The Golden Apple Snail Pomacea Canaliculata: A Review On Invasion, Dispersion and Control
The Golden Apple Snail Pomacea Canaliculata: A Review On Invasion, Dispersion and Control
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    Keywords: Invasive species; rice pest; biological control; biological invasions;      tive organic alternative, as some plant products have been
    Pomacea canaliculata                                                                  proven to be effective molluscicides in laboratory trials and
                                                                                          can be cheaper and safer for the environment and human
                                                                                          health than synthetic chemicals.
DOI: 10.1564/v27_aug_03	                                                        O u t l o o k s o n Pe s t M a n a g e m e n t – A u g u s t 2 0 1 6    1 5 7
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   THE GOLDEN APPLE SNAIL
                                                                            lings resulting in extensive crop damage (Fig 4). There are no
                                                                            known registered products for direct control of snail rice pests
                                                                            in Brazil (Cowie, 2002).
                                                                                 In other Latin American countries, P. canaliculata has
                                                                            been a danger to rice crops since 2005 particularly the
                                                                            lowland regions of the Ecuadorian provinces of Guayas
                                                                            and Los Rios. Surveyed farmers noted that even with heavy
                                                                            use of the molluscicides, endosuflan and metaldehyde, snail
                                                                            rice crop damage remained high, especially during the rainy
                                                                            season. (Rodriguez et al., 2015). However, the predatory snail
                                                                            kite also increased, leading to an expansion of the snail kite’s
                                                                            range which had been contracting since the 1970s (Horgan et
                                                                            al., 2014). Its spread into Mexico can be traced to the release
                                                                            of GAS into tributaries of the Colorado River by aquarists in
                                                                            the City of Yuma, Arizona, from which they dispersed down-
                                                                            stream into Mexican portions of the Colorado River drainage
                                                                            system (Campos et al., 2013).
                                                                                 In Europe, snail damage has been reported in some Portu-
                                                                            guese rice fields and in Spain, where rice is grown in the delta
                                                                            of the River Ebro, where it has been speculated that P. canal-
                                                                            iculata or P. lineata might also be present (Lopez et al., 2010).
                                                                                 Since its release in Asia, the snail has fed on a wide range
                                                                            of aquatic plants of economic value, including young rice
                                                                            seedlings, taro, swamp cabbage, lotus, mat rush, Chinese mat
                                                                            grass, wild rice, Japanese parsley, water chestnuts, and azolla.
                                                                            But, by far, the greatest damage occurs in irrigated rice culture,
                                                                            which provides an ideal environment for GAS dispersal and
                                                                            growth. Thus, after its invasion and spread through direct
Figure 2.  GAS Egg masses in Direct-Seeded Rice, Eldorado do Sul,           release, animal trails or irrigation pipelines, GAS rapidly has
Rio Grande do Sul, December 2015, Brazil. (Photo credits: Ms. Danielle      become one of the most damaging rice pests in Asia (Naylor,
Almeida, IRGA, Brazil).                                                     1996).
Fig. 3. GAS Global Distribution. (Photo credits: Mr. Fabiano Carvalho de Brito, PUCRS, Brazil).
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                                                                                          THE GOLDEN APPLE SNAIL
Table 1. Global Distribution, Origin, Invasion Pathways, and Year reported of Pomacea spp.
    Invasive aquatic invertebrates can have high negative                 into currently uninfested countries. Hence, there is a need for
environmental impacts, but their management is still less well            management practices adapted to local conditions (Cowie,
developed than for other taxa such as mammals or birds. It                2002).
is estimated that aquatic invertebrates account for approxi-                  It is estimated that damage caused by invasions of inva-
mately 24% of all environmental economic impacts (Pysek &                 sive species were costing the United States, United Kingdom,
Richardson, 2010). The degree of these impacts may increase               Australia, South Africa, India and Brazil more than $ 314
as Ampullariid snail populations continue to expand further               billion per year (Pimentel et al., 2001). Quantifying the nega-
                                                              O u t l o o k s o n Pe s t M a n a g e m e n t – A u g u s t 2 0 1 6    1 5 9
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   THE GOLDEN APPLE SNAIL
                                                                           some cost, there is evidence that it has been effective in some
                                                                           Asian and southern Latin American countries (IRGA, 2010).
                                                                               A number of different, fish will eat snails, including
                                                                           the African catfish (Clarias gariepinus) and common carp
                                                                           (Cyprinus carpio), but the latter was more adaptable to vari-
                                                                           ous different farming environments (Teo, 2006). Hence, the
                                                                           common carp is the recommended fish species of choice for
                                                                           controlling GAS in rice culture at a density of 10 fish/plot or
                                                                           2041 fish/ha. Apart from being an alternative to using mollus-
                                                                           cicides, the deployment of carp can provide additional income
                                                                           for farmers. Halwart et al. (2014) studied the efficacy of fish
                                                                           predators for control of GAS in transplanted rice during
                                                                           dry and wet seasons. They showed that common carp were
                                                                           able to suppress snail populations by 58–87% compared to
Fig. 4. GAS damage as cut leaves in Direct-Seeded Rice, Eldorado           48–87% by Nile tilapia (Oreochromis niloticus) both being
do Sul, Rio Grande do Sul, December 2015, Brazil. (Photo credits: Ms.      greater than occurred in no-fish plots. However, neither fish
Danielle Almeida, IRGA, Brazil).                                           species could completely prevent infestation by more mature
                                                                           snails with larger shell sizes.
                                                                               The treatment of GAS eggs with the parasitic fungus Paecilo-
tive impacts of these invasive species is difficult and complex            myces lilacinus led to 100% mortality of 1 day old juvenile
as the knowledge required to assess the impacts of many                    snails, susceptible to the conidia and only 12% of eggs hatched in
taxa at regional scales is still scarce. Certainly, managing P.            contrast to 100% in controls (Maketon et al., 2009). However,
canaliculata damage has become very expensive. Published                   juvenile snails became increasingly less susceptible to the enzy-
data on GAS damage appears to have been grossly underesti-                 matic activity of the fungus with increasing age and maturity,
mated. An estimated annual loss due to crop damage by non-                 limiting its use as a biological control agent. In another labo-
indigenous species in Southeast Asian countries translates to              ratory study Salcedo (2013) evaluated the pathogenicity of the
about $33.5 billion of total damage including that to agricul-             nematode Heterorhabditis bacteriophora and showed that the
ture, the environment and public health. The total estimated               inoculation of up to 16,000 nematodes per snail leads to 100%
damage caused by GAS in Southeast Asian countries is $1.47                 snail mortality in 96 h.
billion annually. In Southeast Asian countries such as Brunei,                 Current biological control with fish seems to be the most
Cambodia, Indonesia, Laos, Malaysia, Myanmar, the Philip-                  promising option for sustainable GAS management. However,
pines, Singapore, Thailand and Vietnam, the estimates are                  biocontrol must be complemented with other methods such
probably conservative as they do not include damage to the                 as lowering water levels or draining the rice field. Draining
environment or human health (Nghiem, 2013).                                will not kill GAS because they are able to survive long peri-
                                                                           ods of desiccation. GAS move only in standing water and are
                                                                           immobile at depths less than half of their shell height, thus
Golden apple snail biological control                                      periodic draining of the fields to a depth of 1 cm is a very
The most effective method to control snails relates to                     effective control practice because it prevents the specimens of
crop establishment. For instance, transplanted 20-day-old                  P. canaliculata from moving and feeding (Wada, 2004). The
seedlings are better able to withstand snail damage than                   field should be well levelled and maintained at saturation,
13-day-old transplanted seedlings or direct-seeded rice.                   minimizing the time it contains standing water. Farmers with
Seedlings more than 30-days-old are more tolerant to snail                 their own pumps can manage water levels better than those
damage than younger seedlings.                                             served by large irrigation systems.
    Over the past 15 years, a number of options for P. canal-
iculata biological control have emerged. The fire ant Solenop-
sis geminata consumed P. canaliculata eggs in Philippine field             Chemical control
experiments in spite of the fact that the eggs are considered              While plant components are natural and socially and envi-
toxic to most animals (Dreon et al., 2014). Although another               ronmentally acceptable, they are not necessarily non-toxic.
ant (Pheidologeton spp.) has also been reported to consume                 Several plants have active ingredients that could be potential
GAS eggs (Yusa, 2006), further studies are needed to confirm               biodegradable molluscicides, including saponins, flavonoids,
the impact of ants. The relative absence of natural predators              steroids, tannins, and other secondary metabolites (Valverde
has allowed the rapid establishment and growth of GAS popu-                et al., 2010).
lations soon after their introduction to an un-infested habitat.               Huang et al (2003) exposed specimens of P. canaliculata
    Ducks have been extensively used to control P. canalicu-               to powder extracts of soap nut pericarp from Sapindus muko-
lata in both transplanted and direct-seeded rice culture, but              rossi (Sapindaceae) and attained LC50 values of 85, 22, and 17
with variable results, depending on the race of the ducks as               ppm after treating for 24, 48, and 72h, respectively. Bioassay
well as the time of release. The effective number of ducks                 experiments with a new acetylated triterpene saponin, hedera-
required is estimated to be around 5–10 ducks per hectare,                 genin, comparing it to niclosamide and metaldehyde revealed
with results being more favorable in transplanted rather than              that all of the isolated saponins exhibited molluscicidal effects
direct-seeded rice (Teo, 2001). While this strategy entails                against P. canaliculata. Niclosamide (0.8 mgL-1) exposure
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                                                                                                  THE GOLDEN APPLE SNAIL
Table 2. Effectiveness of the Biological (Botanicals and Natural Enemies) Control Agents against Pomacea spp.
Chenopodium quinoa Saponins from husk 33-54 mg l-1 San Martin et al. (2008)
Azadirachta indica Aqueous extracts from leaves (LC 50) 142.75 mg l-1 Venturini et al. (2008)
Chenopodium chinoa                       Quinoa Saponins                       9, 11 and 13 mg l-1 (ovicidal effects in 1-5   Joshi et al. (2008)
                                                                               day old )
Oldenlandia affinis and Viola odorata Cyclotides 150-300 µ/ml Plan et al. (2008)
Chenopodium quinoa Alkali modified Quinoa Saponins 30 mg l-1 in 36h San Martin et al. (2009)
Azadiractha indica Dried seed extracts (LC 50) 500 mg l-1 in 96 h Latip et al. (2013)
Oryza sativa                             Rice husk based on activated          0.034 U/ml to disrupt the hatching process Salleh et al. (2013)
                                         carbon
Sapindus saponaria, Solanum              Extracts containing alkaloids,        (LC 50)17.8 mg l-1 and 24.04 mg l-1            Manzano et al. (2014)
mammosum and Jatropha curcas             phenols, tannins and saponins
Ilex paraguariensis St.-Hil Extracts of unripe fruits (LC 50) 26 mg l-1 in a 16 h Brito (2015)
Study covered 46 species in 16           Macrobrachium formosense,             Predates on Juveniles and Sub-adults           Yusa (2006; 2014)
orders: Crayfishes, Dragonfly            Tribolodon hakonensis and Zacco
larvae, Diving beetles, freshwater       temmincki
fishes, Carp and turtles
Fish: Common carp Cyprinus carpio Predates on Juveniles and Sub-adults Ichinose et al. (2002)
Fishes: Common carp and African          Cyprinus carpio and Clarias gariepinus Predates on Juveniles and Sub-adults          Teo (2006)
catfish
Fish: Pearl cichlid Geophagus brasiliensis Predates on Juveniles and Sub-adults Silva & Figueiredo (2014)
Fishes: common and black carps           Cyprinus carpio and                   Predates on Juveniles and Sub-adults           Qiu et al. (2014)
                                         Mylopharyngodon piceus
Fishes: Nile tilapia and Common          Oreochromis niloticus and Cyprinus    Predates on Juveniles and Sub-adults           Halwart et al. (2014)
carp                                     carpio
Fungi                                    Paecilomyces lilacinus                Parasitism by killed newly-hatched juvenile Maketon et al. (2009)
                                                                               snails
Nematode                                 Heterorhabditis bacteriophora         Inoculations septicemia                        Salcedo (2013)
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   THE GOLDEN APPLE SNAIL
yielded an 85% mortality rate while that of metaldehyde (20                    and Sebastian, L.S. (Eds.), Global Advances in Ecology and
ppm) was 40%. Likewise, the soap nut powder of pericarp                        Management of Golden Apple Snails, Nueva Ecija: Philippine
extracts (4ppm) displayed 62% mortality to GAS in paddy                        Rice Research Institute, pp. 73–112.
fields (Huang et al., 2003). These results showed that both                Horgan, F.G., Felix, M.I., Portalanza, D.E., Sanchez, L., Moya Rios,
                                                                               W.M., Farah, S.E., Wither, J.A., Andrade, C.I., Espin, E.B., 2014.
isolated saponins and crude soap nut extract express mollus-
                                                                               Responses by farmers to the apple snail invasion of Ecuador’s
cicidal activity against P. canaliculata. However, at present,                 rice fields and attitudes toward predatory snail kites. Crop
farmers appear to prefer the use of conventional pesticides                    Protection. 62, 135–143.
as none of the botanical molluscicides identified has been                 Huang, H.C., Liao, S.C., Chang, F.R., Kuo, Y.H., Wu, Y.C., 2003.
produced commercially (Joshi, 2007).                                           Molluscicide saponins from Sapindus mukorossi, inhibitory
                                                                               agents of golden apple snails, Pomacea canaliculata. Journal of
                                                                               Agricultural and Food Chemistry. 51, 4916–4919.
Conclusion                                                                 IRGA, 2010. Instituto Riograndense do Arroz: Cresce o número
The Invasive Species Compendium (CABI, 2014) contains                          de marrecos de Pequim na lavoura de arroz. http://www.irga.
extensive information on world-wide GAS invasions, establish-                  rs.gov.br/conteudo/2560/cresce-o-numero-de-marrecos-de-
ment and damage. Extensive documented evidence suggests                        pequim-na-lavoura-de-arroz-
                                                                           Joshi, R.C., 2007. Problems with the management of the golden
that its capacity for damage to invaded wetland agricultural
                                                                               apple snail Pomacea canaliculata: an important exotic pest of
systems should not be underestimated, as its range continues to                rice in Asia. In: Vreysen, M.J.B., Robinson, A.S., Hendrichs, J.,
expand with invasions throughout Asia (Joshi, 2007). The total                 (Eds.), Area-Wide Control of Insect Pests, Springer Netherlands,
cost of managing GAS amounts to more than $ 1200 million                       p.257–264.
annually. This review of alternative methodologies to control              Karraker, N.E., Dudgeon D., 2014. Invasive apple snails (Pomacea
damage by pest snails in wetland agriculture shows that the                    canaliculata) are predators of amphibians in South China.
impact of various biological control systems examined in the                   Biological Invasions. 16, 1785–1789.
laboratory need to be studied more fully under field conditions            Lach, L., Cowie, R., 1999. The spread of the introduced freshwater
before they can be widely used to control GAS.                                 apple snail Pomacea canaliculata (Lamarck) (Gastropoda:
                                                                               Ampullariidae) on O‘ahu, Hawai‘i. Bishop Museum Occasional
                                                                               Papers., 58, 66–71.
                                                                           Lopez, M.A., Altaba, C.R., Andree, K.B., Lopez, V., 2010. First
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                                                                                                THE GOLDEN APPLE SNAIL
Valverde, A.L., Silva-Souza, N., Marques, A.M., Cantanhede,
    S.P., 2010. Atividade moluscicida de plantas: uma alternative             Ravindra C. Joshi is currently a Technical Advisor on rice apple snail to DELTAMED
    profilática. Brazilian Journal of Pharmacognosy. 20(2), 282–288.          (Asociación de Deltas del Mediterráneo) España, Francia, Italia, Rumania, Egipto,
Wada, T., 2004. Strategies for controlling the apple snail Pomacea            Grecia, Vietnam, Argentina i Brasil; and Visiting Professor, Adjunct Professor of
    canaliculata (Lamarck) (Gastropoda: Ampullariidae) in Japanese            Agriculture, and Research Affiliate, with Pampanga State Agricultural Univer-
    direct-sown paddy fields. Japan Agricultural Research Quarterly.          sity, Philippines, University of South Pacific, Fiji, and Cordillera Studies Center,
    38(2), 75–80.                                                             University of the Philippines-Baguio, Philippines, respectively. He is a Fellow of
Yusa, Y., 2006. Predators of the introduced apple snail, Pomacea              the Royal Society of Biology and Royal Entomological Society, UK. His research
    canaliculata (Gastropoda: Ampullariidae): their effectiveness and         focuses on a variety of family food and nutrition related issues, including the
    utilization in biological control. In: Joshi, R.C., and Sebastian,        impacts of agriculturally important invasive species, climate change, and biodi-
    L.S. (Eds.), Global Advances In Ecology and Management of                 versity conservation in Asia, Africa and the Pacific.
    Golden Apple Snail, Nueva Ecija: Philippine Rice Research
    Institute, pp.345–361.                                                    Fabiano Carvalho de Brito is a biologist graduate in Pontifícial Catholic University
                                                                              of Rio Grande do Sul (PUCRS), Brazil, having master’s degree in Zoology with
                                                                              emphasis in Animal Physiology in Pontifícial Catholic University of Rio Grande
                                                                              do Sul (PUCRS), where he investigated the chemical control rice pest snail
                                                                              Pomacea canaliculata through the use of fractions obtained from unripe fruits of
                                                                              yerba mate (Ilex paraguariensis). He is currently pursuing a doctorate in ecology
                                                                              (bioindication) on the Federal University of Rio Grande do Sul, UFRGS, Brazil.
  Similar articles that appeared in Outlooks on Pest Management include – 2004 15(5) 229;
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