First record of Eudorylas schreiteri (Shannon) (Diptera: Pipunculidae) as a parasitoid of the corn leafhopper (Hemiptera: Cicadellidae) in Argentina, with a table of pipunculid-host associations in the neotropical region

Primeiro registro de Eudorylas schreiteri (Shannon) (Diptera: Pipunculidae) como parasitóide da cigarrinha do milho (Hemiptera: Cicadellidae) na Argentina, e uma tabela dos hospedeiros de pipunculídeos na região neotropical

SCIENTIFIC NOTE

First record of Eudorylas schreiteri (Shannon) (Diptera: Pipunculidae) as a parasitoid of the corn leafhopper (Hemiptera: Cicadellidae) in Argentina, with a table of pipunculid-host associations in the neotropical region

Primeiro registro de Eudorylas schreiteri (Shannon) (Diptera: Pipunculidae) como parasitóide da cigarrinha do milho (Hemiptera: Cicadellidae) na Argentina, e uma tabela dos hospedeiros de pipunculídeos na região neotropical

Eduardo G Virla^I; Gustavo Moya-Raygoza^II; José A Rafael^III

^IPROIMI-Biotecnología, Div. Control Biológico, Av. Belgrano y Pje. Caseros (T4001 MVB), San Miguel de Tucumán, Tucumán, Argentina; [e-mail]

^IIDepto. de Botánica y Zoología, C.U.C.B.A., Univ. de Guadalajara, km 15.5 carretera Guadalajara-Nogales, Ap. postal 139, C. postal 45110, Las Agujas, Zapopan, Jalisco, Mexico; [e-mail]

^IIIINPA, Instituto de Pesquisa da Amazônia - INPA, C. postal 478, 69011-970, Manaus, SAM, Brazil; [e-mail]

ABSTRACT

The big-headed fly Eudorylas schreiteri (Shannon) is recorded for the first time as an endoparasitoid of the corn leafhopper Dalbulus maidis (DeLong & Wolcott) in Northern Argentina. A table of known Neotropical pipunculid-host associations is presented.

Key words: Natural enemy, disease vector, Dalbulus maidis

RESUMO

Eudorylas schreiteri (Shannon) é registrada pela primeira vez como endoparasitóide da cigarrinha do milho Dalbulus maidis (DeLong & Wolcott) no norte da Argentina. Uma tabela das espécies neotropicais de pipunculídeos com hospedeiros conhecidos é apresentada.

Palavras-chave: Inimigo natural, vetor, Dalbulus maidis

The corn leafhopper Dalbulus maidis (DeLong & Wolcott) is the most common leafhopper pest on maize in the tropics (Nault 1990). D. maidis is important because efficiently vectors three plant pathogens; the corn stunt spiroplasma, Spiroplasma kunkelii, the maize bushy stunt phytoplasma and the maize rayado fino virus (Nault 1980, Oliveira et al 1998, Virla et al 2004).

Eggs of the corn leafhopper are parasitized by wasps (Trichogrammatidae and Mimaridae) (Gladstone et al 1994, Luft Albarracin et al 2006), whereas nymphs and adults are parasitized by strepsipterans (Halictophagidae), wasps (Dryinidae) and flies (Pipunculidae) (Vega et al 1991, Kathirithamby & Moya-Raygoza 2000, Virla & Olmi 2007). Most of the corn leafhopper parasitoids have been collected in Mesoamerica and little is known about their natural enemies in South America.

The Pipunculidae (big-headed flies) have always been considered exclusively as endoparasitoids of Auchenorrhyncha (Hemiptera), including Cicadellidae, Delphacidae, Cercopidae, Cixiidae, Flatidae, Fulgoridae and Membracidae. They attack host nymphs and adults in all groups except Cercopidae, in which they attack only the adults (Waloff & Jervis 1987). This specialized behavior has been consistently recorded for species throughout the subfamilies Chalarinae and Pipunculinae (Skevington 2005). However a recent discovery by Koenig & Young (2007) showed that Nephrocerus Zetterstedt (Nephrocerinae) was reared from large adults of crane flies (Tipulidae). An overview of pipunculid-host associations was published by Skevington & Marshall (1997), but very little information is available concerning the hosts of tropical species.

In northern Argentina nymphs and adults were sampled by sweeping with a standard entomological net. Samples were collected from December 2005 to February 2007 on corn fields from the sites "El Manantial" (26°49'50.2''S, 65°16'59.4''W, elevation 495 m), San Miguel de Tucumán (26º48'35.7"S, 65º16'25.3"O, 470 m) and Los Nogales (26º42'27.5"S, 65º13'3.9"O, 585 m), all in Tucumán Province.

The above method allowed sampling individuals of the corn leafhopper parasitized by Pipunculidae larva, as evidenced by the voluminous abdomen. These specimens were isolated in glass tubes (10 x 2 cm), with a piece of fresh corn leaf, which was daily replaced, and tapped with a water-wetted cotton pad.

Emerged adults were identified as Eudorylas schreiteri (Shannon). Therefore, we report for the first time the pipunculid E. schreiteri attacking D. maidis in Argentina. Data on host range (Table 1) are available for six species of Pipunculidae that occurs in the tropics.

The species changed the genus several times as below.

Eudorylas schreiteri (Shannon)

Pipunculus schreiteri Shannon 1927: 37.

Eudorylas schreiteri (Shannon) in Aczél (1948): 25.

Pipunculus (Eudorylas) schreiteri (Shannon) in Hardy (1963a): 223.

Metadorylas schreiteri (Shannon) in Rafael (1987): 37.

Eudorylas schreiteri (Shannon) in Skevington & Yeates (2001): 439.

Eudorylas schreiteri was described from Raco (Tucumán province, Argentina), but it is known to Argentina (Entre Rios, Salta, Tucumán, and Santiago del Estero provinces) and Brazil (Rio de Janeiro, São Paulo and Paraná states) (Rafael 1990). Until this contribution, the hosts for this species were unknown.

Material examined. S.M. de (Tucumán), xii/2005, Virla leg. One ♂; El Manantial (Tucumán), 13/xii/2006, Virla leg., one ♂ one ♀; El Manantial (Tucumán), 2-5/i/2007, Virla leg., one ♂; Los Nogales (Tucumán), 15/i/2007, Virla leg., two ♂♂ two ♀♀; Los Nogales (Tucumán), 10/ii/2007, Virla leg. one ♂one ♀.

Dried voucher specimens of E. schreiteri resulting from this study were deposited in the collection of the Instituto Nacional de Pesquisas da Amazônia (INPA) at Manaus, Brazil and Fundación e Instituto Miguel Lillo (IMLA) at San Miguel de Tucumán, Argentina.

It is for the first time that the corn leafhopper pest Dalbulus maidis is recorded here as a natural host for E. schreiteri, and the third pipunculid parasitizing it. E. subopacus (Loew) and E. spinosus (Hardy) were previously recorded attacking the corn leafhopper in central Mexico (Vega et al1991, Moya-Raygoza et al 2004, Moya-Raygoza 2007).

Taking into account the importance of the diseases the corn leafhopper vectors in the Americas, we point out to the need for a proper evaluation of E. schreiteri as a potential biocontrol agent against this leafhopper pest, as the highest parasitism of Dalbulus elimatus (Ball) by E. subopacus was 57% in central Mexico, whereas on D. maidis was 20% (Moya-Raygoza 2007).

Received 04/X/07. Accepted 19/XII/08.

Edited by Fernando Luis Cônsoli - ESALQ/USP

References

• Aczél M (1948) Grundlagen einer Monographie der Dorialiden (Diptera). Dorylaiden-Studien VI. Acta Zool Lilloana 6: 5-168.
• Gladstone S M, Lana A de la, Rios R, López L (1994) Eggs parasitoids of the corn leafhopper, Dalbulus maidis (Delong and Wolcot) (Homoptera: Cicadellidae) in Nicaragua maize. Proc Entomol Soc Wash 96: 143-146.
• Hardy D E (1963a) The Pipunculidae of Argentina. Acta Zool Lilloana 19: 187-241
• Hardy D E (1963b) Studies in Pipunculidae (Diptera) of Colombia. Proc Hawaii Entomol Soc 18: 259-266.
• Hardy D E (1964) Insects of Hawaii (Dipt. Brachy. 2 - Cyclorrh.). Univ Hawaii Press, Honolulu, 458p.
• Kathirithamby J, Moya-Raygoza G (2000) Halictophagus naulti sp. n. (Strepsiptera: Halictophagidae), a new species parasitic in the corn leafhopper (Homoptera: Cicadellidae) from Mexico. Ann Entomol Soc Amer 93: 1039-44.
• Koenig D P, Young C W (2007) First observation of parasitic relations between big-headed flies, Nephrocerus Zetterstedt (Diptera: Pipunculidae) and crane flies, Tipula Linnaeus (Diptera: Tipulidae: Tipulinae), with larval and puparial descriptions for the genus Nephrocerus Proc Entomol Soc Wash 109: 52-65.
• Luft Albarracin E, Virla E, Triapitsyn S (2006) A new host record for the egg parasitoid Anagrus nigriventris (Hymenoptera: Mymaridae) of the corn leafhopper, Dalbulus maidis (Hemiptera: Cicadellidae). Fla Entomol 89: 284-285.
• Moya-Raygoza G (2007) Native parasitoids of Dalbulus elimatus and Dalbulus maidis (Hemiptera: Cicadellidae) in winter crops of central Mexico. Can Entomol 139: 722-727.
• Moya-Raygoza G, Kathirithamby J, Larsen K J (2004) Dry season parasitoids of adult corn leafhoppers (Hemiptera: Cicadellidae) on irrigated maize in Mexico. Can Entomol 136: 119-127.
• Nault L (1980) Maize bushy stunt and corn stunt: a comparison of disease symptoms, pathogen host ranges, and vectors. Phytopathology 70: 659-662.
• Nault L R (1990) Evolution of an insect pest: maize and the corn leafhopper, a case study. Maydica 35: 165-175.
• Oliveira E, Waquil J, Fernandes F, Paiva E, Resende R, Kitajima E (1998) "Enfezamento pálido" e "enfezamento vermelho" na cultura do milho no Brasil central. Fitopatol Bras 23: 45-47.
• Pierce D H (1972) Scaphytopius nitridus: parasitization by Tomosvaryella appendipes Environ Entomol 1: 796-797.
• Rafael J A (1987) Two new genera of Pipunculidae (Diptera) from the New World: Metadorylas, gen. n. and Elmohardyia, gen. n., with new synonyms, designation of lectotypes and revalidation of a species. Rev Bras Entomol 31: 35-39.
• Rafael J A (1990) As espécies neotropicais de Metadorylas Rafael (Diptera, Pipunculidae). Bol Mus Para Emilio Goeldi Ser Zool 6: 127-164.
• Shannon R C (1927) Some new Diptera from Argentina. Rev Soc Entomol Argent 2: 31-42.
• Skevington J H (2005) Revision of Nearctic Nephrocerus Zetterstedt (Diptera: Pipunculidae). Zootaxa 977: 1-36.
• Skevington J H, Marshall S A (1997) First record of a big-headed fly, Eudorylas alternatus (Cresson) (Diptera: Pipunculidae), reared from the subfamily Cicadellinae (Homoptera: Cicadellidae), with an overview of the pipunculid-host associations in the Nearctic region. Can Entomol 129: 387-398.
• Skevington J H, Yeates D K (2001) Phylogenetic classification of Eudorylini (Diptera, Pipunculidae). Syst Entomol 26: 421-452.
• Vega F, Barbosa P, Perez Panduro A (1991) Eudorylas (Metadorylas) sp. (Diptera: Pipunculidae): a previously unreported parasitoid of Dalbulus maidis (De Long & Wolcott) and Dalbulus elimatus (Ball.) (Homoptera: Cicadellidae). Can Entomol 123: 241-2.
• Virla E G, Rafael J A (1996) Datos bionómicos preliminares y descripción de la hembra de Cephalops penepauculus (Hardy) (Diptera: Pipunculidae) un parasitoide de Delphacidae (Homoptera: Auchenorrhyncha) en Argentina. CIRPON, Rev Inv 10: 33-36.
• Virla E G, Díaz C, Carpane P, Laguna I, Ramallo J, Gómez L, Giménez Pecci M (2004) Estimación preliminar de la disminución en la producción de maíz causada por el "Corn Stunt Spiroplasma" (CSS) en Tucumán, Argentina. Bol San Veg 30: 257-267.
• Virla E G, Olmi M (2007) Dryinid (Hymenoptera: Chrysidoidea) parasitoids of the corn leafhopper, Dalbulus maidis (Delong & Wolcott) (Hemiptera: Cicadellidae), in Argentina, with description of the male of Gonatopus moyaraygozai Olmi. Interciencia 32: 847-849.
• Waloff N, Jervis M A (1987) Communities of parasitoids associated with leafhoppers and planthoppers in Europe. Adv Ecol Res 17: 289-402.

Publication Dates

• Publication in this collection
  27 Mar 2009
• Date of issue
  Feb 2009

History

• Accepted
  19 Dec 2008
• Received
  04 Oct 2007