Cacao Diseases pp 511-566 | Cite as

Biological Control of Cacao Diseases

  • G. M. ten HoopenEmail author
  • Ulrike Krauss


This chapter discusses the advances in biological control of cacao diseases over the last 15 years. Most attention has been focused on biological control of frosty pod rot (Moniliophthora roreri), witches’ broom (Moniliophthora perniciosa) and black pod disease (Phytophthora spp.). Research on biocontrol of other diseases in the cacao phyllosphere or rhizosphere is scarce or in its infancy. There is, however, a steady increase in information regarding the factors influencing and the mechanisms underlying biological control of cacao diseases as well as practical aspects such as inoculum production, formulation and application. There has been a clear shift away from inundative approaches using epiphytic BCAs towards more classical biocontrol approaches using bacterial and fungal endophytes as well as vesicular arbuscular mycorrhiza. These have the advantage that they can permanently establish themselves in the cacao tree. Moreover, besides direct competition for space and nutrients, antibiosis and mycoparasitism, through induced resistance and growth promotion, endophytes have a larger arsenal of mechanisms through which they can help protect their host. Endophytic BCAs could thus provide more effective and sustainable disease control. Recent advances in our understanding of the mechanisms through which endophytic biocontrol agents can reduce pest and disease impact provide possibilities for innovative disease control strategies, including combination therapies together with natural or chemical products. Continued work on production, formulation and application is also necessary in order for biocontrol to become economically interesting. However, biological control will not become a stand-alone solution for disease control but should become part of integrated pest management strategies, with cultural management as a central and reinforcing pillar.


Biological Control Arbuscular Mycorrhizal Cacao Tree Trichoderma Isolate Biocontrol Efficacy 
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  1. Ackonnor, J. B. (1997, November). Preliminary studies on breeding and predation on Scymnus (Pullus) sp. and Hyperaspis egregia Mader on Planococcoides njalensis (Laing). In L. A. A. Ollennu, G. K. Owusu, & B. Padi (Eds.), Proceedings of the First International Cacao Pests and Diseases Seminar (pp. 238–241), Accra, Ghana.Google Scholar
  2. Adebola, M. O., & Amadi, J. E. (2010). Screening three Aspergillus species for antagonistic activities against the cacao black pod organism (Phytophthora palmivora). Agriculture and Biology Journal of North America, 1, 362–365.CrossRefGoogle Scholar
  3. Adebola, M. O., & Amadi, J. E. (2012). Studies on Penicillium digitatum, Botryodiploidia theobromae, Alternaria tenuis and Trichoderma harzianum for biocontrol of Phytophthora palmivora cacao black pod disease pathogen. American-Eurasian Journal of Agronomy, 5(2), 30–34.Google Scholar
  4. Adedeji, A. R., Odebode, A. C., & Agbeniyi, S. O. (2008). Bioassay of five Trichoderma strains against Phytophthora megakarya (cacao pod-rot) in Nigeria. Scientific Research and Essay, 3, 190–194.Google Scholar
  5. Agbeniyi, S. O., Adedeji, A. R., & Adeniyi, D. O. (2014). On-farm evaluation of Trichoderma asperellum on the suppression of Phytophthora megakarya causing pod rot of Theobromae cacao in Nigeria. British Journal of Applied Science & Technology, 4, 3153–3159.CrossRefGoogle Scholar
  6. Akrofi, A. Y., Govers, F., Awuah, R. T., & Raaijmakers, J. M. (2012). Exploiting microbial diversity in cacao ecosystems in Ghana to control Phytophthora pod rot disease. Global Advanced Research Journal of Agricultural Science, 1, 305–308.Google Scholar
  7. Allen, D. J., Lenné, J. M., & Waller, J. M. (1999). Pathogen biodiversity: Its nature, characterization and consequences. In D. Wood & J. M. Lenné (Eds.), Agrobiodiversity. characterization, utilization and management (pp. 123–153). Wallingford, UK: CABI Publishing.Google Scholar
  8. Altieri, M. A. (1999). The ecological role of biodiversity in agroecosystems. Agriculture, Ecosystems & Environment, 74, 19–31.CrossRefGoogle Scholar
  9. Ambang, Z., Ngoh Dooh, J. P., Essono, G., Bekolo, N., Chewachong, G., & Asseng, C. C. (2010). Effect of Thevetia peruviana seeds extract on in vitro growth of four strains of Phytophthora megakarya. Plant Omics Journal, 3, 70–76.Google Scholar
  10. Ameyaw, G. A., Dzahini-Obiatey, H. K., & Domfeh, O. (2014). Perspectives on cacao swollen shoot virus disease (CSSVD) management in Ghana. Crop Protection, 65, 64–70.CrossRefGoogle Scholar
  11. Amin, N., Salam, M., Junaid, M., Asman, & Baco, M. S. (2014). Isolation and identification of endophytic fungi from cacao plant resistant VSD M.05 and cacao plant susceptible VSD M.01 in South Sulawesi, Indonesia. International Journal of Current Microbiology and Applied Sciences, 3, 459–467.Google Scholar
  12. Aneja, M., Gianfagna, T. J., & Hebbar, P. K. (2005). Trichoderma harzianum produces nonanoic acid, an inhibitor of spore germination and mycelial growth of two cacao pathogens. Physiological and Molecular Plant Pathology, 67, 304–307.CrossRefGoogle Scholar
  13. Appiah, A. A., Flood, J., Archer, S. A., & Bridge, P. D. (2004). Molecular analysis of the major Phytophthora species on cacao. Plant Pathology, 53, 209–219.CrossRefGoogle Scholar
  14. Aragaki, M., & Uchida, J. (2001). Morphological distinctions between Phytophthora capsici and P. tropicalis sp. nov. Mycologia, 93, 137–145.CrossRefGoogle Scholar
  15. Argyle, T., George, A., ten Hoopen, G. M., & Krauss, U. (2003, October). Rhizosphere populations of antagonistic fungi of cacao (Theobroma cacao) clones tolerant or susceptible to Rosellinia root rot. In A. Y. Akrofi, J. B. Ackonor, & L. A. A. Ollennu (Eds.), 4th INCOPED Seminar (Oral and published paper, pp. 104–111), Accra, Ghana.Google Scholar
  16. Arnold, A. E., & Herre, E. A. (2003). Canopy cover and leaf age affect colonization by tropical endophytes: Ecological pattern and process in Theobroma cacao (Malvaceae). Mycologia, 95, 388–398.PubMedCrossRefGoogle Scholar
  17. Arnold, A. E., Maynard, Z., Gilbert, G. S., Coley, P. D., & Kursar, T. A. (2000). Are tropical fungal endophytes hyperdiverse? Ecology Letters, 3, 267–274.CrossRefGoogle Scholar
  18. Arnold, A. E., Mejía, L. C., Kyllo, D., Rojas, E. I., Maynard, Z., Robbins, N., et al. (2003). Fungal endophytes limit pathogen damage in a tropical tree. Proceedings of the National Academy of Sciences of the United States of America (PNAS), 100, 15649–15654.CrossRefGoogle Scholar
  19. Asante, S. K., & Ackonor, J. B. (1996). Natural enemies of cacao mealybugs (Annual Report, p. 158). Tafo-Akim, Ghana: Cacao Research Institute of Ghana.Google Scholar
  20. Avelino, J., ten Hoopen, G. M., & DeClerck, F. (2011). Ecological mechanisms for pest and disease control in coffee and cacao agroecosystems of the Neotropics. In B. Rapidel, F. DeClerck, J.-F. Le Coq, & J. Beer (Eds.), Ecosystems services from agriculture and agroforestry (p. 320). London, UK: Earthscan.Google Scholar
  21. Backman, P. A., & Sikora, R. A. (2008). Endophytes: An emerging tool for biological control. Biological Control, 46, 1–3.CrossRefGoogle Scholar
  22. Bae, H., Sicher, R. C., Kim, M. S., Kim, S.-H., Strem, M. D., Melnick, R. L., et al. (2009). The beneficial endophyte Trichoderma hamatum isolate Dis 219b promotes growth and delays the onset of the drought response in Theobroma cacao. Journal of Experimental Botany, 60, 3279–3295.PubMedCentralPubMedCrossRefGoogle Scholar
  23. Bagla, P. (2010). Hardy cotton-munching pests are latest blow to GM crops. Science, 327, 1439.PubMedCrossRefGoogle Scholar
  24. Bailey, B. A., Bae, H., Melnick, R., & Crozier, J. (2011). The endophytic Trichoderma hamatum isolate DIS 219b enhances seedling growth and delays the onset of drought stress in Theobroma cacao. In A. M. Pirttilä & A. C. Franks (Eds.), Endophytes of forest trees: Biology and applications (Forestry Sciences 80, pp. 157–172). Berlin, Germany: Springer Science.CrossRefGoogle Scholar
  25. Bailey, B. A., Bae, H., Strem, M. D., Crozier, J., Thomas, S. E., Samuels, G. J., et al. (2008). Antibiosis, mycoparasitism, and colonization success for endophytic Trichoderma isolates with biological control potential in Theobroma cacao. Biological Control, 46, 24–35.CrossRefGoogle Scholar
  26. Bailey, B. A., Bae, H., Strem, M. D., Roberts, D. P., Thomas, S. E., Samuels, G. J., et al. (2006). Fungal and plant gene expression during the colonization of cacao seedlings by endophytic isolates of four Trichoderma species. Planta, 224, 1449–1464.PubMedCrossRefGoogle Scholar
  27. Bailey, B. A., Strem, M. D., & Wood, D. (2009). Trichoderma species form endophytic associations within Theobroma cacao trichomes. Mycological Research, 11, 1365–1376.CrossRefGoogle Scholar
  28. Bailey, G. W., & White, J. L. (1970). Factors influencing the adsorption, desorption, and movement of pesticides in soil. Residue Reviews/Rückstands-Berichte, 32, 29–92.PubMedGoogle Scholar
  29. Barbosa, P. (Ed.). (1999). Conservation biological control (p. 396). San Diego, CA: Academic Press.Google Scholar
  30. Bastos, C. N. (1988). Resultados preliminaries sobre a eficacia de Trichoderma viride no controle da vassoura-de-bruxa (Crinipellis perniciosa) do cacaueiro. Fitopatologia Brasileira, 13, 340–342.Google Scholar
  31. Bastos, C. N. (1996a). Mycoparasitic nature of the antagonism between Trichoderma viride and Crinipellis perniciosa. Fitopatologia Brasileira, 21, 50–54.Google Scholar
  32. Bastos, C. N. (1996b). Potencial de Trichoderma viride no controle da vassourade-bruxa (Crinipellis perniciosa) do cacaueiro. Fitopatologia Brasileira, 21, 509–512.Google Scholar
  33. Bastos, C. N. (2012). Isolate of Trichoderma brevicompactum for the control of cacao witches broom disease: Preliminary results. Agrotropica, 24, 21–26.Google Scholar
  34. Bateman, R. (2004). The use of narrow-angle cone nozzles to spray cacao pods and other slender biological targets. Crop Protection, 23, 989–999. doi: 10.1016/j.cropro.2004.02.014.CrossRefGoogle Scholar
  35. Bateman, R. P., & Alves, R. T. (2000). Delivery system for mycoinsecticides using oil-based formulations (CABI Bioscience Biopesticide Programme, pp. 163–170). Ascot, Berks, UK: CABI.Google Scholar
  36. Bateman, R., Arias, D., Guerrero, R., Hebbar, P., & Súarez Capello, C. (2005a). Assessing the options for spray interventions to control the Moniliophthora disease complex of cacao in Ecuador. Instituto Nacional Autónomo de Investigaciones Agropecuarias (INIAP), Ecuador. Accessed January 23, 2015 from
  37. Bateman, R., Hidalgo, E., García, J., Arroyo, C., ten Hoopen, G. M., Adonijah, V., et al. (2005b). Application of chemical and biological agents for the management of frosty pod rot (Moniliophthora roreri) in Costa Rican cacao (Theobroma cacao). Annals of Applied Biology, 147, 129–138.CrossRefGoogle Scholar
  38. Begoude, B. A. D., Lahlali, R., Friel, D., Tondje, P. R., & Jijakli, M. H. (2007). Response surface methodology study of the combined effects of temperature, pH, and aw on the growth rate of Trichoderma asperellum. Journal of Applied Microbiology, 103, 845–854.PubMedCrossRefGoogle Scholar
  39. Benitez, T., Rincón, A. M., Limón, M. C., & Codón, A. C. (2004). Biocontrol mechanisms of Trichoderma strains. International Microbiology, 7, 249–260.PubMedGoogle Scholar
  40. Boa, E. R. (2000) Tree health and agroforestry (Final Technical Report, DIFD Crop Protection Programme, R7499, p. 89).Google Scholar
  41. Brimner, T. A., & Boland, G. J. (2003). A review of the non-target effects of fungi used to biologically control plant diseases. Agriculture, Ecosystems and Environment, 100, 3–16.CrossRefGoogle Scholar
  42. Butler, D. R. (1980). Dew and thermal lag: Measurements and an estimate of wetness duration on cocoa pods. Quarterly Journal of the Royal Meteorological Society, 106, 539–550.CrossRefGoogle Scholar
  43. Cadavid, S. (1995). Rosellinia in cacao. Cacao Growers’ Bulletin, 49, 52–59.Google Scholar
  44. Carroll, G. C. (1986). The biology of endophytism in plants with particular reference to woody perennials. In N. J. Fokkema & J. van den Heuvel (Eds.), Microbiology of the phylloplane (pp. 205–222). Cambridge, England: Cambridge University Press.Google Scholar
  45. Carroll, G. C. (1988). Fungal endophytes in stems and leaves: From latent pathogen to mutualistic symbiont. Ecology, 69, 2–9.CrossRefGoogle Scholar
  46. Carver, T. L. W., & Gurr, S. J. (2006). Filamentous fungi on plant surfaces. In M. Riederer & C. Müller (Eds.), Biology of the plant cuticle (Annual Plant Reviews, Vol. 23, p. 456). London, UK: Blackwell Publishing.Google Scholar
  47. Castro, B. L. (1995). Antagonismo de algunos aislamientos de Trichoderma koningii, originados en suelo Colombiano contra Rosellinia bunodes, Sclerotinia sclerotiorum y Pythium ultimum. Fitopatologia Colombiana, 19, 7–18.Google Scholar
  48. Chet, I., Harman, G. E., & Baker, R. (1981). Trichoderma hamatum: Its hyphal interactions with 319 Rhizoctonia solani and Pythium spp. Microbial Ecology, 7, 29–38.PubMedCrossRefGoogle Scholar
  49. Chulan, A. H., & Martin, K. (1992). The vesicular-arbuscular (VA) mycorrhiza and its effects on growth of vegetatively propagated Theobroma cacao L. Plant Soil, 144, 227–233.CrossRefGoogle Scholar
  50. Chulan, A. H., & Ragu, P. (1986). Growth response of Theobroma cacao L. seedlings to inoculation with vesicular-arbuscular mycorrhizal fungi. Plant Soil, 96, 279–285.CrossRefGoogle Scholar
  51. Cock, M. W., van Lenteren, J., Brodeur, J., Barratt, B. P., Bigler, F., Bolckmans, K., et al. (2009). The use and exchange of biological control agents for food and agriculture (Commission on Genetic Resources for Food and Agriculture, FAO Background Study Paper No. 47).
  52. Coll, M. (2009). Conservation biological control and the management of biological control services: Are they the same? Phytoparasitica, 37, 205–208.CrossRefGoogle Scholar
  53. Cook, R. J., Bruckart, W. L., Coulson, J. R., Goettel, M. S., Humber, R. A., Lumsden, R. D., et al. (1996). Safety of microorganisms intended for pest and disease control: A framework for scientific evaluation. Biological Control, 7, 333–351.CrossRefGoogle Scholar
  54. Costa, J. C. B., & Bezerra, J. L. (1994). Antagonismo de isolados de Cladosporium, Gliocladium, Penicillium, Streptomyces e Trichoderma sobre Crinipellis perniciosa na região cacueira da Bahia. In 4th Siconbiol Simposio de controle biológico de doenças de Plantas Anais: Sessão de Pôsteres. 59 (abstract only).Google Scholar
  55. Costa, J. C. B., Bezerra, J. L., & Cazorla, I. M. (1996). Controle biológico da vassoura-de-bruxa do cacueiro na Bahia com Trichoderma polysporum. Fitopatologia Brasileira, 21 (suppl.), 397 (abstract only).Google Scholar
  56. Coulibaly, O., Mbila, D., Sonwa, D. J., Adesina, A., & Bakala, J. (2002). Responding to economic crisis in sub-Saharan Africa: New farmer-developed pest management strategies in cacao-based plantation in Southern Cameroon. Integrated Pest Management Reviews, 7, 165–172.CrossRefGoogle Scholar
  57. Crowder, D. W., & Harwood, J. D. (2014). Promoting biological control in a rapidly changing world. Biological Control, 75, 1–7.CrossRefGoogle Scholar
  58. Crozier, J., Arroyo, C., Morales, H., Melnick, R. L., Strem, M. D., Vinyard, B. T., et al. (2015). The influence of formulation on Trichoderma biological activity and frosty pod rot management in Theobroma cacao. Plant Pathology. doi: 10.1111/ppa.12383.Google Scholar
  59. Crozier, J., Thomas, S. E., Aime, M. C., Evans, H. C., & Holmes, K. A. (2006). Molecular characterization of fungal endophytic morphospecies isolates from stems and pods of Theobroma cacao. Plant Pathology, 55, 783–791.CrossRefGoogle Scholar
  60. Cuenca, G., Herrera, R., & Meneses, E. (1990). Effects of VA mycorrhiza on the growth of cacao seedlings under nursery conditions in Venezuela. Plant Soil, 126, 71–78.CrossRefGoogle Scholar
  61. Cuervo-Parra, J. A., Sanchez-Lopez, V., Romero-Cortes, T., & Ramírez-Lepe, M. (2014). Hypocrea Trichoderma viridescens ITV43 with potential for biocontrol of Moniliophthora roreri Cif & Par, Phytophthora megasperma and Phytophthora capsici. African Journal of Microbiology Research, 8, 1704–1712.CrossRefGoogle Scholar
  62. de Marco, J. L., & Felix, C. R. (2002). Characterization of a protease produced by a Trichoderma harzianum isolate which controls cacao plant witches’ broom disease. BMC Biochemistry.
  63. de Souza, J. T., Bailey, B. A., Pomella, A. W. V., Erbe, E. F., Murphy, C. A., Bae, H., et al. (2008). Colonization of cacao seedlings by Trichoderma stromaticum, a mycoparasite of the witches’ broom pathogen, and its influence on plant growth and resistance. Biological Control, 46, 36–45.CrossRefGoogle Scholar
  64. de Souza, J. T., Pomella, A. W. V., Bowers, J. H., Pirovani, C. P., Loguercio, L. L., & Hebbar, P. K. (2006). Genetic and biological diversity of Trichoderma stromaticum, a mycoparasite of the cacao witches’ broom pathogen. Phytopathology, 96, 61–67.PubMedCrossRefGoogle Scholar
  65. Deberdt, P., Mfegue, C. V., Tondje, P. R., Bon, M. C., Ducamp, M., Hurard, C., et al. (2008). Impact of environmental factors, chemical fungicide and biological control on cacao pod production dynamics and black pod disease (Phytophthora megakarya) in Cameroon. Biological Control, 44, 149–159.CrossRefGoogle Scholar
  66. Dik, A. J., Koning, G., & Kohl, J. (1999). Evaluation of microbial antagonists for biological control of Botrytis cinerea stem infection in cucumber and tomato. European Journal of Plant Pathology, 105, 115–122.CrossRefGoogle Scholar
  67. Druzhinina, I. S., Seidl-Seiboth, V., Herrera-Estrella, A., Horwitz, B. A., Kenerley, C. M., Monte, E., et al. (2011). Trichoderma: The genomics of opportunistic success. Nature Reviews Microbiology, 9, 749–759.PubMedCrossRefGoogle Scholar
  68. Durrant, W. E., & Dong, X. (2004). Systemic acquired resistance. Annual Review of Phytopathology, 42, 185–209.PubMedCrossRefGoogle Scholar
  69. Efombagn, M. I. B., Nyassé, S., Bieysse, D., & Sounigo, O. (2013). Analysis of the resistance to Phytophthora pod rot within local selections of cacao (Theobroma cacao L.) for breeding purpose in Cameroon. Journal of Plant Breeding and Crop Science, 4, 111–119.CrossRefGoogle Scholar
  70. Eilenberg, J., Hajek, A., & Lomer, C. (2001). Suggestions for unifying the terminology in biological control. BioControl, 46, 387–400.CrossRefGoogle Scholar
  71. Elad, Y., Zimand, G., Zaqs, Y., Zuriel, S., & Chet, I. (1993). Use of Trichoderma harzianum in combination or alternation with fungicides to control cucumber grey mold (Botrytis cinerea) under commercial greenhouse conditions. Plant Pathology, 42, 324–332.CrossRefGoogle Scholar
  72. Evans, H. C. (1981a). Witches’ broom disease: A case study’. Cocoa Growers’ Bulletin, 5–19.Google Scholar
  73. Evans, H. C. (1981b). Pod rot of cacao caused by Moniliophthora (Monilia) roreri (Phytopathological Papers 24). Kew: CAB Commonwealth Mycological Institute.Google Scholar
  74. Evans, H. C. (1998). Disease and sustainability in the cocoa agroecosystem. In First International Workshop on Sustainable Cocoa Growing. Panama City: Smithsonian Tropical Research Institute, Smithsonian Migratory Bird Center.Google Scholar
  75. Evans, H. C. (1999). Classical biological control. In P. Hebbar & U. Krauss (Eds.), Research methodology in biocontrol of plant diseases with special reference to fungal diseases in cacao (pp. 29–43). Turrialba: CATIE.Google Scholar
  76. Evans, H. C., Edwards, D. F., & Rodriguez, M. (1977). Research on cacao diseases in Ecuador: Past and Present. Pest Abstracts and News Summaries (PANS), 23, 68–80.Google Scholar
  77. Evans, H. C., Holmes, K. A., & Thomas, S. E. (2003a). Endophytes and mycoparasites associated with an indigenous forest tree, Theobroma gileri, in Ecuador and a preliminary assessment of their potential as biocontrol agents of cacao diseases. Mycological Progress, 2, 149–160.CrossRefGoogle Scholar
  78. Evans, H. C., Holmes, K. A., & Thomas, S. E. (2003b, October). Crowd control: Natural enemy biodiversity in a coevolved forest host-pathosystem and its potential as a source of novel biocontrol agents for frosty pod rot of cacao. In A. Y. Akrofi, J. B. Ackonor, & L. A. A. Ollennu (Eds.), Proceedings of INCOPED 4th International Seminar on Cacao Pest and Diseases (pp. 126–135). Accra, Ghana: Ghana Cacao Board.Google Scholar
  79. Everett, K. R., Vanneste, J. L., Hallett, I. C., & Walter, M. (2005). Ecological alternatives for disease management of fruit rot pathogens. New Zealand Plant Protection, 58, 55–61.Google Scholar
  80. Falcäo, L. L., Silva-Werneck, J. O., Vilarinho, B. R., da Silva, J. P., Pomella, A. W. V., & Marcellino, L. H. (2014). Antimicrobial and plant growth-promoting properties of the cacao endophyte Bacillus subtilis ALB629. Journal of Applied Microbiology, 116, 1584–1592.PubMedCrossRefGoogle Scholar
  81. Fitt, B. D. L., McCartney, H. A., & Walklate, P. J. (1989). The role of rain dispersal of pathogen inoculum. Annual Review of Phytopathology, 27, 241–270.CrossRefGoogle Scholar
  82. Flood, J., Guest, D., Holmes, K. A., Keane, P., Padi, B., & Sulistyowati, E. (2004). Cocoa under attack. In J. Flood & R. Murphy (Eds.), Cocoa futures (p. 164). Chincina, CO: CABI-FEDERACAFE.Google Scholar
  83. Flores, D., Ramírez, C., & Galindo, J. J. (1994). Ultrastructure of cacao fruits (Theobroma cacao) of cultivars with contrasting susceptibility to Moniliophthora roreri. Revista Biología Tropical, 42, 29–37.Google Scholar
  84. Freeman, S., & Rodriguez, R. J. (1993). Genetic conversion of a fungal plant pathogen to a nonpathogenic, endophytic mutualist. Science, 260, 75–78.PubMedCrossRefGoogle Scholar
  85. Gidoin, C., Babin, R., Bagny Beilhe, L., Cilas, C., ten Hoopen, G. M., & Ngo Bieng, M. A. (2014). Tree spatial structure, host composition and resource availability influence mirid density or black pod prevalence in cacao agroforests in Cameroon. PLoS One, 9(10), e109405.PubMedCentralPubMedCrossRefGoogle Scholar
  86. Gockowski, J., Tchatat, M., Dondjang, J.-P., Hietet, G., & Fouda, T. (2010). An empirical analysis of the biodiversity and economic returns to cacao agroforests in Southern Cameroon. Journal of Sustainable Forestry, 29, 637–670.CrossRefGoogle Scholar
  87. Gorentz, A. M. (1974). Chemical control of black pod: Fungicides. In P. H. Gregory (Ed.), Phytophthora disease of cacao (pp. 235–258). London, UK: Longman.Google Scholar
  88. Graham, J. H. (2001). What do root pathogens see in mycorrhizas? New Phytology, 149, 357–359.CrossRefGoogle Scholar
  89. Guest, D. (2007). Black pod: Diverse pathogens with global impact on cacao yield. Phytopathology, 97, 1650–1653.PubMedCrossRefGoogle Scholar
  90. Guest, D., & Keane, P. (2007). Vascular-streak dieback: A new encounter disease of cacao in Papua New Guinea and Southeast Asia caused by the obligate basidiomycete Oncobasidium theobromae. Phytopathology, 97, 1654–1657.PubMedCrossRefGoogle Scholar
  91. Hanada, R. E., de Souza, T. J., Pomella, A. W. V., Hebbar, P. K., Pereira, J. O., Ismaiel, A., et al. (2008). Trichoderma martiale sp. Nov. a new endophyte from sapwood of Theobroma cacao with a potential for biological control. Mycological Research, 112, 1335–1343.PubMedCrossRefGoogle Scholar
  92. Hanada, R. E., Pomella, A. W. V., Costa, H. S., Bezerra, J. L., Loguercio, L. L., & Pereira, J. O. (2010). Endophytic fungal diversity in Theobroma cacao (cacao) and T. grandiflorum (cupuaçu) trees and their potential for growth promotion and biocontrol of black-pod disease. Fungal Biology, 114, 901–910.PubMedCrossRefGoogle Scholar
  93. Hanada, R. E., Pomella, A. W. V., Soberanis, W., Loguercio, L. L., & Pereira, J. O. (2009). Biocontrol potential of Trichoderma martiale against the black-pod disease (Phytophthora palmivora) of cacao. Biological Control, 50, 143–149.CrossRefGoogle Scholar
  94. Hannusch, D. J., & Boland, G. J. (1996a). Influence of air temperature and relative humidity and biological control agents on grey mold of bean. European Journal of Plant Pathology, 102, 133–142.CrossRefGoogle Scholar
  95. Hannusch, D. J., & Boland, G. J. (1996b). Influence of air temperature and relative humidity on biological control of white mold of bean (Sclerotinia sclerotiorum). Phytopathology, 86, 156–162.CrossRefGoogle Scholar
  96. Harman, G. E., Howell, C. R., Viterbo, A., Chet, I., & Lorito, M. (2004). Trichoderma species - opportunistic, avirulent plant symbionts. Nature Reviews Microbiology, 2, 43–56.PubMedCrossRefGoogle Scholar
  97. Harman, G. E., & Kubicek, C. P. (1998). Trichoderma and Gliocladium (Enzymes, biological control and commercial applications, Vol. 2, p. 393). London, UK: Taylor and Francis.Google Scholar
  98. Hermosa, R., Belen Rubio, M., Cardoza, R. E., Nicolas, C., Monte, E., & Gutierrez, S. (2013). The contribution of Trichoderma to balancing the costs of plant growth and defense. International Microbiology, 16, 69–80.PubMedGoogle Scholar
  99. Herre, E. A., Mejía, L. C., Kyllo, D. A., Rojas, E., Maynard, Z., Butler, A., et al. (2007). Ecological implications of anti-pathogen effects of tropical fungal endophytes and mycorrhizae. Ecology, 88, 550–558.PubMedCrossRefGoogle Scholar
  100. Hidalgo, E., Bateman, R., Krauss, U., ten Hoopen, G. M., & Martínez, A. (2003). A field investigation into delivery systems for agents to control Moniliophthora roreri. European Journal of Plant Pathology, 109, 953–961.CrossRefGoogle Scholar
  101. Hjeljord, L., & Tronsmo, A. (1998). Trichoderma and Gliocladium in biological control: an overview. In G. E. Harman & C. P. Kubicek (Eds.), Trichoderma and Gliocladium (Enzymes, Biological Control and Commercial Applications, Vol. 2, p. 393). London, UK: Taylor and Francis.Google Scholar
  102. Hokkanen, H. M. T., & Lynch, J. M. (1995). Biological control: Benefits and risks. Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
  103. Holmes, K. A., Evans, H. C., Wayne, S., & Smith, J. (2003). Irvingia, a forest host of the cocoa black-pod pathogen, Phytophthora megakarya, in Cameroon. Plant Pathology, 52, 486–490.CrossRefGoogle Scholar
  104. Holmes, K. A., Krauss, U., Samuels, G., Bateman, R. P., Thomas, S. E., Crozier, J., et al. (2006, October). Trichoderma ovalisporum: A potential biocontrol agent of frosty pod rot (Moniliophthora roreri) (Vol. II, pp. 1001–1006). In Proceedings of 15th International Cacao Research Conference, San José, Costa Rica.Google Scholar
  105. Holmes, K. A., Schroers, H.-J., Thomas, S. E., Evans, H. C., & Samuels, G. J. (2004). Taxonomy and biocontrol potential of a new species of Trichoderma from the Amazon basin of South America. Mycological Progress, 3, 199–210.CrossRefGoogle Scholar
  106. Hughes, J. d’A., & Ollenu, L. A. A. (1994). Mild strain protection of cacao in Ghana against cacao swollen shoot virus – a review. Plant Pathology, 43, 442–457.Google Scholar
  107. Iritié, M. S., Bi, Z., Tié, B. T., Zirihi Guédé, N., Kouadjo Zaka, C. G., Fossou Kouakou, R., et al. (2012). Arbuscular mycorhhizal fungi associated with Theobroma cacao L. in the region of Yamoussoukro (Côte d’Ivoire). African Journal of Agricultural Research, 7, 993–1001.Google Scholar
  108. Jeffries, P., & Barea, J. M. (2012). Arbuscular mycorrhiza: A key component of sustainable plant-soil ecosystems. In B. Hock (Ed.), The Mycota. A comprehensive treatise on fungi as experimental systems for basic and applied research (pp. 51–75). Berlin, Germany: Springer.Google Scholar
  109. Kebe, I. B., Mpika, J., N’Guessan, K. F., Hebbar, P. K., Samuels, G. S., & Ake, S. (2009). Isolement et identification de microorganismes indigènes de cacaoyères en Côte d’Ivoire et mise en évidence de leurs effets antagonistes vis-àvis de Phytophthora palmivora, agent de la pourriture brune des cabosses. Sciences & Nature, 6, 71–82.CrossRefGoogle Scholar
  110. Klapwijk, J. (2011). The use and exchange of biological control agents for food and agriculture (FAO background study paper 47).
  111. Kloepper, J. W., Tuzun, S., & Kuć, J. (1992). Proposed definitions related to induced disease resistance. Biocontrol Science and Technology, 2, 349–351.CrossRefGoogle Scholar
  112. Konam, J. K., & Guest, D. I. (2002). Leaf litter mulch reduces the survival of Phytophthora palmivora under cacao trees in Papua New Guinea. Australasian Journal of Plant Pathology, 31, 381–383.CrossRefGoogle Scholar
  113. Koranteng, S. L., & Awuah, R. T. (2011). Biological suppression of black pod lesion development on detached cocoa pods. African Journal of Agricultural Research, 6, 67–72.Google Scholar
  114. Krauss, U. (1994). Spore movement of Mucor hiemalis in the rhizosphere of groundnut in natural field conditions. In T. Martin (Ed.), Poster and published paper: Seed Treatment - Progress and Prospects (pp. 339–344). Farnham, UK: British Crop Protection Council.Google Scholar
  115. Krauss, U. (2004). Diseases in tropical agroforestry landscapes – The role of biodiversity. In G. Schroth, G. A. B. Fonseca, C. A. Harvey, C. Gascon, H. F. Vasconcelos, & A. M. N. Izac (Eds.), Agroforestry and biological conservation in tropical landscapes (pp. 397–412). Washington, DC: Island Press.Google Scholar
  116. Krauss, U., & Deacon, J. W. (1994). Water-facilitated transport of a pimaricin-resistant strain of Mucor hiemalis in the rhizosphere of groundnut (Arachis hypogaea L.) in a Malawian luvisol. Soil Biology & Biochemistry, 26, 977–985.CrossRefGoogle Scholar
  117. Krauss, U., Hidalgo, E., Bateman, R., Adonijah, V., Arroyo, C., García, J., et al. (2010). Improving the formulation and timing of application of chemical and endophytic biocontrol agents against frosty pod rot (Moniliophthora roreri) in cacao (Theobroma cacao). Biological Control, 54, 230–240.CrossRefGoogle Scholar
  118. Krauss, U., Martínez, A., Hidalgo, E., ten Hoopen, G. M., & Arroyo, C. (2002). Two-step liquid/solid state mass production of Clonostachys rosea. Mycological Research, 106, 1449–1454.CrossRefGoogle Scholar
  119. Krauss, U., & Soberanis, W. (2001a). Biocontrol of cacao pod diseases with mycoparasite mixtures. Biological Control, 22, 149–158.CrossRefGoogle Scholar
  120. Krauss, U., & Soberanis, W. (2001b). Rehabilitation of diseased cacao fields in Peru through shade regulation and timing of biocontrol measures. Agroforestry Systems, 53, 179–184.CrossRefGoogle Scholar
  121. Krauss, U., & Soberanis, W. (2002). Effect of fertilization and biocontrol application frequency on cacao pod diseases. Biological Control, 24, 82–89.CrossRefGoogle Scholar
  122. Krauss, U., ten Hoopen, G. M., Hidalgo, E., Martínez, A., Arroyo, C., García, J., et al. (2003). Manejo integrado de la moniliasis (Moniliophthora roreri) del cacao (Theobroma cacao) en Talamanca, Costa Rica. Revista Agroforestería en las Americas, 10, 52–58.Google Scholar
  123. Krauss, U., ten Hoopen, G. M., Hidalgo, E., Martínez, A., Stirrup, T., Arroyo, C., et al. (2006). The effect of cane molasses amendment on biocontrol of frosty pod rot (Moniliophthora roreri) and black pod (Phytophthora spp.) of cacao (Theobroma cacao) in Panama. Biological Control, 39, 232–239.CrossRefGoogle Scholar
  124. Krauss, U., ten Hoopen, M., Martínez, A., Rees, R., Stirrup, T., Argyle, T., et al. (2013). Mycoparasitism by Clonostachys byssicola and Clonostachys rosea on Trichoderma spp. and implication for the design of mixed biocontrol agents. Biological Control, 67, 317–327.CrossRefGoogle Scholar
  125. Last, F. T. (1955). Seasonal incidence of Sporobolomyces on cereal leaves. Transactions of the British Mycological Society, 38, 221–239.CrossRefGoogle Scholar
  126. Leach, A. W., Mumford, J. D., & Krauss, U. (2002). Modelling Moniliophthora roreri in Costa Rica. Crop Protection, 21, 317–326.CrossRefGoogle Scholar
  127. Leite, H. A. C., Silva, A. B., Gomes, F. P., Gramacho, K. P., Faria, J. C., de Souza, J. T., et al. (2013). Bacillus subtilis and Enterobacter cloacae endophytes from healthy Theobroma cacao L. trees can systematically colonize seedlings and promote growth. Applied Microbiology and Biotechnology, 97, 2639–2651.PubMedCrossRefGoogle Scholar
  128. Leveau, J. H. J. (2006). Microbial communities in the phyllosphere. In M. Riederer & C. Müller (Eds.), Biology of the plant cuticle (Annual Plant Reviews, Vol. 23, p. 456). London, UK: Blackwell Publishing.Google Scholar
  129. Lindow, S. E., & Andersen, G. L. (1996). Influence of immigration on epiphytic bacterial populations on Naval orange leaves. Applied and Environmental Microbiology, 62, 2978–2987.PubMedCentralPubMedGoogle Scholar
  130. Loguercio, L. L., de Carvalho, A. C., Niella, G. R., de Souza, J. T., & Pomella, A. W. V. (2009a). Selection of Trichoderma stromaticum isolates for efficient biological control of witches’ broom disease in cacao. Biological Control, 51, 130–139.CrossRefGoogle Scholar
  131. Loguercio, L. L., Santos, L. S., Niella, G. R., Miranda, R. A. C., de Souza, J. T., Collins, R. T., et al. (2009b). Canopy-microclimate effects on the antagonism between Trichoderma stromaticum and Moniliophthora perniciosa in shaded cacao. Plant Pathology, 58, 1104–1115.CrossRefGoogle Scholar
  132. Lutz, M. P., Wenger, S., Maurhofer, M., Défago, G., & Duffy, B. (2004). Signaling between bacterial and fungal biocontrol agents in a strain mixture. FEMS Microbiology Ecology, 48, 447–455.PubMedCrossRefGoogle Scholar
  133. Macagnan, D., Romeiro, R. S., de Souza, J. T., & Pomella, A. W. V. (2006). Isolation of actinomycetes and endospore-forming bacteria from the cacao pod surface and their antagonistic activity against the witches’ broom and black pod pathogens. Phytoparasitica, 34, 122–132.CrossRefGoogle Scholar
  134. Mbarga, J. B., Begoude, B. A. D., Ambang, Z., Meboma, M., Kuate, J., Schiffers, B., et al. (2014). A new oil-based formulation of Trichoderma asperellum for the biological control of cacao black pod disease caused by Phytophthora megakarya. Biological Control, 77, 15–22.CrossRefGoogle Scholar
  135. Mbarga, J. B., ten Hoopen, G. M., Kuate, J., Adiobo, A., Ngonkeu, M. E. L., Ambang, Z., et al. (2012). Trichoderma asperellum: a potential biocontrol agent for Pythium myriotylum, causal agent of cocoyam (Xanthosoma sagittifolium) root rot disease. Crop Protection, 36, 18–22.CrossRefGoogle Scholar
  136. Medeiros, F. H. V., Pomella, A. W. V., de Souza, J. T., Niella, G. R., Valle, R., Bateman, R. P. B., et al. (2010). A novel, integrated method for management of witches’ broom disease in cacao in Bahia, Brazil. Crop Protection, 29, 704–711.CrossRefGoogle Scholar
  137. Mejía, L. C., Herre, E. A., Sparks, J. P., Winter, K., García, M. N., Van Bael, S. A., et al. (2014). Pervasive effects of a dominant foliar endophytic fungus on host genetic and phenotypic expression in a tropical tree. Frontiers in Microbiology, 5, 1–16.Google Scholar
  138. Mejía, L. C., Rojas, E. I., Maynard, Z., Van Bael, S., Arnold, A. E., Hebbar, P., et al. (2008). Endophytic fungi as biocontrol agents of Theobroma cacao pathogens. Biological Control, 46, 4–14.CrossRefGoogle Scholar
  139. Melnick, R. L., Suárez, C., Bailey, B. A., & Backman, P. A. (2011). Isolation of endophytic endospore-forming bacteria from Theobroma cacao as potential biological control agents of cacao diseases. Biological Control, 57, 236–245.CrossRefGoogle Scholar
  140. Melnick, R. L., Zidack, N. K., Bailey, B. A., Maximova, S. N., Guiltinan, M., & Backman, P. A. (2008). Bacterial endophytes: Bacillus spp. from annual crops as potential biological control agents of black pod rot of cacao. Biological Control, 46, 46–56.CrossRefGoogle Scholar
  141. Mendoza-Garcia, R. A., ten Hoopen, G. M., Kass, D. C. J., Sánchez Garita, V. A., & Krauss, U. (2003). Evaluation of mycoparasites as biocontrol agents of Rosellinia root rot in Cacao. Biological Control, 27, 210–227.CrossRefGoogle Scholar
  142. Merchán, V. M. (1993). Experiencias en el manejo de Rosellinia. Ascolfi Informa, 19, 23–24.Google Scholar
  143. Mfegue, C. V. (2012). Origine et mécanismes de dispersion des populations de Phytophthora megakarya, pathogène du cacaoyer au Cameroun. PhD thesis, SupAgro, Montpellier, France, 185p.Google Scholar
  144. Millennium Ecosystems Assessment. (2005). Ecosystems and human well-being. Synthesis (p. 115). Washington, DC: Island Press.Google Scholar
  145. Monteith, J. L., & Butler, D. R. (1979). Dew and thermal lag: Model for cocoa pods. Quarterly Journal of the Royal Meteorological Society, 105, 207–215.CrossRefGoogle Scholar
  146. Mpika, J., Kébé, I. B., Issali, A. E., N’Guessan, F. K., Druzhinina, S., Komon-Zélazowska, M., et al. (2009). Antagonist potential of Trichoderma indigenous isolates for biological control of Phytophthora palmivora the causative agent of black pod disease on cacao (Theobroma cacao L.) in Côte d’Ivoire. African Journal of Biotechnology, 8, 5280–5293.Google Scholar
  147. Najár, T., & Thomas, S. (2001). El efecto de los microorganismos eficaces en la suppression del hongo Moniliphthora roreri bajo condiciones del laboratorio y campo con inoculación artificial. Tesis de Licenciatura en Ingeniería Agrónoma (p. 60). Guápiles, Costa Rica: EARTH.Google Scholar
  148. Ndoumbe-Nkeng, M., Cilas, C., Nyemb, E., Nyassé, S., Bieysse, D., Flori, A., et al. (2004). Impact of removing diseased pods on cacao black pod caused by Phytophthora megakarya and on cacao production in Cameroon. Crop Protection, 5, 415–424.CrossRefGoogle Scholar
  149. Ndoungue Djeumekop, M. M., Tchana, T., Nana, W., Techou, Z., Petchayo, S., Fontem, A. D., et al. (2012, October). Effet des traitements du sol sur le développement de l’épidémie de la pourriture brune (Phytophthora megakarya) du cacaoyer au Cameroun. Poster presentation at the 17th International Cacao Research Conference, Yaoundé, Cameroon.Google Scholar
  150. Ngo Bieng, M. A., Gidoin, C., Avelino, J., Cilas, C., Deheuvels, O., & Wery, J. (2013). Diversity and spatial clustering of shade trees affect cacao yield and pathogen pressure in Costa Rican agroforests. Basic and Applied Ecology, 14, 329–336. doi: 10.1016/j.baae.2013.03.003.CrossRefGoogle Scholar
  151. Nyadanu, D., Akromah, R., Adomako, B., Awuah, R. T., Kwoseh, C., Dzahini-Obiatey, H., et al. (2012). Effects of cacao swollen shoot virus infection on foliar resistance to P. palmivora and P. megakarya and its implications in selection and breeding against black pod disease. International Journal of Plant Pathology, 3, 45–55.CrossRefGoogle Scholar
  152. Nyassé, S., Grivet, L., Risterucci, A. M., Blaha, G., Berry, D., Lanaud, C., et al. (1999). Diversity of Phytophthora megakarya in Central and West Africa revealed by isozyme and RAPD markers. Mycological Research, 103, 1225–1234.CrossRefGoogle Scholar
  153. Okumoto, S., Ramón, J., Moya, F., Najar, T., Thomas, S., Palacios, R., et al. (2002, August). Aplicaciones de EM5 para el control de la enfermedad de monilia (Moniliophthora roreri) en la producción de cacao orgánico (p. 46). Proceedings of the 14th IFOAM Organic World Congress, “Cultivating Communities” Victoria Conference Centre CA. Ottawa: Ottawa Canadian Organic Growers (COG).
  154. Omacini, M., Eggers, T., Bonkowski, M., Gange, A. C., & Jones, T. H. (2006). Leaf endophytes affect mycorrhizal status and growth of co-infected and neighbouring plants. Functional Ecology, 20, 226–232.CrossRefGoogle Scholar
  155. Opoku, I. Y., Appiah, A. A., & Akrofi, A. Y. (2000). Phytophthora megakarya: A potential threat to the cacao industry in Ghana. Ghana Journal of Agricultural Science, 33, 237–248.CrossRefGoogle Scholar
  156. Pakora, G. A. (2013). Biocontrole de la pourriture brune du cacaoyer par trios isolats de Trichoderma, etude des metabolites secondaires actifs et de leur biotransformation. PhD thesis, Université Pierre et Marie Curie, France, p. 188.Google Scholar
  157. Petrini, O. (1991). Fungal endophytes of tree leaves. In J. H. Andrew & S. S. Hirano (Eds.), Microbial ecology of leaves (pp. 179–197). New York, NY: Springer.CrossRefGoogle Scholar
  158. Phillips-Mora, W., Arciniegas-Leal, A., Mata-Quiros, A., & Motamayor-Arias, J. C. (2012). Catálogo de Clones de Cacao Selecionados por el CATIE para Siembras Comerciales. Turrialba, Costa Rica: CATIE. ISBN 978-9977-57-571-1.Google Scholar
  159. Phillips-Mora, W., Castillo, J., Krauss, U., Rodríguez, E., & Wilkinson, M. J. (2005). Evaluation of cacao (Theobroma cacao) clones against seven Colombian isolates of Moniliophthora roreri from four pathogen genetic groups. Plant Pathology, 54, 483–490.CrossRefGoogle Scholar
  160. Pohe, J., & Agneroh, T. A. (2013). Neem seed oil, an alternative fungicide to copper oxide in the control of brown rot of cacao pods in Cote d’Ivoire. Journal of Applied Biosciences, 62, 4644–4652.CrossRefGoogle Scholar
  161. Pomella, A. W. V., de Souza, J. T., Niella, G. R., Bateman, R. P., Hebbar, P. K., Loguercio, L. L., et al. (2007). The use of Trichoderma stromaticum in the management of witches’ broom disease of cacao in Bahia state, Brazil. In C. Vincent, M. Goetel, & G. Lazarovits (Eds.), Biological control: A global perspective-case studies from around the world (pp. 210–2017). Wallingford, UK: CABI Publishing.CrossRefGoogle Scholar
  162. Poppenborg, P., & Hölscher, D. (2009). The influence of emergent trees on rainfall distribution in a cacao agroforest (Sulawesi, Indonesia). Flora, 204, 730–736.CrossRefGoogle Scholar
  163. Pozo, M. J., & Azcón-Aguilar, C. (2007). Unraveling mycorrhiza-induced resistance. Current Opinion in Plant Biology, 10, 393–398.PubMedCrossRefGoogle Scholar
  164. Pozo, M. J., Jung, S. C., Martínez-Medina, A., López-Ráez, J. A., Azcón-Aguilar, C., & Barea, J.-M. (2013). Root allies: Arbuscular mycorrhizal fungi help plants to cope with biotic stresses. Soil Biology, 37, 289–307.CrossRefGoogle Scholar
  165. Ratnadass, A., Fernandes, P., Avelino, J., & Habib, R. (2012). Plant species diversity for sustainable management of crop pests and diseases in agroecosystems: A review. Agronomy for Sustainable Development, 32, 273–303.CrossRefGoogle Scholar
  166. Ravnskov, S., Jensen, B., Knudsen, I. M. B., Bødker, L., Jensen, D. F., Karliński, et al. (2006). Soil inoculation with the biocontrol agent Clonostachys rosea and the mycorrhizal fungus Glomus intraradices results in mutual inhibition, plant growth promotion and alteration of soil microbial communities. Soil Biology & Biochemistry, 38, 3453–3462.CrossRefGoogle Scholar
  167. Ristaino, J. B., & Gumpertz, M. L. (2000). New frontiers in the study of dispersal and spatial analysis of epidemics caused by species in the genus Phytophthora. Annual Review of Phytopathology, 38, 541–576.PubMedCrossRefGoogle Scholar
  168. Rodrigues, K. F., Petrini, O., & Leuchtermann, A. (1995). Variability among isolates of Xylaria cubensis as determined by isozyme analysis and somatic incompatibility tests. Mycologia, 87, 592–596.CrossRefGoogle Scholar
  169. Rojas, E. I., Rehner, S. A., Samuels, G. J., Van Bael, S. A., Herre, E. A., Cannon, P., et al. (2010). Colletotrichum gloeosporioides s.l. associated with Theobroma cacao and other plants in Panama: Multilocus phylogenies distinguish host-associated pathogens from asymptomatic endophytes. Mycologia, 102, 1318–1338. doi: 10.3852/09-244.PubMedCrossRefGoogle Scholar
  170. Rosmana, A., Samuels, G. J., Ismaiel, A., Ibrahim, E. S., Chaverri, P., Herawati, Y., et al. (2015). Trichoderma asperellum: A dominant endophyte species in cacao grown in Sulawesi with potential for controlling vascular streak dieback disease. Tropical Plant Pathology, 40, 19–25.CrossRefGoogle Scholar
  171. Rubini, M. R., Silva-Ribeiro, R. T., Pomella, A. W. V., Maki, C. S., Araújo, W. L., Santos, D. R., et al. (2005). Diversity of endophytic fungal community of cacao (Theobroma cacao) and biological control of Crinipellis perniciosa, causal agent of witches’ broom disease. International Journal of Biological Sciences, 1, 24–33.PubMedCentralPubMedCrossRefGoogle Scholar
  172. Ruinen, J. (1956). Occurrence of Beijerinckia species in the phyllosphere. Nature, 177, 220–221.CrossRefGoogle Scholar
  173. Ruiz, S. L., & Leguizamón, C. J. (1996). Efecto del contenido de materia org_anica del suelo sobre el control de Rosellinia bunodes con Trichoderma spp. Cenicafé, 47, 179–186.Google Scholar
  174. Ryals, J. A., Neuenschwander, U. H., Willits, M. G., Molina, A., Steiner, H.-Y., & Hunt, M. D. (1996). Systemic acquired resistance. The Plant Cell, 8, 1809–1819.PubMedCentralPubMedCrossRefGoogle Scholar
  175. Samuels, G. J., Dodd, S. L., Lu, B.-S., Petrini, O., Schroers, H.-J., & Druzhinina, I. S. (2006a). The Trichoderma koningii aggregate species. Studies in Mycology, 56, 67–133.PubMedCentralPubMedCrossRefGoogle Scholar
  176. Samuels, G. J., & Ismaiel, A. (2009). Trichoderma evansii and T. lieckfeldtiae two new T. hamatum-like species. Mycologia, 101, 142–156.PubMedCrossRefGoogle Scholar
  177. Samuels, G. J., Ismaiel, A., Rosmana, A., Junaid, M., Guest, D., McMahon, P., et al. (2012). Vascular streak dieback of cacao in Southeast Asia and Melanesia: In planta detection of the pathogen and a new taxonomy. Fungal Biology, 116, 11–23. doi: 10.1016/j.funbio.2011.07.009.PubMedCrossRefGoogle Scholar
  178. Samuels, G. J., Lieckfeldt, E., & Nirenberg, H. I. (1999). Trichoderma asperellum, a new species with warted conidia, and redescription of T. viride. Sydowia, 51, 71–88.Google Scholar
  179. Samuels, G. J., Pardo-Schultheiss, R., Hebbar, K. P., Lumsden, R. D., Bastos, C. N., Costa, J. C., et al. (2000). Trichoderma stromaticum sp. nov., a parasite of the cacao witches broom pathogen. Mycological Research, 104, 760–764.CrossRefGoogle Scholar
  180. Samuels, G. J., Suarez, C., Solis, K., Holmes, K. A., Thomas, S. E., Ismaiel, A., et al. (2006b). Trichoderma theobromicola and T. paucisporum: Two new species isolated from cacao in South America. Mycological Research, 110, 381–392.PubMedCrossRefGoogle Scholar
  181. Schisler, D. A., Slininger, P. J., Behle, R. W., & Jackson, M. A. (2004). Formulation of Bacillus spp. for biological control of plant diseases. Phytopathology, 94, 1267–1271.PubMedCrossRefGoogle Scholar
  182. Schloen, M., Louafi, S., & Dedeurwaerdere, T. (2011). Access and benefit-sharing for genetic resources for food and agriculture–current use and exchange practices, commonalities, differences and user community needs. Commission on Genetic Resources for Food and Agriculture (FAO Background Study Paper #59).
  183. Schmidt, C., Clough, Y., & Vidal, S. V. (2010). Diversity and distribution patterns of foliar fungal endophytes in Theobroma cacao in central Sulawesi and interactions between endophytes and host plant. Thesis der Fakultät für Agrarwissenschaften Universität Göttingen.Google Scholar
  184. Schnell, R. J., Kuhn, D. N., Brown, J. S., Olano, C. T., Phillips-Mora, W., Amores, F. M., et al. (2007). Development of a marker assisted selection program for cacao. Phytopathology, 97, 1664–1669.PubMedCrossRefGoogle Scholar
  185. Schroth, G., Krauss, U., Gasparotto, L., Aguilar, J. A. D., & Vohland, K. (2000). Pests and diseases in agroforestry systems in the humid tropics. Agroforestry Systems, 50, 199–241.CrossRefGoogle Scholar
  186. Sharma, P. (2011). Complexity of Trichoderma-Fusarium interaction and manifestation of biological control. Australian Journal of Crop Science, 5, 1027–1038.Google Scholar
  187. Snoeck, D., Abolo, D., & Jagoret, P. (2010). Temporal changes in VAM fungi in the cacao agroforestry systems of central Cameroon. Agroforestry Systems, 78, 323–328.CrossRefGoogle Scholar
  188. Soberanis, W., Rios, R., Arévalo, E., Zúñiga, L., Cabezas, O., & Krauss, U. (1999). Increased frequency of phytosanitary pod removal in cacao (Theobroma cacao) increases yield economically in eastern Peru. Crop Protection, 18, 677–685.CrossRefGoogle Scholar
  189. Sonwa, D. J., Coulibaly, O., Adesina, A. A., Weise, S. F., & Tchatat, M. (2002). Integrated pest management in cacao agroforests in southern Cameroon: Constraints and overview. Integrated Pest Management Reviews, 7, 191–199.CrossRefGoogle Scholar
  190. Soumaila, Z. B. I.-M., Tra, T. B., Noêl, Z. G., Claude, K. Z., Ghislaine, F. K. R., & Zézé, A. (2012). Arbuscular mycorrhizal fungi associated with Theobroma cacao L. in the region of Yamoussoukro (Cote d’Ivoire). African Journal of Agricultural Research, 7(6), 993–1001.Google Scholar
  191. Sriwati, R., Chamzurni, T., & Sukarman, S. (2011). Deteksi dan identifikasi cendawan endofit Trichoderma yang berasosiasi pada tanaman kakao. Jurnal Agrista, 15, 15–20.Google Scholar
  192. Sriwati, R., Melnick, R. L., Muarif, R., Strem, M. D., Samuels, G. J., & Bailey, B. A. (2015). Trichoderma from Aceh Sumatra reduce Phytophthora lesions on pods and cacao seedlings. Biological Control. doi: 10.1016/j.biocontrol.2015.04.018.Google Scholar
  193. Strickland, A. H. (1951). The entomology of swollen shoot of cacao. II-The bionomics and ecology of the species involved. Bulletin of Entomological Research, 42, 65–103.CrossRefGoogle Scholar
  194. Suryanto, D., Wahyuni, S., Siregar, E. B. M., & Munir, E. (2014). Utilization of chitinolytic bacterial isolates to control anthracnose of cacao leaf caused by Colletotrichum gloeosporioides. African Journal of Biotechnology, 13, 1631–1637.CrossRefGoogle Scholar
  195. Talontsi, F. M., Dittrich, B., Schüffler, A., Sun, H., & Laatsch, H. (2013). Epicoccolides: Antimicrobial and antifungal polyketides from an endophytic fungus Epicoccum sp. associated with Theobroma cacao. European Journal of Organic Chemistry, 2013(15), 3174–3180. doi: 10.1002/ejoc.201300146.CrossRefGoogle Scholar
  196. Tchameni, S. N., Ngonkeu, M. E. L., Begoude, B. A. D., Wakam Nana, L., Fokom, R., Owona, A. D., Mbarga, J. B., Tchana, T., Tondje, P. R., Etoa, F. X., Kuaté J. (2011). Effect of Trichoderma asperellum and arbuscular mycorrhizal fungi on cacao growth and resistance against black pod disease. Crop Protection, 30, 1321–1327.Google Scholar
  197. Tchameni, S. N., Nwaga, D., Wakam, L. N., Ngonkeu, E. L. M., Fokom, R., Kuaté, J., Etoa, Francois-Xavier (2012). Growth enhancement, amino acid synthesis and reduction in susceptibility towards Phytophthora megakarya by arbuscular mycorrhizal fungi inoculation in cacao plants. Journal of Phytopathology, 160, 220–228.Google Scholar
  198. ten Hoopen, G. M. (2007). Monitoring mycoparasites on the fructoplane of cacao (Theobroma cacao L.). PhD Thesis, Royal Holloway University of London, p. 243.Google Scholar
  199. ten Hoopen, G. M., Deberdt, P., Mbenoun, M., & Cilas, C. (2012). Modelling cacao pod growth: Implications for disease control. Annals of Applied Biology, 160, 260–272.CrossRefGoogle Scholar
  200. ten Hoopen, G. M., George, A., Martínez, A., Stirrup, T., Flood, J., & Krauss, U. (2010a). Compatibility between Clonostachys isolates with a view to mixed inocula for biocontrol. Mycologia, 102, 1204–1215.PubMedCrossRefGoogle Scholar
  201. ten Hoopen, G. M., & Krauss, U. (2006). Biology and control of Rosellinia bunodes, Rosellinia necatrix and Rosellinia pepo: A review. Crop Protection, 25, 89–107.CrossRefGoogle Scholar
  202. ten Hoopen, G. M., Kuate, J., Mbarga, J. B., Atangana, J. B., Tchana, T., Bateman, R., et al. (2010a). Integrated control of Phytophthora megakarya in Cameroon (pp. 1189–1194). Proceedings of the 16th International Cacao Research Conference. ISBN 978-065-959-5.Google Scholar
  203. ten Hoopen, G. M., Rees, R., Aisa, P., Stirrup, T., & Krauss, U. (2003). Population dynamics of epiphytic mycoparasites of the genera Clonostachys and Fusarium for the biocontrol of black pod (Phytophthora palmivora) and moniliasis (Moniliophthora roreri) on cacao (Theobroma cacao). Mycological Research, 107, 587–596.PubMedCrossRefGoogle Scholar
  204. Thomas, S. E., Crozier, J., Aime, M. A., Evans, H. C., & Holmes, K. A. (2008). Molecular characterization of fungal endophytic morphospecies associated with the indigenous forest tree, Theobroma gileri, in Ecuador. Mycological Research, 112, 852–860.PubMedCrossRefGoogle Scholar
  205. Thurston, J. L. (1998). Tropical plant diseases (2nd ed., p. 200). Minnesota, MN: APS Press.Google Scholar
  206. Tondje, P. R., Hebbar, K. P., Samuels, G., Bowers, J. H., Weise, S., Nyemb, E., et al. (2006). Bioassay of Geniculosporium species for Phytophthora megakarya biological control on cacao pod husk pieces. African Journal of Biotechnology, 5, 648–652.Google Scholar
  207. Tondje, P. R., Roberts, D. P., Bon, M. C., Widmer, T., Samuels, G. J., Ismaiel, A., Begoude, A. D., Tchana, T., Nyemb-Tshomb, E., Ndoumbe-Nkeng, M., Bateman, R., Fontem, D., Hebbar K. P. (2007). Isolation and identification of mycoparasitic isolates of Trichoderma asperellum with potential for suppression of black pod disease of cacao in Cameroon. Biological Control, 43, 202–212.Google Scholar
  208. Torres de la Cruz, M., Ortiz García, C. F., Téliz Ortiz, D., Mora Aguilera, A., & Nava Díaz, C. (2013). Efecto del azoxystrobin sobre Moniliophthora roreri, agente causal de la moniliasis del cacao (Theobroma cacao). Fitopatología, 31, 65–69.Google Scholar
  209. Tran, H., Ficke, A., Asiimwe, T., Hofte, M., & Raaijmakers, J. M. (2007). Role of the cyclic lipopeptide massetolide A in biological control of Phytophthora infestans and in colonisation of tomato plants by Pseudomonas fluorescens. New Phytologist, 175, 731–742.PubMedCrossRefGoogle Scholar
  210. Tran, H., Kruijt, M., & Raaijmakers, J. M. (2008). Diversity and activity of biosurfactant-producing Pseudomonas in the rhizosphere of black pepper in Vietnam. Journal of Applied Microbiology, 3, 839–851.CrossRefGoogle Scholar
  211. Urdaneta, L. M., & Delgado, A. E. (2007). Identificación de la micobiota del filoplano del cacaotero (Theobroma cacao L.) en el municipio Carraciolo Parra Olmedo, estado Mérida, Venezuela. Revista de la Facultad de Agronomía, 24, 47–68.Google Scholar
  212. Van der Putten, W. H., Vet, L. E. M., Harvey, J. A., & Wäckers, F. L. (2001). Linking above and below ground multitrophic interactions of plants, herbivores, pathogens, and their antagonists. Trends in Ecology and Evolution, 16, 547–554.CrossRefGoogle Scholar
  213. Van Loon, L. C., Bakker, P. A. H. M., & Pieterse, C. M. J. (1998). Systemic resistance induced by rhizosphere bacteria. Annual Review of Phytopathology, 36, 453–483.PubMedCrossRefGoogle Scholar
  214. Van Wees, S. C., van der Ent, S., & Pieterse, C. M. J. (2008). Plant immune responses triggered by beneficial microbes. Current Opinion in Plant Biology, 11, 443–448.PubMedCrossRefGoogle Scholar
  215. Wamberg, C., Christensen, S., Jakobsen, I., Muller, A. K., & Sorensen, S. J. (2003). The mycorrhizal fungus (Glomus intraradices) affects microbial activity in the rhizosphere of pea plants (Pisum sativum). Soil Biology & Biochemistry, 35, 1349–1357.CrossRefGoogle Scholar
  216. Wardle, D. A., Yeates, G. W., Watson, R. N., & Nicholson, K. S. (1995, May). The detritus food-web and the diversity of soil fauna as indicators of disturbance regimes in agro-ecosystems (Vol. 170, pp. 35–43). International Symposium on Soil Biodiversity, East Lansing, MI.Google Scholar
  217. Widmer, T. L. (2014). Screening Trichoderma species for biological control activity against Phytophthora ramorum in soil. Biological Control, 79, 43–48.CrossRefGoogle Scholar
  218. Widmer, T. L., & Laurent, N. (2006). Plant extracts containing caffeic acid and rosmarinic acid inhibit zoospore germination of Phytophthora spp. pathogenic to Theobroma cacao. European Journal of Plant Pathology, 115, 377–388.CrossRefGoogle Scholar
  219. Yánez‐Mendizábal, V., Vinas, I., Usall, J., Torres, R., Solsona, C., Abadias, M., Teixidó (2012). Formulation development of the biocontrol agent Bacillus subtilis strain CPA‐8 by spray‐drying. Journal of Applied Microbiology, 112, 954–965.Google Scholar
  220. Yedidia, I., Benhamou, N., Kapulnik, Y., & Chet, I. (2000). Induction and accumulation of PR proteins activity during early stages of root colonization by the mycoparasite Trichoderma harzianum strain T-203. Plant Physiology and Biochemistry, 38, 863–873.CrossRefGoogle Scholar
  221. Yedidia, I., Benhamou, N., & Chet, I. (1999). Induction of defense responses in cucumber plants (Cucumis sativus L.) by the biocontrol agent Trichoderma harzianum. Applied and Environmental Microbiology, 65, 1061–1070.PubMedCentralPubMedGoogle Scholar
  222. Zhang, Y., Smith, P., Maximova, S. N., & Guiltinan, M. J. (2014). Application of glycerol as a foliar spray activates the defence response and enhances disease resistance of Theobroma cacao. Molecular Plant Ecology, 16, 27–37. doi: 10.1111/mpp. 12158.Google Scholar

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© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.CIRADUPR BioagresseursMontpellierFrance
  2. 2.Palm Integrated Services & Solutions Ltd. (PISS)La BorneWest Indies

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