The Impact of Plant Diseases on World Chocolate Production

© 2001 Plant Healt h Progr ess. Accept ed for publicat ion 14 June 2001. Published 9 July 2001. Th e Im p a ct o f Pla n t D is e a s e s o n W o rld Ch o co la te Pro d u ctio n Joh n H . Bow e r s and Br y a n A. Ba ile y , Resear ch Plant Pat hologist s, USDA, ARS, PSI Alt ernat e Crops & Sy st em s Lab, Belt sville, MD 20705; Pr a k a sh K. H e bb a r , Senior Research Associat e, M&M Mar s, I nc. Research & Developm ent , Belt sville, MD 20705; Sou m a ila Sa n ogo, Resear ch Associat e, Wy e Research & Ext ension Cent er Universit y of Mar y land, Queenst ow n, MD 21658; Rob e r t D . Lu m sd e n , Plant Pat hologist and Collaborat or, USDA, ARS, PSI Alt ernat e Cr ops & Sy st em s Lab, Belt sv ille, MD 20705 Cor responding aut hor : John H. Bow ers. bow [email protected] Bow ers, J. H., Bailey , B. A., Hebbar , P. K., Sanogo, S., Lum sden, R. D. 2001. The im pact of plant diseases on w orld chocolat e product ion. Online. Plant Healt h Progress doi: 10.1094/ PHP- 2001- 0709- 01- RV. I n t r odu ct ion Chocolate has its origins in ancient Cen tral Am erica where the Maya an d the Aztecs cultivated the cacao tree (Theobrom a cacao L.) (Figs. 1A to 1C) an d extracted from the seeds or beans a high ly prized drink (Figs. 2A,2B,3), which was called chocolatl, a precursor to our m odern En glish word chocolate (41). Theobrom a m ean s the source of the “food of the gods,” hence its scien tific nam e Theo (god) an d brom a (food). The Spaniards, notably H ern an Cortez, in troduced Fig. 1A. Pods of Theobrom a cacao, the drin k to the Span ish royalty, but the bitter w hich cont ain 30 - 40 seeds each t hat ar e harvest ed and processed drink did n ot becom e popular for an other on e int o chocolat e product s. hundred years, when additives such as sugar, cinnam on, and chile peppers m ade the drink m ore palatable. Chocolate was the first m ildly stim ulating drink introduced to Europe, appearing even before coffee and tea. Th e presen t-day popularity of chocolate an d the drin k cocoa needs n o verification as attested to by the m any “chocolate lovers” who especially look forward to occasions and n ation al holidays when chocolate is traditionally given as a gift to loved ones and frien ds. The dem an d for chocolate is growin g an d the question now is will the world supply of a product that com es from a strictly tropical, rain forest-in habitin g tree will contin ue to m eet the dem an d. Over the past two decades several im portant fungal diseases have gained considerable im portance and pose a serious threat to the supply of chocolate (Fig. 4). Plant Health Progress 9 July 2001 Fig. 1B. Cacao pods in t he field in Br azil. Fig. 2A. Cocoa beans ( court esy M&M Mars, I nc.) . Fig. 3. Healt hy cacao pod. Fig. 1C. Healt hy cacao t r ee w it h pods, w hich develop from flow er cushions on t he t r unk of t he t r ee. Fig. 2B. Cocoa beans drying in t he sun ( cour t esy M&M Mar s, I nc.) . Fig. 4. Diseased pod w it h infect ed seeds. Depen din g on where cacao is grown , on e or m ore of three diseases (black pod, witches’ broom , and frosty pod rot) m ay reach epiphytotic proportion s th at cause devastatin g losses (Table 1) (8,12,36). Plant Health Progress 9 July 2001 Table 1. Est im at ed annual reduct ion in pot ent ial cocoa product ion by m aj or diseases. Re du ce d Pr odu ct ion D ise a se s Pa t h oge n Re gion ( t ons x 1000) ( $ m illion) * Black Pod Phyt opht hor a spp. Africa/ Br azil/ Asia 450 423 Wit ches' Broom Cr inipellis per niciosa Lat in Am er ica 250 235 Frost y Pod Rot Moniliopht hor a rorer i Lat in Am er ica 30 47 Sw ollen Shoot CSSV Africa 50 28 Vascular st r eak dieback Oncobasidium t heobr om ae Asia 30 28 * January, 2001: v alue = $940.00/ m et r ic t on. Source: The World Cocoa Sit uat ion, M. Taylor , LMC I nt er nat ional Lt d/ Tr ade Discussions ( 36) . In Brazil, the production of cocoa bean s has dropped from 40 0 ,0 0 0 to 10 0 ,0 0 0 m etric tons in just 10 years, largely as the result of the in fection by the fun gus, Crinipellis pern iciosa. This fungus has spread beyond Brazil in to Peru, Ecuador, Venezuela, and Colom bia in South Am erica, and Panam a in Central Am erica. The pathogen also is on the Caribbean islands of Trin idad and Tobago (28,31). A second fun gus, Mon iliophthora roreri, causes an other very dam agin g disease, frosty pod rot, that also destroys the cacao beans inside the pods (7,11). Th is path ogen has not yet m oved in to Brazil, but has m oved beyond Panam a in Central Am erica in to Costa Rica and Nicaragua. Vast num bers of air-born e spores of the fungus, that give the pods a frosty appearance, will undoubtedly spread the disease to other cacao growin g region s (11). Th e disease that causes the m ost widespread destruction of cacao worldwide is black pod, which is caused by several species of Phy tophthora, a fungus-like m icroorgan ism that com es in several form s (13). The m ost widespread species are foun d around the world in all cacao growing areas, and cause sporatic losses. One species, P. m egakary a, is spreadin g throughout West Africa, the world’s prem ier cacao growin g area, an d causes m ajor losses (14). Vascular streak dieback, caused by Oncobasidium theobrom ae, is foun d on ly in Asia (30 ,42), and swollen shoot virus disease, foun d on ly in West Africa (37,38 ), are of relatively m in or im portan ce com pared to the other abovem entioned diseases (10 ). Many factors contribute to a decline in production of cocoa beans worldwide, in cludin g in sect infestations, social pressures to grow other crops, econ om ic issues that discourage lon g-term com m itm en t of sm all acreage farm ers to grow the crop, and societal pressures to destroy rain forest environm ents. Plan t diseases are m ajor com pon en ts of the declin e in production. We as plan t pathologists an d m icrobiologists have as our m andate to discover and devise m ean s to reduce disease losses and to save chocolate for the enthusiastic con sum ers of the world. Plant Health Progress 9 July 2001 Bla ck Pod Black pod disease of cacao is an econ om ically serious problem in all areas of the world where cacao is grown (Fig. 5) (4,8 ,10 ,12,13). Annual losses due to black pod m ay range from 30 -90 % of the crop. This disease is especially severe in West and Central Africa which contributes 60 -70 % of the world production of cocoa beans. Th e disease is caused by a com plex of species of Phy tophthora (the gen us nam ed by An ton de Bary in 1876 as “plant destroyer”) (5). These pathogen s are fun gus-like m icroorgan ism s with a world-wide distribution . Species of Phy tophthora are pathogens on m ost econ om ically im portan t crops grown throughout the world, such as P. in festans, the cause of late blight of potato (6). Previously, isolates of Phy tophthora from cacao were classified as P. palm iv ora (Butl.) Butler (4). Fig. 5. Cacao t ree w it h Th is species has been recogn ized as on e of the m ost healt hy pods on t he left , and pods w it h black pod im portant pathogens in the tropics attacking m any disease on t he right . plantation crops, in cludin g cacao, rubber, black pepper, cocon ut, pin eapple, an d papaya, as well as citrus, avocado, an d m an y ornam en tal plan ts. Early studies of the pathogen revealed som e variation in the m orphology and types of lesion s produced on cacao pods am on g isolates from differen t coun tries. In 1976, isolates of P. palm ivora from cacao were placed in to one of four m orphological groups (MF1, MF2, MF3, an d MF4) (15). Further studies redefin ed the m orphological groups. Th e MF1 form was con sidered to be the typical P. palm iv ora, an d the MF2 form a variant (atypical) of P. palm iv ora (4). The MF3 form was described as a n ew species, P. m egakary a Brasier and Griffin (4), and the MF4 form considered to be P. capsici Leon ian (39,43). Recently, it has been proposed that isolates of P. capsici differing in m orphological an d pathological attributes should be called P. tropicalis (2). Phy tophthora palm iv ora is presen t in m ost coun tries an d is an im portan t part of the black pod com plex, while P. m egakary a is presen t on ly in several coun tries in West Africa (14). However, P. m egakary a appears to be m ore virulent than P. palm iv ora and is becom ing the dom inant species in West Africa, m ovin g from Nigeria an d Cam eroon into coun tries where it has not been reported previously. In the m ajor cacao-growing region of Bahia, Brazil, three species have been im plicated: P. palm iv ora, P. capsici, an d P. citrophthora (Sm ith an d Sm ith) Leon ian (17,22,24). Phy tophthora capsici appears to be the dom inant and m ost im portant species attacking cacao in Brazil, and also has been reported to occur in oth er coun tries in Cen tral and South Am erica, as well as in th e West In dies, In don esia, an d In dia (6). Phy tophthora citrophthora is the least com m on species foun d in Brazil, but is th e m ost virulent (17,24). Phy tophthora heveae Thom pson also has been foun d to cause black pod in som e coun tries (6). Although Phy tophthora species attacks all parts of the cacao plan t, the m ajor econom ic loss is from infection of the pod (Fig.6) (10 ,13). Pods or cherelles (im m ature pods) m ay be in fected at any place on the surface, but infection is m ost often in itiated at the tip or stem end. The disease causes a firm , spreadin g, chocolate-brown lesion that eventually covers th e whole pod. The beans inside the pod m ay rem ain un dam aged for several days after in itial in fection of th e husk, thus frequent harvests m ay preven t m uch yield loss. In advan ced in fection s, Phy tophthora invades the in ternal pod tissues and causes discoloration an d shriveling of the cocoa beans. Diseased pods eventually becom e black an d m um m ify. The pathogen also will cause a seedlin g blight in cacao nurseries as a result of infection of the stem and youn g leaves (Fig.7). Plant Health Progress 9 July 2001 Fig. 6. Black pod disease of cacao caused by P. capsici in Cost a Rica. Fig. 7. Seedling blight of cacao caused by P. m egakar ya. Th e inoculum th at in itiates black pod can com e from the soil and/ or infected roots, stem s, and leaves (5,10 ). Root in fection from residual soil inoculum usually is not an econom ic con cern , however, the pathogen is capable of producin g spores on all in fected plant parts. Thus, infected roots m ay serve as a source of in oculum for in fection of th e pods. Bark an d stem cankers m ay fun ction in the sam e m anner. Once a pod is in fected and sporulating, it m ay then provide a m assive source of in oculum to in fect other pods. Under hum id conditions, sporangia (asexual reproductive structures and a source of secondary in oculum ) m ay form on the surface of in fected roots, can kers, or diseased pods (Fig. 8) (14). This type of propagule can be dispersed by rain fall, splashin g Fig. 8. Sporangia of P. m egakar ya for m ing on t he water, and water m oving over the surface of the soil surface of an infect ed pod (5). When sporangia are in free water, zoospores are in Cam eroon ( court esy form ed in side the sporangia an d released into the Pierr e Roger Tondj e) . water (Fig. 9). Zoospores are m otile spores that actively swim towards an in fection site an d are the prim ary in fective propagules. Thus, win dborn e rain is a prim ary factor in the spread of the disease. Ants also have been reported to tran sport in oculum . Fig. 9. Sporangium and zoospores of P. m egakar ya. Con trol of black pod is difficult because Phy tophthora can persist in soil an d debris for several years (5). Also, since susceptible pods m ay be present on the trees m ost of the year, the pathogen m ay always be presen t in the can opy, ready to cause m ajor epidem ics when en viron m en tal con ditions becom e favorable for sporulation and dispersal (10 ). Frequent harvestin g will lessen the dan ger of spread of the disease from in fected pods (34). Regular prun in g to rem ove Plant Health Progress 9 July 2001 in fected chupon s (sm all suckers at the base of the tree) and in crease air circulation (to reduce the hum idity under the can opy) is an im portan t disease m anagem ent tool. Other m easures, such as the rem oval of in fected pods an d husk piles, m ay have som e effect on in oculum levels. However, un der high rainfall conditions, it is difficult to effectively suppress the inoculum to attain good con trol (10 ). Chem ical con trol relies on th e use of copper an d m etalaxylbased fun gicides. H owever, these are n ot en tirely effective, are expen sive for the sm all farm er, and n ot econ om ically feasible (12,27). Addition ally, there are environ m en tal con cerns regardin g th e heavy use of chem icals in the tropical rainforests, and there m ay be problem s with non -target effects an d resistan ce of the pathogen. At present, there is n o acceptable gen etic resistan ce in cacao to con trol black pod. Active research is un derway throughout the world on this im portant disease of cacao. Control m easures being investigated are aim ed at in tegrated pest m an agem en t (IPM) strategies, and in clude biological con trol m icroorgan ism s, genetic and induced resistance, cultural practices, natural products, and lim ited use of chem icals (18 ). W it ch e s’ Br oom Witches’ broom disease, caused by the fun gus Crinipellis pern iciosa (Stahel) Sin ger (form erly Marasm ius pern iciosus), was first reported in 18 95 from Surin am and is curren tly foun d in several coun tries of South Am erica an d the Caribbean islands (31,40 ). The disease is initiated by basidiospores produced an d released from pin kish m ushroom s called basidiocarps (Fig. 10 ), that are dispersed by wind an d rain on to leaves, flowers, and fruit (pods) of cacao plants. It is estim ated that a sin gle basidiocarp can release 8 0 to 90 m illion basidiospores. In the presen ce of free m oisture (rain an d dew) an d high relative hum idity, basidiospores germ inate an d pen etrate youn g m eristem atic tissues in vegetative and floral buds through stom ata, epiderm is, or trichom es. The colon ized tissues un dergo several physiological and horm on al chan ges Fig. 10. Basidiocarp of C. leadin g to swelling an d form ation of num erous perniciosa ( cour t esy Scot t Bauer, ARS I nform at ion succulent vegetative branches, known as broom s, St aff) . within flower cushions (Fig. 11) an d on vegetative apical (Fig. 12) or axillary buds (26). The broom s are usually form ed within 5 to 6 weeks following infection. The fun gus also in fects pods causing n ecrotic lesion s, un even ripen ing, an d various deform ation s. Broom s and in fected pods becom e progressively brown and dry, and within 3 to 8 m onths following broom an d pod drying, basidiocarps (Fig. 13) are form ed followin g several altern atin g wet and dry periods. Fig. 11. Veget at ive branches ( broom s) arising from a flow er cushion infect ed by C. perniciosa. Plant Health Progress 9 July 2001 Fig. 12. A dr y broom for m ed fr om infect ion of an apical veget at ive bud by C. per niciosa. Fig. 13. Basidiocarps ( pinkish st r uct ur es) form ed on a dry broom and pod infect ed wit h C. per niciosa. Witches’ broom debilitates cacao trees by diverting en ergy to the num erous broom s that do not form flowers, thus reducin g yield poten tial. Further yield loss is in curred by the preven tion of seed form ation in pods in fected early in their developm en t. If seeds are form ed prior to infection they m ay be un usable dependin g on th e extent of pod colonization by C. perniciosa (Fig. 14). In its natural habitat of the Am azon ian forest, cacao is foun d as scattered under story trees which are genetically variable, a characteristic Fig. 14. Cacao pod infect ed w it h C. that ham pers the developm ent of perniciosa show ing lesion on t he surface epidem ics of witches’ broom . The and ext ensive r ot t ing of t he seeds cultivation of cacao has intensified over ( court esy Jose Rondon and Orlando Ar guello) . the years as cocoa has progressively becom e a global trade com m odity. Production environ m en ts that en courage the plantin g of cacao varieties with little genetic diversity ensures a constant supply of susceptible tissue for in fection by C. perniciosa. Managem ent of witches’ broom has received considerable attention from the beginn in g of the 20 th cen tury (10 ,12,28 ,31,40 ). Broadly, there are four m ajor strategies that m ay be adopted: phytosanitation, chem ical control, genetic resistan ce, an d biological con trol (18 ). Phytosan itation, by rem oval an d destruction of diseased plant parts, has been shown to reduce pod loss and delay disease epidem ics (32,34). However, this strategy is tedious and in on e study it has been shown that 95% rem oval is required to achieve 50 % reduction in pod loss (32). Chem ical control of witches’ broom with protectant an d system ic fun gicides is n ot a routin e practice in cocoa production because of high costs an d risks associated with cocoa bean contam ination an d environm ental health (10 ). The developm en t of gen etically resistant cacao cultivars is an on -goin g endeavor in m any coun tries, an d it is expected that the use of these cultivars would reduce the inciden ce of the disease. Prospects of m an agin g witches’ broom disease of cacao through biological con trol have been investigated for over 20 years leadin g to the isolation of a n ew species, Trichoderm a strom aticum , a parasite on the m ycelium and basidiocarps of C. perniciosa (33). In Brazil, com m ercial form ulations of T. strom aticum are currently used in m anaging witches’ broom . H owever, the in consistent perform ance of T. strom aticum indicates the need to further understand the relation ship between the cacao plantation environm ent and the Plant Health Progress 9 July 2001 survival and establishm ent of this m ycoparasitic fungus. Collaborative research efforts by scientists at research institutions in the United States and Cen tral an d South Am erica are curren tly un derway to optim ize the use of T. strom aticum . Fr ost y Pod Rot Frosty pod rot (or Moniliophthora pod rot), caused by Mon iliophthora roreri (Ciferi & Parodi) Evans et al., originally described in 1933 as Mon ilia roreri, is a devastatin g disease of cacao pods (7,11). The conidia (the on ly known in fective propagules) in fect by pen etratin g the surface of the pods. Th e pods are highly susceptible durin g th e first 90 days of their growth. Early sym ptom s include discolored areas of swelling on the pods followed by a den se form ation of cream -colored spores, the so called frosty pod, developin g on the pod surface within 2 weeks after Fig. 15. Fr ost y pod rot of cacao caused by M. in fection (Fig. 15). The area of the ror er i w it h w hit ish t o cream y- colored spores on t he pod surface. pod with sporulation spreads rapidly, an d spore densities have been estim ated to be as high as 44 m illion con idia per square cen tim eter (7,12). The spores are later released by win d or by water droplets durin g rain y periods. Frosty pod rot occurs on all Theobrom a and related Herran ia species. The first report of the disease was by J . B. Rorer (1917-1925) while on a scien tific trip to Ecuador to in vestigate serious losses in yields due to diseases (7). Frosty pod rot curren tly is restricted to northwest South Am erica (Ecuador, Peru, Colom bia) and south Central Am erica (Nicaragua, Costa Rica and Panam a). However, it is an im m ediate threat to Brazil, which is one of th e largest cacao growing areas in South Am erica. Yield losses have been estim ated between 25% to total loss of th e crop if frequen t (7-10 day schedules) phytosan itary m easures are n ot im plem en ted (34). The m ost econ om ical way of con trolling the spread of this disease is to elim inate the inoculum sources, which are dead sporulatin g pods (Fig. 16), with frequen t harvests on regular cycles (32). Other practices should in clude reduction of tree height (m axim um 3.5 m ) to facilitate rem oval of diseased pods, biological control, an d planting of resistant or tolerant cultivars as they becom e available. Fig. 16. Tr ees in abandoned plant at ions w here t he pr esence of dead pods covered w it h spores of M. ror er i is a const ant source of inoculum . Plant Health Progress 9 July 2001 In view of th e difficulty in fin ding a practical and cost-effective fungicidal treatm ent, alternative control strategies, such as biological control are being investigated in Peru, Panam a, an d Costa Rica to m anage frosty pod rot (18 ,19,20 ,34). This in volves the use of naturally occurrin g fungal agents (m ycoparasites) capable of parasitizing the pathogen and preven tin g the dispersal of fungal spores (Fig. 17). Saprophytic fungi belonging to the genus Trichoderm a and Clon ostachy s, selected for their parasitizing capacity, are bein g tested in field trials (29). BiFig. 17. I nfect ed pod sprayed w it h weekly to m onthly sprays of biocon trol biocont r ol agent s ( left ) reduce spore agen ts have been shown to reduce the dispersal by parasit izing t he pat hogen production of con idia on diseased pods m ycelium and spor es ( not e t he cr eam (19). Biocon trol treatm ent along with colored, parasit ized spores) . The pod on phytosanitation has reduced pod loss t he right w as not sprayed ( court esy W. Sober anis and H. Gom ez, SENASA, Per u) . an d increased yields in previously aban don ed cacao plantation s (19). Major gen etic im provem en t efforts are un derway in Costa Rica, Colom bia, and Ecuador to select genotypes resistan t or tolerant to M. roreri, an d n ew hybrid clon es are bein g distributed to farm ers (Fig. 18 ). Breedin g for disease avoidan ce m ay be on e of the safest m ethods to reduce field losses, as this form of resistan ce is less vulnerable to adaptive chan ges by the pathogen s. For exam ple in Ecuador, disease losses due to M. roreri were found to be lower in trees that bring a high proportion of their total pods to m aturity during the later m onths of th e dry season s or early wet season , thus avoiding conditions that favor disease developm ent (9). Fig. 18. A cacao clone from a br eeding program in Colum bia ( court esy Jose Rondon and Orlando Ar guello) . Plant Health Progress 9 July 2001 Ge n e t ic a n d I n du ce d Re sist a n ce in Ca ca o Cacao is an open pollin ated (cross breedin g) species. This poses difficulties when trying to im prove such characteristics as bean quality and yield, or disease and insect resistance in cacao. Individual trees bearin g beneficial traits fail to produce offsprin g that consistently bear the sam e traits. When farm ers select seed from their best trees, the resultin g trees are often of poor quality, produce low yields an d are susceptible to diseases an d in sects. The only way to produce trees of un iform high quality is by vegetative propagation resulting in exact clon es of the parent tree. A n um ber of vegetative propagation m ethods have been developed. Th ese in clude low-tech rooted cuttings and grafting tech niques (Fig. 19) as well as highFig. 19. A young cacao t r ee tech tissue culture an d m icropropagation pr oduced by gr aft ing resist ant budw ood ont o suscept ible techn iques (Fig. 20 ) (23). Un fortun ately, root st ock. high -tech solution s are expensive, requirin g governm ent or industry support, and lowtech solution s are slow. Con siderin g th e in tensive pressure from diseases and in sects on the world cacao crop, these techniques fail to m eet the farm ers’ needs for high quality seedlings. A com bin ation of low-tech an d high-tech m ethods has been worked out an d offers hope for the production of large n um bers of high quality seedlin gs in the future. Fig. 20. Cacao plant let s pr oduced in t issue cult ur e. Th ere is great potential for accelerating the im provem ent of cacao using traditional plant breeding enhan ced by m olecular gen etics techn iques (21). These techn iques allow breeders to m aintain and com bine im portant agronom ic traits controlled by m any genes, such as yield an d disease resistan ce, in their breedin g population s, and produce n ew varieties for release with fewer gen eration s to farm ers. Breeders often have lim ited Fig. 21. A m ixt ur e of pods show ing t he genet ic diversit y in a plant ing of cacao. access to the best germ plasm sources. Som e of the sources m ay h ave yet to be discovered in wild populations in South an d Cen tral Am erican forest or m ay be located in collections separated by great distan ces and nation al boundaries. Th rough in tern ational collaborations, scien tists usin g m olecular techn iques are attem pting to catalogue and characterize the genetic diversity in the world's cacao population s, in cluding both wild an d cultivated population s. It is estim ated that there are 18 ,0 0 0 cacao accession s in collections worldwide, and these accession s can be grouped into 250 0 to 30 0 0 genetic groups (Fig. 21). An Plant Health Progress 9 July 2001 addition al 30 0 to 50 0 genetic groups m ay exist in wild population s. As m ore is learned about the world's cacao population s, we should be better able to exploit this valuable resource to im prove not only production of chocolate, but the lives of m any sm all farm ers depen den t on cacao production worldwide. The com bination of m odern plant breeding and plan t propagation techniques should allow these im provem en ts to have an im pact on global cacao production m ore rapidly than ever thought possible in th e past. Th e genetic control of disease resistance traits can be sim ple, in volving a sin gle gene, or com plex, in volving m any genes. Resistance to disease in cacao has been identified in som e cases, but lim itation s to in creasin g th e n um ber of trees carryin g those traits preven t their wide spread use. In addition , pathogen populations differ between cacao production areas, so resistan ce that is effective in on e area m ay totally fail to provide disease control in an other area. Novel disease Fig. 22. Fungal endophyt es being st udied control m ethods such as biological for t heir abilit y t o cont r ol diseases on con trol usin g beneficial cacao. m icroorgan ism s (Fig. 22), in som e cases, can function regardless of the genetic background (16,33). Biocon trol offers a potential control strategy for the cacao trees presently un der cultivation. Most, if not all, plant species possess the ability to resist disease developm en t. Disease develops when the plan t's defense m ech an ism s are not activated. This phen om en on has provided the ration ale behind the developm ent of a new class of disease control com pounds that activate plant defense m echanism s allowing an oth erwise susceptible plan t to protect itself (25,35). These types of com poun ds are n ow bein g tested for disease m anagem ent in cacao (1). Som e of the sam e factors that lim it the potential for using traditional chem ical control m easures lim it the use of biocon trol. Cacao is often grown in rem ote areas and as an un derstory tree. This situation, com bined with the low m arket value for the product an d the high cost of supplies an d labor, often m ake an y disease con trol strategy requirin g regularly scheduled application s financially im practical. Perhaps an optim um disease m anagem ent strategy would be to identify beneficial m icroorganism s that persist in the cacao canopy an d root system s an d provide disease con trol with out regular spray application s. Th ese types of organ ism s, epiphytes, en dophytes, an d m ycorrhizae exist in cacao an d are currently bein g studied for their beneficial effects (3). It is possible that m icroorgan ism s that induce resistan ce to disease an d insects in cacao can be identified. The use of these m icroorgan ism s could result in lon g term disease control with lim ited cost to th e farm er and could actually be beneficial to the environ m en t. Su st a in a b le Ca ca o Pr odu ct ion Th e chocolate industry is keen ly aware of the requirem en t for an adequate supply of cocoa beans of consistent quality. Therefore, it is essential that the in dustry and all its associated institutions an d interests support scientific research on cacao and its products in key areas such as production, in tegrated pest an d disease m anagem ent, germ plasm con servation an d im provem ent, an d biotechn ology. The cacao research com m un ity is in tern ation al in scope. In dustry, trade organization s, govern m ent, and non-governm ent organizations support the com prehen sive effort to address ecological, social, pest and disease m an agem en t, econom ic, and cacao im provem en t con cern s. The USDA/ ARS alone has form al and inform al research agreem ents with m any organization s, in cludin g those listed in Table 2, an d with other governm ent and nongovernm ent organizations, an d universities. Plant Health Progress 9 July 2001 Table 2. Organizat ions wit h for m al or infor m al r esearch agreem ent s wit h USDA/ ARS. Or ga n iz a t ion Cou n t r y ACRI USA M&M MARS CORP. USA USAI D USA CI CAD OAS CABI - BI OSCI ENCE UK SENASA Per u CEPLAC/ CEPEC Brazil CORPOI CA Colom bia CATI E Cost a Rica I RAD/ I I TA Cam er oon Sm it hsonian I nst ( STRI ) Panam a Univer sit y of Mary land USA Penn St at e Univer sit y USA D 2 Biot echnologies USA To th is end, the basis of such an in itiative is the developm ent and prom otion of sustainable cacao agriculture, defin ed by The Am erican Cocoa Research In stitute (ACRI) as, “...the production practices in which the sm all acreage farm er increases or m aintains productivity at levels that are econ om ically viable, ecologically soun d, an d culturally acceptable, through the efficien t m an agem en t of resources.” Cultivation of cacao within a sustain able, biologically diverse agricultural system also provides habitat to im portan t forest and m igratory bird and m am m al species (41). In Central and South Am erica an d in Africa, strategic preservation of rain forest rem n ants an d the developm en t of forest lin ks h ave offered hope to efforts to preserve rain forest en viron m en ts. Sustain able cacao will not only help the cocoa and chocolate m anufacturers m aintain a constant an d reliable supply of raw m aterial, but it also will aid in the global efforts to con serve tropical forest ecosystem s an d m ove sm all holder farm ers into a m ore favorable econ om y. Accordin g to Youn g (41), prehistoric peoples in Mesoam erica had the correct approach to farm in g cacao. Relatively sm all cacao orchards enclosed by forest or set within sm all, diversified plots of various crops within the forest optim ized the chan ces for high productivity. Pollination and containm ent of diseases and in sects under these conditions m ay have been better than what is typically foun d in large, m onoculture-type plan tation s today. The challenges of disease epiphytotics, insect infestations, poor pollination, and chem ical fertilization were m inim ized because of the practices of the Mayan s, Aztecs, and other m esoam erican people. They kn ew that growin g “the food of the gods” in sm all groves reaped con siderable harvests. Understandin g the com ponents of cacao crop m anagem ent is essential to growing sustainable cacao. The im pact of diseases such as black pod, witches’ broom , and frosty pod rot will contin ue to be devastatin g until progress is m ade to control these diseases. Short term solution s such as chem ical fun gicides are often cost-prohibitive, m ay be dam aging to the environm ent, and leave un desirable residues in the product. Long term solutions such as biotechn ological approaches or breedin g for disease resistance are tim econsum ing to develop and are not readily available for im m ediate application. Th e m ost im m ediate an swer to the disease problem s is to use what tools are Plant Health Progress 9 July 2001 presen tly available in an integrated approach. These in clude lim ited biological control m ethods, disease resistant m aterial, crop sanitation to rem ove diseased m aterial as a source of inoculum , an d cultural practices such as shade optim ization, prun ing, and soil fertility m anagem ent. As stated by Youn g (41), th e cacao tree is truly a creature of n ature an d is cultivated in a relatively prim itive way com pared to m odern row crop agriculture. It m ay be com pelling to protect the tropical ecosystem s that are still left to ensure the world’s coveted supply of ch ocolate an d at the sam e tim e preserve m any m ore biological riches in tegrated in to the com plex fabric of tropical diversity. Lit e r a t u r e Cit e d 1. An eja, M., and Gian fagna, T. 20 0 1. 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Pages 291-295 in: Proc. 7th Int. Cocoa Res. Conf, Douala, Cam eroon, 4-12 Nov., 1979. J . de Lafforest, ed. Tran sla-Inter Ltd, Lon don. Plant Health Progress 9 July 2001 Ele ct r on ic Re sou r ce s for Fu r t h e r I n for m a t ion The Am er ican Cocoa Research I nst it ut e I nt ernat ional Cocoa Organizat ion Cacao I nt egr at ed Pest Managem ent - Ohio St at e Universit y Cocoa Black pod Wit ches' Broom Monilia Pod Rot Theobr om a cacao - Purdue Univ ersit y - Cent er for New Crops & Plant Pr oduct s Theobr om a cacao - Univer sit y of Louisiana Diseases of Cacao - Com m on Nam es of Plant Diseases Chocolat e I nfor m at ion Cent er - Mars, I nc. Cacao - Science Museum of Minnesot a Plant Health Progress 9 July 2001