Coffee Fruit Rot: The Previously Unrecognized Role of Fusarium and Its Interactions with the Coffee Berry Borer (Hypothenemus hampei).

Coffee fruit rot (CFR) is a well-known disease worldwide, mainly caused by Colletotrichum spp., the most important species being C. kahawae subsp. kahawae. In Puerto Rico, Colletotrichum spp. were identified as pathogens of coffee fruits. The coffee berry borer (CBB) was shown to be a dispersal agent of these fungi, and interaction of Fusarium with Colletotrichum affecting coffee fruits was suggested. In this study, we demonstrated that Fusarium spp. also cause CFR in Puerto Rico. Fusarium spp. are part of the CBB mycobiota, and this insect is responsible for spreading the pathogens in coffee fields. We identified nine Fusarium spp. (F. nirenbergiae, F. bostrycoides, F. crassum, F. hengyangense, F. solani-melongenae, F. pseudocircinatum, F. meridionale, F. concolor, and F. lateritium) belonging to six Fusarium species complexes isolated from CBBs and from rotten coffee fruits. Pathogenicity tests showed that F. bostrycoides, F. lateritium, F. nirenbergiae, F. solani-melongenae, and F. pseudocircinatum were pathogens causing CFR on green coffee fruits. F. bostrycoides was the predominant species isolated from the CBB mycobiota and coffee fruits with symptoms of CFR, suggesting a close relationship between F. bostrycoides and the CBB. To our knowledge, this is the first report of F. bostrycoides, F. solani-melongenae, F. pseudocircinatum, and F. nirenbergiae causing CFR worldwide and the first report of F. lateritium causing CFR in Puerto Rico. Understanding the CFR disease complex and how the CBB contributes to dispersing different Fusarium spp. on coffee farms is important to implement disease management practices in Puerto Rico and in other coffee-producing countries.

Establishing an Integrated Pest Management Program for Coffee Berry Borer (Hypothenemus hampei) in Hawaii and Puerto Rico Coffee Agroecosystems: Achievements and Challenges.

Coffee berry borer (CBB) is the most serious insect pest of coffee worldwide, causing significant reductions in yield and quality. Following the introduction of CBB to Puerto Rico (2007) and Hawaii (2010), researchers, extension agents, industry representatives, and coffee growers have worked together to develop an integrated pest management (IPM) program that is both effective and economically feasible for each island. Since the introduction of the IPM program in Hawaii, research efforts have led to a better understanding of CBB population dynamics, as well as optimized monitoring, cultural practices, and commercial Beauveria bassiana applications. As a result of these efforts, a substantial reduction in average CBB infestation and an increase in coffee yields and quality have been documented in Hawaii over the last decade. However, significant challenges remain in addressing high production and labor costs, limited availability of labor, and a lack of training for field workers in both regions. Although considerable effort has gone into research to support CBB IPM in Hawaii and Puerto Rico, the adoption of these strategies by coffee farmers needs to be increased. More diversified methods of outreach and education are needed to reach growers in rural, isolated areas. Significant gaps exist in the ability and willingness of growers and workers to access and digest information online, emphasizing the importance of on-farm workshops and farmer-to-farmer teaching. Additional methods of training are needed to help coffee farmers and field workers learn how to properly conduct cultural controls and optimize the use of biological control agents such as B. bassiana.

Demography and perturbation analyses of the coffee berry borer Hypothenemus hampei (Coleoptera: Curculionidae): Implications for management.

The coffee berry borer (CBB) Hypothenemus hampei Ferrari is the most serious pest of coffee worldwide. Management of the CBB is extremely difficult because its entire life cycle occurs inside the fruit, where it is well protected. Knowing which life stages contribute most to population growth, would shed light on the population dynamics of this pest and help to improve CBB management programs. Two staged-classified matrices were constructed for CBB populations reared in the lab on artificial diets and CBB populations from artificial infestations in the field. Matrices were used to determine demographic parameters, to conduct elasticity analyses, and to perform prospective perturbation analysis. Higher values of the intrinsic rate of natural increase (rm) and population growth rate (λ): were observed for CBB populations growing in the lab than in the field (rm: 0.058, λ: 1.74 lab; rm: 0.053, λ: 1.32 field). Sensitivity values for both CBB populations were highest for the transitions from larva to pupa (G2: 0.316 lab, 0.352 field), transition from pupa to juvenile (G3: 0.345 lab, 0.515 field) and survival of adult females (P5: 0.324 lab, 0.389 field); these three vital rates can be important targets for CBB management. Prospective perturbation analyses indicated that an effective management for the CBB should consider multiple developmental stages; perturbations of >90% for each transition are necessary to reduce λ to <1. However, when the three vital rates with highest sensitivity are impacted at the same time, the percentage of perturbation is reduced to 25% for each transition; with these reductions in survival of larvae, pupae and adult females the value of λ was reduced from 1.32 to 0.96. Management programs for CBB should be focused on the use of biological and cultural measures that are known to affect these three important targets.

Pathogens Causing Anthracnose and Fruit Rots of Coffee Associated with the Coffee Berry Borer and the Entomopathogenic Fungus Beauveria bassiana in Puerto Rico.

Fruit rots reduce coffee production worldwide. Eight Colletotrichum species have been reported to cause coffee fruit rots; the most important is C. kahawae, the cause of coffee berry disease (CBD) in Africa. It is unknown whether these fruit rot pathogens can be dispersed by the coffee berry borer (CBB, Hypothenemus hampei) or whether Beauveria bassiana (a natural enemy of CBB) might reduce coffee fruit rots. We identified pathogens causing coffee fruits rots in Puerto Rico and evaluated whether B. bassiana reduced fruit rot and whether CBB could disperse pathogens. A total of 2,333 coffee fruit with CBB damage were collected; of these, 1,197 had visible growth of B. bassiana. C. fructicola, C. siamense, C. theobromicola, and C. tropicale were isolated and identified from the fruit using morphological traits and phylogeny of three nuclear genes. All four species caused internal and external rot after inoculation of healthy green coffee fruit. Coffee fruit treated with B. bassiana had significantly less fruit rot than untreated fruit, suggesting B. bassiana can protect against fruit rot. To test whether B. bassiana had a protective effect, B. bassiana and Colletotrichum were coinoculated on coffee fruit. Fruit inoculated with both B. bassiana and Colletotrichum had significantly less rot than fruit inoculated with Colletotrichum alone. To test if CBBs dispersed the pathogens, CBBs were exposed to Colletotrichum conidia and placed on green fruit, which resulted in fruit rot. This study identifies new pathogens causing coffee fruit rot, shows that C. kahawae is not the only Colletotrichum that attacks green fruits, suggests a role for B. bassiana in disease management and demonstrates CBB can disperse the pathogens.

The Coffee Berry Borer (Coleoptera: Curculionidae) in Puerto Rico: Distribution, Infestation, and Population per Fruit.

The coffee berry borer (CBB) (Hypothenemus hampei: Ferrar) was first detected in Puerto Rico in 2007. Its distribution since then has been extensive, but not extensively documented. An island-wide survey was carried out from August to November 2014 (the coffee production season) to assess CBB distribution, infestation, and population per fruit. The CBB was well-established throughout the coffee-growing area of Puerto Rico, but was not evenly distributed. Infestation (or percentages of fruits perforated) in sites sampled ranged from 0 to 95%, and CBB number per infested fruit varied from 1 to 34 individuals. CBB infestation and total population per fruit were positively correlated with altitude. Highest infestation and total population were observed in sites located >400 masl; most of the coffee-producing area in Puerto Rico is above this altitude. Coffea arabica (L.) had higher CBB infestation and population per fruit than Coffea canephora (Pierre ex A. Froehner) (robusta coffee). Based on these results, management tools should be implemented to mitigate the severe damage that CBB is causing in Puerto Rico. These management tools should include the removal of all fruits that remain on the plants after harvest and the use of the entomopathogenic fungus Beauveria bassiana (Balls.) Vuill. for biocontrol, especially on coffee farms at higher elevations.

Wolbachia Affects Reproduction and Population Dynamics of the Coffee Berry Borer (Hypothenemus hampei): Implications for Biological Control.

Wolbachia are widely distributed endosymbiotic bacteria that influence the reproduction and fitness of their hosts. In recent years the manipulation of Wolbachia infection has been considered as a potential tool for biological control. The coffee berry borer (CBB), Hypothenemus hampei, is the most devastating coffee pest worldwide. Wolbachia infection in the CBB has been reported, but until now the role of Wolbachia in CBB reproduction and fitness has not been tested. To address this issue we reared the CBB in artificial diets with and without tetracycline (0.1% w/v) for ten generations. Tetracycline reduced significantly the relative proportion of Wolbachia in the CBB microbiota from 0.49% to 0.04%. This reduction affected CBB reproduction: females fed with tetracycline had significantly fewer progeny, lower fecundity, and fewer eggs per female. Tetracycline also reduced the population growth rate (λ), net reproductive rate (R0), and mean generation time (T) in CBB; the reduction in population growth was mostly due to variation in fertility, according to life time response experiments (LTREs) analysis. Our results suggest that Wolbachia contribute to the reproductive success of the CBB and their manipulation represents a possible approach to CBB biocontrol mediated by microbiome management.