Society for Conservation Biology

World-Wide Species Richness Patterns of Tiger Beetles (Coleoptera: Cicindelidae): Indicator

Taxon for Biodiversity and Conservation Studies
Author(s): David L. Pearson and Fabio Cassola
Reviewed work(s):
Source: Conservation Biology, Vol. 6, No. 3 (Sep., 1992), pp. 376-391
Published by: Wiley-Blackwell for Society for Conservation Biology
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World-Wide
SpeciesRichness
Patterns
ofTigerBeetles
(Coleoptera:
Cicindelidae):
Indicator
TaxonforBiodiversit
andConservation
Studies*
DAVID L. PEARSON
Department of Zoology
Arizona State University
Tempe, AZ 85287-1501, U.S.A.

FABIO CASSOLA
via F. Tomassucci 12/20
00144 Rome, Italy

Abstract: The family of tiger beetles (Cicindelidae) is an

appropriate indicator taxon for determiningregional patternsof biodiversitybecause (1) its taxonomyis stabilized;
(2) its biology and general lifehistoryare well understood;
(3) individuals are readilyobservedand manipulated in the
field; (4) thefamilyoccurs world-wideand in a broad range
of habitat types;(5) each species tends to be specialized
withina narrowhabitat; (6) patternsof species richnessare
highlycorrelatedwith thoseof othervertebrateand invertebrate taxa; and (7) the taxon includes species ofpotential
economic importance.Logistical advantages provide some
of the strongestargumentsfor selectingtigerbeetles as an
appropriateindicatortaxon. Species numbersof tigerbeetles
are relativelywell knownfor 129 countries.Eight countries
alone account for more than half the world total of 2028
knownspecies.Species numbersare also indicatedfor eleven
biogeographical zones of the world. For gridded squares
across NorthAmerica,theIndian subcontinent,and Australia, species richness of tiger beetles,birds, and butterflies
shows significantpositive correlations.However,tigerbeetle
species numbers can be reliably determinedwithin fifty
hourson a singlesite,compared to monthsoryearsfor birds
or butterflies,
and the advantage of using tigerbeetles in
conservationbiology is evident
*Studies on tigerbeetles,LXVIII
Paper submittedOctober25, 1991; revisedmanuscriptacceptedFebruary27, 1992.

Resumen: La familia de los escarabajos tigre (Cicindelidae) constituyeun taxon indicador apropiado para determinarpatrones regionales de biodiversidadporque (1) su
taxonomia es estable;(2) su biologia e historia natural son
bien conocidas; (3) los individuos son facilmente observables y manipulables en el campo; (4) la familia tiene una
amplia distribuci6nmundial, asi como un gran variedad de
h*bitats;(5) cada especie tiende a especializarse dentrode
un h*bitat restringido;(6) los patrones de riqueza de especies estdn altamente correlacionados con los de otros taxones de vertebradose invertebrados;
y (7) el taxon incluye
especies de potencial importancia econ6mica. Las ventajas
logisticas de los escarabajos tigreproporcionan una de las
evidencias mds solidas para considerarlosun taxon indicador apropiado. El ntimerode especiesde escarabajos tigrees
bie'nconocido en 129 paises. Ocho de estospaises contienen
mas de la mitad de las 2028 especiesconocidas en el mundo.
Tambien se indica el numero de especiespara once zonas
biogeograficasdel mundo.Mediante el estudio de cuadriculas de muestreosituadas en NorteAmerica,el Subcontinente
Indio y Australia,que ilustran la riqueza de especies de escarabajos tigre,avesy mariposas,se observa una correlaci6n
positiva significativaSin embargo,el numerode especiesde
escarabajos tigrepuede determinarseconfiablementemediante unas cincuenta horas de muestreoen un solo sitio, en
comparaci6n con los meses o anios que se necesitanpara
aves o mariposas,pro lo que la ventaja de utilizar los escarabajos tigreen conservaci6nbiol6gica es obvia

376
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Pearson& Cassola

BeetleDiversity

Introduction
Biodiversityas a focus for conservationhas received
increasingattention(Wilson 1988; Noss 1990; Ehrlich
& Wilson 1991). To testforpertinentpatternsof biodiversity,various protocols and levels of study have
been proposed that include ecological communities
(Hunter et al. 1988), cladistic classifications(VaneWrightet al. 1991), a hierarchicalcompositeofdifferent
levels of organization(Noss 1990), as well as groupsof
taxonomicallyrelatedspecies (Wilson 1988).
Althoughsevere timeand fundinglimitsare problems
formanyresearchprojects,the additionofpolitical,sociological,and culturalpressuresmake conservationbiology a "crisis discipline,"forwhich riskanalysisis a
major considerationin designingprograms(Maguire
1991). A common approach to resolvingthese problems has been to use indicatortaxa as test organisms.
from
The use of indicatortaxa in conservationefforts
pollutioncontrolto biodiversityhas been the focus of
considerableattention(Landres et al. 1988).
No singlespecies or taxon can be expected to represent or indicatepatternsforall otherspecies and taxa.
There are, however,some logisticaland biological criteriathatmaximizethe usefulnessof a taxon as an indicator (Noss 1990), includingthe following:(1) its taxonomyis well-knownand stableso thatpopulationscan
be reliablydefined;(2) its biology and lifehistoryare
well understood-limitingresources,enemies,physical
tolerances,and all stagesof the lifecycle can be incorporated into hypothesesand experimentaldesign;(3)
individualsare readilyobservedin thefield,and studies
are facilitatedby uncomplicatedobservationsand manipulationssuch thatinexperiencedstudentsand nonprofessionalscan be trainedeasilyto help conductstudies; (4) the taxon occurs across a broad geographical
rangeand numberof habitattypesto permitbroad experimentaldesign and comparisons;(5) each population or species tendsto be specializedwithina narrow
habitatand thus sensitiveto habitatdegradationand
regeneration;(6) patternsobserved in the indicator
taxon are reflectedin otherrelatedand unrelatedtaxa,
and (7) the taxon includes species thathave potential
economic importanceso thatscientistsand politicians,
especiallyin ThirdWorldcountrieswherepure or basic
science is frequentlyconsidereda luxury,can be convinced thatthistaxon is worthdedicatinglocal personnel and resourcesforstudies.
The preponderanceofstudiesusingindicatortaxahas
relied on vertebrates,especiallythose "species of high
public interest"(United StatesDepartmentof Interior
[USDI] 1980). Vertebrates,however, tend to be relativelylong-livedand have low rates of population increase, long generationtimes,and comparativelylow
habitatspecificity
(Murphyet al. 1990), all ofwhich tax
time and financesfor proper investigation.More re-

377

centlytherehas been an effort

to overcometheseproblems by using arthropodspecies, especiallyinsects,instead of vertebratesas indicators (Pyle et al. 1981;
Collins& Morris1985; Rosenberget al. 1986; Morris&
Rispin 1988; Murphy& Weiss 1988; Samways 1988,
1989, 1990a,b; Viejo et al. 1989; Webb 1989; den Boer
1990; Rushtonet al. 1990; Thomas 1991).
In additionto displayingthe generalcriteriaforindicatortaxa,insectsare appropriatebecause ofrisingrates
ofhuman-causedextinction(Wilson 1988). Insectsrepresentmore than80% oftheseveralmillionanimalspecies now extantin theworld,and extinctionis probably
in termsof absolute numbersfor inmore significant
sectsthanforanyothergroupoforganismsin theworld.
The familyoftigerbeetles (Coleoptera: Cicindelidae)
is a potentiallyideal indicatortaxon.Theirtaxonomyis
well known.All are predaceous on small arthropods,
and they share similar larval and adult body forms
around the world. Adults are generally diurnal and
foundprimarily
on soil surfaces.Larvaeare easy to raise
in the laboratoryand are relativelyeasy to findand observe in the field (Palmer 1978; Knisley & Pearson
1984; Shivashankaret al. 1988). A journal,Cicindela,
published since 1969, is the result of effortsby both
amateursand professionalsto document basic natural
and identification
history,distribution,
of tigerbeetles
world-wide.
The hypothesisof thispaper is thattigerbeetles are
an ideal bioindicatortaxon.The testswill be comparisons ofthe characteristics
oftigerbeetles to each ofthe
seven criteriaproposed foran ideal indicatortaxon. In
additionto establishingthestrengths
and weaknessesof
tigerbeetlesas indicators,thisprocedurecan be used as
a gauge againstwhich to judge the usefulnessof other
potentialindicatortaxa.

Methodsand Materials
StableTaxonomy
To quantifythe concept of "stable,"we chose fiverelativelyrecent and broad taxonomic revisionsof tiger
beetlesand calculatedthepercentofspecies/subspecies
names that had been eliminated throughsynonymy
fromthose in originalor previous studies.The monographsselected were revisionsof (1) the genus Cicindela (sensu lato) fromAustralia(Freitag1979), (2) the
familyCicindelidaeon the island of New Guinea (Cassola 1987), (3) the familyCicindelidaeon the island of
Sumatra(Wiesner 1986), (4) thegenusCicindela (s. 1.)
on the Indian subcontinent (Acciavatti & Pearson
1989), and (5) the familyCicindelidae on the Indonesian islandof Sulawesi(Cassola 1991).
Biologyand LifeHistory
to quantitatively
Althoughit is difficult
establishwhich
taxa have well-knownbiology and naturalhistory,the

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378

Pearson& Cassola

BeetleDiversity

breadthofstudieson tigerbeetle adultsand larvaefrom

around the world would serve as an indicationof the
level of thisknowledge.
FieldObservations
and Experimentation
To illustratehow readilyand accuratelytigerbeetles
can be surveyed,we chose seven sitesforwhich there
are at least fiveyearsof exhaustivestudiesof tigerbeetles (three tropicalforestsites:La Selva,Heredia,Costa
Rica;Pakitza-Manu NationalPark,Madrede Dios, Peru;
Tambopata,Madre de Dios, Peru; a desert grasslandpond edge habitatnear Willcox,Arizona,U.S.A.;a salt
marsh-oceanbeach area near Puerto Pefiasco,Sonora,
Mexico; and an open forestand a riparianhabitatnear
Bangalore,Karnataka,India). These sitesincludea wide
rangeof habitatsthatrepresentthe most simpleto the
most complex and heterogeneoushabitatsin which tiWe have studiedthesebeeger beetles occur naturally.
the
tlesintensively
duringtheperiod ofgreatestactivity,
early rainyseason, at each of these sites (Pearson &
Mury1979; Pearson 1980, 1984; Ganeshaiah& Belavadi
1986). We determinedthe numberof species of tiger
beetles foundwithinthe firstcumulative50 hours of
fieldstudiesduringperiodsin which tigerbeetles could
be expected to be active,in moistsubstratewithwarm,
sunnyperiods.Then we determinedthe numberof additionalspecies foundin the subsequent 200 to 5000
hoursoffieldworkconductedduringtheseason oftiger
beetle activity.
To establish how readily untrainedpersonnel can
learnto accuratelyobserve and surveythese beetles in
the field,the firstauthorworkedwith biologyand entomologystudentswho had no previous experience
with tigerbeetles.As a partof conservationworkshops
in India, Peru, Bolivia, Ecuador and Brazil,these studentswere takento a fieldsite in which thefirstauthor
had recentlydeterminedthe numberof species of tiger
beetles. For 2-4 hours the studentswere shown the
microhabitatsin which tiger beetle adults occurred,
theirflightpatterns,foragingbehavior,and generalnatural history.Each of the studentsthenwent on the site
alone. Theywere asked to collect as manyof the tiger
beetle species as theycould findin two hours. Their
collectionwas thencomparedto the numberofspecies
predeterminedby the firstauthor.
BreadthofHabitatsand Geographical
RangefortheFamily
As an indicationof how widely the familyof tigerbeetles ranges geographicallyand over habitattypes,we
used publishedhabitatdata.As an indicationofthegeowe used regionaland local
graphicalrangeofthefamily,
publications together with our own unpublished
recordsfromaround the world to determinethe total
numberofspecies now knownworld-wideas well as the
numberofspecies knownforeach of as manycountries

of the world as possible. As an additionalcomparison

thathelped controlfordifferences
in the size of countries,we calculated the numberof km2per species for
each country.Low numbersindicate high diversityof
species (wide rangeofhabitatsand biogeographicinfluences) and highnumbersindicatelow diversityof species (few habitats,extremehabitattypes,and in a few
cases perhaps insufficient
fieldwork). We also calculated how manyof these species were endemic to each
country.
Althoughseldom of biological significance,
the number of species withinpoliticalboundariesnot onlyindicates the world-widedistributionof the family,but it
can also be a significant
parameterformakingconservationdecisions.In addition,thenumberofspecies that
are restrictedto theconfinesofpoliticalboundariescan
be usefulinformation
forconvincingnonbiologistdecision makersofconservationprioritiesthatinvolvetheir
politicalunits.To show one way in which thesespecies
numberdata could be usefulin developinga listofpriorityareas forconservation,we rankedin descending
orderthe 75 countrieswithendemic species. By distinguishingnonendemic species shared between these
countriesand thencalculatinga cumulativetotalnumber of species,we determinedthe countriesexhibiting
the greatestendemismas well as contributing
the most
to globaltigerbeetle species diversity
(Collins & Morris
1985).
Of more biological significance,
an understandingof
distributions
of species numberswithinbiogeographic
regionsand habitattypesalso has broad implicationsfor
basic and conservationresearch.Identifying
patternsof
biodiversityand theircauses can provide insightinto
species co-occurrenceand the evolutionof community
structure(Ricklefs1987) as well as provide a preliminarybasis upon which priorityareas for conservation
can be determined(Kuliopulos 1990). Usingpublished
data and specimensin privateand public collections,we
determinedthe total number of species occurringin
each of eleven biogeographicalzones of theworld (Nearctic,includingmostofMexico; Neotropics;Palearctic,
includingAfricanorthof the Sahara; Ethiopian;Madagascar;Indiansubcontinent;China,includingMongolia,
Korea and Japan; Indomalaysia;New Zealand; PapuaOceania; and Australia).Fromour knowledgeofthe historyoftigerbeetle studyas well as thediversityoflikely
tigerbeetle habitatsyet unstudiedin each area,we estimatedhow manymore undescribedspecies are likely
presentin each zone. We also judged how reliableis the
numberof species now knownfromeach biogeographical area.
ofSpecies
HabitatSpecialization
To establishthe degree ofhabitatspecializationof tiger
beetle species,we used datafromecological studiesthat

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Pearson& Cassola

BeetleDiversity

quantifiedhabitatuse among tigerbeetle species. We

also determinedthepercentofhabitatspecialistsversus
generalistsas reportedin broader naturalhistory,systematic,and ecological publications on tiger beetles
fromAustralia(Freitag 1979), southeastPeru (Pearson
1984), southwesternU.S.A.(Knisley & Pearson 1984),
and the Indian subcontinent(Acciavatti & Pearson
1989).
withOtherTaxa
BiologicalPatterns
Correlated
and temperPreviousstudiesin tropical,semi-tropical,
ate areas indicatethata square 275 km on a side is an
area withinwhich one or two intensivecollectionsof
of the entire
tigerbeetles is likelyto be representative
square (Pearson & Ghorpade 1989). We griddedNorth
line (eviAmericasouth of the near-surface
permafrost
dentlybecause larvaltigerbeetles cannotoverwinterin
thissoil, tigerbeetles are absentnorthof thisline) and
the Indiansubcontinentinto squares 275 km on a side.
Because tigerbeetle faunasfromAustraliaare less well
known,we increaosed
the size of the squares to 350 km
on a side. Usingregionalpublications,taxonomicrevisions, and privatefieldnotes,we determinedthe total
number of tiger beetle species within each of these
squares.To bettervisualizepatternsof species richness
at a continentallevel, we produced isoclines by connectingthe approximatecenter of squares in the grid
thathad similarnumbersof species.
To test the generalityof these patternsof diversity,
we comparedthe numberof tigerbeetle species to the
totalnumberof terrestrial
(nonaquatic and nonmarine)
breedingbird species (Pizzey 1980; Ali & Ripley1987;
NationalGeographicSociety1987) and also,forAustralia and NorthAmerica,thenumberofbreedingbutterfly
species (Common & Waterhouse 1982; Scott 1986)
knownfromeach of these squares.We calculated correlationcoefficients
betweenpairsoftaxa foreach continentalarea.
PotentialEconomicImportance
Althoughnormallynot considered of great economic
importance,as predatorstigerbeetles in some habitats

379

could be preadaptedto help controlpest species of arthropods.

Results
StableTaxonomy
The totalnumberofspecies oftigerbeetles in theworld
now standsat 2028, includingsome as of yet unpublished names.Amongthe fivesystematicrevisionsanalyzed forspecies name stability,a total of 406 species
names (with some duplication of species between
Sumatra,Sulawesi,and India and between Australiaand
New Guinea),or 20.3% oftheworld'stigerbeetle fauna,
are represented(Table 1). Of these406 species,only 11
(2.4% ) were lost throughsynonymy.
The numberofnew species describedin each ofthese
revisions also indirectlyaffectsthe interpretationof
these quantifications
of stability.Because no authority
has yethad the chance to considerthe newlydescribed
species forsynonymy,
the numberof newlydescribed
species in each revisionis pertinent(Table 1).
As a frameof reference,birds are among the most
taxonomicallystable groups at the species level. Revisions fromeven the most poorly-studiedregions,such
as SouthAmerica(Ridgely& Tudor 1989), seldom have
more than2% loss of species throughsynonymy.
Biologyand LifeHistory
A preliminary
list of articlesdealingwith tigerbeetles
has been publishedin two parts(Larochelle 1980a,b).
Ofthese909 papers,over 85% includesome lifehistory
or biology of larvae or adult beetles. A more recent
review(Pearson 1988) summarizesthe extensivebiology knownforspecies of thisfamily.
FieldObservations
andExperimentation
The firstcumulative50 hours of collecting,including
thebiologicallyand physicallycomplex rainforestfield
stations,revealed 78-93% of the tigerbeetle faunafor
each of the seven sites(Table 2). In the additional200
to 5000 hoursof surveywork duringtimesofpotential
beetle activity,
onlytwo to fivespecies were added, and

Table 1. The numberand percentofsynonimized

speciesand thenumberofnewlydescribedspeciesin fiveregionalsystematic
revisionsoftigerbeetles.

Australia(Freitag 1979)
Sumatra(Wiesner 1986)
New Guinea (Cassola 1987)
Indiansubcontinent(Acciavatti&
Pearson 1989)
Sulawesi(Cassola 1991)

Number of
species
considered

Number

% of total

Number of newly
describedspecies

29
65
99

8
1
1

21.6
1.5
1.0

0
24

151
82

1
0

0.6
0

24
26

Names synonymized

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380

BeetleDiversity

& Cassola
Pearson

Table 2. The numberofspeciesoftigerbeetlesfoundwithin

thefirst50 hoursofeffort,
and thenumberofadditionalspeciesfoundin
subsequenthoursof searchat sevenfieldsites.
Numberof species withinfirst50 h
(% of total)
Puerto Peniasco, Sonora, Mexico
La Selva, Heredia, Costa Rica
Pakitza (Manu), Madre de Dios, Peru
Tambopata, Madre de Dios, Peru
Willcox, Arizona, U.S.A.
Bangalore, Karnataka, India (scrub forest)
Bangalore, Karnataka, India (riparian)

Number of species added subsequently

(total additional hours)

7(88)
7(78)
20(80)
27(93)
20(95)
9(100)
10 (83)

these tended to be rare species at the limit of their

geographicalrange(Cicindela wickhamiW. Hornnear
Willcox,Arizona) or arborealspecies (Ctenostoma and
Iresia on the Neotropical forestsites) that are most
readilycollected with special techniquessuch as beating foliageand foggingthe canopywith insecticide.
In addition,the time to trainstudentassistantsadequatelyto observe and collect tigerbeetle specimensis
muchless thanthatforothertaxa.To adequatelytraina
novice studentto observe and identifybirds in these
Amazonianforestswould take severalyears;forbutterfliesit would take several months.In the conservation
workshops,80% of the studentswere trainedwithin4
hoursto findat least 90% of the species oftigerbeetles
on the studysite.
BreadthofHabitatsand Geographical
RangefortheFamily
In a world-widestudyof habitattypeand chemicaldefense,83 species were examined.They occurredfrom
alpinemeadows to desertgrasslandsto tropicalrainforests (Pearson et al. 1988).
By geographical region, the number of species is
greatestin the Neotropics,Ethiopian,and Indomalaysia
areas (Fig. 1). The totalnumberof tigerbeetle species

1 (> 200)
2 (> 1000)
5 (> 200)
2 (> 500)
1(> 5000)
0 (> 1000)
2 (> 500)

and the numberof species whose range is completely

restrictedto thatcountryare listed for 129 countries
(Table 3). By politicalboundaries,Madagascarhas the
greatestnumberofendemicspecies (174), and Indonesia has thehighesttotalnumberofspecies (219). India,
with 193 species, has the second highesttotalnumber
in theworld,butwitha land area of3,287,590km2 ithas
5.6 timesthearea ofMadagascar(587,041 km2) and 1.7
timesthe area of Indonesia (1,904,569 km2). Brazil is
thirdin both total numberof species and numberof
endemic species.
The seven countrieswith the highestamountsof endemic species containa totalof 1014 species (Table 4),
halfthe describedspecies in theworld.Ifthe next nine
countriesare included, 75% of all the species in the
world are represented.The 40 highestcountries togethercontainmore than95% of all the describedspecies in the world, and a minimumof 75 countriestogethercontainthe whole world's tigerbeetle fauna.
Comparisonto a similarstudyon swallow-tailedbutterflies(Papilionidae) (Collins & Morris 1985) shows
thatseven of the top ten countriesforendemic species
are sharedby tigerbeetles,and fiveofthe top ten countriesfortotalnumberof species are shared.
HabitatSpecialization
ofSpecies

4000

~ ~ ~~ ~ ~ ~ ~ ~ ~~~~~

Km

~0

(top number),estimatedtotal numbereventuallyto

be described,and theassessmentofprecision of estimate (a = excellent; b = good; c = poor) for each
of 11 biogeographicalareas.

Studiesof tigerbeetle habitatuse inJapan(Hori 1982),

India (Ganeshaiah& Belavadi 1986), and theU.S. (Shelford1912; Willis 1967; Knisley1984; Schultz& Hadley
1987) all indicaterelativelynarrowadaptationby adults
and larvae. Mechanismsfor these adaptationsinclude
morphology(Pearson & Mury 1979; Schultz& Hadley
1987), physiology(Hadley et al. 1990), and behavior
(Knisley& Pearson 1981; Pearson& Lederhouse1987).
Of 151 species of the genus Cicindela (s. 1.) on the
Indian subcontinent,only one species, C flavomaculata Hope, tends to occur in several distincthabitat
types(Acciavatti& Pearson 1989). Of the 20 species in
the Sulphur SpringsValley of southeasternArizona,
U.S.A.,onlyone species, C nigrocoeruleaLeconte,regularlyoccurs in more than one distincthabitat type
(Knisley & Pearson 1984). Of the 29 species in the

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& Cassola
Pearson

BeetleDiversity 381

Table3. Totalnumberoftigerbeetlespeciesknownfromwithin
thepoliticalboundariesofselectedcountries,
thenumberofspecies
endemicto each country,
and theratioofsurfacearea to totalnumberofspecies.
Total number
of species

Numberof
endemic
species

% Endemic

Area
(Ki2)

Km2Ispecies

29
116
111

0
57
45

0
49
40

9,976,140
1,972,550
9,372,610

344,004
17,004
84,438

64
86
184
6
42
38
11
74
17
23

11
21
97
1
7
1
4
19
1
1

17
24
51
17
16
3
36
26
6
4

2,780,090
1,098,580
8,511,970
756,630
1,138,910
51,100
110,920
283,560
21,041
108,890

43,438
12,774
46,260
126,105
27,116
1344
10,084
3831
1296
4734

& Suriname)

29

17

448,793

15,476

DominicanRep.)
Honduras
Jamaica
Nicaragua
Panama
Paraguay

9
7
4
24
28
38
79
4
17
51

3
1
0
0
4
3
14
1
0
8

33
14
0
0
14
8
18
25
0
16

76,190
112,088
10,990
139,000
75,650
406,750
1,285,215
5128
177,510
912,050

8465
16,012
2747
5791
2702
10,703
16,268
1282
10,441
17,883

19
5
15
9
11
7
4
9
4
15
6
5
14
6
7
30
11
9
17
6
4
23
14

0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
5
0
0
1
1
0
2
3

0
0
7
0
0
0
0
0
0
0
0
0
0
0
0
17
0
0
6
17
0
9
21

649,970
28,750
2,381,740
83,850
110,910
9250
43,070
1,002,000
337,030
543,990
356,130
244,030
131,940
36,150
93,030
1,648,000
438,446
20,770
301,250
1,759,540
315
1,565,000
458,730

34,208
5749
158,782
9317
10,082
1321
10,767
111,333
84,257
36,266
59,355
48,806
9424
6025
13,290
54,933
39,859
2307
17,720
293,256
79
68,043
32,766

10
10

0
0

0
0

16
10

1
0

6
0

NEARCTIC

Canada
Mexico
U.S.A.
NEOTROPICAL

Argentina
Bolivia
Brazil
Chile
Colombia
Costa Rica
Cuba
Ecuador (with Galapagos Is.)
El Salvador
Guatemala

Guyanas (Fr. Guiana, Guyana,

Hispaniola (Haiti and

Peru

Trinidad& Tobago
Uruguay
Venezuela
PAIAEARCTIC

Afghanistan
Albania
Algeria
Austria
Bulgaria
Cyprus
Denmark
Egypt
Finland
France
Germany
GreatBritain
Greece
Holland
Hungary
Iran
Iraq
Israel
Italy
Lybia
Malta
Mongolia
Morocco
Norway
Poland
Portugal
Romania
Saudi Arabia
Spain
Syria

4
7

0
0

0
0

324,220
311,730
92,020
237,500
2,153,170

81,055
44,532
9202
23,750
239,241

185,180

18,518

504,750

31,546

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382

BeetleDiversity

Pearson& Cassola

Table3. Continued.
Total number
of species

Sweden
Switzerland
Tunisia
Turkey
U.S.S.R.
Yemen
Yugoslavia
ETHIOPIAN
Angola
Benin
Botswana
BurkinaFaso
Burundi
Cameroon
Cent.AfricanRepublic
Chad
Congo
Ethiopia
Gabon
Gambia
Ghana
Guinea
Guinea Bissau
Guinea (Equatorial)
Kenya
IvoryCoast
Liberia
Malawi
Mali
Mauritania
Mozambique
Namibia
Niger
Nigeria
Senegal
SierraLeone
Somalia
SouthAfrica
Sudan
Tanzania
Togo
Uganda
Zaire
Zambia
Zimbabwe
MADAGASCAR
Comores Is.
Madagascar,Glorieuses&
Juande Nova Is.
MauritiusIs.
ReunionIs.
SeychellesIs.
ORIENTAL-AUSTRALIAN
Australia
Bangladesh
Bhutan
Burma(Myanmar)
Cambodia
China(PRC)
Fiji

Number of
endemic
species

% Endemic

Area
(Ki2)

Km2ispecies

4
7
14
25
49
10
9

0
0
1
4
4
1
0

0
0
7
16
8
10
0

442,750
41,290
163,610
779,450
22,274,900
482,680
255,800

110,687
5899
11,686
31,178
454,590
48,268
28,422

69
14
27
11
6
43
46
16
27
51
11
13
12
20
34
9
53
21
10
36
16
13
47
31
10
24
33
25
31
94
32
68
24
33
134
53
53

23
0
1
0
0
5
3
0
0
8
0
0
0
0
0
0
9
1
0
0
1
0
7
2
0
0
0
0
12
40
0
8
1
0
27
2
4

33
0
3
0
0
12
6
0
0
16
0
0
0
0
0
0
16
5
0
0
6
0
15
6
0
0
0
0
39
43
0
12
4
0
20
4
8

1,246,700
112,620
600,370
274,200
27,830
470,200
622,980
1,284,000
342,000
1,221,900
267,670
11,290
238,540
245,860
36,120
28,050
582,640
322,460
111,370
118,480
1,240,140
1,030,700
799,380
824,280
1,267,000
923,770
196,190
71,740
637,660
1,221,040
2,505,810
939,700
56,600
235,880
2,344,880
746,250
389,300

18,068
8044
22,235
24,927
4638
10,934
13,543
80,250
12,666
23,958
24,333
868
19,878
12,292
1062
3116
10,993
15,355
11,136
3291
77,508
79,284
17,008
26,589
126,700
38,490
5945
2870
20,570
12,990
78,306
13,819
2358
7147
17,499
14,080
7345

2170

1085

176
3
4
1

174
2
3
0

99
67
75
0

587,040
1860
2512
410

3335
621
628
410

81
53
22
93
33
94
2

72
2
0
12
0
16
1

88
4
0
12
0
17
50

7,617,930
133,910
47,000
657,740
176,520
9,326,410
18,270

94,048
2527
2136
7072
5349
99,217
9136

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Pearson
& Cassola

BeetleDiversity 383

Table3. Continued.

India (with Andaman&

NicobarIs.)
Indonesia
IrianJaya
Java
Kalimantan
Sulawesi
Sumatra
Other
Japan
Korea(N. & S.)
Laos
Malaysia
Peninsular
Borneo
Nepal
New Caledonia
New Zealand
Pakistan
Papua New Guinea
Philippines
Solomon Islands
Sri Lanka
Taiwan
Thailand
Vanuatu
Vietnam
WesternSomoa

Total number
of species

Numberof
endemic
species

% Endemic

193

82

42

3,287,590

17,034

53
45
42
81
67
25
22
15
59

22
8
2
58
8
5
4
0
3

42
18
5
72
12
20
18
0
5

410,650
132,200
534,890
159,000
472,610
195,219
372,540
219,360
230,800

7748
2937
12,735
1962
7053
7808
16,933
14,624
3912

47
73
64
17
14
33
72
94
20
55
26
102
3
93
2

3
19
4
16
14
1
45
74
11
32
9
20
0
25
1

6
26
6
94
100
3
62
79
55
58
35
19
0
27
50

327,810
198,210
140,800
17,400
269,060
796,100
451,710
298,170
27,540
64,740
36,180
511,770
12,190
325,360
2840

6974
2715
2200
1023
19,218
24,124
6273
3172
1377
1177
1391
5017
4060
3498
1421

Tambopata ReservedZone, Madre de Dios, Peru, only

one species, Odontocheila annulicornis Brulle,occurs
in more thanone foresthabitattype(Pearson 1984). Of
29 species ofthegenusCicindela (s. 1.) in Australia,
two
species,C mastersiCastelnauand C semicinctaBrulle,
occur over severalhabitattypes(Freitag 1979).
withOtherTaxa
BiologicalPatterns
Correlated
The numberof species of birds,butterflies,
and tiger
beetles foundwithineach square are indicatedon the
respectivegrids(Figs. 2, 3, 4, 5). Isoclines connecting
squares of similartigerbeetle species numberson the
gridded maps for NorthAmerica (Fig. 6), the Indian
subcontinent(Fig. 7), and Australia(Fig. 8) emphasize
areas of highand low species richness(Myers 1990).
Correlationsby gridsquares withineach continental
area resulted in a significant(p < 0.01) relationbetweentigerbeetle and breedingbirdspecies numbersin
NorthAmerica,the Indian subcontinent,and Australia
(Fig. 9). For NorthAmericaand Australiathe correlations between tigerbeetle and butterfly
species numbers (Fig. 10) as well as between butterfly
and bird
species numbers(Fig. 11) were also all significant
(p <
0.01).

Area

(KM2)

Km2/species

Potential
EconomicImportance
There is a growinginterestin thesenaturalpredatorsas
controlsofcertaincrop pests(Hudson et al. 1988, Pearson 1988). Preliminary
studies in India and Peru indicate that some species common in rice paddies may
proveto be effective
controlsofricepests(A. Marmolof
the UniversidadNacional de la AmazoniaPeruana,Iquitos; and G. K Veeresh of the Universityof Agricultural
Sciences,Bangalore,personalcommunication).

Discussion
Insectsas models or indicatorsforconservationbiology
have manyadvantagesover othertaxa (Rosenberget al.
1986; Wilson 1988; Forney& Gilpin 1989; Samways
1989; Viejo et al. 1989; Lockwood & DeBrey 1990).
Because of theirwell-knownbiology and systematics
and theiraestheticqualities,butterflies
have served as
the most widely-usedinsect group for conservation
studies(Pyle et al. 1981; Collins & Morris1985; Brown
1991; Thomas 1991). To answersome questions,howinsecttaxa such as tigerbeetles maybe
ever,alternative
more appropriate.
Our studyindicatesthateven withincreasingquantificationand analysisof criteria,an indicatortaxon is

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384

BeetleDiversity

Pearson& Cassola

Table4. Analysis
ofcriticaltigerbeetlefaunasoftheworld
(totalnumberof
(afterCollinsand Morris1985). A = country
species);B = numberof endemicspecies;C = nonendemic
speciesnotoccurring
in previouscountries;
D = newly
speciesnumber.
accountable
species;E = cumulative
A
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
29.
30.
31.
32.
33.
34.
35.
36.
37.
38.
39.
40.
41.
42.
43.
44.
45.
46.
47.
48.
49.
50.
51.
52.
53.
54.
55.
56.
57.
58.
59.

Madagascar (176)
Indonesia (217)
Brazil (184)
India (193)
Philippines (94)
Australia (81)
Mexico (116)
U.S.A. (111)
Papua New Guinea (72)
South Africa (94)
Sri Lanka (55)
Zaire (134)
Vietnam (93)
Angola (69)
Malaysia (95)
Bolivia (86)
Thailand (102)
Ecuador (74)
China (94)
New Caledonia (17)
Peru' (79)
New Zealand (14)
Somalia (31)
Burma (Myanmar) (93)
Argentina (64)
Solomon Islands (20)
Kenya (53)
Taiwan (26)
Venezuela (51)
Tanzania (68)
Ethiopia (51)
Mozambique (47)
Colombia (42)
Iran (30)
Cameroon (43)
Guyanas (29)
U.S.S.R. (C.I.S.) (49)
Panama(28)
Turkey (25)
Zimbabwe (53)
Cuba (11)
Japan (22)
Nepal (64)
Morocco (14)
Central African Republic (46)
Laos (59)
Paraguay (38)
Hispaniola (9)
R&union Island (4)
Namibia (31)
Zambia (53)
Bangladesh (53)
Mongolia (23)
Mauritius Island (3)
Costa Rica (38)
Ivory Coast (21)
Italy (17)
Spain (16)
Algeria (15)

174
1(03
97
82
74
72
57
45
45
40
32
27
25
23
22
21
20
19
16
16
14
14
12
12
11
11
9
9
8
8
8
7
7
5
5
5
4
4
4
4
4
4
4
3
3
3
3
3
3
2
2
2
2
2
1
1
1
1
1

2
114
87
88
2
4
58
24
1
52
0
90
29
8
3
21
15
19
31
0
1
0
11
2
8
0
7
2
12
11
4
9
1
17
6
0
10
4
4
2
2
1
0
4
2
0
0
0
0
3
0
0
0
0
8
2
2
2
2

176
217
184
170
76
76
115
69
46
92
32
117
54
31
25
42
35
38
47
16
15
14
23
14
19
11
16
11
20
19
12
16
8
22
11
5
14
8
8
6
6
5
4
7
5
3
3
3
3
5
2
2
2
2
9
3
3
3
3

176
393
577
747
823
899
1014
1083
1129
1221
1253
1370
1424
1455
1480
1522
1557
1595
1642
1658
1673
1687
1710
1724
1743
1754
1770
1781
1801
1820
1832
1848
1856
1878
1889
1894
1908
1916
1924
1930
1936
1941
1945
1952
1957
1960
1963
1966
1969
1974
1976
1978
1980
1982
1991
1994
1997
2000
2003

Table 4.

Continued.

A
60.
61.
62.
63.
64.
65.
66.
67.
68.
69.
70.
71.
72.
73.
74.
75.

1
1
1
1
1
1
1
1
1
1
1
1
1
1
0
0

1
1
1
0
0
0
0
0
0
0
0
0
0
0
3
1

2
2
2
1
1
1
1
1
1
1
1
1
1
1
3
1

2005
2007
2009
2010
2011
2012
2013
2014
2015
2016
2017
2018
2019
2020
2023
2024

Togo (24)
Tunisia (14)
Fiji (2)
Pakistan (33)
Guatemala (23)
Botswana (27)
Mali (16)
El Salvador (17)
Yemen (10)
Honduras (7)
Chile (6)
Lybia (6)
Trinidad & Tobago (4)
Western Samoa (2)
Guinea-Bissau (34)
Uganda (33)

Four species of unknown origin (Odontocheila iodopleuroides

Mandl, LangeafleutiauxiW Horn, TrichotaeniaafricanaCassola, and
CicindelajavetiChaudoir) are not included in this table.
ultimately selected on the basis of compromise. For instance, compared to the numbers of butterfly and bird
species per grid square, the small numbers of tiger beetle species is likely to result in some loss of detail in
constructing patterns of species richness, especially at
higher latitudes. Also, in the correlations between tiger
beetle, butterfly, and bird species, the comparisons using butterflies did not reach an asymptote as rapidly as
those using tiger beetles. On the basis of these two criteria, butterflies could logically be judged a more appropriate indicator taxon.
At the Tambopata site in Madre de Dios, Peru, however, it took less than 50 hours of observation to find
93% of the tiger beetle fauna (29 species). In the same
area, it took nearly a thousand hours of work to find

59

69

694

566

97
64
1

92
68
2

85
57
2

77

95
3

10
4

50

78

36
70
43
1

41
30
1

49
9 4 919 913 717
98
33 3
67
672 5 9
661
0
3
5
0
L1
10
1 08 1 04
9
99
56
77
67
62
64
67
1
4
6
5
_2_ 2
10 2 88
98 1 1 01013 13
66
92
7 7 74
72
64
5
3
6
1
2
6
103
116
108 101
1214
1 03 1018786
97
8
6
5
9
8
88
90
1 06
101
92
87
1
1 10
12 31 1 33
923 11 S7 1 10
9
7
6

590

22
2

32

6 99
96
9
42
46
3
0
0
0
7
79 6
50
59
2
2
77
83
97
99
4 9
64
5
2
1
0
2
5
18
99
96
03
83
62
74
2
5
1
9

5 1
40
1

17
5
30
1
92
55
1

9~~~~~~~~~~~6
93
61
3

95
60
2

59
7
2

9 95 9 6 9
4 6 45
22
31
31
18
0
5
0
0
72
66
34
34
1
0
38
5
87
52
2
9
5

99

Figure 2. Total number of breeding (nonmarine,

nonaquatic)
bird (top number), butterfly (middle
number), and tiger beetle species (bottom number)
occurring within each square (275 km per side) on a
grid

across

northern

North

America

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BeetleDiversity

Pearson& Cassola

1 29
1 21
10
1 24
1 05
0

14
11 5
9
13013
1 26 11 6
9
10
141 126
1 30 1 23
11
10
1 38
1 33
14
1 31
1 24
11
11 3
1 25
13

12 136
1 15 1315
10
9
1 25 1 25
106 1 23
0
0
1 20 1 30
99
1 29
9
13
1 20 1394
1 00 1 43
10
14
1 3 4140
1 26 140
11
16
1 0 7140
1 061 170
7
108
-

2156 0.87
0

90
1 02
16

124
141
7
124
140
11
1 36
14 0
16
14 3
14 5
13
1 44
1 65
22
1 40
1 62
10

90
11
1 04
11l3
12
108
1 17
999
1 29 1 29
2 0
12
00879
1 14
1 51 1 20
108
212
1 2088 37
1 70 1 07
17
222
1 22
91
1 73
96
22
222
657
1 15
140
03
21
212
1 19
647
77
1 60
17
19

1 30
15

1 311212

3 131
1301
95
9

1 19

1_
139
814
19

1 60
60 20
22

I112
1 47
16

115
1 10
14

919
98
91 1103
16
17

03
1 05
14

122
06
9

112
017
8

1125
92119
i1717
90
11i9 -1 07'
16
12
12
90
1 00
11 7
100
11 6
1 261
15
13
15
908111
93
1 191
908 1 05
14
20
16
1 08
90
100
91
1 11
1 131
23
15
13
9 3 1 06
1 06
1 23
99
12 1
14
19
12
09
1 05
100
1 07 1 19
1 171
20
7
17
93
99
969
1 30 1 31
1 241
21
15
17
1 03
1 51
231
93
11 5
1 77 1 27
24
23

03
70
17
91
01
17
01
20
70
01
23
00
00
23
72
05
21
70
02
13
1 01
1 10
1

105
71
6

10 5
68

1 07
64

1 02
67

1 09
77
5

164
69
18

11 8
119
79
04
6 .6,

11 1
21
1616
9111 97
1 03 ~,,9
09
13
1
1 1;1
1/2
1 26
-~1oC 9;21
1
17
121
1515 112 11 9
13
1
108
_I3
12 2
115 11 6 -12 4 1 24
1 11 1 10
119 115
1 21
17
108
14
14
15
1103
1 00
1 05 1 32 1 12
1 24 1 15
140
118105
I
16
16
12
15
16
1 21 10 1
1 05
.0
107
11 1 1 23 13 3
14
14
13
12
19 9
99
100 100
7130
1616 121 1 33
1 5 1 5/16
15
05
91
91
1 31
112 112
14
10
108
06
13 5
9
02
07
13 0
1 20
14
17

172
61
17

1 9104
300
18

139
9

1 39
44
3

161
101
19
1 83
58
7

3
147
4 9
4

6
53
53
5

1
12
4

103
1
1

1 07
3

1 23
21
3

1 49
33
5

2
1395
1 0

6
3

10
21
2

1 04
13
1

11 0
13
0

1 13
17
2

1 08
34
2

1 07
20
0

1 20
2 6
2

1 45
47
2

207
17
1

122
7
3

122
13
5

118
12
2

122
13
1

122
14
2

121
16
2

122
19
4

131
2
4

139
7
4

177
83
5

197
176
9

1 40
3 4
9

1 20
13
7

1 21
13
4

1 15
14
1

11 9
14
0

11 9
15
1

1 23
19
8

11 8
21
4

1 34
34
4

1 73
66
3

20 8
1 83
6

1 32
19
9

1 29
28
10

1 41
3 4
6

1 49
36
4

21 1
1 41
4

206

194

1 79

76

98

115

19

11 7

140

1 60

21

29

43

(nonmarine,
Figure3. Total numberof bree%dfingv
(middle
nonaquatic) bird (top numbe'r),butterfly
beetlespecies (bottom number)
numbe'r),and tigrer
withineaCh"square (275 kmper side) on a
occurringr
southernNorthAmerica
across
grid

201
206
2
1
234
211
24

1 3
63
5

103
25
14

1 20
9 7
15

172
114
17

385

78
4 7

30K4

35OK~~~~~~~~3

88
1 55
16

~~~~~~~~~~1

126
3 9
3

75

Figure5. Total numberof breeding(nonmarine,

nonaquatic) bird (top number),butterfly
(middle
number),and tigerbeetlespecies (bottom number)
90% ofthebutterfly
species (over 1200 species and still
occurringwithineach square (350 km per side) on a
with
subsequent visits,even -aft-er grid across Australia
rising significantly
more thantenyearsof collecting)(Lamas 1981, 1983).
Even when the focus of the surveywas narrowedto
are severe the advantagesofworkingwithtigerbeetles
familieswithinthe order of Lepidopteraat Tambopata
offsetthe disadvantages.
percentof
(Lamas 1984), the time to finda significant
In addition,the habitatspecializationof these tiger
the faunawas extensive.Likewise,the birdlist of more
beetle
species and their presence in the predator
than560 species forthisarea is one thatnecessitatedat
trophic
level make it likelythattheyare highlysuscepseasons of the
least several years of work in different
tible
to
habitatchanges. Paradoxically,this specializayear to approach 90% (T. A. Parker,III, personal comalso
makes possible the survivalof viable population
munication).In termsof riskanalysis,when timelimits
tionsin remnantpatchesofundisturbedhabitat.Species
261

1 7 r-326

2 24

5
1 74

119

3
1 10

1 24

1 45
4

1 20
/i

140

13 7

1 3

33

105

-7
_10

-15 3

2 9

397

490
41

38

1 2 9166
1

106

1 14

ii

34 1

374
5

410
14

156816

25

4
16 9

179

24

17 5

1 78

1 81

18 720

11

17

155

193

184

181

193

1 74

1 81

2 11

53 3

58

51

46

1 65

53 7

5 16

4 5

19S

3
20

4,1,-

12

9'
344
1 8

10~~~~~~~~1

20 8
2 3

2 1

2 31

171

187

19 6

33

14

1 5

20

2 47

177

3 9

24

15

T~~~~~~1

15<1

2 32

173

48

27

275

2 25

19 3

30

5 1

Km

Fig,ure4. Total numberof breeding(nonmarine,

nonaquatic) bird (top number) and tig,erbeetlespecies (bottom numbwer)
occurringwithineach square
(275 km per side) on a grid across theIndian subcontinent

20

<1~~~~~~~~~1
Figure 6 Isoclines connectingapproximate centers
of squares withsimilar numbersof tigerbeetlespecies in NorthAmerica

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BeetleDiversity

386

Pearson& Cassola

160
160
r

10

NORTH AMERICA
*

20
30
15

120

~~~~~~~~~40
-

j !

10

40

10

10
15

200
V0.
E*

205

*S

30C

~N=208

-!4
40

30

20

= 0.375
~~~~~~~~~~~R

.
*

* .*
g

80 -

>50~

150 -

100

*
.

15
20
AUSTRALIA

25

.
. .

R = 0.531
N = 67

*P

P < 0.01

40

>50

4030

Figure 7. Isoclines connectingapproximate centers

of squares withsimilar numbersof tigerbeetlespecies on theIndian subcontinent

10

450050

15
NDIA

20

25
*

R = 0.726
N = 61
P <0.01

*
0

in west Texas, U.S.A.(Gage 1988), along the northeastern seaboard of the UnitedStates(Knisleyet al. 1987),
and in Italy (Cassola 1972) occur in areas of undisturbed remnanthabitatas small as a few hectares.In
manypartsofAmazonia,in which onlysmallpatches of
originalforestremain,manybird (Bierregaard& Love(Lovejoy et al. 1984) species are
joy 1989) and butterfly
no longer able to maintainviable populations.Insects
like tigerbeetles are likelyto maintainviable popula-

300
150 .-

.1.

12

24

36

48

60

NUMBER OF TIGER BEETLE SPECIES

PER SQUARE

Figure9. Correlationbetweenthe numberof tiger

beetleand bird speciesper square on grids across
NorthAmerica,Australia,and theIndian subcontinent

20
5

20

>350 Km1

Figure 8. Isoclines connecting approximate centers

of squares with similar numbers of tiger beetle species in Australia

tionsin much smallerpatches of remnantforests.They

lend themselvesas an indicatortaxonforstudiesundertakento understandthegeneraldistribution
and dynamics of recent historicaldistributionin the face of the
disappearanceof a largeproportionofhabitatand populations(Murphyet al. 1990).
Apartfromregionalstudiesofbiodiversity,
tigerbeetles mayalso be ofuse as an indicatortaxon forstudies
ofunique and threatenedhabitats.Because of extensive
historicalcollections and records that document the
presence and decline of manyspecies associated with
changes in habitatand human impact (Nagano 1982;
Desender & Turin 1989), studies of tigerbeetles may
in at least two ways to enhance
functionsignificantly
thisarea ofconservationbiology.First,the U.S. Fishand
WildlifeServiceis consideringseveralendemic species
oftigerbeetles in Florida,Maryland,
Texas, and Idaho as

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Pearson
& Cassola

BeetleDiversity 387

NORTH AMERICA
180

120

1iI

NORTH AMERICA
0

160

*~**~*

80 -

N
X

60 .113j.:||!R-7

R = 0.772
= 67
P < 0.01

~~~~~~~~~~~~~N

..

...R=0.755

P<0*01
N=20 ..8
.... ....

*t*

40

l.|.|.@

P <0.01

0
0.4

10

15

20

AUSTRALIA

35

25

uz

180

::

= 67
p < 0.01

60

*
.

* .3|.

0.8755
= 208
~~~~~~~N
0

00i2

....

~~~~~~~R
- 0j873

p < 0.01

0
20
5
10
15
NUMBER OF TIGER BEETLE SPECIES
PER SQUARE

25

Figure 10. Correlation between the number of tiger

beetle and butterflyspecies per square on grids
across North America and Australia

endangeredspecies and has alreadydeclared two species, C dorsalis dorsalis Say and C puritana G. Horn, as

threatened(Federal Register1990). This statuswill in

turnbringprotectionto other invertebrateand vertebrate species associated with the habitatsof these endemic tigerbeetles.
Second, several groups of insectshave been used to
documentlongterm(20-100 years) changesin habitats
(Turin & den Boer 1988; van Swaay 1990; Dennis &
Shreeve 1991). In manyareas the uncomplicatedmonitoringof common tigerbeetle species over long periods makesthema usefulindicatorof the disappearance
of species,which can in turnbe associatedwithhuman
impact and the rate of habitat degradation (Wilson
1970; Cassola 1974, 1983; Knisley 1979; Shook 1981;
Nagano 1982; Schultz 1988; Tanner 1988; Desender &
Turin 1989).

210

R =

0
0

175

100
6

140

200

150

120

.t

105

~~~~~AUSTRtALIA

= 0.582
R
N

70
V

oz1580

It is in evaluationsofbiodiversity,
however,thattiger
beetles reach some of theirhighestpotentialas an indicator taxon.Politiciansand scientistslargelyagree that
priorityareas forconservationmustbe identified,
espeifpreservationand rationalecociallyin tropicalforests,
nomicuse ofmanyareas throughouttheworld are to be
accomplished (Vane-Wrightet al. 1991). Recentlyin

40
NUMBER

80

120

OF BUITERFLY
PER SQUARE

160

200

SPECIES

Figure 11. Correlationbetweenthe numberof butterflyand bird speciesper square on grids across
NorthAmerica and Australia
Manaus,Brazil,a meetingof manyof the active biological researchersin the Amazon soughtto establishthe
relativelysimpledistribution
ofpocketsofhighand low
species numbersforvariousplantand animaltaxa across
thebasin.Usingthesedata,an initiallistofpriorityareas
forconservationcould be established,with those areas
exhibitinghighspecies numbersacrossmanytaxa ofthe
highestpriority.Some accord was reached (Kuliopulos
1990), but formosttaxa,highdiversitywas oftenassociatedwiththepresenceofa biologicalfieldstation.It is
unclearwhethermanyofthe intervening
areaswithrelativelylow species numbersactuallyhad fewspecies or
were simplyunderstudied.
To determinevalid patternsof species richnessfor
taxa such as birdsor butterflies
acrosstheAmazonBasin
would take decades. Tiger beetles, on the otherhand,
could yield such patternsin fiveyears(Pearson 1992).
Applyingthe quadrate squares, 275 km per side, used
forNorthAmericaand the Indian subcontinent,one or
two intensive collections within each of about 70
squareswould be the minimumeffort
needed (McKenzie et al. 1989; Owen & Owen 1990). These patternsof
species richness togetherwith phylogenetic (Wiley
1981), biogeographical (Haffer 1969; Endler 1977;
Cracraft1986), and ecological studies(Holloway &Jar-

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388

BeetleDiversity

dine 1968; Pearson 1986; Brown 1988) could thenbe

used to distinguishhistoricalcentersof evolutionand
speciationas the highestpriorityforconservation(Erwin 1991) in a relativelyshorttime.

Acknowledgments
R. L. Huber, R. Naviaux,W. D. Sumlin,and J. Wiesner
generouslyprovided data on tigerbeetle species numbers fromvariouspartsof theworld.Earlydraftsof this
article were criticallyreviewed by G. E. Ball, K Desender,J.A. Endler,T. L. Erwin,R. L. Huber,C. B. Knisley,R. F. Noss,R. L. Rutowski,M.J.Samways,A. T. Smith,
and W. D. Sumlin.Pearson'sfieldworkwas supportedby
grantsfrom ConservationInternational,the National
GeographicSociety,the National Science Foundation,
the SmithsonianInstitution(BIOLAT and PL-480), and
the World WildlifeFund.
Literature
Cited
Acciavatti,R. E., and D. L. Pearson. 1989. The tigerbeetle genus Cicindela (Coleoptera, Insecta) fromthe Indian subcontinent.Annalsof CarnegieMuseum 58:77-353.
Ali,S., and S. D. Ripley.1987. Compact handbookof the birds
ofIndiaand PakistantogetherwiththoseofBangladesh,Nepal,
Bhutanand Sri Lanka. 2nd Edition.OxfordUniversityPress,
Oxford,England.
Bierregaard,
R. O., Jr.,and T. E. Lovejoy. 1989. Effectsofforest
fragmentation
on Amazonianunderstorybird communities.
ActaAmazonica19:215-241.
Brown,J.H. 1988. Species diversity.Pages 57-87 in A.A. Myers and P. Giller,editors.AnalyticalBiogeography:an integratedapproachto the studyofanimaland plantdistributions.
Chapmanand Hall, Routledge,England.
Brown,K S., Jr. 1991. Conservationof neotropicalenvironments:insects as indicators.Pages 349-404 in N. M. Collins
and J.A. Thomas, editors.Conservationof insects and their
environments.
Academic Press,London,England.
Cassola, F. 1972. Studi sui Cicindelidi.VII. Un interessante
repertonella Lagunadi Orbetello:Cephalota (Taenidia) circumdata leonschaeferiCassola (Coleoptera). AttiSocieta Toscana di Scienze Naturali,Memorie(B) 72:92-96.
Cassola,F. 1974. Studisui Cicindelidi.XI. Validit'aspecificadi
Cicindela majalis Mandl,e problemidi conservazionedegli
ambientigolenali italiani(Coleoptera). Lavor Societa Italiana
di Biogeografia(N. S.) 4:57-75.
Cassola, F. 1983. Studi sui Cicindelidi.XXXIII. Note e osservazionisu un interessanteendemitasiciliano:Lophyridiaaphrodisia panormitana (Ragusa) (Coleoptera Cicindelidae). II
NaturalistaSiciliano7:41-56.
Cassola, F. 1987. Studisui cicindelidi.LI. I Cicindelidae(Coleoptera) della Nuova Guinea.Annalidel Museo Civico di Storia Naturaledi Genova 86:281-454.

Pearson& Cassola

Cassola, F. 1991. Studi sui Cicindelidi.LXIII. I Cicindelidae

(Coleoptera) dell'Isola Sulawesi,Indonesia.Annalidel Museo
Civico di StoriaNaturaledi Genova 88:481-664.
Collins,N. M.,and M. G. Morris.1985. Threatenedswallowtail
butterflies
of the world. IUCN Red Data book. IUCN, Gland,
Switzerland.
Common,I. B. F., and D. F. Waterhouse. 1982. Butterfliesof
Australia-Field Edition.Angus and Robertson,London, England.
Cracraft,
J. 1986. Originand evolutionof continentalbiotas:
speciationand historicalcongruencewithintheAustralianavifauna.Evolution40:977-996.
den Boer, P.J. 1990. The survivalvalue of dispersalin terrestrialarthropods.Biological Conservation54:175-192.
Dennis,R. L. H., and T. G. Shreeve.1991. Climaticchange and
the Britishbutterfly
fauna:opportunitiesand constraints.Biological Conservation55:1-16.
Desender,K, and H. Turin.1989. Loss ofhabitatsand changes
in thecompositionofthegroundand tigerbeetle faunain four
west Europeancountriessince 1950 (Coleoptera: Carabidae,
Cicindelidae). Biological Conservation48:277-294.
Ehrlich,P. R.,and E. 0. Wilson. 1991. Biodiversity
studies:science and policy.Science 253:758-762.
Endler,J.A. 1977. Geographicvariation,speciation,and clines.
Monographsin PopulationBiology,no. 10. PrincetonUniversityPress,Princeton,New Jersey.
Erwin,T. L. 1991. An evolutionary
basis forconservationstrategies. Science 253:750-752.
Federal Register.1990. Endangeredand threatenedwildlife
and plants;determination
of threatenedstatusforthe Puritan
Beach TigerBeetle. Federal
TigerBeetle and theNortheastern
Register55:32088-32094.
Forney,K A.,and M. E. Gilpin.1989. Spatialstructureand populationextinction:a studywithDrosophila flies.Conservation
Biology3:45-51.
Freitag,R. 1979. Reclassification,
phylogenyand zoogeographyof the Australianspecies of Cicindela (Coleoptera: Cicindelidae). AustralianJournalof Zoology (SupplementarySeries) 66:1-99.
Gage,E. V. 1988. A new subspeciesofCicindelapolitula from
New Mexico and a range extension for Cicindela politula
barbaraannae (Coleoptera: Cicindelidae). Entomological
News 99:143-147.
Ganeshaiah,K M., and V. V. Belavadi. 1986. Habitatsegregation in fourspecies of adult tigerbeetles (Coleoptera; Cicindelidae). Ecological Entomology11:147-154.
Hadley,N. F., C. B. Knisley,T. D. Schultz,and D. L. Pearson.
1990. Water relations of tiger beetle larvae (Cicindela
marutha): correlationswith habitatmicroclimateand burrowingactivity.JournalofAridEnvironments
19:189-197.
Haffer,
J. 1969. Speciationin Amazonianforestbirds.Science
(Washington,D.C.) 165:131-137.

ConservationBiology
Volume 6, No. 3, September1992

This content downloaded by the authorized user from 192.168.72.229 on Mon, 19 Nov 2012 15:02:38 PM
All use subject to JSTOR Terms and Conditions

Pearson& Cassola

BeetleDiversity

Holloway,J.D., and N. Jardine.1968. Two approachesto zooof butterflies,

geography:a studybased on the distributions
area. Proceedingsof the
birdsand bats in the Indo-Australian
LinneanSocietyof London 179:153-188.
oftwo species oftiger
Hori,M. 1982. The verticaldistribution
with
beetlesat Sugadaira(Mt. Neko-Dake),NaganoPrefecture,
special reference to their habitat preferences. Cicindela
14:19-33.
Hudson,W. G.,J.H. Frank,and J.L. Castner.1988. Biological
controlof Scapteriscusspp. mole crickets(Orthoptera:Gryllotalpidae) in Florida.Bulletinofthe EntomologicalSocietyof
America34:192-198.
Hunter,M. L.,Jr.,G. L. Jacobson,Jr.,and T. Webb, III. 1988.
Paleoecology and the coarse-filterapproach to maintaining
biological diversity.ConservationBiology2:375-385.
abundanceand seasonalityof
Knisley,C. B. 1979. Distribution,
tigerbeetles (Cicindelidae) in the Indiana Dunes region.Indiana Academyof Sciences 88:208-217.
Knisley,C. B. 1984. Ecological distributionof tiger beetles
(Coleoptera: Cicindelidae) in Colfax County,New Mexico.
SouthwesternNaturalist29:93-104.

389

Larochelle,A. 1980b. A preliminary

listofpapers dealingwith
the tigerbeetles (Coleoptera: Carabidae: Cicindelini) of the
world.PartII. Cordulia6:61-73.
Lockwood,J.A., and L. D. DeBrey. 1990. A solution for the
sudden and unexplained extinctionof the Rocky Mountain
grasshopper(Orthoptera:Acrididae).Environmental
Entomology 19:1194-1205.
Lovejoy,T. E.,J.M. Rankin,R. 0. Bierregaard,
Jr.,K S. Brown,
Jr.,L. H. Emmons,and M. Van der Voort. 1984. Ecosystem
decay of Amazon forestremnants.Pages 295-325 in M. H.
of Chicago Press,ChiNitecki,editor.Extinctions.University
cago, Illinois.
Maguire,L. A. 1991. Riskanalysisforconservationbiologists.
ConservationBiology5:123-125.
McKenzie,N. L., L. Belbin,C. R. Margules,and G.J.Keighery.
1989. Selectingrepresentativereservesystemsin remote areas: a case studyin the Nullarborregion,Australia.Biological
Conservation50:239-261.
Morris,M. G.,and W. E. Rispin.1988. A beetle faunaof Oolitic
limestonegrassland,and the responses of species to conservation managementby different
cuttingregimes.Biological
Conservation43:87-105.

Knisley,C. B., and D. L. Pearson. 1981. The functionof turret

buildingbehaviourin the larvaltigerbeetle,Cicindela willistoni (Coleoptera: Cicindelidae). Ecological Entomology
6:40 1-410.

Murphy,D. D., and S. B. Weiss. 1988. Ecological studies and

theconservationoftheBaycheckerspotbutterfly,
Euphydryas
editha bayensis.Biological Conservation46:183-200.

oflarval
Knisley,C. B., and D. L. Pearson. 1984. Biosystematics
tigerbeetles of the SulphurSpringsValley,Arizona.Transactionsof the AmericanEntomologicalSociety110:465-551.

Murphy,D. D., K E. Freas,and S. B. Weiss. 1990. An environment-metapopulation

approachto populationviabilityanalysis
fora threatenedinvertebrate.
ConservationBiology4:41-51.

Knisley,C. B.,J.I. Luebke,and D. R. Beatty.1987. Naturalhistoryand populationdecline of the coastal tigerbeetle,Cicindela dorsalis dorsalis Say(Coleoptera: Cicindelidae).Virginia
Journalof Science 38:293-303.

Myers,N. 1990. The biodiversity

challenge:expandedhot spot
analysis.The Environmentalist
10:243-256.

Science (WashKuliopulos,H. 1990. Amazonianbiodiversity.

ington,D.C.) 248:1305.
Lamas,G. 1981. La faunade mariposasde la Reservade Tambopata,Madre de Dios, Peru. Revistade la Sociedad Mexicana
de Lepidoptera6:23-40.
Lamas,G. 1983. Adicionesy correccionesa la listade mariposas de la Reservade Tambopata,Peru. Revisitade la Sociedad
Mexicana de Lepidoptera8:13-24.
Lamas,G. 1984. Los Papilionoidea(Lepidoptera) de la Zona
Reservadade Tambopata,Madrede Dios, Peru.I: Papilionidae,
Pieridaey Nymphalidae(En parte). RevistaPeruana de Entomologia 27:59-73.

Nagano,C. D. 1982. Populationstatusof the tigerbeetles of

thegenusCicindela (Coleoptera: Cicindelidae) inhabitingthe
marineshorelineof SouthernCalifornia.Atala8:33-42.
NationalGeographicSociety.1987. Field guide to the birdsof
North America. National Geographic Society, Washington,
D.C.
Noss, R. F. 1990. Indicatorsformonitoringbiodiversity:a hierarchicalapproach.ConservationBiology4:355-364.
Owen, D. F., and J. Owen. 1990. Assessing insect speciesrichnessat a singlesite.Environmental
Conservation17:362364.
Palmer,M. K 1978. Growthrates and survivorshipof tiger
beetle larvae.Cicindela 10:49-66.

Landres,P. B., J. Verner,and J.W. Thomas. 1988. Ecological

uses of vertebrateindicatorspecies: a critique.Conservation
Biology2:316-328.

in tropical
Pearson,D. L. 1980. Patternsof limitingsimilarity
foresttiger beetles (Coleoptera: Cicindelidae). Biotropica
12:195-204.

listofpapers dealingwith
Larochelle,A. 1980a A preliminary
the tigerbeetles (Coleoptera: Carabidae: Cicindelini) of the
world. PartI. Cordulia 6:25-60.

Pearson,D. L. 1984. The tigerbeetles (Coleoptera: Cicindelidae) of the TambopataReservedZone, Madre de Dios, Peru.
RevistaPeruanade Entomologia27:15-24.

ConservationBiology
Volume 6, No. 3, September1992

This content downloaded by the authorized user from 192.168.72.229 on Mon, 19 Nov 2012 15:02:38 PM
All use subject to JSTOR Terms and Conditions

390

BeetleDiversity

Pearson& Cassola

Pearson, D. L. 1986. Communitystructureand species cooccurrence: a basis for developing broader generalizations.
Oikos 46:419-423.

Samways,M.J.1990a Landformsand winterhabitatrefugiain

the conservationof montanegrasshoppersin SouthernAfrica.
ConservationBiology4:375-382.

Pearson,D. L. 1988. Biologyoftigerbeetles.AnnualReviewof

Entomology33:123-147.

Samways,M.J. 1990b. Insect conservationethics. EnvironmentalConservation17:7-8.

Pearson,D. L. 1992. Tiger beetles (Coleoptera: Cicindelidae)

as indicatorsforbiodiversitypatternsin Amazonia.National
GeographicResearchand Exploration8:116-117.

Schultz,T. D. 1988. Destructiveeffectsof off-road

vehicleson
tigerbeetle habitatin centralArizona.Cicindela 20:25-29.

Pearson,D. L., and K D. Ghorpade.1989. Geographicaldistributionand ecological historyof tigerbeetles (Coleoptera: Cicindelidae) of the Indian subcontinent.Journalof Biogeography 16:333-344.
Pearson,D. L., and R. C. Lederhouse. 1987. Thermalecology
and the structureof an assemblageof adult tigerbeetles (Cicindelidae). Oikos 50:247-255.
Pearson,D. L.,and E. J.Mury.1979. Characterdivergenceand
convergenceamong tigerbeetles (Coleoptera: Cicindelidae).
Ecology 60:557-566.
Pearson,D. L., M. S. Blum,T. H. Jones,H. M. Fales, E. Gonda,
and B. R. Witte.1988. Historicalperspectiveand the interpretationof ecological patterns:defensivecompounds of tiger
beetles (Coleoptera: Cicindelidae). American Naturalist
132:404-416.
Pizzey,G. 1980. A fieldguide to the birdsofAustralia.Collins,
Sydney,Australia.
Pyle,R.,M. Bentzien,and P. Opler. 1981. Insect conservation.
AnnualReview of Entomology26:233-258.
R. E. 1987. Communitydiversity:
Ricklefs,
relativeroles of local and regional processes. Science (Washington, D.C.)
235:167-171.

Schultz,T. D., and N. F. Hadley.1987. Microhabitatsegregation

and physiologicaldifferences
in co-occurringtigerbeetle species, Cicindela oregona and Cicindela tranquebarica Oecologia (Berlin) 73:363-370.
Scott,J.A. 1986. The butterflies
of NorthAmerica.Stanford
University
Press,Stanford,
California.
V. E. 1912. Ecological succession.BiologicalBulletin,
Shelford,
Woods Hole, Massachusetts23:331-370.
Shivashankar,
T., A. R.V. Kumar,G. K Veeresh,and D. L. Pearson. 1988. Angularturret-building
behavior in a larval tiger
beetle species fromsouth India (Coleoptera: Cicindelidae).
ColeopteristsBulletin42:63-68.
Shook,G. 1981. The statusof the ColumbiaTiger Beetle (Cicindela columbica Hatch) in Idaho (Coleoptera: Cicindelidae). Pan-PacificEntomology57:359-363.
Tanner,0. 1988. Of tigerbeetles and wedge mussels:protecting ConnecticutRiverriches.Nature ConservancyMagazine
38:4-11.
Thomas,C. D. 1991. Habitatuse and geographicrangesofbutterfliesfromthe wet lowlandsof Costa Rica. Biological Conservation55:269-281.

Ridgely,R. S.,and G. Tudor. 1989. The birdsofSouthAmerica,

Vol. 1. University
of Texas Press,Austin,Texas.

Turin,H., and P.J.den Boer. 1988. Changesin the distribution

of carabidbeetles in the Netherlandssince 1880. II. Isolation
of habitatsand long-termtime trendsin the occurrence of
carabidspecieswithdifferent
powersofdispersal(Coleoptera,
Carabidae). Biological Conservation44:179-200.

Rosenberg,D. M., H. V. Danks,and D. M. Lehmkuhl.1986. Importanceof insectsin environmentalimpactassessment.EnvironmentalManagement10:773-783.

USDI. 1980. Habitatevaluationprocedures(HEP). Ecological

servicesManualNumber102. DivisionofEcological Services,
U.S.D.I.Fish and WildlifeService,Washington,D.C.

Rushton,S. P., M. D. Eyre,and M. L. Luff.1990. The effectsof

scrubmanagementon the groundbeetlesofOolitic limestone
grasslandat CastorHanglandsNationalNatureReserve,CamU.K Biological Conservation51:97-111.
bridgeshire,

van Swaay,C. A. M. 1990. An assessmentof the changes in

abundance in the Netherlandsduringthe 20th cenbutterfly
tury.BiologicalConservation52:287-302.

Samways,M.J. 1988. Classical biological control and insect

Conservaconservation:are theycompatible?Environmental
tion 15:349-354.
Samways,M.J. 1989. Insect conservationand landscape ecolofbushcrickets(Tettigoniidae)in southern
ogy:a case-history
France.Environmental
Conservation16:217-226.

R. I., C. J. Humphries,and P. H. Williams.1991.

Vane-Wright,
What to protect?-systematicsand the agonyof choice. Biological Conservation55:235-254.
Viejo, J.L., M. G. de Viedma, and E. MartinezF. 1989. The
importanceof woodlands in the conservationof butterflies
(Lep.: Papilionidaeand Hesperioidae) in the centreofthe IberianPeninsula.Biological Conservation48:101-114.

ConservationBiology
Volume 6, No. 3, September1992

This content downloaded by the authorized user from 192.168.72.229 on Mon, 19 Nov 2012 15:02:38 PM
All use subject to JSTOR Terms and Conditions

Pearson
& Cassola

BeetleDiversity 391

Webb, N. R. 1989. Studies on the invertebratefaunaof fragmented heathiandin Dorset, U.K, and the implicationsfor
conservation.Biological Conservation47:153-165.

Willis,H. L. 1967. Bionomicsand zoogeographyof tigerbeetlesof salinehabitatsin the centralUnitedStates(Coleoptera:

Cicindelidae). Universityof Kansas Science Bulletin47:145313.

Wiesner,J. 1986. Die Cicindelidaevon Sumatra.9. Beitragzur

Kenntnisder Cicindelidae (Coleoptera, Cicindelidae). MitteilungenMunchenerEntomologischeGesellschaft76:5-66.

Wilson,D. A. 1970. Threesubspeciesofcicindelidsthreatened

withextermination.
Cicindela 2:18-20.

Wiley,E. 0. 1981. Phylogenetics:the theoryand practice of

phylogeneticsystematics.
JohnWileyand Sons,New York.

Wilson,E. 0. (editor). 1988. Biodiversity.NationalAcademy

Press,Washington,D.C.

/i

-~~~T

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