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.     

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.     

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.     

Effects of Management Intensity and Season on Arboreal Ant Diversity and Abundance in Coffee Agroecosystems

Agricultural intensification decreases arthropod predator diversity, abundance and population stability, and may affect interactions between top predators and their arthropod prey – ultimately affecting ecosystem services. Coffee management intensification (reduction or removal of shade trees) reduces diversity of arthropod predators (ground-foraging ants). Because ants provide ecosystem services by controlling pests, influences of intensification on arboreal, coffee-foraging ant diversity and abundance are important. We here address how coffee intensification affects: (1) coffee-foraging ant diversity and abundance and (2) seasonal fluctuations in ant abundance. In each of four coffee sites of varying management intensity in Chiapas, Mexico, we sampled vegetation and using two methods, sampled ant diversity and abundance over two years. Sites significantly differed in vegetation and management intensity. Coffee-foraging ant diversity generally decreased with increasing management intensity (16–26% fewer species observed in the most intensively-managed site). Ant abundance was higher in the wet season. Management intensity, however, did not influence ant abundance or seasonal fluctuations in abundance. Our results highlight the importance of diverse agricultural systems in maintaining arthropod predator diversity, and point to one model system in which we may effectively test how diversity per se affects ecosystem services.     

A Keystone Ant Species Provides Robust Biological Control of the Coffee Berry Borer Under Varying Pest Densities

Species’ functional traits are an important part of the ecological complexity that determines the provisioning of ecosystem services. In biological pest control, predator response to pest density variation is a dynamic trait that impacts the provision of this service in agroecosystems. When pest populations fluctuate, farmers relying on biocontrol services need to know how natural enemies respond to these changes. Here we test the effect of variation in coffee berry borer (CBB) density on the biocontrol efficiency of a keystone ant species (Azteca sericeasur) in a coffee agroecosystem. We performed exclosure experiments to measure the infestation rate of CBB released on coffee branches in the presence and absence of ants at four different CBB density levels. We measured infestation rate as the number of CBB bored into fruits after 24 hours, quantified biocontrol efficiency (BCE) as the proportion of infesting CBB removed by ants, and estimated functional response from ant attack rates, measured as the difference in CBB infestation between branches. Infestation rates of CBB on branches with ants were significantly lower (71%-82%) than on those without ants across all density levels. Additionally, biocontrol efficiency was generally high and did not significantly vary across pest density treatments. Furthermore, ant attack rates increased linearly with increasing CBB density, suggesting a Type I functional response. These results demonstrate that ants can provide robust biological control of CBB, despite variation in pest density, and that the response of predators to pest density variation is an important factor in the provision of biocontrol services. Considering how natural enemies respond to changes in pest densities will allow for more accurate biocontrol predictions and better-informed management of this ecosystem service in agroecosystems.     

Vegetation connectivity increases ant activity and potential for ant‐provided biocontrol services in a tropical agroforest

In natural and managed systems, connections between trees are important structural resources for arboreal ant communities with ecosystem‐level effects. However, ongoing agricultural intensification in agroforestry systems, which reduces shade trees and connectivity between trees and crop plants, may hinder ant recruitment rates to resources and pest control services provided by ants. We examined whether increasing connectivity between coffee plants and shade trees in coffee plantations increases ant activity and enhances biological control of the coffee berry borer, the most devastating insect pest of coffee. Further, we examined whether artificial connections buffer against the loss of vegetation connectivity in coffee plants located at larger distances from the nesting tree. We used string to connect Inga micheliana shade trees containing Azteca sericeasur ant nests to coffee plants to compare ant activity before and after placement of the strings, and measured borer removal by ants on coffee plants with and without strings. Ant activity significantly increased after the addition of strings on connected plants, but not on control plants. Borer removal by ants was also three times higher on connected plants after string placement. Greater distance from the nesting tree negatively influenced ant activity on control coffee plants, but not on connected plants, suggesting that connections between coffee plants and nest trees could potentially compensate for the negative effects that larger distances pose on ant activity. Our study shows that favoring connectivity at the local scale, by artificially adding connections, promotes ant activity and may increase pest removal in agroecosystems. Abstract in Spanish is available with online material.     

Relative strengths of top-down and bottom-up forces in a tropical forest community

We tested integrative bottom-up and top-down trophic cascade hypotheses with manipulative experiments in a tropical wet forest, using the ant-plant Piper cenocladum and its associated arthropod community. We examined enhanced nutrients and light along with predator and herbivore exclusions as sources of variation in the relative biomass of plants, their herbivores (via rates of herbivory), and resident predaceous ants. The combined manipulations of secondary consumers, primary consumers, and plant resources allowed us to examine some of the direct and indirect effects on each trophic level and to determine the relative contributions of bottom-up and top-down cascades to the structure of the community. We found that enhanced plant resources (nutrients and light) had direct positive effects on plant biomass. However, we found no evidence of indirect (cascading through the herbivores) effects of plant biomass on predators or top predators. In contrast, ants had indirect effects on plant biomass by decreasing herbivory on the plants. This top-down cascade occurred whether or not plant resources were enriched, conditions which are expected to modify top-down forces. Received: 9 August 1998 / Accepted: 1 December 1998     

Assembly rules for functional groups of North American shrews: effects of geographic range and habitat partitioning

Trophic cascades exist in numerous terrestrial systems, including many systems with ants as the top predator. Many studies show how behavioral modifications of herbivores are especially important in mediating species interactions and trophic cascades. Although most studies of trophic cascades focus on predator-herbivore-plant links, the trophic cascades concept could be applied to almost any level of trophic interactions. Especially considering the importance of parasites we consider here the interactions between the parasitic phorid fly, Pseudacteon sp. (Diptera: Phoridae), its ant host, Azteca instabilis (F. Smith) (Hymenoptera: Formicidae), and the herbivore, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) in the coffee agroecosystem. We investigated the effects of phorid flies on ant behavior by monitoring ant recruitment to tuna baits over a 30-min period in the presence or absence of phorid flies. To study the indirect effects of phorids on larvae, we placed baits on coffee plants to elevate ant foraging levels to levels near to ant nests, placed larvae near baits, and recorded the effects of ants on larvae either in the presence or absence of phorid flies. We found that phorid fly presence significantly reduced ant ability to recruit to baits through behavioral modifications and also significantly lessened ant ability to attack, carry away, or force herbivores off plants. We conclude there is a behaviorally-modified species-level trophic cascade in the coffee agroecosystem, with potentially important effects in ant and herbivore communities as well as for coffee production.     

Diversity cascades in alfalfa fields: from plant quality to agroecosystem diversity

To examine top-down and bottom-up influences on managed terrestrial communities, we manipulated plant resources and arthropod abundance in alfalfa (Medicago sativa L.) fields. We modified arthropod communities using three nonfactorial manipulations: pitfall traps to remove selected arthropods, wooden crates to create habitat heterogeneity, and an arthropod removal treatment using a reversible leaf blower. These manipulations were crossed with fertilizer additions, which were applied to half of the plots. We found strong effects of fertilizer on plant quality and biomass, and these effects cascaded up to increase herbivore abundance and diversity. The predator community also exhibited a consistent positive effect on the maintenance of herbivore species richness and abundance. These top-down changes in arthropods did not cascade down to affect plant biomass; however, plant quality (saponin content) increased with higher herbivore densities. These results corroborate previous studies in alfalfa that show complex indirect effects, such as trophic cascades, can operate in agricultural systems, but the specifics of the interactions depend on the assemblages of arthropods involved.     

Wood-nesting ants and their parasites in forests and coffee agroecosystems

Agricultural intensification is linked to reduced species richness and may limit the effectiveness of predators in agricultural systems. We studied the abundance, diversity, and species composition of wood-nesting ants and frequency of parasitism of poneromorph ants in coffee agroeco systems and a forest fragment in Chiapas, Mexico. In three farms differing in shade management and in a nearby forest fragment, we surveyed ants nesting in rotten wood. We collected pupae of all poneromorph ants encountered, and incubated pupae for 15 d to recover emerging ant parasites. If no parasites emerged, we dissected pupae to examine for parasitism. Overall, we found 63 ant morphospecies, 29 genera, and 7 subfamilies from 520 colonies. There were no significant differences in ant richness or abundance between the different sites. However, there were significant differences in the species composition of ants sampled in the four different sites. The parasitism rates of ants differed according to site; in the forest 77.7% of species were parasitized, and this number declined with increasing intensification in traditional polyculture (40%),commercial polyculture (25%), and shade monoculture (16.6%). For three of four poneromorph species found in >1 habitat, parasitism rates were higher in the more vegetatively complex sites. The result that both ant species composition and ant parasitism differed among by site indicates that coffee management intensification affects wood-nesting ant communities. Further, coffee intensification may significantly alter interactions between ants and their parasites, with possible implications for biological control in coffee agroecosystems.     

Interaction complexity matters: disentangling services and disservices of ant communities driving yield in tropical agroecosystems

Owing to complex direct and indirect effects, impacts of higher trophic levels on plants is poorly understood. In tropical agroecosystems, ants interact with crop mutualists and antagonists, but little is known about how this integrates into the final ecosystem service, crop yield. We combined ant exclusion and introduction of invasive and native-dominant species in cacao agroecosystems to test whether (i) ant exclusion reduces yield, (ii) dominant species maximize certain intermediate ecosystem services (e.g. control of specific pests) rather than yield, which depends on several, cascading intermediate services and (iii) even, species-rich ant communities result in highest yields. Ants provided services, including reduced leaf herbivory and fruit pest damage and indirect pollination facilitation, but also disservices, such as increased mealybug density, phytopathogen dissemination and indirect pest damage enhancement. Yields were highest with unmanipulated, species-rich, even communities, whereas ant exclusion decreased yield by 27%. Introduction of an invasive-dominant ant decreased species density and evenness and resulted in 34% lower yields, whereas introduction of a non-invasive-dominant species resulted in similar species density and yields as in the unmanipulated control. Species traits and ant community structure affect services and disservices for agriculture in surprisingly complex ways, with species-rich and even communities promoting highest yield.     

Local and landscape drivers of biodiversity of four groups of ants in coffee landscapes

Agriculture of varying management intensity dominates fragmented tropical areas and differentially impacts organisms across and within taxa. We examined impacts of local and landscape characteristics on four groups of ants in an agricultural landscape in Chiapas, Mexico comprised of forest fragments and coffee agroecosystems varying in habitat quality. We sampled ground ants found in leaf litter and rotten logs and arboreal ants found in hollow coffee twigs and on tree trunks. Then using vegetation and agrochemical indices and conditional inference trees, we examined the relative importance of local (e.g. vegetation, elevation, agrochemical) and landscape variables (e.g. distance to and amount of nearby forest and rustic coffee) for predicting richness and abundance of ants. Leaf litter ant abundance increased with vegetation complexity; richness and abundance of ants from rotten logs, twig-nests, and tree trunks were not affected by vegetation complexity. Agrochemical use did not affect species richness or abundance of any ant group. Several local factors (including humus mass, degree of decay of logs, number of hollow twigs, tree circumference, and absence of fertilizers) were significant positive predictors of abundance and richness of some ant groups. Two landscape factors (forest within 200 m, and distance from forest) predicted richness and abundance of twig-nesting and leaf litter ants. Thus, different ant groups were influenced by different characteristics of agricultural landscapes, but all responded primarily to local characteristics. Given that ants provide ecosystem services (e.g. pest control) in coffee farms, understanding ant responses to local and landscape characteristics will likely inform farm management decisions.     

Limitation of nesting resources for ants in Colombian forests and coffee plantations

Abstract.  1. This study examines limitation of nesting resources for leaf-litter and twig-nesting ants as a mechanism of diversity loss across an intensification gradient of coffee production in Colombia. Twelve farms were selected and classified into four management types: forest, polygeneric shade coffee, monogeneric shade coffee, and sun coffee (unshaded coffee monocultures).
2. At each of the farms, four treatment subplots were established at the corners of each of 10 25 m² plots: (i) twig augmentation (adding 10 empty bamboo twigs); (ii) litter augmentation (tripling existing litter profile); (iii) twig and litter augmentation; and (iv) no manipulation control, for a total of 480 subplots. A twig addition experiment was also performed on coffee bushes.
3. The results showed significantly more ant colonies in the forest and monogeneric shade coffee litter augmentation plots after 4 months. Litter-nesting ant species richness was higher in all three shade systems than in the sun coffee. The identities of ants nesting on coffee bushes were different from those in the soil level litter. Fewer species nested in bamboo twigs placed in litter in the most intensive systems.
4. More ants nested in the resource addition treatments, and more ant species were found in forested habitats; however, a single mechanism cannot explain the observed patterns. It was concluded that a combination of bottom-up and top-down effects might lead to the loss of associated fauna with the intensification of these agroecosystems.     

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.     

Behavioral diversity of predatory arboreal ants in coffee agroecosystems

Aspects of predator assemblages that alter predator effects on prey have received extensive recent attention. Among other mechanisms, differences in behavior or resource use within predator trophic levels may enhance predator effects on prey, especially if effects of each predator species differ with environmental conditions. We address whether three common ant species (Azteca instabilis F. Smith, Camponotus textor Forel, and Crematogaster spp.) are functionally unique in coffee agroecosystems, asking if each species differs in (1) cooperative foraging behavior, (2) responses to experimentally introduced herbivores, and (3) responses to pest outbreaks. Furthermore, we examined the behaviors and effects of each ant species under different conditions by varying herbivore species, herbivore size, and herbivore density and carrying out observations in different seasons. Ant species significantly differed in foraging behaviors, in effects on individual herbivores, and in responses to pest outbreaks in terms of both type and time of response to herbivores. The behaviors and effects of each ant species differed in the dry and wet seasons and for different herbivore species and sizes. Although A. instabilis generally removed more larvae and more quickly removed larvae, this was not the case under all conditions. The data presented thus support that common ant species in coffee agroecosystems are behaviorally diverse in their responses to herbivores under different conditions. We discuss the implications of these differences in ant behaviors for enhancement of predatory function in light of both multipredator effects and in terms of the potential importance of predator diversity.     

Arboreal Ant Abundance and Leaf Miner Damage in Coffee Agroecosystems in Mexico

Shaded coffee agroecosystems traditionally have few pest problems potentially due to higher abundance and diversity of predators of herbivores. However, with coffee intensification (e.g., shade tree removal or pruning), some pest problems increase. For example, coffee leaf miner outbreaks have been linked to more intensive management and increased use of agrochemicals. Parasitic wasps control the coffee leaf miner, but few studies have examined the role of predators, such as ants, that are abundant and diverse in coffee plantations. Here, we examine linkages between arboreal ant communities and coffee leaf miner incidence in a coffee plantation in Mexico. We examined relationships between incidence and severity of leaf miner attack and: (1) variation in canopy cover, tree density, tree diversity, and relative abundance of Inga spp. shade trees; (2) presence of Azteca instabilis, an arboreal canopy dominant ant; and (3) the number of arboreal twig‐nesting ant species and nests in coffee plants. Differences in vegetation characteristics in study plots did not correlate with leaf miner damage perhaps because environmental factors act on pest populations at a larger spatial scale. Further, presence of A. instabilis did not influence presence or severity of leaf miner damage. The proportion of leaves with leaf miner damage was significantly lower where abundance of twig‐nesting ants was higher but not where twig‐nesting ant richness was higher. These results indicate that abundance of twig‐nesting ants in shaded coffee plantations may contribute to maintenance of low leaf miner populations and that ants provide important ecosystem services in coffee agroecosystems.     

Testing ant predation on the coffee berry borer in shaded and sun coffee plantations in Colombia

Soil‐dwelling ants, many of which are generalist predators, are more diverse in shaded than in sun coffee plantations without trees. We compared ant predation on the coffee berry borer, Hypothenemus hampei (Ferrari) (Coleoptera: Curculionidae: Scolytinae) in three shaded and three sun coffee plantations in Apía, Colombia, in both the wet and the dry seasons. We found that H. hampei adults exposed to ants for 5 days suffered higher removal in shaded plantations and in the wet season. In the laboratory, we observed that ants killed 74–99% of H. hampei adults over the course of 5 days. Ants appear to be important predators of H. hampei, particularly in shaded coffee plantations and in the wet season.     

How does habitat complexity affect ant foraging success? A test using functional measures on three continents

Habitat complexity can mediate key processes that structure local assemblages through effects on factors such as competition, predation and foraging behaviour. While most studies address assemblage responses to habitat complexity within one locality, a more global approach allows conclusions with greater independence from the phylogenetic constraints of the target assemblages, thus allowing greater generality. We tested the effects of natural and manipulated habitat complexities on ant assemblages from South Africa, Australia and Sweden, in order to determine if there were globally consistent responses in how functional measures of foraging success are regulated by habitat complexity. Specifically, we considered how habitat complexity affected ant foraging rates including the speed of discovery and rate of monopolisation. We also tested if habitat complexity affected the body size index, a size-related morphological trait, of ants discovering resources and occupying and monopolising the resources after 180 min. Ants were significantly slower to discover baits in the more complex treatments, consistent with predictions that they would move more slowly through more complex environments. The monopolisation index was also lower in the more complex treatments, suggesting that resources were more difficult to defend. Our index of ant body size showed trends in the predicted direction for complexity treatments. In addition, ants discovering, occupying and monopolising resources were smaller in simple than in complex natural habitats. Responses of discovering ants to resources in natural habitats were clear in only one of three regions. Consistent with our predictions, habitat complexity thus affected functional measures of the foraging success of ants in terms of measures of discovery and monopolisation rates and body size traits of successful ants. However, patterns were not always equally clear in manipulative and mensurative components of the study.     

Land cover diversity increases predator aggregation and consumption of prey

A lower diversity of land cover types is purported to decrease arthropod diversity in agroecosystems and is dependent on patterns of land use and fragmentation. Ants, important providers of ecosystem services such as biological control, are susceptible to landscape‐level changes. We determined the relationships between land cover diversity and fragmentation on the within‐field spatial associations of ants to pests and resulting predation events by combining mapping and molecular tools. Increased land cover diversity and decreased fragmentation increased ant abundance, spatial association to pests and predation. Land cover diversity and fragmentation were more explanatory than land cover types. Even so, specific land cover types, such as deciduous forest, influenced ant and pest diversity more so than abundance. These results indicate that geospatial techniques and molecular gut content analysis can be combined to determine the role of land use in influencing predator–prey interactions and resulting predation events in agroecosystems.     

Dominant meat ants affect only their specialist predator in an epigaeic arthropod community

Ants are thought to exert an important influence on the structure of arthropod assemblages through predation and competition. I examined the effect of a dominant ant, Iridomyrmex purpureus, on epigaeic arthropod assemblages on rock outcrops using an exclusion experiment. I compared arthropod assemblages on four replicate outcrops allocated to each of the following treatments: I. purpureus present; I. purpureus absent; I. purpureus excluded; and procedural control. Nests of I. purpureus were caged in summer 2001 and epigaeic arthropod assemblages were sampled at all sites using pitfall traps in autumn and spring 2001 and summer 2002. I also collected items from foraging workers to determine the diet of I. purpureus. Exclusion cages successfully reduced the abundance of I. purpureus workers in pitfall traps by more than 97%. Exclusion of I. purpureus did not affect the size distribution, biomass or abundance of arthropod predators or non-predatory arthropods, although the total biomass of ants was greater at sites with I. purpureus. Spider biomass, species richness, abundance and composition were also not affected by the presence of I. purpureus, although the I. purpureus mimic and specialist predator, Habronestes bradleyi, became less abundant at sites from which I. purpureus was excluded. Predation by I. purpureus on other arthropods may not have a significant effect on epigaeic arthropod communities, but the complex role of I. purpureus in this ecosystem and the high diversity of species belonging to multiple trophic levels may obscure its effects in this system.