Register      Login
Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
REVIEW (Open Access)

Ergovaline, an endophytic alkaloid. 2. Intake and impact on animal production, with reference to New Zealand

A. M. Nicol A and J. L. Klotz B C
+ Author Affiliations
- Author Affiliations

A AMN Consulting, 1248 Old West Coast Road, RD 1, Christchurch 7671, New Zealand.

B USDA-ARS, Forage-Animal Production Research Unit, Lexington, KY 40546, USA.

C Corresponding author. Email: james.klotz@ars.usda.gov

Animal Production Science 56(11) 1775-1786 https://doi.org/10.1071/AN14963
Submitted: 26 November 2014  Accepted: 28 June 2016   Published: 19 August 2016

Journal Compilation © CSIRO Publishing 2016 Open Access CC BY-NC-ND

Abstract

On the basis of published reports, the daily intake of the alkaloid ergovaline from the consumption of endophyte-containing ryegrass in New Zealand ranges from 0.008 to 0.287 mg ergovaline/kg LW0.75.day. Most of the reports are based on the use of standard endophyte-containing ryegrass and, thus, it is difficult to disassociate the impact of ergovaline consumption from that of lolitrem B. However, physiological effects of ergovaline consumption, such as reduced circulating prolactin concentration, vasoconstriction and elevated core temperature, have been detected at fairly low ergovaline intake, whereas decreased feed intake, liveweight gain and milk production have not generally been observed in animals at an intake below 0.07 mg ergovaline/kg LW0.75.day. Intakes above this value represent only 17% of published values. There are insufficient data to suggest a threshold ergovaline intake associated with heat stress with animal-welfare implications. The relationship between published ergovaline intake and the corresponding ergovaline concentration in pasture is poor (R2 = 0.48), but on average an intake of 0.07 ergovaline/kg LW0.75.day is associated with an ergovaline concentration in ryegrass of 0.70 mg/kg DM. About 16–18% of published ergovaline concentrations in ryegrass pasture exceed this value. The ergovaline concentration in ryegrass is greater in the basal parts of the plant than in the leaf and during the late summer–autumn than in spring. Animals grazing in the lower sward horizons (horizontal grazing plane) are more at risk of high ergovaline intake, although the reduction in grazing intake induced by grazing at low pasture height aids in limiting ergovaline intake. As pasture growth rates decline in late summer, supplementary feed may be used to maintain stocking rate and, if such feeds have zero ergovaline concentration, they serve to dilute the mean dietary ergovaline intake. Ergovaline-containing ryegrass pastures are widely used in New Zealand. It appears that farmers consider the risks of depressed animal production on these pastures to be less than the benefits ergovaline bestows through its deterrent effect of specific insect attack and thus greater survival and pasture persistence.

Additional keywords: ergot alkaloids, livestock, perennial ryegrass, threshold.


References

Aiken GE, Klotz JL, Johnson JM, Strickland JR, Schrick FN (2013) Postgraze assessment of toxicosis symptoms for steers grazed on toxic endophyte-infected tall fescue pasture. Journal of Animal Science 91, 5878–5884.
Postgraze assessment of toxicosis symptoms for steers grazed on toxic endophyte-infected tall fescue pasture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvFOrur3I&md5=4dfda04f5f4b8adaecd283be4c053b63CAS | 24126272PubMed |

Aiken GE, Sutherland BL, Fletcher LR (2011) Haemodynamics of lambs grazing perennial ryegrass (Lolium perenne L.) either infected with AR6 novel, wild-type endophyte, or endophyte-free. New Zealand Veterinary Journal 59, 179–184.

Aldrich CG, Paterson JA, Tate JL, Kerley MS (1993) The effects of endophyte-infected tall fescue consumption on diet utilization and thermal regulation in cattle. Journal of Animal Science 71, 164–170.

Bluett SJ, Hodgson J, Kemp PD, Barry TN (2001) Performance of lambs and the incidence of staggers and heat stress on two perennial ryegrass (Lolium perenne) cultivars using a leader-follower rotational grazing management system. Journal of Agricultural Science, Cambridge. 136, 99–110.
Performance of lambs and the incidence of staggers and heat stress on two perennial ryegrass (Lolium perenne) cultivars using a leader-follower rotational grazing management system.Crossref | GoogleScholarGoogle Scholar |

Bluett SJ, Kolver ES, Auldist MJ, Thom ER, Davis SR, Farr VC, Tapper BA (2003a) Perennial ryegrass endophyte effects on plasma prolactin concentration in dairy cows. New Zealand Journal of Agricultural Research 46, 9–14.
Perennial ryegrass endophyte effects on plasma prolactin concentration in dairy cows.Crossref | GoogleScholarGoogle Scholar |

Bluett SJ, Thom ER, Clark DA, MacDonald KA, Minnee EMK (2003b) Milk solids production from cows grazing perennial ryegrass containing AR1 or wild type endophyte. Proceedings of the New Zealand Grassland Association 65, 83–90.

Bluett SJ, Thom ER, Clark DA, Macdonald KA, Minnee EMK (2005a) Effects of perennial ryegrass infected with either AR1 or wild type endophyte on dairy production in the Waikato. New Zealand Journal of Agricultural Research 48, 197–212.
Effects of perennial ryegrass infected with either AR1 or wild type endophyte on dairy production in the Waikato.Crossref | GoogleScholarGoogle Scholar |

Bluett SJ, Thom ER, Clark DA, Waugh CD (2005b) Effects of a novel ryegrass endophyte on pasture production, dairy cow milk production and calf liveweight gain. Australian Journal of Experimental Agriculture 45, 11–19.
Effects of a novel ryegrass endophyte on pasture production, dairy cow milk production and calf liveweight gain.Crossref | GoogleScholarGoogle Scholar |

Bohnert D, Merrill M (2006) Management strategies for use of high-alkaloid grass seed straw. In ‘Proceedings of the 41st annual Pacific Northwest nutrition conference’, Vancouver, British Columbia, Canada. (Ed. M von Keyserlingk) pp. 113–125. (CR Press Inc.: Portland, OR)

Breen GP, Barrell GK (2002) Effects of pregnancy on the fever response of sheep to a Gram-negative pyrogen. Proceedings of the New Zealand Society of Animal Production 62, 337–339.

Bryant JR, López-Villalobos N, Price JE, Holmes CW, Johnson DL (2007) Quantifying the effect of thermal environment on production traits in three breeds of dairy cattle in New Zealand. New Zealand Journal of Agricultural Research 50, 327–338.
Quantifying the effect of thermal environment on production traits in three breeds of dairy cattle in New Zealand.Crossref | GoogleScholarGoogle Scholar |

Clark DA, Woodward SL (2007) ‘Supplementation of dairy cows, beef cattle, and sheep grazing pasture.’ In ‘Pasture and supplements for grazing animals’. Occasional publication no. 14. (Eds PV Rattray, IM Brookes, AM Nicol) pp. 117–131. (New Zealand Society of Animal Production)

Clark DA, Thom ER, Waugh CD (1996) Milk production from pastures and pasture silage with different levels of endophyte infection. Proceedings of the New Zealand Society of Animal Production 56, 292–296.

Clark DA, Thom ER, Waugh CD, Burggraff VT (1999) Milk production from perennial ryegrass pastures containing different levels of endophyte. Proceedings of the New Zealand Society of Animal Production 59, 258–262.

Cosgrove GP, Edwards GR (2007) Control of grazing intake. In ‘Pasture and supplements for grazing animals’. No. 14. (Eds PV Rattray, IM Brookes, AM Nicol) pp. 61–80. (New Zealand Society of Animal Production)

Cosgrove GP, Anderson CB, Berquist TRN (1996) Fungal endophyte effects on intake, health, and liveweight gain of grazing cattle. Proceedings of the New Zealand Society of Animal Production 57, 43–48.

Cosgrove GP, Anderson CB, Phillot M, Nyfeler D, Hume DE, Parsons AJ, Lane GA (2002) The effect of endophyte alkaloids on diet selection by sheep. Proceedings of the New Zealand Society of Animal Production 62, 167–170.

di Menna ME, Finch SC, Popay AJ, Smith BL (2012) A review of the Neotyphodium lolii/Lolium perenne symbiosis and its associated effects on animal and plant health, with particular emphasis on ryegrass staggers. New Zealand Veterinary Journal 60, 315–328.
A review of the Neotyphodium lolii/Lolium perenne symbiosis and its associated effects on animal and plant health, with particular emphasis on ryegrass staggers.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38bgsVWjuw%3D%3D&md5=b73d9bf777e579085bd51e86604dc29fCAS | 22913513PubMed |

Easton HS, Lane GA, Tapper BA, Keogh RG, Cooper BM, Blackwell M, Anderson M, Fletcher LR (1996) Ryegrass endophyte-related heat stress in cattle. Proceedings of the New Zealand Grassland Association 57, 5

Easton HS, Couchman JN, Keogh RG, Tapper BA (2000) Ryegrass endophyte and cattle in northern New Zealand. In ‘Fourth international Neotyphodium/grass interaction symposium’. (Eds HV Paul, PD Dapprich) pp. 357–363. (Soest, Germany)

Easton HS, Latch GC, Tapper BA, Ball OJ (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=202d7e91cfc7c81c1bd937e68c290fb3CAS | 11756253PubMed |

Edwards GR, Lucas RJ, Johnson MR (1993) Grazing preference for pasture species by sheep is affected by endophyte and nitrogen fertility. Proceedings of the New Zealand Grassland Association 55, 137–141.

Emile JC, Bony S, Ghesquiere M (2000) Influence of consumption of endophyte-infested tall fescue hay on performance of heifers and lambs. Journal of Animal Science 78, 358–364.

Fletcher LR (1999) ‘Non-toxic’ endophytes in ryegrass and their effect on livestock health and production. In ‘Ryegrass endophyte: an essential New Zealand symbiosis’. Grassland research and practice series no. 7. (Eds DR Woodfield, C Matthew) pp. 133–139.

Fletcher LR (2013) ‘Safety of Trojan NEA2 for grazing sheep.’ AgResearch 7. (AgResearch: New Zealand)

Fletcher LR, Easton HS (2007) ‘The importance of endophyte in agricultural systems: changing plant and animal productivity. New Zealand Grassland Association: endophyte symposium.’ pp. 11–18.

Fletcher LR, Sutherland BL (2009) Sheep responses to grazing ryegrass with AR37 endophyte. Proceedings of the New Zealand Grassland Association 71, 127–132.

Fletcher LR, Markham LJ, White SR (1994) Endophytes and heat tolerance in lambs grazing perennial ryegrass. Proceedings of the New Zealand Grassland Association 56, 265–270.

Fletcher LR, Lane GA, Baird DB, Davies E (2000) Seasonal variation of alkaloid concentrations in two perennial ryegrass-endophyte associations. In ‘Fourth international Neotyphodium/grass interactions symposium’. (Eds HV Paul, PD Dapprich) pp. 535–541. (Soest, Germany)

Foote AP, Kristensen NB, Klotz JL, Kim DH, Koontz AF, McLeod KR, Bush LP, Schrick FN, Harmon DL (2013) Ergot alkaloids from endophyte-infected tall fescue decrease reticuloruminal epithelial blood flow and volatile fatty acid absorption from the washed reticulorumen. Journal of Animal Science 91, 5366–5378.
Ergot alkaloids from endophyte-infected tall fescue decrease reticuloruminal epithelial blood flow and volatile fatty acid absorption from the washed reticulorumen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslKkt7vK&md5=f14644ab61948b34a76ee31f5653bba6CAS |

Ganong WF (1981) ‘Review of medical physiology.’ (Lange Medical Publications: Los Altos, CA)

Gustin P, Dhem AR, Lekeux P, Lomba F, Landser FJ, Van de Woestijne KP (1989) Regulation of bronchomotor tone in conscious calves. Journal of Veterinary Pharmacology and Therapeutics 12, 58–64.
Regulation of bronchomotor tone in conscious calves.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1M7pvFOhug%3D%3D&md5=6b02b386a27461f71c828749c7dc250dCAS | 2704063PubMed |

Hovermale JT, Craig AM (2001) Correlation of ergovaline and lolitrem B levels in endophyte-infected perennial ryegrass (Lolium perenne). Journal of Veterinary Diagnostic Investigation 13, 323–327.
Correlation of ergovaline and lolitrem B levels in endophyte-infected perennial ryegrass (Lolium perenne).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38%2Fis1Gjsg%3D%3D&md5=ec2c2f61059f74004668a5f8e05baaa4CAS | 11478604PubMed |

Igono MO, Bjotvedt G, Sanford-Crane HT (1992) Environmental profile and critical temperature effects on milk production of Holstein cows in desert climate. International Journal of Biometeorology 36, 77–87.
Environmental profile and critical temperature effects on milk production of Holstein cows in desert climate.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK38zktVWluw%3D%3D&md5=d1c2dc8a1386cc7f0cc0274a709d955aCAS | 1634283PubMed |

Keogh RG, Blackwell MB, Shepherd P (1999) Performance of dairy cows grazing pasture with or without ergovaline and lolitrem B in Northland. Proceedings of the New Zealand Society of Animal Production 59, 254–257.

Klotz JL, Nicol AM (2016) Ergovaline, an endophytic alkaloid. 1. Animal physiology and metabolism. Animal Production Science 56, 1761–1774.
Ergovaline, an endophytic alkaloid. 1. Animal physiology and metabolism.Crossref | GoogleScholarGoogle Scholar |

Koontz AF, Kim DH, Foote AP, Bush LP, Klotz JL, McLeod KR, Harmon DL (2013) Alteration of fasting heat production during fescue toxicosis in Holstein steers. Journal of Animal Science 91, 3881–3888.
Alteration of fasting heat production during fescue toxicosis in Holstein steers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlOjsbfK&md5=63571c2562033abd954cf1c6b96abd08CAS | 23908162PubMed |

Laird FC, Barrell GK (2010) Lack of effect of hot summer conditions in Canterbury on milk production of dairy cows. Proceedings of the New Zealand Society of Animal Production 70, 19–22.

Lane GA, Ball OJP, Davies E, Davidson C (1997) Ergovaline distribution in perennial ryegrass naturally infected with endophyte. In ‘Neotyphodium/grass interactions’. (Eds CW Bacon, NS Hill) pp. 65–67. (Plenum Press: New York)

Larson BT, Samford MD, Camden JM, Piper EL, Kerley MS, Paterson JA, Turner JT (1995) Ergovaline binding and activation of D2 dopamine receptors in GH4ZR7 cells. Journal of Animal Science 73, 1396–1400.

Layton DL, Fletcher LR, Litherland AJ, Scannell MG, Sprosen J, Hoogendoorn CJ, Lambert MG (2004) Efects of ergot alkaloids on liveweight gain and urine lysergol level in ewe hoggets and cattle. Proceedings of the New Zealand Society of Animal Production 64, 192–196.

Linden AS, Desmecht DJ, Amory H, Rollin FA, Michaux CL, Lekeux P (1993) Pulmonary response to intravenous administration of 5-hydroxytryptamine after type-2 receptor blockade in healthy calves. American Journal of Veterinary Research 54, 168–173.

Morris CA, Towers NR, Hohenboken WD, Maqbool N, Smith BL, Phua SH (2004) Inheritance of resistance to facial eczema: a review of research findings from sheep and cattle in New Zealand. New Zealand Veterinary Journal 52, 205–215.
Inheritance of resistance to facial eczema: a review of research findings from sheep and cattle in New Zealand.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXptFKjsbc%3D&md5=e81cf5d424e53015915be16451f2cd88CAS | 15768115PubMed |

Morris CA, Amyes NC, Orchard RL (2007) Responses to selection in ryegrass staggers lines of sheep. Proceedings of the New Zealand Society of Animal Production 67, 204–208.

Nicol AM, Brookes IM (2007) The metabolisable energy requirements of grazing livestock. In ‘Pasture and supplements for grazing animals’. Occasional publication no. 14. (Eds PV Rattray, IM Brookes, AM Nicol) pp. 151–172. (New Zealand Society of Animal Production)

NIWA (2014) New Zealand national climate database. Available at climo.niwa.co.nz [Verified 20 November 2014]

Nolan A, Livingston A, Waterman A (1986) The effects of alpha 2 adrenoceptor agonists on airway pressure in anaesthetized sheep. Journal of Veterinary Pharmacology and Therapeutics 9, 157–163.
The effects of alpha 2 adrenoceptor agonists on airway pressure in anaesthetized sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XktlGmt7w%3D&md5=988c927be13eb60a4da55cd4a1bd22acCAS | 2873256PubMed |

NFVT (2013) ‘National forage variety trials: trial protocol 2013.’ (New Zealand Plant Breeding Research Association: Christchurch, New Zealand)

Oliver JW (1997) Physiological manifestations of endophyte toxicosis in ruminant and laboratory species. In ‘Neotyphodium/grass interactions’. (Eds CW Bacon, NS Hill) pp. 311–346. (Springer: New York)

Popay AJ, Hume DE (2011) Endophytes improve ryegrass persistence by controlling insects. Pasture persistence.

Reed KFM, Nie ZN, Walker LV, Kearney G (2011) Fluctuations in the concentration of ergovaline and lolitrem B produced by the wild-type endophyte (Neotyphodium lolii) in perennial ryegrass (Lolium perenne) pasture. Animal Production Science 51, 1098–1108.
Fluctuations in the concentration of ergovaline and lolitrem B produced by the wild-type endophyte (Neotyphodium lolii) in perennial ryegrass (Lolium perenne) pasture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFertb3L&md5=d0d8d577db1c2e375cb3c90b4cbf27c1CAS |

Refinetti R, Piccione G (2005) Intra- and inter-individual variability in the circadian rhythm of body temperature of rats, squirrels, dogs and horses. Journal of Thermal Biology 30, 139–146.
Intra- and inter-individual variability in the circadian rhythm of body temperature of rats, squirrels, dogs and horses.Crossref | GoogleScholarGoogle Scholar |

Spiering MJ, Lane GA, Christensen MJ, Schmid J (2005) Distribution of the fungal endophyte Neotyphodium lolii is not a major determinant of the distribution of fungal alkaloids in Lolium perenne plants. Phytochemistry 66, 195–202.
Distribution of the fungal endophyte Neotyphodium lolii is not a major determinant of the distribution of fungal alkaloids in Lolium perenne plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXksVektw%3D%3D&md5=437f3b0d15fb87bb88ae44dcc7ea1e49CAS | 15652576PubMed |

Spiers DE, Zhang Q, Eichen PA, Rottinghaus GE, Garner GB, Ellersieck MR (1995) Temperature-dependent responses of rats to ergovaline derived from endophyte-infected tall fescue. Journal of Animal Science 73, 1954–1961.

Stamm MM, DelCurto T, Horney MR, Brandyberry SD, Barton RK (1994) Influence of alkaloid concentration of tall fescue straw on the nutrition, physiology, and subsequent performance of beef steers. Journal of Animal Science 72, 1068–1075.

Stewart, A, Kerr, G, Lissaman, W, Rowarth, J (2014) Chapter 8. Endophyte in ryegrass and fescue. In ‘Pasture and forage plants for New Zealand’. Grassland research and practice series no. 8. pp. 66–77. (New Zealand Grassland Association)

Thom ER, Clark DA, Waugh CD (1999) Endophyte and dairy production in New Zealand: experience at the Dairy Research Corporation. Grassland research and practice series. Vol. 7. (New Zealand Grasslands Association)

Thom ER, Popay AJ, Hume DE, Fletcher LR (2012) Evaluating the performance of endophytes in farm systems to improve farmer outcomes: a review. Crop and Pasture Science 63, 927–943.
Evaluating the performance of endophytes in farm systems to improve farmer outcomes: a review.Crossref | GoogleScholarGoogle Scholar |

Thom ER, Waugh CD, Minnee EM, Waghorn GC (2013) Effects of novel and wild-type endophytes in perennial ryegrass on cow health and production. New Zealand Veterinary Journal 61, 87–97.
Effects of novel and wild-type endophytes in perennial ryegrass on cow health and production.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38bgsVWnsA%3D%3D&md5=9f5e28c4175c61b4ae346638d81a4fcfCAS | 22913546PubMed |

Tor-Agbidye J, Blythe LL, Craig AM (2001) Correlation of endophyte toxins (ergovaline and lolitrem B) with clinical disease: fescue foot and perennial ryegrass staggers. Veterinary and Human Toxicology 43, 140–146.