ABSTRACT:

The transit of infested plants may favor the introduction of herbivores into pest-free regions. In this study, we reported the occurrence of pest mites in Dendrobium phalaenopsis Fitzg. Mites were collected from orchid leaves with lesions. We identified Brevipalpus californicus (Banks, 1904) (sensu latu), Brevipalpus yothersi Baker, 1949 and Tenuipalpus orchidofilo Moraes & Freire, 2001 (Tenuipalpidae). These species had not been registered in D. phalaenopsis. This study reinforces the importance of adequate phytosanitary care for orchid cultivation, since these mites can infest other cultivated plants and damage orchids.

Key words:
damage; flat mites; plant mites; Tenuipalpidae; Orchidaceae pest

RESUMO:

O trânsito de plantas infestadas pode favorecer a introdução de herbívoros em regiões livres de pragas. Neste estudo, relata-se a presença de ácaros-praga em Dendrobium phalaenopsis Fitzg. Os ácaros foram coletados de folhas de orquídeas com danos. Identificou-se Brevipalpus californicus (BANKS, 1904) (sensu latu), Brevipalpus yothersi Baker, 1949 e Tenuipalpus orchidofilo Moraes & Freire, 2001 (Tenuipalpidae). Até o momento, essas espécies não haviam sido registradas em D. phalaenopsis. O estudo alerta sobre a importância de cuidados fitossanitários adequados para o cultivo e comercialização de orquídeas, uma vez que esses ácaros também podem infestar outras plantas cultivadas, além de danificar orquídeas.

Palavras-chave:
danos; ácaros planos; ácaros de plantas; Tenuipalpidae; Praga de Orchidaceae

Orchids are ornamental plants of the class Liliopsida, Order Aparagales, and Family Orchidaceae (CHASE et al., 2015CHASE, M. W. et al. An updated classification of Orchidaceae. Botanical Journal of the Linnean Society, v.177, n.2, p.151-174, 2015. Available from: <Available from: https://academic.oup.com/botlinnean/article/177/2/151/2416341?login=true >. Accessed: Jan. 08, 2019. doi: 10.1111/boj.12234.
https://academic.oup.com/botlinnean/arti... ) and have relevant socioeconomic importance in the ornamental flower market through the sales of seedlings (JUNQUEIRA & PEETZ, 2014JUNQUEIRA, A. H.; PEETZ, M. S. O. The productive sector of flowers and ornamental plants of Brazil, in the period from 2008 to 2013: updates, balance sheets and prospects. Revista Brasileira de Horticultura Ornamental, v.20, n.2, p.115-120, 2014. Available from: <Available from: http://www.hortica.com.br/artigos/2014/Setor_Produtivo_Cadeia_Flores_Plantas_Ornamentais_2014.pdf >. Accessed: Jan. 17, 2020.
http://www.hortica.com.br/artigos/2014/S... ). However, several species of mites are orchid pests (SULZBACH et al., 2015SULZBACH, M. et al. 2015. Abundance and seasonality of two-spotted spider mite on gerbera cultivars. Ciência Rural, v.45, n.4, p.578-584, 2015. Available from: <Available from: https://www.scielo.br/scielo.php?pid=S0103-84782015000400578&script=sci_arttext&tlng=pt >. Accessed: Oct. 23, 2020. doi: 10.1590/0103-8478cr20131494.
https://www.scielo.br/scielo.php?pid=S01... ).

Phytophagous mites of the family Tenuipalpidae are characterized as pests in ornamental plant crops (MIRANDA et al., 2007MIRANDA, L. C. et al. Brevipalpus mites Donnadieu (Prostigmata: Tenuipalpidae) associated with ornamental plants in Distrito Federal, Brazil. Neotropical Entomology, v.36, n.4, p.587-592, 2007. Available from: <Available from: https://www.scielo.br/scielo.php?pid=s1519-566x2007000400018&script=sci_arttext >. Accessed: May, 25, 2020. doi: 10.1590/S1519-566X2007000400018.
https://www.scielo.br/scielo.php?pid=s15... ; KITAJIMA et al., 2010KITAJIMA, E. W. et al. An annotated list of ornamentals naturally found infected by Brevipalpus mite-transmitted viruses. Scientia Agricola, v.67, n.3, p.348-371, 2010. Available from: <Available from: https://www.scielo.br/scielo.php?pid=S0103-90162010000300014&script=sci_arttext >. Accessed: Mar. 18, 2020. doi: 10.1590/S0103-90162010000300014.
https://www.scielo.br/scielo.php?pid=S01... ; SANTOS et al., 2010SANTOS, R. M. V. et al. Mites (Arachnida: Acari) associated with tropical ornamental plants in the southern coastal region of Bahia, Brazil. Arquivos do Instituto Biológico, v.77, n.1, p.43-48, 2010. Available from: <Available from: https://www.scielo.br/scielo.php?pid=S1808-16572010000100043&script=sci_arttext&tlng=pt >. Accessed: Jul. 25, 2020. doi: 10.1590/1808-1657v77p0432010.
https://www.scielo.br/scielo.php?pid=S18... ), associated to direct and indirect damage, also acting as virus vectors (RODRIGUES & CHILDERS, 2013RODRIGUES, J. C. V.; CHILDERS, C. C. Brevipalpus mites (Acari: Tenuipalpidae): vectors of invasive, non-systemic cytoplasmic and nuclear viroses in plants. Experimental and Applied Acarology, v.59, n.1-2, p.165-175, 2013. Available from: <Available from: https://link.springer.com/article/10.1007/s10493-012-9632-z >. Accessed: Jul. 25, 2020. doi: 10.1007/s10493-012-9632-z.
https://link.springer.com/article/10.100... ; HUANG et al., 2019HUANG, C. H. et al. Biological, pathological, and molecular characteristics of a new Potyvirus, Dendrobium chlorotic mosaic virus, infecting Dendrobium Orchid. Plant Disease, v.103, n.7, p.1605-1612, 2019. Available from: <Available from: https://apsjournals.apsnet.org/doi/full/10.1094/PDIS-10-18-1839-RE >. Accessed: Jan. 17, 2020. doi: 10.1094/PDIS-10-18-1839-RE.
https://apsjournals.apsnet.org/doi/full/... ). Damages reduce the commercial value of orchids, hindering their commercialization, since there is no specific control for all species of mites. The life cycle of Tenuipalpidae comprises egg, larva, protonymph, deutonymph, and adult, as well as chrysalis in which they do not move, but are physiologically active (KRANTZ & WALTER, 2009KRANTZ, G. W.; WALTER D. E. A. A manual of acarology, 3 ed. Texas Tech University Press: Lubbock, 2009. 807p.). Phytophagous mites play an important economic role in commercial crops; therefore, this study investigated the presence of pest mites in Dendrobium phalaenopsis Fitzg. in orchid cultivations in the state of Bahia, Brazil.

The study was carried out from May to July 2019 in an orchid nursery in the municipality of Cruz das Almas (12°40’47.3’’S 39°05’42.9’’W), Bahia State, Brazil. Leaves of D. phalaenopsis with damage characteristics (whitish spots) (Figure 1) were collected, packed in paper bags, and taken to the Insect Study Center (INSECTA) of the Universidade Federal da Bahia Recôncavo for specimen sorting and collection.

Figure 1
Dendrobium phalaenopsis Fitzg. orchid leaves with damages caused by mites.

We removed the mites from the leaves using a stereoscopic microscope and placed them in containers containing 70% alcohol. Then, the mites were mounted on slides with Hoyer medium for identification (KRANTZ & WALTER, 2009KRANTZ, G. W.; WALTER D. E. A. A manual of acarology, 3 ed. Texas Tech University Press: Lubbock, 2009. 807p.). Adults were selected for identification using an optical microscope phase contrast and consultation with specific dichotomous keys for the group to confirm the specimens.

Three mites belonging to the family Tenuipalpidae were identified: Brevipalpus californicus (BANKS, 1904) (sensu latu), Brevipalpus yothersi BAKER, 1949 and Tenuipalpus orchidofilo MORAES & FREIRE, 2001 (Figures 2A, 2B, and 2C, respectively). The occurrence of these species had not been registered in D. phalaenopsis in the state of Bahia, Brazil.

Figure 2
A: Brevipalpus californicus (BANKS, 1904) (sensu latu); B: Brevipalpus yothersi BAKER, 1949; C: Tenuipalpus orchidofilo MORAES & FREIRE, 2001.

These mite species were also reported on other species of ornamental plants (SANTOS et al., 2010SANTOS, R. M. V. et al. Mites (Arachnida: Acari) associated with tropical ornamental plants in the southern coastal region of Bahia, Brazil. Arquivos do Instituto Biológico, v.77, n.1, p.43-48, 2010. Available from: <Available from: https://www.scielo.br/scielo.php?pid=S1808-16572010000100043&script=sci_arttext&tlng=pt >. Accessed: Jul. 25, 2020. doi: 10.1590/1808-1657v77p0432010.
https://www.scielo.br/scielo.php?pid=S18... ). The occurrence of these pests can be favored by factors, such as climatic variations, which can directly affect orchid cultivation, leading to a population decline of natural enemies and favoring the establishment of the pest mites (CASTEX et al., 2018CASTEX, V. et al. Pest management under climate change: The importance of understanding tritrophic relations. Science of the Total Environment, v.616, p.397-407, 2018. Available from: <Available from: https://www.sciencedirect.com/science/article/pii/S0048969717330784?casa_token=LmuxA8zV95IAAAAA:j8hySjs3BOsJmBzrJqQPlB14RU_bZeH_RyNUnriiizxyaEpDCKBgFtzHEbEg4tORD_0desVRaBM >. Accessed: Nov. 10, 2019. doi: 10.1016/j.scitotenv.2017.11.027.
https://www.sciencedirect.com/science/ar... ). In addition, transportation of infested ornamental plants between regions can contribute to the spread of pests (MIRANDA et al., 2007MIRANDA, L. C. et al. Brevipalpus mites Donnadieu (Prostigmata: Tenuipalpidae) associated with ornamental plants in Distrito Federal, Brazil. Neotropical Entomology, v.36, n.4, p.587-592, 2007. Available from: <Available from: https://www.scielo.br/scielo.php?pid=s1519-566x2007000400018&script=sci_arttext >. Accessed: May, 25, 2020. doi: 10.1590/S1519-566X2007000400018.
https://www.scielo.br/scielo.php?pid=s15... ; CHONG et al., 2015CHONG, J. H. et al. Biology and management of Maconellicoccus hirsutus (Hemiptera: Pseudococcidae) on ornamental plants. Journal of Integrated Pest Management, v.6, n.1, p.5, 2015. Available from: <Available from: https://academic.oup.com/jipm/article/6/1/5/2936972?login=true >. Accessed: Jan. 15, 2019. doi: 10.1093/jipm/pmv004.
https://academic.oup.com/jipm/article/6/... ), which may have favored the occurrence of these species in the crops studied, since many of these plants originate from other regions in Brazil.

The direct damage caused by these mites can be identified by parts of the plant attacked with silvery-white areas and/or chlorotic spots on the leaves, which evolve into brown to dark brown discoloration, leading to death and premature leaf drop (MORAES & FLECHTMANN, 2008MORAES, G. J.; FLECHTMANN, C. H. W. Manual de Acarologia: Acarologia Básica e Ácaros de Plantas Cultivadas no Brasil, Ribeirão Preto: Holos, 2008. 308 p.).

The main damage in orchids is the formation of whitish spots in the plant leaf structure, as well as damages associated to virus transmission (KITAJIMA et al., 2010KITAJIMA, E. W. et al. An annotated list of ornamentals naturally found infected by Brevipalpus mite-transmitted viruses. Scientia Agricola, v.67, n.3, p.348-371, 2010. Available from: <Available from: https://www.scielo.br/scielo.php?pid=S0103-90162010000300014&script=sci_arttext >. Accessed: Mar. 18, 2020. doi: 10.1590/S0103-90162010000300014.
https://www.scielo.br/scielo.php?pid=S01... ). For instance, B. californicus is known as a vector for the orchid fleck virus (KONDO et al., 2003KONDO, H. et al. Orchid fleck virus: Brevipalpus californicus mite transmission, biological properties and genome structure. Experimental & Applied Acarology , v.30, n.1-3, p.215-223, 2003. Available from: <Available from: https://link.springer.com/article/10.1023/B:APPA.0000006550.88615.10 >. Accessed: Mar. 18, 2020.
https://link.springer.com/article/10.102... ).

Representatives of these genera causing damage to Phalaenopsis hybrids grown in greenhouses have been recorded in Poland (ŁABANOWSKI & SOIKA, 2011ŁABANOWSKI, G.; SOIKA, G. False spider mites (Acari: Tenuipalpidae) as pests on orchids (Phalaenopsis hybrids) in Poland. Biological Letters, v.48, n.2, p.167-175, 2011. Available from: <Available from: https://content.sciendo.com/view/journals/biolet/48/2/article-p167.xml >. Accessed: May, 25, 2020. doi: 10.2478/v10120-011-0015-7.
https://content.sciendo.com/view/journal... ). In the state of São Paulo, Brazil, the genus Brevipalpus was associated to virus transmission in Dendrobium sp. (KUBO et al., 2009KUBO, K. S. et al. Orchid fleck symptoms may be caused naturally by two different viruses transmitted by Brevipalpus. Journal of General Plant Pathology, v.75, n.3, p.250-255, 2009. Available from: <Available from: https://link.springer.com/article/10.1007/s10327-009-0167-z >. Accessed: Mar. 18, 2020. doi: 10.1007/s10327-009-0167-z.
https://link.springer.com/article/10.100... ). In Distrito Federal (Brazil), MIRANDA et al. (2007MIRANDA, L. C. et al. Brevipalpus mites Donnadieu (Prostigmata: Tenuipalpidae) associated with ornamental plants in Distrito Federal, Brazil. Neotropical Entomology, v.36, n.4, p.587-592, 2007. Available from: <Available from: https://www.scielo.br/scielo.php?pid=s1519-566x2007000400018&script=sci_arttext >. Accessed: May, 25, 2020. doi: 10.1590/S1519-566X2007000400018.
https://www.scielo.br/scielo.php?pid=s15... ) reported the occurrence of mites of the genus Brevipalpus sp. causing injuries to orchids (Dendrobium sp. and Oncidium sp.). Similar damages were observed in this study on leaves of orchid D. phalaenopsis.

Similarly, in Taiwan, HUANG et al. (2019HUANG, C. H. et al. Biological, pathological, and molecular characteristics of a new Potyvirus, Dendrobium chlorotic mosaic virus, infecting Dendrobium Orchid. Plant Disease, v.103, n.7, p.1605-1612, 2019. Available from: <Available from: https://apsjournals.apsnet.org/doi/full/10.1094/PDIS-10-18-1839-RE >. Accessed: Jan. 17, 2020. doi: 10.1094/PDIS-10-18-1839-RE.
https://apsjournals.apsnet.org/doi/full/... ) reported this same genus of mites infesting orchid Dendrobium sp. PIEDRA & GUEVARA (2020PIEDRA, H. Á.; GUEVARA, A. M. S. Nuevos hospederos y registros de ácaros fitófagos para Costa Rica: período 2013-2018. Agronomía Costarricense, v.44, n.1, p.9-28, 2020. Available from: <Available from: https://www.scielo.sa.cr/scielo.php?pid=S0377-94242020000100009&script=sci_arttext >. Accessed: Dec. 20, 2020. doi: 10.15517/rac.v44i1.39996.
https://www.scielo.sa.cr/scielo.php?pid=... ) reported the same mite genus causing damage to Grammatophyllum scriptum (Orchidaceae) in Costa Rica.

Orchids are ornamental plants of commercial interest worldwide and the introduction of specimens infested with phytophagous mites could cause irreversible loss of the culture. In addition, there is a risk of dispersing these mites to other ornamental plants, as observed in Ixora sp. Camellia sp. and Alpinia sp. (MIRANDA et al., 2007MIRANDA, L. C. et al. Brevipalpus mites Donnadieu (Prostigmata: Tenuipalpidae) associated with ornamental plants in Distrito Federal, Brazil. Neotropical Entomology, v.36, n.4, p.587-592, 2007. Available from: <Available from: https://www.scielo.br/scielo.php?pid=s1519-566x2007000400018&script=sci_arttext >. Accessed: May, 25, 2020. doi: 10.1590/S1519-566X2007000400018.
https://www.scielo.br/scielo.php?pid=s15... ), Gerbera sp. (SULZBACH et al., 2015SULZBACH, M. et al. 2015. Abundance and seasonality of two-spotted spider mite on gerbera cultivars. Ciência Rural, v.45, n.4, p.578-584, 2015. Available from: <Available from: https://www.scielo.br/scielo.php?pid=S0103-84782015000400578&script=sci_arttext&tlng=pt >. Accessed: Oct. 23, 2020. doi: 10.1590/0103-8478cr20131494.
https://www.scielo.br/scielo.php?pid=S01... ), Thunbergia sp., Anthurium sp., Trachelospermum sp. and Pelargonium sp. (KITAJIMA et al., 2010KITAJIMA, E. W. et al. An annotated list of ornamentals naturally found infected by Brevipalpus mite-transmitted viruses. Scientia Agricola, v.67, n.3, p.348-371, 2010. Available from: <Available from: https://www.scielo.br/scielo.php?pid=S0103-90162010000300014&script=sci_arttext >. Accessed: Mar. 18, 2020. doi: 10.1590/S0103-90162010000300014.
https://www.scielo.br/scielo.php?pid=S01... ). Therefore, tranportation of these plants may favor the dispersion of these hosts to other crops of economic importance in the state of Bahia, Brazil.

Target host plants of economic importance for these B. californicus mites are Anacardium occidentale L., Mangifera indica L., Spondias pinnata Kurz, Annona muricata L., Benincasa cerifera Savi, and Cucumis melo L. (CHILDERS et al., 2003CHILDERS, C. C. et al. Brevipalpus californicus, B. obovatus, B. phoenicis, and B. lewisi (Acari: Tenuipalpidae): a review of their biology, feeding injury and economic importance. Experimental & Applied Acarology, v.30, n.1-3, p.5, 2003. Available from: <Available from: https://link.springer.com/article/10.1023/B:APPA.0000006543.34042.b4 >. Accessed: Jan. 15, 2019.
https://link.springer.com/article/10.102... ). Moreover, B. californicus and B. yothersi have been associated to leprosis in Citrus sp. (GARCÍA-ESCAMILLA et al., 2018GARCÍA-ESCAMILLA, P. et al. Transmission of viruses associated with cytoplasmic and nuclear leprosis symptoms by Brevipalpus yothersi and B. californicus. Tropical Plant Pathology, v.43, n.1, p.69-77, 2018. Available from: <Available from: https://link.springer.com/article/10.1007/s40858-017-0195-8 >. Accessed: Jan. 15, 2020. doi: 10.1007/s40858-017-0195-8.
https://link.springer.com/article/10.100... ) and other plant species in different regions in the world. Similarly, T. orchidofilo can also adapt to other host plants, damaging crops.

This is the first report of Tenuipalpidae mites, B. californicus, B. yothersi, and T. orchidofilo causing damage to D. phalaenopsis in the state of Bahia, Brazil, reinforcing the importance of phytosanitary care to crops. Monitoring, maintenance, suitable facilities for plant requirements, as well as avoiding the acquisition of infested orchid plants are measures that should be taken into account by producers and phytosanitary defense agencies to mitigate losses caused by pests.

ACKNOWLEDGEMENTS

To professor Gilberto José de Moraes for the confirmation of species. The authors also thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) - Financial Code 001 - and to the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Process 305885/2017).

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