Abstract
Purpureocillium lilacinum is an entomopathogenic fungus. An experiment was conducted to see the sublethal effects of P. lilacinum on Anastrepha ludens adults. The infection of P. lilacinum reduced daily food consumption per fly ranging from 4.25 ± 0.28 to 6.44 ± 0.27 µl for infected flies, and from 6.30 ± 0.28 to 7.81 ± 0.22 µl for non-infected control flies. The age of treatment in males showed a significant effect on their ability to mate (χ2 = 5.32, P < 0.02). Early stage infection (4 days-old), reduced the male mating propensity significantly (10 ± 0.46 treated to 15.4 ± 0.26 untreated, F 8, 5.94 = 5.592, P < 0.01), compared to later stage (8 days-old) insignificant effect. No effect of fungal infection on an ability of male to inseminate the females was noticed, as fertility of the females mated with infected males was not declined. An inoculated single female (mixture of talc and P. lilacinum) was able to transmit conidia to four groups of 10 males within four days. Males exposed to females on the first day acquired in average 1.7 ⋅ 106, on the second day 1.7 ⋅ 105, on the third day 7.3 × 104 and the fourth day 3.5 ⋅ 104 conidia/ male; which resulted 67.5, 55.0, 20.0, and 7.5 % male mortality, respectively. Our study demonstrated that horizontal transmission through copulation could be used to suppress A. ludens populations.
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References
Abbot W (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267. https://doi.org/10.1093/jee/18.2.265a
Aluja M, Rull J, Sivinski J, Trujillo G, Pérez-Staples D (2009) Male and female condition influence mating performance and sexual receptivity in two tropical fruit flies (Diptera: Tephritidae) with contrasting life histories. J Insect Physiol 55: 1091–1098. https://doi.org/10.1016/j.jinsphys.2009.07.012
Arthurs S, Thomas MB (2000) Effects of a mycoinsecticide on feeding and fecundity of the brown locust Locustana pardalina. Biocontrol Sci Technol 10(3):321–329. https://doi.org/10.1080/09583150050044592
Bajan C, Kmitowa K (1972) The effect of entomogenous fungi Paecilomyces farinosus (Dicks.) Brown et Smith and Beauveria bassiana (Bals.) Vuill. on the oviposition by Leptinotarsa decemlineata Say females, and on the survival of larvae. Pol J Ekol 20:423–432
Baverstock J, Roy H, Pell EJK (2010) Entomopathogenic fungi and insect behaviour: from unsuspecting hosts to targeted vectors. Biocontrol 55:89–102. https://doi.org/10.1007/s10526-009-9238-5
Boller EF (1968) An artificial oviposition device for the European cherry fruit fly, Rhagoletis cerasi. J Econ Entomol 61(3):850–852
Cangussu JA, Zucoloto FS (1996) Effect of protein sources on fecundity, food acceptance, and sexual choice by Ceratitis capitata (Diptera, Tephritidae). Rev Brasil Biol 57:611–618
Castillo MA, Moya PM, Hernández E, Primo-Yúfera E (2000) Susceptibility of Ceratitis capitata Wiedemann (Diptera: Tephritidae) to entomopathogenic fungi and their extracts. Biol Control 19:274–282. https://doi.org/10.1006/bcon.2000.0867
Castillo Lopez D, Zhu-Salzman K, Ek-Ramos MJ, Sword GA (2014) The Entomopathogenic fungal endophytes Purpureocillium lilacinum (Formerly Paecilomyces lilacinus) and Beauveria bassiana negatively affect cotton aphid reproduction under both greenhouse and field conditions. PLoS One 9(8):e103891. https://doi.org/10.1371/journal.pone.0103891
Daniel C, Wyss E (2009) Susceptibility of different life stages of the European cherry fruit fly, Rhagoletis cerasi, to entomopathogenic fungi. J Appl Entomol 133:473–483. https://doi.org/10.1111/j.1439-0418.2009.01410.x
De la Rosa W, López FL, Liedo P (2002) Beauveria bassiana as a pathogen of the Mexican fruit fly (Diptera: Tephritidae) under laboratory conditions. J Econ Entomol 95:36–43. https://doi.org/10.1603/0022-0493-95.1.36
Dimbi S, Maniania NK, Ekesi S (2009) Effect of Metarhizium anisopliae inoculation on the mating behavior of three species of African Tephritid fruit flies, Ceratitis capitata. Ceratitis cosyra and Ceratitis fasciventris. Biol Control 50:111–116. https://doi.org/10.1016/j.biocontrol.2009.04.006
FAO/IAEA/USDA (2019) Product quality control for sterile mass-reared and released tephritid fruit flies, Version 7.0. International Atomic Energy Agency, Vienna, Austria, pp 148
Fiedler Z, Sosnowska D (2007) Nematophagous fungus Paecilomyces lilacinus (Thom) Samson is also a biological agent for control of greenhouse insects and mite pests. Biocontrol 52:547–558. https://doi.org/10.1007/s10526-006-9052-2
Flores S, Campos S, Villaseñor A, Valle A, Enkerlin W, Toledo J, Liedo P, Montoya P (2013) Sterile males of Ceratitis capitata (Diptera: Tephritidae) as disseminators of Beauveria bassiana conidia for IPM strategies. Biocontrol Sci Technol 23:1186–1198. https://doi.org/10.1080/09583157.2013.822473
Goettel MS, Inglis GD (1997) Fungi: Hyphomycetes. In: Lacey LA (ed) Manual of Techniques in Insect Pathology. Academic, Cambridge, pp 213–248. https://doi.org/10.1016/B978-012432555-5/50013-0
Gutiérrez JM (2010) El Programa Moscas de la Fruta en México [The Fruit Fly Program in Mexico]. In: Montoya P, Toledo J, Hernández E (eds) Moscas de la Fruta: Fundamentos y Procedimientos para su Manejo [Fruit flies: Principles and procedures for management]. Editorial SyG, Cd México, pp 3–10
Hajek A (1989) Food Consumption by Lymantria dispar (Lepidoptera: Lymantriidae) Lavae Infected with Entomophaga maimaga (Zygomycetes: Entomophthorales). Environ Entomol 18:723–727. https://doi.org/10.1093/ee/18.4.723
Khan I, Prasad NG (2013) Male Drosophila melanogaster show adaptive mating bias in response to female infection status. J Insect Physiol 59:1017–1023. https://doi.org/10.1016/j.jinsphys.2013.07.010
Landolt PE, Sivinski J (1992) Effects of time of day, adult food, and host fruit on incidence of calling by male caribbean fruit flies (Diptera: Tephritidae). Environ Entomol 21:382–387. https://doi.org/10.1093/ee/21.2.382
Liedo P, Orozco D, Cruz-López L, Quintero JL, Becerra-Pérez C, Hernández MR, Oropeza A, Toledo J (2013) Effect of post-teneral diets on the performance of sterile Anastrepha ludens and Anastrepha obliqua fruit flies. J Appl Entomol 137:49–60. https://doi.org/10.1111/j.1439-0418.2010.01568.x
Meza-Hernández JS, Díaz-Fleischer F (2006) Comparison of sexual compatibility between laboratory and wild Mexican fruit flies under laboratory and field conditions. J Econ Entomol 99:1979–1986. https://doi.org/10.1603/0022-0493-99.6.1979
Moller AP (1993) A fungus infecting domestic flies manipulates sexual behavior of its host. Behav Ecol Sociobiol 33:403–407. https://doi.org/10.1007/BF00170255
Moore D, Reed M, Le Patorel G, Abraham YJ, Prior C (1992) Reduction of feeding by the desert locust, Schistocerca gregaria, after infection with Metarhizium flavoviride. J Invertebr Pathol 60:304–307. https://doi.org/10.1016/0022-2011(92)90013-T
Orozco D, Meza JS, Zepeda S, Solís E, Quintero-Fong JL (2013) Tapachula-7, a new genetic sexing strain of the Mexican fruit fly (Diptera: Tephritidae): sexual compatibility and competitiveness. J Econ Entomol 106(2):735–741. https://doi.org/10.1603/EC12441
Ortiz-Urquiza A, Garrido-Jurado I, Santiago-Álvarez C, Quesada-Moraga E (2009) Purification and characterization of proteins secreted by the entomopathogenic fungus Metarhizium anisopliae with insecticidal activity against adults of the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae). Pest Manag Sci 65:1130–1139. https://doi.org/10.1002/ps.1803
Papanastasiou SA, Nakas CT, Carey JR, Papadopoulos NT (2013) Condition-dependent effects of mating on longevity and fecundity of female Medflies: The interplay between nutrition and age of mating. PLos One 8(7):e70181. https://doi.org/10.1371/journal.pone.0070181
Quesada-Moraga E, Ruiz-Garcia E, Santiago-Alvarez C (2006) Laboratory evaluation of entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae against puparia and adults of Ceratitis capitata (Diptera: Tephritidae). J Econ Entomol 99:1955–1966. https://doi.org/10.1603/0022-0493-99.6.1955
Quesada-Moraga E, Martín-Carballo I, Garrido-Jurado I, Santiago-Álvarez C (2008) Horizontal transmission of Metarhizium anisopliae among laboratory populations of Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). Biol Control 47:115–124. https://doi.org/10.1016/j.biocontrol.2008.07.002
R Development Core Team (2018) R: A Language and environment for statistical computing. R Foundation for Statistical Computing, ISBN 3-900051-07-0, Vienna
Rambadan S, Jugmohan H, Khan A (2011) Pathogenicity and haemolymph protein changes in Edessa meditabunda F. (Hemiptera: Pentatomidae) infected by Paecilomyces lilacinus. JBP 4:169–175
Reddy GVP, Furlong MJ, Pell JK, Poppy GM (1998) Zoophthora radicans infection inhibits the response to and production of sex pheromone in the diamondback moth. J Invert Pathol 72:167–169. https://doi.org/10.1006/jipa.1998.4769
Roode JC, Lefèvre T (2012) Behavioral immunity in insects. Insects 3:789–820. https://doi.org/10.3390/insects3030789
Salcedo-Baca D, Terrazas-González GH, Lomelí-Flores JR, Rodríguez-Leyva E (2010) Análisis Costo-Beneficio del Programa Moscamed [Cost-Benefit Analysis of the Medfly Program]. In: Montoya P, Toledo J, Hernandez E (eds) Moscas de la Fruta: Fundamentos y Procedimientos para su Manejo [Fruit flies: Principles and procedures for management]. Editorial S y G, Ciudad de México, pp 27–40
San Andrés V, Ayala I, Abad MC, Primo J, Castañera P, Moya P (2014) Laboratory evaluation of the compatibility of a new attractant contaminant device containing Metharhizium anisopliae with Ceratitis capitata sterile males. Biol Control 72:54–61. https://doi.org/10.1016/j.biocontrol.2014.02.007
TeferaT, Pringle KL (2003) Food consumption by Chilo partellus (Lepidoptera: Pyralidae) larvae infected with Beauveria bassiana and Metarhizium anisopliae and effects of feeding natural versus artificial diets on mortality and mycosis. J Invert Pathol 84:220–225. https://doi.org/10.1016/j.jip.2003.11.001
Thomas MB, Blanford S, Lomer CJ (1997) Reduction of feeding by the variegated grasshopper, Zonocerus variegatus, following infection by the fungal pathogen, Metarhizium Xavoviride. Biocontrol Sci Technol 7:327–334. https://doi.org/10.1080/09583159730730
Thorvilson HG, Pedigo LP, Lewis LC (1985) Soybean leaf consumption by Nomuraea rileyi (Fungi: Deuteromycotinia) infected Plathypena scabra (Lepidoptera: Noctuidae) larvae. J Invert Pathol 46:265–271. https://doi.org/10.1016/0022-2011(85)90068-0
Toledo J, Campos SE, Flores S, Liedo P, Barrera JF, Villaseñor A, Montoya P (2007) Horizontal transmission of Beauveria bassiana in Anastrepha ludens (Diptera: Tephritidae) under laboratory and field cage conditions. J Econ Entomol 100:291–297. https://doi.org/10.1603/0022-0493(2007)100[291:HTOBBI]2.0.CO;2
Toledo-Hernández RA, Toledo J, Sánchez D (2018) Effect of Metarhizium anisopliae (Hypocreales: Clavicipitaceae) on food consumption and mortality in the Mexican fruit fly, Anastrepha ludens (Diptera: Tephritidae). Int J Trop Insect Sc 38(3):254–260. https://doi.org/10.1017/S1742758418000073
Toledo-Hernández R, Toledo J, Valle-Mora J, Holguin-Meléndez F, Liedo P, Huerta-Palacios G (2019) Pathogenicity and virulence of Purpureocillium lilacinum on Mexican fruit fly adults. Fla Entomol 102(2):309–314. https://doi.org/10.1653/024.102.0204
Wang ZG, Knudsen GR (1993) Effect of Beauveria bassiana (Fungi: Hyphomycetes) on fecundity of the Russian wheat aphid (Homoptera: Aphididae). Environ Entomol 22:874–878. https://doi.org/10.1093/ee/22.4.874
Wraight SP, Inglis GD, Goettel MS (2007) Fungi. In: Lacey LA, Kaya HK (eds) field manual of techniques in invertebrate pathology. Springer, The Netherlands, pp 223–248. https://doi.org/10.1007/978-1-4020-5933-9_10
Zepeda-Cisneros CS, Hernández JSM, García-Martínez V, Ibañez-Palacios J, Zacharopoulou A, Franz G (2014) Development, genetic and cytogenetic analyses of genetic sexing strains of the Mexican fruit fly, Anastrepha ludens Loew (Diptera: Tephritidae). BMC Genet 15(2):S1. https://doi.org/10.1186/1471-2156-15-S2-S1
Acknowledgements
We are grateful to Santos Espinosa, Karen Serrano, Oscar Mikery, Jorge Villafuerte, Luis Tort, Marcela Donis, Damaris Cruz, Alehli Martínez, Gonzalo García, Sergio Mejía and Gustavo Rodas for technical assistance. To the Moscafrut program (SENASICA, IICA SADER), for providing the fruit flies. To the Consejo Nacional de Ciencia y Tecnología for scholarship granted to RATH (CONACYT-RATH − 361675).
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The research entitled “Effects of Purpureocillium lilacinum (Hypocreales: Ophiocordycipitaceae) on food and sexual behavior of Anastrepha ludens (Diptera: Tephritidae) fruit flies” was funded by El Colegio de la Frontera Sur. The authors declare that they have no conflict of interest. This research did not involve human participants. We did use animals (insects, fruit flies) and tried to follow standard protocols used in this type of research. Since no human participants were involved, no informed consent was required.
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Figure S1 Males of Anastrepha ludens marked and unmarked with water paint on the thorax. Figure S2 Items used in evaluation fertility of Anastrepha ludens females. (a) Oviposition device as agar spheres, (b) Micrograph of Anastrepha ludens egg on agar sphere, c and d) Anastrepha ludens eggs arranged on a piece of black cloth placed on a water saturated sponge in a Petri dish. Figure S3 Male and female of Anastrepha ludens with mycoses caused by Purpureocillium lilacinum. (PDF 210 KB)
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Toledo-Hernández, R., Toledo, J., Liedo, P. et al. Effects of Purpureocillium lilacinum (Hypocreales: Ophiocordycipitaceae) on food consumption and sexual behavior of Anastrepha ludens (Diptera: Tephritidae) fruit flies. Int J Trop Insect Sci 41, 2401–2408 (2021). https://doi.org/10.1007/s42690-020-00414-2
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DOI: https://doi.org/10.1007/s42690-020-00414-2