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The role of native vegetation on infection rates of Calacarus heveae (Acari: Eriophyidae) by Hirsutella thompsonii (Ascomycota: Ophiocordycipitaceae)

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Abstract

Hirsutella thompsonii (Fischer) (Ascomycota: Ophiocordycipitaceae), a fungal pathogen, often causes high mortality in populations of Calacarus heveae Feres (Acari: Eriophyidae), an important pest mite in rubber tree plantations (Hevea brasiliensis Muell. Arg., Euphorbiaceae). However, the ecological and climatic factors regulating this host-pathogen system are poorly known. We compared fungal infections in agroforestry and traditional rubber plantations to evaluate the role of native vegetation and climatic factors on infection rates of C. heveae by H. thompsonii. While the prevalence of H. thompsonii was higher in managed rubber tree plantations, the abundance of C. heveae was about three times higher in traditional plantations. Abundance of C. heveae, agroecosystem management type and microclimatic variables were responsible for driving the infection rates of H. thompsonii. Native vegetation was a source for H. thompsonii and also modified the crop’s microclimate, which contributed to its maintenance in the crop fields. Therefore, appropriate management practices may enhance the effects of entomopathogens on conservative biological control of pest mites in agroforestry systems.

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References

  • Ab’Saber AN (2003) Os domínios de natureza no Brasil: potencialidades paisagísticas. Ateliê Editorial, São Paulo

    Google Scholar 

  • Altieri MA, Nicholls CI (2004) Effects of agroforestry systems on the ecology and management of insect pest populations. In: Gurr GM, Wratten SD, Altieri MA (eds) ecological engineering for pest management advances in habitat manipulation for arthropods. Csiro Publishing, Collingwood, pp 143–154

    Google Scholar 

  • Bates D, Maechler M, Bolker B (2011) lme4: linear mixed-effects models using S4 classes. R package version 0.999375-39. http://CRAN.R-project.org/package=lme4. Accessed 15 Oct 2012

  • Baverstock J, Clark SJ, Pell JK (2008) Effect of seasonal abiotic conditions and field margin habitat on the activity of Pandora neoaphidis inoculum on soil. J Invertebr Pathol 97:282–290

    Article  CAS  PubMed  Google Scholar 

  • Bitton G, Davidson JM, Farrah SR (1979) On the value of soil columns for assessing the transport pattern of viruses through soils: a critical outlook. Water Air Soil Pollut 12:449–457

    Article  Google Scholar 

  • Bolker BM (2008) Ecological models and data in R. Princeton University Press, Princeton

    Google Scholar 

  • Braga GUL, Flint SD, Miller CD, Anderson AJ, Roberts DW (2001) Both solar UVA and UVB radiation impair conidial culturability and delay germination in the entomopathogenic fungus Metarhizium anisopliae. Photochem Photobiol 74:734–739

    Article  CAS  PubMed  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multi-model inference, 2nd edn. Springer, New York

    Google Scholar 

  • Castro EB, Nuvoloni FM, Mattos CRR, Feres RJF (2013) Population fluctuation and damage caused by phytophagous mites on three rubber tree clones. Neotrop Entomol 42:95–101

    Article  CAS  PubMed  Google Scholar 

  • Crawley MJ (2002) Statistical computing: an introduction to data analysis using S-plus. Wiley, New York

    Google Scholar 

  • Daud RD, Feres RJF, Hernandes FA (2012) Seasonal suitability of three rubber tree clones to Calacarus heveae (Acari, Eriophyidae). Exp Appl Acarol 56:57–68

    Article  PubMed  Google Scholar 

  • Demite PR, Feres RJF (2008) Influência de fragmentos de cerrado na distribuição de ácaros em seringal. Neotrop Entomol 37:196–204

    Article  PubMed  Google Scholar 

  • Fargues J, Goettel MS, Smits N, Ouedraogo A, Vidal C, Lacey LA, Lomer CJ, Rougier M (1996) Variability in susceptibility to simulated sunlight of conidia among isolates of entomopathogenic Hyphomycetes. Mycopathologia 135:171–181

    Article  CAS  PubMed  Google Scholar 

  • Feres RJF (2000) Levantamento e observações naturalísticas da acarofauna (Acari, Arachnida) de seringueiras cultivadas (Hevea spp., Euphorbiaceae) no Brasil. Rev Bras Zool 17:157–173. doi:10.1590/S0101-81752000000100011

    Article  Google Scholar 

  • Fisher PE, Griffiths JT, Thompson WL (1949) An epizootic of Phyllocoptruta oleivora (Ashmead) on citrus in Florida. Phytopathology 39:510–512

    Google Scholar 

  • Fuxa JR (1998) Environmental manipulation for microbial control of insects. In: Barbosa P (ed) Conservation biological control. Academic Press, San Diego, pp 255–289

    Chapter  Google Scholar 

  • Gameiro AH, Gameiro MBP (2008) Perspectivas para o mercado internacional de borracha natural. In: Alvarenga PA, Carmo CAFS (eds) Seringueira. EPAMIG, Viçosa, pp 855–878

    Google Scholar 

  • Gerson U, Kenneth R, Muttath TI (1979) Hirsutella thompsonii a fungal pathogen of mites. II. Host-pathogen interactions. Ann Appl Biol 91:29–40

    Article  Google Scholar 

  • Gliessman SR (1999) Agroecology: ecological processes in agriculture. Ann Arbor Press, Michigan

    Google Scholar 

  • Greif MD, Currah RS (2007) Patterns in the occurrence of saprophytic fungi carried by arthropods caught in traps baited with rotted wood and dung. Mycologia 99:7–19

    Article  CAS  PubMed  Google Scholar 

  • Gurr GM, Wratten SD, Luna JM (2003) Multi-function agricultural biodiversity: pest management and other benefits. Basic Appl Ecol 4:107–116

    Article  Google Scholar 

  • Hajek AE (1999) Pathology and epizootiology of Entomophaga maimaiga infections in forest Lepidoptera. Microbiol Mol Biol Rev 63:814–835

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hernandes FA, Feres RJF (2006) Diversidade e sazonalidade de ácaros (Acari) em seringal (Hevea brasiliensis Muell. Arg.) no noroeste do estado de São Paulo. Neotrop Entomol 35:523–535

    Article  PubMed  Google Scholar 

  • Hesketh H, Roy HE, Eilenberg J, Pell JK, Hails RS (2010) Challenges in modelling complexity of fungal entomopathogens in semi-natural populations of insects. Biocontrol 55:55–73

    Article  Google Scholar 

  • Hochberg ME (1989) The potential role of pathogens in biological control. Nature 337:262–265

    Article  CAS  PubMed  Google Scholar 

  • Inglis GD, Goettel MS, Johnson DL (1995) Influence of ultraviolet light protectants on persistence of the entomopathogenic fungus, Beauveria bassiana. Biol Control 5:581–590

    Article  Google Scholar 

  • Jaronski ST (2010) Ecological factors in the inundative use of fungal entomopathogens. Biocontrol 55:159–185. doi:10.1007/s10526-009-9248-3

    Article  Google Scholar 

  • Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19:101–108

    Article  PubMed  Google Scholar 

  • Johnson PTJ, Longcore JE, Stanton DE, Carnegie RB (2006) Chytrid infections of Daphnia pulicaria: development, ecology, pathology and phylogeny of Polycaryum leave. Freshwater Biol 51:634–648

    Article  Google Scholar 

  • Kaya HK, Tanada Y (1993) Insect pathology. Academic Press, San Diego

    Google Scholar 

  • Kennedy AC (1998) Microbial diversity in agroecosystem quality. In: Collins W, Qualset C (eds) Biodiversity in agroecosystems. CRC Press, London

    Google Scholar 

  • Kenneth R, Muttath TI, Gerson U (1979) Hirsutella thompsonii, a fungal pathogen of mites. I. Biology of the fungus in vitro. Ann Appl Biol 91:21–28

    Article  Google Scholar 

  • McCoy CW (1996) Pathogens of eriophyoid mite. In: Lindquist EE, Sabelis MW, Bruin J (eds) Eriophyoid mites—their biology, natural enemies and control, word crop pests series, vol 6. Elsevier Science Publishers, Amsterdam, pp 481–490

    Chapter  Google Scholar 

  • McCulloch CE, Searle SR (2001) Generalized, linear, and mixed models. Wiley, New York

    Google Scholar 

  • Moraes GJ, Flechtmann CHW (2008) Manual de acarologia, acarologia básica e ácaros de plantas cultivadas no Brasil. Editora Holos, Ribeirão Preto

    Google Scholar 

  • Oliveira-Filho AT, Fontes MAL (2000) Patterns of floristic differentiation among Atlantic forests in southeatern Brazil and the influence of climate. Biotropica 32:793–810

    Article  Google Scholar 

  • Pell JK (2007) Ecological approaches to pest management using entomopathogenic fungi; concepts, theory, practice and opportunities. In: Ekesi S, Manianai N (eds) Use of entomopathogenic fungi in pest management. Research Signpost, Trivandrum, pp 145–177

    Google Scholar 

  • Poinar G Jr, Poinar R (1998) Parasites and pathogens of mites. Annu Rev Entomol 43:449–469

    Article  CAS  PubMed  Google Scholar 

  • Powell W, Dean GJ, Wilding N (1986) The influence of weeds on aphid-specific natural enemies in winter wheat. Crop Prot 5:182–189

    Article  Google Scholar 

  • Quesada-Moraga E, Martin-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

    Article  Google Scholar 

  • R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rand TA, Tylianakis JM, Tscharntke T (2006) Spillover edge effects: the dispersal of agriculturally subsidized insect natural enemies into adjacent natural habitats. Ecol Lett 9:603–614

    Article  PubMed  Google Scholar 

  • Reay SD, Hachet C, Nelson TL, Brownbridge M, Glare TR (2007) Persistence of conidia and potential efficacy of Beauveria bassiana against pinhole borers in New Zealand southern beech forests. For Ecol Manag 246:232–239

    Article  Google Scholar 

  • Roberts DW, Campbell AS (1977) Stability of entomopathogenic fungi. Misc Publ Ent Soc Amer 10:19–76

    Google Scholar 

  • Shah PA, Clark SJ, Pell JK (2004) Assessment of aphid host susceptibility and isolate variability in Pandora neoaphidis (Zygomycota: Entomophthorales). Biol Control 29:90–99

    Article  Google Scholar 

  • Shapiro SS, Wilk MB (1965) An analysis variance tests for normality (complete samples). Biometrika 52:591–611

    Article  Google Scholar 

  • Steinhaus EA (1954) The effects of disease on insect populations. Hilgardia 23:197–261

    Google Scholar 

  • Steinkraus DC (2006) Factors affecting transmission of fungal pathogens of aphids. J Invertebr Pathol 92:125–131. doi:10.1016/j.jip.2006.03.009

    Article  PubMed  Google Scholar 

  • Steinkraus DC, Hollingsworth RG, Boys GO (1996) Aerial spores of Neozygites fresenii (Entomophthorales: Neozygitaceae): density, periodicity, and potential role in cotton aphid (Homoptera: Aphididae) epizootics. Environ Entomol 25:48–57

    Google Scholar 

  • Tanzini MR, Alves SB, Tamai MA, Moraes GJ, Ferla NJ (2000) An epizootic of Calacarus heveae (Acari: Eriophyidae) caused by Hirsutella thompsonii on rubber trees. Exp Appl Acarol 24:141–144. doi:10.1023/A:1006303419987

    Article  CAS  PubMed  Google Scholar 

  • Thomas MB, Wood SN, Lomer CJ (1995) Biological control of locusts and grasshoppers using a fungal pathogen: the importance of secondary cycling. Proc R Soc Lond B 259:265–270. doi:10.1098/rspb 1995.0039

    Article  Google Scholar 

  • Thomas WM, Carvalho AMV, Amorim AMA, Garrison J, Arbeláez AL (1998) Plant endemism in two forests in southern Bahia, Brazil. Biodiver Conserv 7:311–322

    Article  Google Scholar 

  • Van der Geest LP, Elliot SL, Breeuwer JAJ, Beerling EAM (2000) Diseases of mites. Exp Appl Acarol 24:497–560

    Article  PubMed  Google Scholar 

  • Vega FE, Dowd PF, Lacey LA, Pell JK, Jackson DM, Klein MG (2007) Dissemination of beneficial microbial agents by insects. In: Lacey LA, Kaya HK (eds) Field manual of techniques in invertebrate pathology: application and evaluation of pathogens for control of insects and other invertebrate pests, 2nd edn. Springer, Dordrecht, pp 127–146

    Chapter  Google Scholar 

  • Vega FE, Goettel MS, Blackwell M, Jackson MA, Keller S, Koike M, Maniania NK, Monzo′n A, Ownley B, Pell JK, Rangel D, Roy HE (2009) Fungal entomopathogens: new insights on their ecology. Fungal Ecol 2:149–159. doi:10.1016/j.funeco.2009.05.001

    Article  Google Scholar 

  • Vieira MR, Gomes EC, Silva HAS da (2010) Redução na produção de látex da seringueira provocada pela infestação de ácaros. Rev Ceres 57:608–613

    Google Scholar 

  • Weseloh RM (2003) Short and long range dispersal in the gypsy moth (Lepidoptera: Lymantriidae) fungal pathogen, Entomophaga maimaiga (Zygomycetes: Entomophthorales). Environ Entomol 32:111–122

    Google Scholar 

  • Zuur A, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

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Acknowledgments

We would like to thank Carlos R.R. Mattos, Saulo E.A. Cardoso and José F.A. Neto for providing logistical support during data collection. Dr. Fernando Rodrigues da Silva (Departamento de Ciências Ambientais—UFSCar) provided valuable help with the statistical analysis. The staff of the Departamento de Pesquisa e Desenvolvimento of the PMB provided workspace. The Plantações Michelin da Bahia Ltda. (Igrapiúna, BA) and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP Process. 2010/19935-1) for funding the study. This work was partially supported by CAPES, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brazil and “Conselho Nacional de Desenvolvimento Científico e Tecnológico” (CNPq) (Proc. No 303049/2010-3), by fellowship and research grant to second and third authors.

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  1. Programa de Pós-Graduação em Biologia Animal, UNESP, Rua Cristóvão Colombo, 2265, Jardim Nazareth, São José do Rio Preto, SP, 15054-000, Brazil

    Felipe Micali Nuvoloni & Elizeu Barbosa de Castro

  2. Departamento de Zoologia e Botânica, UNESP, Rua Cristóvão Colombo, 2265, Jardim Nazareth, São José do Rio Preto, SP, 15054-000, Brazil

    Reinaldo José Fazzio Feres

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  1. Felipe Micali Nuvoloni
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  2. Elizeu Barbosa de Castro
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  3. Reinaldo José Fazzio Feres
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Correspondence to Felipe Micali Nuvoloni.

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Nuvoloni, F.M., de Castro, E.B. & Feres, R.J.F. The role of native vegetation on infection rates of Calacarus heveae (Acari: Eriophyidae) by Hirsutella thompsonii (Ascomycota: Ophiocordycipitaceae). Exp Appl Acarol 63, 157–169 (2014). https://doi.org/10.1007/s10493-014-9771-5

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