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Silverleaf whitefly

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Silverleaf whitefly
Scientific classification
Kingdom:
Animalia
Phylum:
Arthropoda
Class:
Insecta
Order:
Hemiptera
Suborder:
Sternorrhyncha
Family:
Aleyrodidae
Genus:
Bemisia
Species:
B. tabaci
Binomial name
Bemisia tabaci
(Gennadius, 1889)
Synonyms

Bemisia argentifolii Bellows & Perring[1]

The silverleaf whitefly (Bemisia tabaci, which is also informally referred to as the sweetpotato whitefly) is one of several whiteflies that are currently important agricultural pests.[1] The silverleaf whitefly is classified in the family Aleyrodidae, and is included in the large sub-order of insects, Sternorrhyncha.[2]

The silverleaf whitefly thrives worldwide in tropical, subtropical, and less predominately in temperate habitats. Cold temperatures kill both the adults and the larvae of the species.[3] The silverleaf whitefly can be confused with other insects such as the common fruitfly, but with close inspection, the whitefly is slightly smaller and has a distinct wing color that helps to differentiate it from other insects.

While the silverleaf whitefly had been known in the United States since 1896, in the 1980s a virulent strain appeared in poinsettia crops in Florida during the mid-1980s. For convenience that strain was referred to as strain B (biotype B), to distinguish it from the milder infestation of the earlier known strain A. Less than a year after its identification, strain B was found to have moved to tomatoes, and other fruit and vegetable crops. Within five years, the silverleaf whitefly had caused over $100 million in damage to Texas and California agriculture industries.[1]

Anatomy and life cycle

Bemisia tabaci molting on leaves. The silver empty structures depicted on the leaves are cast-off skins.

During the adult stages of the silverleaf whitefly, the body expands up to 0.8mm in length and has a snow-white color, which is attributed by the secretion of wax across its wings and body.[4] During feeding or resting stages the whitefly adult covers its body over with its wings. When depositing eggs, the females will lay 50 to 400 eggs ranging from 0.10mm-0.25mm on the under part of leaves. Female whiteflies are diploid and emerge from fertilized eggs whereas male whiteflies are haploid and emerge from unfertilized eggs. Eggs are laid in groups, being small in size with dimensions of 0.2 mm wide and .1mm in height. Eggs are initially whitish in color and change to a brown color towards the time of hatching within 5 to 7 days. After the egg stage, the whitefly hatchling develops through four instar stages.

Bemisia tabaci nymph instars on green leaf

In the first instar, commonly called the crawler, the nymph is 0.3mm in size and grows to be 0.6 mm till the fourth instar stage. During the first instar stage the body is greenish in color and flat in body structure.[4] The mobile whitefly nymph walks to find a suitable area on the leaf with adequate nutrients and molts into four other instar or nymphal stages over the span of 40–50 days until it reaches adulthood.[2] During molting, the flies shed silver skins, which are left on the leaves. During the instar phases, the whitefly maintains an opaque white appearance and does not move from the feeding site the crawler originally chooses. At the feeding site the nymphs use parts of their mouth to stab into the plant and consume the plant’s juices.[4] The stage following the nymph stages is the pupal stage when the eyes become a deep red color, the body color becomes yellow, and the body structure thickens. After development is completed, adult whiteflies are approximately four times the size of the egg, with light yellow bodies and white wings.[2]

Native/original community

Poinsettia is one of the silverleaf whitefly's preferred hosts.

Research indicates that the silverleaf whitefly likely came from India. Since the whitefly is predominately associated with areas exhibiting tropical/subtropical climates, the focus shifts to how these insects attained access to crops in habitats with temperate climates.[2] One hypothesis suggests that the transfer of decorative plants from tropical regions may have aided in the spread of the silverleaf whiteflies to temperate environments. The ability of the whitefly to adapt to various plants facilitates the spread of dangerous plant viruses, which these insects are notorious for transmitting.[5] Plants which are affected by the whitefly include: tomatoes, squash, poinsettia, cucumber, eggplants, okra, beans, and cotton.[4] Other common plant damages of whitefly include: removing plant sap, breakdown of the leaves of the plant, and leaf shedding.[4]

Ecological impact

The silverleaf whitefly is considered an invasive species in all areas it inhabits in the United States as well as Australia and several European countries. It was classified as an agricultural pest in Greece around 1889 and had a significant impact on tobacco crops there. The first whitefly found in the United States dates back to 1897, and was found on a crop of sweet potatoes.

This tiny insect wreaks havoc in two simple ways. First, the silverleaf whitefly, a parasite, feeds off of its host plants by piercing the phloem or lower leaf surfaces with its mouth and removing nutrients. Affected areas of the plant may develop chlorotic spots, whither, or lose leaves. Whiteflies also produce a sticky substance called honeydew, which is left behind on the host.[2] Honeydew can induce the growth of sooty molds, which can then reduce the plants ability to absorb light. This results in less growth, lower yield, and poor quality plants. It also requires that crops be thoroughly washed after harvesting, which raises processing costs for the grower.

The second problem with the silverleaf whitefly is its notorious status as a vector for plant disease. It has been transmitting gemniviruses such as lettuce infectious yellows virus, tomato yellow leaf curl virus, and African cassava mosaic virus for years and over many continents[2] and is now a vector for cassava brown streak virus disease.[6]

Bemisia tabacia became a serious issue in crops across the southwestern United States and Mexico in the 1980s. Scientists speculate that this pest was introduced via infested ornamental plants brought into the United States at this time. Florida’s poinsettia greenhouses were crippled by the pest beginning in 1986, and by 1991, the whitefly infestation had spread through Georgia, Louisiana, Texas, New Mexico, and Arizona to plague crop growers in California. California, the state that produces approximately 90% of the United States’ winter vegetable crop, has incurred an estimated $500 million in crop damage due to silverleaf whitefly populations.[7] Across the plant industry, this is thought to cost the state $774 million in private sector plant sales, 12,540 jobs, and $112.5 million in personal income. On a national scale, the United States has suffered crop and ornamental plant damages in excess of $1 billion.[7]

In particular, the whitefly is a devastating pest simply because it feeds on over 500 hosts. Included in its host domain are agricultural crops such as tomatoes, squash, broccoli, cauliflower, cabbage, melons, cotton, carrots, sweet potato, cucumber, and pumpkin, and ornamental plants such as poinsettia, crepe myrtle, garden roses, lantana, and lilies. It can cause specific damage to certain host plants, like "silverleaf" on squash, irregular ripening of tomatoes, whitestalk in broccoli and cauliflower, white stem in poinsettia, and light root in carrots.[7]

The whitefly has many natural predators including parasitoids and various arthropods. More on this subject can be found below in the section titled natural enemies.

Integrated pest management

The silverleaf whitefly is a very costly and common pest to the agricultural world. It destroys crops and causes the transfer of a variety of viruses that affect agricultural plants in harmful ways such as the earlier ripening of tomatoes through the tomato yellow leaf curl virus. As silverleaf whiteflies continue to destroy crops, scientists are trying to find ways to combat these agricultural pests. Some major controls for this pest have come from the development of oils from agricultural wastes, usage of natural enemies such as the four species of Eretmocerus (Eretmocerus sp, Eretmocerus mundus, Eretmocerus hayati, and Eretmocerus emiratus),[8] employment of trap crops, release of insect growth regulators, and implementation of the Light-Emitting Diode Equipped CC trap (LED-CC).

Most of the control tools that have been created affect the plant and soil properties at a minimal level. Scientists are currently focusing on targeting the whitefly through mechanisms that do not cause pollution or contamination (i.e., mechanisms other than insecticides). It is important to be able to reduce the number of B. tabaci individuals that settle on plants to decrease plant damages such as those caused by viral transmissions. This pest can be hindered by reducing settling, decreasing oviposition, and abating its population development.[9]

Biological controls

Classical biological control tends to be the only long-term sustainable solution to controlling exotic pests.[8] One of the main key issues of this type of control is its lack of predictability of success and establishment of the controlling agents.[8] The solution to this problem is finding a way to transition biological control as an empirical method to a more reliable, predictive science.

Entomologists with the U.S. Arid-Land Agricultural Research Center identified the most common causes of death of the whitefly which included predatory insects, parasites, and weather induced dislodgement.[10] They emphasize the importance of exploiting the use of natural predators and have identified predators by the use of enzyme-linked immune sorbent assay (ELISA). Through experimentation it was found that the use of the biological controls and insect growth regulators produces a higher predator-to-prey ratio.[11] Therefore, insect growth regulators, such as buprofezin and pyriproxyfen, conserve natural predators, as opposed to conventional insecticides, which can indiscriminately kill both predator and prey populations.[11]

Natural enemies

Natural enemies are highly effective as biological controls. Species of parasitoids, predators, and pathogens specific to the whitefly keep populations under control. The four Old World species of Eretmocerus (Eretmocerus mundus, Eretmocerus hayati and Eretmocerus emiratus) established in the Western United States are a group of genetic individuals of related taxa that are parasitoids of B. tabaci and serve as biological control agents. Scientists are considering the idea of releasing these parasites in order to be able to control their host’s population growth and save the destruction of important crops.[8] However, not all Eretmocerus can be successfully transplanted into areas where the whiteflies are present due to differences in climate preference.[8] For example, the species Eretmocerus melanoscutus failed to establish in the western United States due to climate issues. Goolsby (2005) mentions that different species of Eretmocerus are matched with the climate they are able to survive in. The success of the species of Eretmocerus in the USA can be contributed to the smaller host range, better climatic adaptation, and higher attack rate. Other natural predators of the B. tabaci include several species of wasps, bigeyed bugs, lacewing larvae, and lady beetle larvae, which all prey on the nymphs of the whitefly.

There are eight different arthropod orders that attack B. tabaci. These include members of the families Phytoseiidae, Coccinellidae, Syrphidae, Anthocoridae, Nabidae, and Miridae, Chrysopidae and Coniopterygidae.[12] There are currently four species that are commercially available; they include Delphastus pusillus, Macrolophus caliginosus, Chrysoperla carnea, and C. rufilabris.[12] D. pusillus are a small, shiny, black beetle species that suck out the contents of the silverleaf whitefly by piercing its shell. Adult and larval stages of this beetle feed at all life stages of the pest.[12] C. rufilabris is only able to feed on the immature stages or the larval stages of B. tabaci.[12]

Another natural mechanism of controlling the population of B. tabaci is the use of fungal pathogens. The most commonly known pathogens to the whitefly pest are Paecilomyces fumosoroseus, Aschersonia aleyrodis, Verticillium lecanii, and Beauveria bassiana.[12] When spore solutions of V. lecanii are sprayed on eggs, first, second, and third instar nymphs of B. tabaci approximately 89% to 90% of these eggs are killed.[12] Strains of whitefly have developed resistance to its fungal pathogens. For example, whitefly pests have grown resistant to infection by V. lecanii.

A technician is applying Beauveria bassiana, a fungus that is a natural enemy to silverleaf whiteflies to a plot of vegetables near Weslaco, Texas.

B. bassiana is only an effective biological control agent at a maximum temperature of 20°C and a humidity level greater than 96%.[12] Not enough studies have been conducted to show the productiveness of fungal pathogen in the real world environment. Much of the success of this biological control on B. tabaci has been conducted in the laboratory.[12] However, it can be concluded though that when the fungal pathogen is combined with an insecticide, the synergistic effect of the two will induce a higher mortality rate of the whitefly. P. fumosoroseus has a broad host range but can attack silverleaf whiteflies at a variety of life stages and these include eggs, nymphs, pupae, and adults stages.[12] On the other hand, A. aleyrodis only infects and destroys nymphs and pupae.[12]

Another natural enemy of the whitefly are parasitoids, which kill their host once their development has been completed. Whitefly parasitoids are affiliated with three hymenopterous families. These families are Platygasteridae, Aphelinidae, and the Eulophidae.[12] The best studied of these whitefly parasitoids are Encarsia formosa and Eretmocerus eremicus, both of which are commercially available. The Encarsia formosa "Beltsville Strain", however, has been unable to control Bemisia tabaci biotype B in commercial greenhouses; it is only able to control the species in small experimental greenhouses. In an experiment done by the Hoddle laboratory, the release of three or more E. formosa on B. tabaci per week failed to control the pure population of the species on poinsettia plants because wasps that are reared in the B. tabaci are less fecund, have a slower development, and fail to allow immature parasitoids to survive and develop.[12] The species Encarsia formosa works much better at controlling the whitefly species Trialeurodes vaporariorum than it does Bemisia tabaci. On the other hand, Eretmocerus sp is much better at controlling silverleaf whitefly than is the Encarsia formosa "Beltsville Strain." In an experiment done again by the Hoddle laboratory, the release of three female wasps of an Eretmocerus species were able to effectively eliminate patches of the fly nymphs right after their discovery. The wasps are faster at searching for patches of nymphs of their host species and are consistent at controlling the population.[12] Eretmocerus are bi-parental ecto-endoparasites, meaning that parents lay their eggs on the outside of the fly. As the wasp larvae grow they penetrate the fly and continue their growth and development inside the host.[12] Plant growers today have been successfully able to control the population of Bemisia tabaci by using a variable release strategy. In the variable release strategy employed, six female parasitoids were released per week for the first half of the growing season, while only one female was released per week for the remaining of the season. The effectiveness of the parasitoid wasps was improved by releasing varying amounts of them per week so that they are continuously available. the number released deceases as the number of hosts decreases due to the wasps effectiveness.[12] If natural enemies are not able to control the pest population at low levels due to a significant increase in pest, an insecticide compatible with the biological control agent could be used to assist in reducing the pest population to low levels again.[12]

Chemical controls

Natural oils

The sugar apple seed oil is an effective chemical control against the whitefly.

One of the important tools for controlling the silverleaf whitefly population is through the usage of natural oils. Currently, the most effective oil in the market is the ultra-fine oil, which is a paraffinic oil product that reduces the settlement of the adult flies, decreases oviposition, and abates the transmission of the tomato yellow leaf curl virus.[9] Ultra-fine oil’s effect can be strengthened through the combination with oils such as limonene or citronellal. On the other hand, olive oil is highly effective in controlling the number of flies that infect the leaves of their host plants and virus transfer. Other oils such as cottonseed, castor, peanut, soybean, and sunflower can also be used to reduce the settling and oviposition of B. tabaci adults. Out of this group of oil, peanut was the most effective in reducing the population. All of these oils cause direct mortality to all immature life stages of the silverleaf whitefly once the life stages come into contact with the oils that have been sprayed on the leaves. The oil extracted from the seeds of sugar apple is as effective against the whitefly as the use of insecticides.[13] The seed oil causes the silverleaf whitefly nymph to shrink in size and therefore detach from the tomato plant leading to starvation, as nymphs require close contact to the leaf to properly feed. In addition, the fourth nymphal stage is the most vulnerable to predation. Spraying a strong concentration on possible areas of nymph habitation can make oil a high-quality treatment.[13] Sugar apple seed oil is not phytotoxic to tomato plants of any concentrations and reduces the survival rate of the pest.[13] Spraying oil on leaves that have been infested or can be potentially infested will help reduce the number of silverleaf whiteflies that will reach the adult stage. The reduction of settling through various mechanisms can also help limit the amount of plants that become infected with viruses transmitted by these pests.

Insect growth regulators

Insecticides are known to be costly, and there is also an increasing resistance of the whitefly to insecticides. In a study of the silverleaf whitefly, a pest of other curcurbits family plants including zucchini squash, cucumber, and pumpkin was examined.[14] In particular squash is infected with Squash silverleaf, which is a serious physiological disorder that involves silvering of the surface of leaves, reduction in chlorophyll concentrations and higher reflectance. To combat this disease, insect growth regulator (IGR), pyriproxyfen has been used. This hormone is a juvenile hormone analogue, which affects hormonal balance and chitin in premature insects, which causes deformation and death during molting and pupation stages. Therefore making pyriproxyfen effective in reducing the whitefly populations. It reduces the fruit damages, and increases the size, weight, and quality of fruit. Effectively, IGR does not kill adult whiteflies, but instead sterilizes the eggs of those adults that are treated. It is also a potent inhibitor of embryogenesis, adult formation and metamorphosis. It kills larva and keeps adults from completing the last nymphal stage. The IGR has low toxicity to mammals, fish, birds and bumblebees.

Mechanical controls

Man-made traps and covers

In addition, the Light-Emitting Diode Equipped CC trap (LED-CC) was developed by plant physiologist Chang-Chi Chu and Thomas Henneberry.[15] Originally, the trap was used to monitor population of silverleaf whitefly populations, but as the trap improved in its effectiveness it was used in control programs to limit whitefly pest populations. The trap itself includes a green LED light that attracts and traps the whiteflies. The LED device works best at night,and is inexpensive and durable. In addition, the LED is parasite friendly and therefore does not harm predators of the whitefly. The trap also does not utilize pesticides.[15]

Another technique used to reduce virus damage include the use of FRC known as floating row covers, which are covers used to keep plants from exposure from pests. Field studies have been conducted in Australia and have shown that the use of FRCs and IGR increase the yield of harvested fruit and quality. The row covers have been known to reduce virus damage to cucurbits.

Trap crops

Squash crops are effectively used as trap crops for attracting silverleaf whitefly.

Another important control is the use of other crops as a source of trap crops. Squashes can act as trap crops for the silverleaf whitefly due to the flies’ attractiveness to these crops.[16] Silverleaf whiteflies are actually more attracted to the squash crop than they are to the tomato plant.[16] When squash serves as a trap crop, the tomato yellow curl leaf virus can be controlled and limited. Scientific experiments show in the fields that growing squash crops around the areas where tomato plants can be found is a useful manipulation in regulating the silverleaf whitefly population as well as the transmission of TYLCV. Other plants that can serve as trap crops include cantaloupe and cucumber.[16]

Cultural controls

Through a cultural control method, different planting areas can limit the amount of B. tabaci infected plants. Planting different host crops away from each other will decrease the number of plants the flies will be able to infect. Thus, the best control is to maximize the distance and time interval between host crops.[17] Good sanitation in winter and spring crops is also required for the maintenance and control of the fly population.[17] Weeds and host crop residues must be removed immediately to avoid infestation. Silver/aluminum cover mulches can repel the adult silverleaf whitefly. Thus, when planting seeds, placing a reflective polyethylene mulch on planting beds will significantly reduce the rate of colonization.[17]

Cultural controls are very important to crops such as vegetables and fruit. For example, in the family of Cucurbitaceae family, vegetables such as watermelon and squash contract squash vein yellowing virus (SqVYV) by the silverleaf whitefly.[18] The SqVYV virus[18] discovered by plant pathologist Benny Bruton and Shaker Kousik is essentially a crippling disease of the watermelon, which leads to the vine of the watermelon to collapse, causing the death of the watermelon before harvest. Kousik and pathologist Scott Adkins at ARS Subtropical Plant Pathology Research Unit worked together in screening the watermelon germplasm for resistance to SqVYV as to search for potential sources of resistance in wild-type watermelon. Kousik examined different combinations of insecticides and silver plastic mulch that could be used to reduce the whitefly populations.[18]

Summary

Under the integrated pest management plan, there are several different ways to control and manage the pest population of B. tabaci. The mechanical control used to control the species population is through the use of natural oils such as sugar apple[13] and the more common type of insecticides. From experimentation, scientists have seen that the sugar apple oil[13] (and other natural oils) has the same strength as insecticides but with the benefit of not causing pollution.[9] Through cultural control methods, the flies are regulated through the process of trap crops and man-made traps, such as the Light-emitting diode. The most important and pollution free method of controlling the amount of damage down by the silverleaf whitefly annually is the usage of natural enemies (i.e. pathogens, parasites, and predators). There are a variety of predators and several different pathogens and parasites that can effectively keep the pest population under a minimal level. The most common parasitoid of the silverleaf is Eretmocerus, a wasp species that finishes its development inside the host, killing the host once it reaches adulthood.[12] Most of the predators of B. tabaci tend to just eat out the insides of the pest, while pathogens transfer deadly viruses.[12]

References

  1. ^ a b c Fan, Yuqing Fan and Petitt, Frederick (1998). "Dispersal of the broad mite, Polyphagotarsonemus latus (Acari: Tarsonemidae) on Bemisia tabaci (Homoptera: Aleyrodidae)". Experimental and Applied Acarology. 22 (7): 411–415. {{cite journal}}: |access-date= requires |url= (help); Check date values in: |accessdate= (help); Text "doi-10.1023/A:1006045911286" ignored (help)CS1 maint: multiple names: authors list (link)
  2. ^ a b c d e f Brown, J. K.; Frohlich, D. R. and Rosell, R. C. (1995). "The Sweetpotato or SilverLeaf whiteflies: Biotypes of Bemisia tabaci or a species complex?". Annual Review of Entomology. 40: 511–534. {{cite journal}}: Unknown parameter |isssue= ignored (help)CS1 maint: multiple names: authors list (link)
  3. ^ Greenberg, S., Legaspi, B., Jones, W. et al. (2000) Temperature Dependent Life History of Eretmocerus eremicus (Hymenoptera: Aphelinidae) on Two Whitefly Hosts (Homoptera: Aleyrodidae). Environmental Entomology. 29: 851-860.
  4. ^ a b c d e Johnson, F. A.; Short, D. E. and Castner, J. L. (2005). Sweetpotato/Silverleaf Whitefly Life Stages and Damage (PDF). Entomology and Nematology Department special publication 90 (revised ed.). Gainesville, Florida: Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida.{{cite book}}: CS1 maint: multiple names: authors list (link)
  5. ^ Azab AK, Megahed MM, EI-Mirsawi, HD. 1971. On the biology of Bemisia tabaci (Genn.). Bull. Soc. Entomol. Egypt 55: 305-15.
  6. ^ Pheneas Ntawuruhunga and James Legg (May 2007). "New Spread of Cassava Brown Streak Virus Disease and its Implications for the Movement of Cassava Germplasm in the East and Central African Region" (PDF).
  7. ^ a b c Service, A. R. National Invasive Species Information Center: Silverleaf Whitefly. United States Department of Agriculture.
  8. ^ a b c d e Goolsby, John A., DeBarro, Paul J., Kirk, Alan A., Sutherst, Robert W., Canas, Luis, Ciomperlik, Matthew A., . . . Vacek, Don C. (2005). Post-release evaluation of biological control of Bemisia tabaci biotype "B" in the USA and the development of predictive tools to guide introductions for other countries. Biological Control, 32(1), 70-77. Retrieved from, http://www.sciencedirect.com/science/article/B6WBP-4DBJHR0-1/2/c1cfefe6cbc3ce3317e6e20dba2d004e doi:10.1016/j.
  9. ^ a b c Schuster, D. J., Thompson, S., Ortega, L. D., & Polston, J. E. (2009). Laboratory Evaluation of Products to Reduce Settling of Sweetpotato Whitefly Adults. Journal of Economic Entomology, 102(4), 1482-1489. Retrieved from http://dx.doi.org/10.1603/029.102.0412 doi:10.1603/029.102.0412.
  10. ^ United States Department of Agriculture: Beyond Insecticides: Improved Methods of Whitefly Control. Retrieved March 15, 2011, from http://www.ars.usda.gov/is/AR/archive/apr06/whitefly0406.htm.
  11. ^ a b McGinnis, L. Alternate Methods of Whitefly Control (2006 April 5) Retrieved March 15, 2011, from http://www.ars.usda.gov/is/pr/2006/060405.htm.
  12. ^ a b c d e f g h i j k l m n o p q r Hoddle, Mark S. (1999). The Biology and Management of the Silverleaf Whitefly, Bemisia argentifolii Bellows and Perring (Homoptera: Aleyrodidae) on Greenhouse Grown Ornamentals Retrieved April 18, 2011, from http://www.biocontrol.ucr.edu/bemisia.html.
  13. ^ a b c d e Chien-Yih. Control of Silverleaf Whitefly, Cotton Aphid and Kanazawa Spider Mite with Oil And Extracts from Seeds of Sugar Apple, from http://apps.isiknowledge.com www.library.gatech.edu:2048/full_record.do?product=WOS&search_mode=Refine&qid=3&SID=4BkCOJBjK2IPk5CGoaM&page=2&doc=18.
  14. ^ Qureshi, M. , Midmore, D. , Syeda, S. , & Playford, C. (2007). Floating Row Covers and Pyriproxyfen Help Control Silverleaf Whitefly Bemisia Tabaci (Gennadius) Biotype B (Homoptera: Aleyrodidae) in Zucchini. Australian Journal of Entomology, 46(Part 4), 313-319.
  15. ^ a b Elstein, David. New Trap To Control Silverleaf Whiteflies. (2002 May 30). Retrieved March 13, 2011, from http://www.ars.usda.gov/is/pr/2002/020530.htm.
  16. ^ a b c Schuster, D. 2004. Squash as a trap crop to protect tomato from whitefly-vectored tomato yellow leaf curl. Pages 281-284. International Journal of Pest Management. Taylor & Francis Ltd.
  17. ^ a b c UC IPM Pest Management Guidelines: Peppers. (2009, December 2009). Retrieved March 17, 2011, from http://www.ipm.ucdavis.edu/PMG/r604300811.html.
  18. ^ a b c Flores, A. (2007). On the Guard Against Watermelon Vine Decline. Pages 10-11 Agricultural Research.
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