Preference-performance linkage in a herbivorous lady beetle: consequences of variability of natural enemies.

We investigated the relationship between oviposition preference and offspring performance in a herbivorous lady beetle Epilachna pustulosa on two co-occurring plant species, thistle Cirsium kamtschaticum and blue cohosh Caulophyllum robustum, in 1994 and 1995. The relative importance of bottom-up effects by host plants and top-down effects by natural enemies on offspring performance were determined using field and laboratory experiments. In both years, egg density on blue cohosh was significantly higher than on thistle. A laboratory experiment demonstrated that larval survival from hatching to adult emergence was significantly higher, and developmental period shorter when larvae were reared on blue cohosh compared to thistle. The positive preference-performance linkage varied between years in the field. Top-down effects had a different impact on larval survival on the two host plant species. Arthropod predators, a lady beetle Harmonia axyridis and an earwig Forficula mikado, considerably depressed immature survival on thistle, while they were negligible on blue cohosh. Although the lack of effective predation increased larval survival on blue cohosh, it led to defoliation due to increased larval feeding late in the season. Because of severe intraspecific competition, old larvae had significantly lower survival on blue cohosh than on thistle. In 1994, as larval survival decreased due to defoliation on blue cohosh, the overall survival rate was significantly higher on thistle than on blue cohosh. This survival pattern was opposite to that found in the laboratory experiment. In contrast, in 1995, the increase in predatory lady beetles on thistle caused greater larval mortality. Thus, the overall survival was significantly lower on thistle than on blue cohosh, although severe intraspecific competition occurred on blue cohosh as it had in 1994. Consequently, the offspring performance on the two host plants is largely determined by the relative importance of arthropod predation determining larval survival on thistle and host plant defoliation reducing late larval survival on blue cohosh. These results indicate the important role of spatial and temporal variability of natural enemies on the preference-performance linkage of herbivorous insects.