Where to sample? Ecological implications of sampling strata in determining abundance and impact of natural enemies of the coffee berry borer,Hypothenemus hampei

Several parasitoids of African origin have been introduced to coffee producing areas of the Americas and Asia as biological control agents of the coffee berry borer (CBB) Hypothenemus hampei (Coleoptera: Curculionidae). These parasitoids have become established in the field but their effect on the CBB has been limited. A two-year field study in Western Kenya has found Prorops nasuta (Hymenoptera: Bethylidae) to be the predominant parasitoid emerging from CBB-infested coffee berries collected on coffee trees or from the ground. P. nasuta comprises more than 75% of the total natural enemies collected. The density of P. nasuta was 90% higher in the berries collected from the ground than from the trees. Its hyperparasitoid, Aphanogmus sp. (Hymenoptera: Ceraphronidae), also emerged from both type of berries. Across the two seasons, the average P. nasuta density per berry was 18–35 times higher than that of Aphanogmus sp. Throughout the two years sampled, significantly higher numbers of P. nasuta and Aphanogmus sp. occurred between February and March, which coincides with the beginning of the rainy season. Higher numbers of live CBB females were recorded in berries collected from the trees. Nevertheless, mortality of adult CBB was considerably higher from January to March and started to decrease from April onwards. The possibly negative effects of cultural control practices in Latin America which include the removal of berries fallen to the ground on biological control of CBB are discussed, and the use of screened collection devices for these berries which would permit the release of parasitoids but prevent escape of the pest is proposed.     

Efficacy of plant essential oils against two major insect pests of coffee (Coffee berry borer,Hypothenemus hampei,and antestia bug,Antestiopsis intricata) and maize weevil,Sitophilus zeamais

Coffee berry borer, antestia bug and maize weevil are serious pest of coffee and maize, respectively. Bioassays of plant essential oils were conducted with coffee berry borer, antestia bug and the maize weevil. Essential oils of Thymus vulgaris, Aloysia sp., Ruta chalepensis, Chenopodium ambrosioides and Cymbopogon nardus resulted in 80%–90% mortality of coffee berry borer, whereas essential oils of C. ambrosioides, T. vulgaris and R. chalepensis achieved 87.5%–92.5% mortality of antestia bug. Essential oils of C. ambrosioides caused significantly the highest percentage mortality of the maize weevils (95%) with “Lethal Dose” (LD₅₀) values of 2.202 ml 100 ml^?1 within 24 h after treatment, whereas essential oils of Mentha spicata, T. vulgaris and R. chalepensis resulted in 82.5%, 77.5% and 73.5% mortality, respectively. The potential of plant essential oils for the management of coffee berry borer, antestia bug and maize weevil for the small-scale farmers is discussed.     

Alternative Hosts for Bethylid Parasitoids of the Coffee Berry Borer, Hypothenemus hampei (Coleoptera: Scolytidae)

Three species of bethylid wasps, Prorops nasuta Waterston, Cephalonomia stephanoderis Betrem, and C. hyalinipennis Ashmead, attack the coffee berry borer, Hypothenemus hampei (Ferrari) (Coleoptera: Scolytidae), by both predation and parasitism. C. hyalinipennis has only recently been reported to attack H. hampei. Its previously recorded hosts belong to the coleopteran families Curculionidae, Anobiidae, and Scolytidae. We evaluated five further coleopteran species, in the families Curculionidae, Bostrichidae, and Bruchidae, as alternative hosts. High proportions of all five species were both fed upon and oviposited on (normally by concurrent host feeding). Offspring developmental mortality varied greatly (12–95%) on different host species. Offspring production per host was about three times greater than on H. hampei when females were presented with the curculionids Caulophilus oryzae (Gyllenhal) and two species of Sitophilus. C. stephanoderis and P. nasuta are currently the main biological control agents of H. hampei: they have long been thought to be monophagous but C. stephanoderis has recently been reported to attack H. obscurus. We evaluated C. oryzae, as a potential host or prey for P. nasuta, and both C. oryzae and Sitophilus sp. for C. stephanoderis. Host feeding was very common in both parasitoid species. The majority of females also oviposited on C. oryzae (71% P. nasuta, 60% C. stephanoderis) and 20% of C. stephanoderis parasitized Sitophilus sp. Fifty-two percent of C. stephanoderis and 7% of P. nasuta offspring survived to adulthood when developing on C. oryzae. The lifetime fecundities of these parasitoids presented with these host species were, however, low (maximum 17 eggs, mean ≤ 8.25) and preoviposition periods were generally long (ca. 19 days). Adult female C. stephanoderis lived longer when presented C. oryzae rather than Sitophilus sp. Host feeding also increased longevity. We discuss these results in the context of mass rearing these bethylids for release as biological control agents.     

Behavioural responses of bethylid parasitoid species of the coffee Berry borer to chemicals cues from host and non-host dust/frass

The bethylid wasps Cephalonomia stephanoderis Betrem and Prorops nasuta Waterston are parasitoids of the coffee berry borer, Hypothenemus hampei (Ferrari), the most serious insect pest of coffee worldwide. Recent studies on the host location behaviour of these parasitoids have shown that females are attracted to volatile compounds released by immature stages and dust/frass of H. hampei. Also, these studies have reported that the locomotory behaviour of parasitoids is influenced by contact chemical cues from host dust/frass. In this study, we investigated the responses of females of both species to volatiles and contact cues from dust/frass from different sources. Volatiles from dust/frass from H. hampei-infested coffee and maize infested with Sitophilus sp were attractive to P. nasuta females. In contrast, C. stephanoderis females were only attracted to the volatiles from dust/frass from H. hampei-infested coffee. Volatiles from an artificial diet used for rearing H. hampei were not attractive to females of both species. The effect of methanolic extracts from dust/frass from different sources on the patch-searching time of parasitoids was analysed using the Ethovision software. P. nasuta females spent more time in the patches treated with extracts of dust/frass from H. hampei-infested berries, artificial diet, and from maize infested with Sitophilus sp than on patches treated with dry coffee extract or solvent control. C. stephanoderis females spent more time on patches treated with dust/frass extracts from H. hampei-infested berries and artificial diet than on patches treated with an extract of dust/frass from maize infested with Sitophilus sp, an extract of dry coffee, and methanol control.     

An aphidiine parasitoid Monoctonia vesicarii (Hymenoptera: Braconidae) and three chalcidoid hyperparasitoids of Pemphigus matsumurai (Homoptera: Aphididae) forming leaf galls on Populus maximowiczii in Japan

More than 300 unopened leaf galls formed by the pemphigine aphid Pemphigus matsumurai on Populus maximowiczii were collected at Nakasatsunai, Hokkaido, Japan, in July and September 2007 and kept in cold conditions during winter. From mummified fundatrices in the galls an aphidiine parasitoid Monoctonia vesicarii and three species of hyperparasitoids belonging to Pteromalidae, Eupelmidae and Eulophidae emerged from March to May 2008. Monoctonia vesicarii, which is new to Japan, is redescribed. The eulophid hyperparasitoid is described as a new species, Aprostocetus (Aprostocetus) doronokianus, and the pteromalid and eupelmid hyperparasitoids are identified as Pachyneuron sp. and Eupelmus sp., respectively. Approximately 180 unopened mummies of P. matsumurai were dissected in August and November 2008 and a living larva of M. vesicarii was found in each of 17 of them. These observations suggest that some individuals of M. vesicarii pass through two‐year cycles. The implications of the three species of hyperparasitoids to P. matsumurai galls are discussed.     

Life history studies of <Emphasis Type="Italic">Prorops nasuta</Emphasis>, a parasitoid of the coffee berry borer

Life history studies were conducted in the laboratory on the African parasitoid Prorops nasuta Waterston (Hymenoptera: Bethylidae), a parasitoid of the coffee berry borer, Hypothenemus hampei (Ferrari) (Coleoptera: Scolytidae). The female wasp enters an infested coffee berry, kills the adult borer and seals the entrance of the berry with the body of the borer, impeding the entry of other organisms into the berry. The preoviposition period ranges from 3 to 14 days (mean 5.42 ± 0.37 SE). During this time females feed on the immature stages and paralyse fully grown larvae and pupae of the CBB. P. nasuta is an idiobiont solitary ectoparasitoid. Eggs are laid externally on the last instar larvae and pupae. Mean development time (egg to adult) for males and females was 27.7 (±0.37 SE) and 30 (±0.12 SE) days, respectively. Median survival for wasps fed on final instar CBB larvae was 27.7 days, significantly longer than any other treatment, while for females without food it was 2.5 days. In culture, females produced an average of 4.3 (±0.39 SE) progeny during their lifetimes. Adults began emerging at 30.6 days (±0.28 SE) after cultures were started and peak production was reached at 36 days, declining thereafter. Males normally emerged from coffee beans 2–3 days before females. Males usually emerged from 07:00 to 09:00h and females from 10:00 to 14:00 h. The culture sex ratio (proportion of males) was 0.21. Virgin females produced only male offspring.     

Evaluation of Beauveria bassiana (Ascomycota: Hypocreales) as a control of the coffee berry borer Hypothenemus hampei (Coleoptera: Curculionidae: Scolytinae) emerging from fallen,infested coffee berries on the ground

The effects of Beauveria bassiana strains on coffee berry borers (CBB), which emerge from infested berries left on soil, and its impact on the infestation of coffee berries on tree branches were evaluated at two Experimental Stations (Naranjal-Caldas and Paraguaicito-Quindio) in the Colombian coffee zone. Using a completely randomized design with 10 repetitions, 50 coffee berries artificially infested with CBB were placed on the base of a coffee tree. Four treatments including B. bassiana strain Bb9205, a mixture of Cenicafé strains (Bb9001, Bb9024 and Bb9119), a commercial formulation of B. bassiana and a control (water) were sprayed with 1×10⁹ conidia per tree. After 30 days, all fungal strains lowered the infestation levels of the coffee berries on the trees at both locations. The mixture of Cenicafé strains decreased the tree infestation between 50 and 30% at both locations. In the berries dissected from each treated tree, insect mortality was about 40% at both locations compared to 15% in the control. B. bassiana strains also decreased the insect population inside the newly infested berries on the trees by 55–75%. The mixture of Cenicafé strains was the most effective for decreasing insect populations. B. bassiana significantly decreased CBB populations that emerged from fallen, infested, coffee berries and reduced future insect generations.     

Interactions among bethylid parasitoid species attacking the coffee berry borer,Hypothenemus hampei (Coleoptera: Scolytidae)

The question of whether biological control is most likely achieved by deploying single or multiple species of biological control agents is much debated. While utilizing several natural enemies may enhance control, there is also the potential for disruptive inter-specific interactions. Such interactions may be studied in the laboratory by focusing on the details of the interactions themselves and attempting to infer population level consequences from their sum, or by focusing more directly on the overall effects on natural enemy populations: we term these approaches ‘reductionist’ and ‘holistic.’ Here we conduct a holistic laboratory study on interactions between three species of parasitoid wasps that are parasitoids of the coffee berry borer, Hypothenemus hampei (Ferrari) (Coleoptera: Scolytidae): Cephalonomia stephanoderis Betrem, C. hyalinipennis Ashmead and Prorops nasuta Waterston (all Hymenoptera: Bethylidae). We find evidence for both intra- and inter-specific resource competition. Interactions between C. stephanoderis and P. nasuta, both indigenous to Africa, appear to be approximately symmetrical, while C. hyalinipennis, naturally found in the coffee plantations of Chiapas, Mexico, may exert a disruptive influence. C. hyalinipennis also has a low population growth rate. We now consider it to be a detrimental invader of the Mexican coffee agro-ecosystem that should not be encouraged by augmentative release or introduced into other regions. Overall, the most successful species, in terms of both emergence and female production, was P. nasuta. We compare these results with those from prior reductionist and holistic studies, and with observations on patterns of establishment of these bethylid species in the field. Given that it is increasingly clear that disruptive inter-specific interactions are generally common when multiple species are deployed in biological control, screening of potential agents should consider such interactions alongside the more ‘traditional’ focus on host specificity.     

Altitude and coffee production systems influence extent of infestation and bean damage by the coffee berry borer

The coffee berry borer (CBB), Hypothenemus hampei Ferrari (Coleoptera: Curculionidae: Scolytinae), is one of the major insect pests of coffee worldwide. The present study was designed to assess the level of infestation of coffee berries at different developmental stages across different altitudes and coffee management systems. The experiment was carried out at three locations in southwestern Ethiopia under two coffee management systems and four coffee berry development stages with three replications. Results of the study showed significantly highest proportion of damaged berries (37.5%), number of holes per berry (10.88) and number of adult CBB per berry (7.55) on dried leftover berries at low-altitude study sites. On the other hand, the lowest mean percent damaged berries, number of holes per berry and number of adults were recorded at mid- and high-altitude study sites. The study also showed that, CBB caused significantly highest damage in plantation coffee management system than garden coffee. Results of this study highlight proper harvesting at red ripe stage in order to minimise incidence of CBB. It is also important to design integrated management strategies to mitigate CBB damage especially in lowland plantation coffee production systems.     

Behavior and Activity Pattern of Cephalonomia stephanoderis (Hymenoptera: Bethylidae) Attacking the Coffee Berry Borer,Hypothenemus hampei (Coleoptera: Scolytidae)

We describe behavioral sequences and daily activities of pre-ovipositing and ovipositing females of Cephalonomia stephanoderis (Hymenoptera: Bethylidae), an ectoparasitoid of the coffee berry borer, Hypothenemus hampei (Coleoptera: Scolytidae). Noticeable behavioral differences among preovipositing and ovipositing females include host examination, host stinging—probing, host feeding, and the oviposition per se. The female of C. stephanoderis feeds primarily on host eggs, but pupae are also exploited, mainly by pre-ovipositing females. After the onset of the oviposition period, C. stephanoderis examines the pupae repeatedly, stings them at frequent intervals, and spends more time feeding than during the pre-oviposition period. Host paralysis is linked both to host feeding and oviposition. It induces irreversible developmental arrest, which presumably allows preservation of the host until subsequent utilization, and contributes to successful offspring development, particularly by reducing host motility. Oviposition consists in a host selection process, a prolonged period of preparation of the potential host, and the egg-laying phase itself. Under our experimental conditions, pre-ovipositing and ovipositing females are active 17% and 36% of the day, respectively. Host handling time averages 6% and 23% in pre-ovipositing and ovipositing females, respectively. All coffee berry borer developmental stages are exploited by C. stephanoderis females, either for host feeding and/or oviposition activities. Such flexible behavior is advantageous given that host availability is limited inside the coffee berries.     

Natural parasitism of Metaparasitylenchus hypothenemi (Tylenchida: Allantonematidae) on the coffee berry borer in Chiapas,Mexico

We assessed the parasitism of Metaparasitylenchus hypothenemi on its host, the coffee berry borer, in 20 coffee plantations of Mexico. A total of 23,568 adult borers were dissected, with 179 of these infected with nematodes (0.76% infection rate). Although the level of parasitism is not encouraging, the nematode is another natural enemy, which limits the population growth of this pest in Mexico.     

Field superparasitism by Phymastichus coffea, a parasitoid of adult coffee berry borer, Hypothenemus hampei

Superparasitism by Phymastichus coffea LaSalle (Hymenoptera: Eulophidae), a parasitoid of adults of the coffee berry borer, Hypothenemus hampei (Ferrari) (Coleoptera: Curculionidae: Scolytinae), was recorded under field conditions in a coffee plantation in Colombia. Parasitoid adults were released 1, 5, and 9 days after artificial infestations of 90‐, 150‐, and 210‐day‐old coffee berries with H. hampei females. The position of the beetle inside the berry and the number of P. coffea larvae per female host were assessed 10 days after each parasitoid release. Under laboratory conditions, P. coffea usually lays two eggs per host, one female and one male. In our studies, we often recorded more than six P. coffea larvae in an individual host and mean numbers of larvae per host ranged from two to 4.45. Superparasitism by P. coffea under field conditions was influenced by the age of the coffee berries, which is the most important factor determining the speed of penetration by H. hampei, and therefore the time the beetles are exposed to a P. coffea attack. The number of parasitoid larvae in each H. hampei female gradually decreased with the age of the berry, and also linearly decreased with the time of parasitoid release. Age‐dependent effects of coffee berries that alter the ratio of available hosts to searching parasitoids by providing refuges to the herbivore, largely determine the extent of superparasitism of H. hampei by P. coffea under fields conditions in Colombia.     

Manipulating tropical fire ants to reduce the coffee berry borer

1. The coffee berry borer Hypothenemus hampei (Coleoptera, Curculionidae) (Ferrari) is the most important pest of coffee production worldwide. 2. The hypothesis that the tropical fire ant, Solenopsis geminata Westwood, indirectly protects the coffee berry borer by suppressing other ant species that are the coffee berry borer's primary predators was tested. 3. It was found that removing S. geminata from coffee plots significantly increased the disappearance of adult coffee berry borer beetles from coffee berries compared with control plots. An average of 6% of beetles disappeared from plots with S. geminata whereas 23% of beetles disappeared from plots from which S. geminata was removed. This pattern was observed on two shade coffee farms with marked differences in ant species composition, one in the rainforest in central Costa Rica and one in the cloudforest in northwest Costa Rica. 4. If the results of this small‐scale study can be replicated on the farm level, then S. geminata suppression may represent a new management technique for the coffee berry borer throughout Central and South America.     

The biology of Phymastichus coffea LaSalle (Hymenoptera: Eulophidae) under field conditions

The coffee berry borer (CBB) Hypothenemus hampei (Ferrari) (Coleoptera: Curculionidae: Scolytinae) was accidentally introduced into México in 1978, and rapidly became the main pest of coffee. As an exotic pest, its management has been mainly based on biological control methods through the introduction of parasitoids from Africa. In this context, at the beginning of the present decade, the parasitoid Phymastichus coffea LaSalle (Hymenoptera: Eulophidae) was imported to Mexico. Since then, several studies have been carried out as part of the post introduction evaluation of this parasitoid. In this paper, information concerning the parasitism and life-cycle of P. coffea in coffee farms is presented with the objective of providing information that elucidates its role as a biological control agent. P. coffea showed highly significant preferences for allocation of two eggs per host, usually one female and one male. Both offspring are able to develop and reach the adult stage successfully. Lifespan of adults is 2–3 days only. The degree of parasitism by P. coffea was more than 95% at the three altitudes tested, when releases consisted of a ratio of 10 CBB:1 parasitoid. The median survivorship of CBB parasitized by this wasp was 13, 15 and 19 days at the low, medium and high altitude coffee zones, respectively. The parasitism by P. coffea was higher when parasitoid releases were carried out simultaneously with the CBB, and decreased with the time between host and parasitoid releases. We showed that using P. coffea at a density of 1 parasitoid per 10 hosts resulted in a 3- to 5.6-fold decrease in CBB damage to the coffee seeds when compared to the control. The importance and value of these results are discussed in terms of the use of P. coffea as a biological control agent of the CBB in Latin America.     

Current status of coffee berry disease (Colletotrichum kahawae Waller & Bridge) in Ethiopia

The current status of coffee berry disease (CBD) caused by Colletotrichum kahawae was intensively assessed and examined in 152 sample coffee farms from 22 districts across major coffee growing regions of Ethiopia. The results showed that CBD was prevalent with significantly (p < 0.001) varied intensity of damage among fields, districts and zones. The highest disease incidence of 70.7, 65.3 and 59.3% was recorded in Hararghe, Gedeo and Jimma, with correspondingly higher severity of 42.7, 46.7 and 32.0%, respectively. The national average incidence and severity of CBD was 52.5 and 29.9% that indicated the present status of the disease is remarkably on increasing trend. The increased intensity of CBD was strongly associated with reduced disease management practices (r = 0.50), altitude (r = 0.42), coffee cultivars (r = 0.23) and production systems (r = 0.28). This empirical evidence shows that CBD is on an upsurge and remains a major challenge to Arabica coffee production in Ethiopia.     

Effect of host‐cocoon mass on adult size in the secondary hyperparasitoid wasp,Pteromalus semotus (Hymenoptera: Pteromalidae)

Abstract Parasitoids have long proven to be model organisms in studying resource‐related constraints on immature development. Here we examine the relationship between host cocoon (= pupal) size in the gregarious endoparasitoid wasp, Cotesia glomerata, and development time and adult size in the solitary idiobiont hyperparasitoid, Pteromalus semotus. Little is known about the biology or ecology of this ecto‐hyperparasitoid species, although it is one of the major secondary hyperparasitoids of C. glomerata. The size of the adult wasp covaried with the size of the host cocoon at parasitism. Moreover, female wasps were larger than male wasps for a given cocoon size. Adult wasps have remarkably long life‐spans, 3 months on average. Longevity did not significantly differ with sex. We also examined how larvae of P. semotus exclude other potential competitors. P. semotus is protandrous, with females taking significantly longer to complete their development than males. In experiments where several eggs of P. semotus were placed on individual pupae of C. glomerata, newly hatched hyperparasitoid larvae moved rapidly over the surface of the host and destroyed the eggs of any conspecifics by biting them before they would initiate feeding on host tissues. Our results are discussed in relation to those with other studies with solitary ichneumonid idiobiont hyperparasitoids of C. glomerata.     

Identification of a coffee berry borer‐associated yeast: does it break down caffeine?

Two yeasts isolated from laboratory reared adult coffee berry borers [Hypothenemus hampei (Ferrari) (Coleoptera: Scolytidae)] and from insects collected in the field in Colombia were identified as Pichia burtonii Boidin and Candida fermentati (Saito) Bai, based on sequencing of the nuclear large subunit 26S rDNA variable D1/D2 domain. Liquid culture experiments using P. burtonii in media containing different caffeine levels indicated that caffeine levels in a range found within coffee seeds can retard yeast growth. HPLC analysis shows that P. burtonii does not break down caffeine.     

A flagellate protozoan from Mythimna separata (Lepidoptera: Noctuidae)

Abstract

A trypanosomatid flagellate, Herpetomonas sp., is recorded from an adult Mythimna separata (Walker) (Lepidoptera: Noctuidae). Promastigote, paramastigote, and opisthomastigote stages measured 3.4–12 × 1.3–4.3 μm, Giemsastained, with flagella measuring 13.8–18.7 μm. A few amastigotes (3.9–8.3 × 3.7–6.7 μm) were also observed. Fourteen larvae fed with a suspension of flagellates were found later to be infected with the protozoan. No flagellate infections were found in the hymenopteran parasitoid, Apanteles ruficus (Haliday), or the hyperparasitoid, Trichomalopsis sp.     

Potential of the parasitoid Heterospilus prosopidis (Hymenoptera: Braconidae) as a vector of plant-pathogenic Colletotrichum spp.

A braconid parasitoid Heterospilus prosopidis was contaminated with either Colletotrichum coffeanum or C. gloeosporioides, causal agents of coffee berry disease and mango anthracnose respectively. Adult parasitoids could collect wetted and unwetted spores of both pathogens on their bodies. Viable spores were recovered in washings from these insects 10 days after infestation. Wetted spores of both species of pathogen had lower viability on the parasitoid's body than unwetted spores, probably because of the loss of the mucilage coating which protects against desiccation. The results suggest that the use of a related parasitoid, H. coffeicola, in biological control against the coffee berry borer, Hypothenemus hampei could pose a phytosanitary risk.     

Diets of Frugivorous Bats in Montane Rain Forest and Coffee Plantations in Southeastern Chiapas,Mexico

Frugivorous are one of the main diaspore dispersers in tropical ecosystems, particularly in open areas and sites in the early stages of ecological succession. Frugivorous bat species respond differentially to habitat modification, and in the context of their diaspore dispersal functions it is important to understand species' ecological requirements. We compared the diversity of diaspores, obtained from fecal samples and from fruits carried by frugivorous bats, among five shaded coffee plantations under different management regimes and a montane rain forest in southeastern Chiapas, Mexico. At each site, bats were captured every 2 mo from March 2004 to July 2005, using six mist‐nets, during two consecutive nights. We captured 2589 individuals from 18 frugivorous species, from which we collected 969 fecal samples, containing 42 diaspore species associated with early and late successional plants. Although, we captured more frugivorous bat species in montane rain forest, the number of diaspore species in this site (N=14) was not significantly different from the coffee plantations under different management regimes (16–24). In montane rain forest, Sturnira ludovici fed mainly on Piper auritum, but in coffee plantations ate Peperomia sp., Saurauia madrensis, Solanum chrysotrichum and Solanum diphyllum. Artibeus jamaicensis and Artibeus intermedius feed mostly Cecropia obtusifolia and Ficus cookii in all coffee plantations. We suggest that the presence of frugivorous bats in shaded coffee plantations is favored by trees and shrubs associated with secondary and introduced vegetation that farmers have allowed to grow within or around the plantations.