Billing 1998

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

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4 THE QUARTERLY REVIEW OF BIOLOGY VOLUME 73
INTRODUCTION oping woody,persistenttissue"and state that

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

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

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

1994) and on-line databases (e.g., Agricola, each country(by numberingrecipes consecu-
Biosis,FSTA, and Medline). Most studieseval- tivelyand consulting a random numbers ta-
uated spices as food preservatives,in attempts ble), and tallied how many of our 30 target
to identifyminimum concentrations neces- bacteria were inhibited by at least one spice
saryto suppress bacterial growthwithoutad- in each recipe. Each set of resultsfor the 30
verselyaffectingflavor. recipes was averaged, yielding an estimateof
We included inhibition studies regardless the mean number of bacterial species inhib-
of whether they tested the spice in its pow- ited per recipe per country.Althoughthisesti-
dered form or as purified active ingredients mate is crude, itis unbiased, and probablyrep-
(e.g., volatile oils or oleoresins). We only in- resentative because most of our 30 target
cluded those studies that identifiedbacteria bacteria are distributedworldwide.
to species, but we did not tryto distinguish
"strains"withinspecies. We also did not differ- CLIMATE DETERMINATIONS
entiateamong studiesthattesteddifferent col- The climateof each countrywas determined
ony sizes of bacteria. Not all bacteria have by averaging monthlytemperature and pre-
been studied foreveryspice, and some spices cipitationdata fromeach major citylisted in
weretestedon manymore bacteriathanothers. TheWeatherHandbook (Conwayand Liston1990).
Studies sometimes reached dissimilarcon- Some countries include regions that differ
clusions about whethera spice inhibiteda par- greatlyin latitude and altitude, resultingin
ticularbacterium. We resolved discrepancies majordifferences in mean annual temperatures.
that resulted fromdifferingdefinitionsof in- Potentiallythis presented us with opportuni-
hibitionwithour "inclusive"definitionofinhi- ties to assess variationsin spice use among dif-
bitionas the mortality or retardationof growth. ferentclimaticregions.Unfortunately, among
Concentrationsof spices testedvaried consid- these countries,we could locate regionalcook-
erably(e.g., 100-100,000ppm), and in some books only for China and the United States.
cases differentspice concentrationsled to dif- We analysedthe climateofthese twocountries
ferentconclusions. Ifa studyreportinginhibi- in the followingmanner.
tion fora particularspice testeda higher con- Although Chinese cuisine often is subdi-
centrationthan the studyor studies reporting vided into fourgeographicalregions (Simoons
no inhibition,we assumed the spice was in- 1991), traditional cookbooks were available
deed inhibitory.However,ifstudies using the onlyfornortheasternand southwesternChina
same concentration reported contradictory (Table 1). Northern and eastern China have
results, or if the study reporting inhibition similar (continental) climates,with hot sum-
used a lowerconcentration,we eliminatedthe mers, cold winters and little precipitation;
bacteriumfromconsideration relativeto that southernand westernChina also have similar
spice. Studies thatdid not reportthe concen- (subtropical) climates,withhot, humid sum-
trationstestedwere not included. mers,mild wintersand moderate rainfall(Si-
We wanted to quantifythe proportion of moons 1991). We calculated the mean annual
local food-spoilagebacteria thatwould be in- temperature and precipitation for the cities
hibited by recipes fromeach country.Unfor- of Lanzhou, Beijing, Tianjin, Shenyang and
tunately,however,no comprehensivelistofin- Shanghai in north and east China, and Kun-
digenous bacteria existsforanycountry,so we ming, Changsha, Hankow, Chungking, Can-
had to estimatethisdegree ofinhibition.First, ton and Nanning in the south and west,using
we listed the 30 species of bacteria that have data in Conway and Liston (1990) and Bair
been experimentally challenged with the (1992).
greatestnumber of spices, regardless of how Traditional cookbooks also were available
frequentlytheywere inhibited (Appendix B). for the northernand southern United States
All 30 were challenged with >10 spices, and (Table 1). We characterizedthese climatesus-
most with ?20 (21/30 = 70.0%); the mean ing Bair's (1992) data on the citiesof Buffalo,
number of spices used to challenge each bac- New York, Pittsburgh,Portland, San Fran-
teriumwas 18.2 ? 3.6 (sd). Next,we randomly cisco, Sault Ste. Marie,Washington(DC), Fair-
picked 30 recipes from the cookbooks for banks andJuneau in the north,and Albuquer-

que, Asheville,Atlanta,Austin,Birmingham, based on correlationof traitvalues of individ-

Brownsville, Los Angeles,
El Paso,Jacksonville, ual species, regardless of relatedness, raises
Louisville,Miami,Nashville,New Orleans and the question ofwhen controllingforphyloge-
Phoenix in the south. netic independence is essential (Weathers
and Siegel 1995).
STATISTICAL ANALYSES Nonetheless,we attemptedto use Mace and
Cross-cultural analysesalwaysconfront"Gal- Pagel's (1994, 1997) phylogenetic methods
ton's problem" (Hartung 1982) of selecting (based on linguisticsimilarities)to select coun-
societies for comparison thatadequately rep- triesfor inclusion in our analyses. However,
resent a range of cultural variation but min- consideringonlycountriesthatbelong, unam-
imizing cases in which similaritiesare due to biguously, to different"linguistic families"
recent common derivationor diffusion.Ana- (Ruhlen 1987) cut our sample size to thepoint
lysingcross-culturaldata also is problematic analysesweremeaningless.More-
thatstatistical
and controversial.Of course, independence over,phylogeneticreconstructionsof societal
of specificculturalpractices is statistically
de- relationships based on linguistic similarities
sirable but, as discussed by Ember and Otter- do not necessarilyyield inferencesabout the
bein (1991) and Mace and Pagel (1994), inde- independence of spice-use patterns.
pendence oftenis impossible to assess. Otterbein (1994:559) stated he "certainly
In an attemptto increase the independence would not cease using worldwide samples in
of our data, we initiallysearched for cook- comparative research because of the alleged
books from cultures or tribes listed in Mur- difficultiesthat arise from the nonindepen-
dock's (1967) StandardCross-Cultural Sample. dence of cases." Moreover,as Hartung (1997:
Unfortunately, we were largelyunsuccessfulin 347) pointed out, "Galton's problem... is like
noise in a signal. It is more likelyto obscure
matching Murdock's sample. Therefore we
truerelationshipsthan to generatefalseones."
sought traditionalcookbooks fromas broad a
We thereforeincluded in our analyses all 36
range of countriesas possible. We discovered
countries for which we obtained traditional
that28 of the 36 countriesforwhichwe found
recipes (Table 1), with the caveat that some
appropriate cookbooks belong to different
countriesare more nearly"independent"than
"tribal clusters"according to Murdock (also
others.
Murdock and White 1969). To improveinde-
We used standard nonparametric statisti-
pendence, we triedomittingall except one of
cal procedures, primarilyPearson product-
the countries that certainlyor probably be-
moment correlations (r), partial correlations,
long to each cluster,but thisseverelyreduced
and chi-squareanalyses (Minitab Release 10.5
our sample size and the range of variation.
Xtra). When multipletestswithina hypothesis
Moreover, the advisabilityof arbitrarilyomit-
were performed,P values were adjusted with
ting countries is questionable when their de-
Bonferronicorrections (Moore and McCabe
grees of independence for a specificcultural
.1993) to minimizeType 1 errors (Rice 1989).
practice are unknown (Ember and Otterbein
Proportional data were appropriately trans-
1991).
formed (arc sine square root) foranalyses.
The use of cladisticmethods to inferinde-
pendence of cultureshas been suggested,but
RESULTS
as pointed out byseveralrespondentsto Mace
and Pagel (1994:557-564) as well as Mace and GENERAL PATTERNS OF SPICE USE
Pagel, themselves (1997:305), it may not be Of the 4578 meat-based recipes we ana-
appropriate to apply maximum parsimony lysed,4241 (93%) called forat least one spice.
techniques thatwere developed forinvestigat- The mean number of spices per recipe was
ing biological origins to inferringcultural 3.9 (?+1.7 sd). In ten countries (28%), namely
"phylogenies."Moreover,the recentreportby Ethiopia, Kenya, Greece, India, Indonesia,
Ricklefsand Starck (1996) that comparative Iran, Malaysia, Morocco, Nigeria and Thai-
analyses of physiological and morphological land, every meat-based recipe called for at
traits(of birds) based on phylogeneticrecon- least one spice. By contrast,in Finland and
structionsyielded similarconclusions to those Norway,respectively,19 of 62 (31%) and 25

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

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

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

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

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

(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.

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

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

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

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

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

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

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

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

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.

spice use when temperatureis statistically con- The final prediction of the antimicrobial
trolled. Although these resultsofferno defi- hypothesis is that the spices used most fre-
nite supportforthe antimicrobialhypothesis, quently in a region should be particularly
theyalso do not militateagainst it. First,tem- effectiveagainst local food-spoilage microor-
peraturetypicallyis more importantforbacte- ganisms.Evaluatingthisrequires comprehen-
rial growththan humidity(Bryan et al. 1979; siveknowledge of indigenous bacteria. Unfor-
Gilbert1979; Hobbs and Roberts1993); more- tunately,this informationdoes not exist for
over,concentrationsof airborne bacteria can any country.We attemptedto generate listsof
actuallybe reduced by high relativehumidity bacteria involved in foodborne disease out-
or rain, whereas concentrations can be in- breaks from data supplied by the World
creased by high temperaturesor wind veloci- Health Organization and the U.S. Centersfor
ties (e.g., Bovallius et al. 1978). Second, mean Disease Control. Such informationwas avail-
annual precipitation may not reflectthe hu- able onlyfornine countries,however,most of
miditythatis typicalof a countryor region if them European, and among these traditional
precipitation is seasonal, the soil porous, or cookbooks were available for only five.More
surface evaporation rapid. Third, in many importantly,only selected bacteria from cer-
countriesopen firesare closelyassociated with tain recent outbreaks were identifiedto spe-
food preparation and storage areas (e.g., Mi- cies, selected bacteria differedamong coun-
chanie et al. 1988), so humiditiesin "kitchens" tries,and causes of many outbreaks remain
maybe lower (and temperatureshigher) than unidentified.Thus, the data were inadequate
in the outside air. for generating comprehensive listsof indige-
A thirdprediction of the antimicrobialhy- nous bacteria.
pothesis is thatthe most potent spices should Althoughwe were unable to testthisfourth
be favoredwhere foods spoil fastest.It is con- predictiondirectly, we note thatthereis a strong
ventionalwisdom thatfood fromhot climates positive correlation between mean tempera-
tends to be spicy ("hot"). Indeed, we found turesand estimatedproportionsoffoodborne
thatmeat-basedrecipesfromhot countriesand bacteria inhibited by the spices in an average
hot regionsofChina and theUnited Statesgen- recipe (Figure 9). The 30 targetbacteria for
erallycontainmore spicesand spiceswithmore this analysis (Appendix B) were chosen be-
potentantibacterialeffectsthan cuisinesfrom cause they have been experimentallychal-
cooler countriesor cooler regionsof countries. lenged with the greatest number of spices.
There are significantpositivecorrelationsbe-
Most of these microorganismsare widelydis-
tween annual temperaturesand use of cinna-
tributed geographically (e.g., Aeromonashy-
mon, cumin,onion, garlicand capsicums (Fig-
drophila,Bacillus cereus,B. subtilus,Clostridium
ure 5), all ofwhichare powerfulantibacterials
botulinum, Escherichia
Listeriamonocytogenes, coli,
(Figure 6). There also is a strongcorrelation
Salmonellapullorum,Staphylococcus aureus), so
betweentemperaturesand proportionsofrec-
theyare likelycontaminants in the foods of
ipes thatcall forthe highlyinhibitory(-75%
most countries.Moreover,actual proportions
inhibition) spices used in each country(Fig-
ure 7a), and a positivebut nonsignificantrela- of indigenous foodborne bacteria inhibited
tionship between proportions of countries per recipe probablyare higherthan indicated
thatuse each spice and proportionsof bacte- in Figure 9 for countrieswithmean tempera-
rial species each spice inhibits (Figure 8). By tures>210 C because the spices used mostfre-
contrast,thereis no correlationbetween tem- quently in hot climates (e.g., capsicums, gar-
peraturesand proportionsof recipes thatcall lic, onion, cinnamon and cumin) are such
for each less inhibitoryspice (<75% inhibi- powerful antibacterials (Figure 6). Use of
tion; Figure 7b). Although a similarfraction these broad-spectrum antimicrobial chemi-
of the spices used in cooler and hotterregions cals should raise the fraction of indigenous
of the United States and China are highlyin- bacteria inhibited in hotterclimates,making
hibitory,proportions of recipes calling for at the actual relationshipbetween temperature
least one highly inhibitoryspice are signifi- and inhibitionper recipe even stronger.
cantlygreaterin hotter (southern) regions of There is an intriguing,order-of-magnitude
both countries. differencein the frequencyof foodborne ill-

nesses between modern Japan and Korea. place in foods that are cooked longer and at
From 1971 to 1990 food poisoning, primarily higher temperatures in the absence of the
of bacterial origin,affected29.2/100,000Jap- acid (Gould et al. 1983; Gould 1992). Pepper
anese but only 3.0/100,000 Koreans (Lee et also has synergistic effects;itfunctionsas a bio-
al. 1996). This differenceseems surprising,es- availabilityenhancer, increasing the rate at
peciallysince these nearbycountrieshave sim- which the active ingredients in other spice
ilar,temperateclimates.Lee et al. (1996) sug- chemicals become physiologicallyavailable to
gested thatthisdifferenceis owing to cultural or are absorbed by epithelial cells (Johriand
differencesin food handling and preparation Zutshi 1992), and also presumablybymicroor-
procedures, and this may well be so. But, in ganisms. In addition, pepper is a powerful
addition, Korean recipes are spicier. Com- antioxidant,which by itselfoftenis sufficient
pared toJapanese recipes, Korean recipes (i) to prevent oxidative food deterioration (Lin
more frequentlycall for at least one spice 1994). Perhaps the widespread use of pepper
(88% vs. 74%), (ii) contain more spices per and citrusjuices relates to theirpropertiesas
recipe on average (3.6 vs. 2.2), and (iii) more antimicrobialsynergists(and antioxidants).
frequentlycall for ,:1 highlyinhibitoryspice Under the antimicrobialhypothesis,correla-
(75% vs. 54%). As a result,the estimatedpro- tionsbetweenfrequenciesofspice use and tem-
portion offoodborne bacteria inhibitedbyan perature occur because food-spoilagemicro-
average recipe is significantly(P<0.01) higher organisms multiplyfasterin hotter climates,
in Korean (51%) thanJapanese cuisine (12%; making antimicrobial substances more valu-
see Figure 9). Why traditionalJapanese reci- able there. But whydon't traditionalrecipes
pes do not call for more potent spices is un- fromcountrieswithcool climatescall for (po-
known. One possibilityis that the spices used tent) spices more often?Certainlysome tropi-
in traditionalJapanesecuisine were adequate cal spices (e.g., allspice, cinnamon, laos and
protection against bacteria when fresh sea- cloves) maynot have been readilyavailable in
food was available from local waters. Today, certaincountrieswhen traditionalrecipeswere
since more food is imported and comes from being developed. Nevertheless, most spices
fartheraway,it may contain more species of have rather broad distributions (Table 2).
foodborne bacteria and fungi. Traditional Moreover, lemon and lime trees and pepper
Japanese recipes may not include enough onlygrowin a fractionofthe countrieswe sam-
spices (antimicrobials) to cope withthese new pled (all tropical), and yet these spices are
infestations. used farand wide, including in Scandinavia.
Use patternsofpepper and lemon and lime Part of the answermaybe thatusing spices
juice at firstappear to contradictthe antimi- involvescertain costs: (1) financial costs asso-
crobial hypothesis.Although theyare among ciated withprocuringdried plants thatdo not
the five most frequentlyused spices (Figure growlocally; (2) illnesses caused by ingesting
1), theyare among thefiveleasteffective against spices thatare themselvescontaminated with
bacteria (Figure 6), and theirfrequencyofuse bacteria or fungi (e.g., due to lengthyor im-
is not positivelycorrelated with temperature proper storage: Pruthi 1980; Pafumi 1986);
(Figure 13). Moreover,most countriesin our and (3) short-termand long-termphysiologi-
sample import these spices; Citrustrees and cal costs associated with ingesting plant sec-
Piperplants are available locally in only 9-11 ondary compounds and essential oils (Saxe
countrieswithwarm climates (Table 2). 1987;Johns 1990). Regarding the latter,Beier
however,lemon and limejuice
Interestingly, and Nigg (1994) comprehensivelyreviewed
to enhance the
(citricacid) act synergistically the mutagenic,teratogenic,carcinogenic and
antibacterial effectsof other spices (Bach- allergenic effects of plant secondary com-
mann 1916; Booth and Kroll 1989; Giese 1994; pounds, including many spices. In hot cli-
Ziauddin et al. 1996), probably because low mates,the benefitsofavoidingfood poisoning
pH disrupts bacterial cell membrane func- and foodborne illnesses apparentlyoutweigh
tion. As a result, foods to which an acid is dangers associated withingestingthese chem-
added require relativelymild heating to cause icals. In cool climates,however,there proba-
the same levelsofbacterialmortalitythattakes blyare fewerindigenous pathogens,and foods

maydecay slowlyenough thatfurtherretarda- medicine, however. In cooking, spices are

tion of spoilage may not be worththe associ- added routinely(regardlessof health statusof
ated health risksof ingestingspices, or the ex- consumers) and in relativelytinyquantities,
pense of obtaining them. whereas medicinal uses of spices are occa-
Strong-tasting and spicyfoods oftenare un- sional (in response to specificmaladies) and
acceptable to pregnant women (Profet 1992, usually in much larger quantities. These dif-
1996), especially during the firsttrimester. ferences implythat spices are used primarily
Profetsuggestedthatmorningsicknessimposes to remedychronicproblemsratherthanacute
adaptive dietaryrestrictionson the mother. illnesses. Among chronic problems, spices
Women who experience morning sickness might (i) supply necessary micronutrients
have lowermiscarriageratesthanwomen who (Johnsand Chapman 1995; Milner 1996), (ii)
do not (Weigel and Weigel 1989), perhaps be- combat persistententeric infections,or (iii)
cause the formerminimize fetal exposure to kill microorganisms that usually colonize
dangerous substances in food, such as plant food. Unfortunately,the micronutritionalval-
secondary compounds. Likewise,young chil- ues ofmostspices are unknown.However,pos-
dren, who are undergoing rapid growthand itive correlations between annual tempera-
are more susceptible than adults to develop- turesand use of spices (Figures 2, 4, 5 and 7)
mental abnormalities,find spicyfoods unac- and regional differenceswithincountriesare
ceptable (Rozin 1980; Rozin and Schiller1980). not predicted by (i), unless for some reason
Perhaps both children and pregnant women people in warmer climates require more mi-
avoid strong (spicy) tastes,even though this cronutrients.Regarding (ii), the rapiditywith
potentiallyexposes them to greater dangers which ingested spice chemicals are catabo-
offood poisoning and foodborne illnesses,be- lized and theireffectson entericinfectionsare
cause of the even greaterrisksassociated with unknown. However, most spices are not in-
ingesting potentially mutagenic chemicals. gested solely in response to feeling ill, and
Context-dependent shifts in spice use be- spices are routinelyused in food preparation
tweenchildhood and adulthood, and between but not routinelyingested alone (garlic is a
pregnancyand nonpregnancy,maythus have notable exception). Thus, presentlyavailable
a common, adaptive basis. data are most consistentwith the hypothesis
Janzen (1978) suggested that animals (in- (iii) that parasites and pathogens on and in
cluding humans) consume plants containing foodsare theprimarytargetsofspice chemicals.
unusual-tastingor foul-tastingand potentially Although humans are the only creatures
poisonous compounds as a means of "self- that elaborately prepare their foods, it is an
medication" (reviewed by Clayton and Wolfe interesting question whether other species
1993). An oftencited example is the ingestion regularly"spice" theirdietswithsmall quanti-
of the leaves of putativelymedicinal plants by ties of plant secondarycompounds. Extensive
chimpanzees afflictedby gastrointestinalpar- informationis available on the food habits of
asites and other maladies (Huffman and wild mammals,based mainlyon analysesoffe-
Wrangham 1994). Virtuallyeveryspice in our ces and stomach contents.Deer (Klimstraand
sample has an ethnopharmacological use Dooley 1990; Johnson et al. 1995) and elk
among traditionalsocieties,oftenas a topical (Sherlock and Fairley 1993) consistentlyin-
or an ingested antimicrobial (e.g., Martinez gest trace amounts of aromaticplants thatare
1944; Perry1980; Koo 1984; Etkin 1986; Chev- foul-tasting or bitter-tasting
to humans. "Vege-
allier 1996). A few spices, particularlygarlic, tation"also formsa small but significantfrac-
ginger, cinnamon and capsicums, have for tion (5-35%) of the diet of most wild carni-
centuries been taken to counteract a broad vores, such as red foxes (Cavallini and Volpi
spectrum of ailments,including pneumonia, 1995; Ferrariand Weber 1995), coyotes (Berg
dysentery, kidneystones,high blood pressure, and Chesness 1978; Parker 1995), bobcats
wormsand nausea (Beuchat and Golden 1989; (Maehr and Brady1986), and cougars (Robin-
Duke 1994; Cichewiczand Thorpe 1996). ette et al. 1959; Ackerman et al. 1984). Un-
Use of spices in food preparation generally doubtedly some of thisvegetationis ingested
differsin twowaysfromtheiruse in traditional foritsmacronutrients,as when meat is scarce.

Nonetheless,frequentingestionofvegetation 1985). Our finding that traditional recipes

is interestingbecause mammalian carnivores, from hotter countries call for more spices
particularlythose that eat carrion, are so fre- (Figure 4), especiallypungentspices,is consis-
quentlyexposed to food-spoilagebacteria and tentwiththishypothesisbecause therewould
fungi.It would interestingto know ifa coyote more often be foul smells or bad tastes to
benefitsin the context of inhibitingsuch mi- "cover up" owing to rapid spoilage.
croorganismsby nipping a fewsage leaves or The "cover-up"hypothesisignores the po-
juniper berries. tentiallyserious negative consequences of in-
Our data are relevantto severalalternatives gestingbacteria-laced foods, however.Across
to the antimicrobial hypothesis.First is the the world,foodborne bacteria (especiallyspe-
possibilitythatspices providemacronutrients, cies of Clostridium, Escherichia,
Listeria,Salmo-
vitaminsor minerals. However, compared to nella,Staphylococcus,Streptococcus,
see Evans and
spices,most common vegetablescontain more Brachman 1991;Jay1994; Todd 1994,1996) or
protein,carbohydrates,fat,starch,fiber,min- theirtoxinsdebilitatemillionsof people annu-
erals and a greatervarietyofvitaminsthan do ally and kill thousands. In the United States
spices (Tan 1985; Holland et al. 1991). No alone, foodborne illnessesafflictan estimated
"nutritionalfacts"panel even appears on the 80 million people per year (World Health Re-
labels ofmostcommercialspices in the United port 1996), and one in ten Americans experi-
States (exceptions are paprika and chili pow- ences bacteria-related food poisoning annually
der, which contain vitaminA). For these rea- (Hui et al. 1994). Moreover,new foodborne
sons several authorities (e.g., Ensminger et pathogens are continuallyevolving(e.g., Not-
al.1983; Farrell 1990; Kirschmannand Dunne ermans and Hoogenboom-Verdegaad 1992;
1984) have stated thatspices are of littleor no Butler 1996). Disguisingtastesassociated with
nutritivevalue, especiallyin the tinyquantities spoilage or contaminationpotentiallyincreases
in which theyare generallyconsumed. exposure to foodborne diseases. Even poorly
Spices may supply rare micronutrients, nourished individualsmightbe betteroffrec-
however.Plant secondarycompounds, includ- ognizing and passing up tainted foods, espe-
ing those found in some spices (particularly cially meat products (Roberts 1990; Sockett
garlic and onions), can have beneficial effects 1995), when thereis a chance of ingestingpo-
such as aiding digestion, modulating energy tentiallydeadly quantities of microorganisms
metabolism,and actingas antioxidants(Johns or theirtoxins.It mayeven be thatthe advan-
1990;Johnsand Chapman 1995). Some phyto- tages of recognizing and avoiding spoiled or
chemicals also may help postpone degenera- contaminated foods explain the sensitivity of
tivediseases such as diabetes, coronaryheart our olfactoryand gustatorysystemsto smells
disease and cancer (Milner 1996). Whether and tastesof decay. Thus, froman evolution-
the majorityofspices in our sample could pro- ary perspective,the "cover-up" hypothesisis
vide thesebenefits,and whetherthequantities seriouslyflawed.
recipes call for supply sufficientmicronutri- A thirdalternativehypothesisis that spicy
ents to do so, are just beginning to be investi- foodsare preferredin hotclimatesbecause they
gated (Aruoma et al. 1997). Regardless, the help cool the body evaporatively by increasing
micronutritionhypothesisdoes not predictor perspiration(see Rozin and Schiller1980; Bos-
explain the multiple positive correlationswe land 1994). Capsicums can produce hypother-
found between mean temperaturesand spice mia, either througha gustofacialsweatingre-
use (Figures 2, 4 and 7), particularlyforcapsa- flex or direct action on the hypothalamus
icins and otherspices withpowerfulantibacte- (Rozin and Schiller 1980). However, most
rial properties (Figure 5). Thus, dietarysup- spices whose use increases withmean temper-
plementation does not appear to be the sole, atures (e.g., garlic, onion, anise, cinnamon,
or even the primary,reason forthe popularity coriander, ginger, lemongrass) do not pro-
of spices, especiallyin hot climates. duce hypothermia,and even chilies do not in-
A second hypothesisis thatspices are used crease perspiration in many people (Rozin
because they disguise the smell or taste of and Schiller 1980). Moreover, sweating is a
spoiled foods (Barker 1982; Govindarajan metabolicallyexpensivewayto cool off,and it

requires abundant water to sustain it. In the ternsbecause proportionsof recipes thatcall
contextofthe spice-usepatternswe have iden- formost spices are higher in countrieswhere
tified,the evaporativecooling hypothesiscan- those spices grow.Moreover,recipes of hotter
not be a general explanation. countries call for greater fractionsof locally
A final possibilityis that spices confer no available spice plants,as indicated bythe posi-
benefits,and that people simplyuse which- tive correlation between temperatures and
ever aromatic plants are at hand to improve proportionsof spices used in the countriesin
the tasteof food. Harris (1985:15), Nesse and which theygrow. However, since there is no
Williams (1994:147-151), and Letarte et al. relationship between mean annual tempera-
(1997) discussed how human taste receptors turesand numbers of spices thatgrowin each
and gustatorypreferenceshave been shaped country(Figure 10), the multiplepositivecor-
by nutritional benefits normally associated relationsbetween temperaturesand frequen-
with favored flavors.Potentiallyedible items cies of spice use (Figures 2, 4, 5 and 7) are not
are expected to be tastyiftheirchemical con- simplyowing to greaterspice plant availability
stituentsmatchcloselyenough those normally in hotter countries. In sum, local availability
found in nutritiousfoods. This "null"hypothe- of a spice plant does not necessarilymean that
sis predicts that spice chemicals should be residentswilluse it,and lack of local availabil-
highlypalatable, and that spice-use patterns itydoes not mean thatresidentswillnot use it.
should correspond closelyto naturalranges of Rozin (1982) hypothesized that humans
spice plants. seek varietyin foods to ensure thattheyobtain
Neither prediction is supported. First,fla- a nutritionallybalanced diet. It is well estab-
vorsof manywidelyused spices are not imme- lished that the perceived diversityof foods
diatelyappealing. Indeed, pungent spices like consumed positivelyinfluences the amount
garlic, ginger, onion, anise, turmeric and consumed (Rozin and Vollmecke 1986). Ac-
black pepper initiallyare unappealing to most cording to Rozin, we habituate to commonly
people, especially to children (Rozin 1980), eaten foods (the "sensory-specificsatietyef-
and the capsaicin in hot chili peppers causes fect") because our taste preferences,which
painful sensations (Caterina et al. 1997). For ensure thatwepursue variety,evolvedat a time
most disagreeable substances,an initialnega- when dietswere chemicallymore diversethan
tive response is sufficientto maintain avoid- theyare today.If so, spice use mayfunctionto
ance throughout an individual's life. How- "trick"our internal mechanisms; by seeming
ever,preferencesforspices develop withage, to provide dietaryvariety,spices encourage
usually under familial guidance (Rozin and consumption of greaterquantities of (bland)
Schiller 1980). The fact that parents encour- foods. This hypothesisis intriguing,but itdoes
age theirchildren to eat (displeasing) spices, not predict or explain patterns of spice use
and thatchildrencome to preferthembyado- demonstrated here, especially relationships
lescence, stronglysuggeststhatusing spices is with temperature (unless for some reason
somehow beneficial. people in hot climatesmore frequentlyexpe-
Second, people do not use everyspice that rience dietarydeficienciesdue to sensory-spe-
grows in their country (Figure 11), but they cificsatiety).
do use many spices that must be imported How do people know what spices to use?
(Figure 12), and for centuries have gone to We can envisiontwopossibilities.First,people
greatlengthsto obtain them (e.g., Govindara- who happened to add spice plantsto meat dur-
jan 1985). An extreme example is pepper, ing preparation, especially in hot climates,
whichis one ofthemostfrequentlyused spices may have been less likelyto sufferfromfood
in all 36 countrieswe sampled (Figure 1), but poisoning or foodborne illnesses than those
which growsin only nine of them (Table 2). who did not. Spice users also may have been
Pepper is the most frequentlyimported spice able to storefoods longer before theyspoiled,
into the United Statestoday (about 87 million enabling them to tolerate longer periods of
pounds in 1991: Tainter and Grenis 1993). scarcity. Observation and imitation of the
Althoughlocal availabilityis not a sufficient eating habits of these healthier individualsby
explanation, it certainlyaffectsspice-use pat- otherscould spread spice use rapidlythrough

a society.Also, familiesthatused appropriate Our correlational or "forwardapproach"

spices would rear more healthyoffspring,to (Sherman and Reeve 1997) analyses of spice
whom spice-use traditionshad been taught use would be usefullycomplemented by ex-
and who possessed appropriatetastereceptors. perimentalstudies of how the use of different
These children would pass to their progeny spices and spice combinations affectsindivid-
both the "memes" (Dawkins 1976) for using ual fitnessin differentcountries and cultures
particularspices and the receptor physiology (i.e., the "backward approach"). A decisive
for tastingthem (e.g., Caterina et al. 1997); testof the antimicrobialhypothesiswould in-
individualdifferencesin receptorsensitivity to volve quantifyingthe frequencyof foodborne
spices are discussed by Drewnowskiand Rock illnesses, and the survivaland reproductive
(1995) and Tepper and Nurse (1997). successes ofindividualslivingin the same geo-
A second possibilityinvolveslearned taste graphic area and eating essentiallythe same
aversions. When people eat something that foods,but using differentspices and combina-
makes them ill, theytend to avoid that taste tions of them.
subsequently (Milgram et al. 1977; Pelchat In sum, we believe that the probable ulti-
and Rozin 1982). The adaptive value of such mate reason whyhumans spice foods is to take
learning is obvious (Letarte et al. 1997). Add- advantage of the antimicrobialactions of the
ing a spice to a food thatcaused nausea might plant secondary compounds that give spices
alter its taste enough to make it palatable their flavors.We hypothesize that,by cleans-
again (i.e., it tastes like a differentfood), as ing foods of pathogens,spice users contribute
well as killthe microorganismsthatcaused the to their health, survival and reproduction.
illness, thus rendering it safe for consump- These then maybe the reasons whymanypeo-
tion. By this process, food aversions would ple, especially those living in or visitinghot
more oftenbe associated withunspiced (and climates,preferfood thatis spicy.
unsafe) foods,and food likingswould be asso-
ciated with spicy foods, especially in places
ACKNOWLEDGMENTS
wherefoods spoil rapidly.Over time,the habit
of spicing foods and use of multiple spices in For helpfulcommentsduringthecourseofthis
each recipe could become prevalentowing to researchwe thankthe Animal BehaviorLunch
Bunch at CornellUniversity PeterS
(particularly
the iteration of this process (i.e., sequential
Buston,HamiltonE Farris, JohnM Peters,H Kern
changes in spices and tastesfor them, associ-
Reeve and PhilipT Starks),the MuseumLunch
ated withinhibitionof differentbacteria and Bunchat theUniversity of Michigan(particularly
fungi). RichardD Alexander,John Cooley,DavidMarshall
Of course, spice use is not the only way to and CynthiaSimmsParr),and ThomasA Gavin,
avoid food poisoning and foodborne patho- GavinB Grant,Bobbi S Low, RichardD Howard
gens. Cooking and completelyconsumingwild and Deedra K McClearn.Forassistancewithrefer-
game immediatelyafterslaughterreduces op- enceswethanktheCornellUniversity Food Science
portunitiesformicroorganismalgrowth.How- and Nutrition Department, theCornellCollegeof
ever,thisis practical onlywhere freshmeat is HumanEcologyand theDivisionofNutritional Sci-
abundant year-round(e.g., Ache hunter-gath- enceStatisticalConsultingService,theCornellUni-
erers in Paraguay: Hill et al. 1984). In areas versityOlin Library Loan Department,
Interlibrary
where freshmeat is not consistentlyavailable, and theCirculation andReference staffatCornell's
Mannand Nest1lLibraries.Forcommentson pre-
preservation may be accomplished by thor-
liminaryversionsofthemanuscriptwethankThomas
oughlycooking, salting,smoking,drying,and
Eisner,ThomasA Gavin,ThomasNeuhaus,Frank
spicing meats. Indeed, salt has been used A Pitelka,H KernReeve,LaurelSouthardand Bev-
worldwidefor centuries to preservefood (Al- erlyI Strassmann. Duringtheresearch, JBwaspar-
ford and Palumbo 1969; Helmy et al. 1985). tiallysupportedbya HowardHughesSummerFel-
We hypothesize that all these practices have lowshipadministeredby Cornell University and
been adopted foressentiallythe same reason: PWSwassupportedbygrantsfromtheNationalSci-
to minimize effectsof foodborne pathogens. ence Foundationand CornellUniversity.

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

APPENDIX A continuation
Capsicums Baczllus cereus Lzsterza monocytogenes Evert Ting and Deibel 1992
(Chilies) Baczllus subtilzs Hargreaves et al. 1975
Sarczna lutea Hefnawy et al. 1993
Staphylococcus aureus Kim and Ryeom 1979
Caraway Acznetobacter calcoaceticus Brevzbacteraum lznens Deans and Ritchie 1987
Aeromonas hydrophzla Clostndzum botulznum Farag et al. 1989
Alcalzgenes faecalis Clostradium sporogenes Hargreaves et al. 1975
Beneckea natnegens Lactobaczllus plantarum Huhtanen 1980
Brocothrix thermosphacta Micrococcus luteus Ramadan et al. 1972
Cztrobacterfreundzz Staphylococcus faecalzs
Enterobacter aerogenes Streptococcusfaecalzs
ErYwznzacarotovora Yersznza enterocolztzca
Klebsiella pneumonzae
Leuconostoc cremoras
Mycobacteraumphlei
Proteus morganzz
Proteus vulgaras
Pseudomonas fluorescens
Salmonella enteritzdzs
Salmonella pullorum
Serratza marcescens
Staphylococcus aureus
Cardamom Aeromonas hydrophzla Aczneto.bacter calcoacetzcus Azzouz and Bullerman 1982

Baczllus anthraczs Alcalzgenes faecalis Bayoumi 1992
Bacillus cereus Beneckea natraegens Deans and Ritchie 1987
Brocothrax thermosphacta Brevzbacteraum lznens El-Kady et al. 1993
Flavobacteraum suaveolens Cztrobacterfteundzi Islam et al. 1990
Lactobaczllus bulgaricus Clostradium sporogenes Kubo et al. 1991
Leuconostoc cremoras Erwznza carotovora
Mzcrococcus (Sarczna) Lactobaczllus plantarum
Pseudomonas fluorescens Micrococcus luteus
Pseudomonas pyocyanea Salmonella pullorum
Salmonella paratyphz Serratza marcescens
Serratia rhadnii Streptococcusfaecalzs
Streptococcus thermophzlus Streptococcus nasik
Yersznza enterocolitzca
Celery Seed Aerobacter aerogenes Acinetobacter calcoaceticus Deans and Ritchie 1987
Baczllus subtzlzs Aeromonas hydrophila Huhtanen 1980
Brocothnx thermosphacta Alcalzgenes faecalis Kivanc and Akgul 1986
Clostradzum botulznum Baczllus cereus Ramadan et al. 1972
Flavobacteraum suaveolens Beneckea natraegens
Leuconostoc cremoris Brevzbacterium lznens
Staphylococcus albus Cztrobacterfreundzz
Staphylococcus aureus Clostradzum sporogenes
Enterobacter aerogenes
ErYwinzacarotovora
Klebszella pneumonzae
Lactobaczllus plantarum
Mzcrococcus luteus
Salmonella pullorum
Serratza marcescens
Staphylococcus faecalzs
Streptococcusfaecalzs
Yersznia enterocolztzca

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
Lactobaczllusbulgaracus
Lactobaczllusplantarum
Leuconostoccremoris
Lzsterzamonocytogenes
Mzcrococcus luteus
Proteusvulgaras
Pseudomonasfluorescens
Pseudomonaspyocyanea
Salmonellaparatyphz
Salmonellapullorum
Serratzamarcescens
Serratzarhadnzz
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
Salmonellaenterntzdzs

Cloves Salmonella pullorum
(contznuatzon) Serratza marcescens
Streptococcusfaecalis
Streptococcus naszk
Streptococcus thermophzlus
Yersznza enterocolztica
Coriander Aerobacter aerogenes Acinetobacter calcoacetzcus Deans and Ritchie 1987

Aeromonas hydrophzla Alcaligenesfaecalzs Hargreaves et al. 1975
Bacillus subtzlis Beneckea natraegens Huhtanen 1980
Brocothrix thermosphacta Brevibacteraum lznens Kivanc and Akgul 1986
Cztrobacterfreundii Clostradium sporogenes Stecchini et al. 1993
Enterobacter aerogenes Micrococcus luteus
Erwinia carotovora Proteus vulgaras
Escherichza colz Salmonella pullorum
Flavobacteraum suaveolens Serratia marcescens
Klebszella pneumoniae Staphylococcus faecalzs
Lactobacillus plantarum Streptococcusfaecalis
Leuconostoc cremoris Yersinia enterocolitzca
Staphylococcus albus
Cumin Aerobacter aerogenes Klebszella pneumonzae Azzouz and Bullerman 1982

Baczllus anthraczs Pseudomonas pyocyanea El-Kady et al. 1993
Baczllus cereus Serratza rhadnzz Farag et al. 1989
Baczllus coagulans Hassan et al. 1989
Bacillus subtilzs Hefnawy et al. 1993
Clostridzum botulznum Huhtanen 1980
Enterobacter aerogenes Kivanc and Akgul 1986
Lactobaczllus plantarum Kivanc et al. 1991
Leuconostoc mesenteroides Ramadan et al. 1972
Listeria monocytogenes Saxena and Vyas 1986
Micrococcus (Sarczna) Shetty et al. 1994
Proteus vulgaris
Pseudomonas aeruginosa
Salmonella enterntidzs
Salmonella paratyphz
Serratia marcescens
Streptococcus nasik
Dill Acznetobactercalcoaceticus Alcalzgenes faecalis Deans and Ritchie 1987

Aerobacter aerogenes Beneckea natraegens Hargreaves et al. 1975
Aeromonas hydrophila Brocothrix thermosphacta Huhtanen 1980
Brevzbacterium lznens Clostridaum botulznum Kivanc and Akgul 1986
Cztrobacterfreundii Clostradium sporogenes Ramadan et al. 1972
Enterobacter aerogenes Lactobacillus plantarum
ErYwznzacarotovora Leuconostoc cremoris
Flavobacteraum suaveolens Micrococcus luteus
Klebszella pneumoniae Salmonella pullorum
Proteus vulgaris Staphylococcus faecalis
Pseudomonas aerugznosa Streptococcusfaecalis
Serratia marcescens Yersznza enterocolitica

Fennel Aerobacter aerogenes Alcaligenesfaecalis Deans and Ritchie 1987
Bacillus cereus Beneckeanatriegens Hargreaves et al. 1975
Baczllussubtzlzs Brevibacterium lznens Huhtanen 1980
Citrobacterfreundzz Brocothrix thermosphacta Kivanc and Akgul 1986
Enterobacter aerogenes Clostridium botulinum Ramadan et al. 1972
ErYwznza carotovora Clostridium sporogenes
Flavobacteraum suaveolens Klebsiellapneumoniae
Leuconostoccremoris Lactobaczllusplantarum
Proteusvulgaras Mzcrococcusluteus
Salmonellaenteritidis Staphylococcusfaecalzs
Salmonellapullorum Yersznzaenterocolitzca
Serratzamarcescens
Garlic Baczllus cereus None Abdou et al. 1972
Baczllussubtzlzs Beuchat 1994
Campylobacterjejuni El-Khateib and El-Rahman 1987
Clostridzum perfrangens Evert Ting and Deibel 1992
Enterobacter cloacae Gandi and Ghodekar 1988
Enterococcus faecalzs Hargreaves et al. 1975
Enterococcus faeczum Hefnawyet al. 1993
Eschernchza colz Hughes and Lawson 1991
Klebsiellaaerogenes Huhtanen 1980
Klebszellapneumonzae Ismaiel and Pierson 1990b
Lactobacillusaczdophzlus Rees et al. 1993
Lactobaczllusplantarum Sato et al. 1990
Listermamonocytogenes Shelef 1984
Pediococcuspentosaceus
Proteusmirabilzs
Proteusmorganzz
Proteusvulgaras
Salmonelladublin
Salmonellaenterntzdzs
Salmonellatyphzmuraum
Serratzamarcescens
Staphylococcus epidermzdzs
Streptococcus agalactiae
Vzbriomimicus
Vzbraoparahaemolytzcus
Yersiniaenterocolitica
Ginger Baczllus anthracis Acznetobactercalcoacetzcus Azzouz and Bullerman 1982
Bacillus subtzlzs Aeromonashydrophila Deans and Ritchie 1987
Brocothrix thermosphacta Alcalzgenesfaecalis Gugnani and Ezenwanze 1985
Flavobacteraum suaveolens Beneckeanatriegens Huhtanen 1980
Leuconostoccremoris Brevibacterium linens Mascolo et al. 1989
Proteusmzrabilis Cztrobacterfreundzz
Salmonellatyphzmurium Clostradium sporogenes
Staphylococcusepzdermzdzs Enterobacteraerogenes
Staphylococcushaemolytzcus Erwznzacarotovora
Streptococcusvzridans Klebszellapneumoniae

Ginger Lactobaczllusplantarum
(contznuatzon) Mzcrococcusluteus
Salmonellapullorum
Serratzamarcescens
Streptococcus
faecalzs
naszk
Streptococcus
Lemon Aerobacter aerogenes Aeromonashydrophzla Deans and Ritchie 1987

Baczllus subtzlzs Alcalzgenesfaecalzs Kivanc and Akgul 1986
Brocothrax thermosphacta Beneckeanatraegens
Flavobacteraum suaveolens Brevibacteraum lznens
Leuconostoccremoras Cztrobacterfreundzz
Staphylococcus albus Clostradzum sporogenes
Staphylococcus aureus Enterobacteraerogenes
Erwzvniacarotovora
Klebszellapneumonzae
Mzcrococcusluteus
Salmonellapullorum
Serratiamarcescens
Lemongrass Baczllus cereus Streptococcusfaecalzs Onawunmi and Ogunlana 1986
Baczllussubtzlis Ramadan 1972
colz
Eschernchia
Salmonellaenteritzdis
Staphylococcusaureus
Lime Aeromonashydrophila Acinetobactercalcoacetzcus Deans and Ritchie 1987

Brocothraxthermosphacta Alcalzgenesfaecalzs Kivanc and Akgul 1986
Flavobacteraumsuaveolens Baczllussubtzlzs
Leuconostoccremoras Beneckeanatraegens
Brevzbacteraum lznens
Cztrobacterfreundzz
Clostradium sporogenes
Enterobacteraerogenes
Ervinza carotovora
Escherichzacoli
Klebsaellapneumoniae
Mzcrococcus luteus
Proteusvulgaris
Salmonellapullorum
Serratzamarcescens
Yerszniaenterocolztzca

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
Erwzvnzacarotovora
Eschernchza colz
Klebszella pneumonzae
Mzcrococcus (Sarczna)
Proteus vulgaras
Pseudomonas pyocyanea
Salmonella enterntzdzs
Salmonella pullorum
Serratza marcescens
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
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

Nutmeg Ervinza carotovora Lactobacillusplantarum
(contznuatzon) Escherichzacolz Micrococcusluteus
Flavobacterium suaveolens Pseudomonasaeruginosa
Leuconostoccremoras Salmonellapullorum
Listertamonocytogenes Staphylococcusaureus
Proteusvulgaras Streptococcus
faecalzs
Serratzamarcescens
Yerszniaenterocolztica
Onion Escherichiacoli None Abdou et al. 1972
Salmonellatyphzmuraum Beuchat 1994
Shigelladysenterzae Hargreaves et al. 1975
Staphylococcusaureus Hughes and Lawson 1991
Huhtanen 1980
Shelef 1984
Oregano Aerobacter aerogenes None Beuchat 1994
Bacillus subtilzs Evert Ting and Deibel 1992
Clostridzum botulznum Huhtanen 1980
Eschernchia colz Ismaiel and Pierson 1990a,b
Lactobaczllusplantarum Kivanc and Akgul 1986
Leuconostocmesenteroides Kivanc et al. 1991
Lzsteriamonocytogenes Shelef 1984
Proteusvulgaras
Parsley Acinetobacter calcoaceticus Aeromonashydrophila Deans and Ritchie 1987
Aerobacter aerogenes Alcaligenesfaecalis Evert Ting and Deibel 1992
Beneckeanatraegens Brevibacterium lznens Kivanc and Akgul 1986
Citrobacterfreundzi Brocothraxthermosphacta Huhtanen 1980
Enterobacter aerogenes Clostradium botulinum
Flavobacteraum suaveolens Clostridium sporogenes
Klebszellapneumonzae Erwzniacarotovora
Salmonellapullorum Lactobacillusplantarum
Serratiamarcescens Leuconostoccremoris
Staphylococcus albus Listeriamonocytogenes
Staphylococcus aureus Micrococcusluteus
Streptococcusfaecalzs Yersinzaenterocolitzca
Pepper Aeromonashydrophila Acinetobactercalcoaceticus Abdou et al. 1972

Bacillus subtilis Alcalzgenesfaecalzs Azzouz and Bullerman 1982
Brocothrix thermosphacta Beneckeanatraegens Deans and Ritchie 1987
Clostradium botulinum Brevibacterium linens Evert Ting and Deibel 1992
Ervinza carotovora Cztrobacterfreundzi Hefnawy et al. 1993
Flavobacteraum suaveolens Clostridzum sporogenes Huhtanen 1980
Lactobacillusmicrococcus Enterobacteraerogenes Islam et al. 1990
Leuconostoccremoras Klebszellapneumoniae Shelef 1984
Streptococcusnaszk Lactobaczllusplantarum Stecchini et al. 1993
Yersinzaenterocolitica Micrococcusluteus
Proteusvulgaras
Salmonellapullorum
Serratzamarcescens
Staphylococcusfaecalis

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
Klebszellapneumonzae
Lzsterzamonocytogenes
Micrococcus(Sarczna)
Mycobacterium phlez
Proteusvulgaras
Pseudomonaspyocyanea
Salmonellaparatyphz
Salmonellapullorum
Salmonellatyphimuraum
Serratzamarcescens
Serratzarhadnzz
Staphylococcus epzdermidzs
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
Streptococcus nasik
Vzbrioparahaemolyticus
Tarragon Aerobacter aerogenes botulznum
Clostradzum Huhtanen 1980
Baczllus subtzlzs Kivanc and Akgul 1986
Escherichzacoli
Proteusvulgaras

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
Ervinia carotovora
Eschernchia coli
Klebszellapneumoniae
Mzcrococcus(Sarczna)
Mzcrococcusluteus
Mycobacteraum phlez
Proteusvulgaris
Pseudomonasaeruganosa
Salmonellaparatyphz
Salmonellapullorum
Salmonellatyphzmuraum
Serratzamarcescens
Serratzarhadnzz
Staphylococcus faecalzs
Streptococcus naszk

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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VOLUME 73, No.

THE QUARTERLY REVIEW

ANTIMICROBIAL FUNCTIONS OF SPICES:

JENNIFER BILLING* AND PAUL W.SHERMAN

* Presentaddress:191 Quail HollowLane, EastAmherst,

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

INTRODUCTION oping woody,persistenttissue"and state that

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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

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

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

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

DiLL Umbelliferae Anethum

FENUGREEK Leguminosae Trigonellafoenumgraecum X -X I I I

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

LAOS Zingiberaceae Alpineagalanga X X X X X X _ I

MINT Lablatae Mentha

NUTMEG Myristicaceae Myristica

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

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

ROSEMARY Labiatae Rosmarinus

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

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

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

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que, Asheville,Atlanta,Austin,Birmingham, based on correlationof traitvalues of individ-

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

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0.8 (b) India

0.4- Kurtosis = 0.7

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20.0 (a) ANTIBACTERIAL PROPERTIES OF SPICES

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0 5 10 152025 30 0 50 100 150200 250

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

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

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. EACH SPICE AND PROPORTIONS OF

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

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and limejuice, green pepper, allspice and cel- 40