Butterflies and Plants: A Study in Coevolution

Transcription

Butterflies and Plants: A Study in Coevolution
Author(s): Paul R. Ehrlich and Peter H. Raven
Reviewed work(s):
Source: Evolution, Vol. 18, No. 4 (Dec., 1964), pp. 586-608
Published by: Society for the Study of Evolution
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BUTTERFLIES
AND PLANTS: A STUDY IN COEVOLUTION'
PAUL R. EHRLICH AND PETER H. RAVEN
Departmentof Biological Sciences,Stanford University,Stanford,California
AcceptedJune 15, 1964
One of the least understoodaspects of plantswiththe hope of answeringthe folpopulation biology is communityevolu- lowinggeneralquestions:
tion-the evolutionaryinteractionsfound
experi1. Withoutrecoursetolong-term
kindsor organismswhere mentationon singlesystems,what can be
amongdifferent
amongthe learnedabout the coevolutionary
exchangeof geneticinformation
responses
kindsis assumedto be minimalor absent. of ecologicallyintimateorganisms?
evolutionhave, in
Studies of community
aboutcomgeneralities
2. Are predictive
general,tendedto be narrowin scope and
to ignorethe reciprocalaspects of these munityevolutionattainable?
interactions.Indeed, one group of orga3. In the absenceof a fossilrecordcan
nismsis all too oftenviewed'as a kind of the patternsdiscoveredaid in separating
physicalconstant.In an extremeexample therateand timecomponents
of evolutiona parasitologistmight not consider the arychangein eitheror bothgroups?
evolutionary
historyand responsesofhosts,
4. Do studiesof coevolutionprovidea
mightaswhilea specialistin vertebrates
reasonable startingpoint for the underparasitesto be
sume speciesof vertebrate
evolutioningeneral?
standingofcommunity
invariateentities. This viewpointis one
factorin thegenerallack ofprogresstoward
FOOD CHOICE
FACTORS DETERMINING
of organicdiversificathe understanding
of
Beforeproceedingto a consideration
tion.
groups
butterfly
between
relationships
the
to
what
we
would
like
One approachto
theworld,
call coevolutionis the examinationof pat- and theirfoodplantsthroughout
some of
consider
to
briefly
is
necessary
it
terns of interactionbetween two major
choice
of
the
determine
that
the
factors
groupsof organismswitha close and eviin
in
and
this
phytophgroup
food
plants
such as plants
dentecologicalrelationship,
and herbivores.The considerableamount agous insects in general. Any group of
animalsmustdraw its food
available about butterflies phytophagous
of information
those
from
plantsthatare available
supply
and theirfood plants make themparticuand ecological range
in
geographical
its
larly suitable for these investigations.
have (Dethier,1954). For instance,the butterFurther,recentdetailedinvestigations
provideda relativelyfirmbasis for state- flies are primarilya tropicalgroup,and
thereis a relativelygreaterutiliof therefore
mentsabout the pheneticrelationships
of
zation
primarilytropicalthan of temthe varioushighergroupsof Papilionoidea
of plants. The choice of
families
perate
It
and
should,
unpubl.).
(Ehrlich, 1958,
that we are con- ovipositionsite by the imago is also imhowever,be remembered
and moths
as a model. They portant.Many adult butterflies
sideringthe butterflies
with
food
certain
on
plants
their
eggs
lay
are onlyone of themanygroupsof herbivMerz
stressed
as
(1959),
by
precision
great
In
with
orousorganisms
plants.
coevolving
therelation- but on the other hand, numerous"misthispaper,we shallinvestigate
ship between butterfliesand their food takes" have been recorded(e.g., Remington, 1952; Dethier,1959). In such cases,
have eitherto findan appropriate
larvae
1 This work has been supported in part by
or
perish. There is an obviousselecplant
GB-123
Foundation
Grants
National Science
tive advantagein ovipositionon suitable
(Ehrlich) and GB-141 (Raven).
EVOLUTION
18: 586-608. December, 1964
586
BUTTERFLIES
plants, but inappropriatechoices can be
overcomeby movement
of thelarvae. Furthermore,larvae feedingon herbs often
consumethe entireplant, and then must
move even if the adult originallymade an
appropriatechoice.
Larval choice therefore
plays an important role in food plant relationships.An
excellentreviewof a long seriesof experimentspertinent
to thissubjecthas recently
been presentedby Merz (1959); muchof
thefollowing
is based on his account. The
conditionof a given larva oftenhas an
effecton what foods it will or will not
accept. In addition,many structuraland
mechanicalcharacteristics
of plantsmodify
theserelationships,
mostlyby limitingthe
acceptabilityof thoseplantsin whichthey
occur. For example,Merz (1959) found
thatlarvaeof Lasiocampaquercus,a moth
that normallyfeeds along the edge of
leaves, could not eat the sharplytoothed
leavesofholly(Ilex, Aquifoliaceae).When
thesesameleaveswerecutso thatuntoothed
marginswere presented,the larvae ate
them,voraciously.In other cases, larvae
eat theyoung,softleaves of plantsbut not
the old, toughleaves of the same plants.
Many Lycaenidae feed on flowers,and
thesebutterflies
may be unable to utilize
the tough foliage of the same plants.
Numeroussimilarexamplescouldbe given,
but it mustbe bornein mindthatchemical
factorsare operativein the same plants
thatpresentmechanicaldifficulties
to larvae (Thorsteinson,1960), and actually
maybe moreimportant.
Chemical factorsare of great general
importancein determininglarval food
choice. In the firstplace, potentialfood
sourcesare probablyall nutritionally
unbalanced to some extent(Gordon, 1961).
The exploitationof a particularplant as
a source of food thus involvesmetabolic
on thepartofan insect.These
adjustments
renderthe insect relativelyinefficient
in
utilizingothersourcesof foodand tendto
restrict
its choiceof foodplants. Secondly,
many plants are characterizedby the
presenceofsecondarymetabolicsubstances.
AND PLANTS
587
These substances are repellentto most
insectsand may oftenbe decisivein patternsof foodplantselection(Thorsteinson,
1960). It has furtherbeen demonstrated
that the chemicalcompoundsthat repel
most animals can serve as triggersubstancesthatinducethe uptakeof nutrients
by membersofcertainoligophagousgroups
1953,
(Dethier,1941, 1954; Thorsteinson,
1960). Presenceof such repellentcomwiththepresence
poundsmaybe correlated
of thenutrients.Both odorand tasteseem
to be important.
ofplantsoften
The chemicalcomposition
changesWithage, exposureto sunlight,or
factors(Merz, 1959;
otherenvironmental
Fliick, 1963), and thismay be criticalfor
insects(Dethier,1954). For
phytophagous
example,insectsthatfeedon Umbelliferae
preferthe old leaves, whichappear to us
less odorous than the youngones. Some
speciesof
insectsthatfeedon alkaloid-rich
Papaver (Papaveraceae) preferthe young
leaves, whichare relativelypoor in alkaloids. Diurnal chemicalcycles,influenced
by exposureof the plant to sunlight,may
the
in determining
be of primeimportance
groups, such as
habits of night-feeding
Argynnini.
Merz (1959, p. 159) has givena particucase of chemicalrepellents
larlyinteresting
at the specificlevel. The larvae of the
moth Euchelia jacobaeae feed on many
species of Senecio (Compositae),but not
S. viscosus.
on the denselyglandular-hairy
was dissubstance
When the glandular
solved in methylalcohol,the larvae ate S.
viscosus. When the same substancewas
painted on the leaves of other normally
acceptable speciesof Senecio, these were
refused.In an extensivestudyof the food
plantsof Plebejus icarioides(Lycaeninae),
Downey (1961, 1962) showedthat larvae
would feed on any species of Lupinus
(Leguminosae) in captivity,but populationsin thefieldnormallyutilizedonlyone
or a fewof the possiblerangeof Lupinus
locally. This worksuggests
speciesgrowing
of ecological,chemithe subtleinteraction
cal, and mechanicalfactorsthat doubtless
588
PAUL R. EHRLICH
AND PETER H. RAVEN
characterizes
mostnaturalsituations.Re- Lycaenidaeabout tied forthird. Difficult
lationships
withpredators(Brower,1958), as this diversity
is to estimate,it is clear
parasites (Downey, 1962), or, at least thatPapilionidaeare a moreheterogeneous
in the case of Lycaenidae,ants (Downey, groupof organismsthan any of the other
1962), may furthermodifypatternsof families,whereas,consideringthe number
foodplant choice.
of speciesand generaincluded,Lycaenidae
Despite all of these modifyingfactors, are remarkably
uniform.A roughidea of
pat- the pheneticrelationshipsof the major
thereis a generaland long-recognized
tern runningthroughthe food plants of groupsof butterflies
is given by Ehrlich
variousgroupsof butterflies,
and it is this (1958).
patternwithwhichwe shall be concerned. Withfoodplantrecordsfrombetween46
It certainlyshould not be inferredfrom and 60% of all butterfly
genera(table 1),
anythingthat followsthat all membersof it seems highlyunlikelythat futuredisa familyor genus of plants are equally coverieswill necessitateextensiverevisions
acceptable to a given butterfly(for ex- oftheconclusions
drawnin thispaper. The
ample, see Remington,1952). We have foodplants of Riodininaeare verypoorly
placed our main emphasis on positive known,however,and it will be interesting
records,especiallyat the level of plant to have moreinformation
about themand
speciesand genera.
recordsforotheroutstanding"unknowns"
suchas Styxand Pseudopontia.It is, however, difficultto imagineany additional
THE DIVERSITY OF BUTTERFLIES
foodplantrecordthatwouldseriouslydiscomprisea singlesuper- tortthe patternsoutlinedhere.
The butterflies
thePapilionoidea.In
familyofLepidoptera,
comparisonwithmanyothersuperfamilies
BUTTERFLY FOOD PLANTS
ofinsectstheyare uniform
morphologically
SourcesofInformation
and behaviorally.Table 1 gives a rough
abstractedin
plantinformation
The
food
idea of the taxonomicdiversityof this
fromtwo
principally
this
is
derived
paper
superfamily.
Papilionoideaare dividedinto fivefam- sources. First,we have examinedall the
ilies. Two of these, Nymphalidae and extensiveand scatteredliteraturethat we
Lycaenidae,containat least three-quarterscould uncoverwith a librarysearch and
of various
of the generaand species; it is uncertain throughthe recommendations
which familyis the larger. Two smaller lepidopterists.Particularlyhelpful have
families,Pieridaeand Papilionidae,include been the volumesof Barrettand Burns
all remaining
butterflies.
Pieridae, (1951), Corbet and Pendlebury(1956),
virtually
manyfewergeneraand Costa Lima (1936), Ehrlichand Ehrlich
althoughcontaining
species than eitherLycaenidae or Nym- (1961), Lee (1958), Seitz (1906-1927),
phalidae, forma prominentpart of the van Son (1949, 1955), Wiltshire(1957),
(1957), as well as the
faunain manypartsof theworld, and Wynter-Blyth
butterfly
makingup in numberof individualswhat Journalof the EntomologicalSociety of
theylack in numberof kinds. Papilionidae South Africa,the Journalof the Lepidopare a groupabouthalfthesize of Pieridae, terists' Society (formerlyLepidopterists'
but gain prominence
throughthelargesize News), and theJournalof Researchon the
of the included forms. The tiny family Lepidoptera.
Libytheidae,closelyrelatedto Nymphali- Our secondmajor sourceof information
exceptbutterfly has been providedby the followingsciendae, is obscureto everyone
tists,who have aided us in thisambitious
taxonomists.
in undertakingnot only by sendingunpubThe Papilionidaelead the butterflies
of theirworks,but
prob- lisheddata and reprints
diversity.
Nymphalidae
morphological
the
to
evaluate
validityof cerPieridae
and
with
helping
by
second
take
place,
ably
BUTTERFLIES
TABLE
Taxon
Papilionidae
Baroniinae
Parnassiinae
Papilioninae
1. Summary of the taxonomicdiversityof Papilionoidea
Approximate number of
Genera*
24(22)
1(1)
8(8)
15(13)
Pieridae
58(40)
Coliadinae
11(8)
Pierinae
43(29)
Dismorphiinae
3(3)
Pseudopontiinae 1(0)
Nymphalidae
Ithomiinae
Danainae
Satyrinae
Morphinae
Charaxinae
Calinaginae
Nymphalinae
Acraeinae
Libytheidae
Lycaenidae
Riodininae
Styginae
Lycaeninae
Total
589
AND PLANTS
575-700
1
45-55
480-640
950-1,150
225-250
650-750
80-120
1
325-400
(ca. 202)
30-40(10)
10-12(10)
120-150
(ca. 70)
23-26(12)
8-10(8)
1(1)
125-150
(ca. 85)
8(6)
4,800-6,200
1(1)
10
325-425
(ca. 167)
75-125(17)
1(0)
250-300
(ca. 150)
730-930
(ca. 432)
Distribution
Species
CentralMexico
Holarcticand Oriental; greatestdiversity,Asia
Worldwide; mainlytropical. Greatestdiversity,Old
World tropics
Cosmopolitan; greatestdiversitytropicsoutsideof Africa
Cosmopolitan; greatestdiversitytropics
PrimarilyNeotropical; one small Palearctic genus
West equatorial Africa
300-400
Neotropical; TellervoAustralian
Cosmopolitan; greatestdiversityOld World tropics
140-200
1,200-1,500 Cosmopolitan; greatestdiversityextratropical
180-250
300-400
1
2,500-3,000
Indomalayan and Neotropical
Tropicopolitan,fewtemperate
Oriental
Cosmopolitan
225-275
Tropical; greatestdiversity,Africa
Cosmopolitan
5,800-7,200
800-1,200 Tropical,fewNearcticand Palearctic. Metropolis,Neotropical
PeruvianAndes
1
5,000-6,000 Cosmopolitan; greatestdiversity,Old World tropics
12,000-15,000
* Number in parenthesesindicatesnumberof generafor which food plant recordsare available.
tain publishedrecordsand commenting
on Iwase (Japan), T. W. Langer (Denmark),
otheraspectsof thework. The cooperation C. D. MacNeill (USA), D. P. Murray
of these people has been trulyextraordi- (England), G. Sevastopulo(Africa), Tanary,and we are particularlyindebtedto kashi Shirozu (Japan), E. M. Shull
them: Remauldo F. d'Almeida (Brazil), (India), Henri Stempffer
(France), V. G.
PeterBellinger(USA), C. M. de Biezanko L. van Someren (Africa), G. van Son
(Brazil), L. P. Brower (USA), C. A. (Africa).
Clarke (England), H. K. Clench (USA),
JohnC. Downey (SouthernIllinoisUniJ. A. Comstock(USA), C. G. C. Dickson versity),GordonH. Orians (Universityof
(Africa), J. C. Downey (USA), Maria Washington),T. A. Geissman(University
Etcheverry(Chile), K. J. Hayward (Ar- of California,Los Angeles),and RobertF.
gentina),T. G. Howarth(England), Taro Thorne (Rancho Santa Ana Botanic Gar-
590
PAUL R. EHRLICH
AND PETER H. RAVEN
den) havebeenso kindas to readtheentire
manuscript.Their advice has been invaluable.
To our knowledge,the data assembled
here representthemostextensivebody of
ever assembledon the interinformation
actionsbetweena majorgroupof herbivorous animalsand theirfoodplants.
ily on broad, repeatedlyverifiedpatterns
of relationship.
The Food PlantsofButterflies
In thissection,we will firstoutlinethe
mainpatternsof foodplantchoiceforeach
and thendiscusswhatbearingthese
family,
of repatternshave on our interpretation
within the various butterfly
lationships
EVALUATION OF THE LITERATURE
families.It is necessaryto give the data
Extremecare has been takenin associat- in considerabledetail,as no comprehensive
ing insectswithparticularfoodplants,as surveyon a worldbasis is available elseis repletewitherrorsand un- where.
theliterature
verifiedrecords. In evaluating records, Papilionidae.-There are threesubfamithe only species
has been given to those which lies. Baronia brevicornis,
preference
are concernedwiththe entirelife cycle of of Baroniinae,occursin Mexico and feeds
a particularinsecton a wildplant. Labora- on Acacia (Leguminosae; Vazquez and
and recordsfromculti- Perez, 1961). In Parnassiinae,all five
tory experiments
vated plants demonstrateonly potentiali- genera of Zerynthiini(Munroe, 1960;
ties, not necessarilynatural associations. Munroeand Ehrlich,1960) feedon Aristolarvaemaybe starvedor lochiaceae,as does Archon (Parnassiini).
In thelaboratory,
plants abnormal.In the wild, larvae are Hypermnestra(Parnassiini) is recorded
(Zygophyllaceae).Parespeciallyif not reared fromZygophyllum
oftenmisidentified,
to maturity(cf. Brower,1958b). Even nassius feedson Crassulaceaeand herbamore seriousis the lack of preciseplant ceous Saxifragaceae,two closely related
withone smallgroupon Fumariaor their identificationin families,
identifications,
the vernacularonly, which almost inevi- ceae. In view of the discussionbelow, it
are close
1932). is of interestthatZygophyllaceae
tablyleads to confusion(Jorgensen,
ani- relativesof Rutaceae,and Fumariaceaeare
Any seriousstudentof phytophagous
mals should preserveadequate herbarium richin alkaloidssimilarto thoseof woody
specimensof the plants withwhichhe is Ranales (Hegnauer,1963).
PapilioniThe thirdand last subfamily,
concerned(cf. Remington,1952, p. 62);
but best developedin
only by doing this can the recordsbe nae, is cosmopolitan
verified. Despite the extremelyerratic theOld World,and consistsof threetribes:
ovipositionbehavioroftenshownby but- Troidini,Graphiini,and Papilionini. The
records eight genera of Troidini feed mostlyon
terflies(Dethier,1959), oviposition
withindividualspeciesof
been accepted as Aristolochiaceae,
have all too frequently
being equivalent to food plant records. Paridesalso recordedfromRutaceae,Meniinclud- spermaceae,Nepenthaceae,and Piperaceae.
difficulties,
Finally,nomenclatural
ing changesin nameand carelessmisspell- Parides (Atrophaneura)daemoniusis reings (e.g., "Oleaceae" forOlacaceae), have portedto feedon Osteomeles(Rosaceae),
givenrise to seriouserrors.In the litera- and P. (A.) antenor,a Malagasy butterfly
of its tribe
foodplants,errorshave that is the only representative
tureon butterfly
oftenbeen compoundedwhencopied from in the Ethiopianregion,feedson Combreonesourceto another,and theyare difficult tum (Combretaceae). Both of theselastto traceback to theirorigins.All of these mentionedrecordsneed confirmation.At
problemsmake quantitativecomparisons least two species of Battus have been rehave been ex- corded fromRutaceae in additiont-othe
unreasonable.We therefore
Records available
ceedingly conservativeabout accepting usual_Aristolochiaceae.
records,and focusedour attentionprimar- for fiveof the seven generaof Graphiini
BUTTERFLIES
AND PLANTS
591
(Eurytides,Graphium,Lamproptera,Pro- ceae, Rutaceae (Ptelea), and Salicaceae
tographium,
Teinopalpus)are mostlyfrom (Brower,1958b).
Annonaceae, Hernandiaceae, Lauraceae,
In Papilionidae, Munroe and Ehrlich
Magnoliaceae,and Winteraceae. This is (1960) have arguedthat the red-tubercuclearly a closely allied group of plant late, Aristolochiaceae-feeding
larvae of
familiesreferableto the woody Ranales. Papilioninae-Troidiniand ParnassiinaeIn addition,somespeciesof Graphiumfeed Zerynthiini,plus Archon (Parnassiinaeon Rutaceae,and othersbothon Apocyna- Parnassini)areso similar,
and thelikelihood
ceae (Landolphia) and Annonaceae (one of theirconverging
on Aristolochiaceae
so
of the latter also on Sphedamnocarpus,remote,that theseprobablyrepresentthe
Malpighiaceae). Several species of Eury- remnantsof the stockfromwhichthe rest
tidesfeedon Vitex(Verbenaceae)and one of Papilioninaeand Parnassiinaewere deon Jacobinia (Acanthaceae). Eurytides rived. Viewed in this contextother food
lysithousfeedsbothon Annonaceaeand on plantsof thesegroupsare secondary.The
Jacobinia,and E. heliosbothon Vitexand tworemaihing
tribesofPapilioninae(PapilMagnoliaceae. The bitypic Palearctic ionini,Graphiini)arelabove all associated
Ipliclides departsfromthe usual pattern with the groupof dicotyledonsknownas
for the groupin feedingon a numberof the woody Ranales. This is a diverse
Rosaceae-Pomoideae.
assemblage of plant families showing
The thirdand last tribe,Papilionini,con- manyunspecializedcharacteristics.
Thorne
sists only of the enormouscosmopolitan (1963) has used the food plant relationgenus Papilio. Two of the five sections shipsof Papilionidaeas a wholeto support
recognizedby Munroe (1960; II, IV) are his suggestionof affinitybetweenAristoprimarilyon Rutaceae, with occasional lochiaceae and Annonaceae (one of the
recordsfromCanellaceae,Lauraceae, and woody Ranales). He appears to have
Piperaceae. Membersof the circumboreal establishedthe existenceof this similarity
Papilio machaon group are not only on on morphological
evidence.Likewise,simiRutaceae but also on Umbelliferaeand lar alkaloidsare sharedby Aristolochiaceae
Artemisia(Compositae). The AfricanP. and woodyRanales (Hegnauer,1963; Aldemodocus,in anothergroup,is knownto stonand Turner,1963,p. 170). Recently,
feed on Rutaceae and Umbelliferae,as Vazquez and Perez (1961) describedthe
the only
well as Pseudospondias (Anacardiaceae), life cycle of Baronia brevicornis,
Ptaeroxylon
(Meliaceae), andHippobromus memberof the third subfamilyof the
(Sapindaceae). AnotherAfricanspecies,P. group. Baronia feedson Acacia (Legumilarvaelikethose
dardanus,is recordedfromRutaceae and nosae) and has tuberculate
also fromXyimalos(Flacourtiaceae;Dick- of the formsthatfeedon Aristolochiaceae.
son,pers. comm.). The Asian and Austra- Consideringits morphological
distinctness,
lian P. demoleusis mostlyon Rutaceaebut and in accordancewiththe schemeof realso locally on Salvia (Labiatae) and lationships presented by Munroe and
Psoralea (Leguminosae). The otherthree Ehrlich (1960, p. 175), it appears likely
line
sections(Munroe'sI, III, V) are primarily thatBaronia represents
a phylogenetic
associated with Annonaceae,Canellaceae, whichdivergedearlyfromthat leadingto
Hernandiaceae,Lauraceae, and Magnolia- the rest of Papilionidae. It may thus be
ceae,witha fewrecordsfromBerberidaceae, the only memberof the familyneither
Malvaceae (TThes
pea), and Rutaceae. The feedingon Aristolochiaceae
nor descended
NorthAmericantemperatePapilio glaucus fromformsthatdid.
group(sect.II) feedsnotonlyon Lauraceae
Followingthisreasoning,
we suggestthat
and Magnoliaceae like its more southern the originaltransitionto Aristolochiaceae
relativesbut also on Aceraceae,Betulaceae, openeda new adaptivezone forPapilioniOleaceae, Platanaceae,Rhamnaceae,Rosa- dae. Their furtherspread and the multi-
592
PAUL R. EHRLICH
AND PETER H. RAVEN
plicationof species was accompaniedby nothingis known of the biology of the
chemi- monobasicWest AfricanPseudopontiinae.
ofotherpresumably
theexploitation
inthree,Dismorphiinae,
cally similarplant groups,such as woody Of the remaining
Ranales, in areas where Aristolochiaceae cluding the NeotropicalDismorphia and
like Africatoday. Pseudopierisand the PalearcticLeptidia,
werepoorlyrepresented,
The site of greatestdiversityfor both are recordedonlyon Leguminosae.Larval
and Papilionidaeis Asia. food plants are known for 7 of the 11
Aristolochiaceae
It is likelytlhatthe major diversificationgeneraof Coliadinae. Catopsilia,Phoebis,
of Papilionidae (involvingdifferentiationAnteos, Eurema, and Colias are mostly
into Parnassiinaeand Papilioninae) took associatedwithLeguminosae,but thereare
placeaftertheevolutionofAristolochiaceae. a fewrecordsfromSapindaceae,Guttiferae,
Oxalidaceae,
When this might have been is entirely Euphorbiaceae,Simarubaceae,
uncertain,despitethe unfoundedspecula- Salicaceae, Ericaceae, and Gentianaceae
and montane
tionsof Forbes (1958).
(the last threewithnorthern
problemis posed by species of Colias). On the other hand,
Anotherinteresting
of Papilioniniand threegeneraareassociatedwithnon-legumithemanyrepresentatives
Graphiinifeedingon Rutaceae,in addition nous plants: Gonepteryxwith Rhamnus
to woodyRanales. Rutaceae are morpho- (Rhamnaceae),NathaliswithCompositae,
fromwoodyRanales, and KricogoniawithGuaiacum(Zygophyllogicallyverydifferent
Leguminosaeare deand have not been closelyassociatedwith laceae). Nonetheless,
them taxonomically.Recently,however, cidedlythe mostimportantfoodplantsof
Hegnauer (1963) has pointed out that Coliadinae.
Pierinae, the third subfamily,are disome Rutaceae possessthe alkaloidswidespreadin woodyRanales,in additionto an vided into two tribes,Pierini (36 genera)
of otheralkaloids. and Euchloini(7). In Euchloini,the temunusuallyrichrepertoire
Earlier,Dethier (1941) showedthe simi- perate Anthocharis, Euchloe, Zegris, and
laritybetweenthe attractantessentialoils Hesperociaris (also from Phrygilantthus,
in Rutaceae and Umbelliferae. Some Loranthaceae) feed on Cruciferae,the
groups of Papilio seem tropical Pinacopteryxand Hebemoia on
Rutaceae-feeding
especially Capparidaceae. For Pierini,14 of the 23
to have shiftedto Umbelliferae,
of the
outside of the tropics. Dethier also im- generaforwhichwe knowsomething
BeleAscia,
Appias,
(namely,
food
plants
species
plicatedsomeof thesimilar-scented
Elodina,
Dixeia,
Colotis,
Ceporis,
nois,
of Artemisia(Compositae),anotherplant
group fed on by at least one species of Eronia, Ixias, Leptosia, Pareronia,Pieris,
on
Papilio. Althoughspecies of Papilio link Prioneris,and Tatolchila)are primarily
thesegroupsof plants,none is knownto Capparidaceaein thetropicsand subtropics
feedon Burseraceae,Cneoraceae,Simaru- and on Cruciferaein temperateregions.
familiesthought Some have occasionallybeen reportedto
baceae,or Zygophyllaceae,
to be relatedto Rutaceae but not known feed on Resedaceae, Salvadoraceae, and
to containalkaloids or coumarins(Price, Tropaeolaceae. There are also a veryfew
1963). On the otherhand, the recordof scatteredrecordsfromotherplants,includon Ptaeroxylon(Melia- ing one or two fromLeguminosae. The
Papilio demaodocus
to numerousRutaceae, basis for selectingCapparidaceae,Crucifin
addition
ceae),
would seem to indicatea promisingplant erae, Resedaceae,Salvadoraceae,and Troeasyto comprehend,
to investigatefor the alkaloids suspected paeolaceaeis relatively
sinceall of theseplantsare knownto con(Price, 1963) in Meliaceae.
Pieridae.-Our discussionof Pieridaeis tainmustardoil glucosides(thioglucosides)
on the genericreview and the associated enzyme myrosinase
based taxonomically
of glucosides
of Klots (1933) as modifiedby Ehrlich whichacts in the hydrolysis
and Turner,
(Alston
oils
mustard
release
to
but
(1958). There are four subfamilies,
BUTTERFLIES
AND PLANTS
593
1963, p. 284-288). In an early series of (Loranthaceae) in South America, and
food choice experiments,VerschaeffeltDelias, a largeIndo-Malaysiangenus,from
(1910) foundthat larvae of Pieris rapae "Loranthus"(Loranthaceae)andExocarpus
and P. brassicaewouldfeedon Capparida- of the closelyrelatedSantalaceae,withD.
ceae, Cruciferae,Resedaceae, and Tro- aglaja on Nauclea (Rubiaceae). Aporia,a
regionsof theOld
paeolaceae,as wellas anotherfamilywhich largegenusof temperate
contains mustard oils but upon which World, has several species on Berberis
Pierinaeare not knownto feedin nature: (Berberidaceae),and one on woodyRosaalso foundthat ceae. Pereute,South American,feeds on
Moringaceae.Verschaeffelt
theselarvaewouldeat flour,starch,or even Ocotea (Lauraceae; Jorgensen,1932),
filterpaper if it was smearedwith juice Tiliaceae, and Polygonaceae. Two very
expressedfromBunias (Cruciferae),and peculiargeneraof theDelias groupare the
Thorsteinson
(1953, 1960) showedthatthe monotypicMexicanEucheira,whichfeeds
larvae would eat other kinds of leaves on woody hard-leavedEricaceae, and the
treatedwithsinigrinor sinalbin(two com- bitypicwesternNorthAmericanNeophasia,
mon mustardoil glucosides)if the leaves whichfeedson variousgeneraof Pinaceae.
that Cepora, which
were not too tough and did not contain It is very interesting
otherkindsof repellents.Veryfewbutter- fallsintotheDelias groupmorphologically,
fliesoutsidePierdinaefeedon theseplants, feedson Capparislike manyotherPierini.
isolated,
Finally,thelarge,taxonomically
but thereis one examplein Lycaeninae.In
feedson Loranthaceae
addition,thereare at least two recordsof EthiopianMylotlhris
Pkoebis (Coliadinae) fromCapparidaceae and Santalaceae (Osyris),withM. bernice
and Cruciferae.Numerousgroupsof in- rubricastaon Polygonum(Polygonaceae).
to understandthe reasons
are character- It is difficult
sects otherthan butterflies
isticallyassociatedwiththissame seriesof for large groups of Pierinae being associated both withplants that possess musplantfamilies(Fraenkel,1959).
It is not so easy to interpretscattered tard oils and with Loranthaceae-Santalanorbiochemical
recordsof thesepierinegenerafeedingon ceae; neither
morphological
on evidencehas been adduced to link these
otherplant families: Belenois raffrayi
Rhus (Anacardiaceae); Nepheroniaargyia two groups of plants. Perhaps the Loon Capparidaceae, but also Cassipourea ranthaceae-feeders
an old offshoot
represent
(Rhizophoraceae)and Hippocratea (Hip- of Pierinae; in any case it would appear
pocrateaceae),withN. thalassinareported that the main diversification
of thisgroup
only fromHippocratea;Ascia monusteon occurredafter it became associated with
Rhamnaceaeand Cassia (Leguminosae),as Capparidaceae-Cruciferae.
wellas Capparidaceae;and Tatochilaautoenormousfamilyis
Nymrphalidae.-This
dice on Cestrum (Solanaceae) and also dividedintoeightsubfamilies
whichwillbe
Medicago' (Leguminosae). Several species discussed one by one in the succeeding
of Appias have been reportedfromdiffer- paragraphs.
ent genera of Euphorbiaceae, whereas
Ithomiinaeare primarilyAmerican,and
others feed both on Capparidaceae and there feed only on Solanaceae (many
Euphorbiaceae,but this probablycan be genera). The Indo-Malaysian Tellervo,
explained somewhat more simply, since onlyOld Worldrepresentative
ofthegroup,
mustardoils have been reportedin some which is segregatedas a distinct tribe
genera of Euphorbiaceae (Alston and Tellervini,has been recordedfromAristoTurner,1963, p. 285).
loclia (Aristolochiaceae).The identityof
The remaininggenera of Pierini fall the plant was inferredfromthe fact that
mostlyintowhathas beencalledtheDelias papilionidlarvae normallyassociatedwith
werefoundon it withTellervo.
group. Of these,Catastictaand Archonias Aristolochia
have been recorded from PhrygilanthusSolanaceae are rich in alkaloids (as are
594
PAUL R. EHRLICH
AND PETER H. RAVEN
Aristolochiaceae),and are very poorly
Closely related to Morphinae are the
representedamong the food plants of more temperateSatyrinae,an enormous
as a whole. The diversificationgroup that feeds mostly on Gramineae
butterflies
of the ithomiinesthat feed on themhas (includingbamboos and canes) and Cyprobably followeda pattern similar to peraceae,occasionallyon Juncaceae.Pseuthat of Papilionidae on Aristolochiaceae donymphavigilansfeedson Restio (Resand Pierinaeon Capparidaceae-Cruciferae.tionaceae), a familyclose to Gramineae,
Many othergroupsof insectsfeedprimar- Physcaneurapione on Zingiberaceae,and
ilyon Solanaceae (Fraenkel,1959).
Elymniason Palmae. Thereare no records
Danainae are a ratheruniformcosmo- of thisgroupfromdicotyledons.Thus the
politan group,obviouslyrelated to Itho- pheneticallysimilar Morphinae-Satyrinae
miinae. The danaines feed primarilyand assemblageis the outstandingexamplein
on Apocynaceae butterflies
interchangeably
apparently
of a groupassociatedprimarily
and Asclepiadaceae.In addition,thereare withmonocotyledons.
Charaxinae
tropicopolitan
The distinctive
recordsofEuploea,Ituna,and Lycorellaon
Moraceae and of the last occasionallyon are oftenassociated with woody Ranales
Carica (Caricaceae). All of these plants (Annonaceae, Lauraceae, Monimiaceae,
have milkyjuice. There is also a single Piperaceae), but also with such diverse
record of Ituna ilione, which normally families as Anacardiaceae, Araliaceae
feedson Ficus (Moraceae), fromMyopo- (Schefflera),Bombacaceae, Celastraceae,
rum (Myoporaceae). Apocynaceae and Connaraceae,Convolvulaceae,EuphorbiaAsclepiadaceaeforma virtualcontinuum ceae, Flacourtiaceae,Hippocrateaceae,LeLinaceae,Malvaceae,Meliaceae,
in their pattern of variation and can guminosae,
scarcelybe maintainedas distinct(Safwat, Melianthaceae, Myrtaceae, Proteaceae,
1962). Both are notedfortheirabundant Rhamnaceae, Rutaceae, Salvadoraceae
bitterglycosidesand alkaloids(Alstonand (Charaxes hansali), Sapindaceae, SterTurner,1963, p. 258), and share at least culiaceae, Tiliaceae, Ulmaceae, and Versome alkaloids (Price, 1963, p. 431) and benaceae. Records (largely Sevastopulo
pyridineswithMoraceae. Thus it appears and van Someren,pers. comm.) are availverylikelythatheretoo theacquisitionof able for about 50 African species of
the ability to feed on Apocynaceaeand Charaxes, most of which are associated
Asclepiadaceae has constitutedfor Da- with dicotyledons.At least threefeed on
nainae the penetrationof a new adaptive grasses(Gramineae),twooftheseon dicotzone,in whichtheyhave radiated.Numer- yledonsalso.
The OrientalCalinaga buddha,the only
ous distinctivesegmentsof other insect
ordersand groupslikewisefeed on these species of Calinaginae, feeds on Morus
(Moraceae).
twoplantfamilies.
ElevengeneraofMorphinaeare recorded Nymphalinaeare a huge cosmopolitan
froma varietyof monocotyledons:Bro- groupwith relativelyfew "gaps" in their
meliaceae, Gramineae(mostlybamboos), patternofvariationwhichwouldpermitthe
Marantaceae,Musaceae,Palmae,Pandana- recognitionof meaningfulsubgroups(cf.
1950). The tribes
ceae, and Zingiberaceae.In contrast,most Reuter,1896; Chermock,
patspecies of Morplhofeed on dicotyledons, do, however,displaysome significant
including Canellaceae, Erythroxylaceae,ternsintheirchoiceoffoodplants,withHelLauraceae,Leguminosae,Menispermaceae, iconiini (Michener,1942) and Argynnini
Myrtaceae,Rhamnaceae,and Sapindaceae, feedingmostlyon the Passifloraceae-FlabutM. aega feedson bamboos(Gramineae) courtiaceae-Violaceae-Turneraceaecomand M. herculeson Musaceae. Whether plex of families,a closely related group
of Morphofedon dicotyle- of plants also importantfor Acraeinae.
theprogenitors
dons or monocotyledonscannot be de- Acraeinae (see below), Heliconiini,and
are closelyrelatedphenetically,
Argynnini
termined.
BUTTERFLIES
AND PLANTS
595
may have taken Melastomaceae,Melianthaceae,Menisperand theirdiversification
place froma commonancestorassociated maceae, Myrtaceae,Oleaceae, Ranunculawith this particularassemblageof plants. ceae (Vanessa on Delphinium),RhamnaNo biochemicalbasis is known for the ceae, Rosaceae, Rubiaceae, Sabiaceae,
association of this series of four plant Salicaceae,Sapotaceae,Saxifragaceae,
Sterpredictthat culiaceae, Thymeleaceae,Tiliaceae, and
families,but we confidently
one eventuallywill be found (cf. also Vitaceae.
Gibbs, 1963, p. 63). Melitaeiniare often
Some of the butterfliesin this group
associatedwithAcanthaceae,Scrophularia- feed on a very wide range of plants,
derivatives and mostof the familiesmentionedin the
-ceae and theirwind-pollinated
Plantaginaceae,and withCompositaeand above list are representedby one or at
Verbenaceae. Nymphalinifeed on plants most a very few records. For example,
of thesame familiesas Melitaeini,but also Euptoieta claudia is known to feed on
on theUlmaceae-Urtica- Berberidaceae (Podophylfum),Crassulaveryprominently
ceae-Moraceaegroupand the Convolvula- ceae, Leguminosae,Linaceae, Menispermaceae, Labiatae, Portulacaceae,and Ver- ceae, Nyctaginaceae,Passifloraceae,
Portubenaceae. A single species in this group, lacaceae,Violaceae,andevenAsclepiadaceae
however, Nymphalis canace, feeds on (Cyanchum), and Precis lavinia is reLiliaceae and Dioscoreaceae. Apaturiniare corded from,among others,Acanthaceae,
withUlmaceae,especially Bignoniaceae, Compositae, Crassulaceae,
associatedchiefly
Cyrestis, Onagraceae (Ludwigia), Plantaginaceae,
Celtis. Cyrestini (CChersonesia,
and Marpesia) and Gynaeciini(Gynaecia Scrophulariaceae,
and Verbenaceae.
andHistoris,butnotCallizonaandSmyrna)
Acraeinae,a rathersmall tropicalgroup,
are oftenassociated with Moraceae, and are oftenassociated with PassifloraceaeHamadryini(Ectima, Hamadryas), Dido- Flacourtiaceae-Violaceae-Turneraceae,
as
nini (Didonis), Ergolini (Byblia, Byblis, notedabove,but also withAmaranthaceae,
Ergolis,Eurytela,Mestra), Eunicini (As- Compositae,Convolvulaceae,
Leguminosae,
terope, Catonephele,Eunica, Myscelia), Lythraceae,Moraceae,Polygonaceae,Rosaand Dynamini(Dynamine) mostlyon the ceae, Sterculiaceae,Urticaceae,and VitarelatedEuphorbiaceae,which,like Mora- ceae. In addition,Acraea encedonis receae, have milkysap. In additionto the portedfromCommelina(Commelinaceae).
Diaethria (CalliEunicinijust mentioned,
For the verydiverseNymphalidaeas a
core, Catagramma),Epiphile,Haematera, whole,the followinggroupsof plants are
and Temenisfeed almost ex- especiallyimportant: (1) PassifloraceaePyrrhogyra,
clusively on Sapindaceae. There is no Flacourtiaceae-Violaceae-Turneraceae;
(2)
obviousdominantthemeforthe last tribe, Ulmaceae-Urticaceae-Moraceae,
as well as
to notethat the closelyrelated (Thorne,pers. comm.)
but it is interesting
Limenitini,
twospeciesof Euphaedra(Najas), a group Euphorbiaceae;(3) Acanthaceae-Scrophuthatis mostlyon Sapindaceae,are on Cocos lariaceae-Plantaginaceae.The second and
and other Palmae. Additional families thirdofthesegroupsare represented
among
representedamong the food plants of thefoodplantsof otherbutterflies,
suchas
Nymphalinaeare: Aceraceae,Amarantha- Lycaeninae, but not abundantly. Conceae, Anacardiaceae,Annonaceae,Berberi- versely,as willbe seen,the groupsof food
in Lycaenidae
daceae, Betulaceae, Bignoniaceae, Bom- plantscommonly
represented
bacaceae, Boraginaceae, Caprifoliaceae, -for example, Fagaceae, Leguminosae,
Combretaceae,Corylaceae, Crassulaceae, Oleaceae, Rosaceae-are rarein NymphalDilleniaceae,Dipterocarpa- idae. Althougheach of thesetwo families
Curcurbitaceae,
ceae, Ebenaceae, Eleagnaceae, Ericaceae, of butterflies
is verywide in its choiceof
to
Fagaceae, Gentianaceae,Geraniaceae,Gut- food plants, thereis a distinctiveness
tiferae,Icacinaceae, Leguminosae (very the two patternswhichsuggestsa history
lines.
uncommonly),Loranthaceae,Malvaceae, ofselectionalongdifferent
596
PAUL R. EHRLICH
AND PETER H. RAVEN
Libytheidae.-Thissmallfamilyconsists daceae), and Stalachtis fromOxpetalum
1932,p. 43,
of a single widespreadgenus, Libythea, (Asclepiadaceae;cf.Jorgensen,
associathat
suggested
is
it
where
however,
which feeds almost exclusivelyon Celtis
(Ulmaceae), but in southernJapan on tionsof larvaeof thisgroupwithants may
Prunus(Rosaceae). Libytheais obviously determinethe food plant on which they
closely related to Nymphalidae(Ehrlich, are found). The scantyfoodplant records
diverse
1958), as has recentlybeen confirmed
by forthisgroupare thussufficiently
a quantitativestudy of adult internal to suggest that furtherstudies of food
interest.The
plantswillbe of considerable
anatomy(Ehrlich,unpubl.).
Lycaenidae.-An enormousgroup, the most salient featureis the occurrenceof
familyLycaenidaemaybe largereventhan Hameaeriniand Abisarition Myrsinaceae
the Nymphalidae.Lycaenidaeare in gen- and Primulaceae,two closelyrelatedfamieral poorlyknownfromthe standpointof lies that are fed on by very few other
foodplants (Downey, 1962). Our discus- butterflies.
sion is based largelyon the classification Lycaeninae likewise consist of three
ofClench(1955 and pers.comm.).Nothing tribes.Of these,Leptininiare Africanand
is knownof thelifehistoryof thePeruvian feedon lichens,some of them (Durbania,
Styx infernalis,
only memberof Styginae. Durbaniopsis,and Durbaniella) even on
Of the two remainingsubfamilies,
Riodin- thelow crustoselichensthatgrowon rocks.
inae, divided into three tribes, will be Liphyrini,almostentirelyconfinedto the
discussedfirst.Euselasia (Euselasiini) has Old World tropics, are predaceous on
been recordedfromMammea (Guttiferae) aphids, coccids, ant larvae, membracids,
and threegeneraof Myrtaceae. The Old and jassids. There are no reliablerecords
in thisgroup.
World Hameariniconsistof threegenera, of phytophagy
The largestofthethreetribes,Lycaenini,
with Dodona and Zemeros on Maesa
arrayof formsthat
(Myrsinaceae) and Hamearis on Primula presentsa bewildering
at present.
(Primulaceae). The twoplant familiesare can be separatedonlyinformally
verycloselyrelated,withMyrsinaceaebe- Many of theselarvaeare closelyassociated
ingprimarily
tropicaland woody,Primula- withand tendedby ants,and thisassociaceae primarilytemperateand herbaceous. tionmay modifytheirfoodplant relationThe thirdand largesttribe,Riodinini,is ships (Downey, 1962; Stempffer,pers.
divided into four subtribes. Abisara comm.). For thelargePlebejusgroup(the
(Abisariti) feeds,like the Hamearini,on "blues"), we have records of the food
Myrsinaceae; Theope (Theopiti) is on plants of 45 genera,and 33 of these are
Theobroma(Sterculiaceae);and Helicopus knownto feed,at leastin part,on Legumi(Helicopiti) is one of two membersof the nosae. Recordsof special interestin this
subfamilyknownto feed on a monocoty- groupincludeNacaduba on severalgenera
ledon,in thiscaseMontrichardia
(Araceae). of Myrsinaceaeand Agriadeson PrimulaThe remaininggeneraof Riodininiare in ceae; in thisway theyare like Hamaerini
the exclusivelyNew WorldRiodiniti,with and Abisaritiof Riodininae. Chiladesand
veryfewrecordsfora greatmanyspecies. Neopithecopsare recordedfromRutaceae.
Plantfamiliesrepresented
are Acanthaceae, Four genera (Philotes,Scolitantides,TaliAnacardiaceae,Aquifoliaceae,Chenopodia- cada, and Tongeia) are knownto feed,at
ceae, Compositae,Euphorbiaceae,Legumi- least in part, on Crassulaceae. Catachrynosae,Moraceae,Myrtaceae,Polygonaceae, sops pandava feedsnot only on Wagatea
Ranunculaceae(Clematis),Rosaceae,Ruta- and Xylia (Leguminosae) but also on
ceae, Sapindaceae, and Sapotaceae. De- Cycas revoluta(Cycadaceae), a cycad to
servingspecial mentionare the recordsof whichit does harmin gardens.Hemiargus
Cariomathusand Rhetus fromLorantha- ceraunusfeedson Marantaceae. Although
ceae, Napaea neposfromOncidium(Orchi- mostspeciesof Jamidesfeedon Legumino-
BUTTERFLIES
AND PLANTS
597
sae, J. alecto feeds on Zingiberaceae(a The morphologically
diverseSouth Amerimonocotyledon).
can group referredto "TThecla"is also
In theStrymon
group(Clenchin Ehrlich extraordinarily
diverse in its choice of
and Ehrlich, 1961, plus Strymonidia), food plants: Bromeliacea.e,Celastraceae,
thereis no obviouspattern,but thereare Compositae,Euphorbiaceae,Leguminosae,
several recordsof interest: Dolymorplha Liliaceae,Malpighiaceae,Malvaceae,SapoonSolanum(Solanaceae; Clench,unpubl.); taceae, Solanaceae,and Ulmaceae. In adEumaeus, with E. debora on both Dioon dition to Callolphrys,
already mentioned,
edule (Cycadaceae) and Amaryllis(Lilia- many distinctiveand in some cases large
ceae) and E. atala on bothManihot (Eu- generafeedprimarily
on Loranthaceaeand
phorbiaceae; Comstock,unpubl.) and on the closelyrelatedSantalaceae: Charana,
Zamia integrifolia
(Cycadaceae); Strymon Deudorix, Hypockrysops,Iolaus s. str.
melinus, which feeds on a variety of (also oftenon Ximenia,Olacaceae), Ogyris,
dicotyledonousplants, but also on the Pretapa, Pseudodipsas, Rathinda, and
flowersof Nolina (Liliaceae); and Tmolus Zesius. It wouldappear thattheepiphytic
echion,whichfeedsnot only on Lantana mistletoesand theirrelativeshave consti(Verbenaceae), Cordia (Boraginaceae), tuted an importantadaptive zone for a
Datura and Solanum(Solanaceae), Hyptis numberof generaof Lycaeninae (as sug(Labiatae), and Mangifera (Anacardia- gested by Clench, pers. comm.). Some
ceae), but also on Ananas (Bromeliaceae). species of Iolaus are on Colocasia (AraThe impressive
patternof foodplantradia- ceae). Olacaceae, Loranthaceae,and SantionamongthefoursubgeneraofCallophrys talaceae are presumablyclosely related
deservesspecial mention,for subg. Cal- (Hutchinson,1959), and interestingly
share
lophrysand Incisalia feedmostlyon angio- some acetylinic fatty acids (Sorensen,
Rosa- 1963) andlipids(Shorland,1963). Chliaria
sperms-Leguminosae,
Polygonaceae,
ceae, and Ericaceae-but threespecies of feedson thebuds and flowersof a number
Incisalia have switchedto conifers,
feeding of generaof Orchidaceae,and Eooxylides,
on Picea and Pinus (Pinaceae). A third Laxura, and Yasoida feed on Smilax, a
subgenus,Mitoura,feedsprimarilyon an- hard-leavedmemberof Liliaceae, and the
othergroupof conifers,
similarDioscorea (DioscoreaCupressaceae,with superficially
twospeciessurprisingly
on thepine mistle- ceae). Artipe lives inside the fruitsof
toes, Arceuthobium(Loranthaceae). Fi- Punica (Punicaceae),and Bindaharainside
nally,Callophrys(Sandia) macfarlandi,
the the fruitsof Salacia (Celastraceae). Fionly species of its group, feeds on the nally,Aphnaeusinhabitsgallerieshollowed
flowersof Nolina (Liliaceae) in thesouth- outby antsin thetwigsofAcacia (LegumiwesternUnited States.
nosae), whereit feedson fungi(van Son,
Lycaena and Helioplhorus,closely re- pers. comm.)!
lated, feed primarilyon Polygonaceae In summary,
the plant familiesthatare
throughoutthe nearly cosmopolitanbut best represented
amongthe foodplantsof
largelyextratropical
rangeof both groups. Lycaenini are Ericaceae, Labiatae, PolyThe theclines,
narrowly
defined(Shirozu gonaceae, Rhamnaceae, and Rosaceae.
and Yamamoto,1956), have recentlybeen Other recordsfromfamiliesnot hitherto
treatedby Shirozu (1962), who has dem- mentionedare: Aizoaceae, Amaranthaonstratedthat Fagaceae are the most im- ceae, Araliaceae,Betulaceae,Boraginaceae,
portant food plants, with a numberof Bruniaceae, Burseraceae, Caprifoliaceae,
generaassociatedwithOleaceae. One genus Caryophyllaceae,Chenopodiaceae,Cista(Shirozua) has become predaceous on ceae, Combretaceae,Convolvulaceae,Coaphids.
riaraceae,Cornaceae,Diapensiaceae,DipAmongtheremaining
generaof Lycaeni- terocarpaceae, Ebenaceae, Eleagnaceae,
nae,a fewpointsare especiallynoteworthy.Gentianaceae,Geraniaceae, Hamamelida-
598
PAUL R. EHRLICH
AND PETER H. RAVEN
ceae, Juglandaceae,Lauraceae, Lecithyda- patterns,but as Merz (1959, p. 181)
assume
ceae,Lythraceae,
Meliaceae,Melianthaceae, pointsout, we should nevertheless
Myricaceae, Oxalidaceae, Pittosporaceae, that they probably do have a chemical
Plantaginaceae,Plumbaginaceae,Protea- basis.
ceae, Rubiaceae, Saxifragaceae,Sterculia- Now let us considerthe groupsof orgalarvae,
ceae, Styracaceae,Symplocaceae,
Theaceae, nismsutilizedas foodby butterfly
Thymeleaceae,and Zygophyllaceae. As startingwiththe mostunusualdiets. Two
beforeit mustbe bornein mindthatmany tribesof Lycaeninaehave departedcomof these listingsrepresentsingle records pletely from the usual range of foods:
only; forexample,thewidespread
Holarctic Liptenini feed on lichens,Liphyriniare
Celastrinaargiolushas been recordedfrom carnivorous.Many otherLycaeninae,howfoodplantsbelongingto at least 14 fami- ever,are tendedby ants and in somecases
lies of dicotyledons.Nonetheless,
it should the larvae are broughtinto the ant nests.
be evidentthatthepatternis verydifferent It wouldseemto be a relativelysmallstep
fromthat of Nymphalinae,the only sub- forsuch larvae to switchand feedon the
familycomparableto Lycaeninaein size. ant grubsor fungipresentin these nests.
A numberof species of the group excannibalism(Downey,
hibitwell-developed
DISCUSSION
1962). SeveralLycaenini,suchas Shirozua,
What generalitiescan be drawn from are carnivorous,
and at least one speciesof
these observed patterns? We shall ap- Aplnaeus feedson fungiin ant galleries.
proachthisquestionfromthestandpointof These transitional
stepssuggestthe evoluthe utilizationof different
plantgroupsby tionarypathwaysto the mostdivergentof
butterflies
and see what lightthis throws butterfly
larval feedinghabits.
on patternsof evolutionin the twogroups.
that
Amongthose groupsof butterflies
Butterflies,
of course,are onlyone of many feed on plants,none is knownto feedon
phytophagous
groupsof organismsaffect- bryophytes
or on Psilopsida,Lycopsida,or
ingplantevolution.
Sphenopsida,noris any knownfromferns.
Withintheappropriateecologicalframe- In fact,veryfewinsectsfeed on fernsat
work,ourviewof theimmediate
potentiali- all (cf. Docters van Leeuwen, 1958), a
ties of studies of phytophagyhas been most surprisingand as yet unexplained
statedclearlyand succinctly
by Bourgogne factwithno evidentchemicalor mechanical
(1951, p. 330), who,speakingof the pat- basis. At least one genusof moths,Papaiternsof foodplant choicein Lepidoptera, pema, is knownto feedon ferns,however
said: "Ces anomaliesapparentespeuvent (Forbes, 1958).
parfois demontrerl'existence,entre deux
that
Thereare a fewgroupsofbutterflies
vegetaux,d'une affinited'ordrechimique, feed on gymnosperms.Two genera of
quelquefoismemed'une parentesystemaLycaenidae (Catachrysops;Eumaeus, two
tique. . . ." Thus, the choices exercised by
feedon Cycadaceae,but all three
phytophagousorganismsmay provideap- species)
also feedon angiosperms.
involved
species
proximatebut neverthelessuseful indicaand threespeciesof
(Pierinae)
Neophasia
tions of biochemicalsimilaritiesamong
Incisalia
(Lycaeninae)
subg.
Calloplhrys
groupsof plants. These do not necessarily
subg.
feed
Callophrys
while
on
Pinaceae,
indicate the plants' overall phenetic or
phylogenetic
relationships.The same can Mitoura feedson Cupressaceae(and also
Loranthaceae,a mistlebe said of the choiceof arrowpoisonsby on Arceuthobium,
primitive human groups (Alston and toe that growson pines). It is well esTurner,1963, p. 293) and of patternsof tablishedthat Cupressaceaeand Pinaceae
parasitismby fungi (Saville, 1954). In are chemicallyquite distinct (Erdtman,
have not 1963,p. 120). Judgingfromthetaxonomic
manyof thesecases, biochemists
groups,it
yet workedout the bases forthe observed distancebetweenthesebutterfly
BUTTERFLIES
AND PLANTS
599
as yet undated
feedingon appearanceof dicotyledons,
can be assumedthatbutterflies
musthave antehad ancestorsthat fed on but surelypre-Cretaceous,
gymnosperms
radiationthat proangiosperms.
dated the evolutionary
greaternumberof ducedthemodernlinesof diversification
An overwhelmingly
in
than Lepidopteraand specifically
larvae feedon dicotyledons
butterfly
in PapilionoiThe only two groups dea. All utilizationof foods other than
on monocotyledons.
primarilyassociated with monocotyledonsdicotyledons
larvae (and probby butterfly
are Satyrinaeand Morphinae,closely re- ably by any Lepidoptera)is assumedto be
lated subfamiliesof Nymphalidae. One the resultof changesfroman earlierpatgenus of morphines(Morp-ho) is more ternof feedingon dicotyledons.
but we
oftenassociatedwithdicotyledons,
In general,thepatternsof utilizationby
whether butterfliesof dicotyledonousfood plants
can thinkof no way to determine
this representsa switch from previous show a great many regularities.Certain
monocotyledonfeeding. No memberof relationships
are veryconstant;the plants
Papilionidae,Pieridae, or Libytheidaeis areusuallyfeduponbya single,phenetically
but in coherentgroup of butterfliesor several
knownto feedon monocotyledons,
Nymphalidaeand Lycaenidae numerous very closelyrelatedgroups. As examples
Papilgenerado so in wholeor in part. Among we have theAristolochiaceae-feeding
the Nymphalidae,severalspeciesof Char- ionidae; Pierinae on Capparidaceae and
axes,one of Acraea,one ofNymphalis,and Cruciferae; Ithomiinae on Solanaceae;
two of Euphaedra (Najas) are knownto Danainae on Apocynaceaeand Asclepiadaall of thesegenera ceae; Acraeinae,Heliconiini,and Argynfeedon monocotyledons;
and someof thesamespeciesfeedon dicot- nini on Passifloraceae, Flacourtiaceae,
yledonsalso. In Lycaenidae,a numberof Violaceae,and Turneraceae;and Riodiniverydiversegroups,includingat least two nae-Hameariniand Abisarition Myrsinagenera of Riodininae (Helicopis on Ara- ceae and Primulaceae. In many of these
ceae, Napaea on Orchidaceae) and 11 cases,thebroadpatternsobservedprobably
generaof Lycaeninae (Jamideson Zingi- support suggestionsof overall phenetic
beraceae; Iolaus on Araceae; Tmolus on similarityamong the plants utilized and
concerned.
Bromeliaceae; Chliaria on Orchidaceae; amongthe groupsof butterflies
on thebasis of foodplant
Hemiargus on Marantaceae; and Cal- Otherclusterings
lophrys,Eooxylides, Eumaeus, Strymon, choice like that of Ulmaceae, Urticaceae,
"Thecla," and Yasoda on Liliaceae) feed Moraceae, and Euphorbiaceaeby certain
on monocotyledons.Representativesof groupsof Nymphalidae,probablyalso remanyof thesegeneraand in somecases the flectphylogeneticrelationshipamong the
same species feed on dicotyledonsalso. plantsconcerned.In severalinstances,the
suggeststhatbutter- patternsof foodplant choice of butterfly
This patternstrongly
flies of two familieshave switched to groups underscorethe close relationship
monocotyledonsfrom dicotyledonsin a betweencertainsets of tropicalwoodyand
lines (probablyat temperateherbaceousfamilieselaborated
numberof independent
by Bews (1927). Examplesare Danainae,
least 18).
on Apocynaceae
presented feedinginterchangeably
A corollaryto theobservations
we see in modern and Asclepiadaceae;Pierinae,on Cappariaboveis thatthediversity
has been elaboratedagainst a daceae and Cruciferae;and partof Riodinibutterflies
background.Indeed thisis nae, on Myrsinaceaeand Primulaceae.In
dicotyledonous
probablytrue forLepidopteraas a whole the firstcase, the familiesare generally
(cf. Forbes, 1958). The dominantthemes thoughtto be closelyrelated.On theother
situation hand,Hutchinson(1959) widelyseparated
in this particularcoevolutionary
of considerableinterest.We the membersof thesecondand thirdpairs
are therefore
conclude fromthis relationshipthat the of plant familiesin his system,but this
600
PAUL R. EHRLICH
AND PETER H. RAVEN
dispositionis consideredinappropriateby
Patternsof foodplantutilizationprovide
almostall botanistssince it is based upon evidence bearing on the relationshipof
his primarydivision of floweringplants Araliaceaeand Umbelliferae.Some groups
intowoodyand herbaceouslines. In mak- of Papilioninae,normallyassociated with
ing such decisionsbased on larval food Rutaceae,feedinterchangeably
on Umbelthatwe are liferae,or in some cases have switchedenplants,it mustbe remembered
dealing only with an indirectmeasureof tirelyto thisfamily.As we have seen,these
biochemicalsimilarity.For example,Pieri- two plant familiesare chemicallysimilar.
nae not only feed on Capparidaceaeand But Araliaceaeare close relativesof UmCruciferae,which most botanists would belliferae(Rodriguez,1957) despitetheir
agree are closelyrelated,but also on Sal- wide separationin the systemof Hutchinvadoraceae, which contain mustard oil son (1959), and are commonin manyreglucosidesbut otherwiseseem totallydif- gionswherePapilioninaefeedon Rutaceae.
ferentfromCapparidaceaeand Cruciferae. Despite,this,thereis not a singlerecordof
More equivocal cases likewiseoccur. For a papilionid butterfly(indeed very few
example,Pierinae feed on Tropaeolaceae. butterflies
of any kind) feedingon AraliaNot onlydo Tropaeolaceaeshare mustard ceae. An evenmoreinteresting
relationship
oil glucosideswithCapparidaceaeand Cru- hingeson thesuggestion
thatthethreesubciferae,theylikewisehave in commonthe familiesof Umbelliferae-Apioideae,Hyrare fattyacid, erucicacid. Can we, with drocotyloideae,and Saniculoideae-may
Alstonand Turner(1963, p. 287), dismiss representthreephylogenetic
lines,derived
this as coincidence,or do these groupsof independently
froma grouplikethepresentplantshave morein commonthan is gen- day Araliaceae. All recordsof Papilioninae
erallyassumed? Finally,is therebiochemi- from Umbelliferaeare concerned with
betweenLoranthaceae-Santa- Apioideae, and indeed Dethier (1941)
cal similarity
both foundthatUmbelliferae-feeding
laceae and Capparidaceae-Cruciferae,
papilionine
groupsof larvae refusedHydrocotyle(Hydrocotycommonfoodplantsof different
Pierinae(and of thegenusHesperocharis). loideae). This verystronglysuggeststhat
Whateverconclusionsare drawnabout biochemical
analysismaygo farin elucidatthe biochemicalaffinitiesof plants from ingrelationships
withintheAraliaceae-Umthe habits of phytophagousor parasitic belliferaecomplex,and that the chemical
organisms,little or no weightshould be propertiesgenerallyascribed to Umbelgiven to individualrecords. This is true liferaeas a whole may be characteristic
not only because of the numeroussources only of one subfamily,
Apioideae. Araliaof errorenumeratedearlier,but also be- ceae and Umbelliferae
are knownto share
cause of the multipleexplanationspossible certaindistinctivefattyacids (Alstonand
for such switches. For example, Atella Turner,1963,p. 121) and acetyliniccom(Nymphalinae) feeds on Flacourtiaceae pounds (Sorensen,1963), and it mightbe
and Salicaceae, amongotherplants. It is very instructiveto see how these were
quite possiblethat these two familiesare distributedin Umbelliferaeoutside of
fairlyclosely related,despite the greatly Apioideae.
reducedanemophilousflowersof the latter
In furtherevaluating the patternsof
(Thorne, pers. comm.). But to assume food plant choice in butterflies,
it is imthat the few records involved indicate portantto considerthose plant families,
biochemicalsimilarity
betweenthe groups especiallydicotyledons,which are absent
wouldbe an unwarranted
extensionof the or verypoorlyrepresented.One outstanddata; it wouldbe farsimplerand saferat ing groupis that partlycharacterizedby
thatpointto make comparativeinvestiga- Merz (1959, p. 169) as "Sphingidpflanzen"
of the two plant -plants fed on by mothsof the family
tionsof the biochemistry
families.
Sphingidae.These include,amongothers,
BUTTERFLIES
AND PLANTS
601
Onagraceae, Lythraceae, Balsaminaceae, (richin alkaloids),Myrtaceae,PolemoniaVitaceae, Rubiaceae, and Caprifoliaceae. ceae, Ranunculaceae (rich in alkaloids),
The firsttwo,and probablythe thirdand and Theaceae. In addition,veryfewbutfourth,are generallyregardedas fairly terfliesfeed on Centrospermae,
a group
closelyrelated. Each one of the firstfive characterized
bothby itsmorphological
and
families(Rubiaceae onlyin part) is char- biochemicaltraits(summaryin Alstonand
acterized by the abundant presence of Turner,1963,p. 141-143, 276-279). This
raphides,bundlesof needlelikecrystalsof group includes such large families as
calcium oxalate (see discussionin Gibbs, Amaranthaceae,Cactaceae, Caryophylla1963). In a very interesting
experiment,ceae, Chenopodiaceae,Nyctaginaceae,and
Merz (1959) offeredmature leaves of Portulacaceae. Althoughno biochemical
Vitis (Vitaceae) to larvae of Pterogon basis forthislack of utilizationis knownat
proserpina(Sphingidae). Younglarvaeate present,one probablyexists. For a family
these leaves, theirpointlikebites falling such as the enormousCompositae,poorly
between the clustersof raphides. Older represented
amongthe foodplantsof butlarvae, which make large slashingbites, terflies,the explanationmay lie eitherin
could not avoid the raphidesand did not theirchemicalcomposition
or largelyextraeat theleaves. Aftertheraphidesweredis- tropicaldistribution,
or mostlikelya comsolvedin verydilutehydrochloric
acid, the binationof these. One prominent
familyof
leaves wereacceptedby larvae of all sizes. monocotyledons
thatis practicallyunrepreAlthoughit cannot be proven that some sented among butterflyfood plants is
otherchemicalrepellentwas not removed Araceae (Helicopis, Riodininae,and speby this treatment,it is obvious that cies of lolaus, Lycaeninae,are exceptions).
raphides offer considerable mechanical One can concludeonlythatat leastsome
difficultyfor phytophagousinsects. A of theplantgroupsenumerated
above have
numberof familiesof mothsother than chemical or mechanical propertiesthat
Sphingidaefeedon thissameseriesofplant renderthemunpalatableto butterfly
larvae.
families(Forbes, 1958).
of circumstances
Thus farthe combination
Rubiaceae,one of thefamiliesmentioned permitting
a shiftinto the adaptivezones
above,is perhapsthemostprominent
fam- representedby these groupshas not ocilythatis nearlyabsentfromtherecordsof curred. The assumptionthat such a shift
food plants. Probablythe third is theoretically
butterfly
possibleis strengthened
by
largestfamilyof dicotyledons,
withnearly the observationthat nearlyeveryone of
10,000 species, it is, like the butterflies theseplant groupsis fed upon by one or
themselves,
mostlytropical. One can only morefamiliesof moths.
speculatethat some chemicalfactor,perCONCLUSIONS
haps the rich representation
of alkaloids,
restricts
the
sharply
ability of butterfly A systematicevaluationof the kindsof
larvae to feedon plantsof thisfamily.In plants fed upon by the larvae of certain
this respect,the similaritiesbetweenthe subgroupsof butterfliesleads unambigualkaloids of Apocynaceae(whichhowever ously to the conclusionthat secondary
have milkyjuice) and Rubiaceae are of plant substancesplay the leading role in
interest. Other dicotyledonousfamilies determining
patternsof utilization. This
that are very poorly representedor not seemstruenot only forbutterflies
but for
representedat all among butterflyfood all phytophagous
groupsand also forthose
plants include Begoniaceae,Bignoniaceae, parasiticon plants. In this context,the
Boraginaceae, Celastraceae, Cornaceae, irregulardistributionin plants of such
Curcurbitaceae
(withcurcurbitacins,
bitter- chemicalcompoundsof unknownphysiotasting terpenes), Gesneriaceae,Hydro- logical functionas alkaloids, quinones,
phyllaceae, Loasaceae, Menispermaceae essentialoils (includingterpenoids),gly-
602
PAUL R. EHRLICH
AND PETER H. RAVEN
cosides (includingcyanogenicsubstances to the success of the larvae of Chlosyne
in westernColorado,the
and saponins),flavonoids,and even raph- harrisii.Similarly,
ides (needlelikecalciumoxalatecrystals)is density of the small plants of Lomatium
immediatelyexplicable (Dethier, 1954; eastwoodiae(Umbelliferae)is an important
Fraenkel,1956, 1959; Lipke and Fraenkel, factorlimitingpopulationsize in Papilio
1960; Gordon,1961). indra (T. and J. Emmel,pers.comm.). In
1956; Thorsteinson,
Angiospermshave, throughoccasional these, and many similarsituations,it is
produceda logicalto assumethatgeneticvariantsable
mutationsand recombination,
seriesof chemicalcompoundsnot directly to utilize anotherfood plant successfully
relatedto theirbasic metabolicpathways would be relativelyfavored.This advanbut not inimicalto normalgrowthand de- tage wouldbe muchenhancedif genotypes
velopment.Some of thesecompounds,by arose that permittedswitchingto a new
novelbiochemically
chance, serve to reduce or destroythe foodplant sufficiently
palatabilityof theplant in whichtheyare that it was not utilized,or littleutilized,
in general.
produced(Fraenkel,1959). Such a plant, by herbivores
specialization
protectedfromtheattacksofphytophagous The degreeofphysiological
animals,would in a sense have entereda acquiredin geneticadjustmentto feeding
unusualgroupof plants
newadaptivezone. Evolutionaryradiation on a biochemically
of the plantsmightfollow,and eventually would very likely also act to limit the
whatbeganas a chancemutationor recom- choiceof foodavailableto theinsectgroup
bination might characterize an entire in the generalflora (Merz, 1959, p. 187;
familyor groupof relatedfamilies.Phy- Gordon, 1961). As stressedby Brower
beclose relationships
tophagousinsects,however,can evolve in (1958a), moreover,
response to physiologicalobstacles, as tweeninsectsand a narrowrangeof food
shown by man's recent experiencewith plants may be promotedby the evolution
commercialinsecticides.Indeed, response of concealmentfrompredatorsin relation
to secondaryplantsubstancesand extreme to a single background.The food plant
imbalancesand theevolutionof providesthe substratefor the larvae, not
nutritional
resistanceto insecticidesseem to be in- just theirfood (Dethier, 1954, p. 38).
of certaingroupsof
Afterthe restriction
timatelyconnected(Gordon, 1961). If a
recombinantor mutationappeared in a insectsto a narrowrange of food plants,
repellentsubstancesof these
populationof insects that enabled indi- the formerly
viduals to feed on some previouslypro- plants might,for the insectsin question,
tected plant group,selectioncould carry become chemicalattractants.Particularly
theline intoa new adaptivezone. Here it interestingis the work of Thorsteinson
would be freeto diversifylargelyin the (1953), who found that certainmustard
fromotherphytoph- oil glucosidesfromCruciferaewould elicit
absenceofcompetition
agous animals. Thus the diversityof feedingresponsesfromlarvae that fed on
plants not only may tend to augment theseplantsiftheseglucosidesweresmeared
the diversityof phytophagousanimals on other, normallyunacceptable,leaves.
(Hutchinson,1959), theconversemayalso But if these glucosideswere smearedon
the alkaloid-richleaves of Lycopersicum
be true.
Changesin food plant choice would be (Solanaceae), thelarvaestillrefusedthem.
especiallyfavoredin situationswherethe Similarly,Sevastopulo(pers. comm.) was
supply of the "preferred"plant is suffi- unable to induce the larvae of Danais
to eat anythingbut Asclepiadafactorin chrysippus
cientlylimitedto be an important
the survivalof the larvae. Such situations ceae even by smearingthe leaves of other
have been describedby Dethier (1959), plants with the juice of Calotropis (Aswho showed that the density of Aster clepiadaceae).
clearlythatthechoiceof
This illustrates
umbellatus(Compositae)plantswascritical
BUTTERFLIES
AND PLANTS
603
a particularfoodplantor of a spectrumof nini, which feed on the same plants as
foodplantsmay be governedby repellents Heliconiiniand Acraeinae,do notplay any
present in other plants (Thorsteinson, prominentrole as models for mimetic
1960) as wellas byattractants
inthenormal forms.This maybe in partbecauseArgynfood plants; this fullyaccords with the nini are best developedin temperateremodeloutlinedabove. It shouldnot,how- gions, where butterfliesand therefore
ever, be assumed without experimentalmimeticcomplexesare less common. It
verificationthat a particularsecondary may further
be suggestedthatthemimicry
plantsubstanceis an attractantor feeding supposed to exist between dark female
stimulantforthe insectsfeedingon plants formsof various species of Speyeriaand
that contain it. Indeed, for the beetle the modelBattus pkilenormay well be a
Leptinotarsa,the alkaloids of the Solana- case of Muillerianrather than Batesian
ceae on whichit feedsserveas repellents mimicry.Indeed, the results of Brower
(summaryin Fraenkel, 1959, p. 1467- (1958) with the model Danais plexippus
1468).
and its mimicLimenitisarchippussuggest
In viewof theseconsiderations,
we pro- thatthereis in factno sharpline between
pose a comparablepattern of adaptive Batesian and Miullerianmimicry.These
radiation for each of the more or less shouldbe thoughtof as the extremesof a
strictlylimitedgroupsof butterflies
enu- continuum.Thus Speyeriafemalesmaybe
meratedabove. It is likewiseprobablethat somewhatdistasteful
but can only acquire
theelaborationof biochemicaldefenseshas warningcolorationwhenthe selectivebalplayed a criticalrole in the radiationof ance is tipped by the presenceof other
those groups of plants characterizedby distastefulforms. This followslogically
unusualaccessorymetabolicproducts.
and observafromnumerousexperiments
Further,it can be pointedout that all tions on the behaviorof predatorswith
in mimeticcomplexes,whichrarelyrevealan
thatare important
groupsof butterflies
models in situationsinvolving "either/or"typeof response(cf. Swynnerfurnishing
mimicryare narrowlyrestrictedin food ton, 1919). Assuminga balance of this
Itho- sortwould resolvesome of the difficulties
plant choice: Papilioninae-Troidini;
Acraei- of interpretation
miinae; Nymphalinae-Heliconiini;
the two kinds
concerning
nae; and Danainae. This is in accordance of mimicry(e.g., Sheppard,1963,p. 145).
with a long-standing
suppositionof natuNumerousunusualfeedingpatternsscatralistsand studentsof mimicrythat the teredamongbutterfly
familiesattestto the
shiftsthatenabledthebutter- frequency
physiological
of radiationinto new groupsof
flygroupsto feedon theseplantsconferred foodplants. We can, however,only guess
a doubleadvantageby makingthe butter- at theprobability
of futureradiationin the
fliesin questionunpalatable.These groups new adaptive zone. For example, does
of butterflies
have been selectedforwarn- Stalacktissusanae (Riodininae), whichis
ing coloration,and once established,this knownto feed on Oxypetalumcampestre
conspicuousnesswould tend to put any- (Asclepiadaceae) in Argentina,represent
thingthatwouldmaintaintheirdistasteful- the start of a new phylogenetic
series of
ness at a selectivepremium.
butterfliesrestrictedto this group of
Conversely,those groups of butterflies plants? Probablynot, since the examples
mostof theBatesianmimics- of thissortof unusualfeedinghabit today
thatfurnish
Papilioninae-Papilioniniand Graphiini; far exceed the numberof radiationsobthe close
Satyrinae;Nymphalinae
exceptHeliconiini; servedin the past. Nevertheless,
Pierinae; and Dismorphiinae-feedmostly patternsof coadaptationwe have discussed
on plantgroupsthatare sharedwithother above must have started in a similar
It is some- fashion. Comparable patterns can be
dissimilargroupsof butterflies.
what surprising
that Nymphalinae-Argyn-foundamongplants with biochemicalin-
604
PAUL R. EHRLICH
AND PETER H. RAVEN
cannotaccept the theoreticalpictureof a
mentionedearlier,or the relationshipof generalizedgroup of polyphagousinsects
Sedum acre to otherspecies of its genus fromwhichspecializedoligophagousforms
(Merz, 1959,p. 160).
weregraduallyderived.Justas thereis no
patternsof food truly"panphagous"insect (cf. Fraenkel,
In viewingpresent-day
acceptable
plant utilization,however,the historical 1959), so thereis no universally
aspect of the situationmust not be ne- foodplant; and this doubtlesshas always
glected. A biochemicalinnovationmight been true. This statementis based on the
selectiveadvantage chemicalvariationobservedin plants and
havehad a considerable
for a group of plants in the Cretaceous. the physiologicalvariationobservedin inSuch an advantagewould,of course,have sects. Leguminosaeare importantfood
animals plantsforseveralgroupsofLycaenidaeand
been in termsof thephytophagous
and parasitespresentin the Cretaceous, Pieridae,and woodyRanalesare wellrepreand not necessarilythose of the present sentedamongthe foodplantsof Papilioniday. The crossingof an adaptivethreshold dae and Nymphalidae;but thisshouldnot
by a memberof a livinggroupof phytoph- be taken to prove that these groups of
agous animals would have an entirely plants are "inert" chemicallyor readily
groupsof
now than thatwhich available to otherphytophagous
different
significance
it wouldhave had in the Cretaceous.
insects. The initialradiationof butterfly
For example,even thougha species of taxa ontothesegroupsmayfora timehave
Stalacktisis able to feedon Asclepiadaceae, produceda patternjust as spectacularas,
it shares the available supply of these forexample,the close associationbetween
seen today.
of numerous Troidiniand Aristolochiaceae
plants with representatives
inother groups of phytophagousanimals. We hold thatplantsand phytophagous
to
in
response
in
in
These have, somewhere the course of sects have evolved part
geologicaltime,acquiredtheabilityto feed one another,and that the stages we have
ifthephytophagous postulatedhave developedin a stepwise
on asclepiads. Further,
organismsswitchingearly to milkweeds manner.
As suggestedby Fraenkel(1956, 1959),
became protectedfrompredatorsby their
ingestionof distastefulplant juices, this secondaryplantsubstancesmusthave been
initialadvantagemighthavebeenovercome formedearlyin thehistoryof angiosperms.
in the intervening
years by correspondingAt thepresentday,manyclassesof organic
to
predators.A species compoundsare nearlyor quiterestricted
changesin prospective
of birdlongselectedto like milkweedbugs this groupof plants (for example,see AlStalacktisa stonand Turner,1963,p. 164; Harborne,
mightfind milkweed-feeding
1963, p. 360; Paris, 1963, p. 357). We
gourmet'sdelight.
As in the occupationof any adaptive suggestthatsomeof thesecompoundsmay
and
zone,the firstorganismsto enterit have a havebeenpresentin earlyangiosperms
advantageand are apt to have affordedtheman unusual degreeof protremendous
di- tectionfromthe phytophagousorganisms
to becomeexceedingly
the opportunity
verse beforeevolutionin otherorganisms of the time,relativeto othercontemporary
theirinitialadvantage.In plant groups. Behind such a biochemical
sharplyrestricts
mayhave developed
short,the natureof any adaptive zone is shieldtheangiosperms
diverse. Such an
altered by the organismsthat enter it. and becomestructurally
From our vantagepoint in timewe view assumptionof the originof angiosperms
only the remnants,doubtlessoftendisar- providesa cogentreasonwhyone of many
shatteredby sub- structurallymodifiedgroups of gymnorangedif not completely
of
the
great adaptive spermswould have been able to give rise
sequent events,
to the bewilderingdiversityof modern
radiationsof the past.
whilemostotherlinesbecame
In view of these considerations,we angiosperms,
novations, for example, Senecio viscosus,
BUTTERFLIES
AND PLANTS
605
reextinct.It seemsat least as convincingto degreeof plasticityof chemoreceptive
us as do theoriesbased on the structural sponseand the potentialforphysiological
peculiaritiesof angiosperms.Althoughthe adjustmentto variousplantsecondarysubchemical basis for the success of early stances in butterflypopulationsmust in
theirpotentialfor
may no longerbe discernible, largemeasuredetermine
angiosperms
it can be mentionedthat woody Ranales, evolutionary
radiation. Of secondary,but
generallyacceptedas the most"primitive" still possibly major importance,are meon other chanicalplantdefenses,
and thebutterflies'
assemblageof livingangiosperms
grounds,are as a groupcharacterizedby responsesto them.
manyalkaloidsas well as by essentialoils.
With respectto the second questionon
Of course this mightalso be interpreted the generationof predictionsthe answer
only to mean that the developmentof also seems clear. We cannot predictthe
alkaloidshas permittedthis groupto per- resultsof any giveninteractionwithpresist despiteits manygeneralizedfeatures. cision-Stalachtis on Asclepiadaceae or
of Neophasia on pines may or may not form
In turn,the fantasticdiversification
modern insects has developed in large the basis forfurther
patternsof radiation.
measureas the resultof a stepwisepattern On the otherhand, the basis fora probof coevolutionary
stages superimposedon abilistic statementof "Furtherradiation
the changingpatternof angiospermvaria- unlikely"seems to have been developed.
to the butter- A great many minorpredictionscan be
tion. Withspecificreference
flies,oneis temptedin termsofpresent-day made, such as the probable presenceof
patternsto place moreemphasison thefull alkaloidsin Ptaeroxylon (Meliaceae), the
exploitationof diurnal feedinghabits by solanaceouscharacterof the foodplantsof
the adults than on the penetrationof any unknownlarvae of Ithomiinae,and so
particularbiochemicalbarrierby the lar- forth.
vae. On the otherhand,pheneticrelation- Althoughthedata we have gatheredperships suggest that Papilionoidea (with mit us to make some reasonablesequence
Hesperioidea,theskippers)are representa- predictionsabout phylogeneticpatterns
of Apocynaceaeand
tivesof a line that is amplydistinctfrom (e.g., diversification
all other living Lepidoptera (Ehrlich, SolanaceaebeforeDanainae andIthomiinae,
1958). Thus it is entirelypossible that respectively),these predictionscannot be
radiationonto a new food plant was de- tested and the relationshipscannot be
in the absenceof a fossil
cisive at the time Papilionoidea first specifiedfurther
of phylogenies
diverged,even thoughthe feedinghabits record. The reconstruction
of theorderas a wholeare nowmuchwider on the basis of this sort of information
than those of the butterfliesalone. The wouldseem an unwarranted
impositionon
of decidingobjectivelywhich the data, since evolutionary
rate and time
impossibility
groupsof Papilionoideaare moreprimitive are stillinseparable.
than others (cf. Ehrlich, 1958, p. 334In responseto the fourthquestion,it
the seems to us that studies of coevolution
335) relegatesthe task of identifying
originalgroupof foodplantsforbutterflies providean excellentstartingpoint forunto the realmof profitlessspeculation.
evolution.Indeed
community
derstanding
We wouldlike to returnnow to the four theseemingease withwhichourconclusions
generalquestionsposed at the beginning have been extendedto includethecomplex
of thispaper. First,whathave we learned interactionsamong plants, phytophagous
of the reciprocalresponsesof butterflies organisms,mimics,models,and predators
and theirfoodplants? The observedpat- leads us to believe that populationbioloternsclearlypointto thecriticalimportance gistsshouldpursuesimilarstudiesof other
in governing
the re- systems. Many examples come to mind
of plant biochemistry
Plasmodiumlationshipsbetweenthe two groups. The suchas parasitoid-caterpillar,
606
PAUL R. EHRLICH
AND PETER H. RAVEN
fungus,in however,also be mentionedthat the relahemoglobin,tree-mycorrhizal
whichstepwisereciprocalselectiveresponse tivelypermissivetropicalclimatepresumof plantlife
is to be expected. Studyingmostof these ably allowsa greaterdiversity
secondarilyof animals
tends to be diffi- formsand therefore
systemsexperimentally
cult, and may be complicatedby lack of (Hutchinson,1959,p. 150).
overallconProbablyourmostimportant
in the results.
repeatability
of reciprocal
An approachto biologythatis concerned clusionis thattheimportance
withbroadpatternsquitepossiblywilllead selective responses between ecologically
of some other closely linked organismshas been vastly
to a betterunderstanding
of the origins
ecology. For ex- underratedin considerations
problemsof community
ample,biologistshave longbeen interested of organicdiversity.Indeed, the plantin species herbivore"interface"may be the major
in thereasonsforthedifferences
responsibleforgeneratdiversitybetweentropicaland temperate zone of interaction
organicdiversity.
areas. An importantfactorin maintaining ing terrestrial
may be the sortof synerthesedifferences
SUMMARY
betweenplantsand hergisticinteractions
relationships
The reciprocalevolutionary
bivores we have been discussing. The
and theirfood plants have
selectiveadvantageof livingin a tropical of butterflies
climate is evidentfor insects,which are been examinedon thebasis of an extensive
poikilothermal.Insects are much more surveyof patternsof plant utilizationand
foodplant
on factorsaffecting
abundantin thetropicsthanelsewhereand information
plant
secondary
The
evolution
of
choice.
of
class
the
major
doubtless constitute
herbivorousanimals. The penetrationof substancesand the stepwiseevolutionary
orgaor otheren- responsesto theseby phytophagous
relativelycold environments
facdominant
been
the
clearly
nisms
have
requiringdiapause is probably
vironments
and
of
butterflies
in
the
evolution
tors
in
most
insect
a ratherrecentoccurrence
groups. Furthermore,
are not otherphytophagous
groups. That these environments
alwaysreadilyenteredis attestedto by the these secondary plant substances have
repeated failure of insects such as the probablybeen criticalin the evolutionof
Mestra amymoneto survivethe angiospermsubgroupsand perhapsof the
butterfly
fringes angiospermsthemselves.The examination
winterin localitiesat the northern
of theirrangeswheresummercolonieshave of broad patternsof coevolutionpermits
been established (Ehrlich and Ehrlich, several levels of predictionsand shows
of
promiseas a routeto the understanding
1961).
information
Little
evolution.
community
insects
The abundanceof phytophagous
of
in tropicalregionswould be expectedto usefulforthereconstruction phylogenies
It is apparentthat reciprocal
supplied.
is
interaccentuatethe pace of evolutionary
selectiveresponseshavebeengreatlyundermay
actionswithplants. These interactions
rated as a factor in the originationof
have been the major factorin promoting organicdiversity.The paramountimporthe species diversityof both plants and tance of plant-herbivoreinteractionsin
animalsobservedin the tropicstoday. As generating
is suggested.
terrestrial
diversity
tlhisdiversitywas being produced,it be- For instance,viewedin thisframework
the
came arrayedin richlyvariedmixturesof richdiversityof tropicalcommunities
may
species with relativelygreat distancesbe- be traced in large part to the hospitality
tweenindividualsof any one plantspecies. of warm climates toward poikilothermal
As Grant(1963,p. 420-422) has suggested, phytophagous
insects.
wouldhave theadditional
thisarrangement
LITERATURE CITED
advantageof providinga maximumdegree
ALSTON, R. E., AND B. L. TURNER. 1963. Bioof protectionfromepidemicoutbreaksof
chemical systematics. Prentice-Hall, Engleplant diseases and plant pests. It must,
wood Cliffs,N. J.
BUTTERFLIES
AND PLANTS
607
A. N. BURNS. 1951. Butterflies
taxonomy. Academic Press, London, p. 167of Australiaand New Guinea. N. H. Seward,
186.
Melbourne.
FORBES, W. T. M. 1958. Caterpillars as botaBEws, J. W. 1927. Studies in the ecological
nists. Proc. Tenth Int. Congr. Ent., 1: 313evolution of the angiosperms. New Phytol.,
317.
26: 1-21, 65-84, 129-148, 209-248, 273-294.
FRAENKEL,
G. 1956. Insects and plant bioBOURGOGNE, J. 1951. Ordre des Lepidopteres.
chemistry.The specificityof food plants for
Traite Zool., 10: 174-448.
insects. Proc. 14th Int. Congr. Zool., p. 383BROWER, JANE VAN ZANDT.
1958. Experimental
387.
studies of mimicryin some North American 1959.. The raison d'etreof secondaryplant
butterflies. Part I. The monarch, Danaus
substances. Science, 129: 1466-1470.
plexippus, and viceroy, Limenitis archippus GIBBS, R. D. 1963. History of chemical taxarchippus. EVOLUTION, 12: 32-47.
onomy. In Swain, T., ed., Chemical plant
BROWER, L. P. 1958a. Bird predation and food
taxonomy. Academic Press, London, p. 41plant specificityin closely related procryptic
88.
insects. Amer. Nat., 92: 183-187.
GORDON, H. T.
1961. Nutritionalfactorsin in^--. 1958b. Larval food plant specificityin
sect resistance to chemicals. Ann. Rev.
butterflies of the Papilio glaucus group.
Entom., 6: 27-54.
Lepidop. News, 12: 103-114.
GRANT, V. 1963. The origin of adaptations.
CHER.MOCK, R. L.
1950. A generic revision of
Columbia University Press, New York and
the Limenitiniof the world. Am. Midl. Nat.,
London.
43: 513-569.
HARBORNE, J. B. 1963. Distribution of anthoCLENCH, H. K. 1955. Revised classificationof
cyanins in higher plants. In Swain, T., ed.,
the butterflyfamilyLycaenidae and its allies.
Chemical plant taxonomy. Academic Press,
Ann. Carnegie Mus., 33: 261-274.
London, p. 359-388.
CORBET, A. S., AND H. M. PENDLEBURY.
1956.
HEGNAUER, R. 1963. The taxonomicsignificance
The butterfliesof the Malay Peninsula. Ed. 2.
of alkaloids. In Swain, T., ed., Chemical plant
Oliver and Boyd, London.
taxonomy. Academic Press, London, p. 389COSTA LIMA, A. M. DA. 1936. Terceiro Catalogo
427.
dos Insectos que vivem nas plantas do Brasil.
HUTCHINSON,
G. E. 1959. Homage to Santa
Directoria de Estatistica da Producao Secao
Rosalia or why are there so many kinds of
de Publicade, Rio de Janeiro,p. 201-231.
animals. Amer. Nat., 93: 145-159.
DETHIER,
V. G. 1941. Chemical factors determining the choice of food plants by Papilio HUTCHINSON, J. 1959. The familiesof flowering
plants. Ed. 2. 2 vols. ClarendonPress, Oxford.
larvae. Amer. Nat., 75: 61-73.
. 1954. Evolution of feedingpreferencesin JORGENSEN, P. 1932. Lepidopterologisches aus
Sudamerika. Deutsch. Ent. Zeitschr. Iris,
phytophagous insects. EVOLUTION, 8: 33-54.
Dresden, 46: 37-66.
1959. Food-plant distributionand density
and larval dispersal as factorsaffectinginsect KLOTS, A. B. 1933. A generic revision of the
Pieridae (Lepidoptera). Entom. Amer. n.s.,
populations. Canad. Entom., 91: 581-596.
12: 139-242.
DOCTERS VAN LEEUWEN, W. M.
1958. Zoocecidia. In Verdoorn,F., ed., Manual of pteridol- LEE, C. L. 1958. Butterflies. Academia Sinica
(in Chinese).
ogy. Martinus Nijhoff, The Hague, p. 192LIPKE, H., AND G. FRAENKEL.
1956. Insect nu195.
trition. Ann. Rev. Ent., 1: 17-44.
DOWNEY,
J. C. 1962. Host-plant relations as
data for butterflyclassification. Syst. Zool., MERZ, E. 1959. Pflanzen und Raupen. Vber
einige Prinzipien der Futterwahl bei Gross11: 150-159.
schmetterlingsraupen.Biol. Zentr., 78: 152AND W. C. FULLER.
1961. Variation in
188.
Plebejus icarioides (Lycaenidae). I. Food
plant specificity. J. Lepidop. Soc., 15: 34-42. MICHENER, C. D. 1942. A generic revision of
the Heliconiinae (Lepidoptera, Nymphalidae).
EHRLICH,
P. R. 1958. The comparative morAm. Mus. Novitates, 1197: 1-8.
phology,phylogenyand higherclassificationof
the butterflies(Lepidoptera: Papilionoidea). MUNROE, E. 1960. The genericclassificationof
the Papilionidae. Canad. Ent., Suppl., 17:
Univ. Kansas Sci. Bull., 39: 305-370.
1-51.
AND A. H. EHRLICH.
1961. How to know
AND P. R. EHRLICH.
1960. Harmonization
the butterflies. Wm. C. Brown, Dubuque.
of concepts of higher classification of the
ERDTMAN, H.
1963. Some aspects of chemotaxPapilionidae. J. Lepid. Soc., 14: 169-175.
onomy. In Swain, T., ed., Chemicalplant taxonomy. Academic Press, London, p. 89-125. PARIS, R. 1963. The distributionof plant glycosides. In Swain, T., ed., Chemical plant
FLUCK, H. 1963. Intrinsicand extrinsicfactors
taxonomy. Academic Press, London, p. 337affectingthe production of secondary plant
products. In Swain, T., ed., Chemical plant
358.
BARRETT, C., AND
608
PAUL R. EHRLICH
AND PETER H. RAVEN
E. C. G. 1949. Butterfliesof Rhodesia.
Rhodesia Sci. Association, Salisbury.
PRICE, J. R. 1963. The distributionof alkaloids
in the Rutaceae. In Swain, T., ed., Chemical
plant taxonomy. Academic Press, London, p.
429-452.
1952. The biologyof nearctic
REMINGTON, C. L.
Lepidoptera I. Food plants and life-histories
of Colorado Papilionoidea. Psyche,59: 61-70.
1896. Uber die Palpen der RhoREUTER, E.
paloceren. Acta Soc. Sci. Fennica, 22: i-xvi,
1-577.
1957. Systematic anatomical
RODRiGUEZ, R. L.
studies on Myrrhidendronand other woody
Umbellales. Univ. Calif. Publ. Bot., 29: 145318, pls. 36-47.
1962. The floral morphology
SAFWAT, FUAD M.
of Secamone and the evolutionof the pollinatingapparatusin Asclepiadaceae. Ann.Missouri
Bot. Gard., 49: 95-129.
1954. The fungi as aids in
SAVILLE, D. B. 0.
the taxonomy of floweringplants. Science,
120: 583-585.
SEITZ, A. 1906-1927. The macrolepidopteraof
the world. Vols. 1, 5, 9, 13. Fritz Lehman
Verlag and AlfredKerner Verlag, Stuttgart.
1963. Some geneticstudies of
SHEPPARD, P. M.
Miillerian mimics in butterfliesof the genus
Heliconius. Zoologica, 48: 145-154, pls. 1-2.
1962. Evolution of the food-habits
SHIROZU, T.
of larvae of the theclinebutterflies. Ty6 to
Ga (Trans. Lepidop. Soc. Japan), 12: 144162.
AND H. YAMAMOTO.
1956. A generic revision and the phylogenyof the tribe Theclini
(Lepidoptera: Lycaenidae). Sieboldia, 1: 329421.
of fatty
SHORLAND, F. B. 1963. The distribution
PINHEY,
acids in plant lipids. In Swain, T., ed., Chemical plant taxonomy. AcademicPress, London,
p. 253-303.
S0RENSEN, N. A. 1963. Chemical taxonomy of
acetylinic compounds. In Swain, T., ed.,
Chemical plant taxonomy. Academic Press,
London, p. 219-252.
SWYNNERTON, C. M. F. 1919. Experimentsand
observations bearing on the explanation of
form and colouring, 1908-1913, Africa. J.
Linn. Soc. Zool., 33: 203-385.
THORNE, R. F. 1963. Some problemsand guiding principlesof angiospermphylogeny. Amer.
Nat., 97: 287-306.
A. J. 1953. The chemotactic
THORSTEINSON,
responsesthat determinehost specificityin an
oligophagous insect (Plutella maculipennis
(Curt.) Lepidoptera). Canad. J. Zool., 31:
52-72.
. 1960. Host selectionin phytophagousinsects. Ann. Rev. Ent., 5: 193-218.
VAN SON, G. 1949. The butterfliesof southern
Africa. Part I, Papilionidae and Pieridae.
Part II (1955), Danainae and Satyrinae.
1961.
VAZQUEZ G., LEONILA, AND PEREZ R., H.
Observaciones sobre la biologia de Baronia
brevicornisSalv. (Lepidoptera: PapilionidaeBaroniinae). An. Inst. Biol. Mex., 22: 295311.
1910. The cause determining
VERSCHAEFFELT, E.
the selection of food in some herbivorousinsects. Proc. Acad. Sci., Amsterdam,13: 536542.
E. P. 1957. The Lepidoptera of
WILTSHIRE,
Iraq. Rev. ed. Nicholas Kaye, London.
M. A. 1957. Butterfliesof the
WYNTER-BLYTH,
Indian region. Bombay Nat. Hist. Soc.,
Bombay.

Butterflies and Plants: A Study in Coevolution

Transcription

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