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A risk assessment of genetically modified organisms [Elektronische Ressource] : potential effects of Bt maize on spiders / vorgelegt von Claudia Ludy

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A risk assessment of genetically modified organisms: Potential effects of Bt maize on spiders As our circle of knowledge expands, so does the circumference of darkness surrounding it. Attributed to Albert Einstein A risk assessment of genetically modified organisms: Potential effects of Bt maize on spiders Dissertation zur Erlangung des akademischen Grades eines Doktors der Naturwissenschaften (Dr. rer. nat.) am Fachbereich Biologie/Chemie der Universität Bremen vorgelegt von Claudia Ludy Freising, November 2005 Gutachter der Dissertation: Prof. Dr. Juliane Filser, Universität Bremen Prof. Dr. Thomas Hoffmeister, Universität Bremen Tag des öffentlichen Kolloquiums: 20. Dezember 2005 im Zentrum für Umweltforschung und Umwelttechnologie (UFT) der Universität Bremen. Acknowledgements First of all, I am very grateful to Dr. Andreas Lang, my tutor and co-autor of the publications, on which this thesis is based. Due to his scientific advice, inspiration, patience and moral support I was able to conduct and finish this thesis. Furthermore, I thank the referee Prof. Dr. Juliane Filser who made it possible to complete this thesis at the University of Bremen and helped me with administrative subjects. I thank the co-referee Prof. Dr. Thomas Hoffmeister for his interest in my work and his time for referring my thesis.

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Published 01 January 2005
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A risk assessment of

genetically modified
organisms:

Potential effects of
Bt maize on spiders




As our circle of knowledge expands,
so does the circumference of darkness surrounding it.

Attributed to Albert Einstein


A risk assessment of genetically
modified organisms:


Potential effects of Bt maize on
spiders


Dissertation


zur
Erlangung des akademischen Grades eines Doktors der
Naturwissenschaften

(Dr. rer. nat.)

am Fachbereich Biologie/Chemie der
Universität Bremen



vorgelegt von Claudia Ludy


Freising, November 2005



















Gutachter der Dissertation: Prof. Dr. Juliane Filser,
Universität Bremen

Prof. Dr. Thomas Hoffmeister,
Universität Bremen


Tag des öffentlichen Kolloquiums: 20. Dezember 2005
im Zentrum für Umweltforschung und
Umwelttechnologie (UFT) der Universität
Bremen.




Acknowledgements

First of all, I am very grateful to Dr. Andreas Lang, my tutor and co-autor of the publications, on
which this thesis is based. Due to his scientific advice, inspiration, patience and moral support I was
able to conduct and finish this thesis.

Furthermore, I thank the referee Prof. Dr. Juliane Filser who made it possible to complete this thesis at
the University of Bremen and helped me with administrative subjects.

I thank the co-referee Prof. Dr. Thomas Hoffmeister for his interest in my work and his time for
referring my thesis.

PD Dr. Broder Breckling, Susanne Pfeffer, Jana Seeger, and Prof. Dr. Martin Diekmann kindly
contributed to the examination board of this thesis.

I thank Juliane Filser, Andreas Lang, Silke Vetter and Volker Weiß for reading and commenting
earlier drafts of the general part of this thesis.

Horst Vetter kindly corrected the English.

PD Dr. Klemens Ekschmitt, Dr. Michaela Hirsch, René Kristen, Prof. Dr. Wolfgang Nentwig, Dr.
Martin Nyffeler, Dr. Stano Pekár, Dr. Hauke Reuter, Silke Vetter, Volker Weiß and Dr. Samuel
Zschokke I thank for reading and commenting earlier drafts of the manuscripts of this thesis.

I am grateful to Klemens Ekschmitt for statistical support and to Theo Blick for confirming the
identified spider species.

I thank Prof. Dr. Volkmar Wolters and the working group of the Department of Animal Ecology at the
University of Gießen, the working group of the Department of General and Theoretical Ecology at the
University of Bremen as well as Prof. Dr. Hannes Kaatz and the Molecular Ecology Research Group
at the University of Halle for scientific advice, especially for fruitful discussions on presenting talks on
my work.

Dr. Ullrich Benker, Holger Damczyk, Alfonso Devilli, Sonja Gubo, Michael Meissle, Hannes
Scheuerer, Robert Schrader, Sandra Schüchen, Bettina Spindler, Marec Tkaczyk, Eva Vojtech and
Barbara Zeilmaier supported me in field and laboratory work.

Last but not least, I thank Volker Weiß for his backup and appreciation which fascilitated the
realisation of this thesis considerably.

The investigations of this thesis were conducted in laboratories and experimental farms of the
Bavarian State Research Center for Agriculture. This study was financially supported by the German
Federal Ministry of Education and Research (BMBF 0312631A) and the Bavarian State Ministry for
Environment, Health and Consumer Protection (Az. 76a-8793-1999/15).






Table of Contents
Page
GENERAL PART 1
SUMMARY / ZUSAMMENFASSUNG 1
1 INTRODUCTION . 7
1.1 Bacillus thuringiensis toxins and its mode of action 8
1.2 Genetically modified Bt plants 9
1.3 Non-target effects of Bacillus thuringiensis and transgenic Bt plants 11
1.4 Risk assessment of genetically modified plants 19
1.5 Spiders as test organisms for a risk assessment of genetically modified plants 21
2 CONCEPTUAL AND METHODOLOGICAL APPROACH 25
2.1 Conceptual approach 25
2.2 Methodological approach 26
3 MAIN RESULTS AND GENERAL DISCUSSION 29
3.1 Baseline data of foliage-dwelling spiders in maize fields and
neighbouring field margins 29
3.2 Catching foliage-dwelling spiders in maize: An evaluation of
sampling methods 30
3.3 Potential exposure of spiders to products of Bt maize 31
3.3.1 Characteristics of Bt maize event 176 31
3.3.2 Characteristics of potential spider prey 32
3.3.3 Characteristics of spiders 33
3.4 Effect of Bt maize on foliage-dwelling spiders 34
3.4.1 Laboratory assay on the potential effect of Bt maize pollen on
the garden spider Araneus diadematus 34
3.4.2 Long-term field-scale monitoring of foliage-dwelling spiders
in Bt maize field and adjacent field margins 35
4 SYNOPSIS 37
5 CONCLUSIONS AND OUTLOOK 39
6 REFERENCES 42
7 CURRICULUM VITAE 57
8 LIST OF PUBLICATIONS 58

PUBLICATIONS 59
Publication I: Ludy, C. & Lang, A., 2004: How to catch foliage-dwelling spiders (Araneae)
in maize fields and their margins: a comparison of two sampling methods. –
Journal of Applied Entomology 128, 501-509. 59

Publication II: Lang, A., Ludy, C. & Vojtech, E., 2004: Dispersion and deposition of Bt
maize pollen in field margins. – Journal of Plant Diseases and Protection
111, 417-428. 81


i
Page
Publication III: Ludy, C. & Lang, A.: Bt maize pollen exposure and impact on the garden
spider Araneus diadematus. – Accepted, Entomologia Experimentalis et
Applicata. 101

Publication IV: Ludy, C., Prey spectra and prey selection of orb-web spiders (Araneae:
Araneidae) on field margins: significance for an exposure assessment of Bt-
contaminated prey. – Submitted to Agriculture, Ecosystems & Environment. 127

Publication V: Ludy, C., 2004: Intentional pollen feeding in the garden spider Araneus
diadematus. – Newsletter of the British Arachnological Society 101, 4-5. 149

Publication VI: Ludy, C. & Lang, A.: A 3-year field-scale field monitoring of foliage-
dwelling spiders (Araneae) in transgenic Bt maize fields and adjacent field
margins. – Under revision, Biological Control. 155

APPENDIX 177
ii General part Summary
Summary


Concerns have been raised that genetically modified Bt maize expressing the Cry1Ab protein
of the soil bacterium Bacillus thuringiensis (Bt toxin) may harm non-target organisms, and
there is a general call and need for a risk assessment of Bt maize. Spiders are important pest
predators in agroecosystems and in maize, and can be exposed to the Bt toxin by active Bt
maize pollen feeding, by ingesting their pollen-dusted webs and by preying on herbivorous or
pollen-collecting prey. In this thesis, the risk potentially arising from Bt maize for foliage-
dwelling spiders was assessed by (i) recording base line data of spiders in maize fields and
adjacent margins, (ii) by an evaluation of adequate sampling methods for foliage-dwelling
spiders, (iii) by the investigation of exposure pathways of Bt maize to spiders and (iv) by
assessing the actual Bt effects on foliage-dwelling spiders on laboratory and field scale.
For recording base line data as well as for the evaluation of different sampling
methods of the foliage-dwelling fauna in maize fields and field margins, foliage-dwelling
spiders were collected in maize fields and on adjacent margins in Bavaria, South Germany.
Two different sampling methods were evaluated: drop cloth sampling and suction sampling.
Maize fields and adjacent field margins were colonized by a typical spider assemblage,
consisting of juvenile web-building spiders e.g. Theridiidae (cob-web spiders), Linyphiidae
(sheet-web spiders), Tetragnathidae (long-jawed spiders) and Araneidae (orb-web spiders,
sensu stricto) in decreasing order with a dominance of space-web spiders (Theridiidae and
Linyphiidae). Generally, field margins harboured more spider individuals and spider species
than maize fields. Suction sampling with a small suction device proved to be a more efficient
and consistent sampling method for foliage-dwelling spiders than drop cloth sampling.
Abundance and species richness of foliage-dwelling spiders in maize was shown to be fairly
high, implying that spiders of higher strata may play a more important role in biological
control than suspected up to now.
To gain information on the potential exposure of spiders to Bt maize pollen, data on
the temporal occurrence, spatial range and dispersion of maize pollen, and thus potentially Bt
maize pollen densities in field margins in Bavaria, South Germany was acquired. The Bt
maize event 176 (variety “Navares” by Syngenta) shed pollen generally during July. Pollen
numbers deposited in field margins were highly variable and decreased with distance to field
edge. The main factors determining pollen densities on field margins were various climate
parameters, growth stage of the maize and distance to field edge. Cry1Ab amounts in Bt
1 General part Summary
maize event 176 pollen was with 2.5 g/g pollen found to be in the range reported so far.
Furthermore, Bt maize pollen was quantified in orb-webs in maize fields and on adjacent field
margins by counting pollen in spider webs which were exposed in maize fields and on field
margins during maize anthesis. In both habitat types, web-building spiders may be exposed to
high amounts of Bt maize pollen. An enzyme-linked immunosorbent assay (ELISA) proved
an uptake of the Cry1Ab protein by spiders via the consumption of Bt maize pollen dusted
webs. The exposure of spiders to potential Bt–contaminated prey was investigated by the
assessment of the actual prey spectra and the selectivity of webs as well as individuals of two
orb-web spider species, the garden spider Araneus diadematus (Clerck) and the wasp-like
spider Argiope bruennichi (Scopoli) (both species Araneae: Araneidae) on two different
structured field margins. In general, prey spectra of both spider species on field margins
consisted of a few, in arable land frequent, taxa (e.g. Diptera, Sternorrhyncha, Heteroptera,
Coleoptera) and were dominated by Diptera. In spider webs, small-sized, broad-winged prey
items such as Sternorrhyncha were caught easily, whereas mobile prey with good optical
skills such as Diptera and Hymenoptera could probably avoid spider webs. Armed prey with
strong mandibles or stings such as Coleoptera and Hymenoptera were avoided by individuals
of both spider species. However, both spider species differed in their selectivity to Apidae.
Whereas Apidae were avoided by individuals of A. diadematus, A. bruennichi showed no
avoidance towards this prey. In conclusion, the investigation of possible exposure pathways
of Bt maize to spiders showed that spiders are potentially exposed to Bt maize pollen in spider
webs in maize fields and on field margins as well as to Bt-contaminated prey on field
margins. However, the wasp-like spider may be more exposed to Bt pollen-collecting prey
than the garden spider.
The potential effect of Bt maize on spiders was investigated in a laboratory assay and a
3-year monitoring of Bt maize on field scale in Bavaria, South Germany. The laboratory
experiment was conducted to evaluate possible effects of the consumption of Bt maize pollen
on juvenile A. diadematus. This study showed no effects of Bt maize pollen on weight
increase, survival, moult frequency, reaction time towards prey and various web variables of
A. diadematus. However, a pyrethroid insecticide (Baythroid) affected weight increase,
survival and reaction time of spiders negatively. A 3-year field-scale monitoring on the
foliage-dwelling spider fauna of Bt maize fields and adjacent margins showed no negative
effect on individual numbers, species richness and guild structure of foliage-dwelling spiders
in maize fields and adjacent field margin strips.
2