Radiation Biology and Inherited Sterility of Light Brown Apple Moth (Lepidoptera: Tortricidae): Developing a Sterile Insect Release Program
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HORTICULTURAL ENTOMOLOGY Radiation Biology and Inherited Sterility of Light Brown Apple Moth (Lepidoptera: Tortricidae): Developing a Sterile Insect Release Program RAJENDRA SOOPAYA,1 LLOYD D. STRINGER,2,3 BILL WOODS,1 ANDREA E. A. STEPHENS,2,4 2 1 1 2 RUTH C. BUTLER, IAN LACEY, AMANDIP KAUR, AND DAVID M. SUCKLING J. Econ. Entomol. 104(6): 1999Ð2008 (2011); DOI: http://dx.doi.org/10.1603/EC11049 ABSTRACT The radiation biology of two geographically isolated populations of the light brown apple moth [Epiphyas postvittana (Walker)] was studied in Australia and New Zealand as an initiation Յ of a SIT/F1 sterility program. Pharate and 2 d pre-emergence pupae were exposed to increasing radiation doses up to a maximum dose of 300 Gy. Fertility and other life history parameters were measured in emerging adults (parental) and their progeny (F1-F3 adults). Parental fecundity was signiÞcantly affected by increasing irradiation dose in pharate pupae only. For both populations, parental egg fertility declined with increasing radiation. This was most pronounced for the irradiated parental females whose fertility declined at a higher rate than of irradiated males. At 250 Gy, females Յ 2 d preemergence pupae produced few larvae and no adults at F1. No larvae hatched from 250 Gy-irradiated female pharate pupae. At 300 Gy, males still had residual fertility of 2Ð5.5%, with pharate pupae being the more radio-sensitive. Radiation-induced deleterious inherited effects in offspring from irradiated males were expressed as increased developmental time in F1 larvae, a reduction in percent F1 female survival, decreased adult emergence and increased cumulative mortality over Ն subsequent generations. Males irradiated at 150 Gy produced few but highly sterile offspring at F1 Ͼ and mortality was 99% by F2 egg. KEY WORDS Epiphyas postvittana, irradiation, sterile insect technique, inherited sterility, eradi- cation Despite progress in border management and surveil- Tortricid moth larvae are among the most devas- lance, the likelihood of exotic moth incursions into tating pests of fruits and vegetables (Van der Geest new areas continues to be high because of increasing and Evenhuis 1991, Vreysen et al. 2006). Their estab- cross border trade. Historically, eradications of exotic lishment in horticultural crops can result in consider- Lepidoptera have been achieved through intensive able economic loss from crop damage, extra control use of broad-spectrum insecticides, but current social costs and market access restrictions. Light brown ap- acceptance for indiscriminate use of broad-spectrum ple moth Epiphyas postvittana (Walker) (Lepidop- insecticides has raised concerns about toxicological tera: Tortricidae) is a member of this family. Indige- effects in the environment and on human health nous to south eastern Australia (Common 1970), it has (Brockerhoff et al. 2010). In addition, the intensive use gradually established in other parts of Australia, in- of insecticides has led to the development of pesticide cluding Western Australia. Elsewhere, it is a wide- resistance (Giliomee and Riedl 1998). There is grow- spread and important leafroller pest in New Zealand ing pressure from consumers, farmers and the com- and is present in the British Isles, Sweden, and Hawaii munity to develop new, or reÞne, current environ- and recently in California (Suckling and Brockerhoff mentally and socially acceptable tools for pest 2010). It is widely polyphagous, feeding on hosts such population suppression. as Rosales and Fabales (Suckling and Brockerhoff 2010). In Australia and New Zealand it is an important pest of apples (Malus domestica Borkh.), pears (Pyrus spp.), stonefruits, citrus, and grapes (Vitis spp.) 1 Department of Agriculture and Food of Western Australia (Wearing et al. 1991). Damage includes defoliation, (DAFWA), Baron-Hay Court, South Perth, WA 6151, Australia. 2 The New Zealand Institute for Plant & Food Research Limited, fruit scarring, fruit drop, and an increase in suscepti- Private Bag 4704, Christchurch 8140, New Zealand. bility of injured plants to disease. Presence of any life 3 Corresponding author, e-mail: lloyd.stringer@plantandfood. stage in shipments can have adverse market access co.nz. implications. 4 Department of Zoology & Biodiversity Research Centre, Univer- sity of British Columbia, 6270 University Blvd., Vancouver, British Biological control, mating disruption, and the sterile Columbia, V6T 1Z4, Canada. insect technique (SIT) are potential alternative tactics 0022-0493/11/1999Ð2008$04.00/0 ᭧ 2011 Entomological Society of America 2000 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 104, no. 6 to broad-spectrum insecticides for use against exotic F1 progeny are produced in the Þeld, they are likely lepidopteran incursions. Biological control is a sus- to be in developmental synchrony, thus emerging at tainable pest management tactic, but it is a poor stra- the same time as the wild population, targeting the tegic Þt with emergency responses to new incursions next generation effectively. Inherited sterility is seen because of the time taken to search for natural ene- as an effective and environmentally safe tactic for mies and assess their nontarget effects before approval lepidopteran pest suppression that is useful under a for release. Mating disruption using pheromones to variety of environmental conditions, crop production disrupt mate Þnding in Lepidoptera is being widely strategies, and is compatible with many pest control used for area-wide pest management (Witzgall et al. tactics (Carpenter 1993). 2008), as well as to slow moth spread (Sharov et al. Coordinated radiation biology studies were under- 2002). Over large areas it is most efÞcient to apply this taken on two geographically-isolated light brown ap- technology aerially, although this has proven to be ple moth populations from Australia and New Zea- socially unacceptable in California (Suckling and land. This was done to verify results using similar Brockerhoff 2010). The sterile insect technique (SIT) methodologies between the two laboratories. The ef- is a sustainable technology that has been used suc- fects of increasing doses of gamma radiation on fe- cessfully against a variety of dipteran pests, particu- cundity and fertility on parental (P) pupae and larly the Mediterranean fruit ßy, Ceratitis capitata radiation-induced inherited effects on subsequent (Wiedemann) (Krafsur 1998) and the New World progenies were assessed using standard methods as far screwworm, Cochliomyia hominivorax (Coquerel) as possible. These results can be used to initiate a (Klassen and Curtis 2005). In addition, SIT may work full-sterility or F1 inherited sterility program against synergistically with other socially acceptable tools this tortricid. that target different life stages of a pest species, such as biological control targeting eggs and larvae (Car- penter et al. 2004), biopesticides such as Bacillus thu- Materials and Methods ringiensis (Bt), and mating disruption (Suckling and Test Insects and Rearing Technique Brockerhoff 2010). Lepidopteran species are more radio-tolerant than New Zealand (NZ). The New Zealand moths were many other insect orders (LaChance 1985, Bakri et al. obtained from a Plant & Food Research laboratory- 2005) and the large dose of radiation required to reared colony that was raised on a modiÞed Singh diet achieve full sterility may reduce their competitiveness (Singh 1983) at 20ЊC, 60% Ϯ 5% RH, and a photoperiod and performance in the Þeld (Suckling et al. 2011). In of 16:8 (L:D) h. The colony was kept disease free by spite of this disadvantage, successful operational SIT washing the eggs in 5% formalin and pupae in 1.5% programs have been implemented against cotton pest chlorine. At the time of the trial, the colony was in its pink bollworm Pectinophora gossypiella (Saunders) in 143th generation. California (Simmons et al. 2007), codling moth Cydia Western Australia (WA). The light brown apple pomonella (L.) in British Columbia, Canada (Bloem et moth laboratory colony was sourced from the al. 2005), and the painted apple moth Teia anartoides South Australian Research & Development Institute Walker in New Zealand (Suckling et al. 2007). (SARDI) and was in its 21st generation at the time of One approach to circumvent the negative effects the Þrst trial. Eggs were washed in a solution of 0.1% associated with the high radio-resistance of lepidop- sodium hypochlorite and allowed to hatch on an ar- Њ teran pests is to take advantage of inherited or F1 tiÞcial diet as described by Singh (1983) at 20Ð25 C, sterility. This genetic phenomenon among Lepidop- 65Ð70% RH, and a daily photoperiod of 14:10 (L:D) h. tera is characterized by the development of dominant Upon pupation, pupae were collected 1Ð2 d after ini- lethal genes in offspring from partially sterile parents. tiation, washed with a 0.1% sodium hypochlorite so- This is expressed by higher sterility than their parents, lution and left to mature at a temperature 25ЊC, 70% lower fecundity, longer larval development times, RH, and a daily photoperiod of 14:10 (L:D) h. higher mortality, and a skewed F1 sex ratio in favor of Irradiation Method. The irradiation studies were males (North 1975, LaChance 1985, Carpenter et al. undertaken in two different laboratories: the Depart- 2001a). As female moths are more sensitive to radia- ment of Agriculture and Food of Western Australia tion than males, in species where separation of the (DAFWA) in Perth, and Plant & Food Research sexes is difÞcult, doses can be adjusted so that females (PFR), Lincoln, New Zealand. are rendered completely sterile and males only par- In Western Australia, pupae were irradiated by ex- tially so for release. Male moths irradiated at sub- posure to gamma radiation by using a Cobalt60 Gam- sterilizing doses have reasonable ßight Þtness and are macell 220 irradiator (Atomic Energy of Canada Ltd., thus more likely to be competitive, bringing about Ottawa, Canada). Pupae were placed in a plastic vial better control than fully sterile but poorly physically (3.5 cm in diameter) on top of a jug used to support competitive counterparts (Kean et al. 2008, Suckling the dosimeter at midpoint in the Gammacell (IAEA et al.