Soil Biology & Biochemistry 40 (2008) 2706–2709
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Selection of selective biocides on soil microarthropods Yanmei Xiong a, b, c, Yuanhu Shao a, b, c, Hanping Xia a, b, c, Zhian Li a, b, c, Shenglei Fu a, b, c, * a
Institute of Ecology, South China Botanical Garden, The Chinese Academy of Sciences, Guangzhou 510650, China Heshan National Field Research Station of Forest Ecosystem, Heshan 529725, China c Heshan Hilly Land Interdisciplinary Experimental Station, The Chinese Academy of Sciences, Heshan 529725, China b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 19 November 2007 Received in revised form 10 July 2008 Accepted 16 July 2008 Available online 13 August 2008
In order to seek for selective biocides on soil microarthropods, we conducted a short-term pot experiment with treatments of five biocides: pyridaben, profenofos, abamectin, triflumuron and naphthalene, and tested their effectiveness and selectivity on soil microarthropods. Under the conditions of our experiment, only pyridaben and naphthalene were selective biocides on soil microarthropods when applied at appropriate rates. Although profenofos significantly decreased soil microarthropod density, it also significantly decreased soil nematode density. Abamectin did not inhibit soil microarthropods but decreased soil nematode density. Profenofos and the highest level of naphthalene application stimulated soil microbial biomass one week after application. Triflumuron showed no negative effect on soil microarthropods, soil nematodes and soil microbial biomass. Ó 2008 Elsevier Ltd. All rights reserved.
Keywords: Biocide Selectivity Soil microarthropod Soil nematode Soil microorganism Defaunation
Soil fauna play a very important role in soil processes (Cole et al., 2006). Soil microarthropods, mainly Collembola (springtails) and Acari (mites) are usually the dominant mesofauna taxa in most soils (Heneghan et al., 1999; Taylor et al., 2004). Although microarthropods have less biomass compared to soil microflora and macrofauna, the functional importance of soil microarthropods is often disproportionate to their actual biomass (Anderson, 1988). There has been wide recognition over the past few decades of the role of removal experiments, namely, removing particular groups of organisms, which showed great potential in revealing the consequences of biodiversity loss in ecosystems (Dı´az et al., 2003). However, the studies on removal of soil biodiversity in field are relatively few due to lack of effective approach to remove target soil organisms (Blair et al., 1995; Kaffe-Abramovich and Steinberger, 2006). From 1970s to early 1990s, great efforts have been done to examine the selectivity of a wide range of biocides on soil organism groups. However, almost all tested biocides had a poor specificity (Ingham and Coleman, 1984; Ingham, 1985; Colinas et al., 1994). A large number of new biocides emerged in the past two decades, but the selectivity of these biocides is poorly known. Naphthalene has long been applied onto litter surface to reduce litter microarthropods in decomposition studies, but its application to remove
* Corresponding author. Institute of Ecology, South China Botanical Garden, The Chinese Academy of Sciences, Guangzhou 510650, China. Tel.: þ86 2037252592; fax: þ86 2037252615. E-mail address:
[email protected] (S. Fu). 0038-0717/$ – see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.soilbio.2008.07.014
soil microarthropods was rare and its effectiveness and selectivity have not been thoroughly tested (Witkamp and Crossley, 1966; Wright and Coleman, 1988; Blair et al., 1989). Therefore, we conducted this study in order to seek for biocides which can inhibit soil microarthropods selectively without any non-target effects on soil nematodes and microorganisms. Five biocides were chosen to represent a wide range of chemicals commonly used for pest control: pyridaben (C19H25ClN2OS), profenofos (C11H15O3PSClBr), abamectin (C48H74O14), triflumuron (C15H10ClN2O3F3) and naphthalene (C10H8). Experimental pots were made of polyvinyl chloride material with 25 cm in diameter and 30 cm in depth. Test soil was a sandy acrisol from 0 to 15 cm layer of a wild land with naturally occurring shrubs and herbs. Three kilograms of soil was filled into each pot, leaving the headspace height of 20 cm to eliminate the migration of soil animals. Seven treatments and a control were included in this experiment, each with four replicates. The treatments were: pyridaben, profenofos, abamectin and triflumuron at manufacturer-recommended rates, namely, pyridaben: 75 mg l1; profenofos: 525 mg l1; abamectin: 4 mg l1; triflumuron: 40 mg l1; and three levels of naphthalene application, representing 0.3, 1 and 2 the common application rate reported in literature (i.e. 30 g m2, 100 g m2 and 200 g m2) (Blair et al., 1989). The controls were treated with water only. Each pot was added with 400 ml corresponding chemical solution or water. Due to low solubility of naphthalene in water (31 mg l1 at 25 C), 400 ml water was added after application of naphthalene onto the soil surface. All pots were placed under a shed at ambient temperature during the
Y. Xiong et al. / Soil Biology & Biochemistry 40 (2008) 2706–2709
10
Nematode individuals g-1 soil
experiment. Soil sampling occurred once a week after application and there were four samplings in total. A soil corer (5 cm in diameter and 5 cm in depth) was used for sampling, and two soil cores per pot were sampled at each time. The holes where samples were taken were refilled with the surface soil in the same pot. All pots were watered twice a week in order to keep soil moisture at 30%. Collembola and Acari were extracted with Tullgren funnels from one soil core of each pot and then counted (Crossley and Blair, 1991). The other soil core was used for nematode extraction and microbial analysis. Nematodes were extracted with Baermann funnels from 50 g fresh soil (McSorley, 1987). All nematodes in each sample were counted and classified into the following five trophic groups: bacterivores, fungivores, plant-parasites, omnivores and predators (Yeates et al., 1993; Bongers and Bongers, 1998). Soil microbial biomass C was measured using the chloroform fumigation-extraction method, with 20 g fresh soil each for fumigated and unfumigated extractions (Vance et al., 1987). Data were analyzed using one-way ANOVA, followed by LSD test for comparison among treatments and the control. All analyses were performed using the SPSS 13.0 software. Acari dominated in test soil over Collembola, being 82.7 9.0% of total microarthropods based on control data. Plant-parasites and bacterivores were the dominant trophic groups of nematodes, accounting for 72.1 4.7% and 17.5 4.6% of the total nematodes, respectively. One week after application, pyridaben, profenofos and the three levels of naphthalene reduced the density of soil microarthropods by 63.6–84.8% compared to the control (P < 0.05 or P < 0.01; Fig. 1). The density of plant-parasitic nematodes was decreased by profenofos and abamectin (P < 0.01 and P < 0.05, respectively; Fig. 2), and the density of bacterivores was reduced by profenofos (P < 0.05; Fig. 2). Soil microbial biomass C was increased by profenofos and 2 naphthalene (P < 0.01 and P < 0.05, respectively; Fig. 3), but none of the biocides showed negative effect on soil microbial biomass.
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Bacterivores Plant-parasites Fungivores Omnivores Predators
8
6
4
*
** 2
** 0 s e e n n e l en ofo mecti muro halen halen len ntro ridab t fen tha a lu ht h f h i p p r p Py Ab Pro a a a T × N 1×N 2×N 0.3
Co
Fig. 2. Effects of biocides on soil nematode density one week after application. Mean number of specimens per gram dry soil (S.E.) for each treatment; n ¼ 4. Treatments significantly different from the control are marked with asterisks (*P < 0.05 and **P < 0.01).
The inhibitory effect of profenofos on soil microarthropods lasted for three weeks (P < 0.01; Fig. 1; Table 1). Pyridaben and the two higher doses of naphthalene also showed inhibitory effects on soil microarthropods, but they only lasted for two weeks (P < 0.05 or P < 0.01; Fig. 1; Table 1). There was no effect of abamectin on soil microarthropods over the four weeks. Profenofos and abamectin lost their effects on plant-parasitic nematodes in the second week after application, but their power recovered in the third and fourth week (P < 0.01 or P < 0.05; Table 2). Unfortunately, soil microbial biomass data of week 2–4 after application were lost in an accident of equipment malfunction.
14
250
Acari Collembola
**
200 -1
Microbial biomass C (mg kg )
Microarthropod individuals per core
12
10
8
6
4
* ** **
2
**
**
* 150
100
50
0 e en
ht ha l
le ne
en e
ha 2
×
N
ap
N ap
ht
th N
×
1×
ap h
ifl Tr 3 0.
Fig. 1. Effects of biocides on soil microarthropod density one week after application. Mean number of specimens per sampling core for each treatment; n ¼ 4. Treatments significantly different from the control are marked with asterisks (*P < 0.05 and **P < 0.01).
al
ur
on
tin um
s
ec
fo
am Ab
en
of en o
Pr
rid ab
on t C
Py
l e e sR n R lene nR in R len len ntro abe fenofo mect umuro phtha phtha phtha d i r a l Py Ab Pro Trif 3× Na 1× Na 2× Na 0.
Co
ro
l
0
Fig. 3. Effects of biocides on soil microbial biomass C one week after application; n ¼ 4. Mean number of microbial biomass C (S.E.) for each treatment. Treatments significantly different from the control are marked with asterisks (*P < 0.05 and **P < 0.01).
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Y. Xiong et al. / Soil Biology & Biochemistry 40 (2008) 2706–2709
Table 1 Soil microarthropod density (individuals per core) two to four weeks after biocide application Weeks
Control
Pyridaben
Profenofos
Abamectin
Triflumuron
0.3 Naphthalene
1 Naphthalene
2 Naphthalene
2 3 4
12.5 (2.5) 10.5 (1.6) 3.8 (1.1)
7.0 (2.6)* 6.7 (2.3) 3.5 (1.0)
0.3 (0.3)** 0.3 (0.3)** 4.8 (2.1)
7.8 (1.2) 11.2 (3.0) 8.8 (2.3)
9.8 (1.3) 13.5 (3.2) 16.0 (4.7)**
9.5 (1.6) 10.3 (2.7) 12.2 (2.1)*
5.5 (1.8)** 8.8 (2.9) 3.5 (0.6)
7.0 (1.5)* 10.3 (1.4) 7.0 (3.0)
Data are means (standard error, n ¼ 4). Treatments significantly different from the control are marked with asterisks (*P < 0.05 and **P < 0.01).
Table 2 Soil plant-parasitic nematode density (individuals g1 dry soil) two to four weeks after biocide application Weeks
Control
Pyridaben
Profenofos
Abamectin
Triflumuron
0.3 Naphthalene
1 Naphthalene
2 Naphthalene
2 3 4
3.1 (0.9) 5.8 (0.9) 7.1 (1.8)
4.3 (0.4) 6.1 (0.3) 4.6 (1.2)
3.0 (1.1) 0.7 (0.2)** 2.7 (0.7)*
3.3 (0.2) 2.4 (0.6)* 2.7 (0.8)*
2.8 (1.1) 3.6 (1.2) 5.6 (2.3)
6.9 (0.2) 4.6 (1.3) 4.6 (0.4)
4.3 (1.1) 3.4 (0.8) 6.1 (1.0)
2.1 (0.9) 2.3 (0.9)* 4.1 (1.1)
Data are means (standard error, n ¼ 4). Treatments significantly different from the control are marked with asterisks (*P < 0.05 and **P < 0.01).
Data from one week after application showed that pyridaben and the two lower levels of naphthalene selectively removed soil microarthropods. Since the effect of 1 naphthalene lasted longer than that of 0.3 naphthalene (Table 1), the former (i.e. 100 g m2) is more appropriate for removing soil microarthropods. Our results justified the application rate of naphthalene in the previous studies (Witkamp and Crossley, 1966; Heneghan et al., 1999). Abamectin selectively decreased plant-parasitic nematodes one week after application and its inhibitory effect lasted for four weeks (Fig. 2; Table 2). Abamectin and triflumuron were tested effective in phytophagous mite and insect control when applied on crops (Sa´enz-decabezo´n et al., 2002; Hardman et al., 2003), however, they showed no negative effect on soil Collembola and Acari in the present study (Fig. 1; Table 1). These studies suggested that there is a discrepancy of biocidal effects between aboveground and belowground applications. The possible reason is that there is a great diversity of mites in soil, with a totally different community from that of aboveground phytophagous mites which usually belong to only a few families such as Tetranychidae and Eriophyidae (Bird et al., 2004). In addition, the power of the pesticides was possibly reduced by high adsorption of the chemicals in soil (Schmidt et al., 2000). As pointed out in a review article by Ingham (1985), poor selectivity is still the main drawback of many pesticides available today (Schmidt et al., 2000; Ja¨nsch et al., 2006). Although profenofos is recognized as an acaricide, it showed inhibitive impacts on soil nematodes in our study (Fig. 2). Application of chemicals would possibly introduce exogenous nutrients like N and P, and an energy source to soil microbes. The increase of soil microbial biomass in profenofos and 2 naphthalene treated soils might be due to the addition of C with both chemicals and of P with profenofos (Fig. 3). Additions of naphthalene and organophosphorus pesticides have been reported to increase microbial biomass (Williams and Wiegert, 1971; Sa´nchez et al., 2004). Therefore, cautions must be taken in selection of selective biocides to evaluate if exogenous nutrients and energy might cause confounding effects.
Acknowledgements This research was supported by the National Science Foundation of China, the ‘‘100 Elites’’ Program and the Knowledge Innovation Program of the Chinese Academy of Sciences. We are grateful to Dr. Weixin Zhu for suggestions on experimental design and to Dr. Xian Cai for providing experimental facilities. We thank Lixia Zhou, Shaowei Chen and Haifang Li for laboratory assistance. Helpful comments from four anonymous reviewers and the Chief Editor, Dr. Joshua P. Schimel, were greatly appreciated.
References Anderson, J.M., 1988. Spatio-temporal effects of invertebrates on soil processes. Biology and Fertility of Soils 6, 216–227. Bird, S.B., Coulson, R.N., Fisher, R.R., 2004. Changes in soil and litter arthropod abundance following tree harvesting and site preparation in a loblolly pine (Pinus taeda L.) plantation. Forest Ecology and Management 202, 195–208. Blair, J.M., Crossley Jr., D.A., Rider, S., 1989. Effects of naphthalene on microbial activity and nitrogen pools in soil–litter microcosms. Soil Biology and Biochemistry 21, 507–510. Blair, J.M., Bohlen, P.J., Stinner, B.R., Edwards, C.A., 1995. Manipulation of earthworm population in field experiments in agroecosystems. Acta Zoologica Fennica 196, 48–51. Bongers, T., Bongers, M., 1998. Functional diversity of nematodes. Applied Soil Ecology 10, 239–251. Cole, L., Bradford, M.A., Shaw, P.J.A., Bardgett, R.D., 2006. The abundance, richness and functional role of soil meso- and macrofauna in temperate grassland – a case study. Applied Soil Ecology 33, 186–198. Colinas, C., Ingham, E., Molina, R., 1994. Population responses of target and nontarget forest soil organisms to selected biocides. Soil Biology and Biochemistry 26, 41–47. Crossley Jr., D.A., Blair, J.M., 1991. A high-efficiency, ‘‘low-technology’’ Tullgren-type extractor for soil microarthropods. Agriculture, Ecosystems and Environment 34, 187–192. Dı´az, S., Symstad, A.J., Chapin III, F.S., Wardle, D.A., Huenneke, L.F., 2003. Functional diversity revealed by removal experiments. Trends in Ecology and Evolution 18, 140–146. Hardman, J.M., Franklin, J.L., Moreau, D.L., Bostanian, N.J., 2003. An index for selective toxicity of miticides to phytophagous mites and their predators based on orchard trials. Pest Management Science 59, 1321–1332. Heneghan, L., Coleman, D.C., Zou, X., Crossley Jr., D.A., Haines, B.L., 1999. Soil microarthropod contributions to decomposition dynamics: tropical–temperate comparisons of a single substrate. Ecology 80, 1873–1882. Ingham, E.R., Coleman, D.C., 1984. Effects of streptomycin, cycloheximide, fungizone, captan, carbofuran, cygon, and PCNB on soil microorganisms. Microbial Ecology 10, 345–358. Ingham, E.R., 1985. Review of the effects of 12 selected biocides on target and nontarget soil organisms. Crop Protection 4, 3–32. Ja¨nsch, S., Frampton, G.K., Ro¨mbke, J., van den Brink, P.J., Scott-Fordsmand, J.J., 2006. Effects of pesticides on soil invertebrates in model ecosystem and field studies: a review and comparison with laboratory toxicity data. Environmental Toxicology and Chemistry 25, 2490–2501. Kaffe-Abramovich, T., Steinberger, Y., 2006. Soil microbial functional diversity response following nematocide and biocide amendments in a desert ecosystem. Soil Biology and Biochemistry 38, 1966–1976. McSorley, R., 1987. Extraction of nematodes and sampling methods. In: Brown, R.H., Kerry, B.R. (Eds.), Principles and Practice of Nematode Control in Crops. Academic Press, Sydney, pp. 13–47. Sa´enz-de-cabezo´n, F.J., Pe´rez-Moreno, I., Marco, V., 2002. Effects of triflumuron on the two-spotted spider mite, Tetranychus urticae (Acari: Tetranichydae). Experimental and Applied Acarology 26, 71–78. Sa´nchez, M.E., Estrada, I.B., Martı´nez, O., Martı´n-Villacorta, J., Aller, A., Mora´n, A., 2004. Influence of the application of sewage sludge on the degradation of pesticides in the soil. Chemosphere 57, 673–679. Schmidt, I.K., Ruess, L., Ba¨a¨th, E., Michelsen, A., Ekelund, F., Jonasson, S., 2000. Longterm manipulation of the microbes and microfauna of two subarctic heaths by addition of fungicide, bactericide, carbon and fertilizer. Soil Biology and Biochemistry 32, 707–720. Taylor, A.R., Schroter, D., Pflug, A., Wolters, V., 2004. Response of different decomposer communities to the manipulation of moisture availability: potential effects of changing precipitation patterns. Global Change Biology 10, 1313–1324.
Y. Xiong et al. / Soil Biology & Biochemistry 40 (2008) 2706–2709 Vance, E.D., Brookes, A.C., Jenkinson, D.S., 1987. An extraction method for measuring soil microbial biomass C. Soil Biology and Biochemistry 19, 703–707. Williams, J.E., Wiegert, R.G., 1971. Effects of naphthalene application on a coastal plain broomsedge (Andropogon) community. Pedobiologia 11, 58–65. Witkamp, M., Crossley Jr., D.A., 1966. The role of arthropods and microflora in breakdown of white oak litter. Pedobiologia 6, 293–303.
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Wright, D.H., Coleman, D.C., 1988. Soil faunal vs. fertilization effects on plant nutrition: results of a biocide experiment. Biology and Fertility of Soils 7, 46–52. Yeates, G.W., Bongers, T., De Goede, R.G.M., Freckman, D.W., Georgieva, S.S., 1993. Feeding habitats in soil nematode families and genera – an outline for soil ecologists. Journal of Nematology 25, 315–331.