Diversity and Seasonal Phenology of Aboveground Arthropods in Conventional and Transgenic Maize Crops in Central Spain

Available online at www.sciencedirect.com Biological Control 44 (2008) 362–371 www.elsevier.com/locate/ybcon Diversity and seasonal phenology of aboveground arthropods in conventional and transgenic maize crops in Central Spain Gema P. Farino´s, Marta de la Poza 1, Pedro Hernańdez-Crespo, Fe´lix Ortego, Pedro Castan˜era * Centro de Investigaciones Biolo´gicas, CSIC, Ramiro de Maeztu 9, 28040 Madrid, Spain Received 20 July 2007; accepted 27 November 2007 Available online 7 January 2008 Abstract One of the major concerns regarding the release of Bt maize is its potential negative impact on non-target organisms present in this crop. In this paper, we compare the temporal phenology and community structure of the aboveground arthropods in commercial Bt maize fields in Central Spain with those of conventional maize crops, with or without an insecticide (imidacloprid) seed treatment, over a period of three years. Spiders, harvestmen, centipedes, ground beetles, rove beetles, carrion beetles, click beetles, earwigs and damsel bugs were captured in pitfall traps every year in sufficient number to provide meaningful phenological data. One predator spider and three omnivorous species of ground beetles have been consistently present in the maize fields: Pardosa occidentalis, Poecilus cupreus, Pseudophonus rufipes and Pseudophonus griseus, respectively. Rove beetles were caught to a lesser extent, with three dominant species: Acrotona aterrima, Philonthus varians and Platystethus nitens. The variability in activity–density patterns of the aboveground fauna was mainly influenced by the year, but no detrimental effects could be attributed to Bt maize. The only exception being the changes detected in rove beetles, although these differences were transitory and varied from year to year. No changes in species richness and diversity indices for spiders and ground beetles resulted from treatments. However, imidacloprid-treated maize caused a reduction in species richness of rove beetles, even though the abundance of the main species was not reduced. Our results suggest that Bt maize could be compatible with natural enemies that are common in maize fields in Spain. Ó 2007 Elsevier Inc. All rights reserved. Keywords: Bt maize; Non-target arthropods; Spiders; Pardosa occidentalis; Ground beetles; Rove beetles; Platystethus nitens 1. Introduction Sesamia nonagrioides (Lefebvre) (Lepidoptera: Noctuidae), and the European corn borer, Ostrinia nubilalis (Hu¨bner) The use of genetically engineered insect-resistant plants (Lepidoptera: Crambidae). The first event commercialised, in agriculture has currently become a powerful tool provid- Bt 176 (var. Compa CB, Syngenta), was grown from 1998 ing an effective control of some key pests. The planting of to 2005. A mean surface of about 20,000–25,000 ha of Bt transgenic maize expressing Cry1Ab toxin from Bacillus maize (5% of the total maize growing area) was cultivated thuringiensis (Bt), an insecticidal toxin-specific to certain between 1998 and 2002, increasing to 50,000–60,000 ha lepidopteran species, was approved in Spain in 1998 to con- (around 12–15%) in the following years with the introduc- trol two major pests: the Mediterranean corn borer, tion of new hybrids derived from the event MON810 (http://www.mapa.es/es/agricultura/pags/semillas/estadist- * icas.htm). The high specificity of Bt maize and the reduc- Corresponding author. Fax: +34 91 536 04 32. tion of insecticides used to control corn borers will likely E-mail address: [email protected] (P. Castan˜era). 1 Present address: Centro Nacional de Biotecnologıá, CSIC, Canto- result in a more favourable environment for natural ene- blanco, 28049 Madrid, Spain. mies. However, laboratory and field studies have warned 1049-9644/$ - see front matter Ó 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2007.11.007 G.P. Farino´s et al. / Biological Control 44 (2008) 362–371 363 about adverse effects on non-target organisms exposed to 2. Materials and methods the insecticidal toxin (Hilbeck et al., 1998; Losey et al., 1999; Harwood et al., 2005; Pilcher et al., 2005). Subse- This study was conducted in a commercial maize field in quently, a debate about the possible detrimental conse- the province of Madrid (Central Spain), over three consec- quences of the deployment of Bt maize on non-target utive years, from 2000 to 2002. The planting dates were arthropods has intensified in recent years, and different 13th April 2000, 19th April 2001 and 9th April 2002. The approaches have been put forward to deal with the assess- three different treatments, contrasted by a randomized ment of this environmental risk (Wolfenbarger and Phifer, block design with three replicates each, were: Bt maize 2000; Conner et al., 2003; Lo¨vei and Arpaia, 2005; Romeis hybrid, Compa CB (Cry1Ab toxin, Event 176; Syngenta et al., 2006; Andow and Zwahlen, 2006). Seeds SA) (Bt+); the isogenic Dracma (Syngenta Seeds Two of the most important components of the ground SA) (BtÀ) and Dracma with imidacloprid insecticide dwelling fauna in farming systems are ground beetles and seed-treatment (ImBtÀ). In this latter treatment, which is spiders (Melnychuk et al., 2003; De la Poza et al., 2005). relatively common in this area for soil and other insect pest Both groups have proved to be beneficial for the control control, the seeds were dressed at 1400 cc of imidacloprid of agricultural pests (Riechert and Lockley, 1984; Kielty (Gaucho 35 FSÒ, Bayer) per 100 kg of seed (4.9 g a.i/kg). et al., 1999; Sunderland, 1999; Lang et al., 1999). Fur- The surface of each block ranged between 0.5 and 0.6 ha, thermore, they contribute to the faunal diversity of agri- with corridors between them and an external border 2– culture landscapes (Booij and Noorlander, 1992). As Bt 5 m wide, depending on the availability of land each year. plants express the insecticidal protein during the whole The fields were maintained according to conventional local season, potential exposure of predators via prey feeding farming practices, but without spraying insecticide. In all on Bt plants may be increased in comparison with Bt plots a postemergence herbicide mixture of 75% isoxaflu- sprays. Different ways have been reported for non-target tol + 47.5% atrazine (Spade + Atrazinax Flo, Rhoˆne Pou- arthropods to come into contact with insecticidal toxins lenc, France) at 5–6 l/ha was sprayed soon after sowing. produced in transgenic plants: by feeding on plant parts Aboveground arthropods were sampled by using pitfall themselves, through feeding on target or non-target her- traps. Each trap consisted of a plastic cup 12.5 cm in diam- bivorous insects, or via the environment, i.e. the soil eter and 12 cm deep with a plastic funnel fitted inside its when toxins persist and do not lose their toxicity after upper rim, and both flush with the ground surface. Under plant parts or insects have died (Groot and Dicke, the funnel and inside the plastic cup, a plastic container of 2002; Zwahlen et al., 2003). Bt toxins are also released 150 cc (Resopal, Madrid), where the insects fell, was half into the rhizosphere in root exudates from Bt maize filled with a 3:1 mixture of water and ethanol. The outer (Saxena et al., 1999; Saxena and Stotzky, 2001), most cup was punched to let the irrigation water drain off. Five likely producing greater concentrations in the soil than traps per plot were placed diagonally across each plot, if they were only incorporated through normal plant starting at least 6 m from the field boundary to minimize dynamics. potential edge effect. Traps were operative for 3 days every The implication of Bt toxin exposure on the perfor- 2 weeks and the sampling period lasted from mid-June to mance of non-target arthropods is still not clear in the the end of September, giving a total of eight sampling dates case of long-term exposure occurring in the field, so field per year. The number of arthropods captured in pitfall studies can be useful in identifying the overall effect on traps is a function not only of the density, but also of the non-target arthropods. As part of a Spanish post-market activity of the sampled organisms and their behavior on environmental monitoring plan for the Bt maize hybrid encountering a trap. Hence, the term ‘‘activity–density’’ is Compa CB (Event Bt176), a three-year farm field study used to refer to population estimates obtained using pitfall was initiated to assess the potential impact of Bt maize traps. The arthropods collected were categorized by order on predatory arthropods. The effect of Compa CB on and family in all groups, and by genus and species in the the abundance of non-target arthropods was studied in predominant groups. Richness and a- and b-diversity indi- two Spanish locations from 2000 to 2002 (De la Poza ces were calculated for the predominant groups collected, et al., 2005). Araneae (spiders), Carabidae (ground bee- namely, spiders, ground beetles and rove beetles. The tles) and Staphylinidae (rove beetles) were the most Shannon–Wiener a-diversity index (H0) was computed to abundant groups collected by pitfall traps. Their abun- detect changes in the community structure of the predom- dance varied from year to year and between locations, inant groups among the three different treatments. This but no clear tendencies relating to Bt maize were index is based on the proportional abundance of species recorded when compared with the isogenic cultivar with and is thus affected by species richness, and was calculated or without imidacloprid seed treatment. using the following formula (Magurran, 1989): The present study enlarges on that of De la Poza et al. X 0 (2005) by focusing on the effects of Bt maize on species H ¼ pi ln pi richness, diversity and seasonal phenology of ground dwelling arthropods present in maize crops in Central pi being the proportion of individuals found in the ith spe- Spain.

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