil condition and degraded soil food web. However, the ratios of nematode trophic groups suggested that the negative effects of elevated O3 on soil food web may be weakened by the UV-B radiations. Keywords Elevated ozone  Ultraviolet-B radiation  Soil nematodes  Open-top chambers  Soybean

Introduction The concentrations of O3 have been decreasing in the upper atmosphere, and increasing in the lower atmosphere (The Royal Society 2008), which led to two separate environmental problems. On one hand, the depletion of the stratosphere O3 layer due to manmade chloride and bromide compounds has led to an increment in ultraviolet-B (UV-B) radiation approaching the earth (UNEP and EEAP 2009). On the other hand, the increase of ground-level O3 (tropospheric O3) has caused significant biological and economic damage to plants (Avnery et al. 2013). UV-B radiation and elevated tropospheric O3 may occur together and cause reductions in plant photosynthesis and carbon fixation, thus resulting in nutrition-limiting stresses (Reiling and Davison 1995) and alteration in soil C flux. However, researches regarding their interactive effects are still limited (Ambasht and Agrawal 2003; Tripathi and Agrawal 2013; Rinnan et al. 2013), and most of them

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focused on the above-ground subsystem (Feng and Kobayashi 2009; Li et al. 2002; Chen et al. 2011). Tripathi et al. (2011) and Tripathi and Agrawal (2013) reported negative effects of enhanced UV-B and tropospheric O3 on linseed including lipid peroxidation, decrease in yield and quality of oil and seeds. Pliura et al. (2008) found that changes in genetic variation of silver birch under elevated O3 and UV-B radiation can alter adaptation, stability, and competitive ability of regenerating populations. These studies have showed that interactive effect of enhanced UV-B and elevated O3 had significant effects on physiological characters and yield components in different plants/ ecosystems. Soil organisms are responsible for recycling nutrients and for maintenance of soil properties which may be affected by altered allocation patterns in plants (Andersen 2003). The individual effect of elevated O3 and UV-B radiation on soil organisms and decomposition processes has been well acknowledged (Caldwell et al. 2007). Tingey et al. (2006) in a chamber experiment found no effects of ozone on soil respiration, fine root biomass and soil fauna. Qiu et al. (2009) reported that soil ozone fumigation could reduce the abundance of Meloidogyne javanica and freeliving nematodes in a sandy loam soil. Li et al. (2012) using free-air ozone enrichment platform found that elevated O3 decreased the fungal PLFA and the fungi to bacteria ratio. On the other hand, enhanced UV-B radiation led to decrease in soil respiration rates (Hu et al. 2010) and the abundance of soil nematodes (Koti et al. 2007). In a UV-B exclusion experiment of Argentina, Robson et al. (2005) found that near-ambient UV-B negatively influenced the numbers of rotifers, nematodes and mites in a Sphagnum peatland. However, researches regarding their interactive effect on the belowground processes are still scarce (Ambasht and Agrawal 2003; Tripathi and Agrawal 2013; Rinnan et al. 2013), which may limit our understanding of the impacts of elevated O3 and UV-B radiation on soil ecosystems. Soybean (Glycine max) is one of the most important crops all over the world. The effects of enhanced O3 and UV-B radiation on growth, morphology and yield of soybean have been studied widely (Li et al. 2002; Kakani et al. 2003; Feng and Kobayashi 2009). These changes can reduce the allocation of assimilates into the root (Andersen 2003; Chen et al. 2009); and then affect the interactions among soil organisms (McCrady and Andersen 2000). In agroecosystems, soil nematodes were regarded as key members of detrital food web, which directly involved in nutrient mineralization and organic matter decomposition (Wardle 2002). Therefore, the objective of this study was to evaluate the response of soil nematodes to the elevated O3 and UV-B radiation individually as well as in combination using the open top chambers (OTC). Yield

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formation period of soybean (from pod-bearing stage to pod-filling stage) is conjunction with the upward transportation of carbohydrate (Chen et al. 2011). Changes in the distribution of carbohydrate might lead to changes in root exudation and/or root turnover, and then affect soil organisms. In this study, we monitored pod-bearing and pod-filling stages of soybean to evaluate the temporal variations in soil nematode community under different treatments. We hypothesized that the interactive effect of elevated O3 and UV-B radiation on soil nematode community was more detrimental than individually due to relatively lower crop residue or plant C input to the soil.

Materials and methods Experimental site and design The experimental site is located in the Shenyang Experimental Station of Ecology, Chinese Academy of Sciences (41°310 N, 123°220 E). This region has a continental monsoon climate with a mean annual temperature of 7.0–8.0 °C, an annual precipitation is 650–700 mm, and an annual non-frost period of 147–164 days. The soil at the study site is classified as an aquic brown soil (silty loam Hapli-Udic Cambosols in Chinese Soil Taxonomy), with 11.28 g kg-1 organic C, 1.20 g kg-1 total N, 0.41 g kg-1 total P, pH (H2O) 6.7 at 0–15 cm depth. The study was conducted on soybean (Glycine max) plants grown in open-top chambers (OTCs), which were established in 2008. The OTCs were 1.15 m in diameter and 2.4 m in height with a 45° sloping frustum and the minimum distance between any two chambers was 4 m. The experimental design was based on completely randomized plots including four treatments belonging to eight OTCs: (1) control (hereinafter referred to as CK, ambient ozone concentration about 45 nmol mol-1; ambient UV radiation intensity about 0.30 W m-2); (2) elevated O3 (ozone concentration of 110 ± 10 nmol mol-1; no artificially UV-B tube); (3) UV-B (ozone concentration about 45 nmol mol-1; UV-B radiation intensity of 0.32 W m-2); (4) O3 9 UVB [a combination of elevated O3 (110 ± 10 nmol mol-1) and UV-B (0.32 W m-2)]. Each treatment has two replicated OTCs and each OTC was divided into two compartments that were subjected to the same treatment as two replications, so all together there are 4 replications for each treatment. Ozone was produced from pure oxygen with an ozone generator (GP-5J, China). Ozone concentrations were continuously monitored by ozone analyzers (S-900 Aeroqual, New Zealand), and were controlled by computers using a professional program for ozone dispensing and monitoring (Zhao et al. 2010). UV-B was artificially supplied with UV-B radiation by 40 W

Interactive effects of elevated ozone

fluorescent tubes (Beijing Lighting Research Institute, peak value was 305 nm) held in mobile and adjustable frames over each pot row. In UV-B treatments, UV-B tubes were covered with 0.08 mm cellulose diacetate filters (to absorb radiation below 280 nm). The distance between the top canopies of the plants and the lamps was maintained at 40 ± 2 cm by the mobile frames to provide UV-B doses of 0.32 W m-2, equivalent to those 5 % enhanced in average of solar UV-B radiation (0.30 W m-2) at Shenyang during clear sky conditions in summer. Plants were exposed to elevated ozone or/and UV-B radiations for 8 h (09:00–17:00) per day in the middle of the photoperiod from June 20 to September 7. The potted soybean (Glycine max) cultivar was Tiefeng 29, which was seeded in each pot (26 9 36 cm2) on May 20 in 2011. Five plants in three leaves stage were established in each pot. Thiry-six pots in each OTC were divided into six rows, every subplot as one replication including three rows (18 pots). The pots were periodically watered to prevent water deficit. Any detected insects were manually removed and standard cultivation practices were followed in all experimental pots. Soil samples were collected from 0 to 15 cm depth at pod-bearing stage (August 12, 2011) and pod-filling stage (September 2, 2011) of soybean. Each soil sample pooled from five soil cores were taken in a mid-row of pots of 2.5 cm diameter and stored at 4 °C until further analyses. Yield parameters were measured using ten plants from each treatment. Soil and plant analyses Soil moisture (SM) was determined as the loss in mass after drying soil at 105 °C for 24 h. Soil pH was determined with a glass electrode in 1:2.5 soil:water solution (w/v). Soil microbial biomass was determined using the fumigation-extraction method (Vance et al. 1987). Both soil microbial biomass C (MBC) and N (MBN) in the filtrate were determined using a TOC analyzer (Multi C/N 3000, Analytik Jena, Germany). Soil basal respiration (SBR) was determined using static alkali absorption method (Kirita 1971). Soybean plants from each pot were partitioned into grain and litter. Litter and grain samples were dried at 65 °C until a constant weight was obtained, and then weighted for individual plant (shoot weight and root weight). Nematode community analysis Nematodes were extracted from 100 g of soil (fresh weight) by a modified cotton-wool filter method (Oostenbrink 1960; Townshend 1963). Nematode populations were

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expressed as number of nematodes per 100 g dry soil and at least 150 nematodes from each sample were identified to genus level using an inverted compound microscope. The nematodes were assigned to the following trophic groups characterized by feeding habits (1) bacterivores (Ba); (2) fungivores (Fu); (3) omnivore–carnivores (Om–Ca) and (4) plant parasites (H) following Yeates et al. (1993). The following nematode community indices were calculated: (1) Shannon–Wiener diversity index: H0 = P P - piln(pi); (2) Dominance index: k = p2i ; (3) Evenness index: J0 = H0 /ln(S); where pi is the proportion of individuals in the taxon and S is the number of taxa (Yeates and Bongers 1999); (4) Channel index CI = 100 9 (0.8Fu2)/(3.2Ba1 ? 0.8Fu2); (5) Structure index SI = P P P 100 9 ( ksns/( ksns ? kbnb)); (6) Enrichment index P P P EI = 100 9 ( kene/( kene ? kbnb)); where kb is the weight assigned to guilds Ba2 and Fu2 and nb is the abundance of nematodes in guilds Ba2 and Fu2, which indicate basal characteristics of the food web; ks the weight assigned to guilds Ba3–Ba5, Fu3–Fu5, Om4–Om5 and Ca2– Ca5, ns is the abundance of nematodes in these guilds, which represent the structure condition of the food web; ke the weight assigned to guilds Ba1 and Fu2, and ne is the abundance of nematodes in these guilds, which represent an enriched condition of the food web (Ferris et al. 2001). Bax, Fux, Cax, Omx, (where x = 1–5) represent the functional guilds of nematodes that are bacterivores, fungivores, carnivores and omnivores where the guilds have the characters indicated by x on the colonizer–persister (c–p) scale (1–5) following Bongers and Bongers (1998). Statistical analysis Nematode abundance was log-transformed prior to statistical analysis. Repeated measures ANOVAs (RMANOVA) were used to examine the temporal variations and the overall effects of elevated O3 and UV-B on environmental parameters, and soil nematode community structure. Between-subject effects were evaluated as elevated O3, elevated UV-B radiation, and their interactions, and withinsubject effects were growth stages (pod-bearing and podfilling stages of soybean) and its interactions with elevated O3 or UV-B. The least significant difference (LSD) test was conducted when the treatment effects were significant at each growth stage. All statistical analyses were performed by SPSS statistical software (SPSS Inc., Chicago, IL, USA). Difference at P \ 0.05 level was considered to be statistically significant. Canonical correspondence analysis (CCA) was performed to study the relationships between soil nematodes and environmental parameters using CANOCO software (ter Braak 1988).

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Table 1 Results (P values) of repeated measures ANOVAs on the effects of elevated O3 (O3), UV-B radiation (U), growth stage (S), and their interactions on environmental parameters, soil nematode community and ecological indices Response

Environmental parameter

Nematode community

Ecological indices

Index

Effect O3 (O3)

UV-B (U)

O3 9 U

Stage (S)

S 9 O3

S9U

S 9 O3 9 U ns

SM

ns

ns

ns

ns

ns

ns

pH

P \ 0.01

P \ 0.01

0.015

ns

0.009

ns

ns

SBR MBC

ns ns

ns P \ 0.01

ns ns

ns ns

ns ns

0.030 ns

ns ns

MBN

ns

0.046

ns

0.022

ns

ns

ns

Shoot

ns

ns

ns

P \ 0.01

ns

ns

ns

Root

P \ 0.01

P \ 0.01

P \ 0.01

P \ 0.01

P \ 0.01

P \ 0.01

P \ 0.01

Root:shoot

P \ 0.01

P \ 0.01

ns

P \ 0.01

P \ 0.01

P \ 0.01

P \ 0.01

TNEM

P \ 0.01

P \ 0.01

ns

P \ 0.01

ns

ns

ns

BF

ns

ns

0.030

P \ 0.01

ns

P \ 0.01

ns

FF

ns

ns

ns

P \ 0.01

ns

ns

ns ns

PP

ns

P \ 0.01

ns

ns

ns

ns

OP

ns

ns

ns

P \ 0.01

P \ 0.01

ns

ns

(BF ? FF)/PP

0.016

P \ 0.01

ns

ns

ns

ns

ns

OP/PP

0.026

0.013

ns

ns

0.049

ns

ns

k

ns

P \ 0.01

P \ 0.01

P \ 0.01

ns

ns

ns

H0

ns

P \ 0.01

P \ 0.01

P \ 0.01

ns

ns

ns

J0 CI

ns 0.033

0.012 ns

ns 0.049

0.038 ns

ns ns

ns ns

ns ns

SI

0.028

0.028

ns

ns

ns

P \ 0.01

ns

EI

ns

ns

ns

ns

ns

0.019

0.019

Significant effects (P \ 0.05) were indicated SM soil moisture, SBR soil basal respiration, MBC microbial biomass carbon, MBN microbial biomass nitrogen, Shoot shoot biomass, Root root biomass, Root:Shoot ratios of root biomass to shoot biomass, TNEM total nematodes, BF bacterivores, FF fungivores, PP plant-parasites, OP omnivore–carnivores, k Simpson dominance index, H0 Shannon–Wiener index, J0 evenness index, CI channel index, SI structure index, EI enrichment index, ns non-significant differences

Results Enviromental parameters No growth stage effects were observed on soil physiochemical parameters except for microbial biomass N (P = 0.022, Table 1). UV-B radiation significantly increased microbial biomass C (P \ 0.01) and microbial biomass N (P = 0.046) relative to the treatments without UV-B (CK and elevated O3) at pod-filling stage. Similar patterns were also observed on the values of SBR and pH at pod-bearing stage, with a stronger UV-B effect found in SBR (Table 2). Significant interactive effect between elevated O3 and UV-B radiation was only observed in pH (P = 0.015, Table 1), with lower pH values observed in the O3 and O3 9 UVB treatments relative to the other treatments. Significant temporal variations (P \ 0.01, Table 1) were observed in plant growth. During the soybean growth stages, the biomass of root responded obviously to the elevated O3, UV-B radiation and their interaction

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(P \ 0.01, Table 1). At both growth stages of soybean, changes of shoot and root biomass were as follows CK [ UV-B [ O3 [ O3 9 UVB (Table 2). Elevated O3 decreased the root to shoot ratio obviously at pod-bearing and pod-filling stages in comparison with the treatments without O3 elevation (CK and UV-B) (Table 2).

Soil nematode community Significant temporal variations were observed in the abundance of total nematodes and nematode trophic groups (P \ 0.01, Table 1), except for plant-parasites. UV-B radiation significantly increased the abundance of total nematodes in comparison with the CK (P \ 0.01, Table 1; Fig. 1b) at pod-filling stage. During the study period, different nematode trophic groups showed response to elevated O3 and UV-B radiation, with more obvious treatment effects observed at podfilling stage. The interactive effect of elevated O3 and

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Table 2 Environmental parameters at pod-bearing and pod-filling stages of soybean under elevated O3 and UV-B conditions (mean ± SD) Index

Growing season

Treatment CK

SM (%) pH

MBN (lg g-1) Shoot (g)

O3 9 UVB

Pod-bearing

18.18 ± 6.39

18.78 ± 6.21

22.85 ± 2.50

20.54 ± 3.74

20.25 ± 1.67

17.66 ± 4.07

20.70 ± 2.42

17.51 ± 2.44

Pod-bearing Pod-bearing Pod-filling

MBC (lg g-1)

UVB

Pod-filling Pod-filling SBR (lg CO2 g-1 d-1)

O3

Pod-bearing Pod-filling

5.62 ± 0.17b

5.56 ± 0.13b

6.27 ± 0.42a

5.93 ± 0.20ab

5.73 ± 0.33b

5.34 ± 0.12c

6.45 ± 0.09a

5.42 ± 0.18c

19.83 ± 6.57b

19.98 ± 6.84b

41.35 ± 6.26a

27.99 ± 9.33b

28.14 ± 2.75a

18.08 ± 2.95b

29.25 ± 5.68a

24.46 ± 2.43a

145.76 ± 18.62 186.09 ± 40.81bc

172.41 ± 57.54 159.20 ± 33.67c

240.99 ± 29.50 235.39 ± 22.98a

178.90 ± 89.72 219.47 ± 26.07ab

Pod-bearing

19.83 ± 8.07

17.35 ± 8.24

25.77 ± 4.52

20.58 ± 11.47

Pod-filling

25.26 ± 2.80b

24.75 ± 6.72b

34.06 ± 7.18a

27.27 ± 1.54ab

Pod-bearing

25.91 ± 1.02a

17.94 ± 0.53c

19.76 ± 1.15b

15.06 ± 0.69d

Pod-filling

46.11 ± 1.10a

38.03 ± 1.12c

40.31 ± 1.17b

34.12 ± 1.93d

2.87 ± 0.09a

1.81 ± 0.09c

2.12 ± 0.18b

1.45 ± 0.08d

Root (g)

Pod-bearing Pod-filling

3.16 ± 0.07a

1.48 ± 0.05c

1.94 ± 0.11b

1.18 ± 0.13d

Root:shoot

Pod-bearing

0.11 ± 0.01a

0.10 ± 0.00bc

0.11 ± 0.01ab

0.10 ± 0.00c

Pod-filling

0.07 ± 0.00a

0.04 ± 0.00bc

0.05 ± 0.00ab

0.04 ± 0.01c

Significant effects (P \ 0.05) were indicated in each row with the same letters suggested non-significant differences in LSD tests SM soil moisture, SBR soil basal respiration, MBC microbial biomass carbon, MBN microbial biomass nitrogen, Root root biomass, Shoot shoot biomass, Root:Shoot ratios of root biomass to shoot biomass

UV-B radiation was only observed on the abundance of bacterivores (P = 0.030, Table 1). In comparison with CK, the abundance of bacterivores was lower in the UV-B treatments at pod-bearing stage (Fig. 1c), while an opposite trend was observed at pod-filling stage, which increased following UV-B radiation (Fig. 1d). The abundance of fungivores and omnivore-predators were significantly lower in the O3 9 UVB treatment than those in the CK (Fig. 1f, j). During the study period, the abundance of plant-parasites only showed response to UV-B radiation (P \ 0.01, Table 1) at pod-bearing stage, with higher values observed in the UV-B and O3 9 UVB treatments than other treatments (Fig. 1g). At pod-filling stage of soybean, changes in the abundance of omnivore-predators were as follows UV-B [ CK [ O3 9 UVB [ O3 (Fig. 1j). Elevated O3 and UV-B radiation significantly influenced the ratio of microbivorous nematodes to plant-parasites (Table 1), with higher values observed in the O3 treatments in comparison with the other treatments at pod-bearing stage (Fig. 2a). The interactive effect of sampling stage and elevated O3 was observed on the ratio of omnivore-predators to plant-parasites (P = 0.049, Table 1), with lower values observed in the O3 treatments compared to the CK at pod-filling stage (Fig. 2d). While no significant differences were observed in these ratios between CK and O3 9 UVB treatments.

Nematode ecological indices Soil nematode taxonomic diversity indices were sensitive to sampling stage and different treatment effects (Table 1). Following elevated O3, nematode diversity index decreased and dominance index increased in relative to the CK at pod-filling stage (Table 3). In addition, elevated O3 and UV-B radiation significantly influenced nematode functional diversity (P \ 0.05, Table 1). At pod-bearing stage, the elevated O3 decreased the values of EI in comparison with the CK, and decreased SI in the O3 9 UVB treatment relative to the UV-B treatment (Table 3).

Correlations between soil nematodes and environmental parameters The CCA analysis suggested that soil pH (P \ 0.01) was the most important parameter which contributed to the distribution of soil nematodes, and then was shoot biomass (P \ 0.01), elevated UV-B (P = 0.066) (Fig. 3). The eigenvalues for the first and second axis were 0.044 and 0.015, respectively. The first and second axis explained 73.1 and 24.2 % of the species-environment relations, respectively; and the two axes accounted for 97.3 % of the species-environment relations.

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Fig. 1 Abundance of total nematode (a, b) and nematode trophic groups [bacterivores (c, d); fungivores (e, f); plantparasites (g, h); omnivore– carnivores (i, j)] at pod-bearing and pod-filling stages of soybean, respectively, under elevated O3 and UV-B radiation conditions (bars represent the standard error). Bars with the different letters present the differences separated by LSD tests, and ns indicates nonsignificant (P [ 0.05)

Discussion Understanding the response of soil nematode diversity to elevated O3 and UV-B radiation is essential for establishing sustainable agroecosystem in a threatening environment.

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Our results indicated that elevated O3 and UV-B radiation had impact not only on the plant growth, but also on the soil nematode community structure and functional diversity. Undeniably, there were pseudo-replication issues with only two repeatable chambers per treatment. However, it

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Fig. 2 Ratio of nematode trophic groups ((BF ? FF)/PP (a, b); OP/PP (c, d)) at podbearing and pod-filling stages of soybean, respectively, under elevated O3 and UV-B radiation conditions (bars represent the standard error); See Table 1 and Fig. 1 for abbreviations

Table 3 Nematode ecological indices at pod-bearing and pod-filling stages of soybean under elevated O3 and UV-B radiation during soybean growing season (mean ± SE) Indices

Growing season

Treatment CK

O3

UVB

O3 9 UVB

Taxonomic diversity k

Pod-bearing

0.28 ± 0.03

0.36 ± 0.04

0.25 ± 0.05

0.39 ± 0.12

H0

Pod-filling Pod-bearing

0.15 ± 0.02b 1.52 ± 0.13

0.26 ± 0.02a 1.39 ± 0.13

0.20 ± 0.01ab 1.75 ± 0.21

0.23 ± 0.02a 1.40 ± 0.29

Pod-filling

2.26 ± 0.13a

1.68 ± 0.09c

2.06 ± 0.07ab

1.80 ± 0.08bc

Pod-bearing

0.77 ± 0.04

0.59 ± 0.04

0.73 ± 0.06

0.63 ± 0.09

Pod-filling

0.80 ± 0.02

0.72 ± 0.03

0.74 ± 0.02

0.73 ± 0.02

J0

Functional diversity CI SI EI

Pod-bearing

14.32 ± 3.27

49.79 ± 4.72

61.11 ± 22.91

60.37 ± 18.85

Pod-filling

47.99 ± 9.93

42.56 ± 13.48

51.52 ± 14.27

49.11 ± 4.65

3.66 ± 3.66c

14.21 ± 5.61bc

71.37 ± 13.24a

36.22 ± 13.28b

Pod-filling

Pod-bearing

51.89 ± 10.12

27.35 ± 13.75

43.81 ± 9.20

19.14 ± 11.89

Pod-bearing

53.30 ± 3.16a

17.93 ± 3.81b

37.58 ± 1.90a

45.01 ± 10.19a

Pod-filling

51.89 ± 3.33

49.20 ± 11.77

36.19 ± 5.36

30.93 ± 3.28

Significant effects (P \ 0.05) were indicated in each row and the same letters suggested non-significant difference in LSD tests k Simpson dominance index, H0 Shannon–Wiener index, J0 evenness index, CI channel index, SI structure index, EI enrichment index

should be certain that changes in plants and soil nematode diversity across the eight chambers in this study were mainly caused by elevated O3 and UV-B radiation, because the eight experimental chambers were located in similar topography and soil nutrient conditions. In this study, significant reduction in root biomass was observed under elevated O3 and UV-B treatments, with the lowest values observed in the O3 9 UVB treatments, which was

consistent with our hypothesis that the interactive effect of O3 and UV-B was more deterioration than individual effect. Our findings were not consistent with those of Tripathi and Agrawal (2013) observed on the linseed, they found that individual effects of elevated O3 and UV-B radiation on the yield and quality parameters of linseed were always higher than their combined effect. These inconsistent observations may be due to the

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Fig. 3 Correspondence analysis between soil nematodes and environmental parameters. SM soil moisture, SBR soil basal respiration, MBC microbial biomass carbon, MBN microbial biomass nitrogen, Root root biomass, Shoot shoot biomass, Root:Shoot ratios of root biomass to shoot biomass, TEM total nematodes, Fu fungivores, Ba bacterivores, H plantparasites, Om ? Ca omnivore–carnivores, O3 and UVB treatment effect

species-specific responses and the differences in experimental durations. Responses of belowground subsystems to elevated O3 and UV-B radiation may result from complex interactions among plants, soil microenvironment and soil microorganisms (Ballare´ et al. 2011). Alteration in C flux to soil may influence soil biota indirectly through changes in plant growth and soil conditions (Andersen 2003). The CCA analysis suggested that soil pH, shoot biomass and microbial biomass C and N were relevant parameters that influenced soil nematode distribution. Rinnan et al. (2013) also found that the effects of elevated O3 and UV-B were limited on the carbon cycle due to environmental conditions, such as temperature, water level and photosynthetically active radiation. UV-B radiation may exert an influence on the ecosystem respiration quotient Q10 through inducing decrease in the stomatal conductance of plant leaves (Jansen and van den Noort 2000) and slowing down the plant activity (Julkunen-Tiitto et al. 2005). Zeuthan et al. (1997) in the chambers found that beech trees showed higher net photosynthesis, and delayed senescence relative to the control, which may due to a more protected environment and altered conditions inside the chambers. Chen et al. (2011) also observed that supplemental UV-B radiation may increase the temperature in the OTC during the late stage of plant growth and could change microbial activity and microbial biomass. These changes may in turn influence soil nematode community.

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Although an additive effect was observed in the belowground biomass, the responses of nematode communities were not consistent with those of plant growth. The interactive effects of elevated O3 and UV-B radiation were less than additive in the abundance of bacterivores, and UV-B radiation increased the abundance of bacterivores in comparison with the CK. Changes in the abundance and the structure of soil food webs may exert a major effect on soil energy and nutrient flow in belowground subsystems through grazing on primary decomposers, such as microbial community (Niwa et al. 2011). Different nematode trophic groups showed different responses to the elevated O3 and UV-B radiation. The abundances of fungivores and omnivore-predators were lower in the O3 9 UVB treatment relative to the CK at pod-filling stage. Tropospheric O3 and UV-B radiation cause direct physiological changes in plants include reduced photosynthesis, stomatal conductance and leaf lifespan (Biswas et al. 2008). This can lead to a decrease in the availability of photosynthate exporting to the roots (Andersen 2003). Responses of plants to environmental changes could affect the bacterivores or fungivores indirectly through altered inputs of root exudates and crop residues (Wardle et al. 2004). Relatively lower shoot and root biomasses may help to explain the lower abundance of ominivore-carnivores under elevated O3 treatments. Since the omnivore–carnivores belonging to the K strategists, which are sensitive to the disturbance and at relatively higher trophic levels in the soil food web (Bongers and Ferris 1999), changes in their abundance might trigger topdown effects on the soil food web (Niklaus et al. 2003). In addition, the abundances of bacterivores decreased and plant parasites increased with the supplemental UV-B in comparison with the control at pod-bearing stage. In a UVB-exclusion experiment in a Sphagnum peatland nearambient UV-B negatively affected the numbers of rotifers, nematodes and mites but positively influenced testate amoebae (Robson et al. 2005). UV-induced changes in crop growth and in the microenvironment might be induced these different treatment effects (Kotilainen et al. 2009). Understanding the effects of ozone and UV-B radiation on belowground processes is complicated due to the trophic complexity associated with soil food webs and our limited knowledge about the processes controlling resource acquisition and use in both individual plants and in ecosystems (Andersen 2003). Our results indicated that elevated O3 and UV-B radiation had impact not only on the plant itself, but also on the soil food web. Both community structure and functional diversity of soil nematodes were affected. The ratio of microbivorous nematodes to plant-parasites indicated the ratio of beneficial to harmful nematodes in the soil food web (Neher and Darby 2006), which increased following

Interactive effects of elevated ozone

the elevated O3. Changes in these ratios suggested that the nematode community, being more beneficial for plant growth in O3 treatment, shifted towards being more harmful for the plant in the O3 9 UVB treatment. This was primarily due to changes in the composition and structure of soil food web resulting from the alterations in their food resources. On the other hand, the ratio of omnivore-predators to plant-parasites suggested that the complexity of soil food web may decrease following the elevated O3. Haddad et al. (2009) assumed that lower predator densities may be able to increase herbivore infestation and then influence the primary productivity. Nematode taxonomic diversity showed response to the elevated O3, where diversity decreased and dominance increased following the elevated O3 at pod-bearing stage, which was consistent with our previous findings (Li et al. 2012). Changes in nematode diversity under O3 elevation may due to the decreasing supply of resources. The effects of elevated O3 and UV-B radiation influenced nematode functional diversity at pod-bearing stage. Elevated O3 decreased SI and increased EI in the O3 9 UVB treatment relative to the UV-B treatment, but increased SI and decreased EI in the O3 treatment in comparison with the CK. Higher enrichment index and lower structure index in O3 9 UVB treatment suggested a stressed soil condition and degraded soil food web under the effects of elevated O3 and UV-B radiation. In addition, these negative effects of elevated O3 on soil food web may be weakened by the UV-B radiations. It has been reported that the increase in O3 concentration may increase the thickness of leaves, and reduced the further penetration of UV-B into the plants (Ljubesˇic´ and Britvec 2006). Similarly, Tripathi and Agrawal (2013) also reported that the supplemental UV-B radiation was partially successful in changing the deleterious response of yield and quality of seeds when they were applied together. In conclusion, elevated O3 and UV-B radiation have impact not only on the plant growth, but also on the nematode taxonomic and functional diversity. Elevated O3 led to a higher enrichment index and lower structure index in the treatments with elevated O3 and UV-B radiation suggesting a degraded soil food web due to the stressed soil condition. The negative effects of elevated O3 on nematode community structure may be weakened by the UV-B radiations. Acknowledgments This research was supported by the National Natural Science Foundation of China (Nos. 31270487, 41101242 and 41101232). Conflict of interest The authors declare that they have no conflict of interests with this research. Declaration The experiments comply with the current laws of the country in which they were performed.

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Interactive effects of elevated ozone and UV-B radiation on soil nematode diversity.

Ultraviolet-B (UV-B) radiation and elevated tropospheric ozone may cause reductions in the productivity and quality of important agricultural crops. H...
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