UC Santa Cruz UC Santa Cruz Previously Published Works Title Ant-mediated (Hymenoptera: Formicidae) biological control of the coffee berry borer: diversity, ecological complexity, and conservation biocontrol Permalink https://escholarship.org/uc/item/4jq1d8hj Journal MYRMECOLOGICAL NEWS, 26 ISSN 1994-4136 Authors Morris, Jonathan R Jimenez-Soto, Esteli Philpott, Stacy M et al. Publication Date 2018-02-01 Peer reviewed eScholarship.org Powered by the California Digital Library University of California ISSN 1994-4136 (print) ISSN 1997-3500 (online) Myrmecological News Volume 26 Online earlier, for print 2018 Schriftleitung / editors Florian M. STEINER, Herbert ZETTEL & Birgit C. SCHLICK-STEINER Fachredakteure / subject editors Jens DAUBER, Falko P. DRIJFHOUT, Evan ECONOMO, Heike FELDHAAR, Nicholas J. GOTELLI, Heikki O. HELANTERÄ, Daniel J.C. KRONAUER, John S. LAPOLLA, Philip J. LESTER, Timothy A. LINKSVAYER, Alexander S. MIKHEYEV, Ivette PERFECTO, Christian RABELING, Bernhard RONACHER, Helge SCHLÜNS, Chris R. SMITH, Andrew V. SUAREZ Wissenschaftliche Beratung / editorial advisory board Barry BOLTON, Jacobus J. BOOMSMA, Alfred BUSCHINGER, Daniel CHERIX, Jacques H.C. DELABIE, Katsuyuki EGUCHI, Xavier ESPADALER, Bert HÖLLDOBLER, Ajay NARENDRA, Zhanna REZNIKOVA, Michael J. SAMWAYS, Bernhard SEIFERT, Philip S. WARD Eigentümer, Herausgeber, Verleger / publisher © 2017 Österreichische Gesellschaft für Entomofaunistik c/o Naturhistorisches Museum Wien, Burgring 7, 1010 Wien, Österreich (Austria) Myrmecological News 26 1-17 Online Earlier, for print 2018 Ant-mediated (Hymenoptera: Formicidae) biological control of the coffee berry borer: diversity, ecological complexity, and conservation biocontrol Jonathan R. MORRIS, Estelí JIMÉNEZ-SOTO, Stacy M. PHILPOTT & Ivette PERFECTO Abstract Ants are important biological control agents of the coffee berry borer (CBB), Hypothenemus hampei (FERRARI, 1867), the most damaging insect pest of coffee around the world. Ants also occur naturally in coffee landscapes, opening the door to conservation biocontrol approaches, which can promote both biodiversity conservation and crop production. Here, we review evidence that shows that ants antagonize and predate CBB, reduce CBB infestation, and contribute to the suppression of CBB populations. We discuss the potential mechanisms and impacts of ant diversity and inter- action complexity on the functioning of CBB biocontrol. We also discuss the implications of conservation biocontrol in coffee farm management, reviewing literature showing that ant communities and CBB respond to coffee farm intensification and the composition of the agricultural matrix. We assess the potential impacts of ant-CBB biocontrol on coffee production and yield, considering the complexities that result from promoting diverse ant communities in conservation biocontrol, and discuss potential disservices of ants. Finally, we end with several research avenues that are needed to further illuminate the overall role of ant communities on coffee pests and yield and to make specific recommendations for ant-CBB biocontrol management. Spanish abstract Abstract S1, as digital supplementary material to this article, at the journal’s web pages. Key words: Coffee, coffee berry borer, conservation biocontrol, biodiversity, interaction complexity, review. Myrmecol. News 26: 1-17 ISSN 1994-4136 (print), ISSN 1997-3500 (online) Received 7 June 2017; revision received 28 August 2017; accepted 29 August 2017 Subject Editor: Jens Dauber Jonathan R. Morris (contact author) & Ivette Perfecto, School for Environment and Sustainability, University of Michigan, 440 Church St., Ann Arbor, MI 48109, USA. E-mail: [email protected] Estelí Jiménez-Soto & Stacy M. Philpott, Environmental Studies Department, University of California, Santa Cruz, 1156 High Street, Santa Cruz, CA 95064, USA. Introduction Globally, agricultural intensification is one of the most natural enemy species (STRAUB & al. 2008, CROWDER & significant drivers of habitat degradation and, subsequently, JAbbOUR 2014) and the ecological networks (VANDERMEER & biodiversity declines. Nearly 40% of earth’s terrestrial al. 2010, WIELGOSS & al. 2014) in which they are embedded. surface is under agricultural production (FOLEY & al. 2011). Coffee is an important global agricultural commod- Agroecological strategies that integrate both conservation ity – more than one billion cups of coffee are consumed and crop production are increasingly necessary (KREMEN every day (JHA & al. 2014). Over 20 million farming fam- 2015). Conservation biocontrol is an approach which aims ilies grow coffee in some 80 countries around the world to bolster naturally occurring enemy communities through and are dependent on its production for their livelihoods the maintenance of habitat, in and around farms, so they may (VEGA & al. 2003, DONALD 2004, VEGA & al. 2015). Most better control pests and may have the benefit of conserving coffee production occurs in biodiversity hotspots in the additional biodiversity in the process (BARBOSA 1998). This tropics – areas known for their conservation importance approach can be more effective than classical biocontrol (MOGUEL & TOLEDO 1999). Coffee farms and landscapes because the natural enemies promoted are typically gener- can provide habitat for an impressive array of biodiversity alists, which persist in the field even when pest populations (PERFECTO & al. 1996, PERFECTO & al. 2005, PHILPOTT & al. are low and may also predate secondary pests (SYMONDSON 2008a, JHA & al. 2014). However, coffee intensification, & al. 2002). Additionally, diverse natural enemy commu- through the removal of shade-trees and increased use of nities may be more robust to environmental disturbances agrochemicals, reduces biodiversity on farms (PHILPOTT & and future pest outbreaks (STRAUB & al. 2008, CROWDER & al. 2008a, PERFECTO & VANDERMEER 2015). Furthermore, JAbbOUR 2014). However, whether natural enemy diversity both planned and associated biodiversity on coffee farms benefits pest control is context-dependent (LETOURNEAU & contributes to important ecosystem services, including pest al. 2009) and is driven by complex interactions between control (VANDERMEER & al. 2010, JHA & al. 2014). Coffee systems are therefore well-suited for the implementation of CBB have been limited, and the rearing and release of natural agroecological practices, such as conservation biocontrol, enemies can be costly and labor-intensive (VEGA & al. 2015). to promote both conservation and production (PERFECTO & Furthermore, classical biocontrol risks that introducing novel VANDERMEER 2015). organisms into systems can result in unintended invasions The coffee berry borer (CBB) (Hypothenemus hampei and the disruption of interaction networks (SImbERLOFF & (FERRARI, 1867), Coleoptera: Curculionidae), is one of the STILING 1996, SImbERLOFF 2012). most economically devastating pests of coffee around the Conservation biocontrol, in contrast, is a promising pest world (DAMON 2000, JARAMILLO & al. 2006). This small control approach in coffee. Recent research has demonstrated beetle specializes on the fruits of both commercial species that native generalist predators, like birds, can significantly of coffee, Coffea arabica and Coffea canephora (robusta), reduce CBB infestation and prevent yield loss, when they for its reproduction and growth. Upon colonization of a are bolstered by the conservation of near-by forest patches coffee plant after dispersal, mature female CBB bore gallery (KELLERMANN & al. 2008, JOHNSON & al. 2010, KARP & al. tunnels into fruits, where they lay their eggs. After the CBB 2013). Ants also occur naturally in coffee and act as important eggs hatch, the larvae consume the endosperm of the fruit natural enemies of CBB, yet are underrepresented in the where they complete their development until they are ready general CBB biocontrol literature (MURPHY & MOORE 1990, to colonize new fruits (DAMON 2000). Infestation damages DAMON 2000, BUSTILLO & al. 2002, JARAMILLO & al. 2006, the fruit through direct consumption by the borers and by VEGA & al. 2009, ARISTIZÁBAL & al. 2016). Some research facilitating the infection of saprophytic microorganisms also suggests a low awareness of ants as natural enemies of which deteriorate the coffee bean (DAMON 2000). This CBB by coffee farmers in Latin America, despite concerns damage reduces the quality of the coffee crop, and in the about CBB by both organic and conventional growers (SE- worst cases can lead to early fruit senescence and complete GURA & al. 2004). This is surprising given the rich history degradation of the berry. CBB is now nearly ubiquitous in and potential of ants as biocontrol agents in agriculture coffee producing regions, with infestation levels in some around the world (CARROLL & RISCH 1990, WAY & KHOO cases at 100% of fruits, and the highest yield losses ranging 1992, PERFECTO & CASTIÑEIRAS 1998, OFFENBERG 2015). Ants from 35% to 80% (VEGA & al. 2015). It is estimated that possess unique traits as natural enemies, where colonies can this damage costs farmers over $500 million (U.S. dollars) efficiently respond to changes in prey density by varying in yield losses annually (VEGA & al. 2015), with additional worker recruitment rates and can consume high numbers expenses in the cost of pesticides used to control it. of prey without satiating by storing resources (RISCH & The literature on CBB is extensive (PÉREZ & al. 2015) CARROLL 1982, OFFENBERG 2015). For these reasons, ants are and a range of control strategies