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.
Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae) was successfully 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 cladodes 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 programs 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 evaluation of biological control agents.
A literature review of natural enemies of Cactoblastis spp. (Pemberton & Cordo 2001) revealed the occurrence of at least 8 or 9 parasitons, among which the braconid Apanteles alexanderi Brèthes (Hymenoptera: 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 potential 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 species, A. alexanderi and the recently described Apanteles opuntiarum Martínez & Berta (Martínez et al. 2012). Both Apanteles spp. have gregariously 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 Agriculture 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 (Gestion 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 occurrence of plant patches in the Cactaceae family. In patches containing more than 50 plants of the same species, at least 50 plants were visually 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 surveyed.
At least 8 species of pyralids in the genera Cactoblastis, Sigelgaita, Tucumania, Salambona, and Ozamia were found attacking 17 species 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 pyralid. 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, occurring at 13 sites on at least 4 species of Cactaceae. The other pyralids 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 species 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. cactorum, 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. opuntiarum. 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., Argyrotaenia 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. opuntiarum (Martínez et al. 2012).
Occurrence of Apanteles species found attacking cactus-feeding Pyralidae on associated host plant species in Argentina.
Our 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 Natalia Cuadra (FuEDEI) for their field assistance and appreciate the comments by Juan Briano (FuEDEI) and Angela Galette (USDA-ARS) on earlier drafts of this manuscript. We also acknowledge James E. Hayden (FDACS) for moth identification. We dedicate this work to the late Fernando Navarro, deceased 23 Aug 2014.