Our Affinity for the Sour

The Raw and the Rotten (7)

I, like many, have wondered why many children are attracted to sour candies, not just mildly attracted, extremely so. And not just moderately sour but exceedingly sour, far beyond what I can tolerate. The candy industry is aware of this and keeps upping the ante on sourness. Some of the most popular sour candies are called “warheads”, first developed in Taiwan but extremely popular with young Americans. Japan produces most of the next generation sour candies which exceed even warheads in their capacity to pucker. The appeal of sourness is not restricted to candy. Many Kids from 5-9 years of age, love vinegars and will eat lemons in much the same way as adults eat oranges.  It’s not for lack of sensitivity to the sour taste. Children in this age range are hyper-sensitive to tastes of all sorts. Our sense of taste increasingly deteriorates as we age.

Ever observant, Charles Darwin was perhaps the first to put pen to this mystery: “I will add that formerly it looked to me as if the sense of taste, at least with my own children when they were still very young, was different from the adult sense of taste; this shows itself by the fact…they strongly preferred the most sour and tart fruits, as for instance unripe gooseberries and Holz apples”.

What puzzled Darwin—and should puzzle advocates of Darwinian Medicine-- is that sourness wouldn’t seem to be a good indicator of food quality. It is associated with the underripe (fruits) and the overripe (everything else). Everything, that is, that seems outside the range of nutritious fare. And by this age children are learning what foods to be disgusted by. Why aren’t more kids disgusted by lemons?

Sourness is directly related to acidity. In fact, perception of sour is perception of acid. Lemons have about the same level of acidity as our stomachs, which is extremely high. Many of us have had occasion to taste stomach acidity through acid reflux. Eating a lemon, is equivalent to acid reflux acid-wise.

There is variation among children in the degree to which they find sour stuff attractive. Those who most seek the sour are also the prone to try new foods. Those less attracted to sour foods tend to be more finicky. (https://doi.org/10.1093/chemse/28.2.173; But even those at the low end find sour stuff much more appealing than other primates. And as adults, long after our taste for the extremely sour has abated considerably, we humans have a greater affinity for acidic foods than any other primate, except for owl monkeys (genus Aotus), unusual nocturnal primates of the New World. Owl monkey consume lots of sour fruits. Chimpanzees/bonobos also have more tolerance for acidic foods than most primates but far less than humans or owl monkeys. For humans, sour fruits may have been the gateway to other forms of sour foods.

Flavor: It’s Not Just Taste; and Taste is Not Just in the Mouth

Let’s now consider some human adaptations to acidic foods. Flavor perception is a complex interaction of three distinct sensory systems: olfaction (smell), taste and chemesthesis. The last one is the least familiar; it refers to the chemically-induced sensations of heat and pain, as well as the perception of tactile stimuli. Chemesthetic receptors reside in the mucosal tissue that lines the mouth. The spiciness we perceive from chilis is mediated through chemesthetic heat sensitive cells that reside there. (So, there’s good reason to call spicy food hot.) These cells don’t respond as quickly as olfactory or taste cells, hence the delayed reaction to spicy foods. The tactile chemesthetic cells in the mucosa play a role in what is known as “mouth feel”.

Chemesthesis is the final stage in flavor perception, olfaction is the first. Our noses are filled with diverse olfactory receptors tuned in hundreds of different ways to respond to diverse chemical odorants. It is often claimed that 75-80% of taste is actually smell. When you are “stuffed up” your sense of taste is greatly compromised because these receptors are impaired. In any case, olfaction and taste are intimately intertwined and they are communicated to the brain packaged together.

Most taste receptors reside in the tongue. Until very recently five distinct types of tastes have been recognized: sweet, bitter, salty, sour and umami (savory). Of these, umami was the last to be recognized as such. But the mechanism for tasting sour was the last to be deciphered.

The same receptors found in the nose and tongue can be found throughout the gut, where they are labeled nutrient receptors. Gut nutrient receptors complement the tongue’s taste receptors. Bitter taste, for example, is often associated with toxicity. Bitter foods are often rejected before they are swallowed. But some bitter foods have health benefits, so not all bitter foods are rejected. The bitter nutrient receptors in the gut can act as a further filter in determining what bitter chemicals are absorbed in the intestine. Conversely, the attraction to sweet, salty and umami foods is reinforced by their respective gut nutrient receptors. These gut nutrient receptors are as connected to the brain as the taste receptors in the tongue. They constitute part of what is known as the Gut-Brain Axis.

Fatty Acid Perception

Fatty acids have come to the fore in discussions of dietary health. Much of the focus has been on saturated, unsaturated, and polyunsaturated forms, where saturation refers to the degree to which the carbon atoms in the fatty acids are bonded to hydrogen atoms, as opposed to each other. We will leave these distinctions aside for now. For present purposes we need to attend to a different way to classify fatty acids, which is by the amount of carbon atoms that form the backbone. The more carbon atoms the longer the fatty acid. Short chain fatty acids have 2-6 carbon atom backbones, medium chain fatty acids 6-12, and long chain fatty acids 12 and up.

Short chain fatty acids are pretty much an unadulterated good thing health-wise. They are produced in abundance by our gut microbiomes. Unsurprisingly, there are abundant and specific receptors in the colon with which short chain fatty acids interact. These same receptors respond to the postbiotic short chained fatty acids that arrive in the colon by way of external acidic fermentation. Moreover, recently, another type of taste receptor in the tongue has been discovered that specifically responds to short chain fatty acids (https://doi.org/10.1016/j.cophys.2021.01.008; https://doi.org/10.1016/j.cophys.2021.01.008Get rights and content ). This sixth taste sense could only have evolved to respond to these particular byproducts of externally fermented foods, because short chain fatty acids are absent in raw foods.

Another gut nutrient receptor responds specifically to a different metabolite of external but not internal acidic fermentation. This metabolite is a “medium chain fatty acid” called hydroxycarboxilic acid (HCA) https://nbn-resolving.org/urn:nbn:de:bsz:15-qucosa2-732849. There are three varieties of HCA, each with its own receptor. It’s the third one (HCA3) that is relevant here. All mammals have HCA1 and HCA2, only the great apes and humans have HCA3, the result of a gene duplication that occurred about 10 million years ago. HCA3 plays an essential role in the immune response and fat metabolism.

This gene duplication that produced HCA3 is one of the genomic alterations that Katherine Amato cites as evidence for the early consumption of fermented foods in the human lineage
https://doi.org/10.1086/715238. We share this gene duplication with all great apes but the human HCA3 receptor is much more sensitive to HCA3 than the great ape versions. Some further modifications in this receptor seems to have occurred after humans diverged from the great apes, perhaps as the fermented component in the human diet increased.

So, humans possess two receptors tuned specifically to the byproducts of fermented foods, one on the tongue, one in the colon. The one in the tongue, a novel taste receptor, responds specifically to short chain fatty acids; the one in the gut, a nutrient receptor, responds to specific medium chain fatty acids. The short chain fatty acid receptors evolved to sense the short chain fatty acids produced by the gut microbiome. But they are equally sensitive to the short chain fatty acids produced by external fermentation. This is known as an exaptation.

Acidic Fermentation of Plant Foods

Did our ancestors eat sour fruits like owl monkeys? The answer is yes and no. Many fruits consumed by owl monkeys are unripe but not all. Some fruits are extremely sour when ripe--such as persimmons, lemons and medlars--Many other ripe fruits are moderately acidic. In contemporary diets these include oranges, tomatoes, grapes, blueberries, pineapples, peppers, apples and mangos; all forbidden in the trendy but deeply misguided Alkaline Diet. Our ancestors may have eaten sour fruits but they were neither ripe nor unripe. They were overripe.

There is a continuum from under-ripeness to over-ripeness. There is also a broad range of states that we call overripe, when the fruit is in the process of rotting.  In the early stages an overripe fruit is sweeter than at any stage of ripeness. But it is at this zenith of sweetness that the microbes colonize the fruit’s interior. I will detail the early stages of the process in a separate post; here I will focus on the later stages.

Lactic acid bacteria have been lurking on the “skin” of the fruit throughout the ripening process. Some avail themselves of the sugars (primarily glucose and fructose) early on, once the skin is breached. But in those early stages the yeasts are in control. And it is the yeasts that consume most of the sugars. As those sugars are consumed the role of yeasts in fermentation declines accordingly. Other members of the fermentative ecosystem come to the fore. Many are lactic acid bacteria, which encompasses a vast number of species and a broad range of metabolic capacities.

The LAB species that consume the sugar disappear with the yeasts and new species take over that utilize other nutrient substrates. Lactic acid levels climb throughout the rotting process and become especially noticeable once the sugars are consumed. No doubt our ancestors would prefer the fermenting fruit in the sweetest state. But given our predilection for sour foodstuffs, they probably did not find the soured remains at all aversive. Moreover, during much of the rotting process, the fruits can be both sweet and sour, an irresistible combination exploited by many cultures today.

Beyond sour fruits what acidic foodstuffs would our ancestors have routinely encountered? Raw plant materials are only mildly acidic at most. Rotting plant foods though can be quite acidic due to lactic acid fermentation. Lactic acid bacteria are present on all living plants; their populations boom when plant tissue—fruit, leaf, stem or seed--dies.

All plant tissues are subject to rot but some plant tissue rot more quickly than others. A compost pile is a good place to observe this variability. Fruits rot most quickly; then greens, followed by USOs, such as potatoes, and lastly, seeds and nuts. Bark is the slowest rotting plant tissue and is not usually composted. But the rot that occurs in a typical compost pile is largely aerobic and the fermentative component is small.

Bokashi is an East Asian method of composting recently adopted in the West.  Bokashi is quicker than traditional composting because it is completely fermentative. Traditionally, the raw plant material is buried in soil and the native LAB that reside there do the fermentation. Sometimes pits were dug to accommodate the compost. Both methods serve to reduce exposure to air. Today bokashi is conducted in sealed containers and seeded with LAB. Modern bokashi resembles ensilage, the process by which grasses and alfalfa are fermented for animal feed. Silage is far more nutritive than traditional hay and other fodder, markedly increasing meat and milk production. The end products of both bokashi and ensilage are moderately acidic.

From the outsourcing perspective, bokashi has ancient roots and silage was originally meant for human consumption. This is certainly not the received view, according to which fermented foods weren’t consumed prior to systematic food storage, which post-dated farming. Amato, however, argues that only rudimentary storage or caching was required for acidic fermentation and it began at a time far beyond the event horizon of current archaeological methods.

Some fermented foodstuffs, notably fruits, can be directly foraged and don’t require any storage. Certain leafy greens seeds could also be directly foraged in various states of fermentation. But temporary storage would be a more reliable way to obtain these plant materials in a fermented state. The fermentation of USOs would certainly require storage. Amato argues that Ardis and Australopiths were capable of the kind of storage required to ferment USOs.

This would not require any premeditation, initially. Fermentation is an inevitable byproduct of storage but so are other forms of rotting. Fermented plant foods from early, rudimentary food storage needed to be distinguished from the spoiled stuff. The taste and odor of sourness would be an easy way to make this distinction. The next step would be to increase the probability of the good kind of rotting. Burial would suffice. The transition from inadvertent to deliberate fermentation was probably gradual. We have no way of knowing when that transition occurred; the evidence is inherently elusive given the current state of archaeology. The new field of molecular archaeology may eventually provide answers.

Two behavioral attributes are required for foragers to conduct deliberate storage. One is delayed gratification, something chimpanzees utterly lack. It also requires a degree of cooperation and sharing of pooled resources that is foreign to chimpanzees. Bonobos are better in this respect but still a long way from human levels of cooperation. We have no way of knowing how cooperative Ardis were. Australopiths, though, were assumed to be highly cooperative by most anthropologists.

Gastrophagy

There was another source of fermented plant material available to even our most carnivorous ancestors. This was a novel way of outsourcing fermentation by exploiting external gut microbiomes. By external gut microbiomes, I mean the gut microbiomes of other animals.

As in humans, the gut microbiomes of any plant consumer ferment the plant material. Those mammals that rely on plants exclusively, called herbivores, have especially efficient fermentative gut microbiomes. For some herbivores, such as rabbits, horses and elephants, most of the fermentation occurs at the back end (colon or cecum), as is the case in humans. This is called hindgut fermentation.  In other herbivores, fermentation occurs at the front end (stomach); this is called foregut fermentation. Those foregut fermenting herbivores called ruminants (cattle, deer, antelope, goats and sheep) are especially adept because of their complex stomach, which consists of four distinct parts. One of these parts, the rumen, is devoted to lactic acid fermentation.

There is now ample evidence that human foragers routinely harvest the guts of both foregut and hindgut fermenting herbivores for plant digesta in varying states of fermentation. This is especially true of ruminants, but even the guts of rabbits, porcupines, and ostriches are exploited in this way. The practice is called gastrophagy. Herbivore guts provide ready-made fermented plant material. Gastrophagy is a way to ingest nutrients from plants that are otherwise undigestible, especially those, like grasses, which require a specialized physiology that we omnivores lack.

Gastrophagy is practiced by contemporary foragers in all climates, from the tropical to the arctic. It is especially well documented for the Hadza of Tanzania. Hunters quickly extract the entire gut of any fresh kill and often consume it on the spot, still steaming. Northern foragers especially benefit from fermented plant digesta, because of the paucity of plants where they live. Pleistocene Neanderthals and Modern Humans would have found large ruminants a welcome source of pre-digested plant material.

Modern northern foragers continue to exploit herbivore guts. The springtime gut contents of caribou are preferred in the Arctic and Subarctic because the plant material consumed by the caribou is at its most nutritious at that time of year.  It also tastes best according to the human consumers. But the caribou gut contents are most valuable In the Arctic winter when there is little in the way of plant material outside of a lichen, misleadingly called reindeer moss. Like all lichens reindeer moss consists of a fungal matrix in which green algae reside, a remarkable symbiosis. It is much more difficult for the caribou to extract nutrients from reindeer moss than from pure plants because the fungal component of the lichen has cell walls made of chitin, the same material responsible for the hard exoskeleton of lobsters. Even ruminants can’t deal with chitin. Caribou only eat reindeer moss as a last resort when nothing else is available.  The algal component of the lichen is where the nutrition lies for the reindeer but in the raw state it is just as indigestible for humans as the fungal component. After it has been fermented in the reindeer rumen, however, the algae provide a welcome source of plant nutrients when harvested from a reindeer kill.

The meat of reindeer is often deliberately subjected to acidic fermentation as well. A different suite of lactic acid bacterial species are involved in this process, which I will discuss in the next post.