Skip to main content
Log in

Geographic and genetic variation in susceptibility of Butomus umbellatus to foliar fungal pathogens

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Large-scale patterns of plant invasions may reflect regional heterogeneity in biotic and abiotic factors and genetic variation within and between invading populations. Having information on how effects of biotic resistance vary spatially can be especially important when implementing biological control because introduced agents may have different impacts through interactions with host-plant genotype, local environment, or other novel enemies. We conducted a series of field surveys and laboratory studies to determine whether there was evidence of biotic resistance, as foliar fungal pathogens, in two introduced genotypes (triploid G1, diploid G4) of the Eurasian wetland weed, Butomus umbellatus L. in the USA. We tested whether genotypes differed in disease attack and whether spatial patterns in disease incidence were related to geographic location or climate for either genotype. We surveyed 27 B. umbellatus populations (17 G1, 10 G4) to determine disease incidence and associated fungal pathogens. For a subset of plant populations, we isolated foliar fungi and tested pathogenicity of three isolates in laboratory assays. After accounting for location (latitude, climate), G1 plants had lower disease incidence than G4 plants in the field (38% vs. 70%) but similar pathogen richness. In contrast, bioassays revealed G1 plants consistently received a higher damage score and had larger leaf lesions regardless of pathogen. The seemingly contradictory results between the field and laboratory may be due to climatic differences between areas that limit the regional pool of pathogens or their effect on plant genotype. These results demonstrate that two widespread B. umbellatus genotypes exhibit different susceptibility to pathogens and effectiveness of pathogen biological controls may depend on local conditions.

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

Similar content being viewed by others

References

  • Agrios GN (2015) Plant pathology, 5th edn. Academic Press, London

    Google Scholar 

  • Allen WJ, Meyerson LA, Cummings D, Anderson J, Bhattarai GP, Cronin JT (2017) Biogeography of a plant invasion: drivers of latitudinal variation in enemy release. Glob Ecol Biogeogr 26:435–446. https://doi.org/10.1111/geb.12550

    Article  Google Scholar 

  • Anderson LC, Zeis CD, Alam SF (1974) Phytogeography and possible origins of Butomus in North America. Bull Torrey Bot Club 101:292–296

    Article  Google Scholar 

  • Bargeron CT, Moorhead DJ (2007) EDDMapS—early detection and distribution mapping system for the southeast exotic pest plant council Wildland. Weeds 10:4–8

    Google Scholar 

  • Bhattarai GP, Meyerson LA, Cronin JT (2017) Geographic variation in apparent competition between native and invasive Phragmites australis. Ecology 98:349–358

    Article  Google Scholar 

  • Bohanec B (2003) Ploidy determination using flow cytometry. In: Maluszynski M, Kasha KJ, Forster BP, Szarejko I (eds) Doubled haploid production in crop plants: a manual. Springer, Dordrecht, pp 397–403. https://doi.org/10.1007/978-94-017-1293-4_52

    Chapter  Google Scholar 

  • Boughton AJ, Pemberton RW (2011) Limited field establishment of a weed biocontrol agent, Floracarus perrepae (Acariformes: Eriophyidae), against Old World climbing fern in Florida-a possible role of mite resistant plant genotypes. Environ Entomol 40:1448–1457

    Article  Google Scholar 

  • Bowen JL et al (2017) Lineage overwhelms environmental conditions in determining rhizosphere bacterial community structure in a cosmopolitan invasive plant. Nat Commun 8:433. https://doi.org/10.1038/s41467-017-00626-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burdon J, Groves R, Cullen J (1981) The impact of biological control on the distribution and abundance of Chondrilla juncea in south-eastern Australia. J Appl Ecol 18:957–966

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2003) Model selection and multimodel inference: a practical information-theoretic approach. Springer, Berlin

    Google Scholar 

  • Burrell AM et al (2015) Exploring origins, invasion history and genetic diversity of Imperata cylindrica (L.) P. Beauv. (Cogongrass) in the United States using genotyping by sequencing. Mol Ecol 24:2177–2193. https://doi.org/10.1111/mec.13167

    Article  CAS  PubMed  Google Scholar 

  • Bussey M, Stevenson W (1991) A leaf disk assay for detecting resistance to early blight caused by Alternaria solani in juvenile potato plants. Plant Dis 75:385–390

    Article  Google Scholar 

  • Castillo JM et al (2018) Low genetic diversity contrasts with high phenotypic variability in heptaploid Spartina densiflora populations invading the Pacific coast of North America. Ecol Evolut 8:4992–5007

    Article  Google Scholar 

  • Croll D, McDonald BA (2017) The genetic basis of local adaptation for pathogenic fungi in agricultural ecosystems. Mol Ecol 26:2027–2040. https://doi.org/10.1111/mec.13870

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Delaat A, Gohde W, Vogelzakg M (1987) Determination of ploidy of single plants and plant populations by flow cytometry. Plant Breed 99:303–307

    Article  Google Scholar 

  • DeLoach C et al. (2007) Beginning success of biological control of saltcedars (Tamarix spp.) in the southwestern USA. In: XII international symposium on biological control of weeds. La Grande Motte, France. pp 22–27

  • DeRivera C, Ruiz GM, Hines AH, Jivoff P (2005) Biotic resistance to invasion: native predator limits abundance and distribution of an introduced crab. Ecology 86:3364–3376. https://doi.org/10.1890/05-0479

    Article  Google Scholar 

  • Develey-Rivière M-P, Galiana E (2007) Resistance to pathogens and host developmental stage: a multifaceted relationship within the plant kingdom. New Phytol 175:405–416. https://doi.org/10.1111/j.1469-8137.2007.02130.x

    Article  PubMed  Google Scholar 

  • Dhingra OD, Sinclair JB (1995) Basic plant pathology methods. CRC Press, Boca Raton

    Google Scholar 

  • Domsch KH, Gams W, Anderson T-H (1980) Compendium of soil fungi. Volume 1. Academic Press (London) Ltd

  • Eckert CG, Massonnet B, Thomas JJ (2000) Variation in sexual and clonal reproduction among introduced populations of flowering rush, Butomus umbellatus (Butomaceae). Can J Bot 78:437–446

    Google Scholar 

  • Eckert CG, Lui K, Bronson K, Corradini P, Bruneau A (2003) Population genetic consequences of extreme variation in sexual and clonal reproduction in an aquatic plant. Mol Ecol 12:331–344. https://doi.org/10.1046/j.1365-294X.2003.01737.x

    Article  PubMed  Google Scholar 

  • Ellis M (1971) Dematiaceous Hyphomycetes.,(Commonwealth Mycological Institute: Kew, Surrey). the Eastern Press Ltd

  • Flory SL, Clay K (2013) Pathogen accumulation and long-term dynamics of plant invasions. J Ecol 101:607–613. https://doi.org/10.1111/1365-2745.12078

    Article  Google Scholar 

  • Foley JR, Minteer C, Tipping PW (2016) Differences in seasonal variation between two biotypes of Megamelus scutellaris (Hemiptera: Delphacidae), a biological control agent for Eichhornia crassipes (Pontederiaceae) in Florida. Fla Entomol 99:569–571. https://doi.org/10.1653/024.099.0340

    Article  Google Scholar 

  • Freedman J, Harms N (2017) Rearing and release of Megamelus scutellaris Berg (Hemiptera: Delphacidae) for biological control of water hyacinth in 2015. ERDC-EL Vicksburg United States

  • Freestone AL, Ruiz GM, Torchin ME (2013) Stronger biotic resistance in tropics relative to temperate zone: effects of predation on marine invasion dynamics. Ecology 94:1370–1377. https://doi.org/10.1890/12-1382.1

    Article  Google Scholar 

  • Gandon S, Van Zandt PA (1998) Local adaptation and host-parasite interactions. Trends Ecol Evol 13:214–216. https://doi.org/10.1016/S0169-5347(98)01358-5

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Rossi D, Rank N, Strong DR (2003) Potential for self-defeating biological control? Variation in herbivore vulnerability among invasive Spartina genotypes. Ecol Appl 13:1640–1649

    Article  Google Scholar 

  • Gaskin JF, Schwarzländer M, Kinter CL, Smith JF, Novak SJ (2013) Propagule pressure, genetic structure, and geographic origins of Chondrilla juncea (Asteraceae): an apomictic invader on three continents. Am J Bot 100:1871–1882. https://doi.org/10.3732/ajb.1200621

    Article  PubMed  Google Scholar 

  • Gbur E et al (2012) Analysis of generalized linear mixed models in the agricultural and natural resources sciences. Crop Science Society of America, Fitchburg

    Google Scholar 

  • Grodowitz M, Nachtrieb J, Harms N, Freedman J (2010) Suitability of using introduced Hydrellia spp. for management of monoecious Hydrilla verticillata (Lf) Royle. ERDC/TN APCRP-BC-17. Vicksburg,MS, U.S. Army Engineer Research and Development Center. p 14

  • Hahn MA, van Kleunen M, Müller-Schärer H (2012) Increased phenotypic plasticity to climate may have boosted the invasion success of polyploid Centaurea stoebe. Plos One 7:e50284. https://doi.org/10.1371/journal.pone.0050284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hao G-Y, Lucero ME, Sanderson SC, Zacharias EH, Holbrook NM (2013) Polyploidy enhances the occupation of heterogeneous environments through hydraulic related trade-offs in Atriplex canescens (Chenopodiaceae). New Phytol 197:970–978. https://doi.org/10.1111/nph.12051

    Article  PubMed  Google Scholar 

  • Harms NE, Grodowitz MJ (2011) Overwintering biology of Hydrellia pakistanae, a biological control agent of hydrilla. J Aquat Plant Manag 49:114–117

    Google Scholar 

  • Harms NE, Shearer JF (2015) Apparent herbivory and indigenous pathogens of invasive flowering rush (Butomus umbellatus L.) in the Pacific Northwest. ERDC/TN-APCRP-BC-35. Vicksburg, MS: US Army Engineer Research and Development Center. p 12

  • Harms NE, Purcell M, Zhang J, Grodowitz MJ, Ding J (2017) Surveys for biological control agents of Hydrilla verticillata in the Peoples Republic of China in 2013. US Army Engineer Research and Development Center, Environmental Laboratory Vicksburg United States

  • He K, Rocchini D (2013) Plant invasion and imaging spectroscopy. In: Wang G, Weng Q (eds) Remote sensing of natural resources. CRC Press, Boca Raton

    Google Scholar 

  • Higgins SI, Richardson DM (2014) Invasive plants have broader physiological niches. Proc Natl Acad Sci USA 111:10610–10614. https://doi.org/10.1073/pnas.1406075111

    Article  CAS  PubMed  Google Scholar 

  • Hilker FM, Lewis MA, Seno H, Langlais M, Malchow H (2005) Pathogens can slow down or reverse invasion fronts of their hosts. Biol Invasions 7:817–832. https://doi.org/10.1007/s10530-005-5215-9

    Article  Google Scholar 

  • Hoffmann AA, Blows MW (1994) Species borders: ecological and evolutionary perspectives. Trends Ecol Evol 9:223–227. https://doi.org/10.1016/0169-5347(94)90248-8

    Article  CAS  PubMed  Google Scholar 

  • Hokkanen HMT, Pimentel D (1989) New associations in biological control: theory and practice. Can Entomol 121:829–840. https://doi.org/10.4039/Ent121829-10

    Article  Google Scholar 

  • King KC, Seppälä O, Neiman M (2012) Is more better? Polyploidy and parasite resistance. Biol Lett 8:598–600. https://doi.org/10.1098/rsbl.2011.1152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kliber A, Eckert CG, Geber M (2005) Interaction between founder effect and selection during biological invasion in an aquatic plant. Evolution 59:1900–1913. https://doi.org/10.1554/05-253.1

    Article  CAS  PubMed  Google Scholar 

  • Knowlton CH (1923) Butomus umbellatus on the St. Lawrence River. Rhodora 25:220–221

    Google Scholar 

  • Kriticos DJ, Jarošik V, Ota N (2014) Extending the suite of bioclim variables: a proposed registry system and case study using principal components analysis. Methods Ecol Evolut 5:956–960

    Article  Google Scholar 

  • Kwong RM, Sagliocco JL, Harms NE, Butler KL, Green PT, Martin GD (2017) Biogeographical comparison of the emergent macrophyte Sagittaria platyphylla in its native and introduced ranges. Aquat Bot 141:1–9

    Article  Google Scholar 

  • Laine AL (2005) Spatial scale of local adaptation in a plant-pathogen metapopulation. J Evol Biol 18:930–938. https://doi.org/10.1111/j.1420-9101.2005.00933.x

    Article  PubMed  Google Scholar 

  • Laine A-L (2007) Detecting local adaptation in a natural plant–pathogen metapopulation: a laboratory vs. field transplant approach. J Evol Biol 20:1665–1673. https://doi.org/10.1111/j.1420-9101.2007.01359.x

    Article  PubMed  Google Scholar 

  • Levin DA (1983) Polyploidy and novelty in flowering plants. Am Nat 122:1–25

    Article  Google Scholar 

  • Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7:975–989. https://doi.org/10.1111/j.1461-0248.2004.00657.x

    Article  Google Scholar 

  • Liu M, Zhou F, Pan X, Zhang Z, Traw MB, Li B (2018) Specificity of herbivore-induced responses in an invasive species, Alternanthera philoxeroides (alligator weed). Ecol Evolut 8:59–70. https://doi.org/10.1002/ece3.3615

    Article  Google Scholar 

  • Louthan AM, Doak DF, Angert AL (2015) Where and When do Species Interactions Set Range Limits? Trends Ecol Evol 30:780–792. https://doi.org/10.1016/j.tree.2015.09.011

    Article  PubMed  Google Scholar 

  • Lui K, Thompson FL, Eckert CG (2005) Causes and consequences of extreme variation in reproductive strategy and vegetative growth among invasive populations of a clonal aquatic plant, Butomus umbellatus L. (Butomaceae). Biol Invasions 7:427–444

    Article  Google Scholar 

  • Madeira PT, Van TK, Center TD (2004) An improved molecular tool for distinguishing monoecious and dioecious hydrilla. J Aquat Plant Manag 42:28–32

    Google Scholar 

  • Maron JL, Vilà M (2008) Exotic plants and enemy resistance specialization, speciation, and radiation: the evolutionary biology of herbivorous insects, University of California Press, Berkeley and Los Angeles, California. pp 280–295

  • Martin JP (1950) Use of acid, rose bengal, and streptomycin in the plate method for estimating soil fungi. Soil science 69:215–232

    Article  CAS  Google Scholar 

  • Meyerson LA et al (2016) Do ploidy level and nuclear genome size and latitude of origin modify the expression of Phragmites australis traits and interactions with herbivores? Biol Invasions 18:2531–2549

    Article  Google Scholar 

  • Mitchell CE, Blumenthal D, Jarošík V, Puckett EE, Pyšek P (2010) Controls on pathogen species richness in plants’ introduced and native ranges: roles of residence time, range size and host traits. Ecol Lett 13:1525–1535. https://doi.org/10.1111/j.1461-0248.2010.01543.x

    Article  PubMed  PubMed Central  Google Scholar 

  • Morais P, Reichard M (2018) Cryptic invasions: a review. Sci Total Environ 613–614:1438–1448. https://doi.org/10.1016/j.scitotenv.2017.06.133

    Article  CAS  PubMed  Google Scholar 

  • Mukherjee A, Williams D, Wheeler G, Cuda J, Pal S, Overholt W (2012) Brazilian peppertree (Schinus terebinthifolius) in Florida and South America: evidence of a possible niche shift driven by hybridization. Biol Invasions 14:1415–1430

    Article  Google Scholar 

  • Mukwevho L, Simelane D, Olckers T (2017) Host-plant variety and not climate determines the establishment and performance of Aceria lantanae (Eriophyidae), a biological control agent of Lantana camara in South Africa. Exp Appl Acarol 71:103–113

    Article  Google Scholar 

  • Mukwevho L, Olckers T, Simelane DO (2018) Occurrence of different Lantana camara varieties across four South African provinces and their susceptibility to a biotype of the gall-forming mite Aceria lantanae Biocontrol. Sci Tech 28:377–387

    Google Scholar 

  • Ordonez A, Olff H (2013) Do alien plant species profit more from high resource supply than natives? A trait-based analysis. Global Ecol Biogeogr 22:648–658. https://doi.org/10.1111/geb.12019

    Article  Google Scholar 

  • Oswald BP, Nuismer SL (2007) Neopolyploidy and pathogen resistance. Proc Biol Sci 274:2393–2397. https://doi.org/10.1098/rspb.2007.0692

    Article  PubMed  PubMed Central  Google Scholar 

  • Pandit MK, Pocock MJ, Kunin WE (2011) Ploidy influences rarity and invasiveness in plants. J Ecol 99:1108–1115

    Article  Google Scholar 

  • Pandit MK, White SM, Pocock MJO (2014) The contrasting effects of genome size, chromosome number and ploidy level on plant invasiveness: a global analysis. New Phytol 203:697–703. https://doi.org/10.1111/nph.12799

    Article  CAS  PubMed  Google Scholar 

  • Parker JD, Burkepile DE, Hay ME (2006) Opposing effects of native and exotic herbivores on plant invasions. Science 311:1459–1461

    Article  CAS  Google Scholar 

  • Pratt R (1996) Screening for resistance to Sclerotinia trifoliorum in alfalfa by inoculation of excised leaf tissue. Phytopathology 86:923–928

    Article  Google Scholar 

  • Prom L, Cuevas H, Isakeit T, Droleskey R (2015) Excised leaf method for high volume evaluation of sorghum germplasm for resistance against Colletotrichum sublineolum. Plant Pathol 15:11–16

    Article  Google Scholar 

  • Purcell M et al (2019) Exploration for candidate biological control agents of the submerged aquatic weed Hydrilla verticillata, in Asia and Australia 1996–2013. BioControl 64:233–247. https://doi.org/10.1007/s10526-019-09940-6

    Article  Google Scholar 

  • Rasband W (2016) ImageJ. National Institutes of Health, Bethesda

    Google Scholar 

  • Rejmanek M, Richardson DM (1996) What attributes make some plant species more invasive? Ecology 77:1655–1661. https://doi.org/10.2307/2265768

    Article  Google Scholar 

  • Richardson DM, Pyšek P (2006) Plant invasions: merging the concepts of species invasiveness and community invasibility. Prog Phys Geogr Earth Environ 30:409–431. https://doi.org/10.1191/0309133306pp490pr

    Article  Google Scholar 

  • Roach D, Wulff R (1987) Maternal Effects in Plants. Annu Rev Ecol Syst 18:209–235. https://doi.org/10.1146/annurev.es.18.110187.001233

    Article  Google Scholar 

  • Russell A et al (2017) Surveys in Argentina and Uruguay reveal Cyrtobagous salviniae (Coleoptera: Curculionidae) populations adapted to survive temperate climates in southeastern USA. Biol Control 107:41–49. https://doi.org/10.1016/j.biocontrol.2017.01.010

    Article  Google Scholar 

  • Saltonstall K (2002) Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. Proc Natl Acad Sci 99:2445

    Article  CAS  Google Scholar 

  • Sax DF, Stachowicz JJ, Gaines SD (2005) Species invasions: insights into ecology, evolution and biogeography. Sinauer Associates Incorporated

  • Schaffner U et al (2011) Plant invasions, generalist herbivores, and novel defense weapons. Ecology 92:829–835. https://doi.org/10.1890/10-1230.1

    Article  PubMed  Google Scholar 

  • Schmidt JP, Drake JM, Stephens P (2017) Residence time, native range size, and genome size predict naturalization among angiosperms introduced to Australia. Ecol Evolut 7:10289–10300. https://doi.org/10.1002/ece3.3505

    Article  Google Scholar 

  • Seherm H, Coakley SM (2003) Plant pathogens in a changing world. Australas Plant Pathol 32:157–165. https://doi.org/10.1071/ap03015

    Article  Google Scholar 

  • Shearer JF, Durham BD, Harms N (2011) Screening of biological control pathogens isolated from Eurasian watermilfoil. J Aquat Plant Manag 49:118–121

    Google Scholar 

  • Siemann E, Rogers WE (2003) Reduced resistance of invasive varieties of the alien tree Sapium sebiferum to a generalist herbivore. Oecologia 135:451–457. https://doi.org/10.1007/s00442-003-1217-4

    Article  PubMed  Google Scholar 

  • Stricker KB, Harmon PF, Goss EM, Clay K, Luke Flory S (2016) Emergence and accumulation of novel pathogens suppress an invasive species. Ecol Lett 19:469–477. https://doi.org/10.1111/ele.12583

    Article  PubMed  Google Scholar 

  • Stutz S, Hinz HL, Konowalik K, Müller-Schärer H, Oberprieler C, Schaffner U (2016) Ploidy level in the genus Leucanthemum correlates with resistance to a specialist herbivore. Ecosphere 7:e01460. https://doi.org/10.1002/ecs2.1460

    Article  Google Scholar 

  • Tano SA, Halling C, Lind E, Buriyo A, Wikström SA (2015) Extensive spread of farmed seaweeds causes a shift from native to non-native haplotypes in natural seaweed beds. Mar Biol 162:1983–1992. https://doi.org/10.1007/s00227-015-2724-7

    Article  Google Scholar 

  • te Beest M, Le Roux JJ, Richardson DM, Brysting AK, Suda J, Kubešová M, Pyšek P (2012) The more the better? The role of polyploidy in facilitating plant invasions. Ann Bot-London 109:19–45. https://doi.org/10.1093/aob/mcr277

    Article  Google Scholar 

  • terHorst CP, Lau JA (2015) Genetic variation in invasive species response to direct and indirect species interactions. Biol Invasions 17:651–659. https://doi.org/10.1007/s10530-014-0756-4

    Article  Google Scholar 

  • Torchin ME, Mitchell CE (2004) Parasites, pathogens, and invasions by plants and animals. Front Ecol Environ 2:183–190. https://doi.org/10.1890/1540-9295(2004)002%5b0183:ppaibp%5d2.0.co;2

    Article  Google Scholar 

  • Tracy JL, Robbins TO (2009) Taxonomic revision and biogeography of the Tamarix-feeding Diorhabda elongata (Brullé, 1832) species group (Coleoptera: Chrysomelidae: Galerucinae: Galerucini) and analysis of their potential in biological control of Tamarisk. Magnolia Press, Auckland

    Book  Google Scholar 

  • Uecker FA (1993) Development and cytology of Plectosphaerella cucumerina. Mycologia 85:470–479. https://doi.org/10.2307/3760707

    Article  Google Scholar 

  • Van Kleunen M, Weber E, Fischer M (2010) A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol Lett 13:235–245

    Article  Google Scholar 

  • Weir BS, Johnston PR, Damm U (2012) The Colletotrichum gloeosporioides species complex. Stud Mycol 73:115–180. https://doi.org/10.3114/sim0011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Witmer SW (1964) Butomus umbellatus L. in Indiana Castanea. pp 117–119

  • Wolfe LM, Elzinga JA, Biere A (2004) Increased susceptibility to enemies following introduction in the invasive plant Silene latifolia. Ecol Lett 7:813–820. https://doi.org/10.1111/j.1461-0248.2004.00649.x

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank the following people for their assistance in the field, laboratory, or greenhouse to complete this work: J. Parsons, C. Welling, B. DeRossette, and D. Lattuca. Additionally, we thank Aaron Schad and Lynde Dodd for their reviews of this manuscript. Their suggestions, along with those from two anonymous reviewers greatly improved the quality of the manuscript. This work was conducted in partial fulfillment of the requirements for the degree of Doctor of Philosophy at Louisiana State University (NEH).

Funding

This research was supported by the US Army Engineer Research and Development Center Aquatic Plant Control Research Program.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nathan Harms.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

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

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Harms, N., Shearer, J., Cronin, J.T. et al. Geographic and genetic variation in susceptibility of Butomus umbellatus to foliar fungal pathogens. Biol Invasions 22, 535–548 (2020). https://doi.org/10.1007/s10530-019-02109-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-019-02109-3

Keywords

Navigation