Theroa zethus caterpillars use behavior and anti-predator weaponry to disarm host plants

Caterpillars within the Notodontidae family (butterflies and moths with approximately 3,800 known species, found in all parts of the world, but mostly in the tropics, especially in the New World; they feed primarily on leaves of ‘woody’ trees and shrubs) use hosts (plants) that differ markedly in defenses and ecology. A notable example, Theroa zethus, feeds on transitory herbs in the Euphorbiaceae family (the ‘spurge’ family, a large family of flowering plants, sometimes called euphorbs, which include tropical shrubs or trees) that germinate and grow rapidly in response to seasonal monsoon rains in the North American Southwest. When damaged, these host plants emit copious quantities of latex — a defensive fluid known to be poisonous to many other plants.

The latex coagulates as it exudes from the plant, potentially entrapping, or gumming up, insect herbivores (plant-eating animals). The Theroa zethus caterpillar is the only known member of its genus, and one of just a few notodontids in North America, that feed on hosts protected by latex canals (laticifers). Latex in euphorbs is stored under pressure, within living cells that form elongated branching tubes; in mature plants, the laticifers occur in the stem, petiole, and midrib and tend to follow the lateral and minor veins in the leaf. Feeding folivores (animals that survive by eating leaves) rupture the canals — which causes the immediate flow of latex from high pressure in the canals — to low pressure at the breach.

Theroa zethus caterpillar larvae disarm the laticifers by co-opting their defensive weaponry: they secrete concentrated acid onto the plant surface — from a gland located on their underside, between the head and prothorax legs; this gland is variously called the ventral eversible gland (VEG), prothoracic gland, or repugnatorial gland. In most notodontids, the caterpillar’s VEG serves to deter predators; when disturbed, larvae spray acid precisely aimed at the attacker.

Authors [see attached article] filmed these caterpillar larvae on poinsettia plants, and then simulated their behaviors and tested how their behaviors (individually, and combined) affect the discharge of latex. Larvae initially scraped the stem, petiole, or midrib with their mandibles (jaws), and then secreted acid from their VEG onto the scraped surface; scraping facilitated acid penetration by disrupting the waxy cuticle. As the acid softened tissues — the larvae used their mandibles to compress the plant repeatedly, thereby rupturing the latex canals. Scraping, acid application, and compression created withered furrows that greatly diminished latex discharge distal to the furrows where the larvae invariably fed.

In summary, the VEG in notodontids ordinarily serves to deter predators; when attacked, larvae spray acid aimed directly at the assailant. Using high-pressure liquid chromatography, authors documented that the caterpillar VEG secretion contains 30% formic acid with small amounts of butyric acid; when applied to poinsettia petioles, these acids decreased latex outflow — similar to that of VEG secretion milked from larvae. VEG acid disrupts latex canals in part by stimulating the normal acid-growth mechanism employed by plants to loosen walls for cell elongation. Histological examination of cross sections in poinsettia midribs confirmed that cell walls within furrows were often highly distorted, as expected when VEG acids weaken walls. This capability may represent a pre-adaptation that facilitated the host shift in the Theroa lineage onto latex-bearing plants by enabling larvae to deactivate laticifers with minimal latex contact. This study elucidates a complicated story in gene-environment interactions. 😊

PLoS ONE July 2019; 14: e0218994

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