Experimental and Applied Acarology

, Volume 76, Issue 3, pp 311–323 | Cite as

Overwintering of the Argentine strain of Neoseiulus californicus (Acari: Phytoseiidae)

  • María Fernanda Gugole Ottaviano
  • Mariángeles Alonso
  • Claudia Cédola
  • Mariana Pascua
  • Martha Roggiero
  • Nancy GrecoEmail author


Overwintering and diapause are variable among mite species and strains. The aims of this study were to determine whether certain crops constitute overwintering sites for the Argentine strain of the predator Neoseiulus californicus and whether females underwent reproductive diapause in winter. Neoseiulus californicus was recorded monthly on the vegetables tomato, sweet pepper, eggplant, and artichoke, and on strawberry, among other crops in Buenos Aires province, Argentina. This mite was found at a lower percentage of crops in the winter than in the other seasons. Since the predator was quite frequent on artichoke, this crop could constitute a refuge during adverse environmental conditions. The mite’s frequency on several crops in other seasons and potential association with a strawberry pest is discussed. In the laboratory, individuals exposed to winter conditions throughout the life cycle exhibited a long pre-oviposition period and low oviposition rate, but did not diapause. After being kept under winter conditions from larva to adult, when individuals were transferred to the optimal spring temperatures and lighting, the pre-oviposition period was shorter and the fecundity higher than under winter conditions. When individuals remained under spring conditions from larva to adult and were then transferred to the winter parameters during the first 15 days of adulthood, the pre-oviposition period was long and the oviposition rate low. Once the optimal conditions were restored, the daily fecundity became similar to that of the individuals remaining under optimal conditions throughout the life cycle. Fecundity of N. californicus decreased significantly under winter conditions but reproductive diapause was not observed.


Neoseiulus californicus Overwintering Diapause Horticultural crops 



This study was supported by the Agencia Nacional de Promoción Científica y Tecnológica de Argentina (the National Agency for Promotion of Science and Technology of Argentina), grant PICT 2015-1427 and the Program of Incentives for Professors-Researchers of the National Ministry of Culture and Education of Argentina, grants N712 and N834. Dr. Donald F. Haggerty is acknowledged for editing a draft version of the manuscript. We thank Graciela Minardi for help with the statistical analyses and María Laura Morote for help with the figures.


  1. Bruce-Oliver SM, Yaninek JS, Hoy MA (1995) Photoperiod and temperature studies to determine whether diapause is found in successive generations of the African phytoseiid, Euseius fustis (Pritchard and Baker) (Acari: Phytoseiidae). Exp Appl Acarol 19:465–472Google Scholar
  2. Castagnoli M, Simoni S (1999) Effect of long-term feeding history on functional and numerical response of Neoseiulus californicus (Acari: Phytoseiidae). Exp Appl Acarol 23:217–234CrossRefGoogle Scholar
  3. Castagnoli M, Simoni S (2003) Neoseiulus californicus (McGregor) (Acari: Phytoseiidae): survey of biological and behavioral traits of a versatile predator. Redia 86:153–164Google Scholar
  4. Castagnoli M, Liguori M, Simoni S, Pintucci M, Guidi S, Falchini L (1996) Observations on diapause induction in three phytoseiid (Phytoseiidae) species. In: Mitchell R, Horn DJ, Needham GR, Welboum WC (eds) Acarology IX proceedings. Ohio Biological Survey, Columbus, pp 9–12Google Scholar
  5. Chant DA (1959) Phytoseiid mites (Acarina: Phytoseiidae). Part I. Bionomics of seven species in southeastern England. Can Entomol 91(Suppl 12):1–44Google Scholar
  6. Coombs MR, Bale JS (2014) Thermal biology of the spider mite predator Phytoseiulus macropilis. Biocontrol 59(2):205–217CrossRefGoogle Scholar
  7. El Taj HF, Jung C (2011) A Korean population of Neoseiulus californicus (McGregor) (Acari: Phytoseiidae) that is non-diapausing. Int J Acarol 37(5):411–419CrossRefGoogle Scholar
  8. Escudero LA, Ferragut F (1999) Abundancia y dinámica estacional de las poblaciones de fitoseidos en los cultivos hortícolas valencianos (Acari: Tetranychidae, Phytoseiidae). Bol Sanid Veg Plagas 25:347–362Google Scholar
  9. Escudero LA, Ferragut F (2005) Life-history of predatory mites Neoseiulus californicus and Phytoseiulus persimilis (Acari: Phytoseiidae) on four spider mite species as prey, with special reference to Tetranychus evansi (Acari: Tetranychidae). Biol Control 32:378–384CrossRefGoogle Scholar
  10. Fitzgerald J, Solomon MG (1991) Diapause induction and duration in the phytoseiidae Tryplodromus pyri. Exp Appl Acarol 12:135–145CrossRefGoogle Scholar
  11. Fraulo AB, Liburd OE (2007) Biological control of twospotted spider mite, Tetranychus urticae, with predatory mite, Neoseiulus californicus, in strawberries. Exp Appl Acarol 43:109–119CrossRefGoogle Scholar
  12. Gotoh T, Akizawa T, Watanave M, Tsuchiya A, Shimazaki S (2005) Cold hardiness of Neoseiulus californicus and N. womersleyi (Acari: Phytoseiidae). J Acarol Soc Jpn 14:93–103CrossRefGoogle Scholar
  13. Greco N, Liljesthröm G, Sánchez N (1999) Spatial distribution and coincidence of Neoseiulus californicus and Tetranychus urticae (Acari: Phytoseiidae, Tetranychidae) on strawberry. Exp Appl Acarol 23:567–580CrossRefGoogle Scholar
  14. Greco NM, Sánchez NE, Liljesthröm GG (2005) Neoseiulus californicus (Acari: Phytoseiidae) as a potential control agent of Tetranychus urticae (Acari: Tetranychidae): effect of pest/predator ratio on the pest abundance on strawberry. Exp Appl Acarol 37:57–66CrossRefGoogle Scholar
  15. Greco NM, Liljesthröm GG, Cédola CV, Roggiero MF (2006) Effect of prey deprivation on survival and reproduction of Neoseiulus californicus (Acari: Phytoseiidae) females. Acarologia 46:13–19Google Scholar
  16. Greco NM, Liljesthröm GG, Gugole Ottaviano MF, Cingolani MF, Cluigt N, Sánchez NE (2011) Pest management plan for the two-spotted spider mite, Tetranychus urticae, based on the natural occurrence of the predator y mite Neoseiulus californicus in strawberries. Int J Pest Manag 57:299–308CrossRefGoogle Scholar
  17. Guanilo AD, De Moraes GJ, Toledo S, Knapp M (2008) Phytoseiid mites (Acari: Phytoseiidae) from Argentina, with description of a new species. Zootaxa 1884:1–35Google Scholar
  18. Gugole Ottaviano MF (2012) Manejo Integrado de la plaga Tetranychus urticae (Acari: Tetranychidae) en cultivos de frutilla del Cinturón Hortícola Platense. Ph.D. thesis, Universidad Nacional de La Plata, p 198Google Scholar
  19. Gugole Ottaviano MF, Cédola CV, Sánchez NE, Greco NM (2015) Conservation biological control in strawberry: effect of different pollen on development, survival, and reproduction of Neoseiulus californicus (Acari: Phytoseiidae). Exp Appl Acarol 67:507–521CrossRefGoogle Scholar
  20. Hart AJ, Bale JS, Tullett AG, Worland MR, Walter K (2002) Effects of temperature on the establishment potential of the predatory mite Amblyseius californicus McGregor (Acari: Phytoseiidae) in the UK. J Insect Physiol 48:593–599CrossRefGoogle Scholar
  21. Jolly R (2001) The status of the predatory mite Neoseiulus californicus (McGregor) (Acari: Phytoseiidae) in the UK, and its potential as a biocontrol agent of Panonychus ulmi (Koch) (Acari: Tetranychidae). Ph.D. thesis. University of Birmingham, p 173Google Scholar
  22. Jung C, Croft BA (2000) Survival and plant-prey finding by Neoseiulus fallacis (Acari: Phytoseiidae) on soil substrates after aerial dispersal. Exp Appl Acarol 24:579–596CrossRefGoogle Scholar
  23. Kawashima M, Jung C (2010) Overwintering sites of the predacious mite Neoseiulus californicus (McGregor) (Acari: Phytoseiidae) in satsuma mandarin orchards on Jeju Island, Korea. Appl Entomol Zool 45:191–199CrossRefGoogle Scholar
  24. Kawashima M, Jung C (2011) Effects of sheltered ground habitats on the overwintering potential of the predacious mite Neoseiulus californicus (Acari: Phytoseiidae) in apple orchards on mainland Korea. Exp Appl Acarol 55:375–388CrossRefGoogle Scholar
  25. Kiritani K (2006) Predicting impacts of global warming on population dynamics and distribution of arthropods in Japan. Popul Ecol 48:5–12CrossRefGoogle Scholar
  26. Kishimoto H, Takafuji A (1994) Variations in the diapause characteristics of Amblyseius womersleyi Schicha (Acari: Phytoseiidae). J Acarol Soc Jpn 3:59–67CrossRefGoogle Scholar
  27. Landis DA, Wratten SD, Gurr GM (2000) Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu Rev Entomol 45:175–201CrossRefGoogle Scholar
  28. McMurtry JA, Flaherty DL (1977) An ecological study of phytoseiid and tetranychid mites on walnut in Tulare County, California. Environ Entomol 6:287–292CrossRefGoogle Scholar
  29. McMurtry JA, Mahr DL, Johnson HG (1976) Geographic races in the predaceous mite, Amblyseius potentillae (Acari: Phytoseiidae). Int J Acarol 2:23–48CrossRefGoogle Scholar
  30. Morewood W (1993) Diapause and cold hardiness of phytoseiid mites (Acarina: Phytoseiidae). Eur J Entomol 90:3–10Google Scholar
  31. Mori H, Saito Y (1979) Biological control of Tetranychus urticae Koch (Acarina: Tetranychidae) populations by the three species of phytoseiid mites (Acarina: Phytoseiidae). J Fac Agric Hokkaido Univ 59:303–311Google Scholar
  32. Nyrop JP, Minns JC, Herring CP (1994) Influence of ground cover on dynamics of Amblyseius fallacis Garman (Acarina; Phytoseiidae) in New York apple orchards. Agric Ecosyst Environ 50:61–72CrossRefGoogle Scholar
  33. Overmeer WPJ (1985) Diapause. In: Helle W, Sabelis MW (eds) Spider mites, their biology, natural enemies and control, vol B. Elsevier, Amsterdam, pp 95–102Google Scholar
  34. Pielou EC (1984) The interpretation of ecological data. A primer on classification and ordination. Wiley, HobokenGoogle Scholar
  35. Putman WL (1959) Hibernation sites of phytoseiids (Acarina: Phytoseiidae) in Ontario peach orchards. Can Entomol 91:735–741CrossRefGoogle Scholar
  36. Raworth DA, Fauvel G, Auger P (1994) Location, reproduction and movement of Neoseiulus californicus (Acari: Phytoseiidae) during autumn, winter and spring in orchards in the south of France. Exp Appl Acarol 18:593–602CrossRefGoogle Scholar
  37. van Houten YM (1989) Photoperiodic control of adult diapause in the predacious mite, Amblyseius potentillae: repeated diapause induction and termination. Physiol Entomol 14:341–348CrossRefGoogle Scholar
  38. van Houten YM, Veerman A (1990) Photoperiodism and thermoperiodism in the predatory mite Amblyseius potentillae are probably based on the same mechanism. J Comp Physiol A 167:201–209CrossRefGoogle Scholar
  39. van Lenteren JC (2012) The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. Biocontrol 57:1–20CrossRefGoogle Scholar
  40. Veerman A (1992) Diapause in phytoseiid mites: a review. Exp Appl Acarol 14:1–60CrossRefGoogle Scholar
  41. Wysoki M, Swirski E (1971) Studies on overwintering of predacious mites of the genera Seiulus Berlese and Phytoseius Ribaga in Israel (Acarina, Phytoseiidae). Israel J Entomol 6:55–70Google Scholar
  42. Zar HJ (1996) Biostatistical analysis. Prentice-Hall, New JerseyGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Departamento de Evaluación Sensorial de Alimentos (DESA–ISETA)Buenos AiresArgentina
  2. 2.Centro de Estudios Parasitológicos y de Vectores (CEPAVE), Facultad de Ciencias Naturales y MuseoUNLP, CONICETLa PlataArgentina
  3. 3.Comisión de Investigaciones Científicas de la Provincia de Buenos AiresLa PlataArgentina

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