Content uploaded by Karen Hardy
Author content
All content in this area was uploaded by Karen Hardy on Oct 21, 2018
Content may be subject to copyright.
Content uploaded by Michael Alan Huffman
Author content
All content in this area was uploaded by Michael Alan Huffman on Jan 29, 2014
Content may be subject to copyright.
Content uploaded by Michael Alan Huffman
Author content
All content in this area was uploaded by Michael Alan Huffman on Jan 28, 2014
Content may be subject to copyright.
Content uploaded by Michael Alan Huffman
Author content
All content in this area was uploaded by Michael Alan Huffman
Content may be subject to copyright.
Debate
Neanderthal self-medication in context
Karen Hardy1, Stephen Buckley2& Michael Huffman3
Introduction
In a recent study, Hardy et al. (2012) identified compounds from two non-nutritional
plants, yarrow and camomile, in a sample of Neanderthal dental calculus from the northern
Spanish site of El Sidr´
on. Both these plants are bitter tasting and have little nutritional
value but are well known for their medicinal qualities. Bitter taste can signal poison. We
know that the bitter taste perception gene TAS2R38 was present among the Neanderthals
of El Sidr´
on (Lalueza-Fox et al. 2009), and their selection of yarrow and camomile was
hence probably deliberate. With few nutritional benefits, reasons must be sought for why
the Neanderthals collected and ingested these plants. They could have consumed them
as flavouring, but this presupposes a degree of complexity in cuisine for which there is
little evidence. The widespread evidence for animal self-medication, or zoopharmacognosy,
however, offers an attractive behavioural context. We propose, indeed, that these plants were
selected and ingested deliberately for the purpose of self-medication. Here, we investigate the
implications of this new finding for Neanderthal knowledge of plants and we offer a context
for plant knowledge and self-medication among early human and hominin populations.
Plant remains rarely survive at early prehistoric sites and for many years absence of
evidence was largely understood to mean evidence of absence. The lack of evidence for
plants, together with the large numbers of animal bones found on many sites (Burke 2000),
led to a perspective on Neanderthal diet that was dominated by meat. This appeared to
be consolidated by stable isotope analyses since the δ15N values were consistent with a
meat-rich diet (Bocherens 2009; Richards & Trinkaus 2009). The potential contribution of
plant foods has not, however, been investigated in stable isotope analyses of Neanderthal diet
(Trinkaus in Barras 2012). Furthermore, although this method is widely used as a primary
indicator of diet, a proportion of the diet can consist of plants without being visible in
the stable isotope signal (Jones 2009). A new perspective on Neanderthal diet is offered by
the increasing numbers of plant remains recovered from sites and by the development of
microscopic and biomolecular techniques which are revealing new evidence for plant foods.
We are little further forwards, however, in understanding the extent of plant consumption.
The Neanderthal occupation at El Sidr´
on dates to between 47 300 and 50 600 BP (Wood
et al. 2013). This places it in a relatively mild climatic period (Van Andel 2003) and most
probably a deciduous forested environment (Huntley & Allen 2003). In addition to yarrow
and camomile, the dental calculus study identified an oil shale or bitumen source, a range
of different carbohydrates, evidence for cooking, what may have been green vegetables and
1ICREA, Department of Prehistory, Universitat Aut`
onoma de Barcelona, Bellaterra, 08193 Barcelona, Spain
(Email: khardy@icrea.cat)
2BioArch, University of York, York YO10 5DD, UK (Email: sb55@york.ac.uk)
3Primate Research Institute, Kyoto University, Inuyama, Aichi 484, Japan (Email: huffman@pri.kyoto-u.ac.jp)
C
Antiquity Publications Ltd.
ANTIQUITY 87 (2013): 873–878 http://antiquity.ac.uk/ant/087/ant0870873.htm
873
Neanderthal self-medication in context
nuts, and inhalation of wood smoke or smoked food, but no evidence for meat ingestion
despite evidence for collagen survival (Hardy et al. 2012).
Yarrow is a flowering plant in the Asteraceae family, common across temperate regions.
It was used as a vegetable in the Middle Ages, notably as a component of soup, but has
an extended history of medicinal use, in particular as an astringent (Chandler et al. 1982).
Camomile tea is well-known today as an aid for stomach complaints and nervousness,
though there is little record of it as a food. Bioactive constituents are linked to antimicrobial
and anti-inflammatory properties (McKay & Blumberg 2006), while its ability to assist with
general anxiety disorder has been demonstrated (Jay et al. 2009).
The same qualities that make plants medicinal can also make a plant poisonous and
are caused by plant secondary compounds (PSCs). These are complex chemicals that
are not essential to the life of the plant. The many thousands of PSCs that exist have
numerous roles, among them the production of pigments and flavouring substances which
are used in cooking. PSCs also include many and diverse natural toxins that act as pesticides
and anti-grazing agents (Fraenkel 1959). Bitter taste is linked to certain plant secondary
compounds, and bitterness can warn of toxins. Possession of the bitter taste perception gene
TAS2R38, which permits individuals to taste the bitter compound phenylthiocarbamide
(PTC), suggests a predisposition to plant eating (Miller 2011) because the bitter taste can
prevent ingestion of potentially toxic substances (Kim & Drayna 2004).
Charred edible plant remains have been found on several Neanderthal sites (Jones 2009)
and plant microfossils have been found in samples of Neanderthal dental calculus (Henry
et al. 2011; Hardy et al. 2012). While there is no doubt that Neanderthals ate substantial
amounts of meat (Bocherens 2009), they were not obligate carnivores. This means they had
to consume something other than meat to counter the high levels of nitrogen which are
generated by a high-meat diet (Jones 2009; Hardy 2010).
All animals except obligate carnivores consume plants to a greater or lesser extent and
have mechanisms for avoiding toxic PSCs. Wild herbivores avoid certain foods and have
metabolic mechanisms to break down or excrete toxins (Freeland & Janzen 1974). Among
higher primates, gorillas have enlarged colons which enable higher rates of fermentation
to accommodate a fibrous diet of low quality plant fibres and greater processing of
indigestible plant secondary compounds than smaller bodied apes (Remis et al. 2001;
Leonard et al. 2007). Humans and other higher primates deal with toxins either by
avoidance or through processing. That processing may be conducted in the mouth, for
example through bitter pith chewing or wadging (Huffman & Seifu 1989; Huffman et al.
1993) or geophagy (Mahaney et al. 2005; Klein et al. 2008). Alternative strategies are ‘timely
dextrous unpacking’ including peeling and removal of spines, and ‘ecological intelligence’
(Jones 2009) that allows understanding of when a plant or part of a plant is at its most
edible. Among human populations, food processing is largely conducted using external
mechanisms. When cooking developed is unknown, but control of fire is certain by
300 000–400 000 years ago (Roebroeks & Villa 2011) and possibly significantly earlier
(Carmody & Wrangham 2009), while grinding tools have been recorded at Middle (Van
Peer et al. 2003) and Upper (Aranguren et al. 2007) Palaeolithic sites. Less visible processing
methods such as cleaning, peeling, soaking, drying, leaching, salting and fermenting leave no
trace but are likely to have a long history and are still widely used in food preparation today.
C
Antiquity Publications Ltd.
874
Debate
Karen Hardy, Stephen Buckley & Michael Huffman
The care that is needed in the selection and ingestion of plants so as to exclude noxious
secondary compounds is essential for survival and requires methods of knowledge transfer.
Observation by infants of their mothers’ feeding behaviour is an early mechanism of
knowledge acquisition (see Huffman & Seifu 1989 for the self-medication context). Socially
influenced copying of conspecifics among adults has also been observed among several
populations of chimpanzees (Huffman & Hirata 2004; Huffman et al. 2010).
In the hominin lineage, the fossil evidence from around 1.8 million years ago indicates a
reduction in gut size linked to important changes in the diet with the emergence of Homo
erectus (Aiello & Wheeler 1995; Snodgrass et al. 2009). This led to greater efficiency in
processing and digesting food but it also reduced the capability to process and expel toxic
PSCs. An increasing sophistication in plant knowledge would have been indispensable from
that stage.
Johns (1990) and Huffman (2001) propose that plant processing techniques thereafter
came to play an increasingly important role. Cooking and other processing methods help
to make food safer, more palatable and more digestible (Carmody & Wrangham 2009;
Jones 2009) as well as reducing the effects of toxic PSCs and tannins. The development of
language may have speeded the flow of information and ideas. This will have resulted in an
increasingly complex knowledge not only of plants but also of their effectiveness in treating
ailments, and the processing and preparation methods that could reduce the effects of toxins
and make plants more digestible (Huffman 2001; Cousins & Huffman 2002).
Self-medication
Animal self-medication or zoopharmacognosy (Rodriguez & Wrangham 1993) is a huge
subject that remains little studied (Engel 2002), but it is clear that most animals from
caterpillars (Singer et al. 2009) to higher primates (Wrangham 1995; Huffman 1997)
practise some degree of self-medication. Parasite expulsion is a primary reason to self-
medicate for many species, but evidence also suggests that a wide range of illnesses could
be treated, given the diversity of bioactivities found in many of the plant items ingested
(Huffman 2001, 2003; Cousins & Huffman 2002; Krief et al. 2006; Masi et al. 2012).
Identifying deliberate self-medication in animals can be challenging since many food
plants also have medicinal qualities and the boundaries between food and medicine can at
times be hazy (Huffman 1997). When they are in their known environment, animals are
able to keep themselves and their offspring in good health by selecting the ‘right’ things to
eat, which may be specifically chosen to address a health problem (Engel 2002).
Neanderthals must also have selected self-medicating plants when they needed them.
They lived in widely fluctuating climatic and environmental regimes with great variability
in plant and animal resources. Berries, roots and nuts are good cold climate sources of plant
food (Nelson 1899; Jones 2009; Hardy 2010); warmer climates will have provided an even
greater availability of edible plant foods. Neanderthals also had the genetic capability for
language (Krause et al. 2007), practised food processing techniques and probably engaged
in conspecific care (Hublin 2009). Their ability to taste, select and use bitter-tasting plants
indicates a sophisticated knowledge which fits into the continuum of acquired, essential
know-how that occurs very widely across the animal kingdom.
C
Antiquity Publications Ltd.
875
Neanderthal self-medication in context
Though all primates (and other animals) have varying levels of enzymes which make us
more or less tolerant of certain toxins, there are plants which are poisonous to all; in order
to survive, hominins needed to know which plants not to eat and how and when to eat
those plants they selected. The use of edible bitter tasting plants by the Neanderthals of El
Sidr´
on suggests their knowledge was sufficiently refined to use plants with confidence even
when their bitter taste warned of potential toxicity. This demonstrates that their knowledge
of plants was at least equal to today’s higher primates; with their additional linguistic and
technological abilities it may have been far more elaborate. Rather than contradicting the
extensive evidence for consumption of meat, the evidence for the use of plants adds a rich
new dimension to our developing knowledge of Neanderthal life. We can never know for
sure why yarrow and camomile were ingested at El Sidr´
on, but we propose that the evidence
for self-medication offers the most convincing behavioural context.
References
AIELLO,L.&P.WHEELER. 1995. The expensive-tissue
hypothesis: the brain and the digestive system in
human and primate evolution. Current
Anthropology 36: 199–211.
ARANGUREN, B., R. BECATTINI,M.M.LIPPI &A.
REVEDIN. 2007. Grinding flour in Upper
Palaeolithic Europe (25 000 years BP). Antiquity
81: 845–55.
BARRAS, C. 2012. Neanderthal dental tartar reveals
evidence of medicine. New Scientist, 18 July 2012.
Available at: http://www.newscientist.com/
article/dn22075-neanderthal-dental-tartar-reveals-
evidence-of-medicine.html (accessed 26 April
2013).
BOCHERENS, H. 2009. Neanderthal dietary habits:
review of the isotopic evidence, in J.-J. Hublin &
M.P. Richards (ed.) The evolution of hominin diets:
integrating approaches to the study of Palaeolithic
subsistence: 241–50. Dordrecht: Springer.
BURKE, A. 2000. Hunting in the Middle Palaeolithic.
International Journal of Osteoarchaeology 10:
281–85.
CARMODY,R.N.&R.W.WRANGHAM. 2009. The
energetic significance of cooking. Journal of Human
Evolution 54: 379–91.
CHANDLER, R.F., S.N. COOPER &M.J.HARVEY. 1982.
Ethnobotany and phytochemistry of yarrow,
Achillea millefolium, compositae. Economic Botany
36: 203–23.
COUSINS, D. & M.A. HUFFMAN. 2002. Medicinal
properties in the diet of gorillas: an
ethno-pharmacological evaluation. African Study
Monographs 23: 65–89.
ENGEL, C. 2002. Wild health. New York:
Houghton-Mifflin.
FRAENKEL, G.S. 1959. The raison d’ˆ
etre of secondary
plant substances. Science 129: 1466–70.
FREELAND,W.J.&D.H.JANZEN. 1974. Strategies in
herbivory by mammals: the role of plant secondary
compounds. The American Naturalist 108: 269–89.
HARDY, B.L. 2010. Climatic variability and plant food
distribution in Pleistocene Europe: implications for
Neanderthal diet and subsistence. Quaternary
Science Reviews 29: 662–79.
HARDY,K.,S.BUCKLEY,M.J.COLLINS,A.ESTALRRICH,
D. BROTHWELL,L.COPELAND,A.
GARC´
IA-TABERNERO,S.GARC´
IA-VARGAS,M.DE LA
RASILLA,C.LALUEZA-FOX,R.HUGUET,M.BASTIR,
D. SANTAMAR´
IA,M.MADELL A,A.FERN ´
ANDEZ
CORT´
ES &A.ROSAS. 2012. Neanderthal medics?
Evidence for food, cooking and medicinal plants
entrapped in dental calculus. Naturwissenschaften
99: 617–26.
HENRY, A.G., A.S. BROOKS &D.R.PIPERNO. 2011.
Microfossils in calculus demonstrate consumption
of plants and cooked foods in Neanderthal diets
(Shanidar III, Iraq; Spy I and II, Belgium).
Proceedings of the National Academy of Sciences of the
USA 108: 486–91.
HUBLIN, J.-J. 2009. The prehistory of compassion.
Proceedings of the National Academy of Sciences of the
USA 106: 6429–30.
HUFFMAN, M.A. 1997. Current evidence for
self-medication in primates: a multidisciplinary
perspective. Yearbook of Physical Anthropology 40:
171–200.
– 2001. Self-medicative behavior in the African great
apes: an evolutionary perspective into the origins of
human traditional medicine. BioScience 51:
651–61.
– 2003. Animal self-medication and ethnomedicine:
exploration and exploitation of the medicinal
propertiesofplants.Proceedings of the Nutrition
Society 62: 371–81.
C
Antiquity Publications Ltd.
876
Debate
Karen Hardy, Stephen Buckley & Michael Huffman
HUFFMAN, M.A. & S. HIRATA. 2004. An experimental
study of leaf swallowing in captive
chimpanzees—insights into the origin of a
self-medicative behavior and the role of social
learning. Primates 45: 113–18.
HUFFMAN, M.A. & M. SEIFU. 1989. Observations on
the illness and consumption of a possibly medicinal
plant Vernonia amygdalina by a wild chimpanzee in
the Mahale Mountains, Tanzania. Primates 30:
51–63.
HUFFMAN, M.A., S. GOTOH,D.IZUTSU,K.KOSHIMIZU
&M.S.KALUNDE. 1993. Further observations on
the use of the medicinal plant Vernonia amygdalina
(Del) by a wild chimpanzee, its possible effect on
parasite load, and its phytochemistry. African Study
Monographs 14: 227–40.
HUFFMAN, M.A., C. SPIEZIO,A.SGARAVATTI & J.-B.
LECA. 2010. Option biased learning involved in the
acquisition and transmission of leaf swallowing
behavior in chimpanzees (Pan troglodytes)? Animal
Cognition 13: 871–80.
HUNTLEY,B.&J.R.M.ALLEN. 2003. Glacial
environments III: paleovegetation patterns in late
glacial Europe, in T.H. Van Andel & W. Davies
(ed.) Neanderthals and modern humans in the
European landscape during the last glaciation:
archaeological results of the Stage 3 Project
(McDonald Institute Monographs): 79–102.
Cambridge: McDonald Institute of Archaeology.
JAY,D.,Y.LI,I.SOELLER,K.ROCKWELL,J.J.MAO &
J. SHULTS. 2009. A randomized, double-blind,
placebo-controlled trial of oral Matricaria recutita
(chamomile) extract therapy for generalized anxiety
disorder. Journal of Clinical Psychopharmacology 29:
378–82.
JOHNS, T. 1990. With bitter herbs they shall eat it.
Tucson: University of Arizona Press.
JONES, M. 2009. Moving north: archaeobotanical
evidence for plant diet in Middle and Upper
Paleolithic Europe, in J.-J. Hublin & M.P. Richards
(ed.) The evolution of hominin diets: integrating
approaches to the study of Palaeolithic subsistence:
171–80. Dordrecht: Springer.
KIM,U.K.&D.DRAYNA. 2004. Genetics of individual
differences in bitter taste perception: lessons from
the PTC gene. Clinical Genetics 67: 275–80.
KLEIN,N.,F.FR¨
OHLICH &S.KRIEF. 2008. Geophagy:
soil consumption enhances the bioactivities of
plants eaten by chimpanzees. Naturwissenschaften
95: 325–31.
KRAUSE,J.,C.LALUEZA-FOX,L.ORLANDO,W.ENARD,
R.E. GREEN, H.A. BURBANO,J.-J.HUBLIN,J.
BERTRANPETIT,C.H
¨
ANNI,M.DE LA RASILLA,
J. FORTEA,A.ROSAS &S.P
¨
A¨
ABO. 2007. The
derivedFOXP2variantofmodernhumanswas
shared with Neanderthals. Current Biology 17:
1908–12.
KRIEF, S., M.A. HUFFMAN,T.S
´
EVENET, T.C.-M.
HLADIK,P.GRELLIER,P.M.LOISEAU &R.W.
WRANGHAM. 2006. Bioactive properties of plant
species ingested by chimpanzees (Pan troglodytes
schweinfurthii) in the Kibale National Park, Uganda.
American Journal of Primatology 68: 51–71.
LALUEZA-FOX,C.,E.GIGLI,M.DE LA RASILLA,J.
FORTEA &A.ROSAS. 2009. Bitter taste perception
in Neanderthals through the analysis of the
TAS2R38 gene. Biology Letters 5: 809–11.
LEONARD, W.R., J.J. SNODGRASS &M.L.ROBERTSON.
2007. Effects of brain evolution on human
nutrition and metabolism. Annual Review of
Nutrition 27: 311–27.
MAHANEY,W.,M.W.MILNER,S.AUFREITER, R.G.V.
HANCOCK,R.W.WRANGHAM &S.CAMPBELL.
2005. Soils consumed by chimpanzees of the
Kanyawara community in the Kibale Forest,
Uganda. International Journal of Primatology 26:
1375–98.
MASI,S.,E.GUSTAFSSON,M.SAINT JALME,V.NARAT,
A. TODD,M.-C.BOMSEL &S.KRIEF. 2012.
Unusual feeding behavior in wild great apes, a
window to understand origins of self-medication in
humans: role of sociality and physiology on learning
process. Physiology and Behaviour 105: 337–49.
MCKAY, D.L. & J.B. BLUMBERG. 2006. A review of the
bioactivity and potential health benefits of
chamomile tea (Matricaria recutita L.). Phytotherapy
Research 20: 519–30.
MILLER, G. 2011. Sweet here, salty there: evidence for a
taste map in the mammalian brain. Science
333: 1213.
NELSON, E. 1899. The Eskimo about Bering Strait.
Washington, D.C.: Smithsonian Institution.
REMIS, M.J., E.S. DIERENFELD, C.B. MOWRY &
R.W. CARROLL. 2001. Nutritional aspects of
western lowland gorilla (Gorilla gorilla gorilla)diet
during seasons of fruit scarcity at Bai Hokou,
Central African Republic. International Journal of
Primatology 22: 807–36.
RICHARDS,M.P.&E.TRINKAUS. 2009. Isotopic
evidence for the diets of European Neanderthals
and early modern humans. Proceedings of the
National Academy of Sciences of the USA 106:
16034–39.
RODRIGUEZ,E.&R.W.WRANGHAM. 1993.
Zoopharmacognosy: the use of medicinal plants by
animals, in K.R. Downum, J.T. Romeo & H.
Stafford (ed.) Phytochemical potential of tropical
plants (Recent Advances in Phytochemistry 27):
89–105. New York: Plenum.
ROEBROEKS,W.&P.VILLA. 2011. On the earliest
evidence for habitual use of fire in Europe.
Proceedings of the National Academy of Sciences of the
USA 108: 5209–14.
C
Antiquity Publications Ltd.
877
Neanderthal self-medication in context
SINGER, M.S., K.C. MACE & E.A. BERNAYS. 2009.
Self-medication as adaptive plasticity: increased
ingestion of plant toxins by parasitized caterpillars.
PLoS ONE 4(3): e4796.
doi:10.1371/journal.pone.0004796
SNODGRASS, J.J., W.R. LEONARD &M.L.ROBERSTON.
2009. The energetics of encephalization in early
hominids, in J.-J. Hublin & M.P. Richards (ed.)
The evolution of hominin diets: integrating approaches
to the study of Palaeolithic subsistence: 15–29.
Dordrecht: Springer.
VAN ANDEL, T.H. 2003. Glacial environments I: the
Weichselian climate in Europe between the end of
the OIS-5 interglacial and the Last Glacial
Maximum, in T.H. Van Andel & W. Davies (ed.)
Neanderthals and modern humans in the European
landscape during the last glaciation: archaeological
results of the Stage 3 Project (McDonald Institute
Monographs): 10–20. Cambridge: McDonald
Institute of Archaeology.
VAN PEER,P.,R.FULLAGAR,S.STOKE S,R.M.BAILEY,
J. MOEYERSONS,F.STEENHOUDT,A.GEERTS,
T. VANDERBEKEN,M.DEDAPPER &F.GEUS. 2003.
The Early to Middle Stone Age transition and the
emergence of modern human behaviour at site
8-B-11, Sai Island, Sudan. Journal of Human
Evolution 45: 187–93.
WOOD, R.E., T.F.G. HIGHAM,T.DE TORRES,N.
TISNER´
AT-LABORDE,H.VALLARDAS,J.E.ORT IZ,C.
LALUEZA-FOX,S.S
´
ANCHEZ-MORALES,J.C.
CA˜
NAVERAS,A.ROSAS,D.SANTAMAR´
IA &M.DE LA
RASILLA. 2013. A new date for the Neanderthals
from El Sidr´
on Cave (Asturias, northern Spain).
Archaeometry 55: 148–58.
doi: 10.1111/j.1475-4754.2012.00671.x
WRANGHAM, R.W. 1995. Relationship of chimpanzee
leaf-swallowing to a tapeworm infection. American
Journal of Primatology 37: 297–303.
doi: 10.1002/ajp.1350370404
Received: 4 October 2012; Accepted: 10 January 2013; Revised: 28 January 2013
C
Antiquity Publications Ltd.
878