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

Abstract

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

“…These old infested berries may act as a population reservoir of borer populations and ant predation at this stage could be very important for limiting CBB populations in the next season. Third, as adult borers disperse (flying or crawling) to colonize new berries, ants may prevent them from entering new berries (Pardee and Philpott 2011;Perfecto and Vandermeer 2006;Philpott et al 2012). To date, no field experiment has specifically investigated how coffee-foraging ants limit CBB colonization of berries.…”

Leaf-Cutter Ant Parasitoids: Current Knowledge

“…The literature is vast and dispersed although there is a review about Pseudacteon biology and interaction with fire ants [2]. Other scarce studies were done on other ant-phorid systems such as Pheidole [3,4], Azteca [5,6], and Paraponera [7]. Until more information is gathered, generalizations will not be possible for these groups.…”

Parasitoids of the endangered leafcutter ant Atta robusta Borgmeier in urban and natural areas

“…For example, phorid fly species that attack Solenopsis invicta in agroecosystems are associated with annual open crops or closed perennial crops (Almeida & Queiroz 2009). Habitat structure affects microclimatic conditions and resource availability for the species, which may result in differences in parasitism rates by both dipteran and hymenopteran parasitoids (De La Mora & Philpott 2010;Vasquez-Ordonez et al 2012;Pardee & Philpott 2011). Although the association of E. breviloba with closed areas and of M. exrobusta with open areas is probably related to environmental conditions, we did not find a relationship between phorid presence and either temperature or humidity.…”