Comparing methods to evaluate the effects of Bt maize and insecticide on spider assemblages
Introduction
The European corn borer Ostrinia nubilalis Hübner (Lepidoptera) is a major pest of maize worldwide (Krattinger, 1997). Chemical insecticides, such as pyrethroids, are widely used to control this and other pests in conventional agriculture. In organic farming, formulations containing Cry1A(b) protein of Bacillus thuringiensis (Bt) ssp. kurstaki de Barjac & Lemille, toxic to lepidopteran larvae, have been applied successfully for several decades (Glare and O’Callaghan, 2000). As a new means of crop protection, genetically modified (GM) maize expressing the Cry1A(b) toxin (Koziel et al., 1993) has been made available commercially in several countries (James, 2002). However, many countries (e.g., the EU member states) are still in the assessment and decision process whether or not Bt maize and other GM crops should be cropped on a large scale.
Plant protection methods usually not only reduce the target pest, but influence the community of non-target organisms in a direct or indirect way. Chemical broad-spectrum insecticides have severe effects on many groups of non-target arthropods, including spiders (e.g., Krause et al., 1993, Reed et al., 2001, Candolfi et al., 2004, Duan et al., 2004). On the other hand, Bt sprays are widely considered as safe for spiders and other beneficial insects (e.g., Glare and O’Callaghan, 2000, Reed et al., 2001, Duan et al., 2004). However, sprayed insecticides remain on the plant surface and have a temporarily limited range of action, as they are sensitive to UV radiation and washed off by rainfall. In contrast, Bt maize expresses the toxin over the whole growing season in all green tissues and pollen. A truncated, partly activated form of the toxin is produced, shortcutting the activation process necessary for toxicity of Cry proteins in Bt formulations (Koziel et al., 1993). Furthermore, the expressed Cry1A(b) protein might be altered by the complex of plant enzymes. Thus, Bt sprays cannot be compared directly to Bt crops and a wider range of effects is potentially possible.
Generalist predators and especially spiders belong to the most abundant invertebrate predators in agroecosystems and play an important role in biological pest control in many crops including maize (e.g., Lang et al., 1999, Marc et al., 1999, Symondson et al., 2002, Lang, 2003). Thus, any negative effect on spider populations has potential consequences for biological control. Spiders are likely to be exposed to Cry1A(b) toxin in Bt maize fields over the whole season as they are known to prey on herbivores (Nyffeler, 1999, Kiss et al., 2003), and herbivores feeding on Bt maize tissue are likely to ingest and pass on the toxin to predators (e.g., Dutton et al., 2002). Furthermore, spiders are likely to be exposed especially during anthesis in Bt maize cultivars expressing high toxin concentrations in pollen such as event 176 (Fearing et al., 1997, Lang et al., 2004). Spiders may forage for pollen actively (Vogelei and Greissl, 1989, Ludy, 2004), ingest pollen when recycling their webs (Smith and Mommsen, 1984), or when their prey has collected or consumed pollen or is dusted with it (Gregory, 1989).
In ecological studies and concurrent risk evaluations of Bt maize concerning spiders, there is a lack of data with regard to three points: (1) baseline data of spider assemblages in European maize fields (Nyffeler and Sunderland, 2003), (2) effects of Bt plants on spider assemblages in relation to common plant protection practice and (3) knowledge of adequate sampling methods for plant-dwelling spiders in maize. All three aspects are fundamental for a risk assessment of and monitoring scheme for present and future cultivars of transgenic maize in Europe. In tiered risk assessment procedures suggested by Poppy and Sutherland (2004) and Dutton et al. (2003), laboratory and semi-field studies are performed to assess potential hazard and exposure for certain indicator species. Additionally, field experiments are important to detect consequences of new GM crops in the environment (Poppy and Sutherland, 2004, Andow and Hilbeck, 2004). Comparing side effects of a new transgenic cultivar to common agricultural practice should be the basis for a decision whether it is an improvement or not (Hails, 2000).
After a GM crop has passed the pre-market risk assessment, regulators usually demand general surveillance over several years accompanying commercial production to ensure long-term environmental safety and sustainability (e.g., EU Directive 2001/18/EC, European Parliament and Council, 2001). Suitable and adequate sampling methods are a requirement for a quantitative and standardized survey of non-target species compositions. Four common methods for sampling plant-dwelling spiders in the field were therefore compared, i.e., stem eclector, beating sheet, suction sampling and plant removal.
The present study aimed to assess and compare the potential effect of Bt maize on plant-dwelling spider assemblages during one season in Bt maize to those in untreated conventional maize and to pyrethroid treated plots and addressed the following questions: How is the plant-dwelling spider community of maize fields composed? Does the community of plant-dwelling spiders differ between insecticide treated and untreated plots? Does the community of plant-dwelling spiders differ between Bt maize fields and fields of a control line? Is the effect of Bt maize different from the effect of insecticide treatment? Which is the most efficient method for monitoring potential effects on plant-dwelling spiders?
Section snippets
Material and methods
The study was carried out between 1 July and 25 September 2001 in maize fields of four state research farms in Bavaria, South Germany. The farms were situated between 366 and 550 m a.s.l., the mean temperature at 2 m above ground during the experimental period was between 15.9 and 16.4 °C and the average rainfall ranged from 224 to 316 mm. The fields were managed, fertilized, herbicide treated and sown according to standard practice (sowing end of April/beginning of May, herbicide treatment
Results
A total of 29 species were identified in 32 genera and 14 families (Table 1). In terms of ecological guilds (Uetz et al., 1999), most spiders were web builders (95.5%). Space web builders (Theridiidae, Dictynidae) dominated (52.9%), followed by orb weavers (Araneidae and Tetragnathidae, 25.5%) and tangle weavers (Linyphiidae, 17.1%). Theridiidae (52.8% of all individuals) dominated the catches, followed by Tetragnathidae (18.6%), Linyphiidae (17.1%) and Araneidae (6.8%). The proportion of adult
Discussion
The spider families recorded in the studied fields generally dominate agroecosystems throughout Europe (Luczak, 1979, Barthel, 1997, Nyffeler and Sunderland, 2003). Spider assemblages consisted mainly of juveniles and small web building spiders, which is in accordance with other studies (Nyffeler et al., 1994, Marc et al., 1999, Ludy and Lang, 2004). Altogether 38 species were distinguished (29 identified to species level). Erigone atra, Oedothorax apicatus, Theridion impressum and Tetragnatha
Acknowledgements
This project was financially supported by the Federal Ministry of Education and Research (BMBF 0312631A). We thank Bettina Spindler, Sandra Bössow and Marek Tkaczyk for their assistance in sampling, Theo Blick and Claudia Ludy for their advice on spider identification, Gabor Lövei and two anonymous referees for valuable comments on the manuscript, and Wilfried Gabriel for fruitful discussions.
References (54)
Genetically modified plants—the debate continues
Trends Ecol. Evol.
(2000)- et al.
Predation by ground beetles and wolf spiders on herbivorous insects in a maize crop
Agric. Ecosyst. Environ.
(1999) - et al.
Spiders (Araneae) useful for pest limitation and bioindication
Agric. Ecosyst. Environ.
(1999) - et al.
Composition, abundance and pest control potential of spider communities in agroecosystems: a comparison of European and US studies
Agric. Ecosyst. Environ.
(2003) - et al.
Science-based risk assessment for non-target effects of transgenic crops
BioScience
(2004) Traps for cave inhabiting insects
J. Elisha Mitchell Sci. Soc.
(1931)Einfluss von Nutzungsmuster und Habitatkonfiguration auf die Spinnenfauna der Krautschicht (Araneae) in einer süddeutschen Agrarlandschaft. Agrarökologie 25
(1997)- et al.
Analysis of the most popular techniques for sampling spiders in large-scale ecological experiments in grasslands
Newsl. Br. Arachnol. Soc.
(2001) - et al.
A faunistic approach to assess potential side effects of genetically modified Bt-corn on non-target arthropods under field conditions
Biocontrol Sci. Technol.
(2004) - et al.
A new method for sampling arthropods using a suction collecting machine and a modified Berlese funnel separator
J. Econ. Entomol.
(1959)
Effects of Bt transgenic and conventional insecticide control on the non-target natural enemy community in sweet corn
Effects of transgenic Bacillus thuringiensis potato and conventional insecticides for Colorado potato beetle (Coleoptera: Chrysomelidae) management on the abundance of ground-dwelling arthropods in Oregon potato ecosystems
Environ. Entomol.
Uptake of Bt-toxin by herbivores feeding on transgenic maize and consequences for the predator Chrysoperla carnea
Ecol. Entomol.
Assessing the risk of insect resistant transgenic plants on entomophagous arthropods: Bt-maize expressing Cry1Ab as a case study
Biocontrol
Gpower: A Priori, Post Hoc and Compromise Power Analysis for MS-DOS [Computer Program]
Quantitative analysis of CryIA(b) expression in Bt maize plants, tissue, and silage and stability of expression over successive generations
Mol. Breeding
Field-evaluation and potential ecological impact of transgenic cottons (Gossypium hirsutum) in Australia
Biocontrol Sci. Technol.
Bacillus thuringiensis: Biology, Ecology and Safety
Field observations of Gasteracantha cancriformis (Araneae Araneidae) in a Florida mangrove stand
J. Arachnol.
Spinnen Mitteleuropas
Ein handliches Vakuumsammelgerät für die Erfassung von Spinnen und Insekten
Arachnol. Mitt.
Mais—Unkräuter, Schädlinge, Krankheiten
Select non-target arthropod abundance in transgenic and non-transgenic field crops in Ohio
Environ. Entomol.
Test systems to determine the ecological risks posed by toxin release from Bacillus thuringiensis genes in crop plants
Mol. Ecol.
Bt-corn: impact on non-targets and adjusting to local IPM systems
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Present address: Institute of Environmental Geosciences, Department of Geosciences, University of Basel, Bernoullistrasse 30, CH-4056 Basel, Switzerland.