Disentangling the direct, indirect, and combined effects of experimental warming on a plant–insect herbivore interaction

Heather M. Kharouba and Louie H. Yang


There is increasing evidence that climate warming will have both direct and indirect effects on species. Whereas the direct effects of climate warming represent the proximate physiological consequences of changing abiotic conditions, the indirect effects of climate change reflect changes mediated by at least one other interacting species. The relative importance of these two kinds of effects has been unclear, limiting our ability to generalize the response of different species to climate change. Here, we used a series of experiments to disentangle some of the key direct and indirect effects of warming on the growth of monarch butterfly caterpillars (Danaus plexippus) and showy milkweed plants (Asclepias speciosa) during a window of rapid growth for both species. The effects of warming differed between direct, indirect, and combined effect experiments. Warming from 26°C to 30°C directly increased the growth of both monarch larvae and milkweeds, with monarch and milkweed growth rates showing similar sensitivity to warming. However, in a subsequent experiment, we did not observe significantly increased growth when comparing caterpillars and plants reared at 27°C and 31°C, suggesting that small differences can change the direct effects of warming. When caterpillars that were maintained at laboratory temperatures were fed leaves from host plants that were exposed to warmer temperatures, warming had a negative indirect effect on larval growth rates likely mediated by decreases in milkweed leaf quality. In experiments combining direct and indirect effects, we observed a net positive effect of warming on larval growth rates. Warming had no combined effects on milkweed growth, potentially due to opposing positive direct and negative indirect effects on growth mediated via increased monarch herbivory. These results show how variability among the direct, indirect, and combined effects of even relatively simple, short-term climatic perturbations can present challenges for predicting the broader effects of climatic warming in multispecies communities.



A meta-analysis of single visit pollination effectiveness comparing honeybees and other floral visitors

M.L. Page, C.C. Nicholson, R.M. Brennan, A.T. Britzman, J. Greer, J. Hemberger, H. Kahl, U. Müller, Y. Peng, N.M. Rosenberger, C. Stuligross, L. Wang, L.H. Yang, N.M. Williams


Many animals provide ecosystem services in the form of pollination, including honeybees which have become globally dominant floral visitors. A rich literature documents considerable variation in single visit pollination effectiveness, but this literature has yet to be extensively synthesized to address whether honeybees are effective pollinators.

We conducted a hierarchical meta-analysis of 168 studies and extracted 1564 single visit effectiveness (SVE) measures for 240 plant species. We paired SVE data with visitation frequency data for 69 of these studies. We used these data to ask: 1) Do honeybees (Apis mellifera) and other floral visitors differ in their SVE?; 2) To what extent do plant and pollinator attributes predict differences in SVE between honeybees and other visitors?; and 3) Is there a correlation between visitation frequency and SVE?

Key results
Honeybees were significantly less effective than the most effective non-honeybee pollinators but as effective as the average pollinator. The type of pollinator moderated these effects. Honeybees were less effective compared to the most effective and average bird and bee pollinators but were as effective as other taxa. Visitation frequency and SVE were positively correlated, but this trend was largely driven by data from communities where honeybees were absent.

Although high visitation frequencies make honeybees important pollinators, they were less effective than the average bee and rarely the most effective pollinator of the plants they visit. As such, honeybees may be imperfect substitutes for the loss of wild pollinators and safeguarding pollination will benefit from conservation of non-honeybee taxa.

American Journal of Botany


The effectiveness of eyespots and masquerade in protecting artificial prey across ontogenetic and seasonal shifts

Elizabeth G. Postema


When constraints on antipredator coloration shift over the course of development, it can be advantageous for animals to adopt different color strategies for each life stage. Many caterpillars in the genus Papilio exhibit unique ontogenetic color sequences: e.g., early instars that masquerade as bird feces, with later instars possessing eyespots. I hypothesize that larvae abandon feces masquerade in lieu of eyespots due to ontogenetic changes in signaler size. This ontogenetic pattern also occurs within broader seasonal shifts in background color and predator activity. I conducted predation experiments with artificial prey to determine how potential signaling constraints (specifically size and season) shape predation risk, and consequently the expression of ontogenetic color change in Papilio larvae. Seasonally, both predation and background greenness declined significantly from July to September, though there was little evidence that these patterns impacted the effectiveness of either color strategy. Caterpillar size and color strongly affected the attack rate of avian predators: attacks increased with prey size regardless of color, and eyespotted prey were attacked more than masquerading prey overall. These results may reflect a key size-mediated tradeoff between conspicuousness and intimidation in eyespotted prey, and raise questions about how interwoven aspects of behavior and signal environment might maintain the prevalence of large, eyespotted larvae in nature.

Current Zoology