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Diversity of mites in blackberry genotypes in Pelotas, Rio Grande do Sul, Brazil

Diversidade de ácaros em genótipos de amoreira-preta em Pelotas, Rio Grande do Sul

ABSTRACT:

Blackberry is part of the small-fruit group and the blackberry cultivation area is expanding as an important option for small farmers using the agroecological production system. Mites are prominent among the world’s major crop pests, as they can affect plants from growth to fruiting. The objective of this study was to evaluate the occurrence of phytophagous and predatory mites in different blackberry genotypes in the municipality of Pelotas, RS, Brazil. This study was carried out in the period Nov. 2015 - Oct. 2016, totaling 14 samples. A total of 11,158 mites were collected [phytophagous (5940) and predatory (323) mites, and those with varied feeding habits (4895)], which were distributed in 8 families. The species Neotetranychus asper (Feres & Flechtmann, 2000), Diptacus rubuscolum (Trinidad, Duarte & Navia, 2018), and Acalitus orthomerus (Keifer, 1951) had highest occurrence. According to the faunistic classification, the N. asper phytophagous species is predominant in genotypes 128 and 178; whereas, D. rubuscolum is predominant in genotype 132. Monitoring of these genotypes is recommended to detect possible damage to the crop.

Key words:
Rubus spp.; faunistic analysis; phytophagous; predators.

RESUMO:

A amoreira-preta faz parte do grupo das pequenas frutas e sua área de cultivo está em plena expansão, sendo uma opção importante para os pequenos agricultores que usam o sistema de produção agroecológico. Os ácaros destacam-se dentre as principais pragas da cultura em nível mundial, pois eles podem comprometer desde o crescimento das plantas até sua frutificação. O objetivo desta pesquisa foi estudar a ocorrência de ácaros fitófagos e predadores em diferentes genótipos de amoreira preta no município de Pelotas, RS, Brasil. Este estudo foi realizado no período novembro de 2015 a outubro de 2016, totalizando 14 amostragens. Um total de 11.158 ácaros coletou-se (5.940 ácaros fitófagos, 323 ácaros predadores, e 4.895 ácaros de alimentação variada), que estavam distribuídos em oito famílias. As espécies Neotetranychus asper (Feres & Flechtmann, 2000), Diptacus rubuscolum (Trinidad, Duarte & Navia, 2018), e Acalitus orthomerus (Keifer, 1951) tiveram maior ocorrência. De acordo com a classificação faunística, a espécie fitófaga N. asper é predominante nos genótipos 128 e 178, enquanto a espécie D. rubuscolum é predominante no genótipo 132. Monitorar esses genótipos é recomendado para detectar possíveis danos à cultura.

Palavras-chave:
Rubus spp.; diversidade; fitófagos; predador.

INTRODUCTION:

Cultivation of the blackberry tree (Rubus spp., Rosaceae) is expanding in Brazil, and it has been used in an agroecological production system (ANTUNES et al., 2010ANTUNES, L. E. C. et al. Fenologia e produção de cultivares de amoreira-preta em sistema agroecológico. Ciência Rural, Santa Maria, v.40, n.9, p.1929-1933, 2010. Available from: <Available from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S0103-84782010000900012 >. Accessed: Jun. 21, 2017. doi: 10.1590/S0103-84782010000900012.
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) due to its great adaptability, low installation cost, and management. In Brazil, its cultivation began in the 1970s, with development in the breeding program (RASEIRA & FRANZON, 2012RASEIRA, M. C. B.; FRANZON, R. C. Melhoramento genético e cultivares de amora-preta e mirtilo. Informe Agropecuário, Belo Horizonte, v.33, n.268, p.11-20, 2012.). The cultivars currently used in Brazil are the result of crosses of the native and North-American genetic material (ANTUNES et al., 2014ANTUNES, L. E. C. et al. Blackberry production in Brazil. Revista Brasileira de Fruticultura, Jaboticabal, v.36, n.1, p.100-111, 2014. Available from: <Available from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S0100-29452014000100012 >. Accessed: Jun. 22, 2017. doi: 10.1590/0100-2945-450/13.
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).

Blackberry is subject to a considerable number of pests, such as with other crops, and they can affect the blackberry tree by affecting its production (PAGOT et al., 2007PAGOT, E.; et al. Cultivo da amora-preta. Bento Gonçalves: Embrapa Uva e Vinhos, 2007. 11p. (Circular Técnica, 75).). Currently, pest management in Brazil is restricted and based only on working knowledge, since research-generated information is lacking (NAVA et al., 2007NAVA, D. E.; et al. 2007. Agência Embrapa de Informação Tecnológica. Available from: <Available from: http://www.agencia.cnptia.embrapa.br/gestor/amora/arvore/CONT000ggtku91902wx5ok05vadr139ze3lr.html >. Accessed: Apr. 13, 2017.
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). Blackberry weevil (Eulechriops rubi) and fruit fly (Anastrephaspp.) were cited as the main pests in Brazil (NAVA et al., 2007NAVA, D. E.; et al. 2007. Agência Embrapa de Informação Tecnológica. Available from: <Available from: http://www.agencia.cnptia.embrapa.br/gestor/amora/arvore/CONT000ggtku91902wx5ok05vadr139ze3lr.html >. Accessed: Apr. 13, 2017.
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; ANTUNES et al., 2014ANTUNES, L. E. C. et al. Blackberry production in Brazil. Revista Brasileira de Fruticultura, Jaboticabal, v.36, n.1, p.100-111, 2014. Available from: <Available from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S0100-29452014000100012 >. Accessed: Jun. 22, 2017. doi: 10.1590/0100-2945-450/13.
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). In addition, the presence of mites has already been reported in Brazil, specifically in Rio Grande do Sul State (MARCHETTI & FERLA, 2011MARCHETTI, M; FERLA, N. J. Diversidade e flutuação populacional de ácaros (Acari) em amora-preta (Rubus fruticosus, Rosaceae) no estado do Rio Grande do Sul, Brasil. Iheringa, Porto Alegre, v.101, n.1-2, p.43- 48. 2011. Available from: <Available from: http://www.scielo.br/pdf/isz/v101n1-2/v101n1-2a05.pdf >. Accessed: Jun. 22, 2017.
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). However, specific studies are necessary to obtain information about the predominant mite species, their potential for harm, and how they could become a threat to commercial systems for blackberry production, as it has occurred with Acalitus essigi Hassan, 1928 (KEIFER et al., 1982KEIFER, H. H. et al. An illustrated guide to plant abnormalities caused by eriophyid mites in North America. United States Department of Agriculture. Agriculture handbook, n.573, p.177, 1982.; BAKER et al., 1996BAKER, E.W. et al. Eriophyoid mites of the United States. Michigan : Indira Publishing House, 1996. 394p.; DAVIES et al., 2001aDAVIES, J. T. et al. Dispersal of Acalitus essigi to blackberry (Rubus fruticosus agg.)frui. Entomologia Experimentalis et Applicata, v.101, p.19-23, 2001a. Available from: <Available from: http://onlinelibrary.wiley.com/doi/10.1046/j.1570-7458.2001.00886.x/full >. Accessed: Jul. 16, 2017. doi: 10.1046/j.1570-7458.2001.00886.x.
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, PINA et al., 2012PINA, S. et al. Os ácaros na cultura da amora em estufa e infestantes. IV Colóquio Nacional da Produção de Pequenos Frutos, Actas Portuguesas de Horticultura. Odemira, n.20, p.69-76, 2012.) or Acalitus orthomerus (Keifer, 1951) (BAKER et al., 1996BAKER, E.W. et al. Eriophyoid mites of the United States. Michigan : Indira Publishing House, 1996. 394p.) in other countries.

Species of phytoseiids, eriophids, tarsonemids, tetranychids, and thideids were reported in association with blackberry cultivars (MARCHETTI & FERLA, 2011MARCHETTI, M; FERLA, N. J. Diversidade e flutuação populacional de ácaros (Acari) em amora-preta (Rubus fruticosus, Rosaceae) no estado do Rio Grande do Sul, Brasil. Iheringa, Porto Alegre, v.101, n.1-2, p.43- 48. 2011. Available from: <Available from: http://www.scielo.br/pdf/isz/v101n1-2/v101n1-2a05.pdf >. Accessed: Jun. 22, 2017.
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; MCMURTRY & SHOW, 2012MCMURTRY, J. A.; SHOW, E. D. Phytoseiidae on blackberry in Central California. Systematic & Applied Acarology, Londres, v.17, n.4, p.384-387, 2012. Available from: <Available from: http://www.bioone.org/doi/abs/10.11158/saa.17.4.6 >. Accessed: Jun. 21, 2017. doi: 10.11158/saa.17.4.6>.
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). According to MCMURTRY & SHOW (2012)MCMURTRY, J. A.; SHOW, E. D. Phytoseiidae on blackberry in Central California. Systematic & Applied Acarology, Londres, v.17, n.4, p.384-387, 2012. Available from: <Available from: http://www.bioone.org/doi/abs/10.11158/saa.17.4.6 >. Accessed: Jun. 21, 2017. doi: 10.11158/saa.17.4.6>.
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, a low diversity of phytoseiid mites has been observed in commercial blackberry trees, and this may be related to intensive cultivation practices, such as lack of plant diversity, alternative foods, and adverse effects of spraying with pesticides. However, six species of mites of the family Phytoseiidae reported in blackberry trees were reported in Portugal as follows: [Neoseiulus californicus (McGregor, 1954), Amblyseius graminis Chant, 1956, Euseius stipulatus (Athias-Henriot, 1960), Neoseiulella perforata (Athias-Henriot, 1960), and Typhlodromus (Anthoseius) recki Wainstein, 1958], and a species of the family Stigmaeidae. The stigmaeid Agistemus longisetus Gonzalez, 1963 and phytoseiid E. stipulatus and N. californicus (PINA et al., 2012PINA, S. et al. Os ácaros na cultura da amora em estufa e infestantes. IV Colóquio Nacional da Produção de Pequenos Frutos, Actas Portuguesas de Horticultura. Odemira, n.20, p.69-76, 2012.) mites were the most common of those predators.

The study conducted by MARCHETTI & FERLA (2011MARCHETTI, M; FERLA, N. J. Diversidade e flutuação populacional de ácaros (Acari) em amora-preta (Rubus fruticosus, Rosaceae) no estado do Rio Grande do Sul, Brasil. Iheringa, Porto Alegre, v.101, n.1-2, p.43- 48. 2011. Available from: <Available from: http://www.scielo.br/pdf/isz/v101n1-2/v101n1-2a05.pdf >. Accessed: Jun. 22, 2017.
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) on blackberry cultivars (Brazo, Caingangue, and Tupy) in the municipality of Ilópolis (RS) showed that the occurrence of phytophagous mites of the families Diptilomiopidae and Tetranychidae was predominant and those of the Tenuipalpidae family was smaller in number. Among predatory mites, the families Stigmaeidae (Agistemus brasiliensis Matioli, Ueckermann & Oliveira, 2002) was the most abundant species) and Phytoseiidae (Typhlodromalus aripo (DeLeon, 1967) was the most prevalent species in the Caingangue cultivar) were outstanding.

Given this scenario, knowledge about mite diversity in various blackberry genotypes in the southern region of RS will provide additional information to further studies in other regions of this state. This knowledge, along with subsequent studies on Biology and Ecology of mites, will contribute to the management of potential pests in the crop. Therefore, the objective of this study was to determine the fauna of mites in blackberry genotypes in the southern region of Rio Grande do Sul.

MATERIALS AND METHODS:

This study was carried out in the period Nov. 2015 - Oct. 2016 in an experimental orchard of Embrapa Clima Temperado (latitude 31° 42’S, longitude 52° 24’O, and altitude de 57m), in the municipality of Pelotas, RS, Brazil. Blackberry genotypes 128, 132, 139, 164, 178, 181, and 198 and “Tupy” were used. All plants were arranged in parallel lines (50cm between plants and 3m between rows), without support system, except those of Tupy cultivar, which were supported by two wire strands and driven approximately in V. Five plants (replicates) per genotype were evaluated. In each crop and in the period of experimentation, the plants were kept without agrotoxic application and the cultural treatments were carried out according to the technical recommendations for the crop.

Samples were collected monthly from November to October, except in November and December (fruiting months), when they were collected biweekly (total: 14 samplings). Six leaflets (two in each of the upper, middle and lower thirds) were collected from each plant (total: 240 leaflets per sample). In the flowering and fruiting period, two flowers and four fruits (both from the upper and middle third) were collected per repetition, and 10 samples were collected per genotype (total: 80 flowers and 160 fruits) per collection season. Samples were placed in paper bags and packed in styrofoam boxes to be transported to the Acarology Laboratory (Federal University of Pelotas), where they were processed (under a Nikon SMZ 745 stereomicroscope, with the help of brushes and tweezers). Mites were identified in the same laboratory using a phase-contrast (Nikon E200) microscope.

In the laboratory, the leaves were observed (on the adaxial and abaxial surface) under a stereomicroscope, when the mites were collected and quantified. Regarding Eriophyoidea, mites were quantified in 1cm2 area of the leaf (on the abaxial surface) by which it is united with the petiole. Fruits were evaluated in only half the sample, examining the regions between drupes and counting the number of specimens. Specimens collected from leaves, flowers, and fruits were transferred to Eppendorf flasks containing 70% alcohol solution. Then, they were mounted on slides containing Hoyer’s medium, remaining in an oven (50oC; 10-15 days), and adult mites were then identified and quantified.

The morphological characters observed on both surfaces of the leaves were described from samples of different parts of the plants. The presence or absence of acule and domatia (GONÇALVES & LORENZI, 2007GONÇALVES, E. G; LORENZI, H. Morfologia Vegetal. São Paulo: Instituto Plantarum de Estudos da Flora, 2007. 416p.) and trichomes and types of tricoma and indument (BEENTJE, 2016BEENTJE, H. J.The Kew Plant Glossary: An Illustrated Dictionary of Plant Terms. ReinoUnido: Kew Publishing, 2016. 184p.) were evaluated according to the literature. Leaf trichome densities were evaluated by comparing genotypes. This morphological description was performed at the Botanical Laboratory (Embrapa Clima Temperado).

Results were analyzed using the AnaFau software (MORAES et al., 2003MORAES, R. C. B.; et al. Software para análise estatística - ANAFAU. In: SIMPÓSIO DE CONTROLE BIOLÓGICO VIII, 2003, São Pedro, SP. Resumos... Piracicaba: ESALQ/USP, 2003, p.195.). The faunistic indexes for dominance, abundance, frequency, constancy, and Shannon-Wiener diversity (H’) were calculated to characterize the mite fauna in different blackberry genotypes.

RESULTS AND DISCUSSION:

The occurrence of 12 species of mites distributed in eight families was recorded (Table 1), totaling 11,158 mites classified as phytophagous (5940), predatory (323), and miscellaneous-feeding (4895) mites. In analyzing mite distribution per family, the Tydeidae, Diptilomiopidae, Tetranychidae, and Eriophyidae families showed a higher representability. The predominance of certain mite families may be associated with their preference for the host plant, favoring their establishment and development. In addition, the presence of the tetranychid Neotetranychus asper (Feres & Flechtmann, 2000) and tydeid Tydeus californicus (Banks, 1904) was observed in all plant genotypes. Conversely, the eriophyoid Diptacus rubuscolum (Trinidad, Duarte & Navia, 2018TRINIDAD, C.T.O. et al. Eriophyoid mites associated with the blackberry in Brazil-a new species in the genus Diptacus Keifer 1951 (Diptilomiopidae) and first report and supplementary description of Acalitus orthomerus (Keifer, 1951) (Eriophyidae). Systematic & Applied Acarology, Auckland, v.23, n.6, p.1199-1216, 2018.) showed a relatively-high population in all plant genotypes in the months of November, December, and January of 2016; although, this species has only been described recently by TRINIDAD et al. (2018TRINIDAD, C.T.O. et al. Eriophyoid mites associated with the blackberry in Brazil-a new species in the genus Diptacus Keifer 1951 (Diptilomiopidae) and first report and supplementary description of Acalitus orthomerus (Keifer, 1951) (Eriophyidae). Systematic & Applied Acarology, Auckland, v.23, n.6, p.1199-1216, 2018.). However, the eriophid Acalitus orthomerus (Keifer, 1951) occurred in drupes in greater quantity in Dec. 2015 and Jan. 2016, when fruits reach maturation and are harvested; although, it has not been sampled in leaves, floral buds, or open flowers. This has led to a drastic reduction in mite population, which is also related to the significant seasonal changes in host plant morphology (DAVIES et al., 2001bDAVIES, J. T. et al. Intraplant distribution of Acalitus essigi (Acari: Eriophyoidea) on blackberries (Rubus fruticosus agg.). Experimental & Applied Acarology, Amsterdam, v.25, n.8, p.625-639, 2001b. Available from: <Available from: https://link.springer.com/article/10.1023/A:1016179817089 >. Accessed: Jun. 20, 2017. doi: 10.1023/A:1016179817089.
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) and it is good if the decrease in the number of mites in the plant is considered.

Table 1
Mite species present in blackberry genotypes. Pelotas, RS.

Significant differences were observed between the number of mites in each genotype evaluated (Table 2). The N. asper had a similar frequency in the plant genotypes 139, 164, 181, and 198 and “Tupy”. However, genotype 164 and “Tupy” were the most favorable for the tetranychid mite Oligonychus yothersi (McGregor, 1915). Diptacus rubuscolum, Polyphagotarsonemus latus (Banks, 1904), and Brevipalpus spp. (Donnadieu, 1875) showed no significant difference in the evaluated genotypes and “Tupy”. Acalitus orthomerus had a similar occurrence in all genotypes (except genotype 128) and “Tupy”. Tydeus californicus occurred similarly in genotypes 132, 139, 164, 178, and 198 and “Tupy”. Few mites Euseius mesembrinus (Dean, 1957) were found mostly in genotype 128 and “Tupy”. Phytoseiid mites Amblyseius operculatus (De Leon, 1967), Galendromus (Galendromus) annectens (De Leon, 1958), and Typhlodromalus aripo (De Leon, 1967) did not differ in the number of individuals in each genotype and “Tupy”.

Table 2
Average number of mites per plant collected in blackberry orchard in the period Nov 2015 - Oct. 2016, in the municipality of Pelotas, RS.

Regarding the number of occurrences, N. asper, D. rubuscolum, and T. californicus showed similar amounts in genotypes 128 and 164 (Table 2). In genotype 132, the observed number of D. rubuscolum and T. californicus was similar. Tydeus californicus showed difference in relation to other mite species reported in genotypes 139 and 178. Genotype 181 showed no difference in the number of N. asper, D. rubuscolum, A. orthomerus, P. latus, Agistemus spp., and T. californicus. Occurrence of N. asper, D. rubuscolum, A. orthomerus, and T. californicus did not differ in the number of individuals in genotype 198 and “Tupy”.

According to the faunal analysis (Tables 3 and 4), variation in mite distribution and behavior was observed in various genotypes. This may be related to the differences between genotypes regarding morphological characters on the adaxial surface of the leaf (Table 5). In genotypes 128 and 178, N. asper, D. rubuscolum, and T. californicus were considered prevailing, as they reached the maximum rates in faunal classification (Tables 3 and 4). For genotype 128, only the E. mesembrinus predatory mite showed to be dominant, very abundant, very frequent, and constant. This may suggest that the complex of phytoseiid mites found in the present study was not sufficient to regulate the number of these species of pest mites.

Table 3
Faunal analysis of adult mites collected in blackberry orchard in the period Nov. 2015 - Oct 2016, in the municipality of Pelotas, RS.
Table 4
Faunal analysis of adult mites collected in blackberry orchard in the period Nov 2015 - Oct 2016, in the municipality of Pelotas, RS.

The same species was also reported by MARCHETTI & FERLA (2011MARCHETTI, M; FERLA, N. J. Diversidade e flutuação populacional de ácaros (Acari) em amora-preta (Rubus fruticosus, Rosaceae) no estado do Rio Grande do Sul, Brasil. Iheringa, Porto Alegre, v.101, n.1-2, p.43- 48. 2011. Available from: <Available from: http://www.scielo.br/pdf/isz/v101n1-2/v101n1-2a05.pdf >. Accessed: Jun. 22, 2017.
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) and occurred in Brazos and Tupy cultivars. Mites of the genus Euseius are classified as generalist predators, for which pollen is an important part of the diet, increasing their reproductive potential after flowering (MCMURTRY et al., 2013MCMURTRY, J. A. et al. Revision of the lifestyles of phytoseiid mites (Acari: Phytoseiidae) and implications for biological control strategies. Systematic & Applied Acarology, Londres, v.18, n.4, p.297-320, 2013. Available from: <Available from: https://www.biotaxa.org/saa/article/view/saa.18.4.1/0 >. Accessed: Jun. 21, 2017. doi: 10.11158/saa.18.4.1.
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).

Typhlodromalus aripo was another phytoseiid that reached high values for abundance and frequency rates in genotype 178. This species was reported in the Caingangue blackberry cultivar (MARCHETTI & FERLA, 2011MARCHETTI, M; FERLA, N. J. Diversidade e flutuação populacional de ácaros (Acari) em amora-preta (Rubus fruticosus, Rosaceae) no estado do Rio Grande do Sul, Brasil. Iheringa, Porto Alegre, v.101, n.1-2, p.43- 48. 2011. Available from: <Available from: http://www.scielo.br/pdf/isz/v101n1-2/v101n1-2a05.pdf >. Accessed: Jun. 22, 2017.
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) and it was confirmed both to use herbivorous-induced volatile compounds to seek prey and discriminate between pubescent and glabrous cultivars in cassava culture (ONZO et al., 2012ONZO, A. et al. The predatory mite Typhlodromalus aripoprefers green-mite induced plant odours from pubescent cassava varieties. Experimental and Applied Acarology, Amsterdam, v.58, n.4, p.359-370, 2012. Available from: <Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3487005/ >. Accessed: Jun. 21, 2017. doi: 10.1007/s10493-012-9595-0.
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). This characteristic and mite morphology were used (MCMURTRY et al., 2013MCMURTRY, J. A. et al. Revision of the lifestyles of phytoseiid mites (Acari: Phytoseiidae) and implications for biological control strategies. Systematic & Applied Acarology, Londres, v.18, n.4, p.297-320, 2013. Available from: <Available from: https://www.biotaxa.org/saa/article/view/saa.18.4.1/0 >. Accessed: Jun. 21, 2017. doi: 10.11158/saa.18.4.1.
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) to classify it as a generalist subtype III-a predator, which prefers pubescent leaves. In all blackberry genotypes analyzed in this study, the leaves have glabrous adaxial surface and pubescent abaxial surface, and only its type of indumentation varied. Thus, the idea that volatile compounds would also influence the behavior of these mites in the crop cannot be disregarded.

Amblyseius operculatus was absent in genotypes 132, 139, 164, and 198. However, its abundance was rare in genotypes 128 and 181 and “Tupy”. According to MCMURTRY et al. (2013MCMURTRY, J. A. et al. Revision of the lifestyles of phytoseiid mites (Acari: Phytoseiidae) and implications for biological control strategies. Systematic & Applied Acarology, Londres, v.18, n.4, p.297-320, 2013. Available from: <Available from: https://www.biotaxa.org/saa/article/view/saa.18.4.1/0 >. Accessed: Jun. 21, 2017. doi: 10.11158/saa.18.4.1.
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), this species is classified as generalist subtype III-b predators, which prefer glabrous leaves. All genotypes analyzed in this study present glabrous adaxial surface, and trichomes have a very low density on the abaxial surface, thus explaining the presence of this species in the culture. This phytoseiid species was not yet reported in the blackberry crop in RS. Occurrence of Amblyseius compositus (Denmark & ​​Muma, 1973), Amblyseius herbicolus (Chant, 1959), and Amblyseius neochiapensis (Lofego, Moraes & McMurtry, 2000) in blackberry culture was reported by MARCHETTI & FERLA (2011MARCHETTI, M; FERLA, N. J. Diversidade e flutuação populacional de ácaros (Acari) em amora-preta (Rubus fruticosus, Rosaceae) no estado do Rio Grande do Sul, Brasil. Iheringa, Porto Alegre, v.101, n.1-2, p.43- 48. 2011. Available from: <Available from: http://www.scielo.br/pdf/isz/v101n1-2/v101n1-2a05.pdf >. Accessed: Jun. 22, 2017.
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).

The phytoseiid Galendromus (G.) annectens, which was classified as common and frequent, was another species found in genotype 178. It was reported to occur in blackberry plants (Rubus fruticosus; MARCHETTI & FERLA, 2011MARCHETTI, M; FERLA, N. J. Diversidade e flutuação populacional de ácaros (Acari) em amora-preta (Rubus fruticosus, Rosaceae) no estado do Rio Grande do Sul, Brasil. Iheringa, Porto Alegre, v.101, n.1-2, p.43- 48. 2011. Available from: <Available from: http://www.scielo.br/pdf/isz/v101n1-2/v101n1-2a05.pdf >. Accessed: Jun. 22, 2017.
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) and wild mulberry along with other phytoseid (MCMURTRY & SHOW, 2012MCMURTRY, J. A.; SHOW, E. D. Phytoseiidae on blackberry in Central California. Systematic & Applied Acarology, Londres, v.17, n.4, p.384-387, 2012. Available from: <Available from: http://www.bioone.org/doi/abs/10.11158/saa.17.4.6 >. Accessed: Jun. 21, 2017. doi: 10.11158/saa.17.4.6>.
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). The presence of Galendromus (G.) annectens, which was classified as a type-II predator (MCMURTRY et al., 2013MCMURTRY, J. A. et al. Revision of the lifestyles of phytoseiid mites (Acari: Phytoseiidae) and implications for biological control strategies. Systematic & Applied Acarology, Londres, v.18, n.4, p.297-320, 2013. Available from: <Available from: https://www.biotaxa.org/saa/article/view/saa.18.4.1/0 >. Accessed: Jun. 21, 2017. doi: 10.11158/saa.18.4.1.
https://www.biotaxa.org/saa/article/view...
), is probably linked to the presence of O. yothersi, which was also reported in the present study.

Agistemus spp. (Sumers, 1960) was classified as common and frequent in almost all (128, 132, 139, 164, 178, and 181) genotypes and “Tupy”. Agistemus brasiliensis was reported in the Caingangue blackberry cultivar (MARCHETTI & FERLA, 2011MARCHETTI, M; FERLA, N. J. Diversidade e flutuação populacional de ácaros (Acari) em amora-preta (Rubus fruticosus, Rosaceae) no estado do Rio Grande do Sul, Brasil. Iheringa, Porto Alegre, v.101, n.1-2, p.43- 48. 2011. Available from: <Available from: http://www.scielo.br/pdf/isz/v101n1-2/v101n1-2a05.pdf >. Accessed: Jun. 22, 2017.
http://www.scielo.br/pdf/isz/v101n1-2/v1...
) and cited as a potential predator of the mite vector of citrus leprosis (MATIOLI & OLIVEIRA, 2007MATIOLI, A. L.; OLIVEIRA, C. A. L. Biologia de Agistemus brasiliensis Matioli, Ueckermann & Oliveira (Acari: Stigmaeidae) e sua potencialidade de predação sobre Brevipalpus phoenicis (Geijskes) (Acari: Tenuipalpidae). Neotropical Entomology, Londrina, v.36, n.4, p.577-582, 2007. Available from: <Available from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S1519-566X2007000400016 >. Accessed: Jun. 21, 2017. doi: 10.1590/S1519-566X2007000400016 .
http://www.scielo.br/scielo.php?script=s...
).

Diptacus rubuscolum and T. californicus reached maximum classification values in genotype 132, as superdominant, superabundant, super frequent, and constant, without significant presence of predators.

Acalitus orthomerus reached high faunal rates in fruits of genotypes 128, 132, and 139, as well as of genotype 178, and this was its first record in Brazil. This deserves more attention due to the potential damage of blackberry because it was reported to cause blisters and warts as a result of its large-scale feeding from buds. In addition, high infestation by A. orthomerus resulted in galls that do not allow budding (BAKER et al., 1996BAKER, E.W. et al. Eriophyoid mites of the United States. Michigan : Indira Publishing House, 1996. 394p.); although, mite-associated symptom was not observed in plants during the study period. It should be noted that symptoms of mite attack were observed outside the sampling period, but such symptoms corresponded to those reported for A. essigi, i.e., those that cause the so-called “redberry” symptom of mulberry (KEIFER et al., 1982KEIFER, H. H. et al. An illustrated guide to plant abnormalities caused by eriophyid mites in North America. United States Department of Agriculture. Agriculture handbook, n.573, p.177, 1982.; BAKER et al., 1996; DAVIES et al., 2001aDAVIES, J. T. et al. Dispersal of Acalitus essigi to blackberry (Rubus fruticosus agg.)frui. Entomologia Experimentalis et Applicata, v.101, p.19-23, 2001a. Available from: <Available from: http://onlinelibrary.wiley.com/doi/10.1046/j.1570-7458.2001.00886.x/full >. Accessed: Jul. 16, 2017. doi: 10.1046/j.1570-7458.2001.00886.x.
http://onlinelibrary.wiley.com/doi/10.10...
). In Portugal, this mite is known as the “red-berry mite” (FERREIRA & PINA, 2012FERREIRA, M. A.; PINA, S. Ácaro-da-vaga-vermelha Acalitus essigi (Hassan). Coleção Técnico-Científica, Odemira, Portugal: INIAV / EUBerry, 2012. 18 p.).

Thus, they are not enough to confirm and consider that it is a pest, compared to other mites in other cultures, despite a relatively high number of eriophid mites was found.

In relation to genotype 139, T. californicus was the predominant mite species. Furthermore, observations during evaluations indicated that the presence of trichomes and domatias would result in an important place for these mites to refuge. These same characteristics could also have favored the occurrence of T. californicus in all genotypes, as they all have trichomes and domatias in their leaves (Table 5). Tydeus californicus was reported by UECKERMANN & GROUT (2007UECKERMANN, E. A.; GROUT, T. G. Tydeoid mites (Acari: Tydeidae, Edbakerellidae, Iolinidae) occurring on citrus in Southern Africa. Journal of Natural History, Londres, v.41, n.37-41, p.2351-2378, 2007.) and occurs as a prey for mite predators of citrus in South Africa. FLESCHNER & ARAKAWA (1952)FLESCHNER, C. A.; ARAKAWA, K. Y. The mite Tydeus californicus on citrus and avocado leaves. Journal of Economic Entomology, Annapolis, v.45, n.6, p.1952. reported the occurrence of this same species on the abaxial surface of leaves in citrus and avocado trees and classified it as phytophagous mite; although, apparent symptoms of damage were not observed. In RS State, T. californicus was reported in association with grapevine (Vitis vinifera) culture (SILVA et al., 2014bSILVA, G. L. da et al. Tydeid and triophtydeid mites (Acari: Tydeoidea) associated with grapevine (Vitaceae: Vitis spp.) in Brazil, with the descriptions of species of Prelorryia (André, 1980) and Tydeus Koch, 1835. Zootaxa, Auckland, v.3814, n.4, p.495-511, 2014b.
https://doi.org/Auckland...
). They offered a diet with and without pollen from Typha angustifolia L. (Typhaceae) to T. californicus and concluded that only leaf is not enough for them to complete their development; and pollen is therefore, an indispensable part of their diet (SILVA et al., 2014aSILVA, G. L. da et al. Life cycle of Tydeus californicus (Acari: Tydeidae) on leaves of Inga marginata with and without pollen of Typha angustifolia under laboratory conditions. International Journal of Acarology, Abingdon, v.40, p.1-4, 2014a.).

Table 5
Morphological characteristics on the adaxial (ADS) and abaxial (ABS) surfaces of leaves from black berry with different genotypes and Tupy cultivar.

Tydeid mites have a worldwide distribution and they can feed on plants,; although, they are recognized as predators of small insects and other mites and their eggs. Thus, T. californicus is a predator of the Aceria sheldoni (Ewing, 1937) citrus bud mite in southern California, USA (BAKER & WHARTON, 1952 BAKER, E. W.; WHARTON, G. W. An Introduction to Acarology. New York: The Macmillan Company. 1952. 490p. Available from: <Available from: https://archive.org/stream/introductiontoac00bake#page/n0 >. Accessed: Jul. 23, 2017.
https://archive.org/stream/introductiont...
). Tydeus gloveri Ashmead and Tydeus coccophagus Ewing were reported as predators of insects and their eggs (MCGREGOR, 1932MCGREGOR, E. A. The ubiquitous mite, a new species on citrus. Proceedings of the Entomological Society of Washington, v.34, n.4, p.60-61, 1932. Available from: <Available from: https://www.biodiversitylibrary.org/page/16144288#page/342/mode/1up >. Accessed: Jul. 23, 2018.
https://www.biodiversitylibrary.org/page...
).

Several foods were offered to two species of tydeid mites and aimed to know the existing nutritional phytophagous relationship. The importance of honeydew in the nutrition of both Lorryia ferulus Baker and Tydeus bakeri was the greatest revelation, because developing complete colonies was then possible. Tetranychus telarius mite eggs showed to be a good nutrient for L. ferulus but not for T. bakeri, which has never been observed in the field in association with mite eggs. The eriophid mites showed no nutritional importance, and the tetranychid Panonychus ulmi (Koch) also showed no positive result for any of both tydeid mites (BRICKHILL, 1958BRICKHILL, C.D. Biological studies of two species of tydeid mites from California. Hilgardia, v.27, n.20, p.601-622, 1958. Available from: <Available from: http://hilgardia.ucanr.edu/fileaccess.cfm?article=152474&p=LNIZKC >. Accessed: Jul. 15, 2018. doi: 10.3733/hilg.v27n20p601.
http://hilgardia.ucanr.edu/fileaccess.cf...
).

Another study suggested that tydeid mites are fungivorous. DUSO et al., (2005DUSO, C. et al. Grape downy mildew spread and mite seasonal abundance in vineyards: effects on Tydeus caudatus and its predators. Biological Control, v.32, p.143-154, 2005. Available from: <Available from: https://www.sciencedirect.com/science/article/pii/S104996440400177X >. Accessed: Jul. 23, 2018. doi: 10.1016/j.biocontrol.2004.09.004.
https://www.sciencedirect.com/science/ar...
) evidenced this fact in Tydeus caudatus (Dugés) through the correlation between this mite and disseminated mildew in the commercial vineyard vegetation, because mite populations on symptomatic leaves were larger than those on asymptomatic leaves. This fact was also confirmed by MELIDOSSIAN et al. (2005MELIDOSSIAN, H. S. et al. Suppression of grapevine powdery mildew by a mycophagousmite. Plant Disease, v.89, n.12, p.1331-1338, 2005. Available from: <Available from: https://apsjournals.apsnet.org/doi/abs/10.1094/PD-89-1331 >. Accessed: Jul. 23, 2017.
https://apsjournals.apsnet.org/doi/abs/1...
), who reported that Orthotydeus lambi (Baker, 1970) can suppress fruit powdery mildew by reducing the inoculum in leaf infections.

Regarding pepper, morphology of the plant and distribution of trichomes influence mite development (MATOS et al., 2009MATOS, C. H. C. et al. Os Tricomas de Capsicum spp. interferem nos aspectos biológicos do ácaro-branco Polyphagotarsonemus latus Banks (Acari: Tarsonemidae)? Neotropical Entomology, Londrina, v.38, n.5, p.1-6, 2009. Available from: <Available from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S1519-566X2009000500005 >. Accessed: Jun. 21, 2017. doi: 10.1590/S1519-566X2009000500005.
http://www.scielo.br/scielo.php?script=s...
). In all genotypes, blackberry leaves presented trichomes on the abaxial surface at very low density (Table 5). The occurrence of P. latus in blackberries with genotypes 181 and 198 could be related to other causes, as well as specific morphological and chemical causes that are attractive or favor the species. In blackberry genotype 164, only the N. asper mite species was predominant. In blackberry genotype 181, D. rubuscolum mite, in addition to the tetraniquid N. asper mite, was classified as dominant, very abundant, very frequent, and constant during the evaluation period. In blackberry genotypes 181 and 198, the tarsonemid P. latus mite was classified as dominant, very abundant, and very frequent. Although, this is the first report on its occurrence in blackberry in Brazil, it is considered a cosmopolitan species. VINCENT et al. (2010VINCENT, C. I. et al. Broad mite on primocane-fruiting blackberry in organic production in Arkansas. Hort Technology, Alexandria, v.20, n.4, p.718-723, 2010. Available from: <Available from: http://horttech.ashspublications.org/content/20/4/718.full >. Accessed: Jun. 22, 2017.
http://horttech.ashspublications.org/con...
) reported the occurrence of the white mite in organic blackberry production causing the ripple symptom in the leaves. It was identified in vine crops (Bento Gonçalves, RS), occurring mainly in new vine leaves after green pruning (JOHANN et al., 2009JOHANN, L. et al. Acarofauna (Acari) associada à videira (Vitisvinifera L.) no Estado do Rio Grande do Sul. Biociências, Porto Alegre, v.17, p.1-19. 2009. Available from: <Available from: https://s3.amazonaws.com/academia.edu.documents/38362691/4756.pdf?AWSAccessKeyId=AKIAIWOWYYGZ2Y53UL3A&Expires=1520186668&Signature=kPmjWnrZZMakyDwByewgfuUmq5w%3D&response-content-disposition=inline%3B%20filename%3DAcarofauna_Acari_associada_a_videira_Vit.pdf >. Accessed: Mar. 04, 2018.
https://s3.amazonaws.com/academia.edu.do...
). The white mite was found associated with the peach crop (Embrapa Clima Temperado; Pelotas, RS), occurring with higher population density in the January-May period, mainly after harvesting (ZANARDI et al., 2013ZANARDI, O. Z. et al. Flutuação Populacional dos Principais ácaros em Pessegueiro nos Sistemas de Cultivos Protegidos e Convencional. Comunicado Técnico, Pelotas, p.1-6, 2013.). Its highest populational density occurs in early summer, especially in years with more rainfall and increased humidity (VIEIRA et al., 2004VIEIRA, M. R. et al. Efeito do cultivo do mamoeiro (Carica papaya L.) em ambiente protegido sobre a ocorrência de ácaros fitófagos e moscas-brancas. Revista Brasileira de Fruticultura, Jaboticabal, v.26, n.3, p.441-445, 2004. Available from: <Available from: http://www.scielo.br/pdf/rbf/v26n3/23141.pdf >. Accessed: Mar. 05, 2018.
http://www.scielo.br/pdf/rbf/v26n3/23141...
). These facts could elucidate its occurrence in mulberry trees, taking into account that dispersion of tarsonemid mites occurs by movement of adult forms to regions of growth of the same plant, contact between plant leaves, wind, and even foretically, as observed in P. latus mites on whiteflies (MORAES & FLECHTMANN, 2008MORAES, G.J.; FLECHTMANN, C.H.W. Manual de Acarologia: Acarologia básica & ácaros de plantas cultivadas no Brasil. Ribeirão Preto: Holos Editora, 2008. 308p.; ZANARDI et al., 2013ZANARDI, O. Z. et al. Flutuação Populacional dos Principais ácaros em Pessegueiro nos Sistemas de Cultivos Protegidos e Convencional. Comunicado Técnico, Pelotas, p.1-6, 2013.).

In “Tupy”, T. californicus and A. asper were classified as dominant, very abundant, very frequent, and constant; whereas, A. orthomerus was present in less than 50% of the samples. However, this is important for the symptoms they could cause on fruits.

In the study of blackberry genotypes, the values for the diversity index (H) of mites varied in the range 0,83-1,79. The maximum value for H was reached in genotype 181 (Table 4). MARCHETTI & FERLA (2011MARCHETTI, M; FERLA, N. J. Diversidade e flutuação populacional de ácaros (Acari) em amora-preta (Rubus fruticosus, Rosaceae) no estado do Rio Grande do Sul, Brasil. Iheringa, Porto Alegre, v.101, n.1-2, p.43- 48. 2011. Available from: <Available from: http://www.scielo.br/pdf/isz/v101n1-2/v101n1-2a05.pdf >. Accessed: Jun. 22, 2017.
http://www.scielo.br/pdf/isz/v101n1-2/v1...
) studied the diversity and fluctuation of mite population in blackberry cultivars and obtained a variable diversity index in the Caingangue (0.42) and Tupy (1.29) cultivars.

CONCLUSION:

Twelve mite species are distributed in eight families in the blackberry orchard (Municipality of Pelotas, RS). The phytophagous N. asper and D. rubuscolum are predominant in blackberry genotypes 164 and 128, respectively. Therefore, future studies should focus on the characterization of damage caused by these mites.

ACKNOWLEDGEMENTS

To the PhD researchers at Embrapa Clima Temperado, Maria do Carmo B Raseira, for her help during sampling, Gustavo Heiden, for his help in the morphological description of the blackberry genotypes studied, and Gilberto José de Moraes, Carlos HW Flechtmann (Escola Superior de Agricultura Luiz de Queiroz (ESALQ)/Universidade de São Paulo (USP)), and Peterson R. Demite, for their help in identifying some mites.

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    CR-2017-0734.R2

Publication Dates

  • Publication in this collection
    2019

History

  • Received
    11 Oct 2017
  • Accepted
    03 Dec 2018
  • Reviewed
    31 Jan 2019
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