Skip to main content
Log in

Alternating temperatures affect life table parameters of Phytoseiulus persimilis, Neoseiulus californicus (Acari: Phytoseiidae) and their prey Tetranychus urticae (Acari: Tetranychidae)

  • Published:
Experimental and Applied Acarology Aims and scope Submit manuscript

Abstract

Increasing energy costs force glasshouse growers to switch to energy saving strategies. In the temperature integration approach, considerable daily temperature variations are allowed, which not only have an important influence on plant growth but also on the development rate of arthropods in the crop. Therefore, we examined the influence of two constant temperature regimes (15 °C/15 °C and 20 °C/20 °C) and one alternating temperature regime (20 °C/5 °C, with an average of 15 °C) on life table parameters of Phytoseiulus persimilis and Neoseiulus californicus and their target pest, the two-spotted spider mite Tetranychus urticae at a 16:8 (L:D) h photoperiod and 65 ± 5 % RH. For females of both predatory mites the alternating temperature regime resulted in a 25–30 % shorter developmental time as compared to the corresponding mean constant temperature regime of 15 °C/15 °C. The immature development of female spider mites was prolonged for 7 days at 15 °C/15 °C as compared to 20 °C/5 °C. With a daytime temperature of 20 °C, no differences in lifetime fecundity were observed between a nighttime temperature of 20 and 5 °C for P. persimilis and T. urticae. The two latter species did show a higher lifetime fecundity at 20 °C/5 °C than at 15 °C/15 °C, and their daily fecundity at the alternating regime was about 30 % higher than at the corresponding mean constant temperature. P. persimilis and T. urticae showed no differences in sex ratio between the three temperature regimes, whereas the proportion of N. californicus females at 15 °C/15 °C (54.2 %) was significantly lower than that at 20 °C/5 °C (69.4 %) and 20 °C/20 °C (67.2 %). Intrinsic rates of increase were higher at the alternating temperature than at the corresponding mean constant temperature for both pest and predators. Our results indicate that thermal responses of the studied phytoseiid predators to alternating temperature regimes used in energy saving strategies in glasshouse crops may have consequences for their efficacy in biological control programs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Adams S, Valdes V, Fuller D (2009) The effects of day and night temperature on Chrysanthemum morifolium: investigating the safe limits for temperature integration. J Hortic Sci Biotech 84:604–608

    Google Scholar 

  • Bakker J (2009) Energy saving greenhouses. Chron Hort 49:19–23

    Google Scholar 

  • Beck S (1983) Thermal and thermoperiodic effects on larval development and diapause in the European corn borer, Ostrinia nubilalis. J Insect Physiol 29:107–112

    Article  Google Scholar 

  • Behrens W, Hoffmann K, Kempa S, Gäßler S, Merkel-Wallner G (1983) Effects of diurnal thermoperiods and quickly oscillating temperatures on the development and reproduction of crickets, Gryllus bimaculatus. Oecologia 59:279–287

    Article  Google Scholar 

  • Birch L (1948) The intrinsic rate of natural increase of an insect population. J Anim Ecol 17:15–26

    Article  Google Scholar 

  • Boudreaux H (1958) The effect of relative humidity on egg-laying, hatching, and survival in various spider mites. J Insect Physiol 2:65–72

    Article  Google Scholar 

  • Bounfour M, Tanigoshi L (2001) Effect of temperature on development and demographic parameters of Tetranychus urticae and Eotetranychus carpini borealis (Acari: Tetranychidae). Ann Entomol Soc Am 94:400–404

    Article  Google Scholar 

  • Bryant S, Bale J, Thomas C (1999) Comparison of development and growth of nettle-feeding larvae of Nymphalidae (Lepidoptera) under constant and alternating temperature regimes. Eur J Entomol 96:143–148

    Google Scholar 

  • Buwalda F, Eveleens B, Wertwijn R (2000) Ornamental crops tolerate large temperature fluctuations: a potential for more efficient greenhouse heating strategies. Acta Hort 515:141–149

    Google Scholar 

  • Castagnoli M, Simoni S (1999) Effect of long-term feeding history on functional and numerical response of Neoseiulus californicus (Acari : Phytoseiidae). Exp Appl Acarol 23:217–234

    Article  Google Scholar 

  • Cranham J, Helle W (1985) Pesticide resistance in Tetranychidae. Spider Mites Biol Nat Enemies Control 1:405–421

    Google Scholar 

  • Davies JT, Ireson JE, Allen GR (2009) Pre-adult development of Phytoseiulus persimilis on diets of Tetranychus urticae and Tetranychus lintearius: implications for the biological control of Ulex europaeus. Exp Appl Acarol 47:133–145

    Article  PubMed  Google Scholar 

  • Davis J, Radcliffe E, Ragsdale D (2006) Effects of high and fluctuating temperatures on Myzus persicae (Hemiptera: Aphididae). Environ Entomol 35:1461–1468

    Article  Google Scholar 

  • de Vis RMJ, de Moraes GJ, Bellini MR (2006) Effect of air humidity on the egg viability of predatory mites (Acari: Phytoseiidae, Stigmaeidae) common on rubber trees in Brazil. Exp Appl Acarol 38:25–32

    Article  PubMed  Google Scholar 

  • Dieleman J, Meinen E, Dueck TA (2005) Effects of temperature integration on growth and development of roses. Acta Hort 691:51–58

    Google Scholar 

  • Erwin JE, Heins RD, Karlsson MG (1989) Thermomorphogenesis in Lilium longiflorum. Am J Bot 76:47–52

    Article  Google Scholar 

  • Eubank W, Atmar J, Ellington J (1973) The significance and thermodynamics of fluctuating versus static thermal environments on Heliothis zea egg development rates. Environ Entomol 2:491–496

    Google Scholar 

  • Fantinou AA, Perdikis DC, Chatzoglou CS (2003) Development of immature stages of Sesamia nonagrioides (Lepidoptera: Noctuidae) under alternating and constant temperatures. Environ Entomol 32:1337–1342

    Article  Google Scholar 

  • Gotoh T, Tsuchiya A (2008) Effect of multiple mating on reproduction and longevity of the phytoseiid mite Neoseiulus californicus. Exp Appl Acarol 44:185–197

    Article  PubMed  Google Scholar 

  • Gotoh T, Yamaguchi K, Mori K (2004) Effect of temperature on life history of the predatory mite Amblyseius (Neoseiulus) californicus (Acari : Phytoseiidae). Exp Appl Acarol 32:15–30

    Article  PubMed  Google Scholar 

  • Hagstrum DW, Hagstrum WR (1970) A simple device for producing fluctuating temperatures, with an evaluation of the ecological significance of fluctuating temperatures. Ann Entomol Soc Am 63:1385–1389

    PubMed  CAS  Google Scholar 

  • Hagstrum DW, Leach CE (1973) Role of constant and fluctuating temperatures in determining development time and fecundity of three species of stored-products Coleoptera. Ann Entomol Soc Am 66:407–410

    Google Scholar 

  • Hagstrum DW, Milliken GA (1991) Modeling differences in insect developmental times between constant and fluctuating temperatures. Ann Entomol Soc Am 84:369–379

    Google Scholar 

  • Hart A, Bale J, Tullett A, Worland M, Walters K (2002) Effects of temperature on the establishment potential of the predatory mite Amblyseius californicus McGregor (Acari: Phytoseiidae) in the UK. J Insect Physiol 48:593–599

    Article  PubMed  CAS  Google Scholar 

  • Helle W (1967) Fertilization in the two-spotted spider mite (Tetranychus urticae: Acari). Entomol Exp Appl 10:103–110

    Article  Google Scholar 

  • Helle W, Sabelis MW (1985) Spider mites: their biology, natural enemies and control. Elsevier, The Netherlands, p 458

    Google Scholar 

  • Hulting FL, Orr DB, Obrycki JJ (1990) A computer program for calculation and statistical comparison of intrinsic rates of increase and associated life table parameters. Fla Entomol 73:601–612

    Article  Google Scholar 

  • Humpesch UH (1982) Effect of fluctuating temperature on the duration of embryonic development in 2 Ecdyonurus Spp. and Rhithrogena Cf. hybrida (Ephemeroptera) from Austrian streams. Oecologia 55:285–288

    Article  Google Scholar 

  • Khayat E, Zieslin N, Mortensen L, Moe R (1988) Effect of alternating temperature on dark respiration and C14 export in rose plants. J Plant Physiol 133:199–202

    Article  CAS  Google Scholar 

  • Körner O, Challa H (2003) Design for an improved temperature integration concept in greenhouse cultivation. Comput Electron Agric 39:39–59

    Article  Google Scholar 

  • Körner O, Challa H (2004) Temperature integration and process-based humidity control in chrysanthemum. Comput Electron Agric 43:1–21

    Article  Google Scholar 

  • Kumari M, Sadana G (1991) Influence of temperature and relative humidity on the development of Amblyseius alstoniae (Acari: Phytoseiidae). Exp Appl Acarol 11:199–203

    Article  Google Scholar 

  • Kutner M, Nachtsheim C, Neter J, Li W (2005) Applied linear statistical models. McGraw-Hill, New York, p 1396

    Google Scholar 

  • Lamb K (1961) Some effects of fluctuating temperatures on metabolism, development, and rate of population growth in the cabbage aphid, Brevicoryne brassicae. Ecology 42:740–745

    Article  Google Scholar 

  • Lewontin RC (1965) Selection for colonizing ability. In: Baker HG, Stebbins GL et al (eds) The genetics of colonizing species. Academic Press, New York, p 588

    Google Scholar 

  • Liu SS, Zhang GM, Zhu J (1995) Influence of temperature variations on rate of development in insects: analysis of case studies from entomological literature. Ann Entomol Soc Am 88:107–119

    Google Scholar 

  • Maia AHN, Luiz AJB, Campanhola C (2000) Statistical inference on associated fertility life parameters using jackknife technique: computational aspects. J Econ Entomol 93:511–518

    Article  Google Scholar 

  • Margolies DC, Wrensch DL (1996) Temperature-induced changes in spider mite fitness: offsetting effects of development time, fecundity, and sex ratio. Entomol Exp Appl 78:111–118

    Article  Google Scholar 

  • McCullagh P, Nelder JA (1989) Generalized linear models. Chapman & Hall, New York, p 511

    Google Scholar 

  • McMurtry JA, Croft BA (1997) Life-styles of phytoseiid mites and their role in biological control. Annu Rev Entomol 42:291–321

    Article  PubMed  CAS  Google Scholar 

  • Meijón M, Feito I, Valledor L, Rodríguez R, Cañal MJ (2011) Promotion of flowering in azaleas by manipulating photoperiod and temperature induces epigenetic alterations during floral transition. Physiol Plantarum 143:82–92

    Article  Google Scholar 

  • Messenger PS (1964) Influence of rhythmically fluctuating temperatures on development + reproduction of spotted alfalfa aphid Therioaphis maculata. J Econ Entomol 57:71–76

    Google Scholar 

  • Messenger P, Flitters N (1959) Effect of variable temperature environments on egg development of three species of fruit flies. Ann Entomol Soc Am 52:191–204

    Google Scholar 

  • Meyer JS, Ingersoll CG, McDonald LL, Boyce MS (1986) Estimating uncertainty in population growth rates: jackknife vs. bootstrap techniques. Ecology 67:1156–1166

    Article  Google Scholar 

  • Mironidis G, Savopoulou-Soultani M (2008) Development, survivorship, and reproduction of Helicoverpa armigera (Lepidoptera: Noctuidae) under constant and alternating temperatures. Environ Entomol 37:16–28

    Article  PubMed  CAS  Google Scholar 

  • Nomikou M, Janssen A, Schraag R, Sabelis M (2001) Phytoseiid predators as potential biological control agents for Bemisia tabaci. Exp Appl Acarol 25:271–291

    Article  PubMed  CAS  Google Scholar 

  • Park HH, Shipp L, Buitenhuis R, Ahn JJ (2011) Life history parameters of a commercially available Amblyseius swirskii (Acari: Phytoseiidae) fed on cattail (Typha latifolia) pollen and tomato russet mite (Aculops lycopersici). J Asia Pac Entomol 14:497–501

    Article  Google Scholar 

  • Pemberton H, Wilkins H (1985) Seasonal variation on the influence of low temperature, photoperiod, light source, and GA in floral development of the evergreen azalea. J Am Soc Hortic Sci 110:730–737

    CAS  Google Scholar 

  • Pollet B, Steppe K, Dambre P, Van Labeke MC, Lemeur R (2009) Temperature integration of Hedera helix L.: quality aspects and growth response. Sci Hort 120:89–95

    Article  Google Scholar 

  • Potter DA, Wrensch DL (1978) Interrupted matings and the effectiveness of second inseminations in the twospotted spider mite. Ann Entomol Soc Am 71:882–885

    Google Scholar 

  • Ratte H (1985) Temperature and insect development. In: Hoffmann KH (ed) Environmental physiology and biochemistry of insects. Springer, New York, p 296

    Google Scholar 

  • Richards AG, Suanraksa S (1962) Energy expenditure during embryonic development under constant versus variable temperatures (Oncopeltus fasciatus (Dallas)) 1. Entomol Exp Appl 5:167–178

    Article  Google Scholar 

  • Rijsdijk A, Vogelezang J (2000) Temperature integration on a 24-hour base: a more efficient climate control strategy. Acta Hort 515:141–149

    Google Scholar 

  • Sabelis M (1981) Biological control of two-spotted spider mites using phytoseiid predators. Part 1. Modelling the predator-prey interaction at the individual level. Pudoc., Wageningen, The Netherlands, p 242

    Google Scholar 

  • Shih CT, Poe SL, Cromroy HL (1976) Biology, life table, and intrinsic rate of increase of Tetranychus urticae. Ann Entomol Soc Am 69:362–364

    Google Scholar 

  • Shipp J, Ward K, Gillespie T (1996) Influence of temperature and vapor pressure deficit on the rate of predation by the predatory mite, Amblyseius cucumeris, on Frankliniella occidentalis. Entomol Exp Appl 78:31–38

    Article  Google Scholar 

  • Siddiqui W, Barlow C, Randolph P (1973) Effects of some constant and alternating temperatures on population growth of the pea aphid, Acyrthosiphon pisum (Homoptera: Aphididae). Can Entomol 105:145–156

    Article  Google Scholar 

  • Stavrinides MC, Mills NJ (2011) Influence of temperature on the reproductive and demographic parameters of two spider mite pests of vineyards and their natural predator. Biocontrol 56:315–325

    Article  Google Scholar 

  • Stenseth C (1979) Effect of temperature and humidity on the development of Phytoseiulus persimilis and its ability to regulate populations of Tetranychus urticae [Acarina, Phytoseiidae, Tetranychidae]. Entomophaga 24:311–317

    Article  Google Scholar 

  • Tanigoshi L, Browne R, Hoyt S, Lagier R (1976) Empirical analysis of variable temperature regimes on life stage development and population growth of Tetranychus mcdanieli (Acarina: Tetranychidae). Ann Entomol Soc Am 69:712–716

    Google Scholar 

  • Tantau HJ (1998) Energy saving potential of greenhouse climate control. Math Comput Simulat 48:93–101

    Article  Google Scholar 

  • Toyoshima S, Amano H (1998) Effect of prey density on sex ratio of two predacious mites, Phytoseiulus persimilis and Amblyseius womersleyi (Acari: Phytoseiidae). Exp Appl Acarol 22:709–723

    Article  Google Scholar 

  • van der Ploeg A, Heuvelink E (2005) Influence of sub-optimal temperature on tomato growth and yield. J Hortic Sci Biotech 80:652–659

    Google Scholar 

  • van der Ploeg A, Carvalho SMP, Heuvelink E (2009) Genotypic variation in the response to suboptimal temperature at different plant densities in cut chrysanthemum. J Am Soc Hortic Sci 134:31–40

    Google Scholar 

  • van Houten YM, van Rijn PCJ, Tanigoshi LK, van Stratum P, Bruin J (1995) Preselection of predatory mites to improve year-round biological control of western flower thrips in greenhouse crops. Entomol Exp Appl 74:225–234

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Worner SP (1992) Performance of phenological models under variable temperature regimes: consequences of the Kaufmann or rate summation effect. Environ Entomol 21:689–699

    Google Scholar 

Download references

Acknowledgments

This research was supported by project number 090931 from the Institute for the Promotion of Innovation through Science and Technology in Flanders (IWT-Vlaanderen).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Patrick De Clercq.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vangansbeke, D., De Schrijver, L., Spranghers, T. et al. Alternating temperatures affect life table parameters of Phytoseiulus persimilis, Neoseiulus californicus (Acari: Phytoseiidae) and their prey Tetranychus urticae (Acari: Tetranychidae). Exp Appl Acarol 61, 285–298 (2013). https://doi.org/10.1007/s10493-013-9704-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10493-013-9704-8

Keywords

Navigation