Subterranean, herbivore-induced plant volatile increases biological control activity of multiple beneficial nematode species in distinct habitats

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Ali, Jared G ^a,e   Alborn, Hans T ^b   Campos Herrera, Raquel ^a,c   Kaplan, Fatma ^b   Duncan, Larry W ^a   Rodriguez Saona, Cesar ^d   Koppenhöfer, Albrecht M ^d   Stelinski, Lukasz L ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b CENTER FOR MEDICAL   (United States)

^c INSTITUTO DE CIENCIAS AGRARIAS   (Spain)

^d RUTGERS UNIVERSITY   (United States)

^e Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PREGEIJERENE; UNCLASSIFIED DRUG; VOLATILE AGENT;

ANOMALA ORIENTALIS; ARTICLE; BIOLOGICAL PEST CONTROL; BLUEBERRY; CITRUS; CONTROLLED STUDY; DIAPREPES ABBREVIATUS; ENTOMOPATHOGENIC NEMATODE; GALLERIA MELLONELLA; HABITAT; HERBIVORE; LARVA; MORTALITY; NONHUMAN; PLANT ROOT; REAL TIME POLYMERASE CHAIN REACTION; WEEVIL;

ANIMALS; CITRUS; ECOSYSTEM; FEEDING BEHAVIOR; FOOD CHAIN; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; HERBIVORY; HOST-PARASITE INTERACTIONS; HYDROCARBONS, CYCLIC; LARVA; PEST CONTROL, BIOLOGICAL; PLANT EXTRACTS; PLANT ROOTS; REAL-TIME POLYMERASE CHAIN REACTION; RHABDITIDA; RHABDITIDA INFECTIONS; WEEVILS;

ANOMALA ORIENTALIS; CITRUS; COLEOPTERA; DIAPREPES ABBREVIATUS; GALLERIA MELLONELLA; NEMATODA; VACCINIUM;

EID: 84863002872     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0038146     Document Type: Article

References (59)

1. Turlings TCJ, Tumlinson JH, Lewis WJ, (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250: 1251-1253.
2. Takabayashi J, Dicke M, (1996) Plant-carnivore mutualism through herbivore-induced carnivore attractants. Trends Plant Sci 1: 109-113.
3. Tumlinson J, Turlings T, Lewis W, (1993) Semiochemically mediated foraging behavior in beneficial parasitic insects. Arch Insect Biochem Physiol 22: 385-391.
4. Turlings TCJ, Wäckers F, (2004) Recruitment of predators and parasitoids by herbivore-injured plants. In: Cardé RT, Millar JG, editors. editors. Advances in insect chemical ecology. Cambridge University Press. pp 21-75.
5. Kant MR, Bleeker PM, Wijk MV, Schuurink RC, Haring MA, (2009) Plant volatiles in defense. In: Loon LCV, editors. editor. Advances in botanical research. Academic Press. pp 613-666.
6. Boff MIC, Zoon FC, Smits PH, (2001) Orientation of Heterorhabditis megidis to insect hosts and plant roots in a Y-tube sand olfactometer. Entomol Exp Appl 98: 329-337.
7. Ali JG, Alborn HT, Stelinski LL, (2010) Subterranean herbivore-induced volatiles released by citrus roots upon feeding by Diaprepes abbreviatus recruit entomopathogenic nematodes. J Chem Ecol 36: 361-368.
8. Ali JG, Alborn HT, Stelinski LL, (2011) Constitutive and induced subterranean plant volatiles attract both entomopathogenic and plant parasitic nematodes. J Ecol 99: 26-35.
9. Rasmann S, Agrawal AA, (2008) In defense of roots: A research agenda for studying plant resistance to belowground herbivory. Plant Physiol 146: 875-880.
10. van Tol RWHM, van der Sommen ATC, Boff MIC, van Bezooijen J, Sabelis MW, et al. (2001) Plants protect their roots by alerting the enemies of grubs. Ecol Lett 4: 292-294.
11. Rasmann S, Köllner TG, Degenhardt J, Hitpold I, Töpfer S, et al. (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434: 732-737.
12. Hiltpold I, Töpfer S, Kuhlmann U, Turlings TCJ, (2010) How maize root volatiles affect the efficacy of entomopathogenic nematodes in controlling the western corn rootworm? Chemoecology 20: 155-162.
13. Degenhardt J, Hiltpolt I, Köllner TG, Frey M, Gierl A, et al. (2009) Restoring a maize root signal that attracts insect-killing nematodes to control a major pest. Proc Natl Acad Sci USA 106: 13213-13218.
14. Hunter MD, (2001) Out of sight, out of mind: the impacts of root-feeding insects in natural and managed systems. Agr Forest Entomol 3: 3-9.
15. Beavers J, (1982) Biology of Diaprepes abbreviatus (Coleoptera: Curculionidae) reared on an artificial diet. Fla Entomol 65: 263-269.
16. Simpson SE, Nigg HN, Coile NC, Adair RA, (1996) Diaprepes abbreviatus (Coleoptera: Curculionidae): host plant associations. Environ Entomol 25: 333-349.
17. Graham J, Bright D, McCoy C, (2003) Phytophthora-Diaprepes weevil complex: Phytophthora spp. relationship with citrus rootstocks. Plant Dis 87: 85-90.
18. Bullock RC, Pelosi RR, Killer EE, (1999) Management of citrus root weevils (Coleoptera: Curculionidae) on Florida citrus with soil-applied entomopathogenic nematodes (Nematoda: Rhabditida). Fla Entomol 82: 1-7.
19. Duncan L, Graham J, Zellers J, (2007) Food web responses to augmenting the entomopathogenic nematodes in bare and animal manure-mulched soil. J Nematol 39: 176-189.
20. Schroeder WJ, (1994) Comparison of two steinernematid species for control of the root weevil Diaprepes abbreviatus. J Nematol 26: 360-362.
21. Kaya H, Gaugler R, (1993) Entomopathogenic nematodes. Annu Rev Entomol 38: 181-206.
22. Gaugler R, (2002) Entomopathogenic nematology. New York: CABI. 388 p.
23. Georgis R, Koppenhöfer AM, Lacey LA, Bélair G, Duncan LW, et al. (2006) Successes and failures in the use of parasitic nematodes for pest control. Biol Control 38: 103-123.
24. Turlings TCJ, Ton J, (2006) Exploiting scents of distress: the prospect of manipulating herbivore-induced plant odours to enhance the control of agricultural pests. Curr Opin Plant Biol 9: 421-427.
25. Degenhardt J, Gershenzon J, Baldwin IT, Kessler A, (2003) Attracting friends to feast on foes: engineering terpene emission to make crop plants more attractive to herbivore enemies. Curr Opin Biotech 14: 169-176.
26. Bruce T, (2010) Exploiting plant signals in sustainable agriculture. In: Baluška F, Ninkovic V, editors. editors. Plant communication from an ecological perspective. Springer. pp 215-227.
27. Thaler JS, Stout MJ, Karban R, Duffey SS, (1996) Exogenous jasmonates simulate insect wounding in tomato plants (Lycopersicon esculentum) in the laboratory and field. J Chem Ecol 22: 1767-1781.
28. James D, Grasswitz T, (2005) Synthetic herbivore-induced plant volatiles increase field captures of parasitic wasps. BioControl 50: 871-880.
29. Kaplan I, (2011) Attracting carnivorous arthropods with plant volatiles: The future of biocontrol or playing with fire? Biol Control 60: 77-89.
30. McCoy C, (2000) Entomopathogenic nematodes and other natural enemies as mortality factors for larvae of Diaprepes abbreviatus (Coleoptera: Curculionidae). Biol Control 19: 182-190.
31. El-Borai FE, Campos-Herrera R, Stuart RJ, Duncan LW, (2011) Substrate modulation, group effects and the behavioral responses of entomopathogenic nematodes to nematophagous fungi. J Invertebr Pathol 106: 347-356.
32. Campos-Herrera R, Johnson EG, El-Borai FE, Stuart RJ, Graham JH, et al. (2011) Long-term stability of entomopathogenic nematode spatial patterns in soil as measured by sentinel insects and real-time PCR assays. Ann Appl Biol 158: 55-68.
33. Campos-Herrera R, El-Borai FE, Stuart RJ, Graham JH, Duncan LW, (2011) Entomopathogenic nematodes, phoretic Paenibacillus spp., and the use of real time quantitative PCR to explore soil food webs in Florida citrus groves. J Invertebr Pathol 108: 30-39.
34. Johnson SN, Murray PJ, (2008) Root feeders. Cambridge, MA: CABI. 226 p.
35. van Dam NM, Heil M, (2011) Multitrophic interactions below and above ground: en route to the next level. J Ecol 99: 77-88.
36. van Dam NM, (2009) Belowground herbivory and plant defenses. Annu Rev Ecol Evol Syst 40: 373-391.
37. De Deyn GB, van Ruijven J, Raaijmakers CE, de Ruiter PC, van den Putten WH, (2007) Above- and belowground insect herbivores differentially affect soil nematode communities in species-rich plant communities. Oikos 116: 923-930.
38. Green TR, Ryan CA, (1972) Wound induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science 175: 776-777.
39. Haukioja E, Hakala T, (1975) Herbivore cycles and periodic outbreaks. Formation of a general hypothesis. Rep Kevo Subarctic Res Stat 12: 1-9.
40. Khan ZR, Ampog-Nyarko K, Chilishwa P, Hassanali P, Kimani S, et al. (1997) Intercropping increases parasitism of pests. Nature 388: 631-632.
41. Birkett MA, Campbell CAM, Chamberlain K, Guerrieri E, Kick AJ, et al. (2000) New roles for cis-jasmone as an insect semiochemical and in plant defense. Proc Natl Acad Sci USA 97: 9329-9334.
42. Ockroy M, Turlings TCJ, Edwards P, (2001) Response of natural populations of predators and parasitoids to artificially induced volatile emissions in maize plants (Zea mays L.). Agr Forest Entomol 3: 201-209.
43. Hunter M, (2002) A breath of fresh air: beyond laboratory studies of plant volatile-natural enemy interactions. Agr Forest Entomol 4: 81-86.
44. Torr P, Spiridonov SE, Heritage S, Wilson MJ, (2007) Habitat associations of two entomopathogenic nematodes: a quantitative study using real-time quantitative polymerase chain reactions. J Anim Ecol 76: 238-245.
45. Holeva R, Phillips MS, Neilson R, Brown DJF, Young V, et al. (2006) Real-time PCR detection and quantification of vector trichodorid nematodes and Tobacco rattle virus. Mol Cell Probes 20: 203-211.
46. Kolb S, Knief C, Stubner S, Conrad R, (2003) Quantitative detection of methanotrophs in soil by novel pmoA-targeted real-time PCR assays. Appl Environ Microb 69: 2423-2429.
47. El-Borai F, Brentu C, Duncan LW, (2007) Augmenting entomopathogenic nematodes in soil from a Florida citrus orchard: non-target effects of a trophic cascade. J Nematol 39: 203-210.
48. Koppenhöfer AM, Fuzy EM, (2004) Effect of white grub developmental stage on susceptibility to entomopathogenic nematodes. J Econ Entomol 97: 1842-1849.
49. Denno RF, Gruner DS, Kaplan I, (2008) Potential for entomopathogenic nematodes in biological control: A meta-analytical synthesis and insights from trophic cascade theory. J Nematol 40: 61-72.
50. Hare J, (2011) Ecological role of volatiles produced by plants in response to damage by herbivorous insects. Annu Rev Entomol 56: 161-180.
51. Hallem EA, Dilman AR, Hong AV, Zhang Y, Yano JM, et al. (2011) A sensory code for host seeking in parasitic nematodes. Curr Biol 21: 377-383.
52. Rasmann S, Ali JG, Helder J, van der Putten W, (2012) Ecology and evolution of soil nematode chemotaxis, J Chem Ecol In press.
53. Lapointe SL, Shapiro JPT, (1999) Effect of soil moisture on development of Diaprepes abbreviatus (Coleoptera: Curculionidae). Fla Entomol 82: 291-299.
54. Stover E, Castle W, (2002) Citrus rootstock usage, characteristics, and selection in the Florida Indian River region. HortTechnology 12: 143-147.
55. Kaya HK, Stock SP, (1997) Techniques in insect nematology. In: Lacey, LA, editors. editor. Manual of techniques in insect pathology. London, UK: Academic Press. pp 281-324.
56. Kuzovkina I, Szarka S Héthelyi, É (2009) Composition of essential oil in genetically transformed roots of Ruta graveolens. Russ J Plant Physl 56: 846-851.
57. Kubeczka K, Ullmann I, (1980) Occurrence of 1, 5-dimethylcyclodeca-1, 5, 7-triene (pregeijerene) in Pimpinella species and chemosystematic implications. Biochem Syst Ecol 8: 39-41.
58. Larkin MA, Blackshields G, Brown PN, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
59. Jenkins W, (1964) A rapid centrifugal-flotation technique for separating nematodes from soil. Plant Dis Rep 48: 692.