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Bio-based and Applied Economics 6(1): 57-79, 2017
ISSN 2280-6180 (print) © Firenze University Press
ISSN 2280-6172 (online) www.fupress.com/bae
Full Research Article
DOI: 10.13128/BAE-18535
A stakeholder engagement approach for identifying
future research directions in the evaluation of current and
emerging applications of GMOs
DaviDe Menozzi1*, Kaloyan Kostov2, Giovanni soGari1, salvatore arpaia3, Daniela MoyanKova2,
Cristina Mora1
1 Department of Food and Drug, University of Parma, Parma 43125, Italy
2 ABI – Agrobioinstitute, Soa 1164, Bulgaria
3 ENEA – National Agency for New Technologies, Energy and Sustainable Economic Development, Rotondella
(MT) 75026, Italy
Date of submission: 2016 30th, June; accepted 2017 3rd, February
Abstract. e yield of several commodity crops is provided in large part by genetically
modied crops in North and South America. However, reservations exist in Europe due
to possible negative eects on human health or environment. is paper aims to ana-
lyse the current research priorities identied in EU countries and to engage European
stakeholders into the formulation of future common research needs regarding the eects
of the possible adoption of commercially available and forthcoming genetically modi-
ed organisms (GMOs) in the areas of socio-economics, human and animal health,
and environment. Additionally, it aims to identify the requirements for sharing avail-
able research capacities and existing infrastructures. First a mapping exercise of existing
research activities in Europe was performed. A questionnaire was developed on a web-
based platform and submitted to national focal points to collect information from EU
Member States. Information was collected from 320 research projects conducted in the
last 10 years in Europe. To rene results of the surveys, twenty invited experts and stake-
holders from the public funding agencies of dierent EU Member States participated in
an international workshop. is paper reports the main ndings of these activities.
Keywords. Genetically modied organisms (GMOs), socio-economic, human and
animal health, environment, workshop
JEL codes. Q16, Q55, O30
1. Introduction
Scientic and technological progress in agriculture has resulted in innovations that
have contributed to increase production and productivity. Genetically modied (GM)
*Corresponding author: davide.menozzi@unipr.it
58 D. Menozzi
crops have shown an extremely rapid adoption rate in many areas of the world. About 12
percent (179.7 million of 1.5 billion hectares) of global cropland was invested with GM
crops in 2015 (James, 2015). Maize area summed up to 53.7 million hectares in 2015 and
GM soybean was cultivated over 92 million hectares during the same cropping season.
Herbicide tolerance (HT) crops occupy 100 million ha, insect resistant (IR) 26 million ha
and crops expressing stacked HT and IR traits were planted on 45 million ha. However
at the same time, in dierent world areas genetically modied organisms (GMOs) have
experienced a transnational opposition from dierent interests groups (Herring, 2008).
Opposition to transgenic crops has oen argued the lack of sucient scientic data dem-
onstrating that GM crops are harmless to humans and to the environment (Rausser et al.,
2015; Yang and Chen, 2016). Although these uncertainties about food and feed products
derived from plant breeding is not conned to transgenic plants (Herring, 2008) and that,
beyond transgenic plants, alternative methods are being applied to obtain new crop varie-
ties (Parisi et al., 2016), GMOs are oen questioned in regards of the uncertainty of their
possible risks. Schurman and Munro (2010) describe how these concerns gained consen-
sus in a network of stakeholders, including consumer, environmental, and social-justice
organizations. e European Union has endorsed the precautionary principle and there-
fore in its risk assessment a central role is sought in addressing and dealing with these
uncertainties. e EU regulations on GMOs constitute a salient issue of risk governance
given the politically high visibility of the topic (Drott et al., 2013). e EU regulatory
framework on GMOs includes rules on authorization conditions, traceability, labelling,
segregation, co-existence, which are established by the European Commission based on
the risk assessment procedures conducted by the European Food Safety Authority (EFSA)
which provides independent scientic advice on this topic (Drott et al., 2013). According-
ly, scientic research promoted by the European Commission so far has also been framed
considering the (potential) positive and negative eects of GMOs.
Despite the global opposition, transgenic crops have spread rapidly in the agribusi-
ness, and the number of GM events at the commercial cultivation, precommercial or reg-
ulatory stages has more than doubled between 2008 and 2014 (Parisi et al., 2016). e
uneven adoption rate of GM crops is still evident. US continues to be the lead country
with 70.9 million hectares (ca 40% of global) with about 90% adoption for the principal
crops: maize, soybean and cotton (James, 2015). While GM plants currently available fea-
ture a limited set of dierent traits, there are several crops with novel traits in the regu-
latory pipeline and at late stages of research and development (R&D) (e.g., resistance to
viruses and pests, tolerance to drought, modied chemical composition, enhanced nutri-
tional content, etc.) (National Academy of Science, Engineering and Medicine, 2016). Cul-
tivation in the EU has remained limited to Bt-maize that in 2013 has been cultivated in
almost 150,000 hectares mainly in Spain (137,000 ha), followed by Portugal, the Czech
Republic, and Romania and Slovakia (European Commission, 2015). However, ve new
GM events for cultivation are currently being examined by EU Commission for a possible
imminent approval. At the same time, the number of experimental eld release trials has
seen a continuous decline over the last years (Gómez-Galera et al., 2012).
It is notable that although a plethora of research projects have been conducted result-
ing in scientic publications which examine the impacts of GM crops on the receiving
environments, on animal and human health, and on the functioning of farms, markets and
59
Stakeholder engagement: identifying future directions for GMO research
rural communities, the technology is still controversial on a number of levels. ere is a
large body of scientic evidence suggesting that, although there are still reasons for concern
and associated risks which must be carefully assessed (e.g., crop failures, price increases,
seed market monopolisation and farmers’ dependency on a few technology providers, co-
existence with non-GM crops, negative impacts on non-target organisms, and resistance
development in target pest populations, etc.), when managed and used appropriately GM
crops may provide notable benets (e.g., reduced use of pesticides, implementation of no-
till agriculture which sequesters carbon and builds up exhausted soils, increased harvests,
revenues and prots for farmers, reduced mycotoxin content in harvested maize, etc.) (Bar-
am and Bourrierm, 2011; Graef et al., 2012; Mora et al., 2012; Jacobsen et al., 2013; Devos
et al., 2014; Mannion and Morse, 2012). At the same time, there is also a growing body
of completed and on-going scientic programmes specically dedicated to the assessment
of the potential socio-economic, environmental and health eects of the use of GM crops
within both Europe and globally (European Commission, 2010).
Given the number of research initiatives, it is important to focus the available resourc-
es for research on the most critical gaps in our knowledge, so that more informed regula-
tory and policy decisions can be made in the future. is means, at the EU level, to sig-
nicantly enhance the alignment of the research programmes of the individual Member
States, identifying knowledge gaps and capacity building needs, in order to avoid duplica-
tion of work in these areas, to leverage complementarities, and to enhance coordination
between scientists from all over Europe. is should be done improving the engagement
of stakeholders (e.g., industry, farming organisations, civil society organisations – CSO,
non-governmental organisations – NGOs, EU and national competent authorities, fund-
ing organisations, academia, etc.) in the shaping of future research agendas and pro-
grammes, in order to make these research programmes more meaningful to the end-users
of the scientic results, and to increase legitimisation of research trajectories and owner-
ship (Ross, 2007; Noteborn and van Duijne, 2011; Graef et al., 2012). e involvement of
stakeholders in the identication of risks and concerns is believed to have a key role in
the process of technology evaluation. e use of GMOs is given as an example for con-
tested innovation in the EU, which failed to take into consideration the ethical concerns,
uncertainties and risks at an early stage of the technology development (van den Hoven,
2013). Although the use of GM crops in agriculture remains greatly questioned in the EU,
new varieties have been developed around the world, which may nd their way into the
EU market in the near future (Parisi et al., 2016). Genomic technologies have substan-
tially improved since the appearance of rst cultivated GM crops, so that individual plant’s
genome can be sequenced and analysed, genotyping methods have improved in through-
put and cost eciency; thus, it is likely that additional traits can be introduced into cul-
tivated plants with increased eciency and reduce costs associated with breeding. Such
developments imply the need to steer the public research policy to invest its resources in
better correspondence to the social concerns related to genetic technologies.
is paper is part of the PreSto GMO ERA-Net project1 aiming at creating and suc-
cessfully implementing an ERA-Net (European Research Area Network)2 that will coor-
1 PreSto GMO ERA-Net (Preparatory steps towards a GMO research ERA-Net), EU FP7, Grant agreement n.
612739. See the website: http://www.presto-gmo-era-net.eu.
2 e objective of the ERA-NET scheme is to step up the cooperation and coordination of research activities
60 D. Menozzi
dinate research activities carried out at national or regional level in the Member States
and the mutual opening of national and regional research programmes on the eects of
GMOs in the areas of socio-economics, human and animal health, and the environment
(Rauschen et al., 2015). In particular, this paper aims to identify knowledge gaps and
future research needs on the eects of GMOs based on the analysis of the research priori-
ties and a dialogue with the stakeholders. We present the results of a mapping exercise of
existing research activities on the eects of GMOs in Europe, and the main outcomes of
an international workshop with relevant experts and stakeholders, European institutions,
and CSOs held in Milan in November 2014.
2. Material and methods
2.1 Mapping of existing research activities
e rst step was to provide an overview of existing research activities and knowl-
edge regarding the socio-economic, health, and environmental eects of GMOs in Europe.
is was performed by an up-to-date mapping of national research programmes, projects,
infrastructures, activities, research groups and capacities in the EU and internationally. e
following GMO assessment databases or datasets were used in mapping existing research
activities: SCAR-Collaborative Working Group “GMO Risk Research” (SCAR-CWG, 2012),
the BiosafeRes database3, and the European Commission’s compendium summarizing the
results of 50 GMO research projects, co-funded by the EC and conducted in the period
2001-2010 (European Commission, 2010). e data were integrated and updated with a
questionnaire developed on a web-based platform (the CADIMA4 database) and submit-
ted to national focal points to collect information from Member States (Moyankova and
Kostov, 2015). rough the questionnaire it was possible to collect details describing
recent and ongoing projects examining the GMO eects, such as the thematic area of the
research, the sources of funding and the type of organizations that carried out the research.
e questionnaire was designed in a specialized section of the CADIMA database for col-
lection of data about the recent and ongoing GMO assessment projects. e projects were
characterized by one reviewer according to several categories including:
a. type of funding (government, EU funding, industry, other);
b. type of project leading organization (research/academy, individual, private company,
other);
c. regional level of the project consortium (national, international EU, international
beyond EU);
d. type of organizations in the project consortium (industry, research/academy, govern-
carried out at national or regional level in the Member States and Associated States through the networking
of research activities conducted at national or regional level, and the mutual opening of national and regional
research programmes.
3 The BiosafeRes database is a worldwide, web-based, free and public-access database of past and current
research projects in GMO Biosafety, is improving communication within the scientic community, and thus
clearly facilitates development of more and better worldwide collaborative research ventures in this eld by
encouraging synergy. Available at: http://biosaferes.icgeb.org.
4 Central Access Database for Impact Assessment of Crop Genetic Improvement Technologies, see the website:
http://www.cadima.info.
61
Stakeholder engagement: identifying future directions for GMO research
ment, other, or mix of them);
e. type of GMO analysed in the project (GM plant, GM animal, GM micro-organisms);
f. main topic of GMO impact assessment (environment, animal health, human health,
technology/society, other);
g. sub-topics of impact assessment (e.g., for environment: soil, water, air, biodiversity,
plant pest and diseases, geochemical variables, landscape structure, target eects, non-
target eects, other).
2.2 The stakeholder engagement approach
Starting from the results of the mapping exercise, the objective of the international
workshop held in Milan on November 24th, 2014, was to use a transparent and structured
approach for recommending a list of transnational research needs regarding the eects of
GMOs in the areas of socio-economics, human and animal health, and environment, as
well as requirements for sharing of available research capacities and existing infrastruc-
tures. e focus of the workshop was on GM crops or other applications (e.g., animals,
micro-organisms, etc.) on the marketplace or near to be commercialized, not necessarily
in the EU, but that may have eects in the EU. Applications intentionally released into
the environment and/or used immediately in feed and food applications were considered.
A Stakeholder Engagement Protocol was agreed with project partners to clarify workshop
aims, activities, and research question development (Menozzi et al., 2014). e stakehold-
er involvement process began with the generation of a “Potential Stakeholder Database”.
e experts were specically selected based on their career, successfully achievements
and long-standing expertise in the eld of GMOs related to scientic, economic, social
and policies aspects. In addition, a broadest group of stakeholders in dierent elds were
added in the database, including representative leaders of farmer’s organizations, public
authorities and agencies, EU research Institutions, private companies and other relevant
stakeholders. A preliminary list was sent to the project partners and integrated with their
suggestions. en, the experts and stakeholders were contacted following a step-by-step
criteria in order to have a right balance between the three scientic areas, as well as a fair
representation of the Member States. A registration before the deadline was required in
order to dene the number of participants, their role and activities, to guarantee the right
balance of the attendees.
Forty-ve stakeholders were invited to represent a right balance of expertise between
the three areas (i.e. socio-economics, human and animal health, and environment), organ-
izational perspective (academic, Member State and EU agency, CSO communities) and
geographical areas. e international workshop activities, conducted by three facilitators
of the University of Parma, were divided into two sections. e morning session was dedi-
cated to share and discuss preliminary results of the project with the participants, includ-
ing the results of the mapping of existing research activities. In the aernoon session the
participants were divided into three working groups, based on the area of expertise or
interest, to identify the relevant transnational research needs. e three working groups
used a structured multi-stage approach, consisting in six steps. Steps from 1 to 5 aimed at
populating the list of transnational research needs (Figure 1), while Step 6 consisted in the
identication of capacity/infrastructure needs to cover those research needs.
62 D. Menozzi
Figure 1. Flow chart for identifying a list of future research needs by the stakeholders.
Stage 1. A questionnaire was sent two weeks before the workshop to all the experts
and stakeholders to identify the main research questions across GM species/traits and
eects. Based on their replies to the questionnaire, a structured dataset of initial research
questions was populated.
Stage 2. Participants in each working group were encouraged to submit modica-
tions to existing research questions or add new ones, given the evidence provided by the
mapping of existing research activities. e initial dataset of research questions was then
established.
Stage 3. Each working group reviewed the initial dataset of research questions on its
area of expertise discussing whether an existing solution to the research need exists and
was available. If this was the case, the use of research outcomes already undertaken was
recommended.
Stage 4. If the research need was not investigated so far, or if the results were not
already available or applicable, the experts considered if it was on the European agenda or
not. If yes, an EU funded project was more appropriate and therefore recommended.
Stage 5. If the research need was not on the current EU agenda, the experts checked
if it could be dened as a transnational interest. If yes, then a programme funded transna-
tionally by the ERA-Net was a likely solution (transnational research need); otherwise, if it
was only on a national agenda, then a national project or programme was suggested.
Stage 6. Once the list of transnational research needs was populated, the moderator
asked participants which capacity/infrastructure needs were available in order to cover
those transnational research needs.
A trained facilitator conducted the discussion in each working group. Potential disagree-
ments were discussed, and eventually reported as such. All inputs from the working groups
were presented in the plenary session, including the areas of persistent disagreements.
63
Stakeholder engagement: identifying future directions for GMO research
3. Results: existing research activities on GMOs in Europe
Information about 320 projects on existing research activities regarding the techno-
and socio-economic, health, and environmental eects of GMOs in Europe were collected
through the mapping exercise (Moyankova and Kostov, 2015). e data included the type
of organizations leading the projects, the funding source, the topics of the GMO assess-
ment projects (human health, animal health, environment, technological/social), and the
studied GMO species. Unfortunately, it was not possible to collect consistent information
about the projects’ budget and timing. is may have introduced a bias since it was not
possible to evaluate the projects’ relative importance and achieved results. Nevertheless,
the number and type of projects alone provides a valid mapping of current research activi-
ties to be used as a starting point for the purposes of the study.
e surveyed GMO projects in Europe have started between 1989 and 2010. Most of
the projects (85%) were led by research or academy organizations such as universities, insti-
tutes or research centers. A relatively small portion of the projects were led by government
organization and private companies, accounting for only 9% and 5% respectively. Most of
the projects were carried out at national level (198 projects). International collaboration was
predominantly among European countries (80 projects), while only 27 projects included
countries outside Europe. A number of 15 projects did not provide this information.
e GMO projects were led by institutions in dierent European countries. When
considering the number of GMO projects per million capita inhabitants, Austria is on
leader position with 6.0 projects per million capita, followed by Denmark (3.1), Norway
(2.8), Finland (2.3), Ireland (1.4), Hungary (1.2) and Belgium (1.1). e other countries,
i.e. France, Germany, Greece, Italy, Netherlands, Spain, Sweden, Switzerland and United
Kingdom, have less than 1 project per million capita. e EU is the only funding source
for projects leaded by Greek and Irish organizations, while other organizations based in
Hungary, Sweden and Switzerland had only projects funded by national sources (Fig-
ure 2). Seven of the project leader countries are funded mainly by governments, namely
UK, Spain, Norway, Italy, Germany, Finland and Austria. e EU was the major funding
source for project leaders based in the Netherlands, Denmark, France and Belgium.
Not surprisingly, projects were mostly focusing on GM plants (196 projects, 68% of
the total, Figure 3). GM micro-organisms and GM animals were analysed only in 20 (6%)
and 10 (3%) projects, respectively. A few projects (7) were dealing with GM plants and
micro-organisms at the same time. Many projects did not specify the type of GMO that
was analysed (n=65, 20%). e interaction of GMO with the environment was investigat-
ed in more than a half of the projects (52%, Figure 3). One third of the projects (33%)
were dealing with the developments of new methods, tools for detection in and analyses
of food and feed, methods for risk assessments, new technique, etc. e eect of GMOs
on human and animal health is a topic of interest in 10% and 4% of the projects, respec-
tively. Many projects covered several topics at the same time. e main subjects (environ-
ment, human health, animal health and technology/society) showed the same distribution
when crossed by type of studied GMOs (Figure 3).
Biodiversity preservation is the predominant sub-topic (58%) in the projects studying
the interaction of GMOs with the environment (Table 1). e eect on non-target spe-
cies was analysed in 25% of the projects. Other sub-categories were objects of only few
64 D. Menozzi
projects. Among the dierent types of GMOs, the GM crops are the most investigated for
their eect on the environment (Table 1). e technological and socio-economic aspects
of the GMOs were analysed in 120 projects. Development of new methods for GMO
detection and technological innovation were predominantly studied in 76% of these pro-
jects. Among the socio-economic issues, the economic eciency was studied the most,
followed by consumer demand and food security (Table 1). Many projects covering this
Figure 2. Number of GMO projects by funding source (EU, Government, Industry and other funding
source) in Europe per country (n = 305).
0% 20% 40% 60% 80% 100%
UnitedKingdom
Switzerland
Sweden
Spai n
Norway
Netherlands
Italy
Ir elan d
Hun gary
Greece
Germany
France
Finland
Denmark
Belgium
Aust ria
EUfunding
Government
Industry
Other
Source: own elaboration.
Figure 3. Type of analysed GMOs and main topics (n = 320*).
050 100 150 200 250 300
GMani mals
GM m i c ro o r ga ni sms
GMc ro ps
GMcropsandmicroorganisms
Notspeci fied
Numberofprojects
Technology/Society
Environment
Humanhealth
Animalhealth
Source: own elaboration. * Note: Many projects covered more than one topic.
65
Stakeholder engagement: identifying future directions for GMO research
topic did not specify the type of GMO and this hampered the data analysis. Fewer pro-
jects treated the eects of GMOs on human health (Table 1). Food safety and allergenicy
were the most explored sub-topics in particular for GM crops. e eect of GMOs on ani-
mal health was explored in 15 projects, where feed safety was the only subject analysed.
GM crops interaction with human and animal health was the most studied topic, whilst
GM animals impact was analysed in only one project. Considering the country of the
leading organization, Switzerland and Spain had projects that only dealt with the eects
of GMOs on the environment. is subject was the most studied in 7 project leader coun-
tries, namely UK, Sweden, Ireland, France, Finland, Denmark and Austria. Organizations
from Belgium, Italy and Norway were leading mainly projects about technology and social
eect of GMOs. GMOs safety for human health is relatively more studied in 2 countries,
i.e. Hungary and Greece. e less studied subject was the eect of GM feed on animal’s
health. Only 5 countries were leading few projects about this topic, the most relevant of
which was Hungary.
Table 1. Health, environment and socio-economics subtopics of the GMO assessment projects in
Europe (n=320*).
GM crops Micro-
organisms
GM
animals
GM crops
and micro-
organisms
Not
specied Tota l
Food safety 17 1 1 - 4 23
Feed safety 13 - - - 2 15
Allergenicity 5 - - - - 5
Toxicity 3 - - - - 3
erapeutic use 1 1 - - - 2
Nutritional value 2----2
Total Health 41 2 1 0 6 50
Biodiversity 67 11 2 4 14 98
Non-target eects 39 - - 2 1 42
Soil 8 2 - 1 1 12
Target eects 6-3--9
Plant pest and diseases 6----6
Other eects 2----2
Total Environment 128 13 5 7 16 169
Economic eciency 11 - - 1 2 14
Consumer demand 1 - - 1 9 11
Food security 2----2
Other eects ----22
Total Socio-Economics 14 0 0 2 13 29
Innovative technology 53 7 4 1 18 83
Technical application 5 - - - 3 8
Total Technology 56 7 4 1 21 91
Tota l 241 22 10 10 55 339
Source: own elaboration. * Note: Many projects covered more than one topic.
66 D. Menozzi
4. Results: stakeholders view on the future research needs
4.1 Workshop participants
Of the total 45 experts contacted for participating in the international workshop, a
nal number of 20 individuals participated in the activities (Table 2); Powers et al. (2014)
suggested that a number between 20 and 25 gives a right balance between the diversity of
technical and sector perspectives and uid working relationships.
Table 2. Workshop contracted persons and participants per category.
Categor y Contacted persons Participants Participation rate
Expert Environment 11 7 64%
Expert Socio-Economics 4 4 100%
Expert Health 7 2 29%
Stakeholders 14 2 14%
European Institutions 4 1 25%
Funding Bodies 5 4 80%
Tot al 45 20 44%
e experts studying the environmental eects of GMOs were the most represented,
followed by the socio-economic experts. e participants were 44% of total the number
of contacted persons. Although a fair gender balance was taken into consideration in
contacting the experts, males were more represented than women in the nal group of
participants (75% males). e weakest participation was found among the stakeholders
(14%), whilst the highest rate was found among the socio-economic experts (100%), then
the environmental (64%) and nally among the health (29%). e participants originat-
ed from ten European countries (Italy 3, Germany 3, e Netherlands 2, Austria 2, UK
2, Swiss 1, Spain 1, Denmark 1, Bulgaria 1, Romania 1); three stakeholders represented
European organizations/institutions (i.e., COPA/Cogeca, the Public Research & Regula-
tion Initiative – PRRI –, and the European Food Safety Authority – EFSA). e career
stage of the participants was quite homogeneous, since most of them were in a senior
position, leaders of research units or project leaders. As observed by Schneider and Gill
(2016) having both young and senior researchers in the same group could discourage
some participants to express their views, leading seniors to control the discussion with
their point of view.
4.2 Initial dataset of research questions
e initial dataset of research questions to consider in developing research needs, as
resulted from stages 1) and 2) (see Section 2.2), have been categorised across the subject
areas (i.e. socio-economics, human and animal health, and environment), and species/
traits (i.e. GM crops, insects, animals, micro-organisms and all GMOs). us, dened cat-
egories of questions were aligned with the results from the mapping exercise to identify
67
Stakeholder engagement: identifying future directions for GMO research
potential gaps in the research that has been done so far, and the future research directions
considered relevant by the stakeholders. Table 3 provides a synthetic representation of the
initial research needs considered by the experts in their deeper analysis.
A list of 48 research questions was developed by the experts in the socio-economic
area. e identied projects in the mapping of current research activities (see Table 1, Sec-
tion 3) are related mainly to the economic eciency and consumer demand. Similarly, the
stakeholders consider important the general economic eects, such as the costs and the
protability, but also more specic subjects like the economics of segregation/co-exist-
ence, legislative framework, consumers perception and attitudes, macro-economic, yields,
and other eects (Table 3). Most of them were considered for all GMOs and GM crops
in general, or insect resistant (IR) crops and herbicide tolerant/herbicide resistant (HT/
HR) crops. For instance, the experts considered the necessity to include ‘non-pecuniary’
benets in the analysis of costs savings related to HT and IR crops (e.g., o-farm income,
management time saving, labour exibility, equipment cost savings, better standability,
etc.), to improve the methodology to analyse the segregation rules of GMOs (e.g., the wel-
fare eects of labelling and segregation policy), and to evaluate the economic eects of
relatively less widespread varieties, such as virus-resistant cassava and Golden rice. Only
one research question was identied by the workshop participants for species other than
crops: the assessment of the socio-economic impact of GM animals. e large portion of
research questions in the initial dataset dened by the stakeholder are specic to dier-
ent types of GM crops which already exist on the market or are under development. GM
plants and crops are also subjects of many projects identied during the mapping exer-
cise (Table 1). Since new GM crops and traits are under development outside the EU, and
potentially access to the common market in the next future, the experts and stakeholders
have suggested to concentrate research eorts on vegetable species.
e European research carried out so far in the area of human and animal health is
primary related to the safety of GM food and feed (Table 1). During stages 1) and 2) a
number of 25 research needs were identied in the area of health (Table 3), divided into
the main eects food and feed safety, nutritional value, allergenicity, toxicity and other.
For instance, the experts considered the need to assess the positive health eects of the
reduced fumonisin content in IR crops. It was argued that GM crop unintentionally pro-
duce high amount of toxic substances, e.g. acetylated aspartic acid, and that animal will be
the main users being exposed to such substances. erefore, research is needed to focus
on developing and validating a test protocol in livestock animals. Most of these research
needs were considered for all GMOs, while none where identied for insects and other
animals. is probably because it was stressed that the focus was on GMOs on the mar-
ket or near to be commercialized. ese results indicate no substantial dierences in the
research carried out so far and the future research needs in the area of human and animal
health as the questions related to the toxicity, allerginicity and food safety are still central
for the novel applications of GMOs (Parisi et al., 2016).
A number of 47 research needs were identify by the experts to cover the area of envi-
ronment (Table 3). Most of the projects carried out so far on the environmental impact
of GMOs are dealing with biodiversity and non-target eects (Table 1). Questions related
to the possible eects to biodiversity of the emerging crop varieties and traits are still of
interest according the stakeholders for dierent kinds of GMOs. Quality of soil and water
68 D. Menozzi
Table 3. Initial research needs in the three areas: health, environment and socio-economics.
All GMOs General
crops IR crops HT/HR
crops
GM crops
with
stacked
traits
RNAi-
based
plants
Other
plants Insects Other
animals
Micro-
organisms Tot al
Food safety 2 - 2 - - - - - - 2 6
Nutritional value 1 1 - - - - 3 - - - 5
Allerginicity 3 - - - - - - - - 1 4
Toxicity 2 - 1 - - - - - - - 3
Feed safety 21--------3
Other eects -----4----4
Total Health 1023004300325
Biodiversity 2 - 3 2 4 - 2 - - 1 14
Soil 2--1--1--26
Wat er - - 2 - - - 1 - - 2 5
Plant pest and diseases 2-11--1- --5
Air - 1 1 - - - - - - 1 3
Ecosystem services 2---------2
Climate change 1---------1
Other eects 2 - - - - 5 4 - - - 11
Total Environment 1117445900647
Economic eects in general 1 3 2 2 2 - 1 - - - 11
Costs - 2 1 2 - - 1 - - - 6
Protability 1 1 2 - 1 - - - - - 5
Segregation/coexistence 2 - 2 - - - - - - - 4
Legislative framework 22--------4
Consumers and society 11--- -1-1-4
Macro-economic eects - 1 1 1 - - - - - - 3
Yields 1 - - - - - 1 - - - 2
Other eects 4 2 2 1 - - - - - - 9
Total Socio-Economics 12 12 10 6 3 0 4 0 1 0 48
Source: own elaboration.
69
Stakeholder engagement: identifying future directions for GMO research
are also pointed as important followed by the eects to plant pest and diseases, air, ecosys-
tem services, climate change, and other eects. Most of the research needs were identied
for all GMOs, IR crops or other plants. For instance, stakeholders claimed to develop eld
methods to monitor soil process intensity and changes, to implement an application of
environmental DNA to detect changes in biodiversity, and to evaluate the potential eects
on non-targeted organisms (NTOs) and the possible protein interactions or synergistic
eects of stacked events expressing Cry and Vip proteins. No research need was identied
for GM insects or other animals.
e initial dataset of research questions was provided to the workshop participant as
a starting point, to support thinking about potential research needs that were outside their
specic expertise area. e lists supplemented explicit encouragement to participants to
think broadly about potential research areas. e activities of the three working groups
have followed the structured multi-stage approach described in Figure 1. Each working
group was arranged of 5/6 experts, one moderator and one note-taker, chosen among the
project partners. e participants in each working group reached a relatively small list of
research needs (from 14 to 18), also by individual questions into groups of questions that
were similar or closely related. Consolidating individual questions into broader research
areas was encouraged when they had similar implications for an assessment or subsequent
risk management decision. e complete list of research needs is reported in Menozzi et
al. (2014).
4.3 Socio-economic research needs
e “Socio-economic” working group identied several categories of research needs.
According to the experts eorts are needed to develop a methodological framework for
assessing the socio-economic eects of GMOs. is framework should be used to inform
policy development. Socio-economic considerations are already included in the regulatory
frameworks on GMOs of some countries (Binimelis and Myhr, 2016). However, it is nec-
essary to work to develop a robust framework and methodology, including criteria, indi-
cators, etc., capturing socio-economic considerations in biosafety decision-making. Gar-
cia-Yì et al. (2014) identied six topics, i.e. the farm-level economic impacts, the econom-
ics of co-existence, the economics of segregation at the supply chain level, the consum-
ers’ acceptance of GMOs, the environmental economics impact and the impacts of GMOs
on food security. us, although there is a high interest in the implementation of socio-
economic considerations in biosafety regulations (Binimelis and Myhr, 2016), research is
needed to establish a robust framework on the socio-economic impacts of GMOs, and
methodology covering data gathering, assessment and decision making.
From the supply chain point of view, Park et al. (2011) have estimated the revenue
forgone by EU farmers due to on-going limited use of IR and HT crops. Similarly, the
eects of the EU regulation on GMOs on EU competitiveness and on innovative research
developed at the EU level should be assessed, as well as the welfare eects across dierent
groups in society (e.g., farmers, consumers, etc.) in the context of dierent policy settings
(e.g., labelling). For instance, the EU co-existence measures aect farmers dierently across
EU Member States according to the isolation distances (between GM and non-GM crops)
required by dierent countries and for dierent species (Ramessar et al., 2010). An eco-
70 D. Menozzi
nomic evaluation of the welfare distribution of exible co-existence regulations may assist
the adoption of proportionate measures (Devos et al., 2014). e stakeholders claimed
that the eects of GMOs along the whole supply chain should be investigated further. is
point goes beyond the common cost-benet analysis; it considers how the structure of sup-
ply chains is aected by innovation, how the eciency is impacted, how the horizontal/
vertical relationships could change, what are the implication on labour market, etc. Up to
now, research mostly concentrates on how costs and benets are distributed along the sup-
ply chain (Garcia-Yì et al., 2014). Few projects have already dealt with supply chain impact,
on structure and performance, of co-existence and segregation measures (e.g., the EU FP6
projects SIGMEA and CO-EXTRA; see also Ghozzi et al., 2016); however, a more deep
analysis of supply chain eects (e.g., on structure and relationships) is missing.
Consumers’ attitude towards the use of new techniques in food production (e.g., new
breeding techniques, nanotechnology – GMOs) needs to be investigated further. In fact,
although most of what can be known by questioning on a hypothetical base has already
been investigated (Dannenberg, 2009), research is missing on consumers’ acceptance stud-
ies using real settings. Further research eorts are needed to explore on the economic
evaluation of the eects (positive and negative) of GMOs on the environment, using a
multidisciplinary approach (Garcia-Yì et al., 2014). In this context, a comparative analysis
of GM, organic and conventional crops in terms of environmental, social and economic
sustainability, should be elaborated.
At farm level, research usually evaluated the main economic eects of GM crops, such
as yield, costs, gross margin (European Commission, 2011). More research is needed to
study the economic implications of more ecient GM varieties, like second generation
GMOs (e.g., nitrogen-ecient GM wheat), e.g., assessing how these GMOs move the yield
frontier, how improvements in yield eciency aect the economic performance of farm-
ers, etc. is research need is likely a transnational one, since not all the countries could
have the same interest. Moreover, other socio-economic impacts are scarcely documented,
such as the indirect eects arising from the GM crops management (e.g., how GM appli-
cations aect farm management planning, cropping system, crop rotation, etc.). Research
should also study the dierences between intensive and extensive margin eects (Bennett
et al., 2013), the stability of new GM crops yields (e.g. draught resistant) on a mid- and
long- term basis, and the economic performance of HT crops (Areal et al., 2012).
Finally, the socio-economic group noted the need to develop systematic reviews and
meta-analyses to consolidate existing knowledge, and to improve the communication of
available evidence. In terms of communication, research is also needed to better under-
stand the key elements in stakeholders’ communication and interaction.
4.4 Human and animal health research needs
e “Human and animal health” working group distinguished research needs across
all types of GM species. Major consideration related to the GM crops intended to be
used as food and feed is whether they are safe for consumption, which should be evalu-
ated under the EU risk assessment frame. While there is substantial amount of experi-
mental data (e.g., feeding studies with laboratory and livestock animals) for the varieties
which already exist on the market (Flachowsky et al., 2012; Snell et al., 2012; Ricroch
71
Stakeholder engagement: identifying future directions for GMO research
et al., 2014), a specic food safety concerns could emerge with the development of new
types of GM crops such as plants combining several modications (stacks) and GM plants
with deliberately modied nutritional properties (Halford et al., 2014; Ramon et al., 2014).
Specic health related questions were pointed by the stakeholders; for instance, the group
agreed that research is needed to explore toxicity eects of multiple Bt proteins in in-vitro
systems, the potential hypo-allergenicity of GM crops, and the denition of the minimal
required inclusion level of plant-expressed phytase for ecient phosphorus utilization of
animals. Traceability and post-marker monitoring are also among the stockholders con-
cerns; there is also a considerable lack of data on the traceability of specic GM crops,
on verication of consumption and/or potential health impacts of GM food ingredients
(e.g., GM crops with enhanced fatty acids), as well as on toxic substances produced by
GM plants used in feed production (i.e. acetylated aspartic acid).
Further, the group noted that little knowledge is available on the health eects of
producing pharmaceuticals by the use of GM plants. While substantial progress has been
made in the development of GM plants for molecular farming, still the scale remains rela-
tively small, mainly performed in laboratory or contained conditions. e major challenge
is the legislative frame and the adaptation of the risk assessment principles to this plant
biotechnology applications (Sparrow et al., 2013). e group agreed that a common fea-
ture of risk assessment of potential protein toxicity is needed (bioinformatics). A specic
issue was raised for myco-toxins in Bt maize; research is needed to assess whether reduced
fumonisin content can be found, as well as their potential and real benets. Although
there is a large body of knowledge available, there is a need to develop a systematic analy-
sis of the data collected by the regulatory bodies.
GM plants producing RNAi molecules represent a biotechnological development
which seems close to the EU market; therefore, experts have raised concerns over the
potential health implications due to the technological dierences with the rst generation
of GM plants. Steps towards the identication and evaluation of the specic human and
animal health risk that may come with the new generations of GMOs and the adaptation
of the regulations and risk assessment guidelines have already been taken by the scien-
tists, agencies and regulatory bodies (Petrick et al., 2013; Ramon et al., 2014). e “health”
working group considered a number of research needs related to RNAi based plants, for
instance more information is needed on survival and uptake in humans and animals, and
post-market monitoring. Although it’s a corporate responsibility to deal with the commer-
cial production and marketing, the EU authorities must provide the appropriate methodol-
ogy and tools for their monitoring along the whole supply chain. An example for this is
the database on food consumption of the EU Member States that is being collated by the
EFSA. e same is needed for feed ingredients. Allergenicity is commonly considered for
humans, whereas there is only limited knowledge available on the impact on farm animals.
is type of investigation should also explore possible links with post-market monitoring.
Finally, there is still uncertainty about the potential for horizontal gene transfer of
genetically modied micro-organisms (GMMs) and viral DNA. Although this concern has
been investigated and discussed in the past (Dröge et al., 1998; Keese, 2008), stakeholders
pointed that better methods need to be developed to assess the presence and diusion of
recombinant DNA and cells.
72 D. Menozzi
4.5 Environmental research needs
e “Environment” working group determined that the research needs can be priori-
tised according to the criterion of “ecosystem services” provision (Tscharntke et al., 2005).
Such an approach would involve the monitoring of cultivated land (on-crop area), but
also of the space between crops in a landscape (o-crop area), and analyse how these two
dierent kinds of areas inuence each other in terms of ecological functionality. In this
respect, the need for comparative study of dierent Integrated Pest Management (IPM)
systems used in the EU Member States was highlighted, as well as the need to assess the
role that GMOs (plants and insects) might play in such IPM systems (Hokkanen, 2015).
Moreover, eorts should be directed to study the ecacy of GMOs in dierent GM events
which hold promises of relevant economic and environmental benets, such as blight
resistance potato (Haverkort et al., 2016), and to a deeper understanding of the develop-
ment dynamics of insecticidal protein resistance mechanisms in target insects (e.g., corn
borers, etc.).
Additionally, regulating and supporting services (pollination, pest control, soil fertility
maintenance, etc.) were considered. e experts concluded that goals for the protection
against undesirable eects have to be assessed at the landscape level. is type of moni-
toring, however, requires instruments to study the possible eects of dierent stressors,
including GMOs, on key species and ecosystem services (e.g., on bees and wild pollina-
tors). System interfaces (i.e. land and water) were also dened as important points to
explore further, as well as the change of dynamics in the system over time. More informa-
tion on species assemblages before introduction of GM crops, to dene appropriate base-
line indicators, is needed for plants, arthropods and micro-organisms (e.g., soil indicators)
(van Capelle et al., 2016).
Further, the protection of cultural services was discussed (e.g., how people perceive
agriculture, recreation, psychological benets from contact with nature, etc.). Research is
needed to study biodiversity in protected areas from dierent perspectives, in particular
to qualify what type and level of biodiversity that society would like to maintain locally.
Cropping practices (i.e. weed control eciency) may have indirect eects on nearby val-
ued areas. For instance, the elimination of weeds by farmers on their elds has also an
impact on the trophic level in terms of available resources for sap feeders, pollinators, nat-
ural enemies, etc., that may in turn aect the functional biodiversity of neighbouring areas
and need to be investigated further (Bürger et al., 2015). In general, there is also a need
to study the people’s perception of dierent agricultural systems, and this should ideally
involve both the natural and the social sciences (multi-disciplinary research).
Finally, the group included research needs not strictly related to ecological services.
ere is strong support for looking more into automated and harmonized methods for
general surveillance, for studying non-target eects of new modes of action (e.g., RNAi)
(Lundgren and Duan, 2013), and for new traits and breeding techniques on the envi-
ronment. ere are still knowledge gaps about the traceability and environmental fate
of GMMs, and to develop bioinformatic tools for studying their evolution in the system.
Finally, there is also limited knowledge about the eects of GM arthropods on the environ-
ment, and this is also an area characterized by quickly progressing of genomic technologies
for possible applications in agricultural as well as in human diseases prevention projects.
73
Stakeholder engagement: identifying future directions for GMO research
5. Results: requirements for sharing capacities and infrastructures
e main requirements for sharing existing (national) capacities and infrastructures
were identied during the working groups’ activities.
e “Human and animal health” working group found that in various countries there
is a high level of expertise available for studying the hypo-allergenicity of GM crops which
needs to be shared. Harmonization and joint initiatives are possible for sharing experiences
on the traceability of specic GM crops. Since applications for RNAi-expressing crops have
been mostly developed outside the EU, and limited expertise is available at the EU level, the
group concluded that a transnational organization of capacities would put the EU in a posi-
tion to overcome this decit in the future. As a lot of research has been done on peptide (e.g.,
cytotoxic peptides, food peptides) and their physiological eects (e.g., dairy research, antibiot-
ics), the group dened the need to integrate these research capacities available across certain
EU countries and sectors, for the purpose of assessing potential protein toxicity as another
important study area. For the assessment of allergenicity in farm animals there are probably
only limited capacities available at the EU level, and future research would also benet from
transnational organization of resources. A high level of expertise for GMMs and viral DNA
horizontal gene transfer was found in various EU countries; again, the relative research needs
are invited to be organized transnationally to increase the overall eciency.
e “Environment” working group dened requirements for sharing controlled exper-
imental eld sites throughout Europe, to allow GMO eld testing on representative envi-
ronments of the various European settings. e elds could also be used to avoid several
regulatory constrains which make it dicult for public research in Europe to study the
eects of GMOs. e group discussed the necessity to have meso-cosm facilities for soil-
based experiments. e group concluded that calls for multi-/inter-disciplinary actions
and projects should invite applications that combine dierent technologies/methods
of scientic enquiry. Finally, it was felt that the GM regulatory, testing and monitoring
methods should be harmonised, as much as possible, with other, similar methods and
approaches in related areas (e.g., pesticide registration, international work on the valuing
and monitoring of ecosystem services, etc.).
e “Socio-economic” working group discussed the need to develop protocols and guide-
lines for conducting socio-economic impact assessments, which would ensure basic compat-
ibility of results, without sacricing the exibility of approaches in the process. Similarly to
the “Environment” group, they also highlighted the need to share eld trials, and to develop
more eld studies for assessing yields, costs, and other economic aspects of the use of GMOs.
In addition, the need to develop multidisciplinary tasks capable of taking qualitative research
(e.g., socio-psychology, behavioural economics, etc.) into account, was included in the list of
priorities. Finally, the group concluded that researchers’ capacities should be shared, via train-
ing and sta exchange programs, thus developing ways to facilitate future collaboration among
researchers from dierent countries (e.g., sharing capacities, PhD programmes, etc.).
6. Conclusions
is paper aims to promote a critical debate among relevant stakeholders and policy
makers by identifying future research directions in the evaluation of environmental, health
74 D. Menozzi
and socio-economic eects of current and emerging applications of GMOs. e outcome
of the international workshop, which was the follow up of a mapping exercise of existing
research activities in Europe, is a list of perceived transnational research needs and con-
sequent requirements for sharing existing capacities and infrastructures; it therefore rep-
resents more than a generalized description of research trends. e list of research needs
will allow those developing research plans to focus more deeply on one or a few themes
that were deemed more relevant by the scientic community as well as the European risk
managers’ network. is process may provide a basis to develop a prioritization from the
perspective of the diverse group of stakeholders, which is to be developed in a next step of
the project. e results of the PreSto GMO ERA-Net project formed the basis for a joint-
ly prepared strategic plan and roadmap for the implementation of the ERA-Net that will
coordinate transnational research on the eects of GMOs (Rauschen et al., 2015).
As pointed by Twardowski and Małyska (2015), the slow progress in the EU decision
making process forced several biotech companies to move R&D and applied activities to
other regions, thus reducing personnel in the EU and transferring existing know-how out-
side the EU. Moreover, this prevented the commercialization of innovative GMOs, possi-
bly resulting in competitive disadvantages for European farmers (Park et al., 2011). Future
directions of socio-economic research on the eects of GMOs should primarily con-
sider the development of a methodological framework for analysing the socio-economic
eects of GMOs. An assessment of the welfare eects across dierent groups in society
may assist the denition of more informed policies. e research questions related to the
eects of newly emerging GMOs to human and animal health raised by the stakehold-
ers during the workshop were general in many occasions or rather case specic in others.
While some of them might be found relevant for the risk assessment to dierent extend,
others are related to traceability and post-market monitoring, and some could appear
to be within the scope of the risk assessment frameworks to be developed for the new
GMOs, such as RNAi plants. e environmental research needs identied were prioritised
according to the criterion of “ecosystem services”, involving the monitoring of on-crop
and o-crop land area, and how these two dierent kinds of areas inuence each other
in terms of ecological functionality. e emerging applications, as well as the tendency
of GM developers to combine dierent traits to produce new commercial varieties (the
so-called “commercial stacks”) (Parisi et al., 2016), pose relevant questions to researchers,
risk assessors and policy makers on how to adapt the EU regulatory framework consider-
ing the environmental and health-related issues, as well as the socio-economic dimensions
(e.g., international trade) when making decisions on GMOs.
A key factor in implementing this process will be the condence that those planning
and funding research have in the method used (Schneider and Gill, 2016). e activi-
ties described in this paper has explicitly taken into account the wider views of a diver-
sity of stakeholders and end-users (i.e. industry, farming organisations, CSOs, NGOs,
EU and national competent authorities, funding organisations, academia). is intended
to encourage participation of dierent scientic communities (scientists from all over
Europe) in the future joint transnational calls managed through the ERA-Net, to enhance
collaboration between actors (to leverage complementarities) and to increase the account-
ability of research trajectories and outcomes (create an internationally recognizable criti-
cal mass). e decision to consider a single group of 20 participants allowed balancing
75
Stakeholder engagement: identifying future directions for GMO research
the greater diversity of technical and sector perspectives, and the facilitation of more uid
working involvement from all participants. Breakout groups allowed the experts to elab-
orate on a greater number of details surrounding the interfaces of their disciplines with
others, and this can thoroughly inform the scientic community in planning and promot-
ing interdisciplinary and transdisciplinary research (Powers, 2014). Viewed from the per-
spective of group dynamics, the entire process aimed to achieve a common understanding
of the research gaps and needs in the evaluation of current and emerging applications of
GMOs able to design future research directions.
7. Funding
is work was supported by the European Commission contract 612739, PreSto GMO
ERA-Net (Preparatory steps towards a GMO research ERA-Net), funded by the EU FP7
programme. e authors declare no competing nancial interests.
8. Acknowledgements
e authors wish to thank the PreSto GMO ERA-Net project partners for their inputs
into the research, in particular the project coordinator Dr. Stefan Rauschen. e authors
gratefully acknowledge the experts and stakeholders who participated in the international
workshop for their active contribution to the identication of future research directions in
the evaluation of emerging applications of GMOs. e authors thank also the anonymous
reviewers for their constructive comments. e views expressed are purely those of the
authors and may not under any circumstances be regarded as stating an ocial position of
the European Commission.
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