Prospective modelling in biological control: An analysis of the dynamics of heteronomous hyperparasitism in a cotton-whitefly-parasitoid system

Journal of Applied Ecology

Volumn 33, Issue 6, 1996, Pages 1379-1394

  Mills, N J ^a   Gutierrez, A P ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

autoparasitism; Bemisia; Encarsia; Eretmocerus; tritrophic population model

Indexed keywords

BIOLOGICAL CONTROL; COTTON; PARASITOID; TRITROPHIC MODEL; WHITEFLY;

ALEYRODIDAE; APHELINIDAE; GOSSYPIUM HIRSUTUM; HEMIPTERA; HIRSUTUM; MAGNOLIOPHYTA; MALVACEAE;

EID: 0030302621     PISSN: 00218901     EISSN: None     Source Type: Journal    
DOI: 10.2307/2404778     Document Type: Article

References (83)

1. Abdel-Fattah, M.I., Hendi, A., Kolaib, M.O. & El-Said. A. (1984) Studies on Prospaltella lutea Masi, a primary parasite of the cotton whitefly. Bemisia tabaci (Genn.) in Egypt. Bulletin de la Sociéte Entomologique d'Egypte, 65, 119-129.
2. Artigues, M., Avilla, J , Sarasúa, M.J. & Albajes, R. (1992) Egg allocation and host stage preference at constant temperatures in Encarsia tricolor. Entomophaga, 36, 107-116.
3. Avilla, J., Anadón, J., Sarasúa, M.J. & Albajes, R. (1992) Egg allocation of the autoparasitoid Encarsia tricolor at different relative densities of primary host (Trialeurodes vapotartorum) and two secondary hosts (Encarsia formosa and E. tricolor). Entomologia Experimentalis et Applicata, 59, 219-227.
4. Avilla, J & Copland, M.J.W. (1987) Effects of host stage on the development of the facultative autoparasitoid Encarsia tricolor (Hymenoptera: Aphelinidae). Annals of Applied Biology, 110, 381-389.
5. Beddington, J.R. & Hammond, P.S. (1977) On the dynamics of host-parasite-hyperparasite interactions. Journal of Animal Ecology, 46, 811-821.
6. Bennett, F.D. (1981) Hyperparasitism in the practice of biological control. The Role of Hyperparasitism in Biological Control: A Symposium (ed. D. Rosen), pp. 43-49, Division of Agricultural Sciences, University of California.
7. Butler, G.D., Henneberry, T.J. & Clayton, T.E. (1983) Bemisia tabaci (Homoptera: Aleyrodidae): development, oviposition and longevity in relation to temperature. Annals of the Entomological Society of America, 76, 310-313.
8. Clausen, C.P. (1978) Introduced Parasites and Predators of Arthropod Pests and Weeds: a world review. USDA Handbook No. 480 USDA, Washington D.C.
9. Coulson, J.R. & Soper, R.S. (1989) Protocols for the introduction of biological control agents in the US. Plant Protection and Quarantine, Vol. 3 (ed. R. P. Kahn), pp 1-35. CRC Press, Baton Rouge, USA.
10. Coulson, J.R., Soper, R.S. & Williams, D.W. (1991) Biological control quarantine: needs and procedures. Appendix III. Proposed ARS Guidelines for Introduction and Release of Exotic Organisms for Biological Control, USDA ARS-99. USDA, Washington D.C.
11. DeBach, P. (1964) Successes, trends, and future possibilities. Biological Control of Insect Pests and Weeds (ed. P. DeBach), pp. 673-713. Reinhold Publishing, New York.
12. DeBach, P. & Rosen, D. (1991) Biological Control by Natural Enemies, 2nd edn. Cambridge University Press, Cambridge.
13. Donaldson, J.S. & Walter, G.H. (1991) Host population structure affects field sex ratios of the heteronomous hyperparasitoid, Coccophagus atratus. Ecological Entomology, 16, 35-44.
14. Doutt, R.L. & DeBach, P. (1964) Some biological control concepts and questions. Biological Control of Insect Pests and Weeds (ed. P. DeBach), pp. 118-167. Reinhold Publishing, New York.
15. Dowell, R.V., Puckett, D. & Johnson, M. (1981) Searching and ovipositional behavior of Amitus hesperidum [Hym.: Platygasteridae] and Encarsia opulenta [Hym., Aphelinidae] parasitoids of the citrus blackfly [Hom., Aleyrodidae]. Entomophaga, 26, 233-239.
16. Ehler, L.E. (1979) Utility of facultative secondary parasites in biological control. Environmental Entomology, 8, 829-832.
17. El-Helaly, M., El-Shazli, A.Y. & El-Gayar, F.H. (1971) Biological studies on Bemisia tabaci (Genn.) (Homoptera: Aleyrodidae) in Egypt Zeitschrift für Angewandte Entomologie, 69, 48-55.
18. Flanders, S.E. (1943) Indirect hyperparasitism and observations on three species of indirect hyperparasites. Journal of Economic Entomology, 36, 921-926.
19. Flanders, S.E. (1969) Herbert Smith's observations on citrus blackfly parasites in India and Mexico and the correlated circumstances. Canadian Entomologist, 101, 467-480.
20. Foltyn, S. & Gerling, D (1985) The parasitoids of the aleyrodid Bemista tabaci in Israel. Development, host preference and discrimination of the aphelinid Eretmocerus mundus. Entomologia Experimentalis et Applicata, 38, 255-260.
21. Gerling, D. (1966a) Studies on whitefly parasitoids of southern California. I. Encarsia pergandiella Howard (Hym.: Aphelinidae). Canadian Entomologist, 98, 707-724.
22. Gerling, D. (1966b) Studies on whitefly parasitoids of southern California II. Eretmocerus californicus Howard (Hym.: Aphelinidae). Canadian Entomologist, 98, 1316-1329.
23. Gerling, D. (1992) Natural enemies of whiteflies, predators and parasitoids Whiteflies. Their Bionomics, Pest Status and Management (ed. D. Gerling), pp. 147-185. Intercept, Andover.
24. Gerling, D. & Foltyn, S (1987) Development and host preference of Encarsia lutea (Mast) and interspecific host discrimination with Eretmocerus mundus (Mercet) (Hymenoptera: Aphelimdae) parasitoids of Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae). Journal of Applied Entomology, 103, 425-433.
25. Godfray, H.C.J. & Waage, J.K. (1990) The evolution of highly skewed sex ratios in aphelinid wasps. American Naturalist, 136, 715-721.
26. Godfray, H.C.J. & Waage, J.K. (1991) Predictive modelling in biological control: the mango mealy bug (Rastrococcus invadens) and its parasitoids. Journal of Applied Ecology, 28, 434-453.
27. Gould, J.R., Bellows, T.S & Paine, T.D. (1992) Population dynamics of Siphoninus phillyreae in California in the presence and absence of a parasitoid, Encarsia partenopea. Ecological Entomology, 17, 127-134.
28. Greathead, D.J. (1986) Parasitoids in classical biological control. Insect Parasitoids (eds J. Waage & D. Greathead), pp. 289-317. Academic Press, London.
29. Greathead, D.J. (1989) Biological control as an introduction phenomenon: a preliminary examination of programs against Homoptera. Entomologist, 108, 28-37.
30. Greathead, D.J. & Greathead, A. (1992) Biological control of insect pests by insect parasitoids and predators: the BIOCAT database. Biocontrol News and Information, 13, 61N-68N.
31. Gutierrez, A.P. & Baumgärtner, J.U. (1984) Multitrophic level models of predator-prey energetics. I. Age-specific energetics models - pea aphid Acyrthosiphon pisum (Harris) (Homoptera: Aphididae) as an example. Canadian Entomologist, 116, 924-932.
32. Gutierrez, A.P., Baumgärtner, J.U. & Hagen, K.S. (1981) A conceptual model for growth, development and reproduction in the ladybird beetle Hippodamia convergens G.-M. (Coccinellidae: Coleoptera). Canadian Entomologist, 113, 21-33.
33. Gutierrez, A P , Dos Santos, W.J., Villacorta, A.M., Pizzamiglio, M A., Ellis, C K., Carvalho, L.H. & Stone, N.D. (1991) Modelling the interaction of cotton and the cotton boll weevil. I. Cotton growth and development: a comparison of growth and development of varieties. Journal of Applied Ecology, 28, 371-397.
34. Gutierrez, A.P., Falcon, L.A., Loew, W., Leipiz, P.A. & van den Bosch, R. (1975) An analysis of cotton production in California: a model for Acala cotton and the effects of defoliators on its yield. Environmental Entomology, 4, 125-136.
35. Gutierrez, A P., Hagen, K. S. & Ellis, C.K. (1990) Evaluating the impact of natural enemies: a multitrophic perspective. Critical Issues in Biological Control (eds M. Mackauer, L. E. Ehler & J. Roland), pp. 81-109. Intercept. Andover, England.
36. Gutierrez, A P., Mills, N.J., Schreiber, S.J. & Ellis, C.K. (1994) A physiological perspective on bottom up-top down regulation of populations. Ecology, 75, 2227-2242.
37. Gutierrez, A.P., Neuenschwander, P. & van Alphen, J.J.M (1993) Factors affecting biological control of cassava mealybug by exotic parasitoids: a ratio-dependent supply demand driven model. Journal of Applied Ecology, 30, 706-721.
38. Gutierrez, A.P., Neuenschwander, P., Schultess, F., Herren, H.R., Baumgartner, J.U. Wermelinger, B., Löhr, B. & Ellis, C.K (1988) Analysis of the biological control of cassava pests in Africa. II. Cassava mealybug Phenacoccus manthott. Journal of Applied Ecology, 25, 921-940.
39. Hall, R.W., Ehler., L.E. & Bisabri-Ershadt, B. (1980) Rate of success in classical biological control of arthropods Bulletin of the Entomological Society of America, 26, 111-114.
40. Hassell, M.P., Waage, J.K. & May, R.M. (1983) Variable parasitoid sex ratios and their effect on host-parasitoid dynamics. Journal of Animal Ecology, 52, 889-904.
41. Hokkanen, H.M.T. (1985) Success in classical biological control. CRC Critical Reciews in Plant Sciences, 3, 35-72.
42. Hudson, W.G. & Williams, M.L. (1986) Release of the parasitic wasp, Encarsia lahorensis (Hymenoptera: Aphelinidae), for control of citrus whitefly (Homoptera: Aleyrodidae) on gardenia in Alabama. Environmental Entomology, 15, 585-589.
43. Hunter, M.D. & Price, P.W. (1992) Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology, 73. 724-732.
44. Hunter, M.S. (1989a) Suitability of stages of female Encarsia pergandiella (Hymenoptera: Aphelinidae) for development of conspecific male hyperparasites. Entomophaga, 34, 265-274.
45. Hunter, M.S. (1989b) Sex allocation and egg distribution of an autoparasitoid, Encarsia pergandiella (Hymenoptera: Aphelinidae). Ecological Entomology, 14, 57-67.
46. Hunter, M.S. (1993) Sex allocation in a field population of an autoparasitoid. Oecologia, 93, 421-428.
47. Kennett, C.E., Huffaker, C.B. & Finney, G.L. (1966) The role of an autoparasitic aphelinid. Coccophagoides utilis Doutt, in the control of Parlatoria oleae (Colvee). Hilgardia, 37, 255-282.
48. Kidd, N.A.C. & Jervis, M.A (1989) The effects of host-feeding behaviour on the dynamics of parasitoid-host interactions, and the implications for biological control. Researches in Population Ecology, 31, 235-274.
49. Lenteren, J.C. van & Woets, J. (1988) Biological and integrated pest control in greenhouses. Annual Review of Entomology, 33, 239-270.
50. Luck, R.F., Messenger, P.S. & Barbieri, J. (1981) The influence of hyperparasitism on the performance of biological control agents. The Role of Hyperparasitism in Biological Control. A Symposium (ed D. Rosen), pp. 34-42. Division of Agricultural Sciences, University of California, USA.
51. May, R.M. & Hassell, M.P. (1981) The dynamics of multiparasitoid-host interactions. American Naturalist, 117, 234-261.
52. May, R.M. & Hassell, M.P. (1988) Population dynamics and biological control. Philosophical Transactions of the Royal Society of London, Series B, 318, 129-169.
53. Mills, N.J (1994) Biological control: some emerging trends. Individuals, Populations and Patterns in Ecology (eds S. Leather, A. D. Watt, N. J. Mills & K. E. F. Walters), pp. 213-222. Intercept, Andover.
54. Munroe, E.G. (1971) Status and potential of biological control in Canada. Technical Communication of the Commonwealth Institute of Biological Control. 4, 213-255.
55. Murdoch, W.W. (1990) The relevance of pest-enemy models to biological control Critical Issues in Biological Control (eds M. Mackauer, L. E Ehler & J. Roland), pp. 1-24. Intercept. Andover.
56. Nguyen, R., Brazzel, J.R & Poucher, C. (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.
57. Nguyen, R. & Sailer, R.I. (1987) Facultative hyperparasitism and sex determination of Encarsia smithi (Silvestri) (Hymenoptera: Aphelinidae). Annals of the Entomological Society of America, 80, 713-719.
58. Powell, D.A & Bellows, T S. (1992a) Preimaginal development and survival of Bemista tabaci on cotton and cucumber. Environmental Entomology, 21, 359-363.
59. Powell, D.A. & Bellows, T.S. (1992b) Adult longevity, fertility and population growth rates for Bemisia tabaci on two host plant species Journal of Applied Entomology, 113, 68-78.
60. Powell, D.A. & Bellows, T.S (1992c) Development and reproduction of two populations of Eretmoterus species (Hymenoptera: Aphelinidae) on Bemista tabaci (Homoptera: Aleyrodidae). Environmental Entomology, 21, 651-658.
61. Price, P.W. (1992) Plant resources as the mechanistic basis for insect herbivore population dynamics. Effects of Resource Distribution on Animal-Plant Interactions (eds M. D. Hunter, T. Ohgushi & P. W. Price), pp. 139-173. Academic Press, San Diego, USA.
62. Rao, V.P., Ghani, M.A., Sankaran, T. & Mathur, K.C. (1971) A review of the biological control of insect and other pests in South-East Asia and the Pacific Region. Technical Communication of the Commonwealth Institute of Biological Control, 6, 7-8.
63. Rose, M. & DeBach, P. (1992) Biological control of Parabemista myricae (Kuwana) (Homoptera: Aleyrodidae) in California. Israel Journal of Entomology, 26, 73-95.
64. Rosen, D. & DeBach, P. (1990) The natural enemies, ectoparasites. Armored Scale Insects their Biology, Natural Enemies and Control. Part B (ed. D. Rosen), pp. 99-120 Elsevier, Amsterdam, Holland.
65. Royama, T. (1971) A comparative study of models for predation and parasitism. Researches in Population Ecology, Supplement, 1, 1-91.
66. Sevenni, M., Baumgärtner, J.U. & Ricca, M. (1990) Theory and practice of parameter estimation of distributed delay-models for insect and plant phenologies. Meteorology and Environmental Sciences (eds R. Guzzi, A. Navarra & J. Shukla), pp. 674-719. World Scientific and International Publishers, Singapore.
67. Sharaf, N.S. & Batta, Y. (1985) Effect of some factors on the relationship between the whitefly Bemisia tabaci Genn. (Homoptera Aleyrodidae) and the parasitoid Ereimocerus mundus Mercet (Hymenoptera. Aphelinidae). Zeitschrift für Angewandte Entomologie, 99, 267-276.
68. Smith, H.S. (1916) An attempt to redefine the host relationships exhibited by entomophagous insects Journal of Economic Entomology, 9, 477-486.
69. Smith, H D., Maltby, H.L. & Jimenez, E.J. (1964) Biological control of the citrus blackfly m Mexico. USDA Technical Bulletin, 1311, 1-30.
70. Tawfik, M F.S., Awadallah, K.T , Hafez, M. & Sarhan, A.A. (1978) Biology of the aphelinid parasite Eretmocerus mundus Mercet Bulletin de la Sociéte Entomologique d'Egypte, 62, 33-18.
71. Thompson, C.R., Cornell, J.A. & Sailer, R.I. (1987) Interactions of parasites and a hyperparasite in biological control of citrus blackfly, Aleurocanthus woglumi (Homoptera: Aleyrodidae), in Florida. Environmental Entomology, 16, 140-144.
72. Vet, L.M. & Lenteren, J C. van (1981) The parasite-host relationship between Encarsia formosa Gah. (Hymenoptera: Aphelinidae) and Trialeurodes vaporartorum (Westw.) (Homoptera: Aleyrodidae). X. A comparison of three Encarsia spp. and one Ereimocerus sp. to estimate their potentialities in controlling whitefly on tomatoes in greenhouses with a low temperature regime. Zeitschrift für Angewandte Entomologie, 91, 327-348.
73. Viggiani, G. (1981) Hyperparasitism and sex differentiation m the Aphelinidae. The Role of Hyperparasitism in Biological Control, a Symposium (ed. D. Rosen), pp. 19-26. Division of Agricultural Sciences, University of California, USA.
74. Viggiani, G. (1984) Bionomics of the Aphelinidae. Annual Review of Entomology, 29, 257-276.
75. Viggiani, G. (1990) The natural enemies, endoparasites, Aphelinidae. Armored Scale Insects their Biology, Natural Enemies and Control, Part B (ed D Rosen), pp. 121-132. Elsevier, Amsterdam, Holland.
76. Viggiani, G. (1994) Recent cases of interspecific competition between parasitoids of the family Aphelinidae (Hymenoptera: Chalcidoidea). Norwegian Journal of Agricultural Sciences Supplement, 16, 353-359.
77. Von Arx, R., Baumgärtner, J. & Delucchi, V. (1983) Developmental biology of Bemisia tabaci (Genn.) (Sternorryncha, Aleyrodidae) on cotton at constant temperatures. Bulletin de la Societe Entomologique de la Suisse, 56, 389-399.
78. Waage, J.K. (1990) Ecological theory and the selection of biological control agents. Critical Issues in Biological Control (eds M. Mackauer, L. E Ehler & J. Roland), pp. 135-157. Intercept, Andover.
79. Waage, J.K. & Mills, N.J. (1992) Biological control. Natural Enemies: The Population Biology of Predators, Parasites and Diseases (ed. M. J. Crawley), pp. 412-430. Blackwell, Oxford.
80. 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, 19, 63-82.
81. Waterhouse, D F. & Norris, K.R. (1987) Biological Control Pacific Prospects. Inkata Press, Melbourne.
82. Williams, J.R. (1977) Some features of sex-linked hyperparasitism in Aphelinidae (Hymenoptera) Entomophaga, 22, 345-350.
83. Williams, T. (1991) Host selection and sex ratio in a heteronomous hyperparasitoid. Ecological Entomology, 16, 377-386.