No full-text available
To read the full-text of this research,
you can request a copy directly from the authors.
An ecologically based method for selecting ecological indicators for assessing risks to biodiversity from genetically-engineered plants
Abstract
The environmental risks associated with genetically-engineered (GE) organisms have been controversial, and so have the models for the assessment of these risks. We propose an ecologically-based environmental risk assessment (ERA) model that follows the 1998 USEPA guidelines, focusing on potential adverse effects to biological diversity. The approach starts by (1) identifying the local environmental values so the ERA addresses specific concerns associated with local biological diversity. The model simplifies the indicator endpoint selection problem by (2) classifying biological diversity into ecological functional groups and selecting those that deliver the identified environmental values. (3) All of the species or ecosystem processes related to the selected functional groups are identified and (4) multi-criteria decision analysis (MCDA) is used to rank the indicator endpoint entities, which may be species or ecological processes. MCDA focuses on those species and processes that are critical for the identified ecological functions and are likely to be highly exposed to the GE organism. The highest ranked indicator entities are selected for the next step. (5) Relevant risk hypotheses are identified. Knowledge about the specific transgene and its possible environmental effects in other countries can be used to assist development of risk hypotheses. (6) The risk hypotheses are ranked using MCDA with criteria related to the severity of the potential risk. The model emphasizes transparent, expert-driven, ecologically-based decision-making and provides formal methods for completing a SL-ERA that can focus ERA on the most significant concerns. The process requires substantial human input but the human capital is available in most countries and regions of the world.
... Since the Cartagena Protocol, new approaches have been discussed and proposed by different scientific forum for ERA of GM plants (Hayes, 2002;Andow & Hilbeck, 2004;Hill, 2005;Sensi, 2011;Sanvido et al., 2012;Andow et al., 2013). However, which nontarget species should be evaluated in risk assessments of GM plants is still under debate. ...
... This approach was specifically aimed at transgenic plants, but should be adaptable to many other agriculture technologies. The ecological approach to species selection considers the local biodiversity associated with the environment where the transgenic plant will be released and uses multi-criteria decision analysis (MCDA) to prioritize the species known to exist in the release environment (Andow et al., 2013). The MCDA uses two sets of ecological criteria: one to rank the potential exposure of each species to the novel environmental stressor (in this case a transgenic plant), and the other to rank the potential magnitude of the adverse environmental consequences should the Pesq. ...
... bras., Brasília, v.49, n.8, p.573-586, ago. 2014 DOI: 10.1590/S0100-204X2014000800001 species be exposed and affected by the novel stressor (Andow et al., 2013). The first set of ecological criteria ranks the species based on their geographical distribution and abundance; the second group of criteria takes into account the species functional role in the agroecosystems. ...
The objective of this work was to list potential candidate bee species for environmental risk assessment (ERA) of genetically modified (GM) cotton and to identify the most suited bee species for this task, according to their abundance and geographical distribution. Field inventories of bee on cotton flowers were performed in the states of Bahia and Mato Grosso, and in Distrito Federal, Brazil. During a 344 hour sampling, 3,470 bees from 74 species were recovered, at eight sites. Apis mellifera dominated the bee assemblages at all sites. Sampling at two sites that received no insecticide application was sufficient to identify the three most common and geographically widespread wild species: Paratrigona lineata, Melissoptila cnecomola, and Trigona spinipes, which could be useful indicators of pollination services in the ERA. Indirect ordination of common wild species revealed that insecticides reduced the number of native bee species and that interannual variation in bee assemblages may be low. Accumulation curves of rare bee species did not saturate, as expected in tropical and megadiverse regions. Species-based approaches are limited to analyze negative impacts of GM cotton on pollinator biological diversity. The accumulation rate of rare bee species, however, may be useful for evaluating possible negative effects of GM cotton on bee diversity.
... So far, a number of criteria have been proposed for selecting the most suitable species to carry out the ERA for GM plants. For instance, the species' exposure to the respective GM plant, the species' sensitivity to the stressor expressed in the GM crop, the species' occurrence and abundance in the agro-ecosystem, the species' protection status and population vulnerability, the species' representativeness of taxonomical and/or of functional groups, and, considering practicability, that the species can be bred, kept and tested successfully under laboratory conditions (EFSA 2010a, b;Römbke et al. 2010;Andow et al. 2013;Hilbeck et al. 2014;EFSA 2016). In this respect, general procedures have been proposed, in a stepwise ecologically-based manner, to identify indicator species for testing effects on NTOs and biological diversity (Hilbeck et al. 2011;Andow et al. 2013). ...
... For instance, the species' exposure to the respective GM plant, the species' sensitivity to the stressor expressed in the GM crop, the species' occurrence and abundance in the agro-ecosystem, the species' protection status and population vulnerability, the species' representativeness of taxonomical and/or of functional groups, and, considering practicability, that the species can be bred, kept and tested successfully under laboratory conditions (EFSA 2010a, b;Römbke et al. 2010;Andow et al. 2013;Hilbeck et al. 2014;EFSA 2016). In this respect, general procedures have been proposed, in a stepwise ecologically-based manner, to identify indicator species for testing effects on NTOs and biological diversity (Hilbeck et al. 2011;Andow et al. 2013). However, practical approaches have rarely been conducted by applying operational tools in a systematic, consistent and transparent manner to support the selection of NTO (cf. the case example of Hilbeck et al. 2014). ...
Citation: Lang A, Dolek M, Lee MS, Freese-Hager A, Otto M (2020) Selection of non-target Lepidoptera species to test Bt maize effects in the laboratory: which species and how to breed them? BioRisk 15: 45-65. https://doi. Abstract Bt maize targeting Lepidopteran pests poses potential risks for non-target (NT) butterflies and moths which are addressed in the environmental risk assessment of genetically modified crop plants. For this purpose, eco-toxicological tests are often conducted with specific NT species in the laboratory in order to assess possible adverse effects. As only a limited number of surrogate species can be addressed, the choice of focal species to be tested is an important decision. However, practical and standardised selection procedures have hardly been developed and applied for NT Lepidoptera, so far. Here, we present a transparent and systematic selection process of suitable test species for Germany, involving selection criteria such as exposure to Bt maize, habitat range and laboratory maintenance of the species. As a result, we compiled a list of 15 lepidopteran species particularly appropriate for testing the adverse effects of Bt maize in the laboratory. In addition, we collected and reviewed published reports for breeding methods of Lepidop-tera, which provides essential information on maintaining lab stocks of NT Lepidoptera. The presented selection procedure allows focusing on the relevant test species in a transparent and reproducible way, and supplies the breeding knowledge required to breed and maintain them, which will be of great utility for the future assessment on possible risks of Bt maize cultivation to non-target Lepidoptera. A peer-reviewed open-access journal Andreas Lang et al. / BioRisk 15: 45-65 (2020) 46
... Each consecutive tier in the ERA should use the feedback acquired in previous steps. Trials in confined conditions are important in early tiers of ERA to establish whether direct effects occur on the life history of particularly important members of the agroecosystem or representatives of important functional groups (Andow et al. 2013;Birch et al. 2007;Houshyani 2012;Romeis et al. 2011Romeis et al. , 2013. ...
... A selection procedure of relevant functional groups and endpoints to test must also be included in the ERA. In this study, we based the selection on the protocol outlined in the EFSA guidance document on ERA of GM plants (EFSA 2010) as well as on several other sources (Andow et al. 2013;Gillund et al. 2013;Romeis et al. 2013Romeis et al. , 2014Scholte and Dicke 2005). We selected the aphid Myzus persicae Sulzer to test in planta the non-target effects of a genetically modified potato expressing resistance to late blight. ...
Insect–plant interactions may be unintentionally affected when introducing genetically modified (GM) crops into an agro-ecosystem. Our aim was to test the non-target effects of a late blight-resistant GM potato on Myzus persicae in greenhouse and climate room experiments and understand how position and number of R gene insertions can affect non-targets in GM events. We also aimed to compare results to baseline differences among three conventional potato varieties varying in resistance to late blight. Aphid development and survival were affected by some GM events in the first generation, though effects disappeared in the second generation. Effects were not dependent on the presence of a marker gene or the insertion of a second resistance gene. Positional effects of gene insertion influenced aphid performance on certain GM events. However, aphid fitness varied considerably more between conventional potato varieties than between Désirée and the GM events. Comparing different GM events to the non-transformed variety is relevant, since unintended effects of insertion can occur. Our protocols can be recommended for in planta risk assessments with aphids. Ecological perspective is gained by selecting several measured endpoints and by comparing the results with a baseline of conventional cultivars.
... In effect, ecological dynamics are evaluated mainly for their potential to mitigate observed physiological hazards to indicator species, rather than for the susceptibility of these dynamics to potential disturbances from the product or practice. As a consequence of this, many authors have raised concerns with the ecological relevance of risk-assessment practices (Obrycki et al., 2001;Andow and Hilbeck, 2004;Andow et al., 2013;Lundgren and Duan, 2013). All phases of the riskassessment process would benefit from being driven by ecological principles, and ensuring that measured indices are ecologically relevant. ...
... This usually involves qualitatively selecting organisms that represent different functional groups (e.g., pollinators, predators, and detritivores) or that have special relevance to producers or society (e.g., honey bees and aquatic insects). Additionally, we know of at least one attempt that has been made to institute a more rigorous system of risk assessment based on large-scale ecological data (Andow et al., 2013). Here, we propose a straightforward, data-driven method for quantifying various ecological aspects of organisms within an agro-ecosystem where transgenic or other plant-incorporated insecticidal products will be used. ...
... This framework should be applied case-by-case because the NTOs' impact will vary depending on the specific GE plant, the introduced trait, and the environmental conditions where the plant is released. Furthermore, we recommend using an ecologically based method for selecting ecological indicators for EcoRA of GE plants for conservation [174]. Risk assessment for the GE plant should be carefully determined whether the collateral damage (cost) exceeds the benefit. ...
Numerous plant taxa are threatened by habitat destruction or overexploitation. To overcome these threats, new methods are urgently needed for rescuing threatened and endangered plant species. Here, we review the genetic consequences of threats to species populations. We highlight potential advantages of genome editing for mitigating negative effects caused by new pathogens and pests or climate change where other approaches have failed. We propose solutions to protect threatened plants using genome editing technology unless absolutely necessary. We further discuss the challenges associated with genome editing in plant conservation to mitigate the decline of plant diversity.
... Replication must be sufficient to allow the detection of adverse Bt effects of a given effect size with a desired probability. A prospective power analysis is mandatory to ensure appropriate replication to detect a pre-defined effect size [12,36,[57][58][59], retrospective power analyses are methodologically not possible [26,60]. In general, an 80% power at an alpha level of α = 0.05 is recommended [34,59]. ...
https://rdcu.be/bHrla
povides a link to the abstract and the full text.
Background and approach: Common standards for laboratory studies of non-target organisms are recognised as
prerequisite to assist the risk assessments regarding the evaluation of environmental effects of transgenic crops. Here,
we provide specific recommendations significant for experimental procedures of laboratory studies to test potential
adverse effects of Bt maize on larvae of non-target Lepidoptera. We searched and analysed both ecotoxicological test
protocols for pesticides in the EU as well as the non-target tests with Lepidoptera applied in unpublished industry
studies submitted officially by agro-companies for the GMO authorisation in Europe.
Results: The classical ecotoxicology protocols applied for testing pesticides could serve as general guidelines, but
do not completely fit the specific and differing requirements for assessing non-target effects of transgenic crops. The
analysis of the non-target studies submitted for the application of the cultivation of Bt maize in Europe revealed critical
limitations, thus corroborating the urgent need for common quality criteria. Based on our evaluations, we identified
several issues requiring harmonisation or standardisation of the experimental conditions and approach, e.g., the
application of Bt maize pollen, synthetic toxins, the provided diet for larvae, experimental controls, magnitude and
duration of exposure to Bt, relevant variables to be recorded, and sufficient statistical power.
Conclusions: Our recommendations should stimulate the development of precise guidance for the authorities, and support
the operationalisation of the required laboratory tests for the evaluation of non-target effects of Bt maize pollen on
non-target Lepidoptera, also contributing to standards of other ecotoxicity tests with Lepidoptera larvae, e.g., for pesticides.
... Plants constitute the base of agro-ecosystems and phenotypic plasticity of plant traits can shape trophic webs (Poelman et al., 2008). In early tiers of environmental risk assessments (ERA) for genetically modified (GM) crops, trials in confined conditions are important to establish possible effects on the life history of representatives of important functional groups such as parasitoids of plant pests (Birch et al., 2007;Romeis et al., 2011Romeis et al., , 2013Andow et al., 2013). Testing selected non-target organisms (NTOs) in planta in greenhouse or climate room assays are compulsory for ERA of GM crops in Europe (EFSA, 2010), according to the rationale that GM plants and their metabolites represent a potential disturbance to the environment. ...
Plants are exposed to microbial pathogens as well as herbivorous insects and their natural enemies. Here, we examined the effects of inoculation of potato with the late blight pathogen Phytophthora infestans (Mont.) de Bary (Peronosporales: Pythiaceae) on an aphid species commonly infesting potato crops and one of its major parasitoids. We observed the peach-potato aphid, Myzus persicae Sulzer (Hemiptera: Aphididae), and its natural enemy, the biocontrol agent Aphidius colemani Viereck (Hymenoptera: Braconidae), on potato plants, Solanum tuberosum L. (Solanaceae), inoculated with water or P. infestans. Population growth of the aphid, parasitism rate of its natural enemy, and other insect life-history traits were compared on several potato genotypes, the susceptible cultivar Désirée and genetically modified (GM) isogenic lines carrying genes conferring resistance to P. infestans. Effects of P. infestans inoculation on the intrinsic rate of aphid population increase and the performance of the parasitoid were only found on the susceptible cultivar. Insect traits were similar when comparing inoculated with non-inoculated resistant GM genotypes. We furthermore tested how GM-plant characteristics such as location of gene insertion and number of R genes could influence non-target insects by comparing insect performance among GM events. Different transformation events leading to different positions of R-gene insertion in the genome influenced aphids either with or without P. infestans infection, whereas effects of position of R-gene insertion on the parasitoid A. colemani were evident only in the presence of inoculation with P. infestans. We conclude that it is important to study different transformation events before continuing with further stages of risk assessment of this GM crop. This provides important information on the effects of plant resistance to a phytopathogen on non-target insects at various trophic levels.
... As for pesticides this regulatory framework uses a single pollinator species in toxicological assessment-the western honeybee A. mellifera. In addition, it does not address the sublethal or indirect effects of herbicide-tolerant and insect-resistant crops on pollinators 88 . Further research would help inform the extent that policy responses are required in this area. ...
Wild and managed pollinators provide a wide range of benefits to society in terms of contributions to food security, farmer and beekeeper livelihoods, social and cultural values, as well as the maintenance of wider biodiversity and ecosystem stability. Pollinators face numerous threats, including changes in land-use and management intensity, climate change, pesticides and genetically modified crops, pollinator management and pathogens, and invasive alien species. There are well-documented declines in some wild and managed pollinators in several regions of the world. However, many effective policy and management responses can be implemented to safeguard pollinators and sustain pollination services.
... The quantification of indirect adverse effects in ecological risk assessments has been a persistent challenge (USEPA 1998) and have been generally ignored in most risk assessment frameworks for GE crops (Andow et al. 2013). Nonetheless, the competitive release of non-target pests highlights the importance of indirect effects. ...
The adoption of transgenic Bt cotton has, in some cases, led to environmental and economic benefits through reduced insecticide use. However, the distribution of these benefits and associated risks among cotton growers and cotton-growing regions has been uneven due in part to outbreaks of non-target or secondary pests, thereby requiring the continued use of synthetic insecticides. In the southeastern USA, Bt cotton adoption has resulted in increased abundance of and damage from stink bug pests, Euschistus servus and Nezara viridula (Heteroptera: Pentatomidae). While the impact of increased stink bug abundance has been well-documented, the causes have remained unclear. We hypothesize that release from competition with Bt-susceptible target pests may drive stink bug outbreaks in Bt cotton. We first examined the evidence for competitive release of stink bugs through meta-analysis of previous studies. We then experimentally tested if herbivory by Bt-susceptible Helicoverpa zea increases stink bug leaving rates and deters
oviposition on non-Bt cotton. Consistent with previous studies, we found differences in leaving rates only for E. servus, but we found that both species strongly avoided ovipositing on H. zea-damaged plants. Considering all available evidence, competitive release of stink bug populations in Bt cotton likely contributes to outbreaks, though the relative importance of competitive release remains an open question. Ecological risk assessments of Bt crops and other transgenic insecticidal crops would benefit from greater understanding of the ecological mechanisms underlying non-target pest outbreaks and greater attention to indirect ecological effects more broadly.
... On the other hand, it is impractical and unnecessary to test every non-target species from the local biodiversity. Instead, methods that do not rely on surrogacy should be used, such as an ecologically based method (Andow et al. 2013 ). This approach identifies the local biological diversity , classifies it into ecological functional groups, and selects key ecological functions for risk assessment. ...
Dose-response assays and surrogate species are standard methods for risk analysis for environmental chemicals. These assume that individuals within a species have unimodal responses and that a surrogate species can predict responses of other related taxa. We exposed immature individuals of closely related aphidophagous coccinellid predators, Cycloneda sanguinea and Harmonia axyridis, to Cry1Ac and Cry1F toxins through uniform and constant artificial tritrophic exposure through Myzus persicae aphids. Both toxins were detected in coccinellid pupae, with individual and interspecific variation. Uptake was significantly higher in H. axyridis than in C. sanguinea, both in the proportion of individuals and the concentrations per individual. We also observed bimodal uptake of the Cry toxins by H. axyridis, which indicated that some individuals had low bioaccumulation and some had high bioaccumulation. This suggests that standard dose-response assays need to be interpreted with caution and future assays should examine the modality of the responses. In addition, the similarity in the biological effects of the Cry toxins in the two predators was due to different biological exposure mechanisms. The majority of H. axyridis were exposed both internally and in the gut, while C. sanguinea was exposed primarily in the gut. Thus, despite their close phylogenetic relatedness, these species would not be good surrogates for each other and the surrogate species methodology should be tested more rigorously.
... These same authors have raised the importance of longer term field studies to detect possible cumulative effects over several seasons, to determine thresholds for detecting any effects and for selecting suitable species for impact studies. The necessity of a more ecological approach in the study of the potential impact of growing GM crops on non-target organisms is raised by Andow et al. (2006Andow et al. ( , 2013, Arpaia et al. (2014), L€ ovei and Arpaia (2005Arpaia ( ), L€ ovei et al. (2009. ...
... The risk is considered the probability that some adverse effect occurs from an environmental hazard, and, classically, the risk is comprised of (i) the probability that the environment is exposed to the hazard (exposure assessment); and (ii) the probability that the adverse effect will occur, given such exposure (effects assessment) e.g., [19]. The overall risk assessment procedure is then made up by four steps: hazard identification, exposure assessment, effects assessment, and risk characterization [20]. ...
Non-target butterfly larvae may be harmed by feeding on host plants dusted with Bt maize pollen. Feeding patterns of larvae and their utilization of host plants can affect the adverse Bt impact because the maize pollen is distributed unequally on the plant. In a field study, we investigated the feeding of larvae of the Small Tortoiseshell, Aglais urticae, on nettles, Urtica dioica. Young larvae used smaller host plants than older larvae. In general, the position of the larvae was in the top part of the host plant, but older larvae showed a broader vertical distribution on the nettles. Leaf blades and leaf tips were the plant parts most often consumed. Leaf veins were consumed but midribs were fed on to a lesser extent than other plant veins, particularly by young larvae. The feeding behavior of the larvae may increase possible exposure to Bt maize pollen because pollen densities are expected to be higher on the top parts and along leaf veins of nettles.
... These same authors have raised the importance of longer term field studies to detect possible cumulative effects over several seasons, to determine thresholds for detecting any effects and for selecting suitable species for impact studies. The necessity of a more ecological approach in the study of the potential impact of growing GM crops on non-target organisms is raised by Andow et al. (2006Andow et al. ( , 2013, Arpaia et al. (2014), L€ ovei and Arpaia (2005Arpaia ( ), L€ ovei et al. (2009. ...
Flea beetles (Chrysomelidae, Alticinae) were collected with Pherocon AM yellow sticky traps in maize plots to compare the assemblages from transgenic Bt-(genetic event MON810, producing Cry1Ab protein effective against lepidopteran pests) and near isogenic maize in Hungary. Altogether, 51,348 flea beetle individuals from 26 species were collected. The dominant species were Phyllotreta atra (F.) and Phyllotreta vittula (Redtenbacher). Their abundances along with other (non-P. atra and non-P. vittula) flea beetle species showed no significant differences between Bt-and isogenic maize plots. Similarly, no difference was found between Bt maize and isogenic maize plots in the species richness of the flea beetle assemblages.
Lepidopteran‐active Bt‐toxins expressed in genetically modified (GM) maize events can adversely affect non‐target lepidopteran (NTL) species when larvae consume harmful amounts of Bt‐maize pollen deposited on their host plants. The briskaR‐NTL project, as commissioned by the European Food Safety Authority, aims to: (i) further develop a spatially‐explicit, generic modelling framework to estimate risks of Bt‐maize pollen to NTLs at landscape scale; and (ii) offer a user‐friendly tool to risk managers to inform decision‐making. Using a literature map and Expert Knowledge Elicitation (EKE), the initial briskaR package was expanded to integrate: (i) a wider range of dispersal kernels for maize pollen; (ii) the variability of exposure to Bt‐maize pollen over time through ToxicoKinetic‐ToxicoDynamic ecotoxicological models; (iii) sublethal effects; and (iv) multi‐year and cumulative effects of chronic exposure. A user‐friendly and public R Shiny application was developed to run the model. Two real‐life case studies were used to test the model in contrasting environmental conditions, and identify key factors that adversely affect larvae of the Common Swallowtail (Papilio machaon). These factors include: the slope of dose‐response for Bt‐toxicity; cumulative effects; impact of an additional stressor (the microsporidian parasite Nosema); and host plant distribution. Overall, the case studies confirm the effect of landscape patterns and crop management practices at local level, suggesting a case‐by‐case approach for the assessment of risks and their possible mitigation. Several sources of uncertainty have been considered, but remaining ones as well as population processes should be considered in future (risk) assessments. While the modelling approach and EKE enabled to address the scarcity of input data by translating uncertainties into wider confidence intervals, gathering additional laboratory and field data is required to support a more robust and ecologically meaningful assessment of impacts of Bt‐maize pollen on NTL and model validation.
Las abejas brindan el servicio de la polinización, con beneficios para seguridad alimentaria y la subsistencia de agricultores y apicultores. Las abejas nativas enfrentan numerosas amenazas, incluyendo la tala y fragmentación de bosques y selvas para uso del suelo en la ganadería y agricultura, los pesticidas y los cultivos genéticamente modificados, los patógenos y la competencia con especies exóticas, además de los efectos del cambio climático. En la región Maya hay evidencias de la perdida de la diversidad de abejas y si bien se conocen 152 especies de abejas, en áreas alteradas se han registrado sólo de 20 a 40 especies. Para conservar M. beecheii (Xunaan kaab, en Maya) se sugiere preservar la vegetación natural y un equilibrio con la apicultura. Las abejas melíferas enfrentan la muerte de colonias por el uso de pesticidas y arribo de nuevas enfermedades. Se recomienda buenas prácticas apícolas, congruentes con la conservación. La Península muestra ambientes fragmentados y áreas con vegetación natural, que son importes refugios para la fauna nativa de abejas. Es urgente tomar medidas para detener el deterioro de la riqueza vegetal y con esto contribuir a la conservación de las abejas.
ResearchGate has not been able to resolve any references for this publication.