Top-down vs. bottom-up is a function of temperature for forest Lepidoptera
The slow-growth-high-mortality hypothesis predicts that prolonged development time in foliage feeding insects results in greater exposure to natural enemies and therefore lower survival. Because higher temperatures increase insect growth rates and reduce the number of days larvae are exposed to predators, the hypothesis predicts that higher temperatures should lower the impact of predators on foliage feeding insects. However, higher temperatures can increase the attack rates of predators (top-down) and can also lower the nitrogen content of the leaves these insects eat (bottom-up).
To test whether the positive effects of warmer temperatures on foliage-feeding caterpillars can outweigh the expected negative effects propagated through increased predator attack rates or reduced foliar quality, we placed late instar Papilio canadensis (Papilionidae) larvae on individual saplings in six forests (1990-1991, Ohio, Michigan, and Alaska, USA), monitored their survival at 24-hour intervals, and used logistic regression to model larval daily survival rate as a function of temperature. We additionally measured the daily survival rate of caterpillars of three common, cryptic Lepidoptera species at the Hubbard Brook Experimental Forest in northern New Hampshire, USA (2012-2013), and quantified larval growth rates as a function of temperature on leaves with two different nitrogen levels.
We found support for a model in which daily survival rate of caterpillars decreased as temperature increased in four of the nine site-years. When present, small decreases in daily survival rate at higher temperatures outweighed the positive effects of faster caterpillar development. Foliar nitrogen was consistently lower in leaves grown at lower, warmer elevations. This difference affected caterpillar growth rates such that the negative effect of decreased food quality balanced the positive effect of increased growth rates at higher temperatures. Thus, we found that negative indirect effects on caterpillars propagated through predators and food quality can outweigh the benefits of faster development time at higher temperatures, but this effect was not consistent across site-years. The slow-growth-high-mortality framework effectively integrated energy- and materials-based approaches to evaluating the effects of temperature on species interactions in a forest food web.