NJAS: Wageningen Journal of Life Sciences

ISSN: 1573-5214 (Print) 2212-1307 (Online) Journal homepage: https://www.tandfonline.com/loi/tjls20

Is there hope for sustainable management of

golden apple snails, a major invasive pest in
irrigated rice?

Janina Schneiker, Wolfgang W. Weisser, Josef Settele, Van Sinh Nguyen, Jesus
Victor Bustamante, Leonardo Marquez, Sylvia Villareal, Gertrudo Arida, Ho
Van Chien, Kong Luen Heong & Manfred Türke

To cite this article: Janina Schneiker, Wolfgang W. Weisser, Josef Settele, Van Sinh Nguyen,
Jesus Victor Bustamante, Leonardo Marquez, Sylvia Villareal, Gertrudo Arida, Ho Van Chien, Kong
Luen Heong & Manfred Türke (2016) Is there hope for sustainable management of golden apple
snails, a major invasive pest in irrigated rice?, NJAS: Wageningen Journal of Life Sciences, 79:1,
11-21, DOI: 10.1016/j.njas.2016.07.001

To link to this article: https://doi.org/10.1016/j.njas.2016.07.001

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 NJAS - Wageningen Journal of Life Sciences 79 (2016) 11–21

Contents lists available at ScienceDirect

NJAS - Wageningen Journal of Life Sciences

journal homepage: www.elsevier.com/locate/njas

Is there hope for sustainable management of golden apple snails, a

major invasive pest in irrigated rice?
Janina Schneiker a , Wolfgang W. Weisser a , Josef Settele b,c , Nguyen Van Sinh d ,
Jesus Victor Bustamante b,e , Leonardo Marquez f , Sylvia Villareal g , Gertrudo Arida f ,
Ho Van Chien h , Kong Luen Heong g , Manfred Türke a,c,i,∗
a
Terrestrial Ecology Research Group, Department of Ecology and Ecosystem Management, Center for Food and Life Sciences Weihenstephan, Technische
Universität München, Hans-Carl-von-Carlowitz-Platz 2, 85354 Freising, Germany
b
UFZ, Helmholtz Centre for Environmental Research, Theodor-Lieser-Strasse 4, 06120 Halle, Germany
c
German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, 04103 Leipzig, Germany
d
Institute of Ecology and Biological Resources, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet, Cau Giay, Hanoi, Vietnam
e
LEGATO Office, 3601 Banaue/Ifugao, Philippines
f
Crop Protection Division, Philippine Rice Research Institute, Maligaya, Science City of Muñoz, 3119 Nueva Ecija, Philippines
g
International Rice Research Institute, DAPO 7777, 1066 Metro, Manila, Philippines
h
Southern Regional Plant Protection Center, Long Dinh, Vietnam
i
Institute of Biology, Leipzig University, Johannisallee 21, D-04103 Leipzig, Germany

a r t i c l e i n f o a b s t r a c t

Article history: The golden apple snail or GAS (Pomacea canaliculata) is an important invasive pest in irrigated rice that
Received 17 June 2016 feeds on young rice plants. In many countries in SE-Asia, governments have recently decreased their
Accepted 21 July 2016 support of training courses for snail management, because farmers are now considered to know how to
Available online 9 August 2016
effectively manage this pest. Although a great number of sustainable control methods is recommended
which do not involve the use of pesticides, it is uncertain whether these are taken up by farmers. Probably,
Keywords:
the easiest way to control GAS, is the application of synthetic ‘instant kill’ molluscicides, which can have
Pesticide
detrimental effects on the environment, non-target species, and health. The aim of this study was to
Molluscicide
Pomacea canaliculata
develop ideas for solutions on how to achieve a sustainable management of GAS without or at least a
Channelled apple snail decreased use of molluscicides. In a large-scale approach, we conducted interviews with rice farmers
Southeast Asia in seven regions across Vietnam and the Philippines, assessing the participation in training courses,
Pest management company knowledge on snail ecology, the methods of controlling and the utilization of the snail, and the farmers’
suggestions on how to improve pest snail control. Only 23% of the farmers had previously received
training in GAS management. We found that training neither had positive nor negative effects on the
number of sustainable methods applied, molluscicide avoidance, concern about using molluscicides,
or on the farmers’ knowledge about GAS. As much as 74% of the respondents applied molluscicides.
Contrary to recommendations, farmers applied only few sustainable control methods. All farmers had
clear knowledge gaps about GAS, especially in species identification, which can even further the ongoing
decline of native mollusks in rice landscapes. We conclude that the decision to phase out information
campaigns has been taken to rash, and that trainings in our study regions carried through previously
had limited success, and thus need revision. To decrease molluscicide use, and to promote sustainable
management on the large scale, we synthesized our results, and we suggest that information for farmers
might be provided through media often accessed, such as TV, radio or the internet (e.g. by entertainment
− education). We further discuss the potential of community cooperation to achieve sustainability. As

∗ Corresponding author at: German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, 04103 Leipzig, Germany.
E-mail addresses: nina.schneiker@yahoo.de (J. Schneiker), wolfgang.weisser@tum.de (W.W. Weisser), josef.settele@ufz.de (J. Settele), nvsinh@gmail.com (V.S. Nguyen),
jappanjesus@yahoo.com (J.V. Bustamante), lvinasmarquez@yahoo.com.ph (L. Marquez), s.villareal@irri.org (S. Villareal), gs arida@yahoo.com (G. Arida), hvchien@vnn.vn
(H.V. Chien), klheong@yahoo.com (K.L. Heong), manfred.tuerke@gmx.net (M. Türke).

http://dx.doi.org/10.1016/j.njas.2016.07.001
1573-5214/© 2016 Royal Netherlands Society for Agricultural Sciences. Published by Elsevier B.V. All rights reserved.
12 J. Schneiker et al. / NJAS - Wageningen Journal of Life Sciences 79 (2016) 11–21
there are distinct limitations to these approaches, we have developed the concept of local GAS manage-
ment and utilization companies (GASMUC) which could take over sustainable control and utilization of
GAS, and native mollusk conservation for an entire community.
© 2016 Royal Netherlands Society for Agricultural Sciences. Published by Elsevier B.V. All rights reserved.
1. Introduction
Agricultural intensification, such as the increase in pesticide
application, leads to a loss of biodiversity, which impairs impor-
tant ecosystem functions and services, especially biocontrol and
pollination [1]. The increased input of chemical pesticides through
agricultural intensification holds a number of environmental haz-
ards, including the contamination of freshwater resources and
of the soil, the acquisition of pest resistances, and threats to
human welfare [39,45]. With the environmental consequences of
agricultural intensification becoming more evident, implementing
integrated methods for pest management is one of the top priori-
ties in striving towards a more sustainable agriculture [39,45,57].
In rice production systems, there is a great demand for increas-
ing yields in the future, based on a more efficient use of natural
resources, while at the same time sustaining the environment [20].
Rice pesticides, which include insecticides, fungicides, herbicides
and molluscicides, have a strong impact on the environment and
on the farmers’ health, and can facilitate insect pest outbreaks
by depleting populations of biocontrol agents [44,48]. The imple-
mentation of environment-friendly integrated pest management
(IPM) practices on the large scale is facing several obstacles, such
as a failure in knowledge dissemination to farmers, or the influ-
ence of pesticide companies on stakeholders, and therefore new
approaches have to be considered for its successful establishment
[48]. An important component of novel IPM strategies is the inte-
gration of humans, from farmers to policy-makers, and their impact
on rice ecosystems, landscapes, and biodiversity [45,48,58]. Eco-
logical Engineering, as a component of IPM, has a great potential
to facilitate biocontrol of insect pests in rice [58]. The implemen-
tation of novel techniques in pest management, however, is often
hindered by the farmers’ lack of knowledge of pests, combined with
wrong beliefs or preconceptions, and a tendency to overestimate
the destructiveness of highly visible pests [11]. Thus, a successful
adoption of sustainable management practices must include direct
communication with the farmers, in order to change their beliefs
and modify their practices [11].
For invasive species, population control by naturally occur-
ring native predators is often limited [35]. Golden apple snails
(GAS; Pomacea canaliculata and P. maculata) were intentionally
introduced from South America to Southeast Asia as a cheap and
protein-rich food source, but in SE-Asia they have become a major
pest in irrigated rice over the past 30 years [22]. The snails devas-
tate plantings of rice seedlings, and farmers suffer high costs in
the form of snail control and yield loss [30]. Nghiem et al. [41]
estimated the annual costs associated with GAS of 806 – 2138 mil-
lion USD for only three (Vietnam, Philippines, and Thailand) out
of 24 invaded countries [22]. Though a variety of native animal
species, occurring naturally in rice fields, prey on GAS [63], their
abundance is often too low to have an effect on population den-
sities of the pest snail (which, however, could also be related to
paddy management and pesticides) [63,61]. If natural predators
and competitors of GAS occur in higher densities than in conven-
tionally managed rice fields, such as in natural rivers, they bear
the potential to keep GAS densities low [61]. Nevertheless, in rice
fields farmers have to take management actions to control GAS.
Numerous suggestions for sustainable management methods of the
pest snail have been made that do not impair non-target organisms
and bring no long-term harm to the ecosystem: cultural (replant-
ing, water management), mechanical (handpicking, screens, traps,
crushing eggs), biological (ducks and fish introduced to rice fields as
predators), botanical (plant derived molluscicides), and crop con-
trol (transplanting older seedlings, seedling broadcasting, reduced
seed densities, crop rotation) [9,50,30,23,62]. In most countries, the
government advises farmers to use a combination of these sustain-
able methods, although often together with chemical control when
necessary [30]. It is alarming that programs on pest snail control
and farmer education run by the governments of many SE-Asian
countries attenuate, as farmers nowadays are supposed to know
how to manage the pest snails properly [30]. Although application
of several sustainable methods in combination can be effective in
controlling the snails [30], we assumed, however, that most farm-
ers rely on regular molluscicide application rather than on time-
and work-intensive sustainable methods, which was also observed
in recently invaded rice fields in Ecuador [21]. In addition, a similar
behavior of farmers has been observed in rat control [52].
The two major active agents currently used in GAS control in SE
Asia are niclosamide and metaldehyde. Both substances are mod-
erate in their impact on the environment, compared to other –
often banned – moluscicides [10]. However, niclosamide is toxic
to a wide variety of freshwater organisms, including fish [42] and
is detrimental to the growth of rice seedlings if used as a preseeding
snail control treatment in direct-seeded rice [28]. Metaldehyde is
recently under emerging concern as a pollutant of ground water,
lakes and rivers [31]. Both before mentioned molluscicides and all
others, of course, are toxic to a wide range of mollusks, to pests and
important native decomposers, edible snails, and mussels. Further,
it is not clear how the environment might change after the regu-
lar application of molluscicides in rice fields each cropping season
over several decades, especially as native snail populations pro-
viding essential ecosystem services, in the form of decomposition
and nutrient cycling, or serving as food for generalist predators
[47], are strongly reduced [22]. Thus, a reduction in the large-scale
application of molluscicides, as for all other pesticides, should be a
prioritized aim to achieve a sustainable management of rice ecosys-
tems [45,48].
In this study we conducted a survey on GAS in irrigated rice fields
with farmer respondents in a large-scale approach in Vietnam and
the Philippines. Rather than focusing on regional differences, we
tried to find general aspects of the current status of GAS for large
geographical distances spanning different regions with varying cul-
tural and structural diversity and land-use intensity. We aimed at
integrating the insights we gained from the farmers’ knowledge and
suggestions, and recent literature, to develop ideas allowing for sus-
tainable management of the pest snails. To develop these ideas, we
first addressed the following hypotheses: (i) farmers consider GAS
still to be one of the most important pests in rice; (ii) farmers pre-
fer synthetic molluscicides to sustainable management methods;
(iii) training courses on GAS management have a positive effect on
pest snail knowledge and sustainable management; (iv) farmers are
not aware of the impact of GAS and its management on non-target
species.
 J. Schneiker et al. / NJAS - Wageningen Journal of Life Sciences 79 (2016) 11–21
2. Material and methods
2.1. Study regions
The study is part of the LEGATO research project on sup-
porting a long-term sustainable development of irrigated rice
production (www.legato-project.net; [49]) and it was performed
in seven regions, four of which located in Vietnam, and three in
the Philippines (detailed information on the regions, landscapes,
and sites is also provided in [33]) The regions were chosen to make
countries comparable, featuring regions with different terrain (low
or mountainous), different land-use intensity, structural diversity,
and cultural identity. The lowland regions are Ha i Duo’ng Province
(VN 1; 20◦ 55 N 106◦ 20 E) and Vı̃nh Phúc Province (VN 2; 21◦ 18 N
` Giang Province (VN 4; 10◦ 25 N
105◦ 36 E) in North Vietnam, Tiên
106 10 E) in South Vietnam and Laguna Province (PH 1; 14◦ 10 N
◦ 
121◦ 20 E) and Nueva Ecija Province (PH 2; 15◦ 35 N 121◦ 00 E) in
Central Luzon, Philippines. The mountainous areas Lào Cai Province
(VN 3; 22◦ 20 N 140◦ 0 E) in the very north of Vietnam and Ifu-
gao Province in the Philippines (PH 3; 16◦ 50 N 121◦ 10 E) are both
famous for man-made rice terraces. The mountainous regions are
characterized by a high cultural and structural diversity, but a lower
land-use intensity, whereas in the lowland regions, a medium to
high land-use intensity, medium to low structural diversity and a
low cultural diversity are common [33].
2.2. Questionnaire and respondent selection
Participants of the survey were rice farmers, either field own-
ers/tenants and/or workers. We interviewed the 65 owners/tenants
of rice fields that were selected as permanent study sites in the
LEGATO project. Additionally, a total of 39 owners or workers
of fields from the same municipalities as the LEGATO-fields or
municipalities close by were chosen at random and asked to partic-
ipate. Interviews were conducted with the help of a questionnaire
(Appendix A. Questionnaire); another five farmers in the Tien Giang
province in South Vietnam answered a short version (Appendix
B. Questionnaire − short version). Thus, a total of 109 rice farm-
ers were involved in the study (Table 1) with 68% males and
32% females. Interviews were conducted in three to six (4.9 ± 1.2
mean ± SD) different municipalities within a 15 × 15 km area in
each region with 3.1 ± 2.0 interviews per municipality. The mean
age of the participants was 51.67 ± 14.02 years, the oldest being
82 and the youngest 22 years old. Respondents had an average of
33.03 ± 13.68 years of experience in rice farming (Table D.1). The
survey was conducted from May to July 2012. The questionnaire
was divided into six topical sections (Appendix A. Questionnaire):
(i-ii) general questions about the socio-economic situation of the
interviewee, rice cultivation, and ownership of rice fields; (iii)
knowledge about rice pests in general and GAS in particular; (iv)
application of control methods against GAS; (v) introduction of GAS
to the respective regions and training of the farmers; and (vi) sug-
gestions farmers might have for future pest snail management. The
Table 1
Number of interviews distributed over the seven study regions according to inter-
views of farmers of LEGATO study rice fields and randomly selected rice farmers.
Region LEGATO Random Total
i Duo’ng
VN1: Ha 9 0 9
VN2: Vı̃nh Phúc 10 0 10
VN3: Lào Cai 10 0 10
` Giang
VN4: Tiên 7 8 + 5 short 20
PH1: Laguna 10 10 20
PH2: Nueva Ecija 9 11 20
PH3: Ifugao 10 10 20
13
regular questionnaire took 60–120 min per personal interview, the
short version only 10–15 min. All interviews were conducted by the
same interviewer in local languages with the help of different trans-
lators (Vietnam: Vietnamese; Philippines: Tagalog, Ifugao, Ilokano,
and English). Questionnaires were discussed prior to the survey
between interviewer and translator to avoid misunderstandings.
All translators had advanced knowledge in rice cultivation and on
GAS.
2.3. Knowledge questions about GAS
We asked 96 farmers twelve questions concerning GAS ecol-
ogy and management (Appendix C. Knowledge questions). Answers
were scored, based on literature as either correct or as false
answers, including questions to which farmers did not know the
answer. Answers were judged lenient, so that even imprecise
answers that were essentially not wrong were judged as correct.
Answers that included correct aspects but also essentially false
information were counted as wrong. Three farmers did not under-
stand one of the questions, and those questions were not scored
for these farmers. Questions ranged from very easy ones (like the
appearance of GAS eggs) to more difficult questions (i.e. whether
the snail transmits any diseases). Questions were grouped in four
levels of difficulty by sorting questions according to the proportion
of correct answers of all farmers, from least correct to most cor-
rect answers. Difficulty was categorized as (1) easy (75% quartile to
maximum correctness of the ranked questions; range 96–99% cor-
rect answers); (2) easy to medium (median to 75% quartile; range
85–94% correct); (3) medium to difficult (25% quartile to median;
range 56–81% correct); and (3) difficult (minimum to 25% quar-
tile; range 1–20% correct). Thus, there were three questions in each
category.
2.4. Snail identification
Farmers were asked to identify all individuals of snails they
considered to be GAS (Pomacea canaliculata Lamarck, 1819) from
eight colored pictures of shells of several locally occurring snail
species (Vietnam and Philippines). There were four pictures of P.
canaliculata, two of native apple snails (Pila ampullacea L. 1758),
a native Vivipariid snail (Filopaludina sumatrensis Dunker, 1852),
and an invasive pest snail of non-irrigated crops (Lissachatina
fulica Bowdich, 1822). Pictures of P. canaliculata and P. ampullacea
showed individuals with natural variations in shell color and mark-
ings. Vivipariid snails and native apple snails are commonly eaten
and also sold on local food markets in SE-Asia. The shells in the pic-
tures were cleaned and photographed in a standardized way (G &
Ph Poppe, Conchology, Inc.). The snail pictures (6.4 × 6.4 cm) were
arranged in random order on a single sheet and numbered from 1
to 8 without showing species names.
2.5. Statistical analysis
For statistical analysis R 3.1.2 [46] and for figures SigmaPlot 12.0
(Systat Software, Inc.) were used. ANOVA was performed using the
function ‘aov’, generalized linear models (GLM) using the function
‘glm’, and generalized linear mixed-effects models (GLMM) using
the function ‘glmer’ in the lme4 package [3]. Global statistics are
derived from analysis-of-variance tables based on the calculation
of type-II likelihood-ratio tests (GLM) and type-II Wald chi-square
tests (GLMM) using the function ‘Anova’ in the car package [14].
Model simplification was performed with the least significant
terms deleted first, starting with the highest-order interactions [8],
and results are reported for best models with lower Akaike Infor-
mation Criterion (AIC) values. Terms removed from models due
to model simplification are placed within square brackets in the
14 J. Schneiker et al. / NJAS - Wageningen Journal of Life Sciences 79 (2016) 11–21
models below. Detailed results of the best models are provided in
Appendix E. Statistical summary. The number of responses varied
according to different topics used for the analyses, as some farm-
ers were (for different reasons) not asked some questions, were
asked a shorter version of the questionnaire only (Appendix B), or
misunderstood questions.
2.5.1. Experience and training
Differences in rice farming experience of farmers (in years) was
compared among regions using ANOVA. Frequency of training in
GAS management by governmental/research institutions (yes or
no) was analyzed using GLM with a binomial error including the
fixed effects experience, region, and [experience:region].
2.5.2. Molluscicide use and sustainable methods
Frequency of molluscicide use (yes or no) was analyzed accord-
ing to experience, training, region, and [the three-way and all two-way
interactions] using GLM with a binomial error. The number of sus-
tainable methods applied by farmers to control GAS was analyzed
using GLMM with a poisson error including the fixed effects experi-
ence, training, molluscicide use, region, and [all two-way interactions]
and the random effect region.
2.5.3. Concerns using pesticides
We compared the number of farmers with health and environ-
mental concerns about using molluscicides/pesticides (yes or no)
using GLMM with a binomial error including the fixed effects expe-
rience, training, molluscicide use, region, and experience:molluscicide
use, experience:training, [training:molluscicide use], and [experi-
ence:training:molluscicide use] and the random effect region. The
same analysis was performed for environmental concerns only.
2.5.4. Knowledge questions
Farmers knowledge about GAS as the score of each answer
to twelve knowledge questions as either correct or false was
analyzed using GLMM with a binomial error including the fixed
effects experience, training, difficulty of questions (4 levels), region,
region:difficulty, [experience:difficulty], and [training:difficulty] and
the random effects farmer ID and question number.
2.5.5. Snail identification
We compared the nominations of eight snail pictures identi-
fied as GAS by farmers (yes and no) using GLMM with a binomial
error including the fixed effects experience, training, region, snail
species (as either GAS or no GAS), snail individual (8 pictures), expe-
rience:species, [training:species], [region:species], and the random
effect region.
3. Results and discussion
3.1. Regional differences
This study was intended to develop ideas for a general sustain-
able management of GAS based on farmers’ knowledge, perceptions
and suggestions derived from a large-scale approach. However,
farmers’ responses differ strongly from region to region, which
must be considered when designing local management recommen-
dations. Thus, we also contrast the results among the seven regions
investigated (Appendix D. Regional differences). Farmers in the Lào
Cai region (VN 3, Vietnam) did not know of GAS at all and there-
fore they were excluded from most of the following sections and
analyses, except stated otherwise.
3.2. Farming experience and training
Farmers interviewed in our survey (N = 94, excluding Lào Cai
region) had on average 34 ± 14 (mean ± SD) years of experience
in rice production (Table D.1). There were no significant differ-
ences in experience among regions (Anova, F5 ,87 = 0.488, p = 0.785).
Only 23% of the respondents (N = 22) said that they had previ-
ously received a training by governmental or research institutions
on how to manage GAS (Fig. D.1), which stands in strong con-
trast to government statements, but training efforts are attenuating
nowadays [30]. Another 12% received training by pesticide compa-
nies − mostly on how to use molluscicides. In our analyses, those
farmers were treated as untrained as to the effects of training on
knowledge or management. Farmers with a longer experience in
rice farming more frequently attended trainings (GLM, chi2 = 4.61,
df = 1, p = 0.0318) and there was a significant difference in the num-
ber of farmers who received training among regions (chi2 = 11.45,
df = 5, p = 0.0431) with more farmers from Nueva Ecija and Ifugao
(Philippines) receiving a training than in the other regions (Fig. D.1).
3.3. Pest perception and utilization
When farmers (N = 94 farmers; N = 130 nominations) were asked
about the factors that have the greatest negative impact on rice
production, farmers mentioned GAS (24%) most often, followed by
insects (23%), abiotic reasons such as storms or flooding (20%), and
rats (15%) (Table D.2). When farmers (N = 94 farmers, N = 104 nom-
inations) were asked about the most damaging pest in their paddy,
however, various kinds of insect pests were mentioned in the first
place, which accounted for 40% of the answers, followed by GAS
(30%) and rats (21%) (Fig. D.2). Please note that farmers, at this time,
did not know that the interview was particularly dealing with GAS.
GAS was declared to be present in all of the rice fields and farmers
confirmed that it damages rice plants. 62% of the farmers agreed
that they suffered from significant yield loss because of GAS, while
35% disagreed with that statement and 3% answered that they did
not know. 99% of the farmers said that yield loss would be a lot
more severe if they did not apply any management methods and
only 1% of the respondents thought otherwise. Many farmers had
problems trying to estimate the yield loss they were suffering due
to GAS. 18 out of 94 farmers said they could not estimate the loss,
because they replanted missing hills immediately, and because of
other management methods. The estimated yield loss caused by
GAS mostly ranged 0–10% (64% of farmers), but higher estimates
were also common (10–30% loss: 13% of farmers; and 30–50% loss:
4% of farmers) (Fig. D.3).
The results of this study have confirmed that GAS, to this date, is
a pest that causes serious economic damage. Even if farmers often
reported yield loss below 10%, they admitted that management
remains an expensive and time-consuming duty. As mentioned
before, farmers in the Lào Cai region (VN 3, Vietnam) said they had
never seen GAS or its characteristic pink eggs. Furthermore, they
had never heard of a snail that ate rice plants. One of the farmers
told us that he sometimes collects snails in the valley to cultivate
them in his rice terraces. Without the knowledge of a rice-eating
snail, this habit could easily lead to spreading the pest.
The perception of GAS as one of the major pests in rice produc-
tion concurs with similar, but spatially more restricted surveys in
Thailand [15], in Ecuador [21], and also in the Ifugao region [27],
where farmers do not apply molluscicides and where the highest
yield losses were reported in our study (Fig. D.3). Interestingly,
according to a survey on GAS in the Ifugao region in 1997 [38],
farmers did not consider GAS a major pest about seven years after
its introduction into this region, and damages on rice plants were
observed rarely, although densities of GAS were already high then.
The farmers’ perception of GAS had already changed a few years
 J. Schneiker et al. / NJAS - Wageningen Journal of Life Sciences 79 (2016) 11–21
later [27], when GAS was considered a severe problem to rice pro-
duction and this is still apparent as our study indicates.
To get an impression of their attitude towards GAS, rice farm-
ers were asked if they saw any positive aspects to the snail being
introduced into their country or region (Fig. D.4). The majority of
the farmers (63%) negated this, while only 14% mentioned the pos-
sibility of using the snails as fodder for animals, and another 14%
mentioned that GAS is edible for humans. Only 8% rated the snail
as valuable, because it helped to control weeds. Almost all farmers
(97%) said that they used to eat native snails before the invasive
snail arrived in their region, but only 40% of the farmers said that
they would now eat GAS (Fig. D.5). The most common reasons
for not eating GAS was the taste (35% of nominations), that GAS
does not look appetizing (18%), or that farmers had heard of cer-
tain health issues (11%) when eating GAS, i.e. cancer or high blood
pressure. 21% of the respondents gave as a reason that they had
never tried eating the snail before at all. The number of farmers
who ate native snails at the time before GAS was introduced to
their region decreased from 97% to 82% who eat native snails today.
Farmers often added that native snails had become rarer since the
introduction of GAS, and some species had vanished altogether
from their regions (see also chapter 3.4). Farmers’ appreciation
of native snails as a food source could be utilized to promote a
molluscicide-free management by informing farmers that native
snail populations have gradually reappeared in rice fields after
implementing a reduction of insecticides [43], and they would do
so after the use of molluscicides was abandoned.
A project to establish GAS as gourmet food was launched in
Hawaii, where wild-caught snails were raised on a specialized
feed to improve their taste and afterwards tried with successful
results [56]. Furthermore, successful attempts have been reported
using GAS as animal feed, i.e. in freshwater prawn cultures in the
Philippines [6]. Three farmers from different regions said that they
boil the snails and feed them to their dogs. Dogs and cats regularly
suffer from allergic reactions to conventional pet food (cutaneous
adverse food reactions in dogs to beef, dairy products, chicken, and
wheat; and in cats to beef, fish, and chicken) [40]. Pet owners in
industrial countries often try really hard to find alternative foods.
Thus, trading the protein-rich GAS [26] as pet food on international
markets might be a very profitable marketing strategy. Especially
when customers are encouraged to buy pet food made from GAS,
emphasizing that in this way they support smallholder farmers and
pest control.
Farmers rarely knew the aspect of GAS as a weed control agent.
Efficient training methods could help to make farmers more aware
of this possibility, and teach them that, once the rice is old enough
to be no longer vulnerable, the snail can be spared to help con-
trol weeds. Former studies affirm that weed control through GAS
is viable, especially in organic rice cultivation [29].
3.4. The molluscicide dilemma
The application of molluscicides is very popular with farmers
and it is regularly applied early in the cropping season in contrast to
insecticides that are mostly applied only when pests are observed.
To manage GAS, 74% of 98 farmers used molluscicides. Farmers with
a longer experience in rice farming more frequently used mollusci-
cides (GLM, chi2 = 6.49, df = 1, p = 0.0109) and there was a significant
difference in the number of farmers who used molluscicides among
regions, particularly as no molluscicides were applied in the Ifugao
region (chi2 = 60.88, df = 5, p < 0.001).
A great variety of brands of molluscicides were mentioned, most
commonly containing metaldehyde or niclosamide as active ingre-
dients. In North Vietnam especially, farmers had no knowledge as to
the kind of molluscicide they were applying and did not recall brand
names. Generally, they bought the molluscicides that pesticide
15
Fig. 1. Variety of sustainable control methods against golden apple snails used by
farmers that applied molluscicides or did not do so, and for trained (grey boxes)
and untrained farmers (white boxes). Numbers in brackets represent the number of
farmers. There were no significant effects of experience in rice farming, molluscicide
use or training (GLMM, p > 0.05). The horizontal line shows the median, the bottom
and top of the box show the 25th and 75th percentiles, respectively, and the whiskers
show either the maximum value (without outliers) or 1.5 times the interquartile
range of the data. Outliers are indicated by points.
traders recommended, or products that were just available with the
risk of using illegal substances, these being even more hazardous
to the environment or the farmers’ health [30,10]. The variety of
sustainable management methods ranged from only one method
(mostly handpicking) to a maximum of applying eight different
sustainable methods (handpicking, crushing eggs, immersing the
eggs into water, using attractants, constructing canals to attract
and easily collect or crush snails, using wooden traps, replanting,
and releasing ducks onto the field; Table D.3). This, however, cov-
ers only a small number of sustainable methods recommended by
government authorities [9]. On average, farmers used 3.16 ± 1.65
(mean ± SD) sustainable management methods (Fig. 1; Fig. D.6).
Experience in rice farming, molluscicide application, and training
had no significant effect on the number of sustainable methods the
farmers used (GLMM, p > 0.05; Appendix E). Only region had a sig-
nificant effect on the number of sustainable methods (chi2 = 31.28,
df = 5, p < 0.001), with farmers in North Vietnam using fewer meth-
ods than in the other regions (Fig. D.6).
Of 92 respondents, most (53%) felt that molluscicides were most
effective in controlling GAS, while 15% answered it would be best
to use a combination of molluscicides and sustainable methods
(mostly handpicking) (Fig. D.7). However, 32% of the respondents
thought that one of the sustainable methods was the most effective
control method. When farmers were asked whether they thought
it was or would be necessary to use molluscicides to ensure enough
yield, 68% agreed, 26% disagreed and 6% said that they did not
know (Fig. D.8). Most farmers indicated that they are satisfied with
their recent GAS management (Fig. D.9). In the Ifugao region, how-
ever, where farmers do not apply pesticides, they were not satisfied
with their recent management (Fig. D.9) and several farmers even
pointed out that they would use molluscicides if they had access
to them. Thus, it seems that management of GAS could be a threat,
especially to the increasing demand for organic rice production as
the avoidance of chemical control appears to be difficult.
Farmers had different attitudes towards molluscicides (Fig.
D.10). 40% of 58 untrained farmers had no concern about using
molluscicides and 25% of their 20 trained peers. Other farmers
16 J. Schneiker et al. / NJAS - Wageningen Journal of Life Sciences 79 (2016) 11–21
mentioned concern. The most common concern related to chemi-
cal control were various health issues, almost equally distributed
among untrained (41%) and trained farmers (45%). Environmen-
tal concern (harming non-target organisms, the soil, or rice plants)
mentioned 35% of the trained farmers and 21% of the untrained
ones. Two farmers expressed general concern about using mollusci-
cides without defining the cause further. There were no significant
effects of experience, training, molluscicide use, their interactions
or region on the frequency of health and environmental concerns
(GLMM, p > 0.05; Appendix E). If only environmental concerns were
considered, there was only a significant interaction of experience
and molluscicide use (GLMM, chi2 = 3.91, df = 1, p = 0.0480). Less
experienced farmers who did not use molluscicides more often
mentioned environmental concerns than more experienced farm-
ers. In contrast, experienced farmers who used molluscicides more
often had concerns than their less experienced peers. Untrained
(9%) and trained farmers (15%) who did not have any concerns,
mentioned that molluscicides would not be harmful to the envi-
ronment (mostly restricted to fish and crabs). 5% of the trained and
7% of the untrained farmers without concerns, related this to the
fact that they used some kind of protection when applying mollus-
cicides.
The results of this study make it very apparent how heavily rice
farmers rely on molluscicides in controlling GAS. This is in line with
rice farmers in Ecuador where an overwhelming majority uses mol-
luscicides (49% of which were using the environmentally harmful
endosulfan), although the government supports sustainable snail
control [21]. To shift to a more sustainable management, one has to
start changing the farmers’ beliefs first of all. Even firmer belief for
the necessity of chemicals was voiced by rice farmers, when asked
about insecticides [17] in Nueva Ecija (PH 2, Philippines), where
97% thought insecticides were indispensable.
Farmers in our study were widely unaware of most of the natural
predators of GAS, which leaves them unaware of killing poten-
tial beneficial organisms when applying molluscicides and other
pesticides, especially ones that are not target-specific.
3.5. Knowledge gaps about GAS
To gauge their knowledge status concerning GAS, the respon-
dents (N = 94 including N = 22 trained and N = 72 untrained farmers)
were asked to answer 12 questions of varying difficulty. On average,
farmers were able to answer 68 ± 9% (mean ± SD) of the ques-
tions correctly (Fig. 2, Fig. D.11). There was a significant difference
in the number of correct answers according to the four levels of
difficulty of questions, as expected from our method of defining dif-
ficulty (GLMM, chi2 = 68.96, df = 3, p < 0.001). The number of correct
answers did not differ significantly according to experience in rice
farming, training, region, and the interaction of region:difficulty
(p > 0.05; Appendix E).
Farmers were able to answer easier questions about GAS cor-
rectly, but had the greatest difficulties in answering whether snails
transmit diseases (1% correct), how to tell the difference in sexes
(12% correct), if snails are more active at a shallow or deep water
level (this is important as managing water level at shallow depths is
a recommended cultural control method [50]) (20% correct), or how
long snails can survive in soil without water (57% correct). Farmer
respondents in our study showed definite knowledge gaps that had
not been covered in previous training campaigns. Although GAS are
still a topic in farmer workshops and field schools, it is no longer the
focus of interest, as the training efforts were mainly concentrated
in the 1990s when GAS first became a serious problem, then, after a
time, many campaigns subsided [30]. Hence, training efforts should
be renewed and revolutionized, based on latest research (see also
chapter 3.7).
3.6. Native mollusks at risk
The invasion of GAS can cause a drastic decline in the abun-
dance of native snails either by direct competition, predation or
by management methods applied by farmers [7,22]. Most farm-
ers (92% of 99 respondents) were well aware of a reduction in the
number of native snails in their region and some even mentioned a
decline in other freshwater organisms such as leeches, frogs and
fish. Molluscicides were mentioned as cause for the decline in
freshwater organisms and native snails, especially. Another farmer
mentioned that GAS consumed the native snails, which is in line
with recent research [22]. A reduction in species richness of snails
had been observed by 76% of the participants, while 21% said that
snail species remained the same and all species could still be found
since GAS became established in the area (3% could not answer).
A certain threat to native snails could be that farmers con-
found them with invasive apple snails and kill them altogether.
Asking farmers to indicate GAS on colored pictures of eight
snail individuals, including also native aquatic snails and another
invasive but terrestrial snail, farmers indicated more often GAS
individuals as GAS than other snails (GLMM, chi2 = 15.78, df = 1,
p < 0.001) with significant differences in nominations among pic-
tures (chi2 = 118.56, df = 6, p < 0.001; Fig. 3). However, farmers often
missed some GAS or indicated wrong species as the invasive pest
(Fig. 3, Table D.4). The two snails most frequently identified as
GAS were indeed correct. The third most frequently chosen snail
(50% of farmers), however, was a native apple snail (Pila ampul-
lacea). If farmers had no difficulty in identifying GAS, identification
of all of the four individuals should be at 100%. By relying heavily
on color in the identification (as indicated by 50% of 96 respon-
dents), farmers proved unable to differentiate between GAS and
native apple snails where shell morphology is reliable for identi-
fication (Fig. 3) [36]. Snails of a golden/yellow color with little or
no banding are much more likely to be recognized as GAS than
darker snails with strong banding. Color of P. canaliculata, how-
ever, is highly variable including unbanded and banded, as well as
bright or dark shells. We observed these various color morphs in
rice fields in our study regions, dark banded ones even more often.
This poses a problem insofar as farmers are likely to control native
apple snail species along with GAS with their handpicking practice,
even if they do not use molluscicides. Thus, they might further the
decline of native snail species, in particular native apple snails, and
destroy a food source for themselves, and important decomposers
in the rice ecosystem [47]. There was a difference in the num-
ber of nominations per farmer among regions (GLMM, chi2 = 19.85,
df = 5, p = 0.00133) with farmers from S-Vietnam (VN 4) nominat-
ing more pictures to be GAS (with the same proportion of wrong
and right nominations as in the other regions; Table D.4). Neither
experience in rice farming, nor training, or the interaction of expe-
rience:snail species (GAS or no GAS) had an impact on nominations
(p > 0.05; Appendix E). Therefore, species identification should be
better represented in farmer teaching courses. We want to empha-
size here, that teaching should involve real specimens rather than
photographs, as certain morphological features of shells relevant
for identification are hard to distinguish on pictures.
3.7. Synthesis and solutions for sustainable management of GAS
Farmers hold the strong belief that regular application of mol-
luscicides is unavoidable to achieve a satisfying control of GAS
in rice fields. The number of sustainable control methods applied
was in most cases low, often restricted to handpicking as the
only method known by farmers. Together with our finding that
knowledge about GAS biology and, especially, their identification
showed distinct gaps, and furthermore that for the farmers in our
study previous training on GAS management had no effect on GAS
 J. Schneiker et al. / NJAS - Wageningen Journal of Life Sciences 79 (2016) 11–21 17

Fig. 2. Proportion of correct answers of the respondents to the 12 knowledge questions about GAS biology, management and pest activity grouped in trained (N = 22, grey
boxes) and untrained farmers (N = 72, white boxes), and according to four levels of difficulty of questions. Training had no significant effect on the number of correct answers
(GLMM, p > 0.05).

Fig. 3. Identification of snail individuals on colored pictures as GAS by rice farmer respondents (N = 97 with N = 224 nominations). Among the eight pictures there were four
golden apple snails (Pomacea canaliculata, black bars), two native apple snails (Pila ampullacea, white bars) and two non-apple snails (grey bars): one aquatic native snail
(Filopaludina sumatrensis s.) and one terrestrial pest snail of field crops (Lissachatina fulica). The order of shells (from top to bottom) was the same as presented to farmers.
Shell pictures copyright by G. & Ph. Poppe.

knowledge, the application of sustainable management methods,
or concerns about using pesticides, we suggest that government
training courses should be renewed. Programs should focus on the
importance of sustainable management in GAS control to conserve
the environment and native invertebrates with special emphasis on
mollusks as important engineers in rice ecosystems, and as a free
additional protein-rich food for the local community. In addition to
the neutral effects of training on GAS management and knowledge
in our study, another big problem that became apparent was that
training reached only few farmers, despite great efforts of govern-
ments in the past [30]. Thus, it is essential to identify the best way
for dissemination of knowledge on GAS management that reaches
many farmers. In our study, the local community was an important
source for the first information about the pest, but also GAS traders,
18 J. Schneiker et al. / NJAS - Wageningen Journal of Life Sciences 79 (2016) 11–21
the government, and, in some regions, the media supplied informa-
tion (Fig. D.12). To arouse the farmers’ awareness for the hazards
of the pest, especially in regions where it has not yet arrived (e.g. in
our field sites in the Lào Cai region (VN 3, Vietnam)), suitable ways
to reach as many farmers as possible have to be found. In our study,
only 42% of the farmers were informed about GAS before it arrived
in their region, and as few as 11% were previously warned that it
was harmful to rice (Fig. D.13).
3.7.1. Entertainment − education
Studies proved that before implementing novel management
techniques, farmers have to alter their perceptions and beliefs [24].
As it became apparent from our study, where only very few farm-
ers informed themselves about GAS after they first had heard of
them (Fig. D.14), knowledge should be disseminated in an enter-
taining way so that farmers readily attend the lectures. According
to Heong et al. [18] rice farmers reduced their insecticide appli-
cation after listening to a radio soap opera that was developed
after an entertainment − education principle. A similar approach
to inform farmers about IPM in rice based on entertainment − edu-
cation was recently launched in the form of a comedy TV series in
the Mekong Delta region of Vietnam [19,12]. Videos provided on
public internet platforms have the potential to reach many indi-
viduals such as stakeholders and farmers. The International Rice
Research Institute (IRRI), for instance, is broadcasting videos on
IPM and other aspects of rice farming on its YouTube, LLC (Google
Inc.) channel (e.g. [25]). A similar campaign could be started to
change GAS management or it could be integrated into already
existing programs. However, while the above-mentioned TV series
were emphasizing e.g. a reduction of pesticide application to sus-
tain beneficial predators of pests, or to plant wild flowers on rice
field bunds to increase their abundance, in contrast, biocontrol of
GAS in rice fields by naturally occurring predators is less success-
ful than for insects, partly because of a lack of adaptation of native
predators to this invasive pest [63,61]. Sustainable management of
GAS requires labor-intensive work and a lot of time. Thus, farmers
who are used to control the snails with chemicals in a compara-
tively easy way, might be deterred. In addition, every year, there
is a constant high output of studies suggesting novel management
techniques to (sustainably) control GAS, such as laser levelling of
rice fields, seedling broadcasting or reducing seed densities in nurs-
ery beds [23,25,62]. Thus, TV series or webcasts on sustainable GAS
management might be outdated quickly. This is of particular con-
cern if treatments considered to reduce GAS numbers, turn out to
promote their populations in the longer-term, as is the case for
the impact of fertilizer on GAS [9,53]. The use of public media to
educate farmers can be seen problematic for farmers with limited
access to media, particularly, in low-income regions. In our study
regions, many farmers did not own a radio or had internet access
(Fig. D.15). In the Lào Cai Province (VN 3, Vietnam), for instance,
only half of the households owned a TV and none of them have
internet access. Furthermore, these videos are often produced in
either a local language and/or in English, which is further limiting
their large-scale dissemination to farmers due to language barriers.
In conclusion, TV series or webcasts on IPM of GAS might success-
fully advance the sustainable management knowledge of farmers,
but we have to emphasize that this approach holds some distinct
limitations and difficulties, as well.
3.7.2. Community cooperation
Several farmers stated that they partly abandoned physical con-
trol of GAS, because it was only effective if the whole community
applied it simultaneously, as the snail would otherwise invade their
paddies from neighboring fields. However, rice even on a small scale
is often planted at different times, and therefore farmers will not
control the snail when their rice plants are not vulnerable, proba-
bly, except the whole community is cooperating under a competent
governance. Simultaneous pest control for the whole community
has been suggested for ecologically based rodent management in
rice, in which neighbors were compelled to work together to con-
trol rats on a village-scale through a trap-barrier system [51]. The
experiment showed additional benefits for the farmers, such as
an increased yield, less control costs, and application of a lower
amount of rodenticides. Similarly, Greene [15] evaluated the suc-
cess of community centers in Thailand to promote sustainable
management of GAS. Farmers from villages with community cen-
ters applied fewer molluscicides, but achieved similar rice yields
in comparison with control groups without community centers.
Community members also applied more sustainable management
methods, and successfully transferred their knowledge to other
farmers in the same villages. Cooperation of community members,
based on place-based cooperatives, community-supported agricul-
ture, and strong community leadership has proven for even a whole
smallholder farmers’ community a successful way to switch from
conventional to sustainable/organic rice production [54]. Thus,
approaches initiating community cooperation, such as commu-
nity centers, might be a promising approach to achieve sustainable
management of GAS. However, similar to farmer field schools, gov-
ernments have to invest money in establishing such centers, and
they have to maintain them for a longer time. This will probably
restrict their large-scale distribution, as only a limited number of
community centers can be established. On the other hand, farm-
ers might be willing to compensate for the costs of IPM training.
Farmers in Nepal, for instance, were willing to pay 25.23 USD per
household for a five-day community IPM training [1].
3.7.3. Golden apple snail management and utilization company
(GASMUC)
While novel methods in knowledge dissemination have some
potential to facilitate sustainable management of GAS, they are
strongly limited by the labor individual farmers can contribute
to this time-consuming duty. This is even more relevant for
community cooperation where all farmers are required to apply
sustainable methods, even if their time is strongly restricted. In
the following, we elaborate an economic solution to overcome this
limitation.
For a profitable management solution in controlling GAS, farm-
ers suggested to buy ducks with contributions from the community,
and to employ a caretaker who would be paid with the money from
selling the duck eggs. The ducks would be released on the rice fields
of the municipality to support snail control. Traditional rice-duck
and also rice-fish production systems are promising ways to foster
sustainability in rice ecosystems, which also provide biocontrol of
GAS [60,34,55], but various local and regional political, economic,
and social constraints in the establishment of these systems have
to be taken into consideration [55]. Another respondent from Ha i
Duo’ng Province mentioned that farmers jointly payed a company,
which was taking over rat control in rice fields for the whole vil-
lage. Here, we propose that a similar model could be applied to the
management of GAS.
Local companies could offer community-wide sustainable and
simultaneous control in combination with commercialization of
the pest snail (Fig. 4). Such companies would create new jobs in
rural areas and relieve farmers from this time-consuming work.
We propose the term Golden Apple Snail Management and Utiliza-
tion Company (GASMUC) for this enterprise. There must be a close
cooperation of the company and crop research institutes, who teach
the managers of the companies on GAS biology and management,
and who convey the philosophy of sustainability. Regular brief-
ings of managers should take place to keep GASMUCs up to date
with the rapidly increasing knowledge on GAS. The costs for GAS
management on the community’s rice fields are to be distributed
 J. Schneiker et al. / NJAS - Wageningen Journal of Life Sciences 79 (2016) 11–21 19

Fig. 4. Model of a local company, called GASMUC, which specializes on sustainable management of GAS and its utilization for a whole municipality, and contributing to
the conservation of native mollusks in rice fields. Pictures (from left to right) show (1) native apple snails (Pila ampullacea), which can hardly be found in GAS invaded rice
fields due to GAS management and competition with GAS; sustainable control methods: (2) screens on water inlets and outlets of rice fields preventing dispersal of GAS, (3)
bamboo sticks installed in rice fields to enforce egg deposition of GAS which are then collected and eggs are crushed, (4) Taro leaves used as attractants to collect GAS, (5)
ducks herded in a rice field to consume GAS; and the utilization of GAS: (6) GAS consuming weeds in rice fields, and (7) apple snails sold on a food market in Vietnam.

among the owners of fields according to the size of their paddies. As
GASMUC is operating management on a large scale within a munic-
ipality, in contrast to single rice fields of smallholder farmers, they
can purchase materials in bulk, such as GAS baits, traps and more
expensive but environment-friendly molluscicides, at a lower price.
The government might have to grant a loan, which, however, could
be refunded, once the company realizes profit. On the other hand,
governments are advised to give financial support to farmers if they
support environmental services [13], and the same should be true
for companies promoting agricultural sustainability.
Rice fields and irrigation channels of all community farmers are
managed by GASMUC with sustainable methods simultaneously,
even if rice is not vulnerable at that time in some fields to prevent
spillovers of GAS. Connecting waterways between a GASMUC-
controlled municipality and conventionally managed neighboring
municipalities must be screened off. Ducks are kept by GASMUC
and are used to control GAS; in addition, proceeds are generated
by selling meat and eggs. The great mass of GAS retained from
molluscicide-free habitats can be sold on local markets for human
consumption or as animal fodder; excesses can be sold on global
markets (e.g. also to novel markets like the pharmaceutical indus-
try for the production of the natural anti-oxidant Astaxanthin from
GAS [4], or for biodiesel production [37], or as food for carnivorous
pets (see chapter 3.3)). Further possibilities for GASMUC could be a
cooperation with local restaurants and households which must be
taught the suitable preparation of the snails to increase their taste
[56,26], and GASMUC could help advertising GAS as a gourmet food.
Whenever feasible, GAS should be spared in times when rice plants
are not vulnerable to allow weed control by GAS [29].
GASMUC will be able to safeguard the declining populations
of native apple snails [7] by species identification, which seems
particularly challenging farmers (see chapter 3.6), and by sub-
sequently sparing these individuals during snail management.
GASMUC could further use its knowledge to reestablish populations
of non-harmful native snails in rice fields once molluscicide appli-
cation is abandoned, and also by teaching locals in conservation
issues. The success of such restoration programs should be eval-
uated by research. For these conservative actions, GASMUC could
receive further payments from the government. Once populations
are established, native snails can then be harvested carefully as
well, as GASMUC will regularly collect them along with GAS (e.g.
in traps). Farmers should receive a fair share in the proceeds from
native snails, so that farmers do not get the impression that GAS-
MUC is stealing their goods. In general, as GASMUC will be making
money from selling GAS, the temptation to breed them commer-
cially is great. Thus, a transparency of the actions of GASMUC is
required. Representatives of the government and the municipal-
ity should have access rights to the facilities of GASMUC to control
that laws (e.g. prohibition of GAS breeding) are strictly followed.
A governmental certificate for GASMUC could be provided, which
signalizes farmers the support of the government and decreases the
chances of companies which might control GAS non-sustainably to
compete with GASMUC. Official certification could also promote
the profitability of rice-duck production systems [55]. Should GAS-
MUC violate the goal of sustainability in GAS management, the
government could impose sanctions, such as the withdrawal of the
certificate, knowledge dissemination or financial support.
GAS management by GASMUC needs to be adaptable to a great
extent to account for regional and local socio-economic and legal
requirements. The efficiency of GASMUC as to sustainability and
profitability should be experimentally verified. If the company is
considered a success, a network of interconnected GASMUCs could
be established, with sinking prices. Given that an international
GASMUC network is established, managers should speak a com-
mon language, such as English, to disseminate new advances in
GAS management among them, especially via public webcasts (see
above) provided by national and international research institutes,
instead of costly regular on-site briefings. Finally, GASMUC could be
implemented into a larger framework for organic rice production
within the respective community [54]. In this way, the knowl-
edge of GASMUC could also promote landscape modifications, e.g.
irrigation channels can be constructed or maintained to harbor a
greater biodiversity, including natural predators of GAS, which can
successfully reduce the population densities of the pest [16]. This
consideration is particularly important as governments in SE-Asia
even recommend a large-scale application of molluscicides to con-
trol various snail species to contain the spread of snail-transmitted
human disease vectors [32]. This approach is also interfering with
20 J. Schneiker et al. / NJAS - Wageningen Journal of Life Sciences 79 (2016) 11–21
the goals to reestablish native snail populations in rice production
landscapes.
3.8. Snail management and the natural environment
GAS have not only invaded rice fields in SE-Asia, but almost
any water body including natural streams, ponds, and lakes. In a
survey on invaded natural wetlands in Thailand, Carlsson et al.
[5] demonstrated that the state and function of the habitats are
strongly altered by the invasive snail, which consumes aquatic
plants almost completely, enhancing nutrient concentrations in the
water, and facilitating the growth of algae. This ecosystem change
likely has also strong negative effects on the native animals depend-
ing on these habitats [5]. Thus, management of GAS should not be
restricted to rice fields, but should also incorporate natural wet-
land habitats within rice dominated landscapes. In addition, as rice
fields are connected to natural wetlands by irrigation canals, mol-
luscicides applied in paddies will also enter these habitats and affect
native mollusk populations with cascading effects on decomposi-
tion, or on predators feeding on mollusks [47]. Rice fields occupy
32% of the total crop land, assessed in 13 countries in SE- and S-Asia
(range 11–84%; almost one million km2 in total) [59]. Most irrigated
rice production areas were established on shallow marshes, often
centuries ago, and are therefore considered agronomically man-
aged marshes, rich in biodiversity, particularly of invertebrates [2].
Thus, rice fields have vastly substituted shallow natural wetlands
in SE-Asia and are now the dominant habitat for aquatic organisms
living in stagnant water and need to be protected by a sustainable
management, not harming the indigenous fauna and flora. Reduc-
tion of pesticide application, including molluscicides, will therefore
help to protect biodiversity in these agroecosystems.
Acknowledgements
We thank all the colleagues and translators who helped us with
the interviews, all the farmers who took part in the survey and gave
us very good suggestions, and G. & Ph. Poppe (Conchology, Inc.)
for giving us the permission to use their snail pictures. C. Türke
contributed to the linguistic improvement of the manuscript. The
work was funded by the German Federal Ministry for Education
and Research (BMBF funding measure “Sustainable land manage-
ment”) within the LEGATO-project (Funding codes 01LL0917A until
01LL0917O).
Appendix Supplementary data
Supplementary data associated with this article can be found, in
the online version, at http://dx.doi.org/10.1016/j.njas.2016.07.001.
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