Impact of cold storage on the performance of

Impact of cold storage on the performance of entomophagous insects: an overview

Mandeep Rathee & Pala Ram

Phytoparasitica ISSN 0334-2123 Phytoparasitica DOI 10.1007/s12600-018-0683-5

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Author's personal copy Phytoparasitica https://doi.org/10.1007/s12600-018-0683-5

Impact of cold storage on the performance of entomophagous insects: an overview Mandeep Rathee

&

Pala Ram

Received: 7 March 2018 / Accepted: 13 July 2018 # Springer Nature B.V. 2018

Abstract Mass rearing for commercial production of high quality beneficial insects is considered as an important tool for biological control programmes worldwide, especially those based on augmentative releases. Low temperature storage is a valuable method for increasing the shelf life of entomophagous insects. Insect predators and parasitoids are used extensively in biological control programmes and, because of this, studies on cold storage started over 90 years ago. The ability to store reared biocontrol agents at low temperatures for certain duration provides an opportunity to accumulate or stockpile sufficient number of entomophagous insects for field release at proper weather conditions and make them available during high demand periods to the concerned farmers. Cold stored natural enemies can be synchronously released in the fields during critical stages of pest outbreaks. Cold storage also helps to keep viable stock of natural enemies when not needed and to minimize laboratory operations by prolonging their survival and delaying eclosion. Cold storage tolerance is highly plastic trait influenced by a range of biotic and abiotic factors experienced before, during and after cold exposure. These factors ultimately affect the development, longevity, fecundity, parasitization, sex-ratio and other fitness parameters along with morphology, behaviour and physiology of entomophagous insects. For the successful implementation of a cold storage project, M. Rathee (*) : P. Ram Department of Entomology, Chaudhary Charan Singh Haryana Agricultural University, Hisar, Haryana 125004, India e-mail: [email protected]

knowledge of these diverse factors that cause storage and post-storage effects is essential. The potential of cold storage protocols in improving mass rearing and commercial production of bioagents is thus reviewed to access the strategies, innovations, techniques, devices and wisdom involved in the process of cold storage of entomophagous insects worldwide. Keywords Cold storage . Temperature . Storage duration . Entomophagous insects . Biological parameters

Introduction Mass rearing of bioagents is a prerequisite of biocontrol programmes; this needs a regular and sufficient production of easily culturable insect hosts and preys (Osman and Selman 1993; van Lenteren 2012; Morales-Ramos et al. 2014; Wadaskar et al. 2015). Mass rearing and commercial production of beneficial insects has long been considered as an important tool for biological control programmes worldwide, especially those based on augmentative releases (van Lenteren and Tommasini 2002). Low temperature storage is a valuable method for increasing the shelf life of natural enemies such as insect parasitoids and predators. Entomophagous insects are used extensively in biological control programmes and, because of this, studies on their cold storage started over 90 years ago (Schread and Garman 1934; Hanna 1935). The ability to store reared biocontrol agents at low temperatures provides an opportunity to accumulate

Author's personal copy Phytoparasitica

sufficient number of parasitoids and predators for field release at proper weather conditions and make them available during high demand periods to the concerned farmers. Cold stored natural enemies can be synchronously released in the fields during critical stages of pest outbreaks (McDonald and Kok 1990; Abdel-Salam and Abdel-Baky 2000; Venkatesan et al. 2000; Coudron et al. 2007; Riddick and Wu 2010; Costa et al. 2016). Cold storage also helps to stockpile viable natural enemies when not needed and minimize laboratory operations by prolonging their survival and delaying eclosion (Pitcher et al. 2002; Ayvaz et al. 2008; Rathee and Ram 2014; Rathee et al. 2015; Singhamuni et al. 2015). Cold storage is usually performed under sub-optimal temperatures (Colinet and Boivin 2011), generally above 0 °C (Leopold 1998). Cold storage of entomophagous insects aids in their overseas transport without risk of thermal injury (Hofsvang and Hagvar 1977; Li et al. 2014). Cold storage of entomophagous insects either as immatures or as adults would not be too much detrimental to them if interrupted at regular intervals of normal respiration and feeding (Flanders 1938; Riddick 2001; Uckan and Ergin 2003; Tunca et al. 2014). Humidification can suppress water loss from these creatures and has great potential for improving their survival during cold storage. The low storage temperature is very important for entomophagous insects because suitable hosts may not be available at the time of adult emergence (Prasad and Ansari 2000). Successful implementation of any augmentative biological control programme targeted against a specific insect pest is limited by timing and cost of rearing beneficial insects in large numbers for mass release. Storage, handling and shipment procedures are important factors influencing the quality of biological control agents. For instance, shipment of the predator Orius insidiosus (Say) by post during 72 h (hrs.) in Styrofoam boxes with plastic containers with vermiculite + rice hulls and Anagasta kuehniella (Zeller) eggs had no negative effects on its survival and predation capacity (Bueno et al. 2014). Unlike pesticides, most biocontrol agents used in pestcontrol programmes have a relatively short shelf life and therefore they are produced shortly before use. The use of low temperature has proved to be a valuable method for enhancing shelf life of natural enemies, allowing flexible and efficient mass production, with a steady and sufficient supply for pest-control programmes (Colinet and Hance 2010). Lee and Denlinger (2010) stated that low temperature affects insects differently based on the severity of the cold and the duration of exposure.

In order to extent their shelf-life, entomophagous insects can be stored at low temperatures ranging from 5 to 15 °C (van Lenteren and Tommasini 2003; Dindo and Grenier 2014; Mahi et al. 2017). The temperature choice for cold storage has to be low enough to decrease or even completely stop the development. This is particularly true for Aphidiines, which are shipped at the mummy stage (Colinet and Hance 2010). Even under these moderately low temperatures, most species show some level of mortality (van Lenteren and Tommasini 2002). Generally, the lower the storage temperature, the higher is the mortality (Ballal et al. 1989; Jalali and Singh 1992; Rundle et al. 2004; Lopez and Botto 2005; Bernardo et al. 2008; Lins et al. 2013; Rathee and Ram 2014; Tunca et al. 2014; Anwar et al. 2016; Rathee and Ram 2016; Perdomo et al. 2017). Cold storage is desirable but risky for the performance of the stored parental generation as well as for its offspring (Hackermann et al. 2008). Indeed, the survival of immature or adult stages of entomophagous insects is dependent on their lipid reserves and water content. Various developmental instars kept at low temperatures slow down their metabolic activities (Chapman 1982; Ladurantaye et al. 2010) and can survive on their fat bodies for a longer time. At low temperatures, they develop more slowly and the period for which they can survive increases, but soon their reserves are exhausted and ultimately they die (Colinet 2007). Furthermore, the consumption of lipids results in fewer individuals surviving, a reduction in the volume of the seminal vesicles and testicles of the males and in the number of eggs in the ovaries of entomophagous insects, for example in case of Aphidius ervi (Haliday) females (Michel 2007). The effect of cold storage stress might not be immediately detectable, but might carry over to another stage, negatively influencing either development, fecundity, survival or other key biological phenomena (Chown and Nicolson 2004). The effects of low temperature storage on the development, longevity, fecundity, parasitization, sex-ratio and other fitness parameters have been reported by various workers on different entomophagous insects. Effect of cold storage, during various stages of life cycle, on the biological characteristics of various Hymenopteran parasitoids viz., Bracon brevicornis Wesmael, Copidosoma varicorne (Nees), Anagyrus kamali Moursi, Trichogramma cacoeciae Marchal, Trichogramma nerudai Pintureau and Gerding, Anagyrus ananatis Gahan, Anagyrus sp. nov. nr. sinope Noyes and Menezes,


Telenomus podisi Ashmead, Trichogramma evanescens (Westwood), Anaphes iole Girault, Aphidius rhopalosiphi De Stephani Perez, Psyttalia humilis (Silvestri), Tetrastichus brontispae (Ferriere), Aenasius arizonensis (Girault) (=Aenasius bambawalei Hayat), Apanteles gelechiidivoris Marsh and Habrobracon hebetor Say has been studied by Jayanth and Nagarkatti (1985), Prasad and Ansari (2000), Sagarra et al. (2000), Ozder (2004), Tezze and Botto (2004), Pandey and Johnson (2005), Chong and Oetting (2006), Foerster and Doetzer (2006), Yilmaz et al. (2008), Abdullah et al. (2009), Bourdais et al. (2012), Daane et al. (2013), Liu et al. (2014), Rathee (2014), Perdomo et al. (2017) and Seyahooei et al. (2018), respectively. Little data are available for tachinids and other Dipterans and most of them are not very recent (Fusco et al. 1978; Gilkeson 1990; Mills and Nealis 1992; Easwaramoorthy et al. 2000; Benelli et al. 2017). Fusco et al. (1978) successfully stored the tachinid parasitoid, Compsilura concinnata (Meigen), both as young larva in the host and as puparium, at 10–15.6 °C for 2– 4 weeks. Another tachinid parasitoid, Archytas marmoratus (Townsend) was stored by Gross and Johnson (1985) as maggot at 13 °C for a few days. Likewise, the possibility of cold storage has been studied for many predators (Shands and Simpson 1972; Quezada and De Bach 1973; Rudolf et al. 1993; Abdel-Salam et al. 1997; Lopez-Arroyo et al. 2000; Ozgokce et al. 2006; Coudron et al. 2007; Amaral et al. 2013; Awad et al. 2013; Nadeem et al. 2014; Costa et al. 2016; Senal et al. 2017). Shands and Simpson (1972) stored Coccinella septempunctata L. eggs at 10 °C. Quezada and De Bach (1973) held Rodolia cardinalis Mulsant pupae and adults at 12.5 °C. Eggs of C. septempunctata and Adalia bipunctata L. were stored for 1 or 2 weeks at 10 °C (Hamalainen and Markkula 1977). Hamalainen (1977) stored adults of the previous species at 6 °C. Harmonia axyridis (Pallas) adults have been stored at 5 °C (Deng 1982) and Abdel-Salam et al. (1997) stored H. axyridis adults at 4, 8 and 12 °C for 15, 30, 45 and 60 days. Ozgokce et al. (2006) stored Cryptolaemus montrouzieri Mulsant adults at 15 °C for 5 days. Therefore, lot of work on the cold storage of entomophagous insects, especially the Hymenopteran and, to a less extent, Dipteran parasitoids, and predators belonging to order Coleoptera, Neuroptera, Hemiptera and Thysanoptera has been carried out and published in India and abroad. The application of cold storage is not only limited to facilitate industrial rearing of beneficial insects, but it is also useful for maintaining insect colonies under laboratory conditions

for research purposes (Leopold 2007); hence cold storage protocols must be developed and improved further in order to ensure availability of quality natural enemies to counteract the insect-pest menace in future and ensure food security. In our opinion cold storage of entomophagous insects is of global interest, but a unified summary is lacking on the same. Thus, a thorough review of literature on the subject is therefore, presented under the following sub-heads: I. Factors affecting survival and fitness of the entomophagous insects in cold storage II. Effect of cold storage during immature stages on biological characteristics and fitness of the entomophagous insects III. Effect of cold storage during adult stage on biological characteristics and fitness of the entomophagous insects

I. Factors affecting survival and fitness of the entomophagous insects in cold storage Worldwide studies have emphasized that cold storage represents a stress factor that can affect survival and key parameters of fitness such as longevity (Rundle et al. 2004; Amice et al. 2008; Ismail et al. 2010, 2012, 2013; Rathee and Ram 2014), fecundity (Larios et al. 2002; Pitcher et al. 2002; Rathee and Ram 2014), sperm production (Lacoume et al. 2007; Michel 2007), sex ratios (Ismail et al. 2010, 2012; Rathee and Ram 2014; Queiroz et al. 2016; Mahi et al. 2017; Forouzan et al. 2018; Seyahooei et al. 2018), female and male sterility (Levie et al. 2005) and flight ability, which in turn can affect dispersal (Luczynski et al. 2007). Cold stress has been reported to affect reproductive behaviour and mating success (Carriere and Boivin 2001; Shreve et al. 2004; Amice et al. 2008; Colinet and Hance 2009), male physiology (Rinehart et al. 2000; David et al. 2005), female patch exploitation and olfaction (Herard et al. 1988; Rinehart et al. 2000; van Baaren et al. 2005), antennal chemoreceptors (Bourdais et al. 2006; Amice et al. 2008), recognition of odours in both the sexes (Bourdais et al. 2012), deformation of wings and ovipositors (Tezze and Botto 2004; Sandanayaka et al. 2015), poor immature survival and increased mortality (Rundle et al. 2004; Luczynski et al. 2007; Sajid et al. 2010; Silva et al. 2013; Liu et al. 2014; Rathee and Ram 2014; Tunca et al. 2014;


Sandanayaka et al. 2015; Vigneswaran et al. 2017). For instance, when immatures of T. evanescens were exposed to 4 °C for 28 days, walking speed decreased (Ayvaz et al. 2008). Similarly, when T. nerudai immatures were kept at 4 °C for 50 days, the emerging adults had poor flying ability. Wings deformity has been reported in Trichogramma brassicae Bezdenko and T. nerudai when immatures were exposed to low temperature (Dutton and Bigler 1995; Tezze and Botto 2004). Long-term exposure to low temperatures may cause cellular damage, metabolism perturbations or accumulation of toxins (Chapman 1982; Knight et al. 1986; Chen et al. 1987; Gagne and Coderre 2001). The parasitoids die because of three main factors namely cold, desiccation and starvation during cold storage (De Bach 1943; Legrand et al. 2004; Colinet et al. 2006; Michel 2007). During these conditions of low temperature storage for short or long term, various exogenous and endogenous factors play vital roles, either synergistically or antagonistically, in the survival and development of the entomophagous insects (Table 1) (Colinet and Boivin 2011). Temperature, humidity, oxygen concentration, duration of storage, photoperiod, acclimation, acclimatization and development temperature are major exogenous factors. Gradual acclimation is a form of phenotypic plasticity to increase cold tolerance by long-term pre-exposure to sub-lethal low temperatures (Hoffmann et al. 2003; Chown and Terblanche 2006; Anguilletta 2009). The terms pre-conditioning or precooling or pre-storage or pre-treatment, all refer to acclimation. In entomophagous insects, acclimation by exposing them to low temperature close to their developmental threshold before cold storage generally had a positive impact on key biological parameters and cold storage tolerance (Polgar 1986; Singh and Srivastava 1988;

Bueno and van Cleave 1997; Pandey and Johnson 2005; Marwan and Tawfiq 2006; Luczynski et al. 2007; Cagnotti et al. 2018). In Thripobius javae (Girault), pupae acclimation at 10 °C for ten days resulted in two fold increase in time to emergence in comparison to non acclimated ones (Bernardo et al. 2008). Rapid acclimation refers to the increase in cold tolerance after a short pre-exposure (minutes to hours) to sub-lethal low temperatures (Hoffmann et al. 2003; Chown and Nicolson 2004; Anguilletta 2009). It increases survival after both cold shock (acute) and prolonged cold exposure (chronic) (Lee and Denlinger 2010). For instance, in A. rhopalosiphii, different shortterm acclimation treatments on mummies reduced mortality after storage as compared to treatments without rapid acclimation (Levie et al. 2005). Gradual and rapid acclimations involve different physiological changes and their combination can result in synergistic and positive effects (Shintani and Ishikawa 2007). Acclimatization process is similar to gradual acclimation, but has been mostly used when referring to acclimation under natural conditions (Hoffmann et al. 2003; Chown and Nicolson 2004; Chown and Terblanche 2006). Boosting cold hardiness in entomophagous insects is a goal that is particularly attractive for increasing shelf life and shipment (Rigaux et al. 2000; Li et al. 2014). Physiological adaptations, namely quiescence and diapause allow insects to survive cold stress in a dormancy state. Quiescence is an immediate direct response to a limiting factor, such as when temperature falls below the insect’s development threshold, but immediate resumption of development occurs when the conditions improve. While diapause is the naturally programmed and genetic response to long-term adverse conditions (Danks 1987, 2002). Hodkova and Hodek (2004) and

Table 1 Exogenous and endogenous factors affecting survival and fitness of entomophagous insects in cold storage Factors of variability

Fitness consequences

Exogenous factors

Endogenous factors

Temperature Storage period Acclimation Acclimatization Development threshold Humidity Photoperiod Oxygen concentration Handling

Mass and body reserve Life history Nutrition Age Gender Mode of reproduction Dormancy status

Development time Mortality Fecundity Longevity Oviposition period Sex-ratio Mating behaviour F1 biomass Mobility Flight capacity


Nadeem et al. (2014) stated that individuals in diapause are generally more cold tolerant than non-diapausing individuals. Temperature is no doubt one of the main abiotic factors affecting survival during cold storage (Colinet and Boivin 2011; Andersen et al. 2015; Sinclair et al. 2015). Kostal et al. (2004) defined the ‘dose of cold exposure’ as a combination of exposure temperature and duration. Susceptibility to cold storage is likely to vary according to temperature conditions during development. When cooled, a majority of insects slow down, eventually lose the ability to move and at a specific temperature, i.e., the critical thermal minimum (CTmin), enter into a reversible state of paralysis, known as chill coma (Hazell and Bale 2011). Because insects cannot move, feed or reproduce while in chill coma, the CTmin provides a useful lower limit to insect functions (Gibert et al. 2001; MacMillan and Sinclair 2011; Andersen et al. 2015). Colinet et al. (2007) observed a reduction in the mortality of Aphidius colemani Viereck mummies developing at low versus high temperature. In contrast, a high developmental temperature (25 °C) was beneficial for cold storage of Trissolcus basalis (Wollaston) and T. podisi (Foerster and Doetzer 2006). Certain developmental stages may be more sensitive to cold than others. In Trichogramma spp., the prepupal stage is less sensitive to low temperature than the larvae (Garcia et al. 2002), while storing adults of Apanteles galleriae Wilkinson for 1 week at 6 °C proved fatal with 85.27% mortality (Uckan and Gulel 2001). Management and provision of supplementary feeding is also important for improving fitness in cold storage as revealed in many studies (Coudron et al. 2007; Chen et al. 2010; Harvey et al. 2012; Tang et al. 2014; Rathee et al. 2015). Several Hymenopteran and Dipteran parasitoid species lack adult lipogenesis, and are unable to store excess energy in the form of lipid reserves (Visser and Ellers 2008), therefore, during storage, sugar source like honey, glucose or sucrose, replenish the energetic and nutritional stores and prevent them from dying due to starvation otherwise.

II. Effect of cold storage during immature stages on biological characteristics and fitness of the entomophagous insects Survival and mortality Mortality represents the ultimate cost of cold exposure. In addition to sub-lethal or lethal effects of chilling

injuries (Hance et al. 2007), entomophagous insects stored as immatures may not have sufficient energy resources to complete their development and/or emerge (Renault et al. 2003). Archer et al. (1973) reported that higher mortality at colder temperature indicates an adverse effect on metamorphosis and survival. In some solitary species, dissection of non-emerged dead parasitoids after cold storage has shown that mortality occurred mainly after metamorphosis in pharate adults (Colinet et al. 2006) or during the eclosion process (Pandey and Johnson 2005; Luczynski et al. 2007; Rathee and Ram 2016). The process of emergence is energy-consuming requiring strong muscle contraction and chilling is known to induce muscular dysfunctions. Pharate adults fail to emerge after cold storage due to lack of energy along with muscular perturbations (Yocum et al. 1994). In both solitary and gregarious parasitoids, mortality generally increases with duration of cold storage (Ozder and Saglam 2004; Bayram et al. 2005; Foerster and Doetzer 2006; Colinet and Hance 2010) but in gregarious species, this temporal effect can be seen as a decreasing number of emerging parasitoids per host as duration of storage increases (Lysyk 2004). In most of the cold storage studies where different storage durations were tested, survival of the entomophagous insects decreased with an increase in storage duration (Stray 1971; Osman and Selman 1993; Okine et al. 1996; Khosa and Brar 2000; Lopez-Arroyo et al. 2000; Gagne and Coderre 2001; Leppla et al. 2002; Pitcher et al. 2002; Slachta et al. 2002; Ozder and Saglam 2004; Bayram et al. 2005; Foerster et al. 2004; Foerster and Doetzer 2006; Larentzaki et al. 2007; Chen et al. 2008b; Viel et al. 2008; Abdel-Gawad et al. 2010; Colinet and Hance 2010; Ladurantaye et al. 2010; Dileep 2012; Amaral et al. 2013; Daane et al. 2013; Rathee and Ram 2014; Binazzi et al. 2015; Sandanayaka et al. 2015; Alam et al. 2016; Perdomo et al. 2017; Vigneswaran et al. 2017; Yan et al. 2017). Among the cold storage temperatures, 5 °C or less seemed to be the least suitable temperatures for storage of entomophagous insects in immature stages (Jalali and Singh 1992; Rossi 1993; Garcia et al. 2002; Lopez and Botto 2005; Daane et al. 2013; Rathee and Ram 2014; Tunca et al. 2014; Sandanayaka et al. 2015; Costa et al. 2016; Nahiyoon et al. 2016). Since chilling injuries are cumulative, the gradual decline in survival may follow linear and thus predictable patterns (Jalali and Singh 1992; Abdel-Gawad et al. 2010) or show complex non-linear patterns (Lysyk 2004) with time of exposure.


Recently, Silva et al. (2018) reported that storage of T. podisi pupae at 5 °C for more than 7 days had negative impact on parasitoid biology. With respect to survival and adult longevity, 10 ± 2 °C seemed to be the most suitable storage temperature range for one week duration (Hamalainen and Markkula 1977; Ferran 1983; Gautam 1986; Ballal et al. 1989; Jalali and Singh 1992; Coudron et al. 2007; Ladurantaye et al. 2010; Nadeem et al. 2010; Daane et al. 2013; Liu et al. 2014; Rathee and Ram 2014; Tunca et al. 2014; Vigneswaran et al. 2017; Ghosh and Ballal 2018). Cold storage of the entomophagous insects has been attempted using different developmental stages viz., egg, larval instars or nymphs, pre-pupa, pupa and adult. Of these, pupal stage was found to be the most appropriate stage for cold storage of parasitoids (Jalali and Singh 1992; Nakama and Foerster 2001; van Lenteren and Tommasini 2002; Rathee and Ram 2014; Binazzi et al. 2015). Generally, smaller individuals suffer more when exposed to low temperatures, which may be, for example, because they have lower reserves (Colinet 2007) or because their bodies have a higher surface area for evaporation relative to their volume (Legrand 2005). Gautam (1986) reported that storage of Telenomus remus Nixon in the pupal stage at 10 °C for 7 days did not influence parasitoid survival. Press and Arbogast (1991) reported that survival of immatures of the parasite Venturia canescens (Gravenhorst) was adversely affected by temperatures of 0, 5 and 10 °C, but were only minimally affected at 15 °C. Ballal et al. (1989) found that cocoons of Allorhogas pyralophagus Marsh, a Mexican parasitoid of graminaceous borers failed to survive when stored for more than 14 days at 2 °C, while at 5 and 10 °C, about 50% survival was recorded up to 21 days of storage. Bayram et al. (2005) investigated that Telenomus busseolae Gahan pupae could be stored for four weeks at 4 and 8 ± 1 °C but only two weeks storage was possible at 12 ± 1 °C due to increased mortality. Pandey and Johnson (2005) reported that A. ananatis prepupal to early pupal stages can only be stored for brief periods (< 2 weeks) at 10.1 °C, because prolonged exposure is lethal. Frere et al. (2011) found that the proportion of A. ervi pupae in mummies of aphid Acyrthosiphon pisum (Harris) that survived cold storage decreased with each successive week, when kept at 2 °C (from 0.61 after 5 weeks, to 0.54 after 6 weeks and 0.46 after 7 weeks). Sandanayaka et al. (2015) indicated that 7–10-day-old larvae of Mastrus ridens (Horstmann), an endoparasitoid of the codling moth, could be stored for 12 weeks at 4 °C

without any detrimental effect on their survival. Costa et al. (2016) reported that eggs of Podisus nigrispinus (Dallas), the pentatomid predator of defoliating larvae in Eucalyptus, could be stored up to 10 and 15 days at 13 and 15 °C, respectively, while storage at 5 °C caused the death of the majority of eggs (embryos). Egg parasitoids belonging to several families have also been successfully reared on refrigerated or cryo-stored host eggs (CorreaFerreira and Moscardi 1993; Greco and Stilinovic 1998; Peres and Correa-Ferreira 2004; Kivan and Kilic 2005; Chen and Leopold 2007; Mahmoud and Lim 2007; Alim and Lim 2009, 2010; Cingolani et al. 2015; Peverieri et al. 2015; Forouzan et al. 2018; Silva et al. 2018). For instance, host eggs of Riptortus pedestris (Fabricius) stored at 6 °C had the highest quality for parasitization by Ooencyrtus nezarae Ishii after 8 days of incubation at 26.6 °C (Mainali and Lim 2013). Cold storage of predators has been studied by various entomologists worldwide (Shands and Simpson 1972; Quezada and De Bach 1973; Abdel-Salam et al. 1997; Lopez-Arroyo et al. 2000; Ozgokce et al. 2006; Ladurantaye et al. 2010; Amaral et al. 2013; Bueno et al. 2014; Nadeem et al. 2014; Abdel-Baky et al. 2015; Costa et al. 2016; Senal et al. 2017). For instance in the late seventies, Hamalainen and Markkula (1977) reported that eggs of C. septempunctata and A. bipunctata could be held for 1 and 2 weeks, respectively at 10 °C without any marked reduction in hatching percentage. Ferran (1983) concluded that third instars of Semiadalia undecimnotata Schn. could be kept at 5 or 10 °C for 3 days without considerable mortality. Rawat et al. (1992) investigated that storage at 6 ± 1 °C was suitable for the pupae of Chilocorus bijugus Mulsant, a coleopteran predator of the San Jose scale, for up to 6 weeks. De Clercq and Degheele (1993) succesfuuly stored eggs of Podisus maculiventris (Say) and Podisus sagitta (Fabricius) at 9 °C for 6 days without affecting their viability. Storage of pupae of the South American lady beetle, Eriopis connexa (Germar) at 4 °C for three weeks gave 100% survival, but mortality reached 100% after 7 weeks (Miller 1995). Likewise, Osman and Selman (1993) held eggs of Chrysoperla carnea (Stephens) at 4 and 8 °C for 1– 20 days and reported little decrease in hatchability. Abdel-Salam et al. (1997) reported cent per cent survival of H. axyridis adults at 4, 8 and 12 °C for 30 days, but after 60 days of cold storage, the survival decreased to 60, 40 and 0 %, respectively, for the same temperatures. Saini (1997) observed high viability of C. carnea eggs


after 14 (66%) and 15 (58%) days of storage at 12 °C. Abdel-Salam and Abdel-Baky (2000) stored the eggs and larvae of Coccinella undecimpunctata L. at 6 °C and reported 65% egg hatching after 7 days of storage, however, no egg hatching was observed after 15, 30, 45 and 60 days of storage. The survival of the third and fourth instar larvae was higher than the first and second instars. Gagne and Coderre (2001) reported that survival of Coleomegilla maculata lengi Timberlake larvae was close to 100% for the first two weeks of storage, but decreased drastically afterwards and was 0 % after 5 weeks at 4 and 8 °C. P. maculiventris eggs survived storage at 10 °C better than 4 °C, and the eggs from dietfed insects survived storage at 10 °C significantly better than eggs from prey-fed insects (Coudron et al. 2007). Larentzaki et al. (2007) successfully stored eggs of predatory thrips Franklinothrips vespiformis (Crawford) for 4–5 weeks at 12.5 °C without affecting survival. Ladurantaye et al. (2010) reported that second instar nymphs of the pentatomid predator, Perillus bioculatus (Fabricius) could be successfully stored for approximately 1 week at 9, 12 and 15 °C without affecting survival. Likewise, one, two and three days old eggs of C. carnea could be stored at 12 °C up to 16, 11 and 7 days with viability of 80, 90 and 95%, respectively (Amaral et al. 2013). The global literature pertaining to cold storage of entomophagous insects is summarized in Tables 2, 3 and 4. Adult emergence Development of immatures and adult emergence (Pereira et al. 2009) after storage are essential parameters for the successful utilization of the entomophagous insects. The per cent adult emergence decreased significantly as the storage durations increased and temperature decreased (Press and Arbogast 1991; Okine et al. 1996; Waggoner et al. 1997; Easwaramoorthy et al. 2000; Ozder 2004; Tezze and Botto 2004; Amice et al. 2008; Bernardo et al. 2008; Abdel-Gawad et al. 2010; Colinet and Hance 2010; Manjoo and Bajpai 2012; Lins et al. 2013; Abdel-Salam et al. 2014; Ahmad and Ahmad 2014; Tunca et al. 2014; Rathee and Ram 2014; Abdel-Baky et al. 2015; Sandanayaka et al. 2015; Anwar et al. 2016; Perdomo et al. 2017; Cagnotti et al. 2018; Forouzan et al. 2018; Ghosh and Ballal 2018). Quezada and De Bach (1973) reported that the emergence of adults from R. cardinalis pupae was 100 and 50% after 5 and 7 weeks of storage at 12.5 °C. Jalali et al.

(1990) found that freshly-formed cocoons of C. marginiventris could be stored at 10 °C for 20 days with 81% adult emergence. Waggoner et al. (1997) reported that per cent emergence of adult parasitoids, Aphelinus asychis Walker and Aphelinus albipodus (Hayat and Fatima), from stored pupae at 10 ± 1 °C decreased from 79 to 53% as the storage duration increased from 2 to 14 days, respectively. Likewise, AbdelSalam and Abdel-Baky (2000) reported 85 to 25% emergence of C. undecimpunctata adults from stored pupae at 6.0 °C after storage for 7 and 30 days, respectively. Easwaramoorthy et al. (2000) found that the puparia of the tachinid, Sturmiopsis inferens Townsend, a larval parasitoid of sugarcane moth borers, could be stored for 30 days at 15 °C without any adverse effect on fly emergence. Venkatesan et al. (2000) reported that storage of cocoons of Goniozus nephantidis Muesebeck at 15 °C for 10 days resulted in maximum adult emergence (90%). Pitcher et al. (2002) compared emergence rates of Trichogramma ostriniae Pang and Chen reared on Sitotroga cerealella (Olivier) eggs held at 6, 9, 12, 15 and 24 °C for up to 8 weeks after parasitism. At 15 °C, emergence occurred in 80% for parasitized eggs stored at 9 and 12 °C for 4 and 6 weeks, respectively, while storage at 6 °C caused a significant decline in emergence after 2 weeks. Rundle et al. (2004) concluded that storage temperatures lower than 10 °C i.e. 4 and 8 °C and storage duration of three weeks or longer had a negative impact on the poststorage emergence of Trichogramma carverae Oatman and Pinto adults. Adult emergence in Trichogramma brasiliense (Ashmead) reached 0 % after 34 days of storage whereas 20.3% was recorded in Trichogramma chilonis (Ishii) and 15.7% in Trichogramma pretiosum Riley after 60 days of storage (Kumar et al. 2005). Abdullah et al. (2009) also reported better adult emergence when eggs of Lygus hesperus Knight parasitized by A. iole were stored at 10 °C than at 4 °C. When sixday old parasitized Lygus eggs were stored in complete darkness at 10 °C for 20, 40, 60 and 80 days there was 62.90, 42.50, 29.60 and 8.35% emergence, respectively. Silva et al. (2013) reported that Diaeretiella rapae (McIntosh) mummies could be stored for up to 24 days at 5 °C, with >83% adult emergence. Daval (2014) revealed that the eggs and pupae of Crysoperla zastrowi arabica (Henry) could be stored effectively without much deterioration up to 14 days at 15 °C while, more than 14 days storage significantly reduced the hatching and adult emergence. Liu et al. (2014) reported that

Chilo infuscatellus Snellen Diuraphis noxia (Kurdjumov)

Sturmiopsis inferens Townsend

Hymenoptera: Braconidae: (Sub family: Aphidiinae)

2 °C constantly, 2 °C for 22 h. and 20 °C for 2 h. 4 °C, 75 ± 5% RH

Sitobion avenae Fabricius

Myzus persicae Sulzer


Aphidius ervi (Haliday)

Aphidius ervi (Haliday), Aphidius matricariae Haliday, Ephedrus cerasicola Stary and Praon volucre Haliday Aphidius picipes Nees

Acyrthosiphon 1–3 °C, 12 °C pisum (Harris)

Aphidius smithi Sharma & Subba Rao

4 °C


Aphidius rhopalosiphi De Stephani Perez

0 and 4 °C

2, 7 and 20 °C

0, 1, 4, 7 and 10 °C

Myzus persicae Sulzer

Aphidius colemani Viereck, Ephedrus cerasicola Stary

Encarsia sophia (Girault and Dodd)

Trialeurodes 4.5 ± 2 °C and vaporarorium 11.5 ± 2 °C Westwood Bemisia tabaci 4, 8 and 12 ± 1 °C (Gennadius)

Encarsia formosa Gahan, Eretmocerus corni Haldeman

1.7, 4.4, 7.2 and 10 °C

Monellia caryella (Fitch)

4.4 °C

10 °C

5 and 10 °C

15 and 20 °C

Aphelinus perpallidius (Gahan)

Aphelinus asychis Walker

Aphelinus albipodus (Hayat and Fatima)

Artificial media, no host

Exorista larvarum (L.)

Hymenoptera: Aphelinidae

Lymantria dispar 8 °C L.

Ceranthia samarensis lengi Timberlake

Temperature

Storage conditions

Diptera: Tachinidae

Laboratory Host

Scientific Name

Order: Family

3, 7 and 10 days old mummies

Pupae, 35% RH

Pupae

Eggs

Pupae

Stage stored and conditions

24 °C, 40% RH

18 °C, 16 L: 8D hr.

22–25 °C, 14 L: 10D hr.

26 ± 1 °C, 65 ± 5% RH, 16 L: 8D Hr. Standard rearing conditions

Standard rearing conditions

Control

–

Mummified aphids stored i.e. pupal stage

7, 14, 28 and 42 days One day old mummies

0, 2, 4, 6 and 8 weeks Pupae

20 ± 1 °C, 70 ± 10% RH, 16 L: 8D hr. 20 ± 1 °C 70 ± 10% RH 16 L: 8D hr. 20 °C

25 ± 1 °C, 65–85% RH, 16 L: 8D hr. 1, 2 and 3 weeks 10 and 12 days old 26 ± 1 °C, pupae, 65–70% RH, 65 ± 10% RH full darkness 14 L: 10D hr. 1, 2, 3, 4, 6, 8, 10, 14, Pupae, acclimation for 21 °C, 16 L: 8D 18 and 22 weeks 2 days at 4 and 10 °C hr. No acclimation 1 to 7 weeks Pupae, 60 ± 10% RH 20 ± 1 °C, 60 ± 10% RH, 16 L: 8D hr. 1 and 2 weeks Pupae, 70 ± 5% RH 20 °C, 60 ± 5% RH, 16 L: 8D hr. 0, 5, 10, 15 and Pupae 18 ± 1 °C, 60% 20 days RH, 16 L: 8D hr.

4–6 day old mummies, (pre storage for one day at 15 °C), complete darkness 7, 14, 21 and 28 days Pupae, 60–75% RH, Full darkness

7, 15 and 30 days

3, 5, 7 and 14 days

0, 2, 7 and 14 days

5–30 days

5 days

1 to 8 months

Duration

Table 2 List of parasitoids examined for cold storage potential as immatures (eggs, larvae, prepupae or pupae)

Stray 1971

Bourdais et al. 2012

Amice et al. 2008

Colinet and Hance 2010

Ismail et al. 2013

Frere et al. 2011

Hofsvang and Hagvar 1977

Kidane et al. 2015

Lopez and Botto 2005

Bueno and van Cleave 1997

Whitaker-Deerberg et al. 1994

Waggoner et al. 1997

Easwaramoorthy et al. 2000

Benelli et al. 2017

Mills and Nealis 1992

Reference


Hymenoptera: Encyrtidae

Hymenoptera: Braconidae

Order: Family

Table 2 (continued)

Aphis fabae Scopoli Aphis gossypii Glover Macrosiphum euphorbiae (Thomas) –

Lysiphlebus fabarum (Marshall)

Lysiphlebus testaceipes (Cresson)

Praon volucre (Haliday)

Spodoptera litura L.

Bactrocera oleae 4, 6, 8, 10 and 12 °C (Rossi)

Microplitis prodeniae Rao and Chandry

Psyttalia humilis (Silvestri) Psyttalia ponerophaga (Silvestri)

Ooencyrtus nezarae Ishii

Aenasius arizonensis (Girault) (=A. bambawalei Hayat) Anagyrus ananatis Gahan

5, 10, 15 and 20 °C

10.1 and 14.8 °C Preconditioni-ng at 14.8 °C and 10 °C 2, 6 and 10 °C

Phaenacoccus solenopsis Tinsley Dysmicoccus brevipes (Cockerell)

0, 4 and 10 °C

5, 10, 15 and 20 °C

2.75 °C

5, 10, 20 and 40 days Egg, larvae and pupae

4 ± 1 °C Chilo partellus Swinhoe

1 and 8 weeks

4 ± 1 °C

1–30 days

2, 4, 6 and 8 weeks

1 to 8 weeks

1, 2 and 4 months

5–50 days

Host eggs

Pupae 75% RH

1-day-old mummies

Egg, young larva, old larva and pupa

Pupae

1/2, 1, 2, 3, 4, 5, 6, 7, Pupae, 68 ± 4% RH 8, 9, 10 and 11 days 10, 15, 20, 25 and Pupae 30 days

Pupae, 70 ± 5% RH

Late pupal stage

Pupae, 70 ± 5% RH and in constant darkness

1, 2, 3, 4 weeks

Cotesia flavipes (Cameron)

Bracon hebetor (Say)

1 and 2 weeks

7 °C constantly, 7 °C for 22 h. and 20 °C for 2 h. 5, 10, 15 and 20 °C

Ephestia kuehniella Zeller Galleria mellonella (L.)

Aphidius ervi (Haliday)

4, 8 and 12 °C

Tuta absoluta Meyrick

2, 5 and 10 °C

5 °C


Pupae, 50–60% RH, 14 L: 10D hr. 3 and 6 days old mummies, 70–80% RH 5, 10, 15 and 20 days Pre-pupae, 70 ± 10% RH, complete darkness 7, 4, 21, 28 and Pupae 35 days 7, 14, 21 or 28 days Pupae

Duration

6 °C and 6 °C + a daily 2 weeks exposure to 21 ± 1 °C for 2 h. 10, 7.2, 4.4 and 15, 30, 45, 60 and 1.7 ± 1 °C 90 days

Temperature

Storage conditions

Apanteles gelechiidivoris Marsh

Allorhogas pyralophagus Marsh

Laboratory Host

Scientific Name

25 ± 1 °C, 55 ± 5% RH 14 L: 10D hr. 26.6 C, 31.4 ± 0.6%

25 ± 1 °C, 70 ± 10% RH, 14 L: 10D hr. 24 ± 2 °C, 40–60% RH, 16 L: 8D hr. 27 °C, 75% RH

27 ± 2 °C, 75 ± 5% RH

20 °C, 60 ± 5% RH, 16 L: 8D hr. 29 ± 1 °C, 65 ± 5% RH 16 L: 8D hr. 26 ± 2 °C, 70 ± 5% RH, 12 L: 12D hr. 27 ± 1 °C, 12 L: 12D hr. 25 ± 2 °C, 70 ± 10% RH

22 ± 1 °C, 70 ± 10% RH, 12 L: 12D hr. Standard rearing conditions –

21 ± 1 °C, 65–75% RH, 16 L: 8D hr. Standard rearing conditions

Control

Mainali and Lim 2013

Pandey 2002

Rathee and Ram 2014, 2016

Daane et al. 2013

Yan et al. 2017

Manjoo and Bajpai 2012

Viel et al. 2008

Anwar et al. 2016

Alam et al. 2016

Al-Tememi and Ashfaq 2005

Ismail et al. 2010

Perdomo et al. 2017

Ballal et al. 1989

Lins et al. 2013

Archer et al. 1976

Mahi et al. 2017

Reference

Author's personal copy

Phytoparasitica

15 °C

Temperature

Storage conditions

Plodia 0, 5, 10 and 15 °C interpunctella (Hubner) Ephestia 5, 10 and 15 °C kuehniella Zeller Lygus hesperus 10 and 4 °C Knight Listronotus oregonensis LeConte Homalodisca vitripennis (Germar) Acrosternum arabicum Wagner Nezara viridula (L.)

Anaphes victus Huber

Psix saccharicola (Mani)

Trissolcus basalis (Wollaston) and Telenomus podisi Ashmead

Hymenoptera: Scelionidae

Gonatocerus ashmeadi Girault

Anaphes iole Girault

120, 150, 180 and 210 days

1 week

10, 20, 30 and 40 days

20, 40, 60 and 80 days

4.5, 6.0 and 7.5 °C

12 and 15 °C

Pupae, 70 ± 10% RH, continuous fluorescent lighting Pupae

Pupae 10 L:14D

Pupae

1-day-old parasitized host eggs

Second larval instar

1, 3, 6 and 9 days parasitized eggs

1, 3, 5, 7 and 15 days Pupae

Up to 216 h.

1 to 7 weeks

0, 3, 6 and 12 weeks

4, 8 and 12 °C

5-day-old parasitized pupae

4th instar larvae, preconditioning at 20–25 °C or at 12–15 °C, 10 h. photoperiod for 24–72 h. before storage 1 and 5 day old pupae

Larvae and pupae


7, 14, 21 and 28 days Pupae, 60% RH, 12 L: 12D hr.

10, 20 and 30 days

1 and 2 month

10–40 days

10 days

Duration

4 °C

4 °C

5, 10 and 15 °C

10 °C

Venturia canescens (Gravenhorst)

Diadegma insulare (Cresson)

Thripobius javae (Girault)

Tetrastichus brontispae (Ferriere)

7 and 10 °C

Liriomyza huidobrensis (Blanchard) Brontispa longissima (Gestro) Heliothrips haemorrhoidalis (Bouche) Plutella xylostella (L.)

Aphis craccivora 4 and 8 °C Koch

Riptortus pedestris (Fabricius) Graphosoma lineatum (L.)

Laboratory Host

Neochrysocharis formosa (Westwood)

Trioxys indicus Subba Rao & Sharma

Ooencyrtus pityocampae Mercet

Scientific Name

Hymenoptera: Platygastridae

Hymenoptera: Mymaridae

Hymenoptera: Ichneumonidae

Hymenoptera: Eulophidae

Order: Family

Table 2 (continued)

27 ± 1 °C

22 ± 1 °C, 10 L: 14D hr.


25 ± 1 °C, 60–70% RH, 16 L: 8D hr. 29 °C


25 ± 1 °C, 50 ± 10% RH, 12 L: 12D hr. 25 ± 2 °C, 70 ± 10% RH

25 ± 2 °C, 60 ± 5% RH, 16 L: 8D hr. 26 °C

26 and 30 °C, 75 ± 5% RH, 16 L: 8D hr. Standard rearing conditions

RH 16 L: 8D hr.

Control

Foerster et al. 2004

Forouzan et al. 2018

Chen et al. 2008b

van Baaren et al. 2005

Abdullah et al. 2009

Tunca et al. 2014

Press and Arbogast 1991

Okine et al. 1996

Bernardo et al. 2008

Liu et al. 2014

Saleh et al. 2010

Singh and Srivastava 1988

Binazzi et al. 2015

Reference


Trissolcus basalis (Wollaston)

Telenomus busseolae Gahan

Scientific Name

Trichogramma chilonis (Ishii) and Trichogramma achaeae Nagaraja and Nagarkatti Trichogramma chilonis (Ishii), Trichogramma achaeae Nagaraja and Nagarkatti, Trichogramma japonicum Ashmead and Trichogramma cordubensis Vargas and Cabello

Trichogramma chilonis (Ishii), Trichogramma japonicum Ashmead

Trichogramma cacoeciae Marchal, Trichogramma embryophagum Hartig Trichogramma carverae Oatman & Pinto, Trichogramma funiculatum Carver, Trichogramma brassicae Bezdenko Trichogramma chilonis (Ishii)

Hymenoptera: Trichogramma achaeae Nagaraja Trichogrammatidaand Nagarkatti, Trichogramma e chilonis (Ishii), Trichogramma japonicum Ashmead, Trichogrammatoidea eldanae Viggiani Trichogramma cacoeciae Marchal

Order: Family

Table 2 (continued)

Corcyra cephalonica (Stainton) Corcyra cephalonica (Stainton) Corcyra cephalonica (Stainton)

4 ± 1 °C

10 °C

4 and 8 °C

15 °C

6, 8, 10, 12, 14 and 16 °C

15 °C

Pupae

4 day old parasitized eggs

Pupae

Pupae, 65 ± 5% RH

5 day old parasitized eggs

5 day old parasitized eggs Host eggs and pupal stage of parasitoids 10, 15, 20, 25, 30, 35, Pupal stage, 75 ± 10% 40, 50 and 60 days RH 16 L:8D hr.

0, 1, 2, 3, 4, 5, 6 and 7 weeks

5, 10, 15, 20 25, 30, 35, 40, 45 days

5, 10, 15, 20, 25, 30, 5 day old parasitized 35, 40 and 45 days eggs 5, 10, 15, 20, 25, 30, Pupae 40 and 50 days

5, 10, 15, 20, 25, 30, 40, 50, 60, 70, 80 and 90 days Up to 57 days

6, 8, 10, 12, 14 and 16 °C At 27 ± 2 °C; and on day 7 at 8–10 °C

1 to 8 weeks

4, 8 and 10 °C

1 to 8 weeks 0–75 days at 5 day interval

0, 4 and 8 °C

Ephestia kuehniella Zeller Corcyra cephalonica (Stainton) Corcyra cephalonica (Stainton) Sitotroga cerealella (Olivier) Corcyra cephalonica (Stainton)

9, 11, 13 and 15 day old parasitized eggs


7, 14, 21 and 28 days Parasitized egg masses 60 ± 5% RH, full darkness 7, 14, 21, 28, 35, 42 Egg, early larval instar, and 49 days late larval instar, prepupal and pupal stage, 68 ± 4% RH

1, 2, 4, 6, 8, 10 and 12 weeks

Duration

6 °C

2, 5 and 10 °C

4, 8, 12, 16 and 20 °C

4, 8 and 12 ± 1 °C

Temperature

Storage conditions

Corcyra cephalonica (Stainton)

Sesamia nonagrioides (Lefebvre) Nezara viridula (L.)

Euschistus heros (Fabr.)

Laboratory Host

Bayram et al. 2005

Reference

Singhamuni et al. 2015

Bhargavi and Naik 2015

Vigneswaran et al. 2017

Dileep 2012

Khosa and Brar 2000

Nadeem et al. 2010

Rundle et al. 2004

Ahmad and Ahmad 2014

Ozder 2004

26 °C 75 ± 10% Ghosh and Ballal RH 12 L: 12D 2018 hr.



Standard rearing conditions 28 ± 1 °C 65 ± 5% RH

25 ± 2 °C 65 ± 5% RH 14 L: 10D hr. 27 ± 2 °C

25 °C, 60–70% RH, 16 L: 8D hr. 27 ± 1 °C 65 ± 5% RH 16 L: 8D hr. 25 °C 16 L: 8D hr.

28.0 ± 1 °C, Abdel-Salam et al. 70.0 ± 5% RH, 2014 14 L: 10D hr. 26 ± 1.5 °C, Jalali and Singh 66 ± 3.5% RH 1992

25 ± 2 °C, 70 ± 10% RH, 12 L: 12D hr. 26 ± 1 °C, 16 L: 8D hr.

Control


Phytoparasitica

Author's personal copy Gardner et al. 2012 25 °C 16 L: 8D hr.

Pitcher et al. 2002 Trichogramma ostriniae Pang and Chen

2 °C constantly, Alternating with 20 °C for 3 h./day Ephestia kuehniella Zeller

3, 6, 9, 12 and 15 °C

1, 2, 4, 6 and 8 weeks Pre-pupae, preconditioned for 6 days at 24 °C, 16 L: 8D hr. 1, 2, 3, 4, 5, 6, 7 and Parasitized host eggs 8 weeks

Pupae, 75 ± 5% RH and in full darkness 25, 50, 75, 100, 125 and 150 days

Sitotroga cerealella Olivier Sitotroga cerealella (Olivier) Trichogramma nerudai Pintureau and Gerding

Temperature

Laboratory Host Scientific Name Order: Family

Table 2 (continued)

Storage conditions

Duration


Control

25 ± 1 °C 75 ± 5% RH 14 L: 10D hr. 24 °C, 16 L: 8D hr.

Reference

Tezze and Botto 2004

Phytoparasitica

pupae of T. brontispae [host: coconut hispine beetle, Brontispa longissima (Gestro)] could be stored up to 30 days at 10 °C without any significant and adverse effect on mean adult emergence and parasitism performance. Rathee and Ram (2014) reported that mummies of Phaenacoccus solenopsis Tinsley i.e. the parasitoid A. bambawalei in pupal stage could be stored for 1, 2 and 3 weeks at 5, 10 and 15 °C, respectively, without any adverse effect on parasitoid adult emergence when compared with control i.e. 27 °C (100%). Bhargavi and Naik (2015) reported that trichocards with eggs parasitized by T. chilonis and Trichogramma japonicum Ashmead could be stored effectively without much damage to the adult emergence up to 15 days at 15 °C. The percentage emergence of Encarsia sophia (Girault and Dodd) from pupae kept at 12 °C for a week was not affected. However, at lower temperatures (8 and 4 °C) percentage emergence after two weeks of storage decreased to 67–87.5% and after three weeks none emerged (Kidane et al. 2015). Singhamuni et al. (2015) reported that pupal stage of T. chilonis and Trichogramma achaeae Nagaraja and Nagarkatti within parasitized Corcyra cephalonica (Stainton) eggs could be stored for up to 2 weeks at 4 °C and 4 weeks at 8 °C while maintaining at least 70% adult emergence. Likewise, Cagnotti et al. (2018) reported that T. nerudi could be stored for up to 50 days without affecting adult emergence at 5 °C with previous acclimation for 20 days at 12 °C. Emergence rate of T. brassicae adults from stored parasitized host eggs decreased gradually as the cold storage duration advanced (0, 30, 60, 90 and 180 days) at 4 °C (Rahimi-Kaldeh et al. 2017). Yan et al. (2017) reported that cold storage regime of 10 days at 10 °C had no adverse effect on the survival of Microplitis prodeniae Rao and Chandry and parasitoid adult emergence was greater than 50% even after 20 days at 10 °C. Considering a minimum 60% emergence rate and 3 days of longevity Ghosh and Ballal (2018) concluded that the optimum duration for storing the pupae of T. chilonis, T. japonicum and T. achaeae was 30 days, while Trichogramma cordubensis Vargas and Cabello recorded 40 days of storage suitability at 10 °C. No emergence occurred in storage at 4.4 or l.7 °C (Archer et al. 1973) and 5 °C (Rathee 2014). In most of the studies, parasitoids did not emerge when the immature stages of the same species were stored for more than 4 weeks at 5 °C (Singh and Srivastava 1988; Rundle et al. 2004 and Bayram et al. 2005; Rathee and Ram 2014; Queiroz et al. 2016). Nadeem (2010) and Rathee

Hymenoptera: Braconidae

Hymenoptera: Encyrtidae

Encarsia formosa Gahan Trialeurodes vaporarorium Westwood and Eretmocerus corni Haldeman Glyptapanteles militaris Mythimna unipuncta (Walsh) (Haworth)

6, 8 and 10 °C 1, 2 and 4 months

4 ± 1 °C

Bactrocera oleae (Rossi)

Galleria mellonella (L.)

Musca domestica L., Chrysomya putoria (Wiedemann) Phenacoccus madeirensis Green

Tachinaephagus zealandicus Ashmead Anagyrus sp. nov. nr. sinope Noyes and Menezes Aenasius arizonensis (Girault) (= A. bambawalei Hayat) Phaenacoccus solenopsis Tinsley

Dichomeris eridantis Meyr.

Copidosoma varicorne (Nees)

Apanteles Tuta absoluta Meyrick gelechiidivoris Marsh Anagyrus kamali Moursi Maconellicoccus hirsutus Green

Psyttalia humilis (Silvestri) Psyttalia ponerophaga (Silvestri) Bracon hebetor (Say)

3, 5 and 7 °C

Ephestia kuehniella Zeller

Adults

Adults

1 to 8 weeks

0, 1, 4, 7, 14 and 21 days

15 and 25 °C

5, 10, 15 and 20 °C

1, 2, 6, 12 and 24 days

48–216 h.

1, 4, 7, 10 and 14 days

15 °C

11 ± 1 °C

20 ± 2° and 27 ± 2 °C

25 ± 1 °C, 60 ± 10% RH, 12 L: 12D hr.


27 ± 2 °C, 60 ± 10% RH, 12 L: 12D hr.


27 ± 1 °C, 12 L: 12D hr.

24 ± 2 °C, 40–60% RH, 16 L: 8D hr.

25 ± 1 °C, 65 ± 5% RH 16 L:8D hr.

28 °C

25 ± 1 °C, 60 ± 5% RH, 12 L: 12D hr.


25 ± 1 °C, 65–85% RH, 16 L: 8D hr.


Control

Freshly emerged adults fed with honey

27 °C, 75% RH

Adults fed with honey 25 °C solution

Adults, 60–75% RH Full darkness

Adults fed with honey solution Adults, 40% RH

4, 8 and 12 °C 7, 14, 21 and 28 days Adults

5, 10, 20 and 40 days Adults

Pharate adults

10, 20, 30, 40, 50 and Adults 70 days 1, 2, 3 and 4 weeks Adults

5 ± 1 °C

Galleria mellonella (L.)

Habrobracon hebetor (Say)

7 and 15 days

Achoria grisella Fabricius

6 ± 1 °C

Adults fed weekly


7, 14, 21 and 28 days Adults, 60–75% RH

15, 30, 60, 90, 105 and 120 days

Duration

15, 20, 25 and – 30 °C

4.5 ± 2 and 11.5 ± 2 °C

10, 7.2, 4.4 and 1.7 °C

Temperature

Storage conditions

Apanteles galleriae Wilkinson

Diuraphis noxia (Kurdjumov)

Aphelinus asychis Walker

Hymenoptera: Aphelinidae

Laboratory Host

Scientific Name

Order: Family

Table 3 List of parasitoids examined for cold storage potential as adults

Rathee et al. 2015

Chong and Oetting 2006

Almeida et al. 2002

Prasad and Ansari 2000

Sagarra et al. 2000

Perdomo et al. 2017

Anwar et al. 2016

Daane et al. 2013

Seyahooei et al. 2018

Chen et al. 2011

Uckan and Gulel 2001

Oliveira et al. 1998

Lopez and Botto 2005

Archer et al. 1976

Reference


Phytoparasitica

0, 30, 60, 90 and 180 days

4 and 10 °C

1 to 4 weeks

1, 2, 3, 4 and 5 days

10 °C

Ephestia kuehniella Zeller

Egg laying females, 20% honey water, preconditioning at 20 ± 1 °C and 10 L: 14D hr.

Adults, 70 ± 5% RH and in constant darkness Adults, 60–70% RH

Adults

Adults

1, 2, 4, 6, 8, 10 and 12 weeks 120, 150, 180 and 210 days

Adults

1, 2, 4 and 8 weeks

4 ± 1 °C

15 and 18 °C

10, 7.2, 4.4 and 1.7 °C 4, 8 and 12 ± 1 °C

Nezara viridula (L.) Euschistus heros (Fabr.)

Trichogramma – cacoeciae Marchal, Trichogramma brassicae Bezdenko and Trichogramma evanescens (Westwood) Trichogramma brassicae Ephestia kuehniella Zeller Bezdenko

Trissolcus basalis (Wollaston) Telenomus podisi Ashmead Hymenoptera: Trichogramma Trichogrammatidae evanescens (Westwood)

Anaphes ovijentatus Lygus hesperus Knight (Crosby and Leonard) Telenomus busseolae Sesamia nonagrioides (Lefebvre) Gahan

Hymenoptera: Scelionidae

10, 20, 30, 40, 50 and Adults fed with 50% 60 days honey

1, 3, 5, 7 and 15 days Adults

5, 10 and 15 °C 2, 4 and 5 °C

Adults


Ephestia kuehniella Zeller Plodia interpunctella Hubner Homalodisca vitripennis (Germar)

Duration

1 and 2 month

Temperature

Storage conditions

Liriomyza huidobrensis (Blanchard) 7 and 10 °C

Neochrysocharis formosa (Westwood) Venturia canescens (Gravenhorst) Gonatocerus ashmeadi Girault

Hymenoptera: Eulophidae Hymenoptera: Ichneumonidae Hymenoptera: Mymaridae

Laboratory Host

Scientific Name

Order: Family

Table 3 (continued)

Chen et al. 2008a

Tunca et al. 2014

Saleh et al. 2010

Reference

20 ± 1 °C, 70 ± 5% RH, 16 L: 8D hr.

Rahimi-Kaldeh et al. 2017

Ozder 2008

Yilmaz et al. 2008

27 ± 1 °C, 70 ± 5% RH


Foerster and Doetzer 2006

25 ± 2 °C, 70 ± 10% RH 12 L: 12D hr.

26 ± 1 °C, 70 ± 20% RH, Jackson 1986 14 L: 10D hr. 26 ± 1 °C, 16 L: 8D hr. Bayram et al. 2005

25 ± 2 °C, 60 ± 5% RH 16 L: 8D hr. 25 ± 1 °C, 60–70% RH, 16 L: 8D hr. 22 ± 1 °C, 14 L: 10D hr.

Control


3, 6.5 and Myzus persicae 10 ± 0.5 °C Sulzer Acyrthosiphon pisum (Harris) Coccinella Aphis craccivora 6 °C undecimpunctata L. Koch Coleomegilla maculata Ephestia kuhniella 4 and 8 °C lengi Zeller Timberlake – 15 °C Cryptolaemus montrouzieri Mulsant Harmonia axyridis Aphis craccivora -3, 0, 3 and 6 °C (Pallas) Koch Acyrthosiphon pisum 6 °C (Harris) Rodolia cardinalis Icerya seychellarum 6, 10 and 14 °C (Mulsant) (Westwood)

Neuroptera: Chrysopidae

Hemiptera: Pentatomidae

Podisus nigrispinus (Dallas) Ceraeochrysa cubana (Hagen), Ceraeochrysa smithi (Navas)

Podisus maculiventris (Say), Podisus sagitta (Fabricius) Podisus maculiventris (Say)

Perillus bioculatus (Fab.)

Diptera: Cecidomyiidae Hemiptera: Anthocoridae

60% RH, complete darkness Larvae 60–70% RH Adults, full darkness and 60–70% RH

15, 30, 45 and 60 days 1 to 5 weeks 5,10, 15 and 20 days

4 and 10 °C 5, 13 and 15 °C 4.5, 7.2, 10, 12.8 and 15.6 °C

– Myzus persicae Sulzer

5, 10, 15 and 20 days 3 weeks

1 to 10 weeks

Eggs, 70–75% RH

Eggs, nymphs and adults, complete darkness, 75% RH Eggs, 70 ± 10% RH

Egg masses and adults, 50 and 95% RH

4 and 9 °C

6 days

5th instar nymphs and adults 70 ± 10% RH Nymphs

30, 60, 90, 120 and Adults, full darkness 150 days and 60–70% RH 1 to 6 months Adults, complete darkness 5, 10, 15, 20, 30 Larvae and pupae and 40 days 70 ± 5%RH 16 L: 8D 10, 20, 30 and Adults 70% RH full 40 days darkness 8 months Nymphs, total darkness

Eggs, 85–95% RH


1–3 weeks

Duration

2, 4, 6, 8, 10, 12, 14, 16, 18 and 20 days 9, 12 and 15 ± 1 °C 2, 4, 6, 8, and 10 days

5, 8, 10 and 12 ± 1 °C

1 to 11 °C

4 and 12 °C

Trichoplusia ni (Hubner)

Leptinotarsa decemlineata (Say) –

Rhyzobius lophantae Aspidiotus nerii Blaisdell Bouche Aphidoletes aphidimyza Aphids (Rondani) Orius insidiosus (Say) Anagasta kuehniella (Zeller)

Coccinella septempunctata L. Adalia bipunctata L.

Temperature

Storage Conditions

Coleoptera: Coccinellidae

Laboratory Host

Scientific Name

Order: Family

Table 4 List of predators examined for cold storage as adults or immatures

Ozgokce et al. 2006

Abdel-Salam and Abdel-Baky 2000 Gagne and Coderre 2001

Hamalainen and Markkula 1977

Reference

Bueno et al. 2014

Gilkeson 1990

Senal et al. 2017

24 ± 1 °C, 70–75% RH 16 L: 8D hr.

Lopez-Arroyo et al. 2000

Costa et al. 2016

Coudron et al. 2007

26 °C, 75% RH 16 L: 8D hr. 25 ± 1 °C

De Clercq and Degheele 1993

23 °C, 75 ± 5% RH 14 L: 10D hr.

20 ± 1 °C, 65 ± 10% RH Ladurantaye et al. 2010 16 L: 8D hr.

25 ± 1 °C, 70% RH 12 L: 12D hr.

21 °C, 16 L: 8D hr.

26 ± 1 °C, 60% RH

25 ± 1 °C, 70% RH Ruan et al. 2012 12 L: 12D hr. 20 °C, 70% RH 18 L: Awad et al. 2013 6D hr. 25 °C 70 ± 5% RH 16 L: Abdel-Baky et al. 2015 8D hr.


28 ± 2 °C, 75 ± 5% RH, 14 L: 10D hr. 24 °C, 60–75% RH 16 L: 8D hr.

20, 28 and 35 °C, 80–90% RH

Control


Phytoparasitica

Author's personal copy Nadeem et al. 2014

Amaral et al. 2013

25 ± 2 °C, 65 ± 5% RH 14 L: 10D hr.

25 ± 1 °C, 70% RH 12 L: 12D hr. 25 °C, 75% RH 14 L: 10D hr.

Adults

1–3 day old eggs, 70% RH Adults and eggs, constant darkness and 75% RH

Nadeem 2010 25 ± 1 °C, 65 ± 5% RH 14 L: 10D hr. Eggs and pupae

Thysanoptera: Aeolothripidae

Chrysoperla externa (Hagen) Franklinothrips vespiformis (Crawford)

Anagasta kuehniella (Zeller) Ephestia kuehniella Zeller

6, 8, 10, 12, 14 and 5, 10, 15, 20, 25, 16 °C 30, 40, 50, 60, 70, 80 and 90 days 6, 8 and 10 °C 5, 10, 15, 20, 25, 30, 40, 50, 60, 70, 80 and 90 days 12 °C 5, 10, 15, 20, 25 and 30 days 5.5, 7, 8.5, 10 10, 20 and 30 days and 12.5 °C Sitotroga cerealella (Olivier) and Chrysoperla externa (Hagen) Chrysoperla carnea (Stephens)

Temperature

Duration


Reference Control Storage Conditions Laboratory Host Scientific Name Order: Family

Table 4 (continued)

Larentzaki et al. 2007

Phytoparasitica

and Ram (2014) reported that cold storage of pupal stages of T. chilonis and A. bambawalei, respectively, was not feasible for even a week at 20 °C, which might be due to faster immature development at high temeperature leading to adult emergence before completion of storage duration (Ismail et al. 2010). Development time Time taken by the entomophagous insects to emerge post cold storage has been reported to decrease as the storage temperatures increased (Mills and Nealis 1992; Whitaker-Deerberg et al. 1994; Pandey 2002; AbdelSalam et al. 2014; Rathee and Ram 2014). In other words, development time of the entomophagous insects significantly increased with extending the storage period at low temperatures (Gagne and Coderre 2001; Ismail et al. 2010; Nadeem et al. 2010; Abdel-Salam et al. 2014; Rathee and Ram 2014; Tunca et al. 2014; Costa et al. 2016; Benelli et al. 2017; Perdomo et al. 2017; Cagnotti et al. 2018). For instance, the length of the life cycle of Lysiphlebus testaceipes (Cresson) and A. pyralophagus increased 3 to 4 and 2 to 6 fold, respectively by cold storage (Archer et al. 1973; Ballal et al. 1989). Post-storage time to emerge for the tachinid Ceranthia samarensis lengi Timberlake, a parasitoid of gypsy moth, decreased with longer cold storage periods and with higher post-storage incubation temperatures (Mills and Nealis 1992). Whitaker-Deerberg et al. (1994) evaluated that time taken to emerge for both male and female parasitoid adults from the mummies of A. aschysis held at 4.4 °C for 3, 5, 7 and 14 days decreased as the storage period advanced. Similarly, Gupta and Bhardwaj (2002) also reported that storage of Trichogrammatoidea bactrae Nagaraja at 15 °C for 10 days after 5 days of parasitization was appropriate. Pandey (2002) and Rathee and Ram (2014) reported that males of the parasitoids A. ananatis and A. bamabawalei, respectively, took less time to emerge post cold storage as compared to the females. Similarly, Bernardo et al. (2008) who studied storage of pupae of T. javae at 10 °C, reported that residual development time from pupa to adult after transfer to 25 °C decreased gradually as the storage duration increased. Ismail et al. (2010) concluded that immature stage continued development to some extent during storage at lower temperatures but development rate was higher during storage at higher temperatures. Rathee and Ram (2014) also reported similar results for A. bambawalei under cold


storage conditions. Development time of tachinid parasitoid, Exorista larvarum (L.) could be extended by 5– 7 days when immatures on artificial media were stored at 15 and 20 °C for 5 days or until pupation as compared to control i.e. 26 °C (Benelli et al. 2017). Cagnotti et al. (2018) reported that T. nerudi could be stored for up to 50 days without affecting time taken to adult emergence at 5 °C with previous acclimation for 20 days at 12 °C. Adult longevity In general, the post storage longevity of the entomophagous insects has been reported to decrease as the storage period increased at cold storage temperatures (Rudolf et al. 1993; Venkatesan et al. 2000; Al-Tememi and Ashfaq 2005; Amice et al. 2008; Yilmaz et al. 2008; Daane et al. 2013; Rathee and Ram 2014; Abdel-Baky et al. 2015; Sandanayaka et al. 2015; Alam et al. 2016; Anwar et al. 2016; Nahiyoon et al. 2016; Perdomo et al. 2017; Yan et al. 2017). Reduced longevity indicates susceptibility of eggs, larvae or pupae to cold storage over time. Females tended to live longer than their male counterparts after removal from cold storage temperatures in majority of the studies conducted worldwide (Jayanth and Nagarkatti 1985; Pitcher et al. 2002; Colinet et al. 2006; Rathee and Ram 2014). Ballal et al. (1989) during cold tolerance studies on cocoons of A. pyralophagus reported that 10 °C seemed to be the most suitable storage temperature with respect to adult longevity. Similar findings have been reported by Jalali and Singh (1992), Rundle et al. (2004), Bernardo et al. (2008) and Ismail et al. (2010). Rathee and Ram (2014) also concluded that the parasitoid A. bambawalei could be stored in the pupal stage for one week at 5 °C and for 3 weeks each at 10 and 15 °C, without significant effect on the male and female longevity. Kidane et al. (2015) stored 10-day -old pupae of En. sophia at 8 and 12 °C for 1, 2 and 3 weeks and reported that the longevity of the adults that emerged from pupae after one week of storage at 12 and 8 °C was not affected, but decreased to 66–72% with increase in storage time. The storage of immatures of E. larvarum, either for 5 days or until pupation at 20 °C, negatively and significantly affected the longevity of the resulting females, about 5 days less than the control (Benelli et al. 2017). Host parasitization The rate of parasitism is usually quantified by providing parasitoids unlimited numbers of hosts. It represents

another means of testing fecundity. Contrary to fecundity, which refers to an absolute number of eggs or progeny produced, the per cent parasitism refers to the proportion of host parasitized among a colony. It thus takes into account the steps of foraging behavior such as host recognition, acceptance and discrimination. Several studies have reported reduction of per cent parasitism with increasing duration of cold storage (Khosa and Brar 2000; Riddick 2001; Larios et al. 2002; Pitcher et al. 2002; Ozder 2004; Bayram et al. 2005; Al-Tememi and Ashfaq 2005; Kumar et al. 2005; Nadeem et al. 2010; Muhammad et al. 2013; Rathee and Ram 2014; Singhamuni et al. 2015). Similar reduction in the ability of individuals to parasitize eggs has also been noted in the fields (Rundle et al. 2004). The reproductive organs are particularly vulnerable to low temperature (Flanders 1938; Denlinger and Lee 1998). For example, in Euchalcidia caryobori (Hanna), exposure to low temperature caused retardation of egg maturation or, in its extremes, malformation of reproductive organs was noiced in both the sexes (Hanna 1935). Male sterility due to cold stress is an important concern that has been reported in several parasitoid species (Levie et al. 2005). This is more important in the sense that female parasitoids generally mate only once, and mating with a sterile male would result in unsuccessful fertilization (Colinet and Hance 2009). Decrease in fecundity of various entomophagous insects has been reported as the storage period increased at cold storage temperatures (Khosa and Brar 2000; Venkatesan et al. 2000; Ozder 2004; Abdel-Gawad et al. 2010; Manjoo and Bajpai 2012; Daane et al. 2013; AbdelSalam et al. 2014; Ahmad and Ahmad 2014; Kidane et al. 2015; Alam et al. 2016; Anwar et al. 2016; Vigneswaran et al. 2017; Yan et al. 2017). Possibly, there is a reduction of body fat reserves during storage at low temperatures affecting the performance of adults with respect to body mobility and consequently affecting parasitism (Couillien and Gregoire 1994; Colinet 2007; Colinet et al. 2007). Rathee and Ram (2014) reported that A. bambawalei could be stored in the pupal stage for one week at 5 °C and for 3 weeks each at 10 and 15 °C, without significant effect on the male and female longevity as compared to control i.e. at 27 °C. Jalali and Singh (1992) reported that fecundity of Trichogramma spp. declined drastically after storage of 14 days each at 2 and 5 °C and after 21 days of storage at 10 °C when exposed to room temperature. Ballal et al. (1989), Kumar et al. (2005) and Liu et al. (2014) also


reported that A. pyralophagus, T. brasiliense and T. brontispae could be stored at 4, 5 and 10 °C, respectively, for one week without adversely affecting their parasitization. Lopez-Arroyo et al. (2000) reported that newly laid eggs of the three neuropteran predators, Ceraeochrysa cubana (Hagen), Ceraeochrysa smithi (Navas) and Chrysoperla externa (Hagen) could be held for approximately 2 weeks at 15.6 °C without any affect on post-storage reproductiveness. Coudron et al. (2007) reported that storage of P. maculiventris second instar larvae at 8 °C for 4 weeks did not reduce their predation capacity, when larvae were returned to 24 °C. Prey-fed P. maculiventris adults were able to withstand cold storage at 10 °C for 4 weeks with very little loss of survival and fecundity. Similarly, Pitcher et al. (2002) reported that rate of parasitism by stored T. ostriniae was generally similar to controls after 2 to 4 weeks storage at 9 and 12 °C but declined with storage longer than 4 weeks. Geden and Kaufmann (2007) using cold-killed pupae stored at 4 °C for a period of up to 2 months obtained parasitism approximately 80% of that obtained with Spalangia cameroni Perkins on live pupae of Musca domestica L. Hackermann et al. (2008) reported that Hyssopus pallidus (Askew), an ectoparasitoid of codling moth, could be cold stored for 14 days without any negative effect on its parasitism and reproductive capacity. Bernardo et al. (2008) found that the fecundity of T. javae adults emerged from stored pupae and fed on honey was reduced significantly after 14 days of storage at 10 °C. Silva et al. (2013) reported that D. rapae mummies could be stored for up to 24 days at 5 °C, at which time the per cent parasitism remained above 38%. The percentage parasitism of Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) by S. cameroni was also unaffected by whether the pupae had been killed recently by cold shock or had been stored at between 4 °C and 6 °C over 15 or 30 days (Tormos et al. 2010). Gryon pennsylvanicum (Ashmead) successfully parasitized Leptoglossus occidentalis Heidemann eggs stored at 4 °C up to six months, while no offsprings were produced when eggs were stored for 12 months (Peverieri et al. 2015). The female counterparts in case of parasitoids are the effective sex as far as biological control of any pest is concerned; hence, importance of female progeny emerging from cold stored parents is of utmost importance for enhancing the field efficacy of entomophagous insects. Low temperatures frequently distort insect sex ratios (Denlinger and Lee 1998). Hymenopteran parasitoids usually possess haplodiploid sex-determination system,

female being able to choose the sex of their progeny by controlling fertilization (Flanders 1956). Distortion of sex ratio may come from different origins. First a modification of the proportion of fertilized eggs oviposited (i.e. primary sex ratio) may be observed following modification of the female reproductive strategy or the inability of males to mate (Colinet and Hance 2009) or to produce viable sperm (Lacoume et al. 2007) after a cold stress. Sex ratio distortion can also result from a differential mortality between sexes when immatures are exposed to cold (i.e. secondary sex ratio). The proportion of females in F1 progeny of cold stored parasitoids has been reported to decline as the storage duration increases at low storage temperatures (Rathee 2014). Riddick (2001) also concluded that cold storage of C. marginiventris pupae for 20 days can limit the production of female progeny. Rathee and Ram (2014) and Pitcher et al. (2002) during cold storage studies on A. bambawalei and T. ostriniae, respectively, reported that the per cent emergence of female progeny from cold stored parents declined after 4 weeks of storage. Ballal et al. (1989), Bayram et al. (2005), Al-Tememi and Ashfaq (2005), Amice et al. (2008), Abdel-Gawad et al. (2010), Ismail et al. (2010), Abdel-Salam et al. (2014), Anwar et al. (2016), Nahiyoon et al. (2016), Queiroz et al. (2016), Mahi et al. (2017), Forouzan et al. (2018) and Seyahooei et al. (2018) during cold storage studies on immature stages of A. pyralophagus, T. busseolae, B. hebetor, Aphidius picipes Nees, T. evanescens, A. ervi, T. basalis, B. hebetor, Dirhinus giffardii Silvestri, T. remus, Lysiphlebus fabarum Marrshall, Psix saccharicola (Mani) and H. hebetor, respectively found that the sex-ratio of F1 progeny became more male biased with increasing length of storage treatment and consisted of only males when stored longer. This is of great concern for storage practices, since the number of females must be maximized for parasitoid release (Hassan et al. 1990; Tezze and Botto 2004; Mahi et al. 2017; Seyahooei et al. 2018).

III. Effect of cold storage during adult stage on biological characteristics and fitness of the entomophagous insects Survival and mortality In general, most of the studies revealed that survival of the adult entomophagous insects decreased as the


storage duration increased (Rawat et al. 1992; Tauber et al. 1993; Bayram et al. 2005; Larentzaki et al. 2007; Ruan et al. 2012; Chen et al. 2013; Daane et al. 2013; Nadeem et al. 2014; Rathee et al. 2015; Senal et al. 2017). Nonetheless, in some studies, adults were found to be more resistant to cold storage than juveniles (Abdel-Salam and Abdel-Baky 2000; Riddick 2001; Bayram et al. 2005; Coudron et al. 2007; Anwar et al. 2016). Males were more susceptible than females and with an increase in storage duration mortality increased (Jalali et al. 1990; Uckan and Gulel 2001; Rathee et al. 2015). Jayanth and Nagarkatti (1985) stored adults of B. brevicornis at 5 °C for 30, 60 and 90 days and reported 12.40, 47.37 and 54.66% mortalities, respectively. It is suggested that the faster depletion of energy reserves in males may cause death or low survival rates during prolonged storage periods (Storey and Storey 1988). In addition, a higher storage tolerance of females could be related to their larger body size, which may contribute to their longer survival at low temperatures (Queiroz et al. 2016). Jackson (1986) stored adults of Anaphes ovijentatus (Crosby and Leonard), a Lygus hesperus parasitoid for 1, 2, 4 and 8 weeks at 1.7, 4.4, 7.2 and 10 °C and found that adults survived for 1 week at all storage temperatures but at 4.4 °C survival of males (100%) and females (98.3%) was judged the best. More females survived than males at 7.2 and 10 °C. Jalali et al. (1990) studied the survival of Cotesia marginiventris (Cresson) adults at low temperatures and found that mortality of females was higher at 5 °C (2.3, 18, 66%) as compared to 10 °C (2, 13, 59%) for 10, 20 and 30 days of storage, respectively. A temperature of 6 ± 1 °C was suitable for keeping adults of C. bijugus for up to 100 days (Rawat et al. 1992). De Clercq and Degheele (1993) successfully stored adults of P. maculiventris and P. sagitta at 9 °C for 1 month without affecting survival, longevity and reproduction. The diapausing adults of C. carnea were stored with success at 5 °C for 31 weeks (Tauber et al. 1993). AbdelSalam and Abdel-Baky (2000) reported higher survival of cold stored C. undecimpunctata adults when fed with aphids after 5 days (100–15%) and 10 days (100–35%) of emergence prior to storage (7–60 days), as compared to storage of freshly emerged and unfed adults (25– 10%) for 7–30 days at 6 °C. Prasad and Ansari (2000) stored freshly emerged male and females of C. varicorne at 11 ± 1 °C and recorded increased mortality rates as the storage duration advanced. Uckan and Gulel (2001) investigated that 85.27% of A. galleriae

adults died after a week and all the adults died within 15 days when stored at 6 °C. Larentzaki et al. (2007) successfully stored adults of the predatory thrips F. vespiformis for 3.5 weeks at 10.0 and 12.5 °C without adversely affecting their survival. Bernardo et al. (2008) reported that temperatures of storage lower than 15 and 10 °C had detrimental effects on adults of T. javae. Chen et al. (2008a) stored the Gonatocerus ashmeadi Girault adults at 2, 5 and 10 °C and showed that these parasitoids did not survive at 2 °C for 5 days. The lethal time (LT)50 (i.e. length of storage time for 50% wasp survival) at 5 °C was 14 days for males and 29 days for females, whereas at 10 °C, (LT)50 for males and females was 32 and 39 days, respectively. Ruan et al. (2012) conducted long term cold storage experiments with adults of the Asian lady beetle, Harmonia axyridis (Pallas) and concluded that after 150 days of storage, survival reduced to 50% at 0 °C while it was more than 82% at 3 and 6 °C, may be due to cold hardiness via cold acclimation or supercooling (Pervez and Omkar 2006). Likewise, O. insidiosus adults could be stored up to 10 days at 8 °C without any adverse effect on their survival (Bueno et al. 2014). Rathee et al. (2015) reported that A. bambawalei adults could be stored only for 1 week at 10 °C without any significant effect on the survival. Anwar et al. (2016) stored eggs, larvae, pupae and adult of ectoparasitoid, B. hebetor at 4 ± 1 °C and life stages of the wasp stored at 27 ± 1 °C acted as control for 5, 10, 20 and 40 days. Highest survival of 24.00 ± 1.41 was observed during storage of adult wasps at 4 °C followed by pupae (20.00 ± 1.41); however larvae and eggs could not survive to adult stage after 40 days cold storage treatment. Mansour (2017) stored adults of B. hebetor at 12 °C and reported that wasps’ mortality increased as storage duration (0, 1, 2, 3 and 4 months) increased and males showed higher percentages of mortality than females. Senal et al. (2017) successfully stored Rhyzobius lophantae Blaisdell adults, natural enemy of most armored scales of Diaspididae family, for 10 days at 4 °C (94.54%) and 12 °C (88%) with comparable survival to unstored adults (100%). Thereafter, survival decreased up to 40 days of storage (61.59%) at 12 °C, while at 4 °C, 100% mortality was recorded after third week of storage. Adult longevity Reduction in the longevity of entomophagous insects after cold storage has been reported many workers


worldwide (Jayanth and Nagarkatti 1985; Jalali et al. 1990; Abdel-Salam and Abdel-Baky 2000; Yilmaz et al. 2008; Bernardo et al. 2008; Ozder 2008; Chen et al. 2013; Daane et al. 2013; Nadeem et al. 2014; AbdelBaky et al. 2015; Anwar et al. 2016; Senal et al. 2017). Yigit et al. (1994) reported that C. montrouzieri adults lived maximum 10 days at 7 °C and 22 days at 15 °C. Nourished and hydrated female Anagyrus sp. nov. nr. sinope parasitoids survived an average of 52.8 days at 15 °C, which was 14 and 8 times longer than starved and hydrated females, respectively (Chong and Oetting 2006). Ozgokce et al. (2006) found that the longevity, total fecundity and daily reproduction of C. montrouzieri adults kept at 15 °C for 5 days were 69.7, 686.7 and 9.8, respectively. Bernardo et al. (2008) studied that when adults of T. javae were stored for more than 10 days, at 15 °C, residual longevity reduced significantly. Likewise, Yilmaz et al. (2008) stored T. evanescens adults at 10 °C for 1 to 4 weeks and reported that the longevity of parental adults and their F1 progeny decreased depending on the length of the storage period. Similarly, Chen et al. (2011) stored the newly emerged females of ectoparasitoid, H. hebetor at 5 ± 1 °C and reported that parental longevity decreased after more than 20 days of storage. Post-storage longevity of A. bamabwalei adults (19.20 and 33.00 days, respectively, for male and female) recorded after one week of storage at 10 °C were comparable with the control (27 °C) (Rathee et al. 2015). Female parasitoids tended to live longer than the males after removal from cold storage temperatures (Rathee et al. 2015; Senal et al. 2017). For instance, females of the coccinellid predator, R. lophantae survived longer than males after storage for 20, 30 and 40 days at 4 and 12 °C (Senal et al. 2017). However, prolonged storage periods had negative effects. Host parasitization In general, storage of adults at low temperature significantly decreased their fecundity with an increase in storage duration. For instance, A. asychis adults stored for 15 days reproduced at the same level as unstored adults, but reproduction declined as the length of storage increased (Archer et al. 1976). C. carnea and C. externa adults were successfully stored at 5 and 10 °C for 30 and 90 days, respectively by Tauber et al. (1997a) and Tauber et al. (1997b) without affecting parasitization potential. Likewise, Almeida et al. (2002) reported that

Tachinaephagus zealandicus Ashmead reared on the third instars of Chrysomya putoria (Wiedemann) could be stored at 15 °C for 12 days with no appreciable loss of fecundity. Bayram et al. (2005) also suggested that T. busseolae adults could be successfully stored up to 12 weeks although with some reduction in per cent parasitism at 8 and 12 °C temperatures. Storage of T. cacoeciae, T. brassicae and T. evanescens adults at 4 ± 1 °C reduced the fecundity of female parasitoids at all storage durations (1, 2, 3, 4 and 5 days) (Ozder 2008). Saleh et al. (2010) studied the effect of cold storage (7 and 10 ± 0.5 °C) on the adults of Neochrysocharis formosa (Westwood) and found the fertility of the mass produced parasitoids after one year of rearing reduced by about 23%. Interestingly, storage of mated female predators, O. insidiosus resulted in a much higher post-storage fecundity than storage of virgin females (Bueno et al. 2014). Cold stored H. axyridis lady beetles had higher predation capacity than unstored adults (Ruan et al. 2012). T. brontispae females stored at 13 ± 1 °C for eight days or longer had lower parasitism rates compared to the control (25 °C) (Tang et al. 2014). Similarly, Jayanth and Nagarkatti (1985), Jalali et al. (1990), Abdel-Salam and Abdel-Baky (2000), Venkatesan et al. (2000), Riddick (2001), Chang et al. (2003), Foerster and Doetzer (2006), Coudron et al. (2007), Awad et al. (2013), Daane et al. (2013), Nadeem et al. (2014) and Senal et al. (2017) reported that fecundity of cold stored adults decreased as the storage period increased. Higher numbers of females than males are considered important in biological control programs because males do not contribute directly to parasitism-induced decline in pest populations (Navarro 1998). In general, storage at low temperatures significantly increased the rate of males in progeny of cold stored adults as the duration advanced. After mating with cold-stored males, female parasitoids may produce only male progeny (i.e. unfertilized eggs), possibly because of male sterility (Rigaux et al. 2000; Levie et al. 2005; Pandey and Johnson 2005) as cold stress may cause alteration of sperm production or reproductive organs. Almeida et al. (2002) reported that males were dominant in the F1 progeny of cold stored T. zealandicus adults at 25 °C. Chen et al. (2013) investigated the effects of long-term cold storage (1 to 8 weeks) on the performance ectoparasitoid H. hebetor at 5 °C and recorded lower percentage of females in the F1 progeny of cold stored insects than the unstored insects (36% vs. 52%). Sagarra et al. (2000),


Riddick (2001), Uckan and Gulel (2001) and Rathee et al. (2015) also concluded that longer storage durations had male preponderance in F1 progeny. Contradictory to the trend, Anwar et al. (2016) reported that sex ratio in B. hebetor became female biased by increasing cold storage duration at 4 ± 1 °C.

increasing demand from farmers, who are progressively moving away from chemical pesticide use to organic agriculture. Innovations in cold storage methods (short or long-term) in near future may lead to a reduction in cost incurred for the production of the biological control agents, thereby ensuring year-round availability and making biological control easier, more economical and ready to apply.

Future prospects of cold storage Cold storage techniques have been undoubtedly fruitful in mass rearing, prolonging survival and stockpiling viable natural enemies since innovated for the first time. In future, improvised techniques and specific insulated cold packings need to be standardized for entomophagous fauna including inscects, mites, nematodes etc. Along with the fitness related parameters; behaviour, morphology and physiology of the test insects need to be studied to improve their storage. Cryogenic procedures for long-term storage in liquid nitrogen by determining chilling tolerance, supercooling points, membrane permeability, cryoprotectants and post-storage recovery requirements need to be devised in future. Moreover, quality control, market facilities, government policies and farmers knowhow regarding importance of entomophagous insects must be improved to ensure widespread use of stockpiled natural enemies.

Conclusion Cold storage tolerance is a highly plastic trait influenced by a range of biotic and abiotic factors experienced before, during and after cold exposure. For the successful implementation of any cold storage project, knowledge of these diverse factors that cause post-storage effects is essential. This review elaborates various documented factors that must be taken into account while designing cold storage protocols. In addition, the fitness indicators such as mortality, per cent emergence, time taken to emerge, longevity, fecundity and sex ratio might be affected by cold storage and therefore impact the effectiveness of the parasitoid and biological control programmes. Ultimately, the success of a storage method depends on the field performance of the cold stored entomophagous insects. Unfortunately, there are very few studies that have assessed post-storage performances through field survey. Augmentative biological control is likely to grow rapidly because of the

Acknowledgements Thanks are extended to Dr. (Mrs.) Asha Kawatra, Dean, Post Graduate Studies, CCSHAU, Hisar for providing necessary and handful library facilities. We would like to acknowledge the other faculty members of the Department of Entomology for their needful help in compiling this review. No funds have been provided from any source. Compliance with ethical standards Conflict of interest The authors declare that they have no conflict of interest.

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