A root aphid Aploneura lentisci is affected by Epichloë endophyte strain and impacts perennial ryegrass growth in the field
Alison J. Popay
A C , David. E. Hume B , Wade J. Mace B , Marty J. Faville B , Sarah C. Finch A and Vanessa Cave A
+ Author Affiliations
- Author Affiliations
A AgResearch, Ruakura Research Centre, Private Bag 3123, Hamilton 3240, New Zealand.
B AgResearch, Grasslands Research Centre, Private Bag 11008, Palmerston North 4442, New Zealand.
C Corresponding author. Email: alison.popay@agresearch.co.nz
Crop and Pasture Science 72(2) 155-164 https://doi.org/10.1071/CP20299
Submitted: 10 August 2020 Accepted: 8 January 2021 Published: 2 March 2021
Abstract
The aphid Aploneura lentisci is widespread in Australia and New Zealand, living all year round on roots of its secondary grass hosts. The fungal endophyte (Epichloë festucae var. lolii), strain AR37 in Lolium perenne is known to greatly reduce populations and was a likely reason for the superior growth and persistence of this association previously observed in the field. Aphid populations were quantified in a field trial near Ballarat, comparing yields of perennial ryegrass infected with eight different endophyte strains and an endophyte-free (Nil) control in a common ryegrass background (Grasslands Samson (G. Samson)). AR37 and another endophyte strain, AR5, had significantly fewer aphids than all other endophytes. These differences were significantly related to yield increases taken before and after sampling that persisted until the end of the trial. In a pot trial comparing commercially available ryegrass-endophyte combinations with equivalent Nil controls, aphid numbers were lower on G. Samson AR37 and Banquet II with AR5 (Endo®5) than on all other cultivar-endophyte combinations. Compared with Nil controls, the common toxic strain in G. Samson, and two strains in Trojan also reduced aphid numbers. The AR5 endophyte produces the alkaloid ergovaline but high concentrations of this in roots of potted plants could not account for differences in root aphid numbers. Root concentrations of epoxyjanthitrems, the only known alkaloids produced by AR37, were low and unlikely to be the cause of resistance to A. lentisci.
Keywords: Aploneura lentisci, aphid, ryegrass yield, cultivar, fungal endophyte, alkaloids, pest status.
References
Aslam TJ, Johnson SN, Karley AJ (2013) Plant‐mediated effects of drought on aphid population structure and parasitoid attack. Journal of Applied Entomology 137, 136–145.| Plant‐mediated effects of drought on aphid population structure and parasitoid attack.Crossref | GoogleScholarGoogle Scholar |
Baldauf MW, Mace WJ, Richmond DS (2011) Endophyte-mediated resistance to black cutworm as a function of plant cultivar and endophyte strain in tall fescue. Environmental Entomology 40, 639–647.
| Endophyte-mediated resistance to black cutworm as a function of plant cultivar and endophyte strain in tall fescue.Crossref | GoogleScholarGoogle Scholar | 22251642PubMed |
Ball OJP, Barker GM, Prestidge RA, Lauren DR (1997) Distribution and accumulation of the alkaloid peramine in Neotyphodium lolii-infected perennial ryegrass. Journal of Chemical Ecology 23, 1419–1434.
| Distribution and accumulation of the alkaloid peramine in Neotyphodium lolii-infected perennial ryegrass.Crossref | GoogleScholarGoogle Scholar |
Collinson NP, Mann RC, Giri K, Malipatil M, Kaur J, Spangenberg G, Valenzuela I (2020) Novel bioassay to assess antibiotic effects of fungal endophytes on aphids. PLoS ONE 15, e0228813
| Novel bioassay to assess antibiotic effects of fungal endophytes on aphids.Crossref | GoogleScholarGoogle Scholar | 32040957PubMed |
Cosgrove GP, Popay AJ, Taylor PS, Wilson DJ, Aalders LT, Bell NL (2018) Implications of grass–clover interactions in dairy pastures for forage indexing systems. 3. Manawatu. New Zealand Journal of Agricultural Research 61, 174–203.
| Implications of grass–clover interactions in dairy pastures for forage indexing systems. 3. Manawatu.Crossref | GoogleScholarGoogle Scholar |
Cottier W (1953) Aphids of New Zealand. New Zealand Department of Scientific and Industrial Research Bulletin 106.
Easton HS, Latch GCM, Tapper BA, Ball OJP (2002) Ryegrass host genetic control of concentrations of endophyte-derived alkaloids. Crop Science 42, 51–57.
Finch SC, Fletcher LR, Babu JV (2012) The evaluation of endophyte toxin residues in sheep fat. New Zealand Veterinary Journal 60, 56–60.
| The evaluation of endophyte toxin residues in sheep fat.Crossref | GoogleScholarGoogle Scholar | 22175431PubMed |
Fletcher LR, Harvey IC (1981) An association of a Lolium endophyte with ryegrass staggers. New Zealand Veterinary Journal 29, 185–186.
| An association of a Lolium endophyte with ryegrass staggers.Crossref | GoogleScholarGoogle Scholar | 6950332PubMed |
Fletcher LR, Sutherland BL (2009) Sheep responses to grazing ryegrass with AR37 endophyte. Proceedings of the New Zealand Grassland Association 71, 127–132.
| Sheep responses to grazing ryegrass with AR37 endophyte.Crossref | GoogleScholarGoogle Scholar |
Fletcher LR, Finch SC, Sutherland BL, deNicolo G, Mace WJ, van Koten C, Hume DE (2017) The occurrence of ryegrass staggers and heat stress in sheep grazing ryegrass-endophyte associations with diverse alkaloid profiles. New Zealand Veterinary Journal 65, 232–241.
| The occurrence of ryegrass staggers and heat stress in sheep grazing ryegrass-endophyte associations with diverse alkaloid profiles.Crossref | GoogleScholarGoogle Scholar | 28506113PubMed |
Huberty AF, Denno RF (2004) Plant water stress and its consequences for herbivorous insects: a new synthesis. Ecology 85, 1383–1398.
| Plant water stress and its consequences for herbivorous insects: a new synthesis.Crossref | GoogleScholarGoogle Scholar |
Hume DE, Sewell JC (2014) Agronomic advantages conferred by endophyte infection of perennial ryegrass (Lolium perenne L.) and tall fescue (Festuca arundinacea Schreb.) in Australia. Crop & Pasture Science 65, 747–757.
| Agronomic advantages conferred by endophyte infection of perennial ryegrass (Lolium perenne L.) and tall fescue (Festuca arundinacea Schreb.) in Australia.Crossref | GoogleScholarGoogle Scholar |
Hume DE, Ryan DL, Cooper BM, Popay AJ (2007) Agronomic performance of AR37-infected ryegrass in northern New Zealand. Proceedings of the New Zealand Grassland Association 69, 201–205.
| Agronomic performance of AR37-infected ryegrass in northern New Zealand.Crossref | GoogleScholarGoogle Scholar |
International VSN (2015) ‘Genstat for Windows.’ 18th edn. (VSN International: Hemel Hempstead, UK)
Lane GA, Christensen MJ, Miles CO (2000) Coevolution of fungal endophytes with grasses: the significance of secondary metabolites. In ‘Microbial endophytes’. (Eds CW Bacon, F White James, Jr.) pp. 341–388. (Marcel Dekker, Inc.: New York, USA)
Lowe AD (1968) Alate aphids trapped over 8 years at two sites in Canterbury, New Zealand. New Zealand Journal of Agricultural Research 11, 829–848.
| Alate aphids trapped over 8 years at two sites in Canterbury, New Zealand.Crossref | GoogleScholarGoogle Scholar |
Moate PJ, Williams SRO, Grainger C, Hannah MC, Mapleson D, Auldist MJ, Greenwood JS, Popay AJ, Hume DE, Mace WJ, Wales WJ (2012) Effects of wild-type, AR1 and AR37 endophyte-infected perennial ryegrass on dairy production in Victoria, Australia. Animal Production Science 52, 1117–1130.
| Effects of wild-type, AR1 and AR37 endophyte-infected perennial ryegrass on dairy production in Victoria, Australia.Crossref | GoogleScholarGoogle Scholar |
Moran NA, Whitham TG (1988) Population fluctuations in complex lifecycles: an example from Pemphigus aphids. Ecology 69, 1214–1218.
| Population fluctuations in complex lifecycles: an example from Pemphigus aphids.Crossref | GoogleScholarGoogle Scholar |
Mortimer PH, di Menna ME (1983) Lolium endophyte aetiology and the discovery of weevil resistance of ryegrass pastures infected with Lolium endophyte. Proceedings of the New Zealand Grassland Association 44, 240–243.
| Lolium endophyte aetiology and the discovery of weevil resistance of ryegrass pastures infected with Lolium endophyte.Crossref | GoogleScholarGoogle Scholar |
Muller JL (2019) Life-cycle, ecology and damage potential of root aphids (Aploneura lentisci Pass.) in New Zealand. PhD thesis, Massey University, Palmerston North, New Zealand.
Nachappa P, Culkin CT, Saya PM, Han J, Nalam VJ (2016) Water stress modulates soybean aphid performance, feeding behavior, and virus transmission in soybean. Frontiers in Plant Science 7, 552
| Water stress modulates soybean aphid performance, feeding behavior, and virus transmission in soybean.Crossref | GoogleScholarGoogle Scholar | 27200027PubMed |
O’Loughlin GT (1963) Aphid trapping in Victoria I. The seasonal occurrence of aphids in three localities and a comparison of two trapping methods. Australian Journal of Agricultural Research 14, 61–69.
| Aphid trapping in Victoria I. The seasonal occurrence of aphids in three localities and a comparison of two trapping methods.Crossref | GoogleScholarGoogle Scholar |
Patterson CG, Potter DA, Fannin FF (1991) Feeding deterrency of alkaloids from endophyte-infected grasses to Japanese beetle larvae. Entomologia Experimentalis et Applicata 61, 285–289.
| Feeding deterrency of alkaloids from endophyte-infected grasses to Japanese beetle larvae.Crossref | GoogleScholarGoogle Scholar |
Popay AJ, Cox NR (2016) Aploneura lentisci (Homoptera: Aphididae) and its interactions with fungal endophytes in perennial ryegrass (Lolium perenne). Frontiers in Plant Science 7, 1395
| Aploneura lentisci (Homoptera: Aphididae) and its interactions with fungal endophytes in perennial ryegrass (Lolium perenne).Crossref | GoogleScholarGoogle Scholar | 27695470PubMed |
Popay AJ, Gerard PJ (2007) Cultivar and endophyte effects on a root aphid, Aploneura lentisci, in perennial ryegrass. New Zealand Plant Protection 60, 223–227.
| Cultivar and endophyte effects on a root aphid, Aploneura lentisci, in perennial ryegrass.Crossref | GoogleScholarGoogle Scholar |
Popay AJ, Thom ER (2009) Endophyte effects on major insect pests in Waikato dairy pasture. Proceedings of the New Zealand Grassland Association 71, 121–126.
| Endophyte effects on major insect pests in Waikato dairy pasture.Crossref | GoogleScholarGoogle Scholar |
Popay AJ, Hume DE, Davis KL, Tapper BA (2003) Interactions between endophyte (Neotyphodium spp.) and ploidy in hybrid and perennial ryegrass cultivars and their effects on Argentine stem weevil (Listronotus bonariensis). New Zealand Journal of Agricultural Research 46, 311–319.
| Interactions between endophyte (Neotyphodium spp.) and ploidy in hybrid and perennial ryegrass cultivars and their effects on Argentine stem weevil (Listronotus bonariensis).Crossref | GoogleScholarGoogle Scholar |
Prestidge RA, Ball OJP (1995) ‘A catch 22’: the utilization of endophytic fungi for pest management. In ‘Multitrophic interactions in terrestrial systems: the 36th symposium of the British Ecological Society’. (Eds AC Gange, VK Brown) (Royal Holloway College, University of London: London, UK)
Prestidge RA, Pottinger RP, Barker GM (1982) An association of Lolium endophyte with ryegrass resistance to Argentine stem weevil. In ‘Proceedings of the 35th New Zealand Weed and Pest Control Conference’. pp. 119–122.
Rasmussen S, Lane GA, Mace W, Parsons AJ, Fraser K, Xue H (2012) The use of genomics and metabolomics methods to quantify fungal endosymbionts and alkaloids in grasses. In ‘Methods in molecular biology (Methods and Protocols)’. Vol. 860. (Eds N Hardy, R Hall) pp. 213–226. (Humana Press)
Rowan DD, Gaynor DL (1986) Isolation of feeding deterrents against Argentine stem weevil from ryegrass infected with the endophyte Acremonium loliae. Journal of Chemical Ecology 12, 647–658.
| Isolation of feeding deterrents against Argentine stem weevil from ryegrass infected with the endophyte Acremonium loliae.Crossref | GoogleScholarGoogle Scholar | 24306905PubMed |
Simpson WR, Schmid J, Singh JB, Faville MJ, Johnson RD (2012) A morphological change in the fungal symbiont Neotyphodium lolii induces dwarfing in its host plant Lolium perenne. Fungal Biology 116, 234–240.
| A morphological change in the fungal symbiont Neotyphodium lolii induces dwarfing in its host plant Lolium perenne.Crossref | GoogleScholarGoogle Scholar | 22289769PubMed |
Tapper BA, Latch GCM (1999) Selection against toxin production in endophyte-infected perennial ryegrass. In ‘Ryegrass endophyte: an essential New Zealand symbiosis’. Grassland Research and Practice Series 7. (Eds DR Woodfield, C Matthew) pp. 107–111.
Thom ER, Popay AJ, Hume DE, Fletcher LR (2012) Evaluating the performance of endophytes in farm systems to improve farmer outcomes – a review. Crop & Pasture Science 63, 927–943.
| Evaluating the performance of endophytes in farm systems to improve farmer outcomes – a review.Crossref | GoogleScholarGoogle Scholar |
Thom ER, Popay AJ, Waugh CD, Minnee EMK (2014) Impact of novel endophytes in perennial ryegrass on herbage production and insect pests from pastures under dairy cow grazing in northern New Zealand. Grass and Forage Science 69, 191–204.
| Impact of novel endophytes in perennial ryegrass on herbage production and insect pests from pastures under dairy cow grazing in northern New Zealand.Crossref | GoogleScholarGoogle Scholar |
Wool D, Manheim O (1986) Population ecology of the gall-forming aphid, Aploneura lentisci (Pass.) in Israel. Researches on Population Ecology 28, 151–162.
| Population ecology of the gall-forming aphid, Aploneura lentisci (Pass.) in Israel.Crossref | GoogleScholarGoogle Scholar |
Yates SG, Fenster JC, Bartelt RJ (1989) Assay of tall fescue seed extracts, fractions, and alkaloids using the large milkweed bug. Journal of Agricultural and Food Chemistry 37, 354–357.
| Assay of tall fescue seed extracts, fractions, and alkaloids using the large milkweed bug.Crossref | GoogleScholarGoogle Scholar |
