DarwinianGastronomy:

Why We Use Spices

Spices taste good because they are good for us

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PaulW. ShermanandJenniferBilling

pices are plant products used in fruits of herbaceous plants (Figure

flavoring foods and beverages. Humans have borrowed 1). Cookbooks generally distinguish
For thousands of years, aro- between seasonings (spices used in
matic plant materials have been used food preparation) and condiments
in food preparation and preserva- plants' chemical "recipes" (spices added after food is served),
tion, as well as for embalming, in for evolutionary survival but not between herbs and spices.
areas where the plants are native, However, herbs, which are defined
such as Hindustan and the Spice Is- for use in cuisine to botanically (as plants that do not
lands (Govindarajan 1985, Dillon develop woody, persistent tissue),
and Board 1994). During and after combat foodborne usually are called for in their fresh
the Middle Ages, seafarers such as state, whereas spices generally are
Marco Polo, Ferdinand Magellan, microorganisms and to dried (Figure 2). Salt is sometimes
and Christopher Columbus under- reduce food poisoning thought of as a spice, but it is a
took hazardous voyages to establish mineral.
routes to trading ports in primary Each spice has a unique aroma
spice-growing regions (Parry 1953). restaurants, or preparing exotic reci- and flavor, which derive from com-
The spice trade was so crucial to pes at home. Japanese dishes are pounds known as phytochemicals or
national economies that rulers re- often "delicate," Indonesian and "secondary compounds" (because
peatedly mounted costly expeditions Szechwan dishes "hot," and middle they are secondary to the plant's
to raid spice-growing countries, and European and Scandinavian dishes basic metabolism). These chemicals
struggles for the control of these "bland." Usually these differences evolved in plants to protect them
countries precipitated several wars. are merely chalked up to cultural against herbivorous insects and ver-
When Alarich, a leader of the Goths, idiosyncrasies. Several years ago, we tebrates, fungi, pathogens, and para-
laid siege to Rome in AD 408, he became curious about this interpre- sites (Fraenkel 1959, Walker 1994).
demanded as ransom various pre- tation. We wondered if there are any Most spices contain dozens of sec-
cious metals and 3000 pounds of predictable patterns of spice use and, ondary compounds. These are plants'
pepper (Scheiper 1993). if so, what factors might underlie recipes for survival-legacies of their
Today, spice use is ubiquitous, them. In this article, we summarize coevolutionary races against biotic
but spices are far more important in the results of our inquiries. We found enemies.
some cuisines than others. Most that spice use is decidedly nonrandom
people have experienced this vari- and that spices have several benefi- Patterns of spice use
ability firsthand, when traveling in cial effects, the most important of
which may be reducing foodborne Conventional wisdom tells us that
foreign lands, dining at international cuisines of tropical countries are
illnesses and food poisoning.
spicier than those of northern coun-
PaulW. Shermanis a professorat Cornell tries, but patterns of spice use around
University.He studiesthe behavioralecol-
Whatis a spice? the world have not been quantified.
ogy of various birds and mammals and "Spice" is a culinary term, not a To do so, we located "traditional"
teaches animal behavior and Darwinian
medicine.JenniferBilling was an under- botanical category-it does not refer cookbooks, which were written pri-
graduateHonors studentat Cornellwhen
to a specific kind of plant or plant marily to archive the author's native
shebeganstudyingspices.Shenow teaches part (Farrell 1990). Indeed, spices cuisine. We analyzed recipes in 93
biology and chemistry at The Dalton come from various woody shrubs traditional cookbooks from 36 coun-
Schoolin New York City. 0 1999 Ameri- and vines, trees, aromatic lichens, ties (at least two books from each
can Instituteof BiologicalSciences. and the roots, flowers, seeds, and country) and quantified the use of 43

June 19999453

University of California Press

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Table 1. Mean annual temperature,number of meat-based recipes analyzed (in 93 cookbooks), mean number of spices per
recipe, and the four most frequentlyused spices (i.e., used in the highest proportion of recipes) for each of the 36 countries
included in this study.
Meanannual
Countrya temperature ('C) Recipes analyzed Spices per recipe Frequently used spicesb
Thailand 27.6 118 4.6 Garlic, onion, chilisc, pepperd
Philippines 27.0 118 3.0 Pepper, onion, garlic, lemon/lime
India 26.9 91 9.3 Ginger, onion, chilis, coriander
Malaysia 26.9 60 5.4 Onion, garlic, chilis, ginger
Indonesia 26.8 120 6.9 Garlic, onion, chilis, coriander
Nigeria 26.5 82 2.6 Chilis, onion, pepper, nutmeg
Ghana 25.9 95 2.2 Onion, pepper, chilis, ginger
Vietnam 24.6 84 4.5 Pepper, garlic, onion, chilis
Brazil 23.9 132 4.2 Onion, pepper, parsley, garlic
Mexico 23.1 123 4.4 Onion, garlic, chilis, pepper
Kenya 22.1 73 5.4 Garlic, onion, pepper, chilis

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Ethiopia 21.1 56 7.5 Onion, garlic, chilis, ginger
Lebanon 20.6 98 4.7 Pepper, onion, cinnamon, garlic
Israel 19.1 145 3.9 Pepper, onion, garlic, lemon/lime
Australia 18.6 64 3.4 Pepper, onion, parsley, lemon/lime
Morocco 18.3 104 5.8 Onion, pepper, parsley, saffron
South Africa 17.2 108 2.6 Pepper, onion, lemon/lime, chilis
Greece 16.7 118 4.4 Pepper, onion, garlic, lemon/lime
Iran 16.7 85 5.0 Onion, pepper, lemon/lime, turmeric
Portugal 15.0 84 4.5 Pepper, garlic, parsley, onion
Japan 14.3 103 2.1 Onion, lemon/lime, ginger, chilis
Italy 14.0 86 3.4 Pepper, garlic, parsley, lemon/lime
Korea 12.1 81 3.5 Garlic, onion, pepper, sesame
France 12.1 216 3.8 Pepper, onion, garlic, parsley
Hungary 10.3 80 3.0 Onion, pepper, paprika, parsley
Ireland 9.6 90 3.2 Pepper, onion, garlic, parsley
England 8.8 223 2.1 Pepper, onion, lemon/lime, parsley
Germany 8.8 169 3.2 Onion, pepper, lemon/lime, parsley
Austria 8.8 188 2.7 Onion, pepper, parsley, lemon/lime
Denmark 8.3 87 1.9 Pepper, onion, bay leaf, parsley
Poland 7.8 141 0.3 Onion, pepper, bay leaf, parsley
Sweden 5.4 134 2.5 Pepper, onion, allspice, parsley
Finland 3.0 62 2.1 Pepper, onion, mustard, lemon/lime
Norway 2.8 77 1.6 Pepper, parsley, onion, lemon/lime
United States
Northern 8.6 284 5.4 Pepper, onion, garlic, parsley
Southern 17.8 248 5.0 Onion, chilis, pepper, parsley
China
Northeast 13.4 187 2.3 Onion, ginger, pepper, garlic
Southwest 19.4 243 3.2 Ginger, onion, pepper, garlic
aCountries are listed in order of mean annual temperature, except for the United States and China. We divided those two countries into two
regions that we analyzed separately.
bIn order of use.
cChilis are capsaicin-containing peppers.
dPepper refers to black and white pepper.

spices in these countries (Table 1). tionship between spoilage and spice quantities called for, they always
In gathering our data, we did not use should be more apparent in meat- contribute their phytochemicals to
distinguish between seasonings and based than vegetable-based recipes. the cuisine. The second problem was
condiments or between herbs and In summarizing the data, we en- how to treat the comparative infor-
spices. We focused on meat-based countered two problems. The first mation statistically, because not all
recipes (those in which at least one- was whether or not to treat onions countries are equally "independent"
third of the volume or weight con- (Allium cepa: chives, leeks, and shal- (e.g., due to shared ancestry or re-
sisted of meat) rather than vegetable- lots) and chilis (Capsicum frutescens: cent immigration). However, because
based recipes for two reasons. First, capsaicin-containing peppers) as it is unclear how to assess indepen-
traditional cookbooks have many more spices. Although these plants are of- dence of a specific cultural practice,
meat-based dishes than vegetarian ten used solely as spices, they are such as spice use, and because our
dishes, enabling us to obtain adequate also served as main dishes. Follow- sample was so broad (representing
sample sizes (Table 1). Second, ing the lead of previous authors (e.g., every continent and 16 of the world's
unrefrigerated meats spoil faster than Farrell 1990, Tainter and Grenis 19 major linguistic groups [Ruhlen
vegetables and are more often asso- 1993, Hirasa and Takemasa 1998), 1987]), we treated all countries as if
ciated with foodborne disease out- we decided to include both plants as they were independent and used non-
breaks (Sockett 1995). Thus, any rela- spices because, regardless of the parametric analyses.

454 BioScience Vol. 49 No. 6

 We tabulated the in- Figure 1. Spices are plant
gredients in 4578 meat- parts. They come from
based recipes and discov- woody shrubs and vines,
ered that most of them ~ ~ trees,aromaticlichens,and
the roots, flowers, seeds,
(93%) call for at least .
one spice. On average, .. ..
Jr and fruits of herbaceous
.'" d plants. Photo: Thomas
recipes called for 3.9 ? "•i- "z"
";: Neuhaus, Neuhaus Fea-
1.7 (SD) spices, although .0
. .. tures.
some lacked spices en-
1 , ---
tirely and others had up a
to 12 spices. In 10 coun- Prediction 1. Spices
tries-Ethiopia, Kenya, shouldexhibitantibac-
Greece, India, Indonesia, terialandantifungal
ac-
Iran, Malaysia, Mo- tivity. Microbiologists
rocco, Nigeria, and andfood-product devel-

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Thailand-every meat- opers have conducted
based recipe we exam- laboratoryexperiments
ined called for at least thatinvolvechallenging
one spice, whereas in numerous foodborne
Scandinavian countries one-third of both "levels of analysis" (Sherman bacteria, fungi, and yeasts with
the recipes did not call for any spices. 1988). phytochemicals extracted from spice
The frequency of use of individual A clue to the ultimate reason for plants. Multiple techniques have been
spices also varied widely (Figure 3). spice use may lie in the protective used to investigate inhibition, and
Black pepper and onion were called effects of phytochemicals against the primary data vary considerably
for most frequently, in 63% and 65% plants' biotic enemies. After all, meat in quality and quantity for different
of all meat-based recipes, respec- and other food items are also attacked spices. Nevertheless, it is now clear
tively. Other commonly used spices by bacteria and fungi, indeed by some that many spices have potent antimi-
included garlic (35% of recipes), of the same species that afflict plants. crobial properties (e.g., Hargreaves
chilis (24%), lemon and lime juice Throughout recorded history, food- et al. 1975, Shelef 1984, Deans and
(23%), parsley (22%), ginger (16%), borne bacteria (especially species of Ritchie 1987, Zaika 1988, Beuchat
and bay leaf (13%). However, the Clostridium, Escherichia, Listeria, 1994, Nakatani 1994, Hirasa and
majority of spices were used infre- Salmonella, Shigella, and Vibrio) or Takemasa 1998).
quently. Of the 43 spices we ana- their toxins have been serious health We were particularly interested in
lyzed, 35 (81%) were used in less concerns, and they still are (Hui et al. the ability of spices to inhibit bacte-
than 10% of the recipes, and 29 1994, WHO 1996). If spices were to ria because bacteria are more com-
(67%) were used in less than 5% of kill such microorganisms or inhibit monly incriminated in foodborne
the recipes. their growth before they could pro- disease outbreaks than yeasts or fungi
duce toxins, use of spices might re- (Varnam and Evans 1991, Todd
Antimicrobialproperties duce foodborne illnesses and food 1994). All 30 spices for which we
of spices poisoning (Billing and Sherman located laboratory test results were
1998). If this antimicrobial hypoth- found at some concentration to kill
Why are spices used? The obvious esis were true, several predictions or inhibit at least 25% of the bacterial
answer is that they enhance food should be fulfilled. species on which they had been tested,
flavor, color, and palat- and 15 of these spices
ability. Of course this is inhibitedat least 75%
true as far as it goes. of bacterial
species(Fig-
However, such a proxi- ure 4). Garlic,onion,
mate (immediate cause) allspice, and oregano
explanation does not ad- were found to be the
dress the ultimate (evo- most potent spices:
lutionary) questions of Theyinhibitedorkilled
why cuisines that con-
-FIE!
every bacteriumthey
tain pungent plant prod- were tested on. Most
ucts appeal to people and of the tested microor-
why some phytochemi-
cals are tastier than oth- Figure 2. The spice trade
flourishestoday, as it has
ers. Answers to proximate -..
for thousands of years.
... ... ....
and ultimate questions
Here,groundspicesaredis-
are complementary, not ...,....
playedat CarmelSouk, an
mutually exclusive, and open-air market in Tel
full understanding re- Aviv. Photo: Eliot M.
quires explanations at Herman.

June 1999 455

U) 1.0o-
ganisms are widely distributed geo-
.- 0.9- graphically, so they have the poten-
tial to contaminate foods everywhere.
S0.8-
0.7- Prediction 2. Use of spices should be
0.6- greatest in hot climates, where
unrefrigerated foods spoil especially
0 0.5- quickly. Uncooked meats and meat
0.4 dishes that are prepared in advance
0 and stored at room temperatures for
L.? 0.3- more than a few hours typically build
o 0.2 up massive bacterial populations,
0o.1 especially in tropical climates (Hobbs
and Roberts 1993). Therefore, we
L mom• m used each country's average annual
o• •u

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...- • - •-m. . .
. uSpic
temperature as a relative indicator
0.0 0.-' 00 E E of its rate of meat spoilage. Our test
"H.U _ •ooa
.,, , E.E
0 C
gE00
0 ccE
. Coc assumes that traditional meat-based
og" O.0EL.- omce
0 o "- recipes were developed before wide-
)c
spread refrigeration. We cannot di-
rectly evaluate this assumption be-
cause the cookbooks we examined
Spice rarely discussed the history of indi-
vidual dishes. However, the assump-
tion seems reasonable because any
Figure 3. Proportions of 4578 meat-basedrecipes that called for each of 43 spices.
The recipes we surveyed came from 93 traditional cookbooks from 36 countries recipe that has been around for more
worldwide. Eachcountrywas representedby at least two cookbooks. Modifed from than five generations (approximately
Billing and Sherman(1998). 100 years) would pre-date electrical
refrigeration. Most of the recipes we
examined probably were at least that
old.
"D We used climate atlases (e.g., Bair
S1.0- 1992) to tabulate information on
0.9- mean temperatures in all 36 coun-
75% bacterial tries (Table 1). Temperatures ranged
C 0.8- inhibition from 2.8 'C (Norway) to 27.6 'C
0.7- (Thailand). Consistent with the pre-
diction, we found that as average
temperatures increased among coun-
0.5-
tries, there were significant increases
0.4- in the fraction of recipes that called
for at least one spice, the mean num-
0.3- bers of spices per recipe, and the
0
0.2- numbers of different spices used (Fig-
ure 5). For example, India's cuisine
0 0.1 -
included 25 different spices, of which
U" 0.0 1 V- I I an average of 9.3 were called for per
0 0C IC L
0 Co 3: C Ec cc recipe, whereas Norwegian cuisine
>o 'ic"cc Eo
' included only 10 different spices and
EE-
-grCLC IM Cc
0 .
E. called for an average of 1.6 per recipe.
. In Hungary, which has a temperate
climate, the cuisine included 21
Spice? spices, of which an average of 3.0
were called for per recipe.
Figure 4. Antimicrobial properties (i.e., killing or growth inhibition) of 30 spices. The relative use of many indi-
The spices are arrayed from greatest to least inhibition. Each bar indicates the vidual spices also varied with cli-
fraction of all food-spoilage bacterial species on which the spice or its phytochemicals
have been tested (at any concentration) in the laboratory that were killed or whose
mate. Among countries, as average
growth was inhibited. (The number of bacterial species on which each spice was temperature increased, so did the
tested ranged from 4 to 31.) All 30 spices inhibited or killed some tested bacterial frequency of use of chilis, garlic, and
species; 15 spices inhibited or killed at least 75% of the species, and 4 spices (garlic, onion (Figures 6 and 7), as well as
onion, allspice, and oregano) inhibited or killed all of the tested species. Modifed that of anise, cinnamon, coriander,
from Billing and Sherman (1998). cumin, ginger, lemongrass, turmeric,

456 BioScience Vol. 49 No. 6

basil, bay leaf, cardamom, celery, m Figure 5. Relationships between mean
1.0 annualtemperatureand spice use for the
cloves, green peppers, mint, nutmeg, -@?
saffron, and oregano (see also Hirasa -. (a) .0 .0 - 34 nonregionalcountrieswe analyzed(i.e.,
0.9- * * excluding the United States and China).
and Takemasa 1998). The first 10 of "0.9
these spices are "highly inhibitory" (a) Relationship between mean annual
temperatureand the proportionof meat-
(at least 75% of tested bacterial spe- 0 0.8 O#0 0 basedrecipescallingfor at least one spice
cies inhibited; see Figure 4), and the (r = 0.740, df = 32, P < 0.001). (b) Rela-
*
positive relationships were statisti- .00.7
t 0 tionship between mean annual tempera-
cally significant. There were nega- 0 tureandthe meannumbersof spicescalled
tive relationships between tempera- 0.6 - for per recipe (r = 0.572, df = 32, P =
ture and frequencies of use for 10 0.002). (c) Relationship between mean
other spices, but they were signifi- -0.5 0.5 ,.. . . .
annualtemperatureand the total number
cant only for dill and parsley, neither of spices used in the country (r = 0.216, df
10- = 32, P = 0.286). Modifed from Billing
of which has potent antimicrobial
. (b) and Sherman (1998).
activity. 8
"

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a) 0
Prediction 3. A greater proportion of 0" - 0 0.* ber of spices per recipe was greater in
bacteria should be inhibited by reci- ,- 6 southern China than in northern
pes from hot climates than from cool . 4- : *
? ? China, but no such difference was
climates. In support of this predic- = o. evident in the United States (Table
tion, as average annual temperatures o 0 e 1). In both countries, the spices called
increased among countries, the mean *.2 # * for in an average southern recipe had
fraction of recipes that called for
?
significantly greater antibacterial po-
each one of the highly inhibitory 0 .. 0.I..n. , . .I '' 1 ' ' tential than those in northern reci-
spices used in those countries in- 30- pes, mirroring the among-country
creased significantly (Figure 8a). *" (c) * * pattern (Billing and Sherman 1998).
However, this correlation did not (C) Because altitude-specific cookbooks
hold for less inhibitory spices (Fig- 3 are rare, we were unable to evaluate
00 ??
ure 8b). There was also a positive 00 how altitude affects spice use.
a) 0
relationship between the fraction of o .m
bacterial species inhibited by each 0•o Prediction 5. Quantities of spices
spice and the fraction of countries called for in recipes should be suffi-
that used that spice, indicating wide- cient to produce antimicrobial ef-
spread use of the spices that are most 0* .0 U fects, and cooking should not de-
effective against bacteria. stroy the potency of phytochemicals.
To further test this corollary, we 0 .... I.... I.... I.... I.... I.... I
The primary literature in food mi-
0 5 10 15 20 25 30
tried to determine if spices used in crobiology that we surveyed usually
each country are particularly effec- Mean Annual reported the minimum concentra-
tive against local bacteria. Unfortu- Temperature (oC) tions of purified phytochemicals that
nately, however, no comprehensive were necessary to inhibit growth of
lists of indigenous bacteria are avail- foodborne bacteria in vitro. Typi-
able for any country in our sample. inhibited by the spices in each cally, these were solutions contain-
To estimate inhibition, therefore, we country's recipes increased signifi- ing 0.5-4.0% purified spice chemi-
chose 30 meat-based recipes at ran- cantly. Therefore, the cuisine of hot- cals (i.e., 30-2000 gg/ml), which is
dom from the cookbooks for each ter countries potentially has greater within the range of spice concentra-
country and tallied how many of 30 antibacterial activity. tions used in cooking (Shelef 1984,
"target" bacterial species would be Giese 1994, Hirasa and Takemasa
inhibited or killed by at least one Prediction 4. Within a country, cui- 1998). However, there are as yet no
spice in each recipe. The target bac- sine from high latitudes and eleva- analyses of how different amounts
teria were those that have been chal- tions (i.e., cooler climates) should and types of spices affect microor-
lenged experimentally with the great- contain fewer and less potent spices ganisms in cuisine. Evaluating the
est number of spices, including such than cuisine from lower latitudes and antimicrobial efficacy of various
widespread species as Aeromonas hy- elevations. We located regional cook- spices in vivo (i.e., restaurants and
drophila, Bacillus cereus, Bacillus books for only two countries, China homes) would be a fascinating (and
subtilus, Clostridium botulinum, Lis- and the United States. Consistent potentially lucrative) project.
teria monocytogenes, Escherichia with the prediction, in both coun- Regarding the effects of cooking,
coli, Salmonella pullorum, Staphy- tries the total number of spices used, most phytochemicals are thermo-
lococcus aureus, and Streptococcus the fraction of recipes that called for stable, although a few are destroyed
faecalis. Results of this analysis (Fig- at least one spice, and the frequency by heat (Moyler 1994). Some spices
ure 9) showed that as annual tem- of use of highly inhibitory spices (e.g., garlic, pepper, rosemary, and
peratures increased, the estimated were greater in southern regions than onion) are typically added at the
fraction of food spoilage bacteria in northern regions. The mean num- beginning of cooking, whereas oth-

June 1999 457

Figure6. Garlic(Liliaceae: spices),picklingspice(15
Allium sativum; top), on- spices),andchilipowder
ion (Alliumcepa;top), and
chilis (Solanaceae:Capsi- (10 spices),are broad-
cum frutescens; bottom) spectrumantimicrobial
grow in all countries we melanges.
sampled and have power-
ful antimicrobial effects. Otherusesof spices
Photos:ThomasNeuhaus,
Neuhaus Features. Inadditionto theiruses
in cooking, individual
ers (e.g., parsley and spices and blends are
cilantro[i.e., coriander employed as coloring
leaf])areaddednearthe agents,antivirals(includ-
end(Figure10).Accord- ing suppressingHIV),
ingtocookbookauthors, brain stimulants, and

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the "delicate" flavorsof aphrodisiacs (Hirasaand
the latterwould be de- Takemasa 1998).Among
stroyedby heat. If, as traditional societies,
seems likely, thermo- many spice plants also
stablespicesaretheones have ethnopharmaco-
addedearlyandthermo- logical uses, often as
labile spicesare added topicaloringestedanti-
later (or are used pri- bacterials and vermi-
marilyas condiments), cides (Chevallier1996,
differencesin timingof Cichewiczand Thorpe
use may function to 1996). A few spices,
maintainbeneficialanti- particularlygarlic,gin-
microbial properties ger, cinnamon, and
(andcorresponding fla- chilis, have for centu-
vors)untilfood is served. ries beenusedto coun-
teracta broadspectrum
of ailments, including
Spicesynergism dysentery, kidneystones,
Pepperandlemon(and arthritis,andhighblood
lime) juice are among pressure(Johns 1990,
the most frequently Duke 1994).
used spices (Figure3), However,the use of
butthey are unusualin that the fre- several useful properties. For example, spices in food preparationdiffers
quency with which they are used the compound piperine inhibits the frommedicinalusein threeways.In
does not change much across the ubiquitous, deadly bacterium Clos- cooking,spicesareusedwithoutre-
temperaturegradient (Figure 11). tridium botulinum (Nakatani 1994). gardto diners'healthstatus,theyare
Moreover,they are amongthe least Black pepper is also a "bioavailability usedin tiny quantities,and theyare
effectivebacteriocides(Figure4). Do enhancer," meaning that it acts syn- routinelyaddedto specificrecipes.
thesepatternsweakentheantimicro- ergistically to increase the rate at This patternsuggeststhat the "tar-
bialhypothesis,ordo thesetwospices which cells, including microorgan- gets"of spicechemicalsareon or in
functionina differentwaythan"typi- isms, absorb phytotoxins (Johri and the food before it is ingested. By
cal"spices? Zutshi 1992). contrast,in medicinalusage,spices
We believethatthe secondexpla- Many other spices exhibit greater are taken in responseto particular
nationis correct,andwe suggestthat antibacterial potency when they are maladies, in large quantities,and
pepperand citric acid play special mixed than when used alone (Ziaud- not with any particulardish-more
roles-that is, as synergists.Citric din et al. 1996). Some are combined likeswallowinga pillthanpreparing
acidpotentiatesthe antibacterialef- so frequently that the blends have a meal.
fectsof otherspicesbecauselow pH acquired special names. An intrigu- Aninterestingquestionis whether
disrupts bacterialcell membranes ing example is the French "quatre otheranimalsalso"spice"foods.Pres-
(Booth and Kroll 1989). Foods to epices" (pepper, cloves, ginger, and ently,theanswerappearsto be "no."
whichlemonor limejuiceareadded nutmeg), which is often used to make However,"vegetation" does form a
requirelessheatingto causethesame sausages. Sausages (botulus in Latin) smallbut significantfractionof the
levelsof bacterialmortalitythattake are a rich medium for bacterial dietof mostwildcarnivores,includ-
placein foods cookedat higherpH growth and have frequently been im- ingfoxes,coyotes,andcougars(e.g.,
and temperaturefor a longertime. plicated as the source of botulinum Parker1995). Undoubtedly,much
BlackpeppercomesfromPipernigrum, toxin. Other blends, such as curry of thisplantmaterialservesas nutri-
an exclusivelytropicalplantthathas powder (which contains 22 different tion,forexample,whenmeatis scarce.

458 BioScience Vol. 49 No. 6

Nevertheless, frequentingestion of veg- Figure7. Relationships 1.0-
etation is potentially interesting in the between each nonre- S (a) Chilis
context of the antimicrobial hypoth- gional country'smean " 0.8-
esis because most wild carnivores annual temperature
and the proportion of III
scavenge carrion, so they are fre- its meat-basedrecipes 0.6 I
quently exposed to food-spoilage thatcallforone of three LL
bacteria and fungi. Moreover, some 0.4?
highlyinhibitoryspices _m 0.62-.
animals that store food add plants (at least 75% bacterial
with antibacterial and antifungal inhibition; see Figure - 0.2 * r
.
properties to their caches (e.g., brown 3). (a) Chilis (capsai- -- 00
0.0* *.p ,eo..@J:???????????????
bears sometimes cover carcasses with cin-containingpeppers; . o.
Spaghnum moss [Elgmork 1982], and r = 0.757, df = 32, P <
1.0-
some stingless bees build honey pots 0.001). (b) Garlic (r = 0 (b) Garlic
by mixing plant resins with wax 0.635, df = 32, P < *
[Roubik 1983]). These possible pro- 0.001). (c) Onion (r = S0.8
df - 32, P < 80

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phylactic uses should not be con- 0.001). Modifed from >0 0.6.
0.652, * 0
fused with consumption of aromatic
Billing and Sherman
plants by wild primates as a poten- (1998). C 0.4
tial means of "self-medication" (e.g., 0
Huffman and Wrangham 1994). o 0.2 *
foods, especially "
Costs of spices ) 0.0
meats. These differ- 00.0= .? . . . .. 0 ..

ences in spice use 1.0-

In light of the beneficial effects of may have a similar S(c) Onion
spices, why aren't spices used equally adaptive basis. For
often everywhere? The answer prob- Profet 0.8 .
example,
ably lies in the costs of spice use, O
including financial costs to procure
(1992) suggested
that morning sick-
o 0.6* 00*0000
0o 0o0
parts of plants that do not grow ness may function to
0.4
00
locally (e.g., consider the price of reduce maternal in-
Spanish saffron), illnesses caused by take of foods con- S0.42 00
L.
ingesting spices that are themselves taining teratogens
contaminated (e.g., with bacteria, during the early 0 S .0
fungi, or animal feces), and other phase of embryo- . 5 15 20 25 30
hazards of ingesting too many plant genesis, when deli-
secondary compounds and essential cate fetal tissues are
1o0
Mean Annual Temperature (oC)
oils. Indeed, Ames et al. (1990) and most susceptible to chemical disrup- proposed to explain spice use; how-
Beier and Nigg (1994) reviewed evi- tion. Indeed, women who experi- ever, careful consideration of the al-
dence that phytochemicals in many ence morning sickness are less likely ternatives reveals that all have signifi-
common spices have mutagenic, ter- to miscarry than women who do not cant flaws. For example, one proximate
atogenic, carcinogenic, or allergenic (Weigel and Weigel 1989). Young hypothesis is that spices disguise the
properties. As one example, in small children, who are growing rapidly, smell and taste of spoiled foods (Gov-
quantities chilis have antimicrobial may also be particularly sensitive to indarajan 1985). Our finding that
and therapeutic effects, but inges- environmental mutagens. Once preg- traditional meat-based recipes from
tion of large amounts of capsaicin nancy has progressed into the sec- hotter countries more frequently
has been associated with necrosis, ond trimester and once children reach called for spices, and more pungent
ulceration, and carcinogenesis (Surh puberty, the dangers of food poison- spices, is consistent with this idea
and Lee 1996). The implication is ing and foodborne illnesses may again because there would more often be
that too much of a good thing can be outweigh the mutagenic risks associ- foul smells and bad tastes to "cover
bad. In hot climates, benefits of ated with phytochemicals (Flaxman up" due to rapid spoilage. However,
avoiding foodborne illnesses and and Sherman in press). Interestingly, the problem with this hypothesis as
food poisoning apparently outweigh maternal ingestion of spices late in an ultimate (evolutionary) explana-
the various costs of spices. But in pregnancy or during lactation can tion is that it ignores the potentially
cool climates, where unrefrigerated slightly bias offspring toward ac- serious negative consequences of in-
foods decay more slowly, benefits of cepting spices (e.g., Altbacker et al. gesting foods laced with bacteria or
further retarding spoilage may not 1995). their toxins. Even poorly nourished
be worth the costs and risks. individuals would often be better off
Even in countries where spices are Alternative hypotheses to if they recognized and passed up
heavily used, pre-adolescent children foods containing potentially deadly
(Rozin 1980) and women in their
explain spice use
spoilage microorganisms.
first trimester of pregnancy (Profet The antimicrobial hypothesis is not A second proximate alternative to
1992) typically avoid highly spiced the only explanation that has been explain spice use is that spicy foods

June 1999 459

Figure8. Relationships a have beneficial effects other than in-
between each nonre- hibiting food spoilage microorgan-
gional country's mean isms. For example, certain phyto-
annualtemperatureand 0.6- Spices that Inhibit:
the proportionof meat- (a) > 75% of bacteria chemicals, especially those found in
based recipes that call 0a.
garlic and onions, can aid digestion,
CL ? modulate energy metabolism, and
for spicesthat inhibitat
least 75% of bacteria $ 0.4 * even help postpone some degenera-
(a; r = 0.668, df = 31, P tive diseases, such as diabetes and
< 0.001) or less than cancer (Johns and Chapman 1995).
75% of bacteria(b; r = o0
CL Some other phytochemicals, particu-
o 000.0 * *
0.248,df=31,P>0.10).
00.2
?o
oo larly those in cloves, rosemary, sage,
Modifed from Billing :2
a. S 0 pepper, and mace, are powerful an-
and Sherman(1998). 0 tioxidants (Lin 1994, Hirasa and
0.
Takemasa 1998). By retarding the
are preferred in hot oxidation of oil or fat, phyto-
0.0 . . . . , . . , .. . . , . . , . . . , . . ,

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climates because they chemicals help preserve foods and
increase perspiration also reduce the production of free radi-
and help cool the b 0.6 Spices that Inhibit: cals, which have been linked to cancer
body evaporatively. (b) < 75% of bacteria and aging. These effects are undeni-
However, although 0.5 ably important, but they probably do
chilis and horserad- as. S
? not represent the primary reason for
ish can cause sweat- 1 spice use because not all spices have
ing in some people, 0.4- ? ? ? ? these beneficial properties. More-
0
most spices do not 0.3- * over, the need for micronutrients or
S0.30 ?
have this effect (Rozin antioxidants does not predict or ex-
* a
and Schiller 1980). plain the use of spices in recipes or
o 0.2
C. the multiple positive correlations be-
Thus, evaporative 0
cooling cannot be a L._ tween temperature and spice use
. 0.1 shown in Figures 5, 7, 8, and 9).
general explanation
for the increased spice Finally, it is also possible that
use in hot climates. 0.0
S0. 5 10 15 20 25 30 spice use may not confer any ben-
Moreover, physiolo- efits. Under this hypothesis, patterns
Mean Annual Temperature (oC)
gical mechanisms of of spice use arise because people just
temperature regula- take advantage of whatever aromatic
tion obviously operate to keep us Figure 7). Also, this hypothesis is plants are available to improve the
cool without the necessity of find- difficult to reconcile with the fact taste of their food. Perhaps the
ing, eating, and dealing with the that the rarest spices tend to be used phytochemicals in spices happen to
potentially negative side effects of most commonly in the tropics, be- resemble those found in sought-after
phytochemicals. cause it is in these locations where foods, such as fat and sugar (Rozin
One alternative ultimate hypoth- the plants are endemic and, presum- and Vollmecke 1986), and as a result
esis for spice use is that wherever ably, therefore, least expensive. spices taste good. If this idea were
spices are difficult to obtain and are A second alternative ultimate correct, spice chemicals should be
therefore expensive, individuals sig- hypothesis is that spices supply highly palatable, and spice-use pat-
nal their wealth and social status chemicals that, in small quantities, terns should correspond to local
(e.g., to rivals or potential mates) by 1.0-
availability of spice plants.
using them lavishly. This hypothesis However, neither prediction is
would apply primarily to spice plants fully supported. Although some
with restricted ranges (e.g., pepper,
0.8
spices are initially appealing (e.g.,
allspice, fenugreek, nutmeg, and cin- ? cinnamon, basil, and thyme), pun-
namon). However, it does not pre- gent spices, such as garlic, ginger,
dict or explain the multiple positive anise, and chilis, are distasteful to
correlations between temperature o 4) 0
most people, especially children
and spice use we found for spices 0*00 (Rozin 1980). Indeed, the capsaicin
that are available ubiquitously (e.g., Ilo. o. 0.4- receptor is a heat-activated ion chan-
s- nel in the pain pathway (Caterina et
Figure9. Relationshipbetweenthe mean o0
..L C.
0. . l al. 1997). For most unpalatable sub-
annual temperatureof each nonregional
•" 0.2 0.2, stances, an initial negative response
country and the estimatedfraction of 30 0"0
is sufficient to maintain avoidance
ubiquitousfoodbornebacterialspeciesthat
would be inhibited by the spices in the throughout life. However, prefer-
recipesof that country(r = 0.516, df= 31, 0.0 ences for spices develop during indi-
P < 0.001). Modifed from Billing and 0 5 10 15 20 25 30 viduals' lifetimes, usually under fa-
Sherman(1998). Mean Annual Temperature (oC) milial guidance. Parents encourage

460 BioScience Vol. 49 No. 6

their children to use - Figure10. Somespices(e.g.,
spices,andmost children garlic, pepper, rosemary,
eventually come to like and shallots) are typically
added at the beginningof
(orat leastaccept)them,
cooking(top),whereasoth-
implying that spice use ers (e.g., parsleyandcilan-
is beneficial.
tro) areaddednearthe end
In addition, spices are orareusedasgarnishes(bot-
not necessarily more tom). Thesepatternsin the
availablein hot climates . timingof use may relateto
... . . ....
.........
than in cool ones. There differencesin the thermal
is no relationship be- stabilityof differentspices.
tween the number of Photos:ThomasNeuhaus,
countries in which each Neuhaus Features.
spice plant grows (i.e.,
its native and domesti- morehealthyoffspring,

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cated range) and either who would then learn
the numberof countries spice-use traditions
in which it is used or from their parents. It
their annual tempera- even seems possible
tures (Billing and Sher- that people who lived
man 1998). Because in areas where certain
spices have been culti- spices were tradition-
vated for thousands of ally usedmighthavede-
years in the Old World ..veloped physiologically
(ZoharyandHopf 1994) heightened abilities to
and hundredsof years in tastethose phytochemi-
the New World (Coe cals. The possibleexist-
1994), it seems likely ence of such inter-
that these patterns of group variations in
spice plant availability taste receptor sensitiv-
reflect those that oc- ity to spices are just
curredwhen traditional beginning to be ex-
recipeswere developing. plored (Drewnowski
Thus, correlations Sand Rock 1995).
between spice use and Eventually, how-
annualtemperaturemust ever, new foodborne
be due to people in hot 4bacteriaor fungiwould
countries using a larger immigrate, or indig-
proportion of whatever spices are Originsof spiceuse enous microorganismswould evolve
availablelocally (or importing more resistance to local spices. Individu-
spices). Indeed, for 22 of 30 spices How did spice use begin? We hy- als eating foods contaminated by
(73%), a largerpercentageof recipes pothesize that people may have be- these microbes would become ill.
calledfor the spice in countrieswhere gun cooking with spices whose fla- After humans, like many other crea-
the plant grows than where it does vors were initially appealing or that tures, eat somethingthat makesthem
not grow; for 14 of the spices, these made them feel good (due to diges- sick, they tend to avoid that taste
differenceswere significant(P < 0.05, tive or vermicidal effects, among (Milgram et al. 1977, Pelchat and
Mann-Whitneytests). Of course, the other things). As a result, spice-using Rozin 1982). The adaptive value of
spice trade (Figure 2) facilitates the familiesmay also have beenless likely such "taste-aversionlearning"is ob-
use of nonindigenous spices. For ex- to suffer from foodborne illnesses or vious (Rozin and Vollmecke 1986,
ample, onion and pepper are the two food poisoning than families that Letarteet al. 1997). Adding a differ-
most frequently used spices in the did not use spices, especially in hot ent spice to a food that caused such
world (Figure 3). Allium grows in all climates. Furthermore, spice-using an illness might change its flavor
36 countries we examined, but Piper families probably would have been enough to make it palatable again-
grows in only 9 countries. Pepper is able to store foods longer before because it tastes like a new food. At
the world's most frequently traded they spoiled, enabling them to toler- the same time, if the spice were to kill
spice (more than 90 million pounds ate prolonged periods of food scar- the microorganism(s)that caused the
per year are imported into the United city. Observation and imitation of illnessin the first place, then the food
States alone; Tainter and Grenis the food-preparationhabits of these would again be rendered safe for
1993). Thus, although local avail- healthierfamiliesby neighborscould consumption. As a result of this se-
ability certainly influences spice use, havespreadspice use rapidlythrough quence of events, food aversions
use is not dictated solely by local a society. Families that used appro- would more often be associated with
availability. priate spices would presumablyrear unspiced(andunsafe)foods, whereas

June 1999 461

food likings would be associated with and more frequently called for highly Conclusion
spicy dishes, especially in climates inhibitory spices (Billing and Sher-
where foods spoil rapidly. Over time, man 1998). As a result, an average Use of spices takes advantage of plant
the number of spices per recipe would Korean recipe most likely inhibits a defensive compounds. Not surpris-
proliferate due to iteration of this significantly greater fraction of bac- ingly, in view of their evolved func-
process-that is, sequential changes teria than an average Japanese recipe. tions, these phytochemicals have
in taste, associated with inhibiting dif- One possible explanation for the fact antioxidant, antimicrobial, and an-
ferent bacteria and fungi. that traditional Japanese recipes do tiviral properties. The use of spices
not call for more spices is that they essentially borrows plants' recipes
date from times when fresh seafood for survival and puts them to similar
Antimicrobial value use in cooking. Over time, recipes
of spices today was continuously available from lo-
cal waters. Today, more food is im- should "evolve" as new bacteria and
Despite the widespread availability ported, and it comes from fartheraway. fungi appear or indigenous species
of electrical refrigeration, antimicro- Traditional Japanese recipes may sim- develop resistance to phytochemicals,
bial properties of spices may still be ply not include enough spices (anti- requiring the addition of more spices

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useful. For example, there is an or- microbials) to cope with the patho- or new spices to combat them effec-
der-of-magnitude difference in the gens in the imported food supply. tively. However, there is a limit to
how much of any one spice can be
frequency of foodborne illnesses be- Of course, spice use is not the only
added before beneficial phyto-
tween modern Japan and Korea, way in which humans attempt to
chemicals become phytotoxins. Thus,
nearby countries with similar tem- hold foodborne pathogens at bay.
cookbooks from different eras are
perate climates. During 1971-1990, Meat products have traditionally
food poisoning-primarily of bacte- been preserved by thoroughly cook- more than just curiosities. Essentially,
rial origin-affected 29.2 out of ev- ing, smoking, drying, and salting them. they represent written records of our
ery 100,000 Japanese but only 3.0 Indeed, salt, which is available the coevolutionary races against food-
out of every 100,000 Koreans (Lee et world over, has been used for preser- borne diseases. By cleansing foods of
al. 1996). Lee et al. (1996) suggested vation for centuries (Multhauf 1996). pathogens before consumption, spice
that the difference may have been And today, of course, the "front line" users contribute to the health, lon-
due to cultural variations in food of defense against spoilage is re- gevity, and fitness of themselves, their
handling and preparation, and this frigeration and freezing. We hypoth- families, and their guests. A Darwin-
esize that all these practices have been ian view of gastronomy thus helps us
explanation may well be correct. But,
understand why "some like it hot"
in addition, Korean meat-based reci- adopted for essentially the same rea-
pes are spicier than those of Japan. son: to minimize the impact of micro- (spicy, that is!).
Although meat-based recipes of Ja- organisms that colonize our food.
pan collectively used Acknowledgments
more kinds of spices
We thank John Alcock, Thomas A.
(14) than those of (a) Pepper (Black & White)
Korea (8), Korean 1.0- Gavin, Thomas Neuhaus, H. Kern
Reeve, Laurel Southard, and Cynthia
recipes more fre- 0.8-
Kagarise-Sherman for ideas and en-
quently called for at
least one spice, con- S couragement; Lee A. Dugatkin, Tho-
0 mas Eisner, Paul W. Ewald, Rebecca
tained more spices 0.6-
Chasan, Gail Jarrow, Mary Ann
per recipe (Table 1), O0
0 0
0.4- Shallenberger, Philip S. Sherman, and
an anonymous reviewer for sugges-
C/) 0.20 tions on the manuscript; the librar-
Figure11. Relationships
between each non- ians at Cornell University's Mann
SL 0.0 and Nestle Libraries for assistance
regionalcountry'smean 0.0.....................
annualtemperatureand with references; and the Howard
the proportion of that L. Hughes Medical Institute, the Na-
country's meat-based 0 1 (b) Lemon & Lime Juice tional Science Foundation, and the
1.0-
recipes that call for two 0 College of Agriculture and Life Sci-
spices(pepperor lemon ences at Cornell University for fi-
or lime juice)that have w 0.8
low antimicrobialactiv- .2 0 nancial support.
ity but that may poten- L 0.6
tiate the antimicrobial S 00 References cited
effects of other spices. 0.4 * Altbacker V, Hudson R, Bilko A. 1995. Rabbit-
(a)Blackandwhitepep- O,. . ?". • . mothers' diet influences pups' later food
per (r = 0.001, df - 32 0.2 choice. Ethology 99: 107-116.
P = 0.996). (b) Lemon Ames BN, Profet M, Gold LS. 1990. Dietary
andlimejuice(r= 0.260, 0.0 0 0
pesticides (99.99% all natural). Proceed-
df = 32, P = 0.137). ings of the National Academy of Sciences of
Modifed from Billing 0 5 10 15 20 25 30 the United States of America 87: 7777-
and Sherman(1998). Mean Annual Temperature (oC) 7781.

462 BioScience Vol. 49 No. 6

Bair FE, ed. 1992. The Weather Almanac. 6th herbs and extracts from these and other teratogens. Pages 327-365 in Barkow J,
ed. Detroit (MI): Gale Research. food plants. Scientific and Technical Sur- Cosmides L, Tooby J, eds. The Adapted
Beier RC, Nigg HN. 1994. Toxicology of natu- veys, British Food Manufacturing Indus- Mind. New York: Oxford University Press.
rally occurring chemicals in food. Pages 1- tries Research Association 88: 1-56. Roubik DW. 1983. Nest and colony character-
186 in Hui YH, Gorham JR, Murrell KD, Hirasa K, Takemasa M. 1998. Spice Science istics of stingless bees from Panama (Hy-
Cliver DO, eds. Foodborne Disease Hand- and Technology. New York: Marcel Dekker. menoptera: Apidae). Journal of the Kansas
book. Vol. 3: Diseases Caused by Hazard- Hobbs BC, Roberts D. 1993. Food Poisoning Entomological Society 56: 327-355.
ous Substances. New York: Marcel Dekker. and Food Hygiene. 6th ed. London: Edward Rozin P. 1980. Acquisition of food preferences
Beuchat LR. 1994. Antimicrobial properties of Arnold. and attitudes to food. International Journal
spices and their essential oils. Pages 167- Huffman MA, Wrangham RW. 1994. Diver- of Obesity 4: 356-363.
179 in Dillon VM, Board RG, eds. Natural sity of medicinal plant use by chimpanzees Rozin P, Schiller D. 1980. The nature and
Antimicrobial Systems and Food Preserva- in the wild. Pages 129-148 in Wrangham acquisition of a preference for chili pepper
tion. Wallingford (UK): CAB International. RW, McGrew WC, DeWaal FBM, Heltne by humans. Motivation and Emotion 4: 77-
Billing J, Sherman PW. 1998. Antimicrobial PG, eds. Chimpanzee Cultures. Cambridge 100.
functions of spices: Why some like it hot. (MA): Harvard University Press. Rozin P, Vollmecke TA. 1986. Food likes and
Quarterly Review of Biology 73: 3-49. Hui YH, Gorham JR, Murrell KD, Cliver DO, dislikes. Annual Review of Nutrition 6:
Booth IR, Kroll RG. 1989. The preservation of eds. 1994. Foodborne Disease Handbook. 433-456.
foods by low pH. Pages 119-160 in Gould Vol. 1: Diseases Caused by Bacteria. New Ruhlen M. 1987. A Guide to the World's Lan-
GW, ed. Mechanisms of Action of Food York: Marcel Dekker. guages. Vol. 1: Classification. Stanford (CA):

Downloaded from https://academic.oup.com/bioscience/article/49/6/453/229475 by guest on 11 March 2023

Preservation Procedures. London: Elsevier. Johns T. 1990. With Bitter Herbs They Shall Stanford University Press.
Caterina MJ, Schumacher MA, Tominaga M, Eat It: Chemical Ecology and the Origins of ScheiperR. 1993. Hot Spice. Contact 57. Spring-
Rosen TA, Levine JD, Julius D. 1997. The Human Diet and Medicine. Tucson (AZ): field (NJ): Haarman and Reimer.
capsaicin receptor: A heat-activated ion University of Arizona Press. Shelef LA. 1984. Antimicrobial effects of spices.
channel in the pain pathway. Nature 389: Johns T, Chapman L. 1995. Phytochemicals Journal of Food Safety 6: 29-44.
816-824. ingested in traditional diets and medicines Sherman PW. 1988. The levels of analysis.
Chevallier A. 1996. The Encyclopedia of Me- as modulators of energy metabolism. Re- Animal Behavior 36: 616-618.
dicinal Plants. New York: DK Publishing. cent Advances in Phytochemistry 29: 161- Sockett PN. 1995. The epidemiology and costs
Cichewicz RH, Thorpe PA. 1996. The antimi- 188. of diseases of public health significance, in
crobial properties of chile peppers (Capsi- Johri RK, Zutshi U. 1992. An Ayurvedic for- relation to meat and meat products. Journal
cum species) and their use in Mayan medi- mulation "Trikatu" and its constituents. of Food Safety 15: 91-112.
cine. Journal of Ethnopharmacology 52: Journal of Ethnopharmacology 37: 85-91. Surh Y-J, Lee SS. 1996. Capsaicin in hot chili
61-70. Lee W-C, Sakai T, Lee M-J, Hamakawa M, Lee pepper: Carcinogen, co-carcinogen, or
Coe SD. 1994. America's First Cuisines. Austin S-M, Lee I-M. 1996. An epidemiological anticarcinogen? Food and Chemical Toxi-
(TX): University of Texas Press. study of food poisoning in Korea and Japan. cology 34: 313-316.
Deans SG, Ritchie G. 1987. Antibacterial prop- International Journal of Food Microbiol- Tainter DR, Grenis AT. 1993. Spices and Sea-
erties of plant essential oils. International ogy 29: 141-148. sonings. New York: VCH Publishers.
Journal of Food Microbiology 5: 165-180. Letarte A, Dube L, Troche V. 1997. Similarities Todd ECD. 1994. Surveillance of foodborne
Dillon VM, Board RG, eds. 1994. Natural and differences in affective and cognitive disease. Pages 461-536 in Hui YH, Gorham
Antimicrobial Systems and Food Preserva- origins of food likings and dislikes. Appetite JR, Murrell KD, Cliver DO, eds. Foodborne
tion. Wallingford (UK): CAB International. 28: 115-129. Disease Handbook. Vol. 1: Diseases Caused
Drewnowski A, Rock CL. 1995. The influence Lin RI-S. 1994. Pharmacological properties by Bacteria. New York: Marcel Dekker.
of genetic taste markers on food accep- and medicinal use of pepper (Piper nigrum Varnam AH, Evans MG. 1991. Foodborne
tance. American Journal of Clinical Nutri- L.). Pages 469-481 in Charalambous G, ed. Pathogens. London: Mosby-Year Book.
tion 62: 506-511. Spices, Herbs, and Edible Fungi. Amsterdam: Walker JRL. 1994. Antimicrobial compounds
Duke JA. 1994. Biologically active compounds Elsevier. in food plants. Pages 181-204 in Dillon
in important spices. Pages 201-223 in Milgram NW, Krames L, Alloway TM. 1977. VM, Board RG, eds. Natural Antimicrobial
Charalambous G, ed. Spices, Herbs, and Food Aversion Learning. New York: Ple- Systems and Food Preservation. Wallingford
Edible Fungi. Amsterdam: Elsevier. num Press. (UK): CAB International.
Elgmork K. 1982. Caching behavior of brown Moyler DA. 1994. Spices-recent advances. Weigel RM, Weigel MM. 1989. Nausea and
bears (Ursus arctos). Journal of Mammal- Pages 1-71 in Charalambous G, ed. Spices, vomiting of early pregnancy and pregnancy
ogy 63: 607-612. Herbs, and Edible Fungi. Amsterdam: outcome: A meta-analytical review. British
Farrell KT. 1990. Spices, Condiments, and Sea- Elsevier. Journal of Obstetrics and Gynaecology 96:
sonings. 2nd ed. New York: Van Nostrand Multhauf RP. 1996. Neptune's Gift: A History 1312-1318.
Reinhold. of Common Salt. Baltimore: Johns Hopkins [WHO] World Health Organization. World
Flaxman SM, Sherman PW. In press. Morning University Press. Health Report 1996. The State of World
sickness: A mechanism for protecting the Nakatani N. 1994. Antioxidative and antimi- Health. Geneva: World Health Organiza-
embryo. Quarterly Review of Biology. crobial constituents of herbs and spices. tion.
Fraenkel GS. 1959. The raison d'etre of second- Pages 251-272 in Charalambous G, ed. Zaika LL. 1988. Spices and herbs: their antimi-
ary plant substances. Science 129: 1466- Spices, Herbs, and Edible Fungi. Amster- crobial activity and its determination. Jour-
1470. dam: Elsevier. nal of Food Safety 9: 97-118.
Giese J. 1994. Spice and seasoning blends: A Parker G. 1995. Eastern Coyote: The Story of Ziauddin KS, Rao HS, Fairoze N. 1996. Effect
taste for all seasons. Food Technology 48: Its Success. Halifax (Canada): Nimbus Pub- of organic acids and spices on quality and
87-90. lishing. shelf-life of meats at ambient temperature.
Govindarajan VS. 1985. Capsicum produc- Parry JW. 1953. The Story of Spices. New Journal of Food Science and Technology
tion, technology, chemistry, and quality. York: Chemical Publishers. 33: 255-258.
Part I: History, botany, cultivation, and Pelchat ML, Rozin P. 1982. The special role of Zohary D, Hopf M. 1994. Domestication of
primary processing. CRC Critical Reviews nausea in the acquisition of food dislikes by Plants in the Old World: The Origin and
in Food Science and Nutrition 22: 109-176. humans. Appetite 3: 341-351. Spread of Cultivated Plants in West Asia,
Hargreaves LL, Jarvis B, Rawlinson AP, Wood Profet M. 1992. Pregnancy sickness as adapta- Europe, and the Nile Valley. 2nd ed. Ox-
JM. 1975. The antimicrobial effects of spices, tion: A deterrent to maternal ingestion of ford (UK): Oxford University Press.

June 1999 463