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Gold, coal and oil
Medical Hypotheses 74 (2010) 534–541
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Gold, coal and oil Sergio U. Dani * Medawar Institute for Medical and Environmental Research, Acangaú Valley, CXP 123, 38600-000 Paracatu-MG, Brazil
a r t i c l e
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Article history: Received 11 September 2009 Accepted 23 September 2009
s u m m a r y Jared Diamond has hypothesized that guns, germs and steel account for the fate of human societies. Here I propose an extension of Diamond’s hypothesis and put it in other terms and dimensions: gold, coal and oil account not only for the fate of human societies but also for the fate of mankind through the bodily accumulation of anthropogenic arsenic, an invisible weapon of mass extinction and evolutionary change. The background is clear; arsenic species fulfill seven criteria for a weapon of mass extinction and evolutionary change: (i) bioavailability to all living organisms; (ii) imperceptibility; (iii) acute toxicity; (iv) bioaccumulation and chronic toxicity; (v) adverse impact on reproductive fitness and reproductive outcomes and early-age development and growth in a wide range of microbial, plant and animal species including man; (vi) widespread geographical distribution, mobility and ecological persistence on a centennial to millennial basis and (vii) availability in necessary and sufficient amounts to exert evolutionarily meaningful effects. The proof is becoming increasingly feasible as human exploitation of gold, coal and oil deposits cause sustainable rises of arsenic concentrations in the biosphere. Paradoxically, humans are among the least arsenic-resistant organisms because humans are long-lived, encephalized and complex social metazoans. An arsenic accumulation model is presented here to describe how arsenic accumulates in the human body with increasing age and at different provisionally safe exposure levels. Arsenic accumulates in the human body even at daily exposure levels which are within the lowest possible WHO provisional tolerance limits, yielding bodily arsenic concentrations which are above WHO provisional limits. Ongoing consequences of global scale arsenic poisoning of mankind include age-specific rises in morbidity and mortality followed by adaptive changes. The potential rise of successful forms of inborn resistance to arsenic in humans will make it certain that a number of other hardly won, nicely balanced human-specific adaptednesses will decline. These include a decline of encephalization and lifespan, and consequentially intelligence and longevity. These changes are likely to have far-reaching impacts on biological and cultural evolution of mankind. The only efficient way of reducing chronic global exposure to arsenic and avoiding further human losses is the inactivation of important sources of anthropogenic arsenic such as hard rock mining and burning of fossil fuels. Ó 2009 Elsevier Ltd. All rights reserved.
Background: it all began with pyrite, arsenopyrite When carbon-based life first obtruded on Earth, it was chemically determined and directionally fixed by a transition-metal catalyst known as pyrite (FeS2), the ‘‘fool’s gold” [1–3]. Arsenic, ‘‘the king of poisons”, a metalloid present in the Earth’s crust, was already there to enact as a factor in evolution processes as seen by the coupled substitution of sulphur (S) with arsenic (As) in the pyrite structure yielding arsenopyrite which is the principal ore of arsenic [4–6]. Inorganic species of arsenic are known to be highly toxic, however, some organic species can be as toxic as inorganic species [7] and organic species can be converted into inorganic species under natural conditions [8]. Therefore and for practical reasons, I shall refer to both organic and inorganic arsenic species – and there * Address: Zimmermannstrasse 28, 37075 Göttingen, Germany. Tel.: +49 15 226 453 423. E-mail address: [email protected] 0306-9877/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.mehy.2009.09.047
are hundreds of different arsenic species – simply as ‘‘arsenic” (As) in this paper. Arsenic acts by disrupting catalytic processes [9–12]. This effect of arsenic has an evolutionary meaning; all living organisms – from chemoautotrophic organisms that grow by reducing or oxidizing arsenic [13–17] to metazoan – carry highly conserved arsenic resistance genes [9,10,18,19] but susceptibility to arsenic toxicity varies between taxa in many orders of magnitude [9,10,20] and even arsenic-hypertolerant organisms will stop to grow and will eventually die when exposed to arsenic over species-specific resistance limits [21–23].
Arsenic as an invisible weapon of mass extinction and evolutionary change Arsenic fulfills seven criteria which I herewith propose for a weapon of mass extinction and evolutionary change: (i)
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bioavailability to all living organisms [9]; (ii) imperceptibility (arsenic trioxide, the ‘‘classic poison” is invisible, odorless and tasteless in aqueous media); (iii) acute toxicity (As species are ranked first on all lists of hazardous substances); (iv) bioaccumulation and chronic toxicity [14]; (v) adverse impact on reproductive fitness and reproductive outcomes [21–33] and early-age development and growth [21–23,28,31,34,35] in a wide range of microbial, plant and animal species including man; (vi) widespread geographical distribution [4,5,36–40], mobility and ecological persistence on a centennial to millennial basis [9,37,39,41–46] and (vii) availability in necessary and sufficient amounts to exert evolutionarily meaningful effects. The last of seven criteria, namely availability in necessary and sufficient amounts to exert evolutionarily meaningful effects, i.e., the evolutionary ‘‘charge” or ‘‘load” of the weapon is less evident and needs an additional explanation in order to fully portray arsenic as a weapon of mass extinction and evolutionary change. The explanation follows on a closer inspection of geological evidence, which reveals some important facts about arsenic sources and sinks in the Earth’s biosphere (Fig. 1). Going back in geological time, terrestrial and submarine volcanic activities have dominated global arsenic geochemical cycles and regulated natural selection processes by directly providing – and indirectly inducing – arsenic input into the biosphere. Among the so called ‘‘trace” toxicants, arsenic is more poisonous and more abundant in the Earth’s crust than cadmium, iodine, mercury and lead [40,47,48]. Crustal arsenic concentration, 1.8 103 ppb [40] is in the same order of magnitude as the lethal arsenic concentration for metazoans such as Homo sapiens [49,50], but some microorganisms will tolerate and accumulate arsenic at concentrations up to 104 higher than the crustal arsenic concentration [20]. Crustal phenomena such as volcanic activity can significantly increase arsenic concentrations in air, soils and water and impact life on Earth. The eruption of the Kilauea volcano (Hawaii, USA) in 1983
Fig. 1. Arsenic cycles in the Earth’s biosphere. Arsenic concentration in biomass ranges from <103 ppb (lethal As concentration for a metazoan, Homo sapiens [49,50]) to <107 ppb (growth-inhibitory concentration for the acidophilic archaeon Ferroplasma acidarmanus [20]). Crustal phenomena such as volcanic activity and hard rock mining can significantly increase arsenic concentrations in air, soils and water and impact life on Earth. Weathering of rocks and sediments converts arsenic sulfides to arsenic trioxide and other arsenic species, which enter the arsenic cycle as dust or gas, or by dissolution in rain, rivers, or groundwater. Augmented weathering and widespread death provide for further increases in arsenic bioavailability in the biosphere and consequently mass extinction of arsenicintolerant species through a feedforward effect.
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increased the local atmospheric concentration of inorganic arsenic by a factor of 106 (from 13 pg/m3 up to 1.6 lg/m3)[51]. As for a comparison, the current OSHA 1910.1018 occupational permissible exposure limit for inorganic arsenic compounds in breathing zone air is 0.010 mg/m3 [52]. One can imagine the global dimensions and catastrophic effects of such arsenic-loaded artillery as thousands of terrestrial and submarine volcanoes firing arsenic at full charge, and accompanying acidic and anoxic conditions caring for maximal arsenic mobility during those incredibly hard times of mass extinction. Augmented weathering and widespread death would have provided for further increase in arsenic bioavailability in the biosphere and consequently mass extinction of less arsenic-tolerant species through a feedforward effect (Fig. 1). Indeed, exacerbated volcanism [53–55] and trace elements [56,57] have been associated with mass extinctions, and we know enough to be able to say that arsenic was an outstanding – though invisible – weapon in the arsenal of natural selection during mass extinction and cladogenesis. This hypothesis is additionally supported by molecular genetic evidence, a sort of ‘‘DNA-written testimony” which indicates that those organisms which had developed protective mechanisms against toxic arsenic species were exactly those who were able to produce viable offspring and survived the charges of this deadly weapon of natural selection. As a result, all known living organisms carry highly conserved genetic instructions do defend themselves against arsenic toxicity, from microorganisms to plants and animals including man [9,10,18,19]. However, as everything in the scheme of evolution, protective systems or devices are highly fallible and do not retain the same level of efficiency over evolutionary time. When volcanic activity ceased and arsenic loads decreased in a millennial time scale, selection pressure slowly relaxed and so did arsenic resistance adaptednesses in newly evolved taxa. Particularly eukaryotic organisms are not completely protected or safe from arsenic accumulation and poisoning. Even the simplest, arsenic-hypertolerant eukaryotic organisms will die when exposed to arsenic at concentrations which are above species-specific tolerance thresholds [21–23]. In present days, anthropogenic arsenic emissions have surmounted natural emissions from volcanic sources, heralding something close to a paradigm shift in the history of human evolution (Table 1). In 2000, the world cumulative industrial-age anthropogenic arsenic production was estimated in 4.53 million tonnes, with global industrial-age anthropogenic arsenic sources (as As cumulative production) following the order [58]: As mining production (hard rock mining of arsenic-rich ore deposits; these are often Au- and to a lesser extent Cu-, Co-, Ni-, Ag-, Pt-, Pb- and Uores which are closely associated with arsenic minerals such as arsenopyrite [4,5,58]) > As generated from coal > As generated from petroleum. It is highly paradoxical that the activities of one of the least arsenic-tolerant species input arsenic into the biosphere at an unprecedented, health threatening global scale [59,61,63]. Jared Diamond has hypothesized that guns, germs and steel account for the fate of human societies [60]. Diamond’s hypothesis can be put in other unexpected terms and dimensions with gold, coal and oil accounting not only for the fate of human societies, but also for the fate of mankind through the bodily accumulation of anthropogenic arsenic, an invisible weapon of mass extinction and evolutionary change.
Loading the weapon Arsenic deliberate use as a poison has been well documented throughout human history. In the Wikipedia it reads: ‘‘Arsenic became a favorite murder weapon of the Middle Ages and
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Table 1 Some data on present-day biologically relevant sources of natural and anthropogenic arsenic (As) and provisional tolerance limits. Unitsa
As sources
1.8 10 85–142 103 1300 59–124 103
ppb tpa – tpa
4,530 103 40 103 1 106 1.74 103 0.018–0.16 1.0–2.8 30.4–77.9 103 0.16–26 103 1.7–3.7 30 106 0.010 10,000 10 36%, 25%, 14% 8%, 3%, 1% 0.002 2 0.5 500 2 2 103
tonnes tpa tonnes tonnes ng/m3 ng/m3 tpa tpa ppb tonnes mg/m3 ng/m3 ppb –
Crustal abundance of As [40] As emission from volcanism (terrestrial and submarine) [37,61] Number of volcanic eruptions in the last 10,000 years (half of which happened during recorded history) [62] Anthropogenic As emission (as of 1995, 23–49% of which are atmospheric emissions. These include As emissions from copper smelting, coal burning, pesticides, lead and zink smelting, glass production, deforestation, wood, pasture burning, etc.) [37,61,63] World cumulative industrial-age anthropogenic As production, as of 2000 [63] Inorganic As output from a single gold mine at Paracatu-MG Brazil, in the period 2009–2039 [58,59] Average global As stocks in the atmosphere [64] Average As concentration in the atmosphere above ocean [37,61] Average As concentration in the atmosphere above land [37,61] As deposition from the atmosphere [37,61] Slow As release from soils [37,61] As concentration in oceanic waters [37,61] Total As content in Earth’s biomass [65] OSHA 1910.1018 occupational permissible exposure limit for inorganic arsenic compounds in breathing zone air in work environments [52] 1993 provisional WHO safe limit for As in drinking water [65,67] Percentage of public water supplies in the USA which have As concentration greater than 1 ppb, 2 ppb, 5 ppb, 10 ppb, 20 ppb, and 50 ppb, respectively [68] Provisional FAO/WHO limit for maximum tolerable daily intake of inorganic As – FAO/WHO PMTDI [66,67] FAO/WHO PLMTDI as above, in ppb [66,67] ATSDR permissible level of As in eggs and uncooked edible tissues of chicken and turkey in the USA [69] ATSDR permissible limit as described above [69], in ppb ATSDR permissible level of As in certain uncooked edible by- products of swine in the USA [69] ATSDR permissible level as above [69], in ppb
Amounts 3
a
mg/kg BW/day ppb ppm ppb ppm ppb
Abbreviations: tpa, tonnes per annum; ppb, parts per billion; mg/kgBW/day, mg/kg of body weight/day; ppm, parts per million.
Renaissance, particularly among ruling classes in Italy, notably the Borgias. Because the symptoms are similar to those of cholera, which was common at the time, arsenic poisoning often went undetected. By the 19th C., it had acquired the nickname ‘‘inheritance powder,” perhaps because impatient heirs were known or suspected to use it to ensure or accelerate their inheritances” [70]. However nothing compares to the emerging global impact on human health caused by anthropogenic arsenic worldwide. As certain as chronic arsenic poisoning is reaching global dimensions with millions of people becoming sick and dying and economies facing bankruptcy [24,59,61,66,71,72], it is also beyond doubt that international and national limits for tolerable or safe arsenic exposure are short of halting the increase in overall arsenic loads in natural and man-made environments. Current criteria for the protection of human health and natural resources against arsenic contamination or poisoning following anthropogenic release in gold mines, for example, do not protect arsenic-sensitive humans, plants and animals [73]. Also, there is no efficient treatment for chronic arsenic intoxication. The only efficient solution is the inactivation of the source of arsenic contamination of natural resources, water, soils, food and atmosphere, or the sustainable provision of uncontaminated resources, which are becoming increasingly scarce. Humans absorb arsenic mainly by the oral (water, food) and respiratory (dust, gases) routes and to a lesser extent by the skin. Evolution and development of most living things – humans, anyway – occur in aquatic environments and such environments are becoming increasingly contaminated by anthropogenic arsenic, beginning in the maternal womb environment. It is now clear that the chronic effects of low concentrations of arsenic in drinking water – in food and air as well, since these are interconnected compartments – have been underestimated. Arsenic volatilization, mobility and environmental persistence are likely to shift contaminations from local to global dimensions. Large populations in various parts of the world are already exposed to levels of arsenic which are well above safe limits. The World Health Organization’s
lowest possible tolerance value of 10 ppb in drinking water [66] was based largely on analytical capability and even such low safety limit will conceivably not compensate for increasing arsenic exposure arising from a number of natural and anthropogenic sources such as airborne arsenic volatilized from microbial activity on arsenic-contaminated soils, sediments and ore tailings of hard rock mines worldwide [20,74–80]. Indeed, several geochemical mapping projects deliver indications for crustal arsenic degassing as an important process leading to arsenic enrichment in the surface environment [39]. The release of inorganic arsenic from a single gold mine is equivalent to 25% of the world cumulative industrial-age anthropogenic arsenic production [58]; the amount of inorganic arsenic to be released from the rocks of this single mine in the next 30 years of mining operations is equivalent to 1/30 of the total arsenic content in the Earth’s biomass [65]. This is potentially enough to affect the health of 10 times as many people as are presently living on Earth [25,49,50,58,59,81]. As I said, this is the arsenic output from just one single mine. However, mine properties all over the world amount to 8585 for gold; 4044 for copper; 2639 for silver; 2476 for coal and 1202 for lead, just to mention some of the main sources of anthropogenic arsenic [82]. Total world gold production in the period 1835–2007 was 160,000 tonnes [83] and estimated gold reserves and resources amount to another 160,000 tonnes [82]. Gold ores associated with pyrite and arsenopyrite are the most abundant worldwide [84] and the arsenic to gold relationships in gold ores vary between 300 and 1000 to 1 [85]. This is equivalent to say that arsenic emissions from gold mining activities alone in the period of 1835–2007 was equivalent to 4.8 107–16 107 tonnes and an equal amount is expected to be released from hard rock gold mining activities in the future. This is equivalent to a global burden of 10–100 kg of arsenic per capita, not to mention the natural arsenic and anthropogenic arsenic from other sources such as coal and oil. These unbelievable amounts of arsenic have the potential to set the stage for a catastrophe of mass extinction stature. Most arsenopyrite anomalies are biogenic and date back to Cambrian time [84]. It is
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intriguing to think of arsenic as a weapon of mass extinction when we have a rationale in the Cambrian mass extinctions and the arsenopyrite anomalies that have formed in those geological times as a result of microbial metabolism. People tend to oversee such appalling scenarios, as if they were unlikely or too distant from reality. However, a closer inspection of present day morbidity and mortality data shall reveal what appear to be inconvenient truths. The leading causes of morbidity and mortality worldwide are vascular diseases (including cardiovascular and cerebrovascular diseases), infectious diseases, cancer (particularly lung cancer), diabetes, diseases of the liver and kidneys, Alzheimer’s disease and other dementias [86]. All these conditions have been causally related to long-term exposure to arsenic [12,18,19,24,25,29,31,32,34,35,49,50,66,72,81,87–99]. With the exception of Alzheimer’s disease – the cause in most cases of which being thought of as ‘‘multiple” or as ‘‘a puzzle” much in the same way the proximate causes of the extinction of the dinosaurs are thought of as being beyond human comprehension, even after associations with arsenic have been found [57] – high risks and exposure-dose relationships have been observed for each of those end-points in studies of different design [24,25,28,29,31,32,34, 49,50,66,72,73,81,93,94,99]. I suspect it is just a matter of taking time, arsenic exposure- and tissue accumulation dynamics and inherited variations in susceptibilities into account in appropriate experimental designs, and Alzheimer’s disease shall be somehow related to long-term arsenic exposure too. Most importantly, it has been shown that arsenic accumulation has adverse impacts on reproductive fitness and reproductive outcomes [21–33] and early-age development and growth [21– 23,28,31,34,35] in a wide range of microbial, plant and animal species including man. This is important because reproductive age and early life fitness ultimately define the evolution of human adaptednesses such as encephalization and prolonged life-span, and consequentially intelligence and longevity [98–102]. Humans evolved into their present form during the Pleistocene [100,103– 106], coinciding with the final stages of a period of exacerbated tectonic activity (therefore a period of presumably high arsenic loads). In the beginning of the Pleistocene, australopithecine species of both human- and non-human ancestry are still present, but during the lower Palaeolithic many had disappeared [100,105]. Volcanism seems to have encouraged dispersal and migration of some early hominids – the clever ones, anyway, the ones who conceivably noticed they would die if they did nothing about a mysterious, invisible killing force – outside the main Ethiopian rift basins during major eruption interludes [105]. Rapid accelerations in the rate of encephalization in the hominid lineage and the emergence of Homo species were verified when subsidence in the Afar area was nearly complete [100,105,106]. Thus, the hypothesis of persistent arsenic concentrations which are above species-specific tolerance limits causing extinctions and setting the stage for cladogenesis should also apply to the hominid lineage. The experimental proof of this hypothesis is likely to affect modern humans in highly incredible ways. Chronic exposure to below lethal doses is sufficient to produce bodily arsenic accumulation and toxicity over the lifetime of reproducing individuals in a population (Figs. 2 and 3). As I have stated before, species-specific tolerance limits are set at the point where chronic accumulation of arsenic does not interfere with the specie’s reproductive success. Unhappily, this point seems to have been already trespassed in many localities and regions of the world [24–35,58,59,66,68,72,73,93–95,99]. In line with geological evidence as above discussed, persistent arsenic concentrations which are above species-specific thresholds are expected to cause extinctions and cladistic events with some degree of certainty at the local scale, and with less certainty at the global scale. Let us explore how this is expected to happen with the human species.
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Fig. 2. Arsenic accumulates in the human body with age, as observed by Raie [110] in a series of autopsied patients in Glasgow. The patients had no clinical sign of arsenicosis; they died from external causes, as accidents. Note that even in such sub-clinical settings, accumulated arsenic is found above FAO/WHO provisional maximum tolerable daily intake of inorganic arsenic (0.002 mg/kg of body weight) [67]. The accumulation curve proposed here to accommodate Raie’s data is compatible with the animal experimental model of Marafante and coworkers [107].
Invisible As and the fate of mankind: the hypothesis Proximate consequences of chronic anthropogenic input of arsenic into the human compartment include rises in morbidity and mortality from diseases for which long-term exposure to arsenic have been causally related, as above referenced. The higher the arsenic exposure levels, the higher and the earlier will be the impacts on health and economical status of the exposed populations (Fig. 3). Even populations which do not present clinical signs of arsenicosis [108–110] are at risk of arsenic co-morbidity and should be more closely watched for a better appraisal of what is going on. Given that arsenic removal from water, soils and air is prohibitively expensive, much will depend on the availability of feasible alternative resources, which are increasingly scarce. The best treatment strategy when symptoms start emerging is the provision of arsenic-free water, food and air which are becoming unfortunately scarce all over the world [111,112]. Global warming and global water shortage are likely to worsen these prospects, for temperature is one of the weathering factors which determine arsenic dissolution in water (Fig. 1). The mobilisation of arsenic is believed to be caused by oxidation of arsenic minerals such as arsenopyrite, exacerbated mostly by mining activities, but also by other industrial, household and agricultural activities. Recent arsenic appearances in groundwaters worldwide have occurred during post-mining, post-pumping groundwater rebounds [41–43,68,72,73,97,113,114]. The full epidemiological implications of arsenic contamination are only now emerging, and it is likely that over the coming decade more arsenicosis cases and arsenic-associated morbidities will be identified. Here I am interested in the impact of arsenic-related morbidity and mortality on human fitness. The hypothesis is this. Large scale arsenic poisoning of mankind has the potential to cause a rise in morbidity and mortality followed by adaptive changes. Adaptive changes include drops in human-specific adaptednesses, namely encephalization and longevity. These changes are likely to have far-reaching impacts on biological and cultural evolution of mankind.
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Fig. 3. A model for arsenic accumulation (top) and ‘‘survival” (bottom, here As% of the individuals in the original population who do not present any known endpoints of chronic arsenic toxicity which otherwise would affect reproductive fitness and long term survival) in aging human populations chronically exposed to increasing doses of toxic arsenic. Curves A–D represent theoretical arsenic accumulation (top) and population ‘‘survival” (bottom) for the following increasing exposures to arsenic (As in micrograms/day/individual): A, 12 ug/d/i; B, 15 ug/d/i; C, 20 ug/d/i; D, 38 ug/d/i. Note the exponential pattern of arsenic accumulation, i.e., small increases in daily exposure levels cause large increases in the bodily As concentrations and hence the upward shifts in the accumulation curves (top) and respective decline in survival (bottom). Accumulation curves B–D would not be verified for all individuals in the population because the most arsenic intolerant – which most people are – would die as bodily arsenic concentrations become lethal (LC50 = 1 mg/kg BW). There is an age-specific rise in morbidity and mortality associated with As accumulation; higher morbidity and mortality rates typically affect fetuses and young children because the highest rates of As accumulation occur during development; children and adults will be affected sooner or later in their lifetimes as a result of age-specific As accumulation and associated morbidities. For practical purposes, all exposed people are at risk of developing arsenicrelated pathologies or will have their age-specific fitness components deteriorated by arsenic exposure and accumulation, sooner or later in their lifetimes. All exposure levels (curves A–D) are within ‘‘safe”, ‘‘normal” or ‘‘acceptable” exposure limits.
Arsenic in the brain is associated with the lipid phase [115], where phospholipids and proteins exert their important roles on brain structure and metabolism. Chronic accumulation of arsenic in the human brain is related to impaired mental functions and neurological and psychological harms including mental retardation,
developmental disabilities such as physical, cognitive, psychological, sensory and speech impairments, and depression [116]. For practical reasons, we shall consider all these changes as functionally equivalent to a drop in encephalization. In extinct hominids, each change in encephalization goes hand-in-hand with changes in adaptability [102] and longevity [101], a process which has been generally associated with extinction of the less encephalized forms and evolution toward more encephalized forms over evolutionary time. Chronic arsenic poisoning has the potential to cause a decline of hardly won and nicely balanced human-specific adaptednesses, namely encephalization and prolonged life-span, and consequentially intelligence and longevity through the following biologically and socially different but complementary mechanisms. Larger brains and more encephalized fetuses and children are metabolically more demanding than smaller brains and less encephalized fetuses and children [100,101]. Altriciality, as opposed to precocity is a hallmark of more encephalized humans. It follows that relatively larger brains demand more food and water and air and time to get fully built up and instructed than relatively smaller brains. Unfortunately arsenic accumulation behaves much in the same fashion: it takes food and water and time into account. Therefore we can expect with some degree of certainty that more encephalized fetuses and children are metabolically bound to be more sensitive to arsenic contamination than the less encephalized. We can then expect families with more encephalized, long-lived members to suffer more from health and economic distresses caused by arsenic accumulation than families with less encephalized members. The health and economic burdens imposed upon families of more encephalized, more intelligent people through the ills of arsenic accumulation will cause them to be poorer. The most intelligent are going to have less children, while the less intelligent are going to have more, and have them earlier in their reproductive lives. Generation by generation, they will tend to have larger families than the more intelligent. Generation by generation, the more encephalized, intelligent and longer-lived families will eventually die out in the population. In summary, more encephalized fetuses and children will die most before reproduction and less encephalized children will have better reproductive advantages. If there are genetic differences in resistance to arsenic within human populations – and we know there are such differences [117] – the genetic structure of the population must clearly change with time and successive generations. Some adaptednesses may be lost in the process in order to maintain adaptability. However, inborn resistance to arsenic does not reveal any general soundness of humane constitution. As a result, the survivors of this evolutionary process led by arsenic will have to deal with all sorts of socio-environmental issues utilizing their less encephalized brains and lower intelligence, shorter life-spans and decreased longevities. There are lots of uncertainties involved in such predictions, but we should not stop making predictions of this degree of importance for fear of being wrong. It may well be the case that these predictions are wrong and we should expect the survivors of an arsenic catastrophe to be fitter and more intelligent, instead of short lived and stupid. Unfortunately this does not seem to be the general rule in the evolutionary schemes directed by arsenic. Instead, the inference we can draw from the study of arsenic resistance in a wide range of microbial, plant and animal species is that the arsenic-tolerant – those which are more arsenic tolerant than Homo sapiens, anyway – are less biologically and sociologically complex than humans. We should not forget that bursts of encephalization in the human lineage occurred outside the places of intense tectonism, consequentially outside the places and times of supposedly high arsenic concentrations [100,102–106].
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We know enough to be able to say that waiting for a general innate arsenic resistance to naturally obtrude in the human lineage – instead of stamping out anthropogenic arsenic itself – is a risky, wasteful and foolish enterprise. As pointed out by Peter Medawar [118], those who accept natural selection of man as a natural solution of the problem of a disfavorable environment are up to mischief; ‘‘they reveal their misunderstanding of Nature, of man’s place in Nature, and of the nature of man.” Humans seek out and store and use gold, coal and oil as if they were energetic foods, as if these stuffs would enhance survival through periods of fast and famine and economic distress; however in doing so humans are traveling just in opposite way as we would have planned or instinctively wanted. In seeking out these stuffs we are building up arsenic stores that threaten the survival of millions – perhaps billions – in the long run. It is becoming increasingly clear that gold, coal and oil are being seek out and stored, bought and sold, and wear or consumed at the expense of our biological fitness. There is no reason to believe that the worldwide protection of the environment from continuing anthropogenic arsenic contamination would have economically negative effects. On the contrary, there is every reason to believe that failure to adopt some measures of control and limitation of anthropogenic arsenic input into the biosphere will lead, in the long run, to diseases, deaths, misery, privation and economic distress. In what seems to be a danger according to present-day evidence and thinking, arsenic is likely to affect our most important evolutionary achievements, namely encephalization and prolonged life-span and consequentially intelligence and longevity. There is thus enough reason to believe that to mobilize arsenic from arsenopyrite, the principal ore of arsenic in thousands of gold mines scattered all over the world is a risky business; it is equivalent to travel the opposite sense in the direction anthropologists tell us we have been traveling during the last 2.5 million years [100].
A final note or warning For better clarity and general tranquility, I should state at the outset of this conclusion section that extinction is rather the rule than the exception in the wasteful schemes of natural evolution. This statement is not intended to console the reader by recalling that sooner or later everyone is going to die anyway. Instead, it is intended to call attention to the question as to whether it makes any sense to jeopardize global health and quality of life for gold, coal and oil. With our global perspective, there comes a global responsibility toward our species and the many more living creatures with which we share our planet. I believe mankind must try and find a humane solution for the problem of anthropogenic arsenic, before our very existence as a species deteriorates. If there are ways to prevent such an outcome, we should find them. Science can help in many ways. For example, natural sources of arsenic contamination can be predicted by geological surveys [36,68] thereby creating the possibility to avoid the de novo arsenic release from those sources. However, science alone is not likely to produce any positive results unless a global change in human behavior takes place. A worldwide concerted action has to be undertaken as to halt the deliberate anthropogenic contamination of the planet and our bodies with arsenic, in similar though hopefully more efficient ways as has been done with the control of CO2 emissions. Or shall there be any reason or hope to believe or to want that some new sort of arsenichypertolerant, intelligent hominid shall evolve from scratch again? As stated at the outset, the first organized entity of life was a composite structure around a growing cluster of pyrite [1–3]. This
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initial organization provided the ‘‘anlage” for evolution by autocatalytic expansion of carbon-fixation pathways with an inherent tendency toward an increasing number of reaction possibilities [1]. As pointed out by Günter Wächtershäuser [1], this inherent tendency to evolve toward higher complexity creates life’s own prospects, and provides the physical basis for the interpretation of evolution as a process of self-liberation. At this point I should finish by quoting one of Sir Peter Medawar’s thoughts: ‘‘The inference we can draw from an analytical study of the differences between ourselves and other animals is surely this: that the bells which toll for mankind are – most of them, anyway – like the bells on Alpine cattle; they are attached to our own necks, and it must be our fault if they do not make a cheerful and harmonious sound [118].” Conflicts of interest statement None declared. Acknowledgements The author wishes to thank P.M. Serrano Neves and B.C. Dani for discussions; C.D. Gama for suggestions; M.A.C. Dani and S.C. Dani for support. References [1] Wächtershäuser G. Life in a ligand sphere. Proc Natl Acad Sci USA 1994;91:4283–7. [2] Wächtershäuser G. From volcanic origins of chemoautotrophic life to bacteria, archaea and eukarya. Philos Trans R Soc Lond B Biol Sci 2006;361:1787–806. discussion 1806–8. [3] Wächtershäuser G. On the chemistry and evolution of the pioneer organism. Chem Biodivers 2007;4:584–602. [4] Vaughan DJ. Arsenic. Elements 2006;2:71–5. [5] Hurlbut CS, Klein C. Manual of mineralogy. 20th ed. New York: John Wiley and Sons; 1985. p. 285–6. [6] O’Neil P. Arsenic. In: Alloway BJ, editor. Heavy metals in soils. London: Blackie; 1995. p. 107–21. [7] Naranmandura H, Ibata K, Suzuki KT. Toxicity of dimethylmonothioarsinic acid toward human epidermoid carcinoma A431 cells. Chem Res Toxicol 2007;20:1120–5. [8] Hanaoka K, Kogure T, Miura Y, Tagawa S, Kaise T. Post-mortem formation of inorganic arsenic from arsenobetaine in a shark under natural conditions. Chemosphere 1993;27:2163–7. [9] Tamaki S, Frankenberger Jr WT. Environmental biochemistry of arsenic. Rev Environ Cont Toxicol 1992;124:79–110. [10] Rosen BP. Biochemistry of arsenic detoxification. FEBS Lett 2002;529:86–92. [11] Bernstam L, Nriagu J. Molecular aspects of arsenic stress. J Toxicol Environ Health B Crit Rev 2000;3:293–322. [12] Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chemico-Biol Interact 2006;160:1–40. [13] Ilyaletdinov AN, Abdrashitova SA. Autotrophic oxidation of arsenic by a culture of Pseudomonas arsenitoxidans. Mikrobiologiya 1981;50:197–204. [14] Ahmann D, Roberts AL, Krumholz LR, Morel FMM. Microbe grows by reducing arsenic. Nature 1994;371:750. [15] Lebrun E, Brugna M, Baymann F, Muller D, Lièvremon D, Lett MC, et al. Arsenite oxidase, an ancient bioenergetic enzyme. Mol Biol Evol 2003;20:686–93. [16] Jackson CR, Dugas SL. Phylogenetic analysis of bacterial and archaeal arsC gene sequences suggests an ancient, common origin for arsenate reductase. BMC Evol Biol 2003;3:18. [17] Muller D, Médigue C, Koechler S, et al. A tale of two oxidation states: bacterial colonization of arsenic-rich environments. PLoS Genet 2007;3:e53. [18] Schmuck EM, Board PG, Whitbread AK, Tetlow N, Cavanaugh JA, Blackburn AC, et al. Characterization of the monomethylarsonate reductase and dehydroascorbate reductase activities of Omega class glutathione transferase variants: implications for arsenic metabolism and the age-atonset of Alzheimer’s and Parkinson’s diseases. Pharmacogenet Genom 2005;15:493–501. [19] Coppin JF, Qu W, Waalkes MP. Interplay between cellular methyl metabolism and adaptive efflux during oncogenic transformation from chronic arsenic exposure in human cells. J Biol Chem 2008;283:19342–50. [20] Baker-Austin C, Dopson M, Wexler M, Sawers RG, Stemmler A, Rosen BP, et al. Extreme arsenic resistance by the acidophilic archaeon ‘Ferroplasma acidarmanus’ Fer1. Extremophiles 2007;11:425–34.
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Medical Hypotheses journal homepage: www.elsevier.com/locate/mehy
Gold, coal and oil Sergio U. Dani * Medawar Institute for Medical and Environmental Research, Acangaú Valley, CXP 123, 38600-000 Paracatu-MG, Brazil
a r t i c l e
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Article history: Received 11 September 2009 Accepted 23 September 2009
s u m m a r y Jared Diamond has hypothesized that guns, germs and steel account for the fate of human societies. Here I propose an extension of Diamond’s hypothesis and put it in other terms and dimensions: gold, coal and oil account not only for the fate of human societies but also for the fate of mankind through the bodily accumulation of anthropogenic arsenic, an invisible weapon of mass extinction and evolutionary change. The background is clear; arsenic species fulfill seven criteria for a weapon of mass extinction and evolutionary change: (i) bioavailability to all living organisms; (ii) imperceptibility; (iii) acute toxicity; (iv) bioaccumulation and chronic toxicity; (v) adverse impact on reproductive fitness and reproductive outcomes and early-age development and growth in a wide range of microbial, plant and animal species including man; (vi) widespread geographical distribution, mobility and ecological persistence on a centennial to millennial basis and (vii) availability in necessary and sufficient amounts to exert evolutionarily meaningful effects. The proof is becoming increasingly feasible as human exploitation of gold, coal and oil deposits cause sustainable rises of arsenic concentrations in the biosphere. Paradoxically, humans are among the least arsenic-resistant organisms because humans are long-lived, encephalized and complex social metazoans. An arsenic accumulation model is presented here to describe how arsenic accumulates in the human body with increasing age and at different provisionally safe exposure levels. Arsenic accumulates in the human body even at daily exposure levels which are within the lowest possible WHO provisional tolerance limits, yielding bodily arsenic concentrations which are above WHO provisional limits. Ongoing consequences of global scale arsenic poisoning of mankind include age-specific rises in morbidity and mortality followed by adaptive changes. The potential rise of successful forms of inborn resistance to arsenic in humans will make it certain that a number of other hardly won, nicely balanced human-specific adaptednesses will decline. These include a decline of encephalization and lifespan, and consequentially intelligence and longevity. These changes are likely to have far-reaching impacts on biological and cultural evolution of mankind. The only efficient way of reducing chronic global exposure to arsenic and avoiding further human losses is the inactivation of important sources of anthropogenic arsenic such as hard rock mining and burning of fossil fuels. Ó 2009 Elsevier Ltd. All rights reserved.
Background: it all began with pyrite, arsenopyrite When carbon-based life first obtruded on Earth, it was chemically determined and directionally fixed by a transition-metal catalyst known as pyrite (FeS2), the ‘‘fool’s gold” [1–3]. Arsenic, ‘‘the king of poisons”, a metalloid present in the Earth’s crust, was already there to enact as a factor in evolution processes as seen by the coupled substitution of sulphur (S) with arsenic (As) in the pyrite structure yielding arsenopyrite which is the principal ore of arsenic [4–6]. Inorganic species of arsenic are known to be highly toxic, however, some organic species can be as toxic as inorganic species [7] and organic species can be converted into inorganic species under natural conditions [8]. Therefore and for practical reasons, I shall refer to both organic and inorganic arsenic species – and there * Address: Zimmermannstrasse 28, 37075 Göttingen, Germany. Tel.: +49 15 226 453 423. E-mail address: [email protected] 0306-9877/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.mehy.2009.09.047
are hundreds of different arsenic species – simply as ‘‘arsenic” (As) in this paper. Arsenic acts by disrupting catalytic processes [9–12]. This effect of arsenic has an evolutionary meaning; all living organisms – from chemoautotrophic organisms that grow by reducing or oxidizing arsenic [13–17] to metazoan – carry highly conserved arsenic resistance genes [9,10,18,19] but susceptibility to arsenic toxicity varies between taxa in many orders of magnitude [9,10,20] and even arsenic-hypertolerant organisms will stop to grow and will eventually die when exposed to arsenic over species-specific resistance limits [21–23].
Arsenic as an invisible weapon of mass extinction and evolutionary change Arsenic fulfills seven criteria which I herewith propose for a weapon of mass extinction and evolutionary change: (i)
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bioavailability to all living organisms [9]; (ii) imperceptibility (arsenic trioxide, the ‘‘classic poison” is invisible, odorless and tasteless in aqueous media); (iii) acute toxicity (As species are ranked first on all lists of hazardous substances); (iv) bioaccumulation and chronic toxicity [14]; (v) adverse impact on reproductive fitness and reproductive outcomes [21–33] and early-age development and growth [21–23,28,31,34,35] in a wide range of microbial, plant and animal species including man; (vi) widespread geographical distribution [4,5,36–40], mobility and ecological persistence on a centennial to millennial basis [9,37,39,41–46] and (vii) availability in necessary and sufficient amounts to exert evolutionarily meaningful effects. The last of seven criteria, namely availability in necessary and sufficient amounts to exert evolutionarily meaningful effects, i.e., the evolutionary ‘‘charge” or ‘‘load” of the weapon is less evident and needs an additional explanation in order to fully portray arsenic as a weapon of mass extinction and evolutionary change. The explanation follows on a closer inspection of geological evidence, which reveals some important facts about arsenic sources and sinks in the Earth’s biosphere (Fig. 1). Going back in geological time, terrestrial and submarine volcanic activities have dominated global arsenic geochemical cycles and regulated natural selection processes by directly providing – and indirectly inducing – arsenic input into the biosphere. Among the so called ‘‘trace” toxicants, arsenic is more poisonous and more abundant in the Earth’s crust than cadmium, iodine, mercury and lead [40,47,48]. Crustal arsenic concentration, 1.8 103 ppb [40] is in the same order of magnitude as the lethal arsenic concentration for metazoans such as Homo sapiens [49,50], but some microorganisms will tolerate and accumulate arsenic at concentrations up to 104 higher than the crustal arsenic concentration [20]. Crustal phenomena such as volcanic activity can significantly increase arsenic concentrations in air, soils and water and impact life on Earth. The eruption of the Kilauea volcano (Hawaii, USA) in 1983
Fig. 1. Arsenic cycles in the Earth’s biosphere. Arsenic concentration in biomass ranges from <103 ppb (lethal As concentration for a metazoan, Homo sapiens [49,50]) to <107 ppb (growth-inhibitory concentration for the acidophilic archaeon Ferroplasma acidarmanus [20]). Crustal phenomena such as volcanic activity and hard rock mining can significantly increase arsenic concentrations in air, soils and water and impact life on Earth. Weathering of rocks and sediments converts arsenic sulfides to arsenic trioxide and other arsenic species, which enter the arsenic cycle as dust or gas, or by dissolution in rain, rivers, or groundwater. Augmented weathering and widespread death provide for further increases in arsenic bioavailability in the biosphere and consequently mass extinction of arsenicintolerant species through a feedforward effect.
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increased the local atmospheric concentration of inorganic arsenic by a factor of 106 (from 13 pg/m3 up to 1.6 lg/m3)[51]. As for a comparison, the current OSHA 1910.1018 occupational permissible exposure limit for inorganic arsenic compounds in breathing zone air is 0.010 mg/m3 [52]. One can imagine the global dimensions and catastrophic effects of such arsenic-loaded artillery as thousands of terrestrial and submarine volcanoes firing arsenic at full charge, and accompanying acidic and anoxic conditions caring for maximal arsenic mobility during those incredibly hard times of mass extinction. Augmented weathering and widespread death would have provided for further increase in arsenic bioavailability in the biosphere and consequently mass extinction of less arsenic-tolerant species through a feedforward effect (Fig. 1). Indeed, exacerbated volcanism [53–55] and trace elements [56,57] have been associated with mass extinctions, and we know enough to be able to say that arsenic was an outstanding – though invisible – weapon in the arsenal of natural selection during mass extinction and cladogenesis. This hypothesis is additionally supported by molecular genetic evidence, a sort of ‘‘DNA-written testimony” which indicates that those organisms which had developed protective mechanisms against toxic arsenic species were exactly those who were able to produce viable offspring and survived the charges of this deadly weapon of natural selection. As a result, all known living organisms carry highly conserved genetic instructions do defend themselves against arsenic toxicity, from microorganisms to plants and animals including man [9,10,18,19]. However, as everything in the scheme of evolution, protective systems or devices are highly fallible and do not retain the same level of efficiency over evolutionary time. When volcanic activity ceased and arsenic loads decreased in a millennial time scale, selection pressure slowly relaxed and so did arsenic resistance adaptednesses in newly evolved taxa. Particularly eukaryotic organisms are not completely protected or safe from arsenic accumulation and poisoning. Even the simplest, arsenic-hypertolerant eukaryotic organisms will die when exposed to arsenic at concentrations which are above species-specific tolerance thresholds [21–23]. In present days, anthropogenic arsenic emissions have surmounted natural emissions from volcanic sources, heralding something close to a paradigm shift in the history of human evolution (Table 1). In 2000, the world cumulative industrial-age anthropogenic arsenic production was estimated in 4.53 million tonnes, with global industrial-age anthropogenic arsenic sources (as As cumulative production) following the order [58]: As mining production (hard rock mining of arsenic-rich ore deposits; these are often Au- and to a lesser extent Cu-, Co-, Ni-, Ag-, Pt-, Pb- and Uores which are closely associated with arsenic minerals such as arsenopyrite [4,5,58]) > As generated from coal > As generated from petroleum. It is highly paradoxical that the activities of one of the least arsenic-tolerant species input arsenic into the biosphere at an unprecedented, health threatening global scale [59,61,63]. Jared Diamond has hypothesized that guns, germs and steel account for the fate of human societies [60]. Diamond’s hypothesis can be put in other unexpected terms and dimensions with gold, coal and oil accounting not only for the fate of human societies, but also for the fate of mankind through the bodily accumulation of anthropogenic arsenic, an invisible weapon of mass extinction and evolutionary change.
Loading the weapon Arsenic deliberate use as a poison has been well documented throughout human history. In the Wikipedia it reads: ‘‘Arsenic became a favorite murder weapon of the Middle Ages and
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Table 1 Some data on present-day biologically relevant sources of natural and anthropogenic arsenic (As) and provisional tolerance limits. Unitsa
As sources
1.8 10 85–142 103 1300 59–124 103
ppb tpa – tpa
4,530 103 40 103 1 106 1.74 103 0.018–0.16 1.0–2.8 30.4–77.9 103 0.16–26 103 1.7–3.7 30 106 0.010 10,000 10 36%, 25%, 14% 8%, 3%, 1% 0.002 2 0.5 500 2 2 103
tonnes tpa tonnes tonnes ng/m3 ng/m3 tpa tpa ppb tonnes mg/m3 ng/m3 ppb –
Crustal abundance of As [40] As emission from volcanism (terrestrial and submarine) [37,61] Number of volcanic eruptions in the last 10,000 years (half of which happened during recorded history) [62] Anthropogenic As emission (as of 1995, 23–49% of which are atmospheric emissions. These include As emissions from copper smelting, coal burning, pesticides, lead and zink smelting, glass production, deforestation, wood, pasture burning, etc.) [37,61,63] World cumulative industrial-age anthropogenic As production, as of 2000 [63] Inorganic As output from a single gold mine at Paracatu-MG Brazil, in the period 2009–2039 [58,59] Average global As stocks in the atmosphere [64] Average As concentration in the atmosphere above ocean [37,61] Average As concentration in the atmosphere above land [37,61] As deposition from the atmosphere [37,61] Slow As release from soils [37,61] As concentration in oceanic waters [37,61] Total As content in Earth’s biomass [65] OSHA 1910.1018 occupational permissible exposure limit for inorganic arsenic compounds in breathing zone air in work environments [52] 1993 provisional WHO safe limit for As in drinking water [65,67] Percentage of public water supplies in the USA which have As concentration greater than 1 ppb, 2 ppb, 5 ppb, 10 ppb, 20 ppb, and 50 ppb, respectively [68] Provisional FAO/WHO limit for maximum tolerable daily intake of inorganic As – FAO/WHO PMTDI [66,67] FAO/WHO PLMTDI as above, in ppb [66,67] ATSDR permissible level of As in eggs and uncooked edible tissues of chicken and turkey in the USA [69] ATSDR permissible limit as described above [69], in ppb ATSDR permissible level of As in certain uncooked edible by- products of swine in the USA [69] ATSDR permissible level as above [69], in ppb
Amounts 3
a
mg/kg BW/day ppb ppm ppb ppm ppb
Abbreviations: tpa, tonnes per annum; ppb, parts per billion; mg/kgBW/day, mg/kg of body weight/day; ppm, parts per million.
Renaissance, particularly among ruling classes in Italy, notably the Borgias. Because the symptoms are similar to those of cholera, which was common at the time, arsenic poisoning often went undetected. By the 19th C., it had acquired the nickname ‘‘inheritance powder,” perhaps because impatient heirs were known or suspected to use it to ensure or accelerate their inheritances” [70]. However nothing compares to the emerging global impact on human health caused by anthropogenic arsenic worldwide. As certain as chronic arsenic poisoning is reaching global dimensions with millions of people becoming sick and dying and economies facing bankruptcy [24,59,61,66,71,72], it is also beyond doubt that international and national limits for tolerable or safe arsenic exposure are short of halting the increase in overall arsenic loads in natural and man-made environments. Current criteria for the protection of human health and natural resources against arsenic contamination or poisoning following anthropogenic release in gold mines, for example, do not protect arsenic-sensitive humans, plants and animals [73]. Also, there is no efficient treatment for chronic arsenic intoxication. The only efficient solution is the inactivation of the source of arsenic contamination of natural resources, water, soils, food and atmosphere, or the sustainable provision of uncontaminated resources, which are becoming increasingly scarce. Humans absorb arsenic mainly by the oral (water, food) and respiratory (dust, gases) routes and to a lesser extent by the skin. Evolution and development of most living things – humans, anyway – occur in aquatic environments and such environments are becoming increasingly contaminated by anthropogenic arsenic, beginning in the maternal womb environment. It is now clear that the chronic effects of low concentrations of arsenic in drinking water – in food and air as well, since these are interconnected compartments – have been underestimated. Arsenic volatilization, mobility and environmental persistence are likely to shift contaminations from local to global dimensions. Large populations in various parts of the world are already exposed to levels of arsenic which are well above safe limits. The World Health Organization’s
lowest possible tolerance value of 10 ppb in drinking water [66] was based largely on analytical capability and even such low safety limit will conceivably not compensate for increasing arsenic exposure arising from a number of natural and anthropogenic sources such as airborne arsenic volatilized from microbial activity on arsenic-contaminated soils, sediments and ore tailings of hard rock mines worldwide [20,74–80]. Indeed, several geochemical mapping projects deliver indications for crustal arsenic degassing as an important process leading to arsenic enrichment in the surface environment [39]. The release of inorganic arsenic from a single gold mine is equivalent to 25% of the world cumulative industrial-age anthropogenic arsenic production [58]; the amount of inorganic arsenic to be released from the rocks of this single mine in the next 30 years of mining operations is equivalent to 1/30 of the total arsenic content in the Earth’s biomass [65]. This is potentially enough to affect the health of 10 times as many people as are presently living on Earth [25,49,50,58,59,81]. As I said, this is the arsenic output from just one single mine. However, mine properties all over the world amount to 8585 for gold; 4044 for copper; 2639 for silver; 2476 for coal and 1202 for lead, just to mention some of the main sources of anthropogenic arsenic [82]. Total world gold production in the period 1835–2007 was 160,000 tonnes [83] and estimated gold reserves and resources amount to another 160,000 tonnes [82]. Gold ores associated with pyrite and arsenopyrite are the most abundant worldwide [84] and the arsenic to gold relationships in gold ores vary between 300 and 1000 to 1 [85]. This is equivalent to say that arsenic emissions from gold mining activities alone in the period of 1835–2007 was equivalent to 4.8 107–16 107 tonnes and an equal amount is expected to be released from hard rock gold mining activities in the future. This is equivalent to a global burden of 10–100 kg of arsenic per capita, not to mention the natural arsenic and anthropogenic arsenic from other sources such as coal and oil. These unbelievable amounts of arsenic have the potential to set the stage for a catastrophe of mass extinction stature. Most arsenopyrite anomalies are biogenic and date back to Cambrian time [84]. It is
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intriguing to think of arsenic as a weapon of mass extinction when we have a rationale in the Cambrian mass extinctions and the arsenopyrite anomalies that have formed in those geological times as a result of microbial metabolism. People tend to oversee such appalling scenarios, as if they were unlikely or too distant from reality. However, a closer inspection of present day morbidity and mortality data shall reveal what appear to be inconvenient truths. The leading causes of morbidity and mortality worldwide are vascular diseases (including cardiovascular and cerebrovascular diseases), infectious diseases, cancer (particularly lung cancer), diabetes, diseases of the liver and kidneys, Alzheimer’s disease and other dementias [86]. All these conditions have been causally related to long-term exposure to arsenic [12,18,19,24,25,29,31,32,34,35,49,50,66,72,81,87–99]. With the exception of Alzheimer’s disease – the cause in most cases of which being thought of as ‘‘multiple” or as ‘‘a puzzle” much in the same way the proximate causes of the extinction of the dinosaurs are thought of as being beyond human comprehension, even after associations with arsenic have been found [57] – high risks and exposure-dose relationships have been observed for each of those end-points in studies of different design [24,25,28,29,31,32,34, 49,50,66,72,73,81,93,94,99]. I suspect it is just a matter of taking time, arsenic exposure- and tissue accumulation dynamics and inherited variations in susceptibilities into account in appropriate experimental designs, and Alzheimer’s disease shall be somehow related to long-term arsenic exposure too. Most importantly, it has been shown that arsenic accumulation has adverse impacts on reproductive fitness and reproductive outcomes [21–33] and early-age development and growth [21– 23,28,31,34,35] in a wide range of microbial, plant and animal species including man. This is important because reproductive age and early life fitness ultimately define the evolution of human adaptednesses such as encephalization and prolonged life-span, and consequentially intelligence and longevity [98–102]. Humans evolved into their present form during the Pleistocene [100,103– 106], coinciding with the final stages of a period of exacerbated tectonic activity (therefore a period of presumably high arsenic loads). In the beginning of the Pleistocene, australopithecine species of both human- and non-human ancestry are still present, but during the lower Palaeolithic many had disappeared [100,105]. Volcanism seems to have encouraged dispersal and migration of some early hominids – the clever ones, anyway, the ones who conceivably noticed they would die if they did nothing about a mysterious, invisible killing force – outside the main Ethiopian rift basins during major eruption interludes [105]. Rapid accelerations in the rate of encephalization in the hominid lineage and the emergence of Homo species were verified when subsidence in the Afar area was nearly complete [100,105,106]. Thus, the hypothesis of persistent arsenic concentrations which are above species-specific tolerance limits causing extinctions and setting the stage for cladogenesis should also apply to the hominid lineage. The experimental proof of this hypothesis is likely to affect modern humans in highly incredible ways. Chronic exposure to below lethal doses is sufficient to produce bodily arsenic accumulation and toxicity over the lifetime of reproducing individuals in a population (Figs. 2 and 3). As I have stated before, species-specific tolerance limits are set at the point where chronic accumulation of arsenic does not interfere with the specie’s reproductive success. Unhappily, this point seems to have been already trespassed in many localities and regions of the world [24–35,58,59,66,68,72,73,93–95,99]. In line with geological evidence as above discussed, persistent arsenic concentrations which are above species-specific thresholds are expected to cause extinctions and cladistic events with some degree of certainty at the local scale, and with less certainty at the global scale. Let us explore how this is expected to happen with the human species.
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Fig. 2. Arsenic accumulates in the human body with age, as observed by Raie [110] in a series of autopsied patients in Glasgow. The patients had no clinical sign of arsenicosis; they died from external causes, as accidents. Note that even in such sub-clinical settings, accumulated arsenic is found above FAO/WHO provisional maximum tolerable daily intake of inorganic arsenic (0.002 mg/kg of body weight) [67]. The accumulation curve proposed here to accommodate Raie’s data is compatible with the animal experimental model of Marafante and coworkers [107].
Invisible As and the fate of mankind: the hypothesis Proximate consequences of chronic anthropogenic input of arsenic into the human compartment include rises in morbidity and mortality from diseases for which long-term exposure to arsenic have been causally related, as above referenced. The higher the arsenic exposure levels, the higher and the earlier will be the impacts on health and economical status of the exposed populations (Fig. 3). Even populations which do not present clinical signs of arsenicosis [108–110] are at risk of arsenic co-morbidity and should be more closely watched for a better appraisal of what is going on. Given that arsenic removal from water, soils and air is prohibitively expensive, much will depend on the availability of feasible alternative resources, which are increasingly scarce. The best treatment strategy when symptoms start emerging is the provision of arsenic-free water, food and air which are becoming unfortunately scarce all over the world [111,112]. Global warming and global water shortage are likely to worsen these prospects, for temperature is one of the weathering factors which determine arsenic dissolution in water (Fig. 1). The mobilisation of arsenic is believed to be caused by oxidation of arsenic minerals such as arsenopyrite, exacerbated mostly by mining activities, but also by other industrial, household and agricultural activities. Recent arsenic appearances in groundwaters worldwide have occurred during post-mining, post-pumping groundwater rebounds [41–43,68,72,73,97,113,114]. The full epidemiological implications of arsenic contamination are only now emerging, and it is likely that over the coming decade more arsenicosis cases and arsenic-associated morbidities will be identified. Here I am interested in the impact of arsenic-related morbidity and mortality on human fitness. The hypothesis is this. Large scale arsenic poisoning of mankind has the potential to cause a rise in morbidity and mortality followed by adaptive changes. Adaptive changes include drops in human-specific adaptednesses, namely encephalization and longevity. These changes are likely to have far-reaching impacts on biological and cultural evolution of mankind.
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Fig. 3. A model for arsenic accumulation (top) and ‘‘survival” (bottom, here As% of the individuals in the original population who do not present any known endpoints of chronic arsenic toxicity which otherwise would affect reproductive fitness and long term survival) in aging human populations chronically exposed to increasing doses of toxic arsenic. Curves A–D represent theoretical arsenic accumulation (top) and population ‘‘survival” (bottom) for the following increasing exposures to arsenic (As in micrograms/day/individual): A, 12 ug/d/i; B, 15 ug/d/i; C, 20 ug/d/i; D, 38 ug/d/i. Note the exponential pattern of arsenic accumulation, i.e., small increases in daily exposure levels cause large increases in the bodily As concentrations and hence the upward shifts in the accumulation curves (top) and respective decline in survival (bottom). Accumulation curves B–D would not be verified for all individuals in the population because the most arsenic intolerant – which most people are – would die as bodily arsenic concentrations become lethal (LC50 = 1 mg/kg BW). There is an age-specific rise in morbidity and mortality associated with As accumulation; higher morbidity and mortality rates typically affect fetuses and young children because the highest rates of As accumulation occur during development; children and adults will be affected sooner or later in their lifetimes as a result of age-specific As accumulation and associated morbidities. For practical purposes, all exposed people are at risk of developing arsenicrelated pathologies or will have their age-specific fitness components deteriorated by arsenic exposure and accumulation, sooner or later in their lifetimes. All exposure levels (curves A–D) are within ‘‘safe”, ‘‘normal” or ‘‘acceptable” exposure limits.
Arsenic in the brain is associated with the lipid phase [115], where phospholipids and proteins exert their important roles on brain structure and metabolism. Chronic accumulation of arsenic in the human brain is related to impaired mental functions and neurological and psychological harms including mental retardation,
developmental disabilities such as physical, cognitive, psychological, sensory and speech impairments, and depression [116]. For practical reasons, we shall consider all these changes as functionally equivalent to a drop in encephalization. In extinct hominids, each change in encephalization goes hand-in-hand with changes in adaptability [102] and longevity [101], a process which has been generally associated with extinction of the less encephalized forms and evolution toward more encephalized forms over evolutionary time. Chronic arsenic poisoning has the potential to cause a decline of hardly won and nicely balanced human-specific adaptednesses, namely encephalization and prolonged life-span, and consequentially intelligence and longevity through the following biologically and socially different but complementary mechanisms. Larger brains and more encephalized fetuses and children are metabolically more demanding than smaller brains and less encephalized fetuses and children [100,101]. Altriciality, as opposed to precocity is a hallmark of more encephalized humans. It follows that relatively larger brains demand more food and water and air and time to get fully built up and instructed than relatively smaller brains. Unfortunately arsenic accumulation behaves much in the same fashion: it takes food and water and time into account. Therefore we can expect with some degree of certainty that more encephalized fetuses and children are metabolically bound to be more sensitive to arsenic contamination than the less encephalized. We can then expect families with more encephalized, long-lived members to suffer more from health and economic distresses caused by arsenic accumulation than families with less encephalized members. The health and economic burdens imposed upon families of more encephalized, more intelligent people through the ills of arsenic accumulation will cause them to be poorer. The most intelligent are going to have less children, while the less intelligent are going to have more, and have them earlier in their reproductive lives. Generation by generation, they will tend to have larger families than the more intelligent. Generation by generation, the more encephalized, intelligent and longer-lived families will eventually die out in the population. In summary, more encephalized fetuses and children will die most before reproduction and less encephalized children will have better reproductive advantages. If there are genetic differences in resistance to arsenic within human populations – and we know there are such differences [117] – the genetic structure of the population must clearly change with time and successive generations. Some adaptednesses may be lost in the process in order to maintain adaptability. However, inborn resistance to arsenic does not reveal any general soundness of humane constitution. As a result, the survivors of this evolutionary process led by arsenic will have to deal with all sorts of socio-environmental issues utilizing their less encephalized brains and lower intelligence, shorter life-spans and decreased longevities. There are lots of uncertainties involved in such predictions, but we should not stop making predictions of this degree of importance for fear of being wrong. It may well be the case that these predictions are wrong and we should expect the survivors of an arsenic catastrophe to be fitter and more intelligent, instead of short lived and stupid. Unfortunately this does not seem to be the general rule in the evolutionary schemes directed by arsenic. Instead, the inference we can draw from the study of arsenic resistance in a wide range of microbial, plant and animal species is that the arsenic-tolerant – those which are more arsenic tolerant than Homo sapiens, anyway – are less biologically and sociologically complex than humans. We should not forget that bursts of encephalization in the human lineage occurred outside the places of intense tectonism, consequentially outside the places and times of supposedly high arsenic concentrations [100,102–106].
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We know enough to be able to say that waiting for a general innate arsenic resistance to naturally obtrude in the human lineage – instead of stamping out anthropogenic arsenic itself – is a risky, wasteful and foolish enterprise. As pointed out by Peter Medawar [118], those who accept natural selection of man as a natural solution of the problem of a disfavorable environment are up to mischief; ‘‘they reveal their misunderstanding of Nature, of man’s place in Nature, and of the nature of man.” Humans seek out and store and use gold, coal and oil as if they were energetic foods, as if these stuffs would enhance survival through periods of fast and famine and economic distress; however in doing so humans are traveling just in opposite way as we would have planned or instinctively wanted. In seeking out these stuffs we are building up arsenic stores that threaten the survival of millions – perhaps billions – in the long run. It is becoming increasingly clear that gold, coal and oil are being seek out and stored, bought and sold, and wear or consumed at the expense of our biological fitness. There is no reason to believe that the worldwide protection of the environment from continuing anthropogenic arsenic contamination would have economically negative effects. On the contrary, there is every reason to believe that failure to adopt some measures of control and limitation of anthropogenic arsenic input into the biosphere will lead, in the long run, to diseases, deaths, misery, privation and economic distress. In what seems to be a danger according to present-day evidence and thinking, arsenic is likely to affect our most important evolutionary achievements, namely encephalization and prolonged life-span and consequentially intelligence and longevity. There is thus enough reason to believe that to mobilize arsenic from arsenopyrite, the principal ore of arsenic in thousands of gold mines scattered all over the world is a risky business; it is equivalent to travel the opposite sense in the direction anthropologists tell us we have been traveling during the last 2.5 million years [100].
A final note or warning For better clarity and general tranquility, I should state at the outset of this conclusion section that extinction is rather the rule than the exception in the wasteful schemes of natural evolution. This statement is not intended to console the reader by recalling that sooner or later everyone is going to die anyway. Instead, it is intended to call attention to the question as to whether it makes any sense to jeopardize global health and quality of life for gold, coal and oil. With our global perspective, there comes a global responsibility toward our species and the many more living creatures with which we share our planet. I believe mankind must try and find a humane solution for the problem of anthropogenic arsenic, before our very existence as a species deteriorates. If there are ways to prevent such an outcome, we should find them. Science can help in many ways. For example, natural sources of arsenic contamination can be predicted by geological surveys [36,68] thereby creating the possibility to avoid the de novo arsenic release from those sources. However, science alone is not likely to produce any positive results unless a global change in human behavior takes place. A worldwide concerted action has to be undertaken as to halt the deliberate anthropogenic contamination of the planet and our bodies with arsenic, in similar though hopefully more efficient ways as has been done with the control of CO2 emissions. Or shall there be any reason or hope to believe or to want that some new sort of arsenichypertolerant, intelligent hominid shall evolve from scratch again? As stated at the outset, the first organized entity of life was a composite structure around a growing cluster of pyrite [1–3]. This
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initial organization provided the ‘‘anlage” for evolution by autocatalytic expansion of carbon-fixation pathways with an inherent tendency toward an increasing number of reaction possibilities [1]. As pointed out by Günter Wächtershäuser [1], this inherent tendency to evolve toward higher complexity creates life’s own prospects, and provides the physical basis for the interpretation of evolution as a process of self-liberation. At this point I should finish by quoting one of Sir Peter Medawar’s thoughts: ‘‘The inference we can draw from an analytical study of the differences between ourselves and other animals is surely this: that the bells which toll for mankind are – most of them, anyway – like the bells on Alpine cattle; they are attached to our own necks, and it must be our fault if they do not make a cheerful and harmonious sound [118].” Conflicts of interest statement None declared. Acknowledgements The author wishes to thank P.M. Serrano Neves and B.C. Dani for discussions; C.D. Gama for suggestions; M.A.C. Dani and S.C. Dani for support. References [1] Wächtershäuser G. Life in a ligand sphere. Proc Natl Acad Sci USA 1994;91:4283–7. [2] Wächtershäuser G. From volcanic origins of chemoautotrophic life to bacteria, archaea and eukarya. Philos Trans R Soc Lond B Biol Sci 2006;361:1787–806. discussion 1806–8. [3] Wächtershäuser G. On the chemistry and evolution of the pioneer organism. Chem Biodivers 2007;4:584–602. [4] Vaughan DJ. Arsenic. Elements 2006;2:71–5. [5] Hurlbut CS, Klein C. Manual of mineralogy. 20th ed. New York: John Wiley and Sons; 1985. p. 285–6. [6] O’Neil P. Arsenic. In: Alloway BJ, editor. Heavy metals in soils. London: Blackie; 1995. p. 107–21. [7] Naranmandura H, Ibata K, Suzuki KT. Toxicity of dimethylmonothioarsinic acid toward human epidermoid carcinoma A431 cells. Chem Res Toxicol 2007;20:1120–5. [8] Hanaoka K, Kogure T, Miura Y, Tagawa S, Kaise T. Post-mortem formation of inorganic arsenic from arsenobetaine in a shark under natural conditions. Chemosphere 1993;27:2163–7. [9] Tamaki S, Frankenberger Jr WT. Environmental biochemistry of arsenic. Rev Environ Cont Toxicol 1992;124:79–110. [10] Rosen BP. Biochemistry of arsenic detoxification. FEBS Lett 2002;529:86–92. [11] Bernstam L, Nriagu J. Molecular aspects of arsenic stress. J Toxicol Environ Health B Crit Rev 2000;3:293–322. [12] Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chemico-Biol Interact 2006;160:1–40. [13] Ilyaletdinov AN, Abdrashitova SA. Autotrophic oxidation of arsenic by a culture of Pseudomonas arsenitoxidans. Mikrobiologiya 1981;50:197–204. [14] Ahmann D, Roberts AL, Krumholz LR, Morel FMM. Microbe grows by reducing arsenic. Nature 1994;371:750. [15] Lebrun E, Brugna M, Baymann F, Muller D, Lièvremon D, Lett MC, et al. Arsenite oxidase, an ancient bioenergetic enzyme. Mol Biol Evol 2003;20:686–93. [16] Jackson CR, Dugas SL. Phylogenetic analysis of bacterial and archaeal arsC gene sequences suggests an ancient, common origin for arsenate reductase. BMC Evol Biol 2003;3:18. [17] Muller D, Médigue C, Koechler S, et al. A tale of two oxidation states: bacterial colonization of arsenic-rich environments. PLoS Genet 2007;3:e53. [18] Schmuck EM, Board PG, Whitbread AK, Tetlow N, Cavanaugh JA, Blackburn AC, et al. Characterization of the monomethylarsonate reductase and dehydroascorbate reductase activities of Omega class glutathione transferase variants: implications for arsenic metabolism and the age-atonset of Alzheimer’s and Parkinson’s diseases. Pharmacogenet Genom 2005;15:493–501. [19] Coppin JF, Qu W, Waalkes MP. Interplay between cellular methyl metabolism and adaptive efflux during oncogenic transformation from chronic arsenic exposure in human cells. J Biol Chem 2008;283:19342–50. [20] Baker-Austin C, Dopson M, Wexler M, Sawers RG, Stemmler A, Rosen BP, et al. Extreme arsenic resistance by the acidophilic archaeon ‘Ferroplasma acidarmanus’ Fer1. Extremophiles 2007;11:425–34.
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