Abstract
Over the last decades, a few fungal species have been mentioned in the literature associated with the rubber tree lace bug, Leptopharsa heveae Drake & Poor (Hemiptera: Tingidae). The rubber plantation area treated with these biocontrol agents has been steady since the 1990s, estimated in 10,000–15,000 ha per year. A few large-scale rubber operations, one biocontrol company, and three government-owned laboratories were, and currently one still is, involved in their commercialization. One species, currently referred to as Sporothrix insectorum, has been historically deployed in biocontrol applications in Brazilian rubber farms. However, L. heveae–infecting isolates have only been identified through morphological examinations; therefore, proper molecular assessments are needed for accurate identifications. Hence, DNA of six L. heveae–infecting isolates (five of which have been deployed in field applications) were extracted and sequenced. Multigene phylogeny found that both Simplicillium lanosoniveum and Cordyceps (formerly Isaria) sp. have been sprayed on rubber plantations to manage L. heveae populations, although the former is the only one currently applied. Simplicillium lanosoniveum and Cordyceps sp. have no relation whatsoever to true Sporothrix species associated with human and animal diseases. Therefore, our molecular data may encourage biocontrol companies to register mycoinsecticides targeting L. heveae. We also added unpublished historical accounts after contacting key contributors to the launching of this not so well-known biocontrol program in the 1980s.
Similar content being viewed by others
References
Almeida JM, Batista Filho A (2006) Microrganismos no controle de pragas. In: Pinto AS, Nava DE, Rossi MM, Malerbo-Souza DT (eds) Controle Biológico de Pragas: na Prática. CP 2, Piracicaba (SP), pp 35–44
Alves SB (1998) Fungos entomopatogênicos. In: Alves SB (ed) Controle Microbiano de Insetos, 2ª edn. FEALQ, Piracicaba, pp 289–381
Alves RT, da Silva EAF, de Sousa KM, Oliveira MAS, Pereira AV, Pereira EBC, Junqueira NTV, Icuma IM (2003) Controle biológico do percevejo-de-renda da seringueira com o uso de micoinseticida formulado em óleo emulsionável. Boletim de Pesquisa e Desenvolvimento n° 113. EMBRAPA, Planaltina (DF), p 23
Campanhola C, Bettiol W (2003) Métodos alternativos de controle fitossanitário. Embrapa Meio Ambiente, Jaguariúna, p 279
Castrillo LA, Wheeler MM (2017) ARSEF Database. http://ARSEF.fpsnl.cornell.edu/4DACTION/W_List_Tables/param. Accessed 10 Feb 2020
Celestino Filho P, Magalhães FEL (1986) Ocorrência do fungo Sporothrix insectorum Hoog & Evans, parasitando a mosca-de-renda (Leptopharsa heveae Drake & Poor) em seringal de cultivo. Pesquisa em Andamento n° 42. EMBRAPA-CNPSD, Manaus, p 2
Charles VK (1937) A fungus on lace bug. Mycologia 29:216–221
Chen W-H, Liu C, Y-Feng H, Liang J-D, Liang Z-Q (2018) Akanthomyces araneogenum, a new Isaria-like araneogenous species. Phytotaxa 379:66–072
Chiriví-Salomón JS, Danies G, Restrepo S, Sanjuan T (2015) Lecanicillium sabanense sp. nov. (Cordycipitaceae) a new fungal entomopathogen of coccids. Phytotaxa 234:63–74
Costa EDS (2015) Tendências e ciclos climáticos em Ouro Branco do Sul (Fazenda Michelin-MT) no período de 1980 a 2011. MSc Dissertation. Universidade Federal do Mato Grosso, Rondonópolis, p 226
De Beer ZW, Duong TA, Wingfield MJ (2016) The divorce of Sporothrix and Ophiostoma: solution to a problematic relationship. Stud Mycol 83:165–191
de Camargo AP, Marin FR, Camargo MBP (2003) Zoneamento climático da heveicultura no Brasil. Embrapa Monitoramento por Satélite, Campinas, p 19
de Hoog GS (1974) The genera Blastobotrys, Sporothrix, Calcarisporium and Calcarisporiella gen. Nov. Stud Mycol 7:1–84
Dias LP, Araújo CAS, Pupin B, Ferreira PC, Braga GUL, Rangel DEN (2018) The Xenon Test Chamber Q-SUN® for testing realistic tolerances of fungi exposed to simulated full spectrum solar radiation. Fungal Biol 122:592–601
Dong QL, Lin TY, Xing XY, Chen B, Han Y (2013) Identification of a symbiotic fungus from blue–green alga and its extracellular polysaccharide. Lett Appl Microbiol 58:303–310
Drake CJ, Poor ME (1935) An underscribed rubber tingitid from Brazil (Hemiptera). J Wash Acad Sci 25:283–284
Gasparotto L (2003) Doenças da seringueira nas áreas tradicionais de cultivo e de escape da Amazônia. In: Frazão DAC, Cruz E d S, Viégas I d JM (eds) . Serinqueira na Amazônia - Situação atual e perspectivas. EMBRAPA, Belém, pp 207–215
Gasparotto L, Santos AF d, Pereira JCR, Ferreira FA (1997) Doenças da seringueira no Brasil. EMBRAPA-CPAA, Manaus, p 168
Gonçalves PS, Martins ALM, Furtado EL, Samburago R, Ottati EL, Ortolani AA, Junior GG (2002) Desempenho de clones de seringueira da série IAC 300 na região do planalto de São Paulo. Pesqui Agropecu Bras 37:131–138
Huang S, Maharachchikumbura SSN, Jeewon R, Bhat J, Phookamsak R, Hyde KD, Al-Sadi AM, Kang J (2018) Lecanicillium subprimulinum (Cordycipitaceae, Hypocreales), a novel species from Baoshan, Yunnan. Phytotaxa 348:99–108
Humber RA, Rocha LF, Inglis PW, Kipnis A, Luz C (2013) Morphology and molecular taxonomy of Evlachovaea-like fungi, and the status of this unusual conidial genus. Fungal Biol 117:1–12
Junqueira NTV, Lima MIPM, Martins MAM, Magalhães FEL (1987) Isolamento e cultivo do fungo Sporothrix insectorum Hoog & Evans a ser utilizado para o controle da mosca-de-renda da seringueira. Comunicado Técnico n° 56. EMBRAPA-CNPSD, Manaus, p 4
Junqueira NTV, Pinheiro E, Alves RT, Celestino Filho P, Pereira AV, Oliveira MAS, Fialho JF, Gasparotto L (1999) Controle biológico do percevejo-de-renda (Leptopharsa heveae Drake & Poor) em seringais de cultivo. Circular Técnica n° 3. EMBRAPA Cerrados, Planaltina, p 30
Kauffman CA (1999) Sporotrichosis. Clin Infect Dis 29:231–237
Kepler RM, Sung GH, Ban S, Nakagiri A, Chen MJ, Huang B, Li Z, Spatafora JW (2012) New teleomorph combinations in the entomopathogenic genus Metacordyceps. Mycologia 104:182–197
Kepler RM, Luangsa-ard J, Hywel-Jones NL, Quandt CA, Sung G-H, Rehner SA, Aime AC, Henkel TW, Sanjuan T, Zare R, Chen M, Li Z, Rossman AY, Spatafora JW, Bhushan Shrestha B (2017) A phylogenetically-based nomenclature for Cordycipitaceae (Hypocreales). IMA Fungus 8:335–353
Leite LG, Batista Filho A, Oliveira SMC (1998) Infectividade do fungo Sporothrix insectorum, na forma de corpos hifais, contra o percevejo de renda da seringueira. In: Simpósio de controle biológico, 6, Rio de Janeiro. Resumos, pp138
Li Z, Alves SB, Roberts DW, Fan M, Delalibera I Jr, Tang J, Lopes RB, Faria M, Rangel DEN (2010) Biological control of insects in Brazil and China: history, current programs and reasons for their successes using entomopathogenic fungi. Biocontrol Sci Techn 20:117–136
Lim SY, Lee S, Kong HG, Lee J (2014) Entomopathogenicity of Simplicillium lanosoniveum isolated in Korea. Mycobiology 42:317–321
Liu YJ, Whelen S, Hall BD (1999) Phylogeentic relationships among Ascomycetes: evidence from an RNA polymerase II subunit. Mol Biol Evol 16:1799–1808
Luangsa-ard JJ, Hywel-Jones NL, Manoch L, Samson RA (2005) On the relationships of Paecilomyces sect. Isarioidea species. Mycol Res 109:581–589
Maddison WP, Maddison DR (2015) Mesquite: a modular system for evolutionary analysis. Version 3.04. http://mesquiteproject.org
Mascarin GM, Lopes RB, Delalibera I Jr, Fernandes EKK, Luz C, Faria M (2019) Current status and perspectives of fungal entomopathogens used for microbial control of arthropod pests in Brazil. J Invert Pathol 165:46–53
Michereff Filho M, Faria M, Wraight SP, Silva KFAS (2009) Micoinseticidas e micoacaricidas no Brasil: Como estamos após quatro décadas? Arq Inst Biol 76:769–779
Mongkolsamrit S, Noisripoom W, Thanakitpipattana D, Wutikhun T, Spatafora JW, Luangsa-ard J (2018) Disentangling cryptic species with isaria-like morphs in Cordycipitaceae. Mycologia 110:230–257
Moreira IPS (1986) Biologia da Leptopharsa heveae (Drake & Poor, 1935) e seus danos nas mudas de Heveae brasiliensis (Müell, 1932). Silvicultura 11:47
Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University
Ordonez-Giraldo AIDH (1993) Sporothrix insectorum: Mèthode biologique de contrôle de la punaise Leptopharsa gibbicarina dans les cultures du palmier du palmier à huile en Amèrique Latine (Hemiptera, Tingidae). B Soc Entomol Fr 98:77–85
Raeder J, Broda P (1985) Rapid preparation of DNA from filamentous fungi. Lett Appl Microbiol 1:17–20
Rangel DEN (2000) Virulência de Aphanocladium album e Verticillium lecanii (Deuteromycotina: Hyphomycetes) para o percevejo-de-renda da seringueira, Leptopharsa hevea (Hemiptera: Tingidae) e comportamento de V. lecanii em meio de cultura, Microbiologia. MSc Dissertation, Universidade Estadual Paulista, Jaboticabal (SP), p 70
Rangel DEN, Correia ACB (2003) Virulência de Aphanocladium album (Preuss) Gams e Verticillium lecanii (zimm.) Viégas (Deuteromycotina: Hyphomycetes) para o percevejo-de-renda da seringueira, Leptopharsa heveae (Drake & Poor) (Demiptera: Tingidae). Ciência e Agrotecnologia 27:1636–1642
Rehner SA, Buckley E (2005) A Beauveria phylogeny inferred from nuclear ITS and EF1-α sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia 97:84–98
Rehner SA, Minnis AM, Sung G-H, Luangsa-ard JJ, Devotto L, Humber RA (2011) Phylogeny and systematics of the anamorphic, entomopathogenic genus Beauveria. Mycologia 103:1055–1073
Ronquist F, Teslenko M, van der Mark P, Ayres D, Darling A, Hohna S, Larget B, Liu L, Huelsenbeck JP (2012) MrBayes v.3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542
Santos RS, da Silva JM (2013) Dinâmica populacional do parasitoide de ovos Erythmelus tingitiphagus (Hymenoptera: Mymaridae) em clone de seringueira, em Itiquira, MT. Revista Árvore 37:237–244
Schoch CL, Robbertse B, Robert V. et al. (2014) Finding needles in haystacks: linking scientific names, reference specimens and molecular data for Fungi. https://doi.org/10.1093/database/bau061
Schroeder S, Kim SH, Cheung WT, Sterflinger K, Breuil C (2001) Phylogenetic relationship of Ophiostoma piliferum to other sapstain fungi based on the nuclear rRNA gene. FEMS Microbiol Lett 195:163–167
Shimazu M, Alves RT, Kishino K (1994) Investigation on entomogenous fungi in the Cerrado region and their utilization for microbial control of pests. In: Centro de Pesquisa Agropecuária dos Cerrados (Planaltina, DF). Relatório técnico do projeto nipo-brasileiro de cooperação em pesquisa agrícola nos Cerrados 1987/1992. EMBRAPA, Planaltina, pp 202–214
Souza RKF, Azevedo RFF, Lobo AO, Rangel DEN (2014) Conidial water affinity is an important characteristic for thermotolerance in entomopathogenic fungi. Biocontrol Sci Techn 24:448–461
Spatafora JW, Sung G-H, Sung JM, Hywel-Jones NL, White JF Jr (2007) Phylogenetic evidence for an animal pathogen origin of ergot and the grass endophytes. Mol Ecol 16:1701–1711
Sterling A, Salas-Tobón YM, Virgüez-Díaz Y (2016) Erinnyis ello (Lepidoptera: Sphingidae) y Leptopharsa heveae (Hemiptera: Tingidae) en Hevea brasiliensis en sistema agroforestal. Rev Colomb Entomol 42:124–132
Stiller JW, Hall BD (1997) The origin of red algae: implications for plastid evolution. P Natl Acad Sci USA 94:4520–4525
Summerbell RC, Gueidan C, Schroers HJ, de Hoog GS, Starink M, Rosete YA, Guarro J, Scott JA (2011) Acremonium phylogenetic overview and revision of Gliomastix, Sarocladium, and Trichothecium. Stud Mycol 68:139–162
Sung G-H, Spatafora JW, Zare R, Hodge KT, Gams W (2001) A revision of Verticillium sect. Prostrata. II. Phylogenetic analyses of SSU and LSU nuclear rDNA sequences from anamorphs and teleomorphs of the Clavicipitaceae. Nova Hedwigia 72:311–328
Sung G-H, Hywel-Jones NL, Sung JM, Luangsa-Ard JJ, Shrestha B, Spatafora JW (2007) Phylogenetic classification of Cordyceps and the clavicipitaceous fungi. Stud Mycol 57:5–59
Tanzini MR (1996) Resistência de clones de seringueira [Hevea brasiliensis (Willd. Ex. Adr. de jus.) Muell. Arg.] a Leptopharsa heveae Drake & Poor, 1935 (Hemiptera: Tingidae) e sua biologia. MSc Dissertation, Universidade Estadual Paulista, Jaboticabal (SP), p 138
Tanzini MR (2002) Controle do percevejo-de-renda-da-seringueira (Leptopharsa heveae) com fungos entomopatogênicos. PhD. Thesis, Universidade de São Paulo (ESALQ), Piracicaba (SP), Brasil, p 140
Tanzini MR, Lara FM (1998) Biologia do percevejo-de-renda-da-seringueira Leptopharsa heveae Drake & Poor (Heteroptera: Tingidae). Ecossistema 23:65–67
Torres MS, White JF Jr, Bischoff JF (2005) Cordyceps spegazzinii sp. nov., a new species of the C. militaris group. Mycotaxon 94:253–263
Trifinopoulos J, Nguyen LT, von Haeseler A, Minh BQ (2016) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucl Acids Res 44(W1):W232–W235
Val AJ d (1994) Névoa Protetora: os fungos pulverizados nos seringais controlam a mosca-de-renda, uma praga nos cultivos do Mato Grosso. Revista Globo Rural, Rio de Janeiro, Março, pp 43–46
Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246
Vu D, Groenewald M, de Vries M, Gehrmann T, Stielow B, Eberhardt U, Al-Hatmi A, Groenewald JZ, Cardinali G, Houbraken J, Boekhout T, Crous PW, Robert V, Verkley GJM (2019) Large-scale generation and analysis of filamentous fungal DNA barcodes boosts coverage for kingdom fungi and reveals thresholds for fungal species and higher taxon delimitation. Stud Mycol 92:135–154
Ward NA, Schneider RW, Aime MC (2011) Colonization of soybean rust sori by Simplicillium lanosoniveum. Fungal Ecol 4:303–308
White TJ, Bruns TD, Lee SB, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322
Zancope-Oliveira RM, Almeida-Paes R, Oliveira MME, Freitas DFS, Gutierrez-Galhardo MC (2012) Outbreaks of sporotrichosis in humans and animals in Brazil. Mycoses 55:33–33
Zare R, Gams W (2001) A revision of Verticillium section Prostrata. IV. The genera Lecanicillium and Simplicillium gen. nov. Nova Hedwigia 73:1–50
Zare R, Gams W, Culham A (2000) A revision of Verticillium sect. Prostrata. I. Phylogenetic studies using ITS sequences. Nova Hedwigia 71:465–480
Zha L-S, Wen T-C, Huang S-K, Boonmee S, Eungwanichayapant PD (2019) Taxonomy and biology of Cordyceps qingchengensis sp. nov. and its allies. Phytotaxa 416:14–24
Zhou X, Rodrigues AM, Feng P, de Hoog GS (2014) Global ITS diversity in the Sporothrix schenckii complex. Fungal Divers 66:153–165
Zhou Y-M, Zhi J-R, Ye M, Zhang Z-Y, Yue W-B, Zou X (2018) Lecanicillium cauligalbarum sp. nov. (Cordycipitaceae, Hypocreales), a novel fungus isolated from a stemborer in the Yao Ren National Forest Mountain Park, Guizhou. MycoKeys 43:59–74
Zimmermann G (2008) The entomopathogenic fungi Isaria farinosa (formerly Paecilomyces farinosus) and the Isaria fumosorosea species complex (formerly Paecilomyces fumosoroseus): biology, ecology and use in biological control. Biocontrol Sci Tech 18:865–901
Acknowledgments
We are grateful to NTV Junqueira (EMBRAPA, Brazil), JEM Almeida and L.G. Leite (Instituto Biológico, Brazil), MB Santaella (EMPAER, Brazil), RT Alves (EMBRAPA, Brazil), I Delalibera (ESALQ, Brazil), DEN Rangel (Univ Brasil, Brazil), and LA Castrillo (USDA-ARS, USA) for information on L. heveae–associated isolates and/or relevant historical information.
Author information
Authors and Affiliations
Corresponding author
Additional information
Edited by Christian S Torres – UFRPE
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic Supplementary Material
Fig S1
Maximum likelihood (ML) phylogenetic tree generated from analysis of ITS sequences dataset. Sporothrix schenckii and Ophiostoma piliferum are the outgroup taxa. Ex-type strains are indicated with superscript T. Isolates obtained from Leptopharsa heveae (Hemiptera: Tingidae) are in bold. Support values above branches were given as the Bayesian prior probability and as the bootstrap proportions derived from ML analysis. (PDF 95 kb)
Fig S2
Maximum likelihood (ML) phylogenetic tree generated from analysis of LSU sequences dataset. Sporothrix schenckii and Ophiostoma piliferum are the outgroup taxa. Ex-type strains are indicated with superscript T. Isolates obtained from Leptopharsa heveae (Hemiptera: Tingidae) are in bold. Support values above branches were given as the Bayesian prior probability and as the bootstrap proportions derived from ML analysis. (PDF 97 kb)
Fig S3
Maximum likelihood (ML) phylogenetic tree generated from analysis of SSU sequences dataset. Ophiostoma piliferum is the outgroup taxa. Ex-type strains are indicated with superscript T. Isolates obtained from Leptopharsa heveae (Hemiptera: Tingidae) are in bold. Support values above branches were given as the Bayesian prior probability and as the bootstrap proportions derived from ML analysis. (PDF 101 kb)
Fig S4
Maximum likelihood (ML) phylogenetic tree generated from analysis of TEF sequences dataset. Sporothrix sp. is the outgroup taxa. Ex-type strains are indicated with superscript T. Isolates obtained from Leptopharsa heveae (Hemiptera: Tingidae) are in bold. Support values above branches were given as the Bayesian prior probability and as the bootstrap proportions derived from ML analysis. (PDF 94 kb)
Fig S5
Maximum likelihood (ML) phylogenetic tree generated from analysis of ITS sequences dataset. Beauveria bassiana is the outgroup taxon. Ex-type strains are indicated with superscript T. Isolates obtained from Leptopharsa heveae (Hemiptera: Tingidae) are in bold. Support values above branches were given as the Bayesian prior probability and as the bootstrap proportions derived from ML analysis. (PDF 323 kb)
Fig S6
Maximum likelihood (ML) phylogenetic tree generated from analysis of LSU sequences dataset. Beauveria bassiana is the outgroup taxon. Ex-type strains are indicated with superscript T. Isolates obtained from Leptopharsa heveae (Hemiptera: Tingidae) are in bold. Support values above branches were given as the Bayesian prior probability and as the bootstrap proportions derived from ML analysis. (PDF 101 kb)
Fig S7
Maximum likelihood (ML) phylogenetic tree generated from analysis of RPB1 sequences dataset. Beauveria bassiana is the outgroup taxon. Ex-type strains are indicated with superscript T. Isolates obtained from Leptopharsa heveae (Hemiptera: Tingidae) are in bold. Support values above branches were given as the Bayesian prior probability and as the bootstrap proportions derived from ML analysis. (PDF 96 kb)
Fig S8
Maximum likelihood (ML) phylogenetic tree generated from analysis of RPB2 sequences dataset. Beauveria bassiana is the outgroup taxon. Ex-type strains are indicated with superscript T. Isolates obtained from Leptopharsa heveae (Hemiptera: Tingidae) are in bold. Support values above branches were given as the Bayesian prior probability and as the bootstrap proportions derived from ML analysis. (PDF 86 kb)
Fig S9
Maximum likelihood (ML) phylogenetic tree generated from analysis of TEF sequences dataset. Beauveria bassiana is the outgroup taxon. Ex-type strains are indicated with superscript T. Isolates obtained from Leptopharsa heveae (Hemiptera: Tingidae) are in bold. Support values above branches were given as the Bayesian prior probability and as the bootstrap proportions derived from ML analysis. (PDF 99 kb)
Rights and permissions
About this article
Cite this article
Faria, M., de Souza, D.A. & Lopes, R.B. Microbial Control of Leptopharsa heveae Drake & Poor (Hemiptera: Tingidae) in Brazilian Rubber Tree Plantations: a Brief Historical Account and Identification of Entomopathogenic Fungi by Means of Multigene Phylogeny. Neotrop Entomol 49, 864–873 (2020). https://doi.org/10.1007/s13744-020-00808-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13744-020-00808-4