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Population Fluctuation of Selenaspidus articulatus Morgan (Hemiptera: Diaspididae) in Rubber Tree

Abstract

Rubber tree is the main source of natural rubber in the world. Because of its economic importance, cultivation was accentuated in several regions of Brazil in the form of monoculture, thus favoring insects to establish in the crop. Among them, the West Indian red scale cochineal Selenaspidus articulatus stands out, responsible for injuring rubber plants due to sap sucking. This work evaluated the fluctuation of S. articulatus in rubber tree clones. Sampling was carried out by collecting leaves every 15 days from PB 235, RRIM 600, PR 255 and GT 1 clones during the period of March 2013 and March 2014. RRIM 600 clone showed the highest population level of S. articulatus, with a population peak of 14.88 insects/leaf in June. PR 255 clone had the lowest scale infestation, demonstrating this clone’s possible resistance to this species. This is the first report of S. articulatus occurrence in Goiás.

Keywords:
West Indian red scale; Hevea brasiliensis; seasonality

1. INTRODUCTION AND OBJECTIVES

The rubber tree Hevea brasiliensis Müell. Arg. (Euphorbiaceae) is a native species to the Amazon region and stands out as being the main source of natural rubber in the world (Coelho et al., 2009Coelho LM Jr, Rezende JLP, Borges LAC, Oliveira AD. Análise temporal da borracha natural brasileira. Cerne 2009; 15(1): 19-26.; Gonçalves et al., 2002Gonçalves PS, Martins ALM, Furtado EL, Sambugaro R, Ottati EL, Ortolani AA et al. Desempenho de clones de seringueira da série IAC 300 na região do planalto de São Paulo. Pesquisa Agropecuária Brasileira 2002; 37(2): 131-138. 10.1590/S0100-204X2002000200003
https://doi.org/10.1590/S0100-204X200200...
). This plant is associated with a pest complex, especially mites (Ferla & Moraes, 2008Ferla NJ, Moraes GJ. Flutuação populacional e sintomas de dano por ácaros (Acari) em seringueira no estado do Mato Grosso, Brasil. Revista Árvore 2008; 32(2): 365-376. 10.1590/S0100-67622008000200019
https://doi.org/10.1590/S0100-6762200800...
), leaf-cutting ants of the Atta and Acromyrmex genus (Anjos et al., 2008Anjos N, Arnhold A, Corrêa GVV, Stumpf K. Árvores e formigas cortadeiras (Hymenoptera: Formicidae) em Viçosa, Minas Gerais. Revista Trópica: Ciências Agrárias e Biológicas 2008; 2(1): 11-16.) and the lace bug Leptopharsa heveae Drake & Poor (Santos & Freitas, 2008Santos RS, Freitas S. Erythmelus tingitiphagus (Hymenoptera: Mymaridae): um agente promissor no controle biológico do percevejo-de-renda (Hemiptera: Tingidae) da seringueira. Agrotrópica 2008; 20: 25-28.). In addition to these, there are reports of other associated insects, among them termites, chrysomelids, whiteflies, cochineals, mole crickets, wood boring beetles and caterpillars (Santos & Pereira, 2008Santos GP, Pereira JMM. Insetos e ácaros associados à cultura da seringueira. In: Alvarenga AP, Carmo CAFS. Seringueira. Viçosa: EPAMIG; 2008. p. 535-597.).

The first report of high Selenaspidus articulatus cochineal populations in rubber trees occurred in 1988 in the municipality of Olímpia, São Paulo state (Bergmann et al., 1988Bergmann EC, Stradioto MF, Brisolla AD. Ocorrência de Selenaspidus articulatus (Morgan, 1889) em cultura de seringueira (Hevea brasiliensis Muell. Arg.) no município de Olímpia, estado de São Paulo. O Biológico 1988; 54(1-6): 27-28.). Belonging to the group of scaled cochineals, they cause damage to perennial and ornamental plants (Culik et al., 2008Culik MP, Martins DS, Ventura JA, Wolff VS. Diaspididae (Hemiptera: Coccoidea) of Espírito Santo, Brazil. Journal of Insect Science 2008; 8(1): 1-6. 10.1673/031.008.1701
https://doi.org/10.1673/031.008.1701...
) and are considered important pests (Henderson, 2011Henderson RC. Diaspididae (Insecta: Hemiptera: Coccoidea). Lincoln: Manaaki Whenus Press; 2011. (Fauna of New Zealand, n. 66).). The main damage is caused by continuous sap sucking from leaves, fruits and branches. However, these insects can introduce toxins that cause leaf fall and influence fruit quality (Bartra, 1974Bartra PCE. Biologia de Selenaspidus articulatus Morgan y sus principales controladores biológicos. Revista Peruana de Entomología 1974; 17(1): 60-68.). The genera Pinnaspis, Aspidiotus and Saissetia are found in the rubber tree culture (Bergmann et al., 1988Bergmann EC, Stradioto MF, Brisolla AD. Ocorrência de Selenaspidus articulatus (Morgan, 1889) em cultura de seringueira (Hevea brasiliensis Muell. Arg.) no município de Olímpia, estado de São Paulo. O Biológico 1988; 54(1-6): 27-28.; Bergmann et al., 1991Bergmann EC, Imenes SDL, Tavares MT. Occurrence of the scale insect Aspidiotus sp. (Hemiptera: Diaspididae) and its parasitoids on ciones of rubber plants in Sao Paulo state. Arquivos do Instituto Biológico 1991; 58(1-2): 65-67.). Santos & Pereira (2008Santos GP, Pereira JMM. Insetos e ácaros associados à cultura da seringueira. In: Alvarenga AP, Carmo CAFS. Seringueira. Viçosa: EPAMIG; 2008. p. 535-597.) report some species associated with rubber tree, such as Pinnaspis sp., Aspidiotus destructor Signoret, Saissetia coffeae Walker, Sa. oleae Oliv., Parasaissetia nigra Nietner, Asterolecanium pustulans Cockerell and Hemiberlesia lataniae Signoret.

West Indian red scale S. articulatus has been reported in Brazil in several species of host plants in the tropical and subtropical regions, namely cherimoya (Annona cherimola), coconut palm (Cocos nucifera), passion fruit (Passiflora edulis), mango (Mangifera indica), banana (Musa spp.), soursop (Annona muricata), avocado (Persea americana), black pepper (Piper nigrum) and palm trees (Bartra, 1974Bartra PCE. Biologia de Selenaspidus articulatus Morgan y sus principales controladores biológicos. Revista Peruana de Entomología 1974; 17(1): 60-68.). However, this species is associated with other host species, among them Citrus limon (Hodgson & Lagowska, 2011Hodgson CJ, Lagowska B. New scale insect (Hemiptera: Sternorrhyncha: Coccoidea) records from Fiji: three new species, records of several new invasive species and an updated checklist of Coccoidea. Zootaxa 2011; 2766(1): 1-29. 10.11646/zootaxa.2766.1.1
https://doi.org/10.11646/zootaxa.2766.1....
), Citrus reticulata (Rodrigues et al., 2009Rodrigues WC, Cassino PCR, Spolidoro MV, Silva Filho R. Insetos sugadores (Sternorrhyncha) em cultivo orgânico de tangerina cv. poncã (Citrus reticulata Blanco): diversidade, constância, freqüência e flutuação populacional. EntomoBrasilis 2009; 2(2): 42-48.), Citrus latifolia (Vargas et al., 2015Vargas AS, Duarte MN, Santos MRG, Moura LC, Cassino PCR. Dinâmica populacional de insetos-praga em um cultivo agroecológico de lima ácida Tahiti (Citrus latifolia Tanaka) no município de Vassouras-RJ. Revista Eletrônica Teccen 2015; 8(2): 81-84. 10.21727/teccen.v8i2.519
https://doi.org/10.21727/teccen.v8i2.519...
), Coffea spp., Ficus sp., Gardenia sp., Pandanus sp. (García et al., 2016García MM, Denno BD, Miller DR, Miller GL, Ben-Dov Y, Hardy NB. ScaleNet: a literature-based model of scale insect biology and systematics. Oxford: Database; 2016. 10.1093/database/bav118
https://doi.org/10.1093/database/bav118...
), rubber tree (Bergmann et al., 1988Bergmann EC, Stradioto MF, Brisolla AD. Ocorrência de Selenaspidus articulatus (Morgan, 1889) em cultura de seringueira (Hevea brasiliensis Muell. Arg.) no município de Olímpia, estado de São Paulo. O Biológico 1988; 54(1-6): 27-28.) and Mimosa caesalpiniaefolia (Ferraz, 1997Ferraz LF. Infestação de cochonilha-pardinha em sansão-do-campo usado como cerca viva em pomares de laranja. Bragantia 1997; 56(2): 289-290. 10.1590/S0006-87051997000200008
https://doi.org/10.1590/S0006-8705199700...
).

In recent years, an increase in the S. articulatus population in escape areas of the rubber tree has been observed. In some areas, the S. articulatus population is higher than L. heveae. However, no studies on this species have been carried out on rubber tree since the first report. It is necessary to verify the seasonality of this insect in several environments to contribute to integrated pest management in rubber tree plantation. In addition, it is necessary to observe if the rubber tree clones influence the population of this species. Thus, the objective of this study was to evaluate the population of West Indian red scale cochineals in rubber tree clones.

2. MATERIALS AND METHODS

The study was carried out in the commercial areas of OL Látex Ltda. (15°19’21” S and 49°9’32” W) (Figure 1) in the municipality of Goianésia, Goiás, Brazil. The climate of the region is Aw, tropical climate with dry winter season, according to the Koppen classification, with a well-defined rainy summer season and dry winter.

Figure 1
Covoá farm rubber tree area. Goianésia, Goiás, Brazil.

Sampling was performed in areas of PB 235, RRIM 600, PR 255 and GT 1 clones. The evaluations occurred every 15 days, quantifying the amount of S. articulatus during the period of March 2013 and March 2014, totalizing 26 evaluations.

At each sampling, 15 trees/clones were randomly selected, and three leaves/plants were collected at a height of 7 m using pruning shears with a telescopic handle. After the collection, the leaves were packed in plastic bags and transported in an isothermal polystyrene box refrigerated with gel packs. The samples were kept in the laboratory under refrigeration at 10 °C for not more than one week until evaluation which was done using a stereoscopic microscope to observe and count the number of nymphs and adults of S. articulatus on the leaves (Figure 2).

Figure 2
Selenaspidus articulatus in a rubber tree leaf.

The relation between population density (mean of adults and nymphs/leaf) and meteorological data (maximum, minimum and mean temperature (°C), relative humidity (%), and precipitation (mm)) was assessed by linear correlation. The climatic data used were obtained from the Usina Jalles Machado S.A. meteorological station (Figure 3), located in the municipality of Goianésia, Goiás, Brazil (15°12’43” S and 48°59’13” W) 22 km from the study area.

Figure 3
Climatic data (precipitation, average temperature, minimum temperature, maximum temperature and relative humidity) in the periods of 2013-2014 of Usina Jalles Machado meteorological station, Goianésia, Goiás, Brazil.

The data obtained from the insect population during the study period are presented in the population fluctuation plot generated by the R program. The comparison between the clones was performed using the 95% confidence interval, considering that the population peak occurred between March and July. The population was compared by checking the overlap of the error bars.

3. RESULTS AND DISCUSSION

Selenaspidus articulatus was observed in greater abundance from March to July, before the natural senescence period of the leaves (Figure 4). After this period, the insect population reduced drastically; however, from December to January a gradual increase in the population was observed, limited by a decrease in February, followed by a new increase in March. The longest occurrence period of S. articulatus was observed in GT 1 and RRIM 600 clones, whose infestation occurred during four months from April to the second fortnight of July, and from March to June, respectively.

Figure 4
Selenaspidus articulatus population fluctuation in rubber tree clones. Goianésia, Goiás, Brazil.

The natural senescence of the clones occurred in July and August. With leaf resprouting, West Indian red scale populations were higher in the months preceding natural senescence, after the end of the rainy season. This population peak coincides with the population increase in the C. heveae mite, which mainly occurs from March (Demite & Feres, 2005Demite PR, Feres RJ. Influência de vegetação vizinha na distribuição de ácaros em seringal (Hevea brasiliensis Muell. Arg., Euphorbiaceae) em São José do Rio Preto, SP. Neotropical Entomology 2005; 34(5): 829-836. 10.1590/S1519-566X2005000500016
https://doi.org/10.1590/S1519-566X200500...
; Hernandes & Feres, 2006Hernandes FA, Feres RJ. Diversidade e sazonalidade de ácaros (Acari) em seringal (Hevea brasiliensis Muell. Arg.) no noroeste do estado de São Paulo. Neotropical Entomology 2006; 35(4): 523-535. 10.1590/S1519-566X2006000400016
https://doi.org/10.1590/S1519-566X200600...
; Martins et al., 2012Martins GLM, Vieira MR, Barbosa JC, Dini TA, Manzano AM, Alves BMS et al. Distribuição espacial de Calacarus heveae Feres na cultura da seringueira em Marinópolis-São Paulo. Revista Árvore 2012; 36(2): 211-217. 10.1590/S0100-67622012000200002
https://doi.org/10.1590/S0100-6762201200...
; Vis et al., 2006Vis RM, Moraes GJD, Bellini MR. Mites (Acari) of rubber trees (Hevea brasiliensis Muell. Arg., Euphorbiaceae) in Piracicaba, state of São Paulo, Brazil. Neotropical Entomology 2006; 35(1): 112-120. 10.1590/S1519-566X200600010001
https://doi.org/10.1590/S1519-566X200600...
). The development, reproduction and survival of C. heveae are favored in rubber tree between January and April (Daud et al., 2012Daud RD, Feres RJF, Hernandes FA. Seasonal suitability of three rubber tree clones to Calacarus heveae (Acari, Eriophyidae). Experimental and Applied Acarology 2012; 56(1): 57-68. 10.1007/s10493-011-9494-9
https://doi.org/10.1007/s10493-011-9494-...
). Therefore, it can be observed that plant phenology is a factor that contributes to the West Indian red scale population increase. According to Santos et al. (2012Santos RS, Costa VA, Silva JM, Freitas S. Population dynamics of Leptopharsa heveae (Hemiptera: Tingidae) and Erythmelus tingitiphagus (Hymenoptera: Mymaridae) in rubber tree plants. Revista Colombiana de Entomología 2012; 38(2): 214-319.), the rubber tree reaches its maximum level of foliage in October, with an increase of soluble nitrogen also occurring due to a rise of precipitation which may favor the population peak of L. heveae.

The increase in the population of this species in PB 235 clone began at the end of April and the population peak occurred at the beginning of July. After leaf senescence in the dry period of the year, the West Indian red scale cochineal population was observed in a reduced number in all studied clones, rising again in March 2014. The second population peak of the species occurred in March in PB 235, GT 1 and PR 255 clones. In the following year, the population only remained low in the RRIM 600 clone.

The RRIM 600 clone presented the highest population level of the West Indian red scale cochineal of 14.88 individuals/leaf, followed by the GT 1 clone with a population peak of 10.26 at the end of June. At the beginning of July, the PB 235 clone had a population of eight insects/leaf. However, at the end of the same month, there was a decrease in the insect population due to natural senescence. Bergmann et al. (1988Bergmann EC, Stradioto MF, Brisolla AD. Ocorrência de Selenaspidus articulatus (Morgan, 1889) em cultura de seringueira (Hevea brasiliensis Muell. Arg.) no município de Olímpia, estado de São Paulo. O Biológico 1988; 54(1-6): 27-28.) observed a high S. articulatus population in March and April in the RRIM 600 clone in the state of São Paulo. The population in this study was mainly observed from April to June 2013, with a population peak in April.

PR 255 clone presented the lowest cochineal infestation throughout the study. The population began to increase in late May, and the peak population occurred in June (1.7 insects/leaf). The population was three times smaller than the other clones. The cochineal population varied among the evaluated rubber tree clones (Figure 5). PR 255 clone stood out with the lowest population, in contrast to PB 235, GT 1 and RRIM 600 clones. The smallest population in PR 255 is possibly related to the resistance of this clone to S. articulatus.

Figure 5
Selenaspidus articulatus (± 95% confidence interval) population in rubber tree clones. Goianésia, Goiás, Brazil.

This result may be indicative of resistance, as Vieira et al. (2009Vieira MR, Silva HAS, Cardoso MM, Figueira JC. Progênies de seringueira com potencial para conferir resistência a ácaros (Calacarus heveae Feres e Tenuipalpus heveae Baker). Ciência Rural 2009; 39(7): 1953-1959. 10.1590/S0103-84782009005000164
https://doi.org/10.1590/S0103-8478200900...
) observed that the FRP/12110 progeny was less attacked by mites (Calacarus heveae and Tenuipalpus heveae), presenting to non-preference or antibiosis resistance. In studies carried out by Ferla & Moraes (2008Ferla NJ, Moraes GJ. Flutuação populacional e sintomas de dano por ácaros (Acari) em seringueira no estado do Mato Grosso, Brasil. Revista Árvore 2008; 32(2): 365-376. 10.1590/S0100-67622008000200019
https://doi.org/10.1590/S0100-6762200800...
), it was possible to observe that PB 260 and PR 255 clones presented larger C. heveae populations and leaf damage. Therefore, rubber tree clones influence the population of mites.

This difference between the West Indian red scale populations may be correlated to the clones’ resistance. However, other factors may influence this population, such as latex production, clone adaptations to soil and climate conditions (Daud et al., 2012Daud RD, Feres RJF, Hernandes FA. Seasonal suitability of three rubber tree clones to Calacarus heveae (Acari, Eriophyidae). Experimental and Applied Acarology 2012; 56(1): 57-68. 10.1007/s10493-011-9494-9
https://doi.org/10.1007/s10493-011-9494-...
). Daud et al. (2013Daud RD, Feres RJF. Community structure of mites (Arachnida: Acari) in six rubber tree clones. International Journal of Acarology 2013; 39(8): 589-596. 10.1080/01647954.2013.856470
https://doi.org/10.1080/01647954.2013.85...
) observed that rubber tree clones may influence the populations of mites. The authors observed that the PB 260 clone presented a smaller population of phytophagous species, whereas the GT 1 clone had the largest population of predators.

The different insect population densities throughout the year are directly related to the climatic conditions, the characteristics of the studied region, and possibly due to the presence of natural enemies that can act in naturally controlling this species. Coccinellids, such as Pentilia egena Mulsant, Coccidophilus citricola Brèthes, Azya luteipes Mulsant, Cycloneda sanguinea L. and Scymnus spp., are important natural enemies of S. articulatus in citrus (Rodrigues et al., 2008Rodrigues WC, Cassino PCR, Silva Filho R. Ocorrência e distribuição de coccinelídeos (Coleoptera, Coccinellidae) associados às plantas cítricas no estado do Rio de Janeiro. EntomoBrasilis 2008; 1(2): 23-27.).

In addition to predatory insects, entomopathogenic fungi stand out, influencing the insect population mainly during periods of high temperature and humidity (Santos & Pereira, 2008Santos GP, Pereira JMM. Insetos e ácaros associados à cultura da seringueira. In: Alvarenga AP, Carmo CAFS. Seringueira. Viçosa: EPAMIG; 2008. p. 535-597.). Long periods of drought may contribute to increasing the insect population due to the lack of favorable conditions for these pathogens to develop.

Perruso & Cassino (1993Perruso JC, Cassino PCR. Flutuação populacional de Selenaspidus articulatus (Morgan) (Hemiptera: Diaspididae) em Citrus sinensis (L.) no estado do Rio de Janeiro. Anais da Sociedade Entomológica do Brasil 1993; 22: 401-404.) observed lower S. articulatus infestation in Citrus sinensis L. between March and July when temperature and precipitation presented low rates. However, it was possible to observe that the difference in the results in the present study mainly occurs due to phenology and the leaf age in the rubber tree. Moreover, a decrease in the cochineal population in the rubber tree was observed during the rainy season.

No significant correlations were observed between S. articulatus infestation in clones and climatic data. In this case, the physiological conditions of the plant may have influenced the West Indian red scale cochineal population. According to Souza et al. (2015Souza GCD, Redaelli LR, Wolff VRDS. Population dynamics of Saissetia oleae (Hemiptera: Coccidae) on olive trees. Revista Brasileira de Fruticultura 2015; 37(4): 852-858. 10.1590/0100-2945-213/14
https://doi.org/10.1590/0100-2945-213/14...
), temperature is the factor that most affects the population size of S. oleae. However, this climatic factor apparently did not influence the West Indian red scale cochineal population in rubber tree.

According to Bergmann et al. (1988Bergmann EC, Stradioto MF, Brisolla AD. Ocorrência de Selenaspidus articulatus (Morgan, 1889) em cultura de seringueira (Hevea brasiliensis Muell. Arg.) no município de Olímpia, estado de São Paulo. O Biológico 1988; 54(1-6): 27-28.), S. articulatus has higher importance in citrus cultivation, and high populations of this insect in rubber trees are related to their proximity to citrus areas. However, the site of this study only has pasture and native vegetation neighboring the rubber tree. Thus, it is believed that the population of this insect is not correlated with citriculture.

West Indian red scale is a cosmopolitan species of African origin (Miller et al., 2005Miller DR, Miller GL, Hodges GS, Davidson JA. Introduced scale insects (Hemiptera: Coccoidea) of the United States and their impact on U.S. agriculture. Proceedings of the Entomological Society of Washington 2005; 107: 123-158.), but it is the only species of Selenaspidus genus that came to be neotropical (Ben-Dov, 2013Ben-Dov Y. ScaleNet catalogue for Selenaspidus [Internet]. 2013 [cited 2019 Aug. 16]. Available from: Available from: https://bit.ly/2OXMQWZ
https://bit.ly/2OXMQWZ...
). The high incidence of this and other insect species represents a potential challenge for tropical forestry and conservation (Normark et al., 2014Normark BB, Morse GE, Krewinski A, Okusu A. Armored scale insects (Hemiptera: Diaspididae) of San Lorenzo National Park, Panama, with descriptions of two new species. Annals of the Entomological Society of America 2014; 107(1): 37-49. 10.1603/AN13110
https://doi.org/10.1603/AN13110...
). S. articulatus was introduced in Brazil and is present in the states of Amazonas, Rio Grande do Norte, Espírito Santo, Minas Gerais, Rio de Janeiro, São Paulo and Rio Grande do Sul (García et al., 2016García MM, Denno BD, Miller DR, Miller GL, Ben-Dov Y, Hardy NB. ScaleNet: a literature-based model of scale insect biology and systematics. Oxford: Database; 2016. 10.1093/database/bav118
https://doi.org/10.1093/database/bav118...
; Martins et al., 2004Martins DS, Culik MP, Wolff VRS. New record of scale insects (Hemiptera: Coccoidea) as pests of papaya in Brazil. Neotropical Entomology 2004; 33(5): 655-657. 10.1590/S1519-566X2004000500018
https://doi.org/10.1590/S1519-566X200400...
). In this way, this is the first report of S. articulatus in the state of Goiás.

4. Conclusions

Population peaks of S. articulatus occurred before the natural senescence period of the rubber tree. PR 255 clone presents the smallest S. articulatus population. This is the first report of S. articulatus occurrence in Goiás state.

Acknowledgements

We thank OL Látex Ltda. for allowing us performing our work in its property and for the technical support for field samples. We also thank Ana Lucia Benfatti Gonzalez Peronti for identifying the cochineal.

References

  • Anjos N, Arnhold A, Corrêa GVV, Stumpf K. Árvores e formigas cortadeiras (Hymenoptera: Formicidae) em Viçosa, Minas Gerais. Revista Trópica: Ciências Agrárias e Biológicas 2008; 2(1): 11-16.
  • Bartra PCE. Biologia de Selenaspidus articulatus Morgan y sus principales controladores biológicos. Revista Peruana de Entomología 1974; 17(1): 60-68.
  • Ben-Dov Y. ScaleNet catalogue for Selenaspidus [Internet]. 2013 [cited 2019 Aug. 16]. Available from: Available from: https://bit.ly/2OXMQWZ
    » https://bit.ly/2OXMQWZ
  • Bergmann EC, Imenes SDL, Tavares MT. Occurrence of the scale insect Aspidiotus sp. (Hemiptera: Diaspididae) and its parasitoids on ciones of rubber plants in Sao Paulo state. Arquivos do Instituto Biológico 1991; 58(1-2): 65-67.
  • Bergmann EC, Stradioto MF, Brisolla AD. Ocorrência de Selenaspidus articulatus (Morgan, 1889) em cultura de seringueira (Hevea brasiliensis Muell. Arg.) no município de Olímpia, estado de São Paulo. O Biológico 1988; 54(1-6): 27-28.
  • Coelho LM Jr, Rezende JLP, Borges LAC, Oliveira AD. Análise temporal da borracha natural brasileira. Cerne 2009; 15(1): 19-26.
  • Culik MP, Martins DS, Ventura JA, Wolff VS. Diaspididae (Hemiptera: Coccoidea) of Espírito Santo, Brazil. Journal of Insect Science 2008; 8(1): 1-6. 10.1673/031.008.1701
    » https://doi.org/10.1673/031.008.1701
  • Daud RD, Feres RJF. Community structure of mites (Arachnida: Acari) in six rubber tree clones. International Journal of Acarology 2013; 39(8): 589-596. 10.1080/01647954.2013.856470
    » https://doi.org/10.1080/01647954.2013.856470
  • Daud RD, Feres RJF, Hernandes FA. Seasonal suitability of three rubber tree clones to Calacarus heveae (Acari, Eriophyidae). Experimental and Applied Acarology 2012; 56(1): 57-68. 10.1007/s10493-011-9494-9
    » https://doi.org/10.1007/s10493-011-9494-9
  • Demite PR, Feres RJ. Influência de vegetação vizinha na distribuição de ácaros em seringal (Hevea brasiliensis Muell. Arg., Euphorbiaceae) em São José do Rio Preto, SP. Neotropical Entomology 2005; 34(5): 829-836. 10.1590/S1519-566X2005000500016
    » https://doi.org/10.1590/S1519-566X2005000500016
  • Ferla NJ, Moraes GJ. Flutuação populacional e sintomas de dano por ácaros (Acari) em seringueira no estado do Mato Grosso, Brasil. Revista Árvore 2008; 32(2): 365-376. 10.1590/S0100-67622008000200019
    » https://doi.org/10.1590/S0100-67622008000200019
  • Ferraz LF. Infestação de cochonilha-pardinha em sansão-do-campo usado como cerca viva em pomares de laranja. Bragantia 1997; 56(2): 289-290. 10.1590/S0006-87051997000200008
    » https://doi.org/10.1590/S0006-87051997000200008
  • García MM, Denno BD, Miller DR, Miller GL, Ben-Dov Y, Hardy NB. ScaleNet: a literature-based model of scale insect biology and systematics. Oxford: Database; 2016. 10.1093/database/bav118
    » https://doi.org/10.1093/database/bav118
  • Gonçalves PS, Martins ALM, Furtado EL, Sambugaro R, Ottati EL, Ortolani AA et al. Desempenho de clones de seringueira da série IAC 300 na região do planalto de São Paulo. Pesquisa Agropecuária Brasileira 2002; 37(2): 131-138. 10.1590/S0100-204X2002000200003
    » https://doi.org/10.1590/S0100-204X2002000200003
  • Henderson RC. Diaspididae (Insecta: Hemiptera: Coccoidea). Lincoln: Manaaki Whenus Press; 2011. (Fauna of New Zealand, n. 66).
  • Hernandes FA, Feres RJ. Diversidade e sazonalidade de ácaros (Acari) em seringal (Hevea brasiliensis Muell. Arg.) no noroeste do estado de São Paulo. Neotropical Entomology 2006; 35(4): 523-535. 10.1590/S1519-566X2006000400016
    » https://doi.org/10.1590/S1519-566X2006000400016
  • Hodgson CJ, Lagowska B. New scale insect (Hemiptera: Sternorrhyncha: Coccoidea) records from Fiji: three new species, records of several new invasive species and an updated checklist of Coccoidea. Zootaxa 2011; 2766(1): 1-29. 10.11646/zootaxa.2766.1.1
    » https://doi.org/10.11646/zootaxa.2766.1.1
  • Martins DS, Culik MP, Wolff VRS. New record of scale insects (Hemiptera: Coccoidea) as pests of papaya in Brazil. Neotropical Entomology 2004; 33(5): 655-657. 10.1590/S1519-566X2004000500018
    » https://doi.org/10.1590/S1519-566X2004000500018
  • Martins GLM, Vieira MR, Barbosa JC, Dini TA, Manzano AM, Alves BMS et al. Distribuição espacial de Calacarus heveae Feres na cultura da seringueira em Marinópolis-São Paulo. Revista Árvore 2012; 36(2): 211-217. 10.1590/S0100-67622012000200002
    » https://doi.org/10.1590/S0100-67622012000200002
  • Miller DR, Miller GL, Hodges GS, Davidson JA. Introduced scale insects (Hemiptera: Coccoidea) of the United States and their impact on U.S. agriculture. Proceedings of the Entomological Society of Washington 2005; 107: 123-158.
  • Normark BB, Morse GE, Krewinski A, Okusu A. Armored scale insects (Hemiptera: Diaspididae) of San Lorenzo National Park, Panama, with descriptions of two new species. Annals of the Entomological Society of America 2014; 107(1): 37-49. 10.1603/AN13110
    » https://doi.org/10.1603/AN13110
  • Perruso JC, Cassino PCR. Flutuação populacional de Selenaspidus articulatus (Morgan) (Hemiptera: Diaspididae) em Citrus sinensis (L.) no estado do Rio de Janeiro. Anais da Sociedade Entomológica do Brasil 1993; 22: 401-404.
  • Rodrigues WC, Cassino PCR, Silva Filho R. Ocorrência e distribuição de coccinelídeos (Coleoptera, Coccinellidae) associados às plantas cítricas no estado do Rio de Janeiro. EntomoBrasilis 2008; 1(2): 23-27.
  • Rodrigues WC, Cassino PCR, Spolidoro MV, Silva Filho R. Insetos sugadores (Sternorrhyncha) em cultivo orgânico de tangerina cv. poncã (Citrus reticulata Blanco): diversidade, constância, freqüência e flutuação populacional. EntomoBrasilis 2009; 2(2): 42-48.
  • Santos GP, Pereira JMM. Insetos e ácaros associados à cultura da seringueira. In: Alvarenga AP, Carmo CAFS. Seringueira. Viçosa: EPAMIG; 2008. p. 535-597.
  • Santos RS, Costa VA, Silva JM, Freitas S. Population dynamics of Leptopharsa heveae (Hemiptera: Tingidae) and Erythmelus tingitiphagus (Hymenoptera: Mymaridae) in rubber tree plants. Revista Colombiana de Entomología 2012; 38(2): 214-319.
  • Santos RS, Freitas S. Erythmelus tingitiphagus (Hymenoptera: Mymaridae): um agente promissor no controle biológico do percevejo-de-renda (Hemiptera: Tingidae) da seringueira. Agrotrópica 2008; 20: 25-28.
  • Souza GCD, Redaelli LR, Wolff VRDS. Population dynamics of Saissetia oleae (Hemiptera: Coccidae) on olive trees. Revista Brasileira de Fruticultura 2015; 37(4): 852-858. 10.1590/0100-2945-213/14
    » https://doi.org/10.1590/0100-2945-213/14
  • Vargas AS, Duarte MN, Santos MRG, Moura LC, Cassino PCR. Dinâmica populacional de insetos-praga em um cultivo agroecológico de lima ácida Tahiti (Citrus latifolia Tanaka) no município de Vassouras-RJ. Revista Eletrônica Teccen 2015; 8(2): 81-84. 10.21727/teccen.v8i2.519
    » https://doi.org/10.21727/teccen.v8i2.519
  • Vieira MR, Silva HAS, Cardoso MM, Figueira JC. Progênies de seringueira com potencial para conferir resistência a ácaros (Calacarus heveae Feres e Tenuipalpus heveae Baker). Ciência Rural 2009; 39(7): 1953-1959. 10.1590/S0103-84782009005000164
    » https://doi.org/10.1590/S0103-84782009005000164
  • Vis RM, Moraes GJD, Bellini MR. Mites (Acari) of rubber trees (Hevea brasiliensis Muell. Arg., Euphorbiaceae) in Piracicaba, state of São Paulo, Brazil. Neotropical Entomology 2006; 35(1): 112-120. 10.1590/S1519-566X200600010001
    » https://doi.org/10.1590/S1519-566X200600010001
  • Financial support This paper was financed by Fundação de Amparo à Pesquisa do Estado de Goiás (FAPEG), rescript n. 05/2012.

Edited by

Associate editor: Natália Corniani 0000-0001-7342-5171

Publication Dates

  • Publication in this collection
    27 Mar 2020
  • Date of issue
    2020

History

  • Received
    03 July 2017
  • Accepted
    08 Aug 2018
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