Skip to main content
SpringerLink
Log in

Population growth of the stored product pest Tyrophagus putrescentiae (Acari: Acaridae) on environmentally and medically important fungi

  • Published:
Experimental and Applied Acarology Aims and scope Submit manuscript

Abstract

The stored food mite Tyrophagus putrescentiae (Schrank) (Acari: Acaridae) has been associated with the presence of several fungal species. The aims of this work were to evaluate T. putrescentiae population growth associated to environmental and medically important fungal species to determine on which fungal species populations of T. putrescentiae performs best, and to evaluate their ability to disperse each fungal species. First, 24 fungal species were inoculated separately in Petri dishes containing Sabouraud agar medium. One week after inoculation, 50 mites were added to each plate. On the 28th evaluation day, mites and eggs were counted in each plate, and 50 mites randomly collected from each replicate were transferred to new plates containing only Sabouraud agar medium. Then, mites, eggs, and fungal population were evaluated in each plate on day 28 again. The highest population increases were on Trichophyton mentagrophytes, Alternaria sp., Microsporum gypseum, and Aspergillus chevalieri. With Fusarium guttiforme and the medically important fungi Microsporum canis, M. gypseum, T. mentagrophytes, and Sporothrix sp., mites were observed to feed on whole mycelium. Only eight fungal species were dispersed by T. putrescentiae to the new Petri dishes: Aspergillus clavatus, Candida tropicalis, Candida albicans, Fusarium guttiforme, Hyphopichia burtonii, Penicillium citrinum, Rhizophus azygosporus, and Trichophyton mentagrophytes. The best performance of T. putrescentiae was found feeding on F. guttiforme, P. citrinum, and T. mentagrophytes. In conclusion, T. putrescentiae successfully used fungi as a food source, and it proved to be an important tool for disseminating both environmental and medically important fungi.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Anagnostou C, Dorsch M, Rohlfs M (2010) Influence of dietary yeasts on Drosophila melanogaster life-history traits. Entomol Exp Appl 136:1–11

    Article  Google Scholar 

  • Arlian L, Geis D, Vyszenski-Moher D, Bernstein I, Gallagher J (1984) Antigenic and allergenic properties of the storage mite Tyrophagus putrescentiae. J Allergy Clin Immunol 74:166–171

    Article  CAS  PubMed  Google Scholar 

  • Armitage DM, George CL (1986) The effect of three species of mites upon fungal growth on wheat. Exp Appl Acarol 2:111–124

    Article  CAS  PubMed  Google Scholar 

  • Ayres M, Ayres Júnior M, Ayres DL, Santos AS (2007) BioEstat 5.0: aplicações estatísticas nas áreas das ciências biológicas e médicas. Belém: MCT; IDSM; CNPq

  • Botha CJ, Truter M, Sulyok M (2018) Multimycotoxin analysis of South African Aspergillus clavatus isolates. Mycotoxin Res 34:91–97

    Article  CAS  PubMed  Google Scholar 

  • Bottalico A, Perrone G (2002) Toxigenic Fusarium species and mycotoxins associated with head blight in small-grain cereals in Europe. Eur J Plant Pathol 108:611–624

    Article  CAS  Google Scholar 

  • Colloff MJ (2009) Dust mites. CSIRO Publishing, Springer, Collingwood, Dordrecht

    Book  Google Scholar 

  • Deschuyffeleer N, Audenaert K, Samapundo S, Ameye S, Eeckhout M, Devlieghere F (2011) Identification and characterization of yeasts causing chalk mould defects on par-baked bread. Food Microbiol 28:1019–1027

    Article  CAS  PubMed  Google Scholar 

  • Dobrosavljevic DD, Popovic ND, Radovanovic SS (2007) Systemic manifestations of Cheyletiella infestation in man. Int J Dermatol 46:397–399

    Article  PubMed  Google Scholar 

  • Druzhinina IS, Komoń-Zelazowska M, Kredics L, Hatvani L, Antal Z, Belayneh T, Kubicek CP (2008) Alternative reproductive strategies of Hypocrea orientalis and genetically close but clonal Trichoderma longibrachiatum, both capable of causing invasive mycoses of humans. Microbiology 154:3447–3459

    Article  CAS  PubMed  Google Scholar 

  • Duek L, Kaufman G, Palevsky E, Berdicevsky I (2001) Mites in fungal cultures. Mycoses 44:390–394

    Article  CAS  PubMed  Google Scholar 

  • Erban T, Hubert J (2008) Digestive function of lysozyme in synanthropic acaridid mites enables utilization of bacteria as a food source. Exp Appl Acarol 44:199–212

    Article  CAS  PubMed  Google Scholar 

  • Erban T, Klimov PB, Smrž J, Phillips TW, Nesvorna M, Kopecky J, Hubert J (2016) Populations of stored product mite Tyrophagus putrescentiae differ in their bacterial communities. Front Microbiol 7:1046

    Article  PubMed  PubMed Central  Google Scholar 

  • Franz J-T, Masuch G, Musken H, Bergmann K-C (1997) Mite fauna of German farms. Allergy 52:1233–1237

    Article  CAS  PubMed  Google Scholar 

  • Franzolin MR, Gambale W, Cuero RG, Correa B (1999) Interaction between toxigenic Aspergillus flavus Link and mites (Tyrophagus putrescentiae Schrank) on maize grains: effect on fungal growth and aflatoxin production. J Stored Prod Res 35:215–224

    Article  Google Scholar 

  • Frisvad JC, Smedsgaard J, Larsen TO, Samson RA (2004) Mycotoxins, drugs and other extrolites produced by species in Penicillium subgenus Penicillium. Stud Mycol 49:201–241

    Google Scholar 

  • Glass NL, Donaldson GC (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol 61:1323–1330

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gow NAR, Latge JP, Munro CA (2017) The fungal cell wall: structure, biosynthesis, and function. Microbiol Spectr. https://doi.org/10.1128/microbiolspec

    Article  PubMed  Google Scholar 

  • Griffiths DA, Hodson AC, Christensen CM (1959) Grain storage fungi associated with mites. J Econ Entomol 52:514–518

    Article  Google Scholar 

  • Hillmann F, Novohradská S, Forberger T, Heinekamp T, Westermann M, Winckler T, Brakhage AA (2015) Virulence determinants of the human pathogenic fungus Aspergillus fumigatus protect against soil amoeba predation. Environ Microbiol 17:2858–2869

    Article  CAS  PubMed  Google Scholar 

  • Hubert J, Stejskal V, Kubátová A, Munzbergová Z, Vánová M, Zd’árková E (2003) Mites as selective fungal carriers in stored grain habitats. Exp Appl Acarol 29:69–87

    Article  PubMed  Google Scholar 

  • Hubert J, Jarosik V, Mourek J, Kubatova A, Zdarkova E (2004) Astigmatid mite growth and fungi preference (Acari: Acaridida): comparisons in laboratory experiments. Pedobiologia 48:205–214

    Article  Google Scholar 

  • Hubert J, Nesvorná M, Ságová-Marečková M, Kopecký J (2012) Shift of bacterial community in synanthropic mite Tyrophagus putrescentiae induced by Fusarium fungal diet. PLoS ONE 7:e48429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hubert J, Nesvorná M, Kopecký J (2014) The effect of Tyrophagus putrescentiae on Fusarium poae transmission and fungal community in stored barley in a laboratory experiment. Insect Sci 21:65–73

    Article  CAS  PubMed  Google Scholar 

  • Katoh Y, Kuninaka A, Yoshino H, Takatsuki A, Yamasaki M, Tamura G (1978) Scanning electron microscopy of giant cells of Penicillium citrinum. J Gen Appl Microbiol 24:233–240

    Article  Google Scholar 

  • Kheradmand K, Kamali K, Fathipour Y, Goltapeh EM (2007) Development, life table and thermal requirement of Tyrophagus putrescentiae (Astigmata: Acaridae) on mushrooms. J Stored Prod Res 43:276–281

    Article  Google Scholar 

  • Kopecky J, Nesvorná M, Mareckova-Sagova M, Hubert J (2014) The effect of antibiotics on associated bacterial community of stored product mites. PLoS ONE 9:e112919

    Article  PubMed  PubMed Central  Google Scholar 

  • Kucerova Z, Horak P (2004) Arthropod infestation in samples of stored seeds in the Czech Republic. Czech J Genet Plant Breed 40:11–16

    Article  Google Scholar 

  • Maraun M, Martens H, Migge S, Theenhaus S, Scheu S (2003) Adding to “the enigma of soil animal diversity”: fungal feeders and saprophagous soil invertebrates prefer similar food substrates. Eur J Soil Biol 39:85–95

    Article  Google Scholar 

  • Matsumoto T, Hisano T, Hamaguchi M, Miike T (1996) Systemic anaphylaxis after eating storage-mite-contaminated food. Int Arch Allergy Immunol 109:197–200

    Article  CAS  PubMed  Google Scholar 

  • Mediavilla A, Angulo J, Rodero JM, Dominguez E, Galán C, Infante F (1996) Fungal contamination of potential medical interest in Spanish grain stores. J Invest Allergol Clin Immunol 6:196–201

    Google Scholar 

  • Mohapatra D, Kumar S, Kotwaliwale N, Singh KK (2017) Critical factors responsible for fungi growth in stored food grains and non-chemical approaches for their control. Ind Crops Prod 108:162–182

    Article  Google Scholar 

  • Mullen GR, O’Connor BM (2009) Mites. In: Mullen GR, Durden L (eds) Medical and veterinary entomology, 2nd edn. Academic Press, London, pp 423–482

    Google Scholar 

  • Naidu J, Singh SM (1994) Aspergillus chevalieri (Mangin) Thom and Church: a new opportunistic pathogen of human cutaneous aspergillosis. Mycoses 37:271–274

    Article  CAS  PubMed  Google Scholar 

  • Nesvorná M, Gabrielova L, Hubert J (2012) Suitability of a range of Fusarium species to sustain populations of three stored product mite species (Acari: Astigmata). J Stored Prod Res 48:37–45

    Article  Google Scholar 

  • Novohradská S, Ferling I, Hillmann F (2017) Exploring virulence determinants of filamentous fungal pathogens through interactions with soil amoebae. Front Cell Infect Microbiol 7:497

    Article  PubMed  PubMed Central  Google Scholar 

  • Nuñez NK, da Cunha AA, dos Santos Dutra M, Barbosa GL, Morassutti AL, de Souza RG, Vargas MHM, Antunes GL, Silveira JS, Silva GL, Pitrez PM (2016) Acute and chronic exposure to Tyrophagus putrescentiae induces allergic pulmonary response in a murine model. Asia Pac Allergy 6:48–55

    Article  PubMed  PubMed Central  Google Scholar 

  • O’Connor BM (1982) Evolutionary ecology of astigmatid mites. Annu Rev Entomol 27:385–409

    Article  Google Scholar 

  • Osborne LE, Stein JM (2007) Epidemiology of Fusarium head blight on small-grain cereals. Int J Food Microbiol 119:103–108

    Article  PubMed  Google Scholar 

  • Ottonelli CDS, Magagnin CM, Castrillón MR, Mendes SD, Heidrich D, Valente P, Scroferneker ML (2014) Antifungal susceptibilities and identification of species of the Sporothrix schenckii complex isolated in Brazil. Med Mycol 52:56–64

    Google Scholar 

  • Pankiewicz-Nowicka D, Boczek J, Davis R (1984) Food selection in Tyrophagus putrescentiae (Schrank) (Acaria: Acarididae). J Georgia Entomol Soc 19:317–321

    Google Scholar 

  • Ploetz RC (2006) Fusarium-induced diseases of tropical, perennial crops. Phytopathology 96:648–652

    Article  PubMed  Google Scholar 

  • Racovitza A (1969) The influence of various moulds on the multiplication of some mycophagous mites. J Gen Microbiol 57:379–381

    Article  CAS  PubMed  Google Scholar 

  • Rajkowska K, Kunicka-Styczyńska A (2018) Typing and virulence factors of food-borne Candida spp. isolates. Int J Food Microbiol 279:57–63

    Article  PubMed  Google Scholar 

  • Reuter M, Bell G, Greig D (2007) Increased outbreeding in yeast in response to dispersal by an insect vector. Curr Biol 17:81–83

    Article  Google Scholar 

  • Ribes JA, Vonover-Sams CL, Baker DJ (2000) Zygomycetes in human disease. Clin Microbiol Rev 13:236–301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodrigues JG, Potts MF, Patterson CG (1984) Mycotoxin-producing fungi: effects on stored product mites. In: Griffths DA, Bowman CE (eds) Proceedings of 6th international congress of acarology, Chichester, vol. 1. pp 343–350

  • Rosa CAR (1986) Perfil bioquímico e sérico de suínos intoxicados experimentalmente com citrinina. Rio de Janeiro, Dissertação de Mestrado. Instituto de Veterinária da Universidade Federal Rural do Rio de Janeiro

  • Rybanska D, Hubert J, Markovic M, Erban T (2016) Dry dog food integrity and mite strain influence the density-dependent growth of the stored-product mite Tyrophagus putrescentiae (Acari: Acaridida). J Econ Entomol 109:454–460

    Article  CAS  PubMed  Google Scholar 

  • Samson RA, Seifert KA, Kuijpers AFA, Houbraken JAMP, Frisvad JC (2004) Phylogenetic analysis of Penicillium subgenus Penicillium using partial β-tubulin sequences. Stud Mycol 49:175–200

    Google Scholar 

  • Samson RA, Visagie CM, Houbraken J, Hong SB, Hubka V, Klaassen CH, Perrone G, Seifert KA, Susca A, Tanney JB, Varga J, Kocsubé S, Szigeti G, Yaguchi T, Frisvad JC (2014) Phylogeny, identification and nomenclature of the genus Aspergillus. Stud Mycol 78:141–173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silva GL, Esswein IZ, Radaelli TFS, Rocha MS, Ferla NJ, Silva OS (2018) Influence of various diets on development, life table parameters and choice oviposition test of Tyrophagus putrescentiae (Acari: Acaridae): an illustration using scanning electron microscopy (SEM). J Stored Prod Res 76:77–84

    Article  Google Scholar 

  • Sinha RN (1966) Feeding and reproduction of some stored-product mites on seed-borne fungi. J Econom Entomol 59:1227–1232

    Article  Google Scholar 

  • Smrž J (2003) Microanatomical and biological aspects of bacterial associations in Tyrophagus putrescentiae (Acari: Acaridida). Exp Appl Acarol 31:105–113

    Article  PubMed  Google Scholar 

  • Smrž J, Čatská V (2010) Mycophagous mites and their internal associated bacteria cooperate to digest chitin in soil. Symbiosis 52:33–40

    Article  Google Scholar 

  • Smrž J, Svobodová J, Čatská V (1991) Synergetic participation Tyrophagus putrescentiae (Schrank) (Acari, Acaridida) and its associated bacteria on the destruction of some soil micromycetes. J Appl Entomol 111:206–210

    Article  Google Scholar 

  • Smrž J, Soukalová H, Čatská V, Hubert J (2016) Feeding patterns of Tyrophagus putrescentiae (Sarcoptiformes: Acaridae) indicate that mycophagy is not a single and homogeneous category of nutritional biology. J Insect Sci 16:94

    Article  PubMed  PubMed Central  Google Scholar 

  • Solarz K, Senczuk L, Maniurka H, Cichecka E, Peszke M (2007) Comparisons of the allergenic mite prevalence in dwelling sand certain outdoor environments of the Upper Silesia (southwest Poland). Int J Hyg Environ Health 210:715–724

    Article  PubMed  Google Scholar 

  • Stejskal V, Hubert J (2008) Risk of occupational allergy to stored grain arthropods and false pest-risk perception in Czech grain stores. Ann Agric Environ Med 15:29–35

    PubMed  Google Scholar 

  • Takeuchi A, Shimizu-Ibuka A, Nishiyama Y, Mura K, Okada S, Tokue C, Arai S (2006) Purification and characterization of an α-amylase of Pichia burtonii Isolated from the traditional starter “Murcha” in Nepal. Biosci Biotechnol Biochem 70:3019–3024

    Article  CAS  PubMed  Google Scholar 

  • Theron-De Bruin N, Dreyer LL, Ueckermann EA, Wingfield MJ, Roets F (2018) Birds mediate a fungus-mite mutualism. Microb Ecol 75(4):863–874

    Article  PubMed  Google Scholar 

  • Vanhaelen M, Vanhaelen-Fastré R, Geeraerts J (1980) Occurrence in mushrooms (Homobasidiomycetes) of cis and trans-octa-1,5-dien-3-ol, attractants to the cheese mite Tyrophagus putrescentiae (Schrank) (Acarina, Acaridae). Experentia 36:406

    Article  CAS  Google Scholar 

  • Varga J, Rigó K, Molnár J, Tóth B, Szencz S, Téren J, Kozakiewicz Z (2003) Mycotoxin production and evolutionary relationships among species of Aspergillus section Clavati. Antonie Van Leeuwenhoek 83:191–200

    Article  CAS  PubMed  Google Scholar 

  • Walsh TJ, Dixon DM (1996) Chapter 75: spectrum of mycoses. In: Baron S (ed) Medical microbiology, 4th edn. University of Texas Medical Branch at Galveston, Galveston, TX

    Google Scholar 

  • Watanabe M, Yonezawa T, Lee K, Kumagai S, Sugita-Konishi Y, Goto K, Hara-Kudo Y (2011) Molecular phylogeny of the higher and lower taxonomy of the Fusarium genus and differences in the evolutionary histories of multiple genes. BMC Evol Biol 11:322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White TJ, Bruns T, Lee S, 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 Inc., New York, pp 315–322

    Google Scholar 

Download references

Acknowledgements

The authors thank Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES-Brazil) and Universidade Federal do Rio Grande do Sul (UFRGS) for the doctoral scholarship granted to the first author. We are grateful to UNIVATES—Universidade do Vale do Taquari for the opportunity to carry out the practical part of this study. Noeli Juarez Ferla, Patricia Valente and Maria Lúcia Scroferneker are supported by a CNPq productivity research scholarship.

Author information

Authors and Affiliations

  1. Laboratório de Acarologia Tecnovates, Univates – Universidade do Vale do Taquari, Lajeado, RS, 95914-014, Brazil

    Guilherme Liberato da Silva, Isadora Zanatta Esswein, Fabíola Dresch, Mônica Jachetti Maciel, Liana Johann & Noeli Juarez Ferla

  2. Departamento de Microbiologia, Imunologia e Parasitologia, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, 90050-170, Brazil

    Guilherme Liberato da Silva, Danielle Machado Pagani, Patrícia Valente, Maria Lúcia Scroferneker & Onilda Santos da Silva

  3. Centro de Ciências Médicas, Univates – Universidade do Vale do Taquari, Lajeado, RS, 95914-014, Brazil

    Daiane Heidrich

Authors
  1. Guilherme Liberato da Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Isadora Zanatta Esswein
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Daiane Heidrich
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fabíola Dresch
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mônica Jachetti Maciel
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Danielle Machado Pagani
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Patrícia Valente
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Maria Lúcia Scroferneker
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Liana Johann
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Noeli Juarez Ferla
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Onilda Santos da Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

GLS, IZE, FD, DH, DMP performed the research, GLS, PV, MLS and LJ prepared the manuscript, GLS, MJM, NJF and OSS conceived and designed the study. GLS, LJ, PV and NJF analyzed the data.

Corresponding author

Correspondence to Guilherme Liberato da Silva.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving human participants and/or animals

For this type of study formal consent is not required.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

da Silva, G.L., Esswein, I.Z., Heidrich, D. et al. Population growth of the stored product pest Tyrophagus putrescentiae (Acari: Acaridae) on environmentally and medically important fungi. Exp Appl Acarol 78, 49–64 (2019). https://doi.org/10.1007/s10493-019-00370-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10493-019-00370-8

Keywords

Search

Navigation