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Home , Diaphorina, Diaphorina citri, Psyllidae, Tamarixia, Tamarixia radiata

citri Key words: New World ispresentedbasedonpublishedliterature. of thetwonaturalenemiesandtheirdistributionin in Guayaquil, Guayas province, Ecuador. A short diagnosis (HLB), the most destructive disease of disease destructive themost (HLB), main vectorofthebacteriathatcausesHuanglongbing ABSTRACT ) attacking psyllid nymphs on Cheilomenes sexmaculata ) and the adventitious ladybird beetle radiata enemies of for the first time the presence of two important natural not beendetected sofarinthiscountry. This paper reports branches of , presence of doi:10.4067/S0718-58392017000200180 Accepted: 24March2017. Received: 24November2016. Palmira, . Calle(CORPOICA), 23,Carrera 3, Continuo alPenal,Palmira, Valle, 4 3 * 15205, Maracaibo,4005,Zulia, Venezuela. 2 box 09-04-100,Guayaquil,Ecuador. 1 biological control agentsof Adrian Fuentes Yilda Chavez sexmaculata Cheilomenes radiata Tamarixia citri Corporación Colombiana de Investigación Agropecuaria Independent Researcher, Nocedal6455LaReina,Santiago,Chile. Corresponding author([email protected]). Universidad delZulia,Facultadde Agronomía, Apartado Postal Universidad Agraria delEcuador, Facultad deCiencias Agrarias, P.O. CHILEAN JOURNAL OF AGRICULTURAL RESEARCH 77(2)APRIL Kuwayama inEcuador D. citri D. citri Asian citruspsyllid,biologicalcontrol, , Ecuador, ,predator. 1 Kuwayama(:)isthe , Dorys T. Chirinos 1 , Rossana Castro inEcuador, i.e.,itsmainparasitoid (Waterston, 1922)(: was reported in Ecuador in 2013 on Citrus (L.)Jack (Rutaceae), but HLB has (Fabricius, 1781) (Coleoptera: CHILEAN JOURNAL OF AGRICULTURAL RESEARCH 77(2)APRIL spp., and jessamine, 1, 2* 1 , andTakumasa Kondo , GuillermoGonzález (Waterston) and M. paniculata Citrus . The - JUNE 2017 , (Fabricius) as Chica, 2014). (Rutaceae), in Guayaquil, Samborondón andDuran(Cornejo Citrus citri family Rutaceae. Although thediseasehasnotbeenfound, and an extensive list of host plants in about 25 genera in the that causesHLB(Bové,2006). This insecthasawidedistribution Liviidae), is themain vector in America and Asia ofthebacteria citrus psyllid (ACP), phloem and eventual death of theplant (Bové, 2006). The Asian production of starch in plants, resulting in clogging of the C. the phloem-limitedbacteria of the disease (Bové, 2006).Inthe New World, HLBiscaused by tristeza virus most serious citrus disease, even more serious than the citrus greeningorHuanglongbing(HLB).HLBisprobablythe the most important problems worldwide isthe disease knownas by theproliferationofinsectpeststhatlimititsyield.One The citrus industry like other agricultural activities is affected INTRODUCTION those ofthe females (Kondo et al., 2012). than longer times 1.5 being and setae fine and long by covered smaller in total length and wing extension, with the antennae is astrongsexualdimorphism,inwhichmalesareslightly than long; the wings are hyaline with pale yellow veins. There with widelyseparatedeyes,andtheheadproportionally wider adult parasitoidsaresmallwasps(0.92to1.04mmin length) Graham (1987) transferred it to the , currentlypartofPakistan(Parraetal.,2016).Subsequently, based on specimens collected in Punjab Province, northwest described by Waterston (1922) in the genus parasitizing nymphsof time in Ecuador basedon parasitoid specimens found naturally 1922) (Hymenoptera:Eulophidae)(Figure1A-1C)forthefirst more anteriorinmale)(Kondo etal.,2012). dark laterally and dorsomedially yellow (less pronounced and carina between the spiracle and median carina, and (iv) abdomen darkened dorsally), (iii) propodeal disc smooth and without a (ii) femora and tibia usually completely yellow (at most slightly combination of features: (i) Wing speculum with sparse setae, be differentiated bythefollowing relatedspecies fromclosely 4 3 americanus that areassociatedwiththeexcessive Herein wereportthepresenceof , Nestor Lemos Diaphorina Diaphorina was first detected in Ecuador in 2013 on branches of citrus, of branches on 2013 in Ecuador in detected first was spp.,andorange jessamine, - JUNE 2017 , andthusposingathreattoregionsthatarestillfree 1 , Diaphorina citri D. citri Candidatus . Murraya paniculata Tamarixia radiata Liberibacter asiaticus and Liberibacterasiaticusand Kuwayama (Hemiptera: Tamarixia Tamarixia radiata Tetrastichus Mercet. The (Waterston, wasfirst (L.) Jack Haliday, Citrus can D. D.

180 SCIENTIFICRESEARCH NOTE CHILEAN JOURNAL OF AGRICULTURAL RESEARCH 77(2)APRIL 2012), and Venezuela (Cermelietal.,2007). (Skelley and Hoy, 2004;Léon and Sétamou, 2010; Hoddle, (Pluke etal.,2008),Uruguay (DeLeonetal.,2010),USA et al., 2013), Paraguay (De Leon et al., 2010), Nicaragua (Agostini, 2011), Panama (Arredondo-Bernal Stansly, 2014), (González-Hernández et al., 2009), et al., 2001), Honduras (Agostini,2011), Jamaica (Chen and study), El Salvador (Hernández, 2016), (Etienne and Stansly, 2010),Cuba(Peralta,2002),Ecuador (present 2006), Colombia (Ebratt et al., 2011), Costa Rica (Qureshi Belize (Lopez et al., 2014), (Gómez-Torres et al., countries: the following (Lizondoetal.,2007), 2012). Inthe New World, programs (Etienneetal.,2001;Pluke2008;Hoddle, which iswhyit has been used inseveral biological control considered animportantmortalityfactorofthispsyllid, on thestudy(Parraetal.,2016). dependingpreference forfourth-andfifth-instarnymphs, fourth- andfifth-instarnymphsof (Parraetal.,2016). to the plantinorderto createashield when it turns intoa this phase,it attaches theremains ofthe psyllid nymph feeding on the hemolymph of the host and at the end of (Parra et al., 2016). When the egg hatches, the larva begins hatches willdevelopintoadulthoodduetocannibalism legs; iftwo eggs are laid,only one of the two larvae that venter of the psyllid, generally between the third pair of females generally lay one ortwo eggs at most onthe reproduction, i.e.,unfertilizedeggsproducemaleprogeny; ectoparasitoid specificto Cheilomenes sexmaculata B. Adult waspof Figure 1. A. Infestationof Tamarixia radiata T. radiata Source: PhotosbyD.T. Chirinos. 10X for A andC;40XforB,D,EF. (Fabricius,1781)isanidiobiont . E. Adult . Diaphorina citri underneath the mummified nymph of nymph mummified the underneath Tamarixia radiata T. radiata D. citri C. sexmaculata D. citri , witharrhenotokous Tamarixia radiata has been reported in withvariouspsyllidnymphs,someshowingexitholesoftheparasitoid withamarked attacksthird-, , “quadriplagiata”color form.F. Adult - JUNE 2017 is is D. citri was foundfeeding upon Fabricius (Coleoptera:Coccinellidae)(Figure1D-1F)also Hibiscus tiliaceus of Guayas,in a mangrove growing area on hibiscus leaves, (2015)intheprovinceEcuador byCornejoandGonzález Venezuela (Anguloetal.,2011). Itwasfirstreportedin Colombia (Kondo etal.,2015),Peru(González, 2007) and adventitious species, recordedfromChile(González,2006), Saeedifar, 2013).InSouth America, India (HusainandNath,1927)Iran(Rakhshani in (Linetal.,1973), (ChienandChu,1996), Yasuda, 2000).In Asia, India andtheOrientalregion Australia (Agarwalaand is aspeciesofladybirdbeetleoriginallyreportedfrom black suturalstripe. The pronotumalsomaybealmost totally blacktospecimenswith yellowelytrawithjust a has an extremely variable design, ranging from almost (Agarwala and Yasuda, 2000). (Acari), andearlystagesof butterfly larvae(Lepidoptera) (Cicadellidae), (Fulgoroidea),spidermites (Pseudococcidae), lacebugs(Tingidae), leafhoppers psyllids (), (Aleyrodidae), mealybugs more than 70species of ,aswell as many species of Worldwide, Koch were studied in Venezuela (Angulo et al., 2011). aspects of above, the species is an excellent predator. Biological feeding fromextrafloralnectariesalreadymentioned nectaries foundontheleafveins.Despiteoccasional Johnst. (Malvaceae), feeding on secretions from linear Another natural enemy, justbefore emergence.C. Adults of C. sexmaculata C. sexmaculata C. sexmaculata L. var. C. sexmaculata D. citri pernambucensis feedingon has been observed preying on Cheilomenes sexmaculata . , “sexmaculata”color form. Cheilomenes sexmaculata Cheilomenes sexmaculata C. sexmaculata T. radiata isknownto occur Aphis craccivora Tamarixia radiata (Arruda) I.M. . D.Pupaof isan .

181 CHILEAN JOURNAL OF AGRICULTURAL RESEARCH 77(2)APRIL D. citri known presence inEcuador oftwonaturalenemies of America alsohavefairlyvariabledesigns. to almostthecenterofdisc.SpecimensfoundinSouth and a discal projection that goesfrom the anterior angles totally black,orhaveclearareasatthebase,withmargins of different stages ofdevelopment (eggs,nymphs and adults) branches about 10 cm long of , oneachcollecting trip, 20-40 samplesofyoung of collecting the For identification. their facilitate and stage to thelaboratoryinorderallowthemreachadult collected province of Guayas, Ecuador. Predatory larvae were (02°06’13.9” N,79°54’12.3” W, 4.5 m a.s.l.), Guayaquil, in April, June and October 2016, in Los Samanes Park A search fornatural enemies of MATERIALS ANDMETHODS morphology basedonpublishedliterature. information ontheirdistribution intheNew World andtheir beetle Asian citrus psyllid, and a generalist predator, the ladybird (2012). The coccinellid (2012). The characteristics givenbyGraham(1987)andKondoetal. parasitoids (malesandfemales)wereidentifiedusingthe overlooked parasitizedpsyllidnymphs. The emerged adult cages in order to obtain adult parasitoids from any parasitization, brancheswereplacedinentomological After separating the psyllid nymphs with symptoms of capsules forthe eventual emergence ofadult parasitoids. branches andplacedindividuallyintransparentgelatin multiplied by100. parasitized nymphsbythetotalnumberofsampled, parasitization was calculated bydividing the number of nymphs (categoriesiiandiii)wascountedtherateof of non-parasitized(categoryi)andparasitizedpsyllid October 2016,respectively. Foreach collection, the number of three collecting trips were carried out, in April, June and holes. total exit A with nymphs mummified (iii) and holes), typical symptomsofamummifiednymph,withoutexit nymphs (nymphs with a brownish coloration, showing nymphs (nymphswithyellowish coloration), (ii) parasitized and separatedintothreecategories:(i)non-parasitized China) Kong, Hong series, 140 SMZ (Motic magnification branches wereobservedunderastereoscopewith10to40X del Ecuador, Guayaquil, Ecuador. deCiencias Facultad de laUniversidad Agrarias Agraria material isdepositedintheentomological collectionofthe images by Iablokoff-Khnzorian (1982). All studied identified fromthegenitalia basedondescriptionsand González (Santiago,Chile), forwhichspecimenswere specimens depositedintheprivatecollectionofGuillermo identified bycomparing itsmorphology and design with The objectiveofthispaperwastoreportthefirst The mummified nymphs were removed from the D. citri Cheilomenes sexmaculata : Tamarixia radiata in situ werecollected. Psyllidnymphspresentonthese and taken alive (together with their prey) Cheilomenes sexmaculata , a M. paniculata

specific parasitoidofthe . We provided also brief D. citri wascarried out infested with - JUNE 2017 was was out; the adults of the psyllid nymph becomesbrownish and eventually dries the parasitoidlarvadevelopsunderneathbodyofitshost, 1B)wereobserved. fully-developed parasitoids(Figure As and pupae nymphs, mummified the of underside the On 1C). obtained from mummified nymphs of were 11.9% (n=1044)in April and21.5%(n=709)inJune. parasitoid accordingtoEtienneetal.(2001).Parasitismrates suspected, because this is a characteristic feature of this the parasitized nymphs, the presence of by the position ofthe exitholes ontheanterior part of no adultparasitoidwaspswerecollected.However, in April andJune2016,forthesefirsttwo collections holes wereobtainedinsamplesofplantmaterialcollected Only oldparasitized nymphs (psyllid mummies) with exit RESULTS ANDDISCUSSION et al.,2007;Ebratt2011; Kondoetal.,2012). radiata (malesandfemales)coincidewiththediagnosesof (n =1655). The morphologicalfeaturesoftheadultparasitoid (Parra etal.,2016). The parasitismrateinOctoberwas81.1% hole onthethoraxatanteriorpartofbody(Figure1A) the generalistpredator there. The presence ofthis specific parasitoid Currently, end of2015,graduallybeginning its colonizationprocess. have alreadyarrivedtothestudiedareainEcuadorby October (11.9% to 81.1%) suggeststhat the parasitoid may irregular transversebandsinzigzag(Figure1F). elytra and six black spots in each elytron that form three form thatgivesthenametospeciesepithet,withred same color on the elytra (Figure 1E); and the “sexmaculata” delimited byalarge blackcrossandathinborderofthe which there is adesignmade up offourlarge red markings corresponds towhatisknownas“quadriplagiata”in sexmaculata feeding onpsyllidnymphsof the lacewing a studyconductedinIndia, control by Venezuela, where low populations were attributed to the citri other naturalenemiesinthecontrolofpopulations importance ofthebiologicalcontrolexertedbytheseand despite itsrecentintroduction. Thus, wesuggest thegreat why high populations of this psyllid have not been observed of ) arethethreemosteffective naturalenemies citri of found. were To report official thefirst is this ourknowledge, until now no natural enemies of this important insect pest detected in Ecuador in2013(Cornejo andChica,2014)but D. citri In October, adult parasitoid wasps of A ladybird beetle, The increase in the rates from April to T. radiata inEcuador. inEcuador. This issimilartoasituationreportedfor providedbyvariousauthors(Graham,1987;Cermeli (ShivankarandRao,2010). T. radiata T. radiata and wereobservedinthepresentstudy;one Mallada boninensis C. sexmaculata T. radiata has fully established as a natural enemy hasfullyestablishedasanaturalenemy (Cermeli et al., 2007). According to C. sexmaculata, C. sexmaculata (Figure 1C) emerge through a C. sexmaculata D. citri asnatural enemies of (Okamoto)(Neuroptera: Diaphorina citri D. citri , probablyexplains . Two formsof also was found T. radiata , T. radiata T. radiata T. radiata (Figure 1A- were was , and , and was and D. D. D. D. C. C. T. T.

182 CHILEAN JOURNAL OF AGRICULTURAL RESEARCH 77(2)APRIL Cornejo, X.,yGonzález,G.2015.Contribución alconocimiento Cornejo, J.F., and Chica, E.J. 2014. First record of Chien, C.C.,andChu, Y.I. 1996.Biologicalcontrolofcitrus Chen, X.,andStansly, P. 2014. Biologyof Cermeli, M.,Morales,P., Perozo,J.,yGodoy, F. 2007. Bové, J.M. 2006. Huanglongbing: A destructive, newly-emerging, Arredondo-Bernal, H.C.,Sánchez-González,J.A.,yMellín- Angulo, J., Arcaya, E.,yGonzález,R.2011. Aspectos biológicos Agostini, J.P. 2011. Cítricos: El HLBysuprevención. Revista de Agarwala, B.K., and Yasuda, H.2000. Competitive ability REFERENCES manuscript andtheEnglishtext. University, Canberra, Australia) forkindlyreviewingthe Many thankstoPennyGullan(The Australian National ACKNOWLEDGEMENTS Puerto Rico,Uruguay, USA and Venezuela. Honduras, Jamaica,Mexico,Nicaragua,Panama,Paraguay, Costa Rica, Cuba, Ecuador, El Salvador, Guadeloupe, is updatedtoinclude Argentina, Belize, Brazil, Colombia, this study, thedistributionof nymphs of psyllid parasitizing and upon preying Ecuador, in time first Cheilomenes sexmaculata Herein wereporttwoimportantnaturalenemies, CONCLUSIONS (Ecuador) 8(2):76-80. Perú. RevistaCientíficadeCiencias Naturalesy Ambientales nuevos registros de Coleoptera: Coccinellidae para Ecuador y Vandenberg y de la faunaentomológica de los manglares: and orangejasminetrees.JournalofInsectScience14(298):1-3. citri Fertilizer TechnologyCenter, Taipei, Taiwan. and Fertilizer Technology CenterBookSeriesNo.47.Foodand Control inSystemsofIntegrated Pest Management-1996. Food psyllid, review. FloridaEntomologist97:1404-1413. disease vector (Hymenoptera: Eulophidae), parasitoid ofthe citrus greening Entomotropica 22:181-184. radiata Kuwayama (Hemiptera, Psyllidae) y presencia de Distribución delpsílidoasiático de loscítricos century-old diseaseofcitrus.JournalPlantPathology88:7-37. la FAO paraMesoamérica,CiudaddePanamá,Panamá. Diaphorina citri Rosas, M.A.2013. Taller subregionaldecontrolbiológico Venezuela) 45(4):423-431. Boletín delCentrodeInvestigacionesBiológicas(Maracaibo, alimentado con de Investigaciones Agropecuarias N°37.p.677. worldwide checklistofpreys.Journal Aphidology 14:1-20. sexmaculata of ladybird predators of aphids: A review of Menochilus sexmaculatus (Hemiptera: Psyllidae) in Ecuador infesting urban citrus (Waterston) (Hymenoptera, Eulophidae) en Venezuela. Diaphorina citri Diaphorina citri (Fabr.) (Coleoptera: Coccinellidae) with a Diaphorina citri Aphis craccivora , vector del HLB. p. 61. Oficina Subregional de Subregional Oficina 61. p. HLB. del vector , Cheilomenes sexmaculata in Taiwan. p.93-105.BiologicalPest and (F.) (Coleoptera:Coccinellidae) , respectively. As aresultof T. radiata (Hemiptera: ): amini Koch(Hemiptera: ). Tamarixia radiata intheNew World Tamarixia radiata Olla roatanensis Fabricius, dos Diaphorina citri Cheilomenes - Diaphorina JUNE 2017 Tamarixia , forthe

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183 CHILEAN JOURNAL OF AGRICULTURAL RESEARCH 77(2)APRIL Peralta, E.L.2002.Principalesenfermedadesemergentes que Lopez, V., Moore,K.,Garcia,M.,andManzanero-Majil, V. 2014. Lizondo, M.,Gastaminza,G.,Costa, A., Augeir, L.,Goméz, Lin, S.J.,Ke, Y.F., and Tao, C.C. 1973.Bionomicsobservationand Léon, J.H.,andSétamou,M.2010.Molecularevidencesuggests Parra, J.R., Alves, G.,Diniz, A.J., and Vieira, J.2016. 17:193-202. plagas emergentes deloscítricos. Revista de Protección Vegetal amenazan lacitriculturadelospaísesdelCaribe. Taller sobre Journal ofIntegratedPestManagement7:1-11. Liviidae): massrearingandpotentialuseoftheparasitoidinBrazil. radiata Manual forthemassproductionofparasitoid Industrial y Agricola de Tucumán 84:21-22. (Hymenoptera: Eulophidae)innorthwestern Argentina. Revista M., and M., Willink, of 2007.Records M. Journal ofHorticulturalSocietyChina19:234-242. integrated control ofcitruspsylla, Society of America 103(1):100-110. Mexico representasinglespecies. Annals oftheEntomological radiata that populations of the Asian citrus psyllid parasitoid radiata Food and Agriculture Organization oftheUnitedNations,Belize. cultured on (Hymenoptera:Eulophidae)× (Hymenoptera:Eulophidae)from Texas, Florida,and on its host, Murraya paniculata Diaphorina citri (OrangeJasmine)inBelize. Diaphorina citri Diaphorina citri (Asian citrus psyllid), Tamarixia radiata Kuwayama. - (Hemiptera: JUNE 2017 Tamarixia Tamarixia Tamarixia

Skelley, L.H.,andHoy, M.A.2004. A synchronousrearing method Shivankar, V.J., and Rao, C.N. 2010. Psyllids and their Rakhshani, E., and Saeedifar, A. 2013. Seasonal fluctuations, Qureshi, J.A., and Stansly, P.A. 2010. Stansly,and P.A.R.W.,flushing J.A., Pluke, Citrus Qureshi, 2008. Biological Control29:14-23. for the Asian citruspsyllidanditsparasitoidsinquarantine. 16(1):1-4. management. PestManagementinHorticulturalEcosystems Entomological Science16:17-25. Diaphorina citri spatial distributionandnaturalenemiesof Asian citruspsyllid (accessed November2016). biocontrol.entomology.cornell.edu/parasitoids/Tamarixia.php citri [Hymenoptera: Eulophidae],anectoparasitoidof in PuertoRico.FloridaEntomologist91:36-42. and parasitismby patterns, Kuwayama [Hemiptera: Psyllidae]. Available at https:// Diaphorina citri Kuwayama (Hemiptera: Psyllidae) inIran. Kuwayama(Hemiptera:Psyllidae) Tamarixia radiata (Hemiptera:Psyllidae)populations Tamarixia radiata (Hymenoptera: Eulophidae) (Hymenoptera:Eulophidae) Diaphorina Waterston

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