Hostname: page-component-848d4c4894-mwx4w Total loading time: 0 Render date: 2024-06-19T14:08:33.348Z Has data issue: false hasContentIssue false
  • English
  • Français

Fungal pathogens and arbuscular mycorrhizal fungi of abandoned agricultural fields: potential limits to restoration

Published online by Cambridge University Press:  09 August 2019

Bridget E. Hilbig Open the ORCID record for Bridget E. Hilbig [Opens in a new window]  and
Edith B. Allen
Bridget E. Hilbig*
Affiliation:
Assistant Professor, Department of Botany, Weber State University, Ogden, UT, USA
Edith B. Allen
Affiliation:
Professor, Department of Botany and Plant Sciences and Center for Conservation Biology, University of California–Riverside, Riverside, CA, USA
*
Author for correspondence: Bridget E. Hilbig, Department of Botany, Weber State University, 1415 Edvalson Road, Ogden, UT 84408, USA. (Email: bridgethilbig@weber.edu)
Get access Rights & Permissions [Opens in a new window]

Abstract

Little is known about impacts of soilborne pathogen legacies on reestablishment of native plant species in abandoned agricultural fields. We tested whether pathogens found in abandoned citrus orchards affect growth of native and invasive plant species in a controlled greenhouse experiment. In previous research, we identified several species of ascomycete (Fusarium spp.) and oomycete (Pythium spp.) pathogens from field roots and soils. The invasive annual grass, ripgut brome [Bromus diandrus (Roth.)], and native forbs, common fiddleneck [Amsinckia intermedia Fisch. & C.A. Mey.], coastal tidytips [Layia platyglossa (Fisch. & C.A. Mey.) A. Gray], and California goldfields [Lasthenia californica (DC. ex Lindl.)], were grown together in four different field soil treatments. Using pesticides on soils collected from abandoned citrus fields, we created four soil treatments that excluded different groups of potential pathogens: (1) untreated control (2) metalaxyl (oomyceticide) (3) fludioxonil (fungicide), and (4) steam-sterilized. Fludioxonil increased aboveground biomass of L. platyglossa (P = 0.005) and L. californica (P= 0.02) compared with sterile and metalaxyl-treated soils. Lasthenia californica had decreased arbuscular mycorrhizal colonization with metalaxyl, suggesting metalaxyl has non-target effects on mycorrhizae. Fludioxonil decreased potential pathogens in L. californica roots while having no effect on mycorrhizal colonization. Bromus diandrus had higher biomass in sterile and fludioxonil-treated soils than untreated soils (P = 0.0001), suggesting a release from soilborne pathogens. The release from soilborne pathogens with the use of fludioxonil in both native forbs and B. diandrus, combined with overall higher biomass across treatments in B. diandrus, suggests that pathogen impacts in a field setting are insufficient to reduce success of this invasive grass, and use of a fungicide would not benefit native species in mixed stands with B. diandrus.

Keywords

Kelly Lyons, Trinity UniversityBromus diandrusfludioxonilmetalaxylsoilborne pathogenssoil legacy effects
Type
Research Article
Information
Invasive Plant Science and Management , Volume 12 , Issue 3 , September 2019 , pp. 186 - 193
Copyright
© Weed Science Society of America 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Afek, U, Menge, JA, Johnson, ELV (1991) Interaction among mycorrhizae, soil solarization, metalaxyl, and plants in the field. Plant Dis 75:665–671CrossRefGoogle Scholar
Allen, EB, Cox, RD, Tennant, T, Kee, SN, Deutschman, DH (2005a) Landscape restoration in southern California forblands: response of abandoned farmland to invasive annual grass control. Isr J Plant Sci 53:237–245CrossRefGoogle Scholar
Allen, MF, Allen, EB, Gomez-Pompa, A (2005b) Effects of mycorrhizae and nontarget organisms on restoration of a seasonal tropical forest in Quintana Roo, Mexico: factors limiting tree establishment. Restor Ecol 13:325–333CrossRefGoogle Scholar
Altieri, MA (1999) The ecological role of biodiversity in agroecosystems. Agric Ecosyst Environ 74:19–31CrossRefGoogle Scholar
Bever, JD (1994) Feedback between plants and their soil communities in an old field community. Ecology 75:1965–1977CrossRefGoogle Scholar
Bonet, A (2004) Secondary succession of semi-arid Mediterranean old-fields in south-eastern Spain: insights for conservation and restoration of degraded lands. J Arid Environ 56:213–233CrossRefGoogle Scholar
Borowicz, VA (2001) Do arbuscular mycorrhizal fungi alter plant–pathogen relations? Ecology 82:3057–3068Google Scholar
Bullock, DG (1992) Crop rotation. Crit Rev Plant Sci 11:309–326CrossRefGoogle Scholar
Callaway, RM, Bedmar, EJ, Reinhart, KO, Silvan, CG, Klironomos, J (2011) Effects of soil biota from different ranges on Robinia invasion: acquiring mutualists and escaping pathogens. Ecology 92:1027–1035CrossRefGoogle ScholarPubMed
Callaway, RM, Thelen, GC, Barth, S, Ramsey, PW, Gannon, J E (2004a) Soil fungi alter interactions between the invader Centaurea maculosa and North American natives. Ecology 85:1062–1071CrossRefGoogle Scholar
Callaway, RM, Thelen, GC, Rodriguez, A, Holben, WE (2004b) Soil biota and exotic plant invasion. Nature 427:731–733CrossRefGoogle ScholarPubMed
Carrenho, R, Bononin, VLR, Graciolli, LA (2000) Effect of the fungicides Fosetyl-Al and Metalaxyl on arbuscular mycorrhizal colonization of seedlings of Citrus sinensis (L.) Osbeck grafted onto C. limon (L.) Burmf. Acta Sci 22:305–310Google Scholar
Cohen, Y, Coffey, MD (1986) Systemic fungicides and the control of oomycetes. Annu Rev Phytopathol 24:311–338CrossRefGoogle Scholar
Cramer, VA, Hobbs, RJ, Standish, RJ (2008) What’s new about old fields? Land abandonment and ecosystem assembly. Trends Ecol Evol 23:104–112CrossRefGoogle ScholarPubMed
Davidse, LC, Gerritsma, OCM, Ideler, J, Pie, K, Velthuis, GCM (1988) Antifungal modes of action of metalaxyl, cyprofuram, benalaxyl and oxadixyl in phenylamide-sensitive and phenylamide-resistant strains of Phytophthora megasperma f. sp. medicaginis and Phytophthora infestans. Crop Prot 7:347–355CrossRefGoogle Scholar
Filser, J, Fromm, H, Nagel, RF, Winter, K (1995) Effects of previous intensive agricultural management on microorganisms and the biodiversity of soil fauna. Plant Soil 170:123–129CrossRefGoogle Scholar
Fisher, DJ, Hayes, AL (1982) Mode of action of the systemic fungicides furalaxyl, metalaxyl and ofurace. Pestic Sci 13:330–339CrossRefGoogle Scholar
Groth, DE, Martinson, CA (1983) Increased endomycorrhizal infection of maize and soybeans after soil treatment and metalaxyl. Plant Dis 67:1377–1378CrossRefGoogle Scholar
Hersh, MH, Vilgalys, R, Clark, JS (2012) Evaluating the impacts of multiple generalist fungal pathogens on temperate tree seedling survival. Ecology 93:511–520CrossRefGoogle ScholarPubMed
Hetrick, BAD, Wilson, GWT (1991) Effects of mycorrhizal fungus species and metalaxyl application on microbial suppression of mycorrhizal symbiosis. Mycologia 83:97–102CrossRefGoogle Scholar
Hilbig, BE (2015) Ecological Assembly Rules and Soil Legacy Effects in the Restoration of an Invaded Plant Community. Ph.D thesis. Riverside: University of California–Riverside. http://escholarship.org/uc/item/42g359z9 122 p. Accessed: June 11, 2016Google Scholar
Hilbig, BE, Allen, EB (2015) Plant–soil feedbacks and competitive interactions between invasive Bromus diandrus and native forb species. Plant Soil 392:191–203CrossRefGoogle Scholar
Jabaji-Hare, SH, Kendrick, WB (1987) Response of an endomycorrhizal fungus in Allium porrum L. to different concentrations of the systemic fungicides, metalaxyl (Ridomil®) and fosetyl-al (Aliette®). Soil Biol Biochem 19:95–99CrossRefGoogle Scholar
Jin, H, Germida, JJ, Walley, FL (2013) Suppressive effects of seed-applied fungicides on arbuscular mycorrhizal fungi (AMF) differ with fungicide mode of action and AMF species. Appl Soil Ecol 72:22–30CrossRefGoogle Scholar
Johnson, NC, Pfleger, FL (1992) Vesicular-arbuscular mycorrhizae and cultural stresses. Pages 71–99 in Bethlenfalvay, GJ, ed. Mycorrhizae in Sustainable Agriculture (ASA/SSSA Special Publication No. 54). Madison, WI: American Society of AgronomyGoogle Scholar
Johnson, NC, Rowland, DL, Corkidi, L, Allen, EB (2008) Characteristics of plant winners and losers during grassland eutrophication - importance of biomass allocation and mycorrhizal function. Ecology 89:2868–2878CrossRefGoogle Scholar
Kardol, P, Cornips, NJ, van Kempen, MML, Bakx-Schotman, JMT, van der Putten, WH (2007) Microbe-mediated plant–soil feedback causes historical contingency effects in plant community assembly. Ecol Monogr 77:147–162CrossRefGoogle Scholar
Klironomos, JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70CrossRefGoogle ScholarPubMed
Kormanik, PP, McGraw, AC (1982) Quantification of vesicular-arbuscular mycorrhizae in plant roots. Pages 37–45 in Schenck, NC, ed. Methods and Principles of Mycorrhizal Research. St. Paul, MN: The American Phytopathological SocietyGoogle Scholar
Koske, RE, Gemma, JN (1989) A modified procedure for staining roots to detect va-mycorrhizas. Mycol Res 92:486–505CrossRefGoogle Scholar
Kulmatiski, A, Beard, KH (2008) Decoupling plant-growth from land-use legacies in soil microbial communities. Soil Biol Biochem 40:1059–1068CrossRefGoogle Scholar
Kulmatiski, A, Beard, KH, Stark, JM (2006) Soil history as a primary control on plant invasion in abandoned agricultural fields. J Appl Ecol 43:868–876CrossRefGoogle Scholar
MacDonald, D, Crabtree, JR, Wiesinger, G, Dax, T, Stamou, N, Fleury, P, Lazpita, JG, Gibon, A (2000) Agricultural abandonment in mountain areas of Europe: environmental consequences and policy response. J Environ Manage 59:47–69CrossRefGoogle Scholar
Mangan, SA, Schnitzer, SA, Herre, EA, Mack, KML, Valencia, MC, Sanchez, EI, Bever, JD (2010) Negative plant–soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466:752–755CrossRefGoogle Scholar
Marushia, RG, Allen, EB (2011) Control of exotic annual grasses to restore native forbs in abandoned agricultural land. Restor Ecol 19:45–54CrossRefGoogle Scholar
Middleton, EL, Bever, JD (2012) Inoculation with a native soil community advances succession in a grassland restoration. Restor Ecol 20:218–226CrossRefGoogle Scholar
Miller, RM (2002) The function of mycorrhizal fungi in soil restoration. Pages 21–22 in International Workshop—Microbial Function in Revegetation Process of Degraded Terrestrial Environments: From Gene to Ecosystem. Tokyo, Japan, November 29, 2002Google Scholar
Mills, KE, Bever, JD (1998) Maintenance of diversity within plant communities: soil pathogens as agents of negative feedback. Ecology 79:1595–1601CrossRefGoogle Scholar
Minnich, RA (2008) California’s Fading Wildflowers: Lost Legacies and Biological Invasions. Berkeley, CA: University of California Press. 360 pGoogle Scholar
Murillo-Williams, A, Pedersen, P (2008) Arbuscular mycorrhizal colonization response to three seed-applied fungicides. Agron J 100:795–800CrossRefGoogle Scholar
Nelson, JW, Zinn, CJ, Strahorn, AT, Watson, EB, Dunn, JE (1919) Soil survey of the Los Angeles area, California. Washington, DC: U.S. Department of Agriculture. 78 pGoogle Scholar
Newsham, KK, Fitter, AH, Watkinson, AR (1995) Arbuscular mycorrhiza protect an annual grass from root pathogenic fungi in the field. J Ecol 83:991–1000CrossRefGoogle Scholar
Oliveira, AAR (1992) Effects of the fungicides metalaxyl and fosetyl-Al on endomycorrhizal development and growth of Rangpur lime. Fitopatologia Brasileira 17:75–79Google Scholar
Pringle, A, Bever, JD, Gardes, M, Parrent, JL, Rillig, MC, Klironomos, JN (2009) Mycorrhizal symbioses and plant invasions. Annu Rev Ecol Evol S 40:699–715CrossRefGoogle Scholar
Pywell, RF, Bullock, J M, Tallowin, JB, Walker, K J, Warman, EA, Masters, G (2007) Enhancing diversity of species-poor grasslands: an experimental assessment of multiple constraints. J Appl Ecol 44:81–94CrossRefGoogle Scholar
Pywell, RF, Meek, WR, Webb, NR, Putwain, PD and Bullock, JM (2011) Long-term heathland restoration on former grassland: the results of a 17-year experiment. Biol Conserv 144:1602–1609CrossRefGoogle Scholar
R Development Core Team (2013) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. http://www.R-project.org/ Accessed: May 1, 2014Google Scholar
Richter, BS, Stutz, JC (2002) Mycorrhizal inoculation of big sacaton: implications for grassland restoration of abandoned agricultural fields. Restor Ecol 10:607–616CrossRefGoogle Scholar
Rosslenbroich, HJ, Stuebler, D (2000) Botrytis cinerea—history of chemical control and novel fungicides for its management. Crop Prot 19:557–561CrossRefGoogle Scholar
Shetty, PK, Magu, SP (1997) Influence of metalaxyl on Glomus fasciculatum associated with wheat (Triticum aestivum L). Curr Sci India 72:275–277Google Scholar
Smith, SE, Read, D (2008) Mycorrhizal Symbiosis. 3rd ed. London: Elsevier. 800 pGoogle Scholar
Standish, RJ, Cramer, VA, Wild, SL, Hobbs, RJ (2007) Seed dispersal and recruitment limitation are barriers to native recolonization of old-fields in western Australia. J Appl Ecol 44:435–445CrossRefGoogle Scholar
van der Heijden, MGA, Boller, T, Wiemken, A, Sanders, IR (1998) Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology 79:2082–2091CrossRefGoogle Scholar
Walker, KJ, Stevens, PA, Stevens, DP, Mountford, JO, Manchester, SJ, Pywell, RF (2004) The restoration and re-creation of species-rich lowland grassland on land formerly managed for intensive agriculture in the UK. Biol Conserv 119:1–18CrossRefGoogle Scholar
Yelenik, SG, Levine, JM (2011) The role of plant–soil feedbacks in driving native-species recovery. Ecology 92:66–74CrossRefGoogle ScholarPubMed
Zhang, JX (2007) The potential of a new fungicide fludioxonil for stem-end rot and green mold control on Florida citrus fruit. Postharvest Biol Technol 46:262–270CrossRefGoogle Scholar
Zumkehr, A, Campbell, JE (2013) Historical US cropland areas and the potential for bioenergy production on abandoned croplands. Environ Sci Technol 47:3840–3847CrossRefGoogle Scholar