A while ago now I discussed how some plants are able to warn others when they're under attack by grazing animals. Now it seems that these responses and interactions are even more subtle - a new paper describes how signalling chemicals in tobacco plants can be altered by the grazers' saliva (Allmann & Baldwin, 2010).
As I described in that earlier post, plants demonstrate a number of responses to grazing. They may produce chemicals that directly harm the grazing animal in some way: poisons, maybe, or substances that inhibit the animal's digestive processes. Other, volatile, chemicals allow communication with other plants - they signal the presence of herbivores and stimulate those plants receiving the signal to produce defensive chemicals in advance of any grazing attack. And it appears that some of these volatiiles can attract predators that in turn feed on the grazers.
Allmann & Baldwin studied the 'herbivore-induced volatiles' (or HIPVs) released by tobacco plants (Nicotiana attenuata) that were being munched on by caterpillars (Manduca sexta). They were interested to see if any of these compounds functioned in attracting specific predators on the caterpillars, something that's been seen in lab experiments but hasn't been well-documented in the field.
HIPVs can very considerably, depending not only on the plant & animal species involved but also with various abiotic environmental factors and on the passing of time. The authors identified compunds known as terpenoids as most likely to be involved in attracting predators, because they're released - after a delay of at least a few hours and up to a day or more - from the whole plant & not just the damaged tissues. The time delay would give opportunity for the plant to manufacture chemicals specific to the particular grazer attacking them. 'Green-leaf volatiles' (GLVs), on the other hand , are released from leaves as soon as they're damaged. With no time for them to be modified by the plant, this class of compounds would provide generalised information about just where on the plant the caterpillars are located: a wasp attracted by the terpenoids could then use the GLVs to home in on their target.
However, it turns out that things are more complex, & more subtle than that.
The researchers found that leaves that had been snipped, to simulate grazing, produced a particular mix of GLVs. But when they collected GLVs from plants that had been nibbled by M.sexta caterpillars, the ratio of diffferent GLVs changed over time. The next step was to snip more leaves (on a new set of plants), treat the wounds with either water or caterpillar drool, & again collect the volatile compounds that the leaves released. The result: caterpillar saliva, but not water, had a lasting effect on the ratio of GLVs. Some complex chemical analyses showed that the saliva wasn't stimulating a change in metabolic pathways within the plant, so the next question was, was there a compound in the saliva that was acting directly to modify the original volatile compounds released by a damaged leaf? Further experiments suggested that the answer was 'yes' - and that it was quite a specific enzyme; saliva from other species of caterpillars didn't have the same effect.
Because of this species-specific effect, Allmann & Baldwin then wondered whether the modified green-leaf volatiles might actually function in attracting carnivores (in this case, the wasp Geocoris) that prey specifically on Manduca sexta caterpillars. To test this one, they first mixed lanolin with different ratios of GLVs (iincluding the 'original release' & saliva-modified mixes). They then attached M.sexta eggs to the undersides of leaves low on the stems of tobacco plants, and placed cotton swabs with the different lanolin/GLV mixes close by. And waited. And discovered that the eggs were much more likely to be predated by Geocoris if they were sitting next to a cotton swab wafting saliva-modified GLVs into the air, basically waving a flag signalling that Manduca eggs (or young caterpillars) were there for the taking. So it wasn't just the terpenoids (that other class of signalling compounds) that were calling in the predators, after all.
All this works well for the plants, but you have to wonder - why do Manduca caterpillars produce this salivary compound? On the face of it, it's actually maladaptive: by altering volatile plant chemicals in a way that clearly identifies the presence of these caterpillars to their predators, it surely places the caterpillars at a selective disadvantage. Allmann & Baldwin suggest that the modified green-leaf volatiles may have some antimicrobial function that in some way enhances caterpillar survival. Now that's an intriguing suggestion for future investigation :) And a reminder that plant and animal interactions are often far more complex than they might first appear.
Allmann S, & Baldwin IT (2010). Insects betray themselves in nature to predators by rapid isomerization of green leaf volatiles. Science (New York, N.Y.), 329 (5995), 1075-8 PMID: 20798319