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Home , Apaturinae, Dione glycera, Dione juno, Dione moneta, Heliconiinae, Heliconiini

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Ann.Rev. EntomoL 1981. 26:427-J6 Copyright@1981 by AnnualReviews Inc, All rightsreserved

THE BIOLOGY OF 06215 AND RELATED GENERA

Keith S. Brown, Jr. Departmentode Zoologia, Instituto de Biologia, UniversidadeEstadual de Carnpinas, C. P. 1170 Campinas,S~o Paulo 13.100

OVERVIEWAND PERSPECTIVES

Biological studies of mimeticNeotropical in the nymphalidtribe Helieoniini have twice comefull cycle in the past 100 years. Bates’s classic writings (6, 7), reflecting observations during his lengthy stay on the Ama- zon, used these in a proposal of the phenomenonof and in support of Darwinian paradigms of adaptation and . During the following thirty years, field biological studies of heliconians were relegated to second place behind heated arguments about "mimicry" in museum specimens; an important exception was the pioneering work of the brothers Fritz and WilhelmMiiller in southern Brazil (100-105). Most papers in this period involved taxonomic description of the seemingly endless phenotypes in the . In the early 1900s, however,a synthesis of heliconiine systemat-

by University College London on 06/29/06. For personal use only. ics (119, 121) opened the way for field studies during subsequent years Kaye(87, 88), Michael(95, 96), Collenette (43), Moss(98), Beebe (in and others. Both these biological studies (primarily undertaken by Eu- Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org ropean visitors to the Neotropics) and the systematic work, which by then was mostly restricted to namingnew individual forms and aberrations, were interrupted in the pre-World War II period. Modernbiological studies began in the 1950s in Trinidad and since have expandedto manycountries, institutions, and areas of investigation. are nowlaboratory ani- mals; experimental methodsand biological theory have derived great benefit from the detailed study of field and captive populations of these butterflies. The affirmation of Turner (155) that they are the "best studied terrestrial invertebrates of no economic importance outside the Drosophilidae" must be qualified, however. The pests Agraulis vanillae and Dionejuno are the 427 0066-4170/81/0101-0427 $01.00 Annual Reviews www.annualreviews.org/aronline

428 BROWN

principal enemies of passion fruit crops from California to (16, 72, 74, 91, 92) and are difficult to control without ecological techniques (30, 72). In addition, self-regulating forest Heliconius populations have been proposed for the control of a pest of passion vine in Hawaii (J. Waage,J. T. Smiley, and L. E. Gilbert, in preparation). This review covers the ten Neotropical genera in the tribe, but not Paleo- tropical members(, possibly also and other relatives). It summarizesthe recent phase of biological work on these insects, trends in the present state of knowledge, and the most promising areas for future research. A comparisonof basic biological data for all 65 species is provided to aid in the selection of study organisms for projected research. Turner’s bibliography (155) covers the important literature on the Heliconiini through 1976-1977;only half of its 317 entries could be quoted here, but other papers through early 1980 have been included.

FOUNDATIONS FOR BIOLOGICAL RESEARCH ON THE HELICONIINI

Turner (143) reviewed pre-Linnaean publications on heliconians [which include an early adult painting by Petiver (111) and life-history sketches Merian (94)] and important biological work before the 20th century. Classi- cal systematic work benefitted from the incisive thinking of Stichel and Riffarth (118, 119, 121) on species-groups, Dixey and Moulton(53, 99) mimicry, Eltringham (60) on male genitalia, and Joicey and Kaye (82, 88) on subspecies intergradations. The tribe was later catalogued by Neus- tetter (107) and Stichel (120). Newmorphological and morphometrictech- niques were brought to bear on heliconian by Michener(97) and Comstock & Brown (22, 44) during and after World War II. Several life histories were published in the nineteenth century by Jones by University College London on 06/29/06. For personal use only. (84, 85) and the Miillers (100, 103, 105). Nocturnal communalroosting adults, first mentionedby Edwards(56), was later described by Jones (86), Poulton (112), Carpenter (41 ), and Moss(98). Odorproduction by heliconi- Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org ans was investigated by F. MiJller (101, 102, 104), Eltringham (61), Barth (4, 5). Migratory behavior on a large scale northward was noted Randolph (113) and O’Byrne (109) in central North America for species (Agraulis vanillae) and on a small scale southward by Beebe (9) the Venezuelancoastal cordillera for manyspecies. Long-term studies of field behavior were conducted by Kaye (87, 88), Michael (95, 96), Collenette (43). Other references to early works are included in Turner’s reviews (143, 155). The still rapidly expanding recent phase of biological investigation of Heliconiini began in William Beebe’s tropical research station at Simla, Annual Reviews www.annualreviews.org/aronline

BIOLOGYOF HELICONIINI 429

Trinidad in the 1950s. The basic groundwork on juvenile biology and host-plant relationships was provided by Beebe, Crane, Fleming, and Alex- ander (2, 3, 11, 65) after the domestication of numerouslocal heliconian species in large, open-air, semi-natural insectaries (50, 51, 63). Jocelyn Crane initiated ecological and ethological studies (48, 49) that soon branched into a multitude of physiological and biochemical investigations (8, 126-139) and fundamental experiments on the phenomenaof aposema- tism and mimicry (20, 21). Philip Sheppard, John Turner, and Michael Emsley followed Beebe’s lead (10) in an investigation of the genetics MiJllerian mimicry (63, 115, 144, 146, 148-150, 158)which continues occupy an increasing numberof scientists. The systematics of the whole tribe were revised by Emsley (62-64) and Turner (141, 142, 145), reduced the 117 species in Neustetter’s (107) and Stichel’s (120) catalogues to 55. The basic data produced during twenty years of heliconian research at Simlalaid the foundations for almost all the present research on the tribe and provided the initial stimulus and orientation for most modemworkers in the area.

TRENDS AND RESULTS IN MODERN RESEARCH

Descriptive morphologyand biology of the heliconians have nowadvanced to the stage where the entire tribe can be analyzed in comparativeterms for a large numberof features (Figures 1-4, Tables 1-3). Biosystematics (Figure 1) Studies of juvenile biology (2, 3, 11, 24, 25, 34--36, 38, 39, 65, 76, 93, 106, 116, 117, 145, 165), genetics (10, 33, 36, 63, 115, 124, 144, 148, 150, 157-159, 162), field ecology(13, 14, 16, 27, 35, 36, 39, 57, 64, 69, 70, 76, 93, 96, 116, 147), and (26, 28, 29, 31, 39, 40, 44, 62, 64, 89, by University College London on 06/29/06. For personal use only. 140, 146, 156) have given a broad base for the present biosystematic ar- rangementof species and subspecies in the tribe Heliconiini (1, 31). In large part, the biological data have served to confirm the (primarily) morphologi- Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org cally-based systematics of Emsley(62, 64), although detailed observations of local and broad sympatries led to an increase in the numberof species recognized in the tribe from 55 to 65 (26, 31, 39). Biological and morpholog- ical characters agree well in indicating the phylogenyand relative antiquity of modemspecies (Figure 1). The arrangementsof difficult groups of sister- species like (26, 38, 79, 80, .118), the silvaniform Heliconius (27, 33), the cydno superspecies (39, 78), and the sapho-group(26, 34, 39) have been extensively tested and refined in field and laboratory workover the past decade. Remainingproblems that need more investigation include the prob- able division of dido into a numberof sibling species, the rela- Annual Reviews www.annualreviews.org/aronline

430 BROWN

Protdae3icmnla~s | OLD WORLD ...... ?VINDULA& relatives moving.... ,, , CE~IOSIA(many specles) P~sslfioraceae[|NEW WORLD (16) PHILAETHRIApygmalion alal wepnickei l | dido(complex) I PODOTRICHA~=) teleslphe (3 | euchrola(4*) ~ juno (5) ~ moneta (31

~GRAULISvanillae (8) DRYADULAphaetusa DRYAS iulla (12}

l pavana lineata emsleyi(2) I~ procula(7*) lampeto (8*) lsabell~ (17") I eanes (5*) a l al = Antarctica- ~ I Australiabreak apart C aliphera

~e I~%PARUSdoris (8) Hindwingcell open; chrysalisvertical [-~-~3 ao~de (n*) Hindwingcell closed;chrysalis horizontal

3-Hydroxykynureninenot stored:short antennae; five-jointedfemale foretarei xanthocles(13") 3-Hydroxykynureninenot stored;short antennae; four-jointedfemale foretarsi ~ wallacei(5) 3-Hydroxykynurenlnestored as plgme~t;longer |a----- burneyi(7*) antennae;five-jointed female foretarsi egeria (4*) I~ astraea (2*) ~) d not used for nutrients;chrysalis horizontal numata (25 is~enlus~) (7 dI Pollenused for nutr~ents~chrysalis vertlcal pardalinus (10~) heeala (28*) = ethilla(22*) N 31 (haploid chromosome number) atthis N = 21-34 in same individual cydno (ii*) --e N = 21-23 pachlnus l = heurippa _.el N 19-32 ~n same population tlmareta(2*) e N = 21 elevatus(8*) 4 luciana(2*) besckel by University College London on 06/29/06. For personal use only. f signa presenton femalebursa copulatrix f melpomene(29~ fl signa absenton femalebursa copulatrix charitonia(9) hermathena(6) g N = 21 erase(28*) clysonymus(4*) Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org gl N " 33 telesiphe(4*) g2 N ~ 56-59 hecalesia(6*)

demeter(9*) ( ) = numberof geographicalsubspecies recognized (31); leueadla(2) (*) = subspeciesclearly restricted to forestcenters sara(7*) of endemismshoxcn in Figure4 (31.32). antiochus(5*) HYPOTHETICAL hewitsoni TIME-SCALE(years before pre~ent) congener(3*) eleuchia(3*) 6 x 107 5 x 107 4 x 107 3 x 107 2 x i07 107 sapho(4*) I I , I I l I

Figure 1 Postulated phylogenyof the Heliconiini (schematic) [Original interpretation based on that in (24), recent data, and available biosystematicinformation]. Annual Reviews www.annualreviews.org/aronline

BIOLOGYOF HELICONIINI 431

tionships betweenEueides lineata, E. emsleyi, and E. libitina, the atfinities of Heliconius egeria and/t, astraea, the complexspeciation and despecia- tion phenomenaobserved in the silvaniforms (27), and the degrees of inter- fertility of membersof the//, cydno group, of H. atthis with//, ethilla, of H. hortense with H. clysonyrnus, and of H. hewitsoni with H. antiochus.

Captive Cultures The Simla group solved the major problems in rearing heliconians in the tropics (50, 51, 63); the domestication of the butterflies in temperate-zone greenhouses was later accomplishedwith success in Britain (151, Sheppard, Cook) and New York (Turner) and especially Texas (69, 70) in America. The butterflies adapt well to captivity with the help of flowers (including preferred natural pollen sources), supplementary feeders honey water, manypassion vines, over 80%humidity and moderate tropi- cal temperatures (20-30° C), protection from wind and predators, and patchy illumination structure combiningstrong but diffuse brightness and deep shade. Care and good fortune in the choice of founding stock also helps; best are relatively undisturbed populations from open woodswith understory flowers and considerable daily and yearly variation in environ- ment. Field-captured males and females almost always outperform reared individuals in courtship and pollen gathering, if not necessarily in adapta- tion to captivity; inbreeding leads to appreciable loss of viability. Intersub- specific crossing can give increased larval survivorship, but also at times impaired adult performance and skewed sex ratios (33). Various authors have published basic methods for obtaining stock in the field (33, 57, 63, 116, 147, 150, 151, 162, 167). Adults maybe maintained alive for manyweeks during field research if they are kept cool and humid in hanging cages or in envelopes and are fed daily. Eggs and larvae encoun- tered in the field mayshow a high rate of parasitism (57, 70, 72), so cultures by University College London on 06/29/06. For personal use only. are often established from adult females. Larvae grow well in closed humid plastic dishes with daily food and air renewal and are quite resistant to disease. Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org

Juvenile Biology (Figure 2, Tables 1-2) The biology and behavior of the early stages of several species was first thoroughly described from work at Simla (2, 3, 11). Manyrecent papers have included descriptions of juvenile biology as adjuncts to systematic (24, 25, 27, 38, 39, 145), biogeographical(34), evolutionary (14, 16), or ecologi- cal (35, 36, 93, 106, 116, 163-165)investigations. Chaetotaxyof first instar larvae was first described by Fleming (65) and has been expandedrecently by M. Johnson and J. Turner (in preparation). Presently, information Annual Reviews www.annualreviews.org/aronline

432 BROWN

juveniles (Table 1) is essentially complete for all species except Neruda godmani and metharme, Eueides lampeto, and Heliconius hecuba, H. luciana, and//, telesiphe (partial only) and Eueides emsleyi, E. libitina, and E. eanes and the high-Andean Podotricha euchroia and Heliconius hierax (lacking). Eggs (Figure 2A-G), if exposed on tendrils, are placed out of reach of predators. Eggs are often imitated by round yellow plant structures that discourage placement of "more" eggs by ovipositioning females of species with cannibalistic larvae, whicheat eggs and smaller caterpillars (I 6, 70; K. Williams and L. Gilbert, submitted). Larvae are often cryptic in early instars and brightly colored when mature (Figure 2H-Q). Pupae (Figure 2R-W)are usually regarded as cryptic and are well armed with spines (145). Morphological characters of juveniles vary appreciably within species (and sometimeseven within a population) (2, 3, 11, 27, 35), often in apparent response to biotic factors or light regimes. For example, eggs of a single species vary greatly in size and numberof ridges (27); pupae also vary and maybe light or dark (24, 36); caterpillars of/-Z, erato chestertonii have a dark side stripe unknownin other erato larvae; and different larval colors and behaviors in two subspecies of H. demeter (35) have been at- tributed to the presence or absence of other commonHeliconiine larvae in the same regions. Adaptive color-pattern mimicry amonglarvae (Figure 2 O-~ Table 2)has been suggested on several occasions (35, 36, 38, 145). The numbersand traits given in Tables 1-2, therefore, should be regarded as potentially very flexible in individual populations or subspecies. Genetics, Evolution, and Mimicry (Figure 3) The ability to maintain Heliconius in captivity has permitted a variety of genetic experiments to be performed. Workhas mostly concentrated on the strongly polytypic and mutually mimetic species, //. melpomeneand//.

by University College London on 06/29/06. For personal use only. erato (150, 158; P. Sheppard, J. Turner, K. Brown, W. Benson, and M. Singer, submitted), and led to newtheories on the evolution, stabilization, and genetics of Miillerian mimicry (157). Density-dependent factors

Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org mimicry, combinedwith temporal and spatial heterogeneity in the mimetic environment, were proposed to explain wide-scale in

Figure2 Earlystages of heliconianbutterflies. ,4-G, eggs, 8 Xlife size: A, Eueidestales, near hatching;B, Nerudaaoede; C, Heliconiusxanthocles; D, H. timareta;E, 11. telesiphe;F, H. demeter,"G, H. eleuchia.H-Q, larvae: H, Heliconiustimareta, first instar; 1, Philaethria wernickeifirst instar; J-~fifth instars: J,, Philaethriapygmalion; K, ; L, Eueides vibilia;M, Eueides lybia; N, Eueidespavana; O, Eueidestales; P, Heliconiusdemeter eratosignis; Q, Heliconiusheurippa. R-W, pupae: R, Philaethriapygmalion; S, Eueidesvibilia; T, HeliconiuswallaceL" U, Heliconiusheurippa; V, Heliconiushecalesia; W, Heliconius sara. A, l,, M,O, P, T, V, Willustrated in previouspublications; others not. Annual Reviews www.annualreviews.org/aronline

BIOLOGY OF HELICONIINI 433 by University College London on 06/29/06. For personal use only. Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org Annual Reviews www.annualreviews.org/aronline

434 BROWN

Table 1 Morphological characteristics of heliconian eggs, larvae, pupae and adultsa Egg Mature (5th Instar) Special ' Height/ Vert/ ' 'Summary of color - pattern , refer- diamt- horiz. (grd ao~stripor species ences er (mu> ridges spots, scoli, M, anal cap) Philaethria pygmation 36 Ye 1.511.1 2018 WhIBkRe-b ,BkWhRe-sc,Re-hd wemickei 36 Ye 1.511.1 2018 WhIBkRe-b,Bk-sc,YeOr-hd dido complex 11 Ye 1.6 11.2 2 2 / 12 WhIBkRe-b ,BkmRe-sc ,Y e-hd Podotricha telesiphe LG,KB YeWh 1.010.8 20114 G~/Yest,Blsp,~Y~sc,Yehd euchroia ? ? ? ? Y,106 Re 1.0/0.7 1215 Br/Or-sp,Bl-sc+hd mone tu KB,JM Wh 1.1/0.8 1417 Bk/Ye to GrUh-spist,Bk-sc,Wih-M gZycera KB Ye 1.210.9 16/10 Bk/Ye-st,Or-sp,Bk-sc,BkOr-hd AgrauZis vani Z Zae 11 Ye 1.1/0.8 16/13 BkIOrYeWh-sp+st,Or or BkOrhd DryaduZa phaetusa 11 Ye 1.711.1 17/20 Bk/Or-hd Dryas iutia 1L165 Ye 1.211.0 20113 BrIReWh-sp,BkYe-sc,BrWh-hd Eueides vibiZia KB ReWh 1.010.8 1616 Ye/Bl-sp+sc+hd pavam KB Wh 1.0/0.8 18/10 GrYe/Bk-sp+st ,Bk-sc,Or-hd Zineata JM GrWh 0.910.8 20111 GrYeIBkWh-sp+st+sc,Or-hdtac emsleyi ? ? ? ? Zibitinu ? ? ? ? promk KB Cr 0.810.8 16/10 Bk/Ye-sp+st,Bk-sc,BkWh-hd lrrmpeto KB Cr 1.110.8 1619 ? isabeZZa ll,165 Cr 1.010.9 1618 Bk/OrYe-st,Wl-rb,ElWhc+Mpac canes ? ? ? ? by University College London on 06/29/06. For personal use only. Zybia 165,KB Cr 1.010.7 1218 Br/Ye-st,Bk-sc,Or-hd+ac taZes 38,145 Cr 1.110.8 1619 Wh/Bk-sp,Or-hd+ac atiphem U,E5 Cr 0.6/0.6 1918 YeIBkOrWh-b+st+sc+hd

Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org Neruda gohni KB Wh 0.910.7 1818 ? metharme KB,wB Wh 1.010.7 17/12 ? aoede 25,145,wB Wh 0.910.7 16/10 Ma/Wh-sc,Bk-hd Laparus &Pis 11,145 Ye 1.110.8 24/14 Ye/Bk-b+sc+hd Heliconius hierax ? ? ? ? hecuba KB ? ? ? GrYe/Bk-b+scfhd xanthocZes 93,KB Ye 1.110.9 24/14 YeIBk-b+sc+hd Annual Reviews www.annualreviews.org/aronline

BIOLOGY OF HELICONIINI 435

Table 1 (ContinuedJ Adult (62,64) Prothom- Head llHead Segments with: ~ I~ Gs~ital ~ Andro- ~ S~gna acic scoli/ appen-rRef]ectlve large ~ valvetip cenial shape plate height dages spots flanges & process distrlbutkn (b~rsa)

dk,br 2.3 Short 3T;I,2A 3A ]Very long Almost )Broad U, dk,br IalI FW~ one~rm dk,sl 2.3 ) V spike }{Wvelns I thicker

dk,br 2.0 "Non-Helieonius" (LG) [Short ,central~Narrow L, ? ? ? ? ? J bulb }~W veins J arms 4:1

dk,br 0.i Short Absent 3,4A )D and FW,central )Broad c~b, IHW veins ~slight 0.4 2A 3,4A .~ (-HWcubital)J S-curve

1.2 Absent 3,5A V tri FW veins Broad J

1.3 Medium 1,3T;I,2A 3,4A 2 D spi~es FW veins Large L

dk, sl 0.9 Absent 3T,IA 3A Rounded FW+-antHWvn Broad V

dk,br 2.0 Hooks Absent Absent ID short, HW SC,R Broad L 1.0 J V tri Straight 1.0 D mod + Broad L ? ? hook,V ? ? tri dk,4-pt 2.0 long~bokSAbsent Absent [D median, ? ? ? ? J V tri d~4-pt 1.7 long~bO~Absent Absent V,D blunt ? ? ? D mod,V trl

by University College London on 06/29/06. For personal use only. dk,sl 3.0 Hooks D+V long HW SC,R+mb Narrow V dk, sl 4.0 D+V long HWSC, R+mb Broad V dk,br 2.5 D rood,V pnt HWSC+R4M4Cu Broad V Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org ? ? ? ? ? )Rounded, HW vn+entmb )Narrow ? ? ? ? ? > V tri [HW ant area~ sickle dk,br AbserZ Knobs Absent Absent (broad) J curve

dk,br 0. i Knobs Absent Absent D knob HWantm5 Narrow J

? ? ? ? ? Dmod, curved HWent v~mb Broad J dk,br 1.0 ? ? ? D sh, V tri ~HW SC,R Broad L 0.3 Short IA 2-7A D sh, Vround ~ + mb Narrow L Annual Reviews www.annualreviews.org/aronline

436 BROWN

Table 1 Morphological characteristics of heliconian eggs, larvae, pupae and adults a (Continued)

Egg Mature (Sth InStar SpecialI Height/ ]Summary of color - patter Genus, Ver~/I species refer- Color d~m~et- hertz. (gronrdcol~E~nd~ stripes ences er (ran) ~dges spots,scol~, he~d, a~al cap) ~e l~eonius wallace~ 11,145 Cr 1.1/0.9 18/11 Ma/Ye-sc,Br-hd burneyi 145, ~B Cr 1.1/0.9 18/11 MaBk/Ye-sc,Bk-hd efferia KB Cr 1.2/0.9 16/13 Or/Bk-sc+hd a~traea 25,KB Cr 1.2/0.9 16/13 Or/Bk-sc+hd nattereri 24 Ye 1.1/0.8 14/11 Wh/Bk-sp+sc,YeBk-hd numata 27 Ye 1.4/0.9 16/10 W~/Bk-sp+sc,Or-hd+ac ismenius 27 Ye 1.3/0.8 14/12 Wh/Bk-sp+sc,Or-hd+ac pardal~nu~ 27 1.4/0.9 16/11 Wn/Bk-sp+sc,Or-hd+ac hecale 27,164 1.9/0.9 16/13 Wh/Bk-sc,Or-hd ethilla ii,25,27 Ye 1.3/0.9 16/13 Wh/Bk-sc,Or-hd atthis 27,KB Ye 1.3/0.8 17/13 Wh/Bk-sc,Or-hd cydno 163,KB 1.8/1.0 14/10 " Wh/Bk-sp+sc,Or-hd paeh~nua ~S Wh/Bk-sp+sc,Or-hd KB,WB Ye 1.6/1.0 16/10 heurippa 1.6/1.0 18/11 W~/Bk-sp+sc,Or-hd timareta KB 1.7/1.1 18/14 W-h/Bk-sp+sc,Or-hd luaiana KB Ye 1.5/1.1 15/14 ? e Zev~tus KB 1.4/1.1 15/12 Wh/Bk-sp+sc,Or-hd+ac besakei KB 1.2/0.9 14/10 Wh/Bk-sp+sc,Or-hd melpomene LLKB 1.5/1.0 15/12 Ye or Wh/Bk-sp+sc,Or-hd charitonia LQKB YeWh 1.2/0.8 14/11 Wh/Bk-sporb+se,BkYeorl~iWh-I hermathena 36 Ye 1.3/0.7 16/13 Re/BkWh-sp+b,Bk-sc,Re-hd crate ii Ye 1.5/0.9 16/11 Wh/BkOr-sp,Bk-sc,Ye-hd eZysonymus 145,JS Ye 1.5/1.0 15/12 Wh/BkOr-sp,Bk-sc,Ye-hd hortense LG Ye Wh/BkOr-sp,Bk-sc,Ye-hd te les~phe KB Ye 1.6/0.8 15/14 ? hecalesia 34,JS Ye 1.2/0.8 Ye/Bk~p+se*hd ~cini II,KB Ye 1.2/0.7 17/15 Ye/Bk-sp+sc+hd

by University College London on 06/29/06. For personal use only. d~meter 35 Ye 1.3/0.7 14/10 Ye/Bk-sp or b+sc+hd leucadia KB YeWh 1.0/0.8 14/10 Br/Bk-b+sc+hd sara 11,36 Ye 1.1/0.7 13/7 Ye or Br/Bk-b+sc+hd

Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org c~ntiochu8 KB Ye 1.1/0.8 12/10 Ye/Bk-se+hd h6~itsoni JS,JM Ye 1.2/0.8 11/10 YeGr/Ye-sc,Bk-hd aon~ener KB YeWh 1.0/0.7 ii/I0 Ye/Bk-se~hd eZeuah~a KB YeWh 1.0/0.8 ii/ii 8aphO LG~,KB,JSYeWh 1.0/0.7 11/10 i

aAbbreviations: ? -- no information available; Colors, Ye = yellow, Wh= white, Cr = cream, Re = re Or = orange, Br = brown, Bk = black, Ma = maroon, Gr = green, dk = dark, It = light; b = bands or rin~ sp = spots, st = longitudinal stripes; sc = scoli, hd= head, ac = anal cap; Prothoracic plate, br = broa sl = slender, pt = partite; Pupal segments, T = thoracic, A = abdominal; Valve shape, D = dorsal, V ventral, tri = triangular, sh = short, rood = moderate length, pnt = pointed; Androconia, FW= forewin Annual Reviews www.annualreviews.org/aronline

BIOLOGY OF HELICONIINI 437

able 1 (ContinuedJ Larva Pupa Adult (62,64) Pro~ Head 1 ~"ead Segments with: l~Ge~ital ~Andro- ~ Slgna acic .scoli/ appen- ’Ref~ec~velarge valvetip conial shape plate he,hi dages spots flanges &process d~ai~utkn (b~rs~

1.0 Short 3T;I,2A 3,4A Long D HWvn+mb ]Narrow L, 1.0 process HW ant mb ~ratlo of 2.0 Very longD 2.0 Short D tN~mtarea~HW ant area arms 5:1 dksl 1.8 Short 1,3~,1,2A 3,4A Nod D tip FW l~ HW SC,~StraightL it. sl 2.0 (projectin~~FW vn, HW | with ver- 2.0 ShortD tip ] SC+R+mb ~ tical arm 2.0 Shortened HWvn+antmb{ broader, 1.8 ThickD tip HW ant mb ~2x horiz- 1.7 ~ ontal arm 1.5 1.2 3,4,6A Short D tip 1.4 1.9 dk.sl 2.0 ? ? ? 9 ? Longertip HW vn~antm~ it,sl 1.6 Short 1,3T;I,2A 3,4A Longertip HW vr~Uantmb it or~ 1.7 Mod D tip HW m~t mb it c~ 1.5 Short tip dk,sl 1.2 Long 3,4,6,7A Rounded HW SC+R Absent 2.0 Ned ium 3,~, sh Mod D tip HW SC,R,M+mb 1.3 Long 3,4,6A Mod D tip 1.2 3,4,6,7ARounded HW SC,R~b 1.3 3,4,6,7ARounded ~ ~R~ ? 9 ? D knob ~ ~R,~ dk,sl 1.0 Long 3T;I,2A 3-7A D mod, V tri ~ ~,R(~ dk,br 0.8 1,3T;I,2A 3,4,6A Rounded HW SC, R~b 2.0 by University College London on 06/29/06. For personal use only. 3,4,6A Rounded HW ~t mb 0.5 3,4A Squared HW SC, R~b 0.4 Rounded HW SC,R~b 1.2 Absent Squared HW R~b-SC Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org 0.3 Squared 0.3 Pointed

HW= hindwing, ant = anterior (costal) region, vn = veins, mb = membrane,SC, R, M, Cu, = subcostal, radial, median, cubital, and anal veins respectively; Signa, U, J, L, V indicate shapes. General references.. 11, 24, 25, 26, 27, 34, 35, 36, 38, 39, 62, 64, 93, 145, 163, 165; unpublished data from L. Gilbert, J. Mallet, J. Smiley, and W. Benson; and personal observations, still unpublished ~KB). Annual Reviews www.annualreviews.org/aronline

438 BROWN by University College London on 06/29/06. For personal use only. Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org Annual Reviews www.annualreviews.org/aronline

BIOLOGY OF HELICONIINI 439

Heliconius numata and other silvaniforms, controlled by supergenes or -complexes (33, 144). Like polymorphismand supergenes, sexual di- morphismwas not predicted to appear in Miillerian mimicry; where it exists in three species of Heliconius, it is correlated with rarity and habitat dis- sociation betweenthe sexes (24, 34, 35). Interspecific hybridization is occasional in Heliconius populations both in the field and in the insectary; it has also been recorded in Eueides, but is most often seen in membersof the silvaniform-cydno-melpomene group (Brown, in preparation). It usually produces broods, including both sexes, with reasonable viability and somefecundity (especially in backcrosses) and thus can lead to limited introgression and the possibility of somereticulate evolution in the tribe. Long-termgenetic experiments, interspecific - ization, and the appearance of "throwback mutations" in captive popula- tions (150; L. Gilbert, J. Turner, personal communication)all suggest high degree of shared major color-pattern in the membersof the genus Heliconius, with appreciable modification and epistasis changing or sup- pressing the expression of genes that are nonetheless present in homologous positions in the different species. These observations permit the tentative extrapolation of phenotypic expressions to genes in species not yet studied in captivity; in one case (Heliconius hermathena), this gave someinsight into the rate of adaptive color-pattern evolution under favorable local selec- tion in the field (36). The effectiveness of Miillerian mimicryin nature was supported by paint- ing over the red forewing band of Costa Rican/t. erato petiverana (making them look like H. e. chestertonii) and noting the appreciably greater attack and mortality rates in the altered, nonmimeticindividuals (13). The Miil- lerian-mimetic convergences evident between various membersof widely divergent lines in Heliconiini (Figure 3) demonstrate natural selection for the evolution of mimicry, as opposed to pattern similarity due only-to by University College London on 06/29/06. For personal use only. commonheritage (154). Reseoablanceseffective in protection against preda- tors develop in part by homologous, but more often by analogous mecha- nisms in the different radiating lines. The development of the Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org Miillerian-mimetic patterns has been related to aspects of the physical environment, especially light distribution and structure, by Emsley (63) and Papageorgis (110) and to biotic selection, on populations isolated in small ecological refuges, by Turner (153, 156, 157); still other hypotheses, equally attractive, await testing with new and more complete data. Isozyme divergence and heterozygosity in Heliconius demonstrate little correlation with homozygouscolor-pattern gene sets in geographical races, suggesting both "classical" and "balanced" modes of evolution within a single genome (159). A sex-linked enzyme is not dosage compensated Annual Reviews www.annualreviews.org/aronline

440 BROWN

females (the heterogametic sex) of H. rnelpomene, suggesting a possible basis for other sex-limited phenomenasuch as female mimicry (81). Preliminary karyological examination of Heliconiini is nearly complete (52, 124, 162; K. Brown, T. Emmel,P. Eliazar, and E. Suomalainen, in preparation), but methodsare still lacking for visualization of fine struc- tures of chromosomes.Achiasmatic oSgenesis in females has been reported in H. melpomeneand other species (125, 160; J. Mallet and L. Gilbert, personal communication), but maynot be universal in the tribe. The main patterns of chromosomenumbers are shown in Figure 1. The outcome of genetic crosses suggests that chromosomearrangements maydiffer between different subspecies of H. erato (A. M. Araujo, K. Brown, and W. Benson, in preparation) and H. melpomene(J. Mallet and L. Gilbert, personal communication), with concomitant reduction in viability and fecundity in intraspecific crosses. Biogeography (Figure 4, Table 2) Following early work by Michael (95), Emsley (63), Turner (140, 146), Sheppard(40), Heliconiini have been used in a broad investigation of geo- graphic patterns of evolution in the Neotropics. The Heliconiini are espe- cially useful for this analysis, since they include widespread polytypic species with markedregional differentiation in color-pattern, whichis gov- erned by a few genes and easily related to stabilizing selection in mimetic environments(40). The clear patterns of regional endemism(26, 28, 29, 32, 89, 153) (Figure 4), based on a sampling network of 3500 stations over the Neotropics, correlated well with areas of high probability for forest continuity during the last glacial maximum,13,000-20,000 years ago (sug- gested by independent paleoclimatological, geomorphological, pedological, and phytosociologicalcriteria), but did not correlate with localities of high species diversity (an ecological rather than evolutionary phenomenon)(30-

by University College London on 06/29/06. For personal use only. 32). Detailed population observations, however, suggest that manyof these endemic patterns could be produced by parapatric differentiation in re- sponse to modernenvironmental gradients (15, 66, 161). There seems little

Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org doubt that both modern and historical factors are involved in regional

Figure4 Biogeographicaldivision of forest heliconiansinto four principalspecies regions (A-D)and 43 importantsubspecies centers in the Neotropics.Thesubspecies "centers endemism"1--43 are boundedby isoline contoursrepresenting one third of the maximumvalue for correctedendemism. This valuewas determined for 1520quadrants of 30’ X30’ latitude and longitudeby a summationof local endemicsubspecies minus double the numberof hybridizedpopulations (with invading subspecies from other endemiccenters) (31, 32). bers in parenthesesafter the center namesare the local endemicsubspecies recognized as associatedwith that center, amongthe 46 speciesof forest heliconiansanalyzed. Note that 46 of the 65 speciesin the tribe are endemicto oneof the four speciesregions A-D. Annual Reviews www.annualreviews.org/aronline

BIOLOGYOF HELICONIINI 441

HELICONIANENDEMISM AMERICA TROPICAL 4. Neehf (13) 5. thee6 (9) 6. Chlmborazo (13) SUBSPECIESCENTERS 7, Cauca (5) 8. Magdalene (5) 1. Guatemala (10) 9. Santa Marts (3) 2. Chlriquf(ii) 10. Catatumbo (7) a. Azuero (2) ll. Rancho Grande (9) 3. Darl~n (3) 12. Sucre-Trinidad (6) a. Tobago (2) 13. Apura (7) 14. Villavicencio(9) 15. Putumayo(8) 16. Napo (ll) 21. Ucayali (10) 17. Abitagua(8) 22. Chanchamayo (4) B. (I) 23. Inambari (7) 18. Suede (8) 24. Yungas (12) 26. Imataca (3) 19. Maranon (5) 25. Guapor4 (5) 27. Pantepul(6) 20. Huallaga(7) 28. Roraima (3) 29. Ventuari (5) 30. Imer~ (12) ’31. Manaus-Gulana(12 + 6) a. Tapar~ (i) 32. Oyapock (ii) 33. Bel~m (5) 34. MaraJ6(4) 35. TapaJBs(ii + i) 36. RondOnia(5) 37. Madeira(i) 38. Tef~ (4) 39. Loreto (5) by University College London on 06/29/06. For personal use only. SPECIESREGIONS:

I Transandean (1~ Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org ~ Centers 1-15 .:~-~southwardextension :~’, in a few species 40. Pernambuco(i) Centers 4-25 41. Araguala(4) (very discontinuous) ~ ~ Amazonian (17 species) 42. Bahia (5) j~’~- : Centers 15-39 43. Rio de Janeiro(5) /~.~;~" ~ : Pautepui subregion.... .~..~5’M~ (i endemic species) ~ .-’~ Centers 26-30 Atlantic (~ species), 40-43 Annual Reviews www.annualreviews.org/aronline

442 BROWN

endemismpatterns; the attempt to identify the causative factors has led to muchimportant parallel research on paleoecology and population ecology, which in somespecific cases has uncovered significant new evolutionary phenomena(14, 15, 30-32). Dispersal undoubtedly plays an important role in many aspects of heliconian biogeography(12, 34, 39, 45, 67). Species with migratory tenden- cies or very wide-ranging flight, at least under someenvironmental condi- tions, include those labelled "Mg"in Table 2; species which are often sedentary include Nerudaaoede and , H. cydno, 1t. erato, and H. hermathena (13, 36, 45, 57, 116, 147). Population Biology ,(Table 2) Field studies of Heliconius often reveal a pattern of small, rather self- contained local populations, composedof long-lived, continually reproduc- ing individuals who learn resource locations by following during the daytime individuals with whomthey roost at night (12, 13, 24, 36, 45, 48-50, 57, 75, 116, 147, 152, 166, 167; K. Saalfeld and A. M. Araujo, submitted). Kin selection is thought to operate strongly in such populations (12, 33, 149). Membersof someother heliconiine genera are shorter-lived, more dispersive, and exist in larger and more ill-defined populations. The two species of Podotricha have dramatically skewedsex ratios (e.g. male: female 10 - 50:1) both in collections (62, 161) and in the field (personal observation), and they mayshow peculiar biological characteristics. Some sex and age classes, especially younger females, maybe highly vagile at sometimes of the year, possibly representing density-dependent dispersal (31, 39); individuals in these classes are often found sleeping awayfrom the communalroosts (K. Brownand J. Vasconcellos-Neto, unpublished data). Populations of Heliconius seem to be regulated largely by egg and early instar larvae mortality [which may come from manysources, including by University College London on 06/29/06. For personal use only. foodplant deterioration or exhaustion, predators, parasitoids, and storms (70, 116)] as well as availability of adult resources, including , pollen, space, and mate location and suitability (17, 75). While population numbers Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org maybe exceedingly constant in somerain forest areas (57), fluctuations are commonlyobserved in more seasonal climate (24, 33, 39), the peak abundance usually occurring from near the end of the wetter season into the dry season.

REPRODUCTIVE BIOLOGY AND PHYSIOLOGY The long reproductive period of adult Heliconius is a function of continuous nutrient intake, mainly from pollen, involving a numberof physiological, morphological, and ethological adaptations (17, 18, 54, 55, 69-71). Laparusand Heliconius collect pollen from certain flowers and incubate it with fluid on their Annual Reviews www.annualreviews.org/aronline

BIOLOGY OF HELICONIINI 443

tongues, releasing nitrogenous nutrients which (like labelled amino-acids ministered in parallel experiments) should be rapidly incorporated into eggs and spermatophores (69, 70). Females also obtain nutrients from digestion of male spermatophores to help in egg production (17, 18, 71). The length of the reproductive period varies within the genus Heliconius and is appar- ently muchshorter in (17, 54, 55); thus, there exist many different reproductive syndromeswithin the tribe. Courtship and mating are complex and variable within the Heliconiini; little has been published recently on comparative ethological characteris- tics, and almost nothing has been written of chemical or visual signals in natural courtship sequences since Crane’s early work(48-50). Certainly the large and complicated 1-1eliconius head, including greatly enlarged com- pound eyes and optic and other sensory ganglia, is important in courtship, food-location and gathering, and the evaluation of host-plant quality (70).

Community Ecology A series of papers by Gilbert and co-workers relates the communityecology of heliconians to a variety of important concepts, from guild structure and habitat displacement through the organization and succession of tropical forest systems to practical aspects of conservation biology (70, 72-76). The tightly coevolved food webs such as that of the Heliconiini//An- guria-Gurania system may represent key units for research on structure, function, and diversity in tropical systems. They also provide a base for conservation planning (the Brazilian governmenthas already included re- suits of heliconian biogeographyin the choice of favorable areas for parks and reserves; 28-32, 72, 74); and since the heliconian/ system is an easily monitored and reliable indicator of manyecological processes in tropical communities(30), it maybe used in the evaluation of preserved systems and the managementof diversity (74). The tight mutualistic rela- by University College London on 06/29/06. For personal use only. tionship between Heliconius and its pollen sources ,4nguria and Gurania (Cucurbitaceae) maybe illustrative of the great importance of such systems in the structure and stability of tropical ecosystems(70, 74); modernecolog- Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org ical theory has largely ignored such interactions, and important models have not taken them into account.

FOODPLANTUTILIZATION (Table 3) Many of the dimensions of a larval heliconian’s world are determined by the female’s choice of oviposition site (16). Recently, this choice has been shown to have a broad ecological component(116, 117), often independent of plant chemistry and larval acceptability. Thus, studies of juvenile biology should include analysis of adult ecology and physiology, as well as plant quality, and should include examination of potential versus realized niche. Annual Reviews www.annualreviews.org/aronline

444 BROWN by University College London on 06/29/06. For personal use only. Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org Annual Reviews www.annualreviews.org/aronline

BIOLOGY OF HELICONIINI 445 by University College London on 06/29/06. For personal use only. Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org Annual Reviews www.annualreviews.org/aronline

446 BROWN by University College London on 06/29/06. For personal use only. Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org Annual Reviews www.annualreviews.org/aronline

BIOLOGYOF HELICONIINI 447

++

+ by University College London on 06/29/06. For personal use only. Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org

~°° Annual Reviews www.annualreviews.org/aronline

448 BROWN

The massive data on foodplant utilization presented by Benson, Brown & Gilbert (16) is of little use for studies in ecological space and time; the interactions reported in Table 3 must be resolved into local foodplant-usage data sets through newfield and laboratory studies. Only in La Selva, (ll6), and along~the Sumar6 road in Rio de Janeiro (14, 16) long-term patterns of resource partitioning in natural heliconian communi- ties be regarded as very:well known; comparisons between these data sets and less complete ones, or ones collected over a larger area, should be drawn with due caution. The’ patterns interpreted in relation to macroclimateby Benson(14) include two data sets from heavy forest where interactions are very difficult to observe; one of these is from an island with a depauperate community.Since these patterns are not the same as those seen in two additional equatorial sites in Brazil (personal observation), it is possible that resource utilization patterns are also determined by factors such as disturbance, heterogeneity, and site accessability. Like other results of pre- sumedcompetition, between-plant resource patterning in heliconians needs to be investigated by experimental manipulation in the field; present views are still mostly based on negative data. The physiological and environmental parameters important to the in- teraction between Agraulis and Passiflora have been studied in an impor- tant work by Copp & Davenport (46, 47) which helps to focus the more anecdotal information widely scattered in other papers (16, 70). Many aspects of the morphologyand biology of Passiflora can best be understood in terms of interactions with Heliconiini (16, 70; K. Williams and L. Gil- bert, submitted); this strengthens the case for powerfulcoevolutionary pres- sures between these two groups of organisms (16, 58, 68). Such specific interactions are very useful in broad studies of communityecology (70, 72-76). Occasional reports exist for the feeding of heliconian larvae on a number by University College London on 06/29/06. For personal use only. of plant families other than Passifloraceae; the only confirmed one is that on the closely related Turneraceae in Costa Rica (D. Janzen, personal communication). Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org

Biochemistry Manyinvestigators assumethat Heliconiini are distasteful due to sequestra- tion of poisonous chemicals derived from their foodplants (16, 19-21, 70), but no evidence for this has yet been published. Preliminary analysis of Heliconius adults has shown presence of cyanogenic glycosides (R. H. Davis and A. Nahrstedt, in preparation), but the presence of these compounds in the larval foodplants of the specimens examinedwas not determined. Even the strong "witch-hazel" (isocyanide?) scent of mated females has still eluded chemical identification, although female odor has been shownto be Annual Reviews www.annualreviews.org/aronline

BIOLOGY OF HELICONIINI 449

important as a "chemical chastity belt" (71) and mayfunction in intras- pecific alarm and interspecific defense roles as well. Also unidentified are the male androconial pheromonesand the female pupal odors that attract males. Wingpigments in the Heliconiini are in part polymeric, but some reds have been shownto include pterins (8), and the light yellows in Neruda, Laparus, and Heliconius are the amino-acid 3-hydroxy-L-kynurenine (23, 37). The silver reflective spots of pupae (Figure 2R, T- ~ are physical nature; spots with a gold color are underlaid by yellow tanning pigments (I08).

Sensory and Behavioral Physiology Manyauthors have commentedon the ability of heliconians to respond to novelty and to learn complexsequences of resource discovery and utiliza- tion, both in the field (57, 70) and in captivity (48, 49, 70); Skinnerian experiments of sequencing and color-form discrimination have been re- ported (48, 49, 127). Extensive investigation of heliconian vision has domi- nated physiological studies, but some information is also available on hearing (132) and temperature tolerance (42). The details of heliconian visual physiology, implicated in complexbehavior patterns, are in accord with daily rhythmsof activity (128, 129), the use of red colors in courtship and flower seeking (39, 48, 49, 126, 127), and image processing along multiple channels (77, 90, 114, 122, 123, 128-131, 133-138). Somecontro- versy has developed around the fundamental neurological processes in- volved in Heliconius color vision and learning, but little doubt remains about the existence of unusual physiological processes in these butterflies.

SYNTHESIS

by University College London on 06/29/06. For personal use only. With an increasingly firm base of systematics, biogeography, and descrip- tive biology, research on Heliconiini has movedon to complexinvestigation of physiology, behavior, ecology, and evolution. Primary areas of intense Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org ongoing research in the last decade include natural selection, sociobiology, evolution at and above the population level, interactions with other organ- isms and implications for tropical communities, developmentof ecological preferences and behavior patterns, neurophysiology, reproductive biology and physiology, and genetics and mimicry. Heliconians now rival Euphy- dryas butterflies (59, 75) in the amount of new information and concepts they have contributed to population biology. Long-term research on the Heliconiini, aided by accurate identification of organisms, an eye for the unexpected, and complementarylaboratory studies, has generated impor- tant insights into tropical biological processes: Annual Reviews www.annualreviews.org/aronline

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1. Muchvariation in fundamental morphologyis possible in these organ- isms; within single widespreadspecies, the variation is often determined by only a few genes and sometimesis capable of interpretation in relation to local selective factors. 2. Historical and modemecological factors interact with intrinsic features of heliconian populations to determine a wide variety of local characters, communitystructures, and regional subspecies distributions in the com- plex and heterogeneous Neotropical forest environment. 3. These long-lived invertebrates with variable and ephemeral resources have developed very complexbehavioral physiology, including response to novelty and correlative learning, within a tight social structure. 4. Specific plant-herbivore interactions like those of Heliconius/Passiflora may form biological subsystems very useful in the study of community structure and function in the tropics. 5. Miillerian mimicry is a verifiable ecological phenomenonwith unex- pected genetic and evolutionary facets and maybe important to larvae as well as adults of host-specific insects feeding on plants presumedto be poisonous. 6. Classical and balanced modesof evolution, occurring within a single genome, can at the same time maintain variety at weakly selected loci and rapidly fix homozygosisat strongly selected loci. As heliconian butterflies gain wider acceptance as laboratory and continue to attract investigators interested in field biology, their already substantial contribution to scientific theory and knowledgeshould increase. Their complexnervous system, rapid development,accessibility in the field, and high degree of ecological specificity makethem well adapted for future research.

by University College London on 06/29/06. For personal use only. ACKNOWLEDGMENTS This review was prepared during a sabbatical year in the laboratories of P. P. Feeny, Cornell University, Ithaca, NY, whomI thank for facilities and Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org supplies. I also wish to thank L. Gilbert, J. Mallet, C. Boggs,J. Smiley, P. Ehrlich, D. Bowers, D. Lincoln, M. Emsley, J. R. G. Turner, P. Ackery, G. Lamas, W. W. Benson, M. Berenbaum, and A. J. Dammanfor reading and commenting on the manuscript and tables and supplying reprints, manuscripts, and unpublished information. Annual Reviews www.annualreviews.org/aronline

BIOLOGY OF HELICONIINI 451

Literature Cited 1. Ackery,P. R., Smiles, R. L. 1976. An 14. Benson, W. W. 1978. Resource parti- illustrated list of the type-specimensof tioningin passionvine butterflies. Evo- the (: Nym- lution 32:493-518 phalidae) in the British Museum(Natu- 15. Benson,W. W. 1980. Alternative mod- ral History). Bull. Br. Mus.Nat. Hist. els for infragenericdiversification in the Entomol.32:171-214 (39 plates) humidtropics. In The Biological Model 2. Alexander,A. J. 1961. A study of the for Diversificationin the Tropics,ed. G. biologyand behaviorof the caterpillars, T. Prance. NewYork: ColumbiaUniv. pupaeand emergingbutterflies of the In press subfamily Heliconiinae in Trinidad, 16. Benson,W. W., Brown,K. S. Jr., Gil- WestIndies. Part I. Someaspects of lar- bert, L. E. 1976. of plants val behavior. ZoologicaNY 46:1-24 (1 and herbivores: passion flower butter- plate) flies. Evolution29:659-80 3. Alexander,A. J. 1961. A study of the 17. Boggs,C. L. 1979. Resourceallocation biologyand behaviorof the caterpillars, and reproductivestrategies in several pupaeand emergingbutterflies of the heliconiinebutterfly speciez PhDthesis. subfamily Heliconiinae in Trinidad, Univ. Texas, Austin. 201 pp. See also WestIndies. Part II. Molting,and the Boggs,C. L. Am.Nat. 115: In press behaviorof pupaeand emergingadults. 18. Boggs,C. L., Gilbert, L. E. 1979.Male Zoologica NY46:105-23 contributionto egg production:first evi- 4. Barth, R. 1952. Os 6rgfios odoriferos dencefor transfer of nutrients at mating masculinosde alguns Heliconiinae do in butterflies. Science206:83-84 Brasil. Mere. lnst. OswaldoCruz 50: 19. Boyden,T. C. 1976. palatabil- 335-442 ity and mimicry: experiments with 5. Barth,R. 1960.Org~.os odoriferos dos Ameivalizards. Evolution30:73-81 Lepid6pteros.BoL Parq. Nac. Itatiaia, 20. Brower,L. P., Brower,J. V. Z. 1964. Minist. .4gric. Rio de Janeiro7:1-159 Birds, butterflies and plant poisons:a 6. Bates, H. W. 1862.Contributions to an studyin ecologicalchemistry. Zoologica insect fauna of the AmazonValley, NY 49:137-59 Lepidoptera:Heliconidae. Trans. Linn. 21. Brower,L. P., Brower,J. V. Z., Collins, Soc. London23:495-566 C. T. 1963. Experimental studies of 7. Bates, H. W.1864. The Naturalist on mimicry.7. Relative palatability and the River Amazons.London: J. Murray. Miillerian mimicryamong neotropi- ix -t- 465pp. (2 maps),2nd ed. cal butterflies of the subfamilyHeli- 8. Baust, J. G. 1967. Preliminarystudies coniinae. Zoologica NY48:65-84 (1 on the isolation of pterins from the plate) wingsof heliconidbutterflies. Zoologica 22. Brown,F. M., Comstock,W. P. 1952. NY 52:15-20 Somebiometrics of Heliconius char# 9. Beebe, W. 1950. Migration of Danai- tonius (Linnaeus). Am. Mus. Novit. dae, Ithomiidae, Aeraeidae and 1574:1-53 Heliconiidae (butterflies) at Rancho 23. Brown,K. S. Jr. 1967. Chemotaxonomy by University College London on 06/29/06. For personal use only. Grande, north-central . and chemomimicry: the case of 3- Zoologica NY 35:57-68 hydroxykynurenine. Syst. ZooL 16: 10. Beebe, W. 1955. Polymorphism in 213-16 reared broodsof Heliconiusbutterflies 24. Brown,K. S. Jr. 1972.The Heliconians Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org fromSuriname and Trinidad. Zoologica of Brazil. Part III. Ecologyand Biology NY 40:139-43 of Heliconiusnattereri, a key primitive 11. Beebe,W., Crane,J., Fleming,H. 1960. species near extinction, and comments A comparisonof.eggs, larvae and pupae on the evolutionary developmentof in fourteen species of Helieoniinebut- Heliconius and Eueides. ZoologicaNY tertties fromTrinidad, W.I. Zoologica 57:41-69 NY 45:111-54 25. Brown,K. S. Jr. 1973. TheHeliconians 12. Benson,W. W. 1971. Evidencefor the of Brazil. Part V. Threenew subspecies evolutionof unpalatability throughkin from Mato Grosso and Rond6nia. Bull selection in the Heliconiinae(Lepidopt- Allyn Mus. 13:1-19 era), Am. Nat. 105:213-26 26. Brown, K. S. Jr. 1976. Geographical 13. Benson,W. W.1972. Natural selection patterns of evolution in Neotropical for Miillerian mimicryin Heliconius Lepidoptera. Systematics and deriva- erato in Costa Pica. Science 176: tion of knownand newHeliconiini. £ 936-39 EntomoLSet. B . 44:201-42 Annual Reviews www.annualreviews.org/aronline

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27. Brown, K. S. Jr. 1976. An illustrated Cramer, with description of a new key to the silvaniform Heliconius with subspe.c.ies from Venezuela. Z. Arbeits- descriptions of newsubspecies. Trans. gem. Osterr. Entomol. 24:44-65 Am. Entomol. Soc. Philadelphia 102: 39. Brown,K. S. Jr., Mielke, O. H. H. 1972. 373-484 The Heliconians of Brazil (Lepidoptera: 28. Brown, K. S. Jr. 1977. Centros de evo- ). Part II. Introduction lu¢~o, reffgios quatermlrios e conserv- and general comments, with a supple- a~o de patrimrnios genrticos na regi- mentaryrevision of the tribe. Zoologica ~o neotropical: padrOes de diferencia- NY 57:1-40 c~o em Ithomiinae (Lepidoptera: Nym- 40. Brown, K. S. Jr., Sheppard, P. M., phalidae). Acta Amazonica 7:75-137 Turner, J. R. G. 1974. Quaternary 29. Brown, K. S. Jr. 1977. Geographical refugia in tropical America: evidence patterns of evolution in neotropieal for- from race formation in Heliconius but- est Lepidoptera (Nymphalidae: Ithomi- terflies. Proc. R. Soc. London Ser. B inae and Nymphalinae-Heliconiini). In 187:369-78 Biogeographie et Evolution en Am~rique 41. Carpenter, G. D. H. 1933. Gregarious Tropicale, ed. H. Descimon, pp. 118- roosting habits of aposematic butter- 60. Paris: Lab. Zool. Ecole Norm. Su- flies. Proc. R. Entomol. Soc. London per., Publ. 9. 344 pp. 8:110-11 30. Brown, K. S. Jr. 1978. Hetero- 42. Clarke, K. U. 1977. The transient and geneidade: fator fundamental na teoria steady state responses in oxygen con- e pr~itica de conservaq~o de ambientes sumptionby tropical butterflies to tem- tropicais. Encontro Nac. Preserva¢~o perature step transfer tests. J. Zool. Fauna e Rec. Faunlst., Brasilia 1977, 183:251-68 pp. 175-83. Brasilia: IBDF 43. Collenette, C. L. 1928. Observations on 31. Brown, K. S. Jr. 1979. Ecologia Geo- the bionomics of the Lepidoptera of gr~fica e Evolucdo nas Florestas Neo- tropicais. Vols. 1, 2. Campinas:Univ. Matto Grosso, Brazil. 1. On some mi- metic combinations of butterflies ob- Estadual de Campinas. xxxi + 265 pp., served. 3. On the odour of two species 120 pp. 32. Brown, K. S. Jr. 1980. Paleoecology of Heliconius. Trans. R. Entomol. Soc. and regional patterns of evolution in London 76:391-401,409-10 Neotropieal forest butterflies. See Ref. 44. Comstock, W. P., Brown, F. M. 1950. 15. In press Geographical variation and subspecia- 33. Brown, K. S. Jr., Benson, W. W. 1974. tion in tteliconius charitonius Linnaeus. Adaptive polymorphism associated Am. Mus. Nov#. 1467:1-21 with multiple Miillerian mimicry in 45. Cook, L. M., Thomason, E. W., Young, . Biotropica 6: A. M. 1976. Population structure, dy- 205-28 namics and dispersal of the tropical but- 34. Brown, K. S. Jr., Benson, W. W. 1975. .,terfly Heliconius charltonius. J.. Anim. West Colombian biogeography: notes .... ’Ecol. 45:851-63 on and//, sapho. J.. 46. Copp, N. H., Davenport, D. 1978. Agraulis and Passiflora. I. Control of

by University College London on 06/29/06. For personal use only. Lepid. Soc. 29:199-212 35. Brown, K. S. Jr., Benson, W. W. 1975. specificity. Biol. Bull. 155:98-112 The Heliconians of Brazil. Part VI. As- 47. Copp, N. H., Davenport, D. 1978. pects of the biology and ecology of dgraulis and Passiflora. II. Behavior Heliconius demeter, with description of and sensory modalities. Biol. Bull. Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org four new subspecies. Bull. Allyn Mus. 155:113-24 26:1-19 48. Crane, J. 1955. Imaginal behavior of a 36. Brown, K. S. Jr., Benson, W. W. 1977. Trinidad butterfly, Evolution in modern Amazonian non- hydara Hewitson, with special refer- forest islands: Heliconius hermathena ence to the social use of color. Zoologica (The Heliconians of Brazil. Part VII). NY 40:167-96 Biotropica 9:95-117 49. Crane, J. 1957. Imaginal behavior in 37. Brown, K. S. Jr., Domingues, C. A. A. butterflies of the Heliconiidae: 1971. A distribuiqS_o do amino-ficido 3- changing social patterns and irrelevant hidroxi-L-quinurenina nos Lepidrp- actions. Zoologica NY 42:135-45 teros. An. Acad. Bras. Cirnc. 42:211-15 50. Crane, J. 1957. Keepinghousefor tropi- (Suppl.) cal butterflies. Natl. Geogr. 112:193- 38. Brown, K. S. Jr., Holzinger, H. 1973. 217 (Aug.) The Heliconians of Brazil. Part IV. Sys- 51. Crane, J., Fleming, H. 1953. Construc- tematies and biology of Eueides tales tion and operation of butterfly insectar- Annual Reviews www.annualreviews.org/aronline

BIOLOGY OF H.ELICONIINI 453

ies in the tropics. Zoologica NY butterflies in:the~,xaguaiaregion, cen- 38:161-72 tral Brazil. Biotropica,12: In press 52. de Lesse, H. 1967. Les hombres de 67. Gilbert, L. E. 1969.The biology of nat- chromosomeschez les Lrpidopt~res ural dispersal: Dionemoneta poeyii in Rhopaloc~resn~otropicaux. Ann. Soc. Texas. J. Lepid. Soc. 23:177-85 Entomol. Fr. (NS) 3:67-136 68. Gilbert, L. E. ii971. Butterfly-plantco- 53. Dixey,R. A. 1909. On Miillerian mim- evolution: has Passiflora adenopoda tornol.icry and Soc. diaposematism. London1908:559-83 Trans. R. En- wonthe selectional race with helicon- iine butterflies? Science172:585-86 54. Dunlap-Pianka,H., Boggs,C. L., Gil- 69. Gilbert, L. E. 1.972. Pollenfeeding and bert, L. E. 1977. Ovarian dynamicsin reproductivebiology of Heliconiusbut- Helieoniine butterflies: programmed terflies. Proc. "Natl. dead. ScL USA senescenceversus eternal youth. Science 69:1403-7 197:487-90 70. Gilbert, L. E. ~19.75.Ecological conse- 55. Dunlap-Pianka, H. L. 1979. Ovarian quences of a coevolved mutualismbe- dynamicsin Heliconiusbutterflies: cor- tweenbutterfliesand plants. In Coevolu- relations amongdaily ovipositionrates, tion of Animalsand Plants, ed. L. E. egg weights,and quantitative aspects of Gilbert, P. H. Ra~ven,pp. 210-40.Aus- otigenesis. J.. Insect PhysioL25:741-49 tin: Univ. TexasPress. 246pp. 56. Edwards,W. H. 1881.On certain habits 71. Gilbert, L. E. 1976.Postmating female of Heliconiacharitonia Linn., a species odor in Helicon~usbutterflies: a male- of butterfly foundin Florida. Papilio contributed anfiaphrodisiae? Science 1:209-15 193:419-20 57.Ehrlich, P. R., Gilbert, L. E. 1973.Pop- 72. Gilbert, L. E. 1977.Therole of insect- ulation structure and dynamicsof the plant coevolutionin ’the organizationof tropical butterfly Heliconiusethilla. Biotropica 5:69-82 ecosystems. In ~Comportementdes ln- 58. Ehrlich, P. R., Raven,P. H. 1965.But- sectes et MilieuTrophique, ed. V. Laby- terflies and plants: a study in coevolu- fie, pp. 399-413.Paris: C.N.R.S.Col- tion. Evolution18:586-608 loq. Int. 265. 493pp. 59. Ehrlich, P. R., White,R. R., Singer, M. 73. Gilbert, L. E. 1979. Developmentof C., McKechnie,S. W., Gilbert, L. E. theoryin the analysisof insect-plantin- 1975.Checkerspot butterflies: a histori- teractions. In AnaC~’sof EcologicalSys- cal perspective. Science 188:221-28 tems, ed. D. Horn,R.. Mittler, G. Stairs, 60. Eltringham, H. 1917. Onspecific and pp. 117-54. Cobambus:Ohio State mimetic relationships in the genus Univ.Press. 312 pp. Heliconiu~ Trans. R. Entomol. Soc. 74. Gilbert, L. E. 1980. Foodweb organiza- London1916:104-48 tion and the conservationof neotropical 61. Eltringham,H. 1925. Onthe abdominal diversity. In ConservationBiology, ed. glands in I-leliconiu~ Tran~ R. En- M. E. Soulr, B. A. Wilcox,pp. 11-33. tomol. Soc. London1925:269-75 Sunderland,Mass: Sinauer Assoc. 62. Emsley, M. 1963. A morphological 75. Gilbert, L. E., Singer, M.C. 1975.But- study of imagine Heliconiinae (Lep.: terfly ecology. Ann. Rev. Ecol. Syst. by University College London on 06/29/06. For personal use only. Nymphalidae)with a consideration of 6:365-97 the evolutionaryrelationships within 76. Gilbert, L. E., Smiley,J. T. 1978.Deter- the group. ZoologicaNY 48:85-130 (1 minantsof local diversity in phytopha- plate) gousinsects: host specialists in tropical

Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org 63. Emsley,M. G. 1964. The geographical environments.In Diversity of Insect distribution of the color-patterncompo- Faunas, ed. L. A. Mound,N. Waloff, nents of Heliconius erato and pp. 89-104.London: Blackwell. 204 pp. Heliconius melpomenewith genetieal 77. Gordon,W. C., Bashager, S. F. 1978. evidencefor the systematicrelationship Retinalpathways in the optic lobe of the betweenthe two species. ZoologicaNY butterfly,Agraulis vanillae. J. CellBiol. 49:245-86(2 plates) 79:102A(Abstr.) 64. Emsley, M. G. 1965. in 78. Holzinger, H., Holzinger, R. 1968. Heliconius: morphologyand geographic Heliconiuscydno gerstner£ n. ssp. und distribution. ZoologicaNY 50:191-254 zwei neue formen yon H. c.ydno cyd- 65. Fleming,H. 1960.The first instar larvae tomol.nides Stgr. 20:17-21 Z. ,~rbeitsgem.Osterr. En- of the Heliconiinae(butterflies) of Trini- dad, W. I. ZoologicaNY 45:91-110 79. Holzinger,H., Holzinger,R. 1969. Zur 66. Gifford, D. R. 1980.Edaphic factors in Synonymicyon Heliconius (Eueides) dispersion of heliconian and ithomiine eanesheliconioides Fldr. trod /-/. (E.) Annual Reviews www.annualreviews.org/aronline

454 BROWN

tales cognatus Weym.Z. .4rbeitsgem. mente coligidos de Passiflora spp. Rev. Osterr. Entomol. 21:64-69 Agric. Piracicaba 29:23-29 80. Holzinger, H., Holzinger, R. 1974. Eu- 93. Mallet, J. L. B., Jackson, D. A.. 1980. eides procula browni, eine neue SubslLe- The ecology and social behaviour of the cies aus Venezuela. Z. Arbeitsgera. Os- Neotropical butterfly Heliconius xan- terr. EntomoL24:147-52 thocles Bates in . Zool. J. 81. Johnson, M. S., Turner, J. R. G. 1979. Linn. Soc. 69: In press A.bsence of dosage compensation for a 94. Merian, M. S. 1705. Metamorphosisln- sex-linked enzyme m butterflies sectorum Surinamensiz Amstelo- (Heliconius). Heredity 43:71-77 damum:(3. Valk. 60 pp. (60 plates) 82. Joieey, J. J., Kaye, W. J. 1917. On a 95. Michael, O. 1912. Ueber die Le- collection of Heliconiine forms from benweise der Heliconiden. Fauna Exot. . Trans. R. Entomol. 2:8, 10-19, 21-22 Soc. London 1916:412-31 96. Michael, O. 1926. Betraehtungen iiber 83. Joicey, J. J., Kaye, W. J. 1919. Notes on die Nymphaliden der Amazonasebene a large Heliconine collection made in und der angrenzenden Teile der an- French Guiana in 1917, compared with dinen Region. I. Teih Die Heliconiden a similar collection made in 1915. und Acraeiden. Entornol. Z. 39:185-94 Tranz R. Entomol. Soc. London 97. Michener, C. D. 1942. A generic revi- 1918:347-53 sion of the Heliconiinae (Lepidoptera, 84. Jones, E. D. 1882. Metamorphoses of Nymphalidae). Am. Mus. Novit. 1197: Lepidoptera from Santo Paulo, Brazil, 1-8 in the Free Public Museum,Liverpool 98. Moss, A. M. 1933. The gregarious (with nomenclature and description of sleeping habits of certain Ithomiine and new forms by F. Moore). Proc. Lit. HeliconineEntomol. Soc.butterflies London in 7:66-67Brazil. Proc. R. Philos. Soc. Liverpool 36:327-77 85. Jones, E. D. 1884. Metamorphoses of 99. Moulton, J. 1909. On some of the prin- Lepidoptera from San Paulo, Brazil, in cipal mimetic (Miillerian) combinations the Free Public Museum, Liverpool of tropical Americanbutterflies. Trans. (with nomenclature and description of R. Entomol. Soc. London 1908:585-606 new forms by F. Moore). Second series. 100. Miiller, F. 1877. Die Maracuj~ifalter. Mus. Rep. Liverpool 4:1-115 Stettin. Entomol. Ztg. 38:492-96 86. Jones, F. M. 1930. The sleeping Heli- 101. Miiller, F. 1877. Beobachtungen an conias of Florida. Nat. Hist. 30:635-44 brasilianischen Schmetterlinge. I-2. Die 87. Kaye, W. J. 1907. Notes on the domi- Duftsehuppen der m~innlichen nant Miillerian group of butterflies from Maracujb.falter. Kosrnos Stuttgart 1: the Potaro districtEntomol. of BritishSoc. LondonGuiana. 391-95 Trans. R. 102. Miiller, F. 1877-78. Beobachtungen an 54:411-39 brasilianischen Sehmetterlinge. II. Die 88. Kaye, W. J. 1916. A reply to Dr. E1- duftschuppen des m~innchens yon Dione tringham’s paper on the genus vanillae. KosmosStuttgart 2:3842 Heliconius. Trans. R. Entomol. Soc. 103. Miiller, F. 1877-78. und die by University College London on 06/29/06. For personal use only. London 64:149-53 Maracujfifalter als Raupen, Puppen und 89. Lamas, G. 1976. Notes on Peruvian Schmetterlinge. Kosmos Stuttgart butterflies (Lepidoptera). II. New 2:218-24 Heliconius from Cusco and Madre de 104. Miiller, F. 1878. Die Stinkktilbchen der

Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org Dios. Rev. . Ent. 19:1-7 weiblichen Maracuj~ifalter. Z. Wiss. 90. Langer, H., Struwe, G. 1972. Spectral Zool. Abt. A 30:167-70 (1 plate) absorbanee by screening pigment gran- 105. Miiller, W. 1886. Sudamerikanische ules in the compoundeye of butterflies Nymphalidenraupen. Versueh eines (Heliconius). Z Comp. Physiol. 79: naturlichen Systems der Nymphalidae. 203-12 Zool. Jahrb. 1:417-678 (4 plates) 91. Lordello, L. G. E. 1952. Insetos que 106. Muyshondt, A., Young, A. M., Muy- vivem sobre o maracuj~zeiro. I. Notas shondt, A. Jr. 1973. The biology of the bion6mieas aeerca de Dione vanillae butterfly Dione juno huascama in El (L., 1758). Rev. Agric. Piracicaba Salvador. J. NY Entomol. Soc. 27:177-87 81:137-51 92. Lordello, L. G. E. 1956. Insetos que 107. Neustetter, H. 1929. Nymphalididae: vivem sobre o maracuj~zeiro. III. Notas subfam. Heliconiinae. Lepid. Cat. 36:1- acerca de Dione juno (Cramer) e rela- 136 ¢~o de alguns outros insetos habitual- 108. Neville, A. C. 1977. Metallic gold and Annual Reviews www.annualreviews.org/aronline

BIOLOGY OF HELICONIINI 455

silver colours in someinsect cuticles. J. 125. Suomalainen, E., Cook, L. M., Turner, Insect Physiol. 23:1267-74 J. R. G. 1973. Achiasmatie oogenesis in 109. O’Byrne, H. 1932. On the migration the heliconiine butterflies. Hereditas and breeding of Dione vanillae in Mis- 74:302-4 souri. Entomol. News 43:97-99 126. Swihart, C. A. 1971. Colour discrimina- 110. Papageorgis, C. 1975. Mimicry in Neo- tion by the butterfly Heliconius tropical butterflies. Am. Sci. 63:522-32 charitonius Linn. Anim. Behav. 19: 111. Petiver, J. 1702-11. Gazophylacii Natu- 156-64 rae et Artis. London: Bateman 127. Swihart, C. A., Swihart, S. L. 1970. Co- 112. Poulton, E. B. 1931. The gregarious lour selection and learned feedin~ pref- sleeping habits of Heliconius chari- erences in the butterfly, Heliconius tonius, L. Proc. R. Entomol. Soc. Lon- charitonius Linn. Anita. Behav. 18: don 6:4-10 113. Randolph, V. 1927. On the seasonal mi- 128. Swihart, S. L. 1963. The electroretino- grations of Dione vanillae in Kansas. gram of H¢liconius erato and its possi- Ann. Entornol. Soc. Am. 20:242-44 ble relation to established behavior pat- 114. Schiimpedi, R. A. 1975. Monocular terns. Zoologica NY 48:155-65 and binocular visual fields of butterfly 129. Swihart, S. L. 1964. The nature of the interneurons in response to white- and eleetroretinogram of a tropical but- coloured-light stimulation. ,/.. Comp. terfly. J. lnsect Physiol. 10:547-62 Physiol. 103:273-89 130. Swihart, S. L. 1965. Evokedpotentials 115. Sheppard, P. M. 1963. Some genetic in the visual pathway of Heliconius studies on Miillerian mimicsin butter- erato. Zoologica NY 50:55-62 flies of the genus Heliconiuz Zoologica 131. Swihart, S. L. 1967. Neural adaptations NY 48:145-54 in the visual pathway of certain Heli- 116. Smiley, J. T. 1978. The host plant coniine butterflies, and related forms, to ecology of Heliconius butterflies in variations in wing coloration. Zoologica northeastern Costa Rica. PhDthesis. NY 52:1-14 Univ. Texas, Austin 132. Swihart, S. L. 1967. Hearing in butter- 117. Smiley, J. T. 1978. Plant chemistry and flies (Heliconius, Ageronia). J. lnsect the evolution of host specificity: newev- Physiol. 13:469-76 idence from Heliconius and Passiflora. 133. Swihart, S. L. 1967. Maturation of the Science 201:745--47 visual mechanisms in the Neotropical 118. Stichel, H. 1903. Synonymisches Ver- butterfly, Heliconius sarae. J. lnsect zeichnis bekannter Eueides-Formen Physiol. 13:1679-88 mit erliiuternden Bemerkungen und 134. Swihart, S. L. 1968. Single unit activity Neubeschreibungen. Berl. Entomol. Z. in the visual pathwayof the butterfly 48:1-34 tteliconius erato. J. lnsect Physiol. 119. Stichel, H. 1906. Lepidoptera, ram. 14:1589-1601 Nymphalidae, subfam. Heliconiinae. In 135. Swihart, S. L. 1972. The neural basis of Genera lnsectorum, ed. P. Wytsman, color vision in the butterfly, 1-1eliconius 37:1-74 (6 plates) erato. J. lnsect Physiol. 18:1015-25 by University College London on 06/29/06. For personal use only. 120. Stichel, H. 1938. Nymphalidae:subfam. 136. Swihart, S. L. 1972. Variability and the Dioniinae, Anetiinae, Apaturinae. nature of the insect electroretinogram. Lepid. Cat. 86:1-374 J. lnsect Physiol. 18:1221-40 121. Stichel, H., Riffarth, H. 1905. Heliconii- 137. Swihart, S. L. 1973. Retinal duality in

Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org dae. Das Tierreich, 22:1-290. Berlin: R. the butterfly Heliconius charitonius. J. Friedlander lnsect Physiol. 19:2035-51 122. Strnwe, G. 1972. Spectral sensitivity of 138. Swihart, S. L. 1974. Acceptance angles the compound eye in butterflies of butterfly ommatidia. J.. lnsect (Heliconius). J. Comp. Physiol. 79: Physiol. 20:1027-36 191-96 139. Swihart, S. L., Baust, J. G. 1965. A 123. Struwe, G. 1972. Spectral sensitivity of technique for the recording of bioelec- single photoreceptors in the compound tric impulses from free-flying insects eye of a tropical butterfly (Heliconius ( Heliconius erato ). Zoologica numata). J. Comp.Physiol. 79:197-201 50:255-58 124. Suomalainen, E., Cook, L. M., Turner, 140. Turner, J. R. 13. 1965. Evolution of J. R. G. 1971. Chromosomenumbers of complex polymorphism and mimicry in heliconiine butterflies from Trinidad, distasteful South Americanbutterflies. West Indies (Lepidoptera, Nym- Proc. 12th lnt. Congr. Entomol, Lon- phalidae). Zoologica NY 56:121-24 don, 1964, p. 267 Annual Reviews www.annualreviews.org/aronline

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141. Turner, J. R. G. 1966. A rare mimetic 155. Turner, J. R. G. 1977..4 bibliography of Heliconiu~ Proc. R. Entomol. Soc. Lon- Heliconius and the related genera. don Ser. B 35:128-32 Stony Brook, NY: SUNY-Stony 142. Turner, J. R. 13. 1967. A little-recog- Brook, Progr. Ecol. Evol., Contrib. 151. nized species of Heliconius butterfly. J. 21 pp. Res. Lepid. 5:97-112 156. Turner, J. R. 13. 1977. Forest refuges 143. Turner, J. R. G. 1967. Some early and ecological islands: disorderly ex- works on heliconiine butterflies and tinction and the adaptive radiation of their biology (Lepidoptera, Nym- muellerian mimics. See Ref. 30, pp. 98- phalidae). J. Linn. Soc. LondonZool. 117 46:255-66 157. Turner, J. R. G. 1978. Butterfly mim- 144. Turner, J. R. G. 1968. Natural selection icry: the genetieal evolution of an adap- for and against a polymorphism which tation. In Evolutionary Biology, ed. M. interacts with sex. Evolution 22:481-95 K. Hecht, W. C. Steere, B. Wallace, 145. Turner, J. R. 13. 1968. Some new 10:163-206. New York: Plenum Heliconius pupae: their taxonomic and 158. Turner, J. R. G., Crane, J. 1962. The evolutionary significance in relation to genetics of some polymorphie forms of mimicry. J. Zool. 155:311-25 the butterflies 146. Turner, J. R. 13. 1970. Mimicry:a study Linnaeus and H. erato Linnaeus. I. Ma- in behaviour, genetics, ecology and bio- jor genes. Zoologica NY 47:141-52 chemistry. Sci. Progr. Oxford 58: 159. Turner, J. R. G., Johnson, M. S., Eanes, 219-35 W. F. 1979. Contrasted modes of evolu- 147. Turner, J. R. 13. 1971. Experiments on tion in the same genome:allozymes and the demographyof tropical butterflies. adaptive change in Heliconiu~ Proc. II. Longevity and home-range behav- Natl. Acad. Sci. USA 76:1924-28 iour in Heliconius erato. Biotropica 160. Turner, J. R. G., Sheppard, P. M. 1975. 3:21-31 Absenceof crossing over in female but- 148. Turner, J. R. 13. 1971. Twothousand terflies ( Heliconius ). Heredity 34: generations of hybridization in a 265-69 Heliconius butterfly. Evolution 25: 161. Vane-Wright, R. I., Aekery, P. R., 471-82 Smiles, R. L. 1975. The distribution, 149. Turner, J. R. G. 1971. Studies of Miil- polymorphism and mimicry of lerian mimicryand its evolution in Bur- Heliconius telesiphe (Doubleday) and net moths and Heliconid butterflies. In the species of Podotricha Michener. Ecological Genetics and Evolution, ed. Trans. R. Entomol. Soc. London 126: E. R. Creed, pp. 224-60. Oxford: Black- 611-36 (1 plate) well 162. Wesley, D. J., Emmel,T. C. 1975. The 150. Turner, J. R. 13. 1972. The genetics of chromosomesof Neotropical butterflies some polymorphic forms of the butter- from Trinidad and Tobago. Biotropica flies Heliconius melpomene(Linnaeus) 7:24-31 and H. erato (Linnaeus). II. The hy- 163. Young, A. M. 1973. Notes on the bridization of subspecies of H. melpo- biology of the butterfly Heliconius mene from and Trinidad. cydno in Costa Rica. WasmannJ. Biol.

by University College London on 06/29/06. For personal use only. Zoologica NY 56:125-57 31:337-50 151. Turner, J. R. 13. 1974. Breeding 164. Young, A. M. 1975. Observations on Heliconius in a temperate climate. J.. the hfe cycle of Lepid. Soc. 28:26-33 zuleika (Hewitson) in Costa Rica. Pan-

Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org 152. Turner, J. R. G. 1975. Communal Pac. Entomol. 51:76-85 roosting in relation to warningcolour in 165. Young, A. M. 1978. Spatial properties two heliconiine butterflies (Nym- of niche separation among Eueides and phalidae). J. Lepid. Soc. 29:221-26 Dryas butterflies in Costa Rica. J NY 153. Turner, J. R. 13. 1976. Muellerian mim- Entomol. Soc. 86:2-19 icry: classical "beanbag"evolution and 166. Young, A. M., Carolan, M. E. 1976. the role of ecological islands in adaptive Daily instability of communalroosting race formation. In Population Genetics in the neotropical butterfly Heliconius and Ecology, ed. S. Karlin, E. Nevo, pp. charitonius. J. Kansas Entomol. Soc. 185-218. New York: Academic 49:346-59 154. Turner, J. R. G. 1976. Adaptive radia- 167. Young, A. M., Thomason, J. H. 1975. tion and convergencein subdivisions of Notes on communal roosting of the butterfly genus Heliconius. ZooL J. Heliconius charitonius in Costa Rica. J. Linn. Soc. 58:297-308 Lepid. Soc. 29:243-55 Annu. Rev. Entomol. 1981.26:427-457. Downloaded from arjournals.annualreviews.org by University College London on 06/29/06. For personal use only.