The History of Cacao and Its Diseases in the Americas

Cacao, Theobroma cacao, the source of chocolate, is a tropical crop originating in South America (Motamayor et al. 2002). It has been important throughout the history of the Americas: fruits played a role in pre-Columbian spirituality; beans constituted the earliest form of currency; consumption as a beverage by indigenous people captivated Spanish conquerors and drove the intensification of cultivation; and the invention of chocolate candy increased demands from Europe, met by more widespread cultivation in Latin America, and eventually into other tropical areas (Dand 1997). Today, cacao is a pantropical crop that supports more than 6 million farmers in developing countries (Wickramasuriya and Dunwell 2018). The spread of cacao to places outside of its center of origin has brought many inherent issues including increasing demands for labor, especially during the colonial period, and the emergence and dissemination of diseases and pests. The problem of diseases (Fig. 1) has been confounded due to the narrow genetic background of cultivars used all over the world (Bartley 2005; Ploetz 2006). Currently, diseases alone account for approximately 38% of global cacao losses (Marelli et al. 2019). Political decisions have also impacted cacao cultivation and the people who produce it, and include subjection of people, reckless explorations for new cultivars, and even collapse of economies. The aim of this review (Fig. 2) is to provide a broad, chronological account of the most important events and human decisions that have had an impact on cacao cultivation, from pre-Columbian (Fig. 3) to colonial (Fig. 4) and republican times (Fig. 5). The movements of cacao germplasm are described, as are the societal issues resulting from cacao cultivation in the Americas. Finally, this review explores how cacao diseases have driven the market, and by extension local and global economies (Table 1).

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TABLE 1 Summary of cacao disease events referred to in the text

Event	Place	Year	Implications	Reference
Putative earliest record and outbreak of Ceratocystis wilt, documented as “alhorra” disease	Caracas province, Venezuela	1630s	More than half of trees in the coast of La Guaira were destroyed, some plantation owners experienced 100% destruction and national production did not recover until the 18th century.	Ferry (1981)
Putative second major outbreak of Ceratocystis wilt, documented as the “blast” disease	Trinidad and the Caribbean	1720s	Trinidad went from producing the best cacao (Criollo) in the world to an accelerated collapse, heavily decimating country’s economy. The introduction of Amelonado cacao allowed the natural hybridization with Criollo cacao and the development of Trinitario cacao.	Motamayor et al. (2003); Motilal and Sreenivasan (2012); Leiter and Harding (2004)
Putative earliest observation of witches’ broom disease (WBD), documented as “lagartão” disease	Barcelos municipality, Amazonas, Brasil	1783–1786	The “lagartão” or WBD disease was severely affecting cacao farmers (rapid spread and able to kill trees within 2 years of planting) of present-day Amazonas state. In this way, WBD started to appear as one of the most catastrophic cacao diseases in the Americas.	Silva (1987); Viera (1942); Supplementary Table S1
Putative earliest observation and outbreak of frosty pod rot (FPR) disease, documented as “la mancha” disease	Norte de Santander, Colombia	1817–1850	Farmers from Cúcuta were affected and government helped by reducing cacao-related taxes. “La mancha” expanded to the entire Norte de Santander and by 1950 plantations in Cúcuta disappeared.	Phillips-Mora (2003)
Outbreak of an unknown diseasea	Caracas province, Venezuela	1820s	Destruction of plantations and introductions of Trinitario cacao to the country.	Reyes and Capriles de Reyes (2000)
First report and spread of WBD	Surinam	1895–1920	By 1920, the disease spread to the entire country and even reached British Guiana. Wild cacao relatives were found to be infected.	Myers (1930); Supplementary Table S1
First report of FPR	Guayas, Ecuador	1895	Most of pods in the farm where FPR was reported were affected and useless. First case in the country which would suffer a lot in the upcoming years.	Phillips-Mora (2003)
First report of WBD	Guayas, Ecuador	1918	Contributed to the cacao crisis Ecuador started to have because FPR.	McCook (2002); Pound (1938)
FPR and WBD epidemic	Ecuador	1916–1931	National cacao production collapse: reduction of 60% and national economic crisis. It led to the discovery of Refractario cacao.
First report of WBD	Trinidad	1928	WBD eventually caused a reduction of more than 80% in the next 50 years. WBD motivated F. J. Pound’s expeditions into the Amazon.	(Laker et al. 1988)
Outbreak of WBD	North eastern Venezuela	1937	WBD caused the abandonment of plantations in Delta Orinoco region and spread to Sucre and other states in eastern Venezuela.	(Parra et al. 2009; Reyes and Capriles de Reyes 2000)
First report of FPR	Maracaibo, Venezuela	1941	FPR affected western Venezuela where Criollo cacao was cultivated and most farmers switched to other crops.
Outbreak of Ceratocystis wilt	Aragua, Venezuela	1940s	Reports indicated the disease killed half a million of Criollo cacao trees. Bad governmental policies in the following decades lead to the almost complete destruction of cacao production.
First report and epidemic of FPR	Costa Rica	1978	Collapse of cacao production that continues nowadays being scattered and tiny compared with what it was before FPR arrival.	(Phillips-Mora 2003)
First report and epidemic of FPR	Amazonas, Peru	1988, 1990s	Incidence greater than 50% in various provinces of Amazonas department, rapidly disseminating to other departments causing production declines. By 2000, 16,500 ha of cacao had been abandoned because of FPR.	(Krauss and Soberanis 2001; Phillips-Mora 2003)
Epidemic of WBD	Bahia, Brazil	1989	Sharp decline of cacao production in Bahia and economic crisis in the country.	(Caldas and Perz 2013)
First report and epidemic of FPR	Alto Beni, Bolivia	2012	By 2015, losses caused by FPR in Alto Beni were estimated in 54%.	(Phillips-Mora et al. 2015)
First report and epidemic of FPR	Jamaica	2016	First case of FPR in the Caribbean having devastating consequences to cacao production.	(Johnson et al. 2017)

^a No symptoms of the disease found in the literature.

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CACAO GERMPLASM

Cacao was traditionally classified into two major groups: Criollo and Forastero (Cheesman 1944). Criollo cacao was cultivated by pre-Columbian people from Mesoamerica, where it was introduced from southwestern Venezuela and northeastern Colombia, and has a narrow genetic background as the result of a single process of domestication after being separated from its most ancestral closely related population (Cornejo et al. 2018; Motamayor et al. 2002). Criollo beans are superior in quality but the trees are susceptible to diseases (Cuatrecasas 1964). Forastero refers to all other forms of cacao, and inherently has a more diverse genetic background (Cheesman 1944). A third term, Trinitario applies to hybrid cultivars between Criollo and Forastero (Cuatrecasas 1964). Trinitario cacao appeared after the cacao production downfall in Trinidad in the 1720s due to a disease, referred to as the “blast” or “blight” (Dand 1997; Leiter and Harding 2004). Trinitario cacao combines the qualities of Criollo with the disease tolerance of the Forastero (Cuatrecasas 1964). However, the term still comprises a variable cacao group. Molecular characterization of cacao germplasm with microsatellite markers distinguishes 11 genetic clusters: Criollo, Marañon, Curaray, Iquitos, Nanay, Contamana, Amelonado (which was shown to be the parental genotype for the old Trinitario group; Motamayor et al. 2003), Purús, Guiana, Nacional (Motamayor et al. 2008), and Nacional Boliviano (Zhang et al. 2012). Therefore, the Forastero cacao comprises 10 current genetic clusters. Furthermore, in Peru there are three recognized native cacao cultivars: ‘Chuncho’ cacao, ‘Cacao Amazonas Peru’ (which has a protected designation of origin; INDECOPI 2016), and ‘Blanco Piurano’ (which has Nacional ancestry but conserves its unique varietal status; Arevalo-Gardini et al. 2019), which have unique organoleptic properties (García Carrión 2010; Guimac Cedillo 2017; Quiñones et al. 2018; Roca and Medina 2018; Rojas et al. 2017).

CENTER OF ORIGIN

Different centers of origin for cacao have been proposed: Mesoamerica (Miranda 1962; Mora Urpi 1958), South America (Cheesman 1944), or a combination with a Mesoamerican origin for Criollo and a South American for Forastero (Cuatrecasas 1964). The main driver for the Mesoamerican hypothesis was the presence of putative wild cacao in the Lacandon forest, Chiapas, Southern Mexico. However, Motamayor et al. (2002) showed that the putative wild cacao in the Lacandon forest has the same genotype as Criollo cacao, and that Mesoamerican Criollo itself originated from a few individuals from Southwestern Venezuela in a “founder effect” fashion. Most efforts pinpointing the origin within South America support an Upper Amazonian origin. A study including most of the countries where cacao is cultivated found that cacao samples with the highest allelic diversity come from the Upper Amazonian regions of Peru and Brazil (Motamayor et al. 2008). These results were corroborated by other studies (Osorio-Guarín et al. 2017; Thomas et al. 2012), supporting that the Peruvian and Ecuadorian Upper Amazon and the Amazonian region shared by Peru, Colombia, and Brazil represent the most likely center of origin of cacao.

CENTERS OF DOMESTICATION

The origins of domestication and usage of cacao have been the focus of hot debate. It was accepted that cacao was domesticated and first cultivated in Mesoamerica by the Mayans ca. 1500 B.P. (Motamayor et al. 2003). However, bioarcheological studies over the last decades have contributed to a revision of this date. First, the discovery of theobromine—the main alkaloid in cacao—residues in Preclassic Mayan pottery pushed the earliest cacao usage back to 2550 to 1700 B.P (Powis et al. 2002). Then, similar analyses demonstrated the use of cacao in Mesoamerica dating to the Olmec society 3800 to 3000 B.P. (Powis et al. 2011). State-of-the-art biochemical, spectrometric, and molecular analyses of pottery vessels found in Palanda, Ecuador from the Mayo-Chinchipe-Marañon culture based in Upper Amazon at the border of Ecuador and Peru revealed not only that cacao was consumed as early as 5450 to 5300 B.P. but that the earliest known center of domestication was in the Upper Amazonian region of South America as opposed to Mesoamerica (Zarrillo et al. 2018). Therefore, science now points to both the center of origin and the earliest center of domestication of cacao as having occurred in the same region of the Upper Amazon of South America.

CULTIVATION OF CACAO AND MOVEMENTS OF GERMPLASM

Pre-Columbian era.

Mesoamerica.

The introduction of cacao to Mesoamerica has also been debated. The ancient people from the coast of Ecuador (e.g., the skilled Valdivia culture which spanned from 6000 to 3200 B.P.) may have influenced the development of civilizations in Peru and Mesoamerica by maritime communication and exchange of products. One early hypothesis is that cacao was introduced to Mesoamerica by Valdivia traders via Pacific Ocean routes (Wolters 1999). However, this was rejected by molecular studies clearly showing Criollo cacao in Mesoamerica came from Venezuela and Colombia (Motamayor et al. 2002) via inland routes, supported by the fact that colonialists did not find cacao in the Caribbean islands during conquest (Bergmann 1969).

Once Criollo cacao reached Mesoamerican pre-Columbian societies, it became the top agricultural product for centuries. Its cultivation was mainly restricted to specific districts in the humid and warm lowlands of the Gulf of Mexico (Tabasco, Mexico), Pacific Ocean (Soconusco, Chiapas, Mexico; Suchitepéquez, Guatemala; and Izalco, El Salvador), the Caribbean (Sula Valley, Honduras) inland coastlines, Lacandon Jungle (Chiapas, Mexico), and Petén Basin (Guatemala), which all underwent intensive production; additionally, there were semi-intensive and minor cacao-producing regions scattered from the lowlands of as north as Colima, Mexico to as far south as Quepos, Costa Rica (Barrera and Fernández 2006; Bergmann 1969). It is estimated that cacao-producing areas under the Aztec realm sent annually at least 22 tons of cacao beans to the capital Tenochtitlan as tribute before Spanish conquest (Millon 1955).

South America.

In pre-Columbian South America, cacao was valued in its wild state for the pulp, which was eaten directly or squeezed for juice to make fermented beverages, while the beans were discarded (Clement et al. 2010). This is true for several indigenous groups such as the Machiguengas in Amazonian Cusco, Peru (Roca and Medina 2018; Rojas et al. 2017) and the Tukuna in the Colombian Amazon, among others (Bletter and Daly 2006). Indigenous groups from what is now Brazil and French Guiana may have even started a “proto-domestication” process of cacao, selecting for pulp content, since natives had been witnessed planting wild cacao seedlings in their villages (Barrau 1979). These observations may be the result of decades of subjection by colonialists during the Amazonian cacao boom (Walker 2007). This incipient process of domestication in pre-Columbian times is supported by the high levels of homozygosity (the two highest after the homozygosity of the fully domesticated Criollo cacao) in the Amelonado and the Guiana genetic groups found in these Amazonian regions, and by their relative fruit uniformity (Clement et al. 2010; Thomas et al. 2012).

In South America there are numerous accounts that prior to the arrival of Europeans, cacao and its beans were just as important as they were in Mesoamerica. Extensive cacao plantations were maintained for producing a drink called chorote, traditional to the natives from the Maracaibo Basin, Northwestern Venezuela, prepared from roasted and ground cacao beans that differed from the Mesoamerican chocolatl drink (Méndez Ramírez 2015; Ogata 2002). The intensity of cacao cultivation in South America may have even surpassed that in Mesoamerica. For instance, a government report from 1602 mentions a 100,000-tree plantation managed by natives near the Maracaibo Lake (Reyes and Capriles de Reyes 2000). Such abundance of cacao can only be explained by human cultivation because in the wild cacao grows scattered within forests and not in high densities (Ogata 2002). Also, this cultivation must have been done by the natives; colonialists would have been unable to bring enough African slaves or laborers from Mesoamerica due to labor shortages caused by introduced lethal diseases (Lovell and Lutz 1992).

The importance of cacao in ancient Ecuador may also be underestimated. Juan López de Velasco in his accounts from the 16th century documented an abundance of cacao in the Loja province (Supplementary Table S1). Additionally, the Spanish, during their first exploration toward Peru in 1526–27, encountered “blooming plantations of cacao” in current Esmeraldas province on the northern coast of Ecuador (Supplementary Table S1). It is difficult to corroborate Prescott’s statement because his sources do not refer to cacao (Bergmann 1969). However, pre-Columbian domestication and cultivation of cacao in Ecuador was recently demonstrated in the Mayo-Chinchipe-Marañon Basin (Valdez 2019; Zarrillo et al. 2018), which make Prescott’s account more likely. It is also likely that the cacao found by the Spanish in Esmeraldas corresponded to the Nacional genetic group, which was introduced from the Upper Amazon to the coast in pre-Columbian times and likely underwent a persistent process of human selection (Loor Solorzano et al. 2012). Moreover, ancient DNA from Mayo-Chinchipe-Marañon pottery artifacts revealed that the cacao consumed in the Upper Amazon of Ecuador 5450 to 5300 B.P. are genetically more similar to Curaray and Purús groups than to the Nacional (Zarrillo et al. 2018). Nowadays, Curaray and Purús cacao can be found in the Ecuadorian Upper Amazon and their geographical range extends to the Upper Amazon in Brazil and to the Northern Amazon of Colombia (Motamayor et al. 2008). Additionally, these two cacao groups have close genetic affinities to the Criollo Mesoamerican group, suggesting they both played an important role in the domestication and further spread of the crop throughout the Amazon Basin and Venezuela in pre-Columbian times (Loor Solorzano et al. 2012; Zarrillo et al. 2018).

Cacao was also important for ancient Peruvian societies. Mayo-Chinchipe-Marañon ruins, known as Montegrande, were found in Jaen (in the Upper Amazon), which supports a hypothesis that cacao was cultivated and consumed as early in Peruvian societies as it was in Ecuador (Olivera-Núñez 2018). Moreover, there are several ancient pottery and goldsmith artifacts depicting cacao found in coastal ancient ruins or recovered from contraband (USIL 2018). The earliest evidence for cacao relevance in Peru is a 3,000-year-old ceramic vessel from the Tembladera people (North coast) depicting two Amazonian organisms: a monkey and what are highly likely to be cacao fruits (Ogata et al. 2006). This reveals that interactions between coastal and Amazonian peoples in ancient Peru occurred since at least 3500 to 2900 B.P.; they presumably exchanged cacao among other agricultural goods, which explains the presence of cacao in Tembladera’s pottery (Ogata et al. 2006). Another source of support for the relevance of cacao in ancient Peru is the “Chachapoyas” society. It flourished from 800 to 1470 A.D. in the cloud forests of modern Utcubamba province, department of Amazonas, in the junction of the North Andes and the Upper Amazon of Peru (Church and von Hagen 2008). The ‘Cacao Amazonas Peru’ cultivar is native from this region and it is highly cultivated with a protected designation of origin (INDECOPI 2016). It has been described as a “cultural step from the wild cocoas of the neighboring Amazon slope” (Soria 1970). During the 15th century, the Incas were trying to conquer the “Chachapoyas” mainly to get access to many tropical forest resources such as cacao and other agricultural and natural products (Church and von Hagen 2008; Ruiz Estrada 2017). Therefore, it is likely the “Chachapoyas” exploited the ‘Cacao Amazonas Peru’ native cultivar. Coincidentally, the “Chachapoyas” domain is in the Southeastern end of the Mayo-Chinchipe-Marañon Binational Basin, where the first known center of domestication of cacao is located (Zarrillo et al. 2018). Unfortunately, the ‘Cacao Amazonas Peru’ was not included in the genetic characterization of the more relevant studies of cacao germplasm (Motamayor et al. 2008; Thomas et al. 2012).

Colonial era.

Christopher Columbus, his brother Bartholomew, his son Ferdinand, and the rest of his crew were likely the first known Europeans to come into contact with cacao beans (Ferdinand described them as “almonds”) during their fourth voyage to the Western Hemisphere in 1502 (Supplementary Table S1). They observed how indigenous people from the North Coast of present-day Honduras transported, among other goods, high quantities of “almonds”. The Columbus men noticed how the Indians were very diligent with their cargo, but never realized the significance these “almonds” would have in the upcoming centuries (Bergmann 1969).

Mesoamerica.

The Spanish rapidly became interested in cacao after the conquest of Mexico in 1519 to 1521, when they realized that the Aztec royals and nobles consumed a special beverage, called chocolatl, made from the ground roasted cacao beans (Alden 1976). Once the viceroyalty of New Spain was established in 1535, the Spanish coerced cacao cultivation by taking over existing plantations, expanding cultivated areas and forcing indigenous people to work in cacao farms to pay imposed levies (Alden 1976). All of this was in response to the increasing local demand for chocolatl by the new settlers and even all classes of indigenous people, once reserved only for the Aztec nobility (Erneholm 1948). An example of the degree of cacao expansion during these times follows. Before the colonial period, in the beginning of the 16th century, exports as a form of tribute from Soconusco to Tenochtitlan were estimated at 5 tons per year (Millon 1955). By the end of the century, the cacao expansion allowed for the existence of 1.6 million trees in Soconusco and exports between 3,000 and 6,000 loads per year (Gasco 1987), which is equivalent to 75 to 150 tons by the calculations of Millon (1955). By this time, Spain was the only consumer of cacao in Europe and its consumption would popularize in the whole continent by the beginning of the 17th century (Dand 1997).

During the first decades of the colonial period in New Spain, the population of native people was in sharp decline due to the spread of introduced infectious diseases. For example, the population in Guatemala decreased from 2,000,000 people in 1520 to 427,850 in 1550; and in El Salvador, from 400,000 to 500,000 in 1524 to 70,000 in 1570 (Lovell and Lutz 1992). As a result, there were much fewer people working on cacao plantations. Therefore, the local supply diminished and the need to import cacao beans increased significantly by the beginning of the 17th century (Erneholm 1948). The main supplier to New Spain during this century was Guayaquil, Ecuador, where cacao was cheaper to produce, while their highly priced Criollo cacao was shipped overseas (Erneholm 1948). This would become the most representative cacao import/export pattern for the rest of the colonial period in Mesoamerica (Erneholm 1948). By the end of the colonial period, there were approximately 400,000 trees in Soconusco and exports from that region were estimated at 500 loads (12.5 tons), an 80 to 90% reduction in the total exports compared with the first decades of the colonial period (Gasco 1987).

The Lacandon society was a Mayan-derived group that resisted Spanish subjection until the end of the 17th century. They developed advanced agricultural production systems, and cacao was one of their main products (Barrera and Fernández 2006). However, in 1695 the Lacandon society could no longer resist oppression and were finally conquered by the Spanish, who exiled them from their forest; thus, their cacao plantations were abandoned and the ancestral knowledge of cultivation in the Lacandon rainforest was lost (Barrera and Fernández 2006). “Wild” cacao trees in the Lacandon forest have the same Criollo genotype and are the remnants from its cultivation in this Mayan society (Motamayor et al. 2002, 2008).

South America.

Venezuela.

It is debatable whether cacao cultivation started before or after the colonial period. Some researchers believe that Venezuelan native people practiced “collection agriculture” in which they only harvested cacao fruits from the wild, and that “plantation agriculture” started with the arrival of the Spanish (Reyes and Capriles de Reyes 2000). However, there is strong evidence that cacao was cultivated by native people from Venezuela before the arrival of Spanish (Méndez Ramírez 2015). Regardless, Venezuelan cacao, of Criollo genetic background (Motamayor et al. 2002), had a reputation of good quality and was highly prized in Europe, and there is no doubt that its cultivation was the main and most dynamic economic activity during the colonial period (Díaz 2000).

The Maracaibo Basin, Northwestern Venezuela, was the first place in South America to export cacao to Europe by the 1560s to 1570s (Erneholm 1948). However, this fertile region was practically forgotten by the Spanish who were more interested in searching for precious metals than working the land (Ogata 2002). Then, the Dutch took advantage of this and, thanks to the strategic location of the Curaçao island, they dominated the cacao exports from the Maracaibo Basin in the 17th century, mostly as contraband (Erneholm 1948; Malavé Mata 1974). East of the Maracaibo Basin, specifically in La Guaira, in the old province of Caracas, important plantations were taking form with the work of African slaves and subjected native people (Delgado 2008; Ferry 1981). Suddenly, during the decades of 1630s to 1640s, Venezuela would suffer its first cacao crisis due to a disease referred as the “alhorra” blight (Ferry 1981). The “alhorra” left cacao groves “without a single fruit-bearing plant” (Ferry 1981), destroying most cacao trees in La Guaira and spreading throughout Caracas with no signs of recovery until the 18th century (Ferry 1981). This descriptions match the symptomatology of Ceratocystis wilt of cacao (caused by Ceratocystis cacaofunesta), which causes sudden death of trees between 10 to 30 days after appearance of first symptoms (García Cabrera et al. 2016; Reyes and Capriles de Reyes 2000). Ceratocystis wilt is one of the major economically important cacao diseases in Northern Venezuela, native to South America and endemically persisting in Venezuela (García Cabrera et al. 2016; Reyes and Capriles de Reyes 2000). Ceratocystis wilt can be rapidly disseminated through the use of agricultural cutting tools (Reyes and Capriles de Reyes 2000), which can explain the magnitude of the spread of the “alhorra” in 1630s-Caracas (Ferry 1981). Therefore, it is highly likely that the “alhorra” corresponds to Ceratocystis wilt. Chambouleyron (2014b) refers to the “alhorra” as pest, which also may be a hint leading to Ceratocystis wilt, because C. cacaofunesta is also vectored by ambrosia beetles of the genus Xyleborus (García Cabrera et al. 2016; Goitía and Rosales 2001; Reyes and Capriles de Reyes 2000). It is also possible that Phytophthora palmivora (which causes stem canker and black pod rot in the Americas) (Morales-Cruz et al. 2020) may have been the causal agent of the “alhorra”. This pathogen can also colonize the cacao tree stem through wounds caused by ambrosia beetles (although this is not the main mode of dissemination) and it can cause the sudden death of cacao trees within 3 months (Reyes and Capriles de Reyes 2000; Surujdeo-Maharaj et al. 2016). However, Venezuelan phytopathological literature highlights the aggressiveness and the economic importance to the country of Ceratocystis wilt over stem canker, and its intimate association with Xyleborus spp. beetles (Goitía and Rosales 2001; Reyes and Capriles de Reyes 2000). Therefore, it was highly likely the causal agent of the “alhorra” disease. The “alhorra” outbreak in the Caracas province may be the reason why the Spanish did not establish cacao cultivation in the Maracaibo Basin during the 17th century.

In 1706, the Dutch shipped cacao from Maracaibo worth half of the Venezuela annual production to the Netherlands, which alerted the Spanish Crown (Israel 1989). The creation of the viceroyalty of New Granada in 1717 by Spain and the foundation of the Guipuzcoana company in 1728 were decisive to recover full sovereignty over the Maracaibo Basin and the cacao international trade (Ferry 1981; Malavé Mata 1974). The Guipuzcoana was the only company allowed to export cacao and other agricultural products to Spain. Because of its rigorous policies, it would double the number of planted cacao trees in the Caracas province, with the Tuy River region being the heart of these plantations (Ferry 1981). The crop then expanded to other provinces and the cacao production was fairly constant throughout the 18th century (Malavé Mata 1974). Smallholder families came together by means of arranged marriages and developed large haciendas of cacao (Ferry 1981). For example, in the Coro jurisdiction alone there were more than 1.7 million trees among 168 haciendas (Supplementary Table S1). From 1700 to 1797, cacao exports increased from 1,500 to 6,750 tons per year (Palma 1953). These prosperous times in Venezuela made hacienda families part of the elite and wealthy class of colonial Caracas (Ferry 1981). During the first half of the 18th century, Venezuela was the top cacao supplier in the world and its closest competitor was Guayaquil (Díaz 2000). After 1765, exports from Guayaquil overpassed Venezuela’s (Clarence-Smith 2000).

Ecuador.

The Nacional cacao was exclusively cultivated during the entire colonial period in Ecuador (Loor Solorzano et al. 2012). The Guayas Basin was the chief Nacional cacao-producing region, and Guayaquil was the second-largest port in the viceroyalty of Peru, after Callao in Lima. Because of the intercolonial trade restrictions in the beginning of the colonial period, the cacao production and exportation system in Ecuador was not very important (Erneholm 1948). It started to develop by the end of the 16th and beginning of the 17th centuries as the Mesoamerican native population was decreasing and local demand increased (Lovell and Lutz 1992). This made cacao a common and highly priced export to Central America during the early 17th century (Clayton 1975). Just as in Venezuela, cacao plantations were maintained by the subordination of Africans and natives under the encomienda system (Bryant 2006). Throughout the 17th century, cacao exports suffered mainly because of pirate attacks, the most important being the one in 1624 by Dutch pirates which destroyed Guayaquil and paralyzed maritime communications (Clayton 1974). Ecuador did not export to Europe because Venezuela was in a better geographical position to do so. Exports to Mesoamerica were difficult because of the colonial protection policies. Thus, contrabands and illegal exports were common during that time (Clarence-Smith 2000; Clayton 1975). Up to the first half of the 18th century, Ecuador was the second largest cacao producer in the world after Venezuela (Díaz 2000).

The middle of the 18th century was a time of conflict in Europe because of disputes for possession and redistribution of colonies and territories, culminating in the Seven Years War (1756 to 1763). This marked the beginning of a new era in colonial commerce, especially for cacao in Ecuador (Clarence-Smith 2000). In 1765, Spain enacted a decree on intercolonial trade in which taxes and regulations were greatly softened, which minimized contraband and enabled the beginning of the first cacao boom era of the country, from 1770 to 1840s (Alden 1976). According to some authors, cacao cultivation was the economic activity that supported independence movements (Suárez et al. 1993), which finally happened in 1820.

Brazil.

Sugarcane production allowed the Portuguese to settle in Brazil during the 16th century in non-Amazonian regions like Bahia and Pernambuco; but the Amazon remained impervious to conquest up until the creation of the “Estado do Maranhão” (present-day States of Pará, Maranhão and Ceará) in 1621, which favored Amazonian explorations (Chambouleyron 2014a). The economic crisis generated by the weakening of the Portuguese presence in India and the appreciation of cacao as the main economic engine in early-17th-century Caracas motivated the Portuguese Crown to enact several measures to promote cacao cultivation in “Estado do Maranhão” (Alden 1976). Although there might have been earlier ephemeral plantations, the first official cacao plantations in Brazil were established in 1674 (Alden 1976; Chambouleyron 2014a). In 1681, cacao cultivation acquired taxation and custom duty benefits which encouraged settlers to cultivate more, driving expansion (Alden 1976; Chambouleyron 2014a). Just as in other regions, expansion implied the need for more people to work, who in this case were almost exclusively Amazonian natives (Walker 2007). It was very common in the 17th century that Portuguese explorers went into the deep Amazon, and allowed by royal policies, ransomed intertribal captives to use them as a labor force (Supplementary Table S1). Since the Portuguese had noted wild cacao was very abundant along the river banks, “ransom” journeys also served to bring Amazonian resources like cacao seeds (Alden 1976). These explorations took place as far as present-day Yurimaguas, in the Peruvian Upper Amazon (Supplementary Table S1).

Despite promotion of cacao cultivation, the crop did not become an important export because it mostly came from wild trees, which only offered one harvest per year and yielded lower quality beans compared with their cultivated counterparts (Alden 1976). By the 1730s, cacao cultivation was well established and expeditions to collect wild cacao were less frequent (Miller et al. 2006). Since then, exports of cacao beans increased, averaging 600 tons/year during the prosperous and revolutionary Pombaline’s regime, 1750 to 1777 (Walker 2007). This period is referred to as the Amazonian cacao boom of the 18th century and, inadvertently, may mark the beginning of dispersal of one of the most present-day devastating diseases of cacao, witches’ broom disease (WBD). Up to this point, the cacao cultivated throughout the current states of Amazonas and Pará was from the Amelonado genetic group (Motamayor et al. 2008).

During the 1780s, the naturalist Alexandre Rodrigues Ferreira set Amazonian expeditions to study the flora and fauna of the region. Along the Negro River close to the present-day municipality of Barcelos, state of Amazonas, he encountered growers complaining about a cacao disease they called the “lagartão” (lizard in Portuguese), which was spreading out into neighboring provinces and killing trees within 2 years after planting (Supplementary Table S1). Researchers strongly believe this “lagartão” disease is WBD because infected branches adopt the shape of a lizard, suggesting Ferreira was the first to document WBD (Silva 1987; Viera 1942). This is consistent with the high genetic diversity of the causal agent, Moniliophthora perniciosa C-biotype, found in states of the West Amazon of Brazil, which provides hints into this region as to its center of origin (Artero et al. 2017).

Cacao cultivation in Brazilian Amazon expanded by approximately two-fold during the last decades of the colonial era; exports account for 753 tons in 1775 to 1,678 tons in 1818 (Erneholm 1948). Expansion of cacao cultivation into the Brazilian Amazon was very limited during this period due to the rise of the Amazonian rubber tree boom (Supplementary Table S1). Therefore, most cacao production moved to the state of Bahia. By 1746, cacao seedlings from Pará (Amelonado genotype) had been introduced to Bahia, in the current municipality of Canavieiras, and gradually disseminated throughout the state, but no official exports from Bahia were registered in the colonial period (Erneholm 1948; Motamayor et al. 2003).

The Caribbean.

The cultivation of cacao in the Caribbean during colonial times would have a tremendous impact on the crop for the next centuries. The most widely used cacao group, Trinitario, was born in this region. Here we will focus on Trinidad and Jamaica, the two largest producers in the region.

The earliest records of cacao in Trinidad date back to a Spanish introduction in 1525 (Motilal and Sreenivasan 2012) but commercially its production started around 1678 with Criollo material brought from Venezuela (Leiter and Harding 2004). Cacao was the only exported product in Trinidad by the beginning of the 18th century (Motilal and Sreenivasan 2012). Similarly, the Spanish introduced cacao to Jamaica around 1638 to 1640 (Fagan 1984) with seeds from Guatemala and maybe Caracas (Momsen and Richardson 2009), i.e., seeds of Criollo genetic background. Its production was continued by the English, after they took possession of the island in 1655 (Supplementary Table S1). However, cacao cultivation was not successful in the following years with reports of unknown “blasts” frequently registered in the literature starting in 1664 (Motilal and Sreenivasan 2012). By 1670, there were around 47 plantations yielding about 94 tons, and by 1772, there were zero plantations (Supplementary Table S1). This can be explained by a disease outbreak in the 1720s that severely affected cacao cultivation in the Caribbean, from Trinidad to Jamaica, historically referred to as the “blast” disease. Several hypotheses to explain the “blast” have been proposed (Motilal and Sreenivasan 2012), including nonscientific explanations such as religious and astronomical reasons and hurricanes even though no hurricanes seem to have hit Trinidad in those years (Reading 1990). Motilal and Sreenivasan (2012) proposed a model to explain the “blast” that combines the poor performance of the Criollo cacao on eroded soils, bad agronomic practices and low temperatures caused by the Little Ice Age. However, no other tropical crops in Trinidad and in the Caribbean seem to have suffered from low temperatures; conversely, sugarcane production experienced a sharp increase during the entire 18th century and the Caribbean became the top world supplier (Galloway 1989). Additionally, the coldest temperatures observed during the Little Ice Age took place between 1400 and 1700 (Mann et al. 2009), which does not overlap with the cacao “blast” times in the Caribbean. The most likely explanation is that a pathogen, most likely C. cacaofunesta (Leiter and Harding 2004), conjunctly with the susceptibility of the Criollo genetic background and the bad agricultural practices contributing to soil erosion, destroyed the crop. In fact, Motilal and Sreenivasan (2012) did not fully discard the possibility of biotic factors as causal agents of the “blast” and left the possibility that “perhaps” C. cacaofunesta was involved in the “blast” cacao collapse of Trinidad. Thorough population genetics studies on C. cacaofunesta may provide hints into the real cause of this epidemic.

The following years were adverse in Trinidad: cacao production stopped, smallpox spread, and people of all classes started to migrate (Momsen and Richardson 2009). There are accounts that the plantation of a farmer who cultivated a “hardier” cacao but of lower quality survived the “blast” (Dand 1997). If this was the case the resistant cacao must have been of a Forastero genetic background (Dand 1997). Nevertheless, there are no accounts of Forastero introduction to the country until 1756, which were made by Capuchin missionaries with seeds from the Amazon Basin (Bartley 2005). Thanks to this foreign introduction cacao cultivation was reintroduced (Leiter and Harding 2004). During the 19th century, Venezuelan migrants from the Paria peninsula, known as the Cocoa Panyols, would lead the resurgence of cacao cultivation in the island (Lans 2018). This golden era of cacao in Trinidad resulted in the natural development of Trinitario cacao. All the events described are consistent with the hypothesis of its genesis: Criollo-background cacao from the Paria Peninsula naturally hybridized with an earlier introduced Forastero cacao from the Lower Amazon (Ciferri 1949; Motamayor et al. 2003). It was demonstrated that this Forastero corresponds to the Amelonado genetic group, highly disseminated in the Amazon Basin around the same time Capuchin missionaries took cacao material to Trinidad (Bartley 2005; Motamayor et al. 2003).

The republican era.

After the colonial period, the now independent nations would experience different circumstances that had an impact on cacao cultivation. Here we focus on Venezuela, the country which suffered the most from the consequences of independence, and Ecuador and Brazil, the top producers of this era in South America.

Venezuela.

By the time Venezuela acquired independence from Spain in 1811, the national cacao production was surpassed by Ecuador and this never reverted. By 1825 cacao of the Criollo genetic group was the most frequent, if not the only, cultivated cacao in the country (Reyes and Capriles de Reyes 2000); then, cacao having the same genetic background was leaving the door open for another disease epidemic. This indeed occurred at the beginning of the 19th century; an unknown disease struck Criollo cacao in Tuy, spread throughout the Caracas province and virtually eliminated cacao from that area (Reyes and Capriles de Reyes 2000). As a consequence, between 1820 and 1830 Trinitario cacao, of lower quality than Criollo, was brought to the province of Caracas and was planted eastward in to the Paria Peninsula (Palma 1953). Unfortunately, these introductions did not improve the overall situation in the following decades, compounded by the aftermath of independence wars and the Federal War (1859 to 1863). Many cacao plantations were physically destroyed by combating troops and many others were either abandoned or replaced with the more-affordable-to-start coffee (Arroyo Abad 2013). Additionally, hacienda owners became broke after the abolition of slavery in 1854 (Arroyo Abad 2013). These circumstances made Ecuador the number one cacao world exporter between 1817 and 1842 (McCook 2002).

At the beginning of the 20th century, the profitable petroleum industry caused a massive migration from rural areas and thus a decline in not just cacao production but in the entire agricultural system (Malavé Mata 1974; Schiavoni and Camacaro 2009). By 1937, WBD had caused the demise of nearly all plantations in the Northeastern regions of the country, and by 1941 a second major disease, frosty pod rot (FPR), appeared in Zulia state, northwestern Venezuela, which worsened the national situation (Parra et al. 2009). Moreover, Ceratocystis wilt killed over half million of Criollo cacao trees in the state of Aragua during the first half of the 20th century (Parra et al. 2009; Reyes and Capriles de Reyes 2000). To mitigate these negative impacts, in 1956, the government created the FNCC (National Cacao and Coffee Fund), to promote both crops and to manage their commercialization (Díaz 2000). In 1975, FNCC split into two independent bodies: FONCACAO (National Cacao Fund) and FONCAFE (National Coffee Fund). FONCACAO was the only institution allowed to collect and buy cacao beans from producers and to manage their exportation, i.e., the cacao trade became monopolized (Díaz 2000). FONCACAO collapsed in the 1990s due to poor management, delayed payment to producers, and migration, among other factors (Díaz 2000). During the FONCACAO years, national cacao production and harvested areas experienced their lowest levels in their most current history (Fig. 6A). There were no resources to combat diseases; for example, in the region south to Maracaibo Lake, only 28% of producers took some management action against these diseases which directly affected their yields (Portillo et al. 1995). Overall, the disastrous consequences of cacao diseases in Venezuela in the 20th century resulted from the lack of knowledge about disease identification among farmers and extension agents and the generalized poor field data in the country (Parra et al. 2009).

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During the late 2000s, governmental measurements to favor cacao producers were initiated; this included promotion of microenterprise, low-interest credits, technical support, facilities, etc. (Schiavoni and Camacaro 2009), which translated in Venezuela to the highest national production by 2012 of the last 60 years. However, by that time there were some cacao areas, such as the Orinoco Delta and Sucre, suffering still from government indifference and high incidence of diseases (Lanz and Granado 2009; Rendiles et al. 2009). Today, cacao production in Venezuela is again in decline (Fig. 6A).

Ecuador.

Unlike in Venezuela, Ecuador’s independence in 1820 brought many economic benefits to the country. Guayaquil trading ships no longer had to transit through Lima or Spain so cacao commerce became unrestricted (Gondard 1986). Subsequently Ecuador was the top world producer of cacao until 1842, the year of the yellow fever epidemic, which reduced the Guayaquil population by half (Supplementary Table S1).

The second cacao boom in Ecuador took place between 1880 and 1910. Many factors contributed to the country’s economic resurgence. During the 1840s, chocolate candy was invented and released to the European market, and suddenly the global demand for cacao dramatically increased (Dand 1997). In the 1850s, African slavery and the “Indian tribute” imposed in the first republican years were abolished, and for the first time in Ecuador’s history, labor people were well paid (Chiriboga 2013; McCook 2002). Enthusiasm among Ecuador’s cacao hacienda owners increased so they started to make decisions designed to maximize income. They acquired more land to expand cultivation and in 1880 introduced the promising Trinitario varieties from Trinidad and Venezuela (Erneholm 1948; McCook 2002). The Trinitario material had high yields but did not have the high quality beans of the Nacional (Erneholm 1948). Hacienda owners then decided to sacrifice quality for quantity by disseminating Trinitario cacao cultivation, which allowed them to accumulate large fortunes (Chiriboga 2013; McCook 2002). The crisis in Venezuela also helped Ecuador to become the largest world supplier of cacao in the 19th century and exports increased by 340% from the 1870s to 1914 (Clarence-Smith 2000). Unfortunately, soon Ecuador’s export incomes relied on the world cacao market, which put Ecuador into a vulnerable position (Pineo 1988). As cultivated area expanded the number of workers remained the same (McCook 2002). This compromised adequate phytosanitary practices (e.g., farmers in Guayas “rarely took care of trees”) which would lead to disastrous consequences in the following years (Pineo 1988).

Ecuador led the world cacao production until 1905 to 1912, when it was surpassed by São Tomé and Príncipe, Ghana, and Brazil (Clarence-Smith 2000). Ecuador’s production started to fall when FPR disease was first reported in Guayas province in 1895 and became an epidemic in 1917−18 in Los Ríos and Guayas provinces (Phillips-Mora 2003). The causal agent of FPR, M. roreri, has two genetic diversity hotspots, cacao-producing regions of Colombia and Ecuador (Díaz-Valderrama et al., unpublished data), which fits into the historical origins of this disease. FPR was first seen in Norte de Santander, Colombia for the first time in 1817, under the name of “la mancha” (“the spot” in Spanish), and several times throughout cacao-producing regions of Colombia causing for example the disappearance of plantations in Cúcuta by 1850 (Phillips-Mora 2003). However, FPR impact in Colombia in the 19th century cannot be compared with the impact in Ecuador in the 20th century (Phillips-Mora 2003). In 1918, WBD was discovered in Ecuador in the Guayas Basin (Pound 1938) and together with FPR caused the biggest decline of Ecuador’s cacao production, a 60% reduction from 1916 to 1931 (McCook 2002). This created an unexpected national economic crisis and subsequently social upheavals such as the one in Guayaquil in 1922, among the worst in Ecuador’s history (Pineo 1988). During these years, the cacao cultivation system was greatly diminished, driving growers to switch to other crops (McCook 2002). The monetary incentives from the government to find solutions against cacao diseases led to the collection and identification of cacao germplasm from the coast of Ecuador with some levels of resistance to WBD; this germplasm is known as Refractario (Pound 1938). Researchers noticed that this Refractario material did not belong to the Nacional genetic group but to the Trinitario, which was introduced to the country since 1880 (Erneholm 1948). Additionally, Pound (1938) found that highly resistant Refractario cacao was very similar to material he found throughout the region of the Napo River, in the Ecuadorian Amazon. He then proposed an earlier introduction of Amazonian cacao to the coast of Ecuador (Pound 1938). More recently, it has been shown that Nacional is one of the parental groups of Refractario cacao (Zhang et al. 2008).

Cacao collections along the Ecuadorian territory continued during the 1930s and 1940s and have been maintained in the two largest germplasm banks of the country, the “Estación Experimental Tropical Pichilingue” in Quevedo and “Centro de Cacao Aroma Tenguel” (Loor et al. 2009). Moreover, the work of the breeder Homero Castro Zurita would have a significant impact on cacao production in Ecuador in the next decades. During the 1950s Castro Zurita performed expeditions to the Canelos valley in the Ecuadorian Amazon and incorporated cacao material into his private collection in Naranjal, known as the “Colección Castro Naranjal” or CCN (Crespo del Campo and Crespo Andía 1997); this collection was also composed of the widespread ICS (Trinitario) and IMC (Iquitos) germplasm (Boza et al. 2014). During the 1960s, one of his crosses (ICS-95 × IMC-67) × ‘Oriente 1’ (from Canelos valley) resulted in the generation of the clone CCN-51 (Boza et al. 2014); although the pedigree information of ‘Oriente 1’ was lost, the genetic composition of CCN-51 corroborates Castro Zurita’s crosses: 45.5% Iquitos, 22.2% Criollo, 21.5% Amelonada, 1.1% Nacional and the rest a mix of other Forastero genotypes (Boza et al. 2014). The beans from CCN-51 were of lower quality than the Nacional’s but had many agronomic advantages including early maturation, high productivity and high levels of disease tolerance (Crespo del Campo and Crespo Andía 1997). Subsequently, CCN-51 gradually gained farmers’ preference, even though it was considered “bulk cacao” and Nacional is highly appreciated in the fine aroma international market and pays a premium price (Flores González 2007). Extensive cultivation of CCN-51 started to appear since 1985 (Crespo del Campo and Crespo Andía 1997). CCN-51 cacao exports have sharply increased from 5.8% of total national exports in 2005 (Flores González 2007) to 30% in 2015 (Moncayo 2016). This planting of CCN-51 has brought many inherent issues: from the conservation perspective, the unavoidable natural hybridization of Nacional and CCN-51 genotypes (and also Trinitario germplasm introduced since 1880) has put at risk the Nacional genetic integrity (Loor Solorzano et al. 2012); from the food industry perspective, adulterations of Nacional cacao bean cargos with CCN-51 beans are frequently reported which has generated the development of molecular and computational imaging methods to detect them (Herrmann et al. 2014; Jimenez et al. 2018); and from the biodiversity perspective, CCN-51 is mainly cultivated as a monocrop requiring major agronomic inputs while Nacional is produced under agroforestry systems (Bentley et al. 2004). Additionally, most of the fine aroma cultivated cacaos are actually hybrids between Nacional and Trinitario that maintain fine aroma characteristics and only 1% is pure Nacional (Bentley et al. 2004). Nowadays, the national priority is to protect the Nacional germplasm (Flores González 2007; Melo and Hollander 2013) as it represents 66% of world fine aroma cacao (Fountain and Huetz-Adams 2018). Moreover, CCN-51 reached other important fine aroma cacao producing countries such as Peru. By 2011, there were 45,445 ha (53.6% of national total) under cultivation of exclusively CCN-51 cacao in this country (García Carrión 2010).

Brazil.

During the first decades of the republican period the Lower Amazon (Maranhão and Pará) was still the main cacao-producing region in Brazil. By 1880, Amazonian exports doubled those from Bahia: 3,121 versus 1,668 tons. However, this situation was reversed by 1900, when exports from Bahia reached 13,131 tons and Amazon exports were 3,085 tons (Walker 2007). Unlike in the Amazon, the main labor force in Bahia were African slaves until abolition in 1888 (Walker 2007). Cacao then represented the door to economic independence for the now ex-slaves in Brazil; many would move to Bahia and encounter large uncultivated areas ideal for the cultivation of the highly demanded cacao (Mahony 2008). Additionally, since 1888 smallholder farmers developed into large haciendas because of the abundance of indigent workers (Erneholm 1948; Walker 2007). Therefore, the cacao production in Bahia rapidly expanded: from 1895 to 1941 to 1945 total production went from about 6,000 to 125,000 tons, i.e., a 1900% increase in 50 years (Erneholm 1948)! Brazil’s highest ever production peak occurred in 1986 with 459,477 tons (Fig. 6B). The only cacao genotype widely cultivated in Brazil has been Amelonado, introduced since 1746 to Bahia (See Colonial Era). There were some attempts to introduce and disseminate Criollo cacao (high quality) in Bahia in the 1920s but they were never successful (Erneholm 1948).

The cacao crisis due to FPR and WBD in Ecuador fomented the production growth in West African countries, where Amelonado-background cacao was the most disseminated (Ploetz 2006). Then, Brazil actively competed with São Tome and Principe and Ghana in the first half, and Côte d’Ivoire in the second half of the 20th century, major producers of the century (Dand 1997). The rest of the Americas was severely affected by WBD, endemic to the Amazon. Bahia was still free of WBD and it was seemingly protected by an approximately 2,000-km-long geographical barrier that separated Amazonian cacao plantations from those on the coast (Rocha 1983). However, concerns of a potential WBD introduction were raised in the early 1980s because of the expansion of cultivation in the Amazon and frequent communications back and forth with Bahia (Rocha 1983). Quarantine controls were established but the imminent spread finally occurred in 1989 (Pereira et al. 1990). It is possible that this introduction of WBD to Bahia was an agro-terrorism attack against the politically influential cacao hacienda owners (Caldas and Perz 2013). WBD introduction in Bahia was immediately followed by a tremendous decline in cacao production from which the state has still not recovered (Fig. 6B). The low genetic background of the Amelonado cacao cultivated in Bahia greatly favored the rapid dissemination of WBD (Santos et al. 2015). This situation has placed West African countries, especially Côte d’Ivoire, in the top of cacao producers (Table 2).

TABLE 2 World cacao bean production and the main cacao genetic background or cultivar associated with each country or region

Country/Region	Tonnesa	%	Genetic background/cultivarb
Côte d’Ivoire	7,427,949	37.0	Amelonado, Trinitario
Rest of Africa	6,648,020	33.2	Amelonado, Trinitario
Asia	2,614,575	13.0	Criollo, Trinitario, Amelonado
Brazil	967,366	4.8	Amelonado
Ecuador	798,880	4.0	Nacional, CCN-51, Trinitario, Refractario
Rest of South America	799,259	4.0	CCN-51, Trinitario, Nacional, Criollo, Iquitos
Mexico, Central America, and the Caribbean	586,888	2.9	Criollo, Trinitario
Oceania	208,844	1.0	Criollo
Total	20,051,781	100.0

^a Data contains 2015 to 2018 official, semiofficial, and estimated values from FAOSTAT (http://faostat.fao.org/).

^b Cacao genotypes make up most of the genetic diversity of current cultivated cultivars in each region or country. The genetic backgrounds associated with Africa, Asia, and Oceania was not discussed in this manuscript, but are referred to in Bartley (2005).

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The Caribbean and other countries.

Most of the Caribbean countries remained European colonies during the 19th and the first half of the 20th century. However, some important events regarding cacao production that occurred in this region would influence the rest of the countries. In 1895, WBD was first observed in Suriname (Supplementary Table S1) rapidly spreading to the Caribbean, where it was especially destructive in Trinidad since 1928 (Laker et al. 1988). Because of the latter invasion, the major expeditions into the Upper Amazon to search for disease resistant cacao germplasm took place, led by Frederick J. Pound from the then Imperial College Station (ICS). This resulted in the creation of the International Cocoa Genebank, Trinidad (ICG,T). Additionally, other collecting expeditions were performed throughout the entire Amazonian region (Zhang and Motilal 2016). WBD persists in the country and it was a direct responsible to the sharp decline of Trinidad cacao production, which went from 34,800 tons in 1921 to 5,900 in 1980 (Laker et al. 1988).

Conversely, a different disease, FPR, was responsible for the collapse of cacao production in Central America. This disease progressively took over plantations beginning with Panama in 1956 (Phillips-Mora 2003). Currently, the disease can be found in all countries of Central America and in Jamaica, the only country in the Caribbean reported to have FPR (Johnson et al. 2017). Among the countries more affected by FPR has been Costa Rica, once the top producer of Central America at the beginning of the 20th century (Clarence-Smith 2000). The first exports from Costa Rica in the Republican era started in 1884 with the very modest amount of four tons (Clarence-Smith 2000). However, by 1977 its exports increased to 5,719 tons (Enríquez and Suárez 1978). Unfortunately, FPR arrived in Costa Rica in 1978, observed for the first time in the Limón province (Enríquez and Suárez 1978), and caused a devastating decline in cacao production in the following years (Fig. 6C). Even more, FPR spread southwards to Peru, reaching Utcubamba in 1988, and to Bolivia, reaching Alto Beni in 2012 (Phillips-Mora 2003; Phillips-Mora et al. 2015). Major breeding efforts in Latin America rely greatly on the germplasm collected during the expeditions of the 20th century. Unfortunately, resistant cacao cultivars to the major diseases, WBD and FPR, have not yet been developed (Marelli et al. 2019).

CURRENT SITUATION OF CACAO CULTIVATION

The appearance of disease epidemics has shaped the modern history of cacao production. The majority of cacao is now produced far from its center of origin (Table 2). African and Asian countries produce approximately 70.2 and 13%, while countries in the Americas produce 15.7% of world cacao (Table 2). Additionally, in the middle of the 19th century, around 95% of cacao produced in the world was of fine quality (Erneholm 1948); nowadays it is exactly the opposite, 95% of world cacao is of low quality and a scarce 5% is fine cacao (Melo and Hollander 2013). Based on the historical movements of germplasm, in the largest producing countries the genetic background to resist disease is very low, even the ones located in or near its center of origin. This means that cacao diseases will continue to diminish cacao yields at least for the near future. Currently, more than 90% of world cacao is produced by about 6 million small-holder farmers in plantations averaging 2 to 4 ha each (Wickramasuriya and Dunwell 2018). Moreover, major producing regions are still free of FPR and WBD, but their introduction into Africa and Asia could have a serious deleterious effect on their economies as they are still considered to be in their invasive stages. Therefore, the goal is to find long-lasting solutions for cacao diseases—through breeding, quarantine, and better management regimes–and in this way avoid a global crisis, as we have seen at least once per century, since colonial times.

ACKNOWLEDGMENTS

We thank Charles Woloshuk, Stephen Goodwin, Rachel Koch, Jumbam Blaise, and Teeratas Kijpornyongpan for helpful comments on earlier versions of this manuscript.