Theobroma cacao L. is a tree native to the Upper Amazon basin that includes territories in Brazil, Ecuador, Peru, and Colombia. T. cacao (cocoa) was first cultivated in Mesoamerica by the Olmec and Maya civilizations and later by the Aztecs. Thanks to the pre-Colombian cultures, it spread throughout the world. The seeds of this fruit (cocoa beans) are used to make chocolate.

Cocoa cultivation depends on the farming method adopted. In general, seeds are planted in a seedbed and transferred to the ground. Although it is not very common, cocoa seeds are sown directly in the soil in some countries. Planting often occurs at the beginning of the rainy season so that the soil remains moist while the roots become firmly established. The cocoa tree needs shade for its protection, and normal development is favoured by high and constant relative humidity. To this purpose, sometimes banana plants, coconut trees, or other species are planted along with the cocoa. Depending on the variety, it will take three or four years until the cocoa tree produces its first fruits, and the maximum harvest is reached after six or seven years. Although the fruits mature throughout the year, in general, there are four harvests each year: a small harvest at the beginning and a large one at the end of each of the two rainy seasons. The cocoa tree produces fruits called pods containing pulp and raw beans, and each pod generally contains from 25 to 40 seeds or cocoa beans [1]. When harvested, the outer pod is removed from the tree to extract the beans. After removing the pod, the beans are subjected to a fermentation stage (an essential step in which mucilaginous pulp surrounding the seed is removed) and a drying stage before being sent for further processing. These are the most crucial production stages, where important cocoa changes occur, ensuring that cocoa gets its characteristic flavours and aroma [2,3].

Cocoa is cultivated in several tropical and subtropical zones around the world. The temperature ranges from 15 to 32 °C, usually at an altitude below 300 m.a.s.l., although in some ecosystems, it can reach 1100 m.a.s.l. For proper growth, the crop requires uniformly distributed rain throughout the year, ranging between 1500 and 3000 mm. The largest producers are the Ivory Coast, Ghana, Indonesia, Ecuador, Nigeria, Cameroon, and Brazil [4]. The International Cocoa Organization reported world productions of 4697 thousand tons during 2019/2020 and estimates that its production tends to increase [4]. It is a market that in 2019 moved more than 50,300 million dollars in raw cocoa and cocoa products [5].

Similar to other crops, cocoa plants and beans are exposed to contamination and colonization by different microorganisms during the sequential production steps (crop, harvest, fermentation, drying, and storage). Indeed, in all countries where cocoa is produced, weather and crop practices support fungal growth and, consequently, product quality deterioration. In general, cocoa production quality depends on the genetic type, natural conditions in the site where plantations and management are located, and the postharvest activities, including fermentation, drying, and storage. In particular, filamentous fungi may infect several stages in cocoa processing, and poor agricultural practice may have a marked influence on the quality attributes of cocoa [6].

2. What about Climate Change?

It is generally known that the effects of climate change (CC) on agriculture include changes in levels of CO₂, ozone, and UV-B that can modify plant diseases by changing host physiology and resistance [142]. In particular, CC includes changes in rainfall patterns, drought, flooding, and temperature that may influence disease epidemiology and/or modify the present land use for food crops, resulting in new pathogen disease complexes [143]. According to the Intergovernmental Panel on Climate Change (IPCC), in the coming years, CC will affect especially the tropics and subtropics, where precipitation will decrease at low altitudes and increase at higher altitudes [144]. Although CC’s impact will vary from region to region, according to the scenarios predicted for the regions where cocoa is produced, higher temperatures, more prolonged droughts, and increasingly frequent and strong storms are predicted to aggravate the current challenges faced by the agricultural production systems [144]. The extreme changes might shape crops and ultimately the yield of cocoa. In a very interesting review, Lahive et al. [145] considered the current research on cocoa’s physiological responses to CC. In the present paper, we consider the influence of CC on cocoa mycobiota during the different production steps because it is possible that new interactions of the fungi may affect the cocoa production chain and the final product’s quality (Figure 3).

Figure 3. Main fungi interaction throughout the cocoa production chain.

Variation in temperature or altered precipitation may result in changes in cocoa pathogens that alter disease incidence and severity. Velásquez et al., [146] suggested that CC may (i) alter the stages and rates of development of pathogens and pests; (ii) accelerate the evolution of pathogens; (iii) reduce incubation periods; (iv) facilitate the introduction of invasive alien species, their establishment and diffusion; (v) change the physiology of the host–pathogen/pest interaction; (vi) produce changes in the geographical distribution of pathogens and pests; and (vii) affect production and consequently the socioeconomic variables. In this context, Bucker Moraes et al. [33] underlined that CC could induce significant risk on increases in moniliasis (produced by M. roreri), as literature shows the correlation between the germination of the disease’s fungal spores and precipitation, which is the only method for infecting other trees. In addition, the highly productive cocoa regions are profoundly affected by shifts in climatic regimes during the El Niño (ENSO)–La Niña (LN) cycle, which can favour fungal pathogenic infection in the productive and vegetative cycles of the cocoa trees [147]. Indeed, ENSO was responsible for the pod losses due to the increase of witches’ broom severity caused by M. perniciosa in the last five years. In this context, Gateau-Rey et al. [148] reported an increase in the pod losses from 2015 (15%) to 2017 (35%) during the drought.

CC has the potential to increase the incidence of pests and diseases, and introduce new types that find a favourable environment in the cocoa farm [149]. Researchers have considered that drought stress is beneficial to opportunistic fungal pathogens that may not otherwise impact crop hosts [150]. According to Kubiak et al. [151], climate change and global warming are not the only factors predisposing the roots of weakened trees to Armillaria infections, but also bacteria and fungi, as well as macro, meso, and micro-organisms growing in the soil around root systems, could enhance the proliferation of the pathogen and decrease the immune barriers in roots.

Although it is already accepted that CC modifies the distribution of phytopathogenic moulds, it is difficult to calculate all the effects also because there is a complete lack of information on host and pathogen adaptation to CC and accurate predictive models still do not exist for many diseases. As a result, evaluating of the possible impact of CC on the cocoa production chain should be treated with attention [142]. In particular, there are limited reports on the CC effects on cocoa fungal pathologies, although modelling studies have provided realistic scenarios on some plant diseases. For example, Ortega Andrade et al. [152], by using species distribution models (SDM) with nineteen climatic variables for the present and the future (5, 35, and 65 years), analysed the impact of CC on the potential distribution of M. roreri and T. cacao in South America. Their results suggested that the precipitation during the wettest month is the most influential variable for the presence and proliferation of M. roreri, and they estimated that this phytopathogenic fungus could extend from southern Ecuador to regions interconnected by cocoa crops in South America (Colombia, Venezuela, Peru, Bolivia, and Western Brazil). On the other hand, de Oliveira et al. [153] suggested that fungal communities in tropical grassland soils have greater sensitivity to drought than to temperature, which might increase the incidence of certain soilborne diseases.

The ability of fungal endophytes to confer stress tolerance to plants may provide a novel strategy for mitigating the impacts of global climate change on agricultural plant communities [154].

There are no studies on the impact that CC could have on cocoa mycorrhizal fungi. However, Bae et al. [155] showed that T. hamatum improved the tolerance to water scarcity of the cocoa seedlings colonized by this endophytic fungus. Recently, Bennett and Classen [156], examining the response of both mycorrhizal fungi and the associated plants, found that mycorrhizal fungi’ promotion of stress tolerance should allow temporal space for plant adaptation to CC. On the other hand, Kivlin et al. [157] suggested that leaf endophytes also respond to global change and improve the effects of drought in their host plants.

Although there is no information available on CC impact on cocoa fermentation, it is important to highlight that changes in temperature influence all the microbiota associated with fermentation (yeasts, bacteria, and filamentous fungi), which dominate in the cocoa seeds as they undergo continuous physical and chemical changes. Speaking about filamentous fungi, they are usually in low counts during fermentation due to the restricted conditions such as the ethanol and organic acid production and high temperatures that can rise above 45 °C after 48 h. As above mentioned, two scenarios could be present in the future: (I) increase of mean and maximum temperatures and drought, (II) periods of intense rainfall. Assuming scenario I, the fungi diversity could be decreased, with a selection of particular strains with particular technological properties that may not necessarily confer valuable cocoa characteristics. Paterson and Lima [150] proposed that existing thermotolerant and thermophilic fungal species will dominate and produce a variety of secondary metabolites and also mycotoxins. With scenario II, the fermentation might be extended, leading to a rise in bacteria of the genus Bacillus and in filamentous fungi that could cause off-flavours and the formation of mycotoxins, including the ochratoxigenic species A. carbonarius and A. niger.

Although some authors suggested that hot countries may produce safer food under CC because mycotoxigenic fungi will be inhibited [158], experimental data showed that the drying period is critical to avoid the formation of mycotoxins in the cocoa beans [131]. Indeed, some strains of A. niger can grow at 41 °C, showing a higher xerophilic ability compared to A. carbonarius and A. ochraceus [159]. Moreover, Moretti and Logrieco [160] suggested that CC may induce the presence of new fungal genotypes with high aggressiveness, increasing the concern of mycotoxin production.