VOLUME 73, No.

1 MARCH 1998

THE QUARTERLY REVIEW

ofB JOLOGY

ANTIMICROBIAL FUNCTIONS OF SPICES:

WHY SOME LIKE IT HOT

JENNIFER BILLING* AND PAUL W.SHERMAN

SectionofNeurobiology
and Behavior,CornellUniversity
Ithaca,NY 14853 USA
ABSTRACT
Althoughspiceshave beenimportant forcenturies infoodpreparationthroughout theworld,
patternsofspiceusedifferconsiderablyamongcultures and countries.Whatfactors underliethese
differences?Whyarespicesusedat all? To investigatethesequestions, wequantified thefrequency
of use of 43 spicesin themeat-based cuisinesof the36 countries for whichwe could locate
traditionalcookbooks.A totalof4578 recipesfrom93 cookbooks was analysed.Wealso compiled
information on thetemperature and precipitation
in eachcountry, therangesofspiceplants,and
theantibacterialpropertiesofeachspice.Thesedata wereused to investigate thehypothesis that
spicesinhibitorkillfood-spoilagemicroorganisms. In supportofthisis thefactthatspiceplant
secondary compoundsarepowerful antimicrobial and antifungal)agents.As
(i.e., antibacterial
mean annual temperatures (an indicatorofrelativespoilageratesofunrefrigerated foods) in-
creased,theproportion ofrecipescontainingspices,numberofspicesperrecipe,totalnumberof
spicesused,and use ofthemostpotentantibacterial spicesall increased,
bothwithinand among
countries.Likewise,theestimatedfractionofbacterialspeciesinhibited perrecipein eachcountry
waspositively withannual temperature.
correlated
Severalalternativehypotheseswereconsidered-thatspicesprovidemacronutrients, disguise
thetasteand smellofspoiledfoods,orincreaseperspiration and thusevaporative cooling;italso
is conceivablethatspiceuseprovidesno benefits. However,noneofthese fouralternatives was
wellsupportedbyour data. Theproximate reasonspicesare used obviously is to enhancefood
palatability.But theultimatereasonis mostlikelythatspiceshelpcleansefoodsofpathogens
and thereby contributeto thehealth,longevity
and reproductive successofpeoplewhofind their
flavorsenjoyable.

* Presentaddress:191 Quail HollowLane, EastAmherst,

NY 14051USA.

The Quarterly March 1998, Vol. 73, No. 1

ReviewofBiology,
Copyright? 1998 by The Universityof Chicago. All rightsreserved.
0033-5770/98/7301-0001$2.00

3
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4 THE QUARTERLY REVIEW OF BIOLOGY
INTRODUCTION
AROMATIC PLANT materialshavebeen
used in food preparation for thousands
of years (Parry1953; Govindarajan1985). An-
cientVedic textsand theAyurvedictextsof Sus-
rutaand Caraca (Johriand Zutshi 1992) indi-
cate systematicuse of spices in regions where
the plantsgrewnaturally(e.g., Hindustan and
the Spice Islands). When Alarich,leader ofthe
Goths, besieged Rome in 408 AD, he de-
manded as ransom 5000 lbs. of gold and 3000
lbs. of pepper(Scheiper 1993). In the Middle
Ages and after,hazardous voyageswereunder-
takenbyfamousseafarers,such as Marco Polo
fromItaly;Pedro Cabral, Vasco da Gama, and
Ferdinand Magellan from Portugal; Christo-
pher Columbus and Hernando Cortes from
Spain; and by numerous sailors fromFrance,
England and the Netherlands in order to es-
tablishroutes to tradingportsin primaryspice-
growingregions (Parry1953). Spice trade was
so crucial to national economies thatrulersre-
peatedlymounted costly expeditions to raid
spice-growingcountries,and strugglesto con-
trolthemprecipitatedseveralwars (Govindar-
ajan 1985).
What are spices?A spice may be defined as
"anydried,fragrant, aromatic,or pungentvege-
table or plant substance,in the whole,broken,
or groundform,thatcontributesflavor,whose
primaryfunctionin food is seasoning rather
than nutrition,and thatmaycontributerelish
or piquancy to foods or beverages" (Farrell
1990:17). Sources of spices include "1) aro-
matic lichens; 2) any part of a tree or woody
shrub or vine used forflavoring;3) roots,flow-
ers, seeds, or fruitsof herbaceous plants such
as saffronand ginger,the leaves of which are
not used forflavoring;and 4) extractsor essen-
tialoils ofanyoftheseplants"(Morton1976:5).
Thus, "spice" is a culinaryratherthan a botani-
cal term.
Culinary texts (e.g., Farrell 1990; Tainter
and Grenis 1993) generally distinguish be-
tween seasonings (spices used in food prepa-
ration) and condiments (spices added after
food is served), but they do not distinguish
between herbs and spices. In their book,
Loewenfeld and Back (1974) define herbs bo-
tanicallyas plants "more or less softor succu-
lent, mostlygrownfromseeds and not devel-
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VOLUME 73
oping woody,persistenttissue"and state that
"herbs are usually used freshand are consid-
ered to be a better flavouringin their fresh
state" (p 17).
But whyare spices used? The most obvious
answeris thattheyenhance the flavorand pal-
atabilityof food, but this is only a proximate
explanation; it does not address the ultimate,
evolutionary question of why people find
foods tastierwhen theyare flavoredwithplant
secondarycompounds. Answersto such proxi-
mate and ultimatequestions are complemen-
tary,and fullunderstandingrequires explana-
tionsat both levels of analysis(Sherman 1988;
Alcock and Sherman 1994). In thispaper we
explore ultimate-levelquestions by focusing
on the hypothesisthatadding spices to foods
is beneficialbecause spices contain substances
thatinhibitor kill food-spoilage microorgan-
isms. It is well known that some spices have
antibacterialand antioxidantproperties(Shelef
1984; Deans and Ritchie 1987; Zaika 1988;
Beuchat and Golden 1989; Beuchat 1994; Na-
katani 1994). Moreover,spices have long been
used to preservefood in traditionalsocieties
(Meyer 1918:186-187; Rivers and Hill 1971;
NkangaandUraih 1981; Rusuletal. 1997) and
industrialcountries(Hoffmanand Evans 1911;
Pruthi1980; Dillon and Board 1994; Ziauddin
et al. 1996). For centuries,spices also wereused
in embalmingto preventthe decay of corpses
(Parry 1953). However, the idea that spices
servean antimicrobialfunctionhas neverbeen
systematically investigated.
Here we evaluate fourcriticalpredictionsof
the antimicrobialhypothesis:(i) spices should
kill or inhibitfood-spoilage microorganisms;
(ii) spice use should be heaviestin hot climates,
where (unrefrigerated)foods spoil most rap-
idly; (iii) spices with the most potent antimi-
crobial propertiesshould be favoredin areas
wherefoods spoil mostquickly;and (iv) spices
used in a region should be especially potent
against local pathogens. We also investigated
several alternativebenefits of spice use, in-
cluding thatof providingmacronutrients,dis-
guisingthe smell or tasteofspoiled foods,and
increasing perspiration (thereby enhancing
evaporative cooling). Finally,we considered
the "null" hypothesisthatspice use per se con-
fers no benefits,and that people simplyuse
whicheveraromaticplantsare available locally
to flavortheirfood.
MARCH 1998 ANTIMICROBIAL FUNCTIONS OF SPICES 5

TABLE 1
Countriesincludedin thisstudy,climaticvariables,numbersofrecipessurveyed,
and traditionalcookbooksconsultedformeat-basedrecipes
Mean Mean Number of
Temperature Precipitation Recipes
Country (OC) (cm) (n) Cookbooks

Thailand 27.6 149.6 118 Chaslin and Canungmai 1987; Vista 1978
Philippines 27.0 193.5 118 Alejandro 1982; Claudio 1977
India 26.9 117.6 91 Sahni 1980; Muthachen 1969; Pandya 1980; Patil 1988
Malaysia 26.9 235.0 60 Harben 1983; Fernandez 1985
Indonesia 26.8 204.7 120 Owen 1976; DeWit and Borghese 1973
Nigeria 26.5 139.2 82 Anthonio and Isoun 1982; Hafner 1993; Ritzberg 1993
Ghana 25.9 106.3 95 Dede 1969; Ritzberg 1993; Nyaho et al. 1970
Vietnam 24.6 170.2 84 Duong and Kiesel 1991; Ngo and Zimmerman 1979
Brazil 23.9 177.8 132 Moliterno 1963; De Andrade 1965
Mexico 23.1 95.3 123 Kennedy 1978; Blue 1977
Kenya 22.1 108.0 73 Hyder 1976; Gardner 1993; Ritzberg 1993
Ethiopia 21.1 88.9 56 Mesfin 1987; Ritzberg 1993
Lebanon 20.6 80.5 98 Salloum 1992; Farah 1979
Israel 19.1 53.8 145 Bar-David 1964; Nahoum 1971
Australia 18.6 91.9 64 McKenzie and Allen 1980; Cameron et al. 1980
Morocco 18.3 25.4 104 Day 1975; Carrier 1987
South Africa 17.2 48.1 108 Higham 1950; De Villiers 1961
Greece 16.7 60.7 118 Kremezi 1993; Mark 1974; Barron 1991
Iran 16.7 20.3 85 Hekmat 1994; Shaida 1992; Batmanglij 1992
Portugal 15.0 77.2 84 Sarvis 1967; Anderson 1986
Japan 14.3 144.5 103 Chen 1988; Martin and Martin 1970
Italy 14.0 80.5 86 Bugialli 1992; De' Medici 1990
Korea 12.1 121.4 81 Morris 1945; Millon and Millon 1991; Shim 1984
France 12.1 75.4 216 Willan 1981; Escudier and Fuller 1968
Hungary 10.3 56.3 80 Lang 1971; Weiss and Buchan 1979
Ireland 9.6 93.5 90 Sheridan 1965; Armstrong1986
England 8.8 72.1 223 Boyd 1976; Grigson 1985
Germany 8.8 67.3 169 Schuler 1955; Adam 1967
Austria 8.8 85.6 188 Mayer-Browne1961; Langseth-Christensen1959
Denmark 8.3 62.2 87 Hazelton 1964; Jensen 1962
Poland 7.8 52.3 141 Zeranski 1968; Czerny 1975
Sweden 5.4 53.8 134 Berg 1963; Jakobsson 1989
Finland 3.0 57.4 62 Benton 1960; Viherjuuri et al. 1974
Norway 2.8 96.0 77 Sverdrup 1962; Holmboe 1957
Countries with Regional Differences
United States
Northern 8.6 92.9 453 Cleveland 1952; White 1993; Ferguson 1989;
Southern 17.8 90.2 Flavor of theSouth1989; Olivet Episcopal 1960;
Wilson 1990; Brown 1987; SouthwestCooking1990;
Karousos et al. 1993
China
Northeast 13.4 85.3 430 Hom 1990; Schreckerand Schrecker1976; Simoons 1991;
Southwest 19.4 132.7 Lo 1971, 1979; Lee and Lee 1976; Low 1982;
Chang et al. 1982; Mei 1978; Kan and Leong 1963

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6 THE QUARTERLY REVIEW OF BIOLOGY VOLUME 73

To evaluate these hypotheses,we gathered ferentspices used and the average number of
data fromseveral extensiveand diverselitera- spices per recipe. If two books togetherpro-
tures.Our approach was, of necessity,correla- vided <50 meat-based recipes, a third (or
tional rather than experimental, and we in- fourth,etc.) book was consulted to increase
ferredbut did not directlymeasure how spice the sample size. Based on these criteria,we
use affectsthe fitnessof individuals.This rep- located 93 traditional cookbooks from 36
resentsthe "forwardmethod" forstudyinghu- countries (Table 1), representingeveryconti-
man social evolution (Sherman and Reeve nent and 16 of the world's 19 "language fami-
1997). Our results suggest that spice use is lies" (Ruhlen 1987).
beneficial, and yield intriguinginsightsinto
the question ofwhycuisines ofdifferentcoun- SELECTION OF SPICES
triesvaryso much in spiciness. We considered all spices (n=43) used in
meat-basedrecipes, regardlessof the quantity
METHODS or form (dried, powdered or fresh) called for
SELECTION OF CUISINES (Table 2). For analyses, we grouped spices
We quantified the spices used in the cui- whose essentialoils contain the same chemical
sines of countries for which we could locate components (Farrell 1990). Thus, "capsicum"
>50, and preferably> 100, meat-basedrecipes includes all capsaicin-containing peppers (chil-
from at least two traditional cookbooks. A ies,genus Capsicum)except paprika and green
meat-basedrecipe is one in which at least one- peppers; the lattertwohave undergone artifi-
thirdof its total volume or weightconsistsof cial selection to contain minimal capsaicin
red meat, poultry, pork, veal or seafood; (Wilkins1994). "Onion" includes leeks,chives,
soups, stews, roasts and casseroles are in- shallots and onions, and "pepper" includes
cluded. We focused on meat-basedrecipes be- white and black pepper (although nearlyev-
cause unrefrigeratedmeats spoil faster and eryrecipe called forblack pepper only).
are associated with foodborne disease out- Onions and chiliespresenteda special prob-
breaks more often than vegetables (Bryan lem because theycan be used either as main
1988; Roberts 1990; Todd 1994, 1996; Sockett dishes or onlyas spices. Since theyalwaysadd
1995), so any relationshipbetween microbial flavor (propyl disulfides and capsaicins, re-
contamination and spice use should be evi- spectively)to recipes, we considered them to
dent in meat-based recipes. And since meat- be spices, regardless of the quantities called
based recipes typicallyare far more common for. Salt was not included in our analyses be-
than vegetarian recipes in traditional cook- cause it is not a plant product and therefore,
books, we were able to obtain adequate sam- technically,not a spice. However, as will be
ple sizes forstatisticalanalyses. seen, reasons for salting and spicing foods
We considered a cookbook "traditional" probably are similar.
when authors stated thattheirpurpose was to
record a country's cuisine for posterity.Au- ANTIBACTERIAL PROPERTIES OF SPICES

thorsoftenwere native to or had lived in the Bacteria have been more commonly in-
country,and our sources frequentlywere En- criminatedin food poisoning and foodborne
glish translations of native-language cook- disease outbreaks than yeastsand fungi (e.g.,
books. We avoided experimentaland modern Varnam and Evans 1991; Todd 1994, 1996).
cookbooks, and those writtenprimarilyfor Therefore,we focused on the possible antibac-
American audiences (as indicated in the title terialpropertiesof spices. We searched the lit-
or preface). Of course, cookbooks were se- erature for informationon foodborne bacte-
lected without regard to the frequencywith ria thathave been experimentallychallenged
which theirrecipes called forspices. To mini- witheach spice, and the "inhibitory"abilityof
mize the possible effectsof authors' biases each spice-whether the spice killed the bac-
(e.g., preferencesforspicyor bland recipes), teriumoutrightor slowed its growth(Appen-
we consulted -2 cookbooks foreach country. dix A). We located original sources by con-
In fact,cookbooks fromthe same countryal- sultingreviewarticles(e.g., Deans and Ritchie
waysdeviated <5% in the totalnumber of dif- 1987; Beuchat and Golden 1989; Beuchat

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MARCH 1998 ANTIMICROBIAL FUNCTIONS OF SPICES 7

TABLE 2
Spiceplants and theirnativeand domesticated rangesin the34 "nonregional"
countries
in thisstudy(i.e., all exceptChina and theUnitedStates)

a (a%
SPICE FAMILY SPECIES ;~~~~~~~~~~~~~~~~~~~~~~I
co
V80
E
0 'V "V -; ) .rd'r- <r C _0<
rd0
m
.(XX0|
@?
XEtr
0 aa 2 Svc(U2 4 r

- a- _ . .

ALLSPICE Myrtaceae PImentad/o/ca X X X X X X I _ I I I I I X_X I I XX

ANISE Umbelliferae PimpInellaanisum X X X _XI I XXX x X x X X XX X

BASIL Labiatae OcImumbasIlicum X _ XXXXXXXXX XX XXXXX XX XX X

BAY Lauraceae Laurus nobills X X X X X X X'X X X XX X X

CAPERS Caparidaceae Capparls

spinosa X I I I XX X
_X X X xXX XX _ X I I I
CARAWAY Umbelliferae Canrm
carv/ I I I X X XXxxXXX X X XX X X X
CARDAMOM Zingiberaceae Elletariacardamomum X X X X X X I X X X. X XXX ||X X

CELERY Umbelliferae Ap,umgraveolens I I I XX X X X X XXX XX XX XX XI X

CHILI PEPPER Solanaceae Capsicum frutescens X X X XlX XXX X X lXlXXX XIX x

XX XX | X |X

CINNAMON Lauraceae Cinnamomumzeylanicum X X X X X X I I I I I X Ix X I I

CLOVES Myrtaceae Syzygiumaromaticum X X X X X X X I ixX

CORIANDER Umbelliferae sativum

Coriandrum X X X X X X X X X X X_ X X X X X X X XI iX X

CUMiN Umbelliferae Cuminumcyminum X X X X X X X X X X X I X I

DiLL Umbelliferae Anethum

graveolens X _ _ _ X X XX X X X
FENNEL Umbeliiferae Foenlculumvulgare XXX. X X X X X X X X X X XX XX XX X| | X

FENUGREEK Leguminosae Trigonellafoenumgraecum X -X I I I

GARLiC Liliaceae Alliumsat/vum X X X X X xxx X xX XXX X X X X X Xx X X X X X X X X XX

GINGER Zingiberaceae Zingiberofficinale X X X X X X X X X X X

HORSERADISHCruciferae Armnoracia
lapathifolia X X X X X X X X X X.
JUNIPER Cupressaceae Juniperuscommunis X X X X X X X X X X X X X

LAOS Zingiberaceae Alpineagalanga X X X X X X _ I

LEMON Rutaceae Citruslimon X X X X X X X. X X_ XI X I I
LEMONGRASSGramineae citratus
Cymbopogon X1 X XX X X X X_ _ I I X X X
LIME Rutaceae Citrusaurantffol/a X X X X X X X X XlX
MARJORAM Labiatae Origanummajorana I X X XX X X XI X X X X X

MINT Lablatae Mentha

arvensis X X X X IX I XXX X X X X X X X X X.X XXX
X X
MUSTARD Cruclferae Brassica juncea XX XXXX X
XXX
XIX XXXXX X X X X |X | I| XI

NUTMEG Myristicaceae Myristica

fragrans X X X X X X X Xx

ONION Lillaceae AllIumcepa X X X X X X X X X X X X X X X X X X X X X XX X X X X X X X X X XX

OREGANO Labiatae Origanum

vulgare X I -X X X X XX _XX X
XIX X
PAPRIKA Solanaceae Capsicum annum X X X X X XlXX X X XXXX X XX XX | X X

PARSLEY Umbelliferae ur
Petroselinumcrispum X X X XX X X X X XXlx X X X X X

PEPPER Plperaceae Piperni/gnm X. X X X X X I _ ___X I I XX

ROSEMARY Labiatae Rosmarinus

oi4icinafis I X X X X X X X X X X X I X_
SAFFRON Irldaceae Crocus sativus X X X X X X X X _

SAGE Labiatae Salvia officinalis X X X X X X X X X X X X X X X X

SAVORY Lablatae SatureJahortensis X I X XI X X I I X X X _ I -X

SESAME Pedaliaceae Sesamum indicum X X X X X X X X I I X X |X X X|

SWEET PEPPER Solanaceae Capsicumgrossum X X X X X X X X X X X X X X X XX

X X X X X X

TAMARIND Leguminosae TamarindusIndica X X X X X X X X X X X X X X

TARRAGON Compositeae Artemlsia dracunculus X XX XX X XlX xlXX

THYME Labiatae Thymusvulgaris X X XXX X X

TURMERIC ZingiberaceaeCurcumalonqa X _X X X XX X XX Xx

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8 THE QUARTERLY REVIEW OF BIOLOGY
1994) and on-line databases (e.g., Agricola,
Biosis,FSTA, and Medline). Most studieseval-
uated spices as food preservatives,in attempts
to identifyminimum concentrations neces-
saryto suppress bacterial growthwithoutad-
verselyaffectingflavor.
We included inhibition studies regardless
of whether they tested the spice in its pow-
dered form or as purified active ingredients
(e.g., volatile oils or oleoresins). We only in-
cluded those studies that identifiedbacteria
to species, but we did not tryto distinguish
"strains"withinspecies. We also did not differ-
entiateamong studiesthattesteddifferent col-
ony sizes of bacteria. Not all bacteria have
been studied foreveryspice, and some spices
weretestedon manymore bacteriathanothers.
Studies sometimes reached dissimilarcon-
clusions about whethera spice inhibiteda par-
ticularbacterium. We resolved discrepancies
that resulted fromdifferingdefinitionsof in-
hibitionwithour "inclusive"definitionofinhi-
bitionas the mortality or retardationof growth.
Concentrationsof spices testedvaried consid-
erably(e.g., 100-100,000ppm), and in some
cases differentspice concentrationsled to dif-
ferentconclusions. Ifa studyreportinginhibi-
tion fora particularspice testeda higher con-
centrationthan the studyor studies reporting
no inhibition,we assumed the spice was in-
deed inhibitory.However,ifstudies using the
same concentration reported contradictory
results, or if the study reporting inhibition
used a lowerconcentration,we eliminatedthe
bacteriumfromconsideration relativeto that
spice. Studies thatdid not reportthe concen-
trationstestedwere not included.
We wanted to quantifythe proportion of
local food-spoilagebacteria thatwould be in-
hibited by recipes fromeach country.Unfor-
tunately,however,no comprehensivelistofin-
digenous bacteria existsforanycountry,so we
had to estimatethisdegree ofinhibition.First,
we listed the 30 species of bacteria that have
been experimentally challenged with the
greatestnumber of spices, regardless of how
frequentlytheywere inhibited (Appendix B).
All 30 were challenged with >10 spices, and
most with ?20 (21/30 = 70.0%); the mean
number of spices used to challenge each bac-
teriumwas 18.2 ? 3.6 (sd). Next,we randomly
picked 30 recipes from the cookbooks for
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VOLUME 73
each country(by numberingrecipes consecu-
tivelyand consulting a random numbers ta-
ble), and tallied how many of our 30 target
bacteria were inhibited by at least one spice
in each recipe. Each set of resultsfor the 30
recipes was averaged, yielding an estimateof
the mean number of bacterial species inhib-
ited per recipe per country.Althoughthisesti-
mate is crude, itis unbiased, and probablyrep-
resentative because most of our 30 target
bacteria are distributedworldwide.
CLIMATE DETERMINATIONS
The climateof each countrywas determined
by averaging monthlytemperature and pre-
cipitationdata fromeach major citylisted in
TheWeatherHandbook (Conwayand Liston1990).
Some countries include regions that differ
greatlyin latitude and altitude, resultingin
majordifferences in mean annual temperatures.
Potentiallythis presented us with opportuni-
ties to assess variationsin spice use among dif-
ferentclimaticregions.Unfortunately, among
these countries,we could locate regionalcook-
books only for China and the United States.
We analysedthe climateofthese twocountries
in the followingmanner.
Although Chinese cuisine often is subdi-
vided into fourgeographicalregions (Simoons
1991), traditional cookbooks were available
onlyfornortheasternand southwesternChina
(Table 1). Northern and eastern China have
similar (continental) climates,with hot sum-
mers, cold winters and little precipitation;
southernand westernChina also have similar
(subtropical) climates,withhot, humid sum-
mers,mild wintersand moderate rainfall(Si-
moons 1991). We calculated the mean annual
temperature and precipitation for the cities
of Lanzhou, Beijing, Tianjin, Shenyang and
Shanghai in north and east China, and Kun-
ming, Changsha, Hankow, Chungking, Can-
ton and Nanning in the south and west,using
data in Conway and Liston (1990) and Bair
(1992).
Traditional cookbooks also were available
for the northernand southern United States
(Table 1). We characterizedthese climatesus-
ing Bair's (1992) data on the citiesof Buffalo,
New York, Pittsburgh,Portland, San Fran-
cisco, Sault Ste. Marie,Washington(DC), Fair-
banks andJuneau in the north,and Albuquer-
MARCH 1998 ANTIMICROBIAL FUNCTIONS OF SPICES
que, Asheville,Atlanta,Austin,Birmingham,
Brownsville, Los Angeles,
El Paso,Jacksonville,
Louisville,Miami,Nashville,New Orleans and
Phoenix in the south.
STATISTICAL ANALYSES
Cross-cultural analysesalwaysconfront"Gal-
ton's problem" (Hartung 1982) of selecting
societies for comparison thatadequately rep-
resent a range of cultural variation but min-
imizing cases in which similaritiesare due to
recent common derivationor diffusion.Ana-
lysingcross-culturaldata also is problematic
and controversial.Of course, independence
of specificculturalpractices is statistically
de-
sirable but, as discussed by Ember and Otter-
bein (1991) and Mace and Pagel (1994), inde-
pendence oftenis impossible to assess.
In an attemptto increase the independence
of our data, we initiallysearched for cook-
books from cultures or tribes listed in Mur-
dock's (1967) StandardCross-Cultural Sample.
Unfortunately, we were largelyunsuccessfulin
matching Murdock's sample. Therefore we
sought traditionalcookbooks fromas broad a
range of countriesas possible. We discovered
that28 of the 36 countriesforwhichwe found
appropriate cookbooks belong to different
"tribal clusters"according to Murdock (also
Murdock and White 1969). To improveinde-
pendence, we triedomittingall except one of
the countries that certainlyor probably be-
long to each cluster,but thisseverelyreduced
our sample size and the range of variation.
Moreover, the advisabilityof arbitrarilyomit-
ting countries is questionable when their de-
grees of independence for a specificcultural
practice are unknown (Ember and Otterbein
1991).
The use of cladisticmethods to inferinde-
pendence of cultureshas been suggested,but
as pointed out byseveralrespondentsto Mace
and Pagel (1994:557-564) as well as Mace and
Pagel, themselves (1997:305), it may not be
appropriate to apply maximum parsimony
techniques thatwere developed forinvestigat-
ing biological origins to inferringcultural
"phylogenies."Moreover,the recentreportby
Ricklefsand Starck (1996) that comparative
analyses of physiological and morphological
traits(of birds) based on phylogeneticrecon-
structionsyielded similarconclusions to those
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9
based on correlationof traitvalues of individ-
ual species, regardless of relatedness, raises
the question ofwhen controllingforphyloge-
netic independence is essential (Weathers
and Siegel 1995).
Nonetheless,we attemptedto use Mace and
Pagel's (1994, 1997) phylogenetic methods
(based on linguisticsimilarities)to select coun-
triesfor inclusion in our analyses. However,
consideringonlycountriesthatbelong, unam-
biguously, to different"linguistic families"
(Ruhlen 1987) cut our sample size to thepoint
analysesweremeaningless.More-
thatstatistical
over,phylogeneticreconstructionsof societal
relationships based on linguistic similarities
do not necessarilyyield inferencesabout the
independence of spice-use patterns.
Otterbein (1994:559) stated he "certainly
would not cease using worldwide samples in
comparative research because of the alleged
difficultiesthat arise from the nonindepen-
dence of cases." Moreover,as Hartung (1997:
347) pointed out, "Galton's problem... is like
noise in a signal. It is more likelyto obscure
truerelationshipsthan to generatefalseones."
We thereforeincluded in our analyses all 36
countries for which we obtained traditional
recipes (Table 1), with the caveat that some
countriesare more nearly"independent"than
others.
We used standard nonparametric statisti-
cal procedures, primarilyPearson product-
moment correlations (r), partial correlations,
and chi-squareanalyses (Minitab Release 10.5
Xtra). When multipletestswithina hypothesis
were performed,P values were adjusted with
Bonferronicorrections (Moore and McCabe
.1993) to minimizeType 1 errors (Rice 1989).
Proportional data were appropriately trans-
formed (arc sine square root) foranalyses.
RESULTS
GENERAL PATTERNS OF SPICE USE
Of the 4578 meat-based recipes we ana-
lysed,4241 (93%) called forat least one spice.
The mean number of spices per recipe was
3.9 (?+1.7 sd). In ten countries (28%), namely
Ethiopia, Kenya, Greece, India, Indonesia,
Iran, Malaysia, Morocco, Nigeria and Thai-
land, every meat-based recipe called for at
least one spice. By contrast,in Finland and
Norway,respectively,19 of 62 (31%) and 25
10 THE QUARTERLY REVIEW OF BIOLOGY VOLUME 73

C 1.0

.2- 0.9-
a 0.8-

0.7-

0.6-

0.5-
0*
0.4-

.2 0.3-
o 0.2-
0.
o 0.1

=
Omm O EE 4& ?) 0 0 E a)
@@w =.
1 E, oO X;
L-
X
0 2C
- OEEo Mme) r0 -

Spice
FIGURE 1. PROPORTIONS OF 4578 MEAT-BASED RECIPES SURVEYED THAT CALLED FOR EACH OF 43 SPICES.
Data are from 93 traditional cookbooks from 36 countries (see Table 1).

of 77 meat-based recipes (33%) did not call "temperate" (10-21? C), and "cold" (<100 C)
forany spices. climates. In general, countries with hot cli-
Among various cuisines, individual spices matesuse numerous spices,manyofwhichare
are not used equally often (Figure 1). Onion commonly called for (i.e., in >40% of reci-
and pepper are called forin well over half ofpes), whereas countries with cooler climates
all meat-basedrecipes (65% and 63%, respec- use fewer spices, most of which are rarely
tively).Other frequentlyused spices are garlic
called for (in <5% ofrecipes). Histogramsfor
(35%), capsicums (24%), lemon and lime hotter countries approximate normal distri-
juice (23%), parsley (22%), ginger (16%), butions while those for cooler countries ap-
and bayleaf (13% ). The vastmajorityofspices proximate negative exponentials. We quanti-
are called forin <10% (35/43 spices = 81 %) fied this variation by calculating kurtosis
or in <5% of all recipes (29/43 = 67%). (degree of peakedness) and skew (degree of
asymmetry)for all 34 frequency-of-use histo-
CLIMATIC VARIABLES
grams (Hinkle etal. 1988). Figure 3 showsthat
Temperature both measures decrease significantly within-
The countries in our sample represent a creasingmean annual temperatures(kurtosis:
wide spectrumofclimates(Table 1), withmean r=-0.542, df=32, P=0.001; skew: r=-0.512,
annual temperatures ranging from 2.80 C P=0.002).
(Norway) to 27.60 C (Thailand). Among the Spice contentsof recipes also varywithcli-
34 nonregional countries (i.e., those without mate. Among the 34 nonregional countries,
regional cookbooks), patterns of spice use there are significantpositive correlationsbe-
also differconsiderably,as illustratedin Fig- tweenmean annual temperaturesand propor-
ure 2 for representativecountries with "very tions of recipes that call forat least one spice
hot" (mean annual temperature >260 C), (r=0.740, df=32, P<0.001; Figure 4a), and

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MARCH 1998 ANTIMICROBIAL FUNCTIONS OF SPICES 11

mean annual temperaturesand mean num-
bers of spices per recipe (r=:0.572, P=0.002;
Figure 4c); the correlationbetween tempera-
turesand numbers of differentspices used in
each countryalso is positive,but not signifi-
cant (r=0.216, P=0.286; Figure 4e). Propor-
tions of all spices used in each countrythat
are called for "frequently"(i.e., in >40% of
recipes) are positivelycorrelated with mean
annual temperatures (r=0.426, P=0.012),
whereas proportions of spices used in each
countrythat are called for "infrequently"(in
<5% of recipes) are inverselycorrelatedwith
temperatures(r=:-0.450, P=0.010).
The use of many individual spices varies
withthe climate.For ten spices thereare posi-
tive correlations between mean annual tem-
peratures and frequencies of use (percent of
recipes per countrythatcalled for the spice).
As shown in Figure 5, thisgroup includes cap-
sicums (r=:0.757, df=32, P<0.001), garlic (r=
0.635, P<0.001), and onion (r=0.652, P<
0.001), as well as anise (r=0.377, P=0.028),
cinnamon (r=0.347, P=0.044), coriander (r=
0.582, P=0.001), cumin (r=0.435, P=0.010),
ginger (r= 0.462, P=:0.006), lemongrass ( r=
0.478, P=0.004), and turmeric (r=0.393,
P=0.021). Among these,cinnamon,coriander,
cumin and gingerare used primarilyin coun-
trieswithmean temperatures >160 C, and anise,
lemongrass and turmericare used almost ex-
clusivelyin veryhot countries ( -26' C). For
twospices,dill (r= -0.365, P=0.034) and pars-
ley (r= -0.365, P=0.034), there are negative
correlationsbetween mean annual tempera-
turesand frequencies of use.
Relationships between mean temperature
and frequencyof use of basil, bay,cardamom,
celery,cloves, green peppers, mint,nutmeg,
saffronand oregano all are positivebut non-
significant(all P>0.05), and relationshipsbe-
tween temperature and frequency of use of
allspice, bay, celery,marjoram, mustard,pa-
prika,rosemary,sage and thymeare negative
but nonsignificant.The other 14 spices in our
sample are used too infrequently(in too few
countriesor too fewrecipes) to permitstatisti-
cal analyses.
Precipitation
Mean annual precipitationamong countries
ranges from20.3 cm (Iran) to 235 cm (Malay-
sia; Table 1). For the 34 nonregional coun-
tries,frequency-of-use histogramsdo not vary
systematically with annual precipitation,and
there are no significantcorrelationsbetween
precipitation and skew (r= -0.316, df=32,
P=0.069) or kurtosis (r=:-0.337, P=0.061).
There also are no correlations (all P>0.10)
between mean annual precipitationand pro-
portions of recipes that call for at least one
spice (r=0.235; Figure 4b), mean numbers of
spices per recipe (r=0.220; Figure 4d), num-
bers of differentspices used in each country
(r=0.129; Figure 4f), or proportionsof spices
used in each countrythat are called for in
>40% of recipes (r=-0.191) orin <5% of reci-
pes (r= -0.304). There are no significantcor-
relations between frequencies of use of any
spice and mean annual precipitation.
We conducted partial correlation analyses
to see ifprecipitationaffectsspice-usepatterns
when temperature is controlled statistically.
Holding mean annual temperaturesconstant,
there still are no significantpartial correla-
tions (all P>0.05) between mean annual pre-
cipitationand numbersof different spicesused
in each country(partial r= 0.229, df=31), pro-
portions of recipes that call for at least one
spice (partial r=-0.328), mean numbers of
spices per recipe (partial r= 0.204), or propor-
tions of spices used in each countrythat are
called for in >40% of recipes (partial r=
0.061) or in <5% ofrecipes (partialr -0.049).
There also are no significantpartial correla-
tions between frequencies of use of any spice
and precipitation,when temperature effects
are controlled.

FIGURE 2. FREQUENCY-OF-USE HISTOGRAMS SHOWING PROPORTIONS OF MEAT-BASED RECIPES THAT CALLED

FOR EACH SPICE IN SELECTED COUNTRIES WITH DIFFERENT MEAN ANNUAL TEMPERATURES.
Indonesia and India represent countries with "hot" climates (mean annual temperature >260 C),
Israel and Hungary representmore "temperate"climates (10-21? C), and Ireland and Norwayrepresent
"cold" climates (<100 C). Spices are arranged from highest to lowest percent of use, so their order
varies. Histograms for hotter countries more closely approximate normal distributionsthan do those
for cooler countries; the latterapproximate negative exponential curves. (See pages 12-13)

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12 THE QUARTERLY REVIEW OF BIOLOGY VOLUME 73

a) 1 (a) Indonesia

(I)
Kurtosis = 1.3
o Skew =1.6
= 120 recipes
QU gn

co a)~~~~~~~E . c
)-9C oE E)
Q c

Israel
0)

_ (~~~~~~~~~C)

I- ~~~~~~~~~~~~~~~~~~~~~~~~~~~~Ku
=7.8
o_
Co- = 2.8
~~~~~~~~~~~~~~~~~~~~~~~~~~Sk
a) n = 145 recipes
.2 CIIUT rT00c IaO
|5 a)Z,tD c:-O10"0 am 10=: T
TE' T 01 oC0~D-'e
-1 co'm?1cDc:
CL~~~~_C
g aX mO U
E , E E a E: E 0 2' Eg E E 3C % ECL 2 m o E CODE
-o3
o. cpaE E : CZ>00 0
;E =3 0E03 C,5
) E _F Z=
t _ C'
)2C13- t
'I- ~~~~~~~~~~~~~~~=: 0) _C C
0-I :C
0t
t
t- ( t$
0)~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~-

.2 (e)Irelan

0
a.
oLM Kurtosis = 8.8
= 3.0
~~~~~~~~~Skew
0.. = 90 recipes
~~~~~~~~~~n

a COc,UU) ~ zCL o t

i~00C: a) C E DC = - =C '
U) Ect CE3 C$
CO,CD t
-0C: EC E
CDEU
)0
0. 0)~~~~~~~~~~~~oC E0)
$ C

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MARCH 1998 ANTIMICROBIAL FUNCTIONS OF SPICES 13

1.0

0.8 (b) India

0.6

0.4- Kurtosis = 0.7

Skew 1.0
0.2- n = 91 recipes

0.0 TVV1F1VFVF r
C~~~~~~EEgo~~c ~CE
C e OCD C 2: COD) 1 5=n ' cO u
Q)(, D
o0o.-e C E E 0 - C
a$ Ct$-C
1.0
-c
0~~~~~cr -c:C C3 00 aO oC5 D~-
) :CoMC

~~
vO.E3~~~~~C 0
0Cc E
1 .0 0~O~E- coCc

0.8 (f Norwary
4 c0 -c ?2 2
0.6- ED 0)>s
C cts.? E E
=3ED
0 (D
4D c
4 D
cD4E:
E E
E:;_
D a)E
E
D Yec
CZC
2~ ODCDX
E_E-Eo
)

CIO)

0.4 ~~~~~~~~~~Kurtosis
= 19.2
0.2 kew =
~~~~~~~~S 4.3
00: ! TT111111II I n1=71rec11es 1

O'cu C Cci-Ci_Lo*
a_ 3 _ 0)E E i,C- E2 cmE:
0 CI)
c Cc
cL ME ,CL-
o
LCD C0 C-%,_ ZC--O0 C ci,
CL E E c 20 0CD
U)~~~~~~~~~~~~~~~~~~c
_ co 0
CD -

1 Cc0- 0

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14 THE QUARTERLY REVIEW OF BIOLOGY VOLUME 73

20.0 (a) ANTIBACTERIAL PROPERTIES OF SPICES

We obtained informationon the antibacte-
15.0- rial propertiesof 30 spices (Appendix A). All
of them (100%) inhibitsome species of bacte-
2 10.0- 0
ria, 24 (80%) inhibit?50%, 15 (50%) inhibit
-75%, and 4 (13%) inhibit100% (Figure 6).
5.0- 0 0 The average spice inhibits 67% (+23%) of
bacteria. Garlic, onion, allspice and oregano
0.0 ,0 ..... inhibiteverybacterium theyhave been tested
on; at the otherextreme,lemon and limejuice
5.0 (b) inhibitonly 24% of bacteria.
4.0- There is a significantpositive correlation
: * 0 0 (r=0.668, df=31, P<0.001) betweenmean an-
3.0- *| . .; ..... .
B nual temperaturesand mean proportions of
recipes that call for each highly inhibitory
Cnl 2.0- (-75% bacterial inhibition) spice used in
0 0

1.0- 0
each country (Figure 7a). This means that
more powerful spices are used more fre-
0.0 . quentlyin hotterclimates. By contrast,there
0 5 10 15 20 25 30 is no correlation between temperaturesand
Mean Annual Temperature(OC) mean proportionsof recipes thatcall foreach
less inhibitory(<75% inhibition) spice used
FIGURE 3. RELATIONSHIPS BETWEEN MEAN ANNUAL in each country(r=0.248, P>0.10; Figure 7b).
TEMPERATURE AND (a) KURTOSIS
There is a positivebut nonsignificantcorre-
(PEAKEDNESS) AND (b) SKEW
lation between proportionsof bacteria inhib-
(ASYMMETRY) IN FREQUENCY-OF-
USE HISTOGRAMS (AS IN FIGURE 2)
ited by each spice and proportions of coun-
FOR SPICES USED IN THE 34 tries that use each spice (r=0.213, df=28,
NONREGIONAL COUNTRIES P=0.06; Figure 8), suggestingthatmore pow-
SAMPLED (EXCLUDING CHINA AND erfulspices are used more widely.Even more
THE UNITED STATES; SEE TABLE 1). interesting(Figure 9), proportions of 30 tar-
get bacterial species (Appendix B) inhibited
by the spices called forin each country'sreci-
By contrast, when precipitation is con- pes increasesignificantlywith increasingannual
trolledstatistically thereare significantpartial temperatures (r=0.516, df=31, P=0.001).
correlations (all P<0.05) between mean an- This implies that recipes from hotter coun-
nual temperaturesand numbers of different trieshave more antibacterialpotential.
spices used in each country(partial r0.324),
MACRONUTRITIONAL PROPERTIES OF SPICES
proportionsof recipes thatcall forat least one
spice (partial r=0.780), mean numbers of Considerable comparative information is
spices per recipe (partial r=0.612), and pro- available on the composition of foods and
portions of spices used in each countrythat spices (e.g., Pruthi 1980; Tan 1985; Holland
are called for in >40% of recipes (partial et al. 1991; Tainter and Grenis1993). Virtually
r0.485); annual temperaturesand propor- everyspice in our analysescontains some pro-
tionsof spices called forin <5% of recipes are tein (5-30 g/100 g), fat (0.5-35.0 g/100 g),
inverselycorrelated (partial r-0.466). Use and carbohydrates(5-50 g/100 g), and small
of capsicums, garlic,onion, anise, cinnamon, quantities (0.1-15.0 mg/100 g) of four vita-
coriander,cumin,ginger,lemongrassand tur- mins (carotene, thiamin,riboflavinand nia-
mericare positivelycorrelatedwithmean tem- cin) and ten inorganic elements. Among the
peratures (all significant,P<0.05) when pre- latter,calcium, magnesium, phosphorus and
cipitation is controlled statistically,whereas potassiumoccur in 0.005-2.5 g/l 00 g concen-
use of dill and parsley show a significantin- trations,and chlorine, copper, iron, manga-
verse correlationwithtemperatures. nese, sodium and zinc occur in 0.001-1.0

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MARCH 1998 ANTIMICROBIAL FUNCTIONS OF SPICES 15

(010 0 * e
0 m 1.0 * .0.: 0*
0. (a) 0 0 (b) . o
, 0.9 0 0.9 0

00.8 0.8

o0.0
.v0.71 0 0.7
011
.0 .

0
C 0.6- 0.6
0
0.5 , ..................

a
10- 10
(c) * (d) 0
O 8- 8-

6- ~ 0 0 6 0-

4 0.-0 4 00-

30~~~~~ 0% 00
2- 4b~~~~~~~~
0
FL *20

. 0. * 0
0 30 - ***0 * 30 - * .01
(e) 20 (f *0 0

0 ... Temperature
00.C) 0 X~0ainfall (

20 - 200

lo-
~~~~~10 0
0~~~~
0 0..

0 5 10 152025 30 0 50 100 150200 250

Mean Annual Mean Annual
Temperature(OC) Rainfall(cm)
FIGURE 4. RELATIONSHIPS BETWEEN MEAN ANNUAL TEMPERATURE (LEFT PANELS), MEAN ANNUAL
PRECIPITATION (RIGHT PANELS), AND (a,b) PROPORTION OF MEAT-BASED RECIPES
THAT CALL FOR :1 SPICE; (c,d) MEAN NUMBER OF SPICES PER RECIPE; AND (e,f)
TOTAL NUMBER OF SPICES USED IN THE 34 NONREGIONAL COUNTRIES.

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16 THE QUARTERLY REVIEW OF BIOLOGY VOLUME 73

1.0 (a) Capsicums tein, carbohydrates,fat and inorganic ele-

mentsthanthosefound in mostspices. In sum,
EL 0.8;
en compared to mostvegetables,spices are poor
0.6. sources of macronutrients,especially in the
U 0.4* tinyquantitiesgenerallyused in cooking.
w
SPICE USE AND AVAILABILITY
o 0.2.
0.0
0 .0 * * 0
We determined the native and domesti-
cated ranges of spice plants fromdata in Hor-
) 1.0 nok (1992), Hylton(1974),Janicket al. (1981),
(b) Garlic
0.8 * . Kowalchikand Hylton (1987), Schery (1972),
and Morton (1976). We had assumed initially
> 0.60
0.4'~~~~~~~~~~ thatmostspice plantsgrowonlyin the tropics,
0 0~~~~~~~~~~ but this turned out to be untrue (Table 2);
0.40.2-~~~~~
0 we found no relationshipbetween a country's
o 0.2. mean annual temperatureand the number of
X 0.0- ,
spice plant species that grow there (r=0.081,
0. df=32, P>0.10; Figure 10). However,positive
Q 1.0 correlationsdo exist between the number of
a) (c) Onion*
Cc0.8- . *8 countriesin which each spice plant growsand
o 0.6 * 00'. 00 the number that use it (r=0.352, df=34,
P--0.035; Figure 11), and between mean an-
0~~~~~
0.4 . nual temperaturesand proportions of spices
used in the countries in which they grow
o 0.2-
?L
0
(r=0.444, df=34, P=0.010). This means that
"L 0-0-i.
OL ...........1'''1''' although residentsof hottercountriesdo not
0 5 10 15 20 25 30 have more local spice plants to choose from
Mean Annual Temperature(?C) than residentsof cooler countries,people in
hottercountriesuse a greaterfractionofthose
FIGURE 5. RELATIONSHIPS BETWEEN MEAN ANNUAL spice plants that are available (especially the
AND PROPORTION OF
TEMPERATURE
potent antimicrobials:Figure 7).
MEAT-BASED RECIPES THAT
Spices are used both in countries where
CALLED FOR CAPSICUMS (CHILIES),
IN THE 34
they grow and where they do not grow. No
GARLIC, AND ONION
NONREGIONAL COUNTRIES
country's recipes include every spice that
(EXCLUDING CHINA AND THE grows there. We quantified the variation by
UNITED STATES). dividing the number of countries in which
each spice growsby the number of countries
thatuse each spice. In our sample, thisindex
ranged from1.0 to 0.1 (Figure 12) witha mean
g/100 g concentrations. Few spices contain of 0.60 ? 0.25, indicatingthatmost spices are
detectable amounts of fattyacids, cholesterol, used in more countriesthan theygrowin. Five
starch,sugars or fiber. spices are used in the same number of coun-
All themacronutrients, vitaminsand miner- tries as grow them. Among these, garlic and
als contained in spices also are found in such onions are grown in everycountrythat uses
common vegetables as carrots, beans, broc- them, whereas juniper, lemongrass and laos
coli, rice,corn,lentils,potatoes and yams.Un- are used in some countrieswhere theydo not
like spices,thesevegetablesalso contain starch, growbut are not used in the same number of
sugars,fiberand fattyacids. In addition, the countrieswhere theydo grow.
vegetables contain concentrations of caro- Proportions of recipes that call for each
tene, thiamin, riboflavinand niacin equiva- spice varybetween countrieswhere thatspice
lent to those found in most spices, a greater growsversuswhere it does not grow.For 22 of
varietyof vitamins (including Bi, B2, C and the 30 spices (73%), proportionaluse is higher
folicacid), and higher concentrationsof pro- in countrieswhere the plant grows;14 ofthese

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MARCH 1998 ANTIMICROBIAL FUNCTIONS OF SPICES 17

~~ 4---1 1 *- _ ~~~~~~~~~75%
bacterial
0.8
100 *** inhibition

0.9

0.7
co
0.. 0.- I :i0004% bacerial

0~~~~~~~~~~~~~~~~~~
0.2-~~~~~~~~~~~~~~~~~~~~~~0
._~
X E m 0 %@
4)oXX

Spice
FIGURE 6. ANTIMICROBIALPROPERTIES(INHIBITIONOF GROWTHOR KILLING) OF 30 SPICES FOR
WHICH APPROPRIATE DATA WERE AVAILABLE (SEE APPENDIX A), ARRAYED FROM
GREATEST TO LEAST INHIBITION.
All spices inhibit some species of food-spoilage bacteria they have been tested on, and about half
inhibit 75% of bacteria.

22 differencesare significant (i.e., P<0.05, peratureonlyamong countrieswhere itgrows

Mann-Whitney U tests).Among the eightspices
used more frequentlyin countrieswhere they
do not grow,only one difference(allspice) is
significant.
We investigatedhow proportionsof recipes
thatcall foreach spice varywithmean annual
temperaturesamong countrieswherethe plant
grows versus where it does not grow. Garlic
and onions grow everywhere,and their fre-
quencies of use are positivelycorrelated with
temperature(Figure 5). There also are signifi-
(r=0.539, P=0.031), and for cinnamon (r=
0.632, P=0.001), cardamom (r=0.460, P-
0.048), and green peppers (r0.753, P=0.005)
significantpositive correlations occur only
where the plants do not grow. For the re-
maining spices, there are no correlationsbe-
tween frequencies of use and temperature
when data are subdivided according to where
each plant grows.
PEPPER AND LEMON AND LIME JUICE

cant positive correlations between tempera- Use patternsof lemon and lime juice and
tureand frequencyofuse ofcapsicums (where black and whitepepper are unusual forseveral
chiliesgrow,r=0.706,P<0.001; wheretheydo reasons. First,although they are among the
notgrow,r0.852, P=0.001), coriander(grows, fivemostfrequentlyused spices (Figure 1) and
r=0.560, P=0.008; does not grow, r=0.648, appear in the meat-based cuisine of every
P=0.017), and cumin (grows, r=0.719, P= countryin our sample, they are among the
0.008; does not grow,r=0.441, P=0.040). For least effectivebacteriocides (Figures 6 and 8).
parsley,use is positivelycorrelated with tem- Indeed, lemon and lime juice inhibit only

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18 THE QUARTERLY REVIEW OF BIOLOGY VOLUME 73

- 1.0-
06 Spices that Inhibit:
. (a) > 75% of bacteria
(0
U) 0.8- 0
co 0.4
0~~~~~~~~~~ ~ ~ ~ ~ ~
0~~~~~~~~~~~ 0

0~~~~~~~~~~~~~~
06 0.20
-
0 0.2
?w 0.4-
X 0

O 0.2-
o
0 0 06-Spices that Inhibit: 0.0-
.(b) 0 < 75% of bacteria 0.0 0.2 0.4 0.6 0.8 1.0
0.,0.5- . Proportion of Bacteria Inhibited
by Each Spice
0. 4-
FIGURE 8. RELATIONSHIP BETWEEN PROPORTIONS
? 0.3-*** * * OF BACTERIAL SPECIES INHIBITED BY

. EACH SPICE AND PROPORTIONS OF

0 0.2-. COUNTRIES WHOSE MEAT-BASED
RECIPES CALL FOR THAT SPICE.
0.10- Circleddata pointsare pepperand lemon/lime
juice.
0.0
600 1 15
0 2 25 30
Mean Annual Temperature (OC)
includesmanycountrieswithtemperateand
F GURE 7. RELATIONSHIPS BETWEEN MEANANNUAL
TEMPERATURE OF COUNTRIES AND
cold climates,wherepepper is typically the
MEAN PROPORTIONS OF MEAT-BASED
mostfrequently used spice (e.g.,Scandinavia;
RECIPES THAT CALL FOR EACH OF THE see Figure2). The averagefrequency ofuse of
(a) (075%
HIGHLY INHIBITORY pepper (mean proportionof recipes/coun-
BACTERIAL INHIBITION) SPICES try)is higherin countrieswhereit does not
USED IN THE COUNTRY, AND (b) LESS grow(X=67.5 ? 17.9%ofrecipes)thanwhere
INHIBITORY (<75% INHIBITION) itdoes grow(X=57.0% ? 22.3%), butthisdif-
SPICES USED IN THE COUNTRY. ferenceis notsignificant.
REGIONAL DIFFERENCES WITHIN COUNTRIES

24% of bacteria studied, pepper only 38% Althoughmany countriesinclude areas

(Appendix A); however,pepper does strongly
inhibit some microorganisms,including the
ubiquitous Clostridiumbotulinum(Nakatani
1994). Second, frequencies of use of pepper
(r=0.001, df=32, P=0.996)
limejuice ( r=0.2 60, P =0. 137) are not corre-
latedwitha country's
meantemperature
(Fig-
ure 13), unlike the patternfor the other "top
five''spices (onion, garlic and capsicums: Fig-
ure 5), as well as many others. Third, lemon
and lime (Citrus) trees and pepper (Piper)
plants grownaturallyor are cultivatedprimar-
ilyin the tropics,so the majorityof countries
we sampled must import them (Table 2). This
withdifferent climates,wewereable to locate
regionalcookbooksonlyfortheUnitedStates
and China (Table 1). In bothcountries, spice-
use patternsdifferbetweenclimaticregions
and lemon and (Figure14). Frequency-of-use histograms for
northeastern China,whichhas a temperate
climate,are significantly(P<0.05) morekur-
totic(12.81) and skewed(3.70) thanthosefor
southwestern China (kurtosis = 6.42, skew=
2.75), whichhas a subtropicalclimate.Like-
wise, histogramsfor the northernUnited
Statesare significantly more kurtotic(8.07)
and skewed(2.83) thanthoseforthesouthern
United States (kurtosis=3.61,skew=2.17).

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MARCH 1998 ANTIMICROBIAL FUNCTIONS OF SPICES
1.0
<v5.-
0.8
0~~~~~~~~~~
0.68
0o 0.4 . (n 10-
OL
C o
X. 0.20
0.0-1
0 ....................
10 15 20 25
Mean Annual Temperature (OC)
FIGURE 9. RELATIONSHIP BETWEEN MEAN ANNUAL
TEMPERATURE AND (ESTIMATED)
PROPORTIONS OF FOODBORNE
BACTERIAL SPECIES INHIBITED PER
RECIPE IN EACH COUNTRY (SEE
TEXT AND APPENDIX B).
The "outlier" data point is Japan (see text) .
These differencesare mirrored in countries
withdifferent mean annual temperatures(see
Figures 2 and 3).
Spice contents of meat-based recipes also
vary between climatic regions within China
and the United States. The patternis similar
to but less dramaticthan thatamong different
countries (e.g., Figure 4) . In China the follow-
ing are greater in the southwest than the
northeast:(i) totalnumber of spices used (15
vs. 14), (ii) proportion of recipes thatcall for
at least one spice (93% vs. 90%), (iii) mean
number of spices per recipe (3.2 vs. 2.3), and
(iv) proportion of spices used in the region
thatare called forin >40% of recipes (21.3%
vs. 13.8%); only the lattertwo differencesare
significant(P<0.05, X2tests).The proportion
of spices used that are rarelycalled for (in
<5% of recipes) is higher in northeast than
southwestChina (50 % vs.42%), but not signif-
icantlyso.
Within the United States the followingare
greaterin the south than the north: (i) total
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19
30
.
O
? 20-
0~~~~~~~~~~~~~0
C, *0 @
0O
0
Z 0 5 10 15 20 25 30
Mean Annual Temperature(OC)
30
FIGURE 10. RELATIONSHIP BETWEEN MEAN ANNUAL
TEMPERATURE OF COUNTRIES AND
NUMBER OF SPICE PLANT SPECIES THAT
ARE GROWN IN EACH COUNTRY.
number of spices used (35 vs. 33), (ii) propor-
tion of recipes that call for at least one spice
(99% vs. 90%), and (iii) proportion of spices
used that are called for in >40% of recipes
(11.3% vs.6.0%); the lattertwodifferencesare
significant(P<0.05). By contrast,the mean
number of spices per recipe (5.4 vs. 5.0) and
the proportion of spices used that are rarely
called for (66% vs.54%) is higherin the north
than in the south; the latterdifferenceis mar-
ginallysignificant(P= 0.05).
Use of some individualspices also variesre-
gionally. The ten most frequentlycalled for
spices are the same in the southernand north-
ern United States,but theirfrequenciesofuse
differ(Figure 14). Among these, pepper, gar-
lic, capsicums and lemon and lime juice are
used more frequentlyin southernthan north-
ern recipes (all significant,P<0.01, x2tests),
whereas the frequencyofuse ofginger,onion,
green pepper, anise, allspice and celeryseed
does not differsignificantly between regions.
In China, the ten most frequentlycalled for
spices also are the same in the southwestand
northeast. Pepper, garlic and capsicums are
used more frequentlyin southwesternrecipes
(all significant,P<0.01), whereas the fre-
quency of use of ginger,onion, anise, lemon
20 THE QUARTERLY REVIEW OF BIOLOGY VOLUME 73

and limejuice, green pepper, allspice and cel- 40

eryseed do not differsignificantly between re-
gions. No spice is used significantly more fre-
quentlyin the northernthan in the southern 30)
D30 . 0
region of either the United States or China.
Recipes from cooler and warmer climatic
o
0l)
..
regions of China and the United Statescall for
spices withsimilarantibacterialproperties.In S20
the southernUnited States,32% of the spices
LU
called forin >5% of recipes are highlyinhibi- Cu 0
en0 1 .
tory(inhibited _75% of bacteria) compared
*O 10.* .*.
to 36% of spices used in the northernUnited 0 0

States.In both southwestand northeastChina

50% of the spices called forin >5% of recipes
are highlyinhibitory.Ginger and onion are 5 10 15 20 25 30 35
the spices most frequentlycalled for in both
regions of both countries;as an antibacterial,
Countries Each Spice Grows In
onion is verypotent, but ginger is relatively 11. RELATIONSHIP BETWEEN THE NUMBER
FIGURE
ineffective(Figure 6; Appendix A). OF COUNTRIES IN WHICH EACH SPICE
In general, frequency of use of the more PLANT CAN BE GROWN (I.E., ITS
potent spices in individual recipes differsbe- NATIVE OR DOMESTICATED RANGE)
tweenclimaticregions.In the southernUnited AND THE NUMBER OF COUNTRIES
States,30% of recipes call forone or more of WHOSE MEAT-BASED RECIPES CALL

the nine highlyinhibitoryspices (>75% inhi- FOR THAT SPICE.

bition) used there,whereas in the north 22%

of recipes call for at least one of these highly
inhibitory spices (P<0.05, Mann-Whitney test).
By contrast, in the southern United States
only 25% of recipes call for at least one less
inhibitory spice (<75% inhibition),versus40%
of northernrecipes (P<0.01). In southwestern
China, 40% of recipes call for at least one of
the four highlyinhibitoryspices used there,
versus 30% of recipes from northeastern
China (P<0.05). In southwesternChina, 39%
of recipes call for at least one less inhibitory
spice, versus 33% of northwesternrecipes
(P>0.08). As a resultof these differences,the
estimated proportion of bacterial species in-
hibited per recipe is 60% + 25% in the south-
ern United States versus 53% ? 32% in the
north,and 33% + 15% in southwesternChina
versus 30% ? 19% in the northeast;neither
differenceis significant.
DISCUSSION
The world over, spices have been used for
centuriesin preparationofmeat forconsump-
tion or long-termstorage (Parry 1953). Our
analysesof traditionalmeat-basedcuisinesindi-
cate, however,thatspices are not used equally
oftenin differentcountries and regions (Fig-
ures 1-3, 14). This variationenabled us to eval-
uate and compare predictionsfromalternative
hypothesesthatwould explain these patterns
of spice use. Although the data we compiled
varywidelyin quality,theyare certainlyunbi-
ased withregard to any particularadaptive or
nonadaptive hypothesisbecause theywere all
gathered forother purposes.
We hypothesizedinitiallythatthe benefitof
spices mightlie in theirantimicrobialproper-
ties. The secondary metabolites and essential
oils that give spice plants theirdistinctivefla-
vors probably evolved to counter biotic ene-
mies such as herbivorous insects and verte-
brates, fungi,pathogens, and parasites (e.g.,
Fraenkel 1959; Ehrlich and Raven 1964; Koul
1993; Walker 1994). This insightis potentially
important because humans are afflictedby
manyof these same biotic enemies, in particu-
lar the bacteria and fungi that live on and in
dead plant and animal matter (Johns 1990).
If spices kill such microorganismsor inhibit
theirproduction of toxins,spice use mightre-
duce chances of contracting foodborne ill-
nesses or food poisoning.
Our results support several predictions of

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MARCH 1998 ANTIMICROBIAL FUNCTIONS OF SPICES 21

1.0-

0.. 0.8-

00o
0L6

U 0.2

0.0 XX XEo Xon E o

E o ucuIMMG 08u t 'c EGw

?C
o XE X om
EQ
'

Spice
FIGURE 12. SPICES ARE USED BOTH WHERE THEY GROW AND WHERE THEY DO NOT GROW.
Each bar represents the number of countries in which each spice grows naturally or is cultivated,
divided by the number of countries that use each spice. For most spices the index is <1.0, indicating
that they are used in more countries than they grow in.

this hypothesis.In agreement with previous
reports (e.g., Shelef 1984; Deans and Ritchie
1987; Zaika 1988; Beuchat 1994; Nakatani
1994), all spices forwhichwe could locate ap-
propriate informationhave some antibacte-
rialeffects(Figure 6; Appendix A): halfinhibit
-75% of bacteria,and four (garlic,onion, all-
spice and oregano) inhibit100% of those bac-
teriatested.In addition, manyspices are pow-
erfulfungicides(e.g., Thompson and Cannon
1986; Thompson 1989; Ahmed et al. 1994;
Beuchat 1994), and can thus preventproduc-
tion of deadly fungal metabolites (e.g., myco-
toxin: Beuchat 1994).
Many spices are also synergists.When com-
bined, those spices exhibit greaterantibacte-
rial effects than when each is used alone
(Shelef 1984; Johns 1990; Beckstrom-Stern-
berg and Duke 1994). This is interestingbe-
cause recipes in our sample call foran average
offourdifferentspices. Some spices are so fre-
quently combined that the blends have ac-
quired special names (see Tainter and Grenis
1993:147-154), such as "chili powder" (typi-
callya mixtureof red pepper, onion, paprika,
garlic,cumin and oregano) and "orientalfive
spice" (pepper, cinnamon, anise, fennel and
cloves). A particularlyintriguingexample is
the French "quatre epices" (pepper, cloves,
ginger and nutmeg), which often is used in
making sausages. Sausages (botulusin Latin)
are a rich medium for bacterial growth,and
frequentlyhave been implicatedas the source
ofdeath frombotulismtoxin;thevalue ofanti-
bacterial compounds in spices for sausage
preservationand preventionof toxin produc-
tion is obvious. Use of multiple spices, espe-
ciallywhen combined withcitricor acetic acid
and salt,and then heated, produces the most
powerful antimicrobial effects (Kurita and
Koike 1982; Gould 1992; Liu and Nakano
1996; Ziauddin et al. 1996).
The antimicrobialhypothesisassumes that
concentrationsofspice chemicalsin meat-based
recipes are sufficientto produce the desirable
effects,and thatthese effectsare not destroyed
by cooking. Analysesof spice concentrations
in prepared dishes,along withtheircombined

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22 THE QUARTERLY REVIEW OF BIOLOGY VOLUME 73

antimicrobialpotency,which are required to 1.0 (a) Pepper (Black & White)

evaluate this assumption, are just beginning
(see Board and Gould 1991; Rusul et al. 1997). 0.8
Concentrationsofspice extractsused to flavor ., 0.6 *
and preservecommercialmeat products,pick-
les and breads generallyrange from0.5 to 1.0 0 0.42
g/kg (1: 2000-1: 1000 or 500-1 000 ppm; Salzer 0 -
1982), althoughhigherconcentrations(>2000
ppm) of some spices are required to preserve 0.0-
certain foods (Galli et al. 1985). Many of the
(b) Lemon & Lime Juice
L_
studies of spices as antibacterials (Appendix
0_
o- ?1.0-
1.0-
A) tested concentrations <1000 ppm (e.g.,
v 0.8
Huhtanen 1980; Kivancand Akgul 1986; Zaika
1988; Ismaiel and Pierson 1990a; Kivanc et al. 0.6-
1991). We calculated that the recipes in our
0.4
sample call forroughly0.25-3.0 g/kgofspices o
0.2 .* x * -.*.
(1:4000-1:3000 or 250-3000 ppm). This im- 0.2' : *. . . .
plies that concentrations of spices used in
cooking are sufficientto yield useful antibac- 0.0
0 5
.
10
. ....
15
.......
20 25 30
terialeffects,in agreementwithShelef (1984), Mean Annual Temperature (OC)
Giese (1994), and Liu and Nakano (1996).
This may not always be true, however. Far- FIGURE 13. RELATIONSHIPS BETWEENMEANANNUAL
brood et al. (1976) reported thatrosemaryin- TEMPERATURE OF COUNTRIES AND
hibited the growthof Staphylococcus aureusin PROPORTION OF MEAT-BASED
media at concentrationsof 0.1%, but was ef- RECIPES THAT CALL FOR (a) BLACK
fectivein meat onlyat concentrationsover an OR WHITE PEPPER, AND (b)

order of magnitude higher. LEMON OR LIME JUICE.

Effectsof cooking on the antimicrobialpo-
tency of spices are essentiallyunknown. On
the one hand, commercial extractionof spice thermostablespices are usuallyadded earlyin
spices
oleoresins and essential oils often involve preparation and the most thermolabile
are added near the end of cooking (or are
steam distillationat high temperatures.Gas
used primarilyas condiments), these differ-
chromatogramsthat compare steam-distilled
ences in timing of use may relate to main-
spice chemicals against C02-extracted prod-
taining beneficial (antimicrobial) properties
ucts (at low temperatures)typicallyshow simi-
until food is served. Loss of flavorwould be a
lar patterns (Moyler 1994), indicating that
useful proximate indicator of loss of antimi-
spices are thermostable.Furthermore,Diebel
crobial potency.
and Banwart(1984) found thatoregano, sage A second prediction of the antimicrobial
and ground cloves stillinhibited Campylobacterhypothesisis thatspice use should be heaviest
jejuni (a major cause of gastroenteritis)after in areas where foods spoil most quickly.Haz-
16 hours of simmeringat 250 C and 42? C. On ard analysesand epidemiological studiesindi-
the other hand, Chen et al. (1985) reported cate thatratesofbacterialgrowthincrease dra-
that higher cooking temperaturesdestroyed maticallywith air temperature (Genigeorgis
the antimicrobialeffectsof a fewother spices. 1981; Brown 1982; Bryan 1988). Meat dishes
Differentspices are oftenadded to recipes that are prepared in advance and stored at
at differentpoints in preparation. For exam- room temperaturesformore thana fewhours,
ple, onion, garlic,pepper and rosemarytypi- especially in tropical climates, typicallyshow
callyare added at thebeginning,whereaspars- massive increases in bacterial counts (Bryan
leyand cilantro (coriander leaf) generallyare et al. 1979; Michanie et al. 1988; Hobbs and
added near the end. According to cookbook Roberts 1993). Moreover, bacteria are con-
authors, the "delicate" flavors of the latter fined to the surface of meat during the loga-
would be destroyed by cooking. If the most rithmic phase of growth (Gill and Penny

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MARCH 1998 ANTIMICROBIAL FUNCTIONS OF SPICES
1977), and thatis where spices would be effec-
tiveagainstthem.Thereforeit is relevantto ask
how spice use changes as temperaturevaries.
We found that countries with hotter cli-
mates used spices more frequentlythan coun-
tries with cooler climates (Figures 2-5). In-
deed, in hot countriesnearlyeverymeat-based
recipe calls forat least one spice and most in-
clude many spices, whereas in cooler coun-
tries substantial fractionsof dishes are pre-
pared withoutspices, or withjust a few.The
result is a significantpositive correlation be-
tweenmean temperaturesand estimatedpro-
portions of foodborne bacteria inhibited per
recipe (Figure 9). Of course, temperatures
withindwellings,particularlyin food prepara-
tion and storage areas, may differfromthose
of the outside air, but usuallyit is even hotter
in the "kitchen"(e.g., Michanie et al. 1988).
In climateswithdistinctiveseasons, annual
mean temperaturesdo not accuratelyreflect
temperaturescharacteristicof each season. A
more detailed analysiswould consider spice-
use patternsrelativeto seasonal differencesin
foodborne diseases. For example, in the north
temperate zone, outbreaks of bacterial food
poisoning peak during the hottest months
(e.g., in summer: Salmonella:Doyle and Cliver
1990; E. coli:Griffinand Tauxe 1991). The an-
timicrobialhypothesispredictsthatmore po-
tent spices and a greater variety of spices
should characterizedishes typicallyprepared
in "summer"than in "winter."Unfortunately,
we wereunable to locate enough seasonal reci-
pes forany countryto evaluate thiscorollary.
Differencesin spice use between northern
and southernregionsof the United Statesand
China (Figure 14) mirrordifferencesamong
countries (Figures 2-4), but these differences
are relativelysmaller.This is unsurprisingsince
regional differencesin the United Stateshave
had onlyabout 200 yearsto develop, and tem-
perature differentials are not great (Table 1).
Differencesbetween northeasternand south-
westernChinese cuisine have had considerably
longer to develop. However,effectsofaltitude
may obfuscate regional differencesin China.
We expectthe cuisineofpeople livingat higher
elevations (cooler climates) to contain fewer
spices and less potent spices than the cuisine
of people livingat lower elevations,where un-
refrigeratedfoods spoil faster.Elevations in
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23
southern and westernChina varywidely.Un-
fortunately,we do not know if recipes from
these regions originated in the lowlands or
highlands. If the latter,theyshould resemble
recipes from northern and eastern China in
spice-usepatterns.A highfrequencyofrecipes
from high-altitudeareas would blur differ-
ences between the southwestand northeast.
Proportionsofrecipes thatcall formanyin-
dividualspicesvarysystematicallywith climate,
both withinand among countries.Use of ten
spices increases with temperature,including
some of the most potent antimicrobials,such
as capsicums, garlic, onions, cinnamon, cu-
min and lemongrass (Figures 5 and 6; Appen-
dix A). Garlic and capsicums also are used
more frequentlyin the southern than the
northernUnited States,and garlic and capsi-
cums are used more frequentlyin southwest
than northeastChina. Frequency of use is in-
verselyrelated to temperatureonlyforparsley
and dill,and these are among the least potent
antibacterials(Figure 6).
Of course, our various testsof the antimi-
crobial hypothesisassume that "traditional"
meat-based recipes existed prior to the wide-
spread availabilityof refrigeration,so that a
country's meat spoilage rate roughly corre-
lates withits annual temperature.We cannot
directlyevaluate thisassumption,because au-
thorsof cookbooks rarelyknew the historyof
theirrecipes. However,anyrecipe in existence
formore than fivegenerations (80-100 years)
predates the widespread availabilityof elec-
tricityand refrigeration.We tried to bias our
sample in favorofthese older recipes through
judicious selection of cookbooks (i.e., we
avoided experimentaland modem cookbooks
and ignored recipes that were said to have
been recentlydeveloped). Although no one
knows precisely how long spice plants have
been grownin any particularregion or coun-
try,spices have been cultivatedforthousands
of years in the Old World (Zohary and Hopf
1994) and hundreds ofyearsin the NewWorld
(Coe 1994).
Spice use does not varysystematically
among
countriesin relationto average annual precip-
itation. Partial correlation analyses confirm
the significanteffectsof temperature when
precipitationis controlledforstatistically,
and
the insignificanteffectsof precipitation on
24 THE QUARTERLY REVIEW OF BIOLOGY VOLUME 73

Proportionof Recipes
0.0 0.2 0.4 0.6 0.8 1.0 0.0 0.2 0.4 0.6 0.8 1.0
gInger gin_er _
onlIon _onn-
pepper(b&w) pepper(b&w)
garilc garilc
capslcums~ _ capsicums
CapsicummpleoinAlI
lemonlilme- _lmni-_ mea
greenpepper~ _ greenpepper
staranise stausni
allspice e
allspic
celeryseed celeryseed
corlander
sesame (asesame) conander
(b)
cinnamon~*
dnnampoan Northern cinnamon
Northeast
anUd ~ United States ta China
-
cumin~ cumin
turmeric turmeric-
lemongrass lemongrass-
bay leaf bayleaf
l
dilweed dilweed-
nutmeg nutmeg-
mace mace-
cloves cloves
cardamom cardamom
pa rka~ pa rka-
*basil Vbasil:
mint mint-
capers capers-
caraway caraway
fennel
-fennel-
fenugreek tenugreek-
horseradish- horseradish-
-
juniper juniper
marjoram-- marJoram -
oregano oregano
rosemary rosemary K-tss=1.
Kurtosis 12.8
saffron Kurtosis 8.1 saffron
sage Skew = 2.8 sage Skew = 3.7
savory- -
n = 284 recipes savoryr n = 187 recipes
-
thyme thyme

ginger- gln er~

onion on
pepper(b&w)- pepper(b&w)
garlic gadlic _
capslcums capsicums
lemonAlme lemoMtEime
greenpepper greenpepper
staranise staranise
allspice allspice
celeryseed celeryseed
corlander - comander
((d)
sesame c sesame
cinnamon cinnamon-
parsl Southern parsley Southwest
tgalanal
cumin
UnitedStates -
galalngal
cumin-
China
turmerlc turmeric-
lemongrass lemongrass -
bayleaf bayleaf-
dillweed dillweed-
nutmeg nutmeg-
mace mace-
cloves cloves-
cardamom cardamom-
paprlka paprika-
basil basil-
mint minti
capers capers-
caraway caraway
fennel fennel-
ienugreek fenugreek
horseradish- horseradish-
juniper- -
Juniper
marioram marjoram--
oregano- oregano
- Kurtosis = 3.6 - Kurtosis 6.4
saffroy safrony
sage- Skew = 2.2 sage- - Skew = 2.8
tarragon n = 248 recipes savoryr n = 243 recipes
lhyme thyme

FIGURE 14. FREQUENCY-OF-USE HISTOGRAMS SHOWING PROPORTION OF MEAT-BASED RECIPES THAT

CALL FOR EACH SPICE IN WARMER (SOUTHERN) AND COOLER (NORTHERN)
CLIMATIC REGIONS OF CHINA AND THE UNITED STATES.

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MARCH 1998 ANTIMICROBIAL FUNCTIONS OF SPICES
spice use when temperatureis statistically con-
trolled. Although these resultsofferno defi-
nite supportforthe antimicrobialhypothesis,
theyalso do not militateagainst it. First,tem-
peraturetypicallyis more importantforbacte-
rial growththan humidity(Bryan et al. 1979;
Gilbert1979; Hobbs and Roberts1993); more-
over,concentrationsof airborne bacteria can
actuallybe reduced by high relativehumidity
or rain, whereas concentrations can be in-
creased by high temperaturesor wind veloci-
ties (e.g., Bovallius et al. 1978). Second, mean
annual precipitation may not reflectthe hu-
miditythatis typicalof a countryor region if
precipitation is seasonal, the soil porous, or
surface evaporation rapid. Third, in many
countriesopen firesare closelyassociated with
food preparation and storage areas (e.g., Mi-
chanie et al. 1988), so humiditiesin "kitchens"
maybe lower (and temperatureshigher) than
in the outside air.
A thirdprediction of the antimicrobialhy-
pothesis is thatthe most potent spices should
be favoredwhere foods spoil fastest.It is con-
ventionalwisdom thatfood fromhot climates
tends to be spicy ("hot"). Indeed, we found
thatmeat-basedrecipesfromhot countriesand
hot regionsofChina and theUnited Statesgen-
erallycontainmore spicesand spiceswithmore
potentantibacterialeffectsthan cuisinesfrom
cooler countriesor cooler regionsof countries.
There are significantpositivecorrelationsbe-
tween annual temperaturesand use of cinna-
mon, cumin,onion, garlicand capsicums (Fig-
ure 5), all ofwhichare powerfulantibacterials
(Figure 6). There also is a strongcorrelation
betweentemperaturesand proportionsofrec-
ipes thatcall forthe highlyinhibitory(-75%
inhibition) spices used in each country(Fig-
ure 7a), and a positivebut nonsignificantrela-
tionship between proportions of countries
thatuse each spice and proportionsof bacte-
rial species each spice inhibits (Figure 8). By
contrast,thereis no correlationbetween tem-
peraturesand proportionsof recipes thatcall
for each less inhibitoryspice (<75% inhibi-
tion; Figure 7b). Although a similarfraction
of the spices used in cooler and hotterregions
of the United States and China are highlyin-
hibitory,proportions of recipes calling for at
least one highly inhibitoryspice are signifi-
cantlygreaterin hotter (southern) regions of
both countries.
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25
The final prediction of the antimicrobial
hypothesis is that the spices used most fre-
quently in a region should be particularly
effectiveagainst local food-spoilage microor-
ganisms.Evaluatingthisrequires comprehen-
siveknowledge of indigenous bacteria. Unfor-
tunately,this informationdoes not exist for
any country.We attemptedto generate listsof
bacteria involved in foodborne disease out-
breaks from data supplied by the World
Health Organization and the U.S. Centersfor
Disease Control. Such informationwas avail-
able onlyfornine countries,however,most of
them European, and among these traditional
cookbooks were available for only five.More
importantly,only selected bacteria from cer-
tain recent outbreaks were identifiedto spe-
cies, selected bacteria differedamong coun-
tries,and causes of many outbreaks remain
unidentified.Thus, the data were inadequate
for generating comprehensive listsof indige-
nous bacteria.
Althoughwe were unable to testthisfourth
predictiondirectly, we note thatthereis a strong
positive correlation between mean tempera-
turesand estimatedproportionsoffoodborne
bacteria inhibited by the spices in an average
recipe (Figure 9). The 30 targetbacteria for
this analysis (Appendix B) were chosen be-
cause they have been experimentallychal-
lenged with the greatest number of spices.
Most of these microorganismsare widelydis-
tributed geographically (e.g., Aeromonashy-
drophila,Bacillus cereus,B. subtilus,Clostridium
botulinum, Escherichia
Listeriamonocytogenes, coli,
Salmonellapullorum,Staphylococcus aureus), so
theyare likelycontaminants in the foods of
most countries.Moreover,actual proportions
of indigenous foodborne bacteria inhibited
per recipe probablyare higherthan indicated
in Figure 9 for countrieswithmean tempera-
tures>210 C because the spices used mostfre-
quently in hot climates (e.g., capsicums, gar-
lic, onion, cinnamon and cumin) are such
powerful antibacterials (Figure 6). Use of
these broad-spectrum antimicrobial chemi-
cals should raise the fraction of indigenous
bacteria inhibited in hotterclimates,making
the actual relationshipbetween temperature
and inhibitionper recipe even stronger.
There is an intriguing,order-of-magnitude
differencein the frequencyof foodborne ill-
26 THE QUARTERLY REVIEW OF BIOLOGY
nesses between modern Japan and Korea.
From 1971 to 1990 food poisoning, primarily
of bacterial origin,affected29.2/100,000Jap-
anese but only 3.0/100,000 Koreans (Lee et
al. 1996). This differenceseems surprising,es-
peciallysince these nearbycountrieshave sim-
ilar,temperateclimates.Lee et al. (1996) sug-
gested thatthisdifferenceis owing to cultural
differencesin food handling and preparation
procedures, and this may well be so. But, in
addition, Korean recipes are spicier. Com-
pared toJapanese recipes, Korean recipes (i)
more frequentlycall for at least one spice
(88% vs. 74%), (ii) contain more spices per
recipe on average (3.6 vs. 2.2), and (iii) more
frequentlycall for ,:1 highlyinhibitoryspice
(75% vs. 54%). As a result,the estimatedpro-
portion offoodborne bacteria inhibitedbyan
average recipe is significantly(P<0.01) higher
in Korean (51%) thanJapanese cuisine (12%;
see Figure 9). Why traditionalJapanese reci-
pes do not call for more potent spices is un-
known. One possibilityis that the spices used
in traditionalJapanesecuisine were adequate
protection against bacteria when fresh sea-
food was available from local waters. Today,
since more food is imported and comes from
fartheraway,it may contain more species of
foodborne bacteria and fungi. Traditional
Japanese recipes may not include enough
spices (antimicrobials) to cope withthese new
infestations.
Use patternsofpepper and lemon and lime
juice at firstappear to contradictthe antimi-
crobial hypothesis.Although theyare among
the five most frequentlyused spices (Figure
1), theyare among thefiveleasteffective against
bacteria (Figure 6), and theirfrequencyofuse
is not positivelycorrelated with temperature
(Figure 13). Moreover,most countriesin our
sample import these spices; Citrustrees and
Piperplants are available locally in only 9-11
countrieswithwarm climates (Table 2).
however,lemon and limejuice
Interestingly,
to enhance the
(citricacid) act synergistically
antibacterial effectsof other spices (Bach-
mann 1916; Booth and Kroll 1989; Giese 1994;
Ziauddin et al. 1996), probably because low
pH disrupts bacterial cell membrane func-
tion. As a result, foods to which an acid is
added require relativelymild heating to cause
the same levelsofbacterialmortalitythattakes
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VOLUME 73
place in foods that are cooked longer and at
higher temperatures in the absence of the
acid (Gould et al. 1983; Gould 1992). Pepper
also has synergistic effects;itfunctionsas a bio-
availabilityenhancer, increasing the rate at
which the active ingredients in other spice
chemicals become physiologicallyavailable to
or are absorbed by epithelial cells (Johriand
Zutshi 1992), and also presumablybymicroor-
ganisms. In addition, pepper is a powerful
antioxidant,which by itselfoftenis sufficient
to prevent oxidative food deterioration (Lin
1994). Perhaps the widespread use of pepper
and citrusjuices relates to theirpropertiesas
antimicrobialsynergists(and antioxidants).
Under the antimicrobialhypothesis,correla-
tionsbetweenfrequenciesofspice use and tem-
perature occur because food-spoilagemicro-
organisms multiplyfasterin hotter climates,
making antimicrobial substances more valu-
able there. But whydon't traditionalrecipes
fromcountrieswithcool climatescall for (po-
tent) spices more often?Certainlysome tropi-
cal spices (e.g., allspice, cinnamon, laos and
cloves) maynot have been readilyavailable in
certaincountrieswhen traditionalrecipeswere
being developed. Nevertheless, most spices
have rather broad distributions (Table 2).
Moreover, lemon and lime trees and pepper
onlygrowin a fractionofthe countrieswe sam-
pled (all tropical), and yet these spices are
used farand wide, including in Scandinavia.
Part of the answermaybe thatusing spices
involvescertain costs: (1) financial costs asso-
ciated withprocuringdried plants thatdo not
growlocally; (2) illnesses caused by ingesting
spices thatare themselvescontaminated with
bacteria or fungi (e.g., due to lengthyor im-
proper storage: Pruthi 1980; Pafumi 1986);
and (3) short-termand long-termphysiologi-
cal costs associated with ingesting plant sec-
ondary compounds and essential oils (Saxe
1987;Johns 1990). Regarding the latter,Beier
and Nigg (1994) comprehensivelyreviewed
the mutagenic,teratogenic,carcinogenic and
allergenic effects of plant secondary com-
pounds, including many spices. In hot cli-
mates,the benefitsofavoidingfood poisoning
and foodborne illnesses apparentlyoutweigh
dangers associated withingestingthese chem-
icals. In cool climates,however,there proba-
blyare fewerindigenous pathogens,and foods
MARCH 1998 ANTIMICROBIAL FUNCTIONS OF SPICES
maydecay slowlyenough thatfurtherretarda-
tion of spoilage may not be worththe associ-
ated health risksof ingestingspices, or the ex-
pense of obtaining them.
Strong-tasting and spicyfoods oftenare un-
acceptable to pregnant women (Profet 1992,
1996), especially during the firsttrimester.
Profetsuggestedthatmorningsicknessimposes
adaptive dietaryrestrictionson the mother.
Women who experience morning sickness
have lowermiscarriageratesthanwomen who
do not (Weigel and Weigel 1989), perhaps be-
cause the formerminimize fetal exposure to
dangerous substances in food, such as plant
secondary compounds. Likewise,young chil-
dren, who are undergoing rapid growthand
are more susceptible than adults to develop-
mental abnormalities,find spicyfoods unac-
ceptable (Rozin 1980; Rozin and Schiller1980).
Perhaps both children and pregnant women
avoid strong (spicy) tastes,even though this
potentiallyexposes them to greater dangers
offood poisoning and foodborne illnesses,be-
cause of the even greaterrisksassociated with
ingesting potentially mutagenic chemicals.
Context-dependent shifts in spice use be-
tweenchildhood and adulthood, and between
pregnancyand nonpregnancy,maythus have
a common, adaptive basis.
Janzen (1978) suggested that animals (in-
cluding humans) consume plants containing
unusual-tastingor foul-tastingand potentially
poisonous compounds as a means of "self-
medication" (reviewed by Clayton and Wolfe
1993). An oftencited example is the ingestion
of the leaves of putativelymedicinal plants by
chimpanzees afflictedby gastrointestinalpar-
asites and other maladies (Huffman and
Wrangham 1994). Virtuallyeveryspice in our
sample has an ethnopharmacological use
among traditionalsocieties,oftenas a topical
or an ingested antimicrobial (e.g., Martinez
1944; Perry1980; Koo 1984; Etkin 1986; Chev-
allier 1996). A few spices, particularlygarlic,
ginger, cinnamon and capsicums, have for
centuries been taken to counteract a broad
spectrum of ailments,including pneumonia,
dysentery, kidneystones,high blood pressure,
wormsand nausea (Beuchat and Golden 1989;
Duke 1994; Cichewiczand Thorpe 1996).
Use of spices in food preparation generally
differsin twowaysfromtheiruse in traditional
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27
medicine, however. In cooking, spices are
added routinely(regardlessof health statusof
consumers) and in relativelytinyquantities,
whereas medicinal uses of spices are occa-
sional (in response to specificmaladies) and
usually in much larger quantities. These dif-
ferences implythat spices are used primarily
to remedychronicproblemsratherthanacute
illnesses. Among chronic problems, spices
might (i) supply necessary micronutrients
(Johnsand Chapman 1995; Milner 1996), (ii)
combat persistententeric infections,or (iii)
kill microorganisms that usually colonize
food. Unfortunately,the micronutritionalval-
ues ofmostspices are unknown.However,pos-
itive correlations between annual tempera-
turesand use of spices (Figures 2, 4, 5 and 7)
and regional differenceswithincountriesare
not predicted by (i), unless for some reason
people in warmer climates require more mi-
cronutrients.Regarding (ii), the rapiditywith
which ingested spice chemicals are catabo-
lized and theireffectson entericinfectionsare
unknown. However, most spices are not in-
gested solely in response to feeling ill, and
spices are routinelyused in food preparation
but not routinelyingested alone (garlic is a
notable exception). Thus, presentlyavailable
data are most consistentwith the hypothesis
(iii) that parasites and pathogens on and in
foodsare theprimarytargetsofspice chemicals.
Although humans are the only creatures
that elaborately prepare their foods, it is an
interesting question whether other species
regularly"spice" theirdietswithsmall quanti-
ties of plant secondarycompounds. Extensive
informationis available on the food habits of
wild mammals,based mainlyon analysesoffe-
ces and stomach contents.Deer (Klimstraand
Dooley 1990; Johnson et al. 1995) and elk
(Sherlock and Fairley 1993) consistentlyin-
gest trace amounts of aromaticplants thatare
foul-tasting or bitter-tasting
to humans. "Vege-
tation"also formsa small but significantfrac-
tion (5-35%) of the diet of most wild carni-
vores, such as red foxes (Cavallini and Volpi
1995; Ferrariand Weber 1995), coyotes (Berg
and Chesness 1978; Parker 1995), bobcats
(Maehr and Brady1986), and cougars (Robin-
ette et al. 1959; Ackerman et al. 1984). Un-
doubtedly some of thisvegetationis ingested
foritsmacronutrients,as when meat is scarce.
28 THE QUARTERLY REVIEW OF BIOLOGY
Nonetheless,frequentingestionofvegetation
is interestingbecause mammalian carnivores,
particularlythose that eat carrion, are so fre-
quentlyexposed to food-spoilagebacteria and
fungi.It would interestingto know ifa coyote
benefitsin the context of inhibitingsuch mi-
croorganismsby nipping a fewsage leaves or
juniper berries.
Our data are relevantto severalalternatives
to the antimicrobial hypothesis.First is the
possibilitythatspices providemacronutrients,
vitaminsor minerals. However, compared to
spices,most common vegetablescontain more
protein,carbohydrates,fat,starch,fiber,min-
erals and a greatervarietyofvitaminsthan do
spices (Tan 1985; Holland et al. 1991). No
"nutritionalfacts"panel even appears on the
labels ofmostcommercialspices in the United
States (exceptions are paprika and chili pow-
der, which contain vitaminA). For these rea-
sons several authorities (e.g., Ensminger et
al.1983; Farrell 1990; Kirschmannand Dunne
1984) have stated thatspices are of littleor no
nutritivevalue, especiallyin the tinyquantities
in which theyare generallyconsumed.
Spices may supply rare micronutrients,
however.Plant secondarycompounds, includ-
ing those found in some spices (particularly
garlic and onions), can have beneficial effects
such as aiding digestion, modulating energy
metabolism,and actingas antioxidants(Johns
1990;Johnsand Chapman 1995). Some phyto-
chemicals also may help postpone degenera-
tivediseases such as diabetes, coronaryheart
disease and cancer (Milner 1996). Whether
the majorityofspices in our sample could pro-
vide thesebenefits,and whetherthequantities
recipes call for supply sufficientmicronutri-
ents to do so, are just beginning to be investi-
gated (Aruoma et al. 1997). Regardless, the
micronutritionhypothesisdoes not predictor
explain the multiple positive correlationswe
found between mean temperaturesand spice
use (Figures 2, 4 and 7), particularlyforcapsa-
icins and otherspices withpowerfulantibacte-
rial properties (Figure 5). Thus, dietarysup-
plementation does not appear to be the sole,
or even the primary,reason forthe popularity
of spices, especiallyin hot climates.
A second hypothesisis thatspices are used
because they disguise the smell or taste of
spoiled foods (Barker 1982; Govindarajan
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VOLUME 73
1985). Our finding that traditional recipes
from hotter countries call for more spices
(Figure 4), especiallypungentspices,is consis-
tentwiththishypothesisbecause therewould
more often be foul smells or bad tastes to
"cover up" owing to rapid spoilage.
The "cover-up"hypothesisignores the po-
tentiallyserious negative consequences of in-
gestingbacteria-laced foods, however.Across
the world,foodborne bacteria (especiallyspe-
cies of Clostridium, Escherichia,
Listeria,Salmo-
nella,Staphylococcus,Streptococcus,
see Evans and
Brachman 1991;Jay1994; Todd 1994,1996) or
theirtoxinsdebilitatemillionsof people annu-
ally and kill thousands. In the United States
alone, foodborne illnessesafflictan estimated
80 million people per year (World Health Re-
port 1996), and one in ten Americans experi-
ences bacteria-related food poisoning annually
(Hui et al. 1994). Moreover,new foodborne
pathogens are continuallyevolving(e.g., Not-
ermans and Hoogenboom-Verdegaad 1992;
Butler 1996). Disguisingtastesassociated with
spoilage or contaminationpotentiallyincreases
exposure to foodborne diseases. Even poorly
nourished individualsmightbe betteroffrec-
ognizing and passing up tainted foods, espe-
cially meat products (Roberts 1990; Sockett
1995), when thereis a chance of ingestingpo-
tentiallydeadly quantities of microorganisms
or theirtoxins.It mayeven be thatthe advan-
tages of recognizing and avoiding spoiled or
contaminated foods explain the sensitivity of
our olfactoryand gustatorysystemsto smells
and tastesof decay. Thus, froman evolution-
ary perspective,the "cover-up" hypothesisis
seriouslyflawed.
A thirdalternativehypothesisis that spicy
foodsare preferredin hotclimatesbecause they
help cool the body evaporatively by increasing
perspiration(see Rozin and Schiller1980; Bos-
land 1994). Capsicums can produce hypother-
mia, either througha gustofacialsweatingre-
flex or direct action on the hypothalamus
(Rozin and Schiller 1980). However, most
spices whose use increases withmean temper-
atures (e.g., garlic, onion, anise, cinnamon,
coriander, ginger, lemongrass) do not pro-
duce hypothermia,and even chilies do not in-
crease perspiration in many people (Rozin
and Schiller 1980). Moreover, sweating is a
metabolicallyexpensivewayto cool off,and it
MARCH 1998 ANTIMICROBIAL FUNCTIONS OF SPICES
requires abundant water to sustain it. In the
contextofthe spice-usepatternswe have iden-
tified,the evaporativecooling hypothesiscan-
not be a general explanation.
A final possibilityis that spices confer no
benefits,and that people simplyuse which-
ever aromatic plants are at hand to improve
the tasteof food. Harris (1985:15), Nesse and
Williams (1994:147-151), and Letarte et al.
(1997) discussed how human taste receptors
and gustatorypreferenceshave been shaped
by nutritional benefits normally associated
with favored flavors.Potentiallyedible items
are expected to be tastyiftheirchemical con-
stituentsmatchcloselyenough those normally
found in nutritiousfoods. This "null"hypothe-
sis predicts that spice chemicals should be
highlypalatable, and that spice-use patterns
should correspond closelyto naturalranges of
spice plants.
Neither prediction is supported. First,fla-
vorsof manywidelyused spices are not imme-
diatelyappealing. Indeed, pungent spices like
garlic, ginger, onion, anise, turmeric and
black pepper initiallyare unappealing to most
people, especially to children (Rozin 1980),
and the capsaicin in hot chili peppers causes
painful sensations (Caterina et al. 1997). For
most disagreeable substances,an initialnega-
tive response is sufficientto maintain avoid-
ance throughout an individual's life. How-
ever,preferencesforspices develop withage,
usually under familial guidance (Rozin and
Schiller 1980). The fact that parents encour-
age theirchildren to eat (displeasing) spices,
and thatchildrencome to preferthembyado-
lescence, stronglysuggeststhatusing spices is
somehow beneficial.
Second, people do not use everyspice that
grows in their country (Figure 11), but they
do use many spices that must be imported
(Figure 12), and for centuries have gone to
greatlengthsto obtain them (e.g., Govindara-
jan 1985). An extreme example is pepper,
whichis one ofthemostfrequentlyused spices
in all 36 countrieswe sampled (Figure 1), but
which growsin only nine of them (Table 2).
Pepper is the most frequentlyimported spice
into the United Statestoday (about 87 million
pounds in 1991: Tainter and Grenis 1993).
Althoughlocal availabilityis not a sufficient
explanation, it certainlyaffectsspice-use pat-
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29
ternsbecause proportionsof recipes thatcall
formost spices are higher in countrieswhere
those spices grow.Moreover,recipes of hotter
countries call for greater fractionsof locally
available spice plants,as indicated bythe posi-
tive correlation between temperatures and
proportionsof spices used in the countriesin
which theygrow. However, since there is no
relationship between mean annual tempera-
turesand numbers of spices thatgrowin each
country(Figure 10), the multiplepositivecor-
relationsbetween temperaturesand frequen-
cies of spice use (Figures 2, 4, 5 and 7) are not
simplyowing to greaterspice plant availability
in hotter countries. In sum, local availability
of a spice plant does not necessarilymean that
residentswilluse it,and lack of local availabil-
itydoes not mean thatresidentswillnot use it.
Rozin (1982) hypothesized that humans
seek varietyin foods to ensure thattheyobtain
a nutritionallybalanced diet. It is well estab-
lished that the perceived diversityof foods
consumed positivelyinfluences the amount
consumed (Rozin and Vollmecke 1986). Ac-
cording to Rozin, we habituate to commonly
eaten foods (the "sensory-specificsatietyef-
fect") because our taste preferences,which
ensure thatwepursue variety,evolvedat a time
when dietswere chemicallymore diversethan
theyare today.If so, spice use mayfunctionto
"trick"our internal mechanisms; by seeming
to provide dietaryvariety,spices encourage
consumption of greaterquantities of (bland)
foods. This hypothesisis intriguing,but itdoes
not predict or explain patterns of spice use
demonstrated here, especially relationships
with temperature (unless for some reason
people in hot climatesmore frequentlyexpe-
rience dietarydeficienciesdue to sensory-spe-
cificsatiety).
How do people know what spices to use?
We can envisiontwopossibilities.First,people
who happened to add spice plantsto meat dur-
ing preparation, especially in hot climates,
may have been less likelyto sufferfromfood
poisoning or foodborne illnesses than those
who did not. Spice users also may have been
able to storefoods longer before theyspoiled,
enabling them to tolerate longer periods of
scarcity. Observation and imitation of the
eating habits of these healthier individualsby
otherscould spread spice use rapidlythrough
30 THE QUARTERLY REVIEW OF BIOLOGY
a society.Also, familiesthatused appropriate
spices would rear more healthyoffspring,to
whom spice-use traditionshad been taught
and who possessed appropriatetastereceptors.
These children would pass to their progeny
both the "memes" (Dawkins 1976) for using
particularspices and the receptor physiology
for tastingthem (e.g., Caterina et al. 1997);
individualdifferencesin receptorsensitivity to
spices are discussed by Drewnowskiand Rock
(1995) and Tepper and Nurse (1997).
A second possibilityinvolveslearned taste
aversions. When people eat something that
makes them ill, theytend to avoid that taste
subsequently (Milgram et al. 1977; Pelchat
and Rozin 1982). The adaptive value of such
learning is obvious (Letarte et al. 1997). Add-
ing a spice to a food thatcaused nausea might
alter its taste enough to make it palatable
again (i.e., it tastes like a differentfood), as
well as killthe microorganismsthatcaused the
illness, thus rendering it safe for consump-
tion. By this process, food aversions would
more oftenbe associated withunspiced (and
unsafe) foods,and food likingswould be asso-
ciated with spicy foods, especially in places
wherefoods spoil rapidly.Over time,the habit
of spicing foods and use of multiple spices in
each recipe could become prevalentowing to
the iteration of this process (i.e., sequential
changes in spices and tastesfor them, associ-
ated withinhibitionof differentbacteria and
fungi).
Of course, spice use is not the only way to
avoid food poisoning and foodborne patho-
gens. Cooking and completelyconsumingwild
game immediatelyafterslaughterreduces op-
portunitiesformicroorganismalgrowth.How-
ever,thisis practical onlywhere freshmeat is
abundant year-round(e.g., Ache hunter-gath-
erers in Paraguay: Hill et al. 1984). In areas
where freshmeat is not consistentlyavailable,
preservation may be accomplished by thor-
oughlycooking, salting,smoking,drying,and
spicing meats. Indeed, salt has been used
worldwidefor centuries to preservefood (Al-
ford and Palumbo 1969; Helmy et al. 1985).
We hypothesize that all these practices have
been adopted foressentiallythe same reason:
to minimize effectsof foodborne pathogens.
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VOLUME 73
Our correlational or "forwardapproach"
(Sherman and Reeve 1997) analyses of spice
use would be usefullycomplemented by ex-
perimentalstudies of how the use of different
spices and spice combinations affectsindivid-
ual fitnessin differentcountries and cultures
(i.e., the "backward approach"). A decisive
testof the antimicrobialhypothesiswould in-
volve quantifyingthe frequencyof foodborne
illnesses, and the survivaland reproductive
successes ofindividualslivingin the same geo-
graphic area and eating essentiallythe same
foods,but using differentspices and combina-
tions of them.
In sum, we believe that the probable ulti-
mate reason whyhumans spice foods is to take
advantage of the antimicrobialactions of the
plant secondary compounds that give spices
their flavors.We hypothesize that,by cleans-
ing foods of pathogens,spice users contribute
to their health, survival and reproduction.
These then maybe the reasons whymanypeo-
ple, especially those living in or visitinghot
climates,preferfood thatis spicy.
ACKNOWLEDGMENTS
For helpfulcommentsduringthecourseofthis
researchwe thankthe Animal BehaviorLunch
Bunch at CornellUniversity PeterS
(particularly
Buston,HamiltonE Farris, JohnM Peters,H Kern
Reeve and PhilipT Starks),the MuseumLunch
Bunchat theUniversity of Michigan(particularly
RichardD Alexander,John Cooley,DavidMarshall
and CynthiaSimmsParr),and ThomasA Gavin,
GavinB Grant,Bobbi S Low, RichardD Howard
and Deedra K McClearn.Forassistancewithrefer-
enceswethanktheCornellUniversity Food Science
and Nutrition Department, theCornellCollegeof
HumanEcologyand theDivisionofNutritional Sci-
enceStatisticalConsultingService,theCornellUni-
versityOlin Library Loan Department,
Interlibrary
and theCirculation andReference staffatCornell's
Mannand Nest1lLibraries.Forcommentson pre-
liminaryversionsofthemanuscriptwethankThomas
Eisner,ThomasA Gavin,ThomasNeuhaus,Frank
A Pitelka,H KernReeve,LaurelSouthardand Bev-
erlyI Strassmann. Duringtheresearch, JBwaspar-
tiallysupportedbya HowardHughesSummerFel-
lowshipadministeredby Cornell University and
PWSwassupportedbygrantsfromtheNationalSci-
ence Foundationand CornellUniversity.
MARCH 1998 ANTIMICROBIAL FUNCTIONS OF SPICES 31

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MARCH 1998 ANTIMICROBIAL FUNCTIONS OF SPICES 39

APPENDIX A
Bacterialspecieskilledor inhibitedin growthbyeach spice(n=30)
Spice Bacteria Inhibited
Allspice Bacillus subtilis
Clostradium botulinum
Escherichiacoli
Listeriamonocytogenes
Serratramarcescens
Anise Aerobacter
aerogenes
Aeromonashydrophila
Flavobacteriumsuaveolens
Leuconostoccremoras
albus
Staphylococcus
naszk
Streptococcus
Basil Acinetobactercalcoaceticus
Alcaligenesfaecalis
Beneckeanatriegens
Cztrobacterfreundii
Enterobacteraerogenes
Erwinia carotovora
Flavobacterium suaveolens
Klebsiellapneumoniae
Leuconostoccremorns
Pseudomonasaeruganosa
Salmonellapullorum
Serratzamarcescens
Bay Leaves Acinetobactercalcoaceticus
Aeromonashydrophzla
Alcaligenesfaecalis
Baczllussubtzlis
Beneckeanatriegens
Brocothrax thermosphacta
Citrobacterfteundii
Clostridium botulznum
Enterobacteraerogenes
Erwznzacarotovora
Escherichzacolz
Flavobacteraum suaveolens
Klebsiellapneumoniae
Lactobacillusplantarum
Leuconostoccremoris
Proteusvulgaras
Pseudomonasaeruginosa
Salmonellapullorum
Serratiamarcescens
Staphylococcusaureus
Staphylococcusfaecalzs
Vibraoparahaemolytzcus
Yersiniaenterocolztzca
Bacteria Not Inhibited References
None Hargreaves et al. 1975
Hefnawyet al. 1993
Huhtanen 1980
Shelef et al. 1980
Alcalagenes
faecalis Azzouz and Bullerman 1982
Brevibacteraum linens Deans and Ritchie 1987
Catrobacterfreundii Hargreaves et al. 1975
Clostridiumbotulinum Huhtanen 1980
Clostridiumsporogenes Kivanc and Akgul 1986
Erwinia carotovora Ramadan et al. 1972
Lactobacillusplantarum
Mzcrococcus luteus
Staphylococcusfaecalis
Streptococcus
faecalzs
Yersiniaenterocolztica
Aeromonashydrophzla Deans and Ritchie 1987
Bacillus subtilus
Brevabacterium lznens
Brocothrix thermosphacta
Clostradzum sporogenes
Eschernchia coli
Lactobaczllusplantarum
Micrococcusluteus
Proteusvulgaris
Staphylococcus aureus
Streptococcusfaecalis
Yersiniaenterocolitica
Brevzbacteriumlznens Aktug and Karapinar 1986
Clostradiumsporogenes Beuchat 1994
Micrococcusluteus Deans and Ritchie 1987
Salmonellatyphimurium Hargreaves et al. 1975
Streptococcus
faecalis Huhtanen 1980

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40 THE QUARTERLY REVIEW OF BIOLOGY
APPENDIX
Spice Bacteria Inhibited
Capsicums Baczllus cereus
(Chilies) Baczllus subtilzs
Sarczna lutea
Staphylococcus aureus
Caraway Acznetobacter calcoaceticus
Aeromonas hydrophzla
Alcalzgenes faecalis
Beneckea natnegens
Brocothrix thermosphacta
Cztrobacterfreundzz
Enterobacter aerogenes
ErYwznzacarotovora
Flavobacteraum suaveolens
Klebsiella pneumonzae
Leuconostoc cremoras
Mycobacteraumphlei
Proteus morganzz
Proteus vulgaras
Pseudomonas fluorescens
Salmonella enteritzdzs
Salmonella pullorum
Serratza marcescens
Staphylococcus aureus
Cardamom Aeromonas hydrophzla
Baczllus anthraczs
Bacillus cereus
Brocothrax thermosphacta
Flavobacteraum suaveolens
Lactobaczllus bulgaricus
Leuconostoc cremoras
Mzcrococcus (Sarczna)
Pseudomonas fluorescens
Pseudomonas pyocyanea
Salmonella paratyphz
Serratia rhadnii
Streptococcus thermophzlus
Celery Seed Aerobacter aerogenes
Baczllus subtzlzs
Brocothnx thermosphacta
Clostradzum botulznum
Flavobacteraum suaveolens
Leuconostoc cremoris
Staphylococcus albus
Staphylococcus aureus
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VOLUME 73
A continuation
Bacteria Not Inhibited References
Lzsterza monocytogenes Evert Ting and Deibel 1992
Hargreaves et al. 1975
Hefnawy et al. 1993
Kim and Ryeom 1979
Brevzbacteraum lznens Deans and Ritchie 1987
Clostndzum botulznum Farag et al. 1989
Clostradium sporogenes Hargreaves et al. 1975
Lactobaczllus plantarum Huhtanen 1980
Micrococcus luteus Ramadan et al. 1972
Staphylococcus faecalzs
Streptococcusfaecalzs
Yersznza enterocolztzca
Aczneto.bacter calcoacetzcus Azzouz and Bullerman 1982
Alcalzgenes faecalis Bayoumi 1992
Beneckea natraegens Deans and Ritchie 1987
Brevzbacteraum lznens El-Kady et al. 1993
Cztrobacterfteundzi Islam et al. 1990
Clostradium sporogenes Kubo et al. 1991
Erwznza carotovora
Lactobaczllus plantarum
Micrococcus luteus
Salmonella pullorum
Serratza marcescens
Streptococcusfaecalzs
Streptococcus nasik
Yersznza enterocolitzca
Acinetobacter calcoaceticus Deans and Ritchie 1987
Aeromonas hydrophila Huhtanen 1980
Alcalzgenes faecalis Kivanc and Akgul 1986
Baczllus cereus Ramadan et al. 1972
Beneckea natraegens
Brevzbacterium lznens
Cztrobacterfreundzz
Clostradzum sporogenes
Enterobacter aerogenes
ErYwinzacarotovora
Klebszella pneumonzae
Lactobaczllus plantarum
Mzcrococcus luteus
Salmonella pullorum
Serratza marcescens
Staphylococcus faecalzs
Streptococcusfaecalzs
Yersznia enterocolztzca
MARCH 1998 ANTIMICROBIAL FUNCTIONS OF SPICES 41

APPENDIX A continuation
Spice Bacteria Inhibited Bacteria Not Inhibited References
Cinnamon Acznetobacter calcoacetzcus Clostradzum
sporogenes Azzouz and Bullerman 1982
Aeromonashydrophzla Enterobacter
aerogenes Bayoumi 1992
Alcalzgenesfaecalzs Pseudomonasaeruginosa Beuchat 1994
Baczllus anthraczs Streptococcus
faecalzs Deans and Ritchie 1987
Baczllus cereus El-Kady et al. 1993
Bacillus subtzlzs Evert Ting and Deibel 1992
Beneckeanatraegens Hargreaves et al. 1975
Brevzbacterium lznens Huhtanen 1980
Brocothrax thermosphacta Islam et al. 1990
Cztrobacterfreundzz Ismaiel and Pierson 1990a
Erwzvnza carotovora Shelef et al. 1984
Eschernchza colz Zaika 1988
Flavobacteraum suaveolens
Lactobaczllusbulgaracus
Lactobaczllusplantarum
Leuconostoccremoris
Lzsterzamonocytogenes
Mzcrococcus luteus
Proteusvulgaras
Pseudomonasfluorescens
Pseudomonaspyocyanea
Salmonellaparatyphz
Salmonellapullorum
Serratzamarcescens
Serratzarhadnzz
Staphylococcus aureus
Streptococcus nasik
Streptococcus thermophzlus
Yersznzaenterocolztzca
Cloves Acznetobactercalcoacetzcus Clostradzumsporogenes Azzouz and Bullerman 1982
Aeromonashydrophzla Mzcrococcus(Sarczna) Bayoumi 1992
Baczllus anthracis Pseudomonaspyocyanea Beuchat 1994
Bacillus cereus Salmonellaparatyphz Briozzo et al. 1989
Bacillus subtzlzs Serratzarhadnzi Deans and Ritchie 1987
Beneckeanatraegens El-Kady et al. 1993
Cztrobacterfreundiz Evert Ting and Deibel 1992
Clostradzum botulinum Farag et al. 1989
Clostradium perfrangens Hargreaves et al. 1975
Enterobacteraerogenes Huhtanen 1980
Erwzvnza carotovora Ismaiel and Pierson 1990a
Escherichzacolz Jayand Rivers 1984
Flavobacteraum suaveolens Ramadan et al. 1972
Klebszellapneumonzae Shelef et al. 1984
Lactobacillusbulgaracus Stecchini et al. 1993
Lactobacillusplantarum Zaika 1988
Leuconostoccremoras
Listertamonocytogenes
Mzcrococcus luteus
Mycobacteraum phlei
Proteusmorganzz
Proteusvulgaras
Pseudomonasaerugznosa
Pseudomonasfluorescens
Salmonellaenterntzdzs

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42 THE QUARTERLY REVIEW OF BIOLOGY
APPENDIX
Spice Bacteria Inhibited
Cloves Salmonella pullorum
(contznuatzon) Serratza marcescens
Staphylococcus aureus
Streptococcusfaecalis
Streptococcus naszk
Streptococcus thermophzlus
Yersznza enterocolztica
Coriander Aerobacter aerogenes
Aeromonas hydrophzla
Bacillus subtzlis
Brocothrix thermosphacta
Cztrobacterfreundii
Enterobacter aerogenes
Erwinia carotovora
Escherichza colz
Flavobacteraum suaveolens
Klebszella pneumoniae
Lactobacillus plantarum
Leuconostoc cremoris
Staphylococcus albus
Staphylococcus aureus
Cumin Aerobacter aerogenes
Baczllus anthraczs
Baczllus cereus
Baczllus coagulans
Bacillus subtilzs
Clostridzum botulznum
Enterobacter aerogenes
Lactobaczllus plantarum
Leuconostoc mesenteroides
Listeria monocytogenes
Micrococcus (Sarczna)
Proteus vulgaris
Pseudomonas aeruginosa
Pseudomonas fluorescens
Salmonella enterntidzs
Salmonella paratyphz
Serratia marcescens
Staphylococcus albus
Staphylococcus aureus
Streptococcusfaecalis
Streptococcus nasik
Dill Acznetobactercalcoaceticus
Aerobacter aerogenes
Aeromonas hydrophila
Brevzbacterium lznens
Cztrobacterfreundii
Enterobacter aerogenes
ErYwznzacarotovora
Flavobacteraum suaveolens
Klebszella pneumoniae
Proteus vulgaris
Pseudomonas aerugznosa
Serratia marcescens
Staphylococcus albus
Staphylococcus aureus
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VOLUME 73
A continuation
Bacteria Not Inhibited References
Acinetobacter calcoacetzcus Deans and Ritchie 1987
Alcaligenesfaecalzs Hargreaves et al. 1975
Beneckea natraegens Huhtanen 1980
Brevibacteraum lznens Kivanc and Akgul 1986
Clostradium sporogenes Stecchini et al. 1993
Micrococcus luteus
Proteus vulgaras
Salmonella pullorum
Serratia marcescens
Staphylococcus faecalzs
Streptococcusfaecalis
Yersinia enterocolitzca
Klebszella pneumonzae Azzouz and Bullerman 1982
Pseudomonas pyocyanea El-Kady et al. 1993
Serratza rhadnzz Farag et al. 1989
Hassan et al. 1989
Hefnawy et al. 1993
Huhtanen 1980
Kivanc and Akgul 1986
Kivanc et al. 1991
Ramadan et al. 1972
Saxena and Vyas 1986
Shetty et al. 1994
Alcalzgenes faecalis Deans and Ritchie 1987
Beneckea natraegens Hargreaves et al. 1975
Brocothrix thermosphacta Huhtanen 1980
Clostridaum botulznum Kivanc and Akgul 1986
Clostradium sporogenes Ramadan et al. 1972
Lactobacillus plantarum
Leuconostoc cremoris
Micrococcus luteus
Salmonella pullorum
Staphylococcus faecalis
Streptococcusfaecalis
Yersznza enterocolitica
MARCH 1998 ANTIMICROBIAL FUNCTIONS OF SPICES
APPENDIX
Spice Bacteria Inhibited
Fennel Aerobacter aerogenes
Bacillus cereus
Baczllussubtzlzs
Citrobacterfreundzz
Enterobacter aerogenes
ErYwznza carotovora
Flavobacteraum suaveolens
Leuconostoccremoris
Proteusvulgaras
Salmonellaenteritidis
Salmonellapullorum
Serratzamarcescens
Staphylococcus albus
Staphylococcus aureus
Garlic Baczllus cereus
Baczllussubtzlzs
Campylobacterjejuni
Clostridzum perfrangens
Enterobacter cloacae
Enterococcus faecalzs
Enterococcus faeczum
Eschernchza colz
Klebsiellaaerogenes
Klebszellapneumonzae
Lactobacillusaczdophzlus
Lactobaczllusplantarum
Listermamonocytogenes
Pediococcuspentosaceus
Proteusmirabilzs
Proteusmorganzz
Proteusvulgaras
Pseudomonasaeruginosa
Pseudomonasfluorescens
Salmonelladublin
Salmonellaenterntzdzs
Salmonellatyphzmuraum
Serratzamarcescens
Staphylococcus aureus
Staphylococcus epidermzdzs
Streptococcus agalactiae
Vzbriomimicus
Vzbraoparahaemolytzcus
Yersiniaenterocolitica
Ginger Baczllus anthracis
Bacillus subtzlzs
Brocothrix thermosphacta
Flavobacteraum suaveolens
Leuconostoccremoris
Proteusmzrabilis
Salmonellatyphzmurium
Staphylococcusepzdermzdzs
Staphylococcushaemolytzcus
Streptococcusvzridans
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A continuation
Bacteria Not Inhibited
Alcaligenesfaecalis
Beneckeanatriegens
Brevibacterium lznens
Brocothrix thermosphacta
Clostridium botulinum
Clostridium sporogenes
Klebsiellapneumoniae
Lactobaczllusplantarum
Mzcrococcusluteus
Staphylococcusfaecalzs
Yersznzaenterocolitzca
None
Acznetobactercalcoacetzcus
Aeromonashydrophila
Alcalzgenesfaecalis
Beneckeanatriegens
Brevibacterium linens
Cztrobacterfreundzz
Clostradium sporogenes
Enterobacteraerogenes
Erwznzacarotovora
Klebszellapneumoniae
43
References
Deans and Ritchie 1987
Hargreaves et al. 1975
Huhtanen 1980
Kivanc and Akgul 1986
Ramadan et al. 1972
Abdou et al. 1972
Beuchat 1994
El-Khateib and El-Rahman 1987
Evert Ting and Deibel 1992
Gandi and Ghodekar 1988
Hargreaves et al. 1975
Hefnawyet al. 1993
Hughes and Lawson 1991
Huhtanen 1980
Ismaiel and Pierson 1990b
Rees et al. 1993
Sato et al. 1990
Shelef 1984
Azzouz and Bullerman 1982
Deans and Ritchie 1987
Gugnani and Ezenwanze 1985
Huhtanen 1980
Mascolo et al. 1989
44 THE QUARTERLY REVIEW OF BIOLOGY
APPENDIX
Spice Bacteria Inhibited
Ginger
(contznuatzon)
Lemon Aerobacter aerogenes
Baczllus subtzlzs
Brocothrax thermosphacta
Flavobacteraum suaveolens
Leuconostoccremoras
Staphylococcus albus
Staphylococcus aureus
Lemongrass Baczllus cereus
Baczllussubtzlis
colz
Eschernchia
Pseudomonasaerugznosa
Salmonellaenteritzdis
Staphylococcusaureus
Lime Aeromonashydrophila
Brocothraxthermosphacta
Flavobacteraumsuaveolens
Leuconostoccremoras
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VOLUME 73
A continuation
Bacteria Not Inhibited References
Lactobaczllusplantarum
Mzcrococcusluteus
Pseudomonasaerugznosa
Salmonellapullorum
Serratzamarcescens
Streptococcus
faecalzs
naszk
Streptococcus
Yersznzaenterocolztzca
Aeromonashydrophzla Deans and Ritchie 1987
Alcalzgenesfaecalzs Kivanc and Akgul 1986
Beneckeanatraegens
Brevibacteraum lznens
Cztrobacterfreundzz
Clostradzum sporogenes
Enterobacteraerogenes
Erwzvniacarotovora
Klebszellapneumonzae
Lactobaczllusplantarum
Mzcrococcusluteus
Salmonellapullorum
Serratiamarcescens
Staphylococcusfaecalzs
Streptococcusfaecalzs
Yersznzaenterocolztzca
Streptococcusfaecalzs Onawunmi and Ogunlana 1986
Ramadan 1972
Acinetobactercalcoacetzcus Deans and Ritchie 1987
Alcalzgenesfaecalzs Kivanc and Akgul 1986
Baczllussubtzlzs
Beneckeanatraegens
Brevzbacteraum lznens
Cztrobacterfreundzz
Clostradium sporogenes
Enterobacteraerogenes
Ervinza carotovora
Escherichzacoli
Klebsaellapneumoniae
Lactobaczllusplantarum
Mzcrococcus luteus
Proteusvulgaris
Pseudomonasaerugznosa
Salmonellapullorum
Serratzamarcescens
Staphylococcusfaecalzs
Streptococcusfaecalzs
Yerszniaenterocolztzca
MARCH 1998 ANTIMICROBIAL FUNCTIONS OF SPICES 45

APPENDIX A continuation
Spice BacteriaInhibited BacteriaNot Inhibited References
Majoram Acznetobacter calcoacetzcus Clostradzum sporogenes Deans and Ritchie 1987
Aeromonas hydrophzla Lactobaczllus plantarum El-Kady et al. 1993
Alcalzgenes faecalzs Leuconostoc cremoras Hargreaves et al. 1975
Baczllus anthraczs Mzcrococcus luteus Ramadan 1972
Baczllus cereus Pseudomonas aerugznosa
Baczllus subtzlzs Salmonella paratyphi
Beneckea natraegens Serratza rhadnzz
Brevzbacteraumlznens Yersznza enterocolztzca
Brocothraxthermosphacta
Cztrobacterfreundzz
Enterobacter aerogenes
Erwzvnzacarotovora
Eschernchza colz
Flavobacteraum suaveolens
Klebszella pneumonzae
Mzcrococcus (Sarczna)
Proteus vulgaras
Pseudomonas fluorescens
Pseudomonas pyocyanea
Salmonella enterntzdzs
Salmonella pullorum
Serratza marcescens
Staphylococcus aureus
Streptococcusfaecalzs

Mint Acznetobacter calcoacetzcus Alcalzgenes faecalzs Aktug and Karapinar 1986

Aeromonas hydrophila Brevzbacteraum lznens Bayoumi 1992
Baczllus subtzlzs Erwznza carotovora Beuchat 1994
Beneckea natraegens Flavobacterium suaveolens Deans and Ritchie 1987
Brocothrax thermosphacta Lactobaczllus bulgaracus El-Kady et al. 1993
Cztrobacterfreundzz Leuconostoc cremoras
Clostradzum sporogenes Mzcrococcus luteus
Enterobacter aerogenes Salmonella typhzmuraum
Eschernchia colz Staphylococcus aureus
Klebszella pneumonzae Streptococcus thermophzlus
Lactobaczllus plantarum
Proteus vulgaras
Pseudomonas aerugznosa
Salmonella pullorum
Serratza marcescens
Streptococcusfaecalis
Yersznza enterocolztzca

Mustard Eschernchza colz Clostridzum botulinum Azzouz and Bullerman 1982

Proteus vulgaras Lzsterza monocytogenes Evert Ting and Deibel 1992
Pseudomonas aerugznosa Hargreaves et al. 1975
Pseudomonas fraga Huhtanen 1980
Staphylococcus aureus Kanemaru and Miyamoto 1990
Streptococcus naszk

Nutmeg Aeromonas hydrophzla Acznetobactercalcoacetzcus Deans and Ritchie 1987

Baczllus subtzlzs Alcalzgenes faecalzs Evert Ting and Deibel 1992
Brevzbacteraum lznens Beneckea natraegens Hargreaves et al. 1975
Brocothrax thermosphacta Clostradzum sporogenes Hefnawy et al. 1993
Cztrobacterfreundzz Enterobacter aerogenes Huhtanen 1980
Clostradzum botulznum Klebszella pneumonzae Stecchini et al. 1993

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46 THE QUARTERLY REVIEW OF BIOLOGY
APPENDIX
Spice Bacteria Inhibited
Nutmeg Ervinza carotovora
(contznuatzon) Escherichzacolz
Flavobacterium suaveolens
Leuconostoccremoras
Listertamonocytogenes
Proteusvulgaras
Serratzamarcescens
Yerszniaenterocolztica
Onion Escherichiacoli
Salmonellatyphzmuraum
Shigelladysenterzae
Staphylococcusaureus
Oregano Aerobacter aerogenes
Bacillus subtilzs
Clostridzum botulznum
Eschernchia colz
Lactobaczllusplantarum
Leuconostocmesenteroides
Lzsteriamonocytogenes
Proteusvulgaras
Pseudomonasaeruginosa
Staphylococcus albus
Staphylococcus aureus
Parsley Acinetobacter calcoaceticus
Aerobacter aerogenes
Beneckeanatraegens
Citrobacterfreundzi
Enterobacter aerogenes
Flavobacteraum suaveolens
Klebszellapneumonzae
Salmonellapullorum
Serratiamarcescens
Staphylococcus albus
Staphylococcus aureus
Streptococcusfaecalzs
Pepper Aeromonashydrophila
Bacillus subtilis
Brocothrix thermosphacta
Clostradium botulinum
Ervinza carotovora
Flavobacteraum suaveolens
Lactobacillusmicrococcus
Leuconostoccremoras
Streptococcusnaszk
Yersinzaenterocolitica
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VOLUME 73
A continuation
Bacteria Not Inhibited References
Lactobacillusplantarum
Micrococcusluteus
Pseudomonasaeruginosa
Salmonellapullorum
Staphylococcusaureus
Streptococcus
faecalzs
None Abdou et al. 1972
Beuchat 1994
Hargreaves et al. 1975
Hughes and Lawson 1991
Huhtanen 1980
Shelef 1984
None Beuchat 1994
Evert Ting and Deibel 1992
Huhtanen 1980
Ismaiel and Pierson 1990a,b
Kivanc and Akgul 1986
Kivanc et al. 1991
Shelef 1984
Aeromonashydrophila Deans and Ritchie 1987
Alcaligenesfaecalis Evert Ting and Deibel 1992
Brevibacterium lznens Kivanc and Akgul 1986
Brocothraxthermosphacta Huhtanen 1980
Clostradium botulinum
Clostridium sporogenes
Erwzniacarotovora
Lactobacillusplantarum
Leuconostoccremoris
Listeriamonocytogenes
Micrococcusluteus
Yersinzaenterocolitzca
Acinetobactercalcoaceticus Abdou et al. 1972
Alcalzgenesfaecalzs Azzouz and Bullerman 1982
Beneckeanatraegens Deans and Ritchie 1987
Brevibacterium linens Evert Ting and Deibel 1992
Cztrobacterfreundzi Hefnawy et al. 1993
Clostridzum sporogenes Huhtanen 1980
Enterobacteraerogenes Islam et al. 1990
Klebszellapneumoniae Shelef 1984
Lactobaczllusplantarum Stecchini et al. 1993
Micrococcusluteus
Proteusvulgaras
Pseudomonasaeruginosa
Salmonellapullorum
Serratzamarcescens
Staphylococcusfaecalis
Streptococcusfaecalzs
MARCH 1998 ANTIMICROBIAL FUNCTIONS OF SPICES 47

APPENDIX A continuation
Spice Bacteria Inhibited Bacteria Not Inhibited References
Rosemary Acinetobacter calcoacetzcus Alcalzgenes
faecalzs Beuchat 1994
Aerobacter aerogenes Brevzbacteraum linens Deans and Ritchie 1987
Aeromonashydrophila Brocothraxthermosphacta El-Kady et al. 1993
Baczllus anthraczs Erwzniacarotovora Evert Ting and Deibel 1992
Bacillus cereus Lactobaczllusplantarum Farag et al. 1989
Baczllus megaterium Leuconostoccremoras Farbrood et al. 1976
Bacillus subtzlzs Micrococcusluteus Hargreaves et al. 1975
Beneckeanatraegens Yersznzaenterocolitica Huhtanen 1980
Cztrobacterfreundii Kivanc and Akgul 1986
Clostradzum botulinum Shelef 1984
Clostradzum sporogenes Shelef et al. 1980
Flavobacteraum suaveolens
Klebszellapneumonzae
Lzsterzamonocytogenes
Micrococcus(Sarczna)
Mycobacterium phlez
Proteusvulgaras
Pseudomonasfluorescens
Pseudomonaspyocyanea
Salmonellaparatyphz
Salmonellapullorum
Salmonellatyphimuraum
Serratzamarcescens
Serratzarhadnzz
Staphylococcus albus
Staphylococcus aureus
Staphylococcus epzdermidzs
Vibraoparahaemolytzcus
Sage Aerobacter aerogenes Acznetobactercalcoacetzcus Azzouzand Bullerman 1982
Baczllus cereus Aeromonashydrophila Beuchat 1994
Bacillus megateraum Alcaligenesfaecalis Deans and Ritchie 1987
Bacillus subtzlzs Brevzbacterium lznens Evert Ting and Deibel 1992
Beneckeanatriegens Brocothrax thermosphacta Farag et al. 1989
Clostradzum botulznum Citrobacterfreundzz Hargreaves et al. 1975
Enterobacter aerogenes Clostradzum sporogenes Hefnawyet al. 1993
Flavobacterium suaveolens Erwinzacarotovora Huhtanen 1980
Lzsteriamonocytogenes Klebsiellapneumonzae Kivanc and Akgul 1986
Mycobacterium phlez Lactobaczllusplantarum Shelef et al. 1980
Pseudomonasfluorescens Leuconostoccremoris Shelef 1984
Staphylococcus aureus Mzcrococcus luteus
Staphylococcus epidermzdzs Yersznzaenterocolztzca
Salmonellapullorum
Salmonellatyphzmurium
Serratzamarcescens
Staphylococcus albus
Streptococcus nasik
Vzbrioparahaemolyticus
Tarragon Aerobacter aerogenes botulznum
Clostradzum Huhtanen 1980
Baczllus subtzlzs Kivanc and Akgul 1986
Escherichzacoli
Proteusvulgaras
Pseudomonasaerugznosa
Staphylococcus aureus
Staphylococcus albus

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48 THE QUARTERLY REVIEW OF BIOLOGY VOLUME 73

APPENDIX A continuation
Spice Bacteria Inhibited Bacteria Not Inhibited References
Thyme Acinetobacter calcoacetzcus Clostradzum
sporogenes Aktug and Karapinar 1986
Aerobacter aerogenes Leuconostoccremoris Arras and Grella 1992
Aeromonashydrophzla Pseudomonaspyocyanea Azzouz and Bullerman 1982
Alcalzgenesfaecalis Beuchat 1994
Bacillus anthracis Deans and Ritchie 1987
Bacillus cereus El-Kady et al. 1993
Baczllus subtilzs Farag et al. 1989
Beneckeanatriegens Huhtanen 1980
Brevzbacterium lznens Ismaiel and Pierson 1990a
Brocothrax thermosphacta Kivanc and Akgul 1986
Cztrobacterfreundzz Shelef 1984
Enterobacter aerogenes
Ervinia carotovora
Eschernchia coli
Flavobacteraum suaveolens
Klebszellapneumoniae
Lactobaczllusplantarum
Mzcrococcus(Sarczna)
Mzcrococcusluteus
Mycobacteraum phlez
Proteusvulgaris
Pseudomonasaeruganosa
Pseudomonasfluorescens
Salmonellaparatyphz
Salmonellapullorum
Salmonellatyphzmuraum
Serratzamarcescens
Serratzarhadnzz
Staphylococcus albus
Staphylococcus aureus
Staphylococcus faecalzs
Streptococcusfaecalzs
Streptococcus naszk
Vibraoparahaemolytzcus
Yersznzaenterocolztzca

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MARCH 1998 ANTIMICROBIAL FUNCTIONS OF SPICES 49

APPENDIX B
ofbactera inhibited
The 30 speciesofbacteriaused to estimatemeanproportion per recipe
(seeFigure9)
Bacterial Species
Acznetobacter calcoacetzcus Clostradzum botulznum Mzcrococcusluteus
Aerobacter aerogenes Clostradzum sporogenes Proteusvulgaris
Aeromonashydrophzla Enterobacteraerogenes Pseudomonasaerugznosa
Alcalzgenesfaecalzs Erwznzacarotovora Salmonellapullorum
Baczllus cereus Eschernchzacolz Serratzamarcescens
Baczllussubtilzs Flavobacteraum suaveolens Staphylococcus
albus
Beneckeanatraegens Klebszellapneumonzae aureus
Staphylococcus
Brevzbacteraum lznens Lactobacillusplantarum Staphylococcus
faecalzs
Brocothrax thermosphacta Leuconostoccremoras Streptococcus
faecalzs
Citrobacterfreundzz Lzsterzamonocytogenes Yersznzaenterocolztzca

References
Abdou et al. 1972 Farbrood et al. 1976 Kivanc and Akgul 1986
Ahmed et al. 1994 Gandi and Ghodekar 1988 Kubo et al. 1991
Aktug and Karapinar 1986 Gugnani and Ezenwanze 1985 Mascolo et al. 1989
Arras et al. 1992 Hargreaves et al. 1975 Onawunmi and Ogunlana 1986
Azzouz and Bullerman 1982 Hassan et al. 1989 Ramadan 1972
Bayoumi 1992 Hefnawy et al. 1993 Rees et al. 1993
Beuchat 1994 Hughes and Lawson 1991 Sato et al. 1990
Briozzo et al. 1989 Huhtanen 1980 Saxena and Vyas 1986
Deans and Ritchie 1987 Islam et al. 1990 Shelef 1984
El-Kady et al. 1993 Ismaiel and Pierson 1990a,b Shelef et al. 1980
El-Khateib and El-Rahman 1987 Jayand Rivers 1984 Shettyet al. 1984
Evert Ting and Deibel 1992 Kanemaru and Miyamoto 1990 Stecchini et al. 1993
Farag et al. 1989 Kim and Ryoem 1979 Zaika 1988
Kivanc et al. 1991

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