Interspecific competition among insect parasitoids: Field experiments with whiteflies as hosts in cotton

Ecology

Volumn 83, Issue 3, 2002, Pages 653-668

  Bográn, Carlos E ^a,c   Heinz, Kevin M ^a   Ciomperlik, Matthew A ^b  

^a TEXAS A AND M UNIVERSITY   (United States)

^b UNITED STATES DEPARTMENT OF AGRICULTURE   (United States)

^c TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Autoparasitoid; Biological control; Community composition; Heteronomous hyperparasitoid; Interspecific interactions; Parasitoid; Resource allocation patterns

Indexed keywords

BIOLOGICAL CONTROL; HOST-PARASITOID INTERACTION; INTERSPECIFIC COMPETITION; INTRAGUILD INTERACTION; POPULATION DYNAMICS; RESOURCE USE; WHITEFLY;

ALEYRODIDAE; APHELINIDAE; BEMISIA; BEMISIA ARGENTIFOLII; ENCARSIA; ENCARSIA FORMOSA; ENCARSIA PERGANDIELLA; ERETMOCERUS; ERETMOCERUS MUNDUS; GOSSYPIUM HIRSUTUM; HEMIPTERA; HOMOPTERA; HYMENOPTERA; INSECTA;

EID: 0000313627     PISSN: 00129658     EISSN: None     Source Type: Journal    
DOI: 10.1890/0012-9658(2002)083[0653:ICAIPF]2.0.CO;2     Document Type: Article

References (96)

1. Baur, M. E., and K. V. Yeargan. 1995. Host selection and larval interactions among three primary parasitoids of Plathypena scabra (Lep: Noctuidae). Entomophaga 40:357-366.
2. Bautista, R. C., and E. J. Harris. 1997. Effects of multiparasitism on the parasitization behavior and progeny development of oriental fruit fly parasitoids (Hymenoptera: Braconidae). Journal of Economic Entomology 90:757-764.
3. Bellows, T. S., Jr., and K. Arakawa. 1986. Dynamics of preimaginal populations of Bemisia tabaci (Homoptera: Aleyrodidae) and Eretmocerus sp. (Hymenoptera: Aphelinidae) in southern California cotton. Environmental Entomology 17:483-487.
4. Bográn, C. E. 2000. Interspecific competition among aphelinid parasitoids: population dynamics, community structure and biological control. Dissertation. Texas A&M University, College Station, Texas, USA.
5. Bográn, C. E., J. Obrycki, and R. Cave. 1998. Assessment of biological control of Bemisia tabaci in Honduras. Florida Entomologist 81:284-295
6. Bokonon-Ganta, A. H., J. J. M. van Alphen, and P. Neuenschwander. 1996. Competition between Gyranusoidea tebygi and Anagyrus mangicola, parasitoids of the mango mealybug, Rastrococcus invadens: interspecific host discrimination and larval competition. Entomologia Experimentalis et Applicata 79:179-185.
7. Briggs, C. J. 1993. Competition among parasitoid species on a stage-structured host and its effect on host suppression. The American Naturalist 141:372-397.
8. Caballero, R. 1993. Moscas blancas neotropicales (Homoptera: Aleyrodidae): hospederos, distribucion, enemigos naturales e importancia economica. Pages 10-15 in L. Hilje and O. Arboleda, editors. Las moscas blancas (Homoptera: Aleyrodidae) en America Central y el Caribe. [In Spanish.] Centro Agronomico Tropical de Investigación y Enseñanza. Serie Técnica No. 205. Turrialba, Costa Rica.
9. Connell, J. H. 1983. On the prevalence and relative importance of interspecific competition: evidence from field experiments. The American Naturalist 122:661-696.
10. Daane, K. M., M. S. Barzman, C. E. Kennett, and L. E. Caltagirone. 1991. Parasitoids of black scale in California: establishment of Prococcophagus probus Annecke & Mynhardt and Coccophagus rusti Compere (Hymenoptera: Aphelinidae) in olive orchards. Pan-Pacific Entomologist 67:99-106.
11. De Barro, P. J., P. J. Hart, and R. Morton. 2000. The biology of two Eretmocerus spp. (Haldeman) and three Encarsia spp. Forster and their potential as biological control agents of Bemisia tabaci biotype B. in Australia. Entomologia Experimentalis et Applicata 94:93-102.
12. Doutt, R. L., D. R Annecke, and E. Tremblay. 1976. Biology and host relationships of parasitoids. Pages 143-168 in C. B. Huffaker and P. S. Mesenger, editors. Theory and Practice of Biological Control. Academic Press, New York, New York, USA.
13. Enkegaard, A. 1993. Encarsia formosa parasitizing the poinsettia-strain of the cotton whitefly Bemisia tabaci on poinsettia: bionomics in relation to temperature. Entomologia Experimentalis et Applicata 69:251-261.
14. Evans, E. W. 1991. Intra- vs. interspecific interactions of ladybeetles (Colleoptera: Coccinellidae) attacking aphids. Oecologia 87:401-408.
15. Foltyn, S., and D. Gerling. 1985. The parasitoids of the aleyrodid Bemisia tabaci in Israel: development, host preference and discrimination of the aphelinid wasp Eretmocerus mundus. Entomologia Experimentalis et Applicata 38:255-260.
16. Force, D. C. 1970. Competition among four hymenopterous parasites of an endemic insect host. Annals of the Entomological Society of America 63:1675-1678.
17. Force, D. C. 1974. Ecology of host-parasitoid communities. Science 184:624-632.
18. Gauthier, N., A. Sanon, J. P. Monge, and J. Huignard. 1999. Interspecific relations between two sympatric species of hymenoptera, Dinarmus basalis (Rond) and Eupelmus vuilleti (Crw), ectoparasitoids of the bruchid Callosobruchus maculatus (F). Journal of Insect Behavior 12:399-413.
19. Gerling, D., editor. 1990. Whiteflies: their bionomics, pest status and management. Intercept Ltd., Andover, UK.
20. Gerling, D., T. Orion, and Y. Delarea. 1990. Eretmocerus penetration and immature development: a novel approach to overcome host immunity. Archives of Insect Biochemistry and Physiology 13:247-253.
21. Gill, R. 1992. A review of the sweetpotato whitefly in Southern California. Pan-Pacific Entomologist 68:144-152.
22. Godfray, H. C. J. 1994. Parasitoids: behavioural and evolutionary ecology. Princeton University Press, Princeton, New Jersey, USA.
23. Godfray, H. C. J., and M. Shimada. 1999. Parasitoids as model organisms for ecologists. Researches in Population Ecology 41:3-10.
24. Godfray, H. C. J., and J. K. Waage. 1991. Predictive modeling in biological control: the mango mealybug (Rastrococcus invadens) and its parasitoids. Journal of Applied Ecology 28:434-453.
25. Goolsby, J. A., M. A. Ciomperlik, A. A. Kirk, W. A. Jones, B. C. Legaspi, J. C. Legaspi, R. A. Ruiz, D. C. Vacek, and L. E. Wendel. 2000. Predictive and empirical evaluation for parasitoids of Bemisia tabaci (biotype "B"), based on morphological and molecular systematics. Pages 347-358 in A. D. Austin and M. Dowton, editors. Hymenoptera: evolution, biodiversity, and biological control. CSIRO Publishing, Collingwood, Australia.
26. Goolsby, J. A., M. A. Ciomperlik, B. C. Legaspi, Jr., J. C. Legaspi, and L. E. Wendel. 1998. Laboratory and field evaluation of exotic parasitoids of Bemisia tabaci (Gennadius) (Biotype "B") (Homoptera: Aleyrodidae) in the Lower Rio Grande Valley of Texas. Biological Control 12:127-135.
27. Goolsby, J., J. C. Legaspi, and B. C. Legaspi, Jr. 1996. Quarantine evaluation of exotic parasitoids of the sweet-potato whitefly, Bemisia tabaci (Gennadius). Southwestern Entomologist 21:13-21.
28. Hassell, M. P., and G. C. Varley. 1969. New inductive population model for insect parasites and its bearing on biological control. Nature 223:1133-1136.
29. Hawkins, B. A. 1990. Global patterns of parasitoid assemblage size. Journal of Animal Ecology 59:57-72.
30. Hawkins, B. A., and N. J. Mills. 1996. Variability in parasitoid community structure. Journal of Animal Ecology 65:501-516.
31. Heinz, K. M., and J. M. Nelson. 1996. Interspecific interactions among natural enemies of Bemisia in an inundative biological control program. Biological Control 6:384-393.
32. Heinz, K. M., and M. P. Parrella. 1990. Biological control of insect pests on greenhouse marigolds. Environmental Entomology 19:825-835.
33. Henneberry, T. J., N. C. Toscano, T. M. Perring, and R. M. Faust. 1998. Silverleaf whitefly: national research, action, and technology transfer plan, 1997-2001 (formerly sweetpotato whitefly strain B): first annual review of the second 5-year plan held in Charleston, South Carolina, February 3-5, 1998. U.S. Department of Agriculture, Beltsville, Maryland, USA.
34. Hoddle, M. S., R. G. Van Driesche, and J. P. Sanderson. 1998. Biology and use of the whitefly parasitoid Encarsia formosa. Annual Review of Entomology 43:645-669.
35. Hogarth, W. L., and P. Diamond. 1984. Interspecific competition in larvae between entomophagous parasitoids. The American Naturalist 124:552-560.
36. Holmer, K. M., L. S. Osborne, F. D. Bennett, and R. Yokomi. 1994. Biological control of sweetpotato whitefly in Florida. Pages 101-104 in D. Rosen, F. Bennet, and J. Capinera, editors. Pest management in the subtropics, Biological Control - a Florida Perspective. Intercept, Andover, UK.
37. Huang, C., and A. Sih. 1991. Experimental studies on direct and indirect interactions in a three trophic-level stream system. Oecologia 85:530-536.
38. Hunter, M. S. 1989. Suitability of stages of female Encarsia pergandiella (Hymenoptera: Aphelinidae) for development of conspecific male hyperparasitoids. Entomophaga 34:265-274.
39. Hunter, M. S., and J. B. Woolley. 2001. Evolution and behavioral ecology of heteronomous aphelinid parasitoids. Annual Review of Entomology 46:251-290.
40. Itioka, T., T. Inoue, T. Matsumoto, and N. Ishida. 1997. Biological control by two exotic parasitoids: eight-year population dynamics and life tables of the arrowhead scale. Entomologia Experimentalis et Applicata 85:65-74.
41. Jackson, J. B. C. 1981. Interspecific competition and species' distributions: the ghosts of theories and data past. American Zoologist 21:889-901.
42. Jones, W. A., and S. M. Greenberg. 1999. Host instar suitability of Bemisia argentifolii (Homopetera: Aleyrodidae) for the parasitoid Encarsia pergandiella (Hymenoptera: Aphelinidae). Journal of Agricultural and Urban Entomology 16:49-57.
43. Jones, W. A., S. M. Greenberg, and B. Legaspi Jr. 1999. The effect of varying Bemisia argentifolii and Eretmocerus mundus rations on parasitism. BioControl 44:13-28.
44. Kakehashi, N, Y. Suzuki, and Y. Iwasa. 1984. Niche overlap of parasitoids in host-parasitoid systems: its consequence to single vs. multiple introduction controversy in biological control. Journal of Applied Ecology 21:115-131.
45. Kaneko, S. 1995. Frequent successful multiparasitism by five parasitoids attacking the scale insect Nipponaclerda biwakoensis. Researches in Population Ecology 37:225-228.
46. Krause, S. C., R. W. Fuester, and P. L. Burbutis. 1990. Competitive interactions between Cotesia melanoscelus and Glyapanteles flavicoxis (Hymenoptera Braconidae): implications for biological control of gypsy moth (Lepidoptera: Lymantriidae). Environmental Entomology 19:1543-1546.
47. Lawton, J. J., and M. P. Hassell. 1984. Interspecific competition in insects. Pages 451-485 in C. B. Huffaker and R. L. Rabb, editors. Ecological entomology. John Wiley and Sons, New York, New York, USA.
48. Liu, T. X., and P. Stansly. 1996. Oviposition, development and survivorship of Encarsia pergandiella (Hymenoptera: Aphelinidae) in four instars of Bemisia argentifolii (Homoptera: Aleyrodidae). Annals Entomological Society of America 89:96-102.
49. Luck, R. F., and H. Podoler. 1985. Competitive exclusion of Aphytis lignanensis by A. melinus: potential role of host size. Ecology 66:904-913.
50. MacNaly, R. C. 1983. On assessing the significance of interspecific competition to guild structure. Ecology 64:1646-1652.
51. May, R. M., and M. P. Hassell. 1981. The dynamics of multiparasitoid-host interactions. The American Naturalist 124:552-560.
52. Mills, N. J., and W. M. Getz. 1996. Modelling the biological control of insect pests: a review of host-parasitoid models. Ecological Modelling 92:121-143.
53. Mills, N. J., and A. P. Gutierrez. 1996. Prospective modelling in biological control: an analysis of the dynamics of heteronomous hyperparasitism in a cotton-whitefly-parasitoid system. Journal of Applied Ecology 33:1379-1394.
54. Mound, L., and S. Halsey. 1978. Whitefly of the world, a systemic catalogue of the Aleyrodidae (Homoptera) with host plant and natural enemy data. British Museum (Natural History), John Wiley and Sons Inc., London, UK.
55. Murdoch, W. W., C. Briggs, and R. M. Nisbet. 1996. Competitive displacement and biological control in parasitoids: a model. The American Naturalist 148:807-826.
56. Naranjo, S. E., and H. M. Flint. 1994. Spatial distribution of preimaginal Bemisia tabaci (Homoptera: Aleyrodidae) in cotton and development of fixed precision sequential sampling plans. Environmental Entomology 23:254-266.
57. Nguyen, R., J. R. Brazzel, and C. Poucher. 1983. Population density of the citrus blackfly, Aleurocanthus woglumi Ashby (Homoptera: Aleyrodidae) and its parasites in urban Florida in 1979-1981. Environmental Entomology 12:878-884.
58. Onillon, J. C., P. Maignet, and C. Cocquepot. 1994. Premiers resultats sur l'efficacie d'Encarsia pergandiella (Hymenopt., Aphelinidae) dans le controle de Bemisia tabaci (Homopt. Aleurodidae) en serres de tomate. Pages 71-80 in R. Albajes, editor. Integrated control in protected crops; mediterranean climate. [In French.] International Organization for Biological and Integrated Control of Noxious Animals and Plants, West Palaearctic Regional Section (IOBC/WPRS) Bulletin 17:71-80.
59. Patil, N. G., P. S. Baker, W. Groot, and J. K. Waage. 1994. Competition between Psyllaephagus yaseeni and Tamarixia leucaenae, two parasitoids of the leucaena psyllid (Heteropsylla cubana). International Journal of Pest Management 40:211-215.
60. Peckarsky, B. L. 1991. Mechanisms of intra- and interspecific interference between larval stoneflies. Oecologia 85:521-529.
61. Pedata, P. A., and M. S. Hunter. 1996. Secondary host choice by the autoparasitoid Encarsia pergandiella. Entomologia Experimentalis et Applicata 81:207-214.
62. Perring, T. M., A. Cooper, D. J. Kazmer, C. Shields, and J. Shields. 1991. New strain of sweetpotato whitefly invades California vegetables. California Agriculture 45:10-12.
63. Pijls, J. W. A. M., K. D. Hofker, M. J. Van Staalduinen, and J. J. M. Van Alphen. 1995. Interspecific host discrimination and competition in Apoanagyrus (Epidinocarsis) lopezi and A. (E.) diversicornis, parasitoids of the cassava mealybug Phenacoccus manihoti. Ecological Entomology 20:326-332.
64. Pijls, J. W. A. M., L. M. Poleij, J. J. M van Alphen, and E. Meelis. 1996. Interspecific interference between Apoanagyrus lopezi and A. diversicornis, parasitoids of the cassava mealybug Phenacoccus manihoti. Entomologia Experimentalis et Applicata 78:221-230.
65. Polaszek, A., G. A. Evans, and F. D. Bennett. 1992. Encarsia parasitoids of Bemisia tabaci (Hymenoptera: Aphelinidae, Homoptera: Aleyrodidae): a preliminary guide to identification. Bulletin of Entomological Research 82:375-392.
66. Polis, G. A. 1991. Complex trophic interactions in deserts: an empirical critique of food-web theory. The American Naturalist 138:123-155.
67. Polis, G. A., and D. R. Strong. 1996. Food web complexity and community dynamics. The American Naturalist 147:813-846.
68. Powell, D. A., and T. S. Bellows, Jr. 1992. Development and reproduction of two populations of Eretmocerus species (Hymenoptera: Aphelinidae) on Bemisia tabaci (Homoptera: Aleyrodidae). Environmental Entomology 21:651-658.
69. Price, P. W. 1971. Niche breath and dominance of parasitic insects sharing the same host species. Ecology 52:587-596.
70. Reeve, J. D., and W. W. Murdoch. 1986. Biological control by the parasitoid Aphytis melinus, and population stability of the California red scale. Journal of Animal Ecology 55:1069-1082.
71. Reitz, S. R. 1996. Interspecific competition between two parasitoids of Helicocoverpa zea: Eucelatoria bryani and E. rubentis. Entomologia Experimentalis et Applicata 79:227-234.
72. Riley, D. G., and M. A. Ciomperlik. 1997. Regional population dynamics of whitefly (Homopetera: Aleyrodidae) and associated parasitoids (Hymenoptera: Aphelinidae). Environmental Entomology 26:1049-1055.
73. Rose, M., and P. DeBach. 1981. Citrus whitefly parasites established in California. California Agriculture 36(7 and 8):21-23.
74. Rosenheim, J. A., H. K. Kaya, L. E. Ehler, J. J. Marois, and B. A. Jafee. 1995. Intraguild predation among biological control agents: theory and evidence. Biological Control 5:303-335.
75. Rosenheim, J. A., L. R. Wilhoit, and C. A. Armer. 1993. Influence of intraguild predation among generalist insect predators on the suppression of an herbivore population. Oecologia 96:439-449.
76. SAS Institute. 1999. SAS Version 8.0. SAS Institute, Cary, North Carolina, USA.
77. Schoener, T. W. 1983. Field experiments on interspecific competition. The American Naturalist 122:240-285.
78. Schuster D. J., and J. F. Price. 1996. Parasitization of Bemisia argentifolii (Hom.: Aleyrodidae) by Encarsia pergandiella (Hym.: Aphelinidae). Entomophaga 41:95-103.
79. Shimada, M. 1985. Niche modification and stability of competitive systems. II: persistence of interspecific competitive systems with parasitoid wasps. Researches on Population Ecology 27:203-216.
80. Shimada, M. 1999. Population fluctuation and persistence of one-host-two-parasitoid systems depending on resource distribution: from parasitizing behavior to population dynamics. Researches on Population Ecology 41:69-79.
81. Sih, A., G. Englund, and D. Wooster. 1998. Emergent impacts of multiple predators on prey. Trends in Ecology and Evolution 13:350-355.
82. Sokal, R. R., and F. J. Rohlf. 1995. Biometry: the principles and practice of statistics in biological research. Third edition. W. H. Freeman and Company, New York, New York, USA.
83. Soluk, D. A., and N. C. Collins. 1988. Synergistic interactions between fish and stoneflies: facilitation and interference among stream predators. Oikos 52:94-100.
84. Takasu, K., Y. Hirose, and M. Takagi. 1998. Occasional interspecific competition and within-plant microhabitat preference in egg parasitoids of the bean bug, Riptortus clavatus (Hemiptera: Alydidae) in soybean. Applied Ehtomology and Zoology 33:391-399.
85. Thompson, C. R., J. A. Cornell, and R. I. Sailer. 1987. Interactions of parasites and a hyperparasite in biological control of citrus blackfly, Aleurocanthus woglumi (Homoptera: Aleyrodidae), in Florida. Environmental Entomology 15:140-144.
86. van Alebeek, F. A. N., D. Rojas-Rousse, and L. Leveque. 1993. Interspecific competition between Eupelmus vuilleti and Dinarmus basalis, two solitary ectoparasitoids of Bruchidae larvae and pupae. Entomologia Experimentalis et Applicata. 69:21-31.
87. van den Berg, M. A., G. Hoeppner, and J. Greenland. 2000. An economic study of the biological control of the Spiny Blackfly, Aleurocanthus spiniferus (Hemiptera: Aleyrodidae), in a citrus orchard in Swaziland. Biocontrol Science and Technology 10:27-32.
88. Van Lenteren, J. C., Y. C. Drost, H. J. W. Van Roermund. and C. J. A. M. Posthuma-Doodeman. 1997. Aphelinid parasitoids as sustainable biological control agents in greenhouses. Journal of Applied Entomology 121:473-485.
89. Vargas, R. I. J., J. D. Stark, G. K. Uchida, and M. Purcell. 1993. Opiine parasitoids (Hymenoptera: Braconidae) of oriental fruit fly (Diptera: Tephritidae) on Kauai island, Hawaii: islandwide relative abundance and parasitism rates in wild and orchard guava habitats. Environmental Entomology 22:246-253.
90. Viggiani, G. 1984. Bionomics of the Aphelinidae. Annual Review of Entomology 29:257-276.
91. Walter, G. H. 1983. "Divergent male ontogenies" in Aphelinidae (Hymenoptera: Chalcidoidea): a simplified classification and a suggested evolutionary sequence. Biological Journal of the Linnean Society 46:261-282.
92. Walter, G. H., and H. E. H. Paterson. 1995. Levels of understanding in ecology; interspecific competition and community ecology. Australian Journal of Ecology 20:463-466.
93. Williams, T. 1996. Invasion and displacement of experimental populations of a conventional parasitoid by a heteronomous hyperparasitoid. Biocontrol Science and Technology 6:606-618.
94. Wissinger, S., and J. McGrady. 1993. Intraguild predation and competition between larval dragonflies: direct and indirect effects on shared prey. Ecology 74:207-218.
95. Yu, D. S., R. F. Luck, and W. W. Murdoch. 1990. Competition, resource partitioning and coexistence of an endoparasitoid Encarsia perniciosi and an ectoparasitoid Aphytis melinus of the California red scale. Ecological Entomology 15:469-480.
96. Zolnerowich, G., and M. Rose. 1998. Eretmocerus Halldeman (Hymenoptera: Aphelinidae) imported and released in the United States for control of Bemisia (tabaci complex) (Homoptera: Aleyrodidae) Bulletin of the Entomological Society of Washington 100:310-323.