Microbial Ecology

, Volume 75, Issue 4, pp 863–874 | Cite as

Birds Mediate a Fungus-Mite Mutualism

  • Natalie Theron-De Bruin
  • Léanne L. Dreyer
  • Eddie A. Ueckermann
  • Michael J. Wingfield
  • Francois RoetsEmail author
Fungal Microbiology


Mutualisms between ophiostomatoid fungi and arthropods have been well documented. These fungi commonly aid arthropod nutrition and, in turn, are transported to new niches by these arthropods. The inflorescences of Protea trees provide a niche for a unique assemblage of ophiostomatoid fungi. Here, mites feed on Sporothrix fungi and vector the spores to new niches. Protea-pollinating beetles transport the spore-carrying mites between Protea trees. However, many Protea species are primarily pollinated by birds that potentially play a central role in the Protea-Sporothrix-mite system. To investigate the role of birds in the movement of mites and/or fungal spores, mites were collected from Protea inflorescences and cape sugarbirds, screened for Sporothrix fungal spores and tested for their ability to feed and reproduce on the fungal associates. Two mite species where abundant in both Protea inflorescences and on cape sugarbirds and regularly carried Sporothrix fungal spores. One of these mite species readily fed and reproduced on its transported fungal partner. For dispersal, this mite (a Glycyphagus sp.) attached to a larger mite species (Proctolaelaps vandenbergi) which, in turn, were carried by the birds to new inflorescences. The results of this study provide compelling evidence for a new mite-fungus mutualism, new mite-mite commensalisms and the first evidence of birds transporting mites with Sporothrix fungal spores to colonise new Protea trees.


Acari Mutualism Phoresy Promerops Protea Sporothrix 



We thank the Department of Science and Technology/National Research Foundation Centre of Excellence in Tree Health Biotechnology and the Harry Crossley Foundation for financial support for this study as well as the Western Cape Nature Conservation board for issuing the necessary colleting permits. We extend our gratitude to Dr. Phoebe Barnard (South African National Biodiversity Institute) and Dr. Anina Coetzee (Stellenbosch University and South African National Biodiversity Institute) for leading avian sampling in the field as well as Carina Wessels and Leon De Bruin for fieldwork assistance; Drs. Kenneth Oberlander and Janneke Aylward for assistance with DNA extractions and ITS sequencing; Carina Wessels, Alan Lee and David Packer for the use of their photographs; and ringers Alan Lee (Blue Hill Nature Reserve, Uniondale), Francis Hannay (Helderberg Nature Reserve, Somerset West) and Michael and Valerie Ford (Fernkloof Nature Reserve, Hermanus) for additional mite samples collected from birds.


  1. 1.
    Dighton J, White JF (eds) (2017) The fungal community: its organization and role in the ecosystem. 4th edn. CRC Press, Taylor & Francis Group, London, United KingdomGoogle Scholar
  2. 2.
    Malloch D, Blackwell M (1992) Dispersal of fungal diaspores. In: Christensen M (ed) The fungal community: its organization and role in the ecosystem. Marcel Dekker Inc, New York, pp. 147–171Google Scholar
  3. 3.
    Malloch D, Blackwell M (1993) Dispersal biology of ophiostomatoid fungi. In: Wingfield MJ, Seifert KA, Webber JF (eds) Ceratocystis and Ophiostoma: taxonomy, ecology and pathogenicity. American Phytopathogical Society Press, St. Paul, pp. 195–205Google Scholar
  4. 4.
    Cassar S, Blackwell M (1996) Convergent origins of ambrosia fungi. Mycologia 88:596–601CrossRefGoogle Scholar
  5. 5.
    Houck MA, OConnor BM (1991) Ecological and evolutionary significance of phoresy in the Astigmata. Annu Rev Entomol 36:611–636CrossRefGoogle Scholar
  6. 6.
    Binns ES (1982) Phoresy as migration-some functional aspects of phoresy in mites. Biol Rev 57:571–620CrossRefGoogle Scholar
  7. 7.
    Krantz G, Walter D (eds.) (2009) A manual of acarology, 3rd edn. Texas Tech University Press, Lubbock, Google Scholar
  8. 8.
    Aslan CE, Zavaleta ES, Tershy B, Croll D (2013) Mutualism disruption threatens global plant biodiversity: a systematic review. PLoS One 8:e66993CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Hoek TA, Axelrod K, Biancalani T, Yurtsev EA, Liu J, Gore J (2016) Resource availability modulates the cooperative and competitive nature of a microbial cross-feeding mutualism. PLoS Biol 14:e1002540CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Kiers ET, Palmer TM, Ives AR, Bruno JF, Bronstein JL (2010) Mutualisms in a changing world: an evolutionary perspective. Ecol Lett 13:1459–1474CrossRefGoogle Scholar
  11. 11.
    Tylianakis JM, Laliberté E, Nielsen A, Bascompte J (2010) Conservation of species interaction networks. Biol Conserv 143:2270–2279CrossRefGoogle Scholar
  12. 12.
    Fricke EC, Tewksbury JJ, Wandrag EM, Rogers HS (2017) Mutualistic strategies minimize coextinction in plant–disperser networks. Proc R Soc B 284:20162302CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Wingfield MJ, Seifert KA, Webber J (1993) Ceratocystis and Ophiostoma: taxonomy, ecology and pathogenicity. APS Press, St. Paul, Google Scholar
  14. 14.
    Seifert KA, De Beer ZW, Wingfield MJ (2013) The ophiostomatoid fungi: expanding frontiers. CBS Biodiversity Series 12. CBS-KNAW Biodiversity Centre, Utrecht, Google Scholar
  15. 15.
    de Beer Z, Duong TA, Wingfield MJ (2016) The divorce of Sporothrix and Ophiostoma: solution to a problematic relationship. Stud Mycol 83:165–191CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Paine TD, Raffa KF, Harrington TC (1997) Interactions among scolytid bark beetles, their associated fungi, and live host conifers. Annu Rev Entomol 42:179–206CrossRefPubMedGoogle Scholar
  17. 17.
    Klepzig KD, Moser JC, Lombardero FJ, Hofstetter RW, Ayres MP (2001) Symbiosis and competition: complex interactions among beetles, fungi, and mites. Symbiosis 30:83–96Google Scholar
  18. 18.
    Klepzig KD, Moser JC, Lombardero MJ, Ayres MP, Hofstetter RW, Walkinshaw CJ (2001b) Mutualism and antagonism: ecological interactions among bark beetles, mites and fungi. In: Jeger MJ, Spence NJ (eds) Biotic interactions in plant-pathogen associations. CAB International, Wallingford, pp. 237–267CrossRefGoogle Scholar
  19. 19.
    Bleiker KP, Six DL (2007) Dietary benefits of fungal associates to an eruptive herbivore: potential implications of multiple associates on host population dynamics. Environ Entomol 36:1384–1396CrossRefPubMedGoogle Scholar
  20. 20.
    Moser JC, Bridges JR (1986) Tarsonemus (Acarina: Tarsonemidae) mites phoretic on the southern pine beetle (Coleoptera: Scolytidae): attachment sites and numbers of bluestain (Ascomycetes: Ophiostomataceae) ascospores carried. Proc Entomol Soc Wash 88:297–299Google Scholar
  21. 21.
    Levieux J, Lieutier F, Moser JC, Perry TJ (1989) Transportation of phytopathogenic fungi by the bark beetle Ips sexdentatus Boerner and associated mites. J Appl Entomol 108:1–11CrossRefGoogle Scholar
  22. 22.
    Moser JC, Konrad H, Blomquist SR, Kirisits T (2010) Do mites phoretic on elm bark beetles contribute to the transmission of Dutch elm disease? Naturwissenschaften 97:219–227CrossRefPubMedGoogle Scholar
  23. 23.
    Hofstetter RW, Moser JC, Blomquist S (2014) Mites associated with bark beetles and their hyperphoretic ophiostomatoid fungi. In: Seifert KA, De Beer ZW, Wingfield MJ (eds), The Ophiostomatoid Fungi: Expanding Frontiers, CBS Biodiversity Series 12, CBS-KNAW Biodiversity Centre, Utrecht, pp 65–176Google Scholar
  24. 24.
    Moser JC (1985) Use of sporothecae by phoretic Tarsonemus mites to transport ascospores of coniferous bluestain fungi. Trans Br Mycol Soc 84:750–753CrossRefGoogle Scholar
  25. 25.
    Bridges JR, Moser JC (1983) Role of two phoretic mites in transmission of bluestain fungus, Ceratocystis minor. Ecol Entomol 8:9–12CrossRefGoogle Scholar
  26. 26.
    Lombardero MJ, Ayres MP, Hofstetter RW, Moser JC, Lepzig KD (2003) Strong indirect interactions of Tarsonemus mites (Acarina: Tarsonemidae) and Dendroctonus frontalis (Coleoptera: Scolytidae). Oikos 102:243–252CrossRefGoogle Scholar
  27. 27.
    Hofstetter RW, Moser JC (2014) The role of mites in insect-fungus associations. Annu Rev Entomol 59:537–557CrossRefPubMedGoogle Scholar
  28. 28.
    Lee S, Roets F, Crous PW (2005) Biodiversity of saprobic microfungi associated with the infructescences of Protea species in South Africa. Fungal Divers 19:69–78Google Scholar
  29. 29.
    Roets F, Wingfield MJ, Crous PW, Dreyer LL (2007) Discovery of fungus-mite mutualism in a unique niche. Environ Entomol 36:1226–1237CrossRefPubMedGoogle Scholar
  30. 30.
    Roets F, Crous PW, Wingfield MJ, Dreyer LL (2009) Mite-mediated hyperphoretic dispersal of Ophiostoma spp. from the infructescences of south African Protea spp. Environ Entomol 38:143–152CrossRefPubMedGoogle Scholar
  31. 31.
    Roets F, Wingfield MJ, Wingfield BD, Dreyer LL (2011) Mites are the most common vectors of the fungus Gondwanamyces proteae in Protea infructescences. Fungal Biol 115:343–350CrossRefPubMedGoogle Scholar
  32. 32.
    Aylward J, Dreyer LL, Steenkamp ET, Wingfield MJ, Roets F (2014a) Development of polymorphic microsatellite markers for the genetic characterisation of Knoxdaviesia proteae (Ascomycota: Microascales) using ISSR-PCR and pyrosequencing. Mycol Prog 13:439–444CrossRefGoogle Scholar
  33. 33.
    Aylward J, Dreyer LL, Steenkamp ET, Wingfield MJ, Roets F (2014b) Panmixia defines the genetic diversity of a unique arthropod-dispersed fungus specific to Protea flowers. Ecol Evol 4:3444–3455CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Aylward J, Dreyer LL, Steenkamp ET, Wingfield MJ, Roets F (2015) Long-distance dispersal and recolonization of a fire-destroyed niche by a mite-associated fungus. Fungal Biol 119:245–256CrossRefPubMedGoogle Scholar
  35. 35.
    Aylward J, Dreyer LL, Laas T, Smit L, Roets F (2017) Knoxdaviesia capensis: dispersal ecology and population genetics of a flower-associated fungus. Fungal Ecol 26:28–36CrossRefGoogle Scholar
  36. 36.
    Roets F, Dreyer LL, Crous PW (2005) Seasonal trends in colonisation of Protea infructescences by Gondwanamyces and Ophiostoma spp. S Afr J Bot 71:307–311CrossRefGoogle Scholar
  37. 37.
    Coetzee JH, Giliomee JH (1985) Insects in association with the inflorescence of Protea repens L. (Proteaceae) and their role in pollination. J Entomol Soc South Afr 48:303–314Google Scholar
  38. 38.
    Coetzee JH, Latsky LM (1985) Faunal list of Protea repens. Int Protea Res Symp 185:241–246Google Scholar
  39. 39.
    Wright MG, Samways MJ (1999) Plant characteristics determine insect borer assemblages on Protea species in the cape Fynbos, and importance for conservation management. Biodivers Conserv 8:1089–1100CrossRefGoogle Scholar
  40. 40.
    Wright MG, Visser D, Coetzee JH, Giliomee JH (1991) Insect and bird pollination of Protea species in the Western Cape—further data. S Afr J Sci 87:214–215Google Scholar
  41. 41.
    Rebelo T (2001) SASOL Proteas: a field guide to the Proteas of South Africa, 2nd edn. Fernwood Press (Pty) Ltd., Vlaeberg, Google Scholar
  42. 42.
    Schmid B, Nottebrock H, Esler KJ, Pagel J, Pauw A, Böhning-Gaese K, Schurr FM, Schleuning M (2015) Reward quality predicts effect of bird-pollinators on the reproduction of African Protea shrubs. Perspect Plant Ecol Evol Syst 17:209–217CrossRefGoogle Scholar
  43. 43.
    Siegfried WR, Crowe TM (1983) Distribution and species diversity of birds and plants in Fynbos vegetation of Mediterranean climate-zone, South Africa. In: Kruger FJ, Mitchell DT, JUM J (eds) Mediterranean-type ecosystems: the role of nutrients. Ecological studies 43. Springer, Berlin, pp. 403–416CrossRefGoogle Scholar
  44. 44.
    Latimer AM, Silander Jr JA, Rebelo AG, Midgley GF (2009) Experimental biogeography: the role of environmental gradients in high geographic diversity in Cape Proteaceae. Oecologia 160:151–162CrossRefPubMedGoogle Scholar
  45. 45.
    Fraser MW (1997) Cape sugarbird Promerops cafer. In: Harrison JA, Allan DG, Underhill LG, Herremans M, Tree AJ, Parker V, Brown CJ (eds) The atlas of southern African birds. Vol. 2: passerines. BirdLife South Africa, Johannesburg, pp. 484–485Google Scholar
  46. 46.
    Mackay B (2014) The effect of urbanisation and climate on the frequency of ecological stress indicators in the Fynbos endemic nectarivore, the cape sugarbird. Dissertation, University of Cape TownGoogle Scholar
  47. 47.
    Mostert DP, Siegfried WR, Louw GN (1980) Protea nectar and satellite fauna in relation to the food requirements and pollinating role of the cape sugarbird. S Afr J Sci. 76:409–412Google Scholar
  48. 48.
    Nicolson SW, Flemming PA (2003) Nectar as food for birds: the physiological consequences of drinking dilute sugar solutions. Plant Syst Evol 238:139–153CrossRefGoogle Scholar
  49. 49.
    Myburg AC, Rust DJ, Starke LC (1973) Pests of Protea cut flowers. J Entomol Soc South Afr 36:251–255Google Scholar
  50. 50.
    Coetzee JH, Rust DJ, Latsky LM (1985) Mites (Acari) on proteas. Int Protea Res Symp 185:247–252Google Scholar
  51. 51.
    Calf KM, Downs CT, Cherry MI (2003) Foraging and territorial behaviour of male cape and Gurney’s sugarbirds (Promerops cafer and P. gurneyi). Afr Zool 38:297–304Google Scholar
  52. 52.
    Collins BG (1983) A first approximation of the energetics of cape sugarbirds (Promerops cafer) and orange-breasted sunbirds (Nectarinia violacea). S Afr J Zool 18:363–369CrossRefGoogle Scholar
  53. 53.
    Broekhuysen GJ (1959) The biology of the cape sugarbird Promerops cafer (L.). Ostrich 30:180–221CrossRefGoogle Scholar
  54. 54.
    Westerkamp C (1990) Bird-flowers: hovering versus perching exploitation. Bot Acta 103:366–371CrossRefGoogle Scholar
  55. 55.
    Bates D, Sarkar D (2008) The lme4 Package, 2006. URL Accessed 1 June 2017
  56. 56.
    White TJ, Bruns T, Lee SJWT, 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. New York Academic Press, New York, pp 315–322Google Scholar
  57. 57.
    Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118CrossRefPubMedGoogle Scholar
  58. 58.
    Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  59. 59.
    de Winter JC (2013) Using the Student’s t-test with extremely small sample sizes. Pract Assess Res Eval 18:1–12Google Scholar
  60. 60.
    Colwell RK (1995) Effects of nectar consumption by the hummingbird flower mite Proctolaelaps kirmsei on nectar availability in Hamelia patens. Biotropica 27:206–217Google Scholar
  61. 61.
    Theron N (2011) Mite communities within Protea infructescences in South Africa. Dissertation, Stellenbosch UniversityGoogle Scholar
  62. 62.
    Roets F, Theron N, Wingfield MJ, Dreyer LL (2012) Biotic and abiotic constraints that facilitate host exclusivity of Gondwanamyces and Ophiostoma on Protea. Fungal Biol 116:49–61CrossRefPubMedGoogle Scholar
  63. 63.
    Klepzig KD, Six DL (2004) Bark beetle-fungal symbiosis: context dependency in complex associations. Symbiosis 37:189–205Google Scholar
  64. 64.
    Hektoen L, Perkins CF (1900) Refractory subcutaneous abscesses caused by Sporothrix schenckii. A new pathogenic fungus. J Exp Med 5:77–89CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    De Lima Barros MB, de Almeida Paes R, Schubach AO (2011) Sporothrix schenckii and Sporotrichosis. Clin Microbiol Rev 24:633–654CrossRefGoogle Scholar
  66. 66.
    Rodrigues AM, De Hoog S, De Camargo ZP (2013) Emergence of pathogenicity in the Sporothrix Schenckii Complex. Med Mycol 51:405–412CrossRefPubMedGoogle Scholar
  67. 67.
    Bajerlein D, Błoszyk J (2003) Two cases of hyperphoresy in mesostigmatic mites (Acari: Gamasida: Uropodidae, Macrochelidae). Biol Lett 40:135136Google Scholar
  68. 68.
    Chmielewski W (1977) Results of observations on associations of mites with insects (Acari-Insecta). Bull Entomol Pologne 47:59–57Google Scholar
  69. 69.
    Knülle W (2003) Interaction between genetic and inductive factors controlling the expression of dispersal and dormancy morphs in dimorphic astigmatic mites. Evolution 57:828–838CrossRefPubMedGoogle Scholar
  70. 70.
    Cutraro JL, Ercelawn AY, LeBrun EG, Lonsdorf EW, Norton HA, McKone MJ (1998) Importance of pollen and nectar in flower choice by hummingbird flower mites, Proctolaelaps kirmsei (Mesostigmata: Ascidae). Int. J. Acarol. 24:345–351CrossRefGoogle Scholar
  71. 71.
    Hockey PAR, Dean WRJ, Ryan PG (2005) Roberts’ birds of Southern Africa. Trustees of the John Voelcker Bird Book Fund, Cape Town, Google Scholar
  72. 72.
    Marais GJ, Wingfield MJ (1994) Fungi associated with infructescences of Protea species in South Africa, including a new species of Ophiostoma. Mycol Res 98:369–374CrossRefGoogle Scholar
  73. 73.
    Roets F, Wingfield MJ, Crous PW, Dreyer LL (2013) Taxonomy and ecology of ophiostomatoid fungi associated with Protea infructescences. In: Seifert KA, De Beer ZW, Wingfield MJ (eds) The ophiostomatoid fungi: expanding frontiers. In: CBS Biodiversity Series 12. CBS-KNAW Biodiversity Centre, Utrecht, pp. 177–187Google Scholar
  74. 74.
    Hargreaves AL, Johnson SD, Nol E (2004) Do floral syndromes predict specialization in plant pollination systems? An experimental test in an “ornithophilous” African Protea. Oecologia 140:295–301CrossRefPubMedGoogle Scholar
  75. 75.
    Theron N, Roets F, Dreyer LL, Esler KJ, Ueckermann EA (2012) A new genus and eight new species of Tydeoidea (Acari: Trombidiformes) from Protea species in South Africa. Int J Acarol 38:257–273CrossRefGoogle Scholar
  76. 76.
    Farrell BD, Sequeira AS, O’Meara BC, Normark BB, Chung JH, Jordal BH (2001) The evolution of agriculture in beetles (Curculionidae: Scolytinae and Platypodinae). Evolution 55:2011–2027CrossRefPubMedGoogle Scholar
  77. 77.
    Currie CR, Wong B, Stuart AE, Schultz TR, Rehner SA, Mueller UG, Sung GH, Spatafora JW, Straus NA (2003) Ancient tripartite coevolution in the attine ant-microbe symbiosis. Science 299:386–388CrossRefPubMedGoogle Scholar
  78. 78.
    Currie CR, Poulsen M, Mendenhall J, Boomsma JJ, Billen J (2006) Coevolved crypts and exocrine glands support mutualistic bacteria in fungus-growing ants. Science 311:81–83CrossRefPubMedGoogle Scholar
  79. 79.
    Aylward FO, Burnum KE, Scott JJ, Suen G, Tringe SG, Adams SM, Barry KW, Nicora CD, Piehowski PD, Purvine SO, Starrett GJ, Goodwin LA, Smith RD, Lipton MS, Currie CR (2012) Metagenomic and metaproteomic insights into bacterial communities in leaf-cutter ant fungus gardens. ISME J 6:1688–1701CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Scott JJ, Oh DC, Yuceer MC, Klepzig KD, Clardy J, Currie CR (2008) Bacterial protection of beetle-fungus mutualism. Science 322:63–63CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Rohr RP, Saavedra S, Bascompte J (2014) On the structural stability of mutualistic systems. Science 345:1253497CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Natalie Theron-De Bruin
    • 1
  • Léanne L. Dreyer
    • 2
  • Eddie A. Ueckermann
    • 3
  • Michael J. Wingfield
    • 4
  • Francois Roets
    • 1
    Email author
  1. 1.Department of Conservation Ecology and EntomologyStellenbosch UniversityStellenboschSouth Africa
  2. 2.Department of Botany and ZoologyStellenbosch UniversityStellenboschSouth Africa
  3. 3.School of Biological Sciences/ZoologyNorth-West University, Potchefstroom CampusPotchefstroomSouth Africa
  4. 4.Forestry and Agricultural Biotechnology Institute (FABI)University of PretoriaPretoriaSouth Africa

Personalised recommendations