Field exploration in Argentina for cactophagous lepidopteran hosts parasitized by the recently described braconid parasitoid Apanteles opuntiarum Martínez & Berta (Hymenoptera: Braconidae) revealed a host range restricted to Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae) and C. doddi. Field collections of cactophagous larvae parasitized by the congeneric and sympatric parasitoid A. alexanderi included the host species C. bucyrus, Sigelgaita nr. chilensis, Tucumania sp., Tucumania tapiacola and Salambona sp. If a narrow host range for A.opuntiarum is confirmed in quarantine with North American cactus-feeding species, then this parasitoid could be released as a biological control agent for C. cactorum with little or no risk to non-target species.Las exploraciones de campo en Argentina de larvas hospedadoras cactófagas parasitadas por Apanteles opuntiarum Martínez & Berta (Hymenoptera: Braconidae), un bracónido recientemente descripto, revelaron un espectro de hospedadores restringido a Cactoblastis cac­torum (Berg) (Lepidoptera: Pyralidae) y C. doddi. Las colecciones de campo de larvas cactófagas parasitadas por la especie congenérica y simpátrica A. alexanderi identificaron a C. bucyrus, Sigelgaita nr. chi­lensis, Tucumania sp., Tucumania tapiacola y Salambona sp. como es­pecies hospedadoras. Si se confirma en cuarentena el estrecho rango de hospedadores de A. opuntiarum sobre especies norteamericanas que se alimentan de cactus, podría ser liberado como agente de con­trol biológico de C. cactorum, con bajo riesgo o ninguno a especies no blanco.Fil: Varone, Laura. Fundación para el Estudio de Especies Invasivas; ArgentinaFil: Logarzo, Guillermo Alejandro. Fundación para el Estudio de Especies Invasivas; ArgentinaFil: Martinez, Juan Jose. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Museo Argentino de Ciencias Naturales ; ArgentinaFil: Navarro, Fernando. Universidad Nacional de Tucumán. Facultad de Ciencias Naturales e Instituto Miguel Lillo. Instituto Superior de Entomología; ArgentinaFil: Carpenter, James E.. United States Department of Agriculture; Estados UnidosFil: Hight, Stephen D.. United States Department of Agriculture; Estados Unido

Carpenter, James E.

Hight, Stephen D.

Logarzo, Guillermo Alejandro

Martinez, Juan Jose

Navarro, Fernando

Varone, Laura

Florida Entomologist

English

LAReferencia - Red Federada de Repositorios Institucionales de Publicaciones Científicas Latinoamericanas

1FuEDEI, Fundación para el Estudio de Especies Invasivas, Hurlingham (1686), Buenos Aires, Argentina2CONICET–División Entomología, Museo Argentino de Ciencias Naturales ‘Bernardino Rivadavia’, Buenos Aires, Argentina3Instituto Superior de Entomología “Dr. Abraham Willink”, (4000) San Miguel de Tucumán, Tucumán, Argentina4USDA-ARS-CPMRU, Tifton, GA 31794, USA5USDA-ARS-CMAVE, Center for Biological Control, FAMU, Tallahassee, FL 32308, USA*Corresponding author; E-mail: lauvarone@fuedei.org†Deceased: 23 August 20142015 — Florida Entomologist — Volume 98, No. 2  803Field host range of Apanteles opuntiarum (Hymenoptera: Braconidae) in Argentina, a potential biocontrol agent of Cactoblastis cactorum (Lepidoptera: Pyralidae) in North AmericaLaura Varone1,*, Guillermo Logarzo1, Juan José Martínez2, Fernando Navarro3,†, James E. Carpenter4, and Stephen D. Hight5Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae) was suc-cessfully used for biological control of Opuntia spp. (Caryophyllales: Cactaceae) in Australia and South Africa, where no native cacti occur (Dodd 1940; Pettey 1948). Larvae feed gregariously inside the clad-odes of many species of Opuntia, often causing death of the plants (Starmer et al. 1988). Since 1989, this South American moth (Mann 1969) has been invading the southeastern United States, threatening the unique cactus diversity and industry in the western United States and Mexico (Hight & Carpenter 2009). Cactoblastis cactorum also was detected on 2 Mexican islands, but was eradicated during 2007–2009 by several control measures, including plant removal and sanitation to lower the population density, followed by the sterile insect technique (SIT) (Carpenter et al. 2008; Hight et al. 2008). In the United States, these control measures also were adopted. However, these action pro-grams targeting C. cactorum outbreaks were not adequately funded and did not prevent the moth from spreading further to the west (US-DA APHIS 2009). Although chemical control can be effective in some cases (Bloem et al. 2005), it has not been recommended because the Opuntia species often are associated with sensitive ecological areas (Habeck & Bennet 1990). In addition, aerial insecticide applications would probably not be effective because the damaging stage of the insect is endophagous (Vigueras & Portillo 2001). Currently, efforts are underway to develop sustainable control tactics, including the evalua-tion of biological control agents.A literature review of natural enemies of Cactoblastis spp. (Pem-berton & Cordo 2001) revealed the occurrence of at least 8 or 9 para-sitoids, among which the braconid Apanteles alexanderi Brèthes (Hy-menoptera: Braconidae) was the most frequent, with parasitism rates as high as 30%. However, because of its broad host range (De Santis 1967), this parasitoid was dropped from further consideration as a po-tential biological control agent in North America (Pemberton & Cordo 2001). After Parker et al. (1950) first reported A. alexanderi from C. cactorum, all braconids subsequently associated with this moth have been identified arbitrarily as this species. However, recent molecular and taxonomic studies confirmed the presence of 2 congeneric spe-cies, A. alexanderi and the recently described Apanteles opuntiarum Martínez & Berta (Martínez et al. 2012). Both Apanteles spp. have gre-gariously feeding larvae, attack the larval stage of their host, and are koinobiont endoparasitoids. Preliminary field observations revealed A. opuntiarum to have a more restricted host range than A. alexanderi, and to show the highest parasitism rates among 7 other parasitoids that attack C. cactorum in Argentina (Mengoni Goñalons et al. 2014). Consequently, A. opuntiarum is a candidate for biological control of C. cactorum. The parasitoid was first exported from Argentina in Mar 2013 to the quarantine facility of the Florida Department of Agricul-ture and Consumer Services, Division of Plant Industry, Gainesville, Florida, USA. A culture is being established in quarantine to perform host specificity tests with cactophagous moths native to the United States. Export permits were issued by Argentine regulatory agencies (Gestión de Uso Sustentable de los Recursos Naturales, Ministerio de Producción, Gobierno de Entre Ríos; Dirección de Fauna Silvestre and Dirección Nacional de Ordenamiento Ambiental y Conservación de la Biodiversidad Permit # 4612/13; Servicio Nacional de Sanidad y Calidad Agroalimentaria; DNPV Permit # 87). The importation permit (P526P-Permit # 13-00380) was issued by the United States Department of Agriculture–Animal and Plant Health Inspection Service.The native range of C. cactorum in Argentina (roughly 23°53’S to 40°48’S; 58°38’W to 66°10’W) was surveyed from Aug 2007 to Mar 2014 for the presence of cactus-feeding moth larvae to determine the field host range of A. opuntiarum. Sites were selected by the occur-rence of plant patches in the Cactaceae family. In patches containing more than 50 plants of the same species, at least 50 plants were visu-ally inspected for the presence of larval damage. In smaller patches, all plants of the same species were inspected. Damaged plants were dissected and examined for the presence of cactus-feeding larvae, and all larvae and their host plants were returned to the laboratory. Once in the laboratory, larvae were reared on the host plant from which they were collected and checked every 2–3 d for the presence of parasitoid cocoons. In total, 394 sites containing 495 cactus patches were sur-veyed.804 2015 — Florida Entomologist — Volume 98, No. 2At least 8 species of pyralids in the genera Cactoblastis, Sigelgaita, Tucumania, Salambona, and Ozamia were found attacking 17 spe-cies of Cactaceae in the genera Opuntia, Trichocereus, Cleistocactus, Monvillea, and Harrisia at 133 sites in Argentina (Table 1). Collection of Sigelgaita nr. chilensis was the second for this genus known to occur east of the Andes Mountains (Monteiro & Becker 2002) and the first for Argentina. Of the 3 species of Cactoblastis collected from Argentine Cactaceae, C. cactorum was, by far, the most frequently observed py-ralid. Cactoblastis cactorum larvae attacked 10 Opuntia spp. at 95 sites; C. doddi Heinrich was found at 9 sites on 2 Opuntia spp.; and C. bucyrus Dyar was found at only 3 sites on 1 species of Cactaceae. Among the non-Cactoblastis moths, Ozamia spp. were found most frequently, oc-curring at 13 sites on at least 4 species of Cactaceae. The other py-ralids were found at 1 to 8 sites (Table 1). Apanteles parasitoids were found at a total of 54 sites; A. opuntiarum and A. alexanderi occurred at 44 and 10 sites, respectively. Apanteles opuntiarum parasitized only C. cactorum and C. doddi, whereas A. alexanderi parasitized the other pyralid species except Ozamia (only non-parasitized larvae were found). Both Apanteles species were sympatric at 7 sites and shared similar geographical ranges (Fig. 1). Although these 2 Apanteles spe-cies parasitized different host species, the host larvae attacked often shared the same Opuntia host species. For example, A. opuntiarum attacked C. cactorum and A. alexanderi parasitized Tucumania sp., both were collected on O. elata var. cardiosperma and O. megapotamica (Table 1), and both were found in the same habitat. Furthermore, over 100 individuals of Tucumania tapiacola Dyar were collected at 2 sites cohabiting and feeding on the same plants and cladodes with C. cac-torum, but only A. alexanderi emerged from T. tapiacola larvae (n = 11), whereas A. opuntiarum emerged from the larvae of C. cactorum. To date, all collections of parasitized C. cactorum larvae were attacked only by A. opuntiarum. Cactoblastis doddi, whose primary host plant was O. sulphurea Gillies ex Salm-Dyck, also was parasitized by A. opun-tiarum. Cactoblastis bucyrus, whose host plant was the tree-like cactus Trichocereus atacamensis var. pasacana (F.A.C. Weber ex Rümpler) F. Ritter, was parasitized by A. alexanderi. Host plants of C. doddi and C. bucyrus occurred in the same habitat and insects were collected in close proximity to one another. Apanteles alexanderi was reported to attack other cactophagous Lepidoptera such as Plutella sp., Argyrotae-nia sp., and Eulia sp. (De Santis 1967). However, these host records may be dubious given the discovery that historical identifications of “A. alexanderi” were composed of 2 species, A. alexanderi and A. opun-tiarum (Martínez et al. 2012).Table 1. Occurrence of Apanteles species found attacking cactus-feeding Pyralidae on associated host plant species in Argentina.Pyralid speciesCactus host # sites Apanteles spp. # sitesCactoblastis cactorum (Berg)Opuntia ficus-indica L. 43 A. opuntiarum 26Opuntia elata var. cardiosperma (K. Schum.) R. Kiesling 21 A. opuntiarum 6Opuntia megapotamica Arechav. 9 A. opuntiarum 5Opuntia elata var. elata Link & Otto ex Salm-Dyck 5 A. opuntiarum 3Opuntia anacantha Speg. 7 A. opuntiarum 1Opuntia quimilo K. Schum. 4 A. opuntiarum 1Opuntia robusta H. L. Wendl. ex Pfeiff. 2 —Opuntia leucotricha DC. 2 —Opuntia auriantiaca Gilles ex Lindley 1 —Opuntia penicilligera Speg. 1 —Cactoblastis doddi HeinrichOpuntia sulphurea 8 A. opuntiarum 1Opuntia penicilligera 1 A. opuntiarum 1Cactoblastis bucyrus DyarTrichocereus atacamensis var. pasacana 3 A. alexanderi 2(F. A. C. Weber ex Rumpler) Britton & RoseSigelgaita nr. chilensisOpuntia elata var. cardiosperma 2 A. alexanderi 1Tucumania tapiacola DyarOpuntia ficus-indica 2 A. alexanderi 2Tucumania sp.Opuntia megapotamica 5 A. alexanderi 2Opuntia elata var. cardiosperma 2 A. alexanderi 2Opuntia sulphurea 1 —Salambona sp.Trichocereus terscheckii (Parm. ex Pfeiff.) Britton & Rose 1 A. alexanderi 1Ozamia spp.Cleistocactus spp. 4 —Opuntia spp. 4 —Monvillea cavendishii (Monv.) Britton & Rose 3 —Harrisia bonplandii (J.Parm. ex Pfeiff.) Britton & Rose 2 —Total 133 54Scientific Notes 805Our findings revealed that the host range of A. opuntiarum was restricted to 2 Cactoblastis species, enhancing the potential of this parasitoid as a biological control agent of the invasive cactus moth, C. cactorum, in North America. Finding C. cactorum larvae parasitized by A. opuntiarum and non-target larvae parasitized by A. alexanderi on the same Opuntia spp. plants (often the same cladodes), provided strong evidence that the limited host range observed was due to host specificity and not due to geographical or host plant isolation of the pyralid larvae. If a narrow host range is confirmed in quarantine with North American cactus-feeding species, then A. opuntiarum will likely be released for biological control of C. cactorum in the United States, with little or no risk to non-target species.We thank Carolina Mengoni Goñalons, Carolina Coulin, and Nata-lia Cuadra (FuEDEI) for their field assistance and appreciate the com-ments by Juan Briano (FuEDEI) and Angela Galette (USDA-ARS) on ear-lier drafts of this manuscript. We also acknowledge James E. Hayden (FDACS) for moth identification. We dedicate this work to the late Fer-nando Navarro, deceased 23 Aug 2014.SummaryField exploration in Argentina for cactophagous lepidopteran hosts parasitized by the recently described braconid parasitoid Apanteles opuntiarum Martínez & Berta (Hymenoptera: Braconidae) revealed a host range restricted to Cactoblastis cactorum (Berg) (Lepidoptera: Py-ralidae) and C. doddi. Field collections of cactophagous larvae parasit-ized by the congeneric and sympatric parasitoid A. alexanderi included the host species C. bucyrus, Sigelgaita nr. chilensis, Tucumania sp., Tucumania tapiacola and Salambona sp. If a narrow host range for A. Fig. 1. Distribution of Apanteles opuntiarum (circles) and Apanteles alexanderi (triangles) that emerged from species of Pyralidae collected in Argentina, Aug 2007–Mar 2014.806 2015 — Florida Entomologist — Volume 98, No. 2opuntiarum is confirmed in quarantine with North American cactus-feeding species, then this parasitoid could be released as a biological control agent for C. cactorum with little or no risk to non-target species.Key Words: parasitoid; host range; cactus moth; Apanteles alexan-deri; Apanteles opuntiarum; biological controlSumarioLas exploraciones de campo en Argentina de larvas hospedadoras cactófagas parasitadas por Apanteles opuntiarum Martínez & Berta (Hymenoptera: Braconidae), un bracónido recientemente descripto, revelaron un espectro de hospedadores restringido a Cactoblastis cac-torum (Berg) (Lepidoptera: Pyralidae) y C. doddi. Las colecciones de campo de larvas cactófagas parasitadas por la especie congenérica y simpátrica A. alexanderi identificaron a C. bucyrus, Sigelgaita nr. chi-lensis, Tucumania sp., Tucumania tapiacola y Salambona sp. como es-pecies hospedadoras. Si se confirma en cuarentena el estrecho rango de hospedadores de A. opuntiarum sobre especies norteamericanas que se alimentan de cactus, podría ser liberado como agente de con-trol biológico de C. cactorum, con bajo riesgo o ninguno a especies no blanco.Palabras Clave: parasitoide; espectro de hospedadores; polilla de la tuna; Apanteles alexanderi; Apanteles opuntiarum; control biológicoReferences CitedBloem S, Mizell RF, Bloem KA, Hight S, Carpenter JE. 2005. Laboratory evaluation of insecticides for control of the invasive Cactoblastis cactorum (Lepidop-tera: Pyralidae). Florida Entomologist 88: 395-400.Carpenter JE, Hight SD, Bellom A. 2008. Eradication and containment of Cacto-blastis cactorum in Mexico and the United States. XXIII International Con-gress of Entomology, Durban, South Africa. 6-12 Jul.De Santis L. 1967. Catálogo de los Himenópteros Argentinos de la serie para-sítica, incluyendo Bethyloidea. La Plata, Provincia de Buenos Aires, Gober-nación.Dodd AP. 1940. The biological campaign against prickly-pear. Brisbane, Austra-lia, Commonwealth Prickly Pear Board.Habeck DH, Bennet FD. 1990. Cactoblastis cactorum Berg (Lepidoptera: Pyrali-dae), a phycitine new to Florida. Florida Department of Agriculture and Con-sumer Services, Division of Plant Industry. Entomology Circular 333.Hight SD, Carpenter JE. 2009. Flight phenology of male Cactoblastis cactorum (Lepidoptera: Pyralidae) at different latitudes in the southeastern United States. Florida Entomologist 92: 208-216.Hight SD, Carpenter JE, Bloem S, Bloem KA, Floyd J. 2008. Development of con-trol tactics against the invasive cactus moth, Cactoblastis cactorum, in North America. XXIII International Congress of Entomology, Durban, South Africa. 6-12 Jul.Mann J. 1969. Cactus-feeding insects and mites. United States National Muse-um Bulletin. Washington D. C., USA Smithsonian Institution Press 256: 158.Martínez JJ, Berta C, Varone L, Logarzo GA, Zamudio P, Zaldívar-Riverón A, Agui-lar-Velasco RG. 2012. DNA barcodes and morphological identification of the southern South American species of Apanteles (Hymenoptera: Braconidae) parasitoids of cactus feeding moths (Lepidoptera: Pyralidae: Phycitinae). In-vertebrate Systematics 26: 435-444.Mengoni Goñalons C, Varone L, Logarzo GA, Guala ME, Rodriguero M, Hight SD, Carpenter JE. 2014. Geographical range and laboratory studies on Apan-teles opuntiarum (Hymenoptera: Braconidae) in Argentina, a candidate for biological control of Cactoblastis cactorum (Lepidoptera: Pyralidae) in North America. Florida Entomologist 97: 1458-1468.Monteiro RF, Becker VO. 2002. A new Sigelgaita Heinrich (Lepidoptera, Pyrali-dae, Phycitinae) feeding on cacti in Brazil. Revista Brasileira de Zoologia 19: 299-304.Pemberton RW, Cordo HA. 2001. Potential and risks of biological control of Cac-toblastis cactorum (Lepidoptera: Pyralidae) in North America. Florida Ento-mologist 84: 513-526.Pettey FW. 1948. The biological control of prickly pear in South Africa. Sci-ence Bulletin, Department of Agriculture of the Union of South Africa 271: 1-163.Starmer WT, Aberdeen V. Lachance MA. 1988. The yeast community associated with decaying Opuntia stricta (Haworth) in Florida with regard to the moth, Cactoblastis cactorum (Berg). Florida Scientist 51: 7-11.USDA-APHIS-PPQ. 2009. United States Department of Agriculture, Animal and Plant Health Inspection Service, Plant Protection and Quarantine. 2009. Cactus Moth Program Annual Report. USDA-PPQ Eastern Region, Pensacola, Florida, USA.Vigueras GAL, Portillo L. 2001. 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Field host range of Apanteles opuntiarum (Hymenoptera: Braconidae) in Argentina, a potential biocontrol agent of Cactoblastis cactorum (Lepidoptera: Pyralidae) in North America

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Field host range of Apanteles opuntiarum (Hymenoptera: Braconidae) in Argentina, a potential biocontrol agent of Cactoblastis cactorum (Lepidoptera: Pyralidae) in North America

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