Fluctuations in the concentration of ergovaline and lolitrem B produced by the wild-type endophyte (Neotyphodium lolii) in perennial ryegrass (Lolium perenne) pasture
K. F. M. Reed A B E , Z. N. Nie A , L. V. Walker C and G. Kearney DA Department of Primary Industries, Private Bag 105, Hamilton, Vic. 3300, Australia.
B Present address: Reed Pasture Science, Hamilton, Vic. 3300, Australia.
C Southern Scientific Services, PO Box 345, Hamilton, Vic. 3300, Australia.
D Paynes Road, Hamilton, Vic. 3300, Australia.
E Corresponding author. Email: rps@eftel.net.au
Animal Production Science 51(12) 1098-1108 https://doi.org/10.1071/AN11143
Submitted: 18 July 2011 Accepted: 8 October 2011 Published: 18 November 2011
Abstract
Mammalian toxins produced by the wild-type endophyte, Neotyphodium lolii, in perennial ryegrass (PRG) pasture cause production losses and animal health and welfare problems in livestock. Managing this risk is limited by the lack of information on fluctuations in the concentration of toxin in Australian pasture. We investigated how the toxin concentrations may be related to recent observations of weather. Swards sown from common seedlots of two cultivars of wild endophyte-infected PRG, grazed short by sheep, were sampled at 2–4 weekly intervals from spring to autumn at two sites in Victoria. The highest concentration of ergovaline and lolitrem B was observed at Hamilton, the site with the longer-growing season. The concentration of ergovaline peaked in early summer, coinciding with seed development, and declined through summer, before increasing with the commencement of autumn growth. The concentration of lolitrem B remained low in summer, then rose in autumn. Variation between the two cultivars in the concentration of toxins was small and rarely significant. The concentration of ergovaline declined as the mean daily maximum temperature over the preceding 1–5 days increased. Similarly, for lolitrem B, the concentration declined over the temperature range 12−20°C, from 1.3 to 0.3 mg/kg. At Hamilton, where solar radiation and soil temperature were recorded, both were superior to maximum temperature for predicting lolitrem B. Serial sampling of PRG from old naturalised pasture on seven farms across south-eastern Australia found two seasonal peaks for both alkaloids in most pastures. The concentration of ergovaline reached or exceeded tolerance levels for livestock in 23 of 43 samples, compared with 5 of 43 for lolitrem B. Ergovaline concentrations initially peaked (at 1.0–1.6 mg/kg) when mature reproductive material was present (coinciding with peduncle elongation and seed development). In pastures with low grazing pressure, i.e. where growth was allowed to continue through summer, ergovaline concentration was relatively low (<0.7 mg/kg) but in a hard-grazed pasture (sward height 3 cm), the ergovaline concentration was greater (up to 1.1 mg/kg). Concentration of lolitrem B also peaked in December, except on pasture where growth continued through summer. High concentrations of lolitrem B associated with neurotoxic signs in sheep (viz. 2.4–3.9 mg/kg) were observed only in mid-summer and autumn, and only if conditions favoured growth or where close grazing by sheep left the crown as the dominant source of herbage.
References
Agee CS, Hill NS (1994) Ergovaline variability in Acremonium-infected tall fescue due to environment and plant genotype. Crop Science 34, 221–226.| Ergovaline variability in Acremonium-infected tall fescue due to environment and plant genotype.Crossref | GoogleScholarGoogle Scholar |
Ball OJ-P, Prestidge RA, Sprosen JM (1995) Interrelationships between Acremonium lolii, peramine and lolitrem B in perennial ryegrass. Applied and Environmental Microbiology 61, 1527–1533.
Ball OJ-P, Barker GM, Prestidge RA, Sprosen JM (1997) Distribution and accumulation of the mycotoxin, lolitrem B, in Neotyphodium lolii-infected perennial ryegrass. Journal of Chemical Ecology 23, 1435–1449.
| Distribution and accumulation of the mycotoxin, lolitrem B, in Neotyphodium lolii-infected perennial ryegrass.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXktVyitLo%3D&md5=17948cbc6ea00067a110ddc5b836d866CAS |
Bluett SJ, Hodgson J, Kemp PD, Barry TN (2001) Performance of lambs and the incidence of staggers and heat stress on two perennial ryegrass cultivars using a leader-follower rotational grazing system. The Journal of Agricultural Science 136, 99–110.
| Performance of lambs and the incidence of staggers and heat stress on two perennial ryegrass cultivars using a leader-follower rotational grazing system.Crossref | GoogleScholarGoogle Scholar |
Bush LP, Wilkinson HH, Schardl CL (1997) Bioprotective alkaloids of grass–fungal endophyte symbioses. Plant Physiology 114, 1–7.
Butler AR (1987) Ryegrass staggers – Tasmania, 1986. Australian Veterinary Association. Advances in Veterinary Science 1987, 111–113.
Clark MF, Adams AN (1977) Characteristics of the microplate method of enzyme-linked immunosorbent assay for the detection of plant viruses. The Journal of General Virology 34, 475–483.
| Characteristics of the microplate method of enzyme-linked immunosorbent assay for the detection of plant viruses.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2s7mslWntQ%3D%3D&md5=28a4c3468853fb3164307606e2ab2753CAS |
Easton HS, Fletcher LR (2007) The importance of endophyte in agricultural systems – changing plant and animal productivity. In ‘Proceedings of the 6th international symposium on fungal endophytes of grasses, Christchurch, 25–28 March 2007’. (Eds AJ Popay, ER Thom) pp. 11–18. (New Zealand Grassland Association: Dunedin, New Zealand)
Easton HS, Latch GCM, Tapper BA, Ball OJ-P (2002) Ryegrass host genetic control of concentrations of endophyte-derived alkaloids. Crop Science 42, 51–57.
| Ryegrass host genetic control of concentrations of endophyte-derived alkaloids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmsVantb8%3D&md5=e63092d8e40941bcfad53c8fd8c6d31eCAS |
Fletcher LR, Lane GA, Baird DB, Davies E (2001) Seasonal variations of alkaloid concentrations in two perennial ryegrass–endophyte associations. In ‘Proceedings 4th international Neotyphodium/grass interactions symposium, Soest, Universitat–Gesamthochschule Paderborn, Abteilung Soest, Germany’. (Eds PH Volker, PD Dapprich) pp. 535–541.
Gallagher RT, Hawkes AD, Steyn PS, Vleggaar R (1984) Tremorgenic neurotoxins from perennial ryegrass causing ryegrass staggers disorder of livestock: structure elucidation of lolitrem B. Journal of the Chemical Society. Chemical Communications 614–616.
| Tremorgenic neurotoxins from perennial ryegrass causing ryegrass staggers disorder of livestock: structure elucidation of lolitrem B.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXmtlSrsrc%3D&md5=91e46a92e885e4caea7255d71506678dCAS |
Genstat Committee (2008) ‘Genstat® for Windows.’ 11th edn. (VSN International: Hertfordshire, UK)
Guy PL (1992) Enzyme-linked immuno absorbent assays (ELISA) to detect perennial ryegrass endophyte (Acremonium lolii) and Metarhizium anisopliae, a potential bio-control agent. In ‘Pests of pastures weed, invertebrate and disease pests of Australian sheep pastures’. (Ed. ES Delfosse) pp. 321–325. (CSIRO: Melbourne)
Hiatt EE, Hill NS, Bouton JH, Stuedemann JA (1999) Tall fescue endophyte detection: commercial immunoblot test kit compared with microscopic analysis. Crop Science 39, 796–799.
| Tall fescue endophyte detection: commercial immunoblot test kit compared with microscopic analysis.Crossref | GoogleScholarGoogle Scholar |
Ju HJ, Hill NS, Abbott T, Ingram KT (2006) Temperature influences on endophyte growth in tall fescue. Crop Science 46, 404–412.
| Temperature influences on endophyte growth in tall fescue.Crossref | GoogleScholarGoogle Scholar |
Lane GA (1999) Chemistry of endophytes: pattern and diversity. In ‘Ryegrass endophyte: an essential New Zealand Symbiosis’. (Eds DR Woodfield, C Matthew) pp. 85–94. New Zealand Grassland Association, Grassland Research and Practice Series No. 7.
Lane GA, Tapper BA, Davies E, Hume DE, Latch GCM, Barker DJ, Easton HS, Rolston MP (1997) Effect of growth conditions on alkaloid concentrations in perennial ryegrass naturally infected with endophyte. In ‘Neotyphodium/grass interactions’. (Eds CW Bacon, NS Hill NS) pp. 179–182. (Plenum Press: New York)
Latch GCM (1994) Influence of Acremonium endophytes on perennial grass improvement. New Zealand Journal of Agricultural Research 37, 311–318.
| Influence of Acremonium endophytes on perennial grass improvement.Crossref | GoogleScholarGoogle Scholar |
Lean IJ (2001) Association between feeding perennial ryegrass (Lolium perenne, cultivar Grasslands Impact) containing high concentrations of ergovaline, and health and productivity in a herd of lactating dairy cows. Australian Veterinary Journal 79, 262–264.
| Association between feeding perennial ryegrass (Lolium perenne, cultivar Grasslands Impact) containing high concentrations of ergovaline, and health and productivity in a herd of lactating dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtlGqtLo%3D&md5=682dfbbb938d06276d1788c61f8af318CAS |
Lean G (2005) Impact on sheep production of perennial ryegrass toxicosis. In ‘Perennial ryegrass toxicosis in Australia’. (Eds KFM Reed, SW Page, I Lean) pp. 37–44. (Meat and Livestock Australia: Sydney)
Moore KJ, Moser LE, Vogel KP, Waller SS, Johnson BE, Pedersen JF (1991) Describing and quantifying growth stages of perennial forage grasses. Agronomy Journal 83, 1073–1077.
| Describing and quantifying growth stages of perennial forage grasses.Crossref | GoogleScholarGoogle Scholar |
Moore AD, Donnelly JR, Freer M (1997) GRAZPLAN: decision support systems for Australian grazing enterprises. III. Pasture growth and soil moisture submodels and the GrassGro DSS. Agricultural Systems 55, 535–582.
| GRAZPLAN: decision support systems for Australian grazing enterprises. III. Pasture growth and soil moisture submodels and the GrassGro DSS.Crossref | GoogleScholarGoogle Scholar |
Musgrave DR, Grose TA, Latch GCM, Christensen MJ (1986) Purification and characterisation of the antigens of endophytic fungi isolated from Lolium perenne and Festuca arundinacea in New Zealand. New Zealand Journal of Agricultural Research 29, 121–129.
Napthine DV, McLeod IK (1987) Perennial ryegrass staggers–1986 Victorian outbreak. Australian Veterinary Association. Advances in Veterinary Science 1987, 107–109.
Reed KFM, Smith KF (2001) Adaptation of perennial grasses to a long dry summer. In ‘Breeding for stress tolerance in fodder crops and amenity grasses’. Proceedings 23rd EUCARPIA fodder crops and amenity grasses meeting, Azores, Portugal, 2–4 October 2000. (Eds P Monjardino, A daCâmara, V Carnide) pp. 26–29. (Department of Agricultural Science, University of Azores: Azores, Portugal)
Reed KFM, Leonforte A, Cunningham PJ, Walsh JR, Allen DI, Johnstone GR, Kearney G (2000) Incidence of ryegrass endophyte (Neotyphodium lolii) and diversity of associated alkaloid concentrations among naturalised populations of perennial ryegrass. Australian Journal of Agricultural Research 51, 569–578.
| Incidence of ryegrass endophyte (Neotyphodium lolii) and diversity of associated alkaloid concentrations among naturalised populations of perennial ryegrass.Crossref | GoogleScholarGoogle Scholar |
Reed KFM, McFarlane NM, Walsh JR (2001) Seasonal alkaloid concentration in perennial ryegrass dairy pasture. In ‘Proceedings 10th Australian agronomy conference, Hobart, 29–31 January 2001’. Available at www.regional.org.au/au/asa/2001/ [Verified 18 October 2011]
Reed KFM, Walsh JR, Cross PA, McFarlane NM, Sprague M (2004) Ryegrass endophyte (Neotyphodium lolii) alkaloids and mineral concentrations in perennial ryegrass (Lolium perenne) from southwest Victorian pasture. Australian Journal of Experimental Agriculture 44, 1185–1194.
| Ryegrass endophyte (Neotyphodium lolii) alkaloids and mineral concentrations in perennial ryegrass (Lolium perenne) from southwest Victorian pasture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmsVOnsw%3D%3D&md5=59fa5331fb923b633267ba79a7ea666aCAS |
Reed KFM, Scrivener CJ, Rainsford KA, Walker LV (2005) Neotyphodium research and application in Australia. In ‘Neotyphodium in cool-season grasses’. (Eds CA Roberts, CP West, DE Spiers) pp. 43–54. (Blackwell Publishing Professional: Ames, IA)
Reed KFM, Nie ZN, Miller S, Hackney B, Boschma SP, Mitchell ML, Albertsen TO, Moore GA, Clark SG, Craig AD, Kearney G, Li GD, Dear BS (2008) Field evaluation of perennial grasses and herbs in southern Australia. 1. Establishment and herbage production. Australian Journal of Experimental Agriculture 48, 409–423.
| Field evaluation of perennial grasses and herbs in southern Australia. 1. Establishment and herbage production.Crossref | GoogleScholarGoogle Scholar |
Reed KFM, Nie Z, Walker LV, Mace W, Clark SG (2011) Weather and pasture characteristic of outbreaks of severe perennial ryegrass toxicosis in southern Australia. Animal Production Science 51, 738–752.
| Weather and pasture characteristic of outbreaks of severe perennial ryegrass toxicosis in southern Australia.Crossref | GoogleScholarGoogle Scholar |
Sackett D, Francis J (2006) The economic assessment of the impact of wild endophyte-infected perennial ryegrass (Lolium perenne) on the productivity of sheep and cattle and the profitability of Australian livestock enterprises. Report AHW.089, Meat and Livestock Australia, Sydney.
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. Entomologia Experimentalis et Applicata 115, 417–426.
| Influence of temperature on alkaloid levels and fall armyworm performance in endophytic tall fescue and perennial ryegrass.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlvFChtL4%3D&md5=65dd27d4b7226349f2f153e3980aa272CAS |
Shelby R, Flieger M (1997) Improved method of analysis for ergovaline in tall fescue by high performance liquid chromatography. Journal of Agricultural and Food Chemistry 45, 1797–1800.
| Improved method of analysis for ergovaline in tall fescue by high performance liquid chromatography.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjtlWrtr8%3D&md5=f03944b53aa77040670c6e42bfbb3b22CAS |
Shelby RA, Olsovska J, Havlicek V, Flieger M (1997) Analysis of ergot alkaloids in endophyte-infected tall fescue by liquid chromatography/electrospray ionization mass spectroscopy. Journal of Agricultural and Food Chemistry 45, 4674–4679.
| Analysis of ergot alkaloids in endophyte-infected tall fescue by liquid chromatography/electrospray ionization mass spectroscopy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXnsVSks7w%3D&md5=ed0e297514ad75b8ec16c4a6ca962147CAS |
Spiering MJ, Davies E, Tapper BA, Schmid J, Lane GA (2002) Simplified extraction of ergovaline and peramine for analysis of tissue distribution in endophyte-infected grass tillers. Journal of Agricultural and Food Chemistry 50, 5856–5862.
| Simplified extraction of ergovaline and peramine for analysis of tissue distribution in endophyte-infected grass tillers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmvFKrsLg%3D&md5=7a8ba25842592ab83991c3d40d1f19edCAS |
Tor-Agbidye J, Blythe LL, Craig AM (2001) Correlation of endophyte toxins (ergovaline and lolium B) with clinical disease: fescue foot and perennial ryegrass staggers. Veterinary and Human Toxicology 43, 140–146.
van Zijll de Jong E, Bannan NR, Stewart AV, Reed KFM, Dobrowolski MP, Smith KF, Spangenberg GC, Forster JW (2005) Genetic variation in the perennial ryegrass fungal endophyte Neotyphodium lolii. In ‘Molecular breeding for the genetic improvement of forage crops and turf’. Proceedings of the 4th international symposium on the molecular breeding of forage and turf, a satellite workshop of the 20th international grassland congress, Aberystwyth, Wales, July 2005. (Ed. MO Humphreys) p. 211.