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Complex Interactions among Sheep, Insects, Grass, and Fungi in a Simple New Zealand Grazing System

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Abstract

Epichloë fungi (Ascomycota) live within aboveground tissues of grasses and can have important implications for natural and managed ecosystems through production of alkaloids. Nonetheless, vertebrate herbivores may possess traits, like oral secretions, that mitigate effects of alkaloids. We tested if sheep saliva mitigates effects of Epichloë alkaloids on a beetle pest of perennial ryegrass (Lolium perenne L.) in a New Zealand pasture setting. Plants with one of several fungal isolates were clipped with scissors, grazed by sheep, or clipped with sheep saliva applied to cut ends of stems. We then assessed feeding damage by Argentine stem weevils on blade segments collected from experimental plants. We found that clipping plants induced synthesis of an alkaloid that reduces feeding by beetles and that sheep saliva mitigates this effect. Unexpectedly, the alkaloid (perloline) that explains variation in beetle feeding is one produced not by the endophyte, but rather by the plant. Yet, these effects depended upon fungal isolate. Such indirect, complex interactions may be much more common in both managed and natural grassland systems than typically thought and could have implications for managing grazing systems.

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References

  • Bellamy W, Yamauchi K, Wakabayashi H, Takase M, Shimamura S, Tomita M (1994) Antifungal properties of lactoferricin B, a peptide derived from the N-terminal region of bovine lactoferrin. Lett Appl Microbiol 18:230–233

    Article  CAS  Google Scholar 

  • Bouton JH, Latch GCM, Hill NS, Hoveland CS, McCann MA, Watson RH, Parish JA, Hawkins LL, Thompson FN (2002) Re-infection of tall fescue cultivars with non-ergot alkaloid producing endophytes. Agron J 94:567–574

    Article  Google Scholar 

  • Bultman TL, Bell G, Martin WA (2004) A fungal endophyte mediates reversal of wound-induced resistance and constrains tolerance in a grass. Ecology 85:679–685

    Article  Google Scholar 

  • Bush LP (2001) Perloline, the forgotten plant alkaloid. In: Gomide JA, WRS M, da Silva SC (eds) Proceed. XIX Inter. Grassland Congr, São Paulo, pp 461–462

  • Bush LP, Streeter C, Buckner RC (1970) Perloline inhibition of in vitro ruminal cellulose digestion. Crop Sci 10:108–109

    Article  CAS  Google Scholar 

  • Clay K (1988) Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecology 69:10–16

    Article  Google Scholar 

  • Daley GT (1990) The grasslands of New Zealand. In: Langer RHM (ed) Pastures, their ecology and management. Oxford Univ. Press, Auckland, pp 1–38

    Google Scholar 

  • DeBattista JP, Bacon CW, Severson R, Plattner RD, Bouton JH (1990) Indole acetic acid production by the fungal endophytes of tall fescue. Agron J 82:878–880

    Article  CAS  Google Scholar 

  • Denno RF, Peterson ME, Gratton C, Cheng J, Langellotto GA, Huberty AF et al (2008) Feeding-induced changes in plant quality mediate interspecific competition between sap-feeding herbivores. Ecology 81:1814–1827

    Article  Google Scholar 

  • Detling JK, Dyer MI, Proctor-Gregg C, Winn DT (1980) Plant herbivore interactions: examination of potential effects of bison saliva on regrowth of Bouteloua gracilis (H.B.K.) Lag. Oecologia 45:26–31

    Article  PubMed  CAS  Google Scholar 

  • Dunn OJ (1961) Multiple comparisons among means. J Am Stat Assoc 56:52–64

    Article  Google Scholar 

  • Easton HS (2007) Grasses and Neotyphodium endophytes: co-adaptation and adaptive breeding. Euphytica 154:295–306

    Article  Google Scholar 

  • Easton S, Tapper B (2005) Neotyphodium research and application in New Zealand. In: Roberts CA, West CP, Spiers DE (eds) Neotyphodium in cool-season grasses. Blackwell Publ., Ames, pp 35–42

    Chapter  Google Scholar 

  • Fuchs B, Krischke M, Mueller MJ, Krauss J (2017) Herbivore-specific induction of defence metabolites in a grass-endophyte association. Funct Ecol 31:318–324

    Article  Google Scholar 

  • Goldson SL (1982) An examination of the relationship between Argentine stem weevil (Listronotus bonariensis (Kuschel)) and several of its host grasses. New Zeal J Agr Res 25:395–403

    Article  Google Scholar 

  • Goldson SL, Tomasetto F, Popay AJ (2014) Biological control against invasive species in simplified ecosystems: its triumphs and emerging threats. Curr Opin Insect Sci 5:50–56

    Article  Google Scholar 

  • Grimmett RE, Waters DF (1943) A fluorescent alkaloid in ryegrass (Lolium perenne L.) II. Extract from fresh ryegrass and separation from other bases. N Z J Sci 24:151B

    Google Scholar 

  • Hovin AW, Buckner RC (1983) Alkaloids in tall fescue and reed canary grass. In: Rechcigl M (ed) Handbook of naturally occurring food toxicants. CRC Press, Boca Raton, pp 241–247

    Google Scholar 

  • IBM CORP (2011) IBM SPSS statistics for windows. Version 21.0. IBM Corp, Armonk

    Google Scholar 

  • Johnson LJ, Debonth ACM, Brigg LR, Caradu SD, Finch SC, Fleetwood DJ et al (2013) The exploitation of Epichloë endophytes for agricultural benefit. Fungal Divers 60:171–188

    Article  Google Scholar 

  • Kauppinen M, Saikkonen K, Helander M, Pirttila AM, Wali PR (2016) Epichloë grass endophytes in sustainable agriculture. Nat Plants 2:1–7

    Google Scholar 

  • Liu J, Wang L, Wang D, Bonser SP, Sun F, Zhou Y et al (2012) Plants can benefit from herbivory: stimulatory effects of sheep saliva on growth of Leymus chinensis. PLoS ONE 7 (1):e29259. https://doi.org/10.1371/journal.pone.0029259

  • Moore JR, Pratley PE, Mace WJ, Weston LA (2015) Variation in alkaloid production from genetically diverse Lolium accessions infected with Epichloë species. J Agric Food Chem 63:10355–10365

    Article  PubMed  CAS  Google Scholar 

  • Pan J, Bhardwaj M, Nagabhyru P, Grossman RB, Schardl CL (2014) Enzymes from fungal and plant origin required for chemical diversification of insecticidal loline alkaloids in grass-Epichloë symbiota. PLoS ONE 9:e115590. https://doi.org/10.1371/journal.pone.0115590

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Popay AJ, McNeil MR, Goldson SL, Ferguson CM (2011) The current status of Argentine stem weevil (Listronotous bonariensis) as a pest in the North Island in New Zealand. N Z Plant Protect-SE 64:55–63

    Google Scholar 

  • Ramankuttry N, Evan AT, Monfreda C, Foley JA (2008) Farming the planet: 1. Geographic distribution of global agricultural lands in the year 2000. Global Biogeochem Cy 22:GB1003

  • Reddy PV, Lam CK, Belanger FC (1996) Mutualistic fungal endophytes express a proteinase that is homologous to proteases suspected to be important in fungal pathogenicity. Plant Physiol 111:1209–1218

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rodriguez RJ, White JF Jr, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330

    Article  PubMed  CAS  Google Scholar 

  • Rowan DD, Gaynor DL (1986) Isolation of feeding deterrents against Argentine stem weevil from ryegrass infected with the endophyte Acremonium loliae. J Chem Ecol 12:647–658

    Article  PubMed  CAS  Google Scholar 

  • Rupport KG, Matthew C, McKenzie CM, Popay AJ (2017) Impact of Epichloe endophytes on adult Argentine stem weevil damage to perennial ryegrass seedlings. Entomol Exp Appl 163:328–337

    Article  CAS  Google Scholar 

  • Saha DC, Jackson MA, Johnson-Cicalese JM (1988) A rapid staining method for detection of endophytic fungi in turf and forage grasses. Phytopathology 78:237–239

    Article  CAS  Google Scholar 

  • Salminen SO, Richmond DS, Grewal SK, Grewal PS (2005) Influence of temperature on alkaloid levels and fall armyworm performance in endophytic tall fescue and perennial ryegrass. Entomol Exp Appl 115:417–426

    Article  CAS  Google Scholar 

  • Schardl CL, Florea S, Pan J, Nagabhyru P, Bec S, Calie JC (2013) The epichloae: alkaloid diversity and roles in symbiosis with grass. Curr Opin Plant Biol 16:480–488

    Article  PubMed  CAS  Google Scholar 

  • Simpson WR, Schmid J, Singh J, Faville MJ, Johnson RD (2012) A morphological change in the fungal symbiont Neotyphodium lolii induces dwarfing in its host plant Lolium perenne. Fungal Biol 116:234–240

    Article  PubMed  CAS  Google Scholar 

  • Steinfeld H, Gerber P, Wassenaar T, Castel V, Rosales M, Dehaan C (2006) Livestock’s long shadow: environmental issues and options. FAO LEAD, Rome http://www.virtualcentre.org/en/library/keypub/longshad/a0701e/A0701E00.pd. Accessed 3 January 2017

    Google Scholar 

  • Strauss SY (2013) Ecological and evolutionary responses in complex communities: implications for invasions and eco-evolutionary feedbacks. Oikos 123:257–266

    Article  Google Scholar 

  • Sullivan TJ, Rodstrom J, Vandop J, Librizzi J, Graham L, Schardl CL et al (2006) Symbiont-mediated changes in defensive strategy in the invasive grass Lolium arundinaceum: evidence from changes in gene expression and foliar elemental composition. New Phytol 176:673–679

    Article  CAS  Google Scholar 

  • Tanentzap A, Vicari M, Bazely D (2014) Ungulate saliva inhibits a grass-endophyte mutualism. Biol Lett 10:20140460. https://doi.org/10.1098/rsbl.2014.0460

    Article  PubMed  PubMed Central  Google Scholar 

  • White JF Jr, Torres MS (2010) Is plant endophyte-mediated defensive mutualism the result of oxidative stress protection? Plant Physiol 138:440–446

    Article  CAS  Google Scholar 

  • Yue Q, Miller CJ, White JF Jr, Richardson MD (2000) Isolation and characterization of fungal inhibitors from Epichloë festucae. J Agric Food Chem 48:4687–4692

    Article  PubMed  CAS  Google Scholar 

  • Zhang D-X, Nagabhyru P, Schardl CL (2009) Regulation of a chemical defense against herbivory produced by symbiotic fungi in grass plants. Plant Physiol 150:1072–1082

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgments

L. Sutherland provided valuable assistance in care and control of sheep and A. De Bonth completed immunoblot analyses. S. Goldson contributed to discussions about grazing ecosystems. Funding was provided by US National Science Foundation award IOS-1119775 to TLB.

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Authors and Affiliations

  1. Biology Department, Hope College, 35 E. 12th St., Holland, MI, 49423, USA

    Thomas L. Bultman & Kelly Krueger

  2. AgResearch, Canterbury Agric. Sci. Centre, Lincoln, Canterbury, New Zealand

    Mark R. McNeill & Gina De Nicolo

  3. AgResearch – Ruakura Research Centre, Hamilton, New Zealand

    Alison J. Popay & Wade J. Mace

  4. AgResearch, Grasslands Research Centre, Palmerston North, New Zealand

    David E. Hume

  5. Prebbleton, New Zealand

    Lester R. Fletcher

  6. Mathematics Department, Hope College, Holland, MI, USA

    Yew Meng Koh

  7. School of Sciences, Indiana University Kokomo, Kokomo, IN, USA

    Terrence J. Sullivan

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  1. Thomas L. Bultman
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  2. Mark R. McNeill
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  3. Kelly Krueger
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  4. Gina De Nicolo
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Correspondence to Thomas L. Bultman.

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Bultman, T.L., McNeill, M.R., Krueger, K. et al. Complex Interactions among Sheep, Insects, Grass, and Fungi in a Simple New Zealand Grazing System. J Chem Ecol 44, 957–964 (2018). https://doi.org/10.1007/s10886-018-0993-6

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  • DOI: https://doi.org/10.1007/s10886-018-0993-6

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