An Alkaline Foregut Protects Herbivores from Latex in Forage, but Increases Their Susceptibility to Bt Endotoxin

Abstract

About 10% of angiosperms, an estimated 20,000 species, produce latex from ubiquitous isoprene precursors. Latex, an aqueous suspension of rubber particles and other compounds, functions as an antifeedant and herbivory deterrent. It is soluble in neutral to alkaline pH, and coagulates in acidic environments. Here, I propose that foregut-fermenting herbivores such as ruminants, kangaroos, sloths, insect larvae, and tadpoles have adapted to latex in forage with the evolution of alkaline anterior digestive chamber(s). However, they consequently become susceptible to the action of Bacillus thuringiensis (Bt) δ-endotoxin and related bioinsecticides which are activated in alkaline environments. By contrast, hindgut-fermenting herbivores, such as horses and rabbits, have acidic anterior digestive chambers, in which latex coagulates and may cause gut blockage, but in which Bt is not activated. The latex-adapted foregut herbivore vs. latex-maladapted hindgut herbivore hypothesis developed in this paper has implications for hindgut-fermenting livestock and zoo animals which may be provided with latex-containing forage that is detrimental to their gut health. Further, ruminants and herbivorous tadpoles with alkaline anterior chambers are at risk of damage by the supposedly “environmentally friendly” Bt bioinsecticide, which is widely disseminated or engineered into crops which may enter animal feed streams.

Reply to Berry, C. Factors Related to Bacillus thuringiensis and Gut Physiology. Comment on “Rajan, V. An Alkaline Foregut Protects Herbivores from Latex in Forage, but Increases Their Susceptibility to Bt Endotoxin. Life 2023, 13, 2195”

“…The primary purpose of the original paper [2] was to put forward a hypothesis that alkaline guts may protect foregut-fermenting herbivores from the antifeedant, latex, in forage. This hypothesis has not been contested.…”

“…In his comment [1], Berry does not address the major claim in the original paper [2] regarding the selective pressure of latex on the development of alkaline guts in herbivores, except to point to a hypothesis that alkaline guts in Lepidoptera may have evolved to adapt to complex dietary tannins [12]. Several other mechanisms besides alkaline guts protect herbivores from antifeedants, such as proline-rich salivary binding proteins, uncharacterized tannin-binding proteins [13], and microbial symbionts whose populations vary with relative levels of phenolic glycosides and condensed tannins [14].…”

“…Another complication is that some target animals that have developed resistance do not show susceptibility despite an alkaline gut pH. Therefore, I withdraw the claim that "While direct measurement may be difficult in very small animals, there is an indirect way to test the pH of the first chamber of the gut by measuring the organism's susceptibility to Bacillus thuringiensis crystal δ-endotoxin (Bt)" [2].…”

“…This is a response to a comment titled "Factors related to Bacillus thuringiensis and gut physiology" [1] which repudiated some claims made in an article titled "An Alkaline Foregut Protects Herbivores from Latex in Forage, but Increases Their Susceptibility to Bt Endotoxin" [2]. The original article was not intended to litigate the safety of insecticidal toxins or dissect their mechanisms of action, but to put forward a hypothesis for how two completely different herbivore digestive systems could have evolved, and that the difference could relate to a disparity in the amount of latex in their forage.…”

Factors Related to Bacillus thuringiensis and Gut Physiology. Comment on Rajan, V. An Alkaline Foregut Protects Herbivores from Latex in Forage, but Increases Their Susceptibility to Bt Endotoxin. Life 2023, 13, 2195

“…Against this background, the recent paper published in this journal by Rajan [5] proposes that alkaline foreguts in a range of herbivores may have evolved to deal with dietary latex and, at the same time, that this increases their susceptibility to endotoxins from Bacillus thuringiensis (Bt). Whether or not latex is likely to be a driver of gut adaptations will not be addressed here, except to note that a range of other factors may also underpin the evolution of physiological conditions in the gut.…”