Human-induced climate change is warming our world, delivering wide-ranging impacts to all animals and plants and the environments they live in. But what if our world were a single leaf on a single apple tree? Would a heat wave affect us in the same way that it would affect bigger animals and their ecosystems? Sylvain Pincebourde and Jérôme Casas from Université de Tours, France, had an inkling that for itsy bitsy beasts, not all microclimates are created equal. To find out, they delved into the diminutive world of plant-eating mites and insects to see whether these critters can beat the heat.

How does one study the microcosm of animals that are only a few millimetres long? Very carefully, taking all environmental factors into account. Pincebourde and Casas chose six species with three different methods of feeding on leaves: two aphids (phloem feeding; phloem is a sugar- and mineral-rich form of sap), a leaf miner (leaf mining), and two spider mites and a lace bug (tissue piercing). First, the authors determined the thermal tolerance limits of each species – or how much heat the critters can handle – by finding their upper lethal temperatures, the temperature at which 50% of the individuals die. They then studied the microclimate on the surface of the leaves by measuring the carbon dioxide intake, water loss and temperature of intact leaves and leaves that had been fed upon by the tiny herbivores. Finally, the authors combined their data on the species’ temperature limits and the leaves’ surface environment to predict just how much heat each species can handle in the wild.

Each species had a different thermal tolerance and, incredibly, the upper temperatures that creatures living on the same plant could withstand varied by 8.5°C. The tissue piercers (spider mites and lace bug) could endure higher temperatures than the phloem feeders (aphids), and the leaf miner sat in between. The phloem feeders increased the leaf transpiration rate – that is, they increased the amount of water vapour leaving microscopic holes in the leaf called stomata – while the tissue piercers decreased transpiration a little and the leaf miner was once again in the middle. Importantly, the duo found that the creatures’ ability to withstand heat is directly related to leaf transpiration.

By increasing leaf transpiration rates, the phloem feeders, which have the lowest thermal tolerance, were able to minimise the temperature increase of the microclimate surrounding the leaf. This means that they can stay cooler than the species that reduce leaf transpiration and allow leaves to warm. The problem with this strategy is that the phloem feeders cannot handle high temperatures because they have adapted to living in a relatively cool environment, so heat waves may spell more trouble for them than tissue piercers, which live on a relatively hot leaves. The authors’ take-home message is that after taking leaf microclimate into account, spider mites, lace bugs, aphids and leaf miners only have a safety margin of 2–3°C, as half the species were already at risk of overheating at the highest temperature (37°C) tested by the scientists.

Mites and insects are likely to be more vulnerable to extreme temperatures than previously thought, and species living in temperate areas may find themselves in serious thermal strife during heat waves. Pincebourde and Casas reveal that current warming tolerances could be overestimated by up to 12°C – an enormous problem for accurately predicting future survival. Additionally, animals with different feeding apparatuses may be at different risks from climate change. It appears that creatures that turn on the air conditioning might not survive as well those that like to live with the windows open.

Narrow safety margin in the phyllosphere during thermal extremes
Proc. Natl. Acad. Sci. USA