Elsevier

Ecological Modelling

Volume 250, 10 February 2013, Pages 126-133
Ecological Modelling

Increased mortality is predicted of Inachis io larvae caused by Bt-maize pollen in European farmland

https://doi.org/10.1016/j.ecolmodel.2012.11.006Get rights and content

Abstract

A potential environmental risk of the field cultivation of insect-resistant (Bt-toxin expressing) transgenic maize (Zea mays) is the consumption of Bt-containing pollen by herbivorous larvae of butterflies (Lepidoptera). Maize is wind-pollinated, and at flowering time large amounts of pollen can be deposited on various plants growing in the landscape, leading to inadvertent ingestion of toxic pollen with plant biomass consumed by these butterfly larvae. To examine the possible effect of this coincidence, we focused our study on the protected butterfly Inachis io and two regions of Europe. Using climatic records, maize and butterfly phenology data, we built a simulation model of the butterfly's annual life cycle, overlaid with the phenology of maize pollen deposition on the leaves of the food plant Urtica dioica, and linked these with the dose–response curve of I. io larvae to Bt-maize pollen (event MON810). The simulations indicated that in Northern Europe, where I. io is univoltine, Bt-maize pollen would not be present on the food plant at the same time as the I. io larvae. However, in Central and Southern Europe, where I. io is bivoltine, Bt-maize pollen and the second generation I. io larvae would coincide, and an increased mortality of the larvae was predicted. This prediction differs from earlier studies which predicted negligible effect of field-grown Bt-maize on I. io larvae. Our model is an improvement over previous efforts since it is based on more detailed, empirical data, includes more biological detail, and provides explicit estimation of all model parameters. The model is open-source software and is available for re-use and for modelling the effects on other species or regions.

Highlights

► We modelled the phenology of Bt-maize pollen and Inachis io larvae. ► Second generation larvae coincided with the presence of Bt-maize pollen. ► The dose–response model of larvae on Bt-maize pollen predicted increased mortality. ► Our model differs in design from earlier models; it has more biological detail. ► Our model differs in predictions from earlier models; we found considerable effects.

Introduction

Transgenic crops are grown over large areas in the America (James, 2011). While in Europe imports prevail and only few transgenic crops have been authorised for cultivation, currently only transgenic Bt-maize (event MON810) is grown commercially and mostly in Spain (CERA, 2010). Seven European countries have a moratorium on growing transgenic crops under field conditions, and in several cases the reason is concerns over possible negative environmental impacts. The environmental effects of transgenic crops vary in direction and magnitude (Andow et al., 2006, Catacora-Vargas, 2011) and include effects on ecosystem services (Arpaia, 2010, Lövei, 2001).

Bt-maize, expressing Cry toxins harmful to Lepidoptera or Coleoptera (Koziel et al., 1993, Van Rie, 2000), is cultivated on a large scale (e.g., in the USA; see USDA, 2011). As most promotors are constitutive, the Bt protein is expressed in all plant tissues, including pollen, in which toxin concentration is highly variable (Szekacs et al., 2010). Herbivores ingesting such pollen may suffer toxic effects. For example, wind dispersed pollen from Bt-maize deposited on the leaves of milkweed (Asclepias sp.) can cause mortality to Monarch butterfly (Danaus plexippus) larvae (Losey et al., 1999). Lepidoptera-specific Bt toxins affect most Lepidoptera but species differ greatly in their susceptibility (van Frankenhuyzen, 2009, Peacock et al., 1998). The effects of Bt toxins include increased mortality, reduced growth rate, prolonged development time, and reduced adult body mass and size (Lang and Otto, 2010).

Since maize pollen is deposited in the vicinity of maize fields (Hofmann et al., 2010, Pleasants et al., 2001;), lepidopteran larvae occurring in field margins or habitats nearby Bt-maize fields are possibly at risk (Losey et al., 2003). In Europe, several butterfly and moth species occurring in arable landscapes could be affected (Felke and Langenbruch, 2005, Lang et al., 2004, Schmitz et al., 2003). Of all Austrian butterfly species, 70% are found in agricultural landscapes, of which only eight species would not risk exposure to Bt-maize pollen; the larvae of most species would temporally overlap with the maize pollen shedding period (Traxler et al., 2005).

The population-wide effect of Bt-maize on a species will depend on the species-specific susceptibility to Bt toxins, the actual exposure to the toxin and the ecology of the species. Yet, only few risk assessments studies take these factors into account. For instance, Dively et al. (2004) detected adverse effects of Bt-maize (events MON810 and Bt11) on the Monarch butterfly, but concluded that the natural population would suffer no harm from Bt-maize cultivation due to a low exposure of the larvae (cf. Sears et al., 2001). A similar conclusion was reached for the pale grass blue butterfly (Pseudozizeeria maha) in Japan (Wolt et al., 2005). In a more detailed analysis, Peterson et al. (2006) modelled the phenology of both maize pollen shedding and larval feeding and combined this with a GIS-based analysis of the co-occurrence of Bt-maize fields and larval habitats. For the species in question (Lycaeides melissa samuelis), they concluded that in most places and for most years, maize pollen shedding would occur after the majority of the butterfly larva population had finished eating. However, while most larval habitats where at a safe distance from Bt-maize fields, there were a few regions where they were interspersed and monitoring of the butterfly population was recommended.

In order to estimate the risk involved with Bt-maize in Europe, Perry et al. (2010) modelled the effects of MON810 Bt-maize cultivation on two butterfly species (Inachis io, Vanessa atalanta) and one moth (Plutella xylostella). In contrast to the model of Peterson et al. (2006), their model did not explicitly include the mechanisms of phenology to simulate temporal overlap of maize pollen and larvae, nor was the calculation of spatial overlap presented in detail. The use of generic parameters, subsuming several mechanisms and informally estimated by the authors, were later debated (Lang et al., 2011, Perry et al., 2011); a more recent version of the model maintains this design (Perry et al., 2012).

In this paper, we present a new model BtButTox which includes the mechanisms of temporal coincidence between pollen shedding and larval feeding. We focused on the nettle (Urtica dioica) feeding butterfly species, Peacock butterfly (I. io) for which empirically based parameter estimates could be obtained from literature, both on the dose–response curve of larvae exposed to Bt-maize pollen and the phenology. Moreover, we chose specific scenarios in regions of Germany where historical data exists, from which the expected period of maize pollen shedding could be derived. The model was implemented in a transparent object-oriented design as open source code. The model predicted that in Northern Germany, where I. io is mostly univoltine, the cultivation of Bt-maize would pose a negligible risk, because pollen shedding is predicted later than larval feeding. But in Southern Germany, where I. io is bivoltine, the second generation of larvae coincides with the peak of maize pollen deposition and consequently is at risk.

Section snippets

Model design

The model follows the object-oriented modelling paradigm for model design (Silvert, 1993). Object-oriented software is ideally composed of well-defined, loosely coupled objects, in our case model components, with a minimal interface to other objects (Martin, 2006). The BtButTox model presented here consists of three model components simulating (1) the pollen density on nettle leaves, (2) the dose–response curve of I. io larvae to pollen density and (3) the phenology of I. io taking the imposed

Results

The I. io phenology model reproduced well the expected periods when adults are usually observed flying (Fig. 5 top), both in scenario 1 (univoltine) and scenario 2 (bivoltine). In 1996 some pupae in scenario 2 did not eclose as adults before the onset of winter. It is not known whether this actually happened, but the phenomenon had no impact on the analysis, because it was the number of larvae reaching pupation that was used to express final population size.

In scenario 1 the single generation

Discussion

We detected a risk to I. io living in an agricultural landscape where Bt-maize is grown. However, the risk depended on I. io phenology which depends on the climate. Only in Southern and Central Europe (scenario 2), where the species is bivoltine, would the period of larval feeding coincide with that of maize pollen shedding (Fig. 5).

The peak average density of pollen on nettle leaves (Npeak, Fig. 2) was important for the resulting reduction in I. io population survival (Fig. 6). The lower

Conclusions

Our model indicated that in European farmland, the exposure of butterfly larvae to Bt-maize toxin constitutes a realistic risk. Specifically I. io is at risk in Central and Southern Europe where it is bivoltine. This suggests that a more comprehensive assessment is warranted of the risk implied to butterflies when and where Bt-maize is grown. We contend that such an assessment is best carried out using empirical data, which invites scientific review and integration of knowledge, rather than on

Acknowledgements

We thank Tobias Vogt and Dr. Klaus-Peter Wittich from the German National Meteorological Service (DWD) for the provision of temperature data used in this model and, two anonymous reviewers for helpful comments. This work was supported by the German Federal Agency for Nature Conservation. Authorship in this paper was determined by ranking.

References (67)

  • S.R. Bryant et al.

    The influence of thermal ecology on the distribution of three nymphalid butterflies

    Journal of Applied Ecology

    (2002)
  • Catacora-Vargas, G., 2011. Genetically modified organisms. A summary of potential adverse effects relevant to...
  • CERA, 2010. GM Crop Database. Center for Environmental Risk Assessment (CERA), Washington, DC,...
  • G.P. Dively et al.

    Effects on monarch butterfly larvae (Lepidoptera: Danaidae) after continuous exposure to Cry1Ab-expressing corn during anthesis

    Environmental Entomology

    (2004)
  • G. Ebert et al.

    Die Schmetterlinge Baden-Württembergs, Band 1: Tagfalter I

    (1991)
  • M. Felke et al.

    Effect of Bt-maize-pollen on caterpillars of Inachis io in a laboratory assay

    Gesunde Pflanz

    (2003)
  • M. Felke et al.

    Impact of transgenic Bt-maize pollen on larvae of selected butterflies. BfN-Skripten 157

    (2005)
  • M. Felke et al.

    Effect of Bt-176 maize pollen on first instar larvae of the Peacock butterfly (Inachis io) (Lepidoptera; Nymphalidae)

    Environmental Biosafety Research

    (2010)
  • K. van Frankenhuyzen

    Insecticidal activity of Bacillus thuringiensis crystal proteins

    Journal of Invertebrate Pathology

    (2009)
  • A.P. Gutierrez

    Applied Population Ecology

    (1996)
  • A.P. Gutierrez et al.

    Analysis of biological control of cassava pests in Africa. II. Cassave mealybug Phenacoccus manihoti

    Journal of Applied Ecology

    (1988)
  • L.C. Hansen Jesse et al.

    Field deposition of Bt transgenic corn pollen: lethal effects on the monarch butterfly

    Oecologia (Berlin)

    (2000)
  • F. Hofmann et al.

    Monitoring of Bt-maize pollen exposure in the vicinity of the nature reserve Ruhlsdorfer Bruch in northeast Germany 2007 to 2008

    Umweltwiss Schadst-Forsch

    (2010)
  • F. Hofmann et al.

    Modellrechnungen zur Ausbreitung von Maispollen unter Worst-Case-Annahmen mit Vergleich von Freilandmessdaten

    (2008)
  • F. Hofmann et al.

    A new method for in situ measurement of Bt-maize pollen deposition on host-plant leaves

    Insects

    (2011)
  • N. Holst

    A universal simulator for ecological models

    Ecological Informatics

    (2012)
  • C. James
  • S. Kawashima et al.

    An algorithm for estimating potential deposition of corn pollen for environmental assessment

    Environmental Biosafety Research

    (2004)
  • D. Kolligs

    Schmetterlinge Schleswig-Holsteins

    (2003)
  • M.G. Koziel et al.

    Field performance of elite transgenic maize plants expressing an insecticidal protein derived from Bacillus thuringiensis

    BioTechnology

    (1993)
  • A. Lang et al.

    Modelling in the light of uncertainty of key parameters: a call to exercise caution in field predictions of Bt-maize effects

    Proceedings of the Royal Society of London Series B: Biological Sciences

    (2011)
  • A. Lang et al.

    Dispersion and deposition of Bt maize pollen in field margins

    Journal of Plant Diseases and Protection

    (2004)
  • A. Lang et al.

    A synthesis of laboratory and field studies on the effects of transgenic Bacillus thuringiensis (Bt) maize on non-target Lepidoptera

    Entomologia Experimentalis et Applicata

    (2010)
  • Cited by (0)

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