99
Views
0
CrossRef citations to date
0
Altmetric
Research Articles

Effect of Bemisia tabaci SSA1 host density and cassava genotype on host feeding capacity and parasitism by two Hymenoptera parasitoid species

ORCID Icon, ORCID Icon, ORCID Icon, , ORCID Icon & ORCID Icon
Pages 19-34 | Received 19 Aug 2022, Accepted 21 Nov 2022, Published online: 01 Dec 2022

References

  • Abate, T., van Huis, A., & Ampofo, J. (2000). Pest management strategies in traditional agriculture: An African perspective. Annual Review of Entomology, 45(1), 631–659.
  • Agounké, D., Fischer, H. U., & Moore, D. (1989). The control of Rastrococcus invadens Williams (Hemiptera: Pseudococcidae) in Togo by the introduction of Gyranusoidea tebygi Noyes (Hymenoptera: Encyrtidae). Bulletin of Entomological Research, 79(4), 671–678. https://doi.org/10.1017/S0007485300018824
  • Alene, A. D., Neuenschwander, P., Manyong, V. M., Coulibaly, O., & Hanna, R. (2005). The impact of IITA-led biological control of major pest in sub-Saharan African agriculture: A synthesis of milestones and empirical results. In CGIAR Standing Panel on Impact Assessment (p. 31). https://ispc.cgiar.org/sites/default/files/pdf/5.impact_major-pest.pdf%0Ahttp://books.google.com/books?id=glAbg4KWaJsC&pgis=1
  • Alicai, T., Omongo, C. A., Maruthi, M. N., Hillocks, R. J., Baguma, Y., Kawuki, R., Bua, A., Otim-Nape, G. W., & Colvin, J. (2007). Re-emergence of cassava brown streak disease in Uganda. Plant Disease, 91(1), 24–29. https://doi.org/10.1094/PD-91-0024
  • Al-Zyoud, F. (2012). The ladybird predator Serangium parcesetosum Sicard (Coleoptera: Coccinellidae): Current status and future perspectives. Journal of Biological Control, 26(4), 297–313. http://journalofbiologicalcontrol.com
  • Al-Zyoud, F., Sengonca, C., & An-Abbadi, S. (2007). Evaluation of Serangium parcesetosum (Col.: Coccinellidae) for biological control of Bemisia tabaci under greenhouse conditions. Journal of Pest Science, 80(2), 85–92. https://doi.org/10.1007/s10340-006-0156-3
  • Arnó, J., Gabarra, R., Liu, T. X., Simmons, A. M., & Gerling, D. (2010). Natural enemies of Bemisia tabaci: Predators and parasitoids. In S. Stansly & P. A. Naranjo (Eds.), Bemisia: Bionomics and management of a global pest (pp. 385–421). Springer. https://doi.org/10.1007/978-90-481-2460-2
  • Asiimwe, P., Ecaat, J. S., Otim, M., Gerling, D., Kyamanywa, S., & Legg, J. P. (2007). Life-table analysis of mortality factors affecting populations of Bemisia tabaci on cassava in Uganda. Entomologia Experimentalis et Applicata, 122(1), 37–44. https://doi.org/10.1111/j.1570-7458.2006.00487.x
  • Bai, B., & Mackauer, M. (1990). Oviposition and host-feeding patterns in Aphelinus asychis (Hymenoptera: Aphelinidae) at different aphid densities. Ecological Entomology, 15(1), 9–16. https://doi.org/10.1111/j.1365-2311.1990.tb00778.x
  • Binu, A., Palaniswami, M. S., & Hennebery, T. (2003). Encarsia transvena (Hymenoptera: Aphelinidae) development on different Bemisia tabaci Gennadius (Homoptera: Aleyrodidae) instars. Environmental Entomology, 32(3), 584–591.
  • Blagbrough, I. S., Bayoumi, S. A. L., Rowan, M. G., & Beeching, J. R. (2010). Phytochemistry Cassava : An appraisal of its phytochemistry and its biotechnological prospects. Phytochemistry, 71(17–18), 1940–1951. https://doi.org/10.1016/j.phytochem.2010.09.001
  • Brown, J. K., Frohlich, D. R., & Rosell, R. (1995). The sweetpotato or silverleaf whiteflies: Biotypes of Bemisia tabaci or species complex? Annual Review of Entomology, 40(1), 511–534. https://doi.org/10.1146/annurev.en.40.010195.002455
  • Burger, J. M. S., Hemerik, L., van Lenteren, J. C., & Vet, L. E. M. (2004). Reproduction now or later: Optimal host-handling strategies in the whitefly parasitoid Encarsia formosa. Oikos, 106(1), 117–130. https://doi.org/10.1111/j.0030-1299.2004.12908.x
  • Burns, A., Gleadow, R., Cliff, J., Zacarias, A., & Cavagnaro, T. (2010). Cassava: The drought, war and famine crop in a changing world. Sustainability, 2(11), 3572–3607. https://doi.org/10.3390/su2113572
  • Dittrich, V., Hassan, S., & Ernst, G. (1985). Sudanese cotton and the whitefly: A case study of the emergence of a new primary pest. Crop Protection, 4(2), 161–176. https://doi.org/10.1016/0261-2194(85)90015-8
  • FAO. (2015). Cassava diseases in Africa: A major threat to food security. Strategic Programme Framework 2010-2015.
  • Felipe de Mendiburu. (2017). Agricolae: Statistical procedures for agricultural research. R package version 1.2-8. https://CRAN.R-project.org/package=agricolae.
  • Gerling, D. (1996). Status of Bemisia tabaci in the Mediterranean countries: Opportunities for biological control. Biological Control, 6(1), 11–22. https://doi.org/10.1006/bcon.1996.0002
  • Gerling, D., Alomar, O., & Arno, J. (2001). Biological control of Bemisia tabaci using predators and parasitoids. Crop Protection, 20(9), 779–799. https://doi.org/10.1016/S0261-2194(01)00111-9
  • Ghahari, H., Huang, J., & Wang, Z. H. (2005). Biology of a thelyotokous biotype of Eretmocerus mundus (Hymenoptera : Aphelinidae) on Bemisia tabaci (Homoptera: Aleyrodidae). Insect Science, 12(6), 461–465. https://doi.org/10.1111/j.1744-7917.2005.00058.x
  • Giorgini, M., & Baldanza, F. (2004). Species status of two populations of Encarsia sophia (Girault & Dodd) (Hymenoptera: Aphelinidae) native to different geographic areas. Biological Control, 30(1), 25–35. https://doi.org/10.1016/j.biocontrol.2003.09.013
  • Guastella, D., Lulah, H., Tajebe, L. S., Cavalieri, V., Evans, G. A., Pedata, P. A., Rapisarda, C., & Legg, J. P. (2015). Survey on whiteflies and their parasitoids in cassava mosaic pandemic areas of Tanzania using morphological and molecular techniques. Pest Management Science, 71(3), 383–394. https://doi.org/10.1002/ps.3810
  • Hanan, A., He, X. Z., & Wang, Q. (2012). Host feeding and oviposition strategy of Eretmocerus warrae (Aphelinidae: Hymenoptera) under different host densities. New Zealand Plant Protection, 65, 133–137. https://doi.org/10.30843/nzpp.2012.65.5382
  • Harbaugh, B., & Mattson, R. (1976). Interaction of the greenhouse whitefly, Trialeurodes vaporariorum westwood, and its parasite, Encarsia formosa Gahan, on tomato cultivars. HortScience, 11(3), 218–219. https://doi.org/10.21273/HORTSCI.11.3.218
  • Heimpel, G., & Collier, T. (1996). The evolution of host-feeding behaviour in insect parasitoids. Biological Reviews, 71(3), 373–400. https://doi.org/10.1111/j.1469-185X.1996.tb01279.x
  • Heinz, K., & Parrella, M. (1994). Poinsettia (Euphorbia pulcherrima Willd. Ex Koltz) cultivar-mediated differences in performance offive natural enemies of Bemisia argentifolii Bellows and Perring, n. Sp. (Homoptera: Aleyrodidae). Biological Control, 4(4), 305–318. https://doi.org/10.1006/bcon.1994.1039
  • Herren, H., & Neuenschwander, P. (1991). Biological control of cassava pests in Africa. Annual Review of Entomology, 36(1), 257–283. https://doi.org/10.1146/annurev.en.36.010191.001353
  • Hoddle, M., Van Driesche, R., & Sanderson, J. (1998). Biology and use of the whitefly parasitoid Encarsia formosa. Annual Review of Entomology, 43(1), 645–669. https://doi.org/10.1146/annurev.ento.43.1.645
  • Horowitz, A. R., Antignus, Y., & Gerling, D. (2011). Management of Bemisia tabaci whiteflies. In W. Thompson (Ed.), The Whitefly, Bemisia tabaci (Homoptera: Aleyrodidae) interaction with geminivirus-infected host plants (pp. 293–322). Springer. https://doi.org/10.1007/978-94-007-1524-0
  • Horowitz, A. R., & Ishaaya, I. (1996). Chemical control of Bemisia – management and application. In D. Gerling & R. Mayer (Eds.), Bemisia: 1995: Taxonomy, biology, damage, control and management (pp. 537–556). Intercept LTD., Andover, Hunts, UK.
  • Hulspas-Jordan, P., & Van-Lenteren, J. (1978). The relationship between host plant leaf structure and parasitization efficiency of the parasitic wasp Encarsia formosa Gahan (Hymenoptera: Aphelinidae). Mededelingen van de Faculteit Landbouwwetenschappen, Rijksuniversiteit Gent, 43(1), 431–440.
  • Jarvis, A., Ramirez-Villegas, J., Campo, B. V. H., & Navarro-Racines, C. (2012). Is cassava the answer to African climate change adaptation? Tropical Plant Biology, 5(1), 9–29. https://doi.org/10.1007/s12042-012-9096-7
  • Jervis, M., & Kidd, N. (1986). Host-feeding strategies in hymenopteran parasitoids. Biological Reviews, 61(4), 395–434. https://doi.org/10.1111/j.1469-185X.1986.tb00660.x
  • Karut, K., & Naranjo, S. E. (2009). Mortality factors affecting Bemisia tabaci populations on cotton in Turkey. Journal of Applied Entomology, 133(5), 367–374. https://doi.org/10.1111/j.1439-0418.2008.01369.x
  • Katono, K., Macfadyen, S., Omongo, C. A., Colvin, J., Karungi, J., & Otim, M. (2022). Effect of temperature and cassava genotype on the development, fecundity and reproduction of Bemisia tabaci SSA1. African Crop Science Journal, 30(2), 185–203. https://doi.org/10.4314/acsj.v30i2.6
  • Katono, K., Macfadyen, S., Omongo, C. A., Odong, T. L., Colvin, J., Karungi, J., & Otim, M. H. (2021). Influence of cassava morphological traits and environmental conditions on field populations of Bemisia tabaci. Insects, 12(7), 604. https://doi.org/10.3390/insects12070604
  • Kawuki, R. S., Kaweesi, T., Esuma, W., Pariyo, A., Kayondo, I. S., Ozimati, A., Kyaligonza, V., Abaca, A., Orone, J., Tumuhimbise, R., Nuwamanya, E., Abidrabo, P., Amuge, T., Ogwok, E., Okao, G., Wagaba, H., Adiga, G., Alicai, T., Omongo, C. A., … Baguma, Y. (2016). Eleven years of breeding efforts to combat cassava brown streak disease. Breeding Science, 66(4), 560–571. https://doi.org/10.1270/jsbbs.16005
  • Kidd, N. A. C., & Jervis, M. A. (1991). Host-feeding and oviposition strategies of parasitoids in relation to host stage. Researches on Population Ecology, 33(1), 13–28. https://doi.org/10.1007/BF02514570
  • Kuznetsova, A., Brockhoff, P., & Christensen, R. (2016). lmerTest: Tests in Linear Mixed Effects Models. R pac kage version 2.0-33. https://CRAN.R-project.org/package=lmerTest
  • Legg, J. P., Jeremiah, S. C., Obiero, H. M., Maruthi, M. N., Ndyetabula, I., Okao-Okuja, G., Bouwmeester, H., Bigirimana, S., Tata-Hangy, W., Gashaka, G., Mkamilo, G., Alicai, T., & Lava Kumar, P. (2011). Comparing the regional epidemiology of the cassava mosaic and cassava brown streak virus pandemics in Africa. Virus Research, 159(2), 161–170. https://doi.org/10.1016/j.virusres.2011.04.018
  • Legg, J. P., Shirima, R., Tajebe, L. S., Guastella, D., Boniface, S., Jeremiah, S., Nsami, E., Chikoti, P., & Rapisarda, C. (2014). Biology and management of Bemisia whitefly vectors of cassava virus pandemics in Africa. Pest Management Science, 70(10), 1446–1453. https://doi.org/10.1002/ps.3793
  • Luo, C., & Liu, T. X. (2011). Fitness of Encarsia sophia (Hymenoptera: Aphelinidae) parasitizing Trialeurodes vaporariorum and Bemisia tabaci (Hemiptera: Aleyrodidae). Insect Science, 18(1), 84–91. https://doi.org/10.1111/j.1744-7917.2010.01394.x
  • Meyerdirk, D., Muniappan, R., Warkentin, R., Bamba, J., & Reddy, G. (2004). Biological control of the papaya mealybug, Paracoccus marginatus (Hemiptera: Pseudococcidae) in Guam. Plant Protection Qaurterly, 19(3), 110–114.
  • Moore, D. (1988). Agents used for biological control of mealybugs (Pseudococcidae). Biocontrol News and Information, 9(4), 209–225. https://doi.org/10.1079/cabireviews/19891131695
  • Mugerwa, H., Colvin, J., Alicai, T., Omongo, C. A., Kabaalu, R., Visendi, P., Sseruwagi, P., & Seal, S. E. (2021). Genetic diversity of whitefly (Bemisia spp.) on crop and uncultivated plants in Uganda: Implications for the control of this devastating pest species complex in Africa. Journal of Pest Science, 1–24. https://doi.org/10.1007/s10340-021-01355-6
  • Nell, H., Sevenster-van der Lelie, L., Woets, J., & van Lanteren, J. (1976). The parasite-host relationship between Encarsia formosa (Hymenoptera: Aphelinidae) and Trialeurodes vaporariorum (Homoptera: Aleyrodidae). Zeitschrift Fur Angewandte Entomologie, 81(1–4), 372–376. https://doi.org/10.1111/j.1439-0418.1976.tb04249.x
  • Neuenschwander, P. (2001). Biological control of the cassava mealybug in Africa: A review. Biological Control, 21(3), 214–229. https://doi.org/10.1006/bcon.2001.0937
  • Neuenschwander, P. (2004). Harnessing nature in Africa: Biological pest control can benefit the pocket, health and the environment. Nature, 432(7019), 801–802. https://doi.org/10.1038/432801a
  • Neuenschwander, P., Boavida, C., Bokonon-Ganta, A., Gado, A., & Herren, H. R. (1994). Establishment and spread of Gyranusoidea tebygi Noyes and Anagyrus mangicola Noyes (Hymenoptera: Encyrtidae), two biological control agents released against the mango Mealybug Rastrococcus invadens Williams (Homoptera: Pseudococcidae) in Africa. Biocontrol Science and Technology, 4(1), 61–69. https://doi.org/10.1080/09583159409355313
  • Neuenschwander, P., & Hammond, W. N. O. (1988). Natural enemy activity following the introduction of Epidinocarsis lopezi (Hymenoptera: Encyrtidae) against the cassava mealybug, Phenacoccus manihoti (Homoptera: Pseudococcidae), in southwestern Nigeria. Environmental Entomology, 17(5), 894–902. https://doi.org/10.1093/ee/17.5.894
  • Omongo, C. A., Kawuki, R., Bellotti, A. C., Alicai, T., Baguma, Y., Maruthi, M. N., Bua, A., & Colvin, J. (2012). African Cassava Whitefly, Bemisia tabaci, resistance in African and South American cassava genotypes. Journal of Integrative Agriculture, 11(2), 327–336. https://doi.org/10.1016/S2095-3119(12)60017-3
  • Otim, M., Kyalo, G., Kyamanywa, S., Asiimwe, P., Legg, J. P., Guershon, M., & Gerling, D. (2008). Parasitism of Bemisia tabaci (Homoptera: Aleyrodidae) by Eretmocerus mundus (Hymenoptera: Aphelinidae) on cassava. International Journal of Tropical Insect Science, 28((03|3)), 158–167. https://doi.org/10.1017/S1742758408093181
  • Otim, M., Legg, J., Kyamanywa, S., Polaszek, A., & Gerling, D. (2005). Occurrence and activity of Bemisia tabaci parasitoids on cassava in different agro-ecologies in Uganda. BioControl, 50(1), 87–95. https://doi.org/10.1007/s10526-004-0822-4
  • Otim, M., Legg, J., Kyamanywa, S., Polaszek, A., & Gerling, D. (2006). Population dynamics of Bemisia tabaci (Homoptera: Aleyrodidae) parasitoids on cassava mosaic disease-resistant and susceptible varieties. Biocontrol Science and Technology, 16(2), 205–214. https://doi.org/10.1080/09583150500335558
  • Otim, M. H. (2007). The distribution, biology and behaviour of major natural enemies of Bemisia tabaci (gennadius) (Homoptera: Aleyrodidae) on cassava (Manihot esculenta Crantz) in Uganda [Doctoral dissertation]. Makerere University.
  • Patil, B. L., Legg, J. P., Kanju, E., & Fauquet, C. M. (2015). Cassava brown streak disease: A threat to food security in Africa. Journal of General Virology, 96(5), 956–968. https://doi.org/10.1099/jgv.0.000014
  • Powell, D. A., & Bellows, J. T. (1992). Development and reproduction of two populations of Eretmocerus species (Hymenoptera: Aphelinidae) on Bemisia tabaci (Homoptera: Aleyrodidae). Environmental Entomology, 21(3), 651–658. https://doi.org/10.1093/ee/21.3.651
  • R Core Team. (2017). R: A language and environment for statistical computing. R Foundation for Statistical Computing. 2017.
  • Rosenheim, J. A., & Rosen, D. (1992). Influence of egg load and host size on host-feeding behaviour of the parasitoid Aphytis lingnanensis. Ecological Entomology, 17(3), 263–272. https://doi.org/10.1111/j.1365-2311.1992.tb01057.x
  • Ruiz-Narváez, E., & Castro-Webb, N. (2003). A simple method to estimate percentage parasitism when the host and parasitoid phenologies are unknown : A statistical approach. BioControl, 48(1), 87–100. https://doi.org/10.1023/A:1021258000572
  • Sandlan, K. (1979). Host-feeding and its effects on the physiology and behaviour of the ichneumonid parasitoid, Cuccygumimus turionellae. Physiological Entomology, 4(4), 383–392. https://doi.org/10.1111/j.1365-3032.1979.tb00631.x
  • Sippell, D. W., Bindra, O. S., & Khalifa, H. (1987). Resistance to whitefly (Bemisia tabaci) in cotton (Gossypium hirsutum) in the Sudan. Crop Protection, 6(3), 171–178. https://doi.org/10.1016/0261-2194(87)90007-X
  • Sohani, N. Z, Shishehbor, P., & Kocheili, F. (2008). Functional and numeric response of Eretmocerus mundus Mercet (Hymenoptera: Aphelinidae) parasitising cotton whitefly, Bemisia tabaci Gennadius (Homoptera: Aleyrodidae. Pakistan Journal of Biological Sciences, 11(7), 1015–1020. https://doi.org/10.3923/pjbs.2008.1015.1020
  • Sseruwagi, P., Sserubombwe, W. S., Legg, J. P., Ndunguru, J., & Thresh, J. M. (2004). Methods of surveying the incidence and severity of cassava mosaic disease and whitefly vector populations on cassava in Africa: A review. Virus Research, 100(1), 129–142. https://doi.org/10.1016/j.virusres.2003.12.021
  • Sutterlin, S., & Van-Lenteren, J. (1996). Hairiness of Gerbera jamesonii leaves and the walking speed of the parasitoid Encarsia formosa. IOBC/WPRS Bulletin, 19(1), 171–174.
  • Takahashi, K. M., Berti-Filho, E., & Lourenção, A. L. (2008). Biology of Bemisia tabaci (Genn.) B-biotype and parasitism by Encarsia formosa (Gahan) on collard, soybean and tomato plants. Scientia Agricola, 65(6), 639–642. https://doi.org/10.1590/S0103-90162008000600011
  • Togola, A., Meseka, S., Menkir, A., Badu-Apraku, B., Boukar, O., Tamo, M., & Djouaka, R. (2018). Measurement of pesticide residues from chemical control of the invasive Spodoptera frugiperda (Lepidoptera: Noctuidae) in a maize experimental field in Mokwa, Nigeria. International Journal of Environmental Researchand Public Health, 15(5), 849. https://doi.org/10.3390/ijerph15050849
  • Torres, L. C., Lourenção, A. L., Costa, V. A., Souza, B., Costa, M. B., & Tanque, R. L. (2014). Records of natural enemies of Bemisia tabaci (Genn.) (Hemiptera: Aleyrodidae) biotype B in Brazil. Neotropical Entomology, 43(2), 189–191. https://doi.org/10.1007/s13744-013-0188-3
  • Urbaneja, A., Sánchez, E., & Stansly, P. A. (2007). Life history of Eretmocerus mundus, a parasitoid of Bemisia tabaci, on tomato and sweet pepper. BioControl, 52(1), 25–39. https://doi.org/10.1007/s10526-006-9014-8
  • Urbaneja, A., & Stansly, P. A. (2004). Host suitability of different instars of the whitefly Bemisia tabaci ‘biotype Q’ for Eretmocerus mundus. BioControl, 49(2), 153–161.
  • van Lenteren, J. C., Hua, L. Z., Kamerman, J. W., & Rumei, X. (1995). The parasite-host relationship between Encarsia formosa (Hym., aphelinidae) and Trialeurodes vaporariorum (Horn., Aleyrodidae) XXVI. Leaf hairs reduce the capacity of Encarsia to control greenhouse whitefly on cucumber. Journal of Applied Entomology, 119(1–5), 553–559. https://doi.org/10.1111/j.1439-0418.1995.tb01335.x
  • Venables, W., & Ripley, B. (2002). Modern applied statistics with S (4th ed.). Springer. ISBN 0 -387-95457-0.
  • Yang, N. W., Ji, L. L., Lövei, G. L., & Wan, F. H. (2012). Shifting preference between oviposition vs. host-feeding under changing host densities in two aphelinid parasitoids. PLoS ONE, 7(7), e41189. https://doi.org/10.1371/journal.pone.0041189
  • Zang, L., & Liu, T. (2007). Intraguild interactions between an oligophagous predator, Delphastus catalinae (Coleoptera: Coccinellidae), and a parasitoid, Encarsia sophia (Hymenoptera : Aphelinidae), of Bemisia tabaci (Homoptera: Aleyrodidae). Biological Control, 41(1), 142–150. https://doi.org/10.1016/j.biocontrol.2007.01.009
  • Zang, L., & Liu, T. (2008). Host-feeding of three parasitoid species on Bemisia tabaci biotype B and implications for whitefly biological control. Entomologia Experimentalis et Applicata, 127(1), 55–63. https://doi.org/10.1111/j.1570-7458.2008.00667.x
  • Zang, L., Liu, T., Zhang, F., Shi, S., & Wan, F. (2011). Mating and host density affect host feeding and parasitism in two species of whitefly parasitoids. Insect Science, 18(1), 78–83. https://doi.org/10.1111/j.1744-7917.2010.01382.x
  • Zhang, X., Zhang, F., Luo, C., & Wang, S. (2014). Ultrastructure of antennal sensilla of an autoparasitoid Encarsia sophia (Hymenoptera: Aphelinidae). Micron, 67, 132–140. https://doi.org/10.1016/j.micron.2014.07.011
  • Zhou, C. Q., Li, Y. X., Liu, T. X., Zhang, F., & Luo, C. (2010). Development and morphology of female immature of Encarsia sophia and their longevity and fecundity. Chinese Journal of Biological Control, 26(2), 113–118.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.