Ecological Entomology (2014), DOI: 10.1111/een.12139 Manipulating tropical fire ants to reduce the coffee berry borer WARING TRIBLE1 and R O N C A R R O L L 2 1The Rockefeller University, New York , New York, U.S.A. and 2Odum School of Ecology, University of Georgia, Athens, Georgia, U.S.A. Abstract. 1. The coffee berry borer Hypothenemus hampei (Coleoptera, Curculion- idae) (Ferrari) is the most important pest of coffee production worldwide. 2. The hypothesis that the tropical !re 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 signi!cantly 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. Key words. Biological control, coffee berry borer, !re ant, Formicidae, Hypothenemus hampei, Solenopsis. Introduction coffee berries in the soil, and soil-dwelling ants may thus play an important role in reducing dry season coffee berry borer Coffee is the second most important commodity in the world by populations and minimising future outbreaks (Armbrecht & value, and the coffee berry borer is a beetle that constitutes the Gallego, 2007; Jaramillo et al.,2007;Chapmanet al.,2009; most important pest in coffee production worldwide (Damon, Vélez et al., 2006). No regimes have been devised to augment 2000). It is estimated that the coffee berry borer causes approxi- this ant-based predation, however, and one recent review sug- mately $500 million worth of damage yearly (Chapman et al., gested that manipulating ant populations to increase predation 2009). Traditional control of the coffee berry borer requires of the coffee berry borer would be extremely dif!cult (Vega extensive application of pesticides, which makes biological con- et al., 2009). trol, controlling pests with predators, parasites, and pathogens, Nevertheless, a few ant species are considered important amuchsought-afteralternative(Vegaet al., 2009). predators of the coffee berry borer (Armbrecht et al.,2005; Biological control of the coffee berry borer has been Armbrecht & Gallego, 2007). The tropical !re ant, Solenopsis attempted using a number of organisms: parasitoid wasps, geminata Westwood, preys on free-living coffee berry borer entomopathogens, and ants (Vega et al.,2009).Antscanenter beetles, but is not known to penetrate coffee berries and prey on the coffee berry and attack embedded beetles, and may therefore embedded beetles (Varón et al., 2004). Solenopsis geminata is serve an important role in reducing the dry-season population a highly dominant ant species from Mexico to Brazil, however, of coffee berry borer beetles (Larsen & Philpott, 2010). In the and it is also possible that S. geminata indirectly protects the dry season, coffee berry borer beetles survive in coffee berries coffee berry borer by suppressing other ant species that may remaining on the bush and on the ground. Many farmers remove exert more ef!cient predation pressure. Indeed, some studies all coffee berries from the bushes at the end of the season to have shown that S. geminata prevalence is inversely correlated reduce this resource for berry borers, but it is dif!cult to locate with ant diversity, and that S. geminata removal can lead to an increase in many arthropod species, including other ants (Risch Correspondence: Waring Trible, 1230 York Avenue, New York, NY &Carroll,1982;Perfecto,1991;Philpottet al.,2006a,butsee 10065, U.S.A. E-mail: [email protected] Perfecto, 1994). © 2014 The Royal Entomological Society 1 2 Waring Trible and Ron Carroll We hypothesised that a greater number of coffee berry borer Fig. 1. Plots were arranged such that each contained one or two beetles would disappear (be preyed upon) from coffee plots S. geminata mounds with a diameter between 20 and 50 cm in without S. geminata than from plots with S. geminata. This the 1.5-m-wide outer plot area only (see Fig. 1). species is particularly relevant because S. geminata is one of Control plots were baited in the morning, then coffee berries afewantsthatattainsahighpopulationdensityinboth‘sun’ containing coffee berry borer beetles were placed in the 2 × 2m and ‘shade’ coffee plantations because of its large geographical inner area of the plots in the afternoon. All experimental plots range (Perfecto and Snelling, 1995; Philpott et al.,2006a; were baited in the morning, and then an organophosphate Varón et al., 2007). If S. geminata removal represents a viable pesticide (Lorsbon-15G, active component 15% Chlopyrifos) control strategy for the coffee berry borer, the procedure may was applied directly to the S. geminata mounds in the outer be applicable throughout much of Central and South America plot areas in the afternoon. This was repeated on the following across a wide variety of coffee management types. day, then on the third day experimental plots were baited in the We tested the hypothesis that S. geminata indirectly protects morning and coffee berries were placed in 2 × 2m innerplot coffee berry borer beetles on two coffee farms in Costa Rica areas in the afternoon. These three sequential baitings were used by monitoring ant populations using tuna !sh baits in 12 plots in experimental plots to verify S. geminata removal. and selectively removing S. geminata with an organophosphate Plots were designed to prevent spillover effects: in experi- pesticide in six randomly assigned experimental plots, then mental plots, pesticide was applied only to S. geminata mounds measuring the disappearance of coffee berry borer beetles from located only in the outer plot area, whereas coffee berries con- coffee berries in experimental and control plots over a 72-h taining coffee berry borer beetles were placed only in the inner period. plot area. Coffee berries were not placed in plots until 24 h after !nal pesticide treatment and were placed in small aluminum dishes to prevent direct contact with the ground. Two treatments Materials and methods of pesticide were used to allow small amounts of pesticide to be applied to the !re ant mounds at each application, which may Farm selection have resulted in less potential for pesticide to leach into the inner plot area. During the rainy season (July to August) 2011, we performed S. geminata removal experiments on two shade coffee farms in Costa Rica. Finca Leon y Parra, ‘Farm 1,’ is located in Baiting regime and activity index Monteverde (cloudforest) at 1100 m above the mean sea level (msl) and Aquiares,‘Farm2,’islocatednearTurrialbaat Plots were systematically baited using tuna !sh baits, accord- 1000 m above msl. The experiment was conducted during the ing to the methods of Perfecto (1994). Tuna !sh baits were rainy season because previous studies have shown that beetle placed every 1 m in the outer plot area and every 50 cm in the predation by ants is highest during this period (Gallego Ropero inner plot area, resulting in 57 baits per plot, as in Fig. 1. Each &Armbrecht,2005;Armbrecht&Gallego,2007).Bothcoffee bait consisted of ∼1.3 g of tuna placed in the centre of a small farms had moderate shade cover (as in Philpott et al.,2006b) Petri dish and left in the !eld for 20 min. Petri dishes were with a small number of shade tree species at low density and used for the baits so that tuna could be removed after baiting active pesticide regimes. However, the two farms differed based to prevent any lasting effect of tuna placement on the plot. After on temperature and the ant species assemblages observed and 20 min, the baits were collected and ant activity was recorded, were thus chosen to test the hypothesis in two ecologically using an ‘activity index’ as in Perfecto, 1994. distinct agroecosystems. Species presence on the bait was recorded and rated as I, II, or III, where I represents 1–10 ants, II represents 11–20, and III represents >20, according to the methods of Perfecto, Plot design 1994. Where multiple species were observed on a single bait, the presence of each species was rated individually. These On each farm, six 5 5mplotsweredesignatedandrandomly × activity index values were summed for each plot and compared assigned to ‘with S. geminata’(control)and‘withoutS. gemi- using the Mann–Whitney U-test. All baiting occurred before nata’ (experimental) treatments. One control plot in Farm 1 was 13.00 hours. Ants observed on the baits were grouped into discarded owing to an unusually low initial activity of S. gem- morphospecies using a 10× hand lens in the !eld. Species inata (see Discussion), resulting in a total of 11 plots used for represented on only a single bait were not included in this analysis in this study. analysis. Multiple vouchers of all other species were collected, The plots selected on both farms contained 12–15 coffee and species or genus identities were con!rmed with the aid of bushes, in three rows spaced approximately 2 m apart with !ve taxonomists at Costa Rica’s Instituto Nacional de Biodiversidad bushes per row, spaced approximately 1m apart. Plots were and Universidad de Costa Rica. chosen so as to standardise S. geminata occurrence and activity. Coffee berry placement and determination of change in beetle Pesticide application and berry placement abundance Each 5 × 5m plotcontaineda 2× 2m ‘innerplotarea’sur- For each plot, 60 immature (green) coffee berries with visible rounded by a 1.5-m-wide border (‘outer plot area’) as shown in coffee berry borer damage were collected [berries used were as © 2014 The Royal Entomological Society, Ecological Entomology,doi:10.1111/een.12139 Coffee berry borer biological control 3 Fig.