Food Science and Technology Bulletin (May 25, 2007) 4, 1-8 
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Prebiotics in Ancient Diet

Abstract

While modern studies continue to expand our knowledge of the health benefits of prebiotics, virtually nothing is known of their use among ancient populations. Drawing on select ethnographic and archaeological data, examples of prebiotic use in ancient diet is presented. By utilizing well-documented cooking facilities found throughout the archaeological record of North America used to cook inulin-bearing plants as a proxy, prebiotic consumption is documented in Europe and the Mediterranean possibly as early as 40,000 years ago. Data is further provided to suggest that early members of the genus Homo had ample ecological opportunity to include prebiotic underground storage organs found throughout the arid African savannah into diet as early as 2.5 million years ago. This cursory view into the nutritional past of our ancestors reveals that prebiotics were likely consumed in quantities higher than seen among modern humans.

Keywords: prebiotics, evolution, archaeology, nutrition, cook-stone technology

Introduction

            Since the 1970s, there has been renewed interest between colonic function and human health (Jenkins et al.1999), with much recent attention being given to prebiotic carbohydrates that are not available for the vertebrate digestive system in general and for the human digestive system in particular and as such are completely available for the abundantly present intestinal bacterial ecosystem. Prebiotics interact in a selective way with the intestinal ecosystem and tend to change it’s composition with potential positive health effects for its consumer (Gibson and Roberfroid1995; Gibson et al. 2004; Van Loo 2005). The well-established ß(2-1) fructans inulin and oligofructose continue to drive much of the current research on the health benefits associated with prebiotics (Roberfroid 2002; Van Loo 2004a, b). Although much current research is aimed at demonstrating health benefits for modern populations, and mechanisms for delivering them safely into the food supply (Franck 2002), very little is known about the consumption of inulin-type fructans throughout human history.

            This paper briefly reviews archaeological evidence for prebiotic consumption in southern North America and select regions of the world. As a component of human health, it is useful to consider the evolutionary role of natural prebiotic foods from the perspective of nutritional ecology (Leach et al 2006a, b). This is defined as the study of essential nutrient intake for the purpose of overall human health, growth and maintenance, and general trends towards population growth (Jenike 2001; Jenkins et al.1999). In other words, a diverse and sufficiently nutritional human diet will result in sustained or improved human health patterns as revealed by lower infant mortality and extension of human life expectancy.       

            The time-depth afforded by archaeology is unique in that it provides a window into the dietary and other environmental variables that have shaped our current genetic makeup and its nutritional parameters. Significant nutritional (agriculture) and technological (industrial revolution) changes in the last 10,000 years occurred too recently on a genetic time-scale for our genome to adjust (Cordain et al. 2002; Eaton et al. 2002 ; Goldsmith 1993; Williams and Nesse 1991). Thus, modern populations are selected biologically and physiologically for an evolution-based diet that did not include many of the popular foods that currently dominate intake. As such, the nature and composition of the modern gut microflora is in discordance and progressively divergent from our original, genetically determined composition. 

Evolution-based Nutrition and Nutritional Ecology

            Humans require a diverse diet of nearly fifty essential nutrients for proper growth, metabolic function and cellular repair (IOM 2002). Current nutrient requirements and physiology have been conditioned by selective pressure and adaptability played out on an ever changing nutritional landscape spanning millions of years. Fossil evidence places the earliest members of our genus (Homo) at ~ 2 million y ago (Finlayson 2005; Wood 2002). Throughout much of our history (>99%), humans evolved on a diet that was void of dairy foods, margarine (separated fats), cultivated cereal grains, and refined sugars, all of which supply as much as 60 to 70% of the calories in many modern diets. Up until ~500 generations ago, all humans consumed plants and animals foraged from their environment, and consumed virtually no agricultural grains, nor processed foods. Our evolution-based hunter-gatherer diet was high in fiber (dietary and functional), lean animal protein, polyunsaturated fats (omega-3 [ω-3] fatty acids), monosaturated fats, vitamins, minerals, phytochemicals, antioxidants, and low in sodium (O’Keefe and Cordain 2004). Astonishingly, ‘semi-modern’ hunter-gatherers and less westernized groups that adhere more closely to this ancient diet and lifestyle than to more westernized diets, are largely free of chronic degenerative diseases (Cordain et al 2002; Shephard and Rode 1996) and biomarkers of illness such as rising blood pressure, increasing adiposity, and insulin resistance (Blackburn and Poineas 1983; Glanville and Geerdink 1970; Joffe et al. 1971; Kuroshima et al. 1972; Merimee et al. 1972; Spielmann et al. 1982).

            Though traditional hunter-gatherer diet and lifestyle vanished in its ‘purest’ form in the early 20^th century (Murray et al. 2001), ongoing studies of diet and lifestyle among less-westernized groups still remaining throughout the world are demonstrating that models of optimal nutrition (therapeutic diets) may be developed from these extant evolution-based diets. Within the medical community (Eaton 2007; Eaton et al. 2002), there is a slow but significant movement towards acknowledging that a conceptual framework for preventing diseases of affluence may be built upon a foundation constructed within evolutionary theory. At the core of this theoretical movement, often referred to as Darwinian medicine (Stearns 1999; Trevathan et al. 1999), is the idea that our current genetic pool was shaped by millions of years of natural selection in environments very different than the ones we live in today and that much of our genetic makeup is based on a nutritional landscape that did not include foods that currently dominate our westernized diet. The discordance between the rapid pace of our recent (last 10,000 yrs) cultural adaptations (agriculture, food processing technology) is far outstripping our biological (genetic) ability to keep pace.

            While some single-gene mutations (e.g., against malaria) are examples of the speed at which natural selection can occur, the pathophysiology of many chronic diseases involve many more genes and much greater periods of time to evolve (Sing et al. 1996). While we are culturally and socially modern, driving around in hybrid cars, we are literally and biologically ancient hunter-gatherers.

            Our modern requirements of a great number of essential nutrients to sustain health and well-being suggest this pattern developed early in our ancestral history. Humans, along with other extant hominoids (apes), evolved from a common plant-eating ancestor some five to ten million years ago (Milton 1999). While orangutans, gorillas, and chimpanzees have evolved on a diet mainly of fruits, leaves, flowers and bark, humans developed a dietary path that allowed for cerebral growth, gut anatomy, and digestive kinetics based on a mixed diet of plants and animals. It is this diverse diet, and our ability to optimize it through intensification and technology, that makes us unique among all mammals.

            Due to poor preservation of food remains in the archaeological record, it is difficult to derive exact macronutrient levels of food intake in a given diet for a specific region. However, field studies of the few remaining hunter-gatherer and foraging groups carried out during the early and mid-twentieth century provide some insight into the likely range and variability of our ancestral, evolution-based diet. In a comprehensive review of the ethnographic data on 229 hunter-gatherer and forager groups from all over the world, Cordain et al (Cordain 2000) suggest the typical hunter-gatherer diet derived as much as 45-65% of total energy from animal food whenever and wherever possible, but that plant-to-animal ratios ranged from 35:65 to 65:35, depending on environment, season, and latitude.

            Clearly, no single diet characterizes the ‘typical or best’ hunter-gatherer, and by extension ancestral, diet. Humans can, and do, thrive on a variety of diets. For example, the Australian aborigines are known to have eaten some 300 different species of fruit and 150 varieties of roots and tubers (Brand-Miller and Holt 1998; Gould 1980), while Alaskan Artic Eskimos are famous for a diet almost exclusively of raw fat and protein from marine mammals (Ho et al. 1972).

            In the 5-7 million years since bipedal primates appeared, nearly 20 species within the taxonomic tribe hominin have been identified in the fossil record, with only modern Homo sapiens sapiens still standing (Finlayson 2005; Wood 2002). At 6 billion strong, modern humans are clearly well-adapted and successful. Within nutritional ecology, the physical and biological success of our species, coupled with our genetically predetermined nutrient requirements and digestive physiology, indicate that a diverse diet of essential nutrients characterized much of our history. As a cornerstone of modern health and nutrition, diverse diets are known to result in lower rates of infant mortality and increased life expectancy (IOM 2002; Shuman 1996), both of which have significant impact of population demographics.

            Support for our diverse diet is found in the ethnographic and historical accounts among the ‘relic’ hunter-gatherer and foraging societies discussed above. The nutritional ecology approach suggests, due to their wide-spread occurrence among the worlds flora and direct evidence in the archaeological record, inulin-type fructans played an important role within a suite of essential nutrients in long-term health and ultimate demographic success of our species.

Prebiotics in Ancient Diet

            The occurrence of the storage carbohydrate fructan in a significant portion (>36,000 species) of the world’s flora (Hendry 1987) all but guaranteed that the now well-studied prebiotics inulin and oligofructose were consumed by our Pliocene and Pleistocene ancestors millions of years ago. As our early ancestors moved from the rainforest to the parched savanna-woodlands of subtropical Africa, subsurface tubers, rhizomes, corms, and perennial bulbs, many rich in prebiotics, would have been a ready and important source of energy (Hatley and Kappelman. 1980; Laden and Wrangham 2005). Today, many of these same resources serve as staples for the modern foragers and farming groups still inhabiting the same subtropical environs (Murray et al. 2001; Vincent 1985). However, digestion-inhibiting compounds and plant toxins present in many below-ground food sources would have limited their role as staples in early diet of Homo until technological adaptations, such as fire, were introduced (Ragir 2000; Stahl 1984). Nevertheless, as early members of the genus Homo began their evolutionary march to mammalian dominance, the inclusion of prebiotics within a diverse and mixed diet would have no doubt conferred a selective advantage for the consuming population. As the archaeological evidence reveals, prebiotics have long been part of the human diet and in quantities for some areas and time periods that far exceed those currently consumed by modern populations (Van Loo 1995).

            The physical evidence for plant consumption by our early ancestors is virtually nonexistent, owing to poor preservation of organic plant parts in the archaeological records, though stable isotope analysis of skeletal remains of early hominids are providing some insight into the quality and diversity of early diet (Lee-Thorp et al. 1994; Richards et al. 2001). For adequate preservation of prebiotic food evidence in early human diet, we must travel millions of years forward to the Upper Paleolithic (~40,000 to 12,000 years ago) of Western Europe and the Mediterranean Basin and to the Early Holocene (~10,000 years ago) of North America before significant direct and indirect evidence of prebiotic food consumption becomes evident.

            Decades of large-scale archaeological research in North America has documented extensive exploitation of prebiotic rich plants such as agave (Agave spp.), sotol (Dasylirion spp), camas (e.g., Camasia quamash, C. leichtlinii), and wild onion (Allium spp.). While a great number of inulin-bearing plants were known as food sources among the prehistoric and historic groups of North America (Wandsnider 1997), these particular plants by far provide the oldest evidence of prebiotic consumption in North America, dating back over 9,000 years.

            In the Lower Pecos Region of the Chihuahuan Desert in west Texas along the US-Mexican border, deeply stratified cave deposits document the use of agave, sotol, and onion that date back nearly 9,500 years. Kept dry and preserved by the large overhangs that characterise many of the caves and shelters of the region, an extraordinary collection of human coprolites and preserved macro botanical plant remains suggest that pit-baked prebiotic foods (e.g., agave, sotol, onion) were a mainstay of this desert economy (Sobolik 1990).

            East of the Lower Pecos on western edge of the Edwards Plateau in central Texas, the deeply buried Wilson-Leonard site has produced a 2 meter diameter rock-lined  earth oven used to cook the nutritious onion-like bulbs of camas (Camassia spp.). Charred camas bulbs recovered during excavation of the oven produced a date of ~ 8,200 years before present (Bousman et al. 2002). Though no charred bulbs of camas were recovered from deeper excavations, “stone-lined hearths” underlying the camas oven were dated to ~ 9,410-9,990 years before present, hinting at possible earlier evidence of prebiotic use.

            At the Stigewalt site in southeastern Kansas, remains of large (> 2 m diameter), rock-filled earth ovens with charred onion (Allium spp.) bulbs dated ~ 8,810-7,910 years before present (Thies 1990). As with the large oven at the Wilson-Leonard site in Central Texas, the occurrence of hand-excavated pits lined with pre-heated stones, seem to be consistently associated with the cooking of prebiotic foods. This same pattern continues throughout the American Southwest, where thousands of agave roasting pits (also known as mescal pits) are scattered about the landscape (Leach 2005). Similarly, in the American northwest, large, rock-lined ovens were used to cook as much as 1,500 kgs of inulin-rich camas bulbs in a single firing event (Thoms 2003). 

            The reoccurring use of large, rock-lined earth ovens, which are often associated with cooking of inulin-rich plants (Wandsnider 1997), is well-documented in the historical and ethnographic records for North America and northern Mexico. For example, Castetter et al. (Castetter et al. 1938) describe cooking agave in pits among the Mescalero and Chiricahua Apache of the American Southwest:

Pits in which the crowns [agave] were baked were about ten to twelve feet in diameter and three or four feet deep, lined with large flat rocks... Upon this, oak and juniper wood was placed, and before the sun came up was set on fire. By noon the fire had died down, and on these hot stones was laid moist grass, such as bunch grass... The largest mescal crown was selected... they threw it in and threw the other crowns after it... After the  mescal [agave] had been covered with the long leaves of bear grass and the whole with earth to a depth sufficient to prevent steam from escaping.

            In the American Southwest, ideal surface conditions and slow rates of soil accumulation, accompanied by repeated use of oven facilities and subsequent accumulation of oven debris (discarded cooking stones) over multiple seasons, has made it possible to map thousands of cooking facilities, which often reach over 1 meter in height and cover areas tens of meters in diameter (Leach et al. 2005). Synthesis of hundreds of radiocarbon dates from cook-stone facilities across extensive areas of southern North America (Leach 2005) has revealed a steady increase in prebiotic food consumption beginning over 9,000 years ago, culminating in substantial intensification around 1,250 years ago. The intensification of prebiotic foods in southern North America (specifically the American Southwest) coincides with increased reliance on cultivated crops such as corn (Zea mays), squash (Cucurbita sp.) and beans (Phaseolus sp.) and large-scale growth in human population. Therefore, while populations were making the transition to a diet heavily dependent on starchy cultivars, prebiotic foods played an important and often increasing regional role in a diverse nutritional economy.

            As we see in North America, the occurrence of cook-stone technology, in the absence of recoverable plant remains, may be used as a proxy indicator to the exploitation of prebiotic foods in the archaeological record. While a great number of foods are known to have been processed with cook-stone, the occurrence of large (>1 m diameter), ovens are consistently associated with many prebiotic foods (Leach 2005; Wandsnider 1997).

            Throughout Western Europe, similar remains of massive cooking facilities are known to occur in Wales, England, Scotland, Ireland, and Scandinavia. Referred to locally as fulacht fiadh,  recent urban development has led to the excavation of a number of these mounds, which can reach over a meter in height and several meters in diameter, representing dozens, if not hundreds, of individual oven events. While moist ground conditions have all but destroyed any evidence of the plants that may have been processed in these features, radiocarbon dates on small amounts of carbonised wood charcoal from initial heating of cook-stone indicate the majority of mounds were constructed within the last 6,000 years.  Similar cook-stone mounds of varying sizes, dating roughly within the same time period, are known in southern parts of Australia (Holdaway et al. 2002). As seen for North America, historical and ethnographic accounts of using large, hand-excavated pits and heated cook-stones is noted throughout Australia. In one example, between 1884 and 1850 British explorers observed the following among the people at Menindee on the Darling River;

The oven is a hole dug into which are placed stones; a fire is then made and when the stones are become sufficiently hot, whatever fibrous things they eat, or animal, is put into this oven and covered over and a fire made over it, when it soon gets cooked (Brock 1988).

            Among the 800 plus plant foods known to have been eaten for tens of thousands of years by Aborigines in Australia (Brand-Miller and Holt1998), many were tuberous roots and corms that contained prebiotic inulin (Van Loo 1995) and required prolonged cooking in rock-lined pits (Gott 1982; Gould 1980; Incoll et al. 1989).

            By far the oldest known evidence of cook-stone technology (ovens) in Europe comes from the cave site of Abri Pataud in the Dordogne region of southern France. In excavations by a joint American-French team between 1958 to 1964, a series of cook-stone features, some greater than 1 meter in diameter, were dated to ca. 33,000-18,000 years ago (Movius 1963). While it is impossible to know if prebiotic plant tissue was processed in these ancient features, as no direct evidence in the form of plant material was reported, their use in cooking vegetal material is inferred from the overwhelming evidence of similar features recorded throughout the world.

            In one final example (Thoms 2003), among the more ancient cook-stone features are those recently excavated at the on the southern Japanese island of Tanegashima in fine-grained tephra-rich sediments and between lenses of well-dated volcanic ash (Dogome 2000). The oldest two features are buried 10 cm below a layer of Tane-4 volcanic ash, which is radiocarbon dated to about 30,500 years ago. One is a sandstone lens about .75 m in diameter and the other is a sandstone-filled basin about 1.15 x .75 m in diameter that is underlain by carbon-stained sediment. Thermally altered sandstone ranges in size from a few cm to 25 cm in maximum dimension. Similar cook-stone features and fire-cracked rock scatters were found in overlying deposits dated as late as 6500 years ago, and including several features associated with 12,000-year-old Incipient-Jomon pottery. Investigators concluded the Late Paleolithic cook-stone features and heavy stone tools were indicative of a plant-based diet (Dogome 2000). These cook-stone features, especially the basin-shaped forms, closely resemble remains of earth ovens found throughout western North America used to cook inulin-rich plant tissue (Leach 2005).

            Whereas our ancestors consumed large amounts of inulin-containing crops, it could be questioned whether the heat treatment by means of cook-stone ovens or other would not destroy the inulin present in these plants. Direct tests in conditions mimicking cook stone ovens have not been done to date. In Louisiana and in Northern Europe inulin containing chicory roots are roasted. The roots are spread on grids that are stacked in a particular building. Hot air that is generated by burning wood or coal is led through the roots, thereby heating them up to a temperature of 180°C (356°F). It was observed that under these conditions between 10% and 20% inulin was degraded (Pazola and Cieslak 1979; Van Loo 1995). In cooking or frying experiments with inulin containing food plants such as onions, it was show that the losses of inulin were limited to 10% or less. From these observations it can reasonably be concluded that the heat treatment in the cook-stone ovens (<100°C, products not immersed in water) preserved the inulin content of the food plants very well, with expected losses of less than 10%.

Discussion

            From the current discussion it is clear that our distant ancestors consumed, in varying quantities, plants containing prebiotic carbohydrates. These by definition are not digested in the upper intestinal tract and interact in a specific way with the bacterial ecosystem which is abundantly present in the lower intestinal tract. Consumption of prebiotic carbohydrates such as inulin selectively promotes the growth of bacteria that are associated with a healthy condition (e.g. lactobacilli, bifidobacteria) and suppress bacteria that are associated with disease (clostridia, etc.). At the same time the metabolic activity of the bacteria is stimulated, which results in the production of metabolites that are absorbed in the blood and exert beneficial effects in the rest of the body with as a direct consequence: improved resistance to infection, better skeletal bone quality, reduced risk for chronic diseases such as cancer, cardiovascular disease etc. (Van Loo 2004a, b, 2005).

            The interesting association between cook-stone technology and prebiotics offers some proxy of initial intensification, in the absence of direct recovery of prebiotic plant tissue. Further, the durability of many of these cook-stone features makes their identification and possible utility in recognizing large-scale patterns of prebiotic use across space and time feasible through inductive principles of investigation. We suspect, that while our ancestors have always included amounts of prebiotic plants in their diet through daily foraging activities and that some evidence for use of cook-stone is present during the Middle Paleolithic (Mellars 1996), it was not until the onset of  the Upper Paleolithic (~40,000 years ago), with its ornaments, decorated tools, deliberate storage facilities, crudely tailored clothing, art, and clear demographic pulses (Steiner 2002), that prebiotic plant foods began to play an increasing role in the dietary evolution of our species.

            Increased demographic pressure resulted in shrinking territories, making access to preferred plants and high-return animal and aquatic resources, less reliable. It is under this cultural pressure that initial intensification (increased diet breadth) of under utilized below-ground resources (tubers, bulbs), many rich in prebiotics, possibly took place. This form of land-use intensification (Holly 2005; Thoms 2003) was the beginning of a long-term, albeit punctuated, prebiotic revolution made possible by the adaptation of cook-stone technology. The evolutionary implications of prebiotic consumption on the development and relative success of our species is unknown, and requires further research. However, advances in processing technology, brought about during the industrial revolution in the late nineteenth century, in conjunction with the increase in “westernized diets” and its accompanying medical maladies, have forever altered the delicate evolutionary-induced balance between food and human health, thereby resetting our metabolic and genetic clocks.

            The concept of prebiotic food ingredients is an important development in nutritional research. Beyond local effects, the idea that prebiotics can selectively modulate gastrointestinal microbial fermentation to influence physiological processes which are known biomarkers of potential illness and human health is profound. However, in the case of even the best-designed human nutrition intervention trial, optimal controls may never be achieved, as the diet and lifestyle of – most likely all – members will differ significantly from their evolution-based and thus genetically determined optimal diet.

            The future of prebiotic  research may be well-served with a better understanding of the essential nutrient profiles that humans evolved on over millions of years of selective pressure and how that relates to intestinal health, as our evolutionary trajectory has arguably been towards maximizing our adaptability – both physically and physiologically (Schlicting and Pigliucci 1998). In other words, our biological and physiological parameters of essential nutrients and their conditioning of human health are, for the most part, predetermined and grounded in our ancient past. Recent genome sequencing of Bifidobacterium longum (Schell et al. 2002) further points to a symbiotic and ancient relationship between our genus and the prebiotic plants on the landscape.

            There is no doubt that the majority of intermediate markers of disease risk and health currently being addressed with prebiotics and modulation of the intestinal flora have, at their source, multifactorial causes (Leach 2007). Evolution has as a consequence that successful living organisms do best in those environments in which they were selected. As a consequence an informed research agenda that includes an evolutionary perspective on ‘ancestral’ parameters of diet and microflora composition may advance the realization and potential of future prebiotic research with its aim of optimum health and nutrition. Through this research agenda, it may be possible to characterize the differences between modern and ancient intestinal health as it pertains to microflora composition, in order to integrate microbiological, nutritional, and epidemiological studies and data into an overarching paradigm that can serve to establish formulations resulting in effective recommendations for consumers.

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Table 1. A sample of inulin-containing plants identified as food among
indigenous populations (adapted from Wandsnider 1997).

 * Over 300 species of agave have been reported throughout the American Southwest and northern Mexico (Gentry 1982), all of which are thought to contain inulin.