Butterflies and Plants: A Study in Coevolution
Transcription
Butterflies and Plants: A Study in Coevolution
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 Stable URL: http://www.jstor.org/stable/2406212 . Accessed: 12/01/2013 19:30 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact support@jstor.org. . Society for the Study of Evolution is collaborating with JSTOR to digitize, preserve and extend access to Evolution. http://www.jstor.org This content downloaded on Sat, 12 Jan 2013 19:30:21 PM All use subject to JSTOR Terms and Conditions 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 This content downloaded on Sat, 12 Jan 2013 19:30:21 PM All use subject to JSTOR Terms and Conditions 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 This content downloaded on Sat, 12 Jan 2013 19:30:21 PM All use subject to JSTOR Terms and Conditions 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 This content downloaded on Sat, 12 Jan 2013 19:30:21 PM All use subject to JSTOR Terms and Conditions 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- This content downloaded on Sat, 12 Jan 2013 19:30:21 PM All use subject to JSTOR Terms and Conditions 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 This content downloaded on Sat, 12 Jan 2013 19:30:21 PM All use subject to JSTOR Terms and Conditions 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- This content downloaded on Sat, 12 Jan 2013 19:30:21 PM All use subject to JSTOR Terms and Conditions 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, This content downloaded on Sat, 12 Jan 2013 19:30:21 PM All use subject to JSTOR Terms and Conditions 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 This content downloaded on Sat, 12 Jan 2013 19:30:21 PM All use subject to JSTOR Terms and Conditions 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. This content downloaded on Sat, 12 Jan 2013 19:30:21 PM All use subject to JSTOR Terms and Conditions 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 This content downloaded on Sat, 12 Jan 2013 19:30:21 PM All use subject to JSTOR Terms and Conditions 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- This content downloaded on Sat, 12 Jan 2013 19:30:21 PM All use subject to JSTOR Terms and Conditions 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- This content downloaded on Sat, 12 Jan 2013 19:30:21 PM All use subject to JSTOR Terms and Conditions 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 This content downloaded on Sat, 12 Jan 2013 19:30:21 PM All use subject to JSTOR Terms and Conditions 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 This content downloaded on Sat, 12 Jan 2013 19:30:21 PM All use subject to JSTOR Terms and Conditions 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, This content downloaded on Sat, 12 Jan 2013 19:30:21 PM All use subject to JSTOR Terms and Conditions 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- This content downloaded on Sat, 12 Jan 2013 19:30:21 PM All use subject to JSTOR Terms and Conditions 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 This content downloaded on Sat, 12 Jan 2013 19:30:21 PM All use subject to JSTOR Terms and Conditions 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- This content downloaded on Sat, 12 Jan 2013 19:30:21 PM All use subject to JSTOR Terms and Conditions 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, This content downloaded on Sat, 12 Jan 2013 19:30:21 PM All use subject to JSTOR Terms and Conditions 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, This content downloaded on Sat, 12 Jan 2013 19:30:21 PM All use subject to JSTOR Terms and Conditions 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. This content downloaded on Sat, 12 Jan 2013 19:30:21 PM All use subject to JSTOR Terms and Conditions 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 This content downloaded on Sat, 12 Jan 2013 19:30:21 PM All use subject to JSTOR Terms and Conditions 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. This content downloaded on Sat, 12 Jan 2013 19:30:21 PM All use subject to JSTOR Terms and Conditions