OUTLOOKS ON PEST MANAGEMENT

INSECT PEST MANAGEMENT IN POSTHARVEST ECOSYSTEMS IN THE UNITED STATES OF AMERICA

Frank H.Arthur,Judy A. Johnson, Lisa G. Neven, Guy J. Hallman and Peter A. Follett1 Considerthe problems and solutions to postharvest pest management

of the kernel. Acomplete list of potential insect pests, as well Keywords: Post-harvest, , control, management, quarantine as information on the biology and range, can be found in Rees (2004). Insect pests in postharvest systems in the United States of Actual monetary losses due to stored-grain insectsare America (USA), which can include bulk grains in storage, generally consideredtobeinthe range of 5to10% of the and also the milling, processing, storage, and retail bulk commodities stored in the USA or about $1.25 to 2.5 industries, account for millions of dollars of losses each year billion (Flinn et al.2007). Management strategies for in direct and indirect costs. Insect pests in harvested fresh controlling insectsinbulk grains include cleaning and commodities can lead to huge economic losses due to sanitation of empty bins, use of aresidual grain protectant rejections of shipments, restrictions on shipments, reduction insecticide as grains are loaded into storage, samplingthe of market quality,and reduction of market price. Reduction bins by direct sampling or with the use of probe pitfall traps, in pest risk to exported fresh commodities as aphytosanitary aeration with low-volume ambient air to lower the internal measure involves some key postharvest steps. Some of the bulk temperature of agrain mass, and fumigation with major insect pests are common to different postharvest phosphine when needed (Hagstrum et al.1999). systems while others are unique to one particular system. In As bulk grains are milled, processed, and distributed, the this article, the major postharvest insect pests and their insect pest complex changes and shifts as well. In millingand impacts will be discussed for grains and processed grain processing facilities, Tribolium castaneum,the red flour products, tree nuts, and fresh fruit crops. beetle, and T. confusum,the confused flour beetle, are major pests. Perhaps the most important economic pest of processed foods products is Plodia interpunctella,the Indian Insect pest managementinbulk grains and meal , which can exist on awide variety of food processed grain products products (Mohandass et al.2007). Other beetle species can In the USA, the most economically-damaging insect pests are cause economic damage as well (Throne et al.2003). the lesser grain borer, Rhyzopertha dominica, Economic losses caused by insects in the processing, distribution, and storage system are estimated as millions of dollars resulting from contamination issues, product returns, legal issues associated with infestations, pest control applications, and consumer complaints (Throne et al.2003). However,actual quantificationofsuch losses is extremely difficult to assess because they are largely borne by private industry.Control of insects in this system is usually accomplished through fumigations of facilities or applications of aerosol insecticides and residual surface treatments (Arthur 2008). Sampling and monitoring is also emphasized as part of management programs, and there are anumber of recent studies that document extensive insect pest populations in and around milling, processing, and storage facilities (Campbell &Mullen 2004), and interpreting the data obtained from trapping and monitoring Figure1. Adult lesser grain borer (Rhyzopertha dominica) programs (Nansen et al.2008). on wheat. Footnote 1 and Sitophilusoryzae and S. zeamais,the rice weevil and the All of the authors areresearch entomologists with the USDA-Agricultural Research Service (ARS). Frank H. Arthur is with the Grain Marketing and maize weevil, respectively.These species feedinternally, cause Production Research Center in Manhattan, KS. Judy A. Johnson is with the San product damage,and when the mature adult exits the kernel, Joaquin ValleyAgricultural Sciences Center in Parlier,CA. Lisa G. Neveniswith it creates alarge hole. There are anumber of beetle pests that the Yakima Agricultural Research LaboratoryinWapato,WA. Guy J. Hallman is with the Kika de la Garza Subtropical Agricultural Research Center in Weslaco, are external feeders and spend their entire life cycle outside TX. Peter A. Follett is aresearch entomologist with US Pacific Basin Agricultural Research Center in Hilo,HI. DOI: 10.1564/20oct00 Outlooks on Pest Management–October 2009 1 ©2009. Research Information Ltd. All rights reserved INSECT PEST MANAGEMENT IN POSTHARVEST ECOSYSTEMSINTHE UNITED STATES OF AMERICA

Insectpest managementintreenuts and dried 2002). fruit Before allowing entrance of productinto their markets, Dried fruits and tree nuts are used in baked goods and other importing countriesmay require phytosanitary certification confectionaries, and as snack foods. after inspection for live insects, therefore processors often ensure passing inspection by applying adisinfestation treatment, usually fumigation. For time-sensitive markets, such as inshell walnuts for the valuable European Union holiday market, methyl bromide has been preferred because of its rapid treatment times. Restrictions on the useofmethyl bromide imposed by the Montreal Protocol (Fields &White 2003) have limited its availabilitytodried fruitand nut processors, who are moving to phosphine or sulfuryl fluoride when possible. However, recentfindings have implicated sulfuryl fluoride as being apotentially important greenhouse gas (Mühle et al.2009), and Californiahas begun regulating field fumigations in an attempt to reduce volatile organic compounds (CDPR 2008). Suggested non-chemical alternatives for phytosanitary treatmentsinclude radio frequency (Wang et al.2007a; 2007b), low temperatures (Johnson 2007), controlledatmospheres(Soderstrom& Brandl 1990), combination treatments (Soderstrom et al. Figure2. Almond orchardinbloom. 1996; Johnson et al.1998; 2002), and vacuum treatments (Mbata &Phillips 2001). Both taste and appearance are extremely important to the As with grain products, it is difficult to estimate the actual perceived quality of these products and there is no tolerance economic loss due to insects in dried fruits and nuts. Aegerter for live insects. The discovery of live insects may result in &Folwell (2001) estimated fumigation costs for almond customer returns, loss of consumer confidence,rejection of processors to be $5.01-5.03/ton for methyl bromide and shipments, and loss of entire markets. Driedfruits and tree $5.47-5.88/ton for phosphine, whileestimates forwalnut nuts may be kept for many months in storage and as such processors were $8.11-9.47/ton for methyl bromide. Other they have several storage pests in common with stored grains control costs may include sanitation and aerosol fogging, but and processed food products, particularly P. interpunctella, the cost of customer returns and the resulting loss of T. castaneum,and Oryzaephilus surinamensis,sawtoothed customer confidence and legal costs must be considered as grain beetle. These pests may infest the product at any time well. during processing and storage, and, if undetected and uncontrolled, populations may build up rapidly.Inaddition, these commoditiesoften have field pests such as Amyelois transitella,the navel orangeworm, Cydia pomonella,the codling moth, Cadra figuliella,the raisin moth, and Carpophilus spp., dried fruit beetles. Any of these species or acombinationmay be present in harvested product and survive processing stages.Although field pests rarely reproduce or persist under commercial storage conditions, their presence poses aserious phytosanitary risk in exported Insect pest managementand quarantine in raw product. postharvest fruitand vegetables Marketing of these products for both foreign and domestic Rhagoletis indifferens,the western cherry fruit fly,isthe markets requires careful attention to sanitation, packaging, major pest of sweet cherries in the western USA. Although and storage to prevent insect infestation. As with storedgrain C. pomonella is listed as aquarantine pest in cherries facilities andmills,monitoring insect populations with destined to , recent research indicates that sweet pheromone trapping programs can help in making cherries are not ahost for this pest (Wearing 2001; Hansen management decisions. Entire warehouses may be fumigated, &Rehmke 2003; Johnson &Hansen 2008). Although C. either on acalendar basis or in response to changes in trap pomonella has rarely been positivelyidentified in sweet numbers, to reduce storage pest populations. Processors may cherries within the past twenty years, fruit exported to Japan limit the introductionofinsects into processing facilitiesby muststill be fumigated with methyl bromide to meet fumigating all incoming product, and finished product may quarantine requirements. In thefield, thereisazero receive afinal fumigation before shipment.With some tolerance level for R. indifferens,and fruit from any orchards products, particularlytree nuts with high oil content like with positive trap catches, or harvested cherries that test walnuts, refrigerated storage (0-5°C) maybeusedto positive for the presence of R. indifferens are ineligible for maintain productquality.Thesetemperatures are also export (Hass 2001). The cherries are then usually diverted to effective at reducing insect infestations (Johnson et al.1998; processing.

2Outlooks on Pest Management–October 2009 INSECT PEST MANAGEMENT IN POSTHARVEST ECOSYSTEMS IN THE UNITED STATES OF AMERICA

Cydia pomonella, Grapholita molesta,the oriental fruit quarantine for Anastrepha suspensa,the Caribbean fruit fly, moth, and A. ludens,the Mexicanfruit fly,respectively.

Figure3. Dead 4th instar oriential fruit moth Grapholita molesta Figure4.Asystems approach will control Mexican fruit fly Anastrepha following CATTS treatment of nectarines ludens (Photo by Jack Dykinga, USDA-ARS). and R. indifferens are the major pests of apples and stone Aphytosanitary systems approach is the primary means of fruits. Rhagoletis pomonella,the apple maggot, and overcoming quarantine, but when it is insufficient,cold or Conotrachelusnenuphar,the plum curculio, are major pests methyl bromide fumigation are used. Alternatives to methyl of appleseast of the Rocky Mountains. In the Pacific bromide are sought because, although the fumigant has been Northwest, G. molesta is not found in apples and is rarely exemptedfrom Montreal Protocol-induced phase out for found in commercial peaches andnectarines.Stone fruits postharvest phytosanitary uses, this status could certainly from this area are shipped under asystems approach to meet change in the futureorthe fumigant could become difficult import restrictionstoCanada. This system approach involves to obtain (Heather &Hallman 2008). Domestic quarantines aseries of safeguardstoprogressively reducerisk to an are imposed for Rhagoletis mendax,the blueberry maggot, insignificantlevel. Cold storage of apples is widely accepted on blueberries, and C. nenuphar on several fruits shipped for insect control. The potential presence of insects in export from the eastern USA to western states. Anumber of tropical apples is managed by asystems approach or methyl bromide and subtropical fruitsfrom Florida are quarantined for fumigation. shipment to several states where A. suspensa or other pests Citrus fruit from Florida and Texasissubject to may become established if introduced.

Ta ble1.Comparison of various commercial and experimental phytosanitarytreatments (After Hallman 2007). In another categoryirradiation is different because,unlikeall other treatments listed, pests areexpected to be aliveupon inspection, which creates particular regulatoryissues (Heather &Hallman 2008).

Treatment Commodity tolerance Cost Acceptance by organic industryLogistics of application Speed of application Cold Moderate LowYes Easy Very slow Heated air Moderate Moderate Ye sModerate Moderate Hot water immersion Moderate LowYes Moderate Fast Radiofrequency heating Moderate Moderate Ye sModerate Fast Ionizing radiation High Moderate No Moderate Fast Methyl bromide fumigation Moderate LowNoEasy Fast Sulfuryl fluoride fumigation LowLow No Easy Fast

Phosphine fumigation (solid formulations) LowLow No Easy Moderate Phosphine fumigation (gaseous formulations) Moderatelylow?Low No Easy Moderate

Modified atmosphereModerate Moderate Ye sModerate Slow Modified atmosphere/heat Moderate Moderate Ye sModerate Fast Non-gaseous pesticides High LowNoEasy Fast

Outlooks on Pest Management–October 2009 3 INSECT PEST MANAGEMENT IN POSTHARVEST ECOSYSTEMSINTHE UNITED STATES OF AMERICA

Methyl bromide fumigation and prolonged cold storage postharvest quarantine treatment such as heat, cold, or are the only commercially practiced postharvest quarantine irradiation before export to the USA mainland. has treatments used for pome fruits and stone fruits in the USA export approvals for more than 100 fresh fruits, vegetables, even though alternative treatments have been developed, and herbs, and 26 of them require apostharvest treatment to including irradiation (Drake &Neven 1997, 1998, Hallman control quarantine pests (Table 2). Postharvest treatments 2004, Mansour 2003, Hallman 2007, Hallman &Hellmich have been developed mainly against fruit flies, but other 2009) (Table 1) and the Controlled Atmosphere internal pests or surface feeders may also require control /TemperatureTreatment System) (CATTS) (Neven 2005; (Follett&Neven 2006). For example, papaya is ahost for Neven et al.2006; Neven &Rehfield-Ray 2006a; b). The fruit flies, but exported fruit must also be free of CATTS treatment is aregime of high-temperature forced air Pseudaulacaspis pentagona,the whitepeach scaleand combined with amodified atmosphere consisting of 1% Paracoccus marginatus,the papaya mealybug. Euscepes oxygen and 15% carbon dioxide. Possible reasons for the postfasciatus,the West Indian weevil and lack of adoption of the alternatives include availability of anastomosalis,the sweetpotato vine borer are the technology,compliance with organicstandards(as is the case main quarantine pests of Hawaii’sunique purple-fleshed withirradiation), logistics in switchingtoalternative variety of sweet potato. Sternochetus mangiferae,the mango technologies, cost or complexity of operation relative to seed weevil must be controlled in mangoes in addition to existing control methods. The CATTS treatments for apples, fruit flies before mangoes can be exported (Follett &Neven sweet cherries, peaches, and nectarinesare to date the only 2006). modified atmosphere treatmentsthat areapproved for Hawaii was aforerunner in the use of irradiation to export quarantine. fresh fruits and vegetables, and currently 24 fruits and

Ta ble2.PhytosanitaryTreatments (Includes Non-Host status) forHawaiian fruits and vegetables.

Fruit Name Treatment Fruit Name Treatment Abiu ILongan H, I Poutertai caimito Dimocarpus longana Atemoya ILychee H, I Annona squamosa x.A. Litchi chinensis cherimola Avocado CMangoI Persea americana Mangiferaindica Banana I, NMangosteen I Musa acuminata Garcinia mangostana Breadfruit IMelons I Artocarpus incus Cucurbita spp. Carambola C, IMoringa I Averrhoa carambola Moringa thouarsi Citrus H, IPapayaH,I Citrus spp. Carica papaya Cowpea IPeppers I Cucurbita spp. Capsicum spp. Dragon fruit IPineapple H, I, N Hylocereus polyrh Ananas comosus Durian NRambutan H, I Durio zibethinus Nephelium lappaceum Eggplant ISapodilla I Solanum melongena Manilkarazapota Jackfruit ISweet potato F, I, N Artocarpus heterophyllus Ipomoea batatas To mato I Lycopersicon esculentum

All fruits andvegetables from Hawaii are under federal vegetables have approvalsfor export with irradiation quarantine regulations due to presence of four invasive treatment(Table 2). The construction of an irradiation tephritid fruit flies: Ceratitiscapitata,the Mediterranean facilityinHawaii designed to treat fresh produce has been fruit fly, Bactrocera dorsalis,the oriental fruit fly, Bactrocera beneficial to the tropical fruit and vegetables industries.For cucurbitae,the melonfly and Bactrocera latifrons,the example, irradiationprovided an alternativefor sweet solanaceous fruit fly (Follett &Armstrong 2004). Fruit flies potatoes to methyl bromide fumigation, subsequently sweet lay clusters of eggs under the skin of the fruit and larvae feed potato production doubled and currently approximately internally on the pulp, making visual inspection for 3.94 million kg of sweet potatoes per year are exported using infestation difficult. Therefore, fruit fly hosts must receive a irradiation treatment (Follett 2006).

4Outlooks on Pest Management–October 2009 INSECT PEST MANAGEMENT IN POSTHARVEST ECOSYSTEMS IN THE UNITED STATES OF AMERICA

pome fruits. The insect pests and associated control strategies can vary among these separate areas, primarily because of the quarantine aspects relating to the export of fresh fruits. Various treatments may be required as acondition of export. Regardless, the cost of infestation, detection, control, and management of insect pests in postharvest commodities and fruits can range in the millions of dollars because of the economic value of these products in the US agricultural system.

Acknowledgment This paper reports the results of research only.Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not implyrecommendationorendorsement by the US Department of Agriculture. Figure5. Sweet potato weevil Cylas formicarius elegantulus,a quarantine pest. Recently,USDA-APHIS approved generic doses of 150 Grays References (Gy) for tephritidfruit flies and 400 Gy for all insects except Aegerter A. F. &FolwellR.J.(2001). Selected alternatives to pupa and adult (USDA-APHIS 2006). For methyl bromide in the postharvest and quarantine commodities using the 400 Gy treatment, lowering thedose treatment of almonds and walnuts: an economic may be beneficial to save money on treatment costs and to perspective. J. Food Process. Preserv. 25:389-410. minimize any adverse effects on quality (Wall 2008). Arthur F. H. (2008). Aerosol distributionand efficacy in a Reducing the dose from 400 to 150 Gy on sweet potatoes commercial food warehouse. Insect Sci. 15:133-40. resulted in a60% cost savings to the commercial x-ray [CDPR] California Department of Pesticide Regulation radiation facility and increased profitsfor growers and (2008) ReducingVOC emissions from field fumigants. shippers (Follett 2006). http://www.cdpr.ca.gov/docs/dept/factshts/voc_rules_11_ Hawaii must prepare pest risk assessments similar to those 08.pdf (Accessed 30-03-2009) required by foreign countries before trade in anew Campbell J. F. &Mullen M. A. (2004). Distribution and commodity is considered, including the evaluation of the dispersal behavior of Trogoderma variabile and Plodia likelihoodofentry,establishment, or spread of apest or interpunctella outside afood processingplant. J. Econ. disease within the territory of the importing nation according Entomol. 97:1455-64. to the phytosanitary measures that might be applied, and of Devorshak C. &Griffin R. (2002).Role and relationship of the associated potential for biological and economic official and scientific information concerning peststatus. consequences (Devorshak &Griffin 2002). The suite of In Invasive in Agriculture: Problems and quarantine pests identified by risk assessment varies Solutions, eds. Hallman G. J. &Schwalbe C. P. pp. 51-70. depending on the commodity,the country of origin, and the Enfield Science Publishers, Enfield NH, USA. importing country. Drake S. R. &Neven L. G. (1997). Quality responses of Overcoming foreign phytosanitary barriers to trade is often ‘Bing’ and ‘Rainier’ sweet cherries to low dose electron more difficult than domestic barriers. The former are beam irradiation. J. Food Process. Preserv. 21:345-51. sometimes accused of being protectionist barriers that are not Drake S. R. &Neven L. G. (1998). Irradiation as an scientifically defensible (Heather &Hallman 2008). Fruits alternative quarantine treatment for stone fruits. J. Food such as apple, cherry,orange, and grapefruit are exported in Qual. 21:529-38. large quantities across quarantine barriers using Fields P. G. &White N. D. G. (2003). Alternatives to methyl phytosanitary measures. For example, Florida has exported bromide treatments for stored-product and quarantine over 200 million kg/year of grapefruit to Japan using acold insects. Ann. Rev.Entomol. 47: 331-59. treatmentdone in ship transit or aphytosanitary system that Flinn P.W.,Hagstrum D. W.,Reed C. &Phillips T. W. (2007). reduces pest risk to negligible levels. Although research with Stored Grain Advisor Pro: Decision support system for irradiation has been done for many key quarantine pests in insect management in commercial grain elevators. J. the USA (e.g., Drake &Neven 1998; Follett 2006a; Hallman Stored Prod. Res. 43:375-83. 1994) no foreign trading partnerhas yet to receive produce Follett P. A. (2006a). Irradiation as amethyl bromide irradiatedfor phytosanitary purposes from the USA. alternativefor postharvest control of (Lepidoptera:Pyralidae) and Euscepes postfasciatus and Cylas formicarius elegantulus Summary (Coleoptera: Curculionidae) in sweet potatoes. J. Econ. Postharvest entomology and control can involve grain and Entomol. 99:32-7. grain based commodities, tree fruits and nuts, and citrusand Follett P. A. (2006b). Irradiation as aphytosanitary

Outlooks on Pest Management–August 2009 5 ©2009. Research Information Ltd. All rights reserved INSECT PEST MANAGEMENT IN POSTHARVEST ECOSYSTEMS IN THE UNITED STATES OF AMERICA

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