Journal of Environmental Science and Health Part B (2007) 42, 279–286 C Taylor & Francis Group, LLC Copyright ! ISSN: 0360-1234 (Print); 1532-4109 (Online) DOI: 10.1080/03601230701229239
Ecological effects of imidacloprid on arthropod communities in and around a vegetable crop 1 ´ FRANCISCO SANCHEZ-BAYO , HANAE YAMASHITA2 , RYU OSAKA1 , MASAHIRO YONEDA3 and KOUICHI GOKA3 1
Faculty of Horticulture, Chiba University, Matsudo, Japan Graduate School of Agriculture and Life Sciences, Tokyo University, Tokyo, Japan 3 National Institute for Environmental Studies, Tsukuba, Ibaraki, Japan 2
To elucidate the ecological impacts of imidacloprid [1-(6-chloro-3-pyridylmethyl)-N-nitroimidazolidin-2-ylideneamine] on vegetable crops and their surrounding areas, arthropods on eggplant patches treated with this insecticide were monitored throughout two cultivation seasons, spring and autumn, and the results compared with those of control crops. Residues of imidacloprid in soil accounted for 4-8% of total applied, and concentrations outside the crop were always below 5 µg/kg. Communities of the crop vegetation experienced significant density reductions, mostly of aphids, and had fewer species diversity during the first month. Those in the surrounding pasture were similarly affected though with less intensity, while non-target ground arthropods both inside and outside the crop only showed significant impacts in the two weeks after planting. Keywords: Neonicotinoid insecticides; eggplant; non-target organisms; biodiversity.
Introduction Imidacloprid [1-(6-chloro-3-pyridylmethyl)-Nnitroimidazolidin-2-ylideneamine] is a neonicotinoid systemic insecticide used worldwide in a variety of crops. Because of its powerful activity, it is usually applied to plant seedlings and roots of plants as granular formulation at very low concentrations. Sucking pest (e.g. aphids and most Hemiptera species) and borer larvae in particular, are effectively controlled by systemic insecticides such as imidacloprid, since the active ingredient is stored in the plant tissues for two or three months[1] , thus providing lasting protection against pests with a minimal chemical input in the initial stages of the crop. However, the same efficacy displayed with pests species affects other non-target arthropods such as honey bees[2,3] , natural predators[4] and invertebrates living in agricultural ecosystems or their surroundings.[5] Indeed, previous studies on rice mesocosms treated with imidacloprid suggest that the ecology of aquatic environments is deeply disturbed for a period of two months[6,7] , which corresponds to the period of activity of this insecticide.
Address correspondence to Francisco Sanchez-Bayo; E-mail:
[email protected] Received October 30, 2006.
Given the solubility and stability of imidacloprid in soil[8] , and consequently its leaching potential[9] , it is likely that its residues could move and spread around the soil and be eventually taken up by weeds growing in the vicinity of the treated crops, in which case they would affect nontarget species and alter the arthropod biodiversity of the surrounding vegetation.[10] Although translocation of imidacloprid between treated plants and soil, and its distribution in the latter media, has been studied previously[1,11] , currently there is no evidence that residues in soil may affect negatively the ecology around the treated crops. In fact, because no spraying is required for its application, imidacloprid is acclaimed as one of the most environmentally safe insecticides, which explains its rapid adoption in pest control all over the world.[12] Some recent studies[13] have questioned to what extent the diffusion of imidacloprid residues in soil may affect underground as well as ground-surface communities of insects, their larvae, spiders, worms, snails and other invertebrate fauna susceptible to this insecticide. After all, a healthy soil community is essential to ensure the recycling of organic matter and guarantee a sustainable supply of nutrients to the vegetation, be crops or wild plants.[14] In this context, the present study aimed at monitoring the ecological impacts of imidacloprid on arthropod communities of a typical vegetable crop in Japan: eggplant. Insects and spiders found in the crop, whether on plants or
S´anchez-Bayo et al.
280 ground, and surrounding vegetation were monitored under standard farming conditions on two different seasons— spring and autumn—and the impacts compared to control (untreated) plots using a variety of techniques. Effects of imidacloprid in and outside the treated crops are required mainly for a thorough evaluation of risks of this insecticide in the context of biodiversity conservation and ecosystem protection.[15] This paper represents a second stage of a larger project designed to study the changes in ecosystems derived from the use of agrochemicals.
Soil samples were analyzed for imidacloprid residues at the certified analytical laboratories of RIKEN Institute in Utsunomiya (Tochigi Prefecture). The method of Baskaran et al.[17] was followed for extraction of residues, using Liquid Chromatography coupled with Mass Spectrometry (Shimadzu LC/MS-2010EV) for their identification and quantification. The limit of detection in the samples was 0.01 µg/kg dry weight. Precipitation and relevant weather data (i.e. air temperature and humidity) were recorded on site throughout the entire experimental period.
Materials and methods
Data analysis
The experimental area was located in Tsukuba, eastern Japan (36◦ N, 140◦ E), and consisted of four small eggplant plots (16 m2 ), each of which had 64 eggplant seedlings planted on May 17, 2006 (spring crop) and 75 seedlings on August 29 of the same year (autumn crop). Two plots were treated with granular Admire (1% imidacloprid) at such times, by placing the granules (1 g) in the hole while the seedling was planted, and then covered with soil; planting depth was approximately 10 cm. Two more plots were planted with the same crop but without any insecticide treatment, to be kept as controls. Crops were harvested after two months, on July 27 and November 5, respectively. Around each plot, a 4-m wide buffer area of clover pasture and weeds (128 m2 ) was established for monitoring the movement and possible effects of imidacloprid residues on arthropod communities outside the eggplant patch.
Changes in the abundance of arthropods within the respective communities were compared between treated and control plots to evaluate the impact of the insecticide, using t-tests on the log-transformed data of particular dates, and paired t-tests on the time series to identify significant differences.[6] Ecosystem indicators, such as Shannon’s diversity and Czenakowski (Sorenson) similarity indices, and multivariate techniques (Principal Components Analysis, PCA) were also used to identify community trends with time[18] both inside and outside the crop. For the latter analysis, densities were transformed using the natural logarithm of the original counts.[19]
Results and discussion Imidacloprid residues in soil
Monitoring and sampling Both treatment and control areas were monitored weekly throughout the two-month period of each growing season. Monitoring included: (i) visual census of all arthropods found on the crop; individual specimens were taken for later identification in the laboratory to the lowest taxon possible, although in many cases this was only feasible to family level; (ii) sampling of arthropods on the buffer area using a sucking device (30 cm diameter) over 5 random spots; (iii) sampling of ground arthropods using pitfall traps set within the crop (5 traps, each covering 7 m2 ) and its surrounding buffer area (8 traps, each covering 14 m2 ); traps were plastic cups set in the ground, and data thus collected represent total number of arthropods caught in weekly periods. To study the movement of imidacloprid in the soil, composite soil samples[16] (8 scoops, 10 cm depth) were taken within the treated plots, and along the perimeter outside them at 1 and 4 m from the edge of the crop. Samples were taken at 2 days, 1 week, 2 weeks, 1 month and 2 months after application, to study also the dissipation of residues with time.
Residues of imidacloprid in soil of the treated plots of the spring crop increased constantly from the day of planting onwards, reaching its highest concentration (10 µg/kg) two months later. Very small amount of chemical, less than 2%, moved outside the crop area during that period, with concentrations at 1 m being a quarter of those found inside the treated plot, while residues found at 4 m from the edge of the plot were forty times lower than inside the crop soil at the time of maximum spread (Table 1). Overall, no more than 4.2% of the active ingredient applied remained in the soil at the time of harvest, of which 57% were found under the crop itself and the remainder was scattered around it. Although most of the insecticide active ingredient was supposedly taken up by the eggplants[1] , a considerable amount may have been washed down the soil profile[9] due to the intense rainfall that took place throughout the experimental period, particularly between mid-June till late July—tsuyu season in Japan—when 332 mm of rain fell on site (Table 1). The highest imidacloprid residues in soil of the autumn crop were measured two weeks after planting (39.6 µg/kg representing 7.6% of total applied), and decreased later to about half that concentration, possibly as a result of the 425 mm of rainfall that washed the soil during the typhoon
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Table 1. Residues of imidacloprid in soil (µg/kg dry weight) and precipitation (mm) during both cultivation periods. Figures in brackets are percentage of applied amounts. Outside Date
Days from planting
Inside crop
1m
4m
Precipitation
19-5-06 23-5-06 30-5-06 13-6-06 25-7-06
2 6 13 27 69
0.19 (0.04%) 0.05 (0.01%) 2.78 (0.62%) 2.99 (0.67%) 10.37 (2.33%)
0.02 (0.01%) 0.01 (
