It is interesting to note that humans, uniquely among the primates so far considered, appear to have stomach pH values more akin to those of carrion feeders than to those of most carnivores and omnivores.
Definition of carrion feeder: Any animal that feeds on dead and rotting flesh.
Gastric acidity is likely a key factor shaping the diversity and composition of microbial communities found in the vertebrate gut. The study conducted a systematic review to test the hypothesis that a key role of the vertebrate stomach is to maintain the gut microbial community by filtering out novel microbial taxa before they pass into the intestines. The study proposes that species feeding either on carrion or on organisms that are close phylogenetic relatives should require the most restrictive filter (measured as high stomach acidity) as protection from foreign microbes. Conversely, species feeding on a lower trophic level or on food that is distantly related to them (e.g. herbivores) should require the least restrictive filter, as the risk of pathogen exposure is lower. Comparisons of stomach acidity across trophic groups in mammal and bird taxa show that scavengers and carnivores have significantly higher stomach acidities compared to herbivores or carnivores feeding on phylogenetically distant prey such as insects or fish. In addition, the study found when stomach acidity varies within species either naturally (with age) or in treatments such as bariatric surgery, the effects on gut bacterial pathogens and communities are in line with our hypothesis that the stomach acts as an ecological filter. Together these results highlight the importance of including measurements of gastric pH when investigating gut microbial dynamics within and across species.
Results
In total, the studies' literature search yielded data on 68 species (25 birds and 43 mammals) from seven trophic groups (Table 1). A general linear model based on diet explained much of the variation in the stomach pH (R2 = 0.63, F1,6 = 17.63, p < 0.01). The trophic groups that were most variable in terms of their stomach pH were omnivores and carnivores that specialize in eating insects or fish.
The studies' hypothesis was that foregut-fermenting herbivores and animals that feed on prey more phylogenetically–distant from them would have the least acidic stomachs. Tukey-Kramer comparisons indicated that scavengers (both obligate and facultative) had significantly higher stomach acidities compared to herbivores (both foregut and hindgut) and specialist carnivores feeding on phylogenetically distant prey. Specifically, foregut-fermenting herbivores had the least acidic stomachs of all trophic groups while omnivores and generalist carnivores, with more intermediate pH levels, were not distinguishable from any other group (Fig 1).
The special case of herbivory
Carrion feeding imposes one sort of constrain on the ecology of the gut, an increase in the potential for pathogens. Herbivory imposes another, the need to digest plant material refractory to enzymatic digestion (cellulose and lignin). In order to digest these compounds, herbivores rely disproportionately on microbial processes. Different regions of the gastrointestinal tract (either rumen, caecum or in the case of the hoatzin a folded crop) function primarily as fermentation chambers. Thus, a challenge with fermentative guts is favoring those microbes that are useful for digestion while reducing the risk of pathogen entry into the gut. The study suggests that because the threat of microbial pathogens is relatively low on live leaves , herbivores can afford to maintain a chamber that is modestly acidic and therefore less restrictive to microbial entry. However, it finds several interesting exceptions to this generality. Beavers, which are known to store food caches underwater where there is a high risk of exposure to a protozoan parasite Giardia lamblia, have very acidic stomachs. The high stomach acidity may have evolved to manage this prevalent environmental pathogen. The other herbivore in our dataset with a very acidic stomach is the rabbit, which provides an interesting example of a behavioral modification of the stomach environment. Rabbits are known to engage in frequent coprophagy which allows them re-inoculate themselves with microbes. The specialized soft pellets that house microbes also reduce the stomach acidity creating an environment suitable for fermentation.
Human evolution and stomach pH
It is interesting to note that humans, uniquely among the primates so far considered, appear to have stomach pH values more akin to those of carrion feeders than to those of most carnivores and omnivores. In the absence of good data on the pH of other hominoids, it is difficult to predict when such an acidic environment evolved. Baboons (Papio spp) have been argued to exhibit the most human–like of feeding and foraging strategies in terms of eclectic omnivory, but their stomachs–while considered generally acidic (pH = 3.7)–do not exhibit the extremely low pH seen in modern humans (pH = 1.5). One explanation for such acidity may be that carrion feeding was more important in humans (and more generally hominin) evolution than currently considered to be the case. Alternatively, in light of the number of fecal-oral pathogens that infect and kill humans, selection may have favored high stomach acidity, independent of diet, because of its role in pathogen prevention.
The human stomach and the loss of mutualistic microbes
In general, stomach acidity will tend to filter microbes without adaptations to an acidic environment. Such adaptations include resistant cell walls, spore-forming capabilities or other traits that confer tolerance to high acidities and rapid changes in pH conditions. The study considered the role of the stomach as a pathogen barrier within the context of human evolution. Another potential consequence of high stomach acidity, when considered in light of other primates and mammals, is the difficulty of recolonization by beneficial microbes. A large body of literature now suggests that a variety of human medical problems relate to the loss of mutualistic gut microbes, whether because those mutualists failed to colonize during hyper-clean C-section births or were lost through use of antibiotics, or other circumstances. The pH of the human stomach may make humans uniquely prone to such problems. In turn, it might be expected that, among domesticated animals, that similar problems should be most common in those animals that, like humans, have very acidic stomachs.
The special risk to juvenile and elderly humans
If, in carnivores and carrion-feeders, the stomach’s role is to act as an ecological filter then it would also be expected to see higher microbial diversity and pathogen loads in cases where stomach pH is higher. We see evidence of this in age-related changes in the stomach. Baseline stomach lumen pH in humans is approximately 1.5 (it can go down to 1) (Table 1). However, premature infants have less acidic stomachs (pH > 4) and are susceptibility to enteric infections. Similarly, the elderly show relatively low stomach acidity ( pH 6.6 in 80% of study participants) and are prone to bacterial infections in the stomach and gut. It is important to note that these differences may be related to differences in the strength of the immune system however it is argued here that the stomach needs more consideration when studying these patterns.
Conclusion
The study demonstrates that stomach acidity increases with the risk of food-borne pathogen exposure and propose that the stomach plays a significant role as an ecological filter and thus a strong selection factor in gut microbial community structure and primate evolution in particular. In light of modern lifestyle changes in diet, hygiene and medical interventions that alter stomach pH, we suggest that stomach acidity in humans is a double-edged sword. On one hand, the high acidity of the human stomach prevents pathogen exposure but it also decreases the likelihood of recolonization by beneficial microbes if and when they go missing. However, in those cases where acidity is reduced, the gut is more likely to be colonized by pathogens. Though it is widely discussed in both the medical and ecological literature, data on pH are actually very scarce. Thus, to fully understand the patterns highlighted here more detailed studies on the gut microbiota across stomach acidities and diet are required.
