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Diapause and winter survival of two Orius species from southern Africa

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Abstract

The cold hardiness and overwintering potential of the southern African pirate bugs, Orius thripoborus (Hesse) and Orius naivashae (Poppius) (Hemiptera: Anthocoridae), were assessed in the laboratory. Diapause traits were studied by observing nymphal development and reproductive performance of adults at 18 °C and three photoperiods (10:14, 12:12 and 14:10 (L:D) h). A 12 h light regime was also tested at 23 °C. A 12 h photoperiod and 18 °C induced reproductive diapause in 84 and 42 % of O. naivashae and O. thripoborus females, respectively. Cold tolerance of adults was measured by determining the supercooling point (SCP, the temperature at which the insect’s body fluids freeze) and lethal time (LT50, the time required to kill 50 % of the population) at 0 and 5 °C. All observed SCPs ranged from −21 to −17 °C. Significantly lower SCP values were observed for acclimated (seven days at 10 °C) O. naivashae females. LT50-values averaged 6.4 and 4.4 days at 0 °C and 11.6 and 7.8 days at 5 °C, for adults of O. thripoborus and O. naivashae, respectively. The findings indicate that O. naivashae is less cold tolerant and has a higher diapause incidence compared with O. thripoborus. Therefore, the latter species may have better potential for use in biological control programmes in the cooler regions of southern Africa or elsewhere.

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References

  • Allen CM (2010) Thermal biology and behaviour of two predatory Phytoseiid mites: Amblyseius swirskii (Athias-Henriot) (Acari: Phytoseiidae) and Phytoseiulus longipes (Evans) (Acari: Phytoseiidae). Doctoral dissertation, University of Birmingham

  • Bale JS (1993) Classes of insect cold hardiness. Funct Ecol 7:751–753

    Google Scholar 

  • Bale JS (1996) Insect cold hardiness: a matter of life and death. Eur J Entomol 93:369–382

    Google Scholar 

  • Bale JS, Hayward SAL (2010) Insect overwintering in a changing climate. J Exp Biol 213:980–994

    Article  CAS  PubMed  Google Scholar 

  • Bale JS, Harrington R, Clough MS (1988) Low temperature mortality of the peach-potato aphid Myzus persicae. Ecol Entomol 13:121–129

    Article  Google Scholar 

  • Beck SD (1980) Insect photoperiodism, 2nd edn. Academic Press, New York

    Google Scholar 

  • Bennett LE, Lee RE (1989) Simulated winter to summer transition in diapausing adults of the lady beetle (Hippodamia convergens): supercooling point is not indicative of cold-hardiness. Physiol Entomol 14:361–367

    Article  Google Scholar 

  • Berkvens N, Bale JS, Berkvens D, Tirry L, De Clercq P (2010) Cold tolerance of the harlequin ladybird Harmonia axyridis in Europe. J Insect Physiol 56:438–444

    Article  CAS  PubMed  Google Scholar 

  • Bonte M, De Clercq P (2011) Influence of predator density, diet and living substrate on developmental fitness of Orius laevigatus. J Appl Entomol 135:343–350

    Article  Google Scholar 

  • Bonte J, De Ro M, Conlong D, De Clercq P (2012a) Thermal biology of the predatory bugs Orius thripoborus and O. naivashae (Hemiptera: Anthocoridae). Environ Entomol 41:989–996

    Article  Google Scholar 

  • Bonte J, Vangansbeke D, Maes S, Bonte M, Conlong D, De Clercq P (2012b) Moisture source and diet affect development and reproduction of Orius thripoborus and Orius naivashae, two predatory anthocorids from southern Africa. J Insect Sci 12:1–16

    Article  PubMed  PubMed Central  Google Scholar 

  • Bonte J, De Hauwere L, Conlong D, De Clercq P (2015) Predation capacity, development and reproduction of the southern African flower bugs Orius thripoborus and Orius naivashae (Hemiptera: Anthocoridae) on various prey. Biol Control 86:52–59

    Article  Google Scholar 

  • Bowler K, Terblanche JS (2008) Insect thermal tolerance: what is the role of ontogeny, ageing and senescence? Biol Rev 83:339–355

    Article  PubMed  Google Scholar 

  • Brand South Africa (2015) South Africa’s weather and climate. http://www.southafrica.info. Accessed date on Feb 2 2015

  • Bueno VHP, Carvalho LM, van Lenteren JC (2014) Performance of Orius insidiosus after storage, exposure to dispersal material, handling and shipment processes. Bull Insectol 67:175–183

    Google Scholar 

  • Callebaut B, van Baal E, Vandekerkhove B, Bolckmans K, De Clercq P (2004) A fecundity test for assessing the quality of Macrolophus caliginosus reared on artificial diets. Parasitica 60:9–14

    Google Scholar 

  • Chown SL, Terblanche JS (2006) Physiological diversity in insects: ecological and evolutionary contexts. Adv Insect Physiol 33:50–152

    Article  Google Scholar 

  • Danks HV (1987) Insect dormancy: an ecological perspective (Biological Survey of Canada Monograph Series, No 1). Entomological Society of Canada

  • Denlinger DL (1991) Relationship between cold hardiness and diapause. In: Lee LE Jr, Denlinger DL (eds) Insects at low temperature. Chapman and Hall, New York, pp 174–198

    Chapter  Google Scholar 

  • Dennil GB (1992) Orius thripoborus (Anthocoridae), a potential biocontrol agent of Heliothrips haemorrhoidalis and Selenothrips rubrocinctus (Thripidae) on avocado fruit in the Eastern Transvaal. S Afr Avocado Growers’ Assoc Yearbook 15:55–56

    Google Scholar 

  • European and Mediterranean Plant Protection Organization (EPPO) (2014) PQR—EPPO database on quarantine pests. http://www.eppo.int. Accessed date on Aug 27 2014

  • Hart AJ, Bale JS, Tullett AG, Worland MR, Walters KFA (2002a) 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  CAS  PubMed  Google Scholar 

  • Hart AJ, Tullett AG, Bale JS, Walters KF (2002b) Effects of temperature on the establishment potential in the UK of the non-native glasshouse biocontrol agent Macrolophus caliginosus. Physiol Entomol 27:112–123

    Article  Google Scholar 

  • Hatherly IS, Hart AJ, Tullett AG, Bale JS (2005) Use of thermal data as a screen for the establishment potential of non-native biological control agents in the UK. BioControl 50:687–698

    Article  Google Scholar 

  • Hatherly IS, Pedersen BP, Bale JS (2008) Establishment potential of the predatory mirid Dicyphus hesperus in northern Europe. BioControl 53:589–601

    Article  Google Scholar 

  • Hernández LM, Stonedahl GM (1999) A review of the economically important species of the genus Orius (Heteroptera: Anthocoridae) in East Africa. J Nat Hist 33:543–568

    Article  Google Scholar 

  • Hesse AJ (1940) A new species of Thripleps (Hemiptera-Heteroptera, Anthocoridae) predaceous of the citrus thrips (Scirtothrips aurantii Faure) in the Transvaal. J Entomol Soc South Afr 3:66–71

    Google Scholar 

  • Hilbe J (2011) Negative binomial regression, 2nd edn. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Hughes GE, Bale JS, Sterk G (2009) Thermal biology and establishment potential in temperate climates of the predatory mirid Nesidiocoris tenuis. BioControl 54:785–795

    Article  Google Scholar 

  • IBM Corp (2012) IBM SPSS statistics for windows, Version 21.0. IBM Corp, Armonk

    Google Scholar 

  • Ito K, Nakata T (1998a) Diapause and survival in winter in two species of predatory bugs, Orius sauteri and O. minutus. Entomol Exp Appl 89:271–276

    Article  Google Scholar 

  • Ito K, Nakata T (1998b) Effect of photoperiod on reproductive diapause in the predatory bugs, Orius sauteri (Poppius) and O. minutus (Linnaeus) (Heteroptera: Anthocoridae). Appl Entomol Zool 33:115–120

    Google Scholar 

  • Ito K, Nakata T (2000) Geographical variation of photoperiodic response in the females of a predatory bug, Orius sauteri (Poppius) (Heteroptera: Anthocoridae) from northern Japan. Appl Entomol Zool 35:101–105

    Article  Google Scholar 

  • Kiritani Y (1985) Effect of stationary and changing photoperiods on nymphal development in Carbula humerigera (Heteroptera: Pentatomidae). Appl Entomol Zool 20:257–263

    Google Scholar 

  • Kirk WD, Terry LI (2003) The spread of the western flower thrips Frankliniella occidentalis (Pergande). Agric For Entomol 5:301–310

    Article  Google Scholar 

  • Kobayashi T, Osakabe M (2009) Pre-winter copulation enhances overwintering success of Orius females (Heteroptera: Anthocoridae). Appl Entomol Zool 44:47–52

    Article  Google Scholar 

  • Kohno K (1997) Photoperiodic effect on incidence of reproductive diapause in Orius sauteri and O. minutus (Heteroptera: Anthocoridae). Appl Entomol Zool 32:644–648

    Google Scholar 

  • Leather SR, Walters KF, Bale JS (1995) The ecology of insect overwintering. Cambridge University Press, Cambridge

    Google Scholar 

  • Lee RE, Strong-Gunderson JM, Lee MR, Grove KS, Riga TJ (1991) Isolation of ice nucleating active bacteria from insects. J Exp Zool 257:124–127

    Article  Google Scholar 

  • Lopatina EB, Balashov SV, Kipyatkov VE (2007) First demonstration of the influence of photoperiod on the thermal requirements for development in insects and in particular the linden-bug, Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae). Eur J Entomol 104:23–31

    Article  Google Scholar 

  • Maes S, Machtelinckx T, Moens M, Grégoire JC, De Clercq P (2012) The influence of acclimation, endosymbionts and diet on the supercooling capacity of the predatory bug Macrolophus pygmaeus. BioControl 57:643–651

    Article  Google Scholar 

  • Maes S, Grégoire JC, De Clercq P (2015) Cold tolerance of the predatory ladybird Cryptolaemus montrouzieri. BioControl 60:199–207

    Article  CAS  Google Scholar 

  • Masaki S (1990) Opportunistic diapause in the subtropical ground cricket, Dianemobius fascipes. In: Gilbert F (ed) Insect life cycles. Genetics, evolution and co-ordination. Springer, London, pp 125–141

    Chapter  Google Scholar 

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

    Book  Google Scholar 

  • Morse JG, Hoddle MS (2006) Invasion biology of thrips. Annu Rev Entomol 51:67–89

    Article  CAS  PubMed  Google Scholar 

  • Musolin DL, Ito K (2008) Photoperiodic and temperature control of nymphal development and induction of reproductive diapause in two predatory Orius bugs: interspecific and geographic differences. Physiol Entomol 33:291–301

    Article  Google Scholar 

  • Musolin DL, Saulich AKh (1997) Photoperiodic control of nymphal growth in true bugs (Heteroptera). Entomol Rev 77:768–780

    Google Scholar 

  • Musolin DL, Tsytsulina K, Ito K (2004) Photoperiodic and temperature control of reproductive diapause induction in the predatory bug Orius strigicollis (Heteroptera: Anthocoridae) and its implications for biological control. Biol Control 31:91–98

    Article  Google Scholar 

  • Nakashima Y, Hirose Y (1997) Winter reproduction and photoperiodic effects on diapause induction of Orius tantillus (Motschulsky) (Heteroptera: Anthocoridae), a predator of Thrips palmi. Appl Entomol Zool 32:403–405

    Google Scholar 

  • Pazyuk IM, Musolin DL, Reznik SY (2014) Geographic variation in thermal and photoperiodic effects on development of zoophytophagous plant bug Nesidiocoris tenuis. J Appl Entomol 138:36–44

    Article  Google Scholar 

  • Riudavets J (1995) Predators of Frankliniella occidentalis (Perg.) and Thrips tabaci Lind.: a review. In: Loomans AJM, van Lenteren JC, Tommasini MG, Maini S, Riudavets J (eds) Biological control of thrips pests. Wageningen Agricultural University, Wageningen, pp 43–87

    Google Scholar 

  • Ruberson JR, Bush L, Kring TJ (1991) Photoperiodic effect on diapause induction and development in the predator Orius insidiosus (Heteroptera: Anthocoridae). Environ Entomol 20:786–789

    Article  Google Scholar 

  • Ruberson JR, Shen YJ, Kring TJ (2000) Photoperiodic sensitivity and diapause in the predator Orius insidiosus (Heteroptera: Anthocoridae). Ann Entomol Soc Am 93:1123–1130

    Article  Google Scholar 

  • Saulich AKh, Musolin DL (2009) Seasonal development and ecology of anthocorids (Heteroptera, Anthocoridae). Entomol Rev 89:501–528

    Article  Google Scholar 

  • Saunders DS (2002) Insect clocks, 3rd edn. Elsevier, Amsterdam

    Google Scholar 

  • Shimizu K, Fujisaki K (2006) Geographic variation in diapause induction under constant and changing conditions in Helicoverpa armigera. Entomol Exp Appl 121:253–260

    Article  Google Scholar 

  • Shimizu T, Kawasaki K (2001) Geographic variability in diapause response of Japanese Orius species. Entomol Exp Appl 98:303–316

    Article  Google Scholar 

  • South African Weather Service (2015) About climate at SAWS. http://www.weathersa.co.za. Accessed date on Feb 2 2015

  • Tanaka S, Zhu DH (2003) Presence of three diapauses in a subtropical cockroach: control mechanisms and adaptive significance. Physiol Entomol 28:323–330

    Article  Google Scholar 

  • Tauber MJ, Tauber CA, Masaki S (1986) Seasonal adaptations of insects. Oxford University Press, Oxford

    Google Scholar 

  • Tommasini MG, Nicoli G (1995) Evaluation of Orius spp. as biological control agents of thrips pests: initial experiments on the existence of diapause in Orius laevigatus. Meded Fac Landbouwwet Univ Gent 60:901–907

    Google Scholar 

  • Tommasini MG, Nicoli G (1996) Evaluation of Orius spp. as biological control agents of thrips pests. Further experiments on the existence of diapause in Orius laevigatus. Bull OILB/SROP (France) 19:183–186

    Google Scholar 

  • van Damme V, Berkvens N, Moerkens R, Berckmoes E, Wittemans L, De Vis R, Casteels H, Tirry L, De Clercq P (2015) Overwintering potential of the invasive leafminer Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) as a pest in greenhouse tomato production in Western Europe. J Pest Sci 88:533–541

    Article  Google Scholar 

  • van den Meiracker RVD (1994) Induction and termination of diapause in Orius predatory bugs. Entomol Exp Appl 73:127–137

    Article  Google Scholar 

  • van den Meiracker RAF, Ramakers PMJ (1991) Biological control of the western flower thrips Frankliniella occidentalis, in sweet pepper, with the anthocorid predator Orius insidiosus. Meded Fac Landbouwwet Univ Gent 56:241–249

    Google Scholar 

  • Watanabe M (2002) Cold tolerance and myo-inositol accumulation in overwintering adults of a lady beetle, Harmonia axyridis (Coleoptera: Coccinellidae). Eur J Entomol 99:5–10

    Article  CAS  Google Scholar 

  • Way MJ, Stiller M, Leslie GW, Conlong DE, Keeping MG, Rutherford RS (2006) Fulmekiola serrata (Kobus) (Thysanoptera: Thripidae), a new pest in southern African sugarcane. Afr Entomol 14:401–403

    Google Scholar 

  • Worland MR, Block W (1999) Ice-nucleating bacteria from the guts of two sub-Antarctic beetles, Hydromedion sparsutum and Perimylops antarcticus (Perimylopidae). Cryobiol 38:60–67

    Article  Google Scholar 

  • Zhang SC, Zhou XM, Wang XP, Lei CL (2008) Oviposition on preference of Orius similis and preservation condition of eggs. Chin Bull Entomol 45:600–603

    Google Scholar 

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Authors and Affiliations

  1. Laboratory of Agrozoology, Department of Crop Protection, Ghent University, Coupure Links 653, 9000, Ghent, Belgium

    Jochem Bonte & Patrick De Clercq

  2. Department of Forest Protection and Game Management, Saint Petersburg State Forest Technical University, Institutskiy per., 5, St. Petersburg, Russia, 194021

    Dmitry L. Musolin

  3. South African Sugarcane Research Institute, Private Bag X02, Mount Edgecombe, 4300, South Africa

    Des Conlong

  4. School of Biological and Conservation Sciences, University of KwaZulu-Natal, Private Bag X01, Scottsville, Pietermaritzburg, 3209, KwaZulu-Natal, South Africa

    Des Conlong

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  1. Jochem Bonte
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Correspondence to Jochem Bonte.

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Bonte, J., Musolin, D.L., Conlong, D. et al. Diapause and winter survival of two Orius species from southern Africa. BioControl 61, 519–532 (2016). https://doi.org/10.1007/s10526-016-9730-7

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