Skip to main content
SpringerLink
Log in

Molecular identification of Botryosphaeria dothidea as a fungal associate of the gall midge Asphondylia prosopidis on mesquite in the United States

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

The gall midge, Asphondylia prosopidis Cockerell, is considered a potential biological control agent for invasive mesquite (Prosopis species) populations in South Africa. Asphondylia species induce galls on mesquite plants by inserting an egg into a bud, and also carry conidia of specific fungal associates in their mycangia that are transferred into the galls. However, fungal associates have not been characterized in flower bud galls formed by A. prosopidis on mesquite. It is essential to identify the fungal associates in the galls formed on natural populations of mesquite prior to host specificity testing. In this study, we showed that Botryosphaeria dothidea (Moug. ex Fr.) Ces. & De Not. is the fungal associate in the flower bud galls on mesquite induced by A. prosopidis in New Mexico by characterization of the internal transcribed spacer (ITS) region. Further, isolates of B. dothidea in A. prosopidis galls formed on mesquite were genetically identical to isolates of B. dothidea carried by other Asphondylia species, particularly on the confamilial Acacia species in South Africa. Our result suggests that A. prosopidis is safe to utilize as a biological control agent for mesquite, if A. prosopidis shows a narrow host range in the pre-release risk assessment, since B. dothidea appears to be ubiquitous. To our knowledge, this is the first report of the association between Asphondylia species and B. dothidea in the United States. We anticipate that A. prosopidis will associate with indigenous B. dothidea in South Africa.

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

Similar content being viewed by others

References

  • Aanen DK, Eggleton P, Rouland-Lefevre C, Guldberg-Frøslev T, Rosendahl S, Boomsma JJ (2002) The evolution of fungus-growing termites and their mutualistic fungal symbionts. Proc Natl Acad Sci 99:14887–14892

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Adair RJ, Burgess T, Serdani M, Barber P (2009) Fungal associations in Asphondylia (Diptera: Cecidomyiidae) galls from Australia and South Africa: implications for biological control of invasive acacias. Fungal Ecol 2:121–134

    Article  Google Scholar 

  • Axelrod DI (1937) A Pliocene flora from the Mount Eden beds, southern California. Carnegie Inst Wash Publ 476:125–183

    Google Scholar 

  • Batra LR, Lichtwardt RW (1963) Association of fungi with some insect galls. J Kans Entomol Soc 36:262–278

    Google Scholar 

  • Bergeron MJ, Leal I, Foord B, Ross G, Davis C, Slippers B, De Groot P, Hamelin RC (2011) Putative origin of clonal lineages of Amylostereum areolatum, the fungal symbiont associated with Sirex noctilio, retrieved from Pinus sylvestris, in eastern Canada. Fungal Biol 115:750–758

    Article  PubMed  Google Scholar 

  • Bernardo U, Nugnes F, Gualtieri L, Nicoletti R, Varricchio P, Sasso R, Viggiani G (2018) A new gall midge species of Asphondylia (Diptera: Cecidomyiidae) inducing flower galls on Clinopodium nepeta (Lamiaceae) from Europe, its phenology, and associated fungi. Environ Entomol 47:609–622

    Article  PubMed  Google Scholar 

  • Bissett J, Borkent A (1988) Ambrosia galls: the significance of fungal nutrition in the evolution of the Cecidomyiidae (Diptera). In: Pirozynski KA, Hawksworth DL (eds) Coevolution of fungi with plants and animals. Academic Press, London, pp 203–205

    Google Scholar 

  • Burgess TI, Crous CJ, Slippers B, Hantula J, Wingfield MJ (2016) Tree invasions and biosecurity: eco-evolutionary dynamics of hitchhiking fungi. AoB PLANTS 8:plw076

    Article  PubMed  PubMed Central  Google Scholar 

  • Carneiro MAA, Branco CSA, Braga CED, Almada ED, Costa MBM, Maia VC, Fernandes GW (2009) Are gall midge species (Diptera, Cecidomyiidae) host-plant specialists? Rev Bras Entomol 53:365–378

    Article  Google Scholar 

  • Center TD, Purcell MF, Pratt PD, Rayamajhi MB, Tipping PW, Wright SA, Dray FA Jr (2012) Biological control of Melaleuca quinquenervia: an Everglade invader. BioControl 57:151–165

    Article  Google Scholar 

  • Cockerell T (1898) XXXVII.—New North-American insects. Ann Mag Nat Hist 2:321–331

    Article  Google Scholar 

  • Coetzer W, Hoffmann JH (1997) Establishment of Neltumius arizonensis (Coleoptera: Bruchidae) on mesquite (Prosopis species: Mimosaceae) in South Africa. Biol Control 10:187–192

    Article  Google Scholar 

  • Dean W, Anderson M, Milton S, Anderson T (2002) Avian assemblages in native Acacia and alien Prosopis drainage line woodland in the Kalahari, South Africa. J Arid Environ 51:1–19

    Article  Google Scholar 

  • Dorchin N, Joy JB, Hilke LK, Wise MJ, Abrahamson WG (2015) Taxonomy and phylogeny of the Asphondylia species (Diptera: Cecidomyiidae) of North American goldenrods: challenging morphology, complex host associations, and cryptic speciation. Zool J Linn Soc 174:265–304

    Article  Google Scholar 

  • Gagné RJ (1989) The plant-feeding gall midges of North America. Cornell University Press, Ithaca

    Google Scholar 

  • Gagné RJ (2004) A catalog of the Cecidomyiidae (Diptera) of the world. Mem Entomol Soc Wash 24:1–408

    Google Scholar 

  • Gagné RJ (2010) Update for a catalog of the Cecidomyiidae (Diptera) of the world. Entomol Soc Wash, Washington

    Google Scholar 

  • Gagné RJ, Waring GL (1990) The Asphondylia (Cecidomyiidae, Diptera) of creosote bush (Larrea tridentata) in North America. Proc Entomol Soc Wash 92:649–671

    Google Scholar 

  • Gagné RJ, Woods WM (1988) Native American plant hosts of Asphondylia websteri (Diptera, Cecidomyiidae). Ann Entomol Soc Am 81:447–448

    Article  Google Scholar 

  • Goloboff PA (1999) NONA, version 2.0. Fundación e instituto Miguel Lillo, Tucumán, Argentina

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Harding GB (1987) The status of Prosopis spp. as a weed. Appl Plant Sci 1:43–48

    Google Scholar 

  • Harding GB, Bate GC (1991) The occurrence of invasive Prosopis species in the north-western Cape, South Africa. S Afr J Sci 87:188–192

    Google Scholar 

  • Hawkins BA, Goeden RD, Gagné RJ (1986) Ecology and taxonomy of the Asphondylia spp. (Diptera: Cecidomyiidae) forming galls on Atriplex spp. (Chenopodiaceae) in Southern California. Entomography 4:55–107

    Google Scholar 

  • Heard TA (2000) Concepts in insect host-plant selection behavior and their application to host specificity testing. In: van Driesche RG, Heard T, McClay A, Reardon R (eds) Proceedings: host specificity testing of exotic arthropod biological control agents: the biological basis for improvement in safety. US Forest Service, Forest Health Technology Enterprise Team, Morgantown, pp 1–10

    Google Scholar 

  • Heath JJ, Stireman JO (2010) Dissecting the association between a gall midge, Asteromyia carbonifera, and its symbiotic fungus, Botryosphaeria dothidea. Entomol Exp Appl 137:36–49

    Article  Google Scholar 

  • Impson F, Moran V, Hoffmann J, Olckers T, Hill M (1999) A review of the effectiveness of seed-feeding bruchid beetles in the biological control of mesquite, Prosopis species (Fabaceae), in South Africa. In: Olckers T, Hill MP (Eds). Biological control of weeds in South Africa (1990–1998). African Entomol Mem 1:81–88

    Google Scholar 

  • Jami F, Slippers B, Wingfield MJ, Loots MT, Gryzenhout M (2015) Temporal and spatial variation of Botryosphaeriaceae associated with Acacia karroo in South Africa. Fungal Ecol 15:51–62

    Article  Google Scholar 

  • Janson EM, Peeden ER, Stireman JO, Abbot P (2010) Symbiont-mediated phenotypic variation without co-evolution in an insect-fungus association. J Evol Biol 23:2212–2228

    Article  CAS  PubMed  Google Scholar 

  • Klein H (2011) A catalogue of the insects, mites and pathogens that have been used or rejected, or are under consideration, for the biological control of invasive alien plants in South Africa. Afr Entomol 19:515–549

    Article  Google Scholar 

  • Kobune S, Kajimura H, Masuya H, Kubono T (2012) Symbiotic fungal flora in leaf galls induced by Illiciomyia yukawai (Diptera: Cecidomyiidae) and in its mycangia. Microb Ecol 63:619–627

    Article  PubMed  Google Scholar 

  • Lebel T, Peele C, Veenstra A (2012) Fungi associated with Asphondylia (Diptera: Cecidomyiidae) galls on Sarcocornia quinqueflora and Tecticornia arbuscula (Chenopodiaceae). Fungal Divers 55:143–154

    Article  Google Scholar 

  • Marsberg A, Kemler M, Jami F, Nagel JH, Postma-Smidt A, Naidoo S, Wingfield MJ, Crous PW, Spatafora JW, Hesse CN (2017) Botryosphaeria dothidea: a latent pathogen of global importance to woody plant health. Mol plant pathol 18:477–488

    Article  CAS  PubMed  Google Scholar 

  • Meyer J (1987) Plant galls and gall inducers. Gebrüder Bornträger, Berlin

    Google Scholar 

  • Miller JR, Strickler KL (1984) Finding and accepting host plants. In: Bell WJ, Cardé RT (eds) Chemical ecology of insects. Sinauer Associates, Boston, pp 127–157

    Chapter  Google Scholar 

  • Montgomery ME (2011) Understanding federal regulations as guidelines for classical biological control programs. In: Onken B, Reardon R (eds) Implementation and status of biological control of the hemlock woolly adelgid. US Department of Agriculture, Forest Service Forest Health Technology Enterprise Team, Morgantown, pp 25–40

    Google Scholar 

  • Moran V, Hoffmann J, Zimmermann H (1993) Objectives, constraints, and tactics in the biological control of mesquite weeds (Prosopis) in South Africa. Biol Control 3:80–83

    Article  Google Scholar 

  • Neger FW (1910) Ambrosiapilze III. Weitere beobachtungen an ambrosia gallen. Ber Deut Bot Ges 28:455–482

    Google Scholar 

  • Nixon KC (2002) WinClada, version 1.00. 08. Published by the author, Ithaca

  • Nylander JAA (2004) MrModeltest v2.2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University

  • Osorio JA, Crous CJ, De Beer ZW, Wingfield MJ, Roux J (2017) Endophytic Botryosphaeriaceae, including five new species, associated with mangrove trees in South Africa. Fungal Biol 121:361–393

    Article  PubMed  Google Scholar 

  • Page RDM (1996) TreeView: an application to display phylogenetic trees on personal computers. Comp Appl Biosci 12:357–358

    CAS  PubMed  Google Scholar 

  • Painter RH (1935) The biology of some dipterous gall-makers from Texas. J Kansas Entomol Soc 8:81–97

    Google Scholar 

  • Palvic D, Wingfield MJ, Barber P, Slippers B, Hardy GE, Burgess TI (2008) Seven new species of the Botryosphaeriaceae from baobab and other native trees in Western Australia. Mycologia 100:851–866

    Article  Google Scholar 

  • Park I (2010) Asphondylia prosopidis complex (Diptera: Cecidomyiidae) and fungal associates: potential biological control candidates for South African mesquite. Master thesis, New Mexico State University

  • Park I, Thompson D (2018) Unisexual broods of Asphondylia species in new floral bud galls on mesquite in New Mexico. Southwest Entomol 43:585–589

    Article  Google Scholar 

  • Park I, Eigenbrode SD, Cook SP, Harmon BL, Hinz HL, Schaffner U, Schwarzländer M (2018) Examining olfactory and visual cues governing host-specificity of a weed biological control candidate species to refine pre-release risk assessment. BioControl 63:377–389

    Article  Google Scholar 

  • Philips AJP, Alves A, Correia A, Luque J (2005) Two new species of Botryosphaeria with brown, 1-septate ascospores and Dothiorella anamorphs. Mycologia 97:513–529

    Article  Google Scholar 

  • Philips AJP, Oudemans PV, Correia A, Alves A (2006) Characterization and epitypifaction of Botryosphaeria corticis, the cause of blueberry cane canker. Fungal Divers 21:141–155

    Google Scholar 

  • Phillips AJP, Alves A, Abdollahzadeh J, Slippers B, Wingfield MJ, Groenewald J, Crous PW (2013) The Botryosphaeriaceae: genera and species known from culture. Stud Mycol 76:51–167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  CAS  PubMed  Google Scholar 

  • Pratt PD, Blackwood S, Wright SA, Purcell M, Rayamajhi MB, Giblin-Davis RM, Scheffer SJ, Tipping PW, Center TD (2013) The release and unsuccessful establishment of the Melaleuca biological control agent Fergusonina turneri and its mutualistic nematode Fergusobia quinquenerviae. BioControl 58:553–561

    Article  CAS  Google Scholar 

  • Raman A, Suryanarayanan TS (2017) Fungus–plant interaction influences plant-feeding insects. Fungal Ecol 29:123–132

    Article  Google Scholar 

  • Rogers C (1973) Bionomics of a gall midge, Asphondylia prosopidis Cockerell, attacking mesquite buds. Cecid Indica 8:131–142

    Google Scholar 

  • Rohfritsch O (2008) Plants, gall midges, and fungi: a three-component system. Entomol Exp Appl 128:208–216

    Article  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Schachtschneider K, February EC (2013) Impact of Prosopis invasion on a keystone tree species in the Kalahari Desert. Plant Ecol 214:597–605

    Article  Google Scholar 

  • Slippers B, Wingfield MJ (2007) Botryosphaeriaceae as endophytes and latent pathogens of woody plants: diversity, ecology and impact. Fungal Biol Rev 21:90–106

    Article  Google Scholar 

  • Slippers B, Crous PW, Denman S, Coutinho TA, Wingfield BD, Wingfield MJ (2004) Combined multiple gene genealogies and phenotypic characters differentiate several species previously identified as Botryosphaeria dothidea. Mycologia 96:83–101

    Article  CAS  PubMed  Google Scholar 

  • Smith H, Kemp GHJ, Wingfield MJ (1994) Canker and dieback of eucalyptus in South Africa caused by Botryosphaeria dothidea. Plant Pathol 43:1031–1034

    Article  Google Scholar 

  • Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57:758–771

    Article  PubMed  Google Scholar 

  • Stone GN, Schönrogge K (2003) The adaptive significance of insect gall morphology. Trends Ecol Evol 18:512–522

    Article  Google Scholar 

  • Swofford DL (2001) Phylogenetic analysis using parsimony (and other methods) version 4.0b10. Sinauer Associates, Sunderland, Massachusetts

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Tokuda M (2012) Biology of Asphondyliini (Diptera: Cecidomyiidae). Entomol Sci 15:361–383

    Article  Google Scholar 

  • van Niekerk JM, Pedro WC, Groenewald JZ, Paul HF, Francois H (2004) DNA phylogeny, morphology and pathogenicity of Botryosphaeria species on grapevines. Mycologia 96:781–798

    Article  PubMed  Google Scholar 

  • Veenstra-Quah AA, Milne J, Kolesik P (2007) Taxonomy and biology of two new species of gall midge (Diptera: Cecidomyiidae) infesting Sarcocornia quinqueflora (Chenopodiaceae) in Australian salt marshes. Aust J Entomol 46:198–206

    Article  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (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, New York, pp 315–322

    Google Scholar 

  • Williams MAJ (1994) Plant galls: organisms, interactions, populations. Clarendon Press, Oxford

    Google Scholar 

  • Winston R, Schwarzländer M, Hinz HL, Day MD, Cock MJ, Julien M (2014) Biological control of weeds: a world catalogue of agents and their target weeds, 5th edn. USDA Forest Service, Forest Health Technology Enterprise Team, Morgantown

    Google Scholar 

  • Zachariades C, Hoffmann JH, Roberts AR (2011) Biological control of mesquite (Prosopis species) (Fabaceae) in South Africa. Afr Entomol 19:402–415

    Article  Google Scholar 

  • Zimmermann H (1991) Biological control of mesquite, Prosopis spp. (Fabaceae), in South Africa. Agric Ecosyst Environ 37:175–186

    Article  Google Scholar 

  • Zimowska B, Viggiani G, Nicoletti R, Furmańczyk A, Becchimanzi A, Kot I (2017) First report of the gall midge Asphondylia serpylli on thyme (Thymus vulgaris), and identification of the associated fungal symbiont. Ann Appl Biol 171:89–94

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank colleagues in the department of Entomology, Plant Pathology, and Weed Science at New Mexico State University: Kevin Gardner, Howard Beuhler, Linda Liess, Deana Baucom, Jennifer Randall, Jorge Achata, Frank Solano, and many others. Special thanks to Robin Adair for providing DNA sequences and personal communication. This project was supported by the Weeds Division of ARC-PPRI and by the New Mexico Agricultural Experiment Station.

Author information

Authors and Affiliations

  1. Department of Entomology, Plant Pathology and Weed Science, New Mexico State University, 945 College Avenue, MSC 3BE, Las Cruces, NM, 88003-8003, USA

    Ikju Park, Soum Sanogo, Stephen F. Hanson & David C. Thompson

Authors
  1. Ikju Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Soum Sanogo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stephen F. Hanson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. David C. Thompson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ikju Park.

Additional information

Handling Editor: S. Raghu.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Park, I., Sanogo, S., Hanson, S.F. et al. Molecular identification of Botryosphaeria dothidea as a fungal associate of the gall midge Asphondylia prosopidis on mesquite in the United States. BioControl 64, 209–219 (2019). https://doi.org/10.1007/s10526-019-09924-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-019-09924-6

Keywords

Search

Navigation