Population Dynamics of Rubber Tree Mites

Joyce Martins Rezende Jaqueline Magalhães Pereira Walter Santos de Araújo Rodrigo Damasco Daud André Júnio Andrade Peres About the authors

Abstract

Calacarus heveae is considered the most common pest mite in rubber tree crops in Southeast and Midwest Brazil. We evaluated the population dynamics of mites in GT 1, PB 235, PR 255 and RRIM 600 rubber tree clones from crops in the Goiás State, Brazil. We sampled leaves between June 2013 and June 2014 in 10 trees for each rubber tree clone. Calacarus heveae and Tenuipalpus heveae populations were counted in four 1 cm2-areas distributed on each middle leaflet sampled, whereas all other mites were found on lateral leaflets. Calacarus heveae reached a population peak between March and May 2014. PR 255 and RRIM 600 sheltered the densest population of C. heveae. We sampled six predatory mite species, highlighting Euseius citrifolius. GT 1 and PB 235 had higher abundance of predatory mites. This is the first study carried out on the population dynamics of phytophagous mites associated with rubber trees in the state of Goiás.

Keywords:
pest mites; Hevea brasiliensis; plant-mite interactions; predatory mites

1. INTRODUCTION AND OBJECTIVES

Calacarus heveaeFeres, 1992Feres RJF. A new species of Calacarus Keifer (Acari,Eriophyidae, Phyllocoptinae) from Hevea brasiliensis Muell. Arg.(Euphorbiaceae) from Brazil. International Journal Acarology 1992; 18(1): 61-65. 10.1080/01647959208683930
https://doi.org/10.1080/0164795920868393...
(Acariformes: Eriophyidae), is considered the most common pest mite in rubber tree cultivations (Hevea brasiliensis Muell. Arg., Euphorbiaceae) of the Brazilian Midwest and Southeastern regions (Daud & Feres, 2007Daud RD, Feres RJF. Dinâmica populacional de ácaros fitófagos (Acari, Eriophyidae, Tenuipalpidae) em seis clones de seringueira no sul do Estado de Mato Grosso. Revista Brasileira de Entomologia 2007; 51(3): 377-381. 10.1590/S0085-56262007000300016
https://doi.org/10.1590/S0085-5626200700...
; Feres, 2000Feres RJF. Levantamento e observação naturalísticas da acarofauna (Acari, Arachnida) de seringueira cultivadas (Hevea spp., Euphorbiaceae) no Brasil. Revista Brasileira de Zoologia 2000; 17(1): 157-173. 10.1590/S0101-81752000000100011
https://doi.org/10.1590/S0101-8175200000...
; Hernandes & Feres, 2006Hernandes FA, Feres RJF. 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...
). High infestations of C. heveae can cause yellowing and tanning of the rubber tree leaflets, resulting in intense defoliation (Feres, 1992Feres RJF. A new species of Calacarus Keifer (Acari,Eriophyidae, Phyllocoptinae) from Hevea brasiliensis Muell. Arg.(Euphorbiaceae) from Brazil. International Journal Acarology 1992; 18(1): 61-65. 10.1080/01647959208683930
https://doi.org/10.1080/0164795920868393...
, 2000Feres RJF. Levantamento e observação naturalísticas da acarofauna (Acari, Arachnida) de seringueira cultivadas (Hevea spp., Euphorbiaceae) no Brasil. Revista Brasileira de Zoologia 2000; 17(1): 157-173. 10.1590/S0101-81752000000100011
https://doi.org/10.1590/S0101-8175200000...
; Vieira et al., 2013Vieira MR, Martins GLM, Scaloppi EJ Jr. Resistência de clones de seringueira à infestação por ácaros. Bragantia 2013; 72(4): 367-372. 10.1590/brag.2013.044
https://doi.org/10.1590/brag.2013.044...
). Calacarus heveae attack can reduces the foliar photosynthetic rate and affect productivity (Daud, Conforto, & Feres, 2012Daud RD, Conforto EC, Feres RJF. Changes in leaf physiology caused by Calacarus heveae (Acari, Eriophyidae) on rubber tree. Experimental and Applied Acarology 2012; 57(2): 127-137. 10.1007/s10493-012-9552-y
https://doi.org/10.1007/s10493-012-9552-...
).

The population peaks of C. heveae occur at the end of the rainy season and the beginning of the dry season, between February and May (Daud & Feres, 2007Daud RD, Feres RJF. Dinâmica populacional de ácaros fitófagos (Acari, Eriophyidae, Tenuipalpidae) em seis clones de seringueira no sul do Estado de Mato Grosso. Revista Brasileira de Entomologia 2007; 51(3): 377-381. 10.1590/S0085-56262007000300016
https://doi.org/10.1590/S0085-5626200700...
). Depending on the infestation level, this mite can cause more than 75% of leaf loss and a reduction of up to 30% in the latex production (Feres, 1992Feres RJF. A new species of Calacarus Keifer (Acari,Eriophyidae, Phyllocoptinae) from Hevea brasiliensis Muell. Arg.(Euphorbiaceae) from Brazil. International Journal Acarology 1992; 18(1): 61-65. 10.1080/01647959208683930
https://doi.org/10.1080/0164795920868393...
; Vieira & Gomes, 1999Vieira MR, Gomes EC. Sintomas, desfolhamento e controle de Calacarus heveae Feres, 1992 (Acari: Eriophyidae) em seringueira (Hevea brasiliensis Muell. Arg.). Cultura Agronômica 1999; 8(1): 53-71.), which may compromise the viability and productivity of the rubber tree (Daud, Conforto, & Feres, 2012Daud RD, Conforto EC, Feres RJF. Changes in leaf physiology caused by Calacarus heveae (Acari, Eriophyidae) on rubber tree. Experimental and Applied Acarology 2012; 57(2): 127-137. 10.1007/s10493-012-9552-y
https://doi.org/10.1007/s10493-012-9552-...
).

Due to the damage caused by C. heveae and other phytophagous arthropods to rubber tree productivity, several control strategies have been evaluated for managing these species in the field, with emphasis on chemical control (Daud, Feres, & Boscolo, 2012Daud RD, Feres RJF, Boscolo M. Efeito inseticida de ésteres de sacarose sobre Calacarus heveae Feres (Acari: Eriophyidae) em dois clones de seringueira. BioAssay 2012; 7(2): 1-6.; Ferla & Moraes, 2003Ferla NJ, Moraes GJ. Oviposição dos ácaros predadores Agistemus floridanus Gonzalez, Euseius concordis (Chant) e Neoseiulus anonymus (Chant & Baker) (Acari) em resposta a diferentes tipos de alimento. Revista Brasileira de Zoologia 2003; 20(1): 153-155. 10.1590/S0101-81752003000100019
https://doi.org/10.1590/S0101-8175200300...
; Vieira et al., 2006Vieira MR, Gomes EC, Figueira JC. Controle químico de Calacarus heveae Feres (Acari: Eriophyidae) em seringueira. BioAssay 2006; 1(9): 1-7, 2006. 10.14295/BA.v1.0.37
https://doi.org/10.14295/BA.v1.0.37...
).

According to Daud & Feres (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...
), the rubber tree clones can affect the structure of mite communities in the crop, including the occurrence and abundance of phytophagous, mycophagous and predatory mites. According to these authors, the highest estimated amount of mite species was recorded for GT 1 and PB 235 clones, while the greatest abundance of predators and mycophagous was found in GT 1 and phytophagous in PB 235. Thus, there is evidence that different clones have different effects on the organization of mite communities in rubber tree plants.

In Brazil, interactions between rubber tree clones and mites have been studied mainly in the western regions of the state of Mato Grosso (e.g. Daud & Feres, 2007Daud RD, Feres RJF. Dinâmica populacional de ácaros fitófagos (Acari, Eriophyidae, Tenuipalpidae) em seis clones de seringueira no sul do Estado de Mato Grosso. Revista Brasileira de Entomologia 2007; 51(3): 377-381. 10.1590/S0085-56262007000300016
https://doi.org/10.1590/S0085-5626200700...
, 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...
; 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...
) and in the northwest regions of the state of São Paulo (e.g. Silva et al., 2011Silva HAS, Vieira MR, Valério WVF, Cardoso MSM, Figueira JC. Clones de seringueira com resistência a ácaros. Bragantia 2011; 70(2): 383-388. 10.1590/S0006-87052011000200019
https://doi.org/10.1590/S0006-8705201100...
), although there is lack of information for the Midwest Brazil. Thus, the objective of this research was to evaluate the population fluctuation of C. heveae and Tenuipalpus heveae Baker (Acariformes: Tenuipalpidae), and to do survey of secondary mites associated with rubber tree clones in the state of Goiás.

2. MATERIALS AND METHODS

The study was carried out in areas belonging to OL Látex Ltda., located in the city of Goianésia, Goiás, Brazil (15° 19’ 21” S and 49° 9’ 32” W). The rubber clones evaluated were GT 1, PB 235, PR 255 and RRIM 600. The area is in the morphological and climatic domain of the Cerrado, with fragments of natural vegetation of this biome, such as forests and savannahs being found in the surroundings. The climate of the region is Aw according to the Köppen classification, characterized by a well-defined dry season between April and September, and a rainy period between October and March (Alvares et al., 2013Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek G. Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift 2013; 22(6): 711-728. 10.1127/0941-2948/2013/0507
https://doi.org/10.1127/0941-2948/2013/0...
). Spraying with insecticides and acaricides were not performed in the evaluated area during the study period.

Bi-weekly sampling for evaluating C. heveae and T. heveae and monthly sampling for evaluating other species were also carried out between June 2013 and June 2014. These were made randomly in ten plants of each clone. Seven leaves were collected around the canopy for each selected plant at a height of 7 m with the aid of a trimmer with telescope cable. The collected leaves were conditioned in individualized, properly labeled paper bags, which were wrapped in plastic bags and transported to the laboratory in isothermal polystyrene boxes refrigerated with plastic bags containing Gelo X®. The samples were kept under refrigeration at 10 °C for a maximum of one week.

In the laboratory, the central leaflet and a lateral leaflet of each leaf were analyzed under a stereoscopic microscope. The central leaflets were used to evaluate C. heveae and T. heveae, which were assessed biweekly. For these species, four 1 cm² areas were randomly arranged in the leaf limb of the adaxial face for C. heveae and the abaxial face for T. heveae of each central leaflet. The lateral leaflets of each collected leaf were used to evaluate the occurrence and abundance of the other species monthly, called here as “secondary mites.” One of the lateral leaflets of each leaf was thoroughly inspected on the adaxial and abaxial surfaces, and all secondary mites found were put on microscopy slides using Hoyer’s medium (Moraes & Flechtmann, 2008Moraes GJ, Flechtmann CHW. Manual de acarologia: acarologia básica e ácaros de plantas cultivadas no Brasil. Ribeirão Preto: Holos; 2008.). The specimens were identified under optical microscope with phase contrast.

Total population counts and population density were calculated in order to obtain the population fluctuation of C. heveae and T. heveae. The clones were compared using the 95% confidence interval, considering the population peak between March and May 2014. The density was compared by graphical analysis to verify the overlap of the error bars (Cumming et al., 2007Cumming G, Fidler F, Vaux DL. Error bars in experimental biology. The Journal of Cell Biology 2007; 177(1): 7-11. 10.1083/jcb.200611141
https://doi.org/10.1083/jcb.200611141...
).

3. RESULTS AND DISCUSSION

In total, 100,807 C. heveae individuals and only 219 T. heveae individuals were counted. During the natural senescence of the leaves, which corresponds to the dry season (July-August), C. heveae population showed a decrease in the four clones (Figure 1). The density of this mite gradually increased after the leaves sprouted (September-October), reaching a population peak between March and May 2014 (the end of the rainy season and the beginning of the dry season).

Figure 1
Population fluctuation of C. heveae in rubber tree clones, from June 2013 to June 2014, Goianésia, Goiás, Brazil.

The density of C. heveae varied among the evaluated clones. PR 255 sheltered a higher mean density of the mite during the period with major infestations (March to May 2014), similar to the RRIM 600 clone. The lower densities of C. heveae were found in the GT 1 and PB 235 clones (Figure 2).

Figure 2
Mean density of C. heveae (± IC 95%) in rubber tree clones, Goianésia, Goiás, Brazil.

Our results corroborate previous studies that indicated C. heveae as the most abundant phytophagous mite in rubber tree crops (Feres, 2000Feres RJF. Levantamento e observação naturalísticas da acarofauna (Acari, Arachnida) de seringueira cultivadas (Hevea spp., Euphorbiaceae) no Brasil. Revista Brasileira de Zoologia 2000; 17(1): 157-173. 10.1590/S0101-81752000000100011
https://doi.org/10.1590/S0101-8175200000...
; Feres et al., 2002Feres RJF, Rossa-Feres DC, Daud RD, Santos RS. Diversidade de ácaros (Acari, Arachnida) em seringueiras (Hevea brasiliensis Muell. Arg., Euphorbiaceae) na região noroeste do Estado de São Paulo, Brasil. Revista Brasileira de Zoologia 2002; 19(1): 137-144. 10.1590/S0101-81752002000100011
https://doi.org/10.1590/S0101-8175200200...
; Hernandes & Feres, 2006Hernandes FA, Feres RJF. 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...
). This species occurred in all clones during the study period, with population peaks between March and May. This pattern has also been observed in previous studies that recorded high C. heveae infestations at the end of the rainy season and beginning of the dry season (Daud & Feres, 2007Daud RD, Feres RJF. Dinâmica populacional de ácaros fitófagos (Acari, Eriophyidae, Tenuipalpidae) em seis clones de seringueira no sul do Estado de Mato Grosso. Revista Brasileira de Entomologia 2007; 51(3): 377-381. 10.1590/S0085-56262007000300016
https://doi.org/10.1590/S0085-5626200700...
; Hernandes & Feres, 2006Hernandes FA, Feres RJF. 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...
; 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...
).

The population dynamics of C. heveae throughout the year is probably associated with the rubber tree phenology. The low densities of the mite during the senescence period can be evidenced by the population resurgence soon after regrowth of the plants leaves, when these are still young, and gradual increase of the population along the plant development and foliar maturation (Daud & Feres, 2007Daud RD, Feres RJF. Dinâmica populacional de ácaros fitófagos (Acari, Eriophyidae, Tenuipalpidae) em seis clones de seringueira no sul do Estado de Mato Grosso. Revista Brasileira de Entomologia 2007; 51(3): 377-381. 10.1590/S0085-56262007000300016
https://doi.org/10.1590/S0085-5626200700...
). The period in which the leaves are more favorable for phytophagous mites development is between January to April (Daud, Feres, & Hernandes, 2012Daud RD, Feres RJF, Hernandes FA. Seasonal suitability of three rubber tree clones to Calaracus heveae (Acari, Eriophyidae). Experimental and Applied Acarology 2012; 56: 57-68. 10.1007/s10493-011-9494-9
https://doi.org/10.1007/s10493-011-9494-...
), coinciding with the C. heveae abundance peak, as observed here and by other authors (Daud & Feres, 2007Daud RD, Feres RJF. Dinâmica populacional de ácaros fitófagos (Acari, Eriophyidae, Tenuipalpidae) em seis clones de seringueira no sul do Estado de Mato Grosso. Revista Brasileira de Entomologia 2007; 51(3): 377-381. 10.1590/S0085-56262007000300016
https://doi.org/10.1590/S0085-5626200700...
; Feres et al., 2002Feres RJF, Rossa-Feres DC, Daud RD, Santos RS. Diversidade de ácaros (Acari, Arachnida) em seringueiras (Hevea brasiliensis Muell. Arg., Euphorbiaceae) na região noroeste do Estado de São Paulo, Brasil. Revista Brasileira de Zoologia 2002; 19(1): 137-144. 10.1590/S0101-81752002000100011
https://doi.org/10.1590/S0101-8175200200...
; Hernandes & Feres, 2006Hernandes FA, Feres RJF. 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...
; 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...
). This pattern of increased density of phytophagous mites with the emission of new leaves and peak population at the end of the rainy season were observed for all evaluated clones.

According to Daud, Feres, & Hernandes (2012Daud RD, Feres RJF, Hernandes FA. Seasonal suitability of three rubber tree clones to Calaracus heveae (Acari, Eriophyidae). Experimental and Applied Acarology 2012; 56: 57-68. 10.1007/s10493-011-9494-9
https://doi.org/10.1007/s10493-011-9494-...
), the leaf age and rubber tree clone influence the development, oviposition and survival of C. heveae. These authors observed under controlled conditions less survival and longer development time when C. heveae individuals were kept in young GT 1 leaves withdrawn from plants in November. However, there was a reduction in the development period, a high reproductive rate, and higher survival of mites were recorded when they were kept in on leaflets removed from plants between January and April. The mites kept in leaves removed from the plants between May and June presented reduced oviposition rates (Daud, Feres, & Hernandes, 2012Daud RD, Feres RJF, Hernandes FA. Seasonal suitability of three rubber tree clones to Calaracus heveae (Acari, Eriophyidae). Experimental and Applied Acarology 2012; 56: 57-68. 10.1007/s10493-011-9494-9
https://doi.org/10.1007/s10493-011-9494-...
). In the current study, we observed decreases in C. heveae populations starting from May, before the natural senescence of the plants, suggesting that leaves with more advanced age are not suitable for mite development. Therefore, the rubber tree phenology can determine the population dynamics of C. heveae.

Daud & Feres (2007Daud RD, Feres RJF. Dinâmica populacional de ácaros fitófagos (Acari, Eriophyidae, Tenuipalpidae) em seis clones de seringueira no sul do Estado de Mato Grosso. Revista Brasileira de Entomologia 2007; 51(3): 377-381. 10.1590/S0085-56262007000300016
https://doi.org/10.1590/S0085-5626200700...
) also found differences in relation to the infestation level of C. heveae among rubber trees clones in a plantation at Itiquira municipality, State of Mato Grosso. The authors observed the largest C. heveae infestations in PR 255 clones. RRIM 600 clone plants showed higher C. heveae density when compared to PB 235, which showed the lowest C. heveae densities (Daud & Feres, 2007Daud RD, Feres RJF. Dinâmica populacional de ácaros fitófagos (Acari, Eriophyidae, Tenuipalpidae) em seis clones de seringueira no sul do Estado de Mato Grosso. Revista Brasileira de Entomologia 2007; 51(3): 377-381. 10.1590/S0085-56262007000300016
https://doi.org/10.1590/S0085-5626200700...
). High density of this mite in PB 235 and low density in GT 1 clones were registered in Jaboticabal, São Paulo (Tanzini, 1999Tanzini MR. Manejo integrado do percevejo-de-renda da seringueira e ácaros na Hevea. In: I Ciclo de palestras sobre heveicultura paulista; 1999; Barretos. Barretos: Associação Paulista de Produtores e Beneficiadores de Borracha; 1999. p. 31-44.). Here, we observed higher C. heveae infestation in PR 255 and RRIM 600, and lowest mite abundance in PB 235 and GT 1, similarly to the results found by Daud & Feres (2007)Daud RD, Feres RJF. Dinâmica populacional de ácaros fitófagos (Acari, Eriophyidae, Tenuipalpidae) em seis clones de seringueira no sul do Estado de Mato Grosso. Revista Brasileira de Entomologia 2007; 51(3): 377-381. 10.1590/S0085-56262007000300016
https://doi.org/10.1590/S0085-5626200700...
.

In the present study, T. heveae is classified as a secondary species, since low abundance was observed during the sampling period. Competition with C. heveae may have influenced their population growth, as suggested by Feres et al. (2002Feres RJF, Rossa-Feres DC, Daud RD, Santos RS. Diversidade de ácaros (Acari, Arachnida) em seringueiras (Hevea brasiliensis Muell. Arg., Euphorbiaceae) na região noroeste do Estado de São Paulo, Brasil. Revista Brasileira de Zoologia 2002; 19(1): 137-144. 10.1590/S0101-81752002000100011
https://doi.org/10.1590/S0101-8175200200...
). In addition, T. heveae is a well-accepted prey by Euseius citrifolius Denmark & Muma (Parasitiformes, Phytoseiidae), preferentially in their larval and nymphal stages (Cardoso et al. 2010Cardoso MS, Vieira MR, Figueira JC, Silva HAS. Atividade predatória de Euseius citrifolius Denmark & Muma (Acari: Phytoseiidae) sobre Tenuipalpus heveae Baker (Acari: Tenuipalpidae). Arquivos do Instituto Biológico 2010; 77(3): 471-476.). In the our study, we recorded E. citrifolius as the highest abundant predatory mite in all rubber tree clones evaluated, suggesting a possible control on the T. heveae populations by this species.

For secondary mites, 902 individuals belonging to 18 species of 10 families (Table 1) were registered. Among these, 523 individuals belonging to eight phytophagous species from three families; 92 individuals of three mycophagous species in two families; 256 specimens of six predatory species in four families, and only one family of mites with unknown food habits with 22 individuals of a single species.

Table 1
Mites collected in a rubber tree plantation separated by family, genus/species and food habit. Goianésia, Goiás, Brazil.

Phytophagous mites represented 58% of the specimens collected, followed by predators with 29.4%, mycophagous with 10.2%, and unknown food habit in 2.4%. The family with the highest diversity was Tetranychidae with five species sampled, namely Eutetranychus sp., Eutetranychus banksi (McGregor), Oligonychus gossypii (Zacher), Oligonychus ilicis (McGregor) and Oligonychus sp. The other families had one to two species. The family with the highest abundance was also Tetranychidae, followed by the Phytoseiidae and Winterschmidtiidae. Euseius citrifolius was the only species registered in the Phytoseiidae. Winterschmidtiidae showed two species identified up to genus level, Oulenzia sp. and Czenspinskia sp.

RRIM 600 presented a lower number of secondary mites in the study, mainly due to the smaller number of Tetranychidae mites and predatory species. A higher abundance of secondary mites was observed for PB 235, followed by GT 1 and PR 255. In relation to the abundance of predatory mites, PB 235 and PR 255 clones had similar results, whereas they were slightly higher in GT 1. Furthermore, all clones presented similar numbers for species variety, with GT 1 presenting 13 species, PR 255 with 11, PB 235 and RRIM 600 with nine species each.

The greater abundance of phytophagous species determines the community structure, influencing the occurrence and abundance of other mites species (Daud & Feres, 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...
). In a study carried out in the state of Mato Grosso by Demite & Feres (2007Demite PR, Feres RJF. Ocorrência e flutuação populacional de ácaros associados a seringais vizinhos de fragmentos de cerrado. Neotropical Entomology 2007; 36(1): 117-127. 10.1590/S1519-566X2007000100015
https://doi.org/10.1590/S1519-566X200700...
), phytophagous represented 98.7% of the total number of individuals collected, while predators represented 1%. Among these, three phytophagous species considered primary mites represented more than 97%, namely Phyllocoptruta seringueirae Feres, T. heveae and C. heveae (Demite & Feres, 2007Demite PR, Feres RJF. Ocorrência e flutuação populacional de ácaros associados a seringais vizinhos de fragmentos de cerrado. Neotropical Entomology 2007; 36(1): 117-127. 10.1590/S1519-566X2007000100015
https://doi.org/10.1590/S1519-566X200700...
). Here we observed a similar abundance pattern since phytophagous mites were the most abundant followed by predatory mites.

Bdellidae, Iolinidae, Phytoseiidae and Stigmaeidae have some important predatory species of phytophagous mites (Gerson et al., 2003Gerson U, Smiley RL, Ochoa R. Mites (Acari) for pest control. Oxford: Blackwell Sciences; 2003.). Euseius citrifolius is the most frequently reported predatory species in the Brazilian natural vegetation remnants (Araújo & Daud, 2017Araújo WS, Daud RD. Insights on plant mite occurrence in natural vegetation remnants from Brazil. Systematic and Applied Acarology 2017; 22(2): 241-261. 10.11158/saa.22.2.12
https://doi.org/10.11158/saa.22.2.12...
), and it is also found in several Brazilian rubber tree plantations (Feres, 2000Feres RJF. Levantamento e observação naturalísticas da acarofauna (Acari, Arachnida) de seringueira cultivadas (Hevea spp., Euphorbiaceae) no Brasil. Revista Brasileira de Zoologia 2000; 17(1): 157-173. 10.1590/S0101-81752000000100011
https://doi.org/10.1590/S0101-8175200000...
; Hernandes & Feres, 2006Hernandes FA, Feres RJF. 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...
). The highest abundance of E. citrifolius found in our study may be related to the presence of Tetranychidae mites. Phytoseiidae mites received more attention from the 1950s on, when these mites were considered important natural enemies of Tetranychidae mites in agroecosystems (Gerson et al., 2003Gerson U, Smiley RL, Ochoa R. Mites (Acari) for pest control. Oxford: Blackwell Sciences; 2003.; Moraes et al., 2004Moraes GJ, McMurtry JA, Denmark HA, Campos CB. A revised catalog of the mite family Phtoseiidae. Zootaxa 2004; 434(1): 1-494. 10.11646/zootaxa.434.1.1
https://doi.org/10.11646/zootaxa.434.1.1...
). Moreover, due to predatory habits, E. citrifolius can contribute to the biological control of the most important pest species (Cardoso et al., 2010Cardoso MS, Vieira MR, Figueira JC, Silva HAS. Atividade predatória de Euseius citrifolius Denmark & Muma (Acari: Phytoseiidae) sobre Tenuipalpus heveae Baker (Acari: Tenuipalpidae). Arquivos do Instituto Biológico 2010; 77(3): 471-476.) and can feed on several mite groups, thrips and whiteflies (McMurtry et al., 2013McMurtry JA, Moraes GJ, Sourassou N. Revision of the lifestyles of phytoseiid mites (Acari: Phytoseiid) and implications for biological control strategies. Systematic & Applied Acarology 2013; 18(4): 297-320. 10.11158/saa.18.4.1
https://doi.org/10.11158/saa.18.4.1...
). The great abundance and frequency of this mite throughout the year is probably due to its general food habit, with high food diversity including phytophagous mites, insects and pollen (Bellini et al., 2008Bellini MR, Feres RJF, Buosi R. Ácaros (Acari) de seringueira (Hevea brasiliensis Muell. Arg., Euphorbiaceae) e de euforbiáceas espontâneas no interior dos cultivos. Neotropical Entomology 2008; 37(4): 463-471. 10.1590/S1519-566X2008000400016
https://doi.org/10.1590/S1519-566X200800...
).

In addition to E. citrifolius, we also sampled Agistemus floridanus Gonzalez (Acariformes: Stigmaeidae), Tetrabdella neotropica Hernandes & Feres (Acariformes, Bdellidae), and two species belonging to Iolinidae. Agistemus floridanus had potential in controlling C. heveae in the field, since the females have relatively high oviposition when fed with this phytophagous species under experimental conditions (Ferla & Moraes, 2003Ferla NJ, Moraes GJ. Oviposição dos ácaros predadores Agistemus floridanus Gonzalez, Euseius concordis (Chant) e Neoseiulus anonymus (Chant & Baker) (Acari) em resposta a diferentes tipos de alimento. Revista Brasileira de Zoologia 2003; 20(1): 153-155. 10.1590/S0101-81752003000100019
https://doi.org/10.1590/S0101-8175200300...
). Moreover, Iolinidae mites are recognized worldwide as important natural enemies of Eriophyidae (Gerson et al., 2003Gerson U, Smiley RL, Ochoa R. Mites (Acari) for pest control. Oxford: Blackwell Sciences; 2003.).

Daud & Feres (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...
) suggested a possible effect of clone type on the abundance of phytophagous species in rubber trees, which in turn affect competing species and predatory mites occurrence. The greater abundance of secondary mites presented in the PB 235 clone in the present study was possibly due to higher abundance of Tetranychidae mites. Thus, host plants play a determining role in the mite community organization on rubber trees.

Host plants influences on acarofauna composition may be related to resistance factors. Some papers reported the influence of rubber tree clone on the development of phytophagous mites (Daud, Feres, & Hernandes, 2012Daud RD, Feres RJF, Hernandes FA. Seasonal suitability of three rubber tree clones to Calaracus heveae (Acari, Eriophyidae). Experimental and Applied Acarology 2012; 56: 57-68. 10.1007/s10493-011-9494-9
https://doi.org/10.1007/s10493-011-9494-...
; Feres et al., 2010Feres RJF, Del’Arco M, Daud RD. Biological cycle of Tenuipalpus heveae Baker (Acari, Tenuipalpidae) on leaflets of three rubber tree clones. Revista Brasileia de Entomologia 2010; 54(2): 298-303. 10.1590/S0085-56262010000200013
https://doi.org/10.1590/S0085-5626201000...
), but more studies are needed to identify biochemical characteristics of the rubber tree clones in relation to resistance against phytophagous mites, as well as the effect of plant physiology on the development of mites (Daud, Feres, & Hernandes, 2012Daud RD, Feres RJF, Hernandes FA. Seasonal suitability of three rubber tree clones to Calaracus heveae (Acari, Eriophyidae). Experimental and Applied Acarology 2012; 56: 57-68. 10.1007/s10493-011-9494-9
https://doi.org/10.1007/s10493-011-9494-...
; Vieira et al., 2013Vieira MR, Martins GLM, Scaloppi EJ Jr. Resistência de clones de seringueira à infestação por ácaros. Bragantia 2013; 72(4): 367-372. 10.1590/brag.2013.044
https://doi.org/10.1590/brag.2013.044...
).

4. CONCLUSIONS

The population peak of C. heveae occurs between March and May in the state of Goiás. Clones differ for the C. heveae population and also for other associated mites. PR 255 and RRIM 600 clones have higher C. heveae infestations. In relation to predatory mites, GT 1 and PB 235 harbored the highest abundance of these organisms.

ACKNOWLEDGEMENTS

Thanks to OL Látex Ltda. for allowing the research in their propriety and for the technical support in the field. To the Acarology Lab team headed by Dr. Reinaldo J. F. Feres (UNESP, São José do Rio Preto) for confirming and identifying the mites species.

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  • FINANCIAL SUPPORT

    Fundação de Amparo à Pesquisa do Estado de Goiás (FAPEG), public notice No. 05/2012, with a scholarship granted to the first author of this article (Grant/Award Number: 201310267000253).

Publication Dates

  • Publication in this collection
    06 July 2020
  • Date of issue
    2020

History

  • Received
    06 Apr 2018
  • Accepted
    27 Nov 2018
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