Abstract
In augmentative biocontrol, more generalists are being investigated for their potential in pest control. Although other food sources such as supplementary food may enhance the survival of generalists, whether they will affect their predation capacity is still an open question. Here, we investigated the influence of Typha orientalis pollen on the predation rates and functional response of Neoseiulus cucumeris (Oudemans) (Acari: Phytoseiidae) to immature Tetranychus urticae Koch (Acari: Tetranychidae). Pollen did lead to a decrease in predation rate of the predator in the short-term test. However, N. cucumeris displayed a type II functional response to immature T. urticae, with high predation rates on eggs and larvae irrespective of the presence of pollen. Pollen also did not have a significant negative influence on the attack rate and handling time of the predators. These findings suggest that N. cucumeris can be an efficient predator of immature T. urticae even when pollen is available.
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References
Ahn JJ, Kim KW, Lee JH (2010) Functional response of Neoseiulus californicus (Acari: Phytoseiidae) to Tetranychus urticae (Acari: Tetranychidae) on strawberry leaves. J Appl Entomol 134(2):98–104
Al-Shammer KA (2011) Plant pollen as an alternative food source for rearing Euseius scutalis (Acari: Phytoseiidae) in Hail, Saudi Arabia. J Entomol 8:365–374
Aljetlawi AA, Sparrevik E, Leonardsson K (2004) Prey–predator size-dependent functional response: derivation and rescaling to the real world. J Anim Ecol 73:239–252
Alves SB, Tamai MA, Rossi LS, Castiglioni E (2005) Beauveria bassiana pathogenicity to the citrus rust mite Phyllocoptruta oleivora. Exp Appl Acarol 37:117–122
Attia S, Grissa KL, Lognay G, Bitume E, Hance T, Mailleux AC (2013) A review of the major biological approaches to control the worldwide pest Tetranychus urticae (Acari: Tetranychidae) with special reference to natural pesticides. J Pest Sci 86:361–386
Badii MH, Hernández-Ortiz E, Flores AE, Landeros J (2004) Prey stage preference and functional response of Euseius hibisci to Tetranychus urticae (Acari: Phytoseiidae, Tetranychidae). Exp Appl Acarol 34:263–273
Bale JS, van Lenteren JC, Bigler F (2008) Biological control and sustainable food production. Phil Trans R Soc B 363:761–776
Berryman AA (1992) The origins and evolution of predator–prey theory. Ecology 73:1530–1535
Carrillo D, Peña JE (2012) Prey-stage preferences and functional and numerical responses of Amblyseius largoensis (Acari: Phytoseiidae) to Raoiella indica (Acari: Tenuipalpidae). Exp Appl Acarol 57:361–372
Chesson J (1989) The effect of alternative prey on the functional response of Notonecta Hoffmani. Ecology 70:1227–1235
De Alfaia JP, Melo LL, Monteiro NV, Lima DB, Melo JWS (2018) Functional response of the predaceous mites Amblyseius largoensis and Euseius concordis when feeding on eggs of the cashew tree giant whitefly Aleurodicus cocois. Syst Appl Acarol 23(8):1559–1566
Everson P (1979) The functional response of Phytoseiulus persimilis (Acarina: Phytoseiidae) to various densities of Tetranychus urticae (Acarina: Tetranychidae). Can Entomol 111:7–10
Everson P (1980) The relative activity and functional response of Phytoseiulus persimilis (Acarina: Phytoseiidae) and Tetranychus urticae (Acarina: Tetranychidae): the effect of temperature. Can Entomol 112:17–24
Farazmand A, Fathipour Y, Kamali K (2012) Functional response and mutual interference of Neoseiulus californicus and Typhlodromus bagdasarjani (Acari: Phytoseiidae) on Tetranychus urticae (Acari: Tetranychidae). Int J Acarol 38(5):369–376
Fathipour Y, Karimi M, Farazmand A, Talebi AA (2017) Age-specific functional response and predation rate of Amblyseius swirskii (Phytoseiidae) on two-spotted spider mite. Syst Appl Acarol 22(2):159–169
Ganjisaffar F, Perring TM (2015) Prey stage preference and functional response of the predatory mite Galendromus flumenis to Oligonychus pratensis. Biol Control 82:40–45
Gerson U, Weintraub PG (2012) Mites (Acari) as a factor in greenhouse management. Annu Rev Entomol 57:229–247
Gotoh T, Nozawa M, Yamaguchi K (2004) Prey consumption and functional response of three acarophagous species to eggs of the two-spotted spider mite in the laboratory. Appl Entomol Zool 39:97–105
Hassell M, Southwood TRE (1978) Foraging strategies of insects. Annu Rev Ecol Evol Syst 9:75–98
Hatt S, Osawa N (2019) The role of Perilla frutescens flowers on fitness traits of the ladybird beetle Harmonia axyridis. BioControl 64:381–390
Huang N, Enkegaard A, Osborne LS, Ramakers PMJ, Messelink GJ, Pijnakker J, Murphy G (2011) The banker plant method in biological control. Crit Rev Plant Sci 30:259–278
Isikber AA (2005) Functional response of two coccinellid predators, Scymnus levaillanti and Cycloneda sanguinea, to the cotton aphid Aphis gossypii. Turk J Agric For 29(5):347–355
Janssen A, Sabelis MW (2015) Alternative food and biological control by generalist predatory mites: the case of Amblyseius swirskii. Exp Appl Acarol 65:413–418
Juliano SA (2001) Nonlinear curve fitting: predation and functional response curves. Des Anal Ecol Exp 2:178–196
Kar F, Lin S, Zhang ZQ (2015) Neocypholaelaps novaehollandiae Evans (Acari: Ameroseiidae) rediscovered: experiments on its life history and behaviour. NZ Entomol 38(2):126–133
Kasap İ (2019) Effect of pollen with different predator release ratios on biological control of Tetranychus urticae by the predaceous mite Kampimodromus aberrans. Syst Appl Acarol 24(7):1310–1318
Khanamani M, Fathipour Y, Talebi AA, Mehrabadi M (2017) How pollen supplementary diet affect life table and predation capacity of Neoseiulus californicus on two-spotted spider mite. Syst Appl Acarol 22:135–147
Leman A, Messelink GJ (2015) Supplemental food that supports both predator and pest: a risk for biological control? Exp Appl Acarol 65:511–524
Li GY, Zhang ZQ (2016) Some factors affecting the development, survival and prey consumption of Neoseiulus cucumeris (Acari: Phytoseiidae) feeding on Tetranychus urticae eggs (Acari: Tetranychidae). Syst Appl Acarol 21:555–567
Li D-X, Tian J, Shen Z-R (2006) Effects of pesticides on the functional response of predatory thrips, Scolothrips takahashii to Tetranychus viennensis. J Appl Entomol 130:314–322
Li L, Jiao R, Yu L, He XZ, He L, Xu C, Zhang L, Liu J (2018) Functional response and prey stage preference of Neoseiulus barkeri on Trasonemus confusus. Syst Appl Acarol 23(11):2244–2258
Liu J-F, Zhang ZQ, Beggs JR, Zou X (2019) Provisioning predatory mites with entomopathogenic fungi or pollen improves biological control of a greenhouse psyllid pest. Pest Manag Sci 75:3200–3209
McMurtry JA, Moraes GJD, Sourassou NF (2013) Revision of the lifestyles of phytoseiid mites (Acari: Phytoseiidae) and implications for biological control strategies. Syst Appl Acarol 18:297–320
Muñoz-Cárdenas K, Fuentes LS, Cantor RF, Rodríguez CD, Janssen A, Sabelis MW (2014) Generalist red velvet mite predator (Balaustium sp.) performs better on a mixed diet. Exp Appl Acarol 62:19–32
Muñoz-Cárdenas K, Ersin F, Pijnakker J, van Houten Y, Hoogerbrugge H, Leman A, Pappas ML, Duarte MVA, Messelink GJ, Sabelis MW, Janssen A (2017) Supplying high-quality alternative prey in the litter increases control of an above-ground plant pest by a generalist predator. Biol Control 105:19–26
Nomikou M, Janssen A, Schraag R, Sabelis MW (2002) Phytoseiid predators suppress populations of Bemisia tabaci on cucumber plants with alternative food. Exp Appl Acarol 27:57–68
Nomikou M, Sabelis MW, Janssen A (2010) Pollen subsidies promote whitefly control through the numerical response of predatory mites. BioControl 55:253–260
Omoto C, Dennehy TJ, McCoy CW, Crane SE, Long JW (1994) Detection and characterization of the interpopulation variation of citrus rust mite (Acari: Eriophyidae) resistance to dicofol in Florida citrus. J Econ Entomol 87:566–572
Pakyari H, Enkegaard A (2013) Functional response of predatory thrips to two-spotted spider mite: influence of pesticides. Int J Acarol 39:526–532
Patel K, Zhang ZQ (2017) Functional and numerical responses of Amblydromalus limonicus and Neoseiulus cucumeris to eggs and first instar nymph of tomato/potato psyllid (Bactericera cockerelli). Syst Appl Acarol 22:1476–1488
Pernando MHJP, Hassell MP (1980) Predator-prey responses in an acarine system. Res Popul Ecol 22(2):301–322
Pimentel D, Burgess M (2014) Environmental and economic costs of the application of pesticides primarily in the United States. In: Peshin R, Pimentel D (eds) Integrated pest management. Springer, Berlin, pp 47–71
Pritchard DW, Barrios-O'Neill D, Bovy H, Paterson R (2017a). Frair-package: tools for functional response analysis in R. https://cran.r-project.org/web/packages/frair/index.html
Pritchard DW, Paterson RA, Bovy HC, Barrios-O’Neill D (2017b) Frair: an R package for fitting and comparing consumer functional responses. Methods Ecol Evol 8:1528–1534
Rogers D (1972) Random search and insect population models. J Anim Ecol 41:369–383
Ryoo MI (1996) Influence of the spatial distribution pattern of prey among patches and spatial coincidence on the functional and numerical response of Phytoseiulus persimilis (Acarina, Phytoseiidae). J Appl Entomol 120:187–192
Sabelis MW, Bakker FM (1992) How predatory mites cope with the web of their tetranychid prey: a functional view on dorsal chaetotaxy in the Phytoseiidae. Exp Appl Acarol 16:203–225
Santos MA (1975) Functional and numerical responses of the predatory mite, Amblyseius fallacis, to prey density. Environ Entomol 4(6):989–992
Schuldiner-Harpaz T, Coll M, Weintraub PG (2016) Prey and pollen food choice depends on previous diet in an omnivorous predatory mite. Environ Entomol 45:995–998
Skirvin DJ, Fenlon JS (2001) Plant species modifies the functional response of Phytoseiulus persimilis (Acari: Phytoseiidae) to Tetranychus urticae (Acari: Tetranychidae): implications for biological control. Bull Entomol Res 91:61–67
Skirvin DJ, Fenlon JS (2003) The effect of temperature on the functional response of Phytoseiulus persimilis (Acari: Phytoseiidae). Exp Appl Acarol 31:37–49
Skirvin DJ, Kravar-Garde L, Reynolds K, Jones J, Mead A, Fenlon J (2007) Supplemental food affects thrips predation and movement of Orius laevigatus (Hemiptera: Anthocoridae) and Neoseiulus cucumeris (Acari: Phytoseiidae). Bull Entomol Res 97:309–315
Su J, Liu M, Fu ZS, Zhu AD, Zhang JP (2019) Effects of alternative and natural prey on body size, locomotion and dispersal of Neoseiulus bicaudus (Acari: Phytoseiidae). Syst Appl Acarol 24(9):1579–1591
Sun B, Zhang YK, Xue XF, Li YX, Hong XY (2015) Effects of Wolbachia infection in Tetranychus urticae (Acari: Tetranychidae) on predation by Neoseiulus cucumeris (Acari: Phytoseiidae). Syst Appl Acarol 20(6):591–602
Symondson WOC, Sunderland KD, Greenstone MH (2002) Can generalist predators be effective biocontrol agents? Annu Rev Entomol 47:561–594
Tschanz B, Bersier L-F, Bacher S (2007) Functional responses: a question of alternative prey and predator density. Ecology 88:1300–1308
VacacelaAjila HE, Colares F, Lemos F, Marques PH, Franklin EC, Santos do Vale W, Oliveira EE, Venzon M, Pallini A (2019) Supplementary food for Neoseiulus californicus boosts biological control of Tetranychus urticae on strawberry. Pest Manag Sci 75:1986–1992
van Leeuwen T, Vontas J, Tsagkarakou A, Dermauw W, Tirry L (2010) Acaricide resistance mechanisms in the two-spotted spider mite Tetranychus urticae and other important Acari: a review. Insect Biochem Mol Biol 40:563–572
van Lenteren JC (2012) The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. BioControl 57(1):1–20
van Rijn PCJ, van Houten YM, Sabelis MW (2002) How plants benefit from providing food to predators even when it is also edible to herbivores. Ecology 83:2664–2679
Vangansbeke D, Nguyen DT, Audenaert J, Verhoeven R, Gobin B, Tirry L, De Clercq P (2016) Supplemental food for Amblyseius swirskii in the control of thrips: feeding friend or foe? Pest Manag Sci 72:466–473
Vantornhout I, Minnaert HL, Tirry L, De Clercq P (2005) Influence of diet on life table parameters of Iphiseius degenerans (Acari: Phytoseiidae). Exp Appl Acarol 35:183–195
Welch KD, Pfannenstiel RS, Harwood JD (2012) The role of generalist predators in terrestrial food webs: lessons for agricultural pest management. In: Gurr GM, Wratten SD, Snyder WE, Read DMY (eds) Biodiversity and insect pests: key issues for sustainable management. Wiley, New York, pp 41–56
Ye SS, Zhang ZQ (2014) Age and size at maturity in Tyrophagus curvipenis (Acari: Acaridae) when fed on three different diets. Syst Appl Acarol 19(4):506–512
Zhang ZQ (2003) Mites of greenhouses: identification, biology and control. CABI Publishing, Cambridge
Zheng Y, De Clercq P, Song ZW, Li DS, Zhang BX (2017) Functional response of two Neoseiulus species preying on Tetranychus urticae Koch. Syst Appl Acarol 22(7):1059–1069
Zhu R, Guo JJ, Yi TC, Xiao R, Jin DC (2019) Functional and numerical responses of Neoseiulus californicus (McGregor) to eggs and nymphs of Oulenziella bakeri and Tetranychus urticae. Syst Appl Acarol 24(7):1225–1235
Acknowledgements
We thank Mr Ray Prebble of Manaaki Whenua – Landcare Research (New Zealand) for revising and reviewing the early draft of this manuscript and Dr Tingting Li of Southwest University (China) for advice on statistics. Comments by two anonymous reviewers and two editors of BioControl also improved the final version. Guang-Yun Li was supported by a PhD scholarship from the China Scholarship Council. Zhi-Qiang Zhang was funded in part by New Zealand Government core funding for Crown Research Institutes from the Ministry of Business, Innovation and Employment’s Science and Innovation Group.
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The manuscript is original and none of the material has been published or is under consideration elsewhere, including the Internet. We have no related manuscripts submitted to other journals. The experiments used arthropods cultured in accordance with institutional guidelines.
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Li, GY., Zhang, ZQ. Can supplementary food (pollen) modulate the functional response of a generalist predatory mite (Neoseiulus cucumeris) to its prey (Tetranychus urticae)?. BioControl 65, 165–174 (2020). https://doi.org/10.1007/s10526-019-09993-7
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DOI: https://doi.org/10.1007/s10526-019-09993-7