Duarte (2014) - Red Ochre and Shells Clues To Human Evolution. Review Article. Trends in Ecology & Evolution, Volume 29, Issue 10, October, Pages 560-565
Duarte (2014) - Red Ochre and Shells Clues To Human Evolution. Review Article. Trends in Ecology & Evolution, Volume 29, Issue 10, October, Pages 560-565
Duarte (2014) - Red Ochre and Shells Clues To Human Evolution. Review Article. Trends in Ecology & Evolution, Volume 29, Issue 10, October, Pages 560-565
The UWA Oceans Institute and School of Plant Biology, University of Western Australia, 35 Stirling Highway, Crawley 6009,
Australia
2
Department of Global Change Research. IMEDEA (CSIC-UIB) Instituto Mediterraneo de Estudios Avanzados, Miquel Marques 21,
07190 Esporles, Spain
560
Opinion
250
50 *
250*
12
23
80
0.5
1.8
92
135
10
5
35
3
40
12
160
Key:
Historical evidence
Paleoanthropological evidence (* = Neanderthals)
TRENDS in Ecology & Evolution
Figure 1. Reports of the joint use of red ochre and shells by humans are rapidly growing in number [40], including reports for both modern humans and Neanderthals
(asterisks). Existing records track the reconstructed dispersal of modern humans, including findings of the joint use of red ochre and shells in Africa, Eurasia, Australia, and
America, ranging from paleorecords starting in 250 ka (red arrows, paleorecords) to present (blue arrows, historical records, Box 1). For paleoanthropological evidence, the
numbers show the dates in ka, where reported [40]. When multiple reports were available for a given region, the oldest one is shown.
ochre (Box 2). Whereas ferric iron forms present low bioavailability, ferric iron forms present in red ochre, other
than hematite, can be assimilated, particularly when combined with protein (Box 2). Indeed, ferric forms present in
red ochre, such as ferrihydrate and maghemite, are used in
pharmaceutical products to treat iron deficiency anemia in
humans (Box 2). Iron deficiency anemia remains a serious
heath issue affecting humans, particularly women, in both
developed and developing nations, increasing the risk for
preterm labor and infant mortality, and accounting for
much of maternal deaths during pregnancy and childbirth
[24,25]. Today, approximately 70% of women emerging
from pregnancy suffer iron deficiency anemia [24,25].
Two iron-rich proteins, the oxygen transport protein
hemoglobin, and the iron storage protein ferritin, which
account for 70% and 25% of the iron in the human body,
respectively, play a key role in brain health and function
[26,27]. Hemoglobin carries oxygen from the lungs to the
brain, which accounts for 20% of the total oxygen consumption with only 2% of body weight [24,26], and a smaller
share of the metabolically-active mass. Iron supply-supporting loads of hemoglobin to satisfy brain oxygen
requirements is, as is that of omega 3 and DHA, particularly critical during the early development of the brain
[24,26]. Ferritin, particularly enriched in the human brain
(30% of total ferritin) [27], plays a role in storing and
releasing iron, buffering against iron deficiency and overload, and is particularly important for brain iron homeostasis and health [2428]. Inside the ferritin shell, iron ions
form crystallites similar to the mineral ferrihydrite, an
iron oxide present in red ochre (Box 2). Therefore, red ochre
can be, depending on the fraction of metastable sources and
mixing with foods, a source of iron that can be stored in
ferritin in the human brain, supplying iron where necessary to maintain adequate levels of hemoglobin and, therefore, oxygen supply for brain function.
561
Opinion
(A)
(B)
dust their faces with powdered ochre. The New Zealanders. . . usually
use it in an oily paste, which they smear on their foreheads and their
hair. . . on feast days a New Zealander does not think he has carried
out a full toilette until he has anointed his whole body, and especially
his face and hair, with fish oil and ochre.
The Western culture is no exception and has continued to use
shells and red ochre to ornate their bodies to date. The ornamental
use of shells and red ochre as make up has been documented in all
ancient cultures, from ancient Mesopotamia, Egypt and Greece, to
Rome [43]. Noble women in the Roman empire used red ochre
extensively in their make up, leading Plautus to assert that, A
woman without paint is like food without salt. Indeed, classical
Romans called the most powerful men in the city coccinati, the
ones who wear red, and the color red signaled at status and power
across a broad range of societies [21]. Portraits show a continuity in
the use of red ochre make up by western women (Figure IB).
Indeed, red ochre, currently reported as FDA-approved cosmetic
Pigment Red 101, remains a key element of modern womens make
up and is present in a broad range of cosmetic products, often worn
along with nacre and pearl jewelry from oysters and other bivalves
(Figure IC).
(C)
Figure I. (A) Photos of the skeleton of a young man dated 23.4 ka, know as Il Principe, showing the perforated shell cap and mass of ochre between the left clavicle and
mandible. (B) A portrait of Marie Antoinette, showing red ochre make up. (C) A young woman wearing hematite, red ochre, pigmentation and shell ornaments. Photos
reproduced with permission from Antiquity Publications Ltd from a figure printed in [41] (A), and Carlos M. Duarte (C).
Opinion
Box 2. Can iron in red ochre be assimilated?
Whether the handling and accidental use of red ochre, alone or
when mixed with bone marrow and other foods, is conducive to iron
assimilation remains to be tested directly, a test that could involve
examination of the iron status of indigenous cultures that continue
to use red ochre in their traditional practices. Most of the iron
contained in red ochre occurs as hematite (aFe2O3), a stable,
oxidized form of iron that is insoluble and which is believed to be
unavailable [44]. However, red ochre also contains variable proportions of other, nonheme meta-stable forms of iron, such as:
ferrihydrite, magnetite, and maghemite [4547], particularly when
depositing under acidic pH [48] as reported in the Kokowai Springs
exploited by Maori, where ferrihydrite is the dominant iron form
[45]; in the materials used in the Pecos River rock paintings [46]; in
artifacts found in Malawi [49]; or in Pinnacles Cave, South Africa
[50]. These metastable forms of iron are bioavailable, although with
variable assimilation efficiency, depending on factors such as the
relative amounts of chelators and ligands (e.g., phytate and citrate),
pH, the amounts of reducing compounds ingested, and pre-heating
[44,51]. Mixing of ferrihydrate with food, as documented in early
uses [8], would be particularly effective, as ferrihydrate would be
coated with protein to yield a ferritin analog [52,53]. Indeed, the
paradigm of iron absorption is shifting due to recent developments
in nanomedicine providing evidence that the dissolution of
ferrihydrate may not be necessary for absorption to take place
[53]. This knowledge has been used recently to develop ferrihydritebased [53] and maghemite-based [54] supplements, combining
these forms of iron with ligands, to fortify foods and are included in
iron-based parenteral drugs used to treat iron deficiency anemia,
such as Ironate1 and Feraheme1 [55].
Opinion
kind. The sharp rise in brain disorders, which, in many
developed countries, involves social costs exceeding those
of heart disease and cancer combined, has been deemed the
most worrying change in disease pattern in modern societies, calling for urgent consideration of seafood requirements to supply the omega 3 and DHA required for brain
health [15]. Likewise, iron deficiency is the most common
form of malnutrition in the world, affecting more than 2
billion people globally [24,25]. These disorders affect
humans across developed and developing nations. In conclusion, the deep and sustained connection between human use of red ochre and shells summarized here delivers a
new perspective on the role of seafood and iron nutrition on
the health of the human brain and human fitness, critical
to both understanding our past evolution and addressing
our future health challenges.
Acknowledgments
I thank J. Erlandson for useful comments, G. Duarte for help with
Box 1, and N. Faria, G. Anderson, E.C. Theil, and C. Hutchinson for
advice on Box 2.
References
1 Marean, C.W. et al. (2007) Early human use of marine resources and
pigment in South Africa during the Middle Pleistocene. Nature 449,
905908
2 Balter, M. (2009) Early start for human art? Ochre may revise timeline.
Science 323, 569
3 Ramos, J. et al. (2011) Marine resources exploitation by Palaeolithic
hunterfishergatherers and Neolithic tribal societies in the historical
region of the Strait of Gibraltar. Quaternary Int. 239, 104113
4 dErrico, F. and Stringer, C.B. (2011) Evolution, revolution or saltation
scenario for the emergence of modern cultures? Philos. Trans. R. Soc. B
366, 10601069
5 Roebroeks, W. et al. (2012) Use of red ochre by early Neanderthals.
Proc. Natl. Acad. Sci. U.S.A. 109, 18891894
6 Bouzouggar, A. et al. (2007) 82,000-year-old shell beads from North
Africa and implications for the origins of modern human behavior.
Proc. Natl. Acad. Sci. U.S.A. 104, 99649969
7 Bar-Yosef Mayer, D.E. et al. (2009) Shells and ochre in Middle
Paleolithic Qafzeh Cave, Israel: indications for modern behavior. J.
Hum. Evol. 56, 307314
8 Henshilwood, C.S. et al. (2011) A 100,000-year-old ochre-processing
workshop at Blombos Cave, South Africa. Science 334, 219222
9 Marean, C.W. (2010) When the sea saved humanity. Sci. Am. 303, 5461
10 Zilhao, J. et al. (2010) Symbolic use of marine shells and mineral
pigments by Iberian Neanderthals. Proc. Natl. Acad. Sci. U.S.A.
107, 10231028
11 Mellars, P. (2006) Going east: new genetic and archaeological
perspectives on the modern human colonization of Eurasia. Science
313, 796800
12 Broadhurst, C.L. et al. (2002) Brain-specific lipids from marine,
lacustrine, or terrestrial food resources: potential impact on early
African Homo sapiens. Comp. Biochem. Physiol. B: Biochem. Mol.
Biol. 131, 653673
13 Gomez-Pinilla, F. (2008) Brain foods: the effects of nutrients on brain
function. Nat. Rev. Neurosci. 9, 568578
14 Bradbury, J. (2011) Docosahexaenoic acid (DHA): an ancient nutrient
for the modern human brain. Nutrients 3, 529554
15 Crawford, M.A. and Broadhurst, C.L. (2012) The role of
docosahexaenoic and the marine food web as determinants of
evolution and hominid brain development: the challenge for human
sustainability. Nutr. Health 21, 1739
16 Delange, F. (2001) Iodine deficiency as a cause of brain damage.
Postgrad. Med. J. 77, 217220
17 Berbel, P. et al. (2007) Iodine supplementation during pregnancy: a
public health challenge. Trends Endocrinol. Metabol. 18, 338343
18 Schrauzer, G.N. (2002) Lithium: occurrence, dietary intakes,
nutritional essentiality. J. Am. Coll. Nutr. 21, 1421
564
Opinion
49 Zipkin, A.M. et al. (2014) Ochre fingerprints: distinguishing
among Malawian mineral pigment sources with Homogenized
Ochre Chip LAICPMS. Archaeometry http://dx.doi.org/10.1111/
arcm.12090
50 Watts, I. (2010) The pigments from Pinnacle Point Cave 13B, Western
Cape, South Africa. J. Hum. Evol. 59, 392411
51 Zhao, G. (2010) Phytoferritin and its implications for human health
and nutrition. Biochim. Biophys. Acta 1800, 815823
52 Faria, N. et al. (2011) Ligand doping of iron oxide nanoparticles as an
approach to novel oral iron therapeutics. In 11th IEEE Conference on
Nanotechnology (IEEE-NANO). pp. 837840 IEEE
565