The slow-growth high-mortality hypothesis: Direct experimental support in a leafmining fly

1. Based on the slow-growth high-mortality (SGHM) hypothesis, which predicts that prolonged larval development increases mortality from their natural enemies, studies have often assumed that low quality of plants that slows larval development would function as a defence against insect herbivores. However, empirical support for the SGHM hypothesis has been limited, especially in natural and ecologically relevant contexts. 2. In a leafminer Amauromyza flavifrons Meigen (Agromyzidae, Diptera), the SGHM hypothesis was tested along with four other hypotheses (e.g. prey size, mine appearance, density-dependent parasitism, and plant quality hypotheses) to control for spurious associations between development time and parasitism that are primarily driven by other larval traits. Two host plant species, Saponaria officinalis and Silene latifolia, were grown under varying nitrogen levels, and leafminers developing on these plants were exposed to, or protected from, a natural assembly of parasitoids across the entire course of larval development. 3. On both host plant species, leafminers that survived to an adult stage in the presence of parasitoids had a shorter development time than those in the absence of parasitoids, indicating that parasitoids disproportionately kill leafminers with longer larval development. The results provided concrete evidence for the SGHM hypothesis within the natural ecological context for these interacting species. Moreover, reduced plant quality was associated with higher larval mortality on Sa. officinalis only in the presence of parasitoids, suggesting that low quality could function as indirect plant resistance via SGHM under some tri-trophic interactions.