Skip to main content
Log in

Nipponaclerda Biwakoensis Infestation of Phragmites australis in the Mississippi River Delta, USA: Do Fungal Microbiomes Play a Role?

  • Wetland Ecology
  • Published:
Wetlands Aims and scope Submit manuscript

Abstract

Recently, significant die-back of nonnative common reed, Phragmites australis, has been reported in the Mississippi River Delta (MRD), Louisiana, USA. This dieback has been attributed to an invasive scale insect, Nipponaclerda biwakoensis. We test whether fungi are involved in the recent infestation by this insect and subsequent die-offs of P. australis. Several haplotypes of P. australis occur in the MRD, and the European (M) and Delta (M1) haplotypes appear to experience differing levels of N. biwakoensis infestation. We tested whether these haplotypes differed in their fungal microbiomes in both their leaf and stem tissues, and whether differences in fungal community composition were linked to the level of infestation using a metabarcoding Internal Transcribed Spacer (ITS) amplicon sequencing approach. Our analyses showed differences in fungal community composition and diversity between haplotypes and tissue types, but none of these differences were directly correlated with N. biwakoensis infestation severity. However, we did find that the European haplotype hosted higher putative pathogen loads in stem tissues compared to the Delta haplotype, which may confer resistance to herbivory, though it is possible that differences in infestation between haplotypes are due to morphology.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abbas HK, Ocamb CM (1995) First report of production of fumonisin B sub (1) by fusarium polyphialidicum collected from seeds of Pinus strobus. Plant Disease 79(6):642

    Article  Google Scholar 

  • Allen WJ, DeVries AE, Bologna NJ, Bickford WA, Kowalski KP, Meyerson LA, Cronin JT (2020) Intraspecific and biogeographical variation in foliar fungal communities and pathogen damage of native and invasive Phragmites australis. Global Ecology and Biogeography, February, 1–13. https://doi.org/10.1111/geb.13097

  • Al-Naemi F, Hatcher PE (2013) Contrasting effects of necrotrophic and biotrophic plant pathogens on the aphid Aphis fabae. Entomologia Experimentalis et Applicata 148(3):234–245. https://doi.org/10.1111/eea.12091

    Article  Google Scholar 

  • Bálint M, Tiffin P, Hallström B, O’Hara RB, Olson MS, Fankhauser JD, Piepenbring M, Schmitt I (2013) Host genotype shapes the foliar fungal microbiome of balsam poplar (Populus balsamifera). PLoS One 8(1). https://doi.org/10.1371/journal.pone.0053987

  • Bickford WA, Goldberg DE, Kowalski KP, Zak DR (2018) Root endophytes and invasiveness: no difference between native and non-native Phragmites in the Great Lakes region. Ecosphere 9(12). https://doi.org/10.1002/ecs2.2526

  • Bowen JL, Kearns PJ, Byrnes JE, Wigginton S, Allen WJ, Greenwood M et al (2017) Lineage overwhelms environmental conditions in determining rhizosphere bacterial community structure in a cosmopolitan invasive plant. Nature Communications 8(1):1–8. https://doi.org/10.1038/s41467-017-00626-0

    Article  CAS  Google Scholar 

  • Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nature Methods 13(7):581–583. https://doi.org/10.1038/nmeth.3869

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cardoza YJ, Hofstetter RW, Vega FE (2012) Insect-associated microorganisms and their possible role in outbreaks. In P. Barbosa, D. K. Letourneau, & A. A. Agrawal (Eds.), Insect outbreaks revisited (first, pp. 155–174). Blackwell Publishing Ltd

  • Cardoza YJ, Lait CG, Schmelz EA, Huang J, Tumlinson JH (2003) Fungus-induced biochemical changes in Peanut plants and their effect on development of beet armyworm, Spodoptera Exigua Hübner (Lepidoptera: Noctuidae) larvae. Environmental Entomology 32(1):220–228. https://doi.org/10.1603/0046-225x-32.1.220

    Article  CAS  Google Scholar 

  • Chambers RM, Meyerson LA, Saltonstall K (1999) Expansion of Phragmites australis into tidal wetlands of North America. Aquatic Botany 64:261–273

    Article  Google Scholar 

  • Choudhary DK, Varma A (2016) Microbial-mediated induced systematic resistance in plants. Springer

    Book  Google Scholar 

  • Clay K, Holah J, Rudgers JA (2005) Herbivores cause a rapid increase in hereditary symbiosis and alter plant community composition. Proceedings of the National Academy of Sciences of the United States of America 102(35):12465–12470. https://doi.org/10.1073/pnas.0503059102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clay K, Shearin ZRC, Bourke KA, Bickford WA, Kowalski KP (2016) Diversity of fungal endophytes in non-native Phragmites australis in the Great Lakes. Biological Invasions 18(9):2703–2716. https://doi.org/10.1007/s10530-016-1137-y

    Article  Google Scholar 

  • Coleman-Derr D, Desgarennes D, Fonseca-Garcia C, Gross S, Clingenpeel S, Woyke T, North G, Visel A, Partida-Martinez LP, Tringe SG (2016) Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species. New Phytologist 209(2):798–811. https://doi.org/10.1111/nph.13697

    Article  CAS  Google Scholar 

  • Coops H, Geilen N, Verheij HJ, Boeters R, Van Der Velde G (1996) Interactions between waves, bank erosion and emergent vegetation: an experimental study in a wave tank. Aquatic Botany 53(3–4):187–198. https://doi.org/10.1016/0304-3770(96)01027-3

    Article  Google Scholar 

  • Cregger MA, Veach AM, Yang ZK, Crouch MJ, Vilgalys R, Tuskan GA, Schadt CW (2018) The Populus holobiont: dissecting the effects of plant niches and genotype on the microbiome. Microbiome 6(1):1–14. https://doi.org/10.1186/s40168-018-0413-8

    Article  Google Scholar 

  • Cronin JT, Bhattarai GP, Allen WJ, Meyerson LA (2015) Biogeography of a plant invasion: plant-herbivore interactions. Ecology 96(4):1115–1127

    Article  Google Scholar 

  • Cronin JT, Johnston J, Diaz R (2020) Multiple potential stressors and dieback of Phragmites australis in the Mississippi River Delta, USA: Implications for Restoration. Wetlands. https://doi.org/10.1007/s13157-020-01356-8

  • Davis NM, Proctor DM, Holmes SP, Relman DA, Callahan BJ (2018) Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data. Microbiome 6(1):1–14. https://doi.org/10.1186/s40168-018-0605-2

    Article  Google Scholar 

  • De Souza RSC, Okura VK, Armanhi JSL, Jorrín B, Lozano N, Da Silva MJ, González-Guerrero M, De Araújo LM, Verza NC, Bagheri HC, Imperial J, Arruda P (2016) Unlocking the bacterial and fungal communities assemblages of sugarcane microbiome. Scientific Reports 6(February):1–15. https://doi.org/10.1038/srep28774

    Article  CAS  Google Scholar 

  • Fox J, Weisberg S (2019) An R companion to applied regression (third). Sage

    Google Scholar 

  • Fraedrich SW, Harrington TC, Rabaglia RJ, Service F, Protection FH, Kent N, Head H, Carolina S (2007) Laurel wilt: A new and devastating disease of redbay caused by a fungal symbiont of the exotic redbay ambrosia beetle. Newsletter of the Michigan Entomological Society 52:15–16

    Google Scholar 

  • Fraedrich SW, Harrington TC, Rabaglia RJ, Ulyshen MD, Mayfield AE, Hanula JL, Eickwort JM, Miller DR (2008) A fungal symbiont of the redbay ambrosia beetle causes a lethal wilt in redbay and other Lauraceae in the southeastern United States. Plant Disease 92(2):215–224. https://doi.org/10.1094/PDIS-92-2-0215

    Article  CAS  PubMed  Google Scholar 

  • Friesen ML (2016) Microbially mediated plant functional traits. In F. J. de Bruijn (Ed.), Molecular microbial ecology of the rhizosphere (first, Vol. 1, pp. 1–8). John Wiley & Sons, Inc. https://doi.org/10.1002/9780470015902.a0026282

  • Galgóczy L, Virágh M, Kovács L, Tóth B, Papp T, Vágvölgyi C (2013) Antifungal peptides homologous to the Penicillium chrysogenum antifungal protein (PAF) are widespread among fusaria. Peptides 39(1):131–137. https://doi.org/10.1016/j.peptides.2012.10.016

    Article  CAS  PubMed  Google Scholar 

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Molecular Ecology 2(2):113–118. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x

    Article  CAS  PubMed  Google Scholar 

  • Gedan KB, Kirwan ML, Wolanski E, Barbier EB, Silliman BR (2011) The present and future role of coastal wetland vegetation in protecting shorelines: answering recent challenges to the paradigm. Climatic Change 106(1):7–29. https://doi.org/10.1007/s10584-010-0003-7

    Article  Google Scholar 

  • Hardoim PR, van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, Döring M, Sessitsch A (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiology and Molecular Biology Reviews 79(3):293–320. https://doi.org/10.1128/mmbr.00050-14

    Article  PubMed  PubMed Central  Google Scholar 

  • Hartley SE, Gange AC (2009) Impacts of plant symbiotic Fungi on insect herbivores: mutualism in a multitrophic context. Annual Review of Entomology 54(1):323–342. https://doi.org/10.1146/annurev.ento.54.110807.090614

    Article  CAS  PubMed  Google Scholar 

  • Hauber DP, Saltonstall K, White DA, Hood CS (2011) Genetic variation in the common reed, Phragmites australis, in the Mississippi River Delta marshes: evidence for multiple introductions. Estuaries and Coasts 34(4):851–862. https://doi.org/10.1007/s12237-011-9391-9

    Article  CAS  Google Scholar 

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biometrical Journal 50(3):346–363

    Article  Google Scholar 

  • Howard RJ, Mendelssohn IA (1995) Effect of increased water depth on growth of a common perennial freshwater-intermediate marsh species in coastal Louisiana. Wetlands 15:82–91

    Article  Google Scholar 

  • Huang Y-L, Devan MMN, U’Ren JM, Furr SH, Arnold AE (2016) Pervasive effects of wildfire on foliar endophyte communities in montane Forest trees. Microbial Ecology 71(2):452–468. https://doi.org/10.1007/s00248-015-0664-x

    Article  PubMed  Google Scholar 

  • Jan FG, Hamayun M, Hussain A, Iqbal A, Jan G, Khan SA, Khan H, Lee IJ (2019) A promising growth promoting Meyerozyma caribbica from Solanum xanthocarpum alleviated stress in maize plants. Bioscience Reports 39(10):1–15. https://doi.org/10.1042/BSR20190290

    Article  Google Scholar 

  • Kaiserer L, Oberparleiter C, Weiler-Görz R, Burgstaller W, Leiter E, Marx F (2003) Characterization of the Penicillium chrysogenum antifungal protein PAF. Archives of Microbiology 180(3):204–210. https://doi.org/10.1007/s00203-003-0578-8

    Article  CAS  PubMed  Google Scholar 

  • Knight IA, Cronin JT, Gill M, Nyman JA, Wilson BE, & Diaz R (2020) Investigating plant phenotype, salinity, and infestation by the Roseau cane scale as factors in the die-Back of Phragmites australis in the Mississippi River Delta, USA. Wetlands. https://doi.org/10.1007/s13157-020-01307-3

  • Knight IA, Wilson BE, Gill M, Aviles L, Cronin JT, Nyman JA, Schneider SA, Diaz R (2018) Invasion of Nipponaclerda biwakoensis (Hemiptera: Aclerdidae) and Phragmites australis die-back in southern Louisiana, USA. Biological Invasions 20(10):2739–2744. https://doi.org/10.1007/s10530-018-1749-5

    Article  Google Scholar 

  • Kruess A (2002) Indirect interaction between a fungal plant pathogen and a herbivorous beetle of the weed Cirsium arvense. Oecologia 130(4):563–569. https://doi.org/10.1007/s00442-001-0829-9

    Article  PubMed  Google Scholar 

  • Lambert AM, Casagrande RA (2007) Susceptibility of native and non-native common reed to the non-native mealy plum aphid (Homoptera: Aphididae) in North America. Environmental Entomology 36(2):451–457. https://doi.org/10.1093/ee/36.2.451

    Article  PubMed  Google Scholar 

  • Lambertini C, Mendelssohn IA, Gustafsson MHG, Olesen B, Riis T, Sorrell BK, Brix H (2012) Tracing the origin of Gulf Coast Phragmites (Poaceae): A story of long-distance dispersal and hybridization. American Journal of Botany 99(3):538–551. https://doi.org/10.3732/ajb.1100396

    Article  CAS  PubMed  Google Scholar 

  • Lumibao CY, Formel S, Elango V, Pardue JH, Blum M, Van Bael SA (2018) Persisting responses of salt marsh fungal communities to the Deepwater horizon oil spill. Science of the Total Environment 642:904–913. https://doi.org/10.1016/j.scitotenv.2018.06.077

    Article  CAS  Google Scholar 

  • Martin LJ, Blossey B (2013) The runaway weed: costs and failures of Phragmites australis management in the USA. Estuaries and Coasts 36(3):626–632. https://doi.org/10.1007/s12237-013-9593-4

    Article  Google Scholar 

  • McMurdie PJ, Holmes S (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8(4). https://doi.org/10.1371/journal.pone.0061217

  • Megali L, Glauser G, Rasmann S (2014) Fertilization with beneficial microorganisms decreases tomato defenses against insect pests. Agronomy for Sustainable Development 34(3):649–656. https://doi.org/10.1007/s13593-013-0187-0

    Article  CAS  Google Scholar 

  • Nelson EB, Karp MA (2013) Soil pathogen communities associated with native and non-native Phragmites australis populations in freshwater wetlands. Ecology and Evolution 3(16):5254–5267. https://doi.org/10.1002/ece3.900

    Article  PubMed  PubMed Central  Google Scholar 

  • Nguyen NH, Song Z, Bates ST, Branco S, Tedersoo L, Menke J, Schilling JS, Kennedy PG (2016) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecology 20:241–248. https://doi.org/10.1016/j.funeco.2015.06.006

    Article  Google Scholar 

  • Nilsson RH, Larsson KH, Taylor AFS, Bengtsson-Palme J, Jeppesen TS, Schigel D, Kennedy P, Picard K, Glöckner FO, Tedersoo L, Saar I, Kõljalg U, Abarenkov K (2019) The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Research 47(D1):D259–D264. https://doi.org/10.1093/nar/gky1022

    Article  CAS  PubMed  Google Scholar 

  • Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara R B, Simpson GL, Solymos P, Stevens HH, Szoecs E, Wagner H (2019). Vegan: community ecology package

  • Pagès H, Aboyoun P, Gentleman R, DebRoy S (2020) Biostrings: efficient manipulation of biological strings (R package version 2.56.0)

  • Park MG, Blossey B (2008) Importance of plant traits and herbivory for invasiveness of Phragmites australis (Poaceae). American Journal of Botany 95(12):1557–1568. https://doi.org/10.3732/ajb.0800023

    Article  PubMed  Google Scholar 

  • Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SCM, Bakker PAHM (2014) Induced systemic resistance by beneficial microbes. Annual Review of Phytopathology 52(1):347–375. https://doi.org/10.1146/annurev-phyto-082712-102340

    Article  CAS  PubMed  Google Scholar 

  • Pineda A, Dicke M, Pieterse CMJ, Pozo MJ (2013) Beneficial microbes in a changing environment: are they always helping plants to deal with insects? Functional Ecology 27(3):574–586. https://doi.org/10.1111/1365-2435.12050

    Article  Google Scholar 

  • Pineda A, Soler R, Pozo MJ, Rasmann S, Turlings TCJ (2015) Editorial: above-belowground interactions involving plants, microbes and insects. Frontiers in Plant Science 6(MAY):1–3. https://doi.org/10.3389/fpls.2015.00318

    Article  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D (2020) Nlme: linear and nonlinear mixed effects models

  • Poitevin CG, Veronesi RS, Pimentel IC, Auer CG (2020) Foliar application of endophytic Wickerhamomyces anomalus against grey mould in Eucalyptus dunnii. Biocontrol Science and Technology 30(2):93–102. https://doi.org/10.1080/09583157.2019.1687645

    Article  Google Scholar 

  • Porras-Alfaro A, Bayman P (2011) Hidden Fungi, emergent properties: endophytes and microbiomes. Annual Review of Phytopathology 49(1):291–315. https://doi.org/10.1146/annurev-phyto-080508-081831

    Article  CAS  PubMed  Google Scholar 

  • Price PW, Bouton CE, Gross P, Bruce A, Thompson JN, Weis, a E. (1980) Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annual Review of Ecology and Systematics 11:41–65

    Article  Google Scholar 

  • R Core Team. (2019). R: A language and environment for statistical computing

  • Ramsey III EW, Rangoonwala A (2017) Mapping the change of Phragmites australis live biomass in the lower Mississippi River Delta marshes. US Geological Survey, 20171098

  • Rudgers JA, Clay K (2008) An invasive plant-fungal mutualism reduces arthropod diversity. Ecology Letters 11(8):831–840. https://doi.org/10.1111/j.1461-0248.2008.01201.x

    Article  PubMed  Google Scholar 

  • Safranyik L, Shrimpton DM, Whitney HS (1975) An interpretation of the interaction between lodgepole pine, the mountain pine beetle, and its associated blue stain fungi in western Canada. Management of Lodgepole Pine Ecosystems Symposium Proceedings, 406–428

  • Saltonstall K (2002) Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. Proceedings of the National Academy of Sciences 99(4):2445–2449. https://doi.org/10.1073/pnas.032477999

    Article  CAS  Google Scholar 

  • Shi W, Tan Y, Wang S, Gardiner DM, De Saeger S, Liao Y, Wang C, Fan Y, Wang Z, Wu A (2017) Mycotoxigenic potentials of fusarium species in various culture matrices revealed by mycotoxin profiling. Toxins 9(1). https://doi.org/10.3390/toxins9010006

  • Shikano I, Rosa C, Tan C-W, Felton GW (2017) Tritrophic interactions: microbe-mediated plant effects on insect herbivores. Annual Review of Phytopathology 55(1):313–331. https://doi.org/10.1146/annurev-phyto-080516-035319

    Article  CAS  PubMed  Google Scholar 

  • Silliman BR, Bertness MD (2004) Shoreline development drives invasion of Phragmites australis and the loss of plant diversity on New England salt marshes. Conservation Biology 18(5):1424–1434. https://doi.org/10.1111/j.1523-1739.2004.00112.x

    Article  Google Scholar 

  • Stepień Ł, Koczyk G, Waśkiewicz A (2013) Diversity of fusarium species and mycotoxins contaminating pineapple. Journal of Applied Genetics 54(3):367–380. https://doi.org/10.1007/s13353-013-0146-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tellez PH (2019) Tropical plants and fungal symbionts: leaf functional traits as drivers of plant-fungal interactions. Tulane University School of Science and Engineering

  • U’Ren JM, Arnold AE (2017) Illumina MiSeq dual-barcoded two-step PCR amplicon sequencing protocol. Protocols Io. https://doi.org/10.17504/protocols.io.fs9bnh6

  • U’Ren JM, Lutzoni F, Miadlikowska J, Laetsch AD, Arnold AE (2012) Host and geographic structure of endophytic and endolichenic fungi at a continental scale. American Journal of Botany 99(5):898–914. https://doi.org/10.3732/ajb.1100459

    Article  PubMed  Google Scholar 

  • Van Bael S, Estrada C, Arnold AE (2017) Chapter 6: foliar endophyte communities and leaf traits in tropical trees. In the fungal community: its organization and role in the ecosystem (pp. 79–94). CRC press

  • Venables W, Ripley B (2002) Modern applied statistics with S, Fourth edition (Fourth Edition). Springer

  • Visser JM, Sandy ER (2009) The effects of flooding on four common Louisiana marsh plants. Gulf of Mexico Science 27:21–29

    Article  Google Scholar 

  • White TJ, Bruns TD, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: A Guide to Methods and Applications 18(1):315–322

    Google Scholar 

  • Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York

    Book  Google Scholar 

  • Zhai LF, Liu J, Zhang MX, Hong N, Wang GP, Wang LP (2013) The first report of leaf spots in Aloe vera caused by Nigrospora oryzae in China. Plant Disease 97(9):1256

    Article  CAS  Google Scholar 

  • Zhang LX, Li SS, Tan GJ, Shen JT, He T (2012) Zhang, L. X., et al. "first report of Nigrospora oryzae causing leaf spot of cotton in China. Plant disease, 96(9), 1379

  • Zheng L, Shi F, Kelly D, Hsiang T (2012) First report of leaf spot of Kentucky bluegrass (Poa pratensis) caused by Nigrospora oryzae in Ontario. Plant Disease 96(6):909

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Funding was provided by the Louisiana State Board of Regents grant LEQSF(2017–20)-RD-A-14, the Louisiana Native Plant Society, and the Tulane Department of Ecology and Evolutionary Biology Student Research Grant. Thank you to the two anonymous reviewers for their incredibly thorough feedback to help us better this manuscript. We would also like to thank members of the Farrer Lab at Tulane University for help with field work, sample preparation, and sequencing, as well as the Louisiana Department of Wildlife and Fisheries, particularly Trebor Victoriano, for providing us with transport to and from the research sites.

Availability of Data and Material

All data and materials are available for download at https://doi.org/10.5061/dryad.hmgqnk9hz.

Code Availability

All code available upon request from the corresponding author.

Funding

Funding provided by the Louisiana State Board of Regents grant LEQSF(2017–20)-RD-A-14, the Louisiana Native Plant Society, and the Tulane Department of Ecology and Evolutionary Biology Student Research Grant.

Author information

Authors and Affiliations

Authors

Contributions

CB and EF conceived of the presented idea and developed the theory. CB carried out the experiment, performed statistical analyses, and wrote the manuscript with the support of EF.

Corresponding author

Correspondence to Caitlin Bumby.

Ethics declarations

Conflicts of Interest/Competing Interests

We know of no conflicts of interest or competing interests associated with this publication, and there has been no significant financial support for this work that could have influenced its outcome.

Ethics Approval

Not applicable.

Consent to Participate

Not applicable.

Consent for Publication

As Corresponding Author, I confirm that the manuscript has been read and approved for submission by all the named authors.

Additional information

Publisher’s Note

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

Supplementary Information

ESM 1

(PDF 323 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bumby, C., Farrer, E.C. Nipponaclerda Biwakoensis Infestation of Phragmites australis in the Mississippi River Delta, USA: Do Fungal Microbiomes Play a Role?. Wetlands 42, 15 (2022). https://doi.org/10.1007/s13157-021-01514-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s13157-021-01514-6

Keywords

Navigation