Twig-Nesting Ants: The Hidden Predators of the Coffee Berry Borer in Chiapas,Mexico

Coffee is a globally important crop that is subject to numerous pest problems, many of which are partially controlled by predatory ants. Yet several studies have proposed that these ecosystem services may be reduced where agricultural systems are more intensively managed. Here we investigate the predatory ability of twig-nesting ants on the main pest of coffee, the coffee berry borer (Hypothenemus hampei) under different management systems in southwest Chiapas, Mexico. We conducted both laboratory and field experiments to examine which twig-nesting ant species, if any, can prey on free-living borers or can remove borers embedded in coffee fruits and whether the effects of the twig-nesting ant community differ with habitat type. Results indicate that several species of twig-nesting ants are effective predators of both free-living borers and those embedded in coffee fruits. In the lab, Pseudomyrmex ejectus, Pseudomyrmex simplex, and Pseudomyrmex PSW-53 effectively removed free-living and embedded borers. In the field, abundance, but not diversity, of twig-nesting ant colonies was influenced by shade management techniques, with the highest colony abundance present in the sites where shade trees were recently pruned. However, borer removal rates in the field were significant only in the shadiest site, but not in more intensively managed sites. This study provides evidence that twig-nesting ants can act as predators of the coffee berry borer and that the presence of twig-nesting ants may not be strongly linked to shade management intensity, as has been suggested for other arthropod predators of the borer.     

Ants defend coffee from berry borer colonization

Ants frequently prevent herbivores from damaging plants. In agroecosystems they may provide pest control services, although their contributions are not always appreciated. Here we compared the ability of eight ant species to prevent the coffee berry borer from colonizing coffee berries with a field exclusion experiment. We removed ants from one branch (exclusion) and left ants to forage on a second branch (control) before releasing 20 berry borers on each branch. After 24 h, six of eight species had significantly reduced the number of berries bored by the berry borer compared to exclusion treatment branches. While the number of berries per branch was a significant covariate explaining the number of berries bored, ant activity (that varied greatly among species) was not a significant factor in models. This study is the first field experiment to provide evidence that a diverse group of ant species limit the berry borer from colonizing coffee berries.     

Metaparasitylenchus hypothenemi n. sp. (Nematoda: Allantonematidae), a parasite of the coffee berry borer, Hypothenemus hampei (Curculionidae: Scolytinae)

Metaparasitylenchus hypothenemi n. sp. (Nematoda: Allantonematidae) is described from the coffee berry borer, Hypothenemus hampei (Ferrari) (Curculionidae: Scolytinae), in Chiapas, Mexico. This species differs from other members of the genus by its small size, annulated cuticle, lateral fields with 3 ridges, free-living stages with an excretory pore located between the pharyngeal gland orifices, a distinct stylet with basal swellings in free-living females, a postvulval uterine extension, a thin stylet lacking basal swellings in males, 2 separate spicules, a gubernaculum, and a peloderan bursa. Parasitic females are white, with a straight or slightly curved body and are ovoviviparous. Third-stage juveniles emerge from parasitized beetles and molt twice before reaching the adult stage. Because the coffee berry borer is the most important pest of coffee throughout the world and this parasite partially or completely sterilizes female beetles, it is worthy of further investigation as a potential biological control agent.     

Agroforestry management affects coffee pests contingent on season and developmental stage

1 Management of vegetational diversity in agroecosystems is a potentially regulating factor of pest population dynamics and may affect developmental stages in different ways.
2 We investigated the population dynamics of red spider mites, coffee leaf miners, and coffee berry borers in three management types of coffee agroforests: increasing plant diversity from a few shade tree species (simple-shade agroforests), intermediate-shade tree species (complex-shade agroforests) to high-shade tree species (abandoned coffee agroforests) in Ecuador. Furthermore, we studied how changes in agroforestry management affect population stage structure of each coffee pest.
3 Our results show that agroforestry management affected seasonal patterns of coffee pests in that higher densities of red spider mites were observed from August to December, coffee leaf miners from December to February, and coffee berry borers from May to July. Moreover, specific developmental stages of red spider mites, coffee leaf miners, and coffee berry borers differed in their responses to agroforestry management. During all stages, red spider mite reached higher densities in simple-shade agroforests compared with complex-shade and abandoned agroforests. Meanwhile, coffee leaf miner densities decreased from simple-shade to complex-shade and abandoned agroforests, but only for larvae, not pupae. Similarly, only coffee berry borer adults (but not eggs, larvae and pupae) demonstrated a response to agroforestry management. Environmental variables characterizing each agroforestry type proved to be important drivers of pest population densities in the field.
4 We emphasize the importance of considering seasonal differences and population structure while investigating arthropod responses to different habitat types because responses change with time and developmental stages.     

On the Eyes of Male Coffee Berry Borers as Rudimentary Organs

The coffee berry borer, Hypothenemus hampei, is the most damaging insect pest of coffee worldwide. Like males in other species in the genus, male coffee berry borers have a lower number of facets in the compound eyes than females. The rudimentary eyes in male coffee berry borers could be an evolutionary response to their cryptic life habit, whereby they are born inside a coffee berry and never leave the berry. The main objective of the study was to determine if the differences in the number of facets translates into differences in visual acuity. We used low-temperature scanning electron microscopy to visualize and quantify the number of facets in the compound eyes. There was a significantly lower (p<0.0001) number of facets in males (19.1±4.10) than in females (127.5±3.88). To assess visual acuity, we conducted optomotor response experiments, which indicate that females respond to movement, while males did not respond under the conditions tested. The coffee berry borer is an example of an insect whereby disuse of an organ has led to a rudimentary compound eye. This is the first study that has experimentally tested responses to movement in bark beetles.     

Cascading indirect effects in a coffee agroecosystem: effects of parasitic phorid flies on ants and the coffee berry borer in a high-shade and low-shade habitat

Nonconsumptive effects (NCE) of parasites on hosts vary with habitat complexity thereby modifying trait-mediated effects on lower trophic levels. In coffee agroecosystems, Pseudacteon sp. phorid fly parasites negatively affect Azteca instabilis F. Smith ants via NCE thereby indirectly benefiting prey. It is unknown how differences in habitat complexity influence Azteca-phorid interactions or how phorids affect the coffee berry borer (Hypothenemus hampei Ferrari), an important pest of coffee (Coffea arabica L). We tested the following hypotheses in field and lab experiments to find the impact of NCE of phorids on A. instabilis and trait-mediated indirect effects of phorids on the coffee berry borer: (1) Phorid effects on A. instabilis differ between complex and simple shade habitats and (2) Phorids, by modifying A. instabilis behavior, indirectly affect coffee berry borer abilities to invade coffee berries. Phorids had greater impacts on A. instabilis activity in low-shade farms, but differences in phorid impacts were not mediated by phorid density or light availability. In the lab, phorids had strong cascading effects on abilities of A. instabilis to deter coffee berry borers. Without phorids, A. instabilis limited coffee berry borer attacks, whereas when the coffee berry borer was alone or with A. instabilis and phorids, more coffee fruits were attacked by coffee berry borer. These results indicate that A. instabilis has stronger biological control potential in high-shade farms, but the exact mechanism deserves further attention.     

Influence of host density on the reproductive strategy of Cephalonomia stephanoderis, a parasitoid of the coffee berry borer

The effect of the density of the coffee berry borer, Hypothenemus hampei (Coleoptera: Scolytidae) on reproductive and host-feeding behaviours of the parasitoid Cephalonomia stephanoderis (Hymenoptera: Bethylidae) was evaluated under laboratory conditions. The number of hosts used for oviposition was density-dependent at low host density. Beyond a density of six hosts/day, the oviposition rate reached a maximum of 1.2 eggs/day due to egg limitation. Cephalonomia stephanoderis females responded to increasing host availability with a linear increase in host feeding. Overall, parasitoids killed more coffee berry borers by feeding and paralysis than by parasitism. At low host density, the pre-oviposition phase was extended, oogenesis was delayed, more males were produced, and host feeding occasionally occurred concurrently with oviposition. We suggest that the efficacy of C. stephanoderis as a biological control agent depends on seasonal variations in host density. Inoculative vs inundative releases in coffee plantations are discussed in relation to the abundance of the coffee berry borer during the fructification and interharvest periods.     

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.     

Spiroacetals in the Colonization Behaviour of the Coffee Berry Borer: A ‘Push-Pull’ System

Coffee berries are known to release several volatile organic compounds, among which is the spiroacetal, conophthorin, an attractant for the coffee berry borer Hypothenemus hampei. Elucidating the effects of other spiroacetals released by coffee berries is critical to understanding their chemo-ecological roles in the host discrimination and colonization process of the coffee berry borer, and also for their potential use in the management of this pest. Here, we show that the coffee berry spiroacetals frontalin and 1,6-dioxaspiro [4.5] decane (referred thereafter as brocain), are also used as semiochemicals by the coffee berry borer for host colonization. Bioassays and chemical analyses showed that crowding coffee berry borers from 2 to 6 females per berry, reduced borer fecundity, which appeared to correlate with a decrease in the emission rates of conophthorin and frontalin over time. In contrast, the level of brocain did not vary significantly between borer- uninfested and infested berries. Brocain was attractive at lower doses, but repellent at higher doses while frontalin alone or in a blend was critical for avoidance. Field assays with a commercial attractant comprising a mixture of ethanol and methanol (1∶1), combined with frontalin, confirmed the repellent effect of this compound by disrupting capture rates of H. hampei females by 77% in a coffee plantation. Overall, our results suggest that the levels of frontalin and conophthorin released by coffee berries determine the host colonization behaviour of H. hampei, possibly through a ‘push-pull’ system, whereby frontalin acts as the ‘push’ (repellent) and conophthorin acting as the ‘pull’ (attractant). Furthermore, our results reveal the potential use of frontalin as a repellent for management of this coffee pest.     

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.     

Simplification of a coffee foliage-dwelling beetle community under low-shade management

Coffee agroforests may be structurally and floristically complex and may contain a significant fraction of species from biodiverse and threatened tropical montane forest biotas; hence, understanding the dynamics of tropical forest biodiversity in coffee agroecosystems has emerged as a centrally important area of tropical conservation biology research. We conducted a morphospecies analysis on foliage-dwelling beetles collected from coffee plants on four coffee farms in southern Chiapas, Mexico, to characterize variation in the abundance, species richness, and species composition of this mega-diverse taxon in relation to coffee cultivation system, spatio-temporal variation, and predator removal. We constructed thirty-two cages to exclude birds and bats on four farms, each enclosing 7–10 coffee plants and paired with an adjacent uncaged control plot, and then collected beetles from coffee foliage with D-Vac aspirators in each plot once every 3 months for one year.We classified the 2662 beetles collected into 293 morphospecies, representing 42 families of beetles. Extrapolation and interpolation analyses revealed a very high level of species richness, with no plateau and only a slight leveling trend observed in our species accumulation curves. We found that low-shade systems contain equal or higher beetle abundance, lower species richness, more highly homogenized species composition, and higher abundance of coffee berry borer pests on coffee foliage than do high-shade systems. We observed no effect of flying vertebrate exclusion on the coffee foliage beetle assemblage, but did find significant variation in abundance, species richness, and species composition of coffee foliage beetles across seasons and study sites.The increased beetle biodiversity of high-shade coffee cultivation systems has important implications both for the preservation of native biodiversity in coffee growing regions and for the control of agricultural pests such as the coffee berry borer.     

Abiotic mortality factors of the coffee berry borer (Hypothenemus hampei)

Mortality of the coffee berry borer was studied under controlled laboratory conditions in Tapachula, Mexico. For adult female borers subjected to a range of relative humidities (RH) without food at 25°C, the longest mean survival time (20 days) was obtained at 93.5% RH. Adult borer survival was also studied at a range of temperatures for a fixed relative humidity (93.5% RH); at 20°C mean survival time was 28 days. Fecundity and mortality of borer stages in berries was studied for a range of humidities at 25°C. Maximum fecundity was obtained at 90 and 93.5% RH. Immature stages were ejected from the berry at 84% RH and above, which is interpreted as a form of brood hygiene.     

Penicillium species endophytic in coffee plants and ochratoxin A production

Tissues from Coffea arabica, C. congensis, C. dewevrei and C. liberica collected in Colombia, Hawaii and at a local plant nursery in Maryland were sampled for the presence of fungal endophytes. Surface sterilized tissues including roots, leaves, stems and various berry parts were plated on yeast-malt agar. DNA was extracted from a set of isolates visually recognized as Penicillium, and the internal transcribed spacer region and partial LSU-rDNA was amplified and sequenced. Comparison of DNA sequences with GenBank and unpublished sequences revealed the presence of 11 known Penicillium species: P. brevicompactum, P. brocae, P. cecidicola, P. citrinum, P. coffeae, P. crustosum, P. janthinellum, P. olsonii, P. oxalicum, P. sclerotiorum and P. steckii as well as two possibly undescribed species near P. diversum and P. roseopurpureum. Ochratoxin A was produced by only four isolates, one isolate each of P. brevicompactum, P. crustosum, P. olsonii and P. oxalicum. The role these endophytes play in the biology of the coffee plant remains enigmatic.     

Effects of predatory ants on lower trophic levels across a gradient of coffee management complexity

1. Ants are important predators in agricultural systems, and have complex and often strong effects on lower trophic levels. Agricultural intensification reduces habitat complexity, food web diversity and structure, and affects predator communities. Theory predicts that strong top-down cascades are less likely to occur as habitat and food web complexity decrease. 2. To examine relationships between habitat complexity and predator effects, we excluded ants from coffee plants in coffee agroecosystems varying in vegetation complexity. Specifically, we studied the effects of eliminating ants on arthropod assemblages, herbivory, damage by the coffee berry borer and coffee yields in four sites differing in management intensification. We also sampled ant assemblages in each management type to see whether changes in ant assemblages relate to any observed changes in top-down effects. 3. Removing ants did not change total arthropod densities, herbivory, coffee berry borer damage or coffee yields. Ants did affect densities of some arthropod orders, but did not affect densities of different feeding groups. The effects of ants on lower trophic levels did not change with coffee management intensity. 4. Diversity and activity of ants on experimental plants did not change with coffee intensification, but the ant species composition differed. 5. Although variation in habitat complexity may affect trophic cascades, manipulating predatory ants across a range of coffee agroecosystems varying in management intensity did not result in differing effects on arthropod assemblages, herbivory, coffee berry borer attack or coffee yields. Thus, there is no clear pattern that top-down effects of ants in coffee agroecosystems intensify or dampen with decreased habitat complexity.     

Diversity of filamentous fungi associated with Hypothenemus hampei (Ferrari) (Coleoptera: Scolytidae) and its galleries in berries of Coffea canephora (Pierre)

Field sampling was carried out in Ouro Preto d'Oeste - Rond?nia (10 degrees 45'S and 62 degrees 15'W) to evaluate the mycobiota associated with Hypothenemus hampei Ferrari [cuticle, mouth, prothorax (mycangia), gut and feces] and its galleries on berries of Coffea canephora Pierre. Ten genera (201 isolates) were directly related with the insect while five genera (20 isolates) were related with galleries on berries. All the genera identified in the insects were also present in their galleries, what indicates that boring may be an active way of fungi inoculation by H. hampei. The fungi genera were more diverse in the mouth and prothorax of borers, and lower in feces. Fusarium, Penicillium and Geotrichum, with abundance of 55.7, 24.3 and 10.8%, respectively, were dominant genera. In the galleries Fusarium, Geotrichum, Trichoderma and Aspergillus with abundance of 33.3, 29.6, 18.5 and 14.8%, respectively, were dominant genera. The overall presence of Fusarium in coffee berry borer and its galleries) reinforces previous indications of a close interaction between H. hampei-Fusarium. The presence of Aspergillus and Penicillium emphasizes the possibility of "ochratoxin dispersion" by the borer. This work provides the first record of the mycobiota associated with H. hampei in C. canephora. Among the identified genera, Cephalosporium, Geotrichum and Oidiodendrum were recorded for the first time in association with H. hampei and its galleries in C. canephora.     

Alpha-amylases of the coffee berry borer (Hypothenemus hampei) and their inhibition by two plant amylase inhibitors

The adult coffee berry borer (Hypothenemus hampei Ferrari [Coleoptera: Scolytidae]), a major insect pest of coffee, has two major digestive alpha-amylases that can be separated by isoelectric focusing. The alpha-amylase activity has a broad pH optimum between 4.0 and 7.0. Using pH indicators, the pH of the midgut was determined to be between 4.5 and 5.2. At pH 5.0, the coffee berry borer alpha-amylase activity is inhibited substantially (80%) by relatively low levels of the amylase inhibitor (alphaAI-1) from the common bean, Phaseolus vulgaris L., and much less so by the amylase inhibitor from Amaranthus. We used an in-gel zymogram assay to demonstrate that seed extracts can be screened to find suitable inhibitors of amylases. The prospect of using the genes that encode these inhibitors to make coffee resistant to the coffee berry borer via genetic engineering is discussed.     

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.     

Anolis lizards as biocontrol agents in mainland and island agroecosystems

Our knowledge of ecological interactions that bolster ecosystem function and productivity has broad applications to the management of agricultural systems. Studies suggest that the presence of generalist predators in agricultural landscapes leads to a decrease in the abundance of herbivorous pests, but our understanding of how these interactions vary across taxa and along gradients of management intensity and eco‐geographic space remains incomplete. In this study, we assessed the functional response and biocontrol potential of a highly ubiquitous insectivore (lizards in the genus Anolis) on the world's most important coffee pest, the coffee berry borer (Hypothalemus hampei). We conducted field surveys and laboratory experiments to examine the impact of land‐use intensification on species richness and abundance of anoles and the capacity of anoles to reduce berry borer infestations in mainland and island coffee systems. Our results show that anoles significantly reduce coffee infestation rates in laboratory settings (Mexico, p = .03, F = 5.13 df = 1, 35; Puerto Rico, p = .014, F = 8.82, df = 1, 10) and are capable of consuming coffee berry borers in high abundance. Additionally, diversified agroecosystems bolster anole abundance, while high‐intensity practices, including the reduction of vegetation complexity and the application of agrochemicals were associated with reduced anole abundance. The results of this study provide supporting evidence of the positive impact of generalist predators on the control of crop pests in agricultural landscapes, and the role of diversified agroecosystems in sustaining both functionally diverse communities and crop production in tropical agroecosystems.     

Artificial diet sandwich reveals subsocial behaviour in the coffee berry borer Hypothenemus hampei (Coleoptera: Curculionidae: Scolytinae)

An artificial diet sandwich, consisting of coffee berry borer artificial diet within two glass plates, has been developed to elucidate the behaviour of the coffee berry borer, an insect that in nature spends most of its life cycle inside the coffee berry. Various types of behaviour have been observed for the first time, including gallery construction, oviposition, gallery blocking, mating and most remarkably, subsocial tasks such as maternal sanitation and tending of eggs and larvae. This observational technique is a breakthrough for studies and manipulations of the coffee berry borer's social behaviour and could be applicable to other bark beetles, consequently yielding important insights into the origin of parental care in scolytine beetles.     

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.