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Impacts of Nighttime Warming on the Soil Nematode Community in a Winter Wheat Field of Yangtze Delta Plain, China
Journal of Integrative Agriculture 2014, 13(7): 1477-1485
July 2014
RESEARCH ARTICLE
Impacts of Nighttime Warming on the Soil Nematode Community in a Winter Wheat Field of Yangtze Delta Plain, China SONG Zhen-wei1, ZHANG Bin2, TIAN Yun-lu3, DENG Ai-xing1, ZHENG Cheng-yan1, Md Nurul Islam4, Md Abdul Mannaf4 and ZHANG Wei-jian1 1
Institute of Crop Sciences, Chinese Academy of Agricultural Sciences/Key Laboratory of Crop Physiology, Ecology & Production, Ministry of Agriculture, Beijing 100081, P.R.China 2 Institute of Rice Sciences, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, P.R.China 3 College of Agriculture, Nanjing Agricultural University, Nanjing 210095, P.R.China 4 Bangladesh Agricultural Research Institute, Joydebpur Gazipur-1701, Bangladesh
Abstract Changes in the soil nematode community induced by global warming may have a considerable influence on agro-ecosystem functioning. However, the impacts of predicted warming on nematode community in farmland (e.g., winter wheat field) have not been well documented. Therefore, a field experiment with free air temperature increase (FATI) was conducted to investigate the responses of the soil nematode community to nighttime warming in a winter wheat field of Yangtze Delta Plain, China, during 2007 to 2009. Nighttime warming (NW) by 1.8°C at 5-cm soil depth had no significant impact on the total nematode abundance compared to un-warmed control (CK). However, NW significantly affected the nematode community structure. Warming favored the bacterivores and fungivores, such as Acrobeles, Monhystera, Rhabditis, and Rhabdontolaimus in bacterivores, and Filenchus in fungivores, while the plant-parasites were hindered, such as Helicotylenchus and Psilenchus. Interestingly, the carnivores/ omnivores remained almost unchanged. Hence, the abundances of bacterivores and fungivores were significantly higher under NW than those under CK. Similarly, the abundances of plant-parasites were significantly lower under NW than under CK. Furthermore, Wasilewska index of the nematode community was significantly higher under NW than those under CK, indicating beneficial effect to the plant in the soil. Our results suggest that nighttime warming may improve soil fertility and decrease soilborne diseases in winter wheat field through affecting the soil nematode community. It is also indicated that nighttime warming may promote the sustainability of the nematode community by altering genera-specific habitat suitability for soil biota. Key words: climate warming, FATI, soil nematodes, community structure,winter wheat
INTRODUCTION Global warming has taken place with an increase of mean surface air temperature by 0.74°C for the past 100 years, and the temperature will further increase at
the rate of 1.1-6.4°C by the end of this century (IPCC 2007). Furthermore, the increased level of the daily minimum temperature was higher than that of the daily maximum temperature, and the increasing trend of the former is expected higher than the latter (Easterling et al. 1997; IPCC 2001; Lobell et al. 2011). Nematodes are the key agents of soil processes, such as organic matter
Received 6 September, 2013 Accepted 29 November, 2013 SONG Zhen-wei, Tel: +86-10-62128815, E-mail: [email protected]; Correspondence ZHANG Wei-jian, Tel: +86-10-62156856, Fax: +86-62128815, E-mail: [email protected]
© 2014, CAAS. All rights reserved. Published by Elsevier Ltd. doi: 10.1016/S2095-3119(14)60807-8
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decomposition, mineralization, nutrient cycling and soil-borne diseases (Meagher 1977; Bongers and Ferris 1999; Liang et al. 2009). Warming-led alterations of the nematode abundance and its community structure may have a considerable influence on soil ecosystem functioning (Bakonyi et al. 2007). Temperature change has been evidenced as an important factor determining nematode abundance under many conditions, such as Antarctic (Simmons et al. 2009), subarctic (Ruess et al. 1999), Alpine summit (Hoschitz and Kaufmann 2004), semiarid (Bakonyi et al. 2007; Li et al. 2013), and arid regions (Pen-Mouratov et al. 2004). Many studies have shown that higher temperature might increase nematode abundances, however, some studies reported that warming impacts could be different and even negative due to the particular conditions of latitude, soil properties and microhabitat types (Bakonyi et al. 2007). Meanwhile, warming may also affect soil nematode community structure. For example, an increase of soil temperature by 1-2°C could significantly decrease soil nematode species diversity, resulting in great changes in nematode trophic structure and species dominance in subarctic soils (Ruess et al. 1999). Bakonyi et al. (2007) observed that nematode community diversity and multivariate structure were more sensitive to changes in soil temperature than soil moisture in a temperate semiarid shrub land. However, Li et al. (2013) found that warming influenced the nematode community diversity less than N addition in a temperate steppe. As we know, most of existing observations about warming impacts on soil nematodes were conducted in natural soils. Moreover, previous studies related to warming impacts were mostly performed at a plant or plant community scale under controlled conditions, rather than at an ecosystem scale in situ (Okada and Ferris 2001; Aronson and McNulty 2009). The impacts of warming on soil nematode abundance and community structure in agro-ecosystem have not been well documented so far. Winter wheat (Triticum aestivum L.) is one of the most important crops in China, and more than 70% of Chinese winter wheat is sown in the eastern areas (Tian et al. 2012). Yangtze Delta Plain is one of the major regions of Chinese winter wheat cropping. Meanwhile, air temperature, especially daily minimum air temperature of
winter wheat growing season has significantly increased over the past decades, and will further increase till 2050 in this area (Chavas et al. 2009; Dong et al. 2011). Thus, to learn about warming impacts on the winter wheat cropping system will greatly facilitate the development of strategies leading to future crop production in China. Many efforts have been made to evaluate the effects of warming on wheat growth and production in this region (Tian et al. 2011, 2012; Zhang et al. 2013), whereas few studies focused on the responses of soil nematode. We, therefore, conducted a field experiment with a facility of free air temperature increase (FATI) in Nanjing, Jiangsu Province, during 2007 to 2009. Our objectives were to investigate the impacts of daily minimum air temperature increase (i.e., nighttime warming) on soil nematode abundance and community structure in a winter wheat field.
RESULTS Total nematode abundance Soil nematode abundance in the 0-20 cm depth showed a decreasing trend with time from wheat booting stage to the maturity stage for the warmed (NW) and un-warmed plots (CK) (Fig. 1). Generally, the nematode abundance reached its highest values at the booting stage except that the highest value under NW occurred at the heading stage in 2008. The average nematode abundance over the sampling time under CK and NW was 257.7 and 251.0 individuals (ind.) per 100 g dry soil in 2008, and 264.6 and 268.3 ind. per 100 g dry soil in 2009, respectively. No significant difference was found in the nematode abundance between the NW and CK plots during the experimental duration. There were similar vertical distribution patterns of nematode abundance between the treatments, with a decreasing trend along with the increase in the soil depth (Fig. 2). Average nematode abundance in 0-5 cm depth in 2008 and 2009 was 371.8 ind. per 100 g dry soil under the CK and 370.2 ind. per 100 g dry soil under the NW, while the corresponding values in 15-20 cm depth were 158.3 and 145.0 ind. per 100 g dry soil. However, no significant differences occurred in nematode abundance in each soil depth between the treatments.
© 2014, CAAS. All rights reserved. Published by Elsevier Ltd.
Impacts of Nighttime Warming on the Soil Nematode Community in a Winter Wheat Field of Yangtze Delta Plain, China CK
NW
2007-2008
Total nematodes 100 g-1 dyr soil
Total nematodes 100 g-1 dyr soil
500 400 300 200 100 0 Booting
Heading
Filling
1479
Maturity
500
2008-2009
400 300 200 100 0 Booting
Heading
Filling
Maturity
Growing stage
Growing stage
Fig. 1 Temporal dynamics of total soil nematodes in 0-20 cm soil depth during winter wheat growing season. CK, un-warmed control; NW, nighttime warming. Values are the means±SE. The same as below.
CK
NW
2007-2008 Total nematodes 100 g-1 dry soil 100
200
300
400
Soil depth (cm)
0-5
a
a a
10-15
a
0
a
a a
5-10
15-20
500
a
100
200
300
400
5-10
a
a
a
a a
10-15 15-20
500 a
0-5 Soil depth (cm)
0
2008-2009 Total nematodes 100 g-1 dry soil
a a
Fig. 2 Vertical distribution of soil nematodes in 0-20 cm soil depth during winter wheat growing season. Means are the averages of total nematodes of four sampling times in each year. Within the same soil depth, means followed by the same letter do not differ significantly (P>0.05). The same as below.
Nematode composition Table 1 shows the data of 32 nematode genera in the experimental field under different treatments, which included 11 genera of bacterivores, 11 genera of plant-parasites, 7 genera of carnivores/omnivores and 3 genera of fungivores. The nematode genera of Mesorhabditis, Placodera, Rhabdontolaimus in bacterivores, and Helicotylenchus, Psilenchus in plant-parasites were most abundant under all treatments of which abundance was higher than 5%. Nighttime warming effects were also found at genus level in case of Acrobeles, Cephalobus, Monhystera, Rhabditis, Rhabdontolaimus in bacterivores, Helicotylenchus, Hoplotylus, Psilenchus in plant-parasites, and Filenchus in fungivores. Nighttime warming
significantly increased the abundances of Acrobeles, Filenchus, Monhystera, Rhabditis, Rhabdontolaimus and Hoplotylus, whereas significantly decreased the abundances of Cephalobus, Helicotylenchus and Psilenchus compared to the CK.
Nematode trophic group Bacterivores and plant-parasites were the dominant trophic groups in 0-20 cm depth, which accounted for 41.9 and 38.2% under the CK, and 45.8 and 32.0% under the NW of total nematode population, respectively (Fig. 3 and Table 1). Significant differences were found in the nematode trophic group composition between the NW and the CK. Nighttime warming significantly favored the bacterivores and fungivores population whereas it
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Table 1 Genus abundances of soil nematodes under different treatments Guild1)
Acrobeles Acrobeloides Cephalobus Mesorhabditis Monhystera Panagrolaimus Pelodera Placodira Rhabditis Rhabdontolaimus Wilsonena
Ba2 Ba2 Ba2 Ba1 Ba2 Ba1 Ba1 Ba2 Ba1 Ba3 Ba2
Helicotylenchus Heterodera Hoplotylus Longidorus Malenchus Paratylenchus Pratylenchus Psilenchus Trichodorus Tylenchorhynchus Tylenchus
H3 H3 H3 H5 H2 H2 H3 H2 H4 H3 H2
Aporcelaimus Dorylaimus Eduorylaimus Labronema Mesodorylaimus Mononchus Pungentus
Om5 Om4 Om4 Om4 Om5 Ca4 Om4
Aphelenchoides Aphelenchus Filenchus
Fu2 Fu2 Fu2
Plant-parasites
Carnivores/Omnivores
Fungivores
Genus abundance (%)2) CK NW 41.9±1.2 b 45.8±1.51 a 0.9±0.27 b 1.8±0.11 a 1.6±0.33 a 1.0±0.25 a 2.9±0.26 a 2.0±0.22 b 5.0±0.78 a 5.2±0.64 a 3.1±0.30 b 4.1±0.21 a 2.6±0.33 a 2.7±0.33 a 0.9±0.34 a 1.1±0.37 a 13.0±1.06 a 13.0±1.01 a 3.4±0.22 b 4.2±0.33 a 8.2±0.44 b 10.4±0.52 a 0.3±0.15 a 0.2±0.04 a 38.2±1.35 a 32.0±2.11 b 20.5±0.55 a 14.8±1.07 b 0.8±0.05 a 0.7±0.05 a 0.8±0.17 b 1.3±0.18 a 2.0±0.34 a 2.1±0.19 a 1.0±0.15 a 1.2±0.14 a 2.5±0.13 a 2.5±0.13 a 0.4±0.13 a 0.6±0.15 a 8.2±0.23 a 6.0±0.31 b 0.3±0.11 a 0.3±0.04 a 0.9±0.19 a 1.2±0.13 a 1.0±0.24 a 1.4±0.11 a 15.4±0.78 a 15.7±0.33 a 0.8±0.13 a 0.7±0.08 a 2.8±0.21 a 2.0±0.15 b 0.6±0.09 b 0.9±0.35 a 1.2±0.19 a 1.1±0.13 a 4.0±0.11 a 4.0±0.21 a 2.2±0.07 a 2.2±0.07 a 3.7±0.27 b 4.8±0.70 a 4.5±0.33 b 6.5±0.28 a 1.5±0.17 a 1.6±0.12 a 0.8±0.16 a 1.2±0.20 a 2.2±0.38 b 3.7±0.43 a
1)
Ba, bacterivores; H, plant-parasites; Ca/Om, carnivores/omnivores; Fu, fungivores. Values are trophic group plus colonizer-persister (c-p) value. 2) CK, un-warmed control; NW, nighttime warming. Values are the means±SE. Means followed by the same letter do not differ significantly (P>0.05). The
Total nematodes 100 g-1 dry soil
Bacterivores
Genus
2007-2008
160 120
NW
a a
b
b
80
a a
40
b a
0
Ba
H
Ca/Om
Fu
Trophic groups
Total nematodes 100 g-1 dry soil
Trophic groups
CK
2008-2009
160 120
b
a a
b
80 a a
40 0
b a Ba
H
Ca/Om
Fu
Trophic groups
Fig. 3 Trophic group composition of soil nematodes in 0-20 cm soil depth during winter wheat growing season. Ba, bacterivores; H, plantparasites; Ca/Om, carnivores/omnivores; Fu, fungivores. Table 2 Ecological indices of soil nematode community under different treatments Ecological index Shannon-Wiener index (H´) Genus dominance index (λ) Pielou’s evenness index (J) Enrichment index (EI) Structural index (SI) Wasilewska index (WI)
CK 1.16±0.02 a 0.35±0.01 a 0.83±0.01 a 66.05±1.17 a 22.57±1.28 a 1.21±0.02 b
NW 1.19±0.02 a 0.34±0.01 a 0.86±0.02 a 66.55±0.15 a 24.40±3.06 a 1.64±0.14 a
same as below.
hindered the plant-parasites population as compared with the CK. However, there was no significant difference in the carnivores/omnivores population between the treatments.
Nematode ecological indices Ecological indices of soil nematode community are shown in Table 2. Nighttime warming significantly increased the Wasilewska index (WI) of nematode community by 35.5% compared to the CK. Though enrichment index (EI), Shannon-Wiener index (H´), Pielou’s
evenness index (J), and structural index (SI) were higher in the NW than that in the CK, no significant difference was found between the treatments. Furthermore, nighttime warming decreased the genus dominance index (λ) but not significantly compared to the CK. Nematode faunal analysis indicated that both the CK and NW plots belonged to the A quadrants (Fig. 4), which indicated the soil food webs were disturbed.
DISCUSSION In the present study, the increase of soil temperature at 5 cm depth by 1.8°C didn’t significantly affect the
© 2014, CAAS. All rights reserved. Published by Elsevier Ltd.
Impacts of Nighttime Warming on the Soil Nematode Community in a Winter Wheat Field of Yangtze Delta Plain, China CK 2007-2008
50
0
0
A
B
D
C
50 Structure index (SI)
NW 2008-2009
100
Enrichment index (EI)
Enrichment index (EI)
100
100
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50
0
0
A
B
D
C
50 Structure index (SI)
100
Fig. 4 Nematode faunal analysis in 0-20 cm soil depth during winter wheat growing season.
nematode abundance compared to un-warming control neither during the growing season of winter wheat nor at different soil depthes. Ruess et al. (1999) observed that warming effects on nematode population were larger on high altitude sites where they were mostly exposed to naturally occurring climatic stresses such as low temperatures, high wind-speed, and moisture limitations. Our experimental site was located in subtropical monsoon climatic zone without temperature and soil moisture stresses, therefore, the warming effects on nematode abundance were not as great as that in high latitude areas. The other reason for unchanged nematode abundance under nighttime warming can be attributed to the ebb and flow of the different nematode genera (Bakonyi et al. 2007). It was evidenced that compared to those under the ambient condition, the abundances of Acrobeles, Filenchus, Monhystera, Rhabditis, Rhabdontolaimus and Hoplotylus were significantly higher, whereas the abundances of Cephalobus, Helicotylenchus and Psilenchus were significantly lower under warming condition in this study. Hence, the tradeoff among the nematode genera partially maintains the stable population size under warming. This may be due to different reactions of nematode genera to soil temperature (McSorley 2003; Treonis and Wall 2005). For example, Sohlenius and Boström (1999) demonstrated that Rhabditis was sensitive to cold, and Papatheodorou et al. (2004) found that Aceobeles increased in warm plots. On the other hand, though nighttime warming had no significant effect on total nematode population, it
influenced the composition of nematode trophic groups which is related to soil processing, for example, organic matter decomposition, mineralization and nutrient cycling. In our study, higher bacterivores population was observed in the NW and higher plant-parasites population in the CK. Bacterivores are closely related to food web accompanying organic matter decomposition and nutrient cycling, and they could be the potential indicators of soil fertility (Pan et al. 2010). Nighttime warming increased the abundance of bacterivores which might be due to higher microbial population and activities caused by warming (Papatheodorou et al. 2004). Furthermore, higher soil microbial activities can increase soil C sequestration and nutrient fixing (Kanchikerimath and Singh 2001). Therefore, it may suggest that higher abundance of bacterivores reflects the high soil fertility of a winter wheat field under warming condition. Plant-parasites are related to soil-borne diseases in a winter-wheat field (Meagher 1977). Seven genera of plant-parasites, Pratylenchus, Helicotylenchus, Heterodera, Tylenchorhynchus, Xiphinema, and Ditylenchus were found associated with cereal crops (Abdollahi 2010). In our study, nighttime warming decreased the abundance of plant-parasites due to significantly lower abundance of Helicotylenchu. This result may suggest that nighttime warming could reduce the risks of soil-borne disease infection, and consequently reduce the grain yield loss. The ecological indices of H´, λ and J are often used to assess the nematode diversity conditions (Pan et al. 2010). In the present study, no significant differences
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were observed between the treatments considering H´, λ and J, which implies that nighttime warming has no effects on the nematode diversity. This result was consistent with previous findings that temperature did not affect several parameters, such as total nematode population and species diversity, but insignificantly affected the nematode abundance of different genera (Bakonyi et al. 2007). Moreover, EI and SI are often used to assess the nematode community structure and indicate the dynamics of soil food webs (Ferris et al. 2001; Li et al. 2010). Our study showed that no significant differences in EI and SI were observed between the treatments, indicating that nighttime warming has no significant effects on soil food webs. It was also confirmed by the nematode faunal analysis that both the CK and NW belonged to the A quadrants with disturbed soil food webs (Ferries et al. 2001; Li et al. 2010). Furthermore, WI can demonstrate the proportion of free nematodes and plant-parasites and reflect the health of plants in the soil (Wasilewska 1994). In this study, WI was significantly higher under the NW compared to the CK due to higher abundance of bacterivores and fungivores, which suggests that nighttime warming may benefit to the plant health and soil environmental sustainability (Chen et al. 2009).
CONCLUSION In this study, an increase of nighttime temperature at 5 cm soil depth by 1.8°C had no significant effects on nematode abundance neither during the growing season of winter wheat nor at different soil layers. Moreover, nighttime warming significantly increased the abundances of Acrobeles, Monhystera, Rhabditis, Rhabdontolaimus and Hoplotylus in bacterivores, and Filenchus in fungivores, and decreased the abundances of Psilenchus and Helicotylenchus in plant-parasites. No significant warming impacts were found in the abundances of carnivores/omnivores. Hence, nighttime warming favored the bacterivores and fungivores while it hindered the plant-parasites in winter wheat field soil. Our results suggest that nighttime warming may improve the soil fertility, maintain soil environmental sustainability, and reduce soil-borne disease infection risk for winter wheat growth through altering soil nematode community.
MATERIALS AND METHODS Experimental site description The experimental site was located at the Experimental Station of Jiangsu Academy of Agricultural Sciences, Nanjing, Jiangsu Province, China (32°02´N, 118°52´E, 11 m a.s.l.). This location belongs to the climatic zone of subtropical monsoon climate. The mean air temperature, the annual precipitation, the sunshine hours and the frost-free days are 16.7°C, 1 050 mm, 1 900 h and 237 d, respectively. The soil at the experimental site is brunisolic silt loam soil (Alfisols in USAST) with 0.5% sand, 75.3% silt and 24.2% clay, respectively. The nutrient conditions were as follows: soil contains 8.2 g kg-1 organic C, 2.6 g kg-1 total N, 0.6 g kg-1 total P, 14.0 g kg-1 total K, 166.2 mg kg-1 available P, and 165.0 mg kg-1 available K. The cropping pattern is a double cropping system of annually winter wheat-rice cropping.
Experimental design and management The field experiment was started in winter 2007 and continued up to summer 2009, including two treatments: nighttime warming (NW) and un-warmed control (CK). The field was laid out in a randomized block design with three replicates. The plot size was 30 m2 (6 m×5 m). The field warming system was constructed according to the design of free air temperature increase (FATI) facility located at the Great Plain Apiaries, USA (Wan et al. 2002). In each warmed plot, a single 180 cm × 20 cm infrared heater (Jiangsu Tiande Special Light Source Co., Ltd., China) was suspended 1.5 m above the ground, which provided with continuous warming from 18:00 to 6:00. In the un-warmed plot, a ‘dummy’ heater of the same shape and size was suspended at the same height to simulate the shading effects of the heater. The distance between the adjacent plots was about 5 m to avoid heating contamination between plots. This FATI facility could provide 2 m×2 m sampling areas with uniform and reliable warming effects. The FAIT facility could significantly increase the mean soil temperature at 5 cm depth by 1.8°C. The same soil water content in 0-20 cm depth was maintained in both the treatments during the entire growth period of wheat (Tian et al. 2010). The winter wheat cultivar Yangmai 11 was manually sown on 15 November, 2007, and 2 November, 2008 at a density of 225 plants m-2 with a row spacing of 20 cm and were harvested on 2 Jun,e 2008 and 24 May, 2009, respectively. In accordance with local agronomic practices, the fertilizer applications of N, P and K in each plot were 225, 75 and 75 kg ha-1, respectively. The total P and K and 50% N were applied 2 days prior to sowing as basal dressing. The other 10% N was applied as side dressing at early tillering stage at the beginning of March, and 40% at the spike initiation stage at the beginning of April. The
© 2014, CAAS. All rights reserved. Published by Elsevier Ltd.
Impacts of Nighttime Warming on the Soil Nematode Community in a Winter Wheat Field of Yangtze Delta Plain, China
precipitations were 396.9 mm in 2007-2008 growing season and 354.1 mm in 2008-2009 growing season, thus, no irrigation was applied during the entire growth period of winter wheat.
Soil sampling For temporal nematode population measurements, soil samples were collected at four key growth stages of winter wheat viz., booting stage (28 March, 2008 and 16 March, 2009 ), heading stage (27 April, 2008 and 9 April, 2009), grain filling stage (13 May, 2008 and 4 May, 2009) and maturity stage (30 May, 2008 and 24 May, 2009). Each soil sample was collected from six randomly selected sampling points at 5 cm intervals from 0 to 20 cm depth. Six sub-samples for each soil depth class were blended to get one composite sample for each depth class per plot. Each soil sample was passed through a 6-mm-mesh soil sieve to remove the plant leaves and roots, and large stones. All samples were stored in a refrigerator at 4°C until subsequent analysis.
Nematode extraction and identification Sucrose solution-elutriation-centrifugation method was used to extract soil nematodes from about 100 g fresh soil (Bulluck et al. 2002). Then the nematodes were heat-killed by immersion in 65°C water for 2 min and preserved in triethanolamine formaldehyde (TAF) solution (Shepherd, 1970). Total nematodes in each sample were counted under an anatomical lens (40×). For each sample, 100 nematodes were randomly selected to identify the genera, trophic groups, and colonizer-persister (c-p) value with the aid of an optical microscope (Yeates et al. 1993; Bongers 1994; Yin 1998; Okada and Harada 2007; Li et al. 2012). In the present study, the nematodes were classified as four trophic groups characterized by feeding habits, bacterivores (Ba), plantparasites (H), carnivores/omnivores (Ca/Om), and fungivores (Fu). Soil moisture was determined by oven-drying samples at 105°C. The density of total and different trophic-group nematodes were adjusted to the number per 100 g dry soil. The nematode abundance for each genus was the percentage of specific genus in total nematodes. Nematode community structure was characterized by Shannon-Wiener index (H´) (Shannon and Weaver 1949), Pielou’s evenness index (J) (Kennedy and Smith 1995), genus dominance index (λ) (Bongers 1990), enrichment index (EI), structure index (SI) (Ferris et al. 1997), and Wasilewska index (WI) (Yeates 2003).
Statistical analysis The analysis of variances for soil nematode population
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density, abundance and community structure were performed independently using the procedure of SPSS 13.0 (SPSS Inc, Chicago, IL, USA). Least significant differences (LSD) at P<0.05 were used to detect significant differences among means (Steel and Torrie 1980).
Acknowledgements
This research was supported by the National Basic Research Program of China (2010CB951501), the Key Technologies R&D Program of China during the 12th Five-Year Plan period (2011BAD16B14), the National Natural Science Foundation of China (30771278) and the Innovation Program of Chinese Academy of Agricultural Sciences, China.
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Impacts of Nighttime Warming on the Soil Nematode Community in a Winter Wheat Field of Yangtze Delta Plain, China
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July 2014
RESEARCH ARTICLE
Impacts of Nighttime Warming on the Soil Nematode Community in a Winter Wheat Field of Yangtze Delta Plain, China SONG Zhen-wei1, ZHANG Bin2, TIAN Yun-lu3, DENG Ai-xing1, ZHENG Cheng-yan1, Md Nurul Islam4, Md Abdul Mannaf4 and ZHANG Wei-jian1 1
Institute of Crop Sciences, Chinese Academy of Agricultural Sciences/Key Laboratory of Crop Physiology, Ecology & Production, Ministry of Agriculture, Beijing 100081, P.R.China 2 Institute of Rice Sciences, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, P.R.China 3 College of Agriculture, Nanjing Agricultural University, Nanjing 210095, P.R.China 4 Bangladesh Agricultural Research Institute, Joydebpur Gazipur-1701, Bangladesh
Abstract Changes in the soil nematode community induced by global warming may have a considerable influence on agro-ecosystem functioning. However, the impacts of predicted warming on nematode community in farmland (e.g., winter wheat field) have not been well documented. Therefore, a field experiment with free air temperature increase (FATI) was conducted to investigate the responses of the soil nematode community to nighttime warming in a winter wheat field of Yangtze Delta Plain, China, during 2007 to 2009. Nighttime warming (NW) by 1.8°C at 5-cm soil depth had no significant impact on the total nematode abundance compared to un-warmed control (CK). However, NW significantly affected the nematode community structure. Warming favored the bacterivores and fungivores, such as Acrobeles, Monhystera, Rhabditis, and Rhabdontolaimus in bacterivores, and Filenchus in fungivores, while the plant-parasites were hindered, such as Helicotylenchus and Psilenchus. Interestingly, the carnivores/ omnivores remained almost unchanged. Hence, the abundances of bacterivores and fungivores were significantly higher under NW than those under CK. Similarly, the abundances of plant-parasites were significantly lower under NW than under CK. Furthermore, Wasilewska index of the nematode community was significantly higher under NW than those under CK, indicating beneficial effect to the plant in the soil. Our results suggest that nighttime warming may improve soil fertility and decrease soilborne diseases in winter wheat field through affecting the soil nematode community. It is also indicated that nighttime warming may promote the sustainability of the nematode community by altering genera-specific habitat suitability for soil biota. Key words: climate warming, FATI, soil nematodes, community structure,winter wheat
INTRODUCTION Global warming has taken place with an increase of mean surface air temperature by 0.74°C for the past 100 years, and the temperature will further increase at
the rate of 1.1-6.4°C by the end of this century (IPCC 2007). Furthermore, the increased level of the daily minimum temperature was higher than that of the daily maximum temperature, and the increasing trend of the former is expected higher than the latter (Easterling et al. 1997; IPCC 2001; Lobell et al. 2011). Nematodes are the key agents of soil processes, such as organic matter
Received 6 September, 2013 Accepted 29 November, 2013 SONG Zhen-wei, Tel: +86-10-62128815, E-mail: [email protected]; Correspondence ZHANG Wei-jian, Tel: +86-10-62156856, Fax: +86-62128815, E-mail: [email protected]
© 2014, CAAS. All rights reserved. Published by Elsevier Ltd. doi: 10.1016/S2095-3119(14)60807-8
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decomposition, mineralization, nutrient cycling and soil-borne diseases (Meagher 1977; Bongers and Ferris 1999; Liang et al. 2009). Warming-led alterations of the nematode abundance and its community structure may have a considerable influence on soil ecosystem functioning (Bakonyi et al. 2007). Temperature change has been evidenced as an important factor determining nematode abundance under many conditions, such as Antarctic (Simmons et al. 2009), subarctic (Ruess et al. 1999), Alpine summit (Hoschitz and Kaufmann 2004), semiarid (Bakonyi et al. 2007; Li et al. 2013), and arid regions (Pen-Mouratov et al. 2004). Many studies have shown that higher temperature might increase nematode abundances, however, some studies reported that warming impacts could be different and even negative due to the particular conditions of latitude, soil properties and microhabitat types (Bakonyi et al. 2007). Meanwhile, warming may also affect soil nematode community structure. For example, an increase of soil temperature by 1-2°C could significantly decrease soil nematode species diversity, resulting in great changes in nematode trophic structure and species dominance in subarctic soils (Ruess et al. 1999). Bakonyi et al. (2007) observed that nematode community diversity and multivariate structure were more sensitive to changes in soil temperature than soil moisture in a temperate semiarid shrub land. However, Li et al. (2013) found that warming influenced the nematode community diversity less than N addition in a temperate steppe. As we know, most of existing observations about warming impacts on soil nematodes were conducted in natural soils. Moreover, previous studies related to warming impacts were mostly performed at a plant or plant community scale under controlled conditions, rather than at an ecosystem scale in situ (Okada and Ferris 2001; Aronson and McNulty 2009). The impacts of warming on soil nematode abundance and community structure in agro-ecosystem have not been well documented so far. Winter wheat (Triticum aestivum L.) is one of the most important crops in China, and more than 70% of Chinese winter wheat is sown in the eastern areas (Tian et al. 2012). Yangtze Delta Plain is one of the major regions of Chinese winter wheat cropping. Meanwhile, air temperature, especially daily minimum air temperature of
winter wheat growing season has significantly increased over the past decades, and will further increase till 2050 in this area (Chavas et al. 2009; Dong et al. 2011). Thus, to learn about warming impacts on the winter wheat cropping system will greatly facilitate the development of strategies leading to future crop production in China. Many efforts have been made to evaluate the effects of warming on wheat growth and production in this region (Tian et al. 2011, 2012; Zhang et al. 2013), whereas few studies focused on the responses of soil nematode. We, therefore, conducted a field experiment with a facility of free air temperature increase (FATI) in Nanjing, Jiangsu Province, during 2007 to 2009. Our objectives were to investigate the impacts of daily minimum air temperature increase (i.e., nighttime warming) on soil nematode abundance and community structure in a winter wheat field.
RESULTS Total nematode abundance Soil nematode abundance in the 0-20 cm depth showed a decreasing trend with time from wheat booting stage to the maturity stage for the warmed (NW) and un-warmed plots (CK) (Fig. 1). Generally, the nematode abundance reached its highest values at the booting stage except that the highest value under NW occurred at the heading stage in 2008. The average nematode abundance over the sampling time under CK and NW was 257.7 and 251.0 individuals (ind.) per 100 g dry soil in 2008, and 264.6 and 268.3 ind. per 100 g dry soil in 2009, respectively. No significant difference was found in the nematode abundance between the NW and CK plots during the experimental duration. There were similar vertical distribution patterns of nematode abundance between the treatments, with a decreasing trend along with the increase in the soil depth (Fig. 2). Average nematode abundance in 0-5 cm depth in 2008 and 2009 was 371.8 ind. per 100 g dry soil under the CK and 370.2 ind. per 100 g dry soil under the NW, while the corresponding values in 15-20 cm depth were 158.3 and 145.0 ind. per 100 g dry soil. However, no significant differences occurred in nematode abundance in each soil depth between the treatments.
© 2014, CAAS. All rights reserved. Published by Elsevier Ltd.
Impacts of Nighttime Warming on the Soil Nematode Community in a Winter Wheat Field of Yangtze Delta Plain, China CK
NW
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Total nematodes 100 g-1 dyr soil
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Heading
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500
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400 300 200 100 0 Booting
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Fig. 1 Temporal dynamics of total soil nematodes in 0-20 cm soil depth during winter wheat growing season. CK, un-warmed control; NW, nighttime warming. Values are the means±SE. The same as below.
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Fig. 2 Vertical distribution of soil nematodes in 0-20 cm soil depth during winter wheat growing season. Means are the averages of total nematodes of four sampling times in each year. Within the same soil depth, means followed by the same letter do not differ significantly (P>0.05). The same as below.
Nematode composition Table 1 shows the data of 32 nematode genera in the experimental field under different treatments, which included 11 genera of bacterivores, 11 genera of plant-parasites, 7 genera of carnivores/omnivores and 3 genera of fungivores. The nematode genera of Mesorhabditis, Placodera, Rhabdontolaimus in bacterivores, and Helicotylenchus, Psilenchus in plant-parasites were most abundant under all treatments of which abundance was higher than 5%. Nighttime warming effects were also found at genus level in case of Acrobeles, Cephalobus, Monhystera, Rhabditis, Rhabdontolaimus in bacterivores, Helicotylenchus, Hoplotylus, Psilenchus in plant-parasites, and Filenchus in fungivores. Nighttime warming
significantly increased the abundances of Acrobeles, Filenchus, Monhystera, Rhabditis, Rhabdontolaimus and Hoplotylus, whereas significantly decreased the abundances of Cephalobus, Helicotylenchus and Psilenchus compared to the CK.
Nematode trophic group Bacterivores and plant-parasites were the dominant trophic groups in 0-20 cm depth, which accounted for 41.9 and 38.2% under the CK, and 45.8 and 32.0% under the NW of total nematode population, respectively (Fig. 3 and Table 1). Significant differences were found in the nematode trophic group composition between the NW and the CK. Nighttime warming significantly favored the bacterivores and fungivores population whereas it
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Table 1 Genus abundances of soil nematodes under different treatments Guild1)
Acrobeles Acrobeloides Cephalobus Mesorhabditis Monhystera Panagrolaimus Pelodera Placodira Rhabditis Rhabdontolaimus Wilsonena
Ba2 Ba2 Ba2 Ba1 Ba2 Ba1 Ba1 Ba2 Ba1 Ba3 Ba2
Helicotylenchus Heterodera Hoplotylus Longidorus Malenchus Paratylenchus Pratylenchus Psilenchus Trichodorus Tylenchorhynchus Tylenchus
H3 H3 H3 H5 H2 H2 H3 H2 H4 H3 H2
Aporcelaimus Dorylaimus Eduorylaimus Labronema Mesodorylaimus Mononchus Pungentus
Om5 Om4 Om4 Om4 Om5 Ca4 Om4
Aphelenchoides Aphelenchus Filenchus
Fu2 Fu2 Fu2
Plant-parasites
Carnivores/Omnivores
Fungivores
Genus abundance (%)2) CK NW 41.9±1.2 b 45.8±1.51 a 0.9±0.27 b 1.8±0.11 a 1.6±0.33 a 1.0±0.25 a 2.9±0.26 a 2.0±0.22 b 5.0±0.78 a 5.2±0.64 a 3.1±0.30 b 4.1±0.21 a 2.6±0.33 a 2.7±0.33 a 0.9±0.34 a 1.1±0.37 a 13.0±1.06 a 13.0±1.01 a 3.4±0.22 b 4.2±0.33 a 8.2±0.44 b 10.4±0.52 a 0.3±0.15 a 0.2±0.04 a 38.2±1.35 a 32.0±2.11 b 20.5±0.55 a 14.8±1.07 b 0.8±0.05 a 0.7±0.05 a 0.8±0.17 b 1.3±0.18 a 2.0±0.34 a 2.1±0.19 a 1.0±0.15 a 1.2±0.14 a 2.5±0.13 a 2.5±0.13 a 0.4±0.13 a 0.6±0.15 a 8.2±0.23 a 6.0±0.31 b 0.3±0.11 a 0.3±0.04 a 0.9±0.19 a 1.2±0.13 a 1.0±0.24 a 1.4±0.11 a 15.4±0.78 a 15.7±0.33 a 0.8±0.13 a 0.7±0.08 a 2.8±0.21 a 2.0±0.15 b 0.6±0.09 b 0.9±0.35 a 1.2±0.19 a 1.1±0.13 a 4.0±0.11 a 4.0±0.21 a 2.2±0.07 a 2.2±0.07 a 3.7±0.27 b 4.8±0.70 a 4.5±0.33 b 6.5±0.28 a 1.5±0.17 a 1.6±0.12 a 0.8±0.16 a 1.2±0.20 a 2.2±0.38 b 3.7±0.43 a
1)
Ba, bacterivores; H, plant-parasites; Ca/Om, carnivores/omnivores; Fu, fungivores. Values are trophic group plus colonizer-persister (c-p) value. 2) CK, un-warmed control; NW, nighttime warming. Values are the means±SE. Means followed by the same letter do not differ significantly (P>0.05). The
Total nematodes 100 g-1 dry soil
Bacterivores
Genus
2007-2008
160 120
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b
b
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2008-2009
160 120
b
a a
b
80 a a
40 0
b a Ba
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Fig. 3 Trophic group composition of soil nematodes in 0-20 cm soil depth during winter wheat growing season. Ba, bacterivores; H, plantparasites; Ca/Om, carnivores/omnivores; Fu, fungivores. Table 2 Ecological indices of soil nematode community under different treatments Ecological index Shannon-Wiener index (H´) Genus dominance index (λ) Pielou’s evenness index (J) Enrichment index (EI) Structural index (SI) Wasilewska index (WI)
CK 1.16±0.02 a 0.35±0.01 a 0.83±0.01 a 66.05±1.17 a 22.57±1.28 a 1.21±0.02 b
NW 1.19±0.02 a 0.34±0.01 a 0.86±0.02 a 66.55±0.15 a 24.40±3.06 a 1.64±0.14 a
same as below.
hindered the plant-parasites population as compared with the CK. However, there was no significant difference in the carnivores/omnivores population between the treatments.
Nematode ecological indices Ecological indices of soil nematode community are shown in Table 2. Nighttime warming significantly increased the Wasilewska index (WI) of nematode community by 35.5% compared to the CK. Though enrichment index (EI), Shannon-Wiener index (H´), Pielou’s
evenness index (J), and structural index (SI) were higher in the NW than that in the CK, no significant difference was found between the treatments. Furthermore, nighttime warming decreased the genus dominance index (λ) but not significantly compared to the CK. Nematode faunal analysis indicated that both the CK and NW plots belonged to the A quadrants (Fig. 4), which indicated the soil food webs were disturbed.
DISCUSSION In the present study, the increase of soil temperature at 5 cm depth by 1.8°C didn’t significantly affect the
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Impacts of Nighttime Warming on the Soil Nematode Community in a Winter Wheat Field of Yangtze Delta Plain, China CK 2007-2008
50
0
0
A
B
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50 Structure index (SI)
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Enrichment index (EI)
Enrichment index (EI)
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100
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0
0
A
B
D
C
50 Structure index (SI)
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Fig. 4 Nematode faunal analysis in 0-20 cm soil depth during winter wheat growing season.
nematode abundance compared to un-warming control neither during the growing season of winter wheat nor at different soil depthes. Ruess et al. (1999) observed that warming effects on nematode population were larger on high altitude sites where they were mostly exposed to naturally occurring climatic stresses such as low temperatures, high wind-speed, and moisture limitations. Our experimental site was located in subtropical monsoon climatic zone without temperature and soil moisture stresses, therefore, the warming effects on nematode abundance were not as great as that in high latitude areas. The other reason for unchanged nematode abundance under nighttime warming can be attributed to the ebb and flow of the different nematode genera (Bakonyi et al. 2007). It was evidenced that compared to those under the ambient condition, the abundances of Acrobeles, Filenchus, Monhystera, Rhabditis, Rhabdontolaimus and Hoplotylus were significantly higher, whereas the abundances of Cephalobus, Helicotylenchus and Psilenchus were significantly lower under warming condition in this study. Hence, the tradeoff among the nematode genera partially maintains the stable population size under warming. This may be due to different reactions of nematode genera to soil temperature (McSorley 2003; Treonis and Wall 2005). For example, Sohlenius and Boström (1999) demonstrated that Rhabditis was sensitive to cold, and Papatheodorou et al. (2004) found that Aceobeles increased in warm plots. On the other hand, though nighttime warming had no significant effect on total nematode population, it
influenced the composition of nematode trophic groups which is related to soil processing, for example, organic matter decomposition, mineralization and nutrient cycling. In our study, higher bacterivores population was observed in the NW and higher plant-parasites population in the CK. Bacterivores are closely related to food web accompanying organic matter decomposition and nutrient cycling, and they could be the potential indicators of soil fertility (Pan et al. 2010). Nighttime warming increased the abundance of bacterivores which might be due to higher microbial population and activities caused by warming (Papatheodorou et al. 2004). Furthermore, higher soil microbial activities can increase soil C sequestration and nutrient fixing (Kanchikerimath and Singh 2001). Therefore, it may suggest that higher abundance of bacterivores reflects the high soil fertility of a winter wheat field under warming condition. Plant-parasites are related to soil-borne diseases in a winter-wheat field (Meagher 1977). Seven genera of plant-parasites, Pratylenchus, Helicotylenchus, Heterodera, Tylenchorhynchus, Xiphinema, and Ditylenchus were found associated with cereal crops (Abdollahi 2010). In our study, nighttime warming decreased the abundance of plant-parasites due to significantly lower abundance of Helicotylenchu. This result may suggest that nighttime warming could reduce the risks of soil-borne disease infection, and consequently reduce the grain yield loss. The ecological indices of H´, λ and J are often used to assess the nematode diversity conditions (Pan et al. 2010). In the present study, no significant differences
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were observed between the treatments considering H´, λ and J, which implies that nighttime warming has no effects on the nematode diversity. This result was consistent with previous findings that temperature did not affect several parameters, such as total nematode population and species diversity, but insignificantly affected the nematode abundance of different genera (Bakonyi et al. 2007). Moreover, EI and SI are often used to assess the nematode community structure and indicate the dynamics of soil food webs (Ferris et al. 2001; Li et al. 2010). Our study showed that no significant differences in EI and SI were observed between the treatments, indicating that nighttime warming has no significant effects on soil food webs. It was also confirmed by the nematode faunal analysis that both the CK and NW belonged to the A quadrants with disturbed soil food webs (Ferries et al. 2001; Li et al. 2010). Furthermore, WI can demonstrate the proportion of free nematodes and plant-parasites and reflect the health of plants in the soil (Wasilewska 1994). In this study, WI was significantly higher under the NW compared to the CK due to higher abundance of bacterivores and fungivores, which suggests that nighttime warming may benefit to the plant health and soil environmental sustainability (Chen et al. 2009).
CONCLUSION In this study, an increase of nighttime temperature at 5 cm soil depth by 1.8°C had no significant effects on nematode abundance neither during the growing season of winter wheat nor at different soil layers. Moreover, nighttime warming significantly increased the abundances of Acrobeles, Monhystera, Rhabditis, Rhabdontolaimus and Hoplotylus in bacterivores, and Filenchus in fungivores, and decreased the abundances of Psilenchus and Helicotylenchus in plant-parasites. No significant warming impacts were found in the abundances of carnivores/omnivores. Hence, nighttime warming favored the bacterivores and fungivores while it hindered the plant-parasites in winter wheat field soil. Our results suggest that nighttime warming may improve the soil fertility, maintain soil environmental sustainability, and reduce soil-borne disease infection risk for winter wheat growth through altering soil nematode community.
MATERIALS AND METHODS Experimental site description The experimental site was located at the Experimental Station of Jiangsu Academy of Agricultural Sciences, Nanjing, Jiangsu Province, China (32°02´N, 118°52´E, 11 m a.s.l.). This location belongs to the climatic zone of subtropical monsoon climate. The mean air temperature, the annual precipitation, the sunshine hours and the frost-free days are 16.7°C, 1 050 mm, 1 900 h and 237 d, respectively. The soil at the experimental site is brunisolic silt loam soil (Alfisols in USAST) with 0.5% sand, 75.3% silt and 24.2% clay, respectively. The nutrient conditions were as follows: soil contains 8.2 g kg-1 organic C, 2.6 g kg-1 total N, 0.6 g kg-1 total P, 14.0 g kg-1 total K, 166.2 mg kg-1 available P, and 165.0 mg kg-1 available K. The cropping pattern is a double cropping system of annually winter wheat-rice cropping.
Experimental design and management The field experiment was started in winter 2007 and continued up to summer 2009, including two treatments: nighttime warming (NW) and un-warmed control (CK). The field was laid out in a randomized block design with three replicates. The plot size was 30 m2 (6 m×5 m). The field warming system was constructed according to the design of free air temperature increase (FATI) facility located at the Great Plain Apiaries, USA (Wan et al. 2002). In each warmed plot, a single 180 cm × 20 cm infrared heater (Jiangsu Tiande Special Light Source Co., Ltd., China) was suspended 1.5 m above the ground, which provided with continuous warming from 18:00 to 6:00. In the un-warmed plot, a ‘dummy’ heater of the same shape and size was suspended at the same height to simulate the shading effects of the heater. The distance between the adjacent plots was about 5 m to avoid heating contamination between plots. This FATI facility could provide 2 m×2 m sampling areas with uniform and reliable warming effects. The FAIT facility could significantly increase the mean soil temperature at 5 cm depth by 1.8°C. The same soil water content in 0-20 cm depth was maintained in both the treatments during the entire growth period of wheat (Tian et al. 2010). The winter wheat cultivar Yangmai 11 was manually sown on 15 November, 2007, and 2 November, 2008 at a density of 225 plants m-2 with a row spacing of 20 cm and were harvested on 2 Jun,e 2008 and 24 May, 2009, respectively. In accordance with local agronomic practices, the fertilizer applications of N, P and K in each plot were 225, 75 and 75 kg ha-1, respectively. The total P and K and 50% N were applied 2 days prior to sowing as basal dressing. The other 10% N was applied as side dressing at early tillering stage at the beginning of March, and 40% at the spike initiation stage at the beginning of April. The
© 2014, CAAS. All rights reserved. Published by Elsevier Ltd.
Impacts of Nighttime Warming on the Soil Nematode Community in a Winter Wheat Field of Yangtze Delta Plain, China
precipitations were 396.9 mm in 2007-2008 growing season and 354.1 mm in 2008-2009 growing season, thus, no irrigation was applied during the entire growth period of winter wheat.
Soil sampling For temporal nematode population measurements, soil samples were collected at four key growth stages of winter wheat viz., booting stage (28 March, 2008 and 16 March, 2009 ), heading stage (27 April, 2008 and 9 April, 2009), grain filling stage (13 May, 2008 and 4 May, 2009) and maturity stage (30 May, 2008 and 24 May, 2009). Each soil sample was collected from six randomly selected sampling points at 5 cm intervals from 0 to 20 cm depth. Six sub-samples for each soil depth class were blended to get one composite sample for each depth class per plot. Each soil sample was passed through a 6-mm-mesh soil sieve to remove the plant leaves and roots, and large stones. All samples were stored in a refrigerator at 4°C until subsequent analysis.
Nematode extraction and identification Sucrose solution-elutriation-centrifugation method was used to extract soil nematodes from about 100 g fresh soil (Bulluck et al. 2002). Then the nematodes were heat-killed by immersion in 65°C water for 2 min and preserved in triethanolamine formaldehyde (TAF) solution (Shepherd, 1970). Total nematodes in each sample were counted under an anatomical lens (40×). For each sample, 100 nematodes were randomly selected to identify the genera, trophic groups, and colonizer-persister (c-p) value with the aid of an optical microscope (Yeates et al. 1993; Bongers 1994; Yin 1998; Okada and Harada 2007; Li et al. 2012). In the present study, the nematodes were classified as four trophic groups characterized by feeding habits, bacterivores (Ba), plantparasites (H), carnivores/omnivores (Ca/Om), and fungivores (Fu). Soil moisture was determined by oven-drying samples at 105°C. The density of total and different trophic-group nematodes were adjusted to the number per 100 g dry soil. The nematode abundance for each genus was the percentage of specific genus in total nematodes. Nematode community structure was characterized by Shannon-Wiener index (H´) (Shannon and Weaver 1949), Pielou’s evenness index (J) (Kennedy and Smith 1995), genus dominance index (λ) (Bongers 1990), enrichment index (EI), structure index (SI) (Ferris et al. 1997), and Wasilewska index (WI) (Yeates 2003).
Statistical analysis The analysis of variances for soil nematode population
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density, abundance and community structure were performed independently using the procedure of SPSS 13.0 (SPSS Inc, Chicago, IL, USA). Least significant differences (LSD) at P<0.05 were used to detect significant differences among means (Steel and Torrie 1980).
Acknowledgements
This research was supported by the National Basic Research Program of China (2010CB951501), the Key Technologies R&D Program of China during the 12th Five-Year Plan period (2011BAD16B14), the National Natural Science Foundation of China (30771278) and the Innovation Program of Chinese Academy of Agricultural Sciences, China.
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