Stewart Postharvest Review

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1 Stewart Postharvest Review An international journal for reviews in postharvest biology and technology Recent advances in development of ultralow oxygen treatment for postharvest pest control on perishable commodities Yong-Biao Liu USDA-ARS, Salinas, California, USA Abstract Purpose of review: This review summarises and discusses recent research progress in controlled atmosphere (CA) treatment with ultralow oxygen (ULO) for postharvest pest control on perishable commodities. Findings: In the last 0 years few studies have been conducted on ULO treatment for postharvest pest control. However, significant progress has been made and several ULO treatments were developed for postharvest pest control on different types of perishable products. Complete control of green peach aphid, sweetpotato whitefly, twopotted spider mite and western flower thrips was achieved with 8 h fumigation using >99% nitrogen without injury to begonia seedlings. Lettuce aphid, western flower thrips and black widow spiders were successfully controlled on head lettuce, broccoli and table grapes, respectively, without negative impact on product quality. Vine mealybug was successfully controlled without reducing the vitality of grape benchgrafts. The tolerance of lettuce to ULO treatment was increased through postharvest storage to improve the safety of ULO treatment. ULO treatment is promising for controlling selected pests on selected fresh commodities, especially on those that are evaluated for their vitality rather than appearance. Directions for future research: More research efforts should be directed towards identifying suitable pests and fresh commodities for ULO treatment. Emphasis should also be given to pest control on products such as rootstocks, bulbs and tubers, which are evaluated by vitality rather than appearance. Research should also be directed at enhancing the tolerance of commodities to CA treatment in order to make ULO and other CA treatments safer to product quality. Large scale studies and collaboration with industry are also vital for industrial adaptation of ULO treatment. Keywords: ultralow oxygen; controlled atmosphere; hypoxia; insect; postharvest pest control; quarantine treatment; lettuce Abbreviations CA ULO Controlled Atmosphere Ultralow Oxygen Correspondence to: Yong-Biao Liu, USDA-ARS, E. Alisal St., Salinas, CA 9905, USA. Tel: ; Fax: ; yongbiao.liu@ars.usda.gov Stewart Postharvest Review 00, :9 Published online 0 September 00 doi: 0./spr Introduction Controlled atmosphere (CA) treatment has been studied for postharvest pest control in the last several decades. However, both research efforts and progress are very limited, judged by the small number of publications and lack of successful treatments [, ]. In ultralow oxygen (ULO) treatments, pests as well as products are exposed to an atmosphere with the oxygen level well below % for certain lengths of time at certain temperatures to kill target pests. Similar treatments are also referred to as anoxia, hypoxia or nitrogen fumigation in literature. In ULO treatments for perishable commodities, the oxygen level is held at certain concentrations to ensure complete control of target pests and prevent or reduce potential negative effects on the quality of treated commodities. In other cases such as treatment of 00 Stewart Postharvest Solutions (UK) Ltd.

2 Liu / Stewart Postharvest Review 00, :9 Table. Summary of ULO treatments for pest control on perishable commodities. Commodity Pest and life stages ULO treatment Pest mortality (%) Lettuce Lettuce aphid, (nymph, adults) Nasonovia ribisnigri T ( C), 5, 0 Oxygen (%) Time (day) Negative impact on commodity References [] Western flower thrips, (larva, adult) Frankliniella occidentalis 5 0, 8, % with heartleaf injury % with heartleaf injury 8% with heartleaf injury [5] Lettuce (fresh) (Stored for week) Western flower thrips, (larva, adult) F. occidentalis % with heartleaf injury [7] Fresh (Stored for days) (Stored for days) (Stored for 5 days) % with heartleaf injury [8] Broccoli Western flower thrips, (larva, adult) F. occidentalis Off-odour [9] Table grapes Black widow spider (medium, large) Latrodectus hesperus [0] Grape benchgrafts Vine mealybug (egg) Planococcus ficus (egg, nymph, adult) [] Studies with unknown oxygen levels are not included. museum artifacts and other non-perishable stored products that are not negatively affected by ULO, the ULO treatment may not have a low limit for oxygen level as in anoxia and nitrogen fumigation. There are also other CA treatments where low or ultralow oxygen levels are used in combination with elevated carbon dioxide or different CA treatments including ULO treatment are used sequentially [, ]. In vacuum or hermitic storage treatments, the main factor for pest control is also the lack of oxygen []. Past research on CA treatments, including ULO treatments, was summarised by Ke and Kedar [5] and Mitcham et al. []. CA treatments for pest control were also reviewed by Fleurat-Lessard [], Carpenter and Potter [7], Mitcham [8] and Mitcham et al. []. The present review is limited to more recent studies on ULO treatments for pest control on perishable commodities. Recent progress in ULO treatment Research on ULO treatment for postharvest pest control in the last 0 years has been very limited. However, significant progress has been made and some ULO treatments have the potential to be used commercially. Unlike non-perishable objects or commodities that are usually not affected by ULO treatment for pest control [9, 0], fresh fruits and vegetables have limited tolerance to low oxygen []. ULO treatments for postharvest pest control often cause deteriorations in product quality and this is the primary reason for the lack of success of ULO treatments and their commercial use [, ]. Yet, different pests and commodities may have very different tolerances to ULO treatment. Effective and safe treatments are possible and have been achieved for the control of different pests on specific commodities. These provided bases as well as insights for further progress in developing ULO treatment as an alternative for postharvest pest control on perishable commodities in the future. Held et al. [] studied the responses of a variety of pests including fungus gnat larvae (Bradysia sp.), green peach aphid (Myzus persicae), sweetpotato whitefly (Bemisia sp.), twospotted spider mite (Tetranychus urticae), and western flower thrips (Franklinella occidentalis) to h exposure

3 Liu / Stewart Postharvest Review 00, :9 to >99% nitrogen and carbon dioxide at 0 C. The authors found that complete control of green peach aphid, twospotted spider mites, western flower thrips, and sweetpotato whiteflies was achieved in 8 h exposure to nitrogen and carbon dioxide. Mortality of fungus gnat larvae and twospotted spider mites varies and there is no complete control for either species. Tolerance of seedlings of different varieties of chrysanthemum and geranium to the nitrogen exposure was less than h. Begonia seedlings, however, are more tolerant and showed no damage from the 8-h exposure to nitrogen []. Liu [] reported on the responses of lettuce aphid (Nasonovia ribisnigri), potato aphid (Macrosiphum euphorbiae) and leafminer (Liriomyza langei) to different CA treatments including exposure to nitrogen under normal atmospheric pressure and vacuum. Complete control of lettuce aphid was achieved with nitrogen exposure under vacuum in days at 0 C. Potato aphid was exposed to -day treatments and complete mortality was achieved in nitrogen + % carbon dioxide, nitrogen under vacuum, and carbon dioxide under vacuum at 5 C. However, none of the treatments had complete control of leafminer larvae or pupae. All of the nitrogen treatments are safe to lettuce. In a later study, lettuce aphid was subjected to ULO treatments with % oxygen at, 5, and 0 C for to days. Complete control of lettuce aphid was achieved in a -day treatment at C, a - day treatment at 5 C, and a -day treatment at 0 C. The ULO treatments for control of lettuce aphid had no negative effects on lettuce quality []. These results suggest that the earlier study might not have achieved proper ULO levels in the nitrogen treatments where no complete control of lettuce aphid was achieved []. Western flower thrips are more tolerant than lettuce aphid to ULO treatment [5]. Both oxygen level and temperature have significant effects on thrips responses to ULO treatments with a much lower oxygen level of %. Mortality rate of thrips increases with decreased oxygen and increased temperature. Complete control of thrips was achieved in a -day treatment at 0 C and a -day treatment at 8 C [5]. ULO treatments for thrips control, however, caused injuries to lettuce heartleaves. The -day treatment at 0 C caused the least injury to lettuce heartleaves and injury became progressively more severe in - and -day treatments at decreased temperatures of 5 and C, respectively (Table ) [5]. Most injuries were in the form of a brown stain, similar to injuries caused by carbon dioxide []. Pre-treatment cold storage of lettuce for week prevented injuries to heartleaves by the -day ULO treatment. In comparison, lettuce without the pre-treatment storage sustained injuries to the heartleaves in a significant proportion of heads (Table ) [7]. The study indicated that ULO treatment can be made safer to lettuce through pre-treatment storage to increase lettuce tolerance. In a later study, a -day pretreatment cold storage was found to be adequate for preventing injury to heartleaves by the ULO treatment used for control of western flower thrips and the ULO treatment can be completed in 5 days after lettuce harvest [8]. The reduction of the time span increases the likelihood for the treatment to be used before lettuce is shipped to export markets. Complete control of western flower thrips was achieved in a 5-day ULO treatment with % oxygen on ice packed broccoli at C [9]. Oxygen level affected efficacy of ULO treatment. At a higher oxygen level of 0.0%, a -day treatment killed approximately 85% of thrips and a 0-day treatment killed all thrips (Table ) [9]. The production of offodour, mainly methanethiol, was a major concern for ULO treatment. Again, a brief and intense treatment is safer than a long and mild treatment. The 5-day ULO treatment for thrips control did not have a detectable off-odour. A 0-day ULO treatment with a higher oxygen level resulted in production of off-odour at the end of the treatment (Table ) [9]. Black widow spiders are often found hitchhike on harvested grape clusters from infested vineyards in California and require treatment for export to certain overseas markets. Western black widow spider, Latrodectus hesperus Chamberlin & Ivie, the dominant species of black widow spiders in California, were found to be highly susceptible to ULO treatment and -day ULO treatments with 0.5% oxygen or lower at C were sufficient for complete control of the spiders [0]. Oxygen level and temperature also affect responses of the spiders to ULO treatment. At C, as oxygen level decreased from % to 0.5%, spider mortality increased from 0 to 00%. At % oxygen, as temperature increased from to 5 C, spider mortality increased from 0% to 00%. The -day ULO treatment with 0.5% oxygen at C was tested on harvested table grapes from Thompson Seedless and Flame Seedless varieties and the treatment had no negative effects on grape quality (Table ) [0]. Because of the relatively short treatment time, effectiveness at low storage temperature, and the easily attainable oxygen level, the ULO treatment seems to have good potential to be implemented commercially for control of black widow spiders on harvested table grapes. Vine mealybug, Planococcus ficus Signoret, is a quarantined pest on grape nursery stocks in California as well as in export markets of USA table grapes. ULO treatments were developed successfully for control of vine mealybug on dormant grape benchgrafts []. ULO treatment with % oxygen at 5 C kills all life stages of vine mealybug in days. At 5 C, it takes days to achieve complete control of the insect. ULO treatments with much lower oxygen levels of < ppm and same temperatures and durations do not have any negative effects on bud-breaking or growth of the treated grape benchgrafts []. Results indicate that ULO treatments can be used to control vine mealybug on dormant grape benchgrafts. Conclusions and directions for future research Among the ULO treatments (Table ), the treatment for black widow spiders on table grapes [0] and the treatment for vine

4 Liu / Stewart Postharvest Review 00, :9 mealybug on grape benchgrafts [] have good potential for commercial use. The current fumigation treatment with carbon dioxide followed by sulphur dioxide for black widow spider requires warming of grapes to 5. C or higher and can result in reduced shelf life []. The ULO treatment is short ( day) and oxygen level of 0.5% is attainable in commercial CA rooms. The ULO treatments for vine mealybug control seems to have advantages over the hot water treatment currently used []. The current hot water dipping treatment requires removal of soil from roots and is labour intensive. The treatment may also cause injuries if the temperature is too high or time is too long. In both cases, ULO treatments seem to be better than the current treatments in both cost and safety. ULO treatments for control of western flower thrips on lettuce and broccoli (Table ), however, may prove difficult for commercial use. The 5 day time span to complete ULO treatment for broccoli and to complete pre-treatment storage and ULO treatment for lettuce means high treatment cost and delay for products to reach markets. In transit ULO treatment will unlikely be feasible in the near future because of technical challenges. In comparison, low temperature fumigation with pure phosphine controls western flower thrips in 8 h at the low storage temperature and therefore becomes a more attractive alternative []. Although lettuce aphid on lettuce can be controlled with ULO treatments relatively easily, no ULO treatment has been found for control of the leafminer, L. langei [, ]. Both lettuce aphid and the leafminer are major pests of lettuce and are quarantined in Japan. Low temperature phosphine fumigation, however, controls both insects even though lettuce aphid is much more tolerant to phosphine than to ULO treatments [, 5]. The success of ULO treatments depends on types of pests and commodities. Black widow spiders are more susceptible to ULO treatments than any other insects [,, 5, 0]. This is likely due to their unique respiratory system. Black widow spider uses a book lung for respiration and a complex protein, haemocyanin, to transport oxygen through an open blood circulating system to reach various organs and cells. Haemocyanin is far less efficient in transporting oxygen than haemoglobin which has a very high binding affinity for oxygen []. In contrast, insects, in general, have well developed tracheal systems for respiration [7]. However, haemoglobin is found mainly in higher insects and haemocyanin is found mainly in lower insects as respiratory proteins [8]. It is unknown whether this has any implications on insect tolerance to ULO. Insects live in very diverse habitats with various extents of hypoxia and there is also a wide range of variation among insect species and life stages in susceptibility to hypoxia [9]. Their varied adaptation to hypoxia means that they likely respond differently to ULO treatments. Eggs and adults in some lepidopteran species are more sensitive to hypoxia while the later larval stage and diapausing larvae are more tolerant. In addition, metabolically-active stages are more sensitive to hypoxia than inactive stages such as pupae [0]. There is also very limited research on mechanisms of CA treatment for insect control [, ]. Research is needed to gain better understanding of insect respiratory physiology and how CA affects insects. Knowledge in these areas will help to develop CA treatment for pest control in the future. Tolerance of perishable commodities is also critical for success of ULO treatment. Commodities that are not evaluated by their visual appearance such as rootstocks, seeds and bulbs seem more suitable for ULO treatments as demonstrated with grape rootstocks for control of vine mealybug []. Fresh fruits and vegetables, on the other hand, are evaluated by their visual quality as well as sensory attributes and the risk of injury by ULO treatment is high as demonstrated by many earlier studies [] and the recent studies on control of western flower thrips on lettuce and broccoli [5, 9]. However, the risk of injury to commodities can also be reduced by modifying the treatment and enhancing tolerance of commodities. In general, brief and intense treatments are safer than long and mild treatments to product quality. This is the case for ULO treatments on broccoli and lettuce for control of western flower thrips [5, 9]. In most CA studies, fruits and vegetables were subjected to CA treatments with little or no cold storage after harvest and potential effects of postharvest storage history were not considered. The case of increased tolerance of lettuce to ULO treatment by pre-treatment storage for control of western flower thrips demonstrated that product tolerance to ULO treatment can be enhanced significantly by pre-treatment storage [7, 8]. In general, after harvest fruits and vegetables in cold storage undergo drastic changes in their metabolism. This includes reduced metabolism rates indicated by lower oxygen consumption and carbon dioxide production as plants gradually use up the substrates presented at the time of harvest []. After their metabolism reaches a more stable low level, their demand for oxygen becomes low and exposure to ULO likely represents milder stress than that when plant tissue is physiologically more active and has a high oxygen demand. For lettuce, oxygen consumption decreases drastically after lettuce is harvested and stored at low temperature and reaches a stable low level in 5 days [, 5]. Hypoxic pre-treatment with % oxygen was also reported to increase tolerance of avocado to subsequent exposure to ULO of 0.5% []. Sequential CA treatments were also demonstrated to be effective against pests and safe to the product []. More research efforts should be directed in this area to explore ways of enhancing tolerance of fresh commodities to ULO or other CA treatments. It is likely that more ULO treatments can be developed by maximising product tolerance to ULO treatment through postharvest cold acclimatisation in combination with optimising treatment time and temperature. There are many challenges facing commercial use of ULO treatments for postharvest pest control on perishable commodities. There are very few ULO treatments that are ready

5 Liu / Stewart Postharvest Review 00, :9 to be commercialised. There is also a lack of suitable facilities for commercial ULO treatments. The relatively longer treatment time than most chemical fumigation treatments and the potential damage to postharvest quality also make ULO treatment less attractive. However, ULO treatment and other CA treatments have the potential to become safe, effective, and, in some cases, economical alternative treatments for postharvest pest control in specific situations as demonstrated with black widow spiders on table grapes and vine mealybug on grape benchgrafts [0, ]. ULO treatment is compatible with organically produced fresh products and therefore may become important for international trade of organic products in the future. The heightened public concerns over potential health risks of pesticide residue may also compel industry to adopt more environmental friendly methods such as ULO treatment for postharvest pest control. There is a great need for research on ULO and other types of environmental friendly techniques for postharvest pest control to address the lack of safe and effective control of postharvest pests on many exported commodities, heightened concerns on environmental and health hazard of chemical pesticides including fumigants, and challenges of pest management on organically produced fresh products. The research efforts in ULO treatment for postharvest pest control are very limited and, therefore, the potential of ULO treatment as well as other CA treatments is far from being fully explored for postharvest pest control. Future research on ULO treatment should focus on understanding effects of ULO treatment on insects and commodities, enhancing tolerance of fresh commodities to ULO treatments, and developing commercial ULO treatment protocols. Like most other postharvest treatments, ULO is not suitable for all pests and all fresh commodities. Emphasis should be given to susceptible pest groups and more tolerant commodities, and to pestcommodity complexes for which there is a lack of effective treatment. Close collaborations between researchers and industry are also critical for commercial use of ULO treatments. With continued research and development efforts, ULO treatment will become an important tool for postharvest pest management in the future. References Mitcham EJ, Zhou S and Kader AA. Potential of CA for postharvest insect control in fresh horticultural perishables: an update of summary tables compiled by Ke and Kader 99. Dept. of Pomology, Univ. of California, Davis, CA; 00. Mitcham EJ, Lee T, Martin A, Zhou S and Kader AA. Summary of CA for arthropod control on fresh horticultural perishables. Acta Horticulturae 00: 00: Zhou S and Mitcham EJ. Sequential controlled atmospheres treatments for quarantine control of Pacific spider mites (Acari: Tetranychidae). Journal of Economic Entomology 998: 9: 7. 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Effects of temperature, time, and oxygen level on insect mortality and lettuce quality. Postharvest Biology and Technology 008: 9: 9. Lipton WJ, Stewart JK and Whitaker TW. An illustrated guide to the identification of some market disorders of head lettuce. USDA, ARS, Marketing Research Report. 950, p. 7, pl. 9; Liu YB. Ultralow oxygen treatment for postharvest control of western flower thrips, Frankliniella occidentalis (Thysanoptera: Thripidae), on iceberg lettuce: II. Effects of pre-treatment storage on lettuce quality. Postharvest Biology and Technology 008: 9: Liu YB. Semi-commercial ultralow oxygen treatment for control of western flower thrips, Frankliniella occidentalis (Thysanoptera: Thripidae), on harvested iceberg lettuce. Postharvest Biology and Technology 00. (in review). 9 Liu YB. Ultralow oxygen treatment for postharvest control of western flower thrips, Frankliniella occidentalis, on broccoli. Journal of Economic Entomology 007: 00: Liu YB, Daane KM, Tebbets JS and Bettiga LJ. Ultralow oxygen treatment for control of Latrodectus hesperus (Araneae: Theridiidae) on harvested table grapes. Journal of Economic Entomology 008: 0: Liu YB, Bettiga LJ and Daane KM. Ultralow oxygen treatment for control of Planococcus ficus (Hemiptera: Pseudococcidae) on grape benchgrafts. Journal of Economic Entomology 00: 0: 7 7. Mitcham EJ, Simpson T, Biasi W, Ahmadi H, Bikoba V, Leesch J, Tebbets S and Tebbets J. Quality of Thompson Seedless table grapes fumigated with CO +SO and methyl bromide. Acta Horticulturae 005: 87: 09. Haviland DR, Bentley WJ and Daane KM. Hot-water treatments for control of Planococcus ficus (Homoptera: Pseudococcidae) on dormant grape cuttings. Journal of Economic Entomology 005: 98: Liu YB. Low temperature phosphine fumigation for postharvest control of western flower thrips (Thysanoptera: Thripidae) on lettuce, broccoli, asparagus, and strawberry. 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6 Liu / Stewart Postharvest Review 00, :9 5 Liu YB. Advances in postharvest pest control on perishable commodities using ultralow oxygen treatment and low temperature phosphine fumigation. Proc. 8 th Intl. Conf. CA and Fumigation in Stored Products, Sept., 008, Chengdu, China; 008. Gillespie RG and Spagna JC. Spiders. In: Encyclopedia of Insects, Resh VH and Carde RT (eds). Academic Press, New York, NY; pp : Harrison JF. Respiration system. In: Encyclopedia of Insects, Resh VH and Carde RT (eds). Academic Press, New York, NY; pp : Burmester T and Hankeln T. The respiratory proteins of insects. Journal of Insect Physiology 007: 5: Harrison JF, Frazier MR, Henry JR, Kaiser A, Klok CJ and Rasc on B. Responses of terrestrial insects to hypoxia or hyperoxia. Respiratory Physiology and Neurobiology 00: 5: 7. 0 Hoback WW and Stanley DW. Insects in hypoxia. Journal of Insect Physiology 00: 7: 5 5. Chervin C, Brady CJ, Patterson BD and Faragher JD. Could studies on cell responses to low oxygen levels provide improved options for fruit storage and disinfestations? Postharvest Biology and Technology 99: 7, Carpenter A, Downes C, Hansen L, Shelton M and Lill R. Metabolic heat: a new way of looking at how controlled atmospheres kill insects. In: Proc. Intl. Conf. Controlled Atmosphere and Fumigation in Stored Products, Fresno, CA Oct 9 v, 000, Donahaye EJ, Navarro S and Leesch JG (eds). Executive Printing Services, Clovis, CA, USA, pp, 00. Kader AA and Saltveit ME. Respiration and gas exchange. In: Postharvest Physiology and Pathology of Vegetables, nd edition, Bartz JA and Brecht JK (eds). Marcel Dekker, Inc., New York, NY. pp Martínez JA and Artés F. Effect of packaging treatments and vacuumcooling on quality of winter harvested iceberg lettuce. Food Research International 999: : 7. 5 Smyth AB, Song J and Cameron AC. Modified atmosphere packaged cut iceberg lettuce: effect of temperature and O partial pressure on respiration and quality. Journal of Agricultural Food Chemistry 998: : El-Mir M, Gerasopoulos D, Metzidakis I and Kanellis AK. Hypoxic acclimation prevents avocado mesocarp caused by subsequent exposure to extreme low oxygen atmosphere. Postharvest Biology and Technology 00: : Published by Stewart Postharvest Solutions (UK) Ltd. All rights reserved.