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The effect of an ant-hemipteran mutualism on the coffee berry borer (Hypothenemus hampei) in southern Mexico
Agriculture, Ecosystems and Environment 117 (2006) 218–221 www.elsevier.com/locate/agee
Short communication
The effect of an ant-hemipteran mutualism on the coffee berry borer (Hypothenemus hampei) in southern Mexico Ivette Perfecto a,*, John Vandermeer a,b a
School of Natural Resources and the Environment, 440 Church, Dana Building, University of Michigan, Ann Arbor, MI 48109, USA b Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USA Received 5 August 2005; received in revised form 6 April 2006; accepted 11 April 2006 Available online 5 June 2006
Abstract The indirect effect of an ant-hemipteran mutualism was investigated in the coffee agroecosystem of Southern Mexico. The ant, Azteca instabilis, forms a mutualistic relationship with the coccid, Coccus viridis, on coffee plants. Through field surveys and experimental studies, the indirect effect of this mutualism on the main coffee pest in the region, Hypothenemus hampei, the coffee berry borer (CBB), was investigated. Results indicate a significant negative relationship between the number of coccids on a plant and the proportion of berries with damage by the CBB. Results also indicate that the effect of the ants is significant on per plant basis but not on per branch basis. Finally, a significant negative linear relationship was found between ant activity and the time it took ants to remove artificially placed borers on coffee berries. This study indicates that the mutualistic relationship between Azteca ants and the coccids has a positive indirect effect on the plant by reducing the numbers of the main insect pest of coffee. # 2006 Elsevier B.V. All rights reserved. Keywords: Integrated pest management; Coffee; Natural enemies; Pest control; Shade trees; Mutualism; Ants
1. Introduction The main pest of coffee in Latin America is the coffee berry borer (CBB), Hypothenemus hampei (Ferrari) (Coleoptera: Scolytidae) a small beetle that bores into the coffee beans as they are maturing (Baker, 1999; Damon, 2000). Effects of the borer are variable but can reach epidemic proportions and cause significant economic damage (Baker, 1999). Biological control potential has been reported for parasitic wasps (Barrera et al., 1990; Damon and Valle, 2002), entomopathogens (Samuels et al., 2002; Mendez-Lopez et al., 2003; Neves and Hirose, 2005) and ants (Armbrecht, 2003; Armbrecht and Perfecto, 2003; Ve´lez et al., 2003; Gallego and Armbrecht, in press). This study examines a complicated interaction involving a mutualism between the ant Azteca instabilis (F. Smith) * Corresponding author. Tel.: +1 734 764 1433; fax: +1 734 936 2195. E-mail address: [email protected] (I. Perfecto). 0167-8809/$ – see front matter # 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.agee.2006.04.007
and the green scale Coccus viridis (Green), in which the ant acts as a predator on the CBB, significantly reducing its impact as a pest. It has previously been demonstrated that the tending of various hemipterans (mainly aphids, coccids, mealybugs and treehoppers) by ants frequently has a net benefit on the host plant (Buckley, 1987; Dansa and Rocha, 1992; Oliveira and Del-Claro, 2005). In the case of A. instabilis and its mutualist C. viridis, the potential for an indirect positive effect using artificially placed larvae of Pieris rapae (L.) has been reported earlier (Vandermeer et al., 2002). While the ants tend coccids in large clumps concentrated on individual branches, they also patrol the rest of the plant and, in the case of an herbivore that requires some time to inflict damage, the ants are potential predators of that pest. This study uses field surveys and experimental manipulations, to investigate whether the ant A. instabilis also acts as a predator on the coffee berry borer.
I. Perfecto, J. Vandermeer / Agriculture, Ecosystems and Environment 117 (2006) 218–221
2. Methods 2.1. Field survey All A. instabilis nests were located in a 45 ha plot on Finca Irlanda, an organic shaded coffee farm located in southern Chiapas, Mexico (158100 North and 928200 West). The plot contains 10,647 shade trees (>10 cm dbh) in about 100 species, most of which seem perfectly suitable for nesting for this species of ant (nests have been found in 35 of the tree species, about what would be expected with a random allocation). Located near each of five nests that were isolated from other nests, six coffee trees were assessed for total number of coccids (C. viridis) (see below). The five nests were taken from widely separated areas within the 45 ha plot. Independent observers then assessed the same coffee trees, for total number of coffee berries and CBB damage. The proportion of damaged fruits per coffee plant was estimated as the number of coffee berries that had CBB (as evidenced from the entrance hole), over the total number of berries. The procedure was repeated in three areas that were isolated from any A. instabilis nests, again sampling areas widely separated from one another in the 45 ha plot. In the end, a total of 34 coffee plants were surveyed for total number of C. viridis, coffee berries and coffee berries damaged by the CBB. An additional survey was conducted on six coffee plants (haphazardly chosen to represent a range of densities for C. viridis) in which the total number of coccids on each branch was directly counted, and subsequently the rate of borer attack determined for the same branches. 2.2. Coccid sampling and estimations The following procedures were adapted, based on a preliminary study of 21 coffee plants for which the actual number of coccids were first determined in absolute terms and then compared with relative estimates obtained in several ways. On a given coffee plant a quick survey was undertaken to determine whether there were any obvious concentrations of coccids or ant activities. Based on this quick survey the plant was placed into one of three categories – a 5-min category, a four-class category, or a full count category. For those plants in the 5-min category the entire plant was scanned systematically from top to bottom during a 5 min period. All coccids (larger than 2 mm in length) on leaves, stems, and berries, were counted concentrating on berries and terminal shoots where the coccids tended to concentrate. The count of total number of coccids greater than 2 mm encountered in a 5 min period is the base number. The estimated actual number was computed as, estimated number = 2.55 base number. If, during the course of counting, more than six individual coccids were encountered on any given branch, the plant was transferred to the fourclass category. For those plants in the four-class category,
219
coccids were counted on each branch to determine which class the branch falls into: 0–6 individuals = low; 7–30 individuals = medium; 30–70 individuals = high; 70 and above = super high category. There was no need to actually count coccids unless the actual number was near the border between the categories. Normally a minute or so of counting made it evident to which class the branch belonged. To make an estimate of the final number estimate, all low branches were multiplied by 0; medium branches by 15; high branches by 46; and super extra branches by 150. Scaling numbers were determined from the initial study of 21 plants. The full count category included those plants that had no berries and fewer than 25 branches. All leaves and stems were examined and all coccids greater than 2 mm were counted. Estimating scales with this procedure and comparing the estimate to the known numbers from the preliminary study of 21 trees provides 93% efficiency in estimation (r2 = 0.926). 2.3. Experimental methods A coffee plant with actively foraging A. instabilis individuals was located near to each of the five ant nests mentioned above. A total of nine branches were chosen so as to represent a range of ant activity from high to low. On each of the branches, ant activity was assessed by watching a single point for a 5 min period and counting the number of ants passing that point, or, if ant activity was especially high, for a single minute. Then, one by one, individual borers were placed on a berry on each of the branches and the time to removal by an ant was recorded. Since it takes a borer a little more than an hour to completely burrow into a coffee berry (personal observations), the beetles were watched for a maximum of 70 min, if they persisted that long.
3. Results The relationship between number of coccids and percentage of coffee berries attacked by the CBB was assessed with a simple regression, which was significant ( p = 0.014, r2 = 0.18) for a linear regression of proportion of fruits with borers versus log of number of C. viridis (Fig. 1). Thus the total number of coccids on a coffee plant was inversely related to the proportion of berries attacked by the CBB. Assessment on a branch-by-branch basis revealed a far weaker relationship, which, while suggestive, was not significant statistically. It appears to be protection of the coffee plant as a whole that is affected by the presence of the ant, and not strictly localized to particular branches with a high concentration of coccids, although some degree of such localization is suggested. The results of the experimental manipulations indicated that there was a negative relationship between ant activity and the time of removal of CBB by ants (Fig. 2), with a significant regression of the log of time to removal versus the
220
I. Perfecto, J. Vandermeer / Agriculture, Ecosystems and Environment 117 (2006) 218–221
log of ant activity ( p < 0.01; r2 = 0.68). If 1 h is taken as approximately the critical time necessary for a borer to become invulnerable to A. instabilis, the simple linear regression of Fig. 2 suggests that the critical ant activity is about 45 ants per minute crossing a given point, which is significantly lower than the maximum ant activity observed in this experiment (114/min). As in previous experiments with P. rapae, even occasional patrolling by ants can thus effect control, although the results with the coffee berry borer are not as evident as with P. rapae (Vandermeer et al., 2002). Furthermore, it is worth noting that in 44% of the cases, the beetle was taken away in the mandibles of an ant, suggesting predation. Unlike the case of P. rapae in which most of the time the caterpillar simply fell off of the branch and escaped predation, the ants frequently carried the borers away, likely using them as a food source (Vandermeer et al., 2002).
4. Discussion
Fig. 1. Relationship between proportion of coffee berries with coffee berry borers and the log of the number of scale insects per coffee plant. Regression equation is above box and explains about 18% of the variance.
Fig. 2. Relationship between log of time to removal of coffee berry borer by ants and the log of the ant activity. Dashed lines indicate approximate position of critical ant activity that will attack an ant before the critical 1 h period (see text).
The results suggest that the mutualistic relationship between A. instabilis and C. viridis affords indirect benefits to the coffee plant through a reduction of the coffee berry borer. Thus, in practical terms, the damage done by the mutualistic herbivore (the coccid) must be judged relative to the protection against the coffee berry borer. This type of indirect interaction has been noted before for other associations in natural systems (Buckley, 1987; Dansa and Rocha, 1992; Fagundes et al., 2005; Oliveira and DelClaro, 2005) but is not well studied in agroecosystems where the net outcome of the interaction can have important economic implications. The only other documented case for an agroecosystem is that of the ant Dolichoderus thoracicus (Smith), its associated mealybugs and several economically important herbivores of cocoa in Malaysia (Khoo and Chung, 1989). In the case of D. thoracicus, the benefit of the ant as predator of cocoa pests is so much higher than the negative effect of the mealybugs that the farmers actively introduce ants with mealybugs to their cocoa plantations as a way of pest control (Perfecto and Castin˜eiras, 1998). The costs and benefits of the A. instabilis complex in coffee have not been studied sufficiently to determine whether the net outcome is likely to be positive for coffee production. Multispecies mutualistic systems can have a wide range of outcomes (Bronstein and Barbosa, 2002), however, the negative impact on CBB of the mutualism suggest that the ant-hemipteran mutualism can have an overall positive effect on coffee production. In the case of the Azteca-coccid–CBB complex, the ant colonies – and therefore also the CBB control – are patchily distributed (Vandermeer and Perfecto, 2006). These patches constitute a very small proportion of the plantation (about 4% of the shade trees in the case of Finca Irlanda). However, since the ant acts as a predator, that 4% represents a sink for
I. Perfecto, J. Vandermeer / Agriculture, Ecosystems and Environment 117 (2006) 218–221
the CBB population. Removal of 4% of the CBB population may have only a small effect on the overall population dynamics, but it does represent one more tool in the toolbox of potential biological control of the most important coffee pest in Latin America, the coffee berry borer. This local level dynamics leads to further speculation about what the dynamics might be on a more regional level. In a landscape dominated by shade coffee rather than unshaded coffee, the additional 4% control could have a major effect, depending on how close the CBB population is to being a stable one. In the current context, it appears that isolated shade plantations in an area of predominantly unshaded coffee may provide sinks that help control the borer over a broad region.
Acknowledgments We wish to thank the Peters family, the owners of Finca Irlanda, for allowing us to conduct this study on their farm. G. Lopez-Batista and B. Estevan Chilel, helped with data collection and the establishment of the 45 ha plot. Guillermo Ibarra and Alvaro Ballinas provided logistical support. The study was supported by NSF grant DEB-0349388.
References Armbrecht, I., 2003. Leaf litter ant diversity and function in coffee under different management systems. Ph.D. Dissertation. University of Michigan, Ann Arbor, MI, USA. Armbrecht, I., Perfecto, I., 2003. Litter-twig dwelling ant species richness and predation potential within a forest fragment and neighboring coffee plantations of contrasting habitat quality in Mexico. Agric. Ecosyst. Environ. 97, 107–115. Baker, P.S., 1999. The coffee berry borer in Colombia. Final Report of the DFID-Cenicafe´-CABI Bioscience IPM for coffee project. 143 pp. Barrera, J.F., Baker, P.S., Valenzuela, J.E., Schwarz, A., 1990. Introduction of two African parasitoid species to Mexico for biological control of the coffee borer Hypothenemus hampei (Ferrari) (Coleoptera: Scolytidae). Folia Entomol. Mex. 79, 245–247. Bronstein, J.L., Barbosa, P., 2002. Multitrophic/multispecies mutualistic interactions: the role of non-mutualists in shaping and mediating mutualisms. In: Tscharntke, T., Hawkins, B.A. (Eds.), Multitrophic Level Interactions. Cambridge University Press, Cambridge, pp. 44–66.
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Buckley, R.C., 1987. Interactions involving plants, Homoptera, and ants. Ann. Rev. Ecol. Syst. 18, 111–135. Damon, A., 2000. A review of the biology and control of the coffee berry borer. Hypothenemus hampei (Coleoptera: Scolytidae). Bull. Entomol. Res. 90, 453–465. Damon, A., Valle, J., 2002. Comparison of two release techniques for the use of Cephalonomia stephanoderis (Hymenoptera: Bethylidae), to control the coffee berry borer Hypothenemus hampei (Coleoptera: Scolytidae) in Soconusco, southeastern Mexico. Biol. Control 24, 117–127. Dansa, C.V.A., Rocha, C.F.D., 1992. An ant-membracid plant interaction in a cerrado area of Brazil. J. Trop. Ecol. 8, 339–348. Fagundes, M., Neves, F.S., Fernandez, G.W., 2005. Direct and indirect interactions involving ants, insect herbivores, parasitoids and the host plant Baccharis dracunculifolia (Asteracea). Ecol. Entomol. 30, 28–35. Gallego, M.C., Armbrecht, I. Depredacio´n por hormigas sobre la broca del cafe´ en cafetales cultivados bajo dos niveles de sombra en Colombia. Revista Manejo Integrado de Plagas, Costa Rica, in press. Khoo, K.C., Chung, G.F., 1989. Use of the black cocoa ant to control mirid damage in cocoa. Plant. Kuala Lampur 65, 370–383. Mendez-Lopez, I., Basurto-Rios, R., Ibarra, J.E., 2003. Bacillus thuringiensis serovar israelensis is highly toxic to the coffee berry borer. Hypothenemus hampei Ferr. (Coleoptera: Scolytidae). Fems Microbiol. Lett. 226, 73–77. Neves, P.M.O.J., Hirose, E., 2005. Beauveria bassiana strains selection for biological control of the coffee berry borer. Hypothenemus hampei (Ferrari) (Coleoptera: Scolytidae). Neotrop. Entomol. 34, 77–82. Oliveira, P.S., Del-Claro, K., 2005. Multitrophic interactions in a neotropical savanna: ant-hemipteran systems, associated insect herbivores and a host plant. In: Burslem, D., Pinard, M., Hartley, S. (Eds.), Biotic Interactions in the Tropics: Their Role in the Maintenance of Species Diversity. Cambridge University Press, Cambridge, pp. 414–438. Perfecto, I., Castin˜eiras, A., 1998. Deployment of the predaceous ants and their conservation in agroecosystems. In: Barbosa, P. (Ed.), Perspectives on the Conservation of Natural Enemies of Pest Species. Academic Press, San Diego, pp. 269–289. Samuels, R.I., Pereira, R.C., Gava, C.A.T., 2002. Infection of the coffee berry borer Hypothenemus hampei (Coleoptera: Scolytidae) by Brazilian isolates of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae (Deuteromycotina: Hyphomycetes). Biocontrol Sci. Techn. 12, 631–635. Vandermeer, J., Perfecto, I., 2006. A keystone mutualism drives pattern in a power function. Science 311, 1000–1002. Vandermeer, J., Perfecto, I., Ibarra Nun˜ez, G., Philpott, S., Garcia Ballinas, A., 2002. Ants (Azteca sp.) as potential biological control agents in shade coffee production in Chiapas, Mexico. Agroforest. Syst. 56, 271– 276. Ve´lez, M., Bustillo, A.E., Posada, F., 2003. Depredacio´n de Hypothenemus hampei por Solenopsis geminata y Gnamptogenys sp. (Hymenoptera: Formicidae). In: Sociedad Colombiana de Entomologı´a (eds) Libro de Resumenes XXX Congreso. Cali, Colombia, p. 26.
Short communication
The effect of an ant-hemipteran mutualism on the coffee berry borer (Hypothenemus hampei) in southern Mexico Ivette Perfecto a,*, John Vandermeer a,b a
School of Natural Resources and the Environment, 440 Church, Dana Building, University of Michigan, Ann Arbor, MI 48109, USA b Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USA Received 5 August 2005; received in revised form 6 April 2006; accepted 11 April 2006 Available online 5 June 2006
Abstract The indirect effect of an ant-hemipteran mutualism was investigated in the coffee agroecosystem of Southern Mexico. The ant, Azteca instabilis, forms a mutualistic relationship with the coccid, Coccus viridis, on coffee plants. Through field surveys and experimental studies, the indirect effect of this mutualism on the main coffee pest in the region, Hypothenemus hampei, the coffee berry borer (CBB), was investigated. Results indicate a significant negative relationship between the number of coccids on a plant and the proportion of berries with damage by the CBB. Results also indicate that the effect of the ants is significant on per plant basis but not on per branch basis. Finally, a significant negative linear relationship was found between ant activity and the time it took ants to remove artificially placed borers on coffee berries. This study indicates that the mutualistic relationship between Azteca ants and the coccids has a positive indirect effect on the plant by reducing the numbers of the main insect pest of coffee. # 2006 Elsevier B.V. All rights reserved. Keywords: Integrated pest management; Coffee; Natural enemies; Pest control; Shade trees; Mutualism; Ants
1. Introduction The main pest of coffee in Latin America is the coffee berry borer (CBB), Hypothenemus hampei (Ferrari) (Coleoptera: Scolytidae) a small beetle that bores into the coffee beans as they are maturing (Baker, 1999; Damon, 2000). Effects of the borer are variable but can reach epidemic proportions and cause significant economic damage (Baker, 1999). Biological control potential has been reported for parasitic wasps (Barrera et al., 1990; Damon and Valle, 2002), entomopathogens (Samuels et al., 2002; Mendez-Lopez et al., 2003; Neves and Hirose, 2005) and ants (Armbrecht, 2003; Armbrecht and Perfecto, 2003; Ve´lez et al., 2003; Gallego and Armbrecht, in press). This study examines a complicated interaction involving a mutualism between the ant Azteca instabilis (F. Smith) * Corresponding author. Tel.: +1 734 764 1433; fax: +1 734 936 2195. E-mail address: [email protected] (I. Perfecto). 0167-8809/$ – see front matter # 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.agee.2006.04.007
and the green scale Coccus viridis (Green), in which the ant acts as a predator on the CBB, significantly reducing its impact as a pest. It has previously been demonstrated that the tending of various hemipterans (mainly aphids, coccids, mealybugs and treehoppers) by ants frequently has a net benefit on the host plant (Buckley, 1987; Dansa and Rocha, 1992; Oliveira and Del-Claro, 2005). In the case of A. instabilis and its mutualist C. viridis, the potential for an indirect positive effect using artificially placed larvae of Pieris rapae (L.) has been reported earlier (Vandermeer et al., 2002). While the ants tend coccids in large clumps concentrated on individual branches, they also patrol the rest of the plant and, in the case of an herbivore that requires some time to inflict damage, the ants are potential predators of that pest. This study uses field surveys and experimental manipulations, to investigate whether the ant A. instabilis also acts as a predator on the coffee berry borer.
I. Perfecto, J. Vandermeer / Agriculture, Ecosystems and Environment 117 (2006) 218–221
2. Methods 2.1. Field survey All A. instabilis nests were located in a 45 ha plot on Finca Irlanda, an organic shaded coffee farm located in southern Chiapas, Mexico (158100 North and 928200 West). The plot contains 10,647 shade trees (>10 cm dbh) in about 100 species, most of which seem perfectly suitable for nesting for this species of ant (nests have been found in 35 of the tree species, about what would be expected with a random allocation). Located near each of five nests that were isolated from other nests, six coffee trees were assessed for total number of coccids (C. viridis) (see below). The five nests were taken from widely separated areas within the 45 ha plot. Independent observers then assessed the same coffee trees, for total number of coffee berries and CBB damage. The proportion of damaged fruits per coffee plant was estimated as the number of coffee berries that had CBB (as evidenced from the entrance hole), over the total number of berries. The procedure was repeated in three areas that were isolated from any A. instabilis nests, again sampling areas widely separated from one another in the 45 ha plot. In the end, a total of 34 coffee plants were surveyed for total number of C. viridis, coffee berries and coffee berries damaged by the CBB. An additional survey was conducted on six coffee plants (haphazardly chosen to represent a range of densities for C. viridis) in which the total number of coccids on each branch was directly counted, and subsequently the rate of borer attack determined for the same branches. 2.2. Coccid sampling and estimations The following procedures were adapted, based on a preliminary study of 21 coffee plants for which the actual number of coccids were first determined in absolute terms and then compared with relative estimates obtained in several ways. On a given coffee plant a quick survey was undertaken to determine whether there were any obvious concentrations of coccids or ant activities. Based on this quick survey the plant was placed into one of three categories – a 5-min category, a four-class category, or a full count category. For those plants in the 5-min category the entire plant was scanned systematically from top to bottom during a 5 min period. All coccids (larger than 2 mm in length) on leaves, stems, and berries, were counted concentrating on berries and terminal shoots where the coccids tended to concentrate. The count of total number of coccids greater than 2 mm encountered in a 5 min period is the base number. The estimated actual number was computed as, estimated number = 2.55 base number. If, during the course of counting, more than six individual coccids were encountered on any given branch, the plant was transferred to the fourclass category. For those plants in the four-class category,
219
coccids were counted on each branch to determine which class the branch falls into: 0–6 individuals = low; 7–30 individuals = medium; 30–70 individuals = high; 70 and above = super high category. There was no need to actually count coccids unless the actual number was near the border between the categories. Normally a minute or so of counting made it evident to which class the branch belonged. To make an estimate of the final number estimate, all low branches were multiplied by 0; medium branches by 15; high branches by 46; and super extra branches by 150. Scaling numbers were determined from the initial study of 21 plants. The full count category included those plants that had no berries and fewer than 25 branches. All leaves and stems were examined and all coccids greater than 2 mm were counted. Estimating scales with this procedure and comparing the estimate to the known numbers from the preliminary study of 21 trees provides 93% efficiency in estimation (r2 = 0.926). 2.3. Experimental methods A coffee plant with actively foraging A. instabilis individuals was located near to each of the five ant nests mentioned above. A total of nine branches were chosen so as to represent a range of ant activity from high to low. On each of the branches, ant activity was assessed by watching a single point for a 5 min period and counting the number of ants passing that point, or, if ant activity was especially high, for a single minute. Then, one by one, individual borers were placed on a berry on each of the branches and the time to removal by an ant was recorded. Since it takes a borer a little more than an hour to completely burrow into a coffee berry (personal observations), the beetles were watched for a maximum of 70 min, if they persisted that long.
3. Results The relationship between number of coccids and percentage of coffee berries attacked by the CBB was assessed with a simple regression, which was significant ( p = 0.014, r2 = 0.18) for a linear regression of proportion of fruits with borers versus log of number of C. viridis (Fig. 1). Thus the total number of coccids on a coffee plant was inversely related to the proportion of berries attacked by the CBB. Assessment on a branch-by-branch basis revealed a far weaker relationship, which, while suggestive, was not significant statistically. It appears to be protection of the coffee plant as a whole that is affected by the presence of the ant, and not strictly localized to particular branches with a high concentration of coccids, although some degree of such localization is suggested. The results of the experimental manipulations indicated that there was a negative relationship between ant activity and the time of removal of CBB by ants (Fig. 2), with a significant regression of the log of time to removal versus the
220
I. Perfecto, J. Vandermeer / Agriculture, Ecosystems and Environment 117 (2006) 218–221
log of ant activity ( p < 0.01; r2 = 0.68). If 1 h is taken as approximately the critical time necessary for a borer to become invulnerable to A. instabilis, the simple linear regression of Fig. 2 suggests that the critical ant activity is about 45 ants per minute crossing a given point, which is significantly lower than the maximum ant activity observed in this experiment (114/min). As in previous experiments with P. rapae, even occasional patrolling by ants can thus effect control, although the results with the coffee berry borer are not as evident as with P. rapae (Vandermeer et al., 2002). Furthermore, it is worth noting that in 44% of the cases, the beetle was taken away in the mandibles of an ant, suggesting predation. Unlike the case of P. rapae in which most of the time the caterpillar simply fell off of the branch and escaped predation, the ants frequently carried the borers away, likely using them as a food source (Vandermeer et al., 2002).
4. Discussion
Fig. 1. Relationship between proportion of coffee berries with coffee berry borers and the log of the number of scale insects per coffee plant. Regression equation is above box and explains about 18% of the variance.
Fig. 2. Relationship between log of time to removal of coffee berry borer by ants and the log of the ant activity. Dashed lines indicate approximate position of critical ant activity that will attack an ant before the critical 1 h period (see text).
The results suggest that the mutualistic relationship between A. instabilis and C. viridis affords indirect benefits to the coffee plant through a reduction of the coffee berry borer. Thus, in practical terms, the damage done by the mutualistic herbivore (the coccid) must be judged relative to the protection against the coffee berry borer. This type of indirect interaction has been noted before for other associations in natural systems (Buckley, 1987; Dansa and Rocha, 1992; Fagundes et al., 2005; Oliveira and DelClaro, 2005) but is not well studied in agroecosystems where the net outcome of the interaction can have important economic implications. The only other documented case for an agroecosystem is that of the ant Dolichoderus thoracicus (Smith), its associated mealybugs and several economically important herbivores of cocoa in Malaysia (Khoo and Chung, 1989). In the case of D. thoracicus, the benefit of the ant as predator of cocoa pests is so much higher than the negative effect of the mealybugs that the farmers actively introduce ants with mealybugs to their cocoa plantations as a way of pest control (Perfecto and Castin˜eiras, 1998). The costs and benefits of the A. instabilis complex in coffee have not been studied sufficiently to determine whether the net outcome is likely to be positive for coffee production. Multispecies mutualistic systems can have a wide range of outcomes (Bronstein and Barbosa, 2002), however, the negative impact on CBB of the mutualism suggest that the ant-hemipteran mutualism can have an overall positive effect on coffee production. In the case of the Azteca-coccid–CBB complex, the ant colonies – and therefore also the CBB control – are patchily distributed (Vandermeer and Perfecto, 2006). These patches constitute a very small proportion of the plantation (about 4% of the shade trees in the case of Finca Irlanda). However, since the ant acts as a predator, that 4% represents a sink for
I. Perfecto, J. Vandermeer / Agriculture, Ecosystems and Environment 117 (2006) 218–221
the CBB population. Removal of 4% of the CBB population may have only a small effect on the overall population dynamics, but it does represent one more tool in the toolbox of potential biological control of the most important coffee pest in Latin America, the coffee berry borer. This local level dynamics leads to further speculation about what the dynamics might be on a more regional level. In a landscape dominated by shade coffee rather than unshaded coffee, the additional 4% control could have a major effect, depending on how close the CBB population is to being a stable one. In the current context, it appears that isolated shade plantations in an area of predominantly unshaded coffee may provide sinks that help control the borer over a broad region.
Acknowledgments We wish to thank the Peters family, the owners of Finca Irlanda, for allowing us to conduct this study on their farm. G. Lopez-Batista and B. Estevan Chilel, helped with data collection and the establishment of the 45 ha plot. Guillermo Ibarra and Alvaro Ballinas provided logistical support. The study was supported by NSF grant DEB-0349388.
References Armbrecht, I., 2003. Leaf litter ant diversity and function in coffee under different management systems. Ph.D. Dissertation. University of Michigan, Ann Arbor, MI, USA. Armbrecht, I., Perfecto, I., 2003. Litter-twig dwelling ant species richness and predation potential within a forest fragment and neighboring coffee plantations of contrasting habitat quality in Mexico. Agric. Ecosyst. Environ. 97, 107–115. Baker, P.S., 1999. The coffee berry borer in Colombia. Final Report of the DFID-Cenicafe´-CABI Bioscience IPM for coffee project. 143 pp. Barrera, J.F., Baker, P.S., Valenzuela, J.E., Schwarz, A., 1990. Introduction of two African parasitoid species to Mexico for biological control of the coffee borer Hypothenemus hampei (Ferrari) (Coleoptera: Scolytidae). Folia Entomol. Mex. 79, 245–247. Bronstein, J.L., Barbosa, P., 2002. Multitrophic/multispecies mutualistic interactions: the role of non-mutualists in shaping and mediating mutualisms. In: Tscharntke, T., Hawkins, B.A. (Eds.), Multitrophic Level Interactions. Cambridge University Press, Cambridge, pp. 44–66.
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