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Pathogenicity and Thermal Biology of Mitosporic Fungi As Pathogenicity and thermal biology of mitosporic fungi as potential microbial control agents of Varroa destructor (Acari: Mesostigmata), an ectoparasitic mite of honey bee, Apis mellifera (Hymenoptera: Apidae) Pedro García-Fernández, Cándido Santiago-Álvarez, Non Renseigné To cite this version: Pedro García-Fernández, Cándido Santiago-Álvarez, Non Renseigné. Pathogenicity and thermal biol- ogy of mitosporic fungi as potential microbial control agents of Varroa destructor (Acari: Mesostig- mata), an ectoparasitic mite of honey bee, Apis mellifera (Hymenoptera: Apidae). Apidologie, Springer Verlag, 2008, 39 (6), pp.662-673. hal-00891963 HAL Id: hal-00891963 https://hal.archives-ouvertes.fr/hal-00891963 Submitted on 1 Jan 2008 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Apidologie 39 (2008) 662–673 Available online at: c INRA/DIB-AGIB/ EDP Sciences, 2008 www.apidologie.org DOI: 10.1051/apido:2008049 Original article Pathogenicity and thermal biology of mitosporic fungi as potential microbial control agents of Varroa destructor (Acari: Mesostigmata), an ectoparasitic mite of honey bee, Apis mellifera (Hymenoptera: Apidae)* Pedro Garc´ia-Fernandez´ 1, Cándido Santiago-Álvarez 2, Enrique Quesada-Moraga2 1 Área de la Producción Agraria, IFAPA, Centro Camino de Purchil, CAP, Junta de Andalucía, C/ Camino de Purchil s.n, 18071 Granada, Spain 2 Departamento de Ciencias y Recursos Agrícolas y Forestales, E.T.S.I.A.M., Universidad de Córdoba, Campus de Rabanales, Edificio C4 Celestino Mutis, Cordoba 14071, Spain Received 16 January 2008 – Revised and accepted 7 July 2008 Abstract – Pathogenicity and thermal biology (tb) were investigated for entomopahogenic fungi isolates (EFI), which were examined as potential biocontrol agents of the ectoparasite Varroa destructor,themajor disease of honey bees in Andalusia (Spain). All 16 of the assayed EFI were pathogenic to V. destructor, while two of them were exceptionally pathogenic to the mite: Metarhizium anisopliae 01/121-Su [AST 35.0 h, 100% mortality at 72 h post infection (p.i.)] and Beauveria bassiana 01/103-Su (AST 39.4 h, 96.0% mortality at 72 h p.i.). The tb of the five most virulent isolates against the mite was investigated at seven temperatures (10–40 oC) by using a modified generalized beta function that accounted for 79.8–96.4% of the data variance. Optimum temperatures and maximum temperatures for growth ranged from 24.9 to 31.2 ◦C and from 30.1 to 35.0 ◦C respectively. On the basis of their pathogenicity, thermal requirements and safety to honey bees, two isolates showed promise as candidates for V. destructor control. Varroa destructor / Apis mellifera / entomopathogenic fungi / virulence / biological control / Beauveria / Metarhizium / Lecanicillium / Hirsutella / mite / parasites/ mycoacaricides 1. INTRODUCTION adult females feed on their host’s haemolymph and transmit viruses that can lead to deformi- Varroa destructor Anderson and Trueman ties (Todd et al., 2007) and that are manifested (2000) is a parasitic mite of western Asia at all stages of development, from larvae to and is responsible for the highest mortality adults (Todd et al., 2007). of colonies of Apis mellifera L. in Andalusia Currently, V. destructor is mainly con- (Spain). Its expansion into Europe, northern trolled with synthetic acaricides, the Africa, and North and South America began pyrethroids, fluvalinate (Apistan)and in the last quarter of the 20th century. V. d e - flumethrin (Bayvarol), and the amitraz structor has devastating consequences in bee neurotoxin (Apivar) and with organic acids colonies and is the most important parasite such as formic acid, lactic acid, and oxalic of honey bee in Andalusia (Spain) (García- acid. The supposed harmlessness of the Fernández et al., 1995, 2001). The parasite’s chemical treatments has come into question. Corresponding author: P. García-Fernández, Repeated use of the same active ingredients [email protected] has promoted the development of resistant * Manuscript editor: Marla Spivak mite populations (Milani, 1999; Anon, 2001; Article published by EDP Sciences Assay of entomopathogenic fungi against Varroa destructor 663 Luzón and García Fernández, 2002), and areas of the honey bee colony (Davidson et al., acaricide residues can contaminate honeybee 2003). The temperature regime within honey products (Wallner, 1999) In addition, the bee colonies is determined by ambient condi- organic acids require careful handling because tions and the absence or presence of brood. sudden release can cause the death of the Temperatures within broodless areas of the brood or the substitution of the queen in colony are around 25 ◦C, while those in brood Spain’s weather conditions. areas are maintained around 34–35 ◦C, with ◦ The use of natural compounds, particularly 32 C in the periphery of the brood (Le Conte essential oils from aromatic plants such as thy- et al., 1990). Thus, fungal isolates selected mol (Apiguard) have limited drawbacks, but from laboratory bioassays to be evaluated in their utilization has not been well accepted by future experiments within honey bee colonies Spanish beekeepers because they are difficult should tolerate the thermal conditions inside to apply and dependent on ambient tempera- the bee hive (Davidson et al., 2003). ◦ ◦ ture (> 15 Cand< 40 C). The studies described here were undertaken Biological control by the natural enemies with the goal of identifying autochthonous iso- of mites provides an option that overcomes lates of mitosposporic fungi that possess good the drawbacks of controlling V. destructor pathogenicity against V. destructor. The fungal with chemicals (Chandler et al., 2001). Among isolates were obtained from the University of entomopathogenic microorganisms, the fun- Cordoba Agricultural Entomology Research gal pathogens show the highest potential for group’s collection. The thermal biology of the biocontrol of the mite as they are the only fungal pathogens was assessed to determine ones that show contact action, via integu- whether or not these isolates could be poten- ment (Chandler et al., 2001). The poten- tial microbial control agents for V. destructor. tial use of mitosporic Ascomycetes such as Metarhizium, Beauveria, Lecanicillium and Hirsutella has been pointed out in particular (Kanga and James, 2002; Kanga et al., 2002, 2. MATERIALS AND METHODS 2003;Meikleetal.,2006, 2007;Shawetal., 2002). To date, only a limited number of B. bassiana isolates have been isolated from V. 2.1. Fungi culture and preservation destructor cadavers, by Meikle et al. (2006) in southern France and by us in southern Spain. The mite’s susceptibility to B. bassiana Sixteen isolates were used in this experiment: (Meikle et al., 2007), to Metarhizium aniso- seven belonged to Beauveria bassiana (Balsamo) pliae (Kanga et al., 2003)andtoHirsutella Vuillemin, five to Metarhizium anisopliae (Metsch) thompsonii Fisher (Kanga and James, 2002; Sorok, one to Lecanicillium lecanii Zimmermann Kanga et al., 2002, 2003;Shawetal.,2002) (Gams & Zare), one to Hirsutella kirchneri (Ros- has been observed in previous laboratory as- trop) Mister, one to H. nodulosa Petch and one to Hirsutella sp. (Tab. I). Two of the B. bassiana iso- says. lates have been obtained from naturally infected The broad spectrum of hosts shown by mites at Granada and Jerez (Andalusia, Spain) af- ff these fungal species and the enormous di er- ter surveying natural populations of the mite during ences in virulence and heat requirements for the period 2005–2007. growth among isolates (Zimmermann, 2007a, All isolated were maintained in Malt Extract b) raises the hope of finding an isolate with Agar medium (MEA) at 4 ◦C, For the susceptibility selective activity against V. destructor, with assays, subcultures were made in Sabouraud Dex- thermal requirements adapted to the environ- trose Agar (SDA) in Petri dishes and incubated at mental conditions found in beehives. Consid- 27 ◦C for 14 d for B. bassiana, M. anisopliae and L. ering the high humidity conditions within the lecanii and incubated for 21 days for the Hirsutella bee hive’s interior environment, the major con- species to ensure proper sporulation. The concen- straint to fungal effectiveness may instead be tration of conidia was assessed by the colony form- the high temperatures maintained within some ing unit method (CFU) (Goettel and Inglis, 1997). 664 P. García-Fernández et al. Table I. Identity of the fungal isolates from the culture collection at A.F.S.R. Department of the University of Cordoba assayed against Varroa destructor. No. Fungal species1 Isolate Insect host or substrate (habitat) Site and date of origin 1 EABb 04/01-Tip Timaspis papaveris (Hymenoptera; Cynipidae) Sevilla (Spain), 2004 2EABb01/110-Su Soil (oak) Sevilla (Spain), 2001 3 Bb-1333 Bactrocera oleae (Diptera; Tephritidae) Grece, 1961 Beauveria bassiana 4EABb01/103-Su Soil (forest) Sevilla (Spain), 2001 5EABb01/33-Su Soil (olive tree orchard) Cádiz (Spain), 2001 6EABb07/05-Vd Varroa destructor Cádiz (Spain), 2007 7EABb07/07-Vd Varroa destructor Granada (Spain),
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