BProceedingslack Twig Boforer the andHawaiian Tropical Entomological Nut Borer inSociety (2012) Beans 44:71–78 71

First Report of Exploitation of Coffee Beans by Black Twig Borer ( Compactus) and Tropical Nut Borer (Hypothenemus obscurus) (Coleoptera; : Scolytinae) in Hawaii

Elsie B. Greco* and Mark G. Wright Department of Plant and Environmental Protection Sciences, University of Hawaii at Manoa, 3050 Maile Way, Honolulu, HI 96822. *Corresponding author, [email protected]; Phone: (808) 956-2451; Fax: (808) 956-2448

Abstract. The black twig borer, Xylosandrus compactus, is an ambrosia that was reported in Hawaii in 1960 and attacks branches of more than 200 plant , including coffee. This beetle was found for the first time boring coffee berries in the district of Hilo on the island of Hawaii. reached the endo- sperm and caused damage without making galleries or ovipositing. The tropical nut borer, Hypothenemus obscurus, is a pest of macadamia nuts that has been in Hawaii since 1988 and was recently found for the first time in Hawaii attacking coffee berries. Its entry hole was observed close to the blossom area or the side of the berry. Sometimes damage was caused near the endosperm but no galleries or eggs were found. Descriptions of the biology, behavior and management of these beetles are provided in this paper.

Key words: Coffea arabica, coffee berry, Xylosandrus compactus, Hypothenemus obscurus

The landscape of the Kona district of the in 1961 attacking pink tecoma, Tabebuia island of Hawaii is characterized by a wide pentaphylla (L.) Hemsl. on Oahu (Beard- diversity of plant species, including both sley 1964), and it is now present on all endemic and naturalized plants (Elevitch major islands of the state (Hara and Beard- et al. 2009). Coffee (Coffea arabica L.), sley 1979, Bittenbender and Easton Smith macadamia nut (Macadamia integrifolia 1999). The black twig borer is classified Maiden & Betche), and (Persea as an because the parent americana Mill.) are the main agricultural beetles provide a food source of fungus for crops in Kona (Beardsley 1990, Jones et their offspring (Hara 1977, Burbano 2010). al. 1992, Bittenbender and Easton Smith The black twig borer is a familiar pest of 1999). Vegetation surrounding coffee coffee in the Kona area, where it bores plantations in Kona often includes plants into stems and causes branches to die that are hosts for several Scolytinae spe- back. The tropical nut borer was reported cies such as the black twig borer Xylosan- in Hawaii in 1988, attacking macadamia drus compactus Eichhoff and the tropical nuts, and its impact is most serious in the nut borer Hypothenemus obscurus Fabri- drier production areas (Beardsley 1990, cius (Coleoptera: Curculionidae) (Hara Jones et al. 1992). Neither of these species 1977, Hara and Beardsley 1979, Jones has previously been reported to attack the 2002). The black twig borer was reported berries of coffee. This paper describes 72 Greco and Wright the biology, damage and management of was first reported in Fort Lauderdale, X. compactus and H. obscurus in coffee Florida in 1941 (Ngoan et al. 1976) and berries in Hawaii. has spread throughout the southeast US, General characteristics of the black along the coastal plain from Texas to twig borer and tropical nut borer. North Carolina. In Hawaii, this beetle The family Curculionidae, subfamily was first reported in 1961 attacking pink Scolytinae, comprises ambrosia beetles tecoma, Tabebuia pentaphylla (L.) Hemsl. that have a symbiotic association with (Beardsley 1964) on Oahu, and it is now fungi and live in wood or other plant present on all major islands of the state tissue, as well as bark beetles and other (Hara and Beardsley 1979, Bittenbender sub-cortical feeding beetles (Rudinsky and Easton Smith 1999). 1962). All species of the tribe Xyleborini Hypothenemus obscurus has been re- are ambrosia beetles and the black twig ported in Florida, Puerto Rico, Mexico, borer, Xylosandrus compactus, is among Guatemala, Nicaragua, Costa Rica, Co- the most economically important species lombia, Panama, Dominican Republic, of this tribe (Wood 1982) (Fig. 1A). This Trinidad, Guyana, Venezuela, Surinam, beetle lives in symbiotic association with Brazil, South Africa, Southeast Asia, and ambrosia fungus cultivated on the walls Jamaica (Wood 1982). This beetle was first of galleries in stems constructed by the reported in Hawaii attacking macadamia female (Hara 1977, Beaver 1989, Daehler nuts in the Kona district of Hawaii island and Dudley 2002). Members of the tribe (Beardsley 1990) and it is now present on Cryphalini, unlike the ambrosia beetles, all major islands of the state (Jones et al. are primarily phloeophagous, feeders of 1992). phloem tissues of the inner bark, or my- Biology. The black twig borer repro- elophagous, feeders on pith within small duces by a form of haplodiploidy (arrhe- stems (Wood 1982). Among the members notokus parthenogenesis), whereby males of the tribe Cryphalini is the tropical nut develop from unfertilized eggs (Hara borer, H. obscurus (Fig. 1B) a pest of 1977). Adult females produce haploid macadamia nuts (Beardsley 1990, Jones males from unfertilized eggs, while fertil- 2002). ized eggs produce diploid female progeny. Origin and distribution. Xylosandrus It is possible however, that a functional compactus attacks more than 200 host haplodiploid breeding system occurs in plant species, including macadamia nut this species, as is the case in closely re- (Macadamia integrifolia F. Muell), litchi lated species (Brun et al. 1995), where the (Litchi chinensis Sonn), avocado (Persea male progeny have the full chromosomal americana Mill), anthurium (Anthurium component, albeit with one chromosome spp. Schott), mango (Mangifera indica set condensed and non-functional. L), coffee (Coffea arabica L.), Eucalyp- Pupation and mating of brood adults tus spp., and koa (Acacia koa A. Gray) occurs within the infested plant material (Hara 1977). The black twig borer is na- before emergence of the brood. Damage tive to Asia and is widespread in Japan, to plants is caused only by adult females; Vietnam, Indonesia, Malaya, Sri Lanka, the male is flightless, remains in the brood Madagascar, South India, Seychelles, galleries and is rarely observed outside the Mauritius, West Africa, Fiji, Cuba, and plant. Female beetles excavate the tunnels Brazil (Venkataramaiah and Sekhar 1964, into the host plant and inoculate the plant Vasquez et al. 1996, Oliveira et al. 2008). with an ambrosia fungus, which is the In the United States, the black twig borer source of nutrients for larvae and adults Black Twig Borer and Tropical Nut Borer in Coffee Beans 73 A B

Figure 1. Dorsal view of adults of Xylosandrus compactus (A, left) and Hypothenemus obscurus (B, right).

(Ngoan et al. 1976, Hara and Beardsley trees by boring into the wood (Kajimura 1979, Beaver 1989). Females initiate cut- and Hijii 1994). However, X. compactus is ting the xylem after reaching the pith one of the few ambrosia beetles that attack (cambium) and excavate it along the twig healthy plants as well as plants that are on either side of the initial entrance tunnel under stressed conditions such as drought, to make a brood chamber where the eggs pruning, or recent transplanting (Hara and are laid. Beardsley 1979, Jones and Johnson 1996, The tropical nut borer exhibits a female- Hayato 2007, Burbano 2010). biased sex ratio, incestuous inbreeding Xylosandrus compactus females bore a (sib-mating) as usually attributed to hole into the branch and construct galler- haplodiploidy, whereby unfertilized eggs ies (Fig. 2A) where they then lay eggs (Fig. result in males (Constantino et al. 2011). 2B) (Hara 1977). There are two potential The life stages consist of the egg stage, two mechanisms through which the black twig larval instars, the pupa, and the adult, and borer can cause damage to, or the death it takes 28 days at 26°C to develop from of, the host plant: mechanical damage and egg to adult (Constantino et al. 2011). the introduction of the ambrosia fungus, Females bore a hole in the pericarp of which may be phytopathogenic (Hara macadamia nuts and construct galleries in and Beardsley 1979, Daehler and Dudley the endosperm where eggs are deposited 2002). Mechanical damage might also be in the husk or in the kernel, and larvae caused by feeding subsequent to excava- can be found in either location (Jones et tion of the gallery and the inoculation of al. 1992, Constantino et al. 2011). Females the ambrosia fungus introduced by the lay between 10 and 30 eggs. Adults and female (Hara and Beardsley 1979). larvae feed within the kernel. After mat- Initially, leaves of infested branches ing, females bore several holes in the turn light green (Fig. 3A), and wilted endocarp and emerge to colonize other leaves and bark beyond the affected area fruits (Jones et al. 1992, Constantino et al. turn brown or black within a few days of 2011). Males are smaller than the females, beetle attack (Fig. 3B) (Ngoan et al. 1976, and are flightless. Daehler and Dudley 2002). The dieback of Damage to host plant material. twigs is the result of the mechanical dam- Beetles of the subfamily Scolytinae are age to water-conducting vessels caused by among the most damaging in the beetle boring (Daehler and Dudley 2002). world. Their cryptic life cycles inside the Subsequent necrosis in the bark and the host plant make these insects difficult to desiccated zone in the xylem is likely the control (Rudinsky 1962). Most ambrosia result of the invasion of associated fungi beetles attack unhealthy, stressed, or dying into the twig tissue, which then invades the 74 Greco and Wright

A B

Figure 2. Gallery of Xylosandrus compactus in coffee branches. Xylosandrus com- pactus female adults (left) and immature stages (right).

A B

Figure 3. Damage symptoms of X. compactus in coffee branches. First leaves turn light green (A, left), then the wilted leaves and bark beyond the affected area turn brown or black (B, right). xylem of the tree, obstructing the flow of stages were not observed. This type of water and nutrients (Hayato 2007). damage was observed in a coffee farm with Xylosandrus compactus has previ- a high level of black twig borer infestation, ously been reported attacking branches trees under stress conditions, and a high or saplings (Ngoan et al. 1976, Hara and density of coffee berries. X. compactus Beardsley 1979, Oliveira et al. 2008, typically lives inside branches and feeds on Burbano 2010). However, in July 2007, ambrosia fungus, and this is the first report females were observed attacking coffee of this beetle attacking coffee berries. Ber- berries in Hawaii in samples from the ries with black twig borer attack become district of Hilo, Hawaii (19.605556 N susceptible to microorganisms, such as 155.045556 W) (Fig. 4A). Females were bacteria or fungi, which cause necrosis of observed burrowing a hole into the fruit the area around the entrance hole. around the blossom area and on the side of Hypothenemus obscurus damage oc- the berry. Damage to the fruit was through curs both in macadamia nuts that are on the exocarp and mesocarp, and occasion- the tree and those that have dropped to ally the tunnel reached the endocarp (Fig. the ground. During the first 7 to 10 days 4B). The damage was characterized by on the ground, females bore the husk and a single hole, and galleries or immature tunnel directly through the shell and into Black Twig Borer and Tropical Nut Borer in Coffee Beans 75

A B

Figure 4. Xylosandrus compactus boring coffee berries around the blossom area. X. compactus boring a coffee berry (A, left), hole made by X. compactus on the endo- sperm (B, right); galleries or immature stages were not found.

A B

Figure 5. Damage of Hypothenemus obscurus to coffee berries. Holes were observed around the blossom area or on the side of the berry (A, left) and sometimes holes were observed reaching the endosperm (B, right). the kernel (Jones et al. 1992). A single en- (Fig. 5B). No H. obscurus immature trance hole is observed on green husks on stages or galleries were found inside the trees, and multiple holes are observed the beans. Hypothenemus obscurus was in mature husks on the ground and on the observed attacking coffee berries when trees (Beardsley 1990, Jones et al. 1992). coffee plantations were located close to Hypothenemus obscurus is similar in size macadamia plantations. In Colombia, H. and appearance to H. seriatus (Eichhoff), obscurus is a pest of macadamia nuts and which has been in Hawaii for several years has been recorded attacking coffee berries (Beardsley 1990). Hypothenemus seriatus without affecting the beans (endosperm) infests branches and occasionally attacks (Constantino et al. 2011). Under labora- seeds (Beardsley 1990). tory conditions, H. obscurus fed on coffee Hypothenemus obscurus was found and 3% of the beans presented superficial tunneling inside coffee branches and damage (Constantino et al. 2011). Thirty- boring into coffee berries around the two percent of the fruits had H. obscurus blossom area (Fig. 5A) or on the side of immature stages present, feeding on pulp the berry, penetrating to the endosperm and mucilage between the beans, and 76 Greco and Wright these were able to develop to adult stage optera: Silvanidae), has been observed (Constantino et al. 2011). Galleries were inside macadamia nuts feeding on the not observed inside beans, and only one tropical nut borer (Jones et al. 1992). egg was laid inside a bean. The present This facultatively predacious beetle was study further confirms the polyphagous also found on coffee trees, inside coffee nature of H. obscurus, including coffee branches, and inside coffee berries feed- as a food source. ing on larvae of the black twig borer and Management. The management of X. on larvae of the Mediterranean fruit fly compactus in Hawaii has focused on the Ceratitis capitata (Diptera: Tephritidae) use of cultural practices such as sanitation (Burbano 2010). This predator can be (removing and destroying the infested ma- considered a potentially useful natural terial) (Burbano 2010). Jones and Johnson enemy for black twig borer, the tropical nut (1996) reported that destruction of pruned borer and other coffee pests with cryptic branches using chippers or shredders behavior. results in approximately 90% mortality The Hawaii Department of Agriculture of the beetles in the stem. Promoting tree introduced and released three Braco- health and vigor has also been recom- nidae species for X. compactus control mended to help in resisting infestation in 1961. They were Dendrosoter ener- or recovering from attack (Jones and vatus Marsh, Dendrosoter protuberans Johnson 1996). Several parasitoids were Nees, and Ecphylus sp. None became released by the Hawaii Department of established (Bernarr Kumashiro, HDoA, Agriculture in 1961 for biological control personal communication). The Eulophidae of X. compactus; however, there were no subfamily Tetrastichinae contains two follow-up studies of their establishment species, Phymastichus xyleborini and in Hawaii. Burbano et al. (2012) studied P. coffea, which attack adult stages of the efficacy of lures and repellents as scolytines (Graham 1987, Chang 1993, another management technique. Japanese LaSalle 1990). Phymastichus xyleborini beetle traps baited with ethanol are an was reported in Hawaii attacking adults of important tool for monitoring black twig Xyleborus perforans Wollaston (Coleop- borer populations, predicting outbreaks, tera: Curculionidae), a pest of macadamia and possibly as a physical control through nuts (LaSalle 1995). Phymastichus coffea mass trapping. is present in Africa and attacks the cof- The management of H. obscurus has fo- fee berry borer (Hypothenemus hampei) cused mainly on cultural practices (Jones there (LaSalle 1990). Although no host et al. 1992). Tropical nut borer damage information exists for P. coffea from in macadamia nuts can be reduced by other areas, it is possible that this species harvesting every two to three weeks and might be present in Hawaii. Therefore, processing nuts immediately. Although they might be good candidates for future this control method was developed for a studies in biological control programs different crop, it may be applicable to H. for the black twig borer, the tropical nut obscurus in coffee following the discov- borer, and the coffee berry borer. To the ery of its feeding habit in coffee berries, extent that these biological control agents should damage levels become economi- may be useful in suppressing damage by cally significant. these three beetles, it will be important to Presence of natural enemies for avoid disrupting their populations through coffee borers in Hawaii. The predatory indiscriminant use of insecticides. beetle Cryptamorpha desjardinsi (Cole- Black Twig Borer and Tropical Nut Borer in Coffee Beans 77 Acknowledgments pest, on Acacia koa in the Hawaiian Islands. This work was funded by grants from Micronesica Supplement. 6: 35–53. USDA (TSTAR), and Hatch grants ad- Elevitch, C.R., T. Idol, J.B. Friday, C. 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