Do Incremental Increases of the Herbicide Glyphosate Have Indirect Consequences for Spider Communities?
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2002. The Journal of Arachnology 30:288±297 DO INCREMENTAL INCREASES OF THE HERBICIDE GLYPHOSATE HAVE INDIRECT CONSEQUENCES FOR SPIDER COMMUNITIES? James R. Bell: School of Life Sciences, University of Surrey Roehampton, Whitelands College, West Hill, London SW15 3SN, UK Alison J. Haughton1: Crop and Environment Research Centre, Harper Adams University College, Newport, Shropshire, TF10 8NB, UK Nigel D. Boatman2: Allerton Research and Educational Trust, Loddington House, Loddington, Leicestershire, LE7 9XE, UK Andrew Wilcox: Crop and Environment Research Centre, Harper Adams University College, Newport, Shropshire, TF10 8NB, UK ABSTRACT. We examined the indirect effect of the herbicide glyphosate on ®eld margin spider com- munities. Glyphosate was applied to two replicated (n 5 8 per treatment) randomized ®eld experiments over two years in 1997±1998. Spiders were sampled using a modi®ed garden vac monthly from May± October in the following treatments: 1997 comprised 90g, 180g, & 360g active ingredient (a.i.) glyphosate ha21 treatments and an unsprayed control; 1998 comprised 360g, 720g and 1440g a.i. glyphosate ha21 treatments and an unsprayed control. We examined the indirect effect of glyphosate on the spider com- munity using DECORANA (DCA), an indirect form of gradient analysis. We subjected DCA-derived Euclidean distances (one a measure of beta diversity and the other a measure of variability), to the scrutiny of a repeated measures ANOVA design. We found that species turnover and cluster variation did not differ signi®cantly between treatments. We attribute the lack of any effect to a large number of common agricultural species which are never eliminated from a habitat, but are instead signi®cantly reduced. Re- duction rather than elimination does not cause the spider communities within these plots to turn over any faster than the control. However, like most other animal communities, the spider community did turn over and change in structure and composition through the season, regardless of treatment. Using Spearman rank correlations, we found that this within-season species turnover is related to the decline in vegetation height and the increase in percentage dead vegetation cover in the ®eld margin. Keywords: Glyphosate, herbicide, spiders, species turnover, DECORANA, ®eld margins Field margins play an important agricultural 1991; Feber et al. 1996; Haughton et al. role in providing a refuge for bene®cial in- 1999a,b). This detrimental effect on non-tar- vertebrate predators (e.g., Araneae, some Car- get invertebrates following an experimental abidae; Staphylinidae; Heteroptera) facilitat- spray application of herbicide simulates what ing movements of invertebrates into the crop may happen when spray is allowed to drift (e.g., Duelli et al. 1990). Data from herbicide- onto non-target areas. Drift may be a product treated and untreated cereal headlands suggest of operator error or a sudden increase in wind that butter¯ies, carabid beetles, Auchenorrhy- speed and in either of these situations, the cha and Heteroptera (Hemiptera) are detri- spray is likely to become misplaced and affect mentally affected by spray applications, but to ®eld margins and adjacent semi-natural habi- differing degrees (e.g., Chiverton & Sotherton tats. Recent evidence suggests that spider num- 1 Current address: Department of Entomology and Nematology, IACR-Rothamsted, Harpenden, Hert- bers are likely to be signi®cantly affected even fordshire. AL5 2JQ, UK. by a relatively low rate of herbicide applica- 2 Current address: Central Science Laboratory, tion (Baines et al. 1998; Haughton et al. Sand Hutton,York, YO41 1LZ, UK. 1999c). This effect, even at low rates, may 288 BELL ET AL.ÐTHE EFFECT OF GLYPHOSATE ON SPIDER COMMUNITIES 289 have detrimental implications for both ®eld Couch-grass (Elymus repens (L.)). Eight rep- margin biodiversity and bio-control programs licates of four treatments, 90 g, 180 g and 360 which use bene®cial spiders to control pests. g a.i. glyphosate ha21 (Roundup Biactive, In the context of a rapid increase in worldwide Monsanto, High Wycombe, Berkshire) and an demand for glyphosate when, for example, 70 unsprayed control, were randomly assigned million hectares of land worldwide were along the ®eld margin. Glyphosate was ap- sprayed in 1997 (Woodburn 2000), it is easy plied to these plots at a volume rate of 200 to demonstrate a need for a clearer under- litres ha21 and a pressure of 2.5 bar using an standing of the potential effect on spiders and Oxford Precision Sprayer ®tted with ¯at fan other non-target invertebrates. nozzles on 30.v.1997, during dry and calm The properties of glyphosate (N-(phosphon- conditions (24 8C, RH 55%, wind speed ,1 omethyl)glycine), an exceedingly effective but ms21). slow-acting broad spectrum herbicide, are The 1998 margin was dominated by False well known. The herbicide acts by inhibiting Oat-grass (A. elatius (L.)) and Yorkshire Fog the biochemical pathway in plants (i.e., 5-en- (Holcus lanatus (L.)). Eight replicates of four olpyruvylshikimate 3-phosphate synthase) by treatments were assigned in a randomized blocking the production of aromatic amino ac- block design: 360 g, 720 g and 1440 g a.i. ids thus restricting protein synthesis and pho- glyphosate ha21 (Roundup Biactive, Monsan- tosynthetic activity (Bayliss 2000). It is used to, High Wycombe, Berkshire) suspended in in a range of agricultural (particularly cereals), water and an unsprayed control. Glyphosate industrial and domestic situations to control was applied to the plots on the 4.vi.1998 dur- grasses and other weeds (Woodburn 2000). ing dry, calm conditions (17.5 8C, RH 84.5%, However, the toxicological effect on inverte- wind speed ,2ms21) with the same equip- brates is little understood except to state that ment, volume rate and pressure as that de- the herbicide is classi®ed as `harmless' to spi- scribed in 1997. ders and a range of other common non-target Data collection.ÐSpiders were sampled invertebrates by The Society of Environmen- using a modi®ed garden-vac (g-vac) (Ryobi tal Toxicology and Chemistry (Europe) (Bar- RSV3100E: engine capacity 31 cm3 with a rett et al. 1994) nozzle size 13 cm). The spider samples from In this paper we investigated the within- each experimental plot comprised 10 sub-sam- season effect of incremental levels of gly- ples of 30 second sucks at 1 m intervals along phosate application (six levels from 90±1440 each experimental plot. Sampling was done on g active ingredient (a.i) glyphosate ha21 with the central 10 m of each plot to avoid edge a control) on ®eld margin spiders from a com- effects from neighboring treatments: the total munity perspective. sampling area per plot approximated to 0.13 m2. Each sample of spiders was emptied from METHODS the g-vac into a plastic bag, extracted with an Study sites.ÐThe ®eld research was based aspirator into 70% alcohol and then identi®ed at the Allerton Research and Educational Trust to species level. Estate, Loddington, Leicestershire, UK (grid Two measures of vegetation structure were reference: SK 789015). We spread the effort taken. Percentage ground cover of dead veg- of conducting such a large experiment over etation in the experimental plots was recorded two years between 1997±1998. Two ®eld mar- using permanent 0.25 m2 quadrats and, aver- gin study sites were used which were sepa- age vegetation height at ®ve positions (as in rated by a minor road but were no more than a domino-5) within the quadrats was recorded 20 m apart. Both sites had an adjacent dense to the nearest cm. Three quadrats were posi- uncut Hawthorn (Crataegus monogyna Jacq.) tioned at 3 m, 6 m and 9 m within each of and Blackthorn (Prunus spinosa L.) hedge the 32 plots and mean percentage dead vege- running along their length. The experimental tation cover and mean vegetation height. Spi- plot size was the same in both years: ®eld der and vegetation sampling was done month- margins were divided into 32 contiguous ly between May±October inclusive, to plots, each measuring 12 m long 3 2 m wide. monitor any changes over the season. The 1997 margin was dominated by False Data analyses.ÐThere are many ways of Oat-grass (Arrhenatherum elatius (L.)) and calculating species turnover, but most index- 290 THE JOURNAL OF ARACHNOLOGY type methods which have traditionally been timately, these Euclidean distances indicate used do not take account of the community the level of species stability (i.e., high or low dynamics as they fail to retain all the infor- rates of turnover) between treatments. mation from the species matrix. However, We then calculated the average Euclidean multivariate statistics have been suggested as distance between all points within the same an inclusive technique which does not over- treatment for each of the months from May± simplify the dynamic nature of the community October inclusive (n 5 672) using the DCA (Williamson 1987). We introduce a simple axis 1 and 2 scores for each year (i.e., we method of calculating species turnover while generated a distance matrix for each treatment retaining most of the ecological information for each month). This approach would indi- from the data matrix. Using DECORANA cate whether the size of the cluster varied be- (DEtrended CORrespondence ANAlysis or tween treatment. The size of the cluster DCA for short), a widely available package equates to a measure of community variation; designed speci®cally for ecological studies to large clusters have more variation in the spe- avoid distortions caused by either the arch or cies complex than small ones. horseshoe effects (Hill 1994), P values are at- Univariate repeated measures, with date as tached to the turnover rates in DCA-Euclidean the within-subject factor and treatment as the space using ANOVAs. This is an extension of main effect, were used to analyze differences Hill's (1994) approximation of the standard in species turnover (i.e., distance moved in deviation of species turnover along the x-axis.