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No evidence of coconut stem bleeding disease transmission by bark beetles in Brazil

Não evidência de transmissão da doença resinose do coqueiro por escolitíneos no Brasil

ABSTRACT:

Stem bleeding disease, caused by the fungus Thielaviopsis paradoxa is one of the most important diseases of coconut palm Cocos nucifera worldwide and some insect species have been found in association with T. paradoxa infected coconut palms. The present research investigated whether coconut palm-infesting bark beetles (Coleoptera: Curculionidae: Scolytinae) could disseminate stem bleeding disease. Adult bark beetles collected from coconut palms presenting stem bleeding symptoms were inoculated in PDA culture medium. Results showed no germination of the fungus T. paradoxa from either cuticle or digestive tract of bark beetles. Thus, we found no evidence that bark beetles carry viable spores of T. paradoxa that could infect healthy coconut palms and disseminate stem bleeding disease.

Key words:
Cocos nucifera; Thielaviopsis paradoxa; Ceratocystis paradoxa; Chalara paradoxa; Scolytinae

RESUMO:

A resinose, causada pelo fungo Thielaviopsis paradoxa, é uma das doenças mais importantes do coqueiro Cocos nucifera em todo o mundo, e algumas espécies de insetos têm sido encontradas em associação com coqueiros infectados por T. paradoxa. O presente trabalho investigou se os besouros escolitíneos (Coleoptera: Curculionidae: Scolytinae) poderiam disseminar a resinose a partir de coqueiros infectados. Escolitíneos adultos coletados de coqueiros com sintomas da resinose foram inoculados em meio de cultura BDA. Os resultados mostraram que não houve germinação do fungo T. paradoxa da cutícula ou do trato digestivo dos insetos. Assim, não encontramos evidências de que besouros escolitíneos carreguem esporos viáveis de T. paradoxa que pudessem infectar coqueiros e disseminar a doença resinose.

Palavras-chave:
Cocos nucifera; Thielaviopsis paradoxa; Ceratocystis paradoxa; Chalara paradoxa; Scolytinae

Coconut palm (Cocos nucifera L.) originated in the Pacific and Indian Ocean basins (GUNN et al., 2011GUNN, B.F. et al. Independent origins of cultivated coconut (Cocos nucifera L.) in the Old World tropics. PLOS ONE, v.6, n.6, e21143, 2011. Available from: http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0021143>. Accessed: Feb. 14, 2017. doi: 10.1371/journal.pone.0021143.
http://journals.plos.org/plosone/article...
) and has been cultivated and disseminated by humans since remote times throughout the tropical lowlands of the world. The species has nowadays hundreds of uses as a source of food, drink, fiber, construction material, charcoal, and oil worldwide, being referred as one of the 20 most important crops upon which human life depends (HOWARD, 2001HOWARD, F.W. The animal class Insecta and the plant family Palmae. In: HOWARD, F.W. et al. Insects on palms. Wallingford: CAB International, 2001. Cap.1, p.1-32.; GUNN et al., 2011GUNN, B.F. et al. Independent origins of cultivated coconut (Cocos nucifera L.) in the Old World tropics. PLOS ONE, v.6, n.6, e21143, 2011. Available from: http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0021143>. Accessed: Feb. 14, 2017. doi: 10.1371/journal.pone.0021143.
http://journals.plos.org/plosone/article...
). Coconut plantations are attacked by several diseases, including the lethal stem bleeding disease, caused by the fungus Thielaviopsis paradoxa (De Seyn) Hölh (syn. Chalara paradoxa, Ceratocystis paradoxa). Stem bleeding symptoms include conspicuous reddish-brown stains coming from a hole or wound that seeps down the coconut stem.

Stem bleeding infections most commonly initiate from T. paradoxa spores or mycelium that survive on decaying plant litter and are spread from soils to coconut stems by splashing rain or irrigation water (NELSON, 2005NELSON, S. Stem bleeding of coconut palm. University of Hawaii, 2005. (Plant Disease; PD-30). Available from: http://www.ctahr.hawaii.edu/oc/freepubs/pdf/PD-30.pdf>. Accessed: Jan. 4, 2017.
http://www.ctahr.hawaii.edu/oc/freepubs/...
; WARWICK & TALAMINI, 2009WARWICK, D.R.N.; TALAMINI, V. Doenças e métodos de controle ajustados à baixa capacidade de investimento dos pequenos produtores rurais. In: CINTRA, F.L.D. et al. Fundamentos tecnológicos para a revitalização das áreas cultivadas com coqueiro gigante no Nordeste do Brasil. Aracaju: Embrapa Tabuleiros Costeiros, 2009. Cap.10, p.157-190.). However, in Venezuela, PARRA et al. (2003PARRA, D. Presencia de Thielaviopsis paradoxa De Seynes Höhn en el tubo digestivo de Rhynchophorus palmarum Linneo (Coleoptera: Curculionidae). Entomotropica, v.18, p.49-55, 2003. Available from: http://www.entomotropica.org/index.php/entomotropica/article/view/80/81>. Accessed: Jan. 4, 2017.
http://www.entomotropica.org/index.php/e...
) recovered T. paradoxa colonies from the alimentary canal of Rhynchophorus palmarum L. (Coleoptera: Curculionidae). WARWICK et al. (2009WARWICK, D.R.N. et al. Presença de Thielaviopsis paradoxa, agente causal da resinose do coqueiro, em coleópteros. In: FEIRA INTERNACIONAL DA FRUTICULTURA TROPICAL IRRIGADA - EXPOFRUIT, 14., 2009, Mossoró, RN, Resumos... CD-ROM.) also obtained T. paradoxa cultures from R. palmarum, Metamasius hemipterus (L.) (internally and externally) and Homalinotus coriaceus (Gyllenhal) (Coleoptera: Curculionidae) (externally) in Brazil, demonstrating the possible role of these important species of coconut borers in disseminating stem bleeding. Furthermore, MARAMOROSCH et al. (1972MARAMOROSCH, K. Platypus rugulosus (Platypodidae) and Xyleborus ferrugineus (Scolytidae) and certain diseases of coconut palms in Puerto Rico. Journal of the New York Entomological Society, v.80, p.238-240, 1972. Available from: http://www.biodiversitylibrary.org/item/206388#page/7/mode/1up>. Accessed: Jan. 5, 2017.
http://www.biodiversitylibrary.org/item/...
) reported Platypus rugulosus (Chapuis) (Coleoptera: Curculionidae: Platypodinae) and Xyleborus ferrugineus (Fabr.) (Coleoptera: Curculionidae: Scolytinae) infesting stems of coconut palms affected by stem bleeding in Puerto Rico, but a relationship between these insects and the disease could not be established.

In Brazil, coconut stem bleeding was first recorded in 2004 in the northeastern state of Sergipe (WARWICK & PASSOS, 2009WARWICK, D.R.N.; PASSOS, E.E.M. Outbreak of stem bleeding in coconuts caused by Thielaviopsis paradoxa in Sergipe, Brazil. Tropical Plant Pathology, v.34, p.175-177, 2009. Available from: http://www.scielo.br/pdf/tpp/v34n3/v34n3a07.pdf>. Accessed: Jan. 19, 2015.
http://www.scielo.br/pdf/tpp/v34n3/v34n3...
). Since then, this disease has spread to several other coconut producing states. As stem bleeding in Brazil is considered to be recent, several epidemiological aspects of this disease are still to be clarified in order to establish management programs. Recently, some unidentified species of bark beetles (Coleoptera: Curculionidae: Scolytinae) have been observed inhabiting stem bleeding-infected coconut palms in Sergipe (unpublished data). Since symbiotic interactions are prevalent in all bark beetle communities (HOFSTETTER et al., 2015HOFSTETTER, R.W. et al. Symbiotic associations of bark beetles. In: VEGA, F.E.; HOFSTETTER, R.W. Bark beetles: Biology and ecology of native and invasive species. Amsterdam: Elsevier Academic Press, 2015. Cap.6, p.209-245.) and adult insects belonging to this group present a wealth of fungi-carrying structures (HULCR et al., 2015HULCR, J. et al. Morphology, taxonomy, and phylogenetics of bark beetles. In: VEGA, F.E.; HOFSTETTER, R.W. Bark beetles: Biology and ecology of native and invasive species. Amsterdam: Elsevier Academic Press , 2015. Cap.2, p.41-84.), we investigated whether coconut palm-infesting bark beetles could disseminate stem bleeding disease.

Sections of bark and cortex were cut from ten coconut palms presenting stem bleeding symptoms (Figure 1A) in a commercial plantation located in Neópolis, Sergipe State (10º20’39.72”S 36º42’30.66”W, 125 meters above sea level), Brazil. Adult bark beetles (Figure 1B, C) found in these sections were collected and killed in freezer (0ºC) for two hours. In order to verify whether T. paradoxa could be carried either on the insect cuticle or in its digestive tract, beetles were: 1) straightly inoculated in Petri dishes containing PDA (potato-dextrose-agar) culture medium + chloramphenicol (500mg L-1), a broad spectrum bactericide; or 2) externally disinfected with 70% alcohol solution (2 seconds) and sodium hypochlorite (60 seconds), washed with distilled water, macerated, and subsequently inoculated in Petri dishes with PDA medium + chloramphenicol (500mg L-1). Dishes received three insects each and were kept in an incubation chamber at 25±1oC and daily evaluated, during seven days. The experiment consisted of a completely randomized design with 60 replications (insects) per treatment.

Figure 1
Stem bleeding symptoms in coconut palm (A) and adult bark beetle in lateral (B) and dorsal (C) views.Scale bars: 1mm.

Although this methodology has been successfully used for isolating T. paradoxa from plant tissue or insect body (WARWICK & PASSOS, 2009WARWICK, D.R.N.; PASSOS, E.E.M. Outbreak of stem bleeding in coconuts caused by Thielaviopsis paradoxa in Sergipe, Brazil. Tropical Plant Pathology, v.34, p.175-177, 2009. Available from: http://www.scielo.br/pdf/tpp/v34n3/v34n3a07.pdf>. Accessed: Jan. 19, 2015.
http://www.scielo.br/pdf/tpp/v34n3/v34n3...
; COSTA E CARVALHO et al., 2011aCOSTA E CARVALHO, R.R. et al. Efeito da temperatura no crescimento micelial, produção e germinação de esporos de Thielaviopsis paradoxa isolado de coqueiros em Sergipe. Scientia Plena, v.7, n.9, p.1-5, 2011a. Available from: https://www.scientiaplena.org.br/sp/article/view/399/178>. Accessed: Jan. 4, 2017.
https://www.scientiaplena.org.br/sp/arti...
, 2011bCOSTA E CARVALHO, R.R. et al. Longevidade de Thielaviopsis paradoxa, agente causal da resinose do coqueiro em Rhynchophorus palmarum. Scientia Plena , v.7, n.4, p.1-6, 2011b. Available from: https://www.scientiaplena.org.br/sp/article/view/139/141>. Accessed: Jan. 4, 2017.
https://www.scientiaplena.org.br/sp/arti...
), there was no T. paradoxa germination from either cuticle or digestive tract of bark beetles in our experiment. The fungus Aspergillus sp. grew in PDA medium but it was considered a contaminant. Bark beetles are known for attacking diseased, weakened or recently dead trees to which they are attracted, and for making galleries in the tree trunk inside which they develop, breed, and oviposit (RAFFA et al., 2015RAFFA, K.F. et al. Natural history and ecology of bark beetles. In: VEGA, F.E.; HOFSTETTER, R.W. Bark beetles: Biology and ecology of native and invasive species. Amsterdam: Elsevier Academic Press , 2015. Cap.1, p.1-40.). Owing to their habit, bark beetles were expected to acquire and transmit the fungus T. paradoxa while tunneling in stem bleeding-infected trees. However, it is possible that the insects we assayed had been attracted to the stem bleeding-infected coconut palms but they had not enough time to be contaminated by T. paradoxa spores and/or mycelia. Nevertheless, we assumed that T. paradoxa could not have colonized the entire stem and its galleries remained uninfected. Furthermore, most of bark beetles symbiotically-associated fungi may inhibit other fungi (HOFSTETTER et al., 2015HOFSTETTER, R.W. et al. Symbiotic associations of bark beetles. In: VEGA, F.E.; HOFSTETTER, R.W. Bark beetles: Biology and ecology of native and invasive species. Amsterdam: Elsevier Academic Press, 2015. Cap.6, p.209-245.), possibly explaining the reason why we did not obtain T. paradoxa from their bodies. Our study is not yet conclusive and further investigations should be carried out in order to elucidate the possible role of bark beetles in transmitting and disseminating T. paradoxa. In the light of current knowledge, we still have no evidence that bark beetles could carry viable spores of T. paradoxa that could infect healthy coconut palms and disseminate stem bleeding disease.

ACKNOWLEDGEMENTS:

Authors are grateful to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for fellowship for the second author; to H. Dantas - Coco Verde de Sergipe, for allowing us to collect insects in its coconut plantations; and to Francisco José dos Santos, from Embrapa Tabuleiros Costeiros, for helping us with bioassays.

REFERENCES:

  • COSTA E CARVALHO, R.R. et al. Efeito da temperatura no crescimento micelial, produção e germinação de esporos de Thielaviopsis paradoxa isolado de coqueiros em Sergipe. Scientia Plena, v.7, n.9, p.1-5, 2011a. Available from: https://www.scientiaplena.org.br/sp/article/view/399/178>. Accessed: Jan. 4, 2017.
    » https://www.scientiaplena.org.br/sp/article/view/399/178
  • COSTA E CARVALHO, R.R. et al. Longevidade de Thielaviopsis paradoxa, agente causal da resinose do coqueiro em Rhynchophorus palmarum Scientia Plena , v.7, n.4, p.1-6, 2011b. Available from: https://www.scientiaplena.org.br/sp/article/view/139/141>. Accessed: Jan. 4, 2017.
    » https://www.scientiaplena.org.br/sp/article/view/139/141
  • GUNN, B.F. et al. Independent origins of cultivated coconut (Cocos nucifera L.) in the Old World tropics. PLOS ONE, v.6, n.6, e21143, 2011. Available from: http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0021143>. Accessed: Feb. 14, 2017. doi: 10.1371/journal.pone.0021143.
    » https://doi.org/10.1371/journal.pone.0021143.» http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0021143
  • HOWARD, F.W. The animal class Insecta and the plant family Palmae. In: HOWARD, F.W. et al. Insects on palms. Wallingford: CAB International, 2001. Cap.1, p.1-32.
  • HOFSTETTER, R.W. et al. Symbiotic associations of bark beetles. In: VEGA, F.E.; HOFSTETTER, R.W. Bark beetles: Biology and ecology of native and invasive species. Amsterdam: Elsevier Academic Press, 2015. Cap.6, p.209-245.
  • HULCR, J. et al. Morphology, taxonomy, and phylogenetics of bark beetles. In: VEGA, F.E.; HOFSTETTER, R.W. Bark beetles: Biology and ecology of native and invasive species. Amsterdam: Elsevier Academic Press , 2015. Cap.2, p.41-84.
  • MARAMOROSCH, K. Platypus rugulosus (Platypodidae) and Xyleborus ferrugineus (Scolytidae) and certain diseases of coconut palms in Puerto Rico. Journal of the New York Entomological Society, v.80, p.238-240, 1972. Available from: http://www.biodiversitylibrary.org/item/206388#page/7/mode/1up>. Accessed: Jan. 5, 2017.
    » http://www.biodiversitylibrary.org/item/206388#page/7/mode/1up
  • NELSON, S. Stem bleeding of coconut palm. University of Hawaii, 2005. (Plant Disease; PD-30). Available from: http://www.ctahr.hawaii.edu/oc/freepubs/pdf/PD-30.pdf>. Accessed: Jan. 4, 2017.
    » http://www.ctahr.hawaii.edu/oc/freepubs/pdf/PD-30.pdf
  • PARRA, D. Presencia de Thielaviopsis paradoxa De Seynes Höhn en el tubo digestivo de Rhynchophorus palmarum Linneo (Coleoptera: Curculionidae). Entomotropica, v.18, p.49-55, 2003. Available from: http://www.entomotropica.org/index.php/entomotropica/article/view/80/81>. Accessed: Jan. 4, 2017.
    » http://www.entomotropica.org/index.php/entomotropica/article/view/80/81
  • RAFFA, K.F. et al. Natural history and ecology of bark beetles. In: VEGA, F.E.; HOFSTETTER, R.W. Bark beetles: Biology and ecology of native and invasive species. Amsterdam: Elsevier Academic Press , 2015. Cap.1, p.1-40.
  • WARWICK, D.R.N.; PASSOS, E.E.M. Outbreak of stem bleeding in coconuts caused by Thielaviopsis paradoxa in Sergipe, Brazil. Tropical Plant Pathology, v.34, p.175-177, 2009. Available from: http://www.scielo.br/pdf/tpp/v34n3/v34n3a07.pdf>. Accessed: Jan. 19, 2015.
    » http://www.scielo.br/pdf/tpp/v34n3/v34n3a07.pdf
  • WARWICK, D.R.N.; TALAMINI, V. Doenças e métodos de controle ajustados à baixa capacidade de investimento dos pequenos produtores rurais. In: CINTRA, F.L.D. et al. Fundamentos tecnológicos para a revitalização das áreas cultivadas com coqueiro gigante no Nordeste do Brasil. Aracaju: Embrapa Tabuleiros Costeiros, 2009. Cap.10, p.157-190.
  • WARWICK, D.R.N. et al. Presença de Thielaviopsis paradoxa, agente causal da resinose do coqueiro, em coleópteros. In: FEIRA INTERNACIONAL DA FRUTICULTURA TROPICAL IRRIGADA - EXPOFRUIT, 14., 2009, Mossoró, RN, Resumos... CD-ROM.
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    CR-2017-0329.R1

Publication Dates

  • Publication in this collection
    2018

History

  • Received
    18 May 2017
  • Accepted
    11 Jan 2018
  • Reviewed
    01 Mar 2018
Universidade Federal de Santa Maria Universidade Federal de Santa Maria, Centro de Ciências Rurais , 97105-900 Santa Maria RS Brazil , Tel.: +55 55 3220-8698 , Fax: +55 55 3220-8695 - Santa Maria - RS - Brazil
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