The effects of maize pollen on development and population growth potential of Amblyseius swirskii and Cydnoseius negevi (Acari: Phytoseiidae)in subsequent generations

Document Type : Original Article

Authors

Pests and Plant Protection Department, National Research Centre (NRC), El-Buhouth Street, Dokki, Cairo, Egypt

Abstract
Diet is an important component of mass-production system of bio-control agents. Thus, using a non-prey diet (such as plant pollen) instead of natural prey could be more cost-effective in mass-production of phytoseiid predatory mites. Therefore, the present study aimed to examine the multigenerational effect of maize, Zea mays L. (Poaceae), pollen diet on life table parameters of Amblyseius swirskii Athias-Henriot and Cydnoseius negevi (Swirski & Amitai) (Acari: Phytoseiidae) reared for one, five and 11 consecutive generations. The predatory mites A. swirskii and C. negevi successfully completed their development on maize pollen for up to 11 generations. In G1, oviposition days, adult longevity, and fecundity showed significantly higher values in the case of C. negevi as compared to A. swirskii. Despite statistically similar oviposition days in the G11, A. swirskii females (44.43 eggs/♀) deposited significantly more eggs than those of C. negevi (40.60 eggs/♀). There were no significant differences in finite rate of increase (λ), intrinsic rate of increase (r), net (R0) and gross (GRR) reproductive rates between the two predatory mites in G1 and G5 (P ≥ 0.05). In G11, individuals of C. negevi had significantly higher values of r (0.181 day−1) and λ (1.198 day−1) compared to those of A. swirskii (r = 0.159 day−1, λ = 1.173 day−1). However, there were no significant differences in R0 and GRR values between A. swirskii (R0 =34.18 offspring, GRR = 39.75 offspring) and C. negevi (R0 = 31.23 offspring, GRR = 35.44 offspring) in G11. In conclusion, maize pollen has a great potential as a suitable and cost-effective diet for developing the mass-production system of A. swirskii and C. negevi on non-prey diets, where the performance of these predators remained to some extent constant across generations.

Keywords


Abou-Awad, B.A., Hafez, S.M. & Farhat, B.M. (2014) Biological studies of the predacious mite Amblyseius swirskii, a predator of the broad mite Polyphagotarsonemus latus on pepper plants (Acari: Phytoseiidae: Tarsonemidae). Archives of Phytopathology and Plant Protection, 47: 349–354.
Abou-Elella, G.M., Saber, S.A. & El-Sawi S.A. (2013) Biological aspects and life tables of the predacious mites, Typhlodromips swirskii (Athias-Henriot) and Euseius scutalis (Athias-Henriot) feeding on two scale insect species and plant pollen. Archives of Phytopathology and Plant Protection, 46: 1717–1725.
Alipour, Z., Fathipour, Y., Farazmand, A. & Khanamani, M. (2019) Resistant rose cultivar affects life table parameters of two-spotted spider mite and its predators Phytoseiulus persimilis and Amblyseius swirskii (Phytoseiidae). Systematic and Applied Acarology, 24: 1620–1630.
Al-Shammery, K.A. (2011) Plant pollens as an alternative food source for rearing Euseius scutalis (Acari: Phytoseiidae) in Hail, Saudi Arabia. Journal of Entomology, 8: 365–374.
Ansari, H.S., Fathipour, Y., Hajiqanbar, H., Riahi, E. & Riddick, E.W. (2022) Quality control of the predatory mite Amblyseius swirskii during long-term rearing on almond Prunus amygdalus pollen. Arthropod-Plant Interactions, 16: 645–655.
Barret, D. & Kreiter, S. (1995) Morphometrics of some phytoseiid predatory mites and characteristics of their habitat: consequences for biological control. In: Kropczynska, D., Boczek, J. & Tomczyk, A. (Eds.), The Acari: physiological and ecological aspects of acari-host relation-ships. Dabor, Warszawa, pp. 461–473.
Bujang, J.S., Zakaria, M.H. & Ramaiya, S.D. (2021) Chemical constituents and phytochemical properties of floral maize pollen. PLoS ONE, 16: e0247327. DOI: 10.1371/journal.pone.0247327
Chi, H. (1988) Life-table analysis incorporating both sexes and variable development rates among individuals. Environmental Entomology, 17: 26–34.
Chi, H. (2023) TWO SEX-MSChart: A computer program for the age- stage, two-sex life table analysis. Available from: http://140.120. 197.173/Ecology/prod02. htm
Chi, H. & Liu, H. (1985) Two new methods for the study of insect population ecology. Bulletin of the Institute of Zoology Academia Sinica, 24: 225–240.
Chi, H., Kara, H., Ozgokce, M.S., Atlihan, R., Guncan, A. & Risvanli, M.R. (2022) Innovative application of set theory, Cartesian product, and multinomial theorem in demographic research. Entomologia Generalis, 42(6): 863–874.
Cloutier, C. & Johnson, G.S. (1993) Interaction between life stages in a phytoseiid predator: western flower thrips prey killed by adults as food for protonymphs of Amblyseius cucumeris. Experimental and Applied Acarology, 17(6): 441–449.
Cook, S.M., Awmack, C.S., Murray, D.A. & Williams, I.H. (2003) Are honeybee foraging preferences affected by pollen amino acid composition. Ecological Entomology, 28: 622–627.
Dalir, S., Hajiqanbar, H., Fathipour, Y. & Khanamani, M. (2021) A comprehensive picture of foraging strategies of Neoseiulus cucumeris and Amblyseius swirskii on western flower thrips. Pest Management Science, 77: 5418–5429.‏
De Clercq, P., Arijs, Y., van Meir, T., van Stappen, G., Sorgeloos, P., Dewettinck, K., Rey, M., Grenier, S. & Febvay, G. (2005) Nutritional value of brine shrimp cysts as a factitious food for Orius laevigatus (Heteroptera: Anthocoridae). Biocontrol Science and Technology, 15: 467–479.
Delisle, J.F., Brodeur, J. & Shipp, L. (2015) Evaluation of various types of supplemental food for two species of predatory mites, Amblyseius swirskii and Neoseiulus cucumeris (Acari: Phytoseiidae). Experimental and Applied Acarology, 65: 483–494.
Eini, N., Jafari, S., Fathipour, Y. & Zalucki, M.P. (2022) How pollen grains of 23 plant species affect the performance of predatory mite Neoseiulus californicus. BioControl, 67: 173–187.
El-Laithy, A.Y.M. & Fouly, A.H. (1992) Life table parameters of the two phytoseiid predators Amblyseius scutalis (Athias-Henriot) and A. swirskii A.-H. (Acari: Phytoseiidae) in Egypt. Journal of Applied Entomology, 113: 8–12.
Elshazly, M.M.Y. (2022) A new design for feeding the predatory mite, Amblyseius swirskii Athias-Henriot (Acari: Phytoseiidae), on a liquid artificial diet. Journal of the Advances in Agricultural Researches, 27: 459–470.
Fadaei, E., Hakimitabar, M., Seiedy, M. & Sarraf Moaieri, H. (2018) Effects of different diets on biological parameters of the predatory mite Amblyseius swirskii (Acari: Phytoseiidae). International Journal of Acarology, 44: 341–346.
Fahim, S.F. & El-Saiedy, E.M. (2021) Life table parameters of Amblyseius swirskii and Neoseiulus californicus (Acari: Phytoseiidae) reared on two strawberry cultivars. International Journal of Acarology, 47: 568–574.
Fahim, S.F. & Momen, F.M. (2022) Biology and life table parameters of some phytoseiid mites fed on Oligonychus mangiferus (Acari: Tetranychidae). Persian Journal of Acarology, 11: 263–274.
Fathipour, Y. & Maleknia, B. (2016) Mite predators, , In: Omkar (Ed.), Ecofriendly pest management for food security. Elsevier, San Diego, CA, pp. 329–366.
Fouly, A.H., Awadalla, S.S., Ata, T.E. & Marouf, E.A. (2021) Influence of alternative food sources on different biological aspects of Cydnoseius negevi (Acari: Phytoseiidae). Journal of Plant Protection and Pathology, Mansoura University, 12: 295–301.
Goleva, I. & Zebitz, C.P.W. (2013) Suitability of different pollen as alternative food for the predatory mite Amblyseius swirskii (Acari, Phytoseiidae). Experimental and Applied Acarology, 61: 259–283.
Gravandian, M., Fathipour, Y., Hajiqanbar, H., Riahi, E. & Riddick, E.W. (2022) Long-term effects of cattail Typha latifolia pollen on development, reproduction, and predation capacity of Neoseiulus cucumeris, a predator of Tetranychus urticae. BioControl, 67: 149–160.
Hadadi, A., Fathipour, Y., Hajiqanbar, H. & Riahi, E. (2022) Long-term effects of cattail pollen on development, population growth potential, and predation capacity of Amblyseius swirskii (Acari: Phytoseiidae). Biocontrol Science and Technology, 32: 1403–1416.
Hashemi, S., Asadi, M. & Khanamani, M. (2021) How does feeding on different diets affect the life history traits of Neoseiulus californicus? International Journal of Acarology, 47(5): 367–373.‏
Hoogerbrugge, H., van Houten, Y., van Baal, E. & Bolckmans, K. (2008) Alternative food sources to enable establishment of Amblyseius swirskii (Athias-Henriot) on chrysanthemum without pest presence. OILB/SROP, 32: 79–82.
Hou, F., Ni, Z.-H., Zou, M.-T., Zhu, R., Yi, T.-C., Guo, J.-J. & Jin, D.-C. (2022) The effects of alternative foods on life history and cannibalism of Amblyseius herbicolus (Acari: Phytoseiidae). Insects, 13: 1–14.
Huang, Y.B. & Chi, H. (2013) Life tables of Bactrocera cucurbitae (Diptera: Tephritidae): with an invalidation of the jackknife technique. Journal of Applied Entomology, 137: 327–339.
Hussein, H.E., El-Ela, M.A. & Reda, A.S. (2016) Development, survival and reproduction of Typhlodromus negevi (Swirski and Amitai) (Acari: Phytoseiidae) on various kinds of food. Egyptian Journal of Biological Pest Control, 26(1): 43–45.
Kadkhodazadeh, F., Asadi, M. & Khanamani, M. (2021) Suitability of different pollen grains and Tetranychus urticae as food for the predatory mite, Amblyseius swirskii (Acari: Phytoseiidae). Persian Journal of Acarology, 10(3): 321–334.‏ DOI: 10.22073/pja.v10i3.66952
Kennett, C.E., Flaherty, D.L. & Hoffmann, R.W. (1979) Effect of wind-borne pollens on the population dynamics of Amblyseius hibisci (Acarina: Phytoseiidae). Entomophaga, 24: 83–98.
Khanamani, M., Basij, M. & Fathipour, Y. (2021) Effectiveness of factitious foods and artificial substrate in mass rearing and conservation of Neoseiulus californicus (Acari: Phytoseiidae). International Journal of Acarology, 47(4): 273–280.
Khanamani, M., Fathipour, Y., Talebi A.A. & Mehrabadi, M. (2017a) How pollen supplementary diet affect life table and predation capacity of Neoseiulus californicus on two-spotted spider mite. Systematic and Applied Acarology, 22(1): 135–147.
Khanamani, M., Fathipour, Y., Talebi, A.A. & Mehrabadi, M. (2017b) Linking pollen quality and performance of Neoseiulus californicus (Acari: Phytoseiidae) in two-spotted spider mite management programmes. Pest Management Science, 73: 452–461.
Khanamani, M., Fathipour, Y., Talebi, A.A. & Mehrabadi, M. (2017c) Quantitative analysis of longterm mass rearing of Neoseiulus californicus (Acari: Phytoseiidae) on almond pollen. Journal of Economic Entomology, 110: 1442–1450.
Knapp, M., van Houten, Y., van Ball, E. & Groot, T. (2018) Use of the predatory mites in commercial biocontrol: current status and future prospects. Acarologia, 58: 72–82.
Lee, H. & Gillespie, D. (2011) Life table and development of Amblyseius swirskii (Acari: Phytoseiidae) at different temperatures. Experimental and Applied Acarology, 53: 17–27.
Lee, M.H. & Zhang, Z.-Q. (2018) Assessing the augmentation of Amblydromalus limonicus with the supplementation of pollen, thread, and substrates to combat greenhouse whitefly populations. Scientific Reports, 8: 1–14.
Li, D.-Y., He, Y.-F. & Li, H.-D. (2006) Biology and life table of the predatory mite Euseius aizawai (Acari: Phytoseiidae). Systematic and Applied Acarology, 11: 159–165.
McMurtry, J.A. & Croft, B.A. (1997) Life-styles of Phytoseiidae mite and their roles in biological control. Annual Review of Entomology, 42: 291–321.
McMurtry, J.A., de Moraes, G.J. & Sourassou, N.F. (2013) Revision of the lifestyles of phytoseiid mites (Acari: Phytoseiidae) and implications for biological control strategies. Systematic and Applied Acarology, 18: 297–320.
Medd, N.C. & Greatrex, R.M. (2014) An evaluation of three predatory mite species for the control of greenhouse whitefly (Trialeurodes vaporariorum). Pest Management Science, 70: 1492–1496.
Messelink, G.J., van Steenpaal, E.F. & Ramakers, P.M.J. (2006) Evaluation of phytoseiid predators for control of western flower thrips on greenhouse cucumber. BioControl, 51: 753–768.
Metwally, A.M., Momen, F.M., Nasr, A.K., Abdallah, A.A., Ebadah, I.M. & Saleh, K.M. (2015) Prey suitability of Tuta absoluta larvae (Lepidoptera: Gelechiidae) for three predatory phytoseiid mites (Acari: Phytoseiidae) under laboratory conditions. Acta Phytopathologica et Entomologica Hungarica, 50: 105–113.
Momen, F., Abdel-Khalek, A. & El-Sawi, S.A. (2009) Life tables of the predatory mite Typhlodromus negevi feeding on prey insect species and pollen diet (Acari: Phytoseiidae). Acta Phytopatholo-gica et Entomologica Hungarica, 44: 353–366.
Momen, F.M. & Abdel-Khalek, A. (2008) Effect of the tomato rust mite Aculops lycopersici (Acari: Eriophyidae) on the development and reproduction of three predatory phytoseiid mites. International Journal of Tropical Insect Science, 28: 53–57.
Naqshbandi, S.S., Fathipour, Y., Hajiqanbar, H. & Yazdanpanah, S. (2023) Long-term effects of saffron pollen on development, reproduction and predation capacity of Neoseiulus cucumeris (Acari: Phytoseiidae). Acarologia, 63: 188–200. DOI: 10.24349/fmo4-ewck
Nemati, A., Riahi, E., Moghadam, K.A., Gwiazdowicz, D.J., Bahari, M.R. & Amini, P. (2019) Comparison of different pollen grains and a factitious prey as food sources for Amblyseius swirskii (Acari: Phytoseiidae). Systematic and Applied Acarology, 24: 2427–2438.
Nemati, A. & Riahi, E. (2020) Does feeding on pollen grains affect the per‌formance of Amblyseius swirskii (Acari: Phytoseiidae) during subsequent generations? Bulletin of Entomological Research, 110: 449–456.
Nguyen, D.T., Vangansbeke, D. & De Clercq, P. (2014) Artificial and factitious foods support the development and reproduction of the predatory mite Amblyseius swirskii. Experimental and Applied Acarology, 62: 181–194.
Nomikou, M., Janssen, A. & Sabelis, M.W. (2003) Phytoseiid predators of whiteflies feed and reproduce on non-prey food sources. Experimental and Applied Acarology, 31: 15–26.
Nomikou, M., Janssen, A., Schraag, R. & Sabelis, M.W. (2001) Phytoseiid predators as potential biological control agents for Bemisia tabaci. Experimental and Applied Acarology, 25: 271–291.
Palevsky, E. (2017) Pollen provisioning for the promotion of biological control by omnivorous phytoseiids in organic greenhouses. Acta Horticulturae, 1164: 383–390.
Park, H.-H., Shipp, L. & Buitenhuis, R. (2010) Predation, development, and oviposition by the predatory mite Amblyseius swirskii (Acari: Phytoseiidae) on tomato russet mite (Acari: Eriophyidae). Journal of Economic Entomology, 103: 563–569.
Park, H.-H., Shipp, L., Buitenhuis, R. & Ahn, J.J. (2011) Life history parameters of a commercially available Amblyseius swirskii (Acari: Phytoseiidae) fed on cattail (Typha latifolia) pollen and tomato russet mite (Aculops lycopersici). Journal of Asia-Pacific Entomology, 14: 497–501.
Pena, J.E., Rodrigues, J.C.V., Roda, A., Carrillo, D. & Osborne, L.S. (2009) Predator-prey dynamics and strategies for control of the red palm mite (Raoiella indica) (Acari: Tenuipalpidae) in areas of invasion in the Neotropics. IOBC-WPRS Bulletins, 50: 69–79.
Pourbahram, P., Hajiqanbar, H., Yazdanpanah, S. & Fathipour, Y. (2022) Generation-dependent demography and predation capacity of Amblyseius swirskii (Acari: Phytoseiidae) fed on saffron pollen. International Journal of Acarology, 48(8): 669–678. DOI: 10.1080/01647954.2023. 2171481
Rahmani Piyani, A., Shishehbor, P., Kocheili, F. & Riddick, E.W. (2021) Comparison of natural prey Tetranychus turkestani, date palm pollen, and bee pollen diets on development, reproduction, and life table parameters of the predator Amblyseius swirskii. Acarologia, 61: 890–900.
Ranabhat, N.B., Goleva, I. & Zebitz, C.P.W. (2014) Life tables of Neoseiulus cucumeris exclusively fed with seven different pollens. BioControl, 59: 195–203.
Riahi, E., Fathipour, Y., Talebi, A.A. & Mehrabadi, M. (2016) Pollen quality and predator viability: life table of Typhlodromus bagdasarjani on seven different plant pollens and two spotted spider mite. Systematic and Applied Acarology, 21: 1399–1412.
Riahi, E., Fathipour, Y., Talebi, A.A. & Mehrabadi, M. (2017) Linking life table and consumption rate of Amblyseius swirskii (Acari: Phytoseiidae) in presence and absence of different pollens. Annals of the Entomological Society of America, 110: 244–253.
Roulston, T.H. & Cane, J.H. (2000) Pollen nutritional content and digestibility for animals. Plant Systematics and Evolution, 222: 187–209.
San, P.P., Tuda, M., Nakahira, K. & Takagi, M. (2020) Optimal rearing medium for the population growth of the predatory mite, Amblyseius swirskii (Athias-Henriot) (Acari: Phytoseiidae). Egyptian Journal of Biological Pest Control, 30: 130. DOI: 10.1186/s41938-020-00332-y
Soltaniyan, A., Kheradmand, K., Fathipour, Y. & Shirdel, D. (2020) Supplementation of natural prey with pollen grains exerts an influence on the life table parameters of Neoseiulus californicus. Bulletin of Entomological Research, 110: 535–541.
Sørensen, J.G., Addison, M.F. & Terblanche, J.S. (2012) Mass rearing of insects for pest management: Challenges, synergies and advances from evolutionary physiology. Crop Protection, 38: 87–94.
van Lenteren, J.C. (2012) The state of commercial augmentative biological control: Plenty of natural enemies, but a frustrating lack of uptake. BioControl, 57: 1–20.
van Rijn, P.C.J. & Tanigoshi, L.K. (1999) The contribution of extrafloral nectar to the survival and reproduction of the predatory mite Iphiseius degenerans on Ricinus communis. Experimental and Applied Acarology, 23: 281–296.
Vangansbeke, D., Nguyen, D.T., Aidenaert, J., Gobin, B., Tirry, L. & Clercq, P.D. (2016) Establishment of Amblyseius swirskii in greenhouse crops using food supplements. Systematic and Applied Acarology, 21: 1174–1184.
Wei, M.F., Chi, H., Guo, Y.F., Li, X.W., Zhao, L.L., Ma, R.Y. (2020) Demography of Cacopsylla chinensis (Hemiptera: Psyllidae) reared on four cultivars of Pyrus bretschneideri and P. communis (Rosales: Rosaceae) pears with estimations of confidence intervals of specific life table statistics. Journal of Economic Entomology 113(5): 2343–2353.
Wimmer, D., Hoffmann, D. & Schausberger, P. (2008) Prey suitability of western flower thrips, Frankliniella occidentalis, and onion thrips, Thrips tabaci, for the predatory mite Amblyseius swirskii. Biocontrol Science and Technology, 18: 533–542.
Yazdanpanah, S., Fathipour, Y., Riahi, E. & Zalucki, M.P. (2021) Mass production of Neoseiulus cucumeris (Phytoseiidae): an assessment of 50 generations reared on almond pollen. Journal of Economic Entomology, 114: 2255–2263.
Yue, B. & Tsai, J.H. (1996) Development, survivorship and reproduction of Amblyseius largoensis (Acari: Phytoseiidae) on selected plant pollens and temperatures. Environmental Entomology, 125: 488–494.
Zannou, I.D. & Hanna, R. (2011) Clarifying the identity of Amblyseius swirskii and Amblyseius rykei (Acari: Phytoseiidae): are they two distinct species or two populations of one species? Experimental and Applied Acarology, 53: 339–347.