The Model and its Components: The bioenergetic model we offer combines two sets of data. The first concerns the notion of obligatory animal fat consumption as found in the literature and our own calculations. The second concerns the role of elephants in human diet and a comparison of faunal data from two Middle Pleistocene, Acheulian and Acheulo-Yabrudian sites in the Levant.

The Obligatory Animal Fat Dietary Model

The ongoing increase in human brain size{Average human encephalization quotient (actual/expected brain mass for body weight) is slightly over 6.0, compared to values between 2.0 and 3.5 for hominids and primates [46]} had its toll: it became the most metabolically energy-expensive organ in the human body, consuming 20–25% of the adult and 70–75% of the newborn metabolic budget [47]. In order to not exceed the human limited “energy budget” (dictated by basal metabolic rate), shrinkage in gut size (another metabolically energy expensive organ) was a necessary accompaniment. It was Aiello and Wheeler [2] who suggested that gut size was a constraining factor on potential brain size, and vice versa. A shorter human gut, henceforth, had evolved to be more dependent on nutrient and energy-dense foods than other primates. The more compact, the human gut is less efficient at extracting sufficient energy and nutrition from fibrous foods and considerably more dependent on higher-density, higher bio-available foods that require less energy for their digestion per unit of energy/nutrition released. It would therefore appear that it was the human carnivorousness rather than herbivorous nature that most probably energized the process of encephalization throughout most of human history [2], [48], .

The physiological ceiling on plant food intake. The intake of plant foods can conceivably be limited due to a physiological ceiling on fiber or toxins intake, limited availability, or technological and time limitations with respect to required pre-consumption preparations, or a combination of these three factors. A significant contribution to the understanding of the physiological consequences of consuming a raw, largely plant-based diet was made by Wrangham et al. [17], [18]. A physiological limitation seems to be indicated by the poor health status of present-day dieters who base their nutrition on raw foods, manifested in sub-fecundity and amenorrhea [17], [18]. Presumably this limitation would have been markedly more acute if pre-agriculture highly fibrous plant foods were to be consumed. Limited availability is manifested by the travails of the obligated high-quality diet consumer of the savanna, the baboon. Baboons are somewhat similar to humans with respect to their ratio of colon to small intestine rendering the quality requirements of their diet comparable to an extent to that of humans. Baboons have been documented at times as devoting “almost all of their daylight hours to painstakingly seeking out small, nutritious food items….[the] adult male baboon (Papio cynocephalus) may pick up as many as 3000 individual food items in a single day” ([59]:103). Nuts, or other high-quality foods of decent size appear only seasonally above ground in the savanna and such is the case in the Levant, too. But not only are they seasonal, they also require laborious collection and most of them contain phytic acid that inhibits the absorption of contained minerals. These foods also contain anti-nutrients and toxins such as trypsin, amylase and protease inhibitors as well as tannins, oxalate, and alkaloids the elimination of which can only be achieved (sometimes only partially) by pre-consumption processing like drying, soaking, sprouting, pounding, roasting, baking, boiling and fermentation. While these technologies are extensively used, mostly conjointly, in present day pre-consumption preparation of many plant foods, some were probably not practiced by H. erectus, especially those requiring accumulation and storage of produce for weeks (see, for example, [60]:173 with respect to Mongongo nuts, or [61]:31 regarding Baobab seeds). Comparing food class foraging returns among recent foragers, Stiner ([62]:160) has found the net energy yield of 3,520–6,508 kj/hour for seeds and nuts compared to 63,398 kj/hour for large game. Roots and tubers returns are not better, ranging from 1,882 kj/hour to 6,120 kj/hour. These numbers point to the substantial time investment required in gathering and preparing plant foods for consumption. Some researchers (e.g., [63], [64]) suggested significant consumption of underground storage organs (USOs), such as tubers and roots that are not easily accessible to animals, as a possible source of high-quality plant food for early hominins in the savanna. Conklin-Brittain et al. [65] used fiber content as the principle measure defining a diet's quality. Fibers, they claim, displace nutritious elements in limited food digestive capabilities while also trapping additional nutrients within their matrix. Consequently and in view of their relatively low fiber content (16% of dry matter compared to 34% for fruit, 46% for seeds and 44% for pith), these researchers propose significant consumption of USOs by the australopithecines. In their view, “post-canine megadondtia and low rounded thick enameled cusps are all compatible with the physical challenges imposed upon dentition by the consumption of USOs … robust gnathic architecture … [is also compatible] in keeping with the heavy chewing that would have been required to comminute USOs” ([65]:66). None of these features were preserved in H. erectus [66]. In other words, H. erectus was not well equipped to consume USOs, even as a fallback diet. Moreover, analysis of H. erectus cranial features in comparison to those of H. habilis, shows gracilization of the jaws, increased occlusal relief, and reduction in post-canine tooth size indicating a continued emphasis on the shearing of food items during mastication and a reduction in the hardness of foods consumed [67], [68]. Dental analysis thus led Ungar ([69]:617) to determine that “meat seems more likely to have been a key tough-food for early Homo than would have USOs”. It thus seems that the attractiveness of USOs as a source of high-quality nutrients would have been limited and that USO processing capabilities were diminished with the apparent evolution of the early Homo cranial and gut features. One way to handle this dietary challenge, as proposed by Wrangham et al. [17], [18] would have been by cooking. However, with respect to early Homo, this is not a likely suggestion and while some have recently claimed that the habitual use of fire emerged only some 400 kyr ago [22], [23], [24], [25], [70] other very recent statements argued in favor of an even later adoption of fire [71]. However, even where the habitual use of fire is known to have existed, it does not seem to lead to high consumption of plant-based foods among Paleolithic populations. Nitrogen (δ15N) isotope studies of H. sapiens in Upper Paleolithic Europe, where control of fire is clearly evidenced, demonstrate a diet rich in animal content rather than vegetal foods [72], [73], even in relatively temperate climates boasting extensive vegetation, such as France, Italy, Romania, and Croatia ([74]:252). Notwithstanding, isotope studies may underestimate consumption of plant foods low in protein such as tubers. Similarly, modern hunter-gatherer (HG) groups, despite having access to fire and metal tools, also seem to have a strong preference for carnivorous foods over vegetal foods ([53]:682), a notion also supported by a recent study [75] that emphasizes limited consumption of carbohydrates by present day HG groups. Indeed, an analysis of nine HG groups for which detailed dietary information exists ([76]:166) shows that five groups, located in an area abundant in vegetation, consumed only a meager amount of plant foods (17% of calories on average). Availability of fatty plant foods like Mongongo nuts, Palm oil, and Baobab seeds is associated with the groups that exhibit high vegetal consumption. Speth ([4]:87–107) describes the preference of several present-day African tribes to hunt and exclusively consume large animals even in the midst of the most nourishing vegetal season. Speth attributes this tendency to cultural or even political motives, an interpretation with which we do not concur (see also [50]). Recent support for the insignificant role of USOs in Paleolithic human diet may be derived from genetic data of present populations. Hancock et al. ([77]:8926) report that the strongest signals of recent genetic adaptations in the human genome of modern populations heavily dependent on roots and tubers, were to starch, sucrose, low folic acid contribution, and the detoxification of plant glycosides (found in tubers). The need for such an adaptation to so many specific USO attributes implies that humans were not previously adapted to consume significant quantities of USOs or any other form of dense starches for that matter. Similarly, Perry [78] reports that an increase in copies of salivary amylase gene (AMY1) begun to appear in humans probably only within the past 200 kyr. Needed to convert starch into glucose, chimpanzees have only two copies of amylase while present day humans have two to sixteen copies, indicating that adaptation to high starch consumption was probably not in place during the Middle Pleistocene (and even, as Perry discovered, is still not present in certain present day low starch consuming populations). Another organ that should be examined when gauging the evolutionary route of humans with respect to fiber is the gut. Unlike humans, all herbivores have the ability to convert large quantities of vegetable fiber and other carbohydrates into short-chain fatty acids which they are able to absorb. Microfloral activity (i.e., fermentation) within their gastrointestinal tract ferment fibers and cellulose to produce these short-chain fatty acids. In fact, the natural diet of mammals is a high-fat diet. Therefore, any evidence of disengagement from fiber consumption would manifest itself in the colon. In weight, the human gut is about 60% of that which would be expected in a primate of similar size. This compensatory reduction, allowing for an increase in brain size while maintaining the necessary metabolic rate, stands against the notion of increased fiber consumption ([2]:204) in as much as the reduced weight is mostly attributed to a very short colon ([59]:99), which in H. sapiens comprises only 20% of their (relatively smaller) gut. In comparison, the chimpanzee's (Pan troglodytes) colon comprises 52% of its gut. Aiello and Wheeler ([2]:210) infer that African H. erectus also had a relatively small gut based on the proportions of their thoracic cage and pelvis which are similar to those of H. sapiens.

Using teeth data to gauge the physiological ceiling on plant consumption. The need for an evolution of a coordinated digestive system, including both the teeth and the gut is described by Lucas et al. ([79]:35). Acting in concert, a coordinated effort is required to ensure flow from the molars to the gut that would not translate to an avalanche of fibrous food. These researchers' note, in regard to the evolutionary responsiveness of the teeth's shape and size, that the use of “any part of the body for 3000 times a day is unlikely to escape selection pressures” ([79]:39). To estimate the physiological limitation placed on the digestion of raw fibrous foods, we thus use McHenry's megadontia quotient, or MQ [5], [67]. MQ takes into account postcanine tooth area in relation to body mass. McHenry himself states that the MQ index was not meant to be precise, however it offers a noted sensitivity, ranging from 0.7 to 2.7 (see Table 1), and showing distinguished values of 0.9 for H. sapiens and 0.7 for the highly carnivorous H. neanderthalensis [73]. Reduction in teeth size can be attributed to either a change in diet or the use of exogenous food preparation techniques through the use of tools. It is therefore logical to start our comparison with the earliest tool-using hominin, the H. habilis. It is remarkable that the MQ (1.9) of H. habilis is closer to that of the Australopithecines and, by average, is nearly double that of the genus Homo as a whole. Given that H. habilis and H. erectus sought food in comparable savanna environments, the difference in diet, as seen from the point of view of molar size and topography, is quite extensive. In order to get an initial estimate of a plant food ceiling we assumed a modest 10% animal diet for H. habilis (MQ = 1.9) and 80% animal diet for H. neanderthalensis (MQ = 0.7) as two extreme points. Assuming linear relation of MQ to Y – the percentage of plant food ceiling – allows the formation of a linear equation Y = 0.583MQ-0.208. The estimate for H. erectus (MQ-1.0) is thus 37.5%. We find this number to be slightly high in view of the HG record, the δ15N isotope studies, the genetics record, and a reasonable estimate of the physiological, inventory and time limitations for raw, non-cooked, plant foods such as USOs, nuts, and seeds. We have decided however to use this result in our following calculations, with the aim of maintaining strict assumptions. For H. erectus, whose DEE is estimated at 2704 calories (see Table 2 and Table S1), we reach a maximum long-term plant protein ceiling of 1014 calories. This level of vegetal consumption means that H. erectus was indeed an omnivore whose diet was significantly varied (e.g., [80]).