Nota científica

Egg parasitoids of the leafhopper Rhabdotalebra flava Catalano (Hemiptera: Cicadellidae) on Handroanthus in Argentina

Parasitoides oófilos de la chicharrita Rhabdotalebra flava Catalano (Hemiptera: Cicadellidae) sobre Handroanthus en Argentina

 

AMIUNE, María J.¹, LUFT ALBARRACIN, Érica² & CATALANO, María I.³

¹ Fundación Miguel Lillo, Instituto de Entomología. San Miguel de Tucumán, Argentina.
² PROIMI-Biotecnología (CONICET), División Control Biológico. San Miguel de Tucumán, Argentina. *E-mail: erluft@hotmail.com
³ Centro de Bioinvestigaciones (UNNOBA - CICBA) Universidad Nacional del Noroeste de Buenos Aires. Pergamino, Argentina.

Received 16 - III - 2018 | Accepted 01 - VI - 2018 | Published 28 - VI - 2018 https://doi.org/10.25085/rsea.770208

---

ABSTRACT. The aim of this study is to report egg parasitoids associated to Rhabdotalebra fava Catalano (Hemiptera: Cicadellidae), in Tucumán province, Argentina. During the summer, Handroanthus impetiginosus (Mart. ex DC.) Mattos (Bignoniaceae) leaves with eggs of Rhabdotalebra fava were collected. T wo species of parasitoids, Anagrus atomus (L.) (Mymaridae) and Epoligosita mexicana (Viggiani) (Trichogrammatidae) were identifed as new host-parasitoid associations.

KEYWORDS. Anagrus. Epoligosita. Leafhoppers. Mymaridae.

RESUMEN. Se citan parasitoides de huevos de Rhabdotalebra fava Catalano (Hemiptera: Cicadellidae) en la provincia de Tucumán, Argentina. Los huevos fueron colectados durante el verano en hojas de Handroanthus impetiginosus (Mart. ex DC.) Mattos (Bignoniaceae). Se identifcaron dos especies: Anagrus atomus (L.) (Mymaridae) y Epoligosita mexicana (Viggiani) (Trichogrammatidae), siendo estas nuevas asociaciones entre hospedador y parasitoide.

PALABRAS CLAVE. Anagrus. Chicharritas. Epoligosita. Mymaridae.

---

 

Cicadellidae, one of the most numerous families of Hemiptera, includes phytophagous insects known as leafhoppers. One of the most interesting aspects of this family is its phytosanitary importance, because its members transmit pathogens to many host plants, causing diseases (Nault & Ammar, 1989). Typhlocybinae is the second most important subfamily in terms of size, with about 5,000 described species known worldwide (McKamey, 2002). These species are agricultural pests because of the mechanical damage they cause to the leaves (called "stippling" and "hopperburn") in crops such as bean, potato, apple tree, and grapevine, resulting in signifcant economic losses (Backus et al., 2005). Species in this subfamily are also vectors of pathogens such as phytoplasma 16Sr III (X-disease), known to be the cause of the garlic decline disease, having a great impact in Argentina (Catalano, 2011).

Rhabdotalebra fava Catalano is a micro leafhopper of yellowish color with dark brown spots. This species lives on leaves of Handroanthus pulcherrimus (Sandw.) Grose and H. impetiginosus (Mart. ex DC.) Mattos (Bignoniaceae) in Tucumán Province. Catalano et al. (2010) have observed damage caused by R. fava on top of leaves of the plant hosts. Both adults and immature stages live in the abaxial surface of leaves causing little yellowish dots until they turn yellowish to dark brown (Catalano et al., 2010).

The parasitoids are antagonists that can be divided into two guilds: those attacking eggs, and those affecting nymphs and adults (Cronin & Strong, 1993). Eggs of several leafhoppers are commonly parasitized by members of Mymaridae and Trichogrammatidae (Hymenoptera: Chalcidoidea), as well as by some species of other Chalcidoidea such as Aphelinidae and Eulophidae. According to Freytag (1985), many of these species can reach attack levels close to 100%. Denno & Roderick (1990) have proven that mortality caused by these egg parasitoids constitutes a key factor in the population dynamics of some species of leafhoppers.

In Argentina, researches about the host-parasitoid associations of Typhlocybinae have been poorly developed. There are some studies dealing with parasitoids of nymphs and adults, attacking species of Empoasca Walsh, that belong to the family Dryinidae (Hymenoptera) (Paradell, 1995; Guglielmino & Olmi, 1997, 2006; Virla & Olmi, 1998). Publications about parasitoids that affect eggs of Typhlocybinae in Argentina seem to be absent. The aim of this contribution is to report egg parasitoids associated to R. fava.

Leaves of H. impetiginosus were collected during summer (November to March), in San Miguel de Tucumán, Tucumán, Argentina (26º 49' 47'' S; 65° 13' 20'' W). Twenty weekly samples took place, with a total of 60 leaves of H. impetiginosus per collection. At the laboratory, leaves with eggs were transferred to Petri dishes containing wet tissue paper on the bottom and covered with polyethylene flm to avoid desiccation as well as to contain the emerging nymphs and/or wasps (Fig. 1 A, B). The dishes were checked daily to ensure leaf quality until the emergence of all the adult wasps in case the eggs were parasitized.

The parasitoid specimens were preserved in 70% ethanol and later slide-mounted in Hoyer's medium following the traditional practices (Luft Albarracin et al., 2017). All emerging parasitoids were identifed using specifc keys (Pinto, 2006; Triapitsyn, 2015) and by comparison with the original description of the species (Pinto & Viggiani, 1987). Identifcation of leafhoppers was made using specifc keys (Young, 1952; Catalano et al., 2010). Voucher specimens were deposited at the entomological collection of the Instituto Fundación Miguel Lillo, San Miguel de Tucumán, Tucumán, Argentina (IMLA).

The females of R. fava deposit eggs isolated on H. impetiginosus leaves, and the eggs are completely covered by plant tissue. The parasitized eggs of R. fava were easily recognized by presenting a dark coloration in contrast to unparasitized eggs, with transparent to whitish coloration. A single wasp emerges in parasitized eggs, through a circular hole made close to the apical end of its host egg. Ten specimens of parasitoids emerged from the collected eggs. There were two parasitoids identifed: one female and two males of Anagrus atomus (L.) (Mymaridae) (Fig. 1 C, D); plus four females and three males of Epoligosita mexicana (Viggiani) (Trichogrammatidae) (Fig. 1 E, F).

Anagrus atomus is a member of the "atomus" species group. This species is characterized by F3 without sensory ridges, F4-F5 with 1 sensory ridges; F6 with two sensory ridges; F2 and F3 together much longer than F6, at least by almost 1/2 of their combined length; bare area on forewing disc short; forewing with longest marginal setae much longer than maximum fore wing width; 3 or 4 rows of microtrichia present anterior to bare area (Chiappini, 1987, 1989). Anagrus atomus is widely distributed in several countries of the Northern hemisphere. It is a common, solitary egg parasitoid of several Cicadellidae (mainly T yphlocybinae) and some Delphacidae (Triapitsyn, 2015).

Material examined. Argentina, Tucumán, San Miguel de T ucumán, emerged from an egg of R. fava , M. J. Amiune col., 6.iii.2016, 1 female and 1 male, 28.iii.2016, 1 male.

The other parasitoid is E. mexicana, which is characterized by presenting the body yellow; eyes and ocelli blackish; tips of mandibles yellowish brown; forewings with basal third and substigmal area infuscated; antenna with scape three times as long as wide; funicle segment as long as wide; club not clearly divided in two segments, twice the length of pedicel, club fve times as long as the funicle segment; fore wing 3.0 as long as wide; ovipositor occurring about half length of gaster, about as long as hind tibia (Pinto & Viggiani, 1987). Epoligosita Girault is a widely distributed genus which contains 22 species (Pinto, 2006). Only E. mexicana occurs in the New World. In Argentina, this species was reported in Northern provinces (Chaco, Formosa, and Salta) (Pinto, 2006; Santos et al., 2009). At the moment, the known hosts associated to E. mexicana were two Typhlocybinae species, Dikrella cockerelli (Gillette) and Erythroneura ziczac Walsh in Mexico (Pinto & Viggiani, 1987), and Leptopharsa heveae Drake & Poor (Hemiptera: Tingidae) eggs in Brazil (Santos et al., 2009).

Material examined. Argentina, Tucumán, San Miguel de T ucumán, emerged from an egg of R. fava , M. J. Amiune col., 13.i.2016, 1 male, 19.i.2016, 1 female, 2 males, 28.iii.2016, 3 females.

This is the frst time that the parasitoids A. atomus and E. mexicana are reported in Argentina associated to eggs of R. fava. Altieri & Nicholls (2000) have observed that conserving natural enemies populations (i.e. Trichogrammatidae) could lead to a long-term regulation of pest species, under the assumption of an appropriate cultural agroecosystem management; this procedure would guarantee an optimal environment to increase both abundance and effciency of parasitoid and predators. Under these conditions, biological control can become a self-perpetuating strategy, with low cost of control and a minimum (or non-existent) environmental impact (Flint & Roberts, 1988). There are many reports of Anagrus Haliday species acting against

Typlocybinae leafhoppers, such as Erytroneura spp., which are important pests of grapevine crops at Northwestern USA (Williams & Martinson, 2000; Prischmann et al., 2007).

Fig. 1. A. Unparasitized eggs of Rhabdotalebra flava on Handroanthus impetiginosus. B. Parasitized eggs of Rhabdotalebra flava on Handroanthus impetiginosus. C. Anagrus atomus, female. D. Anagrus atomus, male. E. Epoligosita mexicana, female. F. Epoligosita mexicana, male.

 

In this way, future studies could be carried out, in which H. impetiginosus plants play a role of insect beneft reservoir with the possibility of being used as "curtains" or "border plants", as well as "vegetal corridors". These techniques could stimulate the movement of parasitoids to crops of high economic importance for Argentina.

The authors acknowledge Fundación Miguel Lillo (FML) and Planta Piloto de Procesos Industriales Microbiologicos (PROIMI) for giving us space and materials to develop this article. We are also grateful to Hugo Pablo Pereyra for his contribution in the image edition and to reviewers for thoughtful comments on the manuscript.

LITERATURE CITED

Altieri, M., & Nicholls, C. (2000) Agroecología T eoría y práctica para una agricultura sustentable.Programa de las Naciones Unidas para el Medio Ambiente, Red de Formación Ambiental para América Latina y el Caribe, Ciudad de México.         [ Links ]

Backus, E., Serrano, M., & Ranger, C. (2005) Mechanisms of hopperburn: an overview of insect taxonomy, behavior, and physiology. Annual Review of Entomology, 50, 125-151.         [ Links ]

Catalano, M.I. (2011) Cicadélidos vectores de ftoplasmas a cultivos de importancia económica en la Argentina sistemáticaybioecología (Insecta-Auchenorrhyncha-Cicadellidae). Tesis doctoral. Universidad Nacional de La Plata, Buenos Aires, Argentina.         [ Links ]

Catalano, M.I., Paradell, S.L., & Marino de Remes Lenicov, A.M. (2010) Revision of the genus Rhabdotalebra Young (Hemiptera: Cicadellidae: Typhlocybinae: Alebrini) and description of two new species from Argentina. Zootaxa, 2601, 53-60.         [ Links ]

Chiappini, E. (1987) Ricerche Sulla variabilità di Anagrus atomus (L.) (Hymenoptera Mymaridae) e di una specie affne presente sul rovo. Bollettino di Zoologia Agrariaedi Bachicoltura, Serie II, 19, 71-97.         [ Links ]

Chiappini, E. (1989) Review of the European species of the genus Anagrus Haliday (Hymenoptera Chalcidoidea). Bollettino di Zoologia Agrariaedi Bachicoltura, Serie II, 21, 85-119.         [ Links ]

Cronin, J.T., & Strong, D.R. (1993) Superparasitism and mutual interference in the egg parasitoid Anagrus delicatus (Hymenoptera: Mymaridae). Ecological Entomology, 18, 293-302.

Denno, R.F., & Roderick, G.K. (1990) Population Biology of Planthoppers. Annual Review of Entomology, 35, 489-520.

Flint, M.L., & Roberts, P.A. (1988) Using crop diversity to manage pest problems: some California examples. American Journal of Agricultural Economics, 3, 164-167.

Freytag, P.H. (1985) The insect parasites of leafhoppers, and related groups. The leafhoppers and planthoppers (ed. Nault, L., & Rodriguez, J.), Wiley, New York. pp. 423-467..

Guglielmino, A., & Olmi, M. (1997) A host-parasite catalog of world Dryinidae (Hymenoptera: Chrysidoidea). Contributions on Entomology International, 2, 165-298.

Guglielmino, A., & Olmi, M. (2006) A host-parasite catalog of world Dryinidae (Hymenoptera: Chrysidoidea): frst supplement. Zootaxa, 1139, 35-62.

Luft Albarracin, E., Triapitsyn, S.V., & Virla, E.G. (2017) Egg parasitoid complex of the corn leafhopper, Dalbulus maidis (DeLong) (Hemiptera: Cicadellidae), in Argentina. Neotropical Entomology, 46, 666-677.

McKamey, S.H. (2002) Leafhoppers of the world database: progress report. In: 11th. International Auchenorrhyncha Congress, Abstracts book, 2002, Potsdam/Berlin. Pp. 85.

Nault, L., & Ammar, E. (1989) Leafhoppers and planthoppers transmission of plant viruses. Annual Review of Entomology, 34, 503-529.

Paradell, S.L. (1995) Estudio sistemático de los tifocibinos argentinos del género Empoasca (Homoptera: Cicadellidae). Revista de la Sociedad Entomológica Argentina, 54, 113-153.

Pinto, J.D. (2006) A review of the new world genera of Trichogrammatidae (Hymenoptera).Journal of Hymenoptera Research, 15, 38-163.

Pinto, J.D., & Viggiani, G. (1987) Two new Trichogrammatidae (Hymenoptera) from North America: Ittysella laguneraPinto e Viggiani (n. gen., n. sp.) and Epoligosita mexicana Viggiani (n. sp.). Pan-Pacifc Entomologist, 63, 374-376.

Prischmann, D.A., James, D.G., Storm, C.P., Wright, L.C., & Snyder, W.E. (2007) Identity, Abundance, and Phenology of Anagrusspp. (Hymenoptera: Mymaridae) and Leafhoppers (Homoptera: Cicadellidae) associated with grape, blackberry, and wild rose in Washington State. Annals of the Entomological Society of America, 100, 41-52.

Santos, R.S., Da Silva, R.B.Q., & Costa, V.A. (2009) Primeiro registro de Epoligosita mexicana Viggiani (Hymenoptera: Trichogrammatidae) no Brasil. Arquivos do Instituto Biológico, São Paulo, 76, 721-723.

Triapitsyn, S.V. (2015) Taxonomy of the genus AnagrusHaliday (Hymenoptera: Mymaridae) of the world: an annotated key to the described species, discussion of the remaining problems, and a checklist. Acta Zoologica Lilloana, 59, 3-50.

Virla, E.G., & Olmi, M. (1998) The Dryinidae of Argentina (Hymenoptera-Chrysidoidea). Acta Entomológica Chilena, 22, 19-35.

Williams, L., & Martinson, T. (2000) Colonization of New York vineyards by Anagrus spp. (Hymenoptera: Mymaridae): Overwintering biology, within-vineyard distribution of wasps, and parasitism of grape leafhopper, Erythroneura spp. (Homoptera: Cicadellidae), eggs. Biological Control, 18, 136-146.

Young, D.A. (1952) A reclassifcation of Western Hemisphere Typhlocybinae (Homoptera, Cicadellidae). Kansas University Science Bulletin, 35, 217.