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Transmission Potential of the Entomopathogenic Fungi Isaria

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Transmission Potential of the Entomopathogenic Fungi Isaria BioControl DOI 10.1007/s10526-016-9733-4 Transmission potential of the entomopathogenic fungi Isaria fumosorosea and Beauveria bassiana from sporulated cadavers of Diaphorina citri and Toxoptera citricida to uninfected D. citri adults Marcos Roberto Conceschi . Celeste Paola D’Alessandro . Rafael de Andrade Moral . Clarice Garcia Borges Deme´trio . Italo Delalibera Ju´nior Received: 22 May 2015 / Accepted: 17 March 2016 Ó International Organization for Biological Control (IOBC) 2016 Abstract Diaphorina citri Kuwayama (Hemiptera: adults, as well as between T. citricida cadavers and Liviidae) is the vector of the causal agent of Huan- uninfected D. citri adults under laboratory and semi- glongbing disease, and Toxoptera citricida Kirkaldy field conditions. In the laboratory, the presence of one (Hemiptera: Aphididae) is the vector of the citrus to ten D. citri cadavers infected with B. bassiana and I. tristeza virus. D. citri and T. citricida share the same fumosorosea in citrus plants resulted in mortality rates habitat and both are susceptible to Beauveria bassiana of D. citri adults ranging from 51.2 to 81.9 % and 36.2 and Isaria fumosorosea. Therefore, the aim of this to 68 %, respectively. When T. citricida cadavers study was to evaluate the horizontal transmission of B. were used, the mortality rates of uninfected D. citri bassiana ESALQ-PL63 and I. fumosorosea ESALQ- adults ranged from 35.4 to 87.7 % with B. bassiana 1296 between D. citri cadavers and uninfected D. citri and from 41.7 to 80.4 % with I. fumosorosea. The horizontal transmission was also confirmed under semi-field conditions. The results indicate that the Handling Editor: Nicolai Meyling. control of D. citri using I. fumosorosea and B. bassiana can be promoted through conidial cycling & M. R. Conceschi Á C. P. D’Alessandro ( ) Á I. D. Ju´nior in T. citricida, by generating new infection cycles, Department of Entomology and Acarology, ‘‘Luiz de Queiroz’’ College of Agriculture (ESALQ), University of which may contribute to the overall performance of Sa˜o Paulo (USP), Av. Padua Dias, 11, microbial control in citrus. P.O. Box 9, Piracicaba, Sa˜o Paulo CEP 13418-900, Brazil e-mail: [email protected]; Keywords Biological control Á Citrus pests Á [email protected] Entomopathogen Á Horizontal transmission Á M. R. Conceschi Diaphorina citri Á Toxoptera citricida e-mail: [email protected] I. D. Ju´nior e-mail: [email protected] Introduction Rafael de AndradeMoral Á C. G. B. Deme´trio Department of Exact Sciences, ‘‘Luiz de Queiroz’’ Direct and indirect damage caused by pests are College of Agriculture (ESALQ), University of Sa˜o Paulo important factors that result in citrus yield losses. (USP), Av. Padua Dias, 11, P.O. Box 9, Piracicaba, Sa˜o Paulo CEP 13418-900, Brazil Diaphorina citri Kuwayama (Hemiptera: Liviidae) e-mail: [email protected] and Toxoptera citricida Kirkaldy (Hemiptera: Aphi- C. G. B. Deme´trio didae) are vectors of two important diseases: citrus e-mail: [email protected] greening, or huanglongbing (HLB) disease, and citrus 123 M. R. Conceschi et al. tristeza (CTV), respectively (Bove´ 2006; Michaud (Avery et al. 2010; Long et al. 2000; Lopes et al. 1998). HLB is caused by the bacteria ‘Candidatus 2011; Sanjaya et al. 2013; Svedese et al. 2013) as well Liberibacter spp.’, which are transmitted by D. citri as between females and males of the same species and affect citrus production in India, China, Indonesia, during copulation (Garcı´a-Munguı´a et al. 2011; Que- South Africa and Brazil (Kuchment 2013). These pests sada-Moraga et al. 2008; Toledo et al. 2007). Avery are usually controlled through intensive applications et al. (2009) demonstrated in laboratory tests that 83 % of agrochemicals, which may result in side effects of D. citri adults exposed to yellow cards sprayed with such as target pest resurgence, secondary pest out- I. fumosorosea blastopores became infected and breaks and phytosanitary product resistance (Gravena cadavers developed conidia externally. Furthermore, 2005). Moran et al. (2011) showed that inoculation of I. Entomopathogenic fungi are important natural fumosorosea blastopores on yellow cards resulted in enemies of pests because they infect a large number less than 40 % of D. citri infected after three weeks of of arthropods, and under favorable conditions, they confinement in plastic boxes under semi-field condi- can initiate epizootics in the field (Alves 1998). The tions. However, the transmission and dissemination pathogenicity of certain fungal species to D. citri has potential of entomopathogenic fungi from sporulating been reported, such as Isaria fumosorosea, Beauveria cadavers without introduction of artificial inoculation bassiana, Hirsutella citriformis, Lecanicillium lecanii, devices have not been reported in citrus pests. L. muscarium, L. longisporum, Metarhizium aniso- The aphid T. citricida shares the same habitat of pliae and M. brunneum (Ascomycota: Hypocreales) young leaves and citrus shoots with D. citri (Gravena (Avery et al. 2009; Casique-Valdes et al. 2011; 2005). Because of its larger size and generally large Gandarilla-Pacheco et al. 2013; Hall et al. 2012; Hoy population densities relative to D. citri, the host T. et al. 2010; Hunter et al. 2011; Lezama-Gutie´rrez et al. citricida may serve as an important source of inocu- 2012; Meyer et al. 2007, 2008; Padulla and Alves lum in the transmission of B. bassiana and I. 2009; Pinto et al. 2012; Stauderman et al. 2012; fumosorosea to D. citri. Therefore, the objective of Subandiyah et al. 2000; Yang et al. 2006). The the present study was to estimate the horizontal entomopathogenic fungi I. fumosorosea, B. bassiana, transmission of I. fumosorosea (ESALQ-1296) and L. lecanii and M. anisopliae have been reported as B. bassiana (ESALQ-PL63) between sporulating pathogens of T. citricida (Balfour and Khan 2012; cadavers and uninfected adult D. citri (intraspecific Herna´ndez-Torres et al. 2006; Pick et al. 2012; transmission) as well as between sporulating T. Poprawski et al. 1999). citricida cadavers and uninfected adult D. citri The dissemination and transmission of ento- (interspecific transmission) under laboratory and mopathogenic fungi are important factors for deter- semi-field conditions. I. fumosorosea ESALQ-1296 mining their potential as microbial control agents of and B. bassiana ESALQ-PL63 were selected since pests in agroecosystems. An important characteristic they were shown to cause high levels of mortality and of entomopathogenic fungi is the dissemination of sporulation in D. citri and T. citricida (unpublished conidia in the environment due to both abiotic (wind, data). Also, B. bassiana ESALQ-PL63 is registered rain or dew) and biotic (primary or secondary host, under the trade name BoverilÒ (Koppert Brazil), and I. parasites, predators, birds and mammals) factors fumosorosea ESALQ-1296 is under registration in (Hesketh et al. 2010). The conidia present on an Brazil. insect can be transferred to the same or different species of insects by horizontal transmission (Harper 1987), and they can develop new infection cycles and Materials and methods natural epizootics in the field (Hajek and St. Leger 1994). Diaphorina citri and Toxoptera citricida rearing Several studies have confirmed the horizontal transmission of the entomopathogenic fungi B. Diaphorina citri was reared on Murraya paniculata bassiana, M. anisopliae and I. fumosorosea in agri- (Rutaceae) seedlings inside cages of 60 9 60 9 cultural pests through the transmission of conidia 50 cm (height, width and depth) with a steel frame- between sporulating and uninfected individuals work and walls covered with voile fabric. T. citricida 123 Transmission potential of the entomopathogenic fungi Isaria fumosorosea… was reared on Citrus sinensis (Rutaceae) plants, and water (humid chamber) and maintained for three days the insects were confined in bags made of voile fabric. in an incubator at 26 ± 1 °C with a 12 h photophase to Both insects were maintained in a climate-contro promote sporulation. lled room at 25 ± 2 °C, 70–80 % RH and 14 h photophase. Quantification of sporulation Fungal cultivation All of the cadavers of D. citri or T. citricida showed abundant sporulation after pulverization of I. fumo- The entomopathogenic fungi I. fumosorosea ESALQ- sorosea ESALQ-1296 and B. bassiana ESALQ-PL63. 1296 and B. bassiana ESALQ-PL63 were obtained These adults were used to quantify the number of from the collection of entomopathogens of the Lab- conidia per insect. Five sporulated cadavers of each oratory of Pathology and Microbial Control of Insects insect species were chosen at random and placed of the ‘‘Luiz de Queiroz’’ College of Agriculture together in Eppendorf tubes. Then, 1 ml of 0.005 % (ESALQ), University of Sa˜o Paulo (USP), which is Tween 80 was added to the tubes, and the material was located in Piracicaba, Sa˜o Paulo State, Brazil. The homogenized with a VortexÒ apparatus to facilitate ESALQ-1296 strain was obtained from adults of the the removal of conidia from the surface of the insects. whitefly Bemisia tabaci biotype B (Hemiptera: Aley- The total number of conidia was quantified in a rodidae) collected in Jaboticabal, Sa˜o Paulo, in 2001. Neubauer chamber, and the concentration of conidia The ESALQ-PL63 strain was isolated from Atta sp. per individual was estimated. For each insect species (Hymenoptera: Formicidae) collected in Piracicaba, and fungus, four replicates were performed, and each Sa˜o Paulo, in 1992. The fungi were cultivated in 9 cm- replicate included five sporulated adults (n = 20). diameter Petri dishes containing Sabouraud dextrose agar medium supplemented with yeast extract (SDYA: Horizontal transmission test under laboratory 2.5 g l-1 bacteriological peptone, 10 g l-1 dextrose, conditions 2.5 g l-1 yeast extract and 20 g l-1 bacteriological agar) and maintained in an incubator at 26 ± 1 °C The experimental unit consisted of a seedling of Citrus with a 12 h photophase for ten days. limonia measuring 15 cm in height, grown in a pot.
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