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Wasps create an acidic environment to deter predators

Gall wasps are small insects that lay eggs on plants and, when the larvae hatch out, they secrete chemicals that induce the plant to form galls. These are atypical, tumor-like growths of tissue that bulge out from a leaf, stem or root, depending on where the adult laid her eggs. The galls grow to envelope the larvae which derive shelter, protection and nourishment from living inside the lump of tissue. 

There are more than a thousand species of gall wasps, each one specializing on one particular species of host plant. Although scientists have long known about gall-inducing insects and their life cycles, the mechanism by which the larvae actually induce a host plant to develop galls is not yet understood. In fact, the induction of plant galls is considered the most complex association between insects and plants in the natural world.

Galls are mostly dully colored and match the tissues of the plants on which they form. But the galls that are induced by one species of cynipid wasp (Amphibolips nubilipennis) on the leaves of red oak trees look like tiny, juicy fruits. Wondering what would protect these structures from being eaten by other herbivores, scientists from Pennsylvania State University investigated the chemical composition of these fruit-like galls. 

In previous research, galls have been found to have an accumulation of tannins on their surface, which protects them against being eaten. After all, the tiny larva that manipulates the plant to produce the gall in which it hides, does not wish to be consumed. Tannins seem to deter some insects from eating galls by decreasing the efficiency of protein digestion in their guts. The researchers used high-performance liquid chromatography and gas chromatography–mass spectrometry to analyze the chemicals found in translucent oak galls (TOGs). 

Their results, published in Biology Letters, were quite surprising. The tiny wasp larvae induce the plant host to produce acids that have a pH of between 2 and 3, making them as acidic as lemon juice. Any herbivore that attempted to eat one of these translucent galls would be in for rather a sour shock. In fact, the interior of the gall is just as acidic as the fluid produced by pitcher plants to dissolve their insect prey. 

“This is exciting because it represents a novel defense system, one we haven’t seen before,” said Antoine Guiguet, an entomologist at Penn State and lead author on a paper about the new discovery.

“It’s so fascinating because this is an animal using chemistry to force a plant to do its bidding,” said John Tooker, professor of entomology at Penn State and co-author on the study. “It’s really a parasitic manipulation. The insect gets the plant to make the exact food it needs, which explains the nutritional hypothesis for why galls evolved, but undoubtedly, it has to be combined with a defense aspect, because if you have a good food source, other things are going to want to eat it.” 

“We know that pH this low is rare in plants generally,” said Tooker. “And the pH that we measured was close to the acidic nature of what’s inside a pitcher plant, which is about the same as a lemon. We are hypothesizing that the role of this is defense. Anything that wants to bore in there would be deterred by that acidic environment.”

The researchers investigated the organic acids present in the oak gall tissue in more depth and compared them with acids found in other galls and in certain fruits. They found that malic acid, a common acid in apples, represents 66 percent of the organic acid detected in the oak galls. The concentration of malic acid was twice as high as in other galls – and twice as high as in apples. 

“Malic acid is a fundamental component of the metabolism of cells, so it’s there within the oak, within all plant and animal cells, just at a low concentration,” said Guiguet. “What’s amazing is that this wasp is capable of inducing its accumulation in the storage compartment in plant cells, called a vacuole.”

With a pH level of between 2 and 3, the translucent oak gall is among the most acidic plant tissues measured to date. Until this discovery, only citrus fruit tissues were known to be capable of this extreme acidity, he explained. The researchers hypothesize the wasp could have developed acidic galls as an alternative strategy to the tannin accumulation observed in most other oak galls. 

But unlike tannins, acidic environments could also prove an efficient deterrent of parasitoid wasps, which are the main enemies of cynipid wasps. The parasitoid wasps use a long, needle-like ovipositor to bore through a gall and lay an egg on the unsuspecting resident larva. When the parasitoid wasp egg hatches, it proceeds to eat the resident larva, all the while living protected inside the gall that the victim induced. The researchers hypothesize that the acidic environment inside the oak gall may damage the ovipositor and deter parasitoid wasps from laying their eggs there.  

“The molecular mechanism by which cynipid wasps induce galls remains a mystery,” said Guiguet. “Now we have added to this mystery by showing they have evolved with capability of altering pH.”

The authors conclude that the “accumulation of organic acid in gall tissues is convergent with fruit morphology and may constitute a new defensive strategy against predators and parasitoids.”

By Alison Bosman, Staff Writer

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