Herbivore dietary specialization increases ant predation on temperate forest caterpillars

Background/Question/Methods

The enemy-free space hypothesis (EFSH) predicts that dietary specialist herbivores are superior to generalists in using host plants for defense or refuge from enemies. The EFSH has received strong support from herbivore community-level tests with generalist predators, especially predaceous ants. Studies using predaceous ants have identified sequestration of plant toxins as the major mechanism by which dietary specialists acquire an advantage in anti-predator deterrence. Here, we test the EFSH with respect to ant predation in an assemblage of dietary specialist and generalist caterpillars living on 8 common tree species in a temperate forest (Middlesex Co., CT, USA). Like most temperate tree species, the young leaves of the tree species included here largely lack toxins that might be sequestered by caterpillars. Therefore, in this experiment, we asked if the EFSH holds for caterpillars facing ant predation in a relatively toxin-free environment. To quantify ant predation on caterpillars, we ran an ant-exclusion field experiment over the same 6-week period over 3 years (2010-12). In addition, we subjected experimental caterpillars to a simulated predation trial to determine if their behavioral responses correlated with diet breadth or ant predation.

Results/Conclusions

Our results contradict the broadest prediction of the EFSH in that dietary specialist caterpillar species experienced increased ant predation relative to generalist species. The simulated predation trials showed that specialist caterpillar species tend to remain still when attacked, whereas many generalist caterpillar species responded with avoidance behavior, such as thrashing, locomotion, or dropping. These results suggest that in the absence of chemical deterrence, the host specificity of specialist herbivores might constrain their ability to gain enemy-free space from ants. As previous work in the system has shown that the same specialist caterpillars gain enemy-free space against avian predators relative to dietary generalist caterpillars, these new results reveal ecological trade-offs for both specialist and generalist herbivores. Cryptic specialists in this system sacrifice protection from ant predators to gain protection from birds; dietary generalists sacrifice protection from avian predators to gain both protection from ants and greater feeding opportunities.