Abstract
The poinsettia thrips, Echinothrips americanus Morgan (Thysanoptera: Thripidae), is a key pest of various ornamental and vegetable greenhouse crops. As current biological control alternatives lack efficiency, applying chemicals remains the dominant control strategy, thereby heavily disturbing the biocontrol-based integrated management of other pests. For a range of other thrips pests, phytoseiid predatory mites have shown to be effective biocontrol agents, being able to overcome the thrips’ physical and chemical defense armory. Here, we investigated potential underlying causes for the lack of phytoseiid efficacy in controlling E. americanus. First, we assessed the nutritional value of E. americanus for the predatory mite Amblydromalus limonicus (Garman and McGregor) (Acari: Phytoseiidae) when its physical or chemical defenses were eliminated by freezing the thrips. The phytoseiid could complete its immature development when frozen thrips instars were offered, but not when these were offered alive. Subsequently, we tested whether adult female A. limonicus had a higher predation rate on first instar E. americanus when they had been given experience with either live or frozen E. americanus during their immature development (i.e., conditioning). Conditioning significantly increased the predation capacity of the phytoseiid. Finally, we tested the control potential of conditioned A. limonicus versus naïve ones when exposed to E. americanus on sweet pepper plants. In contrast to the laboratory trials, at the plant level, conditioning did not yield better control. Possible factors explaining insufficient control of E. americanus by phytoseiids are discussed.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abrams PA, Holt RD, Roth JD (1998) Apparent competition or apparent mutualism? Shared predation when populations cycle. Ecology 79:201–212. https://doi.org/10.1890/0012-9658(1998)079[0201:ACOAMS]2.0.CO;2
Bakker FM, Sabelis MW (1989) How larvae of Thrips tabaci reduce the attack success of phytoseiid predators. Entomol Exp Appl 50:47–51. https://doi.org/10.1111/j.1570-7458.1989.tb02313.x
Bielza P (2008) Insecticide resistance management strategies against the western flower thrips, Frankliniella occidentalis: resistance management in F. occidentalis. Pest Manag Sci 64:1131–1138. https://doi.org/10.1002/ps.1620
Buitenhuis R, Shipp JL (2008) Influence of plant species and plant growth stage on Frankliniella occidentalis pupation behaviour in greenhouse ornamentals. J Appl Entomol 132:86–88. https://doi.org/10.1111/j.1439-0418.2007.01250.x
Carrillo D, de Coss ME, Hoy MA, Peña JE (2012) Variability in response of four populations of Amblyseius largoensis (Acari: Phytoseiidae) to Raoiella indica (Acari: Tenuipalpidae) and tetranychus gloveri (Acari: Tetranychidae) eggs and larvae. Biol Control 60:39–45. https://doi.org/10.1016/j.biocontrol.2011.09.002
Chown SL, Gaston KJ (2010) Body size variation in insects: a macroecological perspective. Biol Rev 85:139–169. https://doi.org/10.1111/j.1469-185X.2009.00097.x
Christiansen IC, Szin S, Schausberger P (2016) Benefit-cost trade-offs of early learning in foraging predatory mites Amblyseius swirskii. Sci Rep 6:23571. https://doi.org/10.1038/srep23571
Cox PD, Matthews L, Jacobson RJ, Cannon R, MacLeod A, Walters KFA (2006) Potential for the use of biological agents for the control of Thrips palmi (Thysanoptera: Thripidae) outbreaks. Biocontrol Sci Technol 16:871–891. https://doi.org/10.1080/09583150600827728
Crawley MJ (2007) The R book. Wiley, Chichester, UK
Crespi BJ (1990) Subsociality and female reproductive success in a mycophagous thrips: an observational and experimental analysis. J Insect Behav 3:61–74. https://doi.org/10.1007/BF01049195
de Almeida AA, Janssen A (2013) Juvenile prey induce antipredator behaviour in adult predators. Exp Appl Acarol 59:275–282. https://doi.org/10.1007/s10493-012-9601-6
de Boer JG, Snoeren TAL, Dicke M (2005) Predatory mites learn to discriminate between plant volatiles induced by prey and nonprey herbivores. Anim Behav 69:869–879. https://doi.org/10.1016/j.anbehav.2004.07.010
Drukker B, Bruin J, Jacobs G, Kroon A, Sabelis MW (2000) How predatory mites learn to cope with variability in volatile plant signals in the environment of their herbivorous prey. Exp Appl Acarol 24:881–895. https://doi.org/10.1023/A:1010645720829
Duarte MVA, Venzon M, Bittencourt MC, de S, Rodríguez-Cruz FA, Pallini A, Janssen A (2015) Alternative food promotes broad mite control on chilli pepper plants. Biocontrol 60:817–825. https://doi.org/10.1007/s10526-015-9688-x
Emmerson MC, Raffaelli D (2004) Predator-prey body size, interaction strength and the stability of a real food web. J Anim Ecol 73:399–409. https://doi.org/10.1111/j.0021-8790.2004.00818.x
Faraji F, Janssen A, Sabelis MW (2002) Oviposition patterns in a predatory mite reduce the risk of egg predation caused by prey: Egg distribution pattern in a predatory mite. Ecol Entomol 27:660–664. https://doi.org/10.1046/j.1365-2311.2002.00456.x
Gaum WG, Giliomee JH, Pringle KL (1994) Life history and life tables of western flower thrips, Frankliniella occidentalis (Thysanoptera: Thripidae), on English cucumbers. Bull Entomol Res 84:219–224. https://doi.org/10.1017/S0007485300039729
Ghasemzadeh S, Leman A, Messelink GJ (2017) Biological control of Echinothrips americanus by phytoseiid predatory mites and the effect of pollen as supplemental food. Exp Appl Acarol 73:209–221. https://doi.org/10.1007/s10493-017-0191-1
Gravandian M, Fathipour Y, Hajiqanbar H, Riahi E, Riddick EW (2021) Long-term effects of cattail Typha latifolia pollen on development, reproduction, and predation capacity of Neoseiulus cucumeris, a predator of Tetranychus urticae. https://doi.org/10.1007/s10526-021-10116-4. Biocontrol
Hansen EA, Funderburk JE, Reitz SR, Ramachandran S, Eger JE, McAuslane H (2003) Within-plant distribution of Frankliniella species (Thysanoptera: Thripidae) and Orius insidiosus (Heteroptera: Anthocoridae) in field pepper. Environ Entomol 32:1035–1044. https://doi.org/10.1603/0046-225X-32.5.1035
Holt RD (1977) Predation, apparent competition, and the structure of prey communities. Theor Popul Biol 12:197–229. https://doi.org/10.1016/0040-5809(77)90042-9
Hoogerbrugge H, Oude-Lenferink K, van Houten Y, Bolckmans K (2014) Screening of three phytoseiid mites species as biocontrol agents of Echinothrips americanus. IOBC/wprs Bull 102:97–101
Janssen A, Faraji F, van der Hammen T, Magalhaes S, Sabelis MW (2002) Interspecific infanticide deters predators. Ecol Lett 5:490–494. https://doi.org/10.1046/j.1461-0248.2002.00349.x
Jensen SE (2000) Insecticide resistance in the Western Flower Thrips, Frankliniella ocidentalis. Integr Pest Manag Rev 5:131–146. https://doi.org/10.1023/A:1009600426262
Kakkar G, Kumar V, Seal DR, Liburd OE, Stansly PA (2016) Predation by Neoseiulus cucumeris and Amblyseius swirskii on Thrips palmi and Frankliniella schultzei on cucumber. Biol Control 92:85–91. https://doi.org/10.1016/j.biocontrol.2015.10.004
Leman TA, Ingegno BL, Tavella L, Janssen A, Messelink G (2020) The omnivorous predator Macrolophus pygmaeus, a good candidate for the control of both greenhouse whitefly and poinsettia thrips on gerbera plants. Insect Sci 27:510–518. https://doi.org/10.1111/1744-7917.12655
Lenth RV (2016) Least-Squares Means: the R Package lsmeans. J Stat Softw 69:1–33. https://doi.org/10.18637/jss.v069.i01
Lewis T (1997) Thrips as crop pests. CAB International, Wallingford, UK
MacDonald KM, Hamilton JGC, Jacobson R, Kirk WDJ (2003) Analysis of anal droplets of the Western Flower Thrips Frankliniella occidentalis. J Chem Ecol 29:2385–2389. https://doi.org/10.1023/A:1026244931536
Messelink GJ, Van Steenpaal SEF, Ramakers PMJ (2006) Evaluation of phytoseiid predators for control of western flower thrips on greenhouse cucumber. Biocontrol 51:753–768. https://doi.org/10.1007/s10526-006-9013-9
Moore BR (2004) The evolution of learning. Biol Rev 79:301–335. https://doi.org/10.1017/S1464793103006225
Mouratidis A, de Lima AP, Dicke M, Messelink GJ (2022) Predator-prey interactions and life history of Orius laevigatus and O. majusculus feeding on flower and leaf-inhabiting thrips. Biol Control 172:8. https://doi.org/10.1016/j.biocontrol.2022.104954
Nemati A, Riahi E (2020) Does feeding on pollen grains affect the performance of Amblyseius swirskii (Acari: Phytoseiidae) during subsequent generations? Bull Entomol Res 110:449–456. https://doi.org/10.1017/S0007485319000804
Nguyen VH, Jonckheere W, Nguyen DT, de Moraes GJ, Van Leeuwen T, De Clercq P (2019) Phytoseiid mites prey effectively on thrips eggs: evidence from predation trials and molecular analyses. Biol Control 137:104012. https://doi.org/10.1016/j.biocontrol.2019.104012
Opit GP, Peterson B, Gillespie DR, Costello RA (1997) The life cycle and management of Echinothrips americanus (Thysanoptera: Thripidae). J Entomol Soc Br Columbia 94:3–6
Pascua MS, Rocca M, Greco N, De Clercq P (2020) Typha angustifolia L. pollen as an alternative food for the predatory mite neoseiulus californicus (McGregor) (Acari: Phytoseiidae). Syst Appl Acarol 25:51–62. https://doi.org/10.11158/saa.25.1.4
Pearce JM (2008) Animal learning & cognition: an introduction, 3rd edn. Psychology Press, Hove, NY, USA
Pijnakker J, Leman A, Vangansbeke D, Wäckers FL (2017) Echinothrips americanus: a bottleneck for integrated pest management in ornamentals? Commun Appl Biol Sci 82:105–111
Pijnakker J, Vangansbeke D, Duarte M, Moerkens R, Wäckers F (2020) Predators and parasitoids-in-first: from inundative releases to preventative biological control in greenhouse crops. Front Sustain Food Syst 4:595630. https://doi.org/10.3389/fsufs.2020.595630
Rahmani H, Schausberger P, Hoffmann D, Walzer A (2010) Food imprinting revisited: early learning in foraging predatory mites. Behaviour 147:883–897. https://doi.org/10.1163/000579510X495799
Ramakers PMJ (1980) Biological control of Thrips tabaci (Thysanoptera: Thripidae) with Amblyseius spp. (Acari: Phytoseiidae). IOBC/wprs Bull 3:203–207
Ramakers PMJ, van den Meiracker RAF, Mulder S (2000) Predatory thrips as thrips predators. Med Fac Landbouww Rijksuniv Gent 65:343–350
Reitz SR, Gao Y, Lei Z (2011) Thrips: pests of concern to China and the United States. Agric Sci China 10:867–892. https://doi.org/10.1016/S1671-2927(11)60073-4
Reitz SR, Gao Y, Kirk WDJ, Hoddle MS, Leiss KA, Funderburk JE (2020) Invasion biology, ecology, and management of Western Flower Thrips. Annu Rev Entomol 65:17–37. https://doi.org/10.1146/annurev-ento-011019-024947
Samaras K, Pappas ML, Pekas A, Wäckers F, Broufas GD (2021) Benefits of a balanced diet? Mixing prey with pollen is advantageous for the phytoseiid predator Amblydromalus limonicus. Biol Control 155:104531. https://doi.org/10.1016/j.biocontrol.2021.104531
Schausberger P, Çekin D, Litin A (2020) Learned predators enhance biological control via organizational upward and trophic top-down cascades. J Appl Ecol 58:158–166. https://doi.org/10.1111/1365-2664.13791
Schoeller EN, McKenzie CL, Osborne LS (2020) Comparison of the phytoseiid mites Amblyseius swirskii and Amblydromalus limonicus for biological control of chilli thrips, Scirtothrips dorsalis (Thysanoptera: Thripidae). Exp Appl Acarol 82:309–318. https://doi.org/10.1007/s10493-020-00556-5
Sdoodee R, Teakle DS (1987) Transmission of tobacco streak virus by Thrips tabaci a new method of plant virus transmission. Plant Pathol 36:377–380. https://doi.org/10.1111/j.1365-3059.1987.tb02247.x
Sugiura S, Yamazaki K (2014) Caterpillar hair as a physical barrier against invertebrate predators. Behav Ecol 25:975–983. https://doi.org/10.1093/beheco/aru080
Teerling CR, Gillespie DR, Borden JH (1993a) Utilization of Western Flower Thrips alarm pheromone as a prey-finding kairomone by predators. Can Entomol 125:431–437. https://doi.org/10.4039/Ent125431-3
Teerling CR, Pierce HD, Borden JH, Gillespie DR (1993b) Identification and bioactivity of alarm pheromone in the western flower thrips, Frankliniella occidentalis. J Chem Ecol 19:681–697. https://doi.org/10.1007/BF00985001
Trdan S, Milevoj L, Raspudic E, Zezlina I (2003) The first record of Echinothrips americanus Morgan in Slovenia. Acta Phytopathol Entomol Hung 38:157–166. https://doi.org/10.1556/aphyt.38.2003.1-2.18
Upton MS (1993) Aqueous gum-chloral slide mounting media: an historical review. Bull Entomol Res 83:267–274. https://doi.org/10.1017/S0007485300034763
van Lenteren JC (2012) The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. Biocontrol 57:1–20. https://doi.org/10.1007/s10526-011-9395-1
van Lenteren JC, Bolckmans K, Kohl J, Ravensberg WJ, Urbaneja A (2018) Biological control using invertebrates and microorganisms: plenty of new opportunities. Biocontrol 63:39–59. https://doi.org/10.1007/s10526-017-9801-4
van Rijn PCJ, van Houten YM, Sabelis MW (1999) Pollen improves thrips control with predatory mites. IOBC/wprs Bull 22:209–212
Vangansbeke D, Nguyen DT, Audenaert J, Verhoeven R, Gobin B, Tirry L, De Clercq P (2014a) Food supplementation affects interactions between a phytoseiid predator and its omnivorous prey. Biol Control 76:95–100. https://doi.org/10.1016/j.biocontrol.2014.06.001
Vangansbeke D, Nguyen DT, Audenaert J, Verhoeven R, Gobin B, Tirry L, De Clercq P (2014b) Performance of the predatory mite Amblydromalus limonicus on factitious foods. Biocontrol 59:67–77. https://doi.org/10.1007/s10526-013-9548-5
Vangansbeke D, Pijnakker J, Arijs Y, Wäckers F (2018) Thrips egg predation by phytoseiids: an overlooked pest control mechanism. IOBC/wprs Bull 124:184–188
Vangansbeke D, Duarte MV, Gobin B, Tirry L, Wäckers F, De Clercq P (2020) Cold-born killers: exploiting temperature–size rule enhances predation capacity of a predatory mite. Pest Manag Sci 76:1841–1846. https://doi.org/10.1002/ps.5713
Vierbergen GB (1998) Echinothrips americanus Morgan, a new thrips in dutch greenhouses (Thysanoptera: Thripidae). Proc Sect Exp Appl Entomol Neth Entomol Soc 9:155–160
Vierbergen GB, Cean M, Szellér IH, Jenser G, Masten T, Simala M (2006) Spread of two thrips species in Europe: Echinothrips americanus and Microcephalothrips abdominalis (Thysanoptera: Thripidae). Acta Phytopathol Entomol Hung 41:287–296. https://doi.org/10.1556/aphyt.41.2006.3-4.11
Walzer A, Paulus HF, Schausberger P (2004) Ontogenetic shifts in intraguild predation on thrips by phytoseiid mites: the relevance of body size and diet specialization. Bull Entomol Res 94:577–584. https://doi.org/10.1079/BER2004329
Warren PH, Lawton JH (1987) Invertebrate predator-prey body size relationships: an explanation for upper triangular food webs and patterns in food web structure? Oecologia 74:231–235. https://doi.org/10.1007/BF00379364
Yano S, Shirotsuka K (2013) Lying down with protective setae as an alternative antipredator defence in a non-webbing spider mite. SpringerPlus 2:637. https://doi.org/10.1186/2193-1801-2-637
Acknowledgements
We want to thank Peggy Bogaerts and Ilse Jacobs for growing and maintaining the pepper plants.
Funding
The authors declare that no funds or grants were received during the preparation of this manuscript.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Dominiek Vangansbeke, Emilie Van Doren and Marcus Duarte. The first draft of the manuscript was written by Dominiek Vangansbeke and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Conflict of interest
The authors declare to have no conflict of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Vangansbeke, D., Van Doren, E., Duarte, M.V. et al. Why are phytoseiid predatory mites not effectively controlling Echinothrips americanus?. Exp Appl Acarol 90, 1–17 (2023). https://doi.org/10.1007/s10493-023-00803-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10493-023-00803-5