Feeding Strategies of Giant African Snail Achatina fulica on Papaya in Samoa

Abstract

The giant African snail (Achatina fulica) is a widely introduced invasive land
snail species, and is considered an important agricultural pest in several regions of
the world including in the south Pacific. In Samoa, A. fulica is a major pest that feeds
on various crops of economic importance, including papaya. This study investigated
the feeding strategies of A. fulica and the damage caused to papaya through field and
laboratory trials in Samoa. Unripe mature fruits were sampled to assess snail damage.
Results showed heavy snail infestation; on average more than two snails were
recovered per papaya tree. The mean number of snails per plant decreased with the
height of the plant. Snails inflicted primary damage through feeding that led to
abrasions on more than 80% of fruits and indirectly caused fungal contamination
through their faeces (93%) and slimy marks. Snail feeding damage induced
premature ripening of papaya fruits. In the host choice tests, the snails preferred to
feed on papaya than tomatoes; however, they showed equal preference to papaya and
cabbage in the field trails. Smaller snails were voracious and ate more papaya leaves
per unit of body weight compared with larger snails. Snails were found to be good
climbers, and 60% of the snails released near the papaya tree trunk were able to
reach the papaya fruits on the tree. However, climbing was less prevalent on wet/rainy
days.

Full text



ActaHortic.1128.ISHS2016.DOI10.17660/ActaHortic.2016.1128.35
XXIXIHC‐Proc.Int.Symp.onHorticultureinDevelopingCountriesand
WorldFoodProduction
Eds.:A.Gracie,M.TaguchiandG.Rogers
229
Feeding strategies of the giant African snail
Achatina
fulica
on papaya in Samoa
R.KantandS.S.Diarra
SchoolofAgricultureandFoodTechnology,TheUniversityoftheSouthPacific,Alafuacampus‐Apia,Samoa.
Abstract
The giant African snail (Achatina fulica) is a widely introduced invasive land
snail species, and is considered an important agricultural pest in several regions of
the world including in the south Pacific. In Samoa, A. fulica is a major pest that feeds
on various crops of economic importance, including papaya. This study investigated
the feeding strategies of A. fulica and the damage caused to papaya through field and
laboratory trials in Samoa. Unripe mature fruits were sampled to assess snail damage.
Results showed heavy snail infestation; on average more than two snails were
recovered per papaya tree. The mean number of snails per plant decreased with the
height of the plant. Snails inflicted primary damage through feeding that led to
abrasions on more than 80% of fruits and indirectly caused fungal contamination
through their faeces (93%) and slimy marks. Snail feeding damage induced
premature ripening of papaya fruits. In the host choice tests, the snails preferred to
feed on papaya than tomatoes; however, they showed equal preference to papaya and
cabbage in the field trails. Smaller snails were voracious and ate more papaya leaves
per unit of body weight compared with larger snails. Snails were found to be good
climbers, and 60% of the snails released near the papaya tree trunk were able to
reach the papaya fruits on the tree. However, climbing was less prevalent on wet/rainy
days.
Keywords:snaildamage,feedingpreference,choicetest,fungusgrowth,antifeedant, snail
faeces
INTRODUCTION
Thegiant African snail(GAS),Achatina fulica Bowdich1982, is thelargest species of
landsnail,andhasalsobeenconsideredthemostwidelyintroduced land snail species
(Thiengoetal.,2007).Itisanimportantagriculturalpestin several countries in different
continents,includinginthePacificIslandcountries.Itisreportedtofeedonmorethan500
species of plants (Thomsen, 1980;Nelson,2012)andactsasavector of plant diseases
causedbydifferentspeciesofPhytophthoraintaro,pepperandeggplant(Muniappan,1983).
A. fulicaishighlyinvasive,andlargecoloniesoflandsnailscanbeformedfromjusta
pairofindividualsnails(Thomsen,1980).Thesnailisnativetohumidareasoftheeastcoast
ofAfricabutisprevalentindifferentecologicalset‐upsincluding in agricultural farms,
coastalland,naturalforests,planted forests,shrublands,urbanareasandwetlands(Mead,
1973).
Thehistory of the introductionofGASin the southPacificregiongoesbackto1938,
butitwasfirstreportedinSamoain1994(PPO,1996).A. fulicaisamajorpestofseveral
economicallyimportantcropsgrowninSamoa,includingcocoa,banana,crucifervegetables,
eggplant,beleandpapaya(R.Kant,unpublished).Currently,snailbaitsimported fromNew
Zealand are the only option available to manage A. fulica in Samoa. Recent management
practiceusingsnailbaitsanduseofrosywolfsnail(Euglandina rosea)has raisedquestions,
asthesepracticesdrasticallyaffectthenativesnailpopulation (Nelson, 2012). Thus,
managementofA. fulicaneedsaproperunderstandingofitsfeedinghabit,whichcouldhelp
in finding an alternative eco‐friendly management approach. This study looked into the
feeding strategies of A. fulica through host‐choice testing in the laboratory and in field
conditions,andthedamageinflictedtopapaya(Carica papaya).

230
MATERIALS AND METHODS
GAS were collected from the field and reared on papaya leaves (‘Samoa Esi’ and
‘Hawaiian Sunrise’) under controlled conditions of 25°C, 65% relativehumidity,and12h
photoperiodintheEntomologyLaboratoryattheSchoolofAgricultureandFoodTechnology,
UniversityoftheSouthPacific,Alafuacampus,Samoa.Variousexperimentsweredesignedin
thefield andlaboratory to studythefeeding strategies ofA. fulicaontheselectedcropsin
Samoa.
Assessment of A. fulica damage to papaya
The damage caused by A. fulica was assessed by examining papaya trees and fruits.
Tenpapayatreesofdifferentsizes(agebetween2and4years)wereselectedtostudysnail
infestationandfruitdamage.Thetreesweredividedintothreegroupsbasedontheirheight:
small(<2m),medium(2‐3m),andtall(>3m).Allthemature‐unripefruitsfromeachtree
were collected and screened for abrasions, slimy marks, and faecal contamination by A.
fulica. After screening, the fruits sampled were grouped and left for3to4dbeforere‐
screeningthefruitsforfungalgrowthandtheirmarketabilitypotential. Small, immature,
yellow fruits were also collected from the selected trees for assessment. The fruits were
examinedforskinandfleshcolourwhereyellow(lighttodark)fleshfruitswereconsidered
ripe.
Host preference testing in A. fulica
HostpreferenceinA. fulicawastestedbyofferingpapayaincombinationwithtomato
orcabbage.Twenty‐fiveand30snailsweretestedforthepapaya vs.tomatoandpapayavs.
cabbage combinations, respectively,inthefield.Snailswereplaced in between the two
choicecrops(wholeplant)withadistanceof1mfromeach.Snailmovementwasrecorded
for 2 h and their preferences were identified. All the host‐choice trials were conducted
between20:00and22:00hinthedark.
A. fulica feeding strategy on papaya
Two trials, one each in laboratory and field, were carried out toqualifythefeeding
strategies of A. fulica. In the laboratory trial, individual snails (n=17) of mixed size were
offeredpapayaleavesfor8hinthedarkina2‐Lplasticcontainer.Theareaofleaveseaten
bysnailswasquantified.
Inthefieldtrial,10snailswerereleasednearthepapayatreetrunk at10pm in the
dark,andthetrialwasreplicatedfivetimes.Thesnailsselectedforthistrailhadmixedsizes
rangingfrom2to9cminlength.Observationsonthesnailmovementwerecollectedafter8
and24 h. Snailswerecategorisedinto three groups,small (<3cm), medium (3‐6cm), and
large(>6cm),fordataanalysis.Allsnailsusedinthisstudywerecollectedfromthewildand
keptfornomorethan24hforthebioassays.
Statistical analysis
Datacollectedonfeedingtrialsweresubjectedtoanormalitytestandthenormaldata
weresubjectedtoanalysisofvariancewhilenon‐normaldatawere analysed by non‐
parametrictests.Regressionanalyseswerecarriedouttoexaminetherelationshipbetween
snailbodysizeandfeedingefficiency,andbodysizeandsnailmovement/climbingefficiency.
U‐test was used to differentiate the climbing success in different snail size groups. Chi‐
squared test was used to analyse host preference. All analyses werecarriedoutatα=0.05
levelofsignificance.
RESULTS AND DISCUSSION
Assessment of A. fulica damage to papaya
The papaya trees were heavily infested with A. fulica. Snails inflicted two types of
damagetopapayafruit–primaryphysicaldamagetothepapayafruitandsecondaryfungal
infection to the physically damaged papaya fruit (Figure 1). The mean number of snails



231
recoveredpertreewas2.7±0.4.Themeannumberofsnailsdecreasedwiththeheightofthe
papayatree(F1,9=12.36;p=0.008).Anaverageof2.2±0.2fruitswereharvestedpertree,and
morethan80%ofthefruitswereinjuredbysnails.Ninetypercentoffruits hadsnailfaecal
contamination, and all had snail marks on them (Table 1). This suggests that snails stick
aroundthe fruits forlong enough tocontaminate them withslime andfaeces. Further,the
rasping slime of A. fulicacouldspreaddiseasesinpapaya(Floydetal.,2005).Noneofthe
fruitssampledwereinmarketableconditionswithoutathoroughwash.

Figure1. GiantAfricansnailAchatina fulica.A)Differentsizes,B)feedingonpapayatrunk,
C)snailsaggregatednearpapayatrunk,D)snailfeedingonpapaya, E) snail
climbing on papaya trunk, F) snail mating pair near papaya tree trunk. Source
Figure1D:Nelson(2012).
Table1. Damage causedbyAchatina fulicatopapayafruits,andthemarketabilitystatusof
thefruitscollected.Valuesrepresentmeanandstandarderror.
Tree size
No. of
snails
collected
tree-1
No. of
fruits
harvested
tree-1
Fruits with
abrasions
(%)
Fruits with
faecal
contamination
(%)
Fruits with
slimy marks
(%)
Fruits unfit
for market
(%)
Small 4.0±0.5 2.0±0.5 100 88.9±11.1 100 100
Medium 2.5±0.6 2.5±0.2 79.2±12.5 100 100 100
Tall 1.67±0.3 2.0±0.5 61.1±20.0 77.7±22.2 88.9±11.1 77.7±22.2
Overall 2.7±0.4 2.2±0.2 80.0±8.5 93.3±4.4 96.7±3.3 93.33±6.6
Forty‐one (41%) of the papaya fruits showing skin aberrations due to snail feeding
wereinflictedwithinternalinjuries.Snail‐infestedfruitsweresubjectedto fungal infection
2‐3dafterharvestandwerenotmarketable(Figure2).Twenty‐threesmall,immature,ripe

232
papaya fruits collected from30 trees were all damaged by snails. This suggests that snail
feedingcould induceprematureripening inpapaya.Mechanical damagecauses premature
senescencesettingandinducesfruitripeninginpapaya(QuintanaandPaull,1993;da Silva
etal.,2007).

Figure2. Giant African snail Achatina fulica. A) Snails competing while climbing papaya
trunk,B) snail feedingmarksonpapayafruitandsnailfaecesonpapayafruit, C)
andD)damagedpapayafruitinfectedwithfungus.
Host preference testing in A. fulica
The “papaya vs. tomato” host‐choice study showed that the snails like papaya more
thantomatoes (χ2=17.2; p<0.05).Only20%of thesnails movedtowardstomatocompared
with70%movingtowardspapaya(Figure3).Thissuggeststhepossibilityofanantifeedant
property in tomato that did not attract snails or repelled them. Plants from the family
Solanaceae contain some glycoalkaloids including solasonine andsoalmarginethatcould
have molluscicidal properties which can kill snails such as Lymnaea cubensisand
Biomphalaria glabrata (Alzérreca and Hart, 1982; Smith et al., 2001). Further, another
alkaloidfoundintomato‘tomatine’hasinsecticidalandinsect‐repellentproperties(Roddick,
1974)andhasbeenfoundeffectiveagainstB. glabrata(Hostettmannetal.,1982).

Figure3. Host‐choice preference between papaya and tomato plants in the giant African
snail Achatina fulica. Bars with different letters are significantly different at
p<0.005.



233
Inthe“papayavs.cabbage”host‐choicestudy,thesnailsshowed no significant
preference (χ2=0.72; p>0.05) (Figure 4). Another study on A. fulica in the pacific region
foundthat cabbageand papayaare importantcrops that areaffected by thesnail (Nelson,
2012).

Figure4. Host‐choice preference between papaya and cabbage plants in the giant African
snail Achatina fulica. Bars with different letters are significantly different at
p<0.005.
A. fulica feeding strategy on papaya
Intheleaf‐feedingtrail,theamountofpapayaleaveseatenbysnailswasproportionate
tothebodysizeofthesnails(F1,16=244.6;p<0.001).Whenweregressedtheleaffeedingper
cmbodysizeofsnail,thesmallersizesnailswerefoundtobevoraciousandatemoreleaves
perunitbodysizethanthelargersnails(F1,16=38.4;p<0.001)(Figure5).

Figure5. Feeding efficiency of the giant African snail Achatina fulicatestedbyoffering
papayaleavesfor24h.
Whenreleasednearthepapayatrunk,60%ofsnailsweresuccessful in climbingand
reachingthefruitsafter8h.Seventypercentofthesnailsremainedon thetree for longer
than 24 h. Medium‐sized snails were more efficient at climbing the trees (U0=5.99, df=2;
p<0.05)(Figure6).Theclimbingspeedofthesnailswasdirectlyproportionaltotheirbody
size(Figure7),butclimbingwaslessprevalentduringrainydays.Thissuggeststhat snails
takerefugeonpapayaindryconditions.Further,papayaandcabbagecouldbeusedassnail
trapcropsandthesnailsattractedtothemcouldbekilledorusedforotherpurposes
includingasachickenfeed(Diarraetal.,2015).

234

Figure6. Climbing success in different sized snails (Achatina fulica) after release near
papayatreetrunks.Thesizesofsnailsweregroupedintothreecategories:small
(<3cm),medium(3‐6cm),andlarge(>6cm).

Figure7. Relationship between the size of giant African snails(Achatina fulica) and their
climbingefficiencyonpapayatrunks.
CONCLUSIONS
Our study found that A. fulica can cause both primary and secondary damage to
papayaand other crops.Primary damagewas basically mechanical damage or abrasion to
papayaskinthatcouldalsoleadtofungalgrowthanddevelopment.Further,snailfaecesand
slimymarksalsoattractedfungalgrowth,andthatcouldmakethemunmarketable.Through
thefeeding‐choicetrails,wefoundthatsnailsrejecttomato.Thissuggeststhepresenceofan
antifeedantpropertyoftomatoagainstsnails.Furtherinvestigation is required to test the
efficacy of the tomato as a feeding‐deterrent against A. fulica. Finally, wefound premature
ripening of snail‐infected papaya. This needs further investigation of the effects of snail
feeding on the physiology of the papaya. In this study, we never recorded snails coming
downfromthepapayatree,whichraisesaquestionifsnailscouldmateandreproduceupon
thepapayatree.A. fulicaispresentinmostPacificIsland countries butstill some countries
includingFijiandTongaareprotectedfromitsmenace.Thesecountries couldpreventthe
introduction of A. fulica through stringent quarantine and biosecurity interception at the
borders.
ACKNOWLEDGEMENTS
We would like to acknowledge Plant protection technician Ian Faleono and
postgraduate students Graham Mala’efoo’o, Amanda Nasse and Leikitah Tamanalevu for
theirassistanceincollectingsnailsfromthefield.



235
Literature cited
Alzérreca,A.,andHart,G.(1982).Molluscicidalsteroidglycoalkaloids possessing stereoisomeric spirosolane
structures.Toxicol.Lett.12(2-3),151–155http://dx.doi.org/10.1016/0378‐4274(82)90178‐3.PubMed
Diarra,S.S.,Kant,R.,Tanhimana,J.,andLela,P.(2015).UtilisationofgiantAfricansnail(Achatina fulica)mealasa
proteinsourceforlayinghens.J.Agric.RuralDev.Trop.Subtrop.116,85–90.
Floyd,J.,Cohen,C.,Hitchcox,M.,Riherd,C.,Robinson,D.,Roda,A.,Smith,J.Stevens,T.,Stibick,J.,andZimmerman,
F. (2005). New PestResponse Guidelines ‐ Giant AfricanSnails: SnailPests in the Family Acatinidae(Beltsville,
MD,USA:USDAEmergencyandDomesticPrograms).
Hostettmann,K., Kizu,H.,andTomimori,T.(1982).Molluscicidal propertiesofvarious saponins.PlantaMed.44
(1),34–35http://dx.doi.org/10.1055/s‐2007‐971396.PubMed
Mead,A.(1973).AprognosisinthespreadofthegiantAfricansnailtocontinentalUnitedStates.Malacologia14,
437.
Muniappan,R.(1983).BiologicalcontrolofthegiantAfricansnail.AlafauAgric.Bull.8,43–46.
Nelson,S.(2012).InjuriesCausedbytheGiantAfricanSnailtoPapaya(Honolulu,HI,USA:UniversityofHawaii,
Manoa).
PlantProtectionOffice.(1996).IntroductionofgiantAfricansnailtovariousPacificislands.InSPCPestAdvisory
LeafletNo.6(Suva,Fiji:SouthPacificCommission).
Quintana,M.E.G.,andPaull,R.E.(1993).Mechanicalinjuryduringpostharvesthandlingofsolo’papayafruit.J.Am.
Soc.Hortic.Sci.118,618–622.
Roddick, J. (1974). The steroidal glycoalkaloid α‐tomatine. Phytochemistry 13(1), 9–25
http://dx.doi.org/10.1016/S0031‐9422(00)91261‐5.
Smith,D.B.,Roddick,J.G.,andJones,J.L.(2001).Synergismbetweenthepotatoglycoalkaloidsα‐chaconineandα‐
solanine in inhibition of snail feeding. Phytochemistry 57(2), 229–234 http://dx.doi.org/10.1016/S0031‐
9422(01)00034‐6.PubMed
TeixeiradaSilva,J.A.,Rashid,Z.,Nhut,D.T.,Sivakumar,D.,Gera,A.,Souza,M.T.,Jr,andTennant,P.F.(2007).Papaya
(Carica papayaL.)biologyandbiotechnology.TreeForest.Sci.Biotechnol.1,47–73.
Thiengo,S.C.,Faraco,F.A.,Salgado,N.C.,Cowie,R.H.,andFernandez,M.A.(2007).Rapidspreadofaninvasivesnail
in South America: the giant African snail, Achatina fulica, in Brasil. Biol. Invasions 9(6), 693–702
http://dx.doi.org/10.1007/s10530‐006‐9069‐6.
Thomsen,T.E.J.(1980).GiantAfricansnail.AlafauaAgric.Bull.5,21–23.


236
