Effects of weed and erosion control on communities of soil mites (Oribatida and Gamasina) in short-rotation willow plantings in central New York

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1 1061 Effects of weed and erosion control on communities of soil mites (Oribatida and Gamasina) in short-rotation willow plantings in central New York Maria A. Minor and Roy A. Norton Abstract: Several pre-emergent herbicides (azafenidin, oxyfluorfen, and imazaquin pendimethalin mixture), used for weed control during the establishment of short-rotation willow plantings, were tested for their impact on population density, species richness, and community structure of predaceous (Gamasina) and saprophagous and (or) mycophagous (Oribatida) soil mites. The experimental control was hand-weeded (no herbicide). Two site preparation treatments were used: conventional (disked) and erosion controlled (no-till with cover crop of winter rye). The influence of herbicide application on non-target organisms (soil mites) cannot be generalized, with groups being differentially affected. Overall, Oribatida were most affected by herbicides. Among specific herbicides, azafenidin and oxyfluorfen had a negative effect on density and species richness of soil mites. The response of Oribatida and Gamasina to herbicides was species-specific. Two species of Oribatida (Sellnickochthonius immaculatus (Forsslund) and Liochthonius lapponicus (Trägårdh)) declined significantly in all herbicidetreated plots. The cover crop residue had positive effect on both Oribatida and Gamasina; the negative effect of herbicides on Oribatida was greatly mitigated by cover crop. Herbicides appear to reduce mite diversity and alter community structure, but they do not always affect abundance. We speculate that the sensitivity of Oribatida to herbicides can reflect the indirect impacts of herbicides on soil microflora. Résumé : Plusieurs herbicides de prélevée (azafénidine, oxyfluorfène et un mélange d imazaquine et de pendiméthaline), utilisés pour maîtriser la végétation lors de l établissement de plantations de saule à courte révolution, ont été testés quant à leur impact sur la densité de population, la richesse en espèces et la structure des communautés d acariens prédateurs (Gamasides) et saprophages ou mycophages (Oribates) dans le sol. La végétation a été éliminée manuellement (aucun herbicide) dans le traitement témoin. Deux traitements de préparation de terrain ont été utilisés : un traitement conventionnel (disquage) et un traitement visant à prévenir l érosion (aucun travail du sol avec une culture de protection de seigle d hiver). L impact de l application d herbicide sur les organismes non visés (acariens du sol) ne peut être généralisé étant donné que les différents groupes ne sont pas affectés delamême façon. Dans l ensemble, les Oribates ont été les plus affectés par les herbicides. Parmi les herbicides spécifiques, l azafénidine et l oxyfluorfène ont eu un effet négatif sur la densité et la richesse en espèces des acariens du sol. La réaction des Oribates et des Gamasides aux herbicides variait selon l espèce. Deux espèces d Oribates (Sellnickochthonius immaculatus (Forsslund) et Liochthonius lapponicus (Trägårdh)) ont significativement décliné dans toutes les parcelles traitées avec un herbicide. Les résidus de la culture de protection ont eu un effet positif tant sur les Oribates que sur les Gamasides; l effet négatif des herbicides sur les Oribates a été grandement atténué par la culture de protection. Les herbicides semblent réduire la diversité des acariens et altérer la structure des communautés mais ils n affectent pas toujours leur abondance. Nous croyons que la sensibilité des Oribates aux herbicides peut refléter les impacts indirects des herbicides sur la microflore du sol. [Traduit par la Rédaction] Introduction In temperate regions of the USA and Europe, plantationgrown willow (Salix spp.) is being developed as a new crop, Received 19 February Accepted 6 November Published on the NRC Research Press Web site at cjfr.nrc.ca on 24 April M.A. Minor 1,2 and R.A. Norton. College of Environmental Science and Forestry, State University of New York, 1 Forestry Drive, Syracuse, NY 13210, USA. 1 Corresponding author ( M.A.Minor@massey.ac.nz). 2 Present address: Institute of Natural Resources, Massey University, Private Bag 11222, Palmerston North, New Zealand. grown and harvested as a renewable source of fuel and fiber. Willows are easily propagated from cuttings, have high growth rates, and are able to resprout (coppice) after harvest, with the potential for high biomass yields every few years (Abrahamson et al. 2002). These crops offer a renewable alternative to fossil fuels as energy feedstock, and provide environmental and rural development benefits (Volk et al. 2006). The ecological sustainability of this new crop is being investigated. Johnston and Crossley (2002) highlighted the link between soil biodiversity, soil condition, and plant biomass production potential in a managed forestry system. In longer-rotation crops, such as commercial pine plantations, the abundance of soil oribatid mites has been related to changes in soil chemical and physical properties, which, in turn, cor- Can. J. For. Res. 38: (2008) doi: /x07-207

2 1062 Can. J. For. Res. Vol. 38, 2008 related with soil fertility and vitality of the trees (Hogervorst et al. 1993). There is abundant evidence that feeding activities of soil fauna increase N and P mineralization flux, contribute to increased nutrient availability in soil, enhance nutrient uptake by plants, and influence plant nutrient content (Bardgett and Chan 1999; Cragg and Bardgett 2001). Grazing by soil oribatid mites (Acari: Oribatida), for example, breaks down plant material, assists the microbial recolonization of litter material, stimulates microbial metabolism in the rhizosphere, and stabilizes nutrient leaching (Maraun et al. 1998b; Renker et al. 2005). Studies have shown that plant productivity increases in the presence of soil fauna, as a result of enhanced nutrient availability (Ingham et al. 1985; Scheu et al. 1999). Composition of the soil community is also important, as species-level changes in biota can differentially alter nutrient mineralization and, therefore, plant growth (Siepel and Maaskamp 1994; Cragg and Bardgett 2001). Plantation willows, grown at densities of plantsha 1, are an intensively managed crop, with tillage, herbicides, and fertilizers used at different stages during their establishment and management. Soil cultivation and the application of biocides and fertilizers are the main factors affecting soil fauna in agroecosystems (Moore et al. 1984; Wardle 1995). With millions of hectares of marginal agricultural lands available for perennial woody biomass crops, their impacts on soil quality and soil biodiversity have become an important focus of research. Among environmental concerns with short-rotation willow biomass crops, the intensive weed control and the soil erosion during the establishment phase are important (Abrahamson et al. 2002). Weed control is a key factor in the successful establishment of willows; a broad-spectrum herbicide is applied before planting, and a pre-emergent herbicide is applied immediately after planting. Currently, only two pre-emergent herbicides (oxyfluorfen and simazine) are used in biomass plantations, because of labeling regulations and high susceptibility of willows to herbicides (Abrahamson et al. 2002). Trials are underway to test other pre-emergent herbicides. Cover crop and conservation tillage have been used to reduce soil erosion during the establishment phase. In the second growing season, a healthy willow crop closes the canopy, which inhibits weed growth and intercepts the rain, so weed control and erosion control measures are usually not required after the first year. In New York, several experimental studies addressed the short-term and long-term impacts of different planting and tillage methods (Minor et al. 2004) and different types of fertilizer (Minor and Norton 2004) used in growing shortrotation willows on soil fauna. Herein we explore the short-term impacts of several pre-emergent herbicides and cover crop that are tested for use during the establishment phase of plantations on two major groups of soil mesofauna: oribatid and gamasine mites (Acari). In a 2 year experimental field study, we assessed the impacts of a rye cover crop and of several pre-emergent herbicides on populations and community structure of Oribatida and Gamasina. Each is vulnerable to various pesticides (Koehler 1994; Salminen et al. 1997), but both the intensity and direction of responses vary among species (Koehler 1992; Prinzing et al. 2002). Gamasina are active, fluid-feeding predators of other microarthropods, insect larvae, and nematodes (Koehler 1997). Oribatid mites, which are particulate feeders, feed primarily on soil fungi, bacteria, algae, and decaying plant material, although some necrophagy or facultative predation occurs (Schneider et al. 2004a, 2004b). They are among the most abundant and speciesrich soil arthropods, and play an important role in decomposer food webs (Siepel and Maaskamp 1994). Materials and methods Site description and sampling The experiment was conducted at the State University of New York, College of Environmental Science and Forestry Genetics Field Station in Tully, New York ( @N, @E), as a part of the herbicide trial for the Biomass for Rural Development project (Wagner 2000). The site is on a glacial outwash terrace with a 0% 3% slope. Parent material is a gravely sandy outwash derived from limestone, sandstone, and shale, and the soil (Glossoboric Hapludalf of the Palmyra series) is a gravely loam with good to excessive drainage. The available water capacity is moderate to high, and ph in the surface layer ranges from medium acid to neutral (Hutton and Rice 1977). The study site (approx. 500 m 2 ) was disked in the summer of A first baseline sampling of soil mites in the site (60 random samples) was conducted on 10 October 1997 using methods described below. In late summer 1998, prior to a second baseline sampling, the site was sprayed with a mixture of glyphosate (RoundUp TM at 2.24 kg active ingredient (a.i.)ha 1 ) and dicamba (Banvel TM at 0.56 kg a.i.ha 1 ) followed 2 weeks later by disking (Wagner 2000). The second baseline sampling was on 13 October 1998 (also 60 random samples). The herbicide experiment was established in fall 1998 in a split-plot design, where the whole plot factor was presence or absence of a cover crop. The cover crop of winter rye (Secale cereale L.) was planted in fall 1998 after disking. In the spring of 1999, rye was killed with a postemergence herbicide (RoundUp TM at 2.24 kg a.i.ha 1 ; T. Volk, personal communication 2006) and left as residue. Plots without cover crop were disked in the spring of 1999 to control germinating weeds. The willow cuttings (Salix dasyclados Wimmer, clone SV1) were hand-planted in all plots on 18 May 1999 in single rows, with cuttings 0.6 m apart and rows 1.2 m apart. The subplot factor (replicated three times) was herbicide presence and type. Twelve treatment subplots (3.1 m 1.2 m) each contained a single row of five cuttings. Preemergent herbicides were applied in a single application on 19 May 1999, the day after planting (Wagner 2000). The following treatments were used in this study: oxyfluorfen (Goal TM 2XL) at g a.i.ha 1 ; azafenidin (Milestone TM DPX-R6447) at 91.8 g a.i.ha 1 ; imazaquin pendimethalin mixture (Scepter TM 70 DG : Prowl TM 3.3 EC) at 23.0 g : 8.6 g a.i.ha 1 ; and control (hand-weeded by weekly hoeing). On 20 July 1999 and 17 October 1999 (at approximately 60 and 150 d, respectively, after treatment), 4 soil cores were collected within each treatment subplot, for a total of 96 cores in each sampling season. Sampling dates were selected to coincide with data collection in other willow trials. Mite extraction Samples (25 cm 2 to 5 cm depth) were taken at random lo-

3 Minor and Norton 1063 cations with a steel corer. Mites were extracted by drying the soil for 7 days in small Berlese Tullgren funnels constructed from commercial 10 cm diameter plastic greenhouse pots, using 7 W light bulbs as a heat source. Adult and immature oribatid and gamasine mites from each sample were counted and identified to species level using published keys, original species descriptions, and reference specimens from the Invertebrate Collection at the State University of New York, College of Environmental Science and Forestry (SUNY-ESF, Syracuse, New York) and the Canadian National Collection of Insects and Arachnids (Ottawa, Ontario). Immature mites that could not be identified to species were included in the abundance count, but excluded from the species richness count. Data analysis The parameters used to describe mite communities were population density (individualssample 1 ) and species richness (number of speciessample 1 ). Statistical analyses were conducted separately for Oribatida and Gamasina using SAS 9.2 (Statistical Analysis System, SAS Institute Inc., Cary, North Carolina). To reduce variance heterogeneity associated with count data, the data sets were log (x + 1) transformed prior to analysis. One-way ANOVA was used to test for differences between 1997 and 1998 baseline samplings. The 1999 experiment was analyzed using SAS MIXED procedure for split plots, to determine the effect of whole plot factor (presence or absence of cover crop), the effect of subplot factor (herbicide presence and type), and possible interaction effects. Effects of individual herbicides were investigated as linear contrasts by comparison with the experimental control; the Tukey Kramer procedure was used to adjust for multiple comparisons. The blocked multiresponse permutation procedures (MRBP in PC-Ord, MjM Software, version 4.41) were used to analyse compositional similarity between mite communities in different herbicide treatments (see McCune and Grace 2002). The MRBP is a non-parametric procedure that tests the hypothesis of no difference between two or more groups (McCune and Grace 2002). We applied MRBP to species abundance matrices using the Euclidean distance as similarity measure, and using experimental treatments as groups. MRBP analysis calculates the chance-corrected within-group agreement statistic (A), which ranges from 1 to 1. Low A values (<0.1) indicate that no substantial differences exist between communities (McCune and Grace 2002). The nonmetric multidimensional scaling (NMS in PC-Ord 4.41) was used to display relationships between mite species and experimental treatments; species with low abundance (less than 10 individuals) were not included in the ordination. The response of individual species to different herbicide treatments was analysed as linear contrasts if the MRBP suggested that there was a significant difference between treatments. All statistical tests were conducted at the level of significance = Results The density (F [1,116] = 0.03, p = 0.853, Fig. 1) and species richness (F [1,116] = 0.62, p = 0.432, Fig. 2) of gamasine Fig. 1. Mean density of (a) Gamasina and (b) Oribatida in herbicide experiment site, willow biomass crop, New York, Open and closed arrows indicate the 1998 site preparation and the 1999 herbicide experiment, respectively. Error bars are the 95% confidence intervals. mites did not differ significantly between October 1997 and October The density of Oribatida (approx individualsm 2 ) also remained stable (Fig. 1), although their species richness declined in 1998 following site preparation (F [1,116] = 4.25, p = 0.041; Fig. 2). Effect of pre-emergent herbicides on density or species richness of Gamasina was not detected in the 1999 experiment, either 60 or 150 days after application (Table 1). By contrast, the species richness and population density of Oribatida were reduced by pre-emergent herbicides both 60 and 150 days after application. Presence of rye cover crop residues had a very strong positive effect on both groups of

4 1064 Can. J. For. Res. Vol. 38, 2008 Fig. 2. Mean species richness of (a) Gamasina and (b) Oribatida in herbicide experiment site, willow biomass crop, New York, Open and closed arrows indicate the 1998 site preparation and the 1999 herbicide experiment, respectively. Error bars are the 95% confidence intervals. mites (Table 1; Figs. 1 and 2). A significant interaction term indicated that the effect of herbicides on Oribatida was mitigated in plots with cover crop residue (Table 1). Among different pre-emergent herbicides, significant negative effect of oxyfluorfen on both groups was detected 60 days after application in disked plots (Figs. 3 and 4). Azafenidin reduced density and richness of Oribatida both 60 and 150 days after application in plots with a rye cover crop. The imazaquin pendimethalin mixture had no significant effect on soil Gamasina and Oribatida (Figs. 3 and 4). Collectively, 19 species of Gamasina and 26 species of Oribatida were represented in the samples. The total species richness declined dramatically following the onset of site preparation; 10 species of Gamasina and 18 species of Oribatida in 1997 were reduced to 5 and 6 species, respectively, in October 1998 (Tables 2 and 3). Seven gamasine species, including surface-dwelling genera Pergamasus and Veigaia, were found only in the first baseline sampling in 1997, while the deep-soil dwelling genera Rhodacarus, Rhodacarellus, and Protogamasellus were found only in postherbicide samplings (Table 2). Eight oribatid species, including such local rarities as Masthermannia mammilaris (Berlese) and Eremobelba leporoides Jacot, were found only in the first baseline sampling. Seven Oribatida species were found only in postherbicide samplings (Table 3). Only rye cover crop plots were analysed for the effect of herbicide on mite assemblages and abundance of individual species, as the counts in disked plots were too low. There was no significant relationship between Gamasina community structure and type and (or) presence of herbicide (MRBP: July A = 0.03, p = 0.344; October A = 0.01, p = 0.424), possibly because of the overall low numbers of mites. By contrast, the Oribatida assemblages were influenced by plot treatments at 60 days past application (A = 0.19, p = 0.048), although the assemblages under three herbicide types did not differ significantly (A = 0.24, p = 0.072). At 150 days past application, the Oribatida assemblages were influenced by both herbicide presence (A = 0.02, p = 0.038) and herbicide type (A = 0.72, p = 0.027). Responses to herbicides were herbicide- and speciesspecific. At 60 days past application, the dominant oribatids Tectocepheus velatus (Michael) and Oppiella nova (Oudemans) were significantly less abundant in herbicide-treated plots (pooled herbicide treatments, T. velatus F [3,42] = 6.06, p = 0.002; O. nova F [3,42] = 2.85, p = 0.049). At 150 days past application, T. velatus (F [3,42] = 3.57, p = 0.022), Sellnickochthonius immaculatus (Forsslund) (F [3,42] = 5.90, p = 0.002), and Liochthonius lapponicus (Trägårdh) (F [3,42] = 2.85, p = 0.048) were significantly less abundant in herbicide-treated plots. The NMS ordination (Fig. 5) suggested that most of Gamasina and Oribatida abundant in 1999 experimental plots were generalist species, not strongly associated with a particular treatment. Positive effects were seen in some species: density of gamasine Rhodacarus denticulatus Berlese was highest in imazaquin pendimethalin-treated plots (pooled 1999 data, F [1,90] = 9.09, p = 0.003); Scheloribates laevigatus (Koch) had highest numbers in oxyfluorfen-treated plots (F [1,90] = 25.27, p < 0.001). The most sensitive species, which declined significantly in all herbicide-treated plots, were Brachychthoniidae oribatids: S. immaculatus and L. lapponicus (S. immaculatus: azafenidin F [1,90] = 12.43, p = 0.001; oxyfluorfen F [1,90] = 11.18, p = 0.001; imazaquin pendimethalin F [1,90] = 10.0, p = 0.002; L. lapponicus: azafenidin F [1,90] = 7.82, p = 0.006; oxyfluorfen F [1,90] = 6.02, p = 0.016; imazaquin pendimethalin F [1,90] = 7.82, p = 0.006). Liochthonius lapponicus and the confamilial Brachychthonius berlesei Willmann associated with the control treatment in the NMS ordination (Fig. 5). Among tested herbicides, azafenidin had the most detrimental effect on Oribatida (Fig. 5); in addition to S. immaculatus and L. lapponicus, the numbers of T. velatus (F [1,90] = 19.96, p < 0.001) and

5 Minor and Norton 1065 Table 1. Effect of herbicide treatments (pooled subplots) and cover crop on mean density (individualssample 1 ) and species richness (speciessample 1 ) of Gamasina and Oribatida in soil under willow biomass crop, New York (1999). Density Richness Group Treatment Effect 60 dpa 150 dpa 60 dpa 150 dpa Gamasina Cover crop Positive Herbicide None Cover crop herbicide Interaction Oribatida Cover crop Positive Herbicide Negative Cover crop herbicide Interaction Note: dpa, days postapplication (herbicide); p values for the hypothesis of no effect. Fig. 3. Density of Gamasina (a and b) and Oribatida (c and d) in experimental treatments, willow biomass crop, New York. Back-transformed means of log-transformed data: disk, disked plots; rye, rye cover crop plots; control, no herbicide; mix, imazaquin + pendimethalin mixture. Means with the same letter are not significantly different (LS means, multiple means comparison, Tukey Kramer adjustment, p < 0.05). *, significantly different from control (LS means contrast, F [1,44] = 6.98, p = 0.011). O. nova (F [1,90] = 9.89, p = 0.023) were significantly reduced in azafenidin-treated plots. Discussion Herbicide effects The observed impact of herbicides on soil mites can be related to the herbicide activity and persistence in soil, and the timing of the sampling. The herbicides used in our study are moderately persistent in soil, with an estimated average field half-life of <70 d (Weed Science Society of America 1994; Smith et al. 2005). The short life span and high mobility of Gamasina (relative to Oribatida) may explain why no clear effects of herbicide on these mites were detected. Other studies suggest that Gamasina can be negatively affected by application of herbicides (Koehler 1994), or may show no effect (Salminen et al. 1997). Minor et al. (2004) found no effect of pre-emergent herbicide (oxyfluorofen, 1.1 kg a.i.ha 1 ) on Gamasina 1 year following the herbicide application in short-rotation forestry (SRF) willows. Consistent with our observations, others have shown that Oribatida are negatively affected by herbicides, although the effects on abundance may be short-lived. The typical pattern is a sharp drop in population density of oribatid mites in response to herbicide application, sometimes followed by a brief increase in density; finally, the populations return to control

6 1066 Can. J. For. Res. Vol. 38, 2008 Fig. 4. Species richness of Gamasina (a and b) and Oribatida (c and d) in experimental treatments, willow biomass crop, New York. Backtransformed means of log-transformed data: disk, disked plots; rye, rye cover crop plots; control, no herbicide; mix, imazaquin + pendimethalin mixture. Means with the same letter are not significantly different (LS means, multiple means comparison, Tukey Kramer adjustment, p < 0.05). *, significantly different from control (LS means contrast, F [1,44] = 6.43, p = 0.014). Table 2. Total abundance of Gamasina: first baseline sampling (1997), second baseline sampling (1998), and herbicide experiment (1999), willow biomass crop, New York. Species July 1999 Oct Pergamasus crassipes (L., 1758) 9 Pergamasus runcatellus (Berlese, 1903) 2 Pergamasus digitulus Karg, Veigaia pusilla (Berlese, 1916) 2 Rhodacarus denticulatus Berlese, Rhodacarellus silesiacus Willmann, Protogamasellus mica (Athias-Henriot, 1961) Gamasellodes bicolor (Berlese, 1918) Arctoseius cetratus (Sellnick, 1940) Proctolaelaps (Paraproctolaelaps) orientalis (Chant, 1963) 1 Neoseiulus agrestis (Karg, 1960) Hypoaspis (Geolaelaps) angusta Karg, Hypoaspis (Cosmolaelaps) vacua (Michael, 1891) 1 Hypoaspis (Cosmolaelaps) sp. 1 Dendrolaelaps sp. A 2 Dendrolaelaps sp. B 1 Macrocheles canadensis Banks, Antennoseius nr. bacatus Athias-Henriot, Antennoseius sp. 3 1 No. of samples Total no. of Gamasina individuals Total no. of species

7 Minor and Norton 1067 Table 3. Total abundance of Oribatida: first baseline sampling (1997), second baseline sampling (1998), and herbicide experiment (1999), willow biomass crop, New York. Species July 1999 Oct Tectocepheus velatus (Michael, 1880) Oppiella nova (Oudemans, 1902) Scheloribates laevigatus (C.L. Koch, 1836) Scheloribates labyrinthicus Jeleva, Scheloribates sp. A Scheloribates sp. B 1 Scheloribates sp. C 1 1 Rhysotritia ardua (C.L. Koch, 1841) 7 5 Masthermannia mammilaris (Berlese, 1904) 1 Cultroribula divergens Jacot, Epilohmannia minuta Berlese, Ramusella (Insculptoppia) insculpta (Paoli, 1908) 1 Microppia minus (Paoli, 1908) Punctoribates punctum (C.L. Koch, 1839) 7 1 Eremobelba leporoides Jacot, Suctobelbella sp. A 1 Suctobelbella sp. B 1 Suctobelbella sp. C 1 1 Eniochthonius minutissimus (Berlese, 1904) 2 Podoribates pratensis (Banks, 1895) 7 Sellnickochthonius immaculatus (Forsslund, 1942) Liochthonius lapponicus (Trägårdh, 1910) 2 13 Brachychthonius berlesei Willmann, Sellnickochthonius zelawaiensis (Sellnick, 1928) 1 Poecilochthonius spiciger (Berlese, 1910) 3 Oripodidae gen. sp. 1 No. of samples Total no. of Oribatida individuals No. of species level within several months (Moore et al. 1984; Tsonev and Furnadzhieva 1984). Other effects can be more persistent; weed control (oxyfluorofen at 1.1 kg a.i.ha 1 ) had significantly reduced diversity (but not density) of Oribatida 1 year following the herbicide application in SRF willows (Minor et al. 2004). The information on direct toxicity of specific pre-emergent herbicides to soil arthropods is very scarce. Oxyfluorfen, pendimethalin, imazaquin, and azafenidin are nontoxic to honeybees at recommended application rates (WSSA 1994). However, Milligan (2000) showed that survival and reproduction in Typhlodromus pyri Scheuten (a plant-dwelling gamasine mite) was affected by oxyfluorfen at a concentration equivalent to 235 g a.i.ha 1, which is about 150% of the typical field application rate. The negative effect of herbicides on Oribatida was greatly mitigated in plots with cover crop residue. The microbial activity is stimulated under cover crop residues (Reddy et al. 2003), which possibly contributed to the degradation of herbicides. Pendimethalin, imazaquin, and azafenidin are rapidly inactivated through microbial degradation (Singh and Kulshrestha 1991; Delaney and Morton 1996; Flint and Witt 1997). In addition, soil organic matter accumulates under cover crop residues (Reddy et al. 2003). Soil organic matter creates additional herbicide adsorption sites, which would reduce the herbicide release into soil solution, and therefore its toxicity (Locke and Bryson 1997). Oxyfluorfen is not subject to significant microbial degradation but is especially readily adsorbed (Weed Science Society of America 1994), which may explain why significant negative effect of oxyfluorfen on both Oribatida and Gamasina was detected in disked plots but not in cover crop plots. Effects of disking and rye cover crop The strong positive effect of cover crop residues on both Gamasina and Oribatida can be attributed to the favorable microenvironment created by the rye residue, combined with the absence of tillage in cover crop plots. The no-till cover crop plots had the thick layer of organic matter from the dead rye, while disked plots had practically no surface litter. Reeleder et al. (2006) observed similar increase in Gamasina and Oribatida under a no-till rye cover crop. Rye cover crop had no obvious effect on mite communities in Minor et al. (2004) study in SRF willows, but in that experiment the cover crop was disked under, instead of forming a surface mat. Taylor and Wolters (2005) found that densities of the dominant oribatid taxa correlate strongly with microbial biomass and water content of the litter. In agricultural systems, a surface layer of crop residue was found to aid in soil moisture retention during droughty periods, and to reduce daily soil temperature amplitudes (Dormaar and Carefoot 1996). Density of soil fungi is higher under no-till management and under crop residue left on the soil surface (Reddy et al.

8 1068 Can. J. For. Res. Vol. 38, 2008 Fig. 5. Ordination of experimental treatments in species space for (a) Gamasina and (b) Oribatida, willow biomass crop, New York. Nonmetric multidimensional scaling, pooled 1999 data, rare species excluded. Control, no herbicide; Mix, imazaquin + pendimethalin mixture. Gamasina: Ace, A. cetratus; Han, H. angusta; Nag, N. agrestis; Pmi, P. mica; Rde, R. denticulatus. Oribatida: Bbe, B. berlesei; Lla, L. lapponicus; Ono, O. nova; Rar, R. ardua; Sim, S. immaculatus; Sla, S. laevigatus; Tve, T. velatus. 2003), so our cover crop plots probably had more available food resources. Tectocepheus velatus, which dominated the oribatid community in cover crop plots, is a ubiquitous early colonizer species with wide ecological range, known to feed on a variety of resources. Luxton (1972) classified it as a mycophage, but Schneider et al. (2004a) found that the 15 N stable isotope signature of T. velatus was similar to that of the L/F litter layer, and suggested that T. velatus may feed predominantly on litter in some situations. A species with short life cycle and parthenogenetic reproduction (Luxton 1981), T. velatus can quickly establish populations of considerable size in favourable conditions, reaching a tremendous population density (up to 628 in a 5 cm 3 sample) under the thick mat of rye residue in our cover crop plots. Oppiella nova, another widespread parthenogenetic oribatid mite, feeds on fungi (Luxton 1972). While O. nova was also a dominant, it did not approach the densities of T. velatus in cover crop plots. Tillage has effects opposite to those of crop residues; it disrupts soil structure, and promotes faster drying and wider temperature fluctuations in the surface soil. The decline in gamasine and oribatid populations in tilled soil is well documented (Wardle 1995; Hülsmann and Wolters 1998). Comparing with no-till treatment, tillage decreased density and diversity of Gamasina during the establishment of SRF willows (Minor et al. 2004). Overall, the more stable microclimate, higher moisture retention, and a richer resource base created by surface rye residue probably contributed to the significantly higher densities of Oribatida and Gamasina in cover crop plots in our experiment. The severe summer drought at the study site, to which oribatid mites are particularly sensitive (Lindberg et al. 2002), may have further contributed to their low abundance in disked plots. Community composition Anderson (1978) suggested that the structure of soil mite communities relates strongly to structural and nutritional properties of a substrate. In addition to possible direct toxicity, pre-emergent herbicides can influence the Oribatida community indirectly, by altering trophic interactions with fungi and bacteria (Salminen et al. 1997), for example, if herbicides alter the community structure of microbes that either comprise the oribatid s food or degrade plant residues to the point of palatability. There is evidence (see recent review by Strandberg and Scott-Fordsmand 2004) that application of a herbicide (pendimethalin) can cause significant reduction in abundance and activity of soil fungi, bacteria, and actinomycetes, although these declines frequently are short term (4 6 weeks). By contrast, other studies cited by these authors reported no effects of pendimethalin on fungi and bacteria. Azafenidin, while not decreasing the total number of microorganisms, can have specific negative effects on soil bacteria and actinomycetes, cause persistent changes in microbial community structure (Milanova et al. 2005), alter functional diversity of soil microbes, and, in vitro, inhibit mycelial growth of some fungi (Daugrois et al. 2005). Such influences on community structure may underlie the detrimental effects of azafenidin on certain oribatid species (T. velatus, O. nova, and Brachychthoniidae), since fungi vary widely in their palatability to these and other soil fungivores (Maraun et al. 1998a; Schneider et al. 2004b). The oribatid S. laevigatus, which reached high density in one of oxyfluorfen-treated rye cover plots, is a generalist able to feed on a variety of resources: fungi, fungal spores, green algae, and plant litter material (Luxton 1972; Schneider et al. 2004a). Although there was no direct effect of herbicides on abundance or species richness of Gamasina, their community shifted from larger surface-dwelling species towards smaller euedaphic Rhodacaridae (R. denticulatus, Rhodacarellus silesiacus Willmann, and Protogamasellus mica (Athias-Henriot)) following the first application of glyphosate, and further towards euedaphic R. denticulatus and

9 Minor and Norton 1069 P. mica in imazaquin pendimethalin- and oxyfluorfentreated plots. A shift in soil microarthropod assemblages towards euedaphic species often follows application of a toxic substance or a contaminant to the soil surface (Filser et al. 2000; Minor and Norton 2004). Conclusions Previous studies had demonstrated that tillage and weed control practices in short-rotation forestry are the critical factors influencing density, species richness, and community composition of soil mites (Minor et al. 2004; Minor and Norton 2004). Unfortunately, in such systems it is often difficult to separate the effects of individual factors (soil cultivation, direct and indirect effects of agrochemicals, and plant biomass) on soil organisms, and the literature dealing with effects of agricultural practices on soil microarthropods is often contradictory (Wardle 1995). Our study shows, for example, that when weed and erosion control measures are combined, the effect on soil microarthropods is not additive. Our study also suggests that the impacts of soil-applied herbicides on non-target soil organisms cannot be generalized; herbicides may reduce mite diversity and produce changes in community structure, but the response is highly herbicide- and species-specific; the total mite abundance may or may not be affected. The abundance-only approach may not be a reliable way of evaluating herbicide impact on soil fauna, and the herbicide-induced changes in community structure and diversity should be recorded; there is evidence, for example, that the effect of Oribatida on decomposition processes in soil is linked to their community composition and the trophic preferences of dominant species (Siepel and Maaskamp 1994). We suggest that the sensitivity of Oribatida to herbicides is an indirect reflection of herbicide impacts on soil microorganisms. Future research should aim to separate the direct and indirect effects of herbicide toxicity; particularly, shifts in microbial species composition and species diversity and their impact on higher trophic levels should be more fully investigated. Acknowledgements We are grateful to Dr. Evert Lindquist (the Canadian National Collection of Insects and Arachnids, Ottawa, Canada) for checking identifications of Gamasina and for help with identification of difficult species. We also thank Dr. Timothy Volk (State University of New York, College of Environmental Science and Forestry (SUNY-ESF), Syracuse, USA) for information on SRF willow management and many discussions, and Dr. Lawrence Abrahamson (SUNY- ESF, Syracuse, USA) for his support of the project. This research was funded by the Biomass for Rural Development Project, sponsored by the Niagara Mohawk Power Corporation and the United States Department of Energy, National Renewable Energy Laboratory. 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