Plants often avoid predation by producing chemicals that are detrimental to the herbivores that might try to eat them. For example, tiny hairs on the tobacco leaf (Nicotina attenuate) produce and secrete viscous liquids containing O-acyl sugars (AS) that are known to inhibit growth in certain insect larvae. Insects such as aphids, white flies and spider mites have each been shown to suffer from eating plants that produce AS. Because AS are known to effectively repel many herbivores, Alexander Weinhold and Ian Thomas Baldwin, from the Max Plank Institute for Chemical Ecology, were surprised when they recently found that one species of caterpillar, Manduca sexta, actually preferred to feed on small hairs flavoured with AS for their first meal after hatching. Weinhold and Baldwin were keen to test whether M. sexta suffered as a result of feeding on the usually lethal N. attenuate plant. The pair first measured the larvae body size and viability of caterpillars fed on AS-containing leaf hairs compared with caterpillars that ate AS-free leaves. They found that larvae fed from each food source grew equally well, and that rather than being a defensive mechanism, the plants provide a sugary first meal that was preferred by the growing caterpillars.
Based on the fact that many herbivore-damaged plants have been shown to produce chemicals that attract the herbivore's natural enemies, Weinhold and Baldwin carefully measured the profile of the odour produced by the caterpillar's faeces after they had been fed leaves that had been washed to removed the AS or leaves that retained their AS. The duo found that the food type directly affected the odour profile in the waste produced by the caterpillar. The caterpillars that consumed AS-containing leaves produced excretions with a strong odour, but they quickly lost the odour when the diet was changed to an AS-free food source.
Knowing that predators often use faecal odour to locate their prey, the team flavoured rice with the caterpillar odour and then allowed ants to collect the flavoured and unflavoured rice and return with it to their nests in order to identify the species that prey on the caterpillar. After counting the number of scented and unscented grains in the nests, Weinhold and Baldwin identified five ant nests all belonging to the same species of rough harvester ant, Pogonomyrmex rugosus. The team then placed caterpillar faeces that contained AS, and faeces that did not, on top of 20 cm wooden sticks and found that the P. rugosus ants preferentially climbed the sticks with fresh AS-containing excrement.
The authors conclude that while N. attenuate does not use AS in the typical way – as a direct defence against being eaten –consuming the sweet AS-containing leaf is not without penalty. Weinhold and Baldwin found that the resulting scent caused by eating AS indirectly helps the natural predators of caterpillars to locate them. So ants benefit from N. attenuate's AS-laced leaves: the odour-labelled caterpillar proves to be an appetizing GPS for the ground-hunting ant to find its prey.