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Prodilis hattie Gordon and Hanley (Coleoptera: Coccinellidae: Cephaloscymnini): New Research on Native Natural Predators of the False Carmine Cochineal, Dactylopius opuntiae (Cockerell) (Hemiptera: Dactylopiidae), in the Brazilian Semiarid Region

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Giorgi, José Adriano, Barbosa, Paulo Roberto Ramos, Oliveira, José Eudes De Morais, Torres, Jorge Braz (2018): Prodilis hattie Gordon and Hanley (Coleoptera: Coccinellidae: Cephaloscymnini): New Research on Native Natural Predators of the False Carmine Cochineal, Dactylopius opuntiae (Cockerell) (Hemiptera: Dactylopiidae), in the Brazilian Semiarid Region. The Coleopterists Bulletin 72 (3): 562-564, DOI: 10.1649/0010-065X-72.3.562, URL: http://dx.doi.org/10.1649/0010-065x-72.3.562

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References

  • The false carmine cochineal, Dactylopius opuntiae (Cockerell) (Hemiptera: Dactylopiidae), has become a severe pest of the cactus Opuntia ficus-indica (L.) Mill (Cactaceae) in the Brazilian semiarid region over the past two decades. The first outbreak of this hemipteran occurred in 2001 in Sertania County, Pernambuco (Lopes 2007). Since then, the pest has been found in nearly the entire region where O. ficus-indica is grown, causing an estimated loss of one-fifth of its cultivated area, which was once the largest in the world (ca. 500,000 ha; Santos et al. 2006; Lopes 2007). The cactus is the main forage for cattle farming among the small producers from the semiarid region (Duque 1964).
  • Several actions have been proposed to control D. opuntiae, but no progress has ever been reported in the literature.Recommendations for chemical control have been proposed (Brito et al. 2008), but the scarcity of water in the region prevents this measure from being a viable option (Instituto Nacional de Pesquisas da Amazonia-INPA, staff personal communication), in addition to other barriers such as cost and contamination of fresh forage (Torres and Giorgi 2018).
  • At least two natural enemies of D. opuntiae from Mexico (the natural origin of the false carmine cochineal), Chilocorus cacti (Linnaeus) and Hyperaspis trifurcata Schaefer, were considered for biological control purposes (Lima 2007), but no introductions occurred. Originally brought for other purposes, the predatory efficiency of the Australian Cryptolaemus montrouzieri Mulsant on D. opuntiae was evaluated in the laboratory (Gama et al. 2016). Despite high rates of prey consumption, the beetle failed to establish a population in the field (Torres and Giorgi 2018).
  • Surprisingly, little is known about the semiarid native predators of D. opuntia. Lopes (2007) reported Cycloneda sanguinea (Linnaeus) and a species of Scymnus Kugelann as natural enemies of the false carmine cochineal. However, C. sanguinea is a wellknown aphid feeder and is probably not the species the author intended to report, as the coccinellid featured in the publication (fig. 10) is clearly Zagreus bimaculosus Mulsant.
  • A more comprehensive survey was carried out by Lima et al. (2011), who surveyed 15 counties in Pernambuco and reported the occurrence of three coccinellid predators associated with D. opuntia: Z. bimaculosus, Brumoides foudrasii (Mulsant) (mistakenly identified as a species of Exochomus Redtenbacher), and Coccidophilus citricola Brethes. To the best of our knowledge, Z. bimaculosus is the only coccinellid from this list in which a predaceous habit on D. opuntiae has been confirmed in the laboratory (Castro et al. 2010). Other species have either not been tested, such as C. citricola and Scymnus sp., or, in the case of B. foudrasii, have proven unable to survive on the cochineal under laboratory conditions (Lima et al. 2017).
  • To further investigate the native fauna of coccinellids associated with O. ficus-indica infested with D. opuntiae, we conducted a survey in the Pernambuco semiarid region. The survey was carried out during the dry season of 2010 and 2011, when the highest levels of cochineal infestation are observed, and included the following counties: Surubim, Arcoverde, Serra Talhada, Sertania, Afogados da Ingazeira, Petrolina, Dormentes, and Juta´i. Here we report, for the first time, the association of Prodilis hattie Gordon and Hanley with D. opuntiae. This is the first record of predation by the beetle on D. opuntiae, not only for the genus but also for Cephaloscymnini. This coccinellid was observed in abundance on heavy cochineal-infested prickly pear fields in the counties of Arcoverde, Sertania, Dormentes, and Juta´i.
  • We also encountered a second coccinellid species that had not been recorded in previous surveys: Tenuisvalvae notata (Mulsant), a well-known mealybug (Pseudoccocidae) predator (Dreyer et al. 1997) that was consistently observed in prickly pear plantations infested with D. opuntiae over the course of our study. Despite the high densities observed in the field, all larvae died in the laboratory during the first instar, and adult females did not reproduce when fed exclusively D. opuntiae (Barbosa et al. 2014).
  • The Cephaloscymnini were recently revised by Gordon and Hanley (2017) to include four genera, two of them (Prodilis Mulsant and Neoparia Gorham) with a South American distribution. Prodilis are Cephaloscymnini with a long pronotum, a long prosternal process, and the lack of a setiferous pit. Comprising around 71 species (21 recorded from Brazil), Prodilis is the largest genus in the tribe. Prodilis hattie is one of the few Brazilian species with two rounded, pale maculae on the otherwise black elytron (Fig. 1A). This species is very similar to Prodilis bipunctata (Weise), but the elytral maculae of P. hattie are larger and the pronotum is laterally pale. The male genitalia provide the most secure basis for differentiating these two species.
  • Almost nothing is known about the biology of the tribe. According to Gordon and Hanley (2017), even the few existing prey associations for Cephaloscymnini (Pseudococcidae, Phenococcus gossypii Townsend and Cockerell, and the "bamboo scale") come from label data and should be interpreted as accidental observations. However, we collected larvae and pupae of this tribe in association with D. opuntiae. Although we will formally describe 564 P. hattie larvae and pupae elsewhere, we include pesticidas no controle da cochonilha-do-carmim na images of them (Fig. 1B and C) to highlight that, Para´iba. Revista de Biologia e Ciencias de Terra 8: unlike previous reports, the association of P. hattie 1-5. with D. opuntiae in the Northeast region of Brazil is Castro, R. M., R. Barros, B. A. J. Paranhos, M. H. A.
  • Gama. 2010. Biologia da joaninha native Zagreus able to successfully complete its life cycle by bimaculosus Mulsant (Coleoptera: Coccinellidae) preying upon D. opuntiae. alimentada com cochonilha do carmim Dactylopius To test the acceptability of D. opuntiae to P. opuntiae. XXIII Congresso Brasileiro de Entomohattie, a colony with approximately 50 individuals logia, Brazil. from Dormentes (S´itio Boa Vista: 09°04ʹ15ʹʹ S, Dreyer, B. S., P. Neuenschwander, J. Baumgartner, and 40°19ʹ5.4ʹʹ W) was established in the Insect Biology S. Dorn. 1997. Trophic influences on survival, Lab of the Universidade Federal Rural de Pernam- development and reproduction of Hyperaspis buco. The coccinellid colony was maintained in notata (Col., Coccinellidae). Journal of Applied
  • Duque, J. G. 1964. O Nordeste e as lavouras xerofilas. in height by 40 cm in length) with lateral openings Banco do Nordeste do Brasil, Fortaleza, Brazil. covered with nylon of 2 mm mesh to allow air flow. Gama, F. C., R. S. Coelho, J. O. Santos, A. J. S. Santos, Infested cladodes of O. ficus-indica were regularly and B. A. J. Paranhos. 2016. Capacidade de collected from the closest commercial growing areas predac~ ao da joaninha Cryptolaemus montrouzieri for the cochineal rearing. The coccinellid and the Mulsant (Coleoptera: Coccinellidae) sobre Dactylocochineal colonies were maintained at 25 ± 2° C, pius opuntiae Cockerell (Hemiptera: Dactylopiidae). with a 12-h photoperiod and 60 ± 10% relative Anais do XXVI Congresso Brasileiro de Entomohumidity. Although no experiments were carried out logia; IX Congresso Latino-Americano de Ento-
  • Gordon, R. D., and G. A. Hanley. 2017. South American solely on D. opuntiae for a few generations, providing Coccinellidae (Coleoptera), Part XVII: Systematic convincing evidence that the false carmine cochineal revision of Western Hemisphere Cephaloscymnini is a suitable source of food for P. hattie. (Coccinellinae) with description of a cryptic new Our findings suggest that P. hattie might be a genus and species of Coccidulini (Coccinellinae). voracious predator of the false carmine cochineal, Insecta Mundi 601: 1-158. which opens up a new possibility for biological Lima, E. 2007. Pesquisadores buscam inimigos naturais da control of this pest. Future research should in- cochonilha-da-palma-forrageira. www.embrapa.br/ vestigate the specificity of this predator as well as its busca-de-noticias/-/noticia/18015076/pesquisadores-
  • forrageira (accessed 12 January 2017). broader surveys on Brazilian cactus fields, which Lima, M. S., J. W. S. Melo, and R. Barros. 2017. may reveal other useful natural enemies of D. Alternative food sources for the ladybird Brumoides opuntiae, thus helping with the sustainability of foudrasii (Mulsant) (Coleoptera: Coccinellidae). cattle farming in the semiarid region. Brazilian Journal of Biology. DOI: 10.1007/
  • Ferreira, L. D. Silva, and B. A. J. Paranhos. We are grateful to Dr. Christine Elise Pulz, Dr. 2011. Predadores associados a Dactylopius opuntiae Guillermo Gonzalez, Dr. Natalia Vandenberg, Dr. (Hemiptera: Dactylopiidae) em palma forrageira no
  • Entomologia 36: 51-54. their valuable suggestions, comments, and correc- Lopes, E. B. 2007. Palma Forrageira: Cultivo, Uso atual e tions. This research was financially supported by Perspectivas de Utilizacao no Semi- arido Nor- "Coordenac~ ao de Aperfeicoamento de Pessoal de destino. EMEPA/FAEPA, Joao Pessoa, Brazil. N´ivel Superior" (CAPES Foundation, Brazil, PNPD Santos, D. C., I. Farias, M. A. Lira, M. V. F. Santos, G. 2116/2009) and "Fundac~ ao de Amparo a Ciencia e P. Arruda, R. S. Coelho, F. M. Dias, and J. N. Tecnologia do Estado de Pernambuco (FACEPE)". Melo. 2006. Manejo e Utilizac~ ao da Palma For-
  • REFERENCES CITED Torres, J. B., and J. A. Giorgi. 2018. Management of the Barbosa, P. R. R., M. D. Oliveira, J. A. Giorgi, C. S. A. false carmine cochineal Dactylopius opuntiae
  • Silva-Torres, and J. B. Torres. 2014. Predatory (Cockerell): Perspective from Pernambuco state,
  • conditions. Florida Entomologist 97: 1026-1034. Brito, C. A., E. B. Lopes, I. C. Albuquerque, and J. L. (Received 27 September 2017; accepted 17 July 2018.
  • Batista. 2008. Avaliac~ ao de produtos alternativos e Publication date 20 September 2018.)