Bibliography of Witches' Broom Crinipellis perniciosa

Witches' broom, Crinipellis perniciosa (Stahel) Singer, is a serious fungal disease of cacao in Latin America. Indigenous to the Amazon, it is now present in most of the cocoa growing regions in South America and several Caribbean islands. It occurs in Bolivia, Brazil, Colombia, Ecuador, Grenada, Guyana, Panama (on the South American side of the canal), Peru, St. Vincent, Surinam, Tobago, Trinidad, and Venezuela. In 1989 witches' broom was detected for the first time in the state Bahia, Brazil. It had invaded the major growing area of Brazil and ravaged production. Yields in Bahia decreased by 60% from 1990 to 1994.

Basidiospores, the only infective propagule of C. perniciosa, are produced in small mushroom-like basidiocarps that develop on brooms and diseased pods during rainy periods. Basidiospores are spread by wind and must land in water to germinate and infect susceptible tissues of cacao. Vegetative brooms develop following infection of terminal and axillary buds; cushion brooms that resemble vegetative brooms develop from infected flower cushions, as well as star blooms (diseased flowers) and chirimoya-like (diseased) pods. Seeds in developing pods infected up to about 12 weeks of age are usually destroyed so that cocoa beans cannot be produced. Infection of older pods results in no or only minimal damage to pod contents. Losses from witches' broom may be more than 90%. Management of cacao in the presence of witches' broom requires knowledge of the local situation relative to disease epidemiology, periods of favorable climate for disease initiation, availability and abundance of pathogen inoculum and susceptible host tissues, sources of inoculum, and the number of vegetative flushes. Also, agronomic knowledge about the plantation (tree spacing, shade, nearness to neighboring diseased plantations, incidence and severity of witches' broom in the plantation, time of harvest, pruning intensity) is essential.

These requirements and a variable economic situation make biologically sound, environmentally safe, and economically feasible management difficult. Phytosanitation (removal from the tree of witches' broom diseased plant parts and prevention of basidiocarp development from the removed items), chemical controls, disease escape, and host resistance to witches' broom may be management choices. Timing and number of phytosanitation prunings are critical, however, pruning should be done during the dry period.

Protective fungicidal chemicals applied to developing pods on 7-day cycles during pod development is costly and usually ineffective. Pods set during the dry period may escape witches' broom, and trees of this type should be selected and used for replanting. Durable resistance, but not immunity, offers the best potential for management of witches' broom. Effective screening of germplasm for resistance to witches' broom is in progress at CEPLAC, Itabuna, Brazil, and at INIAP, Pichilingue, Quevedo, Ecuador. The best resistant germplasm can be used to produce resistant planting stock.

After a few months into the rainy season the "brooms" left on trees begin to sporulate, especially those in the upper canopy. This results in a flow of infective spores over the new foliage, flower and cushions. These brooms continue to sporulate as the season progresses resulting in newly infected brooms. These new brooms sporulate the following season, while affected flower cushions and young distorted pods produce no spores, and are a complete loss for normal pod production. Young infected brooms are easily recognized and sanitation crews can easily prune them off "short" trees.

Because of labor cost, pruned brooms are generally not removed from the ground area around trees. However, these brooms will sporulate in the next year's rainy season for further spore dispersal. Petroleum oil, like that used for Sigatoka on banana, should be applied as a ground cover spray onto the old pruned brooms. The oil should be applied before the rainy season starts. Petroleum oil is not a fungicide, its action being physical, but by stoping the absorption of rain water into necrotic broom surfaces. It is moisture within the infected brooms that triggers the production of the basidiocarps with resultant spore dispersal. Furthermore, oil is not applied to new maturing cocoa pods, but only to the understory ground areas.

Management Suggestions:

Trees must be kept short, under 4 meters, in order for field crews to effectively locate and prune the infective brooms.
Make frequent pruning cycles to remove brooms and other infected material. A suggested interval between pruning cycles is 10 to 14 days; continue these sanitation surveys until the areas are clean.
Pruned wood left on the ground under the trees should not be allowed to sporulate. Spray these brooms with petroleum oil to make their surfaces repellent to rain water.
The key to economical sanitation is thoroughness followed by ground sprays with petroleum oil.

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Achicanoy, L. H. and Buritica, C. P. 1982. In vitro evaluation of fungicides in the control of Crinipellis perniciosa (Stahel) Singer and Moniliophthora roreri (Cif & Par). Pp. 419-423 in Proceedings of the 8th International Cocoa Research Conference, Cartegena, Columbia. Cocoa Producers' Alliance, Lagos, Nigeria. (In Spanish, with summaries in English, French, and Portguese).

Andebrhan, T. 1983. Witches' broom disease of Theobroma cacao in Brazil. I. Inoculation of ungerminated seeds (Cacao, Crinipellis perniciosa). Rev. Theobroma 13 (1): 47-49. ill. (In English with summary in Portuguese. )

Andebrhan, T. 1985. Studies on the epidemiology and control of witches' broom disease of cacao in the Brazilian Amazon. Pp. 395-402 in Proceedings of the 9th International Cocoa Research Conference, Lome, Togo, 12-18 Feb. 1984. Cocoa Producers' Alliance, Lagos, Nigeria.

Andebrhan,T. 1983. Witches' broom disease of Theobroma cacao in Brazil. I. Inoculation of ungerminated seeds (Cacao, Crinipellis perniciosa). Rev. Theobroma 13(1): 47-49.

Andebrhan, T., Hammerstone, J. F. Jr., Romanczyk, L. J. Jr., and D. B. Furtek. (1995) Sensitivity of Crinipellis perniciosa to procyanidins from Theobroma cacao L. Physiological and Molecular Plant Pathology. 46(5):339-348.

Aranzazu Hernandez, F. 1982. Analysis of the evolution and variation in the incidence of witches' broom disease Crinipellis perniciosa in the Uraba region (Colombia). Pp. 387-393 in Proceedings of the 8th International Cocoa Research Conference, 18-23 Oct 1981. Cocoa Producers' Alliance, Lagos, Nigeria. (In Spanish, with summaries in English, French, and Portuguese).

Aranzazu Hernandez, F. 1982. Some aspects of the biology of Crinipellis perniciosa (Stahel) Singer in the Uraba region (Colombia). Pp. 323-328 in Proceedings of the 8th International Cocoa Research Conference, Cartagena, Colombia, 18-23 Oct., 1981. Cocoa Producers' Alliance, Lagos, Nigeria. (In Spanish with summaries in English, French, and Portuguese).

Bastos, C. N. 1978. Antagonism to the fungus Crinipellis perniciosa (Stahel) Singer, causal agent of witches' broom disease of cacao. Rev. Theobroma 8(4): 147-150. (In Portuguese with summary in English.)

Bastos, C. N. 1979. Effect of some fungicides on spore germination of Crinipellis perniciosa (Stahel) Singer (syn. Marasmius perniciosus, cacao pathogen) in vitro. Fitopathol. Bras. 4(2): 313-316. (In Portuguese with summary in English).

Bastos, C. N. 1979. Hyperparasitism by the fungus Dactylium sp. of Crinipelles =Marasmius perniciosa (Stahel) Singer, on witches' broom disease of cacao. Biological Control, Belem, Para State, Brazil. Rev. Theobroma 9(4): 197-200. (In Portuguese with summary in English).

Bastos, C. N. (1985) A new pathotype of Crinipellis perniciosa (witches' broom disease) on solanaceous hosts. Plant Pathology. 34: 306-312.

Bastos, C. N. (1989) Effect of sunlight radiation and post-germination period on the viability of basidiospores of Crinipellis perniciosa. Fitopatologia Brasileira. 14(3-4):261-263.

Bastos, C. N. (1990) Pathogenicity and characteristics of the isolate of Crinipellis perniciosa from Urucuca Bahia Brazil. Fitopatologia Brasileira. 15(4).

Bastos, C. N. (1993) Infection of cocoa seedlings by other types of propagules, other than basidiospores, produced by Crinipellis perniciosa in vitro. Fitopatologia Brasileira 18(3):451-453.

Bastos, C. N. (1994) Ability of Crinipellis perniciosa to produce viable basidiospores on three-year-old brooms and to infect tissue of dormant buds on cocoa. Fitopatologia Brasileira 19(4):585-587.

Bastos, C. N. (1996) Potential of Trichoderma viride for the control of cocoa witches' broom (Crinipellis perniciosa). Fitopatologia Brasileira. 21(4):509-512.

Bastos, C. N. (1996) Effect of water potential on growth and viability on conidia of Trichoderma viride after storage at different temperatures. Summa Phytopathologica. 22(3-4):258-261.

Bastos, C. N. (1996) Mycoparasitic nature of the antagonism between Trichoderma viride and Crinipellis perniciosa. Fitopatologia Brasileira. 21(1):50-54.

Bastos, C. N. (1997) The effect of Piper aduncum oil on Crinipellis perniciosa and other fungal pathogens. Fitopatologia Brasileira. 22(3):441-443.

Bastos, C. N. & Andebrhan, T. 1987. In vitro production of basidiospores of Crinipellis perniciosa, the causative agent of witches' broom disease of cocoa. Trans. Br. Mycol. Soc. 88(3): 406-409.

Bastos, C. N. & J.C. Dias. (1992) Reduction in the production of basidiocarps of Crinipellis perniciosa by Trichoderma viride. Summa Phytopathologica. 18(3-4):235-238.

Bastos, C. N., and G. C. Pereira. (1994) Levels of nutrients in healthy tissues of cocoa and infected by Crinipellis perniciosa. Fitopatologia Brasileira 19(2):245-247.

Brownlee, H. E., Hedger, J. and Scott, I. M. 1992. Effects of a range of procyanidins on the cocoa pathogen Crinipellis perniciosa. Physiol. Mol. Plant Pathol. 40(4): 227-232.

Brownlee, H. E., Hedger, J. and Scott,I. M. 1990. Host extracts cause morphological variation in germ-tubes of the cocoa pathogen, Crinipellis perniciosa. Mycol. Res. 94(4): 543-547.

Brownlee, H. E., McEuen, A. R., Hedger, J. and Scott, I. M. 1990. Anti-fungal effects of cocoa tannin on the witches' broom pathogen Crinipellis perniciosa. Physiol. Mol. Plant Pathol. 36(1): 39-48.

Cairns, D. M. (1994) Spatial pattern analysis of witches' broom disease of cacao at a landscape in Rondonia, Brazil. Tropical Agriculture. 71(1):31-35.

Calle, H., Cook, A. A. and Fernando, S. Y. 1982. Histology of witches' broom caused in cacao (Theobroma cacao) by Crinipellis perniciosa. Phytopathology 72(11): 1479-1481.

Cifuentes, C., Mayorga, M., Prieto, E., Rondon, G. and Tovar, G. 1982. Quantitative study of witches' broom production on cacao plants affected by Crinipellis perniciosa (Stahel), Singer, and its significance in the management of the disease. Pp. 407-413 in Proceedings of the 8th International Cocoa Research Conference Cartagena, Colombia, 18-23 Oct., 1981. Cocoa Producers' Alliance, Lagos Nigeria. (In Spanish, with summaries in English, French, and Portguese).

Cifuentes, C., Mayorga, M., Prieto, E., Rondon, G. and Tovar, G. 1982. Infection and sporulation by Crinipellis perniciosa (Stahel) Singer, causal agent of witches' broom disease of cacao in Guamal, Colombia. Pp. 485-492 in Proceedings of the 8th International Cocoa Research Conference, Cartagena, Colombia, 18-23 Oct., 1981. Cocoa Producers' Alliance, Lagos, Nigeria. (In Spanish with summaries in English, French, and Portguese).

Cifuentes, C., Prieto, E. and Tovar, G. 1982. Evaluation of four systemic fungicides for the control of Crinipellis perniciosa (Stahel) Singer, in Guamal, Colombia. Pp. 545-550 in Proceedings of the 8th International Cocoa Research Conference, Cartagena, Colombia, 18-23 Oct., 1981. Cocoa Producers' Alliance, Lagos, Nigeria.

Cronshaw, D. K. 1979. Fungicide application together with cultural practices to control cocoa diseases caused by Crinipellis perniciosa, Monilia roreri, Phytophthora palmivora in Ecuador. Trop. Agric. 56(2): 165-170.

Cronshaw, D. K. and Evans, H. C. 1978. Witches' broom disease of cocoa Crinipellis perniciosa in Ecuador. ii. Methods of infection. Ann. Appl. Biol. 89(2): 193-200.

Dabydeen, S. and Sreenivasan, T. N. 1989. Occurrence, anatomy, and morphology of "blisters" on cocoa seedlings inoculated with Crinipellis perniciosa. Plant Disease 73 (6): 481-484.

Delgado, J. C. and Cook, A. A. 1976. Arthroconidia formation in cultures of Marasmius perniciosus (Witches' broom of cacao). Phytopathology, 66(6): 717-718. Ref.

Delgado, J. C. and Cook, A. A. 1976. Nuclear conditions of the basidia, basidiospores, and mycelium of Marasmius perniciosus (causal agent of witches'broom of cacao). Can. J. Bot. 54(1/2): 66-72. Ref.

Edwards, D. F. 1978. Studies on the manipulation of the timing of crop maturity of cocoa in Ecuador in relation to losses from pod diseases Crinipellis perniciosa, Monilia roreri, pollination. J. Hortic. Sci. 53(3): 243-254.

Evans, H. C. 1975. Pleomorphism in Crinipellis perniciosa, causal agent of witches' broom disease of cocoa Theobroma cacao. Trans. Br. Mycol. Soc. 74(3): 515-523.

Evans, H. C. 1978. Witches' broom disease of cocoa (Crinipellis perniciosa) in Ecuador. i. The fungus. Ann. Appl. Biol. 89(2): 185-192.

Evans, H. C. 1981. Witches' broom disease: a case study Cocoa in South American countries. Cocoa Grow. Bull. 32: 5-19.

Evans, H. C. & R. W. Barreto. (1996) Crinipellis perniciosa: A much investigated but little understood fungus. Mycologist. 10(2):58-61.

Evans, H. C. and Bastos, C. N. 1975. Basidiospore germination as a means of assessing resistance to Crinipellis perniciosa (witches' broom disease) in cocoa Theobroma cacao cultivars. Trans. Br. Mycol. Soc. 74(3): 525-536.

Evans, H. C. and Bastos, C. N. 1980. A new method of testing resistance of cacao to witches' broom disease Crinipellis perniciosa. Rev. Theobroma 10(4): 175-186. (In Portuguese with summary in English.)

Evans, H. C. and Bastos, C. N. 1981. Preliminary results of research on witches' broom disease of cacao Crinipellis perniciosa in the Amazonian region of Brazil. Pp. 255-256 in Proceedings of the 7th International Cocoa Research Conference, Douala, Cameroun, 4-12 Nov 1979. Cocoa Producers' Alliance, Lagos Nigeria.

Evans, H. C. and Prior, C. 1987. Cocoa pod diseases: causal agents and control. Outlook. Agric. 16(1):35-41.

Evans, H. C. and Solorzano, G. R. 1982. Witches' broom disease: wrong experiment, right results. Pp. 415-418 in Proceedings of the 8th International Cocoa Research Conference , Cartagena, Colombia, 18-23 Oct., 1981. Cocoa Producers' Alliance, Lagos, Nigeria.

Fohnseca, S. E. A. and Wheeler, B. E. J. 1990. Assessing resistance to Crinipellis perniciosa using cocoa callus. Plant Pathol. 39(3): 463-471.

Frias, G. A., Purdy, L. H. and Schmidt, R. A. 1991. Infection biology of Crinipellis perniciosa on vegetative flushes of cacao. Plant Dis. 75 (6): 552-556.

Frias, G. A., Purdy, L. H. and Schmidt, R. A. 1995. An inoculation method for evaluating resistance of cacao to Crinipellis perniciosa. Plant Dis. 79(8): 787-791.

Fulton, R. H. 1989. The cacao disease trilogy: black pod, Monilia pod pot, and witches' broom. Plant Dis. 73 (7): 601-603.

Griffith, G. W. & J. N. Hedger. (1994) Spatial distribution of mycelia of the liana (L-) biotype of the agaric Crinipellis perniciosa (Stahel) singer in tropical forest. New Phytologist 127(2):243-259.

Griffith, G. W. and Hedger, J. N. 1994. The breeding biology of biotypes of the witches broom pathgen of cocoa, Crinipellis perniciosa. Heredity 72(3):278-289.

Hedger, J. N., Pickering, V. and Aragundi, J. 1987. Variability of populations of the witches' broom disease of cocoa Crinipellis perniciosa. Trans. Br. Mycol. Soc. 88(4): 533-546.

Holliday, P. 1974. Witches' broom disease Crinipellis perniciosa of cacao Pp. 279-282 in Phytophthora Disease of Cocoa. (P. H. Gregory, ed).

Laker, H. A., Sreenivasan, T. N. and Raj-Kumar, D. 1988. Present status of witches' broom disease of cocoa in Trinidad. Trop. Pest Manage. 34(3): 318-323.

Laker, H. A. 1990. Reactions of cocoa (Theobroma cacao) seedlings and clonal plants to isolates of Crinipellis perniciosa in Trinidad. Trop. Agric. 67(1):

Laker, H. A. 1991. Evaluation of systematic fungicides for control of witches' broom disease of cocoa in Trinidad. Trop. Agric. 68(2): 119-124.

Laker, H. A. and Ram, A. 1992. Investigations on integrated control of witches' broom disease of cocoa in Rondonia State, Brazil. Trop. Pest Manage. 38 (4): 354-358.

Maddison, A. C., Macias, G., Moreira, C., Arias, R., and R. Neira. (1995) Cocoa production in Ecuador in relation to dry-season escape from pod rot caused by Crinipellis perniciosa and Moniliophthora roreri. Plant Pathology (Oxford). 44(6):982-998.

Maddison, A. C. and Mogrovejo, E. 1985. Witches' broom and the establishment of cacao. Pp. 389-394 in Proceedings of the 9th International Cocoa Research Conference, Lome, Togo, 12-18 Feb 1984. Cocoa Producers' Alliance, Lagos, Nigeria.

Manco, G. R. 1973 General considerations on cacao diseases in Amazonia. (Marasmius perniciosus, Phytophthora palmivora, nematodes) Rev. Theobroma 3(1): 3-13. (In Portuguese with summary in English).

Mayorga P, M. and Aranzazu H, F. 1982. Chemical control of witches' broom in cacao. Pp. 551-555 in Proceedings of the 8th International Research Conference, Cartagena, Colombia, 18-23 Oct., 1981. Cocoa Producers' Alliance, Lagos, Nigeria.

McGeary, F. M. and Wheeler, B. E. J. 1988. Growth rates of, and mycelial interactions between, isolates of Crinipellis perniciosa from cocoa. Plant Pathol. 37 (4): 489-498.

McQuilken, M. P., Supriadi and Rudgard, S. A. 1988. Sensitivity of Crinipellis perniciosa to two triazole fungicides in vitro and their effect on development of the fungus in cocoa. Plant Pathol. 37(4): 499-506.

Muse, R. B., Collin, H. A., Isaac, S., and K. Hardwick. (1996) Effects of the fungus Crinipellis perniciosa, causal agent of witches' broom disease, on cell and tissue cultures of cocoa (Theobroma cacao L.). Plant Pathology (Oxford). 45(1):145-154.

Periera, J. L., Ram, A., Figueiredo, J. M. de, and Almeida, L. C. C., de 1992. First occurrence of Witches' Broom disease in the principal cocoa growing region of Brazil. Trop. Agric. 67 (2): 188-189.

Pickering, V. and Hedger, J. N. 1987. Production of basidiocarps of the cocoa pathogen Crinipellis perniciosa in in vitro culture. Trans. Br. Mycol. Soc. 88(3): 404-406.

Purdy, L. H., Trese, A. T. and Aragundi, J. A. 1983. Proof of pathogenicity of Crinipellis perniciosa to Theobroma cacao by using basidiospores produced in in vitro culture (Brazil). Rev. Theobroma 13(3): 157-163.

Purdy, L. H., Trese, A. T. and Aragundi, J. A. 1983. Proof of pathogenicity of Crinipellis perniciosa to Theobroma cacao by using basidiospores produced in vitro culture. Rev. Theobroma. 13 (3): 157-163. (In English with summary in Portuguese.)

Purdy, L. H. and Dickstein, E. R. 1990. Basidiocarp development on mycelial mats of Crinipellis perniciosa. Plant Dis.: 74 (7): 493-496.

Orchard, J., Collin, H. A., Hardwick, K., and S. Isaac. (1994) Changes in morphology and measurement of cytokinin levels during the development of witches' brooms on cocoa. Plant Pathology (Oxford). 43(1):65-72.

Pereira, J. L., Almeida, L. C. C. D., and S. M. Santos. (1996) Witches' broom disease of cocoa in Bahia: Attempts at eradication and containment. Crop Protection. 15(8):743-752.

Rocha, H. M. and Wheeler, B. E. J. 1982. The water balance as an important factor in basidiocarp production by Crinipellis perniciosa, the causal fungus of cocoa witches' broom. Pp. 381-386 in Proceedings of the 8th International Cocoa Research Conference, Cartagena, Columbia, 18-23 Oct. 1981. Cocoa Producers' Alliance, Lagos, Nigeria.

Rocha, H. M. and Wheeler, B. E. J. 1985. Factors influencing the production of basidiocarps and the deposition and germination of basidiospores of Crinipellis perniciosa, the causal fungus of witches' broom on cocoa (Theobroma cacao). Plant Pathol. 34(3): 319-328.

Rudgard, S. A., Maddison, A. C. and Andebrhan, T. 1993. Disease management in cocoa: comparative epidemiology of witches' broom. (1st ed.) Chapman & Hall, New York. 249 pp.

Rudgard, S. A. 1986. Witches' broom disease of cocoa in Rondonia, Brazil: pod losses. Trop. Pest Manage. 32(1): 24-26.

Rudgard, S. A. 1986. Witches' broom disease on cocoa in Rondonia, Brazil: Basidiocarp production on detached brooms in the field. Plant. Pathol. 35(4): 434-442.

Rudgard, S. A. 1987. Witches' broom disease of cocoa in Rondonia, Brazil: infection of vegetative flushes and flower cushions in relation to host phenology. Plant Pathol. 36(4): 523-530.

Rudgard, S. A. and Butler, D. R. 1987. Witches' broom disease on a cocoa in Rondonia, Brazil: pod infection in relation to pod susceptibility, wetness, inoculum, and phytosanitation. Plant Pathol. 36(4): 515-522.

Silva, A. R., Mizubuti, E. S. G., and H. R. Espinoza. (1995) Effect of different doses of triadimenol and hexaconazole on witches' broom disease of cocoa in Venezuela. Summa Phytopathologica. 21(2):171-174.

Sreenivasan, T. N. and Dabydeen, S. 1989. Modes of penetration of young cocoa leaves by Crinipellis perniciosa. Plant Dis. 73 (6): 478-481.

Tovar Rodriguez, G. 1986. Witches' broom in cacao, science and technology. Agron. Colomb. 3(1/2): 15-30.

Went, Friedrich August Ferdinand Christian. 1904. Witches' broom disease in various types of cacao in Surinam. Verhandelingen der Koninklijke Akademie van Wetenschappen te Amsterdam, Afdeeling Natuurkunde 10(3): 40 pp. (In Dutch).

Wheeler, B. E. J. 1985. The growth of Crinipellis perniciosa in living and dead cocoa tissue. Symp. Ser. Br. Mycol. Soc. (10): 103-115.

Wheeler, B. E. J. and Mepsted, R. 1982. Pathogenic races of Crinipellis perniciosa. Pp. 365-370 in Proceedings of the 8th International Cocoa Research Conference, Cartagena, Colombia, 18-23 Oct. 1981. Cocoa Producers' Alliance, Lagos, Nigeria.

Wheeler, B. E. J. and Mepsted, R. 1988. Pathogenic variability amongst isolates of Crinipellis perniciosa from cocoa (Theobroma cacao). Plant Pathol. 37(4): 475-488.

Zarb, J. and Walters, D. R. 1993. The effect of ornithine decarboxylase inhibition on growth, enzyme activities, and polyamine concentrations in Crinipellis perniciosa. Pestic. Biochem. Physiol. 47(1): 44-50.

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Bibliography of Witches' Broom Crinipellis perniciosa

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