Mollusc herbivory influenced by endophytic clavicipitaceous fungal infections in grasses

Annals of Applied Biology

Volumn 153, Issue 3, 2008, Pages 381-393

  Barker, G M ^a  

^a LANDCARE RESEARCH   (New Zealand)

Author keywords

Deroceras panormitanum; Deroceras reticulatum; Fescue; Festuca; Fungal endophytes; Lolium; Neotyphodium; Ryegrass; Secondary metabolites

Indexed keywords

ARTIFICIAL DIET; DISEASE RESISTANCE; ENDOPHYTE; EXPERIMENTAL STUDY; FOOD PREFERENCE; FUNGAL DISEASE; FUNGUS; GRASS; HERBIVORE; MOLLUSC; PEST CONTROL; SECONDARY METABOLITE; YIELD;

DEROCERAS; DEROCERAS PANORMITANUM; DEROCERAS RETICULATUM; FESTUCA; FUNGI; GASTROPODA; HEXAPODA; LOLIUM; MOLLUSCA; NEOTYPHODIUM; POACEAE; VERTEBRATA;

EID: 57349147715     PISSN: 00034746     EISSN: 17447348     Source Type: Journal    
DOI: 10.1111/j.1744-7348.2008.00267.x     Document Type: Article

References (81)

1. Aguiar R., Wink M 2005) How do slugs cope with toxic alkaloids? Chemoecology, 15, 167 177.
2. Bacon C.W., White J.F Eds 1994) Biotechnology of Endophytic Fungi of Grasses. Ann Arbor, MI, USA : CRC Press.
3. Ball O.J.-P., Prestidge R.A., Sprosen J.M 1995) Interrelationships between Acremonium lolii, peramine, and lolitrem B in perennial ryegrass. Applied and Environmental Microbiology, 61, 1527 1533.
4. Ball O.J.-P., Barker G.M., Prestidge R.A., Lauren D.R 1997) Distribution and accumulation of the alkaloid peramine in Neotyphodium lolii-infected perennial ryegrass. Journal of Chemical Ecology, 23, 1419 1434.
5. Ball O.J.-P., Coudron T.A., Tapper B.A., Davies E., Trently D., Bush L.P., Gwinn K.D., Popay A.J 2006) Importance of host plant species, Neotyphodium endophyte isolate, and alkaloids on feeding by Spodoptera frugiperda (Lepidoptera: Noctuidae) larvae. Journal of Economic Entomology, 99, 1462 1473.
6. Barker G.M Ed 2002) Molluscs as Crop Pests. Wallingford, UK : CABI Publishing.
7. Bony S., Pichon N., Ravel C., Durix A., Balfourier F., Guillaumin J.-J 2001) The relationship between mycotoxin synthesis and isolate morphology in fungal endophytes of Lolium perenne. New Phytologist, 152, 125 137.
8. Bouton J.H., Latch G.C.M., Hill N.S., Hoveland C.S., McCann M.A., Watson R.H., Parish J.A., Hawkins L.L., Thompson F.N 2002) Reinfection of tall fescue cultivars with non-ergot alkaloid-producing endophytes. Agronomy Journal, 94, 567 574.
9. Brattsten L.B 1988) Enzymic adaptations in leaf-feeding insects to host-plant allelochemicals. Journal of Chemical Ecology, 14, 1919 1939.
10. Bultman T.L., Pulas C., Grant L., Bell G., Sullivan T.J 2006) Effects of fungal endophyte isolate on performance and preference of bird cherry-oat aphid. Environmental Entomology, 35, 1690 1695.
11. Burgess R.S.L., Ennos R.A 1987) Selective grazing of acyanogenic white clover: variation in behaviour among populations of the slug Deroceras reticulatum. Oecologia, 73, 432 435.
12. Bush L.P., Fannin F.F., Siegel M.R., Dahlman D.L., Burton H.R 1993) Chemistry, occurrence and biological effects of saturated pyrrolizidine alkaloids associated with endophyte-grass interactions. Agriculture, Ecosystems and Environment, 44, 81 102.
13. Bush L.P., Wilkinson H.H., Schardl C.L 1997) Bioprotective alkaloids of grass-fungal endophyte symbioses. Plant Pathology, 114, 1 7.
14. Cater M.A., Jeffery R.C.V., Williamson P 1979) Food overlap in co-existing populations of the land snails Cepaea nemoralis (L.) and Cepaea hortensis (Müll.). Biological Journal of the Linnean Society, 11, 169 176.
15. Chang H.-W 1991) Food preference of the land snail Cepaea nemoralis in a North American population. Malacological Review, 24, 107 114.
16. Christensen M.J., Latch G.C.M., Tapper B.A 1991) Variation within isolates of Acremonium endophytes from perennial rye-grass. Mycological Research, 94, 918 923.
17. Christensen M.J., Leuchtmann A., Rowan D.D., Tapper B.A 1993) Taxonomy of Acremonium endophytes of tall fescue (Festuca arundinacea), meadow fescue (F. pratensis) and perennial rye-grass (Lolium perenne). Mycological Research, 97, 1083 1092.
18. Clay K 1990) Fungal endophytes of grasses. Annual Review of Ecology and Systematics, 21, 275 297.
19. Clay K 1994) The potential role of endophytes in ecosystems. In Biotechnology of Endophytic Fungi of Grasses, pp. 73 86. Eds C.W. Bacon and J.F. White. Ann Arbor, MI, USA : CRC Press.
20. Clay K., Schardl C.L 2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. The American Naturalist, 160, S99 S127.
21. Cottam D.A 1985) Frequency-dependent grazing by slugs and grasshoppers. Journal of Ecology, 73, 925 933.
22. Craven K.D., Blankenship J.D., Leuchtmann A., Hignight J.K., Schardl C.L 2001a) Hybrid fungal endophytes symbiotic with the grass Lolium pratense. Sydowia, 53, 44 73.
23. Craven K.D., Hsiau P.T.W., Leuchtmann A., Hollin W., Schardl C.L 2001b) Multigene phylogeny of Epichloë species, fungal symbionts of grasses. Annals of the Missouri Botanical Garden, 88, 14 34.
24. Davies E., Lane G.A., Latch G.C.M., Tapper B.A., Garthwaite I., Towers N.R., Fletcher L.R., Pownall D.B 1993) Alkaloid concentrations in field-grown synthetic perennial ryegrass endophyte associations. In Proceedings of the Second International Symposium on Acremonium/Grass Interactions, pp. 72 76. Eds D.E. Hume, G.C.M. Latch and H.S. Easton. Palmerston North, New Zealand : AgResearch.
25. Delaney K., Gelperin A 1986) Post-ingestive food-aversion learning to amino acid deficient diets by the terrestrial slug Limax maximus. Journal of Comparative Physiology A, 159, 281 295.
26. Dirzo R 1980) Experimental studies on slug-plant interactions. 1. The acceptability of thirty plant species to the slug Agriolimax caruanae. Journal of Ecology, 68, 981 998.
27. Fletcher L.R., Easton H.S 1997) The evaluation and use of endophytes for pasture improvement. In Neotyphodium/Grass Interactions, pp. 207 227. Eds C.W. Bacon and N.S. Hill. New York, NY, USA : Plenum Press.
28. Gallagher R.T., Hawkes A.D., Stewart J.M 1985) Rapid determination of the neurotoxin lolitrem B in perennial ryegrass by high-performance liquid chromatography with fluorescence detection. Journal of Chromatography, 321, 217 226.
29. Garner G.B., Rottinghaus G.E., Cornell C.N., Testereci H 1993) Chemistry of compounds associated with endophyte/grass interaction: ergovaline- and ergopeptine-related alkaloids. Agriculture, Ecosystems and Environment, 44, 65 80.
30. Gelperin A 1975) Rapid food-aversion learning by a terrestrial mollusk. Science, 189, 567 570.
31. Gouyon P.H., Fort P.H., Caraux G 1983) Selection of seedlings of Thymus vulgaris by grazing slugs. Journal of Ecology, 71, 299 306.
32. Grime G.P., Blythe G.M 1969) Relationships between snails and vegetation at the Winnats Pass. Journal of Ecology, 57, 45 66.
33. Grime G.P., MacPherson-Stewart S.F., Dearman R.S 1968) An investigation of leaf palatability using the snail Cepaea nemoralis L. Journal of Ecology, 56, 405 420.
34. Hartmann T 1991) Alkaloids. In Herbivores. Their Interactions with Secondary Plant Metabolites, the Chemical Participants. Volume 1, pp. 79 121. Eds G.A. Rosenthal and M.R. Berenbaum. New York, NY, USA : Academic Press.
35. Ingram W.M., Peterson A 1947) Food of the giant western slug, Ariolimax columbianus (Gould). The Nautilus, 61, 49 51.
36. Johnson M.C., Bush L.P., Siegel M.R 1986) Infection of tall fescue with Acremonium coenophialum by means of callus culture. Plant Diseases, 70, 380 382.
37. Kearney J.F., Parrott W.A., Hill N.S 1991) Infection of somatic embryos of tall fescue with Acremonium coenophialum. Crop Science, 31, 979 984.
38. Kuldau G.A., Tsai H.-F., Schardl C.L 1999) Genome sizes of Epichloë species and anamorphic hybrids. Mycologia, 91, 776 782.
39. Lane G.A 1999) Chemistry of endophytes: patterns and diversity. In Ryegrass Endophyte: an Essential New Zealand Symbiosis. Grassland Research and Practice Series No. 7, pp. 85 94. Palmerston North, New Zealand : New Zealand Grassland Association.
40. Lane G.A., Christensen M.J., Miles C.O 2000) Coevolution of fungal endophytes with grasses: the significance of secondary metabolites. In Microbial Endophytes, pp 341 388. Eds C.W. Bacon and J.F. White. New York, USA : Marcel Dekker.
41. Latch G.C.M 1989) Plant improvement using endophytic fungi. In Proceedings of the XVI International Grassland Congress, pp. 345 346. Ed. Association Française pour la Production Fourragère. Nice, France : Association Française pour la Production Fourragère.
42. Latch G.C.M 1993) Physiological interactions of endophytic fungi and their hosts. Biotic stress tolerance imparted to grasses by endophytes. Agriculture, Ecosystems and Environment, 44, 143 156.
43. Latch G.C.M 1994) Influence of Acremonium endophytes on perennial ryegrass improvement. New Zealand Journal of Agricultural Research, 37, 311 318.
44. Latch G.C.M., Christensen M.J 1985) Artificial infection of grasses with endophytes. Annals of Applied Biology, 107, 17 24.
45. Lee J.H., Chang J.J 1986) Learning of post-ingestive food-aversion by the land slug Incilaria frühstorferi daiseniana to amino acid deficient diets. Society of Neuroscience Abstracts, 12, 39.
46. Leuchtmann A., Schmidt D., Bush L.P 2000) Different levels of protective alkaloids in grasses with stroma-forming and seed-transmitted Epichloë/Neotyphodium endophytes. Journal of Chemical Ecology, 26, 1025 1036.
47. Linhart Y.B., Thompson J.D 1995) Terpene-based selective herbivory by Helix aspersa (Mollusca) on Thymus vulgaris (Labiatae). Oecologia, 102, 126 132.
48. Miles C.O., Wilkins A.L., Gallagher R.T., Hawkes A.D., Munday S.C., Towers N.R 1992) Synthesis and tremorgenicity of paxitriols and lolitriol: possible biosynthetic precursors of lolitrem B. Journal of Agricultural and Food Chemistry, 40, 234 238.
49. Miles C.O., Munday S.C., Wilkins A.L., Ede R.M., Hawkes A.D., Embling P.P., Towers N.R 1993) Large scale isolation of lolitrem B, structure determination of some minor lolitrems, and tremorgenic activities of lolitrem B and paxilline in sheep. In Proceedings of the Second International Symposium on Acremonium/Grass Interactions, pp. 85 87. Eds D.E. Hume, G.C.M. Latch and H.S. Easton. Palmerston North, New Zealand : AgResearch.
50. Miles C.O., Munday S.C., Wilkins A.L., Ede R.M., Towers N.R 1994) Large-scale isolation of lolitrem B and structure elucidation of lolitrem E. Journal of Agricultural Food Chemistry, 42, 1488 1492.
51. Miles C.O., di Menna M.E., Jacobs S.W.L., Garthwaite I., Lane G.A., Prestidge R.A., Marshall S.L., Wilkinson H.H., Schardl C.L., Ball O.J.-P., Latch G.C.M 1998) Endophytic fungi in indigenous Australasian grasses associated with toxicity to livestock. Applied and Environmental Microbiology, 64, 601 606.
52. O'Sullivan B.D., Latch G.C.M 1993) Infection of plantlets, derived from ryegrass and tall fescue meristems, with Acremonium endophytes. In Proceedings of the Second International Symposium on Acremonium/Grass Interactions, pp. 16 17. Eds D.E. Hume, G.C.M. Latch and H.S Easton. Palmerston North, New Zealand : AgResearch.
53. Pallant D 1969) The food of the grey field slug (Agriolimax reticulatus (Müller) in woodland. Journal of Animal Ecology, 38, 391 398.
54. Pallant D 1972) The food of the grey field slug (Agriolimax reticulatus (Müller) in grassland. Journal of Animal Ecology, 41, 761 769.
55. Panaccione D.G., Johnson R.D., Wang J., Young C.A., Damrongkool P., Scott B., Schardl C.L 2001) Elimination of ergovaline from a grass-Neotyphodium endophyte symbiosis by genetic modification of the endophyte. Proceedings of the National Academy of Sciences of the United States of America, 98, 12820 12825.
56. Parish J.A., McCann M.A., Watson R.H., Hoveland C.S., Hawkins L.L., Hill N.S., Bouton J.H 2003) Use of nonergot alkaloid-producing endophytes for alleviating tall fescue toxicosis in sheep. Journal of Animal Science, 81, 1316 1322.
57. Penn J., Garthwaite I., Christensen M.J., Johnson C.M., Towers N.R 1993) The importance of paxilline in screening for potentially tremorgenic Acremonium isolates. In Proceedings of the Second International Symposium on Acremonium/Grass Interactions, pp. 88 92. Eds D.E. Hume, G.C.M. Latch and H.S. Easton. Palmerston North, New Zealand : AgResearch.
58. Popay A.J., Ball O.J.-P 1998) The development of fungal endophytes as a pest management tool for New Zealand grasslands. In Pest Management - Future Challenges, Proceedings of the Sixth Australasian Applied Entomological Research Conference. Volume 1, pp. 373 381. Eds M.P. Zalucki, R.A.I. Drew and G.G. White. Brisbane, Australia : The University of Queensland Printery.
59. Popay A.J., Rowan D.D 1994) Endophytic fungi as mediators of plant-insect interactions. In Insect-Plant Interactions. Volume 1, pp. 83 103. Ed. E.A. Bernays. Boca Raton, FL, USA : CRC Press.
60. Porter J.K 1994) Chemical constituents of grass endophytes. In Biotechnology of Endophytic Fungi of Grasses, pp. 103 123. Eds C.W. Bacon and J.F. White. Ann Arbor, MI, USA : CRC Press.
61. Rice R.L., Lincoln D.E., Langenheim J.H 1978) Palatability of monoterpenoid compositional types of Satureja douglassii to a generalist molluscan herbivore, Ariolimax dolichophallus. Biochemical Systematics and Ecology, 6, 45 53.
62. Rowan D.D 1993) Lolitrems, peramine and paxilline: mycotoxins of the ryegrass/endophyte interaction. Agriculture, Ecosystems and Environment, 44, 103 122.
63. Rowan D.D., Gaynor D.L 1986) Isolation of feeding deterrents against Argentine stem weevil from ryegrass infected with the endophyte Acremonium loliae. Journal of Chemical Ecology, 12, 647 658.
64. Rowan D.D., Latch G.C.M 1994) Utilization of endophyte-infected perennial ryegrass for increased insect resistance. In Biotechnology of Endophytic Fungi of Grasses, pp. 169 183. Eds C.W. Bacon and J.F White. Ann Arbor, MI, USA : CRC Press.
65. Rudgers J.A., Koslow J.M., Clay K 2004) Endophytic fungi alter relationships between diversity and ecosystem properties. Ecology Letters, 7, 42 51.
66. Sahley C., Gelperin A., Rudy J.W 1981a) One-trial associative learning modifies food odor preferences of a terrestrial mollusc. Proceedings of the National Academy of Sciences of the United States of America, 78, 640 642.
67. Sahley C., Rudy J.W., Gelperin A 1981b) An analysis of associative learning in a terrestrial mollusc. Journal of Comparative Physiology A, 144, 1 8.
68. Schardl C.L., Clay K 1997) Evolution of mutualistic endophytes from plant pathogens. In The Mycota Plant Relationships, Part B. Volume 5, pp. 221 238. Eds G.C. Carroll and P. Tudzynski. Berlin, Germany : Springer-Verlag.
69. Schardl C.L., Craven K.D 2003) Interspecific hybrization in plant-associated fungi and oomycetes: a review. Molecular Ecology, 12, 2861 2873.
70. Schardl C.L., Leuchtmann A., Tsai H.-F., Collett M.A., Watt D.M., Scott D.B 1994) Origin of a fungal symbiont of perennial ryegrass by interspecific hybridization of a mutualist with the ryegrass choke pathogen, Epichloë typhina. Genetics, 136, 1307 1317.
71. Speiser B., Rowell-Rahier M 1991) Effects of food availability, nutritive value, and alkaloids on food choice in the generalist herbivore Arianta arbustorum (Gastropoda: Helicidae). Oikos, 62, 306 318.
72. Speiser B., Harmatha J., Rowell-Rahier M 1992) Effects of pyrrolizidine alkaloids and sequiterpenes on snail feeding. Oecologia, 92, 257 265.
73. Tapper B.A., Rowan D.D., Latch G.C.M 1989) Detection and measurement of the alkaloid peramine in endophyte-infected grasses. Journal of Chromatography, 463, 133 138.
74. Tsai H.-F., Siegel M.R., Schardl C.L 1992) Transformation of Acremonium coenophialum, a protective fungal symbiont of the grass Festuca arundinacea. Current Genetics, 22, 399 406.
75. Tsai H.-F., Liu J.S., Staben C., Christensen M.J., Latch G.C.M., Siegel M.R., Schardl C.L 1994) Evolutionary diversification of fungal endophytes of tall fescue grass by hybridization with Epichloë species. Proceedings of the National Academy of Sciences of the United States of America, 91, 2542 2546.
76. Whelan R.J 1982) Response of slugs to unacceptable food items. Journal of Applied Ecology, 19, 79 87.
77. White J.F 1988) Endophyte-host associations in forage grasses. XI. A proposal concerning origin and evolution. Mycologia, 80, 442 446.
78. Wilkinson H.H., Siegel M.R., Blankenship J.D., Mallory A.C., Bush L.P., Schardl C.L 2000) Contribution of fungal loline alkaloids to protection from aphids in a grass-endophyte mutualism. Molecular Plant-Microbe Interactions, 13, 1027 1033.
79. Williamson P., Cameron R.A.D 1976) Natural diet of the landsnail Cepaea nemoralis. Oikos, 27, 493 500.
80. Wilson D 1993) Fungal endophytes: out of sight but should not be out of mind. Oikos, 68, 379 384.
81. Wink M 1993) Allelochemical properties or the raison d'être of alkaloids. In The Alkaloids. Volume 43, pp. 171 213. Ed. G.A. Cordell. London, UK : Academic Press.