Abstract
Phytoseiid predatory mites are the most important group of biocontrol agents currently used in protected cultivations worldwide. The possibility to produce these predators at high densities on factitious prey mites is a crucial factor for their success. Commonly used factitious prey mites comprise mainly species belonging to the cohort of Astigmatina. In the present study, we investigated the potential of tarsonemid prey mites as a food source for the spider mite predator Neoseiulus californicus (McGregor) (Acari: Phytoseiidae). The oviposition of N. californicus on mixed stages of Tarsonemus fusarii Cooreman (Acari: Tarsonemidae) was similar to that on its natural prey, the two-spotted spider mite Tetranychus urticae Koch (Acari: Tetranychidae). As most tarsonemids are specialized fungus-feeders, we tested the effect of different fungal species on the growth of T. fusarii. Subsequently, we analysed the impact on the fungal growing medium on the oviposition of N. californicus. The fungal growing medium of T. fusarii had a significant negative effect on the reproductive output of the predatory mite. When T. fusarii was separated from the rearing medium, these detrimental effects were not observed. The present study shows the potential of using tarsonemid prey mites in the production of phytoseiid predatory mites.
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References
Badii MH, McMurtry JA (1984) Feeding behavior of some phytoseiid predators on the broad mite, Polyphagotarsonemus latus (Acari: Phytoseiidae, Tarsonemidae). Entomophaga 29:49–53. https://doi.org/10.1007/BF02372208
Barbesgaard P, Heldt-Hansen H, Diderichsen B (1992) On the safety of Aspergillus oryzae: a review. Appl Microbiol Biotechnol 36:569–572. https://doi.org/10.1007/BF00183230
Barbosa MFC, de Moraes GJ (2015) Evaluation of astigmatid mites as factitious food for rearing four predaceous phytoseiid mites (Acari: Astigmatina; Phytoseiidae). Biol Control 91:22–26
Belczewski RF, Harmsen R (1997) In vitro feeding preferences of the fungivorous mite Tarsonemus confusus Ewing (Tarsonemidae). In: Needham GR, Mitchell R, Horn DJ, Welbourn WC (eds) Acarology IX: Symposia (the proceedings of the Ninth International Conference, Columbus, Ohio, 1994). Ohio Biological Survey, Columbus, OH
Bolckmans K, van Houten Y (2006) Mite composition, use thereof, method for rearing the phytoseiid predatory mite Amblyseius swirskii, rearing system for rearing said phytoseiid mite and methods for biological pest control on a crop. World Intellectual Property Organisation
Calvo FJ, Knapp M, van Houten YM, Hoogerbrugge H, Belda JE (2015) Amblyseius swirskii: What made this predatory mite such a successful biocontrol agent? Exp Appl Acarol 65:419–433. https://doi.org/10.1007/s10493-014-9873-0
Castagnoli M, Nannelli R, Tarchi F, Simoni S (2006) Screening of astgmatid mites for mass-rearing Neoseiulus californicus (McGregor) (Acari: Phytoseiidae). Redia 89:55–58
Crawley MJ (2013) The R book, 2nd edn. Wiley, Chichester
Domsch KH, Gams W, Anderson TH (1980) Compendium of soil fungi. Academic Press, New York
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
Easterbrook MA, Fitzgerald JD, Solomon MG (2001) Biological control of strawberry tarsonemid mite Phytonemus pallidus and two-spotted spider mite Tetranychus urticae on strawberry in the UK using species of Neoseiulus (Amblyseius) (Acari: Phytoseiidae). Exp Appl Acarol 25:25–36. https://doi.org/10.1023/A:1010685903130
Fan YQ, Petitt FL (1994) Biological control of broad mite, Polyphagotarsonemus latus (Banks), by Neoseiulus barkeri Hughes on pepper. Biol Control 4:390–395. https://doi.org/10.1006/bcon.1994.1049
Geeraerts J (1974) Etude de l’attraction exercée par divers champignons sur Tarsonemus fusarii Cooreman 1941. Mycoses 17:27–32. https://doi.org/10.1111/j.1439-0507.1974.tb04246.x
Gerson U (1992) Biology and control of the broad mite, Polyphagotarsonemus latus (Banks) (Acari: Tarsonemidae). Exp Appl Acarol 13:163–178. https://doi.org/10.1007/BF01194934
Gotz H, Reichenberger M (1953) On a mite, ‘Tarsonemus fusarii Cooreman’, destroying fungus cultures. Hautarzt 4:266–268
Huang H, Xu X, Lv J, Li G, Wang E, Gao Y (2013) Impact of proteins and saccharides on mass production of Tyrophagus putrescentiae (Acari: Acaridae) and its predator Neoseiulus barkeri (Acari: Phytoseiidae). Biocontrol Sci Technol 23:1231–1244. https://doi.org/10.1080/09583157.2013.822849
Hubert J, Žilová M, Pekár S (2001) Feeding preferences and gut contents of three panphytophagous oribatid mites (Acari: Oribatida). Eur J Soil Biol 37:197–208. https://doi.org/10.1016/S1164-5563(01)01083-4
Hughes AM (1976) The mites of stored food and houses. H.M.S.O., London
Hummel NA, Castro BA, McDonald EM, Pellerano MA, Ochoa R (2009) The panicle rice mite, Steneotarsonemus spinki Smiley, a re-discovered pest of rice in the United States. Crop Prot 28:547–560. https://doi.org/10.1016/j.cropro.2009.03.011
Hussey NW (1963) A new species of Tarsonemus (Acarina: Tarsonemidae) from cultivated mushrooms. - Acarologia 5:540–544
Ito K, Yoshida K, Ishikawa T, Kobayashi S (1990) Volatile compounds produced by the fungus Aspergillus oryzae in rice Koji and their changes during cultivation. J Ferment Bioeng 70:169–172. https://doi.org/10.1016/0922-338X(90)90178-Y
Kaliszewski M, Sell D (1990) Tarsonemus fusarii Cooreman i Tarsonemus parafusarii Kaliszewski (Acari: Tarsonemidae) w Polsce, ze szczególnym uwzględnieniem ekologii [Tarsonemus fusarii Cooreman and Tarsonemus parafusarii Kaliszewski (Acari: Tarsonemidae) in Poland, with particular regard to their ecology]. Zesz Probl Postepow Nauk Roln 373:195–216 (in polish with russian and english summaries)
Kaliszewski M, Athias-Binche F, Lindquist EE (1995) Parasitism and parasitoidism in Tarsonemina (Acari: Heterostigmata) and evolutionary considerations. In: Advances in parasitology. Elsevier, Amsterdam. https://doi.org/10.1016/S0065-308X(08)60074-3
Knapp M, van Houten Y, van Baal E, Groot T (2018) Use of predatory mites in commercial biocontrol: current status and future prospects. Acarologia 58:72–82. https://doi.org/10.24349/ACAROLOGIA/20184275
Lee MH, Zhang Z-Q (2016) Habitat structure and its influence on populations of Amblydromalus limonicus (Acari: Phytoseiidae). Syst Appl Acarol 21:1361–1378. https://doi.org/10.11158/saa.21.10.7
Lenth RV (2016) Least-squares means: the R package lsmeans. J Stat Softw 69:1–33. https://doi.org/10.18637/jss.v069.i01
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 Tarsonemus confusus. Syst Appl Acarol 23:2244–2258. https://doi.org/10.11158/saa.23.11.16
Lindquist EE (1972) A new species of Tarsonemus from stored grain (Acarina: Tarsonemidae). Can Entomol 104:1699–1708. https://doi.org/10.4039/Ent1041699-11
Lindquist EE (1986) The world genera of Tarsonemidae (Acari: Heterostigmata): a morphological, phylogenetic, and systematic revision, with a a reclassification of family-group taxa in the Heterostigmata. Mem Entomol Soc Can 118:1–517. https://doi.org/10.4039/entm118136fv
Lofego AC, Pitton T, Rezende JM (2016) A new genus and new species of Tarsonemidae (Acari: Heterostigmata) from the Brazilian rainforests. Syst Appl Acarol 21:307–319. https://doi.org/10.11158/saa.21.3.6
Lombardero MJ, Ayres MP, Hofstetter RW, Moser JC, Lepzig KD (2003) Strong indirect interactions of Tarsonemus mites (Acarina: Tarsonemidae) and Dendroctonus frontalis (Coleoptera: Scolytidae). Oikos 102: 243–252. https://doi.org/10.1034/j.1600-0706.2003.12599.x
Machida M, Asai K, Sano M, Tanaka T, Kumagai T, Terai G, Kusumoto K-I, Arima T, Akita O, Kashiwagi Y, Abe K, Gomi K, Horiuchi H, Kitamoto K, Kobayashi T, Takeuchi M, Denning DW, Galagan JE, Nierman WC, Yu J, Archer DB, Bennett JW, Bhatnagar D, Cleveland TE, Fedorova ND, Gotoh O, Horikawa H, Hosoyama A, Ichinomiya M, Igarashi R, Iwashita K, Juvvadi PR, Kato M, Kato Y, Kin T, Kokubun A, Maeda H, Maeyama N, Maruyama J, Nagasaki H, Nakajima T, Oda K, Okada K, Paulsen I, Sakamoto K, Sawano T, Takahashi M, Takase K, Terabayashi Y, Wortman JR, Yamada O, Yamagata Y, Anazawa H, Hata Y, Koide Y, Komori T, Koyama Y, Minetoki T, Suharnan S, Tanaka A, Isono K, Kuhara S, Ogasawara N, Kikuchi H (2005) Genome sequencing and analysis of Aspergillus oryzae. Nature 438:1157–1161. https://doi.org/10.1038/nature04300
Madadi H, Enkegaard A, Brodsgaard HF, Kharrazi-Pakdel A, Mohaghegh J, Ashouri A (2007) Host plant effects on the functional response of Neoseiulus cucumeris to onion thrips larvae. J Appl Entomol 131:728–733. https://doi.org/10.1111/j.1439-0418.2007.01206.x
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. https://doi.org/10.11158/saa.18.4.1
Messelink GJ, van Holstein-Saj R (2007) Biological control of the bulb scale mite Steneotarsonemus laticeps (Acari: Tarsonemidae) with Neoseiulus barkeri (Acari: Phytoseiidae) in amaryllis. IOBC/WPRS Bull 30:81–85
Midthassel A, Leather SR, Baxter IH (2013) Life table parameters and capture success ratio studies of Typhlodromips swirskii (Acari: Phytoseiidae) to the factitious prey Suidasia medanensis (Acari: Suidasidae). Exp Appl Acarol 61:69–78. https://doi.org/10.1007/s10493-013-9682-x
Moser JC (1985) Use of sporothecae by phoretic Tarsonemus mites to transport ascospores of coniferous bluestain fungi. Trans Br Mycol Soc 84:750–753. https://doi.org/10.1016/S0007-1536(85)80138-8
Naranjo SE, Ellsworth PC, Frisvold GB (2015) Economic value of biological control in integrated pest management of managed plant systems. Annu Rev Entomol 60:621–645. https://doi.org/10.1146/annurev-ento-010814-021005
Nuzacci G, Di Palma A, Magowski WL, Aldini P (2002) Mouthparts of Tarsonemus nodosus Schaarschmidt, 1959 (Acari: Tarsonemidae): fine structure and functional morphology. In: Bernini F, Nannelli R, Nuzzaci G, de Lillo E (eds) Acarid phylogeny and evolution. Adaptations in mites and ticks. Kluwer, Dordrecht
Ochoa R, Naskrecki P, Colwell RK (1995) Excelsotarsonemus kaliszewskii, a new genus and new species from Costa Rica (Acari: Tarsonemidae). Int J Acarol 21:67–74. https://doi.org/10.1080/01647959508684045
O’Donnell K, Cigelnik E, Casper HH (1998) Molecular phylogenetic, morphological, and mycotoxin data support reidentification of the Quorn mycoprotein fungus as Fusarium venenatum. Fungal Genet Biol 23:57–67. https://doi.org/10.1006/fgbi.1997.1018
Parkinson CL, Barron CA, Barker SM, Thomas AC, Armitage DM (1991) Longevity and fecundity of Acarus siro on four field and eight storage fungi. Exp Appl Acarol 11:1–8. https://doi.org/10.1007/BF01193724
R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Ramakers PMJ, Van Lieburg MJ (1982) Start of commercial production and introduction of Amblyseius mckenziei Sch. & Pr. (Acarina: Phytoseiidae) for the control of Thrips tabaci Lind. (Thysanoptera: Thripidae) in glasshouses. Meded Fac Landbouw Rijksuniv Gent 47:541–545
Rodriguez JG, Potts MF, Rodriguez LD (1980) Mycotoxin toxicity to Tyrophagus putrescentiae. J Econ Entomol 73:282–284. https://doi.org/10.1093/jee/73.2.282
Sabelis MW (1990) How to analyse prey preference when prey density varies? A new method to discriminate between effects of gut fullness and prey type composition. Oecologia 82:289–298. https://doi.org/10.1007/BF00317473
Scott JJ, Oh D-C, Yuceer CM, Klepzig KD, Clardy J, Currie R (2008) Bacterial protection of beetle-fungus mutualism. Science 332:63. https://doi.org/10.1126/science.1160423()
Smiley RL, Moser JC (1985) A new species, key to females, and distribution records for Heterotarsonemus (Acari: Tarsonemidae). Int J Acarol 11:247–253. https://doi.org/10.1080/01647958508683425
Sousa ASG, Rezende JM, Lofego AC, Ochoa R, Oliveira AR (2018) Daidalotarsonemus and Excelsotarsonemus species (Acari: Tarsonemidae) found in shaded cacao plantations in Brazil, with a description of a new species. Int J Acarol 44:68–79. https://doi.org/10.1080/01647954.2018.1471096
Suski ZW (1972) Tarsonemid mites on apple trees in Poland X. Laboratory studies on the biology of certain mites species of the family Tarsonemidae (Acarina: Heterostigmata). Zesz Probl Postepow Nauk Roln 129:139–157
Tuovinen T, Lindqvist I (2010) Maintenance of predatory phytoseiid mites for preventive control of strawberry tarsonemid mite Phytonemus pallidus in strawberry plant propagation. Biol Control 54:119–125. https://doi.org/10.1016/j.biocontrol.2010.04.006
Van der Walt L, Spotts RA, Ueckermann EA, Smit FJ, Jensen T, McLeod A (2011) The association of Tarsonemus mites (Acari: Heterostigmata) with different apple developmental stages and apple core rot diseases. Int J Acarol 37:71–84. https://doi.org/10.1080/01647954.2010.539981
van Kleeff BHA, Kuenen JG, Heijnen JJ (1993) Continuous measurement of microbial heat production in laboratory fermentors. Biotechnol Bioeng 41:541–549. https://doi.org/10.1002/bit.260410506
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
Vangansbeke D, Audenaert J, Nguyen DT, Verhoeven R, Gobin B, Tirry L, De Clercq P (2015) Diurnal temperature variations affect development of a herbivorous arthropod pest and its predators. PLoS ONE. https://doi.org/10.1371/journal.pone.0124898
Vangansbeke D, Duarte MVA, Bolckmans K, Guilbaud MHL, Benavente AM, Pekas A, Wackers FL (2020) Mite composition and method for growing mites. WO2020070334A1
White NDG, Sinha RN (1981) Life history and population dynamics of the mycophagous mite Tarsonemus granarius Lindquist (Acarina: Tarsonemidae). Acarologia 22:353–360
Wiebe M (2002) Myco-protein from Fusarium venenatum: a well-established product for human consumption. Appl Microbiol Biotechnol 58:421–427. https://doi.org/10.1007/s00253-002-0931-x
Wilson MT (1999) A model for predicting mould growth and subsequent heat generation in bulk stored grain. J Stored Prod Res 35:1–13. https://doi.org/10.1016/S0022-474X(98)00025-3
Zhang Z-Q (2003) Mites of greenhouses: identification, biology and control. CABI, Wallingford
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 24:1225–1235. https://doi.org/10.11158/saa.24.7.7
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We would like to thank Peggy Bogaerts and Ilse Jacobs for the help with growing the plant material and maintenance of the spider mite production.
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Vangansbeke, D., Duarte, M.V.A., Merckx, J. et al. Impact of a tarsonemid prey mite and its fungal diet on the reproductive performance of a predatory mite. Exp Appl Acarol 83, 313–323 (2021). https://doi.org/10.1007/s10493-021-00594-7
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DOI: https://doi.org/10.1007/s10493-021-00594-7