Endophyte-mediated tritrophic interactions between a grass-feeding caterpillar and two parasitoid species with different life histories

Arthropod-Plant Interactions

Volumn 6, Issue 1, 2012, Pages 27-34

  Bixby Brosi, Andrea J ^a   Potter, Daniel A ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Encyrtidae; Life history strategy; Neotyphodium; Parasitoids; Tachinidae; Tritrophic interactions

Indexed keywords

CATERPILLAR; ENDOPHYTE; GRASS; HOST-PARASITE INTERACTION; LIFE HISTORY; PARASITOID; TRITROPHIC INTERACTION; WASP;

AGROTIS IPSILON; COPIDOSOMA; ENCYRTIDAE; LOLIUM PERENNE; NEOTYPHODIUM; NOCTUIDAE; POACEAE; TACHINIDAE;

EID: 84857448336     PISSN: 18728855     EISSN: 18728847     Source Type: Journal    
DOI: 10.1007/s11829-011-9163-2     Document Type: Article

References (66)

1. Analytical Software (2008) Statistix version 8, user's manual. Analytical Software, Tallahassee.
2. Arnaud PH Jr (1978) A host-parasite catalog of North American Tachinidae (Diptera). Misc Pub, No. 1319, SEA, USDA, 860 pp.
3. Bacon CW, Lyons PC, Porter JK, Robbins JD (1986) Ergot toxicity from endophyte-infected grasses: A review. Agron J 78: 106-116.
4. Baehrecke EH, Strand MR (1990) Embryonic morphology and growth of the polyembryonic parasitoid Copidosoma floridanum (Ashmead) (Hymenoptera: Encyrtidae). Int J Insect Morphol Embryol 19: 165-175.
5. Barbosa P, Saunders J (1985) Plant allelochemicals: linkages between herbivores and their natural enemies. In: Cooper-Driver GA, Swain T, Conn EE (eds) Chemically mediated interactions between plants and other organisms. Plenum, New York, pp 107-138.
6. Barbosa P, Gross P, Kemper J (1991) Influence of plant allelochemicals on the tobacco hornworm and its parasitoid, Cotesia congregate. Ecology 72: 1567-1575.
7. Barker GM, Addison PJ (1996) Influence of clavicipitaceous endophyte infection in ryegrass on development of the parasitoid Microctonus hyperodae Loan (Hymenoptera: Braconidae) in Listronotus bonariensis (Kuschel) (Coleoptera: Curculionidae). Biol Control 7: 281-287.
8. Barker GM, Addison PJ (1997) Clavicipitaceous endophytic infection in ryegrass influences attack rate of the parasitoid Microctonus hyperodae (Hymenoptera: Braconidae, Euphorinae) in Listronotus bonariensis (Coleoptera: Curculionidae). Environ Entomol 26: 416-420.
9. Beach RM, Todd LW (1986) Foliage consumption and larval development of parasitized and unparasitized soybean looper, Pseudoplusia includes [Lep: Noctuidae], reared on resistant soybean genotype and effects on an associated parasitoid, Copidosoma truncatellum [Hym: Encyrtidae]. Entomophaga 31: 237-242.
10. Bixby-Brosi AJ, Potter DA (2010) Evaluating a naturally occurring baculovirus for extended biological control of the black cutworm (Lepidoptera: Noctuidae) in golf course habitats. J Econ Entomol 103: 1555-1563.
11. Blanco CA, Portilla M, Abel CA, Winters H, Ford R, Streett D (2009) Soybean flour and wheat germ proportions in artificial diet and their effect on the growth rates of the tobacco budworm, Heliothis virescens. J Insect Sci 9: 59.
12. Breen JP (1994) Acremonium endophyte interactions with enhanced plant resistance to insects. Ann Rev Entomol 39: 401-423.
13. Bultman TL, Borowicz KL, Schneble RM, Coudron TA, Bush LP (1997) Effect of a fungal endophyte on the growth and survival of two euplectrus parasitoids. Oikos 78: 170-176.
14. Bush LP, Wilkinson HH, Schardl CL (1997) Bioprotective alkaloids of grass-fungal endophyte symbioses. Plant Physiol 114: 1-7.
15. Byers JR, Yu DS, Jones W (1993) Parasitism of the army cutworm, Euxoa auxiliaris (GRT) (Lepidoptera: Noctuidae), by Copidosoma bakeri (Howard) (Hymenoptera: Encyrtidae) and effect on crop damage. Can Entomol 125: 329-335.
16. Campbell BC, Duffey SS (1979) Tomatine and parasitic wasps: potential incompatibility of plant antibiosis with biological control. Science 205: 700-702.
17. Clay K (1991) Fungal endophytes, grasses and herbivores. In: Barbosa P, Krischik VA, Jones CG (eds) Microbial mediation of plant-herbivore interactions. Wiley, New York, pp 199-252.
18. Clay K (1997) Fungal endophytes, herbivores and the structure of grassland communities. In: Gange AC, Brown VK (eds) Multitrophic interactions in terrestrial systems. Cambridge University Press, Cambridge, pp 151-170.
19. Cossentine JE, Lewis LC (1986) Potential of Bonnetia comta (Diptera: Tachinidae) in combination with a nuclear polyhedrosis virus to control Agrotis ipsilon (Lepidoptera: Noctuidae) larvae on corn. Environ Entomol 15: 360-364.
20. Crumb SE (1956) The larvae of the Phalaenidae. USDA Tech Bull 1135: 356.
21. De Moraes CM, Lewis WJ, Pare PW, Alborn HT, Tumlinson JH (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393: 570-573.
22. Duffey SS, Bloem KA, Campbell BC (1986) Consequences of sequestration of plant natural products in plant-insect-parasitoid interactions. In: Boethel DJ, Eikenbary RD (eds) Interactions of plant resistance and parasitoids and predators of insects. Ellis Horwood Limited, UK, pp 31-60.
23. Farrar RR Jr, Kennedy GG (1993) Field cage performance of two parasitoids of the tomato fruitworm on insect resistant and susceptible tomato lines. Entomol Exp Appl 67: 73-78.
24. Farrar RR Jr, Kennedy GG, Kashyap RK (1992) Influence of life history differences of two tachinid parasitoids of Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) on their interactions with glandular trichome/methyl Ketone-based insect resistance in tomato. J Chem Ecol 18: 499-515.
25. Fukushima J, Kainoh Y, Honda H, Takabayashi J (2002) Learning of herbivore-induced and nonspecific plant volatiles by a parasitoid, Cotesia kariyai. J Chem Ecol 28: 579-586.
26. Gauld ID, Gaston KJ (1994) The taste of enemy-free space: parasitoids and nasty hosts. In: Hawkins BA, Sheehan W (eds) Parasitoids community ecology. Oxford University Press, Oxford, pp 279-299.
27. Godfray HCJ (1994) Parasitoids: behavior and evolutionary ecology. Princeton University Press, Princeton.
28. Heil M (2008) Indirect defense via tritrophic interactions. New Phytol 178: 41-61.
29. Ivanova-Kasas OM (1972) Polyembryony in insects. In: Counce SJ, Waddington CH (eds) Developmental systems, vol 2. Insects. Academic Press, New York, pp 243-271.
30. Kennedy GG (2003) Tomato, pests, parasitoids, and predators: tritrophic interactions involving the genus Lycopersicon. Annu. Rev. Entomol 48: 51-72.
31. Kunkel BA, Grewal PS (2003) Endophyte infection in perennial ryegrass reduces the susceptibility of black cutworm to entomopathogenic nematodes. Entomol Exp Appl 107: 95-104.
32. Lampert EC, Bowers MD (2010) Host plant species affects the quality of the generalist Trichoplusia ni as a host for the polyembryonic parasitoid Copidosoma floridanum. Entomol Exp Appl 134: 287-295.
33. Lampert EC, Zangerl AR, Berenbaum MR, Ode PJ (2011) Generalist and specialist host-parasitoid associations respond differently to wild parsnip (Pastinaca sativa) defensive chemistry. Ecol Entomol 36: 52-61.
34. Levine E, Clement SL (1981) Effect of Parasitism by Bonnetia comta on larvae of Agrotis ipsilon. J Kansas Ent Soc 54: 219-222.
35. Mackauer M, Sequeira R (1993) Patterns of development in insect parasites. In: Beckage NE et al (eds) Parasites and pathogens of insects, vol 1 parasites. Academic Press, New york, pp 1-23.
36. Nordlund DA, Lewis WJ, Altieri MA (1988) Influences of plant-produced allelochemicals on the host-prey selection behavior of entomophagous insects. In: Barbosa P, le Tourneau DK (eds) Novel aspects of insect-plant interactions. Wiley, New York, pp 65-90.
37. Ode PJ, Strand MR (1995) Progeny and sex allocation decisions of the polyembryonic wasp Copidosoma floridanum. J Animal Ecol 64: 213-224.
38. O'Hara JE (2008) Tachinid flies (Diptera: Tachinidae). In: Capinera JL (ed) Encyclopedia of entomology vol 4, S-Z, 2nd edn. Springer, Dordrecht, pp 3675-3686.
39. O'Hara JE, Wood DM (2004) Catalogue of the Tachinidae (Diptera) of America north of Mexico. Mem Entomol Int 18: 410.
40. Omacini M, Chaneton EJ, Ghersa CM, Muller CB (2001) Symbiotic fungal endophytes control insect host-parasite interaction webs. Nature 409: 78-81.
41. Orr DB, Boethel DJ (1985) Comparative development of Copidosoma truncatellum (Hymenoptera: Encyrtidae) and its host, Pseudoplusia includes (Lepidoptera: Noctuidae), on resistant and susceptible soybean genotypes. Environ Entomol 14: 612-616.
42. Potter DA (1998) Destructive turfgrass insects: biology, diagnosis and control. Wiley, New York.
43. Potter DA, Stokes JT, Redmond CT, Schardl CL, Panaccione DG (2008) Contribution of ergot alkaloids to suppression of a grass-feeding caterpillar assessed with gene knockout endophytes in perennial ryegrass. Entomol Exp Appl 126: 138-147.
44. Price PW (1986) Ecological aspects of host plant resistance and biological control: interactions among three trophic levels. In: Boethel DJ, Eikenbary RD (eds) Interactions of plant resistance and parasitoids and predators of insects. Horwood, UK, pp 11-30.
45. Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weis AE (1980) Interactions among three trophic levels-influence of plants on interactions between insect herbivores and natural enemies. Annu Rev Ecol Syst 11: 41-65.
46. Reitz SR, Trumble JT (1996) Tritrophic interactions among linear furanocoumarins, the herbivore Trichoplusia ni (Lepidoptera: Noctuidae), and the polyembryonic parasitoid Copidisoma floridanum (Hymenoptera: Encyrtidae). Environ Entomol 25: 1391-1397.
47. Richmond DS, Niemczyk HD, Shetlar DJ (2000) Overseeding endophytic perennial ryegrass into stands of Kentucky bluegrass to manage bluegrass billbug (Coleoptera: Curculionidae). J Econ Entomol 93: 1662-1668.
48. Rubink WL, Clement SL (1982) Reproductive biology of Bonnetia comta (Fallen) (Diptera: Tachinidae), a parasitoid of the black cutworm, Agrotis ipsilon Hufnagel (Lepidoptera: Noctuidae). Environ Entomol 11: 981-985.
49. Saeki Y, Crowley PH, Fox CW, Potter DA (2009) A sex-specific tradeoff in clonal broods. Oikos 188: 1552-1560.
50. Schaaf AC (1972) The parasitoid complex of Euxoa ochrogaster (Guenee) (Lepidoptera: Noctuidae). Quaest Entomol 8: 81-120.
51. Schardl CL, Leuchtmann A, Spiering MJ (2004) Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol 55: 315-340.
52. Schardl CL, Panaccione DG, Tudzynski P (2006) Ergot alkaloids-biology and molecular biology. In: Corell GA (ed) The alkaloids: chemistry and biology. Elsevier, UK, pp 45-86.
53. Senthamizhselvan M, Muthukrishnan J (1989) Effect of parasitization by a gregarious and a solitary parasitoid on food consumption and utilization by Porthesia scintillans Walker (Lepidoptera: Lymantriidae) and Spodoptera exigua Hubner (Lepidoptera: Noctuidae). Parasitol Res 76: 166-170.
54. Shelby RA, Dalrymple LWT (1987) Incidence and distribution of the tall fescue endophyte in the United States. Plant Dis 71: 783-786.
55. Siegel MR, Bush LP (1996) Defensive chemicals in grass-fungal endophyte associations. In: Romeo JT, Saunders JA, Barbosa P (eds) Phytochemical diversity and redundancy in ecological interactions, recent advances in phytochemistry, vol 30. Springer, Boston, pp 81-120.
56. Siegel MR, Latch GCM, Johnson MC (1987) Fungal endophytes of grasses. Annu Rev Phytopathol 25: 293-315.
57. Singer MS, Mace KC, Bernays EA (2009) Self-medication as adaptive plasticity: increased ingestion of plant toxins by parasitized caterpillars. PLoS ONE 4: e4796.
58. Slansky F Jr (1986) Nutritional ecology of endoparasitic insects and their hosts: an overview. J Insect Physiol 32: 255-261.
59. Strand MR (1989a) Development of the polyembryonic parasitoid Copidosoma floridanum in Trichoplusia ni. Entomol. Exp. Appl. 50: 37-46.
60. Strand MR (1989b) Oviposition behavior and progeny allocation of the polyembryonic wasp Copidosoma floridanum (Hymenoptera: Encyrtidae). J Insect Behav 2: 355-369.
61. Thorpe KW, Barbosa P (1986) Effects of consumption of high and low nicotine tobacco by Manduca sexta (Lepidoptera: Sphingidae) on survival of gregarious endoparasitoid Cotesia congregate (Hymenoptera: Braconidae). J Chem Ecol 12: 1329-1337.
62. Turlings TCJ, Benrey B (1998) Effects of plant metabolites on the behavior and development of parasitic wasps. Ecoscience 5: 321-333.
63. Turlings TCJ, Wäckers FL, Vet LEM, Lewis WJ, Tumlinson JH (1992) Learning of host-location cues by hymenopterous parasitoids. In: Lewis AC, Papaj DR (eds) Insect learning: ecological and evolutionary perspectives. Chapman and Hall, New York, pp 51-78.
64. van der Meijden E (1980) Can hosts escape from their parasitoids? The effects of food shortage on the braconid parasitoid Apanteles popularis and its host Tyria jacobaeae. Neth J Zool 30: 382-392.
65. Williamson RC, Potter DA (1997) Turfgrass species and endophyte effects on survival, development, and feeding preference of black cutworms. J Econ Entomol 90: 1290-1299.
66. Wood DM (1987) Tachinidae. In: McAlpine JF (ed) Manual of Nearctic Diptera volume 2. Research branch, Agriculture Canada. Monograph No.28. pp 1193-1269.