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The current trend in biological control approaches in the mitigation of golden

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 Biological Control 175 (2022) 105060

Contents lists available at ScienceDirect

Biological Control
journal homepage: www.elsevier.com/locate/ybcon

The current trend in biological control approaches in the mitigation of

golden apple snail Pomacea spp.
Wahizatul Afzan Azmi a, c, 1, Shing Ching Khoo a, 1, Lee Chuen Ng b, Nursalwa Baharuddin a, c,
Azlina Abd Aziz d, Nyuk Ling Ma a, *
a
Faculty of Science & Marine Environment, Universiti Malaysia Terengganu, Malaysia
b
Faculty of Fisheries and Food Science, Universiti Malaysia Terengganu, Malaysia
c
Institute of Tropical Biodiversity & Sustainable Development, Universiti Malaysia Terengganu, Malaysia
d
Faculty of Business, Economics and Social Development, Universiti Malaysia Terengganu, Malaysia

H I G H L I G H T S

• Climate change is expected to worsen GAS infestation and threaten food security.
• Entomopathogenic fungi and nematodes are potential GAS biological controls.
• Integrated and precision pest management improved pest monitoring system.

A R T I C L E I N F O A B S T R A C T

Keywords: Golden apple snails (GAS) (Pomacea spp.) is one of the major pests that rampantly invaded many countries and
Pomacea canaliculata brought a heavy bloom to agricultural cultivation. Their invasion had resulted in huge crop damage and ulti­
Pomacea maculate mately caused massive economic loss. For the past few decades, many strategies had been developed to overcome
Entomopathogenic interaction
the GAS infestation. Among all the strategies, chemical synthetic molluscicides had been the mainstay within the
Precision pest management
Integrated pest management
farmer community. Despite their effectiveness in controlling the GAS infestation, extensive use of chemical
molluscicides has negative impacts on humans, non-targeted organisms, and the environment. Climate change is
expected to hasten the reproduction of GAS, necessitating the development of more sustainable GAS mitigation
strategies. This paper examines the current stage of GAS invasion and its implications for global rice production.
This review also includes an in-depth discussion of the various potential biological based strategies involved in
pest management, and the recent technological breakthroughs in entomopathogenic nematodes and entomo­
pathogenic fungi as molluscicides, integrated pest management, and precision pest management. To summarize,
this review provides a potential trend in the use of biocontrol as a substitute for chemically manufactured
synthetic molluscicides for the sustainable management of GAS.

1. Introduction deliberately introduced or distributed to many continents such as Africa,

South and Central America and Asia as food sources and aquarium trade
Golden apple snails (GAS) Pomacea spp. or ‘siput gondang emas’ are in the early 1980s (Hayes et al., 2015). In the mid of 1990s, the snail-
freshwater snail native to South America, particularly Uruguay and farming projects were abandoned due to low market demands for food
Argentina (CABI, 2021). They belong to the family Ampullariidae sources. This scenario caused the extensive growth of GAS to be left into
encompassing the largest freshwater snails (up to 17 cm). Among the the water system and finally ravaged rice crops (Naylor, 1996). GAS was
members of this family, Pomacea canaliculata and Pomacea maculata established in large populations which later became the most prob­
have been identified as the most invasive species (International Rice lematic invasive species in many Asia regions (CABI, 2021). GAS have a
Research Institute, 2020). Several Pomacea species were accidentally or significant impact on agriculture, economics, the environment, and

* Corresponding author.
E-mail address: [email protected] (N.L. Ma).
1
Authors who have worked together on a publication and contributed equally.

https://doi.org/10.1016/j.biocontrol.2022.105060
Received 11 February 2022; Received in revised form 19 August 2022; Accepted 15 September 2022
Available online 21 September 2022
1049-9644/© 2022 Elsevier Inc. All rights reserved.
W.A. Azmi et al. Biological Control 175 (2022) 105060

Fig. 1. World map regional comparison of rice crop production (tons), golden apple snail (GAS) invasion (labelled as native, introduced, and invasive) and dis­
tribution pattern (regionally presented in blue map) in the year 2019/2020. Data gathered from (CABI, 2021; Knoema, 2020).

potential health issues. Several countries have taken steps to reduce the spent on pesticides to control GAS (Yahaya et al., 2017). In Japan,
invasion, such as limiting GAS transit between islands in the Hawaiian estimated cost for GAS control was USD 64,385 for 176 ha of rice field
archipelago and across the United States (Gaston, 2006). (Mochida, 1991). From a socioeconomic perspective, GAS interfere with
GAS has now become one of the most serious paddy pests in many economic activities and impact human well-being. The loss of income is
countries with high agricultural production, threatening farmers’ live­ the most significant socioeconomic impact because the welfare of
lihoods (Phoong et al., 2018; Rahim and Joshi, 2019). GAS eat up most farmers is the government’s primary concern since many of the paddy
of the young and newly emerging seedlings, ruin the stem of the rice farmers are in the lower-income group. The damage caused by GAS is
plant, further destroying the whole rice plant (International Rice extensive, and economic losses are massive due to the cost of pest con­
Research Institute, 2020). Almost all Asia countries are severely affected trol and replanting. Invasive GAS demonstrated great negative impacts
by serious agricultural crop damage by GAS (Fig. 1 and Table 1). At least on the native biodiversity of snails and wetland ecosystem (Carlsson
18 provinces in China, the world’s largest rice producer with 211 million et al., 2004; Phoong et al., 2018). The invasion of GAS influenced human
tonnes produced in 2019, or 27.92 % of all rice produced worldwide, health such as causing symptoms that are similar to bacterial meningitis
have reportedly suffered economic losses as a result of the GAS invasion if eaten raw as they can act as an active vector for parasites such as rat
(Yang et al., 2018). In addition, rice losses in Taiwan increased quickly lungworms Angiostrongylus cantonensis (Chaichana and Joshi, 2018;
from USD 2.7 million in 1982 to USD 30.9 million in 1986 (Mochida, Yang et al., 2013b; Lv et al., 2018).
1991). For Africa region, the annual economic loss of rice production in Furthermore, climate change has had a significant impact on the
Ethiopia, Tanzania and Uganda are estimated to range within 67–116 spread of P. canaliculata, it is expected that GAS will become more severe
million USD (Djeddour et al., 2021). An estimation of USD 1.2 billion of in the future. According to a mathematical prediction model, when the
annual economic losses has been reported in the Philippines and about representative concentration pathway (RCP) of greenhouse gas con­
28 million crop damages had been reported in Malaysia in 2010 (Joshi centration is RCP 2.6, which means if the global mean temperature is
and Ratcha, 2018; Yahaya et al., 2017). Individual GAS consumes 7–24 maintained within 2C change, will cause an increase of 3.35 % and 3.8 %
rice seedlings per day, resulting in a severe drop in rice productivity in of P. canaliculate in the 2050 s and 2080 s, respectively. The worst
many ASEAN (The Association of Southern East Asia Nation) countries. climate scenario, RCP 8.5 track, will, however encourage an increase in
As all ASEAN countries rely on rice as a staple diet, this has become the P. canaliculate of 8.7 % (Lei et al., 2017). Therefore, this review in­
primary challenge to food security (Salleh et al., 2012). vestigates the available biological control approaches for long-term GAS
Aside from agricultural loss, extensive expenses are required to be mitigation.

2
W.A. Azmi et al. Biological Control 175 (2022) 105060

Table 1
An overview of top 25 rice production countries and global GAS native countries with their distribution of GAS including its origin and invasive pathway and first
reported year.
World Rice Production Country (Continent) Total Rice Origin Invasive pathway First reported Reference
Ranking in 2019 Production (tonnes) year

1 China (Asia) 211, 405.21 Invasive Food 1981 (Halwart, 1994; Yang et al., 2018)
consumption
Anhui Invasive Food 1981 (Yang et al., 2018)
consumption
Chongqing Invasive Food 1985 (Mochida, 1991)
consumption
Fujian Invasive Food 1988 (Mochida, 1991)
consumption
Guangdong Invasive Food 1982 (Halwart, 1994)
consumption
Guangxi Invasive Food 1985 (Karraker and Dudgeon, 2014)
consumption
Guizhou Invasive Food 1985 (Lv et al., 2011)
consumption
Hainan Invasive Food 1983 (Lv et al., 2011)
consumption
Hubei Invasive Food 1981 (Lv et al., 2011)
consumption
Hunan Invasive Food 1981 (Karraker and Dudgeon, 2014)
consumption
Jiangsu Invasive Food 1981 (Lv et al., 2011)
consumption
Jiangxi Invasive Food 1985 (Lv et al., 2011; Mochida, 1991)
consumption
Shanghai Invasive Food 1985 (Lv et al., 2011)
consumption
Sichuan Invasive Food 1985 (Lv et al., 2011)
consumption
Yunnan Invasive Food 1985 (Mochida, 1991)
consumption
Zhejiang Invasive Food 1981 (Mochida, 1991)
consumption
Hong Kong Introduced Food 1979–1981 (Mochida, 1991)
consumption
2 India (Asia) 177,645.00 Introduced Aquarium trade 1995 (Baker, 1998)
3 Indonesia (Asia) 54, 640.03 Introduced Pet and aquarium 1984 (Marwoto et al., 2018; Mochida,
trade 1991; Suharto, 2002)
Java Introduced Pet trade 1989
Lesser Sunda Islands Introduced Pet trade –
Sulawesi Introduced Pet trade –
Sumatra Introduced Pet trade 1989
4 Bangladesh (Asia) 54, 586.34 Introduced Food – (Baker, 1998)
consumption
5 Vietnam (Asia) 43, 448.50 Introduced Aquarium trade 1988 (Duong, 2006; Loiseau, 2009)
6 Thailand (Asia) 28, 356.87 Introduced Aquarium trade 1982–1990 (de Brito and Joshi, 2016; Greene,
2008)
7 Myanmar (Asia) 26, 269.81 Invasive Aquarium trade 1990 (Hayes et al., 2008)
8 Philippines (Asia) 18, 814.83 Introduced Food 1980–1982 (Mochida, 1991)
consumption
9 Pakistan (Asia) 11, 115.43 Introduced Aquarium trade 2012 (Marwoto et al., 2018; Suharto, 2002)
10 Cambodia (Asia) 10, 886.00 Introduced Aquaculture 1985 (Ranamukhaarachchi and
pathways Wickramasinghe, 2006)
11 Japan (Asia) 10, 527.00 Introduced Food 1981 (Mochida, 1991; Wada, 2004)
consumption
Honshu Food 1981
consumption
Kyushu Food 1981
consumption
Ryukyu Islands Food 1981
consumption
Shikoku Food 1981
consumption
12 Brazil (South America) 10, 368.61 Introduced Dispersion (CABI, 2021)
Mato Grosso Introduced Dispersion – (CABI, 2021)
Rio Grande do Sul Introduced Dispersion – (CABI, 2021)
Sao Paulo Introduced Dispersion (CABI, 2021)
13 Nigeria (Africa) 8, 435.00 Absent record – – –
14 United States (North 8, 376.72 Introduced Aquarium Trade 1987–2000 (Howells and Smith, 2002)
America
Alabama Introduced Aquarium trade – (Rawlings et al., 2007)
Arizona Introduced Aquarium trade – (Rawlings et al., 2007)
California Introduced Aquarium trade 1997 (Howells et al., 2006)
(continued on next page)

3
W.A. Azmi et al. Biological Control 175 (2022) 105060

Table 1 (continued )
World Rice Production Country (Continent) Total Rice Origin Invasive pathway First reported Reference
Ranking in 2019 Production (tonnes) year

Florida Introduced Aquarium trade 2007 (Rawlings et al., 2007)

Georgia Introduced Aquarium trade – (Rawlings et al., 2007)
Hawaii Introduced Aquarium trade 1989 (Rawlings et al., 2007)
Louisiana Introduced Aquarium trade – (Rawlings et al., 2007)
South Carolina Introduced Aquarium trade – (Rawlings et al., 2007)
Texas Introduced Aquarium trade 2000 (Rawlings et al., 2007)
15 Egypt (North Afrika) 6, 690.00 Absent / invalid – – (CABI, 2021)
record
16 Nepal (Asia) 5, 610.01 Introduced Aquarium trade – (Budha, 2014)
17 Republic of Korea (Asia) 5, 016.08 Introduced Aquaculture 1981 (Mochida, 1991)
pathway
18 Sri Lanka (Asia) 4,592.06 Introduced Aquarium trade 1982 (Mochida, 1991)
19 Madagascar (Africa) 4, 231.15 Introduced Aquarium trade – (Djeddour et al., 2021)
20 United Republic of 3, 474.77 Introduced Aquarium trade – (Djeddour et al., 2021)
Tanzania (Africa)
21 Laos (Asia) 3, 438.00 Introduced Food 1991 (de Brito and Joshi, 2016)
consumption
22 Mali (Africa) 3, 196.34 Introduced Aquarium trade – (Djeddour et al., 2021)
23 Peru (South America) 3, 188.31 Introduced Aquarium trade –
24 Columbia (South 3, 012.31 Introduced Aquarium trade – (Hayes et al., 2012)
America)
25 Malaysia (Asia) 2, 912.20 Introduced Food (Rahim and Joshi, 2019)
consumption
Penisular 1987 (Phoong et al., 2018)
Sabah 1992 (Teo, 2003)
Sarawak 1987 (Yahaya et al., 2017)
33 Uruguay (South 1, 200.00 Native – – (Hayes et al., 2008)
America)
34 Argentina (South 1, 189.00 Native – – (Hayes et al., 2008)
America)

All data related to rice production and country ranking obtained from Knoema (2020). - denotes for data not available.

Fig. 2. Life cycle of golden apple snails.

2. The biological background of golden apple snails (GAS) the world due to its high reproductive capacity, voracious appetite,
resistance to drought and is an active vector for zoonotic diseases
Effective GAS management involves the biological knowledge in­ (Djeddour et al., 2021; Global Invasive Species Database, 2022). GAS
tegrations on GAS including its natural enemy, alternate hosts, life cycle possesses a high growth rate and high reproduction ability in a short life
and seasonal abundance. GAS has short life cycle and reproduce rapidly cycle (about 2 months) (Fig. 2). The mating process of adult GAS occurs
within 60 days. They demonstrated opportunistic feeding behaviors by within 3–4 h at any time with the presence of water in ambient envi­
feeding on delicate rice seedlings and rarely damage old plant. Once ronment conditions (Philippine Rice Research Institute, 2001). The
introduce into a new region, GAS reproduce in high abundance by reproduction rate of GAS is greatly reduced in the cold region especially
dispersing through wetland and waterways (Horgan et al., 2014). small juveniles who are vulnerable to low temperature (Yoshida et al.,
P. canaliculata had been listed as the top 100 worse invasive species in 2009). The connection of key regulatory elements and population

4
W.A. Azmi et al. Biological Control 175 (2022) 105060

Table 2 to the reddish-orange shell pigmentation with a round edge at the shell
The application of natural enemies in controlling GAS. aperture while P. canaliculata has larger unpigmented angulation on the
Natural Zoological Name Predates Reference shell aperture (Hayes et al., 2012). P. maculata produces higher number
Enemies Stage of of eggs with smaller hatchlings compared to P. canaliculata (Hayes et al.,
GAS 2012). The length and width of eggs mass of P. maculata and
Amphibian P. canaliculata range from 3.7 to 5 cm and 2.2–2.3 cm respectively
Turtle Chimneys reevesii Eggs, (Yoshie and Yusa, 2008) (Abdullah and Reyhan, 2017). However, due to the similarity of
Juvenile, P. canaliculata and P. maculata, molecular analyses are required to
Adult
Mauremys japonica Juvenile, (Yusa et al., 2006)
confirm their identities (Rama Rao et al., 2018). Nuclear DNA
Adult sequencing with elongation and morphological observation with high
Pelodiscus sinensis Eggs, (Dong et al., 2012) imaging technology was used to reveal the taxonomical information,
Juvenile hybridization activity and diversity of several Pomacea spp. such as
Trachemys scripta Eggs, (Guo et al., 2017a)
P. maculata, Pomacea insularum, and P. canaliculata (Matsukura and
elegans Juvenile
Annelida Wada, 2017).
Leech Whitmania pigra Eggs (Guo et al., 2017b) Aquatic pH can influence the distribution and survivability of
Bird Pomacea spp. (Byers et al., 2013; Ito, 2002). Acidic water reduces the
Asian Openbill Anastomus oscitans Eggs (Sawangproh and population density of aquatic organisms (Bemvenuti et al., 2003). In
Poonswad, 2010)
Ducks Anas playyrhynchos Juvenile, (Teo, 2001; Yusa et al.,
addition, high salinity reduces the physiological functions of Pomacea
Sub-adult 2006) spp. and hence limit their distribution (Costil et al., 2001). Food avail­
Crustaceans ability is the main factor affecting the number of offspring produced by
Crab Eriocheir japonicus Juvenile (Yusa et al., 2006) female P. canaliculate (Estoy et al., 2002). Calcium is required for shell
Geothelphusa dehaani Adult snails
development and protection against shell erosion (Glass and Darby,
Crayfish Procambarus clarkii Juvenile, (Yusa et al., 2006)
Adult snails 2008; Kwong et al., 2008). Nevertheless, genome analysis of GAS reveals
Shrimps Macrobranchium Adult (Savaya-Alkalay et al., their high adaptation and plasticity to the environment due to DNA/
formosense 2018; Yusa et al., 2006) hAT-Charlie transposable elements, the expansion of P450 family and
Fish the constitution of the cellular homeostasis system. In addition, activa­
Carps Cyprinus carpio Juvenile, (Ben-Ami and Heller,
tion of perivitelline genes in the ovary and albumen ensure the nutrient
Carassius gibelio Sub-adult 2001; Kelvin et al.,
Mylopharyngodon 2014; Yusa et al., 2006) supply in the egg and activation of diverse genes in gut microbiota for
piceus food digestion and xenobiotics degradation represent the most powerful
Chubs Zacco temmincki Juvenile, (Yusa et al., 2006) defence strategies of GAS (Liu et al., 2018).
Zacco platypus Sub-adult
Dace Tribol- odon Juvenile, (Yusa et al., 2006)
hakonensis Sub-adult 3. Biological strategies in GAS mitigation
Green Tetraodon nigroviridis Juvenile, (Guo et al., 2016)
pufferfish Sub-adult There are two general forms of biological strategies (biological
Gudgeons Pseudogobio esocinus Juvenile, (Yusa et al., 2006) control and bio-rational control) in pest control management (Barua
Pungtungia herzi Sub-adult
et al., 2021). Biological control is the use of natural enemies such as
Pseudorasbora parva
Pearl cichlid Geophagus brasiliensis Juvenile, (da Silva and pathogen, parasites, predators and competitors to suppress the popula­
Sub-adult Figueiredo, 2014) tion of targeted species such as GAS in this context (Fahad et al., 2015),
Sleeper Eleotris oxycephala Juvenile, (Yusa et al., 2006) whereas the bio-rational control employed the products from natural
Sub-adult
source such as plant extract for pest control purpose (Haddi et al., 2020).
Tilapia Oreochromis niloticus Juvenile, (Halwart et al., 2014;
Clarias gariepinus Sub-adult Yusa et al., 2006)
Juvenile, (Su Sin, 2006) 3.1. Biological control
Sub-adult
Insect In biological control strategies, GAS is viewed as a source of food for
Ants Solenopsis geminata Eggs (Yusa, 2001)
Pheidologeton spp.
organisms living in the same habitat, such as birds, ducks, waders, and
Diving Bees Cybister japonicus Small (Yusa et al., 2006) prey birds such as kites and egrets (Ranamukhaarachchi and Wickra­
juvenile masinghe, 2006). The list of natural enemies in controlling GAS had
Aquatic Anax parthenope Small (Yusa et al., 2006) been summarized in Table 2. Majority of the enemies attack GAS
Dragonflies Macromia amphigena juvenile
through eating or destroy of GAS egg, juvenile and parasite the adult
Pantara flavescens
Grasshoppers Conocephalus Eggs (Joshi et al., 2001) snails. For instance, some red ants feed on eggs and newly hatched
longipennis snails, while rats and snakes also prey on GAS (De La Cruz et al., 2001;
Conocephalus Ngoc, 2002; Yusa, 2001). Rice-fish farming system and rice-duck
maculatu farming showed significant success in controlling GAS in the open rice
Mammals
Rat Rattus norvegicus Juvenile (Yusa et al., 2000)
field (Abdullah and Reyhan, 2017; Joshi, 2007; Liang et al., 2014; Su
Sub-adult Sin, 2006; Teo, 2001).
Reptile Despite a large variety of predators, only a small number of natural
Caiman Lizard Dracaena spp. Eggs (Perera and Walls, enemies are of importance to scientific slug control studies. Entomo­
1996)
pathogenic nematodes (EPN) and entomopathogenic fungi (EPF) as
biological control become more favorable due to ease of application,
dynamics across different temporal regions appears to be crucial in GAS mass production, low cost, biodegradable and environmentally friendly
control (Yoshida et al., 2009). (Alramadhan and Mamay, 2019; Ibrahim and Bakry, 2019).
The two GAS species that are most frequently recorded are P.
canaliculata and P. maculata. P. maculata grows relatively faster and 3.1.1. Entomopathogenic nematodes (EPNs)
mature earlier compared to P. canaliculate (Arfan et al., 2015). The adult Entomopathogenic nematodes (EPNs) are nematodes that parasitize
P. maculata is differentiated from P. canaliculata through their yellowish and control insects. The application of EPNs in pest management of
gastropods shows an emerging trend but has not been well studied

5
W.A. Azmi et al. Biological Control 175 (2022) 105060

Table 3 Table 3 (continued )

The overview of current research on the association of entomopathogenic Entomopathogenic Targeted Mitigation References
nematodes with targeted mollusk species. nematodes mollusk species mechanism
Entomopathogenic Targeted Mitigation References Heterorhabditis Bradybaena Physiological (Tunholi et al.,
nematodes mollusk species mechanism indica similaris alteration 2014)
Angiostrongylus Pomacea Parasitic towards (Yang et al., Hugotdiplogaster Athoracophorus Parasitic to host slug (Morand and
cantonensis canaliculated host snails 2013b) neozelandia bitentaculatus Barker, 1995;
(GAS) Sudhaus,
Phasmarhabditis Pomacea Change of protein (Montanari 2018)
hermaphrodita canaliculated expression (PC-bpi) et al., 2020) Neoalloionema Cyclophoridae Parasitic towards (Ivanova et al.,
Pomacea – Reduction of (Boraldi et al., tricaudatum spp. juveniles of snails 2016)
canaliculated functional protein 2021) Phasmarhabditis Theba pisana Genetic variation in (Tandingan De
– Influence californica bacterial associates Ley et al.,
cytoskeletal of the nematodes 2020)
dynamics Phasmarhabditis Theba pisana Genetic variation in (Tandingan De
– Change of energy papillosa bacterial associates Ley et al.,
metabolism of the nematodes 2020)
Parmacella ibera Nematodes infection (Saeedizadeh Pellioditis Discus rotundatus Parasitic towards (Morand et al.,
and Niasti, hermaphrodita host snails 2004)
2020) Eobania Parasitic towards (Azzam, 2006)
Deroceras Nematodes infection (Tandingan De vermiculata host snails
reticulatum Ley et al., Euomphalia Parasitic towards (Azzam, 2006)
2014; Wilson strigella host snails
et al., 1993) Helix pomatia Parasitic towards (Morand et al.,
Deroceras Larval parasitic (Mc Donnell host snails 2004)
reticulatum et al., 2020) Monacha Parasitic towards (Morand et al.,
Deroceras Inhibition of feeding (Cutler and cartusiana host snails 2004)
reticulatum mechanism of snails Rae, 2020; Rae Neohelix Parasitic towards (Sudhaus,
et al., 2006) albolabris host snails 2018)
Deroceras Nematode infection (Cutler and Oxychilus Parasitic towards (Morand et al.,
invadens Rae, 2020) draparnaudi host snails 2004)
Eobania Infect and kill the (Azzam and El- Pomatias elegans Parasitic towards (Morand et al.,
vermiculata eggs of snails Abd, 2021) host snails 2004)
Limax flavus Infect and kill the (Azzam and El- Succinea putris Parasitic towards (Morand et al.,
eggs of snails Abd, 2021) host snails 2004)
Achatina fulica Infect and kill the (Azzam and El- Pelliodistis spp. Bulinus truncatus Parasitic towards (Azzam, 2006)
eggs of snails Abd, 2021) host snails
Lehmannia Nematode infection (Tandingan De Pelliodistis Oxychilus deilus Parasitic towards (Joshi and
valentiana Ley et al., neopapillosa host snails Ratcha, 2018)
2014) Pelliodistis tawfiki Eobania Parasitic towards (Azzam, 2006)
Theba pisana Genetic variation in (Tandingan De vermiculata host snails
bacterial associates Ley et al., Rhabditella axei Archachatina Nematodes infection (Odaibo et al.,
of the nematodes 2020) marginate through 2000;
Alloionema Arionidae spp. Penetration of (Laznik et al., Archachatina gastrointestinal tract Olofintoye and
appendiculatum parasitic juvenile 2009) achatina Olorunniyi,
into snail host 2016)
Arion vulgari Toxicity in bacterial (Nermuť et al., Steinernema Oncomenia Nematodes infection (Li et al., 1986)
associates of the 2019) bibionis hupensis
nematodes Steinernema Parmacella ibera Nematodes infection (Saeedizadeh
Cantareus Parasitic towards Morant 2014 carpocapsae and Niasti,
aspersus host snails 2020)
Cochicella Parasitic towards Morant 2014 Deroceras Nematodes infection (Jaworska,
barbara host snails agreste 1993)
Prietocella Nematode infection (Morand et al., Steinernema feltiae Parmacella ibera Nematode infection (Saeedizadeh
barbara 2004) and Niasti,
Caenorhabditis Achatina fulica Parasitic towards (Guerrero 2020)
briggsae host snails et al., 2018) Oncomenia Nematodes infection (Li et al., 1986)
Heterorhabditis Parmacella ibera Nematodes infection (Saeedizadeh hupensis
bacteriophora and Niasti, Deroceras Nematodes infection (Jaworska,
2020) agreste 1993)
Biomphalaria Physiological (Santos et al., Steinernema glaseri Oncomenia Nematodes infection (Li et al., 1986)
glabrata alteration 2022) hupensis
Deroceras Nematodes infection (Jaworska,
Notes: The first 3 rows are bold to highlight the current literatures reported in
agreste 1993)
Pomacea canaliculate (GAS).
Heterorhabditis Pseudosuccinea Physiological (Larissa
baujardi columella alteration through Bitencourt
increased Vidal et al., (Schurkman and Dillman, 2021). The emerging use of EPNs in pest
haemolymph 2021) management are mainly due to the inexpensive culture feature, capable
activities of
aminotransferases
to infect numerous hosts and long live cycle up to months in the infective
and lactate stage (Alramadhan and Mamay, 2019). EPNs complete infection on
dehydrogenase gastropods within 12–15 days at room temperature, which usually from
Lymnaea Changes the level of (Tunholi et al., infective juvenile penetration to infective juvenile emergence (Nema­
columella galactogen in 2017)
tode, 2008). EPNs had been proven to be safe towards warm blooded
L. culummella
Heterorhabditis Oncomenia Nematodes infection (Li et al., 1986) vertebrate and causing destructive damages towards cold blooded
heliothidis hupensis invertebrate at high doses (Alramadhan and Mamay, 2019). In com­
parison to predator-based biocontrol agent who took up to weeks to kill

6
W.A. Azmi et al. Biological Control 175 (2022) 105060

Table 4
Pathogenic of entomopathogenic fungi to mollusk species.
Targeted mollusk species Entomopathogenic fungi Mitigation mechanism References

Pomacea canaliculate Beauveria bassiana – Enzymatic digestion (Maketon et al., 2009)

Metarhizium anisopliae – Penetrate host cell by mechanical pressure
Metarhizium flavoviride – Protease production to alter embryogenesis of snails
Paecilomyces lilacinus
Pseudomonas aeruginosa – pathogenic attack (Chobchuenchom and Bhumiratana,
Pseudomonas fluorescens 2003)
Amphimelania holandrii Beauveria bassiana Cause vacuolation of digestive cell, resulting in degeneration of secretory cells (TA Abdel-Wareth et al., 2019)
Paecilomyces lilacinus Cause vacuolation of digestive cell, resulting in degeneration of secretory cells (TA Abdel-Wareth et al., 2019)
Biomphalaria alexandrina Aspergillus terreus Release of mycotoxin (Saad et al., 2014)
Penicillium janthinellum
Biomphalaria glabrata Beauveria bassiana Attack juvenile eggs (Duarte et al., 2015)
Cornu aspersum Metarhizium brunneum Enzymatic digestion (Khoja et al., 2019)
Derocerus reticulatum Metarhizium brunneum Toxicity of of fungal volatile organic compounds (Khoja et al., 2019)
Monacha cantiana. Beauveria bassiana Fungus infection (Hendawy et al., 2015)

hosts, EPNs take within 2 days for infestation. For instance, infective parasitic infection on insect host through its nonmobile exogenous spore
juveniles of Heterorhabditis spp. and Steinernema spp. release symbiotic called conidia (Altinok et al., 2019). M. anisopliae displayed various
bacteria from its intestine into the host and resulting in the production of infection modes in insects such as 1) adhesion on host, 2) germination of
toxin within the body cavity of host which kill the host within 48 h conidia, 3) appressorium formation, 4) penetration, 5) colonization of
(Tofangsazi et al., 2018). According to Sudhaus (2008), the interaction hemolymph and 6) sporation and extrusion as insecticide (Aw and Hue,
of EPNs and gastropods include (1) direct or indirect phoresy where the 2017). Understanding the mechanism mode of action of EPF toward pest
nematodes use gastropods for movement or transportation, (2) necro­ control could aid in the technology development for molluscicide
meny where nematodes use gastropods as food source upon its death and application. Despite the fact that EPF is primarily employed as an
transportation, and (3) parasitism where nematodes obtained benefit insecticide rather than a molluscicide at the moment, there is a chance
from gastropods and slowly causing damage towards gastropods. that it might be used as a biological control for different kinds of snails
Pesticide formulated with EPNs can be applied by electrostatic sprayers, (Table 4).
mist blowers and pressurized sprayer to kill gastropods (Tofangsazi M. anisopliae has been shown to be less dangerous than synthetic
et al., 2018). pesticides for crops, vertebrates, people, and the environment (Arthurs
The preliminary examination of nematodes Steinernema bibionis in et al., 2003; Zimmermann, 2007). However, the field application of EPF
snail Oncomenia hupensis control was firstly reported in 1986 (Li et al., required in-depth assessment including the biological properties of the
1986). EPNs started to use as molluscicide when Phasmarhabditis her­ fungus, quantified residues, fate and behavior in the environment and
maphrodita was introduced in 1994 and significantly control the number effects on non-targeted organisms, vertebrates, and humans (Zimmer­
of snails (Glen et al., 1996). P. hermaphrodita control snails by mecha­ mann, 2007). Upon application in the field, microsatellite markers could
nisms such as inhibit the feeding mechanism (Rae et al., 2009), change be used to study the dissemination pattern of fungus on the soil, complex
of functional protein expression (Boraldi et al., 2021; Montanari et al., integration of abiotic and biotic factors influencing the persistence of
2020), parasitic towards larval or juvenile of snails (Azzam and El-Abd, EPF and influence of fungal density should be examined in field trial
2021; Cutler and Rae, 2020). Table 3 highlighted the current research before mass production for massive field application to ensure the safety
studied on the parasitic, pathogenic and toxicity relationship of different and efficiency of EPF application in field (Pilz et al., 2011).
nematodes on the gastropod species. However, the specific reports on
EPN in GAS mitigation is very limited, where only 2 nematode species 3.2. Plant based substitution and redesign approach
Angiostrongylus cantonensis and Phasmarhabditis hermaphroditis, being
reported in GAS control (Boraldi et al., 2021; Montanari et al., 2020; In recent decade, bioactive compounds extracted from plants are
Yang et al., 2013b). Hence, it is critical to address this research gap and getting popular as environmentally friendly molluscicides, this
stimulate more research into the use of EPN’s for GAS mitigation. including saponins, flavonoids, steroids, tannins, and other secondary
metabolites (Cantanhede et al., 2010). Table 5 summarized the appli­
3.1.2. Entomopathogenic fungi (EPF) cation of plant extracts for GAS management. There have also been re­
EPF has received a great deal of attention due to its wide range of ports of polyherbal (Neem, Tobacco, Nerium, Pongamia, Zinger, and
host specificity, environmental friendliness, safety, and ease of mass Piper) where the mixed function of bioactive substances as potent
production and adaptable to various unfavorable conditions (Maravi molluscicide effective for the management of P. maculata (Prabhakaran
et al., 2018; Shah et al., 2016). To date, only few report available on et al., 2017). Polyherbal of Origanum majorana and Ocimum americanum
using EPF to treat Metarhizium anisopliae, Metarhizium flavoviride, Pae­ has relaxing effects on P. canaliculate (Bianchini et al., 2017). Other
cilomyces lilacinus, Beauveria bassiana, Pseudomonas aeruginosa, and plants that show molluscicidal activities that are yet to be tested on
Pseudomonas fluorescens (Chobchuenchom and Bhumiratana, 2003; Pomacea spp including Erigeron speciosus (Meepagala et al., 2002),
Maketon et al., 2009). Reddy et al. (2014) reported that the entomo­ Achyranthes aspera (Mandefro et al., 2017), Solanum sp (El Sherbini
pathogenic fungus M. anisopliae is currently being used to control many et al., 2011), Ambrosia maritima (Sameh et al., 2007), Glinus lotoides
agricultural and forest pests worldwide. M. anisopliae has been regis­ (Kiros et al., 2014), etc. The mode of actions of plant molluscicides on
tered in the USA and other countries as a commercial biopesticide as it is snails includes interference with snail enzymes, neurons, digestive sys­
effective to kill insect pests and gastropods. For instant, M. anisopliae tem, growth toxins, and osmoregulation (Abubakar et al., 2017). There
exhibits ovicidal activity on aquatic planorbid snail Biomphalaria glab­ is also the integration of current technology such as microwave-assisted
rata (Duarte et al., 2015). extraction to improve the targeting effect of certain bioactive com­
There are profound applications of EPF as insecticides has been re­ pounds for the development of sustainable biopesticide (Ramli et al.,
ported (Ambethgar, 2009; Goettel and Glare, 2010; Gul et al., 2014; 2019).
Maina et al., 2018). Among the entomopathogenic fungi, M. anisopliae Other efforts to control the GAS population including the utilization
and B. bassiana had been widely investigated and successfully causing of GAS as protein resources for fish and shrimp feed (Bombeo-Tuburan

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W.A. Azmi et al. Biological Control 175 (2022) 105060

Table 5
Plant extracts as GAS control agents.
Botanical Name Scientific Name Active Compound/Substance Biopesticidal activities on snails Reference

African Dream Entada rheedii Flavonoid, glycosides, saponins, LC50 and LC90 values for 24 h at 1611 and 4266 mg/L (Nur Suraya et al., 2017)
Herb tannins, terpenoids
Black Solanum nigrum Ethanolic extracts LC50 and LC90 values for 24 h at 2.98 and 5.95 mg/L (El Sherbini et al., 2011)
nightshade
Cinnamon Cinnamomum verum Essential oil extracts Show 84.30 % mortality rate for 48 h at 156 ppm (Idris et al., 2020)
extractive
Citronella Cymbopogan nardus (L.) Essential oil extracts Show 62.44 % mortality rate for 48 h at 156 ppm (Idris et al., 2020)
Rendle extractive
Clove Syzygium aromaticum Essential oil extracts Show 47.85 % mortality rate for 48 h at 156 ppm (Idris et al., 2020)
extractive
Coffee ground Coffee liberica Ethanolic extracts Nanoparticle at 553 nm showed lethality on GAS (at (Khalid, 2020)
30-60mins exposure)
Devil’s Achyranthes aspera Aqueous extract LC50 and LC90. values for 24 h at 69.5 mg/L and 93.9 (Mandefro et al., 2017)
horsewhip mg/L
Gallic Allium sativum Alkaloids and Tannins About 80 % mortality observed from 95 % gallic (Garin et al., 2019)
extract
Garlic Allium sativum Skin & Stem extracts Nanoparticle at 1381 nm showed lethality on GAS (Khalid, 2020)
(7–9 mins exposure)
Garden Solanum sinaicum Ethanolic extracts LC50 and LC90 values for 24 h at 3.19 mg/L and 6.04 (El Sherbini et al., 2011)
Nightshade mg/L
Ginger Zingiber officinale and Crude extract Reducing the hatchling success rate of GAS up to 80 % (Ismail and Musa, 2021)
Carica papaya
Ginger Zingiber officinale Essential oil extracts Show 13.77 % mortality rate for 48 h at 156 ppm (Idris et al., 2020)
extractive
Ginger Zingiber officinale L. Rhizome LC50 and LC90 values for 24 h at 485 mg/L And 767 (Prabhakaran et al., 2017)
mg/L
Groundnut Archis hypogaea Skin extract Nanoparticle at 1114 nm showed lethality on GAS (at (Khalid, 2020)
shell 5–9 mins exposure)
Herb plants Glinus lotoides Aqueous extract LC50 and LC90 values for 24 h at 47.1 mg/L and56.96 (Kiros et al., 2014)
mg/L
Lantana Lantana camara Essential oils LC50 value for 24 h at 23.6–40.2 μg/L (Huy Hung et al., 2021)
Mygwort Artemisia douglasiana Vulgarone B (Sesquiterpene) 75 µM saponin extract showed 100 % mortality for 24 (Joshi et al., 2005)
h exposure
Neem Azadirachta indica Azadirachtin Methanolic and ethanol extracts show LC50 value at (Latip et al., 2013;
21.0 mg/ml and 43.7 mg/ml Massaguni and Latip, 2015)
Neem Azadirachta indica A. Juss Kernel Oil LC50 and LC90 values for 24 h at 365 mg/L and 624 (Prabhakaran et al., 2017)
mg/L
Nerium Nerium indicum Mill. Leaves extract LC50 and LC90 values for 24 h at 179 mg/L and 341 (Prabhakaran et al., 2017)
mg/L
Nightshade Solanum villosum Ethanolic extracts LC50 and LC90 values for 24 h at 4.88 mg/L and 8.95 (El Sherbini et al., 2011)
mg/L
Nipple Fruit Solanum mammosum Extracts containing alkaloids, phenols, LC50 value for 48 h at 24.4 mg/L (Quijano et al., 2014)
tannins and saponin
Pigweed Chenopodium quinoa quinoa saponins 13 ppm saponin extract showed 100 % mortality for (Joshi et al., 2008)
24 h exposure
Piper Piper nigrum L. Seeds LC50 and LC90 values for 24 h at 202 mg/L and 309 (Prabhakaran et al., 2017)
mg/L
Pongamia Pongamia pinnata L. Seed oil LC50 and LC90 values for 24 h at 512 mg/Land 804 (Prabhakaran et al., 2017)
mg/L
Powder Puff Barringtonia racemosa (L.) saponin dan flavonoid Show 100 % mortality at 200 ppm exposure of (Musman, 2010)
Tree extractive
Ragweed Ambrosia artemisiifolia Psilostachyin LC50 value for 24 h at 194 mg/L (Ding et al., 2018)
Psilostachyin B.
Axillaxin
Reinw seed Pangium edule Aqueous extract LC50 value for 24 h at 11.574 g/L (Manoppo, 2017)
Sea Rodwood Ambrosia maritima Polyacetylenes, thiarubrine A, LC50 value for 24 h at 897.2 mg/L (Sameh et al., 2007)
thiarubrine A epoxide, thiarubrine A
Diol
Showy Erigeron speciosus Essential oil LC50 value for 24 h at 8 mg/L (Meepagala et al., 2002)
Fleabene
Soapberry Sapindus mukorossi Hederagenin (Saponin extracts) LC50 for 24 h and 48 h at 85 mg/Land 22 mg/L (Huang et al., 2003)
Sweet potato Ipomoea batatas Hexane, methanolic and chloroform Lethality concentration of hexane, methanolic and (Noorshilawati et al., 2020)
extracts chloroform extracts at 1639, 4789, 6709 ppm
respectively.
Tobacco Nicotiana tabacum L Leaves extract LC50 and LC90 values for 24 h at 205 mg/L and 375 (Prabhakaran et al., 2017)
mg/L
Wallich seed Derris elliptic Aqueous extract - tannins, saponin LC50 value for 24 h at 9905 mg/L (Manoppo, 2017)
Water spinach Ipomoea aquatica Stem aqueous extract Nanoparticle at 780 nm showed lethality on GAS (at (Khalid, 2020)
4–6 mins exposure)
Wingleafs Sapindus Extracts containing alkaloids, phenols, LC50 value for 48 h at 184.92 mg/L (Quijano et al., 2014)
oapberry saponariaSaponaria tannins and saponin
Wintersweet Chimonanthus praecox cv. Fatty acids Show 100 % mortality rate for 48 h exposure of (Zhang and Zou, 2020)
Luteus extract
Wintersweet Chimonanthus nitens Flower extracts LC50 value for 24 h and 48 h are 0.287 and 0.247 mg/ (Li and Zou, 2019)
ml

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W.A. Azmi et al. Biological Control 175 (2022) 105060

et al., 1995; Visca and Palla, 2018), as weaning food (Marsyha et al., using internet of things (IoT), big data, artificial intelligence and
2018) and its shell has been used as organic filter (Tepsila and Suksri, human–machine interactions aid in the precision in farming and pest
2018), as kaolin extract for biomaterial applications (Sutthi et al., 2017) management enable the sustainable production with lower cost involved
and calcium phosphate powder as a source of biomaterials (Laonapakul and enhance ecosystem balance (Shi et al., 2018). However, literatures
et al., 2021). The egg extract has been used to synthesis silver nano­ on precision pest management of GAS are scarce, this is mainly due to
particles (AgNPs) that provides bacterial resistance to a wide range of uneven technology distribution over major agricultural production re­
bacterial (Ghada et al., 2019). The shell is also reported to be used as gion and the technology of IoT itself is still in its infancy stage (Shi et al.,
fertilizer to cultivate mushrooms (Meepun and Siriket, 2019). The 2018). An improved predator–prey model has been introducing into an
addition of GAS residue as fertilizer and soil amendment could signifi­ intelligent robot to calculate the activities of GAS in rice field hence
cantly improve the soil condition (Wang et al., 2020). Farmers also use giving a clue of best timing for manual hand picking which proven to
apple wax solvent (morpholine) to suppress egg hatching, however, the control the ecosystem of paddy field (Maldonado and Nakaji, 2008).
applicability of this method remains to be tested in the field (Wu et al., Apart of mathematic model optimization, improvement of image pro­
2005). cessing system enables the detection of GAS eggs precisely up to 91.66 %
In sum, the current understanding on the emerging biological con­ hence corrected chemical spray up to 72.72 %, which reduce the
trols through EPN and EPN and bio-rational approaches through plant- chemical waste and effectively control GAS (Kritphon and Suwicha,
based substitution in GAS mitigation is still scarce, extensive research 2021). Image processing techniques have been optimised for automated
are required to speed up the technology development for GAS control. leaf pest and disease recognition, and the use of drones in imaging ac­
quisitions is definitely advancing this field of study (Bolch et al., 2021;
4. Application challenges in biological control Iost Filho et al., 2019). The application of drone had become a new trend
in precision pest management due to its environmentally friendly and
There are various problems encountered in adopting biological ap­ cost-effective properties (Iost Filho et al., 2019). For instance, an actu­
proaches in GAS mitigation. The main concern is their bio-efficacy and ation drone is used for the precision distribution of pesticide whereas
the available choice of natural enemies in different region and country. sensors drone used for the detection of the pest hotspot and act as crop
Moreover, appropriate population size of natural enemies to be intro­ health monitor (Iost Filho et al., 2019). Remote sensing can be applied in
duce to hectares of rice paddy field is crucial to effectively control GAS the various discipline including acting as a stress detector caused by
while also maintaining the ecological balance. As an illustration, using various pests on the crop fields, species identification, assessment of the
duck would not be practical because it would cause harm to immature performance of biological control agents in fields, and assessment of pest
rice plants and be labor-intensive for farmers to feed the ducks with response to pesticide application (Nansen, 2016; Nansen and Elliott,
commercial feed (Teo, 2001). Similarly, fish is also an impractical 2016). Unmanned aerial vehicles (UAVs) are widely used in monitoring
choice, as they require certain amount of water to stay alive (Su Sin, the incidence of pest and crop diseases, provide real-time information on
2006). the degree of damage of pests on particular infected regions (Gao et al.,
The limitations of using EPN to control GAS include EPN’s suscep­ 2020). Application of Geographical information system (GIS) and global
tibility to desiccation and the possibility of developing a resistant positioning system (GPS) are indispensable components in PPM that
response within the snail species via encapsulation of the snail’s shell. serve as a key information hub on the pest population dynamics (He
(Howlett, 2012). The implantation of EPN such as P. hermaphrodita in et al., 2012; Natikar et al., 2016; Wang et al., 2009). For instance, the
the field may be a complex process because P. hermaphrodita cultivation ArcGIS online software had been utilized in the analysis of the niche
required a large amount of water and exhibited a short life cycle with distribution of P. canaliculate (Lei et al., 2017), haplotype distribution of
strict storage requirements (Barua et al., 2021). Currently, there are only both P. canaliculate and P. maculate (Yang et al., 2018) and visualize the
two EPN-based molluscicide products, namely SLUGTECH ® and Nem­ mapping of P. canaliculate, and P. maculate for habitat suitability (Reilly,
aslug® had been commercialized in the market. In addition, the use of 2017). The infield study (especially snails distribution and behavior) are
EPN may only showed lethal pathogenicity in smaller snail hosts, but not very important to precisely estimate and reduce the dependency on
for larger snail species (GRIMM, 2002). pesticides (Horgan et al., 2014). Moreover, soil nutrient regulation such
Among the natural products, essential oils offered promising features as the supply of nitrogen and silicon soil amendments to alter the
including high toxicity, antifeedant, ovicidal to be used as ideal bio- physiology of rice seedlings in GAS management (Horgan, 2017), lipo­
rational control agent to slugs (Barua et al., 2021). The bioactive com­ protein spingoid based regulation to limit nutrient available for GAS
pounds extracted from plant material are usually exhibit high patho­ survival (Yang et al., 2013a) and the application of copper (Rogevich
genicity towards the pest such as GAS, but also possess nematocidal et al., 2008), when use precisely, can achieve the goal for GAS control.
properties which could kill the beneficial nematodes such as P.her­ Mechanical control method through heat shock protein may regulate the
maphrodita, H.bacteriophora and S.feltiae (Barua et al., 2020). Moreover, physiological responses of GAS under high-temperature conditions and
current cytotoxicity research is primarily focused on molluscicide ac­ improve the fitness of GAS in environment adaptation (Xu et al., 2014;
tivities, with little attention paid to environmental impacts (Csanyi, Zheng et al., 2012). All the examples of GAS control measures listed
2022). above may not be effective to solve the GAS infestation with single
The deliberate or unintentional introduction of natural enemies into approach, it is therefore integration of the promising approaches could
new habitats may have an impact on the ecosystem of native flora and provide unprecedented opportunities in GAS mitigation.
fauna (Jones et al., 2022). Furthermore, there is a lack of investment in Integrated Pest Management (IPM) can be defined as multi- strate­
R&D in this field when compared to chemical or pharmaceutical control gies pest management which comprised of different skills and tech­
agents that can be commercialized and patented (Jones et al., 2022). niques to precisely address pest in crop land (Ahmad and Mahdi, 2018;
Bothikar and Pagire, 2022). IPM played critical roles in pest control
5. Precision pest management and integrated pest management monitoring, particularly in considering all appropriate measures to
farming discourage pest population growth during pest control crises (FAO,
2022). Several integrated techniques had been adopted in IPM such as
Precision pest management (PPM) practices are usually dynamics, biological control, modification of cultural practices, habitat manipu­
and it is a purpose targeted approach that involved a continuous lation, introduction of resistant varieties for long term pest prevention
monitoring system with advanced technology instrumentation to eval­ (Alramadhan and Mamay, 2019). To control crop damage, stopping
uate the invasion strength and the population level of GAS in response to winter flooding approach in the rice paddy field has been established to
every pest control action. The emerging of intelligent agriculture (IA) control GAS, at the same time manage the waterbird abundance in the

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W.A. Azmi et al. Biological Control 175 (2022) 105060

Fig. 3. The IPM activities involved in a different stage of rice production.

Fig. 4. The fundamental principles and beneficial advantages of IPM and PPM.

habitat (Bernardo-Madrid et al. (2022). Liang et al. (2014) integrated overwintering effect (Bae et al., 2012). PPM and IPM integration
direct seeding, duck herding and water management approaches in the consider all factors involved in GAS infestation and develops a set of
rice-duck farming in China that significantly reduce the GAS population. strategies and technologically advanced tools to combat the GAS inva­
IPM program targeted and applied different strategy based on different sion. (Ahmad and Mahdi, 2018). Therefore, when biological control is
focusing area at the same time could compensate each weakness of not feasible in some region, application of acoustic treatment could
different management approaches hence increase the successful rate of provide positive alternative in GAS mitigation (Solé et al., 2021). The
GAS control (Environmental Protection Agency United States, 2021). introduction of sound disturbance had resulted in the pathological
For instance, the conception framework of IPM activities could involve changes in statocysts of GAS which later result in tissue malfunction and
several approaches as in Fig. 3. hence reduce the survival ability of GAS (Solé et al., 2021). The appli­
With the integration of PPM and IPM, microclimate change and its cation of electric shock with 0.35 A/m2 or more can inactivate GAS and
impact on rice production can be estimated, allowing farmers to prepare hence cease their reproduction process (Yagyu et al., 2005). The water
a mitigation plan. Example is the forecast the increase of 45.5 % of the level could also manipulate as prolonged water immersion period
GAS population in the 2020 s to 88.4 % in the 2080 s due to the resulted in the reduction of GAS egg’s hatching up to 75 % (Horn et al.,

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