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Agricultural and Environmental Chemistry

Pest Management Strategies Against the Coffee Berry Borer (Coleoptera: Curculionidae: Scolytinae) Francisco Infante J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.7b04875 • Publication Date (Web): 12 Mar 2018 Downloaded from http://pubs.acs.org on March 13, 2018

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Journal of Agricultural and Food Chemistry

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For: Journal of Agricultural and Food Chemistry

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Running Title: Pest Management of the CBB

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Pest Management Strategies Against the Coffee Berry Borer

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(Coleoptera: Curculionidae: Scolytinae)

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Francisco Infante

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El Colegio de la Frontera Sur (ECOSUR), Carretera Antiguo Aeropuerto km 2.5,

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Tapachula, 30700 Chiapas, México

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Address Correspondence to:

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Dr. Francisco Infante

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Carretera Antiguo Aeropuerto km 2.5

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Tapachula, 30700 Chiapas, México

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Phone: +52 962-6289800 Fax: +52 962-6289806

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E-mail: [email protected]

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ACS Paragon Plus Environment


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ABSTRACT: Coffee (Coffea arabica and C. canephora) is one of the most widely traded

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agricultural commodities and the main cash crop in ca. 80 tropical countries. Among the

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factors that limit coffee production, the coffee berry borer, Hypothenemus hampei

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(Ferrari) has been considered the main insect pest, causing losses of over US$500

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million dollars annually. Control of this pest has been hindered by two main factors: the

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cryptic nature of the insect (i.e., protected inside the coffee berry), and the availability of

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coffee berries in the field allowing the survival of the pest from one generation to the

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next. Coffee berry borer control has primarily been based on the use of synthetic

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insecticides. Management strategies have focused on the use of African parasitoids

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(Cephalonomia stephanoderis, Prorops nasuta and Phymastichus coffea), fungal

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entomopathogens (Beauveria bassiana), and insect traps. These approaches have had

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mixed results. Recent work on the basic biology of the insect has provided novel insights

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that might be useful in developing novel pest management strategies. For example, the

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discovery of symbiotic bacteria responsible for caffeine breakdown as part of the coffee

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berry borer microbiome opens new possibilities for pest management via the disruption

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of these bacteria. Some chemicals with repellent propieties have been identified and

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these have a high potential for field implementation. Finally, the publication of the CBB

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genome has provided insights on the biology of the insect that will help us to understand

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why it has been so successful at exploiting the coffee plant. Here I discuss the tools we

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now have against the CBB, and likely control strategies that may be useful in the near

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future.

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KEYWORDS: Hypothenemus hampei, coffee, Rubiaceae, Coffea arabica, Coffea

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canephora, pest control.


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INTRODUCTION

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Coffee (Coffea sp.) is predominantly an African genus that comprises 124 species.

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Arabica coffee (Coffea arabica L.) and Robusta coffee (Coffea canephora Pierre ex A.

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Froehner), are the two commercial species that are widely cultivated and used in the

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production of coffee. Although Africa is the origin of both species, they came from

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different environments; C. arabica originated in the upland evergreen forests of southern

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Ethiopia, whereas C. canephora is native to the lowland humid forests between Uganda

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and Cameroon.

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subtropical countries, where they are now among the most important cash crops.

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Approximately 11 million hectares worldwide are planted with coffee producing

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approximately 9 million tonnes annually.

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market, coffee remains one of the most valuable agricultural commodity in international

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world trade. The economic revenue in coffee producing countries is about US$12 billion

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annually, while the value of the coffee industry has been estimated at US$173 billion. 5

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The perennial evergreen nature of coffee favours the attraction of a number of

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arthropods.

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coffee, either as phytophagous arthropods or their predators and parasitoids.

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these, more than 850 species of insect are known to feed on the coffee tree,

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approximately 30 species cause economic losses, including the coffee berry borer

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(Curculionidae), leaf miners (Lyonetiidae), antestia bugs (Pentatomidae), stem borers

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(Cerambycidae),

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(Coccidae), aphids (Aphididae), and mealybugs (Pseudococcidae). 6, 9, 10

6

1, 3

1, 2

.

Both species have been introduced into many tropical and

4

Despite the fluctuating prices of the world

More than 3000 species of insects and mites have been associated with

twig

borers

(Curculionidae),

whiteflies


(Aleyrodidae),

7 8

Of and

scales


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With losses over US$500 million annually,

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hampei (Ferrari), is the most devastating pest of coffee worldwide.

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Central Africa, this pest has now been reported in almost every country where the coffee

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plant has been introduced. The first report on the presence of H. hampei outside Africa

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came from Indonesia in 1908.

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1913.

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Americas and the Caribbean. Studies involving molecular methods to track the

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dissemination of the CBB suggested that there were three separate introductions to the

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Americas, and that West Africa was the origin of introductions into America and Asia.

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After this, the CBB slowly spread to the rest of coffee producing countries in the world.

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The most recent detections of this insect in Puerto Rico in 2007,

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and Papua New Guinea in 2016, show that phytosanitary measures to stop H. hampei

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had failed in every country.

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Because H. hampei feeds and reproduces within the coffee seeds inside the coffee

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berry, it is considered a direct pest that negatively affects the crop by causing losses in

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yield and quality. Green and ripe berries are susceptible to attack by the insect.

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dry matter content of the endosperm is the critical factor determining attack; green

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berries with less than 20% dry matter in the endosperm are either abandoned after an

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initial attack, or the female waits for several days in the tunnel she has bored until the

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endosperm has developed.

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green fruit with less than 20% dry matter, these berries are often lost, either by

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premature fall or by decay, because H. hampei damage allows the entry of saprophytic

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microorganisms.

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dry matter (approximately 2-3 months after flowering), because at this stage adult

13, 14

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the coffee berry borer, Hypothenemus 5, 9

Originally from

Later, this pest invaded the Americas through Brazil in

From Brazil H. hampei dispersed to other coffee growing areas in the

18, 20, 21

18, 19

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Hawaii in 2010,

9

15

17

The

Although the coffee berry borer does not breed in

Severe damage also occurs when fruit have more that 20% of


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females colonises the seeds (edosperm).

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H. hampei consume the endosperm, thereby greatly reducing the quality and economic

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value of infested seeds, which can only be sold as a low-grade product.

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100 individuals (eggs, larvae and adults) have been recorded in a single coffee fruit,

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and an estimated density of 11 million borers per hectare has been reported in Mexican 24

During their life cycle, adults and larvae of

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More than 23

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coffee plantations.

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and pest management measures should be performed at earlier stages of infestation, as

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should become clear farther on. As several reviews have been published on the biology

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and ecology of this insect,

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reasonable strategy to manage the coffee berry borer infestations.

Such high infestation levels are difficult to manage at this stage,

5, 19, 20, 21, 25

the aim of the present work is to propose a

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SYNOPSIS OF THE MAIN METHODS FOR CONTROL THE COFFEE BERRY BORER

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Several pest management strategies have been used against the coffee berry borer.

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One of the oldest methods is the cultural (manual) control, i. e., the removal and

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destruction of infested coffee berries (which serve as source for new infestations) to

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reduce the population levels. In theory, this is perhaps the most effective method of

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control against the insect that may perform at any stage of coffee fruit development.

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27, 28

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approximately 80% of the population.

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advantageous, this practice greatly increases the costs of production. 30

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Synthetic insecticides have been widely used against the coffee berry borer. The

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commercial availability, ease of application in the field, and insecticidal efficacy, have

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favoured their use in some countries. Brazil pioneered the use of synthetic organic

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insecticides against H. hampei in 1947,

26,

In Colombia the manual removal of mature berries was found to eliminate 27, 29

31

Despite being effective and environmentally

and this practice was adopted extensively by



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African countries in 1949.

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insecticide endosulfan became the most effective and widely used synthetic compound

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for controlling the insect. A single application of endosulfan reduced CBB infestation up

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to 88% and provided good control for up to 12 weeks.

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insecticide resulted in development of resistance in New Caledonia,

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problems like chronic human intoxication, toxicity to aquatic fauna and non-target

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organisms, and environmental persistence of up to eight months.

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endosulfan has been banned in at least 70 countries. 35, 36 Other insecticides have been

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evaluated against H. hampei with promising results. For instance, pirimiphos-methyl,

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fenitrothion, chlorpyrifos and fenthion, resulted in 98% pest mortality when applied at the

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time the CBB was boring into the coffee berry. 37

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Biological control of H. hampei using three African parasitoids has been another method

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widely used in many countries since the 1980’s. The parasitoids Prorops nasuta

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Waterston (Bethylidae), Cephalonomia stephanoderis Betrem (Bethylidae), and

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Phymastichus coffea LaSalle (Eulophidae), have been introduced in over 15 countries

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outside Africa. This pest management strategy is known as classical biological control

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and unfortunately, results with the coffee berry borer have not been satisfactory.

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three species have been unable to maintain high population levels in the field, such that

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multiple releases of parasitoids have to be performed through the growing season.

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Although the establishment of these species occurs in most coffee plantations,

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parasitoid populations decreased dramatically in the absence of frequent releases and

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the pest population does not fall below the economic threshold. 5, 21, 27, 29, 39 The effect of

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parasitoids on the coffee berry borer has been unsatisfactory as a single method of

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control and other measures of control are needed to check the pest.

In the 1960’s, the broad-spectrum organochlorine


32

Extensive use of this

34

33

and in other

For these reasons,

29, 38, 39

14

All

5

In the case

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of biological control using entomopathogens, the cosmopolitan fungus Beauveria

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bassiana (Balsamo) Vuillemin (Ascomicota: Hypocreales) has been found infecting H.

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hampei adults in coffee plantations wherever the borer is present. The incidence of B.

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bassiana is usually higher when there are young berries attacked by the insect and

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under rainy conditions.

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attempts to control the coffee berry borer. A common practice to increase the natural

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infection of B. bassiana is to culture isolates collected from the field and spray the

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conidial suspensions on coffee berry borer infested fruit.

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levels of mortality up to 84% under field conditions,

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synthetic insecticides. However, the main disadvantages of using B. bassiana is the

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slow infection process that allows the adults live long enough to damage the coffee

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berry, the fast deactivation of conidia after spraying, and high production costs. 30, 40, 43

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Several types of traps to capture coffee berry borer adults have been developed. One of

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these traps is commercially available under the name BROCAP® and uses a mixture of

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ethanol and methanol as an attractant and has been employed in numerous countries.

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This trap can be used permanently throughout the coffee producing cycle, but is likely to

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be more valuable in capturing residual adults after the harvest period. According to

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Dufour

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day when infestations are high. However, to reduce costs, most coffee growers use

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artisanal traps to capture this insect. In Mexico, weekly captures of artisanal traps

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ranged from 83 to 1484,

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adults per week.

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these traps a single method of control do not solve the problem, and other measures of

44

40

The fungus has been widely used throughout the world in

42

41

This practice can result in

similar to the performance of

a single BROCAP® trap can capture more than 10,000 H. hampei adults per

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45

whereas in Brazil, other traps have captured 77 to 609

However effective in capturing coffee berry borer adults, the use of



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control are needed. It is important to point out that alcohol-based traps are not specific to

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the CBB and they may capture and kill many other insects not considered as pests. 47

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USING WHAT WE HAVE: A STRATEGY TO CONTROL THE COFFEE BERRY

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BORER

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An effective strategy to control the coffee berry borer should involve an Integrated Pest

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Management (IPM) approach, in which multiple tactics are combined to reduce the pest

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populations to tolerable levels while maintaining a quality environment.

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available pest control technologies against the coffee berry borer, control measures

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should start when coffee is being harvested (Fig. 1). In fact, the harvesting and

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processing of coffee is itself a major mortality factor for the H. hampei population, where

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most individuals inside the berry die, while a few others escape from the coffee

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fermentation tanks and return to the field. 49, 50, 51 Considering that the coffee berry borer

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can only feed and reproduce in coffee, it is important to reduce the number of surviving

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adults that will eventually infest the fruit of the following coffee cycle. In countries that

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have only one coffee harvest per year, the recommendations are: (i) to carry out efficient

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harvesting, avoiding leaving residual fruit on coffee trees or on the ground, and (ii) to use

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coffee berry borer traps after harvesting to catch and kill residual adults. The

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effectiveness of these two measures will determine the prevalence of the CBB

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infestation in the next cycle. The use of traps may continue when fruit are absent in the

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field and until the following fruiting cycle. A density of 22 traps per hectare uniformly

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distributed, drastically decreased the prevalence of CBB infestation from one season to

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the next. 52


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By using the

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Coffee flowering begins immediately after the rainy season.

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frequency of rainfall, there may be one, two, or more flowering periods. As a

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consequence, several fructifications may occur in a single year, but there will be always

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a main fructification that will concentrate most of the coffee berries. 54 Depending on the

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altitude of coffee plantations, berries will be susceptible to H. hampei attack 2-3 months

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after flowering.

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the field on trees or on the ground after harvesting.

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subsequently leave these fruits to infest the new ones. It is at this time that sprays of B.

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bassiana are recommended, as conditions at this moment are usually ideal for effective

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pest control: low population levels of the pest, high humidity favouring survival and

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germination of the fungus, starving and possibly weak adults that may be more prone to

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fungal infection, and individuals outside the berry or just initiating the boring of the berry,

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among others. A novel trap that combines the use of alcohols and B. bassiana has been

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recently developed.

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colonizing females, contaminate them with B. bassiana, and disperse the fungus in

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coffee plantations after CBB females exited the device. With a mortality of CBB adult

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females from 66 to 92% under field conditions, this trap has a great potential to be used

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as an IPM component.

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Phymastichus coffea, can be undertaken 2-3 weeks after B. bassiana sprays in order to

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reduce the risk of parasitoid mortality due to fungal infection.

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of H. hampei adults controlled by these two natural enemies, the smaller the number of

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progeny and coffee berry damage at harvest.

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Coffee berry borer adults that are not killed by B. bassiana or P. coffea, will penetrate

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and colonise coffee fruits. Inside the seed, the CBB female will oviposit and larvae will

18, 22

Depending on the

Coffee berry borer adults can survive up to 156 days in fruit left in

55

9

The surviving adults will

Using a mixture of ethanol and methanol, the trap attracts

55

Releases of the coffee berry borer adult parasitoid


56

The higher the number


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feed on the same seed to grow and reach the adult stage.

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field is ca. 45 days.

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can be increased through releases of the parasitoids C. stephanoderis and P. nasuta,

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which parasitizes larvae and pupae of the CBB. 20

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Although all the elements for this conceptual strategy have been known for a long time,

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and are implemented in some coffee producing countries, their systematic use to

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achieve a sustainable coffee berry borer management has not been undertaken for

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several reasons. In some cases only one or two types of control are used regardless the

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fruiting phenology of coffee. In other cases, control measures against H. hampei are

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initiated too late in the season, when the insect is already inside the berry and has

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reached high levels of infestation. Under this situation control is difficult to achieve

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because the insect is protected within the fruit and has already reproduce. For this

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reason it is necessary to combine the above mentioned methods of control with due

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attention to timing and fruiting phenology, in order to obtain adequate control of this pest.

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The generation time in the

Mortality of the coffee berry borer population during this phase

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RECENT FINDINGS WITH POTENTIAL FOR CONTROL OF THE COFFEE BERRY

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BORER

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Studies on the microbiota of the coffee berry borer have revealed a wide array of

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microorganisms associated with this insect. Pérez et al.

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in 21 genera isolated from the insect cuticle, gut, and faeces. Fusarium, Penicillium,

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Candida and Aspergillus were the dominant genera. Carrión & Bonet

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fungal species associated with the adult stage. More recently, Ceja-Navarro et al.

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identified 13 bacterial species in the alimentary canal that were able to breakdown

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caffeine: Brachybacterium rhamnosum, Enterobacter sp., Jonesiaceae, Kosakonia


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reported 39 species of fungi

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identified 12 60

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cowanii, Microbacterium binotii, Novosphigobium sp., Ochrobactrum sp., Pantoea

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vagans,

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Stenotrophomonas maltophilia. Antibiotics added to H. hampei artificial diet eliminated

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caffeine degradation, demonstrating the involvement of bacteria in the process. The

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caffeine demethylase gene (ndmA) was expressed in vivo in field specimens as well as

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in P. fulva isolated from the coffee berry borer gut. Diet inoculation with P. fulva restored

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the ability to degrade caffeine (Fig. 2). The remarkable discovery of caffeine

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detoxification in H. hampei opens new research options to manage this pest. Right now

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is too early to propose a practical way to use this information, but the basic idea would

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be to find a mechanism to interfere with the bacteria involved in caffeine detoxification.

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This eventual interference would likely result in the death of the insect.

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Very little is known about the genome of coleopteran species, and a recent study

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reported the genome of H. hampei, the third species reported for this order of insects.

250

The coffee berry borer genome is approximately 163Mb with 19222 predicted protein-

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coding genes. Genome analysis revealed four important aspects of the CBB biology: (i)

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indications of 10 cases of putative horizontal gene transfers from bacteria, (ii)

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paralogous expansion of the antimicrobial peptide repertoire, (iii) the presence of

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enzymes involved in the degradation of complex polysaccharides, and (iv) the presence

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of the gene Rdl, that confers resistance to cyclodiene insecticides, such as endosulfan.

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60

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prove useful in the development of novel technologies for the management of this insect.

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The identification and use of repellents is another promising tool against the CBB.

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Different degrees of repellency of verbenone and methylcyclohexenone were reported in

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the coffee berry borer.

P.

septica,

P.

eucalypti,

Pseudomonas

fulva,

P.

fluorescens,

and

61

However more research is needed, the study provides valuable information that may

62

Jaramillo et al.

63

confirmed H. hampei avoidance to



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verbenone and mentioned that α-pinene was another repellent for this insect. Vega et al.

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berry borer produced by infested coffee fruits, with remarkable results in a field test in

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Hawaii. The results showed up to an 80% decrease in CBB captures in traps with 3:1

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methanol:ethanol attractant, and a bubble cap formulation of (E,E)-α-farnesene,

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compared to traps containing the attractant only.

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To conclude, it is clear that the current technologies for coffee berry borer control require

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intensive labour and careful monitoring to keep the pest under control. Recent studies

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on the microbiota of H. hampei, its genome, and chemical repellents have greatly

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expanded our knowledge of this insect, and will likely provide novel insights of use in the

271

development of pest managemernt strategies in the near future.

identified a sesquiterpene, (E,E)-α-farnesene, as a potential repellent of the coffee

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ACKNOWLEDGEMENTS

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I would like to thank three anonymous reviewers, whose comments helped improve this

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manuscript. Trev Williams (INECOL) provided a valuable language revision.

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Fig. 1. The conceptual strategy to control the coffee berry borer, using a combination of

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several methods of control, based on the fruiting phenology of coffee.

470 471

Fig. 2. Graphic representation of the experiment conducted by Ceja-Navarro et al.

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caffeine degradation in the alimentary canal of the coffee berry borer, Hypothenemus

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hampei.

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TOC Graphic 254x190mm (96 x 96 DPI)


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Figure 1 254x190mm (96 x 96 DPI)



Figure 2 254x190mm (96 x 96 DPI)


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Coleoptera: Curculionidae: Scolytinae - ACS Publications

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