Skip to main content
Log in

Prey consumption by phytoseiid spider mite predators as affected by diurnal temperature variations

BioControl Aims and scope Submit manuscript

Abstract

The consumption rate of an ectothermic predator is highly temperature-dependent and is a key driver of pest-predator population interactions. Not only average daily temperature, but also diurnal temperature variations may affect prey consumption and life history traits of ectotherms. In the present study, we evaluated the impact of temperature alternations on body size, predation capacity and oviposition rate of the predatory mites Phytoseiulus persimilis Athias-Henriot and Neoseiulus californicus McGregor (Acari: Phytoseiidae) when presented with eggs of their natural prey, the two-spotted spider mite Tetranychus urticae Koch (Acari: Tetranychidae). For both predators, mean daily temperature as well as temperature alternation had a substantial impact on the number of prey consumed. At lower average temperatures, more eggs were killed under an alternating temperature regime (20 °C/5 °C and 25 °C/10 °C) than at the corresponding mean constant temperatures (15 and 20 °C). At higher average temperatures (>25 °C), however, the opposite was observed with higher numbers of prey killed at constant temperatures than at alternating temperatures. At 25 °C, temperature variation had no effect on the predation capacity. A similar trend as for the predation rates was observed for the oviposition rates of the phytoseiids. Body size of N. californicus was affected both by average daily temperature and temperature variation, with smaller adult females emerging at alternating temperatures than at constant temperatures, whereas for P. persimilis, temperature variation had no impact on its body size. Our results demonstrate that temperature variations are likely to affect biological control of T. urticae by the studied phytoseiid predators.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abad-Moyano R, Pina T, Ferragut F, Urbaneja A (2009) Comparative life-history traits of three phytoseiid mites associated with Tetranychus urticae (Acari: Tetranychidae) colonies in clementine orchards in eastern Spain: implications for biological control. Exp Appl Acarol 47:121–132

    Article  PubMed  Google Scholar 

  • Angilletta MJ, Steury TD, Sears MW (2004) Temperature, growth rate, and body size in ectotherms: fitting pieces of a life-history puzzle. Integr Comp Biol 44:498–509

    Article  PubMed  Google Scholar 

  • Atkinson D (1994) Temperature and organism size—a biological law for ectotherms? Adv Ecol Res 25:1–58

    Article  Google Scholar 

  • Audenaert J, Vangansbeke D, Verhoeven R, De Clercq P, Tirry L, Gobin B (2014) Predation efficiency of predatory mites from different climatic origin under variable climates in Belgian greenhouses. IOBC/WPRS Bull 102:7–13

    Google Scholar 

  • Barber A, Campbell C, Crane H, Lilley R, Tregidga E (2003) Biocontrol of two-spotted spider mite Tetranychus urticae on dwarf hops by the phytoseiid mites Phytoseiulus persimilis and Neoseiulus californicus. Biocontrol Sci Technol 13:275–284

    Article  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 

  • Blumel S, Walzer A (2002) Efficacy of different release strategies of Neoseiulus californicus McGregor and Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseiidae) for the control of two-spotted spider mite (Tetranychus urticae Koch) on greenhouse cut roses. Syst Appl Acarol 7:35–48

    Google Scholar 

  • Brakefield PM, Mazzotta V (1995) Matching field and laboratory environments: effects of neglecting daily temperature variation on insect reaction norms. J Evol Biol 8:559–573

    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 

  • Croft BA, Luh HK, Schausberger P (1999) Larval size relative to larval feeding, cannibalism of larvae, egg or adult female size and larval-adult setal patterns among 13 phytoseiid mite species. Exp Appl Acarol 23:599–610

    Article  Google Scholar 

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

    Google Scholar 

  • Estay SA, Lima M, Bozinovic F (2014) The role of temperature variability on insect performance and population dynamics in a warming world. Oikos 123:131–140

    Article  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 

  • Garcia-Ruiz E, Marco V, Perez-Moreno I (2011) Effects of variable and constant temperatures on the embryonic development and survival of a new grape pest, Xylotrechus arvicola (Coleoptera: Cerambycidae). Environ Entomol 40:939–947

    Article  CAS  PubMed  Google Scholar 

  • Gerson U, Weintraub PG (2012) Mites (Acari) as a factor in greenhouse management. Annu Rev Entomol 57:229–247

    Article  CAS  PubMed  Google Scholar 

  • Gotoh T, Kameyama Y (2014) Low temperature induces embryonic diapause in the spider mite, Eotetranychus smithi. J Insect Sci 14(68):1–8

    Article  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 

  • Gotoh T, Saito M, Suzuki A, Nachman G (2014) Effects of constant and variable temperatures on development and reproduction of the two-spotted spider mite Tetranychus urticae (Acari: Tetranychidae). Exp Appl Acarol 64:465–478

    Article  PubMed  Google Scholar 

  • Grbić M, van Leeuwen T, Clark RM, Rombauts S, Rouzé P, Grbić V, Osborne EJ, Dermauw W, Ngoc PCT, Ortego F, Hernández-Crespo P, Diaz I, Martinez M, Navajas M, Sucena E, Magalhães S, Nagy L, Pace RM, Djuranivic S, Smagghe G, Iga M, Christiaens O, Veenstra JA, Ewer J, Villalobos RM, Hutter JL, Hudson SD, Velez M, Yi SV, Zeng J, Pires-daSilva A, Roch F, Cazaux M, Navarro M, Zhurov V, Acevedo G, Bjelica A, Fawcett JA, Bonnet E, Martens C, Baele G, Wissler L, Sanchez-Rodriguez A, Tirry L, Blais C, Demeestere K, Henz SR, Gregory TR, Mathieu J, Verdon L, Farinelli L, Schmutz J, Lindquist E, Feyereisen R, van de Peer Y (2011) The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature 479:487–492

    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

    Article  CAS  PubMed  Google Scholar 

  • Hardman JM, Rogers ML (1991) Effects of temperature and prey density on survival, development, and feeding rates of immature Typhlodromus pyri (Acari: Phytoseiidae). Environ Entomol 20:1089–1096

    Article  Google Scholar 

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

  • Janssen A, Sabelis MW (1992) Phytoseiid life-histories, local predator-prey dynamics, and strategies for control of tetranychid mites. Exp Appl Acarol 14:233–250

    Article  Google Scholar 

  • Jeppson LR, Keifer HH, Baker EW (1975) Mites injurious to economic plants. University of California Press, Berkeley, USA

  • Kim T, Ahn J, Lee JH (2009) Temperature-dependent developmental model of Neoseiulus californicus (McGregor) (Acari: Phytoseiidae). J Appl Entomol 133:284–291

    Article  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 

  • 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

    Article  Google Scholar 

  • Logan JD, Wolesensky W, Joern A (2006) Temperature-dependent phenology and predation in arthropod systems. Ecol Model 196:471–482

    Article  Google Scholar 

  • Messelink GJ, Bennison J, Alomar O, Ingegno BL, Tavella L, Shipp L, Palevsky E, Wäckers FL (2014) Approaches to conserving natural enemy populations in greenhouse crops: current methods and future prospects. BioControl 59:377–393

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Messenger P, Flitters N (1958) Effect of constant temperature environments on the egg stage of three species of Hawaiian fruit flies. Ann Entomol Soc Am 51:109–119

    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  CAS  PubMed  Google Scholar 

  • Montserrat M, Magalhaes S, Sabelis MW, de Roos AM, Janssen A (2012) Invasion success in communities with reciprocal intraguild predation depends on the stage structure of the resident population. Oikos 121:67–76

    Article  Google Scholar 

  • Öhlund G, Hedström P, Norman S, Hein CL, Englund G (2015) Temperature dependence of predation depends on relative performance of predators and prey. Proc R Soc B. doi:10.1098/rspb.2014.2254

    PubMed  Google Scholar 

  • Paaijmans KP, Blanford S, Bell AS, Blanford JI, Read AF, Thomas MB (2010) Influence of climate on malaria transmission depends on daily temperature variation. Proc Natl Acad Sci USA 107:15135–15139

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Paaijmans KP, Heinig RL, Seliga RA, Blanford JI, Blanford S, Murdock CC, Thomas MB (2013) Temperature variation makes ectotherms more sensitive to climate change. Glob Change Biol 19:2373–2380

    Article  Google Scholar 

  • Polis GA, Myers CA, Holt RD (1989) The ecology and evolution of intraguild predation: potential competitors that eat each other. Ann Rev Ecol Syst 20:297–330

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Rhodes EM, Liburd OE, Kelts C, Rondon SI, Francis RR (2006) Comparison of single and combination treatments of Phytoseiulus persimilis, Neoseiulus californicus, and Acramite (bifenazate) for control of twospotted spider mites in strawberries. Exp Appl Acarol 39:213–225

    Article  CAS  PubMed  Google Scholar 

  • Ruel JJ, Ayres MP (1999) Jensen’s inequality predicts effects of environmental variation. Trends Ecol Evol 14:361–366

    Article  PubMed  Google Scholar 

  • Sabelis MW (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

    Google Scholar 

  • Schausberger P (1999) Predation preference of Typhlodromus pyri and Kampimodromus aberrans (Acari: Phytoseiidae) when offered con-and heterospecific immature life stages. Exp Appl Acarol 23:389–398

    Article  Google Scholar 

  • Schausberger P, Walzer A (2001) Combined versus single species release of predaceous mites: predator–predator interactions and pest suppression. Biol Control 20:269–278

    Article  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 

  • Skirvin DJ, Fenlon JS (2003) The effect of temperature on the functional response of Phytoseiulus persimilis (Acari: Phytoseiidae). Exp Appl Acarol 31:37–49

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Terblanche JS, Nyamukondiwa C, Kleynhans E (2010) Thermal variability alters climatic stress resistance and plastic responses in a globally invasive pest, the Mediterranean fruit fly (Ceratitis capitata). Entomol Exp Appl 137:304–315

    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 

  • Upton MS (1993) Aqueous gum-chloral slide mounting media: an historical review. Bull Entomol Res 83:267–274

    Article  Google Scholar 

  • van Leeuwen T, Tirry L, Yamamoto A, Nauen R, Dermauw W (2015) The economic importance of acaricides in the control of phytophagous mites and an update on recent acaricide mode of action research. Pestic Biochem Phys. doi:10.1016/j.pestbp.2014.12.009

    Google Scholar 

  • van Lenteren JC (2000) A greenhouse without pesticides: fact or fantasy? Crop Prot 19:375–384

    Article  Google Scholar 

  • Vangansbeke D, De Schrijver L, Spranghers T, Audenaert J, Verhoeven R, Nguyen DT, Gobin B, Tirry L, De Clercq P (2013) 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

    Article  PubMed  Google Scholar 

  • Walzer A, Schausberger P (1999) Cannibalism and interspecific predation in the phytoseiid mites Phytoseiulus persimilis and Neoseiulus californicus: predation rates and effects on reproduction and juvenile development. BioControl 43:457–468

    Article  Google Scholar 

  • Walzer A, Schausberger P (2011) Threat-sensitive anti-intraguild predation behaviour: maternal strategies to reduce offspring predation risk in mites. Anim Behav 81:177–184

    Article  PubMed Central  PubMed  Google Scholar 

  • Walzer A, Schausberger P (2013) Intra-and trans-generational costs of reduced female body size caused by food limitation early in life in mites. PLoS ONE 8:e79089

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Weintraub P, Palevsky E (2008) Evaluation of the predatory mite, Neoseiulus californicus, for spider mite control on greenhouse sweet pepper under hot arid field conditions. Exp Appl Acarol 45:29–37

    Article  CAS  PubMed  Google Scholar 

  • Wilhoit L, Stinner R, Axtell R (1991) CARMOD: a simulation model for Carcinops pumilio (Coleoptera: Histeridae) population dynamics and predation on immature stages of house flies (Diptera: Muscidae). Environ Entomol 20:1079–1088

    Article  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

    Article  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 Dominiek Vangansbeke.

Additional information

Handling Editor: Marta Montserrat.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vangansbeke, D., Nguyen, D.T., Audenaert, J. et al. Prey consumption by phytoseiid spider mite predators as affected by diurnal temperature variations. BioControl 60, 595–603 (2015). https://doi.org/10.1007/s10526-015-9677-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-015-9677-0

Keywords

Navigation