ARTICLES RIA / Vol. 43 / N.º 3

Parasitoids of the bagworm , platensis (: Psychidae) in the calden forests of the of the province of La Pampa

BAUDINO, E.M.1; MARTÍNEZ, J.J.2; FERNÁNDEZ, L.1; GEIST, Y.H.1; GALLARDO, H.E.1; REIMER, A1.

ABSTRACT An important growth in the populations of Oiketicus platensis Berg is being observed since 2006 in native forests of Prosopis caldenia in La Pampa province. The aims of the present work are: 1) to survey larval parasitoids, and 2) to determine which species are most abundant in the study area. The study was carried out at three sites of La Pampa province located in the Espinal biogeographical province. Larvae were collected from November 2012 to March 2013. Seventeen parasitoid species were obtained. Fifteen species of parasitic wasps were identified belonging to the families Eulophidae, Encyrtidae, Eurytomidae, Eupelmidae, Torymidae, Chalcididae, Ichneumonidae, Braconidae and Bethylidae. Additionally, two parasitoid fly species were identified belonging to the family Tachinidae. Parasitoids appear one month after the birth of the larvae. Larval parasitism reached 17,6%, with a clear dominance of dipteran parasitoids (81,6%).

Keywords: Bagworm moth, Parasitoids, Diptera, Hymenoptera.

INTRODUCTION known associations between Oiketicus species and native trees or shrubs in Argentina. The bagworm moth, Oiketicus platensis Berg, is an of the order Lepidoptera, family Psychidae, subfamily Oiketici- In the American continent Oiketicus platensis is distribu- nae. This family includes around 1,000 species that have the ted south of 20 degrees south latitude. It is found in Ar- particularity of completing their life cycle inside the basket built gentina, Bolivia, Paraguay and Uruguay (Bentancourt and in the larval stage. Of the ten subfamilies, nine have species Scatoni, 1999). In Argentina it is widely distributed in the with apterous (neotenic) females (Rhainds et al., 2009). provinces of Buenos Aires, La Pampa, Rio Negro, Mendo- za, Entre Ríos, Santa Fe, Salta and Tucumán (Pastrana, Shrubs and trees of numerous plant species are attacked 2004). In La Pampa, Orrego Aravena (1983) finds it de- by Oiketicus species. In Argentina there are about 20 spe- foliating several species of exotic trees and shrubs, and cies of the genus widely distributed in almost all the terri- mentions Oiketicus geyeri (cigarette moth) on native plants tory, but the best known and abundant is O. platensis (Saini such as calden (Prosopis caldenia) and piquillín (Condalia et al., 1985). microphylla), which would indicate that at that time, while The larvae of several Oiketicus species feed on trees of there was O. platensis in the area, it was possibly not fee- native forests (Pastrana, 2004). Table 1 summarizes the ding on native plants.

1Facultad de Agronomía, Universidad Nacional de La Pampa, Ruta 35, km 334, 6300, Santa Rosa La Pampa. Correo electrónico: [email protected] 2CONICET, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de La Pampa, Uruguay 151, 6300, Santa Rosa, La Pampa. Correo electrónico: [email protected]

Received February 10, 2015 // Accepted May 23, 2017 // Published online November 29, 2017

Parasitoides del bicho canasto, Oiketicus platensis (Lepidoptera: Psychidae) en el caldenal pampeano December 2017, Argentina 5

Since 2006 there has been a significant increase in Oi- and Monetti, 2007). At present, in the province of La Pampa keticus platensis in the calden forests of the province of La there are 6 known parasitoid species from 5 genera obtai- Pampa. Surveys conducted by the General Directorate of ned from bagworm moth collected in the Parque Luro Pro- Statistics and Census [Dirección General de Estadísticas vincial Reserve [Reserva Provincial Parque Luro]. These y Censos] of the province included this species from the parasitoids belong to five families of of the Order year 2008 and account for its presence in different sites of Hymenoptera: Tetrastichus sp. (Eulophidae), Chirotica bru- La Pampa, with a considerable population increase. This chii (Brèthes) (Ichneumonidae), Conura sp.1 (Chalcididae), causes serious problems in the vegetation, not only for the Conura sp. 2 (Chalcididae), Perissocentrus sp. (Torymidae) species typical of the calden forest, but also for other culti- and Chelonus (Braconidae) (Risi et al., 2013). vated plants, such as alfalfa (Medicago sativa L.) pastures Due to the magnitude of the damages observed in recent bordering those forests. seasons and taking into account the extent of the forests, Oiketicus platensis is a species on which numerous spe- the complexity of the environment and the responsibility to cies of parasitoids develop (De Santis and Esquivel, 1966; conserve the ecosystem as much as possible of chemical De Santis, 1967; Blanchard and De Santis, 1975, De Santis pollutants, the aim of this work was to describe the com-

Species Host plant Site Reference Oiketicus platensis Acacia caven Buenos Aires Rizzo, 1971 Aloysia gratissima La Pampa Risi et al., 2013 Condalia microphylla La Pampa Risi et al., 2013 Jodina rhombifolia La Pampa Risi et al., 2013 Parkinsonia aculeata Buenos Aires Rizzo, 1971 Prosopis caldenia La Pampa Risi et al., 2013 Salix humboldtiana Río Negro Berg, 1875 Schinus fasciculatus var. arenicola La Pampa Risi et al., 2013 Oiketicus borsani Prosopis sp. Mendoza Pastrana, 2004 Oiketicus elegans Acacia albocorticata Köehler, 1931; 1939 Acacia caven Orfila, 940 Oiketicus geyeri Acacia aroma Hayward, 1969 Acacia caven Córdoba Pastrana, 2004 Cercidium praecox Catamarca Cates y Rhoades, 1977 Condalia microphylla La Pampa Orrego Aravena, 1983 Prosopis caldenia La Pampa Orrego Aravena, 1983 Prosopis flexuosa Catamarca Cates y Rhoades, 1977 Salix humboldtiana Buenos Aires Rizzo, 1971 Oiketicus ginocchionus Larrea divaricata Mendoza Mallea et al., 1979 Oiketicus horni Acacia sp. Salta Köehler, 1938 Prosopis sp. Salta Köehler, 1938 Oiketicus lizeri Acacia aroma Köehler, 1938 Acacia caven Köehler, 1938 Schinopsis sp. Köehler, 1938 Oiketicus oviformis Prosopis sp. Córdoba Orfila, 1940 Oiketicus westwoodi Anadenanthera colubrina var. cebil Argentina Köehler, 1931 Oiketicus sp. Schinopsis lorentzii Chaco Florentino and Diodato de Medina, 1991 Aspidosperma quebracho-blanco Chaco Florentino and Diodato de Medina, 1991 Prosopis nigra Chaco Florentino and Diodato de Medina, 1991

Table 1. Known associations between Oiketicus species and native trees and shrubs in Argentina.

BAUDINO, E.M.; MARTÍNEZ, J.J.; FERNÁNDEZ, L.; GEIST, Y.H.; GALLARDO, H.E.; REIMER, A. ARTICLES RIA / Vol. 43 / N.º 3

munity of parasitoids associated with the bagworm moth kets per plant, totaling 6000 baskets. Data was registered in natural ecosystems of La Pampa. The identification of in spreadsheets, and included date, georeferenced collec- parasitoids - quantitatively more relevant in their control - is tion site and species of the host plant. crucial to advance in future biological control programs. The collected material was transported to the Agricultu- ral Zoology Laboratory, Faculty of Agronomy, UNLPam. We only collected baskets that - by direct observation - appea- MATERIALS AND METHODS red to contain larvae or pupae (in this case they are com- Study area pletely closed). The field work was conducted in three sites: Rucanelo The samplings (12 in total) were performed from Nov- (36° 9’ S, 64° 51’ W), Parque Luro (S 36° 55’ S, 64° 16’ ember 2012 to March 2013 as follows: 2 in Parque Luro, 2 W) and Bajo Verde (36° 40 ‘S, 65° 9’ O), all in the Espinal in Bajo Verde and 8 in Rucanelo. The collected bags were Phytogeographic Province, Caldenal District. Rucanelo, placed individually in numbered and labeled plastic contai- with the largest number of samplings and observations, is ners (height: 10.5 cm, diameter: 7.5 cm). The top of the a private field, “Don Armando” located 110 km from the city containers were covered with plastic wrap and maintained Santa Rosa and 15 km from Rucanelo. in a breeding laboratory (T: 20-25 °C, RH: ~60%, natural light) to observe and record the hatching of adult males (the The extension of the field is 1100 ha, 500 of which are occu- only ones leave the case) or of the parasitoids. pied by calden forest, where the main productive activity is ex- tensive cattle breeding. The remaining area is destined to pas- We reviewed the material in the chamber every two days, tures. The Provincial Reserve Parque Luro is located on the and we recorded the observed changes under the corres- National Route Nº 35, km 292, District of Toay (35 km south ponding date. of Santa Rosa, La Pampa). It is a 7600 ha protected area of We recorded the emergence date of males, in the ca- calden. 1,600 ha are destined to tourism and recreation. ses where larvae became pupa and, later on, adult. If Bajo Verde is a silvopastoral productive unit of the Natio- the larvae were parasitized, we registered the date of nal University of La Pampa (UNLPam) and managed by the emergence of the parasitoid and the specimen was pre- Faculty of Agronomy. Its area is 1980 ha and is currently served for later identification. All emerged adult parasitoi- destined to extensive cattle breeding. ds were maintained with the original code of the basket from which they emerged to preserve the data of the host plant and the site. The parasitoids were preserved dry for Sampling and breeding in the laboratory identification. The sampling was performed every week or every two Quantitative data was collected from the 4000 baskets weeks, and consisted in the random selection of 5 sites in sampled in Rucanelo, since for logistics reasons it was the each location, 5 plants per site, and we collected 20 bas- only location sampled without interruptions.

Period of emergence of males 80

70

60

50

40

30

20

Number of individuals 10

0 . 3 . 21 May April . 8 April . 3 May April . 10 April . 17 April . 19 April . 24 March . 8 March . 12 March . 14 March . 18 March . 20 March . 26 Dates

Figure 1. Adult males emerged from larvae of Oiketicus platensis collected in the field (Rucanelo, province of La Pampa, 2012-2013) and maintained under laboratory conditions.

Parasitoides del bicho canasto, Oiketicus platensis (Lepidoptera: Psychidae) en el caldenal pampeano December 2017, Argentina 7

Temporal variation of parasitoids 20

18

16

14

12

10

8

6 % parasitoidism

4

2

0 Dec 4 Dec 27 Jan 24 Jan 31 Feb 14 Feb 21 Mar 07 Mar 22 Collection date

Diptera Hymenoptera Total

Figure 2. Percentage of Oiketicus platensis larvae parasitized by wasps and flies at each sampling date (Rucanelo, province of La Pampa, 2012-2013).

RESULTS AND DISCUSSION end of summer. The parasitoids were from to the orders Hymenoptera and Diptera, with a clear dominance of flies, Larval activity and adult emergence of O. platensis that represented 81.6% of the total of emerged parasitoids. The first larvae collected in the field were from the sam- Starting from January there was an abundant presence pling conducted on November 20, 2012. The length of the of Diptera, while Hymenoptera presented an increasing bags ranged between 0.1 cm and 1.5 cm, although the ma- tendency toward the end of summer. Figure 2 shows the jority measured 0.5 cm (x: 0.6; SD: 0.7). The presence of temporal variation of parasitoids in Rucanelo. larvae in the field extended from mid-November to the end of February; the length of the bags increased throughout We obtained two species of parasitoid flies of the family the season and reached a maximum value of 6 cm in the Tachinidae: Chetogena caridei (Blanchard) and Patelloa Rucanelo area and 7 cm in Parque Luro. oeceticola (Brèthes), and 15 species of parasitoid wasps from 9 Hymenoptera families. The information referring to The adult males emerged from the baskets stored in the the abundance, the presence in the surveyed areas and laboratory between March 8 and May 3. Most of the emer- the fundamental biological aspects of the parasitoid spe- gences occurred in April (Figure 1). This was coincident cies are summarized in Table 2. with field observations. Although it was not possible to veri- fy the exact date of the moult of the females because they do not leave the bag (Rhainds et al., 2009), the short adult CONCLUSIONS life of this species allows to suppose a synchronization in The survey of O. platensis parasitoids allowed to recog- the emergence of females and males. nize a complex community of natural enemies composed of It has been observed in the related species O. kirbyi that 17 species between Diptera and Hymenoptera. females, longer lived, moult earlier and are receptive at the Based on its abundance, the species that would have the time of emergence of males (Gara et al., 1990; Rhainds et greatest potential to control bagworm moth in La Pampa, al., 1995; Stephens, 1962). would be the tachinid diptera Patelloa oeceticola. This result is different from the results obtained in the foun- Parasitoids dational works on the biological control of bagworm moth. The total parasitoidism in the 4,000 bags of Rucanelo was For example, Brèthes (1921) mentions Chetogena cari- 12.3%, and the maximum achieved value was 17.6% at the dei as the species responsible for the highest mortality of O.

BAUDINO, E.M.; MARTÍNEZ, J.J.; FERNÁNDEZ, L.; GEIST, Y.H.; GALLARDO, H.E.; REIMER, A. ARTICLES RIA / Vol. 43 / N.º 3

Solitary / Species Order / Family Abundance Location1 Host status gregarious

Patelloa oeceticola Diptera: Tachinidae 353 PL, Ruc larva, pupa solitario, gregario

Chetogena caridei Diptera: Tachinidae 18 Ruc larva solitario Tetrastichus sp. Hymenoptera: Eulophidae 40 BV, PL, Ruc larva, pupa gregario Apsilophrys oeceticola Hymenoptera: Encyrtidae 19 BV, Ruc sin datos solitario, gregario Phylloxeroxenus caridei Hymenoptera: Eurytomidae 12 PL, Ruc larva, pupa solitario, gregario Eupelmus caridei Hymenoptera: Eupelmidae 8 BV, PL, Ruc larva, pupa solitario, gregario

Perissocentrus argentinae Hymenoptera: Torymidae 1 Ruc larva gregario larva Brachymeria cf. koehleri Hymenoptera: Chalcididae 3 Ruc solitario (hiperparasitoide) Conura spp. Hymenoptera: Chalcididae 18 PL, Ruc larva, pupa solitario Chirotica bruchi Hymenoptera: Ichneumonidae 11 BV, PL, Ruc larva, pupa solitario Ichneumonidae indet. Hymenoptera: Ichneumonidae 31 BV, PL, Ruc larva, pupa solitario Bracon cf. lizerianum Hymenoptera: Braconidae 1 BV sin datos gregario Microgastrinae indet. Hymenoptera: Braconidae 4 BV, Ruc sin datos solitario Goniozus sp. Hymenoptera: Bethylidae 3 PL, Ruc larva solitario

Table 2. Abundance (Rucanelo, province La Pampa, 2012-2013), presence in the surveyed areas and biological aspects of the obtained parasitoids. 1Bajo Verde: BV; Parque Luro: PL; Rucanelo: Ruc.

platensis in large areas of the center region of the country. cultad de Agronomía, Universidad de la República. Montevideo, It is not possible to establish if this difference is due to the Uruguay. p. 207. fact that the prevalence of one or another species of tachi- BERG, C. 1875. Lepidópteros patagónicos observados en el nid differs between geographical areas, or if it is due to a viaje de 1874. iv. Acta Acad. Nac. Cs. Exactas Univ. Cordoba. 1: temporary variation in the list of parasitoids of the bagworm 63–101. moth when comparing current data with that of early twen- BLANCHARD, E.E.; DE SANTIS, L. 1975. Primera lista anotada tieth century. Recent informal observations indicate that the de oestromuscarios entomófagos argentinos. Rev. Inv. Agr. serie population density of O. platensis in La Pampa is declining, 5, 12(1): 7–76. although it is a heterogeneous process and some produ- BRÈTHES, J. 1921. El Bicho de Cesto. Instituto Biológico de la cers state that they still have problems with this species. Sociedad Rural Argentina. p. 13. CATES, R.G.; RHOADES, D.F. 1977. Prosopis leaves as a re- source for insects. En: SIMPSON, B.B. (Ed.). Mesquite, its biolo- ACKNOWLEDGEMENTS gy in two desert scrub ecosystems. Dowden. Hutchinson & Ross. Pennsylvania. pp. 61–83. We would like to thank Donald R. Davis (Department of DE SANTIS, L. 1967. Catálogo de los himenópteros argentinos Entomology, Smithsonian Institution, Washington D.C.) for de la serie Parasitica, incluyendo Bethyloidea. Provincia de Bue- the confirmation of the identity of O. platensis and to María nos Aires Gobernación, Comisión de Investigación Científica. La Cecilia Gramajo (INSUE, IFML) for the identification of the Plata. p. 337. Diptera of the Tachinidae family. DE SANTIS, L.; ESQUIVEL, L. 1966. Tercera lista de himenóp- We also thank the reviewers of this study for their va- teros parásitos y predatores de los insectos de la República Ar- gentina. Rev. Mus. La Plata (Nueva Serie) Sec. Zool. 9: 47–215. luable comments. This work was conducted with funds of the Ministry of Production, Government of the Province of DE SANTIS, L.; MONETTI, M.C. 2007. Lista de himenópteros parasitoides y depredadores de los insectos de Argentina: primer La Pampa (Res. 735/12 and 865/13), Faculty of Agronomy suplemento. En: Llorente-Bousquets, J.; Lanteri, A. (Ed.). Contri- UNLPam and partially with a grant from the National Agency buciones taxonómicas en órdenes de insectos hiperdiversos. Las for Scientific Promotion and Technology (PICT 2012-0617). Prensas de Ciencias, UNAM, México D. F. México. pp. 91–139. FLORENTINO, D.C.; DIODATO DE MEDINA, L. 1991. Breve panorama de las plagas entomológicas forestales argentinas. Inst. BIBLIOGRAPHY Nac. Inv. Agr. Sist. y Rec. Forest. España 16: 181–190. BENTANCOURT, C.M.; SCATONI, I.B. 1999. Guía de Insectos KÖEHLER, P. 1931. Los Psychidae argentinos (Lepidoptera: y Ácaros de importancia agrícola y forestal en el Uruguay. Fa- Heterocera). Rev. Son. Ent. Arg. 3(16): 347–352.

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BAUDINO, E.M.; MARTÍNEZ, J.J.; FERNÁNDEZ, L.; GEIST, Y.H.; GALLARDO, H.E.; REIMER, A.