Summary of some alternative treatments from plants and with irradiation on mortality of citrus blackfly stages.
Abstract
Citrus BlackFly (CBF) always represented a threat to Brazil. The impact of the introduction in Brazil of the CBF has led to serious economic and environmental consequences. In this chapter, we will show relevant information on biological aspects, history of occurrence, and impact of CBF on Citrus in Brazil; data about dynamics populations and spatial distribution patterns and dependence will be presented. We are intending to emphasize in this chapter the main challenges and opportunities of some important tactics to promote sustainable management of CBF in citrus, such as: (i) biological control, (ii) chemical and others methods, and (iii) induced resistance.
Keywords
- citrus blackfly
- sampling
- biological control
- insecticides
- induced resistance
- integrated management
1. Introduction
In the southern hemisphere, Brazil dominates a great part of the orange production [1]. Besides the production of fruit, the main destination is orange juice industry, Brazil being one of the largest producer and exporter of that drink in the world [2]. Nevertheless, there are several problems associated with some stages of the production chain, but in plant production the main obstruction is the occurrence of Citrus BlackFly (CBF)
In Brazil, CBF is considered as one of major pest introduced in
CBF was first detected in the Nagpur region of Maharashtra (India) in 1910 by Woglumi. In 1915, it was reported in the rest of Asia by Ashby. [7]. In 1913, it was discovered in the New World and in West Indies in 1913 from where it spread out to other islands and Central and South America [8]. On the American continent, it was first discovered in Jamaica in 1913. Between the years 1934 and 1935, it was detected in Cuba, Florida, and Mexico. In Brazil, this insect was first detected in the state of Pará, in 2001 [9]. In 2007, CBF was officially included in the quarantine pest list of Brazil. But due to the extensive spread, this insect was excluded from pest quarantine list Brazil, after losing its quarantine character (Normative Instruction (NI) no. 42, the Ministry of Agriculture, Livestock and Supply (MAPA)). Register of CBF occurrence already was realized in these following Brazilian states: Amazonas, Bahia, Ceará, Espírito Santo, Goiás, Mato Grosso do Sul, Maranhão, Pará, Paraíba, Paraná, Pernambuco, Piauí, Rio de Janeiro, Rio Grande do Norte, Rondônia, Roraima, São Paulo, Sergipe, and e Tocantins [10].
The Plant Transportation Permission–PTV is an official document issued to monitor the transit of starting plants, parts of plants, or plant products produced in accordance with the standards of plant health protection in order to prevent the spread of pests regulated, as stated in the Normative Instruction 54, of December 4, 2007, of the Brazilian Ministry of Agriculture, Livestock and Food Supply (MAPA). In Brazil, CBF restricted transport of more than 31 vegetable species considered hosts to the pest, which required the issuance of PTV for the transit of these products when transported from a state where the pest is present to another state that did not had its occurrence. Since it is wide spread, on February 20, 2015, the NI no. 2 of MAPA established that currently there is no restriction on the interstate transit of plants and their parts. Transportation of fruit seedling and infested leaves is the main way for the spread of this pest to long distances [11]. The fast spread must have been facilitated by river and road transport, especially on
Since there are a large number of arthropod pests infecting
2. Dynamics populations and dispersal pattern
The knowledge about major infestation potential of CBF and its seasonal dynamics is essential for the orientation of management strategies, which may result in the minimization of production losses [12]. Because with use of CBF sampling, it is possible to prevent outbreaks of the pest and to decide only when necessary. In others words, the tactics of control such as use of chemicals or similar or release of natural enemies will be realized only on the recommended thresholds. The variation in climatic variables, especially temperature and rainy season, is important on infestation potential of CBF [13]. In general, the highest population levels of CBF occur in the low-precipitation season [14, 15]. But in Municipality of São José de Ribamar, State of Maranhão (Brazil), in a commercial orchard of
In a bioclimatic simulation in the North region of Brazil, the optimum bioclimatic zone was established between October, November, and December. In general, summer is favorable for the occurrence of CBF in the South Hemisphere; that is, winter is unfavorable [12]. In Minas Gerais and north of São Paulo, the optimum time is in December and unfavorable months are July, August, and September, a similar pattern may favor the spontaneous migration of the insect between these sites [12]. In Municipality of Artur Nogueira, State of São Paulo (Brazil), with one year of evaluation the peak occurrence of egg was observed in the spring (August) and for nymphs in the autumn (from March to May) in a commercial orchard of
Females of CBF prefer oviposition sites of the canopy with high humidity [11]. But the distribution pattern intratree shows difference between geographical regions and between years and seasons. In an experiment conducted in São Paulo State, the trees were divided in four quadrants (north, south, east, and west), the western quadrant showed more CBF egg masses than the northern, but no difference was observed in the southern and eastern quadrants. Western and eastern quadrants showed highest quantities of CBF nymphs [11]. However, in another experiment in State of Maranhão, Brazil, it was observed that during rain period the insects (eggs and nymphs) were distributed homogeneously on the trees canopies in a commercial orchard. In addition during the period without rain, the north and south quadrants showed less clutches/plant, eggs/plant and nymphs/plant in a non-commercial orchard and clutches/plant, eggs/plant in a commercial orchard [15]. The infestation level may vary in accordance with the crop system, because there is evidence that infestation of CBF is different in agroforestry and conventional system [13].
Upon adjusting the calculated variograms to the spherical model in the dry and rainy seasons [16], it was concluded that the spatial distribution of CBF in the orchard is aggregated, but the level of average aggregation depends on the weather especially during the season, during the rainy season the average aggregation is 162,092 m2, and 9615 m2 in the dry season. They recommend to obtain a reliable estimate of citrus blackfly populations, at least one trap should be used for each 17 hectares during the rainy season and one trap per hectare in the dry season. Silva et al. [17] used a similar approach of spatial dependence described by the spherical model; that model has a simple polynomial expression and its shape had an almost linear growth up to a certain distance and then stabilized. Silva et al. [17] confirmed that spatial distribution of CBF in citrus orchard in the agroforestry field in Pará State was predominantly aggregate, forming clusters from 15.5 to 34 m. This aggregation behavior of CBF increased the initial damage in newly infested orchards [11].
In a general way, some studies have showed evidence of an aggregation behavior of CBF on a spatial scale. In terms of sampling methods to implement this component of CBF IPM, it is interesting to know how the population dynamics is in intratree distribution and in spatial scale of different landscape structures, because some differences of results found about the occurrence of CBF should be considered according to the kind of pest management and the degree of landscape heterogeneity. We would like to encourage future studies about dynamics populations of CBF in a period longer than 2 years of evaluations that may consider spatial mathematical modeling and/or use of statistical models as generalized linear mixed models with overdispersion for helping to understand this cluster behavior and temporal and spatial dispersal patterns according to the landscape structure of
3. Biological control
The use of beneficial organisms as a component of integrated pest management (IPM) is relevant for most crops [18, 19]. The search about natural enemies associated with CBF has enabled the use of biological control worldwide. One of the most effective parasitoids of the CBF is
The parasitoids
The solitary endoparasitoid
The natural enemies of Chrysopidae family, known as lacewings, are predators that play a significant role for controlling the population of the blackfly on various crops of agricultural importance such as cotton
In the last few years, a strong effort has been made to improve techniques for rearing of natural enemies of CBF in laboratory by some Brazilian University Laboratories. The main challenge to release natural enemies on a large scale to biologically control CBF in Brazil is the absence of commercial availability of these natural enemies yet. But a promising perspective of applied biological control will probably happen with government partnerships like Bahia State, Brazil for mass production of CBF’s natural enemies [37].
4. Chemical insecticides and other methods
Chemical insecticides have been used to control its infestation; however, this strategy reduces the insect pest of infestations only temporarily triggering the imbalance in the environment that in turn, poses threat to nontarget organisms [19, 36]. Evaluations about the effect of Dursban 4E [chlorpyrifos] in two different nursery locations by Ref. [37] showed that they observe only limited control, and this product was not phytotoxic to nursery citrus. Monocrotophos (0.05%) was effective to promote nymphal mortality (range from 75.10 to 85.50%) of CBF [38]. They believe that application of monocrotophos (0.05%) during early nymphal stages followed by neem oil (1%) during later stages may be effective and also safe to parasitioids.
In Brazil, four insecticides are registered to control this pest in
In the Texas (USA), it is common that organic growers apply pesticides such as sulphur, oils, and microbials to CBF control [27]. In particular, in the region of Borborema, State of Paraiba, the farms consist of highly diversified systems, with high abundance of natural enemies. The citrus areas are usually in a highly diversified landscape along with the annual crops (e.g.,
The use of mineral oil, vegetable oils, or derivatives may result in improved control strategies for agricultural pests and associated diseases and can cause minimal adverse effects on populations of natural enemies and other non-target species [43, 44]. Therefore as an alternative to chemical control, potential alternative products have been the subject of study by the group of researchers from the Federal University of Paraíba–UFPB [43, 44]. The interesting result is that some vegetable oils were effective and promoted ovicidal activity [42], for example, it is observed that cottonseed oil provided 100% egg mortality. Oils from
Activity on insect stage | Treatment (concentration or dose) [source] |
---|---|
Treatment with product from plants | |
Mortality on egg (90–100%) | Rott Nim® (1.5%), oils from |
Mortality on egg (60–89%) | |
Mortality on egg (40–59%) | Extract from |
Mortality on nymph (90–100%) | Oils from |
Mortality on nymph (50–70%) | Neem oil (1%) [38] |
Treatment with irradiation | |
Mortality on egg (90–100%) | Gamma irradiation (200 Gy) [45] |
In general, the use of chemical control for of CBF mentioned in this section should ultimately be used because it is too costly and inefficient [19], especially when performing on the clutches of this insect. In addition, high-dispersion by means of the adult flight favors the fast infestation of plants and orchard and cross infestation among citrus and other hosts and between neighboring groves [10]. This probably has hindered the effectiveness of chemical control because of the ease of reinfestation, especially in abundance of host sites. In Brazil, many are the hosts of the blackfly [4]. In Rio de Janeiro, for example, recently–three new host plants for
5. Induced resistance in citrus with silicon
Resistance induction corresponds to activation of the latent defense system in plants when they come in contact with compounds called elicitor agents. Among the elicitors, silicon has attracted the attention and interest of researchers. In addition to providing resistance, it may also provide nutritional benefits and increase the production and quality of agricultural products. The resistance induced by silicon is expressed in various ways, such as cell wall lignification, papillae formation, or induction of various defense proteins [48].
The use of silicon for the induced resistance of plants is a potential strategy in the integrated pest management, however this substance has not being considered as an essential nutritional element to the plants [49], but as potassium silicate, calcium silicate, and sodium silicate from other sources has determined the tolerance of many plant species to insects [50–53]. Silicon promoted cuticle thickening and accumulation of crystals on the leaf stomata in sugarcane [54]. The action of silicon may not be only restricted to resistance constitutive or induced but may also involve induced plant chemical defense [51].
Inducing agents sensitize the plant to activate their defense mechanisms in response to the presence of pests. These mechanisms may involve enzymes such as peroxidase, β-1,3-glucanase, chitinase, phenylalanine ammonia lyase, and polyphenol [55]. The peroxidase activity has been implicated in a variety of processes pertaining to the protection of plants, including hypersensitivity reaction, lignification, and suberization [56]. Hypersensitivity reaction is characterized as a fast and localized response. Among the main characteristics of the possible responses are the rapid and localized collapses of plant tissue around the site of infection, caused by the release of toxic compounds, which also act in some cases, directly on the pathogen, causing mortality. Structural barriers may involve lignification and suberisation and can be seen as physical defenses that restrict the development of insect pests. The lignification is a biochemical process that covers monolignol biosynthesis, transport, and polymerization in the cell wall, which in the first stage is highly mediated by enzymes intrinsic to the formation of the forerunners in the cytoplasmic compartments. The second stage is the formation of lignin in the cell wall. The oxy-reducing enzymes such as peroxidases and corresponding isoenzymes, act in the polymerization of lignin in the cell wall, forming a coordinate complex with hydrogen peroxide [57]. The deposition of lignin increases the resistance to the cell wall digestive enzymes of the insect pests. This resistance is also enhanced with presence of suberin or deposition of suberin lamella covering the cell wall of this process is called suberization.
Peroxidases participate in various physiological processes by catalyzing the oxidation and polymerization of hydroxycinnamic alcohol in the presence of hydrogen peroxide, resulting in lignin, an important physical barrier of plant defense [58], which contributes to strengthening the cell walls of the host. Changes in peroxidase activity by treatment with elicitors may indicate their involvement in resistance in plant induction [59]. Phenylalanine ammonia-lyase plays a fundamental role catalyzing the conversion of L-phenylalanine to trans-cinnamic acid, a deamination reaction. This reaction is considered an essential step in the phenylpropanoid pathway producing many products, including lignin, involved in plant defense reaction. The polyphenol oxidases are enzymes that often increase their activity in response to stress, and one of its main roles seems to be to promote the protection of the cell [60].
With hypotheses that silicon could to be an elicitor that potentiates the defense mechanisms of
Using principal components analysis–PCA, it is possible to see a clear characterization of the different patterns of peroxidase, polyphenol oxidase, and PAL activity in response to time after infestation of citrus blackfly. In addition, an isolated activity in relation to peroxidase and polyphenol oxidase may be observed, but there was overlap of activities between polyphenol and peroxidase activity (Figure 1).
There is evidence that the increase in peroxidase and polyphenol oxidase activity revealed the induction of synthesis of compounds for plant defense against CBF, but this effect depended on the time of
Silicon probably triggers the natural defense mechanisms of plants such as the production of phenolic compounds, chitinases, peroxidases, and lignin, which can interfere with the physiology and development insect pests, and consequently silicon can reduce the oviposition preference and provide sublethal effects such as extending the development time and nymphal mortality [50]. A positive correlation between peroxidase activity and the development of
Our results expressed in Figure 2, reveal that silicon doses promote low emergence rate. In the control treatment, an emergence rate was recorded as approximately 40%, significant reduction was observed with increasing of silicon doses with an emergence rate near to 5% in all doses used of silicon. But, it is clear that there is no great influence on eggs/clutch/female (Figure 2).
6. Final considerations
In Brazil, citrus is frequently affected by various pests. CBF has been causing severe damage, impacting the economy and reducing the citrus production. Mapping allows spatial visualization of the pest in the agroecosystem, allowing rational control with targeted applications, reduce production costs and decrease the negative impacts of pesticides, population fluctuation and spatial dependence of CBF in citrus, trapping as a representative sample of CBF is a tool to promote management of CBF, to decision making only when necessary. Conservative and release of natural enemies like Chrysopidae are potential to control CBF populations. Besides, to reduce populations of CBF ovicidal action based in some products such as oils from cotton seed,
References
- 1.
FAO - Food and Agriculture Organization of the United Nations. Citrus Fruit Statistics 2015. Rome: FAO; 2016. 53 p. - 2.
Lorenzi CO, Viana MM, Boteon M. Economic aspects of the São Paulo citrus chain= Aspectos econômicos da cadeia citrícola paulista. In: Andrade DJ, Ferreira MC, Martinelli NM, editors. Citrus Phytosanitary Aspects= Aspectos da Fitossanidade em Citros. 1st ed. Jaboticabal: Cultura Acadêmica; 2014. p. 11–29. - 3.
Vendramim JD, Pena MR, Silva NM. Citrus Fly, Aleurocanthus woglumi Ashby = Mosca-negra-dos-citros,Aleurocanthus woglumi Ashby. In: Vilela EF, Zucchi RA, editors. Introduced Pest in Brazil: insects and mites = Pragas introduzidas no Brasil: insetos e ácaros. Piracicaba: Fealq; 2015. p. 345–357. - 4.
Yamamoto PT; Paiva PEB. Evolution and management of citrus sucking insects = Evolução e manejo dos insetos sugadores dos citros. In: Andrade DJ, Ferreira MC, Martinelli NM, editors. Citrus Phytosanitary Aspects= Aspectos da fitossanidade em citros. 1st ed. Jaboticabal: Cultura Acadêmica; 2014. p. 119–141. - 5.
Lopez VF, Kairo MTK, Pollard GV, Pierre C, Commodore N, Dominique D. Post-release survey to assess impact and potential host range expansion by Amitus hesperidum andEncarsia perplexa , two parasitoids introduced for the biological control of the citrus blackfly,Aleurocanthus woglumi in Dominica. BioControl. 2009;54 :497–503. - 6.
Brasil. Ministério da Agricultura, Pecuária e Abastecimento - Secretaria de Defesa Agropecuária. Manual for control of citrus black fly ( Aleurocanthus woglumi ) = Manual para controle da mosca negra dos citros (Aleurocanthus woglumi ) [Internet]. 2008. Available from:http://www.agricultura.gov.br/arq_editor/file/vegetal/Importacao/Requisitos%20Sanit%C3%A1rios/Rela%C3%A7%C3%A3o%20de%20Pragas/MOSCANEGRADOSCITROS.pdf [Accessed: 2016-09-15] - 7.
Ashby SF. Notes on diseases of cultivated crops observed in 1913-1914. Bulletin of the Department of Agriculture. 1915; 2 :299–327. - 8.
Shivankar VJ, Ghosh DK, Das AK, Rao CN, editors. Insect and mite pests and their management. In: Tropical & Subtropical Citrus Health Management. 1st ed. New Delhi: Satish Serial Publishing House; 2015. p. 26–40. - 9.
Maia WJMS. Citrus black fly = Mosca-negra-dos-citros. In: Pinto, A.S.; Zaccaro, R.P, editors. Production of seedlings and phytosanitary management of citrus = Produção de mudas e manejo fitossanitário dos citros. 1st ed. Piracicaba: CP2; 2008. p. 37–48. - 10.
Mendonça MC, Oliveira DM, Santos TS, Silva LM, Teodoro AV. Phytosanitary management of the citrus fly Aleurocanthus woglumi in Sergipe = Manejo fitossanitário da mosca-negra-dos-citrosAleurocanthus woglumi em Sergipe [Internet]. Comunicado Técnico 157. 2015. Available from:http://ainfo.cnptia.embrapa.br/digital/bitstream/item/141752/1/cot-157.pdf [Accessed: 2016-09-14] - 11.
Raga A, Felippe N, Imperato R. Population dynamic of citrus blackfly, Aleurocanthus woglumi (Hemiptera: Aleyrodidae), in tahiti lime in the eastern of the state of São Paulo, Brazil. Annual Research & Review in Biology. 2016;11 :1–7. - 12.
Moraes BC, Oliveira JV, Maia WJV, Ferreira DBS, Souza, EB. Bioclimatic dynamics of the black citrus fly in Brazil = Dinâmica bioclimática da mosca negra dos citrus no Brasil. Revista Brasileira de Bioclimatologia. 2013; 13 :51–59. - 13.
Silva AG, Boiça Júnior AL, Farias PRS, Barbosa JC. Infestation of the citrus fly in citrus orchards in conventional and agroforestry systems = Infestação da mosca-negra-dos-citros em pomares de citros, em sistemas de plantio convencional e agroflorestal. Revista Brasileira de Fruticultura. 2011; 33 :53–60. - 14.
Figueredo LC. Phytosanitary management of the citrus fly ( Aleurocanthus woglumi Ashby) on the conditions of the citrus company alone [thesis] = Manejo fitossanitario de la mosca prieta de los citricos (Aleurocanthus woglumi Ashby) en las condiciones de la empresa de citricos sola [thesis]. La Havana: Instituto de Investigaciones de Fruticultura Tropical; 2002. - 15.
Medeiros FR, Lemos RNS, Ottati ALT, Araújo JRG, Machado KKG, Rodrigues, AAC. Population dynamics of the citrus fly Aleurocanthus woglumi Ashby (Hemiptera: Aleyrodidae) inCitrus spp. In the municipality of São Luís - MA = Dinâmica populacional da mosca-negra-dos-citrosAleurocanthus woglumi Ashby (Hemiptera: Aleyrodidae) emCitrus spp. no município de São Luís – MA. Revista Brasileira de Fruticultura. 2009;31 :1016–1021. - 16.
Vieira DL, Ottati ALT, Lemos RNS, Lopes GS, Araujo JRG. Population fluctuation and spatial dependence of Aleurocanthus woglumi Ashby, 1915 (Hemiptera: Aleyrodidae) inCitrus latifolia = Flutuação populacional e dependência espacial deAleurocanthus woglumi Ashby, 1915 (Hemiptera: Aleyrodidae) emCitrus latifolia . Revista Brasileira de Fruticultura. 2014;36 :862–871. - 17.
Silva AG, Farias PRS, Boiça Júnior AL, Lima BG, Ponte NHT, Pinho RC, Barbosa RS. Spatial analysis of black fly in citrus agroforestry system = Análise espacial da mosca-negra em sistema agroflorestal de citros. Comunicata Scientiae. 2015; 6 :350–358. - 18.
Orr D. Biological control and integrated pest management. In: Peshin, R, Dhawan AK, editors. Integrated pest management: innovation-development, process. 1st ed. Dordrecht: Springer Science+Business Media B.V.; 2009, p. 207–239. - 19.
Gill HK, Garg H. Pesticide: environmental impacts and management strategies. In: Solenski S, Larramenday ML, editors. Pesticides - Toxic Effects. 1st ed. Rijeka: Intech; 2014. p. 187–230. - 20.
Nguyen R, Fasulo TR. A citrus blackfly parasitoid, Encarsia perplexa Huang & Polaszek (Insecta: Hymenoptera: Aphelinidae) [Internet]. UF/IFAS Extension. Published: October 2001, revised: April 2010, reviewed July 2014. Available from:https://edis.ifas.ufl.edu/pdffiles/IN/IN51000.pdf [Accessed: 2016-08-24] - 21.
White, GL, Kairo MTK, Lopes ZV. Classical biological control of the citrus blackfly Aleurocanthus woglumi byAmitus hesperidum in Trinidad. BioControl. 2005;50 :751–759. - 22.
Nguyen R. A citrus blackly parasitoid, Amitus hesperidum Silvestri (Insecta: Hymenoptera: Platigasteridae) [Internet]. University of Florida – IFAS Extension. (Circular, 243). 2008. Available from:https://edis.ifas.ufl.edu/pdffiles/IN/IN51100.pdf [Accessed: 2016-09-19] - 23.
Oliveira R, Alves PRR, Costa WJD, Batista JL, Brito CH. Predatory capacity of Ceraeochrysa cubana on Aleurocanthus woglumi = Capacidade predatória deCeraeochrysa cubana sobreAleurocanthus woglumi . Revista Caatinga. 2014;27 :177–182. - 24.
Flanders SE. Herbert Smith’s observations on citrus blackfly parasites in India and Mexico and the correlated circumstances. Canadian Entomology. 1969; 101 :467–480. - 25.
Summy KR, Gilstrap FE, Hart WG, Caballero JM, Saenz I. Biological control of citrus blackfly (Homoptera: Aleyrodidae) in Texas. Environmental Entomology. 1983; 12 :782–786. - 26.
Hart WG, Selhime A, Harlan DP, Ingle SJ, Sanchez RM, Rhode RH, Garcia CA, Caballero J, Garcia RL. The introduction and establishment of parasites of citrus blackfly, Aleurocanthus woglumi in Florida (Homoptera: Aleyrodidae). Entomophaga. 1978;23 :361–366. - 27.
Thomas DB. Integrated pest management with the sterile insect technique. In: Koul O, Cuperus GW. Ecologically based integrated pest management. 1st ed. Wallingford: CABI; 2007. p. 200–1. - 28.
Martin, U. Citrus blackfly control in Dominica Tropical. Fruits Newsletter. 1999; 32 : 3-6. - 29.
Nguyen R, Hamon AB. Citrus blackfly, Aleurocanthus woglumi Ashby (Homoptera: Aleyrodidae) [Internet]. Gainvesville Florida Departament of Agriculture & Consumer Service – Division of Planta Industry, 3p. (Circular, 360). 1993. Available from:https://edis.ifas.ufl.edu/pdffiles/IN/IN19900.pdf [Accessed: 2016-07-14] - 30.
Parkinson K, Seales J. Citrus blackfly, its presence and management in Trinidad and Tobago. Procaribe News. Trinidad and Tobago, Caribbean Integrated Pest Management Network. 2000; 11 p. - 31.
Silva AB, Gueiredo HB, Melo MM. The black fly of the citrus ( Aleurocanthus woglumi Ashby): all care is little! Protect your orchard. Do not let this pest enter = A mosca negra dos citros (Aleurocanthus woglumi Ashby): todo cuidado é pouco! Proteja seu pomar. Não deixe esta praga entrar. Belém: Ministério da Agricultura Pecuária e Abastecimento /Secretaria Executiva de Agricultura; 2001. - 32.
Alvim RG, Aguiar-Menezes EL, Lima AF. Dissemination of Aleurocanthus woglumi in citrus plants, its natural enemies and new host plants in the state of Rio de Janeiro, Brazil. Ciência Rural. 2016;46 : 1–7. - 33.
Oliveira R, Barbosa VO, Vieira DL, Oliveira FQ, Batista JL, Brito CB. Development and reproduction of Ceraeochrysa cubana (Neuroptera: Chrysopidae) fed withAleurocanthus woglumi (Hemiptera: Aleyrodidae). Semina: Ciências Agrárias. 2016;37 :17–24. - 34.
Maia WJMS, Maia TJAF, Mendonça DC, Leão TAC, Pinheiro SJP, Oliveira ASS, Bernardes BB. Diversity of the entomofauna of natural enemies of Aleurocanthus woglumi Ashby (Hemiptera: Aleyrodidae), in the municipalities of Belém, Captain Poço and Irituiar = Diversidade da entomofauna de inimigos naturais de Aleurocanthus woglumi Ashby (Hemiptera: Aleyrodidae), nos municípios paraenses de Belém, Capitão Poço e Irituia. Anais do 20˚ Congresso Brasileiro de Entomologia, 2004; Gramado, p. 400 - 35.
Maia WJMS, Souza JC, Marques LC, Silva LMS, Benaduce RV, Gentil RM. Infestation in citrus by Aleurocanthus woglumi (Ashby) and biological control perspectives applied in Pará= Infestação em citros por Aleurocanthus woglumi (Ashby) e perspectivas de controle biológico aplicado no Pará. Anais do 9˚ Simpósio de Controle Biológico; 2005; Recife, p. 183 - 36.
Heu RA, Nagamine WT. Citrus blackfly Aleurocanthus woglumi Ashby (Homoptera: Aleyrodidae). Hawaii Department of Agriculture, Division of Plant Industry, New Pest Advisory. 2001;99 : 1–3. - 37.
French JV, Meagher Jr. RL. Citrus blackfly: chemical control on nursery citrus. Subtropical Plant Science. 1992; 45 : 7–10. - 38.
Jabhav VB, Gohil SN, Patil RV. Management of citrus blackfly ( Aleurocanthus woglumi Ashby) with conventional arid botanical insecticides. Ecology, Environment and Conservation Paper. 2006;12 : 677–679. - 39.
Brasil. Ministério da Agricultura Pecuária e Abastecimento [Internet]. 2016. Available from: http://extranet.agricultura.gov.br/agrofit_cons/principal_agrofit_cons [Accessed: 2016-10-02] - 40.
Knapp JSL. Control of insects, mites and diseases of Florida’s Dooryard Citrus trees [Internet] . Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida, (Circular,139). 1994. Available from: http://www.floridaplants.com/Reprints/citrus.htm [Accessed: 2016-09-02] - 41.
Ramalho FS, Fernandes FS, Nascimento ARB, Nascimento JL, Malaquias JB, Silva CAD. Feeding damage from cotton aphids, Aphis gossypii Glover (Hemiptera: Heteroptera: Aphididae), in cotton with colored fiber intercropped with fennel. Annals of the Entomological Society of America. 2012;105 : 20–27. - 42.
AS-PTA – Assessoria e Serviços a Projetos em Agricultura Alternativa. Use of natural products to combat black flies [Internet] = Uso de produtos naturais no combate à mosca-negra [Internet]. Folha Agroecológica. Pólo Borborema – AS-PTA PB, no. 2, May 2010. Available from: http://aspta.org.br/wp-content/uploads/2011/05/Uso-de-produtos-naturais-no-combate-a-mosca-negra.pdf [Accessed: 2016-09-04] - 43.
Silva JG, Batista JL, Silva JG, Brito CH. Use of vegetable oils in the control of the citrus black fly, Aleurocanthus woglumi (Hemiptera: Aleyrodidae). Revista Colombiana de Entomología. 2012;38 : 182–186. - 44.
Vieira DL, Souza GMM, Oliveira R, Barbosa, VO, Batista JL, Pereira WE. Application of commercial oils in the ovicidal control of Aleurocanthus woglumi Asbhy = Aplicação de óleos comerciais no controle ovicida de Aleurocanthus woglumi Asbhy. Bioscience Journal. 2013;29 : 1126–1129. - 45.
Villavicencio ALCH, Araújo MM, Fanaro GB, Costa HHSF, Silva PPV, Arthur V, Faria JT. Gamma irradiation as a quarantine treatment against eggs of citrus black fly ( Aleurocanthus woglumi Ashby) [Internet]. International Nuclear Atlantic Conference (INAC); Rio de Janeiro. September 27 to October 2 2009. Available from:http://www.iaea.org/inis/collection/NCLCollectionStore/_Public/41/072/41072624.pdf [Accessed: 2016-09-04] - 46.
Oliveira FQ, Malaquias JB, Figueiredo WRS, Batista JL, Bezerra EB. Inhibition of fruit infestation by Mediterranean fruit fly using natural products. African Journal of Biotechnology. 2012; 11 : 13922. - 47.
Oliveira FQ, Malaquias JB, Figueiredo WRS, Batista JL, Beserra EB, Oliveira R. . Insecticidal activity of bioproducts on Ceratitis capitata Wiedemann (Diptera: Tephritidae). African Journal of Biotechnology; 2014;12 : 1430–1438. - 48.
Fauteux FR, Mus-Borel W, Menzies J, Belanger RR. Silicon and plant disease resistance against pathogenic fungi. FEMS Microbiology Letters. 2005; 249 : 1–6. - 49.
Basagli MAB, Moraes JC, Moraes GAC, Ecole CC, Gonçalves-Gervásio RCR. Effect of sodium silicate application on the resistance of wheat plants to the green-aphids Schizaphis graminum (Rond.) (Hemiptera: Aphididae). Neotropical Entomology. 2003;32 : 659–663. - 50.
Correa RSB, Moraes JC, Auad AM, Carvalho GA. Silicon and acibenzolar-S-methyl as resistance inducers in cucumber, against the whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) biotype B. Neotropical Entomology. 2005;34 : 429–433. - 51.
Costa RR, Moraes JC, DaCosta RR. Feeding behaviour of the greenbug Schizaphis graminum on wheat plants treated with imidacloprid and/or silicon. Journal of Applied Entomology. 2011;135 : 115–120. - 52.
Ferreira RS, Moraes JC, Antunes CS. Silicon influence on resistance induction on against Bemisia tabaci Biotype B (Genn.) (Hemiptera: Aleyrodidae) and on vegetative development in two soybean cultivars. Neotropical Entomology. 2011;40 : 495–500. - 53.
Dias PAS, Sampaio MV, Rodrigues MP, Korndörfer AP, Oliveira RS, Ferreira SE, Korndörfer GH. Induction of resistance by silicon in wheat plants to alate and apterous morphs of Sitobion avenae (Hemiptera: Aphididae). Environmental Entomology. 2014;43 : 949–956. - 54.
Vilela M, Moraes JC, Alves, E, Santos-Cividanes, TM, Santos, FA. Induced resistance to Diatraea saccharalis (Lepidoptera: Crambidae) via silicon application in sugarcane. Revista Colombiana de Entomología. 2014;40 : 44–48. - 55.
Cavalcanti LS, Brunelli KR, Stangarlin JR. Biochemical and molecular aspects of induced resistance = Aspectos bioquímicos e moleculares da resistência induzida. In: Cavalcanti LS, Di Piero, RM, Cia P, Pascholati SF, Resende MLV, Romeiro RS, editors. Induction of resistance in plants to pathogens and insects = Indução de resistência em plantas a patógenos e insetos. Piracicaba SP. FEALQ: Piracicaba; 2005. p. 81–124. - 56.
Nicholson RL, Hammerschmidt R. Phenolic compounds and their role in disease resistance. Annual Review of Phytopathology. 1992; 30 : 369–389. - 57.
Ranocha P, Chabanes M, Chamayou S, Jauneau A, Boudet AM, Goffner D. Laccasse down-regulation causes alterations in phenolic metabolism and cell wall structure in poplar. Plant Physiology. 2002; 129 : 145–155. - 58.
Pomar F, Bernal MA, Díaz J, Merino F. Purification, characterization and kinetic proprieties of pepper fruit acid peroxidase. Phytochemistry. 1997; 46 : 1313–1317. - 59.
Pereira LF, Goodwin PH, Erickson L. Peroxidase activity during susceptible and resistant interactions between cassava ( Manihot esculenta ) andXanthomonas axonopodis pv.manihotis andXanthomonas cassavae . Journal Phytopathology. 2000;148 : 575–577. - 60.
Soares RM, Maringoni AC, Lima GPP. Inefficiency of acibenzolar-S-methyl in the induction of resistance of common bean to the wilt-of-shortbacterium = Ineficiência de acibenzolar-S-methyl na indução de resistência de feijoeiro comum à murcha-de-curtobacterium, Fitopatologia Brasileira. 2004; 29 : 372–377. - 61.
Vieira DL, Barbosa VO, Souza WCO, Silva JG, Malaquias JB, Batista JL. Potassium silicate-induced resistance against blackfly in seedlings of Citrus reticulate . Fruits. 2016;71 : 49–55. - 62.
Vieira DL. Induction of resistance in Citrus reticulata and ovicidal action of vegetable oils onAleurocanthus woglumi Asbhy [thesis] = Indução de resistência emCitrus reticulata e ação ovicida de óleos vegetais sobreAleurocanthus woglumi Asbhy [thesis]. Areia: Universidade Federal da Paraíba; 2013. - 63.
Castro RS, Pena MR, Silva NM, Vendramim JD, Costa IB. Ovicidal activity of aqueous extracts of leaves of Piper aduncum L. on the citrus fly,Aleurocanthus woglumi Ashby (Aleyrodidae) under laboratory conditions = Atividade ovicida de extratos aquosos de folhas dePiper aduncum L. sobre a mosca-negra-dos-citros,Aleurocanthus woglumi Ashby (Aleyrodidae) em condições de laboratório. Proceedings of the 61th Reunião Anual da SBPC; UFAM, Manaus, AM. [Internet]. 2009. Available from:http://www.sbpcnet.org.br/livro/61ra/resumos/resumos/4179.htm [19 September 2016].