The spatio-temporal relationships among aphids, the entomophthoran fungus, Pandora neoaphidis, and aphidophagous hoverflies in outdoor lettuce

Worldwide, aphids are the key pests of lettuce, and they coexist with natural enemies in different guilds. In our study, the spatio-temporal patterns of aphids colonizing lettuce were assessed and compared with the distribution of an entomopathogenic fungus and hoverfly larvae during two spring lettuce growing seasons. Counts of aphid density, entomopathogenic fungal-infected aphids and hoverfly larvae present on lettuce plants were recorded and their spatial distribution analyzed using the Spatial Analysis by Distance IndicEs (SADIE) method to determine aggregation and association indices. Three aphid species (Nasonovia ribisnigri, Macrosiphum euphorbiae and Acyrtosiphon lactucae) colonize lettuce plants in early spring; however, their natural enemies arrive several weeks later. Pandora neoaphidis was the only fungus identified to cause aphid mortality, and Sphaerophoria scripta was the most abundant syrphid species preying on lettuce aphids. In both 2007 and 2008, the aphids followed ephemeral spatio-temporal dynamics at the field scale. The maximum aphid aggregation was concurrent with the highest aphid density and with the complete development of the rosette lettuce leaf-stage. P. neoaphidis-infected aphids showed more aggregation over time than hoverfly larvae. The maximum spatial structure was recorded for both natural enemy species close to the harvest date and at the time when the aphid populations were distributed at random. Significant spatial associations between P. neoaphidis and hoverfly larvae were only detected close to the time of harvest, which reduces the risk of intraguild predation between these two natural enemies of aphids at the field scale.