Major And Minor Causes Of Geophagy-Lithophagy In Animals And Humans

About the Terminology

Geophagy

Humans and Animals

One of the first researchers to suggest that the main cause of geophagy in animals and humans might be the same was the Russian geologist P.L. Dravert (1922). P.L. Dravert’s reflections on geophagy are interesting because they were written before the first scientific publications on geophagy in animals, which began to appear only in the 1930s (Mure, 1936; Nasimovich, 1938), and the territorial connection of consumers of earthy substances among humans and at the same time among animals, according to the publications, became clearly visible only in the second half of the XX century, and only in the countries of the equatorial zone.

The analysis of the mineral composition of kudurits, which is presented in detail on the basis of our own research and review of data published in books (Panichev, 1990; 2011), shows that it is similar to the composition of the earth eaten by humans. It is usually the same clay minerals from the kaolinite, smectite, and hydrous mica groups, in some cases with a significant amount of zeolites and carbonates. The primary crystals are the same quartz and feldspars. Among the trace elements, iron and manganese oxides and hydroxides are common, with occasional significant content (more than 1%) of chloride salts or sodium hydrogen carbonates.

Since the first studies of the phenomenon of geophagy in animals, many experts from different disciplines have tried to determine the cause that makes animals regularly ingest earthy substances. However, only a series of hypotheses have been proposed so far, both for animal and for human geophagy. The best known among them are the "sodium" hypotheses: the need for sodium during the periods of lowest sodium intake (Mure, 1936; Stockstad et al. 1953; Staaland, 1980), as well as the need for sodium and mineral sorbents necessary to normalize the electrolyte balance in the digestive tract during periods of seasonal changes in the diet (Kreulen, 1985; Panichev, 1987; Panichev, 1990; Klaus, Schmid, 1998). The second group of hypotheses is about the replenishment of deficiencies of a number of chemical elements in the body (Nasimovich, 1938; Klaus et al.1998; Jones et al. 2000; Mincher et al. 2008; José et al. 2017). The third group is about the use of bacteriostatic properties of clay minerals in the control of pathogenic microflora against diarrhea and intestinal parasites, replenishment of symbiont microorganisms and regulation of pH in the digestive tract (Robertson, 1996; Knezevich, 1998; Abrahams, 1999; Ketch et al. 2001; Wilson, 2003; Banenzoue et al. 2014; Lebedeva et al. 2020). The fourth group is based on the elimination of toxic chemical elements and compounds, including organic ones such as phenols, terpenes, tannins, alkaloids and cyanogenic glycosides from the body with the help of mineral sorbents (Johns, Duquette, 1991; Gilardi et al. 1999; Houston et al. 2001; Dominy et al. 2004; Ekosse et al. 2020). Based on experimental studies, an explanation for geophagy has been proposed as the desire of animals to use clay minerals to influence nutrient assimilation and to protect the intestinal mucosa (Reichardt, 2008). It has even been suggested that geophagy is not related to a physiological need, but to a sense of gustatory pleasure (Krishnamani, Mahaney, 2000; Hladik, Gueguen, 1974).

One of the relatively recent attempts to unify hypotheses on the causes of geophagy in humans and animals is the work of Young et al. (2011), based on the analysis of 482 publications on human geophagy and 330 on animal geophagy. As a main result, it was proposed to explain human geophagy in terms of protection from harmful and toxic substances, parasites and pathogens, while animal geophagy, in addition to such protection, may also be aimed at the absorption of a number of chemical elements, primarily sodium.

In 2015, after analyzing the published data on the geochemistry of earthy substances eaten by animals in different regions of the world (our own and other researchers’ data), as well as taking into account the emerging data on the effects of REE in the body on the nervous, immune, and hormonal spheres, most fully shown in the review by K. Redling (2006), we had the idea that one of the main reasons for the desire for geophagy could be due to the disturbance of REE metabolism in the body (Panichev, 2015; 2016).

In the period from 2020 to 2023, based on the results of special landscape geochemical studies conducted with the financial support of the Russian Science Foundation, we have convincingly demonstrated the relationship between geophagy and REE on the material of studies in a number of regions of southern Siberia and the Far East of Russia (Panichev et al. 2021; 2023a; 2023b).

A reliable connection between mass cases of geophagy and anomalous REE contents in landscape components was first revealed in the territory of the Southern Sikhote-Alin, in the area of the Vanchin graben (the area of the upper Milogradovka River). In this area of about 50 km2 we found 14 places where wild animals (mainly red deer) regularly eat kaolinite and smectite clays in large quantities (kilograms per visit), sometimes with admixture of fine zeolites. As a result of detailed landscape-geochemical studies conducted in the area, we were able to detect anomalously high REE contents, often with a predominance of heavy REE subgroup elements (HREE), in various types of Early Cenozoic volcanogenic rocks, soils, surface waters, vegetation, and even in brain tissues of local reindeer (Panichev et al. 2021). Comparison of the composition of ingested clays and animal feces containing clays showed that clays in the digestive tract actively sorb REE, especially HREE, and remove them from the body. Based on the data obtained, it was concluded that the desire of reindeer to consume clays may be caused by disturbances of REE metabolism in the body due to their high content in feed and drinking water.

We were able to substantiate this conclusion after analyzing the published data on the biological properties of REE. The accumulated experience in the study of the biological properties of REE presented in the literature (Powis at al., 1994; Palasz, 2000; He, Xia, 2001; Jiesheng at al., 2002; Feng at al., 2006; Redling, 2006; Zhao at al., 2012; Panichev, 2015; 2016; Brouziotis et al., 2022), as well as the experience of using this group of elements in animal feeding (Wang et al., 2003; Rambeck et al., 2004; Xun et al., 2014; Tariq et al., 2020), indicate that among these elements, the biologically significant ones are predominantly representatives of the light subgroup (LREE), including: Sc, La, Ce, Pm, and Nd. It seems that among the representatives of HREE only yttrium (Y) performs biological functions in the body. However, all REE without exception can be integrated into biological structures and replace each other, but at the same time almost all HREE except Y are unable to perform the functions required by the body, unlike LREE. Judging by the distribution of REE in the tissues of mammals, critical disorders in the animal bodies may occur in the nervous, immune, and endocrine systems. Thus, we have come to the conclusion that excessive intake of REE into the internal environment of the body may disturb the neuroimmunoendocrine system, which controls all metabolic processes in the body, stimulating animals to consume mineral sorbents in order to regulate the composition and ratio of REE in it. From the point of view of such ideas, the regular consumption of clays is an inevitable necessity for the survival of animals in landscapes with an excess of REE, especially with an excess of HREE. In other words, in this case we are dealing with hypermicroelementosis according to the understanding of A.P. Avtsyn et al. (1991), in which 17 trace elements of the REE group act as the main agent.

Studies in other areas of the Sikhote-Alin (Panichev, 1990; Panichev et al. 2021), as well as in the Altai Mountains (Panichev et al. 2023a), have shown that a wide variety of sorbents are suitable for survival in such landscapes. These may include not only clays of various mineral compositions, but also zeolitic and opal "earths," peat soils, and other varieties of mineral and organomineral sorbents based on diatomites, silica clays, or rotten-stone. According to published data, both animals (Struhsaker et al. 1997) and humans (Chung et al. 2019) can also use purely "carbon-based" sorbents in the form of charcoal. We have recently found that animals can even consume bituminous coal, selecting only REE-enriched varieties (Panichev et al. 2024). Why they do this will become clear in the text below.

In 2022, we conducted detailed landscape geochemical studies on Olkhon Island in Lake Baikal (Panichev et al. 2023b), where the geological and geochemical situation is quite different from that in the Sikhote-Alin and Altai Mountains. Kaolinite clays eaten by wild reindeer and livestock on Olkhon turned out to be significantly enriched in LREE against the background of anomalously low concentrations of this group of elements in all components of the island landscapes. Comparison of the composition of clayey feces of reindeer and the clays eaten by them showed that a part of LREE consumed with clays remains in the body. As a result, it was concluded that the consumption of clays by animals on Olkhon is also caused by disturbances in the composition and concentration of REE in the organism, but against the background of abnormally low content of these elements in feed and drinking water. Thus, in this case we encountered manifestations of typical REE hypomicroelementosis in reindeer. Such endemic metabolic disorders in the bodies of wild and domestic animals should be most common when they live in areas where sedimentary chemogenic and organogenic carbonate rocks predominate, which are known to be characterized by very low REE concentrations (Dubinin, 2006). Meanwhile, REE hypermicroelementoses will be common in the areas of development of magmatic carbonate rocks (carbonatites) characterized by unusually high REE concentrations. These situations are observed, for example, in the territory of the same East African rift system, where REE-enriched rocks such as carbonatites and alkaline basites are known to be widespread. Areas with mass manifestations of geophagy in both animals (Mahaney and Hancock, 1990; Mahaney et al. 1990, 1997) and humans (Annel and Lagerkranz, 1958; Abrahams and Parsons, 1996; Knudsen, 2002) are found there. However, our more detailed study of the landscape-geochemical conditions in this region based on the published data (Panichev et al. 2023b) indicates the possibility of a high contrast in REE distribution in landscapes, caused not only by the contrast in chemical composition of the rocks, but also by the contrast in terrain and climatic conditions.

It should be noted that in the equatorial part of Africa there is almost everywhere a high contrast of REE concentrations in rocks and soils. According to Temga et al. (2021), the total REE content in soils of Cameroon (Central Africa) varies from 0.482 to 5926 mg/kg (5 orders of magnitude difference) with the average value of 297 mg/kg, which is currently the highest among soils in the world.

After the work on Olkhon Island it became clear to us that all areas where geophagy is widespread in mass form are to some extent REE-anomalous, with increased or decreased content of mobile REE forms in landscape components compared to local background values. Some animals living in such conditions, mainly herbivores, to a lesser extent omnivores and carnivores, may suffer from disturbances in the metabolism of this group of elements in the neuroimmunoendocrine system of the body. The hormonal stress that develops in this case most likely triggers the instinctive mechanism of searching for sorbents that, depending on the geochemical conditions of the habitat, are preferred by the animals either in the REE-enriched or in the REE-depleted form. The universal character of the revealed regularities is indicated by our analysis of geological and geochemical situations in a number of regions of the equatorial zone of the Earth, which shows that the connection of mass cases of geophagy with REE-anomalous landscapes in this part of the world is more pronounced than in the middle latitudes, and with a vivid manifestation of REE-endemic diseases in humans.

One such disease is the aforementioned Loeffler endomyocardial fibrosis, which has been shown to be directly associated with excess cerium (Ce) in the heart muscle tissue of diseased individuals (Valiathanet al., 1986), as well as with excess Ce in the plant diet of affected individuals (Eapen, 1998) and in monazite-enriched soils in EMF-endemic areas of India (Kutty et al. 1996). A similar pattern of disease association with REE-enriched soils has been found in Africa (Smith et al., 1998). Our comparison of the areas where EMF diseases are prevalent in Africa according to Bukhman et al. (2008) with the areas where geophagy is historically prevalent among humans according to (Annel, Lagerkranz, 1958) showed good convergence (Figure 1).

In the southern EMF-affected states of India, as well as in Africa, there is an association with areas of animal geophagy. The presence of typical kudurs in Kerala, frequently visited by local ungulates, has been described in particular in the Chinnar Nature Park (Ramachandran et al. 1995), as well as in the Marakkanam Reserved Forest in the neighboring state of Tamil Nadu (Voros et al., 2001). Chinnar Park is located on a mountain plateau with elevations up to 2500 m, composed of metamorphic rocks of Precambrian age, predominantly crystalline schists and gneisses, including charnockite series, enriched in REE, mostly concentrated in monazite (Anitha et al., 2020). From this plateau, rivers flow along the banks and at the mouths of which human biogeochemical endemics have been identified, associated with excess REE in monazite-bearing sands (Kutty et al. 1996). Similar rocks are common not only in the south, but also in the eastern parts of India, i.e. exactly where, according to B. Laufer (1930), geophagy in humans was already widespread at the beginning of the 20th century.

Figure 1. Left – EMF incidence in African countries (Bukhman et al. 2008); right – human geophagy prevalence in Africa (Annel, Lagerkranz, 1958).

Figure 1. Left – EMF incidence in African countries (Bukhman et al. 2008); right – human geophagy prevalence in Africa (Annel, Lagerkranz, 1958).

Previously, referring to the publication of Bukhman et al. (2008), we noted numerous cases of EMF illness in southern China (especially in Guangxi Province). According to Aufreiter et al. (1997), geophagy was common in humans in the neighboring province of Hunan not so long ago. According to Laufer (1930), geophagy was much more widespread in China in the past. In southeastern China, geophagy is also found in animals (Li et al., 2018). At the same time, REE-enriched carbonatite volcanic complexes are common in central and southeastern China, and the world’s largest ion-adsorption-type REE deposit in clayey weathering crusts is located there. That the REE content in soil and products grown on it in China affects human health and longevity is indicated by the REE content in the hair of long-lived Chinese people (Zhang et al., 2020), which is on average 100 times lower than in the hair of people living in areas with high background REE content (Meryem et al., 2016).

It should be noted that the association of endemic diseases with landscape REE anomalies is not limited to EMF. According to Zhu et al. (2005), people living in Jangxi Province in southern China in areas with high background REE levels suffer from gastric disorders and anorexia, with markedly reduced levels of total protein, globulins, albumin, and serum glutamic pyruvic transaminase with higher levels of total immunoglobulin. A paper by Chinese researchers (Liu et al., 2019) also shows that exposure of pregnant women to Ce and Yb leads to lower levels of thyrotropic hormone in infants (this hormone is secreted in the thyroid and epiphysis and largely regulates the body’s growth and development). Henríquez-Hernández et al. (2017) demonstrated that in the inhabitants of sub-Saharan Africa, elevated levels of REE in the blood are somehow related to the development of anemia, since the occurrence of this pathology in them often does not depend on the level of iron in blood. An article by Collignon (1992), citing some researchers, discusses the possibility of a link between geophagy and a blood disorder known as "sickle cell anemia". According to Gómez-Aracena et al. (2006), Ce levels in toenails are associated with an increased risk of acute myocardial infarction. It has also been shown (Zhu et al., 1997) that REE can accumulate in the cerebral cortex with prolonged intake of small amounts from the environment and cause subclinical damage up to oncology. Brain tumor tissue (astrocytoma) has been found to contain significantly higher levels of REE, especially La, Ce, Gd, and Lu, compared to similar normal tissue (Zhuang et al., 1996). Using electron microscopy, we have detected Ce-containing mineral phases in brain tissue from wild deer harvested in an area with high background REE levels in the Sikhote-Alin (Baranovskaya et al., 2024).

In recent years, a number of U.S. researchers have studied unusual pathologies in wild and domestic animals, such as "chronic wasting disease" (CWD), which is associated with atrophy of bone marrow fat and hematopoietic cells (Gilbertson et al., 2022), and "transmissible spongiform encephalopathies", which are associated with damage to the brain and throughout the nervous system (Lavelle et al., 2014; Plummer et al., 2018). This family of diseases, common in both animals and humans, is considered to be caused by misfolded proteins - prions. The term "prion", from fragments of the English words protein and infection, was coined by Stanley Prusiner, who discovered such proteins in 1987. The causes of these diseases remain largely unknown. In wildlife, CWD most commonly affects members of the deer family. In the natural environment, according to the most widespread hypothesis (Plummer et al., 2018), such diseases are transmitted from diseased animals to healthy ones, including at kudurs, when animals eat prion-infected earthy substances. However, it seems to us that the cause of all diseases with prion formation, as well as blood anomalies, which are clearly triggered by the malfunction of the medullary component of the hematopoietic system, is directly related to REE microelementoses. Similarly, this is the main cause of such a neurodegenerative human disease as Alzheimer’s disease.

What is our basis for associating the named diseases with REE elementoses?

As mentioned above, interest in the use of LRE in the fattening of various animals has been actively growing during the last decades. Several researchers (Eisele et al., 1980; He, Rambeck, 2000; Fiddler et al., 2003; Rambeck et al., 2004; Hutchison, Albaaj, 2005) found that only small amounts of mineral forms of these elements are absorbed in the gastrointestinal tract. Nevertheless, due to the apparent ergotropic effects of LRRE supplements, some researchers (He, Rambeck, 2000; He, Xia, 2001) believe that even low doses of LRRE in the blood can cause significant biological effects. The most complete list of biological effects of LREE use that have been identified to date (illustrative in terms of dose dependence) is reported by Chinese researchers (Wang et al., 2003). This list includes stimulation or inhibition of body growth, cell proliferation, apoptosis; antioxidant or pro-oxidant activity; stabilization or destabilization of cytoskeleton; increase or inhibition of cell permeability; positive or negative regulation of cell signaling system; increase or decrease of hemoglobin affinity to oxygen; and enhancement of mineralization or demineralization.

From the brief review of biological effects associated with LREE food supplements, it is clear that the problem of assimilation of such elements in the body is positively solved. However, the mechanism of such assimilation remains unclear.

The fact is that the absorption of metal ions, according to Sullivan et al. (1984) and Kostial et al. (1989), occurs in the small intestine, but not for REE ions. They can only exist in a highly acidified aqueous solution. Once in the intestine, where the pH of the medium rises sharply to 8.0 and above, REE ions are inevitably converted to deionized mineral forms that cannot enter the body. Some researchers (Szasz et al., 1978; Cheng et al., 1999) have suggested that REEs are not absorbed in the intestine in ionic form, but as part of macromolecules capable of penetrating the cell membrane. In support of this idea in general, we propose to develop this hypothesis.

The mechanism of REE entry into the internal environment of the body most likely involves some microorganisms that are able to actively assimilate REE into their protein molecules. Such microorganisms may live in the gastric microbiome, where acidic digestion of food takes place, or in the border area of the stomach and small intestine (in mammals, probably, their maximum number lives in the duodenum). It is possible that assimilation of REE by bacteria occurs not only at the level of amino acids in proteins, but also at the level of DNA. If such microorganisms and products of their metabolism periodically enter the intestine, they decompose there, and REEs in proteins or their components are assimilated by the body. It should be noted that, according to the thesis of A.I. Belyanovskaya (2019), the maximum content of REEs in the tissues of the digestive tract of pigs is found in the large intestine (colon), i.e. exactly there, where the substances synthesized by bacteria are absorbed, including such a fat-soluble vitamin as phylloquinone (Metelsky, 2009), which is necessary for protein synthesis and bone mineralization.

If such a mechanism of REE assimilation exists, it should be universal for all multicellular animals. The specific REE-assimilating microorganisms should include the most ancient representatives, because normal functioning of the earliest multicellular animals would be impossible without them. The most likely candidates for "REE-bacteria" in the microbiome of the digestive tract of animals could be from the group of methanotrophs. Several types of methanol dehydrogenase (MeDH) enzymes have been found in the representatives of this group, in particular in Methylosinus trichosporium OB3b, and the expression of each of them is regulated by different REEs of the light subgroup (Ce, La, Pr, Nd) and sometimes Sm (Gu et al., 2016). Regarding the fact that no significant effect of REEs on the microbial composition in the gastrointestinal tract of pigs, poultry and bovine rumen has been demonstrated during animal fattening, as described in the theses of S. Schuller (2001) and S. Knebel (2004), it can only indicate that the proportion of "REE-bacteria" in the microbiome of the digestive tract of any animal is insignificant both quantitatively and species-wise, and that their localization there is spatially limited.

Since microorganisms participate in REE assimilation in the digestive tract of animals, and specific protein molecules are produced whose expression is regulated by different rare earth elements, it is quite possible that under the combination of some factors, protein molecules with incorrect chirality, i.e. prions, may be produced in the digestive tract.

In evaluating the published information we have collected on human geophagy, it is important to note also that both currently and historically, people practicing geophagy in Europe and the United States are predominantly either African Americans (more often women and children) from the United States itself and other countries in the Americas, or recent immigrants from Africa, as well as from India and Pakistan (Henry, Cring, 2014). All of these individuals come from areas of the world where geophagy was historically prevalent. This fact suggests that the genetic factor (the fixation in the genome of one or another norm of the level of REE content in the body) plays an important role in the impact of landscape REE anomalies on humans and animals. Only this can explain the persistent tendency to geophagy in natives of regions of the world with high levels of REE in landscapes when they move to new places of residence where REE levels differ greatly from their ancestral places. Significant differences in REE levels between human locations are well illustrated by data from Brown et al. (2004). The researchers compared La and Ce concentrations in baby teeth from Uganda and the United Kingdom. Teeth from Uganda had 4 times higher La concentrations than teeth from children in the UK, and Ce concentrations were almost 10 times higher.

Summarizing the review of studies on the relationship between mass geophagy and landscape REE anomalies, we can state with a high degree of certainty that the main cause of geophagy in mammals, including humans, worldwide is due to REE elementosis, which can be caused by both excess and deficiency of REE in feed and drinking water, reaching upper or lower thresholds of their concentrations beyond which the body cannot maintain metabolic processes in normal mode. By positioning the "rare earth" cause of geophagy as the main one, we imply that it is more widespread than the "sodium" cause, which is still the most popular in the scientific community in relation to mammals. As for the other ideas expressed by various authors about the causes of geophagy, we consider them, as well as the "sodium" cause, to be quite reasonable, but of secondary, auxiliary importance. Nevertheless, some seemingly typical kudurs may be visited by animals for the sole purpose of obtaining sodium. A particular craving for sodium is known to be most characteristic of ruminants, in which a large volume of this element is involved in the digestive cycle.

For almost 50 years we have visited and studied dozens of areas with mass manifestations of animal geophagy in the vast expanses of Russia, from the Caucasus Mountains in the west to the Sikhote-Alin Mountains in the east, and from the Verkhoyansk Mountains in the north to the Altai-Sayan Mountains in the south. More than a hundred kudurs were studied and tested in detail. There were only a few cases when animals visited kudurs only for sodium.

Lithophagy-Geophagy

Conclusions

• The instinctive desire to eat earthy substances, products of hypergenic transformation of various rocks, preserved in many groups of animals and partly in humans, is, in its most general form, a manifestation of the evolutionarily conditioned way of regulating the material composition of the internal environment, as well as some biological and physiological processes in the body.
• There are two varieties of instinctive geophagy-lithophagy, which define two types of self-regulation of organisms with the help of natural minerals and earthy substances of complex composition.

3.

The main cause of geophagy-lithophagy in humans and animals is to maintain the required concentration and ratio of rare earth elements in the neuroimmunoendocrine system of the body. This control center of metabolic and immune defense processes in any organism is largely based on the unique physicochemical properties of f-electron atoms of REE, not all seventeen, but at best a few, perhaps six of them. The role of such atoms in the organism is only beginning to be studied. According to the available data, it is determined by the effects on ionotropic receptors. The tendency to regulate REE in the body, in fact, to geophagy, is controlled by the development of specific hormonal stress.

4.

The complexity of maintaining the necessary ratio and concentration of REE in the body consists not only in the fact that all these elements without exception can be integrated into biological structures, but not all of them are capable of performing the functions required by the body. The complexity also lies in the fact that all REE necessary for the body, as well as all other vital elements, follow the law of "threshold" concentrations according to V.V. Kovalsky (1974), i.e. such concentrations above or below which metabolic regulation is disturbed, which is accompanied by dysfunction of life-support systems and, as a result, persistent metabolic disorders with the transition of the body to the state of endemic geochemically determined disease. The nature of REE endemias seems to be determined on the one hand by the ratios and concentrations of REE entering the internal environment of the body, and on the other hand by the genetic characteristics of organisms that have recently settled or have lived for a long time in landscapes that are REE-anomalous for a given organism.

5.

The effect of minerals on any living body is multifactorial and not always positive. The complete list of mineral effects on living systems is presented in a separate table (see Table 1).

6.

Sometimes the need for geophagy in animals (possibly also in humans) may not be related to the regulation of rare earth elements in the body, but is determined by the need to regulate their internal environment based on other functions that the mineral-crystalline substances have.

7.

Instinctive geophagy in animals (especially in mammals) usually acquires traditional forms with long visits to the same places over centuries and millennia, resulting in the formation of specific landscape complexes, which we call by the term "kudurs". Kudurs, as places of wildlife concentration, have always been used by humans for hunting animals.

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