Can Coffee Chemical Compounds and Insecticidal Plants Be

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Can coffee chemical compounds and insecticidal plants be harnessed for control of major coffee pests? Paul Walter Charles Green, Aaron P. Davis, Allard A. Cossé, and Fernando E. Vega J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.5b03914 • Publication Date (Web): 12 Oct 2015 Downloaded from http://pubs.acs.org on October 19, 2015

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Journal of Agricultural and Food Chemistry

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Can coffee chemical compounds and insecticidal plants be harnessed

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for control of major coffee pests?

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PAUL W. C. GREEN *,†, A. P. DAVIS †, ALLARD A. COSSÉ ‡ AND FERNANDO E. VEGA §

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†

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Center for Agricultural Utilization Research, 1815 N. University St., Peoria, IL 61604, U.S.A., §Sustainable Perennial Crops

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Laboratory, USDA, ARS, Beltsville, MD 20705, U.S.A.

Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AB, U.K., ‡Crop Bioprotection Research Unit, USDA, ARS, National

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* Author to whom correspondence should be addressed (telephone +44 20 8332 5375; fax +44 20 8332 5310; e-mail

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[email protected]).

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___________________________________________________________________

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Pests and pathogens threaten coffee production worldwide and are difficult to control using conventional methods, such as insecticides. We review the literature on the chemistry of coffee, concentrating on compounds most commonly reported from Coffea arabica and C. canephora. Differences in chemistry can distinguish coffee species and varieties and plants grown under different biogeographic conditions exhibit different chemotypes. A number of chemical groups, such as alkaloids and caffeoyl quinic acids are known to be insecticidal, but most studies have investigated their effects on coffee quality and flavour. More research is required to bridge this gap in knowledge, so that coffee can be bred to be more resistant to pests. Furthermore, we report on some pesticidal plants that have been used for control of coffee pests. Locally sourced pesticidal plants have been under-utilized and offer a sustainable alternative to conventional insecticides and could be used to augment breeding for resilience of coffee plants.

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___________________________________________________________________

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KEYWORDS: Hypothenemus hampei; Coffea arabica; Coffea canephora; coffee chemistry;

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coffee pests; pest control; pesticidal plants.

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INTRODUCTION

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Of the 124 coffee (Coffea L.) species1 only two are used for commercial

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production of the beverage coffee: Arabica (Coffea arabica L.) and robusta coffee (C.

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canephora Pierre ex. A. Froehner). Production of both species worldwide is

1 ACS Paragon Plus Environment


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negatively impacted by a number of factors, including unfavourable market forces,2

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climate change3-5 and a wide range of pests and diseases, such as bacteria,6 fungi,7

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mites,8,9 insects10,11 and nematodes.12,13 Among the insects, Hypothenemus hampei

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(Ferrari) (Coleoptera: Curculionidae: Scolytinae), a bark beetle commonly known as

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the coffee berry borer (CBB), is the most important global threat to coffee

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production,14-16 although there are more localised pests, such as Antestiopsis Leston

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(Hemiptera: Pentatomidae), which both damages the plants and contaminates the

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beans with a fungus that makes the finished beverage unpalatable.17-19

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The CBB (Figure 1) spends its life cycle protected in the developing coffee

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berry and is therefore difficult to control using insecticides.16

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management strategies include natural enemies - in particular parasitoid wasps20-22 -

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or entomopathogenic fungi,23-25 which provide some degree of protection, although

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their establishment in the field is difficult.16 Trapping of insects has been attempted,

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based upon an alcohol mixture and is useful for monitoring insect numbers26

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although the numbers caught barely impact upon the populations of CBB16,27 when

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heavy infestations are estimated at millions of CBBs per hectare.16,28 No single

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method is effective on its own, so an integrated approach is required, together with a

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better understanding of coffee chemistry and the biology of CBB.16 Climate change is

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likely to alter the population dynamics of pest insects, such as CBB, increasing their

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rate of reproduction,29-31 while widening their geographic range.32,33

Alternative pest

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The study of chemicals in coffee (e.g., alkaloids, caffeoyl quinic acids, fatty

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acids, sterols and sugars) has been focussed on their utility for distinguishing groups

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within the genus Coffea,34-36 varieties and cultivars37,38 or to pinpoint the geographic

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origins of particular plants.39 Ample research has also been dedicated to assessing

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the chemical composition of green coffee,40 roasted and ground coffee,41-44 and to


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relate this to the quality of the finished beverage.45,46 Aside from some of the work

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on volatile attractants for H. hampei16 there have been few studies of the chemical

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resistance of C. arabica to this insect.

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This review will concentrate on the potential use of commonly reported

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compounds for protecting coffee (C. arabica and C. robusta) against pests and

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pathogens.

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developing resistant varieties of Coffea and prior and future use of other species of

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plant as so-called “pesticidal plants” will also be discussed.

The possibilities for investigating other classes of chemicals in

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1. Chemical compounds of coffee

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(i)

Caffeine and trigonelline

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Caffeine (1, 3, 7-trimethylxanthine) is present in the flowers,47 leaves,48 seeds,49

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and in green-34 and roasted coffee.42 The proportion of caffeine in the green beans of

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C. canephora (1.5 to 4%) is greater than in C. arabica (0.7 to 1.6%).50 Caffeine is

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responsible for the stimulatory effect of coffee in mammals51 and together with

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another alkaloid, trigonelline as well as other compounds (see below) contributes to

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the antioxidant and antimicrobial properties.52-55 In a broader context, insects that

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would not normally encounter caffeine in their host plants can be repelled when it is

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introduced into a plant.56

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improves their memory of good sources of nectar.57 Caffeine is produced in

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response to coffee berry disease (Colletotrichum kahawae Waller & Bridge;

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Ascomycota: Sordariomycetes) and this up-regulation can be a marker for

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resistance.58 The CBB is adapted to tolerate caffeine in the seeds59,60 even though

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direct application of caffeine oleate formulations is toxic.61 Caffeine is not toxic to

Some pollinators are also affected by caffeine as it



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leafcutter ants [Atta sexdens rubropilosa Forel (Hymenoptera: Formicidae)], but does

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inhibit the growth of the mutualistic fungi on which the ants feed, leading to the

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possibility that these pests of coffee may select low caffeine coffee varieties.62

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Application of caffeine to coffee leaves increases movement of the crawler stage of

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the soft scale Coccus viridis (Green) (Hemiptera: Coccidae) and therefore reduces

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feeding damage.63

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(ii)

Caffeoyl quinic acids (CQAs) and related compounds

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CQAs and other quinic acids are present in the leaves,64 seedlings,58 green-

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and roasted coffee42 and contribute to the antimicrobial and antioxidant properties of

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coffee.52,55,65,66 The concentrations of hydroxycinnamic acids and their esters, such

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as the mono- and di-caffeoylquinic acids can be used to differentiate between

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genotypes and plants from different locations.34,40,67-69 Conflicting studies using

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different cultivars have shown that CQAs are at their highest levels in shade for C.

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arabica L. cv. Catimor70 or at full sun for a dwarf variety C. arabica L. cv. Costa Rica

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95.71 As CBB population levels can increase when plants are shaded,16,72 it is not yet

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clear whether this is due to raised or lowered levels of CQAs or other biotic or abiotic

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constraints.

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varieties,45 while the prevalence of CBB decreases.72 As part of the response to

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pathogens the concentration of 3-caffeoylquinic acid (3-CQA) in leaves increases

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when plants are challenged with the rust Hemileia vastatrix Berk. & Broome (coffee

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leaf rust; Basidiomycota: Pucciniomycetes)64 and seedlings respond to C. kahawae

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by producing more 3-CQA in a mixture of structurally similar compounds.58 A side-

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effect of coffee leaf miner infestation [Leucoptera coffeella (Guérin-Méneville &

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Levels of CQAs also increase with altitude, especially in traditional


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Perrottet); Lepidoptera: Lyonetiidae], with 6-8 eggs per leaf, is that coffee leaves

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produce less chlorogenic acid and become more susceptible to C. viridis.73

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(iii)

Volatiles

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The volatile profile of coffee berries varies as the drupe ripens, and it has been

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suggested that these mixtures could be used as the basis for developing attractive or

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repellent blends for CBB.74,75 Ortiz et al.74 used dynamic headspace collection,

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coupled to a gas chromatography/mass spectrometry (GC-MS) system to analyse

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compounds from coffee berries and found 27, 34, 41, and 68 chemicals in green,

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half-ripe, ripe and over-ripe berries, respectively.

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different stages, although esters were prominent in over-ripe berries together with an

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overall paucity of monoterpenes.74 Using a different collection technique, Mathieu et

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al.76 analysed samples eluted from a Super Q absorbent using GC-MS and detected

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45 different compounds in volatiles from fresh coffee berries of C. arabica and C.

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canephora at different stages of ripeness and divided these into alcohols,

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ketones/aldehydes, acetates, terpenes and sesquiterpenes. Similarly Cruz Roblero

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et al.77 collected volatiles onto Super Q absorbent and analysed eluted aliquots.

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Although they found fewer compounds, 37 compounds in C. arabica and 41 in C.

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canephora, they linked their chemical analyses to the responses of the insect.77

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Sesquiterpenes, such as α-copaene, together with other volatiles (methyl salicylate,

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2-heptanone, 2-heptanol and phenyl ethyl alcohol) were components that individually

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elicited significant electroantennographic responses from CBB adults.77 As part of an

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integrated pest management (IPM) strategy it is also useful to consider the effects of

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compounds on natural enemies: methyl salicylate, limonene and longifolene can

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attract the natural enemies of CBB.78,79 In contrast, verbenone and limonene, can be

Alcohols predominated in all



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used to repel other coffee pests, such as the black twig borer, Xylosandrus

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compactus (Eichhoff) (Coleoptera: Curculionidae: Scolytinae).80

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(iv)

Fats, carbohydrates and lipids

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The availability of nutrients in plant material can be affected by the presence of

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toxins and metabolic inhibitors, so measuring the levels of fats carbohydrates and

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lipids does not always indicate the nutriment that is available to an herbivore.81 In

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general, plants that are more nutritive for insects are likely to support a larger

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population of pests that reproduce more rapidly and cause more damage.81

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Much of the work on nutritional content of coffee has concentrated on the

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harvested or roasted bean and while some degree of caution is advisable in

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extrapolating these results, these data are useful as they can indicate differences in

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the nutrients available to insect pests of coffee. The fat content of harvested beans

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cannot on its own differentiate between varieties or plants grown at different

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elevations.45,82 However, the ratio of fatty acids in blended coffees can be used to

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discriminate between C. arabica and C. canephora.83 At higher elevations the leaf to

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fruit ratio increases as leaves survive longer, resulting in an increase in carbohydrate

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and bean fat synthesis.71 Environmental conditions can affect levels of fructose,

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glucose and sucrose in beans as plants grown under 60% shading accumulate

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greater levels than those that are either more or less shaded.70 While sucrose

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content of green coffee beans is greater for C. arabica than C. canephora33 sugars

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per se are thought to be most informative as chemical characters when considered

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with other chemical constituents as part of the metabolome.39

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(2).

Pesticidal plants

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As part of an IPM strategy, there is considerable potential for the use of pesticidal

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plants to be expanded for the control of crop pests, especially in Africa84 where

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economic constraints favour low-cost and local approaches to crop management.92

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A few plant species have been tested for their effects on CBB (Table 1) and

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fungal entomopathogens.86-90 Essential oils can be toxic to CBB,88-90 but their

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extraction requires costly specialist equipment.91 Most of the extracts of four different

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plant species in either water or ethanol, were toxic to CBB, but there was variability

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among different plant parts and between solvents.86 In summary, ethanol extracts

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were generally more repellent to CBB, with Moringa oleifera Lam. (Moringaceae)

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(roots) and Tephrosia purpurea (L.) Pers. (Leguminosae) (seeds) showing the

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greatest effect against CBB when applied to leaves, while water extracts of M.

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oleifera (leaves and seeds) and Nerium oleander L. (Apocynaceae) (leaves) were

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the most repellent.86 When extracts were applied to coffee berries, Azadirachta

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indica A. Juss. (Meliaceae) (leaves) was the most repellent.86

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chemical constituents of these extracts was not established, it is possible to use the

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available literature to approximate a picture of the compounds that could cause the

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activity. The essential oils of M. oleifera have been used as fumigants against stored

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product pests,92 but the activity of this plant is derived primarily from lectins93,94 which

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inhibit the enzyme trypsin, and therefore reduce the digestion of protein from foods.95

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Lectins may also have affected the germination of the CBB fungal entomopathogen


Even though the


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Beauveria bassiana (Balsamo) Vuillemin (Ascomycota: Hypocreales) observed by

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Zorzetti et al.86

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Much is known about the chemistry of Tephrosia sp.,96 but there is limited

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information on the insect-activity of T. purpurea (Table 1). Tephrosia vogelii Hook f.

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is insecticidal97 and contains insecticidal rotenoids, although these compounds do

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not occur in all chemotypes of T. vogelii.98

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biological activities against insects, for example, toxicity, developmental inhibition

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and feeding deterrence.99,100 The component tetranotriterpenoids in extracts of A.

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indica can deter feeding at nanomolar concentrations.100-102 It is more common for

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the seed kernels of A. indica to be tested for insecticidal effects as these contain

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insecticidal limonoids,99 and may have been more toxic if they had been assessed

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instead of leaves.

Azadirachta indica, has a range of

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Although N. oleander can repel insects that are not adapted to feed on the

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plant,103 it is poisonous for vertebrates104 as it contains cytotoxic cardiac glycosides

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(cardenolides)105-107 and triterpenoids,108,109 among other compounds.110

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terebinthifolia Raddi (Anacardiaceae) is an invasive weed111 and is unusual as the

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research effort is focussed on finding insects that will feed on the plant and therefore

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act as biological control agents.112 Santos et al.88 found that the essential oils from

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leaves could cause significant mortality of CBB, especially when diluted oils were

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topically applied. Similarly, essential oils from fruit and seeds of S. terebinthifolia are

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toxic to Anopheles, Culex and Stegomyia larvae,113,114 but the composition of

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essential oils varies seasonally,115 so insecticidal effects are also likely to also vary.

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Some of the phenolic components of extracts from S. terebinthifolia have been

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characterised,116-118 but their effect on pest insects, has not been determined.


Schinus

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By the late 1990s nearly 600 chemical constituents had been identified from the

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genus Piper (Piperaceae), even though only 84 from 700 extant species had been

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studied to that point.119,120 Piper alatabaccum Trel. & Yunck. would share some of

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the same chemical components while also containing novel compounds.121 Acetone

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extracts of the roots were tested for their effects on CBB by Santos et al.87 and

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showed promise as 0.5mg mL-1 crude extracts were toxic, although they did not

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observe repellence even at 100 mg mL-1.

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The data from trials of pesticidal plants shows that they have considerable

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potential as a sustainable method of controlling CBB and other insect pests of

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coffee. Even a small sample of eight plants contains a wide range of biologically

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active compounds, with the caveat that many are toxic to humans.

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consider that between 1971 to the end of 2013, 168 different chemicals have been

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identified from Tephrosia species96, pesticidal plants are an un-tapped resource full

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of potential insecticidal compounds. Due consideration needs to be given to the

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interaction of pesticidal plants with natural enemies, pathogens of coffee pests and

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other beneficial insects, such as pollinators.

When we

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(3).

Implications for IPM in coffee

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A sustainable and holistic approach to coffee pest management would include

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breeding for chemical resistance to pests, with appropriate use of natural enemies

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(e.g., Jaramillo et al.122) and pesticidal plants. It is possible that hybridization of wild

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and cultivated species may breed plants that are resistant to pathogens and pests10

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while also producing a palatable beverage.123 There is very little genetic variation in

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the self-pollinated C. arabica based on the fact that many of the plantations in the

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New World tropics are derived from a single tree from Amsterdam Botanic



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Garden.124,125 Generally, worldwide plantations of both C. arabica and C. canephora

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have been derived from limited genetic stock.126,127 Despite this relatively small gene

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pool it is possible to differentiate species and varieties of Coffea using their chemical

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profiles.

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character to distinguish between C. arabica and C. canephora.128,129 Furthermore,

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increased introgression of genes from C. canephora to C. arabica can be detected in

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the volatile profile as the level of kahweol and the ratio of kahweol to another

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diterpene (cafestol) increase.128 The concentration of the alkaloid trigonelline and

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sugars such as sucrose can also vary between different coffee species.33 The

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knowledge gained from these studies of quality and varietal differences would be

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useful to guide entomologists and ecologists in selecting plants that could be tested

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experimentally for their resilience to CBB and other insects. Many of the coffee

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compounds discussed above, such as caffeine and CQAs (e.g., Clifford et al.130)

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would contribute to chemical resistance due to their proven effects on coffee pests

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and pathogens.

For example, kahweol is a diterpene that can be used as a chemical

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Effective pesticidal plants would be complimentary to naturally bred resistance,

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but more research is required both to evaluate a wider range of plants and to

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optimise the use of the material. Leaf extracts of T. vogelii and S. terebinthifolia are

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toxic to CBB, but many of the other plants that have already been tested against

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CBB show comparatively low toxicity (34-75% mortality), although it could be argued

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that any intervention that reduces the population of CBB would be of benefit. To

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convince farmers to persevere with pesticidal plants it is essential for treatment to

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give noticeable improvements in crop health and yield at an affordable cost.85

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CBB has a worldwide distribution10 but there are other equally devastating,

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regional pests, such as Antestiopsis, which is not found worldwide, but is present in


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22 countries1 in Sub-Saharan Africa,131-133 such as Burundi,17 Cameroon,134

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Kenya,135 Rwanda19,136 and Uganda.18,137 This emphasis on CBB is reflected in the

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literature as a bibliographic search138 using either Antestiopsis or Hypothenemus and

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coff* gave 327 hits (CBB) and 10 hits (Antestiopsis). The focus on CBB does not

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take into account the relative impact of different Antestiopsis species in Africa.

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Farmers in Africa are already aware of pesticidal plants as locally harvested

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materials are increasingly used for control of other crop pests.139 Antestiopsis adults

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and nymphs are also a better target for pesticidal plants as they remain exposed on

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the plant surface, whereas female CBBs spend most of their life cycle protected

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inside the berry. Production, processing and distribution of coffee beans provides vital incomes to

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farmers, especially in rural areas of Africa 140,141 and South America.142 Given the

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importance of coffee it is surprising that there are so many questions that remain

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unanswered, especially regarding the biology and control of Antestiopsis. We

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conclude that studies of different coffee chemotypes, together with research into

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pesticidal plants could be used to develop novel and cost-effective IPM strategies for

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coffee pests.

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ACKNOWLEDGEMENT

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We would like to thank three anonymous reviewers for their comments on the manuscript.

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Excludes Zanzibar as a separate country, as it is a semi-autonomous part of Tanzania.



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Figure 1. Female coffee berry borer (Hypothenemus hampei) on coffee seed (Left) and detail of female coffee berry borer head (right). Photos by P. Grebb, USDA, ARS (left) and G. Bauchan, USDA, ARS (right).


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Table 1: Some plants that have been evaluated for the control of CBB.

Plant

Activity(i.e. ≥ 30% mortality) against CBB

Examples of activity against other pests

Aeollanthus pubescens Benth.

220ppm crude essential oil (LD50)90

-

Azadirachta indica A. Juss

10% w/v ethanol extract of leaf (44%)86

Multiple99

Moringa oleifera Lam.

10% w/v ethanol extracts of leaf (48%) and seed (62%)86

Stored product pests92

10% w/v water extract of seed (56%)86 Nerium oleander L.

10% w/v ethanol extract of leaf (34%)86

Leafcutter ants143

Ocimum canum L.

320ppm crude essential oil (LD50)89

Macrotermes subhyalinus144

Piper alatabaccum Trel. & Yunck

0.5 mg ml -1 of a dried acetone extract (75% after 48 h)87

Anopheles darlingi145

Schinus terebinthifolia Raddi.

10-2 to 10-8 v/v dilutions of essential oil (100% to 30%)88

Disease vectors113 114

Tephrosia purpurea (L.) Pers.

10% w/v ethanol extracts of leaf (96%) and root (36%)86

Ae. aegypti146



338x190mm (96 x 96 DPI)

ACS Paragon Plus Environment

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ACS Paragon Plus Environment

Can Coffee Chemical Compounds and Insecticidal Plants Be

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