Ageniaspis citricola, Logvinovskaya, 1983

Paiva, Paulo Eduardo Branco & Yamamoto, Pedro Takao, 2015, Natural parasitism of the citrus leafminer (Lepidoptera: Gracillariidae) over eight years in seven citrus regions of São Paulo, Brazil, Florida Entomologist 98 (2), pp. 660-660 : 660

Key Words: biological control; Ageniaspis citricola ; Phyllocnistis citrella ; insecticide; HLB management

Resumo

A minadora das folhas dos citros (MFC), Phyllocnistis citrella Stainton ( Lepidoptera : Gracillariidae ), foi encontrada pela primeira vez no Brasil em 1996. Em 1998, o parasitoide Ageniaspis citricola Logvinovskaya ( Hymenoptera : Encyrtidae ) foi introduzido e se estabeleceu em várias regiões do país. Nesse estudo, foram feitas130 amostragens, de uma hora, de folhas de laranjeiras doces [Citrus sinensis (L.) Osbeck] com câmaras pupais da MFC, para se estimar o parasitismo da MFC em 7 regiões do estado de São Paulo, entre 2000 e 2008. O tamanho das amostras variou de 10 a 275 folhas (média = 65). O parasitoide mais abundante foi o encirtídeo A. citricola (encontrado em 91.8% das amostragens). O maior parasitismo da MFC por A. citricola foi observado na região sul do estado (Botucatu), 70,2 ± 6,6 (média ± EPM), e o menor parasitismo na região norte (Barretos), 12,8 ± 5,7%. O parasitismo da MFC por A. citricola e seus parasitoides nativos ( Galeopsomyia fausta LaSalle , Cirrospilus spp. and Elasmus sp. ) não diferiram entre as estaÇões do ano. O aumento de seis vezes no uso de inseticidas nos pomares de citros, após 2004, quando o Huanglongbing (HLB) foi encontrado no estado de São Paulo, não reduziu o nível de parasitismo da MFC. O nível médio de parasitismo foi de 50,8 ± 4,2%, antes do HLB (2000-2004), e 56,0 ± 4,4%, após o HLB (2005-2008), indicando a adaptaÇão de A. citricola a um agroecossistema perturbado.

Palavras chaves: controle biológico; Ageniaspis citricola ; Phyllocnistis citrella ; inseticida; manejo de HLB

The citrus leafminer (CLM) Phyllocnistis citrella Stainton ( Lepidoptera : Gracillariidae ) was first recorded in Brazil in March 1996 in São Paulo State ( Prates et al. 1996). Larvae of P. citrella may reduce the foliar area by compromising new leaf growth and by reduced photosynthesis in the damaged leaves ( Schaffer et al. 1997). Necrosis and defoliation also are induced by the larvae, thus hindering plant development, particularly in younger plants. In addition to the direct damage, the presence of the CLM may facilitate the incidence and increase the severity of citrus canker, a disease caused by the bacterium Xanthomonas citri subsp. citri ( Xanthomonadales : Xanthomonadaceae ) ( Chagas et al. 2001; Jesus Jr. et al. 2006; Hall et al. 2010).

Hymenoptera of the genera Galeopsomyia , Cirrospilus ( Eulophidae ), Elasmus ( Elasmidae ), Pachyneuron ( Pteromalidae ), and Teleno- mus ( Scelionidae ) were the first CLM parasitoids identified in citrus groves in Brazil ( Penteado-Dias et al. 1997). Other parasitoids were subsequently reported, including Horismenus spp. ( Eulophidae ), Eu- pelmus sp. ( Eupelmidae ), and Conura sp. ( Chalcididae ) ( Costa et al. 1999). Afer the introduction of CLM in the Americas, 3 new species belonging to the Eulophidae family were described: Cirrospilus floriden- sis Evans, Cirrospilus neotropicus Diez and Fidalgo , and Galeopsomyia fausta LaSalle ( LaSalle & Peña 1997; Evans 1999; Diez & Fidalgo 2003). All 3 species occur in Brazil and were found to be the most frequent parasitoids in São Paulo from 1997 to 1999, particularly the eulophid G. fausta ( Paiva et al. 2000; Sá et al. 2000).

In 1998,the encyrtid Ageniaspis citricola Logvinovskaya ( Hymenoptera : Encyrtidae ) was introduced in Brazil, as part of a classical biologi-

University of São Paulo, Escola Superior de Agricultura Luiz de Queiroz, Department of Entomology and Acarology, 13418-900, Piracicaba,SP, Brazil *Corresponding author; E-mail: [e-mail] cal control program. This species was soon established in several Brazilian states (São Paulo, Paraná, Minas Gerais, Rio Grande do Sul, Santa Catarina, Goiás, Bahia, Rio de Janeiro, Piauí, and Rio Grande do Norte) ( Chagas et al. 2002; Parra et al. 2004). It became the most common CLM parasitoid, with native parasitoids occurring at lower levels ( Sá et al. 2000). The estimated A. citricola parasitism was approximately 30% in post-release samples (1998–2000) ( Chagas et al. 2002).

The combination of the damage caused by CLM and the occurrence of citrus canker highlighted the importance of the management and control of this insect, which generally involves only chemical control in nurseries and young trees. The use of cupric bactericides to prevent the occurrence of canker and insecticides for leafminer control became usual in endemic areas. However, the use of insecticides for CLM control has been incompatible to its biological control efforts in many cases ( Villanueva-Jiménez & Hoy 1998; Villanueva-Jiménez et al. 2000).

In Brazil, the use of insecticides in citrus groves increased dramatically afer Huanglongbing (HLB) was found in 2004, as part of the HLB mitigation, aimed at controlling the insect vector Diaphorina citri Ku- wayama ( Hemiptera : Liviidae ), and,we hypothesized that this could strongly affect the CLM parasitism. From 2003 to 2008, the use of insecticides in citrus, mainly in São Paulo State, increased 6-fold ( Neves et al. 2010). In this scenario, the aims of this study were (i) to estimate the CLM parasitism by A. citricola and native parasitoids in citrus-growing regions of São Paulo State (northern, northeastern, central, western, and southern) between 2000 and 2008, and (ii) to compare how 2 periods, i.e., prior to HLB with lower number of insecticide sprays and afer HLB with higher number of sprays, affected CLM parasitism.